Technical note
Ultrasonographic study of antral follicle development during sexual maturation in ewe lambs

https://doi.org/10.1016/j.smallrumres.2005.02.003Get rights and content

Abstract

Eight February-born Suffolk ewe lambs underwent transrectal ovarian ultrasonography every 2 weeks (from 6 to 38 weeks of age) and during seven 10-day periods, with starting dates every 5 weeks (from 6 to 36 weeks of age), to study antral follicle development. Blood samples were taken at 2 and 4 weeks of age, and before each ultrasonographic examination, for radioimmunoassay (RIA) of serum FSH and estradiol, and daily, from 30 weeks of age, for measurement of progesterone. Six ewe lambs reached puberty (defined as an elevation in serum progesterone concentrations ≥0.1 ng/ml for ≥7 days) between 32 and 36 weeks of age (mean ± S.E.M.: 34.0 ± 0.5 weeks). The total number of all follicles ≥2 mm in diameter/ewe lamb increased from 12 to 14 weeks, declined from 24 to 28 weeks, rose from 28 to 32 weeks, and then decreased after 32 weeks of age (n = 6; P < 0.05). The diameter of the largest follicle increased from 8 to 14 weeks, declined from 14 to 22 weeks, and finally increased between 32 and 36 weeks after birth (P < 0.05). Mean serum FSH concentrations peaked at 30 weeks and increased again from 14 to 4 weeks before attainment of puberty (P < 0.05). There were 2.4 ± 0.09 peaks in the daily serum FSH concentrations and 0.8 ± 0.1 emerging follicular waves per lamb (follicles attaining ovulatory diameters of ≥5 mm; P < 0.05) over each 10-day scanning period. The frequency of FSH peaks and follicle wave emergence did not change significantly throughout the study. Mean circulating concentrations of estradiol increased gradually (P < 0.05) from approximately 6 weeks of age until puberty. It was concluded that antral follicle recruitment and growth increased after the first 8 weeks of age and just before puberty in February-born ewe lambs. A rhythmic pattern of increases in daily serum FSH concentrations, as seen in adult ewes, was present in the ewe lambs of all ages but the pattern of follicular wave emergence was not fully established in pre- and peripubertal ewe lambs.

Introduction

There is considerable interest in the mechanisms governing postnatal ovarian development in domestic ruminants because of the attempts to breed animals at an early age (Gordon, 1996) and to increase overall productivity, as selection for early puberty can increase the lifetime reproductive rate (Mansour, 1959). Knowledge of the development of ovarian antral follicles in prepubertal ewe lambs is still limited as it was derived largely from infrequent examinations of reproductive tracts collected at slaughter (Land, 1970, Kennedy et al., 1974). Ultrasonography allows frequent monitoring of antral follicle development in the same group of conscious, unstressed animals. The pattern of growth and regression of individual antral follicles attaining an ostensibly ovulatory diameter of ≥5 mm has been described in adult ewes by repeated ultrasonographic examinations of ovaries (Ginther et al., 1995, Bartlewski et al., 1998, Bartlewski et al., 1999a, Evans et al., 2000). In sexually mature ewes, follicles emerge every 3–5 days from a fairly constant pool of 2–3-mm follicles, and grow to a maximum size of 4–8 mm in diameter (Noel et al., 1993, Ginther et al., 1995, Rubianes et al., 1997, Bartlewski et al., 1998, Bartlewski et al., 1999a, Evans et al., 2000, Duggavathi et al., 2003). Ultrasonographic studies conducted in both prolific and non-prolific breeds of sheep revealed that ovulations from 4-mm follicles were rare (<2% of ovulating follicles; Ginther et al., 1995, Bartlewski et al., 1999a). Therefore, the follicular wave in sheep is regarded as a follicle, or a group of follicles, growing to ≥5 mm in size (Ginther et al., 1995, Bartlewski et al., 1999a). The pattern of emergence of follicular waves in cyclic and seasonally anestrous sheep appears to be controlled by periodic elevations in FSH secretion (Ginther et al., 1995, Bartlewski et al., 1998, Bartlewski et al., 1999a).

