Phytase super-dosing modulates bone parameters and the concentration of the calcium epithelial carrier calbindin-D28k in quails (Coturnix coturnix japonica) under thermal stress
A. G. Ribeiro
A * , R. S. Silva A , F. S. Costa B , E. G. Silva A , J. E. Santos Ribeiro C , E. P. Saraiva A , F. G. P. Costa A and R. R. Guerra A
A
B
C
Abstract
Thermal stress causes significant changes in the bioavailability of minerals, especially calcium, in laying birds, resulting in reduced egg production, and compromising egg quality. Therefore, it is necessary to use additives that provide better nutrient availability and minimise the negative effects caused by high temperatures.
This study aimed to evaluate the effects of super-dosing the diet of laying quails submitted to different temperatures with phytase on their bone parameters and on the epithelial calcium transporter calbindin-D28K positivity.
Seven hundred and twenty (720) Japanese quails in the production phase were distributed in a completely randomised design, in a 5 × 3 factorial design, with five supplementation levels of phytase (0, 500, 1000, 1500, and 3000 FTU/kg), and three temperatures (24°C, 30°C and 36°C), totalling 15 treatments, and six replications of eight birds each. The study began at the 8th week of age and continued for two cycles of 21 days, totalling 42 days of experiment. Bone parameters of the tibias and calbindin-D28K positivity were measured by immunohistochemistry. The data were submitted to variance, Tukey, and regression analyses.
At 24°C, birds had higher averages for proximal, medial, and distal diaphyses than did birds at 30°C and 36°C, and a greater breaking strength of the tibias than did those at 36°C. There was an increasing linear effect on the medial diaphysis and Seedor index in the tibias with an increasing phytase supplementation level. Calcium (Ca) in the tibias was higher in birds kept at 30°C at a supplementation level of up to 1000 FTU of phytase, than in the birds at 24°C and 36°C, equalling at 1500 FTU, and lower at 3000 FTU. There was a quadratic effect for phosphorus (P) and the Ca:P ratio in the tibias of quails submitted to increasing concentrations of phytase. Quails kept at 30°C showed greater anti-calbindin-D28K positivity in the duodenum and jejunum, when compared to animals subjected to temperatures of 24°C and 36°C. Phytase doses of 500 and 1000 FTU increased calbindin-D28K positivity in the duodenum of quails kept at 30°C. At a supplementation level of 1500 FTU, phytase provided greater eggshell thickness and greater calbindin-D28K positivity in the uterus of quails kept at 36°C.
Therefore, it is recommended to use 1500 FTU of phytase for Japanese quail exposed to high temperatures.
These findings suggest that dietary phytase super-dosing can help alleviate thermal stress in Japanese quail.
Keywords: calcium transporter, exogenous enzyme, minerals, performance, production, supplementation, thermal stress, tibias.
References
Adams JE (2009) Quantitative computed tomography. European Journal of Radiology 71, 415-424.
| Crossref | Google Scholar | PubMed |
Alagawany M, Farag MR, Abd El-Hack ME, Patra A (2017) Heat stress: effects on productive and reproductive performance of quail. World’s Poultry Science Journal 73, 747-756.
| Crossref | Google Scholar |
Attia YA, Abd El-Hamid AE-HE, Abedalla AA, Berika MA, Al-Harthi MA, Kucuk O, Sahin K, Abou-Shehema BM (2016) Laying performance, digestibility and plasma hormones in laying hens exposed to chronic heat stress as affected by betaine, vitamin C, and/or vitamin E supplementation. SpringerPlus 5, 1619.
| Crossref | Google Scholar | PubMed |
Baghban-Kanani P, Hosseintabar-Ghasemabad B, Azimi-Youvalari S, Seidavi A, Laudadio V, Mazzei D, Tufarelli V (2020) Effect of dietary sesame (Sesame indicum L) seed meal level supplemented with lysine and phytase on performance traits and antioxidant status of late-phase laying hens. Asian–Australasian Journal of Animal Sciences 33, 277-285.
| Crossref | Google Scholar | PubMed |
Bar A (2008) Calcium homeostasis and vitamin D metabolism and expression in strongly calcifying laying birds. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 151, 477-490.
