Selection and characterization of probiotic lactic acid bacteria and its impact on growth, nutrient digestibility, health and antioxidant status in weaned piglets

PLoS ONE

Volumn 13, Issue 3, 2018, Pages

  Dowarah, Runjun ^b   Verma, Ashok Kumar ^a   Agarwal, Neeta ^a   Singh, Putan ^a   Singh, Bhoj Raj ^a  

^a INDIAN VETERINARY RESEARCH INSTITUTE   (India)

^b ASSAM AGRICULTURAL UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AZITHROMYCIN; BILE SALT; CEFALOTIN; CHLORAMPHENICOL; CIPROFLOXACIN; CLINDAMYCIN; COTRIMOXAZOLE; ERYTHROMYCIN; GATIFLOXACIN; LINCOMYCIN; OFLOXACIN; PENICILLIN DERIVATIVE; PROBIOTIC AGENT; RNA 16S; VANCOMYCIN; ANTIINFECTIVE AGENT; ANTIOXIDANT;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; AREOMONAS VEONII; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ISOLATE; BACTERIUM ISOLATION; BODY WEIGHT GAIN; BORDETELLA; BORDETELLA BRONCHIOSEPTICA; CELL ADHESION; CELL SURFACE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DIGESTION; ENZYME ACTIVITY; ESCHERICHIA COLI; FECES ANALYSIS; GROWTH INHIBITION; HEALTH STATUS; HOST RANGE; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; KLEBSIELLA OXYTOCA; LACTIC ACID BACTERIUM; LACTOBACILLUS ACIDOPHILUS; NONHUMAN; PEDIOCOCCUS ACIDILACTICI; PH; PHYLOGENY; PIGLET; PROTEOBACTERIA; PROTEUS MIRABILIS; SALMONELLA ENTERICA SEROVAR ENTERITIDIS; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; STAPHYLOCOCCUS; STAPHYLOCOCCUS CHROMOGENES; STAPHYLOCOCCUS INTERMEDIUS; ANIMAL; ANIMAL FOOD; BODY WEIGHT; CLASSIFICATION; DIET; FECES; GENETICS; LACTOBACILLALES; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PHYSIOLOGY; PIG; SPECIES DIFFERENCE; WEANING;

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIOXIDANTS; BODY WEIGHT; DIET; DIGESTION; FECES; LACTOBACILLALES; MICROBIAL SENSITIVITY TESTS; PHYLOGENY; PROBIOTICS; RNA, RIBOSOMAL, 16S; SPECIES SPECIFICITY; SWINE; WEANING;

EID: 85043459439     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0192978     Document Type: Article

References (67)

