QJM: An International Journal of Medicine, 2019, 861–867

doi: 10.1093/qjmed/hcz186
Advance Access Publication Date: 25 July 2019
Original paper

ORIGINAL PAPER

Prevalence and cumulative incidence of cancer,

and mortality in patients with Takotsubo
syndrome with focus on the index event
P. Tornvall, O. Collste and H. Pettersson
From the Department of Clinic Science and Education, Karolinska Institutet, Södersjukhuset, Sjukhusbacken
10, 118 83 Stockholm, Sweden
Address correspondence to P. Tornvall, Department of Clinic Science and Education, Karolinska Institutet, Södersjukhuset, Sjukhusbacken 10, 118 83
Stockholm, Sweden. email: per.tornvall@ki.se

Summary
Background: It has been suggested that Takotsubo syndrome (TS) is associated with cancer but previous studies have
limitations.
Aim: To make a comprehensive analysis of prevalence and cumulative incidence of cancer, and mortality among TS
patients with focus on the index event.
Design: A register-based case–control study.
Methods: The first new cancer occurrences (International Classification of Diseases C00–C75, C81–C96) were compared be-
tween 505 patients with TS without obstructive coronary artery disease (CAD) and four age- and gender-matched controls
comprising patients with acute coronary syndrome with obstructive CAD (CAD controls), respectively, with chest-pain with-
out obstructive CAD at coronary angiography (controls without CAD).
Results: The prevalence of cancer before the index event was non-significantly (P ¼ 0.052) higher in TS patients (15.8%) than
in CAD controls (11.5%), respectively, higher (P ¼ 0.028) than in controls without CAD (11.1%). There were no differences be-
tween the groups in cumulative incidence of cancer after the index event but a higher mortality in TS patients who devel-
oped cancer when compared with controls without CAD that developed cancer after the index event (P ¼ 0.018).
Conclusions: There is an increased prevalence of first diagnosed cancer in TS patients before the index event but no
increased cumulative incidence of cancer after the index event. The results does not support investigation for the possibility
of a malignancy specifically in TS patients but in the event of cancer this patient group might need special care. However, if
there is lack of a clear stressor it could be of importance to investigate the possibility of a malignancy.

Introduction surgical procedures.1 Several studies have shown an association be-

It has been suggested that Takotsubo syndrome (TS) should be div- tween TS and cancer, both before and after the index event.2–6
ided into primary and secondary forms where the secondary form All studies have been relatively small regarding the number of
is caused by severe underlying disease such as cancer and sepsis or included TS patients (50–286 patients) and have been performed as

Received: 15 June 2019; Revised (in revised form): 3 July 2019

C The Author(s) 2019. Published by Oxford University Press on behalf of the Association of Physicians.
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 862 | QJM: An International Journal of Medicine, 2019, Vol. 112, No. 11

