CoChat
Sign Up
Cited by 198Salmonella and Campylobacter epidemiologyBacterial Infections and VaccinesPneumonia and Respiratory Infections

The burden of typhoid and paratyphoid in India: systematic review and meta-analysis

Open access
John, Jacob, Van Aart, Carola J. C., Grassly, Nicholas C.·2016·PLOS Neglected Tropical Diseases
DOI 10.1371/journal.pntd.0004616PMC PMC4833325
Open this paper in CoChat — free accountOpen PDF

Abstract

BACKGROUND: Typhoid is an important public health challenge for India, especially with the spread of antimicrobial resistance. The decision about whether to introduce a public vaccination programme needs to be based on an understanding of disease burden and the age-groups and geographic areas at risk. METHODS: We searched Medline and Web of Science databases for studies reporting the incidence or prevalence of typhoid and paratyphoid fever confirmed by culture and/or serology, conducted in India and published between 1950 and 2015. We used binomial and Poisson mixed-effects meta-regression models to estimate prevalence and incidence from hospital and community studies, and to identify risk-factors. RESULTS: We identified 791 titles and abstracts, and included 37 studies of typhoid and 18 studies of paratyphoid in the systematic review and meta-analysis. The estimated prevalence of laboratory-confirmed typhoid and paratyphoid among individuals with fever across all hospital studies was 9.7% (95% CI: 5.7-16.0%) and 0.9% (0.5-1.7%) respectively. There was significant heterogeneity among studies (p-values<0.001). Typhoid was more likely to be detected among clinically suspected cases or during outbreaks and showed a significant decline in prevalence over time (odds ratio for each yearly increase in study date was 0.96 (0.92-0.99) in the multivariate meta-regression model). Paratyphoid did not show any trend over time and there was no clear association with risk-factors. Incidence of typhoid and paratyphoid was reported in 3 and 2 community cohort studies respectively (in Kolkata and Delhi, or Kolkata alone). Pooled estimates of incidence were 377 (178-801) and 105 (74-148) per 100,000 person years respectively, with significant heterogeneity between locations for typhoid (p<0.001). Children 2-4 years old had the highest incidence. CONCLUSIONS: Typhoid remains a significant burden in India, particularly among young children, despite apparent declines in prevalence. Infant immunisation with newly-licensed conjugate vaccines could address this challenge.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pntd.0004616

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.

A few free checks a day · papers already verified open instantly · results are public

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?

  • Enteric fever imposes a significant public health burden and is a cause for concern in India, with varied geographic heterogeneity across the country.

    “Enteric fever is a condition that imposes a significant public health burden and is a cause for concern in India, with varied geographic heterogeneity across the country [12].”

    From Water, Sanitation, and Hygiene Practices in Urban Slums of Eastern India (2021) · cites this paper as [12]

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

No references could be resolved yet.

