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Ultrasonicated Enterococcus faecium SF68 enhances neutrophil free radical production and udder innate immunity of drying-off dairy cows

Published online by Cambridge University Press:  28 June 2013

Hsing-Yi Peng ,
Attapol Tiantong ,
Shuen-Ei Chen ,
Piya Piamya ,
Wen-Bor Liu ,
Huo-Cheng Peh ,
Jai-Wei Lee ,
Ming-Tsao Chen ,
Hajime Nagahata  and
Chai-Ju Chang
Hsing-Yi Peng
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan, Republic of China
Attapol Tiantong
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan, Republic of China
Shuen-Ei Chen
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan, Republic of China
Piya Piamya
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan, Republic of China
Wen-Bor Liu
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan, Republic of China
Huo-Cheng Peh
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan, Republic of China
Jai-Wei Lee
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan, Republic of China Department of Tropical Agriculture and International Cooperation, National Pingtung University of Science and Technology, Pingtung 912, Taiwan, Republic of China
Ming-Tsao Chen
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan, Republic of China
Hajime Nagahata
Affiliation:
Department of Animal Health, School of Veterinary Medicine, Rakuno Gakuen University, Ebetsu, Hokkaido 069-8501, Japan
Chai-Ju Chang*
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan, Republic of China
*
*For correspondence; e-mail: [email protected]
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Abstract

Proper dry cow management is critical not only for subsequent milk production and fertility but also for mastitis control. A phenomenon of immunosuppression was commonly observed in transition cows, an example being the high susceptibility of the mammary gland during early the dry period to new infectious agents. Polymorphonuclear neutrophils (PMN) play important defence roles in the mammary gland of newly dried cows. One of the bactericidal mechanisms of PMN is through producing reactive oxygen species (ROS), which can be efficiently quantified by chemiluminescence (CL) assay. In the current study, the potential of intramammary application of a commercial Enterococcus faecium SF68 (SF68) product to enhance the local innate immunity of newly dried mammary glands was evaluated based on the CL assay. The preliminary experiments in vitro indicated virtual dose-responsiveness of ROS generation from three different cell preparations, bovine blood PMN, bovine blood PMN pre-conditioned with cow milk, and the post-diapedesis model somatic cells from cow milk, on their exposure to phorbol 12-myristate 13-acetate (PMA), viable SF68, and ultrasonicated SF68, but not dry-heated SF68. Because ultrasonication treatment was found to profoundly enhance the immunogenicity of SF68 in vitro, in the following animal trial, single infusion of either 5 or 10×107 original cfu of ultrasonicated SF68 was randomly applied to the front quarters and phosphate-bufferedsaline (PBS) applied to the rear quarters of each of the four experimental cows on the first day of milk stasis. The results showed that within the first post-infusion week, ultrasonicated SF68 induced a faster and greater (P<0·05) recruitment of PMN into mammary lumen with no apparent local or systemic inflammatory sign. Meanwhile, ultrasonicated SF68 also induced a greater (P<0·05) ROS production in response to PMA challenge by in situ somatic cells of mammary secretion. Taken together, ultrasonicated SF68 modulated ROS generation of bovine neutrophils, and would be a potential enhancer of udder innate immunity in drying-off dairy cows. More thorough work is warranted.

Keywords

Entercoccus faecium SF68drying-off cowmammary glandPMNROS
Type
Research Article
Information
Journal of Dairy Research , Volume 80 , Issue 3 , August 2013 , pp. 349 - 359
Copyright
Copyright © Proprietors of Journal of Dairy Research 2013 