single-center studies, thus not population-based. Only two studies2,6 Statistics

have had age- and sex-matched controls comprising patients with
Data before and after the index event were studied separately.
a previous myocardial infarction (MI) that is a group of patients with
Data are presented as mean 6 standard deviation and percentage
an increased risk of cancer compared with the population.7
(number). Characteristics and cardiovascular risk factor were
The association between TS and cancer has been discussed
compared pair-wise between TS patients and CAD controls, re-
since the initial observation by Burgdorf et al. in 20082 who in a
spectively, controls without CAD by independent Student’s t-test
single-center study retrospectively investigated 50 TS patients
for mean or Fishers exact test for percentage. Cancer diagnoses
together with 50 age- and sex-matched patients with an MI.
were determined by ICD C00–C75 and C81–C96 divided into solid
In this pivotal study, 18% of the TS patients and 6% of the MI
malignancies (C00–75) excluding breast cancer (C50) and blood
patients had a previous history of cancer. After 3 years of
malignancies (C81–96). To study the occurrence of a first new
follow-up an additional 14% of the TS patients were diagnosed
cancer and survival between the groups, we used the Kaplan–
with cancer compared to none of the MI patients. Recently,
Meier method with the corresponding log-rank test. We defined
Sattler et al.6 presented a single-center study of similar design
time (Figure 1) from index event to first new cancer (event), death,
comprising 138 TS patients with 138 age- and sex-matched MI
or 31 December 2013, whichever occurred first. Time (Figure 2)
controls. Twelve percent of the TS patients and 6% of the MI
from index event in patients with first new cancer before the
patients had a previous history of cancer. During a follow-up of
index event to death (event) or 31 December. Or time (Figure 3)
more than 4 years an additional 9% of the TS patients were diag-
from first new cancer after the index event to death (event), or 31
nosed with cancer compared with only 2% of the MI controls.
December. In addition, we used cox regression to adjust for fac-
The results of these studies suggest that TS is a para-malignant
tors that differed between the groups at the index event (Tables 1
phenomenon and that TS patients should be screened for can-
and 2) to study the occurrence of first new cancer and mortality
cer. However, the association between TS and cancer is complex
after the index event (Figures 1 and 2). Analysis was done with
since the mechanisms might be different in cancers detected
the use of SPSS version 25 (IBM, Armonk, NY, USA). The results
before and after the index event. For example, in cancer known
were considered significant if P <0.05, two sided.
at the index event TS might be caused by a para-malignant phe-
nomenon, by the treatment for cancer8 or by the stress of hav-
ing cancer. After the index event an increased incidence could Results
be observed merely due to investigations instigated by TS or by
Characteristics and cardiovascular risk factors for TS patients
a true association between TS and cancer where TS could be
and their respective controls, ‘including cancer patients’, have
considered a para-malignant phenomenon.
been described.10 In Table 1, characteristics and cardiovascular
In 2016, we presented a population-based register study com-
risk factors for TS patients and their respective controls,
prising 505 TS patients with age- and sex-matched controls,
‘excluding patients with cancer before the index event’, are
including not only MI but also healthy controls, with focus on risk
described. Consistent with the original publication, TS patients
markers and prognosis. In this study, in contrast to another regis-
and controls were typically women with a mean age of
ter study,9 we could not observe any overall difference in preva-
67 years.9 As described, TS patients had less frequently treated
lence of life-time number of cancers or relative risk of death due
hypertension and hyperlipidemia whereas smoking habits were
to cancer between the groups.10 The aim of the present study,
intermediate when compared with both control groups.
using the same material, was to focus on first time cancer before
Furthermore, a diagnosis of diabetes mellitus was less common
and in particular after the index event to find support for TS as a
in TS patients than in CAD controls.8 TS patients had more
para-malignant phenomenon in need for cancer screening.
often a diagnosis of chronic obstructive pulmonary disease
Furthermore, we wished to test the hypothesis that patients with
(COPD) than the two control groups also consistent with our ori-
both TS and cancer had a poor prognosis proposed by Sattler et al.6
ginal study.8 Further analyses are divided according to if the
first new cancer occurred before or after the index event.

Materials and methods Prevalence of cancer before the index event

Patients and controls In total, 308 first new cancers occurred before the index event,
divided into 80 (15.8%) in TS patients, 116 (11.5%) in CAD con-
In total, 505 patients with TS without obstructive coronary ar- trols and 112 (11.1%) in controls without CAD. The different
tery disease (CAD) 2009–2013 were identified from the Swedish forms of cancer are shown in Table 2 and Supplementary Table.
Coronary Angiography and Angioplasty Registry (SCAAR) to- The prevalence of cancer was borderline increased in TS
gether with four age- and sex-matched controls comprising patients when compared with CAD controls (P ¼ 0.052) and sig-
patients with an acute coronary syndrome with obstructive nificantly increased when compared with controls without CAD
CAD (CAD controls; n ¼ 1010), respectively, with chest-pain (P ¼ 0.028). When characteristics and cardiovascular risk factors
without obstructive CAD at coronary angiography (controls were compared between patients with cancer before the index
without CAD; n ¼ 1007). Data from SCAAR were merged with the event, TS patients had a lower prevalence of treated hyperten-
national patient register including International Classification sion and hyperlipidemia than both control groups.
of Diseases-10 (ICD-10) codes from in- and out-patient hospital Furthermore, the prevalence of present smoking and COPD was
care. The methodology has been presented in detail.10 Cancer increased 5-fold in TS patients when compared with controls
diagnoses were determined by ICD C00–C75 and C81–C96. without CAD (Table 2).
Contrary to the original publication10 where each patients could
contribute with more than one cancer diagnosis, each patient
contributed only with their first new cancer diagnosis in this
Cumulative incidence of cancer after the index event
study. Follow-up was ascertained, up to a maximum of 5 years, In total, 221 first new cancers occurred after the index event,
through the national patient register. divided into 25 (5.9%) in TS patients, 106 (11.8%) in CAD
 P. Tornvall et al. | 863

