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(Chest. 2005;127:213-219.)
© 2005 American College of Chest Physicians

Multicenter Study of Hospital-Acquired Pneumonia in Non-ICU Patients*

Nieves Sopena, MD, PhD and Miquel Sabrià, MD, PhD; the Neunos 2000 Study Group{dagger}

* From the Infectious Diseases Unit, University Hospital Germans Trias i Pujol, Badalona (Barcelona), Spain. {dagger} A list of Neunos 2000 Study Group members is given in the Appendix.

Correspondence to: Nieves Sopena, MD, PhD, Unitat de Malalties Infeccioses. Hospital Universitari Germans Trias i Pujol, C/Canyet s/n, Badalona CP 08916 (Barcelona), Spain; e-mail: nsopena{at}ns.hugtip.scs.es


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Appendix
 References
 
Study objective: To know the incidence, epidemiology, etiology, and outcome of hospital-acquired pneumonia (HAP) in non-ICUs adult patients.

Setting: Twelve Spanish teaching hospitals.

Interventions: From April 1999 to November 2000, non-ICU HAP was prospectively studied by active, bimonthly 1-week surveillance. Epidemiologic data, etiology, and evolution of pneumonia were recorded. Blood and sputum cultures and Legionella pneumophila and Streptococcus pneumoniae urinary antigen tests were performed.

Results: We included 186 patients, with complete data available in 165 patients (70.3% male gender; mean age, 63.7 ± 16.9 years [ ± SD]) The mean incidence of HAP was 3 ± 1.4 cases/1,000 hospital admissions. Most patients (64.2%) were in medical wards, had severe underlying diseases (66.6%), and had a hospital stay > 5 days (76.4%). Blood cultures were performed in 139 patients (84.2%), sputum cultures were performed in 89 patients (53.9%), and urinary antigen detection was performed in 123 patients (74.5%). An etiologic diagnosis was obtained in 60 cases (36.4%), and 31 were definitive. The most frequent etiologies were S pneumoniae (16 cases, 14 definitive), L pneumophila (7 cases, 7 definitive), Aspergillus sp (7 cases, 3 definitive), Pseudomonas aeruginosa (7 cases, 2 definitive), and several Enterobacteriaceae (8 cases, 4 definitive). Clinical complications occurred in 52.1% of the cases, and mortality was 26% (13.9% attributed to pneumonia).

Conclusions: Non-ICU HAP is an important cause of hospital morbidity, observed most frequently in medical wards and elderly patients with severe underlying diseases. In this setting, S pneumoniae and Legionella sp should be considered in addition to other nosocomial pathogens; urinary antigen detection is useful in determining the prevalence of these microorganisms.

Key Words: hospital-acquired pneumonia • ICU • Legionella pneumonia • Legionnaires’ disease • nosocomial infection


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Appendix
 References
 
Hospital-acquired pneumonia (HAP) is considered the second-most-frequent cause of nosocomial infection, accounting for 15 to 20% of these infections.1 It usually occurs in patients with underlying diseases, increases nosocomial morbidity and mortality, prolongs hospital stay, and raises the cost of health care.2 The incidence of HAP is highest in the ICU, especially among patients who require mechanical ventilation, in whom it carries the greatest mortality.34 However, the frequency of nosocomial pneumonia is increasing in patients admitted to conventional hospitalization wards.56789

Most epidemiologic and etiologic studies3410111213 on nosocomial pneumonia have been focused on critically ill patients and patients receiving mechanical ventilation. On the contrary, there is scarce information on HAP outside the ICU (non-ICU HAP), probably because of the dispersion of cases within the hospital wards hindering surveillance and the difficulty in performing invasive diagnostic techniques.1415 Moreover, the etiologic diagnoses are usually based on results of blood cultures and expectorated sputum or tracheal secretions because of the inability to perform invasive procedures in most of the cases. However, few studies on HAP surveillance have applied urinary antigen detection for Legionella pneumophila and Streptococcus pneumoniae, a test that has been extensively used in community-acquired pneumonia because of its sensitivity and specificity.161718 The aims of this study were to know the incidence, epidemiology, etiology, and outcome of HAP in adult patients admitted to conventional hospitalization wards.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Appendix
 References
 
Setting and Period of Study
The study was performed prospectively in 12 Spanish teaching hospitals with 150 to 1,750 beds, ICU and active medical and surgical departments, from April 1999 to November 2000.

