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Figure.
Documentation of Specific Bacterial Pathogens for Pneumonia From 1993 to 2011
Documentation of Specific Bacterial Pathogens for Pneumonia From 1993 to 2011

Streptococcal species, especially Streptococcus pneumoniae, were the most frequently coded pathogens in 1993. There were decreases in the documentation of streptococcal species, Haemophilus influenzae, and Pseudomonas, whereas documentation of Staphylococcus aureus increased modestly.

Table.  
Reported Pathogens for Pneumonia Admissions From 1993 to 2011
Reported Pathogens for Pneumonia Admissions From 1993 to 2011
1.
Griffin  MR, Zhu  Y, Moore  MR, Whitney  CG, Grijalva  CG.  US hospitalizations for pneumonia after a decade of pneumococcal vaccination. N Engl J Med. 2013;369(2):155-163.
PubMedArticle
2.
Lindenauer  PK, Lagu  T, Shieh  MS, Pekow  PS, Rothberg  MB.  Association of diagnostic coding with trends in hospitalizations and mortality of patients with pneumonia, 2003-2009. JAMA. 2012;307(13):1405-1413.
PubMedArticle
3.
US Census Bureau. US Population by Year, 2013.http://www.multpl.com/united-states-population/table. Accessed July 21, 2014.
4.
Ruiz  M, Ewig  S, Marcos  MA,  et al.  Etiology of community-acquired pneumonia: impact of age, comorbidity, and severity. Am J Respir Crit Care Med. 1999;160(2):397-405.
PubMedArticle
5.
Rozenbaum  MH, Pechlivanoglou  P, van der Werf  TS, Lo-Ten-Foe  JR, Postma  MJ, Hak  E.  The role of Streptococcus pneumoniae in community-acquired pneumonia among adults in Europe: a meta-analysis. Eur J Clin Microbiol Infect Dis.2013;32(3):305-316.
PubMedArticle
6.
Sinclair  A, Xie  X, Teltscher  M, Dendukuri  N.  Systematic review and meta-analysis of a urine-based pneumococcal antigen test for diagnosis of community-acquired pneumonia caused by Streptococcus pneumoniaeJ Clin Microbiol. 2013;51(7):2303-2310.
PubMedArticle
7.
Wunderink  RG.  Community-acquired pneumonia versus healthcare-associated pneumonia: the returning pendulum. Am J Respir Crit Care Med. 2013;188(8):896-898.
PubMedArticle
Research Letter
November 2014

Trends in Pathogens Among Patients Hospitalized for Pneumonia From 1993 to 2011

Author Affiliations
  • 1Department of Pulmonary and Critical Care Medicine, Northwestern University, Chicago, Illinois
  • 2Section of Hospital Medicine, Department of Medicine, University of Chicago, Chicago, Illinois
  • 3School of Medicine and Pharmacology, Royal Perth Hospital Unit, University of Western Australia, Perth, Australia
JAMA Intern Med. 2014;174(11):1837-1839. doi:10.1001/jamainternmed.2014.4344

The Nationwide Inpatient Sample aggregated data from approximately 20% of US hospital admissions from 1993 to 2011. Prior literature found that pneumonia admissions decreased following the introduction of the pneumococcal vaccine in 2000.1 The International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM), codes provide information regarding pneumonia pathogens, but no studies, to our knowledge, have used these codes to analyze longitudinal trends in the pathogens documented during hospitalizations for pneumonia.

Methods

We selected patients 18 years or older admitted for pneumonia based on a principal diagnosis of pneumonia (ICD-9-CM codes 480.0-480.3, 480.8, 480.9, 481, 482.0-482.9, 483.0-483.8, 485, 486, and 487). Consistent with recent literature,2 we also selected hospitalizations with pneumonia as a secondary diagnosis if the principal diagnosis was sepsis (ICD-9-CM codes 038.8, 038.9, 785.52, 995.91, and 995.92) or respiratory failure (ICD-9-CM codes 518.81, 518.82, 518.84, and 799.1). For each pathogen, we used a linear regression model with year of hospitalization as the explanatory variable and the percentage of cases coded with that pathogen as the dependent variable. We obtained annual population estimates from the US Census Bureau.3

Results

From January 1, 1993, to December 31, 2011, hospitalizations for pneumonia increased from 910 676 to 1 378 551 (350.4 to 442.4 per 100 000 US population; P < .001) (Table and Figure). The proportion of admissions with no reported pathogen increased from 65.9% to 83.9% (P < .001). Admissions with the nonpneumonia principal diagnoses were more likely to have pathogens documented (odds ratio, 1.28; 95% CI, 1.25-1.30; P < .001). From 1993 to 2011, there were declines in the coding of streptococcal species (from 7.1% to 2.3%; P < .001), Pseudomonas (from 3.9% to 2.3%; P < .001), and Haemophilus influenzae (from 3.6% to 0.4%; P < .001); however, the coding of Staphylococcus aureus increased (from 3.6% to 3.9%; P = .004).

