PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

Tyurina D.G., Laptev G.Yu., Yildirim E.A., Ilina L.A., Filippova V.A., Brazhnik E.A., Tarlavin N.V., Gorfunkel E.P., Dubrovin A.V., Novikova N.I., Dunyashev T.P., Grozina A.A. The impact of virginiamicin and probiotics on intestinal microbiome and growth performance traits of chicken (Gallus gallus L.) broilers. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2020, Vol. 55, № 6, p. 1220-1232.
(how to cite this article)

doi: 10.15389/agrobiology.2020.6.1220eng

UDC: 636.5.033:636.087.8:579.6:577.2

 

THE IMPACT OF VIRGINIAMICIN AND PROBIOTICS ON INTESTINAL MICROBIOME AND GROWTH PERFORMANCE TRAITS OF CHICKEN(Gallus gallus L.) BROILERS

D.G. Tyurina1, G.Yu. Laptev1, E.A. Yildirim1 ✉, L.A. Ilina1, V.A. Filippova1, E.A. Brazhnik1, N.V. Tarlavin1, E.P. Gorfunkel1, A.V. Dubrovin1, N.I. Novikova1, T.P. Dunyashev1, A.A. Grozina2

1JSC Biotrof+, 19, korp. 1, Zagrebskii bulv., St. Petersburg, 192284 Russia, e-mail tirina@biotrof.ru, georg-laptev@rambler.ru, deniz@biotrof.ru (✉ сorresponding author), ilina@biotrof.ru, filippova@biotrof.ru, bea@biotrof.ru, taгlav1995@biotrof.гu, elena@biotгof.ru, dubrowin.a.v@yandex.ru, novikova@biotтof.ru, timur@biotrof.ru;
2Federal Scientific Center All-Russian Research and Technological Poultry Institute RAS, 10, ul. Ptitsegradskaya, Sergiev Posad, Moscow Province, 141311 Russia, e-mail Alena_fisinina@mail.ru

ORCID:
Tyurina D.G. orcid.org/0000-0001-9001-2432
Tarlavin N.V. orcid.org/0000-0002-6474-9171
Laptev G.Yu. orcid.org/0000-0002-8795-6659
Gorfunkel E.P. orcid.org/0000-0002-6843-8733
Yildirim E.A. orcid.org/0000-0002-5846-5105
Dubrovin A.V. orcid.org/0000-0001-8424-4114
Ilina L.A. orcid.org/0000-0003-2789-4844
Novikova N.I. orcid.org/0000-0002-9647-4184
Filippova V.A. orcid.org/0000-0001-8789-9837
Dunyashev T.P. orcid.org/0000-0002-3918-0948
Brazhnik E.A. orcid.org/0000-0003-2178-9330
Grozina A.A. orcid.org/0000-0001-9654-7710

Received May 12, 2020

 

Today, there is great interest in the development of environmentally friendly feed additives for poultry farming as a worthy alternative to antibiotics capable of positively modulating the microbiota to control pathogenic microorganisms. However, very few studies have been devoted to comparing the effects of probiotics and antibiotics on the structure of the gut microbiome in broilers. In this study, we compared the composition of the intestinal microbiota and zootechnical parameters in chickens of the Cobb 500 cross during the starter, growth and finishing periods when a probiotic (Bacillus subtilis in the composition of Cellobacterin®-T) or an antibiotic (Stafac® 110 based on virginiamycin) was added to the diet and showed that the B. subtilis strain accelerates the formation of intestinal microflora. The probiotic also reduces the number of microorganisms of the Campylobacteriaceae family which includes many types of gastroenteritis pathogens, and also increases the digestibility of fiber. T-RFLP analysis and qPCR method were used to assess changes in the intestinal microbiota of Cobb 500 broiler chickens fed a Bacillus subtilis-based dietary probiotic and virginiamycin-based dietary antibiotic Stafac® 110. On day 14, the total counts of cecal bacteria, as compared to control, were 9.1 times higher (p ≤ 0.05) in broilers fed Stafac® 110, and 54.2 times higher (p ≤ 0.001) when fed B. subtilis preparation. This indicates rapid microbial colonization of gastrointestinal tract of the chickens fed Stafac® 110 and B. subtilis. T-RFLP analysis revealed two dominant cecal phyla, Firmicutes and Proteobacteria, while phyla Actinobacteria, Bacteroidetes, and Fusobacteriawere less abundant. The taxa are detected which ferment non-starch polysaccharides to produce short-chain fatty acids, inhibit the competing pathogens due to production of bacteriocins, and acidize the chyme as synthesize organic acids. Administration of the dietary antibiotic mostly positively influences the cecal microbiota, e.g., the cellulolytic bacteria and Clostridia forms involved in the synthesis of organic acids became more abundant (p ≤ 0.05). Similar beneficial effects, e.g., an increase in Clostridia counts (p ≤ 0.05) compared to control, occurred when the probiotic strain was administered. On day 14 of rearing, the dietary antibiotic and probiotic reduced abundance of Campylobacteriaceae family comprising gastroenteritis pathogens (p ≤ 0.05) when compared to control. An increase in bodyweight as compared to control (from 1845.8±20.9 to 1936.4±17.9 g, p = 0.046) occurred in 36-day-old chickens fed Stafac® 110 but not the probiotic strain but not the probiotic strain, despite recovery of gut microbiota in the chickens fed B. subtilis. A 7.1 % increase infiber digestibility (p = 0.0027) occurred in broilers fed dietary probiotic and a 2.3 % increase (p = 0.047) in those fed the dietary antibiotic, which may be due to the action of cellulolytic microorganisms. Therefore, a dietary B. subtilis-based probiotic which promotes recovery of gut microbiota and increases fiber digestibility in feeds for broiler chickens can be an effective alternative to the virginiamycin-based antibiotic Stafac® 110.

