Eur J Cardiothorac Surg 2003;23:347-353
© 2003 Elsevier Science NL
Diameter changes of occluded venous coronary artery bypass grafts in electron beam tomography: preliminary findings
Christian N.H. Enzweilera,b*,
Till H. Wiesea,
Jan Peterseina,
Alexander E. Lembckea,
Adrian C. Borgesc,
Pascal Dohmend,
Udo Hoffmannb,
Bernd Hamma
a Department of Radiology, Charité, Humboldt-Universität zu Berlin, Berlin, Germany
b Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA
c Department of Internal Medicine I, Charité, Humboldt-Universität zu Berlin, Berlin, Germany
d Department of Cardiothoracic Surgery, Charité, Humboldt-Universität zu Berlin, Berlin, Germany
Received 25 October 2002;
received in revised form 19 November 2002;
accepted 21 November 2002.
* Corresponding author. Tel.: +49-30-450-526117; fax: +49-30-450-527911
e-mail: christian.enzweiler{at}charite.de
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Abstract
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Objective: To differentiate acute from chronic graft occlusions through diameter measurements by means of electron beam tomography (EBT). Methods: Contrast enhanced EBT volume studies were carried out in 37 patients with one or more occluded venous coronary bypass grafts. Seventeen of 37 patients did not meet the inclusion criteria and were excluded from the assessment. The remaining 20 patients had a total of 39 bypasses (16 patent, 23 occluded) and were assigned to one of three groups: group A consisted of patent grafts only (patent grafts, 13 patients). Group B comprised 11 of 23 occluded grafts diagnosed within 10 days after bypass surgery (acutely occluded grafts, ten patients). Group C contained 12 of 23 bypass occlusions that were at least 6 months old as documented by coronary angiography (chronically occluded grafts, ten patients). The mean graft diameter was determined by repetitive measurements on a workstation through blinded readers. The Mann–Whitney-U-test for unpaired samples was used for statistical evaluation. Results: Mean graft diameter for groups A–C (patent, acutely, and chronically occluded bypasses, respectively) was 3.9 mm (±0.6; n=16), 5.4 mm (±1.9; n=11), and 0.3 mm (±.9; n=12), respectively (P<0.01 each). Sensitivity and specificity for the detection of acute and chronic occlusions were 87 and 92% (cut-off 4.5 mm), respectively, and 92 and 96% (cut-off 1 mm), respectively. Conclusions: EBT may allow for non-invasive differentiation between acute and chronic venous coronary bypass occlusions. This could help prevent unnecessary invasive recanalization procedures. Body veins may conserve their ability to increase in diameter in acute thrombosis when transplanted as coronary bypasses.
Key Words: Coronary vessels, diseases • Coronary vessels, stents and prostheses • Coronary vessels, surgery • Coronary vessels, computed tomography • Computed tomography, electron beam • Computed tomography, angiography
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1. Introduction
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Coronary artery disease (CAD) is a prime cause of morbidity and mortality in the industrialized nations. According to the Framingham study, it affects 28.7 out of 1000 people each year [1]. In the United States CAD causes 3.1 deaths per 1000 inhabitants annually, mainly due to complications as myocardial infarction and congestive heart failure [1–3]. The introduction of coronary bypass surgery in the late 1960s has contributed to a decline in mortality from CAD. Now 400,000 coronary bypass operations are performed in the United States each year [4].
Although revascularization of coronary arteries by means of bypass grafting is an effective treatment of advanced CAD, stenosis and occlusion of bypasses diminish the success of surgical therapy [4]. During the first year after bypass surgery up to 15% of venous grafts occlude. The attrition rate between 1 and 6 years and 6 and 10 years is 1–2 and 4% per year, respectively. After 10 years only 60% of vein grafts are patent and 50% of patent grafts show substantial stenosis [5–8].
Coronary angiography as the gold standard for the evaluation of coronary arteries and coronary bypasses is invasive and cannot determine the age of a graft occlusion. Electron beam tomography (EBT) has been proposed as an alternative non-invasive modality for the diagnostic assessment of coronary arteries and coronary bypasses. Sensitivity and specificity for the detection of high-grade stenoses or occlusions of the coronary arteries have been reported to be 92 and 94%, respectively, for evaluable vessels with, however, a high rate of non-evaluable vessels [9]. Determination of bypass patency by EBT relies on graft enhancement following intravenous administration of contrast material [10–13]. However, while the sensitivity and specificity for the diagnosis of coronary bypass occlusions both approach 100%, sensitivity for the detection of graft stenosis seems to be poor [11,12].
