Sex differences in cardiac electrophysiology and clinical arrhythmias: Epidemiology, therapeutics, and mechanisms

Canadian Journal of Cardiology

Volumn 30, Issue 7, 2014, Pages 783-792

  Tadros, Rafik ^a   Ton, Anh Tuan ^a,b   Fiset, Céline ^a,b   Nattel, Stanley ^a  

^a MONTREAL HEART INSTITUTE   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ATRIOVENTRICULAR BLOCK; BRADYCARDIA; BRUGADA SYNDROME; CARDIOMYOPATHY; CARDIOVASCULAR RISK; CONGENITAL HEART DISEASE; CORONARY ARTERY DISEASE; HEART ARRHYTHMIA; HEART ATRIOVENTRICULAR NODE; HEART ATRIUM FIBRILLATION; HEART ATRIUM FUNCTION; HEART ELECTROPHYSIOLOGY; HEART FAILURE; HEART REPOLARIZATION; HEART SUPRAVENTRICULAR ARRHYTHMIA; HEART VENTRICLE ARRHYTHMIA; HEART VENTRICLE FIBRILLATION; HEART VENTRICLE FUNCTION; HEART VENTRICLE TACHYCARDIA; HUMAN; IDIOPATHIC DISEASE; INHERITANCE; LONG QT SYNDROME; PATHOLOGICAL ANATOMY; PATIENT CARE; QT INTERVAL; REVIEW; SEX DIFFERENCE; SICK SINUS SYNDROME; SUPRAVENTRICULAR TACHYCARDIA;

ANTI-ARRHYTHMIA AGENTS; ARRHYTHMIAS, CARDIAC; BUNDLE OF HIS; CARDIAC RESYNCHRONIZATION THERAPY; ELECTROPHYSIOLOGIC TECHNIQUES, CARDIAC; FEMALE; HEART RATE; HUMANS; MALE; MORBIDITY; RISK ASSESSMENT; RISK FACTORS; SEX FACTORS; WORLD HEALTH;

EID: 84902962040     PISSN: 0828282X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cjca.2014.03.032     Document Type: Review

References (107)

1. Bazett H. An analysis of the time-relations of electrocardiograms. Heart 1920, 7:353-370.
2. Taneja T., Mahnert B.W., Passman R., Goldberger J., Kadish A. Effects of sex and age on electrocardiographic and cardiac electrophysiological properties in adults. Pacing Clin Electrophysiol 2001, 24:16-21.
3. Burke J.H., Goldberger J.J., Ehlert F.A. Gender differences in heart rate before and after autonomic blockade: evidence against an intrinsic gender effect. Am J Med 1996, 100:537-543.
4. El Khoury N., Mathieu S., Marger L., et al. Upregulation of the hyperpolarization-activated current increases pacemaker activity of the sinoatrial node and heart rate during pregnancy in mice. Circulation 2013, 127:2009-2020.
5. Liu S., Yuan S., Kongstad O., Olsson S.B. Gender differences in the electrophysiological characteristics of atrioventricular conduction system and their clinical implications. Scand Cardiovasc J 2001, 35:313-317.
6. Insulander P., Vallin H. Gender differences in electrophysiologic effects of mental stress and autonomic tone inhibition: a study in health individuals. JCardiovasc Electrophysiol 2005, 16:59-63.
7. Dhala A., Underwood D., Leman R., et al. Signal-averaged P-wave analysis of normal controls and patients with paroxysmal atrial fibrillation: a study in gender differences, age dependence, and reproducibility. Clin Cardiol 2002, 25:525-531.
8. Tse H.F., Oral H., Pelosi F., et al. Effect of gender on atrial electrophysiologic changes induced by rapid atrial pacing and elevation of atrial pressure. JCardiovasc Electrophysiol 2001, 12:986-989.
9. James A.F., Choisy S.C., Hancox J.C. Recent advances in understanding sex differences in cardiac repolarization. Prog Biophys Mol Biol 2007, 94:265-319.
