Analysis of progesterone and estrone-sulfate in feces of American Bison using liquid chromatography coupled to mass spectrometry: Technical validation and correlation with blood levels
[en] American Bison’s wild nature limits blood sample availability to study its endocrinology. This report describes progesterone (P4) and estrone-sulfate (E1S) assays in American Bison feces using Liquid Chromatography coupled with Mass Spectrometry (LC-MS). In 2 ranches, samples of feces (n = 73) and serum (n = 93) were collected in pregnant and nonpreg- nant American Bison. Feces samples (250 mg) were extracted with methanol, purified, and concentrated. Then, feces and serum samples were assayed using LC-MS, according to our previously described technique. Fecal matrix homogeneity was determined by measuring steroids in different areas of the sample and concentration evolutions were evaluated after storage at room temperature. During the validation process, lower limits of quantification were 20 pg/g (E1S) and 4 ng/g (P4) by meeting the following criteria: relative standard de- viation <15% and relative bias <15%. By measuring hormones in different spots from the same sample, a moderate variability for E1S (coefficient of variation [CV] up to 21.3%) and a high variability for P4 (CV up to 85.5%) were highlighted. Correlation between concen- trations in feces and in serum was higher for E1S (r = 0.77) than for P4 (r = 0.65) and P4 could be assayed in pregnant and nonpregnant animals whereas E1S was only present in pregnant. Feces storage at room temperature induced modification of steroid concen- trations. The quantification of E1S and, at a lower level, of P4 in feces is an interesting alternative to serum assay to describe the pregnancy-related evolution of these steroids in American Bisons, with feces ideally stored frozen and mixed before the LC-MS procedures.
Dufour, Patrice ; Centre Hospitalier Universitaire de Liège - CHU > > Service de toxicologie clinique, médicolégale, environnementale et en entreprise
Frisee, Vincent ; Université de Liège - ULiège > Département d'Enseignement et de Clinique des animaux de Production (DCP)
Rigaux, Goulven; Pan Anima, Tournai
Brutinel, Flore ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Médecine vétérinaire comparée
Egyptien, Sophie ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH)
Bossaert, Philippe ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Productions animales durables
DELEERSNYDER, Jessica ; Centre Hospitalier Universitaire de Liège - CHU > > Service de chimie clinique
Deleuze, Stefan ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Médecine vétérinaire comparée
Peeters, Stéphanie ; Centre Hospitalier Universitaire de Liège - CHU > > Service de chimie clinique
Le Goff, Caroline ; Centre Hospitalier Universitaire de Liège - CHU > > Service de chimie clinique
Ponthier, Jérôme ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Médecine vétérinaire comparée
Cavalier, Etienne ; Centre Hospitalier Universitaire de Liège - CHU > > Service de chimie clinique
Language :
English
Title :
Analysis of progesterone and estrone-sulfate in feces of American Bison using liquid chromatography coupled to mass spectrometry: Technical validation and correlation with blood levels
Kirkpatrick, J.F., Kincy, V., Bancroft, K., Shideler, S.E., Lasley, B.L., Oestrous cycle of the North American bison (Bison bison) characterized by urinary pregnanediol-3-glucuronide. J Reprod Fertil 93 (1991), 541–547, 10.1530/jrf.0.0930541.
Matsuda, D.M., Bellem, A.C., Gartley, C.J., Madison, V., King, W.A., Liptrap, R.M., Goodrowe, K.L., Endocrine and behavioral events of estrous cyclicity and synchronization in wood bison (Bison bison athabascae). Theriogenology 45 (1996), 1429–1441, 10.1016/0093-691X(96)85667-6.
Cervantes, MP, Palomino, JM, Anzar, M, Mapletoft, RJ, Adams, GP, In vivo and in vitro maturation of oocytes collected from superstimulated wood bison (Bison bison athabascae) during the anovulatory and ovulatory seasons. Anim Reprod Sci 173 (2016), 87–96, 10.1016/j.anireprosci.2016.09.001.
Kirkpatrick, J.F., Bancroft, K., Kincy, V., Pregnancy and ovulation detection in bison (Bison Bison) assessed by means of urinary and fecal steroids. J Wildl Dis 28 (1992), 590–597, 10.7589/0090-3558-28.4.590.
