Effect of a Potential Probiotic Candidate Enterococcus faecalis-1 on Growth Performance, Intestinal Microbiota, and Immune Response of Commercial Broiler Chickens

Abstract

The probiotic effect of Enterococcus faecalis-1 (isolated from healthy chickens) on growth performance, immune response, and modulation of the intestinal microbiota of broilers was assessed with a total of 100-day-old commercial Cobb chicks. The chicks were randomly divided into two equal groups. The control group received a basal diet, while the test group received a basal diet and was orally supplied with E. faecalis at a dose of 108 CFU/bird/day. Results showed that E. faecalis-1 supplement significantly (P < 0.05) improved the body weight and feed conversion ratio of treated broilers compared with the control ones. The mortality percentage was reduced in E. faecalis-1-supplemented group. The total IgY serum level was significantly (P < 0.05) increased in broilers receiving E. faecalis-1 supplement (7.1 ± 0.39) compared with the control group (5.8 ± 0.3), while the serum avidin level was significantly (P < 0.05) decreased in E. faecalis-1-supplemented broilers (76 ± 11.1). There was no significant change in the immune response towards avian influenza and Newcastle vaccines in both groups. The total Lactobacillus and Enterococcus counts were significantly (P < 0.05) higher in the cecal contents of broilers given E. faecalis-1 than those that received the control treatment. E. faecalis-1 supplement enhanced the enzyme activities, antioxidant system, and liver functions of treated broilers compared with those in the control group. Collectively, these results showed that E. faecalis-1 could promote growth performance and immunological status and convey beneficial modulation of the cecal microbiota in broilers.

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References

  1. 1.

    Havenstein GB, Ferket PR, Qureshi MA (2003) Growth, livability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult Sci 82(10):1500–1508

    CAS  PubMed  Google Scholar 

  2. 2.

    Barton MD (2000) Antibiotic use in animal feed and its impact on human health. Nutr Res Rev 13(2):279–299

    CAS  PubMed  Google Scholar 

  3. 3.

    Gaskins HR, Collier CT, Anderson DB (2002) Antibiotics as growth promotants: mode of action. Anim Biotechnol 13(1):29–42

    CAS  PubMed  Google Scholar 

  4. 4.

    Williams RJ, Heymann DL (1998) Containment of antibiotic resistance. Science 279(5354):1153–1154

    CAS  PubMed  Google Scholar 

  5. 5.

    Smith DL, Harris AD, Johnson JA, Silbergeld EK, Morris JG Jr (2002) Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proc Natl Acad Sci U S A 99:6434–6439

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6.

    FAO WHO (2001) Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Report of a joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria; FAO/WHO: Amerian Córdoba Park Hotel, Córdoba, 2001; pp:1–34

  7. 7.

    Zheng A, Luo J, Meng K, Li J, Bryden WL, Chang W, Zhang S, Wang LX, Liu G, Yao B (2016) Probiotic (Enterococcus faecium) induced responses of the hepatic proteome improves metabolic efficiency of broiler chickens (Gallus gallus). BMC Genomics 17:89

    PubMed  PubMed Central  Google Scholar 

  8. 8.

    Cao GT, Zeng XF, Chen AG, Zhou L, Zhang L, Xiao YP, Yang CM (2013) Effects of a probiotic, Enterococcus faecium on growth performance, intestinal morphology, immune response, and cecal microflora in broiler chickens challenged with Escherichia coli K88. Poult Sci 92(11):2949–2955

    CAS  PubMed  Google Scholar 

  9. 9.

    Olawale KO, Fadiora SO, Taiwo SS (2011) Prevalence of hospital-acquired enterococci infections in two primary-care hospitals in Osogbo, southwestern Nigeria. Afr J Infect Dis 5:40–46

    PubMed  PubMed Central  Google Scholar 

  10. 10.

    Pirgozliev V, Bravo D, Rose SP (2014) Rearing conditions influence nutrient availability of plant extracts supplemented diets when fed to broiler chickens. J Anim Physiol Anim Nutr (Berl) 98(4):667–671

    CAS  Google Scholar 

  11. 11.

    Czerwinski J, Hojberg O, Smulikowska S, Engberg RM, Mieczkowska A (2010) Influence of dietary peas and organic acids and probiotic supplementation on performance and caecal microbial ecology of broiler chickens. Br Poult Sci 51(2):258–269

    CAS  PubMed  Google Scholar 

  12. 12.

