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Microencapsulation of Lactobacillus plantarum MB001 and its probiotic effect on growth performance, cecal microbiome and gut integrity of broiler chickens in a tropical climate

  • Sasi Vimon (Department of Animal Husbandry, Faculty of Veterinary Science, Chulalongkorn University) ;
  • Kris Angkanaporn (Department of Veterinary Physiology, Faculty of Veterinary Science, Chulalongkorn University) ;
  • Chackrit Nuengjamnong (Department of Animal Husbandry, Faculty of Veterinary Science, Chulalongkorn University)
  • Received : 2022.11.09
  • Accepted : 2023.03.15
  • Published : 2023.08.01

Abstract

Objective: Microencapsulation technologies have been developed and successfully applied to protect the probiotic bacterial cells damaged by environmental exposure. This study aimed to investigate the effects of microencapsulation of Lactobacillus plantarum MB001 on the growth performance, ileal nutrient digestibility, jejunal histomorphology and cecal microbiome of broiler chickens in a tropical climate. Methods: A total of 288 one-day-old female broilers (Ross 308) were randomly allocated into 4 groups (6 replicates of 12 birds). Treatments included, i) a basal diet (NC), ii) NC + avilamycin (10 mg/kg) (PC), iii) NC + non-encapsulated L. plantarum MB001 (1×108 colony-forming unit [CFU]/kg of diet) (N-LP), iv) NC + microencapsulated L. plantarum MB001 (1×108 CFU/kg of diet) (ME-LP). Results: Dietary supplementation of ME-LP improved average daily gain, and feed conversion ratio of broilers throughout the 42-d trial period (p<0.05), whereas ME-LP did not affect average daily feed intake compared with NC group. Both N-LP and ME-LP improved apparent ileal digestibility of crude protein and ether extract compared with NC group (p<0.05). The broilers fed ME-LP supplemented diet exhibited a beneficial effect on jejunal histomorphology of villus height (VH), crypt depth (CD) and villus height to crypt depth ratio (VH:CD) of broilers compared to NC group (p<0.05). At the phylum level, Firmicutes was enriched (p<0.05) and Proteobacteria was decreased (p<0.05) only in the ME-LP group. At the genus level, the ME-LP diets increased (p<0.05) the number of both Lactobacillus and Enterococcus compared to NC, PC, and N-LP groups (p<0.05). Conclusion: Microencapsulation assists the efficient functioning of probiotics. ME-LP could be potentially used as a feed additive for improvement of cecal microbiota, gut integrity and nutrient utilization, leading to better performance of broilers.

Keywords

Acknowledgement

This work was supported by Chulalongkorn University, Thailand Science Research and Innovation (TSRI), and KMP Biotech Company, Thailand. The authors would like to acknowledge the grant of research and researcher for industries (RRI), Thailand (No. PHD60I0005).

