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Epidemic increase in Salmonella bloodstream infection in children, Bwamanda, the Democratic Republic of Congo

European Journal of Clinical Microbiology & Infectious Diseases volume 33, pages 79–87 (2014)Cite this article

Abstract

Salmonella enterica is the leading cause of bloodstream infection in children in sub-Saharan Africa, but few data are available from Central-Africa. We documented during the period November 2011 to May 2012 an epidemic increase in invasive Salmonella bloodstream infections in HGR Bwamanda, a referral hospital in Equateur Province, DR Congo. Salmonella spp. represented 90.4 % (103 out of 114) of clinically significant blood culture isolates and comprised Salmonella Typhimurium (54.4 %, 56 out of 103), Salmonella Enteritidis (28.2 %, 29 out of 103) and Salmonella Typhi (17.5 %, 18 out of 103), with Salmonella Enteritidis accounting for most of the increase. Most (82 out of 103, 79.6 %) isolates were obtained from children < 5 years old. Median ages of patients infected with Salmonella Typhimurium and Salmonella Enteritidis were 14 months (14 days to 64 years) and 19 months (3 months to 8 years) respectively. Clinical presentation was non-specific; the in-hospital case fatality rate was 11.1 %. More than two thirds (69.7 %, 53 out of 76) of children < 5 years for whom laboratory data were available had Plasmodium falciparum infection. Most (83/85, 97.6 %) non-typhoid Salmonella isolates as well as 6/18 (33.3 %) Salmonella Typhi isolates were multidrug resistant (i.e. resistant to the first-line oral antibiotics amoxicillin, trimethoprim-sulfamethoxazole and chloramphenicol), one (1.0 %) Salmonella Typhimurium had decreased ciprofloxacin susceptibility owing to a point mutation in the gyrA gene (Gly81Cys). Multilocus variable-number tandem-repeat (MLVA) analysis of the Salmonella Enteritidis isolates revealed closely related patterns comprising three major and four minor profiles, with differences limited to one out of five loci. These data show an epidemic increase in clonally related multidrug-resistant Salmonella bloodstream infection in children in DR Congo.

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References

  1. Morpeth SC, Ramadhani HO, Crump JA (2009) Invasive non-Typhi Salmonella disease in Africa. Clin Infect Dis 49(4):606–611

    PubMed Central  PubMed  Article  Google Scholar 

  2. Mtove G, Amos B, von Seidlein L et al (2010) Invasive salmonellosis among children admitted to a rural Tanzanian hospital and a comparison with previous studies. PLoS One 5(2):e9244

    PubMed Central  PubMed  Article  Google Scholar 

  3. Brent AJ, Oundo JO, Mwangi I, Ochola L, Lowe B, Berkley JA (2006) Salmonella bacteremia in Kenyan children. Pediatr Infect Dis J 25(3):230–236

    PubMed  Article  Google Scholar 

  4. Enwere G, Biney E, Cheung YB et al (2006) Epidemiologic and clinical characteristics of community-acquired invasive bacterial infections in children aged 2–29 months in The Gambia. Pediatr Infect Dis J 25(8):700–705

    PubMed  Article  Google Scholar 

  5. Sigauque B, Roca A, Mandomando I et al (2009) Community-acquired bacteremia among children admitted to a rural hospital in Mozambique. Pediatr Infect Dis J 28(2):108–113

    PubMed  Article  Google Scholar 

  6. Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Koppen-Geiger climate classification updated. Meteorol Z 15(3):259–263

    Article  Google Scholar 

  7. Food and Health Organization of the United Nations. Interpolated Estimated Dekadal Rainfall by region: Democratic Republic of Congo (2007–2012). Available via: http://www.fao.org/giews/english/ierf/index.htm. Accessed 12 October 2012

  8. US Census Bureau. International Data Base; Available via: http://www.census.gov/population/international/data/idb/informationGateway.php Accessed 16 December 2011

  9. Lunguya O, Lejon V, Phoba MF et al (2012) Salmonella Typhi in the Democratic Republic of the Congo: fluoroquinolone decreased susceptibility on the rise. PLoS Negl Trop Dis 6(11):e1921

    PubMed Central  PubMed  Article  Google Scholar 

  10. Lunguya O, Lejon V, Phoba MF et al (2013) Antimicrobial resistance in invasive non-typhoid Salmonella from the Democratic Republic of the Congo: emergence of decreased fluoroquinolone susceptibility and extended-spectrum beta lactamases. PLoS Negl Trop Dis 7(3):e2103

