ARTICLE
Auteur(s) : H
Papadogeorgaki1, C Caroni2, E
Frangouli1, A Flemetakis1, A
Katsambas1, M Hadjivassiliou1
1Microbiology, STD’s and AIDS Department, “A. Sygros”
Hospital Athens, 5 Ionos Dragoumi str., Athens 161 21, GreeceFax:
(+30) 210 3643282
2Department of Mathematics, National Technical
University of Athens, Greece
accepté le 1 Juillet 2006
In the last twenty years, few areas of medicine have been more
dynamic than the field of sexually transmitted infections (STIs).
The main reasons for this are the advent of the HIV epidemic, the
increased incidence of chlamydial and viral sexually transmitted
infections and the widely implicated role of commercial female and
male sex workers. The fact that HIV infection is enhanced by the
classic STIs, especially those causing genital ulcer disease,
indicates that prevention and control have to be established. Most
STIs can be easily misdiagnosed since they can have a mild
subclinical asymptomatic course with severe complications and
sequelae for the patients and their contacts, especially women in
the reproductive age group.Various protocols and algorithms have
been developed worldwide for symptomatic patients in an attempt to
prevent transmission of STIs [1, 2]. Reliable epidemiological
surveillance plays a central role in the success of this effort [3,
4]. Following the same lines of prevention, intervention programs
on high risk groups such as sex workers or intravenous drug users
together with effective treatment have been shown to reduce the
prevalence and transmission of these infections in the community
[5, 6].The purpose of this study was to establish the prevalence of
sexually transmitted infections –Neisseria gonorrhoeae and
Chlamydia trachomatis infection, syphilis, HIV infection, Herpes
Simplex Virus type II (HSV-2), Hepatitis B (HBV), Hepatitis C
(HCV)- in asymptomatic female sex workers in the greater Athens
area in Greece, where data on prevalence are lacking (except for
HIV infection) [7, 8]. Our study was limited to asymptomatic women
as they represent a high risk reservoir for transmitting STIs when
they are engaged in sex working.
Materials and methods
Study population
Our sample comprised 299 asymptomatic female sex workers who, in a
six month period, between May 2005 and October 2005, applied for an
official license to work as prostitutes and were examined at the A.
Sygros Hospital in Athens, Greece. A. Sygros Hospital is the main
hospital in Greece for the management of Skin and Venereal
Diseases. It serves Athens, Piraeus – the main port –, the
surrounding islands and the rest of the greater Athens area, a
total of 5,000,000 inhabitants, almost half of the population of
Greece.
According to data from the Ministry of Public Order, 700 female
sex workers are holders of an official license for work and 10,000
are working illegally. Most of the illegal sex workers do not have
access to medical services, mainly due to language or religion
problems. Under the Greek law voted in January 2000, to obtain a
working license as a sex worker it is compulsory to be examined for
gonorrhoeae, Chlamydia trachomatis infection, early infectious
syphilis and HIV infection in a public STD and HIV clinic. For the
purposes of the present study, these women were also screened for
HBV, HCV and HSV-2 infection.
All women were asked to answer anonymously a standard
questionnaire with information on age, country of birth, country of
permanent residence, education, STIs in the past, intravenous drug
use at any time, use of condoms and duration of illegal sex
working.
Laboratory methods
Endocervical, rectal and pharyngeal swabs were cultured for N.
gonorrhoeae in New York City medium with vancomycin, colistin and
amphotericin B as inhibitors produced by OXOID which permits the
selective growth of Neisseria gonorrhoeae and Neisseria
meningitidis. Identification of Neisseria gonorrhoeae was made by
using the Neisseria 4H by BIORAD.
The COBAS Amplicor PCR test by Roche Molecular Systems,
Branchburg, NJ, USA, was used for the identification of Chlamydia
trachomatis on endocervical swabs.
A blood sample of 15 mL was drawn from each woman, centrifuged
and the serum was stored in – 20 oC until
tested.
Antibodies to Tr. pallidum were screened by using the VDRL slide
flocculation test (DADE Boehring), the FTA-Abs (Trepo-Spot IF Bio
Merieux), TPHA (Serodia – TR.PA by FUJIREBIO Inc.) and Tr. pallidum
EIA IgG and IgM (BOYTY) Dark field microscopy test was not
performed because none of the 299 women presented with an
appropriate mucocutaneous lesion.
HIV infection was assessed by detecting antibodies to HIV-1 and
HIV-2 by enzyme immunoassay (EIA) (Vironostika HIV Uni-Form II
Ag/Ab by Organon-Teknika). Western Blot (New LAV Blot I by BIO-RAD)
was not used since all blood samples proved negative by EIA.
The AXSYM EIA test by ABBOTT was used to determine HBsAg, HBcAg,
anti-HBs, anti-HBc and anti-HBe for Hepatitis B and anti HCV for
Hepatitis C. Since there is substantial evidence that Hepatitis C
can be transmitted sexually as well as by injecting drug use,
serological markers for it were also screened.
Type specific EIA (HerpeSelect Focus Diagnostics) was used to
screen antibodies to Herpes Simplex Virus type 2 (HSV-2). Direct
HSV-2 antigen detection tests were not performed since no woman
presented with a genital ulcer.
During the same period of time 537,858 blood donors were
screened by the blood banks all over Greece for syphilis, HIV, HBV
and HCV. We used the blood donors as reference population and
compared these data with ours although we are aware of the possible
biases intervening in this comparison. In particular, the blood
donors are drawn from all over the country and we do not have any
information on their sex and age distribution. As reference group
for HSV-2 we took 130 women who attended the same hospital with a
clinical diagnosis of HSV-2 infection and also 53 asymptomatic
Greek women with an age distribution similar to that of the sex
workers.
Statistical methods
Chi-squared tests were used for comparing prevalences or other
qualitative data between subgroups of respondents; Yates’s
correction was used in tests with one degree of freedom. Age of
respondents was compared between two subgroups using the
Mann-Whitney test and between three or more subgroups using the
Kruskal-Wallis test.
Results
A total of 299 female sex workers were evaluated in this study; 240
(80.3%) of them were Greek by birth and 59 (19.7%) were foreigners
by birth residing in Greece. The foreigners were immigrants from
countries of the Former Soviet Union – Ukraine, Georgia, Russia –
and the Balkans – Bulgaria, Romania, Albania.
The mean age was 39.7 years (standard deviation 10.5) in the
total sample, 41.4 years (s.d. 10.4) among Greeks and 32.6 years
(s.d. 7.8) among immigrants. The immigrants were thus younger than
the Greeks on average (p < 0.001) and they were also better
educated (x32 = 21.5, p < 0.001, table 1(
Table 1 )).
In the Greek sample, education was related to age
(Kruskall-Wallis test, p < 0.001), with the better educated
having a lower average age, but this was not the case among the
immigrants (p = 0.68).
Neisseria gonorrhoeae was isolated from the endocervical swabs
of 19 sex workers, 16 Greeks and 3 immigrants (1 Russian, 1
Georgian, and 1 Albanian). None of the pharyngeal or rectal swabs
grew the microorganism. Sensitivity testing was done on Gonococcal
agar base (OXOID) using the Kirby-Bauer method. No PPNG or TRNG
strains were found among the isolates. The b-lactamase test was
negative on all isolated strains (nitrocephin test by Glaxo). There
was no difference in prevalence between the two groups of sex
workers (x12 = 0.199, p = 0.66).
The COBAS Amplicor test revealed Chlamydia trachomatis from 16
endocervical swabs – 12 from Greek sex workers and 4 from
immigrants (3 Russian and 1 Albanian). Between the two examined
groups of sex workers no difference in prevalence was found
(x12 = 0.296, p = 0.59). Coinfection with
Neisseria gonorrhoeae was absent in our sample.
Herpes simplex type 2 infection was significantly more common in
the Greek sex workers than in the immigrants
(x12 = 13.3, p < 0.001) but there was no
difference in prevalence between the two groups for the other STI’s
(p > 0.5) (table 2( Table 2 )).
