Systemic inflammatory and stress markers in cattle and sheep submitted to different reproductive procedures

Costa, Vitória Gasperin Guazzelli; Vieira, Arnaldo Diniz; Schneider, Augusto; Rovani, Monique Tomazele; Gonçalves, Paulo Bayard Dias; Gasperin, Bernardo Garziera

doi:10.1590/0103-8478cr20180336

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ANIMAL PRODUCTION • Cienc. Rural 48 (12) • 2018 • https://doi.org/10.1590/0103-8478cr20180336 copy

Systemic inflammatory and stress markers in cattle and sheep submitted to different reproductive procedures

Marcadores sistêmicos de inflamação e estresse em bovinos e ovinos submetidos a diferentes procedimentos reprodutivos

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT:

Previous studies have evaluated the effects of different reproductive procedures on discomfort markers in sheep and cattle. Such studies may help stimulate the adoption of techniques that are more beneficial for animal welfare. However, markers that are commonly used to evaluate discomfort are highly influenced by external factors. To overcome this, several systemic markers can be evaluated to more precisely identify stress, pain, and inflammation. Such markers include cortisol, acute phase proteins, bradykinin, and substance P. We aimed to review the potential markers of stress, pain, and inflammation, and discuss how and when they are regulated after different stimuli related to reproductive procedures in cattle and sheep. Furthermore, we aimed to review how reproductive procedures with different degrees of invasiveness cause stress and provide information that may help develop strategies to limit animal discomfort.

Key words:
acute phase proteins; cortisol; discomfort; reproductive techniques

Authorship

Vitória Gasperin Guazzelli Costa

Faculdade de Veterinária, Universidade Federal de Pelotas (UFPel), Campus Universitário, 96010-900, Capão do Leão, RS, Brasil. Universidade Federal de Pelotas (UFPel)BrazilCapão do Leão, RS, BrazilFaculdade de Veterinária, Universidade Federal de Pelotas (UFPel), Campus Universitário, 96010-900, Capão do Leão, RS, Brasil.

Arnaldo Diniz Vieira

Augusto Schneider

http://orcid.org/0000-0002-3410-2860

Monique Tomazele Rovani

Paulo Bayard Dias Gonçalves

Programa de Pós-graduação em Bioquímica, Programa de Pós-graduação em Ciência Animal, Universidade Federal do Pampa (Unipampa), Campus Uruguaiana, RS, Brasil.Universidade Federal do Pampa (Unipampa)BrazilUruguaiana, RS, BrazilPrograma de Pós-graduação em Bioquímica, Programa de Pós-graduação em Ciência Animal, Universidade Federal do Pampa (Unipampa), Campus Uruguaiana, RS, Brasil.

Programa de Pós-graduação em Medicina Veterinária, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brasil.Universidade Federal de Santa Maria (UFSM)BrazilSanta Maria, RS, BrazilPrograma de Pós-graduação em Medicina Veterinária, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brasil.

http://orcid.org/0000-0002-0671-1466

Bernardo Garziera Gasperin ^*E-mail: bggasperin@gmail.com. *Corresponding author.

http://orcid.org/0000-0002-3715-2345

E-mail: bggasperin@gmail.com. ^*Corresponding author.

DECLARATION OF CONFLICTING INTERESTS

The authors declare no conflict of interest. The founding sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.

AUTHORS’ CONTRIBUTIONS

The authors contributed equally to the manuscript.

SCIMAGO INSTITUTIONS RANKINGS

Tables

Tables (1)

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Table 1
Effect of different reproductive procedures on systemic markers of discomfort, stress, and inflammation.

Table 1 Effect of different reproductive procedures on systemic markers of discomfort, stress, and inflammation.

