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Acute Phase Response in Dairy Cows with Experimentally Induced Escherichia coli Mastitis

Akut fas respons hos kor med experimenteilt inducerad Escherichia coli mastit

Abstract

Six Finnish Ayrshire cows were challenged intramammarily with 1500 CFU of Escherichia coli (E. coli) into single udder quarters, and the challenge was repeated into contralateral quarters 3 weeks later. All cows received flunixine meglumine once, and 3 of them were also treated with enrofloxacin. At the 2nd challenge, treatments were changed vice versa. The development of mastitis was followed by monitoring of systemic and local clinical signs, and with serial milk and serum samples. Intramarnmary challenge with E. coli produced clinical mastitis in all cows, the severity of the disease varying greatly between the animals. No significant changes between the 2 treatment regimens or sequent challenges were found for any of the clinical parameters. The response of each cow followed the same pattern after both challenges; three of the cows became mildly and the other 3 either moderately or severely affected. Two severely affected cows had to be euthanized because of severe mastitis.

Serum haptoglobin and amyloid-A concentrations peaked 2–3 days after bacterial challenge. Serum haptoglobin did not correlate with the severity of the disease. Serum amyloid-A rose gradually in the severely affected cows, and significant differences were found between severely versus moderately or mildly affected cows at day 4. Serum tumor necrosis factor alpha concentrations increased only in the severely affected cows. Serum Cortisol response was prolonged in the severely diseased animals, and was significantly lower after the second challenge. Serum nitrite/nitrate concentration increased in the severely affected cows. This indicated excess nitric oxide production during acute E. coli mastitis. Strongly decreased milk production, and high bacterial growth in the infected quarters were best predictors for the outcome from acute E coli mastitis.

Sammanfattning

För att åstadkomma experimentell mastit, inokulerades en juverfjärdedel hos sex finska ayrshire kor med 1500 CFU av E. coli. Tre veckor senare inokulerades kornas kontralaterala juverfjärdedel. Utvecklingen av mastit följdes upp genom att iakttaga allmänna och lokala kliniska symptom, och genom analys av serum och mjölkprover. Intramammär Inokulation med E. coli ledde till klinisk mastit hos alla kor, men svårighetsgraden varierade mycket mellan olika kor. Tre kor insjuknade milt, en måttligt och två allvarligt. De två allvarligt insjuknade korna måste avlivas p.g.a. grav mastit.

Serumkoncentrationerna av haptoglobin och amyloid-A nådde sina maximala nivåer 2–3 dagar efter Inokulationen. Serummängden av haptoglobin korrelerade inte med sjukdomens svårighetsgrad. Serumkoncentrationen av amyloid-A steg gradvis hos de allvarligt insjuknade korna, och ledde till signifikanta skillnader mellan grupperna på den fjärde dagen. Serumkoncentrationen av tumor nekros faktorn α steg endast hos de allvarligt sjuka korna. Kortisol-responsen i serum var förlängd hos de allvarligt sjuka korna och signifikant lägre efter den andra Inokulationen. Serumhalten av nitrit/nitrat steg hos kor med grav mastit; eventuellt ett tecken på ökad kväveoxidproduktion i samband med akut E. coli mastit. Å andra sidan är nitrit/nitrat halten i serum inte en pålitlig markör för ökad kväveoxid produktion. Kraftigt minskad mjölkproduktion och snabb bakterietillväxt i den infekterade juverfjärdedelen visade sig vara de viktigaste Symptomen som tyder på dålig prognos vid akut E. coli mastit.

References

  • Adler H, Adler B, Peveri P, Weiner ER, Wachter H, Peterhans E, Jungi TW: Differential regulation of inducible nitric oxide synthase production in bovine and caprine macrophages. J. Infect. Dis. 1996, 173, 971–978.

    Article  CAS  Google Scholar 

  • Alsemgeest SPM, Kalsbeek HC, Wensing Th, Koeman JP, van Ederen AM, Gruys, E: Concentration of serum amyloid-A (SAA) and haptoglobin (Hp) as parameters of inflammatory disease in cattle. Vet. Quart. 1994, 16, 21–23.

    Article  CAS  Google Scholar 

  • Baumann H, Gauldie J: The acute phase response. Immun.Today 1994, 15, 74–80.

    Article  CAS  Google Scholar 

  • Cai T, Weston PG, Lund LA, Brodie M, McKenna DJ, Wagner WC: Association between neutrophil functions and periparturient disorders in cows. Am. J. Vet. Res. 1994, 55, 934–943.

    CAS  PubMed  Google Scholar 

  • Carroll EJ, Schalm OW, Lasmanis J: Experimental coliform (Aerobacter aerogenes) mastitis: characteristics of the endotoxin and its role in pathogenesis. Am. J. Vet. Res. 1964, 25, 720–726.

    CAS  PubMed  Google Scholar 

  • Cebra CK, Garry FB, Dinsmore RP: Naturally occurring acute coliform mastitis in holstein cattle. J. Vet. Int. Med. 1996, 10, 252–257.

