Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-22T22:49:38.289Z Has data issue: false hasContentIssue false
  • English
  • Français

Immune response of bovine milk somatic cells to endotoxin in healthy quarters with normal and very low cell counts

Published online by Cambridge University Press:  08 September 2010

Olga Wellnitz ,
Amandine Baumert ,
Machabbat Saudenowa  and
Rupert M Bruckmaier
Olga Wellnitz
Affiliation:
Veterinary Physiology, Vetsuisse Faculty, University of Bern, Bern, Switzerland
Amandine Baumert
Affiliation:
Veterinary Physiology, Vetsuisse Faculty, University of Bern, Bern, Switzerland
Machabbat Saudenowa
Affiliation:
Veterinary Physiology, Vetsuisse Faculty, University of Bern, Bern, Switzerland
Rupert M Bruckmaier*
Affiliation:
Veterinary Physiology, Vetsuisse Faculty, University of Bern, Bern, Switzerland
*
*For correspondence; e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Low somatic cell count (SCC) is a reliable indicator of high-quality milk free of pathogenic microorganisms. Thus, an important goal in dairy practice is to produce milk with low SCC. Selection for cows with low SCC can sometimes lead to extremely low SCC in single quarters. The cells in milk are, however, predominantly immune cells with important immune functions. To investigate the mammary immune competence of quarters with very low SCC, healthy udder quarters of cows with normal SCC of (40–100)×103 cells/ml and very low SCC of <20×103 cells/ml were challenged with lipopolysaccharide (LPS) from Escherichia coli. In the first experiment, SCC and cell viability after a challenge with 50 ng of LPS/quarter was investigated. In the second experiment, tumour necrosis factor α (TNF-α) concentration and lactate dehydrogenase (LDH) activity in milk, and mRNA expression of various innate immune factors in milk cells were measured after a challenge with 100 μg LPS/quarter. LPS challenge induced an increase of SCC. SCC levels reached were higher in quarters with normal SCC and maximum SCC was reached 1 h earlier than in very low SCC quarters. The increase of TNF-α concentrations in milk in response to LPS challenge was lower in quarters with very low SCC than in quarters with normal SCC. The viability of cells and the LDH activity in milk increased in response to LPS challenge, however, without a difference between the groups. The mRNA expression of IL-1β and IL-8 was increased in milk cells at 12 h after LPS challenge, whereas that of TNF-α and lactoferrin was not increased at the measured time points (12, 24 and 36 h after LPS challenge). No differences of mRNA expression of measured immune factors between normal and very low SCC samples were detected. The study showed that udder quarters with very low SCC responded with a less marked increase of SCC compared with quarters with normal SCC. This difference corresponded with simultaneously lower TNF-α concentrations in milk. However, the immune competence of the cells themselves based on mRNA expression of TNF-α, IL-8, IL-1β, and lactoferrin, did not differ. The results may indicate that very low SCC can impair the immune competence of udder quarters, because the immune response in udder quarters with lower SCC is less efficient as fewer cells contribute to the production of immunoregulators.

Keywords

Bovine somatic cellsimmune responseendotoxinSCC
Type
Research Article
Information
Journal of Dairy Research , Volume 77 , Issue 4 , November 2010 , pp. 452 - 459
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

