JIPH-522; No.

of Pages 6

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Journal of Infection and Public Health (2015) xxx, xxxxxx

Demographic characteristics and risk

factors in Turkish patients with
anogenital warts
Emine Tamer a,, Seray Klc C
akmak a,
Mustafa Necmi Ilhan b, Ferda Artz a
a
b

Ankara Numune Education and Research Hospital, Dermatology Clinic, Turkey

Gazi University Faculty of Medicine, Public Health & Occupational Health, Turkey

Received 3 August 2015 ; received in revised form 9 November 2015; accepted 11 December 2015

KEYWORDS
Anogenital wart;
Demographical
ndings;
HPV infection;
Risk factors;
Turkey

Summary Anogenital warts (AGW) are one of the most common sexually transmitted diseases worldwide. The determination of groups vulnerable to contracting
anogenital warts (AGW) leads to the development of policies for disease control and
of prevention programs. The aim of our study was to investigate the demographical
features and risk factors of Turkish patients with AGW.
This study included 200 patients with AGW and 200 healthy individuals as a control
group. The age, gender, education and marital status, age of rst sexual intercourse,
number of sexual partners, sexual orientation, and smoking status were recorded in
both groups.
In this study, 88% of the patients were male, and 12% were female. The mean age
of the patients was 35.21 0.77 years, and the majority of patients were below 35
years old (63%). Furthermore, 46.0% of the patients were educated at the university
level, and 33.5% had graduated high school. No signicant differences were found
based on sexual orientation or condoms between the patient and control groups. In
the patient group, the mean age of rst sexual intercourse was signicantly earlier,
and the number of single individuals and sexual partners were signicantly higher.
Also, 61% of the patients were current smokers, which was signicantly higher than
the control group. The duration of smoking and the duration of AGW were found to
be correlated. All patients were tested for anti-HIV antibodies, and only one patient
was found to be infected.

Corresponding author at: 435, Cadde Zirvekent Zambak Sitesi No: 50A/50, Birlik Mahallesi, 06610 Cankaya, Ankara, Turkey.
Tel.: +90 5055670488.
E-mail addresses: eminettamer@yahoo.com.tr (E. Tamer), mnilhan@gazi.edu.tr (M.N. Ilhan), ferdaartuz@yahoo.com (F. Artz).

http://dx.doi.org/10.1016/j.jiph.2015.12.009
1876-0341/ 2015 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier Limited. All rights reserved.

Please cite this article in press as: Tamer E, et al. Demographic characteristics and risk factors in Turkish patients
with anogenital warts. J Infect Public Health (2015), http://dx.doi.org/10.1016/j.jiph.2015.12.009
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JIPH-522; No. of Pages 6

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E. Tamer et al.
AGW were more common in patients younger than 35 years old, among men, and
among those who had graduated from high school or university. Early age of rst
sexual intercourse, a high number of sexual partners, being single, and smoking were
also risk factors for the development of anogenital warts.
2015 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier
Limited. All rights reserved.

Introduction
Anogenital warts (AGW) are a common, highly
infectious disease caused by human papilloma virus
(HPV). The high recurrence rate of AGW contributes to direct medical costs, productivity loss
and increased psychosocial impact [1].
Like all sexually transmitted diseases, AGW have
an important impact on the health of society. Being
aware of possible risk factors leads to the use of
efcient protection measures and lowers the cost
of treatment.
Several studies have shown that the lifetime
number of sexual partners and the frequency of
sex or other intimate skin-to-skin contact increase
the chance of being infected with HPV. In addition,
other risk factors have been reported to affect AGW
development, including smoking and immunodeciency [2].
There have been no controlled studies investigating the risk factors in patients with AGW in
Turkey. We aimed to investigate patient demographics and risk factors, including smoking,
which is the most common addictive behavior
in Turkey in patients with AGW. The identication of important risk groups and risk behaviors
associated with AGW in our country would help
to take preventive measures and control the
disease.