The foremost task of EBT in the diagnostic work-up of patients with coronary bypasses is to detect occluded or stenotic bypass grafts. Beyond the mere diagnosis of a bypass occlusion the ability to differentiate acute from chronic graft occlusion would enable the physician to link a patient's symptoms more closely to a bypass occlusion or help exclude a temporal or causal connection. The purpose of this study was to determine if EBT can discriminate acute from chronic graft occlusion and to assess if there is a difference in diameter between patent and occluded venous coronary bypasses.
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2. Materials and methods
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2.1. Patients
One hundred and fourteen consecutive patients with coronary artery bypass grafts referred for bypass assessment with contrast-enhanced EBT (Evolution scanner C-150 XP, Imatron, San Francisco, CA, USA) were scanned using an identical scanning protocol after giving informed written consent. The study was approved by our institutional review board. Thirty-seven of 114 patients (32.5%) had one or more occluded venous bypass grafts. Twenty of 37 patients with an occluded bypass fulfilled the inclusion criteria in that they either had had coronary bypass surgery within 10 days prior to the EBT examination or had undergone conventional coronary angiography 6 months or more before EBT. For our study we defined an acute bypass occlusion as an occlusion that occurred within 10 days of bypass surgery whereas an occlusion known for 6 months or more from a preceding coronary angiogram was considered to be chronic. Seventeen of 37 patients were excluded from further assessment as the catheter report showing bypass occlusion preceded the EBT-study by less than 6 months (n=2) or no catheter report was available (n=15).
2.2. Scanning technique
Sixty scans were acquired in the single slice mode (SSM) using a slice thickness of 3 mm and an increment of 2 mm. Exposure time was 100 ms per scan, the images were triggered to the electrocardiogram (ECG) at enddiastole (80% of the RR-interval). The field of view (FOV) was set at 15 cm, the matrix was 512x512 pixels. Patients were preoxygenated with 100% oxygen (NasOral device, Klinika Produktion, Neufra, Germany) to prolong the voluntary breathhold interval [14]. Total scanning time was 45–60 s. One hundred and eighty milliliters of Iopromide (iodine content 370 mg I/ml, Ultravist 370, Schering, Berlin, Germany) were intravenously administered at a flow rate of 3.0 ml/s via an antecubital vein.
2.3. Image analysis
The studies were randomized and evaluated on a workstation (MagicView, Siemens, Erlangen, Germany) by two radiologists in a consensus reading for the presence of bypass occlusions. The reviewers were blinded to the history of the patients, the total number of bypass grafts, the age of the bypass grafts, and the results of coronary angiography. Both the overall image quality and the adequacy of contrast enhancement of the ascending aorta were assessed by the reviewers (excellent, good, moderate, poor). Criteria for overall image quality and contrast enhancement were signal-to-noise ratio, motion or breathing artifacts, coverage of the volume of interest as well as contrast opacification throughout the scanned volume containing the bypasses, respectively. Only studies with a good or excellent overall image quality and a good or excellent contrast opacification of the aorta underwent further evaluation. A bypass graft was considered patent if contrast opacification was present over the entire length of the graft. A bypass graft was considered occluded if there was opacification of the origin of the bypass at the level of the ascending aorta and if no contrast opacification was otherwise seen over the entire length of the graft. Only venous coronary bypasses were included in the study.
Twenty patients (15 men, 5 women, mean age 59.4 years) had 16 patent and 23 occluded bypass grafts. Measurements of the diameter of each patent and occluded bypass were carried out through the reviewers by determining the entire graft length and then dividing it into six equal segments. The five axial scans between the six segments were considered to be representative and served for measuring the diameter of the patent and occluded grafts. Measurements were performed on the magnified image using digital calipers on the workstation (window setting: width 400 HU, center 40 HU). The course of the bypass relative to the axial scan was taken into account for the measurements by the reviewers by scrolling through the scans to avoid overestimation of graft diameter due to an oblique orientation of the bypass graft. If a graft was not detectable within the mediastinal fat at all the bypass was considered to have a diameter of 0 mm. In the case of an occluded graft presenting as a minute density detectable within the mediastinal fat but not measureable with digital calipers due to its small size, the graft was attributed a diameter of 0.1 mm. In all other cases, the actual diameter was determined through caliper measurements.
