Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Effect of rearing system (free-range vs cage) on gut and muscle histomorphology and microbial loads of Italian White breed rabbits

  • Caterina Losacco (Department of Precision and Regenerative Medicine and Jonian Area, Section of Veterinary Science and Animal Production, University of Bari Aldo Moro) ;
  • Antonella Tinelli (Department of Veterinary Medicine, University of Study of Bari Aldo Moro) ;
  • Angela Dambrosio (Department of Veterinary Medicine, University of Study of Bari Aldo Moro) ;
  • Nicoletta C. Quaglia (Department of Veterinary Medicine, University of Study of Bari Aldo Moro) ;
  • Letizia Passantino (Department of Precision and Regenerative Medicine and Jonian Area, Section of Veterinary Science and Animal Production, University of Bari Aldo Moro) ;
  • Michele Schiavitto (Italian Rabbit Breeders Association (ANCIAIA)) ;
  • Giuseppe Passantino (Department of Veterinary Medicine, University of Study of Bari Aldo Moro) ;
  • Vito Laudadio (Department of Precision and Regenerative Medicine and Jonian Area, Section of Veterinary Science and Animal Production, University of Bari Aldo Moro) ;
  • Nicola Zizzo (Department of Veterinary Medicine, University of Study of Bari Aldo Moro) ;
  • Vincenzo Tufarelli (Department of Precision and Regenerative Medicine and Jonian Area, Section of Veterinary Science and Animal Production, University of Bari Aldo Moro)
  • Received : 2023.05.31
  • Accepted : 2023.07.13
  • Published : 2024.01.01
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Abstract

Objective: The growing consumers' interest on animal welfare has raised the request of products obtained by alternative rearing systems. The present study was conducted to assess the influence of housing system on gut and muscle morphology and on microbial load in rabbits reared under free-range (FR) and cage system (CS). Methods: A total of forty weaned (35 days of age) male Italian White breed rabbits were allotted according to the rearing system, and at 91 days of age were randomly selected and slaughtered for the morphological evaluation of tissue from duodenum and longissimus lumborum. Morphometric analysis of the villus height, villus width, crypt depth, villus height/crypt depth ratio, and villus surface was performed. The microbial loads on hind muscle was determined by total mesophilic aerobic count (TMAC), Escherichia coli and Enterobacteriaceae; whereas, total anaerobic bacteria count (TABC) and TMAC, E. coli and Enterobacteriaceae was determined on caecal content. Results: Rearing system did not interfere with the duodenum and muscle histomorphology in both rabbit groups. Similarly, microbial load of caecal content showed no significant differences on the TABC and TMAC. Conversely, significant difference was found for E. coli strains in caecal content, with the lower counts in FR compared to CS rabbits (p<0.01). Microbiological assay of muscle revealed significant lower TMAC in FR vs CS rabbits (p< 0.05). All rabbit meat samples were negative for E. Coli and Enterobacteriaceae. Conclusion: Free-range could be considered a possible alternative and sustainable rearing system in rabbits to preserve gut environment and muscle quality.

Keywords

Acknowledgement

Authors acknowledge the Apulia Region for supporting the research work within the framework of the Program RIPARTI POC Puglia FESR-FSE 2014/2020 at the University of Bari "Aldo Moro" (Grant No. 31523dd2).

