key: cord-0872519-9ayg9bhl
authors: Vallejo-Janeta, Alexander Paolo; Morales-Jadan, Diana; Freire-Paspuel, Byron; Lozada, Tannya; Cherrez-Bohorquez, Cesar; Garcia-Bereguiain, Miguel Angel
title: COVID-19 outbreaks at shelters for women victims of gender-based violence from Ecuador
date: 2021-06-10
journal: Int J Infect Dis
DOI: 10.1016/j.ijid.2021.06.012
sha: 5bcade2e205279eb78ccf9caa36c135e3e085bee
doc_id: 872519
cord_uid: 9ayg9bhl

BACKGROUND: Limited testing capacity was one of the constraints to contain the impact of COVID-19 pandemic in Ecuador, specially in risk populations such as people living in humanitarian shelters. OBJECTIVE: "United Nations High Commissioner for Refugees" office in Ecuador in collaboration with "Universidad de Las Américas", performed a surveillance screening at shelters for women victims of gender violence granting access to RT-qPCR tests for SARS-CoV-2 diagnosis since July 2020, few weeks after the general population lockdown was lifted. RESULTS: From 411 people tested, 52 tests were SARS-CoV-2 positive, yielding an overall high attack rate of 12.65%. Moreover, COVID-19 outbreaks were found in 9 out of 11 shelters included on the study. While attacks rates vary among shelters, no association was found with occupancy. CONCLUSION: This study is key to clarify the epidemiological situation in this highly vulnerable population in Latin America, and remark the importance of massive testing beyond symptomatic population to prevent the spread of COVID-19.

The outbreak of coronavirus disease 2019 (COVID-19) raised alerts in the global scientific and health communities since the first 27 cases were reported in December 2019 from Wuhan, China. SARS-CoV-2 spread readily and quickly around the world, and the first cases in Latin America were reported just two months after the original report (1). Until March 2021, more than 51 million COVID-19 cases and more than 1 million deaths were reported in the Americas region; and more than 290,000 cases were reported in Ecuador since the arrival of first case in March 2020 (1), but with a limited SARS-CoV-2 testing capacity and a positivity rate over 30% those numbers are far from the true ones.

During the first months of the pandemic, a wide variety of recommendations were endorsed by the World Health Organization, (including social distancing, massive testing and isolation of confirmed cases), to slow down the spread of the disease. However, those measures are difficult to meet in some specific settings. Such settings include refugee shelters, housing for victims of gender-based violence, prisons or provisional detention centers, among others.

Confinement and prevention of spread in those settings is nearly impossible due to the lack of adequate infrastructure and the high occupation of some shelters (2, 3) . Moreover, the confinement represents a harm for the economic needs of the people living in those spaces.

Testing capacity is also lower in those settings when compared with middle-or high-income environments (4), and even worse with weak health systems (e.g. developing countries) (5).

Many humanitarian shelters are generally occupied at their full capacity at times of economic crisis like current ones, therefore represent hotspots for SARS-CoV-2 infection and contagion.

J o u r n a l P r e -p r o o f During the highest peak of the COVID-19 pandemic in Ecuador, the need of massive testing throughout the country was urgent to complement the effort of the public health system and to reach sectors of the population for whom PCR tests remain inaccessible (6) (7) (8) . In this context, "Universidad de Las Américas" (UDLA) and the United Nations High Commissioner for Refugees (UNHCR) office in Ecuador coordinated efforts for granting access to SARS-CoV-2 PCR tests for the occupants of ten shelters for women victims of gender-based violence located across the country. By September 2020 when this study was finished, according to the official information from the Ecuadorian Ministry of Health (https://www.salud.gob.ec/wpcontent/uploads/2020/09/Boletin-196_Nacional_MSP.pdf), a total number of 116,451 SARS-CoV-2 positives cases were reported in the country. However, with a positivity rate of 40,03%, the need to increase SARS-CoV-2 testing was mandatory.

This study aims to clear the epidemiological situation of those women shelters in Ecuador, to remark the importance of testing in such humanitarian settings and to assess whether the occupancy level of each shelter is related to the positivity rate. Thus, a description of the study population is displayed, as well as a comparison between the attack rates at the different shelters and the occupation level.

