International Journal of Gynecology and Obstetrics 125 (2014) 28–32

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CLINICAL ARTICLE

Exposure to life-threatening stressful situations and the risk of preterm birth and low birth weight Tamar Wainstock a,⁎, Eyal Y. Anteby b, Saralee Glasser c, Liat Lerner-Geva c,d, Ilana Shoham-Vardi a a

Department of Public Health, Faculty of Health Sciences, Ben Gurion University of the Negev, Beer-Sheva, Israel Department of Obstetrics and Gynecology, Barzilai Medical Center, Faculty of Health Sciences, Ben Gurion University of the Negev, Ashkelon, Israel Women and Children's Health Research Unit, Gertner Institute for Epidemiology and Health Policy Research, Tel Hashomer, Israel d School of Public Health, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel b c

a r t i c l e

i n f o

Article history: Received 4 June 2013 Received in revised form 24 September 2013 Accepted 31 December 2013 Keywords: Low birth weight Prenatal stress Preterm birth

a b s t r a c t Objective: To evaluate the association between exposure to life-threatening rocket attacks and the risks of preterm birth (PTB) and low birth weight (LBW). Methods: The present retrospective cohort study compared the outcomes of 1851 births by women exposed to rocket attacks and 2979 births by unexposed women. The timing, frequency, and intensity of exposure were calculated for each trimester and for the entire pregnancy period. Demographic and medical data were abstracted from the patients’ records. Results: The rates of PTB and LBW were higher among exposed than unexposed women (PTB: 9.1% versus 6.8%, P = 0.004; LBW: 7.6% versus 5.8%, P = 0.02). The rate of infants who were small for gestational age did not differ between the groups. After controlling for potential confounders, the risks for PTB and LBW remained significantly higher in the exposed group (PTB: adjusted odds ratio 1.3 [95% confidence interval, 1.1–1.7]; LBW: adjusted odds ratio 1.3 [95% confidence interval, 1.03–1.7]). There was no linear association between the intensity of exposure and the risk of PTB or LBW. Conclusion: Maternal exposure to intermittent but repeated life-threatening rocket attacks for a prolonged period might be associated with increased risks of PTB and LBW. © 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.

1. Introduction The incidence of preterm birth (PTB), defined as delivery before completion of 37 weeks of pregnancy and usually associated with low birth weight (LBW), has been rising in all high-income countries [1]. It is the leading cause of infant mortality in these countries and a prime contributor to infant and child morbidity, resulting in a major burden on healthcare systems [2]. Although genetic, behavioral, and social factors are known to increase the risk for PTB [3], its etiology remains unclear. The relationship between prenatal maternal stress and PTB has been extensively researched [4–6], but the evidence is inconclusive. Further, stress has been shown to adversely affect pregnancy through unhealthy behaviors, such as smoking and inadequate prenatal care [7]. However, not all studies have confirmed that stress has a negative impact on pregnancy outcomes [8,9], and some have even found the opposite affect [6,10]. In addition, the data are inconsistent with regard to the period of pregnancy when stress exposure is most likely to affect pregnancy outcome. The unfortunate situation in southern Israel presents an opportunity to study this association. The southern Israeli town of Sderot (population ⁎ Corresponding author at: Department of Epidemiology, Faculty of Health Sciences, Ben Gurion University of the Negev, Beer-Sheva 84 105, Israel. Tel.: +972 52 31 14880; fax: +972 8 64 7638. E-mail address: [email protected] (T. Wainstock).

