The effect of feeding strategy during the pre-follicular phase on subsequent follicular development in the pig

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1 Domestic Animal Endocrinology 29 (2005) The effect of feeding strategy during the pre-follicular phase on subsequent follicular development in the pig W. Hazeleger, N.M. Soede, B. Kemp Department of Animal Sciences, Wageningen University, Marijkeweg 40, PO Box338, 6700 AH Wageningen, The Netherlands Abstract In female pigs feeding level has important effects on reproductive performance. This review is focused on the follicular development after low and high feeding levels during the luteal phase in gilts. Although aspects of diet composition seem to have a role in regulating reproductive performance, the most important aspect appears to be the plane of nutrition. Similar effects are described during lactation in primiparous sows, when their metabolism is challenged to its maximum. Also in this situation feeding level clearly affects weaning to oestrus interval, follicular development, oocyte maturation, ovulation rate and subsequent embryonic survival Elsevier Inc. All rights reserved. Keywords: Nutrition; Follicle development; Ovulation rate; Gilts; Sows 1. Introduction A low feeding level during the pre-follicular phase is known to have several effects on reproductive processes in pigs. Low feeding levels of sows during lactation may negatively affect subsequent weaning-to-oestrus interval, ovulation rate and embryo survival [1 4]. These effects of a negative energy balance seem to be related to the suppressive effects of a low feeding level on LH pulsatility and follicular development [5,6] and have been suggested to be mediated by changes in insulin levels [7]. However, although insulin-stimulating di- Corresponding author. Tel.: ; fax: address: wouter.hazeleger@wur.nl (W. Hazeleger) /$ see front matter 2005 Elsevier Inc. All rights reserved. doi: /j.domaniend

2 W. Hazeleger et al. / Domestic Animal Endocrinology 29 (2005) ets in lactating primiparous sows increased follicle size at day 2 after weaning (P = 0.06), effects on subsequent weaning-to-oestrus interval and other reproductive performance measurements were absent [4,8]. In general, effects of feed restriction on subsequent reproductive performance reveal different results. In some studies only effects on weaning to oestrus interval are found, and in others effects on ovulation rate or embryo survival are found [9]. Most of the time effects have been studied in lactating animals, as will be reviewed briefly. However, in the field of feeding strategy and its effects on follicular development in cyclic gilts, new information has become available recently and will be presented subsequently in this review. 2. Effects of feed intake during lactation on follicular development The role of feed intake in lactating animals on subsequent reproduction has been reviewed several times [9 17]. The effects of limited feed intake during lactation on follicular development vary from no effect to a negative effect. This negative effect has shown to be mediated by a decreased LH pulsatility. Normally, the LH pulsatility increases during lactation and immediately after weaning [18], but because of the relatively low feed intake (especially in primiparous sows) this restoration of LH pulsatility seems to be depressed [19,20]. Several studies show that LH levels and pulsatility directly after weaning are related to restoration of LH pulsatility during lactation [4,18,21]. LH pulsatility is low during early lactation and in those sows in which restoration of LH pulsatility is seen during the course of lactation, also high LH levels and high pulse frequency directly after weaning are found. As a consequence, these sows show a short weaning to oestrus interval [4,22]. Those sows, in which LH pulsatility is not restored during lactation, also have low LH levels and pulse frequency directly after weaning, resulting in poor follicular development, a prolonged weaning to oestrus interval and poor subsequent reproductive performance [9]. It seems, therefore, that the ability of sows to increase levels of LH during lactation is important for proper follicular development, and a subsequent short weaning to oestrus interval, good ovulation rate and embryonic survival. In primiparous sows fed different energy and protein levels during a 28 day lactation period, it was demonstrated that average daily protein intake and energy intake affected mean LH concentration on day 21 of lactation [21]. At a low metabolizable energy (ME) intake, increasing lysine (= protein) intake had little effect on mean LH. The influence of lysine intake on LH secretion increased as energy intake increased. These results indicate that mean LH at day 21 of lactation is reduced by restrictions of either lysine (protein) or energy intake. Similar effects on LH pulse frequency and LH concentration and subsequent follicle development have also been reported [4,23 26], using protein or energy restriction during lactation. It seems, therefore, that nutritional effects on follicular development after weaning are due to a reduced LH release during and after lactation, although no positive effect of GnRH treatment during feed restriction on subsequent reproductive performance was found [3]. In older reviews [12,13] it was concluded that feed intake during lactation has little effect on ovulation rate. However, reduction of feed intake during lactation in primiparous sows resulted in a reduced ovulation rate in more recent studies [4,27,28].