The bypasses of the 20 patients were assigned to one of three groups according to patency of graft or age of graft occlusion. The first group comprised the patent grafts (group A, patent bypasses; 16 grafts, 13 patients). A second group was made up of bypasses of patients who had undergone EBT within 10 days of bypass surgery (group B, acute occlusion; 11 grafts, ten patients). Finally, a third group consisted of grafts of patients who had had conventional coronary angiography demonstrating bypass occlusion 6 months or more prior to the EBT-study (group C, chronic occlusion; 12 grafts, ten patients).
Standard of reference for the patients with chronic graft occlusion (group C) was coronary angiography performed 6 months or more before the EBT-study. In the ten patients with acute graft occlusion (group B), coronary angiography was not performed in addition to EBT. Standard of reference for these patients was a consensus reading of the two reviewers on the patency of the grafts using all available clinical information. The majority of patients with acute occlusion (n=7) presented with early postoperative findings indicative of graft thrombosis (ECG changes and abnormal enzyme levels). Three patients of group B were clinically not suspected of having an acute graft occlusion. Acute graft occlusion was confirmed by surgery (Re-CABG) in three of ten patients.
2.4. Statistical analysis
The statistical analysis was performed using the Mann–Whitney-U-test for unpaired samples after pooling of data. Mean graft diameters were determined for patent bypasses and acutely and chronically occluded grafts. Sensitivity and specificity of EBT for the detection of acute and chronic coronary artery bypass occlusions were determined for an upper and a lower cut-off, respectively. The upper and lower cut-off level were chosen based on our data. The level of significance was 0.05.
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3. Results
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Overall image quality and arterial contrast opacification was good (n=32) or excellent (n=82) in all 114 studies. In group B, (acute occlusion) EBT was performed at a mean of 5.4 days (±2.3 days standard deviation) after bypass surgery. Patients in group C (chronic occlusion) underwent EBT at a mean of 23.1 months (±11.9 months SD) after coronary angiography.
Table 1 shows the results of the measurements of diameter of patent and acutely and chronically occluded bypass grafts. The mean diameter of the patent bypasses was 3.9 mm (±.6 mm SD; n=16). The mean diameter of the acutely occluded bypasses (Figs. 1A–C and 2
) was 5.4 mm (±1.9 mm SD; n=11) as opposed to 0.3 mm (±0.9 mm SD; n=12) for chronic occlusions (Figs. 2A–C and 3
). The difference in diameter between patent and acutely occluded bypasses, patent and chronically occluded bypasses as well as between acutely and chronically occluded bypasses was highly significant (P<0.01 for each; Fig. 4
).
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Table 1. Mean diameter of patent coronary bypasses and acutely and chronically occluded grafts (values are given in millimeters with standard deviation)a
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Fig. 1. Sixty-three-year old man with two venous coronary bypasses 9 days after bypass surgery (acute occlusion, group B). (A) Shows the origin of an opacified, patent bypass (group A) at the ventral face of the ascending aorta (straight arrow) to the circumflex artery (CX, not shown). At the level of the bifurcation of the main pulmonary artery (B) the bypass to the CX is seen adjacent to the main pulmonary artery (straight arrow). A second, non-enhanced bypass to the left anterior descending artery (LAD) is depicted ventrally (curved arrow). (C) Shows the occluded graft (closed curved arrow) lateral to the LAD (straight arrow: patent bypass dorsolateral to the CX; open arrow: RCA). Note the larger diameter of the occluded graft to the LAD compared to the patent one to the CX in (B) and (C).
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Fig. 2. Sixty-six-year old man 42 months after bypass surgery (chronic occlusion, group C). (A) At the level of the right pulmonary artery shows the origin of a venous bypass (open arrow) from the ascending aorta. In (B), the contrasted bypass is seen 5 mm caudal to the origin (straight arrow). Only 2 cm distal to its origin the bypass is no longer detectable within the mediastinal fat (straight arrow) indicating obliteration and severe reduction of graft diameter due to shrinking and scarring typical of chronic occlusion (C).
