Infect Chemother.  2018 Dec;50(4):287-300. 10.3947/ic.2018.50.4.287.

Disease Burden and Etiologic Distribution of Community-Acquired Pneumonia in Adults: Evolving Epidemiology in the Era of Pneumococcal Conjugate Vaccines

• Heo JY
• Song JY

• KMID: 2429932
• DOI: http://doi.org/10.3947/ic.2018.50.4.287

Abstract

Pneumonia is the leading cause of morbidity and mortality, particularly in old adults. The incidence and etiologic distribution of community-acquired pneumonia is variable both geographically and temporally, and epidemiology might evolve with the change of population characteristics and vaccine uptake rates. With the increasing prevalence of chronic medical conditions, a wide spectrum of healthcare-associated pneumonia could also affect the epidemiology of community-acquired pneumonia. Here, we provide an overview of the epidemiological changes associated with community-acquired pneumonia over the decades since pneumococcal conjugate vaccine introduction.

Keyword

Pneumonia; Incidence; Mortality; Epidemiology; Pneumococcal conjugate vaccine

MeSH Terms

Adult*
Epidemiology*
Humans
Incidence
Mortality
Pneumonia*
Population Characteristics
Prevalence
Vaccines, Conjugate*
Vaccines, Conjugate

Reference

1. Choi MJ, Song JY, Noh JY, Yoon JG, Lee SN, Heo JY, Yoon JW, Jo YM, Cheong HJ, Kim WJ. Disease burden of hospitalized community-acquired pneumonia in South Korea: Analysis based on age and underlying medical conditions. Medicine (Baltimore). 2017; 96:e8429.

2. Heo JY, Seo YB, Choi WS, Lee J, Yoon JG, Lee SN, Choi MJ, Noh JY, Ahn JY, Jeong HW, Cheong HJ, Kim WJ, Lee HY, Song JY. Incidence and case fatality rates of community-acquired pneumonia and pneumococcal diseases among Korean adults: Catchment population-based analysis. PLoS One. 2018; 13:e0194598.

3. American Thoracic Society. Infectious Diseases Society of America. Guidelines for the management of adults with hospital-acquired, ventilator-associated, and healthcare-associated pneumonia. Am J Respir Crit Care Med. 2005; 171:388–416.

4. Kalil AC, Metersky ML, Klompas M, Muscedere J, Sweeney DA, Palmer LB, Napolitano LM, O'Grady NP, Bartlett JG, Carratalà J, El Solh AA, Ewig S, Fey PD, File TM Jr., Restrepo MI, Roberts JA, Waterer GW, Cruse P, Knight SL, Brozek JL. Management of Adults With Hospital-acquired and Ventilator-associated Pneumonia: 2016 Clinical Practice Guidelines by the Infectious Diseases Society of America and the American Thoracic Society. Clin Infect Dis. 2016; 63:e61–e111.

5. Jeong BH, Koh WJ, Yoo H, Um SW, Suh GY, Chung MP, Kim H, Kwon OJ, Jeon K. Performances of prognostic scoring systems in patients with healthcare-associated pneumonia. Clin Infect Dis. 2013; 56:625–632.

6. Kamata K, Suzuki H, Kanemoto K, Tokuda Y, Shiotani S, Hirose Y, Suzuki M, Ishikawa H. Clinical evaluation of the need for carbapenems to treat community-acquired and healthcare-associated pneumonia. J Infect Chemother. 2015; 21:596–603.

7. Koh SJ, Lee JH. Clinical characteristics of nursing home-acquired pneumonia in elderly patients admitted to a Korean teaching hospital. Korean J Intern Med. 2015; 30:638–647.

8. Kosai K, Izumikawa K, Imamura Y, Tanaka H, Tsukamoto M, Kurihara S, Takazono T, Morinaga Y, Nakamura S, Miyazaki T, Yanagihara K, Tashiro T, Kohno S. Importance of functional assessment in the management of community-acquired and healthcare-associated pneumonia. Intern Med. 2014; 53:1613–1620.