3 364 W. Hazeleger et al. / Domestic Animal Endocrinology 29 (2005) Older parity sows nowadays often have ovulation rates of about 25 and higher, which is well above the uterine capacity for embryos/foetuses during pregnancy. Therefore, effects of nutrition on ovulation rate have to be substantial to demonstrate effects on litter size in these sows. In first litter sows ovulation rate is substantially lower and therefore relatively modest effects on follicular development and ovulation rate may affect litter size. Besides ovulation rate the quality of the resulting embryos might be affected by an impaired follicle development. Several researchers have found nutritional effects on follicle and oocyte quality just before ovulation or on embryonic survival [3,5,23,29]. 3. Effect of feeding level during the pre-ovulatory phase on follicular development in gilts In gilts, the nutritional status during the luteal phase seems to affect subsequent reproduction too. It has been shown that feed restriction during the luteal phase has a negative effect on subsequent embryonic survival, but not on ovulation rate [30]. However, after insulin treatment during restricted feeding in the luteal phase a substantial increase in ovulation rate was found [31]. This might indicate that besides feeding level (as has been shown in lactating sows), also insulin or insulin stimulating diets might exert an effect on follicular development. The importance of insulin for the effects of nutrition on reproductive performance in gilts has, until now, only been studied using insulin injections [31,32]. Therefore research was conducted at our institute to study effects of feed restriction and feed composition during the last week of a 3 week progesterone dominance (Altrenogest) on the development of the antral follicle pool and on subsequent ovulation rate and embryo survival in gilts (unpublished data). To have a more biological variation in insulin profiles, two diets differing in their insulin-stimulating effects were used [33]. During the first 15 days of the progestagen treatment (day 21 to 7), gilts were given a commercial diet for breeding gilts at two times maintenance (2.0 M). During the last 7 days of the progestagen treatment (day 6 to 0), gilts were divided over four treatment groups and given a high (H: 2.8 M) or a low feeding level (L: 1.5 M) of either a starch-rich (S) or fat-rich (F) diet, according to [4]. Day 0 was the last day of progestagen treatment and all animals returned to the commercial diet for breeding gilts (2.8 M) at day 1. Immediately after ovulation, feed allowance was reduced to 1.5 M. Average follicle size was similar in all treatment groups at the 1st day of treatment (day 7; 2.8 mm, SEM = 0.7; Fig. 1). At day 0, average follicle size was higher in the gilts that had been on the High feeding level than in gilts that had been on the Low feeding level (2.9 mm versus 2.2 mm, P < 0.01). The effects were still apparent at days 2 and 3; 3.8 mm versus 3.4 mm, P = 0.11 and 4.7 mm versus 4.2 mm, P < 0.05, but disappeared by day 4; 5.3 versus 5.4, P = Energy source in the diet never affected follicle size. In each treatment group, seven gilts were slaughtered at day 1 to assess follicle development in more detail. The High feeding level resulted in an increase in the number of follicles larger than 4.5 mm (16.7 versus 7.5; P < 0.01) and in these gilts, average feed intake during the treatment week was positively related to the number of follicles larger than 4.5 mm (P < 0.05). Average IGF-concentration in the follicular fluid of the follicles of mm was not affected by treatments. Microscopical evaluation on every tenth 10 m haematoxylin/eosin stained