1. Smith AL, Stalder KJ, Serenius TV, Baas TI, Mabry JW. Effect of weaning age on nursery pig and sow reproductive performance. J. Swine Health Prod. 2008; 16, 131–137.
2. Jin LZ, Ho YW, Abdullah N, Jalaludin S. Growth performance, intestinal microbial populations and serum cholesterol of broilers fed diets containing Lactobacillus cultures. Poult. Sci. 1998; 77, 1259–1265. https://doi.org/10.1093/ps/77.9.1259 PMID: 9733111
3. FAO/WHO. Guidelines for the evaluation of probiotics in food Report of a Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food Ontario Canada April 30 and May 1 2002; pp.1–11.
4. Singh BR. Axone, a probiotic for pigs promotes growth rate in grower and suckling piglets of large black breed. 2013; https://www.notoare.com/index.php/11591615
5. De Angelis, Siragusa M, Berloco S, Caputo M, Settanni L, Alfonsi L, et al. Selection of potential probiotic lactobacilli from pig feces to be used as additives in pelleted feeding. Res. Microbiol. 2006; 157, 792–801. https://doi.org/10.1016/j.resmic.2006.05.003 PMID: 16844349
6. Pringsulaka O, Rueangyotchanthana K, Suwannasai N, Watanapokasin N, Amnueysit P, Sunthornthummas S, et al. In vitro screening of lactic acid bacteria for multi-strain probiotics. Livest. Sci. 2015; 174, 66–73.
7. Balasingham K, Valli C, Radhakrishnan L, Balasuramanyam D. Probiotic characterization of lactic acid bacteria isolated from swine intestine. Vet. World 2017; 10(7), 825–829. https://doi.org/10.14202/vetworld.2017.825-829 PMID: 28831230
8. Chiang ML, Chen HC, Chen KN, Lin YC, Lin YT, Chen MJ. Optimizing production of two potential probiotic Lactobacilli strains isolated from piglet feces as feed additives for weaned piglets. Asian Australas. J. Anim. Sci. 2015; 8(8), 1163–1170.
9. Wang AN, Yi XW, Yu HF, Dong B, Qiao SY. Free radical scavenging activity of Lactobacillus fermentum in vitro and its anti-oxidative effect on growing–finishing pigs. J. Appl. Microbiol. 2009; 107, 1140–1148. https://doi.org/10.1111/j.1365-2672.2009.04294.x PMID: 19486423
10. Singh K, Kallali B, Kumar A, Thaker V. Probiotics: a review. Asian Pac. J. Trop. Biomed. 2011; 1, 287–290.
11. Yadav R, Puniya AK, Shukla P. Probiotic properties of Lactobacillus plantarum RYPR1 from an indigenous fermented beverage Raabadi. Frontiers in Microbio. 2016; 7, 1683–1691.
12. Dowarah R, Verma AK, Agarwal N. The use of Lactobacillus as an alternative of antibiotic growth promoters in pigs: a review. Anim. Nutr. 2017; 3, 1–6.
13. Quilodrán-Vega SR, Villena J, Valdebenito J, Salas MJ, Parra C, Ruiz A, et al. Isolation of lactic acid bacteria from swine milk and characterization of potential probiotic strains with antagonistic effects against swine-associated gastrointestinal pathogens. Canadian J. Microbio. 2016; 62(6), 514–524.
14. Dowarah R, Verma AK, Agarwal N, Singh P, Patel BHM. Effect of swine based probiotic on performance, diarrhoea scores, intestinal microbiota and gut health of grower-finisher crossbred pigs. Livest. Sci. 2017; 195, 74–79.
15. Wang J, Ji H, Zhang D, Liu H, Wang S, Shan D, et al. Assessment of probiotic properties of Lactobacillus plantarum ZLP001 isolated from gastrointestinal tract of weaning pigs. Afr. J. Biotechnol. 2011; 10 (54), 11303–11308.
16. Wang J, Ji HF, Wang SX, Zhang DY, Liu H, Shan DC, et al. Lactobacillus plantarum ZLP001: In vitro Assessment of antioxidant capacity and effect on growth performance and antioxidant status in weaning piglets. Asian Austral. J. Anim. Sci. 2012; 25(8), 1153–1158.
17. Dowarah R, Verma AK, Agarwal N, Singh P. Effect of swine based probiotic on growth performance, nutrient utilization and immune status of early weaned grower-finisher crossbred pigs. Anim. Nutr. Feed Technol. 2016; 16(3), 451–461.
18. Cai CJ, Cai PP, Hou CL, Zeng XF, Qiao SY. Administration of Lactobacillus fermentum I5007 to young piglets improved their health and growth. J. Anim. Feed Sci. 2014; 23, 222–227.
19. Onifade AA. Growth performance, carcass characteristics, organ measurements and haematology of broiler chickens fed a high fibre diet supplemented with antibiotics or dried yeast. Die Nahrung. 1997; 41: 370–374.
20. Dong X, Zhang N, Zhou M, Tu Y, Deng K, Diao Q. Effects of dietary probiotics on growth performance, faecal microbiota and serum profiles in weaned piglets. J. Basic Microbiol. 2013; 49(2), 220–226.
21. Gilliland SE, Nelson CR, Maxwell C. Assimilation of cholesterol by Lactobacillus acidophilus. Appl. Environ. Microbiol. 1985; 49, 377–381. PMID: 3920964
22. Dowarah R, Verma AK, Agarwal N, Singh P. Efficacy of species-specific probiotic Pediococcus acidilactici FT28 on blood biochemical profile, carcass traits and physicochemical properties of meat in fattening pigs. Res. Vet. Sci. 2018 (in press accepted).
23. Mishra DK, Verma AK, Agarwal N, Mondal SK, Singh P. Effect of dietary supplementation of probiotics on growth performance, nutrients digestibility and faecal microbiology in weaned piglets. Anim. Nutr. Feed Technol. 2014; 14(2), 283–290.
24. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011; 28, 2731–2739. https://doi.org/10.1093/molbev/msr121 PMID: 21546353
25. Lane DJ. 16S/23S rRNA sequencing. In Stackebrandt E. and Goodfellow M. (ed.), Nucleic acid techniques in bacterial systematics. John Wiley & Sons, New York, NY. p. 115–147; 1991.
26. Heilig HGHJ Zoetendal EG, Vaughan EE, Marteau P, Akkermans ADL, Willem MV. Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl. Environ. Microbiol. 68(1), 2002; 114–123. https://doi.org/10.1128/AEM.68.1.114-123.2002 PMID: 11772617
27. Du Toit M, Franz PAMC, Dicks TML, Schillinger U, Haberer P, Warlies B. et al. Characterization and selection of probiotic lactobacilli for a preliminary minipig feeding trial and their effect on serum cholesterol levels, faeces pH and faeces moisture content. Int. J. Food Microbiol. 1998; 40, 93–104. PMID: 9600615
28. Gotcheva V, Hristozova E, Hristozova T, Guo M, Roshkova Z, Angelov A. Assessment of potential probiotic properties of lactic acid bacteria and yeast strains. Food Biotechnol. 2002; 16, 211–225.
29. Palomares IC, Morales PR, Felix AE. Evaluation of probiotic properties in Lactobacillus isolated from small intestine of piglets. Revista Latinoamericana de Microbiologia. 2007; 49 (3–4), 46–54.
30. Vlkova E, Rada V, Popelarova P, Trojanova I, Killer J. Antimicrobial susceptibility of Bifidobacteria isolated from gastrointestinal tract of calves. Livest. Sci. 2006; 105(1–3), 253–259.
31. Kim P, Min J, Chang HY, Kim SJ, Park YH. Probiotic properties of Lactobacillus and Bifidobacterium strains isolated from porcine gastrointestinal tract. Appl. Environ. Microbiol. 2007; 74, 1103–1111.
32. Schillinger U, Lucke KF. Antibacterial activity of Lactobacillus sake isolated from meat. Appl. Environ. Microbiol. 1989; 55(8), 1901–1906. PMID: 2782870
33. Soleimani NA, Kermanshahi RK, Yakhchali B, Nejad TS. Antagonistic activity of probiotic lactobacilli against Staphylococcus aureus isolated from bovine mastitis. Afr. J. Microbiol. Res. 2010; 4(20), 2169–2173.
34. Lim S, Dong-Soon IM. Screening and characterization of probiotic lactic acid bacteria isolated from Korean fermented foods. J. Microbiol. Biotechnol. 2009; 19(2), 178–186. PMID: 19307768
35. Kos B, Uskovic JS, Vukovic S, Impraga MS, Frece J, Matosic S. Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J. Appl. Microbiol. 2003; 94, 981–987. PMID: 12752805
36. NRC. Nutrient Requirements of Swine. 10th Revised edition. National Academy Press, Washington, DC; 1998.
37. Agarwal N, Kamra DN, Chaudhary LC, Agarwal I, Sahoo A, Pathak NN. Microbial status and enzyme profile of crossbred calves fed on different microbial feed additives. Lett. Appl. Microbiol. 2002; 34, 329–336. PMID: 11967054
38. AOAC. Association of official analytical chemists (19th ed.). Gaithersburgh, Maryland, USA: Association of Official Methods of Analysis; 2000.
39. Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 1974; 47, 469–474. PMID: 4215654
40. Menami M, Yoshikawa H. A simplified assay method of superoxide dismutase activity for clinical use. Clin. Chim. Acta. 1979; 92(3), 337–342. PMID: 436274
41. Bergmeyer HU. In: Methods of Enzymatic Analysis. Vol. III, Weinhein, Deer field Beach, Florida, 1983; Pp. 273.
42. Prins HK, Loos JA. Biochemical methods in red cell genetics. Academic Press, London, 1969; Pp, 127–129.
43. Choubey M, Pattanaik AK, Baliyan S, Dutta N, Jadhav SE, Sharma K. Dietary supplementation of a novel phytogenic feed additive: effects on nutrient metabolism, antioxidant status and immune response of goats. Anim. Prod. Sci. 2015; https://doi.org/10.1071/AN14770
44. Duncan DB. Multiple range and multiple F-test. Biometrics 1995; II, 1–42.
45. Jassim RAMA. Lactobacillus ruminis is a predominant lactic acid producing bacterium in the caecum and rectum of the pig. Lett. Appl. Microbiol. 2003; 37(3), 213–217. PMID: 12904222
46. Ahn YT, Lim KL, Ryu JC, Kang DK, Ham JS, Jang YH et al. Characterization of Lactobacillus acidophilus isolated from Piglets and Chicken. Asian-Aust. J. Anim. Sci. 2002; 15(12), 1790–1797.