Patients
Patients admitted to conventional medical, surgical, and trauma hospitalization wards were surveyed for HAP. Cases were detected by means of an active 1-week surveillance performed every 2 months by physicians from the Departments of Infectious Diseases or Microbiology, who received grants to carry out this work. They made a daily review of chest radiograph reports for new infiltrates and/or fever charts of all the hospitalized patients. If the above criteria were positive, the patient was evaluated for possible inclusion in the study.

The case definition was as follows: (1) age > 14 years; (2) clinical and radiologic data of pneumonia, including previously absent pulmonary infiltrate on chest radiography, and at least two of the following criteria: fever > 38°C, dyspnea, cough and purulent expectoration, signs of consolidation on respiratory auscultation, leukocytosis > 12,000/µL or leukopenia < 3,000/µL; and (3) appearance of pneumonia after 72 h of hospital admission or within 10 days following prior discharge. The exclusion criteria included the acquisition of pneumonia in the ICU, and diagnosis made outside the surveillance period.

The patients included were followed up until hospital discharge or death. Complications and mortality were recorded. The judgment of attributable mortality was made by the investigator who followed up the patient at each study site.

Variables Studied
The following data were recorded for all patients included in the study: (1) age and gender; (2) intrinsic and extrinsic risk factors, such as underlying diseases, severity of the comorbid illness, pharmacologic immunosuppression (corticosteroids and chemotherapy), previous antibiotic therapy, histamine type 2 blockers, antacids, nebulization, invasive techniques (endotracheal intubation, tracheotomy, nasogastric tube), surgery, and interval from hospital admission to nosocomial pneumonia and previous admission to ICU; and (3) patient location (hospitalization ward). We also recorded the extent of chest radiographic abnormalities according to the interpretations of the investigators, whether the antibiotic therapy was considered adequate or inadequate, as well as the complications and the crude and attributable mortality.

Definitions
The incidence of HAP was calculated by dividing the number of new cases of pneumonia acquired in the hospital in each period by the number of patients admitted in this period. Underlying diseases were considered as the presence of a comorbid illness. Malnutrition was defined as albumin values < 30 g/L. Depression of consciousness was considered when any degree of alteration in the level of alertness was observed at the time of presentation of pneumonia or within the previous 72 h. Severity of the underlying or actual conditions on hospital admission was classified as fatal (< 1 year), ultimately fatal (in 5 years), or nonfatal (in 5 years) using the method described by Britt et al.19

The extrinsic risk factors (nebulization or respiratory therapy, previous endotracheal intubation, tracheotomy, nasogastric tube, surgery, ICU admission, antibiotic therapy, histamine type 2 blockers, and antacids) were considered if they were present or performed within the 15 days prior to the diagnosis of the pneumonia. Previous antimicrobial therapy was recorded if the patient had taken these drugs for at least 48 h and histamine type 2 blockers for at least 7 days. Corticosteroids referred to treatment with > 60 mg/d of prednisone over > 2 weeks in the last month or > 5 mg/d for more than the previous 3 weeks. Chemotherapy referred to treatment with cytotoxic drugs not including steroid therapy. Length of hospitalization was defined as the time in days from hospital admission to the development of HAP. Antibiotic treatment was defined as adequate if the empirical drugs chosen were administered according to the practice guidelines, and were changed according to the microbiological diagnosis and susceptibility reports.

