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Prenatal Development: Annotated Bibliography
Victoria J. Molfese
University of Nebraska - Lincoln,
[email protected]
Amanda Prokasky
University of Nebraska - Lincoln,
[email protected]
Kathleen Moritz Rudasill
University of Nebraska - Lincoln,
[email protected]
Ibrahim H. Acar
University of Nebraska-Lincoln,
[email protected]
Xiaoqing Tu
University of Nebraska–Lincoln
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Molfese, Victoria J.; Prokasky, Amanda; Rudasill, Kathleen Moritz; Acar, Ibrahim H.; Tu, Xiaoqing; Sirota, Kate; and Keiser, Brian,
"Prenatal Development: Annotated Bibliography" (2013). Faculty Publications, Department of Child, Youth, and Family Studies. Paper
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Prenatal Development
Victoria Molfese,1 Amanda Prokasky,1 Kathleen Moritz Rudasill,2
Ibrahim Hakki Acar,1 Xiaoqing Tu,1 Kate Sirota,2 and Brian Keiser 3
University of Nebraska–Lincoln
1. Child, Youth & Family Studies
2. Educational Psychology
3. College of Engineering
Emails: V. Molfese
[email protected] ; A. Prokasky
[email protected] ;
K.M. Rudasill
[email protected] ; I.H. Acar
[email protected] ;
K. Sirota
[email protected] ; B. Keiser
[email protected]
Introduction
For decades, researchers have investigated how events in the prenatal period impact
women and their infants. These studies, particularly by researchers in the medical,
neuroscience, and behavioral science fields, led to discoveries of important information
regarding the prenatal events that were strongly associated with mortality (or death) and
morbidity (or incidences of injury, pathology and abnormalities/anomalies, and
neurobehavioral sequelae) in the neonatal and infancy periods. Among the many
common findings from early research studies, two are particularly noteworthy. First,
maternal and fetal risk conditions arising in the prenatal period do not do so in isolation.
Sameroff and Chandler characterized this as a continuum of reproductive casualty, in
which several risks become linked together and affect events during pregnancy,
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outcomes at birth, and in infant and child development in subsequent years (Sameroff,
Arnold. J., and Michael J. Chandler. 1975. Reproductive risk and the continuum of
caretaker casualty. In Review of Child Development Research. Vol. 4. Edited by Francis D.
Horowitz, 187–244. Chicago: University of Chicago Press). Second, the impacts of these
risk events on outcomes were found to vary, and not all pregnancies nor all neonates and
infants were impacted to the same extent, if at all. Indeed, Sameroff and Chandler
addressed the variability or uncertainty of impacts of prenatal events by adding a
continuum of caretaking casualty to their model to include the important roles of
family, society, and the environment. This resulting transactional model of
development brought attention to the importance of genetic, biological, and
environmental interactions before and after birth on the outcomes observed in neonates,
infants, and children. Across time, research interests in prenatal and perinatal risks and
their impacts on neonates, infants, and children have expanded to the extent that many
variables heavily researched in the 1970s, 1980s, and 1990s are no longer hot topics.
Instead, advances in research and meta-analysis designs, statistical and data modeling,
new technologies, and multidisciplinary collaborations are enabling investigations that
were either not attempted in the past or only to a limited extent.
The authors would like to thank Jayden Nord for his invaluable input and assistance on this
article.
General Overviews
The framework for the publications included in this article is built from the writings of
several authors whose works have important implications for understanding prenatal
development and infant outcomes. These writings in particular have addressed the
relation between gene-environment interactions, sometimes now framed as fetal
programming, or the resetting of genetic programming during the fetal period due to
environmental variables. There is evidence that fetal programming can change outcomes
in the neonatal period and across the life span. While discussions of gene-environment
interactions are not new, what is new are the efforts of researchers in different fields to
understand whether and how genetic influences set trajectories for outcomes that may
be moderated by environmental variables. Classic publications on genetic and
environmental interactions include Waddington 1957, describing an epigenetic
landscape depicting how the environment can influence the path of development set in
motion by genes. Waddington’s theoretical and research contributions are well described
by in the biography Slack 2002 and in McLearn 1970, in a chapter on genetics and
behavioral development. From these publications we have a better understanding of the
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application of fetal programming—an application to frame reconsiderations of preterm
infant care, as described in Schug, et al. 2012; and a broader understanding of the
continuum of prenatal development and infant outcomes, as presented in Hopkins and
Johnson 2005. These publications, plus Sameroff and Chandler 975, frame this article’s
focus on research investigations of fetal development, evidence of fetal programming,
and the influence of prenatal events on infant outcomes, such as prenatal exposures to
maternal drug use, mental health problems, obstetric events such as weight grain, and
mother-infant attachment. Finally, there is a section on multivariate designs enabling
investigations of the effects of moderating or mediating variables in studies of prenatal
development and infant outcomes. Together, these publications reflect current pathways
in research on prenatal development.
Hopkins, Brian, and Scott P. Johnson, eds. 2005. Prenatal Development of Postnatal
Functions. Westport, CT: Praeger.
The seven chapters in this book focus on the continuity between prenatal events and
postnatal outcomes. Chapters on the sensory and vestibular systems, brain structure
and function, and the impacts of maternal anxiety and stress link theories and findings
related to fetal programming, showing that early life events are detectable across the
life span.
McLearn, Gearld. 1970. Genetic influences on behavior and development. In Carmichael’s
manual of child psychology. 3d ed. Edited by Paul H. Mussen, 39–76. New York: Wiley.
This chapter addresses behavior genetics and includes a description of Waddington’s
epigenetic landscape, complete with a graphic representation and examples from
animal and human research. Although research citations are dated, there is a clear
presentation on the basics of genetics, and behavior genetics intended to inform
researchers focusing on human development.
Sameroff, Arnold J., and Michael J. Chandler. 1975. Reproductive risk and the continuum
of caretaker casualty. In Review of Child Development Research. Vol. 4. Edited by
Francis D. Horowitz, M. Hetherington, S. Scarr-Salapatek, and G. Siegel, 187– 244.
Chicago: Univ. of Chicago Press.
This is a classic chapter focused on variables in the prenatal and perinatal periods that
create risks for pregnancy outcomes and the development of neonates and infants.
Research is reviewed on several reproductive risks and stressors as well as examples
of research illustrating how caretaking casualty negatively impacts infant outcomes.
Schug, Thaddeus T., Adrian Erlebacher, Sarah Leibowitz, et al. 2012. Fetal programming
and environmental exposures: Implications for prenatal care and preterm birth.
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Annals of the New York Academy of Sciences 1276:37–46. DOI: 10.1111/nyas.12003
The chapters herein present findings from multiple fields relevant to fetal programming
through investigations of gene-gene and geneenvironment interactions (or
epigenetics) during the prenatal period. The conference goal is to use research
findings to improve understanding of preterm birth and improve obstetric care.
Available online for purchase or by subscription.
Slack, Jonathan M. W. 2002. Conrad Hal Waddington: The last Renaissance biologist?
Nature Reviews Genetics 3:889–895. DOI: 10.1038/nrg933
This is a biography of the life and works of Conrad Waddington and with relevance to
current research on the human genome. Details of Waddington’s work preceding and
succeeding the publication of The Strategy of the Genes that introduces the
epigenetic landscape helps put Waddington’s work into perspective. Available
online for purchase or by subscription.
Waddington, Conrad H. 1957. The Strategy of the Genes. New York: Macmillian.
This classic work has complex but detailed descriptions of the epigenetic landscape. The
pathways chreodes or creodes and the paths canalization of cell change are
described along with mechanisms by which perturbations can occur. How genetic
variation and environmental influences reach levels necessary for pathway changes
are described.
Fetal Development
The articles in this section include research on fetal development specific to brain
anatomy, the development of auditory and visual sensitivity, early indicators of
temperament, learning and memory, and research evidence for and implications of fetal
programming and epigenetics. Many of the studies reviewed, such as functional MRI
(fMRI), magnetoencephalography, and diffusion tensor magnetic resonance imaging, are
enabled by new or newer technologies and the use of combinations of techniques
(behavioral, imaging, and genetic) to address issues of development as well as brain and
behavior relations.
FETAL BRAIN ANATOMY
The focus here is on the development of fetal brain structures. Bystron, et al. 2008
updates previous research knowledge in a review of variables influencing the timing,
sequencing, and complexity of developments in the cerebral cortex. Clowry, et al. 2010
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reviews information on the neocortex, or the portion of the human brain that is uniquely
human. Huang, et al. 2006 examines white and gray matter development using imaging
techniques to study fetal, neonatal, and child brains, thus enabling an understanding of
the developmental continuum of brain development. Huang, et al. 2012 reviews
molecular genetic studies to discuss abnormalities in brain development. Joseph 2000
provides an overview of research findings on brain structure-function development.
Prayer, et al. 2006 describes the use of in vivo MRIs for examining fetal brain structure
and function. Marsh, et al. 2008 proposes the use of imaging techniques as viable
methods for examining abnormal brain development in the context of psychiatric
disorders in childhood.
Bystron, Irina, Colin Blakemore, and Pasko Rakic. 2008. Development of the human
cerebral cortex: Boulder Committee revisited. National Reviews Neuroscience 9:110–
122. DOI: 10.1038/nrn2252
A review article updating current knowledge about cerebral cortex development
subsequent to the findings from the Boulder Committee report (1970). The focus is on
the timing, sequence and complexity of events in development. Areas that were not
known at the time of the Boulder Committee report, such as the subplate, are
highlighted. Available online for purchase or by subscription.
Clowry, Gavin, Zoltan Molnár, and Pasko Rakic. 2010. Renewed focus on the developing
human neocortex. Journal of Anatomy 217:276–288. DOI: 10.1111/j.14697580.2010.01281.x
This is a literature review examining the unique features of the human brain that set it
apart from animal brains. These new studies are enabled by new methodological
techniques.
Huang, Jin, Isabella Y. M. Wah, Ritsuko K. Pooh, and Kwong Wai Choy. 2012. Molecular
genetics in fetal neurology. Seminars in Fetal & Neonatal Medicine 17:341–346. DOI:
10.1016/j.siny.2012.07.007
This review focuses on research from genetic studies to examine three common fetal
neurological abnormalities related to disruptions in fetal brain development. The
review uses genetic data to add to findings from magnetic imaging techniques on
prenatal diagnoses. Available online for purchase or by subscription.
Huang, Hao, Jiangyang Zjang, Setsu Wakana, et al. 2006. White and gray matter
development in human fetal, newborn and pediatric brains. NeuroImage 33:27–38.
DOI: 10.1016/j.neuroimage.2006.06.009
In response to limited white matter growth studies, the authors use diffusion tensor
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magnetic resonance imaging to examine postmortem fetal brains as well as neonate
and child brains. Three-dimensional representations of the brains provide a glimpse at
the development of white matter. Available online for purchase or by subscription.
Joseph, R. 2000. Fetal brain behavior and cognitive development. Developmental Review
20:81–98. DOI: 10.1006/drev.1999.0486
This is an overview of fetal brain development and its components throughout gestation.
Functional links between developing brain areas and resulting neurobehavioral
development, as well as fetal-neonate neurobehavioral characteristics, are discussed.
Available online for purchase or by subscription.
Marsh, Rachel, Andrew J. Gerber, and Bradley S. Peterson. 2008. Neuroimaging studies
of normal brain development and their relevance for understanding childhood
neuropsychiatric disorders. Journal of the American Academy of Child & Adolescent
Psychiatry 47.11: 1233–1251. DOI: 10.1097/CHI.0b013e318185e703
This article reviews the development of the prenatal and postnatal brain using imaging
techniques, providing insight not only into normal brain development but also
abnormal brain development that gives rise to psychiatric disorders in later life.
Available online for purchase or by subscription.
Prayer, Daniela, Gregor Kasprian, Elisabeth Krampl, et al. 2006. MRI of normal fetal
brain development. European Journal of Radiology 57:199–216. DOI:
10.1016/j.ejrad.2005.11.020
This article reviews in vivo MRI findings of brain maturation rates of fetuses, beginning at
18 weeks gestational age, and describes anatomical, histological, and in vitro MRI data
on progressions in structural development. Structure and function relations are
described with reference to fetal movement. An excellent source of information on
maturation of specific brain areas. Available online for purchase or by subscription.
FETAL SENSATION
Articles in this section examine the development of fetal visual and auditory systems.
Well before birth, there is evidence that these systems are functional. While imaging
technologies enable the inquiry in many of these studies, some studies use multiple
methods. Eswaran, et al. 2004 employs magnetoencephalography (MEG) as a
noninvasive tool for studying the fetal visual system. Fulford, et al. 2003 uses fMRI to
study development of fetal visual and auditory systems, respectively, showing that these
systems are functional before birth. Graven and Browne 2008a and Graven and Browne
2008b provide general overviews of research on structure and functional development of
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the visual and auditory systems. Finally, (uotilainen
describes building blocks of
development in the fetal period that enable emotional and speech perception skills of the
neonate.
Eswaran, Hari, Curtis L. Lowery, James D. Wilson, Pam Murphy, and Hubert Preissl.
2004. Functional development of the visual system in human fetus using
magnetoencephalography. Experimental Neurology 19:S52–S58.
This article demonstrates the utility of MEG for studying human fetal brain development
(28 weeks to term) by serially recording visual evoked responses to light flashes.
Results of this study and the utility of MEG to monitor functional brain abnormalities
are described. Available online for purchase or by subscription.
Fulford, Jonathan, Shantala H. Vadeyar, Senani H. Dodampahala, et al. 2003. Fetal brain
activity in response to a visual stimulus. Human Brain Mapping 20:239–245. DOI:
10.1002/hbm.10139
This study compared fetal and adult fMRI responses to an auditory stimulus. Seven of
eighteen fetal responses and five of thirteen adult responses were localized in the
temporal region. Fetal responses show no average time to peak differences from
adults. Differences in time course of hemodynamic responses are found. Implications
for detecting pregnancy abnormalities are noted. Available online for purchase or by
subscription.
Graven, Stanley N., and Joy V. Browne. 2008a. Auditory development in the fetus and
infant. Newborn and Infant Nursing Reviews 8.4: 187–193. DOI:
10.1053/j.nainr.2008.10.010
Auditory development of the fetus and infant is reviewed, particularly the structure of
the auditory system and the factors involved in auditory development. The
implications of fetal and neonatal sound exposure for system development and the
mother-infant attachment process are described. Available online for purchase or by
subscription.
Graven, Stanley N., and Joy V. Browne. 2008b. Visual development in the human fetus,
infant, and young child. Newborn and Infant Nursing Reviews 8.4: 194–201. DOI:
10.1053/j.nainr.2008.10.011
Visual development of the fetus and infant is reviewed, particularly prenatal and
postnatal structural development, as well as the factors influencing development. The
impacts of prenatal and postnatal sleep deprivation/disruption and rapid eye
movement for visual development are described. Available online for purchase or by
subscription.
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Huotilainen, M. 2010. Building blocks of fetal cognition: Emotion and language. Infant
and Child Development 19:94–98. DOI: 10.1002/icd.658
This review article discusses research findings on the fetal precursors to the auditory and
visual skills that are shown by the neonate. Some information on emotional and
speech perception skills of the neonate are described along with suggestions for
detection of developmental delays. Available online for purchase or by subscription.
FETAL TEMPERAMENT
Although biologically based, temperament is also a product of early environment and
experience. Evaluations of temperament in infancy are often based on parent
perceptions, but researchers have expanded temperament data sources using biological
and behavioral indicators from the prenatal period. These studies highlight pre- and
postnatal factors, such as maternal stress, fetal heart rate and movement, and parent
emotion, related to measures of infant temperament. DiPietro, et al. 1996 examines
antecedents of aversive and less aversive infant temperament traits using data from
the fetal period, while DiPetro, et al. 2003 examines stability of state regulation from the
fetal to infancy periods. Eaton and Saudino 1992 reports that fetal movement meets
established criteria for defining temperament. Werner, et al. 2007 examines infant
temperamental reactivity as predictors of temperament from fetal and postnatal
measures.
DiPetro, Janet A., Katheleen A. Costigan, and Eva K. Pressman. 2003. Fetal state
concordance predicts infant state regulation. Early Human Development 68:1–13. DOI:
10.1016/S0378-3782(02)00006-3
This is an empirical study examining fetal state regulation based on fetal heart rate and
movement for effects on neonatal state regulation to determine the stability of state
regulation. Fetal regulation at 36 weeks and infant state regulation were related.
Available online for purchase or by subscription.
DiPietro, Janet A., Denice M. Hodgson, Kathleen A. Costigan, and Timothy R. B. Johnson.
1996. Fetal antecedents of infant temperament. Child Development 67.5: 2568–2583.
DOI: 10.2307/1131641
An empirical study of infant temperament as predicted by measures of fetal heart rate
and movement. More aversive traits (e.g., more difficult, less adaptable,
unpredictable) were related to higher in utero activity, and less aversive traits (e.g.,
less activity, more predictability) were related to higher heart rates in utero. Findings
support temperament as biologically based and evident early. Available online for
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purchase or by subscription.
Eaton, Warren O., and Kimberly J. Saudino 1992. Prenatal activity level as a
temperament dimension? Individual differences and developmental functions in
fetal movement. Infant Behavior and Development 15.1: 57–70. DOI: 10.1016/01636383(92)90006-R
Fetal activity was evaluated as an indicator of temperament and met criteria of present
early in life, reflecting behavioral tendencies, constitutional foundation, and showing
continuity across time. Links to postnatal temperament were not investigated.
Available online for purchase or by subscription.
Werner, Elizabeth A., Michael M. Myers, William P. Fifer, et al. 2007. Prenatal predictors
of infant temperament. Developmental Psychobiology 49.5: 474–484. DOI:
10.1002/dev.20232
Fetal heart rate and maternal postnatal psychiatric illness were assessed for 50 motherinfant dyads. Both measures were associated with infant reactivity after controlling
for maternal postnatal anxiety levels. Findings suggest that temperament is
identifiable before birth, and intrauterine factors may contribute to infant
temperament. Available online for purchase or by subscription.
FETAL LEARNING AND MEMORY
Studies of fetal learning and memory included in this section use discrimination,
habituation, and learning paradigms. Dirix, et al. 2009 provides evidence of fetal learning
and memory at 30 weeks gestation and notes changes in memory and recall evident at 34
weeks. Gonzalez-Gonzalez, et al. 2006 and Granier-Deferre, et al. 2011 use auditory stimuli
to demonstrate that prenatal exposure to repeated stimuli is related to recognition of
similar stimuli after birth. James 2010 reviews studies of fetal habituation and learning
and questions the implications of these studies for postnatal life. Kisilevsky and Hains
2010 review studies investigating the reliability of fetal heart rate as an indicator of fetal
discrimination, habituation, and learning. Morokuma, et al. 2008 shows that fetuses less
than 35 weeks gestational age do not show consistent habituation to low-intensity
sounds, but those over 35 weeks do.
