Effect of Dietary Bacillus coagulans and Different Forms of Zinc on Performance, Intestinal Microbiota, Carcass and Meat Quality of Broiler Chickens

Abstract

A total of 288-day-old male broilers were allocated to six dietary treatments to evaluate the effects of zinc source and Bacillus coagulans supplements and their interaction on growth, intestinal microbial population, carcass traits and meat quality in broiler chickens. Three levels of dietary supplemental Zn source (100 mg/kg of DM diet zinc oxide, 25 and 50 mg/kg of diet zinc oxide nanoparticles (Zn-nan)) and two levels of B. coagulans (0 and 100 mg/kg of diet) were combined as a completely randomised design with a 3 × 2 factorial arrangement. B. coagulans increased the body weight gain, body weight and feed conversion ratio. The lactic acid producing bactereia of ileal were increased by B. coagulans supplementation, and its coliform count was decreased by Zn-nan in a dose-dependent manner. The B. coagulans increased the relative weights of legs and proventriculus and reduced weights of livers, abdominal fat and meat thiobarbituric acid (TBA) value. Likewise, dietary B. coagulans increased pH, yellowness and lightness values of leg muscles. Birds fed Zn-nan50 had lower liver weight, TBA and cooking loss and higher yellowness values than chicks fed ZnO-100. In conclusion, the dietary supplementation with B. coagulans improved broiler performance, microbial population and meat quality. The Zn-nan in lower dose could be a good substitution in mineral premix instead of zinc oxide. In addition, the Zn-nan improved intestinal microbial population, carcass characteristics and oxidative stability of chicken meat; however, the combination of two levels of Zn-nan with B. coagulans did not vary the measured parameters.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2

References

  1. 1.

    Abbasvali M, Shahram Shekarforoush S, Aminlari M, Ebrahimnejad H (2012) Effects of medium-voltage electrical stimulation on postmortem changes in fat-tailed sheep. J Food Sci 77:47–53. https://doi.org/10.1111/j.1750-3841.2011.02463.x

    CAS  Article  Google Scholar 

  2. 2.

    Abd-El-Samee DL, El-Wardany I, Nematallah GA, Abo-El-Azab OM (2013) Effect of dietary organic zinc and prebiotic on productive performance and immune response of growing quails. Iranian J Appl Anim Sci 3:761–767

    CAS  Google Scholar 

  3. 3.

    Abdulla NR, Mohd Zamri AN, Sabow AB, Kareem KY, Nurhazirah S, Ling FH, Sazili AQ, Loh TC (2017) Physico-chemical properties of breast muscle in broiler chickens fed probiotics, antibiotics or antibiotic–probiotic mix. J Appl Anim Res 45:64–70. https://doi.org/10.1080/09712119.2015.1124330

    CAS  Article  Google Scholar 

  4. 4.

    Abedini M, Shariatmadari F, Torshizi K, Ahmadi H (2018) Effects of zinc oxide nanoparticles on the egg quality, immune response, zinc retention, and blood parameters of laying hens in the late phase of production. J Anim Physiol Anim Nutr 102:1–10. https://doi.org/10.1111/jpn.12871

    CAS  Article  Google Scholar 

  5. 5.

    Agboola AF, Omidiwura BRO, Iyayi EA (2016) Influence of supplemental levels of probiotic on growth response, intestinal microbiota and carcass characteristics of broilers. J Exp Agric Int 12:1–7. https://doi.org/10.9734/AJEA/2016/25082

    Article  Google Scholar 

  6. 6.

    Ahmadi F, Ebrahimnezhad Y, Sis NM, Ghiasi J (2013) The effects of zinc oxide nanoparticles on performance, digestive organs and serum lipid concentrations in broiler chickens during starter period. Int J Biosci 3:23–29. https://doi.org/10.12692/ijb/13.5.457-463

    CAS  Article  Google Scholar 

  7. 7.

    Ajuwon KM (2015) Toward a better understanding of mechanisms of probiotics and prebiotics action in poultry species. J Appl Poult Res 25:277–283. https://doi.org/10.3382/japr/pfv074

    Article  Google Scholar 

  8. 8.

    Alagawany M, El-Hack MEA, Farag MR, Sachan S, Karthik K, Dhama K (2018) The use of probiotics as eco-friendly alternatives for antibiotics in poultry nutrition. Environ Sci Pollut Res 25:‌1–8. https://doi.org/10.1007/s11356-018-1687-x, 10611, 10618

  9. 9.

    Ashida H, Kanazawa K, Minamoto S, Danno GI, Natake M (1987) Effect of orally administered secondary autoxidation products of linoleic acid on carbohydrate metabolism in rat liver. Arch Biochem Biophys 259:114–123. https://doi.org/10.1016/0003-9861(87)90476-0

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Awad WA, Ghareeb K, Abdel-Raheem S, Bohm J (2009) Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult Sci 88:49–56. https://doi.org/10.3382/ps.2008-00244

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Berri C, Wacrenier N, Millet N, Bihan-Duval EL (2001) Effect of selection for improved body composition on muscle and meat characteristics of broilers from experimental and commercial lines. Poult Sci 80:833–838. https://doi.org/10.1093/ps/80.7.833

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Bertrama HC, Andersena HJ, Karlssona AH, Hornc P, Hedegaardc J, Norgaardb L, Engelsenb SB (2003) Prediction of technological quality (cooking loss and Napole Yield) of pork based on fresh meat characteristics. Meat Sci 65:707–712. https://doi.org/10.1016/S0309-1740(02)00272-3

    Article  Google Scholar 

  13. 13.

    Beuge JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310. https://doi.org/10.1016/S0076-6879(78)52032-6

  14. 14.

    Castellini C, Mugnai C, Dal Bosco A (2002) Effect of organic production system on broiler carcass and meat quality. Meat Sci 60:219–225. https://doi.org/10.1016/S0309-1740(01)00124-3

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Chen H, Dong X, Yao Z, Xu B, Zhen S, Li C, Li X (2012) Effects of prechilling parameters on water-holding capacity of chilled pork and optimization of prechilling parameters using response surface methodology. J Anim Sci 90:2836–2841. https://doi.org/10.2527/jas.2011-4239

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Christensen LB (2003) Drip loss sampling in porcine m. longissimus dorsi. Meat Sci 63:469–477. https://doi.org/10.1016/S0309-1740(02)00106-7

    Article  PubMed  Google Scholar 

  17. 17.

    Clavijo V, Florez MJV (2018) The gastrointestinal microbiome and its association with the control of pathogens in broiler chicken production: a review. Poult Sci 97:1006–1021. https://doi.org/10.3382/ps/pex359

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Dieck H, Döring F, Roth HP, Daniel H (2003) Changes in rat hepatic gene expression in response to zinc deficiency as assessed by DNA arrays. J Nutr 133:1004–1010. https://doi.org/10.1093/jn/133.4.1004

    Article  Google Scholar 

  19. 19.

    Dunne PG, Monahan FJ, O’Mara FP, Moloney AP (2009) Colour of bovine subcutaneous adipose tissue: a review of contributory factors, associations with carcass and meat quality and its potential utility in authentication of dietary history. Meat Sci 81:28–45. https://doi.org/10.1016/j.meatsci.2008.06.013

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Eid YZ, Ohtsuka A, Hayashi K (2003) Tea polyphenols reduce glucocorticoid-induced growth inhibition and oxidative stress in broiler chickens. Br Poult Sci 44:127–132. https://doi.org/10.1080/0007166031000085427

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Erener G, Ocak N, Altop A, Cankaya S, Aksoy HM, Ozturk E (2011) Growth performance, meat quality and caecal coliform bacteria count of broiler chicks fed diet with green tea extract. Asian-Australas J Anim Sci 24:1128–1135. https://doi.org/10.5713/ajas.2011.10434

    CAS  Article  Google Scholar 

  22. 22.

    Fathi M (2016) Effects of zinc oxide nanoparticles supplementation on mortality due to ascites and performance growth in broiler chickens. Iranian J Appl Anim Sci 6:389–394

    CAS  Google Scholar 

  23. 23.

    Faustman C, Sun Q, Mancini R, Suman SP (2010) Myoglobin and lipid oxidation interactions: mechanistic bases and control. Meat Sci 86:86–94. https://doi.org/10.1016/j.meatsci.2010.04.025

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Froning GW (1995) Color of poultry meat. Poult Avian Biol Res 6:‌83–‌93

    Google Scholar 

  25. 25.