Non-invasive transrectal ultrasonography was employed to describe changes in follicle numbers and kinetics in heifer calves (Hopper et al., 1993, Adams et al., 1994, Bergfelt et al., 1994, Evans et al., 1994a, Evans et al., 1994b, Rawlings et al., 2003, Honaramooz et al., 2004). When ultrasonography was done daily, over several days, it was discovered that prepubertal heifers produced follicular waves; heifer calves as young as 2 weeks of age exhibited recurrent waves of antral follicle emergence (Adams et al., 1994, Evans et al., 1994b). As in adult cattle (Adams et al., 1992), follicular waves in prepubertal heifers were consistently preceded by transient increases in serum concentrations of FSH. The existence of such a rhythmic wave-like pattern of antral follicle development in pre- and peripubertal ewe lambs was not reported. Ultrasonographic scanning of ovaries in growing ewe lambs, once every 2 weeks, from 4 to 30 weeks of age, was employed to quantify antral follicles (Bartlewski et al., 2002). However, there has been no systematic study of antral follicular populations and wave dynamics in ewe lambs during reproductive development.

The aims of the present study were: (a) to describe changes in antral follicle numbers and wave emergence, using frequent periods of transrectal ovarian ultrasonography, from 6 weeks of age until the first full-length luteal phase of ewe lambs and (b) to correlate these to the changes in circulating concentrations of FSH and estradiol.

Section snippets

Animals and ovarian ultrasonography

Care and treatment of experimental animals were carried out according to the Canadian Council on Animal Care guidelines. The 8 Suffolk ewe lambs used in this study (born between 3rd and 5th February) were initially kept indoors with their mothers. After weaning at 8 weeks of age, they were kept outdoors in pens, under natural conditions of photoperiod and temperature. They were fed alfalfa pellets and barley rations once a day (Rawlings et al., 1991), with hay, water and mineralized salt licks

Body weight and puberty

Mean body weights increased rapidly from birth to 8 weeks and between 10 and 12 weeks of age, then more gradually to 24 weeks of age (P < 0.05), and subsequently plateaued (small gain in mass) until puberty. Puberty was defined as the beginning of the period when serum progesterone concentrations first exceeded 0.1 ng/ml for ≥7 days. The mean age of puberty in six of the eight ewe lambs studied was 34.0 ± 0.5 weeks after birth (range: 32–36 weeks), at an average body mass of 49.9 ± 1.9 kg. Two animals

Discussion

The results of the present study, in which observations were made every 2 weeks in February-born Suffolk lambs, suggest the occurrence of a biphasic pattern of follicular development during sexual maturation of ewe lambs and confirm the findings of our earlier study (Bartlewski et al., 2002). There was an increase in the number of all antral follicles ≥2 mm in size at 14 weeks of age, followed by a decline at 28 weeks, and another increase at 32 weeks of age. The size of the largest follicle was

Conclusion

Transrectal ovarian ultrasonography and hormone measurements in prepubertal ewe lambs revealed that (a) antral follicle numbers (follicles ≥2 mm in diameter) and maximum diameters increased after the first 8 weeks of age and just before puberty (approximately 32 weeks of age) in February-born Suffolk lambs; (b) this pattern of change in antral follicle numbers was due mainly to shifts in the numbers of 2- and 3-mm follicles; (c) circulating concentrations of follicular estradiol increased

Acknowledgements

We thank Ms. Susan Cook, Donna Mattson, Christine Smetschka, Tracy Epp and Mr. Jayaprakash Aravindakashan for their excellent technical assistance; NIDDK and USDA for the provision of reagents for the FSH assays and Mr. Brian Buydens of the Information Technology Services, University of Saskatchewan, for modification of statistical software (The Cycle Detection/Adaptive Threshold Technique). A research grant from NSERC supported this study Dr. P.M. Bartlewski was supported by a University of

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  • Cited by (0)

    1

    Present address: Department of Biomedical Sciences, Ontario Veterinary College, University of Guelph, Guelph, Ont., Canada.

    2

    Present address: School of Agriculture, Food, and Rural Development; University of Newcastle, Newcastle-upon-Tyne, UK.

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