Mohammedamin, Robbert Sifayed Ali

Infectious Skin Diseases in Children in General Practice
Epidemiology and management
Robbert S.A. Mohammedamin
Infectieuze Huidziekten bij Kinderen in de Huisartspraktijk

Epidemiologie en beleid
Financial support by the Department of General Practice, Erasmus University Medical

Center Rotterdam is gratefully acknowledged.
Cover: Nivel/RIVM, 2006
R.S.A. Mohammedamin, 2007
Erasmus MC, afdeling Huisartsgeneeskunde
ISBN: 978-90-8559-264-8
Infectious Skin Diseases in Children in General Practice

Epidemiology and management
Infectieuze Huidziekten bij Kinderen in de Huisartspraktijk

Epidemiologie en beleid
Proefschrift
ter verkrijging van de graad van doctor aan de

Erasmus Universiteit Rotterdam
op gezag van de rector magnificus
Prof.dr. S.W.J. Lamberts
en volgens besluit van het College voor Promoties
De openbare verdediging zal plaatsvinden op
woensdag 14 februari 2007 om 11.45 uur
door
Robbert Sifayed Ali Mohammedamin

geboren te Paramaribo (Suriname)
Promotiecommissie
Promotoren:
Prof.dr. B.W. Koes
Prof.dr. F.G. Schellevis
Overige leden:
Prof.dr. A.P. Oranje
Prof.dr. B.H. Stricker
Prof.dr. J.F.M. Metsemakers
Copromotor:
Dr. J.C. van der Wouden
Voor mijn ouders
Contents
Chapter 1.
Introduction
Chapter 2.
Increasing incidence of skin disorders in children? A comparison
9
19
between 1987 and 2001

Chapter 3.
Impetigo: incidence and management in Dutch general practice
31
in 1987 and 2001. Results from two national surveys

Chapter 4.
Incidence and management of acne in children and adolescents
43
in Dutch general practice. A comparison between 1987 and 2001

Chapter 5.
Incidence and management of warts in children in Dutch
55
general practice. A comparison between 1987 and 2001

Chapter 6.
Incidence and management of dermatophytosis in children in
69
Dutch general practice. A comparison between 1987 and 2001

Chapter 7.
Association between skin diseases and severe bacterial
83
infections in children: case-control study

Chapter 8.
Summary and general discussion
99
Samenvatting
117
Dankwoord
121
Curriculum Vitae
123
Manuscripts based on studies described in this thesis

1. Mohammedamin RSA, van der Wouden JC, Koning S, van der Linden MW, Schellevis FG, van Suijlekom-Smit LWA, Koes BW. Increasing incidence of skin disorders
in children? A comparison between 1987 and 2001. BMC Dermatology 2006; 6:4.
(Chapter 2)
2. Koning S, Mohammedamin RSA, van der Wouden JC, van Suijlekom-Smit LWA, Schellevis FG, Thomas S. Impetigo: incidence and management in Dutch general practice
in 1987 and 2001. Results from two national surveys. British Journal of Dermatology
2006; 154: 239 243. (Chapter 3)
3. Mohammedamin RSA, van der Wouden JC, Koning S, Schellevis FG, van SuijlekomSmit LWA, Koes BW. Incidence and management of acne in Dutch general practice.
A comparison between 1987 and 2001. [submitted] (Chapter 4)
4. Mohammedamin RSA, van der Wouden JC, Koning S, van der Linden MW, Schellevis
FG, van Suijlekom-Smit LWA, Koes BW. Incidence and management of warts in children in Dutch general practice. A comparison between 1987 and 2001. [submitted]
(Chapter 5)
5. Mohammedamin RSA, van der Wouden JC, Koning S, Schellevis FG, van SuijlekomSmit LWA, Koes BW. Incidence and management of dermatophytosis in children in
Dutch general practice. A comparison between 1987 and 2001. [submitted] (Chapter
6)
6. Mohammedamin RSA, van der Wouden JC, Koning S, Willemsen SP, Bernsen RMD,
Schellevis FG, van Suijlekom-Smit LWA, Koes BW. Association between skin diseases
and severe bacterial infections in children: case-control study. BMC Family Practice
2006; 7: 52. (Chapter 7)
Introduction
Introduction
Introduction
Skin diseases form a substantial part (10-24%) of the total childhood morbidity encountered in general practice [1,2,3,4]. Initial analyses of the second Dutch national survey
of general practice showed that skin diseases are the most common disease in children
and form 23% of the total childhood morbidity presented to the general practitioner
(GP) [5]. Scarce data is available about the epidemiology of skin diseases in children in
general practice and many questions in this field are still unanswered.
Relevance of this study

Measurement of disease epidemiology in general practice can contribute to wider improvements in health and health care services, through better understanding of disease
aetiology, use of health care services and the role of different health care interventions
[6]. Measuring and monitoring the actual incidence, prevalence, and treatment of skin
diseases in children in general practice is important for several reasons.
Firstly, the past decades have been characterized by changes in childrens socio-demographic [7] and health characteristics and by health care changes in the Netherlands;
the proportion of children from ethnic minorities increased considerably from 7 to
13% [7] and the proportion of persons younger than 20 years increased in urban areas
whereas it decreased in rural and suburban areas [8]. The prevalence of overweight and
obesity increased in children [9,10] and the incidence of asthma, atopic eczema and
other allergic disorders increased also [11,12,13]. Furthermore, the number of singlehanded practices decreased and nowadays more general practitioners cooperate with
colleagues in daily practice.
Previous analyses by Otters et al showed that childhood morbidity presented in general
practice changed parallel with changing childhood demographics. Accordingly, the proportion of skin diseases and general or unspecified diagnoses increased considerably
whereas respiratory tract disorders decreased [5]. Consequently, the relative importance
of skin diseases in children in general practice increased.
Secondly, by measuring the incidence of skin diseases over time, trends can be identified.
Consequently, changing incidence of skin diseases may necessitate a shift of priorities
in order to optimize management in general practice and/or direct the future research
agenda. A previous study performed in Dutch general practice reported an increase of
the incidence of common infectious skin diseases (warts, impetigo, dermatophytosis)
[14]. Infectious skin diseases are thus becoming quantitatively more important in general practice and this should have consequences for general practitioners. Possibly more
11
dermatological expertise might be needed and implemented in the vocational training

programmes and continuing medical education programmes for general practitioners.
For instance only two days are devoted to dermatology in the Rotterdam vocational
training scheme for general practitioners in training. Of these two days only one day is
devoted to infectious skin diseases [15]. A previous review of the literature reported that
general practitioners performed in about 60% of the cases the correct dermatological
diagnosis compared to dermatologists (93%) [16].
Furthermore, determinants may be identified that are associated with the changing
incidence of skin diseases. These determinants could be useful tools in order to facilitate diagnosis, to improve the management of skin diseases, and to prevent spread of
contagious skin diseases by providing appropriate advice.
Thirdly, in the nineties the Dutch College of General Practitioners issued clinical guidelines for the diagnosis and treatment of a few skin diseases (bacterial skin infections,
dermatophytosis, acne, atopic eczema), which may have had consequences for the
management policy of the general practitioner [17,18,19,20]. These guidelines apply to
patients of all ages. A previous analysis of data from the second Dutch National Survey
Chapter 1
of general practice showed that Dutch general practitioners treated skin diseases overall
12
according to the guidelines; in case of acne vulgaris and dermatophytosis the management of the GP was consistent in 91% of the cases with the guideline [21]. For atopic
eczema and bacterial skin infections this percentage was 24% and 65% respectively
[21]. We do not have a clear insight to what extent these guidelines are being followed
specifically in children in daily practice. Previous studies showed that only a part of
dermatological patients in a tertiary clinic received evidence-based treatment [22,23].
Abeni et al reported that only 50% of the dermatological patients received treatment
that is based on results of randomized controlled trials [22]. Comparable data about
children in general practice is not available. This emphasizes the importance of research
concerning the treatment of dermatological problems in children.
Fourthly, in the past decades patients attitudes showed a shift away from consulting
the general practitioner for minor ailments which are usually self-limiting and can be
relieved with over-the-counter medications or other self-care strategies [24]. This finding
is supported by Otters et al [5] showing a significant decrease of the overall consultation rate in general practice in the past decades. These changes may lead to an overall
decreasing incidence of skin diseases in general practice or patients may consult their
general practitioner in a later phase of the disease which is important for the general
practitioner regarding the choice of the treatment.
Introduction
Fifthly, skin diseases, especially skin infections, are usually curable, but some may lead
to serious complications such as nephritis, carditis, arthritis and sepsis if the diagnosis
is delayed and/or treatment is inadequate [25,26,27,28,29,30,31,32]. In general practice,
skin infections (bacterial, viral, fungal) contribute 42 65% to the total skin morbidity
in children [1,3,4]. It is important to know whether the general practitioner could play
a role in preventing such complications by diagnosing and treating skin diseases timely
and appropriately.
The role of general practice in childrens health care

The Dutch health care system has been structured in four layers. Collective disease prevention forms the basic echelon. The first echelon consists of primary health care that
includes general practitioners, district nurses, physiotherapists, midwives, pharmacists,
home care and social workers. The second and third echelon consists of specialized
health care and long term care (psychiatric hospitals, nursing homes and convalescent
centers) respectively [33].
Although there is freedom of choice of a general practitioner, in the Netherlands general practices have a fixed list size, and all inhabitants are listed in a general practice.
Usually, the first contact with health care is the contact with the general practitioner,
meaning that general practitioners are gatekeepers for specialized medical care and
virtually all health problems in the population, for which professional help is sought,
are presented primarily in general practice.
In only a fraction of children with complaints and symptoms parents or children themselves decide to seek medical help; in general this phenomenon is called the iceberg of
symptoms [34] indicating that the vast majority of health problems is not presented to
the health care system at all. When a child with health problems consults the general
practitioner he or she will decide to treat or to refer to secondary health care only if the
child is critically ill and needs acute specialized care. For most diagnostic procedures
general practitioners rely on external facilities. If the general practitioner is unsure about
a certain diagnosis he may consult the specialist for an opinion. General practitioners
deal with skin diseases in a similar way [35]. Nowadays teledermatology (high quality
photographs of skin lesions sent by email to the dermatologist) is an emerging option
to get an advice from the dermatologist.
This thesis
Summarizing, measurement of morbidity in Dutch general practice provides an overview of the health of the population as far as presented to health care and also provides
13
insight in health care use. As Dutch general practitioners control referrals to specialized
care, insight is also gained in the demand for secondary care.
In this thesis, after a general overview of all skin related morbidity in children in general
practice, we will focus on the changes in the incidence and management of infectious
skin diseases during the past decades.
Moreover, we aim to identify determinants that are associated with the incidence of
infectious skin diseases in children encountered in general practice in order to provide
tools for improvement of general practice care and prevention of infectious skin diseases and their complications.
More precisely our study questions are:
Have the incidence rates of skin diseases, especially the most frequent infectious
skin diseases (impetigo, warts, dermatophytosis, acne) in children in Dutch general
practice changed between 1987 and 2001 and if so, were these changes related to
socio-demographic characteristics?
How do general practitioners manage infectious skin diseases and are their manageChapter 1
ment policies in accordance with the national guidelines and/or evidence-based
14
knowledge on the effectiveness of different therapies?

Are general practitioners able to prevent complications such as sepsis and/or bacteraemia requiring hospital admission by managing skin diseases, especially skin
infections, timely and appropriately?
To address these questions we used data of two successive nation-wide surveys, the
first and the second Dutch national survey of general practice carried out in 1987 and
2001 [36,37].
In chapter 2 of this thesis, an overview of all skin diseases encountered in general
practice is presented. Incidence rates stratified for several socio-demographic characteristics are presented and results of two points in time (1987 and 2001) are compared.
Skin diseases were divided into two groups: infectious (bacterial, viral, fungal, parasitic)
and non-infectious (eczema, neoplasms, injuries). Chapter 3 describes the epidemiology and management of impetigo in children in general practice. Impetigo is the most
common bacterial skin infection in children. Results from two points in time (1987 and
2001) are compared. In chapter 4 a comparison over time of the incidence rate and
management of acne in children and adolescents is presented. As reported in previous studies acne is a mulifactorial disease in which Propionibacterium acnes plays an
important role and therefore acne is considered a bacterial skin infection. In chapter 5,
warts, the most common (viral) skin disease in children in general practice, is examined
in more detail. Incidence rate and management in general practice are compared as
Introduction
before. Chapter 6 describes the incidence rate and management of fungal skin diseases in children in general practice. The association between skin diseases, especially
skin infections, and severe bacterial infections requiring hospitalization in children is
explored in chapter 7. As reported in previous studies skin diseases are considered to
be an important causal factor in children who are hospitalized due to a severe bacterial
infection. Therefore we hypothesize that these critically ill children suffer more often
from skin diseases, especially skin infections, and initially consult the general practitioner more often for that reason than other children. If our hypothesis is true the general
practitioner may play an important role in reducing the risk of being hospitalized due
to a severe infection by diagnosing and treating skin diseases appropriately. To test this
hypothesis we performed a case-control study. In chapter 8 we discuss the main findings of this thesis and offer suggestions for future directions of research.
15
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17
Increasing incidence of skin

disorders in children?
A comparison between 1987
and 2001
Mohammedamin RSA, van der Wouden JC, Koning S, van der Linden MW, Schellevis FG, van Suijlekom-Smit
LWA, Koes BW. Increasing incidence of skin disorders in children? A comparison between 1987 and 2001. BMC
Dermatology 2006; 6:4.
Abstract
Background
The increasing proportion of skin diseases encountered in general practice represents a
substantial part of the morbidity in children. Only limited information is available about
the frequency of specific skin diseases. We aimed to compare incidence rates of skin
diseases in children in general practice between 1987 and 2001.
Methods
We used data of all children aged 0-17 years derived from two consecutive surveys
performed in Dutch general practice in 1987 and 2001. Both surveys concerned a
longitudinal registration of GP consultations over 12 months. Each disease episode was
coded according to the International Classification of Primary Care. Incidence rates of
separate skin diseases were calculated by dividing all new episodes for each distinct
ICPC code by the average study population at risk. Data were stratified for socio-demographic characteristics.
Chapter 2
Results
20
The incidence rate of all skin diseases combined in general practice decreased between
1987 and 2001. Among infants the incidence rate increased. Girls presented more skin
diseases to the GP. In the southern part of the Netherlands children consulted their GP
more often for skin diseases compared to the northern part. Children of non-western immigrants presented relatively more skin diseases to the GP. In general practice incidence
rates of specific skin diseases such as impetigo, dermatophytosis and atopic dermatitis
increased in 2001, whereas warts, contact dermatitis and skin injuries decreased.
Conclusions
The overall incidence rate of all skin diseases combined in general practice decreased
whereas the incidence rates of bacterial, mycotic and atopic skin diseases increased.
Increasing incidence of skin disorders
Background
In general practice, skin disease accounts for a substantial part of the morbidity in
children and adolescents [1,2,3,4]. Compared to 1987, in 2001 the childhood morbidity
encountered in Dutch general practice has changed; proportionally more skin diseases
were presented to the general practitioner (GP) whereas other most frequent diseases
(e.g. respiratory tract and general diseases) were presented less often. By the same
token the overall consultation rate in general practice decreased by 22% [5,6]. Did the
incidence rate of skin diseases in general practice increase?
However, little information is currently available about the epidemiology of skin diseases encountered in general practice. The few studies which have been performed
show a wide variety in the occurrence of skin diseases presented to GPs [3,4,7]. Against
the background of the changing consultation behaviour in general practice [5] and the
increasing population-based prevalence of some skin diseases (e.g. atopic eczema) [8,9]
it is important to estimate current incidence rates of the different skin diseases affecting
children and adolescents in general practice. Further, primary care epidemiology can
contribute to wider improvements in health and health care services, through better
understanding of disease aetiology, use of health care services and the role of different
health care interventions [10].
The present study relies on two consecutive surveys which were performed in Dutch
general practice in 1987 and 2001. As they included all patient-physician contacts during a one-year study period, selection bias and the influence of seasonal variation are
avoided.
To estimate current incidence rates of skin diseases affecting children and adolescents
and to generate reference material for future studies, we conducted a detailed analysis
of the skin diseases encountered in Dutch general practice between 1987 and 2001.
Our research questions were:
How often did the GP see children aged 0-17 with specific skin diseases; to what
extent did that change between 1987 and 2001?
Was the incidence rate of skin diseases encountered in general practice in 1987 and
2001 related to socio-demographic characteristics?
Methods
We used data from the first and second Dutch national surveys of general practice,
which were performed by the Netherlands Institute for Health Services Research (NIVEL) in 1987 and 2001. In the Netherlands, general practices have a fixed list size, and
21
all non-institutionalised inhabitants are listed in a general practice, and GPs have a
gate-keeping role. Usually, the first contact with health care, in a broad sense, is the
contact with the general practitioner. Each survey included a representative sample of
the Dutch population.
In 1987 practices were randomly sampled from a list of all Dutch practices, per stratum
defined by region and degree of urbanization. Sampling fractions differed between
strata. 161 GPs in 103 practices participated in the first national survey [11]. With respect
to age and gender the participating GPs and practices were representative of Dutch GPs
and practices in 1987. The GPs were divided into four groups, and each group used registration forms to register data (e.g. diagnosis, prescription and referrals) on all contacts
between patient and practice during one of four consecutive 3-month periods. Baseline
characteristics such as age and gender were derived from patient records. Other sociodemographic characteristics such as socio-economic status (SES) and ethnicity were
obtained by a questionnaire and filled out by parents, or by the children themselves
if they were older than 12 years (response rate 91.2%). SES was based on the fathers
occupation, which was categorized into five classes non-manual work high (class I),
Chapter 2
non-manual work middle (class II), non-manual low and farmers (class III), manual
22
work high / middle (class IV) and manual work low (class V). Ethnicity was derived
from the country of birth of either parent. If either parent was born in Turkey, Africa,
Asia (except Japan and Indonesia) and Central or South America, their children were
considered to be children of non-western origin (in accordance with the classification of Statistics Netherlands). All other children were defined as western. The degree
of urbanization was derived from the general practices postal code and categorized
into four classes under 30,000 inhabitants, 30,000-50,000 inhabitants, over 50,000
inhabitants and the three large Dutch cities Amsterdam, Rotterdam and The Hague.
The Netherlands were divided into a Northern, Central and Southern region. Season
was divided into four categories: spring was defined as months April- June, summer as
July- September, autumn as October- December and winter as January- March.
The diagnoses made by the GPs were coded afterwards by clerks using the International Classification of Primary Care (ICPC) [12].
In 2001, 195 GPs in 104 practices registered data about all physician-patient contacts
over 12 months [13]. They registered all health problems presented within a consultation, and coded the diagnosis themselves using the ICPC. Patient demographic characteristics such as age and gender were derived from the GPs computerized patient files.
As in 1987, SES and ethnicity were obtained by a questionnaire (response rate 76%).
Degree of urbanization, region and season were derived as in 1987.
In both surveys each contact with the GP was defined as one consultation. All health
problems presented within one consultation were recorded separately. Both surveys
were episode orientated, meaning that a consultation on a new health problem marked
the beginning of a new episode. If there were multiple consultations in a single episode,
the diagnosis made during the last consultation was regarded as the episode-diagnosis.
In order to decide whether two consultations with the same problem belonged to the
same episode or were different episodes, the latter was arbitrarily decided upon if the
interval between two consultations was at least four weeks (28 days).
There were 20 practices that participated in both surveys. In 2001 eight practices were
excluded from analyses for the following reasons: two practices had software problems;
one practice registered only over a three-month period; five practices showed insufficient quality of the morbidity registration.
Ethical approval
The study was carried out according to Dutch legislation on privacy. The privacy regulation of the study was approved by the Dutch Data Protection Authority. According
to Dutch legislation, obtaining informed consent is not obligatory for observational
studies.
Statistical analysis
This study analyzed data from both surveys for children aged 017 years presenting
with skin diseases, classified by ICPC codes. Incidence rates in general practice were
calculated for all combined skin diseases and for each skin disease separately with a
distinct ICPC code. We calculated the incidence rate by dividing the total number of
new episodes (numerator) by the study population at risk multiplied by the follow-up
time (denominator). In 1987 the denominator was calculated by multiplying the number
of all patients listed in the participating practices by the follow-up time (person years).
In 2001, persons that moved into or out of the participating practices during the registration period were assumed to contribute for half a year to the follow-up time. The
so-called mid-time population was calculated as the mean of all listed patients of all
participating GPs, aged 0-17 years, at the beginning and at the end of the registration
period, irrespective of health care use. Data were stratified for age categories, gender,
urbanization level, region, season, SES and ethnicity.
Further we assessed the changes in incidence rates of all skin diseases between 1987 and
2001. Incidence rates were expressed per 1000 person-years; 95% confidence intervals
(CI) were calculated assuming a Poisson distribution. Skin diseases which contributed
23
less than 0.5 percent to the total skin morbidity were not analyzed in detail and were
combined into one residual group.
Results
Study populations in 1987 and 2001
The study population in 1987 consisted of 86,577 children yielding 21,644 person years.
These children presented a total of 9,271 contacts with skin problems which contributed
to 6,870 episodes; 75.4% of these episodes resulted in a single contact with the GP. In
2001 there were 88,307 children yielding 82,053 person-years. These children presented
a total of 29,637 contacts with skin problems that contributed to 23,586 episodes; 76.6%
of these episodes consisted of only one contact with the GP.
All episodes of skin disease

Table 1 shows the distribution and the change in incidence rates of skin diseases in
general practice between 1987 and 2001, stratified for several background characteristics. Compared to 1987, in 2001 the overall incidence rate of skin diseases combined
Chapter 2
had decreased significantly from 317.4, CI: [309.9 325.0] to 287.5, CI: [283.8 291.2]
24
per 1000 person years. The incidence rate of skin diseases presented to the GP increased among infants (children under one year); in all other age categories except age
category 1-4 years the incidence rates decreased.
In 2001, girls presented significantly more skin diseases to the GP than boys. There was
a similar geographic gradient in both surveys: in the southern part of the Netherlands
children presented more often skin diseases to the GP compared to the northern part.
In 2001, the incidence rate of skin diseases presented to the GP increased in rural areas
whereas it decreased in suburban areas. In the big cities the incidence rate remained
stable. In both surveys the seasonal peak was in spring. In 2001 children with parents
in SES class I, II, IV, V showed a decrease of the incidence rate of skin diseases presented to the GP whereas the incidence rate in class III (non-manual low and farmers)
remained stable compared to 1987. In both surveys the incidence rates of skin diseases
in general practice were higher in lower SES classes.
In 2001 children of non-western immigrants visited the GP more often with skin diseases than children of natives and western immigrants combined.
Table 2 shows the incidence rates of skin diseases in general practice for the distinct
ICPC codes. In 2001 incidence rates are shown for separate age categories and compared
with the crude incidence rate in 1987. In both surveys warts, impetigo, dermatophytosis, contact dermatitis, atopic dermatitis and injuries of the skin were the most frequent
skin diseases, accounting for about 57% of the total skin-related morbidity presented to
the GP. Although, in general practice the incidence rate of warts decreased by 23% in
Table 1: Incidence rates per 1000 person years of all new episodes of all skin diseases combined in general practice in 1987
and 2001
1987
2001
Incidence Rates
95% Confidence
Intervals
Incidence Rates
95% Confidence
Intervals
P-value
< 1 year
352.1
321.0 385.5
460.8
441.0 481.3
<0.001
1- 4 years
328.9
312.2 346.2
320.0
311.8 328.3
0.35
5 9 years
340.3
325.4 355.7
273.7
267.1 280.5
<0.001
10 14 years
276.2
262.8 290.1
235.3
229.1 241.6
<0.001
15 17 years
319.0
302.5 336.3
266.9
258.3 275.7
<0.001
Male
315.9
305.5 326.5
279.2
274.2 284.3
<0.001
Female
319.0
308.3 330.0
296.2
290.8 301.5
<0.002
< 30,000
307.8
295.3 320.6
324.3
318.4 330.4
0.02
30,000 50,000
315.4
303.1 328.1
253.9
246.0 261.9
<0.001
> 50,000
349.9
332.6 367.9
258.1
251.9 264.3
<0.001
Big Cities
289.1
265.5 314.2
285.8
271.7 300.5
0.82
Northern
303.3
281.8 326.0
253.6
244.6 262.8
<0.001
Central
310.2
301.0 319.6
282.4
277.6 287.3
<0.001
Southern
342.7
327.1 358.8
314.6
307.4 321.8
0.001
Winter
305.8
290.4 321.8
279.4
272.2 286.8
0.003
Spring
336.6
322.5 351.1
294.5
287.1 302.1
<0.001
Summer
319.3
302.9 336.4
292.5
285.1 300.0
0.004
Autumn
304.9
291.1 319.2
272.7
265.8 279.8
<0.001
Class I
305.0
289.3 321.2
265.2
258.6 271.9
<0.001
Class II
325.2
304.1 347.4
278.8
270.8 287.0
<0.001
Class III
264.2
232.2 299.4
299.0
284.4 314.0
0.06
Class IV
340.9
322.1 360.6
299.5
283.6 316.1
0.001
Class V
336.4
315.8 358.0
283.2
270.4 296.5
<0.001
Natives & Western

Immigrants
315.7
308.1 323.5
275.1
270.7 279.6
<0.001
Non-Western
Immigrants
346.1
313.6 380.9
295.6
281.6 310.0
0.01
Total
317.4
309.9 325.0
287.5
283.8 291.2
<0.001
Age Categories
Gender
Urbanization
Region
Season
SES
Ethnicity
25
Table 2: Incidence rates per 1000 person years of all new episodes of skin diseases according to ICPC codes in Dutch
general practice in 1987 and 2001
2001
1987
<1
year
ICPC
1-4
5-9
10-14 15-17 0-17
years years years years years
0-17
years
S84
Impetigo
1684
7.1
18.6
29.4
27.7
13.4
7.3
20.5
16.5
S11
Localized skin infections
726
3.1
10.2
9.0
9.1
7.4
9.4
8.8
4.5
S09
Infected finger/toe/paronychia
455
1.9
7.7
7.3
5.3
5.1
3.2
5.5
7.7
S10
Carbuncle/cellulitis
196
0.8
0.9
2.0
2.8
2.0
3.1
2.4
6.1
S76
Erysipelas/erythrasma
153
0.6
2.3
2.4
1.4
1.5
2.3
1.9
3.2
S03
Warts
2816
11.9
0.7
13.7
54.8
38.7
27.4
34.3
44.8
S95
Mollusca contagiosa
777
3.3
2.3
18.1
17.0
1.4
0.3
9.5
10.8
S71
Herpes Simplex skin/lip
148
0.6
1.8
2.6
1.2
1.8
1.8
1.8
2.9
S70
Herpes zoster
134
0.6
0.0
1.6
1.4
2.1
1.5
1.6
2.0
S74
Dermatophytosis
2085
8.8
41.0
24.7
20.3
24.6
29.6
25.4
20.8
S75
Moniliasis/candidiasis
801
3.4 112.9
12.5
1.4
1.0
1.2
9.8
4.9
Parasitic
S12
infestations
Insect bite
577
2.4
9.3
11.8
6.9
4.0
4.7
7.0
6.7
Dermatitis
S88
Contact dermatitis/other eczema 1882
8.0
31.1
24.6
18.9
19.8
28.5
22.9
33.2
S87
Atopic dermatitis
1353
5.7
90.9
26.0
9.5
7.1
6.5
16.5
11.3
S86
Seborrhoeic dermatitis
416
1.8
24.7
3.3
2.4
5.2
5.3
5.1
3.4
S89
Diaper rash
406
1.7
48.5
10.3
0.2
0.0
0.0
4.9
10.5
S90
Pityriasis rosea
124
0.5
0.2
0.5
1.1
2.1
2.8
1.5
1.2
S82
Naevus/mole
479
2.0
1.4
1.3
4.5
7.9
11.9
5.8
3.5
S04
Local swelling/mass
372
1.6
8.2
4.6
3.9
4.0
5.0
4.5
2.0
S79
Other benign neoplasms
203
0.9
1.8
1.0
1.6
3.1
5.1
2.5
3.8
S93
Sebaceous cyst
184
0.8
1.4
1.3
1.4
2.2
5.2
2.2
3.9
Bacterial
infections
Viral
infections
Chapter 2
Fungal
infections
26
Neoplasms
2001, it remained the most frequent skin disease in children in both surveys. In 2001, in
general practice the incidence rate of impetigo, dermatophytosis and atopic dermatitis
increased whereas the incidence rate of the most viral skin infections decreased. Also
contact dermatitis and several types of skin injuries showed a decreased incidence rate
in general practice. Most of the specific skin diseases (e.g. dermatophytosis, moniliasis/
candidiasis, contact dermatitis, atopic dermatitis and diaper rash) showed the highest
incidence rate among infants in general practice.
Discussion
These two large and representative surveys give a comprehensive assessment of the
dermatological morbidity in children encountered in Dutch general practice, and enabled us to estimate current incidence rates for all skin diseases.
Table 2: Incidence rates per 1000 person years of all new episodes of skin diseases according to ICPC codes in Dutch
general practice in 1987 and 2001 (continued)
2001
1987
<1
year
Injuries
1-4
5-9
10-14 15-17 0-17
years years years years years
0-17
years
S18
Laceration/cuts
1668
7.1
7.9
30.8
21.8
15.0
15.1
20.3
23.4
S16
Bruises/contusions
713
3.0
6.6
7.9
7.2
10.0
10.2
8.7
7.8
S17
Abrasion/scratch/blister
440
1.9
2.3
5.8
5.3
4.4
7.1
5.4
6.0
S14
Burns/scalds
255
1.1
5.0
4.9
1.4
2.2
4.4
3.1
3.4
S13
Human / animal bite
169
0.7
1.6
2.2
2.0
2.0
2.1
2.1
2.5
S15
Foreign body in skin
131
0.6
0.5
1.6
2.0
1.5
1.3
1.6
1.9
S19
Other injuries to skin
165
0.7
1.6
2.5
2.4
1.6
1.4
2.0
11.8
S98
Urticaria
673
2.9
6.3
12.0
9.2
5.4
6.2
8.2
7.4
S96
Acne
506
2.1
0.2
0.1
0.3
9.9
19.7
6.2
9.9
S06
Erythema/rash
437
1.9
22.4
7.9
3.7
2.5
3.7
5.3
4.2
S94
Ingrown toenail/other diseases

of nail
430
1.8
0.9
1.5
1.6
9.1
11.0
5.2
4.9
S21
Symptoms/complaints of skin
texture
349
1.5
15.6
5.5
3.3
2.3
3.5
4.3
2.3
S02
Pruritis/skin itching
310
1.3
3.2
4.8
3.7
2.7
4.3
3.8
2.3
S29
Other symptoms/complaints skin 207
0.9
8.4
2.0
1.4
2.2
3.5
2.5
1.5
S99
Other diseases of skin/

subcutaneous tissue
184
0.8
4.1
1.6
1.5
2.3
3.6
2.2
5.8
S22
Symptoms/complaints of nails
126
0.5
1.4
1.6
1.2
1.7
1.6
1.5
1.3
Residuals
852
3.6
Total
23586 100
Others
10.4
16.3
287.5
317.4
ICPC = International Classification of Primary Care

N = number of incident episodes of skin diseases
% = percentage of new episodes of skin diseases with a distinct ICPC
The overall incidence rate of skin diseases presented to the GP decreased by 9.4%,
which is surprising given the decreased overall GP consultation rate by children as
reported elsewhere [5]. According to the decrease of the overall GP consultation rate by
22% we expected a lower incidence rate of skin diseases in 2001 in general practice.
In infants, the incidence rate of skin diseases presented to the GP has increased in
2001, especially of atopic dermatitis and moniliasis/candidiasis (table 2). This increase
is in accordance with previous studies showing an increase of atopic dermatitis in the
general population [8,9].
Girls visited the GP more often concerning skin problems which is in accordance with
previous studies [1,2,14]. Probably this difference is based on aesthetic reasons.
Between 1987 and 2001, the incidence rate of skin diseases in general practice increased
in rural areas and decreased in suburban areas. It seems plausible that this increase
27
could partly be explained by the increased incidence of bacterial skin infections in our
data. It is suggested elsewhere that children in rural areas are more exposed to infectious pathogens due to the larger number of animals and farms [15]. Actually, with the
decreasing consultation rate we would expect also a decrease of the incidence rate of
skin diseases in general practice in urban areas but this did not change between 1987
and 2001. Probably children in urban areas are suffering more from skin diseases. This
is in accordance with the pollution hypothesis meaning that children in urban areas
have a higher chance in developing atopic diseases [15,16]. Crowding in urban areas
could be a potential factor in spreading infectious skin diseases.
According to table 1 there is a regional variation in the incidence rates of skin diseases in general practice. The highest incidence rates of skin diseases encountered in
practices in the south is a striking observation, especially for a small country like the
Netherlands. Of the six most frequent skin diseases impetigo (S84) had a geographical
gradient with a two fold higher incidence rate in the south compared to the north. Also
for non-dermatological conditions we found a significantly higher consultation rate in
the south of the Netherlands in both surveys. Practice characteristics seem not to play
Chapter 2
an important role.
28
In 2001, children of non-western immigrants consulted their GP more often with skin
diseases. The significantly higher consultation rate and the proportional increase of
non-western children from 7.4% to 9.7% in the Dutch childhood population might
explain these differences [5,6]. Probably, non-western children suffer more from skin
diseases; a previous study reported that non-western immigrants in the Netherlands
more often felt unhealthy [13].
We found the highest incidence rate of skin diseases in general practice in the lower
SES classes, which is consistent with previous studies [17,18]. The most striking finding
is that the incidence rate of skin diseases in general practice remained stable in SES
class III (table 1). In all other SES classes the incidence rate have decreased between
1987 and 2001 which is in accordance with the decreased consultation rate in general
practice [5].
Furthermore, from table 2 it becomes clear that the incidence rates of some skin diseases presented to the GP have increased while others have decreased substantially. The
increased incidence rate of infectious (bacterial and fungal) and allergic skin diseases
in our data is compatible with reported trends [5,8,9,14]. The increasing use of day-care
and after-school facilities in the Netherlands might explain the increase of infectious
skin diseases in general practice [15]. There are suggestions that the increasing use of
topical antibiotics resulted in more resistant bacterial strains, which could have resulted
in a rise of the incidence of bacterial skin infections in the population. The striking
decrease in incidence rate of most viral skin infections in our data is in parallel with
the decreased overall GP consultation rate. In 2001, infectious skin diseases represent
a substantial part (45%) of the total skin morbidity presented to the GP which is in accordance with previous studies [3,4]. Skin injuries and allergic skin diseases contributed
about 15% and 18% respectively.
This study had some limitations. There were small differences in the design of the two
national surveys, which might disturb the comparability of data. Some of the differences in occurrence may be explained by the fact that ICPC coding was not performed
equally in both surveys: in 1987 clerks coded diagnoses afterwards, whereas in 2001 the
GPs coded the diagnoses themselves during the consultation. We assume that coding
by clerks more often led to a diagnosis-specific ICPC code. In the present study the
accuracy of diagnoses made by the GPs could be a subject of debate. In our analysis
we assumed that the diagnoses made by the GPs were correct. In 2001 the participating
GPs were trained in coding the diagnoses correctly using ICPC codes. Overall these
trained GPs classified diagnoses correctly in about 81% of the test cases [19].
Conclusions
The overall incidence rate of all skin diseases combined in general practice decreased
whereas the incidence rates of bacterial, mycotic and atopic skin diseases increased.
On these topics more detailed epidemiological data and population-based prevalence
studies are needed.
29
References
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Chapter 2
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Julian CG. Dermatology in general practice. Br J Dermatol 1999; 141: 518520.

Keith Steele. Primary dermatologial care in general practice. J R Coll Gen Pract 1984; 34:
2223.
Tunnessen WW Jr. A survey of skin disorders seen in pediatric general and dermatology
clinics. Pediatric Dermatology 1984; 1: 219222.
Hayden GF. Skin diseases encountered in a pediatric clinic: A one year prospective study.
Am J Dis Child 1985; 139: 3638.
1722.
Statistics Netherlands: Statistisch Jaarboek 2002. Voorburg / Heerlen, CBS 2002.
Krowchuk DP, Bradham DD, Fleischer AB Jr. Dermatologic services provided to children
and adolescents by primary care and other physicians in the United States. Pediatr Dermatol 1994; 11: 199203.
in Swedisch schoolchildren between 1979 and 1991. Clin Exp Allergy 1995; 25: 815819.
385391.
Hannaford PC, Smith BH, Elliot AM. Primary care epidemiology: its scope and purpose.
Family Practice 2006; 23: 17.
van Suijlekom-Smit LWA, Bruijnzeels MA, van der Wouden JC, van der Velden J, Visser
HKA, Dokter HJ. Voor welke gezondheidsproblemen bij kinderen wordt de huisarts geconsulteerd en hoe vaak? [For what health problems in children is the GP consulted, and how
often?]. Ned Tijdschr Geneeskd 1995; 139: 16841689.
Lamberts H, Wood M: ICPC. International Classification of Primary Care. Oxford, Oxford
University Press 1987.
van de Lisdonk EH, van den Bosch WJHM, Lagro-Janssen ALM. Ziekten in de huisartspraktijk. [Diseases in General Practice]. 4th edition. Maarssen, Elsevier 2003.
Karmaus W, Botezan C. Does a higher number of siblings protect against the development
of allergy and asthma? A review. J Epidemiol Community Health 2002; 56: 209217.
Sturgill S, Bernard LA. Atopic dermatitis update. Curr Opin Pediatr 2004; 16: 396401.
Saxena S, Majeed A, Jones M. Socioeconomic differences in childhood consultation rates in
general practice in England and Wales: prospective cohort study. BMJ 1999; 318: 642646.
Saxena S, Eliahoo J, Majeed A. Socioeconomic and ethnic group differences in self reported
health status and use of health services by children and young people in England: cross
sectional study. BMJ 2002; 325: 520525.
Linden van der MW, Westert GP, Bakker de DH, Schellevis FG. Klachten en aandoeningen
in de bevolking en in de huisartspraktijk [Symptoms and diseases in the population and in
general practice]. Utrecht / Bilthoven, NIVEL / RIVM 2004.
Impetigo: incidence and

management in general
practice in 1987 and 2001.
Results from two national
surveys
Koning S, Mohammedamin RSA, van der Wouden JC, van Suijlekom-Smit LWA, Schellevis FG, Thomas S.
Impetigo: incidence and management in general practice in 1987 and 2001. Results from two national
surveys. British Journal of Dermatology 2006; 154: 239 243.
Abstract
Objectives
Impetigo is a common skin infection in children. The epidemiology is relatively unknown, and the choice of treatment is subject for debate. The objective of our study
was to determine the incidence and treatment of impetigo in Dutch general practice,
and assess trends between 1987 and 2001.
Methods
We used data of the first (1987) and second (2001) Dutch national survey of general
practice. All diagnoses, prescriptions and referrals were registered by participating general practitioners (GPs), 161 and 195 respectively.
Results
Incidence The incidence rate of impetigo increased from 16.5 (1987) to 20.5 (2001) per
1000 person years under 18 years old (p< 0.01). In both years, the incidence was significantly higher in summer, in rural areas and in the southern region of the Netherlands,
Chapter 3
compared to winter, urban areas and northern region respectively. Socio-economic
32
status was not associated with the incidence rate.

Treatment From 1987 to 2001, there was a trend towards topical antibiotic treatment
(from 40% to 64%), especially fusidic acid cream and mupirocin cream. Oral antibiotic
treatment (from 29% to 14%), and disinfecting agents (from 11% to 3%) were less often
prescribed.
Conclusions
Incidence We have shown an increased incidence of impetigo in the past decades,
which may be the result of increased tendency to seek help, or increased antibiotic
resistance and virulence of Staphylococcus aureus. Further microbiological research of
the marked regional difference in incidence may contribute to understanding the factors
that determine the spread of impetigo.
Treatment Trends in prescribing for impetigo generally follow evidence-based knowledge on the effectiveness of different therapies, rather than the national practice guideline.
Impetigo: incidence and management
Background
Impetigo or impetigo contagiosa is a contagious superficial skin infection. Staphylococcus aureus is currently the most common causative agent. For parents, a child with
impetigo brings about concern and inconvenience, since children with impetigo are
usually barred from schools and kindergartens. Although the incidence and population
prevalence of impetigo seem to have decreased over the past decades, it is still a common disease, particularly in young children [1,2,3].
Not much is known about the epidemiology. There is a general belief that good hygiene
may prevent the occurrence of impetigo [4], and that social factors such as crowding
may increase the risk of developing of this disease. Regarding the level of the causative
agent, specific characteristics of S. aureus have been identified, which affect the development and course of impetigo [5,6,7].
There is debate about the treatment of impetigo. Are topical antibiotics effective? Should
their use be promoted or discouraged because of rising resistance rates, especially
against fusidic acid? [8,9]. Since 1999, there is a guideline for Dutch general practitioners
(GPs) on bacterial skin infections, issued by the Dutch College of General Practitioners.
[9]. In summary, the advice for impetigo is a basic treatment of disinfection, and additional zinc ointment in case of limited lesions or fusidic acid cream in case of more
extensive lesions.
Against the background of changing social behaviour and changing resistance of the
pathogen it is important to establish the occurrence and treatment of impetigo in daily
practice. We investigated the incidence of impetigo and its management by GPs in the
Netherlands, and tried to identify trends between 1987 and 2001. Our questions were:
How often does the GP see children aged 0-17 with impetigo, and how is the incidence related to sex, age, season, region, urbanization level and social economic
status, and how did that change between 1987 and 2001?
What is the treatment policy of the GP, and how did that change between 1987 and
2001?
Methods
We analyzed data from the first and second Dutch national surveys of general practice,
which were carried out by the Netherlands Institute for Health Services Research in
1987 and 2001, respectively. For this study, data from both surveys for children aged
017 years were analyzed. In the Netherlands, general practices have a fixed list size,
and all non-institutionalised inhabitants are listed in a general practice, and GPs have a
33
gate-keeping role. Both surveys included a representative sample of the Dutch population.
First Dutch National Survey 1987

A non-proportionally stratified sample of 161 GPs was selected randomly to participate
in the survey. The GPs were divided into four groups and each group registered data
about all contacts between patient and practice on registration forms during one of four
consecutive 3-month periods during 1987. The four registration periods covered one
calendar year to correct for seasonal variability of morbidity. Data recorded from each
consultation included patient characteristics (age, gender), diagnosis and prescription
of drugs. Specially trained workers using the International Classification of Primary
Care (ICPC) coded diagnoses made by the general practitioner afterwards. Other demographic patient characteristics were obtained by a questionnaire. Because of an underrepresentation of deprived areas, the population was weighted to the Dutch population
of 1987. For further details about the first Dutch national survey, we refer to the book
by Bruijnzeels [1].
Chapter 3
Second Dutch National Survey 2001
34
The second national survey was carried out in 2001. In short, 195 general practitioners
in 104 practices registered data about all physician-patient contacts during 12 months.
GPs registered all health problems presented within a consultation and coded diagnoses
using the ICPC. Also, all prescriptions made by the GP were registered. Characteristics
of participating practices such as settlement in rural or urban area were obtained by a
mailed questionnaire. Patient characteristics such as age and gender were derived from
the GPs computerized patient files. For further details about the second Dutch national
survey, we refer to the article by Westert [11]. For this analysis, data from nine of the
104 practices were excluded for various reasons: five practices with inadequate registration of patient contacts or drug prescription were excluded after quality control. Four
other practices were excluded because of software problems. When several contacts
had taken place for impetigo, and there had been no cure between the contacts, we
constructed an episode.
Statistical analyses
We defined incidence as number of first contacts for impetigo per 1000 person years.
Differences between incidence rates were tested assuming a Poisson distribution with a
significance level of 0.05 using STATA version 8.2.
Results
In the first National Survey (1987) and the second National Survey (2001), 86,577 and
81,716 children aged 0-17 participated respectively. In these groups, there were 380
(1987) and 1682 (2001) episodes of impetigo. These figures form the basis of the incidence rates.
Incidence
The incidence of impetigo in children under 18 was 16,5 per 1000 person years in 1987.
In 2001, the incidence had risen to 20.5, an increase of 24% (p <0.01). The incidence
by age is represented in figure 1. It shows that especially children aged 6-11 years had
impetigo more often in 2001 compared to 1987. Consequently, the peak age group
for impetigo has widened and shifted to an older age. There was no sex difference in
incidence in 1987 whereas in 2001 boys more often consulted the GP for impetigo.
Table 1 shows the incidence of impetigo, related to urbanization level, region, season
and socio-economic status. Like in 1987, impetigo was more frequent in smaller towns
and villages (< 30,000 inhabitants). This difference was statistically significant compared
to all three other categories of urbanization level. There was a geographic gradient in
both surveys, stronger in 2001 than in 1987. In the south of the Netherlands, the incidence of impetigo was twice as high as in the north. In multivariate analysis, this proved
Figure 1: Incidence of impetigo by age in general practice per 1000 person years
35
Table 1: Incidence rates (1000 person years) of impetigo in 0-17 years olds by urbanization level, region, season, and
socio-economic group
2001
Incidence rates
95% CI interval
Incidence rates
95% CI interval
<30,000 inhabitants
22.0
18.75 25.59
25.8
24.13 27.52
30-50,000 inhabitants
13.7
11.27 16.59
12.0
10.33 13.84
>50,000 inhabitants
14.0
10.69 17.96
14.1
12.65 15.57
Big cities
11.5
7.21 17.41
12.9
10.04 16.33
Northern
15.6
11.07 21.46
13.0
11.05 15.25
Central
15.5
13.53 17.74
19.4
18.19 20.74
Southern
19.2
15.68 23.34
26.4
24.35 28.55
Winter
15.6
12.27 19.56
14.8
13.20 16.61
Spring
10.9
8.53 13.83
12.2
10.72 13.81
Summer
21.5
17.38 26.26
31.2
28.78 33.66
Autumn
18.6
15.31 22.38
23.0
20.97 25.08
1 Non-manual high
17.4
13.79 21.58
19.5
17.72 21.37
Chapter 3
1987
2 Non-manual middle
16.0
11.62 21.47
22.6
20.37 25.01
3 Non manual low & farmers
15.0
8.22 25.23
23.5
19.58 28.02
4 Manual high/middle
22.2
17.63 27.67
22.5
18.34 27.41
36
5 Manual low
21.0
16.09 26.90
20.8
17.41 24.62
Total
16.5
14.83 18.30
20.5
19.55 21.53
Urbanization level
Region
Season
Socio-economic group2
1 Amsterdam, Rotterdam, The Hague

