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A. C. O. Evans, G. P. Adams, and N. C. Rawlings

Changes in the pattern of follicular growth and development, and the associated endocrine changes, were examined in prepubertal heifers approaching their first ovulation. Ten, age-matched (± 3 days), Spring-born Hereford heifers were examined daily by transrectal ultrasonography for 17 days beginning 12 weeks before the first ovulation, and daily from just before the first ovulation until the completion of one normal duration ovulatory cycle. On each day of ultrasound examination, the position and diameter of corpora lutea and follicles ≥ 3 mm in diameter were recorded, and one blood sample was collected. Blood samples were also collected every 15 min, for 12 h, at 20, 12 and 4 weeks before the first ovulation, to assess the pulsatile nature of LH and FSH secretion. The first ovulation occurred at 56.0 ± 1.2 weeks of age, at a body weight of 391.9 ± 12.0 kg. Waves of follicular development, similar to those of adult cows, were seen at all ages, and in all heifers, the first ovulation was followed by an ovulatory cycle of short duration (7.7 ± 0.2 days) and then by a normal duration ovulatory cycle (20.3 ± 0.5 days). The maximum diameter of the dominant, or largest subordinate, follicles did not increase as the first ovulation approached, or during the subsequent ovulatory cycles. Similarly, there were no differences between follicle growth rates (1.4 ± 0.1 mm day−1) or regression rates (1.2 ± 0.1 mm day−1) as the animals matured, and the interwave interval increased up to the first ovulation. Waves of follicular development were associated with peaks in FSH concentrations at 12 weeks before the first ovulation. The short duration, ovulatory cycle was associated with low progesterone concentrations and small corpora lutea (mean maximum values 2.75 ± 0.66 ng ml−1 and 19.9 ± 2.0 mm, respectively), compared with normal cycle durations (10.15 ± 0.58 ng ml−1 and 25.8 ± 0.8 mm). Mean serum oestradiol and LH concentrations and LH pulse frequency increased as the first ovulation approached, but FSH concentrations did not. We conclude that, in heifers before the first ovulation, growth and regression of large follicles occur in a wave-like pattern, with characteristics and associated patterns of gonadotrophin secretion similar to those seen in adult, cyclic animals. Hence, in late prepubertal heifers, factors controlling follicle growth are in place, and there are no changes in these parameters in the three months preceding the first ovulation.

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O A Bogle, M H Ratto, and G P Adams

An ovulation-inducing factor (OIF) in the seminal plasma of llamas and alpacas (induced ovulators) and cattle (spontaneous ovulators) suggests that OIF is a conserved constituent of seminal plasma among mammals. In this study, three experiments were designed to determine the biological effects of OIF in different species. In experiment 1, superstimulated prepubertal female CD-1 mice (n=36 per group) were given a single 0.1 ml i.p. dose of 1) phosphate-buffered saline (PBS), 2) 5 μg gonadotropin-releasing hormone (GNRH), 3) 5 IU hCG, or 4) llama seminal plasma. The proportion of mice that ovulated was similar among groups treated with GNRH, hCG, or seminal plasma, and all were higher than the saline-treated group (P<0.001). In experiment 2, female llamas (n=8 or 9 per group) were intramuscularly treated with 1) 2 ml PBS, 2) 1 ml diluted llama seminal plasma, 3) 3 ml equine seminal plasma, or 4) 3 ml porcine seminal plasma. Experiment 3 was the same as experiment 2 except that the dose of equine and porcine seminal plasma was increased to 8 and 10 ml respectively. All llamas that were treated with llama seminal plasma ovulated and none that were treated with saline ovulated (P<0.0001). The proportion of llamas that ovulated in response to equine and porcine seminal plasma was intermediate. We conclude that the mechanism for the biological response to OIF is present in prepubertal CD-1 mice and that OIF is present in equine and porcine seminal plasma.

