Hassan M Al-Emran1, Daniel Eibach1, Ralf Krumkamp1, Mohammad Ali2, Stephen Baker3, Holly M Biggs4, Morten Bjerregaard-Andersen5, Robert F Breiman6, John D Clemens7, John A Crump8, Ligia Maria Cruz Espinoza9, Jessica Deerin9, Denise Myriam Dekker1, Amy Gassama Sow10, Julian T Hertz4, Justin Im9, Samuel Ibrango11, Vera von Kalckreuth9, Leon Parfait Kabore12, Frank Konings9, Sandra Valborg Løfberg5, Christian G Meyer13, Eric D Mintz14, Joel M Montgomery15, Beatrice Olack15, Gi Deok Pak9, Ursula Panzner9, Se Eun Park9, Jean Luco Tsiriniaina Razafindrabe16, Henintsoa Rabezanahary16, Jean Philibert Rakotondrainiarivelo16, Raphaël Rakotozandrindrainy16, Tiana Mirana Raminosoa16, Heidi Schütt-Gerowitt17, Emmanuel Sampo18, Abdramane Bassiahi Soura19, Adama Tall10, Michelle Warren9, Thomas F Wierzba9, Jürgen May1, Florian Marks9. 1. Bernhard Nocht Institute for Tropical Medicine German Center for Infection Research, partner site Hamburg-Borstel-Lübeck, Hamburg, Germany. 2. International Vaccine Institute, Seoul, Republic of Korea Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland. 3. Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam. 4. Division of Infectious Diseases and International Health, Duke University Medical Center Duke Global Health Institute, Duke University, Durham, North Carolina. 5. Bandim Health Project, Bissau, Guinea-Bissau Research Center for Vitamins and Vaccines, Copenhagen, Denmark. 6. Kenya Medical Research Institute-Centers for Disease Control and Prevention Kenya Collaboration, Nairobi Global Health Institute, Emory University, Atlanta, Georgia. 7. International Vaccine Institute, Seoul, Republic of Korea International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka. 8. Division of Infectious Diseases and International Health, Duke University Medical Center Duke Global Health Institute, Duke University, Durham, North Carolina Kilimanjaro Christian Medical Centre, Moshi, Tanzania Centre for International Health, University of Otago, Dunedin, New Zealand. 9. International Vaccine Institute, Seoul, Republic of Korea. 10. Institut Pasteur de Dakar, Université Cheikh Anta Diop de Dakar, Senegal. 11. Ministry of Health. 12. Schiphra Hospital, Ouagadougou, Burkina Faso. 13. Bernhard Nocht Institute for Tropical Medicine Institute of Tropical Medicine, Eberhard-Karls University Tübingen, Germany. 14. National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia. 15. Kenya Medical Research Institute-Centers for Disease Control and Prevention Kenya Collaboration, Nairobi. 16. University of Antananarivo, Madagascar. 17. International Vaccine Institute, Seoul, Republic of Korea Institute of Medical Microbiology, University of Cologne, Germany. 18. Institute of Medical Microbiology, University of Cologne, Germany. 19. University of Ouagadougou, Burkina Faso.
