Bruckner et al. BMC Public Health 2010, 10:273
Male fetal loss in the U.S. following the terrorist
attacks of September 11, 2001
© 2010 Bruckner et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons
Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.
Tim A Bruckner*1, Ralph Catalano2 and Jennifer Ahern2
Background: The secondary sex ratio (i.e., the odds of a male birth) reportedly declines following natural disasters,
pollution events, and economic collapse. It remains unclear whether this decline results from an excess of male fetal
loss or reduced male conceptions. The literature also does not converge as to whether the terrorist attacks of
September 11, 2001 induced "communal bereavement", or the widespread feeling of distress among persons who
never met those directly involved in the attacks. We test the communal bereavement hypothesis among gravid
women by examining whether male fetal deaths rose above expected levels in the US following September 11, 2001.
Methods: We apply interrupted time-series methods to all fetal deaths at or greater than the 20th week of gestation in
the US from 1996 to 2002. Time-series methods control for trends, seasonality, and other forms of autocorrelation that
could induce spurious associations.
Results: Results support the hypothesis in that the fetal death sex ratio (i.e., the odds of a male fetal death) increased
above its expected value in September 2001. Additional analysis of the secondary sex ratio indirectly supports that the
terrorist attacks may have threatened the gestation of male more than female fetuses.
Conclusions: Societal responses to events such as September 11, 2001 do not appear confined only to persons who
have ever met the deceased. The fetal death sex ratio in the US population may serve as a sentinel indicator of the
degree to which pregnant women react to population stressors.
The secondary sex ratio (i.e., the odds of a male birth)
reportedly falls in populations subjected to natural disas-
ters , pollution events , and the contraction or col-
lapse of economies [3,4]. Drops in the secondary sex ratio
deserve public health attention because the literature
indicates that male fetal loss may contribute to this
decline  Although the biological mechanism remains
unclear, male fetuses appear more sensitive than female
fetuses to maternal corticosteroids produced after the
twentieth week of gestation [6,7]. This elevated stress
reactivity apparently jeopardizes the viability of males in
utero. Consistent with the theory of natural selection,
humans may have conserved this male fetal sensitivity to
maximize the mother's total yield of grandchildren .
One study in California suggests male fetal loss may fol-
low stressful events. The authors report that ambient
economic decline precedes an increased risk of a male
fetal death . Mechanisms other than male fetal loss,
however, may account for the inverse association
between environmental stressors and the secondary sex
ratio. Ambient stressors may decrease the odds of a male
conception by reducing sperm motility or the frequency
of coitus [10,11]. Fukuda and colleagues, for instance,
found sub-optimal sperm motility among Japanese males
after the Kobe earthquake .
Distinguishing between the male fetal loss and reduced
male conception explanations holds implications for pub-
lic health. Whereas reduced male conceptions may inter-
est basic researchers, fetal loss induces psychological, if
not somatic, morbidity. Mothers who report a stillbirth or
spontaneous abortion also exhibit an elevated incidence
of subsequent adverse birth outcomes [13,14]. For these
reasons, fetal loss remains the object of much clinical
The terrorist attacks of September 11, 2001 induced
widespread social and economic disruption, leading to
high levels of stress and anxiety in the United States pop-
* Correspondence: firstname.lastname@example.org
1 Public Health & Planning, Policy and Design, University of California at Irvine,
Irvine, CA, USA
Full list of author information is available at the end of the article
Bruckner et al. BMC Public Health 2010, 10:273
Page 2 of 6
ulation [15-17]. The attacks' discrete temporal nature
allows us to test whether and when they increased male
fetal loss. One report of the fetal death sex ratio (i.e., odds
of a male fetal death) after September 11 appears in the
literature. In California, the fetal death sex ratio increased
one month after the attacks . Reports in California
and New York City also indirectly support the male fetal
loss explanation, as the secondary sex ratio decreased
three and four, but not eight, nine, or ten, months after
the attacks .
