Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-25T04:24:02.726Z Has data issue: false hasContentIssue false
  • English
  • Français

Enzyme activity and acute phase proteins in milk utilized as indicators of acute clinical E. coli LPS-induced mastitis

Published online by Cambridge University Press:  17 May 2010

T. Larsen ,
C. M. Røntved ,
K. L. Ingvartsen ,
L. Vels  and
M. Bjerring
T. Larsen*
Affiliation:
Faculty of Agricultural Sciences, Department of Animal Health and Bioscience, Aarhus University, Blichers Allé 20, PO Box 50, DK-8830 Tjele, Denmark
C. M. Røntved
Affiliation:
Faculty of Agricultural Sciences, Department of Animal Health and Bioscience, Aarhus University, Blichers Allé 20, PO Box 50, DK-8830 Tjele, Denmark
K. L. Ingvartsen
Affiliation:
Faculty of Agricultural Sciences, Department of Animal Health and Bioscience, Aarhus University, Blichers Allé 20, PO Box 50, DK-8830 Tjele, Denmark
L. Vels
Affiliation:
Faculty of Agricultural Sciences, Department of Animal Health and Bioscience, Aarhus University, Blichers Allé 20, PO Box 50, DK-8830 Tjele, Denmark
M. Bjerring
Affiliation:
Faculty of Agricultural Sciences, Department of Animal Health and Bioscience, Aarhus University, Blichers Allé 20, PO Box 50, DK-8830 Tjele, Denmark
*
†E-mail: [email protected]
Get access

Abstract

The importance of non-visual and on-line monitoring of udder health increases as the contact between humans and animals decreases, for example, in robotic milking systems. Several indicator systems have been introduced commercially, and a number of techniques are currently in use. This study describes the kinetics of seven indigenous milk parameters for monitoring udder inflammation in an Escherichia coli lipopolysaccharide (LPS, endotoxin)-induced mastitis model. Proportional milk from LPS-infused quarters was compared with milk from parallel quarters, which were placebo-treated with sterile 0.9% NaCl solution. Somatic cell counts (SCCs), the acute phase proteins (APP), that is, milk amyloid A (MAA) and haptoglobin (Hp), and the enzymes N-acetyl-β-D-glucosaminidase (NAGase), lactate dehydrogenase (LDH), alkaline phosphatase (AP) and acid phosphatase (AcP) were measured at fixed intervals during the period from −2 to +5 days after LPS and NaCl infusions. All parameters responded significantly faster and were more pronounced to the LPS infusions compared with the NaCl infusions. All parameters were elevated in the proportional milk collected at the first milking 7 h after infusion and developed a monophasic response, except Hp and MAA that developed biphasic response. SCC, LDH, NAGase and Hp peaked at 21 h followed by AP, AcP and MAA peaking at 31 h with the highest fold changes seen for MAA (23 780×), LDH (126×), NAGase (50×) and Hp (16×). In the recovery phase, AP, AcP and Hp reached base levels first, at 117 h, whereas LDH, NAGase and MAA remained elevated following the pattern of SCC. Minor increases of the milk parameters were also seen in the neighboring (healthy) quarters. Distinction between inflamed and healthy quarters was possible for all the parameters, but only for a limited time frame for AP and AcP. Hence, when tested in an LPS mastitis model, the enzymes LDH, NAGase and AP in several aspects performed equally with SCC and APP as inflammatory milk indicators of mastitis. Furthermore, these enzymes appear potent in the assessment of a valuable time sequence of inflammation, a necessary ingredient in modeling of programs in in-line surveillance systems.

Keywords

mastitisNAGaseLDHAPacute phase proteins
Type
Full Paper
Information
animal , Volume 4 , Issue 10 , October 2010 , pp. 1672 - 1679
Copyright
Copyright © The Animal Consortium 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

