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Published in: BMC Medicine 1/2014

Open Access 01-12-2014 | Research article

Classification of healthcare-associated infection: a systematic review 10 years after the first proposal

Authors: Teresa Cardoso, Mónica Almeida, N Deborah Friedman, Irene Aragão, Altamiro Costa-Pereira, António E Sarmento, Luís Azevedo

Published in: BMC Medicine | Issue 1/2014

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Abstract

Background

Ten years after the first proposal, a consensus definition of healthcare-associated infection (HCAI) has not been reached, preventing the development of specific treatment recommendations. A systematic review of all definitions of HCAI used in clinical studies is made.

Methods

The search strategy focused on an HCAI definition. MEDLINE, SCOPUS and ISI Web of Knowledge were searched for articles published from earliest achievable data until November 2012. Abstracts from scientific meetings were searched for relevant abstracts along with a manual search of references from reports, earlier reviews and retrieved studies.

Results

The search retrieved 49,405 references: 15,311 were duplicates and 33,828 were excluded based on title and abstract. Of the remaining 266, 43 met the inclusion criteria. The definition more frequently used was the initial proposed in 2002 - an infection present at hospital admission or within 48 hours of admission in patients that fulfilled any of the following criteria: received intravenous therapy at home, wound care or specialized nursing care in the previous 30 days; attended a hospital or hemodialysis clinic or received intravenous chemotherapy in the previous 30 days; were hospitalized in an acute care hospital for ≥2 days in the previous 90 days, resided in a nursing home or long-term care facility. Additional criteria founded in other studies were: immunosuppression, active or metastatic cancer, previous radiation therapy, transfer from another care facility, elderly or physically disabled persons who need healthcare, previous submission to invasive procedures, surgery performed in the last 180 days, family member with a multi-drug resistant microorganism and recent treatment with antibiotics.

