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Prevalence and associated factors of HIV self-testing among men who have sex with men in Ningbo, China: a cross-sectional study

Prevalence and associated factors of HIV self-testing among men who have sex with men in Ningbo,... Background: HIV testing and early linkage to care are critical for reducing the risk of HIV transmission. HIV self‑testing (HIVST ) is a useful tool for increasing HIV testing frequency.This study aimed to investigate HIVST rates among men who have sex with men (MSM), the characteristics of MSM who had HIVST, and factors associated with HIVST uptake among MSM in Ningbo, China. Methods: A cross‑sectional study was conducted from April to October 2019 in Ningbo,China. Participants were aged at least 18 years and having had sexual contact with men in the past year. Proportions were used for categorical variables. Adjusted Odds Ratio (AOR) and 95% Confidence Interval (CI) for characteristics associated with HIVST uptake was processed by multivariable logistic regression models. Results: Among a sample of 699 MSM recruited, 38.2% had reported previous use of an HIV self‑test kit. A greater proportion of HIVST users had a higher frequency of HIV testing (≥ 2 times: 70.0% versus 41.2%, p < 0.001) in the past 1 year. The odds of older age (30–39 years: AOR = 0.49, CI 0.32–0.76; more than 40 years: AOR = 0.07, CI 0.04–0.14, compared to 18–29 years), bisexual (AOR = 0.49, CI 0.29–0.84) were lower among HIVST users,and were higher among MSM who were higher education level (high school: AOR = 2.82, CI 1.70–4.69, compared to middle school or less), gay apps use (AOR = 1.86, CI 1.13–3.05), multiple male sex partners (AOR = 1.90, CI 1.29–2.80), frequency of male–male sexual contact ≥ 1 times per week (AOR = 1.86, CI 1.30–2.66), syphilis infection (AOR = 5.48, CI 2.53–11.88). Conclusions: Further HIVST education should be strengthened for school‑aged children and teenagers, and free HIVST kits may be provided to high‑risk MSM through gay apps and CBO to achieve the increased HIV testing frequency. Keywords: MSM, HIV self‑testing, Gay apps, Associated factors, China group of HIV acquisition [2, 3]. MSM accounted for an Introduction estimated 17% of new HIV infections globally, includ- Globally, there were an estimated 37.9 million people ing more than half of new HIV infections in western and are living with HIV (PLWH), with about 1.7 million peo- central Europe and North America [4]. MSM was about ple newly infected with HIV at the end of 2018 [1]. Men 28 times more likely to be living with HIV than it was who have sex with men (MSM) has become the high-risk among all adult men in 2018 [5]. To end the AIDS epidemic by 2030, the "90-90-90" *Correspondence: donghj@nbcdc.org.cn; shenyl26@163.com goal by 2020 set up by UNAIDS in 2014 (90% of people Ningbo Municipal Center for Disease Control and Prevention, 237 with HIV infection diagnosed, 90% of people diagnosed Yongfeng Road, Ningbo 315010, Zhejiang, China on treatment, and 90% of people on treatment achieving Zhejiang Provincial Institute of Dermatology, 61 Wuyuan Road, Deqing 313200, Zhejiang, China virological suppression) [6]. However, it seems unlikely © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Hong et al. AIDS Res Ther (2021) 18:14 Page 2 of 8 that many regions and countries would reach the target, Questionnaire especially the first 90% [7]. In China, an estimated less All data were collected through self-administered paper than 70% of PLWH were aware of their HIV-positive sta- questionnaires by trained project workers. The follow - tus by the end of 2018 [8]. HIV testing and early linkage ing variables were included: (1) demographic information to care were critical for reducing the risk of viral trans- including age, marital status, education level, duration of mission from infected persons However, key population local residence, monthly income, and sexual orientation; groups including MSM were unwilling to seek voluntary (2) gay apps (Blued, Jack’d, and ZANK) use including HIV counseling and testing (VCT) in the hospital or duration and frequency of apps use; (3) Sexual behaviors Centers for Disease Control and Prevention (CDC) due including role and frequency in sexual intercourse, mul- to stigma and discrimination [9–11]. tiple male sex partners, unprotected sex with men and HIV self-testing (HIVST) had recommended being syphilis infection in the past 6  months; (4) HIV testing offered as an additional HIV testing approach by WHO including reasons for test, frequency of test, time since in 2016 [12]. Testers take their blood sample to per- latest test and site of the latest test; (5) HIVST including form HIV rapid tests and interpret the result at the time self-reported used HIVST in the lifetime (HIVST users), and location of their choosing. Several studies showed the type of HIVST kit,way to receive HIVST kit. that HIVST had generally high sensitivity and specific - ity and was an acceptable and feasible testing approach Statistical analysis due to the convenience, privacy, and ease of use [13–15]. Characteristics of all participants were described by cat- These characteristics make it a potentially useful tool for egorical variables presented as absolute values and per- increasing testing frequency and easy to reach first time