Figure 1. Survival curves of a first new cancer ‘after the index event’ in TS patients and controls with and w/o CAD. CAD: coronary artery disease; w/o: without;
TS: Takotsubo syndrome.

Figure 2. Survival curves of mortality ‘after the index event’ in TS patients and controls with and w/o CAD and first new cancer ‘before the index event’. CAD: coronary
artery disease; w/o: without; TS: Takotsubo syndrome.
 864 | QJM: An International Journal of Medicine, 2019, Vol. 112, No. 11

Figure 3. Survival curves of mortality ‘after the index event’ in TS patients and controls with and w/o CAD and a first new cancer ‘after the index event’. CAD: coronary
artery disease; w/o: without; TS: Takotsubo syndrome.

Table 1. Characteristics and cardiovascular risk factors in percentage (numbers) or mean 6 standard deviation in patients without cancer
before the index event

TS patients I CAD controls II Controls w/o CAD III P-value P-value

(N ¼ 425) (N ¼ 894) (N ¼ 895) I vs. II I vs. III

Female gender 88.0 (374) 87.7 (784) 86.9 (778) 0.93 0.66
Age 67 6 11 67 6 10 67 6 10 0.74 0.47
Never smoker 53.6 (228) 43.5 (389) 59.4 (532) <0.01 <0.01
Former smoker 25.9 (110) 23.9 (214) 28.9 (259)
Present smoker 13.6 (58) 27.3 (244) 8.4 (75)
Missing data 6.8 (29) 5.3 (47) 3.2 (29)
Treated hypertension 46.1 (196) 52.9 (473) 52.6 (67) 0.04 0.03
Missing data 2.8 (12) 1.7 (15) 1.5 (13)
Treated hyperlipidemia 26.1 (111) 40.0 (358) 43.0 (385) <0.01 <0.01
Missing data 3.8 (16) 3.0 (27) 1.3 (12)
Diabetes mellitus type 1 1.2 (5) 6.3 (56) 2.3 (21) <0.01 0.20
Diabetes mellitus type 2 5.9 (25) 13.0 (116) 6.7 (60) <0.01 0.63
Myocardial infarction 6.4 (27) 14.7 (131) 0.9 (8) <0.01 <0.01
Heart failure 3.8 (16) 5.1 (46) 5.5 (49) 0.33 0.22
Atrial fibrillation 5.2 (22) 6.5 (58) 11.6 (104) 0.39 <0.01
Stroke/TIA 5.0 (4) 7.8 (9) 7.1 (8) 0.40 0.24
Asthma 4.9 (21) 3.8 (34) 6.3 (56) 0.38 0.38
COPD 8.7 (37) 3.6 (32) 3.8 (34) <0.01 <0.01

CAD: coronary artery disease; COPD: chronic obstructive pulmonary disease; TIA: transitory ischemic attack; TS: Takotsubo syndrome. Bold numbers denote significant
differences between groups.
 P. Tornvall et al. | 865

Table 2. Characteristics, cardiovascular risk factors and type of malignancy in percentage (numbers) or mean 6 standard deviation in patients
with first new cancer before the index event

TS patients I (N ¼ 80) CAD controls II (N ¼ 116) Controls w/o CAD III (N ¼ 112) P-value P-value
I vs. II I vs. III