Conclusions

Based on the evidence gathered we conclude that the definition initially proposed is widely accepted. In a future revision, recent invasive procedures, hospitalization in the last year or previous antibiotic treatment should be considered for inclusion in the definition. The role of immunosuppression in the definition of HCAI still requires ongoing discussion.
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Literature
1.
go back to reference Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM: CDC definitions for nosocomial infections, 1988. Am J Infect Control. 1988, 16: 128-140. 10.1016/0196-6553(88)90053-3.CrossRefPubMed Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM: CDC definitions for nosocomial infections, 1988. Am J Infect Control. 1988, 16: 128-140. 10.1016/0196-6553(88)90053-3.CrossRefPubMed
2.
go back to reference 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.CrossRef 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.CrossRef
3.
go back to reference Friedman ND, Kaye KS, Stout JE, McGarry SA, Trivette SL, Briggs JP, Lamm W, Clark C, MacFarquhar J, Walton AL, Reller LB, Sexton DJ: Health care-associated bloodstream infections in adults: a reason to change the accepted definition of community-acquired infections. Ann Intern Med. 2002, 137: 791-797. 10.7326/0003-4819-137-10-200211190-00007.CrossRefPubMed Friedman ND, Kaye KS, Stout JE, McGarry SA, Trivette SL, Briggs JP, Lamm W, Clark C, MacFarquhar J, Walton AL, Reller LB, Sexton DJ: Health care-associated bloodstream infections in adults: a reason to change the accepted definition of community-acquired infections. Ann Intern Med. 2002, 137: 791-797. 10.7326/0003-4819-137-10-200211190-00007.CrossRefPubMed
4.
go back to reference Park SC, Kang YA, Park BH, Kim EY, Park MS, Kim YS, Kim SK, Chang J, Jung JY: Poor prediction of potentially drug-resistant pathogens using current criteria of health care-associated pneumonia. Respir Med. 2012, 106: 1311-1319. 10.1016/j.rmed.2012.04.003.CrossRefPubMed Park SC, Kang YA, Park BH, Kim EY, Park MS, Kim YS, Kim SK, Chang J, Jung JY: Poor prediction of potentially drug-resistant pathogens using current criteria of health care-associated pneumonia. Respir Med. 2012, 106: 1311-1319. 10.1016/j.rmed.2012.04.003.CrossRefPubMed
5.
go back to reference Benito N, Miró JM, de Lazzari E, Cabell CH, del Río A, Altclas J, Commerford P, Delahaye F, Dragulescu S, Giamarellou H, Habib G, Kamarulzaman A, Kumar AS, Nacinovich FM, Suter F, Tribouilloy C, Venugopal K, Moreno A, Fowler VG, ICE-PCS (International Collaboration on Endocarditis Prospective Cohort Study) Investigators: Health care-associated native valve endocarditis: importance of non-nosocomial acquisition. Ann Intern Med. 2009, 150: 586-594. 10.7326/0003-4819-150-9-200905050-00004. Erratum in: Ann Intern Med 2010, 152:480CrossRefPubMedPubMedCentral Benito N, Miró JM, de Lazzari E, Cabell CH, del Río A, Altclas J, Commerford P, Delahaye F, Dragulescu S, Giamarellou H, Habib G, Kamarulzaman A, Kumar AS, Nacinovich FM, Suter F, Tribouilloy C, Venugopal K, Moreno A, Fowler VG, ICE-PCS (International Collaboration on Endocarditis Prospective Cohort Study) Investigators: Health care-associated native valve endocarditis: importance of non-nosocomial acquisition. Ann Intern Med. 2009, 150: 586-594. 10.7326/0003-4819-150-9-200905050-00004. Erratum in: Ann Intern Med 2010, 152:480CrossRefPubMedPubMedCentral
6.
go back to reference Aguilar-Duran S, Horcajada JP, Sorlí L, Montero M, Salvadó M, Grau S, Gómez J, Knobel H: Community-onset healthcare-related urinary tract infections: comparison with community and hospital-acquired urinary tract infections. J Infect. 2012, 64: 478-483. 10.1016/j.jinf.2012.01.010.CrossRefPubMed Aguilar-Duran S, Horcajada JP, Sorlí L, Montero M, Salvadó M, Grau S, Gómez J, Knobel H: Community-onset healthcare-related urinary tract infections: comparison with community and hospital-acquired urinary tract infections. J Infect. 2012, 64: 478-483. 10.1016/j.jinf.2012.01.010.CrossRefPubMed
7.
go back to reference Siegman-Igra Y, Fourer B, Orni-Wasserlauf R, Golan Y, Noy A, Schwartz D, Giladi M: Reappraisal of community-acquired bacteremia: a proposal of a new classification for the spectrum of acquisition of bacteremia. Clin Infect Dis. 2002, 34: 1431-1439. 10.1086/339809.CrossRefPubMed Siegman-Igra Y, Fourer B, Orni-Wasserlauf R, Golan Y, Noy A, Schwartz D, Giladi M: Reappraisal of community-acquired bacteremia: a proposal of a new classification for the spectrum of acquisition of bacteremia. Clin Infect Dis. 2002, 34: 1431-1439. 10.1086/339809.CrossRefPubMed
8.
