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Original Study| Volume 22, ISSUE 2, P245-252.e2, February 2021

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Clinical Characteristics, Frailty, and Mortality of Residents With COVID-19 in Nursing Homes of a Region of Madrid

Published:December 11, 2020DOI:https://doi.org/10.1016/j.jamda.2020.12.003

      Abstract

      Objectives

      To describe the clinical characteristics, 30-day mortality, and associated factors of patients living in nursing homes (NH) with COVID-19, from March 20 to June 1, 2020.

      Design

      This is a retrospective study. A geriatric hospital-based team acted as a consultant and coordinated the care of older people living in NHs from the hospital.

      Setting and Participants

      A total of 630 patients aged 70 and older with Coronavirus Disease 2019 COVID-19 living in 55 NHs.

      Methods

      A logistic regression was performed to analyze the factors associated with mortality. In addition, Kaplan-Meier curves were applied according to mortality and its associated factors using the log-rank Mantel-Cox test.

      Results

      The diagnosis of COVID-19 was mainly made by clinical compatibility (N = 430). Median age was 87 years, 64.6% were women and 45.9% were transferred to be cared for at the hospital. A total of 282 patients died (44.7%) within the 30 days of first attention by the team. A severe form of COVID-19 occurred in 473 patients, and the most frequent symptoms were dyspnea (n = 332) and altered level of consciousness (n = 301). According to multiple logistic regression, male sex (P = .019), the Clinical Frailty Score (CFS) ≥6 (P = .004), dementia (P = .012), dyspnea (P < .001), and having a severe form of COVID-19 (P = .001), were associated with mortality, whereas age and care setting were not.

      Conclusions and Implications

      Mortality of the residents living in NHs with COVID-19 was almost 45%. The altered level of consciousness as an atypical presentation of COVID-19 should be considered in this population. A severe form of the disease, present in more than three-quarters of patients, was associated with mortality, apart from the male sex, CFS ≥6, dementia, and dyspnea, whereas age and care setting were not. These findings may also help to recognize patients in which the Advance Care Planning process is especially urgent to assist in the decisions about their care.

      Keywords

      The World Health Organization (WHO) declared coronavirus disease 2019 (COVID-19) a public health emergency of international concern on March 11, 2020.
      • Huang C.
      • Wang Y.
      • Li X.
      • et al.
      Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.
      • Liu K.
      • Fang Y.Y.
      • Deng Y.
      • et al.
      Clinical characteristics of novel coronavirus cases in tertiary hospitals in Hubei Province.
      • Chen N.
      • Zhou M.
      • Dong X.
      • et al.
      Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: A descriptive study.
      The clinical range of this infectious disease varies from asymptomatic to critical cases,
      • Guan W.
      • Ni Z.
      • Hu Y.
      • et al.
      Clinical characteristics of coronavirus disease 2019 in China.
      ,
      • Liu K.
      • Chen Y.
      • Lin R.
      • Han K.
      Clinical features of COVID-19 in elderly patients: A comparison with young and middle-aged patients.
      the older population being the group with the highest risk of hospitalization and mortality.
      • Zhao H.L.
      • Huang Y.M.
      • Huang Y.
      Mortality in older patients with Covid-19.
      • Sun H.
      • Ning R.
      • Tao Y.
      • et al.
      Risk factors for mortality in 244 older adults with COVID-19 in Wuhan, China: A retrospective study.
      • Bonanad C.
      • García-Blas S.
      • Tarazona-Santabalbina F.
      • et al.
      The effect of age on mortality in patients with COVID-19: A meta-analysis with 611,583 subjects.
      In this regard, the impact of COVID-19 on older people living in nursing homes (NHs) has been particularly serious at national and international scales.
      • Comas-Herrera A.
      • Zalakaín J.
      • Litwin C.
      • et al.
      Mortality associated with COVID-19 outbreaks in care homes: early international evidence. International Long-Term Care Policy Network, CPEC-LSE.
      By June 23, it is estimated that a total of 19,553 people with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) have died in NHs during the COVID-19 pandemic in Spain, representing 68.1% of all confirmed deaths from COVID-19 in our country.
      • Comas-Herrera A.
      • Zalakaín J.
      • Litwin C.
      • et al.
      Mortality associated with COVID-19 outbreaks in care homes: early international evidence. International Long-Term Care Policy Network, CPEC-LSE.
      Living in community, the lack of personal protective equipment for workers or the health vulnerability due to frequent conditions like frailty, dependence, dementia or high burden of comorbidities are some of the factors that have contributed to the expansion and lethality of the virus in this setting.
      • Abrams H.R.
      • Loomer L.
      • Gandhi A.
      • Grabowski D.C.
      Characteristics of U.S. nursing homes with COVID-19 cases.
      With respect to clinical symptoms in older individuals, they also present cough, dyspnea and fever as the most common, whereas delirium, lower temperature, and abdominal pain have been described as atypical presentations as compared with younger patients.
      • Lithander F.E.
      • Neumann S.
      • Tenison E.
      • et al.
      COVID-19 in older people: A rapid clinical review.
      However, data in this particular group of patients living in NHs are still scarce and come from subgroup analysis in observational studies.
      • Wang L.
      • He W.
      • Yu X.
      • et al.
      Coronavirus disease 2019 in elderly patients: Characteristics and prognostic factors based on 4-week follow-up.
      This research aims to describe the clinical characteristics, 30-day mortality, and risk factors for mortality in older patients with COVID-19 living in NHs in the area of influence of a hospital in the region of Madrid during the first wave of the COVID-19 pandemic, from March 20 to June 1, 2020.