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Fig. 3. Shaded surface display reconstruction (right anterior oblique view downwards; threshold 80 HU) of the heart of a 61-year old man 36 months after triple bypass surgery (chronic occlusion, group C) demonstrates two patent venous grafts (group A) to the left anterior descending artery (LAD, short closed arrow) and the first diagonal branch (curved open arrow). The origin of a third bypass is seen on the right ventral portion of the ascending aorta (long closed arrow). Similar to angiography the diameter of the third bypass cannot be judged in this three dimensional reconstruction due to graft occlusion (straight open arrow: right coronary artery). In the axial scans (not shown) the occluded bypass was not depictable within the mediastinal fat characteristic of chronic occlusion. Coronary angiography performed 22 months prior to the EBT-study demonstrated two patent bypasses to the LAD and the first diagonal branch and one occluded bypass.
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Fig. 4. Histogram comparing mean diameters of patent coronary bypasses and acutely and chronically occluded grafts (values are given in mm with standard deviation).
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Sensitivity and specificity of graft diameter measurements with EBT for the detection of acute graft occlusions were 87 and 92%, respectively, using a cut-off at 4.5 mm. Respective values for chronic bypass occlusions were 92 and 96% for a cut-off at 1 mm. One patient in group B (acute occlusion) was judged to have a graft diameter of 0 mm (not detectable) on all five measurements; this patient had a postoperative hematoma in the anterior mediastinum following bypass surgery. In group C (chronic occlusion) 11 of 12 (91.7%) occluded bypasses had a mean diameter of 0 mm (not detectable; n=4) or 0.1 mm (detectable, but not measureable; n=7), one patient had a mean graft diameter of 3.2 mm.
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4. Discussion
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A significantly larger graft vessel diameter in the case of an acute bypass occlusion versus patent bypasses in our study indicates an increase in diameter of the grafted vein as a result of acute thrombosis. A larger diameter of thrombosed as opposed to patent veins is a typical sign of acute deep venous thrombosis (DVT) and thrombophlebitis at ultrasound [15–17]. It may be hypothesized that veins preserve their ability to increase in diameter as a response to acute thrombosis when transplanted as vessel homografts from typically the lower limbs into the chest in coronary bypass surgery. Moreover, we found that the mean graft diameter in acute occlusion of venous bypasses is significantly larger than in chronic graft occlusions. This could be due to shrinking, scarring and eventually narrowing down of occluded grafts over a time course of weeks to months to a fine line beyond the spatial resolution of EBT. Sonographic assessment of lower limb vein diameters by Hertzberg et al. showed that veins in case of acute DVT were larger than normal veins and that veins with chronic DVT were smaller than normal veins [15]. Meissner et al. at sonography found a decrease in diameter of veins with residual disease after DVT as compared to non-affected veins and a return to normal after complete recanalization [18]. Consequently, it has been proposed to use the vein diameter for sonographic age determination of thrombi [19,16]. Other investigators, however, have pointed out that despite significant differences in diameter between patent and acutely and chronically thrombosed veins a large overlap between these groups does not allow for safe differentiation in each case by means of diameter measurement [15]. Likewise, there may be some overlap of the diameters of coronary vessel grafts between patent bypasses and acutely and chronically occluded grafts. It should be pointed out that the diameter of a patent bypass will increase early after graft occlusion to reach a maximum and then subsequently decrease towards diameters of less than 1 mm in most cases of chronic occlusion. During this process of shrinking, the diameter of the graft will at some time equal the diameter of the patent bypass. This overlap should occur during the first 6 months after bypass surgery, the time window that in our study was excluded from evaluation. In consequence, our results do not allow any conclusions concerning the dynamics of transformation of an acutely thrombosed coronary bypass into a chronically occluded, obliterated graft.
Our results indicate, that the complete or near-total absence of a bypass graft within the mediastinal fat over the entire length of the graft is usually due to a longstanding, i.e. chronic bypass occlusion. In one patient with an acute occlusion, the bypass diameter was found to be 0 mm which may retrospectively be attributed to obscuring of the graft due to a mediastinal hematoma. In a clinical setting, the diagnosis of an obliterated and severely narrowed coronary bypass by EBT in a patient with a sudden onset of chest pain makes an acute graft thrombosis as the cause for this patient's symptoms unlikely and should avert any catheter-guided recanalization attempts. However, in the presence of extensive mediastinal hematoma a graft occlusion may be obscured leading to non-visualization of the graft and inability to assess its diameter.
