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Original Studies

Scaling Up Human Immunodeficiency Virus Screening and Antiretroviral Therapy Among Men Who Have Sex With Men to Achieve the 90-90-90 Targets in China

Zhuang, Xun PhD*; Peng, Peng MPH*; Sun, Huamin MPH; Chu, Minjie PhD*; Jiang, Shengyang PhD*; Jiang, Liying PhD*; Zhou, Pingyu PhD; Zhu, Bowen MPH*; Zhang, Lei PhD*§¶∥

Author Information
Sexually Transmitted Diseases: May 2018 - Volume 45 - Issue 5 - p 343-349
doi: 10.1097/OLQ.0000000000000744

The spread of human immunodeficiency virus (HIV) remains a global threat over the past three decades. The World Health Organization (WHO) estimated that a total of 36.7 million people are living with HIV (PLHIV)/acquired immune deficiency syndrome (AIDS) in 2015.1 In China, the reported total number of PLHIV, not including these undiagnosed, is 577, 423 in 2015 and HIV is spreading rapidly among men who have sex with men (MSM). The estimated population size of Chinese MSM is 5 to 10 million, and the HIV prevalence among them has substantially increased from 1.8% in 2000 to 8.0% in 2015 nationally.2,3 Among new HIV diagnoses in 2015, homosexual transmission accounted for 28.3%.4 The increasingly rampant HIV epidemic among MSM is closely related to their risky sexual behaviors. Multiple concurrent partnerships are common, and condom usage is low.5,6 Bisexual relationship with women are also prevalent because 17% to 50% MSM are currently in marriage and 86% have had female sex partners in lifetime. The HIV prevention and treatment in MSM is a priority for HIV control in China.7–9

To end AIDS by 2030, ambitious targets were put forward by The Joint United Nations Programme on HIV and AIDS (UNAIDS) in 2014. These aimed to achieve “90-90-90” targets by 2020, by enabling 90% of PLHIV aware of their infection status, 90% diagnosed individuals receive antiretroviral therapy (ART), and 90% of all people receiving ART sustained viral suppression. By the end 2016, only Botswana, Denmark, Italy, Netherlands, Sweden, and the United Kingdom had achieved these targets,10 although more are expected to reach the mark in the coming years. The Chinese government has enacted firm health policies in response to the 90-90-90 targets. In 2012, the state council issued “the 12th five-year plan on AIDS prevention and treatment,”11 which prioritized “scaling up HIV monitoring” and “ART and by improving treatment coverage and accessibility” as key HIV interventions. This remains a long way to the 90-90-90 targets. As a key risk population for HIV, reducing HIV disease burden among MSM is essential for reducing the overall HIV epidemic in China to achieve the UNAIDS targets.

Many preventive measures are effective for HIV control. For example, condom promotion, preexposure prophylaxis, and circumcision are effective in preventing new HIV infections, but do not add to the treatment coverage.5,12 In comparison, “test-and-treat,” which means expansion of HIV screening and immediate ART initiation for those diagnosed, is a key strategy for the continuum of HIV care and treatment. Timely diagnosis and treatment for PLHIV significantly prolong life expectancy of PLHIV, reduce AIDS-associated deaths, and the risk of further HIV transmission by lowering the viral load in PLHIV.13 Viral load testing that is routinely offered to patients on ART can diagnose drug resistances early and allow drug-resistant patients to switch to higher line of ART. A mathematical model forecasted a 41% reduction in HIV incidence in San Francisco MSM in 5 years if all people living with HIV MSM receive timely ART.14

Mathematic models are a useful tool to forecast an epidemic trend and evaluate the effectiveness and cost-effectiveness of interventions, which provide important evidence for government policies and long-term strategies.15 A South African study suggested that by testing all people in the test-case community and start on ART immediately for 5 years, it will reduce HIV incidence and mortality to less than 1 case per 1000 people per year.16 Another model on MSM in the United States showed that a universal coverage of HIV screening and initiating ART at diagnosis would reduce new HIV infections for 20 years by 70%.17 An economic evaluation of HIV voluntary counseling and testing for MSM in China is highly cost-effective because it costs only US $184 to avert 1 disability-adjusted life years (DALY).18 In Bangkok, Thailand, a study indicated that an additional US $55.3 million investment would link an extra 46,700 MSM to HIV testing and 12,600 to ART, achieving universal ART coverage of this population by 2022, there would be an estimated 53% reduction in deaths and 35% reduction in HIV new infections from 2012 levels, and the expansion would cost $351 to avert 1 DALY.19 In China, the investment in HIV care and treatment for MSM remain inadequate. The current resources allocated for HIV prevention in MSM do not align with the rapidly increasing HIV disease burden in the population.20 This study, based on a deterministic compartmental model, forecasts the HIV epidemic in Chinese MSM over the next decade and examines the required additional investment to achieve the 90-90-90 targets by 2020, as proposed by UNAIDS, and an alternative delay to 2025. In both scenarios, we evaluate the population impacts and cost-effectiveness of the “test-and-treat” strategy.