Deaths were considered to be attributable to nosocomial pneumonia if the episode of HAP was the primary cause of death or contributed to it. Deaths directly or indirectly related to HAP were joined into a single category provided that they occurred before the episode of nosocomial pneumonia was considered resolved.

Microbiological Methods
The microbiological methods routinely used were as follows: (1) blood cultures (hospital laboratory), (2) sputum or tracheal aspirate cultures (hospital laboratory), and (3) urinary antigen detection of S pneumoniae by immunochromatographic assay and L pneumophila serogroup 1 by enzyme immunoassay (reference laboratory). Invasive techniques such as fiberoptic bronchoscopy with protected catheter technique were performed only when requested by the attending physician.

The etiologic diagnostic criteria were defined as follows: (1) definitive, by isolation of a microorganism in blood cultures, pleural fluid, respiratory sample representative of the lower respiratory tract (fiber-optic bronchoscopy with protected catheter), by isolation of a primary pathogen (such as Legionella sp) in sputum, or by a positive urinary antigen test finding for L pneumophila or S pneumoniae; or (2) possible, with isolation of a nonprimary pathogen in adequate sputum samples (degree 4 to 5 of Murray and Washington20) in pure or predominant culture, which correlated with the predominant morphology in Gram stain.

Statistical Analysis
The data collected from each patient were entered into a database and then analyzed by SPSS version 11.5 for Windows (SPSS; Chicago, IL).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Appendix
 References
 
Incidence and Place of Acquisition of HAP
From April 1999 to November 2000, we included 186 patients, although complete data were only available in 165 patients. Some surveillance was not carried out in four hospitals (one period in one center and two periods in three centers). The number of cases detected in each center ranged from 4 to 29 (mean, 15.5 ± 7.4 [± SD]). The incidence of HAP ranged from 1.3 to 5.9 cases/1,000 hospital admissions, with a mean of 3.1 ± 1.4/1,000 hospital admissions. The hospitalization wards in which patients with nosocomial pneumonia were detected are shown in Table 1 .


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  		Table 1.. Hospitalization Wards in Which HAP Was Diagnosed (n = 165)

 
Patient Demographics and Risk Factors
The demographic characteristics and the risk factors of the 165 patients with HAP are shown in Tables 2, 3 . The mean interval from hospital admission to nosocomial pneumonia was 15 ± 26 days (range, 3 to 126 days).


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  		Table 2.. Demographics and Intrinsic Risk Factors of Patients (n = 165)*

 

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  		Table 3.. Extrinsic Risk Factors of Patients (n = 165)*

 
Microbiological Studies
The microbiological studies performed were blood cultures in 139 cases (84.2%), urinary antigen detection in 123 cases (74.5%), and sputum or tracheal aspirate culture in 89 adequate samples (53.9%) from the 112 samples (67.9%) obtained. Bronchoscopy with protected catheter was only applied in four patients (2.4%).

The blood culture findings were positive in 13 cases (9.3%) (5 for S pneumoniae, 2 for Pseudomonas aeruginosa, 2 for Escherichia coli, 2 for Enterobacter sp, 1 for Klebsiella pneumoniae, and 1 for Staphylococcus aureus). Urinary antigen findings were positive in 21 cases (17.1% of those performed), 7 for L pneumophila, and 14 for S pneumoniae. The sputum or tracheal aspirate culture findings were positive in 37 cases (41.5% of adequate sputum samples).

Etiology of HAP
Etiologic diagnosis was achieved in 60 of 165 patients, representing 36.4% of the cases (Table 4 ). Mixed etiology was considered in eight cases.


