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Characterization of non-typhoidal Salmonella isolates from children with acute gastroenteritis, Kolkata, India, during 2000–2016

  • Clinical Microbiology - Research Paper
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Abstract

Non-typhoidal Salmonella (NTS) is an important cause of acute gastroenteritis in children. The study was undertaken to determine the isolation rate, serovar prevalence, antimicrobial resistance (AMR) profiles, and molecular subtypes of NTS from a hospital-based diarrheal disease surveillance in Kolkata, India. Rectal swabs were collected from children (< 5 years of age) with acute gastroenteritis from 2000 to 2016. Samples were processed following standard procedures for identification of NTS. The isolates were tested for antimicrobial susceptibility, AMR genes, plasmid profiles, multilocus sequence typing (MLST), and pulsed-field gel electrophoresis (PFGE) subtypes. A total of 99 (1.0%) Salmonella isolates were recovered from 9957 samples processed. Of the 17 Salmonella serovars identified, S. Worthington (33%) was predominant followed by S. Enteritidis (13%), S. Typhimurium (12%), and others. The isolates showed high resistance towards nalidixic acid (43%), ampicillin (34%), third-generation cephalosporins (32%), and azithromycin (25%), while low resistance was observed for fluoroquinolones (2%). Extended-spectrum beta-lactamase production (blaCTX-M-15 and blaSHV-12 genes) and azithromycin resistance (mphA gene) were common in S. Worthington, while fluoroquinolone resistance (gyrA and parC mutations) was found in S. Kentucky. Diverse plasmid profiles were observed among the isolates. PFGE analysis identified genetically related strains of each serovar in circulation. MLST also revealed phylogenetically clonal isolates of which S. Worthington ST592 and ciprofloxacin-resistant S. Kentucky ST198 were not reported earlier from India. NTS resistant to current drugs of choice poses a potential public health problem. Continuous monitoring of AMR profiles and molecular subtypes of NTS serovars is recommended for controlling the spread of resistant organisms.

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References

  1. Boschi-Pinto C, Velebit L, Shibuya K (2008) Estimating child mortality due to diarrhoea in developing countries. Bull World Health Organ 86:710–717

    PubMed  PubMed Central  Google Scholar 

  2. Lakshminarayanan S, Jayalakshmy R (2015) Diarrheal diseases among children in India: current scenario and future perspectives. J Nat Sci Biol Med 6:24–28

    PubMed  PubMed Central  Google Scholar 

  3. Scallan E, Mahon BE, Hoekstra RM, Griffin PM (2013) Estimates of illnesses, hospitalizations and deaths caused by major bacterial enteric pathogens in young children in the United States. Pediatr Infect Dis J 32:217–221

    PubMed  Google Scholar 

  4. Li Y, Xie X, Xu X, Wang X, Chang H, Wang C, Wang A, He Y, Yu H, Wang X, Zeng M (2014) Non-typhoidal Salmonella infection in children with acute gastroenteritis: prevalence, serotypes, and antimicrobial resistance in Shanghai. China Foodborne Pathog Dis 11:200–206

    CAS  PubMed  Google Scholar 

  5. Wen SC, Best E, Nourse C (2017) Non-typhoidal Salmonella infections in children: review of literature and recommendations for management. J Paediatr Child Health 53:936–941

    PubMed  Google Scholar 

  6. Saha MR, Saha D, Dutta P, Mitra U, Bhattacharya SK (2001) Isolation of Salmonella enterica serotypes from children with diarrhoea in Calcutta, India. J Health Popul Nutr 19:301–305

    CAS  PubMed  Google Scholar 

  7. Cellai Rustici M, Mangiantini F, Chiappini E, Bartolomè R, Pecile P, Prats G, de Martino M (2006) Antibiotic resistance among Salmonella enterica isolates in southern European children hospitalized for acute diarrhea. Eur J Pediatr 165:577–578

    PubMed  Google Scholar 

  8. Kariuki S, Revathi G, Kariuki N, Kiiru J, Mwituria J, Hart CA (2006) Characterisation of community acquired non-typhoidal Salmonella from bacteraemia and diarrhoeal infections in children admitted to hospital in Nairobi, Kenya. BMC Microbiol 6:101

