Background

The coronavirus disease 2019 (COVID-19) pandemic caused by infection with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) poses a great risk to people experiencing homelessness. Across the United States (US), the estimated 568,000 people who experience homelessness nightly [1] are likely to suffer a disproportionate disease burden and need for hospitalization [2, 3]. People experiencing homelessness are on average older and have a high prevalence of comorbidities that are risk factors for severe COVID-19 [2]. Multiple outbreaks in homeless shelters have occurred in several cities, including San Francisco, Boston, Seattle, Atlanta, and Los Angeles, with attack rates of up to 67% [4,5,6,7,8]. Homeless shelters have remained open in many cities despite the high incidence of infection in the community, concern about the risk of further outbreaks, and uncertainty over the effectiveness of different infection control strategies. There is an immediate need to identify the best infection control strategy to reduce the risk of outbreaks and assess the safety of continuing to operate congregate shelters where transmission in the community is high.

The role of shelters and associated infection control practices in the transmission of COVID-19 among people experiencing homelessness is still poorly understood. Given the current understanding that the SARS-CoV-2 virus is transmitted predominantly through respiratory droplets, with some airborne transmission [9], there is a need to consider policies to limit transmission within high-density congregate living environments. Different infection control strategies are currently recommended based on the level of transmission in the external community [10]. These include routine symptom screening, polymerase chain reaction (PCR) testing, universal mask wearing, and relocation of individuals at high risk of severe disease to non-congregate settings [11]. There is limited evidence on the effectiveness of strategies to reduce transmission in congregate settings, and thus, further research is urgently needed to guide city-level policy across the US.

The goal of this study is to identify the most effective infection control strategy to slow the spread of COVID-19 among people experiencing homelessness who reside in shelters. We address this pressing question by estimating the comparative health outcomes of key infection control strategies using a simulation model calibrated to data on homeless shelter outbreaks.

Methods

Microsimulation model

We developed an individual-level stochastic susceptible-exposed-infectious-recovered (SEIR) model [12] to simulate the transmission of SARS-CoV-2 in a congregate shelter population (Additional file 1: Figure S1) [4,5,6,7, 9, 13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75]. The model defines individuals as susceptible, exposed, infectious, or immune to SARS-CoV-2 (Additional file 1: Table S1). We constructed the model to include important aspects of the natural history of COVID-19, including sub-clinical infection, pre-symptomatic transmission, and age-specific differences in the risk of severe symptoms (see Additional file 1 for full details). In the model, susceptible individuals become infected with SARS-CoV-2 at a rate proportional to the prevalence of infectious individuals inside the shelter and their infectiousness (assuming homogeneous mixing), plus a static force of infection based on the background infection incidence in the community outside the shelter. Upon infection, individuals enter a latent infection stage in which they incubate the virus but are not infectious. They then progress to become infectious and contribute to ongoing transmission. An age-dependent fraction of infected individuals develop clinical symptoms with an associated risk of hospitalization and death (Additional file 1: Table S2), while the remainder have sub-clinical infection. Individuals who recover from infection are assumed to remain immune.

Data

The model was calibrated using aggregate data from PCR testing conducted during COVID-19 outbreaks in five shelters in three US cities—San Francisco (n = 1), Boston (n = 1), and Seattle (n = 3) [4, 6, 7]—from March 28 to April 10, 2020. We obtained de-identified individual-level data from the outbreak in the San Francisco shelter (see Additional file 1 and Additional file 1: Table S3 for details), which is fully described elsewhere [5]. As of April 10, 2020, a total of 89 individuals (84 residents, 5 staff) of 175 tested (130 residents, 45 staff) in the shelter were PCR-positive. We obtained aggregate data from the outbreaks in the Boston and Seattle shelters, where identified COVID-19 cases triggered mass testing events [4, 6, 7]. In the Boston shelter, 147 of 408 residents and 15 of 50 staff were PCR-positive during testing conducted April 2–3, 2020. The numbers of residents and staff tested and positive in the three Seattle shelters (shelters A, B, and C) at two testing events conducted March 30–April 1 and April 7–8, 2020, are given in Additional file 1: Table S4. For the San Francisco shelter, we used daily census data to inform the shelter population size, which decayed over time, and risk stratification for disease severity by age and comorbidity status (Additional file 1: Figure S2). For the other shelters, we assumed a constant population size over time.

