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Programs

Control of Sexually Transmitted Diseases
Section III: Supporting Strategies

Edited by Gina Dallabetta, Marie Laga, Peter Lamptey

Authors: Doris S. Mugrditchian, Gina A. Dallabetta,
Peter R. Lamptey, Marie Laga

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Innovative Approaches to STD Control

Preview Capter 13

Introduction

This chapter provides information about how to implement more effective approaches to STD control. Although some of the proposed interventions are not new, most have not been fully tested or accepted by the medical and scientific communities.

Key Concepts and Issues

The concepts of targeting, improved treatment-seeking behavior and effective treatment at the point of first encounter are key in designing interventions that will have the greatest public health impact.

Targeting STD Services to Priority Groups

These groups include sex workers, persons working away from home and youth. Brothel-based STD services, mobile vans, workplace and peer education programs are examples of strategies to reach them.

Approaches to Management

Discussion focuses on clinical management, screening and case finding, partner referral and treatment, and empiric prophylaxis/treatment.

The last strategy, prophylaxis/treatment, involves giving periodic treatment to everyone in the target group regardless of symptoms. Although it has not been studied extensively, it is recognized as useful particularly when clinic access is poor and behavior change at the individual and community levels might not result in a rapid STD decline.

Improving STD Health-Care-Seeking BehaviorSince the success of efforts depends in part on cultural attitudes and perceptions, ethnographic research can help managers design community-appropriate programs. To this end, a tool has been developed, Targeted Intervention Research (TIR), which assists managers in designing and conducting formative research on STDs.

Treating STDs in Women: Integration of STD Services into Broader Reproductive Health ServicesIntegration of STD services into broader reproductive health services could enhance their acceptability and effectiveness. However, this approach is less likely to reach adolescents, single, sexually active women, including female sex workers, and women who have completed childbearing. The integration concept is new, and many pilot programs will need to be implemented before the appropriate measures of success are available.

The Problem of Self-Medication

Two approaches to self-medication have been field-tested in demonstration projects. One approach is to train pharmacy workers in syndrome management; the other is to promote syndrome-selective packages containing effective drugs and prevention materials. Both hold promise and await further evaluation.

Conclusion

STD service infrastructure are either weak or nonexistent in most developing countries. Building them is essential for long-term STD control. In the meantime, concomitant interventions are needed that can be implemented immediately and achieve a rapid reduction of STDs. These innovative interventions must be able to work with what is available in terms of existing resources and infrastructures.


Introduction

The previous chapters have described the different components and support services that are required for STD prevention and control, and have addressed many of the programmatic issues involved. It is important to recognize that many aspects of the STD control model of specialized treatment and referral centers developed in industrialized countries may not be appropriate, feasible or transferable to many resource-poor settings. There patients, particularly males, commonly seek STD treatment outside the formal sector and STDs are treated along with a multitude of other health problems by primary health-care workers who have received little or no specific training in STD management.

In addition, STD control in these settings must compete for resources with other important and less stigmatized health problems. Although funding for STD control has increased as a result of HIV/AIDS control programs, resources are still inadequate and health infrastructures remain weak. Given the urgency of the task at hand, more innovative approaches must be developed and implemented.

This chapter will explore a number of innovative approaches to STD control. No approach presented is really new. A few are borrowed from other fields and are only innovative in their application. Others are innovative in that they legitimize and standardize current practices that are not well accepted by much of the traditional and conservative medical and scientific communities. Some others recruit and engage providers from the informal sector as new partners in STD service provision. They are pragmatic approaches to which we must be open, and bold enough to consider and field-test.

Key Concepts and Issues

In designing interventions that will have the greatest public health impact, the concepts of targeting, improved treatment-seeking behavior and effective treatment at the point of first encounter are key. The rationale for these strategic concepts and the programmatic issues that arise in operationalizing them are discussed below.

Importance of Targeting

Not all members of a population are at equal risk for acquiring or transmitting STDs. Relatively small groups of community members known epidemiologically as "core groups" or "high frequency transmitters" are responsible for sustaining and perpetuating the spread of STDs in a community.1—4 Targeting limited resources to these priority groups will have a much greater impact on STD prevalence in a community than programs aimed at the general population.5

Challenges in making this concept operational are twofold. First, it can be difficult to identify and access these core groups. Second, it is important not to stigmatize or ostracize them while they are receiving prevention and care services. Although behavioral, ethnographic and epidemiologic surveys defining these core groups are often lacking, experience has shown that sex workers and their clients, people working away from home (e.g., migrant workers, long-distance truck drivers and military personnel) and youth often have high rates of STD infection. In addition, urban populations generally have a higher prevalence of STD infections than rural ones.

Treatment-Seeking Behavior

In many developing countries, the point of first encounter for STD self-medication and treatment is in the informal health sector. Over the counter purchase of antibiotics at pharmacies (drugstores or chemist shops) or from drug vendors and injectionists is almost universal despite laws that regulate their distribution.

The treatment obtained from these sources is frequently inadequate or ineffective, patients do not receive the benefit of prevention education including condom advice and their sexual partners are not referred or treated.

  • In Cameroon, a survey of men leaving pharmacies found that only 9 percent of men in Douala and 15 percent of men in Yaound‚ received their prescription from a medical doctor.6 The majority received their prescriptions from pharmacies, 38 percent and 54 percent, respectively. Pharmacists were the source of the prescription in 7 percent and 9 percent of the cases, respectively. The next most common source of advice was from friends, family or self, 46 percent and 21 percent, respectively. A total of 50 percent to 75 percent of the patients were treated incorrectly. The more "medical" the initial visit the higher was the cost of prescribed treatment.

It can be argued that in most developing countries, STD patients are not likely to receive more effective or comprehensive management in the formal clinic sector. This is generally due to scarce resources, limited provider training and the demands of patient flow and/or profit that often preclude any prevention education.

Although much research is needed on the determinants of STD care-seeking behavior, a number of barriers exist to seeking care in the formal sector. These include the following: the cost of long waiting times and return visits required for laboratory results; treatment failures and drug refills; the cost of transportation, consultation fees, laboratory tests and prescriptions; and the social implications of being seen in an STD clinic where staff are often judgmental, and privacy and confidentiality are often lacking.

These financial and social barriers apply particularly to women, and improving their access to and use of STD services is a major challenge in STD control. There is a low specificity or absence of clinical manifestations when women are infected with an STD.7 A large number of women do not recognize some STD symptoms as abnormal. 8,9 Finally, diagnostic tests for reproductive tract infections are not readily accessible.

