A critical appraisal of probiotics for mastitis control

Frontiers in Veterinary Science

Volumn 5, Issue OCT, 2018, Pages

  Rainard, Pascal ^a   Foucras, Gilles ^b  

^a UNIVERSITÉ DE TOURS   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Dairy ruminants; Immune response; Lactic acid bacteria; Mammary epithelium; Mastitis; Probiotics

Indexed keywords

EID: 85054653017     PISSN: None     EISSN: 22971769     Source Type: Journal    
DOI: 10.3389/fvets.2018.00251     Document Type: Review

References (122)

1. Heikkila AM, Nousiainen JI, Pyorala S. Costs of clinical mastitis with special reference to premature culling. J Dairy Sci. (2012) 95:139-50. doi: 10.3168/jds.2011-4321
2. Huijps K, Lam TJ, Hogeveen H. Costs of mastitis: facts and perception. J Dairy Res. (2008) 75:113-20. doi: 10.1017/S0022029907002932
3. Leslie KE, Petersson-Wolfe CS. Assessment and management of pain in dairy cows with clinical mastitis. Vet Clin N Am Food Anim Pract. (2012) 28:289-305. doi: 10.1016/j.cvfa.2012.04.002
4. De Briyne N, Atkinson J, Pokludova L, Borriello SP. Antibiotics used most commonly to treat animals in Europe. Vet Rec. (2014) 175:325. doi: 10.1136/vr.102462
5. Francoz D, Wellemans V, Dupre JP, Roy JP, Labelle F, Lacasse P, et al. Invited review: a systematic review and qualitative analysis of treatments other than conventional antimicrobials for clinical mastitis in dairy cows. J Dairy Sci. (2017) 100:7751-70. doi: 10.3168/jds.2016-12512
6. Martin P, Barkema HW, Brito LF, Narayana SG, Miglior F. Symposium review: novel strategies to genetically improve mastitis resistance in dairy cattle. J Dairy Sci. (2018) 101:2724-36. doi: 10.3168/jds.2017-13554
7. Deb R, Kumar A, Chakraborty S, Verma AK, Tiwari R, Dhama K, et al. Trends in diagnosis and control of bovine mastitis: a review. Pak J Biol Sci. (2013) 16:1653-61. doi: 10.3923/pjbs.2013.1653.1661
8. Bradley AJ, Breen JE, Payne B, White V, Green MJ. An investigation of the efficacy of a polyvalent mastitis vaccine using different vaccination regimens under field conditions in the United Kingdom. J Dairy Sci. (2015) 98:1706-20. doi: 10.3168/jds.2014-8332
9. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastro Hepat. (2014) 11:506-14. doi: 10.1038/nrgastro.2014.66
10. Joint FAO/WHO working group report on drafting guidelines for the evaluation of probiotics in food. Food and Agricultural Organization of the United Nations and World Health Organization (2002). Available online at: http://www.fao.org/3/a-a0512e.pdf
11. Sanders ME, Benson A, Lebeer S, Merenstein DJ, Klaenhammer TR. Shared mechanisms among probiotic taxa: implications for general probiotic claims. Curr Opin Biotechnol. (2018) 49:207-16. doi: 10.1016/j.copbio.2017.09.007
12. Sanders ME, Lenoir-Wijnkoop I, Salminen S, Merenstein DJ, Gibson GR, Petschow BW, et al. Probiotics and prebiotics: prospects for public health and nutritional recommendations. Ann NY Acad Sci. (2014) 1309:19-29. doi: 10.1111/nyas.12377
13. Arroyo R, Martin V, Maldonado A, Jimenez E, Fernandez L, Rodriguez JM. Treatment of infectious mastitis during lactation: antibiotics versus oral administration of Lactobacilli isolated from breast milk. Clin Infect Dis. (2010) 50:1551-8. doi: 10.1086/652763
14. Fernandez L, Cardenas N, Arroyo R, Manzano S, Jimenez E, Martin V, et al. Prevention of infectious mastitis by oral administration of Lactobacillus salivarius PS2 during late pregnancy. Clin Infect Dis. (2016) 62:568-73. doi: 10.1093/cid/civ974
