- Email: [email protected]
Noninvasive Assessment of Left and Right Internal Mammary Artery Graft Patency with High-Frequency Transthoracic Echocardiography
Noninvasive Assessment of Left and Right Internal Mammary Artery Graft Patency with High-Frequency Transthoracic Echocardiography Luigi De Simone, MD, Pio Caso, MD, Sergio Severino, MD, Marino Scherillo, MD, Antonello D’Andrea, MD, Attilio Varricchio, MD, Roberto Violini, MD, and Nicola Mininni, MD, Napoli, Italy
Objectives: The aim of this study was (1) to visualize internal mammary artery grafts (IMAG) on coronary artery by transthoracic echocardiography and (2) to assess the patency of the grafts. Methods: Twenty-three patients (21 men, 56 ± 6 years) with previous coronary artery bypass grafting were studied at baseline and after they underwent lowdose dipyridamole infusion. The parameters obtained were systolic (SPV) and diastolic (DPV) peak velocities and their ratio (DPV/SPV); the dipyridamole infusion to baseline ratio of DPV was an index of IMAG blood flow reserve (FR). Two groups of patients were selected at baseline: group A, (n = 12) with a DPV/SPV >1, and group B (n = 11), with a DPV/SPV <1. Results: The IMAG was identified in all patients. Intraluminal flow signals obtained with pulsed wave Doppler showed a biphasic pattern (1 systolic and 1
I
n recent years the internal mammary artery has become the conduit of choice for surgical bypass in the coronary artery disease because of its superior long-term patency.1 The correct evaluation of chest pain in patients with recurrence of anginal symptoms after coronary artery bypass surgery may represent a problem, because symptoms are often atypical and the results of provoking tests may be dubious or nondiagnostic. Recent studies in the literature have shown that measurement of internal mammary artery graft (IMAG) velocity profile is feasible with transthoracic color Doppler echocardiography.2-4 However, cardiac cathFrom the Department of Cardiology, Laboratory of Echocardiography, Azienda Ospedaliera Monaldi, Napoli, Italy. Reprint requests: Luigi De Simone, MD, Via D. Fontana 194, 80131, Napoli, Italy (e-mail: [email protected]). Copyright © 1999 by the American Society of Echocardiography. 0894-7317/99 $8.00 + 0 27/1/101244
diastolic wave). After dipyridamole infusion was administered, flow velocities increased in 11 of 12 patients in group A and in 5 of 11 patients in group B. In group A the DPV/SPV increased from 1.79 ± 0.47 to 1.8 ± 0.43 (P = not significant), and the FR was 1.8 ± 0.4. In group B the DPV/SPV increased from 0.46 ± 0.05 to 0.5 ± 0.09 (P = not significant), and the FR was 1.3 ± 0.41. Coronary angiography showed the graft patency in all patients in group A and in 5 patients in group B with increased flow velocity after dipyridamole infusion. In the identification of graft stenosis at baseline, DPV/SPV showed 100% sensibility and 58% specificity, and FR showed 92% sensibility and 84% specificity. Conclusion: Doppler echocardiographic evaluation of the IMAG is a simple noninvasive method to assess the functional impairment of the vessel. (J Am Soc Echocardiogr 1999;12:841-9.)
eterization remains the method of choice for assessing IMAG patency.5,6 Even so, a noninvasive, easily repeatable method of assessing left (LIMA) and right internal mammary artery (RIMA) graft blood velocities and flow reserve (FR) with high diagnostic power would be useful. The aim of our study was to evaluate the feasibility of visualizing both LIMA and RIMA grafts on the left anterior descending coronary artery (LAD) and the right coronary artery (RCA), respectively, by high-frequency transthoracic echocardiography combined with a low-dose dipyridamole infusion to evaluate the coronary artery bypass graft patency.
PATIENTS AND METHODS Twenty-three consecutive patients (21 men, 2 women; mean age, 56 ± 6 years) undergoing coronary angiography because of recurrence of anginal symptoms 5 ± 2 years
841
Journal of the American Society of Echocardiography October 1999
842 De Simone et al
A
B
Figure 1 Doppler flow velocity recorded (A) from patency left internal mammary artery graft and (B) from normal descending anterior coronary artery. A, Characteristic Doppler velocity flow recorded from patent left internal mammary artery graft. Flow is biphasic, with prevalent diastolic velocity. Green, electrocardiogram; grey, left internal mammary artery graft flow. B, Doppler velocity profile in distal tract of patent descending anterior coronary. Flow is biphasic, with prevalent diastolic component. Green, Electrocardiogram; Orange, coronary flow.
after a coronary artery bypass graft were studied. We analyzed 25 mammary grafts (23 LIMA, 2 RIMA). Five patients had an anastomosis of the isolated LIMA graft performed to the LAD, 16 patients had an LIMA graft to the LAD and also a saphenous vein graft, and 2 patients had a LIMA graft to the LAD and an RIMA graft to the RCA. The clinical characteristic of the patients are shown in Table 1.
Echocardiography was performed with a Sequoia ultrasound machine (Acuson Corporation, Mountain View, Calif) equipped with a new color Doppler function: the nondirectional Doppler independent from the direction of the flow but, unlike the traditional Doppler, dependent on the quantity of the blood flow in the vessel analyzed. Compared with the traditional Doppler echocardiography,
Journal of the American Society of Echocardiography Volume 12 Number 10
De Simone et al 843
Table 1 Clinical characteristics of the patients Patients Age (y) Previous myocardial infarction
23 56 ± 6 11/23
Previous unstable angina Time from CABG Bypass
12/23 5±2 5 16 2 8/23 16/23 6/23
Typical chest pain Atypical chest pain Positive provocative tests
21 M, 2 F Anterior myocardial infarction 7/11 Inferior myocardial infarction 4/11
Isolated LIMA to DA LIMA to DA + saphenous vein graft LIMA to DA + RIMA to RCA 35% 69% 23%
CABG, Coronary artery bypass graft; LIMA, left internal mammary artery; DA, descending anterior coronary artery; RIMA, right internal mammary artery; RCA, right coronary artery.
