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Published in: BMC Infectious Diseases 1/2020

01-12-2020 | Acute Gastroenteritis | Research article

Molecular characteristics of Clostridium difficile in children with acute gastroenteritis from Zhejiang

Authors: Huiqun Shuai, Qiao Bian, Yun Luo, Xiaohong Zhou, Xiaojun Song, Julian Ye, Qinghong Huang, Zhaoyang Peng, Jun Wu, Jianmin Jiang, Dazhi Jin

Published in: BMC Infectious Diseases | Issue 1/2020

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Abstract

Background

Clostridium difficile infection (CDI) has an increasing pediatric prevalence worldwide. However, molecular characteristics of C. difficile in Chinese children with acute gastroenteritis have not been reported.

Methods

A five-year cross-sectional study was conducted in a tertiary children’s hospital in Zhejiang. Consecutive stool specimens from outpatient children with acute gastroenteritis were cultured for C. difficile, and isolates then were analyzed for toxin genes, multi-locus sequence type and antimicrobial resistance. Diarrhea-related viruses were detected, and demographic data were collected.

Results

A total of 115 CDI cases (14.3%), and 69 co-infected cases with both viruses and toxigenic C. difficile, were found in the 804 stool samples. The 186 C. difficile isolates included 6 of toxin A-positive/toxin B-positive/binary toxin-positive (A+B+CDT+), 139 of A+B+CDT, 3 of AB+CDT+, 36 of AB+CDT and 2 of ABCDT. Sequence types 26 (17.7%), 35 (11.3%), 39 (12.4%), 54 (16.7%), and 152 (11.3%) were major genotypes with significant differences among different antimicrobial resistances (Fisher's exact test, P < 0.001). The AB+ isolates had significantly higher resistance, compared to erythromycin, rifampin, moxifloxacin, and gatifloxacin, than that of the A+B+ (χ2 = 7.78 to 29.26, P < 0.01). The positive CDI rate in infants (16.2%) was significantly higher than that of children over 1 year old (10.8%) (χ2 = 4.39, P = 0.036).

