Source attribution of human campylobacteriosis using a meta-analysis of case-control studies of sporadic infections
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SUMMARY: Campylobacter spp. is a widespread and important cause of human illness worldwide. Disease is frequently associated with foodborne transmission, but other routes of exposure, such as direct contact with live animals and person-to-person transmission, are also recognized. Identifying the most important sources of human disease is essential for prioritizing food safety interventions and setting public health goals. Numerous case-control studies of sporadic infections of campylobacteriosis have been published. These studies investigated a variety of potential risk factors for disease, often using different methodologies and settings. Systematic reviews (SRs) consist of a formal process for literature review focused on a specific research question, and include the identification of relevant literature, quality assessment of relevant studies, summarization or statistical analysis of data, and conclusions. With the objective of identifying the most important risk factors for human sporadic campylobacteriosis, we performed a SR of case-control studies of human sporadic cases and a meta-analysis of the obtained results. A combined SR focusing on Salmonella and Campylobacter studies was performed and the results analysed separately. From 1295 identified references, 131 passed the relevance screening, 73 passed the quality assessment stage, and data was extracted from 72 studies. Of these, 38 focused on campylobacteriosis. Information on exposures of cases and controls, and estimated odds ratios for investigated risk factors were collected and analysed. In the meta-analysis, heterogeneity between the studies and possible sources of bias were investigated, and pooled odds ratios for identified risk factors were estimated. Results suggest that travelling abroad, eating undercooked chicken, environmental sources, and direct contact with farm animals were significant risk factors for campylobacteriosis. Sub-analyses by geographical region, age group, and study period were performed, and differences were discussed.
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Contact with pets has been identified as a route or risk factor for human salmonellosis in several case reports and studies.
“However, contact with pets has also been identified as a route or a risk factor for human salmonellosis in several case reports and studies (Finley et al. 2006, Domingues et al. 2012, Freeman et al. 2013), indicating that pets which have consumed Salmonella‐contaminated feed also pose an infection risk to owners.”
From Raw diets for dogs and cats: a review, with particular reference to microbiological hazards. (2019) · cites this paper as Domingues et al. 2012
The Discussion identifies pets as an important source of exposure, and the Fig. 4 caption describes studies of pet contact as a risk factor for human campylobacteriosis (page unavailable). The cited paper does not establish pet contact as a risk factor for salmonellosis or link that risk to Salmonella-contaminated feed. (LLM, conf=0.87)
Experimental — accuracy not yet measuredPets that have consumed Salmonella-contaminated feed pose an infection risk to owners.
“However, contact with pets has also been identified as a route or a risk factor for human salmonellosis in several case reports and studies (Finley et al. 2006, Domingues et al. 2012, Freeman et al. 2013), indicating that pets which have consumed Salmonella‐contaminated feed also pose an infection risk to owners.”
From Raw diets for dogs and cats: a review, with particular reference to microbiological hazards. (2019) · cites this paper as Domingues et al. 2012
The Discussion identifies direct contact with pets as a source of exposure, and its Figure 4 caption concerns the risk of human campylobacteriosis after pet contact. It does not establish a risk of salmonellosis from pets that consumed Salmonella-contaminated feed. No page number is available in our copy. (LLM, conf=0.86)
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Cites
A Nonparametric “Trim and Fill” Method of Accounting for Publication Bias in Meta-Analysis
Duval, S., & Tweedie, R. (2000) · Journal of the American Statistical Association · doi:10.1080/01621459.2000.10473905 · Cited by 2,955 · see citing works
A Fail-Safe N for Effect Size in Meta-Analysis
Orwin, R. G. (1983) · Journal of Educational Statistics · doi:10.2307/1164923 · Cited by 2,064 · see citing works
Analysis of foodborne outbreak data reported internationally for source attribution
Greig, J. D., & Ravel, A. (2009) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2008.12.031 · Cited by 451 · see citing works
CAMPYLOBACTER ENTERITIS AT A UNIVERSITY: TRANSMISSION FROM EATINGCHICKEN AND FROM CATS
DEMING, M. S., TAUXE, R. V., BLAKE, P. A., DIXON, S. E., FOWLER, B. S., JONES, T. S., LOCKAMY, E. A., PATTON, C. M., & SIKES, R. O. (1987) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a114685 · Cited by 271 · see citing works
Systematic Reviews to Support Evidence-Based Medicine: How to appraise, conduct and publish reviews
Khan, K. S., & Zamora, J. (2022) · doi:10.1201/9781003220039 · Cited by 151 · see citing works
Flagged first, then by citations
Research works printed but not linked: 57
- Mead PS, et al. Food-related illness and death in the United States. Emerging Infectious Diseases 1999; 5, 607-625.