| Crossref | Google Scholar |
Beggs MR, Alexander RT (2017) Intestinal absorption and renal reabsorption of calcium throughout postnatal development. Experimental Biology and Medicine 242, 840-849.
| Crossref | Google Scholar |
Bernardes RD, de Oliveira CH, Arlindo Calderano A, de Sousa Ferreira R, Norais Maia Dias K, Figueiredo de Almeida B, Eleuterio Aleixo P, Teixeira Albino LF (2022) Effect of phytase and protease combination on performance, metabolizable energy, and amino acid digestibility of broilers fed nutrient-restricted diets. Revista Brasileira de Zootecnia 51, e20210211.
| Crossref | Google Scholar |
Bilal RM, Hassan F-U, Farag MR, Nasir TA, Ragni M, Mahgoub HAM, Alagawany M (2021) Thermal stress and high stocking densities in poultry farms: potential effects and mitigation strategies. Journal of Thermal Biology 99, 102944.
| Crossref | Google Scholar | PubMed |
Broch J, Savaris VDL, Wachholz L, Cirilo EH, Tesser GLS, Pacheco WJ, Eyng C, Pesti GM, Nunes RV (2021) Influence of phytate and phytase on performance, bone, and blood parameters of broilers at 42 days old. South African Journal of Animal Science 51, 160-171.
| Crossref | Google Scholar |
Chalmers HJ, Dykes NL, Lust G, Farese JP, Burton-Wurster NI, Williams AJ, Todhunter RJ (2006) Assessment of bone mineral density of the femoral head in dogs with early osteoarthritis. American Journal of Veterinary Research 67, 796-800.
| Crossref | Google Scholar | PubMed |
Corradino RA, Smith CA, Krook LP, Fullmer CS (1993) Tissue-specific regulation of shell gland calbindin D28K biosynthesis by estradiol in precociously matured, vitamin D-depleted chicks. Endocrinology 132, 193-198.
| Crossref | Google Scholar | PubMed |
Cowieson AJ, Wilcock P, Bedford MR (2011) Super-dosing effects of phytase in poultry and other monogastrics. World’s Poultry Science Journal 67, 225-236.
| Crossref | Google Scholar |
da Silva RM, Furlan AC, Ton APS, Martins EN, Scherer C, Murakami AE (2009) Calcium and phosphorus requirements of finishing meat quail. Revista Brasileira de Zootecnia 38, 1509-1524.
| Crossref | Google Scholar |
da Silva VC, de Sousa Nascimento R, Lopes Neto JP, Riberio Miranda J, de Melo Lopes FF, Furtado DA (2022) Bioclimatic zoning for quails in the dry period in the state of Paraíba, Brazil. Revista Ceres 69, 125-130.
| Crossref | Google Scholar |
Dallmann HM, Avila VS, Krabbe EL, Surek D, Bedendo GC, Toledo TS, Dallmann PR, Roll AAP, Roll VFB, Rutz F (2023) Different phytase levels and energy densities in broiler diets on performance, nutrient digestibility, and bone integrity from 28 to 35 days of age. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 75, 280-292.
| Crossref | Google Scholar |
Dang DX, Chun SG, Kim IH (2022) Feeding broiler chicks with Schizosaccharomyces pombe-expressed phytase-containing diet improves growth performance, phosphorus digestibility, toe ash, and footpad lesions. Animal Bioscience 35, 1390-1399.
| Crossref | Google Scholar | PubMed |
Dersjant-Li Y, Awati A, Schulze H, Partridge G (2014) Phytase in non-ruminant animal nutrition: a critical review on phytase activities in the gastrointestinal tract and influencing factors. Journal of the Science of Food and Agriculture 95, 878-896.
| Crossref | Google Scholar | PubMed |
Dersjant-Li Y, Evans C, Kumar A (2018) Effect of phytase dose and reduction in dietary calcium on performance, nutrient digestibility, bone ash and mineralization in broilers fed corn-soybean meal-based diets with reduced nutrient density. Animal Feed Science and Technology 242, 95-110.
| Crossref | Google Scholar |
Dersjant-Li Y, Bello A, Stormink T, Abdollahi MR, Ravindran V, Babatunde OO, Adeola O, Toghyani M, Liu SY, Selle PH, Marchal L (2022) Modeling improvements in ileal digestible amino acids by a novel consensus bacterial 6-phytase variant in broilers. Poultry Science 101, 101666.
| Crossref | Google Scholar |
Ebeid TA, Suzuki T, Sugiyama T (2012) High ambient temperature influences eggshell quality and calbindin-D28k localization of eggshell gland and all intestinal segments of laying hens. Poultry Science 91, 2282-2287.
| Crossref | Google Scholar | PubMed |
Farias MRS, Leite SCB, Silva HP, Pacheco DB, Alves GC, Abreu CG, Freitas ER (2021) Superdosing phytases in the diets of light laying hens: productive performance and bone quality. Brazilian Journal of Poultry Science 23, eRBCA-2020-1395.
| Crossref | Google Scholar |
Fisinin VI, Kavtarashvili ASH (2015) Heat stress in poultry. I. Danger, related physiological changes and symptoms (review). Agricultural Biology 50, 162-171.
| Crossref | Google Scholar |
Franzini BD, Cruz LCF, Sampaio SA, Borges KF, Barros HSS, Santana FXC, Gouveia ABVS, Paulo LMd, Minafra CS (2022) Blood hematological and hormonal indicators of stress in poultry. Research, Society and Development 11, e16111326303.
| Crossref | Google Scholar |
Gautier AE, Walk CL, Dilger RN (2018) Effects of a high level of phytase on broiler performance, bone ash, phosphorus utilization, and phytate dephosphorylation to inositol. Poultry Science 97, 211-218.
| Crossref | Google Scholar | PubMed |
Hirvonen J, Liljavirta J, Saarinen MT, Lehtinen MJ, Ahonen I, Nurminen P (2019) Effect of phytase on in vitro hydrolysis of phytate and the formation of myo-inositol phosphate esters in various feed materials. Journal of Agricultural and Food Chemistry 67, 11396-11402.
| Crossref | Google Scholar |
Hosseini-Vashan SJ, Golian A, Yaghobfar A (2016) Growth, immune, antioxidant, and bone responses of heat stress-exposed broilers fed diets supplemented with tomato pomace. International Journal of Biometeorology 60, 1183-1192.
| Crossref | Google Scholar | PubMed |
Jankowski J, Mikulski D, Tatara MR, Krupski W (2015) Effects of increased stocking density and heat stress on growth, performance, carcase characteristics and skeletal properties in turkeys. Veterinary Record 176, 21.
| Crossref | Google Scholar | PubMed |
Koelkebeck KW, Harrison PC, Madindou T (1993) Effect of carbonated drinking water on production performance and bone characteristics of laying hens exposed to high environmental temperatures. Poultry Science 72, 1800-1803.
| Crossref | Google Scholar | PubMed |
Manobhavan M, Elangovan AV, Sridhar M, Shet D, Ajith S, Pal DT, Gowda NKS (2016) Effect of super dosing of phytase on growth performance, ileal digestibility and bone characteristics in broilers fed corn–soya-based diets. Journal of Animal Physiology and Animal Nutrition 100, 93–-100.
| Crossref | Google Scholar |
Martínez-Vallespín B, Männer K, Ader P, Zentek J (2022) Evaluation of high doses of phytase in a low-phosphorus diet in comparison to a phytate-free diet on performance, apparent ileal digestibility of nutrients, bone mineralization, intestinal morphology, and immune traits in 21-day-old broiler chickens. Animals 12, 1955.
| Crossref | Google Scholar | PubMed |
Moraes LR, Delicato MEA, Cruz AS, Silva HTFNP, Alves CVBV, Campos DB, Saraiva EP, Costa FP, Guerra RR (2021) Methionine supplementing effects on intestine, liver and uterus morphology, and on positivity and expression of calbindin-D28k and TRPV6 epithelial calcium carriers in laying quail in thermoneutral conditions and under thermal stress. PLoS ONE 16, e0245615.