    PubMed  PubMed Central  Google Scholar 

  9. Araque M (2009) Non typhoid Salmonella gastroenteritis in paediatric patients from urban areas in the city of Merida, Venezuela. J Infect Developing Countr 3:28–34

    CAS  Google Scholar 

  10. Langendorf C, Le Hello S, Moumouni A, Gouali M, Mamaty A-A, Grais RF et al (2015) Enteric bacterial pathogens in children with diarrhea in Niger: diversity and antimicrobial resistance. PLoS One 10:e0120e275

    Google Scholar 

  11. Qu M, Lv B, Zhang X, Yan H, Huang Y, Qian H et al (2016) Prevalence and antibiotic resistance of bacterial pathogens isolated from childhood diarrhea in Beijing, China (2010–2014). Gut Pathog 8:1

    Google Scholar 

  12. Tian L, Zhu X, Chen Z, Liu W, Li S, Yu W et al (2016) Characteristics of bacterial pathogens associated with acute diarrhea in children under 5 years of age: a hospital-based cross-sectional study. BMC Infect Dis 16:253

    PubMed  PubMed Central  Google Scholar 

  13. Harb A, O’Dea M, Hanan ZK, Abraham S, Habib I (2017) Prevalence, risk factors and antimicrobial resistance of Salmonella diarrhoeal infection among children in Thi-Qar governorate, Iraq. Epidemiol Infect 145:3486–3496

    CAS  PubMed  Google Scholar 

  14. Thomson CN, Phan VTM, Le TPT, Pham TNT, Hoang LP, Ha V et al (2013) Epidemiological features and risk factors of Salmonella gastroenteritis in children resident in Ho Chi Minh City, Vietnam. Epidemiol Infect 141:1604–1613

    Google Scholar 

  15. Cahill SM, Wachsmuth IK, Costarrica Mde L, Ben Embarek PK (2008) Powdered infant formula as a source of Salmonella infection in infants. Clin Infect Dis 46:268–273

    PubMed  Google Scholar 

  16. Buch NA, Dhananjiya A (1998) A nursery outbreak of multidrug resistant Salmonella Typhimurium. Indian Pediatr 35:455–459

    CAS  PubMed  Google Scholar 

  17. Bornemann R, Zerr DM, Heath J, Koehler J, Grandjean M, Pallipamu R, Duchin J (2002) An outbreak of Salmonella serotype Saintpaul in a children’s hospital. Infect Control Hosp Epidemiol 23:671–676

    PubMed  Google Scholar 

  18. Smith AM, Mthanti MA, Haumann C, Tyalisi N, Boon GP, Sooka A, Keddy KH, GERMS-SA Surveillance Network (2014) Nosocomial outbreak of Salmonella enterica serovar Typhimurium primarily affecting a pediatric ward in South Africa in 2012. J Clin Microbiol 52:627–631

    PubMed  PubMed Central  Google Scholar 

  19. Su LH, Chiu CH, Chu C, Ou JT (2004) Antimicrobial resistance in non-typhoid Salmonella serotypes: a global challenge. Clin Infect Dis 39:546–551

    CAS  PubMed  Google Scholar 

  20. Arlet G, Barrett TJ, Butaye P, Cloeckaert A, Mulvey MR, White DG (2006) Salmonella resistant to extended-spectrum cephalosporins: prevalence and epidemiology. Microbes Infect 8:1945–1954

    CAS  PubMed  Google Scholar 

  21. Meakins S, Fisher IS, Berghold C, Gerner-Smidt P, Tschäpe H, Cormican M, Luzzi I, Schneider F, Wannett W, Coia J, Echeita A, Threlfall EJ, Enter-net participants (2008) Antimicrobial drug resistance in human nontyphoidal Salmonella isolates in Europe 2000-2004: a report from the Enter-net international surveillance network. Microb Drug Resist 14:31–35