Dirix, Chantal E. H., Jan G. Nijhuis, Henk W. Jongsma, and Gerard Hornstra. 2009.
Aspects of fetal learning and memory. Child Development 80.4: 1251–1258. DOI:
10.1111/j.1467-8624.2009.01329.x
Fetal learning was assessed using habituation of fetal movement to an auditory stimulus.
Fetuses demonstrated learning at 30 to 34 weeks gestation and by 34 weeks
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gestation can store and retrieve information across a 4-week period. Relation of
learning to gestational age is described.
Gonzalez-Gonzalez, N. L., M. N. Suarez, B. Perez-Piñero, H. Armas, E. Domenech, and J. L.
Bartha. 2006. Persistence of fetal memory into neonatal life. Acta Obstetricia et
Gynecologica 85:1160–1164. DOI: 10.1080/00016340600855854
This is an empirical study demonstrating the persistence of fetal auditory memory into
the newborn period. Neonates prenatally exposed to an auditory stimulus habituated
faster than control neonates without prenatal auditory stimulus exposure. These
findings support the presence of learning and memory in fetuses that persist after
birth. Available online for purchase or by subscription.
Granier-Deferre, Carolyn, Sophie Bassereau, Aurelie Ribeiro, Anne-Yvonne Jacquet, and
Anthony J. DeCasper. 2011. A melodic contour repeatedly experienced by human
near-term fetuses elicits a profound cardiac reaction one month after birth. PLoS
ONE 6.2: e17304.
This study extends evidence of prenatal learning and memory at birth to one month after
birth. Infants prenatally exposed to a melody had larger heart rate deceleration when
exposed to a similar melody as compared to infants never prenatally exposed.
Implications of the findings for the perceptual tuning of the auditory system are
discussed.
James, David. K. 2010. Fetal learning: A critical review. Infant and Child Development
19:45–54. DOI: 10.1002/icd.653
The article reviews research involving fetal habituation and learning. Definitions of
learning, methods for studying and measuring fetal learning, as well as findings and
limitations of the studies reviewed are described. The relation of fetal learning to child
development is questioned. Available online for purchase or by subscription.
Kisilevsky, Barbara S., and Sylvia M. J. Hains. 2010. Exploring the relationship between
fetal heart rate and cognition. Infant and Child Development 19.1: 60–75. DOI:
10.1002/icd.655
This review examines the role in fetal heart rate measures in studies of discrimination,
habituation, and auditory learning. Issues related to HR (methodology, maturation,
neural regulation, and links to cognition) are described. Clear evidence from classic
and recent studies of prenatal cognitive skills is presented. Available online for
purchase or by subscription.
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Morokuma, Seiichi, Valentina Doria, Antonio Ierullo, et al. 2008. Developmental change
in fetal response to repeated lowintensity sound. Developmental Science 11.1: 47–52.
DOI: 10.1111/j.1467-7687.2007.00646.x
Developmental differences in fetal habituation to auditory stimuli are examined in this
study. Fetuses at 35 to 37 weeks exhibit rapid heart rate habituation, whereas those
32 to 34 weeks show variable responses and little recovery to a new stimulus. The
findings align with other researchers’ findings that fetuses habituate to auditory
stimulus. Available online for purchase or by subscription.
FETAL PROGRAMMING
There is strong interest in understanding how events in the prenatal period may influence
the course of fetal and infant development. In this section, psychological, cognitive,
health, and social outcomes are considered from the view of fetal programming. Barker
2002 discusses the relation between coronary heart disease in later life and growth in
utero and in childhood. Ellison 2010 discusses epigenetics and fetal programming in the
context of physical and mental health. Gluckman and Hanson 2010 proposes that fetal
programming is adaptive, but maladaptive consequences can arise. The placenta,
carrying nutrients from mother to fetus, plays a role in fetal programming as described in
Godfrey 2002. Kaiser and Sachser 2009 uses results of animal studies to argue for an
adaptive view of stress exposure. Mathers and McKay 2009 points to maternal diet and
impacts on DNA expression, and describes the relations between epigenetics and fetal
programming. Poggi, et al. 2012 examines how prenatal exposure to maternal stress
might program stress responses in infancy. Shlotz and Phillips 2009 discusses the fetal
origins of mental health disorders and prenatal risk conditions.
Barker, David J. P. 2002. Fetal programming of coronary heart disease. Trends in
Endocrinology & Metabolism 13.9: 364–368. DOI: 10.1016/S1043-2760(02)00689-6
This is an empirical study of men and women who developed or died from coronary heart
disease, size at birth and infancy, and gains in weight and body mass index in
childhood. For both genders, small birth and infancy size, and rapid gains in childhood
characterize risk for coronary heart disease. Mechanisms related to these findings are
discussed. Available online for purchase or by subscription.
Ellison, Peter T. 2010. Fetal programming and fetal psychology. Infant and Child
Development 19.1: 6–20. DOI: 10.1002/icd.649
This article reviews the fetal programming hypothesis and implications for public health,
such as impacts of specific perinatal risks on physical and mental health. The authors
address how this hypothesis might reflect an updated theory of evolution when
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considering epigenetic patterns. Evidence from human and animal studies is
discussed. Available online for purchase or by subscription.
Gluckman, Peter D., and Mark A. Hanson. 2010. The plastic human. Infant and Child
Development 19:21–26. DOI: 10.1002/icd.650
The authors discuss fetal programming as developmental plasticity. Such plasticity can
originate as adaptive but maladaptive consequences arise from interactions
between genes and environment. Birth weight has been discussed as a biological
marker for maladaptive consequences, but a broader consideration of early biological
markers is needed to understand phenotypic variations. Available online for purchase
or by subscription.
Godfrey, Keith M. 2002. The role of the placenta in fetal programming: A review.
Placenta 23:S20–S27.
This review examines fetal programming as affected by maternal factors during
pregnancy, placental functioning, and fetal development. Placenta functioning is
discussed as a focus for intervention that can impact the long-term health of the
infant. Available online for purchase or by subscription.
Kaiser, Sylvia, and Norbert Sachser. 2009. Effects of prenatal social stress on offspring
development: Pathology or adaptation? Current Directions in Psychological Science
(Wiley-Blackwell) 18:118–121. DOI: 10.1111/j.1467-8721.2009.01620.x
This review of animal studies examines the influences of prenatal exposure to
environmental stress. Rather than being pathological, the authors argue that stress
exposure preadapts the fetus to the postnatal environment. Social stability and
instability as related to fetal adaptation are discussed. Available online for purchase or
by subscription.
Mathers, John C., and Jill A. McKay. 2009. Epigenetics—potential contribution to fetal
programming. Advances in Experimental Medicine And Biology 646:119–123. DOI:
10.1007/978-1-4020-9173-5_13
The authors discuss evidence of the impact of maternal diet on DNA methylation and
modification of histones of the developing fetus. Epigenetic changes are implicated in
fetal programming and in understanding the developmental origins of health.
Epigenetic changes occurring in later life are also discussed. Available online for
purchase or by subscription.
Poggi Davis, Elysia, Laura M. Glynn, Feizal Waffarn, and Curt A. Sandman. 2012. Prenatal
maternal stress programs infant stress regulation. Journal of Child Psychology And
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Psychiatry 52.2: 119–129. DOI: 10.1111/j.1469-7610.2010.02314.x
This empirical study investigates prenatal maternal cortisol and maternal psychosocial
stress as possible fetal programming sources of infant responses to stress. Exposure
to maternal stress in the last two trimesters was related to higher measures of cortisol
and slower behavioral recovery in infants based on a heel-stick procedure. Available
online for purchase or by subscription.
Shlotz, Wolff, and David I. W. Phillips. 2009. Fetal origins of mental health: Evidence and
mechanisms.
Brain,
Behavior,
and
Immunity
23.7:
905–916.
DOI:
10.1016/j.bbi.2009.02.001
The authors review studies linking personality disorders and risk of psychopathology to
fetal programming. A variety of maternal prenatal, parental genetic, and fetal
environment factors are modeled as relating to mental health outcomes. Implications
for future research and opportunities for interventions are discussed. Available online
for purchase or by subscription.
Prenatal Exposures
Research in this section examines the impacts of prenatal exposures to a variety of fetal
stressors, such as nicotine, alcohol, legal and illegal drugs, as well as poly-drug use, and to
maternal mental health conditions. Reviewed studies examine impacts of these fetal
stressors using a variety of outcomes measured in the neonatal and infancy periods as
well as at other ages across the life span. Complex issues of exposure timing (trimester),
methods of exposure verification and dosage/severity, and how the presence of other
explanatory factors are addressed are all touched on in articles across sections. Research
findings show that infant outcomes differ across timing of exposure and type of
exposure. Researchers discuss the need for considering additional factors in
understanding links between prenatal exposures and infant outcomes.
EXPOSURE TO NICOTINE
Exposure to smoking in utero has been linked to negative infant outcomes, most notably
low birth weight, impaired fetal growth, and preterm birth. Recent research provides
evidence of links between prenatal smoking and cognitive and/or behavioral outcomes.
Bernstein, et al. 2005 and Roza, et al. 2007 explore the effects of timing of fetal nicotine
exposure and fetal and infant birth weight or head growth. Cornelius and Day 2009
reviews behavioral, genetic, and imaging studies of nicotine exposure at several
gestational ages. Ernst, et al. 2001 includes reviews of human and animal studies on
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consequences of prenatal nicotine exposure. Fenercioglu, et al. 2009, Król, et al. 2012,
and Samper, et al. 2012 use somewhat different methods to compare impacts of active,
passive, and nonsmoking on measures of newborn and infant growth. Webhy, et al. 2011
includes consideration of socio-economic status (SES) in investigating the impacts of
maternal smoking on infant neurobehavioral development.
