Abstract The aims of this study were to determine the clinical and epidemiological characteristics of community-acquired pneumonia (CAP) in the elderly, ...
Eur J Clin Microbiol Infect Dis (2001) 20 : 14–19
Q Springer-Verlag 2001
Article
Clinical Aspects and Prognostic Factors in Elderly Patients Hospitalised for Community-Acquired Pneumonia M.A. García-Ordón˜ez, J.M. García-Jiménez, F. Páez, F. Álvarez, B. Poyato, M. Franquelo, J.D. Colmenero, C. Juárez Abstract The aims of this study were to determine the clinical and epidemiological characteristics of community-acquired pneumonia (CAP) in the elderly, to identify prognostic factors, and to establish a predictive model for mortality of CAP. Elderly patients with CAP admitted to “Carlos Haya” Hospital in Malaga, Spain, over a 36-month period were included. Multivariate analysis was used to identify prognostic factors from variables present on admission, from which a discrimination rule was constructed to predict mortality. A total of 343 patients were included, with the annual incidence ranging from 16.3 to 28.1 per 1,000 admissions. Most (82.5%) had some kind of accompanying or underlying disease. Clinical presentation was atypical in 87 (25.4%). Microbiological diagnosis was made in 24.5%. There were 49 (14.3%) deaths. The prognostic factors in multivariate analysis on admission were bilateral radiographic infiltrate, a blood urea nitrogen level of more than 7 mmol/l, absence of fever, a respiratory rate of 30/min or more, confusion, and shock. The discriminating rule to predict mortality comprising three or more of these factors was 91.2% specific, with a negative predictive value of 93.4% and an overall accuracy of 86.9%. CAP in the elderly is associated with a high degree of mortality. The discriminating rule incorporating the prognostic factors identified is a powerful predictor of mortality.
Introduction Due to its high incidence and considerable morbidity and mortality, community-acquired pneumonia (CAP) in the elderly represents a very important public health problem [1]. Despite the availability of adequate antimicrobial agents, CAP is still one of the main causes of death in this age group, with mortality rates ranging from 16 to 33% [2–4]. Although age has been reported to be an independent risk factor for death in several studies analysing outcome in CAP [5–7], age by itself is not the only factor giving rise to the high incidence and
M.A. García-Ordón˜ez, J.M. García-Jiménez, F. Páez, F. Álvarez, B. Poyato, M. Franquelo, J.D. Colmenero, C. Juárez Complejo Hospitalario Universitario “Carlos Haya”, Málaga, Spain M.A. García-Ordón˜ez (Y) c/ Horacio Lengo 17, 4 B, 29006 Málaga, Spain e-mail: magomalaga6airtel.net Tel.: c34-95-1061435 Fax: c34-95-1061435
mortality rates of CAP in the elderly. Other associated factors often present in the elderly could also be involved [8–9]. Knowledge of those factors determining a worse outcome in CAP may help in decisions concerning hospitalisation and the initial treatment of these patients. Although prior studies have described many factors associated with an increased risk of death in a nonselected population due to CAP [10], few have focussed on the prognostic factors in an exclusively elderly population. We therefore analysed the epidemiological characteristics and the clinical spectrum of CAP in the elderly to identify those prognostic features influencing mortality.