Research works printed but not linked: 31

  1. [1]Buckle GC, Walker CL, Black RE (2012) Typhoid fever and paratyphoid fever: Systematic review to estimate global morbidity and mortality for 2010. J Glob Health 2: 010401 23198130 PMC3484760
  2. [2]Mogasale V, Maskery B, Ochiai RL, Lee JS, Mogasale VV, et al (2014) Burden of typhoid fever in low-income and middle-income countries: a systematic, literature-based update with risk-factor adjustment. Lancet Global Health 2: E570– E580. 10.1016/S2214-109X(14)70301-8 25304633 · DOI
  3. [3]Wain J, Hendriksen RS, Mikoleit ML, Keddy KH, Ochiai RL (2014) Typhoid fever. The Lancet. PMC11567078 25458731
  4. [4]Crump JA, Mintz ED (2010) Global Trends in Typhoid and Paratyphoid Fever. Clinical Infectious Diseases 50: 241– 246. 10.1086/649541 20014951 PMC2798017 · DOI
  5. [5]Ochiai RL, Acosta CJ, Danovaro-Holliday MC, Baiqing D, Lhattacharya SK, et al (2008) A study of typhoid fever in five Asian countries: disease burden and implications for controls. Bulletin of the World Health Organization 86: 260– 268. 18438514 PMC2647431
  6. [6]Ochiai RL, Wang XY, von Seidlein L, Yang J, Bhutta ZA, et al (2005) Salmonella paratyphi A rates, Asia. Emerging Infectious Diseases 11: 1764– 1766. 16318734 PMC3367370
  7. [7]Sur D, Ali M, von Seidlein L, Manna B, Deen JL, et al (2007) Comparisons of predictors for typhoid and paratyphoid fever in Kolkata, India. BMC Public Health 7: 289 17935611 PMC2099435
  8. [8]Bhunia R, Hutin Y, Ramakrishnan R, Pal N, Sen T, et al (2009) A typhoid fever outbreak in a slum of South Dumdum municipality, West Bengal, India, 2007: Evidence for foodborne and waterborne transmission. Bmc Public Health 9. PMC2683821 19397806
  9. [9]Ames WR, Robins M (1943) Age and Sex as Factors in the Development of the Typhoid Carrier State, and a Method for Estimating Carrier Prevalence. American journal of public health and the nation's health 33: 221– 230. 18015749 PMC1527221
  10. [10]Pitzer VE, Bowles CC, Baker S, Kang G, Balaji V, et al (2014) Predicting the Impact of Vaccination on the Transmission Dynamics of Typhoid in South Asia: A Mathematical Modeling Study. PLoS Negl Trop Dis 8: e2642. 24416466 PMC3886927
  11. [11]Anwar E, Goldberg E, Fraser A, Acosta CJ, Paul M, et al (2014) Vaccines for preventing typhoid fever. Cochrane Database of Systematic Reviews 96. 24385413
  12. [12]Levine MM, Black RE, Ferreccio C, Germanier R (1987) Large-scale field trial of Ty21a live oral typhoid vaccine in enteric-coated capsule formulation. Lancet 1: 1049– 1052. 2883393
  13. [13]Levine MM, Ferreccio C, Abrego P, San Martin O, Ortiz E, et al (1999) Duration of efficacy of Ty21a, attenuated Salmonella typhi live oral vaccine. Vaccine 17: S22– S27. 10506405
  14. [14]Acharya IL, Lowe CU, Thapa R, Gurubacharya VL, Shrestha MB, et al (1987) Prevention of typhoid-fever in Nepal with the Vi capsular polysaccharide of Salmonella Typhi—a preliminary-report. N Engl J Med 317: 1101– 1104. 3657877
  15. [15]Klugman KP, Koornhof HJ, Robbins JB, LeCam NN (1996) Immunogenicity, efficacy and serological correlate of protection of Salmonella typhi Vi capsular polysaccharide vaccine three years after immunization. Vaccine 14: 435– 438. 8735556
  16. [16]Lin FYC, Ho VA, Khiem HB, Trach DD, Bay PV, et al (2001) The efficacy of a Salmonella typhi Vi conjugate vaccine in two-to-five-year-old children. New England Journal of Medicine 344: 1263– 1269. 11320385
  17. [17]Lanh MN, Bay PV, Ho VA, Thanh TC, Lin FYC, et al (2003) Persistent efficacy of Vi conjugate vaccine against typhoid fever in young children. New England Journal of Medicine 349: 1390– 1391. 14523155
  18. [18]Szu SC (2013) Development of Vi conjugate—a new generation of typhoid vaccine. Expert Rev Vaccines 12: 1273– 1286. 10.1586/14760584.2013.845529 24156285 · DOI
  19. [19]Thiem VD, Lin FY, Canh do G, Son NH, Anh DD, et al (2011) The Vi conjugate typhoid vaccine is safe, elicits protective levels of IgG anti-Vi, and is compatible with routine infant vaccines. Clin Vaccine Immunol 18: 730– 735. 10.1128/CVI.00532-10 21411598 PMC3122535 · DOI
  20. [20]World Health Organisation (2008) Typhoid vaccines: WHO position paper. Wkly Epidemiol Rec 83: 49– 60. 18260212
  21. [21]Vashishtha VM, Choudhury P, Kalra A, Bose A, Thacker N, et al (2014) Indian Academy of Pediatrics (IAP) Recommended Immunization Schedule for Children Aged 0 through 18-years India, 2014 and Updates on Immunization. Indian Pediatrics 51: 785– 800. 25362009
  22. [22]Clarke H, Bonin RP, Orser BA, Englesakis M, Wijeysundera DN, et al (2012) The prevention of chronic postsurgical pain using gabapentin and pregabalin: a combined systematic review and meta-analysis. Anesth Analg 115: 428– 442. 22415535
  23. [25]Viechtbauer Wolfgang (2010) Conducting meta-analyses in R with metafor package. Journal of Statistical Software 36: 1– 48.
  24. [26]Rao PS, Rajashekar V, Varghese GK, Shivananda PG (1993) Emergence of multidrug-resistant Salmonella typhi in rural southern India. Am J Trop Med Hyg 48: 108– 111. 8427378
  25. [27]Sur D, Ochiai RL, Bhattacharya SK, Ganguly NK, Ali M, et al (2009) A cluster-randomized effectiveness trial of Vi typhoid vaccine in India. N Engl J Med 361: 335– 344. 10.1056/NEJMoa0807521 19625715 · DOI
  26. [29]Sur D, Ali M, von Seidlein L, Manna B, Deen JL, et al (2007) Comparisons of predictors for typhoid and paratyphoid fever in Kolkata, India. BMC Public Health 7: 289 17935611 PMC2099435
  27. [30]Bahl R, Sinha A, Poulos C, Whittington D, Sazawal S, et al (2004) Costs of illness due to typhoid fever in an Indian urban slum community: implications for vaccination policy. J Health Popul Nutr 22: 304– 310. 15609783
  28. [31]Sinha A, Sazawal S, Kumar R, Sood S, Reddaiah VP, et al (1999) Typhoid fever in children aged less than 5 years. Lancet 354: 734– 737. 10475185
  29. [32]Bhan MK, Bahl R, Bhatnagar S (2005) Typhoid and paratyphoid fever. Lancet 366: 749– 762. 16125594
  30. [33]Levine MM, Ferreccio C, Black RE, Lagos R, San Martin O, et al (2007) Ty21a live oral typhoid vaccine and prevention of paratyphoid fever caused by Salmonella enterica Serovar Paratyphi B. Clin Infect Dis 45 Suppl 1: S24– 28. 17582564
  31. [34]Kundu R, Ganguly N, Ghosh TK, Yewale VN, Shah RC, et al (2006) IAP Task Force Report: diagnosis of enteric fever in children. Indian Pediatr 43: 875– 883. 17079830

