Effect of in Ovo Inoculation of Bifidobacterium spp. on Growth Performance, Thyroid Activity, Ileum Histomorphometry, and Microbial Enumeration of Broilers

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Abstract

Early colonization by beneficial bacteria stimulates the function and development of the digestive tract, on which the performance and vitality of broilers rely. This experiment evaluated the effects of in ovo injection of bifidobacteria on the performance, thyroid activity, bacterial enumeration, and ileal histomorphometry of broiler chickens. A total of 360 fertile eggs were inoculated into the yolk sac, on day 17 of embryogenesis, and allocated to six experimental groups: negative control (not injected, G1), positive control (injected with sterilized distilled water, G2), and groups inoculated with 2 × 108 CFU of Bifidobacterium bifidum, G3; B. animalis, G4; B. longum, G5; or B. infantis, G6. The results revealed an increase (P < 0.01) in body weight and weight gain in all treated groups increases of at least 5.38 and 8.27%, respectively, compared with the control. Feed consumption was not affected during all experimental periods, while the feed conversion ratio (FCR) was enhanced (P < 0.01) only for the overall experimental period (1–28 days of age). The G3 birds recorded the lowest FCR (1.38), while the highest was observed in G1 birds (1.57). Serum concentrations of thyroxin and triiodothyronine were elevated (P < 0.05) with probiotic inoculation. The antioxidant status and immune response of bifidobacteria injected birds were improved; the serum contents of superoxide dismutase and immunoglobulins Y, M, and A were increased (P < 0.05 and P < 0.01), while the malondialdehyde content was decreased (P < 0.01). Ileal architecture was improved in the bifidobacteria treated groups; the highest values of villus height and the villus height/crypt depth ratio were recorded in G3 (936.6 and 11.80) compared with those of G1 (537.1 and 6.93). Moreover, ileal lactic acid bacteria and Bifidobacterium spp. counts increased by at least 10.64 and 51.75%, while total coliform and bacterial counts reduced by at least 15.46 and 15.18%, respectively, compared with those of the control. In conclusion, all tested strains of bifidobacteria enhanced broiler growth performance, ileal function, and thyroid hormone metabolism without obvious differences among them.

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References

  1. 1.

    Estrada A, Wilkie DC, Drew M (2001) Administration of Bifidobacterium bifidum to chicken broilers reduces the number of carcass condemnations for cellulitis at the abattoir. J Appl Poult Res 10:329–334

    Google Scholar 

  2. 2.

    Abd El-Moneim EA, El-Wardany I, Abu-Taleb AM, Wakwak MM, Ebeid TA, Saleh AA (2019) Assessment of in ovo administration of Bifidobacterium bifidum and Bifidobacterium longum on performance, ileal histomorphometry, blood hematological, and biochemical parameters of broilers. Probiotics Antimicrob Proteins:In Press:1–12. https://doi.org/10.1007/s12602-019-09549-2

  3. 3.

    Williams C, Witherly S, Buddington R (1994) Influence of dietary neosugar on selected bacterial groups of the human faecal microbiota. Microb Ecol Health Dis 7:91–97

    CAS  Google Scholar 

  4. 4.

    Saleh A, Hayashi K, Ijiri D, Ohtsuka A (2014) Beneficial effects of Aspergillus awamori in broiler nutrition. Worlds Poult Sci J 70:857–864

    Google Scholar 

  5. 5.

    Fathi M, Al-Homidan I, Al-Dokhail A, Ebeid T, Abou-Emera O, Alsagan A (2018) Effects of dietary probiotic (Bacillus subtilis) supplementation on productive performance, immune response and egg quality characteristics in laying hens under high ambient temperature. Ital J Anim Sci 17:804–814

    CAS  Google Scholar 

  6. 6.

    Banerjee G, Ray AK (2017) The advancement of probiotics research and its application in fish farming industries. Res Vet Sci 115:66–77

    PubMed  CAS  Google Scholar 

  7. 7.

    Dankowiakowska A, Kozłowska I, Bednarczyk M (2013) Probiotics, prebiotics and snybiotics in poultry–mode of action, limitation, and achievements. J Centr Eur Agri 14:467–478

    Google Scholar 

  8. 8.