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References

Adams, CA 2010 The probiotic paradox: live and dead cells are biological response modifiers. Nutritional Research Review 23 37–46Google Scholar
Babior, BM, Lambeth, JD & Nauseef, W 2002 The neutrophil NADPH oxidase. Archives of Biochemistry and Biophysics 397 342–344Google Scholar
Bedard, K & Krause, K-H 2007 The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiological Reviews 87 245–313Google Scholar
Beecher, C, Daly, M, Berry, DP, Klostermann, K, Flynn, J, Meaney, W, Hill, C, McCarthy, TV, Ross, RP & Giblin, L 2009 Administration of a live culture of Lactococcus lactis DPC 3147 into the bovine mammary gland stimulates the local host immune response, particularly IL-1β and IL-8 gene expression. Journal of Dairy Research 76 340–348Google Scholar
Broom, LJ, Miller, HM, Kerr, KG & Knapp, JS 2006. Effects of zinc oxide and Enterococcus faecium Sf68 dietary supplementation on the performance, intestinal microbiota and immune status of weaned piglets. Research Veterinary Science 80 45–54Google Scholar
Bybee, SN, Scorza, AV & Lappin, MR 2011 Effect of the probiotic Enterococcus faecium SF68 on presence of diarrhea in cats and dogs housed in an animal shelter. Journal of Veterinary Internal Medicine 25 856–860Google Scholar
Chagunda, MGG, Larsen, T, Bjerring, M & Ingvartsen, KL 2006 L-lactate dehydrogenase and N-acetyl-β-D-glucosaminidase activities in bovine milk as indicators of non-specific mastitis. Journal of Dairy Research 73 431–440CrossRefGoogle ScholarPubMed
Chou, WK, Yu, TC, Chen, SE, Peh, HC, Liu, WB, Chen, MT, Nagahata, H & Chang, CJ 2009 TNF α-mediated plasminogen activation on neutrophils is involved in the high plasmin activity in mammary secretion of drying-off cows. Journal of Dairy Research 76 459–468Google Scholar
Chuang, L, Wu, KG, Pai, C, Hsieh, PS, Tsai, JJ, Yen, JH & Lin, MY 2007 Heat-killed cells of lactobacilli skew the immune response toward T helper 1 polarization in mouse splenocytes and dendritic cell-treated T cells. Journal of Agriculture and Food Chemistry 55 11080–11086CrossRefGoogle Scholar
Cross, AR & Segal, AW 2004 The NADPH oxidase of professional phagocytes – prototype of the NOX electron transport chain systems. Biochimica et Biophysica Acta 1657 1–22CrossRefGoogle ScholarPubMed
Crispie, F, Alonso-Gomez, M, O'Loughlin, C, Klostermann, K, Flynn, J, Arkins, S, Meaney, W, Ross, RP & Hill, C 2008 Intramammary infusion of a live culture for treatment of bovine mastitis: effect of live lactococcus on the mammary immune response. Journal of Dairy Research 75 374–384Google Scholar
Drackley, JK 1999 Biology of dairy cows during the transition period: the final frontier? Journal of Dairy Science 82 2259–2273Google Scholar
Food and Agriculture Organization & World Health Organization 2001 Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria. Report of a Joint FAO/WHO Expert Consultation, Rome: FAOGoogle Scholar
Frola, ID, Pellegrino, MS, Espeche, MC, Giraudo, JA, Nader-Macias, MEF & Bogni, CI 2012 Effects of intramammary inoculation of Lactobacillus perolens CRL 1724 in Lactating cows' udders. Journal of Dairy Research 79 84–92Google Scholar
Heyneman, R, Burvenich, C & Vercauteren, R 1990 Interaction between the respiratory burst activity of neutrophil leucocytes and experimentally induced E. coli mastitis in cows. Journal of Dairy Science 73 985–994Google Scholar
