Methods

All cases of Pheo-TS from 1990, the year where the Japanese term takotsubo was introduced, to November 2015 are critically reviewed. The cases were retrieved by searching in the PubMed using the search terms “takotsubo,” “apical ballooning,” “stress cardiomyopathy,” and “broken heart syndrome” and linking them with the terms “pheochromocytoma,” “paraganglioma,” and “catecholamines.” For the reasons mentioned in the discussion, cases with pheochromocytoma-induced transient left ventricular dysfunction where the clinical features and course were consistent with TS are also included. Eighty-one cases were retrieved but because of the extreme similarities between 2 reported cases, 1 case that was reported later was excluded. Eighty case reports constitute the patient material of this report. Nine of the cases deemed to be Pheo-TS were reported before the TS-era, with the TS-era is meant the cases reported after 1999 where the first reports on TS were published in English language. Seventy-one cases were reported during TS-era. One case from 1987 with features typical of mid-apical TS was also included. The reports included were published in English language, 1 case in Swedish and 1 in German, where sufficient information could be obtained. In 7 cases, sufficient information could be acquired from only the abstract. The following information was abstracted from the publications: the year of publications, age and gender of the patients, the clinical presentation, the type of electrocardiographic (ECG) changes, and the cardiac biomarkers. The TS localization patterns were deemed by the description in the text or the available figures in the reports. The hemodynamic complication rates after the presentation, the inhospital mortality, the clinical course of the disease, and the recovery and the recurrence rates available were reviewed ( Table 1 ). The results in this study were compared with the 1,750 patients in a recently published study by Templin et al, where all types of TS were included ( Table 2 ) when comparable information were available in both studies. Continuous variables are presented as means ± SDs and categorical data as absolute values and percentages. Fisher’s exact test or chi-square test was used as appropriate to compare categorical data, and 2-tailed unpaired student’s t test was used for continuous variables; a p <0.05 was considered significant.

Table 1

Clinical features on admission, in-hospital complications and outcome in the 80 patients with pheochromocytoma-triggered TS

Authors	Year	Age	Gender	Presenting symptoms	ECG changes	Complications	TS localization	Recur-rence	Other important descriptions and findings
1-Shaw TR	1987	41	M	Abdominal pain after an assault	STEMI	C-Sh	Mid-apical	0	Before TS-era, TS not mentioned, Transient shock and myocardial impairment
2- Murai K	1991	42	M	Headache, chest pain, palpitation,	ST-depression	C-Sh	Basal or mid-basal	0	Before TS-era: pheochromocytoma with ECG mimicking angina pectoris
3- Salathe M	1992	42	M	Cough, tachycardia and hypertension	STEMI	P-Ed	Global	0	Before TS-era, Pheochromocytoma and catecholamine induced cardiomyopathy
4- Quezado ZN	1992	46	F	Dyspnea, tachypnea,	ST-depression	P-Ed	Global	0	Before TS-era, described as reversible myocardial depression
5- Elian D	1993	41	M	Left flank pain, headache, palpitation and facial flushing	T-wave inversion	P-Ed	Mid-apical	0	Before TS-era, described as reversible catecholamine-induced cardiomyopathy