Bannerman, DD, Paape, MJ, Lee, JW, Zhao, X, Hope, JP & Rainard, C 2004 Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clinical and Diagnostic Laboratory Immunology 11 463–472Google ScholarPubMed
Barkema, HW, Schukken, YH, Lam, TJ, Beiboer, ML, Wilmink, H, Benedictus, G & Brand, A 1998 Incidence of clinical mastitis in dairy herds grouped in three categories by bulk milk somatic cell counts. Journal of Dairy Science 81 411–419CrossRefGoogle ScholarPubMed
Beaudeau, F, Fourichon, C, Seegers, H & Bareille, N 2002 Risk of clinical mastitis in dairy herds with a high proportion of low individual milk somatic cell counts. Preventive Veterinary Medicine 53 43–54CrossRefGoogle ScholarPubMed
Blum, JW, Dosogne, H, Hoeben, D, Vangroenweghe, F, Hammon, HM, Bruckmaier, RM & Burvenich, C 2000 Tumor necrosis factor-α and nitrite/nitrate responses during acute mastitis induced by Escherichia coli infection and endotoxin in dairy cows. Domestic Animal Endocrinology 19 223–235CrossRefGoogle ScholarPubMed
Bogin, E & Ziv, G 1973 Enzymes and minerals in normal and mastitic milk. Cornell Veterinarian 63 666–676Google ScholarPubMed
Boutet, P, Boulanger, D, Gillet, L, Vanderplasschen, A, Closset, R, Bureau, F & Lekeux, P 2004 Delayed neutrophil apoptosis in bovine subclinical mastitis. Journal of Dairy Science 87 4104–4114CrossRefGoogle ScholarPubMed
Bruckmaier, RM & Hilger, M 2001 Milk ejection in dairy cows at different degrees of udder filling. Journal of Dairy Research 68 369–376CrossRefGoogle ScholarPubMed
Burvenich, C, Van Merris, V, Mehrzad, J, Diez-Fraile, A & Duchateau, L 2003 Severity of E. coli mastitis is mainly determined by cow factors. Veterinary Research 34 521–564CrossRefGoogle ScholarPubMed
Burvenich, C, Bannerman, DD, Lippolis, JD, Peelman, L, Nonnecke, BJ, Kehrli, ME Jr & Paape, MJ 2007 Cumulative physiological events influence the inflammatory response of the bovine udder to Escherichia coli infections during the transition period. Journal of Dairy Science 90 (Suppl 1) 39–54 ReviewCrossRefGoogle ScholarPubMed
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 91 970–976CrossRefGoogle ScholarPubMed
Deluyker, HA, Gay, JM & Weaver, LD 1993 Interrelationships of somatic cell count, mastitis, and milk yield in a low somatic cell count herd. Journal of Dairy Science 76 3445–3452CrossRefGoogle Scholar
Didier, A & Bruckmaier, RM 2004 mRNA expression of apoptosis-related genes in mammary tissue and milk cells in response to lipopolysaccharide challenge and during subclinical mastitis. Milchwissenschaft 59 119–123Google Scholar
Glick, JH 1969 Serum lactate dehydrogenase isoenzyme and total lactate dehydrogenase values in health and disease, and clinical evaluation of these tests by means of discriminant analysis. American Journal of Clinical Pathology 53 320–328Google Scholar
Green, MJ, Green, LE & Cripps, PJ 1996 Low bulk milk somatic cell counts and endotoxin-associated (toxic) mastitis. Veterinary Record 138 305–306CrossRefGoogle ScholarPubMed
Harmon, RJ & Heald, CW 1982 Migration of polymorphonuclear leukocytes into the bovine mammary gland during experimentally induced Staphylococcus aureus mastitis. American Journal of Veterinary Research 43 992–998Google ScholarPubMed
Harmon, RJ & Newbould, FHS 1980 Neutrophil leukocyte as a source of lactoferrin in bovine milk. American Journal of Veterinary Research 41 1603–1606Google Scholar
Kauf, AC, Vinyard, BT & Bannerman, DD 2006 Effect of intramammary infusion of bacterial lipopolysaccharide on experimentally induced Staphylococcus aureus intramammary infection. Research in Veterinary Science 82 39–46CrossRefGoogle ScholarPubMed
Kehrli, EM & Schuster, DE 1994 Factors affecting milk somatic cells and their role in health of the bovine mammary gland. Journal of Dairy Science 77 619–627CrossRefGoogle ScholarPubMed
Koess, C & Hamann, J 2008 Detection of mastitis in the bovine mammary gland by flow cytometry at early stages. Journal of Dairy Research 75 225–232CrossRefGoogle ScholarPubMed
Lee, JW, Bannerman, DD, Paape, MJ, Huang, MK & Zhao, X 2006 Characterization of cytokine expression in milk somatic cells during intramammary infections with Escherichia coli or Staphylococcus aureus by real-time PCR. Veterinary Research 37 219–229CrossRefGoogle ScholarPubMed
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 32 131–144CrossRefGoogle ScholarPubMed
