Arrhythmogenic mechano-electric heterogeneity in the long-QT syndrome

Progress in Biophysics and Molecular Biology

Volumn 110, Issue 2-3, 2012, Pages 347-358

  ter Bekke, Rachel M A ^a   Volders, Paul G A ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Aftercontractions; Calcium; Electromechanical window; Long QT syndrome; Torsades de pointes; Ventricular arrhythmia

Indexed keywords

CALCIUM;

ADRENERGIC SYSTEM; ANIMAL; ELECTROPHYSIOLOGY; HUMAN; LONG QT SYNDROME; MECHANICS; MEMBRANE POTENTIAL; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; REVIEW;

ANIMALS; CALCIUM; ELECTROPHYSIOLOGICAL PROCESSES; HUMANS; LONG QT SYNDROME; MECHANICAL PROCESSES; MEMBRANE POTENTIALS; SYMPATHETIC NERVOUS SYSTEM;

ANIMALIA;

EID: 84868146658     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2012.07.007     Document Type: Review

References (112)

1. 2+ release in hypertrophied cardiac myocytes from dogs with chronic atrioventricular block. J. Physiol. 2007, 579:147-160.
2. Antzelevitch C. Role of spatial dispersion of repolarization in inherited and acquired sudden cardiac death syndromes. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H2024-H2038.
3. Antzelevitch C., Sicouri S., Litovsky S.H., Lukas A., Krishnan S.C., Di Diego J.M., Gintant G.A., Liu D.W. Heterogeneity within the ventricular wall. Electrophysiology and pharmacology of epicardial, endocardial, and M cells. Circ. Res. 1991, 69:1427-1449.
4. Berlin J.R., Cannell M.B., Lederer W.J. Cellular origins of the transient inward current in cardiac myocytes: role of fluctuations and waves of elevated intracellular calcium. Circ. Res. 1989, 65:115-126.
5. Beyder A., Strege P.R., Reyes S., Bernard C.E., Terzic A., Makielski J., Ackerman M.J., Farrugia G. Ranolazine decreases mechanosensitivity of the voltage-gated sodium ion channel NaV1.5: a novel mechanism of drug action. Circulation 2012, 125:2698-2706.
6. Birati E.Y., Belhassen B., Bardai A., Wilde A.A., Viskin S. The site of origin of torsade de pointes. Heart 2011, 97:1650-1654.
7. Blazeski A., Zhu R., Hunter D.W., Weinberg S., Zambidis E.T., Tung L. Cardiomyocytes derived from human induced pluripotent stem cells as models for normal and diseased cardiac electrophysiology and contractility. Prog. Biophys. Mol. Biol. 2012, 110(2-3):166-177.
8. Bode F., Sachs F., Franz M.R. Tarantula peptide inhibits atrial fibrillation. Nature 2001, 409:35-36.
9. Bouchard R.A., Clark R.B., Giles W.R. Effects of action potential duration on excitation-contraction coupling in rat ventricular myocytes. Action potential voltage-clamp measurements. Circ. Res. 1995, 76:790-801.
10. Boudoulas H., Geleris P., Lewis R.P., Leier C.V. Effect of increased adrenergic activity on the relationship between electrical and mechanical systole. Circulation 1981, 64:28-33.
11. Boudoulas H., Sohn Y.H., O'Neill W., Brown R., Weissler A.M. The QT greater than QS2 syndrome: a new mortality risk indicator in coronary artery disease. Am. J. Cardiol. 1982, 50:1229-1235.
12. + current in the ferret heart. Circ. Res. 1997, 81:128-135.
13. Brugada P., Wellens H.J. Early afterdepolarizations: role in conduction block, "prolonged repolarization-dependent reexcitation", and tachyarrhythmias in the human heart. Pacing Clin. Electrophysiol. 1985, 8:889-896.
14. Brutsaert D.L. Nonuniformity: a physiologic modulator of contraction and relaxation of the normal heart. J. Am. Coll. Cardiol. 1987, 9:341-348.
15. Burashnikov A., Antzelevitch C. Acceleration-induced action potential prolongation and early afterdepolarizations. J. Cardiovasc. Electrophysiol. 1998, 9:934-948.
