Introduction
Human immunodeficiency virus (HIV) infection and the resulting acquired immune deficiency syndrome (AIDS) is a serious public health threat worldwide. According to the latest global progress report on HIV/AIDS prevention 2021 released by the Joint United Nations Programme on HIV/AIDS (UNAIDS), there was 37.7 million existing HIV/AIDS cases by the end of 2020 and with 1.5 million new infections of HIV/AIDS in 2020 [1], the global spread of the AIDS epidemic is still not promising. Currently, men who have sex with men (MSM) were recognized as high-risk groups for HIV infection [2].
In China, MSM were generally a high-risk population, the proportion of male same-sex sexual transmission increased from 2.5% to 2006 to 28.3% in 2015 among people with HIV/AIDS reported in 2016 [3]. MSM was one of the socially sensitive groups, which easily lead to the transmission of HIV with high-risk sexual behaviors such as multiple sexual partners, frequent changes of sexual partners, high rates of unprotected sex, and complex social networks [4‐7]. In addition, more people were looking for sexual partners through the Internet, which not only increases the number of sexual partners, but may also accelerates the spread of HIV [8]. The incidence of new HIV infection was increasing year by year, due to the complexity and secrecy of the sexual behavior relationship network in the MSM, which brings severe challenges to HIV control and prevention work in China [9].
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Maanshan City is an inland city of Anhui Province in East China, and although it is located in Anhui Province, it is very close to Nanjing City, the capital of Jiangsu Province. As a central city in the Yangtze River Delta region, Nanjing City has a large number of migrants, and the proportion of HIV positive cases reported in Nanjing increased year by year through sexual transmission, mainly through MSM routes [10]. Influenced by the HIV epidemic in Nanjing City, the HIV epidemic in Maanshan City rose rapidly after the first case of HIV infection was detected in 2002 [11], the total number of HIV infectors was 2.40-fold high in September 2009 compared which in December 2007 [12, 13]. In 2012, the HIV-positive rate was 3.5% among MSM in Maanshan City, which has become one of the most important group for HIV infection [14].
Prior to this, many studies focused on the impact of drug abuse on HIV transmission in Maanshan, but there were no in-depth study on the behavioral characteristics of HIV transmission among MSM [13, 15]. The purpose of this study was to explore the behavioral characteristics of the MSM in Maanshan City, and to compare and analyze the behavior of HIV-positive and HIV-negative in MSM, which was helpful to find some potential influencing factors and has important guiding significance for the HIV control and prevention in MSM.
Methods
Study setting
A cross-sectional study was conducted among MSM in Maanshan City from June 2016 to June 2019. All staff underwent rigorous and uniform training prior to the investigation. 30 volunteers were recruited for a pilot survey, the questionnaire (Supplementary material 1) and workflow of investigation were modified according to the feedback of the volunteers. MSM recruited by Blue-Heart working group and a face-to-face interview with anonymous questionnaire was conducted in a separate room upon obtaining informed consent, then, all participants underwent rapid HIV blood testing at the Blue-Heart working group by local Maanshan Center for Disease Control and Prevention (CDC) trained and qualified Blue-Heart working group personnel, with test strips provided by the Maanshan CDC. Early screening HIV-positive participants were referred to laboratory of Maanshan CDC to confirm HIV infection, and obtain the required information from the Integrated HIV Prevention and Control Information System of the Chinese CDC. Fingerprints or unique identification numbers such as WeChat Quick Response (QR) code (contains a specific content format that can only be correctly identification by the WeChat software as a uniqueness for each user) were collected to avoid repetitive investigation. For participants who were not able to complete the survey during the initial visit, a separate appointment was made during a mutually convenient time. Specially-assigned research personnel reviewed the questionnaire on the spot every day, and carried out a supplementary investigation on missing items or logistically promptly.
Participants
The participants were recruited with a peer-driven sampling method by Blue-Heart working group, a community organization that specialized in HIV test, intervention and counseling services for MSM in Maanshan City. And the inclusion criteria of MSM as follows: (1) aged 18 and above; (2) working, living, or studying more than 3 months in Maanshan City; (3) had anal and/or oral sex behavior with at least one man in the last 6 months; (4) self-reported as HIV negative or unknown. Participants with serious mental illness and refused to write informed were excluded.