Model calibration

We calibrated the model to the aggregate numbers of individuals PCR-positive out of those tested in each shelter (daily data for the San Francisco shelter, cross-sectional for the Seattle and Boston shelters) using approximate Bayesian computation techniques (see Additional file 1). We fitted the following parameters: (i) the basic reproduction number R0 (the average number of secondary infections generated by the average infectious individual in an entirely susceptible shelter population), (ii) the number of latently infected individuals who initially entered the shelter E0, and (iii) the number of days before the first case was identified that these individuals entered the shelter D (Table 1). The remaining parameters were sourced from the literature on natural history and epidemiology of SARS-CoV-2 (Table 1 and Additional file 1: Table S5).

Table 1 Microsimulation input parameters based on observed outbreak data from homeless shelters in Seattle, Boston, and San Francisco

Infection control strategies

We simulated six infection control strategies (Additional file 1: Table S6), selected via informal consultation with public health experts. (1) Daily symptom-based screening: daily screening of all individuals in the shelter involving a temperature and symptom survey. Individuals who screened positive were PCR tested, with 80% compliance, and isolated for 1 day pending the test result; if negative, they returned to the population. We assumed that isolated individuals were unable to transmit or become infected. We used published data on the sensitivity of symptom-based screening with time since infection [72], which suggests that close to 100% of symptomatic cases (a subset of all true cases) would eventually be detected under repeated daily screening based on the definition of being symptomatic, even with low sensitivity of symptom screening on any one occasion (here assumed to be 40% to give a 98% probability of detection after 8 days of daily symptom screening). We assumed symptom screening had a daily specificity of 90%, but assumed independence between screenings, meaning the overall specificity over the simulation was much lower and aligned with published estimates [76,77,78]. We assumed a minimum of 3 days between repeat PCR tests for the same individual based on typical clinical practice and test turnaround times. (2) Routine PCR testing: twice-weekly PCR testing of residents and staff based on prior literature analyzing reduction in transmission and cost-effectiveness under different testing frequencies [73,74,75]. We assumed 75% sensitivity and 100% specificity of PCR testing based on published literature [28,29,30,31], a mean duration of detectable viral load (starting prior to development of symptoms) of 20 days (Additional file 1: Figure S3) [17, 20,21,22,23,24], and 80% compliance with testing. We assumed test results were returned in 1 day, after which time individuals who tested PCR-positive were removed from the shelter population. (3) Universal mask wearing: wearing of masks by individuals within the shelter. We assumed that mask wearing reduced the amount of infectious SARS-CoV-2 material breathed into the air by infected individuals by 30% and that inhaled by susceptible individuals by 40% based on a review of the literature on filtration efficiencies of masks and the impact of mask wearing on infection risk (see Additional file 1), and that 60% of individuals adhered to mask wearing [37, 48]. (4) Relocation of “high-risk” individuals: moving high-risk individuals (defined as those ≥60 years and/or with co-morbidities) to single hotel rooms, modeled by replacing such individuals with lower-risk individuals. (5) Routine PCR testing of staff only: twice-weekly testing of staff only, assuming 80% compliance. (6) Combination strategy: strategies 1–4 combined. Daily symptom screening (strategy 1) was included in all strategies as it is considered a minimum requirement under CDC guidelines for control practices in homeless shelters [79].

Prediction of impact of infection control strategies

For each intervention strategy, we simulated transmission within a shelter of 250 residents and 50 staff (based on an average shelter size) over 30 days starting with one latently infected individual 1000 times (to account for stochastic uncertainty). The time period was chosen to capture the trajectory of an outbreak and the differential benefits of strategies. The primary outcome was the probability of averting an outbreak (defined as 3 or more infections originating within the shelter in any 14-day period [80, 81]) under each strategy, with secondary outcomes of the proportional reductions in the total numbers of SARS-CoV-2 infections and clinical cases, and total numbers of hospitalizations, deaths and PCR tests used. Only individuals who tested positive were removed from the shelter population. The initial population was chosen to have the same composition in terms of proportions in different risk groups (by age and co-morbidity status) as the San Francisco shelter. We estimated the probability of averting an outbreak under each intervention strategy (compared with no interventions) for each calibrated R0 value for a range of different background infection rates estimated from incidence of confirmed cases in Seattle, Boston, and San Francisco (see Additional file 1 for details). To account for potential upward bias in the estimated R0 range due to fitting to data from shelters with high attack rates, we performed the same simulations for a shelter environment with a low R0 of 1.5. The analyses were conducted in R version 4.0.0 [82], and the data and model code are available at https://github.com/LloydChapman/COVID_homeless_modelling.

