2013, Wiley Periodicals, Inc.

DOI: 10.1111/echo.12215

Echocardiography

Right Ventricular Abnormalities in Takotsubo

Cardiomyopathy
Ana Clara Rodrigues, M.D., Laise Guimaraes, M.D., Edgar Lira, M.D., Wercules Oliveira, M.D.,
Claudia Monaco, M.D., Adriana Cordovil, M.D., Claudio H. Fischer, M.D., Marcelo Vieira, M.D., and
Samira Morhy, M.D.
Echocardiography Laboratory MDP, Hospital Israelita Albert Einstein, Sao Paulo, Brazil

Background: Takotsubo cardiomyopathy, described as transient regional contractile abnormalities limited to the apical and mid-segments of the left ventricle (LV), has also been reported to involve basal
and/or mid LV segments (inverted Takotsubo); fewer reports, however, have addressed right ventricular
(RV) dysfunction. Aim: To assess the distribution of regional abnormalities and RV involvement in Takotsubo cardiomyopathy and compare it to the literature. Methods and Results: We evaluated 23 patients
with both classical and inverted presentations (19 female, aged 64  19 years), including 2 recurrences, totaling 25 episodes. Classical Takotsubo was observed in 15 patients, while 10 had the inverted
form. LV ejection fraction (EF) was lower for classical compared to inverted presentation (30  7 vs.
45  4%, P < 0.001) with higher troponin values (1.3  1.4 vs. 0.5  0.6, P = 0.034). RV abnormalities were found in 7 patients (28%), mainly with classical presentation (6 patients), presenting with mid
and apical RV impairment. One patient with inverted Takotsubo had mid-RV involvement. Patients with
RV involvement had lower left ventricular ejection fraction (LVEF) (28  10% vs. 40  10%, P = 0.02),
but not when adjusted for presentation type. Overall rate of complications was higher for classical compared to inverted presentation, and not inuenced by RV involvement. Conclusion: RV contractile
abnormalities may follow the same LV regional distribution in Takotsubo cardiomyopathy; the type of
presentation rather than the presence of RV dysfunction seems to be responsible for an increased risk of
complications and severity of functional impairment. (Echocardiography 2013;30:1015-1021)
Key words: Takotsubo, echocardiography, right ventricle
Takotsubo cardiomyopathy (stress-induced
cardiomyopathy) was rst described as transient
regional contractile abnormalities involving the
apical and mid-segments of the left ventricle (LV)
with hypercontractile basal segments, usually
related to triggers such as emotional or physical
stress.1 Classically, the regional abnormalities do
not correspond to any coronary artery territory,
and no signicant coronary artery stenosis is
found. In spite of the amount of myocardium
affected, the prognosis is usually favorable, with
rapid spontaneous recovery. An inverted pattern
of stress-induced transient regional dysfunction
has also been reported, with contractile abnormalities limited to the basal and/or mid segments
of the LV, and a normally contracting apex.24
The association of right ventricular (RV) dysfunction in patients with Takotsubo59 has been
reported, with emphasis on poorer outcome in
this situation.7 However, studies of Takotsubo
Address for correspondence and reprint requests: Ana Clara
Rodrigues, M.D., Echocardiography Laboratory MDP, Hospital Israelita Albert Einstein, Av Albert Einstein, 627 CEP
05652900, Sao Paulo- SP Brazil. Fax: 55 11 21515974;
E-mail: claratude@yahoo.com

cardiomyopathy focusing specically on RV contractile abnormalities are less frequent.6,7 To give

further insights into demographics and clinical
and laboratory features of RV involvement in
Takotsubo cardiomyopathy we assessed a case
series of patients and compared it with ndings
from the available literature.
Methods:
From July 2006 up to August 2011, all patients
who fullled the diagnosis of Takotsubo cardiomyopathy were enrolled in the study. Criteria for
stress-induced cardiomyopathy were the following: (1) acute chest pain/discomfort or dyspnea
with elevation of cardiac enzymes and ECG
changes (ST and T changes) and; (2) transient LV
contractile abnormalities not related to a single
coronary artery; (3) absence of signicant
(>50%) luminal narrowing by coronary arteriography or normal coronary tomography within
2 days of the onset of the symptoms. Patients
were classied into 2 presentations:
Classical Takotsubo: akinesia/hipokinesia of
mid and apical LV segments

1015

Rodrigues, et al.

