Clinical and Molecular Characteristics of Klebsiella pneumoniae Isolates Causing Bloodstream Infections in Japan: Occurrence of Hypervirulent Infections in Health Care

doi:10.1128/JCM.01206-19

. 2019 Oct 23;57(11):e01206-19.

doi: 10.1128/JCM.01206-19. Print 2019 Nov.

Clinical and Molecular Characteristics of Klebsiella pneumoniae Isolates Causing Bloodstream Infections in Japan: Occurrence of Hypervirulent Infections in Health Care

Sohei Harada^{1

2

3}, Kotaro Aoki², Shungo Yamamoto⁴, Yoshikazu Ishii², Noritaka Sekiya⁵, Hanako Kurai⁶, Keiichi Furukawa⁷, Asako Doi⁸, Kentaro Tochitani⁴, Kenji Kubo⁹, Yukihiro Yamaguchi¹⁰, Masashi Narita^{11

12}, Shinya Kamiyama¹³, Jun Suzuki¹⁴, Takahiko Fukuchi¹⁵, Yoshiaki Gu¹⁶, Keiji Okinaka¹⁷, Soichi Shiiki¹², Kayoko Hayakawa¹⁸, Natsuo Tachikawa¹⁹, Kei Kasahara²⁰, Tadahiro Nakamura²¹, Kyoko Yokota^{22

23}, Masanari Komatsu²⁴, Misaki Takamiya²⁵, Kazuhiro Tateda², Yohei Doi²⁶

Affiliations

¹ Department of Infectious Diseases, Fujita Health University School of Medicine, Toyoake, Aichi, Japan haradas-tky@umin.ac.jp.
² Department of Microbiology and Infectious Diseases, Toho University School of Medicine, Tokyo, Japan.
³ Department of Infectious Diseases, Cancer Institute Hospital, Japanese Foundation for Cancer Research, Tokyo, Japan.
⁴ Department of Infectious Diseases, Kyoto City Hospital, Kyoto, Japan.
⁵ Department of Infection Prevention and Control, Tokyo Metropolitan Cancer and Infectious Diseases Center Komagome Hospital, Tokyo, Japan.
⁶ Division of Infectious Diseases, Shizuoka Cancer Center Hospital, Nagaizumi, Shizuoka, Japan.
⁷ Division of Infectious Diseases, St. Luke's International Hospital, Tokyo, Japan.
⁸ Department of Infectious Diseases, Kobe City Medical Center General Hospital, Kobe, Hyogo, Japan.
⁹ Department of Infectious Diseases, Japanese Red Cross Wakayama Medical Center, Wakayama, Japan.
¹⁰ Department of infectious diseases, Kenwakai Otemachi Hospital, Kitakyushu, Fukuoka, Japan.
¹¹ Department of Medicine, Ohta Nishinouchi General Hospital, Koriyama, Fukushima, Japan.
¹² Division of Infectious Diseases, Okinawa Chubu Hospital, Uruma, Okinawa, Japan.
¹³ Department of Clinical Laboratory Medicine and Infectious Diseases, Kurashiki Central Hospital, Kurashiki, Okayama, Japan.
¹⁴ Division of General Internal Medicine, National Hospital Organization Nagoya Medical Center, Nagoya, Aichi, Japan.
¹⁵ Division of Infectious Disease Therapeutics, Department of Microbiology and Infectious Diseases, Kobe University Graduate School of Medicine, Kobe, Hyogo, Japan.
¹⁶ Department of Infectious Diseases, Tohoku University Hospital, Sendai, Miyagi, Japan.
¹⁷ Division of General Internal Medicine, National Cancer Center Hospital, Tokyo, Japan.
¹⁸ Disease Control and Prevention Center, National Center for Global Health and Medicine, Tokyo, Japan.
¹⁹ Department of Infectious Diseases, Yokohama Municipal Citizen's Hospital, Yokohama, Kanagawa, Japan.
²⁰ Center for Infectious Diseases, Nara Medical University, Kashihara, Nara, Japan.
²¹ Department of Internal medicine, Japan Community Health care Organization Osaka Hospital, Osaka, Japan.
²² Department of General Internal Medicine, Faculty of Medicine, Kagawa University, Takamatsu, Kagawa, Japan.
²³ Department of Infectious Diseases, Kagawa Prefectural Central Hospital, Takamatsu, Kagawa, Japan.
²⁴ Division of General Medicine, Kagoshima Seikyo Hospital, Kagoshima, Japan.
²⁵ Department of infectious diseases, Hamamatsu Medical Center, Hamamatsu, Shizuoka, Japan.
²⁶ Department of Infectious Diseases, Fujita Health University School of Medicine, Toyoake, Aichi, Japan.

