Under nutrition in the ewe: Foeto-placental adaptation, and modulation of lamb birth weight: A review

Concentrations of maternal blood metabolites as indicators of nutritional status during pregnancy

Changes in maternal body condition and weight gain during pregnancy may not represent a good measure of the adequacy of foetal nutrition given that greater maternal growth rate and fat deposition can occur due to skewed nutrient partitioning in favour of maternal tissues at the expense of the gravid uterus as commonly observed in adolescent ewes (Wallace et al 2002; 2004; Addah et al 2007; Addah and Karikari 2008). The concentrations of blood metabolites during pregnancy therefore offer a better means of assessing the nutritional status of the ewe than changes in weight gain per se. The chemical composition of blood is often under homeostatic control. Variations in its composition are therefore often maintained within narrow limits (O`Doherty and Crosby 1998). However several factors operate against this equilibrium and when such factors become severe, homeostatic mechanisms are unable to adequately maintain this balance and deviations from the normal concentrations occur. A more immediate assessment of the adequacy of foeto–maternal nutrition is afforded by the measurement of some maternal blood metabolites (Russel 1984).  

Several maternal blood constituents have been used as indices of maternal nutritional adequacy or under–nutrition in the WAD sheep (Adu and Olalou 1979; Tuah and Klusey 1992; Addah and Karikari 2008) and other breeds (Russel 1984; Schloesser et al 1993; O`Doherty and Crosby 1998; O`Callaghan and Boland 1999) but there seems to be no general agreement on the stage of pregnancy at which the concentration of one or more of these is most critical to the growth of the conceptus (Robinson et al 1999). This could be due to the confounding effects of factors such as type of species, age, parity, utero–placental morphology and maternal reserves or body condition of experimental subjects used among studies (McCrabb et al 1991).  

The metabolite most suitable for assessing the adequacy of nutrition may also vary depending on the stage of pregnancy. The metabolites which have been identified as indices of nutritional adequacy in pregnant ewes include glucose and total protein (Adu and Olaloku 1979; Robinson et al1999; Tuah and Klusey 1992), lactate (Bell and Bauman 1997; Bauer et al 1998), ammonia and urea (Tuah and Klusey 1992; Schlosser et al 1993; O`Doherty and Crosby 1998; O`Callaghan and Boland 1999), and ketone bodies (acetoacetic acid, β–hydroxybutyric acid and acetone; Adu and Olaloku 1979; Russel 1984; O`Doherty and Crosby 1998; Schlosser et al 1993). However those that contribute substantially to the energy and protein requirements of ruminant foetuses are glucose and lactate, and amino acids respectively. Glucose and oxygen are the primary substrates for foetal growth (Owens 1991). In order of importance, the foetus in the third trimester of gestation derives approximately 50%, 20–40% and 10–30% of its total energy requirements from glucose, lactate and amino acids, respectively (Bauer et al 1998). Blood glucose concentration therefore offers a direct measure of the energy that is readily available to the foetus. However compared to glucose, plasma 3-hydroxybutyrate, has been identified as the most reliable indicator of nutritional status during pregnancy. This is because its concentration does not subject to much variability due to extraneous conditions such as the stress of animal handling and blood sampling (Russel 1984).  

Tuah and Klusey (1992) found plasma glucose concentration of non–pregnant WAD ewes to be 50% lower than in pregnant ewes, and attributed this to heavy demands of the foetus on the maternal glucose pool during pregnancy. Using the same breed, Adu and Olaloku (1979) found higher plasma glucose concentration for ewes receiving adequate nutrition (527–538 mg/L) and lower concentration (384 mg/L) for moderately malnourished ewes during the last 7 weeks of gestation. In adolescent ewes, plasma glucose was lower in moderate– compared to high–intake ewes during the three trimesters of pregnancy after 2.5 h of feeding (Wallace et al 1999).  

