Several interventions that target sex workers (SWs) by combining the diagnosis and treatment of sexually transmitted infections (STIs) with condom promotion have been conducted in developing countries and have been proven effective in reducing HIV incidence and/or STI rates amongst these high-risk groups.1-6 Mathematical models suggest that such targeted interventions are especially effective in countries that have not yet developed a major HIV epidemic,7,8 and there is growing evidence about them being cost-effective.9 However, recent community-based trials examining prevention of STI as a means to prevent HIV-1 did not have an impact on HIV seroconversion rates.10-13
Previous studies suggest that offering STI care may be feasible and effective in primary health care settings. Additionally, their control is a key element as part of an essential health package.14 However, the integration of STI prevention and care services into health settings is a challenge in STI control,15 and there is little evidence on the efficacy of delivering such services through the public sector in Central America and, in particular, dedicated to SWs.16 The success of HIV prevention interventions can be substantially improved when the structural factors that shape or constrain individual behavior, such as gender, policies, and power, are taken into account.17 However, the incorporation of structural approaches in HIV prevention is still limited by scarce data concerning their effectiveness in averting HIV cases.18
In Guatemala, STI control is a growing concern.19 The country is classified as having a concentrated HIV epidemic20 mainly driven by heterosexual transmission.21 However, the epidemic is rapidly increasing, and recent reports have shown a prevalence of HIV exceeding 1% in pregnant women.20 SWs present an HIV prevalence as high as 4.6%22 and high rates of syphilis (10.0%), Chlamydia trachomatis (20.5%), and Neisseria gonorrhoeae (10.7%).23 This high-risk group contributes to the spread of the STI/HIV epidemic to the general population through clients and sexual partners.24
Within this context, there is an urgent need for SWs to be targeted by effective STI/HIV prevention and care approaches. Yet such interventions are rarely implemented and evaluated, in concentrated HIV epidemics in particular.25 In March 2005, in the context of the UALE Project (UALE means ‘health’ in Latin), we established an open cohort of SWs with ongoing recruitment in the province of Escuintla, Guatemala. It has been run by Fundació Sida i Societat, a nonprofit organization that specializes in providing STI and HIV prevention and care services in resource-constrained settings. The UALE Project is a multilevel preventive intervention originally addressed to SWs. The project includes a biomedical component that offers early diagnosis and treatment of STIs by means of setting up 3 STI clinics within the community health care centers (HCC) of 3 municipalities and of strengthening their existing public laboratories; a behavioral component, by means of individual counseling, focal group discussions, and health education workshops, with SWs and key groups such as the owners of commercial sex establishments (CSE). These activities are organized by health educators and comprise condom negotiation skills with both clients and partners. Lastly, a structural component, aimed at decreasing the criminalization of SWs, increasing access to clinical and preventive services, and improving local prevention and control recommendations. The latter component consists of organizing sensibilization meetings with the owners of CSE and the police, advocacy meetings with the media and policy makers, and establishing boundaries with relevant governmental and nongovernmental organizations. In particular, a great effort is invested in moving from an individual control-based approach toward a health promotion approach.
Our aim is to assess the impact of such intervention on STI/HIV incidence and trends in the use of condoms and HIV knowledge after the initial three and a half years of operation.
The province of Escuintla (609,478 inhabitants26) is located to the southwest of Guatemala city. It ranks first among all Guatemala provinces in reported HIV rates.27 Factors contributing to the high HIV prevalence include widespread sex work, STI treatment provided through the public sector is of poor quality, and the population is highly mobile. The sugarcane harvest attracts seasonable migrant male workers. The Pan-American road crosses through the province, which is highly frequented by truck drivers and migrants from surrounding countries that head to the Mexican Border. Initial mapping exercises showed that sex work was mainly based in CSE. First, we conducted a qualitative study to identify local perceptions and needs, which was used to design the prevention and care services response.28
SWs were found to lack skills related to condom use and to perceive judgmental attitudes of clinic staff that discouraged them from attending the HCC. In Guatemala, sex work is regulated. The Health Department mandates weekly medical checkups (referred to as a prophylaxis visit). However, most of the SWs came less often and were only examined sporadically. Those prophylaxis visits often consisted only of updating a medical stamp, which can be required at any time by local authorities. The STI clinics and the laboratory facilities were integrated within the community HCC of Escuintla (provincial capital), Santa Lucia Cotzumalguapa, and Puerto de San José.
