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Research on acute phase proteins and inflammatory cytokines biomarkers in dromedary camels (Camelus dromedarius) with clinical endometritis

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Abstract

Uterine diseases are prevalent in camels and lead to economic losses because of decreased fertility. The aim of this study is to look into the expression patterns of acute-phase proteins (APPs) and inflammatory cytokines in dromedary camels with clinical endometritis (CE) to highlight their role in the immune pathogenesis of the disease. Moreover, to identify the use of these parameters as a complementary tool for CE screening as well as investigate the efficacy of ceftiofur antibiotic, APPs and inflammatory cytokines were estimated in camels with CE. Values of APPs (Hp, SAA, and Fg), pro-inflammatory (IFN-γ, TNF-α, IL-1α, IL-1β, and IL-6), and anti-inflammatory cytokines (IL-10) were higher in camels with CE than in healthy controls (P < 0.05). The strongest correlations were observed between HP and IFN-γ (r = 0.73) and IL-1β and IL-6 (r = 0.73), while the weakest correlations were observed between Fg and IFN-γ (r = 0.25). Corynebacterium pyogenes and Arcanobacterium pyogenes were the most common pathogens involved in the etiology of CE. All investigated biomarkers demonstrated a high degree of recognition between CE camel and healthy controls (AUC was > 0.90). A higher proportion of camels with CE that were treated with ceftiofur (90%, P < 0.0001) scored clinical cures after the first dose, while 10% required a second dose. In conclusion, CE causes increased APPs and inflammatory cytokine biomarkers, indicating a significant acute phase response in diseased camels with CE. These changes in biomarkers could be beneficial for understanding the immune pathogenesis of CE in dromedary camels, clinical practice, and basic clinical research.

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Data availability

The data that support the findings of this study are available on request from the corresponding author.

References

  • Andrei S., Matei S., Rugina D., Bogdan L., and Ştefănuţ C. 2016. Interrelationships between the content of oxidative markers, antioxidative status, and somatic cell count in cow’s milk. Czech Journal of Animal Science, 61: 407–443.

    Article  CAS  Google Scholar 

  • Belina D., Eshetu, A., Alemu S., Shasho B., Mohammed T., Mohammed A., Mummed B., and Regassa., D. 2021. Reproductive Diseases and Disorders of Female Camels: An Assessment and Pathological and Bacteriological Study in Eastern Ethiopia. Veterinary Medicine International, 13: 6641361.

    Google Scholar 

  • Bhadaniya A. R., Prasad M. C., Savsani H. H., Kalaria V.A., Fefar D. T., Mathpati B.S., and Javia B. B. 2019. Pro-inflammatory cytokine expression studies of subclinical and clinical endometritis in endometrial tissues of buffaloes. Tropical Animal Health and Production, 51: 1161-1166.

    Article  CAS  Google Scholar 

  • Brodzkia P., Kostro K., Krakowski L., and Marczuk J. 2015a. Inflammatory cytokine and acute phase protein concentrations in the peripheral blood and uterine washings of cows with subclinical endometritis in the late postpartum period. Veterinary Research Communication, 39:143–149.

    Article  Google Scholar 

  • Brodzkia P., Kostrob K., Brodzkic A., Wawrona W., Marczukd J., and Kurekd L. 2015b. Inflammatory cytokines and acute-phase proteins concentrations in the peripheral blood and uterus of cows that developed endometritis during early postpartum. Theriogenology, 84: 11-18.

    Article  Google Scholar 

  • Cavalli G., Colafrancesco S., Emmi G., Imazio M., Lopalco G., Maggio M. C., Sota J., and Dinarello C. A. 2021. Interleukin 1α: a comprehensive review on the role of IL-1α in the pathogenesis and treatment of autoimmune and inflammatory diseases. Review Autoimmune Review, 20: 102763.

    Article  CAS  Google Scholar 

  • Chambers H.R. 2007. Beta-lactam and other cell wall and membrane-active antibiotics. In: Katzung B.G. Basic and Clinical Pharmacology. 10th. McGraw Hill Medical, New York, NY: 726–744.