Materials and methods

This study included 200 patients with AGW who
were 18 years of age or older and who were
admitted to our outpatient clinic between January
2014 and April 2015. The control group included
200 individuals of matching age and gender who
were admitted to our outpatient clinic with
complaints other than AGW or other sexually transmitted diseases during the same period. The study
was approved by the ethical committee of our

hospital, and informed consent was obtained from

the patient and the control groups.
Dermatological and physical examinations of the
patients and controls were performed. Information regarding age, gender, education and marital
status, age of rst sexual intercourse, number of
sexual partners, use of condoms, sexual orientation, and anal intercourse were asked by the
physician and recorded for both the patient and the
control groups. In addition, the patients and controls were asked if they were current smokers, and
the duration of smoking was noted. The duration
and localization of AGW were recorded for members of the patient group.
Enzyme immunoassay (EIA) was used to detect
human immunodeciency virus antibody (anti-HIV)
in the patient group.

Statistical analysis
Data analysis was performed using SPSS 15.0
software (Chicago, IL, USA). Quantitative data
are given as the mean standard deviation, and
qualitative variables are presented as frequency
distributions and percentages. Chi-square and
Fisher tests were used for statistical analysis, and
a p value < 0.05 was considered to be statistically
signicant.
Multivariate analysis was performed for variables
found to be statistically signicant in univariate
analysis.

Results
The patient group included 200 patients with AGW;
176 (88%) were male, and 24 (12%) were female.
The control group included 200 individuals; 187
(93.5%) were male and 13 (6.5%) were female.
There was no signicant difference between the
genders of the patient and control groups.

Please cite this article in press as: Tamer E, et al. Demographic characteristics and risk factors in Turkish patients
with anogenital warts. J Infect Public Health (2015), http://dx.doi.org/10.1016/j.jiph.2015.12.009
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Turkish patients with anogenital warts

The age of the patients ranged from 18 to 69
years (mean: 35.21 0.77 years), and the age of
the controls ranged from 18 to 59 years (mean:
32.27 0.71 years). There was no signicant difference in the mean ages of the patient and control
groups.
Ninety-two (46.0%) of the patients were educated at the university level, 67 (33.5%) had
graduated from high school, and the rest of the
patients had lower degrees of education. Fiftythree (26.5%) members of the control group were
educated at university, 66 (33.0%) had graduated
from high school, and the rest had lower degrees of
education.
In the patient group, 86 (43.0%) of the patients
or their partners were using condoms, while in the
control group, 63 (39.1%) of the patients or their
partners were using condoms. There was no signicant difference in the use of condoms between the
patient and control groups.
The age of rst sexual intercourse was between
13 and 33 years (mean: 19.07 3.27 years) in the
patient group and was between 14 and 29 years
(mean: 20.12 3.35 years) in the control group.
The mean age of rst sexual intercourse was signicantly earlier in the patient group.
The number of sexual partners was between
1 and 150 (median: 3) in the patient group and
between 1 and 15 (median: 1) in the control group.
The patient group had a signicantly higher number
of sexual partners.
Eighty-seven (43.5%) of the patients and 115
of the controls (57.5%) were married. The control
group had a signicantly higher number of married
individuals when compared with the patient group.
While 190 (95%) of the individuals in the AGW
group were heterosexual, 8 (4%) were homosexual
and 2 (%1) were bisexual; 196 (98%) of the individuals in the control group were heterosexual, 2 (1%)
were homosexual and 2 (1%) were bisexual. No signicant difference was found between the sexual
orientations of the patient and the control groups
(Table 1).
Anal intercourse prevalence was 12 (6%) in the
AGW group and 4 (2%) in the patient group, with no
signicant difference between the groups (Table 1).
The age of the rst appearance of AGW was
between 16 and 63 years in the patient group
(median: 32.64 10.38 years).
AGW had been present between 1 and 360
months (mean: 29.87 43.41 months) in the
patient group at the time of the study.
In 49.5% of patients, AGW appeared before the
age of 30 years, while in 55.5%, AGW had been
present for less than 12 months.

