Journal of Pediatric Cardiology and Cardiac Surgery 3(1): 20‒27 (2019)

Original Article

Stretching of the Right Ventricle in the Lower Direction is
Associated with a Crochetage Pattern
on Electrocardiogram
Hideharu Oka, MD, Kouichi Nakau, MD, Aya Kajihama, MD,
and Hiroshi Azuma, MD, PhD
Department of Pediatrics, Asahikawa Medical University, Hokkaido, Japan

Background: The crochetage pattern is an important finding in atrial septal defect (ASD); however, the reason
for this pattern is unclear. We hypothesized that the crochetage pattern is related to the right ventricle stretch
direction.
Methods: Stretch values were calculated in eight ASD patients with the crochetage pattern, eight ASD patients
without the crochetage pattern, and eight controls who underwent cardiac catheterization. The right ventricle
systolic area was subtracted from the right ventricle diastolic area in posteroranterior (PA) and left lateral viewson right ventricle angiography. The area was divided into three parts at the position of the tricuspid valve andadjusted according to body surface area.
Results: ASD patients with the crochetage pattern did not have significantly higher pulmonary/systemic bloodflow ratios or right ventricle end diastolic volume indices than those without the crochetage pattern. Stretch values towards the left were higher in ASD patients with the crochetage pattern than in controls. Stretch values in
the lower direction in the PA view were higher in ASD patients with the crochetage pattern than in those without
the crochetage pattern. Multiple regression analysis revealed that stretch values in the lower direction in the PA
view influenced the number of crochetage patterns.
Conclusion: ASD patients with the crochetage pattern have significantly higher stretch values in the lower andleft directions in the PA view than those without the crochetage pattern and controls. Stretch values in the lower
direction of the right ventricle are associated with the crochetage pattern in ASD patients.

Keywords: atrial septal defect, electrocardiography, right ventricle

Background
Secundum atrial septal defect (ASD) is a common
type of congenital heart disease. An electrocardiogram(ECG) is useful in the diagnosis of ASD. The characteristic ECG patterns of secundum ASD include right bundle-branch block (RBBB), right axis deviation (RAD),
isolated negative T wave, and/or rod/stroke (R/S) ratio in
lead V5. Notched R waves in the inferior ECG limb leads
represent a “crochetage pattern” and were first reported
in 1959.1) Heller et al. defined the crochetage pattern as a

rapid up-and-down motion of the R wave on its ascending branch or near its zenith, with an M-shaped or a bifid
pattern in the most typical form, and the initial 80 ms of
the QRS complex in the II, III, and aVF leads is always
observed.2) The crochetage pattern is a characteristic
finding of ASD in children.3) It is believed that the ECGchanges in ASD are caused by right ventricle volume
overload, but findings are not necessarily consistent withthe right ventricle end diastolic volume index (RVEDVI)
or pulmonary/systemic blood flow ratio (Qp/Qs).4, 5)
Therefore, the crochetage pattern can also be observed

Received: May 2, 2018; Accepted: December 3, 2018
Corresponding author: Hideharu Oka, MD, Department of Pediatrics, Asahikawa Medical University, 2‒1‒1‒1 Midorigaoka Higashi,
Asahikawa 078‒8510, Japan
E-mail: oka5p@asahikawa-med.ac.jp
ORCiD: Hideharu Oka (https://orcid.org/0000-0001-8701-826X)
doi: 10.24509/jpccs.190104© 2019 Japanese Society of Pediatric Cardiology and Cardiac Surgery

21Fig. 1 Crochetage pattern in the III and aVF leadsin patients with patent foramen ovale or pulmonary stenosis, or even in patients without any pathology.3, 6) The
cause of the crochetage pattern still remains unknown.
Given that the crochetage pattern occurs as a notch of
QRS in the inferior limb leads, we hypothesized thatthe crochetage pattern is associated with the directionof right ventricular stretch in ASD patients. The aim of
this study was to determine whether the crochetage pattern is associated with the direction of right ventricular
stretch.

Methods
We conducted a retrospective study of patients withcongenital heart disease (age, 1‒21 years) who underwent cardiac catheterization in the Department ofPediatrics of Asahikawa Medical University Hospital
between January 2013 and December 2016. The patientswere divided into two groups: eight ASD patients withthe crochetage pattern (median age, 6.0 years) andeight ASD patients without the crochetage pattern(median age, 11.5 years). The data from these patientswere compared with those of a control group, which
included eight patients with a history of Kawasaki disease, postoperative aortic coarctation, or postoperativeinterrupted aortic arch (median age, 10.0 years). Noneof the patients in the control group had right ventricle
volume overload. We excluded patients with ostium
primum defect, patent foramen ovale, partial anomalous
pulmonary venous connection, and pulmonary hyper-

tension. Informed written consent was obtained fromthe patients or their parents prior to catheterization.
This study was conducted in accordance with the ethicalguidelines of the 1975 Declaration of Helsinki and wasapproved by the Institutional Review Board.
All studies were performed with a standard 12-lead
ECG with a sensitivity of 10 mm/mV and at a paper
speed of 25 mm/s. A complete right bundle-branch
block (CRBBB) was defined as a QRS duration ≥120 ms
in adults, >100 ms in children aged 4 to 16 years, and>90 ms in children aged less than 4 years. QRS waves
have an rsr′, rsR′, or rSR′ in the right precordial leads
V1 or V2, and an S wave of greater duration than the R
wave or >40 ms in leads V6 and I. An incomplete RBBB(IRBBB) was defined as a QRS duration of 110‒120 ms
in adults, 90‒100 ms in children aged between 4 and 16
years, and 86‒90 ms in children aged less than 8 years.
Other criteria were similar as for CRBBB.7) Right axis
deviation (RAD) is >120°, >100°, >140°, >120°,and >90° in 1-month-to-1-year-old, 1-to-5-year-old,
5-to-8-year-old, 8-to-16-year-old, and adult patients,
respectively.7) An isolated negative T wave was defined
as a negative T wave in V4 with discontinuous-to-positive T waves in leads V3 and V5.8) An R/S ratio of <1
in lead V5 was considered positive. The crochetage
pattern̶a notch on the R wave̶was defined as a
rapid up-and-down motion of the R wave tracing on its
ascending branch or near its zenith, with an M-shaped
or a bifid pattern in its most typical form, and the initial© 2019 Japanese Society of Pediatric Cardiology and Cardiac Surgery

22Fig. 2 How to measure the stretch value(a) is a PA and (b) is an LL view. We divided the right ventricle into three separate areas at the position of the tricuspid valve
and the position where the line drawn horizontally from the tricuspid valve on the free wall side intersects. The stretch value
was measured in six directions: in the right and lower, and left directions in the PA view, in the front and lower, and backdirections in the LL view. LL, left lateral; PA, posteroranteriorFig. 3 Images of the stretch value(a) and (b) are control images, and (c) and (d) are ASD with the crochetage pattern images. (a) and (c) are PA views, and (b)and (d) are LL views. ASD, atrial septal defect; LL, left lateral; PA, posteroranterior

J Pediatr Cardiol Card Surg Vol. 3, No. 1 (2019)

23

Table 1 Demographic and hemodynamic data
NumberGender (male)Age (years)
BSA (m2)
Electrocardiographic data
CRBBB/IRBBB
RAD
Isolated negative T wave
R/S <1 of the V5
Crochetage pattern (II/III/aVF)
Hemodynamic data
RVEF (%)
RVEDVI (mL/m2)%RVEDV (% of normal)
Qp/Qs
CI (L/min/m2)
The stretch values (cm2/m2)
the right direction (PA)the lower direction (PA)the left direction (PA)the front direction (LL)
the lower direction (LL)
the back direction (LL)

