Imaging and Diagnostic Testing

Right ventricular function before and after anuncomplicated coronary artery bypass graft asassessed by pulsed wave Doppler tissue imagingof the tricuspid annulusMahbubul Alam, MD, PhD, FESC, Anders Hedman, MD, Rolf Nordlander, MD, PhD, FESC, andBassem Samad, MD, PhD Stockholm, Sweden

Background Right ventricular (RV) function using myocardial velocities before and after a coronary artery bypassgraft (CABG) is not known.

Methods Using pulsed wave Doppler tissue imaging, RV function was studied in 35 patients before and afterCABG. Patients were followed-up for 1 year after the CABG. Myocardial velocities at the tricuspid annulus at the RV freewall were recorded from the apical 4-chamber views.

Results Both the systolic and early diastolic tricuspid annular velocities (TAV) were significantly reduced 1 month afterCABG (P � .001 for both). During the follow-up period, there was no improvement in the diastolic TAV. The systolic TAVshowed no improvement 3 months after CABG but recovered partially 1 year after the CABG (systolic velocities were11.8, 8.7, 8.7 and 9.7 cm/s, the early diastolic velocities were 11.0, 8.1, 8.1 and 8.2 cm/s before and 1 month, 3months and 1 year after the CABG, respectively). The systolic and early diastolic velocities of the interventricular septumwere unchanged during the follow-up period. Unlike the right ventricle, the mitral annular systolic velocity was unchangedshortly after CABG and showed signs of improvement after 1 year (6.4, 6.9, 6.8 and 7.3 cm/s respectively before andafter CABG). Patients underwent dobutamine stress echocardiography (DSE) before and 3 months after the CABG. Thesystolic TAV increased significantly during the DSE before CABG (11.8 vs 15.8 cm/s, P � .001). However, the increasein systolic TAV was limited during DSE 3 months after CABG (8.7 vs 9.9 cm/s, P � .05).

Conclusion RV function, as assessed by TAV, decreased significantly after CABG and the changes were still evidentafter 1 year. The response of systolic TAV during DSE was more pronounced before CABG than after CABG. (Am Heart J2003;146:520–6.)

Decreased right ventricular (RV) function is a factorknown to occur after a coronary artery bypass graft(CABG). Cardiac surgery with cardiopulmonary bypass,perioperative myocardial ischemia, pericardial disrup-tion/adhesions, etc., have been hypothesized to be thereason for the phenomenon.1–6 The decreased RVfunction has been shown to already occur during andimmediately after the cardiac surgery.2,7,8 Although the

echocardiographic assessment of left ventricular func-tion is simple, the evaluation of RV function by echo-cardiography is complicated because of the complexanatomy. In some studies, the amplitude of the tricus-pid annular motion assessed by conventional M-modeor 2-dimensional (2-D) echocardiography has beenused to evaluate systolic RV function.9,10 Using theamplitude of the tricuspid annular motion, the de-creased RV function after CABG has been demon-strated immediately after and 6 months after CABG.7,8

In recent years, myocardial velocities recorded byDoppler tissue imaging (DTI) have been used to assessboth left and right ventricular function.11–14 To ourknowledge, the DTI method has not been used to as-sess RV function in patients with coronary artery dis-ease before and after CABG. Using pulsed wave DTI,the purpose of the present study was to characterize

From the aDepartment of Cardiology, Karolinska Institute at Soder Hospital (Sod-ersjukhuset), Stockholm, Sweden.Submitted August 13, 2002; accepted January 28, 2003.Reprint requests: Mahbubul Alam, MD, PhD, Cardiology Department Sodersjukhuset,S-118 83, Stockholm, Sweden.E-mail: mahbubul.alam@medklin.sos.sll.se© 2003, Mosby, Inc. All rights reserved.0002-8703/2003/$30.00 � 0doi:10.1016/S0002-8703(03)00313-2

the tricuspid annular velocities in patients with coro-nary artery disease and to study the effect of dobut-amine stress echocardiography on the tricuspid annu-lar velocity before and after CABG.

