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(Chest. 2005;128:3233-3239.)
© 2005 American College of Chest Physicians

Etiology and Outcome of Community-Acquired Pneumonia in Patients With Diabetes Mellitus*

Miquel Falguera, MD; Ricard Pifarre, MD; Antonio Martin, MD; Anas Sheikh, MD and Anna Moreno, MD

* From the Department of Internal Medicine, Hospital Universitari Arnau de Vilanova, Lleida, Spain.

Correspondence to: Miquel Falguera, MD, Servei de Medicina Interna, Hospital Universitari Arnau de Vilanova, Rovira Roure 80, 25198 Lleida, Spain; e-mail: mfalguera{at}comll.es


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: It has been suggested that diabetes mellitus is associated with an increased susceptibility to infection, the risk of using more aggressive therapeutic agents, and increased morbidity and mortality; however, current evidence supporting these events in the field of pneumonia is scarce. The aim of the present study was to provide information on clinical and microbiological characteristics and the outcome of community-acquired pneumonia in patients with diabetes mellitus.

Design: Prospective study of cases.

Setting: A university hospital in Lleida, Spain.

Patients: During a 5-year period, we prospectively studied the clinical and radiologic characteristics, the spectrum of causative agents and other microbiological data, and the outcomes of 660 consecutive episodes of community-acquired pneumonia. Data derived from 106 patients with diabetes mellitus were analyzed and compared with data obtained from the remaining population.

Measurements and results: Patients with diabetes mellitus were significantly older (p = 0.001) and more frequently had other concomitant comorbid conditions (p = 0.018). Diabetes was also significantly associated with the development of pleural effusion (p = 0.015) and mortality (p = 0.002); for both events, diabetes remained as an independent predictive factor in multivariate analyses. By contrast, the incidence of the main etiologic agents, and the bacteremia or empyema rates did not show significant differences in relation to the remaining patients. In the subgroup of patients with diabetes, mortality was associated with the presence of multilobar infiltrates (p = 0.004), concomitant underlying diseases (p = 0.004), and some diabetes-related complications (nephropathy, p = 0.040; and vasculopathy, p = 0.002), although only multilobar infiltrates and comorbidities were selected as prognostic factors in the multivariate analysis.

Conclusions: In patients with community-acquired pneumonia, diabetes mellitus is associated with a poor prognosis, increasing the rate of pleural effusion and mortality. Our results suggest that this adverse outcome is more attributable to the underlying circumstances of patients than to uncommon microbiological findings.

Key Words: bacteremia • community-acquired pneumonia • comorbid condition • diabetes mellitus • empyema • etiology • outcome • pleural effusion


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Underlying diseases increase the susceptibility of patients for community-acquired pneumonia; therefore, it is not surprising that epidemiologic studies have found one or more of these conditions in a high proportion of such episodes.12 It has also been reported that some comorbidities can influence the spectrum of causative agents, facilitating unusual and more aggressive microorganisms; alternatively, habitual pathogens could show particular patterns of antimicrobial resistance.345 Undoubtedly, the knowledge of these microbiological characteristics is critical and represents the basis for empirical treatments. Moreover, serious coexisting illnesses have been identified in several studies13456 as modifying factors of the severity of the pneumonia; thus, these conditions can increase the risk of bacteremia and empyema, and usually provide a poor prognosis.

On the basis of these appreciations, published guidelines on community-acquired pneumonia advocate specific criteria for antibiotic selection and the management of patients in the presence of comorbid diseases.7 Unfortunately, the real impact of some of these underlying diseases on pneumonia has not been fully evaluated.

