Influence of transvaginal ultrasound-guided follicular punctures in the mare on heart rate, respiratory rate, facial expression changes, and salivary cortisol as pain scoring.
[en] Transvaginal ultrasound-guided follicular punctures are widely used in the mare for diagnosis, research, and commercial applications. The objective of our study was to determine their influence on pain, stress, and well-being in the mare, by evaluating heart rate, breath rate, facial expression changes, and salivary cortisol before, during, and after puncture. For this experiment, 21 pony mares were used. Transvaginal ultrasound-guided aspirations were performed on 11 mares. After injections for sedation, analgesia, and antispasmodia, the follicles from both ovaries were aspirated with a needle introduced through the vagina wall into the ovary. In the control group, 10 mares underwent similar treatments and injections, but no follicular aspiration. Along the session, heart rate and breath rate were evaluated by a trained veterinarian, ears position, eyelid closure, and contraction of facial muscles were evaluated, and salivary samples were taken for evaluation of cortisol concentration. A significant relaxation was observed after sedative injection in the punctured and control mares, according to ear position, eyelid closure, and contraction of facial muscles, but no difference between punctured and control animals was recorded. No significant modification of salivary cortisol concentration during puncture and no difference between punctured and control mares at any time were observed. No significant modification of the breath rate was observed along the procedure for the punctured and the control mares. Heart rate increased significantly but transiently when the needle was introduced in the ovary and was significantly higher at that time for the punctured mares than that for control mares. None of the other investigated parameters were affected at that time, suggesting discomfort is minimal and transient. Improving analgesia, e.g., through a multimodal approach, during that possibly more sensitive step could be recommended. The evaluation of facial expression changes and heart rate is easy-to-use and accurate tools to evaluate pain and well-being of the mare.
Deleuze, Stefan ; Université de Liège > Dép. clinique des animaux de compagnie et des équidés (DCA) > Obstét. et path. de la reprod. des anim. de comp. et équidés
Goudet, Ghylene
Language :
English
Title :
Influence of transvaginal ultrasound-guided follicular punctures in the mare on heart rate, respiratory rate, facial expression changes, and salivary cortisol as pain scoring.
Publication date :
2016
Journal title :
Theriogenology
ISSN :
0093-691X
eISSN :
1879-3231
Publisher :
Elsevier, New York, United States - New York
Volume :
86
Issue :
7
Pages :
1757-63
Peer reviewed :
Peer Reviewed verified by ORBi
Commentary :
Copyright (c) 2016 Elsevier Inc. All rights reserved.
[1] Dellenbach, P., Nisand, I., Moreau, L., Feger, B., Plumere, C., Gerlinger, P., et al. Transvaginal, sonographically controlled ovarian follicle puncture for egg retrieval. Lancet, 1, 1984, 1467.
[2] Feichtinger, W., Kemeter, P., Transvaginal sector scan sonography for needle guided transvaginal follicle aspiration and other applications in gynecologic routine and research. Fertil Steril 45 (1986), 722–725.
[3] Pieterse, M.C., Kappen, K.A., Kruip, T.A., Taverne, M.A., Aspiration of bovine oocytes during transvaginal ultrasound scanning of the ovaries. Theriogenology 30 (1988), 751–762.
[4] Bruck, I., Raun, K., Synnestvedt, B., Greve, T., Follicle aspiration in the mare using a transvaginal ultrasound-guided technique. Equine Vet J 24 (1992), 58–59.
[5] Duchamp, G., Bézard, J., Palmer, E., Oocyte yield and the consequences of puncture of all follicles larger than 8 millimeters in mares. Biol Reprod Monogr Ser 1 (1995), 233–241.
[6] Kanitz, W., Becker, F., Alm, H., Torner, H., Ultrasound-guided follicular aspiration in mares. Biol Reprod Monogr Ser 1 (1995), 225–231.
[7] Carnevale, E.M., Ginther, O.J., Defective oocytes as a cause of subfertility in old mares. Biol Reprod Monogr Ser 1 (1995), 209–214.