47. Du Toit M, Dicks LMT, Holzapfe WH. Identification of hetero-fermentative lactobacilli isolated from pig faeces by numerical analysis of total soluble cell protein patterns and RAPD- PCR. Lett. Appl. Microbiol. 2003; 37, 12–16. PMID: 12803548
48. Ashmaig A, Hasan A, Gaali EEL. Identification of lactic acid bacteria isolated from traditional Sudanese fermented camel’s milk (Gariss). Afr. J. Microbiol. Res. 2009; 3(8), 451–457.
49. Saarela M, Mogensen G, Fondén R, Matto J, Sandholm TM. Probiotic bacteria: safety, functional and technological properties. J. Biotech. 2000; 84, 197–215.
50. Ouwehand AC, Kirjavainen PV, Shortt C, Salminen S. Probiotics: mechanisms and established effects. Int. Dairy J. 1999; 9, 43–52.
51. Guerra NP, Bernardez PF, Mensez J, Cachaldora P, Castro LP. Production of four potentially probiotic lactic acid bacteria and their evaluation as feed additives for weaned piglets. Anim. Feed Sci. Technol. 2007; 134, 89–107.
52. Barrow PA, Brooker BE, Fuller R, Newport MJ. The attachment of bacteria to the gastric epithelium of the pig and its importance in the micro-ecology of the intestine. J. Appl. Bacteriol. 1980; 48,147–154. PMID: 6246061
53. Taheri HR, Moravej H, Tabandeh F, Zaghari M, Shivazad M. Screening of lactic acid bacteria toward their selection as a source of chicken probiotic. Poult. Sci. 2009; 88, 1586–1593. https://doi.org/10.3382/ps.2009-00041 PMID: 19590072
54. Petsuriyawong B, Khunajakr N. Screening of probiotic lactic acid bacteria from piglet feces. Kasetsart J (Nat. Sci.) 2011; 45, 245–253.
55. Shazali N, Foo HL, Loh TC, Choe DW, Rahim RA. Prevalence of antibiotic resistance in lactic acid bacteria isolated from the faeces of broiler chicken in Malaysia. Gut Pathogens 2014; 6, 1–7. https://doi.org/10.1186/1757-4749-6-1 PMID: 24447766
56. Fairbrother JM, Nadeau E, Gyles CL. Escherichia coli in post weaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Anim. Health Res. Rev. 2005; 6, 17–39. PMID: 16164007
57. Venkatesan S, Kirithika M, Roselin I, Ganesan R, Muthuchelian K. Comparative in vitro and in vivo study of three probiotic organisms, Bifidobacterium sp., Lactobacillus sp., S. Cerevisiae and analyzing its improvement with the supplementation of prebiotics. Int. J. Pl. An. Env.Sci. 2012; 2(2), 94–106.
58. Cho IJ, Lee NK, Hahm YT. Characterization of Lactobacillus spp. isolated from the feces of breast-feeding piglets. J. Biosci. Bioeng. 2009; 108(3), 194–198. https://doi.org/10.1016/j.jbiosc.2009.03.015PMID: 19664551
59. Abbasiliasi S, Tan JS, Ibrahim TAT, Ramanan RN, Vakhshiteh F, Mustafa S, et al. Isolation of Pediococcus acidilacticiKp10 with ability to secrete bacteriocin-like inhibitory substance from milk products for applications in food industry. BMC Microbiol. 2012; https://doi.org/10.1186/1471-2180-12-260PMID: 23153191
60. 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.
61. Shon SK, Hong JW, Min BJ, Lee WB, Kim IH. Effects of Lactobacillus reuteri-based direct-fed microbial supplementation for growing-finishing pigs. Asian Austral. J. Anim. Sci. 2005; 18: 370–374.
62. Balasubramanian B, Lee SI, Kim IH. Inclusion of dietary multi-species probiotic on growth performance, nutrient digestibility, meat quality traits, faecal microbiota and diarrhoea score in growing–finishing pigs. Italian J. Anim. Sci. 2017; 1–7.
63. Friendship RM, Henry HC. Cardiovascular System, Hematology, and Clinical Chemistry. In: Diseases of Swine, Leman AD., Straw B.E., Mengeling W.L., D’Allaire S. and Taylor D.J. (Eds.). Iowa State University Press, Ames, LA. 1992; pp: 3–10.
64. Prieto ML, Laurie OS, Shiau PT, McLoughlin P, O’Donovan O, Rea MC, et al. Evaluation of the efficacy and safety of a marine-derived bacillus strain for use as an in-feed probiotic for newly weaned pigs. PLoS ONE 2014; 9(2): e88599. https://doi.org/10.1371/journal.pone.0088599 PMID: 24586349
65. Hossein AA, Alireza ME, Mohammad R, Majid M. Effects of Bacillus subtilis and Bacillus licheniformis-based probiotic on performance, hematological parameters and blood metabolites in lambs. Intl. J. Food Nutr. Sci. 2014; 3(4): 8–15.
66. Yadav H, Jain S, Sinha PR. Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats. J. Dairy Res. 2008; 75(2), 189–195. https://doi.org/10.1017/S0022029908003129 PMID: 18474136
67. Kumar S, Verma AK, Mondal SK, Gupta M, Patil A, Jangi BL. Effect of live Saccharomyces cerevisiae feeding on serum biochemistry in early weaned cross bred piglets. Vet. World 2012; 5(11), 663–666.