Inverted Takotsubo: contractile abnormalities limited to the basal and/or mid segments of the LV, and no apical
abnormalities

All patients had echocardiograms undertaken

up to 12 hours after the onset of symptoms. The
examinations were repeated at least once until
LV functional recovery. Left ventricular ejection
fraction was obtained by Simpsons modied rule
or visual estimation. Images were reviewed by 2
experienced echocardiographers to assess RV
involvement; at least 2 echocardiographic planes
with clear visualization of the RV were necessary
for analysis (apical four-chamber and subcostal
plane). The RV was divided into basal, mid
and apical segments. Patients with incomplete
recordings or suboptimal images were excluded
from the study. Clinical characteristics (age, gender, onset of symptoms) and the condition that
preceded onset as a possible triggering factor
were analyzed. Cardiac enzyme release (creatine
kinase MB [CKMB] and troponin T) was checked
for determination of peak values, and a 12-lead
ECG (Page Writer Trim III, Philips Medical
Systems, Andover, MA, USA) was examined for
all patients. All echocardiographic examinations
were reviewed up to normalization of ventricular
function. Clinical (arrhythmias, pulmonary
edema, cardiogenic shock) and echocardiographic (LV thrombus, pericardial effusion) complications, the use of intravenous catecholamine
or assist devices and in-hospital death were
examined by review of medical records.
In addition, we searched PubMed database to
identify original English language articles in peerreviewed journals with the terms Takotsubo,
apical ballooning, stress cardiomyopathy, and
ampulla cardiomyopathy. Search was limited to
humans and adults and to studies including more
than 5 consecutive patients in a case series.
We selected studies that assessed RV contractile
abnormalities in Takotsubo patients, including
data on demographic characteristics, symptoms,
clinical and laboratory presentation, RV characteristics, complications, and outcome. A formal
meta-analysis was not used because of the heterogeneity of the methodology and outcome
assessment among the studies, therefore a
narrative synthesis of the collected data were
undertaken.
Statistical Analysis:
Data are expressed as mean  SD. The differences
in continuous variables comparing cardiac
function in the acute and subacute periods were
tested using paired Student t-test. MannWhitney
test was used to test the differences between the

1016

groups. Categorical measures were compared

with chi-square test or Fishers exact test. A
P-value <0.05 was considered to be statistically
signicant. This investigation was approved by
the Institutional Ethics Committee and met the
regulatory requirements for exemption of an
informed patient consent.
Results:
Out of 33 patients with high suspicion of Takotsubo cardiomyopathy, 9 were excluded
because coronary angiography was not performed, and one did not have adequate echocardiographic recordings of the RV. Eventually,
23 patients fullled the proposed criteria for
Takotsubo; they were predominantly women
(19 patients), aged 64  19 years (ranging
from 18 to 88 years old). Body surface area
was 1.66  0.14 m2. Two of 23 patients
exhibited recurrence, both female, presenting
with inverted followed by classical Takotsubo
presentation (1 and 3 years after the initial episode), totaling 25 episodes of Takotsubo. An
average of 3 echocardiograms were undertaken
for each patient (ranging from 2 to 5), with a
mean interval of 3 days between the rst and
second examination. Predisposing events were
mainly noncardiac surgery (n = 7), including 2
liver and 1 kidney transplantation, followed by
various types of intense emotional stress
(n = 7). Other conditions included infection
(n = 3), bronchial asthma (n = 2), subarachnoid hemorrhage (n = 1), and post delivery
(n = 1). The remaining 4 patients disclosed no
evident stress triggers. Nine patients had coexisting malignancy; both patients with a recurrent episode of Takotsubo had a diagnosis of
malignancy after the second event. Electrocardiographic changes included diffuse T-wave
inversion in 14 patients and ST elevation in 3
patients. Elevated CKMB (>5 ng/mL) was
observed in 15 of the 25 episodes (60%) and elevated troponin T (>0.03 ng/mL) was seen in all
but 1 patient (mean value = 0.94  1.2 ng/mL).
Coronary angiography (Allura Xper FD20,
Philips Healthcare, Bothell, WA, USA) was normal except for 2 patients (40% lesion). Three
patients undertook coronary computed tomography (2 female under 32 years and a 57-yearold male after liver transplantation), with
normal ndings. Regression of wall-motion abnormalities took 12  6 days (ranging from 3 to
43 days), with minor segmental abnormalities
persisting in 3 patients. The LV ejection fraction
improved from 34  13% at baseline to 63  6%
(P < 0.00001). Pulmonary artery systolic pressure
was increased (>35 mmHg) in 14 patients (56%),
and measured 40  9 mmHg. Transient left

