Behavioural and serological human immunodeficiency virus risk factors among female commercial sex workers in Cambodia

K Ohshigea, S Moriob, S Mizushimaa, K Kitamuraa, K Tajimac, A Suyamab, S Usukud, P Tiae, LB Hore, S Henge, V Saphonne, O Tochikuboa and K Sodaa

a Department of Public Health, Yokohama City University School of Medicine, 3–9 Fukuura, Kanazawa-ku, Yokohama, 236–0004 Japan.
b Department of Hygiene, Faculty of Medicine, Tottori University, Japan.
c Aichi Cancer Center Research Institute, Japan.
d Yokohama City Institute of Health, Japan.
e National HIV/AIDS Program, Ministry of Health, Cambodia.


    Abstract
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Background The spread of human immunodeficiency virus (HIV) in Cambodia is mainly caused by sexual transmission and the high-risk group in this country are female commercial sex workers (CSW). There are two types of CSW, direct CSW (DCSW) and indirect CSW (IDCSW), who are different from each other in sexual activities. This study was conducted in order to describe the risk factors on HIV for each type of CSW, and to establish effective preventive strategies against the HIV epidemic among CSW.

Methods The participants, 143 DCSW and 94 IDCSW, were interviewed using a questionnaire to determine their demographic characteristics and behaviour. Blood samples were taken for serological tests on HIV, Chlamydia trachomatis and syphilis. The association between their behavioural pattern and their serological results was analysed.

Results The questionnaire study showed that IDCSW had a riskier behavioural pattern than DCSW. The HIV seroprevalence rates of the DCSW and the IDCSW were 52.4% and 22.3%, respectively. Univariate logistic analyses showed a significant association between HIV antibody (HIV-Ab) and current age, age at commencement of commercial sex work, duration of commercial sex work, and the seropositivity of Chlamydia trachomatis—IgG antibody (CT-IgG-Ab) among the DCSW. The analyses also showed a significant relationship between HIV-Ab and CT-IgG-Ab among the IDCSW.

Conclusions Improving condom use rate is very important in order to prevent an HIV epidemic among the two types of CSW. This study also suggests it is important to prevent sexually transmitted disease (STD) such as Chlamydia trachomatis infection. The STD control programme could be efficient for HIV prevention, especially among DCSW.

Keywords Cambodia, female commercial sex workers, behavioural study, seroprevalence, HIV, Chlamydia trachomatis

Accepted 4 November 1999


    Introduction
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Since 1991, when the first human immunodeficiency virus (HIV) infected person was reported in Cambodia, the numbers have increased rapidly. According to a report by the Ministry of Health there were 11 807 diagnosed HIV-infected people and 987 AIDS patients by the end of December 1997 in Cambodia (Official HIV and AIDS case reports: Cambodia. World Health Organization regional office for the Western Pacific 1997). Globally, the Joint United Nations Program on AIDS (UNAIDS) and the World Health Organization (WHO) estimated the number of HIV-infected people at 130 000 at the end of 1997 (Report on the global HIV/AIDS epidemic, June 1998. UNAIDS & WHO, Geneva 1998). The spread of HIV in Cambodia is mainly through heterosexual transmission and the high-risk group are female commercial sex workers (CSW), in whom a high prevalence of HIV and other sexually transmitted diseases (STD) was observed.1 A seroprevalence survey in 1997 showed the HIV seropositive rate among brothel-based CSW was about 39% (445/1132); much higher than that among pregnant women (3%, 160/5003) and blood donors (4%, 649/18 222) (Report on HIV Seroprevalence Survey: Cambodia. World Health Organization regional office for the Western Pacific 1998).

Commercial sex workers are classified into two groups; (i) direct CSW (DCSW) who live in brothels in red light areas, and (ii) indirect CSW (IDCSW) who are non-brothel-based.2–4 There are some differences between the two types of CSW with regard to their behaviour and sexual activities.2 To establish effective preventive strategies against the HIV epidemic among CSW, it is important to reveal the risk factors for HIV infection in each type of CSW.

