Glycosaminoglycans and vitamin C in ovo and the feeding of broiler chickens influence bone and cartilaginous histology

Arthur Zuanetti Curti; Elaine Talita  Santos; Lizandra Amoroso; Julyana Machado da Silva Martins; Jean Kaique Valentim; Sarah Sgavioli

doi:10.1590/1809-6891v26e-80477E

Authors

Arthur Zuanetti Curti Universidade Brasil, Descalvado, São Paulo, Brazil https://orcid.org/0009-0008-4869-1580
Elaine Talita Santos Universidade Estadual Paulista (UNESP), Jaboticabal, São Paulo, Brazil https://orcid.org/0000-0003-1463-1869
Lizandra Amoroso Universidade Estadual Paulista (UNESP), Jaboticabal, São Paulo, Brazil https://orcid.org/0000-0001-9848-7803
Julyana Machado da Silva Martins Universidade do Estado de Minas Gerais (UEMG), Ituiutaba, Minas Gerais, Brazil https://orcid.org/0000-0002-3360-9491
Jean Kaique Valentim Universidade Federal Rural do Rio de Janeiro (UFRRJ), Seropédica, Rio de Janeiro, Brazil https://orcid.org/0000-0001-8547-4149
Sarah Sgavioli Pontifícia Universidade Católica do Paraná (PUCPR), Curitiba, Paraná, Brazil https://orcid.org/0000-0003-1156-2386

DOI:

https://doi.org/10.1590/1809-6891v26e-80477E

Abstract

The objective of this study is to evaluate the effect of in ovo feeding and dietary supplementation with glycosaminoglycans (GAGs) and vitamin C, on the bone and cartilage histology of broiler chickens. A completely randomized factorial design (2 x 2) was used, with two treatments during incubation (non-injected eggs and eggs injected with 4 μg of additive/100 μL of water on the fourth day of incubation), and two treatments during rearing (diet without additive and diet with 0.74 g of additive/100 kg of feed). Each 100 g of in ovo additive contained 30 g of chondroitin sulfate, 30 g of glucosamine sulfate, and 5 g of vitamin C, while each 100 kg of feed contained 30 g of glucosamine sulfate, 24 g of chondroitin sulfate, and 20 g of vitamin C. On day 43 of rearing, the number of chondrocytes in the cartilage, osteocytes, and periosteal osteoblasts in the tibial diaphysis, and tibial diaphysis thickness were evaluated. An interaction (P < 0.05) between the factors was observed. Greater diaphysis thickness and osteoblast numbers were observed in broilers fed with 0.74 g of additive/kg without in ovo injection, as well as in those that received 4 µg of additive in-ovo, and no additive in the diet. On the other hand, the use of the in ovo and dietary additive resulted in a reduction in the number of osteocytes. It was concluded that in ovo feeding or dietary supplementation with vitamin C and chondroitin and glucosamine sulfates during broiler rearing benefited bone and cartilage development.

Downloads

Download data is not yet available.

References

Guevara-Torres BL, Landin-Grandvallet LA, Tirado-Madrid A, Villagómez-Cortés JA. Comparison of locomotion problems and its economic impact on Cobb and Ross broiler strains. Veterinary Science Research. 2021; 3:1–6. DOI: https://journals.bilpubgroup.com/index.php/vsr/article/view/4126

Santos MN, Widowski TM, Kiarie EG, Guerin MT, Edwards AM, Torrey S. In pursuit of a better broiler: walking ability and incidence of contact dermatitis in conventional and slower growing strains of broiler chickens. Poultry Science. 2022; 101:1-19. DOI: https://doi.org/10.1016/j.psj.2022.101768

Wilcox CH, Sandilands V, Mayasari N, Asmara IY, Anang A. A literature review of broiler chicken welfare, husbandry, and assessment. World's Poultry Science Journal. 2024; 80:3–32. DOI: http://dx.doi.org/10.1080/00439339.2023.2264824

Nicol CJ, Abeyesinghe SM, Chang YM. An analysis of the welfare of fast-growing and slower-growing strains of broiler chicken. Frontiers in Animal Science. 2024; 5:1-21. DOI: https://doi.org/10.3389/fanim.2024.1374609