Cited by

Sorted by citations

Authors
John, J., Van Aart, C. J. C., & Grassly, N. C.
Affiliations
  • Christian Medical College, Vellore (IN)
  • Imperial College London (GB)
Corresponding author
John, Jacob
ORCID
Venue
PLOS Neglected Tropical Diseases
Publisher
Public Library of Science (PLoS)
Published
2016-04-15
Volume
10
Issue
4
Pages
e0004616
ISSN
  • 1935-2727 (ISSN-L)
  • 1935-2735
DOI
10.1371/journal.pntd.0004616
PMC
PMC4833325
OpenAlex
W2335972457
Cited by
198
References
0
Citations by year
2026: 7 · 2025: 7 · 2024: 17 · 2023: 17 · 2022: 24 · 2021: 28 · 2020: 26 · 2019: 32 · 2018: 24 · 2017: 11 · 2016: 5
FWCI
2.74
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS neglected tropical diseases (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • Spiral (Imperial College London) (submittedVersion, other-oa)
Funders
Medical Research Council (MR/K010174/1)
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 › Medicine › Epidemiology › Pneumonia and Respiratory Infections
Keywords
typhoid fever, paratyphoid fever, disease burden, prevalence, incidence, India, risk factors, children, antimicrobial resistance, typhoid vaccination, conjugate vaccines, Kolkata, Delhi
MeSH terms
Adolescent, Adult, Age Factors, Aged, Aged, 80 and over, Child, Child, Preschool, Humans, India, Infant, Infant, Newborn, Middle Aged, Paratyphoid Fever, Typhoid Fever, Cohort Studies, Incidence, Prevalence, Topography, Medical, Young Adult

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