Journal of Animal Science and Technology

Korean Society of Animal Sciences and Technology (한국축산학회)
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Innate immunity and carbohydrate metabolism alterations precede occurrence of subclinical mastitis in transition dairy cows

  • Dervishi, Elda (Department of Agricultural Food, and Nutritional Science, University of Alberta) ;
  • Zhang, Guanshi (Department of Agricultural Food, and Nutritional Science, University of Alberta) ;
  • Hailemariam, Dagnachew (Department of Agricultural Food, and Nutritional Science, University of Alberta) ;
  • Dunn, Suzana M. (Department of Agricultural Food, and Nutritional Science, University of Alberta) ;
  • Ametaj, Burim N. (Department of Agricultural Food, and Nutritional Science, University of Alberta)
  • Received : 2015.10.06
  • Accepted : 2015.12.16
  • Published : 2015.12.31
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Abstract

Background: This study examined whether activation of innate immunity and alterations of carbohydrate and lipid metabolism precede development of subclinical mastitis (SCM). Methods: Blood samples were collected from the coccygeal vein from 100 Holstein dairy cows at -8, -4, disease diagnosis week, and +4 weeks postpartum. Six healthy cows (controls - CON) and six cows that showed clinical signs of SCM were selected for serum analyses. All serum samples were analyzed for acute phase proteins (APP) haptoglobin (Hp) and serum amyloid A (SAA); proinflammatory cytokines including interleukin 1 (IL-1), IL-6, and tumor necrosis factor (TNF) and serum lactate, BHBA, and NEFA concentration. Data of DMI, milk production, and milk composition were recorded and analyzed. Results: The results showed that cows with SCM had greater concentrations of SAA, TNF (P < 0.01), and lactate before expected day of parturition (P < 0.05) compared to CON cows. Cows with SCM showed greater concentrations of lactate starting at -8 weeks (P < 0.05) and TNF starting at -4 weeks prior to the expected day of parturition (P < 0.01). Interestingly, at -4 weeks, concentrations of IL-1 and Hp were lower in cows with SCM compared to healthy cows (P < 0.01) followed by an increase during the week of disease diagnosis (P < 0.05). Subclinical mastitis was associated with lower DMI, at -4 weeks before calving, milk production (P < 0.05) and increased somatic cell counts (SCC) (P < 0.01). Conclusions: Results of this study suggest that SCM is preceded by activated innate immunity and altered carbohydrate metabolism in transition dairy cows. Moreover the results support the idea that Hp, lactate, and SAA, at -8 weeks, and TNF and IL-1 at -4 weeks can be used as early indicators to screen cows during dry off for disease state.

Keywords

References

  1. Wilson DJ, Gonzales RN, Das HH. Bovine mastitis pathogen in New York and Pennsylvania: prevalence and effects on somatic cell count and milk production. J Dairy Sci. 1997;80:2592-8. https://doi.org/10.3168/jds.S0022-0302(97)76215-5
  2. Pitkala A, Haveri M, Pyorala S, Myllys V, Honkanen- Buzalski T. Bovine mastitis in Finland 2001- prevalence, distribution of bacteria, and antimicrobial resistance. J Dairy Sci. 2004;87:2433-41. https://doi.org/10.3168/jds.S0022-0302(04)73366-4
  3. Tylor JW, Cullor JS. Mammary gland health and disorders. In: Smith BP, editor. Large animal internal medicine. 3rd ed. London: Mosby; 1990. p. 1019-22.
  4. Sharma N, Singh NK, Bhadwal MS. Relationship of somatic cell count and mastitis: an overview. Asin-Aust J Anim Sci. 2011;24:429-38. https://doi.org/10.5713/ajas.2011.10233
  5. Hillerton JE. Redefining mastitis based on somatic cell count. IDF Bull. 1999;345:4-6.
  6. Kromker V, Graowski NT, Redetzky R, Hamann J. Detection of mastitis using selected quarter milk parameters. Canada: 2nd Intl Symp Bovine Mastitis and Milk Quality Vancouver; 2001. p. 486-7.
  7. Bailey T. Negative influence of subclinical mastitis. Virginia Cooperative Extension. Available at: http://www.ext.vt.edu/news/periodicals/dairy/1996-10/subclinmast.html.