| Crossref | Google Scholar | PubMed |
Nys Y, Le Roy N (2018) Calcium homeostasis and eggshell biomineralization in female chicken. In ‘Vitamin D. Vol. 1’. 4th edn. (Ed. D Feldman) pp. 361–382. (Academic Press) doi:10.1016/B978-0-12-809965-0.00022-7
Oliveira JFd, Rossi Júnior JL, Leite FLG, Oliveira DCd, Costa LAVS, Silva ICCd, Teixeira MW, Costa FS (2012) Densitometria da vértebra dorsal, osso pleural e osso neural em tartarugas verdes hígidas por tomografia computadorizada quantitativa. Ciência Rural 42, 1440-1445 [In Portugese with English abstract].
| Crossref | Google Scholar |
Pieniazek J, Smith KA, Williams MP, Manangi MK, Vazquez-Anon M, Solbak A, Miller M, Lee JT (2017) Evaluation of increasing levels of a microbial phytase in phosphorus deficient broiler diets via live broiler performance, tibia bone ash, apparent metabolizable energy, and amino acid digestibility. Poultry Science 96, 370-382.
| Crossref | Google Scholar | PubMed |
Pirgozliev V, Bedford MR, Acamovic T, Mares P, Allymehr M (2011) The effects of supplementary bacterial phytase on dietary energy and total tract amino acid digestibility when fed to young chickens. British Poultry Science 52, 245-254.
| Crossref | Google Scholar | PubMed |
Porto ML, Teófilo TS, Cavalcanti DMLP, Freitas CIA, Oliveira MF, Fontenele-Neto JD (2021) Incubation variables, performance, and morphometry of the duodenal mucosa of Japanese quails (Coturnixcoturnix japonica) submitted to different incubation temperatures and thermally challenged after hatching. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 73, 495-507.
| Crossref | Google Scholar |
R Core Team (2022) ‘R: a language and environment for statistical computing (ver. 4.2.0).’ (R Foundation for Statistical Computing: Vienna, Austria) Available at https://www.R-project.org/
Rojas IYM, González EA, Menocal JA, Santos TT, Arguello JR, Coello CL (2017) Assessment of a phytase included with lactic acid on productive parameters and on deposition of phosphorus, calcium, and zinc in laying hens fed with sorghum–soybean-meal-based diets. Journal of Applied Animal Research 46, 314-321.
| Crossref | Google Scholar |
Rostagno MH (2020) Effects of heat stress on the gut health of poultry. Journal of Animal Science 98, skaa090.
| Crossref | Google Scholar |
Rostagno HS, Albino LFT, Hannas MI, Donzele JL, Sakomura NK, Perazzo FG, Saraiva A, Teixeira ML, Rodrigues PB, de Oliveira RF, de Toledo Barreto SL, Brito CO (2017) ‘Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais.’ 4th edn. p. 488. (UFV: Viçosa, Brazil) Available at https://edisciplinas.usp.br/pluginfile.php/4532766/mod_resource/content/1/Rostagno%20et%20al%202017.pdf [Portuguese]
Sahin N, Balci TA, Kucuk O, Smith MO, Sahin K (2009) Effects of 25-hydroxycholecalciferol and soy isoflavones supplementation on bone mineralisation of quail. British Poultry Science 50, 709-715.
| Crossref | Google Scholar | PubMed |
Sampath V, Gao S, Park JH, Kim IH (2023) Exogenous phytase improves growth performance, nutrient retention, tibia mineralization, and breast meat quality in ross-308 broilers. Agriculture 13(10), 1906.
| Crossref | Google Scholar |
San J, Zhang Z, Bu S, Zhang M, Hu J, Yang J, Wu G (2021) Changes in duodenal and nephritic Ca and P absorption in hens during different egg-laying periods. Heliyon 7, e06081.
| Crossref | Google Scholar | PubMed |
Seedor JG, Quartuccio HA, Thompson DD (1991) The bisphosphonate alendronate (MK-217) inhibits bone loss due to ovariectomy in rats. Journal of Bone and Mineral Research 6, 339-346.
| Crossref | Google Scholar | PubMed |
Sens RF, Bassi LS, Almeida LM, Rosso DF, Teixeira LV, Maiorka A (2021) Effect of different doses of phytase and protein content of soybean meal on growth performance, nutrient digestibility, and bone characteristics of broilers. Poultry Science 100, 100917.
