Hierarchical clustering as a tool to develop a classification scheme for rabbit meat quality
DOI:
https://doi.org/10.4995/wrs.2021.14368Keywords:
cooking loss, DFD meat, feed withdrawal, hierarchical cluster analysis, pre-slaughter management, rabbitAbstract
This study aimed to characterise the quality of meat from commercially-raised rabbits. Animals came from five different producers and were laughtered in three different plants under provincial or federal inspection jurisdiction. Animal behaviour evaluated by scan sampling prior to feed withdrawal (FW) and transport, as well as blood lactate concentration at exsanguination, did not raise concerns with respect to stress. Stomach pH was higher (P=0.047) when the FW time was short (≤13.5 h), at a mean value of 2.23. All pH values measured 1 h post-mortem from the Biceps femoris (BF) and almost all (97.6%) from the Longissimus lumborum (LL) were higher than 6. Values for ultimate pH measured 24 h postmortem(pHu) ranged from 5.80 to 6.83 and from 5.70 to 6.70 for BF and LL muscles, respectively. The maximum meat drip loss recorded was 2.6%, while cooking loss reached 30%. Meat lightness (L*) and colour intensity (C*) for the long FW times (≥23 h) were no different from those with short and intermediate (15.5 to 17.3 h) FW times. However, these colour parameters were higher for the short FW time class compared to the intermediate FW time class (P<0.02). A hierarchical cluster analysis based on pHu, cooking loss and lightness (L*) from 200 rabbit loins was performed. Of the four clusters created, clusters 1 and 2 had the best and second-best meat quality, respectively. Clusters 3 and 4 had the lowest meat quality and presented DFD-like (dark, firm and dry) characteristics. Meat did not exhibit PSE-like (pale, soft, exudative) characteristics, even for the slaughter lot with the minimum mean pHu. Of the eight slaughter lots evaluated, more than 50% of the meat from three of them fell into clusters 3 and 4; all three were in the intermediate FW time class. Overall, the quality of rabbit meat analysed was acceptable for commercial use, but rather variable. This suggests that there are factors within the value chain that are not yet fully controlled and require further investigation.
Downloads
References
AAFC. 2019. Rabbit supply Canada. Agriculture and Agri-Food Canada. http://www5.agr.gc.ca/resources/prod/Internet-Internet/MISB-DGSIM/SDAD-DDAS/RML-VRB/PDF/17Table38a_eng.pdf. Accessed January 2020.
Adzitey F., Nurul H. 2011. Pale soft exudative (PSE) and dark firm dry (DFD) meats: causes and measures to reduce these incidences-a mini review. Int. Food Res. J., 18: 11-20. https://doi.org/10.3923/ijps.2017.81.87
Allen C.D., Russell S.M., Fletcher D.L. 1997. The relationship of broiler breast meat colour and pH to shelf-life and odor development. Poult. Sci., 76: 1042-1046. https://doi.org/10.1093/ps/76.7.1042
Bianchi M., Petracci M., Venturi L., Cremonini M.A., Cavani C. 2008. Influence of pre-slaughter fasting on live weight loss, carcass yield and meat quality in rabbits. In Proc.: 9th World Rabbit Congress, 10-13 June, 2008. Verona, Italy. 1. 1313-1318.
Blasco A., Ouhayoun J. 1996. Harmonization of criteria and terminology in rabbit meat research. Revised proposal. World Rabbit Sci., 4: 93-99. https://doi.org/10.4995/wrs.1996.278
Blasco A., Nagy I., Hernández. P. 2018. Genetics of growth, carcass and meat quality in rabbits. Meat Sci., 145: 178-185. https://doi.org/10.1016/j.meatsci.2018.06.030
Calnan H., Jacob R.H., Pethick D.W., Gardner, G.E. 2016. Production factors influence fresh lamb longissimus colour more than muscle traits such as myoglobin concentration and pH. Meat Sci., 119: 41-50. https://doi.org/10.1016/j.meatsci.2016.04.009
Carmichael E.B., Strickland J.T., Driver R.L. 1945. The contents of the stomach, small intestine, cecum and colon of normal and fasting rabbits. Am. J. Physiol., 143: 562-566. https://doi.org/10.1152/ajplegacy.1945.143.4.562
Cavani C., Petracci M., Trocino A., Xiccato G. 2009. Advances in research on poultry and rabbit meat quality. Ital. J. Anim. Sci., 8: 741-750. https://doi.org/10.4081/ijas.2009.s2.741
CCAC. 2009. The care and use of farm animals in research, teaching and testing. Canadian Council on Animal Care. Available at http://www.ccac.ca/Documents/Standards/Guidelines/Farm_Animals.pdf. Accessed February 2020.
