Original Scientific Article
The impact of cattle hide cleanliness scores on microbial contamination of carcasses during slaughtering
Buket Kallem,
Pelin Koçak Kizanlik,
Cemil Şahiner,
Ergün Ömer Göksoy*

Mac Vet Rev 2022; 45 (1): 43 - 51

10.2478/macvetrev-2022-0012

Received: 28 July 2021

Received in revised form: 04 January 2022

Accepted: 20 January 2022

Available Online First: 11 February 2022

Published on: 15 March 2022

Correspondence: Ergün Ömer Göksoy, eogoksoy@adu.edu.tr

Abstract

This study aimed to investigate the effects of cleanliness scoring on the microbiological load of hide and the final contamination of cattle carcasses. Fifty cattle were classified from 1 (clean and dry) to 5 (filthy and wet). Aerobic colony count (ACC) and counts of Enterobacteriaceae (EC) and E. coli (ECC) were determined on the brisket, abdominal midline, rump, groin sites of the hides, and brisket, flank, groin, and hock of the carcasses. On hides, ACC ranged from 3.15±0.13 log cfu/cm2 in category 1 to 8.14±0.21 log cfu/cm2 in category 5. EC and ECC were ranging between 1.13±0.07 and 2.80±0.09 log cfu/cm2, and 1.21±0.05 and 2.15±0.07 log cfu/cm2, respectively. While the mean ACC on the carcasses ranged between 2.18±0.07 and 2.63±0.05 log cfu/cm2 irrespective of the categories, Enterobacteriaceae and E. coli could not be counted due to the detection limits. It was concluded that although the level of bacterial load increased significantly (P<0.001) with the increasing cleanliness category on the hide of the animals, the reflection of this increasing trend on carcasses and different parts of the carcasses were inconsistent and the hygiene provided in the slaughterhouse and processing line was the main factor to reduce cross-contamination during processing.

Keywords: cleanliness scoring, cattle carcass, cross-contamination, hide cleanliness, microbial load


