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Cited by 44Salmonella and Campylobacter epidemiologyBacterial Infections and VaccinesAntibiotic Use and Resistance

Multidrug-resistant Nontyphoidal Salmonella Hotspots as Targets for Vaccine Use in Management of Infections in Endemic Settings

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Kariuki, Samuel, Mbae, Cecilia, Onsare, Robert, Kavai, Susan M, Wairimu, Celestine, Ngetich, Ronald, Ali, Mohammad, Clemens, John +1 more·2019·Clinical Infectious Diseases
DOI 10.1093/cid/ciy898PMC PMC6376148
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Abstract

BACKGROUND: Salmonella infections cause a disproportionately high number of deaths in Africa, especially among poor urban populations. The increasing level of multidrug-resistant (MDR) infections is a major cause of concern in these settings where alternative effective treatment is unavailable. Other options for management of these infections must be sought. The knowledge of hotspots in endemic settings can help to prioritize management and control measures in Kenya and the region. METHODS: Using blood cultures, we investigated children presenting with fever of unknown origin for Salmonella infections. We performed antimicrobial susceptibility testing and whole genome sequencing to further characterize Salmonella isolates. Using Global Positioning System technologies, we mapped Salmonella isolates to households of patients in the study site and determined risk factors associated with high concentration of cases in particular sites. RESULTS: A total of 281 Salmonella species (149 from blood and 132 from fecal samples) from febrile children <5 years of age were studied. These consisted of 85 Salmonella Typhimurium, 58 Salmonella Enteritidis, 32 other nontyphoidal Salmonella (NTS) serotypes, and 126 Salmonella Typhi. The prevalence of MDR invasive NTS (iNTS) was 77.2%, with 15% resistant to ceftriaxone, a drug that is last-line treatment for iNTS and other severe gram-negative infections in Kenya. Invasive NTS and S. Typhi together mapped around common water vending points and close to sewer convergence points in the highly populated village. CONCLUSIONS: These hotspots could be targeted for management and control strategies, including a combined introduction of typhoid and iNTS vaccines, aimed at reducing transmission in these endemic settings.

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  • Invasive strains of multidrug-resistant non-typhoidal Salmonella circulating in sub-Saharan Africa are predominantly Salmonella Typhimurium ST313 and Salmonella Enteritidis ST11, although Salmonella Dublin ST10 has only been associated with resistance in West Africa.

    “Invasive strains of multidrug-resistant NTS circulating in SSA are predominantly S. Typhimurium ST313 and S. Enteritidis ST11, although S. Dublin ST10 has only been associated with resistance in West Africa.96,104”

    From Antimicrobial Resistance Rates and Surveillance in Sub-Saharan Africa: Where Are We Now? (2022) · cites this paper as [96]

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Research works printed but not linked: 31