From December 1997 to January 1998, a cross-sectional epidemiological study on sexual behaviour was carried out by a Japanese and Cambodian co-operative research group using questionnaires and serological tests among DCSW and IDCSW who lived in Sisophon, Bantey Mean Chey Province, Cambodia. Sisophon is located in northwest part of Cambodia near the border with Thailand, and is recognized as an epidemic area for HIV because of the flourishing commercial sex industry. This study was conducted to describe the sexual behaviours of the CSW, their serological status with regard to HIV and other STD and to reveal the risk factors for HIV infection among DCSW and IDCSW in order to establish efficient preventive measures against HIV spread.


    Methods
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Study sample
Direct commercial sex workers
There were 20 brothels in Sisophon. The population of DCSW in this area was estimated at approximately 150 by the Cambodian Ministry of Health. The participants were recruited by the brothel owners from all 20 brothels. In all, 148 out of the 150 DCSW came to hear details of the study. Finally 143 DCSW (a response rate of 95%) agreed to participate and verbal informed consent was obtained after a careful explanation of the purpose and procedures of this study, the follow-up care and guaranteed anonymity.

Indirect commercial sex workers
The IDCSW were legitimately employed in hotels, nightclubs or restaurants as maids, waitresses, dancing girls or beer promotion girls and occasionally had sexual contacts with their clients after negotiation. The population of IDCSW in Sisophon was roughly estimated at 120 by the Ministry of Health. The participants were recruited by the owners of hotels, nightclubs and restaurants. Of the 102 IDCSW who came to hear the study explained, eight refused to participate. Finally, verbal informed consent was obtained from 94 after the further explanation (response rate of approximately 78%).

Questionnaires on demographic characteristics and sexual behaviour
Questionnaires were developed for the two types of CSW by the Japan-Cambodia research group.2 It included questions on their age, nationality, marital status, social support and sexual behaviour as these had been suggested previously as risk factors for HIV;3–8 past history of STD, sexual intercourse without condoms, lack of genital hygiene, commencement of commercial sex work at a young age, ignorance of HIV infection, were also included.

Procedure
All eligible subjects were numbered in order to maintain anonymity and to link individual questionnaires with serological tests. They were interviewed by trained female interviewers who belong to the provincial health department. After the interview, 5 ml blood samples were taken from all participants for serological tests.

Each subject received a ticket printed with an individual number after their blood samples had been taken. They could receive the reports on their blood tests at the provincial office in return for the numbered tickets. Appropriate medical care would be provided by the Ministry, in the event of the subjects having positive serological tests.

Laboratory analyses
The blood was separated into sera at the provincial laboratory and then the serum samples preserved at 4°C were immediately transported to the Sianouk Hospital in Phnom Penh. The samples were tested at the hospital laboratory for HIV antibody (HIV-Ab) using enzyme immunoassay (EIA, Generavia-mixt, Pasteur, Paris, France), and for Treponema pallidum using haemagglutination assay (TPHA; Fujirebio, Tokyo, Japan). The remaining serum samples were then frozen and transported to the Yokohama City University, School of Medicine, Japan by air, and were examined for Chlamydia trachomatis IgG antibody (CT-IgG-Ab; ELISA, SRL Inc., Tokyo, Japan). The samples HIV-positive by EIA were confirmed by Western Blot (WB; Diagnostics Pasteur, Paris, France) testing at the laboratory of Yokohama City Institute of Health, Japan.

Statistical analyses
The statistical difference of seroprevalence between the DCSW and the IDCSW was analysed using {chi}2 test. Relationships between the risk factors and HIV seropositivity were analysed univariately by calculating unadjusted odds ratios (OR) with 95% CI. Multiple logistic regression analysis was used to determine the adjusted OR of each factor. These analyses were conducted using SPSS (Windows, version 7.51J).


