Soldevila et al. BMC Geriatrics (2022) 22:123 https://doi.org/10.1186/s12877-022-02779-0 RESEARCH Open Access The interplay between infection risk factors of SARS‑CoV‑2 and mortality: a cross‑sectional study from a cohort of long‑term care nursing home residents Laura Soldevila1,2,3,4, Núria Prat5, Miquel À. Mas6,7, Mireia Massot5, Ramón Miralles6,7, Josep M. Bonet‑Simó5, Mar Isnard5, Marta Expósito‑Izquierdo5, Irene Garcia‑Sanchez5, Sara Rodoreda‑Noguerola5, Nemesio Moreno5, Esther Badia5, Genís López5, Javier Sevilla5, Oriol Estrada5 and Xavier Vallès1,4,8* Abstract Background: Covid-19 pandemic has particularly affected older people living in Long-term Care settings in terms of infection and mortality. Methods: We carried out a cross-sectional analysis within a cohort of Long-term care nursing home residents between March first and June thirty, 2020, who were ≥ 65 years old and on whom at least one PCR test was per‑ formed. Socio-demographic, comorbidities, and clinical data were recorded. Facility size and community incidence of SARS-CoV-2 were also considered. The outcomes of interest were infection (PCR positive) and death. Results: A total of 8021 residents were included from 168 facilities. Mean age was 86.4 years (SD = 7.4). Women represented 74.1%. SARS-CoV-2 infection was detected in 27.7% of participants, and the overall case fatality rate was 11.3% (24.9% among those with a positive PCR test). Epidemiological factors related to risk of infection were larger facility size (pooled aOR 1.73; P < .001), higher community incidence (pooled aOR 1.67, P = .04), leading to a higher risk than the clinical factor of low level of functional dependence (aOR 1.22, P = .03). Epidemiological risk factors asso‑ ciated with mortality were male gender (aOR 1.75; P < .001), age (pooled aOR 1.16; P < .001), and higher community incidence (pooled aOR 1.19, P = < 0.001) whereas clinical factors were low level of functional dependence (aOR 2.42, P < .001), Complex Chronic Condition (aOR 1.29, P < .001) and dementia (aOR 1.33, P <0.001). There was evidence of clustering for facility and health area when considering the risk of infection and mortality (P < .001). Conclusions: Our results suggest a complex interplay between structural and individual factors regarding Covid-19 infection and its impact on mortality in nursing-home residents. Keywords: Long-term care nursing homes, SARS-CoV-2, Epidemiology, Mortality, Covid-19 Introduction It is estimated that in spite of representing less than five per cent of the elderly population (> 65 years old), 47% of all Covid-19 deaths occurred among residents from Long- *Correspondence: xvallesc.mn.ics@gencat.cat 8 Term Care Facilities (LTCF) nursing homes during the Institut per la Recerca en Ciències de la Salut Germans Trias i Pujol, Badalona, Spain first wave of the SARS-CoV-2 pandemic in high-income Full list of author information is available at the end of the article countries [1]. This appalling data could be explained by © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. The Creative Commons Public Domain Dedication waiver (http://​creat​iveco​ mmons.​org/​publi​cdoma​in/​zero/1.​0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Soldevila et al. BMC Geriatrics (2022) 22:123 Page 2 of 9 the fact that LTCF show the ideal epidemiological con- 30, 2020, who were ≥ 65 years old and on whom at last ditions for transmission of an airborne infectious agent one PCR test was performed during the study period. like SARS-CoV-2 since they are densely populated spaces Socio-demographic data (age and gender), and underly- with large numbers of staff who have extensive contact ing chronic conditions as such as comorbidities, level of with highly vulnerable residents. The result has rightly functional impairment and advanced conditions were been regarded as a perfect storm [2]. However, more recorded by their primary care teams according to local detailed examinations of Covid-19 in LTCF have shown clinical guidelines [18], laboratory test results (specific that particular structural factors mediated the impact of Polymerase Chain Reaction henceforth PCR, to detect the disease, including the size of the facility, the quality of SARS-CoV-2) and clinical outcome (recovery/death), as care, and understaffing [3–8]. The lack of preparedness as well as the size of the LTCF (number of residents) and well as short and long-term policy failures also contrib- cumulative incidence of Covid-19 in the Primary Health- uted [9, 10]. Indeed, besides the direct impact of Covid- care Catchment Area where the facility was located (this 19, there have been other secondary consequences due to is the smallest administrative area of the Spanish public the lockdowns and other measures intended to contain healthcare system, typically covering between 15 000 and the infection, among the more important being the exac- 25 000 inhabitants attended by a primary health team). erbation of comorbidities and delayed medical treatment. Following implemented guidelines, PCR