centages. The demographic information, gay apps use, and repeat testers for HIV [16, 17]. In China, HIVST is sexual behaviors and HIV testing compared between highly acceptable and easily available through drugstore, HIVST users and Non-HIVST users were examined by e-commerce platform and community-based organisa- chi-square tests. Univariate and multivariable forward tions (CBO) [18]. stepwise logistic regression models were performed to Given the need to improve HIV testing rates and target examine risk factors associated with HIVST. The statis - the first of the United Nation’s 90-90-90 HIV testing and tical significance was defined as P < 0.05. All statistical treatment goals, the purpose of this study was to inves- analyses were performed in SPSS (version 21.0, IBM, tigate HIVST uptake rates among MSM, the character- Armonk, NY, USA). istics and factors associated with HIVST uptake among MSM in Ningbo, China. Ethical considerations This study protocol was reviewed and approved by the Methods Institutional Review Board of the Ningbo CDC. Informed Study design and participants consent was asked to sign for all eligible participants We conducted a cross-sectional survey from April 1 when the survey was starting. Participants could receive to October 30, 2019, in Ningbo. Ningbo is an eastern a gift for prizes of up to 50 Chinese Yuan (CNY) upon the coastal city of China, nearby Shanghai, with an area of completion of the survey. 9365  km and a population of approximately 8.54 mil- lion people. HIV prevalence among MSM in Ningbo Results was 5.7% [19].Convenience sampling of participants was Participant characteristics recruited through a combined online and offline method. Table 1 demonstrates the characteristics of the 699 MSM Flyer advertisements were posted in MSM venues (Three in Ningbo. The mean age was 31.9 (SD 8.8) years. Most parks, two bars, and eight community events) and VCT participants (81.1%) were less than 30  years, 63.4% were clinic,as well as on gay websites and gay apps. The crite - single, 70.4% had a high school education or above, 77.7% ria for recruiting were (1) being male, (2) aged at least18 had lived in Ningbo for at least 2  years, 62.9% had an years, (3) having resided in Ningbo for at least 6 months, income above 5000 CNY per month, and 74.8% self-iden- (4) having had sexual contact with men in the past year. tified as gay. Interested MSM contacted trained project work- Most participants (83.4%) had used gay apps in the past ers for assessment of eligibility. After providing written 6 months. Of the 583 gay app users, 85.8% (500/583) had informed consent, eligible participants were asked to used gay apps for at least 1  year, 56.9% (332/583) used complete self-administered questionnaires. Project work- them at least 5 times a day. In terms of sexual practice, ers were instructed to check questionnaires in place to half of the participants were engaged in both insertive ensure collection of quality data. anal intercourse and receptive anal intercourse equally. 46.1% had sex with men for at least once per week in the Hong  et al. AIDS Res Ther (2021) 18:14 Page 3 of 8 Table 1 Characteristics of study participants and of HIVST users and Non‑HIVST users in Ningbo, China, 2019 Characteristics All participants Subgroup comparison n (%) HIVST users Non‑HIVST users P‑ value n (%) n (%) Overall 699 (100) 267 (100) 432 (100) Demographics Age (years) 18 ~ 330 (47.2) 155 (58.1) 175 (40.5) < 0.001 30 ~ 237 (33.9) 92 (34.5) 145 (33.6) ≥ 40 132 (18.9) 20 (7.5) 112 (25.9) Marital status Single 443 (63.4) 172 (64.4) 271 (62.7) 0.653 Married 256 (36.6) 95(35.6) 161 (37.3) Education level Middle school or less 207 (29.6) 65 (24.3) 142 (32.9) 0.022 High school 264 (37.8) 101 (37.8) 163 (37.7) College or above 228 (32.6) 101 (37.8) 127 (29.4) Duration of local residence (years) < 2 156 (22.3) 76 (28.5) 80 (18.5) 0.002 ≥ 2 543 (77.7) 191 (71.5) 352 (81.5) Monthly income (CNY ) < 5000 259 (37.1) 74 (27.7) 185 (42.8) < 0.001 ≥ 5000 440 (62.9) 193 (72.3) 247 (57.2) Sexual orientation Gay 523 (74.8) 220 (82.4) 303 (70.1) 0.001 Bisexual 135 (19.3) 34 (12.7) 101 (23.4) Unknown/unsure 41 (5.9) 13 (4.9) 28 (6.5) Gay apps usage Gay apps use Yes 583 (83.4) 237 (88.8) 346 (80.1) 0.003 No 116 (16.6) 30 (11.2) 86 (19.9) Duration of gay apps use (years) < 1 83 (14.2) 25 (10.5) 58 (16.8) 0.035 ≥ 1 500 (85.8) 212 (89.5) 288 (83.2) Missing (No use of gay apps) 116 Frequency of gay apps use (times/day) < 1 66 (11.3) 22 (9.3) 44 (12.7) 0.036 1‑ 185 (31.7) 65 (27.4) 120 (34.7) ≥ 5 332 (56.9) 150 (63.3) 182 (52.6) Missing (No use of gay apps) 116 Sexual behavior Role in sexual intercourse Insertive anal sex 191 (27.3) 74 (27.7) 117 (27.1) 0.983 Receptive anal sex 155 (22.2) 59 (22.1) 96 (22.2) Both 353 (50.5) 134 (50.2) 219 (50.5) Frequency of male–male sexual contact (times/week) < 1 377 (53.9) 124 (46.4) 253 (58.6) 0.002 ≥ 1 322 (46.1) 143 (53.6) 179 (41.4) Multiple male sex partners Yes 196 (28.0) 87 (32.6) 109 (25.2) 0.035 No 503 (72.0) 180 (67.4) 323 (74.8) Hong et al. AIDS Res Ther (2021) 18:14 Page 4 of 8 Table 1 (continued) Characteristics All participants Subgroup comparison n (%) HIVST users Non‑HIVST users P‑ value n (%) n (%) Unprotected sex with men Yes 190 (27.2) 64 (24.0) 126 (29.2) 0.133 No 509 (72.8) 203 (76.0) 306 (70.8) Syphilis Infection Yes 44 (6.3) 29 (10.9) 15 (3.5) < 0.001 No 655 (93.7) 238 (89.1) 417 (96.5) HIV testing Reason for HIV testing Regular HIV testing 432 (71.5) 196 (73.4) 236 (70.0) 0.011 Had unprotected sexual behavior 60 (9.9) 22 (8.2) 38 (11.3) Had suspicions symptoms of AIDS 47 (7.8) 19 (7.1) 28 (8.3) Awareness of HIV testing results before sex 36 (6.0) 10 (3.7) 26 (7.7) Repeated HIV testing 29 (4.8) 20 (7.5) 9 (2.7) Missing(Had never HIV testing before) 95 Frequency of HIV testing 0 114 (16.3) 4 (1.5) 110 (25.5) < 0.001 1 220 (31.5) 76 (28.5) 144 (33.3) ≥ 2 365 (52.2) 187 (70.0) 178 (41.2) Time since latest HIV testing (months) 1 ~ 148 (24.5) 81 (30.3) 67 (19.9) 0.005 4 ~ 176 (29.1) 77 (28.8) 99 (29.4) 7 ~ 92 (15.2) 29 (10.9) 63 (18.7) 13 ~ 188 (31.1) 80 (30.0) 108 (32.0) Missing(Had never HIV testing before) 95 Site of the latest HIV testing CDC 211 (34.9) 85 (31.8) 126 (37.4) 0.029 Hospital 43 (7.1) 13 (4.9) 30 (8.9) NGO 304 (50.3) 169 (63.3) 181 (53.4) Missing (Had never HIV testing before) 95 In the prior 6 months In the prior one year Subgroups were compared using chi-square tests to generate P- prior 6  months.72.0% had multiple male sex partners p < 0.001), had college or above education level (37.8% and 27.2% had unprotected sex with men in the prior versus 29.4%, p = 0.022), had lived in Ningbo less than 6 months. 2  years (28.5% versus 18.5%, p = 0.002), had an income above 5000 China Yuan (CNY) per month (72.3% versus Comparisons of characteristics between HIVST users 57.2%, p < 0.001) and self-identified as gay (82.4% versus and Non‑HIVST users 70.1%, p < 0.001). Among all participants, 604 (86.4%) reported having HIV A larger proportion of HIVST users reported having testing at least once in their lifetimes, and 575 (82.3%) higher frequency of male-male sexual contact (≥ 1 time/ had been tested in the past year. Table  1 describes that week: 53.6% versus 41.4%, p = 0.002), having multiple a total of 267 participants of (699, 38.2%) reported hav- male sex partners (32.6% versus 25.2%, p = 0.035), having ing used an HIV self-test kit before, whereas 432 (61.8%) had syphilis infection (10.9% versus 3.5%, p < 0.001) and reported never having HIV self-test. Compared to non- having used gay apps (88.8% versus 80.1%, p = 0.003) in HIVST users, a larger proportion of HIVST users were the prior 6 months. Among those who had used gay apps, aged between 18 and 29  years (58.1% versus 40.5%, a greater proportion of HIVST users also had a higher Hong  et al. AIDS Res Ther (2021) 18:14 Page 5 of 8 health education for school-age children and teenagers frequency of gay apps use (≥ 5 times/day: 63.3% versus [23]. 52.6%, p = 0.036) in the prior 6 months and used gay apps Gay apps were very popular among MSM in China [19]. over 1 year (89.5% versus 83.2%, p = 0.035). HIV prevention through gay apps was widely applied A greater proportion of HIVST users had a higher toward reducing high-risk behaviors and promoting HIV frequency of HIV testing (≥ 2 times: 70.0% versus testing [26, 27]. Our results showed that HIVST users 41.2%, p < 0.001) in the past 1  year. Among those who had a higher frequency of gay apps use than Non-HIVST had HIV testing before, a greater proportion of HIVST users in the prior 6  months. As with previous findings, users reported having HIV testing regularly (73.4% ver- the utility of mobile health interventions can engage sus 70.0%, p = 0.011), their most recent HIV testing had MSM in HIVST in Heifei and Shenzhen, China [28, been within the prior 3  months (30.3% versus 19.9%, 29], and increase rates of confirmed HIV diagnoses and p = 0.005), the site of latest HIV testing was CBO (63.3% linkage to clinical care in the UK [30]. It indicated that versus 53.4%, p = 0.029). HIVST kits usage and offer can be conducted as a part of HIV prevention through gay apps to access to more high- Factor associated with HIVST uptake risk populations in China. As show in Table  2, multivariable logistic regres- Furthermore, consistent with findings in other stud - sion analyses found that the odds of older age (30– ies [24], those who had high-risk sex behavior, includ- 39  years: AOR = 0.49, CI 0.32–0.76; more than 40  years: ing multiple male sex partners, frequency of male-male AOR = 0.07, CI 0.04–0.14, compared to 18–29  years), sexual contact more than once per week and syphilis bisexual (AOR = 0.49, CI 0.29–0.84) were lower among infection were more likely to have had HIVST. It is pos- HIVST users,and were higher among MSM who were sible that commercial HIVST kits can be easily bought higher education level (high school: AOR = 2.82, CI by online shopping platform in China. These high-risk 1.70–4.69, compared to middle school or less), gay apps MSM would be willingness to pay for HIVST kits instead use (AOR = 1.86, CI 1.13–3.05), multiple male sex part- of testing in the hospital [24]. But to avoid possible cost ners (AOR = 1.90, CI 1.29–2.80), frequency of male–male barriers, free HIVST kits might be provided to high-risk sexual contact ≥ 1 times per week (AOR = 1.86, CI 1.30– populations to achieve the increased testing f requency . 