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Europace (2015) 17, 131–136 CLINICAL RESEARCH

doi:10.1093/europace/euu149 Electrocardiology and risk stratification

Abnormal electrocardiographic QRS transition


zone and risk of mortality in individuals free
of cardiovascular disease
Natalie Bradford 1, Amit J. Shah 2, Andrew Usoro 3, Wesley K. Haisty Jr1,
and Elsayed Z. Soliman 1,4*
1
Department of Internal Medicine-Cardiology, Wake Forest School of Medicine, Winston-Salem, NC 27157, USA; 2Department of Epidemiology and Medicine, Emory University, Atlanta
Veterans Affairs Medical Center, Atlanta, GA 30322, USA; 3Wake Forest School of Medicine, Winston-Salem, NC 27157, USA; and 4Epidemiological Cardiology Research Center
(EPICARE), Department of Epidemiology and Prevention, Division of Public Health Sciences, Wake Forest School of Medicine, Medical Center Blvd, Winston-Salem, NC 27157, USA

Received 5 May 2014; accepted after revision 11 May 2014; online publish-ahead-of-print 17 June 2014

Aims We examined the prognostic significance of abnormal electrocardiographic QRS transition zone (clockwise and coun-
terclockwise horizontal rotations) in individuals free of cardiovascular disease (CVD).
.....................................................................................................................................................................................
Methods A total of 5541 adults (age 53 + 10.4 years, 54% women, 24% non-Hispanic black, 25% Hispanic) without CVD or any
and results major electrocardiogram (ECG) abnormalities from the US Third National Health and Nutrition Examination Survey
were included in this analysis. Clockwise and counterclockwise horizontal rotations were defined from standard 12-
lead ECG using Minnesota ECG Classification. Mortality and cause of death were assessed through 2006. At baseline,
282 participants had clockwise rotation and 3500 had counterclockwise rotation. During a median follow of 14.6
years, 1229 deaths occurred of which 415 were due to CVD. In multivariable-adjusted Cox proportional hazard analysis
and compared with normal rotation, clockwise rotation was significantly associated with increased risk of all-cause mor-
tality {hazard ratio (HR) [95% confidence interval (CI)]: 1.43 (1.15– 1.78); P ¼ 0.002} and CVD mortality [HR (95% CI):
1.61 (1.09, 2.37) P ¼ 0.016]. In contrast, counterclockwise rotation was associated with significantly lower risk of all-
cause mortality [HR (95% CI): 0.86 (0.76, 0.97); P ¼ 0.017] and non-significant association with CVD mortality [HR
(95% CI): 1.07 (0.86, 1.33); P ¼ 0.549]. These results were consistent in subgroup analysis stratified by age, sex, and race.
.....................................................................................................................................................................................
Conclusion In a diverse community-based population free of CVD and compared with normal rotation, clockwise rotation was asso-
ciated with increased risk of all-cause and CVD mortality while counterclockwise rotation was associated with lower risk
of all-cause mortality and non-significant association with CVD mortality. These findings call for attention to these often
neglected ECG markers, and probably call for revising the current definition of normal rotation.
-----------------------------------------------------------------------------------------------------------------------------------------------------------
Keywords Clockwise rotation † Counterclockwise rotation † Transition zone † Mortality † Electrocardiogram

contrast, counterclockwise rotation was associated with significantly


Clinical perspective lower risk of all-cause mortality and non-significant association with
Using data from the US Third National Health and Nutrition Exam- CVD mortality. These findings call for attention to these often
ination Survey (NHANES III), we examined the association neglected electrocardiogram (ECG) markers, and probably call for
between clockwise and counterclockwise rotations with cardiovas- revising the current definition of normal rotation.
cular and all-cause mortality among a diverse, nationally representa-
tive community-based population free of cardiovascular disease
(CVD). In multivariable-adjusted Cox proportional hazard analysis
Introduction
and compared with normal rotation, clockwise rotation was signifi- Current guidelines suggest the need to understand the utility of ECG
cantly associated with increased risk of all-cause mortality. In in screening intermediate risk populations.1 Although the usefulness