testing was Also, psychological, and emotional distress due to social carried out when Covid-19 infection was suspected or isolation [11–14] and the lack of adequate end-of-life when LTCF residents had come in close contact with an care [15], frequently reported during the first wave of the infected individual (i.e. when three or more confirmed or pandemic, added to the impact. suspected cases of Covid-19 within the LTCF including Most of the previous articles on the impact of Covid-19 staff members were detected). Regular testing was imple- in LTCF premises have explored risk factors, both indi- mented starting in mid-April 2020 irrespective of infec- vidual [16] and structural [6], associated with mortal- tion suspicion or exposure. The outcomes of study were ity in LTCF residents. In previous articles, we analyzed infection (PCR positive) and death. contextual and clinical factors related to mortality of a local cohort during the first wave of Covid-19 in Europe Data collection and statistical analysis [6, 17]. In this article we aim to expand previous analysis Data was entered in the database either by health staff by focusing on epidemiological factors related to SARS- using an in-house app developed ad hoc [19] or using the CoV-2 infection in LTCF and the interaction between regional health service’s digital patient records (socio- contextual and societal factors in the evolution and demographic and clinical data), alongside PCR test results of SARS-CoV2 outbreaks and clinical prognosis. results sent from the reference laboratory serving the region. Data regarding incidence from the catchment Methods area was obtained from the official open-source data- Study population base [20] and are expressed by cases over 10,000 inhab- The study region comprises an area immediately to the itants. Community incidence excluded all notified cases north of the city of Barcelona in Catalonia, Spain. Com- from LTCF located in the specific catchment area. LTCF prising a mixture of urban, semi-rural, and rural munici- capacity (number of residents) and community cumula- palities, the area includes a total of 1 986 032 inhabitants, tive incidence were categorized according to interquar- with 190 LTCF which as of March first, 2020, housed a tile ranges (IQR) of <25, 25-50, 50-75 and >75. PCR tests total of 10737 residents. Of these LTCF, 168 (88.4%) were with inconclusive results were considered negative. institutions devoted to elderly adult patients and not The data was analyzed using Stata v14.0 software linked to an hospital institution, with a total of 9553 users (StataCorp, Texas) and R. For the descriptive analysis, registered. Lockdown came into force at these institu- we used means, medians, and Standard Deviation (SD) tions on March 15, 2020, and by the end of that month for continuous variables and proportions and a 95% an emergency task force of health professionals had been Confidence Interval (95%CI) for categorical variables. mobilized to provide back-up support to LTCF staff. Proportions were calculated for all participants with the given data available. For univariate analysis, we used the Study design Chi-Square test to compare categorical variables, and A cross-sectional study was carried out among a cohort the Student’s T test for continuous variables after test- study of residents of LTCF, defined as institutions which ing for normality (skewness and kurtosis tests), or their host for a long term people with age-related depend- non-parametric counterparts (Fisher test or Wilcoxon ency and are not linked to an hospital institution,, liv- test), when necessary. Multilevel mixed-effects logistic ing in the study area between first of March and June regression was used for multivariate analysis to explore Soldevila et al. BMC Geriatrics (2022) 22:123 Page 3 of 9 for the presence of clustering, and factors (LTCF and the study period and were included in the analysis (see catchment area) and tested by means of regress post-esti- Fig. 1). Women accounted for 5939 (74.1%) and men mation (likelihood ratio test, henceforth LR), against the for 2079 (25.9%). The mean age was 86.4 years (SD = usual logistic regression model. Crude and adjusted odds 7.4, range 65-107), with significant difference between ratios (OR and aOR), respective 95%CI and P values were males (83.4 yrs., SD = 7.9) and females (87.4, SD = estimated. 