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Published in: Gut Pathogens 1/2016

Open Access 01-12-2016 | Research

Prevalence and antibiotic resistance of bacterial pathogens isolated from childhood diarrhea in Beijing, China (2010–2014)

Authors: Mei Qu, Bing Lv, Xin Zhang, Hanqiu Yan, Ying Huang, Haikun Qian, Bo Pang, Lei Jia, Biao Kan, Quanyi Wang

Published in: Gut Pathogens | Issue 1/2016

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Abstract

Background

Diarrhea is one of the main causes of morbidity and mortality among children less than 5 years of age worldwide, and its causes vary by region. This study aimed to determine the etiologic spectrum, prevalent characteristics and antimicrobial resistance patterns of common enteropathogenic bacteria from diarrheagenic children in Beijing, the capital of China.

Methods

Stool samples were collected from 2524 outpatients who were aged 0–5 years in Beijing, China during 2010–2014. Microbiological methods, real-time PCR and antimicrobial susceptibility test were used to identify the bacterial causes and antimicrobial resistance patterns in the isolates.

Results

Of the 2524 patients screened, we identified the causes of 269 cases (10.7 %) as follows: diarrheagenic Escherichia coli (4.6 %), Salmonella (4.3 %), Shigella (1.4 %) and Vibrio parahaemolyticus (0.4 %). Atypical EPEC, Salmonella enteritidis, Shigella sonnei and serotype O3:K6 were the most common serogroups or serotypes of the four etiological bacteria. The prevalence of pathogens was correlated with age, season and clinical symptoms. The highest proportion of all causative bacteria was found in children aged 3–5 years and in summer. The clinical symptoms associated with specific bacterial infection, such as fever; abdominal pain; vomiting; and watery, mucus, and bloody stool, were observed frequently in diarrheal patients. Salmonella showed moderate rates of resistance (40–60 %) to ampicillin, nalidixic acid, streptomycin and sulfisoxazole. Resistance to at least three antimicrobials was found in 50 % of isolates. Of the top three serotypes in Salmonella, high-level antimicrobial resistance to single and multiple antibiotics was more common among Salmonella typhimurium and Salmonella 1, 4, [5], 12:i:- than among S. enteritidis. More than 90 % of Shigella isolates showed more alarming resistance to most antibiotics, with a widened spectrum compared to Salmonella.

