Large-scale HIV testing in the older population in China: findings from a cross-sectional study

Abstract

Summary

Aiming to explore universal HIV testing, and to understand the exact HIV prevalence in the older general population, we conducted a community-based cross-sectional epidemiological investigation in two counties of Zhejiang province, China. Using census strategy and convenience sampling method, those participants who were older than 50 years and met eligibility criteria were enrolled, and HIV prevalence was presented as a crude infection rate. A total of 215,441 (64.82%) were enrolled into this study, HIV testing was added into their health exam plan and 18 were confirmed as HIV positive, giving a crude rate of 0.84/10,000. HIV prevalence was higher among men than among women in all age groups (p < 0.05). Unlike previous research, 14 cases (78%) still had a relatively high CD4 + count; 17 cases (94%) had been infected by sexual transmission. Active large-scale HIV screening by integrating into routine health care can be an effective strategy to find people living with HIV at relative early stage of disease.

Keywords

HIV AIDS epidemiology seroprevalence older people over 50 screening China

Introduction

As is known to all, sexually transmitted infections (STIs) predominantly affect the younger population who are usually more sexually active.¹ HIV interventions are also focussed on the young, in whom the highest incidence and health problems are seen in China.^2–4 The World Health Organization (WHO) generally reports HIV rates in adults only up to 49 years of age,⁵ and many national STIs and sexuality surveys concentrate mainly on the younger.^6–8 To date, few studies on HIV have focused on people aged 50 years or older, and these few studies mostly focused on developed countries.^9–11 Also there is an increasing amount of information on HIV among older adults in Africa.^12–15 Studies in sub-Saharan Africa indicated that there are approximately 21 million adult people living with HIV/AIDS (PLWHA), among which 14.3% were ≥50 years.¹³ Older populations of HIV-infected individuals in Australia have doubled from 12–14% to 23–28% in the past decade.¹⁶ Still there have been very little written about HIV among older adults in Asia.

As the population globally is ageing, rapidly increasing numbers of people are living long, healthy, and potentially sexually active lives.¹⁷ At the same time, the success of highly active antiretroviral therapy (HAART) can prolong life, and the average age of HIV-infected people living in resource-rich settings is increasing rapidly.^18–20 With longer life expectancies and improvement in the quality of life, the sexual activity of older people has largely changed. Studies have shown that older people remains sexually active: most men aged 50–64 years and those aged 65 years and older reported recent sex (84% and 75%, respectively) in Malawi.²¹ A subgroup analysis of 120 older women aged 46 years and older in the UK showed that most (70%) had been recently sexually active and more than half (59%) did not use condoms.²² Notably, in Australia among the older age group, half of the men and two-thirds of the women who had casual sexual encounters failed to use condoms consistently.²³ Such findings suggest that, irrespective of sexual orientation, a significant minority of older adults continue to participate in high-risk sexual behaviour. Community-based universal HIV testing has been successfully carried out in developed or developing countries,^24–26 but rarely among older populations.

In the present study, by integrating into public health service, a large-scale HIV testing programme was conducted in an older population, to explore the prevalence and characteristics of HIV infection in this population, so as to provide a reference for HIV aging-related research in similar areas worldwide.

Methods

Study setting and background

Zhejiang province is one of the most densely populated provinces in China, with a reported 11,357 HIV infections at the end of 2012.²⁷ The health exam plan (HEP) was first implemented by Zhejiang province in 2005 and has been provided free of charge to all residents every 2 years since then. In the present study, the HIV antibody test was added into the HEP in the year 2012. A cross-sectional study was carried out and the data were mainly collected from the HEP. We have defined ‘older’ as including members of the population 50 years of age or older.²⁸

Sample

Zhejiang Province covers a population of 54.4 million, involving 90 counties, and in our sample system all of these counties were ordered by their reported HIV rates; based upon these they were divided into levels. Considering the comprehensive organization and coverage of HEP, we chose one county in each level; in this way two counties were chosen. Using convenience sampling methods participants covering the entire older population in the chosen two counties were enrolled, and when the participants reached more than 60% of the entire older population (similar to the census), we finished the sample collection.

The population survey and testing were carried out from March to August 2012. To be eligible for the study, participants had to meet the following requirements: be a resident of the town or have lived there for >6 months, be older than 50 years old, and provide consent to participate in the study.

