key: cord-1026517-mc69vfit
authors: Medina, Narda; Alastruey-Izquierdo, Ana; Bonilla, Oscar; Ortíz, Brenan; Gamboa, Osmar; Salazar, Luis Roberto; Mercado, Danicela; Pérez, Juan C.; Denning, David W.; Arathoon, Eduardo; Rodriguez-Tudela, Juan Luis
title: Impact of the COVID-19 pandemic on HIV care in Guatemala
date: 2021-06-10
journal: Int J Infect Dis
DOI: 10.1016/j.ijid.2021.06.011
sha: a75ad43f8e90418accee4a08d485fc2774513288
doc_id: 1026517
cord_uid: mc69vfit

OBJETIVES: To describe the impact of the COVID-19 pandemic on the diagnosis of HIV and opportunistic infections mortality in Guatemala. METHODS: A retrospective study was conducted to describe the impact of COVID-19 pandemic on people living with HIV in a referral HIV clinic as well as the disruption of the services of a diagnostic laboratory hub (DLH), which provides diagnosis for opportunistic infections to a network of 13 HIV health care facilities. March to August months from two different time periods were used for comparative analysis. These periods included months from March to August: : (i) the pre COVID-19 (2017–2019) and (ii) the COVID-19 period (2020). RESULTS: In the COVID-19 period 7,360 HIV tests were performed at CFLAG in comparison with 16,218 tests performed on average in the pre COVID-19 period, a 54.7% reduction (95% CI, 53.8%-55.4%). OI mortality at 90 days was 10.7% higher in 2020 than observed in 2019 (27.3% vs 16.6%, P = 0.05). Clinical samples for opportunistic infections diagnosis sent to the DLH decreased by 43.7% (95% CI, 41%-46.2%). CONCLUSION: The COVID-19 pandemic is having a substantial impact on HIV care in Guatemala. Diagnostic services for HIV were severely affected and OI mortality increased. Lessons learned must guide the introduction of strategies to reduce the impact of the pandemic.

The severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) emerged in China in late 2019 (Li et al., 2020; Schlottau et al., 2020) . Since the first reported case, the disease spread rapidly and in March 2020, the World Health Organization (WHO) declared the Coronavirus Disease (COVID-19) a pandemic (Archived: WHO Timeline -COVID-19, n.d.).

Currently, a total of 134,957,021 cases have been confirmed around the world (WHO Coronavirus Disease (COVID-19) Dashboard | WHO Coronavirus Disease (COVID-19) Dashboard, n.d.) . In Guatemala, the first case was reported on March 13, and by the end of November, 74,989 cases and 3,094 deaths had been reported (COVID19 en Guatemala, n.d.) .

Beyond the direct impact of the COVID-19 pandemic, all sectors of the health care system have been affected. In this context, access to routine services has been reduced due to reassignment of the clinical staff to activities related to COVID-19, disruption of medical supplies, and restrictions in transportation and personal mobility. According to a WHO survey in 155 countries, 53% of the health care services have been partially or completely disrupted during the COVID-19 pandemic (COVID-19 significantly impacts health services J o u r n a l P r e -p r o o f 4/19 for noncommunicable diseases, n.d.). Among people with HIV (PWH), interruptions in both health care attention and treatment could result in an increased mortality rate and further spread of HIV in the community. This increase in mortality would most likely be attributed to delay in the opportunistic infection diagnosis secondary to a lack of adequate access to care. We therefore evaluated the impact of the COVID-19 pandemic on the diagnosis of HIV and opportunistic infections mortality in Guatemala.

To understand the COVID-19 situation in Guatemala, we collected the total number of monthly COVID-19 cases reported by the Ministry of Health (MOH) from March to August 2020. The MOH and the Pan American Health Organization (PAHO) publish an online openaccess dashboard with essential information on the COVID-19 epidemic in Guatemala (COVID19 en Guatemala, n.d.) . According to the MOH, a positive result for polymerase chain reaction (PCR) or an antigen test was considered a laboratory-confirmed case of COVID-19.

The data was organized according the date of the result. Government policies implemented to contain the COVID-19 pandemic were also collected from the Central America Diary (https://legal.dca.gob.gt).

Since 2017, a program to improve the diagnosis of the most common opportunistic infections in Guatemala was implemented. The diagnostic services were provided to a health care facility network, which is composed by 13 HIV facilities located across the whole country plus a Diagnostic Laboratory Hub in Guatemala city that receives clinical samples daily via a courier service. The Clinica Familiar Luis Angel García (CFLAG) is the largest health J o u r n a l P r e -p r o o f 5/19 care facility of the network and it is located within the Hospital General San Juan de Dios in Guatemala City, which is one of the two national reference hospitals. Since 1987, this clinic has provided inpatient and outpatient services as well as HIV testing and counseling programs. For this study, the total number of outpatient and inpatients diagnosed with HIV as well as opportunistic infections cases detected in CFLAG were included. For comparision, two periods were defined. Each period encompass eight months: The pre COVID-19 period The opportunistic infection screening was done on those newly diagnosed with HIV, out of care patients, and in those on antiretroviral therapy (ART) with symptoms compatible with an OI. The OI screening included testing for: histoplasmosis, cryptococcosis, tuberculosis (TB), and non-tuberculous mycobacteria (NTM) infections, as described by Medina et al. (Medina et al., 2021 . In addition, since 2018, screening for Pneumocystis jirovecii pneumonia was also implemented. To analyze the disruption of the opportunistic infection diagnosis program, we compared the number of samples received at the DLH through the eight first months of COVID-19 period vs. the previous three years free of COVID-19.