16. Calkins H., Maughan W.L., Weisman H.F., Sugiura S., Sagawa K., Levine J.H. Effect of acute volume load on refractoriness and arrhythmia development in isolated, chronically infarcted canine hearts. Circulation 1989, 79:687-697.
17. Cannell M.B., Berlin J.R., Lederer W.J. Effect of membrane potential changes on the calcium transient in single rat cardiac muscle cells. Science 1987, 238:1419-1423.
18. Carlsson L., Abrahamsson C., Almgren O., Lundberg C., Duker G. Prolonged action potential duration and positive inotropy induced by the novel class III antiarrhythmic agent H 234/09 (Almokalant) in isolated human ventricular muscle. J. Cardiovasc. Pharmacol. 1991, 18:882-887.
19. Chambers J.B., Ward D.E. The QT and QS2 intervals in patients with mitral leaflet prolapse. Am. Heart J. 1987, 114:355-361.
20. Chen R.L., Penny D.J., Greve G., Lab M.J. Stretch-induced regional mechanoelectric dispersion and arrhythmia in the right ventricle of anesthetized lambs. Am. J. Physiol. Heart Circ. Physiol. 2004, 286:H1008-H1014.
21. + current: a potential mechanism of the proarrhythmic effects of methanesulfonanilideclass III agents. Cardiovasc. Res. 1999, 43:135-147.
22. + exchanger activation: the autocrine/paracrine loop and its mechanical counterpart. Cardiovasc. Res. 2003, 57:953-960.
23. Craelius W., Chen V., el-Sherif N. Stretch activated ion channels in ventricular myocytes. Biosci. Rep. 1988, 8:407-414.
24. De Caprio L., Ferro G., Cuomo S., Volpe M., Artiaco D., De Luca N., Ricciardelli B. QT/QS2 ratio as an index of autonomic tone changes. Am. J. Cardiol. 1984, 53:818-822.
25. De Ferrari G.M., Nador F., Beria G., Sala S., Lotto A., Schwartz P.J. Effect of calcium channel block on the wall motion abnormality of the idiopathic long QT syndrome. Circulation 1994, 89:2126-2132.
26. 2+ transient in feline ventricular myocytes. Am. J. Physiol. Heart Circ. Physiol. 1989, 257:H746-H759.
27. Dyachenko V., Husse B., Rueckschloss U., Isenberg G. Mechanical deformation of ventricular myocytes modulates both TRPC6 and Kir2.3 channels. Cell Calcium 2009, 45:38-54.
28. Ehara T., Noma A., Ono K. Calcium-activated non-selective cation channel in ventricular cells isolated from adult guinea-pig hearts. J. Physiol. 1988, 403:117-133.
29. Fabiato A. Two kinds of calcium-induced release of calcium from the sarcoplasmic reticulum of skinned cardiac cells. Adv. Exp. Med. Biol. 1992, 311:245-262.
30. Fabiato A., Fabiato F. Contractions induced by a calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J. Physiol. 1975, 249:469-495.
31. Kv43 to transmural heterogeneity of early repolarization and arrhythmogenesis in canine left ventricular myocytes. Am. J. Physiol. Heart Circ. Physiol. 2006, 291:H2617-H2629.
32. Franz M.R., Burkhoff D., Yue D.T., Sagawa K. Mechanically induced action potential changes and arrhythmia in isolated and in situ canine hearts. Cardiovasc. Res. 1989, 23:213-223.
33. + channels promote pause-induced spontaneous diastolic activity in long QT syndrome type 3 myocytes. Circ. Res. 2006, 99:1225-1232.
34. Gaborit N., Le Bouter S., Szuts V., Varro A., Escande D., Nattel S., Demolombe S. Regional and tissue specific transcript signatures of ion channel genes in the non-diseased human heart. J. Physiol. 2007, 582:675-693.
35. Gallacher D.J., Van de Water A., van der Linde H., Hermans A.N., Lu H.R., Towart R., Volders P.G. In vivo mechanisms precipitating torsades de pointes in a canine model of drug-induced long-QT1 syndrome. Cardiovasc. Res. 2007, 76:247-256.
