www.najms.org North American Journal of Medical Sciences 2010 October, Volume 2. No. 10.

Original Article OPEN ACCESS

Pap smear screening in the primary health care setting:

A study from Turkey
Hande Celik Mehmetoglu, Ganime Sadikoglu, Alis Ozcakir, Nazan Bilgel

Uludag University, Department of Family Medicine, Bursa, Republic of Turkey.

Citation: Mehmetoglu HC, Sadikoglu G, Ozcakir A, Bilgel N. Pap smear screening in the primary health care setting: A
study from Turkey. North Am J Med Sci 2010; 2: 468-472.
Doi: 10.4297/najms.2010.2468
Availability: www.najms.org
ISSN: 1947 – 2714

Abstract
Background: Cervical cancer is one of the ten most frequent cancers in Turkey. It is well known that cervical cancer
morbidity and mortality could be significantly reduced with an active cervical smear screening (Pap smear) program. Aims:
The aims of this study were: 1) to evaluate the knowledge and attitudes of women about cervical smear testing; 2) to
establish a cervical smear screening program and to evaluate the cervical cytological abnormalities that were found; 3) to
determine the applicability, limitations and effectiveness of this screening in a primary health care unit. Patients and
Methods: A total of 332 married women were included in our study. We collected data concerning socio-demographic and
fertility characteristics, and knowledge about Pap smear testing was determined through printed questionnaires. A
gynecological examination and Pap smear screening was performed on every woman in our study group. Results: Over
ninety percent of our study group had never heard of and had not undergone Pap smear screening before. Of the 332
smears evaluated, 328 (98.8%) were accepted as normal, whereas epithelial cell anomalies were seen in 4 (1.2%), infection
in 59 (17.7%), and reactive cell differences in 223 (67.2%) of the smears. Conclusions: The frequency of epithelial cell
anomalies in our study group was less than the frequencies reported from Western countries. Knowledge regarding cervical
cancer and Pap smear screening was very low. Pap smears can be easily taken and evaluated through a chain built between
the primary health care unit and laboratory, and this kind of screening intervention is easily accepted by the population
served.

Keywords: Cervical smear, cervical intraepithelial lesion, cervical cancer screening.

Correspondence to: Nazan Bilgel M.D., Professor of Public Health, Department of Family Medicine, Uludag University
Faculty of Medicine, 16059 Bursa, Turkey. Tel.: & Fax: +902244428599, Email: [email protected]