    Results
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Demographic characteristics
The age, nationality and marital status and advisors of the participants are summarized in Table 1Go. The mean ages of the DCSW and the IDCSW were 20.3 years (range 15–33, standard deviation: 3.1,) and 22.0 years (range 15–40, standard deviation: 5.4), respectively. Approximately 98% had Cambodian nationality. Overall, 139 of the DCSW (97.2%) and 82 of the IDCSW (87.2%) were single or separated from partners. The IDCSW included 34 waitresses, 24 beer promotion girls, 21 dancers, 10 hotel maids and 5 singers.


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Table 1 Demographic characteristics of direct commercial sex workers (DCSW) and indirect commercial sex workers (IDCSW) in Sisophon, Cambodia
 
Regarding their social support, we asked the participants: Do you have anyone whom you can consult when you have a problem in your life? Out of 143 DCSW, 61 (42.7%) answered that they did not have any advisors and, if they had, the advisors for many DCSW were the owners of their brothels. None of them answered that they had consulted their parents, husbands, or boyfriends. On the other hand, the advisors for the IDCSW were more varied than those for the DCSW. Twenty-two and 15 of the IDCSW answered that they had consulted their parents, husbands/boyfriends, respectively (Table 1Go).

Behavioural study
The results of the behavioural study for the DCSW and the IDCSW are described in Table 2Go. Many of the IDCSW did not answer several questions (NA in Table 2Go). Differences between the two types of CSW were noted for the number of clients per day, earnings per client, possession of condoms and knowledge on routes of HIV infection. While 94.4% of the DCSW (135/ 143) answered they had more than two clients a day, 43 out of 94 IDCSW answered they had one client in a day. The average earnings of the DCSW were 5566 Riel per client, while the IDCSW earnings averaged 29 362 Riel per client. Most of the DCSW (97.9%) answered that they possessed condoms and 44.8% of them answered that they used a condom during sexual intercourse every time. On the other hand, only a quarter of the IDCSW said they possessed condoms and only 10.6% of them answered they had used a condom every time. With regard to knowledge on HIV transmission, the DCSW tended to answer correctly about the routes of HIV infection (e.g. sexual intercourse, blood/blood products, sharing needles and mother to child transmission) in comparison with the IDCSW.


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Table 2 Results of behavioural study among direct commercial sex workers (DCSW) and indirect commercial sex workers (IDCSW)
 
Serological prevalence
The seroprevalence of HIV-Ab, TPHA and CT-IgG-Ab is presented in Table 3Go. The CT-IgG-Ab is classified into three groups according to an index based on SRL criterion.9,10 The first group was negative or borderline SRL (index <1.1), second was positive but had a low titre (index was >=1.1 and <4) and the third group was positive and had a higher titre (index was >=4).


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Table 3 Results of serological tests among direct commercial sex workers (DCSW) and indirect commercial sex workers (IDCSW)
 
The seropositive rates of HIV-Ab and TPHA among the DCSW were 52.4% and 9.8%, respectively. A large per cent of the DCSW were seropositive for CT-IgG-Ab (83.2%) and more than half of the DCSW had the higher titre of CT-IgG-Ab. The seropositive rates of HIV-Ab and TPHA among the IDCSW were 22.3% and 3.2%, respectively. More than half of the IDCSW were seropositive for CT-IgG-Ab, but the rate of the IDCSW who had a higher titre of CT-IgG-Ab was relatively low (20.2%). The seropositive prevalence of the HIV-Ab and CT-IgG-Ab showed significant differences between the DCSW and the IDCSW (P < 0.001).

Univariate analyses
To study the association of risk factors to HIV among the CSW in this area, univariate logistic regression analyses were performed. Current age and age at commencement of commercial sex work were classified into three categories, <18 years, 18–20 years, and >20 years. The age band is narrow because of the narrowness of the age range of the subjects.

The results of the analyses for the DCSW are shown in Table 4Go. Current age, age at commencement of commercial sex work and duration of commercial sex work showed significant associations with HIV-Ab seropositivity. Based on the results of the serological test, CT-IgG-Ab seropositivity with higher titre (index >=4.0) was significantly related to HIV infection (OR = 3.48, 95% CI : 1.32–9.19).


