Soskolne et al. Disaster and Mil Med (2016) 2:1
DOI 10.1186/s40696-016-0011-x
Disaster and Military Medicine
Open Access
RESEARCH ARTICLE
Glycemic control of diabetes patients
under continuous rocket attacks
Varda Soskolne1*, Rachel Dekel1 and Shlomo Vinker2
Abstract
Background: Evidence regarding the detrimental effects of exposure to stress on glycemic control among diabetes
patients has mainly focused on personal life events or acute trauma. However, the effects of continuous exposure to
extreme stress on type 2 diabetes patients have rarely been studied. The aim of the current study was to examine the
association of continuous exposure to rocket attacks with glycemic control and with risk factors for diabetes complications among civilian type 2 diabetes patients. We focus on patients residing in the Western Negev in the south of
Israel that has been subjected to rocket attacks fired from Gaza since the end of 2001.
Methods: A two-arm retrospective cohort study of type 2 diabetes patients, aged 35–70 years, residing in a region
with chronic exposure to rocket attacks (N = 1697) and in a non-exposed comparison region in Israel (N = 3000).
Data were retrieved from the Health Maintenance Organization (HMO)’s database for four time periods representing
exposure: chronic—2008; elevated—2009 (post’Cast Lead’ operation); return to chronic—2010, 2011. Data included
socio-demographic variables, HbA1c, BMI, LDL cholesterol, blood pressure. General Linear Models (GLM) were used for
analysis.
Results: For HbA1c, the model yielded a significant main effect for time, a borderline significance main effect for
region, and a significant time by region interaction: no differences in HbA1c levels between the regions in 2008 and
2009, followed by significant differences between the regions in 2010 and 2011 when HbA1c continued to increase in
the exposed region but decreased in the comparison region. Regarding risk factors, a significant main effect for time
for LDL cholesterol only, and significant main effects for region were found in all factors: BMI and LDL cholesterol were
higher in the exposed than in the comparison region, but blood pressure values were lower.
Conclusions: Continuous exposure to rocket attacks is associated with glycemic control and risk factors in a complex
pattern. These preliminary findings require further studies of diverse types of civilian exposure to continuous extreme
stress.
Keywords: Type 2 diabetes mellitus, Trauma, Rocket attacks, Glycemic control, Risk factors for complications, Israel
Background
A growing body of research has indicated that exposure
to stressors, such as life events or chronic difficulties,
has detrimental effects on medical state of people living
with a chronic disease, among them diabetes patients
[1]. Evidence on the impact of severe events, acute or
long-term traumatic experiences, on glycemic control is
more limited and inconsistent. Several studies showed
*Correspondence: varda.soskolne@biu.ac.il
1
The Louis and Gabi Weisfeld School of Social Work, Bar Ilan University,
52900 Ramat Gan, Israel
Full list of author information is available at the end of the article
that surviving an acute event, such as floods [2] an earthquake [3, 4] or war [5] led to a significant increase in glycated haemoglobin (HbA1c) levels, followed by a gradual
decline to pre-event levels, while another study found
non-significant changes [6]. Others indicated that higher
levels of exposure to the traumatic event were associated
with elevated HbA1c levels [7]. These studies suffered
from methodological problems such as small sample size
or recruitment of a non-representative sample of patients
from a single medical center. Moreover, these studies
examined a single event and not continuous exposure
to traumatic experiences. In an attempt to expand the
© 2016 Soskolne et al. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License
(http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium,
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and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/
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Soskolne et al. Disaster and Mil Med (2016) 2:1
scientific knowledge on the impact of severe long-term
exposure on medical state of type 2 diabetes patients
and to overcome methodological limitations of previous research, our study examined the traumatic experience of exposure to terror-related events. Such events
have increased in the past two decades affecting civilian
populations in many parts of the world. Yet, to the best
of our knowledge, their impact on clinical state of people
living with chronic illness has not been studied. The present study examined the association between continuous
exposure to rocket attacks and clinical indicators among
type 2 diabetes patients: glycemic control and major risk
factors for diabetes complications—obesity, lipid level
and hypertension. We focus on residents of the Western
Negev in Israel, a region that has been subjected to continuous rocket attacks fired from Gaza since the end of
2001.