Authors	Procedure	Sp.	Main results
MARTIN et al. (1981MARTIN, G. B., et al. Effect of stress due to laparoscopy on plasma cortisol levels, the preovulatory surge of LH, and ovulation in the ewe. Theriogenology, v.16, n.1, p.39-44, 1981. Available from: <Available from: http://www.sciencedirect.com/science/article/pii/0093691X81901114 >. Accessed: Feb. 01, 2018. doi: 10.1016/0093-691x(81)90111-4. http://www.sciencedirect.com/science/art... )	Laparoscopy	O	Cortisol peak (60ng/mL or 165.5nmol/L) after one laparoscopy and concentrations between 70 to 100ng/mL (193.1 to 275.9nmol/L) after two laparoscopic procedures (12h interval).
COHEN et al. (1990COHEN, R., et al. Efficacy and stress of chemical versus surgical castration of cattle. Canadian Journal of Animal Science, v.70, n.4, p.1063-1072, 1990. Available from: <Available from: http://www.nrcresearchpress.com/doi/10.4141/cjas90-129#.W8pa4hNKh1M >. Accessed: Feb. 01, 2018. doi: 10.4141/cjas90-129. http://www.nrcresearchpress.com/doi/10.4... )	Chemical castration	B	Lower cortisol release after chemical castration compared to orchiectomy.
LESTER et al. (1991LESTER, S., et al. Cortisol responses of young lambs to castration and tailing using different methods. New Zealand Veterinary Journal, v.39, n.4, p.134-138, 1991. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/16031640 >. Accessed: Feb. 01, 2018. doi: 10.1080/00480169.1991.35680. https://www.ncbi.nlm.nih.gov/pubmed/1603... )	Surgical castration	O	Cortisol increase up to 4h.
KENT et al. (1993KENT, J. E., et al. Changes in plasma cortisol concentration in lambs of three ages after three methods of castration and tail docking. Research in Veterinary Science, v.55, n.2, p.246-251, 1993. Available from: <Available from: http://www.sciencedirect.com/science/article/pii/003452889390088W >. Accessed: Feb. 01, 2018. doi: 10.1016/0034-5288(93)90088-W. http://www.sciencedirect.com/science/art... )	Surgical castration	O	Cortisol peak of 200nmol/L.
NAKAO et al. (1994NAKAO, T., et al. Plasma cortisol response in dairy cows to vaginoscopy, genital palpation per rectum and artificial insemination. Zentralbl Veterinarmed A, v.41, n.1, p.16-21, 1994. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/8085394 >. Accessed: Feb. 01, 2018. doi: 10.1111/j.1439-0442.1994.tb00060.x. https://www.ncbi.nlm.nih.gov/pubmed/8085... )	Vaginoscopy and rectal palpation	B	Cortisol peak (12ng/ml or 33.1nmol/L) after uterine and ovarian palpation or after AI.
ROBERTSON et al. (1994ROBERTSON, I. S., et al. Effect of different methods of castration on behaviour and plasma cortisol in calves of three ages. Res Vet Sci, v.56, n.1, p.8-17, 1994. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/8146458 >. Accessed: Feb. 01, 2018. doi: 10.1016/0034-5288(94)90189-9. https://www.ncbi.nlm.nih.gov/pubmed/8146... )	Surgical castration	B	Presence of abnormal posture and cortisol concentrations up to 107nmol/L.
LESTER et al. (1996LESTER, S. J., et al. Behavioural and cortisol responses of lambs to castration and tailing using different methods. New Zealand Veterinary Journal, v.44, n.2, p.45-54, 1996. Available from: <Available from: https://doi.org/10.1080/00480169.1996.35933 >. Accessed: Feb. 01, 2018. doi: 10.1080/00480169.1996.35933. https://doi.org/10.1080/00480169.1996.35... )	RR castration	O	Positive correlation between restlessness and cortisol concentrations.
FISHER et al. (2001FISHER, A. D., et al. Effects of surgical or banding castration on stress responses and behaviour of bulls. Aust Vet J, v.79, n.4, p.279-284, 2001. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/11349415 >. Accessed: Feb. 01, 2018. doi: 10.1111/j.1751-0813.2001.tb11981.x. https://www.ncbi.nlm.nih.gov/pubmed/1134... )	Surgical castration	B	Haptoglobin peak (639μg/mL).
HOUDEAU et al. (2002HOUDEAU, E., et al. Plasma levels of cortisol and oxytocin, and uterine activity after cervical artificial insemination in the ewe. Reprod Nutr Dev, v.42, n.4, p.381-392, 2002. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/12510878 >. Accessed: Feb. 01, 2018. doi: 10.1051/rnd:2002033. https://www.ncbi.nlm.nih.gov/pubmed/1251... )	Cervical AI	O	Increased cortisol concentrations after 30min.
