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
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: email@example.com
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 . 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 .
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 .
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 . 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.
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.
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 . We know some interventions can effectively prevent transmission, including providing antiretroviral therapy for mother-to-child transmission [8–14] and blood safety practices . 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.
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.
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.
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.’
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) . 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) . 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] . 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) .
Voluntary counseling and testing
Knowledge of serostatus may lead individuals to avoid engaging in risky behaviors . Several studies have shown that VCT increases condom use [22–24] and increases abstinence . 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) . However, evidence of the impact of VCT on biological outcomes such as HIV and STI incidence is limited.
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) .
Interventions to prevent sexual transmission
Interventions to prevent sexual transmission include condom promotion and distribution and STI screening and treatment.
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 . In fact, condoms appear on average to be at least 90% effective in preventing HIV when used consistently and correctly . 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 . Programs that have combined aspects of condom promotion, VCT and STI treatment have increased condom use [36,44] and decreased STIs [36,45].
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 . 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) . 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 .
Prevention of mother-to-child transmission
Prevention of MTCT can be viewed as a package containing aspects of the specific interventions described below.
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].
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 .
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 .
One study indicated that mixed feeding (breastmilk and formula or other substance) may have a higher risk of transmission than exclusive breastfeeding . 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 .
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.
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 . 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 . 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 . 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) . 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  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 . 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 .
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 . 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 , 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 .
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’ . 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 . 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% . Investigators therefore concluded that gloves may exert some protective effect and should be worn whenever needles are handled.
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) .
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.
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.
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.
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 . 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.
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.
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.
2. USAID, Senegal country profile
3. USAID, What happened in Uganda?
USAID: Washington, DC; 2002.
4. Phoolcharoen W. HIV/AIDS prevention in Thailand: success and challenges. Science 1998; 280:1834–1873.
5. Fleming T, DeMets D. Surrogate end points in clinical trials: are we being misled? Ann Intern Med 1996; 125:605–613.
6. Grassly NC, Garnett GP, Schwartlander B, Gregson S, Anderson RM. The effectiveness of HIV prevention and the epidemiological context. Bull WHO 2001; 79:1121–1132.
7. Feachem RG. The research imperative: fighting AIDS, TB and malaria. Trop Med Int Health 2004; 9:1139–1141.
8. Guay LA, Musoke P, Fleming T, Bagenda D, Allen M, Nakabiito C, et al
. Intrapartum and neonatal single-dose nevirapine compared with zidovudine for prevention of mother-to-child transmission of HIV-1 in Kampala, Uganda: HIVNET 012 randomised trial. Lancet 1999; 354:795–802.
9. PETRA Study Team. Efficacy of three short-course regimens of zidovudine and lamivudine in preventing early and late transmission of HIV-1 from mother to child in Tanzania, South Africa, and Uganda: a randomised, double-blind, placebo-controlled trial
10. Shaffer N, Chuachoowong R, Mock PA, Bhadrakom C, Siriwasin W, Young NL, et al
. Short-course zidovudine for perinatal HIV-1 transmission in Bangkok, Thailand: a randomised controlled trial: Bangkok Collaborative Perinatal HIV Transmission Study Group. Lancet 1999; 353:773–780.
11. Ayouba A, Tene G, Cunin P, Foupouapouognigni Y, Menu E, Kfutwah A, et al
. Low rate of mother-to-child transmission of HIV-1 after nevirapine intervention in a pilot public health program in Yaounde, Cameroon. J Acquir Immune Defic Syndr 2003; 34:274–280.
12. Connor EM, Sperling RS, Gelber R, Kiselev P, Scott G, O'Sullivan MJ, et al
. Reduction of maternal-infant transmission of human immunodeficiency virus type 1 with zidovudine treatment. Pediatric AIDS Clinical Trials Group Protocol 076 Study Group. N Engl J Med 1994; 331:1173–1180.
13. Dabis F, Msellati P, Meda N, Welffens-Ekra C, You B, Manigart O, et al
. 6-month efficacy, tolerance, and acceptability of a short regimen of oral zidovudine to reduce vertical transmission of HIV in breastfed children in Cote d'Ivoire and Burkina Faso: a double-blind placebo-controlled multicentre trial. DITRAME Study Group. Lancet 1999; 353:786–792.