Methods
Study design
In this two-arm cohort study, two geographic regions
in Israel were selected: (a) Chronic exposure—a town
(Sderot) and rural villages within a 20-kilometer radius
surrounding the Gaza Strip, which have been subjected
to continuous rocket attacks fired from Gaza since the
end of 2001, with accelerated frequency in 2007–2008
of 8–9 rockets a day, claiming lives, hundreds of physical casualties, and causing thousands of anxiety attacks
[8], (hereafter exposed region). (b) No exposure—towns
and villages of similar demographic background from
Israel Central region, not exposed to rocket attacks
(comparison region). We carefully selected towns of
the same rank in the socio-economic index as Sderot,
or only one rank lower or higher, south of but not from
Tel-Aviv metropolitan area, as well as villages of similar
size. Four time-periods representing different levels of
exposure to attacks in the exposed region were examined. Time 1: continuous, chronic exposure (2008); Time
2: elevated (2009)—continuous exposure combined with
acute exposure during “Cast Lead” operation, last days of
12/2008 through January 2009, when about 660 rockets
fell mainly in the exposed region, yet reaching further to
towns in the South not affected before, and accompanied
by wide media coverage [8]; Time 3 and Time 4: return
to continuous although decreased and sporadic exposure
(2010, 2011).
Data source and study variables
Data of type 2 diabetes patients, aged 30–70 years,
insured by Clalit Health Services (hereafter HMO), residing in the two regions were included. After approval of
the study protocol by the HMO’s Ethics Committee,
all patients in this age range from the exposed region
Page 2 of 6
(N = 1697) and a random sample of 3000 patients from
the comparison region were selected from the HMO
computerised database. Data on age, gender, socioeconomic status (SES), measured by a dichotomous
variable (yes vs. no exemption from co-payments, an
unspecific indicator of poverty level), and for each time
period, HbA1c values, and risk factors—LDL cholesterol,
BMI (kg/m2), systolic and diastolic blood pressure were
retrieved from the HMO database at the end of 2011. In
order to capture the possible reaction to the acute state in
early 2009, data for HbA1c were restricted only to those
from January–June 2009 (the values closest to January–
March 2009); while for the risk factors any annual test
result was taken for each year. In most cases, only one
value was recorded at each time period.
Description of the sample
Mean age was 59.5 (8.5), 53 % were men. Patients in the
exposed vs. the comparison region were significantly
younger [58.8 (9.4) and 59.9 (8.0), respectively, p < 0.01],
a smaller proportion were men (51 and 55 % respectively,
p < 0.05). Additionally, a small but significant difference
was found between the two regions in SES: a higher proportion of patients (33 %) in the exposed region than
those in the comparison region (27 %, p < 0.001) were
exempt from co-payments.
Statistical analysis
Descriptive statistics were assessed and bivariate differences between the two regions were tested using t test
for continuous variables and χ2 tests for categorical variables. A series of General Linear Models (GLM) was conducted to examine the effect of region (between group
differences) and time periods (within group differences)
on glycemic control and risk factors and included interaction terms for region with time, controlling for age and
sex. p value in all the models was set at p < 0.05 for statistical significance. Data of laboratory test results for some
of the indicators and recorded blood pressure values
were missing in the HMO database. This may be a source
of selection bias because patients who do not come for
regular follow-ups could differ from those who did; yet
we found no significant differences by age, gender, SES or
region in any of the measures.
Results
The GLM results are shown in Table 1. For glycemic control, the model yielded a significant main effect for time,
and of a borderline significance (p = 0.065) main effect
for region. Additionally, the model yielded a significant
time by region interaction: There were no differences in
HbA1c levels between the regions before (2008) or during the acute period (2009), and the levels increased in
Soskolne et al. Disaster and Mil Med (2016) 2:1
Table 1 General Linear Model (GLM) for medical status variables
Time 1 (2008)
Region
Exposed
Measure
Mean (SD)
Time 2 (2009)
Comparison Exposed
Time 3 (2010)
Comparison Exposed
Mean (SD)
Comparison
Mean (SD)
p valuea (Eta2)
Time 4 (2011)
Exposed
Comparison
Time
Region
Time ×region
<0.001 (0.005)
0.065 (0.002) <0.001 (0.007)
Mean (SD)
HbA1c (%)
7.14 (1.48)
7.12 (1.38)
7.41 (1.57)
7.45 (1.49)
7.52 (1.46)
7.33 (1.38)
7.68 (1.51)
7.34 (1.50)
HbA1c (mmol/mol)
54.5
54.3
75.7
57.8
58.7
56.6
60.3
56.7
nb
631
1160
BMI (kg/m2)
30.75 (5.44)
30.09 (5.90)
30.67 (5.58)
30.09 (5.66)
30.58 (5.62)
30.00 (5.64)
30.29 (5.45)
29.80 (5.56)
0.790 (0.000)
0.031 (0.003)
0.433 (0.000)
n
742
1279
2.53 (0.85)
2.48 (0.80)
2.45 (0.87)
2.38 (0.77)
2.36 (0.85)
2.28 (0.75)
<0.001 (0.002)
0.007 (0.002)
0.254 (0.000)
LDL Cholesterol (mmol/l) 2.67 (0.88)
1499
n
2.57 (0.79)
2667
Systolic BP (mmHg)
131.6 (16.37) 134.1 (17.14)
n
755
130.7 (15.63) 132.8 (15.50)
131.9 (17.23) 131.5 (15.92)
129.9 (14.57)
130.6 (14.92)
0.267 (0.001)
0.054 (0.002)
0.002 (0.002)
75.92 (8.67)
75.08 (9.42)
73.72 (9.26)
74.10 (8.34)
0.343 (0.001)
0.007 (0.004)
0.327 (0.001)
1312
Diastolic BP (mmHg)
76.34 (8.83)
77.42 (9.34)
n
755
1312
76.54 (8.23)
75.35 (8.68)
a
p values are based on F test, controlling for age and gender
b
n for HbA1c was restricted to those tested January–June 2009. n for other measures—any test during the year
Page 3 of 6
Soskolne et al. Disaster and Mil Med (2016) 2:1
both regions from 2008 to 2009. However, in the followup years 2010, HbA1c level continued to increase in the
exposed region but decreased in the comparison region.