References

  1. Attia YA, Al-Harthi MA, Elnaggar A. Productive, physiological and immunological responses of two broiler strains fed different dietary regimens and exposed to heat stress. Ital J Anim Sci 2018;17:686-97. https://doi.org/10.1080/1828051X.2017.1416961
  2. Celi P, Verlhac V, Perez Calvo E, Schmeisser J, Kluenter AM. Biomarkers of gastrointestinal functionality in animal nutrition and health. Anim Feed Sci Technol 2019;250:9-31. https://doi.org/10.1016/j.anifeedsci.2018.07.012 
  3. Lara LJ, Rostagno MH. Impact of heat stress on poultry production. Animal 2013;3:356-69. https://doi.org/10.3390/ani3020356 
  4. Van den Bogaard AE, Stobberingh EE. Epidemiology of resistance to antibiotics: links between animals and humans. Int J Antimicrob Agents 2000;14:327-35. https://doi.org/10.1016/S0924-8579(00)00145-X 
  5. De Vos P, Faas MM, Spasojevic M, Sikkema J. Encapsulation for preservation of functionality and targeted delivery of bioactive food components. Int Dairy J 2010;20:292-302. https://doi.org/10.1016/j.idairyj.2009.11.008 
  6. Mountzouris KC, Tsitrsikos P, Palamidi I, et al. Effects of probiotic inclusion levels in broiler nutrition on growth performance, nutrient digestibility, plasma immunoglobulins, and cecal microflora composition. Poult Sci 2010;89:58-67. https://doi.org/10.3382/ps.2009-00308
  7. Chen H, Li X, Liu B, Meng X. Microencapsulation of Lactobacillus bulgaricus and survival assays under simulated gastrointestinal conditions. J Funct Foods 2017;29:248-55. https://doi.org/10.1016/j.jff.2016.12.015 
  8. Etchepare MA, Raddatz GC, Flores EM, et al. Effect of resistant starch and chitosan on survival of Lactobacillus acidophilus microencapsulated with sodium alginate. LWT - Food Sci Technol 2016;65:511-7. https://doi.org/10.1016/j.lwt.2015.08.039 
  9. Gbassi GK, Vandamme T, Yolou FS, Marchioni E. In vitro effects of pH, bile salts and enzymes on the release and viability of encapsulated Lactobacillus plantarum strains in a gastrointestinal tract model. Int Dairy J 2011;21:97-102. https://doi.org/10.1016/j.idairyj.2010.09.006 
  10. Gebara C, Chaves KS, Ribeiro MCE, Souza FN, Grosso CRF, Gigante ML. Viability of Lactobacillus acidophilus La5 in pectin-whey protein microparticles during exposure to simulated gastrointestinal conditions. Food Res Int 2013;51:872-8. https://doi.org/10.1016/j.foodres.2013.02.008 
  11. Han W, Zhang XL, Wang DW, et al. Effects of microencapsulated Enterococcus fecalis CG1.0007 on growth performance, antioxidation activity, and intestinal microbiota in broiler chickens. J Anim Sci 2013;91:4374-82. https://doi.org/10.2527/jas.2012-5956 
  12. Annan NT, Borza AD, Hansen LT. Encapsulation in alginate-coated gelatin microspheres improves survival of the probiotic Bifidobacterium adolescentis 15703T during exposure to simulated gastro-intestinal conditions. Food Res Int 2008;41:184-93. https://doi.org/10.1016/j.foodres.2007.11.001 
  13. Dajian H, Qiling Q, Yuting Z, Wenjie T, Zhuo Z, Xiaohu Q. Dual-network design to enhance the properties of agar aerogel adsorbent by incorporating in situ ion cross-linked alginate. Environ Chem Lett 2020;18:251-5. https://doi.org/10.1007/s10311-019-00932-7 
  14. Xiubin H, Zhixin X, Yanzhi X, et al. Effect of SiO2 nanoparticle on the physical and chemical properties of eco-friendly agar/sodium alginate nanocomposite film. Int J Biol Macromol 2019;125:1289-98. https://doi.org/10.1016/j.ijbiomac.2018.09.109 
  15. Krasaekoopt W, Watcharapoka S. Effect of addition of inulin and galactooligosaccharide on the survival of microencapsulated probiotics in alginate beads coated with chitosan in simulated digestive system, yogurt and fruit juice. LWT - Food Sci Technol 2014;57:761-6. https://doi.org/10.1016/j.lwt.2014.01.037 
  16. Aviagen. Ross broiler management manual. Midlothian, UK: Aviagen; 2018. 
  17. AOAC International. Official methods of analysis of association of official analytical chemists International. 17th ed. Rockville, MD, USA: AOAC Inter; 2016. 
  18. Angkanaporn K, Ravindran V, Bryden WL. Additivity of apparent and true ileal amino acid digestibilities in soybean meal, sunflower meal, and meat and bone meal for broilers. Poult Sci 1996;75:1098-103. https://doi.org/10.3382/ps.0751098 
  19. Zhang L, Li J, Yun TT, et al. Effects of pre-encapsulated and pro-encapsulated Enterococcus faecalis on growth performance, blood characteristics, and cecal microflora in broiler chickens. Poult Sci 2015;94:2821-30. https://doi.org/10.3382/ps/pev262 
  20. SAS Institute. SAS user's guide: Statistics, version 5 ed. Cary, NC, USA: SAS Institute Inc; 1985. 
  21. Rosenberg M, Lee SJ. Calcium-alginate coated, whey protein-based microspheres: Preparation, some properties and opportunities. J Microencapsul 2004;21:263-81. https://doi.org/10.1080/02652040410001673937 
  22. Rather SA, Akhter R, Masoodi FA, Gani A, Wani SM. Effect of double alginate microencapsulation on in vitro digestibility and thermal tolerance of Lactobacillus plantarum NCDC201 and L. casei NCDC297. Lebensmittel-Wissenschaft and Technologie Food Sci Technol 2017;83:50-8. https://doi.org/10.1016/j.lwt.2017.04.036 
