Nutrient Utilizations and Intestinal Morphology of Broilers Treated with Lactobacillus plantarum AKK30 – Oligosaccharides Synbiotic

H. Julendra, A. Sofyan, M. F. Karimy, Abinawanto Abinawanto, Yasman Yasman

Abstract

Lactobacillus plantarum AKK30 inoculum in de Maan Rogosa Sharpe Broth (MRSB) grown on media containing oligosaccharides (inulin or mannan oligosaccharides/MOS) was studied in vitro and in vivo. In vitro assay was conducted to characterize metabolite profiles and its effect on pathogenic bacteria, while in vivo assay was conducted to study the metabolic energy, nitrogen retention, and intestinal morphology of broilers. A total of 24 male broilers-40-day-old (average body weight= 1.725±0.05 kg) strains Cobb-500 were used, where 20 birds were added 1% inoculum L plantarum AKK30 of daily intake and randomly distributed in five treatments and four replications consisted of: A) MRSB + L. plantarum AKK-30 (10⁷ cfu g-1); B) MRSB + inulin 0.5% (w v-1); C) MRSB + MOS 0.5%(w v-1); D) L. plantarum AKK-30 (10⁷ cfu g-1) + MRSB + inulin 0.5% (w v-1).; and E) L. plantarum AKK-30 (10⁷ cfu g-1) + MRSB + MOS 0.5% (w v-1), while 4 birds were fasted as endogenous chicken. The results showed that the highest isoleucine and threonine were found in group E. The highest oleic acid and the lowest conjugated linoleic acid (CLA) were observed in all treatments and inoculum did not affect antibacterial activity. The metabolizable energy values and nitrogen retention in group D and E were higher than other treatments (p<0.05). The lowest height of villi was observed in group A (p<0.05). In conclusion, the addition of oligosaccharides inulin or mannan oligosaccharide (MOS) affects the metabolite profiles of Lactobacillus plantarum AKK30 and their synbiotic effects improve intestinal morphology, metabolizable energy, and nitrogen retention in broilers.

References

Adebola, O. O., O. Corcoran, & W. A. Morgan. 2014. Synbiotics: the impact of potential prebiotics inulin, lactulose and lactobionic acid on the survival and growth of lactobacilli probiotics. J. Funct. Food. 10: 75-48. https://doi.org/10.1016/j.jff.2014.05.010

Ahmed, M.M.N., Z.S.H. Ismail, & A.A.A. Abdel-Wareth. 2018. Effect of dietary supplementation of prebiotic, betaine and their combination on growth performance, nutrient digestibility, carcass criteria and cecum microbial population of ducks under hot environmental conditions. Egypt. Poult. Sci. 38:289-304. https://doi.org/10.21608/epsj.2018.5666

Ajuwon, J.M. 2016. 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

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

Alonge, E.O., D. Eruvbetine, O.M.O. Idowu, A.O. Obadina, & O.O. Olukomaiya. 2017. Effect of dietary feed additives on hematological and serum biochemical parameters of broiler chickens. J. Anim. Feed Res. 7: 18-23.

AOAC. 2005. Official Methods of Analysis of AOAC International 18th ed. Assoc. Off. Anal. Chem., Arlington.

Apajalahti, J. & K. Vienola. 2016. Interaction between chicken intestinal microbiota and protein digestion. Anim. Feed. Sci. Technol. 221: 323-330. https://doi.org/10.1016/j.anifeedsci.2016.05.004

Baurhoo, B., A. Letellier, Z. Xi, & C. A. Ruiz- Feria. 2007. Cecal population of lactobacilli and bifidobacterial and Escherichia coli after in-vivo Escherichia coli challenge in birds fed diets with purified lignin or mannanoligosaccharides. Poult. Sci. 86: 2509-2516. https://doi.org/10.1093/ps/86.6.1070