For gonoccocal and chlamydial infection prevalence was related
to younger age (p < 0.001), however, for syphilis (p <
0.001), Hepatitis B (p = 0.024) and HSV-2 infection (p < 0.001),
prevalence was related to older age (table 3( Table 3 )). There did not seem to be such a
relationship for Hepatitis C (p = 0.67), although the cases were
few.
A statistically significant association was found between HSV-2
infection and syphilis: HSV-2 was present in 161/255 (65.7%) of sex
workers negative for syphilis and in 47/54 (87.0%) of those
positive for syphilis (x12 = 8.52, p =
0.004). There were no other significant associations between pairs
of STIs (p > 0.4).
In table 4( Table 4 ), the greatly
increased prevalence of Hepatitis C and syphilis in the sex workers
compared to blood donors is evident without the need for a
statistical test. For Hepatitis B, there was a marginally
significant relationship (x12 = 3.81, p =
0.051) while for HIV infection the association was not
statistically significant (p = 1.00).
The 74.6% prevalence of HSV-2 infection found in Greek sex
workers was much higher than that recorded in asymptomatic Greek
women of the general population (16/53, 30.2%,
x12 = 36.5, p < 0.0001) and in the sample
of women with a clinical diagnosis of HSV-2 infection (38/130,
29.2%, x12 = 69.7, p < 0.0001). No
injecting drug use was confirmed. The use of condoms and the
duration of illegal sex working were not evaluated since most of
the answers were not satisfactory.
Table 1 Age and educational level of female sex
workers
|
Total sample (n = 299)
|
Greeks (n = 240)
|
Immigrants (n = 59)
|
|
• Age
|
n
|
%
|
n
|
%
|
n
|
%
|
|
19-24
|
21
|
7.0
|
13
|
5.4
|
8
|
13.6
|
|
25-34
|
78
|
26.1
|
50
|
20.8
|
28
|
47.5
|
|
35-44
|
93
|
31.1
|
76
|
31.7
|
17
|
28.8
|
|
45-54
|
79
|
26.4
|
74
|
30.8
|
5
|
8.5
|
|
55-64
|
25
|
8.4
|
24
|
10.0
|
1
|
1.7
|
|
+ 65
|
3
|
1.0
|
3
|
1.3
|
0
|
0
|
|
• Education
|
|
|
|
|
|
|
|
Uneducated
|
13
|
4.3
|
13
|
5.4
|
0
|
0
|
|
Elementary school
|
173
|
57.9
|
150
|
62.5
|
23
|
39.0
|
|
High school
|
99
|
33.1
|
70
|
29.2
|
29
|
49.2
|
|
University
|
14
|
4.7
|
7
|
2.9
|
7
|
11.9
|
Table 2 Prevalence of STIs (by nationality)
|
Total sample (n = 299)
|
Greeks (n = 240)
|
Immigrants (n = 59)
|
|
n
|
%
|
n
|
%
|
n
|
%
|
|
Neisseria gonorrhoeae
|
19
|
6.3
|
16
|
6.6
|
3
|
5.0
|
|
Chlamydia trachomatis
|
16
|
5.3
|
12
|
5.0
|
4
|
6.7
|
|
HSV-2
|
208
|
69.6
|
179
|
74.6
|
29
|
49.2
|
|
Syphilis
|
54
|
18.1
|
44
|
18.3
|
10
|
16.9
|
|
Hepatitis C
|
7
|
2.3
|
5
|
2.1
|
2
|
3.4
|
|
Hepatitis B
|
4
|
1.3
|
4
|
1.7
|
0
|
0
|
|
HIV
|
0
|
0
|
0
|
0
|
0
|
0
|
|
Any of the above
|
220
|
73.6
|
185
|
77.0
|
35
|
59.3
|
Table 3 Prevalence of STIs by age
|
Age
|
n
|
|
|
|
|
|
|
|
19-24
|
21
|
38.1
|
28.6
|
33.3
|
4.8
|
0.0
|
0.0
|
|
25-34
|
78
|
7.7
|
9.0
|
51.3
|
9.0
|
0.0
|
2.6
|
|
35-44
|
93
|
3.2
|
2.2
|
75.3
|
15.1
|
0.0
|
2.2
|
|
45-54
|
79
|
2.5
|
1.3
|
83.5
|
29.1
|
5.1
|
3.8
|
|
55+
|
28
|
0.0
|
0.0
|
89.3
|
32.1
|
0.0
|
0.0
|
Table 4 Prevalence of STIs in female sex workers and
blood donors
|
Sex workers (n = 299)
|
Blood donors (n = 537,858)
|
|
n
|
%
|
n
|
%
|
|
Syphilis
|
54
|
18.1
|
50
|
0.009
|
|
Hepatitis C
|
7
|
2.3
|
457
|
0.085
|
|
Hepatitis B
|
4
|
1.3
|
2,317
|
0.43
|
|
HIV
|
0
|
0
|
27
|
0.005
|
Discussion
The objective of this study was to determine the prevalence of
sexually transmitted infections among legal asymptomatic sex
workers in the greater Athens area in Greece. It is recognised that
these infections have high prevalence among female sex workers and
they are known to enhance the transmission of HIV [3].
