Womb to womb: Maternal litter size and birth weight but not adult characteristics predict early neonatal death of offspring in the common marmoset monkey.

Julienne N Rutherford,Suzette D Tardif,Aubrey Sills,Toni Ziegler,Corinna N Ross,Donna Layne Colon,Victoria A Demartelly,Laren R Narapareddy,Alana D Steffen,Larisa A Burke,Umberto Simeoni

doi:10.1371/journal.pone.0252093

Abstract

A singular focus on maternal health at the time of a pregnancy leaves much about perinatal mortality unexplained, especially when there is growing evidence for maternal early life effects. Further, lumping stillbirth and early neonatal death into a single category of perinatal mortality may obscure different causes and thus different avenues of screening and prevention. The common marmoset monkey (Callithrix jacchus), a litter-bearing nonhuman primate, is an ideal species in which to study the independent effects of a mother's early life and adult phenotypes on pregnancy outcomes. We tested two hypotheses in 59 marmoset pregnancies at the Southwest National Primate Research Center and the Barshop Institute for Longevity and Aging Studies. We explored 1) whether pregnancy outcomes were predicted independently by maternal adult weight versus maternal litter size and birth weight, and 2) whether stillbirth and early neonatal death were differentially predicted by maternal variables. No maternal characteristics predicted stillbirth and no maternal adult characteristics predicted early neonatal death. In univariate Poisson models, triplet-born females had a significantly increased rate of early neonatal death (IRR[se] = 3.00[1.29], p = 0.011), while higher birth weight females had a decreased rate (IRR[se] = 0.89[0.05], p = 0.039). In multivariate Poisson models, maternal litter size remained an independent predictor, explaining 13% of the variance in early neonatal death. We found that the later in the first week those neonates died, the more weight they lost. Together these findings suggest that triplet-born and low birth weight females have distinct developmental trajectories underlying greater rates of infant loss, losses that we suggest may be attributable to developmental disruption of infant feeding and carrying. Our findings of early life contributions to adult pregnancy outcomes in the common marmoset disrupt mother-blaming narratives of pregnancy outcomes in humans. These narratives hold that the pregnant person is solely responsible for pregnancy outcomes and the health of their children, independent of socioecological factors, a moralistic framing that has shaped clinical pregnancy management. It is necessary to differentiate temporal trajectories and causes of perinatal loss and view them as embedded in external processes to develop screening, diagnostic, and treatment tools that consider the full arc of a mother's lived experience, from womb to womb and beyond.

Highlights

Perinatal mortality, defined by the World Health Organization as encompassing stillbirth from the 22nd gestational week and early neonatal death up though the first postnatal week [1], is a common pregnancy outcome evaluated through the lens of maternal “risk factors.”
Our findings demonstrate that stillbirth and early neonatal death may be the consequences of different pathways, and that maternal early life characteristics play an important and clinically underappreciated role in perinatal loss, early neonatal death
We hypothesized that heavier females would suffer greater perinatal loss in both categories, but we did not find that a proxy for prepregnant weight, weight later in gestation, or total weight gain were associated with either category of perinatal mortality

Summary

Introduction

Perinatal mortality, defined by the World Health Organization as encompassing stillbirth from the 22nd gestational week and early neonatal death up though the first postnatal week [1], is a common pregnancy outcome evaluated through the lens of maternal “risk factors.” Deaths across this temporal range are often “grouped on the assumption that similar factors are associated with these losses [2, p. 178].” lumping stillbirth and early neonatal death into a single category may omit, combine, or obscure different causes [3, 4] and different avenues of screening and prevention. Perinatal mortality, defined by the World Health Organization as encompassing stillbirth from the 22nd gestational week and early neonatal death up though the first postnatal week [1], is a common pregnancy outcome evaluated through the lens of maternal “risk factors.” Deaths across this temporal range are often “grouped on the assumption that similar factors are associated with these losses [2, p. A liveborn primate infant, on the other hand, is dependent both on a less physiologically-direct delivery of nutrients via breastmilk or other foods, and on a complex behavioral support system called “parenting” [9]. The differences in these delivery systems suggest that death in these contrasting temporal domains could have underlying causes that need to be differentiated

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