this method is less influenced by the aliasing and also more sensible in detecting low-flow velocities and reduced blood volumes. The Sequoia machine was equipped with a small transthoracic multihertz Vector transducer (3.5 to 7 MHz) easily adaptable to narrow intercostal spaces. Patients were examined in the left lateral position with the use of a left parasternal window, and the long-axis sections were adjusted to identify the LIMA and RIMA grafts in nondirectional Doppler and in 2-dimensional echocardiography7 from their origin in the subclavian artery to the anastomosis to the coronary artery. Once the position of the mammary artery was identified, intraluminal flow signals were obtained with the pulsed Doppler method. The sampling volume was located within the vessel lumen with the most perpendicular position to the long axis of the artery. In all cases a biphasic pattern of blood flow corresponding to systolic and diastolic waves was detected (Figure 1, A). The IMAG showed a gradual transition in the phasic flow pattern from predominant systolic velocity proximally (at the origin from the subclavian artery)8 to predominant diastolic velocity distally (next to the anastomosis with the coronary artery).9 Therefore in our assessment of the IMAG flow velocities, we chose to use a parasternal window near the anastomosis instead of a subclavicular approach to avoid the influence of the subclavian artery flow velocity. However, the search for the best transthoracic window is essential for minimizing the angle between the Doppler beam and the long axis of the artery. With the transthoracic approach, in only 3 patients (2 with RIMA) of our study did we need to correct the angle between the Doppler beam and the blood flow approximately 30° to 40° as a result of the anatomic position of the vessel. At baseline the following parameters were obtained: systolic (SPV) and diastolic peak velocities (DPV), systolic (SVI) and diastolic velocity-time integrals (DVI), the diastolic-to-systolic peak velocity ratio (DPV/SPV) and the velocity-time integrals ratio (DVI/SVI), the diastolic frac-
Table 2 Clinical and echocardiographic data in group A and group B patients Group A
Group B
Patients 12 11 Age (y) 60 ± 6.7 55 ± 11 Graft 12 LIMA 9 LIMA, 2 RIMA DPV m/s 0.33 ± 0.13 0.12 ± 0.03 SPV m/sc 0.2 ± 0.09 0.27 ± 0.051 DPV/SPV 1.79 ± 0.47 0.46 ± 0.05 DVI (m) 0.11 ± 0.042 0.055 ± 0.02 SVI (m) 0.041 ± 0.03 0.06 ± 0.02 DVI/SVI 3.4 ± 1.3 0.93 ± 0.15 DVI/DVI + SVI 0.74 ± 0.08 0.47 ± 0.04 FR 1.8 ± 0.4 1.3 ± 0.41
P value
NS .0004 .05 .00005 .002 NS .0005 .0002 .009
LIMA, Left internal mammary artery graft; RIMA, right internal mammary artery graft; DPV, diastolic peak velocities; SPV, systolic peak velocities; DPV/SPV, systolic–to–diastolic peak velocity ratio; DVI, diastolic velocitytime integral; SVI, systolic velocity–time integral; DVI/SVI, systolic–todiastolic velocity – time integrals ratio; DVI/DVI + SVI, diastolic fraction of velocity – time integral; FR, dipyridamole infusion to baseline ratio of peak diastolic velocities.
tion of the velocity-time integral (ie, the diastolic velocitytime integral divided by the diastolic plus systolic velocitytime integrals: DVI/DVI+SVI). On the basis of the baseline mammary flow pattern, 2 groups of patients were selected: group A (n = 12 patients, 12 LIMA grafts), with a DPV/SPV >1, and group B (n = 11 patients, 11 LIMA grafts, 2 RIMA grafts), with a DPV/SPV <1. Subsequently, a low-dose dipyridamole infusion (0.56 mg/kg in 4 minutes) was performed during the detection of blood flow velocities in both LIMA and RIMA grafts. Blood pressure and electrocardiography were monitored throughout the entire protocol. We also calculated the dipyridamole infusion to baseline ratio of peak diastolic velocities, which was an index of the internal mammary artery graft blood FR. All images were recorded on a magneto-optical disk and analyzed later by 2 observers who were blinded to the angiographic result.
Journal of the American Society of Echocardiography October 1999
844 De Simone et al
A
B
Figure 2 Doppler flow velocity recorded (A) from occluded left internal mammary artery graft, (B) from normal internal mammary artery. A, Characteristic basal Doppler velocity flow recorded from occluded left internal mammary artery graft. Flow is biphasic, with maximum velocity occurring during systole, like native internal mammary artery. Very low velocity is recorded during diastole. Green, electrocardiogram; orange, flow in left internal mammary artery graft. B, Doppler Velocity profile in native internal mammary artery with characteristic prevalent systolic peak. Green, electrocardiogram; orange, internal mammary artery flow.
Coronary angiography was performed within a week after echocardiographic study by a standard Judkins technique. LIMA and RIMA grafts were examined with the use of multiple projections, and the stenosis were classified according to visually determined percent narrowing as severe (>70%), moderate (40% to 70%), and normal (<40%).
Statistics Data are expressed as mean values ± SD. Student paired t test was used for statistical analysis. A P value < .05 was considered statistically significant. We also calculated the sensibility and specificity of the test at baseline and after dipyridamole infusion for the assessment of the graft patency.
Journal of the American Society of Echocardiography Volume 12 Number 10
De Simone et al 845
Table 3 Echo-Doppler data in group A and group B patients at baseline and after Dipyridamole infusion Group A Baseline
DPV (m/s) SPV (m/s) DPV/SPV DVI (m) SVI (m) DVI/SVI DVI/DVI+SVI
0.33 0.2 1.79 0.11 0.04 3.4 0.74
± ± ± ± ± ± ±
0.13 0.09 0.47 0.04 0.03 1.3 0.08
Group B
Dipyridamole infusion
0.51 0.3 1.8 0.22 0.066 3.6 0.79
± ± ± ± ± ± ±
0.1 0.13 0.43 0.08 0.03 1.15 0.09
P value
.005 .04 NS .0002 .045 NS NS
Baseline
0.12 0.27 0.46 0.055 0.06 0.93 0.47
± ± ± ± ± ± ±
0.032 0.05 0.05 0.03 0.02 0.15 0.04
Dipyridamole infusion
0.13 0.27 0.5 0.053 0.06 0.9 0.46
± ± ± ± ± ± ±
0.03 0.04 0.09 0.02 0.02 0.13 0.04
P value
NS NS NS NS NS NS NS
DPV, Diastolic peak velocities; SPV, systolic peak velocities; DPV/SPV, systolic–to–diastolic peak velocity ratio; DVI, diastolic velocity-time integral; SVI, systolic velocity – time integral; DVI/SVI, systolic–to diastolic velocity – time integrals ratio; DVI/DVI + SVI, diastolic fraction of velocity – time integral.
Table 4 Echo-Doppler data in 2 subgroups of group B patients Group B1 (n = 6 grafts) Baseline
DPV (m/s) SPV (m/s) DPV/SPV DVI (m) SVI (m) DVI/SVI DVI/DVI+SVI
0.16 0.22 0.7 0.08 0.05 1.6 0.6
± ± ± ± ± ± ±
0.04 0.02 0.15 0.016 0.01 0.3 0.04
Dipyridamole infusion
0.29 0.33 0.99 0.16 0.08 2.03 0.65
± ± ± ± ± ± ±
0.09 0.09 0.5 0.05 0.02 0.6 0.08
Group B2 (n = 7 grafts) P value
.09 .01 .2 .0001 .008 NS NS
Baseline
0.12 0.25 0.46 0.05 0.05 0.9 0.55
± ± ± ± ± ± ±
0.03 0.06 0.04 0.02 0.02 0.15 0.04
Dipyridamole infusion
0.13 0.26 0.5 0.05 0.05 0.9 0.5
± ± ± ± ± ± ±
0.03 0.04 0.08 0.01 0.02 0.16 0.04
P value
NS NS NS NS NS NS NS
DPV, Diastolic peak velocities; SPV, systolic peak velocities; DPV/SPV, systolic–to–diastolic peak velocity ratio; DVI, diastolic velocity - time integral; SVI, systolic velocity – time integral; DVI/SVI, systolic–to diastolic velocity – time integrals ratio; DVI/DVI + SVI, diastolic fraction of velocity – time integral.
RESULTS LIMA and RIMA grafts were identified in all the patients in the study by the parasternal window. In 18 (78%) of 23 patients, the vessel was followed from its origin from the subclavian artery to the anastomosis to the coronary artery. Intraluminal flow signals obtained with the pulsed Doppler method showed a typical biphasic flow pattern characterized by a prevalent diastolic component (Figure 1, A). On the contrary, in the ungrafted internal mammary artery, the flow was dominant during systole, and low-velocity profiles were recorded during diastole (Figure 2, A). The parameters obtained in the 2 groups at baseline are expressed in Table 2. After dipyridamole infusion was performed, flow velocities increased in 11 (91%) of 12 mammary grafts in group A and in 6 (46%) of 13 mammary grafts in group B. In group A the DPV increased from 0.33 ± 0.12 to 0.51 ± 0.11 m/s (P = .005), the SPV increased from 0.2 ± 0.09 to 0.3 ± 0.13 m/s (P = .04), the DPV/SPV ratio increased from 1.79 ± 0.47 to 1.8 ± 0.43 (P = not significant [NS]), the DVI increased from 0.11 ± 0.04 to 0.22 ± 0.08 m (P = .0002), the
SVI increased from 0.04 ± 0.03 to 0.066 ± 0.03 m (P = .045), the DVI/SVI increased from 3.4 ± 1.3 to 3.6 ± 1.15 (P = NS), the diastolic fraction increased from 0.74 ± 0.08 to 0.79 ± 0.09 (P = NS), and the FR was 1.8 ± 0.4. In group B the DPV increased from 0.12 ± 0.032 to 0.13 ± 0.03 (P = NS), the SPV increased from 0.27 ± 0.05 to 0.27 ± 10.04 (P = NS), the DPV/SPV ratio increased from 0.46 ± 0.05 to 0.5 ± 0.09 (P = NS), the DVI increased from 0.055 ± 0.03 to 0.053 ± 0.02 (P = NS), the SVI increased from 0.06 ± 0.02 to 0.06 ± 0.02 (P = NS), the DVI/SVI ratio increased from 0.93 ± 0.15 to 0.9 ± 0.13 (P = NS), the diastolic fraction increased from 0.47 ± 0.04 to 0.46 ± 0.04 (P = NS), and the FR was 1.3 ± 0.41. Data are also expressed in Table 3. In group B we selected 2 subgroups: group B1, with a baseline DPV/SPV ratio <1 that increased after dipyridamole infusion, and group B2, with a DPV/SPV ratio at rest <1 that did not increase after dipyridamole infusion. Data are summarized in Table 4. Assessment of reproducibility of IMAG flow in 10 randomly selected patients (5 of group A, 5 of group B) revealed an intraobserver mean error of 4% ± 1% and an interobserver error of 5% ± 1.5%.
Journal of the American Society of Echocardiography October 1999
846 De Simone et al
A
B
Figure 3 Doppler velocity flow recorded from patent left internal mammary artery graft before (A) and after (B) dipyridamole infusion. A, At baseline, ratio between systolic and diastolic peak is approximately 1. B, After dipyridamole infusion, diastolic velocity is more increased than systolic velocity, and ratio between systolic and diastolic peak is normalized (<1). Green, electrocardiogram; orange, left internal mammary artery graft flow.
Coronary angiography performed within 7 days from echocardiography showed the graft patency and the native LAD patency distal to anastomosis in all the patients in group A and in 5 patients in subgroup B1 (with 6 mammary grafts) showing increased flow velocity after dipyridamole infusion. In the identification of a significant graft stenosis, the DPV/SPV ratio showed at baseline 100% sensibility and 58% specificity, whereas the variation of FR after
dipyridamole infusion presented 92% sensibility and 84% specificity.
DISCUSSION Coronary artery bypass conduits derived from internal mammary arteries are used more and more in the surgical therapy of ischemic heart diseases because
Journal of the American Society of Echocardiography Volume 12 Number 10
De Simone et al 847
A
B
Figure 4 Doppler velocity flow recorded from occluded left internal mammary artery graft before (A) and after (B) dipyridamole infusion. A, At baseline, systolic velocity is prevalent. B, After dipyridamole infusion, no increase of velocity is registered. Flow is similar to baseline. Green, electrocardiogram; orange, left internal mammary artery graft flow.