14. Jackson JB, Musoke P, Fleming T, Guay LA, Bagenda D, Allen M, et al
. Intrapartum and neonatal single-dose nevirapine compared with zidovudine for prevention of mother-to-child transmission of HIV-1 in Kampala, Uganda: 18-month follow-up of the HIVNET 012 randomised trial. Lancet 2003; 362:859–868.
15. UNAIDS. Blood safety and AIDS: UNAIDS point of view
. Geneva: UNAIDS; 1997.
16. Klepp KI, Ndeki SS, Leshabari MT, Hannan PJ, Lyimo BA. AIDS education in Tanzania: promoting risk reduction among primary school children. Am J Public Health 1997; 87:1931–1936.
17. Stanton BF, Li X, Kahihuata J, Fitzgerald AM, Neumbo S, Kanduuombe G, et al
. Increased protected sex and abstinence among Namibian youth following a HIV risk-reduction intervention: a randomized, longitudinal study. AIDS 1998; 12:2473–2480.
18. Fawole IO, Asuzu MC, Oduntan SO, Brieger WR. A school-based AIDS education programme for secondary school students in Nigeria: a review of effectiveness. Health Educ Resources 1999; 14:675–683.
19. Ross DA, Todd J, Changalucha J, Plummer, M, Mosha F, Obasi A, et al
. A randomised controlled trial of an adolescents sexual and reproductive health intervention programme in rural Mwanza, Tanzania: 3 Results: knowledge, attitudes and behavior
. International Society of Sexually Transmitted Diseases Research Congress
, Ottawa, Canada, July 2003 [Abstract 698].
20. Walker D, Gutierrez JP, Torres P, Bertozzi S. A prospective randomized evaluation of a Mexican school-based HIV prevention intervention: Time to change course
. 2005 (submitted).
21. Sweat M, Gregorich S, Sangiwa G, Furlonge C, Balmer D, Kamenga C, et al
. Cost-effectiveness of voluntary HIV-1 counselling and testing in reducing sexual transmission of HIV-1 in Kenya and Tanzania. Lancet 2000; 356:113–121.
22. Voluntary HIV-1 Counseling and Testing Efficacy Study Group. Efficacy of voluntary HIV-1 counseling and testing in individuals and couples in Kenya, Tanzania, and Trinidad: a randomized trial
23. Kamenga M, Ryder RW, Jingu M, Mbuyi N, Mbu L, Behets F, et al
. Evidence of marked sexual behavior change associated with low HIV-1 seroconversion in 149 married couples with discordant HIV-1 serostatus: experience at an HIV cCounselling center in Zaire. AIDS 1991; 5:61–67.
24. Deschamps MM, Pape JW, Hafner A, Johnson WD Jr. Heterosexual transmission of HIV in Haiti. Ann Intern Med 1996; 125:324–330.
25. Kelly JA, Murphy DA, Sikkema KJ, McAuliffe TL, Roffman RA, Solomon LJ, et al
. Randomised, controlled, community-level HIV-prevention intervention for sexual-risk behaviour among homosexual men in US cities: Community HIV Prevention Research Collaborative. Lancet 1997; 350:1500–1505.
26. Kegeles SM, Hays RB, Coates TJ. The Mpowerment Project: a community-level HIV prevention intervention for young gay men. Am J Public Health 1996; 86:1129–1136.
27. Lauby JL, Smith PJ, Stark M, Person B, Adams J. A community-level HIV prevention intervention for inner-city women: results of the women and infants demonstration projects. Am J Public Health 2000; 90:216–222.
28. Stanton BF, Li X, Ricardo I, Galbraith J, Feigelman S, Kaljee L. A randomized, controlled effectiveness trial of an AIDS prevention program for low-income African-American youths. Arch Pediatr Adolesc Med 1996; 150:363–372.
29. Sikkema KJ, Kelly JA, Winett RA, Solomon LJ, Cargill VA, Roffman RA, et al
. Outcomes of a randomized community-level HIV prevention intervention for women living in 18 low-income housing developments. Am J Public Health 2000; 90:57–63.
30. Norr KF, Norr JL, McElmurry BJ, Tlou S, Moeti MR. Impact of peer group education on HIV prevention among women in Botswana. Health Care Women Intl 2004; 25:210–226.
31. Basu I, Jana S, Rotheram-Borus MJ, Swendeman D, Lee SJ, Newman P, Weiss R. HIV prevention among sex workers in India. J Acquir Immune Defic Syndr 2004; 36:845–852.
32. Ghys PD, Diallo MO, Ettiegne-Traore V, Kale K, Tawil O, Carael M, et al
. Increase in condom use and decline in HIV and sexually transmitted diseases among female sex workers in Abidjan, Cote d'Ivoire, 1991–1998. AIDS 2002; 16:251–258.
33. National Institute of Allergy and Infectious Diseases, DHSS, National Institutes of Health. Workshop summary: Scientific Evidence on Condom Effectiveness for Sexually Transmitted Disease (STD) Prevention, 2000. www.niaid.nih.gov/dmid/stds/condomreport.pdf
. Accessed 29 January 2004.
34. Hearst N, Chen S. Condoms for AIDS prevention in the developing world: a review of the scientific literature.
University of California: California; 2003.
35. Laga M, Alary M, Nzila N, Manoka AT, Tuliza M, Behets F, et al
. Condom promotion, sexually transmitted diseases treatment, and declining incidence of HIV-1 ifection in female Zairian sex workers. Lancet 1994; 344:246–248.
36. Levine WC, Revollo R, Kaune V, Vega J, Tinajeros F, Garnica M, et al
. Decline in sexually transmitted disease prevalence in female Bolivian sex workers: impact of an HIV prevention project. AIDS 1998; 12:1899–1906.
37. Bhave G, Lindan CP, Hudes ES, Desai S, Wagle U, Tripathi SP, Mandel JS. Impact of an intervention on HIV, sexually transmitted diseases, and condom use among sex workers in Bombay, India. AIDS 1995; 9(Suppl 1):S21–S30.
38. Pauw J, Ferrie J, Rivera Villegas R, Medrano Martinez J, Gorter A, Egger M. A controlled HIV/AIDS-related health education programme in Managua, Nicaragua. AIDS 1996; 10:537–544.
39. Ford K, Wirawan DN, Fajans P, Meliawan P, MacDonald K, Thorpe L. Behavioral interventions for reduction of sexually transmitted disease/HIV Transmission among female commercial sex workers and clients in Bali, Indonesia. AIDS 1996; 10:213–222.
40. Egger M, Pauw J, Lopatatzidis A, Medrano D, Paccaud F, Smith GD. Promotion of condom use in a high-risk setting in Nicaragua: a randomised controlled trial. Lancet 2000; 355:2101–2105.
41. Kagimu M, Marum E, Wabwire-Mangen F, Nakyanjo N, Walakira Y, Hogle J. Evaluation of the effectiveness of AIDS health education interventions in the Muslim Community in Uganda. AIDS Educ Prev 1998; 10:215–228.
42. Ngugi EN, Plummer FA, Simonsen JN, Cameron DW, Bosire M, Waiyaki P, et al
. Prevention of transmission of human immunodeficiency virus in Africa: effectiveness of condom promotion and health education among prostitutes. Lancet 1988; 2:887–890.
43. Celentano DD, Bond KC, Lyles CM, Eiumtrakul S, Go VF, Beyrer C, et al
. Preventive intervention to reduce sexually transmitted infections: a field trial in the Royal Thai Army. Arch Intern Med 2000; 160:535–540.
44. Bentley ME, Spratt K, Shepherd ME, Gangakhedkar RR, Thilikavathi S, Bollinger RC, Mehendale SM. HIV testing and counseling among men attending sexually transmitted disease clinics in Pune, India: changes in condom use and sexual behavior over time. AIDS 1998; 12:1869–1877.
45. Jackson DJ, Rakwar JP, Richardson BA, Mandaliya K, Chohan BH, Bwayo JJ, et al
. Decreased incidence of sexually transmitted diseases among trucking company workers in Kenya: results of a behavioural risk-reduction programme. AIDS 1997; 11:903–909.
46. Mehendale SM, Rodrigues JJ, Brookmeyer RS, Gangakhedkar RR, Divekar AD, Gokhale MR, et al
. Incidence and predictors of human immunodeficiency virus type 1 seroconversion in patients attending sexually transmitted disease clinics in India. J Infect Dis 1995; 172:1486–1491.