6.9; P < .001). Overall, 1115 (14.0%) had a cardiovas- cular comorbidity. The most frequently recorded indi- Laboratory methods (PCR test) vidual comorbidities were hypertension (n = 3855, Biological specimens were collected through naso- 48.3%) and dementia (n = 3666, 45.9%). A total of using the Aptima® SARS-CoV-2 assay following manu- pharyngeal swabs. Specific PCR tests were carried out 6013 patients presented functional impairment (80.3%) and 4171 (52.0%) an advanced condition. In the four- facturer instructions [21]. month study period, SARS-CoV-2 infection was detected in 2225 participants (27.7%), and 909 deaths Ethical approval were reported, of which 554 corresponded to residents The study was approved by the Ethics Board of the ref- with proven SARS-CoV-2 infection (Case Fatality Rate, erence hospital of the study region (Hospital Universitari henceforth CFR, 24.9%, see Fig. 1). At the LTCF level, Germans Trias i Pujol), registered under reference num- 97 institutions (57.7%) reported at least one confirmed ber PI-20-349, and was conducted in accordance with the case of SARS-CoV-2 infection, with attack rates rang- principles of the Declaration of Helsinki. ing from 1% to 95%. The median cumulative incidence of Covid-19 in the 52 catchment areas of the study Results region during the period of interest was 95 cases/10 Participant characteristics 000 inhabitants (range 34.7 to 158.2). Table 1 offers a A total of 9158 residents ≥65 years residing in 168 description of the main variables in the total popula- LTCF were included in the study, with a median occu- tion, and in the subgroup of infected people and those pancy of 41 (range 12 to 229, IQR 26-41) and distrib- that dye in the study period. Figure 2 shows the cumu- uted over 52 local catchment areas. Of these residents, lative incidence of SARS-CoV-2 among residents and 8021 (87.6%) underwent at least one PCR test during in catchment areas. Fig. 1 Flow-chart of study population and participants with PCR test available Soldevila et al. BMC Geriatrics (2022) 22:123 Page 4 of 9 Table 1 Prevalence of study variables stratified by infection Totala PCR positive Deathb (N = 8021) (N = 2225; 27.7%) (N = 909; 11.3%) Variable n % n % P n % P Gender Male 2079 25.9 597 28.7 .2 309 14.7 < .001 Female 5939 74.1 1626 27.4 600 10.1 Age in years (m, SD) 86.4 (7.4) 86.5 (7.3) .2 87.4 (7.1) < .001 65-74 638 8.0 166 26.0 .2 47 5.2 75-79 752 9.4 210 27.9 83 9.1 80-84 1362 17.0 346 25.4 133 14.6 < .001† 85-89 2289 28.6 663 29.0 260 28.6 ≥90 2977 37.1 838 28.2 386 42.5 Level of functional depdendence (low/high)c High level of functional dependence 6013 80.3 1497 24.9 < .001 357 5.9 < .001 Low level of functional dependence 1475 19.7 447 30.3 178 12.1 Comorbidities Hypertension 3855 48.3 1164 30.2 < .001 488 12.7 .001 Diabetes Mellitus-II 1593 20.0 471 29.6 .08 208 13.1 .02 Chronic renal insufficiency 1564 19.6 451 28.8 .3 230 14.7 < .001 Dementia 3666 45.9 1002 27.3 .4 472 12.9 < .001 Cardiovascular disease d 1115 14.0 363 32.6 < .001 170 15.3 < .001 Respiratory disease e 824 10.3 262 31.8 .007 124 15.1 < .001 Cerebrovascular disease 211 2.6 46 21.8 .05 28 13.3 .4 Clinical complexity Complex Chronic Condition 723 17.3 202 27.9 .9 533 12.8 < .001 Number of residents f ≤ 40 (N = 84) 2060 25.7 1464 17.6 < .001 194 9.4 < .001g 41-72 (N = 44) 1986 24.8 1419 22.3 196 9.9 73-108 (N = 25) 2049 25.6 1512 31.0 239 11.7 > 108 (N = 16) 1926 24.0 1407 40.7 280 14.5 Community cumulative incidence (cases by 10,000 inhabitants) ≤ 54.7 1994 25.4 1811 16.9 < .001 137 6.9 < .001g 54.8-72.9 1903 24.2 1620 28.6 221 11.6 73.0-83.9 1840 23.4 1515 30.0 200 10.9 ≥ 84.0 2115 26.9 1769 36.8 340 16.1 a Includes participants with data available b Includes mortality among participants with PCR test result available c Levels of functional dependence have been calculated using the Barthel score, which provides a range from 0 to 100. The cut-off between high and low functional dependence has been set up at 50 d Includes ischemic heart disease and heart insufficiency e Include Chronic Obstructive Pulmonary disease, asthma, and emphysema f N indicates the number of LTCF institutions included in each strata g P test for trend Risk factors associated to SARS‑CoV‑2 infection and death age, sex, and chronic conditions, except respiratory dis- Figure 3 displays the aOR of study variables with SARS- eases and cardiovascular disease (P values of .01 and CoV-2 infection and death in our analysis. In brief, the .005, respectively) and low level of functional depend- risk of infection by SARS-CoV-2 was independent of ence on daily living (low level of functional dependence Soldevila et al. BMC Geriatrics (2022) 22:123 Page 5 of 9 Fig. 2 Cumulative incidence of SARS-CoV-2 infection of LTCLTCF residents and corresponding catchment area. The testing coverage was similar between different catchment areas during the study period and was mainly focused on symptomatic cases and contacts of positive cases. The incidence shown here is therefore an underestimation of the true incidence but should be considered proportional to it and an acceptable proxy. The size of the pie charts are correlated to the number of LTCF residents registered in each catchment area, not to the size of the LTCF’s score, aOR 1.22; 95%CI 1.0-1.5; P = .03). There was a 95%CI 3.6-5.1; P < .001), followed by low functional linear correlation between the risk of infection and size dependence (aOR 2.42; 95%CI 1.8-3.2; P < .001), male of LTCF (pooled aOR 1.73; 95%CI 1.6-1.9; P < .001) and gender (aOR 1.75; 95%CI 1.5-2.1; P < .001) and older cumulative incidence in the catchment area (pooled aOR age (pooled aOR 1.16; 95%CI 1.1-1.2; P < .001), whereas 1.77; 