15. Frola ID, Pellegrino MS, Espeche MC, Giraudo JA, Nader-Macias ME, Bogni CI. Effects of intramammary inoculation of Lactobacillus perolens CRL1724 in lactating cows' udders. J Dairy Res. (2012) 79:84-92. doi: 10.1017/S0022029911000835
16. Klostermann K, Crispie F, Flynn J, Ross RP, Hill C, Meaney W. Intramammary infusion of a live culture of Lactococcus lactis for treatment of bovine mastitis: comparison with antibiotic treatment in field trials. J Dairy Res. (2008) 75:365-73. doi: 10.1017/S0022029908003373
17. Amir LH, Griffin L, Cullinane M, Garland SM. Probiotics and mastitis: evidence-based marketing? Int Breastfeeding J. (2016) 11:19. doi: 10.1186/s13006-016-0078-5
18. Lebeer S, Bron PA, Marco ML, Van Pijkeren JP, O'Connell Motherway M, Hill C, et al. Identification of probiotic effector molecules: present state and future perspectives. Curr Opin Biotechnol. (2018) 49:217-23. doi: 10.1016/j.copbio.2017.10.007
19. Lebeer S, Vanderleyden J, De Keersmaecker SC. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol. (2010) 8:171-84. doi: 10.1038/nrmicro2297
20. Werner B, Moroni P, Gioia G, Lavin-Alconero L, Yousaf A, Charter ME, et al. Short communication: Genotypic and phenotypic identification of environmental streptococci and association of Lactococcus lactis ssp. lactis with intramammary infections among different dairy farms. J Dairy Sci. (2014) 97:6964-9. doi: 10.3168/jds.2014-8314
21. Devriese LA, Hommez J, Laevens H, Pot B, Vandamme P, Haesebrouck F. Identification of aesculin-hydrolyzing streptococci, lactococci, aerococci and enterococci from subclinical intramammary infections in dairy cows. Vet Microbiol. (1999) 70:87-94. doi: 10.1016/S0378-1135(99)00124-8
22. Conlon MA, Bird AR. The impact of diet and lifestyle on gut microbiota and human health. Nutrients (2015) 7:17-44. doi: 10.3390/nu7010017
23. Lebeer S, Vanderleyden J, De Keersmaecker SC. Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev. (2008) 72:728-64. doi: 10.1128/MMBR.00017-08
24. Martin R, Heilig HG, Zoetendal EG, Jimenez E, Fernandez L, Smidt H, et al. Cultivation-independent assessment of the bacterial diversity of breast milk among healthy women. Res Microbiol. (2007) 158:31-7. doi: 10.1016/j.resmic.2006.11.004
25. Oikonomou G, Machado VS, Santisteban C, Schukken YH, Bicalho RC. Microbial diversity of bovine mastitic milk as described by pyrosequencing of metagenomic 16s rDNA. PLoS ONE (2012) 7:e47671. doi: 10.1371/journal.pone.0047671
26. Jimenez E, Fernandez L, Maldonado A, Martin R, Olivares M, Xaus J, et al. Oral administration of Lactobacillus strains isolated from breast milk as an alternative for the treatment of infectious mastitis during lactation. Appl Environ Microbiol. (2008) 74:4650-5. doi: 10.1128/AEM.02599-07
27. Rainard P. Mammary microbiota of dairy ruminants: fact or fiction? Vet Res. (2017) 48:25. doi: 10.1186/s13567-017-0429-2
28. Dobson A, Cotter PD, Ross RP, Hill C. Bacteriocin production: a probiotic trait? Appl Environ Microbiol. (2012) 78:1-6. doi: 10.1128/AEM.05576-11
29. Cotter PD, Ross RP, Hill C. Bacteriocins-a viable alternative to antibiotics? Nat Rev Microbiol. (2013) 11:95-105. doi: 10.1038/nrmicro2937
30. Cursino L, Smajs D, Smarda J, Nardi RMD, Nicoli JR, Chartone-Souza E, et al. Exoproducts of the Escherichia coli strain H22 inhibiting some enteric pathogens both in vitro and in vivo. J Appl Microbiol. (2006) 100:821-9. doi: 10.1111/j.1365-2672.2006.02834.x
