Current Opinion in HIV & AIDS:
Epidemiology: Edited by Tim Mastro and Quarraisha Abdool-Karim
Advances and future directions in HIV surveillance in low- and middle-income countries
Diaz, Theresaa; Garcia-Calleja, Jesus Mb; Ghys, Peter Dc; Sabin, Keitha
aCenters for Disease Control, National Center for HIV, Hepatitis, STD, and TB Prevention, Global AIDS Program, Atlanta, Georgia, USA
bWorld Health Organization, Switzerland
cJoint United Nations Programme on HIV/AIDS (UNAIDS), Geneva, Switzerland
Correspondence to Theresa Diaz, MD, MPH, Centers for Disease Control and Prevention, Global AIDS Program, MS E-30, 1600 Clifton Road Atlanta, GA 30033, USA Tel: +1 404 639 6312; e-mail: TDiaz@cdc.gov
Purpose of review: To present recent advances in HIV/AIDS surveillance methods in low- and middle-income countries.
Recent findings: From 2001 to 2008, 30 low- and middle-income countries implemented national population-based surveys with HIV testing. Antenatal clinic HIV sentinel surveillance sites in sub-Saharan Africa increased from just over 1000 in 2003–2004 to almost 2500 in 2005–2006, becoming more representative of rural areas. Between 2003 and 2007, at least 122 behavioral surveys in low- and middle-income countries used respondent-driven sampling for surveillance among high-risk populations, although many countries with concentrated epidemics continue to have major sentinel surveillance gaps. Improvements have been made in modeling estimates of number of persons HIV infected, and systems are now in place to measure HIV drug resistance. However, the reliable monitoring of trends and the measuring of HIV incidence, morbidity, and mortality is still a challenge.
Summary: In the past 5 years, there have been substantial improvements in the quantity and quality of HIV surveillance studies, especially in the countries with high prevalence. Further efforts should be made in countries that lack fully implemented surveillance systems to improve HIV incidence, morbidity, and mortality surveillance and to use data more effectively.
Surveillance is a foundation of the public health response to the HIV pandemic. The ability to understand the important sources of recent infections, to monitor the spread of infection and the trends in specific groups, and to measure the associated morbidity is critical for intervening against further transmission and allocating resources.
The establishment of the Global Fund to Fight AIDS, Tuberculosis and Malaria (GFATM) in 2001 and the President's Emergency Plan for AIDS Relief (PEPFAR) in 2003 brought an unparalleled infusion of funding to combat HIV. Since 2003, investments in fighting the epidemic have risen from US$300 million to US$8 billion a year . With these investments came a greater demand for accountability, trend analysis, and impact evaluation. Surveillance data are critical for these analyses.
In January 2004, over 250 HIV surveillance experts gathered in Addis Ababa, Ethiopia to review the status of HIV/AIDS surveillance methods and activities in low- and middle-income countries. The meeting proceedings [2–10] highlighted new methods in use, the limitations and gaps in HIV surveillance, and recommended future strategies. Advances made since 2004 included implementation of strategies that were suggested at the Ethiopia conference. Recent downward revisions in global HIV estimates in part reflect these improvements .
This article reviews some key advances in HIV surveillance in preparation for a second conference on Global HIV/AIDS Surveillance that took place in Bangkok, Thailand in February of 2009. The study is organized according to the framework of HIV infection and its progression to AIDS and death (Fig. 1).
Surveillance of risk for HIV transmission
The advent of second-generation HIV surveillance guidelines in 2000 recognized the importance of behavioral surveillance . Surveillance of behaviors that place people at greater risk for HIV transmission is critical to an understanding of the trajectory of an epidemic and the required response.
In countries where HIV transmission is largely through heterosexual behaviors in the general population, population-based household surveys of behaviors are warranted . Between 2001 and 2008, 30 countries implemented national population-based surveys with HIV testing . Six countries (Botswana, Côte d'Ivoire, Guyana, Kenya, Tanzania, Uganda, and Vietnam) completed AIDS Indicators Surveys (AIS). AIS are shorter and less expensive as compared with multipurpose surveys such as Demographic Health Surveys (DHS). General national population surveys are usually conducted every 5 years with AIS between these, to discern trends faster.