Abstract
BACKGROUND: Salmonella enterica serovar Typhi is a predominant cause of bloodstream infections in sub-Saharan Africa (SSA). Increasing numbers of S. Typhi with resistance to ciprofloxacin have been reported from different parts of the world. However, data from SSA are limited. In this study, we aimed to measure the ciprofloxacin susceptibility of S. Typhi isolated from patients with febrile illness in SSA. METHODS: Febrile patients from 9 sites within 6 countries in SSA with a body temperature of ≥38.0°C were enrolled in this study. Blood samples were obtained for bacterial culture, and Salmonella isolates were identified biochemically and confirmed by multiplex polymerase chain reaction (PCR). Antimicrobial susceptibility of all Salmonella isolates was performed by disk diffusion test, and minimum inhibitory concentrations (MICs) against ciprofloxacin were measured by Etest. All Salmonella isolates with reduced susceptibility to ciprofloxacin (MIC > 0.06 µg/mL) were screened for mutations in quinolone resistance-determining regions in target genes, and the presence of plasmid-mediated quinolone resistance (PMQR) genes was assessed by PCR. RESULTS: A total of 8161 blood cultures were performed, and 100 (1.2%) S. Typhi, 2 (<0.1%) Salmonella enterica serovar Paratyphi A, and 27 (0.3%) nontyphoid Salmonella (NTS) were isolated. Multidrug-resistant S. Typhi were isolated in Kenya (79% [n = 38]) and Tanzania (89% [n = 8]) only. Reduced ciprofloxacin-susceptible (22% [n = 11]) S. Typhi were isolated only in Kenya. Among those 11 isolates, all had a Glu133Gly mutation in the gyrA gene combined with either a gyrA (Ser83Phe) or gyrB mutation (Ser464Phe). One Salmonella Paratyphi A isolate with reduced susceptibility to ciprofloxacin was found in Senegal, with 1 mutation in gyrA (Ser83Phe) and a second mutation in parC (Ser57Phe). Mutations in the parE gene and PMQR genes were not detected in any isolate. CONCLUSIONS: Salmonella Typhi with reduced susceptibility to ciprofloxacin was not distributed homogenously throughout SSA. Its prevalence was very high in Kenya, and was not observed in other study countries. Continuous monitoring of antimicrobial susceptibility is required to follow the potential spread of antimicrobial-resistant isolates throughout SSA.
BACKGROUND:Salmonella enterica serovar Typhi is a predominant cause of bloodstream infections in sub-Saharan Africa (SSA). Increasing numbers of S. Typhi with resistance to ciprofloxacin have been reported from different parts of the world. However, data from SSA are limited. In this study, we aimed to measure the ciprofloxacin susceptibility of S. Typhi isolated from patients with febrile illness in SSA. METHODS: Febrile patients from 9 sites within 6 countries in SSA with a body temperature of ≥38.0°C were enrolled in this study. Blood samples were obtained for bacterial culture, and Salmonella isolates were identified biochemically and confirmed by multiplex polymerase chain reaction (PCR). Antimicrobial susceptibility of all Salmonella isolates was performed by disk diffusion test, and minimum inhibitory concentrations (MICs) against ciprofloxacin were measured by Etest. All Salmonella isolates with reduced susceptibility to ciprofloxacin (MIC > 0.06 µg/mL) were screened for mutations in quinolone resistance-determining regions in target genes, and the presence of plasmid-mediated quinolone resistance (PMQR) genes was assessed by PCR. RESULTS: A total of 8161 blood cultures were performed, and 100 (1.2%) S. Typhi, 2 (<0.1%) Salmonella enterica serovar Paratyphi A, and 27 (0.3%) nontyphoid Salmonella (NTS) were isolated. Multidrug-resistant S. Typhi were isolated in Kenya (79% [n = 38]) and Tanzania (89% [n = 8]) only. Reduced ciprofloxacin-susceptible (22% [n = 11]) S. Typhi were isolated only in Kenya. Among those 11 isolates, all had a Glu133Gly mutation in the gyrA gene combined with either a gyrA (Ser83Phe) or gyrB mutation (Ser464Phe). One Salmonella Paratyphi A isolate with reduced susceptibility to ciprofloxacin was found in Senegal, with 1 mutation in gyrA (Ser83Phe) and a second mutation in parC (Ser57Phe). Mutations in the parE gene and PMQR genes were not detected in any isolate. CONCLUSIONS:Salmonella Typhi with reduced susceptibility to ciprofloxacin was not distributed homogenously throughout SSA. Its prevalence was very high in Kenya, and was not observed in other study countries. Continuous monitoring of antimicrobial susceptibility is required to follow the potential spread of antimicrobial-resistant isolates throughout SSA.
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