10. Burke J.H., Ehlert F.A., Kruse J.T., et al. Gender-specific differences in the QT interval and the effect of autonomic tone and menstrual cycle in healthy adults. Am J Cardiol 1997, 79:178-181.
11. Surawicz B., Parikh S.R. Prevalence of male and female patterns of early ventricular repolarization in the normal ECG of males and females from childhood to old age. JAm Coll Cardiol 2002, 40:1870-1876.
12. Fulop L., Banyasz T., Szabo G., et al. Effects of sex hormones on ECG parameters and expression of cardiac ion channels in dogs. Acta Physiol (Oxf) 2006, 188:163-171.
13. Xiao L., Zhang L., Han W., Wang Z., Nattel S. Sex-based transmural differences in cardiac repolarization and ionic-current properties in canine left ventricles. Am J Physiol Heart Circ Physiol 2006, 291:H570-H580.
14. Cheng J. Evidences of the gender-related differences in cardiac repolarization and the underling mechanisms in different animal species and human. Fundam Clin Pharmacol 2006, 20:1-8.
15. James A.F., Arberry L.A., Hancox J.C. Gender-related differences in ventricular myocyte repolarization in guinea pig. Basic Res Cardiol 2004, 99:183-192.
16. Bai C.X., Kurokawa J., Tamagawa M., Nakaya H., Furukawa T. Nontranscriptional regulation of cardiac repolarization currents by testosterone. Circulation 2005, 112:1701-1710.
17. Nakajima T., Iwasawa K., Oonuma H., et al. Antiarrhythmic effect and its underlying ionic mechanism of 17beta-estradiol in cardiac myocytes. Br J Pharmacol 1999, 127:429-440.
18. Trepanier-Boulay V., St-Michel C., Tremblay A., Fiset C. Gender-based differences in cardiac repolarization in mouse ventricle. Circ Res 2001, 89:437-444.
19. Brouillette J., Trepanier-Boulay V., Fiset C. Effect of androgen deficiency on mouse ventricular repolarization. JPhysiol 2003, 546:403-413.
20. Saito T., Ciobotaru A., Bopassa J.C., et al. Estrogen contributes to gender differences in mouse ventricular repolarization. Circ Res 2009, 105:343-352.
21. Johnson B.D., Zheng W., Korach K.S., et al. Increased expression of the cardiac L-type calcium channel in estrogen receptor-deficient mice. JGen Physiol 1997, 110:135-140.
22. Liu X.K., Katchman A., Whitfield B.H., et al. Invivo androgen treatment shortens the QT interval and increases the densities of inward and delayed rectifier potassium currents in orchiectomized male rabbits. Cardiovasc Res 2003, 57:28-36.
23. Yang X., Chen G., Papp R., et al. Oestrogen upregulates L-type Ca(2)(+) channels via oestrogen-receptor- by a regional genomic mechanism in female rabbit hearts. JPhysiol 2012, 590:493-508.
24. Chen G., Yang X., Alber S., Shusterman V., Salama G. Regional genomic regulation of cardiac sodium-calcium exchanger by oestrogen. JPhysiol 2011, 589(Pt 5):1061-1080.
25. Ca) in ventricular myocytes isolated from male and female rats. JPhysiol 2002, 544P-57P-58P.
26. Leblanc N., Chartier D., Gosselin H., et al. Age and gender differences in excitation-contraction coupling of the rat ventricle. JPhysiol 1998, 511:533-548.
27. Parks R.J., Howlett S.E. Sex differences in mechanisms of cardiac excitation-contraction coupling. Pflugers Arch 2013, 465:747-763.
28. Gaborit N., Varro A., Le Bouter S., et al. Gender-related differences in ion-channel and transporter subunit expression in non-diseased human hearts. JMol Cell Cardiol 2010, 49:639-646.
29. Kurokawa J., Tamagawa M., Harada N., et al. Acute effects of oestrogen on the guinea pig and human IKr channels and drug-induced prolongation of cardiac repolarization. JPhysiol 2008, 586:2961-2973.
30. Nakamura H., Kurokawa J., Bai C.X., et al. Progesterone regulates cardiac repolarization through a nongenomic pathway: an invitro patch-clamp and computational modeling study. Circulation 2007, 116:2913-2922.
