Multidrug-Resistant Salmonella enterica Serotype Typhi, Gulf of Guinea Region, Africa

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Murielle Baltazar12, Antoinette Ngandjio1, Kathryn Elizabeth Holt, Elodie Lepillet, Maria Pardos de la Gandara3, Jean-Marc Collard, Raymond Bercion4, Ariane Nzouankeu, Simon Le Hello, Gordon Dougan, Marie-Christine Fonkoua, and François-Xavier Weill

Author affiliations: Institut Pasteur, Paris, France (M. Baltazar, E. Lepillet, M. Pardos de la Gandara, S. Le Hello, F.-X. Weill); Centre Pasteur du Cameroun, Yaoundé, Cameroon (A. Ngandjio, A. Nzouankeu, M.-C. Fonkoua);University of Melbourne, Melbourne, Victoria, Australia (K.E. Holt); Wellcome Trust Sanger Institute, Cambridge, UK (K.E. Holt, G. Dougan); Scientific Institute of Public Health, Brussels, Belgium (J.-M. Collard); Institut Pasteur de Bangui, Bangui, Central African Republic (R. Bercion)

Abstract

We identified 3 lineages among multidrug-resistant (MDR) Salmonella enterica serotype Typhi isolates in the Gulf of Guinea region in Africa during the 2000s. However, the MDR H58 haplotype, which predominates in southern Asia and Kenya, was not identified. MDR quinolone-susceptible isolates contained a 190-kb incHI1 pST2 plasmid or a 50-kb incN pST3 plasmid.

Typhoid fever, which is caused by Salmonella enterica serotype Typhi, is endemic to the developing world; there were an estimated 26.7 million cases in 2010 (1). The incidence of typhoid fever in sub-Saharan Africa was an estimated 725 cases/100,000 persons in 2010, despite a lack of incidence studies conducted in West and central Africa (1). Antimicrobial susceptibility data are also scarce for this part of Africa. This issue is problematic because treatment with appropriate antimicrobial drugs is essential for recovery in the context of the global emergence of multidrug resistance.

In the Indian subcontinent and Southeast Asia, the multidrug-resistant (MDR) Salmonella Typhi H58 clone, which was named after its haplotype (a combination of defined chromosomal single-nucleotide polymorphisms [SNPs]) (2,3), has spread rapidly and become endemic and predominant. During the 1990s, this clone acquired a large conjugative incHI1 pST6 plasmid encoding resistance to ampicillin, chloramphenicol, and co-trimoxazole (4,5); also in the 1990s, this MDR clone became resistant to quinolones and showed decreased susceptibility to ciprofloxacin because of point mutations in the chromosomal gyrA gene (2). The H58 clone has also spread to eastern Africa, where it has been the most prevalent haplotype (87%) in Kenya since the early 2000s (6).

During 1997–2011, high incidence of MDR Salmonella Typhi was reported in some countries near the Gulf of Guinea in Africa, including Nigeria (7), Ghana (8,9), Togo (10), and the Democratic Republic of the Congo (11). During 1999–2003, a British surveillance system reported a prevalence of 19% (49/421) for MDR Salmonella Typhi isolates among imported cases of typhoid fever acquired in Africa, particularly in Ghana (12). However, nothing is known about the genotypes of these isolates, including whether they belong to the spreading MDR H58 clone.

We report data for the occurrence, genotypes, and characterization of the resistance mechanisms of MDR Salmonella Typhi isolates. These isolates were obtained from the French National Reference Center for Salmonella (FNRC-Salm), Institut Pasteur (Paris, France), and Centre Pasteur du Cameroun (Yaoundé, Cameroon).

Acknowledgments

We thank all the corresponding laboratories of the FNRC-Salm network for participating in this study.

This study was supported by the Institut Pasteur, the Réseau International des Instituts Pasteur, the Institut de Veille Sanitaire, and the French Government Investissement d'Avenir Program (Integrative Biology of Emerging Infectious Diseases, Laboratory of Excellence, grant ANR-10-LABX-62-IBEID).