Ho, CH, Chang, CJ, Liu, WB, Peh, HC, Chen, SE, Chen, HY, Chen, MT & Nagahata, H 2010 In situ generation of milk protein-derived peptides in drying-off cows. Journal of Dairy Research 77 487–497Google Scholar
Hoeben, D, Monfardini, E, Burvenich, C & Hamann, J 2000 Treatment of acute Escherichia coli mastitis in cows with enrofloxacin: effect on clinical signs and chemiluminescence of circulating neutrophils. Journal of Dairy Science 67 485–502Google Scholar
Ingvartsen, KL & Andersen, JB 2000 Integration of metabolism and intake regulation: a review focusing on periparturient animals. Journal of Dairy Science 83 1573–1597Google Scholar
Ingvartsen, KL & Friggens, NC 2005 To what extent do variabilities in hormones, metabolites and energy intake explain variability in milk yield? Domestic Animal Endocrinology 29 294–304Google Scholar
Kenny, M, Smidt, H, Mengheri, E & Miller, B 2010 Probiotics-do they have a role in the pig industry? Animal 5 462–470Google Scholar
Kim, SY, Shin, S, Koo, HC, Youn, J-H, Paik, H-D & Park, YH 2010 In vitro antimicrobial effect and in vivo preventive and therapeutic effects of partially purified lantibiotic lacticin NK34 against infection by Staphylococcus species isolated from bovine mastitis. Journal of Dairy Science 93 3610–3615Google Scholar
Klostermann, K, Crispie, F, Flynn, J, Ross, RP, Hill, C & Meaney, W 2008 Intramammary infusion of a live culture of Lactococcus lactis for treatment of bovine mastitis: comparison with antibiotic treatment in field trials. Journal of Dairy Research 75 365–373Google Scholar
McClenahan, D, Fagliari, JJ & Evanson, AO 2000. Role of platelet-activating factor in alveolar septal injury associated with experimentally induced pneumonic pasteurellosis in calves. American Journal of Veterinary Research 61 248–254Google Scholar
Mehrzad, J 2012 Molecular aspects of neutrophils' pivotal role in mammary gland immunity. In: Recent Advances in Immunology to Target Cancer, Inflammation and Infectionsp. pp. 383–422 (Ed. Kanwar, J). Rijeka, Croatia: InTech Europe.Google Scholar
Mehrzad, J, Dosogne, H, Meyer, E & Burvenich, C 2001 Local and systemic effects of endotoxin mastitis on the chemiluminescence of milk and blood neutrophils in dairy cows. Veterinary Research 32 131–144Google Scholar
Mehrzad, J, Duchateau, L& Burvenich, C 2009 Phagocytic and bactericidal activity of blood and milk-resident neutrophils against Staphylococcus aureus in primiparous and multiparous cows during early lactation. Veterinary Microbiology 134 106–112Google Scholar
Paape, MJ, Shafer-Weaver, K, Capuco, AV, Van Oostveldt, K & Burvenich, C 2000 Immune surveillance of mammary tissue by phagocytic cell. Advanced Experimental Medical Biology 480 259–277Google Scholar
Piccinini, R, Bronzo, V, Moroni, P, Luzzago, P & Zecconi, A 1999 Study on the relationship between milk immune factors and Staphylococcus aureus intramammary infections in dairy cows. Journal of Dairy Research 66 501–510CrossRefGoogle Scholar
Ryan, MP, Meaney, WJ, Ross, RP & Hill, C 1998 Evaluation of Lacticin 3147 and a teat seal containing this bacteriocin for inhibition of mastitis pathogens. Applied Environmental Microbiology 64 2287–2290Google Scholar
Ryan, MP, Flynn, J, Hill, C, Ross, RP & Meaney, WJ 1999 The natural food grade inhibitor, Lacticin 3147, reduced the incidence of mastitis after experimental challenge with Streptococcus dysgalactiae in nonlactating dairy cows. Journal of Dairy Science 82 2108–2114Google Scholar