References

  1. D'Agata M, Preziuso G, Russo C, Dalle Zotte A, Mourvaki E, Paci G. Effect of an outdoor rearing system on the welfare, growth performance, carcass and meat quality of a slowgrowing rabbit population. Meat Sci 2009;83:691-6. https://doi.org/10.1016/j.meatsci.2009.08.005
  2. Cullere M, Dalle Zotte A. Rabbit meat production and consumption: State of knowledge and future perspectives. Meat Sci 2018;143:137-46. https://doi.org/10.1016/j.meatsci.2018.04.029
  3. European Parliament. European Parliament resolution on minimum standards for the protection of farm rabbits P8_TAPROV 2017;0077. Strasbourg, France: European Parliament; 2017.
  4. DG Health and Food Safety. Communication from the Commission on the European Citizens' Initiative (ECI) "End the Cage Age". Maastricht, The Netherlands: European Union; 2021.
  5. Saxmose Nielsen S, Alvarez J, Bicout DJ, et al. Health and welfare of rabbits farmed in different production systems. EFSA J 2020;18:e05944. https://doi.org/10.2903/j.efsa.2020.5944
  6. Combes S, Postollec G, Cauquil L, Gidenne T. Influence of cage or pen housing on carcass traits and meat quality of rabbit. Animal 2010;4:295-302. https://doi.org/10.1017/S1751731109991030
  7. Xiccato G, Trocino A, Majolini D, Tazzoli M, Zuffellato A. Housing of growing rabbits in individual, bicellular and collective cages: Growth performance, carcass traits and meat quality. Animal 2010;7:627-32. https://doi.org/10.1017/S175173111200198X
  8. Dalle Zotte A, Szendro K, Gerencser Z, et al. Effect of genotype, housing system and hay supplementation on carcass traits and meat quality of growing rabbits. Meat Sci 2015; 110:126-34. https://doi.org/10.1016/j.meatsci.2015.07.012
  9. Loponte R, Secci G, Mancini S, et al. Effect of the housing system (free-range vs. open air cages) on growth performance, carcass and meat quality and antioxidant capacity of rabbits. Meat Sci 2018;145:137-43. https://doi.org/10.1016/j.meatsci.2018.06.017
  10. Krunt O, Zita L, Kraus A, Brues D, Needham S, Volek Z. The effect of housing system on rabbit growth performance, carcass traits, and meat quality characteristics of different muscles. Meat Sci 2022;193:108953. https://doi.org/10.1016/j.meatsci.2022.108953
  11. Tufarelli V, Tateo A, Schiavitto M, Mazzei D, Calzaretti G, Laudadio V. Evaluating productive performance, meat quality and oxidation products of Italian White breed rabbits under free-range and cage rearing system. Anim Biosci 2022;35: 884-91. https://doi.org/10.5713/ab.21.0327
  12. Fetiveau M, Savietto D, Bannelier C, et al. Effect of outdoor grazing area size and genotype on space and pasture use, behaviour, health, and growth traits of weaned rabbits. AnimalOpen Space 2023;2:100038. https://doi.org/10.1016/j.anopes. 2023.100038
  13. Iser M, Martinez Y, Ni H, et al. The effects of Agave fourcroydes powder as a dietary supplement on growth performance, gut morphology, concentration of IgG, and hematology parameters in broiler rabbits. Biomed Res Int 2016;2016:3414319. https://doi.org/10.1155/2016/3414319
  14. Laparra JM, Sanz Y. Interactions of gut microbiota with functional food components and nutraceuticals. Pharmacol Res 2010;61:219-25. https://doi.org/10.1016/j.phrs.2009.11.001
  15. Schreuder J, Velkers FC, Bouwstra RJ, et al. An observational field study of the cloacal microbiota in adult laying hens with and without access to an outdoor range. Anim Microbiome 2020;2:28. https://doi.org/10.1186/s42523-020-00044-6
  16. Hubert SM, Al-Ajeeli M, Bailey CA, Athrey G. The role of housing environment and dietary protein source on the gut microbiota of chicken. Animals 2019;9:1085. https://doi.org/10.3390/ani9121085
  17. Monin G, Ouali A. Muscle differentiation and meat quality. In: Lawrie R, editor. Developments in meat science. London, UK/New York, USA: Elsevier Applied Science; 1991. pp.89-157.
  18. Gondret F, Hernandez P, Remignon H, Combes S. Skeletal muscle adaptations and biomechanical properties of tendons in response to jump exercise in rabbits. J Anim Sci 2009;87:544-53. https://doi.org/10.2527/jas.2008-1286
  19. Blasco A, Ouhayoun J. Harmonization of criteria and terminology in rabbit meat research. Revised proposal. World Rabbit Sci 1996;4:93-9. https://doi.org/10.4995/wrs.1996.278
  20. Jawad I, Kadhim KH, Kadhim DMH, Sadiq DH. A comparative histomorphological and histochemical study of the goblet cells and Brunner's glands in the duodenum of rabbits and rats. Res J Pharm Technol 2019;12:2421-4. https://doi.org/10.5958/0974-360X.2019.00406.2
  21. Huang P, Cui X, Wang Z, et al. Effects of Clostridium butyricum and a bacteriophage cocktail on growth performance, serum biochemistry, digestive enzyme activities, intestinal morphology, immune responses, and the intestinal microbiota in rabbits. Antibiotics 2021;10:1347. https://doi.org/10.3390/antibiotics10111347
