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Estimated HIV Trends and Program Effects in Botswana John Stover1*, Boga Fidzani2,3, Batho Chris Molomo2, Themba Moeti3, Godfrey Musuka3 1 Futures Institute, Glastonbury, Connecticut, United States of America, 2 National AIDS Coordinating Agency, Gaborone, Botswana, 3 African Comprehensive HIV/AIDS Background: This study uses surveillance, survey and program data to estimate past trends and current levels of HIV inBotswana and the effects of treatment and prevention programs.
Methods/Principal Findings: Data from sentinel surveillance at antenatal clinics and a national population survey were usedto estimate the trend of adult HIV prevalence from 1980 to 2007. Using the prevalence trend we estimated the number ofnew adult infections, the transmission from mothers to children, the need for treatment and the effects of antiretroviraltherapy (ART) and adult and child deaths. Prevalence has declined slowly in urban areas since 2000 and has remained stablein rural areas. National prevalence is estimated at 26% (25–27%) in 2007. About 330,000 (318,000–335,000) people areinfected with HIV including 20,000 children. The number of new adult infections has been stable for several years at about20,000 annually (12,000–26,000). The number of new child infections has declined from 4600 in 1999 to about 890 (810–980)today due to nearly complete coverage of an effective program to prevent mother-to-child transmission (PMTCT). Theannual number of adult deaths has declined from a peak of over 15,500 in 2003 to under 7400 (5000–11,000) today due tocoverage of ART that reaches over 80% in need. The need for ART will increase by 60% by 2016.
Conclusions: Botswana’s PMTCT and treatment programs have achieved significant results in preventing new childinfections and deaths among adults and children. The number of new adult infections continues at a high level. Moreeffective prevention efforts are urgently needed.
Citation: Stover J, Fidzani B, Molomo BC, Moeti T, Musuka G (2008) Estimated HIV Trends and Program Effects in Botswana. PLoS ONE 3(11): e3729. doi:10.1371/journal.pone.0003729 Editor: Douglas F. Nixon, University of California San Francisco, United States of America Received July 28, 2008; Accepted October 25, 2008; Published November 14, 2008 Copyright: ß 2008 Stover et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was funded by the Bill and Melinda Gates Foundation through the African Comprehensive HIV/AIDS Partnership. The funders had no role inthe study design, data collection and analysis, decision to publish or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
Botswana has one of the highest levels of HIV in the world.
The HIV surveillance program conducts annual HIV surveys UNAIDS estimated that adult prevalence was about 24% in 2005, among women aged 15–49 years attending ante-natal clinics.
higher than any other country except Swaziland [1]. The epidemic Surveillance has been conducted annually since 1992 and now has imposed a terrible burden due to lives lost, reduced quality of includes 24 sites [5]. Since these surveys measure HIV prevalence life and a large number of orphans. Since 2003 Botswana and its in pregnant women they do not represent prevalence in all adults, development partners have launched strong efforts to prevent the including both men and women. However, since ANC surveil- transmission of HIV from mothers to their children and to provide lance is conducted annually it does provide information on trends advanced treatment to those who need it. Information on in prevalence that should be representative of those in the general epidemic trends is available from sentinel surveillance conducted annually at antenatal clinics around the country. Program statistics The Botswana AIDS Impact Survey II (BAIS II) conducted in describe the expansion of the PMTCT and treatment programs 2004 measured the prevalence of HIV infection in the population aged 18 months and above [6]. Although only 61% of those Comprehensive assessments of the demographic impact of the interviewed in this survey agreed to provide a blood sample for epidemic were conducted for Botswana in 2000 [3] and 2006 [4].
HIV testing, the results of this survey are thought to provide a This report expands and updates those analyses using the latest reasonably accurate measure of HIV prevalence in 2004.
surveillance and program data as well as updated models The UNAIDS Reference Group on Estimates, Models and developed by UNAIDS. It describes the use of these data to Projections has developed several tools to estimate national estimate national prevalence in Botswana and to assess the prevalence. One of these tools, the Estimation and Projection implications of that estimate for other indicators of interest, such as Package (EPP), is used in most countries in sub-Saharan Africa to the number of people infected, the annual number of new estimate prevalence trends from surveillance and survey data in infections, the number of people in need of ART, and the impact countries with generalized epidemics [7]. EPP works by fitting a of the PMTCT and treatment programs.
simple epidemic model to surveillance data from multiple sites November 2008 | Volume 3 | Issue 11 | e3729 over time. Separate estimates are made for urban and rural Table 1. Key HIV/AIDS Indicators and Plausibility Bounds, prevalence and then combined to produce a national estimate.