36. Groh W.J., Gibson K.J., Maylie J.G. Hypotonic-induced stretch counteracts the efficacy of the class III antiarrhythmic agent E-4031 in guinea pig myocytes. Cardiovasc. Res. 1996, 31:237-245.
37. Guharay F., Sachs F. Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J. Physiol. 1984, 352:685-701.
38. Guinamard R., Bois P. Involvement of transient receptor potential proteins in cardiac hypertrophy. Biochim. Biophys. Acta 2007, 1772:885-894.
39. Guinamard R., Demion M., Chatelier A., Bois P. Calcium-activated nonselective cation channels in mammalian cardiomyocytes. Trends Cardiovasc. Med. 2006, 16:245-250.
40. Hales P.W., Schneider J.E., Burton R.A.B., Wright B.J., Bollensdorff C., Kohl P. Histo-anatomical structure of the living isolated rat heart in two contraction states assessed by diffusion tensor MRI. Prog. Biophys. Mol. Biol. 2012, 110(2-3):319-330.
41. Hansen D.E., Craig C.S., Hondeghem L.M. Stretch-induced arrhythmias in the isolated canine ventricle. Evidence for the importance of mechanoelectrical feedback. Circulation 1990, 81:1094-1105.
42. Haugaa K.H., Edvardsen T., Leren T.P., Gran J.M., Smiseth O.A., Amlie J.P. Left ventricular mechanical dispersion by tissue Doppler imaging: a novel approach for identifying high-risk individuals with long QT syndrome. Eur. Heart J. 2009, 30:330-337.
43. Haugaa K.H., Amlie J.P., Berge K.E., Leren T.P., Smiseth O.A., Edvardsen T. Transmural differences in myocardial contraction in long-QT syndrome: mechanical consequences of ion channel dysfunction. Circulation 2010, 122:1355-1363.
44. 2+-transient. J. Mol. Cell. Cardiol. 2011, 50:863-871.
45. 2+-activated monovalent selective cation channel. Curr. Biol. 2003, 13:1153-1158.
46. Hu H., Sachs F. Mechanically activated currents in chick heart cells. J. Membr. Biol. 1996, 154:205-216.
47. 2+ spark rate. Circ. Res. 2009, 104:787-795.
48. 2+ channel agonist Bay K 8644. Circ. Res. 1988, 62:563-571.
49. Ks restricts excessive beat-to-beat variability of repolarization during beta-adrenergic receptor stimulation. J. Mol. Cell. Cardiol. 2010, 48:122-130.
50. R4496C mouse model of CPVT, ß-adrenergic stimulation induces Ca waves by increasing SR Ca content and not by decreasing the threshold for Ca waves. Circ. Res. 2010, 107:1483-1489.
51. Katra R.P., Laurita K.R. Cellular mechanism of calcium-mediated triggered activity in the heart. Circ. Res. 2005, 96:535-542.
52. Kohl P., Bollensdorff C., Garny A. Effects of mechanosensitive ion channels on ventricular electrophysiology: experimental and theoretical models. Exp. Physiol. 2006, 91:307-321.
53. Kohl P., Sachs F., Franz M.R. Cardiac Mechano-Electric Coupling and Arrhythmias 2011, Oxford University Press, Oxford; New York, 345-351. second ed.
54. Komiya N., Tanaka K., Doi Y., Fukae S., Nakao K., Isomoto S., Seto S., Yano K. A patient with LQTS in whom verapamil administration and permanent pacemaker implantation were useful for preventing torsade de pointes. Pacing Clin. Electrophysiol. 2004, 27:123-124.
55. Kozhevnikov D.O., Yamamoto K., Robotis D., Restivo M., El-Sherif N. Electrophysiological mechanism of enhanced susceptibility of hypertrophied heart to acquired torsade de pointes arrhythmias: tridimensional mapping of activation and recovery patterns. Circulation 2002, 105:1128-1134.
56. 2+ release in the heart. Cardiovasc. Res. 1992, 26:193-214.
57. Langton P.D. Calcium channel currents recorded from isolated myocytes of rat basilar artery are stretch sensitive. J. Physiol. 1993, 471:1-11.