31. Svetoch EA, Stern NJ. Bacteriocins to control Campylobacter spp. in poultry-a review. Poult Sci. (2010) 89:1763-8. doi: 10.3382/ps.2010-00659
32. Espeche MC, Otero MC, Sesma F, Nader-Macias ME. Screening of surface properties and antagonistic substances production by lactic acid bacteria isolated from the mammary gland of healthy and mastitic cows. Vet Microbiol. (2009) 135:346-57. doi: 10.1016/j.vetmic.2008.09.078
33. Espeche MC, Pellegrino M, Frola I, Larriestra A, Bogni C, Nader-Macias ME. Lactic acid bacteria from raw milk as potentially beneficial strains to prevent bovine mastitis. Anaerobe (2012) 18:103-9. doi: 10.1016/j.anaerobe.2012.01.002
34. Brooks BW, Barnum DA. The susceptibility of bovine udder quarters colonized with Corynebacterium bovis to experimental infection with Staphylococcus aureus or Streptococcus agalactiae. Can J Comp Med. (1984) 48:146-50. Google Scholar
35. Pankey JW, Nickerson SC, Boddie RL, Hogan JS. Effects of Corynebacterium bovis infection on susceptibility to major mastitis pathogens. J Dairy Sci. (1985) 68:2684-93. doi: 10.3168/jds.S0022-0302(85)81153-X
36. Rainard P, Poutrel B. Effect of naturally occurring intramammary infections by minor pathogens on new infections by major pathogens in cattle. Am J Vet Res. (1988) 49:327-9
37. Blagitz MG, Souza FN, Santos BP, Batista CF, Parra AC, Azevedo LF, et al. Function of milk polymorphonuclear neutrophil leukocytes in bovine mammary glands infected with Corynebacterium bovis. J Dairy Sci. (2013) 96:3750-7. doi: 10.3168/jds.2012-6370
38. Vakkamäki J, Taponen S, Heikkilä AM, Pyörälä S. Bacteriological etiology and treatment of mastitis in Finnish dairy herds. Acta Veter Scand. (2017) 59:33. doi: 10.1186/s13028-017-0301-4
39. Gonçalves JL, Tomazi T, Barreiro JR, Beuron DC, Arcari MA, Lee SHI, et al. Effects of bovine subclinical mastitis caused by Corynebacterium spp. on somatic cell count, milk yield and composition by comparing contralateral quarters. Vet J. (2016) 209:87-92. doi: 10.1016/j.tvjl.2015.08.009
40. Ohland CL, MacNaughton WK. Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastroint Liver Physiol. (2010) 298:G807-19. doi: 10.1152/ajpgi.00243.2009
41. Caballero S, Pamer EG. Microbiota-mediated inflammation and antimicrobial defense in the intestine. Annu Rev Immunol. (2015) 33:227-56. doi: 10.1146/annurev-immunol-032713-120238
42. Melmed G, Thomas LS, Lee N, Tesfay SY, Lukasek K, Michelsen KS, et al. Human intestinal epithelial cells are broadly unresponsive to Toll-like receptor 2-dependent bacterial ligands: implications for host-microbial interactions in the gut. J Immunol. (2003) 170:1406-15. doi: 10.4049/jimmunol.170.3.1406
43. Belkaid Y, Tamoutounour S. The influence of skin microorganisms on cutaneous immunity. Nat Rev Immunol. (2016) 16:353-66. doi: 10.1038/nri.2016.48
44. Nickerson SC, Pankey JW. Cytologic observations of the bovine teat end. Am J Vet Res. (1983) 44:1433-41
45. Goldammer T, Zerbe H, Molenaar A, Schuberth HJ, Brunner RM, Kata SR, et al. Mastitis increases mammary mRNA abundance of beta-defensin 5, toll-like-receptor 2 (TLR2), and TLR4 but not TLR9 in cattle. Clin Diagn Lab Immunol. (2004) 11:174-85. doi: 10.1128/CDLI.11.1.174-185.2004
46. Yang W, Zerbe H, Petzl W, Brunner RM, Günther J, Draing C, et al. Bovine TLR2 and TLR4 properly transduce signals from Staphylococcus aureus and E. coli, but S. aureus fails to both activate NF-kappaB in mammary epithelial cells and to quickly induce TNFalpha and interleukin-8 (CXCL8) expression in the udder. Mol Immunol. (2008) 45:1385-97. doi: 10.1016/j.molimm.2007.09.004
47. Porcherie A, Cunha P, Trotereau A, Roussel P, Gilbert FB, Rainard P, et al. Repertoire of Escherichia coli agonists sensed by innate immunity receptors of the bovine udder and mammary epithelial cells. Vet Res. (2012) 43:14. doi: 10.1186/1297-9716-43-14
48. Wang Y, Zarlenga DS, Paape MJ, Dahl GE. Recombinant bovine soluble CD14 sensitizes the mammary gland to lipopolysaccharide. Vet Immunol Immunopathol. (2002) 86:115-24. doi: 10.1016/S0165-2427(02)00021-1
49. Bougarn S, Cunha P, Harmache A, Fromageau A, Gilbert BF, Rainard P. Muramyl dipeptide synergizes with Staphylococcus aureus lipoteichoic acid to recruit neutrophils in the mammary gland and to stimulate mammary epithelial cells. Clin Vaccine Immunol. (2010) 17:1797-809. doi: 10.1128/CVI.00268-10
50. Lahouassa H, Moussay E, Rainard P, Riollet C. Differential cytokine and chemokine responses of bovine mammary epithelial cells to Staphylococcus aureus and Escherichia coli. Cytokine (2007) 38:12-21. doi: 10.1016/j.cyto.2007.04.006
51. Gilbert FB, Cunha P, Jensen K, Glass EJ, Foucras G, Robert-Granie C, et al. Differential response of bovine mammary epithelial cells to Staphylococcus aureus or Escherichia coli agonists of the innate immune system. Vet Res. (2013) 44:40. doi: 10.1186/1297-9716-44-40
52. Boudjellab N, Chan-Tang HS, Li X, Zhao X. Interleukin 8 response by bovine mammary epithelial cells to lipopolysaccharide stimulation. Am J Vet Res. (1998) 59:1563-7
53. Strandberg Y, Gray C, Vuocolo T, Donaldson L, Broadway M, Tellam R. Lipopolysaccharide and lipoteichoic acid induce different innate immune responses in bovine mammary epithelial cells. Cytokine (2005) 31:72-86. doi: 10.1016/j.cyto.2005.02.010
54. Bannerman DD, Paape MJ, Goff JP, Kimura K, Lippolis JD, Hope JC. Innate immune response to intramammary infection with Serratia marcescens and Streptococcus uberis. Vet Res. (2004) 35:681-700. doi: 10.1051/vetres:2004040
55. Bannerman DD, Paape MJ, Lee JW, Zhao X, Hope JC, Rainard P. Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clin Diagn Lab Immunol. (2004) 11:463-72. doi: 10.1128/CDLI.11.3.463-472.2004
56. Günther J, Czabanska A, Bauer I, Leigh JA, Holst O, Seyfert HM. Streptococcus uberis strains isolated from the bovine mammary gland evade immune recognition by mammary epithelial cells, but not of macrophages. Vet Res. (2016) 47:13. doi: 10.1186/s13567-015-0287-8
57. Bouchard DS, Seridan B, Saraoui T, Rault L, Germon P, Gonzalez-Moreno C, et al. Lactic acid bacteria isolated from bovine mammary microbiota: potential allies against bovine mastitis. PLoS ONE (2015) 10:e0144831. doi: 10.1371/journal.pone.0144831
58. Günther J, Koy M, Berthold A, Schuberth HJ, Seyfert HM. Comparison of the pathogen species-specific immune response in udder derived cell types and their models. Vet Res. (2016) 47:22. doi: 10.1186/s13567-016-0307-3
59. Petersson-Wolfe CS, Wolf SL, Hogan JS. Experimental challenge of bovine mammary glands with Enterococcus faecium during early and late lactation. J Dairy Sci. (2009) 92:3158-64. doi: 10.3168/jds.2008-1755
60. Swanson K, Gorodetsky S, Good L, Davis S, Musgrave D, Stelwagen K, et al. Expression of a beta-defensin mRNA, lingual antimicrobial peptide, in bovine mammary epithelial tissue is induced by mastitis. Infect Immun. (2004) 72:7311-4. doi: 10.1128/IAI.72.12.7311-7314.2004