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Definition of indicators
(1)
MSM were defined as cisgender males who self-identified as gay/bisexual or self-reported having anal sex with another male.
(2)
Multiple partner index defined as having two or more partners who have sex.
(3)
Indicators of unprotected sex (including oral, anal, and vaginal sex) were defined as anything other than the absence of sex or consistent use of condoms during sex.
Statistical analysis
Questionnaires were double-entered and then checked for accuracy using EpiData 3.1 (EpiData Association, Odense, Denmark). SPSS version 23.0 (SPSS Inc., Chicago, IL, USA) was used for statistical analysis after logic check and collation. In descriptive analyses, categorical variables were presented as percentage, while continuous variables were expressed as means and standard deviations (SD) or median and inter-quartile range (P25, P75). The Mann-Whitney U test, chi-square tests, chi-square trend test, Poisson regression analysis and multivariate logistic regression analysis model were used for statistical analysis. Poisson regression analysis and multivariate logistic regression analysis models were used to assess the factors influencing HIV infection, and significant variables from the univariate analysis were included in the regression analysis model. P < 0.05 was considered to be significant.
Ethical considerations
The study protocol was approved by the Biomedical Ethics Committee of Anhui Medical University.
Informed consent was asked to sign for all eligible participants when the survey was starting. Participants could receive a gift for prizes of up to 30 Chinese Yuan (CNY) upon the completion of the survey.
Results
General demographic characteristics of the MSM participants
As show in Table 1, a total of 934 MSM were investigated in this study, including 816 HIV negative participants and 118 HIV positive, and the overall average age was 30.5 (SD = 8.90) years. 73.9% (n = 690) participants were Maanshan household registration, and majority of participants (n = 916, 98.1%) were Han ethnic. Most of participants had lower level of education (senior high school or below, n = 687, 73.6%). Besides these, 53.2% (n = 497) participants were unmarried, 75.7% (n = 707) participants’ monthly income over CNY 3 000, and approximate one in third participants were laborer and freelancer.
Table 1 shows that the HIV-positive rates were significantly associated among occupations, education levels and monthly income categories (all P < 0.05). The participants of freelancer (n = 58, 20.6%) has highest HIV-positive rate, while the rate of HIV-positive in bachelor degree or above (n = 19, 7.7%) and monthly income less than 1 000 yuan (n = 11, 6.8%) were lowest.
Table 1
General demographic characteristics of the MSMa participants in Maanshan, China
Variable | HIV-negative [M(P25,P75)]/[n (%)] | HIV-positive [M(P25,P75)]/[n (%)] | χ2/Z | P-value | |
|---|---|---|---|---|---|
Total | 816(87.4) | 118(12.6) | |||
Age (years old) | 30.3(24.0,34.0) | 31.8(26.0,36.3) | 2.66b | 0.008 | |
Household registration | 1.56c | 0.458 | |||
Maanshan City | 601(87.1) | 89(12.9) | |||
Other cities of Anhui Province | 122(90.4) | 13(9.6) | |||
Other Provinces | 93(85.3) | 16(14.7) | |||
Ethnicity | 0.03c | 0.871 | |||
Han | 801(87.4) | 115(12.6) | |||
Other nations | 15(83.3) | 3(16.7) | |||
Occupation | 36.45c | < 0.001 | |||
Student | 146(95.4) | 7(4.6) | |||
Farmer | 47(97.9) | 1(2.1) | |||
Laborer | 263(88.6) | 34(11.4) | |||
Public institutions | 94(93.1) | 7(6.9) | |||
Freelancer | 223(79.4) | 58(20.6) | |||
othersd | 43(79.6) | 11(20.4) | |||
Education level | 9.31c | 0.025 | |||
Primary school or less | 133(85.8) | 22(14.2) | |||
Junior high school | 212(83.5) | 42(16.5) | |||
Senior high school/Technical secondary school | 243(87.4) | 35(12.6) | |||
Bachelor degree or above | 228(92.3) | 19(7.7) | |||
Marital status | 3.04c | 0.219 | |||
Unmarried | 435(87.5) | 62(12.5) | |||
Married | 304(88.6) | 39(11.4) | |||
Divorced/widower | 77(81.9) | 17(18.1) | |||
Monthly income (yuan/RMB) | 16.21c | 0.001 | |||
< 1 000 | 151(93.2) | 11(6.8) | |||
1 000–2 999 | 50(76.9) | 15(23.1) | |||
3 000–4 999 | 328(84.5) | 60(15.5) | |||
≥ 5 000 | 287(90.0) | 32(10.0) |
Sexual orientation and activity range of MSM
Table 2 shows that of the 934 participants, most (n = 722, 77.3%) MSM to find their male partners with Internet or dating Apps, and they had higher HIV positive rate (n = 100, 13.9%), but the difference among age when they first had sex with another man, sexual orientation and main way to find male partners were no significant difference (all P > 0.05). From Maanshan City to outside of Anhui Province, HIV positive rates increased with the increased scope of activities (trend χ2 = 39.99, P < 0.001), as did the number of MSM friends (trend χ2 = 64.22, P < 0.001) and the number of male sexual partners increased (trend χ2 = 37.27, P < 0.001).
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Table 2
Sexual orientation and activity pattern of MSMa in Maanshan, China
Variable | HIV-negative [M(P25,P75)]/[n (%)] | HIV-positive [M(P25,P75)]/[n (%)] | χ2Z | P-value | |
|---|---|---|---|---|---|
Total | 816(87.4) | 118(12.6) | |||
Age when they first had sex with another man | 22.5(19.0,24.0) | 22.0(20.0,23.0) | 0.38b | 0.701 | |
Sexual orientation | -c | 0.062 | |||
Homosexual | 795(87.3) | 116(12.7) | |||
Bisexual | 4(66.7) | 2(33.3) | |||
Others | 17(100.0) | 0(0.0) | |||
Main way to find male partners | 4.63d | 0.201 | |||
Bar/dance hall/club | 93(91.2) | 9(8.8) | |||
Internet/dating Apps | 622(86.1) | 100(13.9) | |||
Public bathhouse | 55(90.2) | 6(9.8) | |||
Other ways | 46(93.9) | 3(6.1) | |||
Scope of sex partner distribution | 41.46d 39.99e | < 0.001 < 0.001 | |||
In Maanshan City | 205(93.2) | 15(6.8) | |||
Cross-region within Anhui Province | 318(93.0) | 24(7.0) | |||
Outside of Anhui Province | 293(78.8) | 79(21.2) | |||
Number of MSM friends | 60.38d 64.22e | < 0.001 < 0.001 | |||
< 10 | 86(92.5) | 7(7.5) | |||
11–20 | 99(92.5) | 8(7.5) | |||
21–50 | 287(97.0) | 9(3.0) | |||
≥ 51 | 344(78.5) | 94(21.5) | |||
Number of male sexual partners | 31.74d 37.27e | < 0.001 < 0.001 | |||
< 6 | 228(97.0) | 7(3.0) | |||
6–10 | 137(89.5) | 16(10.5) | |||
≥ 11 | 451(82.6) | 95(17.4) |
Sexual behavior and condom use among MSM during the past 6 months
Table 3 shows that in the past 6 months, the majority role of anal sex behaviors among participants were versatile, while the HIV positive rate were highest (χ2 = 14.92, P = 0.001). HIV positive rate increased with the frequency of condom use decreased from consistent use to never use in anal sex with men (trend χ2 = 44.36, P < 0.001). HIV positive rate decreased with the number of oral sex partner increased (trend χ2 = 24.60, P < 0.001), in terms of the frequency of condom use in oral sex, the HIV positive rate were highest among the participants who never use condom, but there was no significant difference (P = 0.754). 115 (12.3%) MSM ever had group sex, while the HIV positive rate was higher than those who never had group sex (χ2 = 30.65, P < 0.001). 31.0% participants had non-steady sex partner with a higher HIV positive rate (20.7%, χ2 = 24.73, P < 0.001). Only 3 (0.3%) participants had use illicit drugs in the sex with men, but 2 of them were confirmed HIV positive (P = 0.044), and HIV positive rate was higher in participants who self-reported aware of partner’s sexually transmitted diseases (STDs) status before sex (χ2 = 13.49, P < 0.001). The results of the univariate logistic regression analysis are consistent with the results of the chi-square analysis, except for age, see Supplementary material 2.
Table 3
Sexual behavior and condom use among MSMa in the past 6 months in Maanshan, China
Variable | HIV-negative [n (%)] | HIV-positive [n (%)] |
χ
2
| P-value | |
|---|---|---|---|---|---|
Total | 816(87.4) | 118(12.6) | |||
Sex role in male anal sex | 14.92b | 0.001 | |||
Insertive | 179(95.7) | 8(4.3) | |||
Receptive | 137(87.3) | 20(12.7) | |||
Versatile | 469(85.0) | 83(15.0) | |||
Number of anal sex partner | 2.30b | 0.317 | |||
0 | 31(81.6) | 7(18.4) | |||
1–5 | 746(87.4) | 108(12.6) | |||
≥ 6 | 39(92.9) | 3(7.1) | |||
Condom use in anal sex with men | 62.43b 44.36d | < 0.001 < 0.001 | |||
Consistent | 37(97.4) | 1(2.6) | |||
Often | 90(94.7) | 5(5.3) | |||
Sometimes | 379(94.5) | 22(5.5) | |||
Never | 279(77.1) | 83(22.9) | |||
Sex role in male oral sex | 1.08b | 0.570 | |||
Insertive | 22(95.7) | 1(4.3) | |||
Receptive | 35(89.7) | 4(10.3) | |||
Versatile | 723(87.4) | 104(12.6) | |||
Number of oral sex partner | 26.31b 24.60d | < 0.001 < 0.001 | |||
0 | 36(80.0) | 9(20.0) | |||
1–2 | 459(83.5) | 91(16.5) | |||
≥ 3 | 321(94.7) | 18(5.3) | |||
Condom use in oral sex with men | -c | 0.754 | |||
Consistent | 8(100.0) | 0(0.0) | |||
Often | 9(100.0) | 0(0.0) | |||
Sometimes | 13(92.9) | 1(7.1) | |||
Never | 750(87.4) | 108(12.6) | |||
Commercial sex with men (Yes) | 50(94.3) | 3(5.7) | 2.48b | 0.116 | |
Sexual intercourse with women (Yes) | 426(87.8) | 59(12.2) | 0.20b | 0.654 | |
Group sex with men (Yes) | 82(71.3) | 33(28.7) | 30.65b | < 0.001 | |
Non-steady sex partners (Yes) | 230(79.3) | 60(20.7) | 24.73b | < 0.001 | |
Illicit drug use during sex with men (Yes) | 1(33.3) | 2(66.7) | -c | 0.044 | |
Aware of partner’s STDse status (including HIV-negative and HIV-positive status) before sex (Yes) | 213(81.0) | 50(19.0) | 13.49b | < 0.001 | |
Using condom when having sex without knowing the STDs status of male partner (Yes) | 762(87.0) | 114(13.0) | 2.81b | 0.094 |
Factors associated with HIV infection in MSM
As show in Table 4, the results of the Poisson model found that the OR increased with scope of sex partner distribution (OR = 1.78, 95% CI: 1.36–2.33, P < 0.001) and number of male sexual partners increased (OR = 2.11, 95% CI: 1.47–3.02, P < 0.001), participants who had group sex (OR = 2.53, 95% CI: 1.06–5.17, P = 0.035) and non-steady sex partners in the past 6 months (OR = 2.14, 95% CI: 1.56–2.93, P < 0.001) had higher risk of HIV infection, meanwhile, the OR decreased with monthly income (OR = 0.68, 95% CI: 0.57–0.82, P < 0.001), education level (OR = 0.79, 95% CI: 0.66–0.95, P = 0.011), condom use in anal sex with men (OR = 0.53, 95% CI: 0.35–0.81, P = 0.003) and number of oral sex partner (OR = 0.35, 95% CI: 0.24–0.51, P < 0.001) in the past 6 months increased. Compared to the students, freelancer and other occupation had higher risk to infect HIV (all P < 0.05). The participants whose role of anal sex with men was receptive (OR = 2.54, 95% CI: 1.25–5.13, P = 0.010) and versatile (OR = 2.34, 95% CI: 1.31–4.19, P = 0.004) in the past 6 months had higher risk compared to the insertive ones. The results of the multivariate logistic regression analysis are consistent with the results of the Poisson regression model, except for the occupation “laborer”, age, education level and number of MSM friends, see Supplementary material 3.
