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a Department of Surgery, University of Maryland, Baltimore, Maryland
b Department of Information Systems, University of Maryland, Baltimore, Maryland
c St. Michael’s Medical Center, Newark, New Jersey
Accepted for publication December 10, 2007.
* Address correspondence to Dr Poston, University of Maryland School of Medicine, 22 S Greene St, Ste N4W94, Baltimore, MD 21201 (Email: rposton{at}smail.umaryland.edu).
Presented at the Basic Science Forum of the Fifty-fourth Annual Meeting of the Southern Thoracic Surgical Association, Bonita Springs, FL, Nov 7–10, 2007.
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Abstract |
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Methods: Twenty-four cadavers and 60 coronary artery bypass graft (CABG) patients scheduled to receive a RA graft underwent OCT imaging before (in situ) and after (ex vivo) open harvest or ERAH. Spasm was quantified by the percentage change in luminal volume between images. Intimal disruption was classified as minor or severe depending on whether the defect was confined to branch ostia or involved the luminal surface. Histology was used to confirm OCT findings.
Results: Luminal volume significantly declined after harvest in all RAs from CABG patients, but there was no difference between groups: –43% ± 29% vs –35% ± 38% change after ERAH (n = 21) vs open harvest (n = 39; p = 0.342). Significantly more intimal injury was noted after ERAH vs open harvest (34/41 vs 9/43, intimal tears/total evaluated RAs, p < 0.0001). Most intimal injury was minor: only 2 tears involved the luminal surface of the RA (both after ERAH). Serial imaging in cadavers revealed that 86% of ostial tears occur in ERAH during the initial blunt dissection step using the endoscope.
Conclusions: Although branch injury is a pitfall of ERAH, OCT imaging documented that the quality of RA procured is acceptable and comparable with open harvest. Catheter-based OCT provides an important quality assurance tool for RA harvest.
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Introduction |
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Particularly concerning is the suitability of the RA for endoscopic harvest (ERAH). Endoscopic techniques require more direct handling of the vessel than a traditional open harvest [7]. Analyses of focal vessel biopsy specimens from harvested RAs have led others to conclude that ERAH has no adverse effect on endothelial integrity [7–9]. However, traumatic harvesting technique would be expected to cause a discrete intimal tear in an otherwise normal-appearing vessel.
Our group has shown that catheter-based optical coherence tomography (OCT) provides images of the conduit at near histologic resolution, which is a far better method for detecting focal pathology within bypass conduits intraoperatively compared with histology [10]. This study used a clinical and cadaver model to evaluate OCT as a tool for intraoperative feedback on the quality of RAs procured using ERAH vs open techniques.
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Material and Methods |
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Conduit Procurement
The RAs were harvested using endoscopic (n = 21 clinical, n = 20 cadaver) and open (n = 39 clinical, n = 4 cadaver) techniques by a single technician with more than 100 total cases of experience with ERAH and open harvest. Group assignment was nonrandomized. In all patients, a tract of saphenous vein was harvested endoscopically and evaluated by OCT as an internal control for comparison of vessel friability vs the RA. The cadaver model was used to determine the influence of the learning curve on ERAH results by comparing RA quality after harvest by 2 technicians, one with minimal (<20 clinical cases) experience vs one with extensive (>500 clinical cases) experience.
Endoscopic RA harvest was initiated by insertion of a conical dissection cannula at the wrist (VasoView6, Guidant Corp, Minneapolis, MN). The balloon on the blunt-tip trochar port was inflated with less than 5 mL of saline to establish a seal necessary to create carbon dioxide pressure within the tunnel of 10 to 12 mm Hg. Exposure of the vessel was created by blunt dissection under direct endoscopic visualization. Bipolar electrocautery (20 W) was used for branch ligation, which was confirmed by lengthwise passage of the vessel C-ring [7]. After proximal ligation (proximal stab incision), the conduit was removed, flushed with heparinized saline, and stored in a plasmalyte solution containing glyceryl trinitrate and verapamil [12]. Open harvest was performed with standard techniques [6] using clips and electrocautery for branch ligation.
Coronary Artery Bypass Graft Technique
A single surgeon performed off-pump CABG through a median sternotomy using suction-based exposure and stabilizing devices (Octopus 4.3, Medtronic Inc, Minneapolis, MN). Heparin was given at the completion of left IMA harvest (activated clotting time >300 seconds and heparin >2 IU/mL) and was reversed by half the dose of protamine calculated by heparin-protamine titration. Preoperative aspirin (325 mg/d) was continued and given within 6 hours after the operation.
