Author:
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-
1.
Kotloff KL et al. 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382: 209–222.
-
2.
Elfving K, Andersson M, Msellem MI, Welinder-Olsson C, Petzold M, Bjorkman A, Trollfors B, Martensson A, Lindh M, 2014. Real-time PCR threshold cycle cutoffs help to identify agents causing acute childhood diarrhea in Zanzibar. J Clin Microbiol 52: 916–923.
-
3.
Liu J et al. 2013. A laboratory-developed TaqMan array card for simultaneous detection of 19 enteropathogens. J Clin Microbiol 51: 472–480.
-
4.
Liu J et al. 2014. Development and assessment of molecular diagnostic tests for 15 enteropathogens causing childhood diarrhoea: a multicentre study. Lancet Infect Dis 14: 716–724.
-
5.
Wolffs PF, Bruggeman CA, van Well GT, van Loo IH, 2011. Replacing traditional diagnostics of fecal viral pathogens by a comprehensive panel of real-time PCRs. J Clin Microbiol 49: 1926–1931.
-
6.
Kharat VB, Ahmed M, Jiang Z-D, Riddle MS, DuPont HL, 2017. Colonization factors in enterotoxigenic Escherichia coli strains in travelers to Mexico, Guatemala, and India compared with children in Houston, Texas. Am J Trop Med Hyg 96: 83–87.
-
7.
Kabayiza JC, Andersson ME, Nilsson S, Bergstrom T, Muhirwa G, Lindh M, 2014. Real-time PCR identification of agents causing diarrhea in Rwandan children less than 5 years of age. Pediatr Infect Dis J 33: 1037–1042.
-
8.
Sinha A et al. 2013. Culture-independent real-time PCR reveals extensive polymicrobial infections in hospitalized diarrhoea cases in Kolkata, India. Clin Microbiol Infect 19: 173–180.
-
9.
Liu J et al. 2016. Use of quantitative molecular diagnostic methods to identify causes of diarrhoea in children: a reanalysis of the GEMS case-control study. Lancet 388: 1291–1301.
-
10.
Keddy KH, Smith AM, Page NA, 2016. GEMS extend understanding of childhood diarrhoea. Lancet 388: 1252–1254.
-
11.
Bhavnani D, Goldstick JE, Cevallos W, Trueba G, Eisenberg JN, 2012. Synergistic effects between rotavirus and coinfecting pathogens on diarrheal disease: evidence from a community-based study in northwestern Ecuador. Am J Epidemiol 176: 387–395.
-
12.
Kotloff KL et al. 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382: 209–222.
-
13.
Lindsay B et al. 2015. Microbiota that affect risk for shigellosis in children in low-income countries. Emerg Infect Dis 21: 242–250.
-
14.
Lindsay B, Ramamurthy T, Sen Gupta S, Takeda Y, Rajendran K, Nair GB, Stine OC, 2011. Diarrheagenic pathogens in polymicrobial infections. Emerg Infect Dis 17: 606–611.
-
15.
Elfving K et al. 2016. Acute uncomplicated febrile illness in children aged 2–59 months in Zanzibar—aetiologies, antibiotic treatment and outcome. PLoS One 11: e0146054.
-
16.
Kabayiza JC, Andersson ME, Nilsson S, Baribwira C, Muhirwa G, Bergstrom T, Lindh M, 2014. Diarrhoeagenic microbes by real-time PCR in Rwandan children under 5 years of age with acute gastroenteritis. Clin Microbiol Infect 20: O1128–O1135.
-
17.
Kabayiza JC, Andersson ME, Welinder-Olsson C, Bergstrom T, Muhirwa G, Lindh M, 2013. Comparison of rectal swabs and faeces for real-time PCR detection of enteric agents in Rwandan children with gastroenteritis. BMC Infect Dis 13: 447.
-
18.
Lacher DW, Steinsland H, Blank TE, Donnenberg MS, Whittam TS, 2007. Molecular evolution of typical enteropathogenic Escherichia coli: clonal analysis by multilocus sequence typing and virulence gene allelic profiling. J Bacteriol 189: 342–350.
-
19.
Ochoa TJ et al. 2009. Age-related susceptibility to infection with diarrheagenic Escherichia coli among infants from periurban areas in Lima, Peru. Clin Infect Dis 49: 1694–1702.
-
20.
Mansour A et al. 2014. Pathogenicity and phenotypic characterization of enterotoxigenic Escherichia coli isolates from a birth cohort of children in rural Egypt. J Clin Microbiol 52: 587–591.
-
21.
Qadri F, Svennerholm AM, Faruque AS, Sack RB, 2005. Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention. Clin Microbiol Rev 18: 465–483.
-
22.
