ORIGINAL STUDY. Symptoms of Sexually Transmitted Infections and Care-Seeking Behaviors of Male Clients of Female Sex Workers in Bangladesh

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1 ORIGINAL STUDY Symptoms of Sexually Transmitted Infections and Care-Seeking Behaviors of Male Clients of Female Sex Workers in Bangladesh Anisuddin Ahmed, MS,* Laura J. Reichenbach, MPA, ScD,* and Nazmul Alam, MPH, DrPH*Þ Background: In Bangladesh, male clients (MCs) of female sex workers (FSWs) represent diverse occupational categories from different socioeconomic strata, and they are considered a bridging group to transmit sexually transmitted infections (STIs) to their spousal and nonspousal female partners. This study aimed to better understand sexual behaviors, STI symptoms, and care-seeking behaviors among MCs of FSWs in Bangladesh. Methods: A cross-sectional study was conducted among MCs from November 2005 to July 2006 in 3 types of sex trade settings in Bangladesh. Of 1565 MCs included in this study, 531 were from brothels, 515 from hotels, and 519 from street-based settings. Results: Among the MCs, 32.2% reported having had STI symptoms within the last 1 year before the interview and 81.5% sought care for those symptoms. Among those who reported symptoms, 44.5% received treatment from pharmacies, 37.4% received treatment from qualified medical professionals, 8.6%, received treatment from nongovernment organization clinics, and 7.8% went to herbal providers. Male clients who had only 1 to 4 years of schooling were 2.4 times more likely to have STI symptoms (adjusted odds ratio [OR], 2.4; 95% confidence interval [CI], 1.5Y3.8) compared with the MCs having 10 or more years of schooling. The MCs who had sex with more than 3 nonmarital sexual partners in the last month were 2 times more likely to have STI symptoms (adjusted OR, 2.0; 95% CI, 1.4Y2.8). The MCs who used condoms consistently in their non-marital sexual contacts were significantly less likely (adjusted OR, 0.4; 95% CI, 0.3Y0.6) to have STI symptoms. Conclusions: Reported risk behaviors, STI symptoms and care-seeking behavior suggest that MCs are a potential risk group for transmission of HIV and STIs. The study findings underscore the need to target HIV/ STI prevention intervention for MCs, which are predominantly geared toward FSWs. Bangladesh has, so far, maintained low HIV prevalence rates (G1.0%) among the general population and in most-at-risk populations. 1 However, the country remains vulnerable due to several risk factors including a large commercial sex industry, From the *Centre for Reproductive Health, International Centre for Diarrhoeal Disease Research, Bangladesh, Mohakhali, Dhaka, Bangladesh; and Unité de santé internationale, Université de Montréal/CRCHUM, Montréal, Canada Supported by Australian Agency for International Development, Grant Number The International Centre for Diarrhoeal Disease Research, Bangladesh, acknowledges with gratitude the commitment of Australian Agency for International Development to its research efforts. Conflict of interest: None declared. Correspondence: Nazmul Alam, MPH, DrPH, Centre for Reproductive Health, International Centre for Diarrhoeal Disease Research, Bangladesh, Mohakhali, Dhaka 1212, Bangladesh. nazmul@ icddrb.org. Received for publication May 17, 2012, and accepted August 28, DOI: /OLQ.0b013e e Copyright * 2012 American Sexually Transmitted Diseases Association All rights reserved. unsafe injecting practices among injecting drug users, high rates of curable sexually transmitted infections (STIs) among most-atrisk populations, and low consistent condom use by sex workers. 2 Globally, heterosexual commercial sex is thought to be a major driver of the HIV epidemic. 3 Studies show that male clients (MCs) of female sex workers (FSWs) are at greater risk for acquiring STIs including HIV and of transmitting infections to their sex partners including wives and girlfriends. 4Y6 In Bangladesh, approximately 18.0% of the men from the general population reported having had nonmarital sexual relationship in the last 1 year. 7 Male clients of FSWs represent diverse occupational groups including truckers, rickshaw pullers, salaried office workers, students, and businessmen. 