1008 Zhao et al.

/ J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2011 12(12):1008-1015

Journal of Zhejiang University-SCIENCE B (Biomedicine & Biotechnology)

ISSN 1673-1581 (Print); ISSN 1862-1783 (Online)
www.zju.edu.cn/jzus; www.springerlink.com
E-mail: [email protected]

Facial dermatosis associated with Demodex: a case-control study*

Ya-e ZHAO†1, Yan PENG1,2, Xiang-lan WANG3, Li-ping WU1,4,

Mei WANG3, Hu-ling YAN3, Sheng-xiang XIAO3
(1Department of Immunology and Pathogen Biology, Xi’an Jiaotong University College of Medicine, Xi’an 710061, China)
(2Xi’an Center for Disease Control and Prevention, Xi’an 710054, China)
3
( Department of Dermatology, the Second Affiliated Hospital, Xi’an Jiaotong University College of Medicine, Xi’an 710004, China)
(4Department of Clinical Laboratory, Chengdu First People’s Hospital, Chengdu 610041, China)
†
E-mail: [email protected]
Received Aug. 29, 2011; Revision accepted Sept. 29, 2011; Crosschecked Nov. 18, 2011

Abstract: Demodex has been considered to be related with multiple skin disorders, but controversy persists. In this
case-control study, a survey was conducted with 860 dermatosis patients aged 12 to 84 years in Xi’an, China to
identify the association between facial dermatosis and Demodex. Amongst the patients, 539 suffered from facial
dermatosis and 321 suffered from non-facial dermatosis. Demodex mites were sampled and examined using the skin
pressurization method. Multivariate regression analysis was applied to analyze the association between facial der-
matosis and Demodex infestation, and to identify the risk factors of Demodex infestation. The results showed that total
detection rate of Demodex was 43.0%. Patients aged above 30 years had higher odds of Demodex infestation than
those under 30 years. Compared to patients with neutral skin, patients with mixed, oily, or dry skin were more likely to
be infested with Demodex (odds ratios (ORs) were 2.5, 2.4, and 1.6, respectively). Moreover, Demodex infestation
was found to be statistically associated with rosacea (OR=8.1), steroid-induced dermatitis (OR=2.7), seborrheic
dermatitis (OR=2.2), and primary irritation dermatitis (OR=2.1). In particular, ORs calculated from the severe infesta-
2
tion (≥5 mites/cm ) rate were significantly higher than those of the total rate. Therefore, we concluded that Demodex is
associated with rosacea, steroid-induced dermatitis, seborrheic dermatitis, and primary irritation dermatitis. The rate of
severe infestation is found to be more correlated with various dermatosis than the total infestation rate. The risk factors
of Demodex infestation, age, and skin types were identified. Our study also suggested that good hygiene practice
might reduce the chances of demodicosis and Demodex infestation.

Key words: Facial dermatosis, Demodex infestation, Association, Case-control study, Age
doi:10.1631/jzus.B1100179 Document code: A CLC number: R384.4; R757.3

1 Introduction while D.b. exists principally in depth of sebaceous

and meibomian glands. These two Demodex species
The Demodex mites belong to the family have been retrieved from almost every area of human
Demodicidae (Acari: Cheyletoidea). Demodex skin but have a predilection for the face. The mites
folliculorum (D.f.) and Demodex brevis (D.b.) are two can be found in any age groups except newborns who
Demodex mites of permanent parasites found on are presumably infested soon after birth by direct
humans (Desch and Nutting, 1972). D.f. occupies the contact (Bonnar et al., 1991). The mite population
hair follicles above the level of the sebaceous glands, increases with host age, and in the adult population,
these two Demodex species parasitize the normal skin
with a prevalence of 100% and a usual density
<5 mites/cm2. Demodex mites are usually considered
*
Project supported by the National Natural Science Foundation of
China (No. 30872199), and the Natural Science Foundation of
Shaanxi Province (No. 2006C247), China to play a pathogenic role when present in an excessive
© Zhejiang University and Springer-Verlag Berlin Heidelberg 2011 number or penetrating into the dermis (Ayres and
 Zhao et al. / J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2011 12(12):1008-1015 1009

