- Email: [email protected]
Effects of Weight Loss After Gastric Bypass on Right and Left Ventricular Function Assessed by Tissue Doppler Imaging
treated because of the 3-dimensional shape of the patch. The absence of wires and soft material (polyurethane) were responsible for the absence of any long-term aortic insufficiency. As noted in the patient with aortic cusp prolapse, the patch was effective, even if the balloon caused aortic insufficiency; however, we cannot generalize on the basis of a single case. We were puzzled about the etiology of ventricular fibrillation in 1 patient despite the favorable outcome. Electrical or electromechanical causes could be responsible, because with repeat inflation of the balloon patch, there was a good outcome. The main disadvantage was the need for relative long immobilization. However, accelerated fibrin formation principles can be applied to selective cases. Such cases include relatively small VSDs with aneurysm of the membranous septum and multipoint patch attachment. The choice of the patch release time in the regular case (48 hours) or the accelerated cases (23 hours) was based on experimental observations in animals; it takes only 6 to 8 hours for accelerated patch release for patent foramen ovale and left atrial appendage occlusion in piglets.9 Our research efforts are focused on further acceleration of the patch release time using fibrin or surgical adhesives.10 Most surgical VSD cases are infants. Unfortunately, the transcatheter patch in its current form is too
bulky to be used in young infants. It is conceivable that older infants weighing ⬎6 kg, with a VSD diameter ⬍11 mm, can undergo repair, providing that the test balloon occlusion is favorable. 1. King T, Mills N. Non-operataive closure of atrial septal defects. Surgery 1974;75:383–386. 2. Rashkind W, Cuaso C. Transcatheter treatment of congenital heart disease. Circulation 1983;67:711–716. 3. Sideris EB, Toumanides S, Macuil B, Gutierrez-Leonard H, Poursanov M, Sokolov A, Moulopoulos SD. Transcatheter patch correction of secundum atrial septal defects. Am J Cardiol 2002;89:1082–1086. 4. Lock JE, Block PC, McKay RG, Beim DS, Keane JF. Transcatheter closure of ventricular septal defects. Circulation 1988;78:361–368. 5. Rigby ML, Redington AN. Primary transcatheter closure of perimembranous ventricular septal defects. Br Heart J 1994;72:368 –371. 6. Sideris EB, Walsh KP, Haddad JL, Chen CR, Ren SG, Kulkarni H. Occlusion of congenital ventricular septal defects by the buttoned device. Heart 1997;77: 275–279. 7. Bass JL, Kaira GS, Arora R. Masura J, Gavora P. Thanopoulos BD, Torres W, Sievert H. Initial human experience with the Amplatzer perimembranous ventricular septal defect occluder device. Cathet Cardiovasc Interventions 2003;58: 238 –245. 8. Sideris EB Sideris CE, Stamatelopoulos SF, Moulopoulos SD. Transcatheter patch occlusion of experimental atrial septal defects. Cathet Cardiovasc Interventions 2002;57:404 – 410. 9. Sideris EB, Toumanides S, Sideris C, Moulopoulos SD. Accelerated transcatheter patch occlusion of heart defects: experimental findings. Cathet Cardiovasc Interventions 2004;62:93:32. 10. Sideris EB, Macuil B, Varvarenko V, Alekyan B. Outpatient transcatheter patch occlusion of large patent ductus arteriosus and perimembranous ventricular septal defect. Cathet Cardiovasc Interventions 2004;62:140:7.
Effects of Weight Loss After Gastric Bypass on Right and Left Ventricular Function Assessed by Tissue Doppler Imaging Howard J. Willens, MD, Simon C. Chakko, MD, Patricia Byers, MD, Julio A. Chirinos, MD, Eugenio Labrador, RDCS, Juan C. Castrillon, RDCS, and Maureen H. Lowery, MD To evaluate the effects of substantial weight loss on tissue Doppler imaging parameters of right ventricular (RV) and left ventricular (LV) systolic and diastolic function, we performed standard echocardiography and tissue Doppler imaging in 17 patients with severe obesity before and after gastric bypass. Patients lost 39 ⴞ 10 kg over 7.6 ⴞ 3.6 months. Adjusted LV mass decreased (134 ⴞ 41 to 119 ⴞ 31 kg/m, p ⴝ 0.031). After weight loss, the ratios of early-to-late diastolic mitral and tricuspid inflow velocities increased (1.3 ⴞ 0.2 to 1.6 ⴞ 0.5, p ⴝ 0.02; 1.0 ⴞ 0.1 to 1.6 ⴞ 0.3, p ⴝ 0.003). Early diastolic tissue Doppler velocities increased at both the lateral and septal mitral annulus (7.6 ⴞ 1.5 to 9.3 ⴞ 2.5 cm/s, p ⴝ 0.009; and 6.6 ⴞ From the Department of Medicine, Division of Cardiology, and Department of Surgery, University of Miami School of Medicine, Miami, Florida. Dr. Willens’ address is: 3513 Greenleaf Circle, Hollywood, Florida 33021-8437. E-mail: [email protected]. Manuscript received December 9, 2004; revised manuscript received and accepted February 11, 2005. ©2005 by Excerpta Medica Inc. All rights reserved. The American Journal of Cardiology Vol. 95 June 15, 2005
1.4 to 7.7 ⴞ 1.7 cm/s; p ⴝ 0.028, respectively) and for their 2-site average (7.2 ⴞ 1.0 to 8.5 ⴞ 1.7 cm/s, p ⴝ 0.007). Early diastolic tricuspid annular velocity increased (7.2 ⴞ 2.8 to 10.6 ⴞ 2.3 cm/s, p <0.001) as did the ratio of early-to-late tricuspid annular diastolic velocity (0.9 ⴞ 0.4 to 1.1 ⴞ 0.2, p ⴝ 0.038). Tricuspid annular systolic velocity increased (8.6 ⴞ 2.5 to 10.3 ⴞ 2.7 cm/s, p ⴝ 0.037). In patients with severe obesity, significant weight loss results in an increase in tricuspid annular systolic and early diastolic velocities and mitral annular early diastolic velocities. 䊚2005 by Excerpta Medica Inc. (Am J Cardiol 2005;95:1521–1524)
besity is associated with multiple cardiopulmonary symptoms and an increased risk of develO oping heart failure. Although weight loss is routinely 1
2
recommended to improve symptoms and decrease risk, the effects of weight loss on cardiac function and the role these effects have on improving symptoms 0002-9149/05/$–see front matter doi:10.1016/j.amjcard.2005.02.029
1521
