Screening acute HIV infections among Chinese men who have sex with men from voluntary counseling & testing centers

Background

Recent studies have shown the public health importance of identifying acute HIV infection (AHI) in the men who have sex with men (MSM) of China, which has a much higher risk of HIV transmission. However, cost-utility analyses to guide policy around AHI screening are lacking.

Methodology/Principal Findings

An open prospective cohort was recruited among MSM living in Liaoning Province, Northeast China. Blood samples and epidemiological information were collected every 10 weeks. Third-generation ELISA and rapid test were used for HIV antibody screening, western blot assay (WB) served for assay validation. Antibody negative specimens were tested with 24 mini-pool nucleic acid amplification testing (NAAT). Specimens with positive ELISA but negative or indeterminate WB results were tested with NAAT individually without mixing. A cost-utility analysis of NAAT screening was assessed. Among the 5,344 follow-up visits of 1,765 MSM in 22 months, HIV antibody tests detected 114 HIV chronic infections, 24 seroconverters and 21 antibody indeterminate cases. 29 acute HIV infections were detected with NAAT from 21 antibody indeterminate and 1,606 antibody negative cases. The HIV-1 prevalence and incidence density were 6.6% (95% CI: 5.5–7.9) and 7.1 (95% CI: 5.4–9.2)/100 person-years, respectively. With pooled NAAT and individual NAAT strategy, the cost of an HIV transmission averted was $1,480. The addition of NAAT after HIV antibody tests had a cost-utility ratio of $3,366 per gained quality-adjusted life year (QALY). The input-output ratio of NAAT was about 1∶16.9.

Conclusions/Significance

The HIV infections among MSM continue to rise at alarming rates. Despite the rising cost, adding pooled NAAT to the HIV antibody screening significantly increases the identification of acute HIV infections in MSM. Early treatment and target-oriented publicity and education programs can be strengthened to decrease the risk of HIV transmission and to save medical resources in the long run.     

HIV-1 Transmission during Early Infection in Men Who Have Sex with Men: A Phylodynamic Analysis

Background

Conventional epidemiological surveillance of infectious diseases is focused on characterization of incident infections and estimation of the number of prevalent infections. Advances in methods for the analysis of the population-level genetic variation of viruses can potentially provide information about donors, not just recipients, of infection. Genetic sequences from many viruses are increasingly abundant, especially HIV, which is routinely sequenced for surveillance of drug resistance mutations. We conducted a phylodynamic analysis of HIV genetic sequence data and surveillance data from a US population of men who have sex with men (MSM) and estimated incidence and transmission rates by stage of infection.

Methods and Findings

We analyzed 662 HIV-1 subtype B sequences collected between October 14, 2004, and February 24, 2012, from MSM in the Detroit metropolitan area, Michigan. These sequences were cross-referenced with a database of 30,200 patients diagnosed with HIV infection in the state of Michigan, which includes clinical information that is informative about the recency of infection at the time of diagnosis. These data were analyzed using recently developed population genetic methods that have enabled the estimation of transmission rates from the population-level genetic diversity of the virus. We found that genetic data are highly informative about HIV donors in ways that standard surveillance data are not. Genetic data are especially informative about the stage of infection of donors at the point of transmission. We estimate that 44.7% (95% CI, 42.2%–46.4%) of transmissions occur during the first year of infection.

Conclusions

In this study, almost half of transmissions occurred within the first year of HIV infection in MSM. Our conclusions may be sensitive to un-modeled intra-host evolutionary dynamics, un-modeled sexual risk behavior, and uncertainty in the stage of infected hosts at the time of sampling. The intensity of transmission during early infection may have significance for public health interventions based on early treatment of newly diagnosed individuals. Please see later in the article for the Editors'' Summary     

Controlling HIV Epidemics among Injection Drug Users: Eight Years of Cross-Border HIV Prevention Interventions in Vietnam and China

Introduction

HIV in Vietnam and Southern China is driven by injection drug use. We have implemented HIV prevention interventions for IDUs since 2002–2003 in Lang Son and Ha Giang Provinces, Vietnam and Ning Ming County (Guangxi), China.

Methods

Interventions provide peer education and needle/syringe distribution. Evaluation employed serial cross-sectional surveys of IDUs 26 waves from 2002 to 2011, including interviews and HIV testing. Outcomes were HIV risk behaviors, HIV prevalence and incidence. HIV incidence estimation used two methods: 1) among new injectors from prevalence data; and 2) a capture enzyme immunoassay (BED testing) on all HIV+ samples.

Results

We found significant declines in drug-related risk behaviors and sharp reductions in HIV prevalence among IDUs (Lang Son from 46% to 23% [p<0.001], Ning Ming: from 17% to 11% [p = 0.003], and Ha Giang: from 51% to 18% [p<0.001]), reductions not experienced in other provinces without such interventions. There were significant declines in HIV incidence to low levels among new injectors through 36–48 months, then some rebound, particularly in Ning Ming, but BED-based estimates revealed significant reductions in incidence through 96 months.

Discussion

This is one of the longest studies of HIV prevention among IDUs in Asia. The rebound in incidence among new injectors may reflect sexual transmission. BED-based estimates may overstate incidence (because of false-recent results in patients with long-term infection or on ARV treatment) but adjustment for false-recent results and survey responses on duration of infection generally confirm BED-based incidence trends. Combined trends from the two estimation methods show sharp declines in incidence to low levels. The significant downward trends in all primary outcome measures indicate that the Cross-Border interventions played an important role in bringing HIV epidemics among IDUs under control. The Cross-Border project offers a model of HIV prevention for IDUs that should be considered for large-scale replication.     