A study to evaluate the burden of SARS-CoV-2 infection among all the occupants (women victims of gender based violence and their children) and staff working (total number of 411 individuals) in 11 shelters was performed in 9 different Ecuadorian cities from July to J o u r n a l P r e -p r o o f September 2020. UNHCR office in Ecuador provided logistics for sampling in the different cities and the samples transportation to the UDLA Laboratory located in Quito, Ecuador. Also, UNHCR coordinated with "Red Nacional de Casas de Acogida" to select the shelters that will be included in the study.

The shelters considered were: "Casa de Acogida Manos Unidas Tejiendo Progreso" (Tulcan), "Casa Mama Zoila Espinoza" (Ibarra), "Casa Tránsito Amaguaña" (Cotacachi), "Casa Amiga" (Lago Agrio), "Casa Paula" (Francisco de Orellana), "Casa de la Mujer" and "Casa Matilde" (Quito), "Casa de Acogida Cotopaxi" (Salcedo), "Casa María Amor" (Cuenca), and "Hogar de Nazareth" (Guayaquil). Also, a group of 100 women refugees and their children, migrating from Colombia and Venezuela were tested at a temporary shelter in Lago Agrio.

Nasopharyngeal swabs were collected on 0.5mL TE pH 8 buffer for SARS-CoV-2 diagnosis by RT-qPCR following an adapted version of the CDC protocol by using "AccuPrep Viral RNA extraction kit" (Bioneer, South Korea) as an alternate RNA extraction method and CFX96 BioRad instrument (9) (10) (11) (12) (13) (14) (15) (16) . Briefly, the CDC designed RT-qPCR FDA EUA 2019-nCoV CDC kit (IDT, USA) is based on N1 and N2 probes to detect SARS-CoV-2 and and RNase P as an RNA extraction quality control (15, 16) . Also, negative controls (TE pH 8 buffer) were included as control for carryover contamination, one for each set of RNA extractions, to guarantee that only true positives were reported. For viral loads calculation, the 2019-nCoV N positive control (IDT, USA) was used, J o u r n a l P r e -p r o o f provided at 200.000 genome equivalents/µL, and a factor of 200 was applied to convert the viral loads to genome equivalents/mL and then converted to logarithmic scale.

For the statistical analysis of data, positivity rates were calculated for each shelter and occupancy rates were provided by UNHCR. To assess differences in the positivity rates among shelters, Chi-squared for comparison of proportions was applied, and a Pearson's correlation test was performed to evaluate correlation between positivity rates and occupancy levels. All statistical analysis was carried out using R software.

A total of 411 people from refugee shelters were tested for SARS-CoV-2 using nasopharyngeal swabs. The shelters were distributed along the different geographical regions of Ecuador in 9 cities: Cotacachi, Cuenca, Ibarra, Latacunga, Quito, and Tulcan in the Andean Region; Guayaquil in the Coastal Region; and Francisco de Orellana and Lago Agrio in the Amazon region ( Figure   1A ). Most of the samples were taken from females (283/411, 68.86%) between 30 and 40 years (mean= 31.55 ± 0.73 years) inhabiting those shelters (Fig. 1B-1C) . The overall attack rate of SARS-CoV-2 in all the shelters was 52/411 (12.65%) (Fig. 1D ). SARS-CoV-2 outbreaks were found in 9 out of the 11 shelters visited.

The subjects who tested positive for SARS-CoV-2 are distributed as shown in Figure 2 , with less positivity ratio in females (33/283, 11.66%) rather than in males (19/128, 14.84%).

Furthermore, more cases are distributed among the younger population (below 40 years old) with an average age of 36.02 ± 2.11 years.

Data for viral loads (VL) were available only for 32 out of the 52 positive individuals in our study, thus only 32 individuals were considered for differences in VL between age groups and sex.

There were no significant differences in the average viral load among different sex or age groups (p-value > 0.05). However, higher viral loads were distributed within young adults years old) and in females ( Figure 3 ). The latter could be attributable to the fact that most of the occupants of different shelters were women and their children.