58. 2+-activated nonselective cation channel mediating cell membrane depolarization. Cell 2002, 109:397-407.
59. Laurita K.R., Katra R., Wible B., Wan X., Koo M.H. Transmural heterogeneity of calcium handling in canine. Circ. Res. 2003, 92:668-675.
60. 2+ overload and inhibited by ranolazine. J. Mol. Cell. Cardiol. 2009, 47:326-334.
61. Ks contributes to the longer action potential of the M cell. Circ. Res. 1995, 76:351-365.
62. Liu G.X., Choi B.R., Ziv O., Li W., de Lange E., Qu Z., Koren G. Differential conditions for early after-depolarizations and triggered activity in cardiomyocytes derived from transgenic LQT1 and LQT2 rabbits. J. Physiol. 2012, 590:1171-1180.
63. Maroto R., Raso A., Wood T.G., Kurosky A., Martinac B., Hamill O.P. TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat. Cell. Biol. 2005, 7:179-185.
64. 2+ exchanger suppresses torsades de pointes in an intact heart model of long QT syndrome-2 and long QT syndrome-3. Heart Rhythm 2008, 5:1444-1452.
65. Morad M., Trautwein W. The effect of the duration of the action potential on contraction in the mammalian heart muscle. Pflügers Arch. 1968, 299:66-82.
66. Morris C.E., Juranka P.F. Nav channel mechanosensitivity: activation and inactivation accelerate reversibly with stretch. Biophys. J. 2007, 93:822-833.
67. Nador F., Beria G., De Ferrari G.M., Stramba-Badiale M., Locati E.H., Lotto A., Schwartz P.J. Unsuspected echocardiographic abnormality in the long QT syndrome. Diagnostic, prognostic, and pathogenetic implications. Circulation 1991, 84:1530-1542.
68. Nakayama K., Yamanari H., Otsuka F., Fukushima K., Saito H., Fujimoto Y., Emori T., Matsubara H., Uchida S., Ohe T. Dispersion of regional wall motion abnormality in patients with long QT syndrome. Heart 1998, 80:245-250.
69. Nélaton A. Eléments de pathologie chirurgicale 1876, Librairie Germer Bateliere et Co., Paris, France.
70. Němec J., Kim J.J., Gabris B., Salama G. Calcium oscillations and T-wave liability precede ventricular arrhythmias in acquired long QT type 2. Heart Rhythm 2010, 7:1686-1694.
71. Nuyens D., Stengl M., Dugarmaa S., Rossenbacker T., Compernolle V., Rudy Y., Smits J.F., Flameng W., Clancy C.E., Moons L., Vos M.A., Dewerchin M., Benndorf K., Collen D., Carmeliet E., Carmeliet P. Abrupt rate accelerations or premature beats cause life-threatening arrhythmias in mice with long-QT3 syndrome. Nat. Med. 2001, 7:1021-1027.
72. Otway R., Vandenberg J.I., Guo G., Varghese A., Castro M.L., Liu J., Zhao J., Bursill J.A., Wyse K.R., Crotty H., Baddeley O., Walker B., Kuchar D., Thorburn C., Fatkin D. Stretch-sensitive KCNQ1 mutation. A link between genetic and environmental factors in the pathogenesis of atrial fibrillation?. J. Am. Coll. Cardiol. 2007, 49:578-586.
73. Priori S.G., Corr P.B. Mechanisms underlying early and delayed afterdepolarizations induced by catecholamines. Am. J. Physiol. Heart Circ. Physiol. 1990, 258:H1796-H1805.
74. Ravens U. Mechano-electric feedback and arrhythmias. Prog. Biophys. Mol. Biol. 2003, 82:255-266.
75. Sato D., Bers D.M. How does stochastic ryanodine receptor-mediated Ca leak fail to initiate a Ca spark?. Biophys. J. 2011, 101:2370-2379.
76. Savoye C., Klug D., Denjoy I., Ennezat P.V., Le Tourneau T., Guicheney P., Kacet S. Tissue Doppler echocardiography in patients with long QT syndrome. Eur. J. Echocardiogr. 2003, 4:209-213.