The Impact of Human Mobility on HIV Transmission in Kenya

Disease spreads as a result of people moving and coming in contact with each other. Thus the mobility patterns of individuals are crucial in understanding disease dynamics. Here we study the impact of human mobility on HIV transmission in different parts of Kenya. We build an SIR metapopulation model that incorporates the different regions within the country. We parameterise the model using census data, HIV data and mobile phone data adopted to track human mobility. We found that movement between different regions appears to have a relatively small overall effect on the total increase in HIV cases in Kenya. However, the most important consequence of movement patterns was transmission of the disease from high infection to low prevalence areas. Mobility slightly increases HIV incidence rates in regions with initially low HIV prevalences and slightly decreases incidences in regions with initially high HIV prevalence. We discuss how regional HIV models could be used in public-health planning. This paper is a first attempt to model spread of HIV using mobile phone data, and we also discuss limitations to the approach.     

The use of operational modeling of HIV/AIDS in a systems approach to public health decision making.

Compartmental models of infectious diseases readily represent known biological and epidemiological processes, are easily understood in flow-chart form by administrators, are simple to adjust to new information, and lend themselves to routine statistical analysis such as parameter estimation and model fitting. Technical results are immediately interpretable in epidemiological and public health terms. Deterministic models are easily stochasticized where this is important for practical purposes. With HIV/AIDS, serial data on both HIV prevalence and AIDS morbidity have been available from San Francisco. Assuming the distribution of the incubation period to be biologically stable, statistical analysis is quite feasible in other regions, even those with no reliable HIV data. Transmission rates must be estimated locally. It is also often possible to estimate the effective size of a population subgroup at risk, from population data on AIDS morbidity only. Computer simulation provides estimates of the evolving pattern of both HIV prevalence and AIDS morbidity. Some public health questions can be answered only by appropriately formulated stochastic models.     

Measuring Population Transmission Risk for HIV: An Alternative Metric of Exposure Risk in Men Who Have Sex with Men (MSM) in the US

Background

Various metrics for HIV burden and treatment success [e.g. HIV prevalence, community viral load (CVL), population viral load (PVL), percent of HIV-positive persons with undetectable viral load] have important public health limitations for understanding disparities.

Methods and Findings

Using data from an ongoing HIV incidence cohort of black and white men who have sex with men (MSM), we propose a new metric to measure the prevalence of those at risk of transmitting HIV and illustrate its value. MSM with plasma VL>400 copies/mL were defined as having ‘transmission risk’. We calculated HIV prevalence, CVL, PVL, percent of HIV-positive with undetectable viral loads, and prevalence of plasma VL>400 copies/ml (%VL400) for black and white MSM. We used Monte Carlo simulation incorporating data on sexual mixing by race to estimate exposure of black and white HIV-negative MSM to a partner with transmission risk via unprotected anal intercourse (UAI). Of 709 MSM recruited, 42% (168/399) black and 14% (44/310) white MSM tested HIV-positive (p<.0001). No significant differences were seen in CVL, PVL, or percent of HIV positive with undetectable viral loads. The %VL400 was 25% (98/393) for black vs. 8% (25/310) for white MSM (p<.0001). Black MSM with 2 UAI partners were estimated to have 40% probability (95% CI: 35%, 45%) of having ≥1 UAI partner with transmission risk vs. 20% for white MSM (CI: 15%, 24%).

Discussion

Despite similarities in other metrics, black MSM in our cohort are three times as likely as white MSM to have HIV transmission risk. With comparable risk behaviors, HIV-negative black MSM have a substantially higher likelihood of encountering a UAI partner at risk of transmitting HIV. Our results support increasing HIV testing, linkage to care, and antiretroviral treatment of HIV-positive MSM to reduce prevalence of those with transmission risk, particularly for black MSM.     

Estimating incidence from prevalence in generalised HIV epidemics: methods and validation

Background

HIV surveillance of generalised epidemics in Africa primarily relies on prevalence at antenatal clinics, but estimates of incidence in the general population would be more useful. Repeated cross-sectional measures of HIV prevalence are now becoming available for general populations in many countries, and we aim to develop and validate methods that use these data to estimate HIV incidence.

Methods and Findings

Two methods were developed that decompose observed changes in prevalence between two serosurveys into the contributions of new infections and mortality. Method 1 uses cohort mortality rates, and method 2 uses information on survival after infection. The performance of these two methods was assessed using simulated data from a mathematical model and actual data from three community-based cohort studies in Africa. Comparison with simulated data indicated that these methods can accurately estimates incidence rates and changes in incidence in a variety of epidemic conditions. Method 1 is simple to implement but relies on locally appropriate mortality data, whilst method 2 can make use of the same survival distribution in a wide range of scenarios. The estimates from both methods are within the 95% confidence intervals of almost all actual measurements of HIV incidence in adults and young people, and the patterns of incidence over age are correctly captured.

Conclusions

It is possible to estimate incidence from cross-sectional prevalence data with sufficient accuracy to monitor the HIV epidemic. Although these methods will theoretically work in any context, we have able to test them only in southern and eastern Africa, where HIV epidemics are mature and generalised. The choice of method will depend on the local availability of HIV mortality data.     

Regression models for disease prevalence with diagnostic tests on pools of serum samples

Whether the aim is to diagnose individuals or estimate prevalence, many epidemiological studies have demonstrated the successful use of tests on pooled sera. These tests detect whether at least one sample in the pool is positive. Although originally designed to reduce diagnostic costs, testing pools also lowers false positive and negative rates in low prevalence settings and yields more precise prevalence estimates. Current methods are aimed at estimating the average population risk from diagnostic tests on pools. In this article, we extend the original class of risk estimators to adjust for covariates recorded on individual pool members. Maximum likelihood theory provides a flexible estimation method that handles different covariate values in the pool, different pool sizes, and errors in test results. In special cases, software for generalized linear models can be used. Pool design has a strong impact on precision and cost efficiency, with covariate-homogeneous pools carrying the largest amount of information. We perform joint pool and sample size calculations using information from individual contributors to the pool and show that a good design can severely reduce cost and yet increase precision. The methods are illustrated using data from a Kenyan surveillance study of HIV. Compared to individual testing, age-homogeneous, optimal-sized pools of average size seven reduce cost to 44% of the original price with virtually no loss in precision.     

