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Papers

Evaluation of Enterococcus faecium NCIMB 11181 and Clostridium butyricum probiotic supplements in post-weaning rabbits reared under thermal stress conditions

, ORCID Icon, , , & ORCID Icon
Pages 1232-1243 | Received 24 Apr 2021, Accepted 05 Jun 2021, Published online: 06 Sep 2021

References

  • Alagawany M, El-Hack A, Mohamed E, Al-Sagheer AA, Naiel MA, Saadeldin IM, Swelum AA. 2018. Dietary cold pressed watercress and coconut oil mixture enhances growth performance, intestinal microbiota, antioxidant status, and immunity of growing rabbits. Animals. 8(11):212.
  • Al-Sagheer AA, Abdel-Rahman G, Ayyat MS, Gabr HA, Elsisi GF. 2020. Productive performance response of growing rabbits to dietary protein reduction and supplementation of pyridoxine, protease, and zinc. An Acad Bras Ciênc. 92(3):e20180989.
  • Al-Sagheer AA, El-Hack A, Mohamed E, Alagawany M, Naiel MA, Mahgoub SA, Badr MM, Hussein EO, Alowaimer AN, Swelum AA. 2019. Paulownia leaves as a new feed resource: chemical composition and effects on growth, carcasses, digestibility, blood biochemistry, and intestinal bacterial populations of growing rabbits. Animals. 9(3):95.
  • AOAC. 2006. Official methods of analysis. 18th ed. Washington (DC): AOAC.
  • Attia YA, Bovera F, Abd‐Elhamid AE-HE, Calabrò S, Mandour MA, Al‐Harthi MA, Hassan SS. 2019. Evaluation of the carryover effect of antibiotic, bee pollen and propolis on growth performance, carcass traits and splenic and hepatic histology of growing rabbits. J Anim Physiol Anim Nutr. 103(3):947–958.
  • Attia YA, Hamed RS, Abd El-Hamid AE, Shahba HA, Bovera F. 2015. Effect of inulin and mannan-oligosaccharides compared with zinc-bacitracin on growing performance, nutrient digestibility and hematological profiles of growing rabbits. Anim Prod Sci. 55(1):80–86.
  • Attia YA, Hamed RS, Abd El-Hamid AE, Al-Harthi MA, Shahba HA, Bovera F. 2015. Performance, blood profile, carcass and meat traits and tissue morphology in growing rabbits fed mannanoligosaccharides and zinc-bacitracin continuously or intermittently. Anim Sci Pap Rep. 33:85–101.
  • Attia YA, Hamid E AE, Ismaiel AM, de Oliveira MC, Al-Harthi MA, El-Naggar AS, Simon GA. 2018. Nitrate detoxification using antioxidants and probiotics in the water for rabbits. Rev Colomb Cienc Pecu. 31(2):130–138.
  • Ayyat MS, Abd El-Latif KM, Helal AA, Al-Sagheer AA. 2021. Interaction of supplementary L-carnitine and dietary energy levels on feed utilization and blood constituents in New Zealand White rabbits reared under summer conditions. Trop Anim Health Prod. 53(2):1–8.
  • Blasco A, Ouhayoun J, Masoero G. 1993. Harmonization of criteria and terminology in rabbit meat research. World Rabbit Sci. 1:3–10.
  • Chen L, Li S, Zheng J, Li W, Jiang X, Zhao X, Li J, Che L, Lin Y, Xu S. 2018. Effects of dietary Clostridium butyricum supplementation on growth performance, intestinal development, and immune response of weaned piglets challenged with lipopolysaccharide. J Anim Sci Biotechnol. 9:1–14.
  • Daader AH, Al Sagheer AA, Gabr HA, Abd El Moniem EA. 2018. Alleviation of heat-stress-related physiological perturbations in growing rabbits using natural antioxidants. Span J Agric Res. 16(3):e0610.
  • De Blas C, Mateos GG. 2010. Feed formulation. In: De Blas C, Wiseman J, editors. Nutrition of the rabbit. London: CAB International; p. 222–232.
  • De Preter V, Vanhoutte T, Huys G, Swings J, De Vuyst L, Rutgeerts P, Verbeke K. 2007. Effects of Lactobacillus casei Shirota, Bifidobacterium breve, and oligofructose-enriched inulin on colonic nitrogen-protein metabolism in healthy humans. Am J Physiol Gastrointest Liver Physiol. 292(1):G358–G368.
  • Domann E, Hain T, Ghai R, Billion A, Kuenne C, Zimmermann K, Chakraborty T. 2007. Comparative genomic analysis for the presence of potential enterococcal virulence factors in the probiotic Enterococcus faecalis strain Symbioflor 1. Int J Med Microbiol. 297(7–8):533–539.
  • EFSA. 2012. Guidance on the safety assessment of Enterococcus faecium in animal nutrition. EFSA J. 10:2682.
  • El-Shafei AER, Younis T, Al-Gamal M, Hesham A. 2019. Impact of probiotic (Lactobacillus planterium) supplementation on productive and physiological performance of growing rabbits under Egyptian conditions. Egypt J Rabbit Sci. 29(1):125–148.