Patients and Methods Selection of Cases. We studied all patients aged 65 years or older who were admitted with CAP to a 1,000-bed teaching hospital from January 1996 to December 1998. CAP was defined as (i) the presence of a new pulmonary infiltrate suggestive of pneumonia
15 on chest radiography; (ii) the presence of clinical signs and symptoms of lower respiratory tract infection; and (iii) acquisition of the infection outside the hospital. Patients were excluded from the study if (i) they had been hospitalised during the 2 weeks prior to admission; (ii) they were also infected with the human immunodeficiency virus; (iii) there was an alternative disease to explain the radiographic findings; or (iv) they were admitted from a nursing home or chronic-care facility. Data Collection. A protocol was drawn up for the collection of data which included social and demographic characteristics, underlying or accompanying diseases, physical symptoms and findings at admission, laboratory values, chest radiography features, complications during hospitalisation, and evolution of CAP. Definitions. Smokers were considered to be those who had smoked 10 or more cigarettes per day for the last 10 years. Alcoholism was considered to be the intake of 80 g/day or more of alcohol over the same period. Immunosuppression was defined as the use of systemic steroids (more than 20 mg of prednisone per day or its equivalent for 2 weeks or more), systemic chemotherapy, or radiotherapy. Malnutrition was defined as a reduction of at least 10% in ideal body weight. CAP was classified according to the initial clinical symptoms at presentation as either typical or atypical. Typical CAP was defined as the presence of two or more of the following: fever (temperature 637.8 7C), cough, purulent expectoration, and pleuritic pain. Atypical pneumonia was defined as the presence of other symptoms in the absence of the previous criteria. Shock was defined as a systolic blood pressure below 90 mmHg, urinary excretion of less than 20 ml/h for more than 4 h, or the need for vasopressor agents. Acute renal failure was defined as an increase in serum creatinine above 1.3 mg/dl not previously noted. An increase in the size of the infiltrate greater than 50% within 48 h of admission was considered evidence of a progressively rapid radiographic spread. Death related to CAP was defined as death due to the pneumonia or one of its direct complications (hypoxaemia, adult respiratory distress syndrome, multiple organ failure, shock, renal failure). Microbiological Investigations. Two or more sets of blood cultures with an aerobic and an anaerobic tube in each set were obtained on admission to hospital. Blood samples were also taken on admission and 3 weeks later to check for the presence or increase in specific antibody titres to Legionella pneumophila, Mycoplasma pneumoniae, Coxiella burnetii, or Chlamydia pneumoniae. The serological tests used were fixed complement for Mycoplasma pneumoniae and Coxiella burnetii and indirect immunofluorescence for Legionella pneumophila. Serological testing for detection of Chlamydia pneumoniae antibodies was performed using microimmunofluorescence. Respiratory samples were obtained when possible, by means of sputum collection, bronchoalveolar lavage, protected specimen brush, and pleural fluid collection. A sputum sample was defined as valid if it contained more than 25 polymorphonuclear leucocytes per field. The degree of certainty of the aetiological diagnosis was established as definite, probable, or unknown. The aetiology of CAP was considered definite [11] in the case of (i) isolation of the bacteria in blood culture, pleural fluid, protected specimen brush sample (cutoff point 610 3 cfu/ml), or bronchoalveolar lavage fluid (cutoff point 610 4 cfu/ml); or (ii) a fourfold increase or greater in the initial specific antibody titres for Legionella pneumophila (IgG61/128), Mycoplasma pneumoniae (IgG61/512), Coxiella burnetii (IgG61/64), or Chlamydia pneumoniae (IgG61/512). The aetiological diagnosis was classified as probable if a valid sputum sample yielded one or more predominant bacterial strains. Data regarding definite and probable aetiological diagnoses were considered together for purposes of analysis. Statistical Analysis. Data were analysed by chi-square test and Fisher’s exact test for comparison of proportions and Student’s t
or Mann-Whitney test for comparison of means. Continuous variables were analysed as categorical variables when appropriate, using clinically relevant cutoff points. Backward-LR multivariate logistic regression analysis was used to analyse the prognostic factors of mortality. A level of significance of less than 0.10 was required for inclusion in the model or greater than 0.05 for exclusion. A predictive model of mortality was established that included variables present only at the time of admission. The odds ratio (OR) and its corresponding 95% confidence intervals (95% CI) were determined for each of the prognostic factors. The goodness of fit of the model was established by means of the Hosmer-Lemeshow test [12]. A discriminating rule was generated from the prognostic factors included in the predictive model in order to predict mortality due to CAP at the time of admission. The diagnostic usefulness of the rule was evaluated by calculating the sensitivity, the specificity, the positive and negative predictive values, the overall accuracy, and the likelihood ratio associated with a positive rule. Calculations were made with the statistical programs EPI-Info 6.0 (Centers for Disease Control, USA) and SPSS 6.0.1. (SPSS, USA).