Elevated risk for HIV infection among men who have sex with men in low- and middle-income countries 2000-2006: a systematic review

Background

Recent reports of high HIV infection rates among men who have sex with men (MSM) from Asia, Africa, Latin America, and the former Soviet Union (FSU) suggest high levels of HIV transmission among MSM in low- and middle-income countries. To investigate the global epidemic of HIV among MSM and the relationship of MSM outbreaks to general populations, we conducted a comprehensive review of HIV studies among MSM in low- and middle-income countries and performed a meta-analysis of reported MSM and reproductive-age adult HIV prevalence data.

Methods and Findings

A comprehensive review of the literature was conducted using systematic methodology. Data regarding HIV prevalence and total sample size was sequestered from each of the studies that met inclusion criteria and aggregate values for each country were calculated. Pooled odds ratio (OR) estimates were stratified by factors including HIV prevalence of the country, Joint United Nations Programme on HIV/AIDS (UNAIDS)–classified level of HIV epidemic, geographic region, and whether or not injection drug users (IDUs) played a significant role in given epidemic. Pooled ORs were stratified by prevalence level; very low-prevalence countries had an overall MSM OR of 58.4 (95% CI 56.3–60.6); low-prevalence countries, 14.4 (95% CI 13.8–14.9); and medium- to high-prevalence countries, 9.6 (95% CI 9.0–10.2). Significant differences in ORs for HIV infection among MSM in were seen when comparing low- and middle-income countries; low-income countries had an OR of 7.8 (95% CI 7.2–8.4), whereas middle-income countries had an OR of 23.4 (95% CI 22.8–24.0). Stratifying the pooled ORs by whether the country had a substantial component of IDU spread resulted in an OR of 12.8 (95% CI 12.3–13.4) in countries where IDU transmission was prevalent, and 24.4 (95% CI 23.7–25.2) where it was not. By region, the OR for MSM in the Americas was 33.3 (95% CI 32.3–34.2); 18.7 (95% CI 17.7–19.7) for Asia; 3.8 (95% CI 3.3–4.3) for Africa; and 1.3 (95% CI 1.1–1.6) for the low- and middle-income countries of Europe.

Conclusions

MSM have a markedly greater risk of being infected with HIV compared with general population samples from low- and middle-income countries in the Americas, Asia, and Africa. ORs for HIV infection in MSM are elevated across prevalence levels by country and decrease as general population prevalence increases, but remain 9-fold higher in medium–high prevalence settings. MSM from low- and middle-income countries are in urgent need of prevention and care, and appear to be both understudied and underserved.     

High Incidence Is Not High Exposure: What Proportion of Prevention Trial Participants Are Exposed to HIV?

Objective

Randomized clinical trials of HIV prevention in high-risk populations of women often assume that all participants have similar exposure to HIV. However, a substantial fraction of women enrolled in the trial may have no or low exposure to HIV. Our objective was to estimate the proportion of women exposed to HIV throughout a hypothetical high-risk study population.

Methods

A stochastic individual-based model was developed to simulate the sexual behavior and the risk of HIV acquisition for a cohort of sexually active HIV-uninfected women in high HIV prevalence settings. Key behavior and epidemic assumptions in the model were based on published studies on HIV transmission in South Africa. The prevalence of exposure, defined as the proportion of women who have sex with HIV-infected partner, and HIV incidence were evaluated.

Results

Our model projects that in communities with HIV incidence rate of 1 per 100 person years, only 5-6% of women are exposed to HIV annually while in communities with an HIV incidence of 5 per 100 person years 20-25% of women are exposed to HIV. Approximately 70% of the new infections are acquired from partners with asymptomatic HIV.

Conclusions

Mathematical models suggest that a high proportion of women enrolled in HIV prevention trials may be unexposed to HIV even when incidence rates are high. The relationship between HIV exposure and other risk factors should be carefully analyzed when future clinical trials are planned.     

Incidence of HIV in Windhoek, Namibia: demographic and socio-economic associations

Objective

To estimate HIV incidence and prevalence in Windhoek, Namibia and to analyze socio-economic factors related to HIV infection.

Method

In 2006/7, baseline surveys were performed with 1,753 private households living in the greater Windhoek area; follow-up visits took place in 2008 and 2009. Face-to-face socio-economic questionnaires were administrated by trained interviewers; biomedical markers were collected by nurses; GPS codes of household residences were recorded.

Results

The HIV prevalence in the population (aged>12 years) was 11.8% in 2006/7 and 14.6% in 2009. HIV incidence between 2007 and 2009 was 2.4 per 100 person year (95%CI = 1.9–2.9). HIV incidence and prevalence were higher in female populations. HIV incidence appeared non-associated with any socioeconomic factor, indicating universal risk for the population. For women a positive trend was found between low per-capita consumption and HIV acquisition. A HIV knowledge score was strongly associated with HIV incidence for both men and women. High HIV prevalence and incidence was concentrated in the north-western part of the city, an area with lower HIV knowledge, higher HIV risk perception and lower per-capita consumption.

Discussion

The HIV incidence and prevalence figures do not suggest a declining epidemic in Windhoek. Higher vulnerability of women is recorded, most likely related to economic dependency and increasing transactional sex in Namibia. The lack of relation between HIV incidence and socio-economic factors confirms HIV risks for the overall urban community. Appropriate knowledge is strongly associated to lower HIV incidence and prevalence, underscoring the importance of continuous information and education activities for prevention of infection. Geographical areas were identified that would require prioritized HIV campaigning.     

Rate Estimation from Prevalence Information on a Simple Epidemiologic Model for Health Interventions

Health intervention control programs, such as vaccination, can be evaluated by comparing incidence rates of infection between unprotected and protected individuals in a population. The ratio of incidence rates is usually estimated by following up control and treated groups in order to collect information on person-time and cases in each group. This approach can be expensive and time consuming. An alternative approach is to use prevalence data to reconstitute incidence. Current-status are readily available or easily gathered and can be used to estimate incidence rates. Under certain assumptions of irreversibility for the outcome of interest, we discuss a simple transmission model appropriate to evaluate health interventions that confer long term protection. Rates and populations are parameter-free functions of age and calendar time. We develop general mathematical relationships that link incidence and intervention rates to prevalence which could be estimated from sampling without requiring knowledge of subpopulation demographics.     

