Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Available phosphorus levels modulate gene expression related to intestinal calcium and phosphorus absorption and bone parameters differently in gilts and barrows

  • Julia Christiane Votterl (Nutritional Physiology, Institute of Physiology, Pathophysiology and Biophysics, Department of Biomedical Sciences, University of Veterinary Medicine Vienna) ;
  • Jutamat Klinsoda (Institute of Food Research and Product Development, University of Kasetsart ) ;
  • Simone Koger (Institute of Animal Nutrition and Functional Plant Compounds, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna) ;
  • Isabel Hennig-Pauka (Field Station for Epidemiology, University of Veterinary Medicine Hannover) ;
  • Doris Verhovsek (University Clinic of Swine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna) ;
  • Barbara U. Metzler-Zebeli (Nutritional Physiology, Institute of Physiology, Pathophysiology and Biophysics, Department of Biomedical Sciences, University of Veterinary Medicine Vienna)
  • Received : 2022.06.23
  • Accepted : 2022.09.26
  • Published : 2023.05.01
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Abstract

Objective: Dietary phytase increases bioavailability of phytate-bound phosphorus (P) in pig nutrition affecting dietary calcium (Ca) to P ratio, intestinal uptake, and systemic utilization of both minerals, which may contribute to improper bone mineralization. We used phytase to assess long-term effects of two dietary available P (aP) levels using a one-phase feeding system on gene expression related to Ca and P homeostasis along the intestinal tract and in the kidney, short-chain fatty acids in stomach, cecum, and colon, serum, and bone parameters in growing gilts and barrows. Methods: Growing pigs (37.9±6.2 kg) had either free access to a diet without (Con; 75 gilts and 69 barrows) or with phytase (650 phytase units; n = 72/diet) for 56 days. Samples of blood, duodenal, jejunal, ileal, cecal, and colonic mucosa and digesta, kidney, and metacarpal bones were collected from 24 pigs (6 gilts and 6 barrows per diet). Results: Phytase decreased daily feed intake and average daily gain, whereas aP intake increased with phytase versus Con diet (p<0.05). Gilts had higher colonic expression of TRPV5, CDH1, CLDN4, ZO1, and OCLN and renal expression of TRPV5 and SLC34A3 compared to barrows (p<0.05). Phytase increased duodenal expression of TRPV5, TRPV6, CALB1, PMCA1b, CDH1, CLDN4, ZO1, and OCLN compared to Con diet (p<0.05). Furthermore, phytase increased expression of SCL34A2 in cecum and of FGF23 and CLDN4 in colon compared to Con diet (p<0.05). Alongside, phytase decreased gastric propionate, cecal valerate, and colonic caproate versus Con diet (p<0.05). Phytase reduced cortical wall thickness and index of metacarpal bones (p<0.05). Conclusion: Gene expression results suggested an intestinal adaptation to increased dietary aP amount by increasing duodenal trans- and paracellular Ca absorption to balance the systemically available Ca and P levels, whereas no adaption of relevant gene expression in kidney occurred. Greater average daily gain in barrows related to higher feed intake.

Keywords

Acknowledgement

The authors thank Sharma Suchitra, Arife Sener-Aydemir, Annegret Lucke, Melanie Wild, Manfred Hollmann and Thomas Enzinger (Institute of Animal Nutrition and Functional Plant Compounds), Lukas Schwarz (University Clinic of Swine) as well as Sylvia Posseth and Tamara Strini (VetFarm) from the University of Veterinary Medicine Vienna for excellent assistance with the animals, sampling and laboratory analysis.