Choe J.H., Choi M.H., Ryu Y.C., Go G.W., Choi Y.M., Lee S.H., Lim K.S., Lee E.A., Kang J.H., Hong K.C., Kim B.C. 2015. Estimation of pork quality traits using exsanguination blood and postmortem muscle metabolites. Asian-Australas. J. Anim. Sci., 28: 862-869. https://doi.org/10.5713/ajas.14.0768
Choe J.H., Kim B.C. 2014. Association of blood glucose, blood lactate, serum cortisol levels, muscle metabolites, muscle fiber type composition, and pork quality traits. Meat Sci., 97: 137-142. https://doi.org/10.1016/j.meatsci.2014.01.024
CIE. 1976. Colorimetry. International Commission on Illumination. Publication 15 Vienna, Austria: Bureau Central de la CIE. Available at http://www.cie.co.at/. Accessed February 2020.
Coppings R.J., Ekhator N., Ghodrati A. 1989. Effects of antemortem treatment and transport on slaughter characteristics of fryer rabbits. J. Anim. Sci., 67: 872-880. https://doi.org/10.2527/jas1989.674849x
Cornejo-Espinoza J.G., Rodríguez-Ortega L.T., Pro-Martínez A., González-Cerón F., Conde-Martínez V.F., Ramírez-Guzmán M.E., López-Pérez E., Hernández-Cázares A.S. 2016. Efecto del ayuno ante mortem en el rendimiento de la canal y calidad de la carne de conejo. Arch. Zootec., 65: 171-175. https://doi.org/10.21071/az.v65i250.484
Correa J.A., Méthot S., Faucitano L. 2007. A modified meat juice container (EZ-DripLoss) procedure for a more reliable assessment of drip loss and related quality changes in pork meat. J. Muscle Foods, 18: 67-77. https://doi.org/10.1111/j.1745-4573.2007.00066.x
Cullere M., Dalle Zotte A. 2018. Rabbit meat production and consumption: State of knowledge and future perspectives. Meat Sci., 143: 137-146. https://doi.org/10.1016/j.meatsci.2018.04.029
Cullere M., Dalle Zotte A. 2019. Carcass traits and meat quality of rabbit, hare, guinea pig and capybara. In: Lorenzo J.M., Munekata P.E.S., Barba F.J., Toldrá F. (ed). More than beef, pork and chicken – the production, processing, and quality traits of other sources of meat for human diet. Springer Nature Switzerland, Gewerbestrasse, Switzerland, 167-210.
Dalle Zotte A. 2000. Propriétés spécifiques de la viande de lapin. Jornadas internacionales de cuniculture, Vila Real, Portugal, 101-110.