These findings raise the obvious question of whether
male fetal loss increased in the remainder of the United
States (U.S.) following the terrorist attacks. This test
could assist in understanding the extent to which preg-
nant mothers experienced "communal bereavement" after
September 11. Although most research on bereavement
concerns individuals with direct relationships to the
deceased, work by Catalano and Hartig  indicates
perinatal sequelae among the broader society without
such social ties. The authors posit that a nation's popula-
tion of pregnant women may experience widespread dis-
tress even if they never met the deceased, particularly
after events in which institutions such as the state fail to
maintain safety and security for its members. We believe
that the terrorist attacks of September 11, 2001 meet this
condition. Much epidemiologic literature, moreover,
reports a nationwide increases in acute mental distress
following the attacks of which the overwhelming majority
of respondents had no direct relationship to the deceased
[15-17]. We also know of no reports that pregnant
women in particular sheltered themselves from this dis-
We test the communal bereavement hypothesis that the
fetal death sex ratio in the U.S. (less California) rose
above its expected level following September 11, 2001.
Consistent with theory and earlier empirical research, we,
as described below, focus our fetal loss test in September,
October, and November 2001 . If results support
male fetal loss, we then test the attending hypothesis that
the secondary sex ratio in the U.S. (less California and
New York City) will fall below its expected value two,
three, or four months after September 11, 2001.
Variables and Data
We use the fetal death public use data files (1996-2002)
from the National Vital Statistics System, which compiles
fetal death data from all fifty of the United States .
The National Center for Health Statistics (NCHS) defines
a fetal death as a
"death prior to the complete expulsion or extraction
from its mother of a product of human conception,
irrespective of the duration of pregnancy and which is
not an induced termination of pregnancy.
The death is indicated by the fact that after such
expulsion or extraction, the fetus does not breathe or
show any other evidence of life ..."
Most states require reporting of fetal deaths at or above
20 weeks of gestation. Although six states report fetal
deaths before 20 weeks, 99% of these deaths have no
information on sex. We therefore restricted our analysis
to non-elective fetal deaths at or greater than 20 weeks.
Several quality assessments indicate underreporting of
fetal deaths, especially those during the 20th to 27th
weeks of gestation . No research, however, suggests a
sex bias in the reporting. Although several variables on
the fetal death records frequently have missing values
(e.g. prenatal care), fetal sex rarely has no value .
From January 1996 to December 2002, the NCHS
imputed the sex of 4.65 percent of fetal deaths. To avoid
potential misclassification of sex status, we excluded
these deaths from the analysis.
We acquired birth public use data files (1996-2002) from
the National Vital Statistics System, which compiles birth
certificate data from all registered births in the United
States . NCHS collaborates with state governments to
provide access to information contained on all birth cer-
tificates in the U.S. NCHS makes these data available to
the public; the data do not contain personal unique iden-
tifiers. Reporting of births in the U.S. is believed to be
more than 99% complete .
We use interrupted time-series designs to test the
hypotheses that the United States fetal death sex ratio
rose following September 11, 2001. Researchers typically
assume that, under the null hypothesis, the statistically
expected value of a variable is its mean. The fetal death
sex ratio, however, may exhibit secular trends, seasonal
cycles, or the tendency to remain elevated or depressed
after high or low values. These patterns, referred to col-
lectively as autocorrelation, complicate hypothesis tests
because the expected value of an autocorrelated series is
not its mean.
Researchers have adjusted for autocorrelation by
"decomposing" time series into predictable and residual
components. This approach removes temporal patterns
from the dependent variable before testing the effect of
the independent variable and precludes spurious associa-
tions due to shared autocorrelation. Our analysis, there-
fore, is net of seasonality or other patterns in the sex ratio
of fetal deaths.
We implemented the approach, recommended in the
epidemiologic literature, through the following steps .
First, we used Auto Regressive, Integrated, Moving Aver-
Bruckner et al. BMC Public Health 2010, 10:273
Page 3 of 6
age (i.e., ARIMA) methods to detect and model autocor-
relation in the fetal death sex ratio from January 1996
through December 2002 . The residuals of this model
exhibit no autocorrelation and have an expected value of
Second, we added a dichotomous variable scored 1 for
September 2001 and 0 otherwise to the best fitting
ARIMA models for the fetal death sex ratio. We specified
the model such that we could measure the association
between the fetal death sex ratio and September 11 for
three monthly birth cohorts starting on September 2001
and ending November 2001.
Third, we estimated the equations resulting from step 2
and inspected their residuals to detect any autocorrela-
tion. If any autocorrelation was detected, we added
ARIMA parameters and estimated the resulting models.
Fourth, we removed from the initial models any coeffi-
cients that did not reach conventional levels of statistical
significance (p < .05).
Fetal Death Sex Ratio
Over the test period, the mean numbers of reported
monthly male and female fetal deaths in the U.S. (less
California) were 995 and 871, respectively. The mean
fetal death sex ratio was 1.14. As indicated in Table 1.,
non-Hispanic white mothers accounted for 49 percent of
the fetal deaths, and over one-half of all deaths occurred
to mothers with an education at or below high school.
The fetal death sex ratio series exhibited autocorrela-
tion in that high or low values were followed twelve
months later by smaller outlying values in the opposite
direction. We removed this pattern (best modeled as an
autoregressive process at a lag of 12 months, see Table 1)
from the series before adding the binary September 11
Table 2 shows the results of the final model in which we
add a constant, the September 11 variable, and any dis-
covered autocorrelation. Consistent with the male fetal
loss explanation, the U.S. fetal death sex ratio (less Cali-
fornia) rose above its expected value in September 2001.
Fetal death sex ratios in October and November 2001,
however, did not differ significantly from expected val-
We conducted several tests to determine if our result
remained robust to control for potential analytic artifacts.
To address whether outliers in the fetal death sex ratio
affected the results, we applied outlier detection and cor-
rection routines to our original analyses . The posi-
tive coefficient at September 2001 increased and
remained statistically significant (coefficient = .1477, SE =
.0377, p < .001, 1-tailed test). To ensure that non-constant
variance of the series over time did not distort our esti-
mates, we transformed the fetal death sex ratio to its nat-
ural logarithm and estimated the test equation again.
Results, other than the metric of the September 2001
coefficient, remained essentially the same (.1111, SE =
.0400, p < .01).
The month of September may exhibit unexpectedly
high fetal death sex ratios even after we controlled auto-
correlation at the twelfth month. We checked the robust-
ness of our finding against this possibility by including as
a control variable an indicator for all Septembers and re-
estimating the equation. The coefficient for September
2001 remained positive and statistically significant (0.112,
SE = .0552, p < .05).
We also examined whether results appear similar when
we included all states in the analysis (i.e., adding Califor-
nia). As in the original test, the coefficient for September
2001 supports male fetal loss (0.103, SE = .047, p < .05)
(full results available upon request).
Secondary Sex Ratio
Support for the above hypothesis led us to test whether
male fetal loss could also be detected via a fall in the sec-
ondary sex ratio two, three, or four months after the ter-
rorist attacks. We applied the time series routines
described above to the monthly secondary sex ratio
Table 1: Descriptive characteristics of fetal deaths >20
weeks of gestation in the United States (less California),
1996-2002 (n = 156,510).
< 18 years10,013 6.40
18-25 years 58,65837.48
26-34 years62,123 39.69
≥ 35 years 25,71616.43
Less than high school graduate 30,82319.69
High school graduate50,812 32.47
Some college 26,80617.13
College graduate 24,37415.57
Non-hispanic white 76,31648.76
Non-hispanic black42,782 27.33
Bruckner et al. BMC Public Health 2010, 10:273
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series. Unlike the earlier test, we measure the association
between September 11 and the secondary sex ratio start-
ing on November 2001 and ending January 2002. We cen-
ter the test on December 2001 since an excess of male
fetal loss, particularly from 20 to 28 weeks of gestation,
immediately after September 11 could precede a reduced
odds of a male birth 12 weeks later (i.e., an estimated 32
to 40 weeks gestation). Research in California and New
York City, moreover, reports lower than expected second-
ary sex ratios in December 2001 and January 2002,
The NCHS recorded 23,604,405 births in the U.S. (less
California and New York City) over the seven-year test
period. The mean monthly secondary sex ratio was 1.048.