61. Bougarn S, Cunha P, Gilbert FB, Harmache A, Foucras G, Rainard P. Staphylococcal-associated molecular patterns enhance expression of immune defense genes induced by IL-17 in mammary epithelial cells. Cytokine (2011) 56:749-59. doi: 10.1016/j.cyto.2011.09.020
62. Isobe N, Hosoda K, Yoshimura Y. Immunolocalization of lingual antimicrobial peptide (LAP) in the bovine mammary gland. Anim Sci J. (2009) 80:446-50. doi: 10.1111/j.1740-0929.2009.00652.x
63. Lopez-Meza JE, Gutierrez-Barroso A, Ochoa-Zarzosa A. Expression of tracheal antimicrobial peptide in bovine mammary epithelial cells. Res Vet Sci. (2009) 87:59-63. doi: 10.1016/j.rvsc.2008.12.005
64. Whelehan CJ, Meade KG, Eckersall PD, Young FJ, O'Farrelly C. Experimental Staphylococcus aureus infection of the mammary gland induces region-specific changes in innate immune gene expression. Vet Immunol Immunopathol. (2011) 140:181-9. doi: 10.1016/j.vetimm.2010.11.013
65. Addis MF, Tedde V, Puggioni GMG, Pisanu S, Casula A, Locatelli C, et al. Evaluation of milk cathelicidin for detection of bovine mastitis. J Dairy Sci. (2016) 99:8250-8. doi: 10.3168/jds.2016-11407
66. Smolenski GA, Wieliczko RJ, Pryor SM, Broadhurst MK, Wheeler TT, Haigh BJ. The abundance of milk cathelicidin proteins during bovine mastitis. Vet Immunol Immunopathol. (2011) 143(1-2):125-30. doi: 10.1016/j.vetimm.2011.06.034
67. Cubeddu T, Cacciotto C, Pisanu S, Tedde V, Alberti A, Pittau M, et al. Cathelicidin production and release by mammary epithelial cells during infectious mastitis. Vet Immunol Immunopathol. (2017) 189:66-70. doi: 10.1016/j.vetimm.2017.06.002
68. Rainard P. Experimental mastitis with Escherichia coli: kinetics of bacteriostatic and bactericidal activities. Ann Rech Vet. (1983) 14:1-11
69. Zecconi A, Hamann J, Bronzo V, Moroni P, Giovannini G, Piccinini R. Relationship between teat tissue immune defences and intramammary infections. Adv Exp Med Biol. (2000) 480:287-93. doi: 10.1007/0-306-46832-8_33
70. Hibbitt KG, Benians M. Some effects in-vivo of teat canal and effects in-vitro of cationic proteins on Staphylococci. J Gen Microbiol. (1971) 68:123-8. doi: 10.1099/00221287-68-1-123
71. Klaenhammer TR, Kleerebezem M, Kopp MV, Rescigno M. The impact of probiotics and prebiotics on the immune system. Nat Rev Immunol. (2012) 12:728-34. doi: 10.1038/nri3312
72. Lebeer S, Claes IJ, Vanderleyden J. Anti-inflammatory potential of probiotics: lipoteichoic acid makes a difference. Trends Microbiol. (2011) 20:5-10. doi: 10.1016/j.tim.2011.09.004
73. Bron PA, van Baarlen P, Kleerebezem M. Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat Rev Microbiol. (2011) 10:66-78. doi: 10.1038/nrmicro2690
74. Lopez P, Gonzalez-Rodriguez I, Gueimonde M, Margolles A, Suarez A. Immune response to Bifidobacterium bifidum strains support Treg/Th17 plasticity. PLoS ONE (2011) 6:e24776. doi: 10.1371/journal.pone.0024776
75. Wells JM, Rossi O, Meijerink M, van Baarlen P. Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci USA. (2011) 108(Suppl. 1):4607-14. doi: 10.1073/pnas.1000092107
76. Yang Y, Torchinsky MB, Gobert M, Xiong H, Xu M, Linehan JL, et al. Focused specificity of intestinal TH17 cells towards commensal bacterial antigens. Nature (2014) 510:152-6. doi: 10.1038/nature13279
77. Kehrli ME Jr, Harp JA. Immunity in the mammary gland. Vet Clin North Am Food Anim Pract. (2001) 17:495-516. doi: 10.1016/S0749-0720(15)30003-7
