Acidification of drinking water improved tibia mass of broilers through the alterations of intestinal barrier and microbiota |
Zhang, Huaiyong
(College of Animal Science and Technology, Henan Agricultural University)
Guo, Yujun (College of Animal Science and Technology, Henan Agricultural University) Wang, Ziyang (College of Animal Science and Technology, Henan Agricultural University) Wang, Yongshuai (College of Animal Science and Technology, Henan Agricultural University) Chen, Bo (College of Animal Science and Technology, Henan Agricultural University) Du, Pengfei (College of Animal Science and Technology, Henan Agricultural University) Zhang, Xiangli (College of Animal Science and Technology, Henan Agricultural University) Huang, Yanqun (College of Animal Science and Technology, Henan Agricultural University) Li, Peng (Novus International) Michiels, Joris (Laboratory for Animal Nutrition and Animal Product Quality, Department of Animal Sciences and Aquatic Ecology, Ghent University) Chen, Wen (College of Animal Science and Technology, Henan Agricultural University) |
1 | Rosen HN, Moses AC, Garber J, et al. Serum CTX: a new marker of bone resorption that shows treatment effect more often than other markers because of low coefficient of variability and large changes with bisphosphonate therapy. Calcif Tissue Int 2000;66:100-3. https://doi.org/10.1007/pl00005830 DOI |
2 | Tobiume H, Kanzaki S, Hida S, et al. Serum bone alkaline phosphatase isoenzyme levels in normal children and children with growth hormone (GH) deficiency: a potential marker for bone formation and response to GH therapy. J Clin Endocrinol Metab 1997;82:2056-61. https://doi.org/10.1210/jcem.82.7.4081 DOI |
3 | Boling SD, Douglas MW, Snow JL, Parsons CM, Baker DH. Citric acid does not improve phosphorus utilization in laying hens fed a corn-soybean meal diet. Poult Sci 2000;79:1335-7. https://doi.org/10.1093/ps/79.9.1335 DOI |
4 | Schirmer M, Franzosa EA, Lloyd-Price J, et al. Dynamics of metatranscription in the inflammatory bowel disease gut microbiome. Nat Microbiol 2018;3:337-46. https://doi.org/10.1038/s41564-017-0089-z DOI |
5 | Nourmohammadi R, Hosseini SM, Farhangfar H. Effect of dietary acidification on some blood parameters and weekly performance of broiler chickens. J Anim Vet Adv 2010;9:3092-7. https://doi.org/10.3923/javaa.2010.3092.3097 DOI |
6 | Islam KMS. Use of citric acid in broiler diets. World Poult Sci J 2012;68:104-18. https://doi.org/10.1017/S0043933912000116 DOI |
7 | Walters JR. Cell and molecular biology of the small intestine: new insights into differentiation, growth and repair. Curr Opin Gastroenterol 2004;20:70-6. https://doi.org/10.1097/00001574-200403000-00004 DOI |
8 | Zaiss MM, Jones RM, Schett G, Pacifici R. The gut-bone axis: how bacterial metabolites bridge the distance. J Clin Invest 2019;129:3018-28. https://doi.org/10.1172/jci128521 DOI |
9 | Zeng H, Chi H. Metabolic control of regulatory T cell development and function. Trends Immunol 2015;36:3-12. https://doi.org/10.1016/j.it.2014.08.003 DOI |
10 | Sato K, Takayanagi H. Osteoclasts, rheumatoid arthritis, and osteoimmunology. Curr Opin Rheumatol 2006;18:419-26. https://doi.org/10.1097/01.bor.0000231912.24740.a5 DOI |
11 | Li P, Schwarz EM, O'Keefe RJ, et al. Systemic tumor necrosis factor alpha mediates an increase in peripheral CD11bhigh osteoclast precursors in tumor necrosis factor alpha-transgenic mice. Arthritis Rheum 2004;50:265-76. https://doi.org/10.1002/art.11419 DOI |