2.66), syphilis infection (AOR = 5.48, CI 2.53–11.88). This study demonstrated that HIVST users were more like to have a higher frequency of HIV testing and regu- Discussion lar HIV testing compared to non-HIVST users. Regular Globally, HIV testing had become an important strat- HIV testing enables early identification and treatment egy to end the HIV epidemic [20, 21]. HIVST is reliable, of HIV among at-risk MSM [31]. As mentioned, the US safe, and accurate, which can help increase serostatus CDC recommends MSM to take up HIV testing every awareness and ultimately linkage-to-care or prevention 3–6 months if they have additional HIV risk factors [32]. services among HIV high-risk populations [22, 23]. The But most of these MSM have no HIV testing routines proportion of HIV testing among MSM in the lifetimes [33]. So some HIV interventions should be improved and the past year in our analysis was higher than in other to encourage MSM to use HIVST regular after VCT or studies, but there is a certain distance to reach the first HIV risk assessment. The results also showed that two- 90% targets by 2020 [7, 21]. The study revealed that 38.2% thirds of MSM received HIVST kits form CBO in the lat- of MSM had used HIVST before in Ningbo, which was est HIV testing. This indicated that CBO had become an lower than the rates reported in studies from other areas important role in HIV intervention in China. So the gov- [24, 25]. The reasons for the relatively low HIVST rate ernment might strengthen support to CBO to promote in our study could be related to the lack of inventions HIVST uptake. to promote HIVST by Ningbo CDC. Our study’s con- tribution to investigate factors associated with HIVST and help the government develop targeted strategies to Limitations improve HIV testing among MSM in China. The present study had several limitations. First, par- Our study showed that those MSM who were younger ticipants were relatively high-educated, had higher or high education levels were more likely to have had income, and our findings may not be generalizable in HIVST. It is possible that younger MSM had more wor- other contexts or settings. Second, some questions ries about positive test results [11]. Worldwide, about were asked in the prior 6  months. Despite imple- 32% of new HIV infections among adults aged 15  years mented quality control measures, recall and social and older have occurred in youth ages 15–24  years in desirability bias might have existed.Third, this was 2018 [4]. Therefore, HIVST education should be included not a representative sample of the MSM population in as a part of comprehensive sexual and reproductive Ningbo, because only those who had a willingness and Hong et al. AIDS Res Ther (2021) 18:14 Page 6 of 8 Table 2 Factors associated with HIVST among study participants in Ningbo, China, 2019 (n = 699) Factor Unadjusted P‑ value Adjusted P‑ value b b OR (CI) OR (CI) Age (years) 18 ~ 1.00 1.00 30 ~ 0.72 (0.51–1.01) 0.054 0.49 (0.32–0.76) 0.001 ≥ 40 0.20 (0.12–0.34) < 0.001 0.07 (0.04–0.14) < 0.001 Marital status Married 1.00 – Single 1.08 (0.78–1.48) 0.653 – – Education level Middle school or less 1.00 1.00 High school 1.74 (1.17–2.57) 0.006 2.82 (1.70–4.69) < 0.001 College or above 1.35 (0.92–1.99) 0.123 1.42 (0.92–2.20) 0.052 Local residence time < 2 1.00 1.00 2 0.57 (0.40–0.82) 0.002 0.66 (0.44–1.00) 0.052 Monthly income (CNY ) < 5000 1.00 1.00 ≥ 5000 1.95 (1.41–2.71) < 0.001 1.35 (0.94–1.93) 0.100 Sexual orientation Gay 1.00 1.00 Bisexual 0.46 (0.30–0.71) < 0.001 0.49 (0.29–0.84) 0.009 Unknown/unsure 0.64(0.32–1.26) 0.198 0.71 (0.34–1.51) 0.379 Gay apps use No 1.00 1.00 Yes 1.96 (1.26–3.07) 0.003 1.86 (1.13–3.05) 0.014 Multiple male sex partners No 1.00 1.00 Yes 1.43 (1.02–2.00) 0.036 1.90 (1.29–2.80) 0.001 Frequency of male–male sexual contact (times/week) < 1 1.00 1.00 ≥ 1 1.63 (1.20–2.22) 0.002 1.86 (1.30–2.66) 0.001 Unprotected sex with men No 1.00 – Yes 0.77 (0.54–1.09) 0.134 – – Syphilis infection No 1.00 1.00 Yes 3.39 (1.78–6.45) < 0.001 5.48 (2.53–11.88) < 0.001 In the prior 6 months Univariate and multivariate regression analyses were used to generate odds ratios (ORs) and 95% confidence intervals (CIs) contacted trained project workers could be recruited Conclusions into the study.Finally, as this was a cross-sectional The coverage of HIVST had a significant gap in Ningbo, study, we are unable to establish a causal relationship. 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Prevalence and associated factors of HIV self-testing among men who have sex with men in Ningbo, China: a cross-sectional study

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Abstract

Background: HIV testing and early linkage to care are critical for reducing the risk of HIV transmission. HIV self‑testing (HIVST ) is a useful tool for increasing HIV testing frequency.This study aimed to investigate HIVST rates among men who have sex with men (MSM), the characteristics of MSM who had HIVST, and factors associated with HIVST uptake among MSM in Ningbo, China. Methods: A cross‑sectional study was conducted from April to October 2019 in Ningbo,China. Participants were aged at least 18 years and having had sexual contact with men in the past year. Proportions were used for categorical variables. Adjusted Odds Ratio (AOR) and 95% Confidence Interval (CI) for characteristics associated with HIVST uptake was processed by multivariable logistic regression models. Results: Among a sample of 699 MSM recruited, 38.2% had reported previous use of an HIV self‑test kit. A greater proportion of HIVST users had a higher frequency of HIV testing (≥ 2 times: 70.0% versus 41.2%, p < 0.001) in the past 1 year. The odds of older age (30–39 years: AOR = 0.49, CI 0.32–0.76; more than 40 years: AOR = 0.07, CI 0.04–0.14, compared to 18–29 years), bisexual (AOR = 0.49, CI 0.29–0.84) were lower among HIVST users,and were higher among MSM who were higher education level (high school: AOR = 2.82, CI 1.70–4.69, compared to middle school or less), gay apps use (AOR = 1.86, CI 1.13–3.05), multiple male sex partners (AOR = 1.90, CI 1.29–2.80), frequency of male–male sexual contact ≥ 1 times per week (AOR = 1.86, CI 1.30–2.66), syphilis infection (AOR = 5.48, CI 2.53–11.88). Conclusions: Further HIVST education should be strengthened for school‑aged children and teenagers, and free HIVST kits may be provided to high‑risk MSM through gay apps and CBO to achieve the increased HIV testing frequency. Keywords: MSM, HIV self‑testing, Gay apps, Associated factors, China group of HIV acquisition [2, 3]. MSM accounted for an Introduction estimated 17% of new HIV infections globally, includ- Globally, there were an estimated 37.9 million people ing more than half of new HIV infections in western and are living with HIV (PLWH), with about 1.7 million peo- central Europe and North America [4]. MSM was about ple newly infected with HIV at the end of 2018 [1]. Men 28 times more likely to be living with HIV than it was who have sex with men (MSM) has become the high-risk among all adult men in 2018 [5]. To end the AIDS epidemic by 2030, the "90-90-90" *Correspondence: donghj@nbcdc.org.cn; shenyl26@163.com goal by 2020 set up by UNAIDS in 2014 (90% of people Ningbo Municipal Center for Disease Control and Prevention, 237 with HIV infection diagnosed, 90% of people diagnosed Yongfeng Road, Ningbo 315010, Zhejiang, China on treatment, and 90% of people on treatment achieving Zhejiang Provincial Institute of Dermatology, 61 Wuyuan Road, Deqing 313200, Zhejiang, China virological suppression) [6]. However, it seems unlikely © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Hong et al. AIDS Res Ther (2021) 18:14 Page 2 of 8 that many regions and countries would reach the target, Questionnaire especially the first 90% [7]. In China, an estimated less All data were collected through self-administered paper than 70% of PLWH were aware of their HIV-positive sta- questionnaires by trained project workers. The follow - tus by the end of 2018 [8]. HIV testing and early linkage ing variables were included: (1) demographic information to care were critical for reducing the risk of viral trans- including age, marital status, education level, duration of mission from infected persons However, key population local residence, monthly income, and sexual orientation; groups including MSM were unwilling to seek voluntary (2) gay apps (Blued, Jack’d, and ZANK) use including HIV counseling and testing (VCT) in the hospital or duration and frequency of apps use; (3) Sexual behaviors Centers for Disease Control and Prevention (CDC) due including role and frequency in sexual intercourse, mul- to stigma and discrimination [9–11]. tiple male sex partners, unprotected sex with men and HIV self-testing (HIVST) had recommended being syphilis infection in the past 6  months; (4) HIV testing offered as an additional HIV testing approach by WHO including reasons for test, frequency of test, time since in 2016 [12]. Testers take their blood sample to per- latest test and site of the latest test; (5) HIVST including form HIV rapid tests and interpret the result at the time self-reported used HIVST in the lifetime (HIVST users), and location of their choosing. Several studies showed the type of HIVST kit,way to receive HIVST kit. that HIVST had generally high sensitivity and specific - ity and was an acceptable and feasible testing approach Statistical analysis due to the convenience, privacy, and ease of use [13–15]. Characteristics of all participants were described by cat- These characteristics make it a potentially useful tool for egorical variables presented as absolute values and per- increasing testing frequency and easy to reach first time centages. The demographic information, gay apps use, and repeat testers for HIV [16, 17]. In China, HIVST is sexual behaviors and HIV testing compared between highly acceptable and easily available through drugstore, HIVST users and Non-HIVST users were examined by e-commerce platform and community-based organisa- chi-square tests. Univariate and multivariable forward tions (CBO) [18]. stepwise logistic regression models were performed to Given the need to improve HIV testing rates and target examine risk factors associated with HIVST. The statis - the first of the United Nation’s 90-90-90 HIV testing and tical significance was defined as P < 0.05. All statistical treatment goals, the purpose of this study was to inves- analyses were performed in SPSS (version 21.0, IBM, tigate HIVST uptake rates among MSM, the character- Armonk, NY, USA). istics and factors associated with HIVST uptake among MSM in Ningbo, China. Ethical considerations This study protocol was reviewed and approved by the Methods Institutional Review Board of the Ningbo CDC. Informed Study design and participants consent was asked to sign for all eligible participants We conducted a cross-sectional survey from April 1 when the survey was starting. Participants could receive to October 30, 2019, in Ningbo. Ningbo is an eastern a gift for prizes of up to 50 Chinese Yuan (CNY) upon the coastal city of China, nearby Shanghai, with an area of completion of the survey. 9365  km and a population of approximately 8.54 mil- lion people. HIV prevalence among MSM in Ningbo Results was 5.7% [19].Convenience sampling of participants was Participant characteristics recruited through a combined online and offline method. Table 1 demonstrates the characteristics of the 699 MSM Flyer advertisements were posted in MSM venues (Three in Ningbo. The mean age was 31.9 (SD 8.8) years. Most parks, two bars, and eight community events) and VCT participants (81.1%) were less than 30  years, 63.4% were clinic,as well as on gay websites and gay apps. The crite - single, 70.4% had a high school education or above, 77.7% ria for recruiting were (1) being male, (2) aged at least18 had lived in Ningbo for at least 2  years, 62.9% had an years, (3) having resided in Ningbo for at least 6 months, income above 5000 CNY per month, and 74.8% self-iden- (4) having had sexual contact with men in the past year. tified as gay. Interested MSM contacted trained project work- Most participants (83.4%) had used gay apps in the past ers for assessment of eligibility. After providing written 6 months. Of the 583 gay app users, 85.8% (500/583) had informed consent, eligible participants were asked to used gay apps for at least 1  year, 56.9% (332/583) used complete self-administered questionnaires. Project work- them at least 5 times a day. In terms of sexual practice, ers were instructed to check questionnaires in place to half of the participants were engaged in both insertive ensure collection of quality data. anal intercourse and receptive anal intercourse equally. 46.1% had sex with men for at least once per week in the Hong  et al. AIDS Res Ther (2021) 18:14 Page 3 of 8 Table 1 Characteristics of study participants and of HIVST users and Non‑HIVST users in Ningbo, China, 2019 Characteristics All participants Subgroup comparison n (%) HIVST users Non‑HIVST users P‑ value n (%) n (%) Overall 699 (100) 267 (100) 432 (100) Demographics Age (years) 18 ~ 330 (47.2) 155 (58.1) 175 (40.5) < 0.001 30 ~ 237 (33.9) 92 (34.5) 145 (33.6) ≥ 40 132 (18.9) 20 (7.5) 112 (25.9) Marital status Single 443 (63.4) 172 (64.4) 271 (62.7) 0.653 Married 256 (36.6) 95(35.6) 161 (37.3) Education level Middle school or less 207 (29.6) 65 (24.3) 142 (32.9) 0.022 High school 264 (37.8) 101 (37.8) 163 (37.7) College or above 228 (32.6) 101 (37.8) 127 (29.4) Duration of local residence (years) < 2 156 (22.3) 76 (28.5) 80 (18.5) 0.002 ≥ 2 543 (77.7) 191 (71.5) 352 (81.5) Monthly income (CNY ) < 5000 259 (37.1) 74 (27.7) 185 (42.8) < 0.001 ≥ 5000 440 (62.9) 193 (72.3) 247 (57.2) Sexual orientation Gay 523 (74.8) 220 (82.4) 303 (70.1) 0.001 Bisexual 135 (19.3) 34 (12.7) 101 (23.4) Unknown/unsure 41 (5.9) 13 (4.9) 28 (6.5) Gay apps usage Gay apps use Yes 583 (83.4) 237 (88.8) 346 (80.1) 0.003 No 116 (16.6) 30 (11.2) 86 (19.9) Duration of gay apps use (years) < 1 83 (14.2) 25 (10.5) 58 (16.8) 0.035 ≥ 1 500 (85.8) 212 (89.5) 288 (83.2) Missing (No use of gay apps) 116 Frequency of gay apps use (times/day) < 1 66 (11.3) 22 (9.3) 44 (12.7) 0.036 1‑ 185 (31.7) 65 (27.4) 120 (34.7) ≥ 5 332 (56.9) 150 (63.3) 182 (52.6) Missing (No use of gay apps) 116 Sexual behavior Role in sexual intercourse Insertive anal sex 191 (27.3) 74 (27.7) 117 (27.1) 0.983 Receptive anal sex 155 (22.2) 59 (22.1) 96 (22.2) Both 353 (50.5) 134 (50.2) 219 (50.5) Frequency of male–male sexual contact (times/week) < 1 377 (53.9) 124 (46.4) 253 (58.6) 0.002 ≥ 1 322 (46.1) 143 (53.6) 179 (41.4) Multiple male sex partners Yes 196 (28.0) 87 (32.6) 109 (25.2) 0.035 No 503 (72.0) 180 (67.4) 323 (74.8) Hong et al. AIDS Res Ther (2021) 18:14 Page 4 of 8 Table 1 (continued) Characteristics All participants Subgroup comparison n (%) HIVST users Non‑HIVST users P‑ value n (%) n (%) Unprotected sex with men Yes 190 (27.2) 64 (24.0) 126 (29.2) 0.133 No 509 (72.8) 203 (76.0) 306 (70.8) Syphilis Infection Yes 44 (6.3) 29 (10.9) 15 (3.5) < 0.001 No 655 (93.7) 238 (89.1) 417 (96.5) HIV testing Reason for HIV testing Regular HIV testing 432 (71.5) 196 (73.4) 236 (70.0) 0.011 Had unprotected sexual behavior 60 (9.9) 22 (8.2) 38 (11.3) Had suspicions symptoms of AIDS 47 (7.8) 19 (7.1) 28 (8.3) Awareness of HIV testing results before sex 36 (6.0) 10 (3.7) 26 (7.7) Repeated HIV testing 29 (4.8) 20 (7.5) 9 (2.7) Missing(Had never HIV testing before) 95 Frequency of HIV testing 0 114 (16.3) 4 (1.5) 110 (25.5) < 0.001 1 220 (31.5) 76 (28.5) 144 (33.3) ≥ 2 365 (52.2) 187 (70.0) 178 (41.2) Time since latest HIV testing (months) 1 ~ 148 (24.5) 81 (30.3) 67 (19.9) 0.005 4 ~ 176 (29.1) 77 (28.8) 99 (29.4) 7 ~ 92 (15.2) 29 (10.9) 63 (18.7) 13 ~ 188 (31.1) 80 (30.0) 108 (32.0) Missing(Had never HIV testing before) 95 Site of the latest HIV testing CDC 211 (34.9) 85 (31.8) 126 (37.4) 0.029 Hospital 43 (7.1) 13 (4.9) 30 (8.9) NGO 304 (50.3) 169 (63.3) 181 (53.4) Missing (Had never HIV testing before) 95 In the prior 6 months In the prior one year Subgroups were compared using chi-square tests to generate P- prior 6  months.72.0% had multiple male sex partners p < 0.001), had college or above education level (37.8% and 27.2% had unprotected sex with men in the prior versus 29.4%, p = 0.022), had lived in Ningbo less than 6 months. 