research protocol, and all patients gave informed consent. Parameter Presurgical Postsurgical Change Clinical and demographic data were obtained by chart review, interWeight (kg) 160 ⫾ 43 121 ⫾ 43* ⫺39 view, and physical examination. The 54 ⫾ 11 40 ⫾ 11* ⫺14 BMI (kg/m2) Heart rate at rest (beats/min) 82 ⫾ 16 70 ⫾ 12† ⫺12 presence of sleep apnea was deterSystolic blood pressure (mm Hg) 145 ⫾ 17 134 ⫾ 17‡ ⫺9 mined by diagnostic polysomnogra† Diastolic blood pressure (mm Hg) 84 ⫾ 12 77 ⫾ 12 ⫺7 phy. Values are expressed as mean ⫾ SD. All subjects underwent complete *p ⬍0.001; †p ⫽ 0.001; ‡p ⫽ 0.012. 2-dimensional echocardiography and tissue Doppler imaging before and 7.4 ⫾ 3.6 months (range 3 to 15) after surgery. Standard echocardioTABLE 2 Two-dimensional and Doppler Echocardiographic Data graphic views were obtained in the Presurgical Postsurgical left lateral decubitus position using Parameter (n ⫽ 17) (n ⫽ 17) p Values commercially available equipment LV end-diastolic diameter (cm) 5.2 ⫾ 0.7 5.0 ⫾ 0.6 0.855 (Vivid 7, GE-Vingmed, Horten, NorLeft atrium (cm) 3.5 ⫾ 0.5 3.7 ⫾ 0.4 0.397 way) after 10 minutes of rest in the Septal wall thickness (cm) 1.2 ⫾ 0.2 1.1 ⫾ 0.2 0.238 supine position. Harmonic imaging Posterior wall thickness (cm) 1.1 ⫾ 0.2 1.0 ⫾ 0.2 0.064 was used in all patients, and LV LV mass index (g/m) 134 ⫾ 41 119 ⫾ 31 0.031 opacification with a contrast agent LV fractional shortening (%) 35 ⫾ 8 32 ⫾ 5 0.198 RV end-diastolic diameter (cm) 3.1 ⫾ 0.5 3.1 ⫾ 0.7 0.895 was used as needed to improve enEarly mitral inflow (cm/s) 94 ⫾ 22 87 ⫾ 16 0.048 docardial definition. Beta-adrenergic Late mitral inflow (cm/s) 73 ⫾ 14 60 ⫾ 17 0.031 and calcium antagonists were withEarly/late diastolic mitral inflow 1.3 ⫾ 0.2 1.6 ⫾ 0.5 0.02 held for 24 hours before the study. Deceleration time (ms) 194 ⫾ 29 181 ⫾ 30 0.302 Early/late tricuspid inflow (n ⫽ 8) 1.0 ⫾ 0.1 1.6 ⫾ 0.3 0.002 One investigator performed all Pulmonary artery systolic pressure (mm Hg) 32 ⫾ 9 32 ⫾ 8 0.58 echocardiographic and tissue Dopp(n ⫽ 8) ler imaging analyses. LV internal diValues are expressed as mean ⫾ SD. mensions and wall thickness were measured from 2-dimensional, guided, M-mode echocardiographic and prognosis have not been fully documented.3,4 Re- tracings obtained at mid-chordal level in the parastercently, tissue Doppler imaging has been shown to be nal short-axis view according to American Society of more sensitive than standard echocardiography for Echocardiography criteria.9 Left atrial internal dimendetecting subclinical right ventricular (RV) and left sion at end-systole and RV internal dimension at endventricular (LV) dysfunction in patients with obesi- diastole were measured in the parasternal long-axis ty.5– 8 In addition, tissue Doppler imaging does not view. The average of 2 measurements was recorded depend on endocardial definition and is less affected for all parameters. LV mass was calculated according by chest wall attenuation than standard echocardiog- to the previously described method of Devereux et al10 raphy. Therefore, in obese patients who may be chal- and normalized to height in meters. Percent fractional lenging to image, sequential tissue Doppler imaging shortening was calculated as a measure of LV systolic may be a more accurate and reproducible technique function. than standard echocardiography for investigating Mitral and tricuspid inflow velocities were obchanges in cardiac function resulting from weight tained by pulse-wave Doppler in the apical 4-chamber loss. This study examines the effects of significant view. The peak early and late diastolic mitral and weight loss after gastric bypass surgery on RV and LV tricuspid inflow velocities were measured and aversystolic and diastolic function in patients with severe aged over 5 cardiac cycles during normal respiration. obesity using conventional echocardiography and tis- The mitral deceleration time was also measured. The sue Doppler imaging. ratio of early diastolic-to-late diastolic inflow velocities was calculated for both the mitral and tricuspid ••• Candidates for this study were patients who had valves. Pulmonary artery systolic pressure was estiundergone stress echocardiography before undergoing mated by adding 10 mm Hg to the transtricuspid long-limb Roux-en-Y gastric bypass for severe obe- pressure gradient. Color tissue Doppler imaging was performed from sity (body mass index [BMI] ⬎40 kg/m2 or ⬎35 kg/m2 plus co-morbidities). Subjects also agreed to the apical 4-chamber view using a 2.5-MHz transundergo echocardiography after achieving substantial ducer and frame rates of ⱖ80/s, and the images were weight loss. Patients with a history of heart failure, digitized. Images of the right and left ventricle were coronary artery disease, atrial fibrillation, left bundle carefully chosen to minimize the angle of incidence branch block, significant valve disease, positive stress between the scan lines and motion of the base of the test results, regional wall motion abnormalities, can- heart for both the pre- and postsurgical studies. Mean cer, and kidney or liver disease were excluded. The myocardial velocity profiles were derived and anainstitutional review board of our facility approved the lyzed off-line using commercially available computer TABLE 1 Pre- and Postsurgical Clinical Parameters
1522 THE AMERICAN JOURNAL OF CARDIOLOGY姞
VOL. 95
JUNE 15, 2005