3
On hundred and twenty-two (61.0%) of the
patients and 91(45.5%) of the control subjects were
current smokers. The incidence of smoking was signicantly higher in the patient group.
The duration of smoking and the duration of AGW
were found to be correlated (r = 0.307, p = 0.001).
Every year of smoking increased the length of the
duration of AGW by 0.30 months.
The main characteristics and risk factors in the
control and patient groups are given in Table 1.
All patients were tested for anti-HIV antibodies; only one patient was found to have an HIV
infection.
Multivariate analysis was performed with variables found to be statistically signicant in the
univariate analysis (i.e., the age of rst sexual
intercourse, the number of sexual partners, and
smoking status). According to the multivariate
analysis, the number of partners was the most
important risk factor for AGW (Table 2).

Discussion
HPV is transmitted via genital contact and is
the most common sexually transmitted infection
worldwide. Apart from genital contact, risk factors for HPV acquisition include younger age, early
coitarche, number of lifetime sexual partners, failure to use condoms consistently, marital status, and
low socioeconomic status. Smoking is postulated to
be an additional risk factor due to increased susceptibility to the acquisition of HPV [3].
The demographical features of individual countries may play an important role in the spread
of sexually transmitted diseases. There has been
a rapid immigration from rural areas of Turkey
where younger population predominates to major
cities. Nearly one quarter of the Turkish population
lives in Istanbul, Ankara and Izmir [4]. Because our
hospital is one of the biggest government hospitals
and serves patients from Ankara as well as the rest
of the Turkey, our study may serve as a model for
AGW in the whole of Turkey.
Although AGW are not life threatening, they generate a sizeable nancial burden on countries and
cause signicant psychological distress. The annual
incidence of AGW is estimated to be 97131 per
100.000 in Turkey, indicating that AGW represent a
sizeable problem in Turkey and that health strategies should be developed for prevention [5].
In our study, we observed a signicant male predominance. The reason for male predominance in
our study may be that female patients frequently
visit gynecology clinics for the treatment of AGW.

Please cite this article in press as: Tamer E, et al. Demographic characteristics and risk factors in Turkish patients
with anogenital warts. J Infect Public Health (2015), http://dx.doi.org/10.1016/j.jiph.2015.12.009
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For personal use only. No other uses without permission. Copyright 2016. Elsevier Inc. All rights reserved.

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Table 1

The main characteristics and risk factors in the control and patient groups.

Age (mean)
Gender, n (%)
Male
Female
Age at rst sexual intercourse (mean)
Number of sexual partners (median)
Married, n (%)
Condom use, n (%)
Current smoker, n (%)
Sexual orientation
Homo/bisexual, n (%)
Anal sex, n (%)

Table 2

Control (n = 200)

Patient (n = 200)

32.27 10.07

35.21 10.91

187 (93.5)
13 (6.5)
20.12 3.35
1
115 (57.5)
63 (39.1)
91 (45.5)
4 (2.0)
4 (2.0)

176 (88)
24 (12)
19.07 3.27
3
87 (43.5)
86 (43.0)
122 (61.0)
10 (5.0)
12 (6.0)

p Value

Test

0.05
0.083

t-Test
Chi-square

0.03
0.0001
0.007
0.519
0.003

t-Test
MannWhitney U
Chi-square
Chi-square
Chi-square

0.139
0.071

Chi-square
Fisher

Risk factors for AGW according to multivariate analysis.

Risk factors

Exp ()

%95 CI

p Value

Current smoker
Number of sexual partners
Age of rst sexual intercourse

0.646
1.523
0.985

0.4031.035
1.3151.763
0.9171.059

0.69
0.0001
0.985

Furthermore, extramarital sexual relationships are

less frequent among women, and the age of rst
sexual intercourse occurs at later ages in Turkish
women due to social constraints enforced by strong
family relations and religious beliefs. Combined,
these factors may lead to a lower frequency of AGW
among Turkish women [4].
In our study, 79.5% patients had graduated from
high school or university. It has been reported that
the prevalence of sexually transmitted diseases
increases with increasing level of education [6,7].
Indeed, patients with AGW have high educational
and socioeconomic statuses; low educational and
socioeconomic statuses do not appear to increase
the risk of AGW in Turkey. Furthermore, the high
prevalence of highly educated individuals in the
AGW group may reect a greater awareness of sexually transmitted disease and symptom recognition
in this group, leading to a higher level of detection.
Condom use serves as a barrier by preventing
direct contact. The risk of HPV transmission can be
reduced by regular condom use [810]. Although
some studies have failed to show a protective
effect of condom use, it has been reported that
consistent condom use signicantly reduces the
risk of acquiring AGW [6,8]. In our study, no
signicant difference was found based on condom
use between the patient and the control groups.
This might be because the patient group did not