Conclusion

Constant antibiotic surveillance is warranted because the bacteria were highly resistant to various antimicrobials. Our study contributes to the strengthening of the existing surveillance system and provides aid for effective prevention and control strategies for childhood diarrhea.
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Literature
1.
go back to reference Bryce J, Boschi-Pinto C, Shibuya K, Black RE, Group WHOCHER. WHO estimates of the causes of death in children. Lancet. 2005;365(9465):1147–52.CrossRefPubMed Bryce J, Boschi-Pinto C, Shibuya K, Black RE, Group WHOCHER. WHO estimates of the causes of death in children. Lancet. 2005;365(9465):1147–52.CrossRefPubMed
2.
go back to reference Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, et al. Global burden of childhood pneumonia and diarrhoea. Lancet. 2013;381(9875):1405–16.CrossRefPubMed Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, et al. Global burden of childhood pneumonia and diarrhoea. Lancet. 2013;381(9875):1405–16.CrossRefPubMed
3.
go back to reference Liu HX, Zhang J. Analysis of reported infectious diarrhea (other than cholera, dysentery, typhoid and paratyphoid) in China in 2011. Zhonghua Yu Fang Yi Xue Za Zhi. 2013;47(4):328–32.PubMed Liu HX, Zhang J. Analysis of reported infectious diarrhea (other than cholera, dysentery, typhoid and paratyphoid) in China in 2011. Zhonghua Yu Fang Yi Xue Za Zhi. 2013;47(4):328–32.PubMed
4.
go back to reference Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, et al. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet. 2012;379(9832):2151–61.CrossRefPubMed Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, et al. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet. 2012;379(9832):2151–61.CrossRefPubMed
5.
go back to reference Ran L, Wu S, Gao Y, Zhang X, Feng Z, Wang Z, et al. Laboratory-based surveillance of nontyphoidal Salmonella infections in China. Foodborne Pathog Dis. 2011;8(8):921–7.CrossRefPubMed Ran L, Wu S, Gao Y, Zhang X, Feng Z, Wang Z, et al. Laboratory-based surveillance of nontyphoidal Salmonella infections in China. Foodborne Pathog Dis. 2011;8(8):921–7.CrossRefPubMed
6.
go back to reference Zhang H, Pan F, Zhao X, Wang G, Tu Y, Fu S, et al. Distribution and antimicrobial resistance of enteric pathogens in Chinese paediatric diarrhoea: a multicentre retrospective study, 2008–2013. Epidemiol Infect. 2015;143(12):2512–9.CrossRefPubMed Zhang H, Pan F, Zhao X, Wang G, Tu Y, Fu S, et al. Distribution and antimicrobial resistance of enteric pathogens in Chinese paediatric diarrhoea: a multicentre retrospective study, 2008–2013. Epidemiol Infect. 2015;143(12):2512–9.CrossRefPubMed
7.
go back to reference Yu J, Jing H, Lai S, Xu W, Li M, Wu J, et al. Etiology of diarrhea among children under the age five in China: results from a 5-year surveillance. J Infect. 2015;71(1):19–27.CrossRefPubMed Yu J, Jing H, Lai S, Xu W, Li M, Wu J, et al. Etiology of diarrhea among children under the age five in China: results from a 5-year surveillance. J Infect. 2015;71(1):19–27.CrossRefPubMed
8.
go back to reference Qu M, Deng Y, Zhang X, Liu G, Huang Y, Lin C, et al. Etiology of acute diarrhea due to enteropathogenic bacteria in Beijing. China. J Infect. 2012;65(3):214–22.CrossRefPubMed Qu M, Deng Y, Zhang X, Liu G, Huang Y, Lin C, et al. Etiology of acute diarrhea due to enteropathogenic bacteria in Beijing. China. J Infect. 2012;65(3):214–22.CrossRefPubMed
9.