* Corresponding author. Tel: +1 336 716 8632; fax: +1 336 716 0834. E-mail address: esoliman@wakehealth.edu
Published on behalf of the European Society of Cardiology. All rights reserved. & The Author 2014. For permissions please email: journals.permissions@oup.com.
132 N. Bradford et al.

were obtained during home interviews and subsequent mobile examin-


What’s new? ation centre visits. Blood pressure data were the averaged reading from
three in-home measurements and three mobile centre measurements.
† Although electrocardiographic rotation has been recognized
Using the height and weight measured during the visit to mobile examin-
since the addition of precordial leads and use of 12 ECG
ation centre, the body mass index was calculated as the weight in kilo-
leads in clinical practice, its prognostic significance has not grams divided by the height in metres squared. Diabetes was defined as
been thoroughly examined in ethnically diverse populations. fasting plasma glucose ≥126 mg/dL, a non-fasting plasma glucose
† Using data from the US Third National Health and Nutrition ≥200 mg/dL, or concurrent use of anti-diabetics medications. Diagnosis
Examination Survey (NHANES III), we showed that clockwise of dyslipidaemia, history of cancer, and smoking were self-reported.
rotation is associated with increased risk of all-cause and CVD The documentation of ECG acquisition and analysis in NHANES III are
mortality. On the other hand, counterclockwise rotation, available at ‘ftp://ftp.cdc.gov/pub/Health_Statistics/NCHS/nhanes/nhanes3/
which is very common, is associated with lower risk of all- 2A/NH3ECG-acc.pdf’. Briefly, standard 12-lead ECGs were acquired using
cause mortality and non-significant association with CVD the Marquette MAC system (Marquette Medical Systems) by trained tech-
mortality. nicians in mobile examination visits. To standardize the chest electrodes
position, an electrode locator (Heartsquare) was used to position the V4
† These findings call for attention to these often neglected ECG
electrode at a 458 angle between the mid-sternal line and the left mid-
markers, and probably call for revising the current definition of
axillary line (location of V6). Electrocardiogram tracings were transmitted
normal rotation. electronically for reading at a central ECG core laboratory (EPICARE
ECG Center, Wake Forest School of Medicine, Winston-Salem, NC,
USA). Electrocardiogram abnormalities including transitional zone rotation
were identified from automated computerized analysis using Minnesota
of several ECG markers as predictors of poor outcomes have been ECG Classification.22 Normal transition zone was characterized by domin-
examined recently,2 – 21 there are still markers that yet to be ance of S-wave in V3 and dominance of R-wave in V4. Counterclockwise
explored. One of these markers is the electrocardiographic transi- rotation was defined as transition zone at V3 or rightward, while clockwise
tional zone, which identifies the direction of the QRS axis in the hori- rotation was defined as transition zone at V4 or leftward.22
zontal plane. Normal transition zone could be easily recognized from Mortality data were obtained through 31 December 2006. The cause
standard 12-lead ECG by observing V3 and V4 where a dominant of of death was determined based on death certificate records and the Inter-
national Classification of Disease (ICD) codes.
S-wave in lead V3 and a dominant of R-wave in lead V4 should be
Out of NHANES participants older than 40 years and younger than 75
present. Transition outside of the normal zone is referred to as
years who underwent 12-lead ECG recording (n ¼ 6931), this analysis
either clockwise or counterclockwise rotation.22 included 5541 participants after excluding 542 participants with CVD,
Although electrocardiographic rotation has been recognized since 844 participants with major ECG abnormality as defined by Minnesota
the addition of precordial leads and use of 12 ECG leads in clinical ECG Classification,22 and 4 participants with poor quality/incomplete
practice, its prognostic significance has not been thoroughly exam- data. The list of excluded major abnormalities included major ventricular
ined. In a Japanese sample, clockwise rotation was associated with conduction defect, definite/possible myocardial infarction, major isolated
increased risk of all-cause mortality.23 Nevertheless, there is no sup- ST/T abnormalities, left ventricular hypertrophy, major atrioventricular
porting literature for these findings in other populations. Further- conduction abnormalities, atrial fibrillation/flutter, major QT prolonga-
more, no standardized chest electrode positioning protocol was tion, pacemaker, and other major rhythm disorders.
applied in that Japanese study which can introduce errors in ascer-
tainment of QRS transitional rotation.
Statistical analysis
Using data from the US Third National Health and Nutrition Exam-
Baseline characteristics were tabulated and compared across study par-
ination Survey (NHANES III), we examined the association between
ticipants stratified by rotation status (normal, clockwise rotation, and
clockwise and counterclockwise rotations with cardiovascular and counterclockwise rotation). x2 Test was used for dichotomous variables,
all-cause mortality among a diverse, nationally representative and analysis of variance was used to test for any pair-wise difference
community-based population free of CVD. The high quality of among the three categories for continuous variables. Cox proportional
digital ECG data that were collected in NHANES III using standar- hazards analysis was used to calculate the unadjusted and multivariate-
dized protocol provides a unique opportunity to examine the prog- adjusted hazard ratios (HRs) and 95% confidence intervals (95% CIs)
nostic significance of different patterns of rotation using appropriate for all-cause and CVD mortality, separately associated with clockwise
methods. and counterclockwise rotation, separately (normal rotation was the ref-
erence group). Multivariate analysis was performed with incremental
models as follows: Model 1 adjusted for demographics (age, sex, and
race); Model 2 adjusted for Model 1 variables plus smoking status, systolic
Methods blood pressure, body mass index, use of blood pressure lowering drugs,
NHANES III is a national survey conducted from 1988 to 1994 by the Na- dyslipidaemia, and diabetes; and finally Model 3 adjusted for variables in
tional Center for Health and Statistics of the Centers for Disease Control Model 2 plus any other remaining ECG abnormalities by Minnesota
(CDC), which examined health and nutritional data from a sample of ci- ECG Classification, cancer, and pulmonary disease (bronchial asthma
vilian non-institutionalized US population. The primary purpose of this and chronic obstructive airway disease). Subgroup analysis by age (using
survey was to identify health and nutrition trends in US populations the median age, 55 years, as the cut point), sex, and race (Whites vs. non-
that can be utilized to influence polices and improve national health. Whites) was conducted using models similar to Model 3 in the main ana-
Baseline characteristics including demographics, past medical history, lysis. Interactions between strata in each subgroup with rotation for each
medication use, and history of traditional cardiovascular risk factors of the all-cause and CVD mortality events, separately, were examined.
Transition zone and mortality 133