    Ganjigohari S, Ziaei N, Ramzani Ghara A, Tasharrofi S (2018) Effects of nanocalcium carbonate on egg production performance and plasma calcium of laying hens. J Anim Physiol Anim Nutr 102:‌225–‌232. https://doi.org/10.1111/jpn.12731

    CAS  Article  Google Scholar 

  26. 26.

    Gray JI, Gomaa EA, Buckley DJ (1996) Oxidative quality and shelf life of meats. Meat Sci 43:111–123. https://doi.org/10.1016/0309-1740(96)00059-9

    Article  Google Scholar 

  27. 27.

    Hood RL (1984) Cellular and biochemical aspects of fat deposition in the broiler chicken. World's Poult Sci J 40:160–169

    Article  Google Scholar 

  28. 28.

    Hossain MM, Begum M, Kim IH (2015) Effect of Bacillus subtilis, Clostridium butyricum and Lactobacillus acidophilus endospores on growth performance, nutrient digestibility, meat quality, relative organ weight, microbial shedding and excreta noxious gas emission in broilers. Vet Med 60:77–86

    CAS  Article  Google Scholar 

  29. 29.

    Hung AT, Lin SY, Yang TY, Chou CK, Liu HC, Lu JJ, Wang B, Chen SY, Lien TF (2012) Effects of Bacillus coagulans ATCC 7050 on growth performance, intestinal morphology, and microflora composition in broiler chickens. Anim Prod Sci 52:874–879. https://doi.org/10.1071/AN11332

    CAS  Article  Google Scholar 

  30. 30.

    Jang A, Liu XD, Shin MH, Lee BD, Lee SK, Lee JH, Jo C (2008) Antioxidative potential of raw breast meat from broiler chicks fed a dietary medicinal herb extract mix. ‌Poult Sci 87:2382–2389. https://doi.org/10.3382/ps.2007-00506

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    La Fata G, Weber P, Mohajeri MH (2018) Probiotics and the gut immune system: indirect regulation. Probiotics Antimicrob Proteins 10:11–21. https://doi.org/10.1007/s12602-017-9322-6

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Ladeira MM, Santarosa LC, Chizzotti ML, Ramos EM, Neto OM, Oliveira DM, Carvalho JR, Lopes LS, Ribeiro JS (2014) Fatty acid profile, color and lipid oxidation of meat from young bulls fed ground soybean or rumen protected fat with or without monensin. Meat Sci 96:597–605. https://doi.org/10.1016/j.meatsci.2013.04.062

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Liu L, Ni X, Zeng D, Wang H, Jing B, Yin Z, Pan K (2017) Effect of a dietary probiotic, Lactobacillus johnsonii BS15, on growth performance, quality traits, antioxidant ability, and nutritional and flavour substances of chicken meat. Anim Prod Sci 57:920–926. https://doi.org/10.1071/AN15344

    CAS  Article  Google Scholar 

  34. 34.

    Liu ZH, Lu L, Li SF, Zhang LY, Xi L, Zhang KY, Luo XG (2011) Effects of supplemental zinc source and level on growth performance, carcass traits, and meat quality of broilers. Poult Sci 90:1782–1790. https://doi.org/10.3382/ps.2010-01215

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Liu ZH, Lu L, Wang RL, Lei HL, Li SF, Zhang LY, Luo XG (2015) Effects of supplemental zinc source and level on antioxidant ability and fat metabolism-related enzymes of broilers. Poult Sci 94:2686–2694. https://doi.org/10.3382/ps/pev251

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Mancini RA, Hunt MC (2005) Current research in meat color. Meat Sci 71:100–121. https://doi.org/10.1016/j.meatsci.2005.03.003

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Mao SY, Lien TF (2017) Effects of nanosized zinc oxide and γ-polyglutamic acid on eggshell quality and serum parameters of aged laying hens. Arch Anim Nutr 71:373–383. https://doi.org/10.1080/1745039X.2017.1355600

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Mohammadi V, Ghazanfari S, Mohammadi-Sangcheshmeh A, Nazaran MH (2015) Comparative effects of zinc-nano complexes, zinc-sulphate and zinc-methionine on performance in broiler chickens. Br Poult Sci 56:486–493. https://doi.org/10.1080/00071668.2015.1064093

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Morrill K, May K, Leek D, Langland N, Jeane LD, Ventura J, Skubisz C, Scherer S, Lopez E, Crocker E, Peters R (2013) Spectrum of antimicrobial activity associated with ionic colloidal silver. J Altern Complement Med 19:224–231. https://doi.org/10.1089/acm.2011.0681

    Article  PubMed  Google Scholar 

  40. 40.