[8] Altermatt, J.L., Suh, T.K., Stokes, J.E., Carnevale, E.M., Effects of age and equine follicle-stimulating hormone (eFSH) on collection and viability of equine oocytes assessed by morphology and developmental competency after intracytoplasmic sperm injection (ICSI). Reprod Fertil Dev 21 (2009), 615–623.
[9] Bézard, J., Goudet, G., Duchamp, G., Palmer, E., Preovulatory maturation of ovarian follicles and oocytes in unstimulated and superovulated mares. Biol Reprod Monogr Ser 1 (1995), 261–271.
[10] Goudet, G., Bézard, J., Duchamp, G., Gérard, N., Palmer, E., Equine oocyte competence for nuclear and cytoplasmic in vitro maturation: effect of follicle size and hormonal environment. Biol Reprod 57 (1997), 232–245.
[11] Goudet, G., Bézard, J., Belin, F., Duchamp, G., Palmer, E., Gérard, N., Oocyte competence for in vitro maturation is associated with histone H1 kinase activity and is influenced by estrous cycle stage in the mare. Biol Reprod 59 (1998), 456–462.
[12] Gérard, N., Duchamp, G., Goudet, G., Bézard, J., Magistrini, M., Palmer, E., A high-molecular-weight preovulatory stage-related protein in equine follicular fluid and granulosa cells. Biol Reprod 58 (1998), 551–557.
[13] Belin, F., Goudet, G., Duchamp, G., Gérard, N., Intrafollicular concentrations of steroids and steroidogenic enzymes in relation to follicular development in the mare. Biol Reprod 62 (2000), 1335–1343.
[14] Martoriati, A., Lalmanach, A.C., Goudet, G., Gérard, N., Expression of interleukin-1 (IL-1) system genes in equine cumulus-oocyte complexes and influence of IL-1beta during in vitro maturation. Biol Reprod 67 (2002), 630–636.
[15] Dell'Aquila, M.E., Caillaud, M., Maritato, F., Martoriati, A., Gérard, N., Aiudi, G., et al. Cumulus expansion, nuclear maturation and connexin 43, cyclooxygenase-2 and FSH receptor mRNA expression in equine cumulus-oocyte complexes cultured in vitro in the presence of FSH and precursors for hyaluronic acid synthesis. Reprod Biol Endocrinol, 2, 2004, 44.
[16] Luciano, A.M., Goudet, G., Perazzoli, F., Lahuec, C., Gérard, N., Glutathione content and glutathione peroxidase expression in in vivo and in vitro matured equine oocytes. Mol Reprod Dev 73 (2006), 658–666.
[17] Deleuze, S., Goudet, G., Caillaud, M., Lahuec, C., Duchamp, G., Efficiency of embryonic development after intrafollicular and intraoviductal transfer of in vitro and in vivo matured horse oocytes. Theriogenology 72 (2009), 203–209.
[18] Franciosi, F., Lodde, V., Goudet, G., Duchamp, G., Deleuze, S., Douet, C., et al. Changes in histone H4 acetylation during in vivo versus in vitro maturation of equine oocytes. Mol Hum Reprod 18 (2012), 243–252.
[19] Accogli, G., Douet, C., Ambruosi, B., Martino, N.A., Uranio, M.F., Deleuze, S., et al. Differential expression and localization of glycosidic residues in in vitro- and in vivo-matured cumulus-oocyte complexes in equine and porcine species. Mol Reprod Dev 81 (2014), 1115–1135.
[20] Jacobson, C.C., Choi, Y.H., Hayden, S.S., Hinrichs, K., Recovery of mare oocytes on a fixed biweekly schedule, and resulting blastocyst formation after intracytoplasmic sperm injection. Theriogenology 73 (2010), 1116–1126.
[21] Mari, G., Merlo, B., Iacono, E., Belluzzi, S., Fertility in the mare after repeated transvaginal ultrasound-guided aspirations. Anim Reprod Sci 88 (2005), 299–308.