The location of each shelter and its SARS-CoV-2 attack rate is detailed as followed (Table 1) was occupied at 30% of its capacity.

-Quito city shelters (Pichincha province; Andean Region). Two shelters from the Ecuadorian capital city were considered in the study: "Casa de la Mujer" and "Casa Matilde". "Casa de la Mujer" had an occupancy percentage of 55%, and 27 samples from 26 females and 1 male were considered: none SARS-CoV-2 positive individuals were found. In contrast, "Casa Matilde" was occupied at the 73% of its capacity, and 7 individuals out of 28 living in the shelter (22 females and 6 males) had positive tests, giving a SARS-CoV-2 attack rate of 25.0%.

-Latacunga city shelter (Cotopaxi province, Andean Region). From "Casa de Acogida Cotopaxi" in Latacunga, 15 women and 3 men were tested for SARS-CoV-2 with 3 positive individuals, yielding an attack rate of 16.7%. This shelter was at 110% of its capacity.

-Ibarra city shelter (Imbabura province, Andean Region). 27 individuals were tested with 4 positive one, giving a SARS-CoV-2 attach rate of 14.8%. No shelter occupancy information was available.

-Cotacachi city shelter (Imbabura province, Andean Region). 13 individuals were tested with 4 positive ones, giving a SARS-CoV-2 attach rate of 30.8%. No shelter occupancy information was available.

J o u r n a l P r e -p r o o f -Cuenca city shelter (Azuay province; Andean Region). "Casa María Amor" was overcrowded at 118% of its full capacity. 49 women and 23 men were tested in this shelter, and 3 individuals were positive, giving an attack rate of 4.17% for this center.

-Guayaquil city shelter (Guayas province, Coastal Region). From the 38 individuals sampled in "Casa Hogar de Nazareth" in Guayaquil, 26 were females and 12 were males, with only 3 individuals being positive for SARS-CoV-2. The attack rate for this shelter was 7.89% and it was occupied at 37%.

The occupation rates for the different shelters with that information available is detailed in Table 1 . Although there are significant differences (p-value < 0.05) in the SARS-CoV-2 attack rates for different shelters, no significant linear correlation was found with the number of individuals at the shelter or the occupation rate (R = 0.36, p-value = 0.39, CI -95%: [-0.466, 0.848]).

Since the early stage of the COVID-19 pandemic in Ecuador, the strategy for prevention or mitigation of the impact of COVID-19 displayed by the Ministry of Health was limited to test symptomatic patients attending hospital facilities. Moreover, despite the huge efforts from the National Reference Laboratories for SARS-CoV-2 surveillance from "Instituto Nacional de Salud Pública e Investigación" to keep up the diagnosis, a limited daily testing capacity below 200 PCR test per million of habitants was installed across the country (17, 18) . However, the few reports about the epidemiological situation of SARS-CoV-2 among vulnerable populations suggest that J o u r n a l P r e -p r o o f community transmission has been happening since the population lockdown was lifted by June 2020 in Ecuador (6-8, 19,20) . Under this scenario, in collaboration with UNHCR, we implemented a surveillance program at shelters from women victims of gender based violence and reported COVID-19 outbreaks at 9 out of 11 shelters visited. At the best of our knowledge, this is the first publication to date addressing SARS-CoV-2 surveillance at shelters for women victims of gender based violence.

After the arrival of SARS-CoV-2 infection to Ecuador, a study revealed that women were less prone to acquire the infection compared with men (17) . This is in accordance with the findings in the overall SARS-CoV-2 attack rate for males and females in our study. The overall high SARS-CoV-2 attack rate of 12.65% is also on agreement with other reports showing SARS-CoV-2 community transmission among community dwelling individuals in Ecuador (6) (7) (8) 19, 20) .

A wide variety of studies sustain the idea that crowded household settings constitute an important site for COVID-19 outbreaks (19, (21) (22) (23) (24) (25) (26) . Our study shows that 9 of 11 of the shelters had active COVID-19 outbreaks confirming that this kind of facilities are of high risk for SARS-CoV-2 transmission. However, we did not find a clear relationship between the occupancy level of each shelter and the attack rates. Those rates varied from 0 to 30.8%. The characteristics of the shelters could explain such variations in attack rates, as the majority of shelters participating in the screening were "long-stay shelters" and the rotation of housed people was low, the exposure of each resident or working-staff being lower in comparison with "short-stay shelters". In fact, one study performed in Rhode Island (USA) found that homeless shelters in densely populated areas, with more transient resident populations had more SARS-CV-2 incidence than shelters with stable residents. The same study recommended resident stability J o u r n a l P r e -p r o o f to reduce COVID-19 cases (25) . Nevertheless, another study carried out at shelters in France also suggest the risk of collective housing for SARS-CoV-2 transmission and found a SARS-CoV-2 attack rate of 7% (26) . Interestingly, we described how the occupation of some shelters included in our study reached or even surpassed the shelter capacity according to data provided by UNHCR; considering that we found COVID-19 outbreaks at most of the shelters, recurrent screening for SARS-CoV-2 infection should be implemented.

Regarding the gender approach of this study, most of women included in our study were victims of gender-based violence, which increased during the strict lockdown implemented in the country. In addition to this, gender inequalities deepens during the COVID-19, which is reflected not only on the increase of gender-based violence, but also on worst posttraumatic stress effects after lockdown, or deeper aftermath from SARS-CoV-2 infection (27, 28) . Actually, studies like ours had been recommended to prevent a deeper impact of COVID-19 pandemic and guarantee health rights for women victims of gender based violence (28) .

The main limitation of our study is the fact that sampling took place only at one time point during the highest peak of the pandemic in Ecuador. Additional screenings months after the first one would be useful to assess the dynamics of the infection in such humanitarian settings and implement control strategies to prevent the spread, but lack of funds did not allow to continue this project. Further prevention strategies in shelters for women and children could include opportune case report, massive testing for control of existent cases and as new residents are accepted, proper isolation of affected residents wherever the infrastructure allows it, and testing for routine control of staff who is highly exposed (29) .

In conclusion, this study constitutes an important report to show the epidemiological situation of COVID-19 in humanitarian shelters in Latin America. Moreover, our findings endorse the importance of massive testing in the prevention of COVID-19 outbreaks, and the importance to close the breach in SARS-CoV-2 testing, making them accessible to disadvantaged sectors of society.

Ethical Approval and Consent to participate. Written consent was obtained for all the individuals included on the surveillance. The study was approved by IRB from Universidad de Las Américas.

Availability of supporting data. Not applicable Competing interests. The authors declare no conflict of interest.

Funding. This study was supported by Fundación CRISFE (Fondo Sumar Juntos) and Universidad de Las Américas.

☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. 

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Interim guidance: public health and social measures for COVID-19 preparedness and response in low capacity and humanitarian settings -Version 1. Inter -Agency Standing Committee

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AccuPower SARS-CoV-2 real time RT-PCR kit (Bioneer, South Korea)

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US CDC Real-Time Reverse Transcription PCR Panel for Detection of Severe Acute Respiratory Syndrome Coronavirus 2

Epidemiological, socio-demographic and clinical features of the early phase of the COVID-19 epidemic in Ecuador

Localising an asset-based COVID-19 response in Ecuador

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Miguel Angel Garcia-Bereguiain, on behalf of the UDLA-COVID-19 Team. High prevalence of SARS-CoV-2 infection among food delivery riders. A case study from Quito

What settings have been linked to SARS-CoV-2 transmission clusters? Wellcome Open Res

Clinical, molecular, and epidemiological characterization of the SARS-CoV-2 virus and the Coronavirus Disease 2019 (COVID-19), a comprehensive literature review

The epidemiology and pathogenesis of coronavirus disease (COVID-19) outbreak

Household Transmission of SARS-CoV-2 A Systematic Review and Meta-analysis + Supplemental content

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Authors' contributions. All authors contributed to data collection and analysis. MAGB and