MethodsSubjects

Thirty-five patients (30 men and 5 women) with a historyof coronary artery disease (CAD) were studied prospectively.All patients had significant CAD and were accepted for CABGwithin 2 months after the diagnostic coronary angiography.Sixteen patients had a history of myocardial infarction. Ninepatients had medically treated diabetes mellitus and 14 hadhypertension. None had atrial fibrillation, previous CABG,significant valvular heart disease, significant pulmonary dis-ease or left bundle branch block on electrocardiograms. Allhad normal septal motion preoperatively. Except for 1 pa-tient who underwent CABG on a beating heart, all patientsunderwent CABG with a cardiopulmonary bypass. None ofthe patients had perioperative or immediately postoperativemyocardial infarction. The patients were followed-up for 1year after the CABG. None of the patients had a myocardialinfarction or congestive heart failure during the follow-upperiod. Nineteen age-matched, healthy subjects (11 men and8 women) without a history of cardiac and pulmonary dis-ease or systemic hypertension and with normal findings onrest electrocardiogram and echocardiography served as con-trols.

InvestigationsThe patients underwent 4 echocardiographic examinations

at rest: before CABG and 1 month, 3 months and 12 monthsafter the CABG; 2 dobutamine stress echocardiography exam-inations (DSE), the first one before CABG (�3 weeks) andthe second one 3 months after CABG. Thirty-three patientsunderwent control angiography 3 months after the CABG.

Conventional echocardiography at restCommercially available echocardiographic equipment was

used (Hewlett-Packard sonos 5500 phased array systemequipped with DTI technology, Andover, Mass). The record-ing and calculations of different echocardiographic parame-ters were carried out according to the recommendations ofthe American Society of Echocardiography.15 An assessmentof the global left ventricular function was made using themagnitude of systolic mitral annular motion recorded by 2-Dguided M-mode echocardiography as described in a previousstudy.16 RV function was assessed using the magnitude of thetricuspid annular motion. The tricuspid annular motion wasrecorded at the RV free wall. From the 2-D guided apical4-chamber view, the M-mode cursor was placed through thetricuspid annulus in such a way that the annulus movedalong the M-mode cursor. The total systolic displacement wasmeasured using the leading edge of the echoes.9 Presence ofparadoxical motion of the interventricular septum was ana-lyzed visually or using M-mode echocardiography from theparasternal and apical views.

Mitral and tricuspid annular velocities by pulsed-wave DTI

Recording of the annular velocities using pulsed-wave DTIwas started by activating the DTI function of the same appa-ratus. A best quality recording was made using a variable fre-quency phased array transducer (2.0–4.0 MHz) and a lowwall filter setting (50 Hz). A 1.7-mm sample volume wasused. The gain was minimized to an optimal level to mini-mize noise. Similar to the recording of the M-mode annularmotion, the annular velocities using DTI were determined at4 sites in the left ventricle (septal, lateral, anterior and infe-rior walls; and a mean value was obtained from 4 differentsites) and at 1 site in the right ventricle corresponding to theRV free wall (Figure 1). Three major velocities were recordedat the annular sites: the peak major positive systolic velocitywhen the annulus moved towards the apex, and 2 major neg-ative velocities when the annulus moved back towards thebase (1 during the early phase of diastole and another duringthe late phase of diastole). The velocities were recorded online at a sweep speed of 50 mm/s. A mean of 5 consecutivecycles was used for the calculations of all echo-Doppler pa-rameters.

Dobutamine stress echocardiographyTwo-dimensional echocardiography and maximum dose

DSE were performed before and 3 months after CABG. Anintravenous infusion of dobutamine at a dosage of 5 �g �kg�1 � min�1 was started. The dose of dobutamine wasthen increased every 3 minutes to a total dose of 40 �g �kg�1 � min�1. If the patients failed to reach the terminatingcriteria, 0.25 mg atropine was given intravenously everyminute until the patients received a total of 1 mg atropine ordeveloped terminating criteria of DSE. To reach the terminat-ing criteria of the test, patients had to have 1 of the follow-

Figure 1

Method of recording the tricuspid annular velocity using Dopplertissue imaging. The systolic velocity and early and late diastolicvelocities are shown.

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ing conditions: development of chest pain, hypokinesia orakinesia of the left ventricular myocardium, ventricular ar-rythmia or a symptomatic fall of blood pressure. Echocardiog-raphy was performed at rest and during the maximum provo-cation of the DSE. The tricuspid annular velocity at the RVfree wall and the interventricular septal velocity from the api-cal 4-chamber view were recorded on line. The velocitieswere calculated as described earlier in the present study.

Coronary angiographyCoronary angiograms were performed twice: before the

CABG and 3 months after the CABG. Pre- and postoperativecoronary angiograms were analyzed independently by an ex-pert physician without knowledge of the echocardiographicfindings. On visual analysis, a �50% reduction of the luminaldiameter of a major coronary artery or one of its majorbranches or a bypass graft was considered to be a significantstenosis.

StatisticsThe results are expressed as the mean and 1 standard devi-

ation. Comparisons of the results between the healthy sub-jects and the patients were made using the Student’s un-paired t test. The repeated measurements of differentparameters during the follow-up period were initially com-pared using ANOVA. When an overall difference was noticed,the paired t test was used to compare the results within thesame group. A P value of �.05 was regarded as significant.

ResultsThe basic clinical and echocardiographic parameters

for the patients, compared with healthy subjects, areshown in Table I. The patients had a significantly de-creased systolic left ventricular function as assessed bythe M-mode mitral annular motion. The tricuspid annu-lar velocities in healthy subjects were the following:systolic velocity 13.9 � 1.8 mm, early diastolic veloc-ity 14.1 � 3.6 mm, and late diastolic velocity 15.3 �2.8 mm. The RV function assessed by the amplitude of

the M-mode recorded tricuspid annular motion wassimilar in both groups. However, the systolic and earlydiastolic tricuspid annular velocities were significantlydecreased in patients compared with healthy subjects(P � .01 for both). Except for the patient who under-went CABG without a cardiopulmonary bypass, all oth-ers showed paradoxical movement of the interventric-ular septum during all the follow-up investigations.Except for the E-wave deceleration time, the transtri-cuspid filling of the right ventricle remained un-changed after the CABG (Table II).

Mitral annular velocity using DTIThe systolic velocity recorded from 4 different sites

of the mitral annulus was unchanged until 3 monthsafter the CABG. However, the velocity improved dur-ing the follow-up period of 1 year (6.4 � 1.1, 6.9 �0.9, 6.8 � 1.3 and 7.3 � 1.4 before, 1 month, 3months and 1 year after CABG, respectively, P � .01for 1 year after compared to value before CABG). Forthe interventricular septum, both the systolic and dia-stolic velocities were calculated. The septal velocitieswere unchanged after CABG compared to the valuesbefore CABG (Table III).

Tricuspid annular velocities recorded by DTIThe systolic tricuspid annular velocity was signifi-

cantly decreased 1 month after the CABG. During thefollow-up period of 3 months, there was no improve-ment of the systolic velocity (Table III). A slight im-provement was noticed, however, 1 year after CABG.Like the systolic velocity, the diastolic velocities weresignificantly reduced after the CABG. No improvementof the diastolic velocities was noted during the fol-low-up period. A composite figure shows the mitraland tricuspid annular velocities before and after CABG(Figure 2).

Effect of DSE on annular velocitiesHeart rate increased similarly during the DSE both

before and 3 months after the CABG. The systolic tri-cuspid annular velocity increased significantly duringthe DSE before the CABG. During DSE after CABG, thesystolic tricuspid annular velocity was also increasedcompared to baseline. However, the increase was of alimited degree compared to the changes before CABG.On the other hand, the interventricular septumshowed a highly significant increase in the systolic ve-locity during DSE both before and after CABG (TableIV).

Pre- and postoperative coronary angiographyAt the initial investigation, 26 patients had 3-vessel, 8

patients had 2-vessel and 1 patient had single-vesseldisease. Thirty-one patients had right coronary artery

Table I. Basic characteristics of patients (n � 35) comparedto age-matched healthy subjects (n � 19)

PatientsHealthysubjects

Age (y) 65 � 10 66 � 5Heart rate 60 � 10 67 � 10LVEDd (mm) 49 � 5 46 � 4*LAD (mm) 38 � 4 34 � 3†MAM (mm) 11.8 � 2.3 14 � 1.7†TAM (mm) 24 � 5 25 � 4

Results are expressed as means and 1 SD. LVEDd, Left ventricular end-diastolicdimension, LAD, left atrial dimension recorded by M-mod echocardiography;MAM, mitral annular motion recorded by M-mod echocardiography; TAM, tricus-pid annular motion recorded by M-mode echocardiography.*P � .05 compared to patients.†P � .001 compared to patients.

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disease. Eight patients had occlusion of at least 1 ofthe grafts or native coronary arteries at the postopera-tive investigation. However, only 1 patient had occlu-sion of the graft to the right coronary artery.

DiscussionAssessment of RV function by conventionalechocardiography

There is no gold standard for assessing RV functionby echocardiography. This is partly due to the com-plex anatomy of the right ventricle. Using contrast ma-terial, the first echocardiographic assessment of RVfunction was described by Kaul et al.10 Later, themethod of recording the tricuspid annular motion byeither conventional 2-D or 2-D guided M-mode echo-cardiography was presented.9,17 Right ventricular sys-tole comprises a complex pattern of contractions ofthe RV myocardium along its long and short axes as

well as rotation along its longitudinal axis. In addition,the interventricular septum contributes to RV func-tion.18 As a result of RV contraction, the tricuspid an-nulus moves toward a stable apex during systole andreturns towards the cardiac base during diastole. Usingthe amplitude of the tricuspid annular motion from 1or several sites, RV function has been described inhealthy subjects and in patients with RV dysfunction.The magnitude of systolic tricuspid annular motion hasbeen shown to be reduced in patients with RV infarc-tion, atrial fibrillation, etc.9,14,17,19,20 The reversibledecrease in tricuspid annular motion during exercisetests has also been reported to detect proximal rightcoronary artery stenosis.21 Recording of the tricuspidannular motion is simple and feasible in most patients.

Previous studies following CABGRight ventricular dysfunction after cardiac surgery is

a well-known phenomenon. RV dysfunction can be

Table II. Clinical and conventional RV echo-Doppler parameters in patients before and after CABG

Before

Post CABG

1 Month 3 Months 12 Months

Heart rate (beats/min) 60 � 10 68 � 10 67 � 9 66 � 12SBP (mm Hg) 148 � 16 – 142 � 18 144 � 23DBP (mm Hg) 84 � 11 – 82 � 11 83 � 10RV dimension (mm) 29 � 4 28 � 3 29 � 4 29 � 4Doppler transtricuspid flow (m/s)

E wave 0.41 � 0.07 0.48 � 0.12 0.44 � 0.12 0.43 � 0.08A wave 0.35 � 0.06 0.41 � 0.12 0.37 � 0.11 0.35 � 0.11E/A ratio 1.16 � 0.25 1.2 � 0.34 1.2 � 0.38 1.2 � 0.36E-dec time (ms) 284 � 63 203 � 47* 188 � 54* –

E, Early; A, late flow during atrial contraction; E-dec, E-wave deceleration; SBP, systolic blood pressure; DBP, diastolic blood pressure.*P � .001 compared to before CABG.