Love, D.M., Mefford, M.T., Ramer, J.C., Validation of the BioPRYN enzyme-linked immunosorbent assay for detection of pregnancy-specific protein-B (PSPB) and diagnosis of pregnancy in American bison (Bison bison). Reprod Domest Anim 52 (2017), 791–797, 10.1111/rda.12980.
Vervaecke, H., Schwarzenberger, F., Endocrine and behavioral observations during transition of non-breeding into breeding season in female American bison (Bison bison). Theriogenology 66 (2006), 1107–1114, 10.1016/j.theriogenology.2006.03.005.
Frisée, V., Rigaux, G., Dufour, P., Barbato, O., Brutinel, F., Egyptien, S., Bossaert, P., Deleuze, S., Cavalier, E., Ponthier, J., American Bison (Bison Bison) reproductive endocrinology: serum pregnancy associated glycoproteins (PAG), progesterone, estrone and estrone-sulfate in non pregnant animals and during gestation. Domest Anim Endocrinol, 78, 2022, 106684, 10.1016/j.domaniend.2021.106684.
Kiewisz, J., Sousa, N.M.de, Beckers, J.-F., Vervaecke, H., Panasiewicz, G., Szafranska, B., Isolation of pregnancy-associated glycoproteins from placenta of the American Bison (Bison Bison) at first half of pregnancy. Gen Comp Endocrinol 155 (2008), 164–175, 10.1016/j.ygcen.2007.04.011.
Dufour, P., Courtois, J., Seynaeve, Y., Peeters, S., Le Goff, C., Cavalier, E., Ponthier, J., Development and validation of a liquid chromatography coupled to mass spectrometer (LC-MS) method for the simultaneous quantification of estrone-3-sulfate, progesterone, estrone and estradiol in serum of mares and American Bisons. Res Vet Sci 136 (2021), 343–350, 10.1016/j.rvsc.2021.03.014.
Isobe, N., Nakao, T., Uehara, O., Yamashiro, H., Kubota, H., Plasma concentration of estrone sulfate during pregnancy in different breeds of Japanese beef cattle. J Reprod Dev 49 (2003), 369–374, 10.1262/jrd.49.369.
Whitlock, B.K., Coffman, E.A., Coetzee, J.F., Daniel, J.A., Electroejaculation increased vocalization and plasma concentrations of cortisol and progesterone, but not substance P, in beef bulls. Theriogenology 78 (2012), 737–746, 10.1016/j.theriogenology.2012.03.020.
Othen, L.S., Bellem, A.C., Gartley, C.J., Auckland, K., King, W.A., Liptrap, R.M., Goodrowe, K.L., Hormonal control of estrous cyclicity and attempted superovulation in wood bison (Bison bison athabascae). Theriogenology 52 (1999), 313–323, 10.1016/S0093-691X(99)00131-4.
Raeside, J.I., A brief account of the discovery of the fetal/placental unit for estrogen production in equine and human pregnancies: relation to human medicine. Yale J Biol Med 90 (2017), 449–461.
Möstl, E., Choi, H.S., Wurm, W., Ismail, N., Bamberg, E., Pregnancy diagnosis in cows and heifers by determination of oestradiol-17α in faeces. Br Vet J 140 (1984), 287–291, 10.1016/0007-1935(84)90115-5.
Choi, H.S., Kiesenhofer, E., Gantner, H., Hois, J., Bamberg, E., Pregnancy diagnosis in sows by estimation of estrogens in blood, urine or feces. Anim Reprod Sci 15 (1987), 209–216, 10.1016/0378-4320(87)90043-1.
Ohtaki, T., Moriyoshi, M., Nakada, K., Nakao, T., Fecal estrone sulfate profile in sows during gestation. J Vet Med Sci 61 (1999), 661–665, 10.1292/jvms.61.661.
Safar-Hermann, N., Ismail, M.N., Choi, H.S., Möstl, E., Bamberg, E., Pregnancy diagnosis in zoo animals by estrogen determination in feces. Zoo Biology 6 (1987), 189–193, 10.1002/zoo.1430060209.
Chapeau, C., King, G.J., Bamberg, E., Fecal estrogens in one primate and several ungulate species during various reproductive stages. Anim Reprod Sci 34 (1993), 167–175, 10.1016/0378-4320(93)90075-3.
Ncube, H., Duncan, P., Grange, S., Cameron, E.Z., Barnier, F., Ganswindt, A., Pattern of fecal 20-oxopregnane and estrogen concentrations during pregnancy in wild plains zebra mares. Gen Comp Endocrinol 172 (2011), 358–362, 10.1016/j.ygcen.2011.03.027.