References

  1. Antic, D., Blagojevic, B., Ducic, M., Mitrovic, R., Nastasijevic, I., Buncic, S. (2010). Treatment of cattle hides with Shellac-in-ethanol solution to reduce bacterial transferability - A preliminary study. Meat Sci. 85(1): 77-81. https://doi.org/10.1016/j.meatsci.2009.12.007 PMid:20374868
  2. Obaidat, M.M. (2020). Prevalence and antimicrobial resistance of Listeria monocytogenes, Salmonella enterica and Escherichia coli O157:H7 in imported beef cattle in Jordan. Comp Immunol Microb Infect Dis. 70, 101447. https://doi.org/10.1016/j.cimid.2020.101447 PMid:32105836
  3. Gill, C.O. (1998). Microbiological contamination of meat during slaughter and butchering of cattle, sheep and pigs. Microbiol Meat Poult. 118-157.
  4. Zweifel, C., Capek, M., Stephan, R. (2014). Microbiological contamination of cattle carcasses at different stages of slaughter in two abattoirs. Meat Sci. 98(2): 198-202. https://doi.org/10.1016/j.meatsci.2014.05.029 PMid:24967539
  5. Cartier, P. (1994). Use of the ownership status of large cattle as an indicator of the microbial load of their leather. Meat and Meat Products 15(4): 119-122. [in French]
  6. Serraino, A., Bardasi, L., Riu, R., Pizzamiglio, V., Liuzzo, G., Galletti, G., Giacometti, F., Merialdi, G. (2012). Visual evaluation of cattle cleanliness and correlation to carcass microbial contamination during slaughtering. Meat Sci. 90(2): 502-506. https://doi.org/10.1016/j.meatsci.2011.08.001 PMid:21906889
  7. Blagojevic, B., Antic, D., Ducic, M., Buncic, S. (2012). Visual cleanliness scores of cattle at slaughter and microbial loads on the hides and the carcases. Vet Rec. 170(22): 563. https://doi.org/10.1136/vr.100477 PMid:22505244
  8. Van Donkersgoed, J., Jericho, K.W.F., Grogan, H., Thorlakson, B. (1997). Preslaughter hide status of cattle and the microbiology of carcasses. J Food Prot. 60(12): 1502-1508. https://doi.org/10.4315/0362-028X-60.12.1502 PMid:31207746
  9. Antic, D., Blagojevic, B., Ducic, M., Nastasijevic, I., Mitrovic, R., Buncic, S. (2010). Distribution of microflora on cattle hides and its transmission to meat via direct contact. Food Control 21(7): 1025-1029. https://doi.org/10.1016/j.foodcont.2009.12.022
  10. Buncic, S., Nychas, G.J., Lee, M.R.F., Koutsoumanis, K., Hébraud, M., Desvaux, M., Chorianopoulos, N., et al. (2014). Microbial pathogen control in the beef chain: Recent research advances. Meat Sci. 97(3): 288-297. https://doi.org/10.1016/j.meatsci.2013.04.040 PMid:23688797
  11. Food Standards Agency [Internet]. Red meat safety & clean livestock. Published by the Food Standards Agency June 2002 [Reprinted March 2004]. https://www.foodstandards.gov.scot/downloads/Red_meat_safety_and_clean_livestock.pdf
  12. European Commission (2004) [Internet]. Regulation (EC) N° 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of foodstuffs. Official Journal of the European Union, L 139(1), 54. https://eur-lex.europa.eu/eli/reg/2004/852/oj
  13. European Commission (2004) [Internet]. Regulation (EC) N° 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for on the hygiene of foodstuffs. Official Journal of the European Union, L 139(853), 55. https://eur-lex.europa.eu/legal-content/en/ALL/?uri=CELEX%3A32004R0853
  14. Food Standards Agency [Internet]. Clean beef cattle for slaughter. A guide for producers. Published by the Food Standard Agency October 2007. https://www.foodstandards.gov.scot/downloads/cleanbeefsaf1007.pdf
  15. AFSCA (2006) [Internet]. Scientific committee of the federal agency for the safety of the food chain. 2006. D/2006/10413/2 - Good condition of the fleece for sour meat. Bruxelles: Gil Houins, 2006b. [in French] https://www.favv-afsca.be/publicationsthematiques/_documents/Folder_VC_FR_26-01-2018_web.pdf
  16. Bastien, D., Lucbert, J., Cartier, P. (2006). Cattle cleanliness at slaughter: observations report, factors involved and a method to grade. Renc Rech Ruminants. 13, 317-320. [in French]
  17. Regulation of special hygiene rules for animal food. Law of authorization: 5996. Official gazette of publication: 27.12.2011. Nr. 28155.
  18. Cenci-Goga, B.T., Miraglia, D., Ranucci, D., Branciari, R., Budelli, L., McCrindle, C.M., Cioffi, A., Mammoli, R. (2007). An in vitro system for the comparison of excision and wet-dry swabbing for microbiological sampling of beef carcasses. J Food Prot. 70(4): 930-936. https://doi.org/10.4315/0362-028X-70.4.930 PMid:17477263
