The HIV prevalence in older men who have sex with men in Western & Central Europe and North America

Abstract

The age of patients living with human immunodeficiency virus (HIV) is increasing and the greatest proportion of aged HIV patients occurred in Western and Central Europe and North America (WCENA). In aged HIV patients in WCENA, older MSM is the main population. The aim of our study was to evaluate the HIV prevalence in older MSM in WCENA. A meta-analysis was conducted. We searched Medline, Embase, PsycINFO, Web of Science, Cochrane library, Ageline databases, and government websites. Studies that estimated HIV prevalence in older MSM in WCENA were selected. The pooled HIV prevalence and odds ratio (OR) of the risk of living with HIV in older MSM were calculated. In total of 23000 records were initially records were identified and 12 records were included. The total sample size of older MSM was 6118. The pooled HIV prevalence in older MSM in WCENA was 26% (95% CI 18%–33%), which was much higher than that in younger MSM (18%, 95% CI 14%–21%). Notably, the HIV prevalence in older MSM has been continuously increasing in the past two decades in WCENA, raising from 16% to 33%. The pooled OR for older MSM to be living with HIV was 1.68 compared to younger MSM. The HIV prevalence in older MSM in WCENA is disproportionately high, with a continuously increasing trend in the past two decades. Older MSM also carry significantly higher risk of living with HIV than younger MSM.

Keywords

HIV men who have sex with men prevalence

Background

The age of patients living with human immunodeficiency virus (HIV) is steadily increasing since the introduction of effective antiretroviral therapy (ART), which has changed the prognosis of HIV infection from a fatal condition to a chronic disease.¹ In the world, the greatest proportion of older HIV patients occurred in Western and Central Europe and North America (WCENA). The proportion of patients living with HIV aged 50 years or over in WCENA was 50%, being much higher than that in other areas (16%–28%).² According to the data of UNAIDS, the number of patients living with HIV (PLWH) aged 15–49 in WCENA has remained stable since 2008, while the number of PLWH aged 50 years or over has increased from 520,000 in 2008 to 1,100,000 in 2018.² A model based on the HIV population in Europe predicted that the median age of HIV patients will increase from 43.9 years in 2010 to 56.6 in 2030 and the proportion of HIV patients aged 50 years or over will increase to 73% in 2030.³

In older aged HIV patients in WCENA, older MSM is the main population. It has been reported that among PLWH aged 50 years or over in WCENA, 78% of them were male patients.² According to the report of UNAIDS in 2018, 57% of new HIV infections in WCENA were attributed to sex between men.⁴ Some reports that were published in recent years also revealed a rapidly increasing trend of the number of older MSM living with HIV in WCENA.^5–8 From 2008 to 2015, the estimated annual percentage change of HIV prevalence in older MSM in USA was 11%, a much higher proportion than that among MSM aged 25–34 years (7.4%).^9,10 At the end of 2015, the number of MSM aged 50 years or over living with HIV in the U.S. was three times that of MSM aged 13–29 years.¹⁰

The increasing number of older MSM can significantly increase the medical demands. Patients living with HIV have a higher incidence and earlier age of onset for age-related non-communicable diseases, such as cardiovascular disease, osteoporosis, and diabetes, compared to HIV-negative people.¹¹ About 83% of PLWH aged 50 and older have at least one comorbidity. Disease management of HIV and comorbid conditions increases the complexity of treatment regimens, which may serve as barriers to adherence for persons in older adulthood.^8,10–12 The financial demands of older MSM would also significantly increase. It has been reported that average costs begin at $30,312 for persons living with HIV who exhibit no co-morbid conditions and increase substantially with additional conditions.¹³ Additionally, the majority of older MSM are at risk for experiences of stigma and discrimination, which highlights the need of psychological therapy and mental care.⁸

Although MSM are disproportionately affected by HIV infection, the published studies predominantly focused on adolescent and young MSM. Older MSM have been, and continue to be, overlooked. To our knowledge, there is a lack of clear and compelling evidence regarding HIV prevalence in older MSM. In consideration of the lack of globally compelling evidence and the potential society demands posed by the increasing number of older MSM living with HIV, we have conducted this systemic review with the intention to conduct a deep, comprehensive, and quantitative analysis on the HIV prevalence in older MSM in WCENA.