Conclusions

CDI has been revealed as a major cause of acute gastroenteritis in children with various genotypes. The role of toxigenic C. difficile and risk factors of CDI should be emphatically considered in subsequent diarrhea surveillance in children from China.
Literature
1.
go back to reference Rupnik M, Wilcox MH, Gerding DN. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol. 2009;7(7):526–36.PubMedCrossRef Rupnik M, Wilcox MH, Gerding DN. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol. 2009;7(7):526–36.PubMedCrossRef
2.
go back to reference Lessa FC, Mu Y, Bamberg WM, Beldavs ZG, Dumyati GK, Dunn JR, et al. Burden of Clostridium difficile infection in the United States. N Engl J Med. 2015;372(9):825–34.PubMedCrossRef Lessa FC, Mu Y, Bamberg WM, Beldavs ZG, Dumyati GK, Dunn JR, et al. Burden of Clostridium difficile infection in the United States. N Engl J Med. 2015;372(9):825–34.PubMedCrossRef
3.
go back to reference Zilberberg MD, Tillotson GS, McDonald LC. Clostridium difficile infections among hospitalized children, United States, 1997-2006. Emerg Infect Dis. 2010;16(4):604–9.PubMedPubMedCentralCrossRef Zilberberg MD, Tillotson GS, McDonald LC. Clostridium difficile infections among hospitalized children, United States, 1997-2006. Emerg Infect Dis. 2010;16(4):604–9.PubMedPubMedCentralCrossRef
4.
go back to reference Kim J, Smathers SA, Prasad P, Leckerman KH, Coffin S, Zaoutis T. Epidemiological features of Clostridium difficile-associated disease among inpatients at children's hospitals in the United States, 2001–2006. Pediatrics. 2008;122(6):1266–70.PubMedCrossRef Kim J, Smathers SA, Prasad P, Leckerman KH, Coffin S, Zaoutis T. Epidemiological features of Clostridium difficile-associated disease among inpatients at children's hospitals in the United States, 2001–2006. Pediatrics. 2008;122(6):1266–70.PubMedCrossRef
5.
go back to reference Spigaglia P, Barbanti F, Castagnola E, Diana MC, Pescetto L, Bandettini R. Clostridium difficile causing pediatric infections: new findings from a hospital-based study in Italy. Anaerobe. 2017;48:262–8.PubMedCrossRef Spigaglia P, Barbanti F, Castagnola E, Diana MC, Pescetto L, Bandettini R. Clostridium difficile causing pediatric infections: new findings from a hospital-based study in Italy. Anaerobe. 2017;48:262–8.PubMedCrossRef
6.
go back to reference Malmqvist L, Ullberg M, Hed Myrberg I, Nilsson A. Clostridium difficile infection in children: epidemiology and trend in a Swedish tertiary care hospital. Pediatr Infect Dis J. 2019;38(12):1208–13.PubMedCrossRef Malmqvist L, Ullberg M, Hed Myrberg I, Nilsson A. Clostridium difficile infection in children: epidemiology and trend in a Swedish tertiary care hospital. Pediatr Infect Dis J. 2019;38(12):1208–13.PubMedCrossRef
7.
go back to reference Kim DH, Jin MC, Yang HR. Clostridium difficile infection at diagnosis and during the disease course of pediatric inflammatory bowel disease. Pediatr Gastroenterol Hepatol Nutr. 2018;21(1):43–50.PubMedPubMedCentralCrossRef Kim DH, Jin MC, Yang HR. Clostridium difficile infection at diagnosis and during the disease course of pediatric inflammatory bowel disease. Pediatr Gastroenterol Hepatol Nutr. 2018;21(1):43–50.PubMedPubMedCentralCrossRef
8.
go back to reference Daida A, Yoshihara H, Inai I, Hasegawa D, Ishida Y, Urayama KY, et al. Risk factors for hospital-acquired Clostridium difficile infection among pediatric patients with Cancer. J Pediatr Hematol Oncol. 2017;39(3):e167–e72.PubMedCrossRef Daida A, Yoshihara H, Inai I, Hasegawa D, Ishida Y, Urayama KY, et al. Risk factors for hospital-acquired Clostridium difficile infection among pediatric patients with Cancer. J Pediatr Hematol Oncol. 2017;39(3):e167–e72.PubMedCrossRef
9.
go back to reference Kim A, Chang JY, Shin S, Yi H, Moon JS, Ko JS, et al. Epidemiology and factors related to clinical severity of acute gastroenteritis in hospitalized children after the introduction of rotavirus vaccination. J Korean Med Sci. 2017;32(3):465–74.PubMedPubMedCentralCrossRef Kim A, Chang JY, Shin S, Yi H, Moon JS, Ko JS, et al. Epidemiology and factors related to clinical severity of acute gastroenteritis in hospitalized children after the introduction of rotavirus vaccination. J Korean Med Sci. 2017;32(3):465–74.PubMedPubMedCentralCrossRef
10.
go back to reference Stokely JN, Niendorf S, Taube S, Hoehne M, Young VB, Rogers MA, et al. Prevalence of human Norovirus and Clostridium Difficile Coinfections in adult hospitalized patients. Clin Epidemiol. 2016;8:253–60.PubMedPubMedCentralCrossRef Stokely JN, Niendorf S, Taube S, Hoehne M, Young VB, Rogers MA, et al. Prevalence of human Norovirus and Clostridium Difficile Coinfections in adult hospitalized patients. Clin Epidemiol. 2016;8:253–60.PubMedPubMedCentralCrossRef
11.
go back to reference Lees EA, Carrol ED, Ellaby NAF, Roberts P, Corless CE, Lenzi L, et al. Characterization of circulating Clostridium difficile strains, host response and intestinal microbiome in hospitalized children with diarrhea. Pediatr Infect Dis J. 2020;39(3):221–8.PubMedCrossRef Lees EA, Carrol ED, Ellaby NAF, Roberts P, Corless CE, Lenzi L, et al. Characterization of circulating Clostridium difficile strains, host response and intestinal microbiome in hospitalized children with diarrhea. Pediatr Infect Dis J. 2020;39(3):221–8.PubMedCrossRef
12.
go back to reference Graaf HD, Pai S, Burns DA, Karas JA, Enoch DA, Faust SN. Co-infection as a confounder for the role of Clostridium difficile infection in children with diarrhoea: a summary of the literature. Eur J Clin Microbiol Infect Dis. 2015;34(7):1281–7.PubMedCrossRef Graaf HD, Pai S, Burns DA, Karas JA, Enoch DA, Faust SN. Co-infection as a confounder for the role of Clostridium difficile infection in children with diarrhoea: a summary of the literature. Eur J Clin Microbiol Infect Dis. 2015;34(7):1281–7.PubMedCrossRef
13.
go back to reference McDonald LC, Gerding DN, Johnson S, Bakken JS, Carroll KC, Coffin SE, et al. Clinical practice guidelines for Clostridium difficile infection in adults and children: 2017 update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clin Infect Dis. 2018;66(7):e1–e48.PubMedPubMedCentralCrossRef McDonald LC, Gerding DN, Johnson S, Bakken JS, Carroll KC, Coffin SE, et al. Clinical practice guidelines for Clostridium difficile infection in adults and children: 2017 update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clin Infect Dis. 2018;66(7):e1–e48.PubMedPubMedCentralCrossRef
14.
go back to reference Pai S, Aliyu SH, Enoch DA, Karas JA. Five years experience of Clostridium difficile infection in children at a UK tertiary hospital: proposed criteria for diagnosis and management. PLoS One. 2012;7(12):e51728.PubMedPubMedCentralCrossRef Pai S, Aliyu SH, Enoch DA, Karas JA. Five years experience of Clostridium difficile infection in children at a UK tertiary hospital: proposed criteria for diagnosis and management. PLoS One. 2012;7(12):e51728.PubMedPubMedCentralCrossRef
15.
go back to reference Hao R, Li P, Wang Y, Qiu S, Wang L, Li Z, et al. Diversity of pathogens responsible for acute diarrheal disease in China. Clin Infect Dis. 2013;57(12):1788–90.PubMedCrossRef Hao R, Li P, Wang Y, Qiu S, Wang L, Li Z, et al. Diversity of pathogens responsible for acute diarrheal disease in China. Clin Infect Dis. 2013;57(12):1788–90.PubMedCrossRef
16.
go back to reference Chen YB, Gu SL, Shen P, Lv T, Fang YH, Tang LL, et al. Molecular epidemiology and antimicrobial susceptibility of Clostridium difficile isolated from hospitals during a 4-year period in China. J Med Microbiol. 2017;67(1):52–9.PubMedCrossRef Chen YB, Gu SL, Shen P, Lv T, Fang YH, Tang LL, et al. Molecular epidemiology and antimicrobial susceptibility of Clostridium difficile isolated from hospitals during a 4-year period in China. J Med Microbiol. 2017;67(1):52–9.PubMedCrossRef
17.