Diabetes mellitus is a very prevalent chronic metabolic disorder that is present in about 5 to 10% of the elderly population.8 Several aspects of immunity, such as polymorphonuclear leukocyte function (ie, leukocyte adherence, chemotaxis, and phagocytosis) and bactericidal activity of serum are depressed in patients with diabetes.910 In consequence, some specific infections are very common in these patients, while others occur with more severity or are associated with an increased risk of complications.11 For patients with community-acquired pneumonia, diabetes mellitus is also one of the most common underlying diseases1212; however, it remains uncertain as to whether pneumonia shows particular clinical manifestations, increases morbidity or mortality, or involves a predisposition for more aggressive agents in patients with diabetes. In this article, we proposed to determine whether the clinical or radiologic findings, the causative microorganisms, or the outcome of community-acquired pneumonia are modified by the presence of diabetes mellitus as the underlying disease.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Setting and Study Design
For a 5-year period (January 1998 to December 2002), all adult patients in whom community-acquired pneumonia had been diagnosed in the emergency department of the Arnau de Vilanova Hospital in Lleida (Catalonia, Spain) were evaluated for inclusion in a prospective study on epidemiologic, clinical, microbiological, and outcome parameters. This study was examined and approved by the scientific and ethics committees of the institution.

Clinical Evaluation of Patients
On study enrollment, all patients gave a complete clinical history and underwent a physical examination, a chest radiograph, and basic chemistry and hematology tests. The presence of comorbid conditions was determined by patient reports and medical record reviews.

For patients with a high initial glucose level, and for those who had a prior diagnosis of diabetes, glycemic monitoring and the measurement of hemoglobin A1c levels was carried out during follow-up. In addition, the presence of diabetes-related complications was carefully evaluated according to the patient’s hospital records, current clinical manifestations, and the presence of blood or urine chemistry abnormalities. When needed, specific tests, such as measurements of the 24-h protein excretion rate in urine, ophthalmoscopy, electromyography, echocardiography, and noninvasive or invasive vascular tests, were ordered.

The validated Pneumonia Severity Index was used to determine the severity of illness at presentation, and patients were stratified in prognostic groups.13 Outcomes of patients and complications during follow-up also were collected for a 30-day period after they reached the clinical resolution of pneumonia.

Definitions
Community-acquired pneumonia was defined as the presence of an acute illness with features of lower respiratory tract infection (with two or more of the following signs and symptoms: fever; new or increasing cough or sputum production; dyspnea; chest pain; and new focal signs on chest examination) and the presence of a consolidation in the chest radiograph that was consistent with acute infection. Patients with tuberculosis or opportunistic infections were excluded from the study.

A diagnosis of diabetes mellitus was based on a previous clinical and/or biochemical diagnosis of diabetes mellitus and/or treatment with oral antidiabetic agents or insulin. Alternatively, diagnosis could be established during this episode of pneumonia when the fasting plasma glucose concentration was ≥ 126 mg/dL (7.0 mmol/L), and/or after ingestion it was ≥ 200 mg/dL (11.1 mmol/L) on two or more separate occasions.14 A diagnosis of nephropathy required an excretion rate of albumin of > 30 mg per 24 h in two separate samples.

Microbiological Studies
Microbiological evaluation included the following tests: two samples for blood aerobic and anaerobic conventional cultures; Gram and culture of sputum, when it was available; urine for detection of antigen of Streptococcus pneumoniae or Legionella pneumophila by using a rapid test (Binax Now test; Leti Laboratories; Barcelona, Spain); Gram stain and culture of pleural fluid, if a sufficient amount of pleural effusion was radiologically detected; a sample of blood and pleural fluid (if it was available) for S pneumoniae DNA detection by the polymerase chain reaction (PCR) method; and paired serum samples for serologic studies to detect antibodies against Mycoplasma pneumoniae, L pneumophila, Coxiella burnetii, Chlamydia psittaci, Chlamydia pneumoniae, and viruses (ie, adenovirus, influenza A, influenza B, and parainfluenza). The methodology used for the PCR test in whole blood or pleural fluid has been described in previous articles.1516

According to microbial results, an etiologic diagnosis was considered to be definite when a respiratory pathogen was isolated from blood or pleural fluid, a fourfold or greater increase in serologic titters was demonstrated, and/or the presence of the genome of S pneumoniae in blood or pleural fluid by PCR or the antigen of L pneumophila or S pneumoniae in urine was detected. In contrast, an etiologic diagnosis was considered probable when a respiratory pathogen was isolated from a good-quality sputum specimen or when high serologic titers without seroconversion were found. The remaining cases were defined as pneumonia of unknown etiology.