9. Maruyama T, Fujisawa T, Okuno M, Toyoshima H, Tsutsui K, Maeda H, Yuda H, Yoshida M, Kobayashi H, Taguchi O, Gabazza EC, Takei Y, Miyashita N, Ihara T, Brito V, Niederman MS. A new strategy for healthcare-associated pneumonia: a 2-year prospective multicenter cohort study using risk factors for multidrug-resistant pathogens to select initial empiric therapy. Clin Infect Dis. 2013; 57:1373–1383.

10. Geno KA, Gilbert GL, Song JY, Skovsted IC, Klugman KP, Jones C, Konradsen HB, Nahm MH. Pneumococcal Capsules and Their Types: Past, Present, and Future. Clin Microbiol Rev. 2015; 28:871–899.

11. Bonten MJ, Huijts SM, Bolkenbaas M, Webber C, Patterson S, Gault S, van Werkhoven CH, van Deursen AM, Sanders EA, Verheij TJ, Patton M, McDonough A, Moradoghli-Haftvani A, Smith H, Mellelieu T, Pride MW, Crowther G, Schmoele-Thoma B, Scott DA, Jansen KU, Lobatto R, Oosterman B, Visser N, Caspers E, Smorenburg A, Emini EA, Gruber WC, Grobbee DE. Polysaccharide conjugate vaccine against pneumococcal pneumonia in adults. N Engl J Med. 2015; 372:1114–1125.

12. McLaughlin JM, Jiang Q, Isturiz RE, Sings HL, Swerdlow DL, Gessner BD, Carrico RM, Peyrani P, Wiemken TL, Mattingly WA, Ramirez JA, Jodar L. Effectiveness of 13-Valent Pneumococcal Conjugate Vaccine Against Hospitalization for Community-Acquired Pneumonia in Older US Adults: A Test-Negative Design. Clin Infect Dis. 2018; 67:1498–1506.

13. Gil-Prieto R, Garcìa-Garcìa L, Alvaro-Meca A, Méndez C, García A, de Miguel AG. The burden of hospitalisations for community-acquired pneumonia (CAP) and pneumococcal pneumonia in adults in Spain (2003-2007). Vaccine. 2011; 29:412–416.

14. Griffin MR, Zhu Y, Moore MR, Whitney CG, Grijalva CG. U.S. hospitalizations for pneumonia after a decade of pneumococcal vaccination. N Engl J Med. 2013; 369:155–163.

15. Gutiérrez F, Masiá M, Rodríguez JC, Mirete C, Soldán B, Padilla S, Hernández I, De Ory F, Royo G, Hidalgo AM. Epidemiology of community-acquired pneumonia in adult patients at the dawn of the 21st century: a prospective study on the Mediterranean coast of Spain. Clin Microbiol Infect. 2005; 11:788–800.

16. Jackson ML, Neuzil KM, Thompson WW, Shay DK, Yu O, Hanson CA, Jackson LA. The burden of community-acquired pneumonia in seniors: results of a population-based study. Clin Infect Dis. 2004; 39:1642–1650.

17. Jain S, Self WH, Wunderink RG, Fakhran S, Balk R, Bramley AM, Reed C, Grijalva CG, Anderson EJ, Courtney DM, Chappell JD, Qi C, Hart EM, Carroll F, Trabue C, Donnelly HK, Williams DJ, Zhu Y, Arnold SR, Ampofo K, Waterer GW, Levine M, Lindstrom S, Winchell JM, Katz JM, Erdman D, Schneider E, Hicks LA, McCullers JA, Pavia AT, Edwards KM, Finelli L, Team CE. CDC EPIC Study Team. Community-Acquired Pneumonia Requiring Hospitalization among U.S. Adults. N Engl J Med. 2015; 373:415–427.

18. Kaplan V, Angus DC, Griffin MF, Clermont G, Scott Watson R, Linde-Zwirble WT. Hospitalized community-acquired pneumonia in the elderly: age- and sex-related patterns of care and outcome in the United States. Am J Respir Crit Care Med. 2002; 165:766–772.

19. Lovering AM, MacGowan AP, Anderson P, Irwin D. Epidemiology and resource utilization for patients hospitalized for lower respiratory tract infection. Clin Microbiol Infect. 2001; 7:666–670.

20. Millett ER, Quint JK, Smeeth L, Daniel RM, Thomas SL. Incidence of community-acquired lower respiratory tract infections and pneumonia among older adults in the United Kingdom: a population-based study. PLoS One. 2013; 8:e75131.

