Abstract
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).
Table.
Reported Pathogens for Pneumonia Admissions From 1993 to 2011
| Year | No. of Admissions per 100 000 | %
|
|||||||
|---|---|---|---|---|---|---|---|---|---|
| No Organism Specified | Any Streptococcal Species | Streptococcus pneumoniae | Any Staphylococcal Species | MRSAa | Pseudomonas | H influenzae | Other Bacteria | ||
| 1993 | 350.4 | 65.9 | 7.1 | 5.7 | 3.6 | NA | 3.9 | 3.6 | 14.0 |
| 1994 | 362.5 | 66.7 | 6.8 | 5.5 | 3.5 | NA | 4.1 | 3.4 | 14.1 |
| 1995 | 381.9 | 66.0 | 6.5 | 5.3 | 3.8 | NA | 3.8 | 3.0 | 15.5 |
| 1996 | 380.9 | 66.8 | 6.2 | 5.2 | 3.9 | NA | 4.0 | 2.7 | 15.0 |
| 1997 | 382.6 | 69.9 | 5.8 | 4.8 | 4.0 | NA | 4.0 | 2.3 | 12.8 |
| 1998 | 433.2 | 76.5 | 5.8 | 4.8 | 4.1 | NA | 3.3 | 2.2 | 6.5 |
| 1999 | 453.2 | 80.8 | 4.8 | 4.1 | 3.8 | NA | 2.8 | 1.5 | 4.2 |
| 2000 | 421.6 | 82.2 | 4.6 | 3.8 | 3.9 | NA | 2.5 | 1.2 | 3.7 |
| 2001 | 405.3 | 84.1 | 4.0 | 3.3 | 4.0 | NA | 2.4 | 1.2 | 3.4 |
| 2002 | 421.9 | 84.9 | 3.7 | 3.1 | 4.1 | NA | 2.3 | 0.9 | 2.9 |
| 2003 | 444.5 | 84.3 | 3.3 | 2.8 | 4.1 | NA | 2.3 | 0.8 | 3.1 |
| 2004 | 418.3 | 85.0 | 3.1 | 2.6 | 4.2 | NA | 2.3 | 0.7 | 3.2 |
| 2005 | 468.1 | 84.8 | 2.8 | 2.3 | 4.3 | NA | 2.3 | 0.7 | 3.0 |
| 2006 | 436.3 | 85.7 | 2.9 | 2.3 | 4.2 | NA | 2.2 | 0.6 | 2.9 |
| 2007 | 428.1 | 85.5 | 2.9 | 2.3 | 4.4 | NA | 2.3 | 0.5 | 3.3 |
| 2008 | 439.5 | 83.4 | 3.0 | 2.5 | 4.7 | 0.7 | 2.3 | 0.5 | 4.0 |
| 2009 | 429.7 | 82.7 | 3.0 | 2.4 | 4.3 | 3.1 | 2.3 | 0.5 | 4.4 |
| 2010 | 411.3 | 84.8 | 2.6 | 2.0 | 3.9 | 2.9 | 2.4 | 0.4 | 4.7 |
| 2011 | 442.4 | 83.9 | 2.3 | 1.7 | 3.9 | 2.8 | 2.3 | 0.4 | 5.2 |
| P Value | .001 | <.001 | <.001 | <.001 | .004 | .31 | <0.01 | <.001 | <.001 |
| R2 | 0.48 | 0.70 | 0.92 | 0.94 | 0.40 | 0.47 | 0.72 | 0.87 | 0.56 |
Abbreviations: MRSA, methicillin-resistant Staphylococcus aureus; NA, not available.
International Classification of Diseases, Ninth Revision, Clinical Modification, coding was unavailable for years with an NA indication.
Figure.
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.
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.
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.
Acknowledgments
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.
Footnotes
Conflict of Interest Disclosures: None reported.
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.
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.
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. doi: 10.1056/NEJMoa1209165. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. doi: 10.1001/jama.2012.384. [DOI] [PubMed] [Google Scholar]
- 3.US Census Bureau. [Accessed July 21, 2014];US Population by Year. 2013 http://www.multpl.com/united-states-population/table.
- 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. doi: 10.1164/ajrccm.160.2.9808045. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1007/s10096-012-1778-4. [DOI] [PubMed] [Google Scholar]
- 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 pneumoniae. J Clin Microbiol. 2013;51(7):2303–2310. doi: 10.1128/JCM.00137-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Wunderink RG. Community-acquired pneumonia versus healthcare-associated pneumonia: the returning pendulum. Am J Respir Crit Care Med. 2013;188(8):896–898. doi: 10.1164/rccm.201308-1536ED. [DOI] [PubMed] [Google Scholar]