Birmani, M. W., A. Nawab, M. Ghani, G. Li, M. Xiao, & L. An. 2019. A Review: role of inulin in animal nutrition. J. Food. Technol. Res. 6:18-27. https://doi.org/10.18488/journal.58.2019.61.18.27

Bonev, B., H. James, & P. Judacael. 2008. Principles of assessing bacterial susceptibility to antibiotics using the agar diffusion method. J. Antimicrob. Chem. 61:1295-1301. https://doi.org/10.1093/jac/dkn090

Cao, L., X.H. Wu, Y.L. Bai, X.Y. Wu, & S.B. Gu. 2019. Anti-inflammatory and antioxidant activities of probiotic powder containing Lactobacillus plantarum 1.2567 in necrotic enteritis model of broiler chickens. Livest. Sci. 223: 157-163. https://doi.org/10.1016/j.livsci.2019.03.009

Chang, C.H., P. Y. Teng, T.T. Lee, & Y. Bi. 2019. Effects of multi-strain probiotics combined with Gardeniae fructus on intestinal microbiota, metabolites, and morphology in broilers. J. Poult. Sci. 56: 32-43. https://doi.org/10.2141/jpsa.0170179

Cohort. 2005. Costat-Coplot Version 6.311. Cohort Software798 Light House Ave. PMB320. Monterey. CA93940 and USA.

Coskun, I.G., G. Erener, H. Cayiroglu, A. Altop, H. Cayan, & A. Sahin. 2017. Effects of dietary synbiotic supplementation on growth performance and duodenum histology of Japanese quail (Coturnix coturnix Japonica) reared in different flooring systems. Rev. Bras. Zootecn. 46: 800-804. https://doi.org/10.1590/s1806-92902017001000002

De Oliveira, A.J.B., R.A.C. Gonçalves, T. P. C. Chierrito, M.M. dos Santos, L. M. de Souza, P.A.J. Gorin, G.L. Sassaki, & M. Iacomini. 2011. Structure and degree of polymerisation of fructooligosaccharides present in roots and leaves of Stevia rebaudiana (Bert.) Bertoni. Food Chem. 129: 305-311. https://doi.org/10.1016/j.foodchem.2011.04.057

Filho, F.D.E., K.A.A. Torres, D.E. Faria, D.M.B. Campos, & P.S. Rosa. 2006. Probiotics for broiler chickens in Brazil: systematic review and meta-analysis. Braz. J. Poult. Sci. 8: 89-98. https://doi.org/10.1590/S1516-635X2006000200004

Forkus, B., S. Ritter, M. Vlysidis, K. Geldart, & Y. N. Kaznessis. 2017. Antimicrobial probiotics reduce Salmonella enterica in turkey gastrointestinal tracts. Sci. Rep. 7: 40695. https://doi.org/10.1038/srep40695

Franz, J., M. Tarantola, & C. Riethmuller. 2017. How tetraspanins shape endothelial and leukocyte nano-architecture during inflammation. Biochem. Soc. Trans. 45: 999-1006. https://doi.org/10.1042/BST20170163

Gibson, G.R., R. Hutkins, M. F. Sanders, S. L. Prescott, R. A. Reimer, S. J. Salminen, K. Scott, C. Stanton, K. S. Swanson, P. D. Cani, & K. Verbeke. 2017. Expert consensus document: The international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics.Nat. Rev. Gastro. Hepat. 14:491. https://doi.org/10.1038/nrgastro.2017.75.