Table 1 Baseline characteristics of the study population

Variable Normal (n 5 1759) Clockwise (n 5 282) Counterclockwise (N 5 3500) P-value


...............................................................................................................................................................................
Age, years 54.8 + 10.3 56.6 + 10.4 55.0 + 10.3 0.03
Black, non-Hispanic 404 (23%) 59 (21%) 875 (25%) 0.09
Hispanic 387 (22%) 51 (18%) 980 (28%) ,0.001
Female sex 897 (51%) 155 (55%) 1960 (56%) 0.002
Hypertension 545 (31%) 104 (37%) 1085 (31%) 0.13
Dyslipidaemia 404 (23%) 73 (26%) 840 (24%) 0.61
Diabetes mellitus 175 (10%) 39 (14%) 315 (9%) 0.03
Current smoker 510 (29%) 84 (30%) 805 (23%) ,0.001
Systolic blood pressure 129.8 (18.0) 130.1 (19.5) 128.6 (17.9) 0.06
Body mass index (kg/m2) 27.5 (5.8) 28.5 (6.6) 28.0 (5.4) 0.003
Minor ECG abnormalities 422 (24%) 81 (29%) 840 (24%) 0.13
Pulmonary disease 193 (11%) 50 (18%) 350 (10%) ,0.001
Cancer 158 (9%) 28 (10%) 280 (8%) 0.29

Values are expressed as mean (SD) or N (%).