Dalle Zotte A. 2002. Perception of rabbit meat quality and major factors influencing the rabbit carcass and meat quality. Livestock Prod. Sci., 75: 11-32. https://doi.org/10.1016/S0301-6226(01)00308-6
Dalle Zotte A., Princz Z., Metzger S., Szabó A., Radnai I., Biró-Németh E., Orova, Z., Szendrő Zs. 2009. Response of fattening rabbits reared under different housing conditions. 2. Carcass and meat quality. Livestock Sci., 122: 39-47. https://doi.org/10.1016/j.livsci.2008.07.021
Dalle Zotte A., Szendrő K., Gerencser Z., Szendrő Z., Cullere M., Odermatt M., Radnai I., Matics Zs. 2015. Effect of genotype, housing system and hay supplementation on carcass traits and meat quality of growing rabbits. Meat Sci., 110: 126-134. https://doi.org/10.1016/j.meatsci.2015.07.012
Dokmanovic M., Baltic M.Z., Duric J., Ivanovic J., Popovic L., Todorovic M., Markovic R., Pantic S. 2015. Correlations among Stress Parameters, Meat and Carcass Quality Parametersin Pigs. Asian-Australas. J. Anim. Sci., 28: 435-441. https://doi.org/10.5713/ajas.14.0322
Edwards L.N., Engle T.E., Correa J.A., Paradis M.A., Grandin T., Anderson D.B. 2010a. The relationship between exsanguination blood lactate concentration and carcass quality in slaughter pigs. Meat Sci., 85: 435-440. https://doi.org/10.1016/j.meatsci.2010.02.012
Edwards L.N., Grandin T., Engle T.E., Porter S.P., Ritter M.J., Sosnicki A.A., Anderson D.B. 2010b. Use of exsanguination blood lactate to assess the quality of pre-slaughter pig handling. Meat Sci., 86: 384-390. https://doi.org/10.1016/j.meatsci.2010.05.022
FAO. 2017. The Statistics Division of the FAO. Food and Agriculture Organization of the United Nation. Available at: http://www.fao.org/faostat/en/#data/. Accessed February 2020.
Faucitano L., Saucier L., Correa J.A., Méthot S., Guigère A., Foury A., Mormède P., Bergeron R. 2006. Effect of feed texture, meal frequency and pre-slaughter fasting on carcass and meat quality, and urinary cortisol in pigs. Meat Sci., 74: 697-703. https://doi.org/10.1016/j.meatsci.2006.05.023
Faucitano L., Ielo M.C., Ster C., Lo Fiego D.P., Methot S., Saucier L. 2010. Shelf life of pork from five different quality classes. Meat Sci., 84: 466-469. https://doi.org/10.1016/j.meatsci.2009.09.017
Fazio F., Casella S, Giudice E, Giannetto C., Piccione G. 2015. Evaluation of secondary stress biomarkers during road transport in rabbit. Livestock Sci., 173: 106-110. https://doi.org/10.1016/j.livsci.2015.01.006
Friendship R.M., Melnichouk S.I., Dewey C.E. 2000. The use of omeprazole to alleviate stomach ulcers in swine during periods of feed withdrawal. Can. Vet. J., 41: 925-928.
Frobose H.L., Dritz S.S., Tokach M.D., Prusa K.J., DeRouchey J.M., Goodband R.D., Nelssen J.L. 2014. Effects of preslaughter feed withdrawal time on finishing pig carcass, body weight gain, and food safety characteristics in a commercial environment. J. Anim. Sci., 92: 3693-3700. https://doi.org/10.2527/jas.2013-7367
Gagaoua M., Picard B., Monteils V. 2018. Associations among animal, carcass, muscle characteristics, and fresh meat color traits in Charolais cattle. Meat Sci., 140: 145-156. https://doi.org/10.1016/j.meatsci.2018.03.004
Gondret F., Bonneau M. 1998. Mise en place des caractéristiques du muscle chez le lapin et incidence sur la qualité de la viande. IRNA Prod. Anim., 11: 335-347.
Gruber S.L., Tatum J.D., Engle T.E., Chapman P.L., Belk K.E., Smith G.C. 2010. Relationships of behavioral and physiological symptoms of pre-slaughter stress to beef longissimus muscle tenderness. J. Anim. Sci., 88: 1148-1159. https://doi.org/10.2527/jas.2009-2183
Hansen L.T., Berthelsen H. 2000. The effect of environmental enrichment on the behaviour of caged rabbits Oryctolagus cuniculus. Appl. Anim. Behav. Sci., 68: 163-178. https://doi.org/10.1016/s0168-1591(00)00093-9
Hassler U., Thadewald T. 2003. Nonsensical and biased correlation due to pooling heterogeneous samples. The Statistician, 52: 367-379. https://doi.org/10.2307/412821
Holdstock J., Aalhus J.L., Uttarob B.A., López-Campos Ó., Larsenb I.L., Bruce H.L. 2014. The impact of ultimate pH on muscle characteristics and sensory attributes of the longissimus thoracis within the dark cutting (Canada B4) beef carcass grade. Meat Sci., 98: 842-849. https://doi.org/10.1016/j.meatsci.2014.07.029
Hopkins D.L., Ponnampalam E.N., van de Ven R.J., Warner R.D. 2014. The effect of pH decline rate on the meat and eating quality of beef carcasses. Anim. Prod. Sci., 54: 407-413. https://doi.org/10.1071/AN12314
Hulot F., Ouhayoun J. 1999. Muscular pH and related traits in rabbits: A review. World Rabbit Sci., 7: 5-36. https://doi.org/10.4995/wrs.1999.378
Interbev. 2006. Le point sur la couleur de la viande bovine. Available at http://www.agrireseau.qc.ca/bovinsboucherie/ documents/couleur_viande_bovine1.pdf. Accessed February 2020.