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  		Table 4.. Etiology in 165 Cases of HAP

 
Characteristics of the Patients by Etiology
S pneumoniae was diagnosed in 16 cases by isolation in blood cultures (5 cases), urinary antigen detection (14 cases, including all the cases with positive blood culture findings), and/or sputum culture (7 cases). The mean age of the patients was 58.2 ± 18.6 years. Twelve patients (75%) had one or more underlying diseases (mainly neoplasms in 7 patients, heart failure in 4 patients, and COPD in 3 cases) that were fatal or ultimately fatal in 11 cases; 5 patients had undergone surgery (mainly thoracic surgery in three patients). Fourteen patients (87.5%) had been hospitalized for > 5 days, with a mean hospitalization interval of 17.2 ± 21.2 days.

L pneumophila was diagnosed in seven cases by urinary antigen detection. The mean age of the patients was 54.3 ± 19.5 years. Six patients had underlying diseases that were fatal or ultimately fatal in four cases; five patients had received steroids, and two patients had received chemotherapy. Cases were detected in several medical5 and surgical2 wards of five different hospitals, with a mean hospitalization interval to pneumonia of 18 ± 9 days.

Aspergillus sp was diagnosed in seven patients from different hospitals, who had fatal or ultimately fatal underlying diseases (five neoplasms with neutropenia in two patients, one COPD, and one HIV infection). Four patients had received steroids, three had received antibiotics, and one had received chemotherapy.

P aeruginosa was diagnosed in seven patients who had fatal or ultimately fatal underlying diseases (five neoplasms, with neutropenia in one case, and two COPD), after a mean hospitalization interval of 11.5 ± 6.7 days. Moreover, three patients had received previously steroids, two had received chemotherapy, and five had received antibiotics.

Outcome of HAP
Radiologic presentation was unilateral segmental (involving a segment or all of one lobe) in 96 cases (58.2%), unilateral extensive (involving more than one lobe in one lung) in 21 cases (12.7%), and bilateral (involving the two lungs) in 48 cases (29.1%). Antibiotic treatment was adequate in 152 of 160 cases (95%), and was inadequate in the remainder.

Complications were observed in 86 cases (52.1%), with respiratory failure in 57 cases (34.5%), pleural effusion in 34 cases (20.6%), septic shock in 16 cases (9.6%), renal failure in 8 cases (4.8%), and empyema in 4 cases (2.4%). Forty-three patients (26%) died. Death was attributable to pneumonia in 30 patients (18.1%), being directly related to nosocomial pneumonia in 23 patients (13.9%) and indirectly related in 7 patients (4.2%).

The rate of crude mortality in the different hospitals ranged from 7.1 to 50%, and the attributable mortality from 0 to 38.5%. The outcome (crude and attributable mortality) of the patients who did not receive appropriate antibiotics was significantly worse than those with appropriate treatment. The crude mortality was 75% (6 of 8 cases) vs 22.4% (34 of 152 cases), respectively (p = 0.003, relative risk, 10.41; 95% confidence interval, 2.01 to 53.95), and the attributable mortality was 50% (4 of 8 cases) vs 15.1% (23 of 152 cases), respectively (p = 0.02; relative risk, 4.92; 95% confidence interval, 1.31 to 18.49).

The etiology of these 30 cases with attributable mortality was known in 15 episodes: S pneumoniae (three definitive), L pneumophila (three definitive), Aspergillus sp (two definitive), P aeruginosa (two possible), Acinetobacter sp (four possible), and Enterococcus faecalis (one possible). The distribution of pathogens in the 13 patients with nonattributable mortality was unknown in eight cases, S pneumoniae in 2 cases, L pneumophila in 1 case, Aspergillus in 1 case, and Xanthomonas in 1 case.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Appendix
 References
 
Most of the epidemiologic and etiologic data of HAP in the literature refers to ventilator-associated pneumonia (VAP) because of its high incidence and elevated morbidity and mortality.24 In this setting, the microorganisms responsible for VAP are well defined, and a series of hospital-wide infection surveillance including VAP patients are probably biased.678910 Patients in conventional hospital wards are not exposed to such aggressive maneuvers as patients receiving mechanical ventilation; thus, changes in the oropharyngeal flora are probably delayed and the community flora persist longer in them. In addition, these patients are more susceptible to the pathogens present in the air and water. These facts had led us to consider the hypothesis that microorganisms responsible for pneumonia acquired in the general hospitalization wards may therefore differ from those implicated in VAP.