Optical Coherence Tomography Imaging
Conduits were imaged by insertion of an OCT catheter (ImageWire, LightLab Imaging, Westford, MA) first into the in situ RA using an upper arm tourniquet and infusion of heparinized saline to clear blood. Examination was performed on saphenous vein and repeated on the RA ex vivo after harvest and removal of the vessel from the limb, as previously described [13].
In cadavers, additional OCT examinations were performed serially after multiple insertions of the OCT probe to rule out intimal injury from the probe itself and after sequential steps of ERAH (ie, after initial RA blunt dissection, after branch ligation using bipolar cautery, and after C-ring manipulation of the vessel).
The OCT images were analyzed by 2 technicians blinded to group assignment, with harvesting injury categorized as minor when intimal disruption was restricted to the ostia of branch points and severe when the luminal surface was involved [10]. Luminal volume of the RA was calculated from OCT data using automated imaging processing software. Spasm was quantified for clinical RAs by comparing the luminal volume before and after harvest. Intimal thickness was quantified by comparison with the media for the calculation of an intima–media thickness (IMT) ratio [14].
Histologic Examination
Biopsy specimens were obtained from cadaveric RAs and discarded portions of clinical RAs to confirm the diagnosis of vascular trauma. To exactly calibrate the OCT images against the corresponding histopathologic sections, the vessel site where the biopsy specimen was obtained was marked externally at the location of the catheter, visualized by gross examination of the infrared light at the catheter tip (13). These image-guided biopsy specimens were embedded and frozen in cutting compound (Tissue-Tek O.C.T., Redding, CA), then sectioned at 5 µm and analyzed for endothelial integrity as described [15].
Ex Vivo Radial Artery Perfusion Analysis
To simulate the effects of grafting into the coronary circulation, 10 cadaveric RAs with minor ostial intimal tears were perfused ex vivo after harvest with Hank’s solution for 30 minutes using a pulsatile perfusion pump (Masterflex L/S, Cole-Parmer Instrument Co, Vernon Hills, IL), as described [16]. Flow into the RA was initiated at 50 mL/min and titrated to maintain pressure of 80 to 110 mm Hg, as monitored by a pressure transducer catheter (Mikro-Tip, Millar Instruments, Inc, Houston, TX).
Graft Patency Analysis
Blood flow was measured in each RA graft using transit time ultrasound imaging (Medistim, Inc, Oslo, Norway) before and after native artery occlusion to rule out competitive flow [17]. Radial artery patency at 1 week was determined by blinded review of computed tomography angiography (CTA). Patency was defined as any flow through the length of the graft regardless of the presence of stenosis, as described [18]. Radial artery graft spasm was defined as a patent graft with a luminal diameter less than the size of its coronary target (ie, Fitzgibbon B patency). To determine the effect of contrast enhancement differences on vessel diameter measurements, the average contrast density, expressed as Hounsfield Units (HU), was measured at the mid-portion of each of the grafts and ascending aorta using the workstation pixel-averaging tool.
Statistics
The primary end point of this study was to compare the incidence of intimal injury (ie, number of intimal tears per conduit) after ERAH vs open harvest using the Fisher exact test. The change in mean luminal volume measured from the in situ and ex vivo OCT scans, a measure of RA spasm, was compared between groups using a t test. In preliminary data using discarded RA segments, we found that ERAH was associated with a fivefold increase in minor intimal injury vs open RA harvest [10]. Therefore, 25 RAs per group were expected to provide an 80% power to detect a fourfold difference in intimal injury between groups at p = 0.05. The reproducibility of OCT interpretations was quantified by interobserver 
correlation coefficients. Baseline patient characteristics were compared between groups using the t test and Fisher exact test, as appropriate. Statistical analysis was performed using the InStat statistical package (GraphPad Software, Inc, San Diego, CA) with assistance of a biostatistician (A. J.).
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Results |
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Validation of Optical Coherence Tomography Findings
Portions of RAs diagnosed as normal vs injured by OCT imaging showed a significant difference in endothelial integrity on analysis of registered biopsy sections (normal OCT, 64% ± 20% endothelial integrity vs intimal tear by OCT, 24% ± 20% endothelial integrity, p = 0.001). On each occasion that OCT diagnosed an intimal tear in the lumen or branch ostium of a portion of RA that was available for biopsy, the OCT diagnosis was confirmed histologically (Fig 1). Identification of intimal damage was highly reproducible, with interobserver correlation values of 0.85 for minor trauma and 1.0 for severe trauma. The ability of OCT to resolve the intima was evidenced by a strong correlation between the IMT ratio measured by OCT vs histology (R = 0.88, p = 0.0007).