Jolley P.D. 1990. Rabbit transport and its effects on meat quality. Appl. Anim. Behav. Sci., 28: 119-134. https://doi.org/10.1016/0168-1591(90)90049-J
Koné A.P., Cinq-Mars D., Desjardins Y., Guay F., Gosselin A., Saucier L. 2016. Effects of plant extracts and essential oils as feed supplements on quality and microbial traits of rabbit meat. World Rabbit Sci., 24: 107-119. https://doi.org/10.4995/wrs.2016.3665
Koné A.P., Velez Zea J.M., Gagné D., Cinq-Mars D., Guay F., Saucier L. 2018. Application of Carnobacterium maltaromaticum as a feed additive for weaned rabbits to improve meat microbial quality and safety. Meat Sci., 135: 174-188. https://doi.org/10.1016/j.meatsci.2017.09.017
Koné A.P., Desjardins Y., Gosselin A., Cinq-Mars D., Guay F, Saucier L. 2019. Plant extracts and essential oil product as feed additives to control rabbit meat microbial quality. Meat Sci., 150: 111-121. https://doi.org/10.1016/j.meatsci.2018.12.013
Lang J., Blikslager A., Regina D., Eisemann J., Argenzio R. 1998. Synergistic effect of hydrochloric acid and bile acids on the pars esophageal mucosa of the porcine stomach. Am. J. Vet. Res., 59: 1170-1176.
Langlois I., Planché A., Boysen S.R., Abeysekara S., Zello G.A. 2014. Blood concentrations of D- and L-lactate in healthy rabbits. J. Small Anim. Pract., 55: 451-456. https://doi.org/10.1111/jsap.12247
Lebas F., Coudert P., Rouvier R., Rochambeau H. 1997. The rabbit: husbandry, health and production. FAO (Ed). Animal Production and Health Series, Rome, Italy.
Lefaucheur L. 2010. A second look into fibre typing – Relation to meat quality. Meat Sci., 84: 257-270. https://doi.org/10.1016/j.meatsci.2009.05.004
MAPAQ. 2015. Monographie de l’industrie cunicole au Québec. Ministère de l’Agriculture et des Pêcheries du Québec. Available at https://www.mapaq.gouv.qc.ca/fr/publications/Monographie_cunicole_br.pdf. Accessed February 2020.
María G.A., Buil T., Liste G., Villarroel M., Sañudo C., Olleta J.L. 2006. Effects of transport time and season on aspects of rabbit meat quality. Meat Sci., 72: 773-777. https://doi.org/10.1016/j.meatsci.2005.10.012
Martín-Peláez S., Martin-Orue S.M., Pérez J.F., Fàbrega E., Tibau J., Gasa J. 2008. Increasing feed withdrawal and lairage times prior to slaughter decreases the gastrointestinal tract weight but favours the growth of cecal Enterobacteriaceae in pigs. Livestock Sci., 119: 70-76. https://doi.org/10.1016/j.livsci.2008.02.012
Martín-Peláez S., Peralta B., Creus E., Dalmau A., Velarde A., Pérez J.F., Mateu E., Martín–Orúe S.M. 2009. Different feed withdrawal times before slaughter influence caecal fermentation and faecal Salmonella shedding in pigs. Vet. J., 182:469-473. https://doi.org/10.1016/j.tvjl.2008.08.002
Masoero G., Riccioni L., Bergoglio G., Napoletano F. 1992. Implications of fasting and of transportation for a high quality rabbit meat product. J. Appl. Rabbit Res., 15: 841-847.