12 | Bianchi ML. Inflammatory bowel diseases, celiac disease, and bone. Arch Biochem Biophys 2010;503:54-65. https://doi.org/10.1016/j.abb.2010.06.026 DOI |
13 | Zhang H, Zeng Q, Bai S, et al. Effect of graded calcium supplementation in low-nutrient density feed on tibia composition and bone turnover in meat ducks. Br J Nutr 2018;120:1217-29. https://doi.org/10.1017/s0007114518002556 DOI |
14 | Chowdhury R, Islam KM, Khan MJ, et al. Effect of citric acid, avilamycin, and their combination on the performance, tibia ash, and immune status of broilers. Poult Sci 2009;88:1616-22. https://doi.org/10.3382/ps.2009-00119 DOI |
15 | Swiatkiewicz S, Koreleski J, Arczewska A. Effect of organic acids and prebiotics on bone quality in laying hens fed diets with two levels of calcium and phosphorus. Acta Vet Brno 2010;79:185-93. https://doi.org/10.2754/avb201079020185 DOI |
16 | Mellor S. Nutraceuticals-alternatives to antibiotics. World Poult 2000;16:30-3. |
17 | Ohlsson C, Nigro G, Boneca IG, Backhed F, Sansonetti P, Sjogren K. Regulation of bone mass by the gut microbiota is dependent on NOD1 and NOD2 signaling. Cell Immunol 2017;317:55-8. https://doi.org/10.1016/j.cellimm.2017.05.003 DOI |
18 | National Research Council. Nutrient requirements of poultry, 9th rev. ed. Washington, DC, USA: National Academies Press; 1994. |
19 | Zhang HY, Liao H, Zeng QF, et al. A study on the sternum growth and mineralization kinetic of meat duck from 35 to 63 days of age. Poult Sci 2017;96:4103-15. https://doi.org/10.3382/ps/pex223 DOI |
20 | Horowitz MC. Cytokines and estrogen in bone: anti-osteoporotic effects. Science 1993;260:626-7. https://doi.org/10.1126/science.8480174 DOI |
21 | Nourmohammadi R, Hosseini SM, Farhangfar H, Bashtani M. Effect of citric acid and microbial phytase enzyme on ileal digestibility of some nutrients in broiler chicks fed cornsoybean meal diets. Ital J Anim Sci 2012;11:e7. https://doi.org/10.4081/ijas.2012.e7 DOI |
22 | D'Amelio P, Sassi F. Gut microbiota, immune system, and bone. Calcif Tissue Int 2018;102:415-25. https://doi.org/10.1007/s00223-017-0331-y DOI |
23 | Ragaa NM, Korany RMS. Studying the effect of formic acid and potassium diformate on performance, immunity and gut health of broiler chickens. Anim Nutr 2016;2:296-302. https://doi.org/10.1016/j.aninu.2016.08.003 DOI |
24 | Poli V, Balena R, Fattori E, et al. Interleukin-6 deficient mice are protected from bone loss caused by estrogen depletion. EMBO J 1994;13:1189-96. https://doi.org/10.1002/j.1460-2075.1994.tb06368.x DOI |
25 | Schepper JD, Collins FL, Rios-Arce ND, et al. Probiotic Lactobacillus reuteri prevents postantibiotic bone loss by reducing intestinal dysbiosis and preventing barrier disruption. J Bone Miner Res 2019;34:681-98. https://doi.org/10.1002/jbmr.3635 DOI |
26 | Sjogren K, Engdahl C, Henning P, et al. The gut microbiota regulates bone mass in mice. J Bone Miner Res 2012;27:1357-67. https://doi.org/10.1002/jbmr.1588 DOI |
27 | Pu J, Chen D, Tian G, et al. Protective effects of benzoic acid, bacillus coagulans, and oregano oil on intestinal injury caused by enterotoxigenic Escherichia coli in weaned piglets. Biomed Res Int 2018;2018:1829632. https://doi.org/10.1155/2018/1829632 DOI |
28 | Yesilbag D, Colpan I. Effects of organic acid supplemented diets on growth performance, egg production and quality and on serum parameters in laying hens. Rev Med Vet 2006;157:280-4. |