Granquist EG, Vasdal G, De Jong IC, Moe RO. Lameness and its relationship with health and production measures in broiler chickens. Animal. 2019; 13:2365–2372. DOI: https://doi.org/10.1017/s1751731119000466

Yang X, Zhao Y, Gan H, Hawkins S, Eckelkamp L, Prado M, Tabler T. Modeling gait score of broiler chicken via production and behavioral data. Animal. 2023; 17:1-10. DOI: https://doi.org/10.1016/j.animal.2022.100692

Sgavioli S, Santos ET, Borges LL, Andrade-Garcia GM, Castiblanco DM, Almeida VR, Baraldi-Artoni SM. Effect of the addition of glycosaminoglycans on bone and cartilaginous development of broiler chickens. Poultry Science. 2017; 96:4017–4025. DOI: https://doi.org/10.3382/ps/pex228

Santos ET, Sgavioli S, Castiblanco DMC, Domingues CHDF, Quadros TCOD, Borges LL, Baraldi-Artoni SM. Glycosaminoglycans and vitamin C in ovo feeding affects bone characteristics of chicks. Revista Brasileira de Zootecnia. 2018; 47:1-6. DOI: https://doi.org/10.1590/rbz4720170304

Santos ET, Sgavioli S, Castiblanco DM, Borges LL, de Quadros TC, de Laurentiz AC, Baraldi-Artoni SM. Glycosaminoglycans and vitamin C affect broiler bone parameters. Poultry Science. 2019; 98:4694–4704. DOI: https://doi.org/10.3382/ps/pez177

Martins JM, dos Santos Neto LD, Sgavioli S, Araújo IC, Reis AA, Santos RS, Café MB. Effect of glycosaminoglycans on the structure and composition of articular cartilage and bone of broilers. Poultry Science. 2023; 102:1-7. DOI: https://doi.org/10.1016/j.psj.2023.102916

Martins JMS, Santos Neto LDD, Gomides LPS, Fernandes EDS, Sgavioli S, Stringhini JH, Café MB. Performance, nutrient digestibility, and intestinal histomorphometry of broilers fed diet supplemented with chondroitin and glucosamine sulfates. Revista Brasileira de Zootecnia. 2020; 49:1-10. DOI: https://doi.org/10.37496/rbz4920190248

Martins JM, dos Santos Neto LD, Noleto-Mendonça RA, de Carvalho GB, Sgavioli S, de Carvalho FB, Café MB. Dietary supplementation with glycosaminoglycans reduces locomotor problems in broiler chickens. Poultry Science. 2020; 99:6974–6982. DOI: https://doi.org/10.1016/j.psj.2020.09.061

Maxwell LK, Regier P, Achanta S. Comparison of glucosamine absorption after administration of oral liquid, chewable, and tablet formulations to dogs. Journal of the American Animal Hospital Association. 2016; 52:90–94. DOI: https://doi.org/10.5326/jaaha-ms-6267

Kantor ED, Lampe JW, Navarro SL, Song X, Milne GL, White E. Associations between glucosamine and chondroitin supplement use and biomarkers of systemic inflammation. The Journal of Alternative and Complementary Medicine. 2014; 20:479–485. DOI: https://doi.org/10.1089/acm.2013.0323

Goel A. Heat stress management in poultry. Journal of Animal Physiology and Animal Nutrition. 2021; 105:1136–1145. DOI: https://doi.org/10.1111/jpn.13496

Del Barrio AS, Mansilla WD, Navarro-Villa A, Mica JH, Smeets JH, Den Hartog LA, García-Ruiz AI. Effect of mineral and vitamin C mix on growth performance and blood corticosterone concentrations in heat-stressed broilers. Journal of Applied Poultry Research. 2020; 29:23–33. DOI: https://doi.org/10.1016/j.japr.2019.11.001

Van Hieu T, Guntoro B, Qui NH, Quyen NTK, Al Hafiz FA. The application of ascorbic acid as a therapeutic feed additive to boost immunity and antioxidant activity of poultry in heat stress environment. Veterinary World. 2022; 15:685-693. DOI: https://doi.org/10.14202/vetworld.2022.685-693