77. Schwartz P.J., Priori S.G., Spazzolini C., Moss A.J., Vincent G.M., Napolitano C., Denjoy I., Guicheney P., Breithardt G., Keating M.T., Towbin J.A., Beggs A.H., Brink P., Wilde A.A., Toivonen L., Zareba W., Robinson J.L., Timothy K.W., Corfield V., Wattanasirichaigoon D., Corbett C., Haverkamp W., Schulze-Bahr E., Lehmann M.H., Schwartz K., Coumel P., Bloise R. Genotype-phenotype correlation in the long-QT syndrome: gene-specific triggers for life-threatening arrhythmias. Circulation 2001, 103:89-95.
78. Seo K., Inagaki M., Nishimura S., Hidaka I., Sugimachi M., Hisada T., Sugiura S. Structural heterogeneity in the ventricular wall plays a significant role in the initiation of stretch-induced arrhythmias in perfused rabbit right ventricular tissues and whole heart preparations. Circ. Res. 2010, 106:176-184.
79. + channel opener in the LQT1 form of congenital long-QT syndrome. Circulation 1998, 97:1581-1588.
80. Shimizu W., Ohe T., Kurita T., Kawade M., Arakaki Y., Aihara N., Kamakura S., Kamiya T., Shimomura K. Effects of verapamil and propranolol on early afterdepolarizations and ventricular arrhythmias induced by epinephrine in congenital long QT syndrome. J. Am. Coll. Cardiol. 1995, 26:1299-1309.
81. Shimizu W., Ohe T., Kurita T., Takaki H., Aihara N., Kamakura S., Matsuhisa M., Shimomura K. Early after depolarizations induced by isoproterenol in patients with congenital long QT syndrome. Circulation 1991, 84:1915-1923.
82. Soltysinska E., Olesen S.P., Christ T., Wettwer E., Varró A., Grunnet M., Jespersen T. Transmural expression of ion channels and transporters in human nondiseased and end-stage failing hearts. Pflügers Arch 2009, 459:11-23.
83. 2+ release on action potentials and after depolarizations in guinea pig ventricular myocytes. Am. J. Physiol. Heart Circ. Physiol. 2003, 285:H2552-H2562.
84. Stern M.D., Capogrossi M.C., Lakatta E.G. Spontaneous calcium release from the sarcoplasmic reticulum in myocardial cells: mechanisms and consequences. Cell Calcium 1988, 9:247-256.
85. Szentadrassy N., Banyasz T., Biro T., Szabo G., Toth B.I., Magyar J., Lazar J., Varro A., Kovacs L., Nanasi P.P. Apico-basal inhomogeneity in distribution of ion channels in canine and human ventricular myocardium. Cardiovasc. Res. 2005, 65:851-860.
86. Taggart P., Sutton P., Opthof T., Coronel R., Kallis P. Electrotonic cancellation of transmural electrical gradients in the left ventricle in man. Prog. Biophys. Mol. Biol. 2003, 82:243-254.
87. Tande P.M., Refsum H. Class III antiarrhythmic action linked with positive inotropy: effects of the d- and l-isomer of sotalol on isolated rat atria at threshold and suprathreshold stimulation. Pharmacol. Toxicol. 1988, 62:272-277.
88. ter Bekke R.M., Haugaa K.H., van den Wijngaard A., Edvardsen T., Volders P.G. Electro-mechanical window: arrhythmogenic marker in genotyped long-QT syndrome (abstract). Heart Rhythm 2012, 9:S86.
89. van der Linde H.J., Van Deuren B., Somers Y., Loenders B., Towart R., Gallacher D.J. The electro-mechanical window: a risk marker for torsade de pointes in a canine model of drug induced arrhythmias. Br. J. Pharmacol. 2010, 161:1444-1454.
90. Venetucci L.A., Trafford A.W., O'Neill S.C., Eisner D.A. The sarcoplasmic reticulum and arrhythmogenic calcium release. Cardiovasc. Res. 2008, 77:285-292.
91. Vincent G.M., Jaiswal D., Timothy K.W. Effects of exercise on heart rate, QT, QTc and QT/QS2 in the Romano-Ward inherited long QT syndrome. Am. J. Cardiol. 1991, 68:498-503.
92. Viswanathan P.C., Rudy Y. Pause induced early afterdepolarizations in the long QT syndrome: a simulation study. Cardiovasc. Res. 1999, 42:530-542.