  8. Rahman MM, Mazzilli M, Pennarossa G, Brevini TAL, Zecconi A, Gandolfi F. Chronic mastitis is associated with altered ovarian follicle development in dairy cattle. J Dairy Sci. 2012;95:1885-93. https://doi.org/10.3168/jds.2011-4815
  9. Roth Z, Dvir A, Kalo D, lavon Y, Krifucks O, Wolfenson D, et al. Naturally occurring mastitis disrupts developmental compentence of bovine oocytes. J Dairy Sci. 2013;96:1-7. https://doi.org/10.3168/jds.2012-5409
  10. Schrick FN, Hockett ME, Saxton AM, Lewis MJ, Dowlen HH, Oliver SP. Influence of subclinical mastitis during early lactation on reproductive parameters. J Dairy Sci. 2001;84:1047-412.
  11. Persson Y, Nyman AKJ, Gronlund- Andersson U. Etiology and antimicrobial susceptibility of udder pathogens from cases of subclinical mastitis in dairy cows in Sweden. Acta Vet Scandinavica. 2011;53:36. https://doi.org/10.1186/1751-0147-53-36
  12. Hamann J, Kromker V. Potential of specific milk composition variables for cow health management. Livestock Prod Sci. 1997;48:201-8. https://doi.org/10.1016/S0301-6226(97)00027-4
  13. Davis SR, Farr VC, Prosser CG, Nicholas GD, Turner SA, Lee J. Milk L-lactate concentration is increased during mastitis. J Dairy Sci. 2004;71:175-81.
  14. Lakshmi R, Thanislass J, Antony PX, Mukhopadhyay HK. Haptaglobin gene expression in spontaneous bovine subclinical mastitis caused by staphylococcus and coliforms microbes. Anim Sci Repor. 2014;8:9-17.
  15. Ohzato H, Yoshizaki K, Nishimoto N, Ogata A, Tagoh H, Monden M, et al. Interleukin -6 as a new indicator of inflammatory status: detection of serum levels of interleukin-6 and C-reactive protein after surgery. Surgery. 1992;111:201-9.
  16. Ametaj BN, Hosseini A, Odhiambo JF, Iqbal S, Deng Q, Lam TH, et al. Application of acute phase proteins for monitoring inflammatory states in cattle. In: Francisco Veas, editor. Acute phase proteins as early non-specific biomarkers of human and veterinary diseases. InTech, 2011. pp. 299-354.
  17. Nielsen BH, Jacobsen S, Andersen PH, Niewold TA, Heegaard PMH. Acute phase proteins concentration in serum and milk from cows with clinical mastitis with extramammary inflammatory conditions and clinically healthy cows. Vet Rec. 2004;154:361-5. https://doi.org/10.1136/vr.154.12.361
  18. O’Mahony MC, Healy AM, Harte D, Walshe KG, Torgerson PR, Doherty ML. Milk amyloid a: correlation with cellular indices of mammary inflammation in cows with normal and raised serum amyloid a. Res Vet Sci. 2006;80:155-61. https://doi.org/10.1016/j.rvsc.2005.05.005
  19. Molenaar AJ, Harris DP, Rajan GH, Pearson ML, Callagan MR, Sommer L, et al. The acute-phase protein serum amyloid A3 is expressed in the bovine mammary gland and plays role in host defense. Biomarkers. 2009;14:26-37. https://doi.org/10.1080/13547500902730714
  20. Akerstedt M, Forseback L, Larsen T, Svennersten-Sjaunja K. Natural variation in biomarkes indicating mastitis in healthy cows. J Dairy Res. 2011;78:88-96. https://doi.org/10.1017/S0022029910000786
  21. Eckersall PD, Young FJ, McComb C, Hogarth CJ, Safi S, Weber A, et al. Acute phase proteins in serum and milk from dairy cows with clinical mastitis. Vet Rec. 2001;148:35-41. https://doi.org/10.1136/vr.148.2.35
  22. Gronlund U, Hallen SC, Persson WK. Haptoglobin and erum amyloid A in milk from dairy cows with chronic sub-clinical mastisi. Vet Res. 2005;36:191-8. https://doi.org/10.1051/vetres:2004063
  23. Eckersall PD, Young FJ, Nolan AM, Knight CH, McComb C, Waterson MM, et al. Acute phase proteins in bovine milk in an experimentatl model of Staphylococcus aureus subclinical mastitis. J Dairy Sci. 2006;89:1488-501. https://doi.org/10.3168/jds.S0022-0302(06)72216-0
  24. Hiss S, Mueller U, Neu-Zahren A, Sauverwein H. Haptaglobin and lactate dehydrogenase measurements in milk for the identification of subclinically diseased udder quarters. Vet Med. 2007;52:245-52.