  1. [1]Majowicz SE, Musto J, Scallan E, et al; International Collaboration on Enteric Disease Burden of Illness Studies The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 2010; 50: 882– 9. 20158401
  2. [2]Murray CJL, Vos T, Lozano R, et al. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012; 380: 2197– 223. 23245608
  3. [3]Crump JA, Sjölund-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: 901– 37. 26180063 PMC4503790
  4. [4]Ao TT, Feasey NA, Gordon MA, Keddy KH, Angulo FJ, Crump JA Global burden of invasive nontyphoidal Salmonella disease. Emerg Infect Dis 2015; 21: 941– 9. PMC4451910 25860298
  5. [5]Muthumbi E, Morpeth SC, Ooko M, et al. Invasive salmonellosis in Kilifi, Kenya. Clin Infect Dis 2015; 61(Suppl 4): S290– 301. 26449944 PMC4596936
  6. [6]Haselbeck AH, Panzner U, Im J, Baker S, Meyer CG, Marks F Current perspectives on invasive nontyphoidal Salmonella disease. Curr Opin Infect Dis 2017; 30: 498– 503. 28731899 PMC7680934
  7. [7]Kariuki S, Onsare RS Epidemiology and genomics of invasive nontyphoidal Salmonella infections in Kenya. Clin Infect Dis 2015; 61(Suppl 4): S317– 24. 26449947 PMC4596933
  8. [8]Feasey NA, Masesa C, Jassi C, et al Three epidemics of invasive multidrug-resistant Salmonella bloodstream infection in Blantyre, Malawi, 1998–2014. Clin Infect Dis 2015; 61: S363– 71. 26449953 PMC4596930
  9. [9]Kalonji LM, Post A, Phoba MF, et al Invasive Salmonella infections at multiple surveillance sites in the Democratic Republic of the Congo, 2011–2014. Clin Infect Dis 2015; 61: S346– 53. 26449951
  10. [10]Obaro SK, Hassan-Hanga F, Olateju EK, et al. Salmonella bacteremia among children in central and northwest Nigeria, 2008-2015. Clin Infect Dis 2015; 61(Suppl 4): S325– 31. 26449948 PMC4596937
  11. [11]Eibach D, Al-Emran HM, Dekker DM, et al. The emergence of reduced ciprofloxacin susceptibility in Salmonella enterica causing bloodstream infections in rural Ghana. Clin Infect Dis 2016; 62(Suppl 1): S32– 6. 26933017
  12. [12]Feasey N, Wansbrough-Jones M, Mabey DC, Solomon AW Neglected tropical diseases. Br Med Bull 2010; 93: 179– 200. 20007668
  13. [13]Moon TD, Johnson M, Foster MA, et al. Identification of Invasive Salmonella enterica serovar Typhimurium ST313 in ambulatory HIV-infected adults in Mozambique. J Glob Infect Dis 2015; 7: 139– 42. 26751031 PMC4693304
  14. [14]Kariuki S, Revathi G, Kariuki N, et al. Invasive multidrug-resistant non-typhoidal Salmonella infections in Africa: zoonotic or anthroponotic transmission? J Med Microbiol 2006; 55: 585– 91. 16585646
  15. [15]Kariuki S, Gordon MA, Feasey N, Parry CM Antimicrobial resistance and management of invasive Salmonella disease. Vaccine 2015; 33(Suppl 3): C21– 9. 25912288 PMC4469558
  16. [16]Bachou H, Tylleskär T, Kaddu-Mulindwa DH, Tumwine JK Bacteraemia among severely malnourished children infected and uninfected with the human immunodeficiency virus-1 in Kampala, Uganda. BMC Infect Dis 2006; 6: 160. 17090299 PMC1660577
  17. [17]Ikumapayi UN, Antonio M, Sonne-Hansen J, et al. Molecular epidemiology of community-acquired invasive non-typhoidal Salmonella among children aged 2–29 months in rural Gambia and discovery of a new serovar, Salmonella enterica Dingiri. J Med Microbiol 2007; 56: 1479– 84. 17965348
  18. [18]Vandenberg O, Nyarukweba DZ, Ndeba PM, et al. Microbiologic and clinical features of Salmonella species isolated from bacteremic children in eastern Democratic Republic of Congo. Pediatr Infect Dis J 2010; 29: 504– 10. 20104200
  19. [19]Kariuki S, Dougan G Antibacterial resistance in sub-Saharan Africa: an underestimated emergency. Ann N Y Acad Sci 2014; 1323: 43– 55. 24628272 PMC4159419
  20. [20]Feasey NA, Houston A, Mukaka M, et al. A reduction in adult blood stream infection and case fatality at a large African hospital following antiretroviral therapy roll-out. PLoS One 2014; 9: e92226. 24643091 PMC3958486
  21. [21]Maltha J, Guiraud I, Kaboré B, et al. Frequency of severe malaria and invasive bacterial infections among children admitted to a rural hospital in Burkina Faso. PLoS One 2014; 9: e89103. 24551225 PMC3925230
  22. [22]Mutisya M, Orindi B, Emina J, Zulu E, Ye Y Is mortality among under-five children in Nairobi slums seasonal? Trop Med Int Health 2010; 15: 132– 9. 19883400
  23. [23]van de Vijver S, Oti S, Oduor C, et al Challenges of health programmes in slums. Lancet 2015; 386: 2114– 6. 26452707
  24. [25]Kariuki S, Okoro C, Kiiru J, et al. Ceftriaxone-resistant Salmonella enterica serotype Typhimurium sequence type 313 from Kenyan patients is associated with the blaCTX-M-15 gene on a novel IncHI2 plasmid. Antimicrob Agents Chemother 2015; 59: 3133– 9. 25779570 PMC4432211
  25. [26]Argimón S, Abudahab K, Goater RJ, et al. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microb Genom 2016; 2: e000093. 28348833 PMC5320705
  26. [27]Menezes GA, Khan MA, Harish BN, et al Molecular characterization of antimicrobial resistance in non-typhoidal salmonellae associated with systemic manifestations from India. J Med Microbiol 2010; 59: 1477– 83. 20813852
  27. [28]Tabu C, Breiman RF, Ochieng B, et al. Differing burden and epidemiology of non-Typhi Salmonella bacteremia in rural and urban Kenya, 2006–2009. PloS One 2012; 7: e31237. 22363591 PMC3283637
  28. [29]Leekitcharoenphon P, Friis C, Zankari E, et al. Genomics of an emerging clone of Salmonella serovar Typhimurium ST313 from Nigeria and the Democratic Republic of Congo. J Infect Dev Ctries 2013; 7: 696– 706. 24129621
  29. [30]Mandomando I, Bassat Q, Sigaúque B, et al. Invasive Salmonella infections among children from rural Mozambique, 2001–2014. Clin Infect Dis 2015; 61: S339– 45 26449950
  30. [31]World Health Organization. Typhoid vaccines: WHO position paper. Wkly Epidemiol Rec 2008; 83: 49– 59. 18260212
  31. [32]Okoro CK, Barquist L, Connor TR, et al. Signatures of adaptation in human invasive Salmonella Typhimurium ST313 populations from sub-Saharan Africa. PLoS Negl Trop Dis 2015; 9: e0003611. 25803844 PMC4372345