Araújo IC, Café MB, Noleto RA, Martins JM, Ulhoa CJ, Guareshi GC, Leandro NS. ffect of vitamin E in ovo feeding to broiler embryos on hatchability, chick quality, oxidative state, and performance. Poultry Science. 2019; 98:3652–3661. DOI: https://doi.org/10.3382/ps/pey439

Peebles ED. In ovo applications in poultry: a review. Poultry Science. 2018; 97:2322–2338. DOI: https://doi.org/10.3382/ps/pey081

Shim MY, Pesti GM. Effects of incubation temperature on the bone development of broilers. The Journal of Poultry Science. 2011; 90:1867–1877. DOI: https://doi.org/10.3382/ps.2010-01242

Ferreira IB, Junior JM, Sgavioli S, Vicentini TI, Morita VS, Boleli IC. Vitamin C prevents the effects of high rearing temperatures on the quality of broiler thigh meat. Poultry Science. 2015; 94:841–851. DOI: https://doi.org/10.3382/ps/pev058

Sgavioli S, Borges LL, de Almeida VR, Thimotheo M, de Oliveira JA, Boleli IC. Egg injection of ascorbic acid stimulates leucocytosis and cell proliferation in the bursa of Fabricius. International Journal of Poultry Science. 2013; 12:464-472. DOI: http://dx.doi.org/10.3923/ijps.2013.464.472

Cobb-Vantress. Manual de manejo de frangos de corte. 2008. Disponível em: https://wp.ufpel.edu.br/avicultura/files/2012/04/Cobb-Manual-Frango-Corte-BR.pdf

Rostagno HS, Albino LFT, Donzele JL, Gomes PC, Oliveira RD, Lopes DC, Euclides RF. Composição de alimentos e critérios nutricionais. Tabelas brasileiras para aves e suínos, 2ª edição. UFV, Viçosa, MG, 2011.

SAS Institute. SAS/STAT user’s guide: statistics. Version 9.2. Cary (NC): SAS Institute Inc.; 2002.

Pizauro Junior JM, Ciancaglini P, Macari M. Discondroplasia tibial: mecanismos de lesão e controle. Brazilian Journal of Poultry Science. 2002; 4:169–186. DOI: https://doi.org/10.1590/S1516-635X2002000300001

Duplomb L, Dagouassat M, Jourdon P, Heymann D. Concise review: embryonic stem cells: a new tool to study osteoblast and osteoclast differentiation. Stem Cells. 2007; 25:544–552. DOI: https://doi.org/10.1634/stemcells.2006-0395

Pizauro Júnior JM, Santos L, Gonçalves A. Estrutura e função do tecido ósseo. In: Fisiologia das aves comerciais. Jaboticabal: FUNEP; 2017.

Florencio-Silva R, Sasso GRDS, Sasso-Cerri E, Simões MJ, Cerri PS. Biology of bone tissue: structure, function, and factors that influence bone cells. BioMed Research International. 2015; 2015:1-17. DOI: https://doi.org/10.1155/2015/421746

Wolff RB. Glucosamine and chondroitin sulfate association increases tibial epiphyseal growth plate proliferation and bone formation in ovariectomized rats. Clinics. 2014; 69:847–853. DOI: https://doi.org/10.6061/clinics/2014(12)10

Choi HK, Kim GJ, Yoo HS, Song DH, Chung KH, Lee KJ, Koo YT, An JH. Vitamin C activates osteoblastogenesis and inhibits osteoclastogenesis via Wnt/β-Catenin/ATF4 signaling pathways. Nutrients. 2019; 11:1-20. DOI: https://doi.org/10.3390/nu11030506

Tat SK, Pelletier JP, Vergés J, Lajeunesse D, Montell E, Fahmi H, Martel-Pelletier J. Chondroitin and glucosamine sulfate in combination decrease the pro-resorptive properties of human osteoarthritis subchondral bone osteoblasts: a basic science study. Arthritis Research & Therapy. 2007; 9:1–10. DOI: https://doi.org/10.1186/ar2325