Effective Management at the Point of First Encounter

A patient's first encounter with the health-care system may be the only contact, and it is likely to affect future treatment-seeking behavior, partner treatment and the treatment's cost-effectiveness. Therefore, STD management at that initial point should be as comprehensive and effective as possible. This first encounter might be in the public or private sector, in the formal or informal sector, at a central specialized clinic or a peripheral primary health-care clinic such as a maternal child health (MCH) or a family planning (FP) clinic.

Most of these providers do not have access to adequate examination or laboratory facilities. The use of standardized flowcharts based on the syndrome management approach (see Chapter 8) will enable them to make a diagnosis and manage the patient effectively. Key issues in improved care, discussed in detail in this handbook, include the availability of effective drugs, provider attitudes toward patients, privacy and confidentiality issues, provision of prevention services (condoms, education about risk reduction and therapy, and partner referral) and curative services.

Targeting STD Services to Priority Groups

At times it can be difficult to identify and access "core groups," and behavioral, ethnographic and epidemiologic information defining them is lacking. Nevertheless, three broad sub-populations in most communities warrant specific services because of their high prevalence of STDs. These three groups are sex workers, persons working away from home and youth. The discussion below will focus on services that have been piloted or proposed to reach these groups. The sustainability, cost and ultimate impact of these interventions have not been evaluated. Naturally, these will depend on STD prevalence in the target population, the effectiveness of the curative and preventive services, and the number of people within the target population covered.

Sex Workers

In designing STD services for sex workers, the main challenge is to target without stigmatizing. If sex workers are going to use services, they must feel comfortable, safe and confident about them. Confidentiality and privacy must be ensured, and service hours must be convenient. This can best be accomplished by involving members of this community in designing the services.

Regular screening of registered sex workers, often a legal requirement, is performed in several countries. However, these services are often stigmatizing and of little public health value since screening tests are either inappropriate or inadequate. Sex workers generally view such services as a legal hurdle rather than a health benefit. Furthermore, this approach does not reach unregistered or "clandestine" sex workers, a group that may be at higher risk for STDs than registered sex workers. In a study recently conducted in the Philippines, the prevalence of gonorrhea among unregistered female sex workers was 37.8 percent compared to 7.2 percent among registered ones.10

Brothel-based STD services have been piloted in Tanzania, Mali, Côte d'Ivoire and India. This approach applies to areas where brothel-based sex workers are prominent. Sex workers prefer these services because they are available at convenient hours and are private and confidential.

  • In many countries in Asia such as Thailand, Indonesia and the Philippines, commercial sex establishment owners contract private practitioners to provide regular (usually weekly or biweekly) on-site STD check-ups and treatment of their employees.11

  • In Tanzania, four types of STD services for sex workers were compared; brothel-based periodic visits; clinic visits outside normal hours; regular clinic attendance at upgraded clinics; and regular clinic attendance at clinics without intervention. Sex workers preferred brothel-based STD services. However, STD services at clinics outside the normal operating hours were more acceptable than STD services offered during normal clinic hours.12

  • In Mali, a visiting medical team regularly provided care to sex workers on site at the brothel during hours that did not interfere with the women's work. Almost all of the women agreed to be examined. To avoid stigmatization, the team traveled by public transport and taxi rather than by government and project vehicles, which would have been conspicuous.13

Mobile vans providing care and prevention services have also been used to reach sex workers.

  • In Tamil Nadu, India, numerous surveys by nongovernmental organizations (NGOs) considering the use of ambulatory clinic vans have shown that sex workers generally work in areas far away from their homes and prefer to live anonymously in their own neighborhoods. A neighborhood clinic, either fixed or mobile, which only provides STD services, would probably draw too much attention from other neighbors. It is unlikely that sex workers would use them for fear of being labeled. These women prefer to seek STD treatment outside their communities or in clinics that cater to the entire family and provide a broad range of primary health services.11

Clinic-based interventions offering either specialized or integrated services have been tried in many countries. Integrating STD services into other basic health services, primary care, FP and MCH services, can reduce the stigma attached to specialized STD clinics as long as health-care providers are nonjudgmental and treat the sex workers with respect.

  • In Kinshasa, Zaire, a special women's health center was established in an area where many sex workers lived.14 The clinic provided health education, free STD treatment and free condoms. The study demonstrated that a clinic-based intervention of care and prevention can reduce the incidence of STD and HIV. It was also noted that once the women realized they were receiving quality services they were more receptive to prevention messages, creating a "care-prevention synergy."15

  • Based on an assessment of the target community's needs in the Sonagachi district of Calcutta, India, a health service center for sex workers and their families was opened at a local youth club in the heart of the "red light" area. Although the emphasis is on sexual health, other basic health services are also provided. Effective STD treatment coupled with peer education and a condom distribution program has resulted in a reduction of STD prevalence in the community, dropping from 80.6 percent to 59.2 percent over three years.16

  • In Nairobi, Kenya, a small storefront clinic providing family planning services to high-risk women in the neighborhood instituted STD care services at the request of the health-care workers. A revolving drug fund was established and community-based distributors of contraceptives were trained to refer symptomatic women to the clinic. 17

  • In Bharatpur, Nepal, and Madras, India, demonstration projects are planned by the Family Planning Association of Nepal and Parivar Seva Sanstha, respectively, to determine whether STD services can be successfully provided to female sex workers through family planning clinics. 11

  • In Tanzania, facilities offering STD services integrated into primary health-care services (PHC) were the least preferred source of care among sex workers along truck routes. The sex workers preferred care at their brothels or in the clinics at hours different from the normal clinic hours.12

  • In Côte d'Ivoire, surveys on health-care seeking behavior among sex workers indicated that services delivered close to the work site were desired. A special clinic to provide STD care was established in the area and peer health educators, trained about safe sex and condom use, referred women to these clinics.15

Private clinics or private practitioners are the choice of many sex workers even if they are required to use government clinics for legal purposes. In some cases, such as in the Philippines, sex workers will first go to a private practitioner to ensure a clean bill of health before next visiting the government social hygiene clinic. 18 In the Dominican Republic, sex workers visit private practitioners when symptomatic to ensure that any potential STDs are treated, even though there is a requirement for regular check-ups in the government clinics. 13

  • In Haiti and Nepal, efforts are now underway to identify a core of private practitioners that currently provide or are committed to providing services to sex workers. The practitioners will be targeted with printed information and receive training on STD management for sex workers. 11,19

  • It has been proposed that coupons or vouchers be provided to sex workers that could be used in selected clinics or with selected private practitioners. Sex workers would then be eligible for discounted, expedited or free treatment.