J o u r n a l P r e -p r o o f 6/19 Services of the DLH functioned according to the government dispositions during the COVID-19 pandemic.

This study is based on data from the public national COVID-19 dashboard and the OI system from the network. Patient informed consent was not required as only overall data was collected and analyzed.

The statistical analysis was performed using the Statistical Package for the Social Sciences, version 25.0 (SPSS Inc., Chicago, IL, USA). For the descriptive analysis we used proportions, medians, and a trend X 2 test. Continuous variables were compared with the Mann-Whitney U-test. A P value <0.05 was considered statistically significant.

Between March to August 2020, a total of 75,004 new cases of COVID-19 had been registered in Guatemala, along with 3,207 deaths. A total of 244,720 COVID-19 tests were performed with a positivity rate of 31%. Figure 1 shows the number of COVID-19 cases per month and the main measures implemented by the government. On the 29 th of March, several restrictions were implemented, including the closure of public transport, establishment of curfew hours, and limitations on mobility between regions. These measures remained in place until July then they were progressively modified. This has led to limit the health care attention given to PWH during this period. Concerning the HIV program for pregnant women, which includes the labor and delivery services as well as the outpatient obstetric clinic, the results were as follows: in the COVID- the overall mortality observed in 2019 (16.6%; P = 0.053), 7.9% higher than in 2018 (19.4%; P=0.191)and 2.3% higher than in 2017 (25%; P = 0.650). Figure 3 shows the number of PWH screened for opportunistic infections, the total number of cases dectected, and the opportunistic infections mortality identified at CFLAG by year.

By January 2020, a total of 3,677 PWH comprised the cohort of patients from CFLAG; by August 2020, 44 (1.2%) cases of COVID-19 had been diagnosed, 36 (81.8%) of which were on ART. The mean age of those diagnosed with COVID-19 was 44 years and 4 patients had coinfections (3 cryptococcal disease and 1 TB). Twenty-six of these patients had a CD4 cell count available, the median cell count was 301 cells/mm 3 (IQR 61-475). The mortality at 90 days of the patients with COVID-19 was 27.2% (12 out of 44 cases).

We also determined the impact of COVID-19 pandemic in the opportunistic infections screening program performed at the diagnostic laboratory hub for the whole network of 13

HIV units. Table 1 shows the number of samples received by the DLH every month. In the COVID-19 period, the number of samples received by the DLH decreased a 38% (95% CI, 36.1%-39.8%), this increases to a 43.7% (95% CI, 41%-46.2%) when we analyze the 12 health care facilities located outside of Guatemala City, are analysed. Compared with the pre COVID-19 period, the decrease observed in April and June of the COVID-19 period was remarkably, 46% and 75% respectively. The COVID-19 pandemic has impacted health care services for PWH. The CFLAG, a referral health care facility in Guatemala City, shows that HIV testing in the COVID-19 period decreased by 54.7% (95% CI, 53.8%-55.4%). HIV testing represents an entry point to identify and bring HIV-infected patients into care. In March 2020, when the first case of was reported in the country, HIV testing numbers dropped, a trend that was maintained during the following months, as Table 1 shows. This finding is in accordance with results from other studies (Bechini et al., 2020; Lagat et al., n.d.; Mhango et al., 2020) . Lagat et al. reported a 50% decline of female index enrollment in an assisted partner notification program for HIV in Kenya (Lagat et al., n.d.) . As expected, the number of HIV tests performed on pregnant women at CFLAG also decreased. Since essential services were maintained in the labor and delivery ward, the difference was lower than the overall decrease in HIV testing (32.5% vs. 54.7%).

Concerning newly diagnosed HIV patients, we found a 10.7% decrease, a value that was lower than expected considering there was a 54.7% decrease in HIV testing. Our results showed that the proportion of MSM patients who were brought into care at CFLAG was 16.2% higher in 2020 compared with those in 2019 or 2018 (P < 0.0001). This could be attributed to a higher amount of HIV-awareness in this group along with an increased number of programs dedicated to testing this specific population. Neverthless a total decrease of newly diagnosed HIV patients was seen, this is a worrisome finding because many cases of recently acquired HIV cases have not been diagnosed, especially within the heterosexual population who were already more likely to progress to advanced HIV disease (AHD), as previous studies shown in Guatemala(Medina et al., 2021; Meléndez et al., 2019) . On the other hand, patients have always been able to select their preferred clinic, which in the context of the COVID-19 pandemic where HIV services have been disrupted in many places, more MSM patients may have been referred to CFLAG.

