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Abstract

Background

is a leading global cause of bacterial gastroenteritis, motivating research to identify sources of human infection. Population genetic studies have been increasingly applied to this end, mainly using multilocus sequence typing (MLST) data.

Objectives

This review aimed to summarise approaches and findings of these studies and identify best practice lessons for this form of genomic epidemiology.

Methods

We systematically reviewed publications using MLST data to attribute human disease isolates to source. Publications were from January 2001, when this type of approach began. Searched databases included Scopus, Web of Science and PubMed. Information on samples and isolate datasets used, as well as MLST schemes and attribution algorithms employed, was obtained. Main findings were extracted, as well as any results’ validation with subsequent correction for identified biases. Meta-analysis is not reported given high levels of heterogeneity.

Results

Of 2,109 studies retrieved worldwide, 25 were included, and poultry, specifically chickens, were identified as principal source of human infection. Ruminants (cattle or sheep) were consistently implicated in a substantial proportion of cases. Data sampling and analytical approaches varied, with five different attribution algorithms used. Validation such as self-attribution of isolates from known sources was reported in five publications. No publication reported adjustment for biases identified by validation.

Conclusions

Common gaps in validation and adjustment highlight opportunities to generate improved estimates in future genomic attribution studies. The consistency of chicken as the main source of human infection, across high income countries, and despite methodological variations, highlights the public health importance of this source.

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2019-10-24
2025-05-23
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References