The standard approach for countries with epidemics concentrated among well defined subpopulations, for example men who have sex with men (MSM), injection drug users (IDUs) and female sex workers (FSWs), was, prior to 2004, serial behavioral surveillance surveys of these groups, typically without HIV testing and using convenience sampling . Major developments since 2004 include routine specimen collection for testing and probability sampling methods [14–17]. Between January 2003 and 1 October 2007, at least 122 behavioral surveys, with and without HIV testing have used respondent-driven sampling (RDS), a technique that often yields a more representative sample. Some countries have collected multiple surveillance rounds, permitting valid trend analyses . Despite the potential of RDS, the methods for analyses of these data are complicated and still being modified . Other sampling methods such as venue-based (e.g., bars and brothels) and time-location sampling (e.g., identifying days and times when the target population gathers at specific venues) continue to be used for populations that congregate in identifiable locations [20,21].
The increased use of qualitative methods (e.g., focus groups and key informants interviews) to inform and enrich surveys represents another advance. Unfortunately, few formative ethnographic works [22,23] are published but these reports demonstrate that the understanding of behaviors in a cultural context can improve the implementation of behavioral surveys.
When data are collected in the general population or among high-risk groups, bias is always possible (e.g., recall and social desirability) and some biases may change over time, rendering interpretation of behavioral trends difficult. Newer survey techniques, such as audio computer-assisted self-interviews (ACASIs), may introduce less bias and can be used despite illiteracy and lack of computer experience .
Sexually transmitted infection (STI) surveillance should also be conducted because high levels of STIs may indicate high levels of risky sexual behavior, putting persons at risk of acquiring HIV . STI prevalence assessments should be incorporated into HIV prevalence surveys, especially in high-risk populations (MSM and FSWs) who acquire HIV through sex.
HIV surveillance of newly infected persons
HIV incidence is estimated in developing countries mostly by mathematical modeling, using data from prevalence surveys [26–28]. These models typically require many assumptions, (mortality rates, risk behaviors, and HIV-transmission probabilities). Since 2004, HIV incidence estimates using data from serological assays that detect recent HIV infections have been used more frequently. Current serologic assays are based on measurement of degrees of antibody maturation (quantitative, qualitative, or both). One such assay is the immunoglobin G capture BED enzyme immunoassay, BED-CEIA. This assay tends to misclassify a substantial proportion of persons with long-standing infection as recent, resulting in overestimations of HIV incidence [29,30]. The USA used BED-CEIA results and HIV case reports [which contains information on antiretroviral therapy (ART) treatment and length of infection] in combination with modeling to report HIV incidence, but low- and middle-income countries lack comprehensive HIV case reporting systems [31,32]. The BED-CEIA assay has been used in some sentinel surveillance and population-based surveys in low- and middle-income countries [33–37]. To avoid biased HIV incidence estimates using BED-CEIA, individuals known to be infected for many years, on ART, or with very low CD4 cell counts need to be identified and removed from the dataset. Locally appropriate adjustments should be made to account for misclassification of persons with long-standing HIV infection as incident [38–42].
Other laboratory assays to measure HIV incidence are being validated. Most of these assays are based on antibody avidity, the low sensitivity of the HIV test, or the order of appearance of antibodies to different proteins [43,44]. A two-test algorithm may be required to increase the accuracy of detecting recent HIV infections and incidence estimates.
Given the increased emphasis on early infant diagnosis and the scarcity of surveillance data among children, the development of national systems to report HIV cases among infants identified by laboratory diagnosis is a critical part of comprehensive HIV case reporting systems.
Among recently infected persons, the rate of transmitted HIV drug resistance (HIVDR) should be measured, especially in countries with extensive treatment coverage . At least seven countries have conducted threshold surveys to measure HIVDR. As of 2008, little or no resistance has been found [46–52].
HIV prevalence surveillance
AIDS case reporting was the standard for surveillance for the past two decades. Increased access to ART has reduced its utility except to monitor therapeutic failure or ability to access certain populations with therapy. Several different case definitions that did not coincide with clinical staging were used for case reporting. The WHO now recommends reporting HIV cases and advanced HIV infection. Since March 2006, WHO's recommended HIV case surveillance definition includes four clinical stages corresponding to clinical treatment determinations .
