Open Access

Risk factors for the in‑hospital and 1‑year mortality of elderly patients hospitalized due to COVID‑19‑related pneumonia

  • Authors:
    • Vasiliki Epameinondas Georgakopoulou
    • Aikaterini Gkoufa
    • Sotiria Makrodimitri
    • Aristeidis Tsakanikas
    • Dimitrios Basoulis
    • Pantazis M. Voutsinas
    • Georgios Karamanakos
    • Irene Eliadi
    • Stamatia Samara
    • Maria Triantafyllou
    • Ioanna Eleftheriadou
    • Olga Kampouropoulou
    • Chrysovalantis V. Papageorgiou
    • Amalia Anastasopoulou
    • Petros Papalexis
    • Ilias Trakas
    • Nikolaos Trakas
    • Demetrios A. Spandidos
    • Paschalis Steiropoulos
    • Nikolaos V. Sipsas
  • View Affiliations

  • Published online on: November 20, 2023     https://doi.org/10.3892/etm.2023.12310
  • Article Number: 22
  • Copyright: © Georgakopoulou et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Coronavirus disease 2019 (COVID‑19) is characterized by poor outcomes and a high mortality rate, particularly among elderly patients. Since the beginning of the pandemic, an older age has been recognized as a critical risk factor for disease severity, with increasing mortality rates in each decade of life. This phenomenon may be a consequence of a poor previous health status, with a higher prevalence of pre‑existing comorbidities and a higher degree of frailty. The majority of studies on the outcomes and risk factors of elderly patients refer to the first waves of the pandemic and the predictors of in‑hospital mortality in these patients. The aim of the present study was to provide a detailed description of the clinical characteristics and management of a cohort of elderly patients (≥65 years of age) who were hospitalized with COVID‑19‑related pneumonia in all phases of the pandemic, presenting their outcomes, and investigating predictors of in‑hospital and out‑of‑hospital mortality over a period of 1 year in this particularly vulnerable population. A total of 1,124 elderly patients (603 males, 53.7%) with a mean age of 78.51±7.42 years and a median Charlson comorbidity index (CCI) of 5 were included in the study. Of these patients, 104 (9.3%) were hospitalized during the period of prevalence of the original strain Wuhan, 385 (34.3%) were hospitalized during the period of prevalence of the Alpha variant, 221 (19.7%) were hospitalized during the period of prevalence of the Delta variant, and 414 (36.8%) were hospitalized during the period of prevalence of the Omicron variant. Overall, the in‑hospital mortality rate was 33.4% (375 patients), and the 1‑year mortality rate was 44.7% (502 patients). The majority of patients had not been vaccinated or had not completed full vaccination against severe acute respiratory syndrome coronavirus‑2 (843 patients, 75%), given the period of infection. Age, immature granulocytes, lactate dehydrogenase (LDH) levels, ferritin levels, chest X‑ray score, as well as the absence of full vaccination, cough and fatigue, were statistically significantly and independently associated with in‑hospital mortality, while age, LDH levels, ferritin levels, alanine aminotransferase levels, CCI, chest X‑ray score, the absence of cough and fatigue, and a history of dementia were statistically significantly and independently associated with 1‑year mortality. On the whole, the present study demonstrates that both the in‑hospital mortality and 1‑year mortality rates of elderly patients hospitalized due to COVID‑19‑related pneumonia are high.

Introduction

On March 11, 2020, the World Health Organization (WHO) characterized the coronavirus disease 2019 (COVID-19), an infection caused by severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), as a pandemic (1). As of May 24, 2023, 766,895,075 confirmed cases of COVID-19 and 6,935,889 related deaths were recorded worldwide, according to the WHO (2). With the progress of the vaccination campaign and the succession of SARS-CoV-2 mutations, the proportion of patients with COVID-19 requiring hospitalization and the mortality associated with COVID-19 have markedly changed during the pandemic, and the incidence of confirmed cases and deaths continues to decline worldwide (2).

Patients with COVID-19 present with a wide range of respiratory manifestations, ranging from mild clinical course to severe and potentially life-threatening pneumonia (3). In addition, some patients experience gastrointestinal symptoms, such as vomiting, diarrhea, abdominal pain and nausea in addition to the respiratory symptoms (4,5), as well as cardiovascular and neurological symptoms (6).

Multiple risk factors for severe COVID-19 infection have been identified since the beginning of the pandemic, such as diabetes mellitus, arterial hypertension, cardiovascular disease and malignancies (7). COVID-19 is characterized by poor outcomes and high mortality rates, particularly among elderly patients. Since the beginning of the pandemic, an older age has been recognized as a critical risk factor for disease severity, with increasing mortality rates in each decade of life (8). This phenomenon may be a consequence of a poor previous health status, with a higher prevalence of pre-existing comorbidities and a higher degree of frailty. It is unclear whether the poorer quality of service provided in health care systems collapsed worldwide by the unprecedented pandemic contributes to the observed poor prognosis of the elderly (9).

The majority of studies on the outcomes and risk factors of elderly patients refer to the first waves of the pandemic and predictors of in-hospital mortality in these patients. A previous systematic review of these studies reported that an increasing age, body mass index, male sex, dementia, reduced functionality or dependence for daily activities, the presence of infiltrates on chest X-ray, hypoxemic respiratory failure and a lower saturation of oxygen upon admission were risk factors for mortality due to COVID-19(10). High levels of D-dimers, 25-hydroxyvitamin D deficiency, high levels of C-reactive protein (CRP) plus any other lymphocyte abnormalities, higher blood urea or lactate dehydrogenase (LDH) levels, and higher platelet count (PLTs) have been established as predictors of poor outcomes in the elderly (10). It has been reported that prior treatment with renin-angiotensin-aldosterone system inhibitors, pharmacological treatments for respiratory diseases and other medications, such as antibiotics, corticosteroids, vitamin K antagonists and antihistamines in combination with other antivirals reduces the likelihood of severe COVID-19 infection and mortality. Seasonal influenza vaccination may also reduce mortality from COVID-19, according to that previous systematic review.

