Effects of dietary inactivated probiotics on growth performance and immune responses of weaned pigs |
Kang, Joowon
(Division of Animal and Dairy Science, Chungnam National University)
Lee, Jeong Jae (Division of Animal and Dairy Science, Chungnam National University) Cho, Jin Ho (Division of Food and Animal Science, Chungbuk National University) Choe, Jeehwan (Department of Beef Science, Korea National Collage of Agriculture and Fisheries) Kyoung, Hyunjin (Division of Animal and Dairy Science, Chungnam National University) Kim, Sung Hun (CJ CheilJedang Corporation) Kim, Hyeun Bum (Department of Animal Resource, Dankook University) Song, Minho (Division of Animal and Dairy Science, Chungnam National University) |
1 | Patil AK, Kumar S, Verma AK, Baghel RPS. Probiotics as feed additives in weaned pigs: a review. Livest Res Int. 2015;3:31-9. |
2 | Isa K, Oka K, Beauchamp N, Sato M, Wada K, Ohtani K, et al. Safety assessment of the Clostridium butyricum MIYAIRI 588® probiotic strain including evaluation of antimicrobial sensitivity and presence of Clostridium toxin genes in vitro and teratogenicity in vivo. Hum Exp Toxicol. 2016;35:818-32. https://doi.org/10.1177/0960327115607372 DOI |
3 | Boyle RJ, Robins-browne RM, Tang MLK. Probiotic use in clinical practice: what are the risks? Am J Clin Nutr. 2006;83:1256-64. DOI |
4 | Gueimonde M, Sanchez B. Enhancing probiotic stability in industrial processes. Microb Ecol Health Dis. 2012;23:2-6. https://doi.org/10.3402/mehd.v23i0.18562 DOI |
5 | Mottet C, Michetti P. Probiotics: wanted dead or alive. Dig Liver Dis. 2005;37:3-6. https://doi.org/10.1016/j.dld.2004.09.010 DOI |
6 | Adams CA. The probiotic paradox: live and dead cells are biological response modifiers. Nutr Res Rev. 2010;23:37-46. https://doi.org/10.1017/S0954422410000090 DOI |
7 | Lahtinen SJ. Probiotic viability - does it matter? Microb Ecol Health Dis. 2012;23:10-4. https://doi.org/10.3402/mehd.v23i0.18567 DOI |
8 | de Almada CN, Almada CN, Martinez RCR, Sant'Ana AS. Paraprobiotics: evidences on their ability to modify biological responses, inactivation methods and perspectives on their application in foods. Trends Food Sci Technol. 2016;58:96-114. https://doi.org/10.1016/j.tifs.2016.09.011 DOI |
9 | Taverniti V, Guglielmetti S. The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes Nutr. 2011;6:261-74. https://doi.org/10.1007/s12263-011-0218-x DOI |
10 | Ou CC, Lin SL, Tsai JJ, Lin MY. Heat-killed lactic acid bacteria enhance immunomodulatory potential by skewing the immune response toward Th1 polarization. J Food Sci. 2011;76:M260-7. https://doi.org/10.1111/j.1750-3841.2011.02161.x DOI |
11 | Pique N, Berlanga M, Minana-Galbis D. Health benefits of heat-killed (Tyndallized) probiotics: an overview. Int J Mol Sci. 2019;20:2534. https://doi.org/10.3390/ijms20102534 DOI |
12 | Dawood MAO, Koshio S, Ishikawa M, El-Sabagh M, Yokoyama S, Wang WL, et al. Physiological response, blood chemistry profile and mucus secretion of red sea bream (Pagrus major) fed diets supplemented with Lactobacillus rhamnosus under low salinity stress. Fish Physiol Biochem. 2017;43:179-92. https://doi.org/10.1007/s10695-016-0277-4 DOI |