    Abe F, Ishibashi N, Shimamura S (1995) Effect of administration of bifidobacteria and lactic acid bacteria to newborn calves and piglets. J Dairy Sci 78:2838–2846

    PubMed  CAS  Google Scholar 

  9. 9.

    Gibson G, Wang X (1994) Regulatory effects of bifidobacteria on the growth of other colonic bacteria. J Appl Bacteriol 77:412–420

    PubMed  CAS  Google Scholar 

  10. 10.

    Misra A, Kuila R (1992) Use of Bifidobacterium bifidum in the manufacture of bifidus milk and its antibacterial activity. Lait 72:213–220

    Google Scholar 

  11. 11.

    Touré R, Kheadr E, Lacroix C, Moroni O, Fliss I (2003) Production of antibacterial substances by bifidobacterial isolates from infant stool active against Listeria monocytogenes. J Appl Microbiol 95:1058–1069

    PubMed  Google Scholar 

  12. 12.

    Shah NP, Dave R (2002) Antimicrobial substances including bacteriocins produced by lactic acid bacteria. Biosci Microflora 21:217–223

    CAS  Google Scholar 

  13. 13.

    Chotinsky D, Lyons TP, Korudjiski N, Krusteva M (2003) Effect of lacto sacc, yea sacc and toyocerin on the performances and the colonization of E. coli in the small intestine and caeca of broiler chicken. Bulg J Agri Sci 9:719–724

    Google Scholar 

  14. 14.

    Chichlowski M, Croom WJ, Edens FW, McBride BW, Qiu R, Chiang CC, Daniel LR, Havenstein GB, Koci MD (2007) Microarchitecture and spatial relationship between bacteria and ileal, cecal, and colonic epithelium in chicks fed a direct-fed microbial, primalac, and salinomycin. Poult Sci 86:1121–1132

    PubMed  CAS  Google Scholar 

  15. 15.

    Hashemzadeh M, Karimi T, Rahimi S, Razban V, Zahraei ST (2010) Prevention of salmonella colonization in neonatal broiler chicks by using different routes of probiotic administration in hatchery evaluated by culture and PCR techniques. J Agri Sci Technol 12:425–432

    Google Scholar 

  16. 16.

    Stefaniak T, Madej JP, Graczyk S, Siwek M, Łukaszewicz E, Kowalczyk A, Sieńczyk M, Bednarczyk M (2019) Selected prebiotics and synbiotics administered in ovo can modify innate immunity in chicken broilers. BMC Vet Res 15:105. https://doi.org/10.1186/s12917-019-1850-8

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Beck CN, McDaniel CD, Wamsley KG, Kiess AS (2019) The potential for inoculating Lactobacillus animalis and Enterococcus faecium alone or in combination using commercial in ovo technology without negatively impacting hatch and post-hatch performance. Poult Sci:In Press. https://doi.org/10.3382/ps/pez441

  18. 18.

    Abd El-Moneim AE, Sabic EM (2019) Beneficial effect of feeding olive pulp and Aspergillus awamori on productive performance, egg quality, serum/yolk cholesterol and oxidative status in laying Japanese quails. J. Anim Feed Sci 28:52–61

    Google Scholar 

  19. 19.

    Wang Y, Wu Y, Wang Y, Xu H, Mei X, Yu D, Wang Y, Li W (2017) Antioxidant properties of probiotic bacteria. Nutrients 9:521. https://doi.org/10.3390/nu9050521

    Article  PubMed Central  CAS  Google Scholar 

  20. 20.

    Sela DA, Garrido D, Lerno L, Wu S, Tan K, Eom H-J, Joachimiak A, Lebrilla CB, Mills DA (2012) Bifidobacterium longum subsp. infantis ATCC 15697 α-fucosidases are active on fucosylated human milk oligosaccharides. Appl Environ Microbiol 78:795–803

    PubMed  PubMed Central  CAS  Google Scholar 

  21. 21.