To our knowledge, this is the first prospective, multicenter study on HAP in patients admitted to conventional hospitalization wards that incorporate urinary antigen testing to diagnose Legionella as well as pneumococcal infection. The incidence of HAP found in this study (3.1 ± 1.4 cases/1,000 hospital admissions) is slightly lower than that reported previously.28 These differences may depend on the definition applied, the methodology used, the characteristics of the hospital population, and the hospital setting.

Contrary to previous studies212 in which HAP prevailed in surgical departments, two thirds of the cases occurred in medical wards. The greater number of patients admitted in medical departments in most centers as well as the longer stay and greater comorbidity than those patients in surgical departments may explain this fact. Coinciding with wide hospital surveys, the oncology and hematology departments were frequently affected due to the characteristics of these patients, although the rate of severely immunosuppressed neutropenic patients was low (7.3%).5910

The risk factors for HAP observed in our study are similar to those considered in the hospital-wide series of the literature.261011131415 Most patients were male and > 60 years old; three quarters had comorbidity, mainly neoplasms, COPD, diabetes, and heart failure, which were fatal or ultimately fatal in two thirds of the cases. We also frequently found some extrinsic risk factors that have been described to interfere with the defenses of the lung or to favor colonization with resistant microorganisms: pharmacologic treatments such as antibiotics in half of the patients, anti-histamine type 2 and corticoids in one third, and surgery in nearly 30% of the cases.45678910 Prolonged hospitalization is another known risk factor for HAP, with most of the patients (84.7%) in our study being hospitalized for > 5 days.10 However, case-control studies, including hospitalized patients without HAP, are necessary to determine the importance of the risk factors observed in this group of patients.

As reported in a previous study14 of HAP in noncritical patients, the rate of etiologic diagnosis was only achieved in one third of the cases, because of the inability to perform invasive procedures in most of the cases. As previously reported, the sensitivity of the blood cultures was low (positive in 5.7% of cases), being most useful in HAP caused by S pneumoniae (positive in 31% of the cases).21 Sputum culture was performed in more than a half of the patients, but its profitability was low because the isolated microorganisms were normal oropharyngeal flora or may colonize hospitalized patients.22 However, urinary antigen detection for L pneumophila and S pneumoniae was the most sensitive test carried out in our study (positive in 17.1% of those performed). The incorporation of these tests to the diagnostic of HAP may be useful to know the prevalence of these relevant pathogens, because they are easy to perform and have a high sensitivity and specificity.161718

S pneumoniae was the most frequent etiology of HAP in patients who had a definitive diagnosis made. Contrary to what is observed in VAP, most of these cases occurred in patients hospitalized for > 5 days and with severe comorbidity.4 On the contrary, the importance of Gram-negative pathogens, widely implicated in ICU patients, seems to be lower in nonseverely immunosuppressed patients. Most of the patients included in our study had not previously undergone oropharyngeal manipulation, which plays an important role in the selection of microorganisms causing pneumonia in patients receiving ventilation.232425 We hypothesize that the normal flora remains longer in these patients, and pathogens causing community-acquired pneumonia such as S pneumoniae may play an important role in HAP. However, the endotracheal tube in patients receiving ventilation is the main risk factor for S aureus VAP, thereby justifying the exceptional presentation of this etiology in HAP.10

