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Ann Thorac Surg 1995;59:1528-1532
© 1995 The Society of Thoracic Surgeons

Clinical Significance of Reverse Redistribution Phenomenon After Coronary Artery Bypass Grafting

Shoji Watarida, MD, Masahiko Onoe, MD, Takaaki Sugita, MD, Ryoko Tabata, MD, Kazuhiko Katsuyama, MD, Yasuhiko Nakajima, MD, Takehisa Nojima, MD, Rie Yamamoto, MD, Shuichi Matsuno, MD, Atsumi Mori, MD

Second Department of Surgery, Shiga University of Medical Science, Shiga, Japan

Accepted for publication February 22, 1995.


   Abstract
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 Footnotes
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
The reverse redistribution (RR) phenomenon is a decrease in thallium 201 uptake during redistribution compared with 201Tl uptake immediately after exercise. We evaluated RR in 23 patients after coronary artery bypass grafting. Postoperative RR was present in 48% and was significantly more common in patients with a history of myocardial infarction (62%). The patients were classified according to the presence (+) or absence (-) of RR. An analysis of left ventricular wall motion showed significant improvement after coronary artery bypass grafting in the RR+ group (n = 12) but not in the RR- group (n = 11). Quantitative myocardial viability was evaluated using the defect volume ratio, mean defect severity, and defect severity index. The preoperative defect volume ratio was higher in the RR+ group than in the RR- group (p < 0.05). In the RR- group, no improvement in these indices was observed after operation. In contrast, the RR+ group showed significant improvement in all three indices (p < 0.05). These results indicate that after coronary artery bypass grafting, an adequate blood supply to the remaining myocardium may induce RR. This phenomenon, therefore, may be a significant indicator of postoperative myocardial viability.


   Introduction
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 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
See also page 1532.

A common noninvasive assessment of coronary revascularization is performed using thallium 201 single-photon emission computed tomography (SPECT) of the myocardium after exercise. The assessment of myocardial ischemia by this technique depends on whether redistribution is present in the area of low 201Tl uptake immediately after exercise. Occasionally, we encounter the reverse redistribution (RR) phenomenon in which 201Tl uptake increases during exercise but decreases during redistribution after exercise. Reverse redistribution was reported in 1979 by Tanasescu and associates [1]. Its etiology remains unclear despite a number of studies that followed that initial report. Tanasescu and co-workers suggested that RR may represent a higher rate of 201Tl washout from a segment with the phenomenon than from adjacent segments possibly because of increased relative regional blood flow. The clinical significance of RR after coronary artery bypass grafting (CABG) has not been yet defined. In this study, we investigated the clinical significance of RR in patients undergoing CABG.


   Patients and Methods
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 Footnotes
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Patient Population
Between March 1, 1989, and January 31, 1990, we studied 23 consecutive patients who underwent 201Tl exercise myocardial SPECT before and after CABG that included the left anterior descending coronary artery (LAD). There were 22 men and 1 woman. Age at operation ranged from 44 to 72 years with a mean of 57.4 ± 7.2 years. The mean number of grafts per patient was 2.5 ± 0.7 (range, 1 to 4). Autografts for the LAD were obtained from the great saphenous vein in 18 patients and from the left internal thoracic artery in 5. Thirteen patients had a history of preoperative anteroseptal myocardial infarction (MI) in the area perfused by the LAD. No patient had evidence of perioperative MI. Thallium 201 exercise myocardial SPECT was performed between postoperative days 28 and 96 (mean time, postoperative day 59). The mean interval between MI and operation was 3.8 ± 2.3 months (range, 1.5 to 8 months). The study was approved by the institutional review board, and informed consent was obtained from each patient.

201Tl Exercise Myocardial SPECT
The patients performed a symptom-limited multistep-exercise treadmill test according to Bruce's protocol. Three millicuries of 201Tl was injected intravenously at maximum exercise, and the patient continued exercising for an additional minute. The 201Tl myocardial SPECT images were made through a 180-degree rotation (64 x 64 matrix, 32 steps) with a Gamma View-D rotation scintillation camera (Hitachi Medico). The collimator rotated 180 degrees around the patient's chest from the left lateral to the right lateral position, obtaining 30 projections 6 degrees apart. Each projection took 30 seconds to obtain. Three-hour delayed images were also made. The 201Tl myocardial SPECT images were analyzed with a HARP RP100 (Hitachi Medico) for data processor. Short-axial images of the left ventricle were shown in a ``bull's-eye view'' by the circumferential profile method and in a ``bullet'' display, a three-dimensional display model of the left ventricle. With the ``bullet'' in the right anterior oblique view, the perfusion area of the LAD was analyzed. The relationship between the bullet display and the perfusion area of the LAD are illustrated in Figure 1Go. The highest count of 201Tl uptake measured in the entire heart was defined as 100% uptake, and the counts in each segment were expressed as percent Tl (%Tl) uptake.