of approximately 20 000) has been a constant target of rocket-firing from the Gaza Strip (4 km away) since 2001. These rocket attacks are preceded by a warning alarm, informing residents to seek shelter. The alarms are loud, sudden, and stress-inducing because they are sounded only a few seconds before rockets hit the town. Between April 2001 and December 2008, over 1000 alarms were sounded around the town [11]. Numerous rockets fell and exploded, causing damage to property and human lives [11]. The aim of the present study was to evaluate the association between exposure to stress during pregnancy (as measured by the number of rocket-attack alarms) and the risks of PTB and LBW. 2. Materials and methods The present retrospective cohort study was carried out at Barzilai Medical Center, the single regional hospital in the area surrounding the Gaza strip, located in the city of Ashkelon. Barzilai is the closest medical center to Sderot (20 km north), and approximately 75% of Sderot’s parturients deliver there. The remaining deliveries are carried out in other medical centers, which provide similar services including operating rooms and neonatal intensive care units. Women residing in Sderot who delivered between January 1, 2002 (that is, women who conceived after April 15, 2001, when rocket attacks on the town began, and who were therefore exposed throughout pregnancy), and December 27, 2008 (the date a military conflict began and a wide area of southern

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T. Wainstock et al. / International Journal of Gynecology and Obstetrics 125 (2014) 28–32

Israel became intensively exposed to rocket attacks), comprised the “exposed” group. Women residing in the town of Kiryat Gat who delivered during the same period at Barzilai Medical Center comprised the “unexposed” group. Kiryat Gat, which—at the time of the study—was outside the range of rocket attacks, was chosen for comparison because it had a similar socioeconomic profile to Sderot [12], and is located the same distance (20 km east) from Barzilai Medical Center. To further test the hypothesis that exposure to rocket attacks may be associated with adverse birth outcomes, we compared birth outcomes in the 2 towns between January 1, 2000, and April 14, 2001, when neither town was exposed to rocket attacks, to establish a historical reference. The study was approved by the Institutional Review Board of Barzilai Medical Center. Informed consent was not required. In Israel, routine prenatal care is covered by universal national health insurance and almost all Jewish women in Israel seek prenatal care. The standard of prenatal care includes an early pregnancy ultrasound scan for confirmation of pregnancy and pregnancy dating, an ultrasound scan of fetal systems in the second trimester, and a glucose tolerance test. Hospital admission records of all women from Sderot and Kiryat Gat who delivered at Barzilai Medical Center between January 1, 2000, and December 27, 2008, were identified during the year 2009. Medical and demographic information of all parturients with a singleton pregnancy, including parity, maternal age, country of birth, and pregnancy complications and outcomes, was collected. Identifying characteristics were coded and all data were analyzed anonymously. The pregnancy duration was determined by early ultrasound or the date of the last menstrual cycle. Preterm birth was defined as delivery before 37 completed weeks. Low birth weight was defined as a birth weight of less than 2500 g, and small for gestational age (SGA) as a birth weight below the 5th percentile for the pregnancy duration at birth, according to the WHO growth tables [13]. Information about the dates when rocket-attack warning alarms were sounded in Sderot during the study period was obtained from local authorities. For each pregnancy, the mean number of alarms per week from conception until delivery and during each trimester was calculated. The intensity of exposure was classified by quintiles and was determined separately for each trimester and for the total pregnancy period. The data were coded and analyzed using SPSS version 17.0 (IBM, Armonk, NY, USA). WinPepi (Brixton Health, London, UK) was used for the power calculation. Univariable comparisons were made using the t, Mann–Whitney U, and χ2 tests as appropriate. The incidences of PTB and LBW in the exposed and unexposed groups were compared using odds ratios (OR) with 2-sided 95% confidence intervals (CI). P b 0.05 was considered statistically significant. Multivariable logistic regression models were created using generalized estimating equations, in which pregnancies occurring in the same woman were entered as a cluster. The models were evaluated using receiver operating characteristic analysis and the final models were chosen by the highest concordance, or c, statistic score. The models were used to evaluate the association of stress exposure with PTB or LBW, with adjustment for all risk factors that were hypothesized to be related to these outcomes or found to be potential confounders in the study population. Exposure variables used in the univariable and multivariable analyses included town of residence (dichotomous variable) and intensity of exposure during each trimester (continuous variable). 3. Results The study included 4830 births (2979 in the unexposed group and 1851 in the exposed group) by 3676 women (2275 unexposed and 1401 exposed). The number of weekly alarms in the exposed group ranged from 0 to 71, with a mean of 2.16 ± 2.71 and a median of 0 during all weeks of pregnancy. There were 2128 women who delivered more than once during the study period, none of whom had moved from one town to the other

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changing their exposure status. Most women in the study population were 21–35 years old, married, and born in Israel, had a high school diploma, and had conceived spontaneously (Table 1). Compared with the exposed group, a larger proportion of women in the unexposed group was older than 35 years, was born in Israel, and had less than 12 years of education. The rate of women in the exposed group with more than 12 years of education remained steady throughout the period of exposure: 32.2% (76/236 women) in 2002, 33.6% (90/268 women) in 2004, 29.9% (61/204 women) in 2006, and 34.3% (86/251 women) in 2008. The exposed and unexposed groups were similar in terms of other characteristics, pregnancy complications, and cesarean delivery rates (Table 1). In the total study population, the mean pregnancy duration was 275.6 ± 13.2 days and the mean birth weight was 3227 ± 503 grams. The rate of LBW was 6.5%, that of PTB was 7.7%, and that of SGA was 3.1% (Table 2). The pregnancy duration was shorter (mean 0.9 days) among exposed than among unexposed women (P = 0.02). There were no significant differences between the groups’ mean birth weights or SGA rates. The rates of PTB and LBW were higher among exposed women than among unexposed women (PTB: 9.1% versus 6.8%, P = 0.004; LBW: 7.6% versus 5.8%, P = 0.018) (Table 2). Among women with a PTB (according to medical records), the primary reason for hospital admission—induced labor versus spontaneous labor (preterm premature rupture of the membranes or uterine contractions)—did not differ significantly between the groups. In the multivariable analysis controlling for maternal age, origin, parity, gestational diabetes mellitus, and pregnancy-induced hypertension, stress exposure remained a risk factor for both PTB and LBW (Table 3). Maternal age and parity were both entered into the multivariable model because the correlation between these 2 parameters was not high (Spearman r = 0.414, P b 0.001). The level of education and the rate of compliance with the recommended standard of prenatal care were removed from the final model because they were no longer statistically significant. A separate multivariable model was created for primiparous women only, to control for a history of PTB (model not presented). The rate of PTB was 10.9% (52/478) among exposed primiparas and 7.5% (57/ 760) among unexposed primiparas. After controlling for maternal age and pregnancy-induced hypertension, the risk for PTB was higher among exposed than unexposed women (adjusted OR 1.51 [95% CI, 1.01–2.26]; P = 0.04). Another multivariable model was created for women with spontaneous PTB following preterm premature rupture of the membranes or contractions. Overall, 94/1324 (7.1%) women in the exposed group and 123/2238 (5.5%) women in the unexposed group had a spontaneous PTB. After controlling for maternal age and pregnancy-induced hypertension, the association between stress exposure and PTB was not significant (adjusted OR 1.3 [95% CI, 0.9–1.7]; P = 0.1). The intensity of exposure (during the entire pregnancy and during each trimester) was not linearly associated with the risk of PTB or LBW. During the period preceding the onset of rocket attacks (before April 15, 2001), the PTB rates were similar between the 2 towns (Table 4). After the onset of the attacks, the PTB rate increased in Sderot (from 7.2% to 9.1%), whereas it decreased in Kiryat Gat (from 7.3% to 6.8%). A similar pattern was observed for the rate of newborns with LBW (increase from 5.8% to 7.6% in Sderot and decrease from 7.5% to 5.8%). In multivariable generalized estimating equation models controlling for possible confounders, the differences in the rates of LBW and PTB between the 2 time periods were not significant in either group (Table 4). 4. Discussion The objective of the present population-based retrospective cohort study was to test the hypothesis that exposure to life-threatening stress

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T. Wainstock et al. / International Journal of Gynecology and Obstetrics 125 (2014) 28–32

Table 1 Demographic and obstetric characteristics of the study population by stress exposure status.a Total (n = 4830) Maternal age at delivery, y Age group, y ≤20 21–35 N35 Marital statusb Married Single Divorced Widowed Country of birth Israel Other Years of educationb b12 12 N12 Mode of conceptionb Assisted reproductive technology Spontaneous Parityb 1 2–3 ≥4 Gravidityb 1 2–3 ≥4 Background health problemsc Poor obstetric historyd Gestational diabetes mellitus Pregnancy-induced hypertension Cesarean delivery No compliance with the recommended standard regimen of prenatal of care in Israele a b c d e

Exposed (n = 1851)

Unexposed (n = 2979)

28.69 ± 5.6

29.49 ± 5.7

203 (4.2) 3894 (80.6) 733 (15.2)

90 (4.9) 1517 (82.0) 244 (13.2)

113 (3.8) 2377 (79.8) 489 (16.4)

4389 (90.9) 66 (1.4) 366 (7.6) 8 (0.2)

1682 (90.9) 25 (1.4) 140 (7.6) 4 (0.2)

2707 (90.9) 41 (1.4) 226 (7.6) 4 (0.1)

3054 (63.2) 1776 (36.8)

1135 (61.3) 716 (38.7)

1919 (64.4) 1060 (35.6)

644 (14.5) 2502 (56.2) 1307 (29.4)

235 (13.6) 924 (53.5) 567 (32.9)

409 (15.0) 1578 (57.9) 740 (27.1)

127 (2.6) 4703 (97.4)

55 (3.0) 1796 (97.0)

72 (2.4) 2907 (97.6)

1469 (30.5) 2356 (48.9) 997 (20.7)

585 (31.7) 904 (48.9) 359 (19.4)

884 (29.7) 1452 (48.8) 638 (21.5)

1235 (25.6) 2107 (43.7) 1486 (30.8) 271 (5.6) 62 (1.4) 343 (7.1) 296 (6.1) 824 (17.1) 20 (b0.01)

477 (25.8) 802 (43.4) 571 (30.9) 104 (5.6) 19 (1.4) 144 (7.8) 113 (6.1) 317 (17.1) 3 (0.2)

758 (25.5) 1305 (43.8) 915 (30.7) 167 (5.6) 32 (1.4) 199 (6.7) 183 (6.1) 507 (17.0) 17 (0.6)

P value

0.003

0.9

0.03

b0.001

0.2

0.2

0.9

N0.99 0.9 0.1 N0.99 0.9 0.03

Values are given as mean ± SD or number (percentage). Data were missing on: marital status, years of education, n = 377; n = 1; parity, n = 2; gravidity, n = 8. Asthma, skin, connective tissue, heart, psychiatric, or neurologic conditions. Defined as a history of intrauterine fetal death; analysis includes women with parity ≥2 only. Defined as women who did not complete the glucose tolerance test and did not have any ultrasound scan of fetal systems.

adversely affects pregnancy outcomes. Pregnancy outcomes of all live births in a population exposed to constant rocket attacks were compared with those of an unexposed population with similar characteristics. The

findings demonstrate a higher risk for PTB and LBW among women living in the “exposed” town compared with those in the “unexposed” town, and no effect on SGA rates.

Table 2 Pregnancy outcomes by stress exposure status.a Pregnancy outcome Preterm birth Pregnancy duration, wk 34–36 32–34 b32 Reason for hospital admission (preterm birth only) Spontaneous laborc Induced labor Low birth weight Birth weight, g N2500 1500–2500 b1500 SGA

Total population (n = 4830)

Exposed (n = 1851)

Unexposed (n = 2979)

371 (7.7)

168 (9.1)

203 (6.8)

303 (6.3) 27 (0.6) 41 (0.8)

143 (7.7) 12 (0.6) 13 (0.7)

160 (5.4) 15 (0.5) 28 (0.9)

217 (58.5) 154 (41.5) 314 (6.5)

94 (56.0) 74 (44.0) 140 (7.6)

123 (60.6) 80 (39.4) 174 (5.8)

4516 (93.5) 285 (90.8)e 29 (9.2)e 150 (3.1)

1711 (92.4) 131 (93.6) 9 (6.4) 61 (3.3)

2805 (94.2) 154 (88.5) 20 (11.5) 89 (3.0)

Abbreviations: CI, confidence interval; OR, odds ratio; SGA, small for gestational age. a Values are given as number (percentage) unless indicated otherwise. b Reference: term pregnancy. c Hospital admission because of contractions or preterm premature rupture of the membranes. All other deliveries were classified as induced. d Reference: birth weight N2500 g. e Percentage among low birth weight. f Reference: appropriate for gestational age.