- Mølbak K, Olsen JE, Wegener H. Salmonella infections, chapter 3, 2006, pp. 57-136.
- Baker MG, et al. Recurring salmonellosis epidemic in New Zealand linked to contact with sheep. Epidemi- ology and Infection 2007; 135, 76-83.
- Neimann J, et al. A case-control study of risk factors for sporadic Campylobacter infections in Denmark. Epidemiology and Infection 2003; 130: 353-366.
- Wallace MA, Thompson G. Salmonellosis in a nursing home patient on enteral feeding. American Journal of Infection Control 2006 ; 34 : 97.
- Engberg J. Contributions to the epidemiology of Campylobacter infections. A review of clinical and microbiological studies. Danish Medical Bulletin 2006; 53 : 361-389.
- Pires SM, et al. Attributing the human disease burden of foodborne infections to specific sources. Foodborne Pathogens and Diseases 2009; 6 : 417-424.
- Clayton D, Hills M. Statistical Models in Epidemiology. Oxford, New York, Tokyo: Oxford University Press, 1993.
- Stafford RJ, et al. Population-attributable risk estimates for risk factors associated with Campylobacter infection, Australia. Emerging Infectious Diseases 2008; 14 : 895- 901.
- Khan K, et al. Systematic reviews to support evidence- based medicine. Preventive Veterinary Medicine 2009; 87 : 213-228.
- Sargeant JM, et al. The process of systematic review and its application in agri-food public-health. Preventive Veterinary Medicine 2006; 75 : 141-151.
- Borenstein M. Introduction to Meta-Analysis. United Kingdom : John Wiley & Sons Ltd, 2009.
- Halasa T, et al. Meta-analysis of dry cow management for dairy cattle. Part 1. Protection against new in- tramammary infections. Journal of Dairy Science 2009; 92 : 3134-3149.
- Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994 ; 50 : 1088-1101.
- Egger M, et al. Bias in meta-analysis detected by a simple, graphical test. British Medical Journal 1997; 315: 629-634.
- Domingues A, et al. Source attribution of human salmonellosis using a meta-analysis of case-control stu- dies of sporadic infections. Epidemiology and Infection. Published online : 8 December 2011. doi:10.1017/ S0950268811002172. · DOI
- Ekdahl K, et al. Travel-associated non-typhoidal salmonellosis : geographical and seasonal differences and serotype distribution. Clinical Microbiology and Infection 2005 ; 11 : 138-144.
- Havelaar AH, et al. Attribution of foodborne patho- gens using structured expert elicitation. Foodborne Pathogens and Diseases 2008; 5 : 649-659.
- Mullner P, et al. Source attribution of food-borne zo- onoses in New Zealand : a modified Hald model. Risk Analysis 2009; 29 : 970-984.
- Evers EG, et al. Campylobacter source attribution by exposure assessment. International Journal of Risk Assessment and Management 2008; 8 : 174-190.
- Vellinga A, Van LF. The dioxin crisis as experiment to determine poultry-related Campylobacter enteritis. Emerging Infectious Diseases 2002; 8: 19-22.
- Rosenquist H, et al. Trends in gastroenteritis (GE) in the Netherlandsm, 1996-2003. Infectieziekten Bulletin 2004 ; 15 : 335-341.
- Mullner P, et al. Molecular and spatial epidemiology of human campylobacteriosis : source association and genotype-related risk factors. Epidemiology and Infection 2010 ; 138: 1372-1383.
- Hald T, et al. The attribution of human infections with antimicrobial resistant Salmonella bacteria in Denmark to sources of animal origin. Foodborne Pathogens and Diseases 2007; 4 : 313-326.
- Halasa T, et al. Meta-analysis of dry cow management for dairy cattle. Part 2. Cure of existing intramammary infections. Journal of Dairy Science 2009; 92 : 3150- 3157.