Methods

Search strategy and selection criteria

The protocol of this systemic review and meta-analysis was registered in PROSPERO (2018: CRD42018110113). We searched Medline, Embase, PsycINFO, Web of Science, Cochrane library, and Ageline. We also searched surveillance reports released by governments, which included Centers for Disease Control and Prevention, European Centre for Disease Prevention and Control, GOV.UK, and Government of Canada. The terms that were used in study searching mainly included “homosexuality”, “bisexuality”, “gay”, “MSM”, “men who have sex with men”, “queer”, “bisexual”, “HIV”, and “human immunodeficiency virus”. The example of searching strategy in Medline is shown in Supplemental Material.

The searches described above were completed on 31st December 2018. Two authors (LBZ and YMH) independently screened the titles and abstracts of search output to remove obviously irrelevant reports. After initial assessment, the full texts of all potentially eligible articles were retrieved. Then two review authors (LBZ and YMH) independently looked through the full texts. We recorded the details of whole screening process by completing a PRISMA flow chart.¹⁴ Multiple reports that derived from the same study were identified and the most informative one was included. Two authors (LBZ and LW) independently extracted data from all included reports. Disagreements on the eligibility of studies and data extraction were resolved through discussion. Consulting the third author or writing to the original investigators was done when necessary.

Eligible studies were those that met the following criteria: 1) with sufficient data for the calculation of HIV prevalence in older MSM; 2) HIV testing should be performed based on samples from blood, urine, or orals; 3) clear descriptions of sampling method; 4) conducted in WCENA area; 5) published in English; and 6) published between 1st of January 2003 and 31st of December 2018. The exclusion criteria included: 1) sample size of older MSM was less than 50; 2) recruitment relied on self-reported HIV infection status; 3) the sample predominantly or completely included individuals with specific behaviors or characteristics (e.g. male sex workers, money boys, transgender people, men who inject drugs, and men in prison), which may place people at high risk of HIV infection; 4) editorials or reviews; and 5) animal studies. For duplicate studies, we included the most informative one.

We defined countries in WCENA according to those specified in the UNAIDS website. In total, 36 countries were included.

Data extraction

Two authors independently extracted the data from all the included articles. The extracted data mainly included study basic information, study period, the definition of old age, demographic data of patients, sample size, and outcomes.

Data analysis

The pooled HIV prevalence and the odds ratio of living with HIV were calculated. Meta-analysis was done by using R 3.6.1 and Stata 12.0. The meta-analysis was performed by using a random-effects model. Statistical heterogeneity was evaluated by I² statistic. Sensitivity analyses according to sample size and study quality and subgroup analyses were performed to investigate the specific source of heterogeneity. Univariate meta regression was performed to further explore the source of heterogeneity by using restricted maximum likelihood (ReML).

Subgroup analyses based on country-level factors were performed to explore underlying factors that may affect the HIV prevalence in older MSM. The evaluated factors included HIV testing rate, high-risk sexual behavior rate, receipt of HIV prevention (individual- or group-level intervention), receipt of HIV prevention through free condom distribution, aging level, income level, and education attainment. Additionally, subgroup analyses were performed based on studied region and study period. Data on HIV testing rates, rate of high-risk sexual behavior, receipt of HIV prevention (individual- or group-level intervention), and receipt of HIV prevention through free condom distribution were directly extracted from original studies or related reports released by the same institution at same yea. Data on aging level were obtained from the estimation of “the population ages 65 and above, male (% of male population)” through the World Bank website.¹⁵ Data on income level were obtained from the estimation on “Gross National Income per capita, Atlas method (current US$)”, which was provided by World Bank.¹⁶ Country-specific estimates on education level were extracted from the data on “Bachelor's or equivalent (%) among 25 or older population”, which was provided by the United Nations Educational, Scientific and Cultural Organization Institute for Statistics.¹⁷

We assessed the quality of the included studies according to the following factors: source of population, rigorous diagnostic approach, controlled confounding factors, and sample size (eTable 1).¹⁸

Results

A total of 22997 records and 3 official reports were initially identified by searching several databases and government websites, respectively. After removing duplicates, the titles and abstracts of 17088 records were screened. In total of 755 records were considered eligible for full-text screening, of which 12 studies were included (Figure 1). The basic characteristics of all included studies^19–30 are listed in Table 1.

Figure 1.

The flowchart of study selection.

Table 1.

Basic characteristics of all included reports.

Study ID	Country	Study period	Sampling method	Sample size of older MSM	HIV prevalence among older MSM	Definition of old age	Sample size of young MSM	HIV prevalence among young MSM	Definition of young age
CDC 2019	USA	2017–2019	venue-based, time-space sampling	1449	32%	≥50	7850	22%	18–49
Mosley 2018	Canada	2012.2–2015.2	Respondent-driven sampling	178	54%	≥49	554	20%	18–48
CDC 2016	USA	2014	venue-based, time-space sampling	1223	28%	≥50	7512	21%	18–49
Welling 2015	Netherlands	2010.7–2011.7	Non-probability sampling	236	70%	≥45	542	28%	18–44
Wallace 2014	UK	2011.5	venue-based, time-space sampling	164	5%	≥46	1039	5%	16–45
CDC 2014	USA	2011	venue-based, time-space sampling	877	26%	≥50	7135	15%	18–49
CDC 2010	USA	2008	venue-based, time-space sampling	792	25%	>=50	7361	19%	18–49
Schwarcz 2007	USA	2002.6–2003.1	Probability sampling	358	20%	≥55	1618	26%	18–54
Williamson 2007	UK	2005	venue-based, time-space sampling	132	5%	≥46	1157	4%	17–45
CDC 2005	USA	2004.6–2005.4	venue-based, time-space sampling	102	31%	>=50	1665	25%	18–49
Xia 2006	USA	2002.5–2002.6	Probability sampling	100	16%	50–65	298	20%	19–49
Dolcini 2003	USA	1996.11–1998.12	Probability sampling	507	13%	≥50	NA	NA	NA

CDC, Centers for Disease; HIV, Human immunodeficiency virus; MSM, men who have sex with men; NA, Not available; UK, The United Kingdom; USA, The United States.

The pooled HIV prevalence in adult MSM (≥18 years old) in the WCENA was 19% (95% CI 15%–23%, I² = 99%). The pooled HIV prevalence in older MSM (≥50 years old) and younger MSM (18–49 years old) were 26% (1697/6118, 95% CI 18%–33%, I² = 98%) and 18% (95% CI 14%–21%, I² = 99%), respectively. The pooled OR for older MSM to be living with HIV was 1.51 (95% CI 1.23–1.87) compared to adult MSM in WCENA. The pooled OR for older MSM to be living with HIV was 1.68 (95% CI 1.27–2.23, I² = 93%) compared to younger MSM.

The trend of HIV prevalence in adult MSM, older MSM, and younger MSM in WCENA from 1997 to 2017 is shown in Figure 2. The HIV prevalence in older MSM was the highest. There was an obviously increasing trend of HIV prevalence in older MSM in the past two decades, raising from 13% to 32.4%. By contrast, the HIV prevalence in younger MSM remained relatively stable.

Figure 2.

The trend of HIV prevalence between 1997 and 2017 in WCENA.

The country-level HIV prevalence data are shown in Figure 3. The HIV prevalence in older MSM in USA, Canada, the UK, and the Netherlands were 24%, 54%, 5%, and 70%, respectively. The HIV prevalence in younger MSM in USA, Canada, the UK, and the Netherlands were 21%, 20%, 5%, and 28%, respectively. Our results also showed that the HIV prevalence in older MSM in USA has more than doubled in the last two decades and has remained far beyond the HIV prevalence in adult MSM since 2004.

Figure 3.

Map of the country-level pooled HIV prevalence in both older MSM and younger MSM in WCENA from 1997 to 2017.h.