    Article  CAS  Google Scholar 

  • Coles EH: Kidney function. In: Coles EH (Author) Veterinary Clinical Pathology. W.B. Saunders Company. Philadelphia, PA, 1986, pp. 191–193.

  • Davis LE: Nonsteroidal antiinflammatory drugs, prostaglandins, and the kidney. J. Am. Vet. Med. Assoc. 1986, 188, 1065–1068.

    Google Scholar 

  • Dinarello CA: Interleukin-1 and the pathogenesis of the acute-phase response. N. Engl. J. Med. 1984, 311, 1413–1418.

    Article  CAS  Google Scholar 

  • Eberhart RJ, Natzke RP, Newbould FHS, Nonnecke B, Thompson PD: Coliform mastitis – a review. J. Dairy Sci. 1979, 62, 1–22.

    Article  Google Scholar 

  • Fabiny DL, Ertigshausen, G: Automated reaction rate method for determination of serum creatinine with Centrifichem. Clin. Chem. 1971, 17, 696–700.

    Article  CAS  Google Scholar 

  • Gutmann I, Bergmeyer HU: Determination of urea with glutamate dehydrogenase as indicator enzyme. In: Bergmeyer, HU (ed.): Methods of enzymatic analysis. 2nd ed. Academic Press, New York, NY, 1974, pp. 1794–1798.

  • Gruys E, Obwolo MJ, Toussaint MJM: Diagnostic significance of the major acute phase proteins in veterinary clinical chemistry. Vet. Bull. 1994, 64, 1009–1018.

    Google Scholar 

  • Hill AW: Factors influencing the outcome of Escherichia coli mastitis in the dairy cow. Res. Vet. Sci. 1981, 31, 107–112.

    Article  CAS  Google Scholar 

  • Hill AW, Shears AL, Hibbitt KG: The pathogenesis of experimental Escherichia coli mastitis in newly calved dairy cows. Res. Vet. Sci. 1979, 26, 97– 101.

  • Jackson JA, Shuster DE, Silvia WJ, Harmon RJ: Physiological responses to intramammary or intravenous treatment with endotoxin in lactating dairy cows. J. Dairy Sci. 1990, 73, 627–632.

    Article  CAS  Google Scholar 

  • Jones B, Kenward MG: Design and analysis of crossover trials. Chapman & Hall (eds), London, 1990, p. 340.

  • Katholm J, Andersen PH: Acute coliform mastitis in dairy cows: endotoxin and biochemical changes in plasma and colony-forming units in milk. Vet. Rec. 1992, 131, 513–514.

    Article  CAS  Google Scholar 

  • Kehrli ME, Nonnecke BJ, Roth JA: Alteration in bovine neutrophil function during the periparturient period. Am. J. Vet. Res. 1989, 50, 207–214.

    PubMed  Google Scholar 

  • Kenison DC, Elsasser T, Fayer R: Radioimmunoassay for bovine tumor necrosis factor: concentrations and circulating molecular forms in bovine plasma. J. Immunoassay 1990, 11, 177–198.

    Article  CAS  Google Scholar 

  • Korody P, Kulcsar M, Huszenicza G, Janosi Sz, Thuroczy J, Balogh L: Simultaneous determination of ACTH stimulated Cortisol release and TRH stimulated thyroid hormone release in dairy cows. Acta Vet. Hung. 1998. In print.

  • Kushner I: The phenomenom of the acute phase response. Ann. NY Acad. Sci. 1982, 389, 39–48.

    Article  CAS  Google Scholar 

  • Lohuis JACM, Schukken YH, Verheijden JHM, Brand A, Van Miert AJSPAM: Effect of severity of systemic signs during the acute phase of experimentally induced Escherichia coli mastitis on milk production losses. J. Dairy Sci. 1990, 73, 333–341.

    Article  CAS  Google Scholar 

  • Maury, CPJ, Teppo AM: Comparative study of serum amyloid-related protein SAA, C-reactive protein, and β2-microglobulin as markers of renal allograft rejection. Clin. Nephrol. 1984, 22, 284– 292.

  • Moshage H, Kok B, Huizenga JR, Jansen PL: Nitrite and nitrate determinations in plasma: a critical evaluation. Clin. Chem. 1995, 41, 892–896.

    Article  CAS  Google Scholar 

  • Myers MJ, Murtaugh MP: Biology of tumour necrosis factor. In: Myers MJ, Murtaugh MP (eds): Cytokines in animal health and disease. Marcel Dekker Inc, New York, NY, 1995, pp. 121–151.

  • Nakajima Y, Mikami O, Yoshioka M, Motoi Y: Elevated levels of tumor necrosis factor-α (TNF-α) and interleukin-6 (IL-6) activities in the sera and milk of cows with naturally occurring coliform mastitis. Res. Vet. Sci. 1997, 62, 297–298.

    Article  CAS  Google Scholar 

  • Olson NC, Hellyer PW, Dodam JR: Mediators and vascular effects in response to endotoxin. Br. Vet. J. 1995, 151, 489–522.

