AIDS in China: recent trends

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R EVIEWS Epidemiology of HIV/AIDS in China: recent trends Yan Cui1, Cynthia X. Shi1,2, Zunyou Wu1* 1 National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China 2 Department of Epidemiology of Microbial Diseases and Center for Interdisciplinary Research on AIDS, Yale School of Public Health, 135 College Street, New Haven, CT 06520, USA Abstract We used nationally reported cases (NCAIDS/China CDC, 2016) and published literature to summarize up-to the end of 2015 epidemiologic trends in the HIV/AIDS epidemic in China. HIV-positive cases are distributed unevenly with most infections found in southwest China and the most affected population being men who have sex with men. Transmission mode of HIV infection has shifted from drug injection to sexual contact, which accounts for 95% of total reported cases. Two thirds of cases are from heterosexual transmission. Transmission pattern varies greatly throughout China. Some provinces in China reported heterosexual transmission accounted for over 90% of cases while other provinces reported homosexual transmission accounted for over 80% of cases. Patterns of heterosexually acquired HIV also vary widely, with 80% of cases attributed to commercial sex in some provinces, while in other provinces non-commercial extramarital sex accounted for over 70% of cases. Significant increase in HIV infection was observed among young students aged 15-24. China has successfully controlled blood transfusion-and injecting drug-related transmissions of HIV. Homosexual and noncommercial extramarital heterosexual transmissions have become new challenges for China’s HIV/AIDS program. Urgent adoption of the UNAIDS/WHO 90-90-90 target will help overcome these new challenges. Keywords: HIV; AIDS; epidemiology; China

Introduction The HIV/AIDS epidemic began in China 30 years ago when the first AIDS case was reported in 1985 [1]. Geographic distribution, modes of transmission, key affected populations of HIV infection have changed significantly over time [2-9]. In terms of relative measurements, such as prevalence, China is ranked low

*Correspondence: [email protected] or [email protected] PEOPLE’S MEDICAL PUBLISHING HOUSE Co., LTD.

among countries that have HIV/AIDS epidemics [10]; in terms of absolute number of people living with HIV (PLHIV) and the number of new HIV infections per year, China is among the top 15 countries that comprise 75% of the global number of PLHIV and new HIV infections [11]. Thus, China’s response to its HIV/AIDS challenge may impact how other countries manage their own crises.

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In developing this article, we used both national reported data and published literature to summarize the current trends and characteristics of HIV/AIDS in China.

Epidemiology At the end of 2015, the official reported number of PLHIV in China was 577,423 [12]. The actual number of PLHIV was estimated to be 850,000, with two thirds of this number diagnosed and the remaining one third undiagnosed [13]. In 2015, the epidemiology of HIV/ AIDS showed new trends in China, including the rising number of newly reported HIV infections among men who have sex with men (MSM), while the number of HIV diagnoses among injecting drug users (IDU) fell. Newly reported infections among heterosexuals remained at two thirds of all new diagnoses [12]. Across all age groups, new infections in youth and older adults significantly increased. In terms of geographic distribution, most newly reported HIV infections were in the southwest regions, although the number of new cases in other areas also increased [12].

Geographic characteristics By the end of 2015 among the 31 provinces, autonomous regions, and municipalities in main land of China (not including Taiwan, HK, and Macao), 15 reported 10,000 or more PLHIV, which accounted for 87.6% of the total number of PLHIV in China [12]. Yunnan, Sichuan, and Guangxi provinces each reported 50,000 or more PLHIV, accounting for 40.5% of the country total [12]. HIV/AIDS distribution in these three provinces was uneven at the provincial, prefectural, and county levels, with 5 counties that each had a prevalence of over 1% [12]. In 2015, about 144 million HIV tests were performed in China, an increase of 12.5% over 2014. Testing resulted in 115,465 new diagnoses of HIV infection, a rise of 11.6% as compared with 2014 [12, 14]. Implementation of HIV testing varies significantly across the country, making it inappropriate to directly compare the number of HIV tests performed among provinces since population sizes vary. If we use the number of HIV tests performed divided by the population size as an indicator to measure the HIV testing effort, the national rate is 10.5%, with 26.5% for Xinjiang Autonomous Region, which had the highest

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testing rate, followed by Yunnan Province at 21.1%, Beijing Municipality at 20.2%, Guangxi Autonomous Region at 20.2%, and Zhejiang Province at 17.3%, while the lowest HIV testing effort was only 1% in Tibet in 2015 [14]. The efficiency of HIV testing depends on HIV prevalence of the subpopulation and the subpopulation selected for HIV testing. We used the number of HIV infections diagnosed divided by the number of people participating in HIV testing as an indicator to measure HIV test efficiency. The national average efficiency rate was 0.08% in 2015, with the three highest rates in Tibet (0.35%), Sichuan (0.2%), and Chongqing (0.19%). The provinces with the lowest rates (0.03% each) were in Hebei, Shandong, and Ningxia [14]. HIV positive rate varied greatly among populations tested. Highest positive rate was among spouses of HIV positive individuals (8.435%), followed by children born to HIV-positive women (4.036%), and people who went to HIV test sites for voluntary counseling and testing (1.361%, Table 1). The lowest positive rate was among paid plasma or blood donors (0.002%). The positive rate (0.058%) in medical settings was lower than the national average (0.08%). The largest number of newly diagnosed HIV infections in health care settings remained the single major source of detected HIV infections, accounting for 52.19% (60,257/115,465) of the total number of cases diagnosed. The second largest source of HIV diagnoses was voluntary counseling and testing, accounting for 28.95% (33,424/115,465) of total newly reported HIV infections. In 2015, a total of 24,827–overall causes of deaths among PLHIVs were reported: 21,687 persons died in 2015 and were reported in the same year, while 3140 died in the previous year and were reported in 2015. The annual national average mortality was 3.5%, 0.3 percent lower than in 2014 (3.8%). Twenty-three of the 31 provinces, autonomous regions, and municipalities, experienced a decline in overall mortality in 2015 compared with the previous year. The greatest reduction occurred in Xinjiang Construction Corps, which saw a drop in overall mortality from 9.8% in 2014 to 4.5% in 2015. However, in 8 provinces, there were increases in mortality, with the largest increase occurring in Guizhou, from 5.8% in 2014 to 6.4% in 2015. The highest mortality PEOPLE’S MEDICAL PUBLISHING HOUSE Co., LTD.

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Table 1  Numbers of HIV tests and newly diagnosed HIV infections in China in 2015 Newly diagnosed HIV

Population tested for HIV

No. HIV tests

Total

143,583,117

115,465

0.080

Medical services

103,296,143

60,257

0.058

 Surgery

44,990,604

13,498

0.030

 Transfusion

6,591,229

974

0.015

  STD clinic attendants

2,503,842

6,739

0.269

  Other patients

30,335,464

37,381

0.122

  Postpartum care

18,875,004

1,665

0.009

Premarital health checkup

6,518,088

2,640

0.041

Voluntary counseling/testing

2,456,330

33,423

1.361

HIV+ individual’s spouses

45,668

3,852

8.435

Children of HIV+women

6,417

259

4.036

Occupational exposure

15,209

5

0.033

Entertainment industry personnel

1,307,214

396

0.030

Paid plasma/blood donors

8,205,738

165

0.002

Voluntary plasma/blood donors

11,864,035

2,769

0.023

Entry/exit border

710,107

280

0.039

Military recruits

374,267

122

0.033

Drug users in detention centers

339,838

1,647

0.485

Female sex workers in detention

15,794

70

0.443

Other detainees

1,394,661

2,523

0.181

Special survey

2,714,989

3,560

0.131

Others

4,318,619

3,497

0.081

infections

HIV positive rate (%)

Source: NCAIDS/China CDC, 2016

rate was 7.0% in Jiangxi province, that nearly double the national average.

Transmission modes In 2015, heterosexual transmission accounted for the largest proportion (66.3%) of newly reported HIV cases, followed by male-to-male sex (28.3%), injecting drug use (4.3%), and mother-to-child transmission (0.6%) (Figure 1). From 2011 to 2015, the proportion of HIV infections via injecting drug use was reduced from 14.2% to 4.3%. However, the proportion of infections via homosexual contact increased from 14.7% to 28.2%. The PEOPLE’S MEDICAL PUBLISHING HOUSE Co., LTD.

proportion by heterosexual contact remained the largest proportion of infections between 65% and 70%. Among males, transmission in the 15-24 age group was primarily through male-to-male sex (69.2%), while among people 50 years or older, heterosexual contact was the primary transmission mode (87.7%). Dose-response relationship was found along with age increasing groups, the proportion of infections through heterosexual contact was increasing (Figure 2). Among females 15 years or older, over 95% of HIV cases were from heterosexual contact (Figure 3). Among heterosexual males, HIV infection was

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Figure 1  HIV transmission modes in China, 2011-2015

Figure 2  New HIV diagnoses in China in 2015 among males by age and transmission mode

Figure 3  HIV transmission mode in China in 2015 among females by age groups

primarily contracted through commercial sex, accounting for 53.4% while non-commercial extramarital sex accounted for 40.2%, and spousal transmission for 3.6% (Figure 4). Among females, non-commercial extramarital sex accounted for 60.2% of all transmissions, spousal transmission for 26.9%, and commercial sex for 10.5%.

Overall, non-commercial extramarital sex was the primary HIV transmission mode, which accounted for 46.3% of newly diagnosed cases, while commercial sex accounted for 40.2%, and spousal transmission accounted for 10.8%. Transmission mode varied throughout the country. In PEOPLE’S MEDICAL PUBLISHING HOUSE Co., LTD.