Control

ASD without the crochetage pattern

ASD with the crochetage pattern

85
10.0 (1‒17)1.10±0.36

84
11.5 (4‒21)
1.22±0.3985
6.0 (1‒18)0.96±0.48

0
0
0
0
0/0/0

0/3
0
1
1
0/0/0

1/4
1
5
0
0/8/7

64.3±3.576.3±17.0
98.2±10.91
4.69±1.28

60.3±7.4
112.7±15.0**
141.3±25.3*
2.02±1.06*
3.74±1.09

56.0±4.1*
112.8±17.6**
162.2±33.8**
2.77±0.72**
4.11±1.36

12.27±2.13
3.94±1.89
0.83±0.40
1.73±0.66
2.72±1.03
2.65±0.99

13.04±3.04
3.42±0.77
1.89±1.49
2.10±1.24
3.13±0.78
2.86±0.95

15.81±6.27
5.97±2.02†
2.57±1.37**
3.23±2.00
4.32±1.31
3.21±1.15* p<0.05 vs. control, ** p<0.01 vs. control, † p<0.05 vs. ASD without the crochetage pattern.
All parameters are expressed as mean±standard deviation, except for age, which is expressed as median. ASD, atrial septal
defect; BSA, body surface area; CI, cardiac index; CRBBB, complete right bundle-branch blocks; IRBBB, incomplete right bundle-branch blocks; LL, left lateral; PA, posteroranterior; Qp/Qs, pulmonary/systemic blood ﬂow ratio; RAD, right axis deviation;
RVEDVI, right ventricle end diastolic volume index; RVEF, right ventricular ejection fraction; R/S, rod/stroke.

80 ms of the QRS complex in the II, III, and aVF leads
was observed (Fig. 1).2)
The patients underwent cardiac catheterization for theevaluation of their hemodynamic parameters. Cardiac
catheterization was performed under the same anesthesia protocol for all patients, which included intravenous
infusion of thiopental and midazolam, blood sampling
for measurement of oxygen content (SaO2), measurement of cardiac index (CI), and Qp/Qs. The oximetry
data were used to calculate intracardiac blood flowusing the Fickʼs principle. Right ventricular volumes
were calculated from biplane cineangiocardiograms andexpressed as percentage of normal values.9) The rightventricular volume was measured using the Graham
method.
The stretch values were calculated to determine how
the right ventricle progressed between systole and diastole (Fig. 2). The stretch values were calculated as follows: We subtracted the right ventricle systolic area fromthe right ventricle diastolic area in posteroanterior (PA)and left lateral (LL) views on right ventricle angiography
and using Cardio Agent analysis software (Toshiba Medical Systems Corporation, Tochigi, Japan). We divided
the area into three parts at the position of the tricuspid

valve and the position where the line drawn horizontallyfrom the tricuspid valve on the free wall side intersects
with the right ventricle. Then, we calculated these areasusing ImageJ v1.33, downloaded from the NIH website(http://rsb.info.nih.gov/ij). We corrected the obtained
data according to the body surface area (BSA). The
stretch was measured in six directions: in the right,
lower, and left directions in the PA view; and in the front,
lower, and back directions in the LL view. A representative image showing the diﬀerences between controls
and ASD patients with the crochetage pattern is shownin Fig. 3. Fig. 3a and 3b are control images and 3c and
3d are images showing ASD with crochetage pattern. To
ensure the reproducibility of our methods, we examined
intraobserver and interobserver diﬀerences in stretch
values. There was good correlation between intraobserver and interobserver values (r=0.994 and r=0.996,
respectively).
All parameters were expressed as mean±standard
deviation, except for age, which is expressed as medianvalue. A Spearmanʼs rank correlation coeﬃcient wasused to assess the correlations between the various
parameters. Statistical diﬀerences were determinedusing a Kruskal‒Wallis test. A p-value of <0.05 indicated© 2019 Japanese Society of Pediatric Cardiology and Cardiac Surgery

24Fig. 4 The correlation between Qp/Qs and the stretch values(a‒f) The correlation between Qp/Qs and the stretch values with the corresponding directions in the PA and LL views. There
was a strong correlation between Qp/Qs and the stretch values in the left direction in the PA view (r=0.818), and the front
and lower directions in the LL view (r=0.755 and r=0.679, respectively). There was no correlation between Qp/Qs and thestretch values in the right and lower directions in the PA view (r=0.417 and r=0.286, respectively), or the back direction in
the LL view (r=0.427). LL, left lateral; PA, posteroranterior; Qp/Qs, pulmonary/systemic blood ﬂow ratio

statistical significance. The obtained data were correctedusing a Bonferroniʼs correction. A multivariate stepwise
linear regression analysis was performed to determine
the eﬀects of stretch values and hemodynamic data. Statistical calculations were performed using the Statistical
Package for the Social Sciences version 24.0 (IBM Corp.,
Armonk, NY, USA).

Results
Table 1 shows the characteristics of the patient groups.
Among the three groups, no significant diﬀerenceswere observed in terms of gender, age, BSA, and CI.
RBBB was found in five (62.5%) and three (37.5%)
ASD patients with and without the crochetage pattern,
respectively. RAD was found in one (12.5%) ASD patient
J Pediatr Cardiol Card Surg Vol. 3, No. 1 (2019)with the crochetage pattern, RAD was not found in anyof the ASD patients without the crochetage pattern.
Isolated negative T wave and R/S <1 in lead V5 were
each found in one (12.5%) ASD patient without the crochetage pattern, whereas five (62.5%) ASD patients withthe crochetage pattern had isolated negative T wave, but
none had R/S <1 in lead V5. In ASD patients with thecrochetage pattern, the patterns were detected in III andaVF in eight (100%) and seven (87.5%) patients, respectively; however, none of the ASD patients with the crochetage pattern had notched R waves in lead II. None of
the control subjects had RBBB, RAD, isolated negative T
wave, R/S <1 in lead V5, or the crochetage pattern. Right
ventricular ejection fraction (RVEF) in the patientswith the crochetage pattern was significantly lower than

25

Fig. 5 Diﬀerence of the stretch values between the 3 groups
Among ASD patients with the crochetage pattern, those without the crochetage pattern, and of the control group, no signiﬁcant diﬀerences were observed in the stretch values in the right, front, and lower direction in the LL view, or the stretch
value in the back direction (a, d‒f). The stretch value in the lower direction in the PA view was higher in the eight ASD
patients with the crochetage pattern (5.97±2.02 cm2/m2) than in the eight ASD patients without the crochetage pattern(3.42±0.77 cm2/m2, p=0.017) (b). The stretch value in the left direction in the PA view was higher in the ASD patients withthe crochetage pattern (2.57±1.37 cm2/m2) than in control subjects (0.83±0.40 cm2/m2, p<0.001) (c). ASD, atrial septal
defect; LL, left lateral; PA, posteroranterior

that in the control subjects. Qp/Qs and RVEDVI weresignificantly higher in the ASD patients than in the control subjects. However, the patients with the crochetage
pattern did not have significantly higher Qp/Qs and
RVEDVI than those without the crochetage pattern(Qp/Qs: 2.77±0.72 vs. 2.02±1.06, p=0.55; RVEDVI:
112.8±17.6 vs. 112.7±15.0 mL/m2, p=1.00). Amongthe 16 patients with ASD, only one patient in the ASD
group without the crochetage pattern was not treated.
Fig. 4a‒f shows the correlation between Qp/Qs andthe stretch values with the corresponding directionin the PA and LL views. There was a strong correlation between Qp/Qs and the stretch values in theleft direction in the PA view (r=0.818), and in thefront and lower directions in the LL view (r=0.755
and r=0.679, respectively). There was no correlation
between Qp/Qs and the stretch values in the right andlower directions in the PA view (r=0.417 and r=0.286,
respectively), or in the back direction in the LL view
(r=0.427). No significant between-group diﬀerenceswere observed in the stretch values in the right, front,
and lower directions in the LL view, or the stretch© 2019 Japanese Society of Pediatric Cardiology and Cardiac Surgery

26

Table 2 Results of univariate and multivariate analysis of the number of crochetage patterns
All patients
Correlation coeﬃcients