    PubMed Central  PubMed  Article  Google Scholar 

  11. CLSI (2013) Performance standards for antimicrobial susceptibility testing; twenty-third informational supplement. CLSI document M100-S23 ed. Clinical and Laboratory Standards Institute, Wayne, PA

    Google Scholar 

  12. EUCAST. Clinical Breakpoints—bacteria (version 3.1) Available via EUCAST. http://www.eucast.org/clinical_breakpoints/ Accessed 14 May 2013

  13. World Health Organization CDSaRVaB (2003) The diagnosis, treatment and prevention of typhoid fever, 1st edn. World Health Organization, Geneva

    Google Scholar 

  14. Mukadi P, Gillet P, Lukuka A et al (2011) External quality assessment of malaria microscopy in the Democratic Republic of the Congo. Malar J 10:308

    PubMed Central  PubMed  Article  Google Scholar 

  15. World Health Organization (1980) Manual of basic techniques for a health laboratory. World Health Organization, Geneva

    Google Scholar 

  16. World Health Organization (2005) Pocket book of hospital care for children. World Health Organization, Geneva

    Google Scholar 

  17. Griggs DJ, Gensberg K, Piddock LJ (1996) Mutations in gyrA gene of quinolone-resistant Salmonella serotypes isolated from humans and animals. Antimicrob Agents Chemother 40(4):1009–1013

    CAS  PubMed Central  PubMed  Google Scholar 

  18. Cavaco LM, Hasman H, Xia S, Aarestrup FM (2009) qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother 53(2):603–608

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  19. Hopkins KL, Peters TM, de Pinna E, Wain J (2011) Standardisation of multilocus variable-number tandem-repeat analysis (MLVA) for subtyping of Salmonella enterica serovar Enteritidis. Euro Surveill 16(32)

  20. Phoba MF, Lunguya O, Mayimon DV et al (2012) Multidrug-resistant Salmonella enterica, Democratic Republic of the Congo. Emerg Infect Dis 18(10):1692–1694

    PubMed  Article  Google Scholar 

  21. Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA (2012) Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 379(9835):2489–2499

    PubMed Central  PubMed  Article  Google Scholar 

  22. Berkley JA, Maitland K, Mwangi I et al (2005) Use of clinical syndromes to target antibiotic prescribing in seriously ill children in malaria endemic area: observational study. BMJ 330(7498):995

    PubMed  Article  Google Scholar 

  23. Lunguya O, Phoba MF, Mundeke SA et al (2012) The diagnosis of typhoid fever in the Democratic Republic of the Congo. Trans Royal Soc Trop Med Hyg 106:348–355

    Article  Google Scholar 

  24. Breiman RF, Cosmas L, Njuguna H et al (2012) Population-based incidence of typhoid fever in an urban informal settlement and a rural area in Kenya: implications for typhoid vaccine use in Africa. PLoS One 7(1):e29119

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  25. Bahwere P, Levy J, Hennart P et al (2001) Community-acquired bacteremia among hospitalized children in rural central Africa. Int J Infect Dis 5(4):180–188

    CAS  PubMed  Article  Google Scholar 

  26. Cheesbrough JS, Taxman BC, Green SD, Mewa FI, Numbi A (1997) Clinical definition for invasive Salmonella infection in African children. Pediatr Infect Dis J 16(3):277–283

    CAS  PubMed  Article  Google Scholar 

  27. Green SD, Cheesbrough JS (1993) Salmonella bacteraemia among young children at a rural hospital in western Zaire. Ann Trop Paediatr 13(1):45–53

    CAS  PubMed  Google Scholar 

  28. Vandenberg O, Nyarukweba DZ, Ndeba PM et al (2010) Microbiologic and clinical features of Salmonella species isolated from bacteremic children in eastern Democratic Republic of Congo. Pediatr Infect Dis J 29(6):504–510

    PubMed  Google Scholar 

  29. Okoro CK, Kingsley RA, Connor TR et al (2012) Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet 44(11):1215–1221

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  30. Berkley JA, Bejon P, Mwangi T et al (2009) HIV infection, malnutrition, and invasive bacterial infection among children with severe malaria. Clin Infect Dis 49(3):336–343

    PubMed Central  PubMed  Article  Google Scholar 

  31. Feasey NA, Archer BN, Heyderman RS et al (2010) Typhoid fever and invasive nontyphoid salmonellosis, Malawi and South Africa. Emerg Infect Dis 16(9):1448–1451