| Crossref | Google Scholar | PubMed |
Sharma NK, Choct M, Wu SB, Smillie R, Morgan N, Omar AS, Sharma N, Swick RA (2016) Performance, litter quality and gaseous odour emissions of broilers fed phytase supplemented diets. Animal Nutrition 2, 288–-295.
| Crossref | Google Scholar |
Simões de Souza JC, Tavares Fernandes TH, de Albuquerque Bonelli M, Séllos Costa F (2018) Quantitative computed tomography of healthy adult boas (boa constrictor). Journal of Zoo and Wildlife Medicine 49, 1012-1015.
| Crossref | Google Scholar | PubMed |
Stapane L, Le Roy N, Ezagal J, Rodriguez-Navarro AB, Labas V, Combes-Soia L, Hincke MT, Gautron J (2020) Avian eggshell formation reveals a new paradigm for vertebrate mineralization via vesicular amorphous calcium carbonate. Journal of Biological Chemistry 295, 15853-15869.
| Crossref | Google Scholar | PubMed |
Sugiyama T, Kikuchi H, Hiyama S, Nishizawa K, Kusuhara S (2007) Expression and localisation of calbindin D28k in all intestinal segments of the laying hen. British Poultry Science 48, 233-238.
| Crossref | Google Scholar | PubMed |
Truong L, Miller MR, Sainz RD, King AJ (2023) Changes in Japanese quail (Coturnix coturnix japonica) blood gases and electrolytes in response to multigenerational heat stress. PLoS Climate 2, e0000144.
| Crossref | Google Scholar |
Vercese F, Garcia EA, Sartori JR, Silva AdP, Faitarone ABG, Berto DA, Molino AdB, Pelícia K (2012) Performance and egg quality of Japanese quails submitted to cyclic heat stress. Brazilian Journal of Poultry Science 14, 37-41.
| Crossref | Google Scholar |
Wang X, Li P, Zhao J, Jiao H, Lin H (2022) The temporal gene expression profiles of calcium and phosphorus transporters in Hy-Line Brown layers. Poultry Science 101, 101736.
| Crossref | Google Scholar | PubMed |
Wasti S, Sah N, Mishra B (2020) Impact of heat stress on poultry health and performances, and potential mitigation strategies. Animals 10, 1266.
| Crossref | Google Scholar | PubMed |
Wu JCY, Smith MW, Mitchell MA, Peacock MA, Turvey A, Keable SJ (1993) Enterocyte expression of calbindin, calbindin mRNA and calcium transport increases in jejunal tissue during onset of egg production in the fowl (Gallus domesticus). Comparative Biochemistry and Physiology Part A: Physiology 106, 263-269.
| Crossref | Google Scholar |
Yan F, Keen CA, Zhang KY, Waldroup PW (2005) Comparison of methods to evaluate bone mineralization. Journal of Applied Poultry Research 14, 492-498.
| Crossref | Google Scholar |
Yan FF, Mohammed AA, Murugesan GR, Cheng HW (2019) Effects of a dietary synbiotic inclusion on bone health in broilers subjected to cyclic heat stress episodes. Poultry Science 98, 1083-1089.
| Crossref | Google Scholar | PubMed |
Zhang YN, Wang S, Li KC, Ruan D, Chen W, Xia WG, Wang SL, Abouelezz KFM, Zheng CT (2020) Estimation of dietary zinc requirement for laying duck breeders: effects on productive and reproductive performance, egg quality, tibial characteristics, plasma biochemical and antioxidant indices, and zinc deposition. Poultry Science 99, 454-462.
| Crossref | Google Scholar | PubMed |
Zhang H, Majdeddin M, Gaublomme D, Taminiau B, Boone M, Elewaut D, Daube G, Josipovic I, Zhang K, Michiels J (2021) 25-hydroxycholecalciferol reverses heat induced alterations in bone quality in finisher broilers associated with effects on intestinal integrity and inflammation. Journal of Animal Science and Biotechnology 12, 104.
| Crossref | Google Scholar | PubMed |