    Nielsen F, Mikkelsen BB, Nielsen JB, Andersen HR, Grandjean P (1997) Plasma malondialdehyde as biomarker for oxidative stress: reference interval and effects of life-style factors. Clin Chem 43:1209–1214

    CAS  Article  Google Scholar 

  41. 41.

    Nollet L, Van der Klis JD, Lensing M, Spring P (2007) The effect of replacing inorganic with organic trace minerals in broiler diets on productive performance and mineral excretion. J Appl Poult Res 16:592–597. https://doi.org/10.3382/japr.2006-00115

    CAS  Article  Google Scholar 

  42. 42.

    Onenc A, Kaya A (2004) The effects of electrical stunning and percussive captive bolt stunning on meat quality of cattle processed by Turkish slaughter procedures. Meat Sci 66:809–815. https://doi.org/10.1016/S0309-1740(03)00191-8

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Park JH, Kim IH (2014) Supplemental effect of probiotic Bacillus subtilis B2A on productivity, organ weight, intestinal Salmonella microflora, and breast meat quality of growing broiler chicks. Poult Sci 93:2054–2059. https://doi.org/10.3382/ps.2013-03818

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Raharjo S, Sofos JN (1993) Methodology for measuring malonaldehyde as a product of lipid peroxideation in muscle tissues: a review. Meat Sci 35:145–169. https://doi.org/10.1016/0309-1740(93)90046-K

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Santoso U, Tanaka K, Ohtani S (1995) Effect of dried Bacillus subtilis culture on growth, body composition and hepatic lipogenic enzyme activity in female broiler chicks. Br J Nutr 74:523–529

    CAS  Article  Google Scholar 

  46. 46.

    Scholz-Ahrens KE, Ade P, Marten B, Weber P, Timm W, Aςil Y, Gluer CC, Schrezenmeir J (2007) Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content, and bone structure. J Nutr 137(3):838–846. https://doi.org/10.1093/jn/137.3.838S

    Article  Google Scholar 

  47. 47.

    Selim NA, Amira M, Khosht AR, El-Hakim AA (2014) Effect of sources and inclusion levels of zinc in broiler diets containing different vegetable oils during summer season conditions on meat quality. Int J Poult Sci 13:619–626 https://scialert.net/abstract/?doi=ijps.2014.619.626

    CAS  Article  Google Scholar 

  48. 48.

    Shah M, Zaneb H, Masood S, Khan R, Ashraf S, Sikandar A, Rehman HFU, Rehman HU (2018) Effect of dietary supplementation of zinc and multi-microbe probiotic on growth traits and alteration of intestinal architecture in broiler. Probiotics Antimicrob Proteins:1–7. https://doi.org/10.1007/s12602-018-9424-9

  49. 49.

    Sinha R, Karan R, Sinha A, Khare SK (2011) Interaction and nanotoxic effect of ZnO and ag nanoparticles on mesophilic and halophilic bacterial cells. Bioresour Technol 102:1516–1520. https://doi.org/10.1016/j.biortech.2010.07.117

    CAS  Article  PubMed  Google Scholar 

  50. 50.

    Sinnhuber RO, Yu TC (1958) 2-Thiobarbituric acid method for the measurement of rancidity in fishery products. II. The quantitative determination of malonaldehyde. Food Technol 12:9–12

    CAS  Google Scholar 

  51. 51.

    Soetan KO, Olaiya CO, Oyewole OE (2010) The importance of mineral elements for humans, domestic animals and plants—a review. Afr J Food Sci 4:200–222

    CAS  Google Scholar 

  52. 52.

    Tatli Seven P, Seven I, Gul Baykalir B, Iflazoglu Mutlu S, Salem AZ (2018) Nanotechnology and nano-propolis in animal production and health: an overview. Ital J Anim Sci 17:1–10. https://doi.org/10.1080/1828051X.2018.1448726

    Article  Google Scholar 

  53. 53.