of their significantly improved long-term patency compared with saphenous vein graft.1 A noninvasive method that allows the identification of the IMAG, the measurement of blood flow, and the assessment of its short- and long-term patency may represent a useful technique in the diagnostic evaluation of patients with ischemia. The rate of direct visualization of the native internal mammary artery is already 100%,7 whereas the visualization of LIMA graft has been attempted in previous studies with a rate of detection variable from 70% to 95%.2,3,8-11 The mobilization of
the internal mammary artery with its neurovascular peduncle during coronary artery bypass grafting may change the anatomic disposition of the vessel. This change may result in a difficult detection of IMAG, especially next to the distal anastomosis to the coronary artery. In our study both the use of a small transthoracic multihertz transducer and the application of new echocardiographic software has led to the visualization of both LIMA and RIMA grafts in all the patients. The new software allows analysis of Doppler flow intensity in the vessels and also the visualization of low velocities
848 De Simone et al
and reduced blood volume. It is independent to flow direction. IMAG without significant stenosis showed a typical pulsed Doppler flow pattern (Figure 1, A) similar to that of a coronary artery (Figure 1, B), characterized by a prevalent diastolic component,3,9-12 with both peak velocities and velocity-time integrals higher in diastole than in systole. On the contrary, in patients with occluded IMAGs or IMAGs with severe stenosis, low velocity profiles were recorded during diastole, with an increase of the systolic component (Figure 2, A). As a result, at baseline flow was dominant during systole,3 and the IMAG velocity flow pattern in these cases was similar to that detected in the ungrafted internal mammary artery (Figure 2, B). As a result of our study, we may propose a new Doppler index for the assessment of the IMAG patency. In the literature previous invasive13,14 and noninvasive3,11,15 studies about the internal mammary artery evaluation already showed that at baseline, both a DPV/SPV ratio <0.6 and a diastolic fraction of the velocity-time integral <0.5 predicted severe stenosis of the IMAG. In our experience all of the patients in group A with a baseline DPV/SPV ratio >1 showed IMAG graft angiographic patency; consequently, dipyridamole infusion did not contribute new information in patients with normal DPV/SPV ratios at rest. All the mammary grafts of the patients in group B showed a DPV/SPV ratio <1 at baseline, 8 of 13 a ratio <0.6, and 7 of 13 a diastolic fraction of the velocity-time integral <0.5. However, a DPV/SPV ratio <0.6 may also be detected in patients with a patent IMAG,3 suggesting that this index has a low specificity. In this case and in all dubious cases, a low-dose infusion of dipyridamole may lead to the assessment of the functional impairment of the vessel. In fact, in our experience the dipyridamole infusion increased flow velocities up to 50% compared with baseline in 11 of 12 patients in group A, with an FR of 1.8 ± 0.4 and in 5 of 11 patients (6 mammary grafts) in subgroup B1, with an FR of 1.84 ± 0.23 (Figure 3), whereas in 6 of 11 patients (7 mammary grafts) in subgroup B2, no significant increase in flow parameters was observed after dipyridamole infusion (Figure 4). Coronary angiography showed a severe (>70%) stenosis of the graft in patients of subgroup B2 only. As a result the response of the internal mammary artery flow velocities to the dipyridamole infusion may distinguish patients with critical versus noncritical graft stenosis.
Journal of the American Society of Echocardiography October 1999
Study Limitations Although measurements of IMAG flow velocities with the use of transthoracic echocardiography have been shown to be feasible, the examination may present some technical problems. As a consequence a stage of learning of the evaluation of the grafts may be useful before this method is used routinely. In some cases a correction of the angle between the Doppler beam and the long axis of the vessel may be necessary; this could lead to undervaluing of the flow velocities. Furthermore a larger population of patients is required to assess the real clinical impact of this technique to the follow-up of patients with IMAG. Future Advances Last generation ultrasound systems equipped with second harmonic technology allow the visualization of the distal portion of the LAD and the analysis of flow velocities within the vessel.12 Therefore the evaluation of both internal mammary artery and native LAD distal to the anastomosis at the same time might give further information for the assessment of the functional significance of a stenotic lesion of the graft. Conclusions The color Doppler echocardiographic evaluation of the IMAG is a simple noninvasive method to assess the functional impairment of the vessel at baseline. Our study showed that with this technique, it may be possible to (1) visualize both LIMA and RIMA grafts, (2) analyze the pulsed Doppler flow patterns of the IMAG with the use of transthoracic echocardiography, and (3) assess the patency and the functional status of the IMAG both at rest and after dipyridamole infusion. In dubious cases with an DPV/SPV ratio equal or inferior to 1 at rest, the infusion of low doses of dipyridamole may increase almost to 50% all the flow velocities, especially the diastolic ones, allowing an indirect assessment of the functional status of the graft. In conclusion, color Doppler assessment of IMAG may represent a filter to the coronary angiography, especially in patients with nondiagnostic clinical signs and provocative tests. REFERENCES 1. Grondin CM, Campeau L, Lesperance J, Enjalbert M, Bourassa MG. Comparison of late changes in internal mammary artery and saphenous vein graft in two consecutive
Journal of the American Society of Echocardiography Volume 12 Number 10
2.
3.
4.
5.
6.
7.
8.
series of patients 10 years after operation. Circulation 1984; 70:I208-212. Crowley JJ, Shapiro LM. Noninvasive assessment of left internal mammary artery graft patency using transthoracic echocardiography. Circulation 1995;92(suppl II):25-30. Rombaut E, Vantrimpont P, Gurné O, et al. Noninvasive functional assessment of left internal mammary artery grafts by transcutaneous Doppler echocardiography. J Am Soc Echocardiogr 1998;11:403-8. Pezzano A, Cali G, Milazzo A, et al. Transthoracic 2D echo color Doppler assessment of internal mammary artery to left anterior descending coronary artery graft. Int J Card Imaging 1995;11:177-84. Fitzgibbon GB, Leach AJ, Kafka HP, Keon WJ. Coronary bypass graft fate: long term angiographic study. J Am Coll Cardiol 1991;17:1075-80. Kyo S, Matsamura N, Yokote Y, Takamoto S, Omoto R. Evaluation of patency of internal mammary artery grafts: a comparison of two–dimensional Doppler echocardiography and coronary angiography. J Cardiol 1990;20:606-16. Ehrsam JE, Spittel PC, Seward JB. Internal mammary artery: 100% visualization using new ultrasound technology. J Am Soc Echocardiogr 1998;11:10-2. Krijne R, Lyttwin RM, Holtgen R, Heinrich KW. Doppler sonographic examination of the internal mammary artery graft: comparison of supraclavicular and high intercostal signals. Cardiology 1993;82:48-50.
De Simone et al 849
9. Voci P, Plaustro G, Testa G, Marino B, Campa PP. Visualizzazione delle arterie mammarie interne native e del graft aortocorarico con ecocardiografia color Doppler ad alta risoluzione. Cardiologia 1998;43:403-6. 10. Bruni A., Chirillo F, Cavallini C, Stritoni P. Studio dei bypass aorto-coronarici con Eco Bidimensionale e Color-Doppler transtoracico. Emodinamica 1998;13:2-5. 11. El Masri M, Salama M, Darwish A. Assessment of left internal mammary artery graft patency by transthoracic Doppler echocardiografphy [abstract]. Eur Heart J 1998;19:66 (P544). 12. Hozumi T, Yoshida K, Ogata Y, et al. Noninvasive assessment of significant left anterior descending artery stenosis by coronary flow velocity reserve with transthoracic color Doppler echocardiography. Circulation 1998;97:1557-62. 13. Bach RG, Kern MJ, Donohue TJ, Aguirre FV, Caracciolo EA. Comparison of phasic blood flow velocity characteristics of arterial and venous coronary artery bypass conduits. Circulation 1993;88:II133-140. 14. Gurné O, Chenu P, Polidori C, et al. Functional evaluation of internal mammary artery bypass grafts in the early and late postoperative periods. J Am Coll Cardiol 1995;25: 1120-8. 15. Takagi T, Yoshikawa J, Yoshida K, Akasaka T. Noninvasive assessment of left internal mammary artery graft patency using duplex Doppler echocardiography from the supraclavicular fossa. J Am Soc Echocardiogr 1993;6:374-81.