Female gender 85.0 (68) 86.2 (100) 92.0 (103) 0.84 0.16
Age 68 6 9 71 6 9 72 6 8 0.12 <0.01
Never smoker 38.8 (31) 45.7 (53) 68.8 (77) 0.80 <0.01
Former smoker 35.0 (28) 31.0 (36) 25.0 (28)
Present smoker 18.8 (15) 15.5 (18) 3.6 (4)
Missing data 7.5 (6) 7.8 (9) 2.7 (3)
Treated hypertension 45.3 (33) 54.2 (74) 53.4 (67) <0.01 <0.01
Missing data 5.0 (4) 0.9 (1) 0 (0)
Treated hyperlipidemia 26.3 (21) 46.6 (54) 48.2 (54) 0.01 <0.01
Missing data 5.0 (4) 3.4 (4) 0.9 (1)
Diabetes mellitus type 1 0 (0) 4.3 (5) 3.6 (4) 0.08 0.14
Diabetes mellitus type 2 3.8 (3) 19.8 (23) 8.9 (10) <0.01 0.24
Myocardial infarction 7.5 (6) 22.4 (26) 0 (0) <0.01 <0.01
Heart failure 5.0 (4) 11.2 (13) 6.3 (7) 0.20 0.76
Atrial fibrillation 10.0 (8) 6.9 (8) 13.4 (15) 0.44 0.51
Stroke/TIA 5.0 (4) 7.8 (9) 7.1 (8) 0.56 0.76
Asthma 12.5 (10) 6.0 (7) 8.0 (9) 0.13 0.33
COPD 17.5 (14) 12.1 (14) 3.6 (4) 0.30 <0.01
Solid malignancies 71.3 (57) 61.2 (71) 68.8 (77) 0.34 0.92
Blood malignancies 3.8 (3) 6.0 (7) 3.6 (4)
Breast cancer 25.0 (20) 32.8 (38) 27.7 (31)

CAD: coronary artery disease; COPD: chronic obstructive pulmonary disease; TIA: transitory ischemic attack; TS: Takotsubo syndrome. Bold numbers denote significant
differences between groups.

Table 3. Characteristics, cardiovascular risk factors and type of malignancy in percentage (numbers) or mean 6 standard deviation in patients
with first new cancer after the index event

TS patients I (N ¼ 25) CAD controls II (N ¼ 106) Controls w/o CAD III (N ¼ 90) P-value P-value
I vs. II I vs. III

Female gender 85.0 (68) 86.2 (100) 92.0 (103) 0.99 0.99
Age 71 6 8 71 6 8 70 6 9 0.69 0.59
Never smoker 52 (13) 52.8 (56) 62.2 (56) 0.48 0.63
Former smoker 28.0 (7) 19.8 (21) 25.6 (23)
Present smoker 12.0 (3) 22.6 (24) 6.7 (6)
Missing data 8.0 (2) 4.7 (5) 5.6 (5)
Treated hypertension 60.0 (15) 57.5 (61) 45.6 (41) 0.85 0.39
Missing data 4.0 (1) 2.8 (3) 4.4 (4)
Treated hyperlipidemia 26.1 (7) 40.8 (43) 43.6 (29) 0.51 0.28
Missing data 4.0 (1) 3.8 (4) 0 (0)
Diabetes mellitus type 1 0 (0) 6.6 (7) 2.2 (2) 0.34 0.99
Diabetes mellitus type 2 8.0 (2) 12.3 (13) 3.3 (3) 0.73 0.30
Myocardial infarction 4.0 (1) 14.2 (15) 0 (0) 0.30 0.22
Heart failure 4.0 (1) 2.8 (3) 2.2 (2) 0.58 0.52
Atrial fibrillation 8.0 (2) 3.8 (4) 13.3 (12) 0.33 0.73
Stroke/TIA 12.0 (3) 6.6 (7) 6.7 (6) 0.40 0.41
Asthma 4.0 (1) 3.8 (4) 6.7 (6) 0.99 0.99
COPD 12.0 (3) 3.8 (4) 3.3 (3) 0.13 0.12
Solid malignancies 88.0 (22) 81.1 (86) 85.6 (77) 0.80 0.41
Blood malignancies 0.0 (0) 3.8 (4) 6.7 (6)
Breast cancer 12.0 (3) 15.1 (16) 7.8 (7)