2 according to education of the father
to be independent of urbanization level. The seasonal peak in incidence in the summer

was stronger in 2001 than in 1987. Socio-economic status appeared no significant factor
in both surveys.
Prescriptions
The data are based on the prescriptions in the first contact of an episode, and are presented in table 2. Sixty nine percent of all prescriptions in 1987 were for an antibiotic;
in 2001 this percentage was 78. In 2001, more topical antibiotics, especially fusidic acid
cream and mupirocin cream, and less oral antibiotics were prescribed than in 1987.
Other topical antibiotics were hardly used anymore. The number of prescriptions for
disinfecting agents decreased from 11% to 3%. In a small minority of the consultations
more than one prescription was issued.
Table 2: Prescriptions in the first contact of the impetigo episode

1987
2001
Number
percentage
Number
percentage
Total number of episodes
380
100
1682
100
Oral antibiotic
109
29
242
14
Amoxicillin and other penicillinase susceptible penicillins
82
22
78
Penicillinase resistant penicillins (flucloxacillin,

amoxicillin + clavulanic acid)
15
89
Macrolides
60
Cefalosporins
14
Other
Topical antibiotic
153
40
1078
64
Fusidic acid
64
17
855
51
Mupirocin
210
12
Tetracyclin
54
14
Other
35
10
Antiseptic
40
11
48
Chloorhexidin
12
19
Povidon-iodine
17
29
Other
11
Other topical medication
80
21
68
No prescription
35
240
14
Referrals
In 1987 three (0.8%) and in 2001 fourteen (0.8%) of the children with impetigo were referred to the dermatologist. In 2001, a similar proportion of boys and girls were referred
to the dermatologist, whereas in 1987 all the referred children were girls.
Discussion
Incidence: increase
We observe an increased incidence of impetigo seen in general practice over the past
14 years, which seems to be an upheaval after decades of decreasing incidence [2].
This increase may reflect a rising tendency of medical attention seeking and should not
necessarily imply an increase at the population level. The unsightly aspect of (facial)
impetigo may now be less acceptable to parents than before. Also, there seems to be
more pressure from schools to undergo antibiotic treatment before the child can be
permitted at school again. This may also explain the fact that the increase has mainly
affected the age group 611 years. Possible explanations for an increased incidence
37
at the population level are either a change in human behaviour, such as increased
travelling or, on the other side, increasing virulence of the causative pathogen. Genetic
characteristics of S aureus are changing, and a selection of more virulent strains may
take place [5]. Also, a rise of antibiotic resistance in staphylococci has been reported
[8,9,12,13]. Cure of impetigo may therefore last longer than before and patients may be
contagious for a longer time. Reports of impetigo epidemics that are difficult to control,
caused by multiple resistant staphylococci, are illustrative in this respect [14,15].
Incidence: regional variance

The twofold higher incidence in the south compared to the north is a striking observation, especially for a small country like the Netherlands. Climatic differences within the
country are small and seem to offer no explanation. The level of urbanization and socio-economic scale turned out to be no factor either, shown by multivariate analysis. We
propose that staphylococcal transfer from animal to man may explain the geographical gradient. Zoonoses in staphylococcal pyogenic skin infections have been proven
before [16]. In the Netherlands, there is a concentration of pig farming in the southern
provinces, where approximately ten times as many pigs are bred as in the northern
Chapter 3
provinces [17]. It has been shown recently that pig farmers in France more frequently
38
were nasal carriers of S aureus than matched non-farmers, and that the S aureus were
more frequently macrolide resistant [18]. The same explanation may account for the
twofold higher incidence of impetigo in rural areas versus other urbanization levels.
Research comparing genetic staphylococcal characteristics of specimens derived from
different regions would be needed to test these hypotheses. The rise in incidence of
impetigo does not seem to continue southwards, as data from Belgian GPs suggest that
the incidence in Belgian general practice is lower than in the Netherlands. (Personal
communication, Dr Stefaan Bartholomeeusen) The higher incidence of impetigo in the
summer is not new and is consistent with many other reports [2,19,20].
Treatment
There is a trend towards prescribing of topical antibiotics for impetigo, at the expense
of oral antibiotics. The trebled increase of fusidic acid cream prescriptions from 1987 to
2001 may be influenced by the publication of the guideline on bacterial skin infections
by the Dutch College of General Practitioners in 1999 [10]. In this guideline, fusidic
acid is the first choice antibiotic treatment. Contrarily, the number of prescriptions of
mupirocin has also increased. Mupirocin cream, not available in 1987 yet, has proven
efficacy in the treatment of impetigo [21], but was not recommended in the 1999 guideline, considering that mupirocin should be reserved for treatment of nasal carriage of S
aureus. Many GPs did not follow the guideline in this respect. Furthermore, the guideline recommends disinfecting therapy with chlorhexidine or povidon-iodine as a basic
treatment. This advice was even less often complied with in 2001 than in 1987. Possibly,
disinfectants have been advised in some cases and were not registered because they
are over-the-counter-medicines. However, a great proportion of GPs apparently has no
faith in the value of disinfecting treatments. The lack of evidence for the effectiveness
of disinfectants may play a role [21]. In the group of oral antibiotics, a remarkable one
third of all prescriptions are still penicillinase susceptible penicillins such as penicillin,
amoxicillin and feneticillin, which are not indicated for the treatment of impetigo.
Referrals
In both surveys less than 1% of the children suffering from impetigo were referred
to the dermatologist indicating that impetigo is a typical disease seen and treated by
general practitioners. Although in 2001 boys more often consulted the GP for impetigo
the referral rate between boys and girls are equal.
Limitations of this study

There are small differences in the design of the two national surveys, which might
hinder the comparability of data. For example, in the first national survey, trained investigators coded diagnoses afterwards, whereas in the second national survey, the GPs
coded the diagnoses themselves during the consultation. Furthermore, the participating
GPs in the two national surveys may not be fully representative for the average GP in
the Netherlands. This and the fact that their actions were recorded might distort our
results.
Conclusions
We have shown an increased incidence of impetigo in the past decades, and marked
regional differences in incidence. Further (microbiological) research of this observation
may contribute to understanding the factors that determine the spread of impetigo. Secondly, we found a variety in the treatment of impetigo by GPs, which was incompatible
with the national guideline.
39
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40
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van de Lisdonk EH, van den Bosch WJHM, Lagro-Janssen ALM. Ziekten in de huisartspraktijk. [Diseases in General Practice]. 4th edition. Maarssen: Elsevier Gezondheidszorg, 2003.
Massa A, Alves R, Amado J, Matos E, Sanches M, Selores M et al. Prevalence of cutaneous lesions in Freixo de Espada a Cinta [Article in Portuguese]. Acta Med Port 2000; 13:
247254.
Luby S, Agboatwalla M, Schnell BM, Hoekstra RM, Rahbar MH, Keswick BH. The effect of
antibacterial soap on impetigo incidence, Karachi, Pakistan. Am J Trop Med Hyg 2002; 67:
430435.
Koning S, van Belkum A, Snijders S, van Leeuwen W, Verbrugh H, Nouwen J. et al. Severity
of nonbullous staphylococcus aureus impetigo in children is associated with strains harboring genetic markers for exfoliative toxin B, Panton-Valentine leukocidin, and the multidrug
resistance plasmid pSK41. J Clin Microbiol 2003; 41: 30173021.
Capoluongo E, Giglio A, Belardi M, Leonetti F, Frasca A, Giannetti A, et al. Association
between lesional or non lesional S. aureus strains from patients with impetigo and exfoliative toxin production. No association with SmaI PFGE patterns. New Microbiol 2000; 23:
2127.
Afset JE, Maeland JA. Susceptibility of skin and soft-tissue isolates of Staphylococcus aureus
and Streptococcus pyogenes to topical antibiotics: indications of clonal spread of fusidic
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Brown EM, Wise R. Fusidic acid cream for impetigo. Fusidic acid should be used with
restraint. BMJ 2002; 324: 1394.
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associated with impetigo bullosa is spreading in Norway. J Antimicr Chemother 2002; 50:
873876.
Laverdiere M, Weiss K, Rivest R, Delorme J. Trends in antibiotic resistance of staphylococci
over an eight-year period: differences in the emergence of resistance between coagulase
positive and coagulase-negative staphylococci. Microb Drug Resist 1998; 4: 119122.
Rortveit S, Rortveit G. An epidemic of bullous impetigo in the municipality of Austevoll in
the year 2002, Tidsskr Nor Laegeforen 2003; 123: 25572560.
Owen SE, Cheesbrough JS. Fusidic acid cream for impetigo. Findings cannot be extrapolated. BMJ 2002; 324: 203-206.
Rao PN, Naidu AS, Rao PR, Rajyalakshmi K. Prevalence of staphylococcal zoonosis in
pyogenic skin infections. Zentralbl Bakteriol Mikrobiol Hyg 1987; 265: 218226.
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41
Incidence and management

of acne in children and
adolescents in Dutch general
practice. A comparison
Mohammedamin RSA, van der Wouden JC, Koning S, Schellevis FG, van Suijlekom-Smit LWA, Koes BW.
Incidence and management of acne in children and adolescents in Dutch general practice. A comparison
between 1987 and 2001 [submitted]
Abstract
Objective
Acne is a multifactorial disease and the most common skin disease among adolescents.
The epidemiology is relatively unknown and there is debate about changes in the
prevalence of acne in the population. We determined the incidence rate and management of acne in children and adolescents in general practice in 1987 and 2001.
Methods
We used data of all participants 10-24 years of age of the first (1987) and second (2001)
Dutch national survey. All diagnoses, prescriptions and referrals were registered by participating general practitioners (GPs), 161 and 195 respectively. Both surveys concerned
a longitudinal registration of GP consultations over 12 months.
Results
The incidence rate of acne in general practice decreased from 20.0 (1987) to 11.8 (2001)
per 1000 person years. Girls, adolescents aged 15-19 years and non-western immigrants
Chapter 4
consulted the general practitioner more often with acne. Overall, general practitioners
44
treated acne according to the clinical guideline.
Conclusions
In general practice the incidence rate of acne in children and adolescents decreased
substantially which could be a consequence of changing consultation behaviour for
acne or a decreasing prevalence in the population. More studies on the population
prevalence of acne and help seeking behaviour in general practice are needed.
Incidence and management of acne
Background
Acne is the most common skin disease among adolescents, with estimates indicating
that 80 to 95% of adolescents will suffer from acne [1,2,3,4]. The prevalence among
school children is high ranging from 27.7% in 10-12 year olds to 93.3% in 16-18 year
olds [4]. Acne is a multifactorial disease in which the Propionibacterium acnes, the rise
in circulating androgen levels during puberty, and emotional stress and diet play an
important role in the onset [1].
There is debate about changes in the prevalence of acne in the population. One study
has reported a decrease of the prevalence of acne over the past decades [5] whereas
some other studies reported that dermatologists are increasingly seeing adolescents
with acne [6,7]. Available data can not indicate whether this is a true increase against
the background of the increasing antibiotic resistence of P. acnes [8,9], or whether
adolescents are simply more aware that dermatologists can do more to relieve acne and
therefore present it more frequently [6]. It is unclear whether these changes can also be
observed in general practice.
Although acne is not associated with severe morbidity, mortality or physical disability,
it can have considerable psychological and social consequences [10,11,12]. Appropriate
management of acne is therefore an important component of routine healthcare for
general practitioners. Given the multifactorial etiology of acne, several potential targets for therapeutic intervention exist [1,2,3,13]. In 1991, the Dutch College of General
Practitioners issued a clinical guideline for the diagnosis and treatment of acne [14]. In
summary, therapy should be appropriately tailored to the severity of acne, with reliance
on topical therapies (such as benzoylperoxide or salicylic acid, tretinoin or a topical
antibiotic) for milder cases and judicious use of systemic antibiotics for inflammatory
acne. Systemic retinoid should be used especially for severe acne. In females who
prefer oral contraception, hormonal treatment is the first therapeutic option, provided
there is no contraindication.
In the present study we compared the results of two consecutive surveys in general
practice performed in 1987 and 2001 respectively and we aimed to know if the introduction of the clinical guideline for diagnosis and treatment of acne has influenced the
management policy (prescriptions, referrals) of GPs. Against the background of the
debate about the changing prevalence of acne in the population and its impact on those
who were affected, it is important to establish the incidence of acne in daily practice.
Knowledge about the contributing factors to the changing incidence might improve
45
the care for patients with acne in general practice and its prevention. Our research
questions were:
What was the incidence rate of acne in children and adolescents aged 10-24 in
general practice and did this change between 1987 and 2001?
Was the incidence rate of acne in general practice related to socio-demographic
characteristics?
How did the GP manage acne (prescription, referral) and did this change between
1987 and 2001?
Methods
We used data from the first and second Dutch national surveys of general practice, which
were performed by the Netherlands Institute for Health Services Research (NIVEL) in
1987 and 2001. Each survey included a representative sample of the Dutch population.
In the Netherlands, general practices have a fixed list size, and all inhabitants are listed
in a general practice, and GPs have a gate-keeping role, meaning that, for example in
the case of acne a dermatologist can only be consulted after referral by a GP. Usually,
Chapter 4
the first contact with health care, in a broad sense, is the contact with the general
46
practitioner.
In 1987 a non-proportionally stratified sample of 161 GPs in 103 practices was selected
randomly to participate in the first national survey [15]. With respect to age and gender
the participating GPs and practices were representative of Dutch GPs and practices in
1987. The GPs were divided into four groups, and each group used registration forms to
register data (e.g. diagnosis, prescription and referrals) on all contacts between patient
and practice during one of four consecutive 3-month periods. Baseline characteristics
such as age and gender were derived from patient records. Other socio-demographic
characteristics such as socio-economic status (SES) and ethnic origin were obtained by
a questionnaire and filled out by parents, or by the children themselves if they were
older than 12 years (response rate 91.2%). SES was based on the fathers occupation,
which was categorized into five classes non-manual work high (class I), non-manual
work middle (class II), non-manual low and farmers (class III), manual work high /
middle (class IV) and manual work low (class V). Ethnic origin was derived from the
country of birth of either parent. If either parent was born in Turkey, Africa, Asia (except
Japan and Indonesia) and Central or South America, their children were considered to
be children of non-western origin (in accordance with the classification of Statistics
Netherlands). All other children were defined as western. The degree of urbanization
was derived from the general practices postal code and categorized into four classes
under 30,000 inhabitants, 30,000-50,000 inhabitants, over 50,000 inhabitants and
the three large Dutch cities Amsterdam, Rotterdam and The Hague. The Netherlands
were divided into a Northern, Central and Southern region. Season was divided into
four categories: spring was defined as months April-June, summer as July-September,
autumn as October-December and winter as January-March.
In 2001, data about all physician-patient contacts over 12 months were derived from
the electronic medical records of all listed patients in 104 practices (195 GPs) [17]. They
registered all health problems presented within a consultation, and coded the diagnosis
themselves using the ICPC. Patient demographic characteristics such as age and gender
were derived from the GPs computerized patient files. As in 1987, SES and ethnicity
were obtained by a questionnaire (response rate 76%). Degree of urbanization, region
and season were derived as in 1987.
the beginning of a new episode. If there were multiple consultations in a single episode,
the diagnosis made during the last consultation was regarded as the episode-diagnosis.
In 2001 we excluded nine practices from the analyses, mainly because of technical
problems with registration.
Ethical approval
studies.
Data-analysis
This study analyzed data from both surveys of children and adolescents aged 10-24
years presenting with acne which was coded as S96 (ICPC). Because of an underrepresentation of deprived areas, the 1987 survey population was weighted to the Dutch
population of 1987. Incidence rate of acne were calculated by dividing the weighted
number of new episodes (numerator) by the study population at risk (denominator).
In 2001 we calculated the incidence rate of acne by dividing the total number of new
episodes (numerator) by the average study population at risk, the mid-time population
(denominator). The mid-time population was calculated as the mean of all listed pa-
47
tients of all participating GPs, aged 10-24 years, at the beginning and at the end of the
registration period. Data were stratified by age categories, gender, urbanization level,
region, season, SES and ethnic origin. Incidence rates were expressed per 1000 personyears; 95% confidence intervals were calculated assuming a Poisson distribution. In this
study we only included the first new episodes of acne.
Different groups of prescriptions at the first contact of each new episode were expressed as a proportion of the number of all new episodes. Referrals were expressed as
a percentage of all new episodes.
Results
The study population in 1987 consisted of 78,470 children and adolescents 10-24 years
of age yielding 19,618 person years. These children and adolescents had 392 episodes
of acne during the one-year registration period. In 2001 the participating children and
adolescents contributed 69,554 person-years (mid-time) to the follow-up. These chilChapter 4
dren had 818 episodes of acne during the one-year registration period.
48
Incidence rate
Table 1 shows the distribution of incidence rates of acne in 1987 and 2001 in general
practice stratified for several background characteristics. Compared to 1987, in 2001
the total incidence rate of acne decreased by 41%. Except SES class I and class III the
incidence rate decreased in all subgroups (table 1).
In both surveys we found the highest incidence rate in the age category 15-19 years.
In 2001, girls presented significantly more acne than boys to the GP. In 1987 we found
the lowest incidence rate in the northern part of the Netherlands, whereas in 2001 the
incidence rate was equal over all regions. In 1987, the incidence rate of acne was the
lowest in rural areas (< 30,000 inhabitants) compared to suburban and urban areas,
whereas in 2001 the incidence rate was equally distributed over all urbanization levels.
In 1987 we observed the lowest incidence rate in autumn and spring and the highest in
summer and winter, whereas in 2001 we observed the lowest incidence rate in spring
and summer and the highest in autumn and winter. In 1987 we found the lowest incidence in SES class III and the highest in SES class V, whereas in 2001 the incidence rate
was equally distributed over all classes. Compared to 1987, in 2001 the incidence rate
of acne decreased significantly in class II, IV and V.
In both surveys non-western children and adolescents visited the GP more often with
acne than western children and adolescents.
Table 1: Incidence rates per 1000 person years of all new episodes of acne in general practice in 1987 and 2001
2001
1987
Incidence
rates
95% Confidence
intervals
Incidence
rates
95% Confidence
intervals
P-value
10 14 years
12.5
11.0 14.1
9.7
8.4 11.0
Age Categories
0.007
15 19 years
33.3
31.1 35.5
16.8
15.1 18.6
< 0.001
2024 years
13.3
12.0 14.7
9.0
7.8 10.3
< 0.001
Total
20.0
19.0 21.0
11.8
11.0 12.6
< 0.001
Male
19.9
18.5 21.3
9.1
8.2 10.2
< 0.001
Female
20.1
18.7 21.5
14.2
13.0 15.5
< 0.001
< 30,000
14.7
13.3 16.1
10.9
9.7 12.2
< 0.001
30,000 50,000
23.2
21.6 25.0
11.3
9.5 13.3
< 0.001
> 50,000
20.4
18.0 23.0
12.3
10.9 13.7
< 0.001
Big Cities1
26.1
20.7 32.4
14.7
11.2 18.8
Northern
16.4
14.7 18.2
10.5
8.7 12.6
< 0.001
Central
20.5
18.9 22.3
11.8
10.7 12.9
< 0.001
Southern
20.2
18.6 21.9
12.1
10.6 13.7
< 0.001
Winter
21.1
19.2 23.1
13.8
12.1 15.7
< 0.001
Spring
17.5
15.6 19.5
10.4
8.9 12.0
< 0.001
Summer
24.4
22.3 26.6
9.2
7.8 10.7
< 0.001
Autumn
17.0
15.1 19.0
13.4
11.7 15.2
0.007
Class I
16.5
13.2 20.5
10.8
5.8 18.5
0.1
Class II
18.4
15.6 21.6
6.1
3.4 10.1
< 0.001
Class III
15.4
13.5 17.3
10.5
6.2 16.6
0.069
Class IV
17.3
15.1 19.8
9.1
5.0 15.3
0.002
Class V
25.2
22.4 28.3
7.8
5.0 11.5
< 0.001
Natives & Western

Immigrants
18.2
17.2 19.4
10.8
9.9 11.9
< 0.001
Non-Western Immigrants
33.8
26.3 42.7
22.1
17.3 27.9
Gender
Urbanization
0.001
Region
Season
SES2
Ethnic origin
0.02
1 = Amsterdam, Rotterdam, The Hague

2 = according to fathers occupation
Prescriptions
In table 2 we present the prescriptions in the first contact of an episode. Between 1987
and 2001 the percentage of prescriptions for systemic antibiotics decreased from 14.6
to 8.7; boys received considerably more frequently antibiotics. Compared to 1987, in
49
Table 2: Prescriptions in first contact of acne episode

1987
Chapter 4
50
2001
number(%)
number(%)
321(100)
818(100)2
boys
girls
boys
girls
146(100)
175(100)
321(100)
497(100)
Oral antibiotic
30(20.5)
17(9.7)
55(17.1)
16(3.2)
Tetracyclines (tetracycline, minocycline,

doxycycline)
28(19.2)
15(8.6)
48(15.0)
15(3.0)
Macrolides (erythromycin, clindamycin)
0(0.0)
1(0.6)
5(1.6)
1(0.2)
Other
2(1.4)
1(0.6)
2(0.6)
0(0)
Other oral drug
1(0.7)
10(5.7)
9(2.8)
106(21.3)
Cyproterone and estrogen
0(0)
7(4.0)
0(0)
102(20.5)
Other
1(0.7)
3(1.7)
9(2.8)
4(0.8)
Anti-acne dermatologicals
102(69.9)
123(70.3)
141(43.9)
315(63.4)
Benzoyl Peroxide
69(47.3)
88(50.3)
92(28.7)
127(25.6)
Clindamycin
13(8.9)
16(9.1)
47(14.6)
74(14.9)
Erythromycin
6(4.1)
5(2.9)
73(22.7)
101(20.3)
Tretinoin
6(4.1)
8(4.6)
23(7.2)
12(2.4)
Other
8(5.5)
6(3.4)
6(1.9)
2(0.4)
Topical antibiotic
1(0.7)
2(1.1)
8(2.5)
13(2.6)
Other dermatologicals
4(2.7)
7(4.0)
10(3.1)
18(3.6)
Unknown
26(17.8)
27(15.4)
14(4.4)
21(4.2)
No prescription in 1st contact
16(11.0)
18(10.3)
48(15.0)
95(19.1)
1 = unweighted number of new episodes