8 Among the different types of MCs of the FSWs, the transport workers (truckers or their helpers and rickshaw pullers), students, and businessmen are reported to buy sex most frequently from FSWs. 9,10 According to the fifth round of the national sero- and behavioral surveillance, 61.4% of the truckers/helpers and 50.0% of the rickshaw pullers were reported to buy sex from FSWs in the last month before the interview. Only 5.4% of the rickshaw pullers and 6.4% truckers reported using a condom during their last sex with FSWs. 11 HIV prevalence is reported to be low among FSWs in Bangladesh, but they have high burden of other STIs. A study among brothel-based FSWs reported rates of 67.4% cervical/ vaginal infection, 12 and another study among hotel-based FSWs found that 57.0% of them were STI symptomatic, of which 35.8% were positive for Gonorrhea, 43.5% for Chlamydia, 8.5% for syphilis, and 4.3% for trichomoniasis. 13 It is therefore anticipated that MCs of FSWs would be at risk for infection with STIs, given the high burden of STIs among FSWs and the low reported use of condoms. There is, however, very limited information available on burden of STIs or STI symptoms among MCs of FSWs in Bangladesh and their care-seeking behavior. A pilot study among clients of brothel-based FSWs found that 12.8% were positive for 1 or more STIs, but the study did not report about care-seeking behavior for STIs. 14 Understanding sexual behaviors and risk factors, identifying the burden of STIs, and documenting care-seeking behavior are important to undertake effective interventions for the prevention of HIV and AIDS in a population. Currently, HIV prevention interventions focus mostly on FSWs and less on their MCs in Bangladesh. These interventions are less effective because the MCs greatly influence the use of male condoms during commercial sex. This study attempts to better understand sexual behaviors, reported STI symptoms, and care-seeking behavior among MCs of FSWs from brothel, street, and hotelbased sex trade settings in Bangladesh. METHODOLOGY Study Design A cross-sectional survey was conducted among MCs of FSWs from November 2005 to July 2006 in brothel, street, and hotel-based sex trade settings in Bangladesh. Male clients of street Sexually Transmitted Diseases & Volume 39, Number 12, December

2 Ahmed et al. and hotel-based settings were recruited from Dhaka and Chittagong metropolitan areas, whereas MCs in brothels were recruited from 2 large brothels (Doulatdia and Tangail) in Dhaka division. Sampling Techniques Multistage cluster sampling technique was adapted for selection of MCs from each setting. A total of 81 street-based cruising spots in and around railway platforms, bus terminals, ship ports, parks, and cinema halls were listed in Dhaka and Chittagong by project staff with the help of 2 collaborating nongovernment organizations (NGOs) working with street-based FSWs. From the list, 30 cruising spots were selected by simple random sampling method. The MCs of street-based FSWs were recruited through an intercept method in which men at the selected cruising spots were randomly approached and asked a series of questions to build rapport and determine eligibility through asking screening questions if they bought sex in the last 1 month in such settings. To identify MCs of hotel-based FSWs, we listed a total of 81 hotels in Dhaka and Chittagong metropolitan area with the help of 2 local NGOs working with this population. Only hotels that hosted sex trade during the last 3 months and with attendance of at least 5 FSWs per day in the last 7 days were included in the listing. From this list, 30 hotels were selected by simple random sampling. In each hotel, MCs were consecutively selected for exit interview. Doulatdia and Tangail were selected because they contain a large number of brothels with a series of rooms hosting FSWs. Brothels in Doulatdia and Tangail were mapped by the study staff. The number of rooms and number of FSWs in each brothel room were enumerated to make clusters within the brothels. From 50 of such clusters (27 in Tangail and 23 in