Li LL, Liu N, Humphries EM, Yu JM, Li S, Lindsay BR, Stine OC, Duan ZJ, 2016. Aetiology of diarrhoeal disease and evaluation of viral-bacterial coinfection in children under 5 years old in China: a matched case-control study. Clin Microbiol Infect 22: 381.e9–381.e16.
-
23.
Zhang SX et al. 2016. Impact of co-infections with enteric pathogens on children suffering from acute diarrhea in southwest China. Infect Dis Poverty 5: 64.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1495 | 1162 | 87 |
| Full Text Views | 1042 | 16 | 2 |
| PDF Downloads | 327 | 10 | 2 |
Coinfection with Enteric Pathogens in East African Children with Acute Gastroenteritis—Associations and Interpretations
Maria Andersson
Maria Andersson
Department of Infectious Diseases, University of Gothenburg, Gothenburg, Sweden;
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Jean-Claude Kabayiza
Jean-Claude Kabayiza
Department of Pediatrics, University of Rwanda, Kigali, Rwanda;
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Kristina Elfving
Kristina Elfving
Department of Infectious Diseases, University of Gothenburg, Gothenburg, Sweden;
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Staffan Nilsson
Staffan Nilsson
Chalmers University of Technology, Gothenburg, Sweden;
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Mwinyi I. Msellem
Mwinyi I. Msellem
Zanzibar Malaria Elimination Programme (ZAMEP), Ministry of Health, Zanzibar, Tanzania;
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Andreas Mårtensson
Andreas Mårtensson
Department of Women’s and Children’s Health, International Maternal and Child Health (IMCH), Uppsala University, Uppsala, Sweden;
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Anders Björkman
Anders Björkman
Malaria Research, Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden
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Tomas Bergström
Tomas Bergström
Department of Infectious Diseases, University of Gothenburg, Gothenburg, Sweden;
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Magnus Lindh
Magnus Lindh
Department of Infectious Diseases, University of Gothenburg, Gothenburg, Sweden;
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Enteric coinfections among children in low-income countries are very common, but it is not well known if specific pathogen combinations are associated or have clinical importance. In this analysis, feces samples from children in Rwanda and Zanzibar less than 5 years of age, with (N = 994) or without (N = 324) acute diarrhea, were analyzed by real-time polymerase chain reaction targeting a wide range of pathogens. Associations were investigated by comparing co-detection and mono-detection frequencies for all pairwise pathogen combinations. More than one pathogen was detected in 840 samples (65%). A negative association (coinfections being less common than expected from probability) was observed for rotavirus in combination with Shigella, Campylobacter, or norovirus genogroup II, but only in patients, which is statistically expected for agents that independently cause diarrhea. A positive correlation was observed, in both patients and controls, between Ct (threshold cycle) values for certain virulence factor genes in enteropathogenic Escherichia coli (EPEC) (eae and bfpA) and toxin genes in enterotoxigenic E. coli (eltB and estA), allowing estimation of how often these genes were present in the same bacteria. A significant positive association in patients only was observed for Shigella and EPEC-eae, suggesting that this coinfection might interact in a manner that enhances symptoms. Although interaction between pathogens that affect symptoms is rare, this work emphasizes the importance and difference in interpretation of coinfections depending on whether they are positively or negatively associated.
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Author Notes
Authors’ addresses: Maria Andersson, Kristina Elfving, Tomas Bergström, and Magnus Lindh, Department of Infectious Diseases, University of Gothenburg, Guldhedsgatan, Gothenburg, Sweden, E-mails: maria.andersson.3@gu.se, kristinaelfving@hotmail.com, tomas.bergstrom@microbio.gu.se, and magnus.lindh@microbio.gu.se. Jean-Claude Kabayiza, Department of Pediatrics, University of Rwanda, Kigali, Rwanda, E-mail: jckaba@yahoo.fr. Staffan Nilsson, Chalmers University of Technology, Gothenburg, Sweden, E-mail: staffan.nilsson@chalmers.se. Mwinyi I. Msellem, Zanzibar Malaria Elimination Programme (ZAMEP), Ministry of Health, Zanzibar, Tanzania, E-mail: mmwinyi@hotmail.com. Andreas Mårtensson, Department of Women’s and Children’s Health, International Maternal and Child Health (IMCH), Uppsala University, Uppsala, Sweden, E-mail: andreas.martensson@kbh.uu.se, Anders Björkman, Malaria Research, Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden, E-mail: anders.bjorkman@ki.se.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Kotloff KL et al. 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382: 209–222.
-
2.
Elfving K, Andersson M, Msellem MI, Welinder-Olsson C, Petzold M, Bjorkman A, Trollfors B, Martensson A, Lindh M, 2014. Real-time PCR threshold cycle cutoffs help to identify agents causing acute childhood diarrhea in Zanzibar. J Clin Microbiol 52: 916–923.
-
3.
Liu J et al. 2013. A laboratory-developed TaqMan array card for simultaneous detection of 19 enteropathogens. J Clin Microbiol 51: 472–480.