Keywords: broiler chickens, Cobb 500, probiotic, Bacillus subtilis, Stafac® 110, T-RFLP analysis, microbiome, Firmicutes, Proteobacteria, Clostridia,Campylobacteriaceae.

 

REFERENCES

  1. Phillips I., Casewell M., Cox T., De Groot B., Friis C., Jones R., Nightingale C., Preston R., Waddell J. Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. Journal of Antimicrobial Chemotherapy, 2004, 53(1): 28-52 CrossRef
  2. Gong J., Yin. F., Hou Y., Yin Y. Chinese herbs as alternatives to antibiotics in feed for swine and poultry production: potential and challenges in application. Canadian Journal of Animal Science, 2014, 94(2): 223-242 CrossRef
  3. Humphreys G., Fleck F. United Nations meeting on antimicrobial resistance. Bull. World Health Organ., 2016, 94(9): 638-639 CrossRef
  4. Onrust L., Ducatelle R., Driessche K.V., Maesschalck C., Vermeulen K., Haesebrouck F., Van Immerssel F. Steering endogenous butyrate production in the intestinal tract of broilers as a tool to improve gut health. Frontiers in Veterinary Science, 2015, 2: 75 CrossRef
  5. Borda-Molina D., Seifert J., Camarinha-Silva A. Current perspectives of the chicken gastrointestinal tract and its microbiome. Computational and Structural Biotechnology Journal, 2018, 16: 131-139 CrossRef
  6. Kohl K.D. Diversity and function of the avian gut microbiota. Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology, 2012, 182(5): 591-602 CrossRef
  7. Lindberg R., Jarnheimer P.A., Olsen B., Johansson M., Tysklind M. Determination of antibiotic substances in hospital sewage water using solid phase extraction and liquid chromatography/mass spectrometry and group analogue internal standards. Chemosphere, 2004, 57(10): 1479-1488 CrossRef
  8. Van Der Waaij D., Nord C.E. Development and persistence of multi-resistance to antibiotics in bacteria; an analysis and a new approach to this urgent problem. International Journal of Antimicrobial Agents, 2000, 16(3): 191-197 CrossRef
  9. Teirlynck E., De Gussem M., Marlen M., Vancraeynest D., Haesebrouck F., Ducatelle R., Van Immerseel F. Morphometric evaluation of “dysbacteriosis” in broilers. Avian Pathology, 2013, 40(2): 139-144 CrossRef
  10. Thomke S., Elwinger K. Growth promotants in feeding pigs and poultry. III. Alternatives to antibiotic growth promotants. Annales De Zootechnie, 1998, 47(4): 245-271 CrossRef
  11. Verstegen M.W.A., Williams B.A. Alternatives to the use of antibiotics as growth promoters for monogastric animals. Animal Biotechnology, 2002, 13(1): 113-127 CrossRef
  12. Yang Y., Iji P.A., Choct M. Dietary modulation of gut microflora in broiler chickens: a review of the role of six kinds of alternatives to in feed antibiotics. World’s Poultry Science Journal, 2009, 65(1): 97-114 CrossRef
  13. Li Z., Wang W., Liu D., Guo Y. Effects of Lactobacillus acidophilus on gut microbiota composition in broilers challenged with Clostridium perfringens. PLoS ONE, 2017, 12(11): 1-16 CrossRef
  14. Mañes-Lázaro R., Van Diemen P.M., Pin C., Mayer M.J., Stevens M.P., Narbad A. Administration of Lactobacillus johnsonii FI9785 to chickens affects colonisation by Campylobacter jejuni and the intestinal microbiota. British Poultry Science, 2017, 58(4): 373-381 CrossRef
  15. Macfarlane S. Antibiotics treatment and microbes in the gut. Environmental Microbiology, 2014, 16(4): 919-924 CrossRef
  16. Ferrer M., Martins dos Santos V.A., Ott S.J., Moya A. Gut microbiota disturbance during antibiotic therapy: a multi-omic approach. Gut Microbes, 2014, 5(1): 64-70 CrossRef
  17. Robinson C.J., Young V.B. Antibiotic administration alters the community structure of the gastrointestinal microbiota. Gut Microbes, 2010, 1(4): 279-284 CrossRef