  25. Suojala L, Orro T, Jarvinen H, Saatsi J, Pyorala S. Acute phase response in two consecutive experimentally induce E. coli intramammary infections in dairy cows. Acta Vet Scandinavica. 2008;50:18. https://doi.org/10.1186/1751-0147-50-18
  26. Canadian Council on Animal Care. Guide to the care and Use of experimental animals, vol. 1. 2nd ed. Ottawa, ON, Canada: CCAC; 1993.
  27. Iqbal S, Zebeli Q, Mazzolari A, Dunn SM, Ametaj BN. Barley grain- based diet treated with lactic acid and heat modulated plasma metabolites and acute phase response in dairy cows. J Anim Sci. 2012;90:3143-52. https://doi.org/10.2527/jas.2011-3983
  28. Iqbal S, Zebeli Q, Mazzolari A, Dunn SM, Ametaj BN. Feeding rolled barley grain steeped in lactic acid modulated energy status and innate immunity in dairy cows. J Dairy Sci. 2010;93:5147-56. https://doi.org/10.3168/jds.2010-3118
  29. Ametaj BN, Koenign KM, Dunn SM, Yang WZ, Zebeli Q, Beauchemin KA. Backgrounding and finishing diets are associated with inflammatory responses in feedlot steers. J Anim Sci. 2009;87:1314-20. https://doi.org/10.2527/jas.2008-1196
  30. Xia J, Psychogios N, Young N, Wishart DS. MetaboAnalyst: a web server for metabolomics data analysis and interpretation. Nucleic Acids Res. 2009;37:652-60. https://doi.org/10.1093/nar/gkp356
  31. Xia J, Sinelnikov IV, Han B,Wishart DS. MetaboAnalyst 3.0--making metabolomics more meaningful. Nucleic Acids Res. 2015; doi:10.1093/nar/gkv380.
  32. Lehtolainen T, Ronved C, Pyorala S. Serum amyloid A and $TNF{\alpha}$ in serum and milk during experimental endoxin mastitis. Vet Res. 2004;35:651-9. https://doi.org/10.1051/vetres:2004043
  33. Blum J, Dosogne H, Hoeben D, Vangroenweghe F, Hammon H, Bruckmaier R, et al. Tumor necrosis alpha and nitrite/nitrate responses during acute mastitis induced by Eschericia coli infection and endotoxin in dairy cows. Domest Anim Endocrinol. 2000;19:223-35. https://doi.org/10.1016/S0739-7240(00)00079-5
  34. Hoeben D, Burvenich C, Trevis E, Bertoni G, Hamann J, Bruckmaier R, et al. Role of endotoxin and $TNF{\alpha}$ in the pathogenesis of experimentally induced coliform mastitis in periparturient cows. J Dairy Res. 2000;67:503-14. https://doi.org/10.1017/S0022029900004489
  35. Hisaeda K, Hagiwara K, Eguchi J, Yamanaka H, Kirisawa R, Iwai H. Interferon-gamma and tumor necrosis factor-alpha levels in sera and whey of cattle with naturally occurring coliform mastitis. J Vet Med Sci. 2001;63:1009-11. https://doi.org/10.1292/jvms.63.1009
  36. Nakajima Y, Mikami O, Yoshioka M, Motoi Y, Ito T, Ishikawa Y, et al. Elevated levels of tumor necrosis factor-alpha (TNF-alpha) and interleukin-6 (IL-6) activities in the sera and milk of cows with naturally occurring coliform mastitis. Res Vet Sci. 1997;62:297-8. https://doi.org/10.1016/S0034-5288(97)90209-5
  37. Politis I, McBride BW, Burton JH, Zhao X, Turner JD. Secretion of interleukin-1 by bovine milk macrophages. Am J Vet Res. 1991;52:858-62.
  38. Riollet C, Rainard P, Poutrel B. Cells and cytokines in inflammatory secretions of bovine mammary gland. Adv Exp Med Biol. 2000;480:247-58.
