Effectiveness of HIV prevention strategies in resource-poor countries: tailoring the intervention to the context

Wegbreit, Jenya; Bertozzi, Stefanob; DeMaria, Lisa Mb; Padian, Nancy Sa

doi: 10.1097/01.aids.0000232229.96134.56
Editorial Review

From the aDepartment of Obstetrics and Gynecology, University of California San Francisco, San Francisco, California, USA

bInstituto Nacional de Salud Pública, Cuernavaca, Morelos, Mexico.

Received 22 July, 2005

Revised 1 December, 2005

Accepted 12 December, 2005

Correspondence to Dr Jeny Wegbreit, UCSF, 50 Beale St., Suite 1200, Box 1224, San Francisco, CA 94105-3444, USA. E-mail: jwegbreit@globalhealth.ucsf.edu

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Although global commitment to control the HIV/AIDS pandemic has significantly increased in recent years, the virus continues to spread with alarming and increasing speed. By the end of 2005, an estimated 40 million people worldwide were living with HIV, a notable rise from the 35 million infected with HIV in 2001 [1]. In 2005, close to 5 million new HIV infections and 3 million AIDS deaths occurred, more than in any previous year. Although sub-Saharan Africa remains the region most affected by HIV/AIDS, the virus is now spreading rapidly in Asia and parts of Eastern Europe. Detailed information on the global burden of HIV/AIDS, regional differences, and trends over time is available in the AIDS Epidemic Update: December 2005 [1].

Despite the rapid spread of HIV, several countries have achieved important advances in curbing its transmission. The extraordinary potential of HIV prevention is exemplified by such diverse efforts as Thailand's 100% condom program; Uganda's remarkable decrease in HIV prevalence and incidence; and Senegal's sustained success in minimizing HIV incidence [2–4]. These prevention successes stemmed, in part, from unique cultural, historic, and infrastructural elements of each country. A critical factor in their success had to do with how appropriately the intervention or package of interventions responded to the underlying dynamic of the epidemic in each country. Although an intervention may be highly efficacious in a controlled setting, its overall effectiveness at the population-level undoubtedly depends on the nature and stage of the epidemic in the setting to which it is applied. However, more often than not, the information required to tailor a response to the national epidemic is sorely lacking.

In fact, one of the greatest challenges to global control of the epidemic is the lack of reliable evidence, particularly evidence from resource-limited countries, to guide the selection of interventions for specific geographic areas or sub-populations. Data on the epidemiological context [valid surveillance data on HIV and sexually transmitted infections (STIs) as well as the prevalence and distribution of behaviors that contribute to the spread of the epidemic] are not widely available. Perhaps most importantly, there is a clear deficit of rigorous evaluation data and among the evaluations that have been conducted few have collected data specifically on HIV infection as an outcome [5].

In addition to the lack of data on intervention effectiveness, there is little information about how structural factors contribute to the success of an intervention. Given vast regional differences in the epidemic and the myriad environments in which HIV transmission occurs, such data is essential to permit appropriate tailoring of interventions. Researchers have increasingly recognized the importance of such structural factors as gender equity, low socio-economic status and poverty, and social norms in shaping epidemiological dynamics, however, rarely have prevention studies incorporated well-defined controls or comparisons that allow such factors to be identified [6]. Systematic and planned phased introduction of programs might allow on-going comparisons between intervention groups or communities with comparable groups that have yet to receive the intervention, thereby identifying structural factors that may have played a role in the success of programs.

In this review the available information on the efficacy of interventions is identified primarily using evidence from studies conducted in resource-limited countries. Resource-limited areas were chosen to be the focus of the review, in recognition of their great need, and since the data derived from those areas is most applicable. The gaps in the information needed to develop appropriate and effective control strategies are discussed and finally, it is argued that because the effectiveness of HIV interventions will vary by regional situations, strategies should be tailored to the nature and stage of regional epidemics.