McLellan M.R., Lind L.R., Kime R.W. 1995. Hue angle determinations and statistical analysis for multiquadrant Hunter L, a, b data. J. Food Quality, 18: 235-240. https://doi.org/10.1111/j.1745-4557.1995.tb00377.x
Nakyinsige K., Sazili A.Q., Aghwan Z.A., Zulkifli I., Goh Y.M., Fatimah A.B. 2013. Changes in blood constituents of rabbits subjected to transportation under hot, humid tropical conditions. Asian-Australas. J. Anim. Sci., 26: 874-878. https://doi.org/10.5713/ajas.2012.12652
Neethling N.E., Suman S.P., Sigge G.O., Hoffman L.C., Hunt M.C. 2017. Exogenous and endogenous factors influencing color of fresh meat from ungulates. Meat Musc. Biol., 1: 253-275. https://doi.org/10.22175/mmb2017.06.0032
NFACC. 2018. Code of practice for the care and handling of rabbits. National farm animal care council. Available at https://www.nfacc.ca/pdfs/codes/rabbit_code_of_practice.pdf. Accessed February 2020.
Ouhayoun J., Lebas F. 1994. Effets de la diète hydrique, du transport et de l’attente avant l’abattage sur les composantes du rendement et sur les caractéristiques physico-chimiques musculaires. In Proc.: 6e Journées de la Recherche Cunicole, December 1994, La Rochelle, France. 443-448.
Pathare P.B., Opara U.L., Al-Said F.A.J. 2013. Colour measurement and analysis in fresh and processed foods: A review. Food Biopro. Technol., 6: 36-60. https://doi.org/10.1007/s11947-012-0867-9
Petracci M., Bianchi M., Cavani C. 2008. A critical appraisal of rabbit pre-slaughter conditions in a commercial production chain. In Proc.: 9th World Rabbit Congress, June 10-13, 2008. Verona, Italy. 1411-1415.
Piattoni F., Demeyer D., Maertens L. 1997. Fasting effects on in vitro fermentation pattern of rabbit caecal contents. World Rabbit Sci., 5: 23-26. https://doi.org/10.4995/wrs.1997.314
Piva A., Panciroli A., Meola E., Formigon A. 1996. Lactitol enhances short-chain fatty acid and gas production by swine caecal microflora to a greater extent when fermenting low rather than high fibre diets. J. Nutr., 126: 280-289. https://doi.org/10.1093/jn/126.1.280
Pla M. 1999. Carcass and meat quality of growing rabbits under high ambient temperature using high fat diets. Cahiers Options Méditerranéennes., 41: 93-98.
Polkinghorne R.J., Thompson J.M. 2010. Meats standards and grading-A world view. Meat Sci., 86: 227-235. https://doi.org/10.1016/j.meatsci.2010.05.010
Ponnampalam E.N., Hopkins D.L., Bruce H., Li D., Baldi G., Eldin Bekhit A. 2017. Causes and contributing factors to “dark cutting” meat: current trends and future directions: A review. Comp. Rev. Food Sci. Food Safety, 16: 400-430. https://doi.org/10.1111/1541-4337.12258
Puente J., Samanta S.S., Bruce H.L. 2019. Bovine M. longissimus thoracis meat quality differences due to Canada quality grade. Meat Sci., 155: 43-49. https://doi.org/10.1016/j.meatsci.2019.05.002
Purslow P.P., Mandell I.B., Widowski T.M., Brown J., deLange C.F. M., Robinson J.A.B., Squires E.J., Cha M.C., VanderVoort G. 2008. Modelling quality variations in commercial Ontario pork production. Meat Sci., 80: 123-131. https://doi.org/10.1016/j.meatsci.2008.05.022
Qu D., Zhoua X., Yang F., Tiana S., Zhang X., Ma L., Han J. 2017. Development of class model based on blood biochemical parameters as a diagnostic tool of PSE meat. Meat Sci., 128: 24-29. https://doi.org/10.1016/j.meatsci.2017.01.012
Rasmussen A.J., Anderson M. 1996. New method for determination of drip loss in pork muscles. In Proc.: 42nd International Congress of Meat Science and Technology,Norway, Lillehammer. 286-287.
