The burden of COVID-19 in long-term care facilities (LTCFs) was high worldwide. According to an Italian national survey, during the first pandemic wave, of the 33.8% of residents who died with COVID-19–like symptoms, only 7.4% had tested positive to a SARS-CoV-2 swab test because of limitations in accessing diagnostic tests.1 The prevalence of frailty, multimorbidity, and dementia,2 , 3 as well as the frequent atypical or asymptomatic manifestations of COVID-19 in such populations,4 were some of the factors that contributed to the spread of the infection in this setting. The picture was further complicated by the fact that a substantial number of residents suffered from conditions that mimic SARS-CoV-2 infection.5 In this study, we aimed to investigate the clinical features associated with SARS-CoV-2 infection and mortality due to COVID-19 in Italian LTCFs.
A prospective study with a 60-day follow-up was performed in a sample of Italian LTCFs, from March 1, 2020, up to December 31, 2020, as part of the GeroCovid Observational study, a multicenter and multisetting study, evaluating the impact of the COVID-19 pandemic on the health of individuals aged ≥60 years in acute, outpatient, and LTC settings.6 The GeroCovid cohort consists of 39 LTCFs from 6 Italian regions, 9 of which reported positive COVID-19 cases. The total number of residents in the facilities involved was 2380; of these, a subsample of 586 aged ≥60 years was enrolled based on the presence of signs and symptoms suspect for COVID-19 or on a judgment of high risk of infection. The residents who had a direct physical contact or a stay in a closed environment with a COVID-19–confirmed case with no suitable personal protective equipment (close contact) were considered at high risk of infection. Furthermore, all new patients admitted to a facility and all residents readmitted after a hospital stay were also considered at high risk of infection. The residents at high risk or with COVID-19–like symptoms underwent SARS-CoV-2 swab testing. Based on the swab results and the above risk factors of infection, we categorized the residents into 3 groups: (1) positive SARS-CoV-2 swab; (2) negative SARS-CoV-2 swab with close contact (asymptomatic); and (3) negative SARS-CoV-2 swab with clinical suspicion (symptomatic). For each participant, we collected data on demographic characteristics, lifestyle, chronic diseases, and clinical outcome in an electronic registry.7 These characteristics were compared among the 3 groups of residents through chi-squared or Fisher exact tests for the categorical variables, and generalized linear model or the Wilcoxon sum-rank test, as appropriate. Multivariate Cox proportional hazard models were used to identify factors associated with death.
As reported in Table 1 , SARS-CoV-2–positive residents were older compared with both SARS-CoV-2–negative groups. The median number of chronic diseases was 3 among SARS-CoV-2–positive residents, 2 among asymptomatic, and 5 among symptomatic SARSCoV-2–negative residents.
Table 1.
Characteristics of Older Adults Enrolled in the GeroCovid LTCFs Study by SARS-CoV-2 Positive or Negative Swab Test, Clinical Suspicion, and High Risk of Infection
| SARS-CoV-2–Positive (n = 179) | SARS-CoV-2–Negative With Close Contact (Asymptomatic) (n = 203) |
SARS-CoV-2–Negative With Clinical Suspicion (Symptomatic) (n = 121) |
P Value | |
|---|---|---|---|---|
| Age, y, mean±SD | 85.6 ± 8.2 | 83.5 ± 9.0 | 84.8 ± 8.8 | .05 |
| Sex, female, n (%) | 135 (75.4) | 156 (76.9) | 91 (75.2) | .93 |
| Smoking status, n (%) | .54 | |||
| Current smoker | 1 (1.5) | 3 (3.5) | 5 (5.3) | |
| Ex-smoker | 14 (20.3) | 11 (12.9) | 16 (16.8) | |
| Nonsmoker | 54 (78.3) | 71 (83.5) | 74 (77.9) | |
| Chronic diseases, n (%)‡ | ||||
| Arterial hypertension | 82 (46.6) | 127 (76.5) | 91 (75.2) | <.001 |
| Cardiomyopathy∗ | 75 (42.4) | 24 (27.0) | 64 (53.8) | <.001 |
| Atrial fibrillation | 6 (6.1) | 7 (8.9) | 16 (14.7) | .11 |
| Central and peripheral arterial disease | 68 (38.9) | 12 (13.3) | 17 (14.3) | <.001 |
| Cardiac failure | 13 (10.6) | 13 (16.1) | 16 (14.6) | .48 |
| Stroke | 30 (24.4) | 9 (11.0) | 18 (16.5) | .044 |
| Diabetes (type 1 or 2) | 47 (27.2) | 40 (37.7) | 32 (26.7) | .12 |
| Depression | 65 (31.4) | 47 (42.7) | 35 (29.7) | .07 |
| Osteoarthrosis | 66 (54.1) | 21 (25.6) | 71 (67.0) | <.001 |
| COPD† | 26 (15.1) | 22 (23.2) | 26 (21.9) | .187 |
| Chronic renal failure | 16 (9.2) | 6 (6.9) | 23 (19.8) | .006 |
| Chronic liver disease | 10 (5.7) | 9 (10.3) | 3 (2.5) | .06 |
| Obesity | 14 (12.0) | 4 (5.4) | 17 (15.7) | .10 |
| Poor nutritional status | 33 (28.0) | 2 (2.7) | 42 (38.5) | <.001 |
| Psychiatric disorders | 46 (43.0) | 77 (48.1) | 55 (51.4) | .46 |
| Nervous system disorders | 73 (68.2) | 42 (26.4) | 62 (56.9) | <.001 |
| Dementia or cognitive impairment | 45 (42.5) | 10 (6.3) | 35 (33.0) | <.001 |
| Total number of chronic diseases, median (Q1, Q3) | 3 (2, 5) | 2 (1, 3) | 5 (3, 6) | .002 |
| Chronic diseases, n (%) | <.001 | |||
| 0, 1, 2 | 20 (11.2) | 76 (37.4) | 1 (0.8) | |
| 3+ | 159 (88.8) | 127 (62.6) | 120 (99.2) |
Q1, quartile 1; Q3, quartile 3; SD, standard deviation.
Ischemic, valvulopathy, or arrhythmia.
Or other bronchopneumopathies.
Information before COVID-19 incidence.
Concerning the patterns of chronic diseases, we found that dementia or cognitive impairment and central and peripheral arterial disease were more prevalent in SARS-CoV-2–positive residents compared with SARS-CoV-2–negative groups; arterial hypertension, cardiomyopathy, osteoarthrosis, and poor nutritional status were more prevalent in SARS-CoV-2–negative residents with suspicious symptoms compared to SARS-CoV-2 asymptomatic and SARS-CoV-2–positive residents. The mortality of SARS-CoV-2–positive residents was 21.6%, compared to 10.8% among SARS-CoV-2–negative symptomatic residents [hazard ratio (HR) 0.27, 95% confidence interval (CI) 0.12-0.59, P = .001), and 1.8% among SARS-CoV-2–negative asymptomatic residents (HR 0.07, 95% CI 0.02-0.25, P = .001).
Our results are partly in line with those of previous studies. For instance, the frequency of hypertension among patients with COVID-19 who were enrolled in other studies ranged between 15% and 35%.7 In our sample, the lower prevalence of hypertension found among SARS-CoV-2–positive residents compared to symptomatic or asymptomatic SARS-CoV-2–negative individuals, may be interpreted as part of the phenomenon of "reverse epidemiology”; that is, some degrees of hypertension may protect against all-cause mortality.8 On the other hand, asymptomatic SARS-CoV-2–negative residents with a history of close contact had the lowest prevalence of neurologic diseases, dementia, and malnutrition, whereas SARS-CoV-2–positive individuals appeared to be more likely to present such conditions. As already underlined by previous study, our data support the higher risk that individuals with dementia may have in getting SARS-CoV-2 infection.9 Finally, worthy of interest is the high mortality found among SARS-CoV-2–negative symptomatic residents, who were likely to have experienced non–SARS-CoV-2 infections or exacerbations of their chronic conditions. Overall, these findings suggest that attributing death to COVID-19 only based on epidemiologic or clinical criteria, without confirmation by nasopharyngeal swab test, may be misleading and probably contributed to overestimating COVID-19–related mortality in the LTC setting, especially during the first pandemic wave.