    Aalaei M, Khatibjoo A, Zaghari M, Taherpour K, Akbari Gharaei M, Soltani M (2018) Comparison of single- and multi-strain probiotics effects on broiler breeder performance, egg production, egg quality and hatchability. Br Poult Sci 59(5):531–538

    CAS  PubMed  Google Scholar 

  13. 13.

    Saini PK, Webert DW (1991) Application of acute phase reactants during antemortem and postmortem meat inspection. J Am Vet Med Assoc 198(11):1898–1901

    CAS  PubMed  Google Scholar 

  14. 14.

    Nakamura K, Ibaraki Y, Mitarai Z, Shibahara T (1999) Comparative pathology of heart and liver lesions of broiler chickens that died of ascites, heart failure, and others. Avian Dis 43(3):526–532

    CAS  PubMed  Google Scholar 

  15. 15.

    Adil S, Magray SN (2012) Impact and manipulation of gut microflora in poultry: a review. J Anim Vet Adv 11:873–877

    Google Scholar 

  16. 16.

    Ognik K, Krauze M, Cholewińska E, Abramowicz K (2017) The effect of a probiotic containing Enterococcus faecium DSM 7134 on redox and biochemical parameters in chicken blood. Ann Anim Sci 17(4):1075–1088

    CAS  Google Scholar 

  17. 17.

    Shehata A, Schrodl W, Neuhaus J, Kruger M (2013) Antagonistic effect of different bacteria on Clostridium botulinum types A, B, D and E in vitro. Vet Rec 172:74–78

    Google Scholar 

  18. 18.

    Shehata AA, Tarabees R, Basiuoni S, Gamil M, Kamel AS, Kruger M (2016) Phenotypic and genotypic characterization of bacteriocinogenic enterococci against Clostridium botulinum. Probiotics Antimicrob Proteins 9(2):182–188

    Google Scholar 

  19. 19.

    CLSI (2015) Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement. CLSI document M100-S25. Wayne, PA: Clinical and Laboratory Standards Institute. http://file.qums.ac.ir/repository/mmrc/CLSI2015.pdf. Accessed Jan 2017

  20. 20.

    Bester LA, Essack SY (2008) Prevalence of antibiotic resistance in Campylobacter isolates from commercial poultry suppliers in KwaZulu-Natal, South Africa. J Antimicrob Chemother 62(6):1298–1300

    CAS  PubMed  Google Scholar 

  21. 21.

    Tarabees R, Gafar KM, El-Sayed MS, Shehata AA, Ahmed M (2018) Effects of dietary supplementation of probiotic mix and prebiotic on growth performance, cecal microbiota composition, and protection against Escherichia coli O78 in broiler chickens. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-018-9459-y

  22. 22.

    OIE (2012) Terrestrial manual. Avian influenza (Chapter 2.3.4). In Manual of diagnostic tests and vaccines for terrestrial animals (Chapter 2.7.12). http://www.oie.int/international-standard-setting/terrestrial-manual/accessonline/. Accessed 12 Oct 2013

  23. 23.

    Shehata AA, Klaus H, Pfalz T, Hafez MH, Krueger M (2016) Efficacy of cold fogging and oral herbal extracts on air quality and immune response of broilers. Aerobiologia (Bologna) 33:37–47

    Google Scholar 

  24. 24.

    Shehata AA, Sultan H, Hafez HM, Kruger M (2013) Safety and efficacy of a metabolic drift live attenuated Salmonella Gallinarum vaccine against fowl typhoid. Avian Dis 57(1):29–35

    PubMed  Google Scholar 

  25. 25.

    Hwang IY, Ku HO, Lim SK, Park CK, Jung GS, Jung SC, Nam HM (2009) Species distribution and resistance patterns to growth-promoting antimicrobials of enterococci isolated from pigs and chickens in Korea. J Vet Diagn Investig 21(6):858–862

    Google Scholar 

  26. 26.

    Sanlibaba P, Tezel BU, Senturk E (2018) Antimicrobial resistance of Enterococcus species isolated from chicken in Turkey. Korean J Food Sci Anim Resour 38(2):391–402

    PubMed  PubMed Central  Google Scholar 

  27. 27.

    Garrido AM, Galvez A, Pulido RP (2014) Antimicrobial resistance in enterococci. J Infect Dis Ther 2:150

    Google Scholar 

  28. 28.