Regarding the reduced detection of newly diganosed HIV patients during the COVID-19 period, in 2018, the national report of the HIV care continuum showed that only 63% of PWH knew their diagnosis (Programa Nacional de Prevención y Control de ITS VIH y SIDA, 2019), much lower than the UNAIDS goal of 90%. Thus, it is critical that the national HIV program develops strategies to identify HIV-patients even in the context of the COVID-19

pandemic. An example of one possible altarnative is HIV self-testing, now recommended by the WHO as an additional method to increase HIV testing rates (Worls Health Organization opportunistic infections (evidenced here by a 38% decrease in referening samples for opportunistic infections screening at the DLH), an indirect impact of COVID-19 on HIV patients affected by opportunistic infections (a 27.2% mortality), and the organizational arrangements that take healthcare workers away from PWH care.

As expected, the number of samples for opportunistic infections received at the DLH from the health care facilities located outside of the city decreased more than the samples obtained from CFLAG, which is located in Guatemala City (43.7% vs. 31.2%). During the COVID-19 period, the overall delivery of clinical samples to the DLH decreased by 38% (95% CI, 36.1%-39.8%). Therefore, limitations in referral of opportunistic infections samples may result in underestimation of cases and deaths.

Other immediate effects of COVID-19 on survival that were not analyzed include the consequences of antiretroviral therapy (ART) interruptions and loss of virological suppression associated with increased ART resistance. In South Africa, a social media survey for PWH found that 13% of the people surveyed did not have access to their ART during lockdowns (HSRC Study on COVID-19 | Yiba, n.d.). Moreover, a mathematical model estimates that these potential effects could lead to 1.63 times more deaths considering the effects of a 6-month interruption of supply of ART . Although the Guatemalan government started to de-escalate restrictions on mobility by the end of July 2020, public transportation remained limited and more costly, making it difficult for many patients to travel to their respective health care facilities to receive their appropriate medications, including ART. Due to this situation, alternatives to minimize the COVID-19

impact have been developed. Several studies proposed the implementation of telemedicine platforms (Mgbako et al., 2020) while the UNAIDS and WHO have also called on governments to provide multi-month dispensing of ART for PWH who are currently stable (Survey shows that many people lack multimonth HIV treatment in Latin America | UNAIDS, n.d., WHO: access to HIV medicines severely impacted by COVID-19 as AIDS response stalls, n.d.), a concept that has already been implemented in CFLAG where ART is dispensed for 3 month periods. In South Africa, one project packaged and delivered medications to community-based locations (Mendelsohn and Ritchwood, 2020) . In Guatemala, a similar strategy was implemented to deliver ART treatment directly to the patients. This program has been functioning for the network since June 2020.

Concerning the direct impact of COVID-19 on PWH, a lower risk of infection was initially hypothesized due to the possible suppression of coronavirus replication by the ART; however, a randomized clinical trial with patients who had severe COVID-19 showed no benefit from the ritonavir-boosted lopinavir over standard care (Cao et al., 2020) . Other analysis also showed no differences in previous use of nucleoside reverse transcriptase inhibitors or non-nucleoside reverse transcriptase inhibitors (Vizcarra et al., 2020) . Despite these findings, there is no additional evidence to support a higher risk of COVID-19 infection among PWH (Vizcarra et al., 2020; Worls Health Organization (WHO) , 2020). Here, we found 44 cases of COVID-19 in one clinic in Guatemala City. Considering the entire cohort of PWH in this facility, the frecuency of COVID-19 infection was 1.2% (95% CI, 0.9%-1.6%). This rate was slightly lower than those reported by Vizcarra et al. in Spain with 1.8% (1.3%-2.3%) (Vizcarra et al., 2020) . Regarding the mortality of these cases, it was much higher than the mortality reported in the Spanish cohort of 4%. Other missed diagnoses, such as Our study has several limitations. Available data represent the situation from one clinic in Guatemala City, while effects on other HIV clinics in more remote parts of the country could be more profound. Unfortunately, it has not been possible to track the effects on these clinics. Furthermore, other aspects that might increase the magnitude of the effect of the COVID-19 pandemic, such as the interruption of ARTwere not determined. Although we included all patients diagnosed with COVID-19 in CFLAG, it is possible that it was underestimated because of the low availability of HIV-testing in patients with COVID-19 in other hospital units. The presence of comorbidities and outcomes were also not estimated.

Despite its limitations, this is the first study that describes the impact of the COVID-19 among PWH in the region. Our study found that the COVID-19 pandemic is having a substantial impact on HIV care in Guatemala, HIV testing programs were severely affected, and OI mortality increased.

Maintaining the most essential health-care services, and implementing new strategies could substantially reduce the overall impact of the pandemic. 

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