The mean age of the Greek sex workers was quite high (41 years).
This represents the fact that these women decide to register
officially in an older age in an attempt to seek some form of
“loyalty” in their profession but also the fact that some of them
have to produce an official license since they are responsible for
the running of the brothels.
Younger Greek sex workers tend to be better educated than older
ones. This happens because a lot of young educated girls go into
this profession due to the lack of jobs and their anxiety to
acquire a “wealthy” standard of living.
The mean age of immigrant sex workers was 32.6 years. They are
better educated than Greeks of the same age and this represents the
difficulty these women face in finding an appropriate job when
moving to a new country. This fact together with the small number
of young immigrants who apply for an official license goes along
with the Police and Immigration Office remark that young girls from
Eastern Europe are quite often forced by networks of prostitution
to migrate and go into illegal sex working.
The prevalence of Neisseria gonorrhoeae infection in our sample
was 6.6%. This is greater than the prevalence of the infection in
the general population of Greece (p < 0.001) [9] but it is
closely related to older findings in STD clinic attendees in
Athens, Greece [10]. Chlamydia trachomatis prevalence was 5.3%
where prevalence in females in Greece is 3.5% (p = 0.08) [11] and
in STD attendees 6.4% [10].
The prevalence rates for both infections are in agreement with
most studies in female sex workers worldwide [12-14] and follow the
trend for these two sexually transmitted infections in the
literature – young age and multiple sexual partners, two factors
consistently associated with the increased risk of the
infection.
All the women in our sample were HIV negative. This is in
agreement with the few similar studies in the literature [13, 14].
All other STIs investigated with the exception of Hepatitis C,
which is not really sexually transmitted, showed an increased
prevalence compared to the reference groups.
Extensive data with type specific serology on the seroprevalence
of HSV-2 infection in the Greek population are lacking. Accurate
type specific serological assays for HSV-2 infection identify
persons with previously unrecognised HSV-2 infection [15, 16].
There is no specific policy for screening for HSV-2 in Greece,
either in the general population or among high risk groups. The
prevalence of the infection in Greek sex workers is high (74.6%)
and this is in agreement with previous studies in the context of an
STD clinic attendees in Athens, Greece [10]. It is higher than in
immigrants (49.2%) but falls within the limits of the infection in
STI patients [17, 18] and professional sex workers in other
countries [19, 20].
Syphilis and genital herpes are the commonest mixed infections
occurring together in 14.6% of the cases. This is common among sex
workers [21] and represents the two most frequent causes of genital
ulcer disease in Europe [22].
It is interesting that between the two investigated groups of
sex workers the prevalence of any of the examined STIs is much
higher in the Greek sample –75.8% versus 57.6% in the immigrant
sample (table 2).
Female sex workers working legally in Greece are only a small
percentage of those working illegally. From January 2000, when the
prostitution law was voted, to today, according to official
estimates from the Ministries of Internal Affairs, National
Security and Health, approximately 10,000 women are working
illegally as sex workers all over Greece. The majority of them are
immigrants. Despite the small sample, the findings of our study
clearly point out that the health system of Greece must find the
way to intervene in the whole population of sex workers working
legally or illegally in order to achieve better control of
STIs.
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|