Subgroup analyses were performed based on country-level variables (Table 2). The results showed that, regions with rates of HIV testing in the last 12 months in older MSM >60% (32%, 95% CI 30%–35%) had significantly higher HIV prevalence in older MSM than regions with rate of HIV testing in last 12 months in older MSM ≤60% (26%, 95% CI 23%–28%, I² = 58%). The rate of high-risk sexual behavior in older MSM being more than 55% (32%, 95% CI 30%–35%) indicated statistically higher HIV prevalence in older MSM, compared to that of ≤55% (24%, 95% CI 19%–30%, I² = 93%,). The HIV prevalence in older MSM during 2008–2018 (33%, 95% CI 23%–43%, I² = 98%) was more than twice that during 1997–2007 (16%, 95% CI 10%–24%, I² = 90%). Countries with Gross National Income (GNI) per capita of more than 50000 US$(41%, 95% CI 30%–53%, I² = 98%) have significantly higher HIV prevalence in older MSM than those with GNI per capita of ≤50000 US$(15%, 95% CI 9%–23%, I² = 94%).

Table 2.

The results of subgroup analyses categorized by multiple variables of interest of HIV prevalence in older MSM.

	Number of studies	Sample of older MSM	Pooled HIV prevalence	95% CI	I2	P^a
Rate of HIV testing in last 12 months among older MSM
>60%	1	1449	32%	30%–35%	/	0·003
≤60%	5	3094	26%	23%–28%	58%	0·003
Rate of high-risk sex behavior among older MSM
>55%	1	1449	32%	30%–35%	/	0·0076
≤55%	5	3501	24%	19%–30%	93%	0·0076
Receipt of HIV prevention in the 12 months before interview (Individual- or group-level intervention)
>13%	3	4443	29%	25%–33%	85%	0·5819
≤13%	2	894	27%	21%–33%	47%	0·5819
Receipt of HIV prevention in the 12 months before interview (Free condoms)
>70%	2	1325	28%	25%–30%	0%	0·6849
≤70%	2	2326	29%	23%–36%	91%	0·6849
Educational attainment, population 25 years and older-Bachelor's or equivalent (%)—Male
>35%	7	2914	26%	18%–34%	95%	0·9404
≤35%	5	3204	25%	12%–41%	99%	0·9404
Study period
2008–2018	7	4919	33%	23%–43%	98%	0·0075
1997–2007	5	1199	16%	10%–24%	90%	0·0075
Region
North America	9	5586	27%	21%–32%	95%	0·8318
Europe	3	532	22%	0%–73%	99%	0·8318
Population ages 65 and above, male (% of male population)
>13%	5	2159	30%	11%–54%	99%	0·5077
≤13%	7	3959	22%	18%–27%	90%	0·5077
Gross National Income per capita, Atlas method (current US$)
>50000	5	3963	41%	30%–53%	98%	0·0001
≤50000	7	2155	15%	9%–23%	94%	0·0001

HIV, Human immunodeficiency virus, MSM, men who have sex with men.

^aDifference between subgroups.

Univariate meta-regression was performed. The sampling method was set as the covariate and prevalence rate was set as the dependent variable. The results showed that sampling method did not contribute to the considerable heterogeneity using ReML method (p = 0.235).

We also accessed the quality of the included studies, and the results showed that ten studies were of high quality, while two were of moderate quality.^27,29 Sensitivity analyses were performed according to sample size and study quality, respectively. The results are shown in eTable 2. After excluding studies with a sample size of less than 200 or of low quality, the pooled HIV prevalence in older MSM were 30% (95% CI 22%–39%, I² = 98.2%) and 20% (14%–26%, I² = 97.2%), respectively.

Discussion

This study is the first meta-analysis evaluating the HIV prevalence in older MSM in WCENA. Our finding showed that HIV prevalence in older MSM in WCENA was 26%, higher than that in adult MSM and younger MSM. Our meta-analysis also highlighted that the HIV prevalence in older MSM has been continuously increasing in the past two decades in WCENA, raising from 16% (between 1997–2007) to 33% (between 2008–2018). Additionally, HIV testing rate, high-risk sexual behavior rate, and income level significantly affected HIV prevalence in older MSM. The results of this meta-analysis emphasized the heavy and continuously increasing HIV prevalence in older MSM, which is helpful for informing policy making, and the design of prevention and treatment strategies.

Few studies have evaluated the trend of HIV prevalence in older MSM in WCENA. An age-stratified survey in the U.S. has concluded that the annually increase rate of HIV prevalence in older MSM was 10.8% between 2008 and 2016,¹⁰ which is consistent with the increasing trend in our results.