47. de Vincenzi I. A longitudinal study of human immunodeficiency virus transmission by heterosexual partners. European Study Group on Heterosexual Transmission of HIV. N Engl J Med 1994; 331:341–346.
48. Centers for Disease Control. HIV prevention through early detection and treatment of other STIs
. Atlanta, GA: Centers for Disease Control;1998.
49. Institute Of Medicine. The hidden epidemic: confronting sexually transmitted diseases
. Washington DC: National Academy Press; 1997.
50. Hook EW 3rd, Cannon RO, Nahmias AJ, Lee FF, Campbell CH Jr, Glasser D, Quinn TC. Herpes simplex virus infection as a risk factor for human immunodeficiency virus infection in heterosexuals. J Infect Dis 1992; 165:251–255.
51. Grosskurth H, Mosha F, Todd J, Mwijarubi E, Klokke A, Senkoro K, et al
. Impact of improved treatment of sexually transmitted diseases on HIV infection in rural Tanzania: randomised controlled trial. Lancet 1995; 346:530–536.
52. Kamali A, Quigley M, Nakiyingi J, Kinsman J, Kengeya-Kayondo J, Gopal R, et al
. Syndromic management of sexually-transmitted infections and behaviour change interventions on transmission of HIV-1 in Rural Uganda: a community randomised trial. Lancet 2003; 361:645–652.
53. Wawer MJ, Sewankambo NK, Serwadda D, Quinn TC, Paxton LA, Kiwanuka N, et al
. Control of sexually transmitted diseases for AIDS prevention in Uganda: a randomised community trial: Rakai Project Study Group. Lancet 1999; 353:525–535.
54. Korenromp EL, White RG, Orroth KK, Bakker R, Kamali A, Serwadda D, et al
. Determinants of the impact of sexually transmitted infection treatment on prevention of HIV infection: a synthesis of evidence from the Mwanza, Rakai, and Masaka intervention trials. J Infect Dis 2005; 191(Suppl 1):S168–S178.
55. Guay LA, Musoke P, Fleming T, Bagenda D, Allen M, Nakabiito C, et al
. Intrapartum and neonatal single-dose nevirapine compared with zidovudine for prevention of mother-to-child transmission of HIV-1 in Kampala, Uganda: HIVNET 012 randomised trial. Lancet 1999; 354:795–802.
56. The PETRA Study Team. Efficacy of three short-course regimens of zidovudine and lamivudine in preventing early and late transmission of HIV-1 from mother to child in Tanzania, South Africa, and Uganda (Petra study): a randomised, double-blind, placebo-controlled trial
57. Wiktor SZ, Ekpini E, Karon JM, Nkengasong J, Maurice C, Severin ST, et al
. Short-course oral zidovudine for prevention of mother-to-child transmission of HIV-1 in Abidjan, Cote d'Ivoire: a randomised trial. Lancet 1999; 353:781–785.
58. Lyons FE, Coughlan S, Byrne CM, Hopkins SM, Hall WW, Mulcahy FM. Emergence of antiretroviral resistance in HIV-positive women receiving combination antiretroviral therapy in pregnancy. AIDS 2005; 19:63–67.
59. Cunningham CK, Chaix ML, Rekacewicz C, Britto P, Rouzioux C, Gelber RD, et al
. Development of resistance mutations in women receiving standard antiretroviral therapy who received intrapartum nevirapine to prevent perinatal human immunodeficiency virus type 1 transmission: a substudy of pediatric AIDS clinical trials group protocol 316. J Infect Dis 2002; 186:181–188.
60. Cates W. A funny thing happened on the way to FHI. Sex Transm Dis 2004; 31:3–7.
61. Coutsoudis A. Breastfeeding and HIV transmission
. In: Michaelsen REBaKF, editor. Public health issues in infant and child nutrition, Vol. 48
. Nestle Nutrition Workshop Series, Lippincott, Williams and Wilkins: Philadelphia; 2002. 147–166.
62. Coutsoudis A, Pillay K, Spooner E, Kuhn L, Coovadia HM. Influence of infant-feeding patterns on early mother-to-child transmission of HIV-1 in Durban, South Africa: a prospective cohort study. South African Vitamin A Study Group. Lancet 1999; 354:471–476.
63. Morrison P. HIV and infant feeding: to breastfeed or not to breastfeed: the dilemma of competing risks. Part 2. Breastfeed Rev 1999; 7:11–20.
64. Nduati R, John G, Mbori-Ngacha D, Richardson B, Overbaugh J, Mwatha A, et al
. Effect of breastfeeding and formula feeding on transmission of HIV-1: A randomized clinical trial. JAMA 2000; 283:1167–1174.
65. Nduati R, John G. Breast milk transmission of HIV-1. NARESA Mongr 1995; 18:1–3.
66. Mesquita F, Doneda D, Gandolfi D, Nemes MI, Andrade T, Bueno R, et al
. Brazilian response to the human immunodeficiency virus/acquired immunodeficiency syndrome epidemic among injection drug users. Clin Infect Dis 2003; 37:S382–S385.
67. Vlahov D, Junge B. The role of needle exchange programs in HIV prevention. Public Health Rep 1998; 113(Suppl 1):75–80.
68. Des Jarlais D, Friedman S. HIV epidemiology and interventions among injecting drug users. Int J STD AIDS 1996; 7(Suppl 2):57–61.
69. Lurie P, Reingold AL, Bowser B, Chen D, Foley J, Guydish J, et al
. The public health impact of needle exchange programs in the United States and abroad, 1993
. volumes 1 and 2. San Francisco, CA: University of California.
70. US General Accounting Office (USGAO). Needle exchange programs: research suggests promise as an AIDS prevention strategy
. Washington, DC: US Government Printing Office; 1993.
71. Des Jarlais DC, Marmor M, Paone D, Titus S, Shi Q, Perlis T, et al
. HIV incidence among injecting drug users in New York City syringe-exchange programmes. Lancet 1996; 348:987–991.
72. Hurley SF, Jolley DJ, Kaldor JM. Effectiveness of needle-exchange programmes for prevention of HIV infection. Lancet 1997; 349:1797–1800.
73. Jenkins C, Rahman H, Saidel T, Jana S, Hussain AM. Measuring the impact of needle exchange programs among injecting drug users through the national behavioural surveillance in Bangladesh. AIDS Educ Prev 2001; 13:452–461.
74. Vlahov D, Junge B, Brookmeyer R, Cohn S, Riley E, Armenian H, Beilenson P. Reductions in high-risk drug use behaviors among participants in the Baltimore needle exchange program. J Acquir Immune Defic Syndr Human Retrovir 1997; 16:400–406.
75. Peak A, Rana S, Maharjan SH, Jolley D, Crofts N. Declining risk for HIV among injecting drug users in Kathmandu, Nepal: the impact of a harm-reduction programme. AIDS 1995; 9:1067–1070.
76. Ksobiech K. A meta-analysis of needle sharing, lending, and borrowing behaviors of needle exchange program attenders. AIDS Educ Prev 2003; 15:257–268.
77. National Consensus Development Panel on Effective Medical Treatment of Opiate Addiction. Effective medical treatment of opiate addiction
78. Needle RH, Coyle SL, Normand J, Lambert E, Cesari H. HIV prevention with drug-using populations - current status and future prospects: introduction and overview. Public Health Rep 1998; 113(Supp. 1):4–18.
79. Metzger DS, Navaline H, Woody GE. Drug abuse treatment as AIDS prevention. Public Health Rep 1998; 113(Suppl 1):97–106.
80. Lollis CM, Strothers HS, Chitwood DD, McGhee M. Sex, drugs, and HIV: does methadone maintenance reduce drug use and risky sexual behavior? J Behav Med 2000; 23:545–557.
81. Marsch LA. The efficacy of methadone maintenance interventions in reducing illicit opiate use, HIV risk behavior and criminality: a meta-analysis. Addiction 1998; 93:515–532.
82. Jacobs B, Mercer A. Feasibility of hospital-based blood banking: a Tanzanian case study. Health Policy Planning 1999; 14:354–362.
83. Foster S, Buve A. Benefits of HIV screening of blood transfusions in Zambia. Lancet 1995; 346:225–227.
84. Laleman G, Magazani K, Perriens JH, Badibanga N, Kapila N, Konde M, et al
. Prevention of blood-borne HIV transmission using a decentralized approach in Shaba, Zaire. AIDS 1992; 6:1353–1358.
