International Journal of Cardiology 174 (2014) 227–229
Contents lists available at ScienceDirect
International Journal of Cardiology journal homepage: www.elsevier.com/locate/ijcard
Editorial
Left ventricular noncompaction cardiomyopathy: Three decades of progress Tsung O. Cheng, M.D. ⁎ Department of Medicine, The George Washington University, Washington, DC, United States
a r t i c l e
i n f o
Article history: Received 10 March 2014 Accepted 31 March 2014 Available online 8 April 2014 Keywords: Noncompaction Cardiomyopathy Echocardiography
Left ventricular noncompaction cardiomyopathy (LVNC), which began first as an interesting autopsy finding nearly half of a century ago [1,2] and then became an echocardiographic curiosity [3] three decades ago, has become a rather common finding in living subjects in the 21st century with the introduction of various newer cardiovascular imaging modalities in addition to echocardiography, including cardiac magnetic resonance imaging (cMRI), computed tomography (CT) and invasive contrast ventriculography [4]. It describes a spongy appearance of the myocardium, instead of a normal compact myocardium (Fig. 1). It can occur in isolation [5] or coexist with other cardiovascular and/or systemic diseases [6]. During normal embryological development, the heart consists of a spongy network of muscle fibers and trabeculae that are separated by recesses that link the myocardium to the left ventricular cavity [6]. Blood is supplied to the myocardium through the intertrabecular spaces. During 5–8 weeks of normal human fetal development, the ventricular myocardium undergoes compaction with transformation of the intertrabecular spaces into capillaries, and the residual spaces within the trabecular meshwork then disappear. The process starts from the epicardium to the endocardium and from the base of the heart to its apex. In LVNC, there is persistence of trabeculation and deep recesses communicating with the ventricular cavity due to noncompaction. The exact cause for the persistence of these deep trabeculations is unknown. ⁎ Department of Medicine, The George Washington University Medical Center, 2150 Pennsylvania Avenue, N.W., Washington, DC 20037, United States. Tel.: +202 741 2426; fax: +202 741 2324. E-mail address: [email protected].
http://dx.doi.org/10.1016/j.ijcard.2014.03.208 0167-5273/© 2014 Elsevier Ireland Ltd. All rights reserved.
Diagnosing LVNC is a challenge for the medical profession. Echocardiography used in routine clinical practice can be overly sensitive and lacks specificity with the presently defined measurements and ratios used to diagnose LVNC [4]. In this regard, speckle-tracking echocardiography, in which left ventricular twist is determined, has some promise [4]. Whereas transthoracic echocardiography will likely remain the initial screening modality, questionable findings and clinical presentations suspicious for LVNC should be followed up with cMRI for definitive diagnosis and subsequent treatment [7–12]. On the other hand, the diagnosis of LVNC may sometimes be missed by some senior cardiologists who were either unfamiliar with this disease of recent fame or trained before the era of modern echocardiography. A recent letter-to-the-editor published in this journal, entitled “Unrecognized noncompaction on the internet” [13] pointed out an image of LVNC, which was presented in two different publications without being identified as an example of LVNC. The diagnosis of LVNC could also be an incidental finding on a chest CT angiogram performed to rule out pulmonary embolism [14]. Although LVNC is primarily a disease of the left ventricle (LV), associated involvement of the right ventricle (RV) has been described. Jennie et al. [15] reported biventricular noncompaction in 1986, although an even earlier report by Feldt et al. in 1969 [2] had already described the angiocardiographic as well as the autopsy findings of such a heart as biventricular, bizarre, spongy myocardial pattern. Several recent reports [12,16] have described associated involvement of RV in 15–41% of patients with LVNC. This high variability is likely related to the suboptimal echocardiographic visualization of the RV; the high spatial resolution of cMRI may be of potential clinical value in producing a more accurate and reproducible evaluation of the RV [12]. However, the diagnosis of noncompaction of the RV may still be troublesome, because of the absence of specific criteria for the diagnosis of involvement of the RV in LVNC and because various degrees of trabeculation are commonly observed even in normal hearts [12]. Nucifora et al. [12], using strict criteria proposed in previous histopathological studies, identified noncompaction in the RV in only 9% of patients with LVNC. Isolated noncompaction of the RV in the adult population has never been reported with the possible exception of one case reported by Chiribiri et al. [17] in 2009. However, with the growing use of cMRI, the identification of such a rarity may be possible [17]. Because LVNC is a genetically heterogeneous disorder, as described by my colleagues from China in this issue [18], it can be associated with other anomalies including hypertrophic cardiomyopathy (HCM), making the correct diagnosis very important for both long-term management and screening of living relatives [4,6,7,19]. Although most
228
Editorial
Fig. 1. Normal heart with a compact myocardium (left) compared with a heart with noncompaction cardiomyopathy showing hypertrabeculations and deep recesses that communicate with the left ventricular cavity (right). Images courtesy of William C. Roberts, M.D., Baylor Heart and Vascular Institute, Baylor University Medical Center, Dallas, TX.
