The Lancet Global Health (Mar 2017)
Incidence of invasive salmonella disease in sub-Saharan Africa: a multicentre population-based surveillance study
- Florian Marks, DrPhD,
- Vera von Kalckreuth, MD,
- Peter Aaby, DMSc,
- Yaw Adu-Sarkodie, ProfPhD,
- Muna Ahmed El Tayeb, MD,
- Mohammad Ali, PhD,
- Abraham Aseffa, PhD,
- Stephen Baker, ProfPhD,
- Holly M Biggs, MD,
- Morten Bjerregaard-Andersen, PhD,
- Robert F Breiman, MD,
- James I Campbell, FIBMS,
- Leonard Cosmas, MPH,
- John A Crump, ProfMD,
- Ligia Maria Cruz Espinoza, MD,
- Jessica Fung Deerin, MPH,
- Denise Myriam Dekker, PhD,
- Barry S Fields, PhD,
- Nagla Gasmelseed, ProfPhD,
- Julian T Hertz, MD,
- Nguyen Van Minh Hoang, MSc,
- Justin Im, MSc,
- Anna Jaeger, BA,
- Hyon Jin Jeon, BA,
- Leon Parfait Kabore, MSc,
- Karen H Keddy, MMed,
- Frank Konings, PhD,
- Ralf Krumkamp, DrPH,
- Benedikt Ley, PhD,
- Sandra Valborg Løfberg, MD,
- Jürgen May, ProfMD,
- Christian G Meyer, MD,
- Eric D Mintz, MD,
- Joel M Montgomery, PhD,
- Aissatou Ahmet Niang, MSc,
- Chelsea Nichols, MPH,
- Beatrice Olack, MPHE,
- Gi Deok Pak, MSc,
- Ursula Panzner, MSc,
- Jin Kyung Park, PhD,
- Se Eun Park, MIS,
- Henintsoa Rabezanahary, MD,
- Raphaël Rakotozandrindrainy, MD,
- Tiana Mirana Raminosoa, PhD,
- Tsiriniaina Jean Luco Razafindrabe, PhD,
- Emmanuel Sampo, MSc,
- Heidi Schütt-Gerowitt, MD,
- Amy Gassama Sow, ProfPhD,
- Nimako Sarpong, MD,
- Hye Jin Seo, BA,
- Arvinda Sooka, MSc,
- Abdramane Bassiahi Soura, PhD,
- Adama Tall, PhD,
- Mekonnen Teferi, MSc,
- Kamala Thriemer, PhD,
- Michelle R Warren, MSc,
- Biruk Yeshitela, MSc,
- John D Clemens, ProfMD,
- Thomas F Wierzba, PhD
Affiliations
- Florian Marks, DrPhD
- International Vaccine Institute, SNU Research Park, Seoul, South Korea; Correspondence to: Dr Florian Marks, International Vaccine Institute, SNU Research Park, 1 Gwanak-ro, Gwanak-gu, Seoul 08826, South Korea
- Vera von Kalckreuth, MD
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Peter Aaby, DMSc
- Bandim Health Project, Bissau, Guinea-Bissau; Research Center for Vitamins and Vaccines, Copenhagen, Denmark
- Yaw Adu-Sarkodie, ProfPhD
- Kumasi Centre for Collaborative Research in Tropical Medicine, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana
- Muna Ahmed El Tayeb, MD
- Faculty of Medicine, University of Gezira, Wad Medani, Sudan
- Mohammad Ali, PhD
- Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
- Abraham Aseffa, PhD
- Armauer Hansen Research Institute, Addis Ababa, Ethiopia
- Stephen Baker, ProfPhD
- Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
- Holly M Biggs, MD
- Kilimanjaro Christian Medical Centre, Moshi, Tanzania; Division of Infectious Diseases and International Health, Duke University Medical Center, Durham, NC, USA
- Morten Bjerregaard-Andersen, PhD
- Bandim Health Project, Bissau, Guinea-Bissau; Research Center for Vitamins and Vaccines, Copenhagen, Denmark
- Robert F Breiman, MD
- Centers for Disease Control and Prevention, Nairobi, Kenya; Global Health Institute, Emory University, Atlanta, GA, USA
- James I Campbell, FIBMS
- Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
- Leonard Cosmas, MPH
- Centers for Disease Control and Prevention, Nairobi, Kenya; WHO-Kenya Country Office, Nairobi, Kenya
- John A Crump, ProfMD
- Kilimanjaro Christian Medical Centre, Moshi, Tanzania; Division of Infectious Diseases and International Health, Duke University Medical Center, Durham, NC, USA; Duke Global Health Institute, Duke University, Durham, NC, USA; Centre for International Health, University of Otago, Dunedin, New Zealand
- Ligia Maria Cruz Espinoza, MD
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Jessica Fung Deerin, MPH
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Denise Myriam Dekker, PhD
- Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany; German Center for Infection Research, Hamburg—Borstel—Lübeck, Germany