go back to reference Fang WJ, Jing DZ, Luo Y, Fu CY, Zhao P, Qian J, et al. Clostridium difficile carriage in hospitalized cancer patients: a prospective investigation in eastern China. BMC Infect Dis. 2014;14(1):523.PubMedPubMedCentralCrossRef Fang WJ, Jing DZ, Luo Y, Fu CY, Zhao P, Qian J, et al. Clostridium difficile carriage in hospitalized cancer patients: a prospective investigation in eastern China. BMC Infect Dis. 2014;14(1):523.PubMedPubMedCentralCrossRef
18.
go back to reference Gu SL, Chen YB, Lv T, Zhang XW, Wei ZQ, Shen P, et al. Risk factors, outcomes and epidemiology associated with Clostridium difficile infection in patients with haematological malignancies in a tertiary care hospital in China. J Med Microbiol. 2015;64(Pt 3):209–16.PubMedCrossRef Gu SL, Chen YB, Lv T, Zhang XW, Wei ZQ, Shen P, et al. Risk factors, outcomes and epidemiology associated with Clostridium difficile infection in patients with haematological malignancies in a tertiary care hospital in China. J Med Microbiol. 2015;64(Pt 3):209–16.PubMedCrossRef
19.
go back to reference Ye GY, Li N, Chen YB, Lv T, Shen P, Gu SL, et al. Clostridium difficile carriage in healthy pregnant women in China. Anaerobe. 2016;37:54–7.PubMedCrossRef Ye GY, Li N, Chen YB, Lv T, Shen P, Gu SL, et al. Clostridium difficile carriage in healthy pregnant women in China. Anaerobe. 2016;37:54–7.PubMedCrossRef
20.
go back to reference Huang H, Wu S, Chen R, Xu S, Fang H, Weintraub A, et al. Risk factors of Clostridium difficile infections among patients in a university hospital in Shanghai. China Anaerobe. 2014;30:65–9.PubMedCrossRef Huang H, Wu S, Chen R, Xu S, Fang H, Weintraub A, et al. Risk factors of Clostridium difficile infections among patients in a university hospital in Shanghai. China Anaerobe. 2014;30:65–9.PubMedCrossRef
21.
go back to reference Cui QQ, Yang J, Niu YN, Qiang CX, Li ZR, Xu KY, et al. Epidemiological investigation of Clostridioides difficile colonization in Chinese community infants. Anaerobe. 2019;56:116–23.PubMedCrossRef Cui QQ, Yang J, Niu YN, Qiang CX, Li ZR, Xu KY, et al. Epidemiological investigation of Clostridioides difficile colonization in Chinese community infants. Anaerobe. 2019;56:116–23.PubMedCrossRef
22.
go back to reference Tian TT, Zhao JH, Yang J, Qiang CX, Li ZR, Chen J, et al. Molecular characterization of Clostridium difficile isolates from human subjects and the environment. PLoS One. 2016;11(3):e0151964.PubMedPubMedCentralCrossRef Tian TT, Zhao JH, Yang J, Qiang CX, Li ZR, Chen J, et al. Molecular characterization of Clostridium difficile isolates from human subjects and the environment. PLoS One. 2016;11(3):e0151964.PubMedPubMedCentralCrossRef
23.
go back to reference Cohen SH, Gerding DN, Johnson S, Kelly CP, Loo VG, Mcdonald LC, et al. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infect Control Hosp Epidemiol. 2010;31(5):431–55.PubMedCrossRef Cohen SH, Gerding DN, Johnson S, Kelly CP, Loo VG, Mcdonald LC, et al. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infect Control Hosp Epidemiol. 2010;31(5):431–55.PubMedCrossRef
24.
go back to reference McDonald LC, Coignard B, Dubberke E, Song X, Horan T, Kutty PK. Recommendations for surveillance of Clostridium difficile–associated disease. Infect Control Hosp Epidemiol. 2007;28(2):140–5.PubMedCrossRef McDonald LC, Coignard B, Dubberke E, Song X, Horan T, Kutty PK. Recommendations for surveillance of Clostridium difficile–associated disease. Infect Control Hosp Epidemiol. 2007;28(2):140–5.PubMedCrossRef
25.
go back to reference Jin D, Luo Y, Huang C, Cai J, Ye J, Zheng Y, et al. Molecular epidemiology of Clostridium difficile infection in hospitalized patients in eastern China. J Clin Microbiol. 2017;55(3):801–10.PubMedPubMedCentralCrossRef Jin D, Luo Y, Huang C, Cai J, Ye J, Zheng Y, et al. Molecular epidemiology of Clostridium difficile infection in hospitalized patients in eastern China. J Clin Microbiol. 2017;55(3):801–10.PubMedPubMedCentralCrossRef
26.
go back to reference McDonald LC, Killgore GE, Thompson A, Owens RCJ, Kazakova SV, Sambol SP, et al. An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med. 2005;353(23):2433–41.PubMedCrossRef McDonald LC, Killgore GE, Thompson A, Owens RCJ, Kazakova SV, Sambol SP, et al. An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med. 2005;353(23):2433–41.PubMedCrossRef