21. Monge V, González A. Hospital admissions for pneumonia in Spain. Infection. 2001; 29:3–6.

22. Ochoa-Gondar O, Vila-Córcoles A, de Diego C, Arija V, Maxenchs M, Grive M, Martin E, Pinyol JL. EVAN-65 Study Group. The burden of community-acquired pneumonia in the elderly: the Spanish EVAN-65 study. BMC Public Health. 2008; 8:222.

23. Ramirez JA, Wiemken TL, Peyrani P, Arnold FW, Kelley R, Mattingly WA, Nakamatsu R, Pena S, Guinn BE, Furmanek SP, Persaud AK, Raghuram A, Fernandez F, Beavin L, Bosson R, Fernandez-Botran R, Cavallazzi R, Bordon J, Valdivieso C, Schulte J, Carrico RM. University of Louisville Pneumonia Study Group. Adults Hospitalized With Pneumonia in the United States: Incidence, Epidemiology, and Mortality. Clin Infect Dis. 2017; 65:1806–1812.

24. Sicras-Mainar A, Ibáñez-Nolla J, Cifuentes I, Guijarro P, Navarro-Artieda R, Aguilar L. Retrospective epidemiological study for the characterization of community- acquired pneumonia and pneumococcal pneumonia in adults in a well-defined area of Badalona (Barcelona, Spain). BMC Infect Dis. 2012; 12:283.

25. Simonsen L, Taylor RJ, Schuck-Paim C, Lustig R, Haber M, Klugman KP. Effect of 13-valent pneumococcal conjugate vaccine on admissions to hospital 2 years after its introduction in the USA: a time series analysis. Lancet Respir Med. 2014; 2:387–394.

26. Fitzwater SP, Chandran A, Santosham M, Johnson HL. The worldwide impact of the seven-valent pneumococcal conjugate vaccine. Pediatr Infect Dis J. 2012; 31:501–508.

27. Tsaban G, Ben-Shimol S. Indirect (herd) protection, following pneumococcal conjugated vaccines introduction: A systematic review of the literature. Vaccine. 2017; 35:2882–2891.

28. Lopardo GD, Fridman D, Raimondo E, Albornoz H, Lopardo A, Bagnulo H, Goleniuk D, Sanabria M, Stamboulian D. Incidence rate of community-acquired pneumonia in adults: a population-based prospective active surveillance study in three cities in South America. BMJ Open. 2018; 8:e019439.

29. Morimoto K, Suzuki M, Ishifuji T, Yaegashi M, Asoh N, Hamashige N, Abe M, Aoshima M, Ariyoshi K. Adult Pneumonia Study Group-Japan (APSG-J). The burden and etiology of community-onset pneumonia in the aging Japanese population: a multicenter prospective study. PLoS One. 2015; 10:e0122247.

30. Schnoor M, Hedicke J, Dalhoff K, Raspe H, Schäfer T. CAPNETZ study group. Approaches to estimate the population-based incidence of community acquired pneumonia. J Infect. 2007; 55:233–239.

31. Simonsen L, Taylor RJ, Young-Xu Y, Haber M, May L, Klugman KP. Impact of pneumococcal conjugate vaccination of infants on pneumonia and influenza hospitalization and mortality in all age groups in the United States. MBio. 2011; 2:e00309–10.

32. Takaki M, Nakama T, Ishida M, Morimoto H, Nagasaki Y, Shiramizu R, Hamashige N, Chikamori M, Yoshida L, Ariyoshi K, Suzuki M, Morimoto K. High incidence of community-acquired pneumonia among rapidly aging population in Japan: a prospective hospital-based surveillance. Jpn J Infect Dis. 2014; 67:269–275.

33. Vila-Corcoles A, Ochoa-Gondar O, Rodriguez-Blanco T, Raga-Luria X, Gomez-Bertomeu F. EPIVAC Study Group. Epidemiology of community-acquired pneumonia in older adults: a population-based study. Respir Med. 2009; 103:309–316.