4 W. Hazeleger et al. / Domestic Animal Endocrinology 29 (2005) Fig. 1. Mean follicle development (±S.D.) as assessed with transcutaneous ultrasonography for gilts at onset (day 7) and end (day 0) of a 7-day period (days of progestagen treatment) in which they were fed a high (2.8 M) or low (1.5 M) level of a starch-rich (S) or fat-rich (F) diet and during the follicular phase thereafter (day 2 5 and the day before ovulation) in which they were fed 2.8 M of a normal sow diet. + P = 0.11, * P < 0.05, ** P < slide of the right ovary did not show an effect of treatment on the level of atresia, classified by judging intactness of the granulose cell layer and occurrence of pycnotic cells. Follicle size at ovulation (Fig. 1) was lower in the gilts that had been on the high feeding level during treatment (6.6 mm versus 7.1 mm, SEM = 0.7; P < 0.05), but ovulation rate was higher in these gilts (17.2 versus 14.8; P < 0.01). In gilts on the high feeding level, feed intake during treatment was related to ovulation rate (b = 5.1, P < 0.05; Fig. 2). Oestrus expression, pregnancy rate and embryo survival at day 10 of pregnancy were not affected by treatment. From these data, it appears that a low feeding level during the last week of progesterone dominance results in a reduced number of antral follicles in the larger size classes at the end of the period of progesterone dominance. These results are comparable with effects of low feeding on follicular pool characteristics in first litter sows at weaning as mentioned before. Subsequent follicular development was affected by low feeding levels during the progesterone dominance period until day 2 and 3 after treatment, but not anymore at day 4 (see Fig. 1). In first litter sows subjected to low feeding levels during lactation, similar carry-over effects were seen on day 2 after weaning [26] and 38 h before estimated time of oestrus [5]. In our study, the 1-week low feeding level during progesterone treatment resulted in a lower ovulation rate (17.2 versus 14.8 CL for high and low feeding level; P < 0.01). Also the individual feed intake in the high feeding treatment was related to ovulation rate (b = 5.1, P < 0.05; Fig. 2). These effects of feeding level on ovulation rate are comparable to results obtained in lactating sows as mentioned above. This suggests that fewer follicles are recruited due to the low feeding level resulting in less antral follicles responding properly to the GnRH/LH pulse generator signal for recruitment [22,34]. The relatively small and short term carry-over effects on follicle growth (only the first 3 days) in our study may be explained by the relative higher feed intake during the follicular phase in gilts fed low feeding levels or relative lower feed intake in the high feeding level

5 366 W. Hazeleger et al. / Domestic Animal Endocrinology 29 (2005) Fig. 2. Relation between average feed intake per day during the last 7 days of a 22-day period of progestagen treatment) and subsequent ovulation rate in gilts with a feed allowance of 2.8 M (M = 420 kj ME W-0.75 day-1) of a starch-rich ( ) or fat-rich ( ) diet (ovulation rate = 5.10 feed intake , P < 0.05). during the treatment week (2.45 M versus 1.85 M for low and high feeding level, respectively; P <.01). This may also explain the larger follicles at ovulation found in these gilts (7.1 mm versus 6.7 mm for low and high feeding level, respectively; P <.05) and the effects on ovulation rate might be masked. However, the potential effect of feed restriction during the last week of progesterone dominance appears to be larger than the effect of feed intake after progesterone withdrawal. In general, it can be concluded that a low feeding level during the pre-follicular phase has a negative effect on follicular development and ovulation rate. Embryo survival at day 10 was not affected by treatment in our study. Using a similar gilt model, effects of feed restriction during the luteal phase on ovulation rate and embryo survival in the subsequent cycle was studied [30]. They did not find an effect on ovulation rate, but embryo survival was lower in gilts fed restricted in the last week of the luteal phase as compared to controls. The negative effects on embryo survival indicate that follicle quality; oocyte quality or corpus luteum function is impaired due to feed restriction in the preceding luteal phase. A negative effect of restricted feeding during a complete oestrous cycle on the final stage of oocyte maturation has been demonstrated before [35]. In our present study, no indications exist that follicle quality (besides size) is impaired as a result of the low feeding level, since levels of atresia and IGF-1 levels in follicles were similar for both treatment groups. However, the effects on embryonic survival cannot be compared, because we studied embryonic survival at day 10, while in the other study embryonic mortality at day 28 of pregnancy was evaluated [30]. The effects of feeding strategy on ovulation rate and embryonic mortality, found in our study contrast with the other study mentioned [30]. In our study, we found increased feed

6 W. Hazeleger et al. / Domestic Animal Endocrinology 29 (2005) intake during the follicular phase of the cycle in gilts fed low feeding levels previously. This may have compensated potential effects on embryo development and survival. In the other study [30], feed intake in the follicular phase was high and similar in the treatment groups. A major difference between the mentioned study [30] and our study is that we studied the effect during an artificial luteal phase (Altrenogest treatment) with no corpora lutea present, while they [30] did their study during the natural luteal phase. Recent research [36] showed that during an artificial luteal phase (Altrenogest) with no corpora lutea, follicular development was suppressed to a lesser extend. This resulted in larger follicles at the end of the Altrenogest treatment (3.01 ± 0.31 mm versus 2.52 ± 0.20 mm for Altrenogest and natural luteal phase, respectively; P < ) and a higher subsequent ovulation rate (16.6 ± 1.7 mm versus 15.1 ± 1.2 mm for Altrenogest and natural luteal phase, respectively; P < 0.05). Probably during an artificial luteal suppression (Altrenogest), follicle development is less suppressed and this might enhance the sensitivity of the follicles to the plane of nutrition as we found. A comparable experiment using Altrenogest was performed using Landrace and Mangalica breed gilts, fed a high and low level during the last week of Altrenogest treatment and subsequent follicular phase [37]. Ovulation was induced by 1000 iu ecg the day after last Altrenogest treatment and 750 iu hcg 72 h later (n = 10 in all groups). In this study no effect on the size of the follicles during any stage of the follicular phase was found. However, a positive effect of feeding level on the number of ovulatory follicles at 34 h after hcg was found in Landrace gilts (32.3 ± 10.5 versus 17.1 ± 12.3 follicles in high and low feeding level, respectively; P <.005), but not in Mangalica gilts (25.3 ± 2.9 versus 28.8 ± 7.3 follicles in high and low feeding level, respectively; P > 0.05). In their study [37] follicles (at 34 h after hcg) were analyzed for oestradiol and progesterone content and maturation stage of oocytes was assessed, but in both breeds no differences between feeding levels were found. Interestingly, the Mangalica breed did not respond to a high feeding level. It might be speculated that the metabolic response of this breed to a high feeding level is different because it is a very fat breed. The lack of effect on follicle development on the beginning of the follicular phase in both breeds might be related to the fact that a part of the gilts may still have had corpora lutea up to the last days of Altrenogest treatment. Probably corpora lutea in combination with Altrenogest treatment result in a more intensive suppression of follicular development, possibly suppressing the sensitivity to metabolic effects, as might be also the case in the previous mentioned study [30], while in a spontaneous oestrous cycle effects of feeding level on oocyte maturation can be found [35]. 4. Effects of insulin The effects of insulin stimulating diets have been studied previously in our laboratory, in gilts and sows [4,33]. It was shown that a starch-rich diet resulted in higher post-prandial insulin and IGF-1 levels in blood as compared to a fat-rich diet. In lactating sows starch-rich diets resulted in larger sized follicles at day 2 after weaning [4]. Insulin has been related to LH receptor formation in granulosa cells and to oestrogen production by antral follicles [32,38,39] and increased ovulation rates [32]. Also plane of nutrition has an effect on postprandial insuline levels and LH pulsatility [35]. Moreover, insulin withdrawal from diabetic