-
4.
Liu J et al. 2014. Development and assessment of molecular diagnostic tests for 15 enteropathogens causing childhood diarrhoea: a multicentre study. Lancet Infect Dis 14: 716–724.
-
5.
Wolffs PF, Bruggeman CA, van Well GT, van Loo IH, 2011. Replacing traditional diagnostics of fecal viral pathogens by a comprehensive panel of real-time PCRs. J Clin Microbiol 49: 1926–1931.
-
6.
Kharat VB, Ahmed M, Jiang Z-D, Riddle MS, DuPont HL, 2017. Colonization factors in enterotoxigenic Escherichia coli strains in travelers to Mexico, Guatemala, and India compared with children in Houston, Texas. Am J Trop Med Hyg 96: 83–87.
-
7.
Kabayiza JC, Andersson ME, Nilsson S, Bergstrom T, Muhirwa G, Lindh M, 2014. Real-time PCR identification of agents causing diarrhea in Rwandan children less than 5 years of age. Pediatr Infect Dis J 33: 1037–1042.
-
8.
Sinha A et al. 2013. Culture-independent real-time PCR reveals extensive polymicrobial infections in hospitalized diarrhoea cases in Kolkata, India. Clin Microbiol Infect 19: 173–180.
-
9.
Liu J et al. 2016. Use of quantitative molecular diagnostic methods to identify causes of diarrhoea in children: a reanalysis of the GEMS case-control study. Lancet 388: 1291–1301.
-
10.
Keddy KH, Smith AM, Page NA, 2016. GEMS extend understanding of childhood diarrhoea. Lancet 388: 1252–1254.
-
11.
Bhavnani D, Goldstick JE, Cevallos W, Trueba G, Eisenberg JN, 2012. Synergistic effects between rotavirus and coinfecting pathogens on diarrheal disease: evidence from a community-based study in northwestern Ecuador. Am J Epidemiol 176: 387–395.
-
12.
Kotloff KL et al. 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382: 209–222.
-
13.
Lindsay B et al. 2015. Microbiota that affect risk for shigellosis in children in low-income countries. Emerg Infect Dis 21: 242–250.
-
14.
Lindsay B, Ramamurthy T, Sen Gupta S, Takeda Y, Rajendran K, Nair GB, Stine OC, 2011. Diarrheagenic pathogens in polymicrobial infections. Emerg Infect Dis 17: 606–611.
-
15.
Elfving K et al. 2016. Acute uncomplicated febrile illness in children aged 2–59 months in Zanzibar—aetiologies, antibiotic treatment and outcome. PLoS One 11: e0146054.
-
16.
Kabayiza JC, Andersson ME, Nilsson S, Baribwira C, Muhirwa G, Bergstrom T, Lindh M, 2014. Diarrhoeagenic microbes by real-time PCR in Rwandan children under 5 years of age with acute gastroenteritis. Clin Microbiol Infect 20: O1128–O1135.
-
17.
Kabayiza JC, Andersson ME, Welinder-Olsson C, Bergstrom T, Muhirwa G, Lindh M, 2013. Comparison of rectal swabs and faeces for real-time PCR detection of enteric agents in Rwandan children with gastroenteritis. BMC Infect Dis 13: 447.
-
18.
Lacher DW, Steinsland H, Blank TE, Donnenberg MS, Whittam TS, 2007. Molecular evolution of typical enteropathogenic Escherichia coli: clonal analysis by multilocus sequence typing and virulence gene allelic profiling. J Bacteriol 189: 342–350.
-
19.
Ochoa TJ et al. 2009. Age-related susceptibility to infection with diarrheagenic Escherichia coli among infants from periurban areas in Lima, Peru. Clin Infect Dis 49: 1694–1702.
-
20.
Mansour A et al. 2014. Pathogenicity and phenotypic characterization of enterotoxigenic Escherichia coli isolates from a birth cohort of children in rural Egypt. J Clin Microbiol 52: 587–591.
-
21.
Qadri F, Svennerholm AM, Faruque AS, Sack RB, 2005. Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention. Clin Microbiol Rev 18: 465–483.
-
22.
Li LL, Liu N, Humphries EM, Yu JM, Li S, Lindsay BR, Stine OC, Duan ZJ, 2016. Aetiology of diarrhoeal disease and evaluation of viral-bacterial coinfection in children under 5 years old in China: a matched case-control study. Clin Microbiol Infect 22: 381.e9–381.e16.
-
23.
Zhang SX et al. 2016. Impact of co-infections with enteric pathogens on children suffering from acute diarrhea in southwest China. Infect Dis Poverty 5: 64.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1495 | 1162 | 87 |
| Full Text Views | 1042 | 16 | 2 |
| PDF Downloads | 327 | 10 | 2 |