J. Anim Sci. 2007. 85:1565-1576. doi:10.2527/jas.2006-743
© 2007 American Society of Animal Science
Effect of maternal dietary restriction during pregnancy on lamb carcass characteristics and muscle fiber composition1
Z. C. T. R. Daniel*,2,
J. M. Brameld*,
J. Craigon*,
N. D. Scollan
and
P. J. Buttery*
* Division of Nutritional Sciences, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire, LE12 5RD, UK; and
and
Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth, SY23 3EB, UK
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Abstract
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Two experiments were conducted to determine whether the decreased proportion of fast muscle fibers seen previously in 2-wk-old lambs from ewes that were dietary restricted from d 30 to 70 of gestation are still evident in older lambs and what the consequences may be in terms of growth rates and carcass composition. Throughout both experiments, ewes were fed on an individual basis according to the recommended dietary allowance throughout pregnancy relative to metabolic BW (BW0.73). Control groups were fed as above, and the treatment groups had their nutrient supply reduced to 50% of this recommended allowance from d 30 to 70 (Exp. 1) or d 30 to 85 (Exp. 2) of gestation, after which they were returned to the same level of nutrition as the control group. All twin lambs were kept with their dams, and at 2 wk were given access to creep. After weaning, lambs were individually housed and fed ad libitum to 24 or 17 wk of age for Exp. 1 and 2, respectively. Although not significant (P = 0.18), growth to 24 wk (Exp. 1) resulted in a small decrease in the protein content and therefore an increase in the fat:lean ratio in the carcass of lambs subjected to maternal dietary restriction. This was not apparent when animals were slaughtered at 17 wk (Exp. 2; P > 0.68). Few significant effects of maternal dietary restriction on the fiber type composition of muscles were observed. In Exp. 1 the number of fast fibers increased (P < 0.008) with no effect on slow fiber number in LM. In Exp. 2 an increase in the total number of fibers in male lambs and an increase in type II (A and B) fibers in female lambs were observed in the LM, and an increase in IIB fiber number was observed in semitendinosus (ST) muscle from male lambs. Prenatal maternal dietary restriction during the time of muscle differentiation demonstrated an increase in type IIB muscle fibers and increase in intramuscular fat; although significant, effects on subsequent carcass quality of lambs were relatively small. These data suggest that the lambs adapted to changes in muscle fiber composition previously observed at 2 wk. However, lambs in this study were well fed during postnatal growth. Whether offspring would still have been able to compensate if they had received poor nutrition postnatally and whether that failure to compensate would have influenced carcass composition remain to be determined.
Key Words: carcass composition • maternal nutrition • muscle fiber characteristic • sheep
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INTRODUCTION
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Evidence suggests that maternal nutrient intake at specific periods during pregnancy can influence subsequent development of the offspring (Wu et al., 2006
). For example, the number of muscle fibers in the adult is set in utero, and maternal dietary restriction can decrease the number of fibers formed, which tends to be associated with decreased growth rates and increased adiposity (Hegarty and Allen, 1978). By monitoring myogenin and various growth factors in developing sheep muscle, we previously demonstrated that the majority of muscle differentiation and fiber formation takes place at approximately d 85 of gestation, with myoblast proliferation occurring before this time (Fahey et al., 2005a). In a second study (Fahey et al., 2005b), maternal nutrient restriction during the proliferation stage immediately before the period of major fiber formation (d 30 to 70 of gestation) resulted in an increased proportion of slow fibers (predominantly derived from primary fibers) and a decreased proportion of fast fibers (predominantly secondary fibers) in 14-d-old lambs. The reduced proportion of fast fibers was associated with increased fast fiber diameters (Fahey et al., 2005b), indicating a reduction in the numbers of fast fibers formed in the young lambs, which is a consistent finding in the literature for most species. Maternal dietary restriction during (d 55 to 95) and after (d 85 to 115) major fiber formation did not alter muscle fiber characteristics of 14-d-old lambs (Fahey et al., 2005b). These studies determined a sensitive period of gestation and demonstrated effects of maternal dietary restriction on muscle fiber characteristics at an early age.
The aim of the current studies was to investigate whether such changes in muscle fiber characteristics persist into adulthood and what the consequences may be in terms of growth rates and carcass composition. We hypothesized that maternal nutrient restriction during pregnancy would result in a reduction in the numbers of muscle fibers in the resulting lambs and therefore lead to reduced lean growth but increased adiposity.
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MATERIALS AND METHODS
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Animals
Animal experiments were conducted in accordance with the UK Animals (Scientific Procedures) Act 1986 and performed within the normal seasonal breeding cycle of the ewe (September to March in the United Kingdom).
Experiment 1.
Experiment 1 aimed to determine whether the changes in muscle fiber development seen in 2-wk-old lambs from ewes undernourished from d 30 to 70 of gestation (Fahey et al., 2005b) are still evident in older animals. Estrus was synchronized in 100 Swaledale x Leicester Blue Face ewes by the withdrawal of synthetic progesterone-impregnated sponges (30 mg of cronolone-flugestone acetate per sponge; Chronogest; Intervet UK Ltd., Cambridge, UK) 12 d after their insertion. Forty-eight hours later, the ewes were introduced to Charolais rams, and mating was monitored using raddle markings to determine d 0 of gestation.
At 24 d of gestation, ewes were individually housed and fed a pelleted diet consisting of (as-fed basis) soybean meal (127 g/kg of straw nuts), straw nuts, and vitamins and minerals (Frank Wright Ltd., Ashbourne, Derbyshire, UK) with 1% of the total diet being vegetable oil. Throughout both experiments, the ewes were fed on an individual basis according to the recommended dietary allowance throughout pregnancy [relative to metabolic BW (BW0.73); AFRC, 1993]. The quantity of diet given to the ewes throughout the trials was always a proportion of the daily requirement to support the ewe and allow for conceptus growth and supplied 8.6 MJ/d until d 90 of gestation from which point the intakes were increased by the gradual addition of barley so that by term the ewes received 14.5 MJ/d. Ewes were weighed twice weekly and fed daily in 2 equal rations at 0800 and 1600, with the ration adjusted according to BW. Ewes were weighed and randomly allocated to treatment groups to begin dietary manipulation from d 30. The control group was fed as above, and the treatment group had their nutrient supply reduced to 50% of this recommended allowance from d 30 to 70 of gestation, after which they were returned to the same level of nutrition as the control group. Diet changes were imposed immediately. The quantity of vitamins and minerals was kept constant throughout, even during restriction, so that any effects were not due to vitamin or mineral deficiencies. Ewes were scanned ultrasonically (Oviscan-4 with a 3.5 MHz probe, BCF Technology, Livingston, UK) at d 32 and 40 after mating, and those confirmed as carrying twins (16 control and 20 restricted ewes; 36% of the total number of animals) continued on the experiment.
After parturition, the lactating ewes were fed a pelleted diet containing (per kg, as-fed basis), 450 g of barley, 200 g of oats, 200 g of soya, 100 g of molassed feed meal, 25 g of mineral and vitamin mix (Frank Wright Ltd., Ashbourne, Derbyshire, UK), 10 g of calcine magnesite, 8 g of dicalcium phosphate, and 7 g of limestone. All surviving twin lambs (28 control and 39 restricted lambs; all males kept intact) were kept with their dams and at 2 wk were given access to creep containing (per kg, as-fed basis) 485 g of barley, 270 g of soya, 150 g of nutritionally improved straw, 50 g of molassed feed meal, 25 g of mineral and vitamin mix (Frank Wright Limited), and 10 g of limestone). At 8 wk after birth, the remaining lambs (26 control and 37 restricted; control female, n = 11; restricted female, n = 25; control male, n = 15; and restricted male, n = 12) were housed in sibling pairs, with access to creep, and were introduced to a concentrate diet fed to appetite. From 12 wk, the lambs were individually housed and fed ad libitum to 24 wk, with feed intake being measured. Ultrasound scanning (Sonovet SA600V with a Kretz Technic 3D Ultrasound Veterin 7.5 MHz probe, BCF Technology) was used to monitor muscle and back-fat depth at the second from the last rib.
At slaughter (24 wk), muscle samples [LM, semitendinosus (ST), and vastus lateralis (VL)] were rapidly removed from the left side of the carcass, snap-frozen in liquid nitrogen-cooled isopentane, and stored at –80°C for determination of muscle fiber characteristics. Samples of subcutaneous (tail fat), perirenal, and omental adipose tissue were also rapidly removed from the left side of the carcass, frozen quickly in liquid nitrogen, and stored at –80°C for determination of adipocyte size. Fresh weights of the 3 muscles, perirenal and omental adipose tissue, and various other organs were also recorded. The carcass was skinned, weight of the cold carcass was recorded, and the carcass was split in half and cut vertically through the flank to the anterior edge of the last rib, thus dividing it into 4 portions. The curve of the ribs was followed to the vertebral column, which was severed at the junction of the 12th and 13th thoracic vertebrae. The following measurements were recorded from the anterior surface of this cross-section: width of the LM (maximum distance from the end adjacent to the spinal process, lateral along the rib), depth of the LM (longest distance, perpendicular, on same surface), and thickness of backfat over the deepest part of the LM. The intact right side of the carcass was placed in a bag and stored at –20°C before being allowed to partially defrost and then minced using a Wolfking mincer (Slagelse, Denmark), once through a 13-mm screen and then twice through a 4-mm screen. A sample was taken and, along with samples from the 3 dissected muscles, was frozen at –40°C before freeze-drying in preparation for determination of DM, fat (Soxhlet), and protein (Kjeldahl) contents.
Experiment 2.
In light of data obtained from Exp. 1, the length of the feed restriction period for Exp. 2 was increased from 40 to 55 d to more fully cover the sensitive period during gestation when muscle fibers are being formed (see Fahey et al., 2005a,b). The age at slaughter was also reduced to 17 wk due to the animals in Exp. 1 being overly fat at 24 wk. Hence, Exp. 2 was conducted as described for Exp. 1 (above), with the following modifications. The ewes in the treatment group had their nutrient supply reduced to 50% of the recommended allowance from d 30 to 85 of gestation. After ultrasound scanning, 24 control and 21 restricted ewes were confirmed as carrying twins. All surviving twin lambs (41 control and 39 restricted lambs) were kept with their dams before being housed in sibling pairs at 10 wk (26 control and 26 restricted; control female, n = 13; restricted female, n = 12; control male, n = 13; and restricted male, n = 14) and individually housed at 12 wk. They were fed ad libitum to 17 wk of age (a more conventional slaughter weight in the United Kingdom), when they were slaughtered and their carcass characteristics were determined as for Exp. 1.
Determination of Adipocyte Diameter
Adipocyte diameter was determined using the method of Pond et al. (1984). Five cross-sections of <1 mm in thickness of adipose tissue were placed in a drop of PBS on a microscope slide, and the cover slip was pressed down lightly to flatten the tissue, which was then examined under a microscope linked to an image capture system (Image-Pro Plus, Media Cybernetics, UK). Diameters of 100 individual, intact adipocytes were measured and used to determine an average adipocyte diameter for each sample.
Histochemical Determination of Muscle Fiber Type Composition
For each muscle, transverse serial tissue sections, 10 µM thick, were cut using a cryostat. For Exp. 1, different fiber types within a muscle were determined using ATPase and oxidative staining methods. The ATPase method was based on that of Wegner et al. (2000), in which sections were reacted for actomyosin Ca2+ adenosine triphosphatase stability after alkaline preincubation at pH 10.4 and then stained with Azure II. Fibers were classified as negative (white, type I, slow) or positive (blue, type II, fast). The oxidative staining method was NADH-tetrazolium reductase (NADH-TR) staining, as described by Brumback and Leach (1984), which distinguished between oxidative (positively stained) and nonoxidative (glycolytic, no staining) fibers. The histochemical detection of ATPase activity provides only the changes in the proportion of slow- and fast-twitch fibers, and the NADH-TR method can demonstrate only the alteration in oxidative capacity. Therefore, for Exp. 2, reactions for the NADH-tetrazolium reductase (Novikoff et al., 1961) and the acid-preincubated ATPase at pH 4.2 (Guth and Samaha, 1970) were combined according to Horak (1983) because this allowed the simultaneous evaluation of the ATPase activity and oxidative capacity of the muscle fibers from a single section. In this combined staining method, fibers stained dark are classified as type I, intermediate as type IIA, and light as type IIB.
For both experiments, the serial sections were viewed on a light microscope linked to an image capture system, and 4 areas were selected randomly for each animal and the numbers of fibers of each type within a known area were counted. The diameter of individual muscle fibers was measured from approximately 25 fibers of each fiber type from each area counted. To minimize any errors associated with any irregular fibers or those that may not have been cut at right angles to the cutting blade, diameters were taken as the smallest diameter across the fiber.
Statistical Analysis
For both experiments, ewes (the experimental unit) were randomly allocated to control or restricted diets. The effect of maternal dietary restriction on carcass parameters was analyzed as a 2-way, linear, factorial mixed model using the REML tool in Genstat (Release 8.1, Lawes Agricultural Trust, Rothamsted Experimental Station, UK), with treatment and sex as fixed effect factors and ewe and lamb as random effect factors. For analysis of the number and diameter of muscle fibers, a 3-way model was used, with treatment, sex, and fiber type as fixed factors and ewe and lamb as random factors. Residuals from all analyses were examined to confirm their normality. Statistical significance was taken as P < 0.10.
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RESULTS
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Experiment 1
Animal Performance and Carcass Characteristics.
This experiment involved maternal dietary restriction between d 30 and 70 of gestation and growing the resulting lambs to 24 wk. The level of maternal nutrition did not appear to affect lamb birth weight, but the expected sex effect was observed with male lambs being heavier (P < 0.001; Table 1). There was, however, an effect (P = 0.02) of maternal nutrition on final slaughter weight with lambs from restricted ewes being lighter than those from control animals, regardless of sex. As expected, male lambs were heavier (P < 0.001) than females at slaughter. Statistical analyses of the data showed strong effects (P < 0.01) of sex on the whole weights of the heart, kidney, liver, and lungs with male lambs having greater weights compared with female lambs. There were also several effects of maternal restriction on the carcass parameters studied, with maternal nutrient restriction resulting in lower (P < 0.05) liver, heart, and lung weights. However, expressing the data on a % BW basis removed most of these differences, but there was an interaction (P = 0.045) between maternal dietary restriction and sex of the lamb on heart weights, which were decreased in male lambs and increased in female lambs with restriction, when expressed on a BW basis.
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Table 1. Effect of maternal dietary restriction from d 30 to 70 of gestation on growth and carcass composition of lambs grown to 24 wk (Exp. 1)
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Maternal dietary restriction did not alter the carcass composition of these lambs (Table 1
), but male lambs had more protein (P = 0.04) than the females. As expected, males had the greater growth rates (P < 0.001), ate more (P < 0.001), and had a greater feed conversion efficiency (P = 0.08) than female lambs. Maternal dietary restriction resulted in slower growing lambs (P = 0.009).
Lambs from restricted mothers had reduced (P < 0.04) whole muscle weights for LM and VL shown in Table 2. With the data expressed on a % BW basis, there was an indication that interactions existed between maternal nutrition and sex of the lamb because dietary restriction reduced weights in male lambs and increased their weights in female lambs for LM (P = 0.03 for treatment x sex interaction) and VL (P = 0.10) for treatment x sex interaction). In the ST muscles, maternal dietary restriction resulted in increased (P = 0.05) fat content in all lambs, whereas in the LM muscles the same effect was observed but only in males (P = 0.08 for treatment x sex interaction). The changes in fat content did not appear related to changes in protein content.
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Table 2. Effect of maternal dietary restriction from d 30 to 70 of gestation on size and composition of muscle of lambs grown to 24 wk (Exp. 1)
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As expected, female lambs had greater (P = 0.04) backfat depth and more (P < 0.02) omental and perirenal (g/kg of BW; Table 3) adipose tissue than male lambs. Female lambs also had greater (P < 0.04) omental and perirenal adipocyte diameters. In the perirenal adipose tissue there was an effect of maternal nutrition, with lambs from restricted mothers having increased (P = 0.04) adipocyte diameters. Ultrasound monitoring showed no effect of treatment on the rate of fat or muscle deposition but demonstrated clear differences in fat and muscle deposition from 8 to 24 wk of age. Muscle depth increased gradually, whereas fat depth remained minimal until approximately 15 wk, after which the fat was deposited rapidly until slaughter (data not shown) at which point its depth had reached a plateau in the majority of animals.
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Table 3. Effect of maternal dietary restriction from d 30 to 70 of gestation on the characteristics of adipose tissue depots of lambs grown to 24 wk (Exp. 1)
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Muscle Fiber Type Composition.
As expected, the ATPase staining showed that all 3 muscles had more (P < 0.001) fast fibers than slow and that fast fibers had a larger (P < 0.001) diameter than slow fibers as shown in Figure 1. In samples of LM, a treatment x fiber type (P = 0.003) interaction was observed because maternal dietary restriction resulted in an increased number of fast fibers, regardless of sex, with no effects on numbers of slow fibers. Also, a sex x type (P = 0.008) effect was noted in the LM because the slow fibers were smaller in female lambs only. A sex x type (P = 0.007) effect was also observed in the ST because female lambs had more fast type with no difference in the slow type fiber composition between the 2 sexes. No effects of maternal nutrition on measures of muscle fiber type, as determined by ATPase staining, were noted in the ST or VL samples. The LD, ST, and VL had more (P < 0.001) glycolytic (nonoxidative) fibers than oxidative fibers, and these glycolytic (nonoxidative) fibers had the greater diameters (P < 0.001), as determined by NADH-TR histochemistry (Figure 2). A treatment x type interaction was observed in ST muscle because there was a small but significant (P = 0.04) decrease in the diameter of oxidative fibers in lambs from dietary restricted mothers, with no treatment effect on glycolytic fiber diameters. In the ST and VL muscles, female lambs had more (P < 0.07) glycolytic fibers with no difference in the number of oxidative fibers between the 2 sexes. The only other effect of maternal nutrition was that lambs from restricted mothers had smaller (P = 0.080) fiber diameters in the VL muscle, regardless of type and sex.
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Figure 1. Effect of maternal dietary restriction from d 30 to 70 of gestation on the number and size of slow and fast fibers in ovine LM (a, b), and semitendinosus (ST; c, d), and vastus lateralis (VL; e, f) muscles of the resulting offspring as determined by ATPase staining. CF = control female, n = 11; RF = restricted female, n = 25; CM = control male, n = 15; and RM = restricted male, n = 12. The single error bar represents the SED for the treatment x sex x type interaction.
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Figure 2. Effect of maternal dietary restriction from d 30 to 70 of gestation on the number and size of oxidative and glycolytic fibers in ovine LM (a, b), and semitendinosus (ST; c, d), and vastus lateralis (VL; e, f) muscles of the subsequent offspring as determined by NADH-tetrazolium reductase staining. CF = control female, n = 13; RF = restricted female, n = 12; CM = control male, n = 13; and RM = restricted male, n = 14. The single error bar represents the SED for the treatment x sex x type interaction.
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Experiment 2
Animal Performance and Carcass Characteristics.
This experiment involved maternal dietary restriction between d 30 and 85 of gestation and growing the resulting lambs to 17 wk. The level of maternal nutrition did not appear to affect lamb birth weight or slaughter weight; however, the expected sex effect on final weight was observed, with male lambs being heavier (P < 0.001, Table 4). Consistent with the previous experiment, strong effects (P < 0.001) of sex on the weights of heart, kidney, liver, and lungs were noted with male lambs having greater weights than did female lambs. However, the only significant effect of maternal restriction was in the kidneys, where maternal nutrient restriction resulted in greater kidney weights (P = 0.08). Expressing the data on a % BW basis removed most of the sex differences, but males still had larger (P = 0.03) hearts than females. Unlike the previous experiment, there were no effects of maternal nutrition on whole body or tissue weights relative to BW.
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Table 4. Effect of maternal dietary restriction from d 30 to 85 of gestation on growth and carcass composition of lambs grown to 17 wk (Exp. 2)
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Although no effects of maternal nutrition were detected in any of the half carcass composition parameters measured, female lambs contained a greater (P < 0.001) proportion of fat and less (P < 0.001) water and protein than the male lambs. As expected, males had greater growth rates (P < 0.001), ate more (P = 0.003), and had a greater feed conversion efficiency (P = 0.002) than female lambs. However, unlike the previous experiment, no effects of maternal dietary restriction were observed.
Male lambs had greater (P = 0.02) whole muscle weights for LM, ST, and VL (Table 5). When the data was expressed on a % BW basis, this pattern seemed to be reversed with females having greater (P = 0.09) LM muscles than the male lambs. However, there were no differences between male and female lambs in weights of ST and VL. The ST muscles from female lambs contained less water (P = 0.01) than from male lambs, but there was no difference in water content in the other 2 muscles. Maternal dietary restriction resulted in increased fat content in LM muscles of male lambs and decreased fat content in the LM muscles of female lambs (P = 0.05 for treatment x sex interaction). There were no effects of treatment or sex on the ST and VL muscles. The protein content of the 3 muscles studied appeared to be unaffected by maternal nutrition.
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Table 5. Effect of maternal dietary restriction from d 30 to 85 of gestation on size and composition of muscle from lambs grown to 17 wk (Exp. 2)
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As expected, female lambs had greater (P = 0.05) backfat depth and more (P < 0.02) omental and perirenal (when expressed on g and g/kg of BW basis) adipose tissue than male lambs (Table 6). Female lambs also had larger (P < 0.002) subcutaneous, omental, and perirenal adipocyte diameters. As with the previous experiment, the ultrasound monitoring (from 10 wk) showed that muscle depth increased gradually, whereas fat depth remained minimal until approximately 14 wk, after which the fat was deposited rapidly until slaughter at 17 wk (data not shown). But this time, in the majority of animals, the backfat depth had not reached a plateau.
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Table 6. Effect of maternal dietary restriction from d 30 to 85 of gestation on the characteristics of adipose tissue depots from lambs grown to 17 wk (Exp. 2)
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Muscle Fiber Type Composition.
The combined AT-Pase/NADH-TR staining method allowed classification of muscle fibers into types I, IIA, and IIB (Figure 3). In all 3 muscles studied, type IIB fibers were in the majority (P < 0.001) and had the largest diameters (P < 0.001). In the LM, a treatment x sex interaction (P = 0.003) was observed, with maternal dietary restriction resulting in an increase in the number of fibers (I, IIA, and IIB) in male lambs only. This may be due to the decreased fiber diameter observed in the restricted male lambs (P = 0.08). Statistical analysis indicated a treatment x sex x type interaction in the ST muscle, with maternal dietary restriction resulting in an increase in the number of IIA and IIB fibers in female lambs, but there was only an increase in the number of IIB fibers in the restricted male lambs. There were no effects of maternal nutrition on ST fiber diameters nor on any muscle fiber characteristics measured in the VL.
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Figure 3. Effect of maternal dietary restriction from d 30 to 85 of gestation on the number and size of type I, IIA, and IIB fibers in ovine LM (a, b), and semitendinosus (ST; c, d), and vastus lateralis (VL; e, f) muscles of the subsequent offspring as determined by combined ATPase/NADH-tetrazolium reductase staining. CF = control female, n = 13; RF = restricted female, n = 12; CM = control male, n = 13; and RM = restricted male, n = 14. The single error bar represents the SED for the treatment x sex x type interaction.
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DISCUSSION
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This study investigated whether maternal nutrient restriction of ewes before muscle fiber formation would alter the muscle and carcass characteristics of the resulting offspring. Russel et al. (1977) demonstrated reductions in birth weights of lambs from ewes that had been severely undernourished during the last 6 wk of pregnancy. Studies in pigs (Bee, 2004) found that neither nutrient restriction nor increased energy intake during the first 50 d of gestation affected birth weights of resulting piglets. Similarly, birth weight was not affected by maternal nutrition in these studies or in our previous studies where ewes were restricted during early-mid gestation (d 30 to 70; Fahey et al., 2005b). This indicates the importance of the timing of any maternal dietary restriction on subsequent lamb birth weights, with late gestation being particularly important. Additive effects of prenatal and postnatal dietary restriction on growth and adult size have previously been shown (Schinckel and Short, 1961; Gunn, 1977), which implies that the postnatal period may be more sensitive to alterations in nutrition or that interactions between pre- and postnatal environment may occur.
Consistent with the findings of Sibbald and Davidson (1998), no effect of maternal dietary restriction on feed intake was observed in these studies. However, lambs from d 30 to 70 dietary restricted ewes (Exp. 1) grew more slowly and were therefore lighter at slaughter (at 24 wk) than those from well-nourished ewes. This finding agrees with previous work by Nordby et al. (1987) in which lambs from ewes restricted to 70% from d 30 before breeding and the first 100 d of gestation took several days longer to reach the required slaughter weight. Greenwood et al. (2000) also suggested that permanent impairment of lean growth potential of sheep may be imparted by dietary restriction during pregnancy. Reduced growth rates have previously been described in pigs from sows whose intake had been restricted during gestation (Pond et al., 1985; Pond and Mersmann, 1988), and a study by Gondret et al. (2006) reported low birth weight pigs took 12 d longer to reach 112 kg of BW than high birth weight pigs. However, in Exp. 2 the slaughter weights did not differ when lambs were grown to 17 wk following maternal dietary restriction between d 30 to 85 of gestation. This is consistent with the findings of Krausgrill et al. (1999) who showed that lambs from dams restricted from mating to d 70 gestation reached their target slaughter weight (35 kg) no later than those from control ewes. Indeed, even though lambs from ewes which had been severely undernourished in early pregnancy (<d 90) were growth retarded at birth and weaning, this effect was progressively diminished with time and became negligible by 7 mo of age (Everitt, 1968). Together these data suggest that the timing of the nutritional insult and the age or weight of follow-up study may be important in terms of effects being studied. Certainly, the timing and duration of dietary restriction seem to be important factors in determining permanency and extent of reduced body size.
The lighter LM and VL muscles observed here in male lambs from d 30 to 70 restricted dams compared with male controls is consistent with the findings of Krausgrill et al. (1999). However, the opposite observation that these 2 muscles were in fact heavier in female lambs from d 30 to 70 restricted mothers is in keeping with the work of Nordby et al. (1987), who showed that feeding ewes 70% for the first 100 d of gestation resulted in lambs with heavier ST muscle weights than in lambs from adequately fed ewes, although no effect of sex was observed. Unfortunately, the Krausgrill et al. (1999) study did not state the sex of the lambs they studied. This suggests that there may be complex interactions involving the sex of the offspring, as well as the specific timing, the degree of nutrient restriction, or both, that impact upon any compensatory growth that may occur to overcome previous diet restriction.
Contrary to our original hypothesis, maternal dietary restriction did not alter the lean content of the lambs, but a few differences were observed in the various measures of fatness. For example, adipocyte diameters were enlarged in perirenal adipose tissue from lambs restricted during d 30 to 70 of gestation and then grown to 24 wk (Exp. 1). This finding agrees with a similar study comparing low and high birth weight pigs subsequently grown to 112 kg of BW (Gondret et al., 2006), where differences in carcass fatness, adipocyte diameter, and backfat were also observed. Similarly, both periods of maternal dietary restriction resulted in an increased fat content in LM from male lambs, which again agrees with previous studies in pigs showing increased muscle fat content in low birth weight compared with high birth weight piglets (Poore and Fowden, 2004; Gondret et al., 2006). Similar effects were also observed in the ST muscle, but only after the 40-d restriction period (Exp. 1), but no effects were observed in VL muscle in either experiment. This finding agrees with the previous suggestion that not all muscles are equally affected by variation in prenatal nutrition (Greenwood et al., 2000), presumably because they develop at different times of gestation. These changes in muscle fat content did not appear to be related to changes in protein content, which is supported by Nordby et al. (1987) who showed maternal dietary restriction for the first 100 d of gestation had no effect on protein content of ST samples from the subsequent lambs at 56-kg slaughter weight. Together the carcass and muscle data indicate that nutritional stress imposed on ewes during early-mid pregnancy appears to have no adverse effect on the carcass composition of the subsequent offspring, unless the lambs are allowed to grow to greater than conventional slaughter weights.
Severe maternal dietary restriction from the commencement of gestation (Swatland and Cassens, 1973) or during early-mid and late pregnancy (Everitt, 1968) has been shown to reduce myofiber number in fetal lambs. Zhu et al. (2004) showed fewer secondary myofibers in muscle from fetus (78 d) from ewes restricted during d 28 to 78 gestation compared with controls. We previously showed (Fahey et al., 2005b) that maternal dietary restriction during (d 55 to 95) and after (d 85 to 115) major fiber formation did not alter the muscle fiber characteristics of 14-d lambs. However, restricted maternal nutrition before muscle fiber formation (d 30 to 70) did alter the muscle fiber composition of the neonatal lambs by reducing the number of fast fibers in both the LM and VL muscles. Similarly, Bee (2004) demonstrated that oxidative capacity was increased and numbers of IIB fibers reduced in the ST from piglets that had experienced low energy intake during the first 50 d of gestation, compared with progeny from sows receiving a high energy supply. This current study was therefore designed to investigate whether these changes in muscle fiber characteristics observed in young animals persisted into adulthood. As expected from studies in adult cattle and sheep (Manabe et al., 1988; Wegner et al., 2000; Peinado et al., 2004), in all 3 muscles studied, there were more fast fibers than slow and more glycolytic (nonoxidative) than oxidative fibers, with the fast and glycolytic fibers also being bigger, which suggests more fast glycolytic or type IIB fibers. In both experiments, dietary restriction during early-mid gestation resulted in increased numbers of fast fibers in the resulting offspring; maternal dietary restriction during d 30 to 70 of gestation increased the number of fast fibers in LM from both sexes, and during d 30 to 85 increased IIA and IIB fibers in female lambs and IIB fibers from male lambs in ST. This finding is supported by Zhu et al. (2006) who saw a similar increase in IIB myofibers in lambs from ewes that had also been subjected to dietary restriction during early (d 28 to 78) gestation. Interestingly, previous work from our laboratory (Fahey et al., 2005b) and Zhu et al. (2004) showed reductions in type II fibers in 2 wk and fetal lambs, respectively, from ewes undernourished during the same time point in early gestation. These changes noted in the adult offspring suggest the animals have somehow managed to compensate for effects of maternal dietary restriction on fiber composition noted in early life. Krausgrill et al. (1999) found that although muscle fiber cross-sectional areas were larger in d 70 fetus from nutrient-restricted dams, such differences were not evident in d-140 fetus or 35-kg lambs, and no effects on the percentage of muscle fiber types were noted at any of the ages studied. Nordby et al. (1987) also reported that moderate dietary restriction of ewes during early pregnancy did not affect muscle fiber type composition of their offspring at 58.5-kg slaughter weight. It therefore seems that age and BW of the offspring affect the magnitude of fiber type alteration observed as a result of maternal dietary restriction in sheep. Together these studies support the findings reported here, that reduced feeding of ewes during early-mid gestation may have short-term effects on muscle development, but that, given good postnatal nutrition, lambs are able to compensate for the changes, resulting in little or no detrimental effects on the carcass or muscle fiber characteristics in adulthood. However, whether this compensation might be compromised by postnatal exposure to other metabolic stresses (e.g., reduced nutrition or a high fat diet) remains to be established.
At conventional slaughter weights (
44 kg), there was no effect of prenatal dietary restriction during the time of muscle differentiation on the subsequent carcass quality of the adult lambs. Allowing the lambs to grow for longer (55 kg) showed evidence of an alteration in fat:lean ratio. This would suggest limited implications for agriculture but may be of more relevance to other species, particularly humans.
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Footnotes
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1 These studies were funded by the Department for Environment, Food and Rural Affairs (DEFRA). The authors wish to acknowledge Charlotte Rehfeldt for providing us with the combined NADH-TR/ ATPase method. 
2 Corresponding author: zoe.daniel{at}nottingham.ac.uk
Received for publication November 10, 2006.
Accepted for publication January 29, 2007.
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Abstract
INTRODUCTION
