Relationship between fragmented QRS complex

and left ventricular systolic and diastolic function

in kidney transplant patients
Background—Kidney transplant is a most important replacement therapy. It reduces Şükrü Ulusoy, MD, Gulsum
cardiovascular mortality and morbidity but does not fully correct impairments in Ozkan, MD, Adem Adar, MD,
cardiac function. Fragmented QRS (fQRS) complex includes various RSR′ patterns
Hüseyin Bektaş, MD, Abdulka-
with different QRS complex morphologies on electrocardiograms.
Objective—To analyze fQRS frequency and the relationship between fQRS and dir Kırış, MD, Şükrü Çelik, MD
Karadeniz Technical University (SU, GO,
left ventricular function in kidney transplant patients.
AK), Ahi Evren Thoracic and Cardiovas-
Method—After demographic data on 39 kidney transplant patients were recorded cular Surgery Training and Research
and biochemical parameters were investigated, electrocardiograms were evaluated Hospital (AA, HB, ŞÇ), Trabzon, Turkey
for the presence of fQRS. Left ventricular ejection fraction, mitral annular plane
systolic excursion, peak early diastolic mitral annular velocities, late diastolic mitral Corresponding author: Şükrü Ulusoy,
annular velocities, and systolic mitral annular velocity were analyzed. MD, Karadeniz Technical University,
Results—Fragmented QRS was detected in 16 patients. A history of hypertension School of Medicine, Department of
was associated with the presence of fQRS. Patients with fQRS had significantly Nephrology, 61080 Trabzon, Turkey
lower systolic and peak early diastolic mitral annular velocities, mitral annular (e-mail: sulusoy2002@yahoo.com)
plane systolic excursion, and left ventricular ejection fraction than did patients
To purchase electronic or print reprints,
without fQRS (P = .03, .01, <.001, and .03, respectively).
contact:
Conclusion—Detection of fQRS on electrocardiograms may be useful in predict- American Association of Critical-Care Nurses
ing systolic and diastolic dysfunction of the left ventricle in kidney transplant 101 Columbia, Aliso Viejo, CA 92656
patients. (Progress in Transplantation. 2014;24:146-151) Phone (800) 899-1712 (ext 532) or
(949) 448-7370 (ext 532)
©2014 NATCO, The Organization for Transplant Professionals Fax (949) 362-2049
doi: http://dx.doi.org/10.7182/pit2014200 E-mail reprints@aacn.org

C ardiac functional and structural abnormalities are

common in patients with chronic kidney disease,
especially those receiving hemodialysis. Left ventricu-
lar and atrial dilatation and diastolic dysfunction, and
especially left ventricular hypertrophy, are common
cardiac abnormalities in such patients.1,2 As a reflection
of these impairments, cardiovascular events remain the
main cause of mortality in patients with chronic kidney
disease today.3
Today, kidney transplant is an increasingly used
renal replacement therapy. Thanks to advances in sur-
gical technique and immunosuppressive agents, kidney
transplant is considered the best replacement therapy.
Kidney transplant prolongs life and reduces mortality
better than dialysis. 4 The decrease in mortality is
thought to be associated with a decline in cardiac com-
plications. In fact, according to data for 2010 from the
US Renal Data System, cardiac problems account for
around 40% of hospitalizations in the pretransplant
period, but only 8.7% in the second year after trans-
plant.3 However, although different studies have yielded
various results in kidney transplant recipients, com-
plete improvement in cardiac function does not seem
to occur, regardless of the drugs used after transplant,
cardiac function before transplant, duration of renal
replacement therapy before transplant, and various post-
transplant abnormalities.2,5,6 Therefore, cardiac evalua-
tion must be performed at specific intervals in kidney
transplant recipients.
Fragmented QRS complex (fQRS) includes var-
ious RSR′ patterns with different morphologies of the
QRS complexes with or without the Q wave on a rest-
ing 12-lead electrocardiogram (ECG). Various RSR′
patterns include an additional R wave (R′) or notching
in the nadir of the S wave, or the presence of more than
1 R′ (fragmentation) in 2 contiguous leads, correspon-
ding to the territory of a major coronary artery.7 Myocar-
dial scarring,8 myocardial fibrosis,9 various structural