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G. P. Adams, A. C. O. Evans, and N. C. Rawlings

Eleven age-matched (±4 days) Hereford heifers were examined by transrectal ultrasonography daily for 18 days beginning 20 weeks (5 months) before puberty (first ovulation) to determine the suitability of the transrectal ultrasound technique for imaging the ovaries of prepubertal heifers and to test the hypothesis that ovarian follicular development occurs in waves in prepubertal heifers. Satisfactory ovarian images were obtained during preliminary ultrasound examinations conducted 4 weeks before the observational period (that is 32 weeks of age), during which a semirigid probe extension was used to allow external manipulation of the intrarectally placed ultrasound transducer. Daily examinations commencing at 36 weeks of age were accomplished by intrarectal placement of the operator's hand and transducer, without complication, in all 11 heifers throughout the observational period. Periodic increases in the number of follicles detected (day effect, P < 0.02) were inversely related to the diameter of the largest follicle (r = −0.3, P < 0.03). Portions of three anovulatory follicular waves were detected in all heifers during the observational period (first and third waves in part and second wave in whole). Individual follicles destined to assume a dominant or subordinate position in a wave were retrospectively identified and monitored beginning at a diameter of 4–5 mm. The interval between the emergence of dominant follicles of successive waves (interwave interval) was 8.0 ± 0.4 days and the interval between successive maxima in the number of follicles per heifer per day was 8.1 ± 0.5 days. The growing phase of the dominant follicles best fit a quadratic curve. The growing phase of the largest subordinate follicles, and the static and regressing phases of dominant and subordinate follicles best fit simple linear expressions. Periodic surges in serum concentrations of FSH (day effect, P < 0.0001), but not of LH (day effect, not significant), were associated with follicular wave dynamics. FSH surges (increase and decrease, respectively, best fit quadratic curves) spanned a mean of 3 days and reached maximum values 0.9 ± 0.3 days before emergence of the wave. Results supported the hypothesis that follicular development occurs in waves in prepubertal heifers. Mechanisms controlling the well-ordered phenomena of wave emergence, follicle selection and follicle regression, similar to those of sexually mature heifers, were present in 36-week-old prepubertal heifers.

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A. C. O. Evans, G. P. Adams, and N. C. Rawling

The aim of this study was to characterize changes in ovarian follicle dynamics in relation to changes in hormone secretion in heifer calves from birth to 8 months of age. The position and diameter of ovarian follicles ≥4 mm in diameter were recorded, the number of ovarian follicles ≥2 mm in diameter counted, and blood samples collected daily for periods of 18 days, starting at 2, 8, 14, 24 and 34 weeks of age in ten heifers. The mean age at first ovulation was 52.8 ± 1.6 weeks. At all ages ovarian follicular development occurred in a wave-like manner, as in mature cattle. The maximum diameter of the dominant and the largest subordinate follicles increased between 2 and 34 weeks of age (P < 0.05); however, the greatest increase occurred between 2 and 8 weeks of age. There was a similar increase in the numbers of small and large ovarian follicles (P < 0.05). The duration of detection of dominant follicles (number of days visible at a diameter of ≥4 mm) also increased between 2 and 34 weeks of age (P < 0.05). The emergence of waves of follicular development was preceded by peaks in plasma FSH concentrations (P < 0.05) at 2 weeks of age but this was less clear at other ages. There was a rise in circulating concentrations of gonadotrophins between 4 and 14 weeks of age. We concluded that in heifer calves as young as 2 weeks of age ovarian follicles grew in a wave-like fashion, similar to those of adult cattle. We speculate that the early rise in gonadotrophin secretion stimulated the increase in numbers of follicles and follicle diameters observed, indicating an early critical step in reproductive development.

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G. P. Adams, J. Sumar, and O. J. Ginther

