Animal Reproduction (AR)
Animal Reproduction (AR)

Oxidative stress, ceruloplasmin and neopterin biomarkers in dromedary camels with clinical endometritis

Wael El-Deeb; Mohammed Ali Abdelghani; Abdulrahman Alhaider; Mahmoud Fayez

Downloads: 0
Views: 379


The purpose of this study is to investigate the role of some oxidative stress (OS), ceruloplasmin (Cp), and neopterin (NPT) as diagnostic biomarkers for dromedary camels endometritis as well as to explore the impact of ceftiofur treatment on endometritis. Camels were categorized into two groups; healthy control group (n = 20) and endometritis group (n = 60). She-camels with clinical signs of endometritis (CE) received 6.6 mg/kg BW of ceftiofur (i/m). On days 7, and 14, she-camels were evaluated and clinical cure or failure to cure was determined. The comparison of the groups for OS demonstrated that endometritis caused an increase in serum malondialdehyde (sMDA), Cp, and NPT levels (P<0.05), but decreased serum levels of superoxide dismutase (SOD), catalase (CAT), and glutathione (GSH) (P<0.05). The most prevalent pathogens involved in the etiology of CE are Arcanobacterium pyogenes, Streptococcus pyogenes, and Staphylococcus aureus. All examined biomarkers demonstrated a high degree of recognition between CE camel and healthy controls (the area under the curve (AUC) was 95.9 for NPT). A higher proportion of camels with CE that were treated with ceftiofur (90%, P<0.0001) showed clinical cure by the first dose, while 10% required a second dose. In conclusion, CE causes increased oxidative reactions and decreased antioxidant defense competence. Subsequently, the alteration in that balance that was represented by the biomarkers of OS could be beneficial for clinical practice and basic clinical research. Additionally, all trials demonstrated the efficacy of ceftiofur for the treatment of CE in she-camel.


camel, ceftiofur, endometritis, neopterin, ceruloplasmin


Adamczyk-Sowa M, Sowa P, Mucha S, Zostawa J, Mazur B, Owczarek M, Pierzchała K. Changes in serum ceruloplasmin levels based on immunomodulatory treatments and melatonin supplementation in multiple sclerosis patients. Med Sci Monit. 2016;22:2484-91. PMid:27420299.

Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121-6. PMid:6727660.

Andrei S, Matei S, Rugina D, Bogdan L, Ştefănuţ C. Interrelationships between the content of oxidative markers, antioxidative status, and somatic cell count in cow’s milk. Czech J Anim Sci. 2016;61(9):407-13.

Belina D, Eshetu A, Alemu S, Shasho B, Mohammed T, Mohammed A, Mummed B, Regassa D. Reproductive diseases and disorders of female camels: an assessment and pathological and bacteriological study in eastern Ethiopia. Vet Med Int. 2021;2021:6641361. PMid:33953900.

Chambers HR. Beta-lactam and other cell wall and membrane-active antibiotics. In: Katzung BG, editor. Basic and clinical pharmacology. 10th ed. New York: McGraw Hill Medical; 2007. p. 726-44.

Chenault JR, McAllister JF, Chester T, Dame KJ, Kausche FM, Robb EJ. Efficacy of ceftiofur hydrochloride sterile suspension administered parenterally for the treatment of acute postpartum metritis in dairy cows. J Am Vet Med Assoc. 2004;224:1634-9. PMid:15154734.

Dalle-Donne I, Rossi R, Colombo R, Giustarini D, Milzani A. Biomarkers of oxidative damage in human disease. Clin Chem. 2006;52(4):601-23. PMid:16484333.

Drillich M, Arlt S, Kersting S, Bergwerff AA, Scherpenisse P, Heuwieser W. Ceftiofur derivatives in serum, uterine tissues, cotyledons, and lochia after fetal membrane retention. J Dairy Sci. 2006;89(9):3431-8. PMid:16899676.

Ehsaei M, Khajavi M, Arjmand MH, Abuee MA, Ghayour-Mobarhan M, Alamdari DH. Prooxidant-antioxidant balance in patients with traumatic brain injury. Acta Neurol Belg. 2015;115(1):69-73. PMid:25027161.