- Barry S Fields, PhD
- Centers for Disease Control and Prevention, Nairobi, Kenya
- Nagla Gasmelseed, ProfPhD
- Faculty of Medicine, University of Gezira, Wad Medani, Sudan; Faculty of Science, University of Hafr Al Batin, Hafr Al Batin, Saudi Arabia
- Julian T Hertz, MD
- Kilimanjaro Christian Medical Centre, Moshi, Tanzania; Division of Infectious Diseases and International Health, Duke University Medical Center, Durham, NC, USA
- Nguyen Van Minh Hoang, MSc
- Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
- Justin Im, MSc
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Anna Jaeger, BA
- Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany
- Hyon Jin Jeon, BA
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Leon Parfait Kabore, MSc
- Schiphra Hospital, Ouagadougou, Burkina Faso
- Karen H Keddy, MMed
- National Institute for Communicable Diseases, Johannesburg, South Africa; Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa
- Frank Konings, PhD
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Ralf Krumkamp, DrPH
- Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany; German Center for Infection Research, Hamburg—Borstel—Lübeck, Germany
- Benedikt Ley, PhD
- International Vaccine Institute, SNU Research Park, Seoul, South Korea; Global and Tropical Health Division, Menzies School of Health Research, Charles Darwin University, Australia
- Sandra Valborg Løfberg, MD
- Bandim Health Project, Bissau, Guinea-Bissau; Research Center for Vitamins and Vaccines, Copenhagen, Denmark
- Jürgen May, ProfMD
- Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany; German Center for Infection Research, Hamburg—Borstel—Lübeck, Germany
- Christian G Meyer, MD
- Institute of Tropical Medicine, Eberhard-Karls University Tübingen, Tübingen, Germany; Duy Tan University, Da Nang, Vietnam
- Eric D Mintz, MD
- National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, USA
- Joel M Montgomery, PhD
- Centers for Disease Control and Prevention, Nairobi, Kenya
- Aissatou Ahmet Niang, MSc
- Institute Pasteur de Dakar, Dakar, Senegal
- Chelsea Nichols, MPH
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Beatrice Olack, MPHE
- Center for Clinical Research, Kenya Medical Research Institute, Nairobi, Kenya
- Gi Deok Pak, MSc
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Ursula Panzner, MSc
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Jin Kyung Park, PhD
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Se Eun Park, MIS
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Henintsoa Rabezanahary, MD
- Laboratory of Microbiology, University of Antananarivo, Antananarivo, Madagascar
- Raphaël Rakotozandrindrainy, MD
- Laboratory of Microbiology, University of Antananarivo, Antananarivo, Madagascar
- Tiana Mirana Raminosoa, PhD
- Laboratory of Microbiology, University of Antananarivo, Antananarivo, Madagascar
- Tsiriniaina Jean Luco Razafindrabe, PhD
- Laboratory of Microbiology, University of Antananarivo, Antananarivo, Madagascar
- Emmanuel Sampo, MSc
- Schiphra Hospital, Ouagadougou, Burkina Faso
- Heidi Schütt-Gerowitt, MD
- International Vaccine Institute, SNU Research Park, Seoul, South Korea; Institute of Medical Microbiology, University of Cologne, Cologne, Germany
- Amy Gassama Sow, ProfPhD
- Institute Pasteur de Dakar, Dakar, Senegal; University Cheikh Anta Diop de Dakar, Dakar, Senegal
- Nimako Sarpong, MD
- Kumasi Centre for Collaborative Research in Tropical Medicine, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana; German Center for Infection Research, Hamburg—Borstel—Lübeck, Germany
- Hye Jin Seo, BA
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Arvinda Sooka, MSc
- National Institute for Communicable Diseases, Johannesburg, South Africa
