Skip to main content

Advertisement

SpringerLink
Log in

The relationship of metabolic parameters and milk acute-phase protein with the outcome of treatment of Staphylococcus aureus subclinical mastitis in dairy cows

  • Regular Articles
  • Published:
Tropical Animal Health and Production Aims and scope Submit manuscript

Abstract

The main aim of the current investigation was to evaluate the relationships between metabolic parameters, acute-phase proteins, and the outcome of treatment of Staphylococcus aureus subclinical mastitis in dairy cows. Serum metabolic parameters and milk haptoglobin were measured in two groups: S. aureus subclinical mastitis cows with successful treatment (n = 26) and S. aureus subclinical mastitis cows with unsuccessful treatment (n = 26). Significantly higher serum aspartate aminotransferase (AST), alkaline phosphatase (ALP), and LDL cholesterol concentrations were seen in subclinical mastitis cows with unsuccessful treatment compared to subclinical mastitis cows with successful treatment (p < 0.05). On the other hand, subclinical mastitis cows with successful treatment demonstrated higher serum iron and copper concentrations than the other group (p < 0.05). Comparison of measured variables before treatment revealed that cows suffering from subclinical mastitis with higher values of serum LDL cholesterol, ALP, and AST did not respond to antibiotic treatment and subclinical mastitis was persisted in the second examination, whereas subclinical mastitis cows with successful treatment demonstrated higher serum copper and iron concentrations (p < 0.05). The findings of the current investigation suggested that there was a relationship between the treatment outcome of S. aureus subclinical mastitis and trace element concentrations and liver health status. Furthermore, the present study provided cutoff values for serum LDL cholesterol, AST, ALP, iron, and copper, which would help predict the treatment outcome in cows with S. aureus subclinical mastitis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Availability of data and materials

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Abdelmegid, S., Kelton, D., Caswell, J., Kirby, G., 2020. Proteomic 2d-dige analysis of milk whey from dairy cows with staphylococcus aureus mastitis reveals overexpression of host defense proteins, Microorganisms. 8, 1-14.

    Article  CAS  Google Scholar 

  • Adkins, P.R.F., Middleton, J.R., 2018. Methods for diagnosing mastitis, Veterinary Clinics of North America: Food Animal Practice, 34, 479–491.

    Google Scholar 

  • Akerstedt, M., Waller, K.P., Sternesjo, A., 2007. Haptoglobin and serum amyloid A in relation to the somatic cell count in quarter, cow composite and bulk tank milk samples, Journal of Dairy Research, 74, 198–203.

    Article  CAS  PubMed  Google Scholar 

  • Bareille, N., Seegers, H., Kiebre-Toe, M.B., Beaudeau, F., Fourichon, C., 2000. Risk factors for elevated milk somatic cell counts during early lactation in dairy heifers, Proceedings of the 10th Int. Congress of Animal Hygienic, Maastricht, the Netherlands, 509–514.

  • Barkema, H.W., Schukken, Y.H., Zadoks, R.N., 2006. Invited review: the role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis, Journal of Dairy Science, 89, 1877–1895.

    Article  CAS  PubMed  Google Scholar 

  • Bathla, S., Sindhu, A., Kumar, S., Pattnaik, S., Rawat, P., Chopra, A., Mohanty, A.K., 2020. Quantitative proteomics revealed the putative biomarker for detection of early-stage intra-mammary gland infection in cow, Journal of Proteins and Proteomics, 11, 173–181.

    Article  CAS  Google Scholar 

  • Baydar, E., Dabak, M., 2014. Serum iron as an indicator of acute inflammation in cattle. Journal of Dairy Science, 97, 222–228

    Article  CAS  PubMed  Google Scholar 

  • Beisel, W.R., 1991. Nutrition and infection. In: Linder, M.C. (Ed.), Nutritional Biochemistry and Metabolism with Clinical Application. , Second ed. Elsevier, New York, pp. 507–542

    Google Scholar 

  • Bianchi, R.M., Schwertz, C.I., Cecco, B.S., Panziera, W., Lorenzo, C. de, Heck, L.C., Snel, G.G.M., Lopes, B.C., Silva, F.S.da, Pavarini, S.P., Driemeier, D., 2019. Pathological and microbiological characterization of mastitis in dairy cows. Tropical Animal Health and Production, 51, 2057-2066.