CAD: coronary artery disease; COPD: chronic obstructive pulmonary disease; TIA: transitory ischemic attack; TS: Takotsubo syndrome.

controls and 90 (10.0%) in controls without CAD. The different results were adjusted for factors that differed between the
forms of cancer are shown in Table 3 and Supplementary groups at the index event (Table 1). There were no major dif-
Table. There were neither differences in cumulative incidence ferences between the groups in characteristics and cardiovas-
of cancer between the groups when the difference in expos- cular risk factors in patients with cancer after the index event
ure time was taken into account (Figure 1), nor when the (Table 3).
 866 | QJM: An International Journal of Medicine, 2019, Vol. 112, No. 11

Mortality after the index event in MI controls rather than an increased incidence in TS patients.
Taking study design and size of the study into account there is
There were no differences in cumulative incidence of mortal-
weak support for TS being a para-malignant phenomenon with
ity after the index event between the three groups with a first
an increased incidence of cancer after a TS event. Thus, no rec-
new cancer ‘before the index event’ (Figure 2), neither in un-
ommendation can be made regarding cancer screening in TS
adjusted nor in analyses adjusted for differences between the
patients. However, in our study we had no information about
groups at the index event (Table 2). The mortality was border-
the amount of patients that not could be classified as primary
line increased in TS patients when compared with
or secondary forms of TS and it can therefore be suggested that
CAD controls (P ¼ 0.072) and significantly increased when
if there is lack of a clear stressor it could be of importance to in-
compared with controls without CAD (P ¼ 0.018) in patients
vestigate the possibility of a malignancy.
that developed a first new cancer ‘after the index event’
Without surprise, several studies have suggested that cancer
(Figure 3).
increase mortality in TS patients. Girardey et al.5 and Kim et al.11
showed that cancer was a negative prognostic factor in patients
hospitalized for TS whereas Möller et al.3 and Sattler et al.4 came to
Discussion a similar conclusion but included TS patients both ‘before and
The results of this population-based register study comprising after the index event’. The finding that TS patients with a previous
505 TS patients with two age- and sex-matched controls history of cancer or with active cancer have a worse prognosis
showed that a first new cancer diagnosis was more common than TS patients without cancer was reinforced by a recent meta-
‘before the index event’ in TS patients than in controls without analysis by Brunetti et al.12 who showed more clinical events both
CAD but there were no differences if the first new cancer in-hospital and during follow-up in TS patients. These studies em-
occurred ‘after the index event’. Intriguingly, the mortality was phasize the need for special care, including intensive care from
increased in TS patients with a first new cancer that occurred both cardiologists and oncologists, for patients with TS and can-
‘after the index event’ but not before when compared with the cer. Recently, Sattler et al.6 proposed that TS patients with cancer
two control groups. have a worse prognosis compared to MI patients with cancer.
The results of the present population-based study of TS Unfortunately, they included cancer patients both ‘before and
patients without obstructive CAD confirmed the results of the after the index event’ making data difficult to interpret. However,
single-center studies by Burgdorf et al.2 and Sattler et al.6 regard- in the present study we could confirm that TS patients who devel-
ing an increased prevalence of cancer ‘before the index event’ oped cancer ‘after the index event’ had a worse prognosis than
when compared with age- and sex-matched patients with MI. controls that developed cancer with and without CAD. This infor-
Of note is that the differences were statistically non-significant, mation should be interpreted cautiously since the reason is un-
including altogether 26 cancer cases in the TS groups compared clear and the number of patients few. Therefore, more and larger
with 11 in the MI control groups in these studies. Our results are studies are needed to confirm a worse prognosis in TS patients
reinforced by the register study by El-Sayed et al.9 where they in with cancer compared with other groups of patients with cancer.
comparison with MI and orthopedic controls showed an
increased prevalence of cancer in TS patients. However, con- Strength and limitations
trols in their study were only matched for age, thus not taking
into account differences in malignancies between men and The major strength of the present investigation is that it is
women. The reason for the association between TS and cancer population-based compared to previous single-center studies
is not clear but could be due to the malignancy itself, the stress and that it included both CAD and healthy controls.
of having cancer or drugs known to cause TS. The results thus Furthermore, the number of cancer cases was comparably high
support the statement that TS should be divided into primary compared to previous controlled studies.2,6 A weakness is the
and secondary forms where the secondary form is caused by an retrospective design with TS cases identified by the individual
underlying severe disease.1 angiographer in SCAAR. Also, the case–control design with pa-
We could not confirm an increased cumulative incidence of tient characteristics and cardiovascular risk factor data at the
cancer ‘after the index event’ seen in the studies by Burgdorf time of the index event, rather than at the time of first new can-
et al.2 and Sattler et al.6 when compared with age- and sex- cer diagnosis, made it not relevant to perform multivariable
matched patients with MI. Although the differences were statis- analysis to adjust for factors that differed between the groups
tically significant, the numbers were small including altogether when the first new cancer occurred or of the prevalence of can-
20 cancer cases in the TS groups compared with 3 in the MI con- cer at the index event. Furthermore, as controls, patients with
trol groups. The reason for this spurious discrepancy is not clear an acute coronary syndrome with obstructive coronary arteries
but could be due to a statistical type 1 error in the studies by but without a confirmed MI were included, thus comprising
Burgdorf et al.2 and Sattler et al.6 since we included 221 cancer both MI and unstable angina pectoris. Finally, there is no infor-
patients in total (25 in TS patients). A further strength to the mation regarding cancer treatments that might have influenced
present study is that we included two control groups. The in particular mortality after the index event.
choice of control groups is also relevant since there has been a
report about an association between cancer and a recent MI
from a Norwegian population-based study.7 The incidence of
Conclusion
cancer was 22.6 cases per 1000 patient-years in MI patients There is an increased prevalence of first diagnosed cancer in TS
compared to 7.3 cases per 1000 patient-years in controls with- patients before the index event but no increased cumulative in-
out MI. Extrapolating from these figures, the expected total cidence of cancer after the index event. Intriguingly, the mortal-
number of cancer in the MI controls in the studies by Burgdorf ity was increased in TS patients who developed cancer after the
et al.2 and Sattler et al.6 would have been 20 that is the number index event. The results does not support investigation for
of TS patients who had cancer in these patients thus indicating the possibility of a malignancy specifically in TS patients but in
that the differences seen were caused by a decreased incidence the event of cancer this patient group might need special
 P. Tornvall et al. | 867

