The global burden of non-typhoidal salmonella invasive disease: a systematic analysis for the Global Burden of Disease Study 2017
Open accessAbstract
BACKGROUND: Non-typhoidal salmonella invasive disease is a major cause of global morbidity and mortality. Malnourished children, those with recent malaria or sickle-cell anaemia, and adults with HIV infection are at particularly high risk of disease. We sought to estimate the burden of disease attributable to non-typhoidal salmonella invasive disease for the Global Burden of Diseases, Injuries, and Risk Factors Study (GBD) 2017. METHODS: We did a systematic review of scientific databases and grey literature, and estimated non-typhoidal salmonella invasive disease incidence and mortality for the years 1990 to 2017, by age, sex, and geographical location using DisMod-MR, a Bayesian meta-regression tool. We estimated case fatality by age, HIV status, and sociodemographic development. We also calculated the HIV-attributable fraction and estimated health gap metrics, including disability-adjusted life-years (DALYs). FINDINGS: We estimated that 535 000 (95% uncertainty interval 409 000-705 000) cases of non-typhoidal salmonella invasive disease occurred in 2017, with the highest incidence in sub-Saharan Africa (34·5 [26·6-45·0] cases per 100 000 person-years) and in children younger than 5 years (34·3 [23·2-54·7] cases per 100 000 person-years). 77 500 (46 400-123 000) deaths were estimated in 2017, of which 18 400 (12 000-27 700) were attributable to HIV. The remaining 59 100 (33 300-98 100) deaths not attributable to HIV accounted for 4·26 million (2·38-7·38) DALYs in 2017. Mean all-age case fatality was 14·5% (9·2-21·1), with higher estimates among children younger than 5 years (13·5% [8·4-19·8]) and elderly people (51·2% [30·2-72·9] among those aged ≥70 years), people with HIV infection (41·8% [30·0-54·0]), and in areas of low sociodemographic development (eg, 15·8% [10·0-22·9] in sub-Saharan Africa). INTERPRETATION: We present the first global estimates of non-typhoidal salmonella invasive disease that have been produced as part of GBD 2017. Given the high disease burden, particularly in children, elderly people, and people with HIV infection, investigating the sources and transmission pathways of non-typhoidal salmonella invasive disease is crucial to implement effective preventive and control measures. FUNDING: Bill & Melinda Gates Foundation.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Invasive non-typhoidal Salmonella accounts for 534,600 (409,000-705,000) cases and 77,470 (46,360-122,800) deaths annually worldwide; out of these, 421,600 (316,000-574,100) cases (26.2% attributed to HIV infection) and 66,520 deaths occur in sub-Saharan Africa.
“iNTS accounts for 534,600 (409,000-705,000) cases and 77,470 (46,360-122,800) deaths annually worldwide; out of these, 421,600 (316,000-574,100) cases (26.2% attributed to HIV infection) and 66,520 deaths occur in SSA.87”
From Antimicrobial Resistance Rates and Surveillance in Sub-Saharan Africa: Where Are We Now? (2022) · cites this paper as [87]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Roth, G. A., Abate, D., Abate, K. H., Abay, S. M., Abbafati, C., Abbasi, N., Abbastabar, H., Abd-Allah, F., Abdela, J., Abdelalim, A., et al. (2018) · The Lancet · doi:10.1016/s0140-6736(18)32203-7 · Cited by 8,600 · see citing works
Self-citationKirk, M. D., Pires, S. M., Black, R. E., Caipo, M., Crump, J. A., Devleesschauwer, B., Döpfer, D., Fazil, A., Fischer-Walker, C. L., Hald, T., et al. (2015) · PLoS Medicine · doi:10.1371/journal.pmed.1001921 · Cited by 1,625 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 22
- [2]GBD 2017 DALYs and HALE Collaborators Global, regional, and national disability-adjusted life-years (DALYs) for 359 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017 Lancet 392 2018 1859 1922 30415748 PMC6252083
- [3]GBD 2017 Disease and Injury Incidence and Prevalence Collaborators Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017 Lancet 392 2018 1789 1858 30496104 PMC6227754
- [4]Crump JA Sjolund-Karlsson M Gordon MA Parry CM Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections Clin Microbiol Rev 28 2015 901 937 26180063 PMC4503790