go back to reference Diniz-Santos DR, Santana JS, Barretto JR, Andrade MG, Silva LR. Epidemiological and microbiological aspects of acute bacterial diarrhea in children from Salvador, Bahia, Brazil. Braz J Infect Dis. 2005;9(1):77–83.CrossRefPubMed Diniz-Santos DR, Santana JS, Barretto JR, Andrade MG, Silva LR. Epidemiological and microbiological aspects of acute bacterial diarrhea in children from Salvador, Bahia, Brazil. Braz J Infect Dis. 2005;9(1):77–83.CrossRefPubMed
10.
go back to reference Moyo SJ, Gro N, Matee MI, Kitundu J, Myrmel H, Mylvaganam H, et al. Age specific aetiological agents of diarrhoea in hospitalized children aged less than 5 year in Dar es Salaam, Tanzania. BMC Pediatr. 2011;11:19.CrossRefPubMedPubMedCentral Moyo SJ, Gro N, Matee MI, Kitundu J, Myrmel H, Mylvaganam H, et al. Age specific aetiological agents of diarrhoea in hospitalized children aged less than 5 year in Dar es Salaam, Tanzania. BMC Pediatr. 2011;11:19.CrossRefPubMedPubMedCentral
11.
go back to reference Rathaur VK, Pathania M, Jayara A, Yadav N. Clinical study of acute childhood diarrhoea caused by bacterial enteropathogens. J Clin Diagn Res. 2014;8:PC01–5.PubMedPubMedCentral Rathaur VK, Pathania M, Jayara A, Yadav N. Clinical study of acute childhood diarrhoea caused by bacterial enteropathogens. J Clin Diagn Res. 2014;8:PC01–5.PubMedPubMedCentral
12.
go back to reference Jafari F, Garcia-Gil LJ, Salmanzadeh-Ahrabi S, Shokrzadeh L, Aslani MM, Pourhoseingholi MA, et al. Diagnosis and prevalence of enteropathogenic bacteria in children less than 5 years of age with acute diarrhea in Tehran children’s hospitals. J Infect. 2009;58(1):21–7.CrossRefPubMed Jafari F, Garcia-Gil LJ, Salmanzadeh-Ahrabi S, Shokrzadeh L, Aslani MM, Pourhoseingholi MA, et al. Diagnosis and prevalence of enteropathogenic bacteria in children less than 5 years of age with acute diarrhea in Tehran children’s hospitals. J Infect. 2009;58(1):21–7.CrossRefPubMed
13.
go back to reference Nic Fhogartaigh C, Dance DAB. Bacterial gastroenteritis. Medicine. 2013;41(12):693–9.CrossRef Nic Fhogartaigh C, Dance DAB. Bacterial gastroenteritis. Medicine. 2013;41(12):693–9.CrossRef
14.
go back to reference Thapar N, Sanderson IR. Diarrhoea in children: an interface between developing and developed countries. Lancet. 2004;363(9409):641–53.CrossRefPubMed Thapar N, Sanderson IR. Diarrhoea in children: an interface between developing and developed countries. Lancet. 2004;363(9409):641–53.CrossRefPubMed
16.
go back to reference Nguyen RN, Taylor LS, Tauschek M, Robins-Browne RM. Atypical enteropathogenic Escherichia coli infection and prolonged diarrhea in children. Emerg Infect Dis. 2006;12(4):597–603.CrossRefPubMedPubMedCentral Nguyen RN, Taylor LS, Tauschek M, Robins-Browne RM. Atypical enteropathogenic Escherichia coli infection and prolonged diarrhea in children. Emerg Infect Dis. 2006;12(4):597–603.CrossRefPubMedPubMedCentral
17.
go back to reference Nataro JP, Mai V, Johnson J, Blackwelder WC, Heimer R, Tirrell S, et al. Diarrheagenic Escherichia coli infection in Baltimore, Maryland, and New Haven, Connecticut. Clin Infect Dis. 2006;43(4):402–7.CrossRefPubMed Nataro JP, Mai V, Johnson J, Blackwelder WC, Heimer R, Tirrell S, et al. Diarrheagenic Escherichia coli infection in Baltimore, Maryland, and New Haven, Connecticut. Clin Infect Dis. 2006;43(4):402–7.CrossRefPubMed
18.