Results A total of 368 patients aged 65 years or older were admitted with CAP during the study period, of whom 25 were excluded from the study: 12 who failed to meet the inclusion criteria and 13 who lacked complete data. Thus, 343 patients were included in the study and evaluated. There were 199 (58%) men and 144 (42%) women, and the mean age was 76.3B7.3 years (range, 65–99 years). The incidence of CAP in elderly persons during this period ranged from 16.3–28.1 per 1,000 admissions, and the mean hospital stay was 13B8.7 days. Table 1 shows the accompanying diseases and underlying conditions of the patients, 283 (82.5%) of whom had some sort of comorbidity and 59 (17.2%) of whom had a prior history of CAP. The clinical presentation was considered typical in 256 (74.6%) patients, and 83 (24.2%) patients had received antibiotic therapy prior to their admission. At admission 48 (14%) patients had shock, 70 (20.4%) tachypnoea (respiratory rate 630/min), 67 (19.5%) confusion, and 118 (34.4%) fever. Table 2 shows the characteristics of the chest radiographs. Microbiological diagnosis was made in 84 patients (24.5%; 95% CI, 20.1–29.5) and was considered definite in 53 patients. The microbial agents found most frequently were Streptococcus pneumoniae (41.7%), Haemophilus influenzae (19%), and other gram-negative bacilli (23.8%). Table 3 shows the microorganisms isolated and the diagnostic methods used. The most common antibiotic therapy was second- or third-generation cephalosporins, used either alone or in combination with macrolides in 256 (74.6%) patients. Pulmonary complications arose in 42 (12.2%) patients during the course of the disease: adult respiratory distress syndrome in 26, empyema in 11, pulmonary thromboembolism in 7, and pneumothorax in 2. There
16 Table 1 Comorbid conditions in elderly patients with community-acquired pneumonia Comorbid condition
No. (%) of patients with comorbidity
No. (%) of patients who died
COPD Congestive heart failure Malnutrition Diabetes mellitus Neurological disease Neoplasia Chronic renal failure Immunosuppression Smoking Alcoholism
139 98 92 84 53 51 18 13 128 31
23 12 15 12 14 11 3 2 17 7
(40.5) (28.6) (26.8) (24.5) (15.5) (14.9) (5.2) (3.8) (37.4) (9.6)
(16.5) (12.2) (16.3) (14.3) (26.4) (21.7) (16.7) (15.4) (13.3) (22.6)
COPD, chronic obstructive pulmonary disease
Table 2 Radiographic findings of community-acquired pneumonia in elderly patients Radiographic finding
No. (%) of patients
Alveolar pattern Interstitial pattern Segmentary infiltrate Lobar infiltrate Infiltrate in 1 1 lobe Unilateral Bilateral Pleural effusion Rapid progressive radiographic spread
322 21 150 139 54 295 48 57 49
(93.9) (6.1) (43.7) (40.6) (15.7) (86) (14) (16.6) (14.3)
were extrapulmonary complications in 24 (7%) patients: acute renal failure in 14, septic shock in 9, upper digestive tract haemorrhage in 5, cerebral stroke in 4, and other complications in 4. A total of 49 (14.3%; 95% CI, 10.9–18.5) patients died, 8 (16.3%) during the first 48 h in hospital. The variables that proved to be significant in univariate analysis
as factors related to mortality are shown in Table 4. Among those prognostic factors present at admission, bilateral pulmonary infiltrate, a blood urea nitrogen level of more than 7 mmol/l, absence of fever, a respiratory rate of 30/min or more, confusion, and shock were predictive of death in multivariate analysis (Table 5). Using the prognostic factors included in the predictive model as a base, a discriminating rule was generated to predict mortality at the time of admission. This rule consisted of the presence of three or more of the prognostic factors included in the predictive model. Table 6 shows the test performance of the rule. A positive discriminating rule was associated with a 16-fold greater risk of death and predicted mortality with 91.2% specificity and a 93.4% negative predictive value.