The epidemic model uses four parameters to determine the prevalence trend over time: the start year of the epidemic, theinitial force of infection, the proportion of the population at risk of infection and the rate of replenishment of the population at riskwhen it is depleted by AIDS deaths. EPP generates 50,000 to 200,000 epidemic curves by randomly selecting values of these four parameters from plausible distributions. Each of these curves is tested to see how well it fits the surveillance and survey data. A sample of curves is drawn from the full set with the likelihood of selection proportional to the goodness of fit. The result is a most likely curve that provides a point estimate of prevalence in eachyear and a range around the point estimate.
The estimates of adult HIV prevalence are used in the AIDS module of Spectrum [8] to estimate the other indicators of interest such as the number of people living with HIV, new infections, AIDS deaths, need for treatment and the number of orphans. HIV prevalence among adults 15–49 is combined with information onthe age and sex distribution of prevalence from the national survey to estimate the distribution of prevalent adult infections by age and sex. The trend in prevalence is combined with information on thedistribution of time from infection to AIDS death from cohort to produce 5% and 95% plausibility bounds around each point studies to estimate the number of new adult infections by age and estimate. (These are not true confidence intervals since the errors sex. New infant infections are estimated from prevalence among around the input assumptions are not measured directly and we pregnant women and the rate of mother-to-child transmission, which is dependent on infant feeding practices and the coverage ofprophylaxis with ARVs. New infections progress over time to a symptomatic stage where ART is needed.
The rate of progression from infection to AIDS death for adults Results for key HIV/AIDS indicators are shown in Table 1.
is a distribution drawn from cohort studies in sub-Saharan Africa The plausibility bounds for prevalence and number of adults [9]. The median time from infection to AIDS death without infected are narrow because the national survey provided an treatment is 11 years. Eligibility for ART is assumed to occur at a accurate estimate of the level of infection in 2004. Bounds for median of three years before AIDS death [10]. Those who receive other indicators rely on additional assumptions, such as the first- and/or second-line ART experience extended survival. In progression period from infection to death and the effects of ART Botswana, program data are available on the proportion of ART and PMTCT and, therefore, are wider.
patients who are known to be alive by time since the initiation oftherapy. As of December 2007 information is available on 75,393 patients. These data show that after 12 months, 91.3% of ART HIV trends at antenatal surveillance sites are shown for urban patients are known to be still alive, and after five year 86% of ART and rural sites in Figure 1. The best fitting curves to these data patients are still alive. These rates mayoverstate the true survival suggest that HIV prevalence has declined somewhat in urban since some of those who were lost to follow-up (i.e. their status is areas since 2000 and has remained stable in rural areas. These unknown) have probably died. The UNAIDS Reference Group on curves need to be adjusted to match the national population survey Estimates, Models and Projections assumes that for most newprograms the annual survival rates are 85% for the first year onART and 95% for subsequent years [10]. However, the first yearsurvival is likely to be lower in new programs with low ARTcoverage since most patients get started on ART very late, withlow CD4 counts. When coverage is high as in Botswana patientsare identified as being in need earlier and generally start ART athigher CD4 counts which should result in better first year survival.
People at any stage are subject to non-AIDS mortality at the same rates as those who are not infected. The progression ofchildren from infection to AIDS death is modeled as a doubleWeibull curve fitted to longitudinal data [11]. AIDS and non-AIDS orphans are estimated from the number of adult deaths eachyear, the fertility history of those who die and the rates of childsurvival.
