Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-23T21:52:57.270Z Has data issue: false hasContentIssue false

Concentrations of bovine lactoferrin and citrate in milk during experimental endotoxin mastitis in early- versus late-lactating dairy cows

Published online by Cambridge University Press:  27 August 2010

Paula Hyvönen*
Affiliation:
Department of Biosciences, University of Eastern Finland, PO Box 1627, FI-70211 Kuopio, Finland
Taina Haarahiltunen
Affiliation:
Department of Production Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, FI-04920 Saarentaus, Finland
Tanja Lehtolainen
Affiliation:
Department of Production Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, FI-04920 Saarentaus, Finland
Jouni Heikkinen
Affiliation:
Department of Biosciences, University of Eastern Finland, PO Box 1627, FI-70211 Kuopio, Finland
Ritva Isomäki
Affiliation:
Department of Process and Environmental Engineering, University of Oulu, FI-90014 Oulu, Finland
Satu Pyörälä
Affiliation:
Department of Production Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, FI-04920 Saarentaus, Finland
*
*For correspondence; e-mail: paula.hyvonen@uef.fi

Abstract

Lactoferrin (Lf) is a molecule naturally present in bovine milk that affects the availability and transport systems of iron. Lf also binds endotoxin (lipopolysaccharide, LPS) of Gram-negative bacteria and modulates the immunological response. In the present study, concentrations of bovine Lf (bLf) and citrate in milk were determined in early (EL) and late (LL) lactating dairy cows, using an experimentally induced endotoxin mastitis model and a crossover design. Nine clinically healthy Finnish Ayrshire cows were challenged twice with 100 μg endotoxin infused into one udder quarter. Milk samples were collected from the challenged and control quarters of each cow before and after endotoxin infusion during 3 d, and bLf and citrate concentrations were measured. In all cows, clinical signs of mastitis were seen at both times of challenge, but the response was more severe in EL than in LL. Concentration of bLf in the milk started to rise approximately 8 h after endotoxin infusion and was still higher than normal on the third day, especially in the late-lactating cows. In milk of the LL group, concentrations of bLf were significantly higher than in the EL group. In contrast, concentrations of citrate were higher in milk of the EL cows compared with the LL cows. Concentration of bLf and citrate varied substantially among cows. The molar ratio of citrate to bLf before and after challenge was significantly higher during the EL period. The results of this study partly explain why cows in early lactation are more susceptible to intramammary infections and why mastitis is more severe in them.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Appelmelk, BJ, An, Y-Q, Geerts, M, Thijs, BG, de Boer, HA, MacLaren, DM, de Graaff, J & Nuijens, JH 1994 Lactoferrin is a lipid A-binding protein. Infection and Immunity 62 26282632CrossRefGoogle ScholarPubMed
Baker, HM & Baker, EN 2004 Lactoferrin and iron: structural and dynamic aspects of binding and release. Biometals 3 209216CrossRefGoogle Scholar
Bishop, JG, Schanbacher, FL, Ferguson, LC & Smith, KL 1976 In vitro growth inhibition of mastitis-causing coliform bacteria by bovine apo-lactoferrin and reversal of inhibition by citrate and high concentrations of apo-lactoferin. Infection and Immunity 4 911918CrossRefGoogle Scholar
Boulanger, V, Zhao, X & Lacasse, P 2002 Protective effect of melatonin and catalase in bovine neutrophil-induced model of mammary cell damage. Journal of Dairy Science 3 562569CrossRefGoogle Scholar
Brock, JH 2002 The physiology of lactoferrin. Biochemistry and Cell Biology 1 16CrossRefGoogle Scholar
Bruckmaier, RM 2005 Gene expression of factors related to the immune reaction in response to intramammary Escherichia coli lipopolysaccharide challenge. Journal of Dairy Research 72 120124CrossRefGoogle Scholar
Burvenich, C, Bannerman, DD, Lippolis, JD, Peelman, L, Nonnecke, BJ, Kehrli, ME & Paape, MJ 2007 Cumulative physiological events influence the inflammatory response of bovine udder to Esherichia coli infections during the transition period. Journal of Dairy Science 90 (Suppl 1) 3954CrossRefGoogle Scholar