Age
BSA
RVEF
RVEDVI
Qp/Qs
CI
The stretch values
the right direction (PA)the lower direction (PA)the left direction (PA)the front direction (LL)
the lower direction (LL)
the back direction (LL)rp value−0.186−0.205−0.5370.401
0.646−0.034

0.384
0.335
0.007
0.052
0.001
0.876

0.280
0.517
0.649
0.373
0.434
0.162

0.184
0.010
0.001
0.073
0.034
0.450

ASD patients

Multivariate analysis
βp value

0.432

0.014

0.452

0.010

Correlation coeﬃcientsr

p value−0.242−0.255−0.328
0.021
0.473
0.231

0.367
0.340
0.215
0.940
0.064
0.389

0.221
0.612
0.541
0.277
0.348
0.096

0.410
0.012
0.030
0.299
0.186
0.724

Multivariate analysis
βp value

0.655

0.006

ASD, atrial septal defect; BSA, body surface area; CI, cardiac index; LL, left lateral; PA, posteroranterior; Qp/Qs, pulmonary/systemic blood ﬂow ratio; RVEDVI, right ventricle end diastolic volume index; RVEF, right ventricular ejection fraction

value in the back direction (Fig. 5a, d‒f). The stretch
value in the lower direction in the PA view was higher
in eight ASD patients with the crochetage pattern(5.97±2.02 cm2/m2) than in eight ASD patients without
the crochetage pattern (3.42±0.77 cm2/m2, p=0.017)(Fig. 5b). The stretch value in the left direction in the PA
view was higher in the ASD patients with the crochetage
pattern (2.57±1.37 cm2/m2) than in the control subjects(0.83±0.40 cm2/m2, p<0.001) (Fig. 5c). Table 2 shows
the results of the univariate and multivariate analysesof the eﬀects of the hemodynamic findings and thestretch values according to directions on the number ofcrochetage patterns. On stepwise multivariate analysis,
Qp/Qs and the stretch value in the lower direction in the
PA view were statistically significant independent predictors of the number of crochetage patterns (p=0.01).
In the ASD patients, only the stretch value in the lower
direction in the PA view was a statistically significant
independent predictor of the number of crochetage patterns (p=0.006).

Discussion
This study is the first to investigate the stretch direction of the right ventricle as a finding associated with thecrochetage pattern in ASD patients. The stretch value inthe lower direction in the PA view was higher in ASD
patients with the crochetage pattern than in those without the crochetage pattern. Given that the crochetage
pattern is an R wave notch in the inferior ECG limb
leads, we believe it is reasonable that a significant diﬀerJ Pediatr Cardiol Card Surg Vol. 3, No. 1 (2019)ence is present between ASD patients with and without
the crochetage pattern. It is possible that the stretchedright ventricular muscles are an obstacle to electricalconduction, resulting in a crochetage pattern on the
ECG. Conversely, because the extension in the lower
direction appears strong along with the left direction
when the right ventricle volume overload is large, we
believe that reproduction of the crochetage pattern iseasy.
Previous studies have reported the presence of thecrochetage pattern in patients with right ventricularvolume overload.5) Considering only RVEDVI and
Qp/Qs, the crochetage pattern may easily occur. However, by taking into consideration the stretch directionof the right ventricle, it is understood that the crochetage
pattern does not occur only due to the right ventricle
volume overload. Even if RVEDVI or Qp/Qs is large,
the chrochetage pattern may not occur. In particular,
the crochetage pattern is less likely to occur if the rightventricle is expanded and only stretched in the left
direction. Therefore, ASD patients might not necessarily show the crochetage pattern. On the contrary, acrochetage pattern indicates that the stretch value in thelower direction is significant even if there is minimal
right ventricle volume overload. Therefore, it is feasiblethat patients with patent foramen ovale, pulmonary
stenosis, or normal hearts can also have this pattern.
However, it is still unclear why the stretching of the rightventricle in the lower direction produces this patternin such patients. Thus, future studies investigating the27stretch value of the right ventricular myocardium using
echocardiography or magnetic resonance imaging are
warranted; determining which part is likely to be related
to the crochetage pattern also needs to be investigated.
In addition, the clinical significance of the crochetage
pattern may be determined by the duration of functionalchanges in the right ventricular myocardium.
This study had some limitations. First, the stretch
value was defined by us and is not a well-known value.
Second, our patient sample size was small, and the threegroups had diﬀerent age groups. There are some reportsthat the crochetage pattern is more frequently seen inyounger people.3) Even in this study, the patients withthe crochetage pattern were relatively younger thanthose in the other groups. Perhaps, the myocardiumof a young person is softer than that of adults, and thestretching of the myocardium tends to occur in the lower
direction. Third, since there were cases of CoA and IAA
postoperatively in the control group, it was undeniable
that the abnormality of cardiac function may be aﬀected.
Fourth, none of the ASD patients with the crochetage
pattern had notched R waves in lead II. Fifth, our patient
sample did not have strong RAD. Thus, we think that thestretching of the right ventricular changes in direction
based on the severity of RAD. For these reasons, further
studies are needed.
In the ASD group, the right ventricle was easily
stretched in the left and front directions in the PA and
LL views, respectively, compared to that in the controls.
In cases with large extensions of the right ventricle in thelower direction in the PA view, the crochetage patterndoes occur. The stretch value in the lower direction of
the right ventricle was associated with the crochetage
pattern in ASD patients.
Financial Support
This research did not receive specific grants from any
funding agency, or commercial or non-profit entities.
Conﬂicts of Interest
The authors have no conflicts of interest.