95%CI 1.0-3.0; P = .04). We observed evidence of dementia and Complex Chronic Condition was associ- clustering by LTCF and catchment area regarding risk ated to mortality (aOR 1.33; 95%CI 1.2-1.6; P < .001 and of infection (P value of LR < .001). After adjusting for aOR 1.29; 95%CI 1.1-1.5; P < .001, respectively) but not study variables, epidemiological risk factors related to to infection. We observed evidence of clustering regard- infection that remain associated with mortality included ing mortality with LTCF and catchment area (P value SARS-CoV-2 infection (positive PCR test, aOR 4.26; of LR < .001). Furthermore, residents living in nursing homes located in catchment areas with a high incidence Soldevila et al. BMC Geriatrics (2022) 22:123 Page 6 of 9 Fig. 3 Forest plot of a OR and 95%CI of studied variables and infection (PCR positive) and death. §. Baseline strata. *Significative results (p ≤ 0,05) of SARS-CoV-2 (≥ 84/10 000 inhabitants) were at sub- LTCF staff and visiting relatives before the lockdown. stantially higher risk of mortality (pooled aOR 1.19; However, it cannot be ruled out that during the first wave 95%CI 1.1-1.3; P < .001). and before the lockdown, these institutions could have become, to a certain extent, hubs of SARS-CoV-2 infec- Discussion tion in the community. This would have been similar to Our results indicate that there is a complex interplay the role that community health centers played during the between the risk of SARS-CoV-2 infection and subse- 2014-2016 Ebola crisis in West Africa [24, 25]. LTCF staff quent clinical outcome, mediated by individual level fac- are known to have been heavily infected whilst at work tors (age, gender, and chronic conditions) and contextual [26, 27], prior to the implementation of effective conten- factors. Particularly, size of residence and community tion measures, and most probably also visiting relatives incidence showed the highest influence on infection before the lockdown, and to have spread the infection acquisition, as has been observed previously [6, 22], within the local communities specially in crowded, urban with high OR (3.18 and 2.28, respectively). This may be and densely populated areas. If this hypothesis turns out explained because large nursing homes were more sus- to be true, the rapid intervention in LTCF carried out by ceptible to a SARS-CoV-2 carrier entering the premises the health authorities’ right at the outset of the Covid-19 due to the higher number of visiting relatives and work- pandemic was more relevant than supposed. It is worth ing staff. Consequently, larger facilities had a greater noting that we do not consider this to be currently the likelihood of having one or more cases of Covid-19 com- case due to the strict Covid-19 prevention measures that pared to smaller ones; (88.1% vs. 37.0%, P < .001). How- have been applied in LTCF since mid of March (strict ever, our data showed highly heterogeneous attack rates lockdown, interdiction of leaving the premises and visits, once the infection was inside an institution (from 1% to generic non-pharmaceutical measures and the hand-over 95%). This may be related to structural factors of each of the LTCF clinical management to the Primary Health LTCF, which showed disparate features (including qual- care teams which occurred on 10 of April). Moreover, the ity of the service provided and residents’ clinical pro- correlation between mortality and community incidence file), as observed in a previous study involving this study has been observed elsewhere and by our group in a pre- population [6] and a comprehensive study carried out in vious analysis [6] and deserves further assessment using England [8]. This is consistent with the clustering effect the LTCF setting as unit of analysis. seen here. The correlation between community incidence Focusing on gender, we found that being male is not and risk of infection in LTCF has been described previ- correlated to SARs-CoV-2 infection but it is an independ- ously [23]. At first glance, the straight correlation may ent risk factor for severe Covid-19 disease, as previously reflect higher chances of irruption in LTCF of infected observed among general and elderly populations [16, 28]. individuals from the general population which include The underlying reasons have not yet been disentangled, Soldevila et al. BMC Geriatrics (2022) 22:123 Page 7 of 9 but this strongly suggests some genetic-based suscep- cases were screened, in later stages all exposed residents tibility [29]. In spite of this, considering the dispropor- and finally regular mass screenings were implemented). tion between males/females (25.9% vs. 74.1%), females Our cross-sectional approach relies under the assump- showed a much higher absolute number of fatalities (600 tion that almost all residents had similar chances to be vs. 309). This cannot simply be explained by the longer tested during the study period. As in other reports, our life expectancy of women but must also reflect societal data indicate that many deaths