Background

The outbreak of the Coronavirus Disease 2019 (COVID-19) pandemic directly caused high morbidity and mortality, as well as threatening general public health services and care delivery worldwide [1]. The severity of the COVID-19 pandemic has resulted in the health systems being overwhelmed and imposed lockdown measures to limit the spread of the virus in the community or region, leading to reduced access to health care [2, 3]. Evidence has shown that these measures have led to restrictions by healthcare facilities on the management of emergency medical conditions and chronic disease care and treatment services [4, 5].

The negative consequences of COVID-19 for some populations are more severe than others, mainly in populations of low-income countries (LIC), including job loss, food insecurity, an inability to manage existing conditions, and an inability to maintain preventive measures such as social distancing and use of personal protective equipment (PPE). Those living in poverty have less control over their living conditions and immediate environment, so the barriers they face in trying to protect themselves and their families are greater than those not living in poverty [6, 7]. Among the most underprivileged and disadvantaged in the era of pandemic are PLWH, people at risk of contracting HIV such as sex workers, people who inject drugs and men who have sex with men and people with other autoimmune diseases [8].

HIV prevention and care is critical to mitigating the public health threat of HIV and comprises HIV care continuum (HCC) measures, which consists of 5 steps, which are (i) diagnosis, (ii) linkage to care, (iii) retention in care, (iv) adherence to antiretroviral therapy, and (v) viral suppression [9,10,11].

The pandemic brought about significant changes in the provision of health services and increased fears about the increase in deaths and illnesses, health inequalities and the consequences of these changes among various subgroups of people living with HIV or at risk of contracting HIV. Containment measures, disruptions to supply chains and loss of income have the potential to exacerbate the impacts of the pandemic on HIV patients [35]. Tolossa et al. found that 21.3% of participants had poor adherence to ART, with 3.37 times greater odds of poor adherence among people residing in rural areas and 3.41 times greater in patients aged less than 35 years. Substance use was strongly associated with poor AA, with 5.42 times greater odds of poor adherence among users [38]. The cohort of Wagner et al. showed an increased risk of running out of personal ART supply, with 11.2% reporting that the pandemic reduced their ability to adhere to medication and 8.3% with worsening adherence during the lockdown. It is noteworthy that there was an increase in the percentage, which corresponded to 12.1% of people who stated that they missed a dose of ART due to lack of food. The authors believe that a facilitator for maintaining treatment was the existence of personal stocks of previous prescriptions, which ensured a sufficient supply of antiretroviral drugs [39]. West et al. found that at the beginning of the pandemic, access to clinics was hampered due to transport limitations, which raised concerns about shortages of ART and increased anxiety [25]. Two studies published in 2023 highlighted interruptions in ART adherence attributed to the depletion of ART inventory [22] and unavailability of medications [32].

The main barriers cited as obstacles included the fear of contracting COVID-19, lockdown and quarantine measures, restrictions on public transportation, and high transportation costs. Additional barriers identified included increased mental health challenges, such as symptoms of depression, and the fear of being judged based on HIV status. Financial instability, food insecurity, and the negative impact on pill-taking practices also posed challenges, as they disrupted the structure and daily routines necessary for consistent adherence. Regarding health services, one study specifically highlighted that inadequate infrastructure during the pandemic, staff shortages, and limitations on home visits further contributed to low ART adherence. On the other hand, certain factors have been identified as facilitators for ART during the pandemic, including modifications to the ART care model, home delivery of ART, multi-month dispensation of ART. Also, mental health support interventions aimed at improving mental well-being and addressing depressive symptoms.

HIV treatment engagement (HTE)

Findings from eight researches showed that both quantitative and qualitative data collectively emphasize the adverse effects of COVID-19 on treatment engagement within the HIV care continuum in low-income countries, including missed refill visits, perceived impact on care and treatment, interruptions in treatment schedules, and compromised access to specialized services. [14, 25, 27, 28, 30, 35, 36, 40]. Only one study among them also reported a positive effect [25].