    Iskender H, Yenice G, Dokumacioglu E, Kaynar O, Hayirli A, Kaya A (2017) Comparison of the effects of dietary supplementation of flavonoids on laying hen performance, egg quality and egg nutrient profile. Br Poult Sci 58:550–556

    PubMed  CAS  Google Scholar 

  22. 22.

    Odamaki T, Horigome A, Sugahara H, Hashikura N, Minami J, J-z X, Abe F (2015) Comparative genomics revealed genetic diversity and species/strain-level differences in carbohydrate metabolism of three probiotic bifidobacterial species. Int J Genom 2015:1–12

    Google Scholar 

  23. 23.

    Ventura M, Meylan V, Zink R (2003) Identification and tracing of Bifidobacterium species by use of enterobacterial repetitive intergenic consensus sequences. Appl Environ Microbiol 69:4296–4301

    PubMed  PubMed Central  CAS  Google Scholar 

  24. 24.

    National Research Council (1994) Nutrition requirements of poultry, 9th edn. The National Academies Press, Washington, DC. https://doi.org/10.17226/2114

    Google Scholar 

  25. 25.

    Bancroft JD, Layton C (2019) The hematoxylins and eosin. In: Suvarna SK, Layton C, Bancroft JD (eds) Bancroft’s theory and practice of histological techniques, 8th edn. Churchill Livingstone, Elsevier, England, pp 126–138. https://doi.org/10.1016/B978-0-7020-6864-5.00003-7

    Google Scholar 

  26. 26.

    Mountzouris K, Tsitrsikos P, Palamidi I, Arvaniti A, Mohnl M, Schatzmayr G, Fegeros K (2010) Effects of probiotic inclusion levels in broiler nutrition on growth performance, nutrient digestibility, plasma immunoglobulins, and cecal microflora composition. Poult Sci 89:58–67

    PubMed  CAS  Google Scholar 

  27. 27.

    Feng P, Weagant SD, Grant MA, Burkhardt W (2002) Bacteriological analytical manual chapter 4: enumeration of Escherichia coli and the coliform bacteria. Food and Drug Administration, Silver Spring https://www.fda.gov/food/laboratory-methods-food/bam-4-enumeration-escherichia-coli-and-coliform-bacteria. Accessed September 2002

    Google Scholar 

  28. 28.

    Rogosa M, Mitchell JA, Wiseman RF (1951) A selective medium for the isolation and enumeration of oral and fecal lactobacilli. J Bacteriol 6:132–133

    Google Scholar 

  29. 29.

    Dave RI, Shah NP (1996) Evaluation of media for selective enumeration of Streptococcus thermophilus, Lactobacillus delbrueckii ssp. bulgaricus, Lactobacillus acidophilus, and bifidobacteria. J Dairy Sci 79:1529–1536

    PubMed  CAS  Google Scholar 

  30. 30.

    Kabir SML, Rahman MM, Rahman MB, Rahman MM, Ahmed SU (2004) The dynamics of probiotics on growth performance and immune response in broilers. Int J Poult Sci 3:361–364

    Google Scholar 

  31. 31.

    Sen S, Ingale S, Kim Y, Kim J, Kim K, Lohakare J, Kim E, Kim H, Ryu M, Kwon I (2012) Effect of supplementation of Bacillus subtilis LS 1-2 to broiler diets on growth performance, nutrient retention, caecal microbiology and small intestinal morphology. Res Vet Sci 93:264–268

    PubMed  Google Scholar 

  32. 32.

    Lan PTN, Le TB, Benno Y (2003) Impact of two probiotic Lactobacillus strains feeding on fecal lactobacilli and weight gains in chicken. J Gen Appl Microbiol 49:29–36

    PubMed  CAS  Google Scholar 

  33. 33.

    Huang M, Choi Y, Houde R, Lee J-W, Lee B, Zhao X (2004) Effects of lactobacilli and an acidophilic fungus on the production performance and immune responses in broiler chickens. Poult Sci 83:788–795

    PubMed  CAS  Google Scholar 

  34. 34.

    Wang Y, Gu Q (2010) Effect of probiotic on growth performance and digestive enzyme activity of arbor acres broilers. Res Vet Sci 89:163–167

    PubMed  CAS  Google Scholar 

  35. 35.