  39. Jiang L, Sorensen P, Rontved C, Vels L, Ingvartsen KL. Gene expression profiling of liver from dairy cows treated intra-mammary with lipopolysaccharide. BMC Genomics. 2008;9:443. https://doi.org/10.1186/1471-2164-9-443
  40. Minuti A, Zhou Z, Graugnard DE, Rodriguez-Zas SL, Palladino AR, Cardoso FC, et al. Acute mammary and liver transcriptome responses after an intramammary Escherichia coli lipopolysaccharide challenge in postpartal dairy cows. Physiol Rep. 2015;3, e12388. https://doi.org/10.14814/phy2.12388
  41. Sheldon IM, Noakes DE, Rycroft AN, Dobson H. Acute phase protein responses to uterine bacterial contamination in cattle after calving. Vet Rec. 2001;148:172-5. https://doi.org/10.1136/vr.148.6.172
  42. Quaye IK. Haptoglobin, inflammation and disease. Trans R Soc Trop Med Hyg. 2008;102:735-42. https://doi.org/10.1016/j.trstmh.2008.04.010
  43. Humblet MF, Guyot H, Boudry B, Mbayahi F, Hanzen C, Rollin F, et al. Relationship between haptoglobin, serum amyloid A, and clinical status in a survey of dairy herds during a 6- month period. Vet Clin Pathol. 2006;35:188-93. https://doi.org/10.1111/j.1939-165X.2006.tb00112.x
  44. Rezamand P, Hoagland TA, Moyes KM, Silbart LK, Andrew SM. Energy status, lipid- soluble vitamins and acute phase proteins in periparturient Holstein and Jersey dairy cows with or without subclinical mastitis. J Dairy Sci. 2007;90:5097-107. https://doi.org/10.3168/jds.2007-0035
  45. Wassell J. Haptoglobin: function and polymorphism. Clin Lab. 2000;46:547-52.
  46. Gronlund U, Hulten C, Eckersall PD, Hogarth C, Waller KP. Haptaglobin and serum amyloid A in milk and serum during acute and chronic experimentally induced Staphylocossus aureus mastitis. J Dairy Res. 2003;70:379-86. https://doi.org/10.1017/S0022029903006484
  47. Gerardi G, Bernardini D, Azzurra Elia C, Ferrari V, Iob L, Segato S. Use of serum amyloid A and milk amyloid A in the diagnosis of subclinical mastitis in dairy cows. J of Dairy Res. 2009;76:411-7. https://doi.org/10.1017/S0022029909990057
  48. Ametaj BN, Bradford BJ, Bobe G, Nafikov RA, Lu Y, Young JW, et al. Strong relationships between mediators of acute phase response and fatty liver in dairy cows. Can J Anim Sci. 2005;85:165-75. https://doi.org/10.4141/A04-043
  49. Nguyen HB, Rivers EP, Knoblich BP, Jacobsen G, Muzzin A, Ressler JA, et al. Early lactate clearance is associated with improved outcome in severe sepsis and septic shock. Crit Care Med. 2004;32:1637-42. https://doi.org/10.1097/01.CCM.0000132904.35713.A7
  50. Arnold RC, Shapiro NI, Alan EJ, Schorr C, Pope J, Casner E, et al. Multicenter study of early lactate clearance as a determinant of survival in patients with presumed sepsis. Shock. 2009;32:35-9. https://doi.org/10.1097/SHK.0b013e3181971d47
  51. Meszaros K, Lang CH, Bagby GJ, Spitzer JJ. Contribution of different organs to increased glucose consumption after endotoxin administration. J of Biological Chem. 1987;262:10965-70.
  52. Lang CH, Bagby GJ, Spitzer JJ. Glucose kinetics and body temperature after lethal and nonlethal doses of endotoxin. Am J Physiol. 1985;248:471-8.
  53. Lopez-Villegas D, Lenkinski RE, Wehrli SL, Ho WZ, Douglas SD. Lactate production by human monocytes/macrophages determined by proton mr spectroscopy. MRM. 1995;34:2-38.
  54. Taylor DJ, Whitehead RJ, Evanson JM, Westmacott D, Feldman M, Bertfield H. Effect of recombinant cytokines on glycolysis and fructose 2, 6-bisphosphate in rheumatoid synovial cells in vitro. Biochem J. 1998;250:111-5.
  55. Husain Z, Huang Y, Seth P, Sukhatme VP. Tumor-derived lactate modifies antitumor immune response: effect on myeloid-derived suppressor cells and NK cells. J Immunol. 2013;191:1486-95. https://doi.org/10.4049/jimmunol.1202702
  56. Fischer B, Muller B, Fischer KG, Baur N, Kreutz W. Acidic pH inhibits non-MHC-restricted killer cell functions. Clin Immunol. 2000;96:252-63. https://doi.org/10.1006/clim.2000.4904
  57. Gottfried E, Kunz-Schughart LA, Ebner S, Mueller-Klieser W, Hoves S, Andreesen R, et al. Kreutz M Tumor-derived lactic acid modulates dendritic cell activation and antigen expression. Blood. 2006;107:2013-21. https://doi.org/10.1182/blood-2005-05-1795
  58. Shime H, Yabu M, Akazawa T, Kodama K, Matsumoto M, Seya T, et al. Tumor-secreted lactic acid promotes IL-23/IL-17 proinflammatory pathway. J Immunol. 2008;180:7175-83. https://doi.org/10.4049/jimmunol.180.11.7175
  59. Ingvartsen KL, Andersen JB. Integration of metabolism and intake regulation: a review focusing on periparturient animals. J Dairy Sci. 2000;83:1573-97. https://doi.org/10.3168/jds.S0022-0302(00)75029-6
  60. Gonzalez LA, Tolkamp BJ, Coffey MP, Ferret A, Kyriazakis I. Changes in feeding behavior as possible indicator for the automatic monitoring of health disorders in dairy cows. J of Dairy Sci. 2008;91:1017-28. https://doi.org/10.3168/jds.2007-0530
  61. Huzzey JM, Viera DM, Weary DM, Von Keyserlingk MAG. Prepartum behavior and dry matter intake identify dairy cows at risk with metritis. J of Dairy Sci. 2007;95:3220-33.