Peer health educators and outreach workers are often used to provide face-to-face prevention information to hard-to-reach populations (see Chapter 4). In STD control, peer health educators have been used to encourage symptomatic individuals to seek care and to provide them with information about where it can be located.

  • In Tanzania, peer health educators at truck stops, who were already involved in condom promotion and HIV risk reduction education, were trained to assess risk using three simple questions.20 An affirmative answer to any of the three questions was supposed to prompt the peer educator into referring the woman for treatment. However, the peer health educators were unable to apply the score properly, even after repeated training. It was surmised that the educators were important for their role in encouraging the women to seek care, but in this pilot project they were unable to refer women at higher risk based on a risk score.21

  • In Madras, India, the AIDS Control and Community Education Programmes Trust has started an outreach program for sex workers in the central train station area. Sex workers with STD complaints are being referred with a letter to the public hospital for free treatment. The referral letter helps to ensure that the women are treated well by the clinic staff. So far the women appear to be pleased with the services and with the attitude of the staff whom they have encountered.22

Persons Away from Home

Persons away from home for long periods may be at increased risk for STDs because their work takes them outside their normal social settings and support systems. As noted previously, this target population typically includes truck drivers, military personnel, and workers at large construction, mining or agricultural sites in remote areas. Although basic health services are often offered to these workers by their employers, many are forced to seek STD care elsewhere to avoid undesirable job repercussions.

There are many challenges and opportunities in providing care to these groups. They include building advocacy among company managers so they will allocate resources for STD prevention and control in the workplace; ensuring that the confidentiality and privacy of the employees are maintained; and making sure that employees have access to high-quality and socially acceptable STD services.

The following are some examples of ways to reach these groups:

  • In Tanzania, STD treatment and prevention services were provided to truck drivers and their families at the main company headquarters in Dar Es Salaam.23 Peer health educators were also trained to encourage early treatment as well as other STD and HIV prevention activities.
  • In Tamil Nadu, India, in a project overseen by the AIDS Research Foundation of India, an arrangement has been made for two private practitioners to provide STD services to the men at three project sites. The men pay for the prescribed medication, but the project pays a set consultation fee. The men are told that a third party is paying for the consultations.24
  • In India, a mobile STD clinic mounted on a van for truck drivers along the Madras-Bangalore highway is being considered by a local NGO. 24
  • In Kenya, Senegal and Nigeria, policy work is being done with company managers to convince them to allocate resources for HIV prevention, including STD management, using the Private Sector AIDS Prevention Package (PSAPP).25
  • In Malawi, assistance is being provided to companies and agricultural estates that have their own health clinics to ensure that health providers are properly trained in STD management using syndrome diagnosis, and to optimize appropriate STD drug procurement.26

The suggestion has been made to require the provision of STD/HIV prevention activities, including care and management, when large public works projects such as dam or road construction are planned. In these transient communities, with men separated from their families for long periods of time, contact between laborers and sex workers increases.

Adolescents

Adolescents have unique reproductive health needs. They need access to convenient, user-friendly, confidential, low-cost STD care and contraceptive services. In general, adolescents have limited information and skills for making responsible sexual decisions. Female adolescents are biologically more susceptible to some STDs because of an increased zone of ectopy and because of other genital tract characteristics due to the hormonal changes of puberty.27

There is limited experience regarding the kind of reproductive health services to provide to adolescents, how to provide them and how cost-effective they are. Current efforts to integrate STD services into broader reproductive health services are unlikely to have a large impact on this population.

The following includes a few examples of how young people are being targeted:

  • In Colombia and Swaziland, UNICEF is developing youth centers or special care units within existing care facilities, with specific days for youth. These centers and units will provide comprehensive health-care, including STD care and family planning services.28

  • In Guatemala, Asociación Pro Familia (APROFAM) offers STD services to adolescents at the "El Camino" youth center it runs in Guatemala City. In addition to clinical services and sex education, the center provides social and educational services (vocational workshops) as well as cultural and recreational activities. Clinical services include general medicine, gynecology, pre- and post-natal care, family planning and psychological counseling. Most of the services are free.11

Approaches to Management

Approaches to managing STDs in both symptomatic and asymptomatic high-risk individuals are reviewed in this section. The discussion focuses on clinical management, screening and case finding, partner referral and treatment, and empiric prophylaxis/treatment.

Clinical Management

The use of standardized STD flowcharts based on the syndrome management approach (see Chapter 8) will enable the majority of providers, who generally lack access to adequate examination or laboratory facilities, to manage symptomatic patients effectively. The syndrome management approach to STD care is patient-centered, rapid and effective, in marked contrast to the classic dermato-venereology approach. Treatment can be provided during the initial visit, which reduces the risk of further spreading the infection, and the risk of sequelae developing from untreated infections. In addition, the need to return for laboratory results is eliminated. Because there are no lab expenses, there are cost savings. And since treatment covers all major pathogens, there are fewer treatment failures.

Women represent a major challenge in STD control (see "An Approach to STDs in Women: Integration of STD Services into Broader Reproductive Health Services") primarily because of the low specificity, or absence, of clinical manifestations when they are infected. The validity of syndrome-based flowcharts for lower genital tract infections in women is not optimal, and laboratory tests remain essential for detecting STDs in asymptomatic and high-risk women.

Screening and Case Finding

Screening and case finding are limited by the availability of validated tools and diagnostics. The use of diagnostic tests for screening purposes is limited by cost, the need for laboratory capabilities and by logistics.

By instituting clinic-based screening, antenatal clinics in Kenya were able to dramatically increase the number of women who were screened for syphilis with a rapid plasma reagin (RPR) and treated. This allowed them to bypass many of the logistical problems of sending specimens to the lab, waiting for results and asking the women to return29 (see Chapter 9). Several research groups are evaluating whether a risk assessment based on behavioral characteristics could be developed to screen asymptomatic women for STDs. The current risk score recommended by WHO was developed for the management of symptomatic women (see Chapter 8). The development of an inexpensive simple bedside diagnostic test for gonorrhea and chlamydial infection in women is now a research priority for several international health organizations.30

However, risk assessment and diagnostic tests are not mutually exclusive approaches to asymptomatic infections. A region in the United States successfully used risk assessment on asymptomatic women to identify those who would undergo a diagnostic test for chlamydia.31 The use of the risk assessment prior to testing made the screening more cost-effective.