The number of low-income countries conducting HIV case reporting has not increased since the change of the case definition. New HIV testing policies and the scale-up of care and treatment should increase the number of people tested for HIV. HIV reporting can provide a good measure of the number of persons with HIV who will access healthcare, allowing countries to plan for the burden on their healthcare systems.
HIV sentinel surveillance among antenatal care (ANC) clients has been implemented since the late 1980s . This surveillance is recommended for countries with generalized epidemics  and entails using leftover blood from routine ANC testing, unlinking samples from identifying information and testing for HIV, referred to as unlinked anonymized testing (UAT). This procedure is typically done over a 12-week period.
The major advances in antenatal sentinel surveillance include the expansion of testing sites in urban and rural areas, increased sample size, and improvement in quality and analysis of these surveys [56•]. In 2003–2004, there were slightly more than 1000 ANC sentinel surveillance sites in 32 African countries. By 2005–2006, this figure rose to almost 2500 in 31 African countries .
Correct trend analysis is critical. Appropriate analyses include nonparametric methods (e.g., Paired Sign test and Wilcoxon sign-rank test) and linear regression applied to data from consistent sites to ensure that additional sites do not erroneously change reported national prevalence or random effects regression to data from all sites. Ideally, trend analysis uses more than one method.
Because prevention of mother-to-child transmission (PMTCT) services has increased, several studies [58–60] have examined the use of PMTCT HIV prevalence data in place of UAT ANC sentinel surveillance. These studies have found substantial variations in HIV prevalence between these data. PMTCT data are often of poor quality and cumbersome to use for surveillance purposes [3,61].
Since 2000, there has been an increase in countries conducting population-based surveys with HIV testing. Compared with ANC surveillance, these surveys are more geographically representative of the country, include more rural areas, larger age ranges, and men [62,63]. Since 2000, around 25 African countries have conducted such surveys . These surveys usually find lower HIV prevalence than that estimated by UAT ANC sentinel surveillance. In countries where most HIV transmission takes place in the general population, the HIV prevalence measured in these surveys is believed to be close to the true population level .
Population-based surveys with HIV testing are not useful to estimate HIV prevalence in settings in which HIV infection is concentrated in groups with high-risk behaviors  For example, Vietnam's Hai Phong province has very high HIV prevalence. Among IDUs (≈60%), but prevalence was 0.5% in a 2005 AIS.
With more countries conducting population-based surveys with HIV testing, associations between HIV status and reported behaviors can be analyzed, although interpretation of cross-sectional data must be undertaken cautiously. Behaviors of HIV-positive persons can also be examined more closely. Additional testing for infectious diseases relevant to HIV progression or coinfection (e.g., syphilis, hepatitis, and HSV2) were added to surveys in Kenya  and Uganda, and CD4 cell count was added in Kenya . HIV prevalence trends can be better assessed as countries repeat these surveys.
A majority of countries (140), representing approximately one-third of all persons living with HIV, have HIV epidemics concentrated in one or more subpopulations, typically MSM, IDUs, sex workers, or all. HIV surveillance of these groups is critical to a strong understanding of the epidemic, yet recent analyses show that major gaps in surveillance of these groups persist in many countries [56•]. Even in generalized epidemics tracking HIV among groups with high-risk behaviors is important because the higher HIV prevalence in these groups can influence the national epidemic. Since 2004, surveillance of high-risk groups frequently combines biological and behavioral data collection.
Morbidity, HIV drug resistance, and mortality surveillance
As more people access treatment and live longer, it is critical to monitor morbidity and mortality. HIVDR surveillance has expanded to include the monitoring of drug resistance among newly infected individuals to assess the transmission of drug-resistant virus and to examine resistance among patients undergoing treatment [67,68].
Surveillance for opportunistic infections, especially tuberculosis (TB), is critical to monitoring the quality and impact of treatment and prophylaxis. Although guidelines exist on HIV surveillance among TB patients, little has been done regarding other opportunistic infections. Instituting HIV or advanced HIV infection case reporting should allow for improved reporting and monitoring of morbidity.
Unfortunately, mortality surveillance has not improved. Although the methods to perform Sample Vital Registration with Verbal Autopsies have been elucidated in training materials, very few countries have implemented this system . Other sources of mortality data, such as burial and demographic surveillance sites, have little coverage and rarely parse out AIDS-related mortality [70,71]. Improving vital registration systems is critical to enhancing the understanding of causes of mortality, including HIV/AIDS and their trends.