occurred in people who gender-based inequalities that increase the likelihood of were infected with Covid-19 but not tested [36]. The CFR females ending up in a LTCF compared to males. Given of this sample subset (those that did not undergo a PCR the disproportionate contribution of LTCF residents to test) was 69.2% (n = 798, see Fig. 1), which increases the the global rate of Covid-19 deaths [1], the observed over- death toll rate of our study population to 18.6%. This representation of female mortality in Spain [30] may be toll is close to the expected total mortality rate among explained by, first, an increased proportion of females in our cohort for an entire year [37]. Considering that Spanish LTCF compared to other countries and, second, most fatalities were Covid-19 patients, the specific CFR the greater impact of the first wave of Covid-19 in LTCF among SARS-CoV-2-infected residents was around 50%. observed in this country [30]. This estimate lies in the upper bounds of previous esti- Besides these factors, we observed an intriguing inter- mates [1, 27, 38]. Therefore, because it included only play between risk of infection and mortality. More patients for whom a PCR test was available and thus pos- autonomous residents (low level of functional depend- sibly excludes the most vulnerable patients, our analysis ence) showed a notably higher risk of SARS-CoV-2 infec- could be to a certain extent biased. Non-tested residents tion, but a disproportionate mortality rate as well, as tended to be older (87.4 years vs. 86.4, p < .001), although we published previously [17]. This may be explained by the gender distribution was similar (p = .2). Nonethe- the fact that residents with greater autonomy may have less, the lower mortality rate observed in later stages had a higher rate of social contacts inside the LTCF and may reflect the effectiveness of the contention measures therefore a higher probability of exposure to infection. implemented. Otherwise, a number of variables that may The higher risk of mortality once infected may be a con- influence on the risk of infection (i.e. proximity between sequence of more efficient transmission and/or multiple residents or number of staff who tested positive) have infections (closeness to and increased frequency of risky not been considered in this study but were extensively contacts) with associated to higher viral loads, which reported in the referenced work in the same study popu- has been correlated with mortality [31]. This association lation [6]. between risk of infection and autonomy as measured Overall, our results may explain the much higher CFR by Activities of Daily Living scores has been previously (around 40%) of older adults living in LTCF infected by observed but not discussed [3]. The increased risk of SARS-CoV-2 compared to the general CFR observed in infection associated with cardiovascular and respiratory people older than 80 years old, estimated to be 14.5% disease could easily be biased in a population with a high [39]. due to the interaction between of structural (institu- prevalence of such conditions. According other reports, tional), as the clustering of our data suggests, which were besides chronic renal failure [17], we observed a lack of in turn consequence of societal and implemented poli- association between negative outcome and other under- cies, and individual factors (related to chronic/advanced lying comorbidities described among general populations conditions, age, gender and autonomy level, as previ- [28, 32, 33], and patients with Covid-19 in geriatric care ously discussed [17], which may be more or less preva- [34]. We hypothesized that in the context of extremely lent in each facility. However, it is worth noting that these high attack rates in LTCF, once SARS-CoV-2 infection results correspond to the conditions of the first wave of occurs tends to behave independently of underlying risk a pandemic, which tends to be characterized by a lack factors, like a primary pathogen. Furthermore, existing of preparedness against an unknown pathogen. There- medications may have had a substantial effect against fore, other risk factors correlated to infection and nega- infection or severe disease in a population that is usually tive outcome in LTCF may emerge in later stages of the polymedicated [35]. pandemic. Our study has some limitations. A substantial num- In spite of the overwhelmingly positive impact of the ber of residents did not undergo PCR testing (n = vaccination of LTCF residents [40, 41], given the cur- 1154; 12.6%) because it was not possible to mobilize rent uncertainty about the role of vaccines in prevent- enough material and human resources in time amidst ing transmission in nursing homes at mid and long term, the extremely demanding circumstances of the early as well as the impact of new variants of the virus [42], stages of the epidemic wave, and only later on was gen- research on Covid-19 in LTCF facilities should still be eral screening implemented (firstly, only symptomatic