Partner Referral and Treatment

Partner treatment is an underutilized and understudied approach to STD control (see Chapter 11). In the U.S., a pilot project is underway to determine the effectiveness of sending the index patient home with therapy for the partner(s).32 Furthermore, in settings that lack the capacity to perform screening tests, partner referral/notification of symptomatic men offers an opportunity to identify and treat women who are asymptomatic or otherwise unaware of their infections.

Empiric Periodic Prophylaxis/Treatment

Empiric periodic prophylaxis/treatment of selected STDs among high-risk groups (often referred to as mass treatment) is a much discussed yet little studied strategy to achieve a rapid decrease in a community's reservoir of STDs. This strategy involves giving periodic treatment to everyone in the target group regardless of symptoms. Depending on the pharmacokinetics of the drug used, periodic administration of antibiotics may treat an existing infection or act as a prophylaxis against a potential infection.

Strategies to rapidly reduce a community's pool of sexually transmitted infections are desirable for the following reasons: (1) sexual behavior changes at the individual and community levels are likely to take time and therefore not result in a rapid STD decline; (2) many patients are asymptomatic or the symptoms are too mild to trigger treatment-seeking behavior; (3) having symptoms does not necessarily lead to treatment-seeking behavior; and (4) even with behavior change, some groups may continue to have relatively high levels of STDs. In addition, with the following problems, empiric treatment/prophylaxis may be more feasible than the existing delivery systems:

  • Access
    Clinical services are either unavailable or unavailable at appropriate hours.
  • Use
    High-risk individuals may be asymptomatic or avoid using services due to issues of stigmatization, provider attitudes, cost, punitive consequences or other barriers.
  • Quality of services
    Clinical services may be inadequate for diagnosing and managing STDs, particularly for women for whom physical examination and testing require some degree of infrastructure.

  • Sensitivity of detection methods
    Existing sensitivity for diagnostic tests (chlamydial infection) or physical examination (genital ulcers in women) may be low.

  • Compliance
    People who come for testing may not come for treatment.

Empiric treatment or mass treatment was used by the World Health Organization and the United Nations Children's Fund to control and eradicate yaws and endemic syphilis in the 1950s and 1960s.33 This program resulted in a dramatic reduction in the number of cases of yaws and endemic syphilis. However, since then there has been an increase in the number of reported cases because a permanent treatment and control program was never established.

There have been a handful of reports addressing the issue of empiric, periodic prophylaxis or treatment of groups for STDs, including the following:

  • Greenland attempted a community-based mass treatment for gonorrhea, supplemented by mass laboratory examinations and contact tracing during the late 1960s.34 The prevalence of gonorrhea was reduced by 50 percent among those examined in the towns and by 75 percent among young people in rural areas. However, this intervention was expensive and ultimately not sustainable, and pre-intervention levels of gonorrhea were seen within three to six months after the program was discontinued

  • In 1967, mass antibiotic treatment with oral ampicillin and probenecid or tetracycline was given for gonococcal infection to 4,000 female sex workers in Olangapo, Philippines, over a one-week period.35 The intervention was attempted after weekly culture and treatment of sex workers had lowered the prevalence of gonorrhea in the sex workers from 11 to 4 percent. After the mass treatment, the prevalence of gonorrhea fell to 1.8 percent. However, this low level was not maintained and within one month of the intervention it rose to the pre-treatment baseline. It appeared that the single empiric mass treatment did little to diminish the prevalence of gonorrhea in a setting where there was already a strong program for its control.

  • In Surabaya, Indonesia, sex workers have received penicillin treatment since 1957.36 The prevalence of reactive syphilis serology measured by nontreponemal screening tests has dropped from 87 percent in 1957 to 1.5 percent in 1992 among registered sex workers, and from 86.6 percent in 1957 to 4.2 percent in 1992 among street-based sex workers. Yaws was endemic in Indonesia until the mass treatment campaigns of the 1950s and 1960s and is likely to be reflected in the earlier serologies. Nonetheless, the persistently low prevalence of syphilis in these sex workers suggests that empiric therapy for syphilis might be effective. The appropriate dose and treatment interval have not been defined.

  • In Fresno, California, in response to an explosive increase in syphilis cases in the mid-1970s, a selective mass treatment campaign against syphilis and gonorrhea was introduced for 12 months as part of a syphilis control program.37 Sixty percent of the cases had occurred among sex workers and seasonal farm workers. In addition to this selective mass treatment program for sex workers, longer clinic hours were established, making the clinic more accessible to sex workers and migrant farm workers. In addition, a migrant outreach program providing STD services to farm workers in a mobile van was introduced. Syphilis cases declined among sex workers, farm workers and other men and women. Because mass treatment was only one of several control program elements, it is not possible to know the extent to which it brought about the decline in syphilis. The long-term impact of the campaign was not reported.

  • In May 1981, in response to an outbreak of chancroid among Hispanic men and sex workers in Orange County, California, a one-day, door-to-door educational campaign was conducted in the ten neighborhoods with the largest clusters of cases.38 Individuals with the potential for the disease were encouraged to attend the municipal STD clinic. All clinic patients with genital ulcer disease and a history of contact with a sex worker, as well as their partners and all sex workers, were presumptively treated for chancroid. These control measures seemed to bring the chancroid outbreak under control.

The impression from these few studies is that empiric prophylaxis/treatment was successful in controlling STD outbreaks of syphilis and chancroid when it was combined with other control efforts such as community outreach, targeting and contract tracing. The Subic Bay, Philippines, experience demonstrates that a reduction in the prevalence of gonorrhea cannot be sustained after a single empiric treatment/prophylaxis event or when the periodicity of the intervention cannot be maintained at a sufficiently short interval to keep up with the rate at which the target population is getting reinfected. The Greenland experience corroborates the Subic Bay experience and demonstrates that empiric periodic treatment/prophylaxis for gonorrhea can be prohibitive because reinfection rates can be very high. Although complicated by the lack of specificity of non-treponemal tests, the persistently low prevalence of positive syphilis serology in Indonesian sex workers suggests that the intervention might be effective. Overall, this data also suggests that diseases with a long duration of infection such as syphilis, chancroid or chlamydial infection may be more amenable to control with this approach than short duration diseases such as gonorrhea.