    CAS  PubMed  Google Scholar 

  22. Nair S, Ashton P, Doumith M, Connell S, Painset A, Mwaigwisya S, Langridge G, de Pinna E, Godbole G, Day M (2016) WGS for surveillance of antimicrobial resistance: a pilot study to detect the prevalence and mechanism of resistance to azithromycin in a UK population of non-typhoidal Salmonella. J Antimicrob Chemother 71:3400–3408

    CAS  PubMed  Google Scholar 

  23. Le Hello S, Bekhit A, Granier SA, Barua H, Beutlich J, Zajac M et al (2013) The global establishment of a highly fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain. Front Microbiol 4:395

    PubMed  PubMed Central  Google Scholar 

  24. Krauland MG, Marsh JW, Paterson DL, Harrison LH (2009) Integron-mediated multidrug resistance in a global collection of nontyphoidal Salmonella enterica isolates. Emerg Infect Dis 15:388–396

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Ranjbar R, Giammanco GM, Farshad S, Owlia P, Aleo A, Mammina C (2011) Serotypes, antibiotic resistance, and class 1 integrons in Salmonella isolates from pediatric cases of enteritis in Tehran, Iran. Foodborne Pathog Dis 8:547–553

    CAS  PubMed  Google Scholar 

  26. Vo AT, van Duijkeren E, Gaastra W, Fluit AC (2010) Antimicrobial resistance, class 1 integrons and genomic island 1 in Salmonella isolates from Vietnam. PLoS One 5:e9440

    PubMed  PubMed Central  Google Scholar 

  27. Menezes GA, Khan MA, Harish BN, Parija SC, Goessens W, Vidyalakshmi K et al (2010) Molecular characterization of antimicrobial resistance in non-typhoidal salmonellae associated with systemic manifestations from India. J Med Micobiol 59:1477–1483

    CAS  Google Scholar 

  28. Wattiau P, Boland C, Bertrand S (2011) Methodologies for Salmonella enterica subsp. enterica subtyping: gold standards and alternatives. Appl Environ Microbiol 77:7877–7885

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Torpdahl M, Skov MN, Sandvang D, Baggesen DL (2005) Genotypic characterization of Salmonella by multi-locus sequence typing, pulsed-field gel electrophoresis and amplified length polymorphism. J Microbiol Methods 63:173–184

    CAS  PubMed  Google Scholar 

  30. Noda T, Murakami K, Asai T, Etoh Y, Ishihara T, Kuroki T (2011) Multi-locus sequence typing of Salmonella enterica subsp. enterica serovar Enteritidis strains in Japan between 1973 and 2004. Acta Vet Scand 53:38

    PubMed  PubMed Central  Google Scholar 

  31. World Health Organization (2013) Diarrheal Diseases In: WHO; Fact sheet No.330. http://www.who.int/mediacentre/factsheets/fs330/en/. Accessed 22 November 2015

  32. Mikoleit ML (2010) WHO global foodborne infections network. “A WHO network building capacity to detect, control and prevent foodborne and other enteric infections from farm to table” laboratory protocol: “isolation of Salmonella and Shigella from Faecal specimens”. Enteric diseases laboratory branch, Centers for Disease Control and Prevention. Atlanta, GA; US. http://antimicrobialresistance.dk/CustomerData/Files/Folders/6-pdf-protocols/62_gfn-stool-culture-nov2010.pdf. Accessed 18 March 2011

  33. Mikoleit ML (2010) WHO Global Foodborne Infections Network “A WHO network building capacity to detect, control and prevent foodborne and other enteric infections from farm to table” Laboratory Protocol: “Biochemical Identification of Salmonella and Shigella Using an Abbreviated Panel of Tests”. Enteric Diseases Laboratory Branch Centers for Disease Control and Prevention. Atlanta, GA; US. http://antimicrobialresistance.dk/CustomerData/Files/Folders/2-newsletter-pdf/20_07-gfn-biochem-v002-final-16oct2015.pdf. Accessed 18 March 2011

  34. Grimont PAD, Weill FX (2007) Antigenic formulae of the Salmonella serovars (9th edition).World Health Organization collaborating Centre for Reference and Research on Salmonella. Institut Pasteur, Paris https://www.pasteur.fr/sites/default/files/veng_0.pdf . Accessed 20 July 2011

    Google Scholar 

  35. Clinical and Laboratory Standards Institute (2017) Performance standards for antimicrobial susceptibility testing, 27th edition. CLSI supplement M100. CLSI, Wayne

    Google Scholar 

  36. Sjölund-Karlsson M, Joyce K, Blickenstaff K, Ball T, Haro J, Medalla FM, Fedorka-Cray P, Zhao S, Crump JA, Whichard JM (2011) Antimicrobial susceptibility to azithromycin among Salmonella enterica isolates from the United States. Antimicrob Agents Chemother 55:3985–3989

    PubMed  PubMed Central  Google Scholar 

  37. Pitout JD, Hossain A, Hanson ND (2004) Phenotypic and molecular detection of CTX-M-beta lactamases produced by Escherichia coli and Klebsiella spp. J Clin Microbiol 42:5715–5721

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Eaves DJ, Randall L, Gray DT, Buckley A, Woodward MJ, White AP, Piddock LJ (2004) Prevalence of mutations within the quinolone resistance-determining region of gyrA, gyrB, parC and parE and association with antibiotic resistance in quinolone-resistant Salmonella enterica. Antimicrob Agents Chemother 48:4012–4015

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Sáenz Y, Briñas L, Domínguez E, Ruiz J, Zarazaga M, Vila J, Torres C (2004) Mechanisms of resistance in multiple-antibiotic-resistant Escherichia coli strains of human, animal, and food origin. Antimicrob Agents Chemother 48:3996–4001

    PubMed  PubMed Central  Google Scholar 

  40. Lunn AD, Fabrega A, Cespedes JS, Vila J (2010) Prevalence of mechanisms of decreasing quinolone-susceptibility among Salmonella spp. clinical isolates. Int Microbiol 13:15–20

    CAS  PubMed  Google Scholar 

  41. Nguyen MCP, Woerther PL, Bouvet M, Andremont A, Leclercq R, Canu A (2009) Escherichia coli as reservoir for macrolide resistance genes. Emerg Infect Dis 15:1648–1650

    CAS  PubMed Central  Google Scholar 

  42. Jain P, Sudhanthirakodi S, Chowdhury G, Joshi S, Anandan S, Ray U et al (2018) Antimicrobial resistance, plasmid, virulence, multilocus sequence typing and pulsed-field gel electrophoresis profiles of Salmonella enterica serovar Typhimurium clinical and environmental isolates from India. PLoS One 13:e0207954

    PubMed  PubMed Central  Google Scholar 

  43. Kado CI, Liu SL (1981) Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 145:1365–1373

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ (2005) Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63:219–228

    CAS  PubMed  Google Scholar 

  45. Centers for Disease Control and Prevention (2013) Standard operating procedure for PulseNet PFGE of Escherichia coli O157:H7, Escherichia coli non-O157 (STEC), Salmonella serotypes, Shigella sonnei and Shigella flexneri. CDC, Atlanta http://www.cdc.gov/pulsenet/PDF/ecoli-shigella-salmonella-pfge-protocol-508c.pdf. Accessed 26 September 2013

    Google Scholar 

  46. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B (1995) Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33:2233–2239

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Zheng J, Keys CE, Zhao S, Ahmed R, Meng J, Brown EW (2011) Simultaneous analysis of multiple enzymes increases accuracy of pulsed-field gel electrophoresis in assigning genetic relationships among homogeneous Salmonella strains. J Clin Microbiol 49:85–94

    CAS  PubMed  Google Scholar 

  48. World Bank (2011) India-Vulnerability of Kolkata metropolitan area to increased precipitation in a changing climate (English). Report No. 53282-IN. Washington DC, USA. http://documents.worldbank.org/curated/en/160411468269379264/pdf/532820ESW0IN0R05B00PUBLIC0100260110.pdf. Accessed 29 June 2019