Statistical Analysis
Data were analyzed using a commercially available software package (SPSS for Windows, version 11.0; SPSS Inc; Chicago, IL). In univariate analyses, differences in proportions were tested with the {chi}2 test or Fisher exact test, and differences in the means of dimensional variables were tested with the Student t test. The level of significance was set at p < 0.05.

Multivariate analyses were performed to evaluate the true impact of diabetes mellitus on the development of pleural effusion and mortality in patients with community-acquired pneumonia. For these analyses, we selected all candidate predictor variables, including demographic variables (age and sex), coexisting illnesses (diabetes mellitus, and other concomitant underlying diseases with the following comorbidities: neoplastic disease; congestive heart failure; cerebrovascular disease; chronic renal disease; HIV infection; and chronic liver disease), and microbiological and radiologic findings.

Multivariate analyses were also performed to determine factors that were independently associated with mortality and the development of pleural effusion among patients with community-acquired pneumonia and diabetes mellitus. We selected demographic variables (age and sex), coexisting illnesses (including the following comorbidities: neoplastic disease; congestive heart failure; cerebrovascular disease; chronic renal disease; HIV infection; and chronic liver disease), length of the disease (> 4 years or < 4 years), glucose and hemoglobin A1c levels, diabetes-related complications (retinopathy, nephropathy, vasculopathy, and peripheral neuropathy), insulin therapy during pneumonia, and microbiological and radiologic findings. Variables were entered into a final model using a stepwise multiple logistic regression analysis.

The pneumonia severity index was excluded from multivariate analyses because it includes most of the remaining potential predictor variables. Results of multivariate analyses are reported as odds ratios with confidence intervals and p values, taking p < 0.05 as the level of statistical significance.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Seven hundred twenty-six patients showing clinical and radiologic findings of community-acquired pneumonia were enrolled in the study; however, 66 patients were subsequently excluded from the study for the following reasons: misdiagnosis at enrollment (n = 59); nosocomial acquisition hospitalization (n = 4); and consent not obtained (n = 3). Thus, 660 patients constituted the final study group. Underlying diseases were found in 324 patients (49%), among which COPD (114 patients), diabetes mellitus (106 patients), and congestive heart disease (58 patients) were the most common.

The subgroup of patients with diabetes mellitus was mainly constituted by patients with type 2 diabetes, which was diagnosed in 100 patients (94%). The mean duration of illness was 8 years, although for 14 patients the diagnosis was established during the present episode of pneumonia. At study entry, the mean plasma glucose level was 238 mg/dL, and the mean hemoglobin A1c value was 8.1%. Diabetes-related complications were common among these patients; thus, 20 patients (19%) had diabetic retinopathy, 18 patients (17%) had diabetic nephropathy, 18 patients (17%) had experienced major macrovascular events (eg, ischemic heart disease, stroke, or intermittent claudication), and 5 patients (5%) had peripheral polyneuropathy; for only 56 patients were complications absent. In addition to diet, 59 patients (56%) were receiving treatment with oral agents, and 40 patients (38%) were receiving treatment with insulin (both therapies were simultaneously used in 18 patients); however, during pneumonia 95 patients (90%) needed insulin therapy.

The characteristics of patients with diabetes and community-acquired pneumonia were compared with those of the remaining subgroup of patients, and the results are shown in Table 1 . In the univariate analysis, patients with diabetes were significantly older (p = 0.001) and had more severe pneumonia according to the prognostic classification (p < 0.001); in consequence, hospitalization was more frequently required (p < 0.001). Pleural effusion was also more likely to occur in patients with diabetes (p = 0.015). By contrast, the incidences of empyema or complicated parapneumonic effusion, as well as other epidemiologic, clinical, or radiologic parameters, did not show statistically significant differences. In this univariate analysis, diabetes appeared as a significant prognostic factor associated with mortality (p = 0.002).