As elderly patients represent a vulnerable population even in the era of omicron mutation prevalence and as the infection becomes endemic, data are required to improve healthcare pathways in the context of COVID-19(11). The aim of the present study was to provide a detailed description of the clinical characteristics and management of a cohort of elderly patients (≥65 years of age) who were hospitalized with COVID-19-related pneumonia in all phases of the pandemic, to present their outcomes, and to investigate predictors of in-hospital and 1-year mortality rates in this particularly vulnerable population.

Patients and methods

Study design

For the purposes of the present study, a retrospective recording of data was carried out on consecutive elderly patients aged ≥65 years who were hospitalized with COVID-19-related pneumonia at the Infectious Diseases Unit of Laiko General Hospital during the period October 1, 2020 to July 15, 2022, including patients who were infected from the initial strain and from the Alpha, Delta, and Omicron variants. The study was conducted in line with the Declaration of Helsinki and obtained approval by the Institutional Review Board of Laiko General Hospital, Athens, Greece (protocol no. 7950/08.06.2023). Written informed was obtained from all the included the patients.

Data collection

The demographic characteristics (sex, age), clinical symptoms, the extent of pneumonia on the chest X-ray with the chest X-ray score (12), the vaccination status against SARS-CoV-2, any comorbidities and the Charlson Comorbidity Index (CCI) were recorded. The following admission laboratory findings were also recorded: Hemoglobin (Hb) and hematocrit (Hct) levels; white blood cells (WBC); neutrophils (Neu); lymphocytes (Lym); PLTs and immature granulocytes (IGs); CRP; serum albumin and LDH levels; D-dimer levels; fibrinogen (FIB); creatinine; ferritin; the levels of liver enzymes aspartate aminotransferase (AST) and alanine aminotransferase (ALT); and cholestatic enzymes gamma-glutamyl transferase (GGT) and alkaline phosphatase (ALP). The patients were treated according to the WHO recommendations which represent the standard clinical practice (13) and these treatments received by the patients for the treatment of COVID-19 pneumonia were recorded.

Recording of outcomes

In-hospital mortality rates were recorded, as well as mortality rates within 1 year of admission. Predictors of mortality were also investigated. Patients without a reliable follow-up at 1 year were excluded from the study.

Statistical analysis

Statistical analysis was performed using IBM SPSS-Statistics version 29.0 (IBM Corp.). The Kolmogorov-Smirnov test was used to examine the normal distribution of parameters. Continuous parameters with a normal distribution are shown as the mean (standard deviation), and those with a non-normal distribution are shown as the median (range). For the analysis of categorical variables, the Chi-squared or the Fisher's exact tests were used. To detect predictors of events (event=in-hospital mortality or mortality at 1 year), statistically significant variables were assessed using univariate and multivariate Cox proportional hazards regression analysis. Values of P<0.05 were considered to indicate statistically significant differences.

Results

A total of 1,124 elderly patients (603 males, 53.7%) with a mean age of 78.51±7.42 years and a median CCI of 5 were included in the study. Of these patients, 104 (9.3%) were hospitalized during the period of prevalence of the original Wuhan strain, 385 (34.3%) were hospitalized during the period of prevalence of the Alpha variant, 221 (19.7%) were hospitalized during the period of prevalence of the Delta variant, and 414 (36.8%) were hospitalized during the period of prevalence of the Omicron variant. Overall, the in-hospital mortality rate was 33.4% (375 patients) and the 1-year mortality was 44.7% (502 patients). The majority of patients had not been vaccinated or had not completed full vaccination against SARS-CoV-2 (843 patients, 75%), given the time period of infection. The demographics of the total study population are summarized in Table I.

Table I

Demographics of the study population.

Table I

Demographics of the study population.

ParameterValue
Age (years), mean ± SD78.51±7.42
CCI, median (range)5 (2-8)
Sex, n (%) 
     Females520 (46.3)
     Males604 (53.7)
In-hospital mortality, n (%) 
     No749 (66.6)
     Yes375 (33.4)
1-year mortality, n (%) 
     No622 (55.3)
     Yes502 (44.7)
Variant, n (%) 
     Alpha385 (34.3)
     Delta221 (19.7)
     Omicron414 (36.8)
     Wuhan104 (9.3)
Omicron variant, n (%) 
     No710 (63.2)
     Yes414 (36.8)
Fully vaccinated, n (%) 
     No843(75)
     Yes281(25)
Vaccination doses, n (%) 
     0704 (62.6)
     166 (5.9)
     2162 (14.4)
     3179 (15.9)
     413 (1.2)

[i] CCI, Charlson comorbidity index.

The most common symptom upon admission was fever (755 patients, 67.2%), followed by dyspnea (619 patients, 55.1%) and cough (312 patients, 27.8%) (Table II). The most common comorbidity was arterial hypertension (558 patients, 49.6%), followed by cardiovascular disease, which included stroke, coronary artery disease, valvular diseases, arrhythmias and cardiomyopathy (433 patients, 38.5%), and diabetes mellitus (305 patients, 27.1%) (Table III).

Table II

Symptoms of patients upon admission.

Table II

Symptoms of patients upon admission.