go back to reference Nair GB, Ramamurthy T, Bhattacharya MK, Krishnan T, Ganguly S, Saha DR, et al. Emerging trends in the etiology of enteric pathogens as evidenced from an active surveillance of hospitalized diarrhoeal patients in Kolkata, India. Gut Pathog. 2010;2(1):4.CrossRefPubMedPubMedCentral Nair GB, Ramamurthy T, Bhattacharya MK, Krishnan T, Ganguly S, Saha DR, et al. Emerging trends in the etiology of enteric pathogens as evidenced from an active surveillance of hospitalized diarrhoeal patients in Kolkata, India. Gut Pathog. 2010;2(1):4.CrossRefPubMedPubMedCentral
19.
go back to reference Saeed A, Abd H, Sandstrom G. Microbial aetiology of acute diarrhoea in children under 5 years of age in Khartoum, Sudan. J Med Microbiol. 2015;64(Pt 4):432–7.CrossRefPubMedPubMedCentral Saeed A, Abd H, Sandstrom G. Microbial aetiology of acute diarrhoea in children under 5 years of age in Khartoum, Sudan. J Med Microbiol. 2015;64(Pt 4):432–7.CrossRefPubMedPubMedCentral
20.
go back to reference Al-Gallas N, Bahri O, Bouratbeen A, Ben Haasen A, Ben Aissa R. Etiology of acute diarrhea in children and adults in Tunis, Tunisia, with emphasis on diarrheagenic Escherichia coli: prevalence, phenotyping, and molecular epidemiology. Am J Trop Med Hyg. 2007;77(3):571–82.PubMed Al-Gallas N, Bahri O, Bouratbeen A, Ben Haasen A, Ben Aissa R. Etiology of acute diarrhea in children and adults in Tunis, Tunisia, with emphasis on diarrheagenic Escherichia coli: prevalence, phenotyping, and molecular epidemiology. Am J Trop Med Hyg. 2007;77(3):571–82.PubMed
21.
go back to reference Ke B, Sun J, He D, Li X, Liang Z, Ke CW. Serovar distribution, antimicrobial resistance profiles, and PFGE typing of Salmonella enterica strains isolated from 2007 to 2012 in Guangdong, China. BMC Infect Dis. 2014;14:338.CrossRefPubMedPubMedCentral Ke B, Sun J, He D, Li X, Liang Z, Ke CW. Serovar distribution, antimicrobial resistance profiles, and PFGE typing of Salmonella enterica strains isolated from 2007 to 2012 in Guangdong, China. BMC Infect Dis. 2014;14:338.CrossRefPubMedPubMedCentral
22.
go back to reference Switt AI, Soyer Y, Warnick LD, Wiedmann M. Emergence, distribution, and molecular and phenotypic characteristics of Salmonella enterica serotype 4,5,12:i. Foodborne Pathog Dis. 2009;6(4):407–15.CrossRefPubMedPubMedCentral Switt AI, Soyer Y, Warnick LD, Wiedmann M. Emergence, distribution, and molecular and phenotypic characteristics of Salmonella enterica serotype 4,5,12:i. Foodborne Pathog Dis. 2009;6(4):407–15.CrossRefPubMedPubMedCentral
23.
go back to reference Niyogi SK, Pazhani GP. Multiresistant Shigella species isolated from childhood diarrhea cases in Kolkata, India. Jpn J Infect Dis. 2003;56(1):33–4.PubMed Niyogi SK, Pazhani GP. Multiresistant Shigella species isolated from childhood diarrhea cases in Kolkata, India. Jpn J Infect Dis. 2003;56(1):33–4.PubMed
24.
go back to reference Bangtrakulnonth A, Vieira AR, Lo Fo Wong DM, Pornreongwong S, Pulsrikarn C, Sawanpanyalert P, et al. Shigella from humans in Thailand during 1993–2006: spatial-time trends in species and serotype distribution. Foodborne Pathog Dis. 2008;5(6):773–84.CrossRefPubMed Bangtrakulnonth A, Vieira AR, Lo Fo Wong DM, Pornreongwong S, Pulsrikarn C, Sawanpanyalert P, et al. Shigella from humans in Thailand during 1993–2006: spatial-time trends in species and serotype distribution. Foodborne Pathog Dis. 2008;5(6):773–84.CrossRefPubMed
25.