78. Porcherie A, Gilbert FB, Germon P, Cunha P, Trotereau A, Rossignol C, et al. IL-17A is an important effector of the immune response of the mammary gland to Escherichia coli infection. J Immunol. (2016) 196:803-12. doi: 10.4049/jimmunol.1500705
79. Herry V, Gitton C, Tabouret G, Reperant M, Forge L, Tasca C, et al. Local immunization impacts the response of dairy cows to Escherichia coli mastitis. Sci Rep. (2017) 7:3441. doi: 10.1038/s41598-017-03724-7
80. Fry PR, Middleton JR, Dufour S, Perry J, Scholl D, Dohoo I. Association of coagulase-negative staphylococcal species, mammary quarter milk somatic cell count, and persistence of intramammary infection in dairy cattle. J Dairy Sci. (2014) 97:4876-85. doi: 10.3168/jds.2013-7657
81. Vanderhaeghen W, Piepers S, Leroy F, Van Coillie E, Haesebrouck F, De Vliegher S. Invited review: effect, persistence, and virulence of coagulase-negative Staphylococcus species associated with ruminant udder health. J Dairy Sci. (2014) 97:5275-93. doi: 10.3168/jds.2013-7775
82. Pyorala S, Taponen S. Coagulase-negative staphylococci-emerging mastitis pathogens. Vet Microbiol. (2009) 134:3-8. doi: 10.1016/j.vetmic.2008.09.015
83. Lam TJGM, Schukken YH, vanVliet JH, Grommers FJ, Tielen MJM, Brand A. Effect of natural infection with minor pathogens on susceptibility to natural infection with major pathogens in the bovine mammary gland. Am J Vet Res. (1997) 58:17-22
84. Matthews KR, Harmon RJ, Langlois BE. Effect of naturally-occurring coagulase-negative staphylococci infections on new infections by mastitis pathogens in the bovine. J Dairy Sci. (1991) 74:1855-9. doi: 10.3168/jds.S0022-0302(91)78350-1
85. Nascimento JDS, Fagundes PC, Brito MAVD, dos Santos KRN, Bastos MDD. Production of bacteriocins by coagulase-negative staphylococci involved in bovine mastitis. Vet Microbiol. (2005) 106:61-71. doi: 10.1016/j.vetmic.2004.10.014
86. Carson DA, Barkema HW, Naushad S, De Buck J. Bacteriocins of non-aureus Staphylococci Isolated from bovine milk. Appl Environ Microbiol. (2017) 83:e01015-17. doi: 10.1128/AEM.01015-17
87. Brooks BW, Barnum DA, Meek AH. An observational study of Corynebacterium bovis in selected Ontario dairy herds. Can J Comp Med. (1983) 47:73-8
88. Zadoks RN, Allore HG, Barkema HW, Sampimon OC, Wellenberg GJ, Grohn YT, et al. Cow-and quarter-level risk factors for Streptococcus uberis and Staphylococcus aureus mastitis. J Dairy Sci. (2001) 84:2649-63. doi: 10.3168/jds.S0022-0302(01)74719-4
89. Compton CWR, Heuer C, Parker K, McDougall S. Risk factors for peripartum mastitis in pasture-grazed dairy heifers. J Dairy Sci. (2007) 90:4171-80. doi: 10.3168/jds.2006-882
90. Reyher KK, Dohoo IR, Scholl DT, Keefe GP. Evaluation of minor pathogen intramammary infection, susceptibility parameters, and somatic cell counts on the development of new intramammary infections with major mastitis pathogens. J Dairy Sci. (2012) 95:3766-80. doi: 10.3168/jds.2011-5148
91. Timms LL, ed. Can somatic cell counts get too low? 29th Annual Meeting, NMC. Louisville, KY: Natinal Mastitis Council (1990). p. 94-101. Google Scholar
92. Schalm OW, Lasmanis J. The leukocytes: origin and function in mastitis. J Am Vet Med Assoc. (1968) 153:1688-94
93. Piepers S, Opsomer G, Barkema HW, de Kruif A, De Vliegher S. Heifers infected with coagulase-negative staphylococci in early lactation have fewer cases of clinical mastitis and higher milk production in their first lactation than noninfected heifers. J Dairy Sci. (2010) 93:2014-24. doi: 10.3168/jds.2009-2897
94. Piepers S, Schukken YH, Passchyn P, De Vliegher S. The effect of intramammary infection with coagulase-negative staphylococci in early lactating heifers on milk yield throughout first lactation revisited. J Dairy Sci. (2013) 96:5095-105. doi: 10.3168/jds.2013-6644
95. Arboleya S, Ruas-Madiedo P, Margolles A, Solis G, Salminen S, de los Reyes-Gavilan CG, et al. Characterization and in vitro properties of potentially probiotic Bifidobacterium strains isolated from breast-milk. Int J Food Microbiol. (2011) 149:28-36. doi: 10.1016/j.ijfoodmicro.2010.10.036
96. Bouchard DS, Rault L, Berkova N, Le Loir Y, Even S. Inhibition of Staphylococcus aureus invasion into bovine mammary epithelial cells by contact with live Lactobacillus casei. Appl Environ Microbiol. (2013) 79:877-85. doi: 10.1128/AEM.03323-12
97. Malvisi M, Stuknyte M, Magro G, Minozzi G, Giardini A, De Noni I, et al. Antibacterial activity and immunomodulatory effects on a bovine mammary epithelial cell line exerted by nisin A-producing Lactococcus lactis strains. J Dairy Sci. (2016) 99:2288-96. doi: 10.3168/jds.2015-10161
98. Armas F, Camperio C, Marianelli C. In vitro assessment of the probiotic potential of Lactococcus lactis LMG 7930 against ruminant mastitis-causing pathogens. PLoS ONE (2017) 12:e0169543. doi: 10.1371/journal.pone.0169543
99. Pellegrino MS, Frola ID, Natanael B, Gobelli D, Nader-Macias MEF, Bogni CI. in vitro characterization of lactic acid bacteria isolated from bovine milk as potential probiotic strains to prevent bovine mastitis. Probiotics Antimicrob Proteins (2018). doi: 10.1007/s12602-017-9383-6. [Epub ahead of print]
100. Camperio C, Armas F, Biasibetti E, Frassanito P, Giovannelli C, Spuria L, et al. A mouse mastitis model to study the effects of the intramammary infusion of a food-grade Lactococcus lactis strain. PLoS ONE (2017) 12:e0184218. doi: 10.1371/journal.pone.0184218
101. Greene WA, Gano AM, Smith KL, Hogan JS, Todhunter DA. Comparison of probiotic and antibiotic intramammary therapy of cattle with elevated somatic cell counts. J Dairy Sci. (1991) 74:2976-81. doi: 10.3168/jds.S0022-0302(91)78483-X
102. Crispie F, Alonso-Gomez M, O'Loughlin C, Klostermann K, Flynn J, Arkins S, et al. Intramammary infusion of a live culture for treatment of bovine mastitis: effect of live lactococci on the mammary immune response. J Dairy Res. (2008) 75:374-84. doi: 10.1017/S0022029908003385
103. Beecher C, Daly M, Berry DP, Klostermann K, Flynn J, Meaney W, et al. Administration of a live culture of Lactococcus lactis DPC 3147 into the bovine mammary gland stimulates the local host immune response, particularly IL-1beta and IL-8 gene expression. J Dairy Res. (2009) 76:340-8. doi: 10.1017/S0022029909004154
104. Frola ID, Pellegrino MS, Magnano G, Giraudo JA, Espeche MC, Nader-Macias ME, et al. Histological examination of non-lactating bovine udders inoculated with Lactobacillus perolens CRL 1724. J Dairy Res. (2013) 80:28-35. doi: 10.1017/S0022029912000581
105. Pellegrino M, Berardo N, Giraudo J, Nader-Macias MEF, Bogni C. Bovine mastitis prevention: humoral and cellular response of dairy cows inoculated with lactic acid bacteria at the dry-off period. Benef Microbes (2017) 8:589-96. doi: 10.3920/BM2016.0194
