1887
Research Open Access
Like 0

Abstract

Background

is an important human and animal intestinal pathogen. Because of increasing indications of an association between and food, in 2015, the Administration of the Republic of Slovenia for Food Safety, Veterinary Sector and Plant Protection (UVHVVR) included in its national food surveillance.

Aim

We aim to report the results and experience with a nationwide and long-term testing of food for as a part of a regular national food surveillance programme.

Methods

Retail minced meat and meat preparations (beef, pork and poultry) were sampled within a three-year period, 2015 to 2017. Selected raw retail vegetables, leaf salads and root vegetables, and ready-to-eat salads were only sampled during 2016 and 2017. Seafood was only sampled in 2017.

Results

Altogether, 434 samples were tested, with 12 of 336 (3.6%) meat samples and 6 of 98 (6.1%) raw vegetables contaminated with . Twelve of 18 recovered food isolates were toxigenic (toxinotypes 0, III, V, XII). The isolates belonged to 13 different PCR ribotypes, 001 being most common (5 isolates). Several food types with an increased potential of being contaminated with were detected by surveillance.

Conclusion

The three-year testing within the national food surveillance revealed a low proportion of -contaminated food and high genotype variability. Because the risk of infection associated with contaminated food is unknown, no measures were recommended in the case of positive results.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2020.25.16.1900479
2020-04-23
2020-10-29
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2020.25.16.1900479
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/25/16/eurosurv-25-16-5.html?itemId=/content/10.2807/1560-7917.ES.2020.25.16.1900479&mimeType=html&fmt=ahah