RV Abnormalities in Takotsubo Cardiomyopathy

intraventricular pressure gradient was documented in only 1 patient.

Classical Takotsubo presentation, with akinesia of mid and apical segments of the LV, was
observed in 15 patients, while 10 patients had
the inverted form of Takotsubo, including the 2
patients with recurrence: 4 patients had akinesia
of both basal and mid- LV segments; 3 had akinesia of all mid segments; and 3 had akinesia of all
basal segments. At the onset of the disease, LV
ejection fraction was signicantly lower (30  7
vs. 45  4%, P < 0.001) for classical compared
to the inverted Takotsubo presentation, and
these patients also expressed higher troponin values. Pleural effusion was common (56% of the
patients, occasionally existing prior to the onset
of Takotsubo (3 patients), and more frequent in
patients with classical presentation (P = 0.04).
Demographics and cardiac markers of classical

and inverted Takotsubo patients are displayed on

Table I.
Right Ventricular Involvement:
Results from the present series regarding RV
involvement are displayed in Table II. In this
study, most patients with RV dysfunction were
female. RV abnormalities were present in 7
patients, and predominantly associated with classical Takotsubo presentation (6 patients). Apical
and mid-RV akinesia was seen in 5 patients and
akinesia restricted to the RV apex (Fig. 1)
observed in 2 patients. Only 1 patient with the
inverted presentation of Takotsubo had RV
involvement, and likewise, the affected segment
(mid ventricular) was analogous to that observed
for the LV (Fig. 2). A lower left ventricular ejection fraction (LVEF) was found for patients with
RV dysfunction compared to those without it

TABLE I
Characteristics of Classical Compared to Inverted Takotsubo
Presentation
Classical
(n = 15)

Inverted
(n = 10)

63  11
11 (73%)
1.66  0.1

61  5
9 (90%)
1.65  0.1

1.3  1.4

0.5  0.6

Variable
Age (years)
Female (n)
Body surface
area (m2)
Troponin T
(ng/mL)
CKMB (ng/mL)
Left atrium (mm)
PASP (mmHg)
Initial LVEF (%)
Final LVEF (%)
Pleural effusion

5.9
38
43
30
60
11







4.2
4
6
7
3

4.5
34
36
45
64
4







2.9
5
7
4
6

NS
NS
NS
0.03
NS
0.056
NS
<0.001
0.03
0.04

CKMB = creatine kinase MB fraction; LVEF = left ventricular

ejection fraction; PASP = pulmonary artery systolic pressure.

Figure 1. An apical four-chamber view showing extensive

mid and apical left ventricular contractile abnormality (akinesia) in a patient with classical Takotsubo. A small area of ventricular akinesia is demonstrated in the RV apical wall (arrows).
RV = Right ventricle; LV = left ventricle.