Ayres, 1961; Ecker and Winkelmann, 1979; Bonnar and pustules, nodus and scar. Based on pathogenesis
et al., 1993; Forton and Seys, 1993; Erbagci and progress, erythematotelangiectatic rosacea, papu-
Ozgoztasi, 1998). They have been implicated in the lopustular rosacea, and phymatous rosacea appear
occurrence of a wide range of clinical features, subsequently. In this study, a total of 91 cases of
including pityriasis folliculorum (Ayres and Ayres, rosacea were diagnosed, with 9 erythematote-
1961), papulopustular and granulomatous rosacea langiectatic rosacea, 65 papulopustular rosacea, and
(Bonnar et al., 1993; Forton and Seys, 1993), 17 phymatous rosacea.
inflammatory papule (Seifert, 1978), folliculitis Steroid-induced dermatitis (SID), a dermatosis
(Purcell et al., 1986), seborrheic dermatitis with obvious “anti-jump phenomenon”, is caused by
(Karincaoglu et al., 2009), perioral dermatitis long-time inappropriate external use of hormone
(Dolenc-Voljc et al., 2005), and blepharitis (Post and drugs (such as cortisone and prednisone). A total of
Juhlin, 1963; Zhao et al., 2011a), although much 26 cases of SID were diagnosed.
controversy persists (Bonnar et al., 1993; Forton and Seborrheic dermatitis (Seb D) is a common con-
Seys, 1993; Forton et al., 2005; Hsu et al., 2009). A dition with uncertain etiology that makes the skin
definitive diagnosis of demodicosis requires a greasy, scaly, and flaky. A total of 153 cases of Seb D
compatible clinical picture and the presence of more were diagnosed.
than 5 mites/cm2 (Forton and Seys, 1993). Facial dermatitis is a facial dermatosis charac-
In order to confirm the association of various terized by red, itchy, and blistering skin. It consists of
facial dermatosis with Demodex mites, we investigated two types: primary irritation dermatitis (PID) and
860 dermatosis patients in Xi’an, China by a case- sensitization dermatitis (SD). We identified 106 cases
control study and conducted multivariate logistic of PID and 34 cases of SD.
regression analysis. Acne vulgaris (AV) is a chronic inflammation of
unknown etiology, predilecting young adults. It is
characterized by skin with comedones, papules, pus-
2 Materials and methods tules, nodules, cysts, etc., mostly affecting follicles
and sebaceous glands. A total of 129 cases of AV
2.1 Study population
were diagnosed.
In the study, final diagnoses of the 860 outpa-
2.3 Questionnaire and Demodex examination
tients aged 12 to 84 years were made by four derma-
tologists who had clinical experience for 10‒35 years The questionnaire covered information about
in Department of Dermatology at the Second Affili- age, gender, family address, telephone number, resi-
ated Hospital of Xi’an Jiaotong University College of dence pattern, hygiene practices (sharing of sanitary
Medicine between October 2008 and December 2009. ware, frequency of face-washing every day, and the
There were 539 patients with facial dermatosis (pa- use of facial cleanser), eating habits (alcohol,
tient group) and 321 with non-facial dermatosis (NFD, sweetmeat, spicy food (such as hot pepper, zingiber)
control group) included. consumptions), skin types (neutral, dry, oily, or
mixed), and the dermatosis (rosacea, SID, Seb D, PID,
2.2 Diagnosis of dermatosis
AV, SD, and NFD) considered in this study. All the
Pathogenicity of Demodex has been under dis- participants signed the written consent form. Ethical
pute for a long time and few demodicosis diagnoses permission was not required for this study because the
have been made by a dermatologist at our clinic. In skin pressurization method was a non-invasive sam-
this study, we investigated the correlation between pling technique routinely used in etiological agent.
each of the following six kinds of facial dermatosis Skin pressurization method was employed in the
probably and Demodex. process of Demodex examination for all patients. It is
Rosacea is a common skin condition of uncertain convenient, quick, and is widely applied in the fast
etiology, which usually affects the center of face diagnosis of outpatients in Mainland China. It was
among the middle-aged, causing transient or perma- conducted with the following steps. First, squeeze the
nent facial erythema, telangiectasia, edema, papules left nasolabial fold and nasal ala (about 1 cm2) with
1010 Zhao et al. / J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2011 12(12):1008-1015