PMID: 31434721
PMCID: PMC6812994
DOI: 10.1128/JCM.01206-19

Clinical and Molecular Characteristics of Klebsiella pneumoniae Isolates Causing Bloodstream Infections in Japan: Occurrence of Hypervirulent Infections in Health Care

Sohei Harada et al. J Clin Microbiol. 2019.

. 2019 Oct 23;57(11):e01206-19.

doi: 10.1128/JCM.01206-19. Print 2019 Nov.

Authors

Affiliations

¹ Department of Infectious Diseases, Fujita Health University School of Medicine, Toyoake, Aichi, Japan haradas-tky@umin.ac.jp.
² Department of Microbiology and Infectious Diseases, Toho University School of Medicine, Tokyo, Japan.
³ Department of Infectious Diseases, Cancer Institute Hospital, Japanese Foundation for Cancer Research, Tokyo, Japan.
⁴ Department of Infectious Diseases, Kyoto City Hospital, Kyoto, Japan.
⁵ Department of Infection Prevention and Control, Tokyo Metropolitan Cancer and Infectious Diseases Center Komagome Hospital, Tokyo, Japan.
⁶ Division of Infectious Diseases, Shizuoka Cancer Center Hospital, Nagaizumi, Shizuoka, Japan.
⁷ Division of Infectious Diseases, St. Luke's International Hospital, Tokyo, Japan.
⁸ Department of Infectious Diseases, Kobe City Medical Center General Hospital, Kobe, Hyogo, Japan.
⁹ Department of Infectious Diseases, Japanese Red Cross Wakayama Medical Center, Wakayama, Japan.
¹⁰ Department of infectious diseases, Kenwakai Otemachi Hospital, Kitakyushu, Fukuoka, Japan.
¹¹ Department of Medicine, Ohta Nishinouchi General Hospital, Koriyama, Fukushima, Japan.
¹² Division of Infectious Diseases, Okinawa Chubu Hospital, Uruma, Okinawa, Japan.
¹³ Department of Clinical Laboratory Medicine and Infectious Diseases, Kurashiki Central Hospital, Kurashiki, Okayama, Japan.
¹⁴ Division of General Internal Medicine, National Hospital Organization Nagoya Medical Center, Nagoya, Aichi, Japan.
¹⁵ Division of Infectious Disease Therapeutics, Department of Microbiology and Infectious Diseases, Kobe University Graduate School of Medicine, Kobe, Hyogo, Japan.
¹⁶ Department of Infectious Diseases, Tohoku University Hospital, Sendai, Miyagi, Japan.
¹⁷ Division of General Internal Medicine, National Cancer Center Hospital, Tokyo, Japan.
¹⁸ Disease Control and Prevention Center, National Center for Global Health and Medicine, Tokyo, Japan.
¹⁹ Department of Infectious Diseases, Yokohama Municipal Citizen's Hospital, Yokohama, Kanagawa, Japan.
²⁰ Center for Infectious Diseases, Nara Medical University, Kashihara, Nara, Japan.
²¹ Department of Internal medicine, Japan Community Health care Organization Osaka Hospital, Osaka, Japan.
²² Department of General Internal Medicine, Faculty of Medicine, Kagawa University, Takamatsu, Kagawa, Japan.
²³ Department of Infectious Diseases, Kagawa Prefectural Central Hospital, Takamatsu, Kagawa, Japan.
²⁴ Division of General Medicine, Kagoshima Seikyo Hospital, Kagoshima, Japan.
²⁵ Department of infectious diseases, Hamamatsu Medical Center, Hamamatsu, Shizuoka, Japan.
²⁶ Department of Infectious Diseases, Fujita Health University School of Medicine, Toyoake, Aichi, Japan.