    Article  PubMed  Google Scholar 

  • Bihon, A., Syoum, A., Assefa, A., 2019. Assessment of risk factors and isolation of Staphylococcus aureus and Escherichia coli from bovine subclinical mastitic milk in and around Gondar, northwest Ethiopia. Tropical Animal Health and Production, 51, 939-948.

    Article  PubMed  Google Scholar 

  • Borges, A.S., Divers, T.J., Stokol, T., Mohammed, O.H., 2007. Serum iron and plasma fibrinogen concentrations as indicators of systemic inflammatory diseases in horses. Journal of Veterinary Internal Medicine, 21, 489–494.

    Article  PubMed  Google Scholar 

  • Burvenich, C., Bannerman, D.D., Lippolis, J.D., Peelman, L., Nonnecke, B.J. Kehrli, W.E. Paape, M.J., 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, 39–54.

    Article  Google Scholar 

  • Cherayil, B.J., 2011. The role of iron in the immune response to bacterial infection. Immunology Research, 50, 1–9.

    Article  CAS  Google Scholar 

  • Corrigall, W., Dalgarno,A.C., Ewen, L.A.,Williums,R.B., 1976.Modulation of plasma copper and zinc concentrations by disease status in ruminants. Veterinary Record 99, 396–397.

    Article  CAS  PubMed  Google Scholar 

  • Doherr, M.G., Roesch, M., Schaeren, W., Schallibaum, M., Blum, J.W., 2007. Risk factors associated with subclinical mastitis in dairy cows on Swiss organic and conventional production system farms, Veterinarni Medicina, 52, 487–495.

    Article  Google Scholar 

  • Duffield, T.F.,&nbsp;Lissemore, K.D., McBride, B.W., Leslie, K.E., 2009. Impact of hyperketonemia in early lactation dairy cows on health and production, Journal of Dairy Science, 92, 571-580.

    Article  CAS  PubMed  Google Scholar 

  • Eckersall, P.D., Bell, R., 2010. Acute phase proteins: Biomarkers of infection and inflammation in veterinary medicine, Veterinary Journal, 185, 23–27.

    Article  CAS  PubMed  Google Scholar 

  • Eckersall, P.D., Young. F.J., Nolan, A.M., Knight, C.H., McComb, C., Waterston, M.M., Hogarth, C.J., Scott, E.M., Fitzpatrick, J.L., 2006. Acute phase proteins in bovine milk in an experimental model of Staphylococcus aureus subclinical mastitis. Journal of Dairy Science, 89, 1488–1501.

    Article  CAS  PubMed  Google Scholar 

  • Gerardi, G., Bernardini, D., Elia, C.A., Ferrari, V., Iob, L., Segato, S., 2009. Use of serum amyloid A and milk amyloid A in the diagnosis of subclinical mastitis in dairy cows, Journal of Dairy Research, 76, 411–417.

    Article  CAS  PubMed  Google Scholar 

  • Gronlund, U., Hulten, C., Eckersall, P.D., 2003. Haptoglobin and serum amyloid A in milk and serum during acute and chronic experimentally induced Staphylococcus aureus mastitis, Journal of Dairy Research, 70, 379–386.

    Article  CAS  PubMed  Google Scholar 

  • Halliwell, B., Gutteridge, J.M.C., 1999. Free Radicals in Biology and Medicine, third ed., New York: Oxford University Press.

    Google Scholar 

  • Harmon, R.J., 1998. Trace minerals and dairy cattle: importance for udder health. In: Lyons TP, Jacques KA eds. Biotechnology in the feed industry, Proceedings of Alltech’s 14th Annual Symposium, Nottingham University Press, Nottingham, UK, 485–495.

  • Heidarpour, M., Mohri, M., Fallah-Rad, A.H., Dehghan Shareze, F., Mohammadi, M., 2012. Acute phase protein concentration and metabolic status affect the outcome of treatment in cows with clinical and subclinical endometritis, Veterinary Record, 171, 219.

    Article  CAS  PubMed  Google Scholar 

  • Hektoen, L., Odegaard, S.A., Loken, T., Larsen, S., 2004. Evaluation of stratification factors and score-scales in clinical trials of treatment of clinical mastitis in dairy cows, Journal of Veterinary Medicine. A, Physiology, Pathology, Clinical Medicine, 51, 196–202.