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A more complete and detailed version of this paper will be included in the forthcoming ‘HIV/AIDS Prevention and Treatment’ chapter in the second edition of the Disease Control Priorities Project. Literature on the effectiveness of selected HIV interventions available via PubMed were searched from 1990 to the present. English language articles published in peer-reviewed journals that contained any of the relevant key words were considered for inclusion. Relevant key words included but were not limited to: HIV/AIDS; school-based education; abstinence education; voluntary counseling and testing; peer-based programs; condom promotion and distribution; information, education and communication; condom social marketing; sexually transmitted infection treatment; antiretroviral treatment/therapy; mother-to-child HIV transmission interventions; feeding substitution; harm reduction; needle exchange; drug substitution; blood safety; universal precautions; post-exposure prophylaxis; behaviour-change programs; efficacy; and effectiveness. Studies with concrete behavioral or biological outcomes (including condom use, number of sexual partners, and HIV and STI incidence) and with rigorous study designs and sufficient sample size were included in this review. Studies from high-income countries were excluded unless there was little or no evidence from resource-poor countries.

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Information needed to develop a control strategy

Knowledge about intervention effectiveness is essential to develop a successful control strategy at the national level, yet this information is often lacking due to a deficit of rigorous evaluations that would provide such data [7]. We know some interventions can effectively prevent transmission, including providing antiretroviral therapy for mother-to-child transmission [8–14] and blood safety practices [15]. However, there is dearth of information on the effectiveness of other interventions.

One reason for the data deficit is that HIV interventions are difficult to force into a typology that clearly distinguishes one intervention from another. For example, the counseling component of voluntary counselling and testing (VCT) has a strong information-sharing element that overlaps with information, education and communication (IEC) via the media, with peer interventions, and with the counseling component of STI treatment. Similarly, the psychological support offered through counseling is difficult to distinguish from that provided through support groups or from interventions designed to increase social support.

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Intervention effectiveness

This section summarizes the existing literature, primarily from resource-limited countries, on the efficacy of HIV interventions, as defined by the impact of the intervention on risky sexual behaviors or biological outcomes including HIV and other STIs. Table 1 outlines the design and sample size, the intervention components, the outcomes, and the quality of evidence using the US Preventive Services Task Force (USPSTF) quality of evidence scale of each study.

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General interventions relevant for all modes of transmission

These interventions include: IEC; school-based sexual education; VCT; and peer-based programs that rely on influential peers to change behavior norms.

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Information, education, and communication

As discussed above, discerning the efficacy of IEC is difficult. Because it is such an integrated part of condom promotion and distribution, it is rarely evaluated alone. We consider the efficacy of IEC in concert with condom promotion and distribution below in the section on ‘Interventions to prevent sexual transmission.’

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School-based sexual education

Some studies have shown that school-based programs may affect sexual behaviors [16,17], but their effect on biological outcomes such as HIV and STIs may be relatively insignificant. In a case–control study of a comprehensive school-based educational program conducted in Nigeria, 17% of intervention youths compared with 9% of control youths remained sexually inexperienced after the program (P > 0.05) [18]. Furthermore, in a community randomized trial of a school-based sexual education curriculum in Tanzania, among the sexually active, intervention youths reported greater condom use in comparison with controls (38% condom use at the 1-year follow-up versus 28%, P < 0.05) [19]. However, in that same study, there was no significant difference in the HIV and herpes simplex virus type 2 (HSV2) incidence [HIV for females: relative risk (RR), 0.76 for HIV; 95% confidence interval (CI), 0.35–1.65; HSV2 for males: RR, 0.92; 95% CI, 0.69–1.22; HSV2 for females: RR, 1.05; 95% CI, 0.83–1.32] [19]. Not all studies have shown school-based sexual education changes adolescents' behaviors. In an evaluation of an HIV education program in Mexico, students receiving the intervention had a more positive attitude towards safe sexual practices [intention to use a use a condom: odds ratio (OR), 1.66; 95% CI, 1.40–1.97], but there was no sustained impact on actual condom use (condom use at first intercourse, 1-year follow-up: OR, 1.02; 95% CI, 0.77–1.34) [20].