P-value derived from x2 for categorical variables and analysis of variance (ANOVA) for continuous variables.

The statistical analysis was conducted using SAS 9.3 (SAS Institute Inc.). cause and CVD mortality, separately. As shown, clockwise rotation
Statistical significant was specified at P , 0.05. was significantly associated with increased risk of both all-cause mor-
The NHANES III protocol was approved by the institutional review tality and CVD mortality in all models. On the other hand, counter-
board of the CDC and all participants provided written informed clockwise rotation was associated with significantly lower risk of
consent.
all-cause mortality and no statistically significant association with
CVD mortality in all models (Table 2). This pattern of associations
was consistent across subgroups of the study participants stratified
Results by age, sex, and race (Table 3).
Of the 5541 participants included in this analysis, 1759 had normal ro-
tation, 282 had clockwise rotation, and 3500 had counterclockwise
rotation. The mean age was 55.0 + 10.4 years, with 54% women,
Discussion
24% non-Hispanic black, and 25% Hispanic. Table 1 shows the base- Although easily detectable, electrocardiographic rotation in the hori-
line characteristics of the study participants stratified by rotation zontal plane is an underutilized parameter which is often overlooked.
status. Participants with clockwise rotation were more likely to be This is probably because there are not much data on its mechanisms
older with a higher body mass index and a higher prevalence of dia- or prognostic significance. In this analysis from the NHANES III
betes, smoking, and pulmonary disease compared with participants survey, we showed that deviation from what is considered as
with normal rotation. On the other hand, participants with counter- normal rotation is common in individuals free of CVD. The preva-
clockwise rotation were more likely to be female and Hispanic com- lence rates of clockwise and counterclockwise rotations in our
pared with those with normal rotation (Table 1). study were 5.1 and 63.2%, respectively, while normal rotation was
During a median follow-up of 14.6 years, a total of 1229 deaths oc- present in only 31.7% according to the current standards of defin-
curred (incidence rate 16.1 per 1000 person-years) of which 415 ition.22,23 We also showed that clockwise rotation is associated
deaths (5.4 per 1000 person-years) were due to CVD death. The in- with increased risk of all-cause and CVD mortality, while counter-
cidence rates of all-cause and CVD mortality were higher in the clockwise rotation is associated with less risk of all-cause mortality
clockwise rotation group compared with the rates in the normal ro- and no significant association with CVD mortality. These findings
tation group (27.7 vs. 17.4 per 1000 person-years for all-cause mor- call for attention to these common yet neglected ECG markers.
tality and 9.2 vs. 5.1 per 1000 person-years for CVD mortality). On The facts that counterclockwise rotation in our study was more
the other hand, the incidence rate of all-cause mortality was lower common than what is typically considered as a normal rotation,
in the counterclockwise rotation group compared with the rate in and is prognostically more benign, mandate reconsidering what
the normal rotation group (14.6 vs. 17.4 per 1000 person-years), should really be labelled as ‘normal’ rotation.
but not difference in the incidence rates of CVD mortality (5.4 vs. Tahara et al.24 evaluated the association of anatomic rotation of the
5.3 per 1000 person-years, respectively). Figures 1 and 2 show the heart as demonstrated by cardiac computed tomography with hori-
Kaplan–Meier survival curves for all-cause mortality and CVD mortality, zontal rotation on ECG. Two-thirds of rotated transition zones were
respectively, in the study participants stratified by rotation status. related to anatomic rotations of the heart with a smaller measured
Table 2 shows the association between clockwise rotation and septal angle in the majority of clockwise rotated hearts and a larger
counterclockwise rotation (compared with normal rotation) with all- septal angle and thickened intraventricular septum in the majority
134 N. Bradford et al.