2  years (28.5% versus 18.5%, p = 0.002), had an income above 5000 China Yuan (CNY) per month (72.3% versus Comparisons of characteristics between HIVST users 57.2%, p < 0.001) and self-identified as gay (82.4% versus and Non‑HIVST users 70.1%, p < 0.001). Among all participants, 604 (86.4%) reported having HIV A larger proportion of HIVST users reported having testing at least once in their lifetimes, and 575 (82.3%) higher frequency of male-male sexual contact (≥ 1 time/ had been tested in the past year. Table  1 describes that week: 53.6% versus 41.4%, p = 0.002), having multiple a total of 267 participants of (699, 38.2%) reported hav- male sex partners (32.6% versus 25.2%, p = 0.035), having ing used an HIV self-test kit before, whereas 432 (61.8%) had syphilis infection (10.9% versus 3.5%, p < 0.001) and reported never having HIV self-test. Compared to non- having used gay apps (88.8% versus 80.1%, p = 0.003) in HIVST users, a larger proportion of HIVST users were the prior 6 months. Among those who had used gay apps, aged between 18 and 29  years (58.1% versus 40.5%, a greater proportion of HIVST users also had a higher Hong  et al. AIDS Res Ther (2021) 18:14 Page 5 of 8 health education for school-age children and teenagers frequency of gay apps use (≥ 5 times/day: 63.3% versus [23]. 52.6%, p = 0.036) in the prior 6 months and used gay apps Gay apps were very popular among MSM in China [19]. over 1 year (89.5% versus 83.2%, p = 0.035). HIV prevention through gay apps was widely applied A greater proportion of HIVST users had a higher toward reducing high-risk behaviors and promoting HIV frequency of HIV testing (≥ 2 times: 70.0% versus testing [26, 27]. Our results showed that HIVST users 41.2%, p < 0.001) in the past 1  year. Among those who had a higher frequency of gay apps use than Non-HIVST had HIV testing before, a greater proportion of HIVST users in the prior 6  months. As with previous findings, users reported having HIV testing regularly (73.4% ver- the utility of mobile health interventions can engage sus 70.0%, p = 0.011), their most recent HIV testing had MSM in HIVST in Heifei and Shenzhen, China [28, been within the prior 3  months (30.3% versus 19.9%, 29], and increase rates of confirmed HIV diagnoses and p = 0.005), the site of latest HIV testing was CBO (63.3% linkage to clinical care in the UK [30]. It indicated that versus 53.4%, p = 0.029). HIVST kits usage and offer can be conducted as a part of HIV prevention through gay apps to access to more high- Factor associated with HIVST uptake risk populations in China. As show in Table  2, multivariable logistic regres- Furthermore, consistent with findings in other stud - sion analyses found that the odds of older age (30– ies [24], those who had high-risk sex behavior, includ- 39  years: AOR = 0.49, CI 0.32–0.76; more than 40  years: ing multiple male sex partners, frequency of male-male AOR = 0.07, CI 0.04–0.14, compared to 18–29  years), sexual contact more than once per week and syphilis bisexual (AOR = 0.49, CI 0.29–0.84) were lower among infection were more likely to have had HIVST. It is pos- HIVST users,and were higher among MSM who were sible that commercial HIVST kits can be easily bought higher education level (high school: AOR = 2.82, CI by online shopping platform in China. These high-risk 1.70–4.69, compared to middle school or less), gay apps MSM would be willingness to pay for HIVST kits instead use (AOR = 1.86, CI 1.13–3.05), multiple male sex part- of testing in the hospital [24]. But to avoid possible cost ners (AOR = 1.90, CI 1.29–2.80), frequency of male–male barriers, free HIVST kits might be provided to high-risk sexual contact ≥ 1 times per week (AOR = 1.86, CI 1.30– populations to achieve the increased testing f requency . 2.66), syphilis infection (AOR = 5.48, CI 2.53–11.88). This study demonstrated that HIVST users were more like to have a higher frequency of HIV testing and regu- Discussion lar HIV testing compared to non-HIVST users. Regular Globally, HIV testing had become an important strat- HIV testing enables early identification and treatment egy to end the HIV epidemic [20, 21]. HIVST is reliable, of HIV among at-risk MSM [31]. As mentioned, the US safe, and accurate, which can help increase serostatus CDC recommends MSM to take up HIV testing every awareness and ultimately linkage-to-care or prevention 3–6 months if they have additional HIV risk factors [32]. services among HIV high-risk populations [22, 23]. The But most of these MSM have no HIV testing routines proportion of HIV testing among MSM in the lifetimes [33]. So some HIV interventions should be improved and the past year in our analysis was higher than in other to encourage MSM to use HIVST regular after VCT or studies, but there is a certain distance to reach the first HIV risk assessment. The results also showed that two- 90% targets by 2020 [7, 21]. The study revealed that 38.2% thirds of MSM received HIVST kits form CBO in the lat- of MSM had used HIVST before in Ningbo, which was est HIV testing. This indicated that CBO had become an lower than the rates reported in studies from other areas important role in HIV intervention in China. So the gov- [24, 25]. The reasons for the relatively low HIVST rate ernment