Summary. The effects of lactational status and reproductive status on patterns of follicle growth and regression were studied in 41 llamas. Animals were examined daily by transrectal ultrasonography for at least 30 days. The presence or absence of a corpus luteum and the diameter of the largest and second largest follicle in each ovary were recorded. Llamas were categorized as lactating (N = 16) or non-lactating (N = 25) and randomly allotted to the following groups (reproductive status): (1) unmated (anovulatory group, N = 14), (2) mated by a vasectomized male (ovulatory non-pregnant group, N = 12), (3) mated by an intact male and confirmed pregnant (pregnant group, N = 15). Ovulation occurred on the 2nd day after mating with a vasectomized or intact male in 26/27 (96%) ovulating llamas. Interval from mating to ovulation (2·0 ± 0·1 days) and growth rate of the preovulatory follicle (0·8 ± 0·2 mm/day) were not affected by lactational status or the type of mating (vasectomized vs intact male). Waves of follicular activity were indicated by periodic increases in the number of follicles detected and an associated emergence of a dominant follicle that grew to ≥7 mm. There was an inverse relationship (r = −0·2; P = 0·002) between the number of follicles detected and the diameter of the largest follicle. Successive dominant follicles emerged at intervals of 19·8 ± 0·7 days in unmated and vasectomy–mated llamas and 14·8 ± 0·6 days in pregnant llamas (P = 0·001). Lactation was associated with an interwave interval that was shortened by 2·5 ± 0·05 days averaged over all groups (P = 0·03). Maximum diameter of anovulatory dominant follicles ranged from 9 to 16 mm and was greater (P < 0·05) for non-pregnant llamas (anovulatory group, 12·1 ± 0·4 mm; ovulatory group, 11·5 ± 0·2 mm) than for pregnant llamas (9·7 ± 0·2 mm). In addition, lactation was associated with smaller (P < 0·05) maximum diameter of dominant follicles averaged over all reproductive statuses (10·4 ± 0·2 vs 11·7 ± 0·3 mm). The corpus luteum was maintained for a mean of 10 days after ovulation in non-pregnant llamas and to the end of the observational period in pregnant llamas. The presence (ovulatory non-pregnant group) and persistence (pregnant group) of a corpus luteum was associated with a depression in the number of follicles detected and reduced prominence of dominant follicles (anovulatory group > ovulatory non-pregnant group > pregnant group). Lactation was also associated with reduced prominence of dominant follicles. The results demonstrate that follicular activity occurred in waves for llamas of all types of reproductive status and that lactation and the presence of a corpus luteum were associated with depressed follicular development.

Keywords: ovaries; follicles; follicular waves; lactation; llamas; camelids

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G. P. Adams, R. L. Matteri, and O. J. Ginther

Summary. The hypothesis was tested that greater growth of the dominant follicle of wave 1 (first follicular wave of an interovulatory interval), compared with that of subsequent anovulatory waves, is due to lower circulating concentrations of progesterone during the growing phase of the follicle. Control heifers (n = 6) were compared with heifers (n = 6) treated with a decreasing dose of progesterone from day 0 to day 5 (ovulation = day 0). Maximum diameter (12·7 ± 0·9 versus 15·3 ± 0·7 mm) and mean diameter of the dominant follicle of wave 1, averaged over days, were smaller (P < 0·05) in the progesterone-treated than in the control group. Progesterone treatment did not suppress circulating follicle-stimulating hormone (FSH); but the second FSH surge was earlier, resulting in earlier emergence of wave 2 as indicated by a tendency (P ≤ 0·1) for group × day interactions attributed to earlier detection of the dominant follicle and an earlier rise in the total number of follicles detected. The stated hypothesis was supported.

We also tested the hypothesis that exposure to low circulating concentrations of progesterone at the end of the growing phase of the anovulatory dominant follicle of wave 1 results in continued growth and prolonged maintenance of the dominant follicle. Heifers (n = 6 per group) were given a luteolytic dose of prostaglandin F (PGF) on day 6 and treated with a low (30 mg day−1), physiological (150 mg day−1), or high (300 mg day−1) dose of progesterone on days 6 to 20. Continued periodic emergence of anovulatory follicular waves occurred (2·1 ± 0·0 waves, 2·8 ± 0·2 waves, 3·8 ± 0·3 waves, respectively; P < 0·05) until treatment was stopped (interovulatory intervals: 26·2 ± 1·0, 30·8 ± 0·6 and 40·3 ± 1·7 days, respectively; P < 0·05). Compared with the physiological dose group, the growth of the dominant follicle was inhibited to a lesser degree in the low-dose group since it grew for longer (P < 0·05) and to a larger diameter (P < 0·05), and persisted for longer (P < 0·05). Prolonged dominance of this oversized (> 20 mm) follicle was associated with delayed emergence of wave 2. The hypothesis was supported. Results also showed that the high dose of progesterone suppressed the dominant follicle more than the physiological dose when given during the growing phase, but not when given after the growing phase. The suppressive effects of progesterone were not mediated by decreased circulating FSH, since progesterone treatment did not suppress FSH. Collectively, the results demonstrated that progesterone inhibited the dominant follicle in a dose-dependent manner when the follicle was exposed during its growing phase.