2 = number of new episodes in the mid-time population
2001 much more systemic hormonal treatments were prescribed in girls. In both surveys
the majority of acne were treated by anti-acne dermatologicals; in 1987 the GPs mostly
prescribed benzoyl peroxide whereas in 2001 benzoyl peroxide, topical erythromycin
and clindamycin were the most prescribed drugs. In 1987, in 10.6% of the episodes the
GPs did not prescribe any treatment at the first contact whereas in 2001 this percentage
was 17.5%.
Referrals
Forty-eight (12.2%) and 104 (12.7%) of the patients with acne were referred to a dermatologist in 1987 and 2001 respectively. In 1987 the boys to girls ratio of referred children
was 1:1, whereas in 2001 this was 3:2. In 1987 we found the highest referral rate in the
age group 20 24 years whereas in 2001 this was in the age group 15 19 years.
Discussion
Incidence and sociodemographics
We observed a decrease of 41% of the incidence rate of acne encountered in general
practice over the past 14 years which is consistent with a previous study performed
in the Netherlands [18]. As reported elsewhere the overall consultation rate in Dutch
general practice (second Dutch national survey) decreased by 22% in children (0-17
years) over the past 14 years [19] which could partly explain our finding. Probably our
finding is a consequence of a decreased prevalence in the population as reported by
Stathakis et al [5].
Currently, little information is available about children and adolescents that use selfcare strategies and do not seek medical help for their acne. Cardol et al reported that
in 2001 patients attitudes showed a shift away from consulting their GP for minor
ailments which are self-limiting and could be relieved with over-the-counter medication
or other self-care strategies [20]. Nowadays more over-the-counter medication for acne
is available and it is quite conceivable that adolescents apply more self-care strategies
and consequently seek less medical help, which could fit in our finding assuming that
acne is a minor ailment. This should have consequences for the treatment policy of the
GPs, because the GPs will see the more severe cases in which self-care strategies have
failed.
Girls and adolescents aged 15-19 years visited the GP more often concerning acne than
boys and persons from other age groups respectively, which is in accordance with
previous studies [18,21]. However, the prevalence of acne in the population in this age
group was found to be higher in boys [4,22,23]. Probably girls are more sensitive for the
esthetic aspects of the disease. A previous study reported that girls suffering from acne
had higher levels of emotional and behavioural difficulties [12].
In 1987 we found a striking regional variation in the incidence rate of acne, which
is especially noteworthy for a small country like the Netherlands. Compared to the
northern part, we found higher incidence rates of acne in the central and southern part
of the Netherlands. In 2001 this variation had decreased. We also observed the lowest
incidence rate of acne in general practice in rural areas (< 30,000) compared to suburban and urban areas. Epidemiological data on acne in general practice are scarce. This
regional variation and the differences in urbanization levels have never been reported
earlier.
51
The seasonal variability as occurred in 2001 is in accordance with previous studies [5,18]
showing an exacerbation in the colder months and an improvement in the warmer
months. However, the seasonal variability as occurred in 1987 is different from 2001. In
1987 we strikingly observed the highest incidence rate of acne in summer.
In both surveys children non-western children and adolescents consulted their GP
more often with acne. The significantly higher consultation rate in non-western children
might explain this difference [19]. This finding is supported by another previous study
that reported that elderly, less educated, and non-western inhabitants in the Netherlands are lagging behind the changing trend, and continuing to consult GPs for minor
ailments [20]. Possibly, children of non-western immigrants suffer more from acne. A
previous study reported that non-western immigrants in the Netherlands more often felt
unhealthy [17].
In 1987 we found the higher incidence rates of acne in general practice in the lower SES
classes, which is consistent with a previous study [18]. However, in 2001 the incidence
rate was similar in all classes, but strikingly the incidence rate decreased considerably
Chapter 4
in the lower SES classes.
52
Prescriptions
Between 1987 and 2001 the prescription of oral hormonal treatments in girls increased
from 4.0% to 20.5%. In 2001 the GPs prescribed less oral antibiotics. These changes
in treatment strategies may have been influenced by the introduction of the clinical
guideline for the diagnosis and treatment of acne by the Dutch College of General
Practitioners in 1991 [14].
In both surveys the majority of acne cases were treated with topical anti-acne dermatologicals which is also consistent with the clinical guideline.
In both surveys boys received much more oral antibiotics than girls which is in agreement with a previous study performed in general practice in north-east England [21]. As
reported elsewhere boys are more frequently affected and had more severe acne than
girls especially in the puberty, which might contribute to this issue [4,6]. In adolescence
girls start with oral hormonal contraceptives which might be another explanation that
boys received more oral antibiotics.
Referrals
The boys to girls ratio of referred patients concerning acne strikingly changed from 1:1
(1987) to 3:2 (2001). As suggested earlier, girls may be more sensitive for the esthetic
reasons of the disease and therefore consulted the GP more often than boys in 2001.
However, a higher proportion of boys were referred to the dermatologist indicating

that boys, especially during puberty, more often suffer from moderate to severe acne
as reported in previous studies [1,4,22]. This might be a consequence of the rise in
circulating androgen levels during puberty in boys [1].
Strenghts and limitations of the study

These two large and representative surveys give a comprehensive assessment of the
morbidity in children and adolescents in general practice, and enabled us to accurately
estimate epidemiological data on acne and a comparison between two points in time.
There were small differences in the design of the two national surveys, which might
disturb the comparability of data. ICPC coding was not performed identically in both
surveys: in 1987 clerks coded diagnoses afterwards, whereas in 2001 the GPs coded
the diagnoses themselves during the consultation. We assume that coding by clerks
more often led to a specific diagnostic ICPC code. In our analysis we assumed that the
diagnoses were coded correctly. In 2001, the participating GPs were trained in coding
the diagnoses using ICPC codes. These trained GPs classified diagnoses correctly in
about 81% of the test cases [24].
Conclusions
In general practice the incidence rate of acne in children and adolescents decreased
substantially which could be a consequence of changing consultation behaviour for
acne or a decreasing prevalence in the population. More studies on the population
prevalence of acne and help seeking behaviour in general practice are needed.
The participating GPs treated acne according to the clinical guideline for general practice.
53
References

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4.
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6.
7.
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10.
11.
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Chapter 4
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Smolinski KN, Yan AC. Acne update: 2004. Curr Opin Ped 2004; 16: 385391.
James WD. Acne. N Engl J Med 2005; 352: 14631472.
Krowchuk DP. Treating acne: a practical guide. Med Clin North Am 2000; 84: 811828.
Kilkenny M, Merlin K, Plunkett A, Marks R. The prevalence of common skin conditions in
Australian school students: 3. Acne vulgaris. Br. J Dermatol 1998; 139: 840845.
Stathakis V, Kilkenny M, Marks R. Descriptive epidemiology of acne vulgaris in the community. Australas J Dermatol 1997; 38: 115123.
Cunliffe WJ. Management of adult acne and acne variants. J Cut Med Surg 1998; 2: S3-7
S3-13.
Goulden V, Clark SM, Cunliffe WJ. Post-adolescent acne: a review of clinical features. Br J
Dermatol 1997; 137: 478479.
Eady EA, Jones CE, Gardner KJ, Taylor JP, Cove JH, Cunliffe WJ. Tetracycline-resistant
propionibacteria from acne patients are cross-resistant to doxycycline, but sensitive to
minocycline. Br J Dermatol 1993; 128: 556560.
Eady EA, Jones CE, Tipper JL, Cove JH, Cunliffe WJ, Layton AM. Antibiotic resistant propionibacteria in acne: need for policies to modify antibiotic usage. BMJ 1993; 306: 555556.
Khan MZ, Naeem A, Mufti KA. Prevalence of mental health problems in acne patients. J
Ayub Med Coll Abbottabad 2001; 13: 78.
Barankin B, Dekoven J. Psychosocial effect of common skin diseases. Can Fam Physician
2002; 48: 712716.
Smithard A, Glazebrook C, Williams HC. Acne prevalence, knowledge about acne and psychological morbidity in mid-adolescence: a community-based study. Br J Dermatol 2001;
145: 274279.
NHG-standaard. [Acne Vulgaris. Guideline of the Dutch College of General Practitioners.].
Huisarts Wet 1991; 34: 183188.
Bensing JM, Foets M, van der Velden J, van der Zee J. De nationale studie van ziekten
1991; 34: 5161.
Lamberts H, Wood M. ICPC: International Classification of Primary Care. Oxford: Oxford
University Press, 1987.
1722.
Cardol M, Schellevis FG, Spreeuwenberg P, Lisdonk van de EH. Changes in patients attitudes towards the management of minor ailments. BJGP 2005; 55: 516521.
Purdy S, Langston J, Tait L. Presentation and management of acne in primary care: a retrospective cohort study. Br J Gen Pract 2003; 53: 525529.
Marks R. The public health approach to the burden of common skin diseases in the community. J Dermatol 2001; 28: 602605.
Larsson P, Lidn S. Prevalence of skin diseases among adolescents 12-16 years of age. Acta
Dermatovener (Stockholm) 1980; 60: 415423.
van der Linden MW, Westert GP, de Bakker DH, Schellevis FG. Klachten en aandoeningen
in de bevolking en in de huisartspraktijk. [Symptoms and diseases in the population and in
general practice]. Utrecht / Bilthoven: NIVEL / RIVM, 2004.
Incidence and management

of warts in children in Dutch
general practice. A comparison
Mohammedamin RSA, van der Wouden JC, Koning S, van der Linden MW, Schellevis FG, van Suijlekom-Smit
LWA, Koes BW. Incidence and management of warts in children in Dutch general practice. A comparison
between 1987 and 2001 [submitted]
Abstract
Background
Warts appear commonly in children. The epidemiology is relatively unknown, and
no single treatment has been defined as most effective. We assessed the self-reported
prevalence of warts in children (0-17 years) and which proportion of these children
sought medical help. Further we determined the incidence rate and management of
warts in children in general practice in 1987 and 2001.
Methods
We used data of all children 0-17 years of age of the first (1987) and second (2001)
Dutch national survey. All diagnoses, prescriptions and referrals were registered by
participating general practitioners (GPs), 161 and 195 respectively. To assess the prevalence of warts and medical helpseeking we used additional health interview data of the
second Dutch national survey. Both surveys concerned a longitudinal registration of GP
consultations over 12 months.
Chapter 5
Results
56
The self-reported prevalence of warts in children is 6.2%, and 23.3% of these children
consulted the general practitioner for warts. The incidence rate of warts in general practice decreased from 44.5 (1987) to 32.1 (2001) per 1000 person years. Girls, especially in
puberty, and natives consulted the general practitioner more often with warts. General
practitioners treated the majority of warts by applying cryotherapy with salicylic acid
on the second place.
Conclusions
The incidence rate of warts in general practice has decreased, probably due to changing
consultation behaviour. The self-reported prevalence has hardly changed over time.
General practitioners do not follow evidence-based knowledge on the effectiveness of
different treatments.
Incidence and management of warts
Background
Cutaneous warts are discrete benign epithelial proliferations caused by the human papillomavirus [1] that mostly affects hands and feet [2]. Warts can be painful depending on
their location (plantar and near the nails), and may cause embarrassment and a negative
appraisal by others [1,3,4,5]. In general practice warts are one of the four most frequent
diseases and the most common skin disease in children [6].
Currently, limited information about the epidemiology of warts in children in the population is available. The prevalence among schoolchildren varies from 2-22% [7,8,9,10].
Region, social class, family size and ethnic origin are related to the incidence of warts [9].
Some studies have suggested that wart frequency in the population has been increasing
during the past decades [7,11]. However, the incidence rate of warts in Dutch general
practice decreased between 1987 and 2001 [6]. This change is poorly understood and it
is unknown whether this change is related to socio-demographic characteristics.
Only a small proportion of children with sufficient complaints have parents that seek
professional medical help. These patients represents the tip of the iceberg [12]. No
data about the shape of the iceberg of patients infected with warts in the Netherlands
has been previously available.
Warts continue to be a therapeutic challenge and no treatment has been defined as
the gold standard. Conventional methods which are painful and poorly tolerated by
children, attempt to destroy infected tissue in a non-specific way. Topical treatments
containing salicylic acid have a therapeutic effect, but cryotherapy is less efficious
[1,2,13].
The present study relies on two large consecutive surveys performed in general practice and aimed to gain more insight in the epidemiology and management of warts in
children.
Our research questions were:
What is the self-reported prevalence of warts in children aged 0-17 years and what
proportion of these children consulted the GP for warts?
What is the incidence of warts in general practice in children aged 0-17 and the GPs
management; did it change between 1987 and 2001?
Methods
We used data from the first (1987) and second (2001) Dutch national survey of general
practice, performed by the Netherlands Institute for Health Services Research (NIVEL).
57
Both surveys included a representative sample of the Dutch population. In the Netherlands, general practices have a fixed list size, all inhabitants are listed in a general
practice, and GPs have a gate-keeping role.
Dutch national survey I (1987)

A non-proportionally stratified sample of 161 GPs in 103 practices was selected randomly [14]. The participating GPs and practices were representative for Dutch GPs
and practices in 1987 with respect to age and gender. Because there was an underrepresentation of solo practices and practices in deprived areas, the population was
weighted to the Dutch population of 1987. The GPs were divided into four groups and
each group registered data (e.g. diagnosis, prescription and referrals) about all contacts
between patient and practice during one of four consecutive 3-month periods. Patient
demographic characteristics (age and gender) were derived from patient records. Socioeconomic status (SES) and ethnic origin were obtained by a questionnaire and filled out
by parents, or by the children themselves if they were older than 12 years (response rate
91.2%). Ethnic origin was derived from country of birth from either parent. Degree of
urbanization was derived from the practices postal zip code and categorized into four
Chapter 5
classes. The Netherlands were divided into a Northern, Central and Southern region.
58
Dutch national survey II (2001)

195 GPs in 104 practices registered data about all physician-patient contacts during 12
months [16]. All health problems were coded (ICPC) by the GPs themselves during the
consultation. Patient demographic characteristics (age and gender) were derived from
the GPs computerized patient files. As in 1987, SES and ethnic origin were obtained by
a questionnaire (response rate 76%). Degree of urbanization, region and season were
derived in a similar way as in 1987. Contrary to 1987, in 2001 therapeutic interventions
apart from prescriptions were registered by only a part of the practices (N=72) during a
part of the registration period (6 weeks).
In both surveys each contact with the practice was defined as one consultation and
recorded separately. Both surveys were episode orientated, meaning that a consultation on a new health problem marked the beginning of a new episode. If there were
multiple consultations in a single episode, the diagnosis made during the last consultation was regarded as the episode-diagnosis. In 2001 we excluded nine practices from
analysis, mainly because of technical problems with registration.
To assess the prevalence of warts in the population and to determine if childhood

warts seen by physicians represent the tip of the iceberg, we used additional health
interview data of the second Dutch national survey in 2001 (similar data of 1987 were
not available). Patients were invited to participate in a health interview (response rate
65%) after they were selected randomly (5% sample) from the list of the participating
GPs. One of the questions in the interview was whether the participants had suffered
from warts during fourteen days before the interview. The interview was conducted
with one parent or caretaker as a proxy when the child was younger than 12 years. In
children 12 through 17 years old the interview was done in the presence of a parent
or caretaker.
Ethical approval
studies.
Data-analysis
Self-reported prevalence of warts was expressed as the proportion of those who reported to suffer from warts, divided by the number of children interviewed, stratified
for sociodemographic characteristics. Among these children we assessed the proportion
of those who consulted the GP for their warts, the so called helpseekers, and those
who did not consult the GP for their warts, the so called non-helpseekers. We defined
helpseekers as those who reported to suffer from warts and consulted their GP within
14 days before and 3 months after the interview, and in whom the GP made the diagnosis of warts or a diagnosis of another skin disease that may be confused with warts
by the lay public. The diagnosis made by the GP in these consultations are listed in the
appendix. Differences between helpseekers and non-helpseekers were assessed at a
significance level of 5% using the Pearson Chi-Square test for categorical variables and
the Linear-by-Linear Association test for ordinal variables.
From both surveys data of children aged 0-17 years were analyzed. Incidence rates
of warts in general practice were calculated by dividing the number of new episodes
with ICPC code S03 (numerator) by the average study population at risk, the so called
mid-time population (denominator). The mid-time population was calculated as the
mean of all listed patients of all participating GPs, aged 0-17 years, at the beginning and
at the end of the registration period. Incidence rates were expressed per 1000 person
years. 95% confidence intervals of incidence rates were calculated assuming a Poisson
distribution.
59
Results
The study population in 1987 consisted of 86,577 children aged 017 years yielding
21,644 person years. In 2001 the study population consisted of 87,952 children aged
017 years yielding 81,716 person years.
Self reported prevalence of warts and help seeking

In total 2847 children aged 017 years were interviewed in 2001 about their health
status; of these 176 (6.2%) reported to suffer from warts. From these 176 children 41
(23.3%) sought medical help and the GP diagnosed warts or a warts-like diagnosis.
In only 20 (11.4%) of the 176 children the GP made the diagnosis warts within a time
window of 14 days before and 3 months after the health interview. We repeated this
analysis for different time windows and found almost similar results.
Table 1 shows the distribution of the self-reported prevalence of warts during the pre-
hort
hort te
te zitten
zittenvious
op
op2 weeks
bladzijde
bladzijde
81.
stratified for 81.
sociodemographic
characteristics. The highest prevalence
were found in the age category 5-9 and 10-14 years. Infants (< 1 year) did not suffer
Chapter 5
from warts. Table 1 also shows a comparison in socio-demographic characteristics

of helpseekers versus non-helpseekers; there were no differences between these two
groups.
cidence
cidence rates
rates
of
ofhort
warts
warts
in
in
general
general
practice
practice per
per 1000
1000 person
person years
years
Deze figuur
te zitten op
bladzijde
81.
Incidence rate of warts in general practice

In 1987,
the GPs saw
episodes
of warts.practice
Of these
episodes
76.2% years
consisted of
Figuur
1: Incidence
rates963
of warts
in general
per
1000 person
a single contact with the GP. In 2001, the GPs saw 2625 episodes of warts. Of these
episodes 71.8% consisted of a single contact with the GP.
1987
2001
1987
1987
2001
2001
120
100
80
Incidence rate
60
60
40
20
0
0
10
Age (years)
Figuur 1: Incidence rates of warts in general practice per 1000 person years
11
12
13
14
15
16
17
Table 1: Prevalence of warts among 2847 children aged 0-17 years in the population during two weeks and sociodemographic characteristics of medical helpseekers versus non-helpseekers
self-reported
prevalence
(%)
N0 = 176
95% Confidence
Intervals (%)
helpseekers
(N1 = 41)
(%)
non-helpseekers
(N2 = 135)
(%)
< 1 year
14
3.7
2.4 5.5
17.1
14.1
59
8.4
6.6 10.6
46.3
40.0
10 14
7.2
5.5 9.2
29.3
37.0
15 17
3.7
2.1 6.1
7.3
Total
6.2
5.3 7.2
Boys
5.9
4.7 7.3
46.3
48.9
Girls
6.5
5.2 8.0
53.7
51.1
< 30,000
5.3
4.1 6.7
31.7
39.3
30,000-50,000
7.2
5.1 9.9
19.5
22.2
> 50,000
7.2
5.5 9.2
43.9
34.1
Big Cities1
4.6
2.0 9.1
4.9
4.4
Northern
6.5
4.4 9.4
15.0
16.3
Central
6.6
5.4 7.9
55.0
60.0
Southern
5.5
4.0 7.4
30.0
23.7
Non-manuel high
5.1
3.7 6.7
30.3
35.8
Non-manuel middle
7.5
5.6 9.8
45.5
33.9
Non-manuel low & farmers
7.0
4.0 11.3
6.1
12.8
Manuel high/middle
6.2
3.2 10.9
12.1
7.3
Manuel low
5.7
3.0 9.7
6.1
10.1
Natives & Western Immigrants
6.3
5.3 7.5
97.1
93.0
Non Western Immigrants
4.3
2.0 8.2
2.9
7.0
P-value
Age categories
100
0.646
8.9
100
Gender
0.941
Urbanization
0.257
Region
0.677
SES
0.544
Ethnicity
0.276
N0 = children who reported to suffer from warts in the population

N1 = children who suffer from warts and consulted the GP within 14 days before and 3 months after the interview
N2 = children who suffer from warts and did not consulted the GP within this timeframe
Figure 1 represents the distribution of incidence rates of warts presented to the GP by

age in years. In 1987 the peak incidence rate was found at the age of seven whereas
in 2001 this peak reached at the age of six. On almost each age between 0-17 the
incidence rate of warts presented to the GP was higher in 1987.
61
Table 2: Incidence rates of warts per 1000 person years in Dutch general practice in 1987 and 2001
1987
2001
Incidence
rates
95% Confidence
intervals
Incidence
rates
95% Confidence
intervals
< 1 year
0 2.8
0 0.8
1 4 years boys
12.7
8.5 18.2
12.2
10.1 14.7
girls
15.0
10.2 21.1
12.5
10.2 15.1
5 9 years boys
71.5
62.2 81.7
48.4
44.6 52.5
girls
75.5
65.6 86.4
55.7
51.4 60.2
Age categories
10 14 years boys
41.4
34.3 49.5
34.4
31.2 38.0
girls
63.4
54.5 73.4
37.3
33.9 41.0
15 17 years boys
39.2
31.5 48.1
18.3
15.3 21.8
girls
42.3
33.8 52.1
30.8
26.7 35.3
Total
44.5
41.7 47.4
32.1
30.9 33.4
Boys
40.6
36.9 44.5
29.4
27.8 31.1
Girls
48.7
44.6 53.1
34.5
32.7 36.3
< 30,000
40.1
35.7 44.9
32.5
30.7 34.5
30,000-50,000
43.1
38.7 48.0
33.0
30.1 36.0
> 50,000
61.2
54.1 69.0
28.7
26.7 30.9
Big cities1
29.8
22.6 38.6
24.1
20.1 28.7
Northern
49.4
40.9 59.0
35.2
31.8 38.8
Central
42.8
39.4 46.4
31.1
29.5 32.7
Southern
46.7
41.1 52.9
32.7
30.4 35.1
Winter
47.2
41.3 53.8
31.3
28.9 33.9
Spring
44.1
39.1 49.6
33.2
30.7 35.8
Summer
31.4
26.4 37.1
31.9
29.5 34.4
Autumn
52.5
46.8 58.6
30.9
28.5 33.3
Non-manuel high
53.4
46.9 60.4
35.5
33.1 38.1
Non-manuel middle
50.9
42.8 60.1
37.1
34.2 40.2
Non-manuel low & farmers
39.7
28.0 54.8
36.8
31.8 42.3
Manuel high/middle
44.5
37.8 51.9
37.7
32.2 43.9
Manuel low
39.9
33.1 47.8
31.0
26.9 35.7
47.1
43.7 50.7
36.2
34.6 37.9
27.4
18.9 38.5
30.0
25.6 34.8
Gender
Chapter 5
Urbanization
62
Region
Season
SES
Ethnicity

Table 2 shows the distribution of the incidence rates of warts in general practice between
1987 and 2001, stratified for socio-demographic characteristics. The total incidence rate
decreased by 28% from 44.5 (1987) to 32.1 (2001). In both surveys the highest incidence
rate were found in age category 5-9 years. Girls showed a higher incidence rate of warts
presented to the GP, but we found the most striking differences in gender among 10-14
year olds in 1987 and among 15-17 year olds in 2001.
In 1987 we found the highest incidence rate in cities (> 50,000 inhabitants) and the
lowest in the three big cities whereas in 2001 the incidence rate was similar over all
urbanization levels. Except for the three big cities in 2001 the incidence rate decreased
over all urbanization levels. In both surveys the incidence rate is similar among all
regions. In 1987 the lowest incidence rate was found in summer whereas in 2001 all
seasons showed the same incidence rates. Except for summer, in 2001 the incidence
rate decreased in all seasons. In 1987 the highest incidence rate was found in SES class
I and class II whereas in 2001 these two classes showed a striking decrease. In both
surveys natives and western immigrants presented more often with warts to the GP
than non-western immigrants, but the difference became smaller in 2001. In 1987 the
incidence rate of warts was higher in practices that treated warts with cryotherapy.
Management of warts in general practice.