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Voluntary counseling and testing

Knowledge of serostatus may lead individuals to avoid engaging in risky behaviors [21]. Several studies have shown that VCT increases condom use [22–24] and increases abstinence [24]. In a large randomized study of adults in Kenya, Tanzania and Trinidad, individuals who had received HIV testing and counseling reported significant reductions in unprotected intercourse in comparison with those who had received basic health information (35% reduction in intervention men versus 13% in the control group; 39% reduction in intervention women versus17% in the control group, P < 0.05) [22]. However, evidence of the impact of VCT on biological outcomes such as HIV and STI incidence is limited.

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Peer-based programs

Although we have much evidence of the success of peer-based HIV prevention programs in the US [25–29], evidence from resource-poor countries is limited. Studies conducted among sex workers and employed urban women have resulted in increased condom use [30,31], and in a multiyear cross-sectional study conducted among sex workers in Cote d'Ivoire, a peer education program resulted in a lower prevalence of HIV infection (from 89 to 32%, P < 0.001) and STI infection (from 21 to 2%, P < 0.001, for syphilis) [32].

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Interventions to prevent sexual transmission

Interventions to prevent sexual transmission include condom promotion and distribution and STI screening and treatment.

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Condom promotion and distribution

Studies overwhelmingly demonstrate that condoms are highly effective in preventing HIV transmission. A workshop co-sponsored by four government agencies responsible for condom research, condom regulation, and HIV/AIDS and sexually transmitted disease (STD) prevention programs (US Agency for International Development, Food and Drug Administration, Center for Disease Control and Prevention, National Institutes of Health, Bethesda, Maryland, USA) was held in June 2000 to evaluate the published evidence establishing the effectiveness of latex male condoms in preventing HIV/AIDS and other STDs. The workshop panel concluded that consistent users of the male condom significantly reduced the risk of HIV infection in men and women [33]. In fact, condoms appear on average to be at least 90% effective in preventing HIV when used consistently and correctly [34]. Given the efficacy of condoms in preventing HIV transmission, condom promotion and distribution programs should be one of the most effective prevention programs.

The available evidence on condom promotion/distribution programs, which often include IEC components, indicates their efficacy. Such programs have increased condom use [35–42] and decreased STI incidence [37,43] and HIV incidence [37]. Programs that have combined aspects of condom promotion, VCT and STI treatment have increased condom use [36,44] and decreased STIs [36,45].

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STI screening and treatment

Untreated, STIs increase by several-fold the risk of sexual HIV transmission [35,46–49]. Numerous epidemiological studies have supported the association of genital ulcers in general, and of genital herpes (HSV-2) in particular, with HIV infection [50]. Therefore, theoretically at least, implementing a program to treat and prevent STIs should be an effective HIV intervention.

Evidence from studies indicates that STI treatment programs decrease both HIV and STI incidence [35,51]. In a community randomized study of improved syndromic STI management conducted among adults in Tanzania, the HIV risk ratio among those in the intervention community was 0.58 (P = 0.007) [51]. However, other studies conducted in Uganda have shown no effect of STI treatment programs on HIV incidence [52,53]. The most recent analyses suggests that the reason for the different study outcomes may be due to a low prevalence of curable STIs resulting from lower-risk sexual behavior in Uganda and the fact that the epidemic in Uganda was mature, with most HIV transmission occurring outside core groups with high STI rates [54].

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Prevention of mother-to-child transmission

Prevention of MTCT can be viewed as a package containing aspects of the specific interventions described below.

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Use of antiretroviral therapy

Available evidence from numerous studies indicates that provision of antiretroviral drugs (nevirapine, lamivudine and zidovudine) to infected mothers significantly reduces vertical transmission, with values ranging from 33–63% reduction in transmission [10–14,55–57]. The range of drug regimens in these studies included: a single dose of maternal nevirapine at the onset of labor and to the infant upon delivery; antepartum and intrapartum maternal zidovudine and to the infant upon delivery; maternal zidovudine twice daily from 36 weeks gestation until labor, at the beginning of labor and post-partum; and maternal zidovudine and lamivudine at 36 weeks gestation until labor, at the beginning of labor and post-partum. Despite these advances in reducing vertical transmission, recent data indicates that women receiving antiretroviral therapy may develop resistance [58,59].