SymptomFrequency (no. of patients)Percentage
Fever  
     No36932.8
     Yes75567.2
Sore throat  
     No1,08696.6
     Yes383.4
Disruptions in smell/taste  
     No1,11098.8
     Yes141.2
Dyspnea  
     No50544.9
     Yes61955.1
Cough  
     No81272.2
     Yes31227.8
Fatigue  
     No99088.1
     Yes13411.9
Gastrointestinal symptoms  
     No1,02491.1
     Yes1008.9
Altered mental status  
     No1,06194.4
     Yes635.6

Table III

Comorbidities of the study population.

Table III

Comorbidities of the study population.

ComorbidityFrequency (no. of patients)Percentage
Lung disease (COPD, asthma, pulmonary fibrosis)  
     No96986.2
     Yes15513.8
Obesity (BMI >30kg/m2)  
     No1,08896.8
     Yes363.2
Diabetes mellitus  
     No81972.9
     Yes30527.1
Arterial hypertension  
     No56650.4
     Yes55849.6
Cardiovascular disease (stroke, coronary artery disease, valvular disease, arrhythmias, cardiomyopathy)  
     No69161.5
     Yes43338.5
Heart failure  
     No1,02391
     Yes1019
Renal disease  
     No1,01990.7
     Yes1059.3
Liver disease  
     No1,10398.1
     Yes211.9
Autoimmune disease  
     No1,05593.9
     Yes696.1
Hematological malignancy  
     No1,06094.3
     Yes645.7
Solid organ malignancy  
     No1,04292.7
     Yes827.3
Solid organ transplantation  
     No1,11298.9
     Yes121.1
Parkinson's disease  
     No1,08996.9
     Yes353.1
Dementia  
     No1,02090.7
     Yes1049.3
Nursing home resident  
     No1,08496.4
     Yes403.6

[i] BMI, body mass index; COPD, chronic obstructive pulmonary disease.

The majority of the patients were treated with anticoagulants, dexamethasone and remdesivir; 83 (7.4%) patients received tocilizumab; 12 (1.1%) patients received baricitinib; and 9 (0.8%) patients received anakinra. In 138 (12.3%) patients, oxygen therapy with a high-flow nasal cannula was applied; in 18 (1.6%) patients, non-invasive mechanical ventilation was applied; and 134 (11.9%) patients were intubated (received invasive mechanical ventilation) (Table IV).

Table IV

Medication that was administrated to the study population during the hospitalization period.

Table IV

Medication that was administrated to the study population during the hospitalization period.

MedicationFrequency (no. of patients)Percentage
Remdesivir  
     No11610.3
     Yes1,00889.7
Dexamethasone  
     No474.2
     Yes1,07795.8
Tocilizumab  
     No1,04192.6
     Yes837.4
Anticoagulants  
     No443.9
     Yes1,08096.1
Anakinra  
     No1,11599.2
     Yes90.8
Baricitinib  
     No1,11298.9
     Yes121.1
High flow nasal cannula  
     No98687.7
     Yes13812.3
Non-invasive ventilation  
     No1,10698.4
     Yes181.6
Invasive mechanical ventilation  
     No99088.1
     Yes13411.9

In total, 3 (0.2%) patients had received prophylactic intravenous remdesivir; 4 (0.4%) patients had received the combination of monoclonal antibodies casirivimab/imdevimab; and 24 (2.1%) patients had received the combination of antiviral agents nirmatrelvir/ritonavir (Table V).

Table V

Prophylactic therapy that patients received for COVID-19 prior to their admission to the hospital.

Table V

Prophylactic therapy that patients received for COVID-19 prior to their admission to the hospital.

TherapyFrequency (no. of patients)Percentage
Remdesivir  
     No1,12199.8
     Yes30.2
Casirivimab/imdevimab  
     No1,11999.6
     Yes50.4
Nirmatrelvir/ritonavir  
     No1,10097.9
     Yes242.1

The univariate analysis of categorical variables for the outcome of in-hospital mortality revealed that patients who succumbed to the disease in the hospital were significantly more likely to be in the Delta variant prevalence period (in-hospital mortality rate: 92/129 patients, 41.6%); these patients also had a statistically higher proportion of cardiovascular disease, heart failure, renal disease and a history of nursing home residency. In addition, the lack of complete vaccination, dyspnea and an altered mental status were significantly associated with the in-hospital mortality rate, and fever, cough, sore throat, disruptions in taste/smell and fatigue were significantly associated with the in-hospital survival rate (P<0.05; Table VI).

Table VI

Univariate analysis for categorical variables (outcome: In-hospital mortality).

Table VI

Univariate analysis for categorical variables (outcome: In-hospital mortality).