Sakai, Y, Tsukahara, T, Bukawa, W, Matsubara, N & Ushida, K 2006 Cell preparation of Enterococcus faecalis strain EC-12 prevents vancomycin-resistant enterococci colonization in the cecum of newly hatched chicks. Poultry Science 85 273–277Google Scholar
Sakai, Y, Tsukahara, T, Matsubara, N, et al. 2007 A cell wall preparation of Enterococcus faecalis strain EC-12 stimulates b-defensin expression in newly hatched chicks. Animal Science Journal 78 92–97Google Scholar
SAS Institute 2008 SAS/STAT User's Guide. Release 9.2. Cary, NC, USA: SAS Institute Inc.Google Scholar
Scharek, L, Guth, J, Reiter, K, Weyrauch, KD, Taras, D, Schwerk, P, Schierack, P, Schimidt, MFG, Wieler, LH & Tedin, K 2005 Influence of a probiotic Enterococcus faecium strain on development of the immune system of sows and piglets. Veterinary Immunology and Immunopathology 105 151–161Google Scholar
Scharek, L, Guth, J, Filter, M & Schmidt, MFG 2007 Impact of the probiotic bacteria Enterococcus faecium NCIMB 10415 (SF68) and Bacillus cereus var. toyoi NCIMB 40112 on the development of serum IgG and faecal IgA of sows and their piglets. Archives of Animal Nutrition 61 223–234Google Scholar
Sheppard, FR, Kelher, MR, Moore, EE, McLaughlin, NJD, Banerjee, A & Silliman, CC 2005 Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation. Journal of Leukocyte Biology 78 1025–1042Google Scholar
Simpson, KW, Rishniw, M, Bellosa, M, Liotta, J, Lucio, A, Baumgart, M, Czarnecki-Maulden, G, Benyacoub, J & Bowman, D 2009 Influence of Enterococcus faecium SF68 probiotics on Giardiasis in Dogs. Journal of Veterinary Internal Medicine 23 476–481Google Scholar
Sordillo, LM & Streicher, KL 2002 Mammary gland immunity and mastitis susceptibility. Journal of Mammary Gland Biology and Neoplasia 7 135–136Google Scholar
Sun, P, Wang, JQ & Zhang, HT 2010 Effects of Bacillus subtilis natto on performance and immune function of preweaning calves. Journal of Dairy Science 93 5851–5855Google Scholar
Tian, SZ, Chang, CJ, Chiang, CC, Peh, HC, Huang, MC, Lee, JW & Zhao, X 2005 Comparison of morphology, viability and function between blood and milk neutrophils from peak lactating goats. Canadian Journal of Veterinary Research 69 39–45Google Scholar
Tsukahara, T, Bukawa, W, Kan, T & Ushida, K 2005 Effect of a cell preparation of Enterococcus faecalis strain EC-12 on digesta flow and recovery from constipation in a pig model and human subjects. Microbial Ecology in Health and Disease 17 107–113Google Scholar
Vandeputte-Van Messom, G, Burvenich, C, Roets, E, Massart-Leën, AM, Heyneman, R, Kremer, WDJ & Brand, A 1993 Classification of newly calved cows into moderate and severe responders to experimentally induced Escherichia coli mastitis. Journal of Dairy Research 60 19–29Google Scholar
Veir, JK, Knorr, R, Cavadini, C, Sherrill, SJ, Benyacoub, J, Satyaraj, E & Lappin, MR 2007 Effect of supplementation with Enterococcus faecium (SF68) on immune functions in cats. Veterinary Therapeutics 8 229–240Google Scholar
Vila, B, Esteve-Garcia, E & Brufau, J 2010 Probiotic micro-organisms: 100 years of innovation and efficacy; modes of action. World Poultry Science Journal 65 369–380Google Scholar
Yu, TC, Chen, SE, Ho, TH, Peh, HC, Liu, WB, Tiantonga, A, Nagahata, H & Chang, CJ 2012 Involvement of TNF-α and MAPK pathway in the intramammary MMP-9 release via degranulation of cow neutrophils during acute mammary gland involution. Veterinary Immunology and Immunopathology 147 161–169Google Scholar