    PubMed  Article  Google Scholar 

  32. Bassat Q, Guinovart C, Sigauque B et al (2009) Severe malaria and concomitant bacteraemia in children admitted to a rural Mozambican hospital. Trop Med Int Health 14(9):1011–1019

    PubMed  Article  Google Scholar 

  33. Nadjm B, Amos B, Mtove G et al (2010) WHO guidelines for antimicrobial treatment in children admitted to hospital in an area of intense Plasmodium falciparum transmission: prospective study. BMJ 340:c1350

    PubMed Central  PubMed  Article  Google Scholar 

  34. Cunnington AJ, de Souza JB, Walther M, Riley EM (2012) Malaria impairs resistance to Salmonella through heme- and heme oxygenase-dependent dysfunctional granulocyte mobilization. Nat Med 18(1):120–127

    CAS  Article  Google Scholar 

  35. Roux CM, Butler BP, Chau JY et al (2010) Both hemolytic anemia and malaria parasite-specific factors increase susceptibility to nontyphoidal Salmonella enterica serovar Typhimurium infection in mice. Infect Immun 78(4):1520–1527

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  36. van Santen S, de Mast Q, Swinkels DW, van der Ven AJ (2013) The iron link between malaria and invasive non-typhoid Salmonella infections. Trends Parasitol 29(5):220–227

    PubMed  Article  Google Scholar 

  37. Wright RC (1986) The seasonality of bacterial quality of water in a tropical developing country (Sierra Leone). J Hyg (Lond) 96(1):75–82

    CAS  Article  Google Scholar 

  38. Kariuki S, Revathi G, Kariuki N et al (2006) Invasive multidrug-resistant non-typhoidal Salmonella infections in Africa: zoonotic or anthroponotic transmission? J Med Microbiol 55(Pt 5):585–591

    CAS  PubMed  Article  Google Scholar 

  39. Akinyemi KO, Bamiro BS, Coker AO (2007) Salmonellosis in Lagos, Nigeria: incidence of Plasmodium falciparum-associated co-infection, patterns of antimicrobial resistance, and emergence of reduced susceptibility to fluoroquinolones. J Health Popul Nutr 25(3):351–358

    PubMed  Google Scholar 

  40. Lutterloh E, Likaka A, Sejvar J et al (2012) Multidrug-resistant typhoid fever with neurologic findings on the Malawi-Mozambique border. Clin Infect Dis 54(8):1100–1106

    PubMed  Article  Google Scholar 

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Acknowledgements

The antibiotic resistance surveillance project in DR Congo is funded by Project 2.01 of the Third Framework Agreement between the Belgian Directorate General of Development Cooperation and the Institute of Tropical Medicine, Antwerp, Belgium. Marie-France Phoba has a scholarship of the Foundation Marguerite-Marie Delacroix, Tienen, Belgium.

Conflict of interest

The authors declare that they have no conflict of interest.

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Affiliations

  1. Department of Clinical Microbiology, National Institute for Biomedical Research, Kinshasa, The Democratic Republic of Congo

    M.-F. Phoba, O. Lunguya & J.-J. Muyembe

  2. Department of Microbiology, University Hospital of Kinshasa, Kinshasa, The Democratic Republic of Congo

    M.-F. Phoba, O. Lunguya & J.-J. Muyembe

  3. Department of Clinical Sciences, Institute of Tropical Medicine, Antwerp, Belgium

    H. De Boeck & J. Jacobs

  4. Health Zone and Hospital of Bwamanda, Bwamanda, The Democratic Republic of Congo

    B. B. Ifeka & J. Dawili

  5. Belgian National Reference Centre for Salmonella, Institute of Public Health, Brussels, Belgium

    R. Vanhoof & S. Bertrand

  6. Department of Pediatrics, University Hospital of Leuven, Leuven, Belgium

    C. Van Geet

  7. Institute of Tropical Medicine, Nationalestraat 155, 2000, Antwerp, Belgium

    H. De Boeck

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  1. M.-F. Phoba
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  2. H. De Boeck
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Correspondence to H. De Boeck.

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Phoba, MF., De Boeck, H., Ifeka, B.B. et al. Epidemic increase in Salmonella bloodstream infection in children, Bwamanda, the Democratic Republic of Congo. Eur J Clin Microbiol Infect Dis 33, 79–87 (2014). https://doi.org/10.1007/s10096-013-1931-8

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  • DOI: https://doi.org/10.1007/s10096-013-1931-8

Keywords

  • Malaria
  • Bloodstream Infection
  • Malaria Rapid Diagnostic Test
  • Health Zone
  • Blood Culture Isolate