 In-hospital mortality 
VariableNoYesP-value
Omicron variant   
     No4682420.513
     Yes281133 
Variant   
     Wuhan66380.014
     Alpha272112 
     Delta12992 
     Omicron281133 
Sex   
     Female3611590.076
     Male388216 
Lung disease   
     No6363330.081
     Yes11342 
Obesity (BMI >30 kg/m2)   
     No7213670.208
     Yes288 
Diabetes mellitus   
     No5452740.943
     Yes204101 
Arterial hypertension   
     No3622040.058
     Yes387171 
Cardiovascular disease   
     No4812100.009
     Yes268165 
Heart failure   
     No6953280.004
     Yes5447 
Renal disease   
     No6923270.006
     Yes5748 
Liver disease   
     No7353680.998
     Yes147 
Autoimmune disease   
     No7043510.793
     Yes4524 
Hematological malignancy   
     No7073530.892
     Yes4222 
Solid organ malignancy   
     No7023400.068
     Yes4735 
Solid organ transplantation   
     No7423700.540
     Yes75 
Parkinson's disease   
     No7313580.067
     Yes1817 
Dementia   
     No6843360.383
     Yes6539 
Nursing home residency   
     No7313530.006
     Yes1822 
Fully vaccinated   
     No5442990.010
     Yes20576 
Vaccination doses   
     04622420.001
     14224 
     29468 
     314039 
     4112 
Fever   
     No2201490.001
     Yes529226 
Sore throat   
     No7173690.022
     Yes326 
Disruptions in smell/taste   
     No7353750.007
     Yes140 
Dyspnea   
     No3661390.001
     Yes383236 
Cough   
     No5043080.001
     Yes24567 
Fatigue   
     No6463440.008
     Yes10331 
Gastrointestinal symptoms   
     No6763480.182
     Yes7327 
Altered mental status   
     No7183430.004
     Yes3132 

[i] P-values in bold font indicate statistically significant differences (P<0.05). BMI, body mass index.

The univariate analysis of continuous variables for the outcome, in-hospital mortality, revealed that the patients who succumbed in hospital had a significantly older age, lower Hb and lower Hct levels, higher CCI, higher WBC, higher Neu count, higher IG count, higher value of D-dimers, higher value of creatinine, higher values of AST, ALP, GGT, LDH, CRP, ferritin and chest X-ray score, and a lower value of Lym count compared to the survivors (P<0.05; Table VII).

Table VII

Univariate analysis for continuous variables (outcome: In-hospital mortality).

Table VII

Univariate analysis for continuous variables (outcome: In-hospital mortality).

VariableIn-hospital mortalityMean/medianStandard deviation/range95% CI for the mean difference Lower95% CI for the mean difference UpperP-value
Age (years)No77.568.23-0.536-0.2860.001
 Yes80.998.54   
Hb (g/dl)No12.572.060.1520.4010.001
 Yes11.962.49   
Hct (%)No37.845.860.1590.4090.001
 Yes36.047.25   
Albumin (g/dl)No38.814.53-0.1821.1430.155
 Yes36.207.02   
CCINo42-11-0.515-0.2650.001
 Yes52-12   
WBC (K/µl)No6.240.40-105.81-0.300-0.0520.001
 Yes7.321.23-43.82   
Neu (K/µl)No4.700.20-97.30-0.376-0.1270.001
 Yes6.100.10-33.09   
Lym (K/µl)No0.990.060-69.19-0.0450.2040.001
 Yes0.770.180-31.21   
IGs (109/l)No0.040.01-21.58-0.2040.0450.001
 Yes0.060.01-5.62   
PLTs (K/µl)No1838-608-0.0520.1960.156
 Yes18411-467   
D-dimers (µg/ml)No1.070.01-35.40-0.417-0.1510.001
 Yes1.740.01-20   
FIB (mg/dl)No521223-1367-0.1970.0580.062
 Yes562256-1133   
Creat (mg/dl)No0.940.30-14.98-0.2250.0240.001
 Yes1.110.29-971   
AST (U/l)No3017-499-0.367-0.1170.002
 Yes368-1222   
ALT (U/l)No2113-433-0.1780.0710.376
 Yes2113-772   
ALP (U/l)No6926-377-0.316-0.0660.010
 Yes7523-1238   
GGT (U/l)No2722-746-0.273-0.0220.001
 Yes344-1060   
LDH (U/l)No295152-1991-0.514-0.2620.001
 Yes349.5101-3091   
CRP (mg/l)No46.080.40-320.76-0.615-0.3630.001
 Yes82.030.68-444.60   
Ferr (ng/ml)No38313-7709-0.546-0.2830.001
 Yes65725.20-33341   
Chest X-ray scoreNo51-6-0.574-0.3210.001
 Yes61-6   

[i] P-values in bold font indicate statistically significant differences (P<0.05). ALP, alkaline phosphatase; ALT, alanine aminotransferase; AST, aspartate aminotransferase; CI, confidence interval; CCI, Charlson comorbidity index; CRP, C-reactive protein; Ferr, ferritin; Creat, creatinine; FIB, fibrinogen; GGT, gamma glutamyl-transferase; Hb, hemoglobin; Hct, hematocrit; IGs, immature granulocytes; LDH, lactate dehydrogenase; Lym, lymphocytes; Neu, neutrophils; PLTs, platelets; WBC, white blood cell.

From the multivariate analysis for the outcome of in-hospital mortality, it emerged that age, IGs, LDH, ferritin, chest X-ray score, as well as the absence of full vaccination, cough and fatigue, were significantly and independently associated with the in-hospital mortality rate (P<0.05; Table VIII).

Table VIII

Multivariate analysis (outcome: In-hospital mortality).

Table VIII

Multivariate analysis (outcome: In-hospital mortality).