patients with LVNC are often asymptomatic and the diagnosis may often be incidental [14,20], it is not always a benign condition. A 2011 publication [21], which was based on a comprehensive computerized search, reported an annual event rate of 4% for cardiovascular deaths, 6.2% for cardiovascular death and its surrogates (heart transplantation and appropriate implantable cardioverter-defibrillator shocks), and 8.6% for all cardiovascular events (death, stroke, implantable cardioverterdefibrillator shocks and heart transplantation). The seriousness of this disease was further supported by a recent report from China [22], which included 106 adult patients diagnosed with LVNC between 2003 and 2012 and indicated that advanced heart failure, left heart dilatation with systolic dysfunction, pulmonary hypertension and right bundle branch block are all predictors of adverse outcomes, and a quarter of the patients either died or underwent heart transplantation. Although LVNC has gained increasing attention in recent years, there are still many physicians, internists, cardiologists and even echocardiographers who may not be familiar with this disease. Disease unfamiliarity is one reason why LVNC may be still overlooked nowadays [23]. Although LVNC is usually congenital in origin, it rarely may be acquired [24–26]. Because symptomatic LVNC is a treatable disease, its early recognition and appropriate treatment are of paramount importance. Finally, the association of LVNC with HCM in a Chinese family as reported in this issue [18] has very important clinical implications. The significance of these possible concomitant cardiomyopathies is not well understood at the present time. The underlying genotype in the patients with HCM seems to have the genetic potential to phenotypically express as two distinct cardiomyopathies in one heart [27]. These unique combinations appear to represent the epitome of genetic heterogeneity; we as cardiologists must intensify our effort in searching for clinical, genetic and imaging links to ascertain the common derivative, which accounts for the concomitant occurrence in the same patient or family of these two distinct cardiomyopathies — the relatively uncommon LVNC and the relatively common HCM [28]. Acknowledgment I certify that I comply with the Principles of Ethical Publishing in the International Journal of Cardiology. References [1] Finsterer J, Zarrouk-Mahjoub S. Grant et al. 1926 did not provide the first description of left ventricular hypertrabeculation/noncompaction. Int J Cardiol 2013;169:e51–2.
[2] Feldt RH, Rahimtoola SH, Davis GD, Swan HJC, Titus JL. Anomalous ventricular myocardial patterns in a child with complex congenital heart disease. Am J Cardiol 1969;23:732–4. [3] Engberding R, Bender F. Identification of a rare congenital anomaly of the myocardium by two-dimensional echocardiography: persistence of isolated myocardial sinusoids. Am J Cardiol 1984;53:1733–4. [4] Paterick TE, Umland MM, Jan MF, et al. Left ventricular noncompaction: a 25-year odyssey. J Am Soc Echocardiogr 2012;25:363–75. [5] Chin TK, Perloff JK, Williams RG, Jue K, Mohrmann R. Isolated noncompaction of left ventricular myocardium. A study of eight cases. Circulation 1990;82:507–13. [6] Udeoji DU, Philip KJ, Morrissey RP, Phan A, Schwarz ER. Left ventricular noncompaction cardiomyopathy: updated review. Ther Adv Cardiovasc Dis 2013;7(5):260–73. [7] Summers J, Mikolich B. Left ventricular noncompaction: a cardiomyopathy with distinct characteristics and risks. J Cardiovasc Nurs Nov 13 2013 [Epub ahead of print]. [8] Peterson SE, Selvanayagam JB, Wiesmann F, et al. Left ventricular non-compaction: insights from cardiovascular magnetic resonance imaging. J Am