27.
go back to reference Ludovic L, Dhalluin A, Testelin S, Mattrat MA, Maillard K, Lemeland JF, et al. Multiplex PCR targeting tpi (triose phosphate isomerase), tcdA (toxin a), and tcdB (toxin B) genes for toxigenic culture of Clostridium difficile. J Clin Microbiol. 2004;42(12):5710–4.CrossRef Ludovic L, Dhalluin A, Testelin S, Mattrat MA, Maillard K, Lemeland JF, et al. Multiplex PCR targeting tpi (triose phosphate isomerase), tcdA (toxin a), and tcdB (toxin B) genes for toxigenic culture of Clostridium difficile. J Clin Microbiol. 2004;42(12):5710–4.CrossRef
28.
go back to reference Griffiths D, Fawley W, Kachrimanidou M, Bowden R, Crook DW, Fung R, et al. Multilocus sequence typing of Clostridium difficile. J Clin Microbiol. 2010;48(3):770–8.PubMedCrossRef Griffiths D, Fawley W, Kachrimanidou M, Bowden R, Crook DW, Fung R, et al. Multilocus sequence typing of Clostridium difficile. J Clin Microbiol. 2010;48(3):770–8.PubMedCrossRef
29.
go back to reference Gonçalves C, Decré D, Barbut F, Burghoffer B, Petit J-C. Prevalence and characterization of a binary toxin (actin-specific ADP-ribosyltransferase) from Clostridium difficile. J Clin Microbiol. 2004;42(5):1933–9.PubMedPubMedCentralCrossRef Gonçalves C, Decré D, Barbut F, Burghoffer B, Petit J-C. Prevalence and characterization of a binary toxin (actin-specific ADP-ribosyltransferase) from Clostridium difficile. J Clin Microbiol. 2004;42(5):1933–9.PubMedPubMedCentralCrossRef
30.
go back to reference Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing of anaerobic bacteria. M11-A8: National Committee for Clinical and Laboratory Standards. Wayne, PA; 2017. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing of anaerobic bacteria. M11-A8: National Committee for Clinical and Laboratory Standards. Wayne, PA; 2017.
31.
go back to reference Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–81.PubMedCrossRef Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–81.PubMedCrossRef
32.
go back to reference Spigaglia P, Barbanti F, Mastrantonio P. Detection of a genetic linkage between genes coding for resistance to tetracycline and erythromycin in Clostridium difficile. Microb Drug Resist. 2007;13(2):90–5.PubMedCrossRef Spigaglia P, Barbanti F, Mastrantonio P. Detection of a genetic linkage between genes coding for resistance to tetracycline and erythromycin in Clostridium difficile. Microb Drug Resist. 2007;13(2):90–5.PubMedCrossRef
33.
go back to reference Schmidt C, Löffler B, Ackermann G. Antimicrobial phenotypes and molecular basis in clinical strains of Clostridium difficile. Diagn Microbiol Infect Dis. 2007;59(1):1–5.PubMedCrossRef Schmidt C, Löffler B, Ackermann G. Antimicrobial phenotypes and molecular basis in clinical strains of Clostridium difficile. Diagn Microbiol Infect Dis. 2007;59(1):1–5.PubMedCrossRef
34.
go back to reference Enoch DA, Butler MJ, Pai S, Aliyu SH, Karas JA. Clostridium difficile in children: colonisation and disease. J Inf Secur. 2011;63(2):105–13. Enoch DA, Butler MJ, Pai S, Aliyu SH, Karas JA. Clostridium difficile in children: colonisation and disease. J Inf Secur. 2011;63(2):105–13.
35.
go back to reference Jangi S, Lamont JT. Asymptomatic colonization by Clostridium difficile in infants: implications for disease in later life. J Pediatr Gastr Nutr. 2010;51(1):2–7.CrossRef Jangi S, Lamont JT. Asymptomatic colonization by Clostridium difficile in infants: implications for disease in later life. J Pediatr Gastr Nutr. 2010;51(1):2–7.CrossRef
36.
go back to reference Centers for Disease Control and Prevention. Surveillance for community-associated Clostridium difficile--Connecticut, 2006. MMWR Morb Mortal Wkly Rep. 2008;57(13):340–3. Centers for Disease Control and Prevention. Surveillance for community-associated Clostridium difficile--Connecticut, 2006. MMWR Morb Mortal Wkly Rep. 2008;57(13):340–3.
37.