go back to reference Vallés J, Alvarez-Lerma F, Palomar M, Blanco A, Escoresca A, Armestar F, Sirvent JM, Balasini C, Zaragoza R, Marín M, Study Group of Infectious Diseases of the Spanish Society of Critical Care Medicine: Health-care-associated bloodstream infections at admission to the ICU. Chest. 2011, 139: 810-815. 10.1378/chest.10-1715.CrossRefPubMed Vallés J, Alvarez-Lerma F, Palomar M, Blanco A, Escoresca A, Armestar F, Sirvent JM, Balasini C, Zaragoza R, Marín M, Study Group of Infectious Diseases of the Spanish Society of Critical Care Medicine: Health-care-associated bloodstream infections at admission to the ICU. Chest. 2011, 139: 810-815. 10.1378/chest.10-1715.CrossRefPubMed
9.
go back to reference Park HK, Song J-U, Um S-W, Koh W-J, Suh GY, Chung MP, Kim H, Kwon OJ, Jeon K: Clinical characteristics of health care-associated pneumonia in a Korean teaching hospital. Respir Med. 2010, 104: 1729-1735. 10.1016/j.rmed.2010.06.009.CrossRefPubMed Park HK, Song J-U, Um S-W, Koh W-J, Suh GY, Chung MP, Kim H, Kwon OJ, Jeon K: Clinical characteristics of health care-associated pneumonia in a Korean teaching hospital. Respir Med. 2010, 104: 1729-1735. 10.1016/j.rmed.2010.06.009.CrossRefPubMed
10.
go back to reference Carratalà J, Mykietiuk A, Fernández-Sabé N, Suárez C, Dorca J, Verdaguer R, Manresa F, Gudiol F: Health care-associated pneumonia requiring hospital admission: epidemiology, antibiotic therapy, and clinical outcomes. Arch Intern Med. 2007, 167: 1393-1399. 10.1001/archinte.167.13.1393.CrossRefPubMed Carratalà J, Mykietiuk A, Fernández-Sabé N, Suárez C, Dorca J, Verdaguer R, Manresa F, Gudiol F: Health care-associated pneumonia requiring hospital admission: epidemiology, antibiotic therapy, and clinical outcomes. Arch Intern Med. 2007, 167: 1393-1399. 10.1001/archinte.167.13.1393.CrossRefPubMed
11.
go back to reference Shorr AF, Tabak YP, Killian AD, Gupta V, Liu LZ, Kollef MH: Healthcare-associated bloodstream infection: a distinct entity? Insights from a large US database. Crit Care Med. 2006, 34: 2588-2595. 10.1097/01.CCM.0000239121.09533.09.CrossRefPubMed Shorr AF, Tabak YP, Killian AD, Gupta V, Liu LZ, Kollef MH: Healthcare-associated bloodstream infection: a distinct entity? Insights from a large US database. Crit Care Med. 2006, 34: 2588-2595. 10.1097/01.CCM.0000239121.09533.09.CrossRefPubMed
12.
go back to reference Kollef MH, Zilberberg MD, Shorr AF, Vo L, Schein J, Micek ST, Kim M: Epidemiology, microbiology and outcomes of healthcare-associated and community-acquired bacteremia: a multicenter cohort study. J Infect. 2011, 62: 130-135. 10.1016/j.jinf.2010.12.009.CrossRefPubMed Kollef MH, Zilberberg MD, Shorr AF, Vo L, Schein J, Micek ST, Kim M: Epidemiology, microbiology and outcomes of healthcare-associated and community-acquired bacteremia: a multicenter cohort study. J Infect. 2011, 62: 130-135. 10.1016/j.jinf.2010.12.009.CrossRefPubMed
13.
go back to reference Kollef MH, Shorr A, Tabak YP, Gupta V, Liu LZ, Johannes RS: Epidemiology and outcomes of healthcare-associated pneumonia: results from a large US database of culture-positive pneumonia. Chest. 2005, 128: 3854-3862. 10.1378/chest.128.6.3854. Erratum in Chest 2006, 129:831CrossRefPubMed Kollef MH, Shorr A, Tabak YP, Gupta V, Liu LZ, Johannes RS: Epidemiology and outcomes of healthcare-associated pneumonia: results from a large US database of culture-positive pneumonia. Chest. 2005, 128: 3854-3862. 10.1378/chest.128.6.3854. Erratum in Chest 2006, 129:831CrossRefPubMed
14.
go back to reference Grenier C, Pepin J, Nault V, Howson J, Fournier X, Poirier M-S, 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. 10.1093/jac/dkr176.CrossRefPubMed Grenier C, Pepin J, Nault V, Howson J, Fournier X, Poirier M-S, 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. 10.1093/jac/dkr176.CrossRefPubMed
15.
go back to reference Pop-Vicas AE, D’Agata EM: The rising influx of multidrug-resistant gram-negative bacilli into a tertiary care hospital. Clin Infect Dis. 2005, 40: 1792-1798. 10.1086/430314.CrossRefPubMed Pop-Vicas AE, D’Agata EM: The rising influx of multidrug-resistant gram-negative bacilli into a tertiary care hospital. Clin Infect Dis. 2005, 40: 1792-1798. 10.1086/430314.CrossRefPubMed
16.
go back to reference Marschall J, Fraser VJ, Doherty J, Warren DK: Between community and hospital: healthcare-associated gram-negative bacteremia among hospitalized patients. Infect Control Hosp Epidemiol. 2009, 30: 1050-1056. 10.1086/606165.CrossRefPubMed Marschall J, Fraser VJ, Doherty J, Warren DK: Between community and hospital: healthcare-associated gram-negative bacteremia among hospitalized patients. Infect Control Hosp Epidemiol. 2009, 30: 1050-1056. 10.1086/606165.CrossRefPubMed
17.
go back to reference Evans CT, Hershow RC, Chin A, Foulis PR, Burns SP, Weaver FM: Bloodstream infections and setting of onset in persons with spinal cord injury and disorder. Spinal Cord. 2009, 47: 610-615. 10.1038/sc.2009.2.CrossRefPubMed Evans CT, Hershow RC, Chin A, Foulis PR, Burns SP, Weaver FM: Bloodstream infections and setting of onset in persons with spinal cord injury and disorder. Spinal Cord. 2009, 47: 610-615. 10.1038/sc.2009.2.CrossRefPubMed