6- Nanda AS	1995	18	F	Agitated with blood pressure elevation, tachycardia and cyanosis	S tachyc, T-wave changes	P-Ed	Mid-apical	0	Before TS-era, pheochromocytoma-induced catecholamine cardiomyopathy
7- Suga K	1996	70	F	Cough and low-grade fever, dyspnea and palpitation.	S tachyc.	P-Ed	Global	+( two times)	Before TS era, described as pheochromocytoma with cardiomyopathy and pulmonary edema
8- Gatzoulis KA (abstract)	1998	45	M	Chest pain in the setting of hypertensive crisis	Acute ischemia	P-Ed	Global	N/A	Before TS-era, described as reversible cardiomyopathy
9- Brilakis ES	1999	43	F	Chest pain, dyspnea, diaphoresis, nausea and vomiting	STEMI	P-Ed, C-Sh and C-A	Global	0	Before TS-era: reversible catecholamine-induced cardiomyopathy
10- Dinckal MH (abstract)	2003	44	F	Chest pain, headache and nausea	T-wave inversion	N/A	Mid-apical	0	Pheochromocytoma induced myocarditis mimicking acute myocardial infarction
11- Darze ES	2004	46	F	Nausea, vomiting, diaphoresis	STEMI	C-Sh	Mid-apical	0	Pheochromocytoma induced segmental myocardial dysfunction mimicking AMI
12- Spes C	2006	56	F	Chest pain associated with hypertension	T-wave inversion	0	Mid-apical	+	Takotsubo-like left ventricular dysfunction (apical ballooning)
13- Otsuka M	2006	63	F	Substernal chest pain	STEMI	0	Mid-apical	0	Left ventricular apical ballooning
14- Grinda JM	2006	49	M	Abdominal pain, vomiting, headache and malaise	Nonspecific changes	P-Ed, C-A, C-Sh and multiple organ failure	Global	0	Under TS-era: unusual cardiogenic shock due to pheochromocytoma
15- Sanchez-Recalde A	2006	41	F	Headache, psychomotor agitation, diaphoresis, nausea and vomiting	ST-depression	C-A, EMD and respiratory deterioration	Mid-basal	0	—
16- Van Spall HG	2007	43	F	Chest tightness, palpitation, light-headedness, and sweating	Deep T-wave inversion	0	Mid-apical	0	—
17- Takizawa M	2007	32	M	Chest pain and back pain	ST-depression	HF	Mid-basal	0	Left ventricular end-diastolic pressure 26 mm Hg
18- Kim HS	2007	47	M	Headache, palpitation and dyspnea	ST-depression	P-Ed, C-Sh and circulatory failure	Mid-basal	0	—
19- Brukamp K	2007	52	F	Fever, nausea, emesis, and diffuse abdominal pain	ST-depression	C-Sh, P-Ed and RF	Mid-basal	0	Rapidly reversible cardiogenic shock
20- Di Valentino M	2008	52	F	Chest pain, dyspnea, hypertensive crisis, and headache	ST-depression	0	Mid-basal	0	—-
21- Kim EM	2008	32	M	Palpitation with squeezing chest pain	STEMI	0	Mid-basal	0	Text: echocardiography midventricular dilatation but on LV angio mid-basal.
22- Pfister R	2008	59	F	Chest pain and dyspnea	T-wave inversion	0	Mid-basal	+(5 times)	Recurrence for the fifth time with different contractile patterns
23- Barriales-vill R	2008	41	F	Anginal chest pain	STEMI	0	Mid-ventricular	0	—
24- Zegdi R	2008	51	F	Symptoms of respiratory failure, tachycardia and hypertension	ST-depression	RF, P-Ed C-Sh, EMD, and metabolic acidosis	Mid-basal	0	—
25- de Souza F	2008	31	F	Precordial pain, associated with palpitation and hypertensive crisis	STEMI	HF	Mid-apical	0	—
26- Mrdovic I	2008	53	F	Anginal chest pain after intense emotional stress	STEMI	LV thrombus, LVOT obstruction	Mid-apical	0	—
27- Lassnig E	2009	71	F	Syncope, nausea, vomiting and hypotension. chest pain	S tachyc	C-Sh, P-Ed, multi-organ failure, fever and death	Mid-apical	+	Recurrence, multiple complications and death
28- Zhou W	2009	43	F	Rapidly progressive dyspnea, and tachycardia	STEMI	VT, HF, Thrombo-embolism	Apical	+	Concurrent pheochromocytoma, VT, LV thrombus, and systemic embolization
29- Cho DK	2009	45	F	Saturation dropped with tachycardia, tachypnea and hypoxia	T-inversion	P-Ed	Mid-ventricular	0	—