The aging HIV epidemic can be a complex process and it is hard to explain this phenomenon with a single factor. According to the results of subgroup analysis in our study, four factors had significant impact on HIV prevalence in older MSM (Table 2). The first one was study period. In recent years, there was a significant improvement in medicine, health service provision, and economy, which might all lead to better HIV prevention and treatment. Therefore, with time passing by, the older MSM with HIV infection can have a prolonged lifetime and more young people with HIV infection can survive in old age, thus leading to the increased HIV prevalence in older MSM.³¹ The second factor was gross national income (GNI). The increased GNI indicates greater investment on HIV infection, which would lead to easy access to HIV services, wide coverage of antiviral treatment, better prognosis of HIV disease, and thus, high HIV prevalence in older MSM. The third factor was HIV testing rate. It has been reported that 14% of MSM in the America were unaware of their HIV infection.^32,33 High rates of HIV testing would increase the awareness of positive HIV status in older MSM and thus lead to higher HIV prevalence.³³ Furthermore, rate of high-risk behaviors was the fourth significant factor. Older MSM tend to exhibit higher-risk sexual behaviors, and their condom use rate was significantly lower than that among heterosexual men (24% VS 53%).^34,35 Higher-risk sexual behavior would make older MSM face greater risk of HIV infection and thus lead to high prevalence of HIV infection.³⁵

Although we reported a great proportion of older MSM living with HIV, the real figure may be higher, because of the low HIV testing rate and continuously active sexual activity in older MSM. A study focusing on the older MSM who use dating application has reported that the testing rate in older MSM was only 47%.³⁶ In the future, widely-covered HIV care and special program on older MSM should be promoted by the government and public health agencies to reach, educate, and help older MSM. Increasing the attention on older MSM is necessary in the implement of “90–90-90” AIDS ending plan.

Considerable heterogeneity existed in the meta-analysis in the present study. Sensitivity analyses, subgroup analyses, and meta-regression were performed to evaluate the impact of interested factors on heterogeneity. The results of all analysis failed to identify the exact source of heterogeneity, except the subgroup analysis categorized by the receipt of HIV prevention in the 12 months before interview (free condoms). In the subgroup analysis of the rate of receipt of free condoms in the 12 months before the interview >70%, the heterogeneity was 0%. Therefore, this factor might be a reason of the considerable heterogeneity in the pooled analysis.

There were some limitations in our meta-analysis. In this review, we focused on the HIV prevalence in WCENA, which include 36 countries. However, there were insufficient data related to many countries in WCENA and the estimates of only four countries were available. Limited data may increase the risk of bias and our results might not represent the actual HIV prevalence in older HIV in WCENA very well.

Conclusion

Although older MSM is an overlooked population in HIV epidemic, the HIV prevalence among this population in WCENA is disproportionately high, with a continuously increasing trend in the past two decades. Older MSM also carry a significantly higher risk of living with HIV than adult MSM and younger MSM.

Supplemental Material

sj-pdf-1-std-10.1177_0956462420967576 - Supplemental material for The HIV prevalence in older men who have sex with men in Western & Central Europe and North America—a meta-analysis

Supplemental material, sj-pdf-1-std-10.1177_0956462420967576 for The HIV prevalence in older men who have sex with men in Western & Central Europe and North America—a meta-analysis by Bozhi Liu, Minghua Yu, Jinglong Chen and Wei Li in International Journal of STD & AIDS

Supplemental Material

sj-pdf-2-std-10.1177_0956462420967576 - Supplemental material for The HIV prevalence in older men who have sex with men in Western & Central Europe and North America—a meta-analysis

Supplemental material, sj-pdf-2-std-10.1177_0956462420967576 for The HIV prevalence in older men who have sex with men in Western & Central Europe and North America—a meta-analysis by Bozhi Liu, Minghua Yu, Jinglong Chen and Wei Li in International Journal of STD & AIDS

Footnotes

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by Capital's Funds for Health Improvement and Research (CFH 2020–2-2175) and the Beijing Talents Project.

ORCID iD

Wei Li

Supplemental material

Supplemental material for this article is available online.

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