Total plasma protein concentration has also been shown not to differ between pregnant (4^th and 5^th month) and non–pregnant WAD ewes (Tuah and Klusey 1992) but Schloesser et al (1993) reported an 11.5% decrease in mean plasma protein concentration between early pregnancy and mid pregnancy when ewes were supplemented with varying levels of soya bean meal.  

Short–chain fatty acids are poorly transported across the placenta in sheep. This is because while placental glucose and lactate are transported by facilitated diffusion and therefore their concentrations in foetal blood are not entirely dependant on maternal–foetal plasma concentrations, maternal acetate is presumably transported by passive diffusion and makes only a minor contribution to foetal metabolism (Brockman 1993). Compared to ATP yield from glucose, acetate contributes less than 2% of ATP to a 19-day embryo and is not metabolized by embryos at the very early stage of cleavage (Robinson and Symounds 1995). In hyperketonaemic ewes, ketones are poorly transported across the placenta while amino acids are transported from maternal blood to placenta by active transport but are subsequently transported to the foetus by passive transport (Brockman 1993). Little is known about the contribution of free fatty acids to foetal metabolism but high foetal fat in some species suggest that our understanding of the contribution of free fatty acids to foetal energy metabolism is constrained by methodological limitations rather than its actual contribution to foetal metabolism (Owens 1991). 

The transport of calcium across the placenta to the foetus is endocrinologically regulated by the foetal parathyroid gland through the secretion of parathyroid hormone and a parathyroid hormone–like protein that may maintain higher calcium levels in the foetus relative to maternal calcium concentration (Loveridge et al 1988). The foetal skeleton is the main sink for maternal calcium and maternal calcium has been used to estimate foetal growth during pregnancy (McCrabb et al 1991). Deficiency of cobalt during the first trimester of pregnancy may also result in reduced lamb vigour and regression in the acquisition of passive immunity since lambs are unable to stand on their feet to suckle the needed colostrum after birth. This “programmed” negative effect is not reversed even when the deficiency is corrected in later trimesters (Robinson et al 1999). Selenium and vitamin E deficiencies are also associated with embryo mortalities and reduction in birth weight.

Plasma albumins are very important in gestation and their concentration generally decreases particularly in the last week of pregnancy (O’Doherty and Crosby 1998). 

α-foetoglobulins found in foetal plasma and amniotic fluid is also a major binding site for fatty acids, tryptophan, Ca²⁺ and  steroid hormones. β–globulins contain transferin which binds and transports Cu²⁺, Zn²⁺ and Fe²⁺. This makes maternal globulins very important during pregnancy. In pregnant WAD sheep, maternal plasma globulins concentration was lower for ewes whose intake was restricted throughout pregnancy compared to those restricted in only the first or second trimesters but was higher than in ewes restricted in third trimester or non–restricted throughout pregnancy (Addah and Karikari 2008). O’Doherty and Crosby (1998) found progressive decline in concentration of serum globulins as pregnancy advanced.

The role of IGF-II in controlling foetal growth is largely undisputed but whether this control is exerted directly or via its effects on placental growth is not certain (Owens 1991). High concentration of plasma insulin and IGF-I in well–fed ewes provide an anabolic stimulus to maternal tissues accretion at the expense of placental growth (Wallace et al 1999). Though this mechanism is relatively less understood, it remains as one of many possible hypotheses for explaining the retarded growth of the placenta in well–nourished adolescent ewes restricted in the second trimester. 