29 | Yang X, Xin H, Yang C, Yang X. Impact of essential oils and organic acids on the growth performance, digestive functions and immunity of broiler chickens. Anim Nutr 2018;4:388-93. https://doi.org/10.1016/j.aninu.2018.04.005 DOI |
30 | Li M, Long S, Wang Q, et al. Mixed organic acids improve nutrients digestibility, volatile fatty acids composition and intestinal microbiota in growing-finishing pigs fed high-fiber diet. Asian-Australas J Anim Sci 2019;32:856-64. https://doi.org/10.5713/ajas.18.0517 DOI |
31 | Hernandez F, Garcia V, Madrid J, Orengo J, Catala P, Megias MD. Effect of formic acid on performance, digestibility, intestinal histomorphology and plasma metabolite levels of broiler chickens. Br Poult Sci 2006;47:50-6. https://doi.org/10.1080/00071660500475574 DOI |
32 | Abbas G, Khan SH, Rehman HU. Effects of formic acid administration in the drinking water on production performance, egg quality and immune system in layers during hot season. Avian Biol Res 2013;6:227-32. https://doi.org/10.3184/175815513X13740707043279 DOI |
33 | Zhang H, Majdeddin M, Gaublomme D, et al. 25-hydroxycholecalciferol reverses heat induced alterations in bone quality in finisher broilers associated with effects on intestinal integrity and inflammation. J Anim Sci Biotechnol 2021;12:104. https://doi.org/10.1186/s40104-021-00627-6 DOI |
34 | Qin SM, Zhang KY, Ding XM, Bai SP, Wang JP, Zeng QF. Effect of dietary graded resistant potato starch levels on growth performance, plasma cytokines concentration, and intestinal health in meat ducks. Poult Sci 2019;98:3523-32. https://doi.org/10.3382/ps/pez186 DOI |
35 | Hamid H, Shi HQ, Ma GY, et al. Influence of acidified drinking water on growth performance and gastrointestinal function of broilers. Poult Sci 2018;97:3601-9. https://doi.org/10.3382/ps/pey212 DOI |
36 | Dibner JJ, Buttin P. Use of organic acids as a model to study the impact of gut microflora on nutrition and metabolism. J Appl Poult Res 2002;11:453-63. https://doi.org/10.1093/japr/11.4.453 DOI |
37 | Mohammadpour AA, Kermanshahi H, Golian A, Gholizadeh M, Gilani A. Evaluation of varying levels of acid-binding capacity of diets formulated with various acidifiers on physical and histological characteristics of leg bones in broiler chickens. Comp Clin Pathol 2014;23:1409-20. https://doi.org/10.1007/s00580-013-1798-1 DOI |
38 | Wu Y, Yin X, Wang Y, et al. Effect of 2-hydroxy-4-(methylthio) butanoic acid and acidifier on the performance, chyme pH, and microbiota of broilers. Anim Sci J 2020;91:e13409. https://doi.org/10.1111/asj.13409 DOI |
39 | Murer H, Forster I, Biber J. The sodium phosphate cotransporter family SLC34. Pflugers Arch Eur J Physiol 2004;447:763-7. https://doi.org/10.1007/s00424-003-1072-5 DOI |
40 | Esmaeilipour O, Shivazad M, Moravej H, Aminzadeh S, Rezaian M, van Krimpen MM. Effects of xylanase and citric acid on the performance, nutrient retention, and characteristics of gastrointestinal tract of broilers fed low-phosphorus wheat-based diets. Poult Sci 2011;90:1975-82. https://doi.org/10.3382/ps.2010-01264 DOI |
41 | Wang J, Wang Y, Gao W, et al. Diversity analysis of gut microbiota in osteoporosis and osteopenia patients. Peer J 2017;5:e3450. https://doi.org/10.7717/peerj.3450 DOI |
42 | Ebrahimnezhad Y, Maheri-sis N, Aghdam SH, et al. The effects of combination of citric acid and microbial phytase on the egg quality characteristics in laying hens. Asian J Anim Vet Adv 2008;3:293-7. https://doi.org/10.3923/ajava.2008.293.297 DOI |