30- Jindal V	2009	55	M	Palpitation, chest pain and headache	ST-depression	P-Ed, C-Sh, RF	Mid-basal	0	—
31- Jang SY	2009	62	F	Dizziness during recurrence, Increased BP during the first attack	T-inversion	0	Mid-apical	+	The first attack manifested with increased BP during anesthesia, mid-basal pattern
32- Rossi AP (abstract)	2009	81	F	Chest discomfort	STEMI	HF	Apical	+	The first attack was of unknown localization
33- von Bergen NH	2009	17	M	Emesis, hypertension and difficulty in maintaining balance	STEMI	P-Ed	Mid-apical	0	—
34- Cesaretti M (abstract)	2010	N/A	F	Abdominal and chest pain, headache, nausea and sweating	STEMI	0	Mid-apical	0	—
35- Tanriver Y	2010	57	M	Chest and epigastric pain, repeated vomiting, and dyspnea	STEMI	P-Ed	Mid-apical	0	In this case, sepsis may have been the trigger factor
36- Kim S	2010	30	M	Severe suprapubic and left lower abdominal pain	ST-depression	P-Ed	Mid-basal	0	—
37- Zielen P	2010	53	M	Chest pain, dyspnea, epigastric discomfort, nausea and vomiting	STEMI	0	Mid-apical	0	—
38- Marcovitz PA	2010	43	F	Waxing and waning headache, palpitation and chest pain	STEMI	0	Mid-apical	0	—
39- Kimura S	2010	36	F	Dyspnea and shock, high BP	ST-depression, tall T-wave	Shock and P-Ed	Mid-basal	0	–
40- Gujja KR	2010	46	F	Chest pain, tightness palpitation, sweating and dyspnea	STEMI	0	Mid-apical	0	—
41- Di Palma G	2010	29	F	Dyspnea, orthopnea and vomiting	Nonspecific changes	P-Ed and C-Sh	Mid-basal	+(twice)	Two recurrences, the second of the same type, the third was unclear
42- Kumar S	2010	57	F	Headache, vomiting, chest discomfort and palpitation	S tachyc and LBBB	P-Ed, C-Sh and metabolic acidosis	Mid-basal	0
43- Ueda H	2011	86	M	Abdominal fullness, diagnosed as ileus and ileus tube was inserted	STEMI	Death	Mid-apical	0 (died)	Died due to pneumonia Pathology: catecholamine-induced cardiomyopathy.
44- Zinnamosca L (abstract)	2011	72	F	Chest pain associated with high BP	Non-STEMI	N/A	Mid-apical	0	—
45- Roghi A	2011	64	F	Breathlessness, dizziness, and palpitation	ST-depression	0	Focal	0	Described as adrenergic myocarditis but all the findings argue for TS
46- Chia PL	2011	69	F	Chest pain, dyspnea, diaphoresis, epigastric pain and palpitation	STEMI	0	Mid-apical	0	—
47- Verrijcken A	2011	62	F	Headache and scotoma and then dizziness and drowsiness	STEMI	P-Ed, C-Sh and LV-thrombo-embolisnm	Mid-apical	0	—
48- Park JH	2011	41	M	Dyspnea	S tachyc	P-Ed	Mid-basal	0	—
49- Park JH	2011	49	F	Dyspnea, chest discomfort, palpitation and recurrent headache	S tachyc	P-Ed and hypoxia	Global	0	—
50- McEntee RK	2011	43	F	Chest pressure, nausea, vomiting, dyspnea, palpitation, diaphoresis	T-wave inversion	C-Sh	Global	0	Severe dilated cardiomyopathy in undiagnosed adrenal pheochromocytoma
51- Subramanyam S	2012	60	M	Chest pain, palpitation, headache and episodes of diaphoresis	STEMI	0	Mid-apical	+	The recurrence had the same TS pattern
52- Celebi H (abstract)	2012	66	F	Chest pain	STEMI	0	Apical	+	The first episode of TS was of the same localization as the index presentation
53- Park JY	2012	28	F	Chest discomfort	ST-depression	0	Mid-basal	0	—
54- Banfi C	2012	20	F	Chest pain, severe dyspnea, cough and hyperthermia	ST-depression	P-Ed and refractory shock	Global	0	The TS localization was described in the text as severe LVD
55- Santoro F	2012	17	F	Epigastric pain, headache, agitation, nausea and vomiting	STEMI	0	Mid-apical	0	—
56- Naderi N	2012	31	F	Palpitation, fatigue, dyspnea, headache, diaphoresis, high BP	ST-depression	HF	Mid-basal	0	The patient was improved on the second day