VariableP-valueHR95% CI lower95% CI upper
Age per year0.0011.0391.0161.061
CCI0.2321.0800.9521.226
Hb (g/dl)0.7371.0520.7821.415
Hct (%)0.4350.9600.8671.063
WBC (K/µl)0.1740.8540.6811.072
Neu (K/µl)0.0911.2340.9671.575
Lym (K/µl)0.3411.1190.8881.411
IGs (109/l)0.0430.7270.5330.990
D-dimers (µg/ml)0.8340.9950.9501.042
Creat (mg/dl)0.3641.0630.9311.214
AST (U/l)0.9302.0000.9961.003
ALP (U/l)0.4191.0020.9981.005
GGT (U/l)0.4280.9990.9961.002
LDH (U/l)0.0031.0021.0011.003
CRP (mg/l)0.0971.0021.0001.005
Ferr (ng/ml)0.0031.0001.0001.000
Chest X-ray score0.0051.2001.0581.362
Cardiovascular disease0.6291.0920.7631.563
Heart failure0.0561.7280.9853.031
Renal disease0.2401.5140.7583.025
Nursing home resident0.2031.6930.7533.805
Absence of full vaccination0.0031.9721.2573.093
Absence of fever0.5071.1310.7861.630
Absence of sore throat0.3651.7140.5345.500
Absence of smell/taste disruptions0.9993.2070.0424.281
Dyspnea0.3241.1990.8361.720
Absence of cough0.0011.9741.3252.940
Absence of fatigue0.0291.8741.0673.292
Altered mental status0.5401.2310.6332.395
Variant    
     WuhanRefRefRefRef
     Alpha0.2230.7060.4031.237
     Delta0.3621.3520.7072.588
     Omicron0.3290.7420.4071.351

[i] P-values in bold font indicate statistically significant differences (P<0.05). HR, hazard ratio, CI, confidence interval; ALP, alkaline phosphatase; AST, aspartate aminotransferase; CI, confidence interval; CCI, Charlson comorbidity index; Creat, creatinine; CRP, C-reactive protein; Ferr, ferritin; GGT, gamma glutamyl-transferase; Hb, hemoglobin; Hct, hematocrit; IGs, immature granulocytes; LDH, lactate dehydrogenase; Lym, lymphocytes; Neu, neutrophils; WBC, white blood cell; Ref, reference for calculation of the hazard ratio.

The univariate analysis of continuous variables for the outcome of 1-year mortality revealed that patients who succumbed within 1 year were significantly more likely to have been ill in the period of prevalence of the Alpha variant (mortality within 1 year, 52%); these patients also had a significantly greater proportion of arterial hypertension, cardiovascular disease, heart failure, renal disease, dementia, Parkinson's disease, hematological malignancy, solid organ malignancy and a history of nursing home residency. Furthermore, dyspnea and an altered mental status were statistically significantly associated with mortality, and fever, cough, sore throat, disruptions in taste/smell and fatigue were statistically significantly associated with the 1-year survival (P<0.05; Table IX).

Table IX

Univariate analysis for categorical variables (outcome: 1-Year mortality).

Table IX

Univariate analysis for categorical variables (outcome: 1-Year mortality).

 1-year mortality 
VariableNoYesP-value
Omicron variant   
     No4112990.025
     Yes211203 
Variant   
     Wuhan60440.001
     Alpha245140 
     Delta106115 
     Omicron211203 
Sex   
     Female2992210.186
     Male323281 
Lung disease   
     No5324370.487
     Yes9065 
Obesity (BMI >30 kg/m2)   
     No5984900.177
     Yes2412 
Diabetes mellitus   
     No4543650.946
     Yes168137 
Arterial hypertension   
     No2952710.031
     Yes327231 
Cardiovascular disease   
     No4072840.003
     Yes215218 
Heart failure   
     No5804430.004
     Yes4259 
Renal disease   
     No5834360.001
     Yes3966 
Liver disease   
     No6124910.512
     Yes1011 
Autoimmune disease   
     No5814740.533
     Yes4128 
Hematological malignancy   
     No5954650.032
     Yes2737 
Solid organ malignancy   
     No5924500.001
     Yes3052 
Solid organ transplantation   
     No6174950.390
     Yes57 
Parkinson's disease   
     No6114780.005
     Yes1124 
Dementia   
     No5844360.001
     Yes3866 
Nursing home residency   
     No6104740.001
     Yes1228 
Fully vaccinated   
     No4693740.730
     Yes153128 
Vaccination doses   
     04043000.061
     13432 
     27587 
     310475 
     458 
Fever   
     No1642050.001
     Yes458297 
Sore throat   
     No5914950.001
     Yes317 
Disruptions in smell/taste   
     No6095010.005
     Yes131 
Dyspnea   
     No3141910.001
     Yes308311 
Cough   
     No4054070.001
     Yes21795 
Fatigue   
     No5324580.004
     Yes9044 
Gastrointestinal symptoms   
     No5624620.344
     Yes6040 
Altered mental status   
     No6014600.001
     Yes2142 

[i] P-values in bold font indicate statistically significant differences (P<0.05). BMI, body mass index.

The univariate analysis of categorical variables for the outcome of 1-year mortality revealed that patients who succumbed within 1 year had a significantly older age, lower Hb and lower Hct levels, higher CCI, higher WBC value, higher Neu value, higher value of IGs, higher value of D-dimers, higher value of creatinine, higher value of ALP, LDH, CRP, ferritin and chest X-ray score, and a lower value of Lym, ALT and GGT compared to the survivors (P<0.05; Table X).

Table X

Univariate analysis for continuous variables (outcome: 1-year mortality).

Table X

Univariate analysis for continuous variables (outcome: 1-year mortality).