Rocha L.M., Dionne A., Saucier L., Nannoni E., Faucitano L. 2015. Hand-held lactate analyzer as a tool for the realtime measurement of physical fatigue before slaughter and pork quality prediction. Animal, 9: 707-714. https://doi.org/10.1017/S1751731114002766
RMAAQ. 2019. Convention de mise en marché du lapin de chair. Régie des Marchés Agricoles et Alimentaires du Québec. Available at www.rmaaq.gouv.qc.ca/fileadmin/DocuCentre/Decision/2019/11551.pdf. Accessed February 2020.
Saucier L., Bernier D., Bergeron R., Méthot S., Giguère A., Faucitano L. 2007. Effect of feed texture, meal frequency and pre-slaughter fasting on behaviour, stomach weight and microbial carcass contamination in pigs. Can. J. Anim. Sci., 87: 479-486. https://doi.org/10.4141/A06-072
Saucier L. 2016. Microbial spoilage, quality and safety within the context of meat sustainability. Meat Sci., 120: 78-84. https://doi.org/10.1016/j.meatsci.2016.04.027
Składanowska-Baryza J., Ludwiczak A., Pruszyńska-Oszmałek E., Kołodziejski P., Bykowska M., Stanisz M. 2018. The effect of transport on the quality of rabbit meat. Anim. Sci. J., 89: 713-721. https://doi.org/10.1111/asj.12966
Sutherland M.A., McDonald A., McGlone J.J. 2009. Effects of variations in the environment, length of journey and type of trailer on the mortality and morbidity of pigs being transported to slaughter. Vet. Rec., 165: 13-18. https://doi.org/10.1136/vetrec.165.1.13
Trocino A., Xiccato G. 2006. Animal welfare in reared rabbits: A review with emphasis on housing systems. World Rabbit Sci., 14: 77-93. https://doi.org/10.4995/wrs.2006.553
Trocino A., Xiccato G., Queaque P.I., Sartori A. 2003. Effect of transport duration and gender on rabbit carcass and meat quality. World Rabbit Sci., 11: 32-43. https://doi.org/10.4995/wrs.2003.494
Trocino A., Zomeñoa C., Birolob M., Di Martinoc G., Stefanic A., Bonfantic L., Bertottoa D., Grattab F., Xiccatob G. 2018. Impact of pre-slaughter transport conditions on stress response, carcass traits, and meat quality in growing rabbits. Meat Sci., 146: 68-74. https://doi.org/10.1016/j.meatsci.2018.07.035
USDA. 2015. Rabbit from farm to table. United States Department of Agriculture. Available at: https://www.fsis.usda.gov/wps/ portal/fsis/topics/food-safety-education/get-answers/foodsafety-fact-sheets/meat-preparation/rabbit-from-farm-totable/rabbit-farm-table. Accessed February 2020.
Verga M., Luzi F., Petracci M., Cavani C. 2009. Welfare aspects in rabbit rearing and transport. Ital. J. Anim. Sci., 8: 191-204. https://doi.org/10.4081/ijas.2009.s1.191
Vergara H., Berruga M.I., Linares M.B. 2005. Effect of gas composition on rabbit meat quality in modified atmosphere packaging. J. Sci. Food Agricul., 85: 1981-1986. https://doi.org/10.1002/jsfa.2181
Viljoen H.F., de Kock H.L., Webb E.C. 2002. Consumer acceptability of dark, firm and dry (DFD) and normal pH beef steaks. Meat Sci., 61: 181-185. https://doi.org/10.1016/S0309-1740(01)00183-8
Xiong G.-Y., Xu1 X.-L., Zhu X.-B., Zhoul G.-H., Shi1 S. 2008. Effects of withholding food and/or water supply on the quality of meat from rex rabbits. J. Muscle Foods, 19: 374-384. https://doi.org/10.1111/j.1745-4573.2008.00123.x
Downloads
Published
Issue
Section
License
This journal is licensed under a "Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)".