Abstract
Calf diarrhea is an important problem that can result in death and which leads to economic losses. Probiotics in the gastrointestinal tract can be effective for the prevention of diarrhea. In this study, some strains were isolated from traditional fermented dairy products (Shubat and Kumiss) and the feces of Holstein calves and heifers. Some probiotic properties were determined using a total of 124 isolates and Lactobacterin-TK2. Most of the isolates and Lactobacterin-TK2 were adversely affected by pH 2.0; however, they maintained their viability at pH 4.0 and 0.3% bile salt. The most effective antifungals on yeast strains were nystatin, voriconazole, and ketoconazole; however, they were resistant to itraconazole and amphotericin B. The majority of LAB strains and Lactobacterin-TK2 were susceptible to penicillin and tetracycline, whereas they were resistant to trimethoprim-sulfamethoxazole. Bacillus spp. strains were susceptible to enrofloxacin, trimethoprim-sulfamethoxazole, and gentamicin but resistant to penicillin. Also, 71% of lactobacilli have high hydrophobicity, whereas other strains have low hydrophobicity or had no hydrophobicity. Antagonistic properties of some selected strains against pathogenic bacteria were examined. All of the LABs inhibited at least one pathogen. The inhibitory effect of yeast strains on pathogens could not be determined. Then, five of the LAB strains were genotypically identified as Enterococcus faecium, one as Lactobacillus casei, and the yeast strains were identified as Saccharomyces cerevisiae and Clavispora lusitaniae. L. casei K2 and S. cerevisiae S430b were selected as superior strains. These strains are capable of being used as a new probiotic candidate following in vivo trials.
Similar content being viewed by others
References
Gulliksen SM, Lie KI, Løken T, Østerås O (2009) Calf mortality in Norwegian dairy herds. J Dairy Sci 92(6):2782–2795. https://doi.org/10.3168/jds.2008-1807
Timmerman HM, Mulder L, Everts H, Van Espen DC, Van Der Wal E, Klaassen G, Rouwers SM, Hartemink R, Rombouts FM, Beynen AC (2005) Health and growth of veal calves fed milk replacers with or without probiotics. J Dairy Sci 88(6):2154–2165. https://doi.org/10.3168/jds.S0022-0302(05)72891-5
Nagashima K, Yasokawa D, Abe K, Nakagawa R, Kitamura T, Miura T, Kogawa S (2010) Effect of a Lactobacillus species on incidence of diarrhea in calves and change of the microflora associated with growth. Biosci Microflora 29(2):97–110. https://doi.org/10.12938/bifidus.29.97
Bazeley K (2003) Investigation of diarrhoea in the neonatal calf. In Pract 25:152–159. https://doi.org/10.1136/inpract.25.3.152
USDA (2008) Dairy 2007, Part III: reference of dairy cattle health and management practices in the United States. Usda:Aphis:Vs.
Constable PD (2004) Antimicrobial use in the treatment of calf diarrhea. J Vet Intern Med 18(1):8–17. https://doi.org/10.1111/j.1939-1676.2004.tb00129.x
Chen J, Ying GG, Deng WJ (2019) Antibiotic residues in food: extraction, analysis, and human health concerns. J Agric Food Chem 67:7569–7586. https://doi.org/10.1021/acs.jafc.9b01334
Marshall BM, Levy SB (2011) Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev 24(4):718–733. https://doi.org/10.1128/CMR.00002-11
Dobrzanska DA, Lamaudière MTF, Rollason J, Acton L, Duncan M, Compton S, Simms J, Weedall GD, Morozov IY (2019) Preventive antibiotic treatment of calves: emergence of dysbiosis causing propagation of obese state-associated and mobile multidrug resistance-carrying bacteria. Microb Biotechnol. https://doi.org/10.1111/1751-7915.13496
Zeng Z, Zhang S, Wang H, Piao X (2015) Essential oil and aromatic plants as feed additives in non-ruminant nutrition: a review. J Anim Sci Biotechnol 6(1):7. https://doi.org/10.1186/s40104-015-0004-5
Ozkaya S, Erbas S, Ozkan O, Baydar H, Aksu T (2018) Effect of supplementing milk replacer with aromatic oregano (Oreganum onites L.) water on performance, immunity and general health profiles of Holstein calves. Anim Prod Sci 58(10):1892–1900. https://doi.org/10.1071/AN16574