might strengthen support to CBO to promote in our study could be related to the lack of inventions HIVST uptake. to promote HIVST by Ningbo CDC. Our study’s con- tribution to investigate factors associated with HIVST and help the government develop targeted strategies to Limitations improve HIV testing among MSM in China. The present study had several limitations. First, par- Our study showed that those MSM who were younger ticipants were relatively high-educated, had higher or high education levels were more likely to have had income, and our findings may not be generalizable in HIVST. It is possible that younger MSM had more wor- other contexts or settings. Second, some questions ries about positive test results [11]. Worldwide, about were asked in the prior 6  months. Despite imple- 32% of new HIV infections among adults aged 15  years mented quality control measures, recall and social and older have occurred in youth ages 15–24  years in desirability bias might have existed.Third, this was 2018 [4]. Therefore, HIVST education should be included not a representative sample of the MSM population in as a part of comprehensive sexual and reproductive Ningbo, because only those who had a willingness and Hong et al. AIDS Res Ther (2021) 18:14 Page 6 of 8 Table 2 Factors associated with HIVST among study participants in Ningbo, China, 2019 (n = 699) Factor Unadjusted P‑ value Adjusted P‑ value b b OR (CI) OR (CI) Age (years) 18 ~ 1.00 1.00 30 ~ 0.72 (0.51–1.01) 0.054 0.49 (0.32–0.76) 0.001 ≥ 40 0.20 (0.12–0.34) < 0.001 0.07 (0.04–0.14) < 0.001 Marital status Married 1.00 – Single 1.08 (0.78–1.48) 0.653 – – Education level Middle school or less 1.00 1.00 High school 1.74 (1.17–2.57) 0.006 2.82 (1.70–4.69) < 0.001 College or above 1.35 (0.92–1.99) 0.123 1.42 (0.92–2.20) 0.052 Local residence time < 2 1.00 1.00 2 0.57 (0.40–0.82) 0.002 0.66 (0.44–1.00) 0.052 Monthly income (CNY ) < 5000 1.00 1.00 ≥ 5000 1.95 (1.41–2.71) < 0.001 1.35 (0.94–1.93) 0.100 Sexual orientation Gay 1.00 1.00 Bisexual 0.46 (0.30–0.71) < 0.001 0.49 (0.29–0.84) 0.009 Unknown/unsure 0.64(0.32–1.26) 0.198 0.71 (0.34–1.51) 0.379 Gay apps use No 1.00 1.00 Yes 1.96 (1.26–3.07) 0.003 1.86 (1.13–3.05) 0.014 Multiple male sex partners No 1.00 1.00 Yes 1.43 (1.02–2.00) 0.036 1.90 (1.29–2.80) 0.001 Frequency of male–male sexual contact (times/week) < 1 1.00 1.00 ≥ 1 1.63 (1.20–2.22) 0.002 1.86 (1.30–2.66) 0.001 Unprotected sex with men No 1.00 – Yes 0.77 (0.54–1.09) 0.134 – – Syphilis infection No 1.00 1.00 Yes 3.39 (1.78–6.45) < 0.001 5.48 (2.53–11.88) < 0.001 In the prior 6 months Univariate and multivariate regression analyses were used to generate odds ratios (ORs) and 95% confidence intervals (CIs) contacted trained project workers could be recruited Conclusions into the study.Finally, as this was a cross-sectional The coverage of HIVST had a significant gap in Ningbo, study, we are unable to establish a causal relationship. China. It is necessary to make continued efforts to expand HIVST coverage among MSM. Further HIVST education should strengthen for school-age children and teenagers, HIV prevention should include HIVST Hong  et al. AIDS Res Ther (2021) 18:14 Page 7 of 8 10. Strömdahl S, Hoijer J, Eriksen J. Uptake of peer‑led venue ‑based HIV kits usage and offer through gay apps and CBO, and testing sites in Sweden aimed at men who have sex with men (MSM) and free HIVST kits might be provided to high-risk MSM to trans persons: a cross‑sectional survey. Sex Transm Infect. 2019;95:575–9. accelerate achieve the "90-90-90" goal. 11. Zhou J, Chen J, Goldsamt L, Wang H, Zhang C, Li X. HIV testing and associated factors among men who have sex with men in Changsha. Ch J Assoc Nurses AIDS Care. 2018;29:932–41. 12. World Health Organization. Guidelines on HIV self‑testing and partner Abbreviations notification: supplement to consolidated guidelines on HIV testing HIVST: HIV self‑testing; PLWH: People are living with HIV; VCT: Voluntary HIV services. Geneva, Switzerland: WHO, 2016. World Health Organization. counseling and testing; CDC: Centers for disease control and prevention. http:// www. who. int/ hiv/ pub/ self‑ testi ng/ hiv‑ self‑ testi ng‑ guide lines/ en/. Accessed date 30 Aug 2020. Authors’ contributions 13. Stevens DR, Vrana CJ, Dlin RE, Korte JE. A global review of hiv self‑testing: HH and HS designed the study, HH and HD coordinated the study, HS and HJ themes and implications. AIDS Behav. 2018;22:497–512. collected the data, HH did the primary data analysis, HH and HS contributed to 14. Harichund C, Moshabela M. Acceptability of HIV Self‑testing in Sub ‑ part of the analysis. HH, HS, and YS drafted the paper. All authors contributed Saharan Africa: scoping Study. 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Publisher’s Note 33. Adam PCG, de Wit JBF, Bourne CP, Knox D, Purchas J. Promoting regular Springer Nature remains neutral with regard to jurisdictional claims in pub‑ testing: an examination of HIV and STI testing routines and associated lished maps and institutional affiliations. socio‑ demographic, behavioral and social‑ cognitive factors among Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions

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AIDS Research and Therapy – Springer Journals

Published: Apr 20, 2021

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