16. Agarwal V. Takotsubo cardiomyopathy with pheochromocytoma: when an
imitator meets a masquerader. JACC Case Rep (2019) 1:91–3. doi: 10.1016/
j.jaccas.2019.07.004
1. Ghadri JR, Wittstein IS, Prasad A, Sharkey S, Dote K, Akashi YJ, et al.
International expert consensus document on takotsubo syndrome (Part I): clinical
characteristics, diagnostic criteria, and pathophysiology. Eur Heart J (2018) 39:2032–
46. doi: 10.1093/eurheartj/ehy076
17. Paur H, Wright PT, Sikkel MB, Tranter MH, Mansfield C, O'gara P, et al. High
levels of circulating epinephrine trigger apical cardiodepression in a beta2-adrenergic
receptor/Gi-dependent manner: a new model of Takotsubo cardiomyopathy.
Circulation (2012) 126:697–706. doi: 10.1161/CIRCULATIONAHA.112.111591
2. Lyon AR, Citro R, Schneider B, Morel O, Ghadri JR, Templin C, et al.
Pathophysiology of takotsubo syndrome: JACC state-of-the-art review. J Am Coll
Cardiol (2021) 77:902–21. doi: 10.1016/j.jacc.2020.10.060
18. Shao Y, Redfors B, Scharin Tang M, Mollmann H, Troidl C, Szardien S,
et al. Novel rat model reveals important roles of beta-adrenoreceptors in stressinduced cardiomyopathy. Int J Cardiol (2013) 168:1943–50. doi: 10.1016/
j.ijcard.2012.12.092
3. Singh T, Khan H, Gamble DT, Scally C, Newby DE, Dawson D. Takotsubo
syndrome: pathophysiology, emerging concepts, and clinical implications. Circulation
(2022) 145:1002–19. doi: 10.1161/CIRCULATIONAHA.121.055854
4. Templin C, Ghadri JR, Diekmann J, Napp LC, Bataiosu DR, Jaguszewski M, et al.
Clinical features and outcomes of takotsubo (Stress) cardiomyopathy. N Engl J Med
(2015) 373:929–38. doi: 10.1056/NEJMoa1406761
19. Shao Y, Redfors B, Stahlman M, Tang MS, Miljanovic A, Mollmann H, et al. A
mouse model reveals an important role for catecholamine-induced lipotoxicity in the
pathogenesis of stress-induced cardiomyopathy. Eur J Heart Fail (2013) 15:9–22. doi:
10.1093/eurjhf/hfs161
5. Wittstein IS, Thiemann DR, Lima JA, Baughman KL, Schulman SP, Gerstenblith
G, et al. Neurohumoral features of myocardial stunning due to sudden emotional stress.
N Engl J Med (2005) 352:539–48. doi: 10.1056/NEJMoa043046
6. Eitel I, Lucke C, Grothoff M, Sareban M, Schuler G, Thiele H, et al. Inflammation
in takotsubo cardiomyopathy: insights from cardiovascular magnetic resonance
imaging. Eur Radiol (2010) 20:422–31. doi: 10.1007/s00330-009-1549-5
20. Redfors B, Ali A, Shao Y, Lundgren J, Gan LM, Omerovic E. Different
catecholamines induce different patterns of takotsubo-like cardiac dysfunction in an
apparently afterload dependent manner. Int J Cardiol (2014) 174:330–6. doi: 10.1016/
j.ijcard.2014.04.103
7. Iacucci I, Carbone I, Cannavale G, Conti B, Iampieri I, Rosati R, et al. Myocardial
oedema as the sole marker of acute injury in Takotsubo cardiomyopathy: a
cardiovascular magnetic resonance (CMR) study. Radiol Med (2013) 118:1309–23.
doi: 10.1007/s11547-013-0931-1
21. Y-Hassan S, Sorensson P, Ekenback C, Lundin M, Agewall S, Brolin EB, et al.
Plasma catecholamine levels in the acute and subacute stages of takotsubo syndrome:
Results from the Stockholm myocardial infarction with normal coronaries 2 study. Clin