The effectiveness of empiric prophylaxis/treatment can be greatly enhanced by concomitant behavior change and condom distribution interventions. This empiric prophylaxis/treatment approach might be regarded as a short-term intervention complementing the longer-term solutions of primary prevention and clinic-based services. Data from commercial sex workers in Nairobi, Kenya, in 1985 indicated that the mean time to reinfection with gonorrhea was 12 days and the weekly incidence of gonococcal infection was 11 percent.39 These data suggest that the cost of mass treatment can become prohibitive if the reinfection rate is high.

Empiric periodic prophylaxis/treatment of selected STDs can be conceptualized for individuals, communities, general populations or for selected high-risk populations. Criteria that might be considered when deciding which populations to target and what disease(s) to direct therapy against include the following:

The population

  • Access to targeted populations
  • Acceptability of the approach to target population
  • Population compliance

The pathogen(s)

  • The disease's prevalence in the population
  • The reinfection rate in the population
  • The population's risk for HIV
  • The therapy (preferably one that is highly effective against the selected pathogen(s), and is given in a single dose, orally administered and has few side effects)
  • The likelihood and severity of complications if left untreated
  • The duration of infectiousness
  • The difficulty in diagnosis (this may be different by sex)

The program

  • Intervention sustainability
  • Marginal yield of empiric prophylaxis/therapy compared with standard control measures
  • Cost-effectiveness (the cost effectiveness will decrease as the prevalence of the disease falls)
  • The presence of a comprehensive STD/HIV prevention program that includes behavior change interventions, condom promotion and other alternate ways to access STD care

There are several potential risks associated with this empiric prophylaxis/treatment approach and with the widespread use of antibiotics that need to be weighed. On the individual level, the efficacy of the antibiotic in treating the current infection and the potential risk of re-exposure with sub-therapeutic levels of the antibiotic need to be examined. Exposure to sub-therapeutic levels could lead to increased antibiotic resistance. Routine antibiotic use might disrupt the mucosal barrier of the normal flora and, in turn, increase the risk of certain diseases. For example, altering the pH of the vagina or eradicating peroxide-producing lactobacilli may increase susceptibility to HIV infection. A change in the vaginal flora also may increase the risk of vaginal candidiasis. Other potential risks include adverse drug reactions and the possibility that unsterilized needles will be reused.

Some epidemiologists would argue that empiric periodic prophylaxis/therapy also may have the effect of increasing higher-risk sexual behavior. It is possible that this approach may affect the number of partners (including those at high risk), the frequency of sexual activity and the frequency of condom use. There have been no studies that address these issues.

On the community level in developing countries, many of the antimicrobials that could be useful for empiric prophylaxis/therapy (fluoroquinolones, third generation cephalosporins and long-acting macrolides) are also used to treat other major diseases. Routine application of these drugs may render them useless in treating such serious diseases such as salmonella, shigella and tuberculosis. In the Rakai district of Uganda, a population-based mass STD treatment trial is underway.40 The study will address some of the issues just outlined and is being watched with great interest.

Approaches to Improving STD Health-Care-Seeking Behavior

Several approaches are being taken both to understand and improve the treatment-seeking behavior of symptomatic individuals. They are discussed below.

Program-Driven Ethnographic Research

It is now well-recognized by public health specialists and social scientists alike that pre-program research (formative research) combining qualitative and quantitative methodologies is required to design and implement programs successfully. Since the community perception of STDs is often quite different from the medical one, STD control managers must first understand the community's perspective before designing STD programs. This ensures that programs meet the perceived needs of community members in a way that is acceptable to them.

A tool has been developed, referred to as Targeted Intervention Research (TIR),41 which assists program managers in designing and conducting formative research on STDs, to ensure maximum relevance to program design and implementation.

The TIR is a set of instruments that helps uncover health-seeking behavior as it relates to clinic-based STD programs and complementary health education activities designed to increase STD knowledge and demand for services. The instruments also try to identify barriers to condom use and ways to increase condom availability in the community. From the community perspective, the instruments address sexually transmitted illness-related concepts and practices, illness management, service delivery, gender specificity, partner notification, post-treatment practices, and communication and prevention issues.

The methodology includes establishing a multi-disciplinary technical advisory group of social scientists, communication experts, clinical experts and public health officials who will assist in identifying research priorities and guide the research.

In Malawi, for example, researchers found that many of the illnesses mentioned by the people who were interviewed closely matched western biomedical definitions of STDs. For some STDs, however, the early and late stages of an infection were considered separate illnesses and were given different names and treatments. An understanding of such distinctions can help STD care providers improve communication with their clients.42

In Zambia, in contrast to expert informants who felt sure that local language easily discriminated between such common STDs as syphilis and gonorrhea, it was found that there was a great disparity between local language and biomedical terms.43 It was recommended that all communication messages refer to symptoms rather than to disease names.

In Ethiopia, getting care from a government health clinic was often the last recourse for therapy. Reasons cited by community members included the stigma of an STD-only examining room in the clinic, long waiting times, condescending and judgmental providers and the lack of privacy during the consultation.44

In the Philippines, sex workers from Manila and Cebu City cited condom use, careful partner selection and examination of partner genitals as methods for preventing STDs. Undergoing a clinical examination to detect and treat STDs was not mentioned.45

Increasing Women's Awareness of STDs

Educating women to recognize abnormal symptoms will increase the number of women seeking care. As long as resources are available to adequately detect, diagnose and treat STDs, the following approaches to improving STD treatment-seeking behavior in women might be considered.

In Thailand, community workers instruct women on how to recognize abnormal symptoms and potential risk factors. This approach is now being evaluated.46

In Bangladesh, camps were set up to determine the magnitude of STDs in the communities, provide STD and HIV education, and raise awareness of STD symptoms and risk behavior. At three different health posts in a Bangladesh city of more than 100,000 inhabitants it was found that women were fourteen-times more likely than men to attend the camps; this may reflect the fact that the camps had previously been used in family planning programs. Although at least half of the women were found to have a history or a physical examination suggesting a reproductive tract infection, many of those who attended had gynecological problems other than STDs. Consequently, it appears that the camps would be more successful if the implementers were prepared to offer more services than STD detection and treatment alone.47

In family planning clinics in Mexico, self-risk assessment rather than risk assessment by clinical staff prior to IUD insertions is being piloted to identify potentially infected women.48

An Approach to STDs in Women: Integration of STD Services into Broader Reproductive Health Services

There has been growing interest in integrating STD care into family planning services, as a way to make STD services more accessible to women.49 The International Conference on Population and Development held in Cairo in 1994 stressed that family planning services should be expanded to encompass more comprehensive reproductive health services and that more attention should be given to the prevention and treatment of STD, including HIV.50

Integration of STD services into broader reproductive health services could enhance their acceptability and effectiveness. However, this approach is less likely to reach adolescents, single, sexually active women, including female sex workers, and women who have completed childbearing.