Sensitivity analysis

We conducted a multi-way sensitivity analysis to assess the impact of uncertainty in key natural history and intervention parameters—relative infectiousness of subclinical infection and the early infectious stage, sensitivities and specificities of symptom screening and PCR tests, testing and masking compliances, and mask effectiveness—on the results, by simulating each intervention strategy across all combinations of the minimum and maximum values of these parameters over their uncertainty ranges (Table 1). We explored the impact of PCR testing frequency on the probability of averting an outbreak by varying the testing frequency in strategy 2 from daily to monthly.

Results

Model calibration

The model reproduced the numbers of PCR-positive individuals in the cross-sectional surveys in the Seattle and Boston shelters (Additional file 1: Figure S4) and the observed numbers of PCR-positive individuals and symptomatic cases over time for the outbreak in the San Francisco shelter (Additional file 1: Figures S4–S5). The estimated R0 values ranged from 2.9 (95% CI 1.1–6.7) for Seattle shelter B to 6.2 (95% CI 4.0–7.9) for the San Francisco shelter (Additional file 1: Table S7), with corresponding estimated cumulative infection incidences at the end of the testing period of 14% (95% CI 1–41%) and 83% (95% CI 72–92%) (Additional file 1: Table S8). The median estimated number of infections initially introduced was 3 for all shelters (95% CI 1–5), but with a relatively flat posterior distribution extending to the bounds of the uniform prior distribution, reflecting considerable uncertainty in this parameter (Additional File 1: Figure S10). The estimated date of introduction of infection ranged from 10 days (95% CI 7–14 days) before the first case was identified for Seattle shelter B to 21 days (95% CI 17–26 days) before for San Francisco.

Impact of infection control strategies

Table 2 shows the projected impact of the six infection control strategies considered, for different transmission environments. Daily symptom screening performed poorly for all levels of transmission (probability of averting an outbreak = 0.04 for San Francisco R0 = 6.2, and probability = 0.35 for R0 = 1.5). Relocating individuals at high-risk of clinical symptoms combined with symptom screening performed similarly to symptom screening alone (probability of averting an outbreak = 0.04–0.33 for R0 = 6.2–1.5). Twice-weekly PCR testing of staff provided some additional benefit over daily symptom screening at lower levels of transmission (probability of averting an outbreak = 0.04–0.41 for R0 = 6.2–1.5). Twice-weekly PCR testing of all individuals and universal masking yielded higher probabilities of averting an outbreak of 0.09–0.53 and 0.08–0.62 for R0 = 6.2–1.5, respectively. The combination strategy involving daily symptom screening, twice-weekly PCR testing of all individuals, universal masking, and removal of high-risk individuals gave the highest probability of averting an outbreak (0.19–0.74 for R0 = 6.2–1.5), but still prevented a minority of outbreaks in all but the lowest-risk setting.

Table 2 Probability of averting an outbreak over a 30-day period in a generalized homeless shelter with simulated infection control strategies

The probability of averting an outbreak under each intervention strategy decreased with increasing transmission potential (R0) inside the shelter and with increasing infection incidence in the community outside the shelter (Fig. 1). Even under the combination strategy, the probability of averting an outbreak in an average-transmission-potential shelter (R0 = 2.9) decreased from 0.77 to 0.12 as the background infection rate increased from 0 to 439 cases per 1 million person-days (the estimated background infection rate in San Francisco between June 27 and July 10, 2020).

Fig. 1
figure 1

Impact of incidence of infection in the community on the probability of averting an outbreak in a generalized homeless shelter under different intervention strategies for different R0 values. The probability of averting an outbreak (≥3 infections over any 14-day period) in a generalized homeless shelter of 250 residents and 50 staff over 30 days was estimated for different infection incidences in the community using the microsimulation model described in the text. A thousand simulations of the counterfactual no-intervention scenario and each of the intervention strategies were run, and the probability of averting an outbreak was calculated as the proportion of simulations with an outbreak in the no-intervention scenario in which there was no outbreak in the intervention scenario. SF, San Francisco

The relative reduction in infection incidence under the different infection control strategies followed the same pattern as the probability of averting an outbreak (Additional file 1: Table S10 and Fig. 2).

Fig. 2
figure 2

Predicted number of SARS-CoV-2 infections over a 30-day period in a generalized homeless shelter under different infection control strategies for different R0 values. Solid lines show the mean daily numbers of new infections, and shaded areas show the minimum and maximum daily numbers over 1000 simulations. Generalized homeless shelter defined as 250 residents and 50 staff. Background infection rate in the community outside the shelter of approximately 120 infections/1,000,000 person-days. SF, San Francisco

PCR test requirements were approximately three times higher (at an average of 6.6 tests per person per month) under twice-weekly PCR testing of all individuals than when only testing individuals identified as symptomatic in daily symptom screening (2.0 tests/person/month) and approximately two times higher than when only testing staff twice-a-week (2.8 tests/person/month) (Additional file 1: Table S11).