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  		Table 1. Characteristics of Community-Acquired Pneumonia, and Comparison Between Patients With and Without Diabetes Mellitus*

 
In the multivariate analysis (Table 2 ), diabetes remained significantly (p = 0.027) associated with mortality. Age > 65, the presence of other concomitant comorbid conditions, bacteremia, empyema, and multilobar infiltrates were also found to be independent factors related to mortality. Diabetes was also an independent factor associated with the development of pleural effusion.


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  		Table 2. Multivariate Analyses of Factors Associated With Mortality and Development of Pleural Effusion in Patients With Community-Acquired Pneumonia*

 
If we perform a study that is restricted to patients with diabetes (Table 3 ), we can see that mortality was associated with the presence of concomitant underlying diseases (p = 0.004), some diabetes-related complications, such as nephropathy (p = 0.040) and vasculopathy (p = 0.002), and multilobar infiltrate (p = 0.004). No relation was found with age, sex, length of the disease, period from diagnosis of diabetes, glucose level at entry, hemoglobin A1c level, insulin therapy during pneumonia, bacteremia, pleural effusion, and empyema or complicated effusion. By contrast, in the multivariate analysis (Table 4 ), only a multilobar infiltrate (p = 0.003) and the simultaneous presence of comorbidities (p = 0.029) were found to be independently associated with mortality. Finally, pleural effusion appeared to be significantly associated with some diabetes-related complications (ie, nephropathy [p = 0.010] and vasculopathy [p = 0.038]), and the presence of other comorbidities in the multivariate analysis.


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  		Table 3. Diabetes-Related Findings and Other Characteristics of Patients With Diabetes Mellitus: Univariate Analysis of Factors Associated With Mortality*

 

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  		Table 4. Multivariate Analyses of Factors Associated With Mortality and Pleural Effusion in Patients With Diabetes Mellitus and Community-Acquired Pneumonia*

 
Microbiological results obtained from patients with diabetes, in comparison with the nondiabetic population, did not show significant differences (Table 5 ). For both groups, S pneumoniae, which was identified in 225 patients (34%), was the agent most commonly isolated. For the 12 strains of S pneumoniae recovered from patients with diabetes (7 in blood, 1 in pleural fluid, and 4 in sputum), 11 (92%) were susceptible to penicillin (minimum inhibitory concentration, ≤ 0.06 µg/mL) and 1 had an intermediate susceptibility (minimum inhibitory concentration, 0.12 to 1 µg/mL). In relation to erythromycin, nine strains (75%) were susceptible, and three were resistant; all 12 strains were sensitive to cefotaxime and quinolones. In comparison, for the 74 isolates of S pneumoniae obtained from patients without diabetes, the rates of resistance were as follows: penicillin, 44% (intermediate, 32%; resistant, 12%); erythromycin, 35%; cefotaxime, 3%; quinolones, 1% (differences not significant). Atypical microorganisms, such as C pneumoniae, M pneumoniae, and L pneumophila, were also frequent etiologic agents. A polymicrobial infection was detected in 10 patients (9%) with diabetes and in 49 patients (9%) without diabetes. For 41 patients with diabetes (29%) and 161 patients without diabetes (39%), the etiology remained unknown.


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  		Table 5. Comparison of Causative Agents in Patients With and Without Diabetes Mellitus*

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
In this study, we evaluated 106 episodes of community-acquired pneumonia in patients with diabetes mellitus, and the results were compared with those observed in a population of 554 patients with community-acquired pneumonia who did not have diabetes. We found that diabetes was significantly associated with advanced age, the simultaneous presence of other comorbidities, and radiologic evidence of pleural effusion; these episodes were classified as more severe pneumonia, and the rates of hospitalization and mortality were increased. Diabetes mellitus was also identified as an independent predictor of mortality and pleural effusion in multivariate analyses. By contrast, microbiological results, including rates of bacteremia and empyema and the spectrum of causative agents, did not show differences in comparison with patients without diabetes. A multivariate analysis, selecting only patients with pneumonia and diabetes, found that a multilobar infiltrate and the presence of other underlying diseases were independently associated with mortality.