93. Volders P.G., Kulcsar A., Vos M.A., Sipido K.R., Wellens H.J., Lazzara R., Szabo B. Similarities between early and delayed afterdepolarizations induced by isoproterenol in canine ventricular myocytes. Cardiovasc. Res. 1997, 34:348-359.
94. Ks are larger in right than left canine ventricular midmyocardium. Circulation 1999, 99:206-210.
95. Ks to canine ventricular repolarization: key role for ß-adrenergic receptor stimulation. Circulation 2003, 107:2753-2760.
96. Volders P.G., Vos M.A., Szabo B., Sipido K.R., de Groot S.H., Gorgels A.P., Wellens H.J., Lazzara R. Progress in the understanding of cardiac early afterdepolarizations and torsades de pointes: time to revise current concepts. Cardiovasc. Res. 2000, 46:376-392.
97. Wan X., Laurita K.R., Pruvot E.J., Rosenbaum D.S. Molecular correlates of repolarization alternans in cardiac myocytes. J. Mol. Cell. Cardiol. 2005, 39:419-428.
98. Wang Y., Joyner R.W., Wagner M.B., Cheng J., Lai D., Crawford B.H. Stretch-activated channel activation promotes early afterdepolarizations in rat ventricular myocytes under oxidative stress. Am. J. Physiol. Heart Circ. Physiol. 2009, 296:H1227-H1235.
99. Ward M.L., Williams I.A., Chu Y., Cooper P.J., Ju Y.K., Allen D.G. Stretch-activated channels in the heart: contributions to length-dependence and to cardiomyopathy. Prog. Biophys. Mol. Biol. 2008, 97:232-249.
100. Wellens H.J., Vermeulen A., Durrer D. Ventricular fibrillation occurring on arousal from sleep by auditory stimuli. Circulation 1972, 46:661-665.
101. Wickenden A.D., Kaprielian R., Kassiri Z., Tsoporis J.N., Tsushima R., Fishman G.I., Backx P.H. The role of action potential prolongation and altered intracellular calcium handling in the pathogenesis of heart failure. Cardiovasc. Res. 1998, 37:312-323.
102. 1). J. Am. Coll. Cardiol. 1999, 33:327-332.
103. Wood E.H., Heppner R.L., Weidmann S. Inotropic effects of electric currents. I. Positive and negative effects of constant electric currents or current pulses applied during cardiac action potentials. II. Hypotheses: calcium movements, excitation-contraction coupling and inotropic effects. Circ. Res. 1969, 24:409-445.
104. 2+ exchange: evidence for differential expression in normal and failing hearts. Circ. Res. 2005, 97:207-209.
105. Yamada K.A., Corr P.B. Effects of β-adrenergic receptor activation on intracellular calcium and membrane potential in adult cardiac myocytes. J. Cardiovasc. Electrophysiol. 1992, 3:209-224.
106. 1325S, in single murine ventricular myocytes. Biochem. Biophys. Res. Commun. 2007, 352:378-383.
107. Zabel M., Koller B.S., Sachs F., Franz M.R. Stretch-induced voltage changes in the isolated beating heart: importance of the timing of stretch and implications for stretch-activated ion channels. Cardiovasc. Res. 1996, 32:120-130.
108. Zeng T., Bett G.C., Sachs F. Stretch-activated whole cell currents in adult rat cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 2000, 278:H548-H557.
109. Zhao Z., Wen H., Fefelova N., Allen C., Baba A., Matsuda T., Xie L.H. Revisiting the ionic mechanisms of early afterdepolarizations in cardiomyocytes: predominant by Ca waves or Ca currents?. Am. J. Physiol. Heart Circ. Physiol. 2012, 302:H1636-H1644.
110. Zipes D.P. The long QT interval syndrome. a Rosetta stone for sympathetic related ventricular tachyarrhythmias. Circulation 1991, 84:1414-1419.
111. NaCa contributes to electrical heterogeneity within the canine ventricle. Am. J. Physiol. Heart Circ. Physiol. 2000, 278:H1671-H1678.
112. Cl(Ca) contribute to isoproterenol-induced delayed after depolarizations in midmyocardial cells. Am. J. Phys. 1998, 275:H1979-H1992.