Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-05T22:27:23.172Z Has data issue: false hasContentIssue false
  • English
  • Français

Mitotic index and morphological characteristics of ovarian small follicles from goats submitted to nutritionally unbalanced regimens

Published online by Cambridge University Press:  24 August 2017

Davide Rondina ,
Vicente J.F. Freitas ,
Jamily B. Bruno ,
Juliana J.H. Celestino  and
Regiane R. Santos
Davide Rondina*
Affiliation:
Faculdade de Veterinária, Universidade Estadual do Ceará, Av. Silas Munguba, 1700. Campus do Itaperi, 60714–903, Fortaleza, Ceará, Brazil.
Vicente J.F. Freitas
Affiliation:
Faculdade de Veterinária, Universidade Estadual do Ceará, Fortaleza, Ceará, Brazil.
Jamily B. Bruno
Affiliation:
Faculdade de Veterinária, Universidade Estadual do Ceará, Fortaleza, Ceará, Brazil.
Juliana J.H. Celestino
Affiliation:
Institute of Health Sciences, Universidade da Integração Internacional da Lusofonia Afro-Brasileira. Acarape-CE, Brazil.
Regiane R. Santos
Affiliation:
Schothorst Feed Research, Lelystad, The Netherlands.
*
All correspondence to: Davide Rondina. Faculdade de Veterinária, Universidade Estadual do Ceará, Av. Silas Munguba, 1700. Campus do Itaperi, 60714–903, Fortaleza, Ceará, Brazil. Tel: +55 85 31019858. Fax: +55 85 31019840. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The objective of this study was to assess the influence of nutritional regimens such as adequate feeding, restricted feeding, and underfeeding–refeeding on the follicle growth and development from caprine ovaries. Goats were divided into three different groups (n = 5 per group). For 24 weeks, goats received elephant grass plus concentrate to provide 1.5 (n = 5) and 0.72 (n = 10) times the energy requirements for maintenance of live weight. Underfed goats were subsequently refed for 6 weeks with the diet of the nourished group (1.5 times the energetic requirements of maintenance). Follicular morphology and morphometry, as well as granulosa cells mitotic index were assessed. Ovarian follicles were classified as small or large preantral follicles, or as small or large antral follicles. Ovarian volume was smaller in animals from both underfed and refed groups than in those animals from fed group. Although no difference in the total number of normal follicles was observed among the nutritional groups, underfed animals presented higher percentages of atretic preantral and small antral follicles when compared with fed animals. Large antral follicles from underfed and refed goats presented a lower mitotic index when compared with fed ones. In conclusion, ovaries from goats challenged with prolonged undernutrition will be functionally compromised, which is characterized by atresia of preantral and small antral follicles and decreased mitotic index of large antral follicles. Refeeding those animals will not recover ovarian function to a same level experienced by goats fed a diet with adequate energy requirements.