the thumb to get some sebum. Second, place the se- analysis revealed that after controlling for the co-
bum on the slide and add a drop of liquid paraffin. variates (Table 1), three variables (gender, residence
Finally, place the cover glass and examine the sample pattern, eating habit) were found to be uncorrelated
with a microscope (4×10). A positive diagnosis was with Demodex infestation, whereas each of the other
made only after observing the Demodex mites (any of four variables (age, hygiene practice, skin type, and
the developmental stages: egg, larva, nymph, adult of facial dermatosis) was still correlated with Demodex
D.f. or D.b.) under microscopic magnification. Based infestation. In particular, patients aged above 30 years
on the limit value found by standardized skin surface had higher odds of Demodex infestation than those
biopsy (n<5 mites/cm2) (Forton and Seys, 1993), we under 30 years. Compared to patients with neutral
decided to apply the same limit value for our sam- skin type, patients with mixed skin type were more
pling method. The Demodex density was classified as prone to Demodex infestation (odds ratio (OR)=2.5),
severe (≥5 mites/cm2) and mild (1‒4 mites/cm2). followed by those with oily skin (OR=2.4) and then
dry skin (OR=1.6).
2.4 Statistical analysis
Table 1 also demonstrated that Demodex infes-
The focus of the study was the occurrence of tation was statistically associated with the develop-
Demodex infestation. The Demodex infestation rate ments of rosacea (OR=8.1), SID (OR=2.7), Seb D
was calculated by sociodemographic characteristics (OR=2.2), PID (OR=2.1), and AV (OR=1.5), whereas
of patients. χ2 test was applied to compare the De- no significant statistical correlation was found be-
modex infestation rates of cases and controls. Seven tween SD and Demodex infestation (OR=0.7).
independent variables (age, gender, residence, eating
3.3 Association between Demodex infestation and
habits, hygienic practice, skin type, and dermatosis)
age of patients
were included in the logistic regression model to
identify significant correlates of Demodex infestation Fig. 1 showed that Demodex infestation rates
and to calculate odds ratios (ORs) and P values, with increased with age among the 12‒30 years old pa-
a 0.05 significant level. Correlation between Demodex tients and remained stable amongst the older patients.
density and the age of patients was shown by a scat- 100
terplot. Associations between the rate of severe De-
Infestation rate/infectiosity constituent ratio (%)

90
modex infestation and each of the six skin diseases
80
(rosacea, SID, Seb D, PID, AV, SD) were estimated. y1=0.0269X2−2.5184X+122.41
70 R2=0.8913
We also estimated the correlation between the rate of
severe Demodex infestation and age amongst the AV 60
Y=−0.0092X2+1.0959X+17.281
patients. 50 R2=0.776

40

30
3 Results
20
y2=−0.0269X2+2.5184X−22.409
3.1 General information 10 R2=0.8913

In this study, 860 dermatosis patients completed 0

10 20 30 40 50 60 70 80
the questionnaire effectively. The total infestation
Age (year)
rate of Demodex mites was 43.0% (370/860). Con-
stituent ratio of D.f. infestation was the highest Fig. 1 Scatterplot of Demodex infestation and age of patients
(52.4%, 194/370), followed by the infestation rate of X [age group (median) (year)]: 12–20 (15), 21–30 (25), 31–40
D.b. (26.5%, 98/370), and the mixed infestation rate (35), 41–50 (45), 51–60 (55), 61–84 (72); Y [infestation rate
was the lowest (21.1%, 78/370). The three constituent (%), ♦]: 31.5 (29/92), 35.9 (94/262), 50.7 (114/225), 47.6
(79/166), 45.3 (34/75), 50.0 (20/40); y1 [mild density constituent
ratios were significantly different (χ2＝93.5, P<0.01). ratio (%), ■]: 93.1 (27/29), 73.4 (69/94), 63.2 (72/114), 69.6
(55/79), 64.7 (22/34), 80.0 (16/20); y2 [severe density constitu-
3.2 Multivariate logistic regression analysis
ent ratio (%), ▲]: 6.9 (2/29), 26.6 (25/94), 36.8 (42/114), 30.4
Results of multivariate logistic regression (24/79), 35.3 (12/34), 20.0 (4/20)
 Zhao et al. / J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2011 12(12):1008-1015 1011