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  		Fig 1. . Relationship between bullet display and perfusion area of left anterior descending coronary artery.

 
Classification of RR Groups
Positive reverse redistribution was considered to be present when the %Tl uptake in the delayed image was reduced in the same area by at least 30% compared with the initial image (RR+ group). Absence of reverse redistribution was defined as %Tl uptake of 70% or higher in the delayed image compared with initial image (RR- group).

Postoperative Coronary and Left Ventricular Angiography
After CABG, coronary angiography and left ventricular angiography were performed between postoperative days 35 and 105 (mean time, postoperative day 62). All LAD grafts were patent on postoperative coronary angiography. The interval between postoperative left ventricular angiography and postoperative 201Tl exercise myocardial SPECT was 3 to 34 days (mean time, 18 days).

Analysis of Myocardial Viability
Myocardial viability was evaluated by analysis of left ventricular wall motion and quantitative analysis.

ANALYSIS OF LEFT VENTRICULAR WALL MOTION.
Preoperative to postoperative changes in left ventricular wall motion were investigated in the two RR groups using the left ventricular angiograms. Left ventricular wall motion was analyzed by the method of Pujadas [2] (Fig 2Go). End-diastolic and end-systolic images of the left ventricular angiogram were divided into five segments according to the criteria of the American Heart Association: anterobasal, anterolateral, apical, diaphragmatic, and posterobasal. The preoperative to postoperative changes in the total rate of shortening (shortening ratio) of the segments primarily perfused by the LAD, the anterobasal and anterolateral walls, were evaluated in the right anterior oblique view of the left ventricular angiogram.



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  		Fig 2. . Left ventricular wall motion as analyzed by method of Pujadas [2]. The shortening ratio was defined as the total rate of shortening of the anterobasal and anterolateral left ventricular walls in the right anterior oblique view of the left ventricular angiogram: shortening ratio = (b/a + d/c) x 100%.

 
QUANTITATIVE ANALYSIS.
A quantitative analysis of the 201Tl exercise myocardial SPECT image was performed using the method presented in Figure 3Go [3–5]. Each delayed short-axial image of the left ventricle was divided into 16 rings at equal intervals from the apex in the direction of the long axis. From the center of each of these rings, 60 radial lines were drawn at intervals of 6 degrees. The highest count on these lines and the distance from the center of this point were determined. The count at each point was expressed as the percentage of the highest count in the entire heart (%Tl uptake), and a circumferential profile curve was prepared from this value for each slice [6].



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  		Fig 3. . Quantitative analysis of myocardial viability by 201Tl exercise myocardial SPECT: (A) delayed short-axial image of left ventricle divided into 16 rings at equal intervals; (B) 60 radial lines at intervals of 6 degrees drawn from center of each ring; (C) number of defective segments in slice n (Nn) and lower limit value in slice n - %Tl uptake value in slice n (un); and (D) volume of one segment in a slice where n = (2{pi}rn x h x d)/60. DVR (defect volume ratio) = myocardial volume in the defect area/total myocardial volume = ({Sigma}2{pi}rn/60 x h x d x Nn)/({Sigma}2{pi}rn x h x d). MDS (mean defect severity) = total defect intensity/myocardial volume in the defect area = ({Sigma}{Delta}Un x 2{pi}rn/60 x h x d)/({Sigma}2{pi}rn/60 x h x d x Nn). (SD = standard deviation.)

 
Using the lower limit of normal (mean - 2 standard deviations) derived from 20 healthy controls as the lower limit, the ratio of a point showing a lower level the entire heart was corrected by the radius of each slice as a defect volume ratio (DVR): DVR = myocardial volume in defect area/total myocardial volume.

The difference from the lower limit was corrected by the radius of each slice and averaged as the mean defect severity (MDS): MDS = total defect intensity/myocardial volume in defect area.

The DVR was multiplied by the MDS to obtain a defect severity index (DSI). Changes in DVR, MDS, and DSI were evaluated prior to and after operation.

Statistical Analysis
Comparison of results in the RR+ and RR- groups was done by paired Student t test with significance determined at a probability of less than 0.05. The data are expressed as the mean ± the standard deviation.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Preoperatively, all patients exhibited redistribution in the perfusion area of the LAD (Table 1Go). Postoperatively, RR was observed in 11 patients (48%) (RR+ group). The other 12 patients without postoperative RR did not show postoperative redistribution or ischemic signs. Eight patients (73%) in the RR+ group and 5 patients (42%) in the RR- group had a history of preoperative anteroseptal MI. Therefore, 13 of the 23 patients had experienced a preoperative anteroseptal MI (Table 2Go), and 8 of them showed RR. These 8 patients constituted 62% of the patients who had experienced an MI. Thus, the incidence of RR was higher among the patients with a history of preoperative MI (p = 0.05 by {chi}2 analysis).


