It is interesting that the effects of PNMS on birth outcomes and postnatal development are related to the timing of the exposure. In animals, poorer outcomes are frequently associated with midgestation exposure 1 , 2. Similar findings have been observed in studies of human populations 14 , For example, Glynn et al. Thus, there may exist a critical period during prenatal development when PNMS may have more significant effects on birth outcomes and postnatal development.

Research on PNMS, however, is hampered by methodological constraints. Human studies do not allow stressful events to be randomly assigned during pregnancy and thus lack internal validity. Moreover, naturally occurring events, such as divorce, job loss, or family and marital discord, may not be independent of the woman's own personality, which may also be passed on to her children genetically.

In addition, most human studies of stress have restricted variance; an extremely large sample of pregnant women is required to include a sufficient number who had experienced moderate to high levels of stress. Finally, retrospective studies such as the earthquake study 10 or the studies of war exposure 11 and moderate daily hassles 12 linking increased risk of cognitive delay to prenatal events do not include timely evaluations of the objective severity of the stress exposure at the time of the event.

Moreover, the results of animal studies, which are ideal in their control of prenatal and postnatal environments, cannot be easily extrapolated to humans because humans have many potential risk and protective factors operating between the objective hardship experienced and the emotional and hormonal reactions. The ice storm crisis was clearly a natural disaster that encompassed several of the aspects of a disaster identified by Norris 16 —scope, loss, and threat—as well as a fourth aspect assessed in the present study reflecting change.

Scope is defined here as the extent to which individuals are exposed to the event. As mentioned earlier, the loss of electricity and telephone service directly related to downed power and telephone lines, because of ice build-up, ranged from only several hours to several weeks. Loss is defined here as the tangible loss of people or property. In terms of the present event, 27 deaths were directly related to the ice storm, and extensive damage to homes occurred, especially in the area from which our participants were drawn.

Moreover, many individuals, particularly those from the area from which our participants were drawn, experienced loss of income as businesses and industries were forced to close for lack of electricity. Threat is defined here as an event that threatens the life or well-being of individuals. The ice storm resulted in numerous threats to the life and well-being of individuals from ice falling off of roofs of residential and commercial structures, from lack of potable water as the water treatment plants were functioning at reduced capacities, and from the build-up of carbon monoxide as many individuals were attempting to heat their residences with propane heaters.

Finally, change was defined as the amount of deviation from normal routines caused by the loss of electricity. The ice storm resulted in the relocation of thousands of individuals from their homes to temporary shelters and an increase in the number of families housing guests, particularly in the area from which our participants were drawn.

As such, a large sample of pregnant women in various stages of pregnancy were randomly exposed to varying degrees of storm-related hardship. The present study offers a rare opportunity to examine the effects that quasi-randomly assigned PNMS has on general intellectual and language development, particularly because these abilities are known to be adversely affected by other pre-and perinatal complications, including prematurity 17 ; exposure to toxins such as lead, nicotine, cocaine, or radiation in utero 18 , 19 ; or maternal medical problems during pregnancy, such as the onset of gestational diabetes Given that performance on cognitive measures, such as the Bayley Mental Development Index MDI scores, in infancy are predictive of reading and spelling abilities at 8 y 21 , 22 and general intellectual functioning in later development 23 , short-term effects of PNMS may have long-term implications.

Moreover, although the timing of exposure to stress has been related to birth outcomes and postnatal development 1 , 2 , 6 , 14 , 15 , no research to date has studied the question of timing as it relates to general intellectual and language development in human populations. Our objective was to determine the extent to which the severity and timing of exposure to the ice storm during the pregnancy explains variance in general intellectual and language development of 2-y-olds, above and beyond perinatal factors, such as, gestational age, birth weight, birth complications, and maternal postpartum depression, and socioeconomic status, which have been associated with developmental outcomes.

We hypothesized that toddlers who were born to mothers who experienced higher levels of PNMS would exhibit poorer general intellectual and language functioning. We expected that the effect of PNMS would be greatest in toddlers whose mothers were exposed to the ice storm early in their pregnancies.