      Methods

      Geriatric Hospital-based Team Procedure

      In March 2020, the Health Authorities of Madrid created the position of the geriatric hospital-based team to act as a consultant to the NH physicians and coordinate the care of older people living in these settings from the hospital, covering from 8 am to 10 pm, 7 days a week. In this hospital, a working group was constituted, including 5 geriatricians and 14 other health care workers.
      The geriatric hospital-based team assessed residents at the request of the NH physicians, who provided a first description of the present illness, mainly by telephone. Additional information was obtained from the electronic health record (EHR) used in Madrid for primary and tertiary care integration. The decisions about the management of the patients had to take into account both the characteristics of the NH (whether that center had a qualified doctor, a 24-hour nurse, and the available material, mainly oxygen, drugs, and nursing equipment) and the situation of residents (the comprehensive geriatric assessment and the clinical presentation). If the patient could be adequately attended at the NH, it was recommended that he or she remained there, and if not, they were referred to the hospital. The transmission of information to patients and their relatives was carried out by the staff of the NH.
      After this initial evaluation, the necessary clinical procedures were carried out, that is, request for ambulances, the delivery of oxygen and hospital medications, the adjustment of oral treatments in the EHR and, when needed, the mobilization of human resources. The prescription included a treatment regimen for 5 days for each patient with the dosage, schedule, and form of administration: This individual package was delivered from the hospital to the NH and included (1) antibiotics, (2) fluid therapy, (3) enoxaparin, (4) hydroxychloroquine, (5) paracetamol, and (6) inhalers. In addition, frequent supplies of palliative drugs and steroids were also provided to be used when the patient suffered from distress or sepsis according to the WHO recommendation at that time.
      World Health Organization
      Clinical management of severe acute respiratory infection (SARI) when COVID-19 disease is suspected: interim guidance, 13 March 2020.
      The therapeutic protocol for COVID-19 in the NH was agreed with the Department of Infectious Diseases and was in common with that of the hospital. Updates to the protocol were communicated periodically to the NH physicians.
      Any changes in the clinical situation of a resident or members of the staff of the NH were evaluated and the appropriate clinical decisions were taken.

      Population and Type of Study

      The study population consisted of the residents attended by the geriatric hospital-based team of a public university hospital during the period of the COVID-19 pandemic, from March 20 to June 1, 2020. This hospital covers a population of 312,000 inhabitants in the north of Madrid, including 55 NHs with nearly 4200 older residents.
      This is a descriptive, observational, retrospective, and longitudinal study. We included only patients aged 70 and older with COVID-19 attended by the geriatric hospital-based team. We excluded those attended by the team with not enough data in the EHR to obtain a diagnosis of COVID-19.
      The study complied with good clinical practice standards set forth in the Declaration of Helsinki of 1975 and was approved by the relevant institutional review boards: Ethical and Research Committee of the hospital (reference, HULP4178).