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Avoidance of unwanted pregnancies

One of the most effective strategies to reduce HIV among infants is to provide better contraception services to infected mothers. One modeling study estimated that in a population of 1,000 HIV-infected women, approximately 150 infants would be infected with HIV during delivery. If nevirapine were available, the number of infected infants would be reduced to 82 (the expected 47% decline). If effective contraceptive services were available, this number would be reduced to 49. If both strategies were adopted, the number of infected infants would be further reduced to 25 [60].

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Feeding substitution

Although complete avoidance of breastfeeding is recommended for HIV-infected mothers in developed countries to prevent postnatal HIV transmission, the feasibility of this approach in less developed countries is often limited by such factors as cost, sustainability, lack of safe water, health, child spacing, and socio-cultural factors [61–63]. However, prolonged breastfeeding can more than double the likelihood of mother-to-child transmission of HIV [64].

One study indicated that mixed feeding (breastmilk and formula or other substance) may have a higher risk of transmission than exclusive breastfeeding [62]. In this prospective study, investigators compared transmission rates in exclusively breastfed, mixed-fed, and formula-fed (never breastfed) infants to assess whether the pattern of breastfeeding affects early mother-to-child transmission of HIV. The proportion of infants who were HIV infected by 3 months was significantly lower for those exclusively breastfed to 3 months in comparison with those who received mixed feeding before 3 months (proportion, 14.6%; 95% CI, 7.7–21.4 versus 24.1%; 95% CI, 19.0–29.2; P = 0.03). After adjustment for potential confounders, exclusive breastfeeding carried a significantly lower risk of HIV transmission than mixed feeding [hazard ratio (HR), 0.52; 95% CI, 0.28–0.98] and a similar risk to no breastfeeding (HR, 0.85; 95% CI, 0.51–1.42). This data, albeit limited, suggests exclusive breastfeeding may offer HIV-infected women in developing countries an affordable, culturally acceptable, and effective means of reducing mother-to-child transmission of HIV while maintaining the overwhelming benefits of breastfeeding. Nevertheless, data are still needed to guide the optimal duration of breastfeeding. In addition, the nutritional and immunologic benefits of breastfeeding should be weighed when developing an effective breastfeeding strategy [65].

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Prevention of blood-borne transmission

Prevention of blood-borne transmission includes harm reduction for injection drug users (IDUs), implementation of blood safety practices, and providing sterile injections.

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Harm reduction for injection drug users

Harm reduction involves a combination of health promotion strategies for IDUs, including needle and syringe exchange programs (NEP), ready access to effective drug treatment and substitution, and provision of counseling and condoms. Brazil, which has reduced HIV incidence from earlier levels and kept HIV prevalence from reaching projected levels, has relied on strong official support for harm reduction as a cornerstone of its national prevention program [66]. In fact, in Santos and Salvador, two of the cities in which harm reduction programs were implemented, HIV servoprevalence among IDUs dropped from 63% in 1994 to 42% in 1999 and from 50% in 1996 to 7% in 2000, respectively.

Needle and syringe exchange. Studies indicate that NEPs reduce the risk of HIV transmission without encouraging increased drug use [67–70]. Here, most evidence derives from studies conducted in the US and Europe. In a randomized study conducted among IDUs who either did or did not participate in NEPs in New York City, not being involved in a NEP was associated with a hazard ratio of 3.35 for incident HIV infection (95% CI, 1.29–8.65) compared with using the exchange programs [71]. At least one other study, a community randomized study among IDUs in US cities, has shown a similar decrease in HIV risk associated with NEPs [72]. In that study, HIV seroprevalence increased by 5.9% per year in cities without NEPs and decreased by 5.8% per year in the cities with NEPs. In addition to decreasing HIV seroprevalence, NEPs may also reduce needle-sharing. In a cross-sectional study conducted among IDUs in Bangladesh, 87% of participants in NEP reported not sharing needles compared to 80% among non-participants (P = 0.000) [73]. Several other studies have also demonstrated an association between NEPs and reduced needle-sharing [74–76].