Ethical Approval
All procedures performed in studies involving humanparticipants were in accordance with the ethical standardsof the institutional and/or national research committee andwith the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed Consent
The families of the patients described provided informed
consent for the study of the children.

References
1) Rodriguez-Alvarez A, Martinez De Rodriguez G, Goggans AM, et al: The vectorcardiographic equivalent of the“crochetage” of the QRS of the electrocardiogram in atrial
septal defect of the ostium secundum type. Preliminary
report. Am Heart J 1959; 58: 388‒3942) Heller J, Hagege AA, Besse B, et al: “Crochetage” (notch)
on R wave in inferior limb leads: A new independent
electrocardiographic sign of atrial septal defect. J Am Coll
Cardiol 1996; 27: 877‒8823) Cohen JS, Patton DJ, Giuﬀre RM: The crochetage patternin electrocardiograms of pediatric atrial septal defectpatients. Can J Cardiol 2000; 16: 1241‒1247
4) Somura J, Nakagawa M, Ukiami M, et al: Relationshipbetween electrocardiographic signs and shunt volume inatrial septal defect. Pediatr Inteʼl 2015; 57: 535‒5405) Bayar N, Arslan S, Koklu E, et al: The importance of electrocardiographic findings in the diagnosis of atrial septal
defect. Kardiol Pol 2015; 73: 331‒336
6) Ay H, Buonanno FS, Abraham SA, et al: An electrocardiographic criterion for diagnosis of patent foramen
ovale associated with ischemic stroke. Stroke 1998; 29:1393‒1397
7) Surawicz B, Childers R, Deal BJ, et al: AHA/ACCF/HRS
recommendations for the standardization and interpretation of the electrocardiogram: Part III: Intraventricular
conduction disturbances: A scientific statement from theAmerican Heart Association Electrocardiography andArrhythmias Committee, Council on Clinical Cardiology;
the American College of Cardiology Foundation; and theHeart Rhythm Society: Endorsed by the International
Society for Computerized Electrocardiology. Circulation
2009; 119: e235‒e2408) Awa S, Linde LM, Oshima M, et al: Isolated T-wave inversion in the electrocardiogram of children. Am Heart J
1971; 81: 158‒165
9) Nakazawa M, Marks RA, Isabel-Jones J, et al: Right andleft ventricular volume characteristics in children withpulmonary stenosis and intact ventricular septum. Circulation 1976; 53: 884‒890© 2019 Japanese Society of Pediatric Cardiology and Cardiac Surgery