- [5]Ao TT Feasey NA Gordon MA Keddy KH Angulo FJ Crump JA Global burden of invasive nontyphoidal Salmonella disease, 2010 Emerg Infect Dis 21 2015 941 949 PMC4451910 25860298
- [6]Feasey NA Dougan G Kingsley RA Heyderman RS Gordon MA Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa Lancet 379 2012 2489 2499 22587967 PMC3402672
- [7]Graham SM Walsh AL Molyneux EM Phiri AJ Molyneux ME Clinical presentation of non-typhoidal salmonella bacteraemia in Malawian children Trans R Soc Trop Med Hyg 94 2000 310 314 10975008
- [8]Keddy KH Musekiwa A Sooka A Clinical and microbiological features of invasive nontyphoidal Salmonella associated with HIV-infected patients, Gauteng Province, South Africa Medicine 96 2017 e6448 28353576 PMC5380260
- [9]Park SE Pak GD Aaby P The relationship between invasive nontyphoidal Salmonella disease, other bacterial bloodstream infections, and malaria in Sub-Saharan Africa Clin Infect Dis 62 suppl 1 2016 S23 S31 26933016 PMC4772835
- [10]Vugia DJ Samuel M Farley MM Invasive Salmonella infections in the United States, FoodNet, 1996–1999: incidence, serotype distribution, and outcome Clin Infect Dis 38 suppl 3 2004 S149 S156 15095184
- [11]Akullian A Montgomery JM John-Stewart G Multi-drug resistant non-typhoidal Salmonella associated with invasive disease in western Kenya PLoS Negl Trop Dis 12 2018 e0006156 29329299 PMC5785031
- [12]Kingsley RA Msefula CL Thomson NR Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype Genome Res 19 2009 2279 2287 19901036 PMC2792184
- [13]Tapia MD Tennant SM Bornstein K Invasive nontyphoidal Salmonella infections among children in Mali, 2002–2014: microbiological and epidemiologic features guide vaccine development Clin Infect Dis 61 suppl 4 2015 S332 S338 26449949 PMC4596934
- [14]Mather AE Phuong TLT Gao Y New variant of multidrug-resistant Salmonella enterica serovar Typhimurium associated with invasive disease in immunocompromised patients in Vietnam MBio 9 2018 e01056 e01118 30181247 PMC6123440
- [15]Parisi A Crump JA Glass K Health outcomes from multidrug-resistant Salmonella infections in high-income countries: a systematic review and meta-analysis Foodborne Pathog Dis 15 2018 428 436 29624414
- [16]Jones TF Ingram LA Cieslak PR Salmonellosis outcomes differ substantially by serotype J Infect Dis 198 2008 109 114 18462137
- [17]Weinberger M Solnik-Isaac H Shachar D Salmonella enterica serotype Virchow: epidemiology, resistance patterns and molecular characterisation of an invasive Salmonella serotype in Israel Clin Microbiol Infect 12 2006 999 1005 16961637
- [19]GBD 2017 Risk Factor Collaborators Global, regional, and national comparative risk assessment of 84 behavioural, environmental and occupational, and metabolic risks or clusters of risks for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017 Lancet 392 2018 1923 1994 30496105 PMC6227755
- [20]Weiss DJ Lucas TCD Nguyen M Mapping the global prevalence, incidence, and mortality of Plasmodium falciparum, 2000-17: a spatial and temporal modelling study Lancet 394 2019 322 331 31229234 PMC6675740
- [21]GBD 2017 Typhoid and Paratyphoid Collaborators The global burden of typhoid and paratyphoid fevers: a systematic analysis for the Global Burden of Disease Study 2017 Lancet Infect Dis 19 2019 369 381 30792131 PMC6437314
- [23]Keddy KH Takuva S Musekiwa A An association between decreasing incidence of invasive non-typhoidal salmonellosis and increased use of antiretroviral therapy, Gauteng Province, South Africa, 2003–2013 PLoS One 12 2017 e0173091 28264046 PMC5338796
- [24]Feasey NA Houston A Mukaka M A Reduction in adult blood stream infection and case fatality at a large African hospital following antiretroviral therapy roll-out PLoS One 9 2014 e92226 24643091 PMC3958486
- [25]Mayanja BN Todd J Hughes P Septicaemia in a population-based HIV clinical cohort in rural Uganda, 1996–2007: incidence, aetiology, antimicrobial drug resistance and impact of antiretroviral therapy: septicaemia in a rural Ugandan HIV cohort Trop Med Int Health 15 2010 697 705 20406428
Cited by
Sorted by citations
Salmonella, food safety and food handling practices
Ehuwa, O., Jaiswal, A. K., & Jaiswal, S. (2021) · Foods · doi:10.3390/foods10050907 · Cited by 551 · see citing works
Antimicrobial Resistance Rates and Surveillance in Sub-Saharan Africa: Where Are We Now?