34. Grijalva CG, Nuorti JP, Arbogast PG, Martin SW, Edwards KM, Griffin MR. Decline in pneumonia admissions after routine childhood immunisation with pneumococcal conjugate vaccine in the USA: a time-series analysis. Lancet. 2007; 369:1179–1186.

35. Welte T, Köhnlein T. Global and local epidemiology of community-acquired pneumonia: the experience of the CAPNETZ Network. Semin Respir Crit Care Med. 2009; 30:127–135.

36. Welte T, Torres A, Nathwani D. Clinical and economic burden of community-acquired pneumonia among adults in Europe. Thorax. 2012; 67:71–79.

37. Arnold FW, Wiemken TL, Peyrani P, Ramirez JA, Brock GN. Mortality differences among hospitalized patients with community-acquired pneumonia in three world regions: results from the Community-Acquired Pneumonia Organization (CAPO) International Cohort Study. Respir Med. 2013; 107:1101–1111.

38. Anevlavis S, Bouros D. Community acquired bacterial pneumonia. Expert Opin Pharmacother. 2010; 11:361–374.

39. Chung MH, Shin WS, Kim YR, Kang MW, Kim MJ, Jung HJ, Park SC, Pai H, Choi HJ, Shin HS, Kim EC, Choe KW, Kim S, Peck KR, Song JH, Lee K, Kim JM, Chong Y, Han SW, Lee KM. Etiology of communityacquired pneumonia surveyed by 7 university hospitals. Korean J Infect Dis. 1997; 29:339–359.

40. Sohn JW, Park SC, Choi YH, Woo HJ, Cho YK, Lee JS, Sim HS, Kim MJ. Atypical pathogens as etiologic agents in hospitalized patients with community-acquired pneumonia in Korea: a prospective multi-center study. J Korean Med Sci. 2006; 21:602–607.

41. Song JH, Oh WS, Kang CI, Chung DR, Peck KR, Ko KS, Yeom JS, Kim CK, Kim SW, Chang HH, Kim YS, Jung SI, Tong Z, Wang Q, Huang SG, Liu JW, Lalitha MK, Tan BH, Van PH, Carlos CC, So T. Asian Network for Surveillance of Resistant Pathogens Study Group. Epidemiology and clinical outcomes of community-acquired pneumonia in adult patients in Asian countries: a prospective study by the Asian network for surveillance of resistant pathogens. Int J Antimicrob Agents. 2008; 31:107–114.

42. Woo JH, Kang JM, Kim YS, Shin WS, Ryu JH, Choi JH, Kim YR, Cheong HJ, Uh ST, Park CS, Chung MH, Chung KS, Lee CJ, Ryu J. A prospective multicenter study of community-acquired pneumonia in adults with emphasis on bacterial etiology. Korean J Infect Dis. 2001; 33:1–7.

43. Yu CW, Park CW, Hwang BY, Song JY, Park O, Sohn JW, Cheong HJ, Kim WJ, Kim MJ, Park SC. Clinical Features and Prognosis of Community-acquired Pneumonia in the Elderly Patients. Korean J Infect Dis. 2000; 32:212–218.

44. Ahn JH, Lee KH, Chung JH, Shin KC, Lee CK, Kim HJ, Choi EY. Clinical characteristics and prognostic risk factors of healthcare-associated pneumonia in a Korean tertiary teaching hospital. Medicine (Baltimore). 2017; 96:e8243.

45. Kim ES, Park KU, Lee SH, Lee YJ, Park JS, Cho YJ, Yoon HI, Lee CT, Lee JH. Comparison of viral infection in healthcare-associated pneumonia (HCAP) and community-acquired pneumonia (CAP). PLoS One. 2018; 13:e0192893.

46. Lee H, Park JY, Lee T, Lee YJ, Lim HJ, Park JS, Yoon HI, Lee JH, Lee CT, Cho YJ. Intermediate risk of multidrug-resistant organisms in patients who admitted intensive care unit with healthcare-associated pneumonia. Korean J Intern Med. 2016; 31:525–534.

47. Seo H, Cha SI, Shin KM, Lim JK, Yoo SS, Lee SY, Lee J, Kim CH, Park JY. Relationship Between Clinical Features and Computed Tomographic Findings in Hospitalized Adult Patients With Community-Acquired Pneumonia. Am J Med Sci. 2018; 356:30–38.