13 | Busanello M, dos Santos Pozza MS, Pozza PC, Nunes RV, Chambo APS, Eckstein II. Probiotics: viable and inactivated cells on the performance, microflora and blood parameters of piglets. Rev Bras Saude e Prod Anim. 2015;16:387-96. https://doi.org/10.1590/S1519-99402015000200013 DOI |
14 | Lan R, Koo J, Kim I. Effects of Lactobacillus acidophilus supplementation on growth performance, nutrient digestibility, fecal microbial and noxious gas emission in weaning pigs. J Sci Food Agric. 2017;97:1310-5. https://doi.org/10.1002/jsfa.7866 DOI |
15 | Uchinaka A, Azuma N, Mizumoto H, Nakano S, Minamiya M, Yoneda M, et al. Anti-inflammatory effects of heat-killed Lactobacillus plantarum L-137 on cardiac and adipose tissue in rats with metabolic syndrome. Sci Rep. 2018;8:1-20. https://doi.org/10.1038/s41598-018-26588-x DOI |
16 | Nishida K, Sawada D, Kuwano Y, Tanaka H, Sugawara T, Aoki Y, et al. Daily administration of paraprobiotic Lactobacillus gasseri CP2305 ameliorates chronic stress-associated symptoms in Japanese medical students. J Funct Foods. 2017;36:112-21. https://doi.org/10.1016/j.jff.2017.06.031 DOI |
17 | Castro-Bravo N, Wells JM, Margolles A, Ruas-Madiedo P. Interactions of surface exopolysaccharides from Bifidobacterium and Lactobacillus within the intestinal environment. Front Microbiol. 2018;9:2426. https://doi.org/10.3389/fmicb.2018.02426 DOI |
18 | Wang Y, Liu Y, Kirpich I, Ma Z, Wang C, Zhang M, et al. Lactobacillus rhamnosus GG reduces hepatic TNFα production and inflammation in chronic alcohol-induced liver injury. J Nutr Biochem. 2013;24:1609-15. https://doi.org/10.1016/j.jnutbio.2013.02.001 DOI |
19 | Oh NS, Joung JY, Lee JY, Kim Y. Probiotic and anti-inflammatory potential of Lactobacillus rhamnosus 4B15 and Lactobacillus gasseri 4M13 isolated from infant feces. PLOS ONE. 2018;13:e0192021. https://doi.org/10.1371/journal.pone.0192021 February DOI |
20 | Ting WJ, Kuo WW, Hsieh DJY, Yeh YL, Day CH, Chen YH, et al. Heat killed Lactobacillus reuteri GMNL-263 reduces fibrosis effects on the liver and heart in high fat diet-hamsters via TGF-β suppression. Int J Mol Sci. 2015;16:25881-96. https://doi.org/10.3390/ijms161025881 DOI |
21 | Yong SJ, Tong T, Chew J, Lim WL. Antidepressive mechanisms of probiotics and their therapeutic potential. Front Neurosci. 2020;13:1361. https://doi.org/10.3389/fnins.2019.01361 DOI |
22 | Moeser AJ, Pohl CS, Rajput M. Weaning stress and gastrointestinal barrier development: implications for lifelong gut health in pigs. Anim Nutr. .2017;3:313-21. https://doi.org/10.1016/j.aninu.2017.06.003 DOI |
23 | Xiao K, Cao ST, Jiao LF, Lin FH, Wang L, Hu CH. Anemonin improves intestinal barrier restoration and influences TGF-β1 and EGFR signaling pathways in LPS-challenged piglets. Innate Immun. 2016;22:344-52. https://doi.org/10.1177/1753425916648223 DOI |
24 | Lee JJ, Kang J, Park S, Cho JH, Oh S, Park DJ, et al. Effects of dietary protease on immune responses of weaned pigs. J Anim Sci Technol. 2020;62:174-9. https://doi.org/10.5187/jast.2020.62.2.174 DOI |
25 | Bloise E, Torricelli M, Novembri R, Borges LE, Carrarelli P, Reis FM, et al. Heat-killed Lactobacillus rhamnosus GG modulates urocortin and cytokine release in primary trophoblast cells. Placenta. 2010;31:867-72. https://doi.org/10.1016/j.placenta.2010.04.007 DOI |
26 | Wang Y, Gong L, Wu YP, Cui ZW, Wang YQ, Huang Y, et al. Oral administration of Lactobacillus rhamnosus GG to newborn piglets augments gut barrier function in pre-weaning piglets. J Zhejiang Univ Sci B. 2019;20:180-92. https://doi.org/10.1631/jzus.B1800022 DOI |
27 | Li XQ, Zhu YH, Zhang HF, Yue Y, Cai ZX, Lu QP, et al. Risks associated with high-dose Lactobacillus rhamnosus in an Escherichia coli model of piglet diarrhoea: intestinal microbiota and immune imbalances. PLOS ONE. 2012;7:e40666. https://doi.org/10.1371/journal.pone.0040666 DOI |
28 | Trevisi P, Casini L, Coloretti F, Mazzoni M, Merialdi G, Bosi P. Dietary addition of Lactobacillus rhamnosus GG impairs the health of Escherichia coli F4-challenged piglets. Animal. 2011;5:1354-60. https://doi.org/10.1017/S1751731111000462 DOI |
29 | Dawood MAO, Koshio S, Ishikawa M, El-Sabagh M, Esteban MA, Zaineldin AI. Probiotics as an environment-friendly approach to enhance red sea bream, Pagrus major growth, immune response and oxidative status. Fish Shellfish Immunol. 2016;57:170-8. https://doi.org/10.1016/j.fsi.2016.08.038 DOI |
30 | Li N, Russell WM, Douglas-Escobar M, Hauser N, Lopez M, Neu J. Live and heat-killed Lactobacillus rhamnosus GG: effects on proinflammatory and anti-inflammatory cytokines/chemokines in gastrostomy-fed infant rats. Pediatr Res. 2009;66:203-7. https://doi.org/10.1203/PDR.0b013e3181aabd4f DOI |
31 | NRC [National Research Council]. Nutrient requirement of swine. 11th ed. Washington, DC: National Academy Press; 2012. |
32 | Bocourt R, Savon L, Diaz J, Brizuela MA, Serrano P, Prats A, et al. Effect of the probiotic activity of Lactobacillus rhamnosus on productive and health indicators of piglets. Cuba J Agric Sci. 2004;38:75-9. |
33 | Food and Agriculture Organization of the United Nations [FAO]. Probiotics in animal nutrition - production, impact and regulation. Rome: FAO; 2016. FAO Animal Production and Health Paper No. 179. |
34 | Lee JJ, Choi SH, Cho JH, Choe J, Kang J, Kim S, et al. Effects of dietary carbohydrases on productive performance and immune responses of lactating sows and their piglets. J Anim Sci Technol. 2019;61:359-65. https://doi.org/10.5187/jast.2019.61.6.359 DOI |
35 | Park S, Lee JJ, Yang BM, Cho JH, Kim S, Kang J, et al. Dietary protease improves growth performance, nutrient digestibility, and intestinal morphology of weaned pigs. J Anim Sci Technol. 2020;62:21-30. https://doi.org/10.5187/jast.2020.62.1.21 DOI |
36 | AOAC [Association of Official Analytical Chemists]. International. Official methods of analysis of AOAC International. Gaithersburg, MD: AOAC International; 2005. |
37 | Sewaka M, Trullas C, Chotiko A, Rodkhum C, Chansue N, Boonanuntanasarn S, et al. Efficacy of synbiotic Jerusalem artichoke and Lactobacillus rhamnosus GG-supplemented diets on growth performance, serum biochemical parameters, intestinal morphology, immune parameters and protection against Aeromonas veronii in juvenile red tilapia (Oreochromis spp.). Fish Shellfish Immunol. 2019;86:260-8. https://doi.org/10.1016/j.fsi.2018.11.026 DOI |
38 | Basu S, Chatterjee M, Ganguly S, Chandra PK. Effect of Lactobacillus rhamnosus GG in persistent diarrhea in Indian children: a randomized controlled trial. J Clin Gastroenterol. 2007;41:756-60. https://doi.org/10.1097/01.mcg.0000248009.47526.ea DOI |
39 | Williams CH, David DJ, Iismaa O. The determination of chromic oxide in faeces samples by atomic absorption spectrophotometry. J Agric Sci. 1962;59:381-5. https://doi.org/10.5187/10.1017/S002185960001546X DOI |
40 | Lewis AJ. Digestion and balance techniques in pigs. In: Lewis AJ, Southern LL, editors. Swine nutrition. 2nd ed. Boca Raton, Fl: CRC Press; 2001. p. 903-16. |
41 | di Gioia D, Biavati B. Probiotics and prebiotics in animal health and food safety: conclusive remarks and future perspectives. In: di Gioia D, Biavati B, editors. Probiotics and prebiotics in animal health and food safety. Cham, Switzerland, Swiss: Springer Nature; 2018. p. 269-73. |
42 | Bernardeau M, Vernoux JP, Gueguen M. Safety and efficacy of probiotic lactobacilli in promoting growth in post-weaning Swiss mice. Int J Food Microbiol. 2002;77:19-27. https://doi.org/10.1016/S0168-1605(02)00059-4 DOI |
43 | Zhao PY, Kim IH. Effect of direct-fed microbial on growth performance, nutrient digestibility, fecal noxious gas emission, fecal microbial flora and diarrhea score in weanling pigs. Anim Feed Sci Technol. 2015;200:86-92. https://doi.org/10.1016/j.anifeedsci.2014.12.010 DOI |
44 | Zhang L, Xu YQ, Liu HY, Lai T, Ma JL, Wang JF, et al. Evaluation of Lactobacillus rhamnosus GG using an Escherichia coli K88 model of piglet diarrhoea: effects on diarrhoea incidence, faecal microflora and immune responses. Vet Microbiol. 2010;141:142-8. https://doi.org/10.1016/j.vetmic.2009.09.003 DOI |
45 | Kim JC, Hansen CF, Mullan BP, Pluske JR. Nutrition and pathology of weaner pigs: nutritional strategies to support barrier function in the gastrointestinal tract. Anim Feed Sci Technol. 2012;173:3-16. https://doi.org/10.1016/j.anifeedsci.2011.12.022 DOI |
46 | Tareb R, Bernardeau M, Gueguen M, Vernoux J. In vitro characterization of aggregation and adhesion properties of viable and heat-killed forms of two probiotic Lactobacillus strains and interaction with foodborne zoonotic bacteria, especially Campylobacter jejuni. J Med Microbiol. 2013;62:637-49. https://doi.org/10.1099/jmm.0.049965-0 DOI |
47 | Stein H. Feeding the pigs' immune system and alternatives to antibiotics. In: Proceedings of the 7th London Swine Conference Proceedings; 2007; London, ON, Canada. p. 65-82. |
48 | Patel S, Majumder A, Goyal A. Potentials of exopolysaccharides from lactic acid bacteria. Indian J Microbiol. 2012;52:3-12. https://doi.org/10.1007/s12088-011-0148-8 DOI |
49 | Kelly D. Probiotics in young and newborn animals. J Anim Feed Sci. 1998;7:15-23. https://doi.org/10.22358/jafs/69952/1998 DOI |
50 | Cho JH, Zhao PY, Kim IH. Probiotics as a dietary additive for pigs: a review. J Anim Vet Adv. 2011;10:2127-34. https://doi.org/10.3923/javaa.2011.2127.2134 DOI |
51 | Zhu GQ, Musa HH, Wu SL, Zhu CH, Seri HI. The potential benefits of probiotics in animal production and health. J Anim Vet Adv. 2009;8:313-21. |