Objectives: The aim of this study was (1) to visualize internal mammary artery grafts (IMAG) on coronary artery by transthoracic echocardiography and (2) to assess the patency of the grafts. Methods: Twenty-three patients (21 men, 56 ± 6 years) with previous coronary artery bypass grafting were studied at baseline and after they underwent lowdose dipyridamole infusion. The parameters obtained were systolic (SPV) and diastolic (DPV) peak velocities and their ratio (DPV/SPV); the dipyridamole infusion to baseline ratio of DPV was an index of IMAG blood flow reserve (FR). Two groups of patients were selected at baseline: group A, (n = 12) with a DPV/SPV >1, and group B (n = 11), with a DPV/SPV <1. Results: The IMAG was identified in all patients. Intraluminal flow signals obtained with pulsed wave Doppler showed a biphasic pattern (1 systolic and 1
I
n recent years the internal mammary artery has become the conduit of choice for surgical bypass in the coronary artery disease because of its superior long-term patency.1 The correct evaluation of chest pain in patients with recurrence of anginal symptoms after coronary artery bypass surgery may represent a problem, because symptoms are often atypical and the results of provoking tests may be dubious or nondiagnostic. Recent studies in the literature have shown that measurement of internal mammary artery graft (IMAG) velocity profile is feasible with transthoracic color Doppler echocardiography.2-4 However, cardiac cathFrom the Department of Cardiology, Laboratory of Echocardiography, Azienda Ospedaliera Monaldi, Napoli, Italy. Reprint requests: Luigi De Simone, MD, Via D. Fontana 194, 80131, Napoli, Italy (e-mail: [email protected]). Copyright © 1999 by the American Society of Echocardiography. 0894-7317/99 $8.00 + 0 27/1/101244
diastolic wave). After dipyridamole infusion was administered, flow velocities increased in 11 of 12 patients in group A and in 5 of 11 patients in group B. In group A the DPV/SPV increased from 1.79 ± 0.47 to 1.8 ± 0.43 (P = not significant), and the FR was 1.8 ± 0.4. In group B the DPV/SPV increased from 0.46 ± 0.05 to 0.5 ± 0.09 (P = not significant), and the FR was 1.3 ± 0.41. Coronary angiography showed the graft patency in all patients in group A and in 5 patients in group B with increased flow velocity after dipyridamole infusion. In the identification of graft stenosis at baseline, DPV/SPV showed 100% sensibility and 58% specificity, and FR showed 92% sensibility and 84% specificity. Conclusion: Doppler echocardiographic evaluation of the IMAG is a simple noninvasive method to assess the functional impairment of the vessel. (J Am Soc Echocardiogr 1999;12:841-9.)
eterization remains the method of choice for assessing IMAG patency.5,6 Even so, a noninvasive, easily repeatable method of assessing left (LIMA) and right internal mammary artery (RIMA) graft blood velocities and flow reserve (FR) with high diagnostic power would be useful. The aim of our study was to evaluate the feasibility of visualizing both LIMA and RIMA grafts on the left anterior descending coronary artery (LAD) and the right coronary artery (RCA), respectively, by high-frequency transthoracic echocardiography combined with a low-dose dipyridamole infusion to evaluate the coronary artery bypass graft patency.
PATIENTS AND METHODS Twenty-three consecutive patients (21 men, 2 women; mean age, 56 ± 6 years) undergoing coronary angiography because of recurrence of anginal symptoms 5 ± 2 years
841
Journal of the American Society of Echocardiography October 1999
842 De Simone et al
A
B
Figure 1 Doppler flow velocity recorded (A) from patency left internal mammary artery graft and (B) from normal descending anterior coronary artery. A, Characteristic Doppler velocity flow recorded from patent left internal mammary artery graft. Flow is biphasic, with prevalent diastolic velocity. Green, electrocardiogram; grey, left internal mammary artery graft flow. B, Doppler velocity profile in distal tract of patent descending anterior coronary. Flow is biphasic, with prevalent diastolic component. Green, Electrocardiogram; Orange, coronary flow.
after a coronary artery bypass graft were studied. We analyzed 25 mammary grafts (23 LIMA, 2 RIMA). Five patients had an anastomosis of the isolated LIMA graft performed to the LAD, 16 patients had an LIMA graft to the LAD and also a saphenous vein graft, and 2 patients had a LIMA graft to the LAD and an RIMA graft to the RCA. The clinical characteristic of the patients are shown in Table 1.
Echocardiography was performed with a Sequoia ultrasound machine (Acuson Corporation, Mountain View, Calif) equipped with a new color Doppler function: the nondirectional Doppler independent from the direction of the flow but, unlike the traditional Doppler, dependent on the quantity of the blood flow in the vessel analyzed. Compared with the traditional Doppler echocardiography,
Journal of the American Society of Echocardiography Volume 12 Number 10
De Simone et al 843
Table 1 Clinical characteristics of the patients Patients Age (y) Previous myocardial infarction
23 56 ± 6 11/23
Previous unstable angina Time from CABG Bypass
12/23 5±2 5 16 2 8/23 16/23 6/23
Typical chest pain Atypical chest pain Positive provocative tests
21 M, 2 F Anterior myocardial infarction 7/11 Inferior myocardial infarction 4/11
Isolated LIMA to DA LIMA to DA + saphenous vein graft LIMA to DA + RIMA to RCA 35% 69% 23%
CABG, Coronary artery bypass graft; LIMA, left internal mammary artery; DA, descending anterior coronary artery; RIMA, right internal mammary artery; RCA, right coronary artery.