Cardiol (2021) 44:1567–74. doi: 10.1002/clc.23723
8. Wilson HM, Cheyne L, Brown P, Kerr K, Hannah A, Srinivasan J, et al.
Characterization of the myocardial inflammatory response in acute stress-induced
(Takotsubo) cardiomyopathy. JACC Basic Transl Sci (2018) 3:766–78. doi: 10.1016/
j.jacbts.2018.08.006
22. Scally C, Abbas H, Ahearn T, Srinivasan J, Mezincescu A, Rudd A, et al. Myocardial
and systemic inflammation in acute stress-induced (Takotsubo) cardiomyopathy. Circulation
(2019) 139:1581–92. doi: 10.1161/CIRCULATIONAHA.118.037975
23. Lachmet-Thebaud L, Marchandot B, Matsushita K, Sato C, Dagrenat C,
Greciano S, et al. Impact of residual inflammation on myocardial recovery and
cardiovascular outcome in Takotsubo patients. ESC Heart Fail (2021) 8:259–69. doi:
10.1002/ehf2.12945
9. Ghadri JR, Templin C. The interTAK registry for takotsubo syndrome. Eur Heart
J (2016) 37:2806–8. doi: 10.1093/eurheartj/ehw364
10. Brinjikji W, El-Sayed AM, Salka S. In-hospital mortality among patients with
takotsubo cardiomyopathy: a study of the National Inpatient Sample 2008 to 2009. Am
Heart J (2012) 164:215–21. doi: 10.1016/j.ahj.2012.04.010
24. Matsushita K, Lachmet-Thebaud L, Marchandot B, Trimaille A, Sato C,
Dagrenat C, et al. Incomplete recovery from takotsubo syndrome is a major
determinant of cardiovascular mortality. Circ J (2021) 85:1823–31. doi: 10.1253/
circj.CJ-20-1116
11. El-Battrawy I, Santoro F, Stiermaier T, Moller C, Guastafierro F,
Novo G, et al. Incidence and clinical impact of recurrent takotsubo syndrome:
results from the GEIST registry. J Am Heart Assoc (2019) 8:e010753. doi: 10.1161/
JAHA.118.010753
25. Vallabhajosyula S, Deshmukh AJ, Kashani K, Prasad A, Sakhuja A. Tako-tsubo
cardiomyopathy in severe sepsis: nationwide trends, predictors, and outcomes. J Am
Heart Assoc (2018) 7:e009160. doi: 10.1161/JAHA.118.009160
12. Kato K, Di Vece D, Cammann VL, Micek J, Szawan KA, Bacchi B, et al.
Takotsubo recurrence: morphological types and triggers and identification of risk
factors. J Am Coll Cardiol (2019) 73:982–4. doi: 10.1016/j.jacc.2018.12.033
26. Ederhy S, Dolladille C, Thuny F, Alexandre J, Cohen A. Takotsubo syndrome in
patients with cancer treated with immune checkpoint inhibitors: a new adverse cardiac
complication. Eur J Heart Fail (2019) 21:945–7. doi: 10.1002/ejhf.1497
13. Abraham J, Mudd JO, Kapur NK, Klein K, Champion HC, Wittstein IS. Stress
cardiomyopathy after intravenous administration of catecholamines and beta-receptor
agonists. J Am Coll Cardiol (2009) 53:1320–5. doi: 10.1016/j.jacc.2009.02.020
27. Sato T, Hagiwara K, Nishikido A, Miyamoto S, Komiyama K, Matsuno H, et al.
Takotsubo (ampulla-shaped) cardiomyopathy associated with microscopic
polyangiitis. Intern Med (2005) 44:251–5. doi: 10.2169/internalmedicine.44.251
14. Bhat S, Gazi H, Mwansa V, Chhabra L. Catecholamine-induced reverse
takotsubo cardiomyopathy. Proc (Bayl Univ Med Cent) (2019) 32:567–9. doi:
10.1080/08998280.2019.1634229
28. Morel O, Sauer F, Imperiale A, Cimarelli S, Blondet C, Jesel L, et al. Importance
of inflammation and neurohumoral activation in Takotsubo cardiomyopathy. J Card
Fail (2009) 15:206–13. doi: 10.1016/j.cardfail.2008.10.031
15. Giavarini A, Chedid A, Bobrie G, Plouin PF, Hagege A, Amar L. Acute
catecholamine cardiomyopathy in patients with phaeochromocytoma or functional
paraganglioma. Heart (2013) 99:1438–44. doi: 10.1136/heartjnl-2013-304073
Frontiers in Immunology
29. Pirzer R, Elmas E, Haghi D, Lippert C, Kralev S, Lang S, et al. Platelet and
monocyte activity markers and mediators of inflammation in Takotsubo
cardiomyopathy. Heart Vessels (2012) 27:186–92. doi: 10.1007/s00380-011-0132-6
08
frontiersin.org
Lim et al.
