Dose-dependent effects of probiotic supplementation on bone characteristics and mineralisation in meat-type female turkeys
E. Tomaszewska A F , M. Kwiecień B , P. Dobrowolski C , R. Klebaniuk B , S. Muszyński D , M. Olcha B , T. Blicharski E and E. R. Grela B
+ Author Affiliations
- Author Affiliations
A Department of Animal Physiology, Faculty of Veterinary Medicine, University of Life Sciences in Lublin, 20-950 Lublin, Poland.
B Department of Bromatology and Food Physiology, University of Life Sciences in Lublin, 20-950 Lublin, Poland.
C Department of Comparative Anatomy and Anthropology, Maria Curie-Skłodowska University, 20-033 Lublin, Poland.
D Department of Physics, Faculty of Production Engineering, University of Life Sciences in Lublin, 20-950 Lublin, Poland.
E Chair and Department of Rehabilitation and Orthopaedics, Medical University in Lublin, Jaczewskiego 8, 20-090 Lublin, Poland.
F Corresponding author. Email: ewaRST@interia.pl
Animal Production Science 58(3) 507-516 https://doi.org/10.1071/AN16289
Submitted: 5 May 2016 Accepted: 8 September 2016 Published: 14 December 2016
Abstract
To evaluate the influence of the probiotic on bone tissue in female turkeys, bone mineral density and geometrical and mechanical properties of the tibia and femur were determined in a dose-dependent manner (107 colony-forming units (cfu)/g, 108 cfu/g, 109 cfu/g). No effect of the treatments on bone mass and wall thickness of femur was observed, but the administration of the probiotic resulted in the elongation and the reduction of both strengths. The increase in the cross-sectional area of the femur was dose-dependent. Probiotic supplementation at a concentration of 108 cfu/g resulted in a reduction in ultimate strength, but at a concentration of 107 cfu/g, it resulted in the enhancement of the maximum elastic strength of the tibia compared with other groups. The influence of the probiotic administration on tibia geometry was dose-dependent. No effect of the treatments on the relative bone weight and the ratio of mass to length was observed. In general, the influence of the probiotic administration on bone mineral density, bone mineral concentration, bone tissue density, and bone ash, calcium and phosphorus concentrations was dose-dependent. The investigated properties of long bones in female turkeys are affected through probiotic-supplemented diets in a dose-dependent manner. However, on the basis of densitometry, it seems that the administration of the probiotic at a higher concentration of cells is more beneficial for bone development in turkeys.
Additional keywords: BMD, bone geometry, femur, mechanical properties, probiotic, tibia.
References
Applegate TJ, Klose V, Steiner T, Ganner A, Schatzmayr G (2010) Probiotics and phytogenics for poultry: myth or reality? Journal of Applied Poultry Research 19, 194–210.| Probiotics and phytogenics for poultry: myth or reality?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvFKrs7c%3D&md5=3571aaca08dbcdf45a59ba389f7d431cCAS |
Association of Official Analytical Chemists (2012) ‘Official methods of analysis of AOAC international.’ 19th edn. (Ed. GW Latimer) (AOAC: Gaithersburg, MD)
Brakenhoff LKPM, van der Heijdeb DM, Hommesa DW, Huizingab TWJ, Fiddera HH (2010) The joint–gut axis in inflammatory bowel diseases. Journal of Crohn’s and Colitis 4, 257–268.
| The joint–gut axis in inflammatory bowel diseases.Crossref | GoogleScholarGoogle Scholar |
Chen KL, Kho WL, You SH, Yeh RH, Tang SW, Hsieh CW (2009) Effects of Bacillus subtilis var. natto and Saccharomyces cerevisiae mixed fermented feed on the enhanced growth performance of broilers. Poultry Science 88, 309–315.
| Effects of Bacillus subtilis var. natto and Saccharomyces cerevisiae mixed fermented feed on the enhanced growth performance of broilers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisV2qsrg%3D&md5=c7f7757e2f29b8770985f8857025da8eCAS |
Crespo R, Stover SM, Droual R, Chin RP, Shivaprasad HL (1999) Femoral fractures in a young male turkey breeder flock. Avian Diseases 43, 150–154.
| Femoral fractures in a young male turkey breeder flock.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M3jt1Ciuw%3D%3D&md5=ab01d83df0118570b7c2b132579f36c1CAS |
Dumont ER (2010) Bone density and the lightweight skeletons of birds. Proceedings of the Royal Society B: Biological Science 277, 2193–2198.
| Bone density and the lightweight skeletons of birds.Crossref | GoogleScholarGoogle Scholar |
EFSA (2015) Evaluation report on the analytical methods submitted in connection with the application for authorisation of a feed additive according to regulation (EC) No. 1831/2003. (The European Food Safety Authority: Parma, Italy)
Food and Agriculture Organization of the United Nations/World Health Organization (2002) Report of a Joint FAO/WHO Working Group on Drafting Guidelines for the evaluation of probiotics in food. Guidelines for evaluation of probiotics in food. London, Ontario, Canada, 2002.
