Introduction

In the first quarter of 2020, the SARS-CoV-2 pandemic disrupted nearly every facet of human interaction worldwide, including efforts to conduct ongoing research. Recognizing the widespread impacts of SARS-CoV-2, the cause of COVID-19, virologists and public health researchers working on HIV infection quickly turned their attention to the structure, pathogenesis, and prevention of this new pathogen. For social and behavioral scientists working on HIV infection, the challenges posed by a novel life-threatening communicable disease were apparent and familiar [1, 2]. For many researchers, ongoing studies that were focused on the health and behavior of people living with HIV (PLWH) were seen as opportunities to study the impacts of COVID-19 on PLWH. Here, we review the social and behavioral research concerning the impacts of COVID-19 on PLWH that reported data collected in the first year of the SARS-CoV-2 pandemic.

COVID-19 complicates the clinical course of HIV infection and vice versa. Early observers reported that PLWH experienced more severe clinical outcomes from COVID-19 compared to people not living with HIV [3]. In a review of 22 studies with 20,982,498 patients across Africa, Asia, Europe, and North America, Ssentongo et al. [4] found that PLWH were significantly more likely to develop COVID-19 and had greater COVID-19 mortality than their HIV-negative counterparts. Greater severity and death rates from COVID-19 among PLWH have been confirmed [5, 6]. Factors such as immune suppression, chronic inflammation, and other underlying conditions associated with HIV infection likely account for greater COVID-19 severity in PLWH [3, 4]. Studies show that when HIV is fully suppressed, the clinical course of COVID-19 may be no different for people with HIV than it is for people who are HIV negative, with comorbid conditions complicating the protective benefits of viral suppression [7]. There is also evidence that antiretroviral therapies (ART) may offer some clinical benefit in COVID-19, although the evidence for these protective effects of ART are inconclusive [4, 8,9,10]. The potential for more severe COVID-19 clinical outcomes among PLWH brought a sense of urgency to understanding the social and behavioral impacts of COVID-19 on PLWH.

A substantial literature on the social and behavioral implications of COVID-19 for PLWH emerged within the first year of the SARSCoV-2 pandemic. Unlike the first years of the HIV pandemic which were met with relative indifference, the early weeks of COVID-19 were met with entire countries and industries mobilized to contain and prevent the spread of infection. In a review of rapidly conducted studies, commentaries, and editorials concerning the social impacts HIV-affected populations, Winwood et al. [11] examined research published through January 31, 2021. Taking a broad approach, the review identified several emerging trends in the early studies of COVID-19-HIV co-infection, including expansion of telehealth and impacts on mental health, food insecurity, social isolation, finances and sexual behavior. The clustering of multiple impacts around COVID-19 and their implications for PLWH indicated that COVID-19 could be considered a contributing condition and complication in the broader context of factors that influence HIV infection.

COVID-19 and HIV Syndemics

The COVID-19 and HIV pandemics intersect in the context of multiple overlapping comorbidities at the individual and structural levels. For example, type-2 diabetes and metabolic syndrome significantly contribute to the severity of COVID-19, as well as contributing to the morbidity and mortality of HIV infection [12,13,14]. Several other health conditions that increase the risk for severe COVID-19 are prevalent in PLWH, including hypertension, obesity, and chronic pulmonary disease [15]. Furthermore, ART is associated with metabolic disruptions that can complicate the clinical course of type-2 diabetes and metabolic syndrome [16]. Stress, depression, and substance use, which are prevalent among PLWH, have immune-suppressive effects which may also complicate COVID-19 [17]. In addition, public health responses to slowing SARS-CoV-2 transmission center on social distancing, which may contribute to social isolation, raising particular concern for many PLWH who are already socially marginalized [18]. The potential for COVID-19’s synergistic relationships with HIV infection and their multiple co-occurring conditions have brought some social and behavioral HIV researchers to conceptualize COVID-19-HIV co-infection within a syndemics framework [19]. Defined as two or more epidemics that interact to synergistically facilitate greater disease burden [20], COVID-19 adds to the already multiple co-occurring conditions in HIV syndemics, including other infectious and non-infectious diseases, mental health conditions, emotional distress, and alcohol and other substance use [20]. A syndemics framework highlights how these conditions and others known to co-occur with HIV are exacerbated by COVID-19 [21]. Subclinical comorbidities such as urogenital inflammation, renal disease, metabolic syndrome, and others are also prevalent in PLWH and increase risks for severe COVID-19 [1]. In addition, social isolation promoted by physical distancing and self-quarantine increases the risk for adverse drug use events driven by limited access to clean drug use supplies and unaccompanied overdose [22]. Because of the synergistic nature of these comorbidities, changes in any one condition will have the potential to impact others.

Like medical and mental health comorbidities, structural inequalities also contribute to COVID-19-HIV syndemics. Food insecurity, for example, can lead to malnutrition, compromise general health status, and impede HIV treatment retention and ART adherence [23, 24]. Likewise, the adverse health effects of food insecurity contribute to risks for severe COVID-19 disease [25]. Housing instability has similar adverse impacts on HIV health outcomes [26], and housing instability can translate to dense congregate living conditions, which can in turn increase COVID-19 exposure risks. For example, in a cohort of marginally housed PLWH in San Francisco, housing instability worsened in early COVID-19 and contributed to increased risks for COVID-19-HIV co-infection [27]. Thus, along with mental health and substance use, structural inequalities fall within a syndemics framework and help explain HIV and COVID-19 health disparities.

Previous authors have conceptualized the complex factors influencing the course of HIV infection as interlocking gears, where changes in one cog invariably shift the next [28, 29]. This same conceptualization can be extended to the whole of HIV syndemics, along with their intersection with COVID-19. Figure 1 illustrates our adaptation of this concept to include the psychosocial sequelae of COVID-19 and their implications for HIV syndemics. In this adaptation, the psychosocial sequelae of COVID-19 such as fear and anxiety of infection, social distancing, and COVID-19 stigma exacerbate mental health conditions such as depression, social isolation, emotional distress, and substance abuse, which in turn contributes to food insecurity, housing instability and poor engagement in healthcare. Furthermore, these synergistic impacts can diminish motivation to engage in COVID-19 mitigation practices, and further suppress immune response, increasing vulnerability to severe COVID-19 [30, 31]. COVID-19 therefore amplifies existing social and health disparities in populations affected by HIV, including those attributed to race, gender, and geographic region [32]. Recognizing that HIV occurs in conjunction with multiple co-occurring epidemics informs clinical and social services as well as creates a framework for research [33]. Our review therefore conceptualizes COVID-19 from the perspective of HIV syndemics by recognizing the synergism of social and behavioral determinants of health that complicate both HIV infection and COVID-19. Our review therefore takes syndemics approach to examining the first year of social and behavioral research on the impacts of COVID-19 on PLWH.

Fig. 1
figure 1

Conceptualization of COVID-19 and HIV as interlocking conditions in a syndemics framework (adapted from Strathdee et al. (2012) and Pellowski et al., 2013)

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Methods

Search Strategy

We performed an initial search of PubMed and Google Scholar in March 2021 and repeated the search on May 25, 2021, to assure up-to-date completeness (see Fig. 2). We used a Boolean approach with search terms (hiv) AND (covid-19) AND (depression OR anxiety OR stress OR stigma OR mental health OR alcohol OR drug use OR substance use Or housing OR food insecurity). The first search did not impose time restrictions, and the second search was restricted to papers published between April and May 2021. Following the second search, there were a total of 177 articles identified, and after removing duplicates spanning across search terms, there were 152 articles screened for data-based studies using the titles and abstracts. Furthermore, we conducted a just-in-time manual search of key journals (AIDS Care, AIDS and Behavior, Journal of Acquired Immunodeficiency Syndromes, AIDS Patient Care and STDs, etc.) on November 12, 2021, after the review process and prior to press, identifying an additional 10 studies that are included in the table of study findings. We also removed studies that concerned COVID-19 impacts on HIV but did not include PLWH, such as samples of people at risk for HIV and studies of HIV pre-exposure prophylaxis. A total of 35 studies were included in our review.

Fig. 2
figure 2

Flow of search strategy and resulting papers for this review

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Results

Methodological Considerations

The studies reviewed from the first year of COVID-19 demonstrated substantial limitations, some of which may have occurred simply because of the obvious time urgency to assess immediate impacts. Thus, studies from the early months of COVID-19 reviewed in this paper cannot tell a complete story of the impacts of COVID-19 on PLWH, as the events of the intersecting pandemics were still evolving. Most of the limitations with these studies are common to cross-sectional research, particularly lacking pre-COVID-19 base rates. Studies reporting high levels of anxiety, depression, social isolation, etc. may not have reflected actual impacts of COVID-19 populations with high base rates. The few studies that reported longitudinal data in this early period suggest that more such studies will become available. Studies that are conducted over time will likely report results from periods included in published cross-sectional studies and will require tracking for redundancy in future reviews. Another limitation in this early literature is the necessity to invent new measures without systematic psychometric development. Again, driven by the immediate urgency of an unfolding pandemic, measures were often developed rapidly and are idiosyncratic to a particular study. Finally, although we reviewed research from the first year of COVID-19, the evolution of the pandemic was not geographically uniform, with research occurring at different stages of local epidemics. Research reported from China, Italy, Spain, the UK, and the USA reflects different stages of COVID-19 in the first year of the pandemic than research from Kenya and Ukraine. These facets of the literature should be considered as the reviewed research is interpreted.

Mental Health

Our review of studies concerning the mental health implications of COVID-19 for PLWH identified five major impacts: social isolation, emotional distress, stigma, coping, and substance use (see Table 1).

Table 1 Summary of studies on COVID-19 impacts on people living with HIV
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Social Isolation

Initial public health responses to COVID-19 emphasized maintaining physical distance to avoid exposure to respiratory droplets and aerosolized virus particles. From a mental health perspective, the common use of the term “social distancing” implied social isolation as an unavoidable consequence of COVID-19 protective behaviors [34]. Cultural differences in living conditions, social relations, and options for interpersonal communication suggest that the social isolating effects of COVID-19 restrictions varied across countries. For example, social relations in Spain emphasize closeness in extended families, frequent gatherings, and community structures for congregating in public spaces, all of which likely helped fuel the devastating early outbreaks of COVID-19 in Spain. Ballester-Arnal [35] described COVID-19 as a “socially cruel” disease, with its impacts on social interactions among PLWH compounded by concerns about continuing care and sustaining social support. Similar concerns, as well as evidence for similar COVID-19 impacts among PLWH, were reported in Italy [36]. In Kenya, adolescents and young adults living with HIV indicated that the greatest impacts of COVID-19 were those that restricted social interactions, including 25% of young people stating that closed churches and 92% of young people stating that closed schools were the greatest adverse impacts of COVID-19 they experienced [37]. However, the adverse social impacts of COVID-19 restrictions were not universal. In Australia, for example, 43% of PLWH reported that COVID-19 negatively impacted social relationships, while 13% reported that COVID-19 had a positive impact on their relationships [38].

Cultural variations notwithstanding, PLWH may have been particularly vulnerable to the adverse effects of social isolation given the limited social support they often experience due to HIV stigma and intersecting sources of rejection (e.g., racism, homophobia, sexism). For example, one study reported that 72% of PLWH participating in a longitudinal cohort were already socially isolated, defined as living alone, not engaged in a relationship, lacking reliable sources of social support, and not being socially satisfied [18]. Subsequent data collection during early COVID-19 found that having recently experienced violence and having a mental illness were correlates of increased social isolation [39]. Other research conducted early in the COVID-19 pandemic reported increased loneliness among PLWH and suggested greater loneliness and stress among women than men [40]. However, there were PLWH who received increases in social support during COVID-19 lockdowns as service providers ramped up outreach efforts and PLWH and HIV care providers became technologically connected [41]. The duration of social isolation and loneliness experienced by PLWH during early COVID-19 may have been relieved as services, communities, and individuals adapted to socially distant communication [42].

Emotional Distress

People living with HIV are typically attuned to the fact that they can be more vulnerable to an array of infectious diseases. Increased vulnerability to co-infections, as well as non-infectious comorbidities, in the daily lives of PLWH provides a basis for the increased stress that was attributable to COVID-19 for many PLWH. Some studies in early COVID-19 reported high rates of depression and anxiety among PLWH [43, 44], although it is not possible to know if these rates in-and-of themselves represent a change from pre-COVID19 levels of distress. However, in Australia, two-thirds of PLWH reported worrying about their health and mental health specifically due to COVID-19 [38]. Other studies that were also able to account for pre-COVID-19 mental health examined changes over time and offer clearer answers. For example, a study of PLWH in New York City found 69% of PLWH experienced symptoms of emotional distress with 4% meeting the threshold for major depression and 14% meeting the criteria for general anxiety disorder during periods of quarantine and lockdown, and emotional distress were partly attributable to prior diagnoses of anxiety and depression [45]. In Peru, PLWH reported experiencing increases in anxiety and stress that they retrospectively attributed to changes in their lives resulting from early COVID-19 [46]. Similarly, one in four PLWH in Turkey reported general anxiety during early COVID-19. In this study, non-specific general anxiety was related to anxiety specifically attributed to COVID-19, and increased anxiety seemed to result from concerns about the transmissibility of COVID-19 [47]. During Italy’s early and severe COVID-19 outbreak, anxiety and stress were greatest among PLWH with additional underlying comorbidities [36].

Two studies concerning the emotional distress of COVID-19-HIV are particularly noteworthy for their methodological approaches. The first study built on assessments that were being conducted weekly before COVID-19 and continued during the outbreak. In this study, older adults living with HIV expressed concerns about potential exposures to COVID-19 and these concerns were the leading source of stress during the early weeks of COVID-19 [41]. In the second study, researchers used an adaptation of the Impact of Events Scale that specified COVID-19 as the impactful event. In this study, Delle Donne et al. [36] found that 45% of participants reported mild to severe symptoms of distress, most commonly depression and anxiety attributable to COVID-19, with greater emotional distress reported by women than men.

Studies also investigated factors that may have contributed to increased COVID-19 distress. For example, because of heightened concerns for contracting COVID-19 among PLWH, conflicting public health messaging and misinformation may have fueled COVID-19 stress [48]. One barrier to COVID-19 information messaging was a lack of trust in public health information sources, such as the CDC and health departments. Using the same measures, two independent studies showed that PLWH in New York City [48] and Atlanta, GA [49], demonstrated low levels of trust in COVID-19 information from all public health institutions, with greater trust in local and state health departments than trust in the CDC and other federal agencies. It is important to note that like social isolation, not all studies provide evidence for adverse effects of COVID-19 on emotional distress among PLWH. Specifically, in Miami, FL PLWH demonstrated less anxiety and COVID-19-related worries than a comparison group of people not living with HIV, and the difference was associated with resilience that served to buffer anxiety [50].

Stigma

Fueled by fear, stigma is an expected consequence of infectious disease outbreaks and serves as another source of COVID-19 stress for PLWH [51]. Past experience with emergent infectious diseases, including H1N1 influenza [52] and SARS [53], provided the groundwork for what to expect with regard to COVID-19 stigma. Characterizing a new infectious disease as originating from outsiders facilitates a process of “othering,” which reinforces the social construction of illness as a foreign invasion with ensuing xenophobia [34]. Because HIV itself is a highly stigmatized condition, stigmas attached to COVID-19 may be particularly stressful for PLWH. Among PLWH, endorsing prejudicial and discriminating attitudes toward COVID-19 is associated with greater concern over contracting COVID-19 and a greater likelihood of implementing social distancing to prevent contracting COVID-19 [54, 55].

Along with HIV stigma, intersecting sources of social inequality have contributed to and have compounded the stress of COVID-19 for PLWH. In qualitative interviews, Gwadz et al. [48] found that experiences of racism and structural inequality often framed PLWH’s experiences with COVID-19. Participants in this study saw a direct link between their experiences living with HIV and COVID-19 health disparities. Just as would be true for people not living with HIV, fear of COVID-19 exposure may have also been greater among PLWH in cities and densely populated areas where social distancing is more difficult [48]. Interruptions to health services and medications as well as anticipated and actual loss of income attributed to COVID-19 also contributed to stress experienced by PLWH. A study of sexual minority men from 103 counties found that 46% of men living with HIV anticipated loss of income due to COVID-19 compared to 38% of men who were not living with HIV, which was a significant difference [56]. And while anxiety and depression did not differ between the two HIV status groups, anticipated loss of income was associated with overall anxiety and depression.

Adaptive Coping

Although the risk for severe COVID-19 is greater for people with HIV, prior experiences living with HIV may serve as a source of resilience for some PLWH. For example, contrary to expectations that PLWH would be adversely affected by COVID-19 stigma [57], Quinn et al. [58] found that men living with HIV believed that having lived through the HIV pandemic helped them manage the stress brought about by COVID-19, including resisting stigmatizing people who contract COVID-19 and facilitating a sense of responsibility for preventing the spread of COVID-19. In Argentina, resilience (defined as responding adaptively to adversity), buffered the association between economic hardship incurred during COVID-19 and perceived COVID-19 stress and loneliness [59]. Resilience has therefore emerged as a key characteristic of adaptive coping with COVID-19, including limiting the adverse effects that COVID-19 has on the mental health and well-being of PLWH [50, 60]. Like other aspects of COVID-19 impacts, there are cultural differences in the influence that resilience has on coping with COVID-19 in PLWH, with resilient coping reducing depression in PLWH in Argentina, but not in the USA [60]. While there were no studies concerning aspects of adaptive coping other than resilience, studies did consider substance use as a maladaptive coping strategy.

Substance Use

The emotional distress of COVID-19 has the potential to prompt increased substance use and relapse to use among individuals in recovery. Increased substance use carries several detrimental implications for the health of PLWH. Studies that examined substance use among PLWH during early COVID-19 reported variable results with no consistent pattern. Some studies reported increases in alcohol consumption [38, 61] and other drug use [44], although it is unclear if these increases differed from those of people not living with HIV. Counter to expectations, some studies reported reductions in drug use among PLWH, including tobacco consumption [50, 61]. There is also mixed evidence for increased adverse consequences from COVID-19 that are expected with increased substance use. Using a 30-day retrospective assessment strategy during early COVID-19, PLWH reported greater marijuana use compared to their HIV-negative counterparts, including a greater increases in use since a previous pre-COVID-19 assessment, and greater use was associated with depression symptoms [62]. In contrast, a study of PLWH in the state of Wisconsin found that while alcohol and marijuana use did not increase during early COVID-019, use of other drugs nearly doubled from 10% reporting use to 18% [63]. Among people who inject drugs, active substance use was associated with less physical distancing to prevent COVID-19 and greater depression, with no differences between participants living with HIV and those not living with HIV [64].

Structural Inequalities

Three major COVID-19 impacts on structural inequalities were assessed in the early COVID-19 studies: food insecurity, housing instability, and accessing health services.

Food Insecurity and Housing Instability

Food insecurity increased in the general US population during early COVID-19, specifically between March and June 2020 by as much as 10% [21]. Decades of research has reported that PLWH have high rates of both food insecurity and housing instability [23, 65, 66], making PLWH a particularly vulnerable population for COVID-19 disruptions in food access and housing security. The impacts of COVID-19 on food security and housing stability were therefore expected to be greater than in other populations, with the greatest disruptions occurring for the least resourced [67]. People living with HIV themselves anticipated greater loss of financial support due to COVID-19 than did people not living with HIV, and the anticipated financial losses were expected to increase depression and anxiety. However, despite no differences between PLWH and their HIV-negative counterparts in terms of job loss or salary reductions during COVID-19, PLWH reported greater increases in financial stress and food insecurity [62]. One study in New York City found that 14% of PLWH were unable to obtain food they needed during the early months of COVID-19 [48]. In St. Louis, Missouri, during the early months of COVID-19, PLWH experienced greater food insecurity including not having enough food they needed and experiencing hunger, than their HIV-negative counterparts [62]. In another major US city, Atlanta, GA, 40% of PLWH reported not being able to access food during the early weeks of COVID-19, with one in five food-insecure participants becoming food insecure during early COVID-19 [1]. For patients receiving Ryan White Care services in a rural area of the Southern United States, 69% of patients who had been employed prior to COVID-19 reported adverse impacts on their employment, including 74% of those patients losing their jobs. In addition, Ryan White services for food support increased 66% and emergency housing services increased 69% in April 2020 [68].

Similar vulnerabilities to structural inequalities exacerbated by COVID-19 were observed across continents. Among young PLWH in Kenya, 25% reported that the early COVID-19 impacted their employment and income [37]. Similarly, 25% of PLWH in Australia reported negative effects of COVID-19 on their incomes [38]. In addition, 13% of PLWH in Australia indicated that they experienced reductions in access and affordability of food during periods of COVID-19 restrictions [38]. In Argentina, the rate of PLWH experiencing financial hardship during COVID-19 was 41% [59].

Access to Health Services

Among the most consistent research findings for PLWH during early COVID-19 were concerns that lockdowns would reduce access to HIV care services. Disruptions to clinical and social services were reported during the earliest days of local responses to COVID-19 [42, 69, 70]. Even when services themselves were available, PLWH expressed concern about losing access and lacked confidence that they could attend upcoming appointments because of COVID-19-related restrictions [71]. Clinic and pharmacy closures had an obvious short-term effect on all patients, including those living with HIV. One factor contributing to healthcare interruptions was trust in public health guidelines. In a study 459 people living with HIV in Atlanta, expressing greater trust in the CDC for COVID-19 information was related to experiencing fewer disruptions to healthcare, suggesting that PLWH were positively impacted by trusting credible COVID-19 information [49].

The impacts of early COVID-19 disruptions on ART adherence also varied across studies. It was widely expected that COVID-19 would interrupt access to ART with adverse effects on adherence, particularly given ubiquitous disruptions to accessing care, pharmacies, and the impacts on factors known to influence adherence, such as stress and substance use [72]. Globally, an estimated one in five PLWH were unable to access their HIV care provider, and close to half of PLWH were unable to access ART refills remotely, with the least access occurring in Belarus, Brazil, Kazakhstan, Mexico, and Russia [73]. During the early weeks of COVID-19, Hochstatter et al. [71] reported that 12% of participants missed taking their ART as compared to 5% during pre-pandemic assessments. Similarly, in Argentina 8% of PLWH were unable to take their ART during early COVID-19 [40].

However, adverse impacts of COVID-19 on ART adherence are not universal. In Australia, 99% of PLWH were able to access their ART without interruption [43]. Some studies reported increased ART adherence during early COVID-19. In Atlanta, Kalichman et al. [1] found that adherence increased in a sample of young PLWH from 53% of ART taken pre-COVID-19 to 78% taken in the first months of COVID-19. In New York City, Gwadz et al. [48] also reported some PLWH improving adherence in early COVID-19, with shelter-in-place orders, increased daily routines, and health consciousness forming a basis for improved adherence.

There is little evidence that substance use treatment and harm reduction services were disrupted in the early months of COVID-19 [74,75,76], while HIV testing may have increased in these settings [77]. Finally, in a study of older adults receiving ART, 42% of participants with substance use disorders, individuals reported being able to sustain ART adherence and substance use treatment during periods of early COVID-19 lockdowns, despite feedings of anxiety and social isolation [78].

Conclusions

The COVID-19 pandemic impacts the mental health and structural inequalities of PLWH, and these impacts can be conceptualized within the context of HIV syndemics. However, the degree to which COVID-19’s impacts on PLWH varied from individuals not living with HIV is unclear. Greater risks for severe COVID-19 among PLWH, especially persons who are not HIV suppressed and/or have HIV comorbidities, suggest that the impacts would be greater for PLWH. However, studies that included both PLWH and people not living with HIV found few consistent differences in COVID-19 impacts. One reliable exception was the greater impact of COVID-19 on the persistent healthcare of PLWH. Greater disruption to services would be expected for PLWH given that they are managing a chronic illness that relies on regular contact with health services. The adverse effects of healthcare disruptions along with risk for severe COVID-19 were among the greatest concerns expressed by PLWH. Because COVID-19 is still evolving, with different countries at varying stages in their epidemiology and vaccination rates, understanding the long-term impacts of COVID-19 will require additional research and future reviews. While studies conducted in the first year of the COVID-19 outbreak did not demonstrate clear patterns of impact on mental health and substance use, and some impacts expected by commentators were not fully realized, such as increases in depression, stigma [2], and interpersonal violence [59, 79], future research on the co-occurring COVID-19 and HIV pandemics may tell a different story.