prioritized. The scope of research Covid-19 in nursing Soldevila et al. BMC Geriatrics (2022) 22:123 Page 8 of 9 homes should be expanded, as well, to ascertain the indi- Consent for publication All authors consent with the publication in the BMC Geriatrics rect consequences of not only lockdown measures but also measures intended to mitigate these effects (i.e. to Competing interests safely allow family visits) [43–45] as well as the ways by None to declare. which such measures might be avoided in the future [46] Author details Furthermore, long-term policies should address struc- 1 International Health Program, Regió Sanitària Metropolitana Nord, Institut tural factors underlined by our results and previous pub- Català de la Salut, Badalona, Spain. 2 Infectious Diseases Unit, Hospital Uni‑ versitari Germans Trias i Pujol, Badalona, Spain. 3 Departament de Medicina, lications, to create a more adequate elderly care system Universitat Autònoma de Barcelona, Bellaterra, Spain. 4 Fight AIDS and Infec‑ like the prioritization of home-based care, the promotion tious Diseases Foundation, Badalona, Spain. 5 Direcció d’Atenció Primària of affordable smaller-scale, high-quality group models Metropolitana Nord, Institut Català de la Salut, Sabadell, Spain. 6 Direcció Clínica Territorial de Cronicitat Metropolitana Nord, Institut Català de la Salut, with a community-based approach for those that caregiv- Badalona, Spain. 7 Department of Geriatrics, Hospital Universitari Germans ing at home is not feasible, and a more comprehensive Trias i Pujol, Badalona, Spain. 8 Institut per la Recerca en Ciències de la Salut and non-profit orientated regulations [47]. Germans Trias i Pujol, Badalona, Spain. Received: 12 August 2021 Accepted: 13 January 2022 Conclusions There was a complex interplay between structural and individual factors regarding Covid-19 infection and its References impact on mortality in nursing-home residents dur- 1. Comas-Herrera A, Zalakaín J, Lemmon E, et al. In: Mortality associated ing the first epidemic wave. The overwhelming impact with Covid-19 outbreaks in care homes Mortality associated with Covid- 19 outbreaks in care homes: early international evidence, 2020. https://​ on LTCF residents could be partially explained by the LTCCo​vid.​org/​2020/​04/​12/​morta​lity-​assoc​iated-​with-​Covid-​19-​outbr​eaks-​ intersect of lack of preparedness and structural factors. in-​care-​homes-​early-​inter​natio​nal-​evide​nce. Accessed 15 June 2021. Risk of SARS-CoV-2 infection was mainly associated to 2. Ouslander JG, Grabowski DC. Covid-19 in Nursing Homes: Calming the Perfect Storm. J Am Geriatr Soc 2020. https://​doi.​org/​10.​1111/​jgs.​16995 contextual level factors (i.e. LTCF structure), whereas 3. Unruh MA, Yun H, Zhang Y et al. Nursing Home Characteristics Associated risk of mortality to individual level factors (i.e. frailty). With Covid-19 Deaths in Connecticut, New Jersey, and New York. J Am Long-term policies should be implemented to develop a Med Dir Assoc 2020. https://​doi.​org/​10.​1016/j.​jamda.​2020.​06.​019 4. Abrams HR, Loomer L, Gandhi A, Grabowski DC. Characteristics of U.S. residential system more resilient to epidemic surges. Sec- Nursing Homes with Covid-19 Cases. J Am Geriatr Soc 2020. https://​doi.​ ondary effects due to lockdowns and social restrictions org/​10.​1016/​10.​1111/​jgs.​16661 among elderly residents should be investigated. 5. Chapman S, Harrington C. Policies Matter! Factors Contributing to Nurs‑ ing Home Outbreaks During the Covid-19 Pandemic Policy. Polit Nurs Pract 2020. https://​doi.​org/​10.​1177/​15271​54420​959021 6. Suñer C, Ouchi D, Mas MA et al. Risk factors for mortality of residents in Authors’ contributions nursing homes with Covid-19: A retrospective cohort study. Nat Aging LS, NP, MAM, RM, MM, OE and XV conceptualized and designed the study. JB, 2021; https://​doi.​org/​10.​1038/​s43587-​021-​00079-7 MI, ME, IG, SR, NM, EB, GL and JS contributed to the data collection, literature 7. Belmin J, Georges S, Franke F et al. Coronavirus Disease 2019 in French revisions and systematization. JS, GL and XV carried out the statistical analysis Residential Care Facilities: A Nationwide Study. J Am Med Dir Assoc 2021; and performed the tables and figures. LS, MAM, RM, MM and XV drafted the https://​doi.​org/​10.​1016/j.​jamda.​2021.​03.​013 manuscript and made final revisions. All authors critically revised, read and 8. Shallcross L, Burke D, Abbott O et al. Factors associated with SARS-CoV-2 approved the final manuscript infection and outbreaks in long-term care facilities in England: a national cross-sectional survey. Lancet Healthy Longev 2021. https://​doi.​org/​10.​ Funding 1016/​S2666-​7568(20)​30065-9 This research did not receive any funding from agencies in the public, com‑ 9. Werner RM, Hoffman AK, Coe NB. Long-Term Care Policy after Covid-19 mercial, or not-for-profit sectors. — Solving the Nursing Home Crisis. N Engl J Med 2020; https://​doi.​org/​ 10.