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  		Table 1. . Incidence of Redistribution and Reverse Redistribution
 

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  		Table 2. . Association Between Postoperative Reverse Redistribution and Preoperative Myocardial Infarction
 
The bullet display from a patient with postoperative RR is shown in Figure 4Go. This patient had a history of preoperative anteroseptal MI and underwent three-vessel CABG involving the middle portion of the right coronary artery, the proximal LAD, and the first diagonal branch. The preoperative images show a marked decrease in %Tl uptake with redistribution in the anterobasal and anterolateral walls. The %Tl uptake in the perfusion area of the LAD, especially in the first diagonal branch, increased postoperatively and demonstrated positive RR in the anterolateral wall.



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  		Fig 4. . Bullet display of patient with postoperative reverse redistribution (RR). The patient had a history of anteroseptal myocardial infarction and underwent three-vessel bypass grafting (middle portion of right coronary artery, proximal LAD, first diagonal branch). The upper two scans are preoperative images and the lower two, postoperative images. The left side shows initial images and the right side, delayed images. Postoperatively, 201Tl uptake in perfusion area of LAD increased with RR at anterobasal and anterolateral walls. Arrow points out area of RR.

 
Left Ventricular Wall Motion
In the RR- group, the postoperative shortening ratio showed no significant improvement (from 121% ± 27% to 103% ± 32%) (Fig 5Go). In the RR+ group, the postoperative shortening ratio showed a significant improvement from 65% ± 24% to 101% ± 35%. Preoperatively, this group had a lower rate of shortening than the RR- group (p < 0.05), a finding indicating a decrease in wall motion caused by preoperative ischemia.



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  		Fig 5. . Analysis of left ventricular wall motion. (N.S. = not significant; RR = reverse redistribution; S.D. = standard deviation; * = p < 0.05 versus preoperative shortening ratio of RR(-) group.)

 
Quantitative Data
The RR+ group exhibited significant postoperative decreases (p < 0.05) in DVR (from 50.9 ± 18.6 to 35.8 ± 14.3), MDS (from 11.2 ± 5.2 to 8.1 ± 4.1), and DSI (from 6.1 ± 4.2 to 3.7 ± 3.7). In contrast, the RR- group showed no significant differences in DVR (from 37.6 ± 9.8 to 36.4 ± 10.2), MDS (from 11.7 ± 5.2 to 9.2 ± 5.4), and DSI (from 4.7 ± 2.9 to 3.9 ± 2.5). Preoperatively, the RR+ group had a higher DVR than the RR- group (p < 0.05).


   Comment
Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
Matsuda and associates [7] studied 33 patients with RR and found that it was significantly more common in patients with myocardial damage than in patients without such damage. These authors suggested that RR is related to revascularization of areas damaged by prior MI. In a study by Nishimura and co-workers [8], patients who underwent CABG and had RR showed a higher coronary blood flow and washout in the bypass graft region compared with regions that did not require bypass grafting. The myocardium in the region with RR during the acute period of an infarction may still be viable and may possibly be protected from myocardial damage and necrosis by recanalization of the coronary artery [9].

In our study, postoperative RR was more common in patients with a history of preoperative MI. In the RR+ group, postoperative left ventricular wall motion and postoperative DVR, MDS, and DSI were improved significantly. These findings indicate that RR occurs in many patients whose preoperative myocardial viability has been decreased because of associated MI. Our results also suggest that postoperative RR is common in patients with severe ischemic injury and that CABG successfully supplies the remaining myocardium with an adequate blood flow. Postoperative RR, therefore, may be a useful indicator of residual myocardial viability.

In our study, the mechanism of RR was thought to result from the reestablishment of satisfactory blood flow to a region with both scarred and normal areas of myocardium, the normal area showing greater 201Tl uptake after exercise than the ischemic portion. When RR occurred, however, the ischemic region showed 201Tl uptake, whereas the scarred area in this mixed region showed no uptake, and the 201Tl was satisfactorily washed out from the normal area. Weiss and colleagues [10] reported that after reperfusion, the washout of 201Tl in an area of MI in humans was rapid. Aoki and associates [11] analyzed the etiology of RR in the early stage after percutaneous transluminal coronary angioplasty and obtained results similar to ours but suggested that the RR phenomenon occurs primarily in minimally damaged myocardium.

Hecht and coauthors [12] reported an RR incidence of 7% and Silberstein and DeVris [13], an incidence of 5%. Nishimura and colleagues [14] found a 21% incidence of RR after CABG. In our study, the incidence of postoperative RR was high, 48%, and this may be due to the high rate of associated prior MI in our patients and the high incidence of advanced coronary lesions that had progressed despite percutaneous transluminal coronary angioplasty.