Istiqomah, L., A. Sofyan, E. Damayanti, & H. Julendra. 2009. Amino acid profile of earthworm and earthworm meal (Lumbricus rubellus) for animal feedstuff. J. Indones. Trop. Anim. Agric. 34:253-257. https://doi.org/34.10.14710/jitaa.34.4.253-257

Jimenez, E.M., M. Frikha, A. de Coca Sinova, J. Garcia, & G.G. Mateos. 2013. Oat hulls and sugar beet pulp in diet of broilers; effect on growth performance and nutrient digestibility. Anim. Feed. Sci. Technol. 182: 33-43. https://doi.org/10.1016/j.anifeedsci.2013.03.011

Kavoi, B. M., D. W. Gakuya, P. N. Mbugua, & S. G. Kiama. 2016. Effects of dietary Moringa oleifera leaf meal supplementation on chicken intestinal structure and growth performance. J. Morphol. Sci. 33: 186-192. http://dx.doi.org/10.4322/jms.095915

Metzler-Zebeli, B.U., E. Magowan, M. Hollmann, M.E.E. Ball, A. Moln’ar, K. Witter, R. Ertl, R.J. Hawken, P.G. Lawlor, N.E. O’Connell, J. Aschenbach, & Q. Zebeli. 2018. Differences in intestinal size, structure, and function contributing to feed efficiency in broiler chickens reared at geographically distant locations. Poult. Sci. 97: 578-591. https://doi.org/10.3382/ps/pex332

McGlone, J. 2010. Guide for The Care and Use of Agricultural Animals in Research and Teaching. Fed. Anim. Sci. Soc. 3th ed. https://www.aaalac.org/ [5 May 2019].

National Research Council (NRC). 1994. Nutrient Requirements of Poultry. 9th Revised Edition. National Academy Press, Washington DC. USA.

Olnood, C.G., S.M.B. Sleman, C. Mingan, & A.I. Paul. 2015. Novel probiotics: their effects on growth performance, gut development, microbial community and activity of broiler chickens. Anim. Nutr. 1: 184-191. https://doi.org/10.1016/j.aninu.2015.07.003

Palaniyandi, S.A., D. Karthiyaini, W.S. Joo, & H.Y. Seung. 2017. In vitro characterization of Lactobacillus plantarum strains with inhibitory activity on enteropathogens for use as potential animal probiotics. Indian J. Microbiol. 57: 201. https://doi.org/10.1007/s12088-017-0646-4

Peng, Q., X.F. Zeng, J. L. Zhu, S. Wang, X. T. Liu, C. L. Hou, P. A. Thacker, & S.Y. Qiao. 2016. Effects of dietary Lactobacillus plantarum B1 on growth performance, intestinal microbiota, and short chain fatty acid profiles in broiler chickens. Poult. Sci. 95: 893-900. https://dx.doi.org/10.3382/ps/pev435

Pourabedin, M. & X. Zhao. 2015. Prebiotics and gut microbiota in chickens. FEMS Microbiol. Lett. 362: 1-8. https://doi.org/10.1093/femsle/fnv122

Pranckute, R., K. Arnoldas, K. Nomeda, & J.C. Donaldas. 2016. Combining prebiotics with probiotic bacteria can enhance bacterial growth and secretion of bacteriocins. Int. J. Biol. Macromol. 89: 669-676. https://doi.org/10.1016/j. ijbiomac.2016.05.041

Rageb, M. M. S., E.A. Abd-Allah, N.S. Abu-Khalil, F.M. Abdel-Maksoud, & U.T. Mahmoud. 2018. Effect of mannan-oligosaccharides and ß-glucan prebiotics on the brain oxidant/ antioxidant balance in broiler under natural egyptian summer conditions. Egypt Acad. J. Biol. Sci., B. Zool. 10: 35-46. https://doi.org/10.21608/eajbsz.2018.13428

Ravangard, A.H., M. Houshmand, M. Khajavi & R. Naghiha. 2017. Performance and cecal bacteria counts of broilers fed low protein diets with and without a combination of probiotic and prebiotic. Braz. J. Poult. Sci. 19: 75-82. https://doi.org/10.1590/1806-9061-2016-0319

Roberfroid, M., G.R. Gibson, & L. Hoyles. 2010. Prebiotic effects: metabolic and health benefits. Br. J. Nutr. 104:51-63. https://doi.org/10.1017/S0007114510003363

