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Published in: BMC Infectious Diseases 1/2017

Open Access 01-12-2017 | Research article

Pneumonia caused by extensive drug-resistant Acinetobacter baumannii among hospitalized patients: genetic relationships, risk factors and mortality

Authors: Yu jun Li, Chu zhi Pan, Chang quan Fang, Zhu xiang Zhao, Hui ling Chen, Peng hao Guo, Zi wen Zhao

Published in: BMC Infectious Diseases | Issue 1/2017

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Abstract

Background

The clonal spread of multiple drug-resistant Acinetobacter baumannii is an emerging problem in China. We analysed the molecular epidemiology of Acinetobacter baumanni isolates at three teaching hospitals and investigated the risk factors, clinical features, and outcomes of hospital-acquired pneumonia caused by extensive drug-resistant Acinetobacter baumannii (XDRAB) infection in Guangzhou, China.

Methods

Fifty-two A. baumannii isolates were collected. Multilocus sequence typing (MLST) was used to assess the genetic relationships among the isolates. The bla OXA-51-like gene was amplified using polymerase chain reaction (PCR) and sequencing. The resistance phenotypes were determined using the disc diffusion method. A retrospective case-control study was performed to determine factors associated with XDRAB pneumonia.

Results

Most of the 52 A. baumannii isolates (N = 37, 71.2%) were collected from intensive care units (ICUs). The respiratory system was the most common bodily site from which A. baumannii was recovered (N = 45, 86.5%). Disc diffusion classified the isolates into 17 multidrug-resistant (MDR) and 35 extensively drug-resistant (XDR) strains. MLST grouped the A. baumannii isolates into 5 existing sequence types (STs) and 7 new STs. ST195 and ST208 accounted for 69.2% (36/52) of the isolates. The clonal relationship analysis showed that ST195 and ST208 belonged to clonal complex (CC) 92. According to the sequence-based typing (SBT) of the bla OXA-51-like gene, 51 A. baumannii isolates carried OXA-66 and the rest carried OXA-199. There were no significant differences with respect to the resistance phenotype between the CC92 and non-CC92 strains (P = 0.767). The multivariate analysis showed that the APACHE II score, chronic obstructive pulmonary disease (COPD) and cardiac disease were independent risk factors for XDRAB pneumonia (P < 0.05). The mortality rate of XDRAB pneumonia was high (up to 42.8%), but pneumonia caused by XDRAB was not associated with in-hospital mortality (P = 0.582).

Conclusions

ST195 may be the most common ST in Guangzhou, China, and may serve as a severe epidemic marker. SBT of bla OXA-51-like gene variants may not result in sufficient dissimilarities to type isolates in a small-scale, geographically restricted study of a single region. XDRAB pneumonia was strongly related to systemic illnesses and the APACHE II score but was not associated with in-hospital mortality.
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Literature
1.
go back to reference Ying J, Lu J, Zong L, Li A, Pan R, Cheng C, et al. Molecular epidemiology and characterization of genotypes of Acinetobacter baumannii isolates from regions of South China. Jpn J Infect Dis. 2016;69:180–5.CrossRefPubMed Ying J, Lu J, Zong L, Li A, Pan R, Cheng C, et al. Molecular epidemiology and characterization of genotypes of Acinetobacter baumannii isolates from regions of South China. Jpn J Infect Dis. 2016;69:180–5.CrossRefPubMed
2.
go back to reference El-Shazly S, Dashti A, Vali L, Bolaris M, Ibrahim AS. Molecular epidemiology and characterization of multiple drug-resistant (MDR) clinical isolates of Acinetobacter baumannii. Int J Infect Dis. 2015;41:42–9.CrossRefPubMedPubMedCentral El-Shazly S, Dashti A, Vali L, Bolaris M, Ibrahim AS. Molecular epidemiology and characterization of multiple drug-resistant (MDR) clinical isolates of Acinetobacter baumannii. Int J Infect Dis. 2015;41:42–9.CrossRefPubMedPubMedCentral
3.
go back to reference Hu FP, Guo Y, Zhu DM, Wang F, Jiang XF, Xu YC, et al. Resistance trends among clinical isolates in China reported from CHINET surveillance of bacterial resistance, 2005–2014. Clin Microbiol Infect. 2016;22 Suppl 1:S9–14.CrossRefPubMed Hu FP, Guo Y, Zhu DM, Wang F, Jiang XF, Xu YC, et al. Resistance trends among clinical isolates in China reported from CHINET surveillance of bacterial resistance, 2005–2014. Clin Microbiol Infect. 2016;22 Suppl 1:S9–14.CrossRefPubMed
5.
go back to reference Li YJ, Pan CZ, Zhao ZW, Zhao ZX, Chen HL, Lu WB. Effects of a combination of amlodipine and imipenem on 42 clinical isolates of Acinetobacter baumannii obtained from a teaching hospital in Guangzhou, China. BMC Infect Dis. 2013;13:548. Li YJ, Pan CZ, Zhao ZW, Zhao ZX, Chen HL, Lu WB. Effects of a combination of amlodipine and imipenem on 42 clinical isolates of Acinetobacter baumannii obtained from a teaching hospital in Guangzhou, China. BMC Infect Dis. 2013;13:548.
6.
go back to reference Batirel A, Balkan II, Karabay O, Agalar C, Akalin S, Alici O, et al. Comparison of colistin-carbapenem, colistin-sulbactam, and colistin plus other antibacterial agents for the treatment of extremely drug-resistant Acinetobacter baumannii bloodstream infections. Eur J Clin Microbiol Infect Dis. 2014;33:1311–22. Batirel A, Balkan II, Karabay O, Agalar C, Akalin S, Alici O, et al. Comparison of colistin-carbapenem, colistin-sulbactam, and colistin plus other antibacterial agents for the treatment of extremely drug-resistant Acinetobacter baumannii bloodstream infections. Eur J Clin Microbiol Infect Dis. 2014;33:1311–22.
7.
go back to reference Apisarnthanarak A, Warren DK. Intervention to limit transmission of extremely drug-resistant Acinetobacter baumannii in patients who underwent surgery. Clin Infect Dis. 2013;57:1215–6.CrossRefPubMed Apisarnthanarak A, Warren DK. Intervention to limit transmission of extremely drug-resistant Acinetobacter baumannii in patients who underwent surgery. Clin Infect Dis. 2013;57:1215–6.CrossRefPubMed
9.
go back to reference Karah N, Sundsfjord A, Towner K, Samuelsen Ø. Insights into the global molecular epidemiology of carbapenem non-susceptible clones of Acinetobacter baumannii. Drug Resist Updat. 2012;15:237–47.CrossRefPubMed Karah N, Sundsfjord A, Towner K, Samuelsen Ø. Insights into the global molecular epidemiology of carbapenem non-susceptible clones of Acinetobacter baumannii. Drug Resist Updat. 2012;15:237–47.CrossRefPubMed
10.