use condoms regularly or began condom use after

the appearance of AGW. Furthermore, a history of
only one sexual partner and being married reduce
the likelihood of using condoms.
In other studies, the number of sexually active
years was found to be correlated with the risk of
HPV transmission [810]. Similarly, we found that
the age of rst sexual intercourse was signicantly
earlier in the patient group.
In most studies, the number of sexual partners
was found to be an important risk factor in the
development and recurrence of AGW [1,3,1116].
In accordance, we found that the number of sexual
partners was signicantly higher in patients with
AGW.
In our study, the number of homosexual and
bisexual individuals was small, both in the patient
and control group. This might be because individuals who are not heterosexual are severely
marginalized in our country.
HIV infection has been reported to be an
important risk factor in the development of AGW
[9,11,17,18]. In our study, only one patient had an
HIV infection. We could not compare HIV positivity with the control group because we did not know
the HIV status of members of the control group.
Because HIV infection is rare in Turkey, the fact that
only one patient in our study was infected is not
surprising.

Please cite this article in press as: Tamer E, et al. Demographic characteristics and risk factors in Turkish patients
with anogenital warts. J Infect Public Health (2015), http://dx.doi.org/10.1016/j.jiph.2015.12.009
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Turkish patients with anogenital warts

In our study, the reason for a higher frequency of
marriage in the control group might be that extramarital relationships are rare in Turkish society; it
is also possible that sexually transmitted diseases
more commonly occur in extramarital relationships.
Tobacco is the most commonly used addictive
substance in Turkey. Being sexually active from
an early age and having a high number of sexual
partners are inevitable risk factors for the development of AGW. The effect of tobacco smoking
on the development of AGW has been investigated
previously, and tobacco smoking was found to be
higher among patients with AGW in several studies [3,8,1015,17,18]. In the literature review by
Kaderli et al., which reviewed 15 studies of AGW,
smoking was reported to increase the risk of AGW,
and smoking for 10 years or longer was a risk factor
for recurrent AGW [3]. Furthermore, Nyitray et al.
reported that in men with anal warts, smoking was
related to persistent infection [12].
In our study, 61% of patients and 45.5% of control
subjects were current smokers. Tobacco smoking
was found to be signicantly higher in the patient
group, and we found that every year of smoking
increased the monthly duration of AGW by 0.30
times. Our results suggest that smoking is a risk factor for the development of AGW and is related to
the duration of AGW.
Smoking has deleterious effects on systemic and
local immunity by suppressing both cell-mediated
and humoral immune responses, which might lead
to the present nding of increased susceptibility to
HPV infection and the development of AGW. Nicotine, the addictive substance in cigarette smoke,
has been shown to be the main immunosuppressive constituent of cigarette smoke. Furthermore,
unmeasured high-risk sexual behaviors might be
potentially important confounders in the association between smoking and the incidence of HPV
infection; it is known that tobacco smoking has serious effects on the health of individuals who might
be prone to other risk behaviors, including risky
sexual behaviors. This is supported by the data of
Herrero et al., who found that sex with multiple
partners is more prevalent among smokers [3].
Our study is the rst to assess both demographical data and possible risk factors in patients with
AGW in Turkey. Our results contribute to the literature about demographical features and risk factors
of AGW, as well as the measures that might be taken
to prevent the development of AGW.

Funding
No funding sources.

Competing interests
None declared.

Ethical approval
Not required.

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Please cite this article in press as: Tamer E, et al. Demographic characteristics and risk factors in Turkish patients
with anogenital warts. J Infect Public Health (2015), http://dx.doi.org/10.1016/j.jiph.2015.12.009
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Please cite this article in press as: Tamer E, et al. Demographic characteristics and risk factors in Turkish patients
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