Thumbnail graphic linked to larger clearer version of the same.How common are STDs among typical FP populations? In developing countries, data on STD prevalence among FP clinics are still scarce. Available data from Africa (see Table 1) indicate that STD rates found among these women reflect fairly well STD rates among general population low-risk women. The data show wide ranges of prevalences depending on the specific infection and on geographic origin. In countries where FP services have been restricted to married women who have completed their child-bearing, STD rates tend to be low. In places where "higher risk" women (such as adolescents or young single women) use FP services, STD rates are found to be much higher.

Thumbnail graphic linked to larger clearer version of the same.There are additional reasons for integrating STD/HIV into FP services. Women need to know if they are at risk for STD/HIV and, ideally, if they have an STD, to tailor contraceptive options and safer sex counseling to their needs. Considering that the most effective methods for STD protection are less effective in preventing pregnancy (see Table 2), the question arises whether health care providers should recommend that people use two methods. It is a complex and continually debated issue for family planning providers.

The answer remains unclear, especially now that data from the U.S. suggest that compliance with a barrier method (condom) decreases with the effectiveness of the contraceptive method used (such as oral contraceptives). The studies show that women who used oral contraceptives or were sterilized were less likely to insist on condom use than women who used a less effective contraceptive method or none at all. In Baltimore, Maryland, in the United States when sexually active teenagers were offered condoms to use in conjunction with oral contraceptives, only 4 percent used both methods simultaneously and consistently.55 Until more data are available, the choice of promoting a dual method (condom and other contraceptive) versus one method for dual purpose (condom for both STD/HIV and pregnancy prevention) should be weighed by factors such as the "risk of unwanted pregnancy" and the "risk of HIV/AIDS" in each clinic setting. It is clear that in most developing countries both risks are high, taking into account the unavailability of safe medical pregnancy termination services and the high prevalence rates of STD/HIV in the general population.

Thumbnail graphic linked to larger clearer version of the same.In India, condoms have been promoted as a dual purpose method to try to motivate more consistent use among high-risk men. Through radio, peer educators, posters and brochures, truck drivers received reinforcing messages that condoms provide double protection. Condom sales at three outreach centers increased from ten per week prior to the intervention, to roughly 1,000 per week after 18 months.56

More research also is needed on the patterns of dual method use. If an individual uses one method with a monogamous partner and adds condoms with other partners, this might effectively reduce risk, even if dual method use is not consistent in all encounters.

The diagnosis and treatment of STDs for women at FP services are the same as anywhere else and have been covered extensively in Chapter 8. Some issues specific to FP services are discussed here. When a woman presents with an acute symptomatic STD or admits having STD symptoms, the FP provider should apply the syndromic approach as discussed in Chapter 8. Whether all FP providers in one clinic should be trained in syndromic diagnosis of STD, or one provider per center should be trained (to whom all the women will then be referred) is still unclear. As summarized in Table 3, both strategies have advantages and disadvantages.

As in other settings, the main obstacle in STD management for women attending FP clinics is defining valid, feasible and affordable case finding strategies, especially for gonococcal and chlamydial cervicitis. So far, few attempts have been made to define risk profiling of STDs among FP attenders in developing countries. In a study in a rural FP clinic in South Africa, the presence of gonococcal and chlamydial cervicitis was associated only with young age and reporting more than one sexual partner. Algorithms including risk scores derived from this data did not have a high enough sensitivity and specificity to be acceptable for widespread use.

As pointed out in Chapter 9, the main reason why appropriate case finding strategies for gonococcal and chlamydial infections cannot be defined is the absence of a simple, rapid, affordable and valid test. Until such a test is available, imperfect approaches such as flowcharts that include risk profiling may still be a better option than doing nothing at all.

The concept of integrating STD services into FP services is still fairly new, and the many implications and consequences of this integration are still unclear. These may become clearer as actual programs are implemented.

Approaches to the Specific Problem of Self Medication

Two approaches to addressing the issue of self-medication have been field-tested in demonstration projects. One approach is to train pharmacy workers in syndrome management. The other approach is to promote syndrome-selective packages containing effective drugs and prevention materials. Both concepts are described in more detail below.

Pharmacy Training

This approach is particularly relevant in settings where the health infrastructure is weak and where drugstore personnel are often the only recourse for medical advice and treatment.

Enlisting pharmacy workers in STD management acknowledges the significant, though informal role this sector plays in providing STD treatment. It also recognizes the sector's potential role in patient education (prevention education, compliance with treatment and partner referral), and condom promotion and distribution. However, it does not overcome the problem of patients purchasing partial prescriptions due to lack of funds. Moreover, it is often difficult in a public business setting to guarantee confidentiality and the privacy necessary for gaining customer trust.

Public health authorities and members of the medical profession usually have no objection to enlisting drugstore personnel in patient education. However, there is much less acceptance for explicitly training them in STD syndrome management. This is perceived by some authorities as condoning the dispensing of antibiotics without prescription, and seen by many in the medical community as a threat to their profession. For this approach to succeed, advocacy must be built among these groups and they must be engaged as partners in the intervention from the outset.

In Nepal, drugstore personnel are being taught to dispense antibiotics using the syndrome management approach and to provide clients with preventive education and condoms. The intervention is being developed and implemented by the Nepal Chemists and Druggists Association in close collaboration with the Nepal Medical Association, the Department of Drug Administration and other relevant government agencies and university experts. The intervention also includes establishing appropriate referral networks between drugstores and clinics.11

In Thailand, the pharmacists' association has adapted the syndrome management flipchart to train Bangkok pharmacists in STD management. It was developed for general practitioners by the Thai Medical Association for the Study of STDs.11

The impact of these interventions awaits evaluation. Over the long term, it is anticipated that as services improve in the formal sector, there will be a gradual shift in health-care-seeking behavior to facilities that offer privacy and are conducive to a more thorough clinical assessment.

Marketing Prepackaged Therapy

Prepackaging of antibiotics for urethritis along with prevention materials (condoms, partner referral cards, instructions and educational material) was field-tested in Cameroon as a demonstration project to raise the level of effective treatment. The project was started to address the following identified problems based on research cited above 6 indicating:

  • High incidence of urethritis in young men
  • High levels of self-treatment
  • Widespread use of inappropriate and ineffective drugs by physicians and pharmacies
  • Widespread under-medication due to partial prescription filling.