  18. Ji S., Jiang T., Yan H., Guo C., Liu J., Su H., Alugongo G.M., Shi H., Wang Y., Cao Z., Li S. Ecological restoration of antibiotic-disturbed gastrointestinal microbiota in foregut and hindgut of cows. Frontiers in Cellular and Infection Microbiology, 2018, 8: 79 CrossRef
  19. Lin J., Hunkapiller A.A., Layton A.C., Chang Y.J., Robbins K.R. Response of intestinal microbiota to antibiotic growth promoters in chickens. Foodborne Pathogens and Disease, 2013, 10(4): 331e7 CrossRef
  20. Danzeisen J.L., Kim H.B., Isaacson R.E., Tu Z.J., Johnson T.J. Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. PLoS ONE, 2011, 6: e27949 CrossRef
  21. Lee K.W., Ho Hong Y., Lee S.H., Jang S.I., Park M.S., Bautista D.A., Ritter G.D., Jeong W., Jeoung H.Y., An D.J., Lillehoj E.P., Lillehoj H.S. Effects of anticoccidial and antibiotic growth promoter programs on broiler performance and immune status. Research in Veterinary Science, 2012, 93(2): 721-728 CrossRef
  22. Zhou H., Gong J., Brisbin J.T., Yu H., Sanei B., Sabour P., Sharif S. Appropriate chicken sample size for identifying the composition of broiler intestinal microbiota affected by dietary antibiotics, using the polymerase chain reaction-denaturing gradient gel electrophoresis technique. Poultry Science, 2007, 86(12): 2541-2549 CrossRef
  23. Gao P., Ma C., Sun Z., Wang L., Huang S., Su X., Xu J., Zhang H. Feed-additive probiotics accelerate yet antibiotics delay intestinal microbiota maturation in broiler chicken. Microbiome, 2017 5(1): 91 CrossRef
  24. Laptev G.Yu. Molochnoe i myasnoe skotovodstvo, 2010, 3: 16-18 (in Russ.).
  25. Tannock G.W., Munro K., Harmsen H.J., Welling G.W., Smart J., Gopal P.K. Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20. Applied and Environmental Microbiology, 2000, 66(6): 2578-2588 CrossRef
  26. RDocumentation. pheatmap. A function to draw clustered heatmaps. Available: https://www.rdocumentation.org/packages/pheatmap/versions/1.0.12/
    topics/pheatmap. Accessed: 08.02.2020.
  27. Murtagh F., Legendre P., Classif J. Ward’s hierarchical agglomerative clustering method: which algorithms implement Ward’s criterion? Journal of Classification, 2014, 31(3): 274-295 CrossRef
  28. Bryus P., Bryus E. Prakticheskaya statistika dlya spetsialistov Data Science [Practical statistics for Data Science specialists]. St. Petersburg, 2018 (in Russ.).
  29. Verzani J. Getting started with RStudio. O'Reilly Media, Sebastopol, 2011 (in Russ.).
  30. RStudio. Available: https://rstudio.com. No date.
  31. Rinttilä T., Apajalahti J. Intestinal microbiota and metabolites — implications for broiler chicken health and performance. Journal of Applied Poultry Research, 2013, 22: 647-658 CrossRef
  32. Jeurissen S.H.M., Janse E.M., Koch G., De Boer G.F. Postnatal development of mucosa-associated lymphoid tissues in chickens. Cell and Tissue Research, 1989, 258(1): 119-124.
  33. Wang L., Lilburn M., Yu Z. Intestinal microbiota of broiler chickens as affected by litter management regimens. Frontiers in Microbiology, 2016, 7: 593 CrossRef
  34. Qu A., Brulc J.M., Wilson M.K., Law B.F., Theoret J.R., Joens L.A. Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLoS ONE, 2008, 3(8): e2945 CrossRef
  35. Józefiak D., Rutkowski A., Martin S.A. Carbohydrate fermentation in the avian ceca: a review. Animal Feed Science and Technology, 2004, 113(1-4): 1-15 CrossRef
  36. Stanley D., Geier M.S., Denman S.E., Haring V.R., Crowley T.M., Hughes R.J., Moore R.J. Identification of chicken intestinal microbiota correlated with the efficiency of energy extraction from feed. Veterinary Microbiology, 2013, 164(1-2): 85-92 CrossRef
  37. Sergeant M.J., Constantinidou C., Cogan T.A., Bedford M.R., Penn C.W., Pallen M.J. Extensive microbial and functional diversity within the chicken cecal microbiome. PLoS ONE, 2014, 9(3): e91941 CrossRef