Unadjusted inpatient mortality did not change significantly (from 8.7% to 7.8%; P = .40). Cases coded with S aureus had the highest mortality (12.0%).

Discussion

To our knowledge, this is the first analysis of trends in the microbiologic pathogens in patients hospitalized for pneumonia based on nationally representative data spanning nearly 2 decades.

Streptococcus pneumoniae has been reported to be the most common cause of community-acquired pneumonia.4 Declines in cases of adult pneumonia due to S pneumoniae may be related to more frequent and effective vaccination as well as to herd immunity from increased pediatric vaccination after 2000.1 In addition to prevention, vaccination reduces the risk of invasive pneumococcal disease and bacteremia. We hypothesize that this reduced risk may have resulted in less-frequent coding because more thorough diagnostic evaluations accompany a higher severity of disease.5 We observed a reduction in Streptococcus, despite the addition of urine antigen testing.6 Furthermore, quality improvement initiatives to reduce the time from presentation to antibiotic administration may also have reduced the yield of traditional culture-based diagnostics. We cannot know with certainty how the contributions of vaccination and changes in diagnostic tests affected the trends that we describe. However, we believe that our findings suggest important changes in pneumonia pathogens.

Streptococcuspneumoniae was the most frequent pathogen in 1993 and S aureus was the most frequent in 2011, most of which was methicillin-resistant S aureus (MRSA). Because we included hospitalizations with certain alternative principal diagnoses, it is likely that our case definition included some patients with health care–associated pneumonia, which may have increased our identification of MRSA. Despite the trends observed, the low incidence of S aureus (<4%) suggests that MRSA coverage is not routinely indicated for patients with community-acquired pneumonia.7

We have described changes in pneumonia pathogens from hospital admissions during 2 decades. We believe that these changes should be considered for public health monitoring and care for pneumonia, which is the leading cause of infectious death in the United States.

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Article Information

Corresponding Author: Sean B. Smith, MD, Department of Pulmonary and Critical Care Medicine, Northwestern University, 675 N St Clair St, Ste 18-250, Chicago, IL 60611 (sean@northwestern.edu).

Published Online: September 8, 2014. doi:10.1001/jamainternmed.2014.4344.

Author Contributions: Dr Smith had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Smith, Weiss, Waterer, Wunderink.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Smith, Ruhnke, Waterer, Wunderink.

Critical revision of the manuscript for important intellectual content: All authors.

Statistical analysis: Smith, Ruhnke.

Administrative, technical, or material support: Wunderink.

Study supervision: Ruhnke, Weiss, Waterer, Wunderink.

Conflict of Interest Disclosures: None reported.

Funding/Support: Dr Smith is supported by National Institutes of Health/National Heart, Lung, and Blood Institute training grant T32HL076139. Dr Weiss is supported by National Institutes of Health/National Heart, Lung, and Blood Institute grant K23HL118139 and a grant from the Parker B. Francis Fellowship Program. Dr Wunderink is supported in part by Centers for Disease Control and Prevention grant 1U18IP000490.

Role of the Sponsor: The sponsors had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Previous Presentation: A preliminary version of this work was presented as a poster at the American Thoracic Society International Conference; May 19, 2013; Philadelphia, Pennsylvania.

References
1.
Griffin  MR, Zhu  Y, Moore  MR, Whitney  CG, Grijalva  CG.  US hospitalizations for pneumonia after a decade of pneumococcal vaccination. N Engl J Med. 2013;369(2):155-163.
PubMedArticle
2.
Lindenauer  PK, Lagu  T, Shieh  MS, Pekow  PS, Rothberg  MB.  Association of diagnostic coding with trends in hospitalizations and mortality of patients with pneumonia, 2003-2009. JAMA. 2012;307(13):1405-1413.
PubMedArticle
3.
US Census Bureau. US Population by Year, 2013.http://www.multpl.com/united-states-population/table. Accessed July 21, 2014.
4.
Ruiz  M, Ewig  S, Marcos  MA,  et al.  Etiology of community-acquired pneumonia: impact of age, comorbidity, and severity. Am J Respir Crit Care Med. 1999;160(2):397-405.
PubMedArticle
5.
Rozenbaum  MH, Pechlivanoglou  P, van der Werf  TS, Lo-Ten-Foe  JR, Postma  MJ, Hak  E.  The role of Streptococcus pneumoniae in community-acquired pneumonia among adults in Europe: a meta-analysis. Eur J Clin Microbiol Infect Dis.2013;32(3):305-316.
PubMedArticle
6.
Sinclair  A, Xie  X, Teltscher  M, Dendukuri  N.  Systematic review and meta-analysis of a urine-based pneumococcal antigen test for diagnosis of community-acquired pneumonia caused by Streptococcus pneumoniaeJ Clin Microbiol. 2013;51(7):2303-2310.
PubMedArticle
7.
Wunderink  RG.  Community-acquired pneumonia versus healthcare-associated pneumonia: the returning pendulum. Am J Respir Crit Care Med. 2013;188(8):896-898.
PubMedArticle
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