Table 1 Results of logistic regression analysis of Demodex infestation (n=860)

Proportion Infestation rate
Characteristics Description Frequency OR (95% CI) P-value
(%) (%)
Age (year) 12–20 92 10.7 31.5
21–30 262 30.5 35.9 1.2 (0.7–2.0) 0.450
31–40 225 26.2 50.7 2.2 (1.3–3.7) 0.002
41–50 166 19.3 47.6 2.0 (1.2–3.4) 0.012
51–60 75 8.7 45.3 1.8 (1.0–3.4) 0.067
61–84 40 4.6 50.0 2.2 (1.0–4.6) 0.043
Gender Male 236 27.4 44.5
Female 624 72.6 42.5 0.9 (0.7–1.2) 0.593
Residence Urban 836 97.2 43.1
Rural 24 2.8 41.7 1.1 (0. 5–2.4) 0.892
Eating habit Drinker No 171 19.9 43.9
Yes 689 80.1 42.8 1.0 (0.7–1.5) 0.805
Spicy diet No 555 64.5 42.5
Yes 305 35.5 43.9 0.9 (0.7–1.3) 0.689
Sweetmeat No 416 48.4 44.2
Yes 444 51.6 41.9 1.1 (0.8–1.4) 0.489
Hygienic With private sanitary ware 553 64.3 39.4
practice Without private sanitary ware 307 35.7 49.5 1.5 (1.1–2.0) 0.004
Washing face once a day 73 8.5 56.2
Washing face twice a day 666 77.4 43.8 0.6 (0.4–1.0) 0.046
Washing face three times a day 121 14.1 30.6 0.3 (0.2–0.6) 0.001
Facial cleanser user 228 26.5 47.8
Otherwise 632 73.5 41.3 0.8 (0.6–1.0) 0.004
Skin type Neutral 194 22.6 28.4
Dry 118 13.7 38.1 1.6 (1.0–2.5) 0.000
Oily 254 29.5 48.8 2.4 (1.6–3.6) 0.000
Mixed 294 34.2 49.7 2.5 (1.7–3.7) 0.000
Dermatosis NFD 321 37.3 30.5
Rosacea 91 10.6 78.0 8.1 (4.7–14.0) 0.000
SID 26 3.0 53.9 2.7 (1.2–6.0) 0.018
Seb D 153 17.8 49.7 2.2 (1.5–3.3) 0.000
PID 106 12.3 48.1 2.1 (1.3–3.3) 0.001
AV 129 15.0 40.3 1.5 (1.0–2.3) 0.047
SD 34 4.0 23.5 0.7 (0.3–1.6) 0.398

Although we found no significant differences be-

3.5 Relationship between Demodex infestation
tween the four subgroups amongst the patients aged
and age among acne patients
31 to 84 years, the average infestation rates between
the patients aged 12‒30 years and 31‒84 years were As shown in Table 3, both the total infestation
significantly different. Similarly, it was shown that rates and the severe infestation rates were higher
Demodex density changed in the same direction as the amongst the 31‒84 year-old acne patients than
infestation rates, except that the density decreased amongst the 12‒30 year-old ones. Acne patients had a
with age amongst patients older than 60 years. higher infestation rate than patients with non-facial
dermatosis in both age groups. Regarding severe
3.4 Correlation between severe Demodex infesta-
infestation, the rates were not significantly different
tion and dermatosis
between the acne patients and ones with non-facial
As shown in Table 2, the severe infestation dermatosis amongst those aged 12‒30 years, whereas
(≥5 mites/cm2) was statistically correlated with rosacea, ORs of older (31‒84 years old) acne patients and the
SID, Seb D, and PID, while not with SD and AV. control patients were statistically different.
1012 Zhao et al. / J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2011 12(12):1008-1015

2
Table 2 Relevance between severe Demodex infestation (≥5 mites/cm ) and various dermatoses
Dermatosis Frequency Infestation rate (%) χ2 P OR ( 95% CI)
NFD 321 5.0
Rosacea 91 38.5 73.3 0.000 11.9 (6.2–23.0)
SID 26 19.2 6.1* 0.012 4.5 (1.5–13.6)
Seb D 153 16.3 16.9 0.000 3.7 (1.9–7.2)
PID 106 13.2 8.2 0.004 2.9 (1.4–6.2)
AV 129 9.3 2.9 0.086 2.0 (0.9–4.3)
SD 34 5.9 0.0* 1.000 1.2 (0.3–5.4)
Patients aged 12–84 years. * Continuity correction χ2 value

Table 3 Relationship between Demodex density/infestation rate and age among acne patients
Demodex density Age (year) Dermatosis Frequency Infestation rate (%) χ2 P OR (95% CI)
Total (≥1 mite/cm2) 12–30 NFD 131 20.6
AV 110 35.5 6.6 0.010 2.1 (1.2–3.8)
31–84 NFD 190 37.4
AV 19 68.4 6.9 0.008 3.6 (1.3–10.0)
Severe (≥5 mites/cm2) 12–30 NFD 131 0.8
AV 110 5.5 3.2* 0.076 7.5 (0.9–63.3)
31–84 NFD 190 7.9
AV 19 31.6 8.3* 0.004 5.4 (1.8–16.2)
* 2
Continuity correction χ value

4 Discussion For instance, pityriasis folliculorum, the most fre-

quent demodicosis (Forton et al., 2005), is rarely
Demodex infestation can cause indistinguishable diagnosed in our hospital. The severe infestation
multiple skin disorders with white follicular scales, could make great contribution to demodicosis. Al-
papules, and pustules as their frequent clinical picture though Forton and Seys (1993) proposed that the mite
(Ayres, 1930; Ayres and Ayres, 1961; Seifert, 1978). density of ≥5 mites/cm2 can be a diagnostic criterion,
Yet it is still under debate whether Demodex is the Erbagci and Ozgoztasi (1998) suggested that a certain
cause of many kinds of skin diseases (Bonnar et al., density might not be an appropriate criterion in the
1993; Forton and Seys, 1993; Forton et al., 2005; Hsu diagnosis of demodicosis. Nevertheless, in our study,
et al., 2009). Based on the results of the present study, the correlation between severe infestation (≥5 mites/cm2)
we conclude that rosacea, SID, Seb D, and PID are rate and various kinds of dermatosis was obviously
significantly associated with Demodex infestation, higher than that between the total infestation
while SD is not. Until now, the dispute mainly fo- (≥1 mite/cm2) rate and the dermatosis (OR values
cuses on the contradiction of high Demodex infesta- were 11.9 and 8.1 in rosacea, 4.5 and 2.7 in SID, 3.7
tion rate in the population (few studies reported 100%) and 2.2 in Seb D, 2.9 and 2.1 in PID, respectively).
(Forton and Seys, 1993) and the low incidence of Second, due to the Chinese dermatologists’ denial of
demodicosis. Some studies even showed that a few Demodex pathogenicity, probably the demodicoses
patients with excessive Demodex had no obvious are often misdiagnosed or confused with other facial
clinical symptoms (Zhang et al., 2008). Three factors dermatoses in our clinical practice, thus leading to the
might explain the low incidence of demodicosis. First, nosological question of the demodicoses. One possi-
the density of Demodex infestation is important. The ble interpretation is that demodicosis is included in
mild cases, the majority of the infested, tend to ignore such related dermatosis as rosacea, SID, Seb D, PID,
the symptoms and hence seldom seek medical advice. etc. The other one is that the same patient can have
 Zhao et al. / J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2011 12(12):1008-1015 1013