annular velocity by tissue Doppler imaging, a measure of LV filling Presurgical Postsurgical pressure, was also calculated.11 Parameter (n ⫽ 17) (n ⫽ 17) p Values All echocardiographic, pulse-wave, and tissue Doppler variables are preLateral mitral annular systolic velocity (cm/s) 5.4 ⫾ 1.5 6.0 ⫾ 1.4 0.069 Septal mitral annular systolic velocity (cm/s) 5.7 ⫾ 1.2 5.9 ⫾ 1.2 0.620 sented as mean ⫾ SD. Pre- and postTwo-site average systolic velocity (cm/s) 5.6 ⫾ 1.2 6.0 ⫾ 1.2 0.218 surgical values were compared using Early diastolic lateral MAV (cm/s) 7.6 ⫾ 1.5 9.3 ⫾ 2.5 0.009 paired Student’s t-test. Pearson’s Late diastolic lateral MAV (cm/s) 5.4 ⫾ 1.5 5.7 ⫾ 1.5 0.447 correlation coefficient was used to Early/late diastolic lateral MAV ratio 1.5 ⫾ 0.4 1.7 ⫾ 0.4 0.229 Early diastolic septal MAV (cm/s) 6.6 ⫾ 1.4 7.7 ⫾ 1.7 0.028 explore univariate relations between Late diastolic septal MAV (cm/s) 6.4 ⫾ 2.4 6.5 ⫾ 1.2 0.852 changes in selected indexes of LV Early/late diastolic septal MAV ratio 1.1 ⫾ 0.5 1.2 ⫾ 0.3 0.572 and RV systolic and diastolic funcTwo-site average early diastolic velocity (cm/s) 7.2 ⫾ 1.0 8.5 ⫾ 1.7 0.007 tion and weight loss. A p value Early diastolic mitral inflow/lateral MAV ratio 12.3 ⫾ 4.0 10 ⫾ 3.3 0.01 ⬍0.05 was considered significant. Values are expressed as mean ⫾ SD. Statistical analysis was performed MAV ⫽ mitral annular velocity. using GraphPad Instat (GraphPad Software, Inc., San Diego, California). TABLE 4 Tissue Doppler Velocities in the Right Ventricle The study group consisted of 17 Presurgical Postsurgical patients (10 women and 7 men; mean Parameters (n ⫽ 17) (n ⫽ 17) p Values age 43 ⫾ 10 years). Ten patients had hypertension and 5 had diabetes melTricuspid annular systolic velocity (cm/s) 8.6 ⫾ 2.5 10.3 ⫾ 2.7 0.037 Early diastolic tricuspid annular velocity (cm/s) 7.2 ⫾ 2.8 10.6 ⫾ 2.3 ⬍0.001 litus. Obstructive sleep apnea was Late diastolic tricuspid annular velocity (cm/s) 8.7 ⫾ 2.1 10.2 ⫾ 2.4 0.227 present in 8 patients who were Early diastolic/late diastolic tricuspid annular 0.9 ⫾ 0.4 1.1 ⫾ 0.2 0.038 treated with continuous positive airvelocity ratio way pressure. Table 1 lists the effects Values are expressed as mean ⫾ SD. of surgery on mean weight, BMI, heart rate, and systolic and diastolic blood pressure. Mean heart rate and systolic and diastolic blood pressure significantly deTABLE 5 Correlations Between Amount of Weight Lost and creased with weight loss. Hypertension and diabetes Changes in Standard Doppler Echocardiographic and resolved in 3 patients, and obstructive sleep apnea Tissue Doppler Imaging Parameters resolved in 2. Two-dimensional echocardiographic Pearson’s images, pulse-wave Doppler mitral inflow, and tissue Parameters Coefficient (r) p Value Doppler imaging velocities were adequate for sequenLateral mitral annular early diastolic ⫹0.51 0.039 tial analysis before and after weight loss in all 17 velocity patients. Pulmonary artery systolic pressure and triEarly/late diastolic mitral inflow ⫹0.51 0.044 cuspid inflow were suitable for sequential analysis in Two-site average early diastolic tissue ⫹0.33 0.236 velocity 8 patients. Tricuspid annular early diastolic velocity ⫹0.34 0.233 Table 2 lists the effects of weight loss on selected Tricuspid annular systolic velocity ⫹0.16 0.575 2-dimensional and Doppler echocardiographic parameters. No significant changes in LV end-diastolic diameter, left atrial dimension, septal and posterior wall software (Echopac, GE-Vingmed) by placing a 6-mm thickness, fractional shortening, RV internal diameter, sample volume at the septal and lateral corners of the deceleration time, or pulmonary artery systolic presmitral annulus and lateral tricuspid annulus. The sam- sure were noted. LV mass indexed to height significantly decreased after weight loss. Although early and ple volume was manually repositioned during systole late mitral inflow velocities decreased after surgery, and early and late diastole to compensate for annular their ratio significantly increased. The ratio of early motion and maintain the sample volume in the area of diastolic-to-late diastolic tricuspid inflow velocities interest. also significantly increased in the 8 patients in whom Peak systolic and early and late diastolic tissue it could be measured. velocities were measured from the lateral and septal The effects of weight loss on tissue Doppler imagcorners of the mitral annulus and lateral tricuspid ing indexes of LV function are shown in Table 3. Peak annulus. The average of 3 consecutive cardiac cycles systolic velocities increased, but not significantly, at was recorded. The ratios of early-to-late diastolic tis- both the lateral and septal mitral annulus and for the sue Doppler velocities were calculated at all 3 annular 2-site average. Lateral and septal mitral annular early sites. In addition, the 2-site average peak systolic and diastolic tissue velocities significantly increased as did early diastolic velocities of the lateral and septal cor- their 2-site average. The ratio of early diastolic mitral ners of the mitral annulus were calculated. The ratio of inflow velocity to lateral mitral annular early diastolic peak early diastolic mitral inflow velocity by pulse- velocity significantly decreased. Table 4 lists the effects of weight loss on tissue wave Doppler to peak early diastolic lateral mitral TABLE 3 Tissue Doppler Velocities in the Left Ventricle
BRIEF REPORTS
1523
Doppler imaging indexes of RV function. Peak systolic and early diastolic tricuspid annular velocities significantly increased. The ratio of early-to-late diastolic tissue Doppler velocities at the tricuspid annulus significantly increased. Table 5 lists the results of Pearson’s correlation coefficients relating the change in selected Doppler echocardiographic and tissue Doppler imaging parameters after surgery with magnitude of weight loss. The increase in early diastolic lateral mitral annulus velocity and the ratio of early-to-late diastolic mitral inflow velocities significantly correlated with absolute amount of weight lost. •••