  1. European Food Safety Authority (EFSA). The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2017. EFSA J. 2018;16(12):5500.  https://doi.org/10.2903/j.efsa.2018.5500 
  2. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne illness acquired in the United States--major pathogens. Emerg Infect Dis. 2011;17(1):7-15.  https://doi.org/10.3201/eid1701.P11101  PMID: 21192848 
  3. Amour C, Gratz J, Mduma E, Svensen E, Rogawski ET, McGrath M, et al. . Epidemiology and Impact of Campylobacter Infection in Children in 8 Low-Resource Settings: Results From the MAL-ED Study. Clin Infect Dis. 2016;63(9):1171-9.  https://doi.org/10.1093/cid/ciw542  PMID: 27501842 
  4. Friesema IH, Havelaar AH, Westra PP, Wagenaar JA, van Pelt W. Poultry culling and Campylobacteriosis reduction among humans, the Netherlands. Emerg Infect Dis. 2012;18(3):466-8.  https://doi.org/10.3201/eid1803.111024  PMID: 22377498 
  5. Stern NJ, Hiett KL, Alfredsson GA, Kristinsson KG, Reiersen J, Hardardottir H, et al. Campylobacter spp. in Icelandic poultry operations and human disease. Epidemiol Infect. 2003;130(1):23-32.  https://doi.org/10.1017/S0950268802007914  PMID: 12613742 
  6. Vellinga A, Van Loock F. The dioxin crisis as experiment to determine poultry-related Campylobacter enteritis. Emerg Infect Dis. 2002;8(1):19-22.  https://doi.org/10.3201/eid0801.010129  PMID: 11749743 
  7. Dingle KE, Colles FM, Falush D, Maiden MC. Sequence typing and comparison of population biology of Campylobacter coli and Campylobacter jejuni. J Clin Microbiol. 2005;43(1):340-7.  https://doi.org/10.1128/JCM.43.1.340-347.2005  PMID: 15634992 
  8. Dingle KE, Colles FM, Wareing DRA, Ure R, Fox AJ, Bolton FE, et al. Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol. 2001;39(1):14-23.  https://doi.org/10.1128/JCM.39.1.14-23.2001  PMID: 11136741 
  9. Ikram R, Chambers S, Mitchell P, Brieseman MA, Ikam OH. A case control study to determine risk factors for Campylobacter infection in Christchurch in the summer of 1992-3. N Z Med J. 1994;107(988):430-2. PMID: 7970341 
  10. Domingues AR, Pires SM, Halasa T, Hald T. Source attribution of human campylobacteriosis using a meta-analysis of case-control studies of sporadic infections. Epidemiol Infect. 2012;140(6):970-81.  https://doi.org/10.1017/S0950268811002676  PMID: 22214729 
  11. Dingle KE, Colles FM, Ure R, Wagenaar JA, Duim B, Bolton FJ, et al. Molecular characterization of Campylobacter jejuni clones: a basis for epidemiologic investigation. Emerg Infect Dis. 2002;8(9):949-55.  https://doi.org/10.3201/eid0809.02-0122  PMID: 12194772 
  12. Sheppard SK, Dallas JF, MacRae M, McCarthy ND, Sproston EL, Gormley FJ, et al. Campylobacter genotypes from food animals, environmental sources and clinical disease in Scotland 2005/6. Int J Food Microbiol. 2009;134(1-2):96-103.  https://doi.org/10.1016/j.ijfoodmicro.2009.02.010  PMID: 19269051 
  13. Mullner P, Spencer SE, Wilson DJ, Jones G, Noble AD, Midwinter AC, et al. Assigning the source of human campylobacteriosis in New Zealand: a comparative genetic and epidemiological approach. Infect Genet Evol. 2009;9(6):1311-9.  https://doi.org/10.1016/j.meegid.2009.09.003  PMID: 19778636 
  14. Boysen L, Rosenquist H, Larsson JT, Nielsen EM, Sørensen G, Nordentoft S, et al. Source attribution of human campylobacteriosis in Denmark. Epidemiol Infect. 2014;142(8):1599-608.  https://doi.org/10.1017/S0950268813002719  PMID: 24168860 
  15. McCarthy ND, Colles FM, Dingle KE, Bagnall MC, Manning G, Maiden MC, et al. Host-associated genetic import in Campylobacter jejuni. Emerg Infect Dis. 2007;13(2):267-72.  https://doi.org/10.3201/eid1302.060620  PMID: 17479890 
  16. Mullner P, Jones G, Noble A, Spencer SE, Hathaway S, French NP. Source attribution of food-borne zoonoses in New Zealand: a modified Hald model. Risk Anal. 2009;29(7):970-84.  https://doi.org/10.1111/j.1539-6924.2009.01224.x  PMID: 19486473 