  • Chapwanya A., Meade K. G., Doherty M. L., Callanan J. J., and O’Farrelly C. 2013. Endometrial epithelial cells are potent producers of tracheal antimicrobial peptide and serum amyloid A3 gene expression in response to E. coli stimulation. Veterinary Immunology and Immunopathology, 151: 157–162.

    Article  CAS  Google Scholar 

  • Chenault J. R., McAllister J. F., Chester T., Dame K. J., Kausche F. M., and Robb E. J. 2004. Efficacy of ceftiofur hydrochloride administered parenterally for the treatment of acute postpartum metritis in dairy cows. Journal of American Veterinary Medical Association, 224: 1634-1639.

    Article  CAS  Google Scholar 

  • Couper K. N., Blount D.G., Riley E. M. 2008. IL-10: the master regulator of immunity to infection. The Journal of Immunology, 180: 5771–5777.

    Article  CAS  Google Scholar 

  • Cray C., Zaias J., and Altman N. H. 2009. Acute phase response in animals: A review. Complementary Medicine Journal, 59: 517–526.

    CAS  Google Scholar 

  • Dalle-Donne I., Rossi R., Colombo R., Giustarini D., and Milzani A. 2006. Biomarkers of Oxidative Damage in Human Disease. Clinical Chemistry, 52: 601–623.

    Article  CAS  Google Scholar 

  • Davalos D., and Akassoglou K. 2012. Fibrinogen as a key regulator of inflammation in disease. Seminars in Immunopathology 34: 43–62.

    Article  CAS  Google Scholar 

  • Davies D., Meade K. G., Herath S., Eckersall P. D., Gonzalez D., White J. O., Conlan R. S., O’Farrelly C., and Sheldon I. M. 2008. Toll-like receptor and antimicrobial peptide expression in the bovine endometrium. Endocrinology and Reproductive Biology, 6, e53.

    Article  Google Scholar 

  • Davis, M. F., Cain, C. L., Brazil, A. M., and Rankin, S. C. 2013. Two coagulase-negative staphylococci emerging as potential zoonotic pathogens: wolves in sheep’s clothing? Front. Microbiol. Antimicrob. Resis. Chemoth. 4:123. https://doi.org/10.3389/fmicb.2013.00123

    Article  Google Scholar 

  • Di Paolo N. C., and Shayakhmetov D. M. 2016. Interleukin 1α and the inflammatory process. Nature Immunology, 17: 906–913.

    Article  Google Scholar 

  • Dinarello C. A. 1991. Interleukin-1 and interleukin-1 antagonism. Blood, 77: 1627–1652.

    Article  CAS  Google Scholar 

  • Dinarello C. A. 2005. Blocking IL-1 in systemic inflammation. Journal of Experimental Medicine, 201: 1355–1359.

    Article  CAS  Google Scholar 

  • Dmowski W. P., and Braun D.P. 2004. Immunology of endometriosis. Best Practice and Research in Clinical Obstetrics and Gynaecology, 18: 245–263.

    Article  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., and 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  Google Scholar 

  • El-Deeb W. M., Ghoneim I., Fayez M., Elsohaby I., Alhaider A., and ElGioushy M. 2019. Acute phase proteins, proinflammatory cytokines and oxidative stress biomarkers in sheep, goats and she-camels with Coxiella burnetii infection induced abortion. Comparative Immunology, Microbiology and Infectious Diseases, 67: 101352.

    Article  Google Scholar 

  • El-Deeb W., Elsohaby I., Fayez M. Mkrtchyan H., El-Etriby D., ElGioushy M. 2020. Use of procalcitonin, neopterin, haptoglobin, serum amyloid A and proinflammatory cytokines in diagnosis and prognosis of bovine respiratory disease in feedlot calves under field conditions. Acta Tropica, 204: 105336.

    Article  CAS  Google Scholar 

  • El-Deeb W., Fayez M., Alhumam N., Elsohaby I., Quadri S. A., and Mkrtchyan H. 2021. The effect of staphylococcal mastitis including resistant strains on serum procalcitonin, neopterin, acute phase response and stress biomarkers in Holstein dairy cows. Peer J, 9: e11511.

    Article  Google Scholar 

  • Gabay C., Kushner I. 1999. Acute-phase proteins and other systemic responses to inflammation. The New England journal of medicine, 340: 448–454.

    Article  CAS  Google Scholar 

  • Galvao K. N., Greco L. F., Vilela J. M., Sa Filho M. F., and Santos, J. E. P. 2009. Effect of intrauterine infusion of ceftiofur on uterine health and fertility in dairy cows. Journal of Dairy Science, 92: 1532–1542.

    Article  CAS  Google Scholar 

  • Gardner I. A., and Greiner M. 2006. Receiver-operating characteristic curves and likelihood ratios: improvements over traditional methods for the evaluation and application of veterinary clinical pathology tests. Veterinary Clinical Pathology, 35: 8–17.

    Article  Google Scholar 

  • Heegaard P. M., Godson D. L., Toussaint M.J., TjØrnehØj K., Larsen L. E., Viuff B. and RØnsholt L. 2000. The acute phase response of haptoglobin and serum amyloid A (SAA) in cattle undergoing experimental infection with bovine respiratory syncytial virus. Veterinary Immunology and Immunopathology, 77: 151-159.

    Article  CAS  Google Scholar 

  • Hirvonen J., and Pyörälä, S. 1998. Acute-phase response in dairy cows with surgically-treated abdominal disorders. Veterinary Journal, 155: 53-61.

    Article  CAS  Google Scholar 

  • Hornish R.E., and Kotarski, S.F. 2002. Cephalosporins in veterinary medicine – Ceftiofur use in food animals. Current Topics in Medicinal Chemistry, 2:717–731.

    Article  CAS  Google Scholar 

  • Jain S., Gautam V., and Naseem S. 2011. Acute-phase proteins: As diagnostic tool. Journal Pharmacy and Bioallied Sciences, 3: 118–127.

    Article  CAS  Google Scholar 

  • Kak G., Raza M., and Tiwari B. K. 2018. Interferon-gamma (IFN-γ): Exploring its implications in infectious diseases. Biomolecular Concepts, 9: 64–79.

    Article  CAS  Google Scholar 

  • Kandeel M., El-Deeb W., Fayez M., and Ghoneim I. 20121. pharmacokinetics of the long-acting ceftiofur crystalline-free acid in arabian she-camels (camelus dromedarius). Slovenian Veterinary Research, 58: 95 –101.

    Google Scholar 

  • Kim H., GuKang H., KwanJeong J., YoungHur T., and HunJung Y. 2014. Inflammatory cytokine concentrations in uterine flush and serum samples from dairy cows with clinical or subclinical endometritis. Theriogenology, 82: 427-432.

    Article  CAS  Google Scholar 

  • Klasing K. C., Laurin D. E., Peng R. K., and Fry D. M. 1987. Immunologically mediated growth depression in chicks: Influence of feed intake, corticosterone and interleukin-1. The Journal of Nutrition, 117: 1629–1637.

    Article  CAS  Google Scholar 

  • Laura L., Healy James G., Cronin I., and Sheldon M. 2015. Endometrial cells sense and react to tissue damage during infection of the bovine endometrium via interleukin 1. Scientific Reports, 4: 7060 | https://doi.org/10.1038/srep07060.

    Article  CAS  Google Scholar 

  • Leung, S. T., Cheng, Z., heldrick, E. L., Derecka, K., Derecka, K., Flint, A. P., and Wathes, D. C. 2001. The effects of lipopolysaccharide and interleukins-1alpha, -2 and -6 on oxytocin receptor expression and prostaglandin production in bovine endometrium. Journal of Endocrinology, 168: 497–508.