Keywords: progesterone; follicle-stimulating hormone; follicles; follicular waves; ultrasound; cow

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J. Singh, R. A. Pierson, and G. P. Adams

Heifers were studied to determine whether computer-assisted quantitative echotexture analysis of ultrasound images reflect functional and endocrine characteristics of dominant and subordinate follicles at specific stages of development. Heifers were examined using transrectal ultrasonography each day until ovariectomy on day 3 (n = 8) and day 6 (n = 9) of wave 1, day 1 of wave 2 (n = 7), or after onset of pro-oestrus ≥ 17 days after ovulation (n = 8) to obtain growing, early-static, late-static and regressing dominant follicles of wave 1, subordinate follicles, preselection follicles and preovulatory dominant follicles. Ultrasound images of the follicles were obtained in vitro and analysed using custom-developed computer algorithms. Mean pixel (picture element) values (grey-scale: black = 0, white = 255) for the follicle wall and stroma increased (P < 0.05) progressively from the growing to the regressing phases of the dominant follicle of wave 1. The antrum and wall of subordinate follicles had higher (P < 0.05) mean pixel values than that of the corresponding dominant follicles. Pixel heterogeneity (a measure of variation of grey-scale values of pixels) of images of the follicle antrum and wall increased (P < 0.05) progressively during the early-static to regressing phases. A progressive increase (P < 0.05) in the slope of the regression line of pixel values for the follicle wall was detected from the growing to the regressing phases of the dominant follicle of wave 1. The regression line of the wall of the preovulatory dominant follicle had the lowest (P < 0.05) slope. Oestradiol concentration in the follicular fluid decreased (P < 0.05) from the growing to the late-static phase, while a marked decrease (P < 0.05) in the androstenedione concentration was recorded between the growing and the early-static phases of the dominant follicle. Progesterone content did not increase until follicles were in the final stages of regression. Pixel heterogeneity of the antrum and wall, and the slope of the follicle wall regression line were negatively correlated (P < 0.001) with oestradiol and the oestradiol:progesterone ratio in follicular fluid. The results of this study support the hypothesis that echotexture characteristics of ultrasound images of the follicle antrum and wall are correlated with the functional and endocrine status of a follicle.

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J. Singh, R. A. Pierson, and G. P. Adams

Nulliparous heifers (n = 58) were studied to determine whether computer-assisted quantitative echotexture analysis of ultrasound images reflects the functional and histomorphological characteristics of the corpus luteum. The ovaries of heifers were examined daily by transrectal ultrasonography from day −2 (day 0 = ovulation) until the day of ovariectomy during metoestrus (day 3; n = 8), early dioestrus (day 6; n = 9), mid-dioestrus (mean, day 10; n = 7), or pro-oestrus (mean, day 18; n = 8; Expt 1). High resolution ultrasound images of corpora lutea were obtained in vitro, and were digitized and analysed using custom-developed computer algorithms optimized for ultrasonography. Cryostat sections of corpora lutea were examined for lipid distribution, and corpora lutea were homogenized to determine the content of progesterone, total protein, cholesterol and triglyceride. In Expt 2, heifers (n = 26) were ovariectomized as in Expt 1, and ovaries were prepared for histomorphometric evaluation. Pixel values (brightness of picture elements) of ultrasound images of corpora lutea were characterized as high during metoestrus, low during early and mid-dioestrus, and increasing again during pro-oestrus (P < 0.05). Changes (P < 0.001) in volume density of luteal cells were characterized as increasing from metoestrus (40.7 ± 0.4%) to mid-dioestrus (55.8 ± 2.8%) and decreasing again at pro-oestrus (41.5 ± 0.9%). The proportion of blood vascular components decreased (P < 0.001) progressively from 31.0 ± 1.0% in metoestrus to 15.6 ± 1.1% in pro-oestrus. Pixel values of ultrasound images of corpora lutea were correlated with luteal (r = −0.72, P < 0.05) and plasma (r = −0.71, P < 0.03) progesterone concentration, and to the volume densities of luteal cells (r = −0.75, P < 0.02) and connective tissue (r = 0.69, P < 0.03). Estimates of triglyceride, protein and cholesterol content of corpora lutea were not correlated with pixel values of ultrasound images. Protein and cholesterol content did not change while triglyceride concentration increased during pro-oestrus (P < 0.05). Results support the hypothesis that ultrasound images reflect luteal and plasma progesterone content, and histomorphological characteristics of the corpus luteum.