SWs were invited to come to the clinics on a 6-month basis for a follow-up visit in which STI/HIV screening and treatment was offered. However, a drop-in service was made available for additional health requirements. We included women who identified themselves as SWs and who signed the written consent form. Each follow-up visit included taking a detailed history, assessing the risk of being infected with an STI, and a clinical examination. A speculum examination was performed during which genital swabs were taken for laboratory screening of STI. Initially they received syndromic treatment for symptomatic STI and information on STI/HIV and reproductive health. A health educator provided HIV counseling and recorded data on sociodemographic characteristics, sexual behavior, and HIV knowledge in a structured questionnaire. Finally, venous blood was drawn for syphilis and HIV testing. SWs were requested to come to the clinic after 7 days. They were reexamined, received post-test counseling sessions, and aetiological treatment for laboratory-confirmed infections. Any genital tract infection identified was treated according to national guidelines. HIV-positive cases were referred to the appropriate hospitals. All services were dispensed at no charge at the clinics.
All tests were performed at the HCC laboratory. The presence of Trichomona vaginalis and yeasts were examined by wet mount preparation microscopy of secretions collected from the posterior vaginal fornix. An endocervical swab was tested by enzyme immunoassay (Chlamydia Ag Card; Ulti med products, GmbH, Ahrensburg Germany) to detect Chlamydia trachomatis. A second endocervical swab was cultured on modified Thayer-Martin medium for the diagnosis of Neisseria gonorrhoeae.29
Syphilis serology was performed using the Venereal Diseases Research Laboratory test (VDRL; Murex Biotech Limited, Dartford, United Kingdom), and all reactive samples were confirmed using Treponema pallidum hemagglutination test (Immutrep TPHA; Omega Diagnostics Ltd, Ontario, Canada). The VDRL test was done quantitatively after the qualitative test result was positive. Active syphilis was diagnosed when both the VDRL and the TPHA tests were positive, regardless of the VDRL title and treatment history. All sera underwent testing for HIV using a rapid test (Determine HIV-1/2, Abbott Laboratories, Tokyo, Japan). All reactive samples were confirmed by enzyme-linked immunosorbent assay (Bioelisa HIV-1 + 2; Biokit, Lliçà d'Amunt, Spain). Discordant results were solved by repeating both tests.
The main outcome measures were STI and HIV incidence that were ascertained by laboratory results. We assumed that those SWs with an STI laboratory diagnoses and who were correctly treated for STI were cured. We defined STI cases as new infections when the SWs were diagnosed with an STI at the current visit and either were not diagnosed with that same STI at the previous visit or were treated for that STI after the previous visit. Once a SW was diagnosed with an STI, we considered her at risk again for that STI after the day on which specific treatment was finished. HIV incidence was defined as a change in serologic result occurring during follow-up from HIV negative to HIV-1/2 positive. The frequency of condom use (measured as ‘always,’ ‘almost always,’ ‘rarely,’ and ‘never’) during vaginal sex with a new client in the past 6 months was further recategorized as consistent use (‘always’) and not consistent (‘all others’). HIV-related knowledge was assessed by asking all women to identify HIV prevention measures and transmission routes. Answers were not prompted.
All data were analyzed and described using STATA version 9.0 (StataCorp, College Station, TX). To calculate the lost to follow-up, we defined temporal criteria: those women who undertook the last follow-up visit before February 2008 (corresponding with the mean time between follow-up visits) were excluded. For descriptive purposes, baseline characteristics, condom use, HIV-related knowledge, and STI/HIV prevalence were determined according to the year of recruitment and compared using the test for trends for independent samples.
Because only 181 of the 1554 SWs exceeded 3 follow-up screening visits, we restricted our analysis from the first visit (baseline) through the third follow-up visit. We compared whether SWs who completed at least 3 follow-up visits differed from those with less than 3 follow-up visits with regard to sociodemographic characteristics, sexual behavior, and HIV-related knowledge (using Pearson χ2 test and Student t test).
We evaluated time trends over the follow-up visits in condom use, HIV-related knowledge, and STI incidence using the information of the total group of 1554 SWs. To obtain the incidence rate and the relative risk of STI corresponding to the change from a 6-month follow-up visit to the next, we took into account the correlations between repeated measurements on individual women using generalized estimating equations assuming a Poisson distribution. We repeated all the analysis based on the information from only those 293 SWs who had completed at least 3 follow-up visits and compared with the trends observed among the 1554 women. HIV incidence was calculated globally and for 4 consecutive study years. Trends were calculated using the χ2 test for linear trends.