Kariuki, S., Kering, K., Wairimu, C., Onsare, R., & Mbae, C. (2022) · Infection and Drug Resistance · doi:10.2147/idr.s342753 · Cited by 231 · see citing works
Stepwise evolution of Salmonella Typhimurium ST313 causing bloodstream infection in Africa
Pulford, C. V., Perez-Sepulveda, B. M., Canals, R., Bevington, J. A., Bengtsson, R. J., Wenner, N., Rodwell, E. V., Kumwenda, B., Zhu, X., Bennett, R. J., et al. (2020) · Nature Microbiology · doi:10.1038/s41564-020-00836-1 · Cited by 151 · see citing works
- Authors
- Stanaway, J. D., Parisi, A., Sarkar, K., Blacker, B. F., Reiner, R. C., Hay, S. I., Nixon, M. R., Dolecek, C., James, S. L., Mokdad, A. H., Abebe, G., Ahmadian, E., Alahdab, F., Alemnew, B. T. T., Alipour, V., Allah Bakeshei, F., Animut, M. D., Ansari, F., Arabloo, J., Asfaw, E. T., Bagherzadeh, M., Bassat, Q., Belayneh, Y. M. M., Carvalho, F., Daryani, A., Demeke, F. M., Demis, A. B. B., Dubey, M., Duken, E. E., Dunachie, S. J., Eftekhari, A., Fernandes, E., Fouladi Fard, R., Gedefaw, G. A., Geta, B., Gibney, K. B., Hasanzadeh, A., Hoang, C. L., Kasaeian, A., Khater, A., Kidanemariam, Z. T., Lakew, A. M., Malekzadeh, R., Melese, A., Mengistu, D. T., Mestrovic, T., Miazgowski, B., Mohammad, K. A., Mohammadian, M., Mohammadian-Hafshejani, A., Nguyen, C. T., Nguyen, L. H., Nguyen, S. H., Nirayo, Y. L., Olagunju, A. T., Olagunju, T. O., Pourjafar, H., Qorbani, M., Rabiee, M., Rabiee, N., Rafay, A., Rezapour, A., Samy, A. M., Sepanlou, S. G., Shaikh, M. A., Sharif, M., Shigematsu, M., Tessema, B., Tran, B. X., Ullah, I., Yimer, E. M., Zaidi, Z., Murray, C. J. L., & Crump, J. A.
- Affiliations
- University of Washington (US)
- ORCID
- Stanaway, Jeffrey D.
- Parisi, Andrea
- Sarkar, Kaushik
- Blacker, Brigette F.
- Reiner, Robert C
- Hay, Simon I.
- Dolecek, Christiane
- James, Spencer L.
- Mokdad, Ali H
- Ahmadian, Elham
- Alahdab, Fares
- Alemnew, Birhan Tamene T
- Animut, Megbaru Debalkie
- Ansari, Fereshteh
- Arabloo, Jalal
- Bagherzadeh, Mojtaba
- Bassat, Quique
- Belayneh, Yaschilal Muche Muche
- Carvalho, Félix
- Daryani, Ahmad
- Demeke, Feleke Mekonnen
- Demis, Asmamaw Bizuneh Bizuneh
- Dubey, Manisha
- Dunachie, Susanna J
- Eftekhari, Aziz
- Fernandes, Eduarda
- Gedefaw, Getnet Azeze
- Gibney, Katherine B
- Hasanzadeh, Amir
- Hoang, Chi Linh
- Kasaeian, Amir
- Lakew, Ayenew Molla
- Malekzadeh, Reza
- Melese, Addisu
- Mengistu, Desalegn Tadese
- Miazgowski, Bartosz
- Mohammad, Karzan Abdulmuhsin
- Mohammadian, Mahdi
- Mohammadian-Hafshejani, Abdollah
- Nguyen, Cuong Tat
- Nguyen, Long Hoang
- Nguyen, Son Hoang
- Olagunju, Andrew T
- Olagunju, Tinuke O
- Pourjafar, Hadi
- Qorbani, Mostafa
- Rabiee, Mohammad
- Rabiee, Navid
- Samy, Abdallah M.
- Sepanlou, Sadaf G.
- Shaikh, Masood Ali
- Sharif, Mehdi
- Tessema, Belay
- Tran, Bach Xuan
- Ullah, Irfan
- Yimer, Ebrahim M
- Zaidi, Zoubida
- Murray, Christopher J L
- Crump, John A
- Venue
- The Lancet Infectious Diseases
- Publisher
- Elsevier BV
- Published
- 2019-12
- Volume
- 19
- Issue
- 12
- Pages
- 1312-1324
- ISSN
- 1473-3099 (ISSN-L)
- PMC
- PMC6892270
- OpenAlex
- W2975535544
- Cited by
- 645
- References
- 2
- Citations by year
- 2026: 87 · 2025: 117 · 2024: 96 · 2023: 117 · 2022: 86 · 2021: 91 · 2020: 49 · 2019: 2
- FWCI
- 43.99
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The Lancet Infectious Diseases (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (publishedVersion, cc-by)
- ANU Open Research (Australian National University) (submittedVersion, cc-by)
- RECERCAT (Consorci de Serveis Universitaris de Catalunya) (submittedVersion, cc-by)
- Funders
- Bill and Melinda Gates Foundation (OPP1132415)
- National Health and Medical Research Council
- Fundação para a Ciência e a Tecnologia
- Ministério da Ciência, Tecnologia e Ensino Superior
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
- Life Sciences › Immunology and Microbiology › Microbiology › Bacterial Infections and Vaccines
- Health Sciences › Health Professions › Health Information Management › Global Health and Epidemiology
- Keywords
- non-typhoidal Salmonella, invasive Salmonella disease, global burden of disease, incidence and mortality, case fatality, disability-adjusted life years, malaria, sickle cell disease, children under five, sub-Saharan Africa, HIV infection, Global Burden of Disease Study 2017, risk factors
- MeSH terms
- Global Burden of Disease, Female, Humans, Male, Risk Factors, Salmonella, Salmonella Infections, Socioeconomic Factors, Incidence, Prevalence, Geography, Medical
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review