Drug substitution programs. Methadone maintenance is both safe and effective as treatment for drug addiction [77] and may help reduce the risk of HIV transmission by enabling individuals to avoid the drug-using behaviors that can lead to HIV infection [78,79] data. As with NEP effectiveness data, much of the methadone maintenance data is from the US. In one study examining the differences in the sexual behaviors of IDUs who received methadone treatment in the previous 6 months and those who did not, methadone patients reported significantly fewer sexual partners and significantly greater use of condoms [80]. Furthermore, in a meta-analysis of 11 studies investigating the impact of methadone maintenance treatment on HIV risk behaviors, investigators found such treatment programs demonstrate a consistently significant reduction in risk behaviors [81].

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Implementation of blood safety practices

HIV can be virtually eliminated through a blood safety program that ensures: (1) a national blood transfusion service; (2) the recruitment of voluntary low-risk donors; (3) the screening of all donated blood for HIV; (4) the reduction of unnecessary and inappropriate transfusions [15]. The available sensitivity and specificity evidence indicates that HIV screening is effective in reducing HIV infections [82–84]. In one study, after HIV rapid transfusion screen tests were implemented, it was estimated that at least 265 cases of HIV-positive blood donation were prevented [84], and in a study investigating the feasibility and efficacy of routine screening of donors for HIV-1 by polymerase chain reaction (PCR), investigators found that PCR screening contributes to a reduction in viral transmission [85].

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Universal precautions

To prevent blood-borne transmission of HIV and other diseases, health care workers, emergency personnel, and others who might experience occupational exposure to blood or body fluids are advised to take ‘universal precautions’ [86]. This approach, which treats all bodily fluids as potentially infectious, includes gloves, gowns, goggles, proper disposal of waste, sterile injection, and other infection control practices [86]. Studies have demonstrated that protective equipment, such as gloves, reduce the likelihood of blood exposure in health care settings. In one study designed to evaluate factors that affect blood volumes transferred to skin during simulated needlestick injuries, glove material reduced the transferred blood volume by 46–86% [87]. Investigators therefore concluded that gloves may exert some protective effect and should be worn whenever needles are handled.

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Post-exposure prophylaxis

Post-exposure prophylaxis (PEP) with antiretroviral agents is considered a standard of care after occupational needle-stick exposure to blood from HIV-infected persons. Limited evidence demonstrates the efficacy of this approach. In a case–control study of health care workers in the US with occupational, percutaneous exposure to HIV-infected blood, investigators found that case patients were significantly less likely than the controls to have taken zidovudine after the exposure (OR, 0.19; 95% CI, 0.06–0.52) [88].

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Tailoring the intervention to the context

Beyond efficacy: information needed for an effective control strategy

Efficacy data alone are not sufficient to inform decision-making. Randomized, controlled trials, which are used to obtain efficacy data, may not mimic the situation in which an intervention will occur. For example, if the conditions under which an intervention was tested differ from the conditions where it is later scaled up, its impact may be less than anticipated. Similarly, if a highly efficacious intervention is targeted at a population or sub-population that is not responsible for the majority of the new infections, it may have little measurable impact on the trajectory of the intervention.

Thus, in addition to effectiveness data, surveillance data to monitor the epidemic profile and contextual and structural data are essential to appropriately tailor an intervention. Nevertheless, some general observations about tailoring interventions to fit the epidemic context are possible.

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Using epidemic profiles to develop prevention guidelines

UNAIDS has developed epidemiological categories for the characterization of individual epidemics based on the prevalence of infection in particular subpopulations and in the general population. These categories are listed in Table 2. The UNAIDS generalized epidemic category is further subdivided into a low and high category.