- Ferguson CJ. Evidence for publication bias in video game violence effects literature : a meta-analytic review. Aggression and Violent Behavior 7; 12 : 470-482.
- Painter JA, et al. Recipes for foodborne outbreaks : a scheme for categorizing and grouping implicated foods. Foodborne Pathogens and Diseases 2009; 6 : 1259-1264.
- Wingstrand A, et al. Fresh chicken as main risk factor for campylobacteriosis, Denmark. Emerging Infectious Diseases 2006; 12 : 280-285.
- Ethelberg S, et al. Spatial distribution and registry- based case-control analysis of Campylobacter infections in Denmark, 1991-2001. American Journal of Epi- demiology 2005; 162: 1008-1015.
- Carrique-Mas J, et al. Risk factors for domestic sporadic campylobacteriosis among young children in Sweden. Scandinavian Journal of Infectious Diseases 2005; 37 : 101-110.
- Schonberg-Norio D, et al. Swimming and Campylo- bacter infections. Emerging Infectious Diseases 2004; 10 : 1474-1477.
- Kapperud G, et al. Factors associated with increased and decreased risk of Campylobacter infection : a prospective case-control study in Norway. American Journal of Epidemiology 2003 ; 158: 234-242.
- Tenkate TD, Stafford RJ. Risk factors for Campylobacter infection in infants and young children: a matched case-control study. Epidemiology and Infection 2001; 127: 399-404.
- Rodrigues LC, et al. The study of infectious intestinal disease in England : risk factors for cases of infectious intestinal disease with Campylobacter jejuni infection. Epidemiology and Infection 2009; 127: 185-193.
- Studahl A, Andersson Y. Risk factors for indigenous Campylobacter infection : a Swedish case-control study. Epidemiology and Infection 2000; 125: 269-275.
- Effler P, et al. Sporadic Campylobacter jejuni infections in Hawaii : associations with prior antibiotic use and commercially prepared chicken. Journal of Infectious Diseases 2001; 183: 1152-1155.
- Neal KR, Slack RC. Diabetes mellitus, anti-secretory drugs and other risk factors for Campylobacter gastro- enteritis in adults : a case-control study. Epidemiology and Infection 1997; 119: 307-311.
- Eberhart-Phillips J, et al. Campylobacteriosis in New Zealand : results of a case-control study. Journal of Epidemiology and Community Health 1997; 51 : 686- 691.
- Adak GK, et al. The Public Health Laboratory Service national case-control study of primary indigenous sporadic cases of Campylobacter infection. Epidemi- ology and Infection 1995; 115: 15-22.
- Schorr D, et al. Risk factors for Campylobacter enteritis in Switzerland. Zentralblat fur Hygiene und Umweltmed 1994; 196: 327-337.
- Kapperud G, et al. Clinical features of sporadic Campylobacter infections in Norway. Scandinavian Journal of Infectious Diseases 1992; 24 : 741-749.
- Hudson SJ, et al. Jackdaws and magpies as vectors of milkborne human Campylobacter infection. Epidemi- ology and Infection 1991; 107: 363-372.
- Grados O, et al. Paediatric Campylobacter diarrhoea from household exposure to live chickens in Lima, Peru. Bulletin of the World Health Organization 1988; 66 : 369-374.
- Stafford RJ, et al. A multi-centre prospective case- control study of Campylobacter infection in persons aged 5 years and older in Australia. Epidemiology and Infection 2007; 135: 978-988.
- Michaud S, Menard S, Arbeit RD. Campylobacteriosis, Eastern Townships, Quebec. Emerging Infectious Diseases 2004; 10 : 1844-1847.
- Cameron S, et al. Consumption of foods by young children with diagnosed Campylobacter infection -a pilot case-control study. Public Health Nutrition 2004; 7 : 85-89.
- Neal KR, Slack RC. The autumn peak in Campylobacter gastroenteritis. Are the risk factors the same for travel-and UK-acquired Campylobacter in- fections ? Journal of Public Health Medicine 1995; 17 : 98-102.
- Schmid GP, et al. A one-year study of endemic campylobacteriosis in a midwestern city : association with consumption of raw milk. Journal of Infectious Diseases 1987; 156: 218-222.
