Sexually Transmitted Diseases:
High HIV Prevalence and Risk of Infection Among Rural-to-Urban Migrants in Various Migration Stages in China: A Systematic Review and Meta-Analysis
Zhang, Lei PhD*; Chow, Eric P.F. MPH*; Jahn, Heiko J. MSc†; Kraemer, Alexander PhD†; Wilson, David P. PhD*
From the *Kirby Institute, Faculty of Medicine, University of New South Wales, Sydney, Australia; and †Department of Public Health Medicine, School of Public Health, Bielefeld University, Germany
This study was funded by the universities of New South Wales (Sydney, Australia) and Bielefeld (Germany) and jointly by the Go8 Germany Joint Research Co-operation Scheme 2011 and the German Academic Exchange Service. The Kirby Institute is funded by the Australian Government, Department of Health and Ageing, and affiliated with the Faculty of Medicine, University of New South Wales. The views expressed in this publication do not necessarily represent the position of the Australian Government.
Correspondence: Lei Zhang, PhD, The Kirby Institute, Faculty of Medicine, University of New South Wales, Sydney NSW 2052, Australia. E-mail: firstname.lastname@example.org.
Received for publication March 4, 2012, and accepted November 29, 2012.
Background: Rural-to-urban migrants represent 17% of the total Chinese population and are considered a potential high-risk bridging population of HIV infection between urban and rural China.
Method: Based on a systematic review and meta-analysis, this study determined HIV prevalence among rural-to-urban migrants in different stages of migration. This review was conducted and reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines.
Results: We identified 54 studies reporting 59 HIV prevalence levels among rural-to-urban migrants in China. Overall, 53.4% (95% confidence interval, 33.5%–72.4%) of urban patients with HIV have migratory background. The floating-out population showed a higher HIV prevalence (0.15% [0.06%–0.34%]) than did the Chinese population (0.057%; odds ratio, 2.63 [1.35–5.14]). The floating-in population showed a higher HIV prevalence (0.38% [0.29%–0.50%]), corresponding to 6.70 (6.05–7.41) times greater odds of HIV infection. Higher prevalence levels were observed among female migrants (0.69% [0.51%–0.93%]), reflecting a much higher odds of HIV infection (12.18 [11.11–13.35]). Infection risk among returning migrants (0.18% [0.12%–0.29%]) was 3.16 (2.06–4.84) times higher than the overall Chinese population. Chinese internal migrants contribute to a substantial amount of the overall HIV epidemic in China.
Conclusion: Migrants are at greater risk for HIV infection than the general Chinese population and likely to facilitate the geographical spread of HIV in China. Targeted strategies for health promotion and HIV prevention for migrants in China should be developed.
Since the implementation of the 1978 “open door policy” that promoted foreign trade and investment, China has experienced rapid economic growth in many coastal urban areas and major cities. Large economic disparities led to the emergence of large population movement patterns, particularly rural-to-urban migration to seek after better employment opportunities, higher income, and a more attractive lifestyle in urban China.1,2 According to the latest official statistics, there are 225.5 million rural-to-urban migrants (also named “floating population”) in China, accounting for 17% of its population.3,4 Owing to the strict household registration (Hukou) system in China, very few migrants are able to obtain urban permanent residency, and a large proportion of them work in an urban city for a certain period and eventually return to their rural hometown or move to another city.5 These migrants travel between urban and rural areas seasonally during Chinese holidays.3,6
Rural-to-urban migrants are often considered a potential high-risk population for HIV infection and transmission in China. Being away from one’s spouse and family leads to increased risks of extramarital sexual behaviors, especially male migrants. In addition, female migrants who are unable to find other employment in urban areas may engage in commercial sex.7–11 Approximately 6% of female migrants have participated in sex work during their stay in urban areas.12 Multiple sources have indicated that migrant workers account for most HIV-infected patients in China cities.13–21 In addition, population mobility of the migrants has been identified as a major risk factor for facilitating transmission of HIV infection in China,22,23 and frequent shifts between work locations and seasonal visits back home may further spread HIV infection to their partners and other uninfected populations9
Scattered sources have reported HIV prevalence among rural-to-urban migrants in China with large variations (0–2.59%).2,24–27 However, little is known about the changes in the prevalence during various stages of the migration. Although these migrants are often thought to be a potential bridge of HIV infection between the urban and the rural areas, there is little quantified evidence that the infection was transmitted by the returning migrants to the uninfected population. Based on a systematic literature review and meta-analysis, this study aimed to determine the HIV prevalence among rural-to-urban migrants at different stages of migration and the likely causes of variations of HIV prevalence. It also compared the risk of HIV infection among different subgroups of migrants using the general Chinese population as the referencing population.
Three independent investigators (E.P.F.C., H.J.J., L.Z.) conducted a systematic review of published peer-reviewed research articles by searching both English and Chinese electronic databases: PubMed (H.J.J., L.Z.), VIP Chinese Journal Database (VIP), China National Knowledge Infrastructure, and Wanfang Data (E.P.F.C., L.Z.) until June 15, 2011. Keywords used in the database search included (“HIV” OR “AIDS”) AND (“floating migrants” OR “rural-to-urban migrants” OR “floating-in” OR “floating-out” OR “migrant workers (Nong Min Gong)”) AND “China.” We also performed a manual search on the reference lists of the retrieved articles. This review was conducted and reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement issued in 2009.28
Studies were eligible for inclusion in this systematic review if they met the following criteria: (1) study published in Chinese or English language, (2) study reported HIV prevalence estimates among rural-to-urban migrants in China, and (3) HIV infection must be diagnosed from laboratory serologic testing.
We excluded review articles, non-peer-reviewed local/government reports, conference abstracts, and presentations. Self-reported HIV infections and nonserologic HIV diagnoses (i.e., urine and oral fluid) were excluded. Studies with non-Chinese migrants or ones focusing exclusively on risk groups such as migrant commercial sex workers were also excluded. If the same data were published in both English and Chinese sources, the articles published in Chinese language were excluded.
In this review, we investigated the prevalence of HIV infection among different types of migrants in China, namely, (1) people who were about to migrate from their mostly rural home to urban areas (floating-out population), (2) migrants who already migrated from rural areas and residing in urban areas when the study took place, and (3) migrants who have returned from urban areas back to their home in rural areas.
The quality of studies was assessed using a validated quality assessment tool for cross-sectional studies.29 The following 8 items were assessed to calculate a total quality score: (1) clear definition of the target population, (2) representativeness of probability sampling, (3) sample characteristics matching the overall population, (4) adequate response rate, (5) standardized data collection methods, (6) reliability of survey measures/instruments, (7) validity of survey measures/instruments, and (8) appropriate statistical methods. Answers were scored 0 and 1 for “No” and “Yes,” respectively. The total quality score varied between 0 and 8 (see Table 1).
We extracted the following information from all eligible studies: first author and published year, study period, study location, type of study, percentage of male and female participants, sample size, testing method for HIV, and HIV prevalence. The studies were categorized in floating-in, floating-out, and return migrants population (Table 1).
Meta-analyses were carried out using the Comprehensive Meta-Analysis software (V2.0; Biostat, Englewood, NJ).30 Pooled HIV prevalence estimates and 95% confidence intervals (CIs) for each study and odds ratios (ORs) for group comparisons (migrant subgroups among each other and migrant subgroups vs. general Chinese population) were calculated. Heterogeneity tests were performed using the Cochran Q test (P < 0.10 represents statistically significant heterogeneity) and I2 statistic.31–33 The value of the I2 statistic indicates low (25), moderate (50), and high (75) heterogeneity between studies. Random-effect model was used when there was a high and significant heterogeneity across studies, whereas fixed-effect model was used otherwise. Results were graphically presented in forest plots. We investigated the factors (i.e., language of article, type of study, study location, and study period) that were associated with heterogeneities in the stratified meta-analyses using meta-regression analysis.34 Potential presence of publication bias was measured by the Begg and Mazumdar rank correlation (P < 0.05 represents statistically significant publication bias).35,36
Study Identification and Selection
Our initial search criteria identified 1753 articles from 4 electronic databases, and 5 additional articles were identified through reference lists from identified articles. We excluded 976 articles because they were unrelated to the topics or duplicated titles from different databases. Abstracts were screened among the remaining 782 articles, and 164 were excluded because they were not related to floating migrants. After screening the full text of the 618 eligible articles, 564 were further excluded because they did not cover the population of floating migrants (N = 110) or did not report the HIV prevalence among the rural-to-urban migrants population (N = 454). The remaining 54 studies (4 in English and 50 in Chinese) were eligible for quantitative synthesis. Of 54 eligible studies, 3 reported HIV prevalence in multiple years,27,37,38 which resulted in 59 HIV prevalence estimates. We performed stratified meta-analyses for the different types of migrants: floating-out population (N = 7), floating-in population (N = 48), and return population (n = 4). The selection process is illustrated in Figure 1.
In the total of 54 studies, the sample size of the selected studies ranged from 182 to 37,829 (median, 818; interquartile range, 505–1854), and the reported HIV prevalence among Chinese migrants ranged from 0% to 2.59%. Seven studies provided data from floating-out migrants, 43 studies reported floating-in population data, and 4 studies referred to returning migrants. Four studies were national sentinel analyses, and the remaining 50 articles were independent studies. A total of 121,027 migrants were surveyed. The mean age of the migrant participants was 33.71 years. Approximately one third of the migrants (36.39%) were primary school graduates or illiterate. Furthermore, 69.22% of migrants were Han ethnic, 61.04% were currently married, and 57.41% of study participants were female.
Quantitative Data Synthesis
It is well accepted that the HIV epidemic in China remains concentrated among the key behavioral populations (of intravenous drug users, female sex workers, and men who have sex with men), and HIV prevalence among the Chinese population is low (0.057%23,39). This official national HIV prevalence level was calculated based on the current estimate of 78,000 people living with HIV/AIDS nationwide in China. Our results show that rural-to-urban migrants, recruited before they leave their home towns, had a higher HIV prevalence (0.15%; 95% CI, 0.060–0.34%; Fig. 2C), representing higher odds of HIV infection as compared with the Chinese population (OR, 2.63; 95% CI, 1.34–5.14).
In comparison, migrants who were recruited in their residing urban areas had a much higher HIV prevalence (0.38%; 95% CI, 0.29%–0.50%; Fig. 2A), corresponding to 6.70 (95% CI, 6.05–7.41) times higher odds of HIV infection than the overall Chinese population. Strikingly, among these urban recruited migrants, HIV prevalence among women was even higher (0.69%; 95% CI, 0.51%–0.93%; Fig. 2B), reflected in a much higher OR of 12.18 (95% CI, 11.11–13.35). The pooled estimated HIV prevalence among migrants returning from urban areas, regardless of temporary stay or permanent residence, was 0.18% (0.12%–0.29%; Fig. 2D), and their OR for HIV infection was 3.16 (95% CI, 2.06–4.84) in comparison with the overall Chinese population (Table 2). However, our findings did not show a significant higher odds of HIV infection among returning migrants than among the floating-out migrants (OR, 1.20; 95% CI, 0.54–2.65; Table 2).
Of 18 studies that reported percentages of female migrants and HIV prevalence, HIV prevalence was found to be positively correlated with the proportion of female migrants (Spearman ρ: r = 0.506; 95% CI, 0.23–0.71; P < 0.001). We identified 4 studies that exclusively reported on male migrants, 3 of which reported zero HIV prevalence40–42 and 1 reported 9 infections of 1624 male migrants (0.55%).43
Twelve studies reported a more detailed migratory history of HIV-infected individuals,13–21,44–46 and the pooled estimate from our meta-analysis showed that a proportion of 53.4% (95% CI, 33.5%–72.4%) of HIV-infected individuals in urban China was among migrants (Fig. 2E).
No publication biases were observed among the 4 types of migrants in the meta-analyses (P = 0.881, 0.455, 0.307, and 0.497 for floating-out and floating-in, floating-in female, and returning populations, respectively; Fig. 2A–D). Significantly high heterogeneities were observed in the floating-in population (I2 = 74.87, P < 0.001) and floating-in female population (I2 = 82.33, P < 0.001). Meta-regression analyses showed that the language of the articles (β = −4.133, P = 0.008), study location (β = −0.260, P = 0.007), and study period (β = −0.568, P = 0.036) significantly contributed to this relatively high heterogeneity among the floating-in population, whereas only study period (β = −0.913, P = 0.007) significantly contributed to high heterogeneity among the floating-in female population.
To our knowledge, this is the first study that systematically reviewed HIV prevalence among rural-to-urban migrants in China according to their status of migration based on an exhaustive search in both Chinese and English literature. Our results indicated that most people living HIV in urban China have a migratory background. In addition, we identified a higher HIV prevalence among migrants who were migrating from their registered rural areas of residency to urban cities in comparison with the overall Chinese population.
In comparison, migrants recruited from urban areas had 6.70 times higher odds of being infected with HIV than did the overall Chinese population. Furthermore, the odds of female migrants in this group were 12.18-fold higher than the overall Chinese population. It was previously documented that both male and female migrants are more likely to participate in high-risk behaviors when they are away from their home town. Male migrants are more likely to have multiple sexual partners and/or seek for commercial sex, whereas female migrants are more likely to offer commercial sex in case they face financial difficulties in the urban cities.7–11 Past findings indicated that 70% to 95% of the female sex workers in China were from a rural-to-urban migrant background.47–53 This is in line with our result that HIV prevalence was positively correlated with the percentage of females in the collected studies.
One of our key results is that migrants returning to their registered rural home residence, regardless of their length of stay, had a much lower HIV prevalence than those recruited in urban areas. This clearly suggests that HIV-infected migrants tend to stay in urban areas, rather than returning to their rural home residence.54–57 This may partly be caused by to social stigmatization and less sufficient HIV/AIDS-related medical support within the public health care service sector. The nature of participation in commercial sex work of female migrants, in the context of strong cultural and moral values among their rural families and communities, could be a reason for their extended stay in urban areas. In addition, infected migrants may be reluctant to return to their hometown because of strong stigmatization toward HIV-infected individuals.58 Since 2003, the Chinese government launched extensive programs to provide affordable and reachable health care services for HIV-infected people in China.59 However, implementation of the intervention programs fell substantially behind in rural China because of its geographical isolation, underdeveloped medical facilities, and undersupported staffs to provide comprehensive HIV/AIDS treatment including second-line antiretroviral therapy and treatment of multiple opportunistic diseases.60 Because returning migrants had a 3.16 times higher odds of being HIV infected than did the overall Chinese population, their return may pose a threat for bridging HIV infection to the rural general population.
Several limitations of this study should be noted. First, the result that 53.4% of HIV-infected urban cases have a migratory background needs to be interpreted with caution. In China’s sentinel surveillance system, the migrant population is as one of key populations subjected to HIV screening. Therefore, HIV cases among migrants are more likely to be detected than the general population, indicating an overestimate of the actual contribution of migrants to HIV cases. HIV prevalence among rural-to-urban migrants remains low in comparison with highly at-risk groups in China, implying that a large sampling size is required to detect any HIV infections. As a result, our analysis may underestimate the actual HIV prevalence among the migrants because of the small sampling sizes of individual studies. Besides, strong social stigma against HIV-infected individuals in their rural hometown may substantially reduce their participation in the collected studies, leading to an underestimate of HIV prevalence among return migrants. Furthermore, the rural-to-urban migrant population includes a diverse array of subpopulations with different occupations that can be quite different in their risk of HIV infection. For instance, migrants who are long-distance truck drivers or miners are more prone to purchasing sex, whereas female migrants employed in entertainment industries are more likely to be involved in commercial sex trade than those with other occupations. It is important to note that, of course, there are many migrants who are at very low or no risk for HIV acquisition when away from home. In the current study, we were unable to investigate these effects because of the limitations and unavailability of the relevant demographic data in the collected studies. Owing to limited available studies that stratified according to sex, subgroup analysis with the sex factor was not performed for floating-out and return populations.
The trend of rural-to-urban migration will increase if the economic disparity between the 2 areas of China remains large. Hence, our findings have important implications for HIV prevention and interventions in China. A number of previous reviews have identified rural-to-urban migrants as a high-risk population for HIV infection and transmission.42,61–63 Consistently, our results demonstrate that most HIV-infected individuals in urban China (53.4%; 95% CI, 33.5%–72.4%) had a migratory background. Thus, intervention strategies preventing HIV transmission among rural-to-urban migrants would expectedly have large impacts on confining the overall HIV epidemic in China.
HIV prevention strategies targeting migrants in urban China need to be implemented with the involvement of key institutions at various administrative levels, including both provincial- and inner-city district–level governmental institutions. Grassroots partners such as employers of migrants and workers’ unions in urban cities should also be engaged in strategies to protect the health of migrants. An integrated and concerted intervention approach can reach and be implemented to prevent the further spread of HIV among the migrants. Intervention strategies for migrants should also address the issue of mobility. Considering the regular movement and the higher odds of HIV infection among returning migrants, voluntary HIV counseling and testing (VCT) should be substantially scaled up among migrants traveling back and forth between rural and urban areas. Mobile VCT services can be set up at major train and long-distance bus stations to offer free VCT. In this case, rapid HIV testing may be provided as screening tests; also, posttest counseling and referral of confirmation test can be offered to those tested positive. The increase in HIV diagnosis may, in turn, encourage timely initiation of antiretroviral treatment that reduces the risk of further transmission. Furthermore, commercial sex provision among female migrants and utilization among male migrants should be targeted. Health education, in combination with condom distribution, should be tailored for the migrant population. For instance, employment agencies that are frequently used by working migrants could be a channel to offer health materials in prevention and treatment of sexually transmitted diseases and HIV. Health education should start early in rural schools to reduce stigmatization of people living with HIV/AIDS (PLHIV) and risk of HIV transmission in rural communities.
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