    Article  CAS  PubMed  Google Scholar 

  • Hisaeda, K., Arima, H., Sonobe, T., Nasu, M., Hagiwara, K., Kirisawa, R., Takahashi, T., Kikuchi, N., Nagahata, H., 2011. Changes in acute-phase proteins and cytokines in serum and milk whey from dairy cows with naturally occurring peracute mastitis caused by Klebsiella pneumoniae and the relationship to clinical outcome, The Journal of Veterinary Medical Science, 73, 1399–1404.

    Article  CAS  PubMed  Google Scholar 

  • Jackson, R.A., Wills, J.R., Kendall, N.R., Green, M.J., Murray, R.D., Dobson, H., 2011. Energy metabolites in pre- and postpartum dairy cattle as predictors of reproductive disorders, Veterinary Record, 28, 168.

    Google Scholar 

  • Jacobsen S., Jensen, J.C., Frei, S., Jensen, A.L., Thoefner, M.B., 2005. Use of serum amyloid A and other acute phase reactants to monitor the inflammatory response after castration in horses: a field study. Equine Veterinary Journal, 37, 552–556.

  • Klasing, K.C., 1988. Nutritional aspects of leukocytic cytokines. Journal of Nutrition, 118, 1436–1446.

    Article  CAS  PubMed  Google Scholar 

  • LeBlanc, S., 2010. Monitoring metabolic health of dairy cattle in the transition period, Journal of Reproduction and Development, 56, 29-35.

    Article  Google Scholar 

  • Lindmark-Mansson, H., Branning, C., Alden, G., 2006. Relationship between somatic cell count, individual leukocyte populations and milk components in bovine udder quarter milk, International Dairy Journal, 16, 717–727.

    Article  Google Scholar 

  • Loor, J.J., Dann, H.M., Guretzky, N.A., Everts, R.E., Oliveira, R., Green, C.A., Litherland, N.B., Rodriguez-ZAS, S.L., Lewin, H.A., Drackley, J.K., 2005. Plane of nutrition prepartum alters hepatic gene expression and function in dairy cows as assessed by longitudinal transcript and metabolic profiling, Physiological Genomics, 27, 29–41.

    Article  CAS  Google Scholar 

  • Maity, S., Das, D., Ambatipudi, K., 2020. Quantitative alterations in bovine milk proteome from healthy, subclinical and clinical mastitis during S. Aureus infection, Journal of Proteomics, 223, 103815.

    Article  CAS  PubMed  Google Scholar 

  • Neumann, S. 2003. Serum iron level as an indicator for inflammation in dogs and cats. Comparative Clinical Pathology, 12, 90–94

    Article  Google Scholar 

  • NRC. 2001. Nutrient requirements of dairy cattle. 7th rev. ed. Natl. Acad. Press, Washington, DC

    Google Scholar 

  • Nyman, A.K., Emanuelson, U., Holtenius, K., Ingvartsen, K.L., Larsen, T., Waller, K.P., 2008. Metabolites and immune variables associated with somatic cell counts of primiparous dairy cows, Journal of Dairy Science, 91, 2996-3009.

    Article  CAS  PubMed  Google Scholar 

  • Ohtsuka, H., Kohiruimaki, M., Hayashi, T., Katsuda, K., Matsuda, K., Masui, M., Abe, R., Kawamura S., 2006. Relationship between leukocyte population and nutritive conditions in dairy herds with frequently appearing mastitis. Journal of Veterinary Medical Science, 68, 113–118.

    Article  PubMed  Google Scholar 

  • Oliveira, L., Ruegg, P.L., 2014. Treatments of clinical mastitis occurring in cows on 51 large dairy herds in Wisconsin, Journal of Dairy Science, 97, 5426–5436.

    Article  CAS  PubMed  Google Scholar 

  • Oliver, S.P., Gillespie B.E., S.J., Headrick, Moorehead, H., Lunn, P.L Dowlen, H.H., Johnson, D.L., Lamar, K.C., Chester, S.T., Moseley, W.M., 2004. Efficacy of extended ceftiofur intramammary therapy for treatment of subclinical mastitis in lactating dairy cows. Journal of Dairy Science, 87, 2393–2400.