Roberts, T., J. Wilson, A. Guthrie, K. Cookson, D. Vancraeynest, J. Schaeffer, R. Moody, & S. Clark. 2015. New issues and science in broiler chicken intestinal health: Emerging technology and alternative interventions. J. Appl. Poult. Res. 24: 257-266. http://dx.doi.org/10.3382/japr/pfv023

Rodjan, P., K. Soisuwan, K. Thongprajukaew, Y. Theapparat, S. Khongthong, J. Jeenkeawpieam, & T. Salaeharae. 2018. Effect of organic acids or probiotics alone or in combination on growth performance, nutrient digestibility, enzyme activities, intestinal morphology and gut microflora in broiler chickens. J. Anim. Physiol. Anim. Nutr. 102: e931-e940. https://doi.org/10.1111/jpn.12858

Rotaru, A.S., I.D. Pop, A. Vatca, & A. Cioban. 2012. Usefulness of principal component analysis in agriculture. Bull. Univ. Agric. Sci. Vet. Hort. 69: 504-509. http://dx.doi.org/10.15835/buasvmcn-hort:8837

Santos, F.R., J.H. Stringhini, P.R. Oliveira, E.F. Duarte, C.S. Minafra & M.B. Café. 2015. Values of metabolizable energy and metabolization of nutrients for slow- and fast-growing birds at different ages. Braz. J. Poult. Sci. 17: 517- 522. https://doi.org/10.1590/1516-635X1704517-522

Schrezenmeir, J. & M. deVrese. 2001. Probiotics, prebiotics, and synbiotics approaching a definition. Am. J. Clin. Nutr. 73:361-364. https://doi.org/10.1093/ajcn/73.2.361s

Sethiya, N.K. 2016. Review on natural growth promoters available for improving gut health of poultry: an alternative to antibiotic growth promoters. Asian. J. Poult. Sci. 10: 21-29. https://doi.org/10.3923/ajpsaj.2016

Sibbald, I. R. & M.S. Wolynets. 1985. Relationships between estimates of bioavailable energy made with adult cockerels and chicks: effects of feed intake and nitrogen retention. Poult. Sci. 64: 127-138. https://doi.org/10.3382/ps.0640127

Sofyan, A., R. S. H. Martin, E. B. Laconi, A. Jayanegara, H. Julendra, E. Damayanti, & A. E. Suryani. 2019. The assays of bacteria-yeast consortia as probiotics candidates and their influences on nutrients utilization of quails diet. Trop. Anim. Sci. J. 42: 196-202. https://doi.org/10.5398/tasj.2019.42.3.196

Soto, C. 2013. Lactobacillus plantarum as source of conjugated linoleic acid: Effect of pH, incubation temperature and inulin incorporation. J. Biochem. Technol. 5:649-653.

Thorat, S.G., V.S. Panwar, D.S. Dahiya, & B.S. Tewatia. 2015. Efficacy of probiotics, prebiotics and enzymes as growth promoters on the performance of broiler chicken. Haryana Vet. 54:75-78.

Titze, B. & G. Christel. 2016. Volume scanning electron microscopy for imaging biological ultrastructure. Biol. Cell. 108:307-337. https://doi.org/10.1111/boc.201600024

Tsirtsikos, P.K., K. Fegeros, C. Balaskas, A. Kominakis, & K.C. Mountzouri. 2012. Dietary probiotic inclusion level modulates intestinal mucin composition and mucosal morphology in broilers. Poult. Sci. 91:1860-1868. https://doi.org/10.3382/ps.2011-02005

USDA. 2017. National Nutrient Database for Standard Reference. Version Current. https://ndb.nal.usda.gov/ndb. [April 2019].