Because the present study was designed to provide initial analyses of potential short-term outcomes and because of budgetary limitations, 80 families were selected in which the toddler was not born prematurely and the mother had not smoked or consumed alcohol during pregnancy. Of the families identified for participation in the study, 58 participated in the present study.

An additional 14 families were assessed, but their data were not included in the present analyses as the mothers became pregnant only after the completion of the ice storm. As such, the toddlers of these mothers were not subjected to the effects of the ice storm while in utero.

The remaining eight families did not agree to participate in the study. The present sample was divided into trimester of gestation and gender groups.

Twenty-one toddlers were in their first trimester of gestation, 14 toddlers were in their second trimester of gestation, and 23 toddlers were in their third trimester of gestation when their mothers were exposed to the ice storm. Twenty-seven of the toddlers were boys, and 31 were girls. To ensure the confidentiality of their patients, these obstetricians agreed to mail our first questionnaire Reactions to the Storm to women who met our criteria: being pregnant during the ice storm, French speaking, and 18 y of age or older.

Questionnaire 1 was sent to women. A total of women More importantly, women included their name and address within Questionnaire 1 and allowed us to contact them with a follow-up questionnaire Outcomes of the Pregnancy 6 mo after their due date. Finally, when the children were 2 y of age, the subsample of 58 parents and their children were observed in our laboratory at the Centre de Recherche Fernand-Seguin in Montreal, Quebec, Canada.

In January , mothers who agreed to participate in our study were, on average, 30 y, 5 mo old range: 19 y, 9 mo to 41 y, 7 mo , had completed at least grade 10, and worked, on average, All of the respondents' partners had completed at least grade 10 and worked during the preceding year.

The majority of the respondents owned their own homes Age of mother, education of parents, marital status, job classification of parents, and household income were collected from the parents during our initial questionnaire survey in Socioeconomic status was computed using Hollingshead Index criteria As seen in Table 1 , nearly three quarters of the families in the present sample were categorized as upper-middle or upper class. As such, the families of the toddlers in the present study are representative of the full sample of families who agreed to participate in our larger longitudinal study.

Objective stress was estimated using the mothers' responses to questions from categories of exposure used in other disaster studies: threat, loss, scope, and change Because each natural disaster presents unique experiences to the exposed population, questions pertaining to each of the four categories must be tailored-made Table 2. Each dimension was scored on a scale of 0—8, ranging from no exposure to high exposure.

A total objective stress score was calculated by summing scores from all four dimensions using McFarlane's approach Because there was no theoretical basis to believe that any one of the four dimensions of our scale was more distressing than the other dimensions and on the basis of McFarlane's study of Australian firefighters 27 , each dimension was weighted equally to obtain the total score of our scale.

Total objective stress scores Storm32 ranged from 4 to 20 out of a possible of 32 points. This scale is one of the most widely used measures in the disaster literature for the assessment of distress after trauma.

The item scale describes symptoms from three categories relevant to posttraumatic stress disorder: intrusive thoughts, hyperarousal, and avoidance. Scale items were written to reflect the mothers' symptoms relative to the ice storm crisis. The total score was used in the analyses. Because perinatal factors are frequently associated with general intellectual and specific linguistic outcomes 21 , gestational age, birth weight, number of reported pregnancy and birth complications, and level of postpartum depression were included as potential covariates.

The mothers reported gestational age and birth weights in the questionnaire that they received after the birth of their children Outcomes of the Pregnancy Questionnaire.

In the same questionnaire, the number of obstetric complications was determined by maternal recall using an adaptation of the scale used by Jacobsen and Kinney The level of postpartum depression was assessed using the Edinburgh Postpartum Depression Scale The toddlers' general intellectual abilities were assessed by trained assistants using the Mental Scale of the Bayley Scales of Infant Development 2nd Ed.

Data for the present study were available for 52 of the 58 toddlers. The mothers completed the inventory by indicating which of the words provided that their child either understood receptive language or spoke productive language.

MCDI data were available for 55 of the 58 toddlers. The assistants who evaluated the toddlers' intellectual and language abilities were blind to the extent and timing of the PNMS and to the nature of all covariates. The following statistical procedures were performed on the data. First, descriptive analyses were performed on the three dependent and all of the predictor variables. Second, Pearson Product-Moment correlation coefficients were obtained for all pairs of dependent and predictor variables.