Effects of under–nutrition on intrauterine growth during the first trimester

Except under management systems where there are controlled mating programmes, sheep in the early stages of pregnancy are not often fed with the intention of optimizing their early pregnancy requirements, consequently, most studies examining the impact of ovine under–nutrition on IUGR have focused on the second and last trimesters of pregnancy when most of the increase in placental and foetal size occurs. However, through its impact on pre–implanted oocytes (McEvoy et al 1997; Borowczyk et al 2006; Castello et al 2008), and embryo and placental development (Robinson et al 1999; 2002), nutrition in early pregnancy may profoundly affect embryo viability and foetal growth and development through its effects on maternal progesterone concentration (O`Callaghan and Boland 1999). Increased dietary energy intake in sheep for a relatively short time will increase the rate of ovulation by increasing gonadotropin secretion but high nutrition during early pregnancy generally has a negative effect on oocyte (Borowczyk et al 2006) and embryo quality (O`Callaghan and Boland 1999). Lower rates of fertilization, poor oocyte viability and quality, and lower rates of blastocyst cleavage and formation have been observed in ewes whose intake was restricted by 60% compared to the control (Borowczyk et al 2006). Under–nutrition in early pregnancy may also programme the foetal ovary (Robinson et al 1999), and bone and muscle development with consequences for adult body conformation and carcass quality (Osgerby et al 2002; Greenwood 2007).  

Reduced foetal growth and muscle development are usually the result of under–nutrition during early pregnancy because the establishment of muscle fibres primarily occurs early in foetal development and remains permanent thereafter (Robinson et al 1999; Vonnahme 2007). The ovine placenta is cotyledonary (Figure 1), hence reduction in the size and number of cotyledons due to under–nutrition will reduce the transport capacity of the placenta and restrict foetal growth. Moderate restriction in feed intake resulting in gain of 55 g/d compared to unrestricted ewes gaining 300 g/d in the first trimester significantly increased foetal cotyledon numbers (Wallace et al 1999) but Steyn et al (2001) found no difference between the placental weights of ewes whose nutrient intake was moderately restricted (15%) compared to those that received their full nutrient requirement during the first 70 days of gestation. 

The effects of under–nutrition in early pregnancy could also adversely affect foetal growth in later gestation; for example, poor placental development early in pregnancy may also lead to a chronic reduction of substrate delivery for optimal foetal growth in late gestation (Morrison 2008). Foetal cotyledon numbers have similarly been found to be lower in ewes maintained on a higher dietary energy intake regime in the first trimester with no compensatory placental growth occurring in ewes maintained on a high dietary energy intake thereafter during the second and third trimesters (Wallace et al 1999). 

High blood glucose and urea concentrations are deleterious to embryo development (Furnus et al 1996; McEvoy et al 1997; O`Callaghan and Boland 1999) because toxic by–products of nitrogen metabolism, such as ammonium ions increase intrauterine pH and impair embryo survival especially when the diet offered contains higher proportion of rumen degradable protein than carbohydrates. Foetal thoracic girth and gut weight  were increased  in the first trimester, unchanged in the second but reduced in the third trimester when the daily maintenance requirements of ewes were restricted by 70% compared those whose requirements were fully met (Osgerby et al 2002). The density of foetal myofibres and number of blood capillaries in the foetal triceps brachii were reduced in Welsh mountain ewes whose feed intake was restricted by 60% at the pre–implantation stage of pregnancy (Costello et al 2008).

These data suggest that under–nutrition in early pregnancy can influence birth weight as well as adult body conformation given that the net number of muscle fibres formed prenatally remain unchanged in adult life. 

Effects of under–nutrition on intrauterine growth during the second trimester

The second trimester of pregnancy represents the period when the metabolic rates of the placenta, the foetus and its rapidly developing visceral organs are at their peak (Kelly 1992; Robinson and Symonds 1995). Data from studies by Ehrhardt and Bell (1995) show that ovine foetal weight increases exponentially (4.6 to 100 g) between day 40 and 100 of gestation. Similarly, the ratio of placental to foetal weight is also greater in the second trimester (1:1) than in the last trimester (1:10; Robinson et al 1999). These data suggest that the growth rate of the placenta may be more sensitive than the foetus to alterations in nutrition during mid pregnancy (McCrabb et al 1986; 1991; Wallace et al 1999). Of 16 experiments comparing under–nourished to highly–nourished ewes in the second trimester, 14 (87%) reported  effects on placental weight of which high nutrition increased placental size in 9 and decreased it in 3 of such studies (Kelly 1992). Such rapid growth requires a high input of ATP to fuel cell metabolism and function. In vitro studies have found that glucose uptake during this period was greater compared to the first and final trimesters (Pörtner 2009).  

The timing of nutritional restriction within the second trimester determines whether the restriction will affect foetal or placental growth. A 28-day restriction period commencing on day 75 of gestation will affect placental growth since the placenta continues to grow rapidly between day 80 and 100 whereas restriction from day 95 will result in direct effects only on foetal growth (Ehrhardt and Bell 1995; Wallace et al 1999). Imposition of under–nutrition between day 90 and 118 of gestation did not therefore result in any adverse effects on birth weight (Holst and Allen 1992). Moderate under–nutrition resulting in a loss of 0.5 body condition score in the second trimester meant to stimulate placental function through increased blood flow followed by a restoration of maternal requirements in the third trimester increased lamb birth weight both in tropical (Addah and Karikari 2008) and temperate (Holst and Allan 1992; Wallace et al 2002) ewes. This supposition is however true only for adolescent ewes in good body condition otherwise there is the opposite effect for those in poor condition (Robinson et al 1999).  

Two main hypotheses may explain this phenomenon; in adolescent growing ewes, the efficiency of ME use for conceptus growth is lower (0.1–0.15) compared to that for maternal growth and fattening (0.3–0.8) due to high heat increment of pregnancy. Partitioning of this heat indicates that the foetus’s contribution is generally far less than that of utero–placenta in both the first and second trimesters of pregnancy (Figure 4; Robinson and Symounds 1995). Secondly, a moderate degree of restriction of dietary ME intake during the second trimester has been shown to stimulate placental nutrient and oxygen uptake and increased blood flow rate leading to greater foetal growth rate if full nutrient supply is restored in the third trimester. However, placentome number and weight are reduced when ewes are well–nourished (Robinson et al 1999; Metcalfe et al 1988). Similarly, when maternal glucose concentration increases in the rapidly growing over–nourished ewe, placental glucose receptor proteins (GLUT 1 and 3) become insensitive leading to restricted utero–placental blood flow and transport of oxygen, glucose and amino acids to the foetus as well as  reduced placental lactogen secretion (Wallace et al 2004). These result in a decreased demand on the maternal glucose pool which in turn leads to increased glucose utilization by the maternal tissues at the expense of the gravid uterus. The ultimate result of this phenomenon is increased maternal growth rate, fat deposition, high body condition score, reduction in placental mass and lower birth weight of lambs (Wallace et al 1997; 2004). Similar regimes however failed to stimulate consistent placental growth and function in adult primiparous ewes (Wallace et al 1997; 2003).  

Given the rapid growth of the placenta and other products of conception during the second trimester, it appears logical to suggest that glucose, because of its higher yield of ATP, is the most important maternal metabolite for foetal growth (Mellor 1983) yet maternal plasma glucose concentration and partitioning has been shown not to affect foetal growth when the level of feeding was restricted in the first and second trimesters of pregnancy (McCrabb et al 1991).

The ovine foetus also has a relatively high demand for amino acid nitrogen in mid than in late pregnancy, averaging about 18 mg/day/g DM of foetus during mid pregnancy and only 4.6 mg/day/g DM during the last trimester (Robinson et al 1999). The inability to meet its energy requirement in mid pregnancy from maternal sources only, often triggers a glucogenic response from the foetal liver and kidneys for the biosynthesis of glutamate, an energy metabolite of amino acid metabolism as an alternative fuel for foetal growth (Bell et al 1989; Neu 2001; Battaglia 2000; Brosnan 2000; Figure 3). An efflux of glutamate from foetal skeletal muscle also contributes to this foetal glutamate pool in the adaptation of the foetus to maternal under–nutrition (Cetin 2001). The role of amino acids gluconeogenesis in the generation of energy during periods of nutritional stress suggest that amino acid supply to the maternal tissues during the second trimester of pregnancy may be more important than ME in alleviating the adverse effects of under–nutrition on lamb birth weight (Lippert et al 1983). The question of which nutrient is most critical in the second trimester has not thus been adequately answered yet. The severity of under–nutrition imposed during pregnancy is dependent on the ability of maternal reserves to adequately offset the impact without jeopardizing the life of the mother. For ewes in good body condition (score = 3.0), a moderate level of under–nutrition in mid pregnancy followed by a restoration of nutrient requirements in the last 15 weeks before parturition leads to maximum birth weight (Wilkinson and Chesnutt 1988; Addah and Karikari 2008). Pre–weaning survival rates and weaning weights of lambs born of ewes whose intake was restricted in the second trimester of pregnancy were similar to those of unrestricted ewes (Holst and Allan 1992). Although low–level feeding (70% of requirements) of ewes during the first 100 day of gestation had no detrimental effects on the carcass or muscle fibre characteristics of their lambs at slaughter, it resulted in lambs with heavier semitendinosus muscle weights, larger muscle fibre diameters and shorter sarcomere lengths than in lambs from adequately fed ewes (Nordby et al 1987). 

When dietary intake of pregnant WAD ewes was restricted in either the first, second or third trimester of pregnancy or unrestricted throughout pregnancy, gross maternal weight gains were greater for ewes supplemented throughout gestation, however, these ewes did not give birth to heavier lambs, rather those restricted in the second trimester had highest placental and birth weights (Addah et al 2007; Addah and Karikari 2008; Figure 2). It was also observed that lambs born of ewes whose intake was restricted in the second trimester had superior pre–weaning average daily gain and survivability than those well–fed throughout pregnancy or restricted in the first or third trimesters of pregnancy (Addah et al 2004). This may be explained by higher initial yield, increased nutrient and IgG content of colostrum in ewes whose intake was restricted in the second trimester (Wallace et al 2001; 2004).

The influence of moderate maternal under–nutrition on placental function and its subsequent effect on lamb birth weight appears to be manifested between the first and second trimesters or before the end of the second trimester only and does not affect lamb birth in the third trimester (Wallace et al 1999) when placental DNA and mass has reached a plateau (Ehrhardt and Bell 1995). Under–nutrition in the second trimester did not also affect the weight of individual foetal organs or whole–body foetal weight (McCrabb et al 1991). Maternal adaptation through tissue mobilization and shifts in nutrient partitioning in favour of the foetus has been widely postulated to explain the phenomenon (Robinson et al 1999).  

Wallace et al (2004) attributed the major limitations to foetal growth in rapidly growing adolescent ewes to the smaller size of the placenta rather than to alterations in its nutrient metabolism or transport capacity. Evidence showing that placental function as opposed to placental size in determining foetal growth  was demonstrated in a study in which the nutrient transport capacity of small placentae of unrestricted ewes were similar to large placentae of restricted ewes (McCrabb et al 1991).

A 15% reduction in nutrient intake during the first 70 days followed by  restoration of recommended daily intake up to day 130 of gestation resulted in a significant alteration in placental morphology in the form of increased growth of the foetal side of the placenta (type D; Figure 1) without affecting foetal size, suggesting placental adaptations to under–nutrition in the second trimester in the form of gross morphological alterations may preserve foetal growth if maternal under–nutrition is not very severe (Steyn et al 2001). Recent studies of the effects of maternal environment on lamb birth weight, however found that maternal energy intake from first to second trimester had little influence on lamb birth weight but intake during the third trimester was positively associated with weight at birth (Gardner et al 2007; Morrison 2008). 