A kit for urethritis was developed under the brand name Mstop, the French abbreviation for STD (MST) and the word STOP. The kit contained two 500 mg tablets of cefuroxime axetil as a single-dose therapy for gonorrhea; twenty 100 mg tablets of doxycycline for a 10-day course for chlamydial infection; an STD education leaflet; eight condoms; and two partner referral cards encouraging partners to seek medical care. The kit was priced at US $17 with the brand-name antibiotics accounting for most of the cost. At the time of the project, generic, untaxed drugs could not be sold in Cameroon. This price was found to be competitive when compared to the mean cost per STD episode estimated in a pharmacy exit survey.6 Although the kit was originally designed to be sold in pharmacies without prescription, health authorities ultimately only allowed Mstop to be sold in a limited number of government clinics and private pharmacies.

The sales never achieved their target. This was due, in part, to poor physician acceptance of syndrome management, since a consensus on the syndrome approach to STD management had not been reached in Cameroon when the project was implemented. It was also due to the limited distribution of the product. However, follow-up with patients who received the kit showed a high level of satisfaction: 98 percent reported taking the two tablets of cefuroxime axetil and 83 percent reported completing the 10-day course of doxycycline; 84 percent reported using condoms while on treatment; and 44 percent used their partner referral cards. The number of partners who actually sought treatment could not be monitored.

Based on the Cameroon project, the following recommendations should be considered in implementing future projects using the syndrome selective packaging approach:

  • The medical community's and the Ministry of Health's endorsements of the syndrome management approach to STDs should be a prerequisite since syndrome selective packaging implies acceptance of this approach.

  • The project should be launched as an integral part of the national STD control program and the antibiotics chosen for the kits ideally should be based on national STD treatment guidelines and drug recommendations. This also ensures that the drugs selected for the kit are approved by the country's regulatory bodies. Ideally, these national guidelines should be based on laboratory and epidemiologic data.

  • Local pharmaceutical regulations need to be clearly understood and the influence and power of the pharmaceutical industry cannot be underestimated. For example, generic drugs, which would make the kits more affordable, are not allowed to be sold in some countries. In some, brand-name drugs cannot be promoted or advertised. In others, drugs that are sold are subject to import taxation.

  • A project advisory committee should be formed and consulted throughout the project, from the design phase through the implementation phase. The committee should include experts and key influential representatives of the Ministry of Health and other relevant government authorities and regulatory bodies, the medical, pharmacy, and research communities, and the pharmaceutical industry.

  • Although the Cameroon project did not achieve the anticipated level of success, the rationale for marketing syndrome selective kits for treatment and prevention remains valid. The final word on this approach should be reserved for after it has been given a fair chance to succeed. The concept of packaging effective drugs (ideally single-dose drugs) and prevention material for managing STD syndromes could be modified for specific country situations. Here are some examples:

  • A syndrome package of generic drugs and prevention materials could be sold in public sector clinics as part of a cost-recovery scheme. By limiting sales to the public sector clinics where drugs are often supplied free of charge or for a nominal cost, there might be less resistance from the pharmaceutical industry.

  • A syndrome management kit of effective drugs and prevention materials could be marketed to health-care providers through the usual and accepted routes of current pharmaceutical marketing. This would ensure consistently effective treatment for STD syndromes and reinforce the syndrome management approach.

  • A syndrome management kit could be marketed to pharmacists to be made available by prescription.

  • A syndrome management kit could be marketed to the public as an over-the-counter product available without prescription. The argument that this approach will increase antibiotic resistance in a community would be attenuated if single-dose, single-pill antibiotics were provided in the kit.

Conclusion

In contrast to the enormity of the STD problem, the existing STD service infrastructure, whether it be a vertical or horizontal system, is either weak or nonexistent in most developing countries. Building this infrastructure is essential for long-term STD control, but will take time. In addition, a broader approach to service delivery must be envisioned that engages primary health-care, MCH and FP services; enlists the private and informal sectors as partners in service delivery; provides services that are convenient, effective, expedient and non-stigmatizing; and, recognizes the critical role of preventing infections, in addition to treating infections. In the meantime, concomitant interventions are needed that can be implemented right away and can achieve a rapid reduction of STDs, making use of existing and often scarce resources and infrastructures.