References

  1. Lessa FC, Winston LG, McDonald LCEmerging Infections Program C. difficile Surveillance Team. Burden of Clostridium difficile infection in the United States. N Engl J Med. 2015;372(24):2369-70. PMID: 26061850 
  2. van Dorp SM, Kinross P, Gastmeier P, Behnke M, Kola A, Delmée M, et al. Standardised surveillance of Clostridium difficile infection in European acute care hospitals: a pilot study, 2013. Euro Surveill. 2016;21(29):30293.  https://doi.org/10.2807/1560-7917.ES.2016.21.29.30293  PMID: 27472820 
  3. Kola A, Wiuff C, Akerlund T, van Benthem BH, Coignard B, Lyytikäinen O, et al. Survey of Clostridium difficile infection surveillance systems in Europe, 2011. Euro Surveill. 2016;21(29):30291.  https://doi.org/10.2807/1560-7917.ES.2016.21.29.30291  PMID: 27469420 
  4. McFarland LV, Surawicz CM, Vindigni SM. Clostridium difficile infections: Epidemiology, diagnosis, and treatment. Evidence-Based Gastroenterology and Hepatology. 2019;4e:284-305.
  5. Nacionalni inštitut za javno zdravje (NIJZ). [National Institute for Public Health]. Epidemiološko spremljanje nalezljivih bolezni v Sloveniji v letu 2017. [Report on infectious disease surveillance in Slovenia for the year 2017]. Ljubljana: NIJZ; 2018. Slovenian. Available from: https://www.nijz.si/sites/www.nijz.si/files/uploaded/epidemiolosko_spremljanje_nb_v_sloveniji_2017_november2018_1.pdf
  6. Nacionalni inštitut za javno zdravje (NIJZ). [National Institute for Public Health]. Epidemiološko spremljanje nalezljivih bolezni v Sloveniji v letu 2015. [Report on infectious disease surveillance in Slovenia for the year 2015]. Ljubljana: NIJZ; 2016. Slovenian. Available from: http://www.nijz.si/sites/www.nijz.si/files/datoteke/epidemiolosko_spremljanje_nb_v_letu_2015.pdf
  7. Rupnik M. Is Clostridium difficile-associated infection a potentially zoonotic and foodborne disease? Clin Microbiol Infect. 2007;13(5):457-9.  https://doi.org/10.1111/j.1469-0691.2007.01687.x  PMID: 17331126 
  8. Rodriguez-Palacios A, Borgmann S, Kline TR, LeJeune JT. Clostridium difficile in foods and animals: history and measures to reduce exposure. Anim Health Res Rev. 2013;14(1):11-29.  https://doi.org/10.1017/S1466252312000229  PMID: 23324529 
  9. Brown AWW, Wilson RB. Clostridium difficile colitis and zoonotic origins-a narrative review. Gastroenterol Rep (Oxf). 2018;6(3):157-66.  https://doi.org/10.1093/gastro/goy016  PMID: 30151199 
  10. Rodriguez Diaz C, Seyboldt C, Rupnik M. Non-human C. difficile reservoirs and sources: animals, food, environment. Adv Exp Med Biol. 2018;1050:227-43.  https://doi.org/10.1007/978-3-319-72799-8_13  PMID: 29383672 
  11. Candel-Pérez C, Ros-Berruezo G, Martínez-Graciá C. A review of Clostridioides [Clostridium] difficile occurrence through the food chain. Food Microbiol. 2019;77:118-29.  https://doi.org/10.1016/j.fm.2018.08.012  PMID: 30297042 
  12. Knetsch CW, Connor TR, Mutreja A, van Dorp SM, Sanders IM, Browne HP, et al. Whole genome sequencing reveals potential spread of Clostridium difficile between humans and farm animals in the Netherlands, 2002 to 2011. Euro Surveill. 2014;19(45):20954.  https://doi.org/10.2807/1560-7917.ES2014.19.45.20954  PMID: 25411691 
  13. Knight DR, Squire MM, Collins DA, Riley TV. Genome analysis of Clostridium difficile PCR Ribotype 014 Lineage in Australian pigs and humans reveals a diverse genetic repertoire and signatures of long-range interspecies transmission. Front Microbiol. 2017;7:2138.  https://doi.org/10.3389/fmicb.2016.02138  PMID: 28123380 
  14. Knetsch CW, Kumar N, Forster SC, Connor TR, Browne HP, Harmanus C, et al. Zoonotic transfer of Clostridium difficile harboring antimicrobial resistance between farm animals and humans. J Clin Microbiol. 2018;56(3):e01384-17. PMID: 29237792 
  15. Knight DR, Riley TV. Genomic delineation of zoonotic origins of Clostridium difficile. Front Public Health. 2019;7:164.  https://doi.org/10.3389/fpubh.2019.00164  PMID: 31281807 
  16. Romano V, Pasquale V, Lemee L, El Meouche I, Pestel-Caron M, Capuano F, et al. Clostridioides difficile in the environment, food, animals and humans in southern Italy: Occurrence and genetic relatedness. Comp Immunol Microbiol Infect Dis. 2018;59:41-6.  https://doi.org/10.1016/j.cimid.2018.08.006  PMID: 30290886 
  17. Rodriguez C, Taminiau B, Van Broeck J, Delmée M, Daube G. Clostridium difficile in food and animals: A comprehensive review. Adv Exp Med Biol. 2016;932:65-92.  https://doi.org/10.1007/5584_2016_27  PMID: 27350639 
  18. Pasquale V, Romano VJ, Rupnik M, Dumontet S, Cižnár I, Aliberti F, et al. Isolation and characterization of Clostridium difficile from shellfish and marine environments. Folia Microbiol (Praha). 2011;56(5):431-7.  https://doi.org/10.1007/s12223-011-0068-3  PMID: 21901293 
  19. Pasquale V, Romano V, Rupnik M, Capuano F, Bove D, Aliberti F, et al. Occurrence of toxigenic Clostridium difficile in edible bivalve molluscs. Food Microbiol. 2012;31(2):309-12.  https://doi.org/10.1016/j.fm.2012.03.001  PMID: 22608238 