Doulotdia) each having 30 rooms, 15 clusters were selected randomly from each of the 2 brothels. Male clients were consecutively selected from those clusters for exit interview. For brothel and hotel settings, the recruitment process was done during daytime, but for streetbased settings, MCs were recruited after sunset. The study was approved by the research review committee and ethical review committee of icddr,b. Data Collection A semistructured questionnaire was administered by trained male interviewers to collect information on sociodemographic characteristics, HIV/AIDS knowledge and risk perception, sexual behavior and condom use practices, STI symptoms, and treatment seeking behavior. Data quality was monitored through close supervision at the field level and an automated data management system with logical restrictions to prevent data entry errors. STI symptoms were determined if MCs self-reported having had any symptoms suggesting STIs in the last 12 months before the interview. We considered urethral discharge, genital ulcer, and pain during urination among the symptoms suggesting STIs. Consistent condom use was defined as use of condom in the premarital or extramarital penetrative sex with FSWs, casual female partners, or males/transgenders in the last 1 month before the interview. Data Analysis Data analysis was done using SPSS (version 17). Descriptive analyses were performed to compare sociodemographic characteristics of the study participants by STI symptoms reported by MCs using W 2 test. Logistic regression model was fitted on having STI symptoms for MC s sexual behavior to assess relationship. Odds ratios (ORs) were estimated with adjustment for sex trade settings and sociodemographic factors including MC s age, education, marital status, income, occupation, and sexual behaviors. RESULTS A total of 1565 MCs were interviewed in the study. Of these, 531 were from brothels, 515 were from hotels, and 519 were from street settings. We excluded 151 who did not have any knowledge about STIs or their symptoms because these were the focus of the study. This exclusion was based on the responses given by the MCs during interviews on specific questions assessing knowledge of STIs and their symptoms. There were no significant differences in sexual and condom use behaviors between the groups excluded and those who were included in the study. Sociodemographic Characteristics of the MCs Of the remaining 1414 MCs included in this study, most (55.7%) were between 20 and 29 years of age, whereas TABLE 1. Sociodemographic Characteristics of MCs of FSWs Reporting STI Symptoms in the Last 12 Months Sociodemographic Characteristics Had STI Symptoms (n = 455) % of MCs of FSWs Had No STI Symptoms (n = 959) Total (n = 1414) Sex trade settings Street Brothel Hotel G0.01 Age, y e Y Y Q G0.01 Schooling, y Y Y Q G0.01 Average monthly income* in Taka) e Y Y10, , G0.01 Marital status Never-married Ever-married Occupation Businessman General services holder Transport worker Construction worker Other day labor Farmer Student Unemployed Service in defense/ police Porter Fisherman Other G0.01 *USD 1 = 68.9 Taka in P 980 Sexually Transmitted Diseases & Volume 39, Number 12, December 2012

3 Male Clients of FSWs in Bangladesh approximately one-tenth (8.9%) were 19 years or younger. Nearly one-third (28.9%) of the MCs never attended school, and one-fourth (23.2%) had 10 or more years of schooling. Nearly one-third (27.2%) of the MCs had an average monthly income of Taka 3000 (USD 44.0; USD 1 = 68.9 Taka in 2006) per month or less. More than one-half (53.4%) of the MCs were never married. Approximately three-fifths (60.5%) of the MCs reported their occupation as businessmen, general service holders, students, or police/defense employees. Nearly one-half (47.3%) of the MCs of street-based FSWs reported experiencing STI symptoms in the last 12 months compared with 27.9% of MCs in brothel and 24.8% in hotelbased settings (Table 1). Male clients younger than 30 years were more likely (73.4%) to report STI symptoms in the last 12 months. Approximately one-third (32.3%) of the MCs who reported having STI symptoms had never attended school. On the contrary, STI symptoms were less common (15.8%) among those who had 10 years or more of schooling. Likewise, MCs belonging to lower-income groups (Taka e5000 [USD 73.0]) reported more STI symptoms compared with those in higherincome groups (Taka 910,000 [USD 145.0]; 66.8% vs. 7.3%, respectively). The never-married MCs reported more STI symptoms compared with ever-married (56.9% vs. 43.1%, respectively) group. Significant differences in those who had STI symptoms compared with those who did not have symptoms were observed by professional categories of the MCs. Transport workers and day laborers had a significantly higher proportion of STI symptoms. Sexual Behavior of the MCs by Self-Reported STI Symptoms Among the MCs, most (66.2%) had their first sexual experience by 19 years of age (Table 2). The MCs who had their first sexual experience at an early age (e19 years) reported more STI symptoms (76.2%) as compared with those who had their first sexual experience after 19 years of age (23.8%). Most (92.7%) of the MCs had their first sexual relationship with nonmarital sexual partners. More than four-fifths (85.3%) of the MCs reporting STI symptoms had a sexual relationship with FSWs in the last month. There was a significant difference in STI symptoms (7.1% vs. 1.2%) of those who had male/transgender sex partners in the last month. Significantly higher proportion of those who had more than 3 partners in the last month reported having had STI symptoms (34.6% vs. 19.7%). Only 9.4% of the MCs reporting STI symptoms in this study used condoms consistently during their non-marital sexual practice in the last month; 26.9% who did not have any STI symptoms used condoms consistently. Illicit substance use was significantly associated for having STI symptoms in the last 12 months. Among the MCs who had STI symptoms, 43.3% ever-used illicit TABLE 2. Sexual Behaviors of MCs by STI Symptoms in the Last 12 Months Had STI Symptoms (n = 455) % of MCs of FSWs Had No STI Symptoms (n = 959) Total (n = 1414) Age at first sex of MCs, y e Y Y G0.01 Types of partner at first sex Wife Casual female partners FSWs Males/transgenders G0.01 Types of partner in the last month n = 448 n = 904 n = 1352* FSWs Casual female partners Males/transgenders G0.01 No. any types of partner in the last month Y G0.01 Condom used consistently in the last month Yes No G0.01 Used illicit substances ever n = 455 n = 959 n = 1414 Yes No G0.01 Types of illicit substances n = 197 n = 241 n = 438 Cannabis G0.01 Alcohol Heroin Sleeping pill Fensidyl Injecting drugs Tobacco powder Others *Sixty-two clients did not have any sexual contacts in the last month. Female sex workers, Casual female partners, Males/transgenders. Multiple responses. P Sexually Transmitted Diseases & Volume 39, Number 12, December

4 Ahmed et al. substances including cannabis (70.1%), alcohol (46.2%), heroin (8.1%), sleeping pill (7.6%), fensidyl (6.1%), and other injecting drugs (2.5%). Reported STI Symptoms and Care-Seeking Behaviors Among the 1414 MCs of the FSWs, approximately one third (32.2%) reported having had STI symptoms in the last 12 months. Almost 72.7% had experienced STI symptoms at least once, approximately 16.9% had experienced STI symptoms 2 times, and 10.2% had experienced STI symptoms more than 2 times in the last 12 months. When asked about their care seeking for STI symptoms, 18.5% mentioned that they did not seek treatment for STI symptoms. Of those who received treatment, nearly one-half (44.5%) received treatment from pharmacies, 37.4% received treatment from qualified medical professionals (public/private), 8.6% received treatment from NGO clinics, and 7.8% went to herbal providers. The relationship between income level and source of care-seeking for STIs symptoms is presented in Figure 1. Briefly, low-income MCs mostly sought care to the pharmacies as compared with qualified providers (50.0% vs. 26.9%); however, pharmacies remained as a major source of care-seeking for high-income MCs, as well (46.7% vs. 42.2%). Determinants of STI Symptoms Among MCs To determine associated factors of having STI symptoms, we estimated crude and adjusted ORs (Table 3). Compared with