Acknowledgments
Angela Marie Abbatecola, MD [RSA INI Città Bianca, Veroli (FR)], Domenico Andrieri, MD [RSA Villa Santo Stefano, S. Stefano di Rogliano (CS)], Francesco Raffaele Addamo, MD [RSA San Giovanni di Dio, Patti (ME)], The GeroCovid LTCFs Working Group members are as follows (in alphabetical order). Rachele Antognoli, MD [RSA Villa Isabella, Pisa], Paola Bianchi, BA [Associazione Nazionale Strutture Territoriali e per la Terza Età, Roma], Carmine Cafariello, MD [RSA Villa Sacra Famiglia, IHG, Roma; I RSA Geriatria, IHG, Guidonia (RM); III RSA Geriatria, IHG, Guidonia (RM); RSA Estensiva, IHG, Guidonia (RM); RSA Intensiva, IHG, Guidonia (RM)], Valeria Calsolaro, MD [RSA Villa Isabella, Pisa], Francesco Antonio Campagna, MD [Centro di Riabilitazione San Domenico, Lamezia Terme (CZ)], Sebastiano Capurso, MD [RSA Bellosguardo, Civitavecchia (RM)], Silvia Carino, MD [RSA San Domenico, Lamezia Terme (CZ); Centro di Riabilitazione San Domenico, Lamezia Terme (CZ); RSA Villa Elisabetta, Cortale (CZ); Casa Protetta Madonna del Rosario, Lamezia Terme (CZ)], Manuela Castelli, MD [ASP Golgi Redaelli, Istituto Geriatrico Camillo Golgi, Abbiategrasso (MI)], Arcangelo Ceretti, MD [ASP Golgi Redaelli, Istituto Geriatrico Camillo Golgi, Abbiategrasso (MI)], Mauro Colombo, MD [ASP Golgi Redaelli, Istituto Geriatrico Camillo Golgi, Abbiategrasso (MI)], Antonella Crispino, MD [RSA Villa Santo Stefano, S. Stefano di Rogliano (CS); RSA Villa Silvia, Altilia Grimaldi (CS)], Roberta Cucunato, MD [RSA Villa Santo Stefano, S. Stefano di Rogliano (CS); RSA Villa Silvia, Altilia Grimaldi (CS)], Ferdinando D'Amico, MD [RSA San Giovanni di Dio, Patti (ME); RSA Sant'Angelo di Brolo (ME)], Annalaura Dell'Armi, MD [III RSA Geriatria, IHG, Guidonia (RM)], Christian Ferro, MD [RSA Sant'Angelo di Brolo (ME)], Serafina Fiorillo, ND [RSA Madonna delle Grazie, Filadelfia (VV); Casa di Riposo Mons. Francesco Luzzi, Acquaro (VV); Casa di Riposo Villa Betania, Mileto (VV); Casa di Riposo Pietro Rosano, Dasà (VV); Casa di Riposo Serena Diocesi, Mileto (VV); Alloggio per Anziani Villa Amedeo, Francavilla Angitola (VV); Casa Albergo Villa Fabiola, Monterosso Calabro (VV); Casa di Riposo Villa Sara, San Nicola da Crissa (VV); Casa di Riposo Don Mottola, Tropea (VV); Casa di Riposo San Francesco, Soriano Calabro (VV); RSA Anziani, Soriano Calabro (VV); Casa di Riposo Suore Missionarie del Catechismo, Pizzo (VV)], Pier Paolo Gasbarri, BS [Associazione Nazionale Strutture Territoriali e per la Terza Età, Roma], Roberta Granata, MD [RSA Villa Sacra Famiglia, IHG, Roma], Nadia Grillo, MD [RSA San Domenico, Lamezia Terme (CZ); Casa di Riposo San Domenico, Lamezia Terme (CZ); RSA Villa Elisabetta, Cortale (CZ)], Antonio Guaita, MD [ASP Golgi Redaelli, Istituto Geriatrico Camillo Golgi, Abbiategrasso (MI)], Marilena Iarrera, MD [RSA Sant'Angelo di Brolo (ME)], Valerio Alex Ippolito, MD [Casa Protetta Villa Azzurra, Roseto Capo Spulico (CS)], Alba Malara, MD [RSA San Domenico, Lamezia Terme (CZ); Casa di Riposo Villa Marinella, Amantea (CS); Casa Protetta Madonna del Rosario, Lamezia Terme (CZ); Casa Protetta Villa Azzurra, Roseto Capo Spulico (CS); Centro di Riabilitazione San Domenico, Lamezia Terme (CZ); RSA Casa Amica, Fossato Serralta (CZ); RSA La Quiete, Castiglione Cosetino (CS); RSA San Domenico, Lamezia Terme (CZ); RSA Villa Elisabetta, Cortale (CZ); RSA Villa Santo Stefano, S. Stefano di Rogliano (CS); RSA Villa Silvia, Altilia Grimaldi (CS)], Irene Mancuso, MD [RSA San Giovanni di Dio, Patti (ME)], Eleonora Marelli, MD [ASP Golgi Redaelli, Istituto Geriatrico Camillo Golgi, Abbiategrasso (MI)], Paolo Moneti, MD [RSA Villa Gisella, Firenze], Fabio Monzani, MD [RSA Villa Isabella, Pisa], Marianna Noale, MSc [RSA AltaVita, Istituzioni Riunite di Assistenza, Padova], Sara Osso, MD [RSA La Quiete, Castiglione Cosentino (CS)], Agostino Perri, MD [RSA La Quiete, Castiglione Cosentino (CS)], Maria Perticone, MD [Casa di Riposo Villa Marinella, Amantea (CS)], Carmine Romaniello , MD [RSA INI Città Bianca, Veroli (FR)]; Marcello Russo, MD [RSA INI Città Bianca, Veroli (FR)], Giovanni Sgrò, MD [RSA Istituto Santa Maria del Soccorso, Serrastretta (CZ); RSA San Vito Hospital, San Vito sullo Jonio (CZ); Casa Protetta Villa Mariolina, Montauro (CZ); Casa Protetta Villa Sant'Elia, Marcellinara (CZ)], Federica Sirianni, MD [Casa di Riposo Villa Marinella, Amantea (CS)], Deborah Spaccaferro, MD [RSA Estensiva, IHG, Guidonia (RM); RSA Intensiva, IHG, Guidonia (RM)], Fausto Spadea, MD [RSA Casa Amica, Fossato Serralta (CZ)], Rita Ursino, MD [I RSA Geriatria, IHG, Guidonia (RM)].