      Variables and Data Collection

      Mortality rate within 30 days after the first geriatric hospital-based team attention in patients diagnosed with COVID-19 was our main outcome. The diagnosis of COVID-19 was made based on positive SARS-CoV-2 polymerase chain reaction (PCR), positive serology, or clinical compatibility (at least 1 of the following symptoms at the initial evaluation: fever, arthromyalgia, headache, upper respiratory tract symptoms, dyspnea, epileptic seizures, chest pain, abdominal pain, cough, nausea or vomiting, diarrhea, hemoptysis, ageusia, or anosmia). We categorized a case as severe when any of the following were initially present: temperature >38°, systolic blood pressure <100 mm Hg, heart rate >100 beats per minute, basal saturation less than 90%, respiratory rate >30 per minute, or altered level of consciousness.
      World Health Organization
      Clinical management of severe acute respiratory infection (SARI) when COVID-19 disease is suspected: interim guidance, 13 March 2020.
      ,
      • Wu Z.
      • McGoogan J.M.
      Characteristics of and important lessons from the Coronavirus Disease 2019 (COVID-19) outbreak in China: Summary of a report of 72314 cases from the Chinese Center for Disease Control and Prevention.
      We also recorded age, sex, previous intake of angiotensin-converting enzyme inhibitors or angiotensin receptor blockers and the presence of any of the following comorbidities: hypertension, cirrhosis, diabetes, chronic renal disease, obesity, chronic neurological disease, active smoking, heart failure, chronic inflammatory disease, ischemic heart disease, solid neoplasm, hematological neoplasm, chronic obstructive pulmonary disease (COPD), or sleep apnea syndrome. With respect to the comprehensive geriatric assessment, the previous Barthel Index (BI)
      • Cid-Ruzafa J.
      • Damián-Moreno J.
      Valoración de la discapacidad física: el indice de Barthel.
      and the cognitive status according to the Global Deterioration Scale were collected.
      • Reisberg B.
      • Ferris S.H.
      • De Leon M.J.
      • Crook T.
      The global deterioration scale for assessment of primary degenerative dementia.
      Frailty was assessed through the Rockwood Clinical Frailty Scale (CFS), taking into account the preexisting level of function and mobility, considering the usual cutoff points, from (1) very fit to (9) terminally ill.
      • Ellis H.L.
      • Wan B.
      • Yeung M.
      • et al.
      Complementing chronic frailty assessment at hospital admission with an electronic frailty index (FI-Laboratory) comprising routine blood test results.
      The treatments used were grouped into (1) antibiotics (ie, ceftriaxone 2 g intravenous, azithromycin 500 mg or cefixime 400 mg), (2) fluid therapy, (3) enoxaparin, (4) hydroxychloroquine, and (5) inhalers.
      Finally, we recorded whether the patient was being treated in the hospital or in the NH. If in the hospital, we additionally recorded length of stay and whether the patient was re-admitted within the first 30 days after their first care.

      Statistical Analysis

      Results for continuous and categorical variables are reported as median and interquartile range and number (percentage), respectively. Differences between survivors and nonsurvivors, patients admitted to the hospital and those who were not, and those classified as severe and mild cases were examined using the Mann-Whitney U test and the χ2 test for continuous and categorical variables, respectively. Multiple logistic regression was carried out to assess factors associated with mortality. We explored and found association between the tools that explore functional domains (ie, CFS and BI), through Spearman's rho correlation test, including only the CFS in the multiple logistic regression. Therefore in the model, the mortality was adjusted for age, sex, hospital admission, CFS ≥6, dementia, hypertension, COPD, sleep apnea syndrome, dyspnea, epileptic seizures, abdominal pain, cough, anosmia, and severe case. Finally, Kaplan-Meier curves were made for overall survival and for the main factors associated with mortality, applying a log-rank Mantel-Cox test. The existence of statistical significance was considered when the P value was less than .05. The analysis was performed with IBM SPSS Statistics program version 21.0 (IBM Corp., Armonk, NY).