Variable1-Year mortalityMean/medianStandard deviation/range95% CI for the mean difference Lower95% CI for the mean difference UpperP-value
Age (years)No76.687.82-0.674-0.4350.002
 Yes81.228.62   
Hb (g/dl)No12.782.010.3030.5410.001
 Yes11.852.39   
Hct (%)No38.375.670.2830.5210.001
 Yes35.846.98   
Albumin (g/dl)No39.584.520.0671.3270.721
 Yes35.916.04   
CCINo42-7-,0.44-0.5030.001
 Yes63-8   
WBC (K/µl)No6.012.36-11.29-0.383-0.1460.001
 Yes7.853.32-24.52   
Neu (K/µl)No4.701.50-9.70-0.450-0.2130.001
 Yes6.102.1-21.1   
Lym (K/µl)No1.120.58-2.61-0.0190.2170.001
 Yes1.030.33-5.17   
IGs (109/l)No0.040.02-0.13-0.091-0.0550.001
 Yes0.060.01-5.620   
PLTs (K/µl)No163112-416-0.1060.1300.668
 Yes16065-443   
D-dimers (µg/ml)No1.050.29-6.20-0.434-0.1820.001
 Yes1.920.48-6.88   
FIB (mg/dl)No53843-860-0.1030.1380.783
 Yes493308-893   
Creat (mg/dl)No0.960.58-8.55-0.1950.0410.001
 Yes1.200.56-6.57   
AST (U/l)No3115-127-0.273-0.0370.517
 Yes3014-297   
ALT (U/l)No237-65-0.0950.1400.001
 Yes166-36   
ALP (U/l)No6040-102-0.398-0.1590.001
 Yes7125-279   
GGT (U/l)No3512-204-0.313-0.0750.003
 Yes3012-271   
LDH (U/l)No288212-566-0.376-0.1380.001
 Yes307151-966   
CRP (mg/l)No61.831.15-206-0.536-0.2970.001
 Yes940.93-414   
Ferr (ng/ml)No49933-7510-0.461-0.2140.001
 Yes63554.7-33341   
Chest X-ray scoreNo41-6-0.550-0.3100.001
 Yes61-6   

[i] P-values in bold font indicate statistically significant differences (P<0.05). ALP, alkaline phosphatase; ALT, alanine aminotransferase; AST, aspartate aminotransferase; CCI, Charlson comorbidity index; CRP, C-reactive protein; Ferr, ferritin; Creat, creatinine; FIB, fibrinogen; GGT, gamma glutamyl-transferase; Hb, hemoglobin; Hct, hematocrit; IGs, immature granulocytes; LDH, lactate dehydrogenase; Lym, lymphocytes; Neu, neutrophils; PLTs, platelets; WBC, white blood cell.

From the multivariate analysis for the outcome of 1-year mortality, it was found that age, LDH, ferritin, ALT, CCI, chest X-ray score, the absence of cough and fatigue, and a history of dementia were significantly and independently associated with mortality within 1 year (P<0.05; Table XI).

Table XI

Multivariate analysis (outcome: I-year mortality)

Table XI

Multivariate analysis (outcome: I-year mortality)

VariableP-valueHR95% CI lower95% CI upper
Age per year0.0011.0431.0201.066
Variant    
     WuhanRefRefRefRef
     Alpha0.3180.7540.4341.312
     Delta0.8321.0700.5741.995
     Omicron0.8320.9410.5381.647
Absence of fever0.1691.2820.9001.828
Absence of sore throat0.1172.3240.8096.671
Absence of disruptions in smell/taste0.1874.4360.48640.48
Dypsnea0.4481.1430.8101.613
Absence of cough0.0121.6051.1082.327
Absence of fatigue0.0141.9171.1383.228
Altered mental status0.3431.3910.7032.751
CCI0.0021.2641.0861.471
Arterial hypertension0.0960.7630.5541.049
Cardiovascular disease0.5890.9080.6401.288
Heart failure0.4091.2720.7192.251
Renal disease0.8971.0460.5332.052
Solid organ malignancy0.9141.0440.4802.269
Hematological malignancy0.4431.4070.5883.367
Parkinson's disease0.4531.3900.5883.284
Dementia0.0082.0651.2133.513
Nursing home residency0.2351.7140.7044.173
Hb (normal range 13-17 g/dl)0.6960.9430.7031.265
Hct (normal range 38-48%)0.7930.9860.8911.092
WBC (normal range 4.5-11 K/µl)0.2610.8790.7021.101
Neu (normal range 1.5-6.6 K/µl)0.1421.2010.9401.535
Lym (normal range 1.2-3.4 K/µl)0.7501.0380.8261.304
IGs (1 normal range 0-0.4 109/l)0.3541.7780.5266.011
D-dimers (normal <0.5 µg/ml)0.9540.9990.9511.049
Creat (normal range 0.7-1.2 mg/dl)0.1221.1110.9721.269
ALT (normal range <41 U/l)0.0210.9950.9900.999
ALP (normal range 40-129 U/l)0.1661.0030.9991.008
GGT (normal range 8-61 U/l)0.9511.0000.9971.003
LDH (normal range 135-225 U/l)0.0041.0021.0011.003
CRP (normal range 0-5 mg/l)0.1471.0020.9991.005
Ferr (normal range 30-400 ng/ml)0.0291.0001.0001.000
Chest X-ray score0.0011.2091.0791.355

[i] P-values in bold font indicate statistically significant differences (P<0.05). HR, hazard ratio, CI, confidence interval; ALP, alkaline phosphatase; ALT, alanine aminotransferase; CI, confidence interval; CCI, Charlson comorbidity index; Creat, creatinine; CRP, C-reactive protein; Ferr, ferritin; GGT, gamma glutamyl-transferase; Hb, hemoglobin; Hct, hematocrit; IGs, immature granulocytes; LDH, lactate dehydrogenase; Lym, lymphocytes; Neu, neutrophils; WBC, white blood cell; Ref, reference for calculation of the hazard ratio.

As shown in Table I, an additional 127 elderly patients succumbed within 1 year of admission. As regards the causes of death, the majority of patients succumbed due to cardiac events, including acute myocardial infarction, arrhythmia, cardiogenic shock, or pulmonary edema. The second cause of death was septic shock (36 patients, 28.3%); in 13 patients, the cause of death was not specified, while it is noteworthy that 3 patients (2.4%) succumbed due to a new SARS-CoV-2 infection (Table XII).

Table XII

Causes of 1-year mortality.

Table XII

Causes of 1-year mortality.

Cause of 1-year mortalityFrequency (no. of patients)Percentage
Unknown1310.2
Cardiac events4132.3
Septic shock3628.3
Pneumonia-ARDS107.9
End-stage cancer107.9
Ischemic stroke53.9
Pulmonary embolism43.1
Mesenteric ischemia10.8
Gastrointestinal hemorrhage10.8
Hepatic encephalopathy10.8
Acute renal failure10.8
COPD exacerbation10.8
New SARS-CoV-2 infection32.4

[i] ARDS, acute respiratory distress syndrome; COPD, chronic obstructive pulmonary disease; SARS-Cov-2, severe acute respiratory syndrome coronavirus 2.

Discussion

According to the present study, the in-hospital and out-of-hospital mortality of elderly patients with COVID-19 was high. Overall, the in-hospital mortality rate was 33.4% (375 patients), and the 1-year mortality rate was 44.7% (502 patients). As regards in-hospital mortality, the findings of the present study are in agreement with those of previous studies (14-18), reporting on the in-hospital mortality of elderly patients from the first waves of the pandemic. The present study is one of the few studies reporting on in-hospital mortality of elderly patients over a long period of the pandemic, including the period of prevalence of the Omicron variant. It is also the first study, to the best of our knowledge, to present the 1-year mortality for elderly patients who were hospitalized during all periods of the pandemic.

The majority of the patients who succumbed within 1 year did not survive mainly due to cardiac events. It has been documented that after COVID-19, there is an increased risk of cardiovascular events such as arrhythmias, ischemic and non-ischemic heart disease, pericarditis, myocarditis, acute heart failure and thromboembolic events. Mechanisms underlying the association between COVID-19 and the development of cardiac complications include the prolonged damage from direct viral invasion of myocardial cells and cell death, endothelial cell infection and subsequent endothelitis, the activation of the complement and complement-mediated coagulation and microangiopathy, transcriptional alteration of multiple cell types in cardiac tissue, ACE2 downregulation and renin-angiotensin-aldosterone system dysfunction, autonomic nervous system dysfunction, increased levels of pro-inflammatory cytokines, and activation of TGF-β signaling through the Smad pathway leading to fibrosis and scarring of cardiac tissue. In addition, a possible factor explaining cardiac complications is an abnormal, persistent hyperactivated immune response, either autoimmune or in the context of the persistence of the virus in immunologically privileged sites. The integration of their SARS-CoV-2 genome into the DNA of infected human cells, which can then express some transcripts containing viral and cellular human sequences, has also been reported as a putative mechanism for the sustained activation of the immune-inflammatory procoagulant cascade (19,20).

The second cause of death within 1 year was septic shock. No association was observed with the administration of immunosuppressive agents, such as corticosteroids and tocilizumab. It is likely that the emergence of new infections and septic shock after COVID-19 are due to the dysfunction of the immune system combined with the impaired immune response of the elderly following COVID-19 infection (21,22).

Of note, 3 patients succumbed due to a new SARS-CoV-2 infection, and 2 of these patients were hospitalized during the time period of the prevalence of the Omicron variant. Protection against reinfection by the original strain and the Alpha and Delta variants was found to decrease over time, but remained at 78.6% (49.8-93.6) at 40 weeks. Protection against reinfection by the Omicron BA.1 subvariant declined more rapidly and was estimated at 36.1% (24.4-51.3) at 40 weeks. However, protection against severe disease has been reported to remain high for all variants, with 90.2% (69.7-97.5) for the original strain and the Alpha and Delta variants and 88.9% (84.7-90.9) for the Omicron BA.1 subvariant at 40 weeks (23).

In the present study, age, IGs, LDH, ferritin, chest X-ray score and the absence of full vaccination, cough and fatigue were significantly and independently associated with the in-hospital mortality of this older population. The majority of these findings are consistent with those of previous studies of the in-hospital mortality of elderly patients with COVID-19 (14,16,24-27). Among studies in the general population, age has been reported as an independent predictor of mortality within 1 year after COVID-19 (28,29). It has also been reported that in the general population, chronic obstructive pulmonary disease, chronic cardiovascular disease and active malignancy are also independent predictors of 1-year mortality following infection with SARS-CoV-2(29). However, there are no data to date, as mentioned above, on mortality within 1 year for elderly patients, and the present study is the first (at least to the best of our knowledge) to report that age, LDH, ferritin, ALT, CCI, chest X-ray score, the absence of cough and fatigue, and a history of dementia were statistically significantly and independently associated with mortality within 1 year.

Several factors accompanying aging, including the altered expression of the ACE2 receptor, the increased production of reactive oxygen species, the increased activity of senescent adipocytes, altered autophagy and mitophagy, immunosenescence, as well as vitamin D deficiency, may be involved in the pathophysiology of severe disease and poor outcomes in elderly patients with COVID-19(30). Increased IG counts detected in peripheral blood demonstrate an enhanced bone marrow activity and have been linked to poor outcomes in patients with COVID-19(31). Increased LDH levels in the circulation could reflect either the direct SARS-CoV-2 infection of cells or marked tissue damage secondary to an excessive systemic inflammatory response (32). Ferritin is known as an acute phase reactant, and its levels are increased in acute and chronic inflammation; in COVID-19, ferritin has been linked to disease severity (33). Elevated ALT levels have also been associated with poor outcomes of patients with COVID-19, reflecting liver injury (34-36).