    Article  CAS  Google Scholar 

  • Paape MJ, Schultze WD, Desjardins C, Miller RH: Plasma corticosteroid, circulating leukocyte and milk somatic cell responses to Escherichia coli endotoxin-induced mastitis. Proc. Soc. Exp. Biol. Med. 1974, 5 14, 553–559.

  • Pannen BHJ, Robotham JL: The acute-phase response. New Horiz. 1995, 3, 183–197.

    CAS  PubMed  Google Scholar 

  • Payen D, Bernard C, Beloucif S: Nitric oxide in sepsis. Clin. Chest Med. 1996, 17, 333–350.

    Article  CAS  Google Scholar 

  • Peel JE, Voirol M-J, Kolly C, Gobet D, Martinod S: Induction of circulating tumor necrosis factor cannot be demonstrated during septicemic salmonellosis in calves. Inf.Immun. 1990, 58, 439–442.

    Article  CAS  Google Scholar 

  • Pighetti GM, Sordillo LM: Regulation of mammary gland macrophage tumour necrosis factor-α production with inteferon-γ. Res. Vet. Sci. 1994, 56, 252–255.

    Article  CAS  Google Scholar 

  • Pyörälä S: Clinical aspects of bovine mastitis and treatment during lactation. Thesis, College of Vet. Med., Helsinki, Finland, 1988.

  • Pyörälä S, Kaartinen L, Käck H: Efficacy of two therapy regimes for treatment of experimentally induced Escherichia coli mastitis in cows. J. Dairy Sci. 1994, 77, 453–461.

    Article  Google Scholar 

  • Pyörälä S, Pyörälä, E: Efficacy of parenteral administration of three antimicrobial agents in treatment of clinical mastitis in lactating cows: 487 cases (1989–1995). J. Am. Vet. Med. Assoc. 1998, 212, 407–412.

    PubMed  Google Scholar 

  • Rainard P, Paape MJ: Sensitization of the bovine mammary gland to Escherichia coli endotoxin. Vet. Res. 1997, 28, 231–238.

    CAS  PubMed  Google Scholar 

  • Rossevatn K, Andresen PK, Sletten K, Husebekk A, Husby G, Norstoga K, Johnson KH, Westermark GT, Westermark P: The complete amino acid sequence of bovine serum amyloid protein (SAA) and of subspecies of the tissue-deposited amyloid fibril protein A. Scand. J. Immun. 1992, 35, 217– 224.

  • Sahnen M, Hirvonen J, Pyörälä S, Sankari S, Sandholm M: Quantitative determination of bovine serum haptoglobin in experimentally induced Escherichia coli mastitis. Res. Vet. Sci. 1996, 60, 88–91.

    Article  Google Scholar 

  • Shuster DE, Lee EK, Kehrli Jr. ME: Bacterial growth, inflammatory cytokine production, and neutrophil recruitment during coliform mastitis in cows within ten days after calving, compared with cows at midlactation. Am. J. Vet. Res. 1996, 57, 1569–1575.

    CAS  PubMed  Google Scholar 

  • Sordillo LM, Peel JE: Effect of Interferon-γ on the production of tumor necrosis factor during acute Escherichia coli mastitis. J. Dairy Sci. 1992, 75, 2119–2125.

    Article  CAS  Google Scholar 

  • Sordillo LM, Peel JE, Babiuk LA: Potential role of cytokines in determining the outcome of acute coliform mastitis. Proc. Annu. Meet. Natl. Mastitis Council 1991, pp. 50–58.

  • Vandeputte-van Messom G, Burvenich C, Roets E, Massart-Leen AM, Heyneman R, Kremer WDJ, Brand A: Classification of newly calved cows into moderate and severe responders to experimentally induced Escherichia coli mastitis. J. Dairy Res. 1993, 60, 19–29.

    Article  Google Scholar 

  • Verdon CP, Burton BA, Prior RL: Sample pretreatment with nitrate reductase and glucose-6-phosphate dehydrogenase quantitatively reduces nitrate while avoiding interference by NADP+ when the griess reaction is used to assay for nitrite. Anal. Biochem. 1995, 224, 502–508.

    Article  CAS  Google Scholar 

  • Werling D, Sutter F, Arnold M, Kun G, Tooten PC, Gruys E, Kreuzer M, Langhans W: Characterisation of the acute phase response of heifers to a prolonged low dose infusion of lipopolysaccharide. Res. Vet. Sci. 1996, 61, 252–257.

    Article  CAS  Google Scholar 

  • Zeballos GA, Bernstein RD, Thompson CI, Forfia PR, Seyedi N, Shen W, Kamisnski PM, Wolin MS, Hinze TH: Pharmacodynamics of plasma nitrate/nitrite as an indication of nitric oxide formation in conscious dogs. Circulation 1995, 91, 2982–2988.

    Article  CAS  Google Scholar 

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Hirvonen, J., Eklund, K., Teppo, A.M. et al. Acute Phase Response in Dairy Cows with Experimentally Induced Escherichia coli Mastitis. Acta Vet Scand 40, 35–46 (1999). https://doi.org/10.1186/BF03547039

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