Keywords

MitosisMorphologyOvarySmall ruminantsUndernourishment
Type
Research Article
Information
Zygote , Volume 25 , Issue 5 , October 2017 , pp. 567 - 574
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acero-Camelo, A., Valencia, E., Rodríguez, A. & Randel, P.F. (2008). Effects of flushing with two energy levels on goat reproductive performance. Livest. Res. Rural Dev. 20, 1–8.Google Scholar
Agricultural and Food Research Council (AFRC) (1998). The Nutrition of Goats. An advisory manual prepared by the AFRC technical committee on responses to nutrients. Wallingford, UK: CAB International.Google Scholar
Bentzen, J.K.D., Hansen, H.S. & Nielsen, H.W. (1999). The prognostic importance of volume-weighted mean nuclear volume, mitotic index, and other stereologically measured quantitative parameters in supraglottic laryngeal carcinoma. Cancer 86, 2222–8.Google Scholar
Boland, M.P., Lonergan, P. & O'Callaghan, D. (2001). Effect of nutrition on endocrine parameters, ovarian physiology, and oocyte and embryo development. Theriogenology 55, 1323–40.Google Scholar
Borwick, S.C., Rhind, S.M., McMillen, S.R. & Racey, P.A. (1997). Effect of undernutrition of ewes from the time of mating on fetal development in mid gestation. Reprod. Fert. Dev. 9, 711–5.Google Scholar
Chan, K.A., Bernal, A.B., Vickers, M.H., Gohir, W., Petrik, J.J., et al. (2015). Early life exposure to undernutrition induces ER stress, apoptosis, and reduced vascularization in ovaries of adult rat offspring. Biol. Reprod. 92, 110.Google Scholar
Chilliard, Y., Bocquier, F. & Doreau, M. (1998). Digestive and metabolic adaptations of ruminants to undernutrition and consequences on reproduction. Reprod. Nutr. Dev. 38, 131–52.Google Scholar
De Bruin, J.P., Dorland, M., Bruinse, H.W., Spliet, W., Nikkels, P.G., et al. (1998). Fetal growth retardation as a cause of impaired ovarian development. Early Hum. Dev. 51, 39–46.Google Scholar
Garcia, R., Ballesteros, L.M., Hernandez-Perez, O., Rosales, A.M., Espinosa, R., et al. (1997). Metalloproteinase activity during growth, maturation and atresia in the ovarian follicles of the goat. Anim. Reprod. Sci. 47, 211–28.Google Scholar
Garcia-Garcia, R.M. (2012). Integrative control of energy balance and reproduction in females. ISRN Vet. Sci. 2012, Article ID 121389.Google Scholar
Gundersen, H.J.G., Bendtsen, T.F., Korbo, L., Marcussen, N., Moller, A., et al. (1988). Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96, 379–94.Google Scholar
Hooper, C.E.S. (1961). Use of colchicine for the measurement of mitotic rate in the intestinal epithelium. Am. J. Anat. 108, 231–44.Google Scholar
Kusina, N.T., Chinuwo, T., Hamudikuwanda, H., Ndlovu, L.R. & Muzanenhamo, S. (2001). Effect of different dietary energy level intakes on efficiency of estrus synchronization and fertility in Mashona goat does. Small Rum. Res. 39, 283–8.Google Scholar
Lintern-Moore, S. & Everitt, A.V. (1978). The effect of restricted feed intake on the size and composition of the ovarian follicle population in the Wistar rat. Biol. Reprod. 19, 688–91.Google Scholar
Lussier, J.G., Matton, P. & Dufour, J.J. (1987). Growth rates of follicles in the ovary of the cow. J. Reprod. Fertil. 81, 301–7.Google Scholar
Mossa, F., Carter, F., Walsh, D.A., Kenny, D.A., Sith, G.W., et al. (2013). Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring. Biol. Reprod. 88, 92–100.CrossRefGoogle ScholarPubMed
Munakata, Y., Kawahara-Miki, R., Shiratsuki, S., Tasaki, H., Itami, N., et al. (2016). Gene expression patterns in granulosa cells and oocytes at various stages of follicle development as well as in in vitro grown oocyte-and-granulosa cell complexes. J. Reprod. Dev. 62, 359–66.CrossRefGoogle ScholarPubMed
O'Callaghan, D., Yaakub, H., Hyttel, P., Spicer, L.J., Boland, M.P. (2000). Effect of nutrition and superovulation on oocyte morphology follicular fluid composition and systemic hormone concentrations in ewes. J. Reprod. Fertil. 118, 303–13.Google Scholar
Paula, N.R.O., Galeati, G., Teixeira, D.I.A., Lopes Junior, E.S., Freitas, V.J.F., et al. (2005). Responsiveness to progestagen–eCG–cloprostenol treatment in goat food restricted for long period and refed. Reprod. Domest. Anim. 40, 108–10.Google Scholar
Pedersen, T. & Peters, H. (1968). Proposal for a classification of oocytes and follicles in the mouse ovary. J. Reprod. Fertil. 17, 555–7.Google Scholar