The secondary sex ratio series exhibited seasonality in
that high or low values were followed six months later by
smaller outlying values in the opposite direction. We
removed this pattern (best modeled as an autoregressive
process at a lag of 6 months, see Table 3) from the series.
The ARIMA model also detected that unusually high or
low values were "remembered" into the following month
(modeled as an autoregressive process at a lag of 1
Table 3 displays the results in which we add a constant,
the September 11 variable, and any discovered autocorre-
lation. The secondary sex ratio in December 2001 fell
below its expected value (coefficient = -.0079, SE = .0039,
p < 0.05, 2-tailed test).
We tested whether outliers in the series may have
inflated the variance . No outliers were detected. We
also transformed the secondary sex ratio to its natural
logarithm to ensure that non-constant variance did not
distort our findings. The coefficients did not appreciably
change. We then tested the possibility that our findings
arise from predictably low secondary sex ratios in all
Decembers by adding an indicator variable for all Decem-
bers and re-estimating the equation. The December 2001
coefficient remained negative and increased in magni-
tude (-.0107 SE = .004, p < .01).
We then included data from California and New York
City to determine whether the secondary sex ratio in the
entire U.S. fell after September 11. The results support a
drop in the secondary sex ratio in December 2001 as the
coefficient was negative and statistically significant (-
.0069, SE = .0036, p < .05, 1-tailed test) (results available
Analysis of fetal deaths in the U.S. (less California) indi-
cates that the terrorist attacks of September 11 coincided
with an increase in the fetal death sex ratio in September
2001. Results converge with findings in California and
support the communal bereavement hypothesis in that
ambient shocks may affect the U.S. population of gravid
mothers by threatening the gestation of male more than
female fetuses .
The communal bereavement hypothesis contends that
societies may react adversely to unsettling national events
despite having no direct connection to persons involved
in these events. This hypothesis builds on reports that
witnessing harm to others triggers physiological
responses in the witness that mirrors those in the persons
harmed . These responses can include the production
Table 2: Coefficients for model of the fetal death sex ratio
(i.e., male/female) in the United States (less California) for
September, October, and November 2001. Standard errors
appear in parentheses.
Predictor Initial modelFinal model
Constant 1.143** (.0036)1.143** (.0035)
AR at 12 -.4823** (.1132)-.4713** (.1103)
AR at 3 -.2558* (.1188)-.2657* (.1164)
September 11 variable lagged at:
September 2001 .1279** (.0466).1232** (.0468)
October 2001 .0196 (.0463)
November 2001 .0076 (.0462)
* p < 0.05, 2-tailed test
** p < 0.01, 2-tailed test
Table 3: Coefficients for initial and final model of the
secondary sex ratio in the United States (less California and
New York City) for November 2001, December 2001 and
Predictor Initial modelFinal model
Constant1.048* (.0005) 1.048* (.0004)
AR at 1.2403* (.1136) .2487* (.1108)
AR at 6-.2294* (.1128) -.2353* (.1097)
MA at 16.2986* (.1249) .2933* (.1243)
September 11 variable lagged at:
November 2001 -.0019 (.0038)
December 2001-.0079* (.0039) -.0074* (.0036)
January 2002-.00005 (.0038)
Standard errors appear in parentheses.
* p < 0.05, 2-tailed test
Bruckner et al. BMC Public Health 2010, 10:273
Page 5 of 6
of corticosteroids alluded to above as those implicated in
the spontaneous abortion of males .
The literature reports that between 10 to 30 percent of
fetal deaths greater than 20 weeks gestation are registered
with state and federal vital statistics departments [30,31].