  • Petersen, H.H., Nielsen, J.P., Heegaard, P.M.H., 2004. Application of acute phase protein measurements in veterinary clinical chemistry, Veterinary Research, 35, 163–187.

    Article  CAS  PubMed  Google Scholar 

  • Rahularaj, R., Deshapriya, R.,M.,C.,&nbsp;Ranasinghe, R.M.,S.,B.,K., 2019. Influence of bovine sub-clinical mastitis and associated risk factors on calving interval in a population of crossbred lactating cows in Sri Lanka. Tropical Animal Health and Production, 51, 2413-2419.

    Article  CAS  PubMed  Google Scholar 

  • Ranjan R., Swarup D., Naresh R., Patra R.C., 2005. Enhanced erythrocytic lipid peroxides and reduced plasma ascorbic acid, and alteration in blood trace elements level in dairy cows with mastitis. Veterinary Research Communications, 29, 27-34.

    Article  CAS  PubMed  Google Scholar 

  • Roncada P., Piras, C., Soggiu,A ., Turk, R., Urbani, A., Bonizzi, L., 2012. Farm animal milk proteomics. Journal of Proteomics, 75, 4259-4274.

    Article  CAS  PubMed  Google Scholar 

  • Royster, E., Wagner, S., 2015. Treatment of mastitis in cattle, Veterinary Clinics of North America: Food Animal Practice, 31, 17–46.

    Google Scholar 

  • Ruegg, P.L., 2018. Making antibiotic treatment decisions for clinical mastitis, Veterinary Clinics of North America: Food Animal Practice, 34, 413–425.

    Google Scholar 

  • Safi, S., Khoshvaghti, A., Jafarzadeh, S.R., Bolourchi, M., Nowrouzian, I., 2009. Acute phase proteins in the diagnosis of bovine subclinical mastitis, Veterinary Clinical Pathology, 38, 471–476.

    Article  PubMed  Google Scholar 

  • Scaletti, R.W., Trammel, D.S., Smith, B.A., Harmon, R.J., 2003. Role of dietary copper in enhancing resistance to Escherichia coli mastitis, Journal of Dairy Science, 6, 1240–1249.

    Article  Google Scholar 

  • Simojoki, H., Orro, T., Taponen, S., Pyorala, S., 2009. Host response in bovine mastitis experimentally induced with Staphylococcus chromogenes. Veterinary Microbiology, 134, 95–99.

    Article  CAS  PubMed  Google Scholar 

  • Sol, J.,&nbsp;Sampimon, O.C., Snoep, J.J., Schukken, Y.H., 1994. Factors associated with bacteriological cure after dry cow treatment of subclinical Staphylococcal mastitis with antibiotics, Journal of Dairy Science, 77, 75-79.

    Article  CAS  PubMed  Google Scholar 

  • Sol, J., Sampimon, O.C., Barkema, H.W., Schukken, Y.H., 2000. Factors associated with cure after therapy of clinical mastitis caused by Staphylococcus aureus, Journal of Dairy Science, 83, 278–284.

    Article  CAS  PubMed  Google Scholar 

  • Spears, J.W., 2000. Micronutrients and immune function in cattle. Proceedings of the Nutrition Society, 59, 587–594.

    Article  CAS  PubMed  Google Scholar 

  • Spears, J.W., Weiss W.P., 2008. Role of antioxidants and trace elements in health and immunity of transition dairy cows. Veterinary Journal, 176, 70-76.

    Article  CAS  PubMed  Google Scholar 

  • Suriyasathaporn, W., Heuer, C., Noordhuizen-Stassen, E.N., Schukken, Y.H., 2000. Hyperketonemia and udder defense: a review, Veterinary Research, 31, 397-412.

    Article  CAS  PubMed  Google Scholar 

  • Sweeney, R.W., Divers, T.J., Whitlock, R.H., Acland, H.M., Tulleners, E.P., Palmer, J.E., 1988. Hepatic failure in dairy cattle following mastitis or metritis. Journal of Veterinary Internal Medicine, 2, 80–84.

    Article  CAS  PubMed  Google Scholar 

  • Tiwari, J.G., Babra, C., Tiwari, H.K., Williams, V., Wet S.D., Gibson, J., Paxman, A., Morgan, E., Costantino, P., Sunagar, R., Isloor, S., Mukkur, T., 2013. Trends In therapeutic and prevention strategies for management of bovine mastitis: an overview, Journal of Vaccines & Vaccination, 4, 1-11.