El-Deeb W, Elsohaby I, Fayez M, Mkrtchyan H, El-Etriby D, ElGioushy M. 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 Trop. 2020;204:105336. PMid:31926143.

El-Deeb W, Fayez M, Alhumam N, Elsohaby I, Quadri SA, Mkrtchyan H. The effect of staphylococcal mastitis including resistant strains on serum procalcitonin, neopterin, acute phase response and stress biomarkers in Holstein dairy cows. PeerJ. 2021;9:e11511. PMid:34131523.

El-Deeb W, Ghoneim I, Fayez M, Elsohaby I, Alhaider A, ElGioushy M. Acute phase proteins, proinflammatory cytokines and oxidative stress biomarkers in sheep, goats and she-camels with Coxiella burnetii infection induced abortion. Comp Immunol Microbiol Infect Dis. 2019;67:101352. PMid:31568899.

El-Deeb WM, Buczinski S. The diagnostic and prognostic importance of oxidative stress biomarkers and acute phase proteins in urinary tract infection (UTI) in camels. PeerJ. 2015;3:e1363. PMid:26587339.

El-Deeb WM, Elmoslemany AM. Cardiac and oxidative stress biomarkers in Trypanosoma evansi infected camels: diagnostic and prognostic prominence. Parasitology. 2015;142(6):767-72. PMid:25578857.

Erskine RJ, Bartlett PC, VanLente JL, Phipps CR. Efficacy of systemic ceftiofur as a therapy for severe clinical mastitis in dairy cattle. J Dairy Sci. 2002;85(10):2571-5. PMid:12416809.

Galvão KN, Greco LF, Vilela JM, Sá MF Fo, Santos JEP. Effect of intrauterine infusion of ceftiofur on uterine health and fertility in dairy cows. J Dairy Sci. 2009;92(4):1532-42. PMid:19307634.

Gardner IA, Greiner M. Receiver-operating characteristic curves and likelihood ratios: improvements over traditional methods for the evaluation and application of veterinary clinical pathology tests. Vet Clin Pathol. 2006;35(1):8-17. PMid:16511785.

Gaschler MM, Stockwell BR. Lipid peroxidation in cell death. Biochem Biophys Res Commun. 2017;482(3):419-25. PMid:28212725.

Gosmaro F, Bagnati M, Berto S, Bellomo G, Prenesti E. Measurement of total antioxidant capacity of human plasma: setting and validation of the CUPRAC-BCS method on routine apparatus ADVIA 2400. Talanta. 2013;115:526-32. PMid:24054628.

Haimerl P, Heuwieser WJ. Invited review: antibiotic treatment of metritis in dairy cows: a systematic approach. J Dairy Sci. 2014;97(11):6649-61. PMid:25218751.

Hanafi EM, Ahmed WM, Sherein I, Moez AE, Khadrawy HHE, Hameed AEAR. Effect of clinical endometritis on ovarian activity and oxidative stress status in Egyptian buffalo. Am-Eurasian J Agric Environ Sci. 2008;4:530-6.

He L, He T, Farrar S, Ji L, Liu T, Ma X. Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species. Cell Physiol Biochem. 2017;44(2):532-53. PMid:29145191.

Hornish RE, Katarski SF. Cephalosporins in veterinary medicine – Ceftiofur use in food animals. Curr Top Med Chem. 2002;2(7):717-31. PMid:12052187.

Jeon SJ, Cunha F, Daetz R, Bicalho RC, Bicalho RC, Lima S, Galvão KN. Ceftiofur reduced Fusobacterium leading to uterine microbiota alteration in dairy cows with metritis. Anim Microbiome. 2021;3(1):15. PMid:33509303.

Kandeel M, El-Deeb W, Fayez M, Ghoneim I. Pharmacokinetics of the long-acting ceftiofur crystalline-free acid in arabian she-camels (camelus dromedarius). Slov Vet Res. 2021;58:95-101.