    Sugiharto S (2016) Role of nutraceuticals in gut health and growth performance of poultry. J Saudi Soc Agri Sci 15:99–111

    Google Scholar 

  36. 36.

    Siddiqui S, Rahman M, Islam S, Islam S, Hasan MMI, Rahman MM (2017) Biological effects of commercial enzymes, probiotics and liver tonic on live weight and hematobiochemical parameters in broiler. Int J Res Agri Sci 4:56–59

    Google Scholar 

  37. 37.

    Yazhini P, Visha P, Selvaraj P, Vasanthakumar P, Chandran V (2018) Dietary encapsulated probiotic effect on broiler serum biochemical parameters. Vet World 11:1344

    PubMed  PubMed Central  CAS  Google Scholar 

  38. 38.

    Zubillaga M, Weill R, Postaire E, Goldman C, Caro R, Boccio J (2001) Effect of probiotics and functional foods and their use in different diseases. Nut Res 21:569–579

    CAS  Google Scholar 

  39. 39.

    Saleh AA, Gálik B, Arpášová H, Capcarová M, Kalafová A, Šimko M, Juráček M, Rolinec M, Bíro D, Abudabos A (2017) Synergistic effect of feeding Aspergillus awamori and lactic acid bacteria on performance, egg traits, egg yolk cholesterol and fatty acid profile in laying hens. Ital J Anim Sci 16:132–139

    CAS  Google Scholar 

  40. 40.

    Mukherjee A, Banerjee G, Mukherjee P, Ray AK, Chandra G, Ghosh K (2019) Antibacterial substances produced by pathogen inhibitory gut bacteria in Labeo rohita: physico-chemical characterization, purification and identification through MALDI-TOF mass spectrometry. Microb Pathog 130:146–155

    PubMed  CAS  Google Scholar 

  41. 41.

    Nandi A, Banerjee G, Dan SK, Ghosh K, Ray AK (2017) Probiotic efficiency of Bacillus sp. in Labeo rohita challenged by Aeromonas hydrophila: assessment of stress profile, haemato-biochemical parameters and immune responses. Aquac Res 48:4334–4345

    CAS  Google Scholar 

  42. 42.

    Abudabos A, Alyemni A, Zakaria H (2016) Effect of two strains of probiotics on the antioxidant capacity, oxidative stress, and immune responses of salmonella-challenged broilers. Rev Bras Ciênc Avíc 18:175–180

    Google Scholar 

  43. 43.

    Higgins SE, Higgins JP, Wolfenden AD, Henderson SN, Torres-Rodriguez A, Tellez G, Hargis B (2008) Evaluation of a lactobacillus-based probiotic culture for the reduction of Salmonella enteritidis in neonatal broiler chicks. Poult Sci 87:27–31

    PubMed  CAS  Google Scholar 

  44. 44.

    Vicente JL, Torres-Rodriguez A, Higgins SE, Pixley C, Tellez G, Donoghue AM, Hargis BM (2008) Effect of a selected Lactobacillus spp.–based probiotic on Salmonella enterica serovar Enteritidis–infected broiler chicks. Avian Dis 52:143–146

    PubMed  Google Scholar 

  45. 45.

    Okanović D, Čolović R, Tasić T, Zekić V, Ikonić P (2014) The impact of probiotics additives added into diet on economic results of broilers production. J Hyg Eng Des 7:150–153

    Google Scholar 

  46. 46.

    Aluwong T, Hassan F, Dzenda T, Kawu M, Ayo J (2013) Effect of different levels of supplemental yeast on body weight, thyroid hormone metabolism and lipid profile of broiler chickens. J Vet Med Sci 75:291–298

    PubMed  CAS  Google Scholar 

  47. 47.

    Klieverik LP, Janssen SF, van Riel A, Foppen E, Bisschop PH, Serlie MJ, Boelen A, Ackermans MT, Sauerwein HP, Fliers E (2009) Thyroid hormone modulates glucose production via a sympathetic pathway from the hypothalamic paraventricular nucleus to the liver. Proc Natl Acad Sci USA 106:5966–5971

    PubMed  CAS  Google Scholar 

  48. 48.