Coll Cardiol 2005;46:101–5. [9] Dursun M, Agayev A, Nisli K, et al. MR imaging features of ventricular noncompaction: emphasis on distribution and pattern of fibrosis. Eur J Radiol 2010;74:147–51. [10] Cheng H, Zhao S, Jiang S, et al. Comparison of cardiac magnetic resonance imaging features of isolated left ventricular non-compaction in adults versus dilated cardiomyopathy in adults. Clin Radiol 2011;66:853–60. [11] Shemisa K, Li J, Tam M, Barcena J. Left ventricular noncompaction cardiomyopathy. Cardiovasc Diagn Ther 2013;3(3):170–5. [12] Nucifora G, Aquaro GD, Masci PG, Pingitore A, Lombardi M. Magnetic resonance assessment of prevalence and correlates of right ventricular abnormalities in isolated left ventricular noncompaction. Am J Cardiol 2014;113:142–6. [13] Finsterer J, Stöllberger C. Unrecognized noncompaction on the internet. Int J Cardiol 2011;152:e42–3. [14] Dubourg B, D'Heré B, de Vecchi C, et al. Incidental diagnosis of a familial left ventricular noncompaction on a chest CT angiography. Diagn Intervent Imaging 2014;95:91–3. [15] Jenni R, Goebel N, Tartini R, Schneider J, Arbenz U, Oelz O. Persisting myocardial sinusoids of both ventricles as an isolated anomaly: echocardiographic, angiographic and pathologic anatomical findings. Cardiovasc Intervent Radiol 1986;9(3):127–31. [16] Said S, Cooper CJ, Quevedo K, Rodriguez E, Hernandez GT. Biventricular noncompaction with predominant right ventricular involvement, reduced left ventricular systolic and diastolic function, and pulmonary hypertension in a Hispanic male. Am J Case Rep 2013;14:539–42. [17] Chiribiri A, Leuzzi S, Salvetti J, et al. Isolated noncompaction of the right ventricular myocardium in the adulthood? Int J Cardiol 2009;134:e17–9. [18] Yuan L, Xie M, Cheng TO, et al. Left ventricular noncompaction associated with hypertrophic cardiomyopathy: echocardiographic diagnosis and genetic analysis of a new pedigree in China. Int J Cardiol 2014;174:249–59. [19] Murphy RT, Thaman R, Blanes JG, et al. Natural history and familial characteristics of isolated left ventricular non-compaction. Eur Heart J 2005;26:187–92. [20] Arbustini E, Narula N, Dec GW, et al. The MOGE(S) classification for a phenotype– genotype nomenclature of cardiomyopathy: endorsed by the World Heart Federation. J Am Coll Cardiol 2013;62:2046–72. [21] Bhatia NL, Tajik AJ, Wilansky S, Steidley DE, Mookadam F. Isolated noncompaction of the left ventricular myocardium in adults: a systematic overview. J Card Fail 2011;17:771–8. [22] Tian T, Liu Y, Gao L, et al. Isolated left ventricular noncompaction: clinical profile and prognosis in 106 adult patients. Heart Vessels Oct 2 2013 [Epub ahead of print].
Editorial [23] Anderson RH. Ventricular non-compaction — a frequently ignored finding? Eur Heart J 2008;29:10–1. [24] Finsterer J, Stöllberger C, Schubert B. Acquired left ventricular noncompaction as a cardiac manifestation of neuromuscular disorders. Scand Cardiovasc J 2008;42:25–30. [25] Finsterer J, Dumser M. Noncompaction in a septic heart, missed on echocardiography. Int J Cardiol 2014;171:e70–1. [26] Finsterer J, Stöllberger C. Acquired/hidden noncompaction in metabolic encephalopathy with nonconvulsive epileptic state. Int J Cardiol 2014;172:e341–3.
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[27] Paterick TE, Tercius AJ, Agarwal A, Treiber SC, Khandheria BK, Tajik AJ. Double jeopardy in the echocardiographic laboratory: coexistence of two distinct cardiomyopathies? Echocardiography Jan 21 2014. http://dx.doi.org/10.1111/ echo.12502. [28] Maron BJ. Recognition of hypertrophic cardiomyopathy as a contemporary, relatively common, and treatable disease (from the International Summit V). Am J Cardiol 2014;113:739–44.