This under-registration indicates that using our discov-
ered coefficient to estimate the total number of male
fetuses lost in the U.S. as a result of September 11 would
most likely approximate the lower bound of the true
Strengths of our study include the population-based
nature of NCHS data and coverage of over 156,000 fetal
deaths over the test period. We have, in fact, tested our
theory in the universe of exposed gestations. Use of this
large population avoids instabilities in sex ratios associ-
ated with small numbers of fetal deaths. We also tested a
population shock that assessments independent of ours
established as stressful. The shock, moreover, affected the
population at an unambiguous point in time allowing us
to use the temporal patterning of responses to test male
fetal loss. Results cannot arise from trends, seasonality, or
other temporal patterns in the fetal death sex ratio
because our methods removed autocorrelation.
Limitations of our test include the welcomed rarity of
population stressors such as the events of September 11,
2001. Our findings may not generalize to other, more
commonly experienced stressors on the population,
although analyses in California suggest that regular
swings in the economy may affect male fetal deaths . In
addition, we cannot know when in gestation (e.g., 20-24th
week, 24-28th week, etc.) male fetuses appear most sensi-
tive to population stressors. Whereas the NCHS gathers
information on gestational age of the fetus, this variable
often receives no score and has questionable accuracy
even when reported . Data limitations also preclude
examination of physiologic mechanisms that may con-
nect population stressors to male fetal loss. We await fur-
ther research to identify these mechanisms.
Consistent with male fetal loss, the secondary sex ratio
fell three months after the attacks. This finding indicates
that an excess of males scheduled to be born in December
2001 may have been lost in utero due to the sequelae of
the terrorist attacks. We also explored whether the sec-
ondary sex ratio in the entire U.S. fell below expected val-
ues eight, nine, and ten months after September 11, 2001.
A decline in the secondary sex ratio in any of these
months would support the reduced male conceptions
argument. Findings provide no evidence for reduced male
conceptions in that the secondary sex ratios eight, nine,
and ten months after the terrorist attacks did not differ
from expected values (results not shown).
A recent study of active-duty military families found no
drop in the live birth sex ratio among mothers in their
first trimester during September 11, 2001 . We recon-
cile our findings with this null result in two ways. First,
consistent with the literature that reports heightened
male sensitivity to stressors after the 20th week of gesta-
tion, we specified an induction period of 3 to 5 months
(rather than 7 to 9 months) between the terrorist attacks
and the birth sex ratio [6,7,18,19]. Second, our examina-
tion of the universe of gestations in the US may permit
identification of sex ratio changes that would remain oth-
erwise undetected when studying samples.
Despite the fact that the fetal death rate after the 20th
week of gestation (6.2 deaths per 1,000 live births and
fetal deaths) approaches the infant mortality ratio (6.9
deaths per 1,000 live births), relatively little research and
public health attention has focused on fetal death [31,33].
This circumstance arises in part from the lack of etiologic
knowledge and perceived lack of opportunities for pre-
vention. Here we report one population-based test that
furthers understanding of psychosocial antecedents of
fetal death. Results, moreover, suggest that the fetal death
sex ratio may serve as a sentinel indicator of the degree to
which pregnant women, at least, react to population
The authors declare that they have no competing interests.
TAB co-designed the research question, retrieved the data, performed the sta-
tistical analysis, and served as the lead author of the manuscript. RC co-
designed the research question, assisted with the statistical analysis, and co-
authored the Methods and Discussion. JA assisted with the research design,
performed the data management, assisted with interpretation of the data, and
edited all sections. All authors read and approved the final manuscript.
The Ruth L. Kirschstein National Research Service Award (T-32, no. HS-00086-
09) offered through the Agency for Healthcare Research and Quality supported
the research described in this manuscript.
1Public Health & Planning, Policy and Design, University of California at Irvine,
Irvine, CA, USA and 2School of Public Health, University of California at Berkeley,
Berkeley, CA, USA
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Received: 30 November 2009 Accepted: 25 May 2010
Published: 25 May 2010
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Cite this article as: Bruckner et al., Male fetal loss in the U.S. following the
terrorist attacks of September 11, 2001 BMC Public Health 2010, 10:273