Biomarker-based HIV incidence in a community sample of men who have sex with men in Paris, France

BACKGROUND: Population-based estimates of HIV incidence in France have revealed that men who have sex with men (MSM) are the most affected population and contribute to nearly half of new infections each year. We sought to estimate HIV incidence among sexually active MSM in Paris gay community social venues. METHODOLOGY/ PRINCIPAL FINDINGS: A cross-sectional survey was conducted in 2009 in a sample of commercial venues such as bars, saunas and backrooms. We collected a behavioural questionnaire and blood sample. Specimens were tested for HIV infection and positive specimens then tested for recent infection by the enzyme immunoassay for recent HIV-1 infection (EIA-RI). We assessed the presence of antiretroviral therapy among infected individuals to rule out treated patients in the algorithm that determined recent infection. Biomarker-based cross-sectional incidence estimates were calculated. We enrolled 886 MSM participants among which 157 (18%) tested HIV positive. In positive individuals who knew they were infected, 75% of EIA-RI positive results were due to ART. Of 157 HIV positive specimens, 15 were deemed to be recently infected. The overall HIV incidence was estimated at 3.8% person-years (py) [95%CI: 1.5-6.2]. Although differences were not significant, incidence was estimated to be 3.5% py [0.1-6.1] in men having had a negative HIV test in previous year and 4.8% py [0.1-10.6] in men having had their last HIV test more than one year before the survey, or never tested. Incidence was estimated at 4.1% py [0-8.3] in men under 35 years and 2.5% py [0-5.4] in older men. CONCLUSIONS/ SIGNIFICANCE: This is the first community-based survey to estimate HIV incidence among MSM in France. It includes ART detection and reveals a high level of HIV transmission in sexually active individuals, despite a high uptake of HIV testing. These data call for effective prevention programs targeting MSM engaged in high-risk behaviours.     

Human giardiasis in Serbia: asymptomatic vs symptomatic infection

Despite the public health importance of giardiasis in all of Europe, reliable data on the incidence and prevalence in Western Balkan Countries (Serbia, Bosnia and Herzegovina, Croatia, Montenegro and FYR Macedonia) are scarce, and the relative contribution of waterborne and food-borne, or person-to-person and/or animal-to-person, transmission of human giardiasis is not yet clear. To provide baseline data for the estimation of the public health risk caused by Giardia, we here review the information available on the epidemiological characteristics of asymptomatic and symptomatic human infection in Serbia. Although asymptomatic cases of Giardia represent a major proportion of the total cases of infection, high rates of Giardia infection were found in both asymptomatic and symptomatic populations. No waterborne outbreaks of giardiasis have been reported, and it thus seems that giardiasis mostly occurs sporadically in our milieu. Under such circumstances, control measures to reduce the high prevalence of giardiasis in Serbia have focused on person-to-person transmission, encouraging proper hygiene, but for more targeted intervention measures, studies to identify other risk factors for asymptomatic and symptomatic infections are needed.     

A non-parametric method for the reconstruction of age- and time-dependent incidence from the prevalence data of irreversible diseases with differential mortality.

A method is proposed for reconstructing the time and age dependence of incidence rates from successive age-prevalence cross sections taken from the sentinel surveys of irreversible diseases when there is an important difference in mortality between the infected and susceptible subpopulations. The prevalence information at different time-age points is used to generate a surface; the time-age variations along the life line profiles of this surface and the difference in mortality rates are used to reconstruct the time and age dependence of the incidence rate. Past attempts were based on specified parametric forms for the incidence or on the hypothesis of time-invariant forms for the age-prevalence cross sections. The proposed method makes no such assumptions and is thus capable of coping with rapidly evolving prevalence situations. In the simulations carried out, it is found to be resilient to important random noise components added to a prescribed incidence rate input. The method is also tested on a real data set of successive HIV age-prevalence cross sections from Burundi coupled to differential mortality data on HIV(+) and HIV(-) individuals. The often-made assumption that the incidence rate can be written as the product of a calendar time component and an age component is also examined. In this case, a pooling procedure is proposed to estimate the time and the age profiles of the incidence rate using the reconstructed incidence rates at all time-age points.     

Analysis of multistage pooling studies of biological specimens for estimating disease incidence and prevalence

The testing of pooled samples of biological specimens for the purpose of estimating disease prevalence may be more cost effective than testing individual samples, particularly if the prevalence of disease is low. Multistage pooling studies involve testing pools and then sequentially subdividing and testing the positive pools. A simple estimator of disease prevalence and its variance are derived for general multistage pooling studies and are shown to be natural generalizations of Thompson's (1962) original estimators for single-stage pooling studies. The reduction in variance associated with each additional stage is calibrated. The results are extended to estimating disease incidence rates. The methods are used to estimate HIV incidence rates from a prevalence study of early HIV infection using a PCR assay for HIV RNA.     

A Decline in New HIV Infections in South Africa: Estimating HIV Incidence from Three National HIV Surveys in 2002, 2005 and 2008

Background

Three national HIV household surveys were conducted in South Africa, in 2002, 2005 and 2008. A novelty of the 2008 survey was the addition of serological testing to ascertain antiretroviral treatment (ART) use.

Methods and Principal Findings

We used a validated mathematical method to estimate the rate of new HIV infections (HIV incidence) in South Africa using nationally representative HIV prevalence data collected in 2002, 2005 and 2008. The observed HIV prevalence levels in 2008 were adjusted for the effect of antiretroviral treatment on survival. The estimated “excess” HIV prevalence due to ART in 2008 was highest among women 25 years and older and among men 30 years and older. In the period 2002–2005, the HIV incidence rate among men and women aged 15–49 years was estimated to be 2.0 new infections each year per 100 susceptible individuals (/100pyar) (uncertainty range: 1.2–3.0/100pyar). The highest incidence rate was among 15–24 year-old women, at 5.5/100pyar (4.5–6.5). In the period 2005–2008, incidence among men and women aged 15–49 was estimated to be 1.3/100 (0.6–2.5/100pyar), although the change from 2002–2005 was not statistically significant. However, the incidence rate among young women aged 15–24 declined by 60% in the same period, to 2.2/100pyar, and this change was statistically significant. There is evidence from the surveys of significant increases in condom use and awareness of HIV status, especially among youth.

