A decrease in sex ratio at birth nine months after the earthquake in L'Aquila.

Abstract

Multiple factors influence the secondary sex ratio (SSR) including stress, which appears to affect mainly the males born.
We evaluate the effects of the earthquake in L'Aquila on the SSR.
The SSR for the first six months of 2010 was compared to that of the same period of 2008. The chi-square test and Fisher's test were used for the statistical analysis.
Nine months after the earthquake, an important reduction in the SSR was recorded: January 2010 versus January 2008 =0.62 versus 0.96. An overall fall in the SSR was also recorded when the first 3 months of 2010 were compared to the first three months of 2008: 0,82 versus 1,11. When the first three months of 2010 were compared with the second three months of 2010, a statistically significant increase of the sex ratio at birth was noted (0,82 versus 1,27).

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The Scientific World Journal
Volume 2012, Article ID 162017, 3 pages
doi:10.1100/2012/162017
The cientificWorldJOURNAL
Research Article
ADecreaseinSex Ratio at BirthNineMonths after the
EarthquakeinL’Aquila
A.D’Alfonso,1F.Patacchiola,2I.Colagrande,1G.D’Alessandro,1
A.DiFonso,1P. Palermo,1andG.Carta1
1Department of Gynecology and Obstetrics, San Salvatore Hospital, L’Aquila, Italy
2Department of Health Sciences, University of L’Aquila, 67100 L’Aquila, Italy
Correspondence should be addressed to G. Carta, gasparecarta@libero.it
Received 24 April 2012; Accepted 28 May 2012
Academic Editors: T. Levy and H. Taskinen
Copyright © 2012 A. D’Alfonso et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Introduction. Multiple factors influence the secondary sex ratio (SSR) including stress, which appears to affect mainly the males
born. Objective. We evaluate the effects of the earthquake in L’Aquila on the SSR. Materials and Methods. The SSR for the first six
months of 2010 was compared to that of the same period of 2008. The chi-square test and Fisher’s test were used for the statistical
analysis. Results. Nine months after the earthquake, an important reduction in the SSR was recorded: January 2010 versus January
2008 =0.62 versus 0.96. An overall fall in the SSR was also recorded when the first 3 months of 2010 were compared to the first
three months of 2008: 0,82 versus 1,11. When the first three months of 2010 were compared with the second three months of 2010,
a statistically significant increase of the sex ratio at birth was noted (0,82 versus 1,27).
1.Introduction
In the human species the ratio between males and females at
birth,thesecondarysexratio(SSR),isnot50:50aswouldbe
expected given the equal number of X and Y spermatozoa,
but slightly biased towards the male sex. Worldwide, the
average value of the SSR is 1.07 in favour of the male sex
indicating that other factors influence this ratio [1].
2.Selection of the Sex of the UnbornChild
Scientific literature has shown that the sex of an unborn
child can be influenced by a number of factors (hormonal
factors, parents’ age, pollution, nutritional and energetic
factors,stress)that,inthepreconceptionphase,canaffectthe
penetration of either the X or the Y spermatozoon and, in
the postconception phase, determine the negative selection
of the conceived male or female child.
In particular, both physical and psychological stress
influences fertility exercising a negative effect in the very
early stages of pregnancy resulting in miscarriage, notably
of male fetuses [2]. Stress may also influence the ratio of
males to females at conception, the Primary Sex Ratio (PSR),
as a result of its effect on preconception factors such as
hormonal state, sexual activity, and seminal liquid quality.
Natural catastrophes also represent a source of intense acute
stress: M. Fukuda et al. noted a fall in the number of male
infants born nine months after the earthquake that hit the
city of Kobe in 1995 [3]; this fall was associated with a
reduction in the motility of spermatozoa [4]. Similarly, a
decline in the sex ratio was reported in a study carried out
after the earthquake in the city of Bam, in Iran in 2003 [5].
Further stressful events include terrorism and war: a decline
in the SSR, as a result of a fall in the conception of males,
and an increase in the number of male fetal deaths following
the terrorist attack on the twin towers on 11th September
2001 was observed [6]. The war in Slovenia in 1991, which
only lasted 10 days, resulted in a temporary fall in the level
of sex hormones and sexual activity, as well as the quality
and mobility of spermatozoa; this was reflected in the fall
in the sex ratio recorded for Lubiana, the capital and target
of consistent bombing [7]. The war in Iran and Iraq (1980–
1988) also resulted in a fall in the number of males born but