      Results

      Demographics and Baseline Clinical Characteristics

      Of the 841 patients attended by the geriatric hospital-based team, 630 presented COVID-19 and complied with the criteria for inclusion in the study. Most of the diagnoses were based on clinical compatibility (n = 430) with the disease (Figure 1). The median age was 87 years (82.9–91.1) and 407 were women (64.6%). As shown in Table 1, the median of comorbidities per patient was 2 (1–3) and the most frequent were hypertension (n = 408, 64.8%), chronic neurological disease (n = 67, 10.6%), diabetes (n = 110, 17.5%), heart failure (n = 69, 11%), chronic renal disease (n = 67, 10.6%), and ischemic heart disease (n = 64, 10.2%). The most frequent symptoms at presentation were dyspnea (n = 332, 52.7%), altered level of consciousness (n = 301, 47.8%), fever (n = 243, 38.6%), and cough (n = 101, 16.3%). Regarding the treatment regimen, 354 patients (56.9%) received antibiotics, 296 fluid therapy (47%), 466 inhalers (74%), 502 enoxaparin (79.7%), and 91 hydroxychloroquine (14.4%).
      Table 1Baseline Characteristics of Study Participants and Characteristics of the Population According to Survival Status
      VariableTotal (N = 630)Alive (n = 348)Dead (n = 282)P Value
      Age, y87 (82.9–91.1)87 (82.5–91.5)87 (82.5–91.5).433
      Age by groups, y
       70–7549 (7.8)30 (8.6)19 (6.7).696
       76–8066 (10.5)39 (11.2)27 (9.6)
       81–85120 (19)68 (19.5)52 (18.4)
       86–90207 (32.9)114 (32.8)93 (33.0)
       >90188 (29.8)97 (27.9)91 (32.3)
      Sex
       Female407 (64.6)240 (69.0)167 (59.2).011
       Male223 (35.4)108 (31.0)115 (40.8)
      Comprehensive geriatric assessment
       Clinical Frailty Scale7 (6–8)7 (5.5–8.0)7 (6–8)<.001
       Barthel Index36 (7–65)40.5 (10–71)30 (4.5–55.5)<.001
       Dementia311 (49.4)148 (42.5)163 (57.8)<.001
      Global Deterioration Scale6 (5–7)6 (5–7)6 (5–7).665
       Comorbidities per patient2 (1–3)2 (1.5–2.5)2 (1–3).749
       Most frequent comorbidities
      Hypertension408 (64.8)222 (63.8)186 (66.0).572
      Cirrhosis3 (0.5)1 (0.3)2 (0.7).589
      Diabetes110 (17.5)57 (16.4)53 (18.8).427
      Chronic renal disease67 (10.6)32 (9.2)35 (12.4).193
      Obesity36 (5.7)15 (4.3)21 (7.4).092
      Chronic neurological disease153 (24.3)83 (23.9)70 (24.8).777
      Active smoking14 (2.2)8 (2.3)6 (2.1).885
      Heart failure69 (11)37 (10.6)32 (11.3).775
      Chronic inflammatory disease19 (3)11 (3.2)8 (2.8).813
      Ischemic heart disease64 (10.2)36 (10.3)28 (9.9).864
      Solid neoplasm58 (9.2)38 (10.9)20 (7.1).098
      Hematological neoplasm8 (1.3)2 (0.6)6 (2.1).149
      COPD67 (10.6)43 (12.4)24 (8.5).119
      Sleep apnea syndrome16 (2.5)8 (2.3)9 (3.2).492
      ACE inhibitors or ARBs105 (16.6)60 (17.2)45 (16.0).667
      Symptoms
       Fever243 (38.6)107 (30.7)133 (47.2)<.001
       Arthromyalgia4 (0.6)1 (0.3)3 (1.1).330
       Headache1 (0.2)2 (0.6)1 (0.4).999
       Symptoms of upper respiratory tract12 (1.9)5 (1.4)7 (2.5).340
       Dyspnea332 (52.7)140 (40.2)192 (68.1)<.001
       Epileptic seizures7 (1.1)5 (1.4)2 (0.7).469
       Chest pain4 (0.6)4 (1.1)0 (0.0).132
       Abdominal pain7 (1.1)3 (0.9)4 (1.4).706
       Cough101 (16.3)49 (14.1)52 (18.4).138
       Vomiting18 (2.9)16 (4.6)2 (0.7).004
       Diarrhea18 (2.9)14 (4.0)4 (1.4).051
       Hemoptysis0 (0.0)0 (0.0)0 (0.0)NA
       Ageusia0 (0.0)0 (0.0)0 (0.0)NA
       Anosmia2 (0.3)1 (0.3)1 (0.4).999
       Alteration of the level of consciousness301 (47.8)148 (42.5)153 (54.3).003
      Vital signs
       Temperature (° Celsius)37.4 (36–38.8)37.2 (36.5–37.9)37.7 (37.1–38.3)<.001
       Systolic blood pressure (mm Hg)115 (89–141)120 (110–130)110 (97–123)<.001
       Heart rate (beats per minute)85 (62–108)84 (76–92)87 (73–101).016
       Basal saturation (%)90 (81–99)92 (88–96)88 (84–92)<.001
       Respiration rate (breaths per min)24 (14–34)21.5 (18.5–24.5)27 (23–31)<.001
      Severe case
      Severe case if any of the following were present: temperature >38°, systolic blood pressure <100 mm Hg, heart rate >100 beats per minute, basal saturation less than 90%, respiratory rate >30 per minute, altered level of consciousness.
      473 (75.08)227 (65.2)246 (87.2)<.001
      Treatment regimens
       Antibiotic354 (56.9)194 (55.7)160 (56.7).803
       Fluidotherapy296 (47.0)149 (42.8)147 (52.1).020
       Hydroxychloroquine91 (14.4)48 (13.8)33 (11.7).436
       Enoxaparin502 (79.7)299 (85.9)203 (72.0)<.001
       Inhalers466 (74.0)231 (66.4)235 (83.3)<.001
      Location of attention
       Nursing home338 (53.6)183 (52.6)158 (56.0).389
       Hospital292 (46.3)165 (47.4)124 (44.0)
      ACE, angiotensin-converting enzyme; ARB, angiotensin receptor blocker; COPD, chronic obstructive pulmonary disease.
      Results are expressed as n (%) or median (Q1–Q3).
      Severe case if any of the following were present: temperature >38°, systolic blood pressure <100 mm Hg, heart rate >100 beats per minute, basal saturation less than 90%, respiratory rate >30 per minute, altered level of consciousness.