We know the main characteristics of pneumonia in several subgroups of patients that were defined on the basis of some demographic or clinical parameters. Thus, patients at the extremes of the age range (ie, children and the elderly or the very elderly) with pneumonia have been evaluated, and their specific differences have been recognized.171819 Similarly, patients with pneumonia and HIV infection have been extensively analyzed in the past decades, and there has been research conducted on pneumonia in patients with neutropenia or COPD.342021 By contrast, for patients with diabetes mellitus, which is one of the most prevalent coexisting diseases, the available information in the literature regarding clinical characteristics and microbiological data is very limited.11

Diabetes mellitus has been associated with many alterations of the immune system. In a review of the subject by Joshi et al,11 the most significant changes were identified within humoral-mediated immunity, particularly related to the polymorphonuclear function. Pulmonary function abnormalities, in particular a reduction in diffusion capacity, have been found in patients with diabetes and signs of microangiopathy.22 Moreover, evidence has been found that better glycemic control improves immune mechanisms, and reduces the predisposition to infections and their severity.2324 In relation to pulmonary infections, the few available studies32526 suggest, but do not prove, certain associations between diabetes and susceptibility by uncommon microorganisms, poor prognosis of pneumonia, and high rates of bacteremia and empyema. However, these conclusions are not supported by strong scientific evidence. In fact, the most extensive study13 on the prognosis of community-acquired pneumonia, found plasma glucose levels in blood, but not diabetes, to be an independent mortality risk factor.

The methodology applied by researchers in the study of patients with pneumonia is not uniform. The selection of microbiological tests and methods, the guidelines for the management of patients, and even criteria for the definition of clinical parameters can have substantial differences. In consequence, in order to recognize specific differences in a subgroup of patients, it is advisable to perform studies that simultaneously include, as we did, a comparative population that was analyzed using the same methods.

Six significant differences defined our subgroup of patients with diabetes mellitus, in contrast with the remaining sample of patients with pneumonia. Two of them, age and the presence of other underlying diseases, are unmodifiable baseline characteristics. In addition, two other variables are clearly dependent on these baseline data; thus, in the calculation of the prognostic score, age and comorbidities play a decisive role,13 and both should be considered in making decisions about hospitalization.7 Finally, diabetes was also significantly associated with two adverse events in patients with pneumonia, mortality and the development of a pleural effusion. We may speculate that these complications were also dependent on the baseline characteristics of patients with diabetes, particularly their advanced age and concomitant comorbid conditions. Certainly, age and prior comorbidities, as well as multilobar infiltrates, bacteremia, and empyema, parameters that have already been related to poor prognosis in previous investigations,61327 were variables that were independently associated with mortality; however, in this multivariate analysis, diabetes also remained a significant prognostic factor of mortality. Similarly, diabetes was found to be independently associated with the development of pleural effusions, although the percentage of cases of empyema or complicated pleural effusion was not increased. In this situation, we can attribute many episodes of pleural effusion to certain diabetes-related complications, such as chronic renal insufficiency, hypoalbuminemia, or congestive heart failure; the statistical analysis supported this opinion.

An extensive use of diagnostic tests, including sensitive and specific newly developed methods, allowed us to determine the microbial etiology in a high proportion of episodes of community-acquired pneumonia. A high predisposition for bacteremia or uncommon microorganisms, which has been suggested by others,252528 was not found in our study. These results allow us to suspect that the spectrum of causative agents of pneumonia in patients with diabetes does not show relevant differences in comparison with the overall population.

In summary, the findings from this study can help the management of patients with diabetes and community-acquired pneumonia. Diabetes was significantly associated with mortality and the development of pleural effusions; in both circumstances, diabetes was an independently contributive factor. By contrast, microbiological results did not support the opinion that diabetes predisposes patients to bacteremia, empyema, or more aggressive etiologic agents.


   Acknowledgements
 
We thank Javier Trujillano, MD, for his contribution to the statistical analysis of the data.


   Footnotes
 
Abbreviation: PCR = polymerase chain reaction

Received for publication March 2, 2005. Accepted for publication May 18, 2005.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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