146 Progress in Transplantation, Vol 24, No. 2, June 2014

 Fragmented QRS complex and left ventricular function in kidney transplant patients
I aVR
aVL
II
III aVF
Figure Examples of fragmented QRS complex (arrows).
anomalies of the heart,10 and ventricular dysrhythmia11
are associated with fQRS. Das et al 8 reported that
fQRS can be used to estimate mortality and cardiovas-
cular events in patients with coronary artery disease.
However, no studies have shown the presence of
fQRS in kidney transplant patients or its relationship
to left ventricular function.
The purpose of this study was to evaluate the inci-
dence of fQRS, which is easy to detect on ECGs in
clinical practice and has not previously been evaluated
in kidney transplant patients, and to determine the rela-
tionship between fQRS and left ventricular function.
Materials and Methods
Once approval had been granted by the local
ethics committee from the Karadeniz Technical Uni-
versity Faculty of Medicine, 39 patients being followed
up at the adult kidney transplant clinic who agreed to
participate were enrolled in the study. Patients were
given a detailed physical examination. The following
demographic data were collected for all patients: age,
sex, body mass index (calculated as weight in kilo-
grams divided by height in meters squared), drugs
used, history of diabetes mellitus, history of hyperten-
sion, cigarette use, primary kidney diseases, duration
of primary disease, and duration of kidney transplant
follow-up. Patients with the following features were
excluded from the study: history of acute coronary
syndrome, significant organic disease of a heart valve,
history of coronary bypass, nonischemic dilated car-
diomyopathy, history of cancer, findings indicating
active infection or inflammation, bundle-branch block
or intraventricular conduction delay (QRS >120 ms)
at ECG, or permanent pacemakers.
Progress in Transplantation, Vol 24, No. 2, June 2014
II 0.02 V2 0.03
III 0.01 V3 0.04
aVR -0.01 V4 0.04
aVL 0.01 V5 0.04
aVF 0.01 V6 0.02
V1 V4
V2 V5
V3 V6
Complete blood cell count, serum urea nitrogen,
creatinine, calcium, phosphorus, low-density lipopro-
tein, high-density lipoprotein, triglyceride, and albumin
values were measured in blood specimens collected
for biochemical tests. Glomerular filtration rate was
calculated according to the short formula from the
Modification of Diet in Renal Disease Study Group.12
ECG
Standard 12-lead surface resting ECGs (filter range,
0.5-150 Hz, 25 mm/s, 10 mm/mV) were recorded from
all patients. These ECGs were reviewed blindly by 2
independent authors (A.A., H.B.). Fragmented QRS
was defined by the presence of various RSR′ patterns
(QRS <120 ms) with or without a Q wave, which
includes an additional R wave (R′) or notching of the
R wave or S wave, or the presence of more than one
R′ (fragmentation) without typical bundle-branch block
in 2 contiguous leads corresponding to a major lead
set for the territory of a major coronary artery (see
Figure).8,9 Standard 12-lead ECG was analyzed with-
out using any magnification, and fragmentations were
considered to be present if a visually identifiable sig-
nal was apparent in all complexes of a particular lead.
The QRS duration was determined by the longest
QRS in any lead.
Echocardiography
All patients were placed in the left lateral decubi-
tus position for echocardiography. Echocardiographic
examinations were recorded on commercially avail-
able equipment (Vivid 7 GE Medical System) with a
phased-array 3.5-MHz transducer and software for
tissue Doppler imaging.
147
Ulusoy et al
Two-Dimensional Echocardiography and
Pulsed-Wave Tissue Doppler Imaging
Two echocardiographers unaware of the study per-
formed the examinations. They were blinded to the ECGs
and to the clinical status of each patient. The conven-
tional M-mode, B-mode, and Doppler parameters were
measured according to the American guidelines.13 Left
ventricular ejection fraction (LVEF) was calculated by
using a Simpson biplane method.13 The measurements
obtained directly in the M-mode on the 2-dimensional
image included left atrial diameter, left ventricular dias-
tolic diameter, left ventricular systolic diameter, left
ventricular posterior wall thickness, interventricular
septum thickness, transmitral filling velocities includ-
ing peak early and late diastole, and E-wave decelera-
tion time.14 The tissue Doppler imaging was performed
from the lateral mitral annulus. Tissue velocities includ-
ing peak early (Em) and late (Am) diastolic mitral annu-
lar velocities and systolic mitral annular velocity (Sm)
were analyzed. Mitral annular plane systolic excursion
(MAPSE) was performed with the M-mode cursor placed
at mitral lateral and septal angles. MAPSE was meas-
ured as the distance between the innermost point and
the outermost point of the motion displacement.
Statistical Analysis
All the results are expressed as mean (standard
deviation). Demographic, biochemical, and echocardio-
graphic variables were compared by using a Student t
test or the Mann-Whitney U test. A χ2 test was used for
categorical variables. Pearson and Spearman correla-
tion coefficients were calculated in the correlation
analysis. The significance level was set at P less than
.05. SPSS software version 13.0 (SPSS, Inc) was used
for statistical analyses.
Results
No fQRS was detected in 23 (mean [SD] age, 37.30
[12.29] y; 8 female/15 male) of the 39 kidney trans-
plant patients in the study, but fQRS was present in the
other 16 (mean [SD] age, 42.00 [15.30] y; 4 female/12
male). Patients with fQRS did not differ significantly
from patients without fQRS with respect to age, sex,
body mass index, medications, duration of transplant,
primary disease, history of diabetes mellitus, or duration
of chronic kidney disease. A history of hypertension was
present in 81.1% of the patients with fQRS and 47.8% of
the patients without fQRS (P = .04). A positive correla-
tion was found between presence of fQRS and history of
hypertension (P = .04, r = 0.34). Biochemical parameters
and glomerular filtration rates did not differ significantly
between the fQRS and non-fQRS patients (Table 1).
Echocardiography
Routine 2-dimensional echocardiographic meas-
urements for patients with fQRS and patients without
148
fQRS are shown in Table 2. The LVEF was signifi-
cantly lower (P = .03) in patients with fQRS (mean,
61.25%; SD, 2.23%) than in patients without fQRS
(mean, 63.82%; SD, 3.91%). None of the other
parameters differed significantly between the 2 groups
(Table 2).
Patients’ pulsed-wave Doppler tissue imaging
measurements are given in Table 3. Mean Em in
patients with fQRS was 10 (SD, 0.02) cm/s, compared
with 12 (SD, 0.03) cm/s in patients without fQRS,
and the difference was statistically significant (P=.03).
Mean Sm in patients with fQRS was 9 (SD, 0.02) cm/s,
significantly lower (P = .01) than the mean Sm in
patients without fQRS, which was 11 (SD, 0.02) cm/s.
Mean Am values did not differ significantly between
patients with or without fQRS, but MAPSE was sig-
nificantly lower (P < .001) in patients with fQRS, at
13.81 (SD, 1.79) mm, compared with 16.95 (2.61) mm
in patients without fQRS (Table 3).
Correlation Between fQRS and
Echocardiography Parameters
A negative correlation was found between the pres-
ence of fQRS and LVEF (P = .047, r = -0.32), and also
between the presence of fQRS and Em (P = .047, r = -
0.32), Sm (P = .02, r = -0.36), and MAPSE (P < .001,
r = -0.62).
Discussion
Our aim in this study was to evaluate the param-
eters affecting development of fQRS in kidney trans-
plant patients and to investigate the relationship
between fQRS and left ventricular function. None of
our demographic and biochemical parameters were
associated with the presence of fQRS in our study
group, except for a history of hypertension. Values
of Em, Sm, MAPSE, and ejection fraction were sig-
nificantly lower in patients with fQRS than in
patients without fQRS.
Structural and functional cardiac abnormalities
are common in patients with chronic kidney disease
and lead to an increase in mortality and morbidity.3,15
Researchers in several studies have investigated
whether or not kidney transplant causes an improve-
ment in these cardiac abnormalities. Results of those
studies2,5,16-18 indicated that left ventricular hypertro-
phy, left ventricular end-diastolic diameter, left atrial
diameter, LVEF, and left ventricular systolic and dias-
tolic functions all improved after transplant. However,
cardiac functions do not fully return to normal after
transplant, a situation that has been attributed to vari-
ous factors affecting cardiac function in kidney trans-
plant patients.
Although different results are reported in various
studies, factors affecting cardiac function include a long
period of hemodialysis before transplant; hypertension;
Progress in Transplantation, Vol 24, No. 2, June 2014
 Fragmented QRS complex and left ventricular function in kidney transplant patients