Burvenich, C, Paape, MJ, Hill, AW, Guidry, AJ, Miller, RH, Heyneman, R, Kremer, WD & Brand, A 1994 Role of the neutrophil leucocyte in the local and systemic reactions during experimentally induced E. coli mastitis in cows immediately after calving. Veterinary Quarterly 1 4550CrossRefGoogle Scholar
Chaneton, L, Tirante, L, Maito, J, Chaves, J & Bussmann, LE 2008 Relationship between milk lactoferrin and etiological agent in the mastitic bovine mammary gland. Journal of Dairy Science 5 18651873CrossRefGoogle Scholar
Cheng, JB, Wang, JQ, Bu, DP, Liu, GL, Zhang, CG, Wei, HY, Zhou, LY & Wang, JZ 2008 Factors affecting the lactoferrin concentration in bovine milk. Journal of Dairy Science 3 970976CrossRefGoogle Scholar
Dhillon, KS & Singh, J 2009 Managing chronically mastitic cows. Veterinary Record 6 183184CrossRefGoogle Scholar
Elass-Rochard, E, Roseanu, A, Legrand, D, Trif, M, Salmon, V, Motas, C, Montreuil, J & Spik, G 1995 Lactoferrin-lipopolysaccharide interaction: involvement of the 28–34 loop region of human lactoferrin in the high-affinity binding to Escherichia coli 055B5 lipopolysaccharide. Biochemical Journal 312 839845CrossRefGoogle ScholarPubMed
Faulkner, A & Peaker, M 1982 Reviews of the progress of dairy science: secretion of citrate into milk. Journal of Dairy Research 1 159169CrossRefGoogle Scholar
Garnsworthy, PC, Masson, LL, Lock, AL & Mottram, TT 2006 Variation of milk citrate with stage of lactation and de novo fatty acid synthesis in dairy cows. Journal of Dairy Science 5 16041612CrossRefGoogle Scholar
Gaunt, SN, Raffio, N, Kingsburry, RA, Damon, RA Jr., Johnson, WH & Mitchell, A 1980 Variation of lactoferrin and mastitis and their heritabilities. Journal of Dairy Science 63 18741880CrossRefGoogle ScholarPubMed
Guidry, AJ, Ost, M, Mather, IH, Shainline, WE & Weinland, BT 1983 Sequential response of milk leukocytes, albumin, immunoglobulins, monovalent ions, citrate, and lactose in cows given infusions of Escherichia coli endotoxin into the mammary gland. American Journal of Veterinary Research 12 22622267Google Scholar
Hagiwara, S, Kawai, K, Anri, A & Nagahata, H 2003. Lactoferrin concentrations in milk from normal and subclinical mastitic cows. Journal of Veterinary Medicine Science 3 319323CrossRefGoogle Scholar
Harmon, RJ & Newbould, FSH 1980 Neutrophil leukocyte as a source of lactoferrin in bovine milk. American Journal of Veterinary Research 41 16031606Google Scholar
Hyvönen, P, Suojala, L, Orro, T, Haaranen, J, Simola, O, Rontved, C & Pyörälä, S 2006 Transgenic cows that produce recombinant human lactoferrin in milk are not protected from experimental Escherichia coli intramammary infection. Infection and Immunity 11 62066212CrossRefGoogle Scholar
Isomäki, R 1999 Separation of whey antimicrobial proteins and development of bovine lactoferrin immunoassays. Licenciate thesis, University of Oulu, Oulu, FinlandGoogle Scholar
Kawai, K, Hagiwara, S, Anri, A & Nagahata, H 1999 Lactoferrin concentration in milk of bovine clinical mastitis. Veterinary Research Communications 7 391398CrossRefGoogle Scholar
Kutila, T, Pyörälä, S, Kaartinen, L, Isomäki, R, Vahtola, K, Myllykoski, L & Saloniemi, H 2003 Lactoferrin and citrate concentrations at drying-off and during early mammary involution of dairy cows. Journal of Veterinary Medicine A 7 350353CrossRefGoogle Scholar
Kutila, T, Pyörälä, S, Saloniemi, H & Kaartinen, L 2003 Antibacterial effect of bovine lactoferrin against udder pathogens. Acta Veterinarian Scandinavica 1–2 3542CrossRefGoogle Scholar
Legrand, D, Pierce, A, Elass, E, Carpentier, M, Briand, JP, Mariller, C & Mazurier, J 2008 Lactoferrin structure and functions. Advances in Experimental Medicine and Biology 606 163197CrossRefGoogle ScholarPubMed
Lehtolainen, T, Suominen, S, Kutila, T & Pyörälä, S 2003 Effect of intramammary Escherichia coli endotoxin in early- vs. late-lactating dairy cows. Journal of Dairy Science 7 23272333CrossRefGoogle Scholar
Lehtolainen, T, Røntved, C & Pyörälä, S 2004 Serum amyloid A and TNFα in serum and milk during experimental endotoxin mastitis. Veterinary Research 35 651659CrossRefGoogle ScholarPubMed
Lin, J, Hogan, JS & Smith, KL 1999 Antigenic homology of the inducible ferric citrate receptor (FecA) of coliform bacteria isolated from herds with naturally occurring bovine intramammary infections. Clinical Diagnostic and Laboratory Immunology 6 966969CrossRefGoogle ScholarPubMed
Majewski, T 1986 The level of certain milk components in acute mastitis. Polskie Archiwum Weterynaryjne 1 915Google Scholar