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T. E. Adams, J. F. Quirke, J. P. Hanrahan, B. M. Adams, and J. G. Watson

Summary. Rates of ovulation differed significantly (P < 0·01) among ewes of the different genetic lines. However, of the reproductive characteristics studied, only progesterone concentration at the height of luteal function, duration of oestrus, and interval from onset of oestrus to peak of the preovulatory gonadotrophin surge showed significant positive association with rate of ovulation. The pattern of secretion of LH during the periovulatory period did not differ in the Galway and Finnish Landrace breeds. The total amount of LH secreted during the preovulatory surge did not differ amongst lines. Similarly, no difference in the plasma concentration of LH at the height of the preovulatory surge was noted among Galway and reference Finnish Landrace lines. However, the concentration of LH at the height of the surge was significantly (P < 0·05) reduced in the selected Finnish Landrace line. Plasma concentrations of FSH during the preovulatory period were significantly (P < 0·05) elevated in the breed (Galway) with the lowest prolificacy. When contrasted with either of the Finnish Landrace lines, the magnitudes of the preovulatory surge of FSH and the secondary surge of FSH were significantly greater (P < 0·05) in Galway ewes. These results suggest that genetic difference in rate of ovulation among sheep breeds is not tightly coupled to quantitative differences in plasma concentration of gonadotrophic hormones during the periovulatory period.

Keywords: gonadotrophins; periovulatory period; ovulation rate; prolific sheep

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G. P. Adams, R. L. Matteri, J. P. Kastelic, J. C. H. Ko, and O. J. Ginther

Summary. The effects of ablation of a dominant follicle and treatment with follicular fluid on circulating concentrations of follicle-stimulating hormone (FSH) were studied and the temporal relationships between surges of FSH and follicular waves were studied in heifers with two or three follicular waves/interovulatory interval. Cauterization of the dominant follicle on Day 3 or Day 5 (ovulation on Day 0) (six control and six treated heifers/day) resulted in a surge (P < 0·05) in FSH beginning the day after cautery. The FSH surge prior to wave 2 (first post-treatment follicular wave) occurred 4 days (Day 3 cautery) and 2 days (Day 5 cautery) before the surge in control groups, corresponding to a 4-day and a 2-day advance in emergence of wave 2 compared with controls. It was concluded that the dominant follicle on Day 3 and Day 5 was associated with the suppression of circulating FSH concentrations. Heifers (n = 4/group) were untreated or treated intravenously with a proteinaceous fraction of bovine follicular fluid on Days 0–3, 3–6, or 6–11. Concentrations of FSH were suppressed (P < 0·05) for the duration of treatment, regardless of the days of treatment. Cessation of treatment was followed within 1 day by the start of a surge in FSH. The FSH surge prior to wave 2 occurred 2 days earlier (treatment on Days 0–3), 1 day later (treatment on Days 3–6), and 6 days later (treatment on Days 6–11) than in controls, corresponding to an equivalent advance or delay, respectively, in the emergence of wave 2 compared with controls. The results suggest that the effects of exogenous follicular fluid on follicular development were mediated, in whole or in part, by altering plasma FSH concentrations. Control heifers combined for the two experiments were separated into those with 2-wave (n = 11) or 3-wave (n = 5) interovulatory intervals. Two-wave heifers had two FSH surges and 3-wave heifers had three apparent FSH surges during the interovulatory interval. Results of the cautery and follicular fluid experiments indicated that a surge in FSH necessarily preceded the emergence of a wave. The FSH surges in treated and control heifers began 2–4 days before the detectable (ultrasound) emergence of a follicular wave (follicles of 4 and 5 mm), peaked 1 or 2 days before emergence and began to decrease approximately when the follicles of a wave begin to diverge into a dominant follicle and subordinate follicles (follicles 6–7 mm).

Keywords: FSH; follicles; follicular waves; follicular fluid; inhibin; heifer