18.
go back to reference Son JS, Song J-H, Ko KS, Yeom JS, Ki HK, Kim S-W, Chang H-H, Ryu SY, Kim Y-S, Jung S-I, Shin SY, Oh HB, Lee YS, Chung DR, Lee NY, Peck KR: Bloodstream infections and clinical significance of healthcare-associated bacteremia: a multicenter surveillance study in Korean hospitals. J Korean Med Sci. 2010, 25: 992-998. 10.3346/jkms.2010.25.7.992.CrossRefPubMedPubMedCentral Son JS, Song J-H, Ko KS, Yeom JS, Ki HK, Kim S-W, Chang H-H, Ryu SY, Kim Y-S, Jung S-I, Shin SY, Oh HB, Lee YS, Chung DR, Lee NY, Peck KR: Bloodstream infections and clinical significance of healthcare-associated bacteremia: a multicenter surveillance study in Korean hospitals. J Korean Med Sci. 2010, 25: 992-998. 10.3346/jkms.2010.25.7.992.CrossRefPubMedPubMedCentral
19.
go back to reference Rodríguez-Baño J, López-Prieto MD, Portillo MM, Retamar P, Natera C, Nuño E, Herrero M, del Arco A, Muñoz A, Téllez F, Torres-Tortosa M, Martín-Aspas A, Arroyo A, Ruiz A, Moya R, Corzo JE, León L, Pérez-López JA, SAEI/SAMPAC Bacteraemia Group: Epidemiology and clinical features of community-acquired, healthcare-associated and nosocomial bloodstream infections in tertiary-care and community hospitals. Clin Microbiol Infect. 2010, 16: 1408-1413. 10.1111/j.1469-0691.2010.03089.x.CrossRefPubMed Rodríguez-Baño J, López-Prieto MD, Portillo MM, Retamar P, Natera C, Nuño E, Herrero M, del Arco A, Muñoz A, Téllez F, Torres-Tortosa M, Martín-Aspas A, Arroyo A, Ruiz A, Moya R, Corzo JE, León L, Pérez-López JA, SAEI/SAMPAC Bacteraemia Group: Epidemiology and clinical features of community-acquired, healthcare-associated and nosocomial bloodstream infections in tertiary-care and community hospitals. Clin Microbiol Infect. 2010, 16: 1408-1413. 10.1111/j.1469-0691.2010.03089.x.CrossRefPubMed
20.
go back to reference Shindo Y, Sato S, Maruyama E, Ohashi T, Ogawa M, Hashimoto N, Imaizumi K, Sato T, Hasegawa Y: Health-care-associated pneumonia among hospitalized patients in a Japanese Community Hospital. Chest. 2009, 135: 633-640. 10.1378/chest.08-1357.CrossRefPubMed Shindo Y, Sato S, Maruyama E, Ohashi T, Ogawa M, Hashimoto N, Imaizumi K, Sato T, Hasegawa Y: Health-care-associated pneumonia among hospitalized patients in a Japanese Community Hospital. Chest. 2009, 135: 633-640. 10.1378/chest.08-1357.CrossRefPubMed
21.
go back to reference Pascual V, Salvador M, Calvo E, Freixas N, Riera M, Xercavins M, Garau J: Healthcare-associated pneumonia: a category under review. Abstr Intersci Conf Antimicrob Agents Chemother. 2010, 50: P1658. Pascual V, Salvador M, Calvo E, Freixas N, Riera M, Xercavins M, Garau J: Healthcare-associated pneumonia: a category under review. Abstr Intersci Conf Antimicrob Agents Chemother. 2010, 50: P1658.
22.
go back to reference Umeki K, Tokimatsu I, Yasuda C, Iwata A, Yoshioka D, Ishii H, Shirai R, Kishi K, Hiramatsu K, Matsumoto B, Kadota J: Clinical features of healthcare-associated pneumonia (HCAP) in a Japanese community hospital: comparisons among nursing home-acquired pneumonia (NHAP), HCAP other than NHAP, and community-acquired pneumonia. Respirology. 2011, 16: 856-861. 10.1111/j.1440-1843.2011.01983.x.CrossRefPubMed Umeki K, Tokimatsu I, Yasuda C, Iwata A, Yoshioka D, Ishii H, Shirai R, Kishi K, Hiramatsu K, Matsumoto B, Kadota J: Clinical features of healthcare-associated pneumonia (HCAP) in a Japanese community hospital: comparisons among nursing home-acquired pneumonia (NHAP), HCAP other than NHAP, and community-acquired pneumonia. Respirology. 2011, 16: 856-861. 10.1111/j.1440-1843.2011.01983.x.CrossRefPubMed
23.
go back to reference Seki M, Hashiguchi K, Tanaka A, Kosai K, Kakugawa T, Awaya Y, Kurihara S, Izumikawa K, Kakeya H, Yamamoto Y, Yanagihara K, Tashiro T, Kohno S: Characteristics and disease severity of healthcare-associated pneumonia among patients in a hospital in Kitakyushu, Japan. J Infect Chemother. 2011, 17: 363-369. 10.1007/s10156-010-0127-8.CrossRefPubMed Seki M, Hashiguchi K, Tanaka A, Kosai K, Kakugawa T, Awaya Y, Kurihara S, Izumikawa K, Kakeya H, Yamamoto Y, Yanagihara K, Tashiro T, Kohno S: Characteristics and disease severity of healthcare-associated pneumonia among patients in a hospital in Kitakyushu, Japan. J Infect Chemother. 2011, 17: 363-369. 10.1007/s10156-010-0127-8.CrossRefPubMed
24.
go back to reference Garcia-Vidal C, Viasus D, Roset A, Adamuz J, Verdaguer R, Dorca J, Gudiol F, Carratalà J: Low incidence of multidrug-resistant organisms in patients with healthcare-associated pneumonia requiring hospitalization. Clin Microbiol Infect. 2011, 17: 1659-1665. 10.1111/j.1469-0691.2011.03484.x.CrossRefPubMed Garcia-Vidal C, Viasus D, Roset A, Adamuz J, Verdaguer R, Dorca J, Gudiol F, Carratalà J: Low incidence of multidrug-resistant organisms in patients with healthcare-associated pneumonia requiring hospitalization. Clin Microbiol Infect. 2011, 17: 1659-1665. 10.1111/j.1469-0691.2011.03484.x.CrossRefPubMed