It has been reported that initial chest X-ray scores of patients with COVID-19 are linked to clinical outcomes, such as mortality, the length of hospitalization and the duration of invasive ventilation (37). Since the beginning of the pandemic, comorbidities have been known to affect the outcomes of patients with COVID-19. In the three stages of COVID-19, from the initial viral replication phase to the inflammatory tissue injury and long-term consequences, specific comorbidities can either exacerbate these pathological mechanisms that determine health outcomes or lower the patient's tolerance for organ injury (38). One established risk factor for the mortality of patients with COVID-19 is a lack of vaccination (39). Furthermore, vaccination against COVID-19 has been proven to be highly beneficial in reducing hospitalization and mortality among the elderly (40,41).

In addition, cough has been shown to be associated with better outcomes in patients with COVID-19(42). As regards the symptom of fatigue, it has been linked to poor outcomes of patients with COVID-19(43); however, in the present study, it was associated with in-hospital and with 1-year survival.

Dementia is also a well-established risk factor for the poor outcomes of elderly patients hospitalized due to COVID-19 (43,44) and according to the present study, it was an independent risk factor for 1-year mortality.

The present study has certain limitations which should be mentioned. The present study was a single-center study without a control group. In addition, medications that patients were receiving for underlying diseases were not included in the analysis. Finally, SARS-CoV-2 variants were not identified individually for patients. Variant assignment was based on the prevalent variant at the time the patient was diagnosed with the infection, and distinction was made only based on whether patients were diagnosed before or after the appearance of the Omicron variant.

In conclusion, both the in-hospital and 1-year mortality of elderly patients hospitalized due to COVID-19 pneumonia is high. As regards the causes of death, the majority of patients succumbed due to cardiac events. Age, IGs, LDH, ferritin, chest X-ray score, as well as the absence of full vaccination, cough and fatigue were significantly and independently associated with in-hospital mortality, while age, LDH, ferritin, ALT, CCI, chest X-ray score, the absence of cough and fatigue, and a history of dementia were significantly and independently associated with 1-year mortality.

Acknowledgements

Not applicable.

Funding

Funding: No funding was received.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Authors' contributions

NVS and VEG conceptualized the study. VEG, AT, DB, DAS, SM, AG, GK, PMV, IrE, SS, MT, IoE, OK, CVP, AA, IT, NT, PP, PS and NVS made a substantial contribution to data interpretation and analysis and wrote and prepared the draft of the manuscript. PS and NVS analyzed the data and provided critical revisions. VEG and NVS confirm the authenticity of all the data. All authors contributed to manuscript revision, and have read and approved the final version of the manuscript.

Ethics approval and consent to participate

The present study was conducted in line with the Declaration of Helsinki and gained approval by the regional Institutional Review Board (protocol number protocol no. 7950/08.06.2023). Written informed was obtained from all the included patients.

Patient consent for publication

Not applicable.

Competing interests

DAS is the Editor-in-Chief for the journal, but had no personal involvement in the reviewing process, or any influence in terms of adjudicating on the final decision, for this article. The other authors declare that they have no competing interests.

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January-2024
Volume 27 Issue 1

Print ISSN: 1792-0981
Online ISSN:1792-1015

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Spandidos Publications style
Georgakopoulou VE, Gkoufa A, Makrodimitri S, Tsakanikas A, Basoulis D, Voutsinas PM, Karamanakos G, Eliadi I, Samara S, Triantafyllou M, Triantafyllou M, et al: Risk factors for the in‑hospital and 1‑year mortality of elderly patients hospitalized due to COVID‑19‑related pneumonia. Exp Ther Med 27: 22, 2024.
APA
Georgakopoulou, V.E., Gkoufa, A., Makrodimitri, S., Tsakanikas, A., Basoulis, D., Voutsinas, P.M. ... Sipsas, N.V. (2024). Risk factors for the in‑hospital and 1‑year mortality of elderly patients hospitalized due to COVID‑19‑related pneumonia. Experimental and Therapeutic Medicine, 27, 22. https://doi.org/10.3892/etm.2023.12310
MLA
Georgakopoulou, V. E., Gkoufa, A., Makrodimitri, S., Tsakanikas, A., Basoulis, D., Voutsinas, P. M., Karamanakos, G., Eliadi, I., Samara, S., Triantafyllou, M., Eleftheriadou, I., Kampouropoulou, O., Papageorgiou, C. V., Anastasopoulou, A., Papalexis, P., Trakas, I., Trakas, N., Spandidos, D. A., Steiropoulos, P., Sipsas, N. V."Risk factors for the in‑hospital and 1‑year mortality of elderly patients hospitalized due to COVID‑19‑related pneumonia". Experimental and Therapeutic Medicine 27.1 (2024): 22.
Chicago
Georgakopoulou, V. E., Gkoufa, A., Makrodimitri, S., Tsakanikas, A., Basoulis, D., Voutsinas, P. M., Karamanakos, G., Eliadi, I., Samara, S., Triantafyllou, M., Eleftheriadou, I., Kampouropoulou, O., Papageorgiou, C. V., Anastasopoulou, A., Papalexis, P., Trakas, I., Trakas, N., Spandidos, D. A., Steiropoulos, P., Sipsas, N. V."Risk factors for the in‑hospital and 1‑year mortality of elderly patients hospitalized due to COVID‑19‑related pneumonia". Experimental and Therapeutic Medicine 27, no. 1 (2024): 22. https://doi.org/10.3892/etm.2023.12310