Discussion As evidenced by the 343 cases in the elderly included in the 3-year study period, CAP is a relatively common cause of hospital admission in this age group, particularly in persons weakened by disease or underlying comorbidity. The incidence of CAP in the elderly is increasing along with the progressive ageing of the population, there being two main factors involved: the consequences of aging on the respiratory system and the general presence of concomitant disease [13]. The high percentage of accompanying disease found in our patients (83%), similar to that reported by others [14–20], confirms this circumstance. A high percentage of patients in this study (25%) had an atypical clinical presentation. Prior studies [15–20] have reported that elderly patients with CAP report a subjectively lower number of respiratory and nonrespiratory symptoms compared to younger patients. This phenomenon may reflect the independent physiological effects of aging or, alternatively, the effects of the increased illness burden that parallels advanced age. The lower prevalence of symptoms in the elderly can
Table 3 Microbial agents involved in the etiological diagnosis of community-acquired pneumonia in the elderly Agent
No. (%) of patients
Source of isolation
Streptococcus pneumoniae Haemophilus influenzae Other gram-negative bacilli a Legionella pneumophila Chlamydia pneumoniae Staphylococcus aureus Mycoplasma pneumoniae Moraxella catarrhalis Streptococcus agalactiae Total
35 16 20 4 3 2 2 1 1 84
19 sputum, 12 blood culture, 9 BAL 12 sputum, 3 BAL, 1 protected specimen brush 7 sputum, 12 blood culture, 6 BAL 1 sputum, 4 serum b 3 serology 2 sputum, 1 blood culture 2 serum b protected specimen brush sputum
a
(41.7) (19) (23.8) (4.8) (3.6) (2.4) (2.4) (1.2) (1.2) (24.5)
Escherichia coli (np7), Pseudomonas aeruginosa (np4), Klebsiella pneumoniae (np4), Proteus mirabilis (np2), Serratia marcescens (np2), Citrobacter freundii (np1)
b Antibodies detected by serological testing BAL, bronchoalveolar lavage
17 Table 4 Univariate analysis of prognostic factors associated with community-acquired pneumonia in the elderly Risk factor
No. (%) of survivors
No. (%) of deaths
Unadjusted odds ratio
95% CI
Age ( 1 75 years) Atypical syndrome Tachypnoea Shock Absence of fever Confusion Leucopaenia (^4,000!10 9/l) Hyperazotaemia (BUN 1 7 mmol/l) Hypoalbuminaemia (~25 g/l) Hypoxaemia (pO2~60 mmHg) Hypoprothrombinaemia (^60%) Bilateral radiographic infiltrate Radiographic spread Pulmonary complications Extrapulmonary complications
151 65 44 28 89 41 9 83 82 146 24 31 27 13 11
34 22 26 20 29 26 5 31 22 32 9 17 22 29 13
2.2 2.9 6.4 6.6 3.3 7 3.6 4.4 2.1 1.9 2.5 4.5 8.1 32.8 9.6
1.1–4.4 1.5–5.6 3.2–13 3.1–13.9 1.7–6.6 3.4–14.2 0.9–12.6 2.2–8.7 1.1–4.1 1–3.8 1.1–6.2 2.1–9.6 3.8–16.9 13.7–80.6 3.6–25.3
(51.4) (22.1) (15) (9.5) (30.3) (13.9) (2.6) (28.2) (27.9) (49.6) (8.2) (10.5) (9.2) (4.4) (3.7)
(69.4) (44.9) (53.1) (40.8) (5.2) (53.1) (10.2) (63.2) (44.9) (65.3) (18.4) (34.7) (44.9) (59.2) (26.5)
BUN, blood urea nitrogen
Table 5 Multivariate analysis of prognostic factors associated with mortality Variable
Adjusted odds ratio
95% CI
Bilateral radiographic infiltrate Hyperazotaemia Absence of fever Tachypnoea Confusion Shock
5.2 4.3 4.2 4.1 3.7 2.8
2–13.2 1.9–9.4 1.9–9.2 1.9–9.1 1.6–8.5 1.1–7.2
have an important impact on the initial clinical care because it may delay the diagnosis and initiation of adequate treatment, thereby worsening the prognosis [20]. CAP in elderly patients also has a different distribution of aetiological agents compared to those found in younger persons. The most frequent pathogens in our series were Streptococcus pneumoniae and gram-negative bacilli (including Haemophilus influenzae), similar to those found by others [3, 18–21]. However, it was only possible to make an aetiological diagnosis in 84 (24.5%) patients; of these diagnoses, 53 were considered definite. This low percentage of identification of the microbiological agent could have several explanations. First, 83 (24.2%) patients had received antibiotic therapy prior to their admission, which could have