Bernstein, Ira M., A. Mongeon Joan, Gary J. Badger, Laura Solomon, Sarah H. Heil, and
Stephen T. Higgins. 2005. Maternal smoking and its association with birth weight.
Obstetrics
Gynecology
106.5,
Part
1:
986–991.
DOI:
10.1097/01.AOG.0000182580.78402.d2
Mothers’ patterns of smoking by trimester were examined to determine the relationship
to infant birth weight. Smoking during the third trimester was associated with lower
birth weight. Effects at the per-cigarette level in the third trimester and effects on
birth weight are presented.
Cornelius, Marie D., and Nancy L. Day. 2009. Developmental consequences of prenatal
tobacco exposure. Current Opinion in Neurology 22.2: 121–125. DOI:
10.1097/WCO.0b013e328326f6dc
This is a review of human research (2007–2008) focusing largely on prospective studies
with biologically verified tobacco exposure. Evidence is presented on infant through
adolescent samples (including contrary findings) from behavioral, genetic, and some
imaging methodologies. Each article is reviewed, and reviewed sections are very brief.
Available online for purchase or by subscription.
Ernst, Monique, Eric T. Moolchan, and Miqun L. Robinson. 2001. Behavioral and neural
consequences of prenatal exposure to nicotine. Journal of the American Academy of
Child and Adolescent Psychiatry 40.6: 630–641. DOI: 10.1097/00004583-20010600000007
The article reviews human and animal research on prenatal nicotine exposure and
prenatal, perinatal, and postnatal outcomes. Human studies include evidence of
effects on neurobehavioral outcomes (infancy to adulthood). Animal studies include
evidence of impacts, in utero and postnatal, and evidence of impacts on neural
mechanisms. Available online for purchase or by subscription.
Fenercioglu, A. K., I. Tamer, G. Karatekin, and A. Nuhoglu. 2009. Impaired postnatal
growth of infants prenatally exposed to cigarette smoking. Tohoku Journal of
Experimental Medicine 218.3: 221–228. DOI: 10.1620/tjem.218.221
Maternal smoking, passive smoking, and nonsmoking were examined in relation to head
circumference, weight, and height at birth, 3 months, and 6 months. Deficits in
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growth on the three measures were found at 6 months for infants of smokers, but
infants of passive smokers had caught up. Available online for purchase or by
subscription.
Król, Marzenna, Ewa Florek, Wojciech Piekoszewski, Renata Bokiniec, and Maria K.
Kornacka. 2012. The influence of prenatal exposure to tobacco smoke on neonatal
body proportions. Journal of Women’s Health Care 1:117. DOI: 10.4172/21670420.1000117
This empirical study examines neonatal anthropometric outcomes (weight, crown-heel
length, head and chest circumference, ponderal index [relation of weight to length])
and maternal active/passive smoking and nonsmoking. Impacts of active smoking
were found for all outcomes except ponderal index; passive smoking effects on
outcomes were not significant.
Roza, Sabine J., Bero Verburg, Vincent W. V. Jaddoe, et al. 2007. Effects of maternal
smoking in pregnancy on prenatal brain development. The generation R study.
European Journal of Neuroscience 25.3: 611–617. DOI: 10.1111/j.1460-9568.2007.05393.x
This prospective study of maternal smoking in early, mid-, and late pregnancy uses
questionnaires and measures of head and brain growth. Prenatal smoking reduced
head and brain growth. Three mechanisms to explain links of smoking in pregnancy
and neurobehavioral development of the fetus and infant are discussed. Available
online for purchase or by subscription.
Samper, M. P., A. Jiménez-Muro, I. Nerín, A. Marqueta, P. Ventura, and G. Rodríguez.
2012. Maternal active smoking and newborn body composition. Early Human
Development 88.3: 141–145. DOI: 10.1016/j.earlhumdev.2011.07.015
This empirical study examines effects of exposure to maternal smoking and body
composition. While all measures of infant body composition were heavier for
nonsmoking than smoking mothers, no differences were found for the ponderal
index. Infants prenatally exposed to smoke had leaner body mass, lower body fat, and
lower birth weights. Available online for purchase or by subscription.
Webhy, George L., Kaitlin Prater, Ann Marie McCarthy, Eduardo E. Castilla, and Jeffrey C.
Murray. 2011. The impact of maternal smoking during pregnancy on early child
neurodevelopment. Journal of Human Capital 5.2: 207–254. DOI: 10.1086/660885
This is a prospective study of maternal smoking in pregnancy, SES, and neurobehavioral
outcomes in South American infants (3 and 24 months). Neurobehavioral outcomes
were poorer in the smoking group, with increased negative neurodevelopmental
outcomes in the low SES sample. Smoking rates were higher in the low SES compared
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to high SES sample. Available online for purchase or by subscription.
EXPOSURE TO ALCOHOL
Articles in this section address evidence of the consequences of prenatal exposure to
alcohol. Consistent across studies are findings that negative outcomes are dependent
upon dosage and timing of exposure to alcohol. Chen 2012 finds relations between
alcohol use during pregnancy and infant temperament, and to a lesser extent on birth
weight; Haley, et al. 2006 reports impacts on infant stress reactions from fetal alcohol
exposure. Hannigan and Armant 2000 provides descriptions of diagnostic criteria used in
studies of prenatal alcohol exposure and reviews evidence of impacts on a variety of
outcomes. Henderson, et al. 2007 reviews outcomes from exposure to low-to-moderate
alcohol use. Testa, et al. 2003 describes results of a meta-analysis showing that alcohol
exposure impacted infant outcomes only in a narrow age range.
Chen, Jen-Hao. 2012. Maternal alcohol use during pregnancy, birth weight, and early
behavioral outcomes. Alcohol and Alcoholism 47.6: 649–656. DOI:
10.1093/alcalc/ags089
This study examined a national dataset for effects of maternal alcohol use during
pregnancy on infant behavior, temperament, and birth weight. Models tested were
adjusted for some confounds. Prenatal alcohol use had less impact on birth weight
compared to temperament, with effects found for temperamental difficultness
even when use was low-to-moderate. Available online for purchase or by subscription.
Haley, David W., Nancy S. Handmaker, and Jean Lowe. 2006. Infant stress reactivity and
prenatal alcohol exposure. Alcoholism: Clinical and Experimental Research 30.12:
2055–2064. DOI: 10.1111/j.1530-0277.2006.00251.x
This study examined the effect of prenatal alcohol exposure on emotion and stress
regulation measured by cortisol level, heart rate, and behavior in 5- to 7-month olds.
Impacts on all emotion and stress measures were found, along with some gender
effects. Controls for maternal depression and income did not alter results. Available
online for purchase or by subscription.
Hannigan, John H., and D. Randall Armant. 2000. Alcohol in pregnancy and neonatal
outcome. Seminars in Neonatology 5:243–254. DOI: 10.1053/siny.2000.0027
This review targets prenatal alcohol consumption and its impacts on the fetus and
newborn. Diagnostic criteria for fetal alcohol syndrome (FAS) and alcohol-related
neurodevelopmental disorder (ARND) are described, along with information on
outcomes (e.g., spontaneous abortion, gestation length, birth weight, facial
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dysmorphology, and other selected birth defects). FAS and ARND are evident in the
newborn. Available online for purchase or by subscription.
Henderson, J., R. Gray, and P. Brocklehurst. 2007. Systematic review of effects of low–
moderate prenatal alcohol exposure on pregnancy outcome. International Journal of
Obstetrics and Gynecology 114:243–252. DOI: 10.1111/j.1471-0528.2006.01163.x
This article is a systematic review of 46 studies of the impacts of low-to-moderate alcohol
consumption in pregnancy. No consistent effects are reported for selected outcomes
(stillbirth, impaired growth, birth weight, preterm birth, and physical malformations).
Methodological weaknesses in reviewed studies are noted. Tables summarizing
reviewed studies are provided.
Testa, Maria, Brian M. Quigley, and Rina Das Eiden. 2003. The effects of prenatal alcohol
exposure on infant mental development: A meta-analytical review. Alcohol and
Alcoholism 38.4: 295–304. DOI: 10.1093/alcalc/agg087
This meta-analysis includes 10 studies examining the effects of prenatal alcohol exposure
on infant mental development at 6–8, 12–13, and 18–24 months. Alcohol exposure had
negative effects on mental development at 12–13 months only. Impacts were related
to dosage level. Possible reasons for inconsistencies across age groups are discussed.
EXPOSURE TO ANTIPSYCHOTIC AND PSYCHOTROPIC DRUGS
The articles in this section explore relations between negative infant outcomes and use
of antipsychotic and psychotropic medications in pregnancy, with the caveat that
disentangling mental health and drug use is difficult. Emory and Dieter 2006 reports the
results of three studies indexing fetal sensitivity to maternal depression and psychotropic
drug use. Gentile 2010 identifies methodological difficulties in the consistency of findings
across forty-one studies involving psychotropic drug exposure. Johnson, et al. 2012
differentiates impacts of antipsychotic and psychotropic drugs on infant outcomes.
Oberlander, et al. 2006 separates antidepressant drug use and nonuse in depressed
mothers to study impacts of newborn outcomes. Weikum, et al. 2012 links fetal and infant
auditory discrimination with maternal depression and use of antidepressants.