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2The Scientific World Journal
in this case other factors may have influenced the sex ratio
such as chemical warfare [8].
Allthesefindingssupportagreatersusceptibilityofmales
to stressful events during pregnancy.
3.The GreaterVulnerabilityof Males during
Pregnancyand atBirth
The primary sex ratio is not 100/100 but biased towards
males. However, during pregnancy, both in humans and
other species, there is a greater loss of male embryos and
fetuses. At the end of the second month of pregnancy the
ratio of male to females is 151/100; this falls to 132/100 by
the end of the third month [9] and continues to fall until
birth when the average ratio is 107/100 [1, 10]. It would
therefore appear that a higher number of male embryos are
conceivedtocompensateforthegreatermortalityofthemale
sex as a result of their greater susceptibility to adverse and
stressfulevents.Infactspontaneous miscarriages,eveninthe
absence of chromosomal abnormalities, tend to be of male
embryos or fetuses [11, 12]; moreover an intensive neonatal
care is more frequently required for male infants according
to lower Apgar scores 1 to 5 minutes [13], and perinatal
mortalityisgreaterinmalesthaninfemalesbothinendterm
pregnancies and in preterm pregnancies [13–15]. Similarly it
would appear that the SSR at birth is still biased towards the
male sex to compensate for higher mortality during infancy,
childhood, and adult life which only equals out towards the
fourth decade of life. The mortality at one year of life is 5,4%
in males versus 4,1% in females [12].
4.The EarthquakeinL’Aquila
On6thofApril2009,at3:32am,anearthquakeofmagnitude
5.9 on the Richter Scale hit the region of L’Aquila; 308 people
died and 1600 were injured of whom 200 seriously. Patients
were taken to hospitals in the surrounding areas as the city’s
mainhospitalhadtobeevacuated.Theearthquakedestroyed
approximately 48% of residential property, 21.2% of public
property, and 53.7% of the city’s cultural patrimony. The
entire population was evacuated, and a significant propor-
tionofpeoplelosttheirjobs.Thegovernmentdeclaredastate
of emergency, and 67,459 people required assistance and
accommodation in the following months. Two hundred and
fifty aftershocks a day were recorded for the entire month of
April; the aftershocks fell to 40–60 in May and continued
in the following months [16]. An earthquake, like other
catastrophes, is a source of acute stress, and the aim of this
study was to evaluate its impact on the SSR.
5.MaterialsandMethods
On the basis of the fact that the children conceived after
6th April 2009 would be born in January 2010, we studied
and compared births from the 1st of January to June 30,
2010 (800 born) and for comparison purposes from the 1st
of January to June, 30, 2008 (1026 born), using the records
from the Clinical Obstetrics and Gynaecology Department
0
December January February MarchApril May June
1.21
1.24
1.02
0.84
1.02
0.96
0.96
0.62
1.03
0.82
1.2
1.1
1.53
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
1.8
1.17
2008
2010
Sex ratio
Figure 1: Sex ratio trends using the chi-squared test P = 0.22.
of the San Salvatore Hospital, L’Aquila. The chi-square test
and Fisher’s test were used for the statistical analysis.
6.Results
Nine months after the earthquake an important reduction
in the secondary sex ratio at birth was recorded, although
the overall fall was not statistically significant: the SSR for
January 2010 was 0,62, whilst a value of 0,96 was recorded
for the same month in 2008 (P = 0.23). The percentage of
males and females born in January 2010 was, respectively,
38,30% and 61,70%, whilst for January 2008 these figures
were 48,91% and 51,09%, respectively. A fall in the sex
ratio (0,82 versus 1,11) (P = 0.13) was also observed when
births over three months were compared: the first trimester
of 2010 (January, February and March) compared to the
same period of 2008. Statistically significant differences in
the sex ratio were recorded when the first trimester of 2010
was compared to the second: 0,82 versus 1,27 (P = 0.031).
Lastly, variations in the SSR over the two years taken into
consideration were compared using the chi-squared test for
trend; however no statistically significant findings emerged
(P = 0.22) (Figure 1).
7.Discussion
This study highlights a fall in the percentage of males born
nine months after the earthquake in L’Aquila: in January
2010 the SSR was approximately 0.62, much lower than the
global average value of 1.07. These findings echo those of
M. Fukuda et al. concerning the earthquake in Kobe [3] and
confirm clinical evidence pointing to a greater vulnerability
of the male sex at conception and during embryo-fetal
development, as well as following acute stress. We also found
that the sex ratio returned to its expected values six months
aftertheearthquake.Infactaftertheinitialfallinmalebirths,
there was an inversion of the trend and the value of the SSR
which, from its lowest value of 0.62 in January, rose steadily
to reach a peak of 1.53 in June. This statistically significant
variation underlines how catastrophic events can determine
changes in the SSR in favour of the female sex especially in
the immediate term. In fact the adverse effects of acute stress