interfered with the identification of the aetiological agent. Second, it was not possible to carry out serological tests in those patients who died, so that the identification of determinate pathogens may be underestimated. Finally, identification of the pathogen was not always attempted, especially in those debilitated patients requiring invasive diagnostic techniques. There were 49 (14.3%) deaths among our patients. The mortality associated with CAP in the elderly is still high, with rates from 13 to 40% [3, 9, 19–22]. Few studies concerning the factors predictive of mortality in this group of patients have been published. In this study several independent prognostic factors of mortality were identified, suggesting that death is related to the severity of the pneumonia (tachypnoea and bilateral radiological infiltrate), to an inadequate response to infection (absence of fever, shock, and confusion), and to the burden of underlying and associated diseases that worsen the state of health (hyperazotaemia). These prognostic factors have been described in other studies in both nonselected [10] and elderly patients [3, 20–22]. Despite the fact that advanced age has been described as a specific risk factor for death in CAP [2, 19, 23–26], in our study, after adjustment for other factors, older age was not an independent risk factor for death. This agrees with results from other authors [8, 20–22] suggesting that age by itself is not a predictor of death. In studies that included an exclusive subset of elderly patients only,
Table 6 Test performance of discriminating rule in predicting mortality in elderly patients with community-acquired pneumonia Discriminating rule to predict mortality
Positive predictive value
Negative predictive value
Overall accuracy
Sensitivity
Specificity
Likelihood ratio
Presence of 63 prognostic factors
30/56 (53.6%)
268/287 (93.4%)
298/343 (86.9%)
30/49 (61.2%)
268/294 (91.2%)
6.9
18
age would lose specific weight as a prognostic factor in CAP, so that other factors, such as those related to the underlying disease burden or an inadequate response to infection, would acquire greater importance. In our opinion, an important contribution of this study is the establishment of a simple discriminating rule to predict mortality in elderly patients with CAP. Previous studies have elaborated similar rules to predict death from CAP in nonselected patients [11,27–29], but their suitability for use with older patients remains uncertain. Fine et al. [29] have developed a specific prognostic index for CAP in adults that adequately identifies those patients with a low risk of mortality. However, although these indices are useful for determining prognosis in the general adult population, their usefulness is less clear in subsets of patients such as the elderly. The aetiological spectrum of CAP is different in elderly patients than in young patients. Moreover, elderly patients with CAP have a greater burden of underlying diseases, a less manifest clinical presentation, and a different therapeutic response than younger patients. In the present study, the discriminating rule, composed of the presence of at least three prognostic factors identified by multivariate analysis, was a powerful predictor of death, with high specificity, negative predictive value, and overall accuracy. Several limitations of this study should be noted. First, since the definition of pneumonia was based on clinical and radiological criteria, and, given the low percentage of microbiological isolates, the possibility of incorrect diagnoses of pneumonia cannot be ruled out. However, we believe these criteria are well defined and correspond to those used in daily clinical practice. Second, the study group was composed of elderly hospitalised patients, and no ambulatory patients were included. This could hamper the general applicability of our results to all elderly patients with CAP. Likewise, because nursing home residents were excluded, our findings may not apply to this population, which is at high risk for pneumonia. These patients are often debilitated and are not similar to those in the study group with respect to associated pathogens, morbidity, or mortality. Our study shows the predictive value of a simple discriminating rule that incorporates prognostic factors identified by multivariate analysis. This predictive rule may help clinicians decide on the initial therapeutic management and the requirement for specialised care in those patients at risk of death. Nevertheless, as others have pointed out [26, 30–31], it remains to be seen whether, despite special care and attention, the outcome in these patients is modified. Moreover, given the special aetiological, clinical, and evolutionary characteristics of elderly patients with CAP compared with unselected adult patients, further studies should be undertaken in order to validate widely accepted prog-
nostic indicators, such as those of Fine et al. [29], for this special group of patients. Acknowledgements The authors thank I. Johnstone for help with the English language of the manuscript.
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