go back to reference Benson L, Song X, Campos J, Singh N. Changing epidemiology of Clostridium difficile-associated disease in children. Infect Control Hosp Epidemiol. 2007;28(11):1233–5.PubMedCrossRef Benson L, Song X, Campos J, Singh N. Changing epidemiology of Clostridium difficile-associated disease in children. Infect Control Hosp Epidemiol. 2007;28(11):1233–5.PubMedCrossRef
38.
go back to reference Adams DJ, Eberly MD, Rajnik M, Nylund CM. Risk factors for community-associated Clostridium difficile infection in children. J Pediatr. 2017;1(Suppl 1):105–9.CrossRef Adams DJ, Eberly MD, Rajnik M, Nylund CM. Risk factors for community-associated Clostridium difficile infection in children. J Pediatr. 2017;1(Suppl 1):105–9.CrossRef
39.
go back to reference Predrag S, Branislava K, Nikola S, Niko R, Zorica SR, Stanković-Đorđević D. Community-acquired Clostridium difficile infection in Serbian pediatric population. Eur J Clin Microbiol Infect Dis. 2018;37(6):1061–9.PubMedCrossRef Predrag S, Branislava K, Nikola S, Niko R, Zorica SR, Stanković-Đorđević D. Community-acquired Clostridium difficile infection in Serbian pediatric population. Eur J Clin Microbiol Infect Dis. 2018;37(6):1061–9.PubMedCrossRef
40.
go back to reference Pechal A, Lin K, Allen S, Reveles K. National age group trends in Clostridium difficile infection incidence and health outcomes in United States community hospitals. BMC Infect Dis. 2016;16(1):682–7.PubMedPubMedCentralCrossRef Pechal A, Lin K, Allen S, Reveles K. National age group trends in Clostridium difficile infection incidence and health outcomes in United States community hospitals. BMC Infect Dis. 2016;16(1):682–7.PubMedPubMedCentralCrossRef
41.
go back to reference Liao F, Li W, Gu W, Zhang W, Liu X, Fu X, et al. A retrospective study of community-acquired Clostridium difficile infection in Southwest China. Sci Rep. 2018;8(1):3992–4002.PubMedPubMedCentralCrossRef Liao F, Li W, Gu W, Zhang W, Liu X, Fu X, et al. A retrospective study of community-acquired Clostridium difficile infection in Southwest China. Sci Rep. 2018;8(1):3992–4002.PubMedPubMedCentralCrossRef
42.
go back to reference Denno DM, Stapp JR, Boster DR, Qin X, Clausen CR, Del Beccaro KH, et al. Etiology of diarrhea in pediatric outpatient settings. Pediatr Infect Dis J. 2005;24(2):142–8.PubMedCrossRef Denno DM, Stapp JR, Boster DR, Qin X, Clausen CR, Del Beccaro KH, et al. Etiology of diarrhea in pediatric outpatient settings. Pediatr Infect Dis J. 2005;24(2):142–8.PubMedCrossRef
43.
go back to reference Taori SK, Wroe A, Hardie A, Gibb AP, Poxton IR. A prospective study of community-associated Clostridium difficile infections: the role of antibiotics and co-infections. J Inf Secur. 2014;69(2):134–44. Taori SK, Wroe A, Hardie A, Gibb AP, Poxton IR. A prospective study of community-associated Clostridium difficile infections: the role of antibiotics and co-infections. J Inf Secur. 2014;69(2):134–44.
44.
go back to reference Borali E, Ortisi G, Moretti C, Stacul EF, Lipreri R, Gesu GP, et al. Community-acquired Clostridium difficile infection in children: a retrospective study. Dig Liver Dis. 2015;47(10):842–6.PubMedCrossRef Borali E, Ortisi G, Moretti C, Stacul EF, Lipreri R, Gesu GP, et al. Community-acquired Clostridium difficile infection in children: a retrospective study. Dig Liver Dis. 2015;47(10):842–6.PubMedCrossRef
45.
go back to reference Tang C, Cui L, Xu Y, Xie L, Sun P, Liu C, et al. The incidence and drug resistance of Clostridium difficile infection in mainland China: a systematic review and meta-analysis. Sci Rep. 2016;6:37865.PubMedPubMedCentralCrossRef Tang C, Cui L, Xu Y, Xie L, Sun P, Liu C, et al. The incidence and drug resistance of Clostridium difficile infection in mainland China: a systematic review and meta-analysis. Sci Rep. 2016;6:37865.PubMedPubMedCentralCrossRef
46.
go back to reference Boschi-Pinto C, Lanata CF, Black RE. The global burden of childhood diarrhea. Matern Child Health: Springer; 2009. p. 225–43. Boschi-Pinto C, Lanata CF, Black RE. The global burden of childhood diarrhea. Matern Child Health: Springer; 2009. p. 225–43.