References

Buckle GC, Walker CL, Black RE. Typhoid fever and paratyphoid fever: systematic review to estimate global morbidity and mortality for 2010. J Glob Health. 2012;2:010401. DOI PubMed
Roumagnac P, Weill FX, Dolecek C, Baker S, Brisse S, Chinh NT, Evolutionary history of Salmonella Typhi. Science. 2006;314:1301–4.DOI PubMed
Holt KE, Parkhill J, Mazzoni CJ, Roumagnac P, Weill FX, Goodhead I, High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat Genet. 2008;40:987–93. DOI PubMed
Phan MD, Kidgell C, Nair S, Holt KE, Turner AK, Hinds J, Variation in Salmonella enterica serovar Typhi IncHI1 plasmids during the global spread of resistant typhoid fever. Antimicrob Agents Chemother. 2009;53:716–27. DOI PubMed
Holt KE, Phan MD, Baker S, Duy PT, Nga TV, Nair S, Emergence of a globally dominant IncHI1 plasmid type associated with multiple drug resistant typhoid. PLoS Negl Trop Dis. 2011;5:e1245. DOI PubMed
Kariuki S, Revathi G, Kiiru J, Mengo DM, Mwituria J, Muyodi J, Typhoid in Kenya is associated with a dominant multidrug-resistant Salmonella enterica serovar Typhi haplotype that is also widespread in Southeast Asia. J Clin Microbiol. 2010;48:2171–6. DOI PubMed
Akinyemi KO, Coker AO. Trends of antibiotic resistance in Salmonella enterica serovar typhi isolated from hospitalized patients from 1997 to 2004 in Lagos, Nigeria. Indian J Med Microbiol. 2007;25:436–7. DOI PubMed
Mills-Robertson F, Addy ME, Mensah P, Crupper SS. Molecular characterization of antibiotic resistance in clinical Salmonella typhi isolated in Ghana.FEMS Microbiol Lett. 2002;215:249–53. DOI PubMed
Gross U, Amuzu SK, de Ciman R, Kassimova I, Gross L, Rabsch W, Bacteremia and antimicrobial drug resistance over time, Ghana. Emerg Infect Dis.2011;17:1879–82. DOI PubMed
Dagnra AY, Akolly K, Gbadoe A, Aho K, David M. Emergence of multidrug resistant Salmonella strains in Lome (Togo) [in French]. Med Mal Infect.2007;37:266–9. DOI PubMed
Lunguya O, Lejon V, Phoba MF, Bertrand S, Vanhoof R, Verhaegen J, . Salmonella Typhi in the Democratic Republic of the Congo: fluoroquinolone decreased susceptibility on the rise. EPLoS Negl Trop Dis. 2012; 6:e1921. Doe: . Pub 2012 Nov 5.DOI
Cooke FJ, Day M, Wain J, Ward LR, Threlfall EJ. Cases of typhoid fever imported to England, Scotland and Wales (2000–2003). Trans R Soc Trop Med Hyg. 2007;101:398–404. DOI PubMed
Loury P, Tillaut H, Faisant M, Paillereau N, Marquis M, Mari C, Cluster of typhoid fever cases in Ille-et-Vilaine (France), April 2009 [in French]. Bull Epidémiol Hebd. 2010;44:446–8.
Le Hello S, Harrois D, Bouchrif B, Sontag L, Elhani D, Guibert V, Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: a microbiological study. Lancet Infect Dis. 2013;13:672–9. DOI PubMed
Fabre L, Le Hello S, Roux C, Issenhuth-Jeanjean S, Weill FX. CRISPR is an optimal target for the design of specific PCR assays for Salmonella entericaserotypes Typhi and Paratyphi A. PLoS Negl Trop Dis. 2014;8:e2671 . DOI PubMed

Figures

Table

Table. Characteristics of Salmonella enterica serotype Typhi isolates, France and Cameroon, 1996–2013

Technical Appendix

. Characteristics of 61 serotype Typhi isolates and strains studied. 16 KB

Suggested citation for this article: Baltazar M, Ngandjio A, Holt KE, Lepillet E, Pardos de la Gandara M, Collard J-M, et al. Multidrug-resistant Salmonella enterica serotype Typhi, Gulf of Guinea Region, Africa. Emerg Infect Dis. 2015 Apr [date cited]. http://dx.doi.org/10.3201/eid2104.141355

DOI: 10.3201/eid2104.141355

1These authors contributed equally to this article.

2Current affiliation: University of Limoges, Limoges, France.

3Current affiliation: Rockefeller University, New York, New York, USA.

4Current affiliation: Institute Pasteur de Dakar, Dakar, Senegal.