this method is less influenced by the aliasing and also more sensible in detecting low-flow velocities and reduced blood volumes. The Sequoia machine was equipped with a small transthoracic multihertz Vector transducer (3.5 to 7 MHz) easily adaptable to narrow intercostal spaces. Patients were examined in the left lateral position with the use of a left parasternal window, and the long-axis sections were adjusted to identify the LIMA and RIMA grafts in nondirectional Doppler and in 2-dimensional echocardiography7 from their origin in the subclavian artery to the anastomosis to the coronary artery. Once the position of the mammary artery was identified, intraluminal flow signals were obtained with the pulsed Doppler method. The sampling volume was located within the vessel lumen with the most perpendicular position to the long axis of the artery. In all cases a biphasic pattern of blood flow corresponding to systolic and diastolic waves was detected (Figure 1, A). The IMAG showed a gradual transition in the phasic flow pattern from predominant systolic velocity proximally (at the origin from the subclavian artery)8 to predominant diastolic velocity distally (next to the anastomosis with the coronary artery).9 Therefore in our assessment of the IMAG flow velocities, we chose to use a parasternal window near the anastomosis instead of a subclavicular approach to avoid the influence of the subclavian artery flow velocity. However, the search for the best transthoracic window is essential for minimizing the angle between the Doppler beam and the long axis of the artery. With the transthoracic approach, in only 3 patients (2 with RIMA) of our study did we need to correct the angle between the Doppler beam and the blood flow approximately 30° to 40° as a result of the anatomic position of the vessel. At baseline the following parameters were obtained: systolic (SPV) and diastolic peak velocities (DPV), systolic (SVI) and diastolic velocity-time integrals (DVI), the diastolic-to-systolic peak velocity ratio (DPV/SPV) and the velocity-time integrals ratio (DVI/SVI), the diastolic frac-
Table 2 Clinical and echocardiographic data in group A and group B patients Group A
Group B
Patients 12 11 Age (y) 60 ± 6.7 55 ± 11 Graft 12 LIMA 9 LIMA, 2 RIMA DPV m/s 0.33 ± 0.13 0.12 ± 0.03 SPV m/sc 0.2 ± 0.09 0.27 ± 0.051 DPV/SPV 1.79 ± 0.47 0.46 ± 0.05 DVI (m) 0.11 ± 0.042 0.055 ± 0.02 SVI (m) 0.041 ± 0.03 0.06 ± 0.02 DVI/SVI 3.4 ± 1.3 0.93 ± 0.15 DVI/DVI + SVI 0.74 ± 0.08 0.47 ± 0.04 FR 1.8 ± 0.4 1.3 ± 0.41
P value
NS .0004 .05 .00005 .002 NS .0005 .0002 .009
LIMA, Left internal mammary artery graft; RIMA, right internal mammary artery graft; DPV, diastolic peak velocities; SPV, systolic peak velocities; DPV/SPV, systolic–to–diastolic peak velocity ratio; DVI, diastolic velocitytime integral; SVI, systolic velocity–time integral; DVI/SVI, systolic–todiastolic velocity – time integrals ratio; DVI/DVI + SVI, diastolic fraction of velocity – time integral; FR, dipyridamole infusion to baseline ratio of peak diastolic velocities.
tion of the velocity-time integral (ie, the diastolic velocitytime integral divided by the diastolic plus systolic velocitytime integrals: DVI/DVI+SVI). On the basis of the baseline mammary flow pattern, 2 groups of patients were selected: group A (n = 12 patients, 12 LIMA grafts), with a DPV/SPV >1, and group B (n = 11 patients, 11 LIMA grafts, 2 RIMA grafts), with a DPV/SPV <1. Subsequently, a low-dose dipyridamole infusion (0.56 mg/kg in 4 minutes) was performed during the detection of blood flow velocities in both LIMA and RIMA grafts. Blood pressure and electrocardiography were monitored throughout the entire protocol. We also calculated the dipyridamole infusion to baseline ratio of peak diastolic velocities, which was an index of the internal mammary artery graft blood FR. All images were recorded on a magneto-optical disk and analyzed later by 2 observers who were blinded to the angiographic result.
Journal of the American Society of Echocardiography October 1999
844 De Simone et al
A
B
Figure 2 Doppler flow velocity recorded (A) from occluded left internal mammary artery graft, (B) from normal internal mammary artery. A, Characteristic basal Doppler velocity flow recorded from occluded left internal mammary artery graft. Flow is biphasic, with maximum velocity occurring during systole, like native internal mammary artery. Very low velocity is recorded during diastole. Green, electrocardiogram; orange, flow in left internal mammary artery graft. B, Doppler Velocity profile in native internal mammary artery with characteristic prevalent systolic peak. Green, electrocardiogram; orange, internal mammary artery flow.
Coronary angiography was performed within a week after echocardiographic study by a standard Judkins technique. LIMA and RIMA grafts were examined with the use of multiple projections, and the stenosis were classified according to visually determined percent narrowing as severe (>70%), moderate (40% to 70%), and normal (<40%).
Statistics Data are expressed as mean values ± SD. Student paired t test was used for statistical analysis. A P value < .05 was considered statistically significant. We also calculated the sensibility and specificity of the test at baseline and after dipyridamole infusion for the assessment of the graft patency.
Journal of the American Society of Echocardiography Volume 12 Number 10
De Simone et al 845
Table 3 Echo-Doppler data in group A and group B patients at baseline and after Dipyridamole infusion Group A Baseline
DPV (m/s) SPV (m/s) DPV/SPV DVI (m) SVI (m) DVI/SVI DVI/DVI+SVI
0.33 0.2 1.79 0.11 0.04 3.4 0.74
± ± ± ± ± ± ±
0.13 0.09 0.47 0.04 0.03 1.3 0.08
Group B
Dipyridamole infusion
0.51 0.3 1.8 0.22 0.066 3.6 0.79
± ± ± ± ± ± ±
0.1 0.13 0.43 0.08 0.03 1.15 0.09
P value
.005 .04 NS .0002 .045 NS NS
Baseline
0.12 0.27 0.46 0.055 0.06 0.93 0.47
± ± ± ± ± ± ±
0.032 0.05 0.05 0.03 0.02 0.15 0.04
Dipyridamole infusion
0.13 0.27 0.5 0.053 0.06 0.9 0.46
± ± ± ± ± ± ±
0.03 0.04 0.09 0.02 0.02 0.13 0.04
P value
NS NS NS NS NS NS NS
DPV, Diastolic peak velocities; SPV, systolic peak velocities; DPV/SPV, systolic–to–diastolic peak velocity ratio; DVI, diastolic velocity-time integral; SVI, systolic velocity – time integral; DVI/SVI, systolic–to diastolic velocity – time integrals ratio; DVI/DVI + SVI, diastolic fraction of velocity – time integral.