  • Galeano JAC, Herrera AL, Suescún JP. 2016. The probiotic Enterococcus faecium modifies the intestinal morphometric parameters in weaning piglets. Revista Facultad Nacional de Agronomía Medellín. 69:7803–7811.
  • Han J, Wang Y, Song D, Lu Z, Dong Z, Miao H, Wang W, He J, Li A. 2018. Effects of Clostridium butyricum and Lactobacillus plantarum on growth performance, immune function and volatile fatty acid level of caecal digesta in broilers. Food Agric Immunol. 29(1):797–807.
  • Hassan F, Mobarez S, Mohamed M, Attia Y, Mekawy A, Mahrose K. 2021. Zinc and/or selenium enriched spirulina as antioxidants in growing rabbit diets to alleviate the deleterious impacts of heat stress during summer season. Animals. 11(3):756.
  • Herzig I, Gőpfert E, Písaříková B, Strakova E. 2003. Testing of growth promoting and protective activity of the probiotic lactiferm in weaned piglets. Acta Vet Brno. 72(3):331–338.
  • Huang L, Luo L, Zhang Y, Wang Z, Xia Z. 2019. Effects of the dietary probiotic, Enterococcus faecium NCIMB11181, on the intestinal barrier and system immune status in Escherichia coli O78-challenged broiler chickens. Prob Antimicro Prot. 11(3):946–956.
  • Jain NC. 1986. Schalm's veterinary hematology. Philadelphia: Lea and Febiger.
  • Józefiak D, Kaczmarek S, Rutkowski A. 2008. A note on the effects of selected prebiotics on the performance and ileal microbiota of broiler chickens. J Anim Feed Sci. 17(3):392–397.
  • Kelly CJ, Zheng L, Campbell EL, Saeedi B, Scholz CC, Bayless AJ, Wilson KE, Glover LE, Kominsky DJ, Magnuson A, et al. 2015. Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host Microbe. 17(5):662–671.
  • Kim J, Ingale S, Kim Y, Kim K, Sen S, Ryu M, Lohakare J, Kwon I, Chae B. 2012. Effect of supplementation of multi‐microbe probiotic product on growth performance, apparent digestibility, cecal microbiota and small intestinal morphology of broilers. J Anim Physiol Anim Nutr. 96(4):618–626.
  • Kong Q, He G-Q, Jia J-L, Zhu Q-L, Ruan H. 2011. Oral administration of Clostridium butyricum for modulating gastrointestinal microflora in mice. Curr Microbiol. 62(2):512–517.
  • Kreuzer-Redmer S, Bekurtz JC, Arends D, Bortfeldt R, Kutz-Lohroff B, Sharbati S, Einspanier R, Brockmann GA. 2016. Feeding of Enterococcus faecium NCIMB 10415 leads to intestinal miRNA-423-5p-induced regulation of immune-relevant genes. Appl Environ Microbiol. 82(8):2263–2269.
  • Lambert JM, Bongers RS, de Vos WM, Kleerebezem M. 2008. Functional analysis of four bile salt hydrolase and penicillin acylase family members in Lactobacillus plantarum WCFS1. Appl Environ Microbiol. 74(15):4719–4726.
  • Liong M, Shah N. 2005. Acid and bile tolerance and cholesterol removal ability of lactobacilli strains. J Dairy Sci. 88(1):55–66.
  • Liong MT, Shah NP. 2006. Effects of a Lactobacillus casei synbiotic on serum lipoprotein, intestinal microflora, and organic acids in rats. J Dairy Sci. 89(5):1390–1399.
  • Liu C, Zhu Q, Chang J, Yin Q, Song A, Li Z, Wang E, Lu F. 2017. Effects of Lactobacillus casei and Enterococcus faecalis on growth performance, immune function and gut microbiota of suckling piglets. Arch Anim Nutr. 71(2):120–133.
  • Lye H-S, Rahmat-Ali GR, Liong M-T. 2010. Mechanisms of cholesterol removal by lactobacilli under conditions that mimic the human gastrointestinal tract. Int Dairy J. 20(3):169–175.
  • Lye H-S, Rusul G, Liong M-T. 2010. Removal of cholesterol by lactobacilli via incorporation and conversion to coprostanol. J Dairy Sci. 93(4):1383–1392.
  • Mallo J, Riopérez J, Honrubia P. 2010. The addition of Enterococcus faecium to diet improves piglet's intestinal microbiota and performance. Livestock Science. 133(1-3):176–178.
  • Marai IFM, Ayyat MS, Abd El-Monem UM. 2001. Growth performance and reproductive traits at first parity of New Zealand white female rabbits as affected by heat stress and its alleviation under Egyptian conditions. Trop Anim Health Prod. 33(6):451–462.
  • Marciano R, Santamarina AB, de Santana AA, Silva M. d L C, Amancio OMS, do Nascimento C. M d P O, Oyama LM, de Morais MB. 2015. Effects of prebiotic supplementation on the expression of proteins regulating iron absorption in anaemic growing rats. Br J Nutr. 113(6):901–908.