  23. Jahromi MF, Liang JB, Ebrahimi R, et al. Protective potential of Lactobacillus species in lead toxicity model in broiler chickens. Animal 2017;11:755-61. https://doi.org/10.1017/S175173111600224X 
  24. Zulkifli I, Abdullah N, Azrin NM, Ho YW. Growth performance and immune response of two commercial broiler strains fed diets containing Lactobacillus cultures and oxytetracycline under heat stress conditions. Br Poult Sci 2000; 41:593-7. https://doi.org/10.1080/713654979 
  25. Jahromi MF, Altaher YW, Shokryazdan P, et al. Dietary supplementation of a mixture of Lactobacillus strains enhances performance of broiler chickens raised under heat stress conditions. Int J Biometeorol 2016;60:1099-110. https://doi.org/10.1007/s00484-015-1103-x 
  26. Navidshad B, Liang JB, Jahromi MF. Correlation coefficients between different methods of expressing bacterial quantification using real time PCR. Int J Mol Sci 2012;13:2119-32. https://doi.org/10.3390/ijms13022119 
  27. Lee KW, Lee SH, Lillehoj HS, et al. Effects of direct-fed microbials on growth performance, gut morphometry, and immune characteristics in broiler chickens. Poult Sci 2010;89:203-16. https://doi.org/10.3382/ps.2009-00418 
  28. Li LL, Hou ZP, Li TJ, et al. Effects of dietary probiotic supplementation on ileal digestibility of nutrients and growth performance in 1- to 42-day-old broilers. J Sci Food Agric 2008;88:35-42. https://doi.org/10.1002/jsfa.2910 
  29. Zeng Z, Xu X, Zhang Q, et al. Effects of essential oil supplementation of a low-energy diet on performance, intestinal morphology and microflora, immune properties and antioxidant activities in weaned pigs. Anim Sci J 2015;86:279-85. https://doi.org/10.1111/asj.12277 
  30. Thu TV, Loh TC, Foo HL, Yaakub H, Bejo MH. Effects of liquid metabolite combinations produced by Lactobacillus plantarum on growth performance, faeces characteristics, intestinal morphology and diarrhea incidence in postweaning piglets. Trop Anim Health Prod 2011;43:69-75. https://doi.org/10.1007/s11250-010-9655-6 
  31. Awad WA, Bohm J, Razzazi-Fazeli E, Ghareeb K, Zentek J. Effect of addition of a probiotic microorganism to broiler diets contaminated with deoxynivalenol on performance and histological alterations of intestinal villi of broiler chickens. Poult Sci 2006;85:974-9. https://doi.org/10.1093/ps/85.6.974 
  32. Kareem KY, Loh TC, Foo HL, Akit H, Samsudin AA. Effects of dietary postbiotic and inulin on growth performance, IGF1 and GHR mRNA expression, faecal microbiota and volatile fatty acids in broilers. BMC Vet Res 2016;12:163. https://doi.org/10.1186/s12917-016-0790-9 
  33. Obajuluwa OV, Sanwo KA, Egbeyale LT, Fafiolu AO. Performance, blood profile and gut morphometry of broiler chickens fed diets supplemented with Yohimbe (Pausynistalia yohimbe) and Larvacide. Vet Anim Sci 2020;10:100127. https://doi.org/10.1016/j.vas.2020.100127 
  34. Vicente JL, Torres-Rodriguez A, Higgins SE, et al. Effect of a selected Lactobacillus spp.-based probiotic on Salmonella enterica serovar enteritidis-infected broiler chicks. Avian Dis 2008;52:143-6. https://doi.org/10.1637/7847-011107 
  35. Song D, Wang YW, Lu ZX, et al. Effects of dietary supplementation of microencapsulated Enterococcus fecalis and the extract of Camellia oleifera seed on laying performance, egg quality, serum biochemical parameters, and cecal microflora diversity in laying hens. Poult Sci 2019;98:2880-7. https://doi.org/10.3382/ps/pez033 
  36. Suzuki K, Harasawa R, Yoshitake Y, Mitsuoka T. Effects of crowding and heat stress on intestinal flora, body weight gain, and feed efficiency of growing rats and chicks. Nihon Juigaku Zasshi 1983;45:331-8. https://doi.org/10.1292/jvms1939.45.331 
  37. Greiner T, Backhed F. Effects of the gut microbiota on obesity and glucose homeostasis. Trends Endocrinol Metab 2011;22:117-23. https://doi.org/10.1016/j.tem.2011.01.002 
  38. Videnska P, Sedlar K, Lukac M, et al. Succession and replacement of bacterial populations in the caecum of egg laying hens over their whole life. PLoS One 2014;9:e115142. https://doi.org/10.1371/journal.pone.0115142 
  39. Loh T, Thanh N, Foo H, Hair-Bejo M. Effects of feeding metabolite combinations from Lactobacillus plantarum on plasma and breast meat lipids in broiler chickens. Rev Bras Cienc Avic 2013;15:307-16. https://doi.org/10.1590/S1516-635X2013000400004 
  40. Marteau P, Shanahan F. Basic aspects and pharmacology of probiotics: An overview of pharmacokinetics, mechanisms of action and side-effects. Best Pract Res Clin Gastroenterol 2003;17:725-40. https://doi.org/10.1016/s1521-6918(03)00055-6 
  41. Rimoldi S, Lasagna E, Sarti FM, et al. Expression profile of six stress-related genes and productive performances of fast and slow growing broiler strains reared under heat stress conditions. Meta Gene 2015;6:17-25. https://doi.org/10.1016/j.mgene.2015.08.003