      Characteristics of the Population According to the Location of Attention

      A total of 289 patients (45.9%) were transferred and treated at the hospital, and 341 (54.1%) remained in the NH. Table 2 shows that in the NH, the disease was less often diagnosed by PCR than in the hospital (13.5 vs 48.8, percentage). Patients attended at the NH were significantly older (88 vs 87, median age), frailer (CFS 7 vs CFS 6, median), presented a lower BI (30 vs 45, median), more frequently had dementia (57.8 vs 39.4, percentage), and presented fewer comorbidities (1 vs 2, median). However, there was no difference in the severity of the cases (74.2 vs 76.1, percentage), or in the mortality (Supplementary Figure 1) of patients attended in either setting (46.3 vs 42.9, percentage).
      Table 2Characteristics of the Population According to the Location of Attention
      VariableNursing Home (n = 341)Hospital (n = 289)P Value
      Aged, y88 (83.5–92.5)87 (82.0–92.0).012
      Aged by groups, y
       70–7521 (6.2)28 (9.7).255
       76–8031 (9.1)35 (12.1)
       81–8564 (18.8)56 (19.4)
       86–90116 (34.0)91 (31.5)
       >90109 (32.0)79 (27.3)
      Sex
       Female227 (66.6)180 (62.3).262
       Male114 (33.4)109 (37.7)
      Diagnosis of COVID-19
       PCR-confirmed infection for SARS-CoV-246 (13.5)141 (48.8)<.001
       Positive serology for COVID-193 (0.9)10 (3.5).023
       Symptoms compatible with COVID-19292 (85.6)138 (47.8)<.001
      Negative/Undetermined or inhibited PCR3 (0.9)109 (37.7)<.001
      No extraction of PCR289 (84.8)29 (10.0)<.001
      Comprehensive geriatric assessment
       Clinical Frailty Scale7 (6–8)6 (5–7)<.001
       Barthel Index30 (5–55)45 (20–70)<.001
       Dementia197 (57.8)114 (39.4)<.001
      Global Deterioration Scale6 (5.3–6.7)5 (4–6).048
       Comorbidities per patient1 (0.5–1.5)2 (1–3)<.001
       Most frequent comorbidities
      Hypertension206 (60.4)202 (69.9).013
      Cirrhosis1 (0.3)2 (0.7).596
      Diabetes52 (15.2)58 (20.1).112
      Chronic renal disease30 (8.8)37 (12.8).104
      Obesity20 (5.9)16 (5.5).859
      Chronic neurological disease76 (22.3)77 (26.6).204
      Active smoking5 (1.5)9 (3.1).162
      Heart failure34 (10.0)35 (12.1).391
      Chronic inflammatory disease6 (1.8)13 (4.5).045
      Ischemic heart disease32 (9.4)32 (11.1).485
      Solid neoplasm30 (8.8)28 (9.7).700
      Hematological neoplasm4 (1.2)4 (1.4).999
      COPD25 (7.3)42 (14.5).003
      Sleep apnea syndrome7 (2.1)10 (3.5).277
      ACE inhibitors or ARBs49 (14.4)56 (19.4).093
      Symptoms
       Fever147 (43.1)93 (32.2).005
       Arthromyalgia2 (0.6)2 (0.7).999
       Headache3 (0.9)0 (0.0).254
       Symptoms of upper respiratory tract10 (2.9)2 (0.7).040
       Dyspnea186 (54.5)146 (50.5).313
       Epileptic seizures4 (1.2)3 (1.0).999
       Chest pain3 (0.9)1 (0.3).629
       Abdominal pain1 (0.3)6 (2.1).052
       Cough67 (19.6)34 (11.8).007
       Vomiting8 (2.3)10 (3.5).403
       Diarrhea11 (3.2)7 (2.4).546
       Anosmia2 (0.6)0 (0.0).503
      Severe case
      Severe case if any of the following were present: temperature >38°, systolic blood pressure <100 mm Hg, heart rate >100 beats per minute, basal saturation less than 90%, respiratory rate >30 breaths per minute, altered level of consciousness.
      253 (74.2)220 (76.1).577
      Treatment regimens
       Antibiotic199 (58.4)155 (53.6).234
       Fluidotherapy168 (49.3)128 (44.3).212
       Hydroxychloroquine11 (3.2)70 (24.2)<.001
       Enoxaparin256 (75.1)246 (85.1).002
       Inhalers259 (76.0)207 (71.6).217
      Mortality at 30 d158 (46.3)124 (42.9).389
      Place of death
       Hospital0 (0.0)124 (42.9)<.001
       Nursing home158 (46.3)0 (0.0)
      ACE, angiotensin-converting enzyme; ARB, angiotensin receptor blocker; COPD, chronic obstructive pulmonary disease; COVID-19, Coronavirus Disease 2019; PCR, polymerase chain reaction; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2.
      Results are expressed as n (%) or median (Q1–Q3).
      Severe case if any of the following were present: temperature >38°, systolic blood pressure <100 mm Hg, heart rate >100 beats per minute, basal saturation less than 90%, respiratory rate >30 breaths per minute, altered level of consciousness.

      Characteristics of the Population According to the Severity of COVID-19

      We identified 473 patients (75.08%) presenting with a severe form of the disease. In these cases, dementia was significantly more frequent (52.2 vs 40.8, percentage), whereas there were no differences in age, sex, and BI. Fever (43.1 vs 22.9, percentage) and dyspnea (65.1 vs 15.3, percentage), were more frequent in severe forms. Regarding the treatment regimen, antibiotic (66.6 vs 24.8, percentage), inhalers (90.3 vs 24.8, percentage), fluidotherapy (61.1 vs 5.1, percentage) and hydroxychloroquine (15.6 vs 4.5, percentage) were prescribed more in these cases. Finally, mortality (58.6% vs 30.6%) was significantly higher in the severe forms of the disease (Supplementary Table 1).

