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Published in: BMC Infectious Diseases 1/2019

Open Access 01-12-2019 | Ampicillin | Research article

Invasive Salmonella infections among children in Bintulu, Sarawak, Malaysian Borneo: a 6-year retrospective review

Authors: Anand Mohan, Chandran Munusamy, Yee-Chin Tan, Sobana Muthuvelu, Rohaidah Hashim, Su-Lin Chien, Ming-Kui Wong, Nurul Aiman Khairuddin, Yuwana Podin, Peter Sie-Teck Lau, David Chun-Ern Ng, Mong-How Ooi

Published in: BMC Infectious Diseases | Issue 1/2019

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Abstract

Background

Invasive Salmonella infections result in significant morbidity and mortality in developing countries. In Asia, typhoid and paratyphoid fever are reported to be the major invasive Salmonella infections, while invasive non-typhoidal Salmonella (iNTS) infections are believed to be uncommon. Data from Sarawak, in Malaysian Borneo, are limited.

Methods

A retrospective study identifying all children aged < 15 years with invasive Salmonella infections from 2011 to 2016 was conducted in Bintulu Hospital in Sarawak. Population incidences, clinical and bacterial characteristics were examined.

Results

Forty-four patients were identified during the 6-year study period: 43 had iNTS infection and 1 had typhoid fever. The average annual iNTS incidence was 32.4 per 100,000 children aged < 5 years. None of the children had malaria or HIV infection, and only 7% were severely malnourished. Salmonella Enteritidis and Salmonella Java were the commonest NTS serovars identified. Pneumonia was the most common manifestation of iNTS disease, present in 20 (47%) children. Other manifestations included gastroenteritis, fever without a source, septic arthritis and meningitis. Salmonella Enteritidis was identified in 76% of those with pneumonia, significantly more frequently than in children with other manifestations. Over 25% of children with iNTS developed severe disease and nearly 10% suffered long term morbidity or mortality. While 78% of Salmonella Java isolates were multi-drug resistant, nearly all other isolates were susceptible to most antimicrobials, including ampicillin.

Conclusions

Bintulu Division in Sarawak observed a very high incidence of childhood iNTS infections. Enteric fever was uncommon. The epidemiology of invasive Salmonella infections in Malaysian Borneo differs considerably from that of neighbouring countries in Asia.
Literature
1.
go back to reference Crump JA, Sjolund-Karlsson M, Gordon MA, Parry CM. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial Management of Invasive Salmonella Infections. Clin Microbiol Rev. 2015;28(4):901–37.CrossRefPubMedPubMedCentral Crump JA, Sjolund-Karlsson M, Gordon MA, Parry CM. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial Management of Invasive Salmonella Infections. Clin Microbiol Rev. 2015;28(4):901–37.CrossRefPubMedPubMedCentral
2.
go back to reference Crump JA, Heyderman RSA. Perspective on invasive Salmonella disease in Africa. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2015;61(Suppl 4):S235–40.CrossRef Crump JA, Heyderman RSA. Perspective on invasive Salmonella disease in Africa. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2015;61(Suppl 4):S235–40.CrossRef
3.
go back to reference Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2010;50(6):882–9.CrossRef Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2010;50(6):882–9.CrossRef
4.
go back to reference Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA. Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet. 2012;379(9835):2489–99.CrossRefPubMedPubMedCentral Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA. Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet. 2012;379(9835):2489–99.CrossRefPubMedPubMedCentral
5.
go back to reference Uche IV, MacLennan CA, Saul A. A systematic review of the incidence, risk factors and case fatality rates of invasive Nontyphoidal Salmonella (iNTS) disease in Africa (1966 to 2014). PLoS Negl Trop Dis. 2017;11(1):e0005118.CrossRefPubMedPubMedCentral Uche IV, MacLennan CA, Saul A. A systematic review of the incidence, risk factors and case fatality rates of invasive Nontyphoidal Salmonella (iNTS) disease in Africa (1966 to 2014). PLoS Negl Trop Dis. 2017;11(1):e0005118.CrossRefPubMedPubMedCentral
6.
go back to reference Marks F, von Kalckreuth V, Aaby P, Adu-Sarkodie Y, El Tayeb MA, Ali M, et al. Incidence of invasive salmonella disease in sub-Saharan Africa: a multicentre population-based surveillance study. Lancet Glob Health. 2017;5(3):e310–23.CrossRefPubMedPubMedCentral Marks F, von Kalckreuth V, Aaby P, Adu-Sarkodie Y, El Tayeb MA, Ali M, et al. Incidence of invasive salmonella disease in sub-Saharan Africa: a multicentre population-based surveillance study. Lancet Glob Health. 2017;5(3):e310–23.CrossRefPubMedPubMedCentral
7.
go back to reference Khan MI, Ochiai RL, von Seidlein L, Dong B, Bhattacharya SK, Agtini MD, et al. Non-typhoidal Salmonella rates in febrile children at sites in five Asian countries. Tropical medicine & international health : TM & IH. 2010;15(8):960–3.CrossRef Khan MI, Ochiai RL, von Seidlein L, Dong B, Bhattacharya SK, Agtini MD, et al. Non-typhoidal Salmonella rates in febrile children at sites in five Asian countries. Tropical medicine & international health : TM & IH. 2010;15(8):960–3.CrossRef
8.
go back to reference Ochiai RL, Acosta CJ, Danovaro-Holliday MC, Baiqing D, Bhattacharya SK, Agtini MD, et al. A study of typhoid fever in five Asian countries: disease burden and implications for controls. Bull World Health Organ. 2008;86(4):260–8.CrossRefPubMedPubMedCentral Ochiai RL, Acosta CJ, Danovaro-Holliday MC, Baiqing D, Bhattacharya SK, Agtini MD, et al. A study of typhoid fever in five Asian countries: disease burden and implications for controls. Bull World Health Organ. 2008;86(4):260–8.CrossRefPubMedPubMedCentral
9.
go back to reference Nor Azizah A, Fadzilah MN, Mariam M, Anis Siham ZA, Ariza A, Noor Shafina MN, et al. Community-acquired bacteremia in Paediatrics: epidemiology, aetiology and patterns of antimicrobial resistance in a tertiary care Centre, Malaysia. Med J Malaysia. 2016;71(3):117–21.PubMed Nor Azizah A, Fadzilah MN, Mariam M, Anis Siham ZA, Ariza A, Noor Shafina MN, et al. Community-acquired bacteremia in Paediatrics: epidemiology, aetiology and patterns of antimicrobial resistance in a tertiary care Centre, Malaysia. Med J Malaysia. 2016;71(3):117–21.PubMed
13.
go back to reference WHO. Pocket Book of Hospital care for children: Guideline for the management of common illnesses with limited resources. WHO press; 2005. WHO. Pocket Book of Hospital care for children: Guideline for the management of common illnesses with limited resources. WHO press; 2005.
14.
go back to reference El-Tayeb MA, Ibrahim ASS, Al-Salamah AA, Almaary KS, Elbadawi YB. Prevalence, serotyping and antimicrobials resistance mechanism of Salmonella enterica isolated from clinical and environmental samples in Saudi Arabia. Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology]. 2017;48(3):499–508.CrossRef El-Tayeb MA, Ibrahim ASS, Al-Salamah AA, Almaary KS, Elbadawi YB. Prevalence, serotyping and antimicrobials resistance mechanism of Salmonella enterica isolated from clinical and environmental samples in Saudi Arabia. Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology]. 2017;48(3):499–508.CrossRef
15.
go back to reference Malorny B, Bunge C, Helmuth R. Discrimination of d-tartrate-fermenting and-nonfermenting Salmonella enterica subsp. enterica isolates by genotypic and phenotypic methods. J Clin Microbiol. 2003;41(9):4292–7.CrossRefPubMedPubMedCentral Malorny B, Bunge C, Helmuth R. Discrimination of d-tartrate-fermenting and-nonfermenting Salmonella enterica subsp. enterica isolates by genotypic and phenotypic methods. J Clin Microbiol. 2003;41(9):4292–7.CrossRefPubMedPubMedCentral
16.
go back to reference Mandomando I, Bassat Q, Sigauque B, Massora S, Quinto L, Acacio S, et al. Invasive Salmonella infections among children from rural Mozambique, 2001-2014. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2015;61(Suppl 4):S339–45.CrossRef Mandomando I, Bassat Q, Sigauque B, Massora S, Quinto L, Acacio S, et al. Invasive Salmonella infections among children from rural Mozambique, 2001-2014. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2015;61(Suppl 4):S339–45.CrossRef
17.
go back to reference Muthumbi E, Morpeth SC, Ooko M, Mwanzu A, Mwarumba S, Mturi N, et al. Invasive Salmonellosis in Kilifi, Kenya. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2015;61(Suppl 4):S290–301.CrossRef Muthumbi E, Morpeth SC, Ooko M, Mwanzu A, Mwarumba S, Mturi N, et al. Invasive Salmonellosis in Kilifi, Kenya. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2015;61(Suppl 4):S290–301.CrossRef
18.
go back to reference Ao TT, Feasey NA, Gordon MA, Keddy KH, Angulo FJ, Crump JA. Global burden of invasive nontyphoidal Salmonella disease, 2010(1). Emerg Infect Dis. 2015;21(6). Ao TT, Feasey NA, Gordon MA, Keddy KH, Angulo FJ, Crump JA. Global burden of invasive nontyphoidal Salmonella disease, 2010(1). Emerg Infect Dis. 2015;21(6).
19.
go back to reference Park SE, Pak GD, Aaby P, Adu-Sarkodie Y, Ali M, Aseffa A, et al. The relationship between invasive Nontyphoidal Salmonella disease, other bacterial bloodstream infections, and malaria in sub-Saharan Africa. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2016;62(Suppl 1):S23–31.CrossRef Park SE, Pak GD, Aaby P, Adu-Sarkodie Y, Ali M, Aseffa A, et al. The relationship between invasive Nontyphoidal Salmonella disease, other bacterial bloodstream infections, and malaria in sub-Saharan Africa. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2016;62(Suppl 1):S23–31.CrossRef
20.
go back to reference Phu Huong Lan N, Le Thi Phuong T, Nguyen Huu H, Thuy L, Mather AE, Park SE, et al. Invasive non-typhoidal Salmonella infections in Asia: clinical observations, disease outcome and dominant Serovars from an infectious disease Hospital in Vietnam. PLoS Negl Trop Dis. 2016;10(8):e0004857.CrossRefPubMedPubMedCentral Phu Huong Lan N, Le Thi Phuong T, Nguyen Huu H, Thuy L, Mather AE, Park SE, et al. Invasive non-typhoidal Salmonella infections in Asia: clinical observations, disease outcome and dominant Serovars from an infectious disease Hospital in Vietnam. PLoS Negl Trop Dis. 2016;10(8):e0004857.CrossRefPubMedPubMedCentral
21.
go back to reference Tapia MD, Tennant SM, Bornstein K, Onwuchekwa U, Tamboura B, Maiga A, et al. Invasive Nontyphoidal Salmonella infections among children in Mali, 2002-2014: microbiological and epidemiologic features guide vaccine development. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2015;61(Suppl 4):S332–8.CrossRef Tapia MD, Tennant SM, Bornstein K, Onwuchekwa U, Tamboura B, Maiga A, et al. Invasive Nontyphoidal Salmonella infections among children in Mali, 2002-2014: microbiological and epidemiologic features guide vaccine development. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2015;61(Suppl 4):S332–8.CrossRef
22.
go back to reference Lee WS, Puthucheary SD, Parasakthi N, Choo KE. Antimicrobial susceptibility and distribution of non-typhoidal Salmonella serovars isolated in Malaysian children. J Trop Pediatr. 2003;49(1):37–41.CrossRefPubMed Lee WS, Puthucheary SD, Parasakthi N, Choo KE. Antimicrobial susceptibility and distribution of non-typhoidal Salmonella serovars isolated in Malaysian children. J Trop Pediatr. 2003;49(1):37–41.CrossRefPubMed
23.
go back to reference Dhanoa A, Fatt QK. Non-typhoidal Salmonella bacteraemia: epidemiology, clinical characteristics and its' association with severe immunosuppression. Ann Clin Microbiol Antimicrob. 2009;8:15.CrossRefPubMedPubMedCentral Dhanoa A, Fatt QK. Non-typhoidal Salmonella bacteraemia: epidemiology, clinical characteristics and its' association with severe immunosuppression. Ann Clin Microbiol Antimicrob. 2009;8:15.CrossRefPubMedPubMedCentral
24.
go back to reference MacLennan CA, Msefula CL, Gondwe EN, Gilchrist JJ, Pensulo P, Mandala WL, et al. Presentation of life-threatening invasive nontyphoidal Salmonella disease in Malawian children: a prospective observational study. PLoS Negl Trop Dis. 2017;11(12):e0006027.CrossRefPubMedPubMedCentral MacLennan CA, Msefula CL, Gondwe EN, Gilchrist JJ, Pensulo P, Mandala WL, et al. Presentation of life-threatening invasive nontyphoidal Salmonella disease in Malawian children: a prospective observational study. PLoS Negl Trop Dis. 2017;11(12):e0006027.CrossRefPubMedPubMedCentral
25.
go back to reference Brent AJ, Oundo JO, Mwangi I, Ochola L, Lowe B, Berkley JA. Salmonella bacteremia in Kenyan children. Pediatr Infect Dis J. 2006;25(3):230–6.CrossRefPubMed Brent AJ, Oundo JO, Mwangi I, Ochola L, Lowe B, Berkley JA. Salmonella bacteremia in Kenyan children. Pediatr Infect Dis J. 2006;25(3):230–6.CrossRefPubMed
26.
go back to reference Schwarz NG, Sarpong N, Hunger F, Marks F, Acquah SE, Agyekum A, et al. Systemic bacteraemia in children presenting with clinical pneumonia and the impact of non-typhoid salmonella (NTS). BMC Infect Dis. 2010;10:319.CrossRefPubMedPubMedCentral Schwarz NG, Sarpong N, Hunger F, Marks F, Acquah SE, Agyekum A, et al. Systemic bacteraemia in children presenting with clinical pneumonia and the impact of non-typhoid salmonella (NTS). BMC Infect Dis. 2010;10:319.CrossRefPubMedPubMedCentral
27.
go back to reference Punpanich W, Netsawang S, Thippated C. Invasive salmonellosis in urban Thai children: a ten-year review. Pediatr Infect Dis J. 2012;31(8):e105–10.CrossRefPubMed Punpanich W, Netsawang S, Thippated C. Invasive salmonellosis in urban Thai children: a ten-year review. Pediatr Infect Dis J. 2012;31(8):e105–10.CrossRefPubMed
28.
go back to reference Chart H. The pathogenicity of strains of Salmonella paratyphi B and Salmonella java. J Appl Microbiol. 2003;94(2):340–8.CrossRefPubMed Chart H. The pathogenicity of strains of Salmonella paratyphi B and Salmonella java. J Appl Microbiol. 2003;94(2):340–8.CrossRefPubMed
29.
go back to reference Gobin M, Launders N, Lane C, Kafatos G, Adak B. National outbreak of Salmonella Java phage type 3b variant 9 infection using parallel case-control and case-case study designs, United Kingdom, July to October 2010. Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin. 2011;16(47):20023. Gobin M, Launders N, Lane C, Kafatos G, Adak B. National outbreak of Salmonella Java phage type 3b variant 9 infection using parallel case-control and case-case study designs, United Kingdom, July to October 2010. Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin. 2011;16(47):20023.
30.
go back to reference Koch K, Kristensen B, Holt HM, Ethelberg S, Molbak K, Schonheyder HC. International travel and the risk of hospitalization with non-typhoidal Salmonella bacteremia. A Danish population-based cohort study, 1999-2008. BMC Infect Dis. 2011;11:277.CrossRefPubMedPubMedCentral Koch K, Kristensen B, Holt HM, Ethelberg S, Molbak K, Schonheyder HC. International travel and the risk of hospitalization with non-typhoidal Salmonella bacteremia. A Danish population-based cohort study, 1999-2008. BMC Infect Dis. 2011;11:277.CrossRefPubMedPubMedCentral
31.
go back to reference Laupland KB, Schonheyder HC, Kennedy KJ, Lyytikainen O, Valiquette L, Galbraith J, et al. Salmonella enterica bacteraemia: a multi-national population-based cohort study. BMC Infect Dis. 2010;10:95.CrossRefPubMedPubMedCentral Laupland KB, Schonheyder HC, Kennedy KJ, Lyytikainen O, Valiquette L, Galbraith J, et al. Salmonella enterica bacteraemia: a multi-national population-based cohort study. BMC Infect Dis. 2010;10:95.CrossRefPubMedPubMedCentral
32.
go back to reference Keddy KH, Sooka A, Musekiwa A, Smith AM, Ismail H, Tau NP, et al. Clinical and Microbiological Features of Salmonella Meningitis in a South African Population, 2003–2013. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America 2015, 61 Suppl 4:S272–S282.CrossRefPubMedPubMedCentral Keddy KH, Sooka A, Musekiwa A, Smith AM, Ismail H, Tau NP, et al. Clinical and Microbiological Features of Salmonella Meningitis in a South African Population, 2003–2013. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America 2015, 61 Suppl 4:S272–S282.CrossRefPubMedPubMedCentral
33.
go back to reference Lee WS, Puthucheary SD, Omar A. Salmonella meningitis and its complications in infants. J Paediatr Child Health. 1999;35(4):379–82.CrossRefPubMed Lee WS, Puthucheary SD, Omar A. Salmonella meningitis and its complications in infants. J Paediatr Child Health. 1999;35(4):379–82.CrossRefPubMed
34.
go back to reference Wen SC, Best E, Nourse C. Non-typhoidal Salmonella infections in children: review of literature and recommendations for management. J Paediatr Child Health. 2017;53(10):936–41.CrossRefPubMed Wen SC, Best E, Nourse C. Non-typhoidal Salmonella infections in children: review of literature and recommendations for management. J Paediatr Child Health. 2017;53(10):936–41.CrossRefPubMed
35.
go back to reference Lavy CB. Septic arthritis in Western and sub-Saharan African children-a review. Int Orthop. 2007;31(2):137–44.CrossRefPubMed Lavy CB. Septic arthritis in Western and sub-Saharan African children-a review. Int Orthop. 2007;31(2):137–44.CrossRefPubMed
36.
go back to reference Levings RS, Lightfoot D, Partridge SR, Hall RM, Djordjevic SP. The genomic island SGI1, containing the multiple antibiotic resistance region of Salmonella enterica serovar typhimurium DT104 or variants of it, is widely distributed in other S. enterica serovars. J Bacteriol. 2005;187(13):4401–9.CrossRefPubMedPubMedCentral Levings RS, Lightfoot D, Partridge SR, Hall RM, Djordjevic SP. The genomic island SGI1, containing the multiple antibiotic resistance region of Salmonella enterica serovar typhimurium DT104 or variants of it, is widely distributed in other S. enterica serovars. J Bacteriol. 2005;187(13):4401–9.CrossRefPubMedPubMedCentral
37.
go back to reference Djordjevic SP, Cain AK, Evershed NJ, Falconer L, Levings RS, Lightfoot D, et al. Emergence and evolution of multiply antibiotic-resistant Salmonella enterica serovar Paratyphi B D-tartrate-utilizing strains containing SGI1. Antimicrob Agents Chemother. 2009;53(6):2319–26.CrossRefPubMedPubMedCentral Djordjevic SP, Cain AK, Evershed NJ, Falconer L, Levings RS, Lightfoot D, et al. Emergence and evolution of multiply antibiotic-resistant Salmonella enterica serovar Paratyphi B D-tartrate-utilizing strains containing SGI1. Antimicrob Agents Chemother. 2009;53(6):2319–26.CrossRefPubMedPubMedCentral
38.
go back to reference Mulvey MR, Boyd D, Cloeckaert A, Ahmed R, Ng LK. Emergence of multidrug-resistant Salmonella Paratyphi B dT+, Canada. Emerg Infect Dis. 2004;10(7):1307–10.CrossRefPubMedPubMedCentral Mulvey MR, Boyd D, Cloeckaert A, Ahmed R, Ng LK. Emergence of multidrug-resistant Salmonella Paratyphi B dT+, Canada. Emerg Infect Dis. 2004;10(7):1307–10.CrossRefPubMedPubMedCentral
39.
go back to reference Ministry of Health Malaysia. National Antibiotic Guideline. In: Ministry of Health Malaysia; 2008. Ministry of Health Malaysia. National Antibiotic Guideline. In: Ministry of Health Malaysia; 2008.
Metadata
Title
Invasive Salmonella infections among children in Bintulu, Sarawak, Malaysian Borneo: a 6-year retrospective review
Authors
Anand Mohan
Chandran Munusamy
Yee-Chin Tan
Sobana Muthuvelu
Rohaidah Hashim
Su-Lin Chien
Ming-Kui Wong
Nurul Aiman Khairuddin
Yuwana Podin
Peter Sie-Teck Lau
David Chun-Ern Ng
Mong-How Ooi
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2019
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-019-3963-x

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