We obseved an increase in tricuspid annular systolic and early diastolic velocities and septal and lateral mitral annular early diastolic velocities in patients with severe obesity shortly after they achieved substantial weight loss with gastric bypass. These increases in mitral and tricuspid annnular velocities are consistent with subtle improvements in LV and RV diastolic function and RV systolic function.12 The tissue Doppler findings suggestive of improvement in LV and RV diastolic function are supported by the observed increase in the ratios of early diastolic to late diastolic mitral and tricuspid inflow velocities obtained with pulse-wave Doppler. Furthermore, the changes in pulse-wave and tissue Doppler indexes of LV diastolic function had a significant positive correlation with the amount of weight loss. This suggests that LV diastolic function may improve as more weight is lost. Additional observations in this study were a decrease in indexed LV mass and a reduction in peak early diastolic mitral inflow/peak early diastolic lateral mitral annular velocity ratio, suggesting a decrease in LV filling pressures. The finding of increased early diastolic mitral annular velocities suggestive of improved LV diastolic function after weight loss and the correlation of this increase with the amount of weight lost is consistent with previous studies that used standard Doppler to measure LV diastolic function in obese patients undergoing bariatric surgery.13–15 There have been few reports of the effects of obesity and subsequent weight loss on RV function. This scarcity of investigations may be due to difficulties imaging the right ventricle in obese patients16 and accurately evaluating global RV function noninvasively with echocardiography because of the chamber’s complex geometry.17 Evaluation of regional RV myocardial function by measuring tricuspid annular velocities with tissue Doppler imaging may therefore be particularly advantageous for understanding the effects of obesity and weight loss on RV function. Recently, 2 studies using tissue Doppler imaging to investigate RV function in obese patients reported impaired filling of the right ventricle.5,7 Our observation of increased early diastolic tricuspid annular velocities after gastric bypass is consistent with a recent report of improvement in a dif-
1524 THE AMERICAN JOURNAL OF CARDIOLOGY姞
VOL. 95
ferent tissue Doppler imaging parameter of RV diastolic function, RV relaxtion time, in patients achieving modest weight loss with diet and exercise.18 Our finding of an increase in tricuspid annular systolic velocities consistent with a subclinical improvement in RV systolic function has not been previously reported. Because tricuspid and mitral annular motion and velocity may be interdependent,19 our findings of increased tricuspid annular systolic and early diastolic velocities after weight loss must be interpreted with caution. 1. Sjostrom L, Larsson B, Backman L, Bengtsson C, Bouchard C, Dahlgren S, Hallgren P, Jonsson E, Karlsson J, Lapidus L. Swedish obese subjects (SOS): recruitment for an intervention study and a selected description of the obese state. Int J Obes Relat Metab Disord 1992;16:465– 479. 2. Kenchaiah S, Evans JC, Levy D, Wilson PWF, Benjamin EJ, Larson MG, Kannel WB, Vasan RS. Obesity and the risk of heart failure. N Engl J Med 2002;347:305–313. 3. Karason K, Lindroos AK, Stenlof K, Sjostrom L. Relief of respiratory symptoms and increased physical activity after surgically induced weight loss-results from the Swedish Obese Subjects study. Arch Intern Med 2000;160:1797–1802. 4. Alpert MA. Management of obesity cardiomyopathy. Am J Med Sci 2001;321: 237–241. 5. Willens HJ, Chakko SC, Lowery MH, Byers P, Labrador E, Gallagher A, Castrillon JC, Myerburg RJ. Tissue Doppler imaging of the right and left ventricle in severe obesity (body mass index ⬎35 kg/m2). Am J Cardiol 2004; 94:1087–1090. 6. Peterson LR, Waggoner AD, Schechtman KB, Meyer T, Gropler RJ, Barzilai B, Davila-Roman VG. Alterations in left ventricular structure and function in young healthy obese women: assessment by echocardiography and tissue Doppler imaging. J Am Coll Cardiol 2004;43:1399 –1404. 7. Otto ME, Belohlavek M, Khandheria B, Gilman G, Svatikova A, Somers V. Comparision of right and left ventricular function in obese and nonobese men. Am J Cardiol 2004;93:1569 –1572. 8. Mehta SK, Holliday C, Hayduk L, Wiersma L, Richards N, Younoszai A. Comparision of myocardial function in children with body mass indexes ⱖ25 versus those ⬍25 kg/m2. Am J Cardiol 2004;93:1567–1569. 9. Schiller NB, Shah PM, Crawford M, DeMaria A, Devereux R, Feigenbaum H, Gutfesell H, Reichek N, Sahn D, Schnittinger I, Silverman NH, Tajik AJ, and the American Society of Echocardiography Committee on Standards, Subcommittee on Quantitation of Two-Dimensional Echocardiograms. Recommendations for quantitation of left ventricler by two-dimensional echocardiography. J Am Soc Echocardiogr 1989;2:358 –367. 10. Devereux RB, Alonso DR, Lutas, Gottlieb GJ, Campo, Sachs I, Reichek N. Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol 1986;57:450 – 458. 11. Nagueh SF, Middleton KJ, Kopelen HA, Zoghbi WA, Quinones MA. Doppler tissue imaging: a noninvasive technique for evaluation of left ventricular relaxation and estimation of filling pressures. J Am Coll Cardiol 1997;30:1527–1533. 12. Alam M, Wardell J, Andersson E, Samad BA, Nordlander R. Characteristics mitral and tricuspid annular velocities determined by pulsed wave Doppler tissue imaging in healthy subjects. J Am Soc Echocardiogr 1999;12:618 – 628. 13. Alpert MA, Lambert CR, Terry BE, Cohen MV, Mulekar M, Panayiotou H, Mukerji V. Effect of weight loss on left ventricular diastolic filling in morbid obesity. Am J Cardiol 1995;76:1198 –1201. 14. Karason K, Wallentin I, Larsson B, Sjostom L. Effects of obesity and weight loss on cardiac function and valvular performance. Obes Res 1998;6:422– 429. 15. Kanoupakis E, Michaloudis D, Fraidakis O, Parthenakis F, Vardas P, Melissas J. Left ventricular function and cardiopulmonary performance following surgical treatment of morbid obesity. Obes Surg 2001 11:552–558. 16. Alpert MA, Kelly DL. Value and limitations of echocardiography in the evaluation of obese patients. Echocardiography 1986;3:261–272. 17. Helbing WA, Bosch HG, Maliepaard C, Rebergen SA, van der Geest RJ, Hansen B, Ottenkamp J, Reiber JHC, de Roos A. Comparison of echocardiographic methods with magnetic resonance imaging for assessment of right ventricular function in children. Am J Cardiol 1995;76:589 –594. 18. Marfella R, Esposito K, Siniscalchi M, Cacciapouti F, Giugliano F, Labriola D, Ciotola M, Di Palo C, Misso L, Giugliano D. Effect of weight loss on cardiac synchronization and proinflammatory cytokines in premenopausal obese women. Diabetes Care 2004;27:47–53. 19. Hoffman R, Hanrath P. Tricuspid annular velocity measurement. Simple and accurate solution for a delicate problem? Eur Heart J 2001;22:280 –282.