Uyeno Y, Shigemori S, Shimosato T (2015) Effect of probiotics/prebiotics on cattle health and productivity. Microbes Environ 30(2):126–132. https://doi.org/10.1264/jsme2.me14176
FAO (2016) Probiotics in animal nutrition - production, impact and regulation. In: Bajagai YS, Klieve AV, Dart PJ, Bryden WL, HPS M (eds) . FAO Animal Production and Health. Paper No. 179, Rome
Uyeno Y, Sekiguchi Y, Kamagata Y (2010) rRNA-based analysis to monitor succession of faecal bacterial communities in Holstein calves. Lett Appl Microbiol 51:570–577. https://doi.org/10.1111/j.1472-765X.2010.02937.x
Chaucheyras-Durand F, Durand H (2010) Probiotics in animal nutrition and health. Benef Microbes 1(1):3–9. https://doi.org/10.3920/BM2008.1002
Tulemissova Z, Kassenova G, Myktybaeva R, Kozhakhmetova Z, Urazbekova G (2016) The use of probiotics “Lactobacterin-TK2” in dyspepsia of newborn calves. In: Membership in the WTO:prospects of scientific researches and international technology market” materials of the international scientific-practical conference, pp 295–300
Salminen S, Von Wright A, Morelli L, Marteau P, Brassart D, De Vos WM, Fonden R, Saxelin M, Collins K, Mogensen G, Birkeland SE, Mattila-Sandholm T (1998) Demonstration of safety of probiotics-a review. Int J Food Microbiol 44:93–106. https://doi.org/10.1016/S0168-1605(98)00128-7
Strompfová V, Lauková A, Ouwehand AC (2004) Selection of enterococci for potential canine probiotic additives. Vet Microbiol 100:107–114. https://doi.org/10.1016/j.vetmic.2004.02.002
Kiliç GB, Karahan AG (2010) Identification of lactic acid bacteria isolated from the fecal samples of healthy humans and patients with dyspepsia, and determination of their pH, bile, and antibiotic tolerance properties. J Mol Microbiol Biotechnol 18(4):220–229. https://doi.org/10.1159/000319597
Syal P, Vohra A (2013) Probiotic potential of yeasts isolated from traditional Indian fermented foods. Int J Microbiol Res 5(2):390–398. https://doi.org/10.9735/0975-5276.5.2.390-398
Brashears MM, Jaroni D, Trimble J (2003) Isolation, selection, and characterization of lactic acid bacteria for a competitive exclusion product to reduce shedding of Escherichia coli O157:H7 in cattle. J Food Prot 66(3):355–363. https://doi.org/10.4315/0362-028x-66.3.355
Prasad J, Gill H, Smart J, Gopal PK (1998) Selection and characterisation of Lactobacillus and Bifidobacterium strains for use as probiotics. Int Dairy J 8:993–1002. https://doi.org/10.1016/S0958-6946(99)00024-2
CLSI (2016) M100S: performance standards for antimicrobial susceptibility testing. M100S, 26th edition
CLSI (2009) M44-A2: Method for antifungal disk diffusion susceptibility testing of yeasts; approved guideline—second edition. CLSI Doc. M44-A2(August):29(17)
Maroszyńska M, Kunicka-Styczyńska A, Rajkowska K, Maroszyńska I (2013) Antibiotics sensitivity of Candida clinical and food-borne isolates. Acta Biochim Pol 60(4):719–724. https://doi.org/10.18388/abp.2013_2047
Claudia Otero M, Ocaña VS, Elena Nader-Macías M (2004) Bacterial surface characteristics applied to selection of probiotic microorganisms. In: JFT S, Ragout de Spencer AL (eds) Public health microbiology. Humana Press, New Jersey, pp 435–440
Espeche MC, Otero MC, Sesma F, Nader-Macias MEF (2009) Screening of surface properties and antagonistic substances production by lactic acid bacteria isolated from the mammary gland of healthy and mastitic cows. Vet Microbiol 135(3–4):346–357. https://doi.org/10.1016/j.vetmic.2008.09.078
Edwards U, Emde M (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17(19):7843–7853. https://doi.org/10.1093/nar/17.19.7843
Minitab 17 Statistical Software (2010) Computer software. Minitab, Inc., State College www.minitab.com
Magalhães VJA, Susca F, Lima FS, Branco AF, Yoon I, Santos JEP (2008) Effect of feeding yeast culture on performance, health, and immunocompetence of dairy calves. J Dairy Sci 91(4):1497–1509. https://doi.org/10.3168/jds.2007-0582
Kowalski ZM, Górka P, Schlagheck A, Jagusiak W, Micek P, Strzetelski J (2009) Performance of Holstein calves fed milk-replacer and starter mixture supplemented with probiotic feed additive. J Anim Feed Sci 18:399–411. https://doi.org/10.22358/jafs/66409/2009
