Maternal Undernutrition in Cows Impairs Ovarian and Cardiovascular Systems in Their Offspring1

Abstract

Severe prenatal undernutrition is usually associated with low birth weights in offspring and disorders including hypertension, obesity, and diabetes. Whether alterations in maternal nutrition insufficient to impair birth weight or prenatal growth impact the cardiovascular, stress, or metabolic systems is unknown. In addition, little is known about the effects of maternal dietary restriction on development of the reproductive system in mammals. Here, we use the bovine model, which has a gestational length and birth rate similar to humans, to show that offspring from nutritionally restricted dams (during the first trimester) were born with identical birth weights and had similar postnatal growth rates (to 95 wk of age), puberty, glucose metabolism, and responses to stress compared to offspring from control mothers. However, an increase in maternal testosterone concentrations was detected during dietary restriction, and these dams had offspring with a diminished ovarian reserve (as assessed by a reduction in antral follicle count, reduced concentrations of anti-Müllerian hormone, and increased follicle-stimulating hormone concentrations), enlarged aorta, and increased arterial blood pressure compared with controls. Our study links transient maternal undernutrition and enhanced maternal androgen production with a diminished ovarian reserve as well as potential suboptimal fertility, enlarged aortic trunk size, and enhanced blood pressure independent of alterations in birth weight, postnatal growth, or stress response and glucose tolerance. The implications are that relatively mild transient reductions in maternal nutrition during the first trimester of pregnancy (even those that do not affect gross development) should be avoided to ensure healthy development of reproductive and cardiovascular systems in offspring.

Nutritional Characteristics of the Dairy Cow During Early Gestation and Subsequent Growth and Cardiac Measurements of Her Offspring

“…Therefore, nutrient restriction during early pregnancy may improve late gestation placental functional capacity in cattle; however, the mechanisms behind this compensatory response remain elusive. Birth weight is often correlated with nutritional availability throughout pregnancy in ovine models of intrauterine growth restriction (Reynolds et al, 2005;; however, similar nutrient restriction studies in cattle have shown limited alterations to birth weight and early post-natal growth (Mossa et al, 2013). Expectedly, concentration of glucose in dams did not cause a difference in calf birth weight in the current study.…”

“…Lacking iron during early gestation was associated with greater mean arterial pressure and systolic blood pressure in humans (Bourque et al, 2008;Gambling et al, 2003;Lewis et al, 2001;Lisle et al, 2003). Similarly, in cattle increased arterial pressure and enlargement of the aorta have been observed in offspring born to dams subjected to early gestational undernutrition (Mossa et al, 2013). As stated above, substantial evidence exists that supports that nutrient availability in early gestation can impact metabolic characteristics in offspring, particularly if nutrient availability dramatically changes between the environment in the uterus and out of the uterus (Lakshmy, 2013).…”

Epigenetics and developmental programming of welfare and production traits in farm animals

“…Similar to sheep, prenatal maternal nutrition did not affect the onset of puberty in beef cattle (Martin et al 2007;Sullivan et al 2009;Mossa et al 2013), but higher offspring pregnancy rates were observed following protein supplementation in late pregnancy (Martin et al 2007) and when the AFC before breeding was high (Cushman et al 2009). In contrast, manipulation of the post-weaning diet in beef heifers did not affect AFC or overall pregnancy rate (Eborn et al 2013).…”

“…Reduced ovarian weight and large follicle diameter at 30 months is reported following slow prenatal growth rates (Wilkins et al 2006), whereas a general reduction in all follicle types was evident following exposure to a low-then highprotein diet during the first two-thirds of gestation (Sullivan et al 2009). A direct effect of maternal undernutrition during the first third of gestation on the ovarian follicle reserve has been documented using serial ultrasound (five occasions) during prepubertal and adult life (Mossa et al 2013). The robust decrease in follicle number reported is associated with increased maternal testosterone during dietary restriction and was independent of calf birthweight and postnatal growth.…”

Effects of parity and periconceptional metabolic state of Holstein–Friesian dams on the glucose metabolism and conformation in their newborn calves

“…This effect could not be confirmed in the current study. Very recently, calves born out of energyrestricted heifers from conception up to 110 days in gestation were compared with calves born from control-fed heifers: BW, growth rate and glucose metabolism were comparable between both groups (Mossa et al, 2013).…”