Spectrum estimates the uncertainty around the estimate of each indicator by using a Monte Carlo approach. One thousand Figure 1. HIV prevalence among women attending antenatal projections are calculated using different prevalence curves clinics, 1991–2007. Data from urban clinics (Figure 1a) and rural provided by EPP and drawing random values of other key clinics (Figure 1b) are shown in the gray lines. The smooth curve parameters (such as the progression time to AIDS death, and the produced by EPP is shown in the dark dashed line for each region.
effectiveness of ART) for each projection. The results are analyzed November 2008 | Volume 3 | Issue 11 | e3729 of 2004. The urban curve needs to be adjusted downwards by 40% lower. We estimate that prevalence would have declined to 22.7% to account for the bias in urban surveillance sites compared to the in 2007, three percentage points lower than the actual estimate.
entire urban population. The rural curve needs to be adjusted Those currently receiving ART will continue to need it for downwards by only 15%. In making this adjustment we assume many years to come. In addition, about 23,000 adults newly that the ANC data represent the trend in prevalence and the progress to need for ART each year. As a result the need for ART national survey best represents the level.
is expected to increase by almost 60% from 120,000 (101,000– When these curves are adjusted to match the national 136,000) in 2007 to about 190,000 by 2016 if the high levels of population survey of 2004 and weighted by the adult urban and coverage are maintained. This has important cost and sustain- rural populations they suggest that national prevalence among all ability implications for the programme.
adults 15–49 in Botswana peaked at about 26% in 2001 and hassince declined slightly to 25.7% (24.8%–26.7%) by 2007. This Child infections and the effects of PMTCT implies that 280,000 adults 15–49 are currently infected, 47% in The high levels of HIV infection in adults mean that many urban areas and 53% in rural areas. While the national survey in children are exposed to the risk of acquiring infection from their 2004 found that the peak ages for prevalence were 30–34 for both mothers. The estimated number of new infections among children men and women, high levels of prevalence persist up to ages 70– peaked at around 4600 in 1999. PMTCT services were introduced 74. When adult infections over the age of 49 are included the total in 2002 and coverage expanded rapidly. By 2007 91% of HIV- number of adults infected with HIV is estimated to be about positive pregnant women received antiretrovirals to reduce the risk of mother-to-child transmission [12]. More than half of these womenreceive a combination of single dose Nevirapine and AZT. The program carefully tracks women attending antenatal care and The prevalence trend combined with the pattern of progression women giving birth recording HIV status and for those HIV+ from new infection to AIDS death indicates that the annual women it reports the number of women evaluated for ART, eligible number of new adult infections peaked at around 33,000 in 1995 for ART, already on ART, and use of AZT, Nevirapine and co- and declined to about 20,000 by 2002 and is currently around trimoxazole. Since early 2007 the program has tracked outcomes for children born to HIV-positive mothers by using dried blood spots Incidence among those 15–49 is declining, from 3.5% in 2000 and PCR tests on all children born to HIV+ mothers. The results to to 2.4% in 2007. While the overall population growth rate in date indicate that the program has reduced the average mother-to-child transmission rate to just 3.7% by 2007 [12]. Using this figure Botswana has declined to about 1.7% today, the annual growth we estimate that the annual number of new child infections is now rate among all adults is still 2.4%. Therefore, the overall absolute about 890 (810–980) (Figure 2a). The expansion of the PMTCT number of new infections each year is approximately constant.
program has averted 10,000 child infections from 2002 to 2007.
HIV-positive children have benefited from an expansion of treatment programs. By the end of 2007 7,400 children were The annual number of adult AIDS deaths rose steadily during receiving ART, nearly all those estimated to be in need, and almost the 1980s and 1990s to a peak of nearly 16,000 in 2003. Without 10,000 were receiving co-trimoxazole. As a result child AIDS deaths any ART program adult AIDS deaths would have continued have been reduced from about 3,000 in 2001 to 790 (600–1020) in increasing to nearly 23,000 in 2007. However, Botswana has 2007. Nearly 11,000 child deaths have been averted by the implemented a vigorous treatment program that has expanded the combined effects of PMTCT, child treatment and adult ART.
number of adults receiving ART from 932 in 2000 to 85,497 bythe end of 2007, about 83% of need [11]. As a result the estimated number of adult AIDS deaths has dropped to 7400 (5000–11,000) As a result of adult AIDS deaths a significant proportion of in 2007 (Figure 2b). The provision of ART has averted an children have lost one or both parents. We estimate that there estimated 53,000 deaths from 2000 to 2007. If these deaths had were 130,000 (110,000–150,000) orphans in 2007, about 16% of not been averted by ART then AIDS deaths would have exceeded all children under the age of 18. Three-quarters of these orphans new infections and adult HIV prevalence would have been much are due to AIDS. One-third of households caring for orphans arereceiving external support [12]. The success of the adult ARTprogram has reduced the number of new orphans each year by40%, from 20,000 in 2002 to 12,000 in 2007.