Footnotes
The authors declare no conflicts of interest.
Contributor Information
GeroCovid LTCFs Working Group:
Angela Marie Abbatecola, Francesco Raffaele Addamo, Domenico Andrieri, Rachele Antognoli, Paola Bianchi, Carmine Cafariello, Valeria Calsolaro, Francesco Antonio Campagna, Sebastiano Capurso, Silvia Carino, Manuela Castelli, Arcangelo Ceretti, Mauro Colombo, Antonella Crispino, Roberta Cucunato, Ferdinando D'Amico, Annalaura Dell'Armi, Christian Ferro, Serafina Fiorillo, Pier Paolo Gasbarri, Roberta Granata, Nadia Grillo, Antonio Guaita, Marilena Iarrera, Valerio Alex Ippolito, Alba Malara, Irene Mancuso, Eleonora Marelli, Paolo Moneti, Fabio Monzani, Marianna Noale, Sara Osso, Agostino Perri, Maria Perticone, Carmine Romaniello, Marcello Russo, Giovanni Sgrò, Federica Sirianni, Deborah Spaccaferro, Fausto Spadea, and Rita Ursino
References
- 1.Lombardo F.L., Bacigalupo I., Salvi E., et al. Italian National Institute of Health Nursing Home Study Group The Italian national survey on Coronavirus disease 2019 epidemic spread in nursing homes. Int J Geriatr Psychiatry. 2021;36:873–882. doi: 10.1002/gps.5487. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Abbatecola A.M., Antonelli-Incalzi R. Editorial: COVID-19 spiraling of frailty in older Italian patients. J Nutr Health Aging. 2020;24:453–455. doi: 10.1007/s12603-020-1357-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Bielza R., Sanz J., Zambrana F., et al. Clinical characteristics, frailty, and mortality of residents with COVID-19 in nursing homes of a region of Madrid. J Am Med Dir Assoc. 2021;22:245–252.e2. doi: 10.1016/j.jamda.2020.12.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Arons M.M., Hatfield K.M., Reddy S.C., et al. Presymptomatic SARS-CoV-2 infections and transmission in a skilled nursing facility. N Engl J Med. 2020;382:2081–2090. doi: 10.1056/NEJMoa2008457. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Rutten J.J.S., van Loon A.M., van Kooten J., et al. Clinical suspicion of COVID-19 in nursing home residents: Symptoms and mortality risk factors. J Am Med Dir Assoc. 2020;21:1791–1797.e1. doi: 10.1016/j.jamda.2020.10.034. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Trevisan C., Del Signore S., Fumagalli S., et al. GeroCovid Working Group Assessing the impact of COVID-19 on the health of geriatric patients: The European GeroCovid Observational Study. Eur J Intern Med. 2021;87:29–35. doi: 10.1016/j.ejim.2021.01.017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Tadic M., Cuspidi C., Grassi G., Mancia G. COVID-19 and arterial hypertension: Hypothesis or evidence? J Clin Hypertens (Greenwich) 2020;22:1120–1126. doi: 10.1111/jch.13925. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Ahmadi S.F., Streja E., Zahmatkesh G., et al. Reverse epidemiology of traditional cardiovascular risk factors in the geriatric population. J Am Med Dir Assoc. 2015;16:933–939. doi: 10.1016/j.jamda.2015.07.014. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Rutten J.J.S., van Kooten J., van Loon A.M., et al. Dementia and Parkinson’s disease: Risk factors for 30-day mortality in nursing home residents with COVID-19. J Alzheimers Dis. 2021;84:1173–1181. doi: 10.3233/JAD-210319. [DOI] [PMC free article] [PubMed] [Google Scholar]