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Salmonella Bloodstream Infections in Hospitalized Children with Acute Febrile Illness—Uganda, 2016–2019
Grace D. Appiah
Grace D. Appiah
Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Arthur Mpimbaza
Arthur Mpimbaza
Infectious Disease Research Collaboration, Kampala, Uganda;
Child Health and Development Center, Makerere University, Kampala, Uganda;
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Child Health and Development Center, Makerere University, Kampala, Uganda;
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Mohammed Lamorde
Mohammed Lamorde
Infectious Diseases Institute, Kampala, Uganda;
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Molly Freeman
Molly Freeman
Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Henry Kajumbula
Henry Kajumbula
Department of Microbiology, Makerere University, Kampala, Uganda;
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Zainab Salah
Zainab Salah
Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Kiersten Kugeler
Kiersten Kugeler
Division of Vector-Borne Disease, Centers for Disease Control and Prevention, Fort Collins, Colorado;
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Matthew Mikoleit
Matthew Mikoleit
Division of Global Health Protection, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Porscha Bumpus White
Porscha Bumpus White
Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia;
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James Kapisi
James Kapisi
Infectious Disease Research Collaboration, Kampala, Uganda;
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Jeff Borchert
Jeff Borchert
Division of Vector-Borne Disease, Centers for Disease Control and Prevention, Fort Collins, Colorado;
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Asadu Sserwanga
Asadu Sserwanga
Infectious Disease Research Collaboration, Kampala, Uganda;
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Susan Van Dyne
Susan Van Dyne
Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Paul Mead
Paul Mead
Division of Vector-Borne Disease, Centers for Disease Control and Prevention, Fort Collins, Colorado;
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Sunkyung Kim
Sunkyung Kim
Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Ana C. Lauer
Ana C. Lauer
Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Alison Winstead
Alison Winstead
Division of Parasitic Disease and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Yukari C. Manabe
Yukari C. Manabe
Division of Infectious Diseases, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland
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Robert J. Flick
Robert J. Flick
Division of Infectious Diseases, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland
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Eric Mintz
Eric Mintz
Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Abstract.
Invasive Salmonella infection is a common cause of acute febrile illness (AFI) among children in sub-Saharan Africa; however, diagnosing Salmonella bacteremia is challenging in settings without blood culture. The Uganda AFI surveillance system includes blood culture-based surveillance for etiologies of bloodstream infection (BSIs) in hospitalized febrile children in Uganda. We analyzed demographic, clinical, blood culture, and antimicrobial resistance data from hospitalized children at six sentinel AFI sites from July 2016 to January 2019. A total of 47,261 children were hospitalized. Median age was 2 years (interquartile range, 1–4) and 26,695 (57%) were male. Of 7,203 blood cultures, 242 (3%) yielded bacterial pathogens including Salmonella (N = 67, 28%), Staphylococcus aureus (N = 40, 17%), Escherichia spp. (N = 25, 10%), Enterococcus spp. (N = 18, 7%), and Klebsiella pneumoniae (N = 17, 7%). Children with BSIs had longer median length of hospitalization (5 days versus 4 days), and a higher case-fatality ratio (13% versus 2%) than children without BSI (all P < 0.001). Children with Salmonella BSIs did not differ significantly in length of hospitalization or mortality from children with BSI resulting from other organisms. Serotype and antimicrobial susceptibility results were available for 49 Salmonella isolates, including 35 (71%) non-typhoidal serotypes and 14 Salmonella serotype Typhi (Typhi). Among Typhi isolates, 10 (71%) were multi-drug resistant and 13 (93%) had decreased ciprofloxacin susceptibility. Salmonella strains, particularly non-typhoidal serotypes and drug-resistant Typhi, were the most common cause of BSI. These data can inform regional Salmonella surveillance in East Africa and guide empiric therapy and prevention in Uganda.
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Author Notes
Financial support: The funding for this work was supported through a CDC cooperative agreement (no. 5NU2GGH001744-02-00).
Disclaimer: The opinions expressed by authors contributing to this manuscript do not necessarily reflect the opinions of the CDC or the institutions with which the authors are affiliated.