CHASTANT-MAILLARD et al. (2003CHASTANT-MAILLARD, S., et al. Consequences of transvaginal follicular puncture on well-being in cows. Reproduction, v.125, n.4, p.555-563, 2003. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/12683926 >. Accessed: Feb. 01, 2018. doi: 10.1530/rep.0.1250555. https://www.ncbi.nlm.nih.gov/pubmed/1268... )	Follicular aspiration	B	Cortisol concentrations and leucogram values did not differ between cows submitted to OPU and control cows.
STAFFORD et al. (2006STAFFORD, K. J., et al. Stress caused by laparoscopy in sheep and its alleviation. New Zealand Veterinary Journal , v.54, n.3, p.109-113, 2006. Available from: <Available from: https://doi.org/10.1080/00480169.2006.36621 >. Accessed: Feb. 01, 2018. doi: 10.1080/00480169.2006.36621. https://doi.org/10.1080/00480169.2006.36... )	Laparoscopy	O	Detomidine inhibited cortisol increase compared to ewes sedated with acepromazin.
PANG et al. (2006PANG, W. Y., et al. Effect of carprofen administration during banding or burdizzo castration of bulls on plasma cortisol, in vitro interferon-gamma production, acute-phase proteins, feed intake, and growth. J Anim Sci, v.84, n.2, p.351-359, 2006. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/16424263 >. Accessed: Feb. 01, 2018. doi: 10.2527/2006.842351x. https://www.ncbi.nlm.nih.gov/pubmed/1642... )	RR castration	B	Increase in haptoglobin concentrations three days after procedure.
MELCHES et al. (2007MELCHES, S., et al. Castration of lambs: A welfare comparison of different castration techniques in lambs over 10 weeks of age. The Veterinary Journal, v.173, n.3, p.554-563, 2007. Available from: <Available from: http://www.sciencedirect.com/science/article/pii/S1090023306000165 >. Accessed: Feb. 01, 2018. doi: 10.1016/j.tvjl.2006.01.006. http://www.sciencedirect.com/science/art... )	RR castration	O	Surgical castration induced higher cortisol concentrations compared to RR and emasculator. RR castration induces response to local palpation for up to 30 days.
PETYIM et al. (2007PETYIM, S., et al. Ovum Pick up in Dairy Heifers: Does it Affect Animal Well being? Reproduction in domestic animals, v.42, n.6, p.623-632, 2007. Available from: <Available from: https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1439-0531.2006.00833.x >. Accessed: Feb. 01, 2018. doi: 10.1111/j.1439-0531.2006.00833.x. https://onlinelibrary.wiley.com/doi/abs/... )	Follicular aspiration	B	Increase in cortisol concentrations up to 46nmol/L.
ORIHUELA et al., (2009ORIHUELA, A., et al. Breaking down the effect of electro-ejaculation on the serum cortisol response, heart and respiratory rates in hair sheep (Ovis aries). Journal of Animal and Veterinary Advances, v.8, n.10, p.1968-1972, 2009. Available from: <Available from: http://medwelljournals.com/abstract/?doi=javaa.2009.1968.1972 >. Accessed: Feb. 01, 2018. http://medwelljournals.com/abstract/?doi... )	Electroejaculation	O	The increase in cortisol concentrations and cardiac rate are consequences of electric stimulus.
GONZÁLEZ et al. (2010GONZÁLEZ, L. A., et al. Pain mitigation after band castration of beef calves and its effects on performance, behavior, Escherichia coli, and salivary cortisol. J Anim Sci, v.88, n.2, p.802-810, 2010. Available from: <Available from: http://dx.doi.org/10.2527/jas.2008-1752 >. Accessed: Feb. 01, 2018. doi: 10.2527/jas.2008-1752. http://dx.doi.org/10.2527/jas.2008-1752... )	EB castration	B	Epidural xylazine and intravenous flunixin inhibit salivary cortisol increase. Chronic pain was not accompanied by changes in cortisol concentrations.
LONG et al. (2011LONG, S. T., et al. Plasma cortisol concentrations after CIDR insertion in beef cows. Reprod Domest Anim, v.46, n.1, p.181-184, 2011. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/20403126 >. Accessed: Feb. 01, 2018. doi: 10.1111/j.1439-0531.2010.01611.x. https://www.ncbi.nlm.nih.gov/pubmed/2040... )	TAI	B	Cortisol increases (8.8ng/mL or 24.3nmol/L) after intravaginal device insertion.
DAMIÁN & UNGERFELD (2011)	Electroejaculation	O	Cortisol peak (2.5μg/dL or 69nmol/L), increased TPP (up to 6.3g/dL) and vocalizations.