Since 2004, HIV surveillance systems have expanded and improved considerably, providing more reliable data for modeling estimates of number of persons with HIV infection. There have been great advances in modeling estimates and projections since 2004. Joint United Nations Programme on HIV/AIDS (UNAIDS) Estimation and Projection Package (EPP), Workbook and Spectrum tools generate an HIV prevalence curve based on HIV prevalence data from surveillance, surveys, and special studies, and allow to estimate the number of people living with HIV, HIV incidence, ART needs, and orphanhood due to AIDS and mortality. Data from national surveys have been used in several countries with generalized epidemics to adjust HIV prevalence [72,73]. Findings from multiple studies have resulted in the increase in assumed time from seroconversion to ART eligibility and assumed median survival time from 9 to 11 years in most low and middle-income countries . These changes yielded a higher estimate of the number of people requiring ART . Improved methods have produced more appropriate plausibility ranges around the estimates .
One of the best ways for countries to guide their prevention programs is to examine where the newest infections arise. Analysis of data in Ghana and Benin showed a large proportion of adult male infections were likely due to sex with a commercial sex worker, whereas only 1% of World Bank prevention funding goes toward programs for sex workers . UNAIDS has led the development of an analytic tool to estimate HIV incidence by mode of transmission, which uses surveillance data, population size estimates, and transmission probabilities .
Triangulation, examining different surveillance and program data together, has been used in several countries to determine the overall trend of HIV prevalence and the reach and coverage of prevention programs based on these trends or the impact of ART programs on mortality [79,80].
Surveillance data should be used for impact evaluation by measuring the extent to which change in a population-based outcome can be attributed to program intervention. To this end, in November 2006, GFATM began to study the impact of its investments and those of other funding partners in reducing the health burden of HIV, TB, and malaria in select countries. The study uses HIV surveillance data and modeling to compare incidence, prevalence, mortality, and behavior change trends with changes in prevention and treatment program coverage .
One challenge of surveillance for HIV infection is to collect valid data while maintaining ethical standards of confidentiality and not harming individuals . The current debate focuses on the rights of persons to know their HIV test results when their blood is used for surveillance purposes, either knowingly or unknowingly . A component of the challenge is when and how to incorporate a program to return HIV test results with counseling. When conducting surveillance, governments should follow the Declaration of Helsinki, which states that individual autonomy should be respected; the endeavor should benefit the population, if not individuals, and no harm should be done .
The future of surveillance activities should concentrate on the implementation of sentinel surveillance in groups with high-risk behaviors in a large number of countries, improving methods to estimate HIV incidence, improving our ability to monitor trends in prevalence, implementing HIV infection, case reporting, using data from ART treatment programs, increasing mortality surveillance, and improving overall vital registration systems. Greater attention should be paid to improving the quality of behavioral survey instruments through cognitive research and anthropology, understanding risky behaviors, including concurrent sexual partnerships. Additionally, the introduction of social network data and analysis to further enrich surveillance data requires exploration. As more antiretroviral treatment and prophylaxis is provided to HIV-infected mothers, national-level information on mother-to-child HIV transmission rates and HIV treatment outcomes is urgently needed. It is vital to improve surveillance quality and emphasize local capacity building to collect, analyze, evaluate, and utilize data.
Countries should move away from basing programmatic decisions on narrow categories that have been used to classify epidemics in the past (e.g., generalized and concentrated), and instead focus on the local importance of different population groups for HIV transmission.
Finally, we must use data more effectively. We have entered a data-rich time in the history of this epidemic and we need to use the data to support decisions on resource allocation, program planning, and impact assessment.
In the past 5 years, there have been substantial improvements in the quantity and quality of HIV surveillance studies in resource-constrained countries. Challenges still exist in measuring incidence, morbidity, and mortality. Data have been used more frequently to plan for HIV care, treatment, and prevention activities, but given the substantial increase in data, more analyses and interpretation are needed.
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Additional references related to this topic can also be found in the Current World Literature section in this issue (p. 336).
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AIDS; HIV; low- and middle-income countries; surveillance
© 2009 Lippincott Williams & Wilkins, Inc.
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