- Abdramane Bassiahi Soura, PhD
- Institut Supérieur des Sciences de la Population, University of Ouagadougou, Ouagadougou, Burkina Faso
- Adama Tall, PhD
- Institute Pasteur de Dakar, Dakar, Senegal
- Mekonnen Teferi, MSc
- Armauer Hansen Research Institute, Addis Ababa, Ethiopia
- Kamala Thriemer, PhD
- International Vaccine Institute, SNU Research Park, Seoul, South Korea; Global and Tropical Health Division, Menzies School of Health Research, Charles Darwin University, Australia
- Michelle R Warren, MSc
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Biruk Yeshitela, MSc
- Armauer Hansen Research Institute, Addis Ababa, Ethiopia
- John D Clemens, ProfMD
- International Vaccine Institute, SNU Research Park, Seoul, South Korea; International Centre for Diarrheal Disease Research, Bangladesh, Dhaka, Bangladesh; University of California Fielding School of Public Health, Los Angeles, CA, USA
- Thomas F Wierzba, PhD
- International Vaccine Institute, SNU Research Park, Seoul, South Korea
- Journal volume & issue
-
Vol. 5,
no. 3
pp. e310 – e323
Abstract
Summary: Background: Available incidence data for invasive salmonella disease in sub-Saharan Africa are scarce. Standardised, multicountry data are required to better understand the nature and burden of disease in Africa. We aimed to measure the adjusted incidence estimates of typhoid fever and invasive non-typhoidal salmonella (iNTS) disease in sub-Saharan Africa, and the antimicrobial susceptibility profiles of the causative agents. Methods: We established a systematic, standardised surveillance of blood culture-based febrile illness in 13 African sentinel sites with previous reports of typhoid fever: Burkina Faso (two sites), Ethiopia, Ghana, Guinea-Bissau, Kenya, Madagascar (two sites), Senegal, South Africa, Sudan, and Tanzania (two sites). We used census data and health-care records to define study catchment areas and populations. Eligible participants were either inpatients or outpatients who resided within the catchment area and presented with tympanic (≥38·0°C) or axillary temperature (≥37·5°C). Inpatients with a reported history of fever for 72 h or longer were excluded. We also implemented a health-care utilisation survey in a sample of households randomly selected from each study area to investigate health-seeking behaviour in cases of self-reported fever lasting less than 3 days. Typhoid fever and iNTS disease incidences were corrected for health-care-seeking behaviour and recruitment. Findings: Between March 1, 2010, and Jan 31, 2014, 135 Salmonella enterica serotype Typhi (S Typhi) and 94 iNTS isolates were cultured from the blood of 13 431 febrile patients. Salmonella spp accounted for 33% or more of all bacterial pathogens at nine sites. The adjusted incidence rate (AIR) of S Typhi per 100 000 person-years of observation ranged from 0 (95% CI 0–0) in Sudan to 383 (274–535) at one site in Burkina Faso; the AIR of iNTS ranged from 0 in Sudan, Ethiopia, Madagascar (Isotry site), and South Africa to 237 (178–316) at the second site in Burkina Faso. The AIR of iNTS and typhoid fever in individuals younger than 15 years old was typically higher than in those aged 15 years or older. Multidrug-resistant S Typhi was isolated in Ghana, Kenya, and Tanzania (both sites combined), and multidrug-resistant iNTS was isolated in Burkina Faso (both sites combined), Ghana, Kenya, and Guinea-Bissau. Interpretation: Typhoid fever and iNTS disease are major causes of invasive bacterial febrile illness in the sampled locations, most commonly affecting children in both low and high population density settings. The development of iNTS vaccines and the introduction of S Typhi conjugate vaccines should be considered for high-incidence settings, such as those identified in this study. Funding: Bill & Melinda Gates Foundation.