  49. Taneja N, Appannanavar SB, Kumar A, Varma G, Kumar Y, Mohan B, Sharma M (2014) Serotype profile and molecular characterization of antimicrobial resistance in non-typhoidal Salmonella isolated from gastroenteritis cases over nine years. J Med Microbiol 63:66–73

    CAS  PubMed  Google Scholar 

  50. Ansari S, Sherchand JB, Parajuli K, Mishra SK, Dahal RK, Shrestha S, Tandukar S, Pokhrel BM (2012) Bacterial etiology of acute diarrhea in children under five years of age. J Nepal Health Res Counc 10:218–223

    CAS  PubMed  Google Scholar 

  51. Sang WK, Oundo V, Schnabel D (2012) Prevalence and antibiotic resistance of bacterial pathogens isolated from childhood diarrhoea in four provinces of Kenya. J Infect Dev Ctries 23:572–578

    Google Scholar 

  52. Eguale T, Gebreyes WA, Asrat D, Alemayehu H, Gunn JS, Engidawork E (2015) Non-typhoidal Salmonella serotypes, antimicrobial resistance and co-infection with parasites among patients with diarrhea and other gastrointestinal complaints in Addis Ababa, Ethiopia. BMC Infect Dis 15:497

    PubMed  PubMed Central  Google Scholar 

  53. Moyo SJ, Gro N, Matee MI, Kitundu J, Myrmel H, Mylvaganam H et al (2011) Age specific aetiological agents of diarrhoea in hospitalized children aged less than five years in Dar es Salam, Tanzania. BMC Pediatr 23:11–19

    Google Scholar 

  54. Chiyangi H, Muma JB, Malama S, Manyahi J, Abade A, Kwenda G et al (2017) Identification and antimicrobial resistance patterns of bacterial enteropathogens from children aged 0-59 months at the University Tyeaching Hospital, Lusaka, Zambia: a prospective cross-sectional study. BMC Infect Dis 17:117

    PubMed  PubMed Central  Google Scholar 

  55. Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, Aarestrup FM (2011) Global monitoring of Salmonella serovar distribution from the World Health Organization global foodborne infections network country data bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis 8:887–900

    PubMed  Google Scholar 

  56. Kumar Y, Sharma A, Sehgal R, Kumar S (2009) Distribution trends of Salmonella serovars in India (2001-2005). Trans R Soc Trop Med Hyg 103:390–394

    PubMed  Google Scholar 

  57. Bassal R, Reisfeld A, Andorn N, Yishai R, Nissan I, Agmon V, Peled N, Block C, Keller N, Kenes Y, Taran D, Schemberg B, Ken-Dror S, Rouach T, Citron B, Berman E, Green MS, Shohat T, Cohen D (2012) Recent trends in the epidemiology of non-typhoidal Salmonella in Israel, 1999–2009. Epidemiol Infect 140:1446–1453

    CAS  PubMed  Google Scholar 

  58. Reis ROD, Souza MN, Cecconi MCP, Timm L, Ikuta N, Simon D, Wolf JM, Lunge VR (2018) Increasing prevalence and dissemination of invasive nontyphoidal Salmonella serotype Typhimurium with multidrug resistance in hospitalized patients from southern Brazil. Braz J Infect Dis 22:424–432

    PubMed  Google Scholar 

  59. Dos Reis RO, Cecconi MC, Timm L, Souza MN, Ikuta N, Wolf JM, Lunge VR (2019) Salmonella isolates from urine cultures: serotypes and antimicrobial resistance in hospital settings. Braz J Microbiol 50:445–448

    PubMed  PubMed Central  Google Scholar 

  60. Ghadage DP, Bal AM (2002) Antibiotic susceptibility pattern of Salmonella Worthington isolated from neonates - a retrospective study. Jpn J Infect Dis 55:45–46

    CAS  PubMed  Google Scholar 

  61. Gal-Mor O, Valinsky L, Weinberger M, Guy S, Jaffe J, Schorr YI, Raisfeld A, Agmon V, Nissan I (2010) Multidrug-resistant Salmonella enterica serovar Infantis, Israel. Emerg Infect Dis 16:1754–1757