METHODS

Data Source

We collected various parameters, including demographic and behavioristics, biological, epidemiological and economical health evaluation-associated parameters and economical health evaluation-associated parameters from published literatures, government reports, sentinel surveillance reports, and international organization websites (WHO, UNAIDS) for the mathematical model. The demographic and behavioral parameters included the number of Chinese MSM and those becoming MSM each year, the number of homosexual partners and number of sexual acts per partner per year, the possibility of HIV transmission in per anal intercourse, and the usage and effectiveness of condom. The biological parameters included the rate from each disease stage to the next and the death rate in each stage. We collected the epidemiological parameters including HIV prevalence, number of newly diagnosed, newly infectious, HIV-related death, newly initiating ART and the total number of MSM on ART, the parameters for economic evaluation including the cost of HIV testing, ART, and viral load tests. For indicators with multiple data points, we included the best point estimate and an uncertainty range, whereas for data points with a single value, we assumed ±25% as the uncertainty range (Table S1–3, https://links.lww.com/OLQ/A207).

Model Structure

We constructed a compartmental model based on a system of differential equations that describe the HIV epidemic among Chinese MSM (Figure S1, https://links.lww.com/OLQ/A207). We simulated 6 disease progression stages: (1) susceptible, (2) infected but undiagnosed, (3) diagnosed but untreated, (4) on first-line treatment, (5) treatment failure, and (6) on second-line treatment. Men who have sex with men who are people living with HIV were further stratified to 5 CD4 categories, resulting in a total of 31 compartments representing 31 health status, respectively. We simulated disease progression with the following parameters: (1) from undiagnosed to diagnosed (η1–6), which depends on HIV screening and MSM population size; (2) diagnosed and receiving first-line ART treatment (σ11–16); (3) first-line or second-line treatment failure (ωtf11-tf16; ωtf21-tf26); (4) switch to second-line treatment after 1st-line treatment failure (σ21–26); (5) CD4 count declined in untreated patients (from CD4 > 500 to CD4 < 50, τμ1-μ5, τd1-d5, τtf1-tf5); (6) CD4 count increased in patients on treatment (τt15-t11, τt25-t21); (7) death, including background mortality (μ) and HIV/AIDS-associated deaths (μμ1-μ6, μd1-d6, μt11-t16, μtf1-f6, μt21-t26). The completed HIV epidemic model structure is illustrated in Figure S1, https://links.lww.com/OLQ/A207.

Probability of HIV Acquisition in MSM

We estimated the probability of HIV acquisition based on the assumption that most HIV transmitted among MSM was due to unprotected anal intercourse. It depended on the infectiousness of HIV-positive MSM, which means the average number of MSM who may be infected by an HIV-positive MSM annually. The probability was a function of the numbers of homosexual partners, average times of anal sex behaviors, the usage frequency, and the effectiveness of condoms. Because of the effective HIV infection control with condoms, we considered the probability of HIV acquisition with and without condoms, respectively. The complete expression for the probability of HIV acquisition was:

where β is the possibility of HIV transmission in per anal intercourse, Na is the number of anal sexual intercourses per partnership in the past 12 months, Np is the number of homosexual partners in the past 12 months, Pc is the usage rate of condom in last anal intercourse, ε is the effectiveness of condom. P(t) is the proportion of MSM living with HIV without ART to the whole MSM population.

Model Calibration

We sampled behavioral and epidemiological parameters between their corresponding uncertainty bounds using Latin Hypercube sampling. For each created set of data, we simulated the behavior parameter of the possibility of HIV transmission per anal intercourse and the epidemic parameters of HIV prevalence, the number of newly diagnoses, the number of newly initiating treatments, and the number of MSM on ART and compared with collected epidemiological data. The difference between model simulations and actual epidemiological data was measured by the sum of squared residuals, which was regarded as the “goodness of fit” of the simulation. The sampling and simulation procedures were repeated for 1000 times, and we ranked the goodness of fit in an ascending order. We selected the top 5% of calibrated simulations to represent the epidemic for further calculations and projections.

Epidemic Projection and Impact Assessments

Based on the calibrated model, we forecasted the HIV epidemic trend and assessed intervention effects of expanding HIV screening test and treatment. In this context, we explored the scenarios that would best use health resources in achieving the targets. We increased the current HIV screening and ART coverage independently, and allowed the combination of these scenarios to project the future epidemic trends. Of these scenarios, we select the scenario that achieved the 90-90-90 targets by 2020 with a minimum number of HIV tests and ART person-years required. We repeated the same procedures to select an alternative scenario of achieving the targets by 2025. In both scenarios, we estimated epidemiological indicators, including the number of new HIV cases, number of diagnoses, people on ART and treatment failure, and number of HIV-related deaths. We hence estimated the percentage of diagnosis, timely treatment, and viral suppression. In this model, we approximated viral suppression percentage as the proportion of MSM on ART who did not fail the treatment in the past 12 months. We compared these epidemiological indicators with the status quo to estimate the number of new infections averted, deaths averted, and DALY averted over the next 2 decades.

Cost-Effectiveness Analysis

We estimated the total HIV investment cost for 2 periods: from 2016 to 2020 and 2016 to 2025, respectively. The total investment cost was calculated as the sum spent on HIV screening, ART, and viral load testing. The cost of HIV testing included the cost for HIV screening and confirmations. The cost of ART included both costs for first-line treatment and second-line treatment. The population impacts were assessed as the averted number of HIV infections, HIV-related deaths, and DALYs by the intervention compared with the status quo. For the cost-effectiveness analysis, we calculated the cost to avert 1 new HIV infection, HIV-related death, and DALY. If cost for each DALY averted was lower than the three times of per capita gross domestic product, we would deem the intervention as cost-effective.21 In China, per-capita gross domestic product was US $7924 in 2015.22 All original cost was in Renminbi and converted to US dollars (US $1 = RMB 6.85 as in 2016). The cost-effectiveness analysis was conducted in a government’s perspective. We used 3% as the discounting rate in our economic analysis.

RESULTS

HIV Epidemic Among MSM in 2016 to 2025

The model forecasted an increasing HIV epidemic trend between 2016 and 2025 (Figure S2, https://links.lww.com/OLQ/A207). By the end of 2020, the HIV prevalence in Chinese MSM would reach 12.6% (9.2–15.6%),;during 2016 to 2020, the accumulated number of new HIV infections and HIV-related deaths would amount to 236,926 (120,007–365,387) and 138,046 (78,151–211,967), respectively. The increase in the number of infected MSM would result in an additional 285,784 (188,655–368,250) people initiating ART in the next 4 years, leading to a total of 110,665 408,616 (239,557–539,411) MSM on ART by 2020. If the same trend continued, by 2025, the HIV prevalence would reach 16.2% (11.3–20.0%), whereas a further 508,492 (257,053–876,170) new infections and 307,666 (169,720–534,167) HIV-related deaths would occur. The increase number result in additional 245,749 (230,127–235,922) people initiating ART in the next 9 years, leading to a total of 578,187 (329,503–731,556). With the testing and treatment coverage, only 49.2% of the infected MSM will be diagnosed, 40.1% of the diagnosed MSM will be on treatment, and 93.5% MSM on treatment will achieve viral suppression by 2020, falling short of the 90-90-90 targets. Furthermore, these targets could not be achieved even by 2025 if there is no further scale-up of HIV screening and treatment in MSM.