go back to reference Vinh H, Nhu NT, Nga TV, Duy PT, Campbell JI, Hoang NV, et al. A changing picture of shigellosis in southern Vietnam: shifting species dominance, antimicrobial susceptibility and clinical presentation. BMC Infect Dis. 2009;9:204.CrossRefPubMedPubMedCentral Vinh H, Nhu NT, Nga TV, Duy PT, Campbell JI, Hoang NV, et al. A changing picture of shigellosis in southern Vietnam: shifting species dominance, antimicrobial susceptibility and clinical presentation. BMC Infect Dis. 2009;9:204.CrossRefPubMedPubMedCentral
26.
go back to reference von Seidlein L, Kim DR, Ali M, Lee H, Wang X, Thiem VD, et al. A multicentre study of Shigella diarrhoea in six Asian countries: disease burden, clinical manifestations, and microbiology. PLoS Med. 2006;3(9):e353.CrossRef von Seidlein L, Kim DR, Ali M, Lee H, Wang X, Thiem VD, et al. A multicentre study of Shigella diarrhoea in six Asian countries: disease burden, clinical manifestations, and microbiology. PLoS Med. 2006;3(9):e353.CrossRef
27.
go back to reference Langendorf C, Le Hello S, Moumouni A, Gouali M, Mamaty AA, Grais RF, et al. Enteric bacterial pathogens in children with diarrhea in Niger: diversity and antimicrobial resistance. PLoS ONE. 2015;10(3):e0120275.CrossRefPubMedPubMedCentral Langendorf C, Le Hello S, Moumouni A, Gouali M, Mamaty AA, Grais RF, et al. Enteric bacterial pathogens in children with diarrhea in Niger: diversity and antimicrobial resistance. PLoS ONE. 2015;10(3):e0120275.CrossRefPubMedPubMedCentral
28.
go back to reference Zhang Y, Zhao Y, Ding K, Wang X, Chen X, Liu Y, et al. Analysis of bacterial pathogens causing acute diarrhea on the basis of sentinel surveillance in Shanghai, China, 2006–2011. Jpn J Infect Dis. 2014;67(4):264–8.CrossRefPubMed Zhang Y, Zhao Y, Ding K, Wang X, Chen X, Liu Y, et al. Analysis of bacterial pathogens causing acute diarrhea on the basis of sentinel surveillance in Shanghai, China, 2006–2011. Jpn J Infect Dis. 2014;67(4):264–8.CrossRefPubMed
29.
go back to reference Xia S, Hendriksen RS, Xie Z, Huang L, Zhang J, Guo W, et al. Molecular characterization and antimicrobial susceptibility of Salmonella isolates from infections in humans in Henan Province, China. J Clin Microbiol. 2009;47(2):401–9.CrossRefPubMed Xia S, Hendriksen RS, Xie Z, Huang L, Zhang J, Guo W, et al. Molecular characterization and antimicrobial susceptibility of Salmonella isolates from infections in humans in Henan Province, China. J Clin Microbiol. 2009;47(2):401–9.CrossRefPubMed
30.
go back to reference Koziel M, Kiely R, Blake L, O’Callaghan I, Corcoran GD, Lucey B, et al. Improved detection of bacterial pathogens in patients presenting with gastroenteritis by use of the EntericBio real-time gastro panel I assay. J Clin Microbiol. 2013;51(8):2679–85.CrossRefPubMedPubMedCentral Koziel M, Kiely R, Blake L, O’Callaghan I, Corcoran GD, Lucey B, et al. Improved detection of bacterial pathogens in patients presenting with gastroenteritis by use of the EntericBio real-time gastro panel I assay. J Clin Microbiol. 2013;51(8):2679–85.CrossRefPubMedPubMedCentral
31.
go back to reference Haque R, Mondal D, Kirkpatrick BD, Akther S, Farr BM, Sack RB, et al. Epidemiologic and clinical characteristics of acute diarrhea with emphasis on Entamoeba histolytica infections in preschool children in an urban slum of Dhaka, Bangladesh. Am J Trop Med Hyg. 2003;69(4):398–405.PubMed Haque R, Mondal D, Kirkpatrick BD, Akther S, Farr BM, Sack RB, et al. Epidemiologic and clinical characteristics of acute diarrhea with emphasis on Entamoeba histolytica infections in preschool children in an urban slum of Dhaka, Bangladesh. Am J Trop Med Hyg. 2003;69(4):398–405.PubMed
32.