47.
go back to reference Mobeen F, Sharma V, Tulika P. Enterotype variations of the healthy human gut microbiome in different geographical regions. Bioinformation. 2018;14(9):560–73.PubMedPubMedCentralCrossRef Mobeen F, Sharma V, Tulika P. Enterotype variations of the healthy human gut microbiome in different geographical regions. Bioinformation. 2018;14(9):560–73.PubMedPubMedCentralCrossRef
48.
go back to reference Luo Y, Cheong E, Bian Q, Collins DA, Ye J, Shin JH, et al. Different molecular characteristics and antimicrobial resistance profiles of Clostridium difficile in the Asia-Pacific region. Emerg Microbes Infec. 2019;8(1):1553–62.CrossRef Luo Y, Cheong E, Bian Q, Collins DA, Ye J, Shin JH, et al. Different molecular characteristics and antimicrobial resistance profiles of Clostridium difficile in the Asia-Pacific region. Emerg Microbes Infec. 2019;8(1):1553–62.CrossRef
49.
go back to reference Luo Y, Zhang W, Cheng JW, Xiao M, Sun GR, Guo CJ, et al. Molecular epidemiology of Clostridium difficile in two tertiary care hospitals in Shandong Province, China. Infect Drug Resist. 2018;11:489–500.PubMedPubMedCentralCrossRef Luo Y, Zhang W, Cheng JW, Xiao M, Sun GR, Guo CJ, et al. Molecular epidemiology of Clostridium difficile in two tertiary care hospitals in Shandong Province, China. Infect Drug Resist. 2018;11:489–500.PubMedPubMedCentralCrossRef
50.
go back to reference Stoesser N, Crook DW, Fung R, Griffiths D, Harding RM, Kachrimanidou M, et al. Molecular epidemiology of Clostridium difficile strains in children compared with that of strains circulating in adults with Clostridium difficile-associated infection. J Clin Microbiol. 2011;49(11):3994–6.PubMedPubMedCentralCrossRef Stoesser N, Crook DW, Fung R, Griffiths D, Harding RM, Kachrimanidou M, et al. Molecular epidemiology of Clostridium difficile strains in children compared with that of strains circulating in adults with Clostridium difficile-associated infection. J Clin Microbiol. 2011;49(11):3994–6.PubMedPubMedCentralCrossRef
51.
go back to reference Zhao L, Luo Y, Bian Q, Wang L, Ye J, Song X, et al. High-level resistance of toxigenic Clostridioides difficile genotype to macrolide-Lincosamide-Streptogramin B in community acquired patients in eastern China. Infect Drug Resist. 2020;13:171–81.PubMedPubMedCentralCrossRef Zhao L, Luo Y, Bian Q, Wang L, Ye J, Song X, et al. High-level resistance of toxigenic Clostridioides difficile genotype to macrolide-Lincosamide-Streptogramin B in community acquired patients in eastern China. Infect Drug Resist. 2020;13:171–81.PubMedPubMedCentralCrossRef
52.
go back to reference Chatedaki C, Voulgaridi I, Kachrimanidou M, Hrabak J, Papagiannitsis CC, Petinaki E. Antimicrobial susceptibility and mechanisms of resistance of Greek Clostridium difficile clinical isolates. J Glo Antimicrob Resist. 2019;16:53–8.CrossRef Chatedaki C, Voulgaridi I, Kachrimanidou M, Hrabak J, Papagiannitsis CC, Petinaki E. Antimicrobial susceptibility and mechanisms of resistance of Greek Clostridium difficile clinical isolates. J Glo Antimicrob Resist. 2019;16:53–8.CrossRef
53.
go back to reference Kachrimanidou M, Tzika E, Filioussis G. Clostridioides (Clostridium) difficile in food-producing animals, horses and household pets: a comprehensive review. Microorganisms. 2019;7(12):667.PubMedCentralCrossRef Kachrimanidou M, Tzika E, Filioussis G. Clostridioides (Clostridium) difficile in food-producing animals, horses and household pets: a comprehensive review. Microorganisms. 2019;7(12):667.PubMedCentralCrossRef
Metadata
Title
Molecular characteristics of Clostridium difficile in children with acute gastroenteritis from Zhejiang
Authors
Huiqun Shuai
Qiao Bian
Yun Luo
Xiaohong Zhou
Xiaojun Song
Julian Ye
Qinghong Huang
Zhaoyang Peng
Jun Wu
Jianmin Jiang
Dazhi Jin
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2020
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-020-05030-6

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