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Table 4 Univariate logistic regression analyses between human immunodeficiency antibody (HIV-Ab) seropositivity and risk factors among direct commercial sex workers (DCSW) (N = 143)
 
The results of the analyses for IDCSW are summarized in Table 5Go. For these women HIV seropositivity does not have a significant association with their age and their risk behaviours. However, CT-IgG-Ab seropositivity, for both the lower and higher titre groups, showed a significant association with HIV seropositivity (OR = 6.50, 95% CI : 1.64–25.80, OR = 7.58, 95% CI : 1.69–33.95, respectively).


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Table 5 Univariate logistic regression analyses between HIV-Ab seropositivity and risk factors among indirect commercial sex workers (IDCSW) (N = 94)
 
Multivariate analyses
Multiple logistic regression analysis was applied to adjust for confounding among the risk factors and to determine the most influential factor on HIV prevalence among the CSW in this area. The adjusted OR were calculated with a model that included type of commercial sex work and theoretically relevant risk factors as the independent variables among the 143 DCSW and 47 IDCSW who answered all the questions on those factors. The result of the analysis is presented in Table 6Go. The analysis showed only a statistically significant association between HIV infection and CT-IgG-Ab seropositivity with higher titre (adjusted OR = 3.13, 95% CI : 1.20–8.13). The association was also observed using multivariate logistic regression analysis for adjusting risk factors among the 143 DCSW (adjusted OR = 3.23, 95% CI : 1.04–10.03). However, it was not observed with this analysis among the IDCSW because of their low response to the questions.


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Table 6 Multivariate logistic regression analyses between human immunodeficiency antibody (HIV-Ab) seropositivity and risk factors among 143 direct commercial sex workers (DCSW) and 47 indirect commercial sex workers (ICSW) who completely answered the questions on risk factors
 

    Discussion
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Limitations
There are some limitations in this study. First of all, the sample size was small due to the small population of CSW in Sisophon, however this study obtained a high response. Secondly, generally, questionnaire studies have a limitation whereby interviewees are apt to select favourable answers possibly resulting in interview bias. In this questionnaire study, additionally, the IDCSW answered fewer of the questions, even though the IDCSW interviews were carried out in the same way as for the DCSW. The IDCSW answered questions about their demographic characteristics frankly but were hesitant to answer questions about their sexual behaviour. The different way of recruiting clients might result in the different attitudes to the survey between the DCSW and the IDCSW; however, the exact reason is not clear. Thirdly, the two groups are probably not exclusive. Women who are concerned with commercial sex work may change their strategies for earning their livelihoods.

Demographic characteristics
Difference with regard to their marital status and advisors were observed between the DCSW and the IDCSW. More DCSW than IDCSW answered that they were single or separated from partners and that they did not have not an advisor. Additionally, many of the IDCSW but none of the DCSW answered that their parents, husbands or boyfriends acted as their advisors. Morio et al. also reported, in a questionnaire study in Phnom Penh, Cambodia,2 that almost all DCSW were single or separated and that their advisors were mainly their brothels' owners, while about one-third of IDCSW were married and two-thirds of them mentioned that their parents, husbands or boyfriends acted as their advisors. These indicate that social support for DCSW was poor and that the brothel owners had great influence with DCSW. In this study, when asked their reasons for commitment to brothel-based commercial sex work, 75 DCSW answered that they had selected the job in order to get money or they could not find another job. The instability of the socioeconomic situation induces poor women in to the commercial sex industry. Additionally, the other 27 DCSW answered that they were working in brothels because they had either been sold into this work or had been lied to. This indicates that quite a few women were involved in brothel-based commercial sex work against their will.

Sexual behaviour
Differences between the two types of CSW were noted with regard to their sexual activity and behaviour. The average number of clients for DCSW was 4.01 a day, but for IDCSW it was around one a day. The earnings per client of the DCSW were much lower than those of the IDCSW. This suggests that the DCSW offer their service to lower-income groups and that they have to have more clients than the IDCSW in order to make a living. However, this study did not find out the social strata of the clients. Several reports have indicated that lower charges for commercial sex work are related to higher risk of an HIV epidemic3,6,11–13 because the CSW have contact with clients frequently. As a logical consequence this must raise the risk of HIV infection. Additionally, HIV prevalence among the clients of lower class brothels may possibly be high. In this study, IDCSW daily earnings were higher than these of DCSW despite the small number of clients probably because their clients were richer. Furthermore, the IDCSW received a salary for their legitimate work and so it might not be necessary for them to have many clients in a day.2

Most of the DCSW possessed condoms and nearly half of them answered that they had used them in every sexual contact. Almost all the condoms which the DCSW had at that time had been provided by their brothels. On the other hand, only 24.5% of the IDCSW had condoms and 10.6% said they used them every time. Additionally, more than half of the condoms which the IDCSW had at the time of the questionnaire had been purchased by themselves. These results indicate that DCSW are managed by their brothel owners but IDCSW operate independently.

The DCSW had some knowledge of HIV infection. They also recognized the preventive role of condoms in HIV transmission. Several educational programmes on HIV prevention promoted by bodies such as non-governmental organizations, have been aimed at DCSW in Cambodia. It is likely that such education contributed to the knowledge of HIV infection of our subjects. Additionally, the Thai government's 100% condom use campaign14 for CSW might influence the results because this survey was carried out in a region near the Thai border where trans-border mobility is high.

Serological situation
Serological differences were also observed between the DCSW and the IDCSW. Seropositive rates for HIV and CT-IgG-Ab among DCSW were much higher than those among IDCSW. Prevalence of the CT-IgG-Ab seropositivity with higher titre was also very high among the DCSW, but relatively low in IDCSW. We examined C. trachomatis IgG antibody with ELISA to identify current and previous infection. The feasibility and validity of the technique has been confirmed previously.9,15–18 The IgG antibody indicates past infection but the appearance of very high titre, or more than a four-fold increase in pre-existing titre, can also signify acute infection.10,19–21 In this study, 51.7% of the DCSW had the higher titre which implies that active C. trachomatis was spreading into the population of DCSW at that time.

Relationships between risk factors and HIV seropositivity
In the univariate logistic regression analyses among the DCSW, current age and duration of commercial sex work showed a statistically significant association with HIV-Ab seropositivity. The reason is probably that long-term sexual activity raises the risk of HIV infection due to increased exposure to HIV. Commencement of commercial sex work at a younger age is considered as a risk factor of HIV infection. Griensven et al. reported in a study in Thailand that a younger age at commencement of commercial sex work was significantly related to HIV infection.4 In this study, however, the OR of HIV seropositivity among the DCSW who commenced commercial sex work aged under 18 was significantly low. The reason is probably that current age confounded the relationship between the age at commencement of commercial sex work and HIV-Ab seropositivity due to the short duration of commercial sex work. The other statistically significant relationships were not shown in the univariate logistic regression analyses among the DCSW and the IDCSW. Condom use is an effective method of protecting against HIV infection. A number of studies have shown an association between condom use and HIV seropositivity.36,8,12,22–25 In this study, however, there was no difference in the HIV seroprevalence between every time use and sometimes use. This result was also shown by several studies.4,26 It might be supposed that the subjects overreported the frequency of their condom use or they were infected with HIV before they began to use condoms.

On the relationship between HIV and other STD, CT-IgG-Ab seropositivity was significantly related to HIV-Ab seropositivity. The univariate logistic analyses on HIV-Ab with risk factors for the IDCSW also showed a significant relationship between HIV-Ab and CT-IgG-Ab.

The association between HIV with C. trachomatis has been demonstrated in several previous studies8,27–33 and it seems that active C. trachomatis infection increases the risk of HIV infection. There are, however, several possible explanations of the relationship between the two infections. In the first place, STD including HIV and C. trachomatis have the same behavioural risk factors, for example, inconsistent condom use and frequency of sexual intercourse. In the multivariate logistic regression analysis with adjustment for such risk factors, the result showed that the risk factors had some mutual relationship with HIV infection but acute C. trachomatis infection had an association with HIV infection independent of the sexually transmissible risk factors including the type of commercial sex work. Secondly, there are two possible relationships between HIV infection and C. trachomatis infection: (1) immunological changes due to HIV infection may favour C. trachomatis infection;34,35 (ii) C. trachomatis infection may encourage HIV infection, through a change in vaginal flora or a histological change in the vaginal epithelium.34,36 The present cross-sectional epidemiological study indicated a statistically significant association between HIV-Ab and CT-IgG-Ab seropositivity, however the causal relationship is not entirely clear. This study, however, suggested that C. trachomatis was prevalent prior to the HIV epidemic among the CSW because the rate of the CT-IgG-Ab positive individuals was much higher than that of the HIV-Ab positive individuals (72.2% and 40.5%) and it is not likely that the lower prevalence of HIV induced a higher prevalence of C. trachomatis. The prevalence of C. trachomatis and HIV among IDCSW was lower than among the DCSW even though they had a riskier behavioural pattern than the DCSW. The reason was probably that their relatively lower frequency of sexual contact was related with their lower prevalence of C. trachomatis and HIV.

Preventive strategies against HIV epidemic
In Cambodia, prostitution is prohibited by law, but it is hard to eliminate because it is a simple way for poor women to earn money. However, legal measures should be implemented because some women are involved in brothel-based commercial work involuntarily. Economic development is also very important: if there were other good jobs, many CSW would not undertake commercial sex work.

In this questionnaire survey, the DCSW who had learned about preventive methods against HIV from educational programmes tended to answer correctly on the routes of HIV transmission. However, their knowledge on HIV did not relate to their habit of using condoms. Laga et al. reported an effective intervention against HIV spread, which was a programme of STD treatment combined with condom promotion in Zaire.8 This report showed a dramatic decline in HIV incidence rate among female sex workers. Such combined programmes must be a relatively cost-effective intervention for the DCSW in the present study. Firstly, the DCSW live together with their colleagues in a particular place. The red light area is easily identified. Secondly, it is likely they might accept such interventions considering their high response to the questions of this study. Thirdly, more than 80% of the DCSW had been infected with C. trachomatis which is suspected of facilitating HIV transmission. The treatment of STD, including C. trachomatis, could reduce the possibility of HIV transmission.37,38

In this study, half the CT-IgG-Ab positive women did not answer that they had been infected with STD previously and none of them confirmed that they had been infected with C. trachomatis. They might not have been aware of C. trachomatis infection because a large percentage of C. trachomatis infected women remain asymptomatic.39 This indicates that not only medical treatment but also regular checkups for these C. trachomatis and other STD are very important. The treatment and checkup system for STD can also provide a good opportunity for prevention and education on HIV.

In comparison interventions for the IDCSW might be difficult because it is hard to identify where they are in the daytime and their lifestyles vary. The first step in HIV prevention for the IDCSW must be identifying their characteristics more clearly. Moreover, education on HIV is very important to improve the condom use rate because nearly half of them had no knowledge of HIV transmission and only 10.6% of them answered they had used a condom every time. Education by their employers may be effective because the IDCSW were highly co-operative towards their employers' recruitment to this study. Establishing a STD checkup and care system for IDCSW is also important; however, the cost would probably be expensive, compared with the system for DCSW.


    Acknowledgments
 
The research in this paper was partially supported by the Ministry of Education, Science, Sports and Culture, Japan on grant-in-aid for International Scientific Research (No. 09041189). K Ohshige is in receipt of Research Resident Fellowship from the Japanese Foundation for AIDS Prevention.


    References
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
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