25.
go back to reference Jung JY, Park MS, Kim YS, Park BH, Kim SK, Chang J, Kang YA: Healthcare-associated pneumonia among hospitalized patients in a Korean tertiary hospital. BMC Infect Dis. 2011, 11: 61-10.1186/1471-2334-11-61. doi:10.1186/1471-2334-11-61CrossRefPubMedPubMedCentral Jung JY, Park MS, Kim YS, Park BH, Kim SK, Chang J, Kang YA: Healthcare-associated pneumonia among hospitalized patients in a Korean tertiary hospital. BMC Infect Dis. 2011, 11: 61-10.1186/1471-2334-11-61. doi:10.1186/1471-2334-11-61CrossRefPubMedPubMedCentral
26.
go back to reference Jeon EJ, Cho S-G, 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. 10.3349/ymj.2011.52.2.282.CrossRefPubMedPubMedCentral Jeon EJ, Cho S-G, 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. 10.3349/ymj.2011.52.2.282.CrossRefPubMedPubMedCentral
27.
go back to reference Depuydt P, Putman B, Benoit D, Buylaert W, De Paepe P: Nursing home residence is the main risk factor for increased mortality in healthcare-associated pneumonia. J Hosp Infect. 2011, 77: 138-142. 10.1016/j.jhin.2010.09.031.CrossRefPubMed Depuydt P, Putman B, Benoit D, Buylaert W, De Paepe P: Nursing home residence is the main risk factor for increased mortality in healthcare-associated pneumonia. J Hosp Infect. 2011, 77: 138-142. 10.1016/j.jhin.2010.09.031.CrossRefPubMed
28.
go back to reference Lee JH, Kim YH: Comparison of clinical characteristics between healthcare-associated pneumonia and community-acquired pneumonia in patients admitted to secondary hospitals. Braz J Infect Dis. 2012, 16: 321-328. 10.1016/j.bjid.2012.06.019.CrossRef Lee JH, Kim YH: Comparison of clinical characteristics between healthcare-associated pneumonia and community-acquired pneumonia in patients admitted to secondary hospitals. Braz J Infect Dis. 2012, 16: 321-328. 10.1016/j.bjid.2012.06.019.CrossRef
29.
go back to reference Wu KS, Lee SS, Tsai HC, Wann SR, Chen JK, Sy CL, Wang YH, Tseng YT, Chen YS: Non-nosocomial healthcare-associated infective endocarditis in Taiwan: an underrecognized disease with poor outcome. BMC Infect Dis. 2011, 11: 221-10.1186/1471-2334-11-221. doi:10.1186/1471-2334-11-221CrossRefPubMedPubMedCentral Wu KS, Lee SS, Tsai HC, Wann SR, Chen JK, Sy CL, Wang YH, Tseng YT, Chen YS: Non-nosocomial healthcare-associated infective endocarditis in Taiwan: an underrecognized disease with poor outcome. BMC Infect Dis. 2011, 11: 221-10.1186/1471-2334-11-221. doi:10.1186/1471-2334-11-221CrossRefPubMedPubMedCentral
30.
go back to reference Kao CH, Kuo YC, Chen CC, Chang YT, Chen YS, Wann SR, Liu YC: Isolated pathogens and clinical outcomes of adult bacteremia in the emergency department: a retrospective study in a tertiary referral center. J Microbiol Immunol Infect. 2011, 44: 215-221. 10.1016/j.jmii.2011.01.023.CrossRefPubMed Kao CH, Kuo YC, Chen CC, Chang YT, Chen YS, Wann SR, Liu YC: Isolated pathogens and clinical outcomes of adult bacteremia in the emergency department: a retrospective study in a tertiary referral center. J Microbiol Immunol Infect. 2011, 44: 215-221. 10.1016/j.jmii.2011.01.023.CrossRefPubMed
31.
go back to reference Al-Hasan MN, Eckel-Passow JE, Baddour LM: Impact of healthcare-associated acquisition on community-onset Gram-negative bloodstream infection: a population-based study: healthcare-associated Gram-negative BSI. Eur J Clin Microbiol Infect Dis. 2012, 31: 1163-1171. 10.1007/s10096-011-1424-6.CrossRefPubMed Al-Hasan MN, Eckel-Passow JE, Baddour LM: Impact of healthcare-associated acquisition on community-onset Gram-negative bloodstream infection: a population-based study: healthcare-associated Gram-negative BSI. Eur J Clin Microbiol Infect Dis. 2012, 31: 1163-1171. 10.1007/s10096-011-1424-6.CrossRefPubMed
32.
go back to reference Lenz R, Leal JR, Church DL, Gregson DB, Ross T, Laupland KB: The distinct category of healthcare associated bloodstream infections. BMC Infect Dis. 2012, 12: 85-10.1186/1471-2334-12-85. doi:10.1186/1471-2334-12-85CrossRefPubMedPubMedCentral Lenz R, Leal JR, Church DL, Gregson DB, Ross T, Laupland KB: The distinct category of healthcare associated bloodstream infections. BMC Infect Dis. 2012, 12: 85-10.1186/1471-2334-12-85. doi:10.1186/1471-2334-12-85CrossRefPubMedPubMedCentral
33.
go back to reference 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. 10.1128/AAC.00851-07.CrossRefPubMedPubMedCentral 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. 10.1128/AAC.00851-07.CrossRefPubMedPubMedCentral
34.