OR (95% CI)

P value

1.4 (1.1–1.7)b

0.004 0.017

1.2 (0.80–1.83)

0.400

1.3 (1.01–1.6)d

0.018 0.027

1.1 (0.79–1.54)f

0.500

T. Wainstock et al. / International Journal of Gynecology and Obstetrics 125 (2014) 28–32 Table 3 Adjusted odds ratios (95% confidence intervals) for the risks of preterm birth and low birth weight (multivariable logistic regression model using generalized estimating equations). Variables Exposure (residence) No (Kiryat Gat) Yes (Sderot) Maternal age at delivery b21 years 21–35 years N35 years Country of birth Israel Other Parity 1 2–3 ≥4 Marital status Married Unmarried GD-M PIH

Preterm birtha

Low birth weightb

Ref. 1.30 (1.05–1.63)

Ref. 1.29 (1.02–1.64)

1.21 (0.76–1.94) Ref. 1.01 (0.71–1.4)

1.49 (0.93–2.41) Ref. 1.05 (0.70–1.57)

Ref. 0.80 (0.63–1.00)

Ref. 0.79 (0.62–1.02)

Ref. 0.78 (0.61–1.00) 0.79 (0.55–1.15)

Ref. 0.56 (0.43–0.72) 0.63 (0.42–0.94)

Ref. 1.22 (0.85–1.74) 1.62 (1.14–2.31) 2.37 (1.69–3.32)

Ref. 1.27 (0.87–1.86) 0.87 (0.54–1.41) 2.04 (1.41–2.95)

Abbreviations: GDM, gestational diabetes mellitus; PIH, pregnancy-induced hypertension. a c statistic, 60.8; P b 0.001. b c statistic, 62.3; P b 0.001.

Although alternative explanations are possible for the difference in PTB and LBW rates between the 2 groups, comparisons with the respective rates during 2000–2001 (before the onset of rocket attacks) indicate that there were no significant differences between the groups during the earlier period, whereas the rates were significantly different during the period when there were rocket attacks in one of the towns. The PTB and LBW rates rose with the onset of rocket attacks among exposed women, whereas they decreased during the same period among unexposed women. These findings indicate that exposure to life-threatening stress increases the risks of PTB and LBW. Stress may be associated with PTB and LBW by means of several possible mechanisms, the main one involving the corticotropin-releasing hormone axis [14–16]. Specifically, chronic stress may be associated with stimulation and chronic activation of the central nervous system, lowering its activation threshold and causing hypersensitivity to stressful stimuli. This may lead to an activation of parturition and PTB [14]. Stress is also associated with a poor immune status and may increase the risk of PTB through this mechanism as well [17]. Because there was no difference in the SGA rates between the groups, LBW can be assumed to be mainly a result of a shorter pregnancy duration rather than of intrauterine growth retardation, a conclusion that is supported by previous observations that chronic stress exposure is associated with a shorter pregnancy duration [4,18]. Because the proportions of women with spontaneous versus induced PTB were similar in the 2 groups, the increased rate of PTB among the exposed women is unlikely to reflect a greater tendency to induce labor in Sderot versus