7 368 W. Hazeleger et al. / Domestic Animal Endocrinology 29 (2005) gilts during the luteal phase reduced ovulation rate and increased the rate of follicular atresia [40]. It was therefore hypothesized that dietary energy source may affect follicle development. However, in our study dietary energy source did not affect follicular development in gilts during and after the treatment period. In a gilt model, insulin injections during feed restriction in the last week of the luteal phase positive effects on peri-oestrus LH, FSH and oestrogen profiles were found [31]. In other studies, however, insulin administration fails to exert positive effects on reproduction [26,41]. Effects of stimulation of insulin, dietary or by injection, on reproduction therefore remain ambiguous. It might be that feeding strategy acts more through the metabolic status of the animal, with all metabolic hormones involved, rather than through insulin and/or IGF-1 alone. Concluding, it can be stated that feeding level during the luteal phase in gilts and during lactation in sows affects subsequent follicular development, ovulation rate and embryo survival. This effect seems to depend on the suppression of follicular development by lactation or luteal phase. Probably these effects are not only mediated by effects on LH release, but also by other regulatory mechanisms acting directly on the ovary. Although insulin and or IGF-1 seem to be involved in such a regulatory process, probably more metabolic regulatory aspects affect follicular development. References [1] Kirkwood RN, Lythgoe ES, Aherne FX. Effect of lactation feed intake and gonadotropin-releasing hormone on the reproductive performance of sows. Can J Anim Sci 1987;67: [2] Kirkwood RN, Baidoo SK, Aherne FX, Sather AP. The influence of feeding level during lactation on the occurrence and endocrinology of the post-weaning oestrus in sows. Can J Anim Sci 1987;67: [3] Zak LJ, Cosgrove JR, Aherne FX, Foxcroft GR. Pattern of feed intake and associated metabolic and endocrine changes differentially affect post-weaning fertility in primiparous lactating sows. J Anim Sci 1997;75: [4] Van den Brand H, Dieleman SJ, Soede NM, Kemp B. Dietary energy source at two feeding levels during lactation of primiparous sows: I. Effects on glucose, insulin, and luteinizing hormone and on follicle development, weaning-to-oestrus interval, and ovulation rate. J Anim Sci 2000;78: [5] Zak LJ, Xu X, Hardin RT, Foxcroft GR. Impact of different patterns of feed intake during lactation in the primiparous sow on follicular development and oocyte maturation. J Reprod Fertil 1997;110: [6] Quesnel H, Pasquier A, Mounier AM, Prunier A. Influence of feed restriction during lactation on gonadotropic hormones and ovarian development in primiparous sows. J Anim Sci 1998;76: [7] Cox NM. Control of follicular development and ovulation rate in pigs. J Reprod Fertil Suppl 1997;52: [8] Van den Brand H, Soede NM, Kemp B. Dietary energy source at two feeding levels during lactation of primiparous sows: II. Effects on perioestrus hormone profiles and embryonal survival. J Anim Sci 2000;78: [9] Prunier A, Soede N, Quesnel H, Kemp B. Productivity and longevity of weaned sows. In: Pluske JR, de Lividich J, Verstegen MWA, editors. Weaning the pig. Wageningen Academic Publishers; p [10] Dourmad JY, Etienne M, Prunier A, Noblet J. The effect of energy and protein intake of sows on their longevity: a review. Livestock Prod Sci 1994;40: [11] Cosgrove JR, Foxcroft GR. Nutrition and reproduction in the pig: ovarian aetiology. Anim Reprod Sci 1996;42: [12] Whittemore CT. Nutrition reproduction interactions in primiparous sows. Livestock Prod Sci 1996;46: [13] Hughes PE. Effects of parity, season and boar contact on the reproductive performance of weaned sows. Livestock Prod Sci 1998;54: [14] Van den Brand H. Energy partitioning and reproduction in primiparous sows: effects of dietary energy source. PhD Thesis, Wageningen University, The Netherlands, 2000; 140 p. [15] Prunier A, Quesnel H. Nutritional influences on the hormonal control of reproduction in female pigs. Livestock Prod Sci 2000;63:1 16.

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