Journal of Psychosomatic Res

Lower birth weight of Dutch neonates who were in utero at the

time of the 9/11 attacks

Luc Smitsa,4, Lydia Krabbendamb, Rob de Biea, Gerard Essedc, Jim van Osb

aDepartment of Epidemiology, Care and Public Health Research Institute, Maastricht University, Maastricht, The NetherlandsbDepartment of Psychiatry and Neuropsychology, South Limburg Mental Health Research and Teaching Network,

European Graduate School of Neuroscience Maastricht, Maastricht University, Maastricht, The NetherlandscDepartment of Obstetrics and Gynaecology, Maastricht University, University Hospital, Maastricht, The Netherlands

Received 25 August 2005; received in revised form 24 April 2006; accepted 27 April 2006

Abstract

Objective: Maternal stress during pregnancy has been reported

to have an adverse influence on fetal growth. The terrorist attacks

of September 11, 2001, on the United States have provoked

feelings of insecurity and stress worldwide. Our aim was to test

the hypothesis that maternal exposure to these acts of terrorism via

the media had an unfavorable influence on mean birth weight in the

Netherlands. Methods: We compared birth weights of 1885 Dutch

neonates who were in utero during the attacks with those of 1258

neonates who were in utero exactly 1 year later. Results: In the

0022-3999/06/$ – see front matter D 2006 Elsevier Inc. All rights reserved.

doi:10.1016/j.jpsychores.2006.04.020

4 Corresponding author. Department of Epidemiology, P.O. Box 616,

6200 MD, Maastricht University, Maastricht, The Netherlands. Tel.: +31 43

3882821.

E-mail address: luc.smits@epid.unimaas.nl (L. Smits).

exposed group, birth weight was lower than in the nonexposed

group (difference, 48 g; 95% confidence interval=13.6, 82.9;

P=.006). The difference in birth weight could not be explained by

tobacco use, maternal age, parity, or other potential confounders or

by shorter pregnancy durations. Conclusion: These results provide

evidence supporting the hypothesis that exposure of Dutch

pregnant women to the 9/11 events via the media has had an

adverse effect on the birth weight of their offspring.

D 2006 Elsevier Inc. All rights reserved.

Keywords: Birth weight; Netherlands; Pregnancy; September 11 Terrorist Attacks; Stress; Psychological

Introduction

The terrorist attacks against the United States on

September 11, 2001, had a profound psychological impact,

both on those directly involved and on those that were

exposed to them via the media. Seventeen percent of the

U.S. population outside of New York reported symptoms of

9/11-related posttraumatic stress 2 months after the attacks

[1]. Women were found to be more liable to posttraumatic

stress after these events than men (odds ratio, 1.64), and so

were individuals who suffered from anxiety or depression

before the events (odds ratio, 1.84). Since pregnant women

exhibit higher rates of depression and anxiety, exposure to

the 9/11 attacks via the media may have had relatively high

psychological impact within this group.

Experimental animal studies and human studies have

shown associations between maternal stress and pregnancy

outcome [2,3]. Increased risks have been found for, among

others, low birth weight and preterm delivery. We hypothe-

sized that women who were pregnant at the time of the 9/11

attacks on the United States gave birth to smaller babies and

had shorter pregnancy lengths than a comparable group of

women who were pregnant exactly 1 year later.

Methods

We used data from a prospective cohort study of

pregnancy-related pelvic girdle pain, conducted in 2001,

2002, and 2003 in the southeastern part of the Netherlands

[4]. For this study, women were recruited by midwives and

earch 61 (2006) 715–717

Fig. 1. Mean birth weight of offspring of 1885 Dutch women pregnant on

September 11, 2001 (white bars), and of offspring of 1258 Dutch women

pregnant on September 11, 2002 (gray bars).

L. Smits et al. / Journal of Psychosomatic Research 61 (2006) 715–717716

gynecologists at the time of the women’s first visit in

connection with their pregnancy (around 14 weeks of

pregnancy). An initial questionnaire was handed out then,

and subsequent questionnaires were sent by mail at around

30 weeks of pregnancy, as well as at 2 weeks and at 6 and

12 months after delivery. An additional questionnaire

(obstetric record) was completed by the midwife or

gynecologist who carried out the delivery.

Of the 4995 women under study, 1885 women were

pregnant at the time of the 9/11 attacks and did not deliver

before 24 weeks of pregnancy (hereafter, they will be

collectively called the exposed group). We compared the

pregnancy outcomes of these women with those of mothers

who were pregnant on September 11, 2002, and who did not

deliver before 24 weeks of pregnancy (n=1258, hereafter,

they will be collectively called the nonexposed group). In

this way, we accounted for possible seasonal influences on

pregnancy outcome [5].

We additionally excluded preterm births (37 weeks of

gestation or less) from both groups (n=185), except in the

analysis of gestational length. Since the impact of stress may

vary with the period of gestation, pregnancy outcome was

compared both unstratified and stratified by pregnancy

trimester (i.e., being in the first, second, or third trimester on

September 11). Pregnancy trimester was calculated on the

basis of the date of delivery combined with pregnancy term

at delivery as estimated by gynecologists and midwives on

the basis of ultrasound testing or the date of the last

menstrual period.

We used multiple regression analysis in order to control

for the following potentially confounding factors: maternal

age (five categories), maternal length (four categories),

prepregnancyweight (six categories), educational level (three

categories: low, medium, or high), parity (two categories:

either primiparous or not), pregnancy-induced hypertension

(two categories: present or absent), and use of tobacco

(two categories: present or absent). Information on preg-

nancy-induced hypertension was derived from the obstetrical

record; the remaining information was provided by the

women via questionnaire at around 14 weeks of pregnancy.

