Ann Thorac Surg 2004;78:122-128
© 2004 The Society of Thoracic Surgeons
Original article: cardiovascular
Efficacy of transmyocardial laser revascularization and thoracic sympathectomy for the treatment of refractory angina
Manuel Galiñanes, MD, PhDa*,
Mahmoud Loubani, MD, FRCSIa,
Penelope R. Sensky, MRCPb,
Ashraf Hassouna, FRCSIa,
Graham R. Cherryman, FRCRc,
Joseph N. Leverment, FRCSa,
Nilesh J. Samani, MRCPa,b
a Department of Integrative Human Cardiovascular Physiology and Cardiac Surgery, Leicester, United Kingdom
b Division of Cardiology, Leicester, United Kingdom
c Department of Radiology, Glenfield Hospital, University of Leicester, Leicester, United Kingdom
Accepted for publication December 10, 2003.
* Address reprint requests to Professor Galiñanes, Department of Integrative Human Cardiovascular Physiology and Cardiac Surgery, Glenfield Hospital, University of Leicester, Groby Rd, Leicester LE3 9QP, UK
e-mail: mg50{at}le.ac.uk
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Abstract
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BACKGROUND: Transmyocardial laser revascularization (TMR) is an effective treatment for relief of refractory angina. This benefit may be mediated by increase in myocardial perfusion or by cardiac denervation. We investigate the efficacy of TMR and thoracic sympathectomy (TS) for relief of angina and whether any clinical benefit is associated with enhanced myocardial perfusion.
METHODS: Twenty consecutive patients with nonrevascularizable coronary arteries and intractable angina were prospectively randomized to have TMR by holmium: yttrium aluminum garnet laser or TS. Subjects were clinically evaluated before, and for 42 months after, surgery. They underwent exercise tolerance testing and rest and stress quantitative perfusion magnetic resonance imaging (MRI) before, and 6 months after surgery.
RESULTS: The demographics of the two groups were similar. There was no perioperative mortality; however, two patients died in the TS group during follow-up. The Canadian Cardiovascular Society angina score improved from 3.4 ± 0.5 to 2.6 ± 1.1 (p = 0.06) in the TS group at 6 months but returned to 3.2 ± 0.7 at 42 months, while in the TMR group it improved from 3.6 ± 0.5 to 1.9 ± 0.7 (p = 0.008) at 6 months and deteriorated to 2.5 ± 0.9 (p = 0.01) after 42 months of surgery. The TMR-treated patients showed significant improvements in the SF-36 scores and Seattle Angina Questionnaire only at 6 months, whereas TS-treated patients did not show amelioration at any time during follow-up. The MRI protocol was completed in 15 of 20 (TMR = 8; TS = 7) patients and no significant differences in qualitative or quantitative perfusion variables were demonstrated in either group.
CONCLUSIONS: A greater clinical benefit was obtained with TMR than with TS early after surgery but this clinical effect did not seem to be associated with improvement in myocardial perfusion as assessed by MRI and part of the beneficial effect was lost by 42 months after surgery.
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Introduction
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Patients with severe diffuse coronary artery disease and refractory angina that cannot be treated with conventional coronary artery bypass graft (CABG) surgery or angioplasty may be candidates for transmyocardial laser revascularization (TMR) therapy. Recent randomized studies on TMR have demonstrated relief of angina [1–4] and improvement in exercise tolerance [2], but the cause of these beneficial effects is unclear. To explain the clinical results it has been proposed that TMR may increase myocardial perfusion by promoting angiogenesis [5, 6]. A number of studies have reported that TMR induces an increase in myocardial perfusion [3, 7] although the validity of this thesis has been questioned by inconsistent findings in several clinical studies [1, 2, 4, 8]. On the other hand, it has been shown that TMR causes myocardial denervation in dogs [9] and in humans [10]. Left thoracic sympathectomy has also been suggested as a means to relieve angina [11], but its efficacy relative to TMR is unknown.
Therefore, the objectives of this study were to (1) compare the efficacy of TMR and TS on the relief of angina and the improvement of exercise tolerance in patients with severe coronary artery disease not amenable to conventional revascularization in the immediate and midterm, and (2) investigate the controversial issue of whether any clinical benefit is associated with enhanced myocardial perfusion, using magnetic resonance imaging (MRI) to evaluate myocardial perfusion.
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Material and methods
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Patient selection
Ethical approval was obtained from the Leicestershire Health Ethics Committee. Patients with severe angina Canadian Cardiovascular Society (CCS) score of III or IV, coronary artery disease not amenable to routine revascularization with bypass surgery or angioplasty, left ventricular ejection fraction (EF) above 30% on ventriculography and with no contraindications to adenosine stress MRI were included. To permit evaluation under standardized conditions, all patients were continued postoperatively on their full preoperative antianginal medications. The patients were randomized with the use of a simple sealed envelope method to receive either TMR or TS.
Clinical assessment
The twenty patients included in the study were interviewed, the study was discussed, and informed consent was obtained. Two blinded independent observers graded angina using the CCS score before and at 6 and 42 months after surgery and the average for the two observers was taken as the score at each time point. All patients completed the EuroQol quality of life scale, the SF-36 health survey, and the Seattle Angina Questionnaire before surgery and at 6 months and 42 months after the operation.
Exercise tolerance test
Exercise tolerance testing was performed preoperatively and six months postoperatively using the Bruce protocol. ß-blocker medication was withheld for 48 hours before the test. Indications for terminating the test were chest pain, ischemic changes on the electrocardiogram (ECG), limiting dyspnea, or fatigue. The total exercise time in seconds was noted and the reason for stopping the test documented.