48. Lee MS, Oh JY, Kang CI, Kim ES, Park S, Rhee CK, Jung JY, Jo KW, Heo EY, Park DA, Suh GY, Kiem S. Guideline for Antibiotic Use in Adults with Community-acquired Pneumonia. Infect Chemother. 2018; 50:160–198.

49. Kang YS, Ryoo SR, Byun SJ, Jeong YJ, Oh JY, Yoon YS. Antimicrobial Resistance and Clinical Outcomes in Nursing Home-Acquired Pneumonia, Compared to Community-Acquired Pneumonia. Yonsei Med J. 2017; 58:180–186.

50. Ladhani SN, Collins S, Djennad A, Sheppard CL, Borrow R, Fry NK, Andrews NJ, Miller E, Ramsay ME. Rapid increase in non-vaccine serotypes causing invasive pneumococcal disease in England and Wales, 2000-17: a prospective national observational cohort study. Lancet Infect Dis. 2018; 18:441–451.

51. Pelton SI, Bornheimer R, Doroff R, Shea KM, Sato R, Weycker D. Decline in Pneumococcal Disease Attenuated in Older Adults and Those with Comorbidities Following Universal Childhood PCV13 Immunization. Clin Infect Dis. 2018.

52. Choi MJ, Song JY, Cheong HJ, Jeon JH, Kang SH, Jung EJ, Noh JY, Kim WJ. Clinical usefulness of pneumococcal urinary antigen test, stratified by disease severity and serotypes. J Infect Chemother. 2015; 21:672–679.

53. Chong YP, Jung KS, Lee KH, Kim MN, Moon SM, Park S, Hur J, Kim DM, Jeon MH, Woo JH. The bacterial etiology of community-acquired pneumonia in Korea: A nationwide prospective multicenter study. Infect Chemother. 2010; 42:397–403.

54. Jeon EJ, Cho SG, Shin JW, Kim JY, Park IW, Choi BW, Choi JC. The difference in clinical presentations between healthcare-associated and community-acquired pneumonia in university-affiliated hospital in Korea. Yonsei Med J. 2011; 52:282–287.

55. Seong GM, Kim M, Lee J, Lee JH, Jeong SY, Choi Y, Kim WJ. Healthcare-Associated Pneumonia among Hospitalized Patients: Is It Different from Community Acquired Pneumonia? Tuberc Respir Dis (Seoul). 2014; 76:66–74.

56. Yoo KH, Yoo CG, Kim SK, Jung JY, Lee MG, Uh ST, Shim TS, Jeon K, Shim JJ, Lee HB, Chung CR, Kang KW, Jung KS. Economic burden and epidemiology of pneumonia in Korean adults aged over 50 years. J Korean Med Sci. 2013; 28:888–895.

57. Pilishvili T, Lexau C, Farley MM, Hadler J, Harrison LH, Bennett NM, Reingold A, Thomas A, Schaffner W, Craig AS, Smith PJ, Beall BW, Whitney CG, Moore MR. Active Bacterial Core Surveillance/Emerging Infections Program Network. Sustained reductions in invasive pneumococcal disease in the era of conjugate vaccine. J Infect Dis. 2010; 201:32–41.

58. Klugman KP. Herd protection induced by pneumococcal conjugate vaccine. Lancet Glob Health. 2014; 2:e365–6.

59. Kollef MH, Shorr A, Tabak YP, Gupta V, Liu LZ, Johannes RS. Epidemiology and outcomes of health-care-associated pneumonia: results from a large US database of culture-positive pneumonia. Chest. 2005; 128:3854–3862.

60. Micek ST, Kollef KE, Reichley RM, Roubinian N, Kollef MH. Health care-associated pneumonia and community-acquired pneumonia: a single-center experience. Antimicrob Agents Chemother. 2007; 51:3568–3573.

61. Fukuyama H, Yamashiro S, Kinjo K, Tamaki H, Kishaba T. Validation of sputum Gram stain for treatment of community-acquired pneumonia and healthcare-associated pneumonia: a prospective observational study. BMC Infect Dis. 2014; 14:534.