Third, because of the relatively small sample size and because the dependent variables and the majority of predictor variables were continuous in nature, hierarchical multiple regression analyses were performed on each dependent variable. Moreover, because one of the goals of the present study was to determine whether the timing of the PNMS i. Likewise, the gender of the toddler was included in the equation. This method of analysis was used to determine whether the mothers' objective stress exposure in the present study accounted for variance in the dependent variables above and beyond that already accounted for by events and circumstances other than the ice storm.

The means and standard deviations of the dependent and predictor variables and covariates are listed in Table 3. On average, the toddlers' Bayley MDI scores were close to the norm of , with no toddlers scoring within the mentally retarded range i.

On average, the toddlers' MCDI productive language scores were slightly lower than the norm of 65 words for mo-old toddlers. Norms are not available for receptive language. The average gestational age and birth weight of the toddlers were within the normal ranges. On average, scores on the Edinburgh Postnatal Depression Scale were below the cut-off of 12 for clinical depression, with only four mothers scoring in the clinical level. The subjective stress IES-R scores of the mothers were, on average, 9.

As indicated in Table 4 , the level of the mothers' degree of objective stress exposure i. Storm32 was negatively correlated with each of the three dependent variables, indicating that higher levels of objectively measured hardship during the ice storm were associated with lower Bayley MDI scores and lower productive and receptive language abilities. Of the remaining predictor variables, the toddlers' birth weight was negatively correlated with the Bayley MDI scores, and their age at testing was positively correlated with the MCDI productive language scores.

The results of the analysis are presented in Table 5. In the first stepwise block, only the toddlers' birth weight entered the equation and accounted for When the level of PNMS was added, the amount of variance accounted for rose to Examination of the semipartial correlations for each factor indicates that the toddlers' birth weight and the level of PNMS uniquely accounted for 8.

The toddlers' birth weight and the level of PNMS jointly accounted for the remaining 3. As such, the unique contribution of the toddlers' birth weight was reduced once the level of PNMS was entered into the model. The addition of the month of pregnancy during which the toddlers were exposed to the effects of the ice storm did not significantly increase the amount of variance accounted for.

According to the semipartial correlations, the toddlers' birth weight and the level of PNMS uniquely accounted for 9. The remaining 0. As indicated in Table 6 , the toddlers' birth weight was not significantly related to the Bayley MDI scores for toddlers who were exposed to the ice storm when their mothers were in either their first or second trimester of pregnancy.

The toddlers' birth weight did, however, account for However, the level of PNMS accounted for The level of PNMS did not significantly account for any additional variance of the Bayley MDI scores for the toddlers who were exposed to the ice storm when their mothers were in their third trimester of pregnancy.

The results of this analysis are presented in Table 7. The power for the final models was approximated for the linear multiple regressions with two coefficients. Thus, medium-sized and small effects could not be sufficiently detected in our 5-year-follow-up sample. The present study aimed at evaluating possible long-term consequences of emotional stress during pregnancy and postpartum anxiety disorders on mother—child interaction at pre-school age taking infant stress reactivity during infancy into account.

First, our results show that mothers with postpartum anxiety disorders report higher levels of emotional stress during pregnancy. This is in line with previous studies indicating higher levels of perinatal emotional stress in women with postpartum anxiety disorder Britton, Secondly, our study revealed no differences in postpartum cortisol reactivity in infants of mothers with postpartum anxiety disorders and infants of the control group. This is a rather surprising result, as studies describe an association between maternal psychopathology in the postpartum period and the cortisol reactivity of their infants e.

One explanation for this unexpected result could be that our clinical sample consisted of women with various anxiety disorders. Moreover, there might be some methodological reasons for this non-expected finding of our study, for example a missing mean increase in cortisol following the FFSF in our sample. This might be due to the fact, that infant salivary cortisol samples were only taken prior to, immediately after and 20 min after the FFSF.

Consequently, we may not have had a full coverage of the possible cortisol peak times, though many studies have used similar intervals as demonstrated in the review of Gunnar et al. Further research studies should lengthen the observation interval to 30 min as suggested by a review of Provenzi et al.

Second, the finding of a decline in the mean value of infant cortisol-reactivity AUCI may be surprising given the established stressful nature of the FFSF. It must be noted that the lack of reactivity does not imply that the measurement of cortisol reactivity in response to psychological stressors is not meaningful. Rather, it has been argued that the individual differences might bring to light factors that account for the individual differences as well as potential risk factors that may adversely affect infant development.

Moreover, a dampening of cortisol-responses to stressors in rodents and humans during early development Gunnar and Donzella, might play a role for our results. Although the reasons and duration of this dampening period is still unknown, there are many factors affecting stress reactivity.

These include genetic influences Montirosso et al. Furthermore, a recent meta-analysis Provenzi et al. Even though we did not find group differences regarding infant stress reactivity, emotional stress during pregnancy was significantly correlated with infant stress reactivity. This finding adds to the heterogeneous picture about the association between maternal prenatal stress and infant cortisol reactivity.

While some studies report an associations between prenatal stress and modified infant stress reactivity e. As a majority of women in our clinical sample already had perinatal anxiety disorders, it is likely that our results arise from a longer exposure to stress of the fetus due to maternal stress during pregnancy and in the postpartum period.

In contrast, time-limited exposure to stress is usually characterized by high chronicity and are often highly inter-correlated across gestation Davis and Sandman, Further research is needed to disentangle timing and duration influences of maternal stress on infant stress reactivity. The results of our study suggest that maternal stress during pregnancy influences infant development Davis and Sandman, ; Buss et al.

This result of our study could suggest programming influences of maternal psychobiological stress response on the developing fetus, but as the results yield from correlative analyses, we cannot draw causal conclusion. A variety of alternative factors, such as genetics, autonomous nervous and immune system functioning Van den Bergh et al.

In our study, we did not find differences between the clinical and the control group with regard to the quality of interaction at pre-school age. This result was against our hypotheses and could be due to the heterogeneity regarding the anxiety disorders in our sample. Nevertheless, this finding is in line with a number of studies also reporting no difference in mother—infant interaction in mothers with anxiety disorders Murray et al. Although, data about maternal interaction behavior in course of postpartum anxiety disorders is heterogeneous, as some studies did report reduced sensitivity in mothers with anxiety disorders Feldman et al.

Notwithstanding, our results show an association between the quality of dyadic interaction at pre-school age and infant cortisol reactivity in the postpartum period as well as current maternal anxiety symptoms.

Therefore, our results revealed the crucial role of maternal current anxiety symptoms for dyadic reciprocity as well as for dyadic negative states. Dyads with mothers suffering from current anxiety symptoms show lower mutual exchange, collaboration, and joint activity in interaction. Furthermore, these dyads display poor emotional expressiveness, more feelings of discomfort and the atmosphere is tense.

Our results point toward this direction, as infant cortisol reactivity in the postpartum period significantly predicted child socio-emotional development at pre-school age operationalized as dyadic negative states as well as dyadic reciprocity during mother—child interaction. Both interactive patterns, dyadic negative affect and less dyadic reciprocity, can be seen as markers for a lack of emotion regulation skills Feldman, This is in line with a current study by Neuenschwander et al.

Apart from this, our results are in line with recent studies reporting that negative developmental pathways in children with a dysregulation of their HPA-axis function even increase, if familial risks factors are evident, such as parental social anxiety Poole et al. Contrary to our hypothesis emotional stress during pregnancy did not predict mother—child interaction quality at pre-school age. This is in line with the findings of Endendijk et al.

In our study, maternal emotional stress during pregnancy was significantly correlated with infant cortisol reactivity during postpartum period, indicating that especially stress during pregnancy might influence stress reactivity during infancy. Therefore, this research issue should be addressed in further research, at best with a mediation analysis, regarding the influence of infant stress reactivity as a potential mediator between prenatal stress and interaction quality at pre-school age.

Furthermore, future research should address the impact of further confounders, such as child temperament and parenting behavior postpartum. Unfortunately, our study sample was too small to run these analyses, wherefore further research with larger study samples are urgently needed.