PMID: 31434721
PMCID: PMC6812994
DOI: 10.1128/JCM.01206-19

Abstract

Although hypervirulent Klebsiella pneumoniae (hvKp) has been associated with severe community-acquired infections that occur among relatively healthy individuals, information about hvKp infections in health care settings remains limited. Here, we systematically analyzed the clinical and molecular characteristics of K. pneumoniae isolates causing bloodstream infections in a cross-sectional study. Clinical characteristics of K. pneumoniae bloodstream infections from hospitals across Japan were analyzed by a review of the medical records. Whole-genome sequencing of the causative isolates was performed. Bacterial species were confirmed and hvKp were identified using whole-genome sequencing data. Clinical characteristics of hvKp infections were compared with those of non-hvKp infections by bivariate analyses. Of 140 cases of K. pneumoniae bloodstream infections, 26 cases (18.6%) were caused by various clones of hvKp defined by the carriage of cardinal virulence genes. Molecular identification revealed that 24 (17.1%) and 14 (10%) cases were caused by Klebsiella variicola and Klebsiella quasipneumoniae, respectively. Patients with hvKp infections had higher proportions of diabetes mellitus (risk ratio [RR], 1.75; 95% confidence interval [CI], 1.05 to 2.94), and their infections had significantly higher propensity to involve pneumonia (RR, 5.85; 95% CI, 1.39 to 24.6), liver abscess (RR, 5.85; 95% CI, 1.39 to 24.6), and disseminated infections (RR, 6.58; 95% CI, 1.16 to 37.4) than infections by other isolates. More than one-half of hvKp infections were health care associated or hospital acquired, and a probable event of health care-associated transmission of hvKp was documented. hvKp isolates, which are significantly associated with severe and disseminated infections, are frequently involved in health care-associated and hospital-acquired infections in Japan.

Keywords: bloodstream infection; disseminated infection; hypervirulent Klebsiella pneumoniae; whole-genome sequencing.

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References

1. Wang JH, Liu YC, Lee SS, Yen MY, Chen YS, Wang JH, Wann SR, Lin HH. 1998. Primary liver abscess due to Klebsiella pneumoniae in Taiwan. Clin Infect Dis 26:1434–1438. doi:10.1086/516369. - DOI - PubMed
1. Chuang YP, Fang CT, Lai SY, Chang SC, Wang JT. 2006. Genetic determinants of capsular serotype K1 of Klebsiella pneumoniae causing primary pyogenic liver abscess. J Infect Dis 193:645–654. doi:10.1086/499968. - DOI - PubMed
1. Brisse S, Fevre C, Passet V, Issenhuth-Jeanjean S, Tournebize R, Diancourt L, Grimont P. 2009. Virulent clones of Klebsiella pneumoniae: identification and evolutionary scenario based on genomic and phenotypic characterization. PLoS One 4:e4982. doi:10.1371/journal.pone.0004982. - DOI - PMC - PubMed
1. Decré D, Verdet C, Emirian A, Le Gourrierec T, Petit JC, Offenstadt G, Maury E, Brisse S, Arlet G. 2011. Emerging severe and fatal infections due to Klebsiella pneumoniae in two university hospitals in France. J Clin Microbiol 49:3012–3014. doi:10.1128/JCM.00676-11. - DOI - PMC - PubMed
1. Iwasaki Y, Inokuchi R, Harada S, Aoki K, Ishii Y, Shinohara K. 2017. Bacterial meningitis caused by hypervirulent Klebsiella pneumoniae capsular genotype K54 with development of granuloma-like nodal enhancement in the brain during the subacute phase. Intern Med 56:373–376. doi:10.2169/internalmedicine.56.7384. - DOI - PMC - PubMed