Data collection

The Prevention and Treatment Working Group of HIV/AIDS in the Zhejiang Major Infectious District carried out the field investigation after receiving appropriate training offered by the lead researchers in this study. The collected information consisted of demographics (gender and age) and HIV antibody status. For those who were HIV positive, epidemic information such as route of transmission, HIV risk behaviour, CD4+ cells count and marital status were also recorded.

Ethics

The study was approved by the Ethics Committee of The First Affiliated Hospital at the School of Medicine of Zhejiang University. Written consent was obtained from each participant. Those who were confirmed HIV positive were enrolled into China’s HIV/AIDS follow-up management system and cohort study.

Blood test

Blood samples were screened for HIV antibodies using an enzyme-linked immunosorbent assay technique (Beijing Wantai Ltd, China) according to the manufacturer's instructions. If the results were positive, two additional assays (the original assay plus a second confirmatory assay) were carried out in parallel. If both results were positive or the results were not in agreement, a confirmatory test was carried out using a Western blot assay (HIV BLOT 2.2; Genelabs Diagnostics Pty. Ltd, Singapore). The CD4 + T cells were counted by flow cytometry (Beckman Coulter Inc., Brea, CA, USA) according to a standard protocol.²⁹ All tests were performed in State Key Laboratory for Diagnosis and Treatment of Infectious Diseases.

Data analysis

All data collected by paper-and-pencil surveys were entered manually into a custom-designed database and analyzed using SPSS for Windows Version 16.0 (SPSS Inc., Chicago, IL, USA). Descriptive statistics were generated for each of the general characteristics variables. We used Chi square tests to compare the infection rate differences among the different demographic groups. All statistical tests were two-sided with a significance level of p < 0.05. Those in clinical stage IV (WHO) or with CD4+ <200 cells/mm³ were defined as “AIDS progression”, and the others were defined as “HIV progression”.³⁰

Results

Demographic characteristics

There were 332,369 older people in the two chosen counties; 215,441 (64.82%) completed HIV testing – 140,888 (72.72%) in county A and 74,553 (53.78%) in county B (Table 1). A total of 91,046 (36.66%) were men and the average age was 63.51 ± 8.76, ranging from 50 to 93 years (Table 2).

Table 1.

Coverage of the enrolled population in the two counties.

	≥50 population	Enrolled population	Participation rate (%)
Total	332,369	215,441	64.82
County A	193,748	140,888	72.72
County B	138,621	74,553	53.78

Table 2.

HIV infection situation in the older population.

	No. of participants	HIV+	Crude rate (/10,000)	p Value
Total	215,441	18	0.84
Gender				<0.01
Man	91,046	15	1.65
Woman	124,395	3	0.24
Age group				<0.01
50–59	80,341	9	1.12
60–69	84,967	7	0.82
70+	50,133	2	0.4

HIV infection prevalence in the older population

Of the 215,441 participants screened for HIV, 18 were positive, giving a crude rate of 0.84/10,000 (Table 1). Among men, the crude rate was 1.65/10,000, and among women, the crude rate was 0.24/10,000. HIV infection rate was higher among men than among women in all age groups (p < 0.05; Table 2).

As expected, we found significant differences in HIV infection rate by age (Table 2). HIV infection rate was significantly higher in participants aged 50–59 years than in older participants: the crude rate was 1.12/10,000. HIV infection rate was lowest for the 70+ age group: the crude rate was 0.4/10,000. The HIV infection rate difference between age groups was mainly due to the variability in male prevalence rates and no significant variation was seen among women throughout all age groups (Figure 1).

Figure 1.

Gender and age distribution of HIV prevalence. Note: * Significant difference (p < 0.05) between the 50–59 and 60–69 age groups in male population; ** Significant difference (p < 0.01) between male and female in 50–59 age group.

PLWHA character analysis

Of the 18 newly diagnosed PLWHA, 15 were men, with an average age of 60.67 ± 7.63 years. 2 of them had known their infection status (>4 years) and received HAART, while 16 of them did not know their infection status, and were newly diagnosed by this cross-sectional study. The mean CD4 + T count was 353 ± 145 cells/mm³, range from 146 to 625 cells/mm³. Only 22% (4/18) of them were in clinical stage IV (WHO) or CD4+ <200 cells/mm³; most of them were in “HIV progression” with relative high CD4+ cell counts. All of them were married, and most of the older PLWHA had been infected by sexual transmission: four cases (22%) by homosexual transmission and 14 cases (78%) by heterosexual transmission. Among the 13 cases that were infected heterosexually, four were couples, and further epidemiological investigation showed that two female PLWHA had been infected from their husbands, who were infected through unprotected sexual behaviour with female sex workers previously (Figure 2).

Figure 2.

Transmission routes of the 18 cases of PLWHA. Abbreviations: M, male; F, female.

Discussion

To our knowledge, the present study is the largest HIV screening programme focusing on the older population, by integrating it into the routine public health care of Zhejiang province. In two chosen counties, 64.82% of the older population completed HIV testing and we found that the crude HIV rate in this population was 0.84/10,000, which was almost the same as the prevalence recorded by routine monitoring of the general population of Zhejiang (0.01%).³¹ We postulate that the HIV infection rate in our study was much higher than the rate of the older population in the routine monitoring system, since HIV prevalence in the older population is usually much lower than that of the general population in China.³² Also there is growing evidence that the rate of new HIV diagnoses in the older population is rising, both in developed and developing countries.^21,33 For instance, in 2010, 14% of new HIV diagnoses were in the older population in the US.³⁴ The average age of HIV-infected populations in developing countries can also be expected to increase with the roll out of antiretroviral therapy (ART).³⁵ Due to widespread HIV screening, more PLWHA could be found, suggesting that such results might be more representative of the current epidemiology.

HIV prevalence in older men was significantly higher than that in the women (p < 0.05), and compared with women, men seem to have a greater risk of contracting HIV infection. This might reflect a high rate of sexual contact with female sex workers and low condom use rates in the older male population and high subsequent risk for STIs.³⁶ A community-based US study found that heterosexual men with HIV were more likely to report recent sexual activity than heterosexual women with HIV (72% vs. 21%, respectively).³⁷ With increasing age, the infection rate showed a downward trend, from 1.12/10,000 to 0.4/10,000. In a cross-sectional study of 541 PLWHA in the US, recent sexual activity declined significantly with age.³⁸ From the cross-sectional analysis between gender and age, the decline in the infection rate between age groups was mainly due to the decline in the male population infection rate, with no significant differences seen among women.

HIV late diagnosis was significantly more common in the older population than in the younger (62 vs. 48% respectively, p < 0.0001) in the UK³⁹ and often together with lower CD4+ cells counts. Increasing age is also an independent predictor of HIV progression or death among HIV-infected individuals, and delayed HIV diagnosis is associated with an increased risk of both HIV progression and death.⁴⁰ Unlike previous research that showed the older population were diagnosed at later stages of HIV infection than younger individuals,⁴¹ our study found that among PLWHA detected in this investigation, only 22% (4/18) were in AIDS progression; most (78%) were in “HIV progression”, with high CD4ﬂ cell counts. This may be due to the large scale of this HIV testing project where 16 of 18 were newly diagnosed. Such testing might lead to more PLWHA being diagnosed with higher CD4ﬂ counts, which may reduce the risk of opportunistic infections or death.

Most of the older PLWHA were infected by sexual transmission and among the 13 cases infected by heterosexual transmission, four were couples and two women might have been infected from their husbands, who were themselves infected by having sex with female sex workers. Very high rates of commercial sex worker contact (46%) among men aged 50 years and older were reported in a cross-sectional study in China, with 24% reporting multiple sexual partners and less than 4% reporting condom use.³⁶ Notably, extra-marital sex in women is rarely reported in China; evidence indicates that they are mostly infected via their husbands.^10,42 Female sex workers and their clients have became a bridge between the infection source and the general population.

The present study demonstrated successful HIV testing of the older population by integrating it into routine public health care in China. We found that HIV infection rate in the older population was 0.84/10,000, the first such rate to be reported in China. Unprotected sexual behaviour in the older male population might be the most important factor for HIV infection in this population, and prevention efforts are warranted, even though they are at lower risk of STIs compared with the younger population.

Footnotes

Acknowledgments

We thank the Bureau of Health of Zhejiang Province, and the members of the Bureau of Health of counties chosen in this study, for implementing of HEP. We also thank Prevention and Treatment Working Group of HIV/AIDS in Zhejiang Major Infectious District for supporting the data collection. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflict of interest

The authors declare no conflict of interest.

Funding

This study was supported in part by grants from the Mega-Project for National Science and Technology Development under the “11th and 12th, Five-Year Plan of China” (2011ZX10004-901, 2013ZX10004-904).

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