Achieving the 90-90-90 Targets by 2020

Our findings indicated that at least 850,000 extra HIV screening tests, 112,500 extra person-year of ART, and a similar number of viral load tests during ART would be required to achieve UNAIDS’ 90-90-90 targets in MSM by 2020 (Fig. 1–3). This amounted to a total investment of US $478 million (US $302–723 million), an additional US $312 million compared with the status quo. After this scenario, the HIV prevalence at 2020 would be lowered slightly to 11.8% (8.4–13.7%). The intervention was forecasted to reduce 98,603 (58,914–162,440) HIV new infections, 67,600 (41,381–108,760) HIV-related deaths and 349,230 (215,250–565,770) DALYs, resulting in cost-effectiveness ratios of US $3201(US $2810–3435), US $4263 (US $3763–4956), and US $830 (US $733–931) for each of these aversions (Table 1). The strategy is highly cost-effective.

Figure 1
Figure 1:
Projected HIV epidemic trend in (1) status quo; (2) achieving 90-90-90 targets by 2020; (3) achieving 90-90-90 targets by 2025. The line in blue is the status quo, the line in black is in the scenario of achieving 90-90-90 targets by 2020; the line in red is in the scenario of achieving 90-90-90 targets by 2025.
Figure 2
Figure 2:
Impacts of HIV screening and treatment scale-up in Chinese MSM. In each of these subfigures, the x and y axes represent the extra number of HIV screening, ART person-years and viral tests per annum that our intervention scenarios add to the status quo. The contour curves (with color coding) represent the percentage of diagnosis, percentage on treatment, and percentage of viral suppression on 2020 (subplots A–C) and 2025 (subplots D–E). The red line represents the contour curve where 90% percentage has been achieved.
Figure 3
Figure 3:
The (A) percentage of diagnosis, (B) percentage on treatment, and (C) percentage of viral suppression in status quo and 2 scale-up scenarios aiming to achieve 90-90-90 targets by 2020 and 2025. The dashed green line represents the 90-90-90 targets, the line in blue is the status quo, the line in black is in the scenario of achieving 90-90-90 targets by 2020; the line in red is in the scenario of achieving 90-90-90 targets by 2025.
TABLE 1
TABLE 1:
Health Economical Evaluation of Scaling Up HIV Monitoring Tests and ART Among MSM

Achieving the 90-90-90 Targets by 2025

We investigated an alternative to achieving the 90-90-90 targets by 2025, in this case, about 340,000 extra HIV screening tests, 60,000 extra person-year on ART, and viral load tests annually will be required (Figs. 2 and 3). Over the next 9 years, the total extra investment would be US $412 million (US $256–594 million). The investment was expected to avert 111,430 (71,439–178,950) HIV infections, 90,720 (49,964–136,920) HIV-related deaths, and 480,710 (271,260–721,950) DALYs, corresponding to US $3612 (US $3125–4117), US $4544 (US $3986–5209), and US $851 (US $762–960) for each of these aversions (Table 1). The strategy is highly cost-effective.

DISCUSSION

Our findings indicated that the current HIV screening and ART coverage would not be sufficient to achieve the 90-90-90 targets in Chinese MSM by 2020, nor by 2025. Achieving these targets by 2020 requires a dramatic (188%) scale-up of HIV screening and ART over the next 4 years, but an extension of 5 years allows a more progressive scale-up (52%) in achieving these targets. We demonstrated that the interventions are both highly effective and cost-effective.

“Test-and-treat” is a highly effective and cost-effective means to achieving the 90-90-90 targets.14,17,23 A similar modeling study in Beijing MSM found that the total number of HIV new infections over the next 10 years would decline by 50% to 70% if the coverage of timely testing and treatment increase to 70%.24 Wang et al18 demonstrated that voluntary HIV testing and counselling was cost-effective in MSM. Studies in other countries, for example in India, demonstrated that one-off screening (incremental cost-effectiveness ratio, US $800/years-of-life saved) and annual screening (incremental cost-effectiveness ratio, US $1800/year of life saved) were both cost effective in high-risk groups.25 Similarly, a study based on urban MSM in New York City, indicated a scale up to 95% test rate and treatment all diagnosed patients would reduce the cumulative number of new infections by 69% over a 20-year period.17 However, a different voice appeared in the 21st International AIDS Conference. The first major population study for the “test-and-treat” strategy for HIV in a general African population showed that despite a high acceptance of HIV testing (85%), a poor overall linkage to HIV care (41%) in the intervention group resulted in no differences in HIV incidence compared with the control group which followed national guideline.26 The success of the intervention appears to rely on a strong linkage to HIV care that enable diagnosed individuals to initiate a timely treatment.