  62. Goff JP. Major advances in our understanding of nutritional influences on bovine health. J of Dairy Sci. 2006;89:1292-301. https://doi.org/10.3168/jds.S0022-0302(06)72197-X
  63. Lohuis JACM, Verheijden JHM, Burvenich C, van Miert ASJPAM. Pathophysiological effects of endotoxins in ruminants. Vet Q. 1988;10:109-25. https://doi.org/10.1080/01652176.1988.9694157
  64. Steiger M, Senn M, Altreuther G, Werling D, Sutter F, Kreuzer M, et al. Effect of a prolonged low-dose lipopolysaccharide infusion on feed intake and metabolism in heifers. J Anim Sci. 1999;77:2523-32. https://doi.org/10.2527/1999.7792523x
  65. Allen MS, Bradford BJ. The cow as a model to study food intake regulation. Annu Rev Nutr. 2005;25:523-47. https://doi.org/10.1146/annurev.nutr.25.050304.092704
  66. Mungube EO, Tenhagen BA, Regassa F, Kyule MN, Shiferaw Y, Kasa T, et al. Reduced milk production in udder quarters with subclinical mastitis and associated economic losses in crossbred dairy cows in Ethiopia. Tropical Anim Health Prod. 2005;37:503-12. https://doi.org/10.1007/s11250-005-7049-y
  67. Theas MS, De Laurentiis A, Lasaga M, Pisera D, Duvilanski BH, Seilicovich A. Effect of lipopolysaccharide on tumor necrosis factor and prolactin release from rat anterior pituitary cells. Endocrine. 1998;8:241-5.
  68. Kushibiki S, Hodate K, Shingu H, Obara Y, Touno E, Shinoda M. Metabolic and lactational responses during recombinant bovine tumor necrosis factor-${\alpha}$ treatment in lactating cows. J Dairy Sci. 2003;86:819-27. https://doi.org/10.3168/jds.S0022-0302(03)73664-9
  69. Zebeli Q, Dijkstra J, Tafaj M, Steingass H, Ametaj BN, Drochner W. Modeling the adequacy of dietary fiber in dairy cows based on the responses of ruminal pH and milk fat production to composition of the diet. J Dairy Sci. 2008;91:2046-66. https://doi.org/10.3168/jds.2007-0572
  70. Zebeli Q, Aschenbach JR, Tafaj M, Boguhn J, Ametaj BN, Drochner W. Role of physically effective fiber and estimation of dietary fiber adequacy in high-producing dairy cattle. J Dairy Sci. 2012;95:1041-56. https://doi.org/10.3168/jds.2011-4421
  71. Duffield TF, Kelton DF, Leslie KE, Lissemore KD, Lumsden JH. Use of test day milk fat and milk protein to detect subclinical ketosis in dairy cattle in Ontario. Can Vet J. 1997;38:713-8.
  72. Zebeli Q, Ametaj BN. Relationships between rumen lipopolysaccharide and mediators of inflammatory response with milk fat production and efficiency in dairy cows. J Dairy Sci. 2009;92:3800-9. https://doi.org/10.3168/jds.2009-2178
  73. Sargeant JM, Leslie KE, Shirley JE, Pulkrabek BJ, Lim GH. Sensitivity and specificity of somatic cell account and California mastitis test for identifying intramammary infection in early lactation. J Dairy Sci. 2001;84:2018-24. https://doi.org/10.3168/jds.S0022-0302(01)74645-0
  74. Obled C, Papet I, Breuille D. Metabolic bases of amino acid requirements in acute disease. Curr Opin Clin Nutr Metab Care. 2002;5:189-97. https://doi.org/10.1097/00075197-200203000-00012

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