  38. McWhorter T.J., Caviedes-Vidal E., Karasov W.H. The integration of digestion and osmoregulation in the avian gut. Biological Reviews of the Cambridge Philosophical Society, 2009: 84(4): 533-565 CrossRef
  39. Tellez G., Higgins S.E., Donoghue A.M., Hargis B.M. Digestive physiology and the role of microorganisms. Journal of Applied Poultry Research, 2006, 15(1): 136-144.
  40. Cummings J.H., Pomare E.W., Branch W.J., Naylor C.P., Macfarlane G.T. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut, 1987, 28(10): 1221-1227 CrossRef
  41. van Der Wielen P.W., Biesterveld S., Notermans S., Hofstra H., Urlings B.A.P., van Knapen F. Role of volatile fatty acids in development of the cecal microflora in broiler chickens during growth. Applied and Environmental Microbiology, 2000, 66(6): 2536-2540 CrossRef
  42. Hungate R.E. The rumen and its microbes. Academic Press, NewYork, 1966.
  43. Zhan K., Gong X., Chen Y., Jiang M., Yang T., Zhao G. Short-chain fatty acids regulate the immune responses via G protein-coupled receptor 41 in bovine rumen epithelial cells. Frontiers in Immunology, 2019, 10: 2042 CrossRef
  44. Walker S.E., Sander J.E., Cline J.L., Helton J.S., Characterization of Pseudomonas aeruginosa isolates associated with mortality in broiler chicks. Avian Diseases, 2002, 46(4): 1045-1050 CrossRef
  45. Wegener H.C., Hald T., Wong D.L.F., Madsen M., Korsgaard H., Bager F., Gerner-Smidt P., Mølbak K. Salmonella control programs in Denmark. Emerging Infectious Diseases journal, 2003, 9(7): 774-780 CrossRef
  46. Oakley B.B., Lillehoj H.S., Kogut M.H., Kim W.K., Maurer J.J., Pedroso A., Lee M.D., Collett S.R., Johnson T.J., Cox N.A. The chicken gastrointestinal microbiome. FEMS Microbiology Letters, 2014, 360(2): 100-112 CrossRef
  47. Ramiah S.K., Zulkifli I., Rahim N.A., Ebrahimi M., Meng G.Y. Effects of two herbal extracts and virginiamycin supplementation on growth performance, intestinal microflora population and Fatty Acid composition in broiler chickens. Asian-Australasian Journal of Animal Sciences, 2014, 27(3): 375-382 CrossRef
  48. Forte C., Moscati L., Acuti G., Mugnai C., Franciosini M.P., Costarelli S., Cobellis G., Trabalza-Marinucci M. Effects of dietary Lactobacillus acidophilus and Bacillus subtilis on laying performance, egg quality, blood biochemistry and immune response of organic laying hens. Journal of Animal Physiology and Animal Nutrition, 2016, 100(5): 977-987 CrossRef
  49. Zulkifli I., Hashemi S.R., Somchit M.N., Zunita Z., Loh T.C., Soleimani A.F., Tang S.C. Effects of Euphorbia hirta and virginiamycin supplementation to the diet on performance, digestibility, and intestinal microflora population in broiler chickens. Archiv für Geflugelkünde, 2012, 76(1): 6-12.
  50. Andrianova E.N., Egorov I.A., Prisyazhnaya L.M., Akhmetova L.T., Sibgatullin Zh.Zh., Slesarenko N.A., Laptev G.Yu. Feed additive Vinivet of apicultural products as an alternative for antibiotic growth promoters in broiler chick di-ets — bactericidal and biostimulating effect. Agricultural Biology [Sel'skokhozyaistvennaya biologiya], 2016, 51(2): 213-222 CrossRef
  51. Niewold T.A. The nonantibiotic anti-inflammatory effect of antimicrobial growth promoters, the real mode of action? A hypothesis. Poultry Science, 2007, 86(4): 605-609 CrossRef
  52. Abu-Akkada Somaia S., Awad Ashraf M. Protective effects of probiotics and prebiotics on Eimeria Tenella-infected broiler chickens. Pakistan veterinary journal, 2015, 35(4): 446-450.
  53. Yadav S., Jha R. Strategies to modulate the intestinal microbiota and their effects on nutrient utilization. performance and health of poultry. Journal of Animal Science and Biotechnology, 2019, 10: 2 CrossRef

 

back

 


CONTENTS

 

 

Full article PDF (Rus)

Full article PDF (Eng)