31. Porter M.J., Morton J.B., Denman R., et al. Influence of age and gender on the mechanism of supraventricular tachycardia. Heart Rhythm 2004, 1:393-396.
32. Rodriguez L.M., de Chillou C., Schlapfer J., et al. Age at onset and gender of patients with different types of supraventricular tachycardias. Am J Cardiol 1992, 70:1213-1215.
33. Munger T.M., Packer D.L., Hammill S.C., et al. Apopulation study of the natural history of Wolff-Parkinson-White syndrome in Olmsted County, Minnesota, 1953-1989. Circulation 1993, 87:866-873.
34. Hsu J.C., Tanel R.E., Lee B.K., et al. Differences in accessory pathway location by sex and race. Heart Rhythm 2010, 7:52-56.
35. Klein G.J., Bashore T.M., Sellers T.D., et al. Ventricular fibrillation in the Wolff-Parkinson-White syndrome. NEngl J Med 1979, 301:1080-1085.
36. Rosano G.M., Leonardo F., Sarrel P.M., et al. Cyclical variation in paroxysmal supraventricular tachycardia in women. Lancet 1996, 347:786-788.
37. Myerburg R.J., Cox M.M., Interian A., et al. Cycling of inducibility of paroxysmal supraventricular tachycardia in women and its implications for timing of electrophysiologic procedures. Am J Cardiol 1999, 83:1049-1054.
38. Liuba I., Jonsson A., Safstrom K., Walfridsson H. Gender-related differences in patients with atrioventricular nodal reentry tachycardia. Am J Cardiol 2006, 97:384-388.
39. Rosano G.M., Leonardo F., Dicandia C., et al. Acute electrophysiologic effect of estradiol 17beta in menopausal women. Am J Cardiol 2000, 86:1385-1387. A5-6.
40. Dagres N., Clague J.R., Breithardt G., Borggrefe M. Significant gender-related differences in radiofrequency catheter ablation therapy. JAm Coll Cardiol 2003, 42:1103-1107.
41. Lessmeier T.J., Gamperling D., Johnson-Liddon V., et al. Unrecognized paroxysmal supraventricular tachycardia. Potential for misdiagnosis as panic disorder. Arch Intern Med 1997, 157:537-543.
42. Michelena H.I., Powell B.D., Brady P.A., Friedman P.A., Ezekowitz M.D. Gender in atrial fibrillation: ten years later. Gend Med 2010, 7:206-217.
43. Benjamin E.J., Levy D., Vaziri S.M., et al. Independent risk factors for atrial fibrillation in a population-based cohort. The Framingham Heart Study. JAMA 1994, 271:840-844.
44. Feinberg W.M., Blackshear J.L., Laupacis A., Kronmal R., Hart R.G. Prevalence, age distribution, and gender of patients with atrial fibrillation. Analysis and implications. Arch Intern Med 1995, 155:469-473.
45. Friberg J., Scharling H., Gadsboll N., Truelsen T., Jensen G.B. Comparison of the impact of atrial fibrillation on the risk of stroke and cardiovascular death in women versus men (The Copenhagen City Heart Study). Am J Cardiol 2004, 94:889-894.
46. Avgil Tsadok M., Jackevicius C.A., Rahme E., et al. Sex differences in stroke risk among older patients with recently diagnosed atrial fibrillation. JAMA 2012, 307:1952-1958.
47. Mikkelsen A.P., Lindhardsen J., Lip G.Y., et al. Female sex as a risk factor for stroke in atrial fibrillation: a nationwide cohort study. JThromb Haemost 2012, 10:1745-1751.
48. Friberg L., Benson L., Rosenqvist M., Lip G.Y. Assessment of female sex as a risk factor in atrial fibrillation in Sweden: nationwide retrospective cohort study. BMJ 2012, 344:e3522.
49. Gurevitz O.T., Varadachari C.J., Ammash N.M., et al. The effect of patient sex on recurrence of atrial fibrillation following successful direct current cardioversion. Am Heart J 2006, 152(155):e9-13.