85. Roth WK, Weber M, Seifried E. Feasibility and efficacy of routine PCR screening of blood donations for hepatitis C virus, hepatitis B virus, and HIV-1 in a blood-bank setting. Lancet 1999; 353:359–363.
86. Centers for Disease Control. Guidelines for the prevention of HIV and hepatitis B
. Atlanta, GA: CDC; 1989.
87. Mast S, Woolwine J, Gerberding J. Efficacy of gloves in reducing blood volumes transferred during simulated needlestick injury. J Infect Dis 1993; 168:1589–1592.
88. Cardo DM, Culver DH, Ciesielski CA, Srivastava PU, Marcus R, Abiteboul D, et al
. A case-control study of HIV seroconversion in health care workers after percutaneous exposure. Centers for Disease Control and Prevention Needlestick Surveillance Group. N Engl J Med 1997; 337:1485–1490.
89. Auvert B, Taljaard D, Lagarde E, Sobngwi-Tambekou J, Sitta R, Puren A. Randomized, controlled intervention trial of male circumcision for reduction of HIV infection risk: The ANRS 1265 Trial. PLoS Med 2005; 2:e298.
90. Janssen RS, Holtgrave DR, Valdiserri RO, Shepherd M, Gayle HD, De Cock KM. The serostatus approach to fighting the HIV epidemic: prevention strategies for infected individuals. Am J Public Health 2001; 91:1019–1024.
91. De Cock K, Marum E, Mbori-Ngacha D. A serostatus-based approach to HIV/AIDS prevention and care in Africa. Lancet 2003; 362:1847–1849.
This article has been cited 18 time(s).
Bmc Public HealthHealth diplomacy the adaptation of global health interventions to local needs in sub-Saharan Africa and Thailand: evaluating findings from Project Accept (HPTN 043)Bmc Public Health
Revista Panamericana De Salud Publica-Pan American Journal of Public Health
Effectiveness of antiretroviral treatment in Colombia
Revista Panamericana De Salud Publica-Pan American Journal of Public Health, 32(5):
Plos OneChanges in Sexual Behaviors among HIV-Infected Individuals after Their HIV Diagnosis in a Rural Prefecture of Eastern ChinaPlos One
Patterns of antiretroviral drug prescripcion in 997 Colombian patients
Moving beyond the alphabet soup of HIV prevention
Plos OnePotential Impact of Antiretroviral Chemoprophylaxis on HIV-1 Transmission in Resource-Limited SettingsPlos One
Infectious Disease Clinics of North AmericaThe future of HIV prevention: Control of sexually transmitted infections and circumcision interventionsInfectious Disease Clinics of North America
Reproductive Health MattersPreventing HIV with young people: A case study from ZambiaReproductive Health Matters
How can we calculate the "E" in "CEA"?
Bmc Public HealthHIV prevention for South African youth: which interventions work? A systematic review of current evidenceBmc Public Health
International Journal of EpidemiologyLocalized spatial clustering of HIV infections in a widely disseminated rural South African epidemicInternational Journal of Epidemiology
Journal of Health Care for the Poor and Underserved
An Effective, Low-cost Approach to Implementing HIV/AIDS Education Programs in Low Literacy Populations: An Example from Rural Haiti
Journal of Health Care for the Poor and Underserved, 21(2):
Sexually Transmitted InfectionsA systematic review of published evidence on intervention impact on condom use in sub-Saharan Africa and AsiaSexually Transmitted Infections
Journal of Clinical InvestigationThe spread, treatment, and prevention of HIV-1: evolution of a global pandemicJournal of Clinical Investigation
Journal of Child Psychology and PsychiatryPromoting child and adolescent mental health in the context of the HIV/AIDS pandemic with a focus on sub-Saharan AfricaJournal of Child Psychology and Psychiatry
JAIDS Journal of Acquired Immune Deficiency SyndromesIndividual, Social, and Environmental Influences Associated With HIV Infection Among Injection Drug Users in Tijuana, MexicoJAIDS Journal of Acquired Immune Deficiency Syndromes
HIV interventions; HIV prevention; effectiveness; efficacy; resource-limited countries
© 2006 Lippincott Williams & Wilkins, Inc.
Highlight selected keywords in the article text.