62. Ishida T, Tachibana H, Ito A, Yoshioka H, Arita M, Hashimoto T. Clinical characteristics of nursing and healthcare-associated pneumonia: a Japanese variant of healthcare-associated pneumonia. Intern Med. 2012; 51:2537–2544.

63. Parrott G, Nebeya D, Kinjo T, Miyagi K, Haranaga S, Higa F, Tateyama M, Fujita J. Etiological analysis and epidemiological comparison among adult CAP and NHCAP patients in Okinawa, Japan. J Infect Chemother. 2017; 23:452–458.

64. Polverino E, Torres A, Menendez R, Cillóniz C, Valles JM, Capelastegui A, Marcos MA, Alfageme I, Zalacain R, Almirall J, Molinos L, Bello S, Rodríguez F, Blanquer J, Dorado A, Llevat N, Rello J. HCAP Study investigators. Microbial aetiology of healthcare associated pneumonia in Spain: a prospective, multicentre, case-control study. Thorax. 2013; 68:1007–1014.

65. Vallés J, Martin-Loeches I, Torres A, Diaz E, Seijas I, López MJ, Garro P, Castillo C, Garnacho-Montero J, Martin MM, de la Torre MV, Olaechea P, Cilloniz C, Almirall J, García F, Jiménez R, Seoane E, Soriano C, Mesalles E, Posada P. Epidemiology, antibiotic therapy and clinical outcomes of healthcare-associated pneumonia in critically ill patients: a Spanish cohort study. Intensive Care Med. 2014; 40:572–581.

66. Chalmers JD, Rother C, Salih W, Ewig S. Healthcare-associated pneumonia does not accurately identify potentially resistant pathogens: a systematic review and meta-analysis. Clin Infect Dis. 2014; 58:330–339.

67. Chen JI, Slater LN, Kurdgelashvili G, Husain KO, Gentry CA. Outcomes of health care-associated pneumonia empirically treated with guideline-concordant regimens versus community-acquired pneumonia guideline-concordant regimens for patients admitted to acute care wards from home. Ann Pharmacother. 2013; 47:9–19.

68. Webb BJ, Dangerfield BS, Pasha JS, Agrwal N, Vikram HR. Guideline-concordant antibiotic therapy and clinical outcomes in healthcare-associated pneumonia. Respir Med. 2012; 106:1606–1612.

69. Grenier C, Pépin J, Nault V, Howson J, Fournier X, Poirier MS, Cabana J, Craig C, Beaudoin M, Valiquette L. Impact of guideline-consistent therapy on outcome of patients with healthcare-associated and community-acquired pneumonia. J Antimicrob Chemother. 2011; 66:1617–1624.

70. Yang TU, Song JY, Noh JY, Cheong HJ, Kim WJ. Influenza and Pneumococcal Vaccine Coverage Rates among Patients Admitted to a Teaching Hospital in South Korea. Infect Chemother. 2015; 47:41–48.

71. Tan CG, Ostrawski S, Bresnitz EA. A preventable outbreak of pneumococcal pneumonia among unvaccinated nursing home residents in New Jersey during 2001. Infect Control Hosp Epidemiol. 2003; 24:848–852.

72. Nuorti JP, Butler JC, Crutcher JM, Guevara R, Welch D, Holder P, Elliott JA. An outbreak of multidrug-resistant pneumococcal pneumonia and bacteremia among unvaccinated nursing home residents. N Engl J Med. 1998; 338:1861–1868.

73. Baek JY, Kang CI, Kim SH, Ko KS, Chung DR, Peck KR, Lee NY, Song JH. Emergence of multidrug-resistant clones in levofloxacin-nonsusceptible Streptococcus pneumoniae isolates in Korea. Diagn Microbiol Infect Dis. 2018; 91:287–290.

74. Choi MJ, Noh JY, Cheong HJ, Kim WJ, Kim MJ, Jang YS, Song JY. Spread of ceftriaxone non-susceptible pneumococci in South Korea: Long-term care facilities as a potential reservoir. PLoS One. 2018; [In press].

75. Park M, Kim HS, Kim HS, Park JY, Song W, Cho HC, Kim JS. Novel Levofloxacin-Resistant Multidrug-Resistant Streptococcus pneumoniae Serotype 11A Isolates, South Korea. Emerg Infect Dis. 2016; 22:1978–1980.