Table 4 Echo-Doppler data in 2 subgroups of group B patients Group B1 (n = 6 grafts) Baseline
DPV (m/s) SPV (m/s) DPV/SPV DVI (m) SVI (m) DVI/SVI DVI/DVI+SVI
0.16 0.22 0.7 0.08 0.05 1.6 0.6
± ± ± ± ± ± ±
0.04 0.02 0.15 0.016 0.01 0.3 0.04
Dipyridamole infusion
0.29 0.33 0.99 0.16 0.08 2.03 0.65
± ± ± ± ± ± ±
0.09 0.09 0.5 0.05 0.02 0.6 0.08
Group B2 (n = 7 grafts) P value
.09 .01 .2 .0001 .008 NS NS
Baseline
0.12 0.25 0.46 0.05 0.05 0.9 0.55
± ± ± ± ± ± ±
0.03 0.06 0.04 0.02 0.02 0.15 0.04
Dipyridamole infusion
0.13 0.26 0.5 0.05 0.05 0.9 0.5
± ± ± ± ± ± ±
0.03 0.04 0.08 0.01 0.02 0.16 0.04
P value
NS NS NS NS NS NS NS
DPV, Diastolic peak velocities; SPV, systolic peak velocities; DPV/SPV, systolic–to–diastolic peak velocity ratio; DVI, diastolic velocity - time integral; SVI, systolic velocity – time integral; DVI/SVI, systolic–to diastolic velocity – time integrals ratio; DVI/DVI + SVI, diastolic fraction of velocity – time integral.
RESULTS LIMA and RIMA grafts were identified in all the patients in the study by the parasternal window. In 18 (78%) of 23 patients, the vessel was followed from its origin from the subclavian artery to the anastomosis to the coronary artery. Intraluminal flow signals obtained with the pulsed Doppler method showed a typical biphasic flow pattern characterized by a prevalent diastolic component (Figure 1, A). On the contrary, in the ungrafted internal mammary artery, the flow was dominant during systole, and low-velocity profiles were recorded during diastole (Figure 2, A). The parameters obtained in the 2 groups at baseline are expressed in Table 2. After dipyridamole infusion was performed, flow velocities increased in 11 (91%) of 12 mammary grafts in group A and in 6 (46%) of 13 mammary grafts in group B. In group A the DPV increased from 0.33 ± 0.12 to 0.51 ± 0.11 m/s (P = .005), the SPV increased from 0.2 ± 0.09 to 0.3 ± 0.13 m/s (P = .04), the DPV/SPV ratio increased from 1.79 ± 0.47 to 1.8 ± 0.43 (P = not significant [NS]), the DVI increased from 0.11 ± 0.04 to 0.22 ± 0.08 m (P = .0002), the
SVI increased from 0.04 ± 0.03 to 0.066 ± 0.03 m (P = .045), the DVI/SVI increased from 3.4 ± 1.3 to 3.6 ± 1.15 (P = NS), the diastolic fraction increased from 0.74 ± 0.08 to 0.79 ± 0.09 (P = NS), and the FR was 1.8 ± 0.4. In group B the DPV increased from 0.12 ± 0.032 to 0.13 ± 0.03 (P = NS), the SPV increased from 0.27 ± 0.05 to 0.27 ± 10.04 (P = NS), the DPV/SPV ratio increased from 0.46 ± 0.05 to 0.5 ± 0.09 (P = NS), the DVI increased from 0.055 ± 0.03 to 0.053 ± 0.02 (P = NS), the SVI increased from 0.06 ± 0.02 to 0.06 ± 0.02 (P = NS), the DVI/SVI ratio increased from 0.93 ± 0.15 to 0.9 ± 0.13 (P = NS), the diastolic fraction increased from 0.47 ± 0.04 to 0.46 ± 0.04 (P = NS), and the FR was 1.3 ± 0.41. Data are also expressed in Table 3. In group B we selected 2 subgroups: group B1, with a baseline DPV/SPV ratio <1 that increased after dipyridamole infusion, and group B2, with a DPV/SPV ratio at rest <1 that did not increase after dipyridamole infusion. Data are summarized in Table 4. Assessment of reproducibility of IMAG flow in 10 randomly selected patients (5 of group A, 5 of group B) revealed an intraobserver mean error of 4% ± 1% and an interobserver error of 5% ± 1.5%.
Journal of the American Society of Echocardiography October 1999
846 De Simone et al
A
B
Figure 3 Doppler velocity flow recorded from patent left internal mammary artery graft before (A) and after (B) dipyridamole infusion. A, At baseline, ratio between systolic and diastolic peak is approximately 1. B, After dipyridamole infusion, diastolic velocity is more increased than systolic velocity, and ratio between systolic and diastolic peak is normalized (<1). Green, electrocardiogram; orange, left internal mammary artery graft flow.
Coronary angiography performed within 7 days from echocardiography showed the graft patency and the native LAD patency distal to anastomosis in all the patients in group A and in 5 patients in subgroup B1 (with 6 mammary grafts) showing increased flow velocity after dipyridamole infusion. In the identification of a significant graft stenosis, the DPV/SPV ratio showed at baseline 100% sensibility and 58% specificity, whereas the variation of FR after
dipyridamole infusion presented 92% sensibility and 84% specificity.
DISCUSSION Coronary artery bypass conduits derived from internal mammary arteries are used more and more in the surgical therapy of ischemic heart diseases because
Journal of the American Society of Echocardiography Volume 12 Number 10
De Simone et al 847
A
B
Figure 4 Doppler velocity flow recorded from occluded left internal mammary artery graft before (A) and after (B) dipyridamole infusion. A, At baseline, systolic velocity is prevalent. B, After dipyridamole infusion, no increase of velocity is registered. Flow is similar to baseline. Green, electrocardiogram; orange, left internal mammary artery graft flow.