Sensitivity analysis

The probability of averting an outbreak was most sensitive to uncertainty in masking compliance and effectiveness and relative infectiousness of the early infectious stage, with the mean probability of averting an outbreak under combined interventions across all combinations of the minimum and maximum values of the other parameters varying from 0.40–0.71 for 30–100% masking compliance, 0.49–0.62 and 0.48–0.63 for 10–50% and 20–60% mask exhalation and inhalation effectiveness, and 0.63–0.48 for early-stage relative infectiousness of 1–3 for R0 = 2.9 (Additional file 1: Figure S9). After this, the probability of averting an outbreak was most sensitive to PCR sensitivity and testing compliance, with the mean probability of averting an outbreak under combined interventions varying from 0.50–0.61 and 0.51–0.60 over the uncertainty ranges of these parameters. Decreasing the frequency of PCR testing from daily to monthly decreased the probability of averting an outbreak for R0 = 1.5, 2.9, and 3.9 from 0.71 to 0.33, 0.28 to 0.12, and 0.21 to 0.08, respectively, but had little impact on the already low probability of averting an outbreak for R0 = 6.2 (Fig. 3).

Fig. 3
figure 3

Impact of varying the frequency of routine PCR testing of residents and staff on the probability of averting an outbreak in a generalized homeless shelter for different R0 values. The probability of averting an outbreak (≥3 infections over any 14-day period) over 30 days was estimated for different frequencies of routine PCR testing from daily (1 day between tests) to monthly (30 days between tests). Generalized homeless shelter defined as 250 residents and 50 staff. Background infection rate in the local community of approximately 120 infections/1,000,000 person-days. SF, San Francisco

Discussion

Several outbreaks of COVID-19 with high attack rates have occurred in homeless shelters across the US, and there remains uncertainty over the best infection control strategies to reduce outbreak risk in shelters. In this study, we applied a simulation analysis to identify infection control strategies to prevent future outbreaks. We found that in high-risk shelters that are unable to maximize basic infection control practices that sufficiently reduce the transmissibility of SARS-CoV-2 (e.g., social distancing, reduced living density), no additional infection control strategy is likely to prevent outbreaks. Similarly, in cities with high community incidence, no infection control practices are likely to prevent an outbreak. In contrast, in lower-risk shelters with low background community incidence, the implementation of strategies such as symptom screening, routine PCR testing, and masking would help reduce outbreak risk.

We found a wide range of transmissibility of SARS-CoV-2 based on observed outbreaks in homeless shelters, which greatly affects intervention impact. We estimated basic reproduction numbers (R0) of 2.9–6.2 from aggregate PCR test data from outbreaks in five shelters in Seattle, Boston, and San Francisco between March and April 2020. This range of R0 values is at the high end of estimates reported in the literature [52, 63, 83, 84] and likely reflects a high degree of heterogeneity in infectiousness between individuals [62,63,64,65,66] and a highly conducive environment for transmission within these shelters early in the pandemic due to lack of existing infection control practices and high living density at the time of the outbreaks. For these R0 values and representative background infection rates, we found that the infection control strategies considered are unlikely to prevent outbreaks (probability < 50%), even when combined. Nevertheless, they do reduce the incidence of infection and clinical disease and slow the growth of the outbreak (Fig. 2). Our R0 estimates are likely not entirely representative of general transmission potential in shelters now given that the outbreaks occurred early during the pandemic when control measures were limited and that non-outbreaks and smaller outbreaks may go undetected or unreported. Control measures such as rehousing of individuals to single hotel rooms appear to have been successful, and incidence has in general been lower in the homeless population than anticipated [85]. However, there have been subsequent large outbreaks in homeless shelters despite reduced shelter density and stringent control efforts [86,87,88]. This supports our finding that outbreaks in congregate shelters remain likely even with fairly intensive infection control practices.

In lower transmissibility settings, e.g., with R0 = 1.5, which may be more representative of typical shelters now due to improved social distancing and basic infection control practices, the intervention strategies we have considered are more likely to prevent outbreaks (probability up to nearly 75% under combined interventions, for a moderate background infection rate of approximately 120/1,000,000/day).