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Cadaver Model of Intimal Injury
The pattern of OCT-detected intimal injury was similar between cadaveric and clinical groups (Table 3). Serial OCT imaging during ERAH performed in the cadaver model revealed that insertion of the OCT imaging probe itself was not associated with RA injury on any occasion. Instead, 86% of ostial tears were found immediately after the blunt "tunneling" dissection step. The remaining ostial tears (14%) were noted immediately after the branch dissection step using the C-ring. The incidence of ostial injury differed between experienced and inexperienced harvesters (16% vs 14% injured branch ostia respectively, p = 0.843). Ostial tears were only noted in branches that had a thickened intima (ie, IMT ratio >0.6) and within branches having a diameter of less than 0.3 mm (Fig 1C, D).
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Comment |
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These data may be interpreted as suggesting that ERAH is a step back from the harvesting principles that helped to revive the RA as an effective bypass graft. However, severe intimal injury and intraoperative and postoperative spasm, the features most likely to affect the ultimate outcome of RA grafts, were not increased in RAs procured by ERAH compared with an open harvest control group. Although not statistically powered to confirm equivalence between groups, our data lend further credence to prior reports suggesting that ERAH is a safe method for RA procurement [7–9].
Despite a favorable experience with ERAH relative to the open technique, we did note a subtle pattern of intimal injury centering on the ostia of branches that was more common after endoscopic harvest. Serial OCT imaging in the cadaver model established a temporal relationship of this ostial injury to one specific step of ERAH: blunt endoscopic dissection of the RA away from subcutaneous tissues in the forearm. Although necessary for creating visualization around the vessel, this step can cause traction on RA branches leading to intimal injury at their ostia. Ostial tears were not associated with the risk of RA vasospasm either intraoperatively (defined by OCT imaging) or postoperatively (defined by CTA). In addition, these minor intimal rents did not propagate onto the luminal surface after exposure to arterial pressure in an ex vivo perfusion apparatus. Therefore, the clinical importance of this finding remains uncertain and requires further study.
Severe intimal tears or spasm of the RA were not associated with detectable abnormalities on gross appearance, leaving OCT imaging as perhaps the only reliable way for our group to have made these findings. Optical coherence tomography provides an ideal method to screen for subtle intimal injury distributed heterogeneously within the vessel [20]. Measurements of luminal volume of the RA before and after harvest provide means for quantifying spasm with a high level of precision. The applications of OCT imaging in cardiology have been hindered by the need to flush blood from the vasculature to obtain an optimal image [14]. In contrast, conduit imaging is performed on an exsanguinated segment of vessel flushed with crystalloid solution, providing images with optimal quality that correlate closely with histology, corroborating prior applications of OCT for evaluating the coronary [14] and peripheral vasculature [21]. More important, imaging can be obtained in real time on the portion of the RA that is actually used for grafting.
Our study was limited because it was not a randomized comparison of harvesting methods but a prospective investigation of conduit quality in an effort to improve practice at a single institution, a study design that has the potential to introduce bias. We controlled for this possibility by using several measures. First, the influence of the learning curve was addressed in the cadaver model by demonstrating that there was no relationship between intimal injury and experience of the harvesting technician.
Second, we analyzed end points such as intimal injury and graft spasm by using highly the sensitive methods of OCT and CTA with technicians blinded to study group assignment.
Third, we monitored closely for sources of variability that would likely confound the analyses, such as comparisons of baseline characteristics to measure selection bias, measurements of blood flow in the RA graft to rule out poor anastomotic quality, and competitive flow.
Fourth, we attempted to minimize the technical differences between the open and endoscopic procedures as much as possible, such as the use of electrocautery to assist in RA dissection during both. Although the use of the harmonic scalpel may be associated with less risk of spasm [22], it is not compatible with the VasoView endoscopic system and was therefore not used in the open cases during this comparison.
Despite these safeguards, our data should be considered "hypothesis generating" until completion of an ongoing clinical trial demonstrates whether these intimal abnormalities detected by OCT relate to the risk of RA graft failure.
In summary, our data suggest that intimal disruption and spasm of the harvested RA are sequelae of both open and endoscopic harvest that can be easily and rapidly identified by intraoperative OCT. Optical coherence tomography screening may therefore prove to be a critical tool providing feedback about surgical harvesting technique. These data support the prospective investigation of an imaging strategy that combines in situ OCT scanning to select only healthy portions of the RA for harvest and ex vivo examinations to provide feedback about conduit quality to reduce the variability of RA grafting.
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Acknowledgments |
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References |
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