Effects of under–nutrition on intrauterine growth during the third trimester

The third trimester represents the period during which under–nutrition has its greatest effect on production through its effects on udder development, lactational and colostrum yield, development of maternal instincts, and weight and vigour of lambs at birth (Russel 1984). This period of pregnancy is particularly important because approximately 75–80% of foetal growth occurs during the last trimester of pregnancy while feed intake around this time is constrained by reduced volume of the gastrointestinal tract. This is also the period when protein requirement is greatest; approximately 33% greater than the requirement in mid pregnancy (Schloesser et al 1993). Paradoxically a restriction of placental and foetal amino acid supply in the last trimester of pregnancy often results in an efflux of amino acids from the foetus to placenta (Robinson 1999; Owens 1995; Cetin 2001) further demonstrating the nutritional priority of the placenta over the foetus  during periods of nutritional stress. However, this should not be confused with the placental glutamate–glutamine shuttle and amino acid transamination (Figure 1) orchestrated by the foetus itself in periods of nutritional inadequacy.  

In normal feeding management programmes, the nutritional requirement of sheep during pregnancy is often determined based on linear changes in body weight as the conceptus and its associated products increase in weight, however, placental growth is not linearly related to foetal nutrient requirements or growth (Erhardt and Bell 1995) given that moderate nutrient restriction may stimulate placental and lamb growth (Wallace et al 2001; 2004). Earlier studies had demonstrated that the rate at which glucose was partitioned to the foetus in under–nourished and optimally–nourished ewes during the third trimester was similar (McCrabb et al 1991). It was therefore hypothesized that the effects of materno–placental nutrient restriction on foetal growth are insignificant and the factors regulating the rate of foetal growth during the third trimester originate from sources other than the placenta alone (McCrabb et al 1999).

According to Adu and Olaloku (1979), an average WAD ewe of about 17.5 kg requires 3 MJ ME for maternal maintenance plus 1.5 MJ ME/kg foetus. They reported that a 33% reduction of the full energy requirement of the WAD ewe reduces birth weight by 15%.  Even though the third trimester represents the period of rapid foetal growth, pregnant ewes may lose weight during this period if attention is not paid to maintenance of body condition.  

Malnutrition of the ewe also results in the production of ketone bodies as a consequence of reduced plasma glucose. A 62% increase in plasma ketones during the third trimester of pregnancy reduced the birth weight of WAD lambs by ~37% (Adu and Olaloku 1979). But when plasma glucose concentration was reduced by 58% due to under–nutrition during the last 4 weeks of pregnancy, no effect on lamb birth weight was observed in European ewes (Robinson et al 1999). Based on the relationship between maternal plasma ketone concentration in third trimester and lamb birth weight in European and WAD under–nourished ewes, it has also been found that under–nutrition may have a greater effect on birth weight of WAD lambs than those of European origin (Adu and Olaloku 1979). 

Russel (1984) has recommended a feeding practice of achieving a compromise between meeting the nutrient requirements in full, which is generally unnecessary and uneconomical and a higher degree of under–nutrition which seriously depresses ewe productivity in the third trimester of pregnancy. Another maternal adaptation to under–nutrition in the third trimester is increasing the proximity of nutrients to the foetus through increasing the concentration of nutrients in visceral organs at the expense of the skeletal muscles (Robinson et al 1999). 

Moderate maternal under–nutrition throughout pregnancy may also stimulate placental growth, increase weight of lambs at birth and decrease colostrum yield, and is associated with higher incidence of spontaneous abortions in adolescent ewes (Wallace at al 2001). Higher mortality in lambs born of over–nourished ewes has been attributed to lower intake of colostrum. This is probably because colostrum of over–nourished adolescent ewes has lower energy content compared to moderately under–nourished ewes due to lower concentration of crude protein, lactose and butterfat (Wallace et al 2001). However, in adult ewes, under–nutrition in late pregnancy is reported to have adverse long–term effects on pre–weaning lamb growth rate and mortality as milk production in subsequent lactations decrease compared to ewes which were adequately nourished (McDonald et al 1995). The effects of under–nutrition on peri–natal lamb mortality are difficult to determine as loss of immunity predisposes lambs to diseases. Consequently, diseases and parasites have often been reported as the main cause of early post–natal deaths in WAD lambs in Africa (Abassa 1995).  

Effects of environment on intrauterine growth restriction

Oxygen, glucose, lactate and amino acids are the main substrates that fuel foetal growth. Lower atmospheric oxygen concentration and pressure at higher altitudes results in insufficient concentration of oxygen reaching the materno–foetal tissues via blood circulation (hypoxia).  Hypoxia is therefore expected to directly influence materno–foetal nutrition and has been found to be the main cause of lower birth weights in women living at higher (>2500 m) altitudes (Moore et al 2004). Gestation length and placental weight increased and birth weight decreased by 26–29%  in Chilean native ewes kept at higher altitude compared to those kept at sea level (Parraguez et al 2005). In sheep, the foetus adapts to chronic hypoxia by increasing its ability to acquire and transport oxygen but this compensation is not sufficient to prevent foetal growth retardation or changes to the pattern of tissue growth in ewes chronically exposed to higher altitudes, thereby resulting in reduction in foetal body weight (Jacobs et al 1988). This decline is mainly due to slowing of foetal growth rate in the third trimester (Moore et al 2004). However, in some studies, utero–placental oxygen content and delivery decreased initially in chronically hypoxemic pregnant ewes but this was restored to normal levels after 3 d and the general effects of hypoxia were found to be minor and similar between pregnant and non pregnant ewes (Kitanaka et al 1989). From the above, it appears there is no general trend in the effects of higher altitude on foetal growth. This may be due to differences in genetic and maternal adaptation to altitude–associated IUGR as observed in humans (Moore et al 2004). 

Moderate levels of heat stress have also been shown to decrease placental and foetal weights by 139% and 89% respectively (Wallace et al 2002). In most arid regions of Africa, the effect of hypoxia on foetal growth may be confounded by seasonal variation in temperature which can have detrimental effects on reproductive performance of the ewe through its direct effects on embryo mortality and restricted foetal growth, and indirectly through its impact on availability of feed especially in extensively raised flocks. Foetal losses in the form of abortions and stillbirths are therefore major causes of reproductive losses in most arid areas of Africa. Nearly 50% of all abortions in Burkina Faso and 75% in Niger occur during or towards the end of the hot dry season (Abassa 1995).

Conclusion

• The trajectory of intrauterine growth is largely influenced by nutrition than by genetics during pregnancy. Factors that largely influence foetal growth during periods of under–nutrition include maternal nutrient pool and body condition. Placental mediations also act to reduce the impact of under–nutrition on the conceptus. The effects of under–nutrition during pregnancy on foetal growth will therefore vary depending on maternal growth and body condition during pregnancy and the extent and duration of under–nutrition imposed. Meeting the requirements of pregnancy optimally to reduce adverse effects on productivity will therefore involve a balance between meeting the nutrient requirements in full in the first and third trimesters, and achieving a moderate degree of under–nutrition in the second. Therefore in situations of limited feed availability, farmers may selectively restrict feed intake in the second trimester if pregnant ewes are in good body condition without detectable adverse effects on productivity. Under tropical conditions where small ruminants are rarely supplemented and natural forage quality varies considerable with season, the impact of under–nutrition on the productivity of the ewe through its effects on higher foetal losses, lower birth weight and pre–weaning growth rate, and higher mortality, is estimated to be greater than in other regions with superior forage quality.

Acknowledgement

Original research cited by the authors in this review was funded by the World Bank through the Agricultural Sub–sector Investment Project (AgSSIP) of the Council for Scientific and Industrial Research, Ghana. We also acknowledge original data from other authors that have been used in the review. 

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Received 29 June 2012; Accepted 8 August 2012; Published 3 September 2012

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