Examining the source of the interaction revealed significant differences between the regions only in 2010
and 2011, and significant differences within each region
between the 2008 and all the other times (p < 0.05, after
Bonferroni correction). Yet, the effects of time, region
and the interaction are minimal (<1 %).
The GLM models of risk factors yielded a significant
main effect for time only for LDL cholesterol, which
improved over the years, and significant main effects for
region in all risk factors. Compared to patients in the
comparison region, patients in the exposed region had
higher BMI and LDL cholesterol levels but lower blood
pressure values. Additionally, the model for systolic blood
pressure yielded a significant time by region interaction:
the levels decreased in the comparison region over time
(significant differences between 2008, 2009 and 2011),
they fluctuated in the exposed region and were significantly different from those in the comparison region in
2008 and 2009 (p < 0.05, after Bonferroni correction).
Discussion
Our findings demonstrate that exposure to continuous
rocket attacks was related to a progressive poor glycemic
control, even when the frequency of attacks subsided. Yet
glycemic control of patients in the exposed region differs
from that of patients residing in a non-exposed region
only in the years following an acute stress. Less consistent are the differences in risk factors: while the patients
in the exposed region also have higher BMI and LDL
cholesterol levels than those shown for the comparison
region, their blood pressure levels were lower.
Previous evidence on the effects of stress on glycemic
control focused on exposure to acute, natural events [2,
4] or on war stress that affects the total population [6]
and relied on small samples [5]. The current study is the
first to examine exposure of a civilian population of diabetes patients to continuous threat of intermittent rocket
attacks. Its strengths include the incorporation of risk
factors in addition to HbA1c, a large sample size, of community dwelling patients, a comparison region, and a
longer follow-up.
Our analysis demonstrates a complicated pattern of the
consequences of continuous exposure and acute attack
periods. The interaction of time by region for HbA1c
showed that there were no significant differences between
the regions in 2008, despite the fact that the exposed area
was already subjected to rocket attacks since 2001. This
pattern could be explained, in part, by the habituation
hypothesis, suggesting that repeated exposure to a stressful event may serve to normalize perceived threats and
Page 4 of 6
make the circumstances of unusual events more understandable [9]. Thus, victims become toughened and more
resilient to subsequent experiences [10].
Second, while we expected an increase in 2009 in the
exposed area, following “Cast Lead” operation, the similar increase in the level of HbA1c in the comparison
region, indicates that this stressful time affected patients
in other regions via media exposure or personal contacts. Reactions to such indirect exposure are known
to be expressed in elevated levels of distress symptoms
[11], even reaching the same magnitude of the exposed
individuals [12]. Others support our findings that the
reactions to indirect exposure are also expressed in an
increase of medical problems, such as those found in the
US general population following the 9/11 attacks [13].
Once the acute period was over, HbA1c values decreased
among the comparison patients while they continued
to increase in 2010 and 2011 in patients in the exposed
region. One potential explanation may be that habituation may have its limits: the residents in the exposed
region were expecting that there would be a quiet period
following the military operation but the rocket attacks
continued (although more sporadically).
The increased risk for diabetes comorbidities was also
expressed in the significantly higher levels of BMI and
LDL cholesterol among patients in the exposed region,
suggesting that they may have had more difficulties in
adherence to healthy life style and/or impaired compliance to medications. Additionally, although systolic and
diastolic blood pressure values were lower in patients
in the exposed region, the decrease (in systolic BP) over
time was smaller than in patient in the comparison
region. In view of the absence of findings on changes
in these medical factors in previous studies, our findings are preliminary. Further examination is required in
order to understand the physiological mechanisms of the
effects of the risk factors and in conjunction with HbA1c,
as part of the neuroendocrine system role in response to
stress. One assumption is that responses to acute stressful events that are protective and adaptive in nature differ
from those to chronic stress which elicits neurochemical, neuroanatomical and cellular changes that may have
deleterious consequences upon higher brain functioning
[14].
Our findings suggest that the continuous chronic and
acute stress periods of exposure to rocket attacks has
complex pattern of consequences for glycemic control:
no difference between the regions after several years of
exposure (the already chronic state in 2008), but an activation of reaction—poorer glycemic control—after an
acute period. However, this pattern should be interpreted
in the context of the study limitations. First, no causality
can be assumed as we lack of data on glycemic control
Soskolne et al. Disaster and Mil Med (2016) 2:1
in the pre-exposure to rocket attacks period and the first
years of exposure. Second, although the analyses controlled for demographic differences, it may be that despite
our efforts in selecting similar towns and villages (not
from a metropolitan area) in the comparison region, differences in the delivery of medical care between central
and peripheral regions persisted. Due to our unmatched
design we cannot rule out the possibility that patients in
the comparison region differed on other important variables unknown to us, such as adherence to diabetes selfmanagement or depression. A third limitation relates
to the generalizability of our results. Continuous rocket
attacks are a unique type of extreme traumatic stress,
and reactions to other types of continuous traumatic
situations may be different. Fourth, our reliance on data
retrieved from the HMO database restricted our ability
to adjust for additional confounders (e.g., robust socioeconomic status measures, the number or intensity of prescribed medications, adherence to medications) and was
compounded by missing test results for some of the indicators that, although no selection bias was detected, was
subjected to other differences in ways we were unable to
measure. Therefore, our preliminary findings should be
further examined in studies with a matched case design
of patients by age, gender, SES and duration of diabetes,
and include a wider array of variables, and different patterns of exposure to chronic extreme stress. They will
benefit from inclusion of more representative samples
as well as other chronic patients in order to reach better
conclusions about long-term effects.
Conclusions
The current study, although being preliminary, provides
data that, to our best knowledge, have not been studied
before. These findings have significant implications for
clinical practice. Health care professionals need to be
aware of a potential association of continuous exposure
to trauma with health outcomes for diabetic patients
and probably for patients with other chronic diseases.
This chronic exposure and the prospects for acute peaks
of tension, may lead to allostatic load, and should be
monitored for its potential effects on glycemic control
and other implications of chronic diseases control and
management in the long run. In addition to individuallevel interventions, group stress management programs
are another effective tool in a “real-world” setting to
achieve clinically significant benefits for patients with
type 2 diabetes [15], calling for a multidisciplinary diabetes team approach. Health care providers should actually consider residence in a region exposed to continuous
terror-related threats as a risk marker requiring special
attention and resources.
Page 5 of 6
Abbreviations
HbA1c: glycated haemoglobin; BMI: Body Mass Index; LDL: low-density lipoprotein; GLM: General Linear Models; HMO: Health Maintenance Organization.
Authors’ contributions
VS and RD conceived of the study and all the authors participated in the
design of the study and planning of the data analysis. SV retrieved the data
from the HMO database. VS drafted the manuscript. All the authors read,
revised and approved the final manuscript. All authors read and approved the
final manuscript.
Authors’ information
The authors have a joint interest in studying impact of stress on physical wellbeing, yet from diverse research interests and clinical backgrounds.
VS—BSW, MPH, PhD is an Associate Professor of Social Work and Chairperson
of the Israel Forum for Social Policy Research, ESPANet-Israel. Her research
areas include psychosocial and behavioral factors in health, adjustment to
chronic illness, social inequalities in health, social work in health care.
RD—BSW, MSW, PhD is a Full Professor of Social Work and the Head of the
School of Social Work. Her research interests focus on studying the consequences of exposure to traumatic events on individuals and specifically on
families.
SV—MD, MHA is a Full Professor in Family Medicine, and Former Chair of the
Department of Family Medicine, at the Sackler School of Medicine, Tel Aviv
University, Tel Aviv. He is also Chairman of the Israeli Association of Family
Physicians since 2009. His research areas are: family medicine, military primary
care medicine, chronic diseases management and quality of care.
Author details
1
The Louis and Gabi Weisfeld School of Social Work, Bar Ilan University,
52900 Ramat Gan, Israel. 2 Department of Family Medicine, Sackler School
of Medicine, Tel Aviv University, Tel Aviv, Israel.
Acknowledgements
This research was supported by grant 300000-5984 from the Chief Scientist
Office, Israel Ministry of Health. We thank Dr. Gabi Liberman for statistical
consultation and analysis.
Competing interests
The authors declare that they have no competing interests.
Received: 8 January 2015 Accepted: 5 January 2016
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