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).
[en] Developing the zoos' ability to assess the reproductive status of the individuals they house is essential to improve the husbandry and management of these species. The use of non-invasive techniques such as fecal hormone analysis has been proven to be a simple and effective way to achieve this. Designed by bioMérieux, mini VIDAS® instrument is used in human and veterinary medicine to evaluate different endocrinological parameters, including serum or plasma progesterone. This study evaluates VIDAS® Progesterone (PRG) assay's efficacy to monitor fecal progestagens using a simple sample extraction protocol adapted to the zoo environment. We compared (1) VIDAS® PRG fecal profiles with established assays specifically designed for fecal progestagens analysis at the VetmedUni (Vienna, Austria) for okapis (Okapia johnstoni), greater one-horned rhinoceros (Rhinoceros unicornis), giraffes (Giraffa camelopardalis reticulata) and hippopotamus (Hippopotamus amphibius) (2) VIDAS® PRG fecal profiles with VIDAS® PRG serum profiles for African elephants (Loxodonta Africana), giant anteater (Myrmecophaga tridactyla) and white rhinoceros (Ceratotherium simum). Spearman mean correlations were: 0.6748 for African elephants (n = 2 animals), 0.7969 for giant anteater (n = 1 animal), 0.7926 for okapis (n = 2 animals), 0.6072 for greater one-horned rhinoceros (n = 4 animals), 0.6062 for giraffes (n = 4 animals) and 0.5740 for hippopotamus (n = 2 animals). Fecal progestagens analysis revealed estrous cycles in several species: 12.5 ± 0.5 weeks for African elephants (n = 2 cycles), 15.3 ± 1.1 days for okapis (n = 6 cycles), 44 ± 2.1 days for greater one-horned rhinoceros (n = 4 cycles) and 15.5 ± 0.5 days for giraffes (n = 4 cycles). We observed pregnancies in a giant anteater, an okapi and a hippopotamus. We observed a strong positive Spearman correlation (r > 0.60) for individuals exhibiting estrous cycles. These first results indicate that the mini VIDAS® can be used for monitoring of the reproductive status of non-domesticated species and can be a useful tool for the reproductive management through fecal progesterone analysis. A simple extraction protocol was suitable for sample preparation of fecal progesterone metabolite analysis. Further studies using a larger number of individuals per species at different reproductive stages could confirm the relevance of mini VIDAS® in the zoo community.
Disciplines :
Zoology
Author, co-author :
Meunier, Maxime ; Zooparc de Beauval & Beauval Nature, 41110, Saint-Aignan, France, UMR Physiologie de la Reproduction et des Comportements, INRAE, CNRS, IFCE, Université de Tours, 37380, Nouzilly, France. Electronic address: maxime.meunier18@outlook.com
Schwarzenberger, Franz; University of Veterinary Medicine, Department of Biomedical Sciences, Physiology - Endocrinology, Veterinärplatz 1, 1210, Vienna, Austria
Mulot, Baptiste ; Zooparc de Beauval & Beauval Nature, 41110, Saint-Aignan, France
Language :
English
Title :
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).
This work was supported by the Beauval Nature association . We want to thank the ZooParc de Beauval's veterinary service and the animal keepers for blood sampling and fecal sample collection. We also thank BioMérieux for supplying the VIDAS® Progesterone (PRG) assay kits (7 boxes of 60 tests were offered). The mini VIDAS® used in this study was in the possession of the zoo. Finally, we thank the endocrine laboratory of the Vetmeduni Vienna, Austria (Unit of Physiology, Pathophysiology and Experimental Endocrinology) for its participation in the project.This work was supported by the Beauval Nature association. We want to thank the ZooParc de Beauval's veterinary service and the animal keepers for blood sampling and fecal sample collection. We also thank BioM?rieux for supplying the VIDAS? Progesterone (PRG) assay kits (7 boxes of 60 tests were offered). The mini VIDAS? used in this study was in the possession of the zoo. Finally, we thank the endocrine laboratory of the Vetmeduni Vienna, Austria (Unit of Physiology, Pathophysiology and Experimental Endocrinology) for its participation in the project.
Schwarzenberger, F., Möstl, E., Palme, R., Bamberg, E., Faecal steroid analysis for non-invasive monitoring of reproductive status in farm, wild and zoo animals. Anim Reprod Sci 42 (1996), 515–526, 10.1016/0378-4320(96)01561-8.
Schwarzenberger, F., Brown, J.L., Hormone monitoring: an important tool for the breeding management of wildlife species. Wien Tierarztl Monatsschr 100 (2013), 209–225.
Brown, J.L., Comparative ovarian function and reproductive monitoring of endangered mammals. Theriogenology 109 (2018), 2–13, 10.1016/j.theriogenology.2017.12.004.
Hodges, J.K., Brown, J.L., Heistermann, M., Endocrine monitoring of reproduction and stress. Wild Mamm Captiv Princ Tech Zoo Manag, 2010, 447–467.
Peter, I.D., Haron, A.W., Jesse, F.F.A., Ajat, M., Han, M.H.W., Fitri, W.N., et al. Opportunities and challenges associated with fecal progesterone metabolite analysis. Vet World 11 (2018), 1466–1472, 10.14202/vetworld.2018.1466-1472.
Schwarzenberger, F., Palme, R., Bamberg, E., Möstl, E., A review of faecal progesterone metabolite analysis for non-invasive monitoring of reproductive function in mammals. Int J Mamm Biol 62 (1997), 214–221.
Graham, L., Schwarzenberger, F., Möstl, E., Galama, W., Savage, A., A versatile enzyme immunoassay for the determination of progestogens in feces and serum. Zoo Biol 20 (2001), 227–236, 10.1002/zoo.1022.
Anckaert, E., Mees, M., Schiettecatte, J., Smitz, J., Clinical validation of a fully automated 17β-estradiol and progesterone assay (VIDAS®) for use in monitoring assisted reproduction treatment. Clin Chem Lab Med, 40, 2002, 10.1515/CCLM.2002.143.
Merkl, M., Ulbrich, S.E., Otzdorff, C., Herbach, N., Wanke, R., Wolf, E., et al. Microarray analysis of equine endometrium at days 8 and 12 of Pregnancy1. Biol Reprod 83 (2010), 874–886, 10.1095/biolreprod.110.085233.
Brugger, N., Otzdorff, C., Walter, B., Hoffmann, B., Braun, J., Quantitative determination of progesterone (P4) in canine blood serum using an enzyme-linked fluorescence assay. Reprod Domest Anim 46 (2011), 870–873, 10.1111/j.1439-0531.2011.01757.x.
Schwarzenberger, F., Patzl, M., Francke, R., Ochs, A., Buiter, R., Schaftenaar, W., et al. Fecal progestagen evaluations to monitor the estrous cycle and pregnancy in the okapi (Okapia johnstoni). Zoo Biol 12 (1993), 549–559, 10.1002/zoo.1430120606.
Schwarzenberger, F., Rietschel, W., Matern, B., Schaftenaar, W., Bircher, P., Van Puijenbroeck, B., et al. Noninvasive reproductive monitoring in the okapi (Okapia johnstoni). J Zoo Wildl Med 30 (1999), 497–503.
Schwarzenberger, F., Rietschel, W., Vahala, J., Holeckova, D., Thomas, P., Maltzan, J., et al. Fecal progesterone, estrogen, and androgen metabolites for noninvasive monitoring of reproductive function in the female Indian rhinoceros, rhinoceros unicornis. Gen Comp Endocrinol 119 (2000), 300–307, 10.1006/gcen.2000.7523.
Palme, R., Touma, C., Arias, N., Dominchin, M.F., Lepschy, M., Steroid extraction: get the best out of faecal samples. Wiener Tierärztliche Monatsschrift Spec Iss 100 (2013), 238–246.
Brown, J.L., Bellem, A.C., Fouraker, M., Wildt, D.E., Roth, T.L., Comparative analysis of gonadal and adrenal activity in the black and white rhinoceros in North America by noninvasive endocrine monitoring. Zoo Biol 20 (2001), 463–486, 10.1002/zoo.10028.
Hildebrandt, T.B., Lueders, I., Hermes, R., Goeritz, F., Saragusty, J., Reproductive cycle of the elephant. Anim Reprod Sci 124 (2011), 176–183, 10.1016/j.anireprosci.2010.08.027.
Brown, J.L., Comparative reproductive biology of elephants. Holt, W.V., Brown, J.L., Comizzoli, P., (eds.) Reprod. Sci. Anim. Conserv., vol. 753, 2014, Springer New York, New York, NY, 135–169, 10.1007/978-1-4939-0820-2_8.
Schwarzenberger, F., Walzer, C., Tomasova, K., Vahala, J., Meister, J., Goodrowe, K.L., et al. Faecal progesterone metabolite analysis for non-invasive monitoring of reproductive function in the white rhinoceros (Ceratotherium simum). Anim Reprod Sci 53 (1998), 173–190, 10.1016/S0378-4320(98)00112-2.
Stoops, M.A., Pairan, R.D., Roth, T.L., Follicular, endocrine and behavioural dynamics of the Indian rhinoceros (Rhinoceros unicornis) oestrous cycle. Reproduction 128 (2004), 843–856, 10.1530/rep.1.00328.
Bercovitch, F.B., Bashaw, M.J., del Castillo, S.M., Sociosexual behavior, male mating tactics, and the reproductive cycle of giraffe Giraffa camelopardalis. Horm Behav 50 (2006), 314–321, 10.1016/j.yhbeh.2006.04.004.
Lueders, I., Hildebrandt, T.B., Pootoolal, J., Rich, P., Gray, C.S., Niemuller, C.A., Ovarian ultrasonography correlated with fecal progestins and estradiol during the estrous cycle and early pregnancy in giraffes (giraffa camelopardalis rothschildi)1. Biol Reprod 81 (2009), 989–995, 10.1095/biolreprod.109.077743.
Kusuda, S., Morikaku, K., Kawada, K., Ishiwada, K., Doi, O., Excretion patterns of fecal progestagens, androgen and estrogens during pregnancy, parturition and postpartum in okapi (Okapia johnstoni). J Reprod Dev 53 (2007), 143–150, 10.1262/jrd.18041.
Patzl, M., Schwarzenberger, F., Osmann, C., Bamberg, E., Bartmann, W., Monitoring ovarian cycle and pregnancy in the giant anteater (Myrmecophaga tridactyla) by faecal progestagen and oestrogen analysis. Anim Reprod Sci 53 (1998), 209–219, 10.1016/S0378-4320(98)00114-6.
Palme, R., Non-invasive measurement of glucocorticoids: advances and problems. Physiol Behav 199 (2019), 229–243, 10.1016/j.physbeh.2018.11.021.
Ghosal, R., Sukumar, R., Seshagiri, P.B., Prediction of estrus cyclicity in Asian elephants (Elephas maximus) through estimation of fecal progesterone metabolite: development of an enzyme-linked immuno-sorbent assay. Theriogenology 73 (2010), 1051–1060, 10.1016/j.theriogenology.2010.01.004.
Schwarzenberger, F., Tomášová, K., Holečková, D., Matern, B., Möstl, E., Measurement of fecal steroids in the black rhinoceros (Diceros bicornis) using group-specific enzyme immunoassays for 20-oxo-pregnanes. Zoo Biol 15 (1996), 159–171, 10.1002/(SICI)1098-2361(1996)15:2<159::AID-ZOO6>3.0.CO;2-A.
del Castillo, S.M., Bashaw, M.J., Patton, M.L., Rieches, R.R., Bercovitch, F.B., Fecal steroid analysis of female giraffe (Giraffa camelopardalis) reproductive condition and the impact of endocrine status on daily time budgets. Gen Comp Endocrinol 141 (2005), 271–281, 10.1016/j.ygcen.2005.01.011.
Dumonceaux, G.A., Bauman, J.E., Camilo, G.R., Evaluation of progesterone levels in feces of captive reticulated giraffe (Giraffa camelopardalis reticulata). J Zoo Wildl Med 37 (2006), 255–261, 10.1638/04-081.1.
Houwald, F von, Pagan, O., Rieches, R., International studbook for the greater one-horned or Indian rhinoceros, Rhinoceros unicornis. 2019, Basel Zoo, Basel.
Graham, L.H., Reid, K., Webster, T., Richards, M., Joseph, S., Endocrine patterns associated with reproduction in the Nile hippopotamus (Hippopotamus amphibius) as assessed by fecal progestagen analysis. Gen Comp Endocrinol 128 (2002), 74–81, 10.1016/S0016-6480(02)00066-7.
Fieß, M., Heistermann, M., Hodges, J.K., Patterns of urinary and fecal steroid excretion during the ovarian cycle and pregnancy in the African elephant (Loxodonta africana). Gen Comp Endocrinol 115 (1999), 76–89, 10.1006/gcen.1999.7287.
Wasser, S.K., Papageorge, S., Foley, C., Brown, J.L., Excretory fate of estradiol and progesterone in the African elephant (Loxodonta africana) and patterns of fecal steroid concentrations throughout the estrous cycle. Gen Comp Endocrinol 102 (1996), 255–262, 10.1006/gcen.1996.0067.
Schwarzenberger, F., Strauss, G., Hoppen, H.-O., Schaftenaar, W., Dieleman, S.J., Zenker, W., et al. Evaluation of progesterone and 20-oxo-progestagens in the plasma of Asian (Elephas maximus) and African (Loxodonta africana) elephants. Zoo Biol 16 (1997), 403–413, 10.1002/(SICI)1098-2361(1997)16:5<403::AID-ZOO3>3.0.CO;2-E.
Patton, M.L., Swaisgood, R.R., Czekala, N.M., White, A.M., Fetter, G.A., Montagne, J.P., et al. Reproductive cycle length and pregnancy in the southern white rhinoceros (Ceratotherium simum simum) as determined by fecal pregnane analysis and observations of mating behavior. Zoo Biol 18 (1999), 111–127, 10.1002/(SICI)1098-2361(1999)18:2<111::AID-ZOO3>3.0.CO;2-0.
Radcliffe, R.W., Czekala, N.M., Osofsky, S.A., Combined serial ultrasonography and fecal progestin analysis for reproductive evaluation of the female white rhinoceros (Ceratotherium simum simum): preliminary results. Zoo Biol 16 (1997), 445–456, 10.1002/(SICI)1098-2361(1997)16:5<445::AID-ZOO7>3.0.CO;2-A.