Conclusions

Our analysis demonstrates how serial measures of HIV prevalence obtained in population-based surveys can be used to estimate national HIV incidence rates. We also show the need to determine the impact of ART on observed HIV prevalence levels. The estimation of HIV incidence and ART exposure is crucial to disentangle the concurrent impact of prevention and treatment programs on HIV prevalence.     

BED estimates of HIV incidence: resolving the differences, making things simpler

Objective

Develop a simple method for optimal estimation of HIV incidence using the BED capture enzyme immunoassay.

Design

Use existing BED data to estimate mean recency duration, false recency rates and HIV incidence with reference to a fixed time period, T.

Methods

Compare BED and cohort estimates of incidence referring to identical time frames. Generalize this approach to suggest a method for estimating HIV incidence from any cross-sectional survey.

Results

Follow-up and BED analyses of the same, initially HIV negative, cases followed over the same set time period T, produce estimates of the same HIV incidence, permitting the estimation of the BED mean recency period for cases who have been HIV positive for less than T. Follow-up of HIV positive cases over T, similarly, provides estimates of the false-recent rate appropriate for T. Knowledge of these two parameters for a given population allows the estimation of HIV incidence during T by applying the BED method to samples from cross-sectional surveys. An algorithm is derived for providing these estimates, adjusted for the false-recent rate. The resulting estimator is identical to one derived independently using a more formal mathematical analysis. Adjustments improve the accuracy of HIV incidence estimates. Negative incidence estimates result from the use of inappropriate estimates of the false-recent rate and/or from sampling error, not from any error in the adjustment procedure.

Conclusions

Referring all estimates of mean recency periods, false-recent rates and incidence estimates to a fixed period T simplifies estimation procedures and allows the development of a consistent method for producing adjusted estimates of HIV incidence of improved accuracy. Unadjusted BED estimates of incidence, based on life-time recency periods, would be both extremely difficult to produce and of doubtful value.     

Risk Denial and Socio-Economic Factors Related to High HIV Transmission in a Fishing Community in Rakai,Uganda: A Qualitative Study

Background

In Kasensero fishing community, home of the first recorded case of HIV in Uganda, HIV transmission is still very high with an incidence of 4.3 and 3.1 per 100 person-years in women and men, respectively, and an HIV prevalence of 44%, reaching up to 74% among female sex workers. We explored drivers for the high HIV transmission at Kasensero from the perspective of fishermen and other community members to inform future policy and preventive interventions.

Methods

20 in-depth interviews including both HIV positive and HIV negative respondents, and 12 focus-group discussions involving a total of 92 respondents from the Kasensero fishing community were conducted during April-September 2014. Content analysis was performed to identify recurrent themes.

Results

The socio-economic risk factors for high HIV transmission in Kasensero fishing community cited were multiple and cross-cutting and categorized into the following themes: power of money, risk denial, environmental triggers and a predisposing lifestyle and alcoholism and drug abuse. Others were: peer pressure, poor housing and the search for financial support for both the men and women which made them vulnerable to HIV exposure and or risk behavior.

Conclusions

There is a need for context specific combination prevention interventions in Kasensero that includes the fisher folk and other influential community leaders. Such groups could be empowered with the knowledge and social mobilization skills to fight the negative and risky behaviors, perceptions, beliefs, misconceptions and submission attitudes to fate that exposes the community to high HIV transmission. There is also need for government/partners to ensure effective policy implementation, life jackets for all fishermen, improve the poor housing at the community so as to reduce overcrowding and other housing related predispositions to high HIV rates at the community. Work place AIDS-competence teams have been successfully used to address high HIV transmission in similar settings.     

The HIV epidemic among men who have sex with men—behaviour beats science

More than three decades after the emergence of HIV/AIDS, more than 30 million people worldwide still live with the disease. In the West, those most at risk are men who have sex with men owing to a combination of social factors and, ironically, improved healthcare.The acquired immune deficiency syndrome (AIDS) pandemic that started more than 30 years ago remains one of the greatest public-health concerns worldwide: in 2009, it was estimated that 33.3 million individuals were infected with human immunodeficiency virus (HIV), with 2.6 million new infections globally (see graphic; [1]). Even in the affluent countries of North America, Australia, New Zealand and Western and Central Europe, the numbers of people infected with HIV have grown over the past two decades. Although the availability of efficient diagnostics and highly active antiretroviral therapy (HAART) have drastically improved life expectancy and quality of life—at least in those parts of the world where both are available and affordable—HAART does not cure the disease. Moreover, despite massive research efforts, there is no efficient vaccine on the market to protect against infection with HIV.Given the lack of either a vaccine or a cure, the main public-health intervention to halt the pandemic is to prevent viral transmission in the first placeGiven the lack of either a vaccine or a cure, the main public-health intervention to halt the pandemic is to prevent viral transmission in the first place. In fact, the transmission of HIV is not as efficient as other, more resistant blood-borne viruses such as hepatitis B and hepatitis C viruses (HBV and HCV), and it requires direct contact of blood or semen from an infected person with the blood system of the exposed person. This feature puts certain groups at greater risk of transmission: heterosexuals with many sexual partners, including sex workers, men who have sex with men (MSM—a technical term used by health professionals to avoid forcing individuals to define themselves in a specific sexuality), people who inject drugs, newborns of HIV-infected mothers, blood recipients and healthcare workers. Yet, the risk of infection differs for each of these groups. There is also a geographical dimension to the risk, as different parts of the world have unique epidemiological characteristics, reflecting biological, behavioural and socio-economic factors. In many parts of Africa and Asia, for example, the most susceptible groups are heterosexuals and sex workers; in Eastern Europe, people who inject drugs are mainly affected; and in western countries, the most vulnerable population are MSM, followed by heterosexual migrants from areas where HIV is endemic [2].

Science & Society Series on Sex and Science

Sex is the greatest invention of all time: not only has sexual reproduction facilitated the evolution of higher life forms, it has had a profound influence on human history, culture and society. This series explores our attempts to understand the influence of sex in the natural world, and the biological, medical and cultural aspects of sexual reproduction, gender and sexual pleasure.Public-health programmes intended to prevent the transmission of HIV therefore have to address these groups individually. Such measures require education and the involvement of at-risk populations, and recommendations must be based on a thorough understanding of the social, economic and other factors that determine disease risk among certain groups of people. For instance, one of the most efficient measures to decrease the risk of HIV infection among people who inject drugs is to offer clean syringes and needles,and safe places to use them. One of the most efficient ways to prevent HIV transmission during sexual intercourse is the use of condoms. But, the answers are not always as simple; human behaviour is complex and even irrational at times. This paper outlines the main causes of the HIV epidemic among MSM in western countries, highlights specific behavioural factors that increase exposure to HIV and discusses how these can be addressed in public-health programmes.AIDS was first identified and described in the USA in June 1981 [3]. Following reports from Los Angeles and New York City about clusters of otherwise healthy Caucasian MSM who developed Kaposi''s sarcoma and fatal Pneumocystis carinii (jirovecii) pneumonia, the US Centers for Disease Control and Prevention (CDC) conducted an epidemiological investigation and identified a man they referred to as ‘patient zero'': a flight attendant working for Air Canada named Gaëtan Dugas, who had numerous male sexual partners in North America. Dugas might not have been the first person who was infected with HIV, but the first one who was identified with the disease.​disease.Open in a separate windowSee full size illustration: http://staging-www.nature.com/embor/journal/v13/n11/full/embor2012152i1.htmlIt was a combination of a general liberal attitude towards sex that was prevalent among MSM, unprotected anal sex and having multiple sexual partners that allowed HIV to spread quickly among the gay community in the early 1980s. Owing to the overwhelming impact on MSM in the early years of the AIDS epidemic—when many MSM saw close friends, partners and lovers die—gay communities adopted a range of practices to reduce the risk of infection successfully by changing sexual behaviours. Regretfully, these achievements did not last; many other developed countries also recorded a resurgence in the number of MSM newly diagnosed with HIV/AIDS since the mid-1990s [4]. The main reason for the re-emergence of the disease was the come-back of risky sexual behaviours, triggered by wider social and cultural changes, greater social acceptance for gay men and, somehow unpredictably, the introduction of more efficient drugs [5].The most important risk factor for exposure to HIV among MSM remains sexual practices. As the rectal mucosa is more fragile than the vaginal or oral, anal sex increases the risk for transmitting HIV and other sexually transmitted infections (STIs). The frequency of risky sexual practices between MSM seems to be increasing [6], which would go some way to explaining the resurgence of AIDS.Another main factor for the resurgence of AIDS among the gay communities in western countries is, ironically, the efficiency of HAARTIn addition, gay communities have a relatively liberal attitude towards sex and partnership. The way they form partnerships may differ from many heterosexuals: the sexual contact is more instantaneous and spontaneous, and sexual intercourse may take place early in a relationship [7]. Relationships between some MSM may be more flexible, and concurrent sex with casual partners during a relationship is generally more tolerable [8,9]. Concomitancy and age-mixing of sexual partners has a strong influence on the dynamic of HIV transmission if an infected man is unaware of his infection owing to the asymptomatic nature during the first years of HIV infection, or because he has not been tested for HIV [10]. Early sexual debut is another reason for greater exposure to HIV, as MSM would have more partners during their lifetime.Social changes have also played a role in increasing the HIV transmission rate among MSM. Since the 1990s, homosexuality and gay lifestyle have become much more accepted in many western societies. This increasing tolerance and acceptance has enabled many MSM ‘to get out of the closet'', that is to disclose their sexual orientation and have fulfilling lives. It has also encouraged entrepreneurs to tap into this customer base by offering services and establishments specifically for MSM including cafés, bars, clubs, restaurants, hotels and bath houses, all specifically intended for the purpose of meeting other men. This sexually liberal climate, along with the venues to meet other gay men, has amplified the risk of having sex with an HIV-infected partner.Similarly, the rise of internet-dating sites has increased the ease with which new partners can be found. New sexual practices and behavioural norms are quickly diffused between cultures, with possible international importing of HIV and other STIs. The internet, which is affordable, immediate and discrete, has become the most popular way of searching for other MSM. Most gay-related internet sites are free and guarantee anonymity until participants find the preferred fit and disclose their personal details or picture. The discrete nature of the web also allows MSM who are still ‘in the closet'' or ‘on the down low'' to search for sexual partners. This electronic meeting place might modify the sexual risk, as it exposes users to a diverse pool of men and increases their ability to search and negotiate for sexual practices [11]. The anonymity also allows MSM to search explicitly for unprotected anal sex [12]. MSM who originate from low-resource countries and migrate to developed countries might not be familiar with the risk of unprotected sex and may also be excited about the sizeable and versatile MSM community in the hosting country [12]. A combination of insufficient knowledge about HIV/AIDS, coupled with their interest in experiencing gay life, may increase the risk for those migrants to become infected with HIV.