Botswana has an HIV surveillance system and a national HIV survey that provide the basis for estimates of the extent of the HIVepidemic and its dynamics. These data indicate that prevalence iscurrently declining slightly in urban areas and stable in rural areas.
The estimates produced from these data indicate that the numberof new infections rose rapidly during the early 1990s, peaking inthe mid-1990s before falling to a stable level of about 18,000 newinfections per year today. The number of AIDS deaths started togrow rapidly about 10 years later than the rise in new infections,peaking just before the expansion of ART.
The successful expansion of the ART program has increased Figure 2. Annual number of new child infections (Figure 2a)and adult deaths (Figure 2b), 1980–2007.
coverage to over 80% of those in need of treatment. This expansion has had significant benefits, reducing the annual November 2008 | Volume 3 | Issue 11 | e3729 The PMTCT program represents a major success with over 90% of HIV-positive women receiving antiretrovirals to prevent trans-mission of HIV to their children. The program has averted anestimated 10,000 child infections since its inception. The combinedeffects of the PMTCT program and the child treatment programhave averted an estimated 11,000 child AIDS deaths. With fewernew child infections the need for child treatment is also be reduced.
Unfortunately similar progress has not been made in reducing the number of new adult infections (Figure 3). Some preventionprograms have been expanded to scale. Condom use in Botswanais among the highest anywhere in the world. High coverage hasbeen achieved for voluntary counseling and testing and AIDSeducation in the schools. But these programs have not beenenough to make a significant difference. The proportion of adults Figure 3. Annual number of new adult HIV infections and AIDS with more than one sexual partner remains very high. A high level of partner concurrency contributes to rapid reproduction of new infections. New approaches are urgently needed. At the currentrate of new infections prevalence will remain at very high levels number of AIDS deaths by half and, as a consequence, also cutting and the burden to expand treatment programs in the future will in half the number of new orphans each year. The high coverage of adult ART has also contributed to a reduction in mother-to-child transmission of HIV.
Due to the high number of new infections in the past 24,000 adults progress to eligibility for ART each year. As a result, the need for Conceived and designed the experiments: BF TM GM. Analyzed the data: adult ART will increase by nearly 60% by 2016. This presents a JS BF TM. Wrote the paper: JS BF BCM TM GM.
major challenge to maintain the current levels of high coverage.
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9. Todd J, Glynn J, Marston M, Rangsin R, Lutalo T, et al. (2007) ‘‘Time from 3. Abt Associates South Africa Inc. (2000) An Impact Assessment of HIV/AIDS on HIV sero-conversion to death prior to ART: a collaborative analysis of eight Current and Future Population Characteristics and Demographics in Botswana. Gaborone, studies in six developing countries.’’ AIDS vol 21 sup 6: S55–S63.
Botswana: Coordinated by the Ministry of Finance and Development Planning 10. Stover J, Johnson P, Zaba B, Zwahlen M, Dabis F, Ekpini R (2008) ‘‘The in collaboration with UNDP and the Ministry of Health.
Spectrum projection package: improvements in estimating mortality, ART 4. Dorrington RE, Moultrie TA, Daniel T (2006) The Demographic Impact of needs, PMTCT impact and uncertainty bounds.’’ Sex. Transm. Inf. 84: i24–30.
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11. Marston M, Zaba B, Solomon JA, et al. (2005) ‘‘Estimating the net effect of HIV 5. Ministry of Health (2005) Botswana Second Generation HIV/AIDS Surveillance, 2005.
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12. National AIDS Coordinating Agency (2007) 2008 Progress Report of the 6. National AIDS Coordinating Agency (NACA), CSO and Other Development National Response to the UNGASS Declaration of Commitment on HIV/ Partners (2005) Botswana AIDS Impact Survey II: Statistical Report. Gaborone: AIDS, Ministry of State President, National AIDS Coordinating Agency, 7. Brown T, Grassly NC, Garnett G, Stanecki K (2005) ‘‘Improving projections at 13. Tlale J, Keapoletswe K, Anderson MG, Gomez FdlH, Mmelesi M, Seipone K the country level: the UNAIDS Estimation and Projection Package 2005.’’ Sex (2008) Mother-to-child transmission rate in Botswana–analysis of dried blood spot (DBS) results from the national PMTCT programme, Abstract presented atthe International AIDS Conference, Mexico City, August 2008.
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