  19. ISO-ISO 4833-2:2013 [Internet]. Microbiology of the food chain - Horizontal method for the enumeration of microorganisms - Part 2: Colony count at 30 degrees C by the surface plating tech-nique. International Standard 2013, Geneva, Switzerland. [Retrieved February 19, 2021]. https://www.iso.org/standard/29824.html
  20. ISO - ISO 21528-2:2004 [Internet]. Microbiology of food and animal feeding stuffs -Horizontal methods for the detection and enumeration of Enterobacteriaceae - Part 2: Colony-count method. [Retrieved February 19, 2021]. https://www.iso.org/standard/34566.html
  21. ISO - ISO 16649-2:2001 [Internet]. Microbiology of food and animal feeding stuffs -horizontal method for the enumeration of beta-glucuronidase-positive Escherichia coli - Part 2: Colony-count technique at 44 degrees C using 5-bromo-4-chloro-3-indolyl beta-D-glucuronide. [Retrieved February 19, 2021]. https://www.iso.org/standard/29824.html
  22. Barco, L., Belluco, S., Roccato, A., Ricci, A. (2015). A systematic review of studies on Escherichia coli and Enterobacteriaceae on beef carcasses at the slaughterhouse. Int J Food Microbiol. 207, 30-39. https://doi.org/10.1016/j.ijfoodmicro.2015.04.027 PMid:25978803
  23. ICMSF (International Commission on Microbiological Specifications for Foods) (2000). Microorganisms in foods 6: Microbial ecology of food commodities. Maryland: Aspen Publishers Inc.
  24. Nastasijevic, I., Tomasevic, I., Smigic, N., Milicevic, D., Petrovic, Z., Djekic, I. (2016). Hygiene assessment of Serbian meat establishments using different scoring systems. Food Control 62, 193-200. https://doi.org/10.1016/j.foodcont.2015.10.034
  25. Hauge, S., Nafstad, O., Røtterud, O.J., Nesbakken, T. (2012). The hygienic impact of categorisation of cattle by hide cleanliness in the abattoir. Food Control 27(1): 100-107. https://doi.org/10.1016/j.foodcont.2012.03.004
  26. Johanson, L., Underdal, B., Grøsland, K., Whelehan, O.P., Roberts, T.A. (1983). A survey of the hygienic quality of beef and pork carcasses in Norway. Acta Vet Scand. 24(1): 1-13. https://doi.org/10.1186/BF03546753 PMid:6869140 PMCid:PMC8291255
  27. Arthur, T.M., Bosilevac, J.M., Nou, X., Shackelford, S.D., Wheeler, T.L., Kent, M.P., Jaroni, D., et al. (2004). Escherichia coli O157 prevalence and enumeration of aerobic bacteria, Enterobacteriaceae, and Escherichia coli O157 at various steps in commercial beef processing plants. J Food Prot. 67(4): 658-665. https://doi.org/10.4315/0362-028X-67.4.658 PMid:15083715
  28. Reid, C.A., Small, A., Avery, S.M., Buncic, S. (2002). Presence of food-borne pathogens on cattle hides. Food Control 13(6-7): 411-415. https://doi.org/10.1016/S0956-7135(01)00050-0
  29. Garcia, A.B., Steele, W.B., Reid, S.W.J., Taylor, D.J. (2010). Risk of carcass contamination with Campylobacter in sheep sent for slaughter into an abattoir in Scotland. Prev Vet Med. 95(1-2): 99-107. https://doi.org/10.1016/j.prevetmed.2010.03.008 PMid:20381181
  30. Jericho, K.W.F., Bradley, J.A., Gannon, V.P.J., Kozub, G.C. (1993). Visual demerit and microbiological evaluation of beef carcasses: Methodology. J Food Prot. 56(2): 114-119. https://doi.org/10.4315/0362-028X-56.2.114 PMid:31084117
  31. Mackey, B.M., Roberts, T.A. (1993). Improving slaughter hygiene using HACCP and monitoring. Fleischwirtschaft Int. 2, 40-45.
  32. Reneau, J.K., Seykora, A.J., Heins, B.J. (2003). Relationship of cow hygiene scores and SCC. Proc Natl Mast Coun. Madison, WI. 362-363.
  33. Ruud, L.E., Bøe, K.E., Østerås, O. (2010). Risk factors for dirty dairy cows in Norwegian freestall systems. J Dairy Sci. 93(11): 5216-5224. https://doi.org/10.3168/jds.2010-3321 PMid:20965336
  34. Ridell, J., Korkeala, H. (1993). Special treatment during slaughtering in Finland of cattle carrying an excessive load of dung; Meat hygienic aspects. Meat Sci. 35(2): 223-228. https://doi.org/10.1016/0309-1740(93)90052-J
  35. Alvseike, O., Røssvoll, E., Røtterud, O.J., Nesbakken, T., Skjerve, E., Prieto, M., Sandberg, M., et al. (2019). Slaughter hygiene in European cattle and sheep abattoirs assessed by microbiological testing and hygiene performance rating. Food Control 101, 233-240. https://doi.org/10.1016/j.foodcont.2019.01.033


Copyright

© 2022 Kallem B. This is an open-access article published under the terms of the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Conflict of Interest Statement

The authors have declared that no competing interests exist.

Citation Information

Macedonian Veterinary Review. Volume 45, Issue 1, Pages 43-51, e-ISSN 1857-7415, p-ISSN 1409-7621, DOI: 10.2478/macvetrev-2022-0012, 2022