Table III. Tricuspid annular velocities recorded by Doppler tissue imaging and expressed in cm/s in patients before and after CABG

Before

Post CABG

1 Month 3 Months 12 Months

Tricuspid annular velocitiesSystolic velocity 11.8 � 2.4* 8.7 � 1.6 8.7 � 1.7 9.7 � 1.4†‡Early diastolic velocity (E) 11 � 2.7* 8.1 � 2.3 8.1 � 2.7 8.2 � 2.4Late diastolic velocity (L) 13.6 � 3.5* 9.3 � 2.9 8.9 � 2.9 10.1 � 2.8E/L ratio 0.86 � 0.34 0.87 � 0.48 0.91 � 0.5 0.81 � 0.27

Interventricular septal velocitiesSystolic 6.2 � 1.3 6.3 � 1.6 6.1 � 1.2 6.1 � 1.3Early diastolic (E) 6.2 � 1.9 6.5 � 1.8 6.3 � 1.9 6.8 � 2.2Late diastolic (L) 9.1 � 1.8 8.7 � 2.1 8.3 � 2.5 9.4 � 2.4E/L ratio 0.68 � 0.21 0.78 � 0.21 0.75 � 0.31 0.73 � 0.33

Results are expressed as means and 1 SD.*P � .001 compared to values during all the follow-up periods after CABG.†P � .001 compared to value at 3 months.‡P � .001 compared to values before CABG.

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seen during and immediately after cardiac surgery.Both RV filling and RV contraction are impaired after aCABG. The mechanism of this phenomenon is not wellestablished. The changes in RV function that developafter a CABG are found in all subjects irrespective ofthe type of cardiac surgery supported by a cardiopul-monary bypass, the duration of the cardiopulmonarybypass or aortic clamp time or the methods used forcardioplegia and to preserve the myocardium.1–4,7,8

Although most studies included observations of RVfunction during and immediately after cardiac sur-gery,2,3,8 the long-term results of follow-ups of RVfunction are not fully known. Few studies using thesystolic tricuspid annular motion as a tool for evaluat-ing RV function have reported a significantly reducedtricuspid annular motion immediately after CABG.7,8

The reduced tricuspid annular motion recorded byM-mode echo was partly present 6 months afterCABG.7

Present study using the DTI and tricuspid annularvelocity

Assessment of myocardial function using myocardialvelocity as assessed by DTI is new. At present, thereare only a few reports available dealing with RV func-tion.14,22,23 The systolic and diastolic tricuspid annularvelocities recorded by DTI represent the respectivesystolic and diastolic functions of the right ventricle

and were found to be decreased in RV infarction, car-diomyopathy, etc.14,23 To our knowledge, the presentstudy is the first describing the characteristics of tri-cuspid annular velocities in patients with coronary ar-tery disease before and after CABG. In addition, thepresent study has followed the patients as long as 12months after bypass surgery.

Unlike the left ventricle, both the tricuspid annularvelocities were significantly decreased 1 month afterthe CABG. The results reflect a tethering of the RVwall as it was previously described in other studiesusing other techniques.7,8 Up to 3 months after CABG,no improvement of the tricuspid annular velocitieswas noted. During the control echocardiography 1year after CABG, a slight improvement in the systolictricuspid annular velocity was noted without anychange in the diastolic velocity. It is difficult to hy-pothesize whether the minor improvement of the sys-tolic velocity is a sign of recovery of the “stunned” RVwall that occurred during the cardiac surgery. AfterCABG, a preserved left ventricular function with a con-comitant reduced RV function, as assessed by the tri-cuspid annular velocity in the present study, mightgive rise to the question of an imbalance in the flowfrom the right to the left side of the heart. The para-doxical movement of the interventricular septum,which was noticed in all the patients after the CABGwith cardiopulmonary bypass, with its unaltered veloc-ity after CABG might contribute to the retention of atleast part of the RV function.

A previous study, using pulsed wave DTI during do-butamine stress echocardiography, showed a highlysignificant increase in the systolic tricuspid annularvelocity in patients with coronary artery disease andwithout right coronary artery stenosis.23 In the presentstudy, the systolic velocity of the tricuspid annulusincreased significantly at the maximum dobutaminetest before CABG. The increase in systolic velocity wasmarginal after CABG, although the increase in heartrate was similar to that before CABG. This findingmight support the hypothesis that the reduced RVfunction after CABG cannot only be explained by thedevelopment of “stunning” of the RV wall after CABG.However, the present study lacks information aboutthe tricuspid annular velocity during low-dose DSE. Infact, there is no consensus about the exact mechanismof reduced RV function after CABG.

Study limitationsThis study has some limitations. Only 1 site of the

tricuspid annulus was studied. In clinical practice, re-cording of other tricuspid annular sites might not befeasible in all patients. In addition, no method was in-cluded to assess the global RV function. In fact, thereis no consensus regarding the echocardiographic as-sessment of global RV function. No invasive or radio-

Figure 2

Systolic and early diastolic tricuspid annular velocities at rest be-fore and after CABG and systolic tricuspid annular velocity at DSEbefore and 3 months after CABG. #P � .001 compared to systolicvelocity at rest during the same investigation period. §P � .05compared to systolic velocity at rest during the same investigationperiod. * P � .001 compared to same parameter before CABG.€P � .001 compared to same parameter 3 months after CABG.

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nuclide method for detecting RV function was used.To compensate for this limitation, the interventricularseptum, which contributes to the pumping function ofthe right ventricle, was also included in the study. Anoninvasive perfusion or ischemic study of the rightventricle might have been appropriate to test the sig-nificance of the reduced tricuspid annular velocities.However, there is no standard study available for thispurpose. During the DSE, only the systolic velocitieswere recorded. Due to difficulties in the interpretationof diastolic velocities during peak dobutamine echocar-diography, no such parameters were presented in thepresent study. Intra- and interobserver variations inrecording the annular velocities were not carried outin the present study. However, these variations hadbeen tested previously and the values were negligi-ble.24

ConclusionRight ventricular function, as assessed by recording

the tricuspid annular velocities using Doppler tissueimaging, decreased significantly after CABG. Thechanges were still evident 1 year after CABG. The in-crease in the systolic tricuspid annular velocity duringDSE was more pronounced before CABG than afterCABG.

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8. Mishra M, Swaminathan M, Malhorta R, et al. Evaluation of rightventricular function during CABG: transesophageal echocardio-graphic assessment of hepatic venous flow versus conventionalright ventricular performance indices. Echocardiogr 1998;15:51–8.

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Table IV. DSE and pre- and postoperative changes in tricuspid annular velocity

Preop rest Preop DSE Postop rest Postop DSE

Heart rate 60 � 10 113 � 24 (147%)* 67 � 13 119 � 16 (144%)*Systolic tricuspid annular

velocity (cm/s)11.8 � 2.4 15.8 � 3 (134%)* 8.7 � 1.7 9.9 � 2.7 (113%)†

Systolic interventricularseptal velocity (cm/s)

6.2 � 1.3 9.2 � 2.3 (148%)* 6.1 � 1.2 8.0 � 2.1 (131%)*

Results are expressed in mean and 1 SD. Preop, Values before CABG; postop, values after CABG; 1, increase in percentage compared to values in the resting conditioneither pre- or postoperatively.*P � .001 compared to values at rest.†P � .05 compared to values at rest.

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18. Santamore WP, Dell’Italia LJ. Ventricular interdependance: signifi-cant left ventricular contributions to right ventricular systolic func-tion. Prog Cardiovasc Dis 1998;40:289–308.

19. Alam M, Samad B, Hedman A, et al. Cardioversion of atrial fibril-lation and its effect on right ventricular function as assessed bytricuspid annular motion. Am J Cardiol 1999;84:1256–8.

20. Xiong C, SonnHag C, Nylander E, et al. Atrial and ventricularfunction after cardioversion of atrial fibrillation. Br Heart J 1995;74:254–60.

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24. Alam M, Wardell J, Andersson E, et al. Effects of first myocardialinfarction on left ventricular systolic and diastolic function withthe use of mitral annular velocity determined by pulsed waveDoppler tissue imaging. J Am Soc Echocardiogr 2000;13:343–52.

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