WHITLOCK et al. (2012WHITLOCK, B. K., et al. Electroejaculation increased vocalization and plasma concentrations of cortisol and progesterone, but not substance P, in beef bulls. Theriogenology, v.78, n.4, p.737-746, 2012. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/22537995 >. Accessed: Feb. 01, 2018. doi: 10.1016/j.theriogenology.2012.03.020. https://www.ncbi.nlm.nih.gov/pubmed/2253... )	Electroejaculation	B	Cortisol peak (above 100nmol/L) and vocalizations.
MARTI et al. (2015MARTI, S., et al. Effect of anti-gonadotropin-releasing factor vaccine and band castration on indicators of welfare in beef cattle. J Anim Sci, v.93, n.4, p.1581-1591, 2015. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/26020180 >. Accessed: Feb. 01, 2018. doi: 10.2527/jas.2014-8346. https://www.ncbi.nlm.nih.gov/pubmed/2602... )	Immunocastration or EB	B	Increase in salivary cortisol concentrations up to 60 and 120min after anti-GnRH vaccination and EB castration, respectively.
UNGERFELD et al. (2015UNGERFELD, R., et al. Physiological responses and characteristics of sperm collected after electroejaculation or transrectal ultrasound-guided massage of the accessory sex glands in anesthetized mouflons (Ovis musimon) and Iberian ibexes (Capra pyrenaica). Theriogenology, v.84, n.7, p.1067-1074, 2015. Available from: <Available from: http://www.sciencedirect.com/science/article/pii/S0093691X15003143 >. Accessed: Feb. 01, 2018. doi: 10.1016/j.theriogenology.2015.06.009. http://www.sciencedirect.com/science/art... )	Electroejaculation	O	Increase in cortisol concentrations after electroejaculation compared to accessory glands massage.
MELÉNDEZ et al. (2017MELÉNDEZ, D. M., et al. Effect of band and knife castration of beef calves on welfare indicators of pain at three relevant industry ages: I. Acute pain1. J Anim Sci, v.95, n.10, p.4352-4366, 2017. Available from: <Available from: http://dx.doi.org/10.2527/jas2017.1762 >. Accessed: Feb. 01, 2018. doi: 10.2527/jas2017.1762. http://dx.doi.org/10.2527/jas2017.1762... )	Surgical castration or EB	B	Increase in cortisol concentrations for 120min after surgical or EB castration.
OLIVEIRA et al. (2017OLIVEIRA, F. C., et al. Chemical castration in cattle with intratesticular injection of sodium chloride: Effects on stress and inflammatory markers. Theriogenology, v.90, p.114-119, 2017. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/28166957 >. Accessed: Feb. 01, 2018. doi: 10.1016/j.theriogenology.2016.12.001. https://www.ncbi.nlm.nih.gov/pubmed/2816... )	Surgical castration	B	Increase in cortisol concentrations for 60min and increase in scrotal temperature.
OLIVEIRA et al. (2017OLIVEIRA, F. C., et al. Chemical castration in cattle with intratesticular injection of sodium chloride: Effects on stress and inflammatory markers. Theriogenology, v.90, p.114-119, 2017. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/28166957 >. Accessed: Feb. 01, 2018. doi: 10.1016/j.theriogenology.2016.12.001. https://www.ncbi.nlm.nih.gov/pubmed/2816... )	Chemical castration	B	Cortisol peak (1.8±0.2µg/dL or 5nmol/L) only after 30min.
OLIVEIRA et al. (2018OLIVEIRA, F., et al. Inflammatory markers in ewes submitted to surgical or transcervical embryo collection. Small Ruminant Research, v.158, p.15-18, 2018. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S0921448817303085 >. Accessed: Jul. 01, 2018. doi: 10.1016/j.smallrumres.2017.11.012. https://www.sciencedirect.com/science/ar... )	ET	O	Increase in haptoglobin concentrations from three to six days and TPP nine days after procedures.
KASIMANICKAM et al. (2018KASIMANICKAM, R. K., et al. Flunixin meglumine improves pregnancy rate in embryo recipient beef cows with an excitable temperament. Theriogenology, v.107, p.70-77, 2018. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/29132037 >. Accessed: Jul. 01, 2018. doi: 10.1016/j.theriogenology.2017.10.043. https://www.ncbi.nlm.nih.gov/pubmed/2913... )	ET	B	Positive correlation between cortisol and substance P concentrations in embryo recipient cows.

Sp: species; AI: artificial insemination; O: ovine; B: bovine; RR: rubber ring; OPU: ovum-pick up; EB: elastic band; TAI: timed AI; ET: embryo transfer; TPP: total plasma protein.

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[1] E-mail: bggasperin@gmail.com. ^*Corresponding author.