Emory, Eugene K., and John N. I. Dieter. 2006. Maternal depression and psychotropic
medication effects on the human fetus. Annals of the New York Academy of Sciences
1094.1: 287–291. DOI: 10.1196/annals.1376.036
Three studies examined: 1) fetal activity of depressed mothers across gestation; 2) effects
of maternal depression and anxiety on responsivity in late term fetuses; and 3) effects
of psychotropic medication on fetal cerebral blood flow. Findings show evidence of
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fetal sensitivity to maternal mental state and use of psychotropic medication.
Available online for purchase or by subscription.
Gentile, Salvatore. 2010. Neurodevelopmental effects of prenatal exposure to
psychotropic medications. Depression and Anxiety 27:675–686. DOI: 10.1002/da.20706
This is a review of forty-one studies on the effects of prenatal exposure to psychotropic
medications and infant mental development. Separate tables are presented with
results for each medication considered. Some consistencies in results are noted.
Difficulty in finding consistent results with some medications is attributed to varying
dosages and timing of exposure in utero. Available online for purchase or by
subscription.
Johnson, Katrina C., Jamie L. LaPrarie, Patricia Brennan, Zachary Stowe, and Jeffrey
Newport. 2012. Prenatal antipsychotic exposure and neuromotor performance
during infancy. Archives of General Psychiatry 69.8: 787–794. DOI:
10.1001/archgenpsychiatry.2012.160
This is a prospective study of prenatal exposure to antipsychotic, antidepressant, or no
medication and neuromotor performance and habituation in 6-month-old infants.
Antipsychotic (but not antidepressant exposure) impacted infant neuromotor
performance. Performance was related to maternal psychiatric history. No effect on
habituation was observed. Available online for purchase or by subscription.
Oberlander, Tim F., William Warburton, Shaila Misri, Jaafar Aghajanian, and Clyde
Hertzman. 2006. Neonatal outcomes after prenatal exposure to selective serotonin
reuptake inhibitor antidepressants and maternal depression using population-based
linked health data. Archives of General Psychiatry 63:898–906. DOI:
10.1001/archpsyc.63.8.898
A population database is used to study prenatal exposure to antidepressants and
maternal depression on newborn outcomes compared with those of mothers with
depression but not medication exposed. Exposed infants had lower birth weights and
higher incidence of respiratory distress, jaundice, and feeding problems. Propensity
matching controlled for mental illness severity.
Weikum, Whitney M., Tim F. Oberlander, Takao K. Hensch, and Janet F. Werker. 2012.
Prenatal exposure to antidepressants and depressed maternal mood alter trajectory
of infant speech perception. Proceedings of the National Academy of Sciences of the
United States of America 109:17221–17227. DOI: 10.1073/pnas.1121263109
This empirical study examined the impacts of exposure to antidepressants (serotonin reuptake
inhibitors, or SRIs) during pregnancy on fetal consonant and vowel discrimination and infant
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speech and language discrimination. Maternal prenatal depression and using SRIs during
pregnancy affect development of speech perception skills.
EXPOSURE TO ILLEGAL DRUGS
The use of illicit drugs during pregnancy is difficult to research due to many factors
including legal implications. However, the articles in this section provide evidence that
prenatal exposure to cocaine, marijuana, and methamphetamine does have some, but
often differential, impacts on infant outcomes. Behnke, et al. 2013 reports on prevalence,
mechanisms, and detection of prenatal exposure to common illegal drugs and infant
outcomes. Frank, et al. 2002 reports that prenatal cocaine exposure is related to infant
outcomes but impacts can be modified by caretaking and birth weight variables. Fried
and Smith 2001 reviews the literature on prenatal marijuana exposure and infant and
child executive function skills, as well as the issues that complicate conclusions from drug
exposure studies. Jutras-Aswad, et al. 2009 reviews possible mechanisms by which
exposure impacts brain development. Singer, et al. 2002 reports impacts of prenatal
cocaine exposure on mental development of infants and toddlers, and Smith, et al. 2011
reports impacts of methamphetamine exposure on infant motor development.
Behnke, Marylou, and Vincent C. Smith 2013. Prenatal substance abuse: Short- and longterm effects on the exposed fetus. Pediatrics 131.3: e1009–e1024. DOI:
10.1542/peds.2012-3931
A technical report presenting findings on prevalence of common illegal drug in prenatal
exposures, methods of exposure identification, mechanisms of action in fetal
development, and short- and long-term outcomes of exposed infants.
Frank, Deborah A., Ruth Rose Jacobs, Marjorie Beeghly, et al. 2002. Level of prenatal
cocaine exposure and scores on the Bayley Scales of Infant Development: Modifying
effects of caregiver, early intervention, and birth weight. Pediatrics 110.6: 1143–1152.
DOI: 10.1542/peds.110.6.1143
This is a prospective longitudinal study of differential prenatal cocaine exposures on
infant development at 6, 12, and 24 months. Cocaine dosage from maternal report
assays did not affect measured outcomes, but cocaine exposure, gestational age, low
birth weight, and kinship care were related to developmental scores. Available online
for purchase or by subscription.
Fried, Peter A., and A. M. Smith. 2001. A literature review of the consequences of
prenatal marihuana exposure: An emerging theme of a deficiency in aspects of
executive function. Neurotoxicology and Teratology 23:1–11. DOI: 10.1016/S0892-
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0362(00)00119-7
This is a review of the literature examining effects of prenatal marijuana exposure on
outcomes (IQ, executive function, brain structure and function, neurobehavioral, and
cognitive abilities) from newborn to school-age children. Issues that complicate the
interpretation of results of empirical studies are reviewed. Available online for
purchase or by subscription.
Jutras-Aswad, Didier, Jennifer A. DiNieri, Tibor Harkany, and Yasmin L. Hurd. 2009.
Neurobiological consequences of maternal cannabis on human fetal development
and its neuropsychiatric outcome. European Archives of Psychiatry and Clinical
Neuroscience 259:395–412. DOI: 10.1007/s00406-009-0027-z
This literature review examines the effect of prenatal marijuana exposure on fetal brain
development, infant behaviors, cognitive abilities, and subsequent neuropsychiatric
disorders. Mechanisms by which marijuana exposure may influence later outcomes
due to its effect on neurotransmitters are described with supporting research
evidence. Available online for purchase or by subscription.
Singer, Lynn T., Robert Arendt, Sonia Minnes, et al. 2002. Cognitive and motor outcomes
of cocaine-exposed infants. Journal of the American Medical Association 287.15: 1952–
1960. DOI: 10.1001/jama.287.15.1952
This prospective, longitudinal study examines high-risk, low SES, prenatal, cocaine
exposed infant at 6.5, 12, and 24 months of age. Cocaine exposure significantly
depressed mental development performance at 2 years old. No effects of cocaine
exposure on motor development were found. Discussion of study limitations and
conclusions is detailed.
Smith, Lynne M., Linda L. LaGasse, Chris Derauf, et al. 2011. Motor and cognitive
outcomes through three years of age in children exposed to prenatal
methamphetamine. Neurotoxicology and Teratology 33.1: 176–184. DOI:
10.1016/j.ntt.2010.10.004
This prospective study examines prenatal methamphetamine exposure on motor and
cognitive skills of children at 1–3 years of age. Multiple controls for covariates were
used. Methamphetamine exposure impacted fine motor skills at age 1, but not age 3.
No effects on cognitive development were found. The need for follow-ups beyond 3
years is discussed. Available online for purchase or by subscription.
POLYDRUG EXPOSURE
One difficulty in conducting research on impacts of prenatal drug exposure is that drug
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use often involves more than one drug. Thus, it is difficult to attribute specific outcomes
to specific drugs. The articles in this section examine the effects of polydrug exposure in
utero. Asanbe, et al. 2006 reports that children prenatally exposed to cocaine and/or
polydrugs differed from matched controls on some but not all cognitive measures.
Noland, et al. 2003 investigates impacts of cocaine and polydrug exposure on executive
function skills of infants. Singer, et al. 2012 investigates use of Ecstasy and polydrug use
during pregnancy and outcomes for the women and for their infants. Smith, et al. 2006
examines prenatal Ecstasy and polydrug exposure and SES on fetal growth. Thompson,
et al. 2009 reviews the results of animal studies for evidence of drug exposure impacts on
brain development.
Asanbe, Comfort B., and Edna Lockert. 2006. Cognitive abilities of African American
children with prenatal cocaine/polydrug exposure. Journal of Health Care for the Poor
and Underserved 17.2: 400–412. DOI: 10.1353/hpu.2006.0054
Prenatal cocaine/polydrug exposed and nonexposed African American children ages 6
and 8 years were studied. Compared to matched controls, IQ differences, but not
differences in distractibility tasks, were identified. Interpretations of findings question
generalizations about cocaine exposure and child outcomes. Available online by
subscription.
Noland, Julia S., Lynn T. Singer, Sudhir K. Mehta, and Dennis Super. 2003. Prenatal
cocaine/polydrug exposure and infant performance on an executive functioning
task.
Developmental
Neuropsychology
24.1:
499–517.
DOI:
10.1207/S15326942DN2401_05
An investigation of level of exposure to cocaine and/or polydrugs prenatally and 9- to 12month-old infants’ working memory, inhibitory control, and planning assessed by Anot-B task performance. Effects of heavy exposure remained even after an array of
possible confounding variables and mediators were analyzed. Available online for
purchase or by subscription.
Singer, Lynn T., Derek G. Moore, Sarah Fulton, et al. 2012. Neurobehavioral outcomes of
infants exposed to MDMA (Esctasy) and other recreational drugs during pregnancy.
