Introduction

The coronavirus disease 2019 (COVID-19) pandemic began in Wuhan, China in 2019 and quickly spread to the rest of the world. This virus has had profound consequences worldwide but especially in low-and-middle income countries (LMIC), where healthcare and related resources are typically sparsely available and inequitably distributed [1]. Latin America and the Caribbean (LAC) has been hit hard by COVID-19. The first confirmed COVID-19 case in LAC happened in Brazil on February 25th, 2020 [2], and the first death was reported in Argentina on March 7th, 2020 [3]. By March 19th, every Latin American country had reported cases of COVID-19. The region has had one of the highest COVID-19 death rates in the world, due to a combination of political instability, corruption, flawed health systems, and deeply ingrained structural inequalities [4••].

The literature suggests that the presence of comorbidities, such as coronary artery disease, obesity, diabetes, and hypertension, are important risk factors for severity of COVID-19 [5, 6]. However, there is also growing concern for the direct and indirect effects of COVID-19 on people with other chronic conditions, such as HIV infection. The impact that COVID-19 could have on this population is complex: Although people living with HIV (PLWH) could potentially develop abnormal cellular and humoral responses leading to higher risk of infections, in the past couple of decades, access to ART has enabled PLWH to live longer by achieving viral suppression [7, 8]. However, they are exposed to the additive challenges of long-term secondary effects of lifelong medication and HIV infection, possibility leading to early manifestations of other chronic comorbidities like cardiovascular or metabolic pathologies, both of which might put them at higher risk of COVID-19 adverse outcomes [9]. Another aspect to consider are social determinants of health which could place PLWH at a higher risk of exposure. Moreover, the pandemic and consequent establishment of nationwide lockdowns could have affected various services for PLWH, including testing, preventive interventions, and treatment [10].

In 2019, the UNAIDS estimated that at least 2.4 million people live with HIV in LAC. There has been a slow progress in the region achieving the UNAIDS 90–90-90 goals: In 2019, 60% of PLWH were on antiretroviral therapy (ART) and 53% had achieved viral suppression compared to 53% and 44% in 2015. Additionally, since 2010, new HIV infections are on the rise in LAC, with 21% more new infections, and only 8% decrease on AIDS-related deaths [11]. In this context, it becomes urgent to understand the effects and impacts that the COVID-19 pandemic may have on PLWH in LAC. In this review, we summarized the interactions between the HIV and COVID-19 pandemics in the region of LAC.

Impact of HIV on the Infection Risk and Severity of COVID-19 in LAC

Early in the pandemic, there were global concerns about the interactions of HIV and COVID-19 based on studies showing higher mortality in PLWH compared with general population during seasonal influenza [12].

However, studies mainly from Europe and the USA suggest that PLWH are not more susceptible than the general population to SARS-CoV-2 infection, but they are more likely to be tested and to have similar clinical outcomes than patients who are HIV negative [13], although the largest population-based study to address the risk of death from COVID-19 on PLWH, done in South Africa, found a higher mortality rate in this population, which could be associated with the burden of other comorbidities [14].

The Latin American literature on the impact of HIV on the infection risk and severity of COVID-19 is scarce, and mainly based on case reports or small case series. A study from Mexico City based on a single-center review of eleven HIV-infected patients diagnosed with COVID-19 between March and May 2020 found that only 9/11 PLWH were hospitalized, most have comorbidities (obesity 70%, hypertension 30%), and despite critical clinical presentations, most made a full recovery. They conclude that outcomes were similar to those seen for HIV-negative persons [15]. An observational study in Chile recruited all PLWH with confirmed SARS-CoV-2 infection and hospitalized in any of 23 hospitals of eight regions. Of the 15 patients enrolled between April and June 2020, 92% were men with a mean age of 44 years old and 80% were on ART and good virologic control. PLWH were more likely to be admitted to an ICU, but the rates of mechanical ventilation and death were similar to that of the Chilean general population. Hypertension and cardiovascular comorbidities were the most important risk factors for mortality in these PLWH [16••].

PLWH remain susceptible to COVID-19 even when virally suppressed, or when receiving ART in both out-patient and in-patient settings [17]. A case report from Peru highlighted the potential for in-hospital-acquisition of COVID-19 in PLWH hospitalized for HIV-associated complications [18]. ART was previously hypothesized to affect the course of COVID-19 in PLWH due to antiviral activity. Some antiretroviral drugs, such as lopinavir-ritonavir, have already been shown not to be effective in hospitalized patients with COVID-19 [19,20,21]. However, other studies seem to suggest a positive effect of chronic ART on COVID-19 outcomes in PLWH [22]. Tenofovir/emtricitabine might have a protective effect, though there is no definitive evidence yet [23]. A case series of 8 HIV-infected kidney transplant recipients in Brazil seemed to suggest that ART does not mitigate the poor outcomes of COVID-19 in this population, though they have the additional risk factor of solid organ transplant-related immunosuppressive treatment [24].

Other coinfections have been described in Latin America during SARS-CoV-2 infection in PLWH. One case from Argentina described a woman with a new diagnosis of advanced HIV, diagnosed with COVID-19 and Pneumocystis jirovecii simultaneously, who had a favorable evolution after treatment [25]. Histoplasma capsulatum is an emergent systemic fungal infection in several Latin American countries, with an estimated median seropositivity of 22% in the general population and even higher infection rates in PLWH [26]. This fungal infection has been reported as a coinfection in PLWH and COVID-19 in a few case reports [27,28,29]. Another coinfection described in the literature is SARS-CoV-2 and Mycobacterium tuberculosis in PLWH, which is a matter of concern and has not been well studied [30, 31]. Mycobacterium tuberculosis coinfection detection and prompt treatment are crucial as it could increase COVID-19 susceptibility, and have been well described as an independent risk factor for COVID-19 severity and mortality, irrespective of HIV status [32, 33]. For PLWH, the risk is even higher, as tuberculosis is already the leading cause of death among this population, accounting for about 270,000 deaths in 2019 [34].

These case reports reflect the importance of investigating coinfections in SARS-CoV-2/HIV patients, and of having readily available diagnostic tests according to the local epidemiology.

Impact of the COVID-19 Pandemic on HIV Prevention and Care of PLWH in LAC

The collision of COVID-19 and HIV has disrupted the global HIV response and its advance, since services and supply chains have been affected [35].

In March 2020, the World Health Organization (WHO) released operational guidelines to maintain essential health services throughout the COVID-19 pandemic [36]. It was followed by another document in June 2020, which emphasized the importance of maintaining an effective HIV response during the public health emergency through multi-month prescriptions and dispensing of PrEP, ART, and prophylaxis for common comorbidities; enabling of community dispensing points; implementation of online or telephone counseling for HIV testing while prioritizing high-risk individuals; implementation of HIV self-testing (HIVST); and reducing viral load testing to every 12 months unless there is a clear clinical indication [37]. The Pan American Health Organization (PAHO) also released at the beginning of the LAC pandemic recommendations on COVID-19 prevention and HIV care delivery adjustments to be made [38]. However, these recommendations have been followed to varying degrees across countries in LAC.

HIV Testing and Prevention

There has been clearly a decrease in routine HIV testing worldwide in 2020 [35]. The WHO recommends HIVST as an additional strategy for HIV prevention [39, 40]. The utility of HIVST in LAC is worth noting as it has the advantages of reducing the risk of contagion associated with use of public transport, reducing lines in facility-based HIV testing, and avoiding the issue of privacy given stigma often associated with HIV in LAC [41].

One survey of 680 Brazilian MSM on PrEP found that the willingness to use HIVST was 79% and 32% had HIVST during the quarantine [42]. HIVST has also been proposed in the Caribbean as a measure to mitigate the lack of routine HIV testing in laboratories and minimize risk of exposure and infection; however, only the Bahamas and Jamaica have implemented guidelines on its use [43••].

Although there are no reports of the lack of barrier prevention methods from LAC during 2020, the COVID-19 pandemic is expected to have had adversely affected the supply chain by disrupting the manufacture of components of condoms and by delaying their transportation particularly in LMIC [44, 45]. Reductions of equipment and staff involved in the provision of sexual and reproductive health services during the pandemic, closure of clinics offering these services, and reluctance of persons to attend health facilities for these services may also affect the distribution of barrier prevention methods.

However, there is one publication of successful implementation of condom and PrEP home delivery as part of a study with Brazilian adolescent men who have sex with men (MSM) and transgender individuals [46].

Brazil has been offering free access to PrEP to high-risk populations for HIV infection since 2018 [47]. During the pandemic, they continue providing these services introducing different strategies like extending the dispense to 120-day supplies [48]. A study conducted in southeastern Brazil with sexual minority populations reported that nearly 70% continued daily oral PrEP during the pandemic, and among those who reported having stopped it, the most common reasons were impediments to pick up their PrEP refills at their HIV clinic [49]. Another study of patients from Sao Paulo, Brazil found that oral PrEP use was associated with lower self-reporting of COVID-19-related symptoms during the pandemic after controlling for confounders such as age and social distancing frequency [50]. Nonetheless, the number of people benefiting from PrEP in Brazil seems to have continued to grow steadily despite the pandemic, with 8108 people starting in 2018, 8536 in 2019, and 10,120 until October, 2020 [51]. Conversely, worldwide, there seem to be diminishing numbers of people receiving PrEP, perhaps in part due to a reduction in sexual activity due to social distancing recommendations, interruptions in supply chains, and lack of access to services [52].

Access to HIV Care

Early in the pandemic, modelers estimated that HIV mortality in the next 5 years could be increased by 10–36% depending on the level of disruptions on HIV services, especially in the provision of ART [53]. The UNAIDS has been working with countries trying to track the HIV service utilization which has been showing, when the data is available, clear disruptions in many countries, with important drops in treatment coverage in LAC in countries like the Dominican Republic, Guyana, and Peru [35]. There have been also reductions in the number of PLWH initiating treatment in several countries, with at least one country from LAC, the Dominican Republic, with a steady and worrisome decline.

Attempts have been made by Ministries of Health in LAC to maintain the ART supply during the pandemic. New guidelines have been set up to ensure continuity of care for PLWH while reducing their risk of infection during the pandemic. These guidelines include, for example, multi-month prescriptions of ART and permitting pickup of ART by healthy family members [51, 54,55,56,57,58]. An article written by a Brazilian government representative stated that there had been no decrease in the number of people being treated for HIV in the country due to the national HIV program measures implemented [51]. However, an independent report found that the slowing down of government-run AIDS programs due to stay-at-home orders had forced non-governmental organizations to step up and ensure that PLWH received much-needed ART [59]. In a study of Brazilian sexual minorities with a large population of PLWH, 18% reported poor ART adherence during social distancing [49], emphasizing the variability in availability of ART and barriers to their access across the same country [60, 61].

At the start of the pandemic, Costa Rica quickly assembled special teams and locations, and enabled electronic prescriptions and mailing of medication to chronic patients to ensure continuity of ART, but the results were mixed. One local news outlet reported that though there was no shortage of medications, patients experienced delays of up to 15 days in receiving ARTs. Additional barriers to receiving treatment were identified for indigenous and remote communities, communities living in poverty, and undocumented migrants, partly due to lack of connectivity [62].

In a study among middle-aged to older Peruvians with HIV, PLWH reported difficulty accessing ART due to clinic closures or long lines; however, 97% reported adherence with ART [63••].

Caribbean countries are facing the challenges of overcrowded hospitals and limited access to healthcare workers, increasing the risk that patients with HIV may not initiate appropriate treatment in a timely manner [64]. In one study of patients with HIV in Haiti, the mean number of HIV visits fell from 121.5 to 92.5 visits over a 16-week period, and an abrupt decline of ART refills by 18%, demonstrating the changes in HIV care utilization that occurred in Haiti during the pandemic [65].

Several LAC countries have implemented guidelines that promote using mobile phones and social networks to monitor stable patients, and teleconsultations for those that require visits. Some have opted to space out appointments for stable patients, and most have postponed CD4 and viral load measurements indefinitely [54,55,56,57]. One multi-country Latin American survey including HIV services participating in the Caribbean, Central and South America network for HIV epidemiology (CCASAnet) and additional Brazilian HIV care sites in Argentina, Brazil, Chile, Haiti, Honduras, Mexico, and Peru found that most surveyed sites reported decreased hours and providers for HIV care (11/13 sites), increased use of telehealth (12/13), and suspension or deferral of routine HIV appointments (12/13) [66]. In Brazil, the government has begun to implement telemedicine services, and digitized laboratory exam requests, certificates, and prescriptions [51]. Nearly one-third of Brazilian PLWH in one study reported changing the form of HIV care received from in-person care to teleconsultation [67]. In another study of Brazilian PLWH, 21% had a PrEP teleconsultation during the pandemic with 70% reporting it as acceptable [68]. In one Argentinian study, 35% of respondents reported being unable to access medical care due to lack of connectivity, but only 4% reported problems obtaining ART [69]. This demonstrates that longer supplies of ART provided by clinics may have prevented ART interruption despite lack of access to an HIV care provider. Similarly, another study of MSM (including respondents from Brazil and Mexico and a substantial proportion of PLWH) found that 23% lost access to their HIV providers due to quarantine measures and only 17% had access to telehealth services [70]. Despite the acceptability of telemedicine among 70% of Brazilian PLWH [42], the reality of implementation of these services faces the challenges of clinics not having the equipment for telehealth services and patients not having access to smartphones or stable internet connections.

Overlap Between HIV-Related and COVID-Related Stigma in LAC

Stigma associated with HIV is known to be prevalent in LMIC and is detrimental to HIV care, particularly in that it prevents PLWH from receiving care for fear of being persecuted or rejected from their communities [71]. The authors of one study have proposed that some drivers of stigma related to COVID-19 significantly overlap with those observed during the HIV pandemic and the Ebola outbreaks, including lack of information or misinformation and misconceptions about how the disease spreads [72]. This may lead to specific individuals being singled out as causes or carriers of the disease, increasing the stigma associated with the disease. Fear of contagion drives prejudice and stereotypes of the individuals affected by the disease. Even healthcare workers face stigmatization as they are seen as possible carriers of the disease. Policies that single out and separate vulnerable groups of people for their own protection or the protection of others also bolster stigma associated with the disease.

In Latin America, in particular, groups that are known to be more vulnerable to both HIV-related and COVID-19-related stigma include those in poverty or informal workers, minority ethnicities, and persons of genders or sexual orientations that may be chastised for their sexual preference given religious and sociocultural factors in LAC [4••, 72]. Notably, in LAC, several countries including Panama, Peru, and Colombia (only in Bogota) implemented policies to enforce physical distancing and mobility restrictions on its citizens based on binary understandings of gender. On alternating days, either men or women could go outside for their daily needs, further validating these gender-based binary ideologies that are often accepted as “norms” in many LAC cultures. These laws placed transgender people in a gray zone of when they are legally allowed to access services such as food and medical supplies [73].

Mental Health Impact of the COVID-19 Pandemic on PLWH in LAC

PLWH are known to be at higher risk of mental health challenges compared with the general population [74]. And given other vulnerabilities common among PLWH in LMIC (poverty, being informal workers, food insecurity, etc.), mental health impacts are particularly important to be explored in PLWH in LAC during the pandemic. Community-based support groups, which may have helped PLWH to cope, have often had to be suspended during the lockdowns. The multi-country Latin American survey on HIV services mentioned before in this article found that in 12 out of 13 participating sites, community-based support activities had to be partially or completely canceled due to the pandemic [66]. One international study consisting of nearly 30% PLWH from Brazil found that nearly one-quarter reported depressive disorders and 16% reported both anxiety and depression, which was less than the reported frequency of mental health disorders among PLWH prior to the pandemic [67]. In another study in Peru, 64% of the PLWH surveyed reported increased stress and 77% reported increased anxiety during the pandemic [63••].

In a survey among 1336 PLWH from Argentina, 11% reported disruption of their routine mental health services, 33% reported less adherence to ART and 1.3% disruption of substance abuse treatment. Among those who endorsed more resilience in coping, the relationship between economic hardship and mental health challenges was mitigated by their resilient coping style [69]. In another study including the same group of PLWH from Argentina and another group of PLWH from the USA, social support and resilient coping skills contributed to lower rates of depression among Argentinian compared with the American PLWH [75]. This highlights the importance of continuation of mental health services, particularly, mental health interventions that focus on building resilience and more adaptive coping skills during this tenuous pandemic period [76].

Socioeconomic Impact During the Pandemic Among PLWH in LAC

Economic hardship and food insecurity have increased during the pandemic worldwide. In Peru, a study with PLWH showed that nearly half of those who were employed prior to the pandemic reported job loss [63••]. A survey in PLWH from Argentina reported that more than 40% experienced economic hardship during the pandemic [69]. Food insecurity is associated with suboptimal ART adherence and poor HIV control. The increased risk of food insecurity among PLWH and the socioeconomic hardship and high prevalence of informal workers without steady contracted wages in LAC put PLWH in LAC at potentially higher risk of ART non-adherence and poor virologic control [77].

Lessons from HIV Applied for the COVID-19 Pandemic from LAC

Four decades ago, the HIV pandemic swept through the world, affecting health systems and socioeconomic structures everywhere. Since then, almost 32 million people have died of HIV-related causes around the globe [78]. Similarly, the COVID-19 pandemic has also shaken the world’s foundations, exposing the great inequities in our countries—especially in the LAC—and the weaknesses of our health systems and exacerbating social, political, and economic issues. Despite differences in these viruses, both HIV and COVID-19 generate fear, stigma, and anxiety related to transmission concerns, and both tend to affect marginalized communities with intersecting identities, exacerbating disparities that are already very prevalent in LAC, as evidenced by the disease risk and case fatality rates in the region [79]. Though the overall health status of individuals in LAC has improved in the past decades, progress remains unequal across and within countries. Furthermore, many LAC nations have important gaps in health access caused by political instability, budgetary constraints, and fragmented health services, among other issues [4••].

The HIV epidemic has taught us that scientific evidence by itself is not sufficient to end fear and combat stigma; additional efforts are required too in public health: Community actors, youth, and women’s organization, among others, must be included in national responses [78]. As an example, in the Dominican Republic, early in the HIV epidemic, it was considered a hidden disease, making affected individuals especially susceptible to stigmatization. Now, the Dominican Republic’s COVID-19 response is a hybrid of previous experiences involving massive educational resources and community engagement [80]. The UNAIDS emphasizes the importance of community-led responses, combating all forms of stigma and discrimination, including those based on race, social contacts, profession, and those directed towards marginalized groups that prevent them from accessing care [81].

Another lesson from the HIV pandemic is to take advantage of all components of healthcare systems. Globally it has been recognized that the successful global response to the HIV epidemic is due to the strengthening of all pillars of the health system [82]. In LAC, Cuba repurposed strategies that were initially created to fight the HIV pandemic have been used to face the threat of COVID-19 [83]. In 1986, amid widespread international controversy, Cuba instituted a mandatory quarantine policy for PLWH in order to curb infection rates, creating sanatoriums across the country [84]. They trained healthcare workers in contact tracing and rigorously tested anyone with risk factors. Though the quarantine was lifted in 1994, sanatoriums continued to function both as housing for PLWH and as centers for counseling and care. When the first cases of COVID-19 were reported in the country, the government decided to turn those capacities into an efficient system for contact tracing and isolation of cases. Sanatoriums were used as quarantine centers and well-trained contact tracers were sent into the community, using previous experience with HIV, to curb the spread of the epidemic, which kept the number of cases lower compared with what has been seen in other Latin American countries [83].

Involving civil society organizations is another lesson from HIV to the COVID-19 pandemic. In Venezuela, where a humanitarian crisis has all but collapsed the health system for much of the past decade, civil society organizations and international allies have played a pivotal role in ensuring continuity of care for HIV patients throughout the crisis. Many of the systems put in place by these organizations are so robust that during the COVID-19 pandemic they were easily adapted to face new challenges. For example, civil society organizations established a mechanism to monitor and document the availability of ART in government pharmacies to strengthen advocacy efforts. This monitoring system was adapted to monitor stocks of personal protective equipment during the COVID-19 pandemic, helping to keep health workers safe [85].

Conclusion

In this review, we have synthesized the information available regarding the interaction of the HIV and COVID-19 pandemics in LAC. Data published regarding the impact of HIV on the infection risk and severity of COVID-19 is scarce in the region and mainly based on case reports or small case series, some referring to coinfections of HIV, COVID-19, and opportunistic infections. In addition, the pandemic has had an important impact on PLWH, with disruption of the continuity-of-care cascade in terms of prevention, access to treatment, and follow-up. However, many Ministries of Health around LAC have promptly responded with HIVST, extension of medication supplies (including PrEP and ART), and providing telehealth services to PLWH and other strategies with variable results. However, there is still a need to document and quantify better the short-term, medium-term, and long-term effects of the HIV service disruptions in the LAC. Finally, we also report lessons learned from HIV applied in some Latin American countries to deal with the COVID-19 pandemic such as community engagement, take advantage of all components of healthcare systems, and adapt them during the crisis and the involvement of the civil society organizations and international allies. Being Latin America one of the regions hardest hit by the pandemic, a better understanding of HIV and COVID-19 in the region is very much needed to target specific measures of prevention, continuity of care, and favorable outcomes among people with HIV.