Quantitative data from a cross-sectional study at Ethiopia, by Chilot et al., with 212 participants revealed that 27.4% of individuals missed their refill visits, indicating disruptions in accessing necessary medications [28]. Additionally, Wang et al., in a cross-sectional study in the Dominican Republic, 187 female sex workers, reported that 34% of individuals stated that COVID-19 had an impact on their HIV care and treatment [35]. Qualitative findings by Muwanguzi et al., in prospective interviews with 44 men, at Uganda, highlighted few participants who experienced interruptions in their treatment schedules [30].

A mixed-methods study by Linnemayr et al. conducted in Uganda, with 100 participants, had quantitative findings from descriptive statistics, which demonstrated that 76% of participants reported negative effects on their ability to travel to HIV clinics, while 54% perceived an increased risk of acquiring COVID-19 by attending the clinics [14]. Qualitative results were obtained through transcription and analysis of interviews with participants. This portion of this study identified themes including the impact of COVID-19 lockdowns on clinic attendance, concerns about exposure at clinics, effects on antiretroviral therapy adherence, perceptions of susceptibility to COVID-19, and strategies to reduce risk and increase resilience. These insights emphasize the challenges faced in accessing and engaging in HIV care during the pandemic, highlighting the need for targeted interventions to maintain continuity of care in low-income settings.

As for the barriers mentioned in studies that evaluated the impact of the COVID-19 pandemic on HTE, barriers commonly mentioned included individuals being over 55 years old, fear of contracting COVID-19, limited access to personal protective equipment like masks and sanitizers, difficulty in accessing healthcare services, and insufficient funding for services tailored to adolescents. Other significant obstacles involved transportation disruptions, high costs associated with traveling to healthcare facilities, lockdown measures, and stay-at-home directives. Additionally, financial concerns stemming from COVID-19, mental health challenges, emotional abuse from partners, partner stigma or fear, and challenges related to family planning were also reported as barriers. It is worth noting that no facilitators were identified in the studies addressing this phase of the HCC.

Viral suppression (VS)

The COVID-19 pandemic positively affected viral suppression along the HIV care continuum in a 2022 study by Kalua et al. from Malawi. The cohort study conducted among 556,281 people found that viral suppression rate increased slightly during COVID-19 pandemic, rising from 93% pre-COVID-19 to 94% during COVID-19 [41]. Similar finding of 1% improvement in VS was reported in qualitative study conducted among 9952 PLHIV in Uganda [27]. A study reported no significant changes in VS during pandemic [31].

Facilitators for sustaining VS during restrictions include the implementation of nationwide guidelines, support from initiatives like the Presidential Emergency Plan for AIDS Relief (PEPFAR), utilization of multiple service delivery models for medication distribution, as well as factors such as older age, longer time on ART, being women.

Discussion

Understanding HIV interaction as a life-long lasting infectious disease with other infectious diseases, especially those causing pandemics such as COVID-19, can provide a roadmap for care planning and management during the next pandemics. This study constituted a comprehensive examination of the interaction of HIV and COVID-19 pandemic in low-income countries in a period of approximately four years. Research findings have elucidated that although the pandemic had a discernible impact on healthcare services across a spectrum of diseases, individuals with chronic conditions, notably those who are HIV-positive, exhibited a heightened vulnerability [42,43,44].

We identified negative impact of COVID-19 on preventive methods. Limited access to condom due to concentration of HIV services on COVID-19 led to increased engagement in condom less sex in MSM/TGW. This finding indicates the importance of availability of HIV-related healthcare services during pandemics to access preventing methods in case of high-risk sexual behaviors. Efforts to provide condoms and prevention methods should prioritize diverse distribution channels, alongside integrating condom provision into COVID-19 service delivery models.

The diverse impacts of the COVID-19 pandemic on HIV testing services were observed. While some observations noted a decrease in testing rates, others highlighted nuanced shifts in testing practices. Factors such as fear of COVID-19 contraction and associated lockdown measures, including curfews and travel restrictions, likely contributed to the decline in testing. However, the emergence of self-testing methods [22] presented a potential avenue for maintaining testing accessibility amidst pandemic-related disruptions to traditional services. These findings underscore the need for tailored interventions to address barriers to HIV testing and ensure continuity of care within the context of ongoing public health crises. This finding aligns with a study conducted in a high-income country, indicating that the impacts of COVID-19 extend beyond economic status [45].