1.0
+ Censored

0.8

Survival probability
0.6 Normal rotation
Clockwise rotation
Counterclockwise
0.4

0.2

0.0
0 5 10 15
Follow-up in years

Figure 1 Kaplan– Meier survival curves for all-cause mortality stratified by rotation status. Number of participants at risk (surviving) at Years 5, 10,
and 15 is 5963, 5262, and 2431, respectively.

1.0 + Censored

0.8
Survival probability

0.6 Normal rotation


Clockwise rotation
Counterclockwise
0.4

0.2

0.0
0 5 10 15
Follow-up in years

Figure 2 Kaplan– Meier survival curves for cardiovascular mortality stratified by rotation status. Number of participants at risk (surviving) at Years
5, 10, and 15 is 5963, 5262, and 2431, respectively.

Table 2 Rotation status and risk of all-cause mortality and cardiovascular mortality

All-cause mortality Cardiovascular mortality


.................................................................. ..................................................................
Clockwise rotation Counterclockwise Clockwise rotation Counterclockwise
HR (95% CI) rotation HR (95% CI) rotation
...............................................................................................................................................................................
Model 1a 1.51 (1.21–1.88) 0.80 (0.70–0.90) 1.73 (1.17– 2.54) 0.99 (0.79–1.22)
b
Model 2 1.45 (1.16–1.81) 0.86 (0.76–0.97) 1.64 (1.11– 2.41) 1.07 (0.86–1.33)
Model 3c 1.43 (1.15–1.78) 0.87 (0.77–0.98) 1.61 (1.09– 2.37) 1.07 (0.86–1.33)

a
Adjusted for age, sex, and race.
b
Adjusted for variables in Model 1 variables plus smoking status, systolic blood pressure, body mass index, blood pressure medications, dyslipidaemia, and diabetes mellitus.
c
Adjusted for variables in Model 2 plus any other ECG abnormalities, cancer, and pulmonary disease (bronchial asthma and chronic obstructive pulmonary disease).
Transition zone and mortality 135

of counterclockwise rotated hearts. Clockwise rotation was fre-

Adjusted for age, sex, and race, smoking status, systolic blood pressure, body mass index, blood pressure medications, dyslipidaemia, diabetes mellitus, any other ECG abnormalities, cancer, and pulmonary disease (bronchial asthma and chronic
Interaction P-value
.........................................................................................................
..................................................
.............................................................................................................................................................................................................................................
quently seen with right ventricular heart disease compressing the
left ventricle and noted in dilated cardiomyopathy when the septal
angle was not elevated. In other previous reports, clockwise rotation
has been reported with acute massive pulmonary embolism.25,26 In
Counterclockwise rotation our study and despite excluding participants with history of CVD, de-

0.667

0.816

0.529
viation from normal rotation was very common. This suggests that
not all deviation from normal rotation has an anatomical basis, but
1.10 (0.79, 1.55)
1.02 (0.77, 1.37)
1.06 (0.79, 1.43)
1.02 (0.73, 1.41)
1.22 (0.74, 2.03)
01.02 (0.80, 1.30)
instead could implicate electrophysiological changes that worth
HR (95% CI)a

further investigation.
To this point, there has been limited literature concerning the clin-
ical associations and prognostic significance of horizontal rotation. In
1987, Rajala et al.27 reported an association between clockwise rota-
tion and cerebrovascular accident mortality in a geriatric sample of
.................................................
Interaction P-value