Magnetic resonance imaging
Patients underwent MRI with a 1.5 Tesla imager (Siemens Vision, Erlangen, Germany) immediately before surgery (visit A), and at six months (visit B) after the procedure. Substances containing caffeine were stopped 12 hours before each scan. On each visit, first pass contrast enhanced perfusion MRI was performed at rest and 3 minutes after commencement of an adenosine infusion (140 µg kg–1 min–1 for 6 minutes) as a stressor. A dynamic inversion recovery snapshot-FLASH sequence (repetition time = 4.5 ms, total repetition time = 1,080 ms, inversion time = 300 ms, echo time = 2 ms, flip angle = 8 degrees, field of view = 300 mm x 300 mm, slice thickness = 9 mm, 96 x 128 matrix, 25 measures) was used. Sequential images were acquired in the basal, midpapillary, and apical short axis planes of the left ventricle. A bolus of gadodiamide (0.025 mmol kg–1 [Omniscan, Nycomed Amersham, Amersham, UK]) was given via the antecubital vein after the third measurement. A proton density image, after full longitudinal relaxation, was obtained before each application of the sequence to enable calculation of the longitudinal relaxation rate (R1). Pulse, blood pressure, and cardiac rhythm were monitored continuously throughout the scan. The infusions were stopped on completion of the protocol if intolerability developed in the patient side effects or if clinical and(or) electrocardiographic changes of ischemia or arrhythmia occurred.
Quantitative analysis of myocardial blood flow was performed on the midpapillary slice from each examination with the use of a computer workstation (Sun Microsystems, Mountain View, CA) and image analysis software Analyze AVW 2.5 (Mayo Foundation, Rochester, MN). Epicardial and endocardial contours were traced by hand and regional signal intensity changes over time were extracted. The anterior attachment of the right ventricle to the left ventricle was used as a reference marker for image registration. The myocardium was then divided radially into four equal regions of interest (ROIs), representing anterior, lateral, inferior, and septal walls, respectively. Myocardial longitudinal R1 time curves were then calculated to estimate the gadodiamide concentration within each ROI [12, 13]. A curve for the contrast agent bolus (input function) was similarly generated from a circular ROI placed in the center of the left ventricular cavity in the corresponding basal short axis slice. Tissue and input functions were then entered into a deconvolution algorithm to calculate the unidirectional transfer constant (Ki) for gadodiamide at rest and during adenosine stress for each myocardial ROI. The theory and method of this calculation has been described in detail previously [12, 14]. The stress-rest Ki ratios were calculated to give an index of myocardial perfusion reserve (MPRI) for each ROI.
Perfusion images were also evaluated qualitatively by an experienced reviewer (PRS). Each ROI was divided circumferentially into inner and outer layers. Abnormal perfusion was defined as visually evident reduced and(or) delayed peak signal intensity following contrast agent enhancement. If a perfusion deficit was limited to the inner layer it was described as subendocardial. If it affected both inner and outer layers it was described as transmural. Stress and rest images were reported together to allow recognition of reversible (only apparent on stress) and fixed (similar on stress and rest) defects.
Exogenous extracellular contrast media may be used in combination with MRI techniques to provide qualitative and quantitative information about myocardial perfusion [15–17]. Cross-sectional images through the myocardium are rapidly repeated at predetermined slice positions before, during, and after the rapid bolus administration of a gadolinium containing MRI contrast agent. The presence of the paramagnetic gadolinium, as it passes through the myocardial microvasculature and transiently accumulates in the myocardial extracellular fluid space, reduces the local T1 relaxation time. In clinical work this altered T1 signal intensity may be observed visually [18]. In research studies the change in signal intensity over time is usually quantified. To quantify perfusion, ROIs are drawn over the myocardium and the MR signal intensity measured in each ROI. Image acquisition is triggered at specific points within the cardiac cycle through ECG gating. This ensures images may be coregistered in space and against the cardiac cycle [19, 20]. Visual analysis of the combined stress and rest images is used to show regional variation in peak enhancement or time to peak enhancement. Fixed and reversible defects may be demonstrated. Defects may be transmural or subendocardial. The longitudinal relaxation rate R1 may be calculated from the measured signal intensity [13]. A deconvolutional algorithm is then used to calculate the unidirectional Ki for the gadolinium contrast agent [21, 22]. Myocardial perfusion is typically measured twice, once at rest and the other during maximal stress. The stress to rest ratio of the Ki values is then used to calculate an index of myocardial perfusion reserve for each [14]. The ROIs may be assigned to different vascular territories using the coronary angiogram [23].
Surgery
All patients received standard premedication and anesthetic technique. Transmyocardial laser revascularization was performed through a left anterolateral thoracotomy in the fifth intercostal space. The myocardium was inspected to ascertain that only areas devoid of fibrous tissue were lased with the holmium:yttrium-aluminum-garnet laser (Ho:YAG) (CardioGenesis Corp, Sunnyvale, CA). This delivers 2 J of energy per pulse and 5 to 8 pulses were required to traverse the myocardium. The channels were distributed at 1 cm2 throughout the lased area. The laser was synchronized to fire at the peak of the R wave of the ECG of the patient's beating heart.
Thoracic sympathectomy was performed using a mediastinoscope introduced through a small anterior thoracotomy in the left second intercostal space. Ablation of the sympathetic chain was achieved by diathermy skeletonization from the left border of the vertebral bodies and posterior thirds of the ribs. This was completed from the level of the second to the fourth vertebrae. The sympathectomy was performed by a senior surgeon (JNL) with more than three decades experience in performing this procedure for various clinical conditions.
Statistical analysis
Data are expressed as mean ± standard deviation. Paired and unpaired Student's t test and two-way analysis of variance (ANOