Intersecting epidemics: the impact of coronavirus disease 2019 on the HIV prevention and care continua in the United States : AIDS

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EDITORIAL REVIEW

Intersecting epidemics: the impact of coronavirus disease 2019 on the HIV prevention and care continua in the United States

Spears, Camille E.; Taylor, Barbara S.; Liu, Albert Y.; Levy, Sera M.; Eaton, Ellen F.

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doi: 10.1097/QAD.0000000000003305
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Abstract

Introduction

With the emergence of the novel coronavirus, SARS-CoV-2 and its clinical syndrome, coronavirus disease 2019 (COVID-19), in the United States in 2020, people who are marginalized because of poverty and structural racism have been disproportionately impacted in terms of both COVID infections and exacerbations of chronic disease [1,2]. Marginalized populations, including those with chronic diseases and lack of insurance, were among the first group to be infected as many live in congregate settings and/or work in frontline jobs, such as food service. In addition, this group experienced delays in COVID diagnosis and treatment because of lack of resources and healthcare access. Beyond COVID infection, the pandemic led to disruptions in service delivery for routine healthcare that were more devastating to people who are chronically ill, sexual and gender minority populations, and racial/ethnic minority groups who face structural barriers to care [3–5]. People at risk for, and living with, HIV are at heightened risk for poor HIV outcomes at least in part because of underlying social determinants of health and barriers to care, including poverty, transportation issues, and stigma. The purpose of this review is to summarize the broad impact of the COVID-19 pandemic on HIV prevention and care in the United States with a focus on the status-neutral HIV care continuum.

Dynamic trends in sexual risk behaviors

Although risk behaviors are not built into the traditional HIV care continuum, background transmission risk informs prevention efforts and underscores the importance of testing and linkage to care, and these behaviors evolved significantly in the first year of the pandemic. Early social distancing and perceptions of COVID-19 risk may have precipitated initial changes in sexual behavior and ongoing HIV and sexually transmitted infection (STI) risk but data are mixed on COVID-19's overall impact on sexual behavior [6]. In a cross-sectional online survey among MSM from April to May 2020, there was a mean increase of 2.3 sex partners during early COVID-19, with increases more common in those reporting substance use [7]. In contrast, several studies reported significant decreases in the number of sex partners and/or decreased sexual activity [8–11].

McKay et al. performed a sub-analysis of a survey of MSM from April to May 2020 and found that 9 out of 10 men in the sample reported having either one sexual partner or no sexual partners in the 30 days prior to the survey, a substantial decrease for many. This group also reported changing their methods of sexual activity presumably to reduce risk (e.g. more virtual encounters) [9]. In a sample of 1051 US MSM, Sanchez et al. reported that the vast majority of participants maintained or had a decrease in the number of sexual partners. The use of apps and websites to find sex partners remained high; however, with 49% reporting no change in the use of these sites [11]. Several online surveys showed young MSM, particularly, continued to engage online, and were more likely to report increasing use of social networking apps to connect with men [9,11,12].

Although there are discrepancies in the direction of behavioral changes (increased vs. decreased), there is more consensus in the literature that changes occurred early in the pandemic followed by a rebound effect. Latinx sexual minority men reported an initial increase in sex with a primary partner and fewer sexual partners, followed by ‘quarantine fatigue’ with a return to prepandemic levels of activity, reflecting this rebound effect [13]. Quarantine fatigue may lead individuals to prematurely relax COVID-19 mitigation measures because of weariness or exhaustion and can also be seen with social distancing, masking, and other mitigation measures.

Similarly, in a study of 136 MSM in Amsterdam, participants reported sex with casual partners rebounded to prepandemic levels after 8 weeks [14]. This holds true for other sexual health outcomes as well. After the COVID-19 stay at home orders in March 2020, weekly STI cases in the United States dropped for chlamydia, gonorrhea, and syphilis. However, these declines were transient, with a significant resurgence in reported STI cases by the end of the year 2020; gonorrhea and syphilis cases rose by 135 and 151% of 2019 levels, respectively [15]. As proxies for sexual behavior and risk, this increase in weekly reported STIs raises concern for significant background HIV transmission risk. Thus, early pandemic shifts did not signify a durable decline in the need for HIV and STI prevention and testing efforts.

Impact of coronavirus disease 2019 on the status-neutral HIV care continuum

Challenges to HIV and sexually transmitted illness testing during the pandemic

HIV testing is the gateway to the HIV prevention and care continua and affords an opportunity to offer timely HIV prevention services, linkage to care, and antiretroviral therapy (ART) initiation. In 2019, 87% of people living with HIV in the United States were aware of their diagnosis; however, the Centers for Disease Control and Prevention (CDC) has yet to release data for the year 2020–2021, a period when behavior, prevention, and testing services dramatically changed [16]. The COVID-19 pandemic created a number of barriers to testing and sexual health services, including clinic closures and reduced drop-in services, as well as interruptions to public transportation [15]. Additionally, the demand for COVID-19 testing required re-allocating sexual health services and staff to the COVID-19 frontlines and added to supply chain problems [17]. For example, demand for COVID-19 testing materials led to shortages in Neisseria gonorrhea and Chlamydia trachomatis nucleic acid amplification tests (NAAT) tests, and there were national shortages and delays in laboratory reporting because of increased send out testing with a longer turn-around time [18]. On the basis of testing data from one large commercial lab, HIV testing volume decreased by 18% nationwide in 2020, with the largest declines in the mid-Atlantic and West regions [19]. One study examined testing rates in four United States urban areas and saw a 68–97% reduction in the number of HIV tests per week during each state's shelter in place (SIP) period, compared with pre-SIP. HIV testing levels then remained reduced 11–54% below previous levels even after the areas transitioned to advisory phases [20]. Similar trends were observed in Europe, with a majority of sites reporting more than 50% decreases in HIV, hepatitis, and STI testing volume early in the pandemic [21]. Data from patient and provider surveys indicated numerous barriers in accessing testing and prevention services early in the pandemic. In surveys of MSM during the spring of 2020, 14–32% reported experiencing difficulties getting HIV/STI testing [9,11,12]. In an American Academy of HIV Medicine survey on PrEP users and providers, the intensive SIP period greatly impacted HIV and STI testing. Almost three-quarters of providers indicated they had to delay recommended HIV and STI testing and routine monitoring. Fifteen percent of providers opted to forgo HIV/STI testing and lab monitoring altogether [22].

Berzkalns et al. queried whether early reported declines in STI cases were because of actual reduced STI transmission or simply reduced screening. They examined King County STI surveillance and sexual health clinic data during the pre-SIP, SIP, and reopening periods. The more symptomatic primary and secondary syphilis and male urethral gonorrhea were used as proxies for sexual behavior, given their tendency to cause patients to present for care, whereas asymptomatic and early latent syphilis diagnosis was considered a proxy for STI screening as it was assumed these patients would be identified from regular screening practices. As comparably larger decreases were observed in asymptomatic early latent syphilis, they concluded that a substantial portion of the observed decrease in STI cases may have been because of reduced screening rather than a true decrease in STI transmission [21]. The apparent impact of reduced STI screening on accurate reported diagnoses is concerning, given the aforementioned overall increase of gonorrhea and syphilis in late 2020, which may be an underestimation [15].

Pandemic influences on HIV prevention and preexposure prophylaxis

Decreases in PrEP initiation were seen across multiple geographic areas, age groups, and race/ethnicity groups during COVID-19. Pronounced declines were seen among white individuals in the South. In this group, there was a 21% decrease in PrEP prescriptions overall, and a 28% decrease in the number of new PrEP users during the first 6 months of the pandemic [23,24]. PrEP initiation data from the San Francisco AIDS Foundation Magnet Clinic showed PrEP initiations decreased 62% during SIP, and rebounded post-SIP but only reached 45% of the pre-SIP level. PrEP discontinuations also rose by 21%, and were more common in younger patients [25]. At San Francisco City Clinic, PrEP initiations were on the rise in early 2020 but fell sharply with San Francisco's SIP orders from March to May 2020, and by June 2021 had not returned to pre-SIP levels (S. Cohen, Personal communication, 2021). Several national online surveys of MSM showed respondents, particularly youth, reported trouble accessing PrEP, with one study showing one out of seven young MSM discontinuing PrEP despite 60% meeting CDC criteria to continue [9,11,12]. Latinx sexual minority men and Latinx transgender women also reported difficulty in obtaining prevention services, with a third of a Los Angeles sample reporting difficulty accessing PrEP [4].

Declines in PrEP use were likely multifactorial and may have been in part because of changes in provider behavior, staffing shortages, and clinic access [26]. The American Academy of HIV Medicine surveyed PrEP users and providers on the impact of COVID-19 on PrEP practices. The provider survey showed 90% of providers instituted some form of practice changes during SIP, including increased reliance on telemedicine visits by telephone and televideo and offering PrEP refills without lab testing; 40% prescribed only PrEP refills but avoided PrEP initiations [22]. At the patient level, the majority reported stopping PrEP because of lower risk behavior, and 8% reported having lost access to PrEP. Of significance, one-third of patients reported discontinuing PrEP by April/May 2020 [22]. These early dramatic declines in PrEP initiation and continuation followed by a lack of recovery to prepandemic levels may point to a more durable negative impact in the realm of HIV prevention throughout the first year of the pandemic, at least.

Modeling the impact of coronavirus disease 2019 on HIV/sexually transmitted illness incidence

The durability of changes like these shows significant impact in available modeling studies. Mitchell et al. used a calibrated HIV transmission model for MSM in Baltimore, Maryland to examine the impact of COVID-19-related disruptions on 1-year and 5-year HIV incidence. When it comes to different service disruptions, a 10% reduction in viral suppression had the greatest impact, yielding a 6.4% increase in new infections over the next year [27]. Jenness et al. modeled the impact of clinical service interruption on HIV and STI incidence over time. The model showed that service interruption alone resulted in increased HIV and STI incidence over 18 months but when this was combined with reduced sexual risk behaviors (i.e. sexual distancing), they generally offset each other in terms of incident HIV, with a net protective effect on STIs. However, if sexual distancing only lasted 3 months with service interruptions continuing for 18 months, the model predicted there would be an additional 890 HIV cases and 57 500 STI cases over the next 5 years [28]. In other words, if service disruptions lasted longer than sexual distancing, HIV and STI incidence could experience a steep rise.

Linkage to HIV care and engagement

Similar to challenges in testing and prevention, the pandemic made it harder to engage with patients diagnosed with HIV because of disrupted community testing events, decreased navigator availability, and reduced onsite visits. Furthermore, during the pandemic, many infectious disease-trained physicians and providers who serve as HIV providers have been diverted to cover COVID-19 testing and treatment sites. These disruptions in staffing and visits likely limited initial care linkage, renewals of prescriptions, and reengagement in care.

As a response to shelter in place orders, the Health Resources and Services Administration's Ryan White HIV/AIDS Program encouraged providers for people with HIV (PWH) to use telemedicine to allow patients to stay at home and avoid delayed prescriptions [29]. Many HIV providers transitioned to an increased number of telemedicine visits and services [30–34]. Telehealth served a vital role in closing service gaps and allowed many providers and patients flexibility to continue healthcare engagement; however, it posed new challenges for many patients. Many patients did not have reliable internet or mobile phones to utilize these services and this likely deepened existing disparities for these groups [35]. African American clients, those with public insurance, and those with detectable viral load appeared to be less likely to engage in telemedicine [36,37]. Telemedicine visits may prompt privacy concerns and preclude point of care, wrap around services (e.g. counseling, housing, and nutrition services) provided by many brick and mortar multidisciplinary clinics. Tedaldi et al.[26] examined data from the HIV Outpatient Study (HOPS) and found that small increases (2%) in telemedicine visits did not outweigh a larger decline (26%) in office visits. However, perhaps as a testament to the resilience and flexibility of providers and patients alike, telemedicine enabled visit completion, both unchanged or increasing rates with a majority of telemedicine visits, and some sites actually reported a mean increase in overall visits compared with 2019 [31,32,34].

Although telemedicine is successful in bridging gaps to care, it also presents barriers to linkage to care for some patients. Lara-Paez et al. examined care linkage and reengagement at the UC San Diego Emergency Department (ED) through an existing opt out HIV and Hepatitis C screening program. They noted that uninsured patients that needed to enroll in federal assistance programs were switched to virtual visits [38]. This may have created challenges for individuals with structural barriers of homelessness, unemployment, and racism. The digital divide is well documented and is a tremendous barrier to PWH from racial/ethnic minority backgrounds and those with limited resources. African Americans, rural patients, and those living in poverty are all less likely to utilize health information technology (i.e. patient portals), own a personal computer, or to have internet access [36,37]. Lara-Paez et al. showed requirements, such as proof of income, residency, and picture ID were additional barriers to enroll in assistance programs. Before the pandemic, individuals newly diagnosed with HIV in the San Diego Emergency Department were scheduled for their initial appointment within a week of diagnosis but in early 2020, visits were pushed out to a median of 2.5 weeks. The greatest delays were experienced by patients aware of their HIV-positive status who had fallen out of care with earliest appointments usually 3–4 weeks after the initial Emergency Department visit.

Retaining patients in care has its own challenges with telemedicine, provider shortages, appointment cancellations, and prescription delays. Yet, retention and patient experience varies by location and race. Fadul et al. showed retention in care in an academic HIV clinic in Nebraska was down from 69 to 40%, and the number of patients with no visit at all for over 6 months increased from 14 to 25%. Others, however, reported that visit completion rates did not decrease [31–33]. In a New York City survey of people of color with longstanding HIV, 70% reported visits cancelled by providers and 2% stopped ART; however, 40% actually reported increased medication adherence because of COVID-19-related concerns [39].

Antiretroviral therapy adherence and viral suppression

Disruption in care services, decreased access to antiretrovirals, and deepening socioeconomic vulnerabilities, including a loss of social support, stable food and housing, may have affected ART adherence and success [40]. Viral suppression data is mixed, with some reporting increased viral loads post-COVID-19 and others with no changes in virologic suppression [30–32,41]. One San Francisco clinic saw 31% higher odds of detectable viral load after SIP, despite stable retention-in-care and visit volume with a disproportionate impact on homeless individuals [31]. Data from a Brooklyn, NY clinic comparing 2019 and early 2020 showed stable virologic suppression but the proportion of patients with CD4+ cell counts greater than 200 decreased from 92.6 to 78.3% [41]. Although these differences in controlled disease were varied across studies, the aforementioned models have shown that even small changes can have profound consequences [27,28].

The power of these small but durable disruptions in the status neutral care continuum are a reminder of the importance of each moving part of HIV care. Barriers to testing, prevention, linkage, adherence, and virologic suppression ultimately present major challenges to reduce the incidence of HIV as we move through the pandemic (Table 1). Beyond these traditional steps in the continuum, mental health and substance use underlie and intersect with all stages of HIV prevention and care, and have provided additional challenges for the communities we serve.

Table 1 - Observational studies reporting changes in steps in the HIV Care Continuum pre, during, and post shelter in place orders.
Care continuum step Setting Timeframe Impact
Testing National reference laboratory [19] 2020 HIV testing volume decreased 18% nationwide, largest declines in mid-Atlantic and West
New Orleans, Minneapolis, Providence, and Seattle [20] January 2019 to December 2020 Weekly HIV tests decreased 68–97% during each location's SIP period compared with previous level, and HIV testing remained at 11–54% lower level after SIP
PrEP engagement San Francisco [25] July 2019 to March 2020 PrEP initiations decreased 62% during SIP, rebounded post-SIP to 45% of the previous level, discontinuations rose 21%
National online survey [22] 21 April 2020 to 15 May 2020 33% discontinued PrEP by May 2020
HIV care engagement Baltimore [33] Pre-SIP: 14 weeks pre 16 March 2020 vs. SIP: 14 weeks post 16 March 2020 Visit completion: 79% pre and 82% post, 82% of visits were TM and 70% of TM via phone
HOPS [34] January 2010 to June 2020 26% decline in office visits between December 2019 and June 2020 (despite 2% increase in TM visits)
San Francisco [31] Pre-SIP December 2019 to February 2020 vs. SIP April 2020 Visit completion unchanged: pre-SIP 69%, SIP 70% (54% TM)
Boston [32] Pre-SIP 2019 vs. SIP March to April 2020 Drop in in-person visits but increase in telemedicine led to mean visits/month higher than same months in 2019
Nebraska [30] Pre-SIP FY2020 vs. SIP March to June2020 Retention in care down from 69 to 40%, no visits more than 6 months up from 14 to 25%
Viral suppression San Francisco [31] Pre-SIP December 2019 to February 2020 vs. SIP April 2020 Odds of detectable VL 31% higher during SIP
Boston [32] Pre-SIP 2019 vs. SIP March to April 2020 No difference in viral suppression pre-SIP (77%) vs. SIP (74%)
Nebraska [30] Pre-SIP FY2020 vs. SIP March to June 2020 No difference in viral suppression pre and during SIP (both 91%)
SIP, shelter in place; TM, telemedicine; VL, viral load.

The intersection of coronavirus disease 2019, mental health, and substance use

Significant mental health and substance use challenges existed in the United States prior to the pandemic for gender and sexual minority populations, as well as those living with HIV. The CDC reported that by June 2020, approximately 4 months into the pandemic, 40% of US adults reported struggles with their mental health. This same CDC survey showed mental distress impacted many different populations, including individuals with no history of mental illness, younger adults, racial and ethnic minorities, and essential workers [42]. Among PWH, depression and substance use are common, and given that the two often interact, these interacting elements constitute additional barriers to HIV and addiction care [43–45].

Overall health, physical activity, and lifestyle patterns shifted with shelter in place orders. Several international studies have demonstrated that the general population shifted to more unhealthy food consumption patterns and lower levels of physical activity, factors that are known to intersect with mental health [46–48]. These changes in diet and lifestyle may disproportionately burden communities of color, poor communities, and PWH [49,50]. The significant and varied stressors of the pandemic likely worsened the already high prevalence of mental illness among gender and sexual minority populations, as well as PWH. Studies among gender minority populations showed barriers to gender affirming care may have exacerbated mental health stressors, and reports of mental health challenges in these groups increased during the pandemic [3,4,11,51]. Participants in a survey of Latinx sexual minority men and transgender women reported increased alcohol consumption (23.1%), problems with sleep (67.3%) and mental health difficulties (78.4%), and half reported loss of employment [4]. Sexual and gender minority (SGM) groups had significantly higher levels of depression, post-traumatic stress disorder (PTSD) symptoms, and COVID-19-related worries and grief than non-SGM, even when controlling for minority stress factors of family support, lifetime discrimination, and preexisting mental health diagnoses [52]. Sanchez et al. collected data on psychosocial impacts of the COVID-19 epidemic among MSM. A significant proportion of their sample reported decreased sleep quality, decreased connection to family, and approximately 20% reported a loss of employment because of the COVID-19 pandemic [11]. PWH also commonly reported feelings of isolation, hopelessness, and worry related to the pandemic [40]. A survey of Ryan White providers found declines in mental health to be the top stressor faced by clients, followed by job loss, and decreased access to support services [26].

During the COVID-19 pandemic, the general population of Americans experienced an increase in reported anxiety, as compared with the year prior [53]. Given that many individuals living with HIV also experience mental illness, it can be presumed that anxiety may have increased in this population during this time, as well. The Sanchez et al.[11] study previously referenced found an increase in reported anxiety during the beginning months of the pandemic, with the highest reports being made by participants over the age of 25 years. A different study utilizing a qualitative approach with 16 participants from Ryan White clinics in Pennsylvania discovered that a recurring theme in interviews was concern and worry about living with HIV during this time. More specifically, participants expressed a fear of disrupted HIV services, acknowledging that they have a compromised immune system [54]. In contrast, a sample of predominantly black and Hispanic individuals living with HIV, residing in a poor urban sector of Miami, Florida, reported fewer anxiety symptoms during the pandemic, compared with HIV-uninfected participants. Further, these individuals appeared to have less COVID-related worry, when compared with their HIV-uninfected peers [55]. Authors from this study suggest that individuals living with HIV have gained resilience through chronically living with a potentially deadly disease (HIV infection), and are better equipped to cope with pandemic-related psychosocial stress. However, COVID-related anxiety in PWH is worthy of ongoing investigation, as other studies have found this group to be especially vulnerable to anxiety and mental illness [52,56,57].

Beyond the social and economic challenges of the pandemic, there are important direct neuropsychiatric effects of SARS-CoV-2 infection, which may be more debilitating in persons with chronic diseases, such as HIV. Known neurological consequences can include impaired consciousness, immune-mediated neuropathies, encephalopathies, and large-vessel strokes [58]. Many individuals, including those living with HIV, have now experienced postacute sequelae of COVID-19 (PASC), the lasting and/or evolving symptoms of COVID-19 after the initial phase of acute infection. Although direct causality is difficult to establish with current limited studies, one systematic review by Rogers et al. helped to substantiate the connection with increased incidence of depression, anxiety, fatigue, and insomnia following COVID-19 [59]. Data in populations living with HIV are limited, however. One group of PWH in India with PASC reported close to 20% experienced fatigue and 10% had persistent symptoms at 109 days [60]. There are few studies in the United States with data on PASC or direct neuropsychiatric effects of COVID-19 infection in PWH, and this area of research needs increased attention.

As mental illness increased, substance use rates climbed beyond what was an already worsening drug use and addiction epidemic prior to COVID. In 2019, nationwide use of opiates and methamphetamines was already on the rise [61]. From 2014 to 2018, the annual number of diagnosed HIV infections attributed to injection drug use was increasing [62]. After the arrival of the pandemic, the CDC reported 13% of US adults started or increased substance use to cope with stress or emotions related to COVID-19. This trend continued and impacted patients with regard to substance use and access to HIV prevention and treatment. Young MSM reported increases in alcohol and drug use, as did Latinx sexual minority men and Latinx transgender women [4,11]. A follow-up survey in the fall of 2020 on a cohort living with HIV showed a high prevalence of anxiety and depression, 27.1 and 27.9%, respectively. And concerningly, substance use levels actually increased from a previous survey in April 2020 [56,57]. Those with substance use disorders experienced challenges in accessing care. In one study focused on people who inject drugs, while most did not report barriers to accessing HIV/STI testing, 42% reported difficulty accessing an appointment with a doctor, while a quarter had trouble accessing PrEP, and 20% stopped PrEP altogether [63]. Of those living with both HIV and substance use disorder, illicit substance use increased during the pandemic as did the proportion of people missing their HIV medications. PWH and substance use disorder reported decreased confidence in their ability to stay sober and attend recovery meetings, as well as decreased confidence in their ability to attend HIV follow-up appointments [64]. These trends are especially problematic as untreated mental health and substance use disorders can increase HIV risk behaviors and decrease ART adherence, which in turn increases HIV transmission, morbidity, and mortality [43–45,65,66]. The many intersecting mental health and substance use challenges during the pandemic underscore the need for the continued development of integrated HIV, mental health, substance use, and COVID-19-related services.

Models for innovation, new directions

Despite the many disruptions to the status neutral care continua and surrounding forces at play, PWH, providers, and health systems have demonstrated resilience and innovation to combat the challenges of the pandemic (Table 2). Many innovative testing and PrEP delivery models should be considered for routine care beyond the pandemic in order to reach all persons at risk for and living with HIV. Expansion of testing methods, changes in PrEP dispensing, and adoption of telemedicine helped to close gaps in testing and prevention. Home HIV testing was used to circumvent staffing and clinic shortages. Between March 2020 and March 2021, a novel public–private partnership distributed more than 5000 free HIV self-test kits tailored for MSM across 17 health jurisdictions; 36% of participants reported they had never tested, 56% had tested over a year ago, and approximately 10% reported accessing STI testing and PrEP services after using a self-test [67]. Participants found the testing easy to use, discreet, and well tolerated [68]. Carnevale et al. at New York Presbyterian also launched a home HIV/STI testing program, which coupled home test kits with a video visit in which a provider reviewed their sexual history, discussed PrEP adherence, and reviewed the use of the kit. Between April and July 2020, they mailed over 200 test kits, of which 74% were returned for processing. There were no cases of HIV identified but 19 patients tested positive for gonorrhea or chlamydia, all of which were asymptomatic and treated [69].

Another novel testing strategy that arose during the pandemic was linkage of opt-out HIV testing with SARS-CoV-2 testing. Stanford and colleagues described a program of linking universal HIV screening with COVID-19 testing in the University of Chicago Emergency Department. Although HIV testing across 13 health centers in Chicago decreased by nearly half in the first quarter of 2020, the Emergency Department program maintained HIV screening volumes with more than 14 000 tests conducted during 2020. Moreover, they detected 12 acute HIV infections, which was more than double compared with the prior 4 years. Importantly, 11 of these 12 presented with symptoms consistent with COVID-19, suggesting that these diagnoses may have been mistaken, missed, or delayed without this linked testing [70]. Zang et al.[71] modeled the effects of linked opt-out HIV testing in six US cities, and showed that linking HIV and COVID testing could avert between 500 and 7200 new HIV infections. Universal testing in cases of acute viral sequelae should be an enduring practice long after the pandemic.

In response to the pandemic's impact on HIV prevention, the CDC issued a ‘Dear Colleague’ letter to encourage PrEP retention in resource-constrained settings and emphasized that PrEP is an essential service. Important provisions included lab-only visits, home HIV/STI testing if available, and extended prescriptions, such as a 90-day supply of medication [72]. Since the start of the pandemic, PrEP prescribed via telemedicine (telePrEP) has proven successful. Hill et al. demonstrated that, in three Midwest states, clinics were able to sustain a similar number of PrEP visits in 2020 compared with 2019; the major difference was that 74% of visits were telemedicine visits in 2020, as compared with all in-person visits in 2019. Importantly, a significantly greater proportion of health visits were PrEP visits, indicating that PrEP visits were being prioritized during the pandemic [73].

Pharmacy-led models provide another novel approach to increasing PrEP access during the pandemic. Pharmacies, such as Kelly Ross Pharmacy in Seattle, Mission Wellness Pharmacy in San Francisco, a regional telePrEP program led by University of Iowa and Iowa Department of Public Health, Equitas Health in the Midwest, and others have been able to offer one-stop PrEP services, allowing patients to bypass the clinic. Several groups have developed pharmacy-driven telePrEP models, where pharmacists conduct initial consultations remotely, and after lab testing either at home or at a local lab, medications get mailed to the patient. These low-barrier PrEP programs have demonstrated high levels of PrEP initiation and retention and serve as models of PrEP care delivery beyond COVID [74–76].

Many of these programs have been successful in caring for difficult-to-reach populations using care integration, linking emergency care, COVID-19 testing, and pharmacy services to improve HIV care continuum outcomes. Other programs have incorporated HIV testing into temporary housing programs during the early pandemic, combined intensive telemedicine case management, and even emergency financial assistance and walk-in clinics with multidisciplinary teams and financial incentives [77]. Integrating care for substance use and HIV is a well recognized strategy to reach and retain vulnerable patients in care, and the pandemic adds an opportunity to incorporate COVID-19-related testing, treatment and social services into care [78]. One program in San Francisco used a high-intensity low-barrier ‘POP-UP’ program to care for 85 patients experiencing homelessness and care engagement; clients experienced sustained viral suppression in the 5 months following implementation [79]. An integrated HIV and Opioid Use Disorder Clinic in Birmingham, Alabama saw an increase in the number of clinic visits per patient from a median of three to four visits over the 6 months following SIP orders, and viral load suppression remained high [80]. Programs like these remain critical, even beyond the pandemic, and should be modeled to reach marginalized populations. Table 2 includes a summary of COVID-19-related challenges and interventions in HIV service delivery.

Table 2 - Innovations and scale up of HIV-related programs to adapt to the coronavirus disease pandemic and associated barriers.
Challenges to HIV prevention and care Recommended interventions Anticipated barriers
Testing: clinic closures, reduced drop-in services, interruptions to public transportation, supply chain problems [15,17] Expansion of home-based HIV and STI testing [68,69] Awareness of risk, testing needsLinking positive tests to care
Linked COVID/HIV testing and integrated care models for patients experiencing homelessness or with substance use disorder [77,79,80,81] Work forceLack of integrated HIV and social services
PrEP initiation and continuation: provider avoidance of PrEP initiation, patient perceptions of lower sexual risk, loss of patient access because of staffing shortages [22,26] Pharmacy-led models of PrEP delivery [74,75]Telehealth platforms [76]Multimonth and mail order PrEP [76] Training personnelScope of practice restrictions
Care engagement and viral suppression: stay at home orders, delayed visits and prescriptions because of staffing shortages [15,17,29] Adoption of telehealth and other mobile health platforms for ART [30–34,82] Privacy concernsAt least one out of four people in United States may not have digital access or literacy [83,84]
Community hubs for ART distribution and lab monitoring [76,77,79,80] Work forceFinancial resources
Home delivery of medications [17] Privacy concerns
Multimonth ART [85] Financial resources
Distribution systems
ART, antiretroviral treatment; COVID, coronavirus disease; PrEP, preexposure prophylaxis; STI, sexually transmitted illness.

In closing, the pandemic has heightened disparities for people at risk for, and living with HIV, as well as exacerbated substance use and mental illness, to which PWH are uniquely vulnerable. HIV risk behaviors have fluctuated, and access to sexual healthcare and has been sporadic. Hence, the challenges of delivering prevention and care services in a pandemic have not only been especially disruptive for HIV status neutral continuum outcomes but also impact comorbid diseases like mental illness. But, there is hope. Through integration of HIV and SARS-CoV-2 services, innovative telemedicine strategies, and outreach to PWH beyond brick and mortar HIV clinics, many health systems and clinics have achieved and maintained engagement in HIV prevention and care. We must build on these strategies to create health systems that are durable and accessible through future public health crises, and we must continue to advocate for policy that supports these services through fair compensation [81].

Acknowledgements

We would like to thank Dr Wendy Armstrong and the Infectious Disease Society of America for convening a symposium in which some of the information in this manuscript was presented.

C.S. performed literature review, drafted the manuscript, and made edits throughout. B.T., A.L., E.E. performed literature review, critically reviewed the manuscript, and made substantive edits. S.L. drafted the abstract, and made substantive edits. All authors critically reviewed the final version of the manuscript and gave their final approval.

Conflicts of interest

There are no conflicts of interest.

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Keywords:

antiretroviral therapy; coronavirus disease 2019; HIV; mental health disorders; preexposure prophylaxis; sexual risk behaviors; substance use

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