We used the bullet display, a three-dimensional display model of the left ventricle, for the assessment of RR because the course of the coronary arteries can be readily matched with the left ventricle and because the ischemic region can be easily localized and the area perfused by this coronary artery, analyzed for difference in blood flow distribution. A bullet display does not result in underestimation at the apex and overestimation at the base as does the conventional bull's-eye display [15].

In summary, we investigated the clinical significance of RR using 201Tl exercise myocardial SPECT before and after CABG. The patients exhibiting postoperative RR showed significant postoperative improvement in left ventricular wall motion compared with preoperative motion. The determination of the quantitative myocardial viability (DVR, MDS, and DSI) before and after operation revealed that patients exhibiting postoperative RR showed significant postoperative improvement in myocardial viability. The onset of RR after CABG suggests that the operation results in a sufficient supply of blood flow to the residual myocardium, indicating that the onset of RR is a highly useful indicator for postoperative assessments.



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  		Fig 6. . Quantitative analysis of myocardial viability. (DSI = defect severity index; DVR = defect volume ratio; MDS = mean defect severity; RR = reverse redistribution; S.D. = standard deviation.)

 

   Footnotes
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 Footnotes
Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Address reprint requests to Dr Watarida. Second Department of Surgery, Shiga University of Medical Science, Tsukinowa Seta, Otsu, Shiga, 520-21, Japan.


   References
Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Tanasescu D, Berman D, Staniloff H, Brachman M, Ramanna L, Waxman A. Apparent worsening of thallium-201 myocardial defect during redistribution-what does it mean? J Nucl Med 1979;20:688.
  2. Pujadas G. The ventriculogram: coronary angiography. New York: McGraw-Hill, 1980:142–8.
  3. Prigent F, Maddahi J, Garcia EV, et al. Quantification of myocardial infarct size by thallium-201 single-photon emission tomography: experimental validation in the dog. Circulation 1986;74:852–61.[Abstract/Free Full Text]
  4. Fujioka T, Sasaki J, Kashima K, et al. Quantitative evaluation of SPECT images using myocardial phantom: concentric circular display (bull's eye format). Med J Osaka Pol Hosp 1986;10:163–8.
  5. Matsumura Y, Komamura K, Yamamoto K, et al. Quantification of myocardial infarct size by thallium-201 myocardial scintigraphy. Med J Osaka Pol Hosp 1987;11:43–50.
  6. Burow RD, Pond M, Schafter AW, et al. Circumferential profiles: a new method for computer analysis of thallium-201 myocardial perfusion image. J Nucl Med 1979;20:771–7.[Abstract/Free Full Text]
  7. Matsuda H, Onoguchi M, Ootake E, et al. Reverse redistribution in the stress thallium scan: correction of coronary blood flow and myocardial damage. Kaku Igaku 1989;26: 55–60.[Medline]
  8. Nishimura T, Uehara T, Hayashida K, Kozuka T, Saito M, Sumiyoshi T. Reverse redistribution in the patient with aorto-coronary bypass surgery by stress thallium scan. Kaku Igaku 1985;22:1679–83.[Medline]
  9. Naka K, Motoki K, Ootani H, Naka Y. Long-term follow-up of thallium-201 myocardial scintigraphy in acute myocardial infarction-clinical significance of reverse redistribution during acute period. Kaku Igaku 1989;26:539–43.[Medline]
  10. Weiss AT, Maddahi J, Geft I, et al. ``Apparent worsening'' in late post streptokinase rest-redistribution Tl-201 scans: a sign of reperfused, viable myocardium [Abstract]. Circulation 1983;68(Suppl 3):245.
  11. Aoki T, Futagami Y, Konishi T, et al. Clinical significance of redistribution in exercise thallium-201 SPECT after percutaneous transluminal coronary angioplasty. Kaku Igaku 1989;26:821–8.[Medline]
  12. Hecht HS, Hoplums JM, Rose JG, Blumfield DE, Wong M. Reverse redistribution: worsening of thallium-201 myocardial images from exercise to redistribution. Radiology 1981;140:177–81.[Abstract/Free Full Text]
  13. Silberstein EB, DeVris DF. Reverse redistribution phenomenon in thallium-201 stress tests: angiographic correlation and clinical significance. J Nucl Med 1985;26:707–10.[Abstract/Free Full Text]
  14. Nishimura T, Uehara T, Hayashida K, Kozuka T. Clinical significance of 201-thallium reverse redistribution in patients with aorto-coronary bypass surgery. Eur J Nucl Med 1987;13:139–42.[Medline]
  15. Imai K, Ando T, Yukimura S, et al. Two-dimensional representation (bullet) method of the thallium-201 myocardial SPECT: comparison with polar map. Kaku Igaku 1987;24:865–9.[Medline]



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S. Watarida, S. Shiraishi, K. Katsuyama, Y. Nakajima, and A. Mori
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