Table 1 Clinical and laboratory characteristics of study population

Fragmented QRS complex

Characteristic Absent (n = 23) Present (n = 16)
Age, mean (SD), y 37.30 (12.29) 42.00 (15.30)
Sex, female/male 8/15 4/12
Body mass index,a mean (SD) 25.39 (4.34) 24.80 (3.02)
Blood pressure, mean (SD), mm Hg
Systolic 135.00 (12.00) 137.00 (15.00)
Diastolic 90.00 (5.00) 95.00 (4.00)
Months of primary disease, mean (SD) 84.78 (62.07) 108.62 (94.28)
Months since transplant, mean (SD) 41.17 (58.17) 37.68 (50.10)
Medications, % of patients
Steroid + Tac + MMF 60.90 62.50
Steroid + CsA + MMF 34.80 37.50
Steroid + MMF 4.30 0
Primary renal disease, % of patients
Unknown 43.50 37.50
Hypertensive nephrosclerosis 17.40 12.50
Polycystic kidney disease 4.30 6.30
Diabetes mellitus 21.70 25.00
Glomerulonephritis 4.30 12.60
Obstructive uropathy 8.70 6.30
Hypertension history,b % 47.80 81.13
Glomerular filtration rate, mL/min 58.78 (15.02) 63.37 (25.92)
Serum urea nitrogen, mg/dL 20.80 (9.25) 18.22 (12.79)
Creatinine, mg/dL 1.34 (0.54) 1.28 (0.58)
Calcium, mg/dL 9.61 (0.61) 9.75 (0.56)
Phosphorus, mg/dL 3.30 (0.69) 3.16 (0.71)
Albumin, g/dL 4.61 (0.36) 4.50 (0.32)
Cholesterol, mean (SD), mg/dL
Low-density lipoprotein 117.46 (33.18) 129.12 (38.00)
High-density lipoprotein 45.57 (14.64) 52.50 (10.60)
Triglycerides, mg/dL 175.08 (85.20) 154.20 (78.46)
Hemoglobin, g/dL 11.8 (1.25) 12.00 (0.87)
Abbreviations: CsA, cyclosporine; MMF, mycophenolate mofetil; Tac, tacrolimus.
SI conversion factors: To convert serum urea nitrogen to mmol/L, multiply by 0.357; to convert creatinine to μmol/L, multiply by 88.4; to convert calcium to mmol/L,
multiply by 0.25; to convert phosphorus to mmol/L, multiply by 0.323; to convert albumin to g/L, multiply by 10; to convert cholesterol to mmol/L, multiply by
0.0259; to convert triglycerides to mmol/L, multiply by 0.0113.
a Calculated as body mass in kilograms divided by height in meters squared.
b The only significant difference between the 2 groups (P = .04). Statistical significance was set at P < .05.

sex of the patient; posttransplant anemia; graft func-
tion; significance level; pretransplant LVEF, peak
transmitral filling velocity in early diastole, and peak
mitral annular velocity in early diastole; presence of
arteriovenous fistula; angiotensin-converting enzyme
gene polymorphism; and use of cyclosporine.2,6,16-21
In our study, we demonstrated the presence of fQRS,
which had been associated with impairment of myocar-
dial structure in previous studies, in posttransplant
patients and its relation to left ventricular systolic and
diastolic dysfunction.
Fragmented QRS is defined as various RSR′ pat-
terns with or without Q waves on a 12-lead resting
ECG. Clinical studies have shown that presence of
fQRS is associated with scarring after myocardial
infarction. In addition, myocardial perfusion imaging
has shown that regional fQRS is associated with focal
regional myocardial scarring. 7,9,22 The presence of
fQRS in patients with known or suspected coronary
artery disease leads to a need for revascularization
after myocardial infarction and to an increase in
deaths of cardiac origin.8,9,11 Using magnetic resonance
imaging, Park et al23 showed a powerful correlation
between presence of fQRS and myocardial fibrosis.
Studies10,11 have shown that presence of fQRS is corre-
lated with development of ventricular arrhythmia and