      Characteristics of the Population According to Survival Status and Factors Associated With Mortality

      Within 30 days of the first care, 282 patients (44.76%) died, as presented in Table 1. Compared with COVID-19 survivors, nonsurvivors showed a lower BI (30 vs 40.5, median), more frequently presented dementia (57.8% vs 42.5%), and were significantly frailer (CFS 7 [6–8] vs CFS 7 [5.5–8.0]) (Supplementary Figure 2). There were no differences in any of the comorbidities between the groups. Nonsurvivors showed a higher temperature (37.7° vs 37.2°, median), higher respiratory rate (27 vs 21.5, median), and higher heart rate per minute (87 vs 84, median). Moreover, basal saturation (88% vs 92%, median) and systolic blood pressure were lower (110 mm Hg vs 120 mm Hg, median) in nonsurvivors. As expected, severe cases (87.2% vs 65.2%) were more frequent in nonsurvivors. However, there were no statistically significant differences in the mortality of patients attended at the NH or in the hospital.
      A Spearman correlation between BI and CFS scales was established with an r = −0.974, and therefore we just include CFS in the logistic regression analyses as a measurement of functional status of the patient. According to logistic regression analyses (Figure 2), male sex, dementia, dyspnea, presenting a severe form of the illness, and the CFS ≥6 were factors significantly associated with mortality. No multiplicative interactions were found between CFS, dyspnea and severe case. In Figure 3, survival curves according to overall survival and Kaplan-Meier curves were made with the main factors associated with mortality applying a log-rank Mantel-Cox test.
      Figure thumbnail gr2
      Fig. 2Multiple logistic regressions analyzing the factors associated with mortality.
      Figure thumbnail gr3
      Fig. 3Survival curves. (A) Kaplan-Meier curves for overall survival. (B) Kaplan-Meier curves according to presence of dyspnea vs non-dyspnea. Log-rank Mantel-Cox test. (C) Kaplan-Meier curves according to severity of the case. Log-rank Mantel-Cox test. (D) Kaplan-Meier curves according to sex. Log-rank Mantel-Cox test. (E) Kaplan-Meier curves according to presence of dementia vs nondementia. Log-rank Mantel-Cox test. (F) Kaplan-Meier curves according to CFS. Log-rank Mantel-Cox test.