References

  1. Skiba G, Sobol M, Raj S. Femur morphometry, densitometry, geometry and mechanical properties in young pigs fed a diet free of inorganic phosphorus and supplemented with phytase. Arch Anim Nutr 2017;71:81-92. https://doi.org/10.1080/1745039X.2016.1250542
  2. Dersjant-Li Y, Awati A, Schulze H, Partridge G. Phytase in non-ruminant animal nutrition: a critical review on phytase activities in the gastrointestinal tract and influencing factors. J Sci Food Agric 2015;95:878-96. https://doi.org/10.1002/jsfa.6998
  3. Miller HM, Slade RD, Taylor AE. High dietary inclusion levels of phytase in grower-finisher pigs. J Anim Sci 2016; 94:121-4. https://doi.org/10.2527/jas.2015-9784
  4. Gonzalez-Vega JC, Stein HH. Calcium digestibility and metabolism in pigs. Asian-Australas J Anim Sci 2014;27:1-9. https://doi.org/10.5713/ajas.2014.r.01
  5. Votterl JC, Klinsoda J, Hennig-Pauka I, Verhovsek D, MetzlerZebeli BU. Evaluation of serum parameters to predict the dietary intake of calcium and available phosphorus in growing pigs. Transl Anim Sci 2021;5:txab095. https://doi.org/10.1093/tas/txab059
  6. Gerlinger C, Oster M, Borgelt L, et al. Physiological and transcriptional responses in weaned piglets fed diets with varying phosphorus and calcium levels. Nutrients 2019;11:436. https://doi.org/10.3390/nu11020436
  7. Breves G, Kock J, Schroder B. Transport of nutrients and electrolytes across the intestinal wall in pigs. Livest Sci 2007; 109:4-13. https://doi.org/10.1016/j.livsci.2007.01.021
  8. Kiela PR, Hishan FK. Physiology of intestinal absorption and secretion. Best Pract Res Clin Gastroenterol 2016;30:145-59. https://doi.org/10.1016/j.bpg.2016.02.007
  9. Taylor JG, Bushinsky DA. Calcium and phosphorus homeostasis. Blood Purif 2009;27:387-94. https://doi.org/10.1159/000209740
  10. Klinsoda J, Votterl J, Zebeli Q, Metzler-Zebeli BU. Alterations of the viable ileal microbiota of the gut mucosa-lymph node axis in pigs fed phytase and lactic acid-treated cereals. Appl Environ Microbiol 2020;86:e02128-19. https://doi.org/10.1128/AEM.02128-19
  11. Metzler-Zebeli BU, Klinsoda J, Votterl JC, Verhovsek D. Maturational changes alter effects of dietary phytase supplementation on the fecal microbiome in fattening pigs. Microorganisms 2020;8:1073. https://doi.org/10.3390/microorganisms8071073
  12. Schneider S, Brunlehner EM, Schaffler M, et al. Feed calculation for pigs, 22. Auflag. Bayerische Landesanstalt fur Landwirtschaft(LfL); 2019.
  13. Committee on Nutrient Requirements of Swine, National Research Council. Nutrient requirements of swine. 11th ed. Washington, DC, USA: National Academy Press; 2012
  14. Votterl JC, Klinsoda J, Zebeli Q, Hennig-Pauka I, Kandler W, Metzler-Zebeli BU. Dietary phytase and lactic acid-treated cereal grains differently affected calcium and phosphorus homeostasis from intestinal uptake to systemic metabolism in a pig model. Nutrients 2020;12:1542. https://doi.org/10.3390/nu12051542
  15. Hegde S, Lin YM, Golovko G, et al. Microbiota dysbiosis and its pathophysiological significance in bowel obstruction. Sci Rep 2018;8:13044. https://doi.org/10.1038/s41598-018-31033-0
  16. Olsen KM, Gould SA, Walk CL, Serao NVL, Hansen SL, Patience JF. Evaluating phosphorus release by phytase in diets fed to growing pigs that are not deficient in phosphorus. J Anim Sci 2019;97:327-37. https://doi.org/10.1093/jas/sky402
  17. Sulabo RC, Jones CK, Tokach MD, et al. Factors affecting storage stability of various commercial phytase sources. J Anim Sci 2011;89:4262-71. https://doi.org/10.2527/jas.2011-3948
  18. Carbonare LD, Giannini S. Bone microarchitecture as an important determinant of bone strength. J Endocrinol Invest 2004;27:99-105. https://doi.org/10.1007/bf03350919
  19. Rupp T, Butscheidt S, Vettorazzi E, et al. High FGF23 levels are associated with impaired trabecular bone microarchitecture in patients with osteoporosis. Osteoporos Int 2019;30:1655-62. https://doi.org/10.1007/s00198-019-04996-7
  20. Metzler-Zebeli BU, Ertl R, Klein D, Zebeli Q. Explorative study of metabolic adaptations to various dietary calcium intakes and cereal sources on serum metabolome and hepatic gene expression in juvenile pigs. Metabolomics 2015;11:545-58. https://doi.org/10.1007/s11306-014-0714-2
  21. Zemel MB. Role of calcium and dairy products in energy partitioning and weight management. Am J Clin Nutr 2004; 79:907S-12S. https://doi.org/10.1093/ajcn/79.5.907s
  22. Malagutti L, Colombini S, Pirondini M, Crovetto GM, Rapetti L, Galassi G. Effects of phytase on growth and slaughter performance, digestibility and nitrogen and mineral balance in heavy pigs. Ital J Anim Sci 2012;11:e70. https://doi.org/10.4081/ijas.2012.e70
  23. Van den Broeke A, Aluwe M, Kress K, et al. Effect of dietary energy level in finishing phase on performance, carcass and meat quality in immunocastrates and barrows in comparison with gilts and entire male pigs. Animal 2022;16:100437. https://doi.org/10.1016/j.animal.2021.100437
  24. Erben RG. Update on FGF23 and Klotho signaling. Mol Cell Endocrinol 2016;432:56-65. https://doi.org/10.1016/j.mce.2016.05.008
  25. Slifer ZM, Blikslager AT. The integral role of tight junction proteins in the repair of injured intestinal epithelium. Int J Mol Sci 2020;21:972. https://doi.org/10.3390/ijms21030972
  26. Wongdee K, Rodrat M, Teerapornpuntakit J, Krishnamra N, Charoenphandhu N. Factors inhibiting intestinal calcium absorption: hormones and luminal factors that prevent excessive calcium uptake. J Physiol Sci 2019;69:683-96. https://doi.org/10.1007/s12576-019-00688-3
  27. Fujita H, Sugimoto K, Inatomi S, et al. Tight junction proteins Claudin-2 and -12 are critical for Vitamin D-dependent Ca2+ absorption between enterocytes. Mol Biol Cell 2008;19:1912-21. https://doi.org/10.1091/mbc.e07-09-0973
  28. Lee B, Moon KM, Kim CY. Tight junction in the intestinal epithelium: Its association with diseases and regulation by phytochemicals. J Immunol Res 2018;2018:2645465. https://doi.org/10.1155/2018/2645465