    Champagne J, Diarra MS, Rempel H, Topp E, Greer CW, Harel J, Masson L (2011) Development of a DNA microarray for enterococcal species, virulence, and antibiotic resistance gene determinations among isolates from poultry. Appl Environ Microbiol 77(8):2625–2633

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Miller WR, Munita JM, Arias CA (2014) Mechanisms of antibiotic resistance in enterococci. Expert Rev Anti-Infect Ther 12(10):1221–1236

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Dada AC, Ahmad A, Usup G, Heng LY (2013) Speciation and antimicrobial resistance of enterococci isolated from recreational beaches in Malaysia. Environ Monit Assess 185(2):1583–1599

    CAS  PubMed  Google Scholar 

  31. 31.

    Liu Y, Liu K, Lai J, Wu C, Shen J, Wang Y (2013) Prevalence and antimicrobial resistance of Enterococcus species of food animal origin from Beijing and Shandong province, China. J Appl Microbiol 114(2):555–563

    CAS  PubMed  Google Scholar 

  32. 32.

    Beukers AG, Zaheer R, Cook SR, Stanford K, Chaves AV, Ward MP, McAllister TA (2015) Effect of in-feed administration and withdrawal of tylosin phosphate on antibiotic resistance in enterococci isolated from feedlot steers. Front Microbiol 6:483

    PubMed  PubMed Central  Google Scholar 

  33. 33.

    Gueimonde M, Sanchez B, GdLR-G C, Margolles A (2013) Antibiotic resistance in probiotic bacteria. Front Microbiol 4:202

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    Alali WQ, Hofacre CL, Mathis GF, Faltys G (2013) Effect of essential oil compound on shedding and colonization of Salmonella enterica serovar Heidelberg in broilers. Poult Sci 92(3):836–841

    CAS  PubMed  Google Scholar 

  35. 35.

    Mountzouris KC, Tsirtsikos P, Kalamara E, Nitsch S, Schatzmayr G, Fegeros K (2007) Evaluation of the efficacy of a probiotic containing Lactobacillus, Bifidobacterium, Enterococcus, and Pediococcus strains in promoting broiler performance and modulating cecal microflora composition and metabolic activities. Poult Sci 86(2):309–317

    CAS  PubMed  Google Scholar 

  36. 36.

    Patterson JA, Burkholder KM (2003) Application of prebiotics and probiotics in poultry production. Poult Sci 82(4):627–631

    CAS  PubMed  Google Scholar 

  37. 37.

    Samli HE, Senkoylu N, Koc F, Kanter M, Agma A (2007) Effects of Enterococcus faecium and dried whey on broiler performance, gut histomorphology and intestinal microbiota. Arch Anim Nutr 61(1):42–49

    PubMed  Google Scholar 

  38. 38.

    Samli HE, Dezcan S, Koc F, Ozduven ML, Okur AA, Senkoylu N (2010) Effects of Enterococcus faecium supplementation and floor type on performance, morphology of erythrocytes and intestinal microbiota in broiler chickens. Br Poult Sci 51(4):564–568

    CAS  PubMed  Google Scholar 

  39. 39.

    Levkut M, Revajova V, Laukova A, Sevcikova Z, Spisakova V, Faixova Z, Levkutova M, Strompfova V, Pistl J (2012) Leukocytic responses and intestinal mucin dynamics of broilers protected with Enterococcus faecium EF55 and challenged with Salmonella Enteritidis. Res Vet Sci 93(1):195–201

    CAS  PubMed  Google Scholar 

  40. 40.

    Abdel-Latif MA, Abd El-Hack ME, Swelum AA, Saadeldin IM, Elbestawy AR, Shewita RS, Ba-Awadh HA, Alowaimer AN, Abd El-Hamid HS (2018) Single and combined effects of Clostridium butyricum and Saccharomyces cerevisiae on growth indices, intestinal health, and immunity of broilers. Animals (Basel) 8(184):1–13

    Google Scholar 

  41. 41.

    Campana R, van Hemert S, Baffone W (2017) Strain-specific probiotic properties of lactic acid bacteria and their interference with human intestinal pathogens invasion. Gut Pathog 9:12

    PubMed  PubMed Central  Google Scholar 

  42. 42.

    Rosebrough RW, McMurtry JP, Mitchell AD, Steele NC (1988) Chicken hepatic metabolism in vitro. Protein and energy relations in the broiler chicken-VI. Effect of dietary protein and energy restrictions on in vitro carbohydrate and lipid metabolism and metabolic hormone profiles. Comp Biochem Physiol B 90(2):311–316

    CAS  PubMed  Google Scholar 

  43. 43.