    Tsai YH, Mao SY, Li MZ, Huang JT, Lien TF (2016) Effects of nanosize zinc oxide on zinc retention, eggshell quality, immune response and serum parameters of aged laying hens. Anim Feed Sci Technol 213:99–107. https://doi.org/10.1016/j.anifeedsci.2016.01.009

    CAS  Article  Google Scholar 

  54. 54.

    Vinderola CG, Gueimonde M, Delgado T, Reinheimer JA, De Los Reyes-Gavilan CG (2000) Characteristics of carbonated fermented milk and survival of probiotic bacteria. Int Dairy J 10:213–220. https://doi.org/10.1016/S0958-6946(00)00031-5

    CAS  Article  Google Scholar 

  55. 55.

    Wang C, Wang MQ, Ye SS, Tao WJ, Du YJ (2011) Effects of copper-loaded chitosan nanoparticles on growth and immunity in broilers. Poult Sci 90:2223–2228. https://doi.org/10.3382/ps.2011-01511

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    Wealleans AL, Sirukhi M, Egorov IA (2017) Performance, gut morphology and microbiology effects of a Bacillus probiotic, avilamycin and their combination in mixed grain broiler diets. Brit Poult Sci 58:‌523–529. https://doi.org/10.1080/00071668.2017.1349298, 523

  57. 57.

    Wu Y, Shao Y, Song B, Zhen W, Wang Z, Guo Y, Shahid MS, Nie W (2018) Effects of Bacillus coagulans supplementation on the growth performance and gut health of broiler chickens with Clostridium perfringens-induced necrotic enteritis. J Anim Sci Biotechnol 9:‌1–‌9. https://doi.org/10.1186/s40104-017-0220-2

    CAS  Article  Google Scholar 

  58. 58.

    Yang XJ, Sun XX, Li CY, Wu XH, Yao JH (2011) Effects of copper, iron, zinc, and manganese supplementation in a corn and soybean meal diet on the growth performance, meat quality, and immune responses of broiler chickens. J Appl Poult Res 20:263–271. https://doi.org/10.3382/japr.2010-00204

    CAS  Article  Google Scholar 

  59. 59.

    Yang Z, Xie C (2006) Zn+2 release from zinc and zinc oxide in simulated uterine solution. Colloids Surf B Biointerfaces 47:‌140–‌145. https://doi.org/10.1016/j.colsurfb.2005.12.007

    CAS  Article  PubMed  Google Scholar 

  60. 60.

    Zhang ZF, Kim IH (2014) Effects of multistrain probiotics on growth performance, apparent ileal nutrient digestibility, blood characteristics, cecal microbial shedding, and excreta odor contents in broilers. Poult Sci 93:364–370. https://doi.org/10.3382/ps.2013-03314

    CAS  Article  PubMed  Google Scholar 

  61. 61.

    Zhou X, Wang Y, Gu Q, Li W (2010) Effect of dietary probiotic, Bacillus coagulans, on growth performance, chemical composition, and meat quality of Guangxi yellow chicken. Poult Sci 89:588–593. https://doi.org/10.3382/ps.2009-00319

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Miss Catherine Fudge, Prestage Department of Poultry Science, North Carolina State University, and also Department of Foreign Language of Shahid Bahonar University of Kerman, for assistance in editing the English of the manuscript. We would also like to thank the anonymous editor and reviewers for their helpful suggestions for this study.

Funding

The authors gratefully acknowledge the Shahid Bahonar University of Kerman for financial support.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Mohammad Khajeh Bami.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

All institutional and national guidelines for the care and use of laboratory animals were followed.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Khajeh Bami, M., Afsharmanesh, M. & Ebrahimnejad, H. Effect of Dietary Bacillus coagulans and Different Forms of Zinc on Performance, Intestinal Microbiota, Carcass and Meat Quality of Broiler Chickens. Probiotics & Antimicro. Prot. 12, 461–472 (2020). https://doi.org/10.1007/s12602-019-09558-1

Download citation

Keywords

  • Broiler
  • Growth performance
  • Microbial population
  • B. coagulans
  • Zinc oxide nanoparticles