go back to reference Naumova EN, Jagai JS, Matyas B, DeMaria A Jr, MacNeill IB, Griffiths JK. Seasonality in six enterically transmitted diseases and ambient temperature. Epidemiol Infect. 2007;135(2):281–92.CrossRefPubMed Naumova EN, Jagai JS, Matyas B, DeMaria A Jr, MacNeill IB, Griffiths JK. Seasonality in six enterically transmitted diseases and ambient temperature. Epidemiol Infect. 2007;135(2):281–92.CrossRefPubMed
33.
go back to reference Zhu M, Cui S, Lin L, Xu B, Zhao J, Xia S, et al. Analysis of the aetiology of diarrhoea in outpatients in 2007, Henan province, China. Epidemiol Infect. 2013;141(3):540–8.CrossRefPubMed Zhu M, Cui S, Lin L, Xu B, Zhao J, Xia S, et al. Analysis of the aetiology of diarrhoea in outpatients in 2007, Henan province, China. Epidemiol Infect. 2013;141(3):540–8.CrossRefPubMed
34.
go back to reference Tiruneh M. Serodiversity and antimicrobial resistance pattern of Shigella isolates at Gondar University teaching hospital, Northwest Ethiopia. Jpn J Infect Dis. 2009;62(2):93–7.PubMed Tiruneh M. Serodiversity and antimicrobial resistance pattern of Shigella isolates at Gondar University teaching hospital, Northwest Ethiopia. Jpn J Infect Dis. 2009;62(2):93–7.PubMed
35.
go back to reference Bhattacharya D, Sugunan AP, Bhattacharjee H, Thamizhmani R, Sayi DS, Thanasekaran K, et al. Antimicrobial resistance in Shigella–rapid increase and widening of spectrum in Andaman Islands, India. Indian J Med Res. 2012;135:365–70.PubMedPubMedCentral Bhattacharya D, Sugunan AP, Bhattacharjee H, Thamizhmani R, Sayi DS, Thanasekaran K, et al. Antimicrobial resistance in Shigella–rapid increase and widening of spectrum in Andaman Islands, India. Indian J Med Res. 2012;135:365–70.PubMedPubMedCentral
37.
go back to reference Yang H, Chen G, Zhu Y, Liu Y, Cheng J, Hu L, et al. Surveillance of antimicrobial susceptibility patterns among Shigella species isolated in China during the 7-year period of 2005–2011. Ann Lab Med. 2013;33(2):111–5.CrossRefPubMedPubMedCentral Yang H, Chen G, Zhu Y, Liu Y, Cheng J, Hu L, et al. Surveillance of antimicrobial susceptibility patterns among Shigella species isolated in China during the 7-year period of 2005–2011. Ann Lab Med. 2013;33(2):111–5.CrossRefPubMedPubMedCentral
38.
go back to reference Zhang J, Jin H, Hu J, Yuan Z, Shi W, Yang X, et al. Antimicrobial resistance of Shigella spp. from humans in Shanghai, China, 2004–2011. Diagn Microbiol Infect Dis. 2014;78(3):282–6.CrossRefPubMed Zhang J, Jin H, Hu J, Yuan Z, Shi W, Yang X, et al. Antimicrobial resistance of Shigella spp. from humans in Shanghai, China, 2004–2011. Diagn Microbiol Infect Dis. 2014;78(3):282–6.CrossRefPubMed
39.
go back to reference Ke B, Ran L, Wu S, Deng X, Ke C, Feng Z, et al. Survey of physician diagnostic and treatment practices for patients with acute diarrhea in Guangdong province, China. Foodborne Pathog Dis. 2012;9(1):47–53.CrossRefPubMed Ke B, Ran L, Wu S, Deng X, Ke C, Feng Z, et al. Survey of physician diagnostic and treatment practices for patients with acute diarrhea in Guangdong province, China. Foodborne Pathog Dis. 2012;9(1):47–53.CrossRefPubMed
Metadata
Title
Prevalence and antibiotic resistance of bacterial pathogens isolated from childhood diarrhea in Beijing, China (2010–2014)
Authors
Mei Qu
Bing Lv
Xin Zhang
Hanqiu Yan
Ying Huang
Haikun Qian
Bo Pang
Lei Jia
Biao Kan
Quanyi Wang
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2016
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-016-0116-2

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