      Discussion

      To our knowledge, this is the first study that provides information about clinical characteristics and outcome of older residents of NHs with COVID-19 attended by a geriatric hospital-based team. Disappointingly, almost 45% of the patients died within 30 days of the first attendance. Fever, dyspnea, cough, and altered level of consciousness were the most frequent symptoms at presentation. Approximately three-quarters of the residents showed a severe form of COVID-19. Male sex, CFS score ≥6, dementia, dyspnea, and having a severe clinical form of COVID-19 were factors associated with mortality, whereas the age and the setting in which the resident was treated had no impact on mortality.
      The high number of deaths in the NH have been a critical piece of the worldwide pandemic numbers, with 19% to 72% of COVID-19 deaths occurring in these settings.
      • Comas-Herrera A.
      • Zalakaín J.
      • Litwin C.
      • et al.
      Mortality associated with COVID-19 outbreaks in care homes: early international evidence. International Long-Term Care Policy Network, CPEC-LSE.
      ,
      • Lau-Ng R.
      • Caruso L.B.
      • Perls T.T.
      COVID-19 deaths in long-term care facilities: A critical piece of the pandemic puzzle.
      Particularly in Madrid, from March 8 to April 19, 2020, 19% of older patients (n = ∼8300 cases) living in these facilities died, a sixfold increase compared with the same period in previous years.
      • Martinez-Peromingo J.
      • Serra-Rexach J.A.
      Long-term care facilities and the COVID-19 pandemic: Lessons learned in Madrid.
      The high mortality we reported in our study (44.76%) is consistent with previous publications on hospitalized patients with COVID-19 aged 80 and older.
      • Zhao H.L.
      • Huang Y.M.
      • Huang Y.
      Mortality in older patients with Covid-19.
      ,
      • Richardson S.
      • Hirsch J.S.
      • Narasimhan M.
      • et al.
      Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized with COVID-19 in the New York City Area.
      ,
      • Borobia A.M.
      • Carcas A.J.
      • Arnalich F.
      • et al.
      A cohort of patients with COVID-19 in a major teaching hospital in Europe. J Clin Med.
      However, it contrasts with the 22.4% shown in a coordinated on-site medicalization program conducted in 4 care homes of Seville with 272 residents, where only 23.5% of patients were hospitalized, suggesting that the population did not present forms of COVID-19 as severe as ours.
      • Bernabeu-Wittel M.
      • Ternero-Vega J.E.
      • Díaz-Jiménez P.
      • et al.
      Death risk stratification in elderly patients with covid-19. A comparative cohort study in nursing homes outbreaks.
      Moreover, according to preliminary results, approximately 60% of the older population living in care facilities in Madrid have humoral immunity to SARS-CoV-2, implying that approximately 2500 residents in our area of influence would have been affected by COVID-19.
      Comunidad de Madrid
      Consejería de Servicios Sociales.
      These data suggest that we may have attended more severe cases and, therefore, with worse prognosis.
      According to recent studies, and in line with our findings, delirium has been described as a clinical manifestation in older patients with COVID-19.
      • Lithander F.E.
      • Neumann S.
      • Tenison E.
      • et al.
      COVID-19 in older people: A rapid clinical review.
      ,
      • Poloni T.E.
      • Carlos A.F.
      • Cairati M.
      • et al.
      Prevalence and prognostic value of delirium as the initial presentation of COVID-19 in the elderly with dementia: An Italian retrospective study.
      In this regard, we did not evaluate the other items of the Confusion Assessment Method (ie, acute and fluctuating course, inattention, or disorganized thinking); however, we suspect that the incidence of delirium was high due to the large number of patients presenting altered level of consciousness and the prevalence of dementia in our sample. These data also reveal the importance of identifying atypical presentations of this disease in the older population.
      • Norman R.E.
      • Stall N.M.
      • Sinha S.K.
      Typically atypical: COVID-19 presenting as a fall in an older adult.
      According to the literature and in consonance with our results, frailty or dementia are factors associated with mortality more than age or comorbidities in older patients with COVID-19.
      • Lithander F.E.
      • Neumann S.
      • Tenison E.
      • et al.
      COVID-19 in older people: A rapid clinical review.
      ,
      • De Smet R.
      • Mellaerts B.
      • Vandewinckele H.
      • et al.
      Frailty and mortality in hospitalized older adults with COVID-19: Retrospective observational study.
      ,
      • Hewitt J.
      • Carter B.
      • Vilches-Moraga A.
      • et al.
      The effect of frailty on survival in patients with COVID-19 (COPE): A multicentre, European, observational cohort study.
      These are very common conditions in older residents in NHs, typically leading to frequent visits to emergency departments and admissions to hospital in a nonpandemic.
      • Renom-Guiteras A.
      • Uhrenfeldt L.
      • Meyer G.
      • Mann E.
      Assessment tools for determining appropriateness of admission to acute care of persons transferred from long-term care facilities: A systematic review.
      Several issues regarding how to better care for this population have become even more compelling during the pandemic, many related to adequately identifying which patients benefit from hospitalization. The risk/benefit of hospitalizations of older residents living in NHs, the medicalization of these facilities, and the screening tools for an adequate referral to the hospital are unresolved issues of paramount importance during the COVID-19 pandemic.
      • Farrell T.W.
      • Francis L.
      • Brown T.
      • et al.
      Rationing limited healthcare resources in the COVID-19 era and beyond: Ethical considerations regarding older adults.
      The similar mortality observed in residents treated with the same therapeutic protocol for SARS-CoV-2 in both settings suggests that the comprehensive and tailored intervention by the geriatric hospital-based team were appropriate. However, advance care planning was absent in most of the residents evaluated, a tool that should be included to improve the care and decision-making process.
      • Gordon A.L.
      • Goodman C.
      • Achterberg W.
      • et al.
      Commentary: COVID in care homes-challenges and dilemmas in healthcare delivery.
      In addition to being retrospective, our study is limited by the fact that the disclosure of the SARS-CoV-2 protocol in care facilities allowed the NH physicians to manage mild cases that are not included in our registry. Of note, the availability of a stock of palliative medicines and corticoids did not allow monitoring the end-of-life scenario in the NH, whose adequate management is essential in this lethal disease and in some cases may alter outcomes.
      • Mitchell S.
      • Maynard V.
      • Lyons V.
      • et al.
      The role and response of primary healthcare services in the delivery of palliative care in epidemics and pandemics: A rapid review to inform practice and service delivery during the COVID-19 pandemic.

      Conclusions and Implications

      Almost 45% of the older patients with COVID-19 living in NHs died within 30 days of the first contact with the geriatric hospital-based team. Apart from the classical symptoms, altered level of consciousness is an atypical presentation of COVID-19 and should be taken into account for its diagnosis. Approximately three-quarters of the residents showed a severe form of COVID-19 that was associated with higher mortality. Sex, CFS score ≥6, dementia, and dyspnea were factors that contributed to increased mortality, whereas the age and whether the patient was treated in the hospital or in the NH had no impact on mortality. These findings may also help to recognize patients in which the advance care planning process is especially urgent to assist in the decisions about their care.