go back to reference Fu Y, Zhou J, Zhou H, Yang Q, Wei Z, Yu Y, et al. Wide dissemination of OXA-23-producing carbapenem-resistant Acinetobacter baumannii clonal complex 22 in multiple cities of China. J Antimicrob Chemother. 2010;65:644–50.CrossRefPubMed Fu Y, Zhou J, Zhou H, Yang Q, Wei Z, Yu Y, et al. Wide dissemination of OXA-23-producing carbapenem-resistant Acinetobacter baumannii clonal complex 22 in multiple cities of China. J Antimicrob Chemother. 2010;65:644–50.CrossRefPubMed
11.
go back to reference Ruan Z, Chen Y, Jiang Y, Zhou H, Zhou Z, Fu Y, et al. Wide distribution of CC92 carbapenem-resistant and OXA-23-producing Acinetobacter baumannii in multiple provinces of China. Int J Antimicrob Agents. 2013;42:322–8.CrossRefPubMed Ruan Z, Chen Y, Jiang Y, Zhou H, Zhou Z, Fu Y, et al. Wide distribution of CC92 carbapenem-resistant and OXA-23-producing Acinetobacter baumannii in multiple provinces of China. Int J Antimicrob Agents. 2013;42:322–8.CrossRefPubMed
12.
go back to reference Zhong Q, Xu W, Wu Y, Xu H. Clonal spread of carbapenem non-susceptible Acinetobacter baumannii in an intensive care unit in a teaching hospital in China. Ann Lab Med. 2012;32:413–9.CrossRefPubMedPubMedCentral Zhong Q, Xu W, Wu Y, Xu H. Clonal spread of carbapenem non-susceptible Acinetobacter baumannii in an intensive care unit in a teaching hospital in China. Ann Lab Med. 2012;32:413–9.CrossRefPubMedPubMedCentral
13.
go back to reference He C, Xie Y, Zhang L, Kang M, Tao C, Chen Z, et al. Increasing imipenem resistance and dissemination of the ISAba1-associated blaOXA-23 gene among Acinetobacter baumannii isolates in an intensive care unit. J Med Microbiol. 2011;60:337–41.CrossRefPubMed He C, Xie Y, Zhang L, Kang M, Tao C, Chen Z, et al. Increasing imipenem resistance and dissemination of the ISAba1-associated blaOXA-23 gene among Acinetobacter baumannii isolates in an intensive care unit. J Med Microbiol. 2011;60:337–41.CrossRefPubMed
14.
go back to reference Hamouda A, Evans BA, Towner KJ, Amyes SG. Characterization of epidemiologically unrelated Acinetobacter baumannii isolates from four continents by use of multilocus sequence typing, pulsed-field gel electrophoresis, and sequence- based typing of bla OXA-51-like genes. J Clin Microbiol. 2010;48:2476–83.CrossRefPubMedPubMedCentral Hamouda A, Evans BA, Towner KJ, Amyes SG. Characterization of epidemiologically unrelated Acinetobacter baumannii isolates from four continents by use of multilocus sequence typing, pulsed-field gel electrophoresis, and sequence- based typing of bla OXA-51-like genes. J Clin Microbiol. 2010;48:2476–83.CrossRefPubMedPubMedCentral
15.
go back to reference Evans BA, Hamouda A, Towner KJ, Amyes SG. OXA-51-like beta-lactamases and their association with particular epidemic lineages of Acinetobacter baumannii. Clin Microbiol Infect. 2008;14:268–75.CrossRefPubMed Evans BA, Hamouda A, Towner KJ, Amyes SG. OXA-51-like beta-lactamases and their association with particular epidemic lineages of Acinetobacter baumannii. Clin Microbiol Infect. 2008;14:268–75.CrossRefPubMed
16.
go back to reference Zander E, Nemec A, Seifert H, Higgins PG. Association betweenβ-Lactamase-Encoding blaOXA-51 variants and DiversiLab rep-PCR-Based typing of Acinetobacter baumannii isolates. J Clin Microbiol. 2012;50:1900–4.CrossRefPubMedPubMedCentral Zander E, Nemec A, Seifert H, Higgins PG. Association betweenβ-Lactamase-Encoding blaOXA-51 variants and DiversiLab rep-PCR-Based typing of Acinetobacter baumannii isolates. J Clin Microbiol. 2012;50:1900–4.CrossRefPubMedPubMedCentral
17.
go back to reference Clinical and Laboratory Standard Institute. Performance standards for antimicrobial susceptibility testing. Nineteenth informational supplement. CLSI Document M100 S22. Wayne: Clinical and Laboratory Standard Institute; 2012. Clinical and Laboratory Standard Institute. Performance standards for antimicrobial susceptibility testing. Nineteenth informational supplement. CLSI Document M100 S22. Wayne: Clinical and Laboratory Standard Institute; 2012.
18.
go back to reference Bartual SG, Seifert H, Hippler C, Luzon MA, Wisplinghoff H, Rodríguez-Valera F. Development of a multilocus sequence typing scheme for characterization of clinical isolates of Acinetobacter baumannii. J Clin Microbiol. 2005;43:4382–90.CrossRefPubMedPubMedCentral Bartual SG, Seifert H, Hippler C, Luzon MA, Wisplinghoff H, Rodríguez-Valera F. Development of a multilocus sequence typing scheme for characterization of clinical isolates of Acinetobacter baumannii. J Clin Microbiol. 2005;43:4382–90.CrossRefPubMedPubMedCentral