of their significantly improved long-term patency compared with saphenous vein graft.1 A noninvasive method that allows the identification of the IMAG, the measurement of blood flow, and the assessment of its short- and long-term patency may represent a useful technique in the diagnostic evaluation of patients with ischemia. The rate of direct visualization of the native internal mammary artery is already 100%,7 whereas the visualization of LIMA graft has been attempted in previous studies with a rate of detection variable from 70% to 95%.2,3,8-11 The mobilization of
the internal mammary artery with its neurovascular peduncle during coronary artery bypass grafting may change the anatomic disposition of the vessel. This change may result in a difficult detection of IMAG, especially next to the distal anastomosis to the coronary artery. In our study both the use of a small transthoracic multihertz transducer and the application of new echocardiographic software has led to the visualization of both LIMA and RIMA grafts in all the patients. The new software allows analysis of Doppler flow intensity in the vessels and also the visualization of low velocities
848 De Simone et al
and reduced blood volume. It is independent to flow direction. IMAG without significant stenosis showed a typical pulsed Doppler flow pattern (Figure 1, A) similar to that of a coronary artery (Figure 1, B), characterized by a prevalent diastolic component,3,9-12 with both peak velocities and velocity-time integrals higher in diastole than in systole. On the contrary, in patients with occluded IMAGs or IMAGs with severe stenosis, low velocity profiles were recorded during diastole, with an increase of the systolic component (Figure 2, A). As a result, at baseline flow was dominant during systole,3 and the IMAG velocity flow pattern in these cases was similar to that detected in the ungrafted internal mammary artery (Figure 2, B). As a result of our study, we may propose a new Doppler index for the assessment of the IMAG patency. In the literature previous invasive13,14 and noninvasive3,11,15 studies about the internal mammary artery evaluation already showed that at baseline, both a DPV/SPV ratio <0.6 and a diastolic fraction of the velocity-time integral <0.5 predicted severe stenosis of the IMAG. In our experience all of the patients in group A with a baseline DPV/SPV ratio >1 showed IMAG graft angiographic patency; consequently, dipyridamole infusion did not contribute new information in patients with normal DPV/SPV ratios at rest. All the mammary grafts of the patients in group B showed a DPV/SPV ratio <1 at baseline, 8 of 13 a ratio <0.6, and 7 of 13 a diastolic fraction of the velocity-time integral <0.5. However, a DPV/SPV ratio <0.6 may also be detected in patients with a patent IMAG,3 suggesting that this index has a low specificity. In this case and in all dubious cases, a low-dose infusion of dipyridamole may lead to the assessment of the functional impairment of the vessel. In fact, in our experience the dipyridamole infusion increased flow velocities up to 50% compared with baseline in 11 of 12 patients in group A, with an FR of 1.8 ± 0.4 and in 5 of 11 patients (6 mammary grafts) in subgroup B1, with an FR of 1.84 ± 0.23 (Figure 3), whereas in 6 of 11 patients (7 mammary grafts) in subgroup B2, no significant increase in flow parameters was observed after dipyridamole infusion (Figure 4). Coronary angiography showed a severe (>70%) stenosis of the graft in patients of subgroup B2 only. As a result the response of the internal mammary artery flow velocities to the dipyridamole infusion may distinguish patients with critical versus noncritical graft stenosis.
Journal of the American Society of Echocardiography October 1999
Study Limitations Although measurements of IMAG flow velocities with the use of transthoracic echocardiography have been shown to be feasible, the examination may present some technical problems. As a consequence a stage of learning of the evaluation of the grafts may be useful before this method is used routinely. In some cases a correction of the angle between the Doppler beam and the long axis of the vessel may be necessary; this could lead to undervaluing of the flow velocities. Furthermore a larger population of patients is required to assess the real clinical impact of this technique to the follow-up of patients with IMAG. Future Advances Last generation ultrasound systems equipped with second harmonic technology allow the visualization of the distal portion of the LAD and the analysis of flow velocities within the vessel.12 Therefore the evaluation of both internal mammary artery and native LAD distal to the anastomosis at the same time might give further information for the assessment of the functional significance of a stenotic lesion of the graft. Conclusions The color Doppler echocardiographic evaluation of the IMAG is a simple noninvasive method to assess the functional impairment of the vessel at baseline. Our study showed that with this technique, it may be possible to (1) visualize both LIMA and RIMA grafts, (2) analyze the pulsed Doppler flow patterns of the IMAG with the use of transthoracic echocardiography, and (3) assess the patency and the functional status of the IMAG both at rest and after dipyridamole infusion. In dubious cases with an DPV/SPV ratio equal or inferior to 1 at rest, the infusion of low doses of dipyridamole may increase almost to 50% all the flow velocities, especially the diastolic ones, allowing an indirect assessment of the functional status of the graft. In conclusion, color Doppler assessment of IMAG may represent a filter to the coronary angiography, especially in patients with nondiagnostic clinical signs and provocative tests. REFERENCES 1. Grondin CM, Campeau L, Lesperance J, Enjalbert M, Bourassa MG. Comparison of late changes in internal mammary artery and saphenous vein graft in two consecutive
Journal of the American Society of Echocardiography Volume 12 Number 10
2.
3.
4.
5.
6.
7.
8.
series of patients 10 years after operation. Circulation 1984; 70:I208-212. Crowley JJ, Shapiro LM. Noninvasive assessment of left internal mammary artery graft patency using transthoracic echocardiography. Circulation 1995;92(suppl II):25-30. Rombaut E, Vantrimpont P, Gurné O, et al. Noninvasive functional assessment of left internal mammary artery grafts by transcutaneous Doppler echocardiography. J Am Soc Echocardiogr 1998;11:403-8. Pezzano A, Cali G, Milazzo A, et al. Transthoracic 2D echo color Doppler assessment of internal mammary artery to left anterior descending coronary artery graft. Int J Card Imaging 1995;11:177-84. Fitzgibbon GB, Leach AJ, Kafka HP, Keon WJ. Coronary bypass graft fate: long term angiographic study. J Am Coll Cardiol 1991;17:1075-80. Kyo S, Matsamura N, Yokote Y, Takamoto S, Omoto R. Evaluation of patency of internal mammary artery grafts: a comparison of two–dimensional Doppler echocardiography and coronary angiography. J Cardiol 1990;20:606-16. Ehrsam JE, Spittel PC, Seward JB. Internal mammary artery: 100% visualization using new ultrasound technology. J Am Soc Echocardiogr 1998;11:10-2. Krijne R, Lyttwin RM, Holtgen R, Heinrich KW. Doppler sonographic examination of the internal mammary artery graft: comparison of supraclavicular and high intercostal signals. Cardiology 1993;82:48-50.
De Simone et al 849
9. Voci P, Plaustro G, Testa G, Marino B, Campa PP. Visualizzazione delle arterie mammarie interne native e del graft aortocorarico con ecocardiografia color Doppler ad alta risoluzione. Cardiologia 1998;43:403-6. 10. Bruni A., Chirillo F, Cavallini C, Stritoni P. Studio dei bypass aorto-coronarici con Eco Bidimensionale e Color-Doppler transtoracico. Emodinamica 1998;13:2-5. 11. El Masri M, Salama M, Darwish A. Assessment of left internal mammary artery graft patency by transthoracic Doppler echocardiografphy [abstract]. Eur Heart J 1998;19:66 (P544). 12. Hozumi T, Yoshida K, Ogata Y, et al. Noninvasive assessment of significant left anterior descending artery stenosis by coronary flow velocity reserve with transthoracic color Doppler echocardiography. Circulation 1998;97:1557-62. 13. Bach RG, Kern MJ, Donohue TJ, Aguirre FV, Caracciolo EA. Comparison of phasic blood flow velocity characteristics of arterial and venous coronary artery bypass conduits. Circulation 1993;88:II133-140. 14. Gurné O, Chenu P, Polidori C, et al. Functional evaluation of internal mammary artery bypass grafts in the early and late postoperative periods. J Am Coll Cardiol 1995;25: 1120-8. 15. Takagi T, Yoshikawa J, Yoshida K, Akasaka T. Noninvasive assessment of left internal mammary artery graft patency using duplex Doppler echocardiography from the supraclavicular fossa. J Am Soc Echocardiogr 1993;6:374-81.