      Acknowledgments

      We thank all the staff of the Pharmacy, Palliative Care, Urology, General Surgery, Ophthalmology, Neurology, Orthopedics, Endocrinology, Dermatology, and Rehabilitation departments who participated in the geriatric hospital team. The authors also express their acknowledgment to Manuel Freire and the Admission Department of the Infanta Sofía University Hospital for the collection of the hospital discharge reports, and to the Department of Internal Medicine and Infectious Diseases for the design of the therapeutic protocols of COVID-19, to Cristina García for providing the results of the PCR-SARS-CoV-2 test of the sample, to José Manuel Bautista for making the laboratory of the Complutense University of Madrid available to the nursing homes for the performance of the PCR test, to Belén Ubach and Gonzalo Serralta for collaborating in the design of the assistance protocol, and to Álvaro Leal for the data collection work. Finally, we thank all the staff working in the nursing homes for their hard daily work with the elderly patients during the pandemic period.

      Supplementary Data

      Supplementary Table 1Characteristics of the Population According to the Severity of the Clinical Presentation of COVID-19
      VariableNonsevere (n = 157)Severe Case
      Severe case if any of the following were present: temperature >38°, systolic blood pressure <100 mm Hg, heart rate >100 beats per minute, basal saturation less than 90%, respiratory rate >30 per minute, altered level of consciousness.
      (n = 473)
      P Value
      Age, y88 (83.5–92.5)87 (82.8–91.2).344
      Age by groups, y
       70–7510 (6.4)39 (8.2).425
       76–8012 (7.6)54 (11.4)
       81–8536 (22.9)84 (17.8)
       86–9053 (33.8)154 (32.6)
       >9046 (29.3)142 (30.0)
      Sex
       Male52 (33.1)171 (36.2).491
       Female105 (66.9)302 (63.8)
      Comprehensive geriatric assessment
       Clinical Frailty Scale6 (4.5–7.5)7 (6–8).037
       Barthel Index45 (13–77)35 (8–62).077
       Dementia64 (40.8)247 (52.2).013
      Global Deterioration Scale6 (5–7)6 (5–7).773
       Comorbidities per patient2 (1–3)1 (0.25–1.75).044
       Most frequent comorbidities
      Hypertension108 (68.8)300 (63.4).223
      Cirrhosis1 (0.6)2 (0.4).999
      Diabetes31 (19.7)79 (16.7).384
      Chronic renal disease17 (10.8)50 (10.6).928
      Obesity10 (6.4)26 (5.5).683
      Chronic neurological disease39 (24.8)114 (24.1).852
      Active smoking4 (2.5)10 (2.1).757
      Heart failure24 (15.3)45 (9.5).045
      Chronic inflammatory disease5 (3.2)14 (3.0).999
      Ischemic heart disease17 (10.8)47 (9.9).749
      Solid neoplasm16 (10.2)42 (8.9).622
      Hematological neoplasm1 (0.6)7 (1.5).687
      COPD16 (10.2)51 (10.8).835
      Sleep apnea syndrome3 (1.9)14 (3.0).583
      ACE inhibitors or ARBs27 (17.2)78 (16.5).837
      Symptoms
       Fever36 (22.9)204 (43.1)<.001
       Arthromyalgia1 (0.6)3 (0.6).999
       Headache0 (0.0)3 (0.6).999
       Symptoms of upper respiratory tract3 (1.9)9 (1.9).999
       Dyspnea24 (15.3)308 (65.1)<.001
       Epileptic seizures3 (1.9)4 (0.8).374
       Chest pain2 (1.3)2 (0.4).260
       Abdominal pain2 (1.3)5 (1.1).999
       Cough25 (15.9)76 (16.1).966
       Vomiting5 (3.2)13 (2.7).784
       Diarrhea7 (4.5)11 (2.3).172
       Anosmia0 (0.0)2 (0.4).999
      Treatment regimens
       Antibiotic39 (24.8)315 (66.6)<.001
       Fluidotherapy8 (5.1)289 (61.1)<.001
       Hydroxychloroquine7 (4.5)74 (15.6)<.001
       Enoxaparin118 (75.2)384 (81.2).104
       Inhalers39 (24.8)427 (90.3)<.001
      Location of attention
       Nursing home88 (56.1)253 (53.5).577
       Hospital69 (43.9)220 (46.5)
      Mortality at 30 d36 (22.9)246 (52.0)<.001
      ACE, angiotensin-converting enzyme; ARB, angiotensin receptor blocker; COPD, chronic obstructive pulmonary disease; COVID-19, Coronavirus Disease 2019.
      Results are expressed as n (%) or median (Q1-Q3).
      Severe case if any of the following were present: temperature >38°, systolic blood pressure <100 mm Hg, heart rate >100 beats per minute, basal saturation less than 90%, respiratory rate >30 per minute, altered level of consciousness.
      Figure thumbnail fx1
      Supplementary Fig. 1Kaplan-Meier curves according to location of attention.
      Figure thumbnail fx2
      Supplementary Fig. 2CFS. (A) CFS and severity. (B) CFS and mortality.

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