References

  1. Anderson RM, May RM. Epidemiological parameters of HIV transmission. Nature 1988;333:514—519.
  2. Brunham RC, Plummer FA. STD epidemiology and its implications for control. Med Clin North Am 1990; 74:1339—1352.
  3. Brunham RC. The concept of core and its relevance to the epidemiology and control of sexually transmitted diseases. Sex Transm Dis April—June 1991:67—68.
  4. Yorke JA, Heathcote HW, Nold A. Dynamics and control of the transmission of gonorrhea. Sex Transm Dis 1978;5:51—57.
  5. Over M, Piot P. HIV infection and sexually transmitted diseases. In: Jamison DT, Mosley WH, Measham AR, Bobadilla JL, eds. Disease control priorities in developing countries. New York: Oxford University Press, 1993:445—529.
  6. Trebucq A, Louis JP, Tchupo JP, Migliani R, Smith J, Delaporte E. Treatment regimens of STD patients in Cameroon: a need for intervention. Sex Transm Dis 1994;21:124—126.
  7. Vuylsteke B, Laga M, Alary M, et al. Clinical algorithms for the screening of women for gonococcal and chlamydial infection: evaluation of pregnant women and prostitutes in Zaire. Clin Infect Dis 1993;17:82—88.
  8. Moses S, Ngugi E, Bradley JE, et al. Health care-seeking behavior related to the transmission of sexually transmitted diseases in Kenya. Am J Public Health 1994;84:1947—1951.
  9. Olukoya A, Elias C. Perceptions of reproductive morbidity among Nigerian women and men: implication for family planning services. New York: The Population Council Report, June 1994.
  10. Abelanosa I, Manalastas R, Tan M, et al. Comparison of STD prevalence and the behavioral correlates of STD among registered and unregistered female sex workers in Manila and Cebu City, Philippines. In: Abstract book from the third international conference on AIDS in Asia and the Pacific. Chiang Mai, Thailand: Abstract PB147; 1995.
  11. Mugrditchian D. Personal communication, 1995.
  12. Mbuya C, Nyamuryekung'e K, Laukamm-Josten U, et al. STD services for women in truck stops in Tanzania: an evaluation of acceptable approaches. Abstract presented during the 3rd USAID HIV/AIDS prevention conference. Washington, DC: U.S. Agency for International Development, August 7—9, 1995.
  13. Ryan C. Personal communication, 1995.
  14. Laga M, Alary M, Nzila N, et al. Condom promotion, sexually transmitted diseases treatment, and declining incidence of HIV-1 infection in female Zairian sex workers. Lancet 1994;344:246—248.
  15. Laga M. Personal communication, 1995.
  16. Jana S. Three year stint at Sonagachi: an exposition. Calcutta, India: All India Institute of Hygiene and Public Health, Department of Epidemiology, 1994.
  17. Kairu M. Personal communication, 1995.
  18. Wi T. Personal communication, 1995.
  19. Génécé E. Personal communication, 1995.
  20. Mbuya C, Nyamuryekung'e K, Laukamm-Josten U, et al. Defining a risk score for STD treatment for women in 7 truck stops in Tanzania. In: Abstract book from the VIIIth international conference on AIDS in Africa & VIIIth African conference on sexually transmitted diseases. Marrakech, Morocco; 1993.
  21. Mbuya C. Personal communication, 1995.
  22. Narayan H. Personal communication, 1995.
  23. Final project report. Tanzania: AIDS education and condom promotion for transport workers; strengthening STD services. Nairobi, Kenya: African Medical and Research Foundation, 1992.
  24. Sundaraman S. Personal communication, 1995.
  25. Roberts M. Conducting a workplace HIV/AIDS policy needs assessment. Arlington, Virginia: AIDSCAP/Family Health International, 1994.
  26. Costello Daly C. Personal communication, 1995.
  27. Brookman RR. Adolescent sexual behavior. In: Holmes KK, Mardh P, Sparling PF, et al., eds. Sexually transmitted diseases. 2nd ed. New York: McGraw-Hill Inc, 1990:77—84.
  28. Islam M. Personal communication, 1995.
  29. Temmerman M, Mohamedali F, Fransen L. Syphilis prevention in pregnancy: an opportunity to improve reproductive and child health in Kenya. Health Policy Plan 1993:8;122—127.
  30. Berkley S. Diagnostic tests for sexually transmitted diseases: a challenge. Lancet 1994;343:685—686.
  31. Britten TF, DeLisle S, Fine D. STDs and family planning clinics: a regional program for chlamydia that works. American Journal of Gynecologic Health 1992;6(3);24—31.
  32. Handsfield HH. Design and implementation of a successful chlamydial control program. In: Abstract book from the 35th interscience conference on antimicrobial agents and chemotherapy. San Francisco, California: Interscience Center on Antimicrobial Agents and Chemotherapy, Abstract S65; 1995.
  33. Antal GM. Causse G. The control of endemic treponematoses. Rev infect Dis 1985;7:S220—2226.
  34. Olsen, GA. Epidemiological measures against gonorrhea: experience in Greenland. Br J Vener Dis 1973;49:130—133.
  35. Holmes K. Personal communication, 1995.
  36. Sastrowidjojo H. Personal communication, 1995.
  37. Jaffe HW, Rice DT, Voigt R, et al. Selective mass treatment in a venereal disease control program. Am J Public Health 1979;69:1181—1182.
  38. Blackmore CA, Limpakarnjanarat K, Rigau-Perez JG, et al. An outbreak of chancroid in Orange County, California: descriptive epidemiology and disease-control measures. J Infect Dis 1985;151:840—844.
  39. D'Costa LJ, Plummer FA, Bowmer I, et al. Prostitutes are a major reservoir of sexually transmitted diseases in Nairobi, Kenya. Sex Transm Dis 1985:12;64—67.
  40. Wawer MJ, Grey RH, Quinn TC, et al. Design and feasibility of population-based mass treatment, rural Rakai District, Uganda. In: Abstract book from the eleventh meeting of the International Society for STD Research. New Orleans, Louisiana: Abstract 079; 1995.
  41. Helitzer-Allen DL, Allen HA. The manual for targeted intervention research on sexually transmitted illnesses with community members. Arlington, Virginia: AIDSCAP/Family Health International, 1994.
  42. Dallabetta GA, Allen H, Helitzer-Allen D, et al. Sexually transmitted infections (STD) in Malawi: local perceptions, knowledge and behavior. In: Abstract book from IX international conference on AIDS. Berlin, Germany: Abstract PO-D01-3404; 1993.
  43. Kendall C, Nzima M, Anyangwe S, Jackson R. Application of STD-TIR in Zambia: findings for STD interventions and policy. In: Abstract book from the eleventh meeting of the International Society for STD Research. New Orleans, Louisiana: Abstract 235; 1995.
  44. Gebre A. Personal communication, 1995.
  45. Tempongko SB, Tigalo TV, Ghee AE, Wi TE, Mugrditchian D. Targeted intervention research on sexually transmitted diseases in the setting of commercial sex, Manila and Cebu City, The Philippines. In: Abstract book from the eleventh meeting of the International Society for STD Research. New Orleans, Louisiana: Abstract 236; 1995.
  46. Thongkrajai E. Personal communication, 1995.
  47. Bhatt P. Personal communication, 1995.
  48. Barone M. Personal communication, 1995.
  49. Fox LJ, Williamson NE, Cates W, Dallabetta G. Improving reproductive health = integrating STD and contraceptive services. JAMWA 1995;50:1—9.
  50. Cohen SA and Richards CL. The Cairo consensus: population, development and women. Fam Plann Perspect 1994;26:272—277.
  51. Kapiga SH, Shao JF, Lwihula GK, et al. Risk factors for HIV infection among women in Dar-es-Salaam, Tanzania. J Acquir Immune Defic Synder 1994; 7:301—309.
  52. Temmerman M, Kidula N, Muchiri L et al. The supermarket for women's reproductive health: a demonstration and intervention project in Nairobi, Kenya. In: Abstract book from the IUVDT world STD/AIDS congress. Singapore: International Union of Venereal Disease and Treponematoses, Abstract 179; 1995.
  53. Fehler HG, Ye H, Dangor Y, et al. STD among women attending STD family planning and antenatal clinics in Moseru, Lesotho. In: Abstract book from the eleventh meeting of the International Society for STD Research. New Orleans, Louisiana: Abstract 344; 1995.
  54. Chout R, Quest D, Vaton S, et al. Chlamydia trachomatis in asymptomatic female adolescents and young adults in Martinique. In: Abstract book from the Xth international meeting of the International Society for STD Research. Helsinki, Finland: Abstract 331; 1993.