Achieving the 90-90-90 targets among the Chinese MSM still faces many challenges. One of these is identifying all individuals living with undiagnosed HIV infection. Stigma and discrimination against MSM, especially from health care providers, are a main barrier. One study on MSM in Beijing suggested that 86% of them were unaware of their infection status, and one third of them had never tested for HIV.27 Recently, WHO issued a guideline for HIV self-testing.28 The recommendation collated evidence from 5 randomized controlled trials worldwide and indicated that HIV self-testing, including home testing, significantly increased the uptake and frequency of HIV screening. This may be a potential strategy for the Chinese MSM. Location and time inconvenience is another potential barrier for the scale-up of HIV screening and ART in MSM. CDC clinics and hospitals are currently the only places providing HIV testing for MSM. Office hours are usually conflicted with MSM working time, and most MSMs are unwilling to leave work for the sensitive issue and undertake the potential income loss.29 Mobile clinics and setting up user-friendly clinics in MSM hotspots with the MSM community-based organizations may be an alternative for providing HIV screening.

Achieving the 90-90-90 targets in MSM require adjustments in the current HIV investment and resource allocation from the Chinese government. With the growing emphasis on HIV prevention and treatment, the national Chinese government has increased its spending on HIV prevention from US $15 million in 2002 to US $540 million in 2015. However, there is a misalignment of investment and resources for HIV care and treatment across the risk groups. Despite accounting for 17% new diagnoses, only 12.7 million dollars was spent on HIV among MSM in 2010, representing only 2% to 3% of the year’s whole budget.30 A study conducted in Dehong prefecture, southwest China, indicated that HIV prevalence among MSM has the second high HIV prevalence (28%) is comparable to injecting drug users (30%), but the proportion of spending on MSM is only 7% and is far lower than the 47% in injecting drug users.31 This spending is not matched with the rapidly increasing epidemic in MSM, suggesting a substantial underinvestment in this population. We forecast the current investment average of US $42 million annually on HIV screening and treatment will not meet the 90-90-90 targets in MSM by 2020. An additional US $78 million per year would provide extra HIV screening, person-years on ART, and viral load tests, achieving the targets by 2020. This scenario requires almost tripling the current governmental investment. Alternatively, if we postpone the targets to 2025, the increase of annual investment is only 52%. Achieving 90-90-90 by 2025 appears to be a more feasible approach for the Chinese government, which has taken over the financial burdens for HIV care and treatment since the withdrawal of the Global Fund in 2011. The extra investment requires matching development of health facility, training of medical personnel, and laboratory capabilities. A quality study among Chinese MSM indicated that among the six major effect factors of linkage and engagement in HIV care, the health institute and personnel played key roles.29 The latter scenario enables a more gradual improvement in health institute capacities and professional training of medical personnel for the scale-up.

Several limitations of the study should be noted. First, we assumed that a homogenous sexual behavioral pattern in Chinese MSM did not distinguish between the high-risk and low-risk MSM. The model did not account for the geographical differences, population migration, and the contribution of socioeconomic status to risk sexual behaviors. Such that, our model may have underestimated the population impacts of scale-up. Second, our model only included HIV testing conducted through official voluntary counseling and testing sites and hospitals appointed by the Chinese government, as we performed cost-effectiveness analysis from a government perspective. We did not include HIV testing through other means including self-testing and testing services through community-based organizations.3,32 Our model finding represents a conservative estimate to the percentage of HIV diagnosis. Third, data on HIV mortality and treatment failure rates by CD4 categories in Chinese MSM were rare. For these parameters, we consulted experienced HIV clinicians and used their expert estimates. Fourth, the model did not account for economies of scale, such as additional cost for reaching out to those who are currently not in care and less cost when coupled with other intervention programs. Fifth, both testing and treatment costs for HIV are declining in China, suggesting that the model may have overestimated the cost and underestimated the cost-effectiveness of the intervention for the studied period.

Our modeling study forecasted a less optimistic HIV epidemic trend among the Chinese MSM, indicating that the achievement of the 90-90-90 targets by 2020, and even by 2025, with the current investment is highly unlikely. However, an additional 52% investment for the next decade will achieve the 90-90-90 targets by 2025, and the scale-up is highly effective and cost-effective. This finding provides an important evidence that informs the government’s health policy decisions and resource allocations for HIV in the years to come.

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