Overfeeding and underfeeding have detrimental effects on oocyte quality measured by in vitro fertilization and early embryonic development in sheep

doi:10.1016/j.domaniend.2012.05.001

Domestic Animal Endocrinology

Volume 43, Issue 4, November 2012, Pages 289-298

https://doi.org/10.1016/j.domaniend.2012.05.001 Get rights and content

Abstract

To determine effects of maternal diet on in vitro fertilization (IVF) and early embryonic development, ewes (n = 48) were divided into control, overfed (ad libitum feeding), and underfed (60% of control) nutritional planes for 8 wk before oocyte collection. Follicular development was induced by twice-daily injections of FSH on days 13 and 14 of the estrous cycle, and ovaries and blood samples were collected on day 15 of the estrous cycle. During the 8-wk experiment, for control ewes BW and BCS did not change, but for overfed ewes mean (± SEM) BW and BCS increased (11.8 ± 1.1 kg and 2.0 ± 0.1, respectively) and for underfed ewes decreased (14.2 ± 0.9 kg and 0.7 ± 0.1, respectively). The number of follicles was determined; oocytes were collected and subjected to in vitro maturation and fertilization. After IVF, developing embryos were evaluated throughout the 8-d culture period. The proportion of cleaved oocytes after IVF and developing morula and blastocyst were less (P < 0.0001) in overfed and underfed ewes than in control ewes. However, number of visible follicles, total number of oocytes, number of healthy oocytes, and percentage of healthy oocytes were similar for control, overfed, and underfed ewes. Serum insulin concentration was greater (P < 0.05) in overfed ewes than in underfed ewes, estradiol 17-β (E₂) concentration was greater (P < 0.05) in underfed ewes than in overfed ewes, but triiodothyronine (T₃) and thyroxine (T₄) concentrations were similar in all treatment groups. These data show that inadequate feeding has a negative effect on oocyte quality which results in lower oocyte cleavage after IVF and morula and blastocyst formation; overfeeding increased serum insulin and underfeeding increased serum E₂ but not T₃ or T₄. These data emphasize the importance of diet for reproductive and metabolic functions. Furthermore, the mechanisms through which enhanced or decreased energy in diet affect oocyte quality and serum insulin and E₂ concentrations remain to be elucidated.

Introduction

Reproductive function can be affected by numerous environmental factors, including nutrition that may affect hormone production, fertilization, embryonic development and survival, and pregnancy outcome in several species [1], [2], [3], [4], [5], [6], [7]. Nutritional status is a key factor that influences efficiency in assisted reproductive technologies (ARTs) [8], [9]. However, conflicting results have been reported for the effects of plane of nutrition on reproductive function in domestic ruminants. For example, positive, negative, or no effects of high- or low-energy diets on oocyte quality, fertilization rate, and early embryonic development have been reported for sheep and cows [10], [11], [12], [13], [14], [15], [16], [17].

It has been clearly found that oocyte quality is important for fertilization and embryogenesis [18], [19], [20], [21], [22]. In fact, oocyte quality profoundly affects early embryonic survival, maintenance of pregnancy, and fetal and postnatal development [23], [24], [25]. Thus, fetal programming likely starts during oocyte development [26], [27], [28].

Oocyte quality can be determined by its ability to be fertilized and develop into a healthy embryo, fetus, or offspring or by expression of specific markers. Numerous factors involved in the regulation of oocyte function and expressed in ovarian tissues, including oocytes, cumulus cells, or present in follicular fluid, have been identified as potential markers of oocyte quality, including gap junctional protein Cx43, FSH and LH receptors, leptin, progesterone receptor, members of the IGF system, glucose transporters, reactive oxygen species, and several other factors [18], [25], [29]. Having a reliable marker of oocyte quality would enhance ART through more accurate prediction of in vitro fertilization (IVF) rates and overall pregnancy outcome.

The effect of diet on hormones that regulate metabolic functions (eg, insulin, triiodothyronine [T₃], thyroxine [T₄]) or reproduction (eg, GnRH, FSH, LH, estradiol-17β [E₂], progesterone) in domestic ruminants has been reported in several studies [4], [6], [9], [30]. For example, enhanced concentrations of insulin were frequently observed in sheep or cows fed a high-energy diet [8], [31], [32]. However, the existing data about the effects of diet on peripheral hormone concentrations in ruminant species are frequently contradictory and relatively limited.

Assisted reproductive technologies have been applied in agriculture, veterinary, and human medicine for several decades [33], [34], [35]. Research directed toward improved quality of oocytes and embryo production systems has focused on numerous aspects of ART, including optimization of oocyte donor/recipient hormonal treatment, culture conditions, cryopreservation, and others [36], [37], [38], [39]. Several studies investigated also the effects of diet manipulation of donor ewes [40], [41], [42] and cows [31], [43], [44] on oocyte quality.

We hypothesized that inadequate nutrition (diet excess or restriction) will have negative effects on oocyte quality measured by the rates of IVF and early embryonic development and on peripheral concentration of selected metabolic hormones and E₂ in sheep. Therefore, the aim of the present study was to evaluate the effects of nutritional plane (control vs overfeeding or underfeeding) on follicular development, oocyte cleavage after IVF, morula and blastocyst formation, and plasma concentration of insulin, T₃, T₄, and E₂ in FSH-treated ewes.

Section snippets

Treatment of animals

All procedures were performed at the Animal Nutrition and Physiology Center of North Dakota State University located in Fargo, ND (approximately 46.5° latitude and −96.5° longitude) and were approved by the Institutional Animal Care and Use Committee of North Dakota State University. Western range (predominantly Targhee and Rambouillet) 2- to 3-yr-old ewes were standardized for live BW and BCS. Body condition score was determined with the use of a 5-point scale (1 = extremely thin and 5 =

Results

At the time treatment was initiated, BW was similar for control, overfed, and underfed ewes (59.4 ± 2.2 kg; Fig. 1A). At 2 to 8 wk of the experiment, BW of overfed ewes was greater (P < 0.0001) than for control or underfed ewes, and BW of underfed ewes was lower (P < 0.0001) than for control ewes (Fig. 1A). When compared with initial BW, control ewes maintained, overfed ewes gained 11.8 ± 1.1 kg (P < 0.0001) but underfed ewes lost 14.2 ± 0.9 kg (P < 0.0001) during the 8-wk experiment (Fig. 1A).

Discussion

The present study found that an 8-wk period of underfeeding and overfeeding had detrimental effects on oocyte quality measured by the proportion of cleaved oocytes after IVF and morula and blastocyst formation. In agreement, previous studies have reported decreased rates of IVF and/or early embryonic development in ewes fed low (nutrient restricted) or high (ad libitum intake) during the periconception period [15], [17], [41]. By contrast, others have shown that alteration of nutritional plane

Acknowledgments

This study was supported by ND SBARE grant for ATGB. We thank Dr David Buchanan for statistical consultation and Ms Tammi Neville, Mr James D. Kirsch, Mr Kim C. Kraft, Mr Robert Weigl, Mr Tim Johnson (deceased), Mr Terry Skunberg, and other members of our laboratory for their technical assistance.

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