JUNE 15, 2005
bulky to be used in young infants. It is conceivable that older infants weighing ⬎6 kg, with a VSD diameter ⬍11 mm, can undergo repair, providing that the test balloon occlusion is favorable. 1. King T, Mills N. Non-operataive closure of atrial septal defects. Surgery 1974;75:383–386. 2. Rashkind W, Cuaso C. Transcatheter treatment of congenital heart disease. Circulation 1983;67:711–716. 3. Sideris EB, Toumanides S, Macuil B, Gutierrez-Leonard H, Poursanov M, Sokolov A, Moulopoulos SD. Transcatheter patch correction of secundum atrial septal defects. Am J Cardiol 2002;89:1082–1086. 4. Lock JE, Block PC, McKay RG, Beim DS, Keane JF. Transcatheter closure of ventricular septal defects. Circulation 1988;78:361–368. 5. Rigby ML, Redington AN. Primary transcatheter closure of perimembranous ventricular septal defects. Br Heart J 1994;72:368 –371. 6. Sideris EB, Walsh KP, Haddad JL, Chen CR, Ren SG, Kulkarni H. Occlusion of congenital ventricular septal defects by the buttoned device. Heart 1997;77: 275–279. 7. Bass JL, Kaira GS, Arora R. Masura J, Gavora P. Thanopoulos BD, Torres W, Sievert H. Initial human experience with the Amplatzer perimembranous ventricular septal defect occluder device. Cathet Cardiovasc Interventions 2003;58: 238 –245. 8. Sideris EB Sideris CE, Stamatelopoulos SF, Moulopoulos SD. Transcatheter patch occlusion of experimental atrial septal defects. Cathet Cardiovasc Interventions 2002;57:404 – 410. 9. Sideris EB, Toumanides S, Sideris C, Moulopoulos SD. Accelerated transcatheter patch occlusion of heart defects: experimental findings. Cathet Cardiovasc Interventions 2004;62:93:32. 10. Sideris EB, Macuil B, Varvarenko V, Alekyan B. Outpatient transcatheter patch occlusion of large patent ductus arteriosus and perimembranous ventricular septal defect. Cathet Cardiovasc Interventions 2004;62:140:7.
Effects of Weight Loss After Gastric Bypass on Right and Left Ventricular Function Assessed by Tissue Doppler Imaging Howard J. Willens, MD, Simon C. Chakko, MD, Patricia Byers, MD, Julio A. Chirinos, MD, Eugenio Labrador, RDCS, Juan C. Castrillon, RDCS, and Maureen H. Lowery, MD To evaluate the effects of substantial weight loss on tissue Doppler imaging parameters of right ventricular (RV) and left ventricular (LV) systolic and diastolic function, we performed standard echocardiography and tissue Doppler imaging in 17 patients with severe obesity before and after gastric bypass. Patients lost 39 ⴞ 10 kg over 7.6 ⴞ 3.6 months. Adjusted LV mass decreased (134 ⴞ 41 to 119 ⴞ 31 kg/m, p ⴝ 0.031). After weight loss, the ratios of early-to-late diastolic mitral and tricuspid inflow velocities increased (1.3 ⴞ 0.2 to 1.6 ⴞ 0.5, p ⴝ 0.02; 1.0 ⴞ 0.1 to 1.6 ⴞ 0.3, p ⴝ 0.003). Early diastolic tissue Doppler velocities increased at both the lateral and septal mitral annulus (7.6 ⴞ 1.5 to 9.3 ⴞ 2.5 cm/s, p ⴝ 0.009; and 6.6 ⴞ From the Department of Medicine, Division of Cardiology, and Department of Surgery, University of Miami School of Medicine, Miami, Florida. Dr. Willens’ address is: 3513 Greenleaf Circle, Hollywood, Florida 33021-8437. E-mail: [email protected]. Manuscript received December 9, 2004; revised manuscript received and accepted February 11, 2005. ©2005 by Excerpta Medica Inc. All rights reserved. The American Journal of Cardiology Vol. 95 June 15, 2005
1.4 to 7.7 ⴞ 1.7 cm/s; p ⴝ 0.028, respectively) and for their 2-site average (7.2 ⴞ 1.0 to 8.5 ⴞ 1.7 cm/s, p ⴝ 0.007). Early diastolic tricuspid annular velocity increased (7.2 ⴞ 2.8 to 10.6 ⴞ 2.3 cm/s, p <0.001) as did the ratio of early-to-late tricuspid annular diastolic velocity (0.9 ⴞ 0.4 to 1.1 ⴞ 0.2, p ⴝ 0.038). Tricuspid annular systolic velocity increased (8.6 ⴞ 2.5 to 10.3 ⴞ 2.7 cm/s, p ⴝ 0.037). In patients with severe obesity, significant weight loss results in an increase in tricuspid annular systolic and early diastolic velocities and mitral annular early diastolic velocities. 䊚2005 by Excerpta Medica Inc. (Am J Cardiol 2005;95:1521–1524)
besity is associated with multiple cardiopulmonary symptoms and an increased risk of develO oping heart failure. Although weight loss is routinely 1
2
recommended to improve symptoms and decrease risk, the effects of weight loss on cardiac function and the role these effects have on improving symptoms 0002-9149/05/$–see front matter doi:10.1016/j.amjcard.2005.02.029
1521
research protocol, and all patients gave informed consent. Parameter Presurgical Postsurgical Change Clinical and demographic data were obtained by chart review, interWeight (kg) 160 ⫾ 43 121 ⫾ 43* ⫺39 view, and physical examination. The 54 ⫾ 11 40 ⫾ 11* ⫺14 BMI (kg/m2) Heart rate at rest (beats/min) 82 ⫾ 16 70 ⫾ 12† ⫺12 presence of sleep apnea was deterSystolic blood pressure (mm Hg) 145 ⫾ 17 134 ⫾ 17‡ ⫺9 mined by diagnostic polysomnogra† Diastolic blood pressure (mm Hg) 84 ⫾ 12 77 ⫾ 12 ⫺7 phy. Values are expressed as mean ⫾ SD. All subjects underwent complete *p ⬍0.001; †p ⫽ 0.001; ‡p ⫽ 0.012. 2-dimensional echocardiography and tissue Doppler imaging before and 7.4 ⫾ 3.6 months (range 3 to 15) after surgery. Standard echocardioTABLE 2 Two-dimensional and Doppler Echocardiographic Data graphic views were obtained in the Presurgical Postsurgical left lateral decubitus position using Parameter (n ⫽ 17) (n ⫽ 17) p Values commercially available equipment LV end-diastolic diameter (cm) 5.2 ⫾ 0.7 5.0 ⫾ 0.6 0.855 (Vivid 7, GE-Vingmed, Horten, NorLeft atrium (cm) 3.5 ⫾ 0.5 3.7 ⫾ 0.4 0.397 way) after 10 minutes of rest in the Septal wall thickness (cm) 1.2 ⫾ 0.2 1.1 ⫾ 0.2 0.238 supine position. Harmonic imaging Posterior wall thickness (cm) 1.1 ⫾ 0.2 1.0 ⫾ 0.2 0.064 was used in all patients, and LV LV mass index (g/m) 134 ⫾ 41 119 ⫾ 31 0.031 opacification with a contrast agent LV fractional shortening (%) 35 ⫾ 8 32 ⫾ 5 0.198 RV end-diastolic diameter (cm) 3.1 ⫾ 0.5 3.1 ⫾ 0.7 0.895 was used as needed to improve enEarly mitral inflow (cm/s) 94 ⫾ 22 87 ⫾ 16 0.048 docardial definition. Beta-adrenergic Late mitral inflow (cm/s) 73 ⫾ 14 60 ⫾ 17 0.031 and calcium antagonists were withEarly/late diastolic mitral inflow 1.3 ⫾ 0.2 1.6 ⫾ 0.5 0.02 held for 24 hours before the study. Deceleration time (ms) 194 ⫾ 29 181 ⫾ 30 0.302 Early/late tricuspid inflow (n ⫽ 8) 1.0 ⫾ 0.1 1.6 ⫾ 0.3 0.002 One investigator performed all Pulmonary artery systolic pressure (mm Hg) 32 ⫾ 9 32 ⫾ 8 0.58 echocardiographic and tissue Dopp(n ⫽ 8) ler imaging analyses. LV internal diValues are expressed as mean ⫾ SD. mensions and wall thickness were measured from 2-dimensional, guided, M-mode echocardiographic and prognosis have not been fully documented.3,4 Re- tracings obtained at mid-chordal level in the parastercently, tissue Doppler imaging has been shown to be nal short-axis view according to American Society of more sensitive than standard echocardiography for Echocardiography criteria.9 Left atrial internal dimendetecting subclinical right ventricular (RV) and left sion at end-systole and RV internal dimension at endventricular (LV) dysfunction in patients with obesi- diastole were measured in the parasternal long-axis ty.5– 8 In addition, tissue Doppler imaging does not view. The average of 2 measurements was recorded depend on endocardial definition and is less affected for all parameters. LV mass was calculated according by chest wall attenuation than standard echocardiog- to the previously described method of Devereux et al10 raphy. Therefore, in obese patients who may be chal- and normalized to height in meters. Percent fractional lenging to image, sequential tissue Doppler imaging shortening was calculated as a measure of LV systolic may be a more accurate and reproducible technique function. than standard echocardiography for investigating Mitral and tricuspid inflow velocities were obchanges in cardiac function resulting from weight tained by pulse-wave Doppler in the apical 4-chamber loss. This study examines the effects of significant view. The peak early and late diastolic mitral and weight loss after gastric bypass surgery on RV and LV tricuspid inflow velocities were measured and aversystolic and diastolic function in patients with severe aged over 5 cardiac cycles during normal respiration. obesity using conventional echocardiography and tis- The mitral deceleration time was also measured. The sue Doppler imaging. ratio of early diastolic-to-late diastolic inflow velocities was calculated for both the mitral and tricuspid ••• Candidates for this study were patients who had valves. Pulmonary artery systolic pressure was estiundergone stress echocardiography before undergoing mated by adding 10 mm Hg to the transtricuspid long-limb Roux-en-Y gastric bypass for severe obe- pressure gradient. Color tissue Doppler imaging was performed from sity (body mass index [BMI] ⬎40 kg/m2 or ⬎35 kg/m2 plus co-morbidities). Subjects also agreed to the apical 4-chamber view using a 2.5-MHz transundergo echocardiography after achieving substantial ducer and frame rates of ⱖ80/s, and the images were weight loss. Patients with a history of heart failure, digitized. Images of the right and left ventricle were coronary artery disease, atrial fibrillation, left bundle carefully chosen to minimize the angle of incidence branch block, significant valve disease, positive stress between the scan lines and motion of the base of the test results, regional wall motion abnormalities, can- heart for both the pre- and postsurgical studies. Mean cer, and kidney or liver disease were excluded. The myocardial velocity profiles were derived and anainstitutional review board of our facility approved the lyzed off-line using commercially available computer TABLE 1 Pre- and Postsurgical Clinical Parameters
1522 THE AMERICAN JOURNAL OF CARDIOLOGY姞
VOL. 95
JUNE 15, 2005
annular velocity by tissue Doppler imaging, a measure of LV filling Presurgical Postsurgical pressure, was also calculated.11 Parameter (n ⫽ 17) (n ⫽ 17) p Values All echocardiographic, pulse-wave, and tissue Doppler variables are preLateral mitral annular systolic velocity (cm/s) 5.4 ⫾ 1.5 6.0 ⫾ 1.4 0.069 Septal mitral annular systolic velocity (cm/s) 5.7 ⫾ 1.2 5.9 ⫾ 1.2 0.620 sented as mean ⫾ SD. Pre- and postTwo-site average systolic velocity (cm/s) 5.6 ⫾ 1.2 6.0 ⫾ 1.2 0.218 surgical values were compared using Early diastolic lateral MAV (cm/s) 7.6 ⫾ 1.5 9.3 ⫾ 2.5 0.009 paired Student’s t-test. Pearson’s Late diastolic lateral MAV (cm/s) 5.4 ⫾ 1.5 5.7 ⫾ 1.5 0.447 correlation coefficient was used to Early/late diastolic lateral MAV ratio 1.5 ⫾ 0.4 1.7 ⫾ 0.4 0.229 Early diastolic septal MAV (cm/s) 6.6 ⫾ 1.4 7.7 ⫾ 1.7 0.028 explore univariate relations between Late diastolic septal MAV (cm/s) 6.4 ⫾ 2.4 6.5 ⫾ 1.2 0.852 changes in selected indexes of LV Early/late diastolic septal MAV ratio 1.1 ⫾ 0.5 1.2 ⫾ 0.3 0.572 and RV systolic and diastolic funcTwo-site average early diastolic velocity (cm/s) 7.2 ⫾ 1.0 8.5 ⫾ 1.7 0.007 tion and weight loss. A p value Early diastolic mitral inflow/lateral MAV ratio 12.3 ⫾ 4.0 10 ⫾ 3.3 0.01 ⬍0.05 was considered significant. Values are expressed as mean ⫾ SD. Statistical analysis was performed MAV ⫽ mitral annular velocity. using GraphPad Instat (GraphPad Software, Inc., San Diego, California). TABLE 4 Tissue Doppler Velocities in the Right Ventricle The study group consisted of 17 Presurgical Postsurgical patients (10 women and 7 men; mean Parameters (n ⫽ 17) (n ⫽ 17) p Values age 43 ⫾ 10 years). Ten patients had hypertension and 5 had diabetes melTricuspid annular systolic velocity (cm/s) 8.6 ⫾ 2.5 10.3 ⫾ 2.7 0.037 Early diastolic tricuspid annular velocity (cm/s) 7.2 ⫾ 2.8 10.6 ⫾ 2.3 ⬍0.001 litus. Obstructive sleep apnea was Late diastolic tricuspid annular velocity (cm/s) 8.7 ⫾ 2.1 10.2 ⫾ 2.4 0.227 present in 8 patients who were Early diastolic/late diastolic tricuspid annular 0.9 ⫾ 0.4 1.1 ⫾ 0.2 0.038 treated with continuous positive airvelocity ratio way pressure. Table 1 lists the effects Values are expressed as mean ⫾ SD. of surgery on mean weight, BMI, heart rate, and systolic and diastolic blood pressure. Mean heart rate and systolic and diastolic blood pressure significantly deTABLE 5 Correlations Between Amount of Weight Lost and creased with weight loss. Hypertension and diabetes Changes in Standard Doppler Echocardiographic and resolved in 3 patients, and obstructive sleep apnea Tissue Doppler Imaging Parameters resolved in 2. Two-dimensional echocardiographic Pearson’s images, pulse-wave Doppler mitral inflow, and tissue Parameters Coefficient (r) p Value Doppler imaging velocities were adequate for sequenLateral mitral annular early diastolic ⫹0.51 0.039 tial analysis before and after weight loss in all 17 velocity patients. Pulmonary artery systolic pressure and triEarly/late diastolic mitral inflow ⫹0.51 0.044 cuspid inflow were suitable for sequential analysis in Two-site average early diastolic tissue ⫹0.33 0.236 velocity 8 patients. Tricuspid annular early diastolic velocity ⫹0.34 0.233 Table 2 lists the effects of weight loss on selected Tricuspid annular systolic velocity ⫹0.16 0.575 2-dimensional and Doppler echocardiographic parameters. No significant changes in LV end-diastolic diameter, left atrial dimension, septal and posterior wall software (Echopac, GE-Vingmed) by placing a 6-mm thickness, fractional shortening, RV internal diameter, sample volume at the septal and lateral corners of the deceleration time, or pulmonary artery systolic presmitral annulus and lateral tricuspid annulus. The sam- sure were noted. LV mass indexed to height significantly decreased after weight loss. Although early and ple volume was manually repositioned during systole late mitral inflow velocities decreased after surgery, and early and late diastole to compensate for annular their ratio significantly increased. The ratio of early motion and maintain the sample volume in the area of diastolic-to-late diastolic tricuspid inflow velocities interest. also significantly increased in the 8 patients in whom Peak systolic and early and late diastolic tissue it could be measured. velocities were measured from the lateral and septal The effects of weight loss on tissue Doppler imagcorners of the mitral annulus and lateral tricuspid ing indexes of LV function are shown in Table 3. Peak annulus. The average of 3 consecutive cardiac cycles systolic velocities increased, but not significantly, at was recorded. The ratios of early-to-late diastolic tis- both the lateral and septal mitral annulus and for the sue Doppler velocities were calculated at all 3 annular 2-site average. Lateral and septal mitral annular early sites. In addition, the 2-site average peak systolic and diastolic tissue velocities significantly increased as did early diastolic velocities of the lateral and septal cor- their 2-site average. The ratio of early diastolic mitral ners of the mitral annulus were calculated. The ratio of inflow velocity to lateral mitral annular early diastolic peak early diastolic mitral inflow velocity by pulse- velocity significantly decreased. Table 4 lists the effects of weight loss on tissue wave Doppler to peak early diastolic lateral mitral TABLE 3 Tissue Doppler Velocities in the Left Ventricle
BRIEF REPORTS
1523
Doppler imaging indexes of RV function. Peak systolic and early diastolic tricuspid annular velocities significantly increased. The ratio of early-to-late diastolic tissue Doppler velocities at the tricuspid annulus significantly increased. Table 5 lists the results of Pearson’s correlation coefficients relating the change in selected Doppler echocardiographic and tissue Doppler imaging parameters after surgery with magnitude of weight loss. The increase in early diastolic lateral mitral annulus velocity and the ratio of early-to-late diastolic mitral inflow velocities significantly correlated with absolute amount of weight lost. •••
We obseved an increase in tricuspid annular systolic and early diastolic velocities and septal and lateral mitral annular early diastolic velocities in patients with severe obesity shortly after they achieved substantial weight loss with gastric bypass. These increases in mitral and tricuspid annnular velocities are consistent with subtle improvements in LV and RV diastolic function and RV systolic function.12 The tissue Doppler findings suggestive of improvement in LV and RV diastolic function are supported by the observed increase in the ratios of early diastolic to late diastolic mitral and tricuspid inflow velocities obtained with pulse-wave Doppler. Furthermore, the changes in pulse-wave and tissue Doppler indexes of LV diastolic function had a significant positive correlation with the amount of weight loss. This suggests that LV diastolic function may improve as more weight is lost. Additional observations in this study were a decrease in indexed LV mass and a reduction in peak early diastolic mitral inflow/peak early diastolic lateral mitral annular velocity ratio, suggesting a decrease in LV filling pressures. The finding of increased early diastolic mitral annular velocities suggestive of improved LV diastolic function after weight loss and the correlation of this increase with the amount of weight lost is consistent with previous studies that used standard Doppler to measure LV diastolic function in obese patients undergoing bariatric surgery.13–15 There have been few reports of the effects of obesity and subsequent weight loss on RV function. This scarcity of investigations may be due to difficulties imaging the right ventricle in obese patients16 and accurately evaluating global RV function noninvasively with echocardiography because of the chamber’s complex geometry.17 Evaluation of regional RV myocardial function by measuring tricuspid annular velocities with tissue Doppler imaging may therefore be particularly advantageous for understanding the effects of obesity and weight loss on RV function. Recently, 2 studies using tissue Doppler imaging to investigate RV function in obese patients reported impaired filling of the right ventricle.5,7 Our observation of increased early diastolic tricuspid annular velocities after gastric bypass is consistent with a recent report of improvement in a dif-
1524 THE AMERICAN JOURNAL OF CARDIOLOGY姞
VOL. 95
ferent tissue Doppler imaging parameter of RV diastolic function, RV relaxtion time, in patients achieving modest weight loss with diet and exercise.18 Our finding of an increase in tricuspid annular systolic velocities consistent with a subclinical improvement in RV systolic function has not been previously reported. Because tricuspid and mitral annular motion and velocity may be interdependent,19 our findings of increased tricuspid annular systolic and early diastolic velocities after weight loss must be interpreted with caution. 1. Sjostrom L, Larsson B, Backman L, Bengtsson C, Bouchard C, Dahlgren S, Hallgren P, Jonsson E, Karlsson J, Lapidus L. Swedish obese subjects (SOS): recruitment for an intervention study and a selected description of the obese state. Int J Obes Relat Metab Disord 1992;16:465– 479. 2. Kenchaiah S, Evans JC, Levy D, Wilson PWF, Benjamin EJ, Larson MG, Kannel WB, Vasan RS. Obesity and the risk of heart failure. N Engl J Med 2002;347:305–313. 3. Karason K, Lindroos AK, Stenlof K, Sjostrom L. Relief of respiratory symptoms and increased physical activity after surgically induced weight loss-results from the Swedish Obese Subjects study. Arch Intern Med 2000;160:1797–1802. 4. Alpert MA. Management of obesity cardiomyopathy. Am J Med Sci 2001;321: 237–241. 5. Willens HJ, Chakko SC, Lowery MH, Byers P, Labrador E, Gallagher A, Castrillon JC, Myerburg RJ. Tissue Doppler imaging of the right and left ventricle in severe obesity (body mass index ⬎35 kg/m2). Am J Cardiol 2004; 94:1087–1090. 6. Peterson LR, Waggoner AD, Schechtman KB, Meyer T, Gropler RJ, Barzilai B, Davila-Roman VG. Alterations in left ventricular structure and function in young healthy obese women: assessment by echocardiography and tissue Doppler imaging. J Am Coll Cardiol 2004;43:1399 –1404. 7. Otto ME, Belohlavek M, Khandheria B, Gilman G, Svatikova A, Somers V. Comparision of right and left ventricular function in obese and nonobese men. Am J Cardiol 2004;93:1569 –1572. 8. Mehta SK, Holliday C, Hayduk L, Wiersma L, Richards N, Younoszai A. Comparision of myocardial function in children with body mass indexes ⱖ25 versus those ⬍25 kg/m2. Am J Cardiol 2004;93:1567–1569. 9. Schiller NB, Shah PM, Crawford M, DeMaria A, Devereux R, Feigenbaum H, Gutfesell H, Reichek N, Sahn D, Schnittinger I, Silverman NH, Tajik AJ, and the American Society of Echocardiography Committee on Standards, Subcommittee on Quantitation of Two-Dimensional Echocardiograms. Recommendations for quantitation of left ventricler by two-dimensional echocardiography. J Am Soc Echocardiogr 1989;2:358 –367. 10. Devereux RB, Alonso DR, Lutas, Gottlieb GJ, Campo, Sachs I, Reichek N. Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol 1986;57:450 – 458. 11. Nagueh SF, Middleton KJ, Kopelen HA, Zoghbi WA, Quinones MA. Doppler tissue imaging: a noninvasive technique for evaluation of left ventricular relaxation and estimation of filling pressures. J Am Coll Cardiol 1997;30:1527–1533. 12. Alam M, Wardell J, Andersson E, Samad BA, Nordlander R. Characteristics mitral and tricuspid annular velocities determined by pulsed wave Doppler tissue imaging in healthy subjects. J Am Soc Echocardiogr 1999;12:618 – 628. 13. Alpert MA, Lambert CR, Terry BE, Cohen MV, Mulekar M, Panayiotou H, Mukerji V. Effect of weight loss on left ventricular diastolic filling in morbid obesity. Am J Cardiol 1995;76:1198 –1201. 14. Karason K, Wallentin I, Larsson B, Sjostom L. Effects of obesity and weight loss on cardiac function and valvular performance. Obes Res 1998;6:422– 429. 15. Kanoupakis E, Michaloudis D, Fraidakis O, Parthenakis F, Vardas P, Melissas J. Left ventricular function and cardiopulmonary performance following surgical treatment of morbid obesity. Obes Surg 2001 11:552–558. 16. Alpert MA, Kelly DL. Value and limitations of echocardiography in the evaluation of obese patients. Echocardiography 1986;3:261–272. 17. Helbing WA, Bosch HG, Maliepaard C, Rebergen SA, van der Geest RJ, Hansen B, Ottenkamp J, Reiber JHC, de Roos A. Comparison of echocardiographic methods with magnetic resonance imaging for assessment of right ventricular function in children. Am J Cardiol 1995;76:589 –594. 18. Marfella R, Esposito K, Siniscalchi M, Cacciapouti F, Giugliano F, Labriola D, Ciotola M, Di Palo C, Misso L, Giugliano D. Effect of weight loss on cardiac synchronization and proinflammatory cytokines in premenopausal obese women. Diabetes Care 2004;27:47–53. 19. Hoffman R, Hanrath P. Tricuspid annular velocity measurement. Simple and accurate solution for a delicate problem? Eur Heart J 2001;22:280 –282.
JUNE 15, 2005