MCs 40 years or older, all other age groups except the 30- to 39-year age group were more likely to have STI symptoms. For the MCs 19 years or younger, the magnitude of OR was highest (adjusted OR, 1.7; 95% confidence interval [CI], 0.9Y3.3) and was relatively low in the higher-age groups. Compared with MCs having 10 or more years of schooling, those who had only 1 to 4 years of schooling (adjusted OR, 2.4; 95% CI, 1.5Y3.8) were 2.4 times more likely to have STI symptoms. Lower-income MCs group (average monthly income GTaka 5000 [USD 73.0]) were 73.0% more likely to have STI symptoms as compared with those in the higher-income group (9Taka 10,000 [USD 145.0]). The ever-married MCs were approximately 14.0% more likely to have STI symptoms than the never-married MCs. The MCs having male/transgender sex partners were almost 3 times more likely to have STI symptoms (adjusted OR, 2.9; 95% CI, 1.4Y6.3). The MCs who had sex with more than 3 nonmarital sexual partners in the last month TABLE 3. Determinants ORs of MCs With STI Symptoms in the Last 12 Months Crude OR (95% CI) Adjusted OR (95% CI)* Sex trade settings Street 2.5 (1.9Y3.4) 1.1 (0.8Y1.6) Brothel 1.2 (0.9Y1.6) 1.1 (0.8Y1.5) Hotel Age, y e (1.3Y3.6) 1.7 (0.9Y3.3) 20Y (0.9Y1.9) 1.2 (0.7Y2.0) 30Y (0.5Y1.1) 0.7 (0.4Y1.2) Q Schooling, y (1.4Y2.8) 1.3 (0.8Y2.0) 1Y4 3.7 (2.5Y5.4) 2.4 (1.5Y3.8) 5Y9 1.4 (1.0Y2.0) 1.1 (0.8Y1.6) Q Average monthly income (in Taka) e (1.5Y3.6) 1.3 (0.7Y2.3) 3001Y (1.5Y3.4) 1.7 (1.0Y2.9) 5001Y10, (1.1Y2.6) 1.6 (1.0Y2.5) 910, Marital status Never-married Ever-married 0.8 (0.7Y1.0) 1.1 (0.8Y1.6) Occupation Businessman 0.8 (0.5Y1.6) 0.7 (0.3Y1.4) General services holder 1.0 (0.6Y1.9) 0.7 (0.3Y1.5) Transport worker 1.6 (0.9Y3.1) 0.8 (0.4Y1.7) Other day labor 2.8 (1.4Y5.5) 1.1 (0.5Y2.6) Farmer 0.7 (0.3Y1.6) 0.6 (0.2Y1.5) Student Service in defense/police 0.8 (0.3Y2.6) 0.6 (0.2Y2.3) Porter 2.4 (0.8Y6.8) 0.9 (0.3Y2.8) Types of partner in the last month FSWs Casual female partners 1.1 (0.7Y1.7) 0.9 (0.6Y1.5) Males/transgenders 6.3 (3.1Y12.6) 2.9 (1.4Y6.3) No. any types of partner in the last month Y3 1.7 (1.3Y2.2) 1.5 (1.1Y2.0) (2.1Y3.8) 2.0 (1.4Y2.8) Condom used consistently in the last month Yes 0.3 (0.2Y0.4) 0.4 (0.3Y0.6) No Used illicit substances ever Yes 2.3 (1.8Y2.9) 1.7 (1.3Y2.2) No *Adjusted for MC s age, education, marital status, income level, occupation, and sexual behavior. USD 1 = 68.9 Taka in Figure 1. Proportion of MCs with STI symptoms who sought care from providers by income level. were 2 times more likely to have STI symptoms (adjusted OR, 2.0; 95% CI, 1.4Y2.8). The MCs who used condoms consistently in the last month during their non-marital sexual practice were significantly less likely (adjusted OR, 0.4; 95% CI, 0.3Y0.6) to have STI symptoms. The MCs ever using any illicit substances were 70.0% more likely to have STI symptoms than MCs who did not use illicit substances (adjusted OR, 1.7; 95% CI, 1.3Y2.2). DISCUSSION This study underscores a high rate (32.2%) of reported STI symptoms among the MCs and also high overall care-seeking 982 Sexually Transmitted Diseases & Volume 39, Number 12, December 2012

5 Male Clients of FSWs in Bangladesh behaviors for STI symptoms, although mostly from informal providers. High rates of STI symptoms correspond with higher level of sexual behaviors reported by the MCs in this study and burden of STIs among FSWs, as reported in other studies in Bangladesh. 12,13 Ever-married clients were more likely to have STI symptoms than the never-married respondents. These findings suggest that this group of MCs is a potential source of transmitting HIV/ STIs to the general population including to their spouse. Another key finding of the study is that the nearly three-fourths (72.8%) of the MCs with symptoms of STIs also visited 2 or more nonmarital sexual partners including FSWs and casual female partners or male/transgender in the past 1 month. Previous studies have suggested concurrent partnerships to be a significant risk factor in the spread of STIs in the general population. 