50. Rienstra M., Van Veldhuisen D.J., Hagens V.E., et al. Gender-related differences in rhythm control treatment in persistent atrial fibrillation: data of the Rate Control Versus Electrical Cardioversion (RACE) study. JAm Coll Cardiol 2005, 46:1298-1306.
51. Wolbrette D.L. Risk of proarrhythmia with class III antiarrhythmic agents: sex-based differences and other issues. Am J Cardiol 2003, 91:39D-44D.
52. Essebag V., Reynolds M.R., Hadjis T., et al. Sex differences in the relationship between amiodarone use and the need for permanent pacing in patients with atrial fibrillation. Arch Intern Med 2007, 167:1648-1653.
53. Paquette M., Roy D., Talajic M., et al. Role of gender and personality on quality-of-life impairment in intermittent atrial fibrillation. Am J Cardiol 2000, 86:764-768.
54. Santangeli P., di Biase L., Pelargonio G., Natale A. Outcome of invasive electrophysiological procedures and gender: are males and females the same?. JCardiovasc Electrophysiol 2011, 22:605-612.
55. Forleo G.B., Tondo C., De Luca L., et al. Gender-related differences in catheter ablation of atrial fibrillation. Europace 2007, 9:613-620.
56. Patel D., Mohanty P., Di Biase L., et al. Outcomes and complications of catheter ablation for atrial fibrillation in females. Heart Rhythm 2010, 7:167-172.
57. Shoemaker M.B., Muhammad R., Farrell M., et al. Relation of morbid obesity and female gender to risk of procedural complications in patients undergoing atrial fibrillation ablation. Am J Cardiol 2013, 111:368-373.
58. Iwasaki Y.K., Nishida K., Kato T., Nattel S. Atrial fibrillation pathophysiology: implications for management. Circulation 2011, 124:2264-2274.
59. Tsai W.C., Chen Y.C., Lin Y.K., Chen S.A., Chen Y.J. Sex differences in the electrophysiological characteristics of pulmonary veins and left atrium and their clinical implication in atrial fibrillation. Circ Arrhythm Electrophysiol 2011, 4:550-559.
60. Tsai W.C., Chen Y.C., Kao Y.H., et al. Distinctive sodium and calcium regulation associated with sex differences in atrial electrophysiology of rabbits. Int J Cardiol 2013, 168:4658-4666.
61. Ambrosi C.M., Yamada K.A., Nerbonne J.M., Efimov I.R. Gender differences in electrophysiological gene expression in failing and non-failing human hearts. PLoS One 2013, 8:e54635.
62. Pfannmuller B., Boldt A., Reutemann A., et al. Gender-specific remodeling in atrial fibrillation?. Thorac Cardiovasc Surg 2013, 61:66-73.
63. Nowak B., Misselwitz B., Erdogan A., et al. Do gender differences exist in pacemaker implantation?-results of an obligatory external quality control program. Europace 2010, 12:210-215.
64. Schuppel R., Buchele G., Batz L., Koenig W. Sex differences in selection of pacemakers: retrospective observational study. BMJ 1998, 316:1492-1495.
65. Lamas G.A., Pashos C.L., Normand S.L., McNeil B. Permanent pacemaker selection and subsequent survival in elderly Medicare pacemaker recipients. Circulation 1995, 91:1063-1069.
66. Brunner M., Olschewski M., Geibel A., Bode C., Zehender M. Long-term survival after pacemaker implantation. Prognostic importance of gender and baseline patient characteristics. Eur Heart J 2004, 25:88-95.
67. Pyatt J.R., Somauroo J.D., Jackson M., et al. Long-term survival after permanent pacemaker implantation: analysis of predictors for increased mortality. Europace 2002, 4:113-119.
68. Sanguinetti M.C., Tristani-Firouzi M. hERG potassium channels and cardiac arrhythmia. Nature 2006, 440:463-469.
69. Makkar R.R., Fromm B.S., Steinman R.T., Meissner M.D., Lehmann M.H. Female gender as a risk factor for torsades de pointes associated with cardiovascular drugs. JAMA 1993, 270:2590-2597.