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Table 4
Poisson regression analysis of factors associated with HIV infection among MSMa in Maanshan, China
Variable |
β
| SE | Wald | P-value | ORb (95% CIc) |
|---|---|---|---|---|---|
Age (years old) | 0.015 | 0.010 | 2.517 | 0.113 | 1.02(1.00-1.04) |
Education level | |||||
Increase from low level to higher | -0.238 | 0.090 | 6.414 | 0.011 | 0.79(0.66–0.95) |
Occupation (Reference: student) | |||||
Farmer | -0.743 | 1.111 | 0.447 | 0.504 | 0.48(0.05–4.20) |
Laborer | 0.683 | 0.366 | 3.476 | 0.062 | 1.98(0.97–4.06) |
Public institutions | 0.353 | 0.523 | 0.455 | 0.500 | 1.42(0.51–3.97) |
Freelancer | 1.391 | 0.366 | 14.479 | < 0.001 | 4.02(1.96–8.23) |
Others | 1.098 | 0.414 | 7.031 | 0.008 | 3.00(1.33–6.75) |
Monthly income (yuan/RMB) | |||||
Increase from small number to bigger | -0.384 | 0.092 | 17.605 | < 0.001 | 0.68(0.57–0.82) |
Scope of sex partner distribution | |||||
Increase from small area to bigger | 0.575 | 0.138 | 17.478 | < 0.001 | 1.78(1.36–2.33) |
Number of MSM friends | |||||
Increase from small number to bigger | 0.326 | 0.197 | 2.744 | 0.098 | 1.39(0.94–2.04) |
Ever had group sex (Reference: no) | 0.853 | 0.404 | 4.464 | 0.035 | 2.35(1.06–5.17) |
The role of anal sex with men in the past 6 months (Reference: insertive) | |||||
Receptive | 0.930 | 0.360 | 6.693 | 0.010 | 2.54(1.25–5.13) |
Versatile | 0.852 | 0.297 | 8.246 | 0.004 | 2.34(1.31–4.19) |
Condom use in anal sex with men in the past 6 months | |||||
Increase from never use to consistent use | -0.637 | 0.217 | 8.648 | 0.003 | 0.53(0.35–0.81) |
Number of oral sex partner in the past 6 months | |||||
Increase from small number to bigger | -1.061 | 0.195 | 29.670 | < 0.001 | 0.35(0.24–0.51) |
Non-steady sex partners in the past 6 months (Reference: no) | 0.760 | 0.160 | 22.447 | < 0.001 | 2.14(1.56–2.93) |
Number of male sexual partners | |||||
Increase from small number to bigger | 0.744 | 0.185 | 16.225 | < 0.001 | 2.11(1.47–3.02) |
Illicit drug use during sex with men (Reference: no) | 2.123 | 0.747 | 8.078 | 0.004 | 8.36(1.93–36.14) |
Discussion
This study investigated HIV infection, sexual behavior and associated factors among MSM population in Maanshan City. Previous studies showed that the rate of HIV infection among MSM was 3.5% in Maanshan City in 2012 [14]. The prevalence of HIV was 12.6% (118/934) in this survey, suggesting a marked increase in the HIV prevalence among MSM in Maanshan City in recent years. And the rate of HIV infection in the study was much higher than that of Shandong Province (2.99%) [16] and Fuyang City (5.7%), Anhui Province [17].
In our survey, the average age of participants was 30.5 years and most of the them were young MSM. But the multivariate analysis found that the risk of HIV infection did not gradually increase with increasing age, contrary to findings from other studies showing a higher incidence of HIV in younger MSM [18]. In addition, our study showed that freelancers had higher risk for HIV infection in MSM, which was consistent with finding of Longshuo [19], possibly because of the flexible and less constrained working hours of these occupations.
The present study found that 77.3% of the participants had been found sexual partners through the Internet/dating Apps, which was higher than that (60%) of MSM in Shenyang, China [20]. More and more MSM were looking for sexual partners through the Internet, which may increases the number of sexual partners [8, 20]. Although the number of MSM friends was not an influencing factor for HIV infection in this study, the number of male sex partners and scope of sex partner distribution were risk factors for infection with HIV. The distribution of sexual partners affects the occurrence and transmission range of dangerous behaviors during HIV epidemics, and is a huge challenge for HIV prevention.
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About 69.5% of the known HIV transmission routes were associated with sexual behavior in MSM [21]. HIV is mainly transmitted through anal sex among MSM, because it is easy to bleed due to large anal friction during anal sex. Thus, particular modes of sexual behavior increase the risk of HIV infection than in the general population [22]. 99.6% of participants had anal sexual behavior in this survey. What’s more, participants whose role of sex was receptive and versatile were more likely to be infected with HIV than insertive ones, which was confirmed with many findings [23‐25]. Besides, 12.3% participants ever had group sex in this survey, and our finding showing a higher positive rate of HIV with ever had group sex. Sex, especially unprotected sex with multiple male partners, was a major risk factor infection with HIV for MSM, and it was important for comprehensive intervention based on risk factors [6, 7]. Furthermore, group sex will increase the risk for HIV infection significantly due to its field specificity and uncontrollability and accelerate the transmission of HIV among MSM [26].
Only 14.8% of MSM consistent used or often used condoms in our study. Unprotected anal sex was a high-risk practice for HIV transmission, and the correct use of condoms can prevent transmission of HIV effectively [27, 28]. The propaganda about correct condom-using among MSM should be strengthened in order to prevent HIV infection themselves in the future. Condom promotion in high-risk population is an effective measure to control and prevent the sexual transmission of HIV, but also an effective means of AIDS prevention and treatment with lower investment and higher income. Besides, intervention efforts targeting MSM should focus not only on the promotion of condom use, but also on changing risky behaviors, in particular, reducing number of non-steady sex partners and their distribution range, and intensive testing of high-risk groups, coupled with the immediate use of antiretroviral treatment (ART) and pre-exposure prophylaxis (PrEP) program, may reduce the prevalence of HIV [29].
Limitations
There are some limitations in this study. Firstly, this study was a cross-sectional study, which precludes any conclusions on causality. Secondly, the results could only reflect the characteristics and conditions of MSM in Maanshan during the survey, which may not be generalized to the greater population of MSM. Thirdly, drug use was defined as use illegal drugs in this study, such as injction heroin or direct smoking of marijuana, etc. Some new drugs were not on the illegal list such as Rush were not included in our definition of drug use, which may be the main reason why only three participants used illicit drugs. In addition, this study specifically mentioned whether the participants used illicit drugs while having sex with men, rather than in general, which may narrow the scope further.
Conclusions
The prevalence of HIV in MSM in Maanshan had been increasing rapidly in recent years. Our study confirmed some factors that were associated with an increased risk of sexual transmission of HIV infection in MSM, and reasonable control of the risk factors can effectively reduce the incidence of HIV in MSM.
Acknowledgements
We thank the public welfare linkage research program of Anhui Science and technology department and key project of natural science research in Universities of Anhui Province for supporting this study. We would like to thank all of the project actors who participated in investigation and provided information and data, and the Blue-Heart working group, who assisted in the data collection for the study.
Declarations
Ethics approval and consent to participate
The study protocol was approved by the Biomedical Ethics Committee of Anhui Medical University (approval number 20150114). Written informed consent was obtained from all of the participants in the study.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
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