    Article  CAS  Google Scholar 

  • Li C., Corraliza I., and Langhorne J. 1999. A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect. Immunology, 67: 4435-4442.

    CAS  Google Scholar 

  • Lu D., Song H., and Shi G. 2013. Anti-TNF-α treatment for pelvic pain associated with endometriosis. Cochrane Database of Systematic Reviews, 3: CD008088.

    Google Scholar 

  • Mandrekar J. N. 2010. Receiver Operating Characteristic Curve in Diagnostic Test Assessment. Journal of Thoracic Oncology, 5: 1315-1316.

    Article  Google Scholar 

  • Meade K. G., O'Gorman G. M., Hill E. W., Narciandi F., Agaba M., Kemps S. J., O'Farrellys C., and MacHughs D. E. 2009. Divergent antimicrobial peptide (AMP) and acute phase protein (APP) responses to Trypanosoma congolense infection in trypanotolerant and trypanosusceptible cattle. Molecular Immunology Journal, 47: 196-204.

    Article  CAS  Google Scholar 

  • Medcalf R. L. 2007. Fibrinolysis, inflammation and regulation of the plasminogen activating system. Journal of Thrombosis and Haemostasis 5: 132–142.

    Article  CAS  Google Scholar 

  • Moore K. W., Malefyt D. W., Coffman R. L., O’Garra A. 2001. Interleukin-10 and the interleukin-10 receptor. Annual Review of Immunology, 19: 683-765

    Article  CAS  Google Scholar 

  • Murata H., Shimada N., and Yoshioka M. 2004. Current research on acute phase proteins in veterinary diagnosis: an overview. The Veterinary Journal, 168: 28–40.

    Article  CAS  Google Scholar 

  • Nasreldin N., FAZ A., Abd-Elhafeez H. H., Hassan M., El-Zeftawy M., and Senosy W. 2020. Characterization of immunological, biochemical and inflammatory response of clinical and subclinical endometritis in ewes in the subtropics. Animal Reproduction Science, 219: 106541.

    Article  CAS  Google Scholar 

  • Okuda K., Sakumoto R., Okamoto N., Acosta T. J., Abe H., Okada H., Sinowatz F., and Skarzynski D. J. Cellular localization of genes and proteins for tumor necrosis factor-α (TNF), TNF receptor types I and II in bovine endometrium. Molecular and Cellular Endocrinology, 2330: 41–48.

    Article  Google Scholar 

  • Opal S. M., and DePalo V. A. 2000. Anti-inflammatory cytokines. Chest, 117: 1162–1172.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Plata-Salamán C. R., and Borkoski J. P. 1994. Chemokines/intercrines and central regulation of feeding. American Journal of Physiology, 266: R1711–R 1715.

    Google Scholar 

  • Raynes J. D. 1994. The acute phase response. Biochemical Society Transactions, 22: 69–74.

    Article  CAS  Google Scholar 

  • Richards C., Gauldie J., and Baumann H. 1991. Cytokine control of acute phase protein expression. European Cytokine Network, 2: 89–98.

    CAS  Google Scholar 

  • Rider P., Carmi Y., Voronov E., and Apte R. N. 2013. Interleukin-1α. Seminars in Immunology, 25 : 430-438.

    Article  CAS  Google Scholar 

  • Rubel C., Fernàndez G., Dran G., Bompadre M., Isturiz M., and Palermo M. 2001. Fibrinogen Promotes Neutrophil Activation and Delays Apoptosis. Journal of Immunology, 166: 2002-2010.

    Article  CAS  Google Scholar 

  • Sheldon I. M., Noakes D. E., Rycroft A., and Dobson H. 2001. Acute phase protein response to postpartum uterine bacterial contamination in cattle. Veterinary Record, 148: 172–175.

    Article  CAS  Google Scholar 

  • Sheldon I. M., Lewis G. S., LeBlanc S., and Gilbert R.O. 2006. Defining postpartum uterine disease in cattle. Theriogenology, 65: 1516-1530.