    Article  CAS  Google Scholar 

  • Torre P.M., Harmon R.J., Sordillo L.M., Boissonneault G.A., Hemken R.W., Trammell D.S., Clark T.W., 1995. Modulation of bovine mononuclear cell proliferation and cytokine production by dietary copper insufficiency. Journal of Nutritional Immunology, 3, 3-20.

    CAS  Google Scholar 

  • Torre, P.M., Harmon, R.J., Hemken, R.W., Clark, T.W., Trammell D.S., Smith, B.A., 1996. Mild dietary copper insufficiency depresses blood neutrophil function in dairy cattle. Journal of Nutritional Immunology, 4, 3–24.

    CAS  Google Scholar 

  • Turk, R., Rosic, N., Kules, J., Horvatic, A., Gelemanovic, A., Galen, A., Ljubic, B.B., Benic, M., Stevanovic, V., Mrljak, V., Chadwick, C.C., Eckersall, P.D., 2021. Milk and serum proteomes in subclinical and clinical mastitis in Simmental cows. Journal of Proteomics, 244, 104277.

    Article  CAS  PubMed  Google Scholar 

  • Wanger, H.M., Buesher, H.U., Rollinghoff, M., Solbach, W., 1991. Interferon-gamma inhibits the efficacy of interleukin-1 to generate a Th2-cell biased immune response induced by Leishmania major. Immunobiology, 182, 292–306.

    Article  Google Scholar 

  • Wathes, D.C., Fenwick. M., Cheng. Z., Bourne, N., Llewellyn, S., Morris, D.G., Kenny, D., Murphy, J., Fitzpatrick, R., 2007. Influence of negative energy balance on cyclicity and fertility in the high producing dairy cow, Theriogenology, 68, 232–241.

    Article  CAS  Google Scholar 

  • Weiss, W.P., Spears, J.W., 2006. Vitamin and trace mineral effects on immune function of ruminants, In: Sejrsen, K., Hvelplund, T., Nielsen, M.O., Ruminant Physiology. Utrecht, Wageningen Academic Publishers, 473–496

  • Zaatout, N., Ayachi, A., Kecha, M., 2019. Epidemiological investigation of subclinical bovine mastitis in Algeria and molecular characterization of biofilm-forming Staphylococcus aureus, Tropical Animal Health and Production, 52, 283–292.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Dr. Fallah Rad, Ferdowsi University of Mashhad, who kindly helped us for English revision of the manuscript.

Funding

The present study was supported by the Ferdowsi University of Mashhad (grant number 3/46066).

Author information

Authors and Affiliations

  1. Department of Clinical Sciences, School of Veterinary Medicine, Ferdowsi University of Mashhad, PO Box 91775-1793, Mashhad, Iran

    N. Golshan, B. Khoramian Toosi & M. Heidarpour

  2. Center of Excellence in Ruminant Abortion and Neonatal Mortality, School of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran

    M. Heidarpour

Authors
  1. N. Golshan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Khoramian Toosi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Heidarpour
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

N. Golshan: investigation, methodology, writing. M. Heidarpour: conceptualization, methodology, validation, formal analysis, writing—review and editing, supervision. B. Khoramian Toosi: writing—original draft, methodology, investigation.

Corresponding author

Correspondence to M. Heidarpour.

Ethics declarations

Ethics approval

The present study was confirmed by the Animal Welfare Committee of the Ferdowsi University of Mashhad with the code of 3/46066 under the institutional, national, and international guidelines.

Consent to participate

The authors declare that all authors have contributed significantly and are in agreement with the content of the manuscript.

Consent for publication

The authors declare that the work described here has not been published before, that it is not under consideration for publication anywhere else, and that the publisher has the author’s permission to publish the relevant contribution.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Golshan, N., Toosi, B.K. & Heidarpour, M. The relationship of metabolic parameters and milk acute-phase protein with the outcome of treatment of Staphylococcus aureus subclinical mastitis in dairy cows. Trop Anim Health Prod 53, 489 (2021). https://doi.org/10.1007/s11250-021-02942-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11250-021-02942-6

Keywords

Search

Navigation