  • Mateos G, Rebollar P, De Blas C. 2010. Minerals, vitamins and additives. In: de Blas C, Wiseman J, editors. Nutrition of the rabbit. Wallingford: CABI Publishing; p. 119–150.
  • Nakanishi S, Kataoka K, Kuwahara T, Ohnishi Y. 2003. Effects of high amylose maize starch and Clostridium butyricum on metabolism in colonic microbiota and formation of azoxymethane-induced aberrant crypt foci in the rat colon. Microbiol Immunol. 47(12):951–958.
  • Ouwehand A, Tölkkö S, Kulmala J, Salminen S, Salminen E. 2000. Adhesion of inactivated probiotic strains to intestinal mucus. Lett Appl Microbiol. 31(1):82–86.
  • Pajarillo EAB, Chae JP, Balolong MP, Kim HB, Park C-S, Kang D-K. 2015. Effects of probiotic Enterococcus faecium NCIMB 11181 administration on swine fecal microbiota diversity and composition using barcoded pyrosequencing. Anim Feed Sci Technol. 201:80–88.
  • Palmquist D, Conrad H. 1971. Origin of plasma fatty acids in lactating cows fed high grain or high fat diets. J Dairy Sci. 54(7):1025–1033.
  • Pereira DI, Gibson GR. 2002. Cholesterol assimilation by lactic acid bacteria and bifidobacteria isolated from the human gut. Appl Environ Microbiol. 68(9):4689–4693.
  • Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ. 2002. The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett. 217(2):133–139.
  • Romero C, Rebollar PG, Moscati L, Dal Bosco A, Castellini C, Cardinali R. 2012. Effect of substitution of medium-chain organic acids for zinc bacitracin in a diet containing colistin on performance and development of intestinal lymphoid tissues in growing rabbits experimentally infected with Escherichia coli O103 and Clostridium perfringens toxinotype A. Anim Feed Sci Technol. 174(3–4):174–181.
  • Salim HM, Kang HK, Akter N, Kim DW, Kim JH, Kim MJ, Na JC, Jong HB, Choi HC, Suh OS, et al. 2013. Supplementation of direct-fed microbials as an alternative to antibiotic on growth performance, immune response, cecal microbial population, and ileal morphology of broiler chickens. Poultr Sci. 92(8):2084–2090.,
  • 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.
  • Seyyedin S, Nazem MN. 2017. Histomorphometric study of the effect of methionine on small intestine parameters in rat: an applied histologic study. Folia Morphol. 76(4):620–629.
  • Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, Shi H, Thangaraju M, Prasad PD, Manicassamy S, Munn DH, et al. 2014. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity. 40(1):128–139.,
  • Stamilla A, Messina A, Sallemi S, Condorelli L, Antoci F, Puleio R, Loria GR, Cascone G, Lanza M. 2020. Effects of microencapsulated blends of organics acids (OA) and essential oils (EO) as a feed additive for broiler chicken. A focus on growth performance, gut morphology and microbiology. Animals. 10(3):442.
  • Suvarna KS, Layton C, Bancroft JD. 2013. Bancroft's theory and practice of histological techniques. 7th ed. Oxford: Churchill Livingstone.
  • Taverniti V, Guglielmetti S. 2011. The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes Nutr. 6(3):261–274.
  • Van Soest P V, Robertson J, Lewis B, 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597.
  • Vonderheid SC, Tussing-Humphreys L, Park C, Pauls H, OjiNjideka Hemphill N, LaBomascus B, McLeod A, Koenig MD. 2019. A systematic review and meta-analysis on the effects of probiotic species on iron absorption and iron status. Nutrients. 11(12):2938.
  • Vrotniakienė V, Jatkauskas J. 2013. Effects of probiotics dietary supplementation on diarrhea incidence, fecal shedding of Escherichia coli and growth performance in post-weaned piglets. Veterinarija Ir Zootechnika. 63:81–88.
  • Wang K, Cao G, Zhang H, Li Q, Yang C. 2019. Effects of Clostridium butyricum and Enterococcus faecalis on growth performance, immune function, intestinal morphology, volatile fatty acids, and intestinal flora in a piglet model. Food Funct. 10(12):7844–7854.
  • Wu Y, Zhen W, Geng Y, Wang Z, Guo Y. 2019. Effects of dietary Enterococcus faecium NCIMB 11181 supplementation on growth performance and cellular and humoral immune responses in broiler chickens. Poultr Sci. 98(1):150–163.
  • Yang C, Cao G, Ferket P, Liu T, Zhou L, Zhang L, Xiao Y, Chen A. 2012. Effects of probiotic, Clostridium butyricum, on growth performance, immune function, and cecal microflora in broiler chickens. Poultr Sci. 91(9):2121–2129.
  • Zhang J, Xie Q, Ji J, Yang W, Wu Y, Li C, Ma J, Bi Y. 2012. Different combinations of probiotics improve the production performance, egg quality, and immune response of layer hens. Poultr Sci. 91(11):2755–2760.