From March 2005 to September 2008, 1554 SWs attended the STI clinics at least once. Taking into account the temporal criteria defined to calculate lost to follow-up, 665 of 1401 (47.39%) were lost to the first follow-up visit, 205 of 1203 (17.04%) to the second, 94 of 939 (10.01%) to the third, and 65 of 720 (9.03%) to the fourth. The average time among those visits was 215.22 days (SD: 96.46). At baseline, 52.11% self-reported STI symptoms, vaginal discharge being the most common one (44.52%). Seventeen percent were indigenous. More than half (56.76%) were illiterate. Thirty-seven percent were migrant SWs from surrounding countries, of whom, 61.22% were illegal and 62.53% had arrived in Escuintla within the last year. Only 5.29% were married. However, 83.34% had at least 1 child, and 23.48% reported having had an abortion. The duration of sex work was less than 1 year in 59.63% of SWs. Most of the sex encounters (74.23%) took place in CSE. None reported ever using intravenous drugs. Less than 4.40% reported cocaine, and 1.74% reported crack consumption. The proportion of SWs who reported ever being in prison was low (6.98%).
Sociodemographic characteristics, the use of condoms, HIV-related knowledge, and STI/HIV prevalence did not differ significantly at baseline according to the year of recruitment (data not shown). Table 1 shows sociodemographic characteristics, sexual behavior, and HIV-related knowledge at baseline comparing SWs with at least 3 follow-up visits with the 1554 SWs.
Changes in Sexual Behavior and HIV-Related Knowledge Over Time
The proportion of participants who reported consistent condom use with both new and regular clients in the last 6 months was initially high and increased significantly over follow-up visits (Table 2). There was a reduction in reported consistent condom use with regular partners in the last 6 months from 38.22% at the baseline visit to 33.30% at the third follow-up visit. The proportion of women who reported condom use as an HIV preventive measure significantly increased from the baseline visit through the third follow-up visit (87.00%-97.22%), as did the proportion of women who reported knowing about mother-to-child transmission of HIV (27.54%-49.40%). When we repeated the analysis with only the 293 women who had completed at least 3 follow-up visits, the upward trend in condom use with clients and HIV-related knowledge remained present and significant (data not shown).
Changes in STI and HIV Incidence Over Time
The incidence of all STI (Table 3) significantly declined over each follow-up visit, with the exception of active syphilis. For the latter infection, we found a reduction from the first to the last follow-up visit, but this decline was not significant. When we repeated the analysis based on the 293 women who undertook at least 3 follow-up visits, a significant declining trend was still present for all STI, with the exception of active syphilis (Table 3). Over three and a half years, the global incidence of HIV was 0.41 per 100 person-years. Over the study period, HIV incidence significantly dropped from 1.85 per 100 person-years in 2005 to 0.42 per 100 person-years in 2008 (P value for trend 0.046), remaining almost constant in 2006 at 1.86 per 100 person-years and being 1.75 per 100 person-years in 2007.
The UALE Project is one of the few comprehensive interventions for the prevention and control of STI/HIV among SWs in Central America that includes a clinical, behavioral, and structural component. The STI/HIV services were integrated into the HCC and offered in real-life conditions for a targeted population in an area of high STI prevalence. The project was run almost exclusively by local professionals who received local salaries. We monitored outcomes using clinical, behavioral, and laboratory routinely collected data. In three and a half years, many SWs attended the clinic at least once suggesting that this relatively simple intervention is feasible for this group in Guatemala.
The results suggest that regular STI/HIV screening and treatment combined with condom promotion and sexual risk prevention is effective in reducing HIV and STI acquisition in SWs receiving the intervention. Although most randomized controlled trials failed to show that the control of STIs is effective in averting HIV,2 as in other cohort studies, we have found such protective effect in HIV incidence.1,3-5 Over the study period, the incidence of HIV significantly dropped, as in other cohort studies conducted among high-risk groups.1,5,10,30 At the third follow-up visit, the incidence of all STI had significantly dropped, although the reduction was not significant for syphilis, like in other studies.3 This might be partly due to the observed lack of compliance with the treatment regimens31 and might reflect high syphilis rates among both SWs partners and clients.22
It is not possible to separate the effect on STI and HIV incidence from the different components of the intervention. However, factors that might have contributed to the decline in STI and HIV incidence are as follows: first, the adoption of safer sexual behaviors through the use of condoms with clients.30 Despite methodological limitations, we have observed an increase in self-reported condom use with clients that corresponds with a reduction in infection rates, the direction of change is consistent, it is biologically plausible, and there is evidence that condom promotion is effective in reducing HIV incidence. Second, over the study period, women entering the study did not differ on baseline characteristics and STI/HIV prevalence, which suggests that the intervention had an impact in declining STI/HIV incidence, risk behaviors, and increasing HIV-related knowledge. However, we cannot rule out that the follow-up time was not long enough to observe significant contextual changes that might have affected the results.6 And third, the decline in the incidence of STI among cohort participants might have contributed to a subsequent decline in HIV incidence.10,30
The study has some bias. We cannot rule out a greater loss to follow-up in subgroups at greater HIV risks.30,32 At baseline, women with at least 3 follow-up visits reported a significantly less risky behavior than those with less than 3 follow-up visits, which might have led to a healthier cohort during the latter follow-up period.30,33 However, when we repeated all the analysis based on only those women who had completed at least 3 follow-up visits, the HIV and STI downward trends were still present and remained significant, like previously, which points to a positive effect of the intervention on dropping the incidence of HIV. Data on sexual behavior were reported by participants. Therefore, recall bias and misreporting, especially when answering sensitive topics, cannot be excluded.34 Despite STI and HIV incidence dropping, potential impact at this stage is limited by high loss to follow-up, which was favored by the high mobility of SWs. A proportion as high as 47.82% attended the clinics only once. We need to reach community-based SWs who work outside brothel-based settings and red-light districts. It seems from our observations in the field that these women do not identify themselves as SWs because they have additional sources of income and meet clients occasionally. There is some evidence that strategies that empower women and policy support for SWs interventions could help to improve coverage and adherence to the intervention.25
Despite the use of condoms with clients significantly increased over the follow-up, evidence for such an increasing trend with regular partners was lacking. It has been described that the use of condoms is initially high at the beginning of a relationship but decreases over time.35 This occurs despite most women showing good knowledge about HIV prevention6,36 and constitutes a major challenge for HIV prevention programs targeting SWs.37,38 In addition, drugs, poverty, and gender inequity can hamper SWs' ability to act on their intentions and make the necessary changes toward safer sex.18 The intervention has shown a positive effect in dropping bacterial STI and HIV incidence and in raising the use of condoms and HIV knowledge. Nevertheless, we still documented a considerably high STI incidence and poor condom use with regular partners at the third follow-up visit, which shows potential risk for a rapid expansion of the HIV epidemic.39
Although a better assessment of the intervention's impact will require a longer study period, this first evaluation has proven that the intervention is feasible and well accepted by local health authorities, health care professionals, SWs, and the owners of the CSE. Offering a proper medical service to SWs and acting to reduce the criminalization and stigma toward this population group has resulted in high participation in the program and active involvement of both SWs and the owners in health promotion activities. Health care seeking behavior and follow-up rates are key parameters that should be progressively improved to continue decreasing STI/HIV rates among SWs and their clients. In Central America, where poverty, violence, gender inequity, and irregular immigration across countries are clear determinants for acquiring STI and HIV, the challenge that remains is to proportionally scale up and maintain global and integrated interventions at the regional level.
We would like to thank the Ministry of Health in Guatemala, the National AIDS Program in Guatemala, the Primary Health Care Centre in Escuintla, the Health Department/Generalitat de Catalunya in Catalonia, and the Microbiology Laboratory of Hospital Germans Trias i Pujol in Badalona, Catalonia, for their trust and support. The Catalan Agency of Cooperation for Development, the Spanish Agency for Cooperation, and the Global Fund for their financial support. We also thank the Center for Epidemiological Studies on HIV/AIDS and STI of Catalonia (CEEISCAT) personnel for their scientific and methodological support. Finally, we want to recognize the strong commitment and hard dedication of all members of the UALE project in Guatemala.
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The UALE Project includes the following: director: Jordi Casabona; project coordinator: Jaume Font; Ministry of Health in Guatemala: Anabela Batres, Bianca Rosa Guevara; local coordinators: Victor Hugo Fernández, José Ernesto Monzón; medical doctors: Rudy Ortiz, Lilian Batz; nurses: Elva Orellana, Irma Mazariegos, Isabel Barrientos, and Leticia Roldan; health educators: Estuardo Cabrera, Kristian Villavicencio, Miguel Meléndez; psicologist: Karla Guzman; microbiologists: Gabriela Hernández, Olga Gálvez, Cristina Cu, Samuel Churuc, Amelia Gerónimo, Xavier Vallès, Victoria González, Elisa Bartró, Lourdes Mata, Vicenç Ausina; Statisticians: Federica Giardina, Alexandra Montoliu, Anna Esteve; I.T: Eva Loureiro; epidemiologists: Meritxell Sabidó, Virginia Isern; National AIDS Program: Mariel Castro; primary health care centre: Maribel Godoy (Santa Lucía Cotzumalguapa), Lucía Gallardo (Puerto de San José), Karina Sazo (Escuintla); María Isabel Pedroza, Laura Figueroa; data entry: Hugo Caceros; technical support: Fabiola Llanos, Chus Sanz, Mirian Guadalupe Bran̂as, Cristina Díaz.