  17. Wilson DJ, Gabriel E, Leatherbarrow AJH, Cheesbrough J, Gee S, Bolton E, et al. Tracing the source of campylobacteriosis. PLoS Genet. 2008;4(9):e1000203.  https://doi.org/10.1371/journal.pgen.1000203  PMID: 18818764 
  18. mlstdbNet Home Page. Available at: http://pubmlst.org/software/database/mlstdbnet/
  19. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155(2):945-59. PMID: 10835412 
  20. Sheppard SK, Colles F, Richardson J, Cody AJ, Elson R, Lawson A, et al. Host association of Campylobacter genotypes transcends geographic variation. Appl Environ Microbiol. 2010;76(15):5269-77.  https://doi.org/10.1128/AEM.00124-10  PMID: 20525862 
  21. Bessell PR, Rotariu O, Innocent GT, Smith-Palmer A, Strachan NJ, Forbes KJ, et al. Using sequence data to identify alternative routes and risk of infection: a case-study of Campylobacter in Scotland. BMC Infect Dis. 2012;12(1):80.  https://doi.org/10.1186/1471-2334-12-80  PMID: 22462563 
  22. Cody AJ, McCarthy ND, Bray JE, Wimalarathna HM, Colles FM, Jansen van Rensburg MJ, et al. Wild bird-associated Campylobacter jejuni isolates are a consistent source of human disease, in Oxfordshire, United Kingdom. Environ Microbiol Rep. 2015;7(5):782-8.  https://doi.org/10.1111/1758-2229.12314  PMID: 26109474 
  23. Di Giannatale E, Garofolo G, Alessiani A, Di Donato G, Candeloro L, Vencia W, et al. Tracing Back Clinical Campylobacter jejuni in the Northwest of Italy and Assessing Their Potential Source. Front Microbiol. 2016;7:887.  https://doi.org/10.3389/fmicb.2016.00887  PMID: 27379033 
  24. French NP. Enhancing Surveillance of Potentially Foodborne Enteric Diseases in New Zealand: Human Campylobacteriosis in the Manawatu. Final report: FDI / 236/2005 2008. [Accessed 19 Nov 2018]. Available from: https://www.foodsafety.govt.nz/elibrary/industry/enhancing-surveillance-potentially-research-projects-2/Campy_Attribution_Manawatu.pdf
  25. Jonas R, Kittl S, Overesch G, Kuhnert P. Genotypes and antibiotic resistance of bovine Campylobacter and their contribution to human campylobacteriosis. Epidemiol Infect. 2015;143(11):2373-80.  https://doi.org/10.1017/S0950268814003410  PMID: 25511436 
  26. Kittl S, Heckel G, Korczak BM, Kuhnert P. Source attribution of human Campylobacter isolates by MLST and fla-typing and association of genotypes with quinolone resistance. PLoS One. 2013;8(11):e81796.  https://doi.org/10.1371/journal.pone.0081796  PMID: 24244747 
  27. Kovac J, Stessl B, Čadež N, Gruntar I, Cimerman M, Stingl K, et al. Population structure and attribution of human clinical Campylobacter jejuni isolates from central Europe to livestock and environmental sources. Zoonoses Public Health. 2018;65(1):51-8.  https://doi.org/10.1111/zph.12366  PMID: 28755449 
  28. Lévesque S, Fournier E, Carrier N, Frost E, Arbeit RD, Michaud S. Campylobacteriosis in urban versus rural areas: a case-case study integrated with molecular typing to validate risk factors and to attribute sources of infection. PLoS One. 2013;8(12):e83731.  https://doi.org/10.1371/journal.pone.0083731  PMID: 24386265 
  29. Mossong J, Mughini-Gras L, Penny C, Devaux A, Olinger C, Losch S, et al. Human Campylobacteriosis in Luxembourg, 2010-2013: A Case-Control Study Combined with Multilocus Sequence Typing for Source Attribution and Risk Factor Analysis. Sci Rep. 2016;6(1):20939.  https://doi.org/10.1038/srep20939  PMID: 26860258 
  30. Mughini Gras L, Smid JH, Wagenaar JA, de Boer AG, Havelaar AH, Friesema IH, et al. Risk factors for campylobacteriosis of chicken, ruminant, and environmental origin: a combined case-control and source attribution analysis. PLoS One. 2012;7(8):e42599.  https://doi.org/10.1371/journal.pone.0042599  PMID: 22880049 
  31. Mughini Gras L, Smid JH, Wagenaar JA, Koene MG, Havelaar AH, Friesema IH, et al. Increased risk for Campylobacter jejuni and C. coli infection of pet origin in dog owners and evidence for genetic association between strains causing infection in humans and their pets. Epidemiol Infect. 2013;141(12):2526-35.  https://doi.org/10.1017/S0950268813000356  PMID: 23445833 
  32. Nohra A, Grinberg A, Midwinter AC, Marshall JC, Collins-Emerson JM, French NP. Molecular Epidemiology of Campylobacter coli Strains Isolated from Different Sources in New Zealand between 2005 and 2014. Appl Environ Microbiol. 2016;82(14):4363-70.  https://doi.org/10.1128/AEM.00934-16  PMID: 27208097 
  33. Rosner BM, Schielke A, Didelot X, Kops F, Breidenbach J, Willrich N, et al. A combined case-control and molecular source attribution study of human Campylobacter infections in Germany, 2011-2014. Sci Rep. 2017;7(1):5139.  https://doi.org/10.1038/s41598-017-05227-x  PMID: 28698561 
  34. Roux F, Sproston E, Rotariu O, Macrae M, Sheppard SK, Bessell P, et al. Elucidating the aetiology of human Campylobacter coli infections. PLoS One. 2013;8(5):e64504.  https://doi.org/10.1371/journal.pone.0064504  PMID: 23734204 
  35. Sears A, Baker MG, Wilson N, Marshall J, Muellner P, Campbell DM, et al. Marked campylobacteriosis decline after interventions aimed at poultry, New Zealand. Emerg Infect Dis. 2011;17(6):1007-15.  https://doi.org/10.3201/eid/1706.101272  PMID: 21749761 
  36. Sheppard SK, Dallas JF, Strachan NJ, MacRae M, McCarthy ND, Wilson DJ, et al. Campylobacter genotyping to determine the source of human infection. Clin Infect Dis. 2009;48(8):1072-8.  https://doi.org/10.1086/597402  PMID: 19275496 
  37. Sheppard SK, Dallas JF, Wilson DJ, Strachan NJ, McCarthy ND, Jolley KA, et al. Evolution of an agriculture-associated disease causing Campylobacter coli clade: evidence from national surveillance data in Scotland. PLoS One. 2010;5(12):e15708.  https://doi.org/10.1371/journal.pone.0015708  PMID: 21179537 
  38. Smid JH, Mughini Gras L, de Boer AG, French NP, Havelaar AH, Wagenaar JA, et al. Practicalities of using non-local or non-recent multilocus sequence typing data for source attribution in space and time of human campylobacteriosis. PLoS One. 2013;8(2):e55029.  https://doi.org/10.1371/journal.pone.0055029  PMID: 23405107 
  39. Strachan NJ, Gormley FJ, Rotariu O, Ogden ID, Miller G, Dunn GM, et al. Attribution of Campylobacter infections in northeast Scotland to specific sources by use of multilocus sequence typing. J Infect Dis. 2009;199(8):1205-8.  https://doi.org/10.1086/597417  PMID: 19265482 
  40. Strachan NJ, Rotariu O, MacRae M, Sheppard SK, Smith-Palmer A, Cowden J, et al. Operationalising factors that explain the emergence of infectious diseases: a case study of the human campylobacteriosis epidemic. PLoS One. 2013;8(11):e79331.  https://doi.org/10.1371/journal.pone.0079331  PMID: 24278127 
  41. Thépault A, Méric G, Rivoal K, Pascoe B, Mageiros L, Touzain F, et al. Genome-Wide Identification of Host-Segregating Epidemiological Markers for Source Attribution in Campylobacter jejuni. Appl Environ Microbiol. 2017;83(7):e03085-16.  https://doi.org/10.1128/AEM.03085-16  PMID: 28115376 
  42. Strachan NJ, Rotariu O, Smith-Palmer A, Cowden J, Sheppard SK, O’Brien SJ, et al. Identifying the seasonal origins of human campylobacteriosis. Epidemiol Infect. 2013;141(6):1267-75.  https://doi.org/10.1017/S0950268812002063  PMID: 22989449 
  43. French NP, Midwinter A, Holland B, Collins-Emerson J, Pattison R, Colles F, et al. Molecular epidemiology of Campylobacter jejuni isolates from wild-bird fecal material in children’s playgrounds. Appl Environ Microbiol. 2009;75(3):779-83.  https://doi.org/10.1128/AEM.01979-08  PMID: 19047378 
  44. Van Pelt W, Van De Giessen AW, Van Leeuwen WJ, et al. Oorsprung, omvang en kosten van humane salmonellose. Deel 1. Oorsprung van human salmonellose met betrekking tot varken, rund, kip, ei en overige bronnen. Infectiezikten Bulletin. 1999:240-3.
  45. Hald T, Vose D, Wegener HC, Koupeev T. A Bayesian approach to quantify the contribution of animal-food sources to human salmonellosis. Risk Anal. 2004;24(1):255-69.  https://doi.org/10.1111/j.0272-4332.2004.00427.x  PMID: 15028016 