Bulgaria are the EU countries with the highest cervical

Introduction cancer incidences and death rates [6] .
Cervical cancer is the seventh cancer in overall frequency,
but the second most common cancer among women
According to official statistics the annual incidence of
worldwide. An estimated 493,000 new cases and 274,000
cervical cancer in the Republic of Turkey is 8 per 100,000
deaths occurred from cervical cancer in the year 2002 [1,
[1]. In the year 2002, 4.9% of all cancers and 4.1% of all
2]. In general terms, cervical cancer is much more cancer deaths among women were due to cervical cancer
common in developing countries, where 83% of cases
[1]. In Turkey, cervical cancer is in the 8th most frequent
occur and where cervical cancer accounts for 15% of
cause of mortality and morbidity due to neoplasia in
female cancers, with a risk before age 65 of 1.5%. In
women. In the year 2007 the Ministry of Health of
developed countries, cervical cancer accounts for only
Turkey announced a cervical screening program (Pap
3.6% of new cancers, with a cumulative risk (0 to 64) of
smear testing) which will be integrated into routine
0.8% [3-5]. The estimated burden of neoplasia of the primary health care services. The 6 key strategies of this
uterine cervix in the 27 EU member states sums up to prevention program for cervical cancer include the
34,300 cases and 16,200 deaths. Romania, Lithuania and
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following: reaching a significant proportion of women in with a special endocervical brush. During the examination
their 30s and 40s; using locally understood messages to disposable speculums were used. All of the vaginal
increase the awareness of the disease; motivating women examinations were performed and all of the smears were
to get tested at once; making outpatient treatment widely taken by the same medical doctor who was trained for this
available; arranging appropriate follow-up care; and procedure before the study. Smears were fixed with
evaluating the impact of the program on health outcomes. ethanol and sent to the laboratory at the end of every
working day. The laboratory was accredited for cytological
This program has not begun yet, but training and testing, and evaluations of the smears were made by a
education of the primary health care personnel, logistic pathologist.
support of the primary health care centers for Pap smear
testing, and arrangements for the necessary follow-up Cytologic tests
procedures are proceeding. We hope that in the near future The conventional Pap smear test was used for cytology.
Pap smear testing will be a routine procedure throughout The Pap smear has been the method of choice for cervical
the primary health care system in the whole country. cancer screening since the 1950s, proving valuable for
mass screening and enabling detection of lesions early
The objectives of our study were as follows: 1) to evaluate enough for effective treatment [7]. The Pap smear has
the knowledge and attitudes of women about cervical some limitations, however. The most important are its
smear testing; 2) to establish a smear screening program limited sensitivity, which is between 47-62%, and the
and to evaluate the cervical cytological abnormalities subjective interpretation of the results [7]. On the other
found; and 3) to determine the applicability, limitations hand, Pap smear testing also has strengths, such as wide
and effectiveness of screening in a family medicine clinic. acceptance, meeting most of the criteria for a good
screening test in settings with adequate resources,
Patients and Methods obtaining a permanent record of the test in the form of a
Study participants slide, and having a high specificity of 60-95% [7].
The study group included 332 married women who visited Evaluation of the cervical cells was done using the
the Family Medicine Clinic in Bursa, Turkey . This clinic Bethesda System 2001 as follows:
is a training center for medical students and serves as an
outreach primary health care unit to a population of 10,000. 1) Negative for intraepithelial lesion or malignancy
Women who attended the clinic during a period of six a) Organisms
months for various reasons were asked to participate to our • Trichomonas vaginalis
study. Married women (currently or ever married), women • Fungal organisms morphologically consistent
without a hysterectomy, women without a history of any with Candida spp.
type of cancer, women who were not pregnant or who did • Shift in flora suggestive of bacterial vaginosis
not give birth recently were recruited. All the women were • Bacteria morphologically consistent with
informed about the study and were asked to give their Actinomyces spp.
written consent. During the study period 443 women • Cellular changes consistent with Herpes
attended the clinic, of whom 27 were never married, 15 simplex virus.
were pregnant, 9 gave birth recently, 2 had a history of b) Other non-neoplastic findings
cancer and 3 had had a hysterectomy. Thirty-eight women • Reactive cellular changes
did not want to participate in the study. For these reasons a • Atrophy
total of 94 women were excluded from the study. The
study was approved by the ethical committee of Uludag 2) Epithelial cell abnormalities
University. a) Squamous cell
• Atypical squamous cells
Study instruments • Of undetermined significance
In the first phase of the study, a questionnaire prepared by (ASC-US)
the authors was used to determine the women’s • Can not exclude HSIL (ASC-H)
socio-demographic and fertility characteristics, and the • Low grade squamous intraepithelial lesion
knowledge of the women regarding Pap smear testing. A (LSIL) encompassing: human papilloma
total of 349 women answered the questionnaire. After virus (HPV)/mild dysplasia/CIN 1
the questionnaire was completed, women were invited to • High grade squamous intraepithelial lesion
the family medicine clinic on a given date for Pap smear (HSIL) encompassing: moderate and severe
testing at the proper time of their menstrual cycle. The dysplasia, CIS/CIN 2 and CIN3 with
women were advised not to take a vaginal shower, have features suspicious for invasion (if invasion
sexual intercourse, or use a tampon, gel or vaginal cream is suspected)
within 48 hours before coming to the clinic. Seventeen • Squamous cell carcinoma
women did not come to their appointment, and were b) Glandular cell
excluded from the study. The participation rate was 95.1%.
• Atypical
In the second phase of the study, after a vaginal
• Endocervical adenocarcinoma in situ
examination, cervical smears were taken from 332 women
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• Adenocarcinoma examination are shown in Table 2.