[22] Purcell, S.H., Seidel, G.E., McCue, P.M., Squires, E.L., Aspiration of oocytes from transitional, cycling, and pregnant mares. Anim Reprod Sci 100 (2007), 291–300.
[23] Coutinho da Silva, M.A., When should a mare go for assisted reproduction?. Theriogenology 70 (2008), 441–444.
[24] Galli, C., Duchi, R., Colleoni, S., Lagutina, I., Lazzari, G., Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice. Theriogenology 81 (2014), 138–151.
[25] Carnevale, E.M., Squires, E.L., Maclellan, L.J., Alvarenga, M.A., Scott, T.J., Use of oocyte transfer in a commercial breeding program for mares with reproductive abnormalities. J Am Vet Med Assoc 218 (2001), 87–91 37.
[26] Hinrichs, K., Assisted reproduction techniques in the horse. Reprod Fertil Dev 25 (2012), 80–93.
[27] Velez, I.C., Arnold, C., Jacobson, C.C., Norris, J.D., Choi, Y.H., Edwards, J.F., et al. Effects of repeated transvaginal aspiration of immature follicles on mare health and ovarian status. Equine Vet J Suppl, 2012, 78–83.
[28] Bogh, I.B., Brink, P., Jensen, H.E., Lehn-Jensen, H., Greve, T., Ovarian function and morphology in the mare after multiple follicular punctures. Equine Vet J 35 (2003), 575–579.
[29] Vanderwall, D.K., Hyde, K.J., Woods, G.L., Effect of repeated transvaginal ultrasound-guided follicle aspiration on fertility in mares. J Am Vet Med Assoc 228 (2006), 248–250.
[30] Bottoms, G.D., Roesel, O.F., Rausch, F.D., Akins, E.L., Circadian variation in plasma cortisol and corticosterone in pigs and mares. Am J Vet Res 33 (1972), 785–790.
[31] Schmidt, A., Biau, S., Mostl, E., Becker-Birck, M., Morillon, B., Aurich, J., et al. Changes in cortisol release and heart rate variability in sport horses during long-distance road transport. Domest Anim Endocrinol 38 (2010), 179–189.
[32] Schmidt, A., Hodl, S., Mostl, E., Aurich, J., Muller, J., Aurich, C., Cortisol release, heart rate, and heart rate variability in transport-naive horses during repeated road transport. Domest Anim Endocrinol 39 (2010), 205–213.
[33] Peeters, M., Sulon, J., Beckers, J.F., Ledoux, D., Vandenheede, M., Comparison between blood serum and salivary cortisol concentrations in horses using an adrenocorticotropic hormone challenge. Equine Vet J 43 (2011), 487–493.
[34] Bussieres, G., Jacques, C., Lainay, O., Beauchamp, G., Leblond, A., Cadore, J.L., et al. Development of a composite orthopaedic pain scale in horses. Res Vet Sci 85 (2008), 294–306.
[35] Ashley, F.H., Waterman-Pearson, A.E., Whay, H.R., Behavioural assessment of pain in horses and donkeys: application to clinical practice and future studies. Equine Vet J 37 (2005), 565–575.
[36] Grunau, R.V., Craig, K.D., Pain expression in neonates: facial action and cry. Pain 28 (1987), 395–410.
[37] Jordan, A., Hughes, J., Pakresi, M., Hepburn, S., O'Brien, J.T., The utility of PAINAD in assessing pain in a UK population with severe dementia. Int J Geriatr Psychiatry 26 (2011), 118–126.
[38] Langford, D.J., Bailey, A.L., Chanda, M.L., Clarke, S.E., Drummond, T.E., Echols, S., et al. Coding of facial expressions of pain in the laboratory mouse. Nat Meth 7 (2010), 447–449.