…the chances that an HIV-negative MSM finds himself engaged in sexual contact with an HIV-infected partner are higher than 15 years agoCorresponding with the increased number of sexual partners and the greater risk during sexual intercourse, MSM are also exposed to other STIs, especially if they are already infected with HIV. Increasing incidence of syphilis, as well as outbreaks of primary and secondary syphilis among MSM, has been reported during the past decade from developed countries [13,14]. Primary syphilis might manifest in a ‘chancer''—a sore—which is a possible port of entry for HIV. Additionally, the immunological reaction to STIs includes the migration of macrophages and lymphocytes to the affected organs. These cells are also the target of HIV, and thus one STI increases the chances of infection with further STIs or HIV. Over the past years, several outbreaks of lymphogranuloma venereum (an uncommon STI), presenting proctitis (inflammation of the rectum), and genital ulcers with inguinal adenopathy (inflammation of the lymph nodes in the groin) have been reported [15]. The asymptomatic nature of some STIs, along with the limited success of the risk-reduction strategies practiced by MSM, might explain the increased incidence of STIs among gay men [16,17]. Among HIV-infected individuals, genital infections with common STI pathogens have been associated with increased HIV viral load in semen, thus negating the benefit of HAART [18].Another important factor for the resurgence of AIDS among the gay communities in western countries is, ironically, the efficiency of HAART, which has converted AIDS from a death sentence into a manageable chronic medical condition. As the perceived threat of HIV/AIDS diminishes and direct experience with death disappears, some MSM may be more inclined to take higher risks. Before the introduction of HAART in the mid-1990s, most MSM had direct experience of the devastating effects of HIV/AIDS on friends and loved ones. It is important to note that HAART reduces the viral load in HIV-infected persons to undetectable levels in the blood and thereby decreases the risk of infecting partners. However, studies have documented the persistence of HIV virions and infected cells in semen of HIV-infected MSM treated with HAART [19]. Most physicians, therefore, do not recommend unprotected sex for HAART-treated HIV/AIDS patients, although the risk of HIV transmission has been significantly reduced.…public-health measures to reduce the prevalence of HIV among MSM should focus on the behavioural and psychosocial factors that increase the risk of infectionAs such, HAART has profoundly changed the impact of HIV/AIDS: people who live with HIV/AIDS who adhere to their drug regimen are usually asymptomatic and seem healthy. The non-fatal prognosis for AIDS, the large communities of HIV-infected MSM who live apparently healthy lives and the greater social acceptability of the disease have together reduced the perceived threat of HIV/AIDS.The success of HAART has affected sexual behaviour, a phenomenon called ‘AIDS optimism''. First, as HIV-infected MSM feel healthy and their sex-drive is preserved, they have a normal sex life and seek sexual partners, similarly to HIV-negative MSM. Second, before HAART and during its introduction in the 1990s, people living with HIV/AIDS could be recognized either by their cachectic posture or by the lipodystrophic features of their cheekbones and limbs due to loss of subdermal fat—a side-effect of the first generation of protease inhibitors. HIV-negative MSM could therefore decline sexual contact or insist on safer sex practices. However, modern HAART has diminished side-effects and HIV-infected men are usually unrecognizable. MSM may wrongly consider their sexual partners to be HIV-negative and might have unprotected sex. Third, some MSM may be aware of the availability of post-exposure prophylaxis as an additional use of ART, and might have unprotected sex then request the treatment, which is available up to 72 hours after sex [20]. These men may not be aware that post-exposure treatment has not been proven to be efficient in humans in randomized clinical trials. Finally, young MSM, who have not witnessed the devastation of AIDS, may no longer feel threatened by the disease and might engage in unprotected sex. The advanced manageability of HIV, as portrayed in the media and advertisements sponsored by the pharmaceutical industry, may further disinhibit their sexual behaviour.Moreover, the success of HAART and decades of public-health recommendations to practice safe sex may have led to ‘AIDS fatigue''. Some MSM may become desensitized to safe-sex messages and might develop a negative emotional response to HIV issues. As the number of newly diagnosed HIV-positive MSM is increasing, some will also remain unaware of their infection and may ignore safe-sex practices. Thus, the chances that an HIV-negative MSM finds himself engaged in sexual contact with an HIV-infected partner are higher than 15 years ago. Some public-health professionals argue that the uptake of HIV tests among MSM has more to do with the increased acceptance of their lifestyle than an increasing infection rate; thus the high HIV rates recorded are no more than epidemiological fallacy. However, even if this assumption is true, it neither explains the rapid dynamic of HIV transmission among MSM communities, nor the increased syphilis infection rates. Additionally, ART-resistant strains of HIV have emerged, which complicates treatment and prolongs the transmission period. The prevalence of primary or transmitted drug-resistant HIV strains in North America and Western Europe is as high as 26% [21].…it crucially requires the involvement and engagement of the gay community themselves to maintain effective and acceptable interventionsDrug abuse is another relevant risk factor. Even if the percentage of intravenous drug users among MSM may not differ compared with the percentage among heterosexuals, it creates a twofold risk of acquiring HIV: by blood-to-blood transmission when sharing needles and syringes, and by semen-to-blood exposure when having sex. Some males who inject drugs may also engage in sex with other males, although they are heterosexuals, to finance their addiction.MSM are generally aware of their risk of acquiring HIV and of the importance of condom use. Yet, they have developed alternative strategies to prevent possible HIV exposure that involve evaluating their partners and the environment in which they meet more carefully, and then taking calculated risks [22]. One such strategy used is called ‘negotiated safety'', in which both men disclose to each other their HIV status before they have sexual intercourse and may decide to perform unprotected anal sex if they are both negative. The efficacy of this strategy depends on the time at which they were tested, their honesty and being safe if performing sex outside the primary sexual relationship. The second strategy is ‘sero-sorting'', when MSM restrict unprotected anal intercourse only to partners they believe to be concordant [23]. MSM negotiate and try to identify signs that might indicate that a partner could be HIV-positive, such as special physical features—being cachectic or lypodystrophic—the venue and context in which they meet, and when visiting the home of a partner, taking a quick look in their drawers or in the bathroom closet to search for HAART tablets (‘sero-guessing''). Another strategy is called ‘strategic positioning'', which is the use of sero-status to determine sexual roles in which MSM may perform only oral sex or take the active role in anal sex. However, these risk reduction strategies, widely used by MSM, offer only limited protection from HIV [24].The recommended use of condoms during anal sex can fall by the wayside after recreational drug use. Drugs such as alcohol and methamphetamine, which are commonly used at clubs, discos and other venues, lower social barriers and increase sociability. MSM using such drugs are therefore more inclined to have sex with an unknown partner and might not use a condom, as their judgment is impaired. This risky combination of drug use during sexual contact is called ‘party and play'' on internet sites for MSM who are searching for a partner [25].The result is that in the post-HAART era, MSM still remain the group most at risk of acquiring HIV, with substantial evidence for continuing HIV transmission. It has been estimated that more than 40% of HIV-positive young MSM are involved in risky sexual behaviour, despite their awareness of their infection [26,27]. Behavioural, emotional, psychological, environmental and epidemiological factors all act synergistically to increase risk-taking when it comes to sexual practices, thus exacerbating HIV incidence in MSM. These factors might be even more dominant among HIV-positive MSM, driving them to perform unprotected anal sex. They face specific psychosocial factors such as the need to be loved and cared for, a different meaning of sex as an emotional connection and a decreased desire for intimacy after their diagnosis, owing to mixed feelings of shame and guilt [24].By contrast, HIV-infected MSM who receive HAART and achieve undetectable viral load in their blood usually reduce the risk of transmitting the virus to their sexual contacts, and probably engage less in risky sexual behaviour than those who are not on ART [28]. One explanation is that they frequent HIV clinics more often and are therefore more aware of the need to use condoms, and receive positive self-care advice. Some studies have shown that many HIV-positive men are also engaged in both sero-sorting and strategic positioning, probably to avoid HIV transmission to members of their social and sexual networks [29].…the success of HAART and decades of public-health recommendations to practice safe sex might have led to ‘AIDS fatigue''Some HIV-infected MSM therefore prefer to contact sero-concordant HIV-positive partners to experience unprotected anal intercourse, free from the worry of infecting a negative partner, or the embarrassment of having to disclose their HIV status to a negative partner, exposing themselves to the stigma attached to HIV. These perceived benefits seem to outweigh the perceived risks of contracting another strain of HIV, potentially drug-resistant, or STIs.Lacking an efficient vaccine or cure for AIDS, public-health measures to reduce the prevalence of HIV among MSM should focus on the behavioural and psychosocial factors that increase the risk of infection. Effectively, this means educational and outreach campaigns to address risky sexual behaviour and to promote the use of condoms and other protective strategies. These interventions should involve all relevant parties: non-governmental and governmental organizations, health providers, public-health experts and gay-related agencies. The message about the continuing risks and dangers of HIV/AIDS should go through multiple routes to address as many men as possible through the internet, media, clubs, bars and public spaces, to reinforce consistent condom use and other risk-reduction strategies, and to promote early diagnosis and treatment.Such campaigns should address both HIV-negative and HIV-positive men, but with a different focus on the needs of each. HIV-negative MSM should be informed about the possible routes of HIV transmission, the importance of using condoms, improving negotiation skills and other risk-reduction strategies to protect themselves and their partners. Innovative interventions could also attempt to associate the strong motivation of MSM for masculinity with the use of condoms. Additionally, frequent HIV testing in MSM-friendly clinics and community settings should be encouraged to detect new infections as early as possible. HIV-infected MSM should be instructed with safe-sex recommendations and prescribed HAART to reduce seminal viral load. Intervention in this group should address the unique psychological, social and medical status of each patient. As pointed out above, it crucially requires the involvement and engagement of the gay community themselves to maintain effective and acceptable interventions.Health educators must also respect the needs, wishes and behaviour of MSM when addressing them about the risk of HIV/AIDS, and making recommendations about safe-sex practices. Although condoms are indeed efficient at preventing HIV transmission, they might nonetheless be the ‘incorrect'' instrument in the ‘wrong'' place for many people. Condom use breaks the intimacy and spontaneity of sex and reduces the pleasure. Although we hope that we can convince a young, HIV-positive MSM to use condoms, this might not be a realistic goal. As such, addressing the risks requires a sensitive, ‘down-to-earth'' approach that respects gay culture and the dynamic of finding partners, as well as training physicians to provide counselling for MSM in a friendly and confident way.Reducing the use of illicit drugs in both HIV-infected and uninfected MSM is another priority, although in some cases drugs are used to cope with the stress related to living with HIV. Appropriate interventions for HIV-infected MSM must therefore include stress-reduction techniques, psychological services and counselling about the negative effects of substance use. Another public-health priority is to promote the disclosure of HIV status as part of the ethics related to using gay-dating sites. As the perceived threat of HIV has diminished owing to the success of ART and the non-fatal medical prognosis of HIV/AIDS, noticeable messages should be more positive and reflect contemporary gay life, using gay-related and non-gay-related venues frequented by MSM, such as gyms, airports, shops or tourist resorts.To address the problem and slow or halt the pandemic requires focused, evidence-based measures that respect biological, emotional and social aspects in a holistic approach…In conclusion, HIV prevalence among MSM remains high and, given the increase in survival of HIV-infected individuals and the high rate of new infections, this hyper-endemic state is likely to be sustained in developed countries [14]. To address the problem and slow or halt the pandemic requires focused, evidence-based measures that respect biological, emotional and social aspects in a holistic approach [24], taking into account psychological stressors, drug habits, discrimination and the quest for intimacy. It is also important to increase the sensitivity of health providers towards the special needs of MSM, to conduct open and non-judgemental discussions with their patients. A supportive medical environment can encourage MSM to adhere to periodical HIV testing, HBV and hepatitis A virus immunizations and, possibly, to comply with condom use [19]. Finally, due to the similarities in MSM behaviours in industrialized countries, a closer collaboration is required between researchers from countries that have large MSM communities. We are entering the fourth decade of the AIDS epidemic, and despite awareness among MSM of their greater vulnerability to HIV and the introduction of new medical interventions, the rate of new infections continues to rise disproportionately. It is time for new interventions.? Open in a separate windowZohar MorOpen in a separate windowMichael Dan