Our results show an increase in diameter of acutely thrombosed bypasses as compared to patent bypasses. However, this may only hold true for early postoperative acute bypass occlusions. An acute occlusion of an old, partly degenerated and possibly calcified graft with an already reduced diameter may not lead to an increase in bypass diameter. Our data cannot prove or refute this hypothesis as only acute bypass occlusions that occurred within 10 days of bypass surgery were included in the study. Similarly, an old, pathologically altered graft may not undergo narrowing following acute occlusion as apparently do acutely thrombosed grafts in the early postoperative phase. This could explain the relatively high mean diameter of 3.2 mm in one of our patients with a chronic occlusion.
Thrombosis of venous coronary bypass grafts is the result of a number of prothrombotic and technical factors [4]. Consequently, varicose veins are generally not used as vessel grafts. It is conceivable that non-varicose veins of relatively large diameter could be at a higher risk than thin veins of undergoing thrombotic occlusion. In this case, the larger diameter of occluded grafts versus patent grafts as found in our study would not result from an increase in diameter following thrombosis but would rather be due to a primarily larger diameter of the grafts before occlusion occurs.
The gold standard for the assessment of patency of coronary bypasses is conventional coronary angiography. As a limitation of our study, coronary angiography was the reference method only in the patients with late occlusions, but not, however, for the patients with early postoperative occlusions. Several investigators have shown that EBT has a high sensitivity in the detection of occlusions of venous bypasses of up to 100% [10–12,20]. In our study patients were preoxygenated prior to scanning which has been shown to reduce breathing artifacts that are considered to be among the leading causes for reduced image quality [21,10,20]. Preoxygenation should enable an even better depiction of coronary bypasses due to a reduction of breathing artifacts and an overlapping of scans [14]. Image quality and contrast opacification in our study were considered to be good or excellent in all cases by the reviewers. In addition, internal mammary artery bypasses which are more difficult to assess with EBT than venous grafts were excluded from the study. Concordant judgement of two reviewers on occlusion or patency of coronary bypasses constituted the reference standard in our study. The diagnosis of acute graft thrombosis in EBT is supported by early postoperative findings suggestive of bypass occlusion in seven out of ten patients and was confirmed by surgery in three out of ten patients. All in all, sensitivity of our reference standard for the detection of bypass occlusions should approach 100%.
The reviewing process and the measurement of bypass diameters in our study were carried out by two radiologists blinded to the history of the patients, the total number of bypass grafts, the age of the bypass grafts, and the results of coronary angiography. However, using a consensus reading rather than an independent reading of the EBT studies must be noted as a study limitation weakening the statistical power of the data.
In spite of the blinded character of the reading, the patients in group B (acute occlusion) were in an early postoperative phase at a mean of 5.4 days after bypass surgery while the patients with chronic occlusions were scanned at a mean of 11.9 months after surgery. Consequently, in group B early postoperative changes as pleural and pericardial effusions, subcutaneous or mediastinal hematoma or air inclusions, mediastinal edema, atelectasis, chest drains and skin closure material were potentially visible on the scans preventing true blinded reading.
In conclusion, EBT may enable non-invasive differentiation between acute and chronic coronary artery bypass graft occlusion through measurement of bypass diameter; our results indicate that the majority of occluded bypasses shrink over a time course of several months to a diameter beyond detectability with EBT. It remains to be determined, if acute and chronic graft occlusion can be discriminated on non-contrast scans. It seems that veins transplanted to the coronary arteries as bypass grafts preserve their ability to increase in diameter when thrombosis occurs, as known from DVT or thrombophlebitis. In consequence, EBT could help link acute chest pain of a patient to an acute bypass thrombosis or prevent such conclusions in the case of a chronic graft occlusion. EBT beyond the mere diagnosis of coronary bypass graft occlusion can thereby potentially prevent unsuccessful invasive recanalization attempts. It could help differentiate acute from chronic bypass occlusions in patients with both types of occlusion and assist in guiding catheter-based recanalization procedures to the site of the potentially reversible acute bypass occlusion.
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Acknowledgments
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We would like to thank Marie-Luise Rode, Gabriele Urbansky, Simone Schwedler, and Julka Koschmann for their help with acquiring the scans and Il Panificio for excellent technical assistance.
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Abstract
1. Introduction