Neurotoxicology and Teratology 34.3: 303–310. DOI: 10.1016/j.ntt.2012.02.001
This prospective study examines exposure to MDMA in the prenatal period in polydrug
using women and neonatal and infant outcomes. MDMA exposure did not yield
differences in neurobehavioral outcomes at 1 month or differences on cognitive
measures at 4 months. Differences in motor performance were found at 4 months.
Maternal consequences of MDMA use are described. Available online for purchase or
by subscription.
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Smith, Lynne M., Linda L. LaGasse, Chris Derauf, et al. 2006. The infant development,
environment, and lifestyle study: Effects of prenatal methamphetamine exposure,
polydrug exposure, and poverty on intrauterine growth. Pediatrics 118.3: 1149–1156.
DOI: 10.1542/peds.2005-2564
This prospective study investigates prenatal MDMA exposure and fetal growth. MDMA
exposed infants were more likely to be small for gestational age and have lower birth
weight, after adjusting for covariates (smoking, alcohol, marijuana) than nonexposed
infants. The developmental sequelae of small for gestational age and low birth weight
are discussed. Available online for purchase or by subscription.
Thompson, Barbara L., Pat Levitt, and Gregg D. Stanwood. 2009. Prenatal exposure to
drugs: Effects on brain development and implications for policy and education.
National Review of Neuroscience 10.4: 303–312. DOI: 10.1038/nrn2598
This review article includes evidence from animal models to examine the effect of
prenatal drug exposure, including cocaine, methamphetamine, nicotine, alcohol,
antidepressants, and other prescription medications on brain development. Future
directions for research studies and implications of findings for policymakers are
described. Available online for purchase or by subscription.
EXPOSURE TO MATERNAL DEPRESSION AND ANXIETY
Maternal depression and anxiety may arise due to biological changes (i.e., hormonal),
environmental effects (i.e., domestic violence, medical problems) during pregnancy, or
idiopathically. Davalos, et al. 2012; Field 2011; Pearson, et al. 2012; and Van BatenburgEddes, et al. 2009 each target prenatal and postnatal influences from maternal anxiety
and/or depression to investigate impacts on fetal, infant, and/or child development and
mother-infant interactions. There are methodological differences across studies. While
postnatal anxiety and/or depression are studied most often, these authors argue for the
importance of studying mental health conditions during pregnancy. Brouwers, et al. 2001
investigates how timing of prenatal exposure to maternal anxiety impacts infant
development. Kinsella and Monk 2009 uses a fetal programming view to integrate
findings in their literature review on effects of maternal mental health across the lifespan. Wojcicki, et al. 2011 finds that Latino infants grew at a slower rate when exposed
pre- and postnatally to maternal depression.
Brouwers, Evelien, Anneloes L. van Barr, and Victor J. M. Pop. 2001. Maternal anxiety
during pregnancy and subsequent infant development. Infant Behavior and
Development 24:95–106. DOI: 10.1016/S0163-6383(01)00062-5
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This prospective study investigates the influence of prenatal maternal anxiety on infant
and child outcomes. Timing of exposure, particularly in late pregnancy, influenced
outcomes. Explanations of these findings using the current study and results of other
studies are provided. Available online for purchase or by subscription.
Davalos, Deana B., Carly A. Yadon, and Hope C. Tegellas. 2012. Untreated prenatal
maternal depression and the potential risks to offspring: A review. Archives of
Women’s Mental Health 15:1–14. DOI: 10.1007/s00737-011-0251-1
This review article examines the influence of unmedicated maternal prenatal depression
and infant outcomes. The authors argue that prenatal depression is understudied
compared to postpartum depression. A detailed table summarizing the reviewed
literature is provided. Available online for purchase or by subscription.
Field, Tiffany. 2011. Prenatal depression effects on early development: A review. Infant
Behavior & Development 34:1–14. DOI: 10.1016/j.infbeh.2010.09.008
The article reviews literature on prenatal and postnatal depression and influences on
fetal, infant, and child outcomes. The need for research to address the knowledge gap
and the methodological complexities that influence the findings from the studies
reviewed are discussed. Available online for purchase or by subscription.
Kinsella, Michael T., and Catherine Monk. 2009. Impact of maternal stress, depression,
and anxiety on fetal neurobehavioral development. Clinical Obstetrics & Gynecology
52:425–440. DOI: 10.1097/GRF.0b013e3181b52df1
This review of the literature is relevant to the fetal programming hypothesis in finding
that exposure in utero to the influence of maternal psychological states can have
long-term effects across the lifespan. A detailed table is provided that summarizes the
studies reviewed. Clinical implications are described. Available online for purchase or
by subscription.
Pearson, R. M., R. Melotti, J. Heron, et al. 2012. Disruption to the development of
maternal responsiveness? The impact of prenatal depression on mother–infant
interactions.
Infant
Behavior
&
Development
35:613–626.
DOI:
10.1016/j.infbeh.2012.07.020
This empirical study investigates the influence of prenatal and postnatal maternal
depression and infant outcomes and the possible mediating influence of depression in
reducing maternal responsiveness. Timing of depression influenced the outcomes.
The importance of interventions of facilitate maternal responsiveness in depressed
women who are pregnant is discussed. Available online for purchase or by
subscription.
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van Batenburg-Eddes, Tamara, Laila de Groot, Anja C. Huizink, et al. 2009. Maternal
symptoms of anxiety during pregnancy affect infant neuromotor development: The
generation R study. Developmental Neuropsychology 34:476–493. DOI:
10.1080/87565640902964508
This empirical study investigates the impacts of maternal depression and anxiety during
and after pregnancy and infants’ neuromotor development at 3 months. High prenatal
maternal anxiety and depression impacted infant outcomes. Available online for
purchase or by subscription.
Wojcicki, Janet M., Katherine Holbrook, Robert H. Lustig, et al. 2011. Chronic maternal
depression is associated with reduced weight gain in Latino infants from birth to 2
years of age. PloS One 6.2: e16737.
Prenatal and postnatal depressive symptoms experienced during pregnancy were
examined in relation to growth in Latino infants aged birth to 2 years. Depression
during the prenatal and postnatal periods was associated with reduced weight gain in
Latino infants and failure to thrive.
EXPOSURE TO MATERNAL STRESS AND DISTRESS
A large body of research has shown that prenatal exposure to maternal stress influences
fetal as well as infant postnatal development. The types of stress mothers experience
during pregnancy vary from daily hassles to traumatic events. Class, et al. 2011 and Davis
and Sandman 2010 explore the timing of stress exposure as determinants of fetal growth
and infant outcomes. Kinney, et al. 2008 reviews the impact of prenatal environmental
stress and autism. Kingston, et al.
uses a broader construct, distress, that
combines stress with other mental health problems to study impacts on infant outcomes.
Mulder, et al. 2002 includes both human and animal studies in a review of maternal stress
exposure and fetal and birth outcomes. Zhu, et al. 2010 reports finding lower birth
weights in infants born to mothers experiencing stress resulting from severe life events.
Mackey, et al. 2000 and Rondo, et al. 2003 report findings from studies of exposure of
women to multiple stress sources on labor, fetal growth, and birth outcomes.
Class, Quetzal A., Paul Lichtenstein, Niklas Långström, and Brian M. D Onofrio.
.
Timing of prenatal maternal exposure to severe life events and adverse pregnancy
outcomes: A population study of 2.6 million pregnancies. Psychosomatic Medicine
73.3: 234–241. DOI: 10.1097/PSY.0b013e31820a62ce
This investigates the effects of stress exposure and timing on gestational age, preterm
birth, birth weight, and size for gestational age. Greatest impacts were noted during
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the second trimester, particularly months 5 and 6. There are implications for a fetal
programming hypothesis.
Davis, Elysia, and Curt A. Sandman. 2010. The timing of prenatal exposure to maternal
cortisol and psychological stress is associated with human infant cognitive
development. Child Development 81.1: 131–148. DOI: 10.1111/j.1467-8624.2009.01385.x
This empirical study investigates timing of exposure to pregnancy-specific anxiety and
elevated levels of maternal cortisol, with early versus late exposure having opposite
effects on the cognitive performance of infants at 12 months of age. Presumed fetal
programming effects based on cognitive performance in infancy are discussed.
Available online for purchase or by subscription.
Kingston, Dawn, Suzanne Tough, and Heather Whitfield. 2012. Prenatal and postpartum
maternal psychological distress and infant development: A systematic review. Child
Psychiatry and Human Development 43:683–714. DOI: 10.1007/s10578-012-0291-4
This is a review of research on prenatal and postnatal maternal psychological distress and
infant outcomes. Prenatal maternal distress influences cognitive, behavioral, and
psychomotor outcomes, postnatal maternal distress influences socio-emotional and
cognitive outcomes. Discussions on research, clinical, and policy implications are
included. Details on reviewed studies are in tables. Available online for purchase or by
subscription.
Kinney, Dennis K., Kerim M. Munir, David J. Crowley, and Andrea M. Miller. 2008.
Prenatal stress and risk for autism. Neuroscience Biobehavior Review 32:1519–1532.
DOI: 10.1016/j.neubiorev.2008.06.004
This article is a comprehensive review of effects of prenatal exposure to environmental
stress on autism as well as other postnatal abnormalities. Studies reviewed include a
variety of methods and participants (human and animal). Evidence of links between
prenatal stress and autism is provided. The findings have possible implications for
prevention and treatment. Available online for purchase or by subscription.
Mackey, Marlene C., Carol A. Williams, and Cecilia M. Tiller. 2000. Stress, pre‐term
labour, and birth outcomes. Journal of Advanced Nursing 32.3: 666–674. DOI:
10.1046/j.1365-2648.2000.01526.x
The impacts of stress (daily hassles and mood) on birth outcomes were studied in
matched groups of black women and white women, with and without preterm labor.
Stress measures were not related to preterm labor, preterm birth, or birth weight, but
differences within the preterm labor group were found for stress and impacts on birth
outcomes. Available online for purchase or by subscription.
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Mulder, E. J. H., P. G. Robles de Medina, A. C. Huizink, B. R. H. Van den Bergh, J. K.
Buitelaar, and G. H. A. Visser. 2002. Prenatal maternal stress: Effects on pregnancy
and the (unborn) child. Early Human Development 70:3–14. DOI: 10.1016/S03783782(02)00075-0
The article reviews animal and human research studies on maternal stress and its
consequences on pregnancy, fetal development, and birth outcomes. A graphic
detailing these relations is provided. Possible intervention approaches to reducing
prenatal maternal stress and the need for increased awareness of the importance of
stress regulation are discussed. Available online for purchase or by subscription.
Rondo, Patricia H. C., Renato F. Ferreira, Fabane Nogueira, M. C. N. Ribeiro, H. Lobert,
and Rinaldo Artes. 2003. Maternal psychological stress and distress as predictors of
low birth weight, prematurity and intrauterine growth retardation. European Journal
of Clinical Nutrition 57.2: 266–272. DOI: 10.1038/sj.ejcn.1601526
This prospective study investigates impacts of maternal stress, distress, and anxiety on
pregnancy outcomes. Distress, but not stress or anxiety, was related to birth weight
and prematurity at some trimester points, but not to intrauterine growth retardation.
Some obstetric risks (alone or with distress) predicted outcomes.
Zhu, Peng, Fangbiao Tao, Jiahu Hao, Ying Sun, and Xiaomin Jiang. 2010. Prenatal life
events stress: Implications for preterm birth and infant birthweight. American
Journal of Obstetrics and Gynecology 203.1: 34.e1–34.e8.
Exposure to severe life events stress was defined using cut scores on a questionnaire
asking about events and perceptions of events. The prospective study found that
trimester of exposure to severe life events influenced preterm birth and birth weight
outcomes. Other assessed covariates were not systematically related to outcomes.
Available online for purchase or by subscription.
EXPOSURE TO MATERNAL WEIGHT GAIN AND OBESITY
Maternal weight gain is common during pregnancy, but excessive weight gain can be
associated with adverse infant outcomes. Research evidence on effects of weight gain as
well as maternal obesity is important to understanding the bases of concerns about
impacts on weight in infancy and childhood and future health status. Farah, et al. 2011
examines the timing of maternal weight gain and maternal body composition in
influencing infant birth weight. Hull, et al. 2008 and Sewell, et al. 2006 examine how
normal and overweight/obese body mass index (BMI) of mothers influenced that of their
infants. Hull, et al. 2011 finds that obesity, even in women with appropriate gestational
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weight gain (GWG), resulted in infants with more body fat and fat mass. Josefson, et al.
2013 finds excessive GWG in women with normal prepregnancy weight resulted in the
birth of infants with more fat mass and body fat. Modi, et al. 2011 studies relations
between increases in maternal BMI and infant adiposity. Ode, et al. 2012 reports on the
decelerated growth in infants at 3 months who had been born to overweight or obese
mothers. Stothard, et al. 2009 reviews evidence of relations between maternal
overweight or obesity and risks for fetal anomalies.
Farah, Nadine, Bernard Stuart, Valerie Donnelly, Mairead M. Kennelly, and Michael J.
Turner. 2011. The influence of maternal body composition on birth weight. European
Journal of Obstetrics & Gynecology and Reproductive Biology 157.1: 14–17. DOI:
10.1016/j.ejogrb.2010.12.047
Measures of maternal body composition at each trimester were examined for impact on
birth weight. Gestational weight gain before the third trimester, but not early
pregnancy weight gain, influenced infant birth weight. Details on specific measures of
maternal body composition are informative. Available online for purchase or by
subscription.
Hull, Holly R., Mary K. Dinger, Allen W. Knehans, David M. Thompson, and David A.
Fields. 2008. Impact of maternal body mass index on neonate birthweight and body
composition. American Journal of Obstetrics and Gynecology 198.4: 416.e1– 416.e5.
The study examined body weight and composition (percent fat, fat mass, and fat-free
mass) of infants born to women with prepregnancy normal or overweight/obese BMI.
Infants of normal BMI mothers had less percent fat and fat mass and less fat free
mass but no differences in birth weight were found. Available online for purchase or
by subscription.
Hull, Holly R., John C. Thornton, Yin Ji, et al. 2011. Higher infant body fat with excessive
gestational weight gain in overweight women. American Journal of Obstetrics and
Gynecology 205.3: 211.e1–211.e7.
Groups were identified by prepregnancy BMI (normal, overweight, obese) and
gestational weight gain (GWG: appropriate/excessive). Higher percent fat and fat
mass was associated with obesity in both GWG groups. Infants of normal and
overweight women with appropriate GWG had less percent fat and fat mass. Optimal
intervention times for overweight and obese women are discussed. Available online
for purchase or by subscription.
Josefson, Jami L., Joseph A. Hoffmann, and Boyd E. Metzger. 2013. Excessive weight
gain in women with a normal prepregnancy BMI is associated with increased
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neonatal adiposity. Pediatric Obesity. DOI: 10.1111/j.2047-6310.2012.00132.x
This is an empirical study of gestational weight gain (GWG) in women with normal
prepregnancy BMI. Infants of women with excessive GWG had more fat mass and
body fat, indicators of adiposity linked with risk of obesity. Timing of participants’
excessive weight gain was not known. Available online for purchase or by
subscription.
Modi, Neena, Dominika Murgasova, Rikke Ruager-Martin, et al. 2011. The influence of
maternal body mass index on infant adiposity and hepatic lipid content. Pediatric
Research 70.3: 287–291. DOI: 10.1203/PDR.0b013e318225f9b1
Unit increases in maternal BMI of women with normal BMI were examined for impacts on
newborn adipose tissue content and distribution and liver lipid. The authors discuss
evidence needed to establish whether the found relations index life-long trajectories
of health consequences.
Ode, Katie Larson, Heather L. Gray, Sara E. Ramel, Michael K. Georgieff, and Ellen W.
Demerath. 2012. Decelerated early growth in infants of overweight and obese
mothers. Journal of Pediatrics 161.6: 1028–1034. DOI: 10.1016/j.jpeds.2012.06.001
This prospective study investigates maternal prepregnancy BMI and infant outcomes
(weight, length, fat-free mass, and fat mass) at 2 weeks and 3 months. At 3 months
(but not 2 weeks), infants of overweight or obese mothers showed decelerations in
gains. Breastfeeding did not influence the results, and smoking data were not
available. Available online for purchase or by subscription.
Sewell, Mark F., Larraine Huston-Presley, Dennis M. Super, and Patrick Catalano. 2006.
Increased neonatal fat mass, not lean body mass, is associated with maternal
obesity. American Journal of Obstetrics and Gynecology 195.4: 1100–1103. DOI:
10.1016/j.ajog.2006.06.014
The study examined overweight/obese and lean/normal mothers based on BMI and
neonate body composition. Outcomes of infant body composition and weight were
measured along with maternal weight. Heavier infants with increased levels of
adiposity are born to overweight/obese mothers, which may be risk factors for
adolescent obesity metabolic disorder. Available online for purchase or by
subscription.
Stothard, Katherine J., Peter W. G. Tennant, Ruth Bell, and Judith Rankin. 2009.
Maternal overweight and obesity and the risk of congenital anomalies: A systematic
review and meta-analysis. Journal of the American Medical Association 301.6: 636–650.
DOI: 10.1001/jama.2009.113
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This review focuses on the impacts of maternal weight and fetal anomalies (e.g., neural
tube defects, cardiovascular anomalies, cleft palate, limb anomalies). Many of the
hypothesized associations are confirmed. Detailed information is provided on article
selection and meta-analysis methods, study findings for each fetal anomaly, and
sensitivity analyses.
Influence of Prenatal Attachment
Attachment refers to the emotional bond between mother, father, or caregiver and child.
Maternal-infant attachment begins in the prenatal period based on interactions between
mother and fetus in the womb and is influenced by a myriad of variables, including fetal
movement, information from medical imaging, and maternal hormonal change.
Technological advances (such as the ultrasound) have changed the way that a woman
experiences this relationship. The articles in this section address attachment before birth.
Prenatal and postnatal attachment is not the same construct, and do not use the same
measures. However, there is general agreement that both are strongly related to child
outcomes and that prenatal attachment is an antecedent of postnatal attachment. Fetal
attachment refers to a mother’s feeling toward her fetus, and recent literature
emphasizes the transactional nature of the relationship. Alhusen 2008 provides a detailed
review of the breadth of literature on maternal and fetal attachment. Brandon, et al.
2009 includes maternal and paternal attachment research in a review of attachment
theory and research. Cannella 2005 identifies correlated and uncorrelated relations
between attachment and psychosocial, demographic, and pregnancy outcomes. Condon,
et al. 2013 focuses on paternal attachment in a longitudinal study of prenatal and
postnatal attachment. Laxton-Kane and Slade 2002 relates prenatal attachment to the
pregnancy experience and infant care. Perry, et al. 2011 examines attachment quality of
mothers with depression. Shin, et al. 2006 explores relations between mother-fetal and
mother-infant attachment quality. Yarcheski, et al. 2009 reports results of a meta-analysis
of predictors of attachment.
Alhusen, Jeanne L. 2008. A literature update on maternal-fetal attachment. Journal of
Obstetric, Gynecologic, & Neonatal Nursing 37.3: 315–328. DOI: 10.1111/j.15526909.2008.00241.x
This article reviews 22 studies, published since 2000, exploring factors that influence
maternal-fetal attachment. The review defines and reports study findings on the roles
of technology and diagnostics, demographics, mood states, and risk or perceived risk
factors. The section clinical implications and future directions provides information
on research knowledge gaps. Available online for purchase or by subscription.
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Brandon, Anna R., Sandra Pitts, Wayne H. Denton, C. Allen Stringer, and H. M. Evans.
2009. A history of the theory of prenatal attachment. Journal of Prenatal & Perinatal
Psychology & Health 23.4: 201–222.
This article reviews Bowlby’s theory of attachment and attachment theory research.
Prenatal attachment theory and construct measurement studies are described, along
with reviews of published critiques and studies of the relevance of prenatal
attachment to infant outcomes. Research on paternal attachment is also reviewed. A
Cannella, Barbara L. 2005. Maternal-fetal attachment: An integrative review. Journal of
Advanced Nursing 50.1: 60–68. DOI: 10.1111/j.1365-2648.2004.03349.x
This review focuses on 41 studies of mother-fetal attachment. While some significant
correlations are reported, many relations are not significant. The author describes
some short-comings of existing research along with recommendations for needed
research. Available online for purchase or by subscription.
Condon, John, Carolyn Corkindale, Philip Boyce, and Elizabeth Gamble. 2013. A
longitudinal study of father-to-infant attachment: Antecedents and correlates.
Journal of Reproductive and Infant Psychology 31.1: 15–30. DOI:
10.1080/02646838.2012.757694
This empirical study examines father’s prenatal and postnatal attachment to their infants.
A continuity of attachment is documented using self-report measures, along with
measures of some partner characteristics and father emotional well being. Prenatal
attachment measures are more strongly related than postnatal attachment. Clinical
implications of the findings are discussed. Available online for purchase or by
subscription.
Laxton-Kane, Martha, and Pauline Slade. 2002. The role of maternal prenatal attachment
in a woman s experience of pregnancy and implications for the process of care.
Journal of Reproductive and Infant Psychology 20.4: 253–266. DOI:
10.1080/0264683021000033174
This review article examines a variety of factors to determine evidence of impacts on
maternal-fetal attachment. Factors examined include demographics, pregnancy risk,
prenatal care, psychological factors, and social supports. Implications for attachment
of low levels of prenatal attachment and maternal behaviors with known negative
impacts on fetal development are described. Available online for purchase or by
subscription.
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Perry, Deborah F., Anna K. Ettinger, Tamar Mendelson, and Huynh-Nhu Le. 2011. Prenatal
depression predicts postpartum maternal attachment in low-income Latina mothers
with infants. Infant Behavior and Development 34.2: 339–350. DOI:
10.1016/j.infbeh.2011.02.005
This empirical study examines variations in postnatal attachment quality in a sample of
mothers enrolled a prenatal depression prevention trial. Quality of attachment is
related to depressive symptoms in late pregnancy, and pregnancy intention.
Applications to intervention with women who are depressed or at risk are discussed.
Available online for purchase or by subscription.
Shin, Hyunjeong, Young‐Joo Park, and Mi Ja Kim. 2006. Predictors of maternal
sensitivity during the early postpartum period. Journal of Advanced Nursing 55.4:
425–434. DOI: 10.1111/j.1365-2648.2006.03943.x
This empirical study of Korean mothers examines prenatal factors affecting maternal
attachment within 6 weeks of birth. Among the significant predictors is maternal-fetal
attachment. Maternal identify and social support are also associated with attachment.
Available online for purchase or by subscription.
Yarcheski, Adela, Noreen E. Mahon, Thomas J. Yarcheski, Michele M. Hanks, and Barbara
L. Cannella. 2009. A meta-analytic study of predictors of maternal-fetal attachment.
International
Journal
of
Nursing
Studies
46.5:
708–715.
DOI:
10.1016/j.ijnurstu.2008.10.013
This meta-analysis of 72 studies examined relations between 14 predictors and maternalfetal attachment. Moderate predictors included social support and prenatal testing, 10
low predictors included anxiety, self-esteem, depression, age, parity, marital status,
education and high-risk pregnancy was a trivial predictor. The findings are related to
research knowledge gaps and practice. Available online for purchase or by
subscription.
Moderators of Prenatal Development
A simple but common research design is one that explores direct relations between an
independent variable, such as prenatal exposure of a fetus to an auditory stimulus, and a
dependent variable, such as infant habituation to the auditory stimulus. However, more
complex designs can be created to explore the role of moderating variables to determine
if findings exploring direct relations between variables change when moderating
variables are considered. In this section, some examples of recent publications report the
influence of moderating variables in study outcomes. Two studies investigate attachment
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or parenting quality as moderators. Bergman, et al. 2010 investigates mother-infant
attachment as a moderator of prenatal maternal anxiety/stress and infant outcomes,
while Hayes, et al. 2013 investigates parenting quality as a moderator of maternal
depression and infant behavior. Bouchard 2011 explores socialenvironmental variables as
moderator of the quality of prenatal attachment. Buchmayer, et al. 2009 explores the
moderating roles of obstetric and neonatal complications on associations between
preterm birth and autism risk. DiPietro 2010 includes psychological and
psychophysiological variables in considering mother-fetal attachment. Grote, et al. 2010
explores social variables as moderators of maternal depression and infant outcomes.
Schuetze, et al. 2006 finds that maternal anxiety moderated links between cocaine and
sleep problems.
Bergman, Kristin, Pampa Sarkar, Vivette Glover, and Thomas G. O Connor.
.
Maternal prenatal cortisol and infant cognitive development: Moderation by infant–
mother
attachment.
Biological
Psychiatry
67.11:
1026–1032.
DOI:
10.1016/j.biopsych.2010.01.002
This study sought to extend findings from animal studies to humans by investigating the
role of mother-infant attachment as a moderator of maternal anxiety/stress on infant
cognitive development. Findings of relations between prenatal cortisol level and
cognitive impairment was moderated by quality of the mother-infant relationship.
Available online for purchase or by subscription.
Bouchard, Geneviève. 2011. The role of psychosocial variables in prenatal attachment: An
examination of moderational effects. Journal of Reproductive and Infant Psychology
29.3: 197–207. DOI: 10.1080/02646838.2011.592975
This article examines interactions in the mother’s psychosocial environment prenatal
attachment, neuroticism, marital quality, attachment to parents, and pregnancy
planning) to show associations of risk and protective factors on prenatal attachment.
Psychosocial variables influencing fathers’ prenatal attachment are included. Available
online for purchase or by subscription.
Buchmayer, Susanne, Stefan Johansson, Anna Johansson, Christina M. Hultman, Par
Sparén, and Sven Cnattingius. 2009. Can association between preterm birth and
autism be explained by maternal or neonatal morbidity?. Pediatrics 124.5: e817– e825.
This empirical, retrospective study investigates links between prematurity and autism.
Risk of autism is higher in preterm infants, but risk is moderated by obstetric and
neonatal conditions. Complications influencing brain development increase autism
risk. Better understanding of autism risk factors for children born preterm and at term
is needed.
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DiPietro, Janet A. 2010. Psychological and psychophysiological considerations regarding
the maternal–fetal relationship. Infant And Child Development 19.1: 27–38. DOI:
10.1002/icd.651
This theoretical article examines relations between maternal psychological state,
responsiveness and psychophysiological functioning, and fetal response in an effort to
better understand maternal-fetal attachment. The roles of different moderators are
discussed. Available online for purchase or by subscription.
Grote, Nancy K., Jeffrey A. Bridge, Amelia R. Gavin, Jennifer L. Melville, Satish Iyengar,
and Wayne J. Katon. 2010. A metaanalysis of depression during pregnancy and the
risk of preterm birth, low birth weight, and intrauterine growth restriction. Archives
of General Psychiatry 67.10: 1012–1024. DOI: 10.1001/archgenpsychiatry.2010.111
This is a meta-analysis targeting studies of prenatal maternal depression and risks of
preterm birth, low birth weight, and intrauterine grow restriction. Predicted
associations of depression and preterm birth and low birth weight outcomes are
identified, but country location and SES moderate outcomes. The importance of
screening for depression is discussed.
Hayes, Lisa J., Sherryl H. Goodman, and Elizabeth Carlson. 2013. Maternal antenatal
depression and infant disorganized attachment at 12 months. Attachment & Human
Development 15.2: 133–153. DOI: 10.1080/14616734.2013.743256
This study examines the influence of maternal prenatal and postnatal depression,
parenting quality, and infant attachment. Parenting quality is found to moderate the
link between depression and infant attachment quality. Targeting parenting behaviors
could be a fruitful approach for interventions. Available online for purchase or by
subscription.
Schuetze, Pamela, Desirae Lawton, and Rina Eiden. 2006. Prenatal cocaine exposure and
infant sleep at 7 months of age: The influence of the caregiving environment. Infant
Mental Health 27.4: 383–404. DOI: 10.1002/imhj.20097
An empirical study examining the relationship between prenatal cocaine exposure and
infant sleep problems at 7 months of age. Infants exposed to cocaine in utero have
more severe sleep problems. Maternal anxiety positively moderates links between
cocaine and sleep problems. Cocaine-exposed infants in nonparental care had less
severe sleep problems. Available online for purchase or by subscription.