Progress in Transplantation, Vol 24, No. 2, June 2014 149

Ulusoy et al
Table 2 Two-dimensional echocardiographic measurementsa
Fragmented QRS complex
Absent
Measurement (n = 23)
Left ventricular diastolic
diameter, mm 43.86 (4.86)
Left ventricular systolic
diameter, mm 27.69 (4.55)
Interventricular septum
thickness, mm 10.39 (1.55)
Left atrial diameter, mm 36.26 (4.85)
Ejection fraction,b % 63.82 (3.91)
Peak early transmitral filling
velocity, m/s 90.60 (18.57)
Late transmitral filling
velocities, m/s 76.04 (19.91)
E-wave deceleration time, ms 227.82 (38.81) 229.43 (61.04)
Posterior wall thickness, mm 10.26 (1.60)
a Allvalues are presented as mean (SD).
b The
only significant difference between the 2 groups (P = .03). Statistical sig-
nificance was set at P < .05.
structural cardiac anomalies. In our study, we evalu-
ated the presence of fQRS in kidney transplant
patients and the parameters affecting this. Except for a
history of hypertension, patients with or without fQRS
did not differ in terms of either demographic data or
biochemical parameters. Fragmented QRS was more
common in patients with a history of hypertension.
Remodeling is known to occur gradually in the
left ventricle of the heart in hypertensive persons. This
remodeling appears in the form of myocardial hyper-
trophy and perivascular hypertrophy and fibrosis as a
result of the compensatory mechanism for pump func-
tion maintenance in association with an increase in
afterload. Over the years, hypertrophy and fibrosis
lead to impairment in cardiac function.24,25 The pres-
ence of myocardial scarring and fibrosis is correlated
with fQRS 7,9,22,23 ; however, no studies to date have
shown a correlation between presence of fQRS and
myocardial function in hypertensive persons. We think
that the correlation of a history of hypertension with
fQRS that we found in our study is a reflection of
myocardial fibrosis developing in hypertensive persons.
Another aim of this study was to evaluate the
relationship between left ventricular systolic and dias-
tolic functions and fQRS in kidney transplant patients.
We used tissue Doppler imaging as well as 2-dimen-
sional Doppler echocardiography to evaluate left ven-
tricular function. Doppler imaging permits evaluation
of velocities of myocardial wall motion during the
myocardial cycle and is used in the analysis of global
and regional left ventricular systolic functions and
150
Table 3 Pulsed-wave Doppler tissue ımaging measurementsa
Fragmented QRS complex
Present Measurement Absent Present Pb
(n = 16) Peak early diastolic mitral
annular velocity, cm/s 12.87 (0.03) 10.44 (0.02) .03
45.50 (4.54) Late diastolic mitral
annular velocity, cm/s 11.48 (0.03) 10.56 (0.01 NS
28.81 (4.08) Systolic mitral annular
velocity, cm/s 11.61 (0.02) 9.63 ± 0.02 .01
10.87 (1.08) Mitral annular plane
35.81 (5.24) systolic excursion, mm 16.95 (2.61) 13.81±1.79 <.001
61.25 (2.23) a All values are presented as mean (SD).
b Statistical significance was set at P < .05
90.68 (25.63)
abnormal left ventricular relaxation. 2 6 , 2 7 Various
83.37 (27.82)
parameters are used in the evaluation of systolic and
diastolic function. Em and Am are reliable parameters
10.75 (1.18) widely used in the analysis of left ventricular dysfunc-
tion.27 Studies in recent years have shown that Sm is a
more reliable parameter than LVEF in the evaluation
of left ventricular systolic functions.28 Magnetic reso-
nance imaging studies29 show that MAPSE, on the
other hand, correlates with left ventricular systolic
function. In our study, Em values in patients with
fQRS were lower than in patients without fQRS. This
finding supports the presence of left ventricular dias-
tolic dysfunction in patients with fQRS. Additionally,
our determination of significantly lower Sm, MAPSE,
and LVEF values in patients with fQRS supports left
ventricular systolic impairment. In light of these data,
we thought that the presence of fQRS in kidney trans-
plant patients may be correlated with impairment in
left ventricular systolic and diastolic functions.
The fact that this study, in which we evaluate the
presence of fQRS in kidney transplant recipients and
its association with left ventricular systolic and dias-
tolic function, has a cross-sectional design imposes
various limitations. First, it is unclear whether fQRS
was present before transplant. Second, we did not
assess prospectively the effect of the presence of
fQRS on mortality and morbidity. However, we think
that new prospective, randomized studies can be
planned and an answer to these questions found in
light of the present study findings.
Conclusion
Although cardiac mortality and morbidity decrease
compared with the pretransplant period in kidney
transplant patients, they do not fully return to normal.
It will therefore be useful to monitor cardiac function
at specific intervals. In this study, we showed the pres-
ence of fQRS in kidney transplant patients by using
12-lead ECG, an easily accessible and economical
test. We think that this parameter, which can easily be
Progress in Transplantation, Vol 24, No. 2, June 2014
 Fragmented QRS complex and left ventricular function in kidney transplant patients
evaluated in clinical practice, can also be a useful guide
in predicting left ventricular function in kidney trans-
plant patients. The effect of the presence of fQRS
on mortality and morbidity should be examined further
in studies with more patients and clinical follow-up.
Financial Disclosures
None reported.
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