Environmental microorganisms such as Legionella sp and Aspergillus sp should be taken into account in HAP in patients not receiving ventilation. In hospital outbreaks of Legionella, the patients receiving ventilation are not affected because they are not exposed to contaminated aerosols (except in cases in which nonsterile water is used in the mechanical ventilators).26 L pneumophila was diagnosed in seven patients in five different hospitals without an outbreak situation. In one hospital, it was the first case of nosocomial legionellosis diagnosed in the center. Most of the patients had severe underlying disease and had received steroid therapy. Consequently, the application of the Legionella urinary antigen test to all cases of HAP seems to be necessary, since this microorganism may be more prevalent than expected in previous reports. Moreover, environmental cultures looking for Legionella may be necessary to determine which hospitals are at risk for Legionnaires’ disease.26

Likewise, pneumonia caused by Aspergillus sp is exceptional in the ICU setting, being mainly described in severely immunosuppressed patients (neutropenic and transplanted, steroid therapy). Diagnosis of invasive pulmonary aspergillosis is difficult because there is no enough sensitive or specific test. However, as observed in our study, it should also be considered in patients admitted to conventional hospitalization areas with severe underlying disease undergoing steroid therapy and frequently previous antibiotics.27

Non-ICU HAP has considerable morbidity and mortality.28 However, the mortality of the patients in this series was lower compared to other series of HAP including VAP.711 Extensive radiologic presentation and clinical complications were observed in half of the patients. According to other authors, early appropriate antibiotic therapy improved the outcome of HAP with a lower attributable mortality.11

There are some limitations in our study. The methodology applied (1-week periods of active surveillance every 2 months) was scheduled to improve protocol compliance in all the centers. The participation of several hospitals of different characteristics may provide us with a wider view of the problem, although bias may be produced. The application of noninvasive diagnostic tests did not allow us determination of the importance of the microorganisms that are normal oropharyngeal flora or colonize hospitalized patients.

In conclusion, nosocomial pneumonia in noncritical patients is an important cause of hospital morbidity that involves mainly medical wards and elderly patients with severe underlying disease. S pneumoniae and Legionella sp should be seriously considered in this setting, with urinary antigen detection being an useful noninvasive method to know the prevalence of these clinically relevant microorganisms.


   Appendix
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Appendix
References
 
The Neunos 2000 Study Group: Infectious Diseases Unit, University Hospital Germans Trias i Pujol, Badalona, Barcelona (Drs. Pedro-Botet and Reynaga); Microbiology Department, Complexo Hospitalario Juan Canalejo, A Coruña (Drs. Losada and Guerrero); Infectious Diseases Department, Hospital Clinic, Barcelona (Drs. Moreno and Mensa; Infectious Diseases Department, University Hospital Virgen de la Arriaxaca, Murcia (Drs. Ortín and Gómez); Microbiology and Infectious Diseases Department, Hospital Gregorio Marañón, Madrid, Spain (Drs. Perez and Bouza); Microbiology Department, Hospital La Fe, Valencia (Drs. Gutierrez and Gobernado); Internal Medicine-Infectious Diseases Department, Hospital del Mar, Barcelona (Drs. Gonzalez and Saballs); Infectious Diseases Department, Hospital Virgen del Rocío, Sevilla (Drs. Cordero and Pachón); Infectious Diseases Department, Hospital Vall d’Hebron, Barcelona (Drs. Paradiñeiro and Almirante); Microbiology Department, Hospital de Basurto, Bilbao (Drs. Liendo and Cisterna); Infectious Disease Department, Hospital Parc Taulí, Sabadell, Barcelona (Drs. Antón and Segura); Infectious Disease Unit, Hospital del Aire, Madrid (Drs. Ledesma and Gomis), Spain.


   Footnotes
 
Abbreviations: HAP = hospital-acquired pneumonia; VAP = ventilator-associated pneumonia

This article has been presented in part at the 41st Interscience Conference on Antimicrobial Agents and Chemotherapy, Chicago, IL, December 2001.

This study was conducted with the financial support of Bristol-Myers-Squibb and the Red Respira (Instituto de Salud, Carlos III).

Received for publication February 5, 2004. Accepted for publication August 13, 2004.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Appendix
 References
 

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