70. Lehmann M.H., Hardy S., Archibald D., Quart B., MacNeil D.J. Sex difference in risk of torsade de pointes with d,l-sotalol. Circulation 1996, 94:2535-2541.
71. Rodriguez I., Kilborn M.J., Liu X.K., Pezzullo J.C., Woosley R.L. Drug-induced QT prolongation in women during the menstrual cycle. JAMA 2001, 285:1322-1326.
72. Locati E.H., Zareba W., Moss A.J., et al. Age- and sex-related differences in clinical manifestations in patients with congenital long-QT syndrome: findings from the International LQTS Registry. Circulation 1998, 97:2237-2244.
73. Zareba W., Moss A.J., Locati E.H., et al. Modulating effects of age and gender on the clinical course of long QT syndrome by genotype. JAm Coll Cardiol 2003, 42:103-109.
74. Priori S.G., Schwartz P.J., Napolitano C., et al. Risk stratification in the long-QT syndrome. NEngl J Med 2003, 348:1866-1874.
75. Costa J., Lopes C.M., Barsheshet A., et al. Combined assessment of sex- and mutation-specific information for risk stratification in type 1 long QT syndrome. Heart Rhythm 2012, 9:892-898.
76. Han W., Wang Z., Nattel S. Slow delayed rectifier current and repolarization in canine cardiac Purkinje cells. Am J Physiol Heart Circ Physiol 2001, 280:H1075-H1080.
77. Migdalovich D., Moss A.J., Lopes C.M., et al. Mutation and gender-specific risk in type 2 long QT syndrome: implications for risk stratification for life-threatening cardiac events in patients with long QT syndrome. Heart Rhythm 2011, 8:1537-1543.
78. Barsheshet A., Dotsenko O., Goldenberg I. Genotype-specific risk stratification and management of patients with long QT syndrome. Ann Noninvasive Electrocardiol 2013, 18:499-509.
79. Priori S.G., Wilde A.A., Horie M., et al. Executive summary: HRS/EHRA/APHRS expert consensus statement on the diagnosis and management of patients with inherited primary arrhythmia syndromes. Europace 2013, 15:1389-1406.
80. Benito B., Sarkozy A., Mont L., et al. Gender differences in clinical manifestations of Brugada syndrome. JAm Coll Cardiol 2008, 52:1567-1573.
81. Di Diego J.M., Cordeiro J.M., Goodrow R.J., et al. Ionic and cellular basis for the predominance of the Brugada syndrome phenotype in males. Circulation 2002, 106:2004-2011.
82. Haissaguerre M., Derval N., Sacher F., et al. Sudden cardiac arrest associated with early repolarization. NEngl J Med 2008, 358:2016-2023.
83. Benito B., Guasch E., Rivard L., Nattel S. Clinical and mechanistic issues in early repolarization of normal variants and lethal arrhythmia syndromes. JAm Coll Cardiol 2010, 56:1177-1186.
84. Viskin S., Adler A., Belhassen B. Idiopathic ventricular fibrillation. Electrical Diseases of the Heart 2013, Vol 1:629-646. Springer-Verlag, London. 2nd ed. I. Gussak, C. Antzelevitch (Eds.).
85. Antzelevitch C., Yan G.X. Jwave syndromes. Heart Rhythm 2010, 7:549-558.
86. Alders M., Koopmann T.T., Christiaans I., et al. Haplotype-sharing analysis implicates chromosome 7q36 harboring DPP6 in familial idiopathic ventricular fibrillation. Am J Hum Genet 2009, 84:468-476.
87. Xiao L., Koopmann T.T., Ordog B., et al. Unique cardiac Purkinje fiber transient outward current beta-subunit composition: a potential molecular link to idiopathic ventricular fibrillation. Circ Res 2013, 112:1310-1322.
88. Hayashi M., Denjoy I., Extramiana F., et al. Incidence and risk factors of arrhythmic events in catecholaminergic polymorphic ventricular tachycardia. Circulation 2009, 119:2426-2434.