[39] Sotocinal, S.G., Sorge, R.E., Zaloum, A., Tuttle, A.H., Martin, L.J., Wieskopf, J.S., et al. The Rat Grimace Scale: a partially automated method for quantifying pain in the laboratory rat via facial expressions. Mol Pain, 7, 2011, 55.
[40] Keating, S.C., Thomas, A.A., Flecknell, P.A., Leach, M.C., Evaluation of EMLA cream for preventing pain during tattooing of rabbits: changes in physiological, behavioural and facial expression responses. PLoS One, 7, 2012, e44437.
[41] Dalla Costa, E., Minero, M., Lebelt, D., Stucke, D., Canali, E., Leach, M.C., Development of the Horse Grimace Scale (HGS) as a pain assessment tool in horses undergoing routine castration. PLoS One, 9, 2014, e92281.
[42] Mugnier, S., Dell'Aquila, M.E., Pelaez, J., Douet, C., Ambruosi, B., De Santis, T., et al. New insights into the mechanisms of fertilization: comparison of the fertilization steps, composition, and structure of the zona pellucida between horses and pigs. Biol Reprod 81 (2009), 856–870.
[43] Carnevale, E.M., Sessions, D.R., In vitro production of equine embryos. J Equine Vet Sci 32 (2012), 367–371.
[44] Alam, M.G., Dobson, H., Effect of various veterinary procedures on plasma concentrations of cortisol, luteinising hormone and prostaglandin F2 alpha metabolite in the cow. Vet Rec 118 (1986), 7–10.
[45] Goudet, G., Leclercq, L., Bézard, J., Duchamp, G., Guillaume, D., Palmer, E., Chorionic gonadotropin secretion is associated with an inhibition of follicular growth and an improvement in oocyte competence for in vitro maturation in the mare. Biol Reprod 58 (1998), 760–768.
[46] Schonbom, H., Kassens, A., Hopster-Iversen, C., Klewitz, J., Piechotta, M., Martinsson, G., et al. Influence of transrectal and transabdominal ultrasound examination on salivary cortisol, heart rate, and heart rate variability in mares. Theriogenology 83 (2015), 749–756.
[47] Driessen, B., Pain: systemic and local/regional drug therapy. Clin Tech Equine Pract 6 (2007), 135–144.
[48] Viñuela-Fernández, I., Jones, E., Chase-Topping, M.E., Price, J., Comparison of subjective scoring systems used to evaluate equine laminitis. Vet J 188 (2011), 171–177.
[49] Graubner, C., Gerber, V., Doherr, M., Spadavecchia, C., Clinical application and reliability of a post abdominal surgery pain assessment scale (PASPAS) in horses. Vet J 188 (2011), 178–183.
[50] Love, E.J., Assessment and management of pain in horses. Equine Vet Educ 21 (2009), 46–48.
[51] Hughes, T., Creighton, E., Coleman, R., Salivary and fecal cortisol as measures of stress in horses. J Vet Behav 5 (2010), 59–60.
[52] Cordero, M., Brorsen, B.W., McFarlane, D., Circadian and circannual rhythms of cortisol, ACTH, and alpha-melanocyte-stimulating hormone in healthy horses. Domest Anim Endocrinol 43 (2012), 317–324.
[53] Bohak, Z., Szabo, F., Beckers, J.F., Melo de Sousa, N., Kutasi, O., Nagy, K., et al. Monitoring the circadian rhythm of serum and salivary cortisol concentrations in the horse. Domest Anim Endocrinol 45 (2013), 38–42.
[54] Satue, K., Domingo, R., Redondo, J.I., Relationship between progesterone, oestrone sulphate and cortisol and the components of renin angiotensin aldosterone system in Spanish purebred broodmares during pregnancy. Theriogenology 76 (2011), 1404–1415.
[55] Aurich, J., Wulf, M., Ille, N., Erber, R., von Lewinski, M., Palme, R., et al. Effects of season, age, sex, and housing on salivary cortisol concentrations in horses. Domest Anim Endocrinol 52 (2015), 11–16.