Ferretti JL, Capozza RF, Mondelo N, Zanchetta JR (1993) Interrelationships between densitometric, geometric and mechanical properties of rat femora: inferences concerning mechanical regulation of bone modelling. Journal of Bone and Mineral Research 8, 1395–1399.
Fuller R (1989) Probiotics in man and animals. The Journal of Applied Bacteriology 66, 365–378.
| Probiotics in man and animals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1MzislSqsw%3D%3D&md5=1f4eecb67b42a15aa33401c508b38f4bCAS |
Glodin BR (1998) Health benefits of probiotics. British Journal of Nutrition 80, S203–S207.
Godwin JL, Grimes JL, Christensen VL, Wineland MJ (2005) Effect of dietary phosphorus and phytase levels on the reproductive performance of large white turkey breeder hens. Poultry Science 84, 485–493.
| Effect of dietary phosphorus and phytase levels on the reproductive performance of large white turkey breeder hens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisVSmsLg%3D&md5=3b38ec796a5ec95516bd1342c77bdbbfCAS |
Hancock RD, Viola R (2001) The use of micro-organisms for L-ascorbic acid production: current status and future perspectives. Applied Microbiology and Biotechnology 56, 567–576.
| The use of micro-organisms for L-ascorbic acid production: current status and future perspectives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslGgsrc%3D&md5=5448ae3e7d88780e7a10bbbe51d1a063CAS |
Hedstrom OR, Chevillaen F, Horst RL (1986) Pathology of vitamin D deficiency in growing turkeys. Veterinary Pathology 23, 485–498.
| Pathology of vitamin D deficiency in growing turkeys.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XltFCjt7o%3D&md5=eb923defd16e2d713fb329ce587b58e4CAS |
Hocking PM, Robertson GW, Nikey C (2002) Effects of dietary calcium and phosphorus on mineral retention, growth, feed efficiency and walking ability in growing turkeys. British Poultry Science 43, 607–614.
| Effects of dietary calcium and phosphorus on mineral retention, growth, feed efficiency and walking ability in growing turkeys.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFKku7w%3D&md5=807d358641a5f26472abd5355210cfc5CAS |
Huff WE, Huff GR, Clark FD, Moore PA, Rath NC, Balog JM, Barnes DM, Erf GF, Beers KW (1999) Research on probable cause of an outbreak of field rickets in turkeys. Poultry Science 78, 1699–1702.
| Research on probable cause of an outbreak of field rickets in turkeys.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FptVSksg%3D%3D&md5=d1e36f9950d55aaece6e084575ddb830CAS |
Jankowski J, Lichtorowicz K, Zduńczyk Z, Juśkiewicz J (2012) The effect of different dietary sodium levels on blood mineral concentrations and tibia mineralization in turkeys. Polish Journal of Veterinary Sciences 15, 227–232.
| The effect of different dietary sodium levels on blood mineral concentrations and tibia mineralization in turkeys.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVansLfO&md5=7be5b205323724a251adc999d8f8bf96CAS |
Julian RJ (2005) Production and growth related disorders and other metabolic diseases of poultry: a review. Veterinary Journal 169, 350–369.
| Production and growth related disorders and other metabolic diseases of poultry: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsFGqtL8%3D&md5=4a178653af79f74aa79043491bc66321CAS |
Kozłowski K, Jankowski J, Jeroch H (2010) Efficacy of Escherichia coli-derived phytase on performance, bone mineralization and nutrient digestibility in meat-type turkeys. Veterinarija ir Zootechnika 52, 59–65.
Kumari A, Catanzaro R, Marotta F (2011) Clinical importance of lactic acid bacteria: a short review. Acta Biomedica 82, 177–180.