Contents lists available at ScienceDirect
International Journal of Cardiology journal homepage: www.elsevier.com/locate/ijcard
Editorial
Left ventricular noncompaction cardiomyopathy: Three decades of progress Tsung O. Cheng, M.D. ⁎ Department of Medicine, The George Washington University, Washington, DC, United States
a r t i c l e
i n f o
Article history: Received 10 March 2014 Accepted 31 March 2014 Available online 8 April 2014 Keywords: Noncompaction Cardiomyopathy Echocardiography
Left ventricular noncompaction cardiomyopathy (LVNC), which began first as an interesting autopsy finding nearly half of a century ago [1,2] and then became an echocardiographic curiosity [3] three decades ago, has become a rather common finding in living subjects in the 21st century with the introduction of various newer cardiovascular imaging modalities in addition to echocardiography, including cardiac magnetic resonance imaging (cMRI), computed tomography (CT) and invasive contrast ventriculography [4]. It describes a spongy appearance of the myocardium, instead of a normal compact myocardium (Fig. 1). It can occur in isolation [5] or coexist with other cardiovascular and/or systemic diseases [6]. During normal embryological development, the heart consists of a spongy network of muscle fibers and trabeculae that are separated by recesses that link the myocardium to the left ventricular cavity [6]. Blood is supplied to the myocardium through the intertrabecular spaces. During 5–8 weeks of normal human fetal development, the ventricular myocardium undergoes compaction with transformation of the intertrabecular spaces into capillaries, and the residual spaces within the trabecular meshwork then disappear. The process starts from the epicardium to the endocardium and from the base of the heart to its apex. In LVNC, there is persistence of trabeculation and deep recesses communicating with the ventricular cavity due to noncompaction. The exact cause for the persistence of these deep trabeculations is unknown. ⁎ Department of Medicine, The George Washington University Medical Center, 2150 Pennsylvania Avenue, N.W., Washington, DC 20037, United States. Tel.: +202 741 2426; fax: +202 741 2324. E-mail address: [email protected].
http://dx.doi.org/10.1016/j.ijcard.2014.03.208 0167-5273/© 2014 Elsevier Ireland Ltd. All rights reserved.
Diagnosing LVNC is a challenge for the medical profession. Echocardiography used in routine clinical practice can be overly sensitive and lacks specificity with the presently defined measurements and ratios used to diagnose LVNC [4]. In this regard, speckle-tracking echocardiography, in which left ventricular twist is determined, has some promise [4]. Whereas transthoracic echocardiography will likely remain the initial screening modality, questionable findings and clinical presentations suspicious for LVNC should be followed up with cMRI for definitive diagnosis and subsequent treatment [7–12]. On the other hand, the diagnosis of LVNC may sometimes be missed by some senior cardiologists who were either unfamiliar with this disease of recent fame or trained before the era of modern echocardiography. A recent letter-to-the-editor published in this journal, entitled “Unrecognized noncompaction on the internet” [13] pointed out an image of LVNC, which was presented in two different publications without being identified as an example of LVNC. The diagnosis of LVNC could also be an incidental finding on a chest CT angiogram performed to rule out pulmonary embolism [14]. Although LVNC is primarily a disease of the left ventricle (LV), associated involvement of the right ventricle (RV) has been described. Jennie et al. [15] reported biventricular noncompaction in 1986, although an even earlier report by Feldt et al. in 1969 [2] had already described the angiocardiographic as well as the autopsy findings of such a heart as biventricular, bizarre, spongy myocardial pattern. Several recent reports [12,16] have described associated involvement of RV in 15–41% of patients with LVNC. This high variability is likely related to the suboptimal echocardiographic visualization of the RV; the high spatial resolution of cMRI may be of potential clinical value in producing a more accurate and reproducible evaluation of the RV [12]. However, the diagnosis of noncompaction of the RV may still be troublesome, because of the absence of specific criteria for the diagnosis of involvement of the RV in LVNC and because various degrees of trabeculation are commonly observed even in normal hearts [12]. Nucifora et al. [12], using strict criteria proposed in previous histopathological studies, identified noncompaction in the RV in only 9% of patients with LVNC. Isolated noncompaction of the RV in the adult population has never been reported with the possible exception of one case reported by Chiribiri et al. [17] in 2009. However, with the growing use of cMRI, the identification of such a rarity may be possible [17]. Because LVNC is a genetically heterogeneous disorder, as described by my colleagues from China in this issue [18], it can be associated with other anomalies including hypertrophic cardiomyopathy (HCM), making the correct diagnosis very important for both long-term management and screening of living relatives [4,6,7,19]. Although most
228
Editorial
Fig. 1. Normal heart with a compact myocardium (left) compared with a heart with noncompaction cardiomyopathy showing hypertrabeculations and deep recesses that communicate with the left ventricular cavity (right). Images courtesy of William C. Roberts, M.D., Baylor Heart and Vascular Institute, Baylor University Medical Center, Dallas, TX.