​1056/​NEJMp​20148​11 Availability of data and materials 10. O’Neill D, Briggs R, Holmerová I, Samuelsson O et al. Covid-19 highlights The data underlying this article cannot be shared publicly due to it is subject the need for universal adoption of standards of medical care for physi‑ to Ethical approval before accessing to it. The data will be shared on reason‑ cians in nursing homes in Europe. Eur Geriatr Med 2020. https://​doi.​org/​ able request to the corresponding author and with previous Ethical Approval 10.​1007/​s41999-​020-​00347-6 by the Ethics Board of reference. 11. Miller EA. Protecting and Improving the Lives of Older Adults in the Covid-19 Era. J Aging Soc Policy 2020. https://​doi.​org/​10.​1080/​08959​420.​ Declarations 2020.​17801​04 12. Simonetti A, Pais C, Jones M et al. Neuropsychiatric Symptoms in Elderly Ethics approval and consent to participate With Dementia During Covid-19 Pandemic: Definition, Treatment, and The study was approved by the Ethics Board of the reference hospital of the Future Directions. Front Psychiatry 2020. https://​doi.​org/​10.​3389/​fpsyt.​ study region (Hospital Universitari Germans Trias i Pujol), registered under 2020.​579842 reference number PI-20-349, and was conducted in accordance with the 13. Lombardo FL, Salvi E, Lacorte E et al. Adverse Events in Italian Nursing principles of the Declaration of Helsinki. Homes During the Covid-19 Epidemic: A National Survey. Front Psychia‑ The consent form from participants was waived since all study data was try 2020. https://​doi.​org/​10.​3389/​fpsyt.​2020. retrospectively obtained from the routine clinical data registration system with 14. Ayalon L, Zisberg A, Cohn-Schwartz E et al. Long-term care settings in previous anonymization. the times of Covid-19: challenges and future directions. Int Psychogeriatr 2020. https://​doi.​org/​10.​1017/​S1041​61022​00014​16 Soldevila et al. BMC Geriatrics (2022) 22:123 Page 9 of 9 15. Strang P, Bergström J, Martinsson L et al. Dying From Covid-19: Loneli‑ long-term care facilities: an exploratory analysis. Int J Infect Dis. 2021. ness, End-of-Life Discussions, and Support for Patients and Their Families https://​doi.​org/​10.​1016/j.​ijid.​2021.​07.​007. in Nursing Homes and Hospitals. A National Register Study. J Pain Symp‑ 36. Dutey-Magni PF, Williams H, Jhass A et al. Covid-19 infection and attribut‑ tom Manage 2020. https://​doi.​org/​10.​1016/j.​jpain​symman.​2020.​07.​020 able mortality in UK care homes: Cohort study using active surveillance 16. Panagiotou OA, Kosar CM, White EM et al. Risk Factors Associated With and electronic records (March-June 2020). Age Ageing 2021. https://​doi.​ All-Cause 30-Day Mortality in Nursing Home Residents With Covid-19. org/​10.​1093/​ageing/​afab0​60. JAMA Intern Med 2021. https://​doi.​org/​10.​1001/​jamai​ntern​med.​2020.​ 37. Amblàs-Novellas J, Santaeugènia SJ, Vela E et al. What lies beneath: A 7968 retrospective, population-based cohort study investigating clinical and 17. Mas MA, Massot M, Miralles R et al. Clinical factors related to Covid-19 resource-use characteristics of institutionalized older people in Catalonia. outcomes in institutionalized older adults: cross-sectional analysis from a BMC Geriatr 2020. https://​doi.​org/​10.​1186/​s12877-​020-​01587-8 cohort in Catalonia. J Am Med Dir Assoc 2021. https://​doi.​org/​10.​1016/j.​ 38. Graham NSN, Junghans C, Downes R et al. SARS-CoV-2 infection, clinical jamda.​2021.​07.​004 features and outcome of Covid-19 in United Kingdom nursing homes. J 18. Contel JC, Ledesma A, Blay C et al. Chronic and integrated care in Catalo‑ Infect 2020. https://​doi.​org/​10.​1016/j.​jinf.​2020.​05.​073. nia. Int J Integr Care. 2015. https://​doi.​org/​10.​5334/​ijic.​2205 39. Wu Z, McGoogan JM. Characteristics of and Important Lessons From 19. Echeverría P, Mas Bergas MA, Puig J et al. CovidApp as an Innovative Strat‑ the Coronavirus Disease 2019 (Covid-19) Outbreak in China: Summary egy for the Management and Follow-Up of Covid-19 Cases in Long-Term of a Report of 72314 Cases From Chinese Center for Disease Control and Care Facilities in Catalonia: Implementation Study. JMIR Public Health Prevention. JAMA 2020. https://​doi.​org/​10.​1001/​jama.​2020.​2648 Surveill 2020. https://​doi.​org/​10.​2196/​21163 40. Mor V, Gutman R, Yang X et al. Short-term impact of nursing home SARS- 20. AQUAS. In: Map of Coronavirus Incidence from Catalonia. 2020. https://​ CoV-2 vaccinations on new infections, hospitalizations, and deaths. J Am aquas.​gencat.​cat/​ca/​actua​litat/​ultim​es-​dades-​coron​avirus/​mapa-​per-​ Geriatr Soc. 2021. https://​doi.​org/​10.​1111/​jgs.​17176 munic​ipis/. Accessed Feb 2021 41. White EM, Yang X, Blackman C, Feifer RA, Gravenstein S, Mor V. Incident 21. Pham J, Meyer S, Nguyen C et al. Performance Characteristics of a High- SARS-CoV-2 Infection among mRNA-Vaccinated and Unvaccinated Nurs‑ Throughput Automated Transcription-Mediated Amplification Test for ing Home Residents. N Engl J Med 2021. https://​doi.​org/​10.​1056/​NEJMc​ SARS-CoV-2 Detection. J Clin Microbiol 2020. https://​doi.​org/​10.