care. However, if there is lack of a clear stressor it could be of 4. Sattler K, El-Battrawy I, Lang S, Zhou X, Schramm K, Tülümen
importance to investigate the possibility of a malignancy. E, et al. Prevalence of cancer in Takotsubo cardiomyopathy:
short and long-term outcome. Int J Cardiol 2017; 238:159–65.
5. Girardey M, Jesel L, Campia U, Messas N, Hess S, Imperiale A,
et al. Impact of malignancies in the early and late time course
Supplementary material
of Takotsubo cardiomyopathy. Circ J 2016; 80:2192–8.
Supplementary material is available at QJMED online. 6. Sattler K, El-Battrawy I, Gietzen T, Lang S, Zhou X, Borggrefe
M, et al. Long term outcome of patients suffering from cancer
and Takotsubo syndrome or myocardial infarction. QJM 2018;
Funding 111:473–81.
7. Rinde LB, Småbrekke B, Hald EM, Brodin EE, Njølstad I,
The present study was supported by the Swedish Heart and Mathiesen EB, et al. Myocardial infarction and future risk of
Lung Foundation with grant number 20150612. cancer in the general population-the Tromsø Study. Eur J
Epidemiol 2017; 32:193–201.
Conflict of interest: None declared.
8. Desai R, Abbas SA, Goyal H, Durairaj A, Fong HK, Hung O, et al.
Frequency of Takotsubo cardiomyopathy in adult patients
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