HIV testing uptake, enablers, and barriers among African migrants in China: A nationwide cross-sectional study

Background African migrants in China face social, structural, and cultural barriers to human immunodeficiency virus (HIV) testing with scarce information on their HIV testing behaviours. This study estimated the prevalence of HIV testing and its social and behavioural correlates to understand how to better provide HIV testing services for African migrants living in China. Methods We conducted a national cross-sectional survey among adult African migrants who lived in China for more than one month between January 19 to February 7, 2021. The survey was disseminated online through six African community organizations and via participant referrals. We collected data on HIV testing behaviours and history of HIV testing, social, and cultural factors and applied univariate and multivariable logistic regression to identify testing correlates. Results Among a total of 1305 participants, 72.9% (n = 951/1305) tested for HIV during their stay in China and yielded a self-reported HIV prevalence of 0.4% (n = 4/951). The most common reason for HIV testing was to comply with Chinese residence policy requirements (88.5%, n = 842/951); for not testing was “no need to be tested” (79.4%, n = 281/354). We found most African migrants have experienced low acculturation stress (54.5%, n = 750/1305), low social discrimination (65.6%, n = 856/1305), have a moderate stigma towards HIV (54.3%, n = 709/1305), and low community engagement around sexual health and HIV topics. In multivariable analysis, African migrants who were students (adjusted odds ratio (aOR) = 3.36, 95% CI = 2.40-4.71), living in student dormitories (aOR = 3.86, 95% CI = 1.51-9.84), received health services in China in past year (aOR = 1.67, 95% CI = 1.25-2.23), had lifetime sexually transmitted infections (STI) testing (aOR = 1.95, 95% CI = 1.23-3.10), had HIV testing before coming to China (aOR = 13.56, 95% CI = 9.36-19.65), and those engaged in community discussions of HIV and sexual health (aOR = 2.77, 95% CI = 1.31-5.83) were more likely to test for HIV in China. Conclusions Despite 73% of African migrants having tested for HIV in China, there are unmet needs and barriers identified in our study, such as language barriers. Access to HIV knowledge and testing services were the most important enablers for testing, including studentship, past STI/HIV testing, and community discussion on sexual health. Culturally appropriate and community-based outreach programs to provide information on HIV and testing venues for African migrants might be helpful to promote testing uptake.

Africans are among the fastest-growing migrant populations worldwide, transitioning from historically high-income destinations (HICs) to low-and middle-income countries (LMICs) [1,2]. 31% (12 millions) of African migrants moved to LMICs in 2019 compared with 17% in 2010, with the Asian continent quickly becoming the second largest recipient of African migrants after Europe [1,3]. Increasing numbers of Africans are migrating and residing in China due to increased trade and economic relations between the regions [4]. International evidence shows that migrants were at higher risk for human immunodeficiency virus (HIV) infections and faced additional structural and social challenges to access local health services [3,[5][6][7][8][9][10]. However, there is scarce data on African migrants' HIV testing behaviours and sexual health needs in China or in other LMICs to inform public health authorities on how best to support this population.
Currently, there are an estimated 200 000 to 450 000 Africans living in China including both students and workers [11][12][13][14]. Most African migrants self-identify as "traders/businessmen" or "students" and reside in China on short-term and long-term stays [13]. African businessmen usually travel frequently between their home country and destination cities in China. In 2016, around 62 000 African students were studying in China, with an annual increase of 24% [12]. African students are the fastest growing group among foreign students [12]. Interpersonal and cultural challenges, varying expectations of medical care, logistical problems at hospitals, and language issues were expressed as barriers to African migrants' health care-seeking processes in China [15]. Since 2013, Chinese policy had required all foreigners who apply for visas longer than one year to submit HIV testing records in order to obtain the visa, regardless of the test results; though there are no mandates at the national level to get tested for HIV once foreigners enter China [16,17].
To date, there is little data on African migrants' HIV testing behaviour, needs, and barriers in China. Given increasing globalization, more understanding of HIV testing and service utilization among African migrants is necessary and beneficial to both the local and global context. European studies found African migrants were at higher risk for HIV infection with lower rates of HIV testing compared with local residents, calling for tailored interventions to support this population [18][19][20]. A Belgian study found a high HIV prevalence of 4.2%-5.9% in sub-Saharan African migrants [19], yet due to cultural, financial, and structural barriers, they often presented to hospitals later when infected with HIV [3][4][5][6][7][8][9]. Delays in diagnosis and treatment can result in higher morbidity and mortality and increased HIV transmission risks in the community [21][22][23]. European studies found knowledge of HIV and high-risk behaviours, access to primary care, risky sexual behaviours, and non-stigma toward HIV was associated with increased HIV testing [18,20,24].
Evidence from HICs suggests that HIV stigma reduction, risk awareness education, strengthened linkage to care, and structural inclusion in health care would promote HIV testing in African migrants [5]. However, HIV testing behaviours and challenges can be inherently different in resource-limited settings than in HICs. Databased interventions addressing the unique needs of African migrants in China and other LMICs are urgently needed to fill the gap in the literature. This study aims to examine HIV testing experiences and its determinants among African migrants in China.

Study design and participants
We conducted a national online cross-sectional survey between January 19 and February 7, 2021, using Wen-JuanXing online software (Changsha Haoxing Information Technology, China), a widely used online survey software in China. Individuals were deemed eligible if they self-identified as an African or of African parentage, aged more than 18 years old, cumulatively lived in China for more than one month, and were able to provide informed consent. All eligible participants received 5 US$ after completing the survey.

Sample size
The primary outcome of this study was the HIV testing rate in China. A Chinese previous study reported a testing rate of 47.8% for HIV among African migrants [25]. We applied two-sided confidence intervals (CI) for one proportion method to estimate a sample size of 1096 for this study to produce a two-sided 95% CI and a width of 0.060. prevention. The questionnaires were piloted among 20 African migrants to ensure they were clear and comprehensible for the intended participants. The pilot data were excluded from the final data.
We used a peer-driven method for data collection. We first identified six active African community organization leaders (communities from Zimbabwe, Nigeria, Zambia, Tanzania, and Ghana) in China to facilitate initial study recruitment, where they mobilized peer networks to disseminate online recruitment to potential participants through WeChat (a widely-used Chinese messaging app). Through the link in WeChat, study participants access the questionnaire hosted on Wenjuanxing software. We did not collect any identifiable data and all responses were kept confidential. Second, participants were encouraged to recruit other eligible individuals to our questionnaire and informed that they would receive 2 US$ for each effective referral.
Participation in this survey was completely voluntary. Participants were informed it would take 20 minutes to complete the survey and that all responses would be kept confidential. Study individuals clicked "agree to participate" and signed the electronic informed consent if they were willing to participate in this study. To minimize repetitive recruitment, we only allowed the survey link to be accessed once by one IP address, phone, or WeChat account.

Outcomes and exploratory variables
The primary outcome of interest is HIV testing or not while in China. Other HIV testing information collected included: the place of HIV counselling/ testing in China (public hospital/STI specialist hospital, private hospital, blood centre); latest HIV testing results (positive, negative, never got results); reasons for having HIV test (Chinese residence policy requirements, want to know my HIV status, enlightenment of publicity and education); and reason for not having HIV test (no need to be tested, language communication barriers, I don't know where to test).
Social demographic information collected included: gender (male, female), age (years), marital status (never married, ever married /engaged/ widowed/ divorced), highest educational attainment (high school or below, some college, bachelor or above), annual income (USD), religion, reasons for migration, cumulative stay in China, living arrangement in China and health insurance. Sexual behaviours information collected included: types of sexual partners, commercial sexual activities, and consistent condom use in sexual activities. Consistent condom use was defined as always using condoms when engaged in sexual activities.
Acculturative stress was measured by nine items, with each item coded 0 for no and 1 for yes, adapted from the National Latino and Asian American Study (Table S1 in the Online Supplementary Document) [26]. One example item is "Do you feel guilty for leaving family or friends in your country of origin". The total scores ranged from 0 to 9 with 3 categories: low (0-3), moderate (4)(5)(6), and high (7)(8)(9). Higher score indicates greater self-reported acculturative stress. The Cronbach's α of the acculturative stress scale in this study was 0.546. Discrimination was measured by ten items, with each item scored 0-5 on a Likert-type scale (never, less than once a year, few times a year, few times a month, at least once a week, and almost every day), adapted from the Detroit Area Study (Table S2 in the Online Supplementary Document) [27]. One example is "Have you ever been treated with less courtesy while in China". The total scores ranged from 0 to 50 with 3 categories: low (0-20), moderate (21)(22)(23)(24)(25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40), and high (41-50). A higher score indicates greater self-reported daily discrimination. The Cronbach's α of the discrimination scale in this study was 0.930.
Anticipated HIV stigma was measured by seven items, with each item scored 0-3 on a Likert-type scale (strongly disagree, disagree, agree and strongly agree), developed by Golub and Gamarel among men who have sex with men in New York (Table S3 in the Online Supplementary Document) [28]. One example item is "If I had HIV, I'd worry about people discriminating against me". The total scores ranged from 0 to 21 with 3 categories: low (0-8), moderate (9)(10)(11)(12)(13)(14)(15)(16), and high (17)(18)(19)(20)(21). A higher score indicates a greater self-reported anticipated HIV stigma. The Cronbach's α of the anticipated HIV stigma scale in this study was 0.879.
Community engagement on sexual and HIV topics was measured by six items that elicited participants' awareness and advocacy involvement of HIV and sexual health, and each item was coded 0 for No and 1 for Yes. (Table S4 in the Online Supplementary Document) [29]. One example item is "Have you ever participated in online forums or discussions on social media (i.e., WhatsApp, WeChat, Weibo, Twitter, or other online communities) about sexual health, condom use, or HIV/STI testing or related services?" The total scores ranged from 0 to 6 with 3 categories: low (0-2), moderate (3)(4), and high (5-6). A higher score indicated greater self-reported community engagement. The Cronbach's α of community engagement scale in this study was 0.690.

Statistical analysis
From the cross-sectional data, we described the socio-demographics, sexual behaviours, HIV testing, acculturative stress, discrimination, HIV stigma, and community engagement of African migrants in China. Categorical parameters were presented as the number (percentage) of participants. All the continuous data have been tested for normality using Kolmogorov-Smirnov method. We found that all the continuous data were normally distributed. Continuous data were expressed as mean ± standard deviation. The χ 2 test was used to compare categorical variables. The difference in acculturative stress, discrimination, anticipated HIV stigma, and community engagement between the HIV testing subgroup and non-HIV testing subgroup in China was assessed with t test.
Univariable and multivariable logistic regression was conducted to explore socio-demographic, sexual behavioural factors, acculturative stress, discrimination, anticipated HIV stigma, and community engagement association with HIV testing. In the multivariable model, we adjusted for gender, age, legal marital status, highest educational attainment, annual income, and religion as these were considered non-changeable demographic features. In subgroup analysis comparing mandatory HIV testers and voluntary HIV testers, the same methods were used to compare socio-demographics and identify correlates for mandatory HIV testing. All analyses were conducted using SAS (V9.4, SAS Institute Inc., Cary, NC). All the results are deemed to be statistically significant when P ≤ 0.05.

RESULTS
The survey platform was accessed by 2147 individuals, where twenty individuals did not provide informed consent and 822 did not meet the eligibility criteria (262 were not from an African country or of African parentage, 552 were younger than 18 years old and 8 did not cumulatively live in China for one month or longer) (Figure 1). A total of 1305 individuals were enrolled and completed the online survey.

Feeling discriminated against as a foreigner in China
3.8% (n = 49/1305) of participants experienced a high level of discrimination as a foreigner in China, a third reported moderate discrimination (30.6%, n = 400/1305), and the majority experienced no or low level of discrimination (65.6%, n = 856/1305). Ever had HIV testing in China was found to be associated with feeling discriminated against as a foreigner in China (P = 0.029).

Anticipated HIV stigma
A minority of participants displayed a high level of stigma towards HIV (13.6%, n = 178/1305), most participants expressed a moderate level of stigma towards HIV (54.3%, n = 709/1305), and about one-third of participants showed a low level of HIV stigma (32.0%, n = 418/1305). There was no statistically significant association between the anticipated HIV stigma of the participants and having an HIV test in China (P = 0.385).

Community engagement on HIV and sexual health
Few (4.8%, n = 62/1305) participants actively engaged in community discussion around HIV and sexual health, 12.8% (n = 167/1305) were moderately involved with these discussions, and the majority of participants had low or no involvement in a community discussion on HIV and sexual health (82.4%, n = 1076/1305). HIV testing in China was found to be associated with a higher score of community engagement on this topic (P < 0.001) ( Table 3).

Regression analysis: Correlates of HIV testing
After adjusting for gender, age, marital status, educational attainment, annual income, and religion, multivariable logistic regression analysis indicated that African migrants who migrated to China for study (adjusted odds   (Table 4).
Subgroup analysis between mandatory testers (n = 842) and voluntary testers (n = 109) found that those who tested for HIV mandatorily were younger, living in staff/student dormitories, and have health insurance in China; those who tested for HIV voluntarily were more likely to have had a sexual contact in China. The two groups also differed in annual income levels (

DISCUSSION
Our study provides the first national cross-sectional estimates of HIV testing uptake and sexual behaviours of African migrants in China. We found that 72.9% African migrants tested for HIV in China, comparable to 58.3%-89.6% African migrants tested in European countries [18][19][20]24]. 75.2% of sexually active migrants tested for HIV, slightly higher than those not having sex in China (71.5%). Self-reported HIV prevalence is 0.4%, lower than the 4.2%-5.9% found among African migrants in Europe and the prevalence in their home countries ranging from 1.4% to 12.9%, while 10 times the estimated prevalence of 0.037% in general Chinese population [19,30,31]. Our finding stresses the relevance to continually promote HIV testing uptake for African migrants to diagnose those infected with HIV and link them to care in a timely manner.
Since 2013, Chinese policy removed negative HIV testing result as a visa requirement for foreigners entering the border but have kept a proof of HIV test as a required document in the visa application materials. Once foreigners entered China, there are no mandates at the national level to get tested for HIV during their stay [16,17]. Among those never tested in China, the most common reason reported was "no need to be tested" (79.4%), despite the fact that only 53% of participants who have had sex reported consistent use of condoms, and 12% had sex with casual partners. Our findings of low risk perception as a dominant reason for not testing echoes with findings from Zimbabwe and Europe, where 33%-48% African migrants who had sex with non-steady partners consistently used condom and "not necessary to get tested" continuedly being expressed as a top reason for not testing [18,20,32]. Additionally, language barrier (14.4%), and lack of information on testing venues (9.9%) were also identified as barriers for testing, suggesting that support for more accessible and visible routes for African migrants to test for HIV is needed, for example, providing multiple language services or information brochures at public and community health facilities. Offering HIV testing to African migrants in general medical practice was also found to be acceptable and feasible in European settings [33,34].
Successfully delivering HIV prevention efforts for African migrants will require expanding culturally and socially appropriate services. We observed a lower frequency of community engagement on sexual health and HIV than in a German study, where 57% of African migrants reported discussion of HIV within their community [16]. We did find that participating in community discussion around sexual health and HIV, moderately or frequently, was associated with doubled and tripled odds of testing for HIV, aligned with the German study which reported discussing HIV in the community increased HIV testing odds by 92% [20]. This might be because community discussion on such sexual health topics can disseminate accurate information and knowledge on HIV, which can improve testing uptake based on data from an African migrant community in Britain [35]. We also observed low-to-medium level of acculturation stress, social discrimination, and over half present moderate stigma towards HIV, consistent with findings from North America and UNAIDS [36,37]. Studies have shown that acculturation stress, social discrimination and HIV stigma were barriers for HIV testing [38][39][40], though they were not associated to HIV testing as hypothesized in our study.
African students are more likely to participate in HIV testing in China. This might be attributable to health requirement policies on campus and their better knowledge and education on HIV, which were found as promoting factors for HIV testing [35]. Compared with businessmen and workers, students may have better access to HIV-related information and testing, through school-based HIV advocacy and education events, self-testing kits on campus, and routine health examinations for students [41,42]. This alarms policy-makers of the current vacuum in HIV testing efforts to reach non-student migrants. For health service utilization, 87.5% of African migrants in our study had health insurance in China and 34.1% have received health care services in China in past year, which was associated with a 67% increase in likelihood of testing for HIV. Existing care utilization, including previous STI and HIV testing, may remove the initial logistical and psychological barriers for getting tested for HIV. The findings align with the experience of African migrants in 9 countries in Europe, where access to primary care being a strong enabler for HIV testing [18]. Considered as a whole, our findings highlight that access to accurate HIV knowledge and testing services can be important enablers to improve HIV testing uptake.
Our study has several limitations. The cross-sectional study design limits causal inference ability. Africans in China are a hard-to-reach population and there are no known registries to ensure a representative sample, the participants were recruited using non-probabilistic sampling method, which may result in sampling bias. However, we reached 26 out of 34 provinces in China and covered the most populous and economically developed regions to increase the representativeness of this sample. The questionnaire was in English language and all data collected in this study was self-reported by participants, which may be biased and not verified. We offered research subjects financial incentives for their participation in this study, which may lead to biased REFERENCES Acknowledgements: We are grateful to all participants in this study, without whom this study cannot be completed. We thank all dedication and efforts of the study implementation team at Dermatology Hospital Guangzhou site that made this research possible. We appreciate our collaborating community organizations for their help to facilitate and coordinate this study.
Ethics statement: This study was approved by the Ethical Committee of Dermatology Hospital of Southern Medical University (2020074). All participants provided electronic informed consent.
Data availability: Please contact the corresponding author for data requests.
Funding: Natural Science Foundation of Guangdong Province of China(2022A1515011454).
Authorship contributions: CW conceptualized the study and acquired funding. PZ managed data collection, conducted data analysis, wrote the draft of methods and result. JW drafted introduction, discussion section, and led all revisions. CW, BJH, MYR, KS, AB reviewed and contributed to the final manuscript. All authors reviewed and approved the final manuscript.

Disclosure of interest:
The authors completed the ICMJE Disclosure of Interest Form (available upon request from the corresponding author) and disclose no relevant interests.

Additional material
Online Supplementary Document enrollment. Further studies to understand how enablers and barriers impact HIV testing uptake, and implementation science study to tailor efforts for migrant subgroups, such as students, businessmen, and seasonal migrants who face different social environment are in urgent need.

CONCLUSIONS
Our study presents the first HIV testing prevalence among African migrants in China. Though 73% African migrants tested for HIV in China, unmet needs and barriers for testing were identified, such as language, lack of knowledge on testing venues, and potentially low risk perception. Access to accurate HIV knowledge and HIV testing services were the most important enablers for HIV testing uptake. Studentship, past STI/HIV testing, and community discussion on sexual health topics were promoting factors for HIV testing. Culturally appropriate and community-based outreach programs to facilitate knowledge sharing on HIV, sexual health, and testing access will be beneficial to promote testing and HIV prevention efforts for this population.