​1128/​ 21048​49. JCM.​01669-​20 42. National Collaborating Centre for Methods and Tools. In:What strategies 22. Costa AP, Manis DR, Jones A et al. Risk factors for outbreaks of SARS-CoV-2 mitigate risk of Covid-19 outbreaks and mortality in long-term care facili‑ infection at retirement homes in Ontario, Canada: a population-level ties? Update 2. https://​www.​nccmt.​ca/​knowl​edge-​repos​itori​es/​Covid-​19-​ cohort study. CMAJ 2021. https://​doi.​org/​10.​1503/​cmaj.​202756 rapid-​evide​nce-​servi​ce. Accessed Apr 2021 23. Chatterjee P, Kelly S, Qi M, Werner RM. Characteristics and Quality of US 43. Verbeek H, Gerritsen DL, Backhaus R et al. Allowing Visitors Back in the Nursing Homes Reporting Cases of Coronavirus Disease 2019 (Covid-19). Nursing Home During the Covid-19 Crisis: A Dutch National Study Into JAMA Netw Open 2020. https://​doi.​org/​10.​1001/​jaman​etwor​kopen.​2020.​ First Experiences and Impact on Well-Being. J Am Me Di Assoc 2020. 16930. https://​doi.​org/​10.​1016/j.​jamda.​2020.​06.​020 24. Fischer WA, Hynes NA, Perl TM. Protecting Health Care Workers From 44. Hado E, FrissFeinberg L. Amid the Covid-19 Pandemic, Meaningful Com‑ Ebola: Personal Protective Equipment Is Critical but Is Not Enough. Ann munication between Family Caregivers and Residents of Long-Term Care Intern Med 2014. https://​doi.​org/​10.​7326/​M14-​1953. Facilities is Imperative. J Aging Soc Policy 2020. https://​doi.​org/​10.​1080/​ 25. Kilmarx PH, Clarke KR, Dietz PM et al. Ebola virus disease in health 08959​420.​2020.​17656​84 care workers—Sierra Leone, 2014. MMWR Morb Mortal Wkly Rep 45. van Dyck LI, Wilkins KM, Ouellet J et al. Combating Heightened Social 2014;12:1168–71. Isolation of Nursing Home Elders: The Telephone Outreach in the Covid- 26. Ladhani SN, Chow JY, Janarthanan R et al. Increased risk of SARS-CoV-2 19 Outbreak Program. Am J Geriatr Psychiatry 2020. https://​doi.​org/​10.​ infection in staff working across different care homes: enhanced Covid- 1016/j.​jagp.​2020.​05.​026 19 outbreak investigations in London care Homes. J Infect 2020. https://​ 46. Anderson DC, Grey T, Kennelly S, O’Neill D. Nursing Home Design and doi.​org/​10.​1016/j.​jinf.​2020.​07.​027. Covid-19: Balancing Infection Control, Quality of Life, and Resilience. J Am 27. Sacco G, Foucault G, Briere O, Annweiler C. Covid-19 in seniors: Findings Med Dir Assoc 2020. https://​doi.​org/​10.​1016/j.​jamda.​2020.​09.​005 and lessons from mass screening in a nursing home. Maturitas 2020. 47. Werner RM, Hoffman AK, Coe NB. Long-Term Care Policy after Covid-19 - https://​doi.​org/​10.​1016/j.​matur​itas.​2020.​06.​023. Solving the Nursing Home Crisis. N Engl J Med. 2020. https://​doi.​org/​10.​ 28. Chang TS, Ding Y, Freund MK et al. Prior diagnoses and medications as risk 1056/​NEJMp​20148​11 factors for Covid-19 in a Los Angeles Health System. medRxiv [Preprint] 2020. https://​doi.​org/​10.​1101/​2020.​07.​03.​20145​581. 29. Cao Y, Li L, Feng Z, Wan S et al. Comparative genetic analysis of the novel Publisher’s Note coronavirus (2019-nCoV/SARS-CoV-2) receptor ACE2 in different popula‑ Springer Nature remains neutral with regard to jurisdictional claims in pub‑ tions. Cell Discov 2020. https://​doi.​org/​10.​1038/​s41421-​020-​0147-1 lished maps and institutional affiliations. 30. Kontis V, Bennett JE, Rashid T et al. Magnitude, demographics and dynamics of the effect of the first wave of the Covid-19 pandemic on all- cause mortality in 21 industrialized countries. Nat Med 2020. https://​doi.​ org/​10.​1038/​s41591-​020-​1112-​02014;​63:​1168-​71. 31. Pujadas E, Chaudhry F, McBride R et al. SARS-CoV-2 viral load predicts Covid-19 mortality. Lancet Respir Med 2020. https://​doi.​org/​10.​1016/​ Ready to submit your research ? Choose BMC and benefit from: S2213-​2600(20)​30354-4. 32. Zheng Z, Peng F, Xu B et al. Risk factors of critical & mortal Covid-19 cases: • fast, convenient online submission A systematic literature review and meta-analysis. J Infect 2020. https://​ doi.​org/​10.​1016/j.​jinf.​2020.​04.​021. • thorough peer review by experienced researchers in your field 33. Fang X, Li S, Yu H et al. Epidemiological, comorbidity factors with severity • rapid publication on acceptance and prognosis of Covid-19: a systematic review and meta-analysis. Aging • support for research data, including large and complex data types (Albany NY) 2020. https://​doi.​org/​10.​18632/​aging.​103579. 34. Hägg S, Jylhävä J, Wang Y et al. Age, Frailty, and Comorbidity as Prognos‑ • gold Open Access which fosters wider collaboration and increased citations tic Factors for Short-Term Outcomes in Patients With Coronavirus Disease • maximum visibility for your research: over 100M website views per year 2019 in Geriatric Care. J Am Med Dir Assoc 2020. https://​doi.​org/​10.​ 1016/j.​jamda.​2020.​08.​014. At BMC, research is always in progress. 35. Soldevila L, Valerio-Sallent L, Roure S et al. Drug exposure may have a substantial influence on Covid-19 prognosis among residents of Learn more biomedcentral.com/submissions