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Kiryat Gat residents. This interpretation is further supported by the multivariable model, where adjustments were made for gestational diabetes mellitus and pregnancy-induced hypertension—among the main reasons for labor induction [19]. The finding that the risk of spontaneous PTB among exposed women was not higher than among unexposed women may be attributable to a lack of power (1 – β = 0.46) to test this difference. In the present study, stress exposure and exposure intensity were quantified for each trimester of pregnancy. In contrast to previous studies [5,16,20,21], which found different PTB risks depending on the duration of pregnancy, the current study did not reveal an association between the effect of stress exposure and a particular period of pregnancy. Class et al. [20] studied the effect of death of a first-degree relative and found an increased PTB risk among “exposed” mothers during the fifth or sixth month of pregnancy only. Other studies found PTB to be associated with stress exposure during early [21] or late pregnancy [5,16]. Most studies that identified a critical period of exposure [5,16,20,21] measured one-time events only. By contrast, most women in the current cohort were exposed to stress for an extended period of time before conception and throughout pregnancy. They therefore experienced a prolonged period of intermittent but repeated life-threatening events, rather than acute stress. It is possible that exposure to acute stress, such as stress induced by the death of a first-degree relative, a terror attack, or a natural disaster, has a different effect on the risk of PTB during the preconception and pregnancy periods than does chronic stress exposure as investigated in the present study. Elevated risks of PTB and LBW have also been reported in populations that were chronically exposed to other types of stress, such as racial discrimination or low socioeconomic status [4,22]. This negative effect on pregnancy outcomes may be related to the body’s “wear and tear” response (allostatic load) to stress, as suggested by Hobel et al. [23]. The proportion of women giving birth at the study hospital who came from Sderot was relatively stable and there was no change in the proportion of women with more than 12 years of education, indicating a stable socioeconomic profile. These observations preclude the “drift hypothesis”—outmigration of less vulnerable women from the exposed town during the exposure period (2001–2008)—as a possible explanation for the present findings. We acknowledge a number of limitations of the present study. Data were not available for history of previous PTB, maternal body mass index, and smoking habits. These characteristics are known to influence the risks of PTB and LBW [24]. A history of PTB, for instance, increases the risk for PTB in subsequent pregnancies. However, there is no reason to assume a difference in the rate of prior PTB between the study groups. Moreover, in the subgroup analysis of primiparous women, which was conducted to control for history of PTB, exposure remained a risk factor for PTB. Another limitation was that stress exposure was not directly ascertained and was not subjectively measured. However, in a pilot study [25] that was conducted on a sample of the present study population, women in both towns were interviewed, residency was verified,

Table 4 Comparison of preterm birth and low birth weight rates before and after the onset of rocket attacks (n = 5982).a,b Preterm birth

Before (n = 1152) After (n = 4830) aOR (95% CI); P value for before vs after

Low birth weight

Exposed

Unexposed

aOR (95% CI); P value for exposed vs unexposed

Exposed

Unexposed

aOR (95% CI); P value for exposed vs unexposed

31 (7.2) 168 (9.1) 1.03 (0.81–1.32); 0.8

53 (7.3) 203 (6.8) 1.12 (0.81–1.53); 0.6

1.03 (0.82–1.23); 0.8 1.30 (1.05–1.63); 0.01 NA

25 (5.8) 140 (7.6) 1.25 (0.96–1.63)

54 (7.5) 174 (5.8) 1.34 (0.97–1.87)

1.16 (0.91–1.49); 0.2 1.29 (1.02–1.64); 0.03 NA

Abbreviations: aOR, adjusted odds ratio; CI, confidence interval; NA, not applicable. a Values are given as number (percentage) unless indicated otherwise. b All models were adjusted for maternal age, gravidity, marital status, country of birth (Israel versus other), gestational diabetes mellitus, and pregnancy-induced hypertension.

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and information about health characteristics was obtained. No differences in the body mass index and the rate of smoking were observed between the exposed and unexposed groups. The results of the present study indicate that populations exposed to chronic stress may be at risk for PTB and LBW. The clinical relevance of these findings is that stress exposure can potentially be prevented or reduced. Intervention programs aimed at reducing stress, with the possibility of lowering the risk for unfavorable pregnancy outcomes, should be considered.

Acknowledgments The present study was supported in part by grant 3–00 000–6643/ 2011 from the Chief Scientist Office of the Ministry of Health, Israel. Conflict of interest The authors have no conflicts of interest.

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Exposure to life-threatening stressful situations and the risk of preterm birth and low birth weight.

To evaluate the association between exposure to life-threatening rocket attacks and the risks of preterm birth (PTB) and low birth weight (LBW)...
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