106. Mignacca SA, Dore S, Spuria L, Zanghi P, Amato B, Dupre I, et al. Intramammary infusion of a live culture of Lactococcus lactis in ewes to treat staphylococcal mastitis. J Med Microbiol. (2017) 66:1798-810. doi: 10.1099/jmm.0.000641
107. Yu J, Ren Y, Xi XX, Huang WQ, Zhang HP. A novel lactobacilli-based teat disinfectant for improving bacterial communities in the milks of cow teats with subclinical mastitis. Front Microbiol. (2017) 8:1782. doi: 10.3389/fmicb.2017.01782
108. Martin R, Langa S, Reviriego C, Jimenez E, Olivares M, Boza J, et al. The commensal microflora of human milk: new perpectives for food bacteriotherapy and probiotics. Trends Food Sci Technol. (2004) 15:121-7. doi: 10.1016/j.tifs.2003.09.010
109. Perez PF, Dore J, Leclerc M, Levenez F, Benyacoub J, Serrant P, et al. Bacterial imprinting of the neonatal immune system: lessons from maternal cells? Pediatrics (2007) 119:e724-32. doi: 10.1542/peds.2006-1649 CrossRef Full Text
110. Murphy JM, Stuart OM. The effect of introducing small numbers of Streptococcus agalactiae (Cornell 48 strain) directly into the bovine teat cavity. Cornell Vet. (1953) 43:290-310
111. Newbould FHS, Neave FK. The recovery of small numbers of Staphylococcus aureus infused into the bovine teat cistern. J Dairy Res. (1965) 32:157-62. doi: 10.1017/S0022029900018483
112. Hill AW, Shears AL, Hibbitt KG. The elimination of serum-resistant Escherichia coli from experimentally infected single mammary glands of healthy cows. Res Vet Sci. (1978) 25:89-93
113. Plumed-Ferrer C, Uusikyla K, Korhonen J, von Wright A. Characterization of Lactococcus lactis isolates from bovine mastitis. Vet Microbiol. (2013) 167(3-4):592-9. doi: 10.1016/j.vetmic.2013.09.011
114. Woodward WD, Besser TE, Ward AC, Corbeil LB. in vitro growth inhibition of mastitis pathogens by bovine teat skin normal flora. Can J Vet Res. (1987) 51:27-31
115. Braem G, De Vliegher S, Verbist B, Piessens V, Van Coillie E, De Vuyst L, et al. Unraveling the microbiota of teat apices of clinically healthy lactating dairy cows, with special emphasis on coagulase-negative staphylococci. J Dairy Sci. (2013) 96:1499-510. doi: 10.3168/jds.2012-5493
116. Piccinini R, Cesaris L, Dapra V, Borromeo V, Picozzi C, Secchi C, et al. The role of teat skin contamination in the epidemiology of Staphylococcus aureus intramammary infections. J Dairy Res. (2009) 76:36-41. doi: 10.1017/S0022029908003671
117. Charlier C, Cretenet M, Even S, Le Loir Y. Interactions between Staphylococcus aureus and lactic acid bacteria: an old story with new perspectives. Int J Food Microbiol. (2009) 131:30-9. doi: 10.1016/j.ijfoodmicro.2008.06.032
118. Al-Qumber M, Tagg JR. Commensal bacilli inhibitory to mastitis pathogens isolated from the udder microbiota of healthy cows. J Appl Microbiol. (2006) 101:1152-60. doi: 10.1111/j.1365-2672.2006.03004.x
119. Smolenski GA. The Bovine Teat Canal: Its Role in Pathogen Recognition and Defence of the Mammary Gland [PhD]. Universiy of Waikato (2018). Available online at: http://researchcommons.waikato.ac.nz/
120. Paulrud CO. Basic concepts of the bovine teat canal. Vet Res Commun. (2005) 29:215-45. doi: 10.1023/B:VERC.0000047496.47571.41
121. Hoffmann DE, Fraser CM, Palumbo FB, Ravel J, Rothenberg K, Rowthorn V, et al. Probiotics: finding the right regulatory balance. Science (2013) 342:314-5. doi: 10.1126/science.1244656
122. Grzeskowiak L, Isolauri E, Salminen S, Gueimonde M. Manufacturing process influences properties of probiotic bacteria. Br J Nutr. (2011) 105:887-94. doi: 10.1017/S0007114510004496