Table 3 shows rates of prescriptions, therapeutic interventions and referrals concerning
warts per 100 episodes in 1987 and 2001. In both surveys the prescription rate was
similar and salicylic acid was the most frequently prescribed treatment. In both surveys
the majority of warts were treated with cryotherapy. The rate of surgery and referrals
decreased by about 50% in 2001. Practices that did not apply cryotherapy had a considerable higher referral rate in both surveys.
Table 3: Prescriptions, interventions and referrals of children with warts per 100 episodes
1987
2001
All prescriptions
23.1
23.9
Salicylic acid
11.1
10.3
Antiseptic
0.5
0.6
Emollients
0.3
2.3
Others
11.1
10.8
Cryotherapy (liquid nitrogen)
58.0
48.0
Surgery
8.0
4.8
All referrals
6.1
3.1
Referrals in practices applying cryotherapy
2.1
2.6
Referrals in practices not applying cryotherapy
18.1
7.9
63
Discussion
Summary of main findings
The self-reported prevalence of warts among Dutch children (0-17 years) is 6.2%; of
these children 23.3% consulted the GP for warts.
Between 1987 and 2001 the total incidence rate of warts presented to the GP decreased
by 28%.
In both surveys GPs treated the majority of children with warts by applying cryotherapy
(liquid nitrogen) with salycilic acid on the second place. In 2001 GPs referred fewer
children to secondary care compared to 1987.

These two large representative and comprehensive surveys enabled us to assess accurately epidemiological data on warts in children. For this study data of only two points
in time were available. Actually to identify a sustained trend of the incidence of warts
in general practice data of multiple points in time are needed. Although our health
interview had a response rate of 65%, the responders were representative for the Dutch
Chapter 5
population [17].
64
disturb the comparability of data. For example ICPC coding of the diagnoses was not
performed equally in both surveys: in 1987 clerks coded diagnoses afterwards, whereas
in 2001 the GPs coded the diagnoses themselves during the consultation.
Comparison with existing literature

The self-reported prevalence in our study is consistent with one previous study performed among Romanian school children (6-12 years) showing a prevalence of 6.3%
[10]. A Dutch study (1959) among schoolchildren reported a prevalence of 7.2%; the
prevalence in our study among children of the same age (5-14 years) is 7.8% indicating
that the prevalence has hardly changed over time [5].
No data about the so-called iceberg phenomenon of warts in the Netherlands is available. A Dutch study showed that 28% of the children (0-14 years) that reported to suffer
from skin diseases consulted their GP for that reason [18].
The decrease in incidence rate of warts in general practice, which is in proportion to
the decreasing overall GP consultation rate in the Netherlands [6], is not consistent
with a previous study which has been performed in four practices in the eastern part
of the Netherlands [19]. The decreasing overall GP consultation rate is a consequence
of changing patients attitudes showing a shift away from consulting their GP for minor
ailments [20]. Assuming that warts are a minor ailment the decreased incidence rate
could be explained by a changing patients attitude. Further it is unclear whether the
proportion of children suffering from warts used over-the-counter medication or other
self-care strategies and did not seek medical help, has changed over time.
In both surveys, girls especially between 10-17 years, visited the GP more often concerning warts, which is in accordance with a previous study [19]. However most large
studies have found no evidence of a sex difference in wart prevalence [7]. Probably girls
are more sensitive for the esthetic aspects of the disease.
Williams et al. reported in 1993 that being a resident in the south of Britain, having a
father with non-manual occupation and belonging to an ethnic group other than white
European were associated with a decreased risk of warts [9]. Beside ethnic origin our
results are different. Natives and western immigrants more often consulted the GP
concerning warts.
The majority of patients with warts were treated with cryotherapy (liquid nitrogen), although the evidence for this treatment is weak [1,2,13]. Probably the use of cryotherapy
is simple and safe. In both surveys Dutch GPs chose for salicylic acid if it came to a
prescription, which is in accordance with evidence about efficacy [1,2,13].
In 2001 more practices (85%) provided cryotherapy than in 1987 (70%). However, in
2001 the use of cryotherapy and surgery (table 3) is lower than in 1987. Probably
patients used primarily self-care strategies and consulted their GP in a later phase of
the disease which should have consequences for the GPs management and choice
of treatment. In both surveys about 11% of the prescriptions (table 3) were magistral
preparations. In both surveys practices that did not apply cryotherapy had a considerable higher referral rate.
Implications for future research or clinical practice

More insight should be gained in what proportion of children with warts primarily apply self-care and do not seek medical help or consult their GP in a later phase of the
disease.
More high quality randomized controlled trials should be performed in order to confirm
the efficacy of cryotherapy (liquid nitrogen) in the treatment of warts.
65
References
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2.
3.
4.
5.
6.
7.
8.
9.
Chapter 5
10.
66
11.
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17.
18.
19.
20.
Sladden MJ, Johnston GA. Common skin infections in children. BMJ 2004; 329: 9599.
Gibbs S, Harvey I, Sterling JC, Stark R. Local treatments for cutaneous warts. The Cochrane
Database of Systematic Reviews. 2003, Issue 3. Art. No.: CD001781. DOI: 10.1002/14651858.
CD001781.
Ciconte A, Campbell J, Tabrizi S, Garland S, Marks S. Warts are not merely blemishes on
the skin: A study on the morbidity associated with having viral cutaneous warts. Australas
J Dermatol 2003; 44: 169173.
Allen AL, Siegfried EC. Whats new in human papillomavirus infection. Curr Opin Pediatr
2000; 12: 365369.
van der Werf E. Een onderzoek naar het vrkomen en het verloop van wratten bij schoolkinderen. [Study on the incidence and course of warts in schoolchildren]. Ned Tijdschr
Geneeskd 1959; 103: 12041208.
1722.
Kilkenny M, Marks M. The descriptive epidemiology of warts in the community. Australas
J Dermatol 1996; 37: 8086.
Kilkenny M, Merlin K, Young R, Marks R. The prevalence of common skin condition in
Australian school students: Common, plane and plantar viral warts. Br J Dermatol 1998;
138: 840845.
Williams HC, Pottier A, Strachan D. The descriptive epidemiology of warts in British schoolchildren. Br J Dermatol 1993; 128: 504511.
Popescu R, Popescu CM, Williams HC, Forsea D. The prevalence of skin conditions in
Romanian school children. Br J Dermatol 1999; 140: 891896.
Silverberg NB. Human papillomavirus infections in children. Curr Opin Pediatr 2004; 16:
402409.
Last JM. The iceberg: Completing the clinical picture in general practice. Lancet 1963; 2:
28 31.
Bensing JM, Foets M, van der Velden J, van der Zee J. De nationale studie van ziekten
1991; 34: 5161.
Westert GP, Schellevis FG, de Bakker DH, et al. Monitoring health inequalities through
general practice: the Second Dutch National Survey of general practice. Eur J Public Health
2005; 15: 5965.
Bruijnzeels MA, Foets M, van der Wouden JC, van den Heuvel WJA, Prins A. Everyday
symptoms in childhood: occurrence and general practitioner consultation rates. Br J Gen
Pract 1998; 48: 880884.
Cardol M, Schellevis FG, Spreeuwenberg P, van de Lisdonk EH. Changes in patients attitudes towards the management of minor ailments. Br J Gen Pract 2005; 55: 516521.
Appendix
Skin diseases and the corresponding ICPC [15] codes diagnosed by the GP among
helpseekers:
S03
Warts
S05
Lumps / swellings generalized
S06
Rash localized
S11
Skin infection post-traumatic
S20
Corn / callosity
S74
Dermatophytosis
S75
Moniliasis / candidiasis skin
S82
Naevus / mole
S87
Dermatitis / atopic eczema
S88
Dermatitis contact / allergic
S90
Pityriasis rosea
S93
Sebaceous cyst
S95
Molluscum contagiosum
67
Incidence and management of

dermatophytosis in children in
general practice. A comparison
Mohammedamin RSA, van der Wouden JC, Koning S, Schellevis FG, van Suijlekom-Smit LWA, Koes BW.
Incidence and management of dermatophytosis in children in general practice. A comparison between 1987
and 2001 [submitted].
Abstract
Background
Dermatophytosis is a common skin infection in children. Although the epidemiology is
relatively unknown it is becoming a major health problem in some countries.
Objectives
To determine the incidence and management of dermatophytosis in Dutch general
practice, and assess trends between 1987 and 2001.
Methods
We used data of all children aged 0-17 years derived from two national surveys performed in Dutch general practice in 1987 and 2001 respectively. Both surveys concerned a longitudinal registration of GP consultations over 12 months. All diagnoses,
prescriptions and referrals were registered by the participating general practitioners
(GPs), 161 and 195 respectively.
Each disease episode was coded according to the International Classification of Primary
Chapter 6
Care. Incidence rates were calculated by dividing all new episodes by the average study
70
population at risk. Data were stratified for socio-demographic characteristics.
Results
Compared to 1987, in 2001 the total incidence rate of dermatophytosis in children
in general practice increased. Infants (< one year), girls, children in rural areas and
children of non-western immigrants more often consulted the GP for dermatophytosis
in 2001
In both surveys GPs treated the majority of children with dermatophytosis with topical
drugs, especially with azoles.
Conclusions
The incidence rate of dermatophytosis in children in general practice increased; however it is unclear whether this is a consequence of an increasing prevalence in the
population or a changing help seeking behaviour. GPs generally follow the national
guideline for the treatment of dermatophytosis in children which is in accordance with
evidence-based knowledge on the effectiveness of different therapies.
Incidence and management of dermatophytosis
Background
Superficial fungal skin infections (dermatophytosis) caused by dermatophytes are known
as tinea and will have a specific name depending on body location, as in tinea capitis,
tinea corporis, or tinea pedis [1]. Dermatophytoses are common in children [2,3,4].
Little data is available about the epidemiology of dermatophytosis in children in the population. Most studies in this field dealt with adults or with a specific form of dermatophytosis. The few surveys performed in children reported a prevalence that varies from 2.5
15.2% [5,6,7] and differ from country to country. Tinea capitis is predominantly a disease of children, especially under 12 years of age, and rare in adults [2,3,4,7,8,9,10,11,12].
The frequency of tinea capitis is declining in developed nations; however in the United
Kingdom and the United States it is becoming a major public health problem, and AfroCaribbean children are particularly affected [5,9,10,11,12,13]. Data about the other forms
of dermatophytosis in children are relatively limited available.
Initial analysis by Otters et al showed that the incidence rate of dermatophytosis in children in Dutch general practice has increased between 1987 and 2001 [14]. It is unclear
whether this increase reflected an increase of the incidence in the population and is
related to socio-demographic characteristics. Knowledge about the factors contributing
to the increasing incidence might improve the care for patients with dermatophytosis in
general practice and its prevention.
Both topical and oral treatments are proven to be effective [15,16,17]. However, in a
British study only 7% of children had received appropriate treatment for tinea capitis
before referral to dermatology practice [11]. The evaluation of management of dermatophytosis in children in general practice is therefore important. In 1997, the Dutch
College of General Practitioners issued a clinical guideline for the diagnosis and treatment of dermatophytosis for all ages [18]. We do not have a clear insight in the degree
of application of this guideline in children.
In the present study we compared the results of two consecutive surveys in general
practice performed in 1987 and 2001 respectively and aimed to answer the following
research questions:
What was the incidence rate of dermatophytosis in children aged 0-17 in general
practice in 1987 and in 2001?
Were these incidence rates related to socio-demographic characteristics?
How did the GP manage dermatophytosis (prescription, referral) and did this change
between 1987 and 2001?
71
Methods
We used data from the first and second Dutch national surveys of general practice, which
were performed by the Netherlands Institute for Health Services Research (NIVEL) in
1987 and 2001. Each survey included a representative sample of the Dutch population.
In the Netherlands, general practices have a fixed list size, all inhabitants are listed in a
general practice, and GPs have a gate-keeping role. Usually, the first contact with health
care, in a broad sense, is the contact with the general practitioner.
In 1987 a non-proportionally stratified sample of 161 GPs in 103 practices was selected
randomly to participate in the first national survey [19]. With respect to age and gender
the participating GPs and practices were representative of Dutch GPs and practices in
1987. The GPs were divided into four groups, and each group used registration forms to
register data (e.g. diagnosis, prescription and referrals) on all contacts between patient
and practice during one of four consecutive 3-month periods. Baseline characteristics
such as age and gender were derived from patient records. Other socio-demographic
characteristics such as socio-economic status (SES) and ethnic origin were obtained by
Chapter 6
a questionnaire and filled out by parents, or by the children themselves if they were
72
older than 12 years (response rate 91.2%). SES was based on the fathers occupation,
which was categorized into five classes non-manual work high (class I), non-manual
work middle (class II), non-manual low and farmers (class III), manual work high /
middle (class IV) and manual work low (class V). Ethnic origin was derived from the
country of birth of either parent. If either parent was born in Turkey, Africa, Asia (except
Japan and Indonesia) and Central or South America, their children were considered to
be children of non-western origin (in accordance with the classification of Statistics
Netherlands). All other children were defined as western. The degree of urbanization
was derived from the general practices postal code and categorized into four classes
under 30,000 inhabitants, 30,000-50,000 inhabitants, over 50,000 inhabitants and
the three large Dutch cities Amsterdam, Rotterdam and The Hague. The Netherlands
were divided into a Northern, Central and Southern region. Season was divided into
four categories: spring was defined as months April-June, summer as July-September,
autumn as October-December and winter as January-March. The diagnoses made by
the GPs were coded afterwards by clerks using the International Classification of Primary Care (ICPC) [20].
In 2001, data about all physician-patient contacts over 12 months were derived from
the electronic medical records of all listed patients in 104 practices (195 GPs) [21]. The
GPs registered data on diagnosis, prescriptions and referrals, and coded the diagnosis
themselves using the ICPC. Patient demographic characteristics such as age and gender
were derived from the GPs computerized patient files. As in 1987, SES and ethnicity
were obtained by a questionnaire (response rate 76%). Degree of urbanization, region
and season were defined as in 1987.
the beginning of a new episode. If there were multiple consultations in a single episode, the diagnosis made during the last consultation was regarded as the episode-diagnosis. In both surveys all prescriptions were coded according to the ATC classification
(Anatomical-Therapeutical-Chemical) [22]. Concerning referrals, the GPs registered the
indication and specialism of referral. In 2001 we excluded data from nine practices from
the analyses, mainly because of technical problems with registration.
Ethical approval
studies.
Data-analysis
This study analyzed data from both surveys for children aged 0-17 years presenting with
dermatophytosis which was coded as S74 (ICPC). Because of an underrepresentation
of deprived areas, the 1987 survey population was weighted to the Dutch population
of 1987. Incidence rates were calculated by dividing the weighted number of new
episodes (numerator) by the study population at risk (denominator).
For 2001 we calculated the incidence rate of dermatophytosis by dividing the total
number of new episodes (numerator) by the average study population at risk, the midtime population (denominator). The mid-time population was calculated as the mean
of all listed patients of all participating GPs, aged 0-17 years, at the beginning and at the
end of the registration period. Data were stratified by age, gender, urbanization level,
region, season, SES and ethnic origin. Incidence rates per 1000 person-years and 95%
confidence intervals were calculated assuming a Poisson distribution. In both surveys,
we only included the first new episode for every child. Thus we excluded two recurrent
episodes in 1987 and 77 in 2001.
Prescriptions and referrals were expressed as proportions of all new episodes.
73
Results
The study population in 1987 consisted of 86,577 children aged 0-17 years yielding
21,644 person years. These children had 559 contacts concerning dermatophytosis
which contributed to 450 episodes; 85.3% of these episodes included a single contact
with the GP. In 2001 there were 87,952 children yielding 81,716 person-years. These
children had 2318 contacts concerning dermatophytosis which contributed to 2007 episodes; 88.2% of these episodes consisted of only one contact with the GP.
Incidence rate
Table 1 shows the distribution of incidence rates of dermatophytosis in 1987 and 2001
in general practice stratified for several background characteristics. Compared to 1987,
in 2001 the total incidence rate of dermatophytosis in general practice increased by
18%.
In 2001 versus 1987 the incidence rate of dermatophytosis in general practice increased
in young children (0-4 years); infants (< one year) showed in 2001 a three fold higher
Chapter 6
incidence rate.
74
Compared to 1987 in 2001, the GP more often diagnosed dermatophytosis in girls than
boys. In 1987 we found the highest incidence rate in the three big cities and the lowest
in the rural areas (< 30,000) whereas in 2001 it was distributed equally over all urbanization levels. Compared to 1987, in 2001 the incidence rate increased in the rural areas
(< 30,000) and decreased in small cities (30,000-50,000), whereas it remained stable in
larger cities (> 50,000) and the three big cities. In 1987 we found the highest incidence
rate in the central part of the Netherlands compared to the northern part whereas in
2001 the incidence rates were not different between regions. In 2001, the incidence rates
increased in the northern and southern part of the Netherlands compared to 1987.
In both surveys the incidence rates were distributed equally over all seasons and SES
classes. In 2001 versus 1987 the incidence rate of dermatophytosis in general practice
increased in summer.
In 2001, the GP more often diagnosed dermatophytosis in children of non-western
immigrants than in children of natives and western immigrants.
Prescriptions
In 1987 the GPs made 388 prescriptions in the first contact of the episode; in 92.5% of
these episodes only one drug was prescribed. In 10% of the episodes the GPs did not
prescribe any medication in the first contact. During all episodes the GPs made 464
Table 1: Incidence rates per 1000 person years of all new episodes of dermatophytosis in general practice in 1987 and 2001
1987
2001
Incidence
Rates
95% Confidence
Intervals
Incidence
Rates
95% Confidence
Intervals
P-value
< 1 year
12.8
7.520.5
35.1
29.8 41.1
< 0.01
1 4 years
17.4
13.7 21.7
24.8
22.6 27.2
< 0.01
5 9 years
19.7
16.3 23.7
18.9
17.2 20.8
0.69
10 14 years
24.8
20.9 29.2
24.0
22.1 26.1
0.73
15 17 years
22.7
18.5 27.7
27.6
24.9 30.6
0.07
Total
20.8
18.9 22.8
24.6
23.5 25.7
< 0.01
Boys
20.0
17.4 22.8
22.6
21.2 24.1
0.08
Girls
21.7
18.9 24.7
26.0
24.4 27.6
< 0.01
< 30,000
16.6
13.9 19.8
23.0
21.5 24.7
< 0.01
30,000 50,000
23.3
20.0 26.9
18.2
16.1 20.5
0.01
> 50,000
20.4
16.4 25.1
19.8
18.1 21.6
0.80
Big Cities 1
27.7
20.8 36.2
24.1
20.1 28.7
0.41
Northern
14.4
10.0 20.0
24.8
22.0 27.9
< 0.01
Central
22.3
19.9 24.9
23.9
22.5 25.3
0.28
Southern
19.8
16.2 24.0
25.7
23.7 27.9
< 0.01
Winter
19.3
15.6 23.7
22.7
20.7 24.9
0.14
Spring
23.1
19.6 27.2
26.4
24.2 28.7
0.13
Summer
19.9
16.0 24.5
25.4
23.3 27.7
0.02
Autumn
20.3
16.8 24.2
22.2
20.3 24.3
0.36
Non-manual high
21.0
17.1 25.6
21.9
20.0 23.9
0.70
Non-manual middle
20.0
15.1 26.0
24.0
21.7 26.5
0.18
Non-manual low & farmers
23.6
14.8 35.8
25.6
21.5 30.3
0.71
Manual high / middle
21.7
17.1 27.0
23.4
19.1 28.4
0.62
Manual low
26.7
21.2 33.3
25.1
21.4 29.3
0.66
Natives & Western

Immigrants
21.7
19.4 24.1
22.3
21.0 23.6
0.65
29.9
20.9 41.4
33.6
29.0 38.7
0.50
Age Categories
Gender
Urbanization
Region
Season
SES
Ethnic origin

prescriptions resulting in an average prescription rate of 1.16 per episode; in 7.5% of the
episodes the GPs did not prescribe any medication.
75
Table 2: Prescriptions in the first contact of dermatophytosis episode

1987
2001
Number (%)
Number (%)
400 (100)
2007 (100) 2
Oral treatments
Antifungals
13 (3.3)
113 (5.6)
Azoles
13 (3.3)
48 (2.4)
Allylamines
0 (0)
60 (3.0)
Others
0 (0)
5 (0.2)
Antifungals
231 (57.8)
1098 (54.7)
Azoles
209 (52.3)
1002 (49.9)
Allylamines
0 (0)
43 (2.1)
Undecenoic acid
20 (5.0)
41 (2.0)
Others
2 (0.5)
12 (0.6)
Combinations (antifungals & corticosteroids)
94 (23.5)
375 (18.7)
Corticosteroids
10 (2.5)
20 (1.0)
Emollients
3 (0.8)
31 (1.5)
Others
37 (9.3)
78 (3.9)
No prescription in 1st contact
40 (10)
451 (22.5)
Chapter 6
Topical treatments
76
1 = unweighted number of new episodes