TABLE II
Characteristics of RV Involvement in Takotsubo Cardiomyopathy
Variable
Age (years)
Female Gender (n)
Troponin T (ng/mL)
CKMB (ng/mL)
LVEF (%)
PASP (mmHg)
Classical/inverted form
Pleural effusion

No RV Involvement
(n = 18)

RV Involvement
(n = 7)

67  15
15 (83%)
0.8  1.3
4.6  5.2
39  10
41  10
9/9
10 (55%)

58  25
6 (86%)
1.5  1.2
7.2  6.9
28  10
38  10
6/1
4 (57%)

P
NS
NS
NS
NS
0.02
NS
NS
NS

RV = right ventricular; CKMB = creatine kinase MB fraction; LVEF = left ventricular ejection fraction; PASP = pulmonary artery systolic pressure.

1017

Rodrigues, et al.

In our series, RV involvement was not associated to a higher prevalence of cardiovascular complications. During follow-up (13  14 months)
there were 3 deaths (3, 6, and 9 months after the
onset of Takotsubo) due to malignancy (breast
cancer, lymphoma, and lung cancer, respectively). Mortality was not higher for patients with
RV dysfunction.

Figure 2. A modied apical echocardiographic view to focus

on the right chambers, depicting involvement of mid segment of RV free wall (arrows), sparing the apex and basal segment. The LV also showed akinesia of mid ventricular
segments in this patient with inverted Takotsubo (bedside
echocardiography). RV = Right ventricle; LV = left ventricle;
RA = right atrium.

(28  10% vs. 40  10%, P = 0.02). However,

when controlled for the type of presentation
(patients with classical Takotsubo), there was no
signicant difference in LVEF, but a trend for
lower LVEF (P = 0.08) in patients with RV involvement. Cardiac injury markers were similar for
patients with and without RV impairment. A
rapid recovery of RV contractile abnormalities
was the rule (5.7  4.0 days, ranging from 1 to
13 days) and observed in all 7 patients. Regression of wall-motion abnormalities was earlier for
the right than for the LV (P < 0.05).
The literature search identied a total of 11
potentially relevant studies assessing Takotsubo
cardiomyopathy, with 5 meeting eligibility criteria (2 from the United States, 1 from South
Korea, 1 from Germany, and 1 from multiple
countries).59 Evaluation was undertaken either
by echocardiography (2 studies) or magnetic resonance (MR) (3 studies); data from the pooled
studies are shown in Table III.
Clinical Outcome and Complications:
Overall rate of complications was higher
(P < 0.05) for classical (Table IV) as compared to
inverted Takotsubo presentation, and increased
in patients with lower LVEF. One patient had cardiogenic shock requiring intravenous dobutamine infusion and 1 had a resuscitated cardiac
arrest. There was 1 episode of atrial brillation
requiring cardioversion, and 1 pulmonary embolism. An apical LV thrombus was observed in 2
patients and a small pericardial effusion with
spontaneous resolution in 5. Pleural effusion was
comparable for patients with and without RV
contractile abnormalities.
1018

Discussion:
Takotsubo cardiomyopathy has been described
as transient regional contractile abnormalities
involving the apical and mid segments of the LV,
usually related to triggers such as emotional or
physical stress.1 Subsequently, involvement of
myocardial regions other than the apex was
reported, with contractile abnormalities limited
to the basal and/or mid segments of the LV and a
normally contracting apex, suggesting a new
clinical entity.3,4 Reports on RV involvement
associated to Takotsubo are less frequent59 and
mainly described in patients with classical
Takotsubo variant. In our series, RV regional
dysfunction was found in 7 patients (28%,
considering 25 episodes), a nding comparable
to the reported prevalence of RV abnormalities
(ranging from 21 to 34%).59 Accordingly, most
patients with RV abnormalities were female; on
the other hand, compared to studies that
reported on patients age,59 patients with RV
involvement in our series were younger; of note,
mean age in our series was also lower
(64  19 years old).
Interestingly, stress-induced regional dysfunction involving the RV may follow the same pattern of contractile dysfunction found in the LV: in
6 patients with classical Takotsubo there was RV
apical involvement (isolated or in association
with mid-RV segment), whereas in 1 patient with
inverted Takotsubo (and contractile abnormalities involving the mid segments of the LV) the
corresponding mid-RV segment was affected. RV
apical involvement in patients with classical
Takotsubo has been characterized in previous
reports.7,10 Accordingly, in the 3 studies reporting the distribution of LV wall-motion abnormalities,57 RV dysfunction was associated with
classical Takotsubo (apical ballooning) in 2
reports, with only one study describing the association with inverted (mid-ventricular variant)
presentation.5 Elesber,7 in patients with classical
Takotsubo, also found a similar pattern of wallmotion abnormalities for both the left and RV.
Detailed distribution of RV wall-motion abnormalities was reported in only 1 of the 5 selected
studies,6 but correspondence with LV abnormalities was not described.
Of interest, regression of RV dysfunction was
rapid, and complete normalization of contractile