two pathologies at the same time. Thirdly, the sus- non-facial dermatosis (OR=7.5, 95% CI 0.9–63.3;
ceptibility of hosts could affect the effect of Demodex P>0.05). After the 12‒30 year-old patients with ado-
infestation. Akilov and Mumcuoglu (2003) have lescent acne and non-facial dermatosis were excluded,
evidenced that people with the Cw2 and Cw4 haplo- the severe infestation rate of AV patients became
types are more susceptible to demodicosis compared significantly higher than that of non-facial dermatosis
to people without the Cw2 and Cw4 haplotypes. In in the 31‒84 years age group (OR=5.4, 95% CI
particular, the risk of developing clinical symptoms of 1.8–16.2; P<0.05). Therefore, any conclusions about
demodicosis is 5.0 times higher for people with the the association between Demodex infestation and AV
Cw2 haplotype and 3.1 times higher for those with the require further study.
Cw4 haplotype, whereas individuals who have the In addition, we found that Demodex infestation
human leucocyte antigen (HLA) A2 phenotype are could be affected by age, skin type, and hygienic
2.9 times more resistant to demodicosis. practice. The infestation rate and the density of De-
The role of Demodex mites as risk factors for modex change with age. In our study, the Demodex
rosacea has been confirmed recently (OR=7.6) (Zhao detection rate increased along with age amongst the
et al., 2010). The conclusion was drawn from 48 12‒30 year-old patients, which was in agreement with
selected studies (9 in English and 39 in Chinese) the study of 102 students aged 18‒27 years reported
conducted in 10 countries by meta synthetic quanti- by Okyay et al. (2006) and 2 248 medical students
tative study, which involved 28 527 participants aged 19‒24 reported by Hu and Wang (2001). How-
(4 307 rosacea patients and 24 220 controls). That ever, the high Demodex detection rate remained stable
finding was confirmed by the present study (OR=8.1). in the 31‒84 year-old patients, which differed from
The hypothesis that SID and Seb D were associated the particularly big increase in the infestation rate of
with Demodex mites has not been confirmed at pre- both Demodex species during the hosts’ fifth and sixth
sent, but our results were consistent with those of decades reported by Aylesworth and Vance (1982).
Dolenc-Voljc et al. (2005) and Karincaoglu et al. At the same time, the Demodex density kept a high
(2008; 2009). level amongst the 30‒60 year-old patients, signifi-
It is worth clarifying that although English pa- cantly higher than that amongst the 12‒30 year-old
pers about the association between Demodex infesta- ones and those older than 60 (Fig. 1). This might be
tion and AV are very few and mostly give negative attributed to the development of sebum secretion,
conclusions (Baysal et al., 1997; Okyay et al., 2006), which is more mature at the age of 30‒60 years than at
a great number of Chinese papers have reported a 12‒30 years, and less functional above 60 years.
positive association between Demodex infestation and Skin type is closely related with Demodex in-
the development of AV (Yang et al., 2006; Ma et al., festation. Our study revealed that the detection rate of
2009; Wang et al., 2010; Zhao et al., 2011b). More- mites in dermatosis patients with oily or mixed skin
over, effective acaricidal treatments have also sup- was higher than that in patients with neutral or dry
plied indirect proof of a causal relationship between skin. This corresponded to the conclusions of some
Demodex infestation and AV (Yang et al., 2006; Ma previous studies (Cao et al., 2009; Peng et al., 2009).
et al., 2009). In this study, a significant association A possible reason is that Demodex mainly consumes
between Demodex infestation and AV was estab- living cells in follicles and sebaceous glands. The
lished according to the total infestation rate (OR=1.5, destruction of massive epithelial cells could lead to
95% CI 1.0–2.3; P<0.05), whereas a weaker correla- compensatory hyperplasia and secretion enhancement.
tion was obtained according to the severe infestation To make it worse, the movement of chelae and claws
rate (OR=2.0, 95% CI 0.9–4.3; P>0.05). The weaker of the mites in the pilosebaceous unit would stimulate
correlation might be a result of statistical bias, be- sebaceous follicles and enhance the secretion. Con-
cause severe infestation of Demodex is rather rare versely, the detection rate of mites in dermatosis pa-
amongst the 12‒30 year-old patients in our study. For tients with dry skin was found to be higher than that in
the younger age group (12‒30 years old), we found no patients with neutral skin in our study. The reason
significant difference in the rate of severe infestation might be that the dry skin is only a false sensation
between the group with AV and the group with (Forton et al., 2005), which is a result of the
1014 Zhao et al. / J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2011 12(12):1008-1015

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Baysal, V., Aydemir, M., Yorgancigil, B., Yildirim, M., 1997.
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