89. Mazzanti A., Kanthan A., Monteforte N., et al. Novel insights in the natural history of short QT syndrome. JAm Coll Cardiol 2014, 63:1300-1308.
90. Hoffmayer K.S., Gerstenfeld E.P. Diagnosis and management of idiopathic ventricular tachycardia. Curr Probl Cardiol 2013, 38:131-158.
91. Nakagawa M., Takahashi N., Nobe S., et al. Gender differences in various types of idiopathic ventricular tachycardia. JCardiovasc Electrophysiol 2002, 13:633-638.
92. Hu X., Wang J., Xu C., et al. Effect of oestrogen replacement therapy on idiopathic outflow tract ventricular arrhythmias in postmenopausal women. Arch Cardiovasc Dis 2011, 104:84-88.
93. Abi-Gerges N., Small B.G., Lawrence C.L., et al. Evidence for gender differences in electrophysiological properties of canine Purkinje fibres. Br J Pharmacol 2004, 142:1255-1264.
94. Kannel W.B., Wilson P.W., D'Agostino R.B., Cobb J. Sudden coronary death in women. Am Heart J 1998, 136:205-212.
95. Buxton A.E., Hafley G.E., Lehmann M.H., et al. Prediction of sustained ventricular tachycardia inducible by programmed stimulation in patients with coronary artery disease. Utility of clinical variables. Circulation 1999, 99:1843-1850.
96. Olsson G., Wikstrand J., Warnold I., et al. Metoprolol-induced reduction in postinfarction mortality: pooled results from five double-blind randomized trials. Eur Heart J 1992, 13:28-32.
97. Santangeli P., Pelargonio G., Dello Russo A., et al. Gender differences in clinical outcome and primary prevention defibrillator benefit in patients with severe left ventricular dysfunction: a systematic review and meta-analysis. Heart Rhythm 2010, 7:876-882.
98. van der Heijden A.C., Thijssen J., Borleffs C.J., et al. Gender-specific differences in clinical outcome of primary prevention implantable cardioverter defibrillator recipients. Heart 2013, 99:1244-1249.
99. Bhavnani S.P., Pavuluri V., Coleman C.I., et al. The gender-paradox among patients with implantable cardioverter-defibrillators: a propensity-matched study. Pacing Clin Electrophysiol 2013, 36:878-884.
100. Alba A.C., Braga J., Gewarges M., et al. Predictors of mortality in patients with an implantable cardiac defibrillator: a systematic review and meta-analysis. Can J Cardiol 2013, 29:1729-1740.
101. Hernandez A.F., Fonarow G.C., Liang L., et al. Sex and racial differences in the use of implantable cardioverter-defibrillators among patients hospitalized with heart failure. JAMA 2007, 298:1525-1532.
102. Vriesendorp P.A., Schinkel A.F., Van Cleemput J., et al. Implantable cardioverter-defibrillators in hypertrophic cardiomyopathy: patient outcomes, rate of appropriate and inappropriate interventions, and complications. Am Heart J 2013, 166:496-502.
103. O'Mahony C., Lambiase P.D., Quarta G., et al. The long-term survival and the risks and benefits of implantable cardioverter defibrillators in patients with hypertrophic cardiomyopathy. Heart 2012, 98:116-125.
104. Bauce B., Frigo G., Marcus F.I., et al. Comparison of clinical features of arrhythmogenic right ventricular cardiomyopathy in men versus women. Am J Cardiol 2008, 102:1252-1257.
105. Verheugt C.L., Uiterwaal C.S., van der Velde E.T., et al. Gender and outcome in adult congenital heart disease. Circulation 2008, 118:26-32.
106. Khairy P., Aboulhosn J., Gurvitz M.Z., et al. Arrhythmia burden in adults with surgically repaired tetralogy of Fallot: a multi-institutional study. Circulation 2010, 122:868-875.
107. Khairy P., Harris L., Landzberg M.J., et al. Sudden death and defibrillators in transposition of the great arteries with intra-atrial baffles: a multicenter study. Circ Arrhythm Electrophysiol 2008, 1:250-257.