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Authors
Kariuki, S., Mbae, C., Onsare, R., Kavai, S. M., Wairimu, C., Ngetich, R., Ali, M., Clemens, J., & Dougan, G.
Affiliations
  • Kenya Medical Research Institute (KE)
  • Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi
  • Johns Hopkins University (US)
  • International Centre for Diarrhoeal Disease Research (BD)
  • Department of Medicine, University of Cambridge, United Kingdom
Corresponding author
Kariuki, Samuel
ORCID
Venue
Clinical Infectious Diseases
Publisher
Oxford University Press (OUP)
Published
2019-02-15
Volume
68
Issue
Supplement_1
Pages
S10-S15
ISSN
  • 1058-4838 (ISSN-L)
  • 1537-6591
DOI
10.1093/cid/ciy898
PMC
PMC6376148
OpenAlex
W2912585496
Cited by
44
References
1
Citations by year
2026: 3 · 2025: 7 · 2024: 9 · 2023: 7 · 2022: 5 · 2021: 5 · 2020: 8
FWCI
3.05
Type
journal article
Language
en
Open access
Licence
Locations
  • Clinical Infectious Diseases (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • Apollo (cc-by)
  • Greater South Information System
Funders
  • National Institute of Allergy and Infectious Diseases
  • National Institutes of Health (1R01AI099525)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
  • Life Sciences › Immunology and Microbiology › Microbiology › Bacterial Infections and Vaccines
  • Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
Keywords
multidrug-resistant Salmonella, non-typhoidal Salmonella, invasive Salmonella infection, hot spots, typhoid fever, Salmonella typhi, Salmonella typhimurium, Salmonella Enteritidis, pediatric fever, ceftriaxone resistance, typhoid vaccine, vaccine introduction, Kenya
MeSH terms
Adolescent, Anti-Bacterial Agents, Child, Child, Preschool, Feces, Genotype, Humans, Infant, Kenya, Salmonella, Salmonella Infections, Endemic Diseases, Salmonella Vaccines, Drug Resistance, Multiple, Bacterial, Serogroup

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