Wang, H. L., S. Meng, X. Xiao, P. Long, F.Z. Pan, K.M. Xiao, Y.T. Qi, & S.P. Xiang. 2016. Effects of flavomycin, Bacillus licheniformis and enramycin on performance, nutrient digestibility, gut morphology and the intestinal microflora of broilers. J. Poult. Sci. 53: 128-135. https://doi.org/10.2141/jpsa.0150077

Wang, Y., Q. Yuxuan, Z. Ying, W. Ruiyun, & L. Pinglan. 2019. Antibacterial mechanism of plantaricin LPL-1, a novel class IIa bacteriocin against Listeria monocytogenes. Food Cont. 97: 87-93. http://doi.org/10.1016/j.foodcont.2018.10.025

Wealleans, A. L., M.C. Walsh, L.F. Romero, & V. Ravindran. 2017. Comparative effects of two multi-enzyme combinations and a bacillus probiotic on growth performance, digestibility of energy and nutrients, disappearance of non-starch polysaccharides, and gut microflora in broiler chickens. Poult. Sci. 96:4287-4297. https://doi.org/10.3382/ps/pex226

Wilson, B. & K. Whelan. 2016. Prebiotic inulin-type fructans and galacto -oligosaccharides: definition, specificity, function, and application in gastrointestinal disorders. J. Gastroen. Hepatol. 32 (Suppl. 1): 64-68. https://doi.org/10.1111/jgh.13700

Yan, W., C. Sun, J. Yuan, & N. Yang. 2017. Gut metagenomic analysis reveals prominent roles of lactobacillus and cecal microbiota in chicken feed efficiency. Sci. Rep. 7: 45308. https://doi.org/10.1038/srep45308

Yang, Y., P. Iji, A. Kocher, E. Thomson, L. Mikkelsen, & M. Choct. 2008. Effects of mannanoligosaccharide in broiler chicken diets on growth performance, energy utilization, nutrient digestibility and intestinal microflora. Br. Poult. Sci. 49: 186-194. https://doi.org/10.1080/00071660801998613

Zhang, L., L. Zhang, X. Zeng, L. Zhou, G. Cao, & C. Yang. 2016. Effects of dietary supplementation of probiotic, Clostridium butyricum, on growth performance, immune response, intestinal barrier function, and digestive enzyme activity in broiler chickens challenged with Escherichia coli K88. J. Anim. Sci. Biotechnol. 7: 3. https://doi.org/10.1186/s40104-016-0061-4

Zhu, H., C.A. Hart, D. Sales, & N.B. Roberts. 2006. Bacterial killing in gastric juice- effect of pH and pepsin on Escherichia coli and Helicobacter pylori. J. Med. Microbiol. 55: 1265-1270. https://doi.org/10.1099/jmm.0.46611-0

Authors

H. Julendra
A. Sofyan
M. F. Karimy
Abinawanto Abinawanto
abinawanto.ms@sci.ui.ac.id (Primary Contact)
Yasman Yasman
Author Biographies

H. Julendra, Research Group of Bio-Feed Additive- Research Division for Natural Product Technology (BPTBA)- Indonesian Institute of Sciences (LIPI)

Group Research Bio-Feed Additive

A. Sofyan, Research Group of Bio-Feed Additive Technology, Research Unit for Natural Product Technology (BPTBA), Indonesian Institute of Science (LIPI)

Research Group of Bio-Feed Additive Technology, Research Unit for Natural Product Technology (BPTBA), Indonesian Institute of Science (LIPI)

M. F. Karimy, Research Group of Bio-Feed Additive Technology, Research Unit for Natural Product Technology (BPTBA), Indonesian Institute of Science (LIPI)

Research Group of Bio-Feed Additive Technology, Research Unit for Natural Product Technology (BPTBA), Indonesian Institute of Science (LIPI)

Abinawanto Abinawanto, Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia

Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia

Yasman Yasman, Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia

Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia

JulendraH., SofyanA., KarimyM. F., AbinawantoA., & YasmanY. (2020). Nutrient Utilizations and Intestinal Morphology of Broilers Treated with Lactobacillus plantarum AKK30 – Oligosaccharides Synbiotic. Tropical Animal Science Journal, 43(2), 158-168. https://doi.org/10.5398/tasj.2020.43.2.158

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