The first half of gestation is critical for placental growth, differentiation and vascularization as well as fetal organogenesis. Placentomes are the functional units of placental exchange in the ewe, and are classified as A, B, C or D types (Figure 1), associated with increasing placentomal efficiencies. We compared two groups of multiparous Rambouillet ewes: 1) adapted to a nomadic existence (grazed ~250 miles/year); Baggs ewes and 2) relatively sedentary ewes supplied with more than adequate nutrition (UW ewes). Equal numbers of UW and Baggs ewes were fed to 50% (nutrient restricted, NR) or 100% (control fed, CF) of NRC requirements from day 28 to 78 of gestation. A ~30% reduction of fetal weight was observed in the NR vs. CF UW ewes, but not Baggs ewes on day 78. Further, placentome type was more advanced in NR Baggs ewes (B,C and D) than NR UW ewes (vertially all A). Conversion to more advanced placentomal types resulted in similar placentomal efficiencies (fetal weight/ placentomal weight) for NR and CF Baggs ewes, while placentomal efficiency of NR UW ewes declined markedly. These data suggest that selection of ewes under different production schemes can alter the negative impacts of early maternal undernutrition on fetal growth and development. The impacts of these maternally dependent changes in placentomal and fetal growth and development on the resultant offspring are currently under investigation.
Measurements taken in this study included diet-associated changes in maternal body weight and body condition, fetal size and organ weights, placentomal numbers, weights and morphologies, and fetal blood glucose concentrations.
Climates with extreme variations in precipitation, such as Wyoming, routinely experience significant fluctuations in both quantity and quality for forage. In fact, prolonged bouts during early gestation, where >50% of the National Research Council’s (NRC) requirements for gestation are not met, are common. Sheep on rangeland may lose a significant amount of weight from early to mid gestation, and even after supplementation later in gestation, the health and growth potential of their lambs may have been compromised. Growth and carcass characteristics of ruminants are known to vary considerably even when genetics and nutritional management are constant. It has been proposed that prolonged maternal undernutrition may permanently alter fetal growth and development, predisposing offspring to cardiovascular metabolic and endocrine diseases in adult life. More specifically, maternal undernutrition has been shown in other species to increase the incidence of obesity, diabetes and coronary heart disease in their offspring. There is no information, however, about the impacts of selection for reproductive efficiency under different management regimens on the health and growth efficiency of their lambs. This is especially pertinent, as researchers frequently utilize ewes purchased from commercial sources, where their previous life histories, including reproductive histories, are unknown. This diversity in research animals may contribute to the highly variable impacts of maternal undernutrition reported on conceptus growth and development in this species, making interpretation of results very difficult. The objective of this study was to compare the impact of a constant reduction in feed intake to 50% of NRC requirements, from day 28 through day 78 of gestation in ewes selected for reproductive efficiency under markedly different management systems.
On day 20 of gestation, ewes in both groups (Baggs ewes and UW ewes) were weighed, and placed in individual pens, where they could be individually fed and watered for the duration of the study. All ewes were reweighed weekly, and individual diets fed on a metabolic body weight basis ( wt.75 ). From day 21-27, all ewes were fed 100% of NRC requirements (control diet). On day 28, both UW and Baggs ewes were randomly assigned in equal numbers to one of two groups: 1) fed 100% of NRC requirements from day 28-78 (CF; control fed group) and 2) fed 50% of NRC requirements from day 28-78 (NR; nutrient restricted group). All ewes were slaughtered on day 78 and the gravid uterus was quickly recovered. The umbilical cord was located, double ligated and severed. Fetal blood was then collected for later glucose determination. Fetal size and selected organ weights, as well as placentome number, morphology, weight and surface area, was then obtained.
Body condition scores of UW and Baggs ewes were similar on day 28 of gestation at the start of the experimental period. Body condition score remained constant from day 28 through day 78 of gestation in both UW and Baggs CF ewes. Body condition was similar for all ewes on day 28, but declined (P< 0.05) from day 28 to 78 in NR ewes from both groups (Table 1). Further, the decline of body condition score from day 28 to day 78 in NR ewes was less for Baggs ewes than for UW ewes. Nutrient restriction led to a progressive decrease in maternal body weight from day 28 to day 78 in both Baggs and UW ewes. However, UW ewes lost a greater percentage of body weight than Baggs ewes during the nutrient restriction period (4.4 vs. 4.7 %; P<0.05, respectively; Figure 2). Further, while we observed a marked reduction of fetal weight and CRL in the NR vs. CF UW ewes on day 78, no effect of nutrient restriction on these fetal measurements was seen in Baggs ewes (Table 2). This lack of nutrient restriction on fetal size in the Baggs ewes is consistent with the failure of nutrient restriction to reduce fetal blood glucose concentrations (major fetal nutrient source) in this group when compared to fetuses in their CF group. In contrast, blood glucose was reduced (P<0.05) in NR UW fetuses when compared with their CF controls. Interestingly, fetuses of both UW and Baggs NR groups exhibited left ventricular hypertrophy (increased weight relative to fetal weight) when compared to fetuses from their respective CF groups (Table 2). Placentome number, but not weight or surface area was significantly reduced by nutrient restriction in Baggs ewes but not UW ewes in this study (Table 3). Possibly to compensate for decreased placentome number, placentome type of NR Baggs ewes, but not NR UW ewes was more advanced (more B, C and D placentomes) than their respective CF groups (Figure 3). Conversion to more advanced (i.e. efficient) placentomal types resulted in similar placentomal efficiencies (fetal weight/ placentomal weight) for NR and CF Baggs ewes. In contrast, the placentomal efficiency of NR UW ewes declined markedly when compared to their CF group.
These data suggest that a relatively severe (50%) nutrient deprivation during the first half of gestation has variable impacts on placentomal differentiation, fetal growth and organ development, which appear to be dependent, in part, on the production system in which dams were selected. The long-term consequences of these maternally dependent changes in fetal and placental growth and development, in response to under nutrition during early gestation, are currently under investigation.
Educational & Outreach Activities
Refereed Journal Articles:
1) Murdoch, W.J., E.A. Van Kirk, K.A. Vonnahme and S.P. Ford. 2003. Ovarian responses to undernutrition in pregnant ewes. Reproductive Biology and Endocrinology ( http://www.rbej.com/content/pdf/1477_7827_1_6.pdf)).
2) Vonnahme, K.A., B.W. Hess, T.R. Hansen, R.J. McCormick, D.C. Rule, G.E. Moss, W.J. Murdoch, M.J. Nijland, D.C. Skinner, P.W. Nathanielsz and S.P. Ford. 2003. Maternal undernutrition from early to mid gestation leads to growth retardation, cardiac ventricular hypertrophy and increased liver weight in the fetal sheep. Biol. Reprod. 69:133-140.
Department of Animal Science Publications:
3) Vonnahme, K.A., S.P. Ford, T.R. Hansen, B.W. Hess, R. McCormick, G.E. Moss, W.J. Murdoch, P.W. Nathanielsz, M. Nijland, D.C. Rule and D. Skinner. 2002. Preliminary data on the impacts of undernutrition from early to mid gestation on fetal and placental development in the ewe. In: Department of Animal Science, Univ. of Wyoming 2002 Annual Report (pp. 73-77).
4) Han, H.C., K.J. Austin, K.A. Vonnahme, S.P. Ford, P.W. Nathanielsz. and T.R. Hansen. 2003. Maternal nutrient restriction programs gene expression in ovine fetal hearts. In: Department of Animal Science, Univ. of Wyoming 2003 Annual Report (pp.35-38).
5) Ford, S.P., K.A. Vonnahme, J.S. Gilbert, B.W. Hess, M.J. Nijland and P.W. Nathanielsz. 2003. Placentomal differentiation may compersate for maternal nutrient restriction early to mid-gestation in Rambouillet ewes adapted to range conditions. In: Department of Animal Science, Univ. of Wyoming 2003 Annual Report (39-41).
6) Schwope, M.M., W.J. Means, A.W. Wolf, B.W. Hess and S.P. Ford. 2003. Fetal growth at day 78 of gestation in nutrient restricted ewes. In: Department of Animal Science, Univ. of Wyoming 2003 Annual Report (54-56).
7) Vonnahme, K.A., B.W. Hess, R.J. McCormick, M.J. Nijland, P.W. Nathanielsz, T.R. Hansen and S.P. Ford. 2002. Undernutrition during early pregnancy alters cardiac development in the fetal sheep. Proceedings, Society for the Study of Reproduction, Baltimore, MD. (Abstract)
8) Gilbert, J.S., K.A. Vonnahme , M.J. Nijland, P.W. Nathanielsz and S.P. Ford. 2003. Maternal Undernutrition during early to mid gestation alters fetal development in the ovine fetus. Proceedings, Society for Gynecologic Investigation, Washington D. C. (Abstract)
9) Vonnahme, K.A., J.S. Gilbert. M.J. Nijland, P.W. Nathanielsz and S. P. Ford. 2003. Influence of a constant nutrient restriction from early to mid gestation on maternal and fetal blood glucose concentration and hepatic glycogen content in the sheep. Proceedings, Society for Gynecologic Investigation, Washington D. C.(Abstract)
10) Nathanielsz, P.W., K.A. Vonnahme, G. Wu, T.E. Spencer, M.J. Nijland and S.P. Ford. 2003. Placental-hepatic amino acid cycling is impaired during maternal nutrient restriction (NR) between 28 and 78 days of gestation (dGA) in sheep. Proceedings, Society for Gynecologic Investigation, Washington D.C. (Abstract)
11) Ford, S.P., K.A. Vonnahme, J.S. Gilbert, B.W. Hess, M.J. Nijland and P.W. Nathanielsz. 2003 Placental differentiation may compensate for maternal nutrient restriction from early to mid gestation in Rambouillet ewes adapted to range conditions. Proceedings, Society for the Study of Reproduction, Cincinnati, OH. (Abstract)
12) Nijland, M.J., Y. Kimura, K. Aida, K.A. Vonnahme, J.S. Gilbert, S.P. Ford and P.W. Nathanielsz. 2003. Ovine fetal placentomal arteries at 78 days gestation lack functional endothelin-B receptor subtype activity. Proceedings, Society for the Study of Reproduction, Cincinnati, OH. (Abstract)
13) Gilbert, J.S., K.A. Vonnahme, M.J. Nijland, P.W. Nathanielsz and S.P. Ford. 2003. Impacts of gender and re-alimentation after maternal nutrient restriction from early to mid gestation on kidney development in the ovine fetus. Proceedings, Society for the Study of Reproduction, Cincinnati, OH. (Abstract)
During the 2002 Department of Animal Science Field Day (September 2002), I gave a presentation to livestock producers summarizing the research finding on this project.
None was done.