Finnish population. Also, Horibe et al.28 published data from the Japa-
nese National Surgery NIPPON DATA80 which showed a high rate
of all-cause mortality with clockwise rotation. Most recently, Naka-
Table 3 Rotation status and risk of all-cause mortality and cardiovascular mortality in sex, race, and age subgroups

mura et al. examined the association between rotation and mortality


Cardiovascular mortality

0.511

0.346

0.386

in 3958 Japanese men and 5109 Japanese women greater than 30


years of age. In that study, there was an increased risk of mortality
Clockwise rotation

with clockwise rotation and an inverse association of cardiovascular


2.01 (1.13, 3.57)
1.48 (0.87, 2.53)

1.39 (0.79, 2.43)


2.23 (0.95, 5.24)
1.48 (0.95, 2.28)
2.00(1.16, 3.44)

mortality with counterclockwise rotation. Our findings from


a
HR (95% CI)

NHANES III, an ethnically diverse sample of the general US popula-


tion, accord with the results from these patient-based and non-US
populations. Unlike our study, however, prior studies had several
major limitations that risk the validity of their results. First, none of
the prior studies used chest electrode locator to standardize chest
........................................................................................................
..................................................
Interaction P-value

electrode locations. It is known that appropriate ascertainment of


electrocardiographic rotation requires careful and standardized
chest electrode locations. Secondly, ECG tracings in almost all of
Counterclockwise rotation

these studies were not digital, and subsequently were manually


0.691

0.946

0.764

read. This risks the reproducibility of the results. Finally, there was
lack of ethnic diversity in all of prior studies. In contrast, in
NHANES, digital ECG tracings were recorded using a chest elec-
0.854(0.70, 1.01)
0.84 (0.70, 1.01)
0.88 (0.75, 1.04)
0.83 (0.70, 0.98)

0.83 (0.64, 1.08)


0.87 (0.76, 1.00)
a

trode locator as part of standardized protocol, and the ECGs were


HR (95% CI)

automatically processed at a central ECG core laboratory, and we


were able to examine the consistency of the results across subgroups
of sex, race, and age to confirm the generalizability of our results.
Our results should be read in the context of certain limitations. Al-
though we have adjusted for several potential confounders, we rec-
Interaction P-value
.................................................

ognize the possibility of residual confounding which is the case in all


similar observational studies. We could not examine the association
between rotation as an electrophysiological phenomenon with
cardiac function and structure as measured by echocardiography
0.982

0.401

0.408

because such data were not available. In addition, NHANES III does
All-cause mortality
Clockwise rotation

not have serial ECGs that could have enabled us to examine the
natural history of rotation over time. Despite these limitations, this
1.47 (1.05, 2.04)
1.47 (1.09, 1.98)
1.57 (1.14, 2.17)
1.30 (0.96, 1.77)
1.71 (1.07, 2.74)
1.35 (1.05,1.74)
a
HR (95% CI)

is the first large study from a racially diverse, community-based US


population that examined the prognostic significance of horizontal
obstructive pulmonary disease).

rotation. Other strengths include well-ascertained outcomes and


variables including standard ECG recording using a chest electrode
locator and centrally automated process of reading the ECG tracings.
Age ,55 years
Age .55 years

In conclusion, deviation from normal horizontal rotation is a


Non-Whites

common ECG finding in individuals free of CVD. Clockwise rotation


Women

Whites

is associated with a substantial increase in all-cause mortality and


Men

CVD mortality compared with normal rotation. On the other


a

hand, counterclockwise rotation has an inverse association with all-


136 N. Bradford et al.

cause mortality and no significant association with CVD mortality. 12. Rautaharju PM, Zhang ZM, Haisty WK Jr, Prineas RJ, Kucharska-Newton AM,
Rosamond WD et al. Electrocardiographic predictors of incident heart failure in
These findings suggest that horizontal rotation carries important
men and women free from manifest cardiovascular disease (from the Atheroscler-
prognostic information, which may merit routine evaluation. osis Risk in Communities [ARIC] study). Am J Cardiol 2013;112:843 –9.
Further investigation is needed to look into the mechanisms of devel- 13. Zhang ZM, Rautaharju PM, Soliman EZ, Manson JE, Martin LW, Perez M et al. Differ-
ent patterns of bundle-branch blocks and the risk of incident heart failure in the
oping rotation and its progression overtime as well as considering re-
Women’s Health Initiative (WHI) study. Circ Heart Fail 2013;6:655–61.
defining normal rotation. 14. Rautaharju PM, Zhang ZM, Warren J, Gregg RE, Haisty WK, Kucharska-Newton AM
et al. Electrocardiographic predictors of coronary heart disease and sudden cardiac
Conflict of interest: none declared. deaths in men and women free from cardiovascular disease in the Atherosclerosis
Risk in Communities study. J Am Heart Assoc 2013;2:e000061.
15. Li Y, Dawood FZ, Chen H, Jain A, Walsh JA III, Alonso A et al. Minor isolated Q waves
Funding and cardiovascular events in the MESA study. Am J Med 2013;126:450.e9 –16.
16. Mandyam MC, Soliman EZ, Heckbert SR, Vittinghoff E, Marcus GM. Long-term out-
This work was supported in part by the National Center for Advancing
comes of left anterior fascicular block in the absence of overt cardiovascular disease.
Translational Sciences of the National Institutes of Health under Award JAMA 2013;309:1587 –8.
Number UL1TR000454 and KL2TR000455 to A.J.S. 17. Carnethon MR, Ning H, Soliman EZ, Lewis CE, Schreiner PJ, Sidney S et al. Associ-
ation of electrocardiographically determined left ventricular mass with incident dia-
betes, 1985 –1986 to 2010 –2011: Coronary Artery Risk Development in Young
References Adults (CARDIA) study. Diabetes Care 2013;36:645–7.
1. Moyer VA. Screening for coronary heart disease with electrocardiography: U.S. Pre- 18. Zhang ZM, Prineas RJ, Soliman EZ, Baggett C, Heiss G; ARIC Research Group. Prog-
ventive Services Task Force recommendation statement. Ann Intern Med 2012;157: nostic significance of serial Q/ST-T changes by the Minnesota Code and Novacode in
512 –8. the Atherosclerosis Risk in Communities (ARIC) study. Eur J Prev Cardiol 2012;19:
2. Bakhoya VN, Kurl S, Laukkanen JA. T-wave inversion on electrocardiogram is related 1430 –6.
to the risk of acute coronary syndrome in the general population. Eur J Prev Cardiol 19. Ilkhanoff L, Liu K, Ning H, Nazarian S, Bluemke DA, Soliman EZ et al. Association of
2014;21:500 –6. QRS duration with left ventricular structure and function and risk of heart failure in
3. Inohara T, Kohsaka S, Okamura T, Watanabe M, Nakamura Y, Higashiyama A et al. middle-aged and older adults: the Multi-Ethnic Study of Atherosclerosis (MESA). Eur
Cumulative impact of axial, structural, and repolarization ECG findings on long-term J Heart Fail 2012;14:1285 –92.
cardiovascular mortality among healthy individuals in Japan: National Integrated 20. Soliman EZ, Howard G, Cushman M, Kissela B, Kleindorfer D, Le A et al. Prolonga-