2 = number of new episodes in the mid-time population
In 2001 the GPs made 1715 prescriptions in the first contact of the episode; in 90.4% of
these episodes only one drug was prescribed. In 22.5% of the episodes the GPs did not
prescribe any medication in the first contact. During all episodes the GPs made 2333
prescriptions resulting in an average prescription rate of 1.16 per episode; in 18.3% of
the episodes the GPs did not prescribe any medication.
In table 2 we present the drugs prescribed in the first contact of the episode. In both
surveys about three quarters of the dermatophytosis cases were treated with topical
drugs; GPs prescribed in about 50% of the children with dermatophytosis topical antifungals and in about 20% topical antifungals combined with topical steroids. Oral antifungals were applied in only a very small proportion of the cases. However, compared
to 1987, in 2001 the proportion of oral antifungal prescriptions almost doubled from 3.3
to 5.6%. For oral treatment in 1987 only azoles were prescribed whereas in 2001 both
azoles and allylamines were prescribed in almost equal proportions.
Referrals
In 1987 twelve (2.6%) and in 2001 thirty-two (1.6%) of the children with dermatophytosis were referred to the dermatologist. In 1987 the boys to girls ratio of referred children
was 3:1, whereas in 2001 this was 1:2.
Discussion
Incidence and sociodemographics
The incidence rate of dermatophytosis in general practice increased over the past 14
years which is consistent with a previous study performed in the Netherlands [23].
Considering the decrease of the overall consultation rate of children in Dutch general
practice (second Dutch national survey) [14] the increased incidence rate of dermatophytosis in general practice is substantial. Probably our finding is a consequence of an
increased prevalence in the population as reported by Sladden et al [12] who showed
that dermatophytosis is becoming a major health problem in the U.K. and the U.S.A. A
previous study reported that the consultation rate for onychomycosis in Dutch general
practice increased from 5.9 (1999) to 8.2 (2000-1) and fell to 4.9 (2002) following a
nationwide information campaign performed by the manufacturer of terbinafine in the
Netherlands, advising people with onychomycosis to visit their GP [24]. Alternatively the
increased incidence rate does not reflect an increase in incidence of dermatophytosis in
the population but a higher inclination to present this disease to the GP.
The GPs more often diagnosed dermatophytosis in girls which is different from a previous Dutch study [23]. However, the prevalence of dermatophytosis in the population
was found to be higher in boys [3,4,6] in three studies in Mediterranean countries.
Probably girls are more sensitive for the esthetic aspects of the disease and therefore
present this problem more easily to their GP.
The incidence rate increased in rural areas (< 30,000) and remained stable in urban areas. A previous study performed in children in rural areas in Turkey [6] reported that the
prevalence of dermatophytosis is higher under poor hygienical conditions. However, in
the Netherlands, the difference in hygiene conditions between rural and urban areas is
negligible. Considering the decrease of the overall consultation rate of children in Dutch
general practice (second Dutch national survey) [14] it might reflect an increase in incidence rate of dermatophytosis in children in general practice in urban areas. However,
our finding is consistent with two British studies that reported an increased prevalence
of tinea capitis in south-east London, a highly urbanized area [10,11].
Children of non-western immigrants consulted their GP more often with dermatophytosis; in 2001 this difference became more apparent. The significantly higher overall
consultation rate in non-western children might explain this difference [14]. The increasing racial and ethnic heterogeneity of the Dutch childhood population might contribute
to an increased incidence of dermatophytosis in the population. This is supported by
previous studies reporting that Afro-Caribbean children are particularly affected by tinea
77
capitis in the UK [12] and that the prevalence of tinea capitis in Stockholm increased
corresponding with the increased immigration from Africa [25].
Prescriptions
Between 1987 and 2001 the prescription pattern of the GP changed. In 2001 more oral
antifungals especially terbinafine (not available in 1987) were prescribed. Probably,
this was influenced by the nationwide information campaign, as mentioned earlier [24].
In 2001 there were more episodes in which the GP did not prescribe any medication.
Probably this has to do with the fact that nowadays more over-the-counter drugs are
available for dermatophytosis; patients who initially use these medications may consult
their GP in a later phase of the disease which should have consequences for the GPs
management.
The majority of the dermatophytosis patients were treated with topical azoles and a
very small proportion with allylamines or other antifungals indicating that dermatophytoses were primarily treated with azoles. This is in accordance with the results of the
Cochrane reviews [15,16] and the clinical guideline for the treatment of dermatophytosis
Chapter 6
issued by the Dutch College of General Practitioners in 1997 [18].
78
In 2001 there were more episodes that included only one contact with the GP and more
oral medication especially allylamines were prescribed. In both surveys the prescription
rate per episode is the same, but in 2001 there were more episodes in which the GP
did not prescribe any medication. The referral rate per episode in 2001 is lower than in
1987. These changes in disease management could be the consequence of the introduction of the clinical guideline for diagnosis and treatment of dermatophytosis issued by
the Dutch College of General Practitioners in 1997 [18] which may have improved the
care for patients with dermatophytosis in general practice.
Referrals
The boys to girls ratio of referred children concerning dermatophytosis strikingly
changed from 3:1 (1987) to 1:2 (2001). As suggested earlier, girls may be more sensitive
for the esthetic reasons of the disease and therefore consulted the GP more often than
boys in 2001. This is supported by our previous analysis [27] showing that girls more
often consulted the GP than boys concerning all skin diseases combined. Possibly, for
cosmetic reasons girls or their parents put more pressure on the GPs for being referred
to a dermatologist.
Strengths and limitations of the study

These two large representative and comprehensive surveys enabled us to assess accurately epidemiological data on dermatophytosis in children. For this study data of
only two points in time were available. To identify a sustained trend of the incidence of
dermatophytosis in general practice data of multiple points in time are needed.
disturb the comparability of data. For example ICPC coding of the diagnoses was not
performed equally in both surveys: in 1987 clerks coded diagnoses afterwards, whereas
in 2001 the GPs coded the diagnoses themselves during the consultation. We assume
that coding by clerks more often led to a specific diagnostic ICPC code.
In the present study the accuracy of diagnoses (S74) made by the GPs could be a
subject of debate. In our analysis we assumed that the diagnoses made by the GPs were
correct. In 2001 the participating GPs were trained in coding the diagnoses correctly
using ICPC codes. Overall these trained GPs classified diagnoses correctly in about 81%
of the test cases [26].
However, initial analysis showed that the incidence rate of diaper rash (S89) decreased
by about 50% in 2001 [27]. Possibly GPs have coded diaper rash as dermatophytosis
which may have lead to an overestimation of the incidence rate of dermatophytosis
in 2001. Another possibility is that GPs have coded dermatophytosis as diaper rash in
1987, which may have led to an underestimation of the incidence rate of dermatophytosis in 1987.
Conclusions
In general practice the incidence rate of dermatophytosis in children increased, especially in girls, children of non-western immigrants, rural areas and in the northern and
southern part of the Netherlands. This increase in incidence rate could be a consequence of an increasing prevalence in the population. More studies on the population
prevalence of dermatophytosis and help seeking behaviour are needed, especially in
children of non-western immigrants and rural areas to test this hypothesis.
GPs generally follow the clinical guideline for diagnosis and treatment of dermatophytosis in children which is in accordance with evidence-based knowledge on the
effectiveness of different therapies.
79
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general practice]. Utrecht / Bilthoven, NIVEL / RIVM 2004.
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81
Association between skin

diseases and severe bacterial
infections in children:
case-control study
Mohammedamin RSA, van der Wouden JC, Koning S, Willemsen SP, Bernsen RMD, Schellevis FG, van
Suijlekom-Smit LWA, Koes BW. Association between skin diseases and severe bacterial infections in children:
case-control study. BMC Family Practice 2006; 7: 52.
Abstract
Background
Sepsis or bacteraemia, however rare, is a significant cause of high mortality and serious complications in children. In previous studies skin disease or skin infections were
reported as risk factor. We hypothesize that children with sepsis or bacteraemia more
often presented with skin diseases to the general practitioner (GP) than other children.
If our hypothesis is true the GP could reduce the risk of sepsis or bacteraemia by
managing skin diseases appropriately.
Methods
We performed a case-control study using data of children aged 017 years of the second
Dutch national survey of general practice (2001) and the National Medical Registration
of all hospital admissions in the Netherlands. Cases were defined as children who were
hospitalized for sepsis or bacteraemia. We selected two control groups by matching
each case with six controls. The first control group was randomly selected from the GP
patient lists irrespective of hospital admission and GP consultation. The second control
Chapter 7
group was randomly sampled from those children who were hospitalized for other rea-
84
sons than sepsis or bacteraemia. We calculated odds ratios and 95% confidence intervals
(CI). A two-sided p-value less than 0.05 was considered significant in all tests.
Results
We found odds ratios for skin related GP consultations of 3.4 (95% CI: [1.1 10.8], p =
0.03) in cases versus GP controls and 1.4 (95% CI: [0.5 3.9], p = 0.44) in cases versus
hospital controls. Children younger than three months had an odds ratio (cases / GP
controls) of 9.2 (95% CI: [0.81106.1], p = 0.07) and 4.0 (95% CI: [0.67 23.9], p = 0.12)
among cases versus hospital controls. Although cases consulted the GP more often with
skin diseases than their controls, the probability of a GP consultation for skin disease
was only 5% among cases.
Conclusions
There is evidence that children who were admitted due to sepsis or bacteraemia consulted the GP more often for skin diseases than other children, but the differences are
not clinically significant indicating that there is little opportunity for GPs to reduce the
risk of sepsis and/or bacteraemia considerably by managing skin diseases appropriately.
Association between skin diseases and severe bacterial infections
Background
Sepsis or bacteraemia requiring hospital admission is rare, however it is a significant
cause of high mortality and serious complications such as septic shock and multi organ
dysfunction syndrome [1,2,3]. Currently, little data is available about the causal factors
of sepsis or bacteraemia in children in the population. The available studies in this field
deal particularly with adults or with children belonging to high-risk groups such as
neonates and those who are immunocompromized due to HIV infection and children
with underlying malignancies [4,5,6,7]. The few studies which have been performed on
sepsis or bacteraemia in children from the general population are case series [8,9,10] or
deal with specific causative bacterial agents [1,11,12,13].
Three previous studies of which only one performed in children reported that from the
identifiable primary focus in patients with sepsis or bacteraemia most often (22-37%) an
infection of the skin was detected [1,2,12]. Children suffering from atopic dermatitis are
chronic carriers of Staphylococcus Aureus and run therefore a higher risk to develop
sepsis or bacteraemia [9,14]. Skin infections are almost always curable, but some may
lead to serious complications such as nephritis, carditis, arthritis and sepsis if the diagnosis is delayed and/or treatment is inadequate [15].
A Dutch study performed in children aged 0-14 years reported that 28% of those with
skin diseases consulted the general practitioner (GP) [16]. Hence, for this reason, we
hypothesize that children who were admitted to hospital due to sepsis or bacteraemia
suffered more often from skin diseases, especially skin infections, and therefore visited
their GP for this reason more often prior to their admission compared to their controls.
If our hypothesis is true and given the fact that skin diseases account for 23% of the
total morbidity in children in general practice [17], the GP may be able to reduce the
risk of sepsis or bacteraemia by recognizing the skin diseases in time and treating them
adequately.
To test this hypothesis we performed a case-control study, aiming to answer the following research question:
- Did children who were admitted to a hospital for sepsis or bacteraemia visit their GP
more often for skin diseases before their admission, compared to matched controls?
85
Methods
We used data of the second Dutch National Survey of general practice performed by
NIVEL (Netherlands Institute for Health Services Research) in 2001 and data of the LMR
(National Medical Registration in the Netherlands).
Second Dutch National Survey

In the Netherlands, general practices have a fixed list size and all inhabitants are listed
with a general practice, and GPs have a gate-keeping role. Usually, the first contact with
health care, in a broad sense, is the contact with the general practitioner. This survey
included a representative sample of the Dutch population. Data about all physicianpatient contacts, prescriptions and referrals during 12 months in 2001 were extracted
from electronic medical records of all listed patients of 104 practices (195 GPs) [18]. All
diagnoses were coded using the International Classification of Primary Care (ICPC) [19].
Different health problems within one consultation were recorded separately. Sociodemographic characteristics such as age, gender, region and urbanization level of all
patients listed to the participating GPs were derived from the GPs computerized patient
Chapter 7
file. The degree of urbanization was derived from the general practices postal code
86
and categorized into four classes under 30,000 inhabitants, 30,000-50,000 inhabitants, over 50,000 inhabitants and the three large Dutch cities Amsterdam, Rotterdam
and The Hague. The Netherlands were divided into a Northern, Central and Southern
region. Childrens socioeconomic status (SES) and ethnic origin were obtained by a
questionnaire filled out by parents or by the children themselves if they were older than
12 years (response rate 76%). SES was based on the fathers occupation, which was categorized into five classes non-manual work high (class I), non-manual work middle
(class II), non-manual low and farmers (class III), manual work high / middle (class
IV) and manual work low (class V). Ethnicity was derived from the country of birth
of either parent. If either parent was born in Turkey, Africa, Asia (except Japan and
Indonesia) and Central or South America, their children were considered to be children
of non-western origin (in accordance with the classification of Statistics Netherlands).
All other children were defined as western. Eight practices were excluded from analysis
because of insufficient quality of data registration.
National Medical Registration (LMR)

This continuous registration contains information about hospital admissions, diagnostic
and therapeutic interventions of all hospitals in the Netherlands. All diagnoses were
coded using the International Classification of Diseases 9th revision (ICD-9) [20]. Previous research revealed that about 87% of the patients referred by the GP to a specialist
can be linked to a record of the hospital register [21].
Definition of cases
Cases were defined as being diagnosed with sepsis or bacteraemia at discharge. The
corresponding ICD-9 codes for sepsis and bacteraemia are listed in Appendix 1. Cases
were only selected when their admission date was at least 14 days after the start and
before the end of the one-year registration period of the survey in general practice. If
cases had more than one admission within a week concerning the same health problem
only the first admission was selected. We excluded all children who were primarily
admitted to a hospital for skin diseases (N = 29), but assessed GP consultations of these
children 14 days prior to their hospital admission.
Selection of controls
We selected two control groups by matching each case with six controls. Cases and controls were matched on age group (table 1), gender and region. The first control group
was randomly selected from the GP patient lists irrespective of hospital admission and
GP consultation, the so called GP controls. The second control group was composed
by drawing a random sample from those children who were admitted to a hospital for
other reasons than sepsis or bacteraemia, the so called hospital controls. This second
control group was added because we can not rule out that some of our severely ill cases
bypassed the general practitioner prior to their hospital admission which might lead to
an under-estimation of contacts with the GP in this group.
Data-analysis
We analyzed data of all children aged 0-17 years and assessed whether a higher proportion of cases visited the GP with any disease, especially skin disease as listed in
the S-chapter of the ICPC (Appendix 2), within 14 days prior to their admission than
controls (GP controls and hospital controls). We calculated odds ratios for presence of
GP consultations for all diseases, skin diseases and other diseases than skin diseases
(cases / controls) and 95% confidence intervals (CI) using a conditional logistic regression model. We performed the same analysis for skin diseases within 30 days prior to
the hospital admission of the cases. We repeated the latter analysis in a more strictly
defined group (N = 44) of cases suffering from sepsis or severe bacteraemia and their
matched controls. These cases were explicitly defined as being admitted to hospital
due to sepsis, meningitis, acute osteomyelitis, acute pyelonefritis, acute mastoiditis,
infectious arthritis or pneumonia. A two-sided p-value less than 0.05 was considered
significant in all tests.
87
Table 1: Baseline characteristics in percentages of cases and controls

Cases
(N = 101)
GP Controls1
(N = 597)
Hospital Controls2
(N = 583)
Age group
0 3 months
8.9
7.7
9.3
3 6 months
6.9
6.9
5.8
6 24 months
27.7
30.2
28.3
24 72 months
27.7
26.8
26.8
6 17 years
28.7
28.5
29.8
Boys
63.4
63.7
64.3
Girls
36.6
36.3
35.7
< 30,000
36.6
38.0
36.4
30,000 50,000
18.8
15.9
17.5
> 50,000
37.6
39.2
36.9
Big cities3
6.9
6.9
9.3
Northern
19.8
20.1
18.0
Central
61.4
60.8
62.4
Southern
18.8
19.1
19.6
Nonmanual high
34.1
37.4
38.8
Nonmanual middle
31.8
31.3
35.6
Nonmanual low & farmers
15.9
13.5
5.0
Gender
Urbanization
Chapter 7
Region
88
SES
Manual high / middle
2.3
7.5
9.6
15.9
10.3
11.0
85.7
89.8
87.2
Non Western Immigrants
14.3
10.2
12.8
Manual low
Ethnicity
1 = control group randomly sampled from the general practitioners (GP) patient lists irrespective of hospital admission and GP
consultation
2 = control group randomly sampled from those children who were being hospitalized for other reasons than sepsis or bacteraemia
Results
Study population
The total general practice population included 88,307 children aged 0-17 years. We
found 101 cases that could be matched with 597 GP controls and 583 hospital controls.
Table 1 shows the baseline characteristics of cases and both control groups. Cases were
comparable to their controls regarding socio-demographic characteristics.
GP consultations
Sixty eight cases (67%) consulted the GP 161 times within 14 days prior to their hospital
admission; five cases (5%) consulted the GP for a skin disease. Among the GP controls
67 consultations were made by 53 (9%) children within 14 days prior to the admission of the case they were linked to; nine controls (1.5%) consulted the GP for a skin
disease. In the same period 255 (43.7%) children among the hospital controls consulted
their GP 477 times; of these children 20 (3.4%) presented a skin disease. Table 2 shows
which skin diseases were presented to the GP by cases and controls.
Children who were primarily admitted to hospital for a skin disease (N = 29) and
excluded from analysis had the following diagnosis at discharge: skin abscesses, cellulitis, erysipelas, impetigo, infected finger/toe, paronychia and local skin infections. Of
these children 14 (48%) consulted the GP 28 times within 14 days prior to their hospital
admission. Eight children (28%) consulted the GP for a skin disease.
Table 2: GP consultation for skin diseases within 14 days prior to hospital admission of cases
Diagnoses
ICPC1
Cases
(N = 101)
GP Controls2
(N = 597)
Hospital Controls3
(N = 583)
Pruritis
S02
Rash localized
S06
S11
Insect bite / sting
S12
Burn / scald
S14
Bruise / contusion
S16
Laceration / cut
S18
Dermatophytosis
S74
S75
Naevus / mole
S82
Impetigo
S84
Dermatitis seborrhoeic
S86
S87
S88
Diaper rash
S89
Sebaceous cyst
S93
S95
Urticaria
S98
1 = International Classification of Primary Care

2 = control group randomly selected from the general practitioners (GP) patient lists irrespective of hospital admission and GP
consultation
3 = control group randomly sampled from those children who were being hospitalized for other reasons than sepsis or bacteraemia
89
Strengths of relationships
Table 3 shows the odds ratios (cases / controls) for whether or not a GP was consulted
stratified for skin diseases and other diseases than skin diseases within 14 days prior
to the hospital admission of the cases for children aged 0-17 years. Compared to their
controls, more cases consulted the GP. The odds ratio for skin diseases (cases / GP
controls) was 3.4 (95% CI: [1.1-10.8], p = 0.03) and 1.4 (95% CI: [0.5 3.9], p = 0.44) for
cases versus hospital controls.
Table 3a and 3b show the odds ratios of skin diseases and other diseases for children
younger than three months and for children aged three months 17 years respectively.
Cases younger than three months showed an odds ratio (cases / GP controls) of 9.2
(95% CI: [08.1 106.1], p = 0.07). In this age group the odds ratio (cases / hospital controls) was 4.0 (95% CI: [0.67 23.9], p = 0.12). In all age groups significantly more cases
consulted the GP for other diseases than skin diseases 14 days prior to their hospital
admission compared to matched controls.
Chapter 7
Table 3: GP consultations of children aged 0-17 years admitted for severe bacterial infections and matched controls: odds
ratios, 95% confidence intervals and p-values
90
Diagnoses according
to ICPC1
Cases (N = 101)
vs
GP controls (N = 597)
Cases (N = 101)
vs
Hospital controls (N = 583)
Skin diseases
(S01 S99)
OR2 3.4 [1.1 10.8], p = 0.03
OR 1.4 [0.5 3.9], p = 0.44
Other diseases
OR 33.0 [16.4 66.7], p < 0.0001
OR 2.8 [1.8 4.5], p < 0.0001
All diseases
OR 25.9 [13.6 49.4], p < 0.0001
OR 2.7 [1.7 4.2], p < 0.0001

2 = Odds ratio
Table 3a: GP consultations of children < 3 months admitted for severe bacterial infections and matched controls: odds
ratios, 95% confidence intervals and p-values
Diagnoses according
to ICPC1
Cases (N = 9)
vs
Cases (N = 9)
vs
Skin diseases
(S01 S99)
OR2 9.2 [0.81 106.1], p = 0.07
OR 4.0 [0.67 23.9], p = 0.12
Other diseases
OR 19.2 [2.2 164.0], p = 0.007
OR 5.8 [1.13 30.3], p = 0.03
All diseases
OR 15.3 [1.8 130.1], p = 0.012
OR 5.9 [1.13 30.3], p = 0.03

2 = Odds ratio
Table 3b: GP consultations of children aged 3 months 17 years admitted for severe bacterial infections and matched
controls: odds ratios, 95% confidence intervals and p-values
Diagnoses according
to ICPC1
Cases (N = 92)
vs
Cases (N = 92)
vs
Skin diseases
(S01 S99)
OR2 2.5 [0.7 9.9], p = 0.17
OR 1.0 [0.3 3.5], p = 0.98
Other diseases
OR 34.8 [16.6 73.2], p < 0.0001
OR 2.6 [1.6 4.2], p < 0.0001
All diseases
OR 27.2 [13.7 53.2], p < 0.0001
OR 2.4 [1.5 4.0], p = 0.002

2 = Odds ratio
Repeated analysis of consultations for skin diseases within 30 days prior to the hospital
admission of the cases showed similar results, as did repetition of the analysis restricted
to the most severe cases (N = 44) and their controls.
Discussion
We tested the null hypothesis that there is no difference between children admitted for
sepsis or bacteraemia and other children as to consulting a GP for skin diseases in a
period of 14 days before admission to hospital. We found that there is an association
between skin diseases presented to the GP and subsequent hospitalization for sepsis or
bacteraemia among GP controls but not for hospital controls.
We performed the same analysis in cases and controls younger than three months and
found an even stronger relationship, though not significant. This lack of significance is
probably due to the small number of cases in this age group.
From a clinical point of view the difference between cases and controls may not be very
relevant. The probability that a case consulted the GP for skin diseases prior to their
hospital admission is only about 5% and therefore not a point of departure for GPs to
reduce the risk of sepsis and/or bacteraemia considerably by diagnosing and treating
skin diseases appropriately. However, considering cases younger than 3 months (N =
9) about 22% consulted the GP for skin diseases prior to their hospital admission which
means that GPs may have possibilities in this age group to reduce the risk of sepsis
and/or bacteraemia considerably by diagnosing and treating skin diseases appropriately. We recommend replication of our study in a larger dataset for this age group.
91
Compared with both control groups our cases visited the GP about two times as high
with both infectious skin diseases and atopic skin diseases as well, which could support
the association between sepsis or bacteremia and infectious and atopic skin diseases
[1,2,9,12,14].
In all age groups we found odds ratios concerning GP consultations for other diseases
than skin diseases that are considerably high and significantly different (p < 0.0001)
compared to the odds ratios for skin diseases. This finding indicates that there is a very
strong association between GP consultations for other diseases than skin diseases, 14
days prior to hospital admission, and being hospitalized for sepsis or bacteraemia.
These two large and representative datasets enabled us to assess accurately odds ratios
among cases and their matched controls and to test our hypothesis. By matching our
cases and controls on age, gender and region we adjusted for differences concerning
these variables and also for other socio-demographic characteristics (table 1). To limit
the seasonal variation of the GP consultations we selected only the consultations that
took place within 14 days prior to the admission date of the case to whom the controls
Chapter 7
were linked to.
92
Overall the odds ratio for a GP consultation concerning skin diseases among cases
versus GP controls 14 days prior to the admission of the cases is higher compared to the
odds ratio among cases versus hospital controls. Our findings are in accordance with an
earlier finding by Infante-Rivard [22] that inferences of severe childhood diseases using
hospital controls in comparison with population controls resulted in odds ratios closer
to the null value.
Conclusions
There is evidence that children who were admitted due to sepsis or bacteraemia consulted the GP more often for skin diseases prior to their admission, than other children,
but the differences are not clinically relevant which means that there is little opportunity
for GPs to reduce the risk of sepsis and/or bacteraemia considerably by diagnosing and
treating skin diseases appropriately.
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93
Appendix 1
To select our sepsis cases we used the ICD-9 code [20].
Chapter 7
We used the following codes and subcodes:
94
036
Meningococcal infection
036.0
Meningococcal meningitis
036.1
Meningococcal encephalitis
036.2
Acute meningococcaemie (meningococcal septicemia)
036.3
Waterhouse-Friderichsen
036.4
Meningococcal heart disease (carditis, endocarditis, myocarditis, pericarditis)
036.8
Other meningococcal infections (optic neuritis)
036.9
Meningococcal infection, unspecified
038
Septicaemia
038.0
Streptococcal septicaemia
038.1
Staphylococcal septicaemia
038.2
Pneumococcal septicaemia
038.3
Septicaemia due to anaerobes
038.4 Septicaemia due to other Gram-negative organisms (Haemophilus Influenzae,