RV Abnormalities in Takotsubo Cardiomyopathy

TABLE III
Characteristics of Studies Reporting on RV Involvement in Takotsubo Cardiomyopathy
Studies
Examination
n
RV dysfunction (%)
Age (years)
Female Gender (n)
Classical/inverted form
Initial LVEF (%)
Final LVEF (%)
Troponin T (ng/ml)
Pleural effusion (n/%)
CHF (n/%)
Thrombus (n)
LVOT (n)
Death (n)

Sharkey et al.5
MR/TTE/CT
136 (95 with MR)
23(24%)

18/5
26  8

Hagui et al.6

Elesber et al.7

Lee et al.8

Eitel et al.10

Present Series

MR
34
9 (26%)
70  8
8 (89%)
9/0
40  6

TTE
25
8 (32%)
70  13
8 (100%)
8/0
29  9
58  9

TTE
56
12 (21%)

MR
239
81 (34%)
73  12

TTE
25
7 (28%)
58  25
6 (86%)
6/1
28  10
65  7
1.5  1.2
4 (57%)
4 (57%)
0
1
2

9.7  11.2
6 (67%)

43.1  8.5

62%
6 (75%)
0
0
2

RV = right ventricular; MR = magnetic resonance; TTE = transthoracic echocardiography; CT = computed tomography;

LVEF = left ventricular ejection fraction; CHF = congestive heart failure; LVOT = left ventricular outow tract obstruction.
TABLE IV
Complications of Takotsubo Cardiomyopathy

Pericardial effusion
Thrombus
Shock/sudden death
Atrial brillation
PE
CHF
Death
Total

Classical
(n = 15)

Inverted
(n = 10)

RV Involvement
(n = 7)

3
2
2
1
1
8
2
19

2
0
0
0
0
2
1
5

0
0
2
1
0
4
2
9

RV = Right ventricular; CHF = congestive heart failure; PE = pulmonary embolism.

abnormalities observed in all 7 patients; in the

particular patient with inverted pattern of
Takotsubo and RV mid-wall akinesia, a repeat
echocardiogram undertaken after 24 hours no
longer showed RV contractile abnormalities.
Accordingly, it is likely that early RV involvement
may be missed in some patients either because a
RV angiography is not regularly undertaken, or
echocardiography is performed later, when RV
abnormalities have resolved. In previous studies,
there was either incomplete7 or no adequate
follow-up for RV performance.5,6,8
In our series, LVEF was lower in patients with
RV involvement, but contrary to other reports,
when controlled for presentation type, there was
no signicant difference regarding this variable.
Data on initial LVEF were reported in 4 studies,59
with considerable variability among them (measurements ranging from 26 to 43%) and higher
values mainly observed for MR measured EF.6,9 In
these reports, RV dysfunction was associated with

a lower LVEF; however, the effect of presentation

type on LVEF was not taken into account, and a
multivariate analysis undertaken in only one
study.7 Of note, cardiac injury markers were similar for patients with and without RV impairment
in our series. These data were reported in only
one study6 and likewise, no difference was seen
for patients with RV abnormalities. Indeed, it is
possible that patients with extensive LV myocardial involvement, as in classical Takotsubo, will
most likely have associated RV involvement.
In spite of the amount of myocardium
affected, the long-term prognosis is generally
favorable in Takotsubo cardiomyopathy, with
spontaneous functional recovery. In our series
there were 2 in-hospital noncardiac deaths, both
associated with malignancy, and one later death;
complications, however, were fairly common,
with 2 patients experiencing serious complications (cardiac arrest and a cardiogenic shock). In
addition, 2 patients with apical akinesia had LV
1019