Mehrzad, J, Duchateau, L & Burvenich, C 2004 Viability of milk neutrophils and severity of bovine coliform mastitis. Journal of Dairy Science 87 4150–4162CrossRefGoogle ScholarPubMed
Nickerson, SC & Pankey, JW 1984 Neutrophil migration through test end tissues of bovine mammary quarters experimentally challenged with Staphylococcus aureus. Journal of Dairy Science 67 826–834CrossRefGoogle ScholarPubMed
Olde Riekerink, RG, Barkema, HW, Veenstra, W, Berg, FE, Stryhn, H & Zadoks, RN 2007 Somatic cell count during and between milkings. Journal of Dairy Science 90 3733–3741CrossRefGoogle ScholarPubMed
Paape, MJ, Guidry, AJ, Kirk, ST & Bolt, DJ 1975 Measurement of phagocytosis of 32P-labeled Staphylococcus aureus by bovine leukocytes: lysostaphin digestion and inhibitory effect of cream. American Journal of Veterinary Research 36 1737–1743Google ScholarPubMed
Paape, MJ & Guidry, AJ 1977 Effect of fat and casein on intracellular killing of Staphylococcus aureus by milk leukocytes. Proceeding of the Society for Experimental Biology and Medicine 155 588–593CrossRefGoogle ScholarPubMed
Paape, MJ, Pearson, RE, Wergin, WP & Guidry, AJ 1977 Enhancement of chemotactic response of polymorphonuclear leukocytes into the mammary gland and isolation from milk. Journal of Dairy Science 60 53–62CrossRefGoogle ScholarPubMed
Paape, MJ, Rautiainen, PM, Lilius, EM, Malstrom, CE & Elsasser, TH 2002 Development of anti-bovine TNF-alpha mAb and ELISA for quantitating TNF-alpha in milk after intramammary injection of endotoxin. Journal of Dairy Science 85 765–773CrossRefGoogle ScholarPubMed
Persson-Waller, K, Colditz, IG, Lun, S & Ostensson, K 2003 Cytokines in mammary lymph and milk during endotoxin-induced bovine mastitis. Research in Veterinary Science 74 31–36CrossRefGoogle ScholarPubMed
Pfaffl, MW, Wittmann, SL, Meyer, HH & Bruckmaier, RM 2003 Gene expression of immunologically important factors in blood cells, milk cells and mammary tissue of cows. Journal of Dairy Science 86 538–545CrossRefGoogle ScholarPubMed
Rainard, P & Riollet, C 2006 Innate immunity of the bovine mammary gland. Veterinary Research 37 369–400 ReviewCrossRefGoogle ScholarPubMed
Sarikaya, H, Werner-Misof, C, Atzkern, M & Bruckmaier, RM 2005 Distribution of leucocyte populations, and milk composition, in milk fractions of healthy quarters in dairy cows. Journal of Dairy Research 72 486–492CrossRefGoogle ScholarPubMed
Sarikaya, H, Schlamberger, G, Meyer, HH & Bruckmaier, RM 2006 Leukocyte populations and mRNA expression of inflammatory factors in quarter milk fractions at different somatic cell score levels in dairy cows. Journal of Dairy Science 89 2479–2486CrossRefGoogle 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 26 111–126CrossRefGoogle ScholarPubMed
Schukken, YH, Grommers, FJ, Van de Geer, D, Erb, HN & Brand, A 1991 Risk factors for clinical mastitis in herds with a low bulk milk somatic cell count. 2. Risk factors for Escherichia coli and Staphylococcus aureus. Journal of Dairy Science 74 826–832CrossRefGoogle ScholarPubMed
Schukken, YH, Bennet, G, Green, L & Van Werven, T 2001 Can somatic cell counts get too low?National Mastitis Council Annual Meeting ProceedingsGoogle Scholar
Shook, GE 1989 Selection for disease resistance. Journal of Dairy Science 72 1349–1362CrossRefGoogle ScholarPubMed
Sordillo, LM & Streicher, KL 2002 Mammary gland immunity and mastitis susceptibility. Journal of Mammary Gland Biology and Neoplasia 7 135–146CrossRefGoogle ScholarPubMed
Suriyasathaporn, W, Schukken, YH, Nielen, M & Brand, A 2000 Low somatic cell count: a risk factor for subsequent clinical matitis in a dairy herd. Journal of Dairy Science 83 1248–1255CrossRefGoogle Scholar
Vangroenweghe, F, Rainard, P, Paape, M, Duchateau, L & Burvenich, C 2004 Increase of Escherichia coli inoculum doses induces faster innate immune response in primiparous cows. Journal of Dairy Science 87 4132–4144CrossRefGoogle ScholarPubMed
Van Merris, V, Meyer, E & Burvenich, C 2002 Functional maturation during bovine granulopoiesis. Journal of Dairy Science 85 2859–2868CrossRefGoogle ScholarPubMed
Werner-Misof, C, Pfaffl, MW & Bruckmaier, RM 2007 Dose-dependant immune response in milk cells and mammary tissue after intramammary administration of lipopolysaccharide in dairy cows. Veterinarni Medicina 52 231–244CrossRefGoogle Scholar