go back to reference Schreiber MP, Chan CM, Shorr AF: Resistant pathogens in Nonnosocomial pneumonia and respiratory failure is it time to refine the definition of health-care-associated pneumonia?. Chest. 2010, 137: 1283-1288. 10.1378/chest.09-2434.CrossRefPubMed Schreiber MP, Chan CM, Shorr AF: Resistant pathogens in Nonnosocomial pneumonia and respiratory failure is it time to refine the definition of health-care-associated pneumonia?. Chest. 2010, 137: 1283-1288. 10.1378/chest.09-2434.CrossRefPubMed
35.
go back to reference Guimaraes C, Lares Santos C, Costa F, Barata F: Pneumonia associated with health care versus community acquired pneumonia: different entities, distinct approaches. Rev Port Pneumol. 2011, 17: 168-171. 10.1016/j.rppneu.2011.01.001.CrossRefPubMed Guimaraes C, Lares Santos C, Costa F, Barata F: Pneumonia associated with health care versus community acquired pneumonia: different entities, distinct approaches. Rev Port Pneumol. 2011, 17: 168-171. 10.1016/j.rppneu.2011.01.001.CrossRefPubMed
36.
go back to reference Chalmers JD, Taylor JK, Singanayagam A, Fleming GB, Akram AR, Mandal P, Choudhury G, Hill AT: Epidemiology, antibiotic therapy, and clinical outcomes in health care-associated pneumonia: a UK cohort study. Clin Infect Dis. 2011, 53: 107-113. 10.1093/cid/cir274.CrossRefPubMed Chalmers JD, Taylor JK, Singanayagam A, Fleming GB, Akram AR, Mandal P, Choudhury G, Hill AT: Epidemiology, antibiotic therapy, and clinical outcomes in health care-associated pneumonia: a UK cohort study. Clin Infect Dis. 2011, 53: 107-113. 10.1093/cid/cir274.CrossRefPubMed
37.
go back to reference Taşbakan MS, Bacakoğlu F, Kaçmaz Başoğlu O, Gürgün A, Başarik B, Çitim Tuncel S, Sayiner A: The comparison of patients with hospitalized health-care-associated pneumonia to community-acquired pneumonia. Tüberküloz ve Toraks Dergisi. 2011, 59: 348-354.CrossRef Taşbakan MS, Bacakoğlu F, Kaçmaz Başoğlu O, Gürgün A, Başarik B, Çitim Tuncel S, Sayiner A: The comparison of patients with hospitalized health-care-associated pneumonia to community-acquired pneumonia. Tüberküloz ve Toraks Dergisi. 2011, 59: 348-354.CrossRef
38.
go back to reference 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. 10.2169/internalmedicine.51.7987.CrossRefPubMed 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. 10.2169/internalmedicine.51.7987.CrossRefPubMed
39.
go back to reference Miyashita N, Kawai Y, Akaike H, Ouchi K, Hayashi T, Kurihara T, Okimoto N: Clinical features and the role of atypical pathogens in nursing and healthcare-associated pneumonia (NHCAP): differences between a teaching university hospital and a community hospital. Intern Med. 2012, 51: 585-594. 10.2169/internalmedicine.51.6475.CrossRefPubMed Miyashita N, Kawai Y, Akaike H, Ouchi K, Hayashi T, Kurihara T, Okimoto N: Clinical features and the role of atypical pathogens in nursing and healthcare-associated pneumonia (NHCAP): differences between a teaching university hospital and a community hospital. Intern Med. 2012, 51: 585-594. 10.2169/internalmedicine.51.6475.CrossRefPubMed
40.
go back to reference Wu CL, Ku SC, Yang KY, Fang WF, Tu CY, Chen CW, Hsu KH, Fan WC, Lin MC, Chen W, Ou CY, Yu CJ: Antimicrobial drug-resistant microbes associated with hospitalized community-acquired and health care-associated pneumonia: a multi-center study in Taiwan. J Formos Med Assoc. 2013, 112: 31-40. 10.1016/j.jfma.2011.09.028.CrossRefPubMed Wu CL, Ku SC, Yang KY, Fang WF, Tu CY, Chen CW, Hsu KH, Fan WC, Lin MC, Chen W, Ou CY, Yu CJ: Antimicrobial drug-resistant microbes associated with hospitalized community-acquired and health care-associated pneumonia: a multi-center study in Taiwan. J Formos Med Assoc. 2013, 112: 31-40. 10.1016/j.jfma.2011.09.028.CrossRefPubMed
41.
go back to reference Sugisaki M, Enomoto T, Shibuya Y, Matsumoto A, Saitoh H, Shingu A, Narato R, Nomura K: Clinical characteristics of healthcare-associated pneumonia in a public hospital in a metropolitan area of Japan. J Infect Chemother. 2012, 18: 352-360. 10.1007/s10156-011-0344-9.CrossRefPubMed Sugisaki M, Enomoto T, Shibuya Y, Matsumoto A, Saitoh H, Shingu A, Narato R, Nomura K: Clinical characteristics of healthcare-associated pneumonia in a public hospital in a metropolitan area of Japan. J Infect Chemother. 2012, 18: 352-360. 10.1007/s10156-011-0344-9.CrossRefPubMed
42.
go back to reference Giannella M, Pinilla B, Capdevila JA, Martínez Alarcón J, Muñoz P, López Álvarez J, Bouza E, on behalf of the Estudio de Neumonía En Medicina Interna (ENEMI) study Group from the Sociedad Española de Medicina Interna (SEMI): Pneumonia treated in the internal medicine department: focus on healthcare-associated pneumonia. Clin Microbiol Infect. 2012, 18: 786-794. 10.1111/j.1469-0691.2011.03757.x.CrossRefPubMed Giannella M, Pinilla B, Capdevila JA, Martínez Alarcón J, Muñoz P, López Álvarez J, Bouza E, on behalf of the Estudio de Neumonía En Medicina Interna (ENEMI) study Group from the Sociedad Española de Medicina Interna (SEMI): Pneumonia treated in the internal medicine department: focus on healthcare-associated pneumonia. Clin Microbiol Infect. 2012, 18: 786-794. 10.1111/j.1469-0691.2011.03757.x.CrossRefPubMed
43.
go back to reference Swenson BR, Metzger R, Hedrick TL, McElearney ST, Evans HL, Smith RL, Chong TW, Popovsky KA, Pruett TL, Sawyer RG: Choosing antibiotics for intra-abdominal infections: what do we mean by “high risk”?. Surg Infect. 2009, 10: 29-39. 10.1089/sur.2007.041.CrossRef Swenson BR, Metzger R, Hedrick TL, McElearney ST, Evans HL, Smith RL, Chong TW, Popovsky KA, Pruett TL, Sawyer RG: Choosing antibiotics for intra-abdominal infections: what do we mean by “high risk”?. Surg Infect. 2009, 10: 29-39. 10.1089/sur.2007.041.CrossRef
44.
go back to reference Merli M, Lucidi C, Giannelli V, Giusto M, Riggio O, Falcone M, Ridola L, Attili AF, Venditti M: Cirrhotic patients are at risk for health care-associated bacterial infections. Clin Gastroenterol Hepatol. 2010, 8: 979-985. 10.1016/j.cgh.2010.06.024.CrossRefPubMed Merli M, Lucidi C, Giannelli V, Giusto M, Riggio O, Falcone M, Ridola L, Attili AF, Venditti M: Cirrhotic patients are at risk for health care-associated bacterial infections. Clin Gastroenterol Hepatol. 2010, 8: 979-985. 10.1016/j.cgh.2010.06.024.CrossRefPubMed
45.
go back to reference Ha YE, Kang C-I, Joo E-J, Park SY, Kang SJ, Wi YM, Chung DR, Peck KR, Lee NY, Song J-H: Clinical implications of healthcare-associated infection in patients with community-onset acute pyelonephritis. Scand J Infect Dis. 2011, 43: 587-595. 10.3109/00365548.2011.572907.CrossRefPubMed Ha YE, Kang C-I, Joo E-J, Park SY, Kang SJ, Wi YM, Chung DR, Peck KR, Lee NY, Song J-H: Clinical implications of healthcare-associated infection in patients with community-onset acute pyelonephritis. Scand J Infect Dis. 2011, 43: 587-595. 10.3109/00365548.2011.572907.CrossRefPubMed
46.
go back to reference Sy RW, Kritharides L: Health care exposure and age in infective endocarditis: results of a contemporary population-based profile of 1536 patients in Australia. Eur Heart J. 1890–1897, 2010: 31. Sy RW, Kritharides L: Health care exposure and age in infective endocarditis: results of a contemporary population-based profile of 1536 patients in Australia. Eur Heart J. 1890–1897, 2010: 31.
47.
go back to reference Liu X, Han X, Ge Y, Wei F: Clinical analysis of healthcare-associated pneumonia. Chin J Infect Chemother. 2011, 11: 452-456. Liu X, Han X, Ge Y, Wei F: Clinical analysis of healthcare-associated pneumonia. Chin J Infect Chemother. 2011, 11: 452-456.
48.
go back to reference Falcone M, Venditti M, Shindo Y, Kollef MH: Healthcare-associated pneumonia: diagnostic criteria and distinction from community-acquired pneumonia. Int J Infect Dis. 2011, 15: E545-E550. 10.1016/j.ijid.2011.04.005.CrossRefPubMed Falcone M, Venditti M, Shindo Y, Kollef MH: Healthcare-associated pneumonia: diagnostic criteria and distinction from community-acquired pneumonia. Int J Infect Dis. 2011, 15: E545-E550. 10.1016/j.ijid.2011.04.005.CrossRefPubMed
49.
go back to reference Attridge RT, Frei CR: Health care-associated pneumonia: an evidence-based review. Am J Med. 2011, 124: 689-697. 10.1016/j.amjmed.2011.01.023.CrossRefPubMed Attridge RT, Frei CR: Health care-associated pneumonia: an evidence-based review. Am J Med. 2011, 124: 689-697. 10.1016/j.amjmed.2011.01.023.CrossRefPubMed
50.
go back to reference Lopez A, Amaro R, Polverino E: Does health care associated pneumonia really exist?. Eur J Intern Med. 2012, 23: 407-411. 10.1016/j.ejim.2012.05.006.CrossRefPubMed Lopez A, Amaro R, Polverino E: Does health care associated pneumonia really exist?. Eur J Intern Med. 2012, 23: 407-411. 10.1016/j.ejim.2012.05.006.CrossRefPubMed
51.
go back to reference Seddon J, Bhagani S: Antimicrobial therapy for the treatment of opportunistic infections in HIV/AIDS patients: a critical appraisal. HIV Aids. 2011, 3: 19-33. Seddon J, Bhagani S: Antimicrobial therapy for the treatment of opportunistic infections in HIV/AIDS patients: a critical appraisal. HIV Aids. 2011, 3: 19-33.
52.
go back to reference Donowitz GR, Maki DG, Crnich CJ, Pappas PG, Rolston KV: Infections in the neutropenic patient--new views of an old problem. Hematology Am Soc Hematol Educ Program. 2001, 113-139. doi:10.1182/asheducation-2001.1.113 Donowitz GR, Maki DG, Crnich CJ, Pappas PG, Rolston KV: Infections in the neutropenic patient--new views of an old problem. Hematology Am Soc Hematol Educ Program. 2001, 113-139. doi:10.1182/asheducation-2001.1.113
53.
go back to reference Naimi TS, LeDell KH, Como-Sabetti K, Borchardt SM, Boxrud DJ, Etienne J, Johnson SK, Vandenesch F, Fridkin S, O’Boyle C, Danila RN, Lynfield R: Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA. 2003, 290: 2976-2984. 10.1001/jama.290.22.2976.CrossRefPubMed Naimi TS, LeDell KH, Como-Sabetti K, Borchardt SM, Boxrud DJ, Etienne J, Johnson SK, Vandenesch F, Fridkin S, O’Boyle C, Danila RN, Lynfield R: Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA. 2003, 290: 2976-2984. 10.1001/jama.290.22.2976.CrossRefPubMed