  20. Lim SC, Foster NF, Elliott B, Riley TV. High prevalence of Clostridium difficile on retail root vegetables, Western Australia. J Appl Microbiol. 2018;124(2):585-90.  https://doi.org/10.1111/jam.13653  PMID: 29193458 
  21. Tkalec V, Janezic S, Skok B, Simonic T, Mesaric S, Vrabic T, et al. High Clostridium difficile contamination rates of domestic and imported potatoes compared to some other vegetables in Slovenia. Food Microbiol. 2019;78:194-200.  https://doi.org/10.1016/j.fm.2018.10.017  PMID: 30497603 
  22. European Commission. Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. 30.4.2004: L 139. [Accessed 17 Apr 2020]. Available from: http://data.europa.eu/eli/reg/2004/853/2014-06-01
  23. Biasizzo M, Vadnjal S, Henigman U, Krizman M, Kirbis A, Jamnikar-Ciglenecki U. Development and validation of a new protocol for detecting and recovering Clostridium difficile from meat samples. J Food Prot. 2018;81(4):561-8.  https://doi.org/10.4315/0362-028X.JFP-17-354  PMID: 29517350 
  24. Best EL, Fawley WN, Parnell P, Wilcox MH. The potential for airborne dispersal of Clostridium difficile from symptomatic patients. Clin Infect Dis. 2010;50(11):1450-7.  https://doi.org/10.1086/652648  PMID: 20415567 
  25. Rupnik M. Clostridium difficile toxinotyping. Methods Mol Biol. 2010;646:67-76.  https://doi.org/10.1007/978-1-60327-365-7_5  PMID: 20597003 
  26. Janezic S. Direct PCR-Ribotyping of Clostridium difficile. Methods Mol Biol. 2016;1476:15-21.  https://doi.org/10.1007/978-1-4939-6361-4_2  PMID: 27507330 
  27. Rodriguez-Palacios A, Staempfli HR, Duffield T, Weese JS. Clostridium difficile in retail ground meat, Canada. Emerg Infect Dis. 2007;13(3):485-7.  https://doi.org/10.3201/eid1303.060988  PMID: 17552108 
  28. Songer JG, Trinh HT, Killgore GE, Thompson AD, McDonald LC, Limbago BM. Clostridium difficile in retail meat products, USA, 2007. Emerg Infect Dis. 2009;15(5):819-21.  https://doi.org/10.3201/eid1505.081071  PMID: 19402980 
  29. Warriner K, Xu C, Habash M, Sultan S, Weese SJ. Dissemination of Clostridium difficile in food and the environment: Significant sources of C. difficile community-acquired infection? J Appl Microbiol. 2017;122(3):542-53.  https://doi.org/10.1111/jam.13338  PMID: 27813268 
  30. Indra A, Lassnig H, Baliko N, Much P, Fiedler A, Huhulescu S, et al. Clostridium difficile: a new zoonotic agent? Wien Klin Wochenschr. 2009;121(3-4):91-5.  https://doi.org/10.1007/s00508-008-1127-x  PMID: 19280132 
  31. Hoffer E, Haechler H, Frei R, Stephan R. Low occurrence of Clostridium difficile in fecal samples of healthy calves and pigs at slaughter and in minced meat in Switzerland. J Food Prot. 2010;73(5):973-5.  https://doi.org/10.4315/0362-028X-73.5.973  PMID: 20501051 
  32. Von Abercron SM, Karlsson F, Wigh GT, Wierup M, Krovacek K. Low occurrence of Clostridium difficile in retail ground meat in Sweden. J Food Prot. 2009;72(8):1732-4.  https://doi.org/10.4315/0362-028X-72.8.1732  PMID: 19722410 
  33. Bakri MM, Brown DJ, Butcher JP, Sutherland AD. Clostridium difficile in ready-to-eat salads, Scotland. Emerg Infect Dis. 2009;15(5):817-8.  https://doi.org/10.3201/eid1505.081186  PMID: 19402979 
  34. Metcalf DS, Costa MC, Dew WM, Weese JS. Clostridium difficile in vegetables, Canada. Lett Appl Microbiol. 2010;51(5):600-2.  https://doi.org/10.1111/j.1472-765X.2010.02933.x  PMID: 21069911 
  35. Eckert C, Burghoffer B, Barbut F. Contamination of ready-to-eat raw vegetables with Clostridium difficile in France. J Med Microbiol. 2013;62(9):1435-8.  https://doi.org/10.1099/jmm.0.056358-0  PMID: 23449876 
  36. Eckert C, Burghoffer B, Barbut F. Contamination of ready-to-eat raw vegetables with Clostridium difficile in France. J Med Microbiol. 2013;62(9):1435-8.  https://doi.org/10.1099/jmm.0.056358-0  PMID: 23449876 
  37. Harvey RB, Norman KN, Andrews K, Hume ME, Scanlan CM, Callaway TR, et al. Clostridium difficile in poultry and poultry meat. Foodborne Pathog Dis. 2011;8(12):1321-3.  https://doi.org/10.1089/fpd.2011.0936  PMID: 21877928 
  38. Weese JS, Reid-Smith RJ, Avery BP, Rousseau J. Detection and characterization of Clostridium difficile in retail chicken. Lett Appl Microbiol. 2010;50(4):362-5.  https://doi.org/10.1111/j.1472-765X.2010.02802.x  PMID: 20102510 
  39. Atidégla SC, Huat J, Agbossou EK, Saint-Macary H, Glèlè Kakai R. Vegetable Contamination by the Fecal Bacteria of Poultry Manure: Case Study of Gardening Sites in Southern Benin. Int J Food Sci. 2016;2016:4767453.  https://doi.org/10.1155/2016/4767453  PMID: 27069914 
  40. Janezic S, Potocnik M, Zidaric V, Rupnik M. Highly divergent Clostridium difficile strains isolated from the environment. PLoS One. 2016;11(11):e0167101.  https://doi.org/10.1371/journal.pone.0167101  PMID: 27880843 
  41. Weese JS, Avery BP, Rousseau J, Reid-Smith RJ. Detection and enumeration of Clostridium difficile spores in retail beef and pork. Appl Environ Microbiol. 2009;75(15):5009-11.  https://doi.org/10.1128/AEM.00480-09  PMID: 19525267 
/content/10.2807/1560-7917.ES.2020.25.16.1900479
Loading

Data & Media loading...

Comment has been disabled for this content
Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error