    Article  Google Scholar 

  • Sheldon M., Cronin J., Goetze L., Donofrio G., and Schuberth H. J. 2009: Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biology of Reproduction, 81: 1026–1032.

    Article  Google Scholar 

  • Singh J., Murray R. D., Mshelia G., and Woldehiwet Z. 2008. The immune status of the bovine uterus during the peripartum period. Veterinary Journal, 175: 301–309.

    Article  CAS  Google Scholar 

  • Tanikawa, M., Acosta, T. J., Fukui, T., Murakami, S., Korzekwa, A., Skarzynski, D. J., Piotrowska, K. K., Park, C. K., and Okuda, K. 2005. Regulation of prostaglandin synthesis by interleukin-1alpha in bovine endometrium during the estrous cycle. Prostaglandins and Other Lipid Mediators Journal, 78: 279–290.

    Article  CAS  Google Scholar 

  • Thomas J. S. 2000. Overview of plasma proteins. In: Schalm’s Veterinary Hematology, 5thedn, eds B. F. Feldman, J. G. Zinkl & N. C. Jain, Lippincott Williams, Wilkins, Philadelphia, pp. 891–898.

    Google Scholar 

  • Tothova C. S., Nagy O., Seidel H., Konvicna J., Farkasova Z., and Kovac G. 2008. Acute phase proteins and variables of protein metabolism in dairy cows during the preand postpartal period. Acta Veterinaria Brno Journal, 77: 51–57.

    Article  Google Scholar 

  • Tothova C. S., Nagy O., Seidel H., and Kovac G. 2014. Acute phase proteins and their use in the diagnosis of diseases in ruminants: a review. Veterinary Medicine Czech, 59: 163–180.

    Article  Google Scholar 

  • Turner M. L., Healey G. D., Sheldon I. M. 2012: Immunity and inflammation in the uterus. Reproduction Domestic Animal, 47: 402–409.

    Article  Google Scholar 

  • Wernerry U., and Kumar B. N. 1994. Reproductive disorders in dromedary camels due to infectious causes and its treatment. Journal of Camel Practice and Research, 1: 85-87.

    Google Scholar 

  • Zhang J. M., and An J. 2007. Cytokines, Inflammation and Pain. International Anesthesiology Clinics, 45: 27–37.

    Article  CAS  Google Scholar 

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Funding

This work was supported by the Deanship of Scientific Research, Vice Presidency for Graduate Studies and Scientific Research, King Faisal University, Saudi Arabia (Grant No. 1478). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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  1. W. El-Deeb and Mohammed A. Abdelghani equally contributed.

Authors and Affiliations

  1. Department of Clinical Sciences, College of Veterinary Medicine, King Faisal University, Al Hofuf, Al-Ahsa, 31982, Saudi Arabia

    W. El-Deeb & A. Alhaider

  2. Department of Internal Medicine, Infectious Diseases and Fish Diseases, Faculty of Veterinary Medicine, Mansoura University, Mansoura, Egypt

    W. El-Deeb

  3. Department of Theriogenology, Faculty of Veterinary Medicine, Assiut University, Assiut, 71526, Egypt

    Mohammed A. Abdelghani

  4. Al Ahsa Veterinary Diagnostic Laboratory, Ministry of Environment, Water and Agriculture, Al Hofuf, Saudi Arabia

    M. Fayez

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  1. W. El-Deeb
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WE and MAA: contributed equally to the study design, acquisition of data, data collection, manuscript preparation, analysis or interpretation, revisions, and final approval of the paper. AH and MF: study design, data collection, and study supervision.

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El-Deeb, W., Abdelghani, M.A., Alhaider, A. et al. Research on acute phase proteins and inflammatory cytokines biomarkers in dromedary camels (Camelus dromedarius) with clinical endometritis. Trop Anim Health Prod 54, 361 (2022). https://doi.org/10.1007/s11250-022-03356-8

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