Kuckelkorn, B., Assessment of pregnancy in Kiang mares (Equushemionusholdereri) using estrogen determination in feces. Theriogenology 42 (1994), 37–42, 10.1016/0093-691X(94)90660-B.
Kapke, C.A., Arcese, P., Ziegler, T.E., Scheffler, G.R., Estradiol and progesterone metabolite concentration in white-tailed deer (Odocoileus virginianus) feces. J Zoo Wildl Med 30 (1999), 361–371.
Messier, F., Desaulniers, D.M., Goff, A.K., Nault, R., Patenaude, R., Crete, M., Caribou pregnancy diagnosis from immunoreactive progestins and estrogens excreted in feces. J Wildl Manag 54 (1990), 279–283, 10.2307/3809042.
Schoenecker, K.A., Lyda, R.O., Kirkpatrick, J., Comparison of three fecal steroid metabolites for pregnancy detection used with single sampling in bighorn sheep (Ovis canadensis). J Wildl Dis 40 (2004), 273–281, 10.7589/0090-3558-40.2.273.
Meunier, M., Schwarzenberger, F., Mulot, B., Use of a simplified non-invasive technic to monitor fecal progesterone metabolites and reproduction function in several zoo species: Efficacy of mini VIDAS® automate (bioMérieux). Theriogenology 179 (2022), 69–77, 10.1016/j.theriogenology.2021.11.015.
Tanaka, Y., Sandoval, E.D.P., Duarte, J.M.B., Non-homogeneous distribution of steroids in fecal pellets: an example in brown brocket deer (Mazama gouazoubira) with progesterone metabolites. Gen Comparat Endocrinol, 282, 2019, 113206, 10.1016/j.ygcen.2019.06.010.
Wang, P., Chen, Q., Yuan, P., Lin, S., Chen, H., Li, R., Zhang, X., Zhuo, Y., Li, J., Che, L., Feng, B., Lin, Y., Xu, S., Wu, D., Fang, Z., Gut microbiota involved in desulfation of sulfated progesterone metabolites: A potential regulation pathway of maternal bile acid homeostasis during pregnancy. Front Microbiol, 13, 2022, 1023623.
Adlercreutz, H., Pulkkinen, M.O., Hämäläinen, E.K., Korpela, J.T., Studies on the role of intestinal bacteria in metabolism of synthetic and natural steroid hormones. J Steroid Biochem 20 (1984), 217–229, 10.1016/0022-4731(84)90208-5.
Wang, P.-H., Chen, Y.-L., Wei, S.T.-S., Wu, K., Lee, T.-H., Wu, T.-Y., Chiang, Y.-R., Retroconversion of estrogens into androgens by bacteria via a cobalamin-mediated methylation. Proc Natl Acad Sci 117 (2020), 1395–1403, 10.1073/pnas.1914380117.
Cotton, S., Clayton, C.A., Tropini, C., Microbial endocrinology: the mechanisms by which the microbiota influences host sex steroids. Trends Microbiol, 2023, 10.1016/j.tim.2023.03.010 S0966-842X(23)00090–2.
Ramachandran, R., Vinothkumar, A., Sankarganesh, D., Suriyakalaa, U., Aathmanathan, V.S., Kamalakkannan, S., Nithya, V., Angayarkanni, J., Archunan, G., Akbarsha, M.A., Achiraman, S., Detection of estrous biomarkers in the body exudates of Kangayam cattle (Bos indicus) from interplay of hormones and behavioral expressions. Domest Anim Endocrinol, 72, 2020, 106392, 10.1016/j.domaniend.2019.106392.
Ledeck, J., Dufour, P., Evrard, É., Le Goff, C., Peeters, S., Brutinel, F., Egyptien, S., Deleuze, S., Cavalier, É., Ponthier, J., Evolution of 17-β-estradiol, estrone and estrone-sulfate concentrations in late pregnancy of different breeds of mares using liquid chromatography and mass spectrometry. Theriogenology 189 (2022), 86–91, 10.1016/j.theriogenology.2022.06.004.
Peris, S.I., Bilodeau, J.-F., Dufour, M., Bailey, J.L., Impact of cryopreservation and reactive oxygen species on DNA integrity, lipid peroxidation, and functional parameters in ram sperm. Mol Reprod Dev 74 (2007), 878–892, 10.1002/mrd.20686.