A key remaining issue given the limited availability of alternative housing for people experiencing homelessness is identifying the characteristics that distinguish low-risk shelters (those similar to the R0 = 1.5 scenario considered here) that can be operated with low outbreak risk with implementation of infection control strategies. Data are limited, but available evidence suggests that social distancing and reductions in super-spreading are likely to be key factors [62, 63, 89,90,91]. Strategies that may achieve these goals include reducing living density, spacing bedding, reducing communal activities, and adopting staffing models that limit social contacts.

The fact that intervention impact and the probability of averting an outbreak decrease significantly with increasing background infection rate in the community (Fig. 1) suggests a need for alternative housing arrangements for people experiencing homelessness in locations in which community incidence is moderate to high—100–500 infections/1,000,000/day, equivalent to 25–125 confirmed cases/1,000,000/day assuming fourfold underreporting (see Additional file 1). In lower background incidence settings, combined daily symptom-based screening, twice-weekly PCR testing, universal masking, and relocation of high-risk individuals to non-congregate settings would reduce outbreak risk and limit the incidence of infection and severe disease if outbreaks do occur.

Our findings broadly agree with those of two other modeling studies of interventions against COVID-19 in homeless shelters: one in the US [92] and the other in England [93]. The former found that a combination of daily symptom screening with PCR testing of symptom-positive individuals, universal PCR testing every 2 weeks, and alternative care sites for those with mild/moderate COVID-19 would significantly reduce infections, while remaining cost-effective, but unlike our analysis did not consider variation in the effectiveness of interventions with community incidence. The latter study supports our results on the high risk of outbreaks in congregate homeless shelters, as it found that outbreaks in homeless shelters are likely even when incidence in the general population is low and estimated that closure of congregate shelters during the first pandemic wave in England averted over 90% of infections that would have otherwise occurred in the homeless population.

Each infection control strategy is limited in some aspect [17, 18, 69, 94,95,96]. Symptom-based screening has very low sensitivity to detect infections early in the clinical course (when people are most infectious) and has poor specificity [72, 76, 77, 97]. The impact of routine PCR testing is limited by imperfect PCR sensitivity (~ 75%), especially early in the infection course [28], as well as the need for frequent testing and missing onset of infectiousness between testing periods. Other analyses support our finding that testing less than once or twice weekly leaves a high risk of outbreaks (e.g., testing once every 2 weeks gives a 30% lower probability of averting an outbreak than twice-weekly testing, Fig. 3) [73,74,75]. However, once- or twice-weekly testing may be financially and logistically infeasible. Similarly, relocation of high-risk persons to independent housing is resource-intensive. Frequent testing and universal masking also suffer issues with adherence and may not be possible for all individuals at all times in homeless shelters.

This study has a number of limitations. Due to limited data availability, we only calibrated the model to a small number of shelter outbreaks, the R0 estimates for which are likely to be higher than for the average shelter since they occurred early in the pandemic and larger outbreaks are more likely to be reported. The cross-sectional aggregate nature of the majority of the data also led to wide uncertainty intervals around the fitted parameters, without independent identifiability between them (Additional file 1: Figure S10). Our results suggest that universal masking would significantly reduce the risk of outbreaks in homeless shelters, even with 60% compliance. However, the impact of masking is highly sensitive to the assumed masking effectiveness and compliance, estimates for which still vary considerably despite accumulating evidence that masks reduce infection risk [36, 37, 39, 98, 99]. Many uncertainties in the biology of SARS-CoV-2 transmission remain, particularly regarding differential infectiousness over time and by the severity of illness, and the relationship of PCR positivity and infectiousness [17, 19, 67]. Our assumption of equal infectiousness for different individuals means that our model is unlikely to fully reproduce super-spreading events [62, 63]. We made several simplifying assumptions in modeling transmission within the shelter and from the surrounding community, namely, homogenous mixing within the shelter population, no entry of new people, a stable background infection rate over time, and full immunity upon recovery from infection given the short duration of the simulation. Our assumption that individuals who are isolated within homeless shelters while awaiting test results are unable to transmit or become infected may have led to a slight overestimation of the impact of testing, since in reality isolation is not perfect. We assumed homogeneous mixing due to a lack of contact data for the shelter outbreaks, which meant that we were not able to consider cohorting and contact tracing as interventions.

Conclusions

This study defines conditions for operating homeless shelters with a lower risk of COVID-19 outbreaks and estimates the impact of various interventions on outbreak risk. Our findings demonstrate the need for combined interventions (symptom-based screening, PCR testing, and masking) and regular testing to protect persons experiencing homelessness from COVID-19, while highlighting the limitations of these interventions in preventing outbreaks.