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Prevention guidelines informed by epidemic profiles

Generally, low-level and concentrated epidemics should place greater emphasis on interventions that are targeted to individuals at especially high risk of becoming infected or transmitting the virus, whereas generalized epidemics should adopt population-level interventions that target entire populations or population subgroups. In the following paragraphs, we illustrate how the implementation of two interventions: condom promotion and distribution, and VCT, may vary based on epidemic profiles.

Low-level epidemic. In general, providing widespread routine voluntary counseling and testing (VCT) may not be effective in this setting because of the low HIV prevalence and high cost of such an intervention. In a low-level epidemic, as in the Middle East and North Africa, VCT should be available to key populations with the highest levels of risk behavior and infection rates. Condom promotion should address market inefficiencies in condom procurement and distribution, including strategies such as bulk purchases and incentives.

Concentrated epidemic. In a concentrated epidemic, as in countries in the Pacific, Europe and East, Central, and South Asia, Latin America and the Caribbean, VCT should be subsidized and promoted among key populations. Condom promotion should include peer-based programs for key populations to educate individuals at risk, promote safer behaviors, and distribute condoms.

Generalized low-level epidemic. In a generalized low-level epidemic, as is the case in some countries in sub-Saharan Africa, (for example, Tanzania), the emphasis on targeted interventions must be maintained or even strengthened, but interventions for broader populations must also be aggressively implemented. Routine voluntary and confidential HIV testing should be promoted beyond key populations. Additionally, subsidizing and social marketing of condoms and strengthened distribution to ensure universal access should be promoted.

Generalized high-level epidemic. In a generalized high-level epidemic, such as in some countries in sub-Saharan Africa, for instance, Botswana and Zimbabwe, an attack on all fronts is required. Prevention efforts should focus on broadly based, population-level interventions that mobilize an entire society to address prevention and care at all levels. Condom promotion and free distribution in all possible venues should be promoted and VCT for couples seeking to have children should be provided.

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Research agenda

As mentioned previously, we have data indicating some interventions can effectively prevent transmission, including providing antiretroviral therapy for mother-to-child transmission [8–14] and blood safety practices [15]. We also have limited evidence that STI treatment may be effective in reducing HIV incidence [35,51]. However, with the majority of interventions, such as school-based sexual education, VCT, and condom promotion we lack sufficient data on whether they reduce HIV incidence.

One of the most important barriers to HIV control is a dearth of rigorous evaluations of interventions that measure HIV incidence as an outcome. In addition, we have incomplete data on the epidemiologic profile of regions and we lack essential contextual information. Research on policy or structural interventions, which by definition must be conducted on a population level, is also needed. Last, information on how to properly scale-up interventions is necessary for effective decision-making.

There are numerous interventions currently in the pipeline (Table 3) with a great deal of promise, including the development of an HIV vaccine. However, results for most of these strategies are at best years away and although vaccine development has a great deal of potential, given both the uncertainty concerning whether developing an effective vaccine is possible and the long delay until a new vaccine can be widely applied, research efforts must be accompanied by the development of other new biomedical and behavioral prevention technologies.

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Even though the current deficit in evaluation research is glaring, the magnitude and seriousness of the global pandemic demands that action is nevertheless required. Despite such gaps in knowledge, we can improve control strategies by tailoring interventions to the nature and scope of the epidemic. If intervention policies are not guided by firm effectiveness, surveillance and contextual data, national strategies will not accurately reflect the priorities dictated by the particular epidemic profile. As a result, countries will undoubtedly make highly inefficient investments in HIV/AIDS prevention.

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The authors are also deeply indebted to Andrew Beggs, Susan Foster, James Kahn, Lilani Kumaranayake, Elliot Marseille, Fern Terris-Prestholt, Seema Vyas, and Charlotte Watts for their background papers that have informed this paper. They would also like to thank Carol Medlin for her valuable input on this paper.

Sponsorship; the authors would like to acknowledge the financial support received from the Disease Control Priorities Project through the Fogarty International Center of the National Institutes of Health and the Bill & Melinda Gates Foundation.

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HIV interventions; HIV prevention; effectiveness; efficacy; resource-limited countries

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