    Lin M-Y, Yen C-L (1999) Antioxidative ability of lactic acid bacteria. J Agri Food Chem 47:1460–1466

    CAS  Google Scholar 

  49. 49.

    Popović SJ, Kostadinović LM, Puvača NM, Lević JD, Đuragić OM, Kokić BM, Čabarkapa IS, Vranješ MV (2015) Effect of synbiotic on growth and antioxidant status of blood in broiler chicken. Food Feed Res 42:163–169

    Google Scholar 

  50. 50.

    Aluwong T, Kawu M, Raji M, Dzenda T, Govwang F, Sinkalu V, Ayo J (2013) Effect of yeast probiotic on growth, antioxidant enzyme activities and malondialdehyde concentration of broiler chickens. Antioxidants 2:326–339

    PubMed  PubMed Central  CAS  Google Scholar 

  51. 51.

    Erdoğan Z, Erdoğan S, Aslantaş Ö, Celik S (2010) Effects of dietary supplementation of synbiotics and phytobiotics on performance, caecal coliform population and some oxidant/antioxidant parameters of broilers. J Anim Physiol Anim Nutr 94:e40–e48

    Google Scholar 

  52. 52.

    Ochsenbein AF, Fehr T, Lutz C, Suter M, Brombacher F, Hengartner H, Zinkernagel RM (1999) Control of early viral and bacterial distribution and disease by natural antibodies. Science 286:2156–2159

    PubMed  CAS  Google Scholar 

  53. 53.

    Abd El-Moneim EA (2017) Influence of in ovo injection with an effective bacterial preparation (Bifidobacterium spp.) on some productive and physiological traits in poultry. Doctoral dissertation, Ain Shams University, Faculty of Agriculture Accessed March 2017

  54. 54.

    Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H, Zinkernagel RM (2000) A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288:2222–2226

    PubMed  CAS  Google Scholar 

  55. 55.

    Abdel-Moneim AE, Selim DA, Basuony HA, Sabic EM, Saleh AA, Ebeid TA (2019) Effect of dietary supplementation of Bacillus subtilis spores on growth performance, oxidative status and digestive enzyme activities in Japanese quail birds. Trop Anim Health Prod:In Press:1–10. https://doi.org/10.1007/s11250-019-02055-1

  56. 56.

    Awad W, Ghareeb K, Abdel-Raheem S, Böhm 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

    PubMed  CAS  Google Scholar 

  57. 57.

    APHA (American Public Health Association) (1915) Standard methods for the examination of water and wastewater. American Public Health Association Inc., New York

    Google Scholar 

  58. 58.

    Difco M (1977) Dehydrated culture media and reagents for microbiological and clinical laboratory procedures. Difco laboratories Incorparated, Detroit

    Google Scholar 

  59. 59.

    Atlas RM (2004) Handbook of microbiological media. CRC press, Boca Raton

    Google Scholar 

  60. 60.

    OxoidManual (2006) Culture media, ingredients and other laboratory services. Oxoid Ltd., London

    Google Scholar 

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Acknowledgments

The authors acknowledge the Biological Application Department, Nuclear Research Center, Egyptian Atomic Energy Authority, Desert Research Center, Cairo, Egypt, and Poultry Production Department, Faculty of Agriculture, Ain Shams University, Egypt, for their cooperation.

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Correspondence to Abdel-Moneim Eid Abdel-Moneim.

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The current study was approved by the Ethics Committee of the Local Experimental Animals Care Committee, Egyptian Atomic Energy Authority (Number 6/2018EC).

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Abdel-Moneim, AM.E., Elbaz, A.M., Khidr, R.ES. et al. Effect of in Ovo Inoculation of Bifidobacterium spp. on Growth Performance, Thyroid Activity, Ileum Histomorphometry, and Microbial Enumeration of Broilers. Probiotics & Antimicro. Prot. 12, 873–882 (2020). https://doi.org/10.1007/s12602-019-09613-x

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Keywords

  • Bifidobacteria
  • Performance
  • Thyroid activity
  • Ileal histomorphometry
  • Bacterial population
  • Broilers