The study has some limitations. Firstly, besides a rather small sample size and a low power, especially at the 5-year follow-up, mothers with different anxiety disorders are included in our clinical sample.

Furthermore, a majority of women suffered from more than one anxiety disorder. The sample size does not allow subgroup analyses for the different anxiety disorders, and therefore it is impossible to draw conclusions about the specific effect of different anxiety disorders. Secondly, our sample is characterized by an overproportion of academic degrees, whereby our data is not representative for the overall population.

Thirdly, the maternal stress questionnaire PESI retrospectively assesses emotional stress during pregnancy via self-report which may have affected postpartum answering tendencies. Moreover, it would be of great interest to assess saliva cortisol samples during pregnancy, enabling future studies to analyze the impact of maternal stress during pregnancy for child development prospectively. Fourthly, infant salivary cortisol was assessed prior to, immediately after and 20 min after the Still-Face paradigm.

Due to few samples or the small time frame it is possible that we missed peak cortisol reactivity times, which may in part account for the negative mean cortisol reactivity. Lastly, the study design was observational, causality assumptions are not appropriate. Taken together, our empirical results as well as theoretical assumptions emphasize the importance to further investigate the influence of stress during pregnancy for infant and child development.

Our results underline that emotional stress during pregnancy is linked to infant stress reactivity and this in turn influences mother—child interaction up to pre-school age.

Regarding maternal stress and its influences on infant and child development, it would be of major importance to disentangle different time-effects as well as different kinds of stressors, such as psychological stress, anxiety, or depressive symptoms and life events trauma, loss, or natural disasters. Furthermore, potential moderators should be addressed, such as early life experiences, stress coping strategies, social support or maternal face processing, since current studies show the detrimental effect of anxiety De Carli et al.

With regard to possible long-term consequences for infant and child development early intervention and prevention programs are of vital importance. In sum, the foundation of socio-emotional competencies and especially affect and stress regulation capacities are laid early in life. This study was carried out in accordance with the recommendations of the independent ethics committee of the Heidelberg University Medical Faculty with written informed consent from all subjects in accordance with the Declaration of Helsinki.

A-LZ and MM contributed to the analysis and interpretation of the data, drafting of the manuscript, and final approval of the final version of the manuscript. NN and BD contributed to the study and manuscript conception, and approval of the final version of the manuscript.

CR contributed to the study conception and design, drafting of the manuscript, and final approval of the final version of the manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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The link between stress and fetal brain development is especially disturbing for women who are pregnant during the pandemic, Limperopoulos said, as her prior research has found stress for pregnant women in the era of Covid has doubled or even tripled. Parents and other caregivers are more stressed and in poorer health due to pandemic, report finds.

The impact of maternal stress. Prior research has linked stress, anxiety and depression in pregnant mothers to social, emotional and behavioral problems in their offspring at later ages. Exercise, eat right, get good sleep: The top 3 ways to prevent so many diseases. Clinical studies have found neurobehavioral deficits, such as impaired motor coordination, higher emotional reactivity and language delays in children born to stressed mothers.

Limperopoulos published a study earlier this year that found high levels of stress during pregnancy impaired a baby's brain biochemistry and the growth of the hippocampus -- the area of the brain involved in the formation of new memories, which is also associated with learning and emotions.

Prior studies have also found unusual electroencephalographic patterns in the frontal lobes of children, along with changes in the white matter responsible for organizing communication between the various parts of the brain. Stress has also been linked to preterm birth.

Women who felt overwhelmed and unable to cope during the months and even years before conception had shorter pregnancies than other women, according to a study published in July. Another study published this month found that maternal stress -- even before conception -- can shorten the length of a baby's telomeres, the compound DNA structures located at the tips of our chromosomes.

Think of telomeres as the protective plastic caps on the ends of your shoelaces. Shortened telomeres have been linked to a higher risk of heart disease, cancers and earlier death.

Stress among low-risk pregnancies. The latest study in JAMA Open Network analyzed the stress levels of 50 women whose pregnancies were between 24 and 39 weeks and considered low risk due to the expectant mothers' higher sociodemographic category.

These well-educated, professional women were already healthy "control" volunteers in a larger study on fetal brain development. None of the women were on medication.