  22. Mourao JL, Pinheiro V, Alves A, et al. Effect of mannan oligosaccharides on the performance, intestinal morphology and cecal fermentation of fattening rabbits. Anim Feed Sci Technol 2006;126:107-20. https://doi.org/10.1016/j.anifeedsci.2005.06.009
  23. Vantus VB, Kovacs M, Zsolnai A. The rabbit caecal microbiota: development, composition and its role in the prevention of digestive diseases - a review on recent literature in the light of molecular genetic methods. Acta Agraria Kaposvariensis 2014;18:55-65.
  24. Artuso-Ponte V, Pastor A, Andratsch M. The effects of plant extracts on the immune system of livestock: The isoquinoline alkaloids model. In: Florou-Paneri P, Christaki E, Giannenas I, editors. Feed additives, aromatic plants and herbs in animal nutrition and health. London, UK/SanDiego, CA, USA: Academic Press; 2020. pp. 295-310.
  25. Placha I, Bacova K, Zitterl-Eglseer K, et al. Thymol in fattening rabbit diet, its bioavailability and effects on intestinal morphology, microbiota from caecal content and immunity. J Anim Physiol Anim Nutr 2022;106:368-77. https://doi.org/10.1111/jpn.13595
  26. Gerritsen J, Smidt H, Rijkers GT, de Vos WM. Intestinal microbiota in human health and disease: the impact of probiotics. Genes Nutr 2011;6:209-40. https://doi.org/10.1007/s12263-011-0229-7
  27. Cui Y, Wang Q, Liu S, Sun R, Zhou Y, Li Y. Age-related variations in intestinal microflora of free-range and caged hens. Front Microbiol 2017;8:1310. https://doi.org/10.3389/fmicb.2017.01310
  28. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009;9:313-23. https://doi.org/10.1038/nri2515
  29. Lee SH, Joo ST, Ryu YC. Skeletal muscle fiber type and myofibrillar proteins in relation to meat quality. Meat Sci 2010; 86:166-70. https://doi.org/10.1016/j.meatsci.2010.04.040
  30. Joo ST, Kim GD, Hwang YH, Ryu YC. Control of fresh meat quality through manipulation of muscle fiber characteristics. Meat Sci 2013;95:828-36. https://doi.org/10.1016/j.meatsci.2013.04.044
  31. Dalle Zotte A. Perception of rabbit meat quality and major factors influencing the rabbit carcass and meat quality. Livest Prod Sci 2002;75:11-32. https://doi.org/10.1016/S0301-6226(01)00308-6
  32. Ryu YC, Rhee MS, Kim BC. Estimation of correlation coefficients between histological parameters and carcass traits of pig longissimus dorsi muscle. Asian-Australas J Anim Sci 2004;17:428-33. https://doi.org/10.5713/ajas.2004.428
  33. Kim GD, Jeong JY, Jung EY, Yang HS, Lim HT, Joo ST. The influence of fiber size distribution of type IIB on carcass traits and meat quality in pigs. Meat Sci 2013;94:267-73. https://doi.org/10.1016/j.meatsci.2013.02.001
  34. Lee SH, Kim GD, Ryu YC, Ko KS. Effects of morphological characteristics of muscle fibers on porcine growth performance and pork quality. Food Sci Anim Resour 2016;36: 583-93. https://doi.org/10.5851/kosfa.2016.36.5.583
  35. Damez JL, Clerjon S. Meat quality assessment using biophysical methods related to meat structure. Meat Sci 2008;80:132-49. https://doi.org/10.1016/j.meatsci.2008.05.039
  36. Greenwood PL, Harden S, Hopkins DL. Myofibre characteristics of ovine longissimus and semitendinosus muscles are influenced by sire breed, gender, rearing type, age and carcass weight. Aust J Exp Agric 2007;47:1137-46. https://doi.org/10.1071/EA06324
  37. Lefaucheur L, Vigneron P. Post-natal changes in some histochemical and enzymatic characteristics of three pig muscles. Meat Sci 1986;16:199-216. https://doi.org/10.1016/0309-1740(86)90026-4
  38. Ouhayoun J. Influence of the diet on rabbit meat quality. In: De Blas CJ, Wisemann J, editors. The nutrition of the rabbit. Wallingford Oxon, UK: CABI; 1998. pp. 177-95.
  39. El-Sabrout K. Effect of rearing system and season on behaviour, productive performance and carcass quality of rabbit: a review. J Anim Behav Biometeorol 2018;6:102-8. https://doi.org/10. 31893/2318-1265jabb.v6n4p102-108 https://doi.org/10.31893/2318-1265jabb.v6n4p102-108
  40. Matics Z, Cullere M, Dalle Zotte A, et al. Effect of cage and pen housing on the live performance, carcase, and meat quality traits of growing rabbits. Ital J Anim Sci 2019;18:441-9. https://doi.org/10.1080/1828051X.2018.1532329
  41. Koutsoumanis K, Sofos JN. Microbial contamination. In: Encyclopedia of Meat Sciences. Academic Press; 2004. pp. 727-37. https://doi.org/10.1016/B0-12-464970-X/00070-2
  42. Pereira M, Malfeito-Ferreira M. A simple method to evaluate the shelf life of refrigerated rabbit meat. Food Control 2015; 49:70-4. https://doi.org/10.1016/j.foodcont.2013.10.021
  43. Branciari R, Galarini R, Trabalza-Marinucci M, et al. Effects of olive mill vegetation water phenol metabolites transferred to muscle through animal diet on rabbit meat microbial quality. Sustainability 2021;13:4522. https://doi.org/10.3390/su13084522
  44. Petracci M, Cavani C. Rabbit meat processing: Historical perspective to future directions. World Rabbit Sci 2013;21: 217-26. https://doi.org/10.4995/wrs.2013.1329