Lan GQ, Abdullah N, Jalaludin S, Ho YW (2002) Efficacy of supplementation of a phytase-producing bacterial culture on the performance and nutrient use of broiler chickens fed corn-soybean meal diets. Poultry Science 81, 1522–1532.
| Efficacy of supplementation of a phytase-producing bacterial culture on the performance and nutrient use of broiler chickens fed corn-soybean meal diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xotlantb4%3D&md5=df4a1216eaa3060e740e664f28c27e47CAS |
Lievers WB, Lee V, Arsenault SM, Waldman SD, Pilkey AK (2007) Specimen size effect in the volumetric shrinkage of cancellous bone measured at two level of dehydration. Journal of Biomechanics 40, 1903–1909.
| Specimen size effect in the volumetric shrinkage of cancellous bone measured at two level of dehydration.Crossref | GoogleScholarGoogle Scholar |
Matar C, Amiot J, Savoie L, Goulet J (1996) The effect of milk fermentation by Lactobacillus helveticus on the release of peptides during in vitro digestion. Journal of Dairy Science 79, 971–979.
| The effect of milk fermentation by Lactobacillus helveticus on the release of peptides during in vitro digestion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xktlaltb0%3D&md5=ca72a80800077b4238a70acc6d237b0fCAS |
McCabe LR, Irwin R, Schaefer L, Britton RA (2013) Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. Journal of Cellular Physiology 228, 1793–1798.
| Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtF2mtLs%3D&md5=21966a9cab47e7b7ed64990c3f991456CAS |
Mutuş R, Kocabali N, Alp M, Acar N, Eren M, Gezen ŞŞ (2006) The effect of dietary probiotic supplementation on tibial bone characteristics and strength in broilers. Poultry Science 85, 1621–1625.
| The effect of dietary probiotic supplementation on tibial bone characteristics and strength in broilers.Crossref | GoogleScholarGoogle Scholar |
National Research Council (NRC) (1994) ‘Nutrients requirements of poultry.’ 9th edn. (National Academic Press: Washington, DC)
Olson WG, Dziuk HE, Walser MM, Hanlon GF, Waibel PE, Stevens JB, Jorgensen NA (1981) Field rickets in turkey poults: biochemical findings. Avian Diseases 25, 550–554.
| Field rickets in turkey poults: biochemical findings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXkt1eht7c%3D&md5=2eec4f25cb2469396ce92779e9b01c81CAS |
Onyango EM, Hester PY, Stroshine R, Adeola O (2003) Bone densitometry as an indicator of percentage tibia ash in broiler chicks fed varying dietary calcium and phosphorus levels. Poultry Science 82, 1787–1791.
| Bone densitometry as an indicator of percentage tibia ash in broiler chicks fed varying dietary calcium and phosphorus levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvFygsbs%3D&md5=459dd670401f393b7acd08e4fd6c74a8CAS |
Plavnik I, Scott ML (1980) Effects of additional vitamins, minerals or brewer’s yeast upon leg weaknesses in broiler chickens. Poultry Science 59, 459–464.
| Effects of additional vitamins, minerals or brewer’s yeast upon leg weaknesses in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXht1Oms74%3D&md5=462a0498e66debce9a48f105c40df5ccCAS |
Qian H, Kornegay ET, Denbow DM (1997) Utilization of phytate phosphorus and calcium as influenced by microbial phytase, cholecalciferol, and the calcium: total phosphorus ratio in broiler diets. Poultry Science 76, 37–46.
| Utilization of phytate phosphorus and calcium as influenced by microbial phytase, cholecalciferol, and the calcium: total phosphorus ratio in broiler diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsVOisr4%3D&md5=617ac2761634d2d3f6deadb54e0ae0a2CAS |
Rama Rao SV, Raju MVLN, Reddy MR (2007) Performance of broiler chicks fed high levels of cholecalciferol in diets containing sub-optimal levels of calcium and non-phytate phosphorus. Animal Feed Science and Technology 134, 77–88.
| Performance of broiler chicks fed high levels of cholecalciferol in diets containing sub-optimal levels of calcium and non-phytate phosphorus.Crossref | GoogleScholarGoogle Scholar |
Rantala M, Nurmi E (1973) Prevention of the growth of Salmonella in chicks by the flora of the alimentary tract of chickens. British Poultry Science 14, 627–630.
| Prevention of the growth of Salmonella in chicks by the flora of the alimentary tract of chickens.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2c%2FkslKrtw%3D%3D&md5=72c4318b1f71555786b29990c125cd7cCAS |
Rath NC, Huff GR, Huff WE, Balog JM (2000) Factors regulating bone maturity and strength in poultry. Poultry Science 79, 1024–1032.
| Factors regulating bone maturity and strength in poultry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhvFersLk%3D&md5=e7b2c67568dde120236ab6c7ed66c1d5CAS |
Roberson KD, Klunzinger MW, Charbeneau RA (2004) Benefit of feeding dietary calcium and nonphytate phosphorus levels above national research council recommendations to tom turkeys in the growing-finishing phases. Poultry Science 83, 689–695.
| Benefit of feeding dietary calcium and nonphytate phosphorus levels above national research council recommendations to tom turkeys in the growing-finishing phases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjs1WnsLw%3D&md5=05f87549f6fecb79381358c521226e9eCAS |
Selle PH, Ravindran V (2007) Microbial phytase in poultry nutrition. Animal Feed Science and Technology 135, 1–41.
| Microbial phytase in poultry nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkt1artb8%3D&md5=10c873cc2a2fa70b4c8c35c36f7ce39aCAS |
Sjögren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, Bäckhed F, Ohlsson C (2012) The gut microbiota regulates bone mass in mice. Journal of Bone and Mineral Research 27, 1357–1367.
| The gut microbiota regulates bone mass in mice.Crossref | GoogleScholarGoogle Scholar |
Śliwa E, Radzki RP, Puzio I (1996) Osteochondrosis and tibial dyschondroplasia in chickens, pigs and foals. Medycyna Weterynaryjna 52, 156–159.
Tatara MR, Brodzki A, Krupski W, Śliwa E, Silmanowicz P, Majcher P, Pierzynowski SG, Studziński T (2005) Effect of alpha-ketoglutarate (AKG) on bone homeostasis and plasma amino acids in turkeys. Poultry Science 84, 1604–1609.
| Effect of alpha-ketoglutarate (AKG) on bone homeostasis and plasma amino acids in turkeys.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGltrvO&md5=2e3f3a6ee41c10bfaf51109f019d1b1bCAS |
Tatara MR, Śliwa E, Krupski W, Brodzki A, Pasternak K (2006) Ornithine alpha-ketoglutarate increases mineralization and mechanical properties of tibia in turkeys. Bone 39, 100–105.
| Ornithine alpha-ketoglutarate increases mineralization and mechanical properties of tibia in turkeys.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xls1ejsbw%3D&md5=cc20c40316071a6196d9db71474582ecCAS |
Tatara MR, Krupski W, Jankowski M, Zduńczyk Z, Jankowski J, Studziński T (2011) Effects of dietary calcium content and vitamin D source on skeletal properties in growing turkeys. British Poultry Science 52, 718–729.
| Effects of dietary calcium content and vitamin D source on skeletal properties in growing turkeys.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtFChtw%3D%3D&md5=d393e2784c3e9e21d5f4f8070d8c091dCAS |
Tatara MR, Krupski W, Kozłowski K, Drażbo A, Jankowski J (2015) Effects of administration of four different doses of Escherichia coli phytase on femur properties of 16-week-old turkeys. BMC Veterinary Research 11, 69
| Effects of administration of four different doses of Escherichia coli phytase on femur properties of 16-week-old turkeys.Crossref | GoogleScholarGoogle Scholar |
Tomaszewska E, Dobrowolski P, Kostro K, Jakubczak A, Taszkun I, Jaworska-Adamu J, Żmuda A, Rycerz K, Muszyński S (2015) The effect of HMB and 2-Ox administered during pregnancy on bone properties in primiparous and multiparous minks (Neivison vison). Bulletin of the Veterinary Institute in Pulawy 59, 563–568.
| The effect of HMB and 2-Ox administered during pregnancy on bone properties in primiparous and multiparous minks (Neivison vison).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1KgtLg%3D&md5=86a4097701e289853263e04ef5e4116cCAS |
Tomaszewska E, Dobrowolski P, Kwiecień M, Wawrzyniak A, Burmańczuk N (2016) Comparison of the effect of a standard inclusion level of inorganic zinc to organic form at lowered level on bone development in growing male Ross broiler chickens. Annals of Animal Science 16, 1–13.
| Comparison of the effect of a standard inclusion level of inorganic zinc to organic form at lowered level on bone development in growing male Ross broiler chickens.Crossref | GoogleScholarGoogle Scholar |
Waldenstedt L (2006) Nutritional factors of importance for optimal leg health in broilers: a review. Animal Feed Science and Technology 126, 291–307.
| Nutritional factors of importance for optimal leg health in broilers: a review.Crossref | GoogleScholarGoogle Scholar |
Walter J (2008) Ecological role of Lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Applied and Environmental Microbiology 74, 4985–4996.
| Ecological role of Lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVehu7jF&md5=62e10a6e0d2dbba56406d02845507e33CAS |
Webster AB (2004) Welfare implications of avian osteoporosis. Poultry Science 83, 184–192.
| Welfare implications of avian osteoporosis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c%2FovFygsQ%3D%3D&md5=5c21a0eed3ebbf67a2758a390e3acd98CAS |
Wu HJ, Wu E (2012) The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes 3, 4–14.
| The role of gut microbiota in immune homeostasis and autoimmunity.Crossref | GoogleScholarGoogle Scholar |