- Harris NV, Weiss NS, Nolan CM. The role of poultry and meats in the etiology of Campylobacter jejuni/coli enteritis. American Journal of Public Health 1986; 76 : 407-411.
- Lighton LL, Kaczmarski EB, Jones DM. A study of risk factors for Campylobacter infection in late spring. Public Health 1991; 105: 199-203.
- Fullerton KE, et al. Sporadic Campylobacter infection in infants : a population-based surveillance case-control study. Pediatric Infectious Diseases Journal 2007; 26 : 19-24.
- Bellido-Blasco JB, et al. Risk factors for the occurrence of sporadic Campylobacter. Salmonella and rotavirus diarrhea in preschool children. Anales of Pediatria (Barcelona) 2007 ; 66 : 367-374.
- Potter RC, Kaneene JB, Hall WN. Risk factors for sporadic Campylobacter jejuni infections in rural michigan: a prospective case-control study. American Journal of Public Health 2003; 93 : 2118-2223.
- Unicomb LE, et al. Age-specific risk factors for sporadic Campylobacter infection in regional Australia. Food- borne Pathogens Diseases 2008; 5 : 79-85.
- Hopkins RS, Olmsted R, Istre GR. Endemic Campylobacter jejuni infection in Colorado : identified risk factors. American Journal of Public Health 1984; 74 : 249-250.
- Kapperud G, et al. Risk factors for sporadic Campylobacter infections : results of a case-control study in southeastern Norway. Journal of Clinical Microbiology 1992; 30 : 3117-3121.
- Gallay A, et al. Risk factors for acquiring sporadic Campylobacter infection in France : results from a national case-control study. Journal of Infectious Diseases 2008; 197: 1477-1484.
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Hald, T., Aspinall, W., Devleesschauwer, B., Cooke, R., Corrigan, T., Havelaar, A. H., Gibb, H. J., Torgerson, P. R., Kirk, M. D., Angulo, F. J., et al. (2016) · PLOS ONE · doi:10.1371/journal.pone.0145839 · Cited by 242 · see citing works
Self-citationRaw diets for dogs and cats: a review, with particular reference to microbiological hazards.
Davies, R. H., Lawes, J. R., & Wales, A. D. (2019) · Journal of Small Animal Practice · doi:10.1111/jsap.13000 · Cited by 195 · see citing works
“…with pets has also been identified as a route or a risk factor for human salmonellosis in several case reports and studies (Finley et al. 2006, Domingues et al. 2012, Freeman et al. 2013), indicating that pets which have consumed Salmonellacontaminated feed also pose an infection risk to…”
BackgroundCardoso, M. J., Nicolau, A. I., Borda, D., Nielsen, L., Maia, R. L., Møretrø, T., Ferreira, V., Knøchel, S., Langsrud, S., & Teixeira, P. (2021) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12753 · Cited by 97 · see citing works
- Authors
- DOMINGUES, A. R., PIRES, S. M., HALASA, T., & HALD, T.
- Affiliations
- Technical University of Denmark (DK)
- Corresponding author
- DOMINGUES, A. R.
- Venue
- Epidemiology and Infection
- Publisher
- Cambridge University Press (CUP)
- Published
- 2012-01-03
- Volume
- 140
- Issue
- 6
- Pages
- 970-981
- ISSN
- 0950-2688 (ISSN-L)
- 1469-4409
- OpenAlex
- W2052878156
- Cited by
- 207
- References
- 5
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 9 · 2023: 12 · 2022: 7 · 2021: 11 · 2020: 27 · 2019: 20 · 2018: 18 · 2017: 17 · 2016: 16 · 2015: 18 · 2014: 9 · 2013: 24 · 2012: 7
- FWCI
- 2.44
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Epidemiology and Infection (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
- Life Sciences › Agricultural and Biological Sciences › Food Science › Food Safety and Hygiene
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Listeria monocytogenes in Food Safety
- Keywords
- campylobacteriosis, Campylobacter, sporadic infection, risk factors, source attribution, foodborne transmission, international travel, environmental exposure, human-to-human transmission, Salmonella, odds ratio
- MeSH terms
- Animals, Campylobacter Infections, Environment, Food Microbiology, Humans, Risk Factors, Travel, Odds Ratio
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