An HM, Lee DK, Cha MK, Lee SW, Lee SJ, Kim BS, Ha NJ (2011) Effects of lactic acid bacteria (LAB) supplement on the growth rate and elimination of enteropathogenic bacteria in calves. Biotechnol Biotechnol Equip 25(4):2597–2603. https://doi.org/10.5504/BBEQ.2011.0085
Constable PD, Ahmed AF, Misk NA (2005) Effect of suckling cow’s milk or milk replacer on abomasal luminal pH in dairy calves. J Vet Intern Med 19:97–102. https://doi.org/10.1111/j.1939-1676.2005.tb02665.x
Constable PD, Wittek T, Ahmed AF, Marshall TS, Sen I, Nouri M (2006) Abomasal pH and emptying rate in the calf and dairy cow. XXIV World Buiatrics Congress, Nice, France. http://www.ivis.org. Accessed 10 June 2019
Suárez BJ, Van Reenen CG, Stockhofe N, Dijkstra J, Gerrits WJJ (2007) Effect of roughage source and roughage to concentrate ratio on animal performance and rumen development in veal calves. J Dairy Sci 90:2390–2403. https://doi.org/10.3168/jds.2006-524
Laarman AH, Oba M (2015) Short communication: effect of calf starter on rumen pH of Holstein dairy calves at weaning. J Dairy Sci 94(11):5661–5664. https://doi.org/10.3168/jds.2011-4273
Chen L-S, Ma Y, Maubois J-L, He S-H, Chen L-J, Li H-M (2010) Screening for the potential probiotic yeast strains from raw milk to assimilate cholesterol. Dairy Sci Technol 90(5):537–548. https://doi.org/10.1051/dst/2010001
Sourabh A, Kanwar SS, Sharma PN (2010) Diversity of bacterial probiotics in traditional fermented foods of Western Himalayas. Int J Probiotics Prebiotics 5(4):193–202
Zhang DY, Ji HF, Wang SX, Liu H, Wang J, Wang YM (2019) In vitro characterisation of two Lactobacillus strains and evaluation of their suitability as probiotics for growing-finishing pigs. Anim Prod Sci 59(8):1537–1545. https://doi.org/10.1071/AN17039
Gilliand S, Staley T, Bush L (1984) Importance of bile tolerance of Lactobacillus acidophilus used as dietary adjunct. J Dairy Sci 67:3045–3051. https://doi.org/10.3168/jds.S0022-0302(84)81670-7
Goldin BR, Gorbach SL, Saxelin M, Barakat S, Gualtieri L, Salminen S (1992) Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig Dis Sci 37:121–128. https://doi.org/10.1007/BF01308354
Danielsen M, Wind A (2003) Susceptibility of Lactobacillus spp. to antimicrobial agents. Int J Food Microbiol 82(1):1–11. https://doi.org/10.1016/S0168-1605(02)00254-4
Mathur S, Singh R (2005) Antibiotic resistance in food lactic acid bacteria - a review. Int J Food Microbiol 105(3):281–295. https://doi.org/10.1016/j.ijfoodmicro.2005.03.008
Klein G (2003) Taxonomy, ecology and antibiotic resistance of enterococci from food and the gastro-intestinal tract. Int J Food Microbiol 88:123–131. https://doi.org/10.1016/S0168-1605(03)00175-2
Amachawadi RG, Giok F, Shi X, Soto J, Narayanan SK, Tokach MD, Apley MD, Nagaraja TG (2018) Antimicrobial resistance of Enterococcus faecium strains isolated from commercial probiotic products used in cattle and swine. J Anim Sci 96(3):912–920. https://doi.org/10.1093/jas/sky056
Adimpong DB, Sørensen KI, Thorsen L, Stuer-Lauridsen B, Abdelgadir WS, Nielsen DS, Derkx PMF, Jespersen L (2012) Antimicrobial susceptibility of Bacillus strains isolated from primary starters for African traditional bread production and characterization of the bacitracin operon and bacitracin biosynthesis. Appl Environ Microbiol 78(22):7903–7914. https://doi.org/10.1128/aem.00730-12
Gueimonde M, Sánchez B, de los Reyes-Gavilán CG, Margolles A (2013) Antibiotic resistance in probiotic bacteria. Front Microbiol 4:1–6. https://doi.org/10.3389/fmicb.2013.00202
Rochette F, Engelen M, Vanden Bossche H (2003) Antifungal agents of use in animal health - practical applications. J Vet Pharmacol Ther 26(1):31–53. https://doi.org/10.1046/j.1365-2885.2003.00457.x
Vanden Bossche H, Engelen M, Rochette F (2003) Antifungal agents of use in animal health--chemical, biochemical and pharmacological aspects. J Vet Pharmacol Ther 26(1):5–29. https://doi.org/10.1046/j.1365-2885.2003.00456.x