E.Coli, Pseudomonas, Serratia)
038.8
Other specified septicaemias
041
Bacterial infection in conditions classified elsewhere
041.0
Streptococcus
041.1
Staphylococcus
041.2
Pneumococcus
041.3
Friedlanders bacillus
041.4
Escherichia coli (E.coli)
041.5
Haemophilus influenzae (H. influenzae)
041.6
Proteus (mirabilis, morganii)
041.7
Pseudomonas
041.8
Other
041.9
Bacterial infection, unspecified
320
Bacterial meningitis, not elsewhere classified
320.0
Haemophilus meningitis
320.1
Pneumococcal meningitis
320.2
Streptococcal meningitis
320.3
Staphylococcal meningitis
320.8
Meningitis due to other specified bacteria
320.9
Meningitis due to unspecified bacterium
383
Mastoiditis and related conditions
383.0
Acute mastoiditis (abscess of mastoid, empyema of mastoid)
420
Acute pericarditis
421
Acute and subacute endocarditis
421.0
Acute and subacute bacterial endocarditis
481
Pneumococcal pneumonia
482
Other bacterial pneumonia
482.0
Pneumonia due to Klebsiella pneumoniae
482.1
Pneumonia due to Pseudomonas
482.2
Pneumonia due to H. Influenzae
482.3
Pneumonia due to Streptococcus
482.4
Pneumonia due to Staphylococcus
482.8
Pneumonia due to other specified bacteria
482.9
Bacterial pneumonia, unspecified
483
Pneumonia due to other specified organism
513
Abscess of lung and mediastinum
513.0
Abscess of lung
513.1
Abscess of mediastinum
580
Acute glomerulonephritis (includes: acute nephritis)
590
Infections of kidney
590.1
Acute pyelonephritis (acute pyelitis, acute pyonephrosis)
711
Arthropathy associated with infections
711.0 Pyogenic arthritis (arthritis due to E. coli, H. influenzae, Pneumococ, Staphylococ, Streptococ)
730
Osteomyelitis, periostitis, and other infections involving bone
730.0
Acute osteomyelitis
95
Appendix 2
The S-chapter (skin diseases) of the International Classification of Primary Care (ICPC)
Chapter 7
[18]:
96
S01
Pain / tenderness of skin
S02
Pruritus
S03
Warts
S04
Lump / swelling localized
S05
Lumps / swellings generalized
S06
Rash localized
S07
Rash generalized
S08
Skin colour change
S09
Infected finger / toe
S10
Boil / carbuncle
S11
S12
Insect bite / sting
S13
Animal / human bite
S14
Burn / scald
S15
Foreign body in skin
S16
Bruise / contusion
S17
Abrasion / scratch / blister
S18
Laceration / cut
S19
Skin injury other
S20
Corn / callosity
S21
Skin texture symptom / complaint
S22
Nail symptom / complaint
S23
Hair loss / baldness
S24
Hair / scalp symptom / complaint
S26
Fear of cancer of skin
S27
Fear of skin disease other
S28
Limited function / disability(s)
S29
Skin symptom / complaint other
S70
Herpes zoster
S71
Herpes simplex
S72
Scabies / other acariasis
S73
Pediculosis / skin infestation other
S74
Dermatophytosis
S75
S76
Skin infection other
S77
Malignant neoplasm of skin
S78
Lipoma
S79
Neoplasm skin benign / unspecified
S80
Solar keratosis / sunburn
S81
Haemangioma / lymphangioma
S82
Naevus / mole
S83
Congenital skin anomaly other
S84
Impetigo
S85
Pilonidal cyst / fistula
S86
Dermatitis seborrhoeic
S87
S88
S89
Diaper rash
S90
Pityriasis rosea
S91
Psoriasis
S92
Sweat gland disease
S93
Sebaceous cyst
S94
Ingrowing nail
S95
S96
Acne
S97
Chronic ulcer skin
S98
Urticaria
S99
Skin disease other
97
Summary and general

discussion
Summary
The increasing proportion of skin diseases, especially infectious and allergic skin diseases, encountered in general practice represents a substantial part of the morbidity in
children. Only limited information is available about the epidemiology of skin diseases
in children in general practice and many questions in this field are still unanswered. In
this thesis, after a general overview of all skin related morbidity in children in general
practice, we will focus on the changes in the incidence and management of infectious
skin diseases during the past decades.
Moreover, we aim to identify determinants that are associated with the incidence of
infectious skin diseases in children encountered in general practice in order to provide
tools for improvement of general practice care and prevention of infectious skin diseases and their complications.
We performed an observational study comparing data of the two Dutch national surveys. The setting of the research was general practice as, in the Netherlands, the majority of skin diseases were diagnosed and treated by general practitioners.
In chapter 2 we compared incidence rates of all skin diseases presented by children
aged 0 17 years in general practice between 1987 and 2001.
The incidence rate of all skin diseases combined in general practice decreased between
1987 and 2001. Among infants (<one year) the incidence rate increased. Girls presented
more skin diseases to the GP. In the southern part of the Netherlands children consulted their GP more often for skin diseases compared to the northern part. Children of
non-western immigrants presented relatively more skin diseases to the GP. In general
practice incidence rates of specific skin diseases such as impetigo, dermatophytosis and
atopic dermatitis increased in 2001, whereas warts, contact dermatitis and skin injuries
decreased.
In chapter 3 we describe the epidemiology and management of impetigo in children
in general practice. Impetigo is the most common bacterial skin infection in children.
Results from two points in time (1987 and 2001) are compared.
The incidence rate of impetigo increased from 16.5 (1987) to 20.5 (2001) per 1000
person years under 18 years old (p < 0.01). In both years, the incidence was significantly higher in summer, in rural areas and in the southern region of the Netherlands,
compared to winter, urban areas and northern region respectively. Socio-economic
status was not associated with the incidence rate. From 1987 to 2001, there was a trend
towards prescribing topical antibiotic treatment (from 40% to 64%), especially fusidic
acid cream and mupirocin cream.
101
In chapter 4 a comparison over time of the incidence rate and management of acne
in children and adolescents is presented. Acne is a mulifactorial disease in which the
Propionibacterium acnes plays an important role and therefore acne is considered a
bacterial skin infection.
The incidence rate of acne in general practice decreased from 20.0 (1987) to 11.8 (2001)
per 1000 person years. Girls, adolescents aged 15-19 years and non-western immigrants
consulted the general practitioner more often with acne compared to boys, other age
groups and western immigrants respectively. Overall, general practitioners treated acne
according to the clinical guideline.
In chapter 5, warts, the most common (viral) skin disease in children in general practice, is examined in more detail. Self-reported prevalence and trends in incidence rates
and management in children in general practice are identified over time.
The self-reported prevalence of warts in children is 6.2%, and 23.3% of these children
consulted the general practitioner for warts. The incidence rate of warts in general practice decreased from 44.5 (1987) to 32.1 (2001) per 1000 person years. Girls, especially
in puberty, and children of natives consulted the general practitioner more often with
Chapter 8
warts compared to boys and children of non-western immigrants respectively. General
102
practitioners treated the majority of warts by applying cryotherapy with salicylic acid
on the second place.
In chapter 6 we determine the incidence and management of dermatophytosis in
children in general practice, and assess trends between 1987 and 2001.
Dermatophytosis is a common skin infection in children. Although the epidemiology is
relatively unknown it is becoming a major health problem in some countries.
Compared to 1987, in 2001 the total incidence rate of dermatophytosis in children in
general practice increased. Infants (< one year), girls, children in rural areas and children
of non-western immigrants more often consulted the GP for dermatophytosis in 2001
compared to older children, boys, children from urban areas and natives respectively.
GPs generally follow the clinical guideline for the treatment of dermatophytosis in
children.
In chapter 7 we explored the association between skin diseases, especially skin infections, and severe bacterial infections requiring hospitalization in children. Sepsis or
bacteraemia, however rare, is a significant cause of high mortality and serious complications in children. Skin diseases are considered to be an important causal factor in
children who are hospitalized due to sepsis or bacteraemia. Therefore we hypothesize
that these critically ill children suffer more often from skin diseases, especially skin
infections, and initially consult the general practitioner more often for that reason than
other children.
We found odds ratios for skin related GP consultations of 3.4 (95% CI:[1.1 10.8], p =
0.03) in cases versus GP controls and 1.4 (95% CI:[0.5 3.9], p = 0.44) in cases versus
hospital controls. Children younger than three months had an odds ratio (cases / GP
controls) of 9.2 (95% CI: [0.81106.1], p = 0.07) and 4.0 (95% CI: [0.67 23.9], p = 0.12)
among cases versus hospital controls. Although cases consulted the GP more often with
skin diseases than their controls, the probability of a GP consultation for skin disease
was only 5% among cases.
There is evidence that children who were admitted due to sepsis or bacteraemia consulted the GP more often for skin diseases than other children, but the differences are
not clinically relevant indicating that there is little opportunity for GPs to reduce the risk
of sepsis and/or bacteraemia considerably by managing skin diseases appropriately.
103
General discussion
The main objective of this thesis is to evaluate the epidemiology and management, and
clinical consequences of (infectious) skin diseases in children in general practice. This
thesis provides an overview of skin diseases presented by children in general practice
with special attention for the most frequent infectious skin diseases such as impetigo,
warts, dermatophytosis and acne.
This chapter discusses our findings, the general implications, the strengths and limitations of the study, and provides suggestions for future studies.
Increasing incidence of skin diseases?

An important finding, with considerable consequences for health care workers in general practice, is the declining incidence rate of skin diseases in children. In 2001, the
incidence rate decreased by about 10% compared with 1987. However, it is not clear
whether this decrease is a consequence of a changing frequency of skin diseases in
the general population or whether a change in help seeking behaviour has occurred.
Initial analysis of data from the same surveys by Otters et al [1] showed a decrease
Chapter 8
of the overall consultation rate by 22% in Dutch general practice between 1987 and
104
2001. Considering this decrease in consultation rate we could expect an even lower
incidence rate of skin diseases in 2001 in Dutch general practice. In the Netherlands no
comparable data about trends in the incidence rate of skin diseases in general practice
is available.
In part, the decreasing incidence rate of skin diseases in general practice could be a
consequence of changing consultation behaviour. We assume that, in 2001, there is a
higher threshold for contacting general practice by children for which there are several
arguments:
Parents postpone consulting the general practitioner in 2001?
It is possible that parents nowadays are better informed and more confident on how
to handle self-limiting health problems themselves, and therefore will wait longer before contacting general practice. This is supported by recent analyses which showed
that expectations of general practice care are lower for common and often self-limiting health problems [2,3]. Most skin diseases are common and/or self-limiting.
Since September 1999, the costs of frequently used self-care drugs are no longer
reimbursed by health insurance, which could have been a reason for consulting the
general practitioner in 1987 [2].
Nowadays more over-the-counter medications are available for which no prescription of the general practitioner is needed. Probably, nowadays patients use primarily
over-the-counter medication or other self-care strategies for minor ailments [2,3] and
do not seek medical help or consult their general practitioner in a later phase of the
disease. We assume that the most skin diseases are minor ailments.
Possibly, a societal phenomenon of the past years could also explain the decrease of
consultation rate in Dutch general practice. Nowadays it is much more common for
both parents to have daytime jobs, either full- or part-time. Consequently, children
may consult general practice less frequently and only if considered necessary by
parents.
General practitioners keep off consultation in 2001?
Possibly, due to the higher workload [4], general practitioners keep off consultation
for childhood conditions longer in 2001 than in 1987. In general, most skin diseases
in children have a benign course, and a wait and see advice is often justified. Therefore it is possible that general practitioners instruct their assistants to select more
strictly when parents call to make an appointment. As a possible consequence, these
parents may wait longer to contact general practice in a future episode of illness in
their child.
Changing childhood skin morbidity pattern in general practice between 1987 and 2001?
Children presented a different skin morbidity pattern in 2001 than in 1987. Overall
the incidence rate of allergic, bacterial and fungal skin diseases in general practice
increased whereas viral skin diseases decreased during the past decades.
For example the incidence rate of atopic eczema in general practice increased during
the past decades. Considering the decline in overall consultation rate in general practice
we could assume that the frequency of atopic eczema in the population has increased
which is in accordance with previous studies [5,6]. This increase can be explained by
the well-known hygiene theory. This theory states that the decrease in exposure to
infectious pathogens (smaller families, increase of hygienic customs) gives rise to an
increase of allergies and allergy related diseases [7,8,9].
However, parallel with the increasing incidence rates of atopic eczema, increasing incidence rates of impetigo and dermatophytosis are also observed in general practice.
This is an unexpected finding and it is hypothesized that the increased close contacts
between children in day care facilities and after school activities may be associated with
the higher occurrence of these skin infections in 2001 compared to 1987. A clinical
review by Sladden et al reported an increase of the population-based frequency of
dermatophytosis in the UK and the USA which is becoming a major health problem and
Afro-Caribean children are usually affected [10]. Currently, it is estimated that more than
105
13% of all 0-17 year olds belong to ethnic minority groups, compared with less than 7%
two decades ago.
The increased incidence rate of impetigo in general practice may also reflect a rising
tendency of medical attention-seeking; the unsightly aspect of (facial) impetigo may
now be less acceptable to parents than before. Also, there seems to be more pressure
from school for the child to undergo antibiotic treatment before they can be permitted
at school again. Possible explanations for an increased incidence at the population level
are either a change in human behaviour, such as increased traveling or, alternatively,
increased virulence of S. aureus [11]. Also, arise of antibiotic resistance in staphylococci
has been reported [12].
Conversely, acne vulgaris which we considered as a bacterial skin infection showed
a substantial decrease in incidence rate in general practice of 41% during the past
decades. This decrease is two fold as high as the decrease of the overall consultation
rate in general practice. Probably the population-based frequency of acne vulgaris has
Chapter 8
decreased during the past decades which is in accordance with a previous study [13].
106
Viral skin diseases (e.g. warts, mollusca contagiosa) showed also a decrease in incidence
rate which is in parallel with the declining overall consultation rate in general practice.
We assessed a self-reported prevalence of warts in children (0-17 years) of 6.2%. A
previous Dutch study performed in 1959 among schoolchildren reported a prevalence
of 7.2%; the self-reported prevalence in our study among children of the same age (5-14
years) is 7.8% indicating that the prevalence has hardly changed over time [14].
Are the incidence rates of skin diseases in general practice and its changes related to sociodemographic characteristics?
Age: overall we found the highest incidence rate of skin diseases encountered in general practice in young children, especially in infants (under one year) which is consistent
with previous studies [15,16]. The overall incidence rate in infants increased strikingly
between 1987 and 2001 whereas it decreased or remained stable in other age categories. We observed a similar trend in dermatophytosis. Impetigo and dermatophytosis
more often occurred in young children whereas warts and acne more often occurred in
older children and adolescents.
Gender: in 2001 girls presented more skin diseases in general practice than boys,
however the frequency of most skin diseases in the population is similar in both gender
or even higher in boys [17,18]. We observed a similar trend in the most frequent infec-
tious skin diseases such as warts, dermatophytosis and acne. Probably girls are more
sensitive for the esthetic aspects of skin diseases.
Regional variation: overall there is a north-south gradient of skin diseases presented
to the general practitioner with the highest incidence rate in the southern part of the
Netherlands. This is a very striking observation for a small country like the Netherlands.
It is of interest to know whether the frequency of skin diseases in the population is
higher in the southern part of the Netherlands. A sub-analysis of our data showed that
the overall GP consultation rate in children (0-17 years) is significantly higher in the
south compared to the north. Among the four most frequent infectious skin diseases
(impetigo, warts, dermatophytosis, acne) only impetigo showed a similar trend.
The twofold higher incidence rate of impetigo in the south compared with the north is
striking. Climatic differences within the country are small and seem to offer no explanation. We propose that staphylococcal transfer from pigs to humans may explain the
geographical gradient. There is a concentration of pig farming in the southern provinces
of the country, where approximately 10 times as many pigs are bred as in the northern
provinces [19]. It has been shown that pig farmers in France were more frequently nasal
carriers of S. Aureus than matched non-farmers [20].
No comparable data concerning regional variation of skin diseases in the Netherlands
is available about children.
Urbanization level: there seems to be a relation between incidence rate of skin diseases in general practice and urbanization level. Between 1987 and 2001, the overall
incidence rate of skin diseases in general practice increased in rural areas and decreased
or remained stable in suburban and urban areas. We observed a similar trend in impetigo and dermatophytosis. It is suggested elsewhere that children in rural areas are
more exposed to infectious pathogens due to the larger number of animals and farms
[21]. Probably, the population-based frequency of infectious (bacterial and fungal) skin
diseases increased in rural areas between 1987 and 2001. Actually, with the decreasing
overall consultation rate we would expect also a decrease of the incidence rate of skin
diseases in general practice in urban areas but this did not change between 1987 and
2001. Probably children in urban areas are suffering more from skin diseases. In part,
this is in accordance with the pollution hypothesis meaning that children in urban areas have a higher chance in developing atopic diseases [21,22]. Crowding in urban areas
could be a potential factor in spreading infectious skin diseases. The incidence rate of
acne and warts in general practice seems not to be related with urbanization levels.
107
Ethnic origin: the incidence rate of skin diseases encountered in general practice is
related to the ethnic origin. Children from non-western parents presented overall more
skin diseases to the general practitioner which is in parallel with the higher overall
consultation rate among these children [1]. However, we can not rule out whether
the population-based frequency of skin diseases is higher in children of non-western
immigrants. Previous studies reported the racial predisposition of some skin diseases;
viral warts especially occurs in white children [23] whereas tinea capitis occurs most
frequently in Afro-Caribbean children [24]. This is in accordance with our results. Except
for viral warts children of non-western immigrants presented more often with impetigo,
dermatophytosis and acne to the general practitioner.
Seasonal variability: in general practice the incidence rate of all skin diseases combined was higher in the warmer months (summer, spring) and lower in the colder
months (winter, autumn). No comparable data on this topic is available. Similar trends
were found in dermatophytosis and impetigo whereas in acne it was the other way
around. The incidence rate of warts is not related to season. These findings are consis-
Chapter 8
tent with previous studies [13,16].
108
Socio-economic status: we found higher incidence rates of skin diseases combined

in the lower socio-economic classes, which is consistent with previous studies [25,26].
From the four most frequent infectious skin diseases (impetigo, dermatophytosis, warts,
acne) only dermatophytosis showed a similar trend. Contrary to our results van de
Lisdonk et al [16] reported higher incidence rates of impetigo and acne in the lower
social classes in general practice.
Did general practitioners management of skin diseases in children change between 1987 and 2001?
Nowadays, general practitioners see a different pattern of skin diseases in children than
in 1987. It is of interest whether or how this shift is reflected in general practitioners
management. Referral to secondary health care and drug prescription are focused on
and these issues are discussed in the next part of this chapter. Moreover, the guidelines
issued by the Dutch College of General Practitioners could have affected general practitioners management [27,28,29].
General practitioners increasingly handle more skin problems themselves and refer
fewer children to secondary health care compared to 1987. In 2001, the referral rate of
the four most frequent infectious skin diseases (impetigo, warts, dermatophytosis and
acne) decreased substantially compared to 1987. Prescription patterns of general practitioners also changed between 1987 and 2001. Probably, these changes were induced
by the introduction of the national practice guidelines, issued by the Dutch College of
General Practitioners, for diagnosis and treatment of diseases. In general, Dutch general
practitioners prescribed treatments according to the national practice guideline and/or
evidence-based knowledge on the effectiveness of different therapies concerning impetigo, dermatophytosis and acne.
However, Dutch general practitioners treated warts applying a different strategy than is
recommended in literature [30]. Although there is only weak evidence for cryotherapy
with liquid nitrogen general practitioners treated the majority of patients with warts
by applying cryotherapy and with salycilic acid on the second place, indicating that
general practitioners do not follow the evidence-based knowledge on the effectiveness
of the treatment. Probably the use of liquid nitrogen is simple, cheap and safe. More
randomized controlled trials are needed to confirm or to reject the effectiveness of
liquid nitrogen.
General practitioners referral rate of warts decreased from 6.1% (1987) to 3.1% (2001).
Practices applying cryotherapy with liquid nitrogen for the treatment of warts have
a significant lower referral rate than practices that do not apply liquid nitrogen. This
may reflect that general practitioners believe in the effectiveness of liquid nitrogen due
to their experiences in daily practice and this should not necessarily imply that liquid
nitrogen is effective
The Dutch College of General Practitioners has not yet issued a guideline for the treatment of warts. Probably general practitioners need a guideline to hold on. The development of a treatment guideline is needed which could be based on evidence-based
knowledge of the effectiveness of the therapy and or consensus.
Over-the-counter medication: Nowadays more and more over-the-counter medications are available. Several topical drugs are obtainable without a prescription of the
general practitioner concerning the treatment of warts, dermatophytosis and acne. There
is a trend that more and more patients are applying self-care [3] and do not seek medical
help or consult the general practitioner in a later phase of the disease after it becomes
clear that the self-care does not improve the complaints adequately. This could have
consequences for the general practitioners management and choice of treatment. This
could for example, explain that general practitioners sometimes apply another treatment strategy than is recommended in the national practice guidelines. Although at
present we do not have a clear insight in what proportion of children primarily apply
self-care strategies.
109
Do infectious skin diseases predict serious complications?

Skin infections are almost always curable, but some may lead to serious complications
such as nephritis, carditis, arthritis and sepsis if the diagnosis is delayed and/or treatment is inadequate [31,32,33,34,35,36,37,38]. It is of interest to know whether general
practitioners could play a role in preventing such complications by diagnosing and
treating skin diseases timely and appropriately. We found that there is little difference between children being admitted in hospital for sepsis or bacteraemia and other
children as to consulting a general practitioner for skin diseases in a period of 14 days
before admission to hospital.
Moreover, general practitioners could only play a role in preventing such complications
if children with skin diseases consulted their general practitioner in time. A Dutch study
performed in children aged 0-14 years reported that 28% of those with skin diseases
consulted the general practitioner [39].
From a clinical point of view the difference with regard to skin diseases between
children being admitted to hospital due to sepsis or bacteraemia and other children is
Chapter 8
not relevant. The probability that a child being admitted to hospital due to sepsis or
110
bacteraemia consulted the general practitioner for skin diseases prior to their hospital
admission is only about 5% and therefore not a point of departure for general practitioners to reduce the risk of sepsis and/or bacteraemia considerably by diagnosing and
treating skin diseases appropriately.