Project for Prospective Observation of Non-Communicable Disease and its tion of QTc and risk of stroke: The REGARDS (REasons for Geographic and Racial
Trends in the Aged, 1980 and 1990. Eur J Prev Cardiol 2013. [Epub ahead of print] Differences in Stroke) study. J Am Coll Cardiol 2012;59:1460 –7.
PubMed PMID: 23918839. 21. Soliman EZ, Prineas RJ, Case LD, Russell G, Rosamond W, Rea T et al. Electrocardio-
4. Hadaegh F, Hatami M, Mohebi R, Hasheminia M, Bozorgmanesh M, Sheikholeslami F graphic and clinical predictors separating atherosclerotic sudden cardiac death from
et al. Electrocardiography-defined silent CHD and risk of cardiovascular events incident coronary heart disease. Heart 2011;97:1597 –601.
among diabetic patients in a Middle Eastern population. Eur J Prev Cardiol 2012;19: 22. Prineas RJ, Blackburn H. The Minnesota Code Manual of Electrocardiographic Findings:
1227 –33. Standards and Procedures for Measurement and Classification. Boston, MA: John
5. Godsk P, Jensen JS, Abildstrøm SZ, Appleyard M, Pedersen S, Mogelvang R. Prognos- Wright—PSG, Inc.; 1982. p330.
tic significance of electrocardiographic Q-waves in a low-risk population. Europace 23. Nakamura Y, Okamura T, Higashiyama A, Watanabe M, Kadota A, Ohkubo T et al.
2012;14:1012 – 7. Prognostic values of clockwise and counterclockwise rotation for cardiovascular
6. Schröder K, Wegscheider K, Wenger NK, Vettorazzi E, Schröder R. Resting electro- mortality in Japanese subjects: a 24-year follow-up of National Integrated Project
cardiogram predicts mortality in postmenopausal women with coronary heart for Prospective Observation of Noncommunicable Disease and Its Trends in the
disease or with risk factors for coronary heart disease. Eur J Prev Cardiol 2012. Aged; 1980– 2004 (NIPPON DATA80). Circulation 2012;125:1226 –33.
[Epub ahead of print] PubMed PMID: 22752417. 24. Tahara Y, Mizuno H, Ono A, Ishikawa K. Evaluation of the electrocardiographic tran-
7. Usoro AO, Bradford N, Shah AJ, Soliman EZ. Risk of mortality in individuals with low sitional zone by cardiac computed tomography. J Electrocardiol 1991;24:239 –45.
QRS voltage and free of cardiovascular disease. Am J Cardiol 2014;113:1514 –7. 25. Yoshinaga T, Ikeda S, Skikuwa M, Miyahar Y, Kohno S. Relationship between ECG
8. Li Y, Shah AJ, Soliman EZ. Effect of electrocardiographic P-wave axis on mortality. Am findings and pulmonary artery pressure in patients with acute massive pulmonary
J Cardiol 2014;113:372 –6. thromboembolism. Circulation 2003;67:229 – 32.
9. Soliman EZ, Safford MM, Muntner P, Khodneva Y, Dawood FZ, Zakai NA et al. Atrial 26. Stein PD, Dalen JI, McIntrye KM, Sasahra AA, Wenger NK, Willis PW. The electro-
fibrillation and the risk of myocardial infarction. JAMA Intern Med 2014;174:107 – 14. cardiogram in acute pulmonary embolism. Prog Cardiovasc Dis 1975;17:247 –57.
10. Walsh JA III, Prineas R, Soliman EZ, Liu K, Ning H, Daviglus ML et al. Association of 27. Rajala S, Haavisto M, Kaltiala K, Mattila K. Electrocardiographic findings and 5-year
isolated minor non-specific ST-segment and T-wave abnormalities with subclinical cardiovascular mortality in very old people. Ann Clin Res 1987;19:324 – 7.
atherosclerosis in a middle-aged, biracial population: Coronary Artery Risk Devel- 28. Horibe H, Kasagi F, Kagaya M, Matsutani Y, Okayama A, Ueshima H. A nineteen-year
opment in Young Adults (CARDIA) study. Eur J Prev Cardiol 2013;20:1035 –41. cohort study on the relationship of electrocardiographic findings in all-cause mortal-
11. Mandyam MC, Soliman EZ, Alonso A, Dewland TA, Heckbert SR, Vittinghoff E et al. ity among subjects in the National Survey on Circulatory Disorders, NIPPON
The QT interval and risk of incident atrial fibrillation. Heart Rhythm 2013;10:1562 –8. DATA80. J Epidemiol 2005;15:125 –34.

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