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[1] Wang JH, Liu YC, Lee SS, Yen MY, Chen YS, Wang JH, Wann SR, Lin HH. 1998. Primary liver abscess due to Klebsiella pneumoniae in Taiwan. Clin Infect Dis 26:1434–1438. doi:10.1086/516369. - DOI - PubMed

[2] Wang JH, Liu YC, Lee SS, Yen MY, Chen YS, Wang JH, Wann SR, Lin HH. 1998. Primary liver abscess due to Klebsiella pneumoniae in Taiwan. Clin Infect Dis 26:1434–1438. doi:10.1086/516369. - DOI - PubMed

[3] Chuang YP, Fang CT, Lai SY, Chang SC, Wang JT. 2006. Genetic determinants of capsular serotype K1 of Klebsiella pneumoniae causing primary pyogenic liver abscess. J Infect Dis 193:645–654. doi:10.1086/499968. - DOI - PubMed

[4] Chuang YP, Fang CT, Lai SY, Chang SC, Wang JT. 2006. Genetic determinants of capsular serotype K1 of Klebsiella pneumoniae causing primary pyogenic liver abscess. J Infect Dis 193:645–654. doi:10.1086/499968. - DOI - PubMed

[5] Brisse S, Fevre C, Passet V, Issenhuth-Jeanjean S, Tournebize R, Diancourt L, Grimont P. 2009. Virulent clones of Klebsiella pneumoniae: identification and evolutionary scenario based on genomic and phenotypic characterization. PLoS One 4:e4982. doi:10.1371/journal.pone.0004982. - DOI - PMC - PubMed

[6] Brisse S, Fevre C, Passet V, Issenhuth-Jeanjean S, Tournebize R, Diancourt L, Grimont P. 2009. Virulent clones of Klebsiella pneumoniae: identification and evolutionary scenario based on genomic and phenotypic characterization. PLoS One 4:e4982. doi:10.1371/journal.pone.0004982. - DOI - PMC - PubMed

[7] Decré D, Verdet C, Emirian A, Le Gourrierec T, Petit JC, Offenstadt G, Maury E, Brisse S, Arlet G. 2011. Emerging severe and fatal infections due to Klebsiella pneumoniae in two university hospitals in France. J Clin Microbiol 49:3012–3014. doi:10.1128/JCM.00676-11. - DOI - PMC - PubMed

[8] Decré D, Verdet C, Emirian A, Le Gourrierec T, Petit JC, Offenstadt G, Maury E, Brisse S, Arlet G. 2011. Emerging severe and fatal infections due to Klebsiella pneumoniae in two university hospitals in France. J Clin Microbiol 49:3012–3014. doi:10.1128/JCM.00676-11. - DOI - PMC - PubMed

[9] Iwasaki Y, Inokuchi R, Harada S, Aoki K, Ishii Y, Shinohara K. 2017. Bacterial meningitis caused by hypervirulent Klebsiella pneumoniae capsular genotype K54 with development of granuloma-like nodal enhancement in the brain during the subacute phase. Intern Med 56:373–376. doi:10.2169/internalmedicine.56.7384. - DOI - PMC - PubMed

[10] Iwasaki Y, Inokuchi R, Harada S, Aoki K, Ishii Y, Shinohara K. 2017. Bacterial meningitis caused by hypervirulent Klebsiella pneumoniae capsular genotype K54 with development of granuloma-like nodal enhancement in the brain during the subacute phase. Intern Med 56:373–376. doi:10.2169/internalmedicine.56.7384. - DOI - PMC - PubMed

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Clinical and Molecular Characteristics of Klebsiella pneumoniae Isolates Causing Bloodstream Infections in Japan: Occurrence of Hypervirulent Infections in Health Care

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Clinical and Molecular Characteristics of Klebsiella pneumoniae Isolates Causing Bloodstream Infections in Japan: Occurrence of Hypervirulent Infections in Health Care

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