Rodrigues, et al.

thrombus, and 1 patient had a pulmonary embolism. Dyskinetic/akinetic left or RV segments can
facilitate intracavitary thrombus formation, and
are a potential risk for thromboembolic complications.
Predictably, complications were more common for classical Takotsubo presentation, probably resulting from more severe initial LV
dysfunction. A higher prevalence of complications for patients with RV involvement as
reported in one study7 was not observed in the
present series, suggesting again that complications may be associated to a lower LVEF and
indeed be related to the larger amount of LV
myocardium involved. Contrary to other
reports,6,9 we did not observe a higher prevalence of pleural effusion in patients with RV
impairment6; in fact, 3 patients showed pleural
effusion on chest tomography before the onset
of Takotsubo. In agreement with a previous
report,7 mortality was not higher for patients
with RV dysfunction in this study.
Pathophysiology of Takotsubo has not been
clearly established, but an exaggerated sympathetic stimulation with catecholamine cardiotoxicity1 is a key theory among several others
proposed. This theory holds true for most cases
of Takotsubo, including those with RV involvement, as regional differences in adrenergic sensitivity or innervation11 could explain distinct
clinical presentations and regional dysfunction,
both for the left and the right ventricle. Interestingly, the 2 patients with recurrent episodes of
Takotsubo had different forms of the disease: one
had classical Takotsubo followed by inverted
form with associated RV involvement and the
other started with an inverted form followed by
classical presentation of Takotsubo. This does not
agree with the theory of contractile abnormalities
resulting exclusively from a different distribution
of the sympathetic nerves, unless individual sensitivity or density of receptors changes from 1
episode to the other. It actually implies a functional, not structural, response from adrenergic
receptors, with the distribution (or density) of
adrenergic receptors in the myocardium a potentially dynamic process. Varying LV wall-motion
abnormalities in the same patient with Takotsubo
have also been described.12 Other proposed
mechanisms (thrombosis of a left anterior
descending artery that wraps around the apex
with rapid resolution by endogenous brinolysis13 and transient obstruction of LV outow tract
in response to stress14) have been described as
potentially implicated in the pathogenesis of
Takotsubo. Only 1 patient in our series had an
intra-ventricular gradient; additionally, neither
theory explains fully the presence of RV
apical involvement or apical-sparing contractile
1020

abnormalities. Takotsubo is most likely a heterogeneous disorder, with multiple causes playing a
role in its pathogenesis; it has gained attention
during the past few years, however, alternative
presentations are possibly under recognized.
Careful evaluation of the RV should bring more
attention to regional abnormalities in this chamber; however, as recovery may rapidly occur, earlier examinations are crucial to observe RV
contractile abnormalities.
Limitations:
A major limitation is the small number of
patients, resulting from the fact that Takotsubo is
an uncommon disease. Moreover, due to complex geometry, assessment of the RV using echocardiography is limited, and mainly qualitative or
semiquantitative7; however, for serial cardiac
evaluation it is more suitable than other examinations; tissue Doppler velocities and tricuspid
annular plane systolic excursion (TAPSE) have
been used for RV evaluation; however, RV
involvement was restricted to RV apical or mid
segments, with hypercontractile basal segments,
limiting the use of these techniques in this
population.
Conclusion:
RV involvement is relatively common in Takotsubo
cardiomyopathy and may follow the same distribution of LV regional abnormality. At present, it
remains unclear if RV involvement can be denitely associated to a higher rate of complications.
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