Aida, Y, Pabst, MJ 1991. Neutrophil responses to lipopolysaccharides. Effect of adherence on triggering and priming of the respiratory burst. Journal of Immunology 146, 1271–1276.CrossRefGoogle ScholarPubMed
Åkerstedt, M, Björk, L, Waller, KP, Stjernesjö, Å 2006. Biosensor assay for determination of haptoglobin in bovine milk. Journal of Dairy Research 73, 299–305.CrossRefGoogle ScholarPubMed
Anderson, M, Brooker, BE, Andrews, AT, Alichanidis, E 1974. Membrane material isolated from milk of mastitic and normal cows. Journal of Dairy Science 57, 1448–1458.CrossRefGoogle ScholarPubMed
Anderson, M, Brooker, BE, Andrews, AT, Alichanidis, E 1975. Membrane material in bovine skim-milk from udder quarters infused with endotoxin and pathogenic organisms. Journal of Dairy Research 42, 401–417.CrossRefGoogle Scholar
Andrews, AT 1991. Indigenous enzymes in milk, phosphatases. In Food enzymology, vol. 1. (ed. PF Fox), pp. 90–99. Elsevier Applied Science, London, UK.Google Scholar
Andrews, AT, Alichanidis, E 1975. The acid phosphatases of bovine leucocytes, plasma and the milk of healthy and mastitic cows. Journal of Dairy Research 42, 391–400.CrossRefGoogle Scholar
Banga, HS, Gupta, HS, Ahuja, SP, Srivastava, AK, Roy, KS 1989. Biochemical alterations in the blood, milk and tissues of sheep mammary gland after experimental mycoplasmal mastitis. Acta Veterinary Brno 58, 97–111.CrossRefGoogle Scholar
Bogin, E, Ziv, G 1973. Enzymes and minerals in normal and mastitic milk. Cornell Veterinary 63, 666–676.Google ScholarPubMed
Bogin, E, Ziv, G, Avidar, J 1976. Enzyme activities in normal and inflamed bovine udder tissues. Zentralblatt Veterinary Medicine A 23, 460–466.CrossRefGoogle ScholarPubMed
Burvenich, C, Bannerman, DD, Lippolis, JD, Peelman, BJ, Nonnecke, BJ, Kehrli, ME, 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 (E. suppl.), E39–E54.CrossRefGoogle ScholarPubMed
Chagunda, MGG, Larsen, T, Bjerring, M, Ingvartsen, KL 2006a. L-lactate dehydrogenase and N-acetyl-β-D-glucosaminidase activities in bovine milk as indicators of clinical mastitis. Journal of Dairy Research 73, 431–440.CrossRefGoogle Scholar
Chagunda, MGG, Friggens, NC, Rasmussen, MD, Larsen, T 2006b. A model for detection of individual cow mastitis based on an indicator measured in milk. Journal of Dairy Science 89, 2980–2998.CrossRefGoogle Scholar
Cooray, R, Waller, KP, Venge, P 2007. Haptoglobin comprises about 10% of granule protein extracted from bovine granulocytes isolated from healthy cattle. Veterinary Immunology and Immunopathology 119, 310–315.CrossRefGoogle ScholarPubMed
Eckersall, PD, Young, FJ, McComb, C, Hogarth, CJ, Safi, S, Weber, A, McDonald, T, Nolan, AM, Fitzpatrick, JL 2001. Acute phase proteins in serum and milk from dairy cows with clinical mastitis. Veterinary Records 148, 35–41.CrossRefGoogle ScholarPubMed
Fernley, HN, Walker, PG 1969. Studies on alkaline phosphatase (transient-state and steady state kinetics of E. coli alkaline phosphatase). Biochemical Journal 111, 187–194.CrossRefGoogle Scholar
Friggens, NC, Chagunda, MGG, Bjerring, M, Ridder, C, Højsgaard, S, Larsen, T 2007. Estimating degree of mastitis from time-series measurements in milk: a test of a model based on lactate dehydrogenase measurements. Journal of Dairy Science 90, 5415–5427.CrossRefGoogle Scholar
Grönlund, U, Sandgren, CH, Waller, KP 2005. Haptoglobin and serum amyloid A in milk from dairy cows with chronic sub-clinical mastitis. Veterinary Research 36, 191–198.CrossRefGoogle ScholarPubMed
Grönlund, U, Hultén, C, Eckersall, PD, Hogarth, C, Waller, KP 2003. Haptoglobin and serum amyloid A in milk and serum during acute and chronic experimentally induced Staphyllococcus aureus mastitis. Journal of Dairy Research 70, 379–386.CrossRefGoogle Scholar
Heyneman, R, Burvenich, C 1992. Kinetics and characteristics of bovine neutrophil alkaline phosphatase during acute Eschericia coli mastitis. Journal of Dairy Science 75, 1826–1834.CrossRefGoogle Scholar
Jacobsen, S, Niewold, TA, Kornalijnslijper, E, Toussaint, MJM, Gruys, E 2005. Kinetics of local and systemic isoforms of serum amyloid A in bovine mastitic milk. Veterinary Immunology and Immunopathology 104, 21–31.CrossRefGoogle ScholarPubMed
Kato, KK, Mori, K, Katoh, N 1989. Contribution of leucocytes to the origin of lactate dehydrogenase isoenzymes in milk of bovine mastitis. Japanese Journal of Veterinary Science 51, 530–539.Google Scholar
Kitchen, BJ 1976. Enzymic methods for estimation of somatic cell count in bovine milk. Journal of Dairy Research 43, 251–258.CrossRefGoogle ScholarPubMed
Kitchen, BJ 1981. Review of the progress of dairy science: bovine mastitis: milk compositional changes and related diagnostic tests. Journal of Dairy Research 48, 167–188.CrossRefGoogle ScholarPubMed
