Disparities in healthcare access and utilization among people living with HIV in China: A scoping review and meta‐analysis

This review aims to assess the status of healthcare disparities among people living with HIV (PLWH) in China and summarize the factors that drive them.


BACKGROUND
Inequalities undermine global efforts to end the HIV pandemic [1].New data from The Joint United Nations Program on HIV/AIDS (UNAIDS) revealed that approximately one-quarter of all people living with HIV (PLWH) did not have access to antiretroviral therapy (ART) in 2021 [2].This proportion is even higher among children living with HIV and those in low-and middle-income countries.For example, in China, more than 26% of children living with HIV aged ≤14 years had not received ART as of the end of 2018 [3].Stigma, discrimination, marginalization of communities and unequal access to health and other essential services have contributed to increased healthcare disparities among PLWH [4].In this study, we define healthcare disparities as disparities in access to and utilization of healthcare services among population groups [5][6][7].
Prompt initiation of ART and retention in HIV care are recognized as key steps in improving clinical health outcomes among PLWH [8].And the success of the free ART programme in China has effectively reduced HIV-related mortality [9].However, healthcare disparities are still a problem in China [10][11][12].For example, a retrospective cohort in Guangxi, China, showed that only 72.1% of PLWH aged ≥50 years received ART from 1996 to 2019, far lower than among younger PLWH (86.1%) [13].In an era of 'treating all', the coverage of ART among men who have sex with men (MSM) in China was only 60.3% in 2016 [14].Just 60.1% of PLWH aged ≥15 years who injected drugs in China received ART during 2001-2020 [15].Thus, great disparities exist in access to healthcare among PLWH in China.As life expectancy gets closer to that of the general population, the rising morbidity from non-AIDS-defining diseases (NADs) indicates that PLWH needs more intensive non-HIV healthcare than people without HIV [16].Details about the overall current situation are not clear, and limited studies have sought to summarize the overall situation in China, although this is important for resolving healthcare disparities in China.
The aims of this study are: (1) to understand the status of healthcare disparities among PLWH in China in both HIV-focused and non-HIV-focused care, and (2) to summarize the factors driving healthcare disparities among PLWH in China.

Study design
A scoping review approach was adopted because it allows researchers to rapidly map out key concepts in a complex research area well based on the main sources of evidence available [17].The review followed the framework outlined by Arksey and O'Malley [18] and included five steps: (1) identifying a research question, (2) identifying relevant studies, (3) eligibility screen, (4) charting the data, and (5) collating, summarizing and reporting the results.

Searching strategy
We searched and retrieved relevant articles from PubMed, Web of Science, Cochrane Library, Scopus, China National Knowledge Infrastructure (CNKI) and China Wanfang.The search query consisted of terms such as health disparities, health inequities, healthcare disparities, people living with HIV, PLWH, PLHIV, HIV-infected, or other associated terms, which were tailored to the specific requirements of each database.Full search terms, with the respective database, are listed in File S1.Original articles published from January 2000 to July 2022 and published in English or Chinese were eligible for inclusion.All identified articles from the searches were transferred to the Endnote X9 software tool for managing bibliographies, citations and references, and sharing with other reviewers.Duplicate articles were excluded.

Eligibility criteria
All included studies met the following criteria: (1) the study had to be conducted among people living with HIV in China; (2) it had to be focused on disparities in healthcare, including access and utilization of medical services; and (3) it must have used quantitative, qualitative or mixed-method study designs.To keep the inclusion criteria as broad as possible, dissertations were eligible.However, grey literature, reviews, conference articles and commentaries were excluded.

Data screening and extraction
Two reviewers (WA, CF) first independently assessed the titles and abstracts to identify relevant records for inclusion following the eligibility criteria.When two reviewers disagreed on article selection, a consensus was sought from the third researcher (WT).Full texts of the eligible studies were retrieved and assessed for inclusion following the same screening method.The following data were recorded from the final included studies independently by the same reviewers using Excel data extraction and synthesis sheets.As data were extracted, a data charting form was collectively developed to map studies based on forms of disparity, and the extracted data included, author name(s), year, region, study population, sample sizes, study design, factors associated with healthcare access and utilization (such as types of healthcare, variables and data), and facilitators and barriers of healthcare disparities.

Data analysis
Quantitative data on healthcare access/utilization among PLWH were pooled using a random-effects model in a meta-analysis utilizing R-Language version 4.1.1.The rate of receiving ART was defined as the number of people receiving ART in their survey period divided by the total number of people surveyed.Full ART adherence was defined as participants not missing a dose of antiretroviral drugs in their survey period.The 95% and above ART adherence category was defined as participants taking ≥95% of the dose of antiretroviral drugs in their survey period.The higher than 90% ART adherence category was defined as participants taking >90% of the dose of antiretroviral drugs in their survey period.The 2-week medical consultation rate was defined as the number of people who utilized outpatient services in the 2 weeks before their survey divided by the total number of people surveyed [19].The 2-week morbidity without medical consultations category was defined as the number of people who reported any illnesses but without medical consultation in the 2 weeks before their survey divided by the number of people who reported any illnesses in the 2 weeks before their survey [19].The annual inpatient rate was defined as the number of people hospitalized in the year before their survey divided by the total number of people surveyed [19].The rate of nonhospitalization among those who required hospitalization was defined as the number of people who required hospitalization but were not hospitalized divided by the number who required hospitalization [19].In addition, the driving factors of healthcare disparities were classified into three categories based on a socio-ecological framework: individual level, community and interpersonal level, and structural level [20].Individual-level factors refer to biological and other personal characteristics, such as knowledge, behaviour, income, health history, and so forth.Community-and social-level factors are characterized as related to the individual's social networks and life environment.Structural factors include cultural and social norms and health, economic and social policies.

Overall characteristics of the included studies
Figure 1 is the PRISMA flow diagram.The initial search generated a total of 8728 articles.After excluding duplicate references, 7291 articles remained.A review of titles and abstracts revealed that 6669 articles were irrelevant or not conducted in China, leaving 622 articles for full-text screening.Of these, 571 articles did not meet the inclusion criteria because they were review/comments (n = 47), full texts were not found (n = 31), they reported the wrong outcomes (n = 221), they reported the wrong population (n = 28), overlapped data (n = 14), or were conducted in other countries (n = 230).The final records consisted of 51 articles.
Table 1 describes the characteristics of included articles.The articles reviewed were published from 2000 to 2022, with the majority of articles published after 2010 (n = 41, 80.4%).Figure 2 displays the distribution of study regions.Studies were carried out across seven regions of China: eastern China (n = 8), northern China (n = 1), southern China (n = 5), central China (n = 7), southwest China (n = 21), northwest China (n = 2), and northeast China (n = 1).The remaining six studies were conducted in multiple regions.Thirty-seven of the 51 studies were quantitative studies, seven were qualitative studies and seven used mixed methods.
Table 2 demonstrates the pooled rate of PLWH characteristics.In the included studies, 27% of PLWH had CD4 cell counts <200 cells/μL, 51% of PLWH were between 200 and 500 cells/μL, and 18% of PLWH were >500 cells/μL.About 4% of women living with HIV were diagnosed as HIV-positive before pregnancy, 27% were diagnosed during pregnancy and delivery, and 29% were diagnosed after delivery (forest plot in Figure S1).For HIV testing sites, 39% of PLWH were tested at medical facilities, 48% of PLWH were tested at the Centers for Disease Control and Prevention (CDC), 4% of PLWH were tested at custody institutions and 7% of PLWH were tested at blood centres (forest plot in Figure S2).
Fifty-one studies reported factors associated with healthcare access and utilization among PLWH.These factors were often interrelated and exerted their influence at different levels in different contexts.This review identified the factors in each category based on the socioecological framework and illustrated them in Figure 3.
At the structural level, our findings focused on the health systems and policy.Overall, the clinic environment [28], inflexible clinic working hours for The pooled rates of characteristics of people living with HIV (PLWH) in China (n = 51).

Categories
Pooled rate HIV-designated healthcare facilities [33], long-distance travel to health facilities and lack of transportation [24,27,33,48], and limited service capability [48] were the most commonly cited barriers to uptake and adherence.Out-of-pocket medical expenditures such as extra laboratory tests [22,35,39], opportunistic infection treatment costs [33,47] and second-line antiviral drug costs [33] were also identified as barriers, and failure

T A B L E 4
The pooled rates of non-HIV-focused care among people living with HIV (PLWH) in China (n = 11).
to meet the criteria for free ART was the policy barrier for non-ART initiation [38,40,58,59].

Non-HIV-focused care
The most cited individual-level barrier was financial concern [58][59][60][61][62][63][64][65].Concern about HIV status disclosure in the course of seeking medical care [61,66,67] resulted in medical facility avoidance in some PLWH.Perceived severity of healthcare needs was also associated with healthcare services utilization.People perceiving the symptom or disease not to be serious showed lower odds of seeking healthcare services [58-60, 64, 65, 68].Men living with HIV were less likely to utilize outpatient and in-patient services than women, and family factors such as having more children and having more PLWH in the household were also identified as being associated with poorer utilization of outpatient and in-patient services [68].Lack of attention and pessimism related to HIV infection posed obstacles for female PLWH in cervical cancer screening [67].PLWH who were homosexual [69] and had low socio-economic status [70] experienced more challenges in utilizing mental health services, while those with religious beliefs [70] were more willing to take mental health assessments.At the community and social level, PLWH who experienced discrimination from healthcare providers [66,71] or distrust of healthcare services [61] had a low willingness to seek healthcare services.Support from family members facilitated healthcare utilization [64].
Structural factors, such as PLWH from rural areas, did not have an urban hukou (household register system), and thus they are excluded from urban medical care [71].

DISCUSSION
Summarizing the status of healthcare disparities among PLWH is essential for improving healthcare equity.This scoping review summarizes literature that examines disparities in healthcare access and utilization among PLWH in China and yielded 51 articles.It extends the existing literature by understanding the status of the disparity, assessing the driving forces of disparity from different levels, and providing evidence for future intervention.Our review found substantial healthcare access and utilization disparities among PLWH in China.We also identified different factors affecting healthcare access and utilization.
Our review found disparities in receiving ART and ART adherence among PLWH in China.Although the nationwide free ART programme began in 2003, only PLWH with CD4 counts <200 cells//μL were eligible for free treatment before 2016 [72].The treatment criteria were updated in 2016 enabling all ART for all PLWH to access ART [72].The rate of receiving ART among PLWH aged ≥45 years is higher than those aged <45 years, which is different from a report from Canada [73].Avoidant coping, fear of unintentional disclosure, and stigmatizing social norms may diminish the intention of young PLWH to initiate ART [74].Similar to the findings from South Africa and Thai [75,76], we found that the rate of receiving ART is higher among women living with HIV than among men.Evidence has shown that for men in some contexts, having HIV may be perceived as an impediment to being able to provide for a family, and the fear of losing masculine respectability undermines treatment-seeking for men living with HIV [77].In addition, PLWH attributed to injecting drug use appear to have a lower rate of receiving ART than those attributed to sexual transmission, similar to the finding of a Spanish study [78].Due to legal challenges, unstable housing, poverty, and lack of social and family support [79,80], people who inject drugs face multiple barriers to accessing health services, which largely delay ART initiation.The pooled rate of ≥95% ART adherence reported by PLWH in China (82%) is higher than that reported in India (77%) and Ethiopia (73.1%) [81,82].The various management models, such as follow-up management of localization, humanity management, health management and active self-management implemented in China among PLWH, have greatly improved ART adherence [83].Similar to the findings in Zambia and Nepal, adherence to ART was higher among women living with HIV than among men living with HIV [84,85].Men living with HIV who admit they are sick and seek help can feel their masculinity is compromised, and thus they may discontinue treatment [86].Poverty, stigma and fear of being perceived as a failure for acquiring HIV also pose barriers to maintaining HIV care among men living with HIV [87].For non-HIV-focused care utilization, the 2-week morbidity of PLWH without medical consultation and the rate of non-hospitalization among those who required hospitalization were both higher than the national general population (2-week morbidity of residents without medical consultation = 1.7%,rate of nonhospitalization among residents who required hospitalization = 10.2%)[88].This indicates that access to non-HIV-focused healthcare services in PLWH is inadequate.
Personal financial constraints were the primary cited barrier between the intention to seek care and the actual use of care services.Failure to meet the eligibility criteria for the national free ART programme caused some PLWH to pay out-of-pocket for antiviral medication.Also, the costs of laboratory tests and expenditures related to adverse drug events (ADEs) are not covered or subsidized, although the free ART policy covers the cost of antiviral drugs for PLWH.This may explain some of the financial constraints cited by PLWH, as a Nigerian study showed that the incidence rate of ADEs among PLWH was high at 28.3% [89].In addition, the reimbursement rate of medical insurance for the treatment of PLWH is low.For example, medical insurance only covers 12.7% of PLWH outpatient medical expenses in Dongguan City, while in Nanchang City, medical insurance covers 20.8% [90].Expanded insurance policies, including coverage of more medical services and higher reimbursement rates, are needed to reduce the burden of medical costs on PLWH in China.
Fear of HIV status disclosure was also a common reason for the lack of care engagement and treatment retention.Many people diagnosed with HIV face difficulties in deciding when and how to disclose their status to those around them.The anticipated negative consequences of HIV disclosure are considered an important driver in the disclosure process [91].Some studies have shown that stigma is a major factor in non-disclosure [92,93].Stigma is rooted in culture and driven by personal and social values [94].HIV-related stigma stems from perceptions of 'sexual immorality' and misconceptions about the mechanisms of HIV transmission [95].In Chinese society, the phenomenon of prejudice against PLWH is widespread.A study among PLWH in central China showed a moderate to high level of perceived stigma [96].More than 70% of healthcare workers had discriminated against PLWH in the delivery of medical services in healthcare settings [97].Therefore, interventions to reduce HIV-related stigma such as enhancing social support, improving the quality of HIV care, and strengthening the capacity of healthcare providers to promote the availability of healthcare services among PLWH are necessary.
This review summarizes the status and the driving forces of healthcare utilization disparities for PLWH in China and provides directions for future interventions to promote healthcare equity.Creating a supportive social environment and expanding insurance policies could be considered to promote healthcare equity.However, there are some limitations to our scoping review.First, the included articles were published from 2000 to 2022, in which the free ART policy underwent several adjustments.Thus, part of our study before 2016 was based on the old policy, which may reduce the applicability of the results.Second, the pooled adherence rate estimated in this review may be overestimated, as the 13 included studies used PLWH self-reports to estimate adherence.Third, we did not pool the rate of undetected viral load due to the scarcity of information provided in the cited studies.Fourth, we could not analyse our findings according to the 90-90-90 framework because of a lack of information on the number of people diagnosed as HIV-positive and viral suppression in the studies we cited.Furthermore, the studies we cited did not provide information on the use of pre-and post-exposure prophylaxis and the impact of undetectable = untransmittable (U=U) in China.Another shortcoming is that studies included in this review are only related to the Chinese context, which may limit generalizability.Nevertheless, the findings of this review will provide a good basis for further syntheses.

CONCLUSION
This review indicated great disparities in ART access, adherence and utilization of non-HIV-focused care services among PLWH.Financial issues, social discrimination, structural problems in the healthcare system and lack of psychological support are prominent in the process of utilizing medical services for PLWH.Expanding current insurance policies, including covering more medical services and increasing reimbursement rates, are needed to ease the burden of medical costs for PLWH.Also, the government could negotiate with private insurance to subsidize the cost of covering non-HIV-focused services for PLWH.Creating a supportive social environment is needed to reduce HIV-related stigma and discrimination by using crowdsourcing to develop more innovative and participatory stigma reduction interventions.

F I G U R E 3
Factors of healthcare access and utilization for people living with HIV (PLWH) in China.
T A B L E 1*n ≥ 51 as some studies included multiple data types and/or participant groups.
The pooled rates of receiving antiretroviral therapy (ART) and adherence among people living with HIV (PLWH) in China (n = 37).
T A B L E 3