The model with birth weight as the outcome was

additionally adjusted for duration of pregnancy. We carried

out t tests and regression analyses using the STATA

statistical package (version 8).

Results

In the group exposed to the 9/11 attacks during

pregnancy, mean birth weight was 3489 g (S.D.=474),

whereas in the nonexposed group, mean birth weight was

3537 [S.D.=478; difference, 48 g; 95% confidence interval

(CI)=14, 83; P=.006]. Differences in mean birth weight

were equally large for exposure during the second trimester

(67 g; 95% CI=6, 129; P=.031) and the third trimester (71 g;

95% CI=18, 24; P=.008; Fig. 1). No meaningful difference

was observed for exposure during the first trimester (�2 g;

95% CI=�84, 79; P=.960). After adjustment for potential

confounders, the associations between exposure to the

attacks and birth weight increased somewhat (difference,

58 g; 95% CI=25, 92; P=.001). Additional adjustment for

duration of pregnancy reduced the association, but the

difference remained statistically significant (difference, 38 g;

95% CI=7, 69; P=.017).

Pregnancy duration did not differ much between the

exposed and the nonexposed groups (mean durations:

278.2 days, S.D.=11.4, and 278.9 days, S.D.=11.1, respec-

tively; difference, 0.7 days; P=.07), although the difference

was in the expected direction. For Trimesters 1, 2, and 3, the

respective differences were as follows: �0.7 days (95%

CI=�2.8, 1.4; P=.52), 1.1 days (95% CI=�0.4, 2.6), and0.5 days (95% CI=�0.7, 1.6).

Discussion and conclusion

Two other studies have been devoted to pregnancy

outcomes in relation to the 9/11 events. Both studies were

carried out among women living or present in the New

York City area at the time of the events. One study showed

that living in the proximity of the World Trade Center

(WTC) at the time of the disaster had led to a decrease in

mean birth weight of 122 g and smaller mean birth length

(�0.74 cm) [6], while the other study reported a twofold

increase in the risk of intrauterine growth retardation among

neonates of women present in five exposure zones near

the WTC on September 11, 2001, 0900 h, or within the

succeeding 3 weeks [7].

Two possible explanations have been proposed for the

unfavorable reproductive effects among these women, the

first being exposure to dust and toxins from the WTC and

the other being maternal stress induced by the events [6,7].

Since exposure to dust or environmental toxins is an

unlikely explanation for the differences in mean birth

weight among the children in our Dutch cohort, the most

plausible mechanism would be that point exposures to high

levels of maternal stress may influence fetal growth.

L. Smits et al. / Journal of Psychosomatic Research 61 (2006) 715–717 717

Although we were not able to adequately measure levels of

stress and anxiety in our population during the first months

after September 11, 2001, and September 11, 2002, other

authors have observed a rise in PTSD symptoms and a rise

in suicidal behavior in the Dutch population in the aftermath

of the terrorist attacks [8,9].

Mulder et al. [2] have proposed several mechanisms by

which maternal stress may reach the fetus and exert

unfavorable effects on fetal growth and gestational length.

First, although a large part of maternal cortisol is converted

in the placenta to the biologically inactive cortisone, rises in

maternal cortisol have been shown to lead to higher cortisol

levels in the fetus. Second, activation of the maternal

sympathetic nervous system by stress may lead to reduced

blood flow to the uterus and fetus, which may contribute to

fetal growth restriction. Third, maternal stress provokes

increased secretions of maternal and placental corticotropin-

releasing hormone, which in turn may initiate a cascade of

events that eventually lead to (early) delivery.

An alternative explanation of our findings could be that

there is a trend of increasing birth weight over the years. We

evaluated this possibility by carrying out regression analyses

of birth weight and gestational duration as a function of time

(days) for children not included in the analysis. These

children were conceived during the following periods: July

2000 to January 2001, September 2001 to January 2002, and

September 2002 to October 2002. The results of the

regression analyses indicate that there were no time trends

in birth weight (b=.03057; P=.55) or gestational duration(b=�.00113; P=.36).

The finding that the effects on birth weight were

confined to the second and third trimesters of pregnancy

is at odds with the observation of some authors that

maternal stress is more harmful during the first trimester, as

opposed to the second and third trimesters of pregnancy

[10]. Notably, the two aforementioned studies of repro-

ductive outcomes after the 9/11 events also did not observe

any statistically significantly larger effect on birth weight,

after controlling for gestational duration, and exposure

during the first trimester as opposed to later exposure [6,7].

Without adjustment for gestational duration, one study

found larger effects for women whose first trimester

encompassed the 9/11 events (�104 g, P=.057) [6]. In

that study, there was also a statistically significant effect of

first-trimester exposure, as opposed to later exposure, on

gestational length (�3.55 days, P=.001).

The external validity of these findings is not easy to

judge. The magnitude of the carnage is unmatched, and the

events brought about immediate and sweeping changes on

the levels of politics, society, and individual psychology.

We surmise that more recent terrorist acts, like the

bombings in Bali, as well as in Madrid and London, did

not have as large an impact on levels of stress, unsafety,

and anxiety worldwide as did the 9/11 events. However,

surviving victims, relatives of affected individuals, or

people living or working close to the afflicted areas may

have experienced more serious psychological effects from

these bombings than from the attacks in New York City

and Washington, DC.

In conclusion, our data provide evidence supporting the

hypothesis that exposure of Dutch pregnant women to the

9/11 terrorist attacks via the media has had a small

unfavorable effect on mean birth weight of their offspring.

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