Mehrzad, J, Duchateau, L, Pyörälä, S & Burvenich, C 2002 Blood and milk neutrophil chemiluminescence and viability in primiparous and pluriparous dairy cows during late pregnancy, around parturition and early lactation. Journal of Dairy Science 85 32683276CrossRefGoogle ScholarPubMed
Mutzelburg, I 1979 An enzymatic method for the determination of citrate in milk. Australian Journal of Dairy Technology June 8284Google Scholar
O'Halloran, FO, Bahar, B, Buckley, F, O'Sullivan, O, Sweeney, T & Giblin, L 2009 Characterisation of single nucleotide polymorphisms identified in the bovine lactoferrin gene sequences across a range of dairy cow breeds. Biochimie 91 6875CrossRefGoogle ScholarPubMed
Oliver, SP & Sordillo, LM 1989 Approaches to the manipulation of mammary involution. Journal of Dairy Science 6 16471664CrossRefGoogle Scholar
Oshima, M & Fuse, H 1981 Citric acid concentration in subclinical mastitic milk. Journal of Dairy Research 53 387392CrossRefGoogle Scholar
Peaker, M & Linzell, JL 1975 Citrate in milk: a harbinger of lactogenesis. Nature 5491 464CrossRefGoogle Scholar
Pyörälä, S 2008 Mastitis in postpartum dairy cows. Reproduction of Domestic Animals 43 (Suppl 2) 256259CrossRefGoogle Scholar
Rainard, P 1983 Experimental mastitis with Escherichia coli: kinetics of bacteriostatic and bactericidal activities. Annales de Recherches Veterinaires 1 111Google Scholar
Schanbacher, FL, Goodman, RE & Talhouk, RS 1993 Bovine mammary lactoferrin: implications from messenger ribonucleic acid (mRNA) sequence and regulation contrary to other milk proteins. Journal of Dairy Science 76 38123831CrossRefGoogle ScholarPubMed
Schanbacher, FL & Smith, KL 1975 Formation and role of unusual whey proteins and enzymes: relation to mammary function. Journal of Dairy Science 58 10481062CrossRefGoogle ScholarPubMed
Schmitz, S, Pfaffl, MW, Meyer, HH & Bruckmaier, RM 2004 Short-term changes of mRNA expression of various inflammatory factors and milk proteins in mammary tissue during LPS-induced mastitis. Domestic Animal Endocrinology 2 111126CrossRefGoogle Scholar
Shuster, DE, Harmon, RJ, Jackson, JA & Hemken, RW 1991 Suppression of milk production during endotoxin-induced mastitis. Journal of Dairy Science 74 37633774CrossRefGoogle ScholarPubMed
Shuster, DE, Lee, EK & Kehrli, ME 1996 Bacterial growth, inflammatory cytokine production, and neutrophil recruitment during coliform mastitis in cows within ten days after calving, compared with cows at midlactation. American Journal of Veterinary Research 11 15691575CrossRefGoogle Scholar
Sloth, KH, Friggens, NC, Lovendahl, P, Andersen, PH, Jensen, J & Ingvartsen, KL 2003 Potential for improving description of bovine udder health status by combined analysis of milk parameters. Journal of Dairy Science 86 12211232CrossRefGoogle ScholarPubMed
Soini, E & Lövgren, T 1987 Time-resolved fluorescence of lanthanide probes and application in biotechnology. CRC Critical Reviews in Analytical Chemistry 18 105154CrossRefGoogle Scholar
Suriyasathaporn, W, Heuer, C, Noordhuizen-Stassen, EN & Schukken, YH 2000 Hyperketonemia and the impairment of udder defence: a review. Veterinary Research 31 397412CrossRefGoogle ScholarPubMed
Todhunter, D, Smith, KL & Hogan, JS 1990 Growth of Gram-negative bacteria in dry cow secretion. Journal of Dairy Science 73 363372CrossRefGoogle ScholarPubMed
Tsuji, S, Hirata, Y, Mukai, F & Ohitaki, S 1990 Comparison of lactoferrin content in colostrum between different cattle breeds. Journal of Dairy Science 73 125128CrossRefGoogle ScholarPubMed
Walstra, P 2006 Milk components. In: Dairy Science and Technology. 2nd Edn. (Eds Walstra, P, Wouters, JTM, Geurts, TJ) pp. 17108. Boca Raton, FL USA: CRC Press, Taylor & Francis GroupGoogle Scholar
Vandeputte-Van Messom, G, Burvenich, C, Roets, E, Massrat-Leen, AM, Heyneman, R, Kremer, WD & Brand, A 1993 Classification of newly calved cows into moderate and severe responders to experimentally induced Escherichia coli mastitis. Journal of Dairy Research 60 1929CrossRefGoogle ScholarPubMed
Weinberg, ED 1978 Iron and infection. Microbiological Reviews 1 4566CrossRefGoogle Scholar
Welty, FK, Smith, KL & Schanbacher, FL 1976 Lactoferrin concentration during involution of the bovine mammary gland. Journal of Dairy Science 59 224231CrossRefGoogle ScholarPubMed
Zhao, X & Lacasse, P 2008 Mammary tissue damage during bovine mastitis: causes and control. Journal of Animal Science 13 (Suppl) 5765CrossRefGoogle Scholar