15Y17 One approach that has been adopted in some countries to address this is to encourage men to limit their number of sexual partners and to avoid multiple partners. Experiences from Uganda and Thailand suggest that reducing the numbers of multiple sexual partners has contributed, at least in the short term, to holding the HIV epidemic. 18Y20 Certain sociodemographic characteristics of the MCs were found to have a significant role in experiencing STI symptoms in the last 12 months. Male clients of street-based FSWs were more likely to have STI symptoms than the MCs of brothel-based or hotel-based FSWs. This may be because these MCs belong to a lower-income group, have lower rates of consistent condom use, and have poor knowledge about HIV and other STIs. Younger clients (aged G30 years) with no formal education, lower average monthly income (TakaG5000 [USD 73.0]) also had higher rates of reported STI symptoms. Transport workers and day laborers who most often represent a lower socioeconomic status were reported to have had more STI symptoms compared with other types of occupation. Reported STI symptoms among the MCs varied significantly by illicit substance use status and condom use rates during commercial sex in the last month. Male clients were more likely to have had STI symptoms if they used illicit substances (adjusted OR, 1.7; 95% CI, 1.3Y2.2) and less likely if they used condoms consistently (adjusted OR, 0.4; 95% CI, 0.3Y0.6) during commercial sex act in the last month. A higher proportion of MCs reported care-seeking for their STI symptoms (81.5%), but mostly from informal providers including pharmacies (44.5%) and herbal providers (7.5%). The quality and appropriateness of the treatment provided by these informal providers are not known. Informal providers including pharmacies continue to play a vital role in curative services for STIs and other diseases in developing countries. In Thailand, 39.0% of men who had risky sexual behavior sought treatment for their STIs at a pharmacy. 21 Quality of care for services provided by informal providers may not be adequate because of their limitation in knowledge and skills; therefore, further initiatives to improve their skills and knowledge are recommended. 22 Effort should also be made to focus on enhancing care-seeking behaviors among MCs of FSWs with STI symptoms and to address the issues hindering care-seeking for STI symptoms. Recruitment of MCs into a study to interview them about their sexual exposure, STI-related symptoms, and care-seeking for such symptoms is challenging. Given our sampling approach of recruiting clients facilitated by the FSWs and the other stakeholders in the area, it is likely that the sample represents actual clients. We used experienced and well-trained male data collectors and involved the gatekeepers and the FSWs to keep the refusal rate to a very negligible rate (0.7%), which was otherwise expected to be higher, as found in India. 23 A limitation of the study is that we only addressed self-reported STI symptoms that could not be confirmed by any laboratory or clinical procedures. Given that many STIs are asymptomatic or present with atypical symptoms in some cases and the possibility of underreporting because of social desirability or recall biases, the study results may underestimate the true levels STIs in the population. The level of risk behaviors and symptoms suggesting STIs reported in this study are indicative of MCs as being potentially high-risk groups and important bridges for transmission of HIV and STIs to women in the general population in Bangladesh. The findings presented here have important programmatic implications for targeting prevention strategies to address the needs of MCs of FSWs. The current focus of these prevention strategies is predominantly geared toward FSWs. We call for additional research to determine the true prevalence of STIs and associated risk factors in the MC of FSWs rather than just relying on self-reported symptoms. Our findings also suggest the need to strengthen interventions for improving the skills of informal providers such as pharmacists and traditional practitioners for better management of STIs, especially referral and prevention services. REFERENCES 1. 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