Authors’ addresses: Grace D. Appiah, Molly Freeman, Zainab Salah, Porscha Bumpus White, Susan Van Dyne, Sunkyung Kim, Ana C. Lauer, and Eric Mintz, Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, GA, E-mails: gappiah@cdc.gov, evy7@cdc.gov, pli1@cdc.gov, ofu1@cdc.gov, mdv9@cdc.gov, wox0@cdc.gov, ybp6@cdc.gov, and edm1@cdc.gov. Arthur Mpimbaza, Infectious Disease Research Collaboration, Kampala, Uganda, and Child Health and Development Center, Makerere University, Kampala, Uganda, E-mail: arthurwakg@yahoo.com. Mohammed Lamorde, Infectious Diseases Institute, Kampala, Uganda, E-mail: mlamorde@idi.co.ug. Henry Kajumbula, Department of Microbiology, Makerere University, Kampala, Uganda, E-mail: henrykajumbula427@gmail.com. Kiersten Kugeler, Jeff Borchert, and Paul Mead, Division of Vector-Borne Disease, Centers for Disease Control and Prevention, Fort Collins, CO, E-mails: bio1@cdc.gov, gqx1@cdc.gov, and pfm0@cdc.gov. Matt Mikoleit, Division of Global Health Protection, Centers for Disease Control and Prevention, Atlanta, GA, E-mail: euh1@cdc.gov. James Kapisi and Asadu Sserwanga, Infectious Disease Research Collaboration, Kampala, Uganda, E-mails: jkapisi@idrc-uganda.org and asadusserwanga@gmail.com. Alison Winstead, Division of Parasitic Disease and Malaria, Centers for Disease Control and Prevention, Atlanta, GA, E-mail: nrc0@cdc.gov. Yukari C. Manabe and Robert J. Flick, Division of Infectious Diseases, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, E-mails: ymanabe@jhmi.edu and rjf@jhmi.edu.
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1.
Crump JA , Youssef FG , Luby SP , Wasfy MO , Rangel JM , Taalat M , Oun SA , Mahoney FJ , 2003. Estimating the incidence of typhoid fever and other febrile illnesses in developing countries. Emerg Infect Dis 9: 539.
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2.
Crump JA , 2012. Typhoid fever and the challenge of nonmalaria febrile illness in sub-Saharan Africa. Clin Infect Dis 54: 1107–1109.
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3.
Prasad N , Murdoch DR , Reyburn H , Crump JA , 2015. Etiology of severe febrile illness in low-and middle-income countries: a systematic review. PLoS One 10: e0127962.
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4.
Marchello CS , Dale AP , Pisharody S , Rubach MP , Crump JA , 2019. Prevalence of community-acquired bloodstream infections among hospitalized patients in Africa and Asia: a systematic review and meta-analysis. Antimicrob Agents Chemother 64: e01974–e019.
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Stanaway JD , Reiner RC , Blacker BF , Goldberg EM , Khalil IA , Troeger CE , Andrews JR , Bhutta ZA , Crump JA , Im J , 2019. The global burden of typhoid and paratyphoid fevers: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Infect Dis 19: 369–381.
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6.
Stanaway JD , Parisi A , Sarkar K , Blacker BF , Reiner RC , Hay SI , Nixon MR , Dolecek C , James SL , Mokdad AH , 2019. The global burden of non-typhoidal Salmonella invasive disease: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Infect Dis 19: 1312–1324.
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7.
Crump JA , 2019. Progress in typhoid fever epidemiology. Clin Infect Dis 68: S4–S9.
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8.
Andrews JR , Barkume C , Yu AT , Saha SK , Qamar FN , Garrett D , Luby SP , 2018. Integrating facility-based surveillance with healthcare utilization surveys to estimate enteric fever incidence: methods and challenges. J Infect Dis 218: S268–S276.
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Marks F , Von Kalckreuth V , Aaby P , Adu-Sarkodie Y , El Tayeb MA , Ali M , Aseffa A , Baker S , Biggs HM , Bjerregaard-Andersen M , 2017. Incidence of invasive Salmonella disease in sub-Saharan Africa: a multicentre population-based surveillance study. Lancet Glob Health 5: e310–e323.
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