3) Other malignant neoplasms Of the 332 Pap smears, 9.1% were found to be normal,
while 17.7% were evaluated as infection, 4.8% as atrophy,
Statistical analyses 67.2% showed reactive cellular changes and 1.2% as
Socio-demographic data obtained in the first phase of the atypical squamous cells. Details of the Pap smear results
study and Pap smear results were recorded and statistical are shown in Table 3.
analyses were made with the SPSS V.11.0 program (SPSS
Inc., Chicago ILL). Frequency distributions, descriptive Table 1 Socio-demographic and fertility characteristics of the
statistics and chi-square tests were calculated. A p value participants
<0.05 was considered significant. Data are reported as Mean ± Standard Deviation
mean values ± standard deviation. Age (years) 38.0 ± 9.7
Age of first marriage (years) 19.3 ± 3.0
Results Number of sexual partners 1.0 ± 0.2
Socio-demographic and fertility characteristics: Age of menarche (years) 13.5 ± 1.4
The mean age of the women in the study group was 38.0 ± Number of pregnancies 3.4 ± 2.0
9.7 years. Most of the participants (96.4%) reported that Number of live births 2.5 ± 1.4
they had one sexual partner during their lifetime, while Number of abortions 0.9 ± 1.2
3.6% reported that they had two partners. Their Number of living children 2.3 ± 1.2
educational attainments were as follows: 19.6% illiterate,
64.2% primary school, 14.7% high school and 1.5%
Table 2 Vaginal examination results
university graduated. Most of the participants (93.7%)
Number of cases %
were housewives.
Normal 98 29.5
About 2/3 of the women reported that they had regular Erosion 116 35.0
menses, while 19% reported they had irregular menses, Ectropion 19 5.7
and 14.8% reported that they were in menopause. The Nabothian cysts 11 3.3
mean number of pregnancies for the women in the study Cervical Polyps 5 1.5
group was 3.4 ± 2.0, but 4.5% of the study group had Hyperemia 83 25.0
never had a pregnancy. Twenty-four percent of the
Total 332 100.0
participants said that they were not using any
contraceptive method currently, while 37.3% were using a
modern method and 38.7% a traditional method. The most Table 3 Pap smear results
commonly used contraceptive method was CI (coitus Number of cases %
interruptus) (38.3%), followed by IUD (intrauterine device) Normal 30 9.1
(16.3%), condom (9.6%) and sterilization (5.4%). Infection 59 17.7
Trichomonas 2 0.6
Most women reported they had never smoked (73.5%), Vaginosis
whereas 20.2% had smoked irregularly and 6.3% had quit Candidiasis 20 6.0
smoking. Seventy-seven percent of participants reported Bacterial 35 10.5
no familial history of any type of cancer. Vaginosis
Actinomyces 2 0.6
The percent of the participants who had never heard of Atrophy 16 4.8
Pap smear screening and had never undergone testing was Reactive cellular changes 223 67.2
90.7%. Thirty-one women had one previous Pap smear
Atypical squamous cells 4 1.2
screening. The reported results of the previous Pap smear
screenings were as follows: normal (13); infection (15); HSIL 2 0.6
malignancy (1); unknown (2). The socio-demographic LSIL 2 0.6
and fertility characteristics of the study group are shown in Total 332 100.0
Table 1. HSIL: High grade squamous intraepithelial lesion, LSIL: Low
grade squamous intraepithelial lesion.
Vaginal examination and Pap smear
Before the vaginal examination and Pap smear the We found no statistically significant relationship between
participants were asked about their gynecological age, number of births, currently used family planning
complaints. According to their reports 12% had no method and having reactive cellular changes or infection.
complaints, 30% had one, 29% two, 19% three, and 10% The number of women with atypical squamous cells were
more than three complaints. The most often reported inadequate (n=4) to perform a statistical analysis. Some
complaint was vaginal discharge, followed by itching and characteristics of the participants with atypical cell
lower genital tract burning. The results of the vaginal changes are shown in Table 4.

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Table 4 Some characteristics of participants with atypical cervical HPV colonization was 2.1% [11]. Another
epithelial cell changes hospital-based study with 4487 patients reported the
Case LSIL HSIL prevalence of LSIL as 4.2% and HSIL as 2.8% [12].
characteristics (n=2) (n=2)
(n=4)
Studies in primary health care settings gave also low
Age 40 42 41 41
Education Primary Primary Illiterate Primary frequencies of atypical cell abnormalities of 1.7% [13] and
Occupation Housewife Housewife Housewif Housewife 5.3% [14]. In our study the majority of Pap smears were
e evaluated as reactive cellular changes (67.2%), followed
Menarche 13 14 13 13 by infections (17.7%). Similar results were obtained from
age (years) other studies done both in hospital or primary health care
Age at first 17 17 15 16 settings: 45% reactive cellular changes and 13.0%
marriage
infections [9]; 23.4% reactive cellular changes and 50.6%
(years)
Number of 1 1 1 1 infections [10]; 42.9% reactive cellular changes and 26.0%
sexual infections; [14] and 28.9% reactive cellular changes and
partners 49.8% infection [13]. These results show that vaginal
Number of 4 7 6 6 infections are important and may be a public health
pregnancies problem that should receive more attention.
Number of 2 3 2 2
live births
The low frequency of atypical epithelial cell abnormalities
Number of 1 3 4 4
abortions in our study could be due to a low-risk population. Risk
Currently factors for cervical cancer are as follows [15]: persistent or
used family CI CI CI CI chronic infection with oncogenic types of HPV (types 16,
planning 18, 31, 33, 45, 58); immunodeficiency; high parity;
method tobacco smoking; coinfection with HIV or other sexually
History of No No No No transmitted diseases; and long term (>5 years) use of oral
smoking contraceptives. The status of Turkish women according to
Familial Yes Yes Yes Yes
these risk factors has been reported in some published
history of
cancer
reports.
History of Absent Absent Absent Absent
STD To the best of our knowledge, there is only one published
Complaints Vaginal Pruritus Vaginal Vaginal study in regarding the HPV infection prevalence among
discharge discharge discharge Turkish women [11]. This study reported a low general
LSIL: Low grade squamous intraepithelial lesion, HSIL: High frequency (2.1%) of cervical HPV colonization.
grade squamous intraepithelial lesion, CI: Coitus interruptus, Forty-eight percent of HPV-positive cases were infected
STD: Sexually transmitted disease. with types 16, 18 and 31 which are accepted as oncogenic
variants. This study suggested that HPV infection with
The study group was not familiar with Pap smear testing; oncogenic types is not very common among Turkish
91% had never heard of it. We found no statistically women. There are insufficient data about
significant relationship between their knowledge and age immunodeficiency and HIV infection prevalence in Turkey,
(χ2=1.251, P>.05) or educational attainment (χ2=2.982, but the latest official statistics showed a low prevalence of
P>.05). HIV infection and AIDS cases. The total number of cases
reported in the year 2008 was 2,412, of whom 750 were
Discussion women, in a population of 73,000,000 [16].
Our Pap smear results showed a low rate of atypical
cervical epithelial cell abnormalities among our study High parity is common in Turkey, and according to the
population. However, these results should be regarded Turkey Demographic and Health Survey 2003, the total
cautiously due to the low sensitivity of Pap smear testing. fertility rate was 2.2 per thousand. Among our study group
We have not had the opportunity to evaluate our results the mean number of pregnancies was 3.4 ± 2.0 and of live
with other more sensitive tests like AAT (acetic acid test) births was 2.5 ± 1.4 which could be considered high parity
and HPV identification [8]. [6].

A few studies have been performed among Turkish women Cigarette smoking is a growing problem among Turkish
using the Pap smear test, and have also found low rates of women and studies have shown that about 40% - 50%
atypical cervical cells. A hospital-based study between percent of women were regular smokers [17]. Among our
1997 and 1999 among 24,178 women reported atypical study group this percentage was 20.2%.
cell abnormalities as 0.4% [9]. Another study among 3,013
women reported a frequency of atypical cell abnormalities Oral contraceptives are not widely used by Turkish women,
and only 4.7% of all married women of childbearing age
of 1% [10]. A recent study done in a hospital setting found
a frequency of atypical cells of 0.7%, but the frequency of use oral contraceptives [17]. In our study group the use
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of oral contraceptives was found to be 3.6%, which could our study group.
be evaluated as low risk.
The cost of the Pap smear test was as low as $20 per test
We conclude that among Turkish women the risk factors in our study and was covered by all the health insurance
for cervical cancer are high parity, cigarette smoking and schemes that exist in Turkey. Service in all primary health
vaginal infections. In spite of these existing risk factors, care units is free of charge; no additional costs were
studies both in hospital and primary health care settings accrued, and there were no transportation costs because
have shown a low prevalence of atypical cervical cell the primary health care unit where the specimens were
changes. Modifying factors for risk should be further taken was within walking distance of the laboratory.
evaluated and other factors such as cultural characteristics,
sexual patterns and sociological aspects should be taken The announcement by the Ministry of Health that
into account. Some published studies have showed that envisions Pap smear testing as a routine screening at
circumcision and having only one sexual partner may have primary health care units should be a reality in the very
a negative impact on developing cervical cancer by near future. This application will not only help prevent
decreasing the risk of HPV infection [18, 19]. However, in cervical cancer but will also create an opportunity for
men with low-risk sexual behavior and monogamous educating women and their husbands regarding this health
female partners, circumcision makes no difference to the issue.
risk of cervical cancer [20]. Menczer quotes research that
male circumcision probably does not contribute to a lower Acknowledgments
incidence of cervical cancer in Jewish populations [21]. Author’s contributions
Since circumcision is a traditional and religious pattern H. Celik-Mehmetoglu: planning and design of the study,
among the Turkish population, all the husbands of the the questionnaire, data acquisition process, interpretation
study group women were circumcised. Following culture of the results, drafting of the article and final approval.
and tradition, 96.4% of the women had had only one
sexual partner, and all of the sexual partnerships were G. Sadikoglu: planning and design of the study,
marital. Could all these patterns be linked with the low presentation of results, critical revision of the content and
prevalence of atypical cervical cell abnormalities? These final approval.
relationships should be further evaluated.
A. Ozcakir: planning and design of the study, critical
In our study, 90.7% of the study participants reported that revision of the article and final approval.
they had not heard about Pap smears before. In previous
studies, the percentages of women who had heard of Pap N. Bilgel: design of the study, preparation of the
smear testing were reported to be 29.7% and 76.9% [22, manuscript and final approval.
23].
This study and manuscript has no conflict of interests.
Conclusions
Although the relatively small size of our study group may The authors would like to acknowledge the editorial
have been a limitation, we believe that this study reveals assistance of Dr. Belinda Peace.
some important issues. In conclusion we want to
emphasize some key points. References
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