Kitchen, BJ 1985. Indigenous milk enzymes. In Developments in dairy chemistry, vol. 3. (ed. PF Fox), pp. 239–279. Elsevier Applied Science, London, UK.CrossRefGoogle Scholar
Kitchen, BJ, Middleton, G, Salmon, M 1978. Bovine milk N-acetyl-β-D-glucosaminidase and its significance in the detection of abnormal udder secretions. Journal of Dairy Research 45, 15–20.CrossRefGoogle ScholarPubMed
Kitchen, BJ, Durward, IG, Middleton, G, Andrews, RJ, Salmon, MC 1980. Mastitis diagnostic tests to estimate mammary gland epithelial cell damage. Journal of Dairy Science 63, 978–983.CrossRefGoogle ScholarPubMed
Kitchen, BJ, Kwee, WS, Middleton, G, Andrews, RJ 1984. Relationship between the level of N-acetyl-β-D-glucosaminidase (NAGase) in bovine milk and the presence of mastitis pathogens. Journal of Dairy Research 51, 11–16.CrossRefGoogle ScholarPubMed
Korhonen, H, Kaartinen, L 1995. Changes in the composition of milk induced by mastitis. In The bovine udder and mastitis (ed. M Sandholm, T Honkanen-Buzolski, L Kaartinen and S Pyörölä), pp. 76–82. University of Helsinki, Finland.Google Scholar
Larsen, T 2005. Determination of lactate dehydrogenase (LDH) activity in milk by a fluorometric assay. Journal of Dairy Research 72, 209–216.CrossRefGoogle ScholarPubMed
Larson, MA, Weber, A, Weber, AT, McDonald, TL 2005. Differential expression and secretion of bovine serum amyloid A3 (SAA3) by mammary epithelial cells stimulated with prolactin or lipopolysaccharide. Veterinary Immunology and Immunopathology 107, 255–264.CrossRefGoogle ScholarPubMed
Lehtolainen, T, Røntved, C, Pyörälä, S 2004. Serum amyloid A and TNFα in serum and milk during experimental endotoxin mastitis. Veterinary Research 35, 651–659.CrossRefGoogle ScholarPubMed
Nielsen, NI, Larsen, T, Bjerring, M, Ingvartsen, KL 2005. Quarter health, milking interval, and sampling time during milking affect the concentration of milk constituents. Journal of Dairy Science 88, 3186–3200.CrossRefGoogle ScholarPubMed
Pyörälä, S 2003. Indicators of inflammation in the diagnosis of mastitis. Veterinary Research 34, 565–578.CrossRefGoogle Scholar
Pyörälä, S, Pyörälä, E 1997. Accuracy of methods using somatic cell count and N-acetyl-β-D-glucosaminidase activity in milk to assess the bacteriological cure of bovine clinical mastitis. Journal of Dairy Science 80, 2820–2825.CrossRefGoogle ScholarPubMed
Rinaldi, M, Li, RW, Bannerman, DD, Daniels, KM, Evock-Clover, C, Silva, MVB, Paape, MJ, Van Ryssen, B, Burvenich, C, Capuco, AV 2009. A sentinel function for teat tissues in dairy cows: dominant innate immune response elements define early response to E. coli mastitis. Functional & Integrative Genomics 10, 21–38.CrossRefGoogle ScholarPubMed
Sandholm, M, Pyörälä, S 1995. Coliform mastitis. Endotoxin mastitis – endotoxin shock. In The bovine udder and mastitis (ed. M Sandholm, T Honkanen-Buzolski, L Kaartinen and S Pyörölä), pp. 149–160. University of Helsinki, Finland.Google Scholar
SAS Institute Inc 2004. SAS OnlineDoc® 9.1.3. SAS Institute Inc, Cary, NC.Google Scholar
Schaar, J, Funke, H 1986. Effect of subclinical mastitis on milk plasminogen and plasmin compared with that on sodium, antitrypsin and N-acetyl-β-D-glucosaminidase. Journal of Dairy Research 53, 515–528.CrossRefGoogle ScholarPubMed
Schüttel, M 1999. Vergleich von N-acetyl-β-D-glycosamidase-Aktivitäten (NAGase) in Milch, Blut und Harn beim laktierenden Rind. Dissertation, Dr. Med. Vet. Tierärtslicher Hochschule Hannover, Germany.Google Scholar
Symons, DBA, Wright, LJ 1974. Changes in bovine mammary gland permeability after intramammary endotoxin infusion. Journal of Comparative Pathology 84, 9–17.CrossRefGoogle Scholar
Thielen, MA, Mielenz, M, Hiss, S, Sauerwein, H 2005. Quantitative detection of haptoglobin mRNA in bovine and human blood leucocytes and bovine milk somatic cells. Veterinary Medicine- Czech 50, 515–520.CrossRefGoogle Scholar
Thielen, MA, Mielenz, M, Hiss, S, Zerbe, H, Petzi, W, Schubert, HJ, Seyfert, HM, Sauerwein, H 2007. Cellular localization of haptoglobin mRNA in the experimentally infected bovine mammary gland. Journal of Dairy Science 90, 1215–1219.CrossRefGoogle ScholarPubMed
Vels, L, Røntved, CM, Bjerring, M, Ingvartsen, KL 2009. Cytokine and acute phase protein gene expression in liver biopsies from dairy cows with a lipopolysaccharide–induced mastitis. Journal of Dairy Science 92, 922–934.CrossRefGoogle ScholarPubMed
Winter, P, Fuchs, K, Walshe, K, Colditz, IG 2003. Serum amyloid A in the serum and milk of ewes with mastitis induced experimentally with Staphyllococcus epidermidis. Veterinary Records 152, 558–562.CrossRefGoogle Scholar