The pandemic period had deleterious repercussions on ART adherence and the commencement of pharmaceutical treatment in low-income countries. Potential impediments to adherence included impediments such as blockades and lockdown measures enforced due to quarantine restrictions and heightened apprehensions regarding COVID-19 transmission. Moreover, contributory factors encompassed a paucity of social support, the pervasive stigmatization of HIV, depressive states, substance misuse, obstacles in procuring medication, transportation-related challenges, and the exorbitant costs associated with public transportation. Additionally, concerns arose pertaining to fundamental resources such as sustenance, financial means, and employment. Several studies reported compromised functionality of HIV care facilities and anxieties regarding the availability of pharmaceutical drugs. In the context of resources aimed at enhancing antiretroviral adherence, the following strategies were identified: the provision of extended medication supplies [36], the home delivery of antiretroviral drugs [29], the establishment of individual antiretroviral stockpiles [33], and the option to adhere to medication regimens while remaining at home. These measures facilitated the establishment of a structured routine for adherence to medication protocols.

Regarding engagement with treatment, there were evident negative repercussions observed in the form of missed follow-up appointments and medication refill replacements, which had a detrimental impact on HIV care overall. Concurrently, there were shortcomings in the care provision by healthcare teams in HIV care services. The pandemic also hampered various sectors that, in turn, hindered the engagement of PLWH in their care. These challenges encompassed difficulties related to travel to healthcare clinics and the impracticability of available transportation means. Barriers to clinical care included concerns about attending face-to-face appointments and the heightened risk of COVID-19 exposure. Disruptions in transportation, partial lockdowns im**ing on mobility, and income reductions all played pivotal roles in individuals' inability to access healthcare appointments, corroborating the findings of earlier research [46, 47] and aligning with analogous circumstances observed globally [30, 48,49,50]. These studies affirm that COVID-19 containment measures significantly curtailed patients' capacity to avail themselves of healthcare facilities. The findings pertaining to healthcare engagement reveal adverse effects on healthcare continuum compliance and underscore inadequacies in the methods employed for healthcare delivery and follow-up. These shortcomings are imperative to address in order to surmount the identified barriers experienced during the pandemic period in low-income countries.

Viral suppression was poorly reported as a phase of HCC impacted during the pandemic. There may have been a beneficial impact on virus suppression rates during the epidemic, according to reports. Despite the challenges posed by the pandemic, a combination of factors including the implementation of national guidelines, support from international programs like PEPFAR, and the utilization of diverse service delivery methods for medication distribution have likely contributed to the maintenance of viral suppression. This study highlights the significant positive impact of models such as PEPFAR on achieving viral suppression. PEPFAR's holistic approach, which encompasses ensuring access to antiretroviral therapy, adapting service delivery to current needs, strengthening health systems, fostering community engagement, and addressing health disparities, has played a pivotal role in advancing viral suppression efforts. By providing a detailed account of PEPFAR's contributions to promoting viral suppression, valuable insights can be gleaned for replication in various settings, thereby optimizing health services and improving outcomes for individuals living with HIV/AIDS. It's essential to acknowledge that the pandemic has affected different areas and populations unevenly, and variations in healthcare resources and access may have influenced outcomes. To fully grasp the dynamics of viral suppression throughout the pandemic and to identify effective strategies for enhancing the provision of HIV care during emergencies, additional research is necessary.

Conclusion

Overall, researchers have discerned numerous adverse effects of COVID-19 restrictions on the HIV care continuum during the pandemic. In comparison to the period before the pandemic, a decline in various aspects of HIV care practices has been noted, encompassing the use of preventive measures, counseling and testing, the receipt of HIV healthcare services, attendance at HIV medical appointments, antiretroviral adherence, engagement with treatment, and suboptimal viral suppression. Nevertheless, certain observations have pointed to indirect positive impacts on specific facets of HIV care as a result of the implementation of condom distribution, self-testing services, extended medication supplies, and the home delivery of ART medications during the pandemic. Further research is needed to understand and address the disparities in healthcare access during emergencies.

Limitations

The limitations that may compose the review are due to the small number of articles identified, despite having started from a broad search in various databases, the limited number reflects the impact on low-income countries, but as only a limited cut in the studies identified. If there were other studies in more low-income countries it would be beneficial to implement the big picture.