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are mostly felt in the first months of pregnancy which are
also the most vulnerable period in biological terms and the
trimester in which the highest number of miscarriages occur.
It has been suggested that, vice versa, as pregnancy proceeds,
the woman and her child are less susceptible to the effects of
stress [17].
References
[1] World Sex Ratio, http://www.chartsbin.com/.
[2] L. A. Zonta, P. Astolfi, and L. Ulizzi, “Early selection and sex
composition in Italy: a study at the regional level,” Human
Biology, vol. 68, no. 3, pp. 415–426, 1996.
[3] M. Fukuda, K. Fukuda, T. Shimizu, and H. Moøer, “Decline
in sex ratio at birth after Kobe earthquake,” Human Reproduc-
tion, vol. 13, no. 8, pp. 2321–2322, 1998.
[4] M. Fukuda, K. Fukuda, T. Shimizu, W. Yomura, and S.
Shimizu, “Kobe earthquake and reduced sperm motility,”
Human Reproduction, vol. 11, no. 6, pp. 1244–1246, 1996.
[5] M. Saadat, “Decline in sex ratio at birth after Bam (Kerman
Province, Southern Iran) earthquake,” Journal of Biosocial
Science, vol. 40, no. 6, pp. 935–937, 2008.
[6] R. Catalano, T. Bruckner, A. R. Marks, and B. Eskenazi,
“Exogenous shocks to the human sex ratio: the case of
September 11, 2001 in New York City,” Human Reproduction,
vol. 21, no. 12, pp. 3127–3131, 2006.
[7] B. Zorn, V.ˇSuˇ cur, J. Stare, and H. Meden-Vrtovec, “Decline
in sex ratio at birth after 10-day war in Slovenia,” Human
Reproduction, vol. 17, no. 12, pp. 3173–3177, 2002.
[8] W. H. James, B. Zorn, V. Sucur, J. Stare, and H. Meden-
Vrtovec, “Sex ratios of births conceived during wartime
(multiple letters),” Human Reproduction, vol. 18, no. 5, pp.
1133–1135, 2003.
[9] V. I. Kukharenko, “The primary sex ratio in man. (analysis of
1014 embryos),” Genetika, vol. 6, pp. 142–149, 1973.
[10] G. C. S. Smith, “Sex, birth weight, and the risk of stillbirth in
Scotland, 1980–1996,” American Journal of Epidemiology, vol.
151, no. 6, pp. 614–619, 2000.
[11] J. Byrne and D. Warburton, “Male excess among anatomically
normalfetusesinspontaneousabortions,”AmericanJournalof
Medical Genetics, vol. 26, no. 3, pp. 605–611, 1987.
[12] I. Ingemarsson, “Gender aspects of preterm birth,” An Inter-
national Journal of Obstetrics and Gynaecology, vol. 110,
supplement 20, pp. 34–38, 2003.
[13] D. K. Stevenson, J. Verter, A. A. Fanaroff et al., “Sex differences
in outcomes of very low birthweight infants: the newborn
male disadvantage,” Archives of Disease in Childhood: Fetal and
Neonatal Edition, vol. 83, no. 3, pp. F182–F185, 2000.
[14] R.L.Naeye,L.S.Burt,D.L.Wright,W.A.Blanc,andD.Tatter,
“Neonatal mortality, the male disadvantage,” Pediatrics, vol.
48, no. 6, pp. 902–906, 1971.
[15] L. J. Vatten and R. Skjærven, “Offspring sex and pregnancy
outcome by length of gestation,” Early Human Development,
vol. 76, no. 1, pp. 47–54, 2004.
[16] Facts and figures relatived to the earthquake in L’Aquila,
http://www.protezionecivile.it.
[17] L. M. Glynn, P. D. Wadhwa, C. Dunkel-Schetter, A. Chicz-
DeMet, and C. A. Sandman, “When stress happens matters:
effects of earthquake timing on stress responsivity in preg-
nancy,” American Journal of Obstetrics and Gynecology, vol.
184, no. 4, pp. 637–642, 2001.