57- Demircelik MB	2013	64	M	Chest pain and palpitation	STEMI	0	Mid-apical	0	Very short case report
58- Kashioulis P (Swedish)	2013	39	F	Palpitation, shoulder pain, nausea and profuse sweating	S tachyc	P-Ed, C-Sh, RF and Biventricular svikt	Global	0	Pregnant patient: pheochromocytoma is a life threatening cause of heart failure
59- Kaese S	2013	43	M	Polymorph VT	Polymorph VT	Polymorph VT, refractory HFand C-Sh	Global	+	First attack, mid-apical; the present, severe impairment of LV function
60- Law C	2013	23	F	Intractable vomiting and acute chest pain	Tachycardia (arrhythmia)	Arrhythmia, P-Ed, C-Sh and biventricular failure	Global	0	The TS localization was described as severe biventricular failure
61- Iio K	2013	29	F	Severe dyspnea and shock	ST-depression	P-Ed, C-Sh, RF, coma and metabolic acidosis	Mid-basal	0	—
62- Battimelli A	2014	63	F	Chest pain, resting dyspnea and peripheral coldness	STEMI	P-Ed, Right tibial artery embolization	Mid-apical	0	—
63- Kobayashi Y	2014	N/A	F	Chest pain	T-wave inversion	0	Apical or mid-apical	0	—
64- Jozwik-Plebanek K	2014	32	F	Postoperative headache and shortness of breath	N/A	P-Ed, C-Sh, C-A, and stroke	Mid-apical	0	—
65- Cho SK	2014	45	M	Chest pain	Tall peaked T-wave	0	Basal	0	—
66- Pereira-da-Silva T	2014	41	F	Cardiogenic shock	S tachyc	C-Sh	Global	+	The first attack, during pregnancy complicated by pulmonary edema
67-Satendra M	2014	40	M	Cough, dyspnea, constricting chest pain, pallor and profuse sweating	S tachyc and long QT interval	HF	Global	0	—
68- Saporito F	2014	32	M	Palpitation, sweating, and effort dyspnea	Nonspecific ST-T changes	0	Global	0	Described as acute heart failure due to pheochromocytoma crisis
69- Zhu D	2014	67	F	Dizzines, vomiting, stomache, chest pain and dyspnea	STEMI	P-Ed, C-Sh and metabolic acidosis	Mid-apical	0	Multiple complications (tachycardia, tachypnea, hypoxia, acidosis, fever)
70- Flam B	2014	46	F	Abdominal pain, dyspnea, nausea and vomiting	ST-depression	P-Ed, C-Sh, C-A, RF, stroke, metabolic acidosis, and biventricular F	Mid-basal	0	Mid-basal TS progresses to severe global biventricular failure
71- Gervais MK	2015	26	M	Right abdominal flank pain, diarrhea and vomiting	Non-specific T-wave abnormality	Hypertensive crisis and EMD	Mid-basal	0	—
72- Kounatiadis P	2015	33	F	Dizziness, profuse sweating and increased BP	STEMI	Bred QRS tachycardia and SVT	Global	0	Deemed as global due to diffuse myocardial hypokinesia
73- Brugts JJ	2015	75	F	Chest pain	ST-depression	0	Mid-basal	+	The recurrence was 2 years later and of the same pattern (mid-basal)
74- Y-Hassan S	2015	68	F	Chest pain	T-wave inversion	HF and ischemic stroke during recurrence	Mid-apical	+	The recurrence was of the same TS localization pattern
75- Sharkey SW	2015	16	M	Chest pain	STEMI	0	Mid-ventricular	0	—
76- Sharkey SW	2015	66	M	Acute hypertension, tachycardia, and symptoms of pulmonary edema	ST-depression	P-Ed and RF	Basal	0	—
77- Ibrahim M	2015	39	F	Chest pain associated with diaphoresis and syncope	STEMI	P-Ed, C-Sh and RF	Mid-apical	0	—
78- Yang TH	2015	54	F	Chest tightness, cold sweating, upper back pain, and palpitation	STEMI	0	Mid-apical	0	Recurrent pheochromocytoma in the left adrenal with liver metastases
79- Tagawa M	2015	33	F	Headache, palpitation, chest pain, fatigue and dyspnea	T-wave inversion	Hemodynamic compromise, low BP	Mid-ventricular	0
80- Assefa D English abstract	2015	42	F	Symptoms and signs of cardiogenic shock	ST-depression	C-Sh, P-Ed, RF, hypertensive crisis	Mid-basal	0	Presented with cardiogenic shock

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