These two large representative and comprehensive surveys enabled us to assess current epidemiological data of skin diseases presented by children in general practice.
We were able to identify a trend in the incidence rates of skin diseases encountered in
general practice between 1987 and 2001. These two surveys also enabled us to compare
general practitioners management between 1987 and 2001.
The data of the second National Survey (2001) enabled us also to assess the selfreported prevalence of warts in the population and what proportion of children that
reported to suffer from warts consulted their GP for that reason. Although the health
interview had a response rate of 65%, the responders were representative for the Dutch
population [40].
It is inevitable that comparison of nation-wide surveys of such magnitude has limitations and these should be considered when interpreting the results of this thesis. There
were small differences in the design of the two national surveys, which might disturb
the comparability of data.
Firstly, three-month incidence rates of 1987 were weighted to one-year incidence rates
and this may lead to skewed incidence rates (for 1987), especially if disease-specific
episodes consist of more than one contact.
Secondly, some of the differences in occurrence may be explained by the fact that ICPC
coding was not performed equally in both surveys. We assume that coding by clerks
in 1987 more often led to a specific diagnostic ICPC code, than in 2001, where general practitioners coded themselves leading to more symptom codes. These differences
should be considered when comparing incidence rates of both surveys.
Thirdly, in the present study the accuracy of diagnoses made by the GPs could be a
subject of debate. Concordance of GPs diagnoses with dermatologists diagnoses have
been shown to be around 50% [41]. In our analysis we assumed that the diagnoses
made by the participating GPs were correct. In 2001 the participating GPs were trained
in coding the diagnoses correctly using ICPC codes. Overall these trained GPs classified
diagnoses correctly in about 81% of the test cases [40].
Fourthly, because of the underrepresentation of deprived and urban areas in the survey
of 1987, the population was weighted to correct for morbidity presented in these areas.
In common disorders in children such as respiratory tract infections and most skin
diseases, comparability of rates between both surveys will be more valid. However, in
rare diseases the weight factor may lead to skewed rates.
Fifthly, for this study data of only two points in time were available. Actually to identify
a trend of the incidence rates of skin diseases in general practice data of multiple points
in time are needed.
General implications
Health care
This thesis provides an overview of current childhood skin morbidity as presented in
general practice and changes over the past decades. Dutch general practitioners are
provided with a frame of reference for their own daily practice.
Incidence rates of skin diseases in children in general practice are related to sociodemographic characteristics such as age, gender, urbanization, region, season, socioeconomic status and ethnic origin. Knowledge about these contributing factors may be
useful tools for preventive actions and to provide appropriate advices to patients. The
striking regional variation, especially in impetigo, and the racial predisposition (e.g.
warts, dermatophytosis) could be useful in diagnosing the disease.
111
This thesis shows that children presented a different skin morbidity pattern in general
practice in 2001 compared to 1987. They presented more infectious (bacterial and
fungal) and atopic skin diseases. These emerging skin problems should be monitored
in order to assess the future health burden and should be intervened if and where
necessary.
In addition, general practitioners seem to manage childhood skin problems increasingly themselves, implying that referrals to secondary care are made more selectively.
Specialists in secondary care, especially dermatologists to whom children with skin
diseases are usually referred to, should be aware of this trend in order to make a better
judgement of morbidity that is presented to them.
Overall, general practitioners follow evidence-based knowledge on the effectiveness of
different therapies and/or the national practice guideline, issued by the Dutch College
of General Practitioners.
Health care research
This thesis not only provides an overview of current childhood skin morbidity as preChapter 8
sented in general practice and changes over the past decades, but also reference mate-
112
rial of skin diseases for future studies. Consequently, this overview of childhood skin
morbidity and its changes over time may direct the future research agenda.
The childhood population of this study and their use of primary and secondary care
are representative for the population and demand of care of the near future. Moreover,
the children studied in this survey are representative for futures adolescents and adults.
Future studies on emerging skin problems (bacterial, fungal and atopic) are necessary
in order to introduce preventive strategies. The Dutch Health Council and public health
workers should be aware of trends therein in order to optimize the assessment of the
need of futures health services.
For instance, more dermatological expertise might thus be implemented in the vocational training programmes and continuing medical education programmes for GPs and
primary health care workers.
Recommendations for future studies

The emerging skin diseases such as infectious (bacterial and fungal) and atopic skin
diseases should be monitored in order to assess the future health burden and should be
intervened if and where necessary. Based on the results of our study, the major issues
to be evaluated in the future include:
As part of the issue of antibiotic resistance, more studies that establish the contribution
of a given treatment for impetigo to the development of bacterial resistance, such as
Ravenscroft [12], are desirable. Our hypothesis that there may be causality in the association of the incidence of impetigo and the location of the pig farming industry in
the southern part of the Netherlands merits further study. This research would consist of
bacteriological typing and comparison of staphylococcal strains derived from impetigo
patients in different regions of the country and from pigs.
Other questions that need to be answered are whether prompt treatment of impetigo
reduces contagiousness or prevents epidemics, and whether barring affected children
from school is an effective measure towards prevention. Research trying to establish the
untreated course of impetigo would be very useful.
Considering the increasing incidence rate of dermatophytosis in general practice, which
is most pronounced in rural areas and in children of non-western origin, more epidemiological research on the population-based frequency of dermatophytosis and medical
help-seeking behaviour are needed.
Although there is a considerable lack of evidence on the effectiveness of cryotherapy
by using liquid nitrogen Dutch general practitioners widely used this therapeutic option
for warts. More randomized controlled trials are needed to study the effectiveness of
cryotherapy.
Considering the striking and substantial decrease of the incidence rate of acne in children and adolescents in general practice more studies on the population-based frequency of acne and medical help-seeking behaviour are needed.
We currently do not have a clear insight in the use of over-the-counter medication.
Additional studies are necessary to assess what proportion of children and adolescents
with skin diseases, especially warts, dermatophytosis and acne apply self-care strategies.
Finally, it is recommendable to repeat these nation-wide surveys at time intervals of five
to ten years in order to identify trends in occurrence of diseases, medical help-seeking
behaviour and management strategies.
113
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115
Samenvatting
Samenvatting
Huidziekten vormen een belangrijk deel van de totale morbiditeit gepresenteerd door
kinderen aan de huisarts. In de afgelopen twee decennia zagen we een toename van
huidziekten gepresenteerd aan de huisarts door kinderen van 017 jaar. Er is relatief
weinig bekend over de epidemiologie van huidziekten in de huisartspraktijk.
In dit proefschrift wordt er in de eerste plaats een overzicht gegeven van alle aan de
huisarts gepresenteerde huidziekten door kinderen waarna er meer in detail wordt
gekeken naar de veranderende incidentie van infectieuze huidziekten in de afgelopen
decennia, en het beleid van de huisarts.
Verder wordt er geprobeerd determinanten te identificeren die geassocieerd zijn met
de incidentie van infectieuze huidziekten. Kennis over eventuele determinanten zou
kunnen bijdragen aan een adequate preventie van infectieuze huidziekten en mogelijke
complicaties. Wij hebben een observationele studie uitgevoerd waarbij wij gebruik hebben gemaakt van de data van beide Nationale Studies.
Alle studies uit dit proefschrift zijn in de huisartspraktijk uitgevoerd aangezien bijna alle
huidziekten bij kinderen door de huisarts worden gediagnostiseerd en behandeld.
In hoofdstuk 2 wordt er een overzicht gegeven van de incidentiecijfers van alle aan de
huisarts gepresenteerde huidziekten door kinderen (017 jaar) in 1987 en 2001.
Tussen 1987 en 2001 is de totale incidentie van de aan de huisarts gepresenteerde
huidziekten gestegen. Zuigelingen (< 1 jaar), meisjes, kinderen uit de zuidelijke provincies van Nederland en kinderen van niet westerse immigranten consulteren vaker
de huisarts voor een huid gerelateerd probleem ten opzichte van oudere kinderen,
jongens, kinderen uit centraal en noordelijk Nederland en kinderen van autochtone Nederlanders. Verder is de incidentie van impetigo, dermatophytosis and atopisch eczeem
gestegen tussen 1987 en 2001, terwijl wratten, contacteczeem en huidbeschadigingen
een daling laten zien van de incidentie bij kinderen in de huisartspraktijk.
In hoofdstuk 3 worden de epidemiologie en het beleid van de huisarts met betrekking
tot impetigo bij kinderen beschreven. Impetigo is de meest voorkomende bacterile
huidinfectie bij kinderen. Resultaten van twee meetpunten (1987 en 2001) worden
vergeleken.
Het incidentiecijfer van impetigo is gestegen van 16.5 (1987) naar 20.5 (2001) per 1000
persoonsjaren bij kinderen jonger dan 18 jaar, een statistisch significant verschil. Zowel
in 1987 alsook in 2001 zagen we dat in de zomer, op het platteland en in de zuidelijke
provincies van Nederland kinderen vaker impetigo aan de huisarts presenteerden. Sociaal-economische klasse is niet geassocieerd met de incidentie van impetigo. Tussen
1987 en 2001 zijn er veranderingen opgetreden met betrekking tot de behandeling van
117
impetigo: huisartsen zijn veel meer locale antibiotica gaan voorschrijven (van 40% naar
64% van alle recepten), waarbij fusidinezuurcreme and mupirocinecreme het meest
worden voorgeschreven.
In hoofdstuk 4 vergelijken we de incidentie van acne in de huisartspraktijk en het beleid van de huisarts bij kinderen en adolescenten op twee meetpunten (1987 en 2001).
Acne is een multifactorile huidziekte waarbij de Propionibacterie acnes onder andere
een belangrijke rol speelt bij het ontstaan van acne.
De incidentie van acne in de huisartspraktijk is gedaald van 20.0 (1987) naar 11.8
(2001) per 1000 persoonsjaren. Meisjes, adolescenten uit de leeftijdscategorie 15-19
jaar en niet-westerse immigranten consulteren de huisarts vaker met acne klachten dan
jongens, adolescenten uit andere leeftijdscategorien en autochtone Nederlanders. In
het algemeen behandelen huisartsen acne volgens de bestaande richtlijnen.
In hoofdstuk 5 bestuderen wij de epidemiologie van wratten en behandelstrategien
van de huisarts. Wratten worden veroorzaakt door een virus en vormen de meest voorkomende huidziekte bij kinderen.
Chapter 8
De zelf-gerapporteerde prevalentie van wratten bij kinderen is 6.2%; 23.3% van de
118
kinderen die rapporteren last te hebben van wratten consulteren de huisarts hiervoor.
De incidentie van wratten bij kinderen in de huisartspraktijk is gedaald van 44.5 (1987)
naar 32.1 (2001) per 1000 persoonsjaren. Meisjes, met name in de puberteit, en kinderen van autochtone Nederlanders consulteren de huisarts vaker voor wratten dan jongens en kinderen van niet-westerse immigranten. Huisartsen behandelen het overgrote
deel van de wratten door deze te bevriezen middels vloeibare stikstof. Van de meest
toegepaste therapien staat salicylzuur op de tweede plaats.
In hoofdstuk 6 worden de epidemiologie en het beleid van de huisarts met betrekking
tot dermatophytosis bij kinderen beschreven.
Dermatophytosis is een veel voorkomend schimmelinfectie van de huid bij kinderen.
Ofschoon de epidemiologie relatief weinig is opgehelderd, is de incidentie van dermatophytosis bij kinderen in sommige landen excessief gestegen in de afgelopen decennia.
Tussen 1987 en 2001 is de totale incidentie van dermatophytosis bij kinderen in de
huisartspraktijk gestegen. Zuigelingen (< 1 jaar), meisjes, kinderen op het platteland,
kinderen van niet-westerse immigranten consulteren vaker de huisarts voor dermatophytosis dan oudere kinderen, kinderen uit verstedelijkte gebieden en kinderen van
autochtone Nederlanders.
In het algemeen volgen huisartsen de behandelrichtlijnen bij de behandeling van dermatophytosis bij kinderen.
Samenvatting
In hoofdstuk 7 wordt de associatie tussen huidziekten, in het bijzonder huidinfecties,

en een ziekenhuisopname ten gevolge van sepsis of bacteraemie bij kinderen (017
jaar) gexploreerd. Sepsis of bacteraemia komt relatief weinig voor, maar gaat gepaard
met een hoge mortaliteit en/of ernstige complicaties. Er lijkt een causaal verband te
bestaan tussen huidziekten en een ziekehuisopname voor sepsis of een ernstige bacterile infectie.
Wij hebben de volgende hypothese getest: kinderen die opgenomen zijn geweest voor
sepsis of bacteraemie hebben vaker last van huidziekten vr de opname en bezoeken
dientengevolge de huisarts vaker voor een huidprobleem dan andere kinderen.
We vinden odds ratios van 3.4 (95% BI:[1.1 10.8], p = 0.03) voor huisarts consultaties
betreffende een huidziekte in cases vergeleken met een controlegroep uit de huisartspraktijk GP controles en 1.4 (95% BI:[0.5 3.9], p = 0.44) in cases vergeleken met
een controlegroep uit het ziekenhuis hospital controles. Kinderen jonger dan drie
maanden hebben een odds ratio (cases / GP controles) van 9.2 (95% BI: [0.81106.1], p
= 0.07) en 4.0 (95% BI: [0.67 23.9], p = 0.12) in cases versus hospital controles. Slechts
5% van de cases consulteren de huisarts voor een huidziekte vr hun opname.
119
Dankwoord
Het schrijven van een proefschrift is grotendeels een eenzame onderneming, doch ook
een proeve van samenwerking. Ofschoon de laatste loodjes het zwaarst wegen, ben ik
blij dat het einde in zicht is en met het schrijven van dit dankwoord begin ik dan echt
met de afronding van mijn proefschrift. Het schrijven van een proefschrift is niet altijd
makkelijk, maar gelukkig stond ik er niet alleen voor. Gedurende het hele traject waarin
ik aan dit proefschrift heb gewerkt, hebben vele mensen, dichtbij en op afstand, elk met
hun eigen kwaliteiten, meegewerkt, geholpen en ondersteuning geboden waardoor het
mogelijk werd dat dit proefschrift tot een goede afronding is gekomen. Gaarne wil ik
van de gelegenheid gebruik maken om deze personen te bedanken.
Om te beginnen gaat mijn dank uit naar mijn beide promotoren prof.dr. B.W. Koes en
prof.dr. F.G. Schellevis.
Beste Bart, bedankt voor je oprechte betrokkenheid en de positieve feedback die je
altijd gaf. Jouw commentaar bij artikelen ging altijd gepaard met complimenten, en
dat motiveert. Zelfs de meest slechte manuscripten wist jij te voorzien van positief
commentaar. Door je epidemiologische kwaliteiten kon je heel precies en helder beargumenteren om zaken anders aan te pakken. Ik heb daar veel van geleerd.
Beste Franois, ik dank jou voor jouw relativerende opmerkingen en inhoudelijke bijdragen aan dit proefschrift. Door je heldere en kritische commentaar op de tekst van
dit proefschrift heb ik heel wat bijgeleerd over het schrijfproces. Jouw methodologische
inbreng was onmisbaar want je doorzag altijd heel snel de valkuilen. Ook dank ik jou
voor de talloze reisjes die jij naar Rotterdam maakte om de voortgang van artikelen te
bespreken.
Dan mijn co-promotor en begeleider dr. J.C. van der Wouden. Beste Hans, je oprechte
betrokkenheid bij mij en mijn onderzoek is een stimulans geweest om dit proefschrift
tot een goed einde te brengen. Ik ben je zeer erkentelijk voor jouw onvermoeibare en
creatieve begeleiding. Je was altijd aanwezig en hulpvaardig. Je hebt niet alleen een
inhoudelijke bijdrage geleverd aan dit proefschrift, maar ook inspireerde je mij tijdens
dit onderzoek. Jouw methodologische en tekstuele inbreng hebben zeker de kwaliteit
van dit proefschrift verbeterd.
Verder dank ik alle huisartsen en patinten die hebben deelgenomen aan de Eerste
en Tweede Nationale Studie, want zonder hun bijdrage was dit proefschrift er niet
geweest.
Lisette van Suijlekom-Smit, kinderarts verbonden aan het Erasmus MC Rotterdam, en

Sander Koning, huisarts te Vlaardingen; op jullie heb ik altijd kunnen rekenen. Jullie
zijn vanaf het begin betrokken geweest bij de voortgang van het onderzoek en het tot
stand komen van de artikelen. Bedankt voor jullie heldere en nuttige commentaar op
de artikelen.
Michiel van der Linden, destijds projectleider van de module morbiditeit en collega op
de afdeling huisartsgeneeskunde, wil ik bedanken voor zijn bijdrage met betrekking tot
de data-analyse en het kritische commentaar op de artikelen.
Roos Bernsen was destijds statistica op de afdeling huisartsgeneeskunde. Beste Roos,
bedankt voor je statistische bijdragen en dat je altijd tijd voor mij vrij wilde maken om
vervolgens geduldig mijn vragen te beantwoorden en mijn statistische problemen op
te lossen.
Sten Willemsen, statisticus op de afdeling huisartsgeneeskunde wil ik onder meer be-
Dankwoord
danken voor het geduldig en eindeloos herhalen van de statistische analyses.
122
De kleine commissie leden, prof.dr. A.P. Oranje, prof.dr. B.H. Stricker en prof.dr. J.F.M
Metsemakers wil ik bedanken voor het lezen en het beoordelen van mijn proefschrift.
Verder wil ik iedereen van de afdeling huisartsgeneeskunde, de collega onderzoekers
en overige medewerkers, bedanken voor hun bijdrage aan de goede sfeer op de afdeling. Helaas zijn er teveel collegas en medewerkers om allemaal met naam te noemen
in dit dankwoord.
Miriam Montenij en Imraan Ali Mohammedamin, mijn paranimfen, bedankt dat jullie
mij tijdens en rondom de promotie terzijde willen staan. Ik ben er trots op dat jullie
naast mij staan!
Mijn familie en vrienden dank ik dat zij altijd begrip toonden als ik het druk had.
Lieve ma en pa, jullie zijn er altijd voor mij! Ik geloof niet dat woorden echt goed
kunnen beschrijven hoe bijzonder ik dat vind. Jullie onvoorwaardelijke liefde en steun
hebben mij het vertrouwen gegeven om mijn eigen weg te gaan in dit leven. Als ik ook
maar iets van jullie warme belangstelling, oprechte aandacht en zorg voor anderen heb
meegekregen dan hoop ik dat dat tot uiting mag komen in mijn werk als arts.
Tot slot mijn thuis. Lieve Carmen, zonder jouw liefde, steun, geduld, stimulatie en interesse was het nooit zover gekomen. Maar ook bedankt voor zoveel meer dan dat
Curriculum Vitae
Robbert SA Mohammedamin werd op 1 juni 1968 geboren te Paramaribo (Suriname).
Na het afronden van het voortgezet onderwijs begon hij de studie geneeskunde in 1989
aan de Erasmus Universiteit te Rotterdam en legde het artsexamen met goed gevolg af
in 1996.
Van 1996 tot 2001 werkte hij als arts-assistent niet in opleiding op diverse klinische
afdelingen te weten Urologie (ErasmusMC Rotterdam), Interne Geneeskunde (Oogziekenhuis Rotterdam), Cardio-thoracale chirurgie (LUMC Leiden) en Spoedeisende Hulp
(MCH Haaglanden).
Hij startte de huisartsopleiding in 2001 aan de Universiteit van Maastricht en liep zijn
eerstejaars stage te Venray (opleider H. Schraven). Hij liep zijn derdejaars stage te
Brielle (opleider B. Ponsioen) en rondde in 2003 de huisartsopleiding af aan het Erasmus MC te Rotterdam. Aansluitend begon hij aan zijn promotietraject. Van 2003 tot 2005
is hij verbonden geweest als huisarts-onderzoeker op de afdeling Huisartsgeneeskunde
van het Erasmus MC te Rotterdam waar hij aan de in dit proefschrift beschreven studies
heeft gewerkt. In juni 2005 behaalde hij het Master of Science diploma in de Klinische
Epidemiologie aan de Netherlands Institute for Health Sciences (NIHES).
In juli 2006, tijdens de Annual Scientific Meeting (ASM) van de Society for Academic
Primary Care (SAPC), te Keele in Engeland, werd zijn abstract gebaseerd op hoofdstuk
7 van dit proefschrift tot beste uitgeroepen en ontving hij de SAPC/EGPRN (European
General Practitioners Research Network) award.

Mohammedamin, Robbert Sifayed Ali

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Infectious Skin Diseases in Children in General Practice

Epidemiology and management

Robbert S.A. Mohammedamin

Infectieuze Huidziekten bij Kinderen in de Huisartspraktijk

Financial support by the Department of General Practice, Erasmus University Medical

Infectious Skin Diseases in Children in General Practice

Infectieuze Huidziekten bij Kinderen in de Huisartspraktijk

ter verkrijging van de graad van doctor aan de

Robbert Sifayed Ali Mohammedamin

Prof.dr. B.W. Koes

Prof.dr. F.G. Schellevis

Prof.dr. A.P. Oranje

Prof.dr. B.H. Stricker

Prof.dr. J.F.M. Metsemakers

Dr. J.C. van der Wouden

Voor mijn ouders

Increasing incidence of skin disorders in children? A comparison

between 1987 and 2001

Impetigo: incidence and management in Dutch general practice

in 1987 and 2001. Results from two national surveys

Incidence and management of acne in children and adolescents

in Dutch general practice. A comparison between 1987 and 2001

Incidence and management of warts in children in Dutch

general practice. A comparison between 1987 and 2001

Incidence and management of dermatophytosis in children in

Dutch general practice. A comparison between 1987 and 2001

Association between skin diseases and severe bacterial

infections in children: case-control study

Summary and general discussion

Manuscripts based on studies described in this thesis

Relevance of this study

dermatological expertise might be needed and implemented in the vocational training

The role of general practice in childrens health care

ment policies in accordance with the national guidelines and/or evidence-based

knowledge on the effectiveness of different therapies?

Increasing incidence of skin

Increasing incidence of skin disorders

Increasing incidence of skin disorders

All episodes of skin disease

Increasing incidence of skin disorders

Natives & Western

Localized skin infections

Herpes Simplex skin/lip

Contact dermatitis/other eczema 1882

Other benign neoplasms

Increasing incidence of skin disorders

Human / animal bite

Foreign body in skin

Other injuries to skin

Ingrown toenail/other diseases

Other symptoms/complaints skin 207

Other diseases of skin/

ICPC = International Classification of Primary Care

Increasing incidence of skin disorders

Julian CG. Dermatology in general practice. Br J Dermatol 1999; 141: 518520.

Impetigo: incidence and

compared to winter, urban areas and northern region respectively. Socio-economic

status was not associated with the incidence rate.

Impetigo: incidence and management