10.3389/fimmu.2023.1254011
30. Fitzgibbons TP, Edwards YJK, Shaw P, Iskandar A, Ahmed M, Bote J, et al.
Activation of inflammatory and pro-thrombotic pathways in acute stress
cardiomyopathy. Front Cardiovasc Med (2017) 4:49. doi: 10.3389/fcvm.2017.00049
53. Tiwary SK, Hayashi T, Kovacs A, Mann DL. Recurrent myocardial injury leads
to disease tolerance in a murine model of stress-induced cardiomyopathy. JACC Basic
Transl Sci (2023), 8(7):783–97. doi: 10.1016/j.jacbts.2022.12.007
31. Ghadri JR, Kato K, Cammann VL, Gili S, Jurisic S, Di Vece D, et al. Long-term
prognosis of patients with takotsubo syndrome. J Am Coll Cardiol (2018) 72:874–82.
doi: 10.1016/j.jacc.2018.06.016
54. Hayashi T, Tiwary SK, Lim KRQ, Rocha-Resende C, Kovacs A, Weinheimer C,
et al. Refining the reproducibility of a murine model of stress-induced reversible
cardiomyopathy. Am J Physiol Heart Circ Physiol (2023) 324:H229–40. doi: 10.1152/
ajpheart.00684.2022
32. Gudenkauf B, Goetsch MR, Vakil RM, Cingolani O, Adamo L. Case report:
steroid-responsive takotsubo cardiomyopathy associated with cytokine storm and
obstructive shock. Front Cardiovasc Med (2022) 9:931070. doi: 10.3389/
fcvm.2022.931070
55. Hayashi T, Tiwary SK, Lavine KJ, Acharya S, Brent M, Adamo L, et al. The
programmed death-1 signaling axis modulates inflammation and LV structure/
function in a stress-induced cardiomyopathy model. JACC Basic Transl Sci (2022)
7:1120–39. doi: 10.1016/j.jacbts.2022.05.006
33. Santoro F, Costantino MD, Guastafierro F, Triggiani G, Ferraretti A, Tarantino
N, et al. Inflammatory patterns in Takotsubo cardiomyopathy and acute coronary
syndrome: A propensity score matched analysis. Atherosclerosis (2018) 274:157–61.
doi: 10.1016/j.atherosclerosis.2018.05.017
56. Liao X, Chang E, Tang X, Watanabe I, Zhang R, Jeong HW, et al. Cardiac
macrophages regulate isoproterenol-induced Takotsubo-like cardiomyopathy. JCI
Insight (2022) 7:e156236. doi: 10.1172/jci.insight.156236
34. Santoro F, Tarantino N, Ferraretti A, Ieva R, Musaico F, Guastafierro F, et al.
Serum interleukin 6 and 10 levels in Takotsubo cardiomyopathy: Increased admission
levels may predict adverse events at follow-up. Atherosclerosis (2016) 254:28–34. doi:
10.1016/j.atherosclerosis.2016.09.012
57. Forte E, Panahi M, Baxan N, Ng FS, Boyle JJ, Branca J, et al. Type 2 MI induced
by a single high dose of isoproterenol in C57BL/6J mice triggers a persistent adaptive
immune response against the heart. J Cell Mol Med (2021) 25:229–43. doi: 10.1111/
jcmm.15937
35. Scally C, Rudd A, Mezincescu A, Wilson H, Srivanasan J, Horgan G, et al.
Persistent long-term structural, functional, and metabolic changes after stress-induced
(Takotsubo) cardiomyopathy. Circulation (2018) 137:1039–48. doi: 10.1161/
CIRCULATIONAHA.117.031841
58. Forte E, Perkins B, Sintou A, Kalkat HS, Papanikolaou A, Jenkins C, et al. Crosspriming dendritic cells exacerbate immunopathology after ischemic tissue damage
in the heart. Circulation (2021) 143:821–36. doi: 10.1161/CIRCULATIONAHA.