  46. Bessell PR, Rotariu O, Innocent GT, Smith-Palmer A, Strachan NJ, Forbes KJ, et al. Using sequence data to identify alternative routes and risk of infection: a case-study of Campylobacter in Scotland. BMC Infect Dis. 2012;12(1):80.  https://doi.org/10.1186/1471-2334-12-80  PMID: 22462563 
  47. Griekspoor P, Colles FM, McCarthy ND, Hansbro PM, Ashhurst-Smith C, Olsen B, et al. Marked host specificity and lack of phylogeographic population structure of Campylobacter jejuni in wild birds. Mol Ecol. 2013;22(5):1463-72.  https://doi.org/10.1111/mec.12144  PMID: 23356487 
  48. Clark CG, Price L, Ahmed R, Woodward DL, Melito PL, Rodgers FG, et al. Characterization of waterborne outbreak-associated Campylobacter jejuni, Walkerton, Ontario. Emerg Infect Dis. 2003;9(10):1232-41.  https://doi.org/10.3201/eid0910.020584  PMID: 14609457 
  49. Kovac J, Stessl B, Čadež N, Gruntar I, Cimerman M, Stingl K, et al. Population structure and attribution of human clinical Campylobacter jejuni isolates from central Europe to livestock and environmental sources. Zoonoses Public Health. 2018;65(1):51-8. https://doi.org/10.1111/zph.12366  PMID: 28755449 
  50. Mossong J, Mughini-Gras L, Penny C, Devaux A, Olinger C, Losch S, et al. Human Campylobacteriosis in Luxembourg, 2010-2013: A Case-Control Study Combined with Multilocus Sequence Typing for Source Attribution and Risk Factor Analysis. Sci Rep. 2016;6(1):20939.  https://doi.org/10.1038/srep20939  PMID: 26860258 
  51. Yahara K, Méric G, Taylor AJ, de Vries SP, Murray S, Pascoe B, et al. Genome-wide association of functional traits linked with Campylobacter jejuni survival from farm to fork. Environ Microbiol. 2017;19(1):361-80.  https://doi.org/10.1111/1462-2920.13628  PMID: 27883255 
  52. Ogden ID, Dallas JF, MacRae M, Rotariu O, Reay KW, Leitch M, et al. Campylobacter excreted into the environment by animal sources: prevalence, concentration shed, and host association. Foodborne Pathog Dis. 2009;6(10):1161-70.  https://doi.org/10.1089/fpd.2009.0327  PMID: 19839759 
  53. Maiden MCJ, Jansen van Rensburg MJ, Bray JE, Earle SG, Ford SA, Jolley KA, et al. MLST revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol. 2013;11(10):728-36.  https://doi.org/10.1038/nrmicro3093  PMID: 23979428 
  54. Food Standards Agency. Employing Source Attribution and Molecular Epidemiology to measure the impact of interventions on human campylobacteriosis in Scotland. Final Report. 2018. [Accessed 19 Nov 2018]. Available from: https://www.foodstandards.gov.scot/downloads/Campylobacter_Attribution_Extension_-_University_of_Aberdeen_-_FSS00017_-_iCaMPS_Report_-_FINAL_-_13th_Dec_2017.pdf
A systematic review of source attribution of human campylobacteriosis using multilocus sequence typing
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Alison+J+Cody&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cody Alison J</a>, <a href="/search?value1=Martin+CJ+Maiden&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Maiden Martin CJ</a>, <a href="/search?value1=Norval+JC+Strachan&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Strachan Norval JC</a>, <a href="/search?value1=Noel+D+McCarthy&option1=author&noRedirect=true" class="nonDisambigAuthorLink">McCarthy Noel D</a></span>. A systematic review of source attribution of human campylobacteriosis using multilocus sequence typing. <a href="/content/ecdc">Euro Surveill.</a> 2019;24(43):pii=1800696. <a href="https://doi.org/10.2807/1560-7917.ES.2019.24.43.1800696" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2019.24.43.1800696</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 19 Dec 2018;&nbsp;&nbsp; <span class="generated">Accepted</span>: 07 Jun 2019 </span> </p>
/content/10.2807/1560-7917.ES.2019.24.43.1800696
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