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Figure 4  Newly reported HIV infections among heterosexuals in China in 2015 by sex and sexual pattern

general, in 2015 male-to-male sex was the primary mode of HIV transmission in urban areas, while heterosexual contact was the dominant mode in rural areas. For example, MSM is the major sex behavior underlying HIV transmission in the municipalities of Beijing, Shanghai, Tianjin, and in provinces such as Liaoning, Jilin, Heilongjiang, and Jiangsu. Heterosexual contact is the most common mode of transmission in the provinces of Guangxi, Yunnan, Sichuan, and the municipality of Chongqing. There was also disparity in heterosexual transmission. For example, among reported heterosexual cases, most acquired HIV infection via commercial sex, while most heterosexual HIV infections in Yunnan were acquired via non-commercial extra-marital sex [12,13].

Demographic characteristics Among new cases, males outnumbered females, with the male to female ratios increasing year over year from 2.6∶1 in 2011, 2.8∶1 in 2012, 3.1∶1 in 2013, 3.4∶1 in 2014, to 3.7∶1 in 2015. This persistent increase suggests that new infections among males, particularly MSM, continued to rise during those 5 years. The male to female ratio varied among different age groups, with the highest ratio of 5.9:1 observed in 20-24 year olds, followed by 5.1∶1 among those≥65 years , and 4.8∶1 in 15-19 and 25-29 year olds. Among males, most HIV diagnoses were in young adults, with 25-29 year olds accounting for the highest proportion of total cases (15.5%, Figure 5).

Figure 5  Distribution of newly reported HIV infections by sex and age group in 2015 PEOPLE’S MEDICAL PUBLISHING HOUSE Co., LTD.

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Unexpectedly, persons 65 years or older accounted for a considerable proportion of newly reported cases (9.9%). In females, the proportions in among the various age groups from 20-24 through 60-64 were similar, with women 65 years or older accounting for 7.2% of new cases, though this proportion was smaller than that observed in males.

HIV infection among youth By the end of 2015, there were 9569 HIV diagnoses among youth aged 15-24, accounting for 1.7% of total PLHIV in China. Based on Wu’s work [15] the HIV epidemic among youth can be summarized as follows: (1) New diagnoses continued to rise year over year. In 2008, newly reported HIV infections numbered 482 and by 2015 this number had risen to 3,236. (2) Sexual contact was the primary transmission mode, and the proportion of HIV infection via MSM increased between 2008 and 2015, from 58.5% to 82.6%. (3) In terms of newly diagnosed cases, high school students aged 15-17 years accounted for 12.3%, college students aged 18-22 years accounted for 77.5%, and graduate students aged 23-24 years accounted for 10.3%. Male to female ratio of newly reported cases was 45.9:1 in 2015. (4) Among all provinces, autonomous regions, and municipalities, total numbers of newly diagnosed HIV infections among youth were inconsistent. The five provinces with the highest total newly reported cases were Yunnan (86,483), Sichuan (78,261), Guangxi (69,379), Henan (47,617), and Guangdong (41,706), while the provinces and municipality with the highest numbers of new cases among youth were Sichuan (271), Jiangsu (202), Chongqing (187), Hunan (172), and Guangdong (171).

Discussion Recent evidence of changes in modes of HIV transmission requires different response strategies than previously. For heterosexual transmission by commercial sex, female sex workers, particularly those who accept low fees and older women, who were most unlikely to use prevention measures, should be a key group for HIV/AIDS program efforts. In areas where HIV transmission is primarily through non-commercial extramarital sex, each HIVinfected individual has the potential key to spread HIV. Therefore, expanding HIV testing to identify and initiate

treatment of these undiagnosed carriers is an important step toward preventing spread of the disease. China was among the first countries [16] to formally to adopt the UNAIDS/WHO 90-90-90 target: by 2020, 90% of infected people should know their status, 90% of diagnosed cases should be on antiretroviral medication, and 90% of those being treated should have fully suppressed viral load [17]. It is currently estimated that in China close to 70% of people currently infected have been diagnosed [14]. Screening confidentiality remains a deterrent to uptake of testing [18]. To overcome this barrier, China is promoting the use of self-testing [16]. Increased personalized services provided by communitybased groups who have the freedom to work with greater independence from the health authorities are also likely to encourage those who test positive at home to seek care. A recent policy change will contribute greatly to increasing treatment among those diagnosed. In February 2016, the Chinese government dropped the biological threshold for treatment. Prior to this, patients were required to undergo testing for a CD4 cell count, which had to be below 500 cells/mm3 before they could be treated. With the threshold restriction the proportion of diagnosed people eligible for treatment was only 78%. By eliminating this restriction, it is hoped that more individuals at risk of HIV infection will seek testing and thus treatment.

Additional files Contributors YC designed the study and conducted the data analysis. ZW designed the study and wrote the draft of the manuscript. All authors contributed to the interpretation of the data, revisions of the manuscript, and approved the final manuscript.

Conflicts of interest None declared.

Disclaimer The opinions expressed herein reflect the collective views of the authors and do not necessarily represent

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the official position of the National Center for AIDS/STD Control and Prevention, Chinese Center for Diseases Control and Prevention.

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