Lima FS, Vieira-Neto A, Vasconcellos GS, Mingoti RD, Karakaya E, Solé E, Bisinotto RS, Martinez N, Risco CA, Galvão KN, Santos JE. Efficacy of ampicillin trihydrate or ceftiofur hydrochloride for treatment of metritis and subsequent fertility in dairy cows. J Dairy Sci. 2014;97(9):5401-14. PMid:24952780.

Malinowski E, Lassa H, Markiewicz H, Kaptur M, Nadolny M, Niewitecki W, Zietara J. Sensitivity to antibiotics of Arcanobacterium pyogenes and Escherichia coli from the uteri of cows with metritis/endometritis. Vet J. 2011;187(2):234-8. PMid:20129803.

Mandrekar JN. Receiver operating characteristic curve in diagnostic test assessment. J Thorac Oncol. 2010;5(9):1315-6. PMid:20736804.

Murr C, Widner B, Wirleitner B, Fuchs D. Neopterin as a marker for immune system activation. Curr Drug Metab. 2002;3(2):175-87. PMid:12003349.

Nielsen F, Mikkelsen BB, Nielsen JB, Andersen HL, Grandjean P. Plasma malondialdehyde as a biomarker for oxidative stress: reference interval and effects of life style factors. Clin Chem. 1997;43(7):1209-14. PMid:9216458.

Oliveira EB, Cunha F, Daetz R, Figueiredo CC, Chebel RC, Santos JE, Risco CA, Jeong KC, Machado VS, Galvão KN. Using chitosan microparticles to treat metritis in lactating dairy cows. J Dairy Sci. 2020;103(8):7377-91. PMid:32505402.

Peng QL, Zhang YM, Liang L, Liu X, Ye LF, Yang HB, Zhang L, Shu XM, Lu X, Wang GC. A high level of serum neopterin is associated with rapidly progressive interstitial lung disease and reduced survival in dermatomyositis. Clin Exp Immunol. 2020;199(3):314-25. PMid:31797350.

Sheldon IM, Lewis GS, LeBlanc S, Gilbert RO. Defining postpartum uterine disease in cattle. Theriogenology. 2006;65(8):1516-30. PMid:16226305.

Sheldon IM, Noakes DE, Rycroft AN, Dobson H. Effect of postpartum manual examination of the vagina on uterine bacterial contamination in cows. Vet Rec. 2002a;151(18):531-4. PMid:12448489.

Sheldon IM, Noakes DE, Rycroft AN, Pfeiffer DU, Dobson H. Influence of uterine bacterial contamination after parturition on ovarian dominant follicle selection and follicle growth and function in cattle. Reproduction. 2002b;123(6):837-45. PMid:12052238.

Su LJ, Zhang JH, Gomez H, Murugan R, Hong X, Xu D, Jiang F, Peng ZY. Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis. Oxid Med Cell Longev. 2019;2019:5080843. PMid:31737171.

Sunderman FW Jr, Nomoto S. Measurement of human serum ceruloplasmin by its p-phenylenediamine oxidase activity. Clin Chem. 1970;16(11):903-10. PMid:5473551.

Tiwari A, Singh P, Sharma S, Prakash A, Mandil R, Choudhury S, Garg SK. Influence of experimentally-induced endometritis on redox state and comparative modulatory efficacy of eucalyptus robusta leaves crude extract and cefixime in rats. J Vet Pharmacol Toxicol. 2017;16:69-76.

Wang Y, Branicky R, Noe A, Hekimi S. Superoxide dismutases: dual roles in controlling ROS damage and regulating ROS signaling. J Cell Biol. 2018;217(6):1915-28. PMid:29669742.

Wernerry U, Kumar BN. Reproductive disorders in dromedary camels due to infectious causes and its treatment. J Camel Pract Res. 1994;1:85-7.

Williams EJ, Fischer DP, Noakes DE, England GC, Rycroft A, Dobson H, Sheldon IM. The relationship between uterine pathogen growth density and ovarian function in the postpartum dairy cow. Theriogenology. 2007;68(4):549-59. PMid:17574659.

Submitted date:

Accepted date:

631f3823a953953f61309724 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections