The Italian national survey on Coronavirus disease 2019 epidemic spread in nursing homes

Abstract Introduction Residents in facilities such as nursing homes (NHs) are particularly vulnerable to Coronavirus disease 2019 (COVID‐19). A national survey was carried out to collect information on the spreading and impact of severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2) infection in nursing homes, and on how suspected and/or confirmed cases were managed. We carried out a survey between 25 March 2020 and 5 May 2020. Materials and Methods All Italian nursing homes either public or providing services both privately and within the NHS were included in the study. An on‐line questionnaire was sent to 3292 nursing homes across all Italian regions. Nursing homes were also contacted by telephone to provide assistance in completing the questionnaire. Results A total of 1356 nursing homes voluntarily participated to the survey, hosting a total of 100,806 residents. Overall, 9154 residents died due to any cause from February 1 to the time when the questionnaire was completed (from March 25 to May 5). Of these, 7.4% had COVID‐19 and 33.8% had flu‐like symptoms, corresponding to a cumulative incidence of 0.7 and 3.1, respectively. Lack of personnel, difficulty in transferring patients to hospital or other facility, isolating residents with COVID‐19, number of beds and geographical area were the main factor positively associated to the presence of COVID‐19 in nursing homes. Discussion This survey showed the dissemination and impact of SARS‐CoV‐2 infection in Italian nursing homes and on how older and potentially chronically ill people residing in these long‐term care facilities were managed.

2 infection, is an acute respiratory infection mainly involving the lower respiratory tract. Symptoms are usually mild, and some people may also remain completely asymptomatic throughout the course of the disease. However, some people can develop more severe symptoms, that may lead to life threatening complications and even death. This unfavorable course has mostly been observed among frail, older people, who are paying the highest toll in the ongoing pandemic. 5 An analysis of a subgroup of patients with COVID-19 deceased in Italy confirmed the higher mean age of patients (79.5 years) and the higher frequency of underlying conditions such as ischemic heart disease (30%), diabetes (35.5%), active cancer (20.3%), or atrial fibrillation (24.5%), with 48.5% having ≥3 underlying conditions, with a case fatality rate of 12.8% in people aged 70-79 years and of 20.8% in people aged ≥80 years. 5 Then, advancing age and the presence of concomitant chronic conditions (e.g., ischemic heart disease, diabetes, and cancer) have been reported as relevant risk factors for poorer outcomes. 5 Therefore, the elderly and chronically ill people residing in longterm care facilities such as nursing homes (NHs) are particularly vulnerable to COVID-19 [6][7][8][9][10][11][12][13] as they live in a communal setting along with other at-risk people. This close contact 10,14 can exponentially increase the risk of outbreaks of COVID-19 within these structures. 7,9,10 In addition, staff members in NHs often work in multiple facilities, including hospitals and clinics, thus increasing the risk of spreading the virus. This close contact, along with a higher vulnerability of older residents, due to their comorbid chronic conditions, 10,14 can exponentially increase the risk of outbreaks of COVID-19 within this type of facilities. 7,9,10 Moreover, a lack of personal protective equipment (PPE) was recorded in all the country due to the sudden increase in the request, and facilities might not guarantee a timely isolation, transferral, and care of positive patients. 11 The role of staff members in containing the infection is essential in both recognizing the symptoms among frail residents, and preventing and controlling the epidemic within the facility. 15 All these aspects highlight the vulnerability of long-term care facilities to COVID-19 outbreaks and thus the need to protect and monitor the safety of both residents and staff members in NHs and other long-term care facilities. [9][10][11][16][17][18] In this context, the Italian National Institute of Health (INIH) in collaboration with the Italian National Guarantor for the rights of persons detained or deprived of liberty, carried out a flash survey aiming at collecting information, provided on a voluntary basis, on the spreading and impact of SARS-CoV-2 infection in NHs and on how potential cases were managed.

| METHODS
This national survey involved 3292 NHs, either public or providing services both privately and within the national health system, out of the 3417 NHs covering the whole Italian territory (Figure 1). We included all the NHs for which we had an available reference contact.
The list of NHs was provided by the Dementia Observatory, an online map of Italian dementia services, constituting one of the objectives of the implementation of the Italian National Dementia Plan. 19,20

| Data source
A questionnaire with a cover letter was addressed to the director of each NH between 24 March and 27 April 2020. NHs were also contacted by telephone to provide assistance in completing the questionnaire. Some of the NHs were further contacted to solve incongruences in some of the provided data. The questionnaire was

| Statistical analysis
Descriptive statistics were performed on overall data and by region.
Frequencies were used to describe dichotomous variables, means and standard deviations were used for continuous variable, and median and range values for data with asymmetric distributions. The nonparametric Spearman rank coefficient was used to assess potential correlations between measures. Data from the national surveillance system 22 were used to test for possible correlations with the spreading of COVID-19 at a regional level. Missing data on number of residents were imputed using the number of beds.
No other data were imputed. An univariate and a multivariate regression logistic model were performed to assess whether critical aspects and characteristics of the NHs, adjusted for geographical area, were associated to COVID-19 outbreaks defined as the presence of laboratory-confirmed cases among deceased and hospitalized residents or staff members, and among residents currently living in the facility.
Interaction of factors with the time of response categorized as either within 3 weeks or after 3 weeks from the start of the survey, was tested. This cut-off was chosen because after week 3 an increased proportion of NHs with an outbreak was observed compared to the previous weeks. A separate multivariate model was performed for lack of laboratory tests as these data were gathered starting from April 8.
A sensitivity analysis was performed including also flu-like symptoms within the definition of COVID-19 outbreak.
All data analyses were performed using STATA software, version

(Stata Corp).
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.

| Response rate
Overall, 1356 (41.2%) of the 3292 NHs that were contacted responded to the survey as of May 5. A total of 52% of the NHs responded within 2 weeks from the first email. A response rate F I G U R E 1 Number of nursing homes (percentage on the total) and COVID-19 attack rates (per 100,000 habitants) [Colour figure can be viewed at wileyonlinelibrary.com] LOMBARDO ET AL.
-875 higher than 40% was achieved in some of the regions with a high number of COVID-19 cases (Table 1). However, a negative association was observed between the response rate and the attack rate per region, even if not statistically significant (Spearman's rho = -0.21, p = 0.344). Two of the 21 regions did not participate in the survey.
All questionnaires were considered as completed, as the proportion of answers was higher than 93% for all questions and 98% for crucial questions. The number of residents was missing for seven NHs, therefore these data were imputed using the number of beds.
Overall, a total of 100,806 residents were living in the interviewed NHs (Table 1).

| Characteristics of the facilities
This survey included either public structures or structures providing services both privately and within the NHS. A median of 60 beds (range 8-667) per facility was reported, with a wide variability between regions. When considering the number of HCSW, the NHs T A B L E 1 Distribution and description of facilities (response rate, number of participating nursing homes, residents, number of beds, and average number of beds per unit of staff), overall and by region reported a median of 32 workers per facility, with a mean of two beds per HCSW in each facility (Table 1).

| Infection prevention and control
The management of residents with COVID-19 (suspected or labo-

| Factors associated with the spreading of COVID-19
Univariate and multivariate logistic models were performed to  Table 4).
The sensitivity analysis performed including influenza-like symptoms in the definition of no COVID-19 free NH substantially confirmed the results (Table S1).

| DISCUSSION
To our knowledge, this is the first national survey carried out among nursing home conducted during the COVID-19 pandemics.
The mortality profile in the Italian NHs was influenced by the spreading of the epidemics among the Italian regions. In particular, a higher mortality rate was observed in the northern regions of Italy.
Moreover, in the Center, South and Islands of Italy, the observed outbreaks were mainly delimited in the areas where NHs were located. 23  isolating them in a single room, lack of medications and impossibility to perform swab tests. Moreover, the NHs with a higher number of beds were probably at a higher risk to develop an outbreak ( Table 4).
The association between lack of PPE and status of the NHs was different depending on whether NHs responded to the survey within the first 3 weeks of the survey or after 3 weeks (Table 4). This is probably due to when the questionnaire was completed, considering that the number of facilities with an active outbreak increased over This information was gathered in a second wave of the survey, therefore the OR is referred to a model performed in a subset of data collected since April 8, that is starting week 3 (n = 598).

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issues that have affected the NHs across all the countries 6,8,12 with the objective of protecting one of the most vulnerable group of population.

| Lessons learned so far and implementation of active surveillance systems
Measures adopted in the first phase of COVID-19 outbreak in Italy contributed significantly to the flattening of the epidemic curve with reduction of new cases and consequent lightening of the care response borne by the health service. However, human lives lost, especially among elderly residents living in NHs due to SARS-CoV-2 exposed major flaws in health care system. Currently, the consoli-