Iliev ID, Leonardi I (2017) Fungal dysbiosis: immunity and interactions at mucosal barriers. Nat Rev Immunol 17(10):635–646. https://doi.org/10.1038/nri.2017.55
Ocaña VS, Bru E, de Ruiz Holgado AAP, Nader-Macias ME (2005) Surface characteristics of lactobacilli isolated from human vagina. J Gen Appl Microbiol 45(5):203–212. https://doi.org/10.2323/jgam.45.203
Maldonado NC, de Ruiz CS, Otero MC, Sesma F, Nader-Macías ME (2012) Lactic acid bacteria isolated from young calves - characterization and potential as probiotics. Res Vet Sci 92(2):342–349. https://doi.org/10.1016/j.rvsc.2011.03.017
Otero MC, Morelli L, Nader-Macías ME (2006) Probiotic properties of vaginal lactic acid bacteria to prevent metritis in cattle. Lett Appl Microbiol 43(1):91–97. https://doi.org/10.1111/j.1472-765X.2006.01914.x
Iñiguez-Palomares C, Pérez-Morales R, Acedo-Félix E (2008) Evaluation of probiotic properties in Lactobacillus isolated from small intestine of piglets. Rev Latinoam Microbiol 49(3–4):46–54
Koshikawa T, Yamazaki M, Yoshimi M, Ogawa S, Yamada A, Watabe K, Torii M (1989) Surface hydrophobicity of spores of Bacillus spp. J Gen Microbiol 135:2717–2722. https://doi.org/10.1099/00221287-135-10-2717
Wiencek KM, Klapes NA, Foegeding PM (1990) Hydrophobicity of Bacillus and Clostridium spores. Appl Environ Microbiol 56(9):2600–2605
Ezequiel B, Porfírio C, Ribeiro CL, Oliveira MDS, Ribeiro EL (2017) Cell surface hydrophobicity and biofilm formation of Candida yeast species in different culture media. Biosci J 33(3):739–746. https://doi.org/10.14393/BJ-v33n3-34770
Abdullah M, Akter MR, Kabir SML, Khan MAS, Ibne MS, Aziz A (2013) Characterization of bacterial pathogens isolated from calf diarrhoea in Panchagarh District of Bangladesh. J Agric Food Technol 3(6):8–13
Gao Z, Daliri EB-M, Wang J, Liu D, Chen S, Ye X, Ding T (2019) Inhibitory effect of lactic acid bacteria on foodborne pathogens: a review. J Food Prot 82(3):441–453. https://doi.org/10.4315/0362-028x.jfp-18-303
Willard MD, Simpson RB, Cohen ND, Clancy JS (2000) Effects of dietary fructooligosaccharide on selected bacterial populations in feces of dogs. Am J Vet Res 61(7):820–825. https://doi.org/10.2460/ajvr.2000.61.820
Benyacoub J, Pérez PF, Rochat F, Saudan KY, Reuteler G, Antille N, Humen M, De Antoni GL, Cavadini C, Blum S, Schiffrin EJ (2005) Enterococcus faecium SF68 enhances the immune response to Giardia intestinalis in mice. J Nutr 135(5):1171–1176. https://doi.org/10.1093/jn/135.5.1171
Vahjen W, Jadamus A, Simon O (2002) Influence of a probiotic Enterococcus faecium strain on selected bacterial groups in the small intestine of growing Turkey poults. Arch Tierernahr 56(6):419–429. https://doi.org/10.1080/00039420215634
Brugman S, Ikeda-Ohtsubo W, Braber S, Folkerts G, Pieterse CMJ, Bakker PAHM (2018) A comparative review on microbiota manipulation: lessons from fish, plants, livestock, and human. Front Nutr 5:1–15. https://doi.org/10.3389/fnut.2018.00080
Cooper CR (2011) Yeasts pathogenic to humans. In: Kurtzman CP, Fell JW, Boekhout T (eds) The Yeasts, A Taxonomic Study, 5th edn. Elsevier B.V, Amsterdam, pp 9–19. https://doi.org/10.1016/B978-0-444-52149-1.00002-1
Laborde JM (2008) Effects of probiotics and yeast culture on rumen development and growth of dairy calves. Dissertation, Louisiana State University
Bakutis B, Baliukonienë V, Paðkevièius A (2005) Use of biological method for detoxification of mycotoxins. Bot Lith Suppl 7:123–129
Sretenovic L, Petrovic M, Aleksic S, Pantelic V, Katic V, Bogdanovic V, Beskorovajni R (2009) Influence of yeast, probiotics and enzymes in rations on dairy cows performances during transition. Biotechnol Anim Husb 24(5–6):33–43. https://doi.org/10.2298/bah0806033s
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Boranbayeva, T., Karahan, A.G., Tulemissova, Z. et al. Properties of a New Probiotic Candidate and Lactobacterin-TK2 Against Diarrhea in Calves. Probiotics & Antimicro. Prot. 12, 918–928 (2020). https://doi.org/10.1007/s12602-020-09649-4
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12602-020-09649-4