54.
go back to reference Zahar JR, Lanternier F, Mechai F, Filley F, Taieb F, Mainot EL, Descamps P, Corriol O, Ferroni A, Bille E, Nassif X, Lortholary O: Duration of colonisation by Enterobacteriaceae producing extended-spectrum beta-lactamase and risk factors for persistent faecal carriage. J Hosp Infect. 2010, 75: 76-78. 10.1016/j.jhin.2009.11.010.CrossRefPubMed Zahar JR, Lanternier F, Mechai F, Filley F, Taieb F, Mainot EL, Descamps P, Corriol O, Ferroni A, Bille E, Nassif X, Lortholary O: Duration of colonisation by Enterobacteriaceae producing extended-spectrum beta-lactamase and risk factors for persistent faecal carriage. J Hosp Infect. 2010, 75: 76-78. 10.1016/j.jhin.2009.11.010.CrossRefPubMed
55.
go back to reference Chen SY, Wu GH, Chang SC, Hsueh PR, Chiang WC, Lee CC, Ma MH, Hung CC, Chen YC, Su CP, Tsai KC, Chen TH, Chen SC, Chen WJ: Bacteremia in previously hospitalized patients: prolonged effect from previous hospitalization and risk factors for antimicrobial-resistant bacterial infections. Ann Emerg Med. 2008, 51: 639-646. 10.1016/j.annemergmed.2007.12.022.CrossRefPubMed Chen SY, Wu GH, Chang SC, Hsueh PR, Chiang WC, Lee CC, Ma MH, Hung CC, Chen YC, Su CP, Tsai KC, Chen TH, Chen SC, Chen WJ: Bacteremia in previously hospitalized patients: prolonged effect from previous hospitalization and risk factors for antimicrobial-resistant bacterial infections. Ann Emerg Med. 2008, 51: 639-646. 10.1016/j.annemergmed.2007.12.022.CrossRefPubMed
56.
go back to reference Collins AS: Preventing health care-associated infections. Patient Safety and Quality: an Evidence-Based Handbook for Nurses. Edited by: Hughes RG. 2008, Rockville (MD): Agency for Healthcare Research and Quality, U.S. Department of Health and Human Services Collins AS: Preventing health care-associated infections. Patient Safety and Quality: an Evidence-Based Handbook for Nurses. Edited by: Hughes RG. 2008, Rockville (MD): Agency for Healthcare Research and Quality, U.S. Department of Health and Human Services
57.
go back to reference Polverino E, Dambrava P, Cilloniz C, Balasso V, Marcos MA, Esquinas C, Mensa J, Ewig S, Torres A: Nursing home-acquired pneumonia: a 10 year single-centre experience. Thorax. 2010, 65: 354-359. 10.1136/thx.2009.124776.CrossRefPubMed Polverino E, Dambrava P, Cilloniz C, Balasso V, Marcos MA, Esquinas C, Mensa J, Ewig S, Torres A: Nursing home-acquired pneumonia: a 10 year single-centre experience. Thorax. 2010, 65: 354-359. 10.1136/thx.2009.124776.CrossRefPubMed
58.
go back to reference El Solh AA, Pietrantoni C, Bhat A, Bhora M, Berbary E: Indicators of potentially drug-resistant bacteria in severe nursing home-acquired pneumonia. Clin Infect Dis. 2004, 39: 474-480. 10.1086/422317.CrossRefPubMed El Solh AA, Pietrantoni C, Bhat A, Bhora M, Berbary E: Indicators of potentially drug-resistant bacteria in severe nursing home-acquired pneumonia. Clin Infect Dis. 2004, 39: 474-480. 10.1086/422317.CrossRefPubMed
59.
go back to reference Mandell LA, Wunderink RG, Anzueto A, Bartlett JG, Campbell GD, Dean NC, Dowell SF, File TM, Musher DM, Niederman MS, Torres A, Whitney CG, Infectious Diseases Society of America; American Thoracic Society: Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin Infect Dis. 2007, 44: S27-S72. 10.1086/511159.CrossRefPubMed Mandell LA, Wunderink RG, Anzueto A, Bartlett JG, Campbell GD, Dean NC, Dowell SF, File TM, Musher DM, Niederman MS, Torres A, Whitney CG, Infectious Diseases Society of America; American Thoracic Society: Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin Infect Dis. 2007, 44: S27-S72. 10.1086/511159.CrossRefPubMed
60.
go back to reference Brito V, Niederman MS: Healthcare-associated pneumonia is a heterogeneous disease, and all patients do not need the same broad-spectrum antibiotic therapy as complex nosocomial pneumonia. Curr Opin Infect Dis. 2009, 22: 316-325. 10.1097/QCO.0b013e328329fa4e.CrossRefPubMed Brito V, Niederman MS: Healthcare-associated pneumonia is a heterogeneous disease, and all patients do not need the same broad-spectrum antibiotic therapy as complex nosocomial pneumonia. Curr Opin Infect Dis. 2009, 22: 316-325. 10.1097/QCO.0b013e328329fa4e.CrossRefPubMed
Metadata
Title
Classification of healthcare-associated infection: a systematic review 10 years after the first proposal
Authors
Teresa Cardoso
Mónica Almeida
N Deborah Friedman
Irene Aragão
Altamiro Costa-Pereira
António E Sarmento
Luís Azevedo
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2014
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/1741-7015-12-40

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Reviewer acknowledgement

Reviewer acknowledgements for 2013