    El-Baky AAA (2013) Clinicopathological and immunological effects of multistrain probiotic on broiler chicken vaccinated against avian influenza virus. Global Vet 10:534–541

    Google Scholar 

  44. 44.

    Panda AK, Rama Rao SV, Raju MVLN, Sharma SR (2006) Dietary supplementation of lactobacillus sporogenes on performance and serum biochemico-lipid profile of broiler chickens. J Poult Sci 43:235–240

    CAS  Google Scholar 

  45. 45.

    Kalavathy R, Abdullah N, Jalaludin S, Ho YW (2003) Effects of Lactobacillus cultures on growth performance, abdominal fat deposition, serum lipids and weight of organs of broiler chickens. Br Poult Sci 44(1):139–144

    CAS  PubMed  Google Scholar 

  46. 46.

    Kullisaar T, Zilmer M, Mikelsaar M, Vihalemm T, Annuk H, Kairane C, Kilk A (2002) Two antioxidative lactobacilli strain as promising probiotics. Int J Food Microbiol 72(3):215–224

    CAS  PubMed  Google Scholar 

  47. 47.

    Ognik K, Krauze M (2016) The potential for using enzymatic assays to assess the health turkeys. Worlds Poult Sci J 72:535–550

    Google Scholar 

  48. 48.

    Panda AK, Reddy MR, Ramarao SV, Raju MVLN, Praharaj NK (2000) Growth, carcass characteristics, immunecompetence and response to Escherichia coli of broilers fed diets with various levels of probiotic. Arch Geflugelkd 64:152–156

    Google Scholar 

  49. 49.

    Sohail MU, Rahman ZU, Ijaz A, Yousaf MS, Ashraf K, Yaqub T, Zaneb H, Anwar H, Rehman H (2011) Single or combined effects of mannan-oligosaccharides and probiotic supplements on the total oxidants, total antioxidants, enzymatic antioxidants, liver enzymes, and serum trace minerals in cyclic heat-stressed broilers. Poult Sci 90(11):2573–2577

    CAS  PubMed  Google Scholar 

  50. 50.

    Ferreira CL, Salminen S, Grezkowiak L, Brizuela M, Sanchez L, Carneiro H, Bonnet M (2011) Terminology concepts of probiotic and prebiotic and their role in human and animal health. Rev Salud Anim 33(3):137–146

    Google Scholar 

  51. 51.

    Rhee KJ, Sethupathi P, Driks A, Lanning DK, Knight KL (2004) Role of commensal bacteria in development of gut-associated lymphoid tissues and preimmune antibody repertoire. J Immunol 172(2):1118–1124

    CAS  PubMed  Google Scholar 

  52. 52.

    Muira WI, Brydenb WL, Husband AJ (2000) Immunity, vaccination and the avian intestinal tract. Dev Comp Immunol 24:325–342

    Google Scholar 

  53. 53.

    Luo J, Zheng A, Meng K, Chang W, Bai Y, Li K, Cai H, Liu G, Yao B (2013) Proteome changes in the intestinal mucosa of broiler (Gallus gallus) activated by probiotic Enterococcus faecium. J Proteome 91:226–241

    CAS  Google Scholar 

  54. 54.

    Morishita TY, Aye PP, Harr BS, Cobb CW, Clifford JR (1997) Evaluation of an avian-specific probiotic to reduce the colonization and shedding of Campylobacter jejuni in broilers. Avian Dis 41(4):850–855

    CAS  PubMed  Google Scholar 

  55. 55.

    Huff GR, Huff WE, Jalukar S, Oppy J, Rath NC, Packialakshmi B (2013) The effects of yeast feed supplemention on Turkey performanc and pathogen colonization in a transport stress / Escherichia coli challenge. Poult Sci 92(3):655–662

    CAS  PubMed  Google Scholar 

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Funding

The authors would like to acknowledge the Science and Technology Development Fund, Egypt, Grant No. 9222 for their financial support.

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Shehata, A.A., Tarabees, R., Basiouni, S. et al. Effect of a Potential Probiotic Candidate Enterococcus faecalis-1 on Growth Performance, Intestinal Microbiota, and Immune Response of Commercial Broiler Chickens. Probiotics & Antimicro. Prot. 12, 451–460 (2020). https://doi.org/10.1007/s12602-019-09557-2

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Keywords

  • Enterococci
  • Probiotic
  • Broiler performance
  • Intestinal microbiota
  • Serum avidin
  • IgY