patients with LVNC are often asymptomatic and the diagnosis may often be incidental [14,20], it is not always a benign condition. A 2011 publication [21], which was based on a comprehensive computerized search, reported an annual event rate of 4% for cardiovascular deaths, 6.2% for cardiovascular death and its surrogates (heart transplantation and appropriate implantable cardioverter-defibrillator shocks), and 8.6% for all cardiovascular events (death, stroke, implantable cardioverterdefibrillator shocks and heart transplantation). The seriousness of this disease was further supported by a recent report from China [22], which included 106 adult patients diagnosed with LVNC between 2003 and 2012 and indicated that advanced heart failure, left heart dilatation with systolic dysfunction, pulmonary hypertension and right bundle branch block are all predictors of adverse outcomes, and a quarter of the patients either died or underwent heart transplantation. Although LVNC has gained increasing attention in recent years, there are still many physicians, internists, cardiologists and even echocardiographers who may not be familiar with this disease. Disease unfamiliarity is one reason why LVNC may be still overlooked nowadays [23]. Although LVNC is usually congenital in origin, it rarely may be acquired [24–26]. Because symptomatic LVNC is a treatable disease, its early recognition and appropriate treatment are of paramount importance. Finally, the association of LVNC with HCM in a Chinese family as reported in this issue [18] has very important clinical implications. The significance of these possible concomitant cardiomyopathies is not well understood at the present time. The underlying genotype in the patients with HCM seems to have the genetic potential to phenotypically express as two distinct cardiomyopathies in one heart [27]. These unique combinations appear to represent the epitome of genetic heterogeneity; we as cardiologists must intensify our effort in searching for clinical, genetic and imaging links to ascertain the common derivative, which accounts for the concomitant occurrence in the same patient or family of these two distinct cardiomyopathies — the relatively uncommon LVNC and the relatively common HCM [28]. Acknowledgment I certify that I comply with the Principles of Ethical Publishing in the International Journal of Cardiology. References [1] Finsterer J, Zarrouk-Mahjoub S. Grant et al. 1926 did not provide the first description of left ventricular hypertrabeculation/noncompaction. Int J Cardiol 2013;169:e51–2.
[2] Feldt RH, Rahimtoola SH, Davis GD, Swan HJC, Titus JL. Anomalous ventricular myocardial patterns in a child with complex congenital heart disease. Am J Cardiol 1969;23:732–4. [3] Engberding R, Bender F. Identification of a rare congenital anomaly of the myocardium by two-dimensional echocardiography: persistence of isolated myocardial sinusoids. Am J Cardiol 1984;53:1733–4. [4] Paterick TE, Umland MM, Jan MF, et al. Left ventricular noncompaction: a 25-year odyssey. J Am Soc Echocardiogr 2012;25:363–75. [5] Chin TK, Perloff JK, Williams RG, Jue K, Mohrmann R. Isolated noncompaction of left ventricular myocardium. A study of eight cases. Circulation 1990;82:507–13. [6] Udeoji DU, Philip KJ, Morrissey RP, Phan A, Schwarz ER. Left ventricular noncompaction cardiomyopathy: updated review. Ther Adv Cardiovasc Dis 2013;7(5):260–73. [7] Summers J, Mikolich B. Left ventricular noncompaction: a cardiomyopathy with distinct characteristics and risks. J Cardiovasc Nurs Nov 13 2013 [Epub ahead of print]. [8] Peterson SE, Selvanayagam JB, Wiesmann F, et al. Left ventricular non-compaction: insights from cardiovascular magnetic resonance imaging. J Am Coll Cardiol 2005;46:101–5. [9] Dursun M, Agayev A, Nisli K, et al. MR imaging features of ventricular noncompaction: emphasis on distribution and pattern of fibrosis. Eur J Radiol 2010;74:147–51. [10] Cheng H, Zhao S, Jiang S, et al. Comparison of cardiac magnetic resonance imaging features of isolated left ventricular non-compaction in adults versus dilated cardiomyopathy in adults. Clin Radiol 2011;66:853–60. [11] Shemisa K, Li J, Tam M, Barcena J. Left ventricular noncompaction cardiomyopathy. Cardiovasc Diagn Ther 2013;3(3):170–5. [12] Nucifora G, Aquaro GD, Masci PG, Pingitore A, Lombardi M. Magnetic resonance assessment of prevalence and correlates of right ventricular abnormalities in isolated left ventricular noncompaction. Am J Cardiol 2014;113:142–6. [13] Finsterer J, Stöllberger C. Unrecognized noncompaction on the internet. Int J Cardiol 2011;152:e42–3. [14] Dubourg B, D'Heré B, de Vecchi C, et al. Incidental diagnosis of a familial left ventricular noncompaction on a chest CT angiography. Diagn Intervent Imaging 2014;95:91–3. [15] Jenni R, Goebel N, Tartini R, Schneider J, Arbenz U, Oelz O. Persisting myocardial sinusoids of both ventricles as an isolated anomaly: echocardiographic, angiographic and pathologic anatomical findings. Cardiovasc Intervent Radiol 1986;9(3):127–31. [16] Said S, Cooper CJ, Quevedo K, Rodriguez E, Hernandez GT. Biventricular noncompaction with predominant right ventricular involvement, reduced left ventricular systolic and diastolic function, and pulmonary hypertension in a Hispanic male. Am J Case Rep 2013;14:539–42. [17] Chiribiri A, Leuzzi S, Salvetti J, et al. Isolated noncompaction of the right ventricular myocardium in the adulthood? Int J Cardiol 2009;134:e17–9. [18] Yuan L, Xie M, Cheng TO, et al. Left ventricular noncompaction associated with hypertrophic cardiomyopathy: echocardiographic diagnosis and genetic analysis of a new pedigree in China. Int J Cardiol 2014;174:249–59. [19] Murphy RT, Thaman R, Blanes JG, et al. Natural history and familial characteristics of isolated left ventricular non-compaction. Eur Heart J 2005;26:187–92. [20] Arbustini E, Narula N, Dec GW, et al. The MOGE(S) classification for a phenotype– genotype nomenclature of cardiomyopathy: endorsed by the World Heart Federation. J Am Coll Cardiol 2013;62:2046–72. [21] Bhatia NL, Tajik AJ, Wilansky S, Steidley DE, Mookadam F. Isolated noncompaction of the left ventricular myocardium in adults: a systematic overview. J Card Fail 2011;17:771–8. [22] Tian T, Liu Y, Gao L, et al. Isolated left ventricular noncompaction: clinical profile and prognosis in 106 adult patients. Heart Vessels Oct 2 2013 [Epub ahead of print].
Editorial [23] Anderson RH. Ventricular non-compaction — a frequently ignored finding? Eur Heart J 2008;29:10–1. [24] Finsterer J, Stöllberger C, Schubert B. Acquired left ventricular noncompaction as a cardiac manifestation of neuromuscular disorders. Scand Cardiovasc J 2008;42:25–30. [25] Finsterer J, Dumser M. Noncompaction in a septic heart, missed on echocardiography. Int J Cardiol 2014;171:e70–1. [26] Finsterer J, Stöllberger C. Acquired/hidden noncompaction in metabolic encephalopathy with nonconvulsive epileptic state. Int J Cardiol 2014;172:e341–3.
229
[27] Paterick TE, Tercius AJ, Agarwal A, Treiber SC, Khandheria BK, Tajik AJ. Double jeopardy in the echocardiographic laboratory: coexistence of two distinct cardiomyopathies? Echocardiography Jan 21 2014. http://dx.doi.org/10.1111/ echo.12502. [28] Maron BJ. Recognition of hypertrophic cardiomyopathy as a contemporary, relatively common, and treatable disease (from the International Summit V). Am J Cardiol 2014;113:739–44.