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Tamang MD, Nam HM, Kim TS, Jang GC, Jung SC, Lim SK (2011) Emergence of extended-spectrum β-lactamase (CTX-M-15 and CTX-M-14)-producing nontyphoid Salmonella with reduced susceptibility to ciprofloxacin among food animals and humans in Korea. J Clin Microbiol 49:2671–2675

    PubMed  PubMed Central  Google Scholar 

  63. Hopkins KL, Liebana E, Villa L, Batchelor M, Threlfall EJ, Carattoli A (2006) Replicon typing of plasmids carrying CTX-M or CMY beta-lactamases circulating among Salmonella and Escherichia coli isolates. Antimicrob Agents Chemother 50:3203–3206

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Achtman M, Wain J, Weill FX, Nair S, Zhou Z, Sangal V et al (2012) Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog 8:e1002776

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Professor R. Bonnet, CHU Clermont-Ferrand, France, for providing CTX-M control strains. We acknowledge the help of Dr. B. Manna, ex-Scientist F from ICMR-NICED, in statistical calculation. The help of NICED staffs in sample collection and transport is also gratefully acknowledged.

Funding

The study was supported in part by the Indian Council of Medical Research (ICMR), New-Delhi intramural fund and Japan Initiative for Global Research Network on Infectious Diseases (J-GRID) of the Japan Agency for Medical Research and Development (AMED) under grant number JP18fm0108002. ICMR senior research fellowship to P. Jain and S. Samajpati are received.

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Authors and Affiliations

  1. Division of Bacteriology, ICMR-National Institute of Cholera and Enteric Diseases, P-33 CIT Road, Scheme XM, Beliaghata, Kolkata, 700010, India

    Priyanka Jain, Goutam Chowdhury, Sriparna Samajpati, Arindam Ganai, Asish K. Mukhopadhyay & Shanta Dutta

  2. Division of Bioinformatics, ICMR- National Institute of Cholera and Enteric Diseases, Kolkata, India

    Surajit Basak

  3. Department of Pediatrics, Dr. B. C. Roy Post Graduate Institute of Paediatric Sciences, Kolkata, India

    Sandip Samanta

  4. Collaborative Research Centre of Okayama University for Infectious Diseases at NICED, Kolkata, India

    Keinosuke Okamoto

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  1. Priyanka Jain
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  2. Goutam Chowdhury
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  3. Sriparna Samajpati
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  9. Shanta Dutta
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Contributions

Conceptualization: Shanta Dutta. Methodology: Priyanka Jain, Sriparna Samajpati, Arindam Ganai, Surajit Basak. Data curation: Priyanka Jain, Goutam Chowdhury, Surajit Basak, Sandip Samanta. Formal analysis and investigation: Priyanka Jain, Surajit Basak, Asish K. Mukhopadhyay, Keinosuke Okamoto. Resources: Goutam Chowdhury, Sandip Samanta, Asish K. Mukhopadhyay, Keinosuke Okamoto. Supervision: Shanta Duta. Writing-original draft preparation: Priyanka Jain, Shanta Dutta. Writing-review and editing: Goutam Chowdhury, Sriparna Samajpati, Surajit Basak, Arindam Ganai, Sandip Samanta, Keinosuke Okamoto, Asish K. Mukhopadhyay.

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Correspondence to Shanta Dutta.

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Ethical approval

The present study was reviewed and approved (no. C-48/2011-T & E) by the Institutional Ethical Committee (IEC) of ICMR-National Institute of Cholera and Enteric Diseases (NICED), Kolkata.

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Informed consents were obtained from the parents or guardians of each patient enrolled in this study.

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Responsible Editor: Tânia A. Tardelli Gomes.

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Table S1

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Figure S1

Phylogenetic tree of non-typhoidal Salmonella isolates (n = 82) derived from a maximum likelihood analysis. (PNG 844 kb)

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Jain, P., Chowdhury, G., Samajpati, S. et al. Characterization of non-typhoidal Salmonella isolates from children with acute gastroenteritis, Kolkata, India, during 2000–2016. Braz J Microbiol 51, 613–627 (2020). https://doi.org/10.1007/s42770-019-00213-z

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