120.044581
36. Neil C, Nguyen TH, Kucia A, Crouch B, Sverdlov A, Chirkov Y, et al. Slowly
resolving global myocardial inflammation/oedema in Tako-Tsubo cardiomyopathy:
evidence from T2-weighted cardiac MRI. Heart (2012) 98:1278–84. doi: 10.1136/
heartjnl-2011-301481
59. Surikow SY, Nguyen TH, Stafford I, Chapman M, Chacko S, Singh K, et al.
Nitrosative stress as a modulator of inflammatory change in a model of takotsubo
syndrome. JACC Basic Transl Sci (2018) 3:213–26. doi: 10.1016/j.jacbts.2017.10.002
37. Scally C, Ahearn T, Rudd A, Neil CJ, Srivanasan J, Jagpal B, et al. Right
ventricular involvement and recovery after acute stress-induced (Tako-tsubo)
cardiomyopathy. Am J Cardiol (2016) 117:775–80. doi: 10.1016/j.amjcard.2015.11.057
60. Kolodzinska A, Czarzasta K, Szczepankiewicz B, Glowczynska R, Fojt A, Ilczuk
T, et al. Toll-like receptor expression and apoptosis morphological patterns in female
rat hearts with takotsubo syndrome induced by isoprenaline. Life Sci (2018) 199:112–
21. doi: 10.1016/j.lfs.2018.02.042
38. Nef HM, Mollmann H, Kostin S, Troidl C, Voss S, Weber M, et al. Tako-Tsubo
cardiomyopathy: intraindividual structural analysis in the acute phase and after
functional recovery. Eur Heart J (2007) 28:2456–64. doi: 10.1093/eurheartj/ehl570
61. Wallner M, Duran JM, Mohsin S, Troupes CD, Vanhoutte D, Borghetti G, et al.
Acute catecholamine exposure causes reversible myocyte injury without cardiac
regeneration. Circ Res (2016) 119:865–79. doi: 10.1161/CIRCRESAHA.116.308687
39. Surikow SY, Raman B, Licari J, Singh K, Nguyen TH, Horowitz JD. Evidence of
nitrosative stress within hearts of patients dying of Tako-tsubo cardiomyopathy. Int J
Cardiol (2015) 189:112–4. doi: 10.1016/j.ijcard.2015.03.416
62. Sachdeva J, Dai W, Kloner RA. Functional and histological assessment of an
experimental model of Takotsubo's cardiomyopathy. J Am Heart Assoc (2014) 3:
e000921. doi: 10.1161/JAHA.114.000921
40. Elsokkari I, Cala A, Khan S, Hill A. Takotsubo cardiomyopathy: not always
innocent or predictable. A unique post mortem insight. Int J Cardiol (2013) 167:e46–
48. doi: 10.1016/j.ijcard.2013.03.090
63. Ellison GM, Torella D, Karakikes I, Purushothaman S, Curcio A, Gasparri C,
et al. Acute b-adrenergic overload produces myocyte damage through calcium leakage
from the ryanodine receptor 2 but spares cardiac stem cells. J Biol Chem (2007)
282:11397–11409.
41. Kapellos TS, Bonaguro L, Gemund I, Reusch N, Saglam A, Hinkley ER, et al.
Human monocyte subsets and phenotypes in major chronic inflammatory diseases.
Front Immunol (2019) 10:2035. doi: 10.3389/fimmu.2019.02035
64. Redfors B, Shao Y, Wikstrom J, Lyon AR, Oldfors A, Gan LM, et al. Contrast
echocardiography reveals apparently normal coronary perfusion in a rat model of
stress-induced (Takotsubo) cardiomyopathy. Eur Heart J Cardiovasc Imaging (2014)
15:152–7. doi: 10.1093/ehjci/jet079
42. Ozanska A, Szymczak D, Rybka J. Pattern of human monocyte subpopulations
in health and disease. Scand J Immunol (2020) 92:e12883. doi: 10.1111/sji.12883
65. Willis BC, Salazar-Cantu A, Silva-Platas C, Fernandez-Sada E, Villegas CA, RiosArgaiz E, et al. Impaired oxidative metabolism and calcium mishandling underlie
cardiac dysfunction in a rat model of post-acute isoproterenol-induced
cardiomyopathy. Am J Physiol Heart Circ Physiol (2015) 308:H467–477. doi:
10.1152/ajpheart.00734.2013
43. Liu S, Ngo D, Chirkov Y, Stansborough J, Chong CR, Horowitz JD. Prolonged
suppression of the anti-oxidant/anti-inflammatory effects of BNP post-Takotsubo
syndrome. ESC Heart Fail (2020) 7:2250–7. doi: 10.1002/ehf2.12729
44. Venkatraman A, Bajaj NS, Khawaja A, Meador W. Cardiogenic shock from
atypical Takotsubo cardiomyopathy attributed to acute disseminated encephalomyelitis
lesion involving the medulla. Clin Auton Res (2016) 26:149–51. doi: 10.1007/s10286016-0346-x
66. Ali A, Redfors B, Lundgren J, Alkhoury J, Oras J, Gan LM, et al. Effects of
pretreatment with cardiostimulants and beta-blockers on isoprenaline-induced
takotsubo-like cardiac dysfunction in rats. Int J Cardiol (2019) 281:99–104. doi:
10.1016/j.ijcard.2018.12.045
45. Srichawla BS. Dimethyl fumarate-induced takotsubo cardiomyopathy in a
patient with relapsing-remitting multiple sclerosis. Cureus (2022) 14:e23789. doi:
10.7759/cureus.23789
67. Grimm D, Elsner D, Schunkert H, Pfeifer M, Griese D, Bruckschlegel G, et al.
Development of heart failure following isoproterenol administration in the rat: role of
the renin-angiotensin system. Cardiovasc Res (1998) 37:91–100. doi: 10.1016/S00086363(97)00212-5
46. Lin W, Tay SH, Mak A. Takotsubo syndrome and rheumatic diseases-a critical
systematic review. Rheumatol (Oxford) (2021) 60:11–22. doi: 10.1093/rheumatology/
keaa504
68. Angelini P, Tobis JM. Is high-dose catecholamine administration in small
animals an appropriate model for takotsubo syndrome? Circ J (2015) 79:897. doi:
10.1253/circj.CJ-15-0099
47. Mirijello A, D'errico MM, Curci S, Bossa F, D'angelo C, Vendemiale G, et al.
Takotsubo syndrome and inflammatory bowel diseases: does a link exist? Dig Dis
(2020) 38:204–10. doi: 10.1159/000502088
69. Seong SY, Matzinger P. Hydrophobicity: an ancient damage-associated
molecular pattern that initiates innate immune responses. Nat Rev Immunol (2004)
4:469–78. doi: 10.1038/nri1372
48. De Giorgi A, Fabbian F, Pala M, Parisi C, Misurati E, Molino C, et al. Takotsubo
cardiomyopathy and acute infectious diseases: a mini-review of case reports. Angiology
(2015) 66:257–61. doi: 10.1177/0003319714523673
70. Lin Q, Li M, Fang D, Fang J, Su SB. The essential roles of Toll-like receptor
signaling pathways in sterile inflammatory diseases. Int Immunopharmacol (2011)
11:1422–32. doi: 10.1016/j.intimp.2011.04.026
49. Shah RM, Shah M, Shah S, Li A, Jauhar S. Takotsubo syndrome and COVID-19:
associations and implications. Curr Probl Cardiol (2021) 46:100763. doi: 10.1016/
j.cpcardiol.2020.100763
71. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy.
Nat Rev Cancer (2012) 12:252–64. doi: 10.1038/nrc3239
50. Y-Hassan S. Myocarditis is an essential feature rather than an exclusion criterion
for takotsubo syndrome: Case report. Int J Cardiol (2015) 187:304–6. doi: 10.1016/
j.ijcard.2015.03.275
72. Cueto FJ, Del Fresno C, Sancho D. DNGR-1, a dendritic cell-specific sensor of
tissue damage that dually modulates immunity and inflammation. Front Immunol
(2019) 10:3146. doi: 10.3389/fimmu.2019.03146
51. Kvetnansky R, Sun CL, Lake CR, Thoa N, Torda T, Kopin IJ. Effect of handling
and forced immobilization on rat plasma levels of epinephrine, norepinephrine, and
dopamine-beta-hydroxylase. Endocrinology (1978) 103:1868–74. doi: 10.1210/endo103-5-1868
73. Rona G, Chappel CI, Balazs T, Gaudry R. An infarct-like myocardial lesion and
other toxic manifestations produced by isoproterenol in the rat. AMA Arch Pathol
(1959) 67:443–55.
52. Ueyama T, Kasamatsu K, Hano T, Yamamoto K, Tsuruo Y, Nishio I. Emotional
stress induces transient left ventricular hypocontraction in the rat via activation of
cardiac adrenoceptors: a possible animal model of 'tako-tsubo' cardiomyopathy. Circ J
(2002) 66:712–3. doi: 10.1253/circj.66.712
Frontiers in Immunology
74. Bruns B, Antoniou M, Baier I, Joos M, Sevinchan M, Moog M-C, et al.
Calcineurin signaling promotes takotsubo syndrome. Nat Cardiovasc Res (2023)
2:645–55. doi: 10.1038/s44161-023-00296-w
09
frontiersin.org
...