21.
go back to reference Héritier C, Poirel L, Fournier P-E, Claverie J-M, Raoult D, Nordmann P. Characterization of the naturally occurring Oxacillinase of Acinetobacter baumannii. Antimicrob Agents Chemother. 2005;49:4174–9.CrossRefPubMedPubMedCentral Héritier C, Poirel L, Fournier P-E, Claverie J-M, Raoult D, Nordmann P. Characterization of the naturally occurring Oxacillinase of Acinetobacter baumannii. Antimicrob Agents Chemother. 2005;49:4174–9.CrossRefPubMedPubMedCentral
22.
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
23.
go back to reference Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control. 2008;36:309–32.CrossRefPubMed Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control. 2008;36:309–32.CrossRefPubMed
24.
go back to reference Lowings M, Ehlers MM, Dreyer AW, Kock MM. High prevalence of oxacillinases in clinical multidrug-resistant Acinetobacter baumannii isolates from the Tshwane region, South Africa – an update. BMC Infect Dis. 2015;15:521.CrossRefPubMedPubMedCentral Lowings M, Ehlers MM, Dreyer AW, Kock MM. High prevalence of oxacillinases in clinical multidrug-resistant Acinetobacter baumannii isolates from the Tshwane region, South Africa – an update. BMC Infect Dis. 2015;15:521.CrossRefPubMedPubMedCentral
25.
go back to reference Zhou Y, Wu X, Zhang X, Hu Y, Yang X, Yang Z, et al. Genetic characterization of ST195 and ST365 carbapenem-resistant Acinetobacter baumannii harboring blaOXA-23 in Guangzhou, China. Microb Drug Resist. 2015;21:386–90.CrossRefPubMed Zhou Y, Wu X, Zhang X, Hu Y, Yang X, Yang Z, et al. Genetic characterization of ST195 and ST365 carbapenem-resistant Acinetobacter baumannii harboring blaOXA-23 in Guangzhou, China. Microb Drug Resist. 2015;21:386–90.CrossRefPubMed
26.
go back to reference Runnegar N, Sidjabat H, Goh HM, Nimmo GR, Schembri MA, Paterson DL. Molecular epidemiology of multidrug-resistant Acinetobacter baumannii in a single institution over a 10-year period. J Clin Microbiol. 2010;48:4051–6. Runnegar N, Sidjabat H, Goh HM, Nimmo GR, Schembri MA, Paterson DL. Molecular epidemiology of multidrug-resistant Acinetobacter baumannii in a single institution over a 10-year period. J Clin Microbiol. 2010;48:4051–6.
27.
go back to reference Pournaras S, Gogou V, Giannouli M, Dimitroulia E, Dafopoulou K, Tsakris A, et al. Single-locus-sequence-based typing of blaOXA-51-like genes for rapid assignment of Acinetobacter baumannii clinical isolates to international clonal lineages. J Clin Microbiol. 2014;52:1653–7.CrossRefPubMedPubMedCentral Pournaras S, Gogou V, Giannouli M, Dimitroulia E, Dafopoulou K, Tsakris A, et al. Single-locus-sequence-based typing of blaOXA-51-like genes for rapid assignment of Acinetobacter baumannii clinical isolates to international clonal lineages. J Clin Microbiol. 2014;52:1653–7.CrossRefPubMedPubMedCentral
28.
go back to reference Wang H, Guo P, Sun H, Wang H, Yang Q, Chen M, et al. Molecular epidemiology of clinical isolates of carbapenem-resistant Acinetobacter spp. From Chinese hospitals. Antimicrob Agents Chemother. 2007;51:4022–8.CrossRefPubMedPubMedCentral Wang H, Guo P, Sun H, Wang H, Yang Q, Chen M, et al. Molecular epidemiology of clinical isolates of carbapenem-resistant Acinetobacter spp. From Chinese hospitals. Antimicrob Agents Chemother. 2007;51:4022–8.CrossRefPubMedPubMedCentral
29.
go back to reference Tsai H-T, Wang J-T, Chen CJ, Chang S-C. Association between antibiotic usage and subsequent colonization or infection of extensive drug-resistant Acinetobacter baumannii: a matched case-control study in intensive care units. Diagn Microbiol Infect Dis. 2008;62:298–305.CrossRefPubMed Tsai H-T, Wang J-T, Chen CJ, Chang S-C. Association between antibiotic usage and subsequent colonization or infection of extensive drug-resistant Acinetobacter baumannii: a matched case-control study in intensive care units. Diagn Microbiol Infect Dis. 2008;62:298–305.CrossRefPubMed
30.
go back to reference Dent LL, Marshall DR, Pratap S, Hulette RB. Multidrug resistant Acinetobacter baumannii: a descriptive study in a city hospital. BMC Infect Dis. 2010;10:196.CrossRefPubMedPubMedCentral Dent LL, Marshall DR, Pratap S, Hulette RB. Multidrug resistant Acinetobacter baumannii: a descriptive study in a city hospital. BMC Infect Dis. 2010;10:196.CrossRefPubMedPubMedCentral
31.
go back to reference Zheng YL, Wan YF, Zhou LY, Ye ML, Liu S, Xu CQ, et al. Risk factors and mortality of patients with nosocomial carbapenem-resistant Acinetobacter baumannii pneumonia. Am J Infect Control. 2013;41:e1–5.CrossRef Zheng YL, Wan YF, Zhou LY, Ye ML, Liu S, Xu CQ, et al. Risk factors and mortality of patients with nosocomial carbapenem-resistant Acinetobacter baumannii pneumonia. Am J Infect Control. 2013;41:e1–5.CrossRef
32.
go back to reference Li Y, Guo Q, Wang P, Zhu D, Ye X, Wu S, et al. Clonal dissemination of extensively drug-resistant Acinetobacter baumannii producing an OXA-23 β-lactamase at a teaching hospital in Shanghai, China. J Microbiol Immunol Infect. 2015;48:101–8.CrossRefPubMed Li Y, Guo Q, Wang P, Zhu D, Ye X, Wu S, et al. Clonal dissemination of extensively drug-resistant Acinetobacter baumannii producing an OXA-23 β-lactamase at a teaching hospital in Shanghai, China. J Microbiol Immunol Infect. 2015;48:101–8.CrossRefPubMed
33.
go back to reference Özgür ES, Horasan ES, Karaca K, Ersöz G, Naycı Atış S, Kaya A. Ventilator-associated pneumonia due to extensive drug-resistant Acinetobacter baumannii: risk factors, clinical features, and outcomes. Am J Infect Control. 2014;42:206–8.CrossRefPubMed Özgür ES, Horasan ES, Karaca K, Ersöz G, Naycı Atış S, Kaya A. Ventilator-associated pneumonia due to extensive drug-resistant Acinetobacter baumannii: risk factors, clinical features, and outcomes. Am J Infect Control. 2014;42:206–8.CrossRefPubMed
34.
go back to reference Chan MC, Chiu SK, Hsueh PR, Wang NC, Wang CC, Fang CT. Risk factors for healthcare-associated extensively drug-resistant Acinetobacter baumannii infections: a case-control study. PLoS One. 2014;9, e85973.CrossRefPubMedPubMedCentral Chan MC, Chiu SK, Hsueh PR, Wang NC, Wang CC, Fang CT. Risk factors for healthcare-associated extensively drug-resistant Acinetobacter baumannii infections: a case-control study. PLoS One. 2014;9, e85973.CrossRefPubMedPubMedCentral
35.
go back to reference Yang Y-S, Lee Y-T, Huang TW, Sun J-R, Kuo S-C, Yang C-H, et al. Acinetobacter baumannii nosocomial pneumonia: is the outcome more favorable in non-ventilated than ventilated patients? BMC Infect Dis. 2013;13:142.CrossRefPubMedPubMedCentral Yang Y-S, Lee Y-T, Huang TW, Sun J-R, Kuo S-C, Yang C-H, et al. Acinetobacter baumannii nosocomial pneumonia: is the outcome more favorable in non-ventilated than ventilated patients? BMC Infect Dis. 2013;13:142.CrossRefPubMedPubMedCentral
36.
go back to reference Özvatan T, Akalın H, Sınırtaş M, Ocakoğlu G, Yılmaz E, Heper Y, et al. Nosocomial Acinetobacter pneumonia: treatment and prognostic factors in 356 cases. Respirology. 2016;21:363–9.CrossRefPubMed Özvatan T, Akalın H, Sınırtaş M, Ocakoğlu G, Yılmaz E, Heper Y, et al. Nosocomial Acinetobacter pneumonia: treatment and prognostic factors in 356 cases. Respirology. 2016;21:363–9.CrossRefPubMed
37.
go back to reference Sunenshine RH, Wright M-O, Maragakis LL, Harris AD, Song X, Hebden J, et al. Multidrug-resistant Acinetobacter infection mortality rate and length of hospitalization. Emerg Infect Dis. 2007;13:97–103.CrossRefPubMedPubMedCentral Sunenshine RH, Wright M-O, Maragakis LL, Harris AD, Song X, Hebden J, et al. Multidrug-resistant Acinetobacter infection mortality rate and length of hospitalization. Emerg Infect Dis. 2007;13:97–103.CrossRefPubMedPubMedCentral
Metadata
Title
Pneumonia caused by extensive drug-resistant Acinetobacter baumannii among hospitalized patients: genetic relationships, risk factors and mortality
Authors
Yu jun Li
Chu zhi Pan
Chang quan Fang
Zhu xiang Zhao
Hui ling Chen
Peng hao Guo
Zi wen Zhao
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2017
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2471-0

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