43 | Chen YC, Greenbaum J, Shen H, Deng HW. Association between gut microbiota and bone health: potential mechanisms and prospective. J Clin Endocrinol Metab 2017;102:3635-46. https://doi.org/10.1210/jc.2017-00513 DOI |
44 | Zhang H, Zeng Q, Bai S, et al. Dietary supplementation of 25-hydroxycholecalciferol increases tibial mass by suppression bone resorption in meat ducks. Anim Nutr 2020;6:467-79. https://doi.org/10.1016/j.aninu.2020.05.006 DOI |
45 | Boling-Frankenbach SD, Snow JL, Parsons CM, Baker DH. The effect of citric acid on the calcium and phosphorus requirements of chicks fed corn-soybean meal diets. Poult Sci 2001;80:783-8. https://doi.org/10.1093/ps/80.6.783 DOI |
46 | Waldenstedt L. Nutritional factors of importance for optimal leg health in broilers: a review. Anim Feed Sci Technol 2006;126:291-307. https://doi.org/10.1016/j.anifeedsci.2005.08.008 DOI |
47 | Luckstadt C. Acidifiers in animal nutrition. Nottingham, UK: Nottingham University Press; 2007. |
48 | Ziaie H, Bashtani M, Torshizi MK, Naeeimipour H, Farhangfar H, Zeinali A. Effect of antibiotic and its alternatives on morphometric characteristics, mineral content and bone strength of tibia in Ross broiler chickens. Glob Vet 2011;7:315-22. |
49 | Zhang HY, Majdeddin M, Gaublomme D, et al. 25-hydroxycholecalciferol reverses heat induced alterations in bone quality in finisher broilers associated with effects on intestinal integrity and inflammation. J Anim Sci Biotechnol 2021;12:104. https://doi.org/10.1186/s40104-021-00627-6 DOI |
50 | Irwin R, Raehtz S, Parameswaran N, McCabe LR. Intestinal inflammation without weight loss decreases bone density and growth. Am J Physiol Regul Integr Comp Physiol 2016;311: R1149-57. https://doi.org/10.1152/ajpregu.00051.2016 DOI |
51 | Devi SM, Lee KY, Kim IH. Analysis of the effect of dietary protected organic acid blend on lactating sows and their piglets. Rev Bras Zootec 2016;45:39-47. https://doi.org/10.1590/S1806-92902016000200001 DOI |
52 | Vieira EL, Leonel AJ, Sad AP, et al. Oral administration of sodium butyrate attenuates inflammation and mucosal lesion in experimental acute ulcerative colitis. J Nutr Biochem 2012;23:430-6. https://doi.org/10.1016/j.jnutbio.2011.01.007 DOI |
53 | Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, Teitelbaum SL. TNF-alpha induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest 2000;106:1481-8. https://doi.org/10.1172/jci11176 DOI |
54 | Liem A, Pesti GM, Edwards HM. The effect of several organic acids on phytate phosphorus hydrolysis in broiler chicks. Poult Sci 2008;87:689-93. https://doi.org/10.3382/ps.2007-00256 DOI |
55 | Shidara K, Inaba M, Okuno S, et al. Serum levels of TRAP5b, a new bone resorption marker unaffected by renal dysfunction, as a useful marker of cortical bone loss in hemodialysis patients. Calcified Tissue Int 2008;82:278-87. https://doi.org/10.1007/s00223-008-9127-4 DOI |
56 | Schwarzer M, Makki K, Storelli G, et al. Lactobacillus plantarum strain maintains growth of infant mice during chronic under-nutrition. Science 2016;351:854-7. https://doi.org/10.1126/science.aad8588 DOI |
57 | Abdel-Fattah SA, El-Sanhoury MH, El-Mednay NM, Abdel-Azeem F. Thyroid activity, some blood constituents, organs morphology and performance of broiler chicks fed supplemental organic acids. Int J Poult Sci 2008;7:215-22. https://doi.org/10.3923/ijps.2021.224.230 DOI |
![]() |