Rae, M.T., Palassio, S., Kyle, C.E., Brooks, A.N., Lea, R.G., et al. (2001). Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheep fetuses. Reproduction 122, 915–22.Google Scholar
Reilly, J.S. (2001). Euthanasia of Animals Used for Scientific Purposes. Adelaide: ANZCCART, 106 pp.Google Scholar
Rhodes, F.M., Entwistle, K.W. & Kinder, J.E. (1996). Changes in ovarian function and gonadotropin secretion preceding the onset of nutritionally induced anestrus in Bos indicus heifers. Biol. Reprod. 55, 1437–43.Google Scholar
Rondina, D., Freitas, V.J.F., Spinaci, M. & Galeati, G. (2005). Effect of nutrition on plasma progesterone levels, metabolic parameters and small follicles development in unstimulated goats reared under constant photoperiod regimen. Reprod. Domest. Anim. 40, 548–52.Google Scholar
Sabra, H.A. & Hassan, S.G. (2008). Effect of new regime of nutritional flushing on reproductive performances of Egyptian Barki ewes. Global Veterinaria 2, 28–31.Google Scholar
Safari, J., Kifaro, G.C., Mushi, D.E., Mtenga, L.A., Adnoy, T., et al. (2012). Influence of flushing and season of kidding on reproductive characteristics of Small East African goats (does) and growth performance of their kids in a semi arid area of Tanzania. Afr. J. Agric. Res. 7, 4948–55.Google Scholar
Scaramuzzi, R.J., Campbell, B.K., Downing, J.A., Kendall, N.R., Khalid, M., et al. (2006). A review of the effects of supplementary nutrition in the ewe on the concentrations of reproductive and metabolic hormones and the mechanisms that regulate folliculogenesis and ovulation rate. Reprod. Nutr. Dev. 46, 339–54.Google Scholar
Schmidt, I.G. (1942). Mitotic proliferation in the ovary of the normal mature guinea pig treated with colchicine. Am. J. Anat. 71, 245–70.Google Scholar
Selvaraju, S., Agarwal, S.K., Karche, S.D. & Majumbar, A.C. (2003). Ovarian response, embryo production and hormonal profile in superovulated goats treated with insulin. Theriogenology 59, 1459–68.Google Scholar
Sen, U., Sirin, E. & Kuran, M. (2013). The effect of maternal nutritional status during mid-gestation on placental characteristics in ewes. Anim. Reprod. Sci. 137, 31–6.Google Scholar
Shinohara, Y., Matsumoto, H. & Mori, T. (1997). Granulosa cell kinetics examined by bromodeoxyuridine in combination with colchicine in the mouse ovarian follicles. In Vivo 11, 249–52.Google Scholar
Sirotkin, A. (2010). Effect of two types of stress (heat shock/high temperature and malnutrition/serum deprivation) on porcine ovarian cell functions and their response to hormones. J. Exp. Biol. 213, 2115–30.Google Scholar
Somchit-Assavacheep, A. (2011). Influence of nutritional management on folliculogenesis in ewes. Thai. J. Vet. Med. Suppl. 41, 25–9.Google Scholar
Sormunen-Cristian, R. & Jauhiainen, L. (2002). Effect of nutritional flushing on the productivity of Finnish landrace ewes. Small Rumin. Res. 43, 75–83.Google Scholar
Tanaka, T., Yamaguchi, T., Kamomae, H. & Kaneda, Y. (2003). Nutritionally induced body weight loss and ovarian quiescence in Shiba goats. J. Reprod. Dev. 49, 113–9.CrossRefGoogle ScholarPubMed
Walkden-Brown, S.W. & Restall, B.J., 1996. Environmental and social factors affecting reproduction. In 7th International Conference on Goats. 6–11 May, 1996, Beijing China. 2, 762–75.Google Scholar
Webb, R., Campbell, B.K., Garverick, H.A., Gong, J.G., Gutierrez, C.G., et al. (1999). Molecular mechanisms regulating follicular recruitment and selection. J. Reprod. Fertil. Suppl. 54, 33–48.Google Scholar
Webb, R., Garnsworthy, P.C., Gong, J.-G. & Armstrong, D.G. (2004). Control of follicular growth: local interactions and nutritional influences. J. Anim. Sci. 82 (E. Suppl.), E63–74.Google Scholar
Ying, S., Wang, Z., Wang, C., Nie, H., He, D., et al. (2011). Effect of different levels of short-term feed intake on folliculogenesis and follicular fluid and plasma concentrations of lactate dehydrogenase, glucose, and hormones in Hu sheep during the luteal phase. Reproduction 142, 699–710.CrossRefGoogle ScholarPubMed
Zare-Shahneh, A., Sadeghipanah, A., Javaheri-Barfourooshi, H. & Emami-mibody, M.A. (2008). Effects of equine chorionic gonadotropin (eCG) administration and flushing on reproductive performance in Nadooshan goats of Iran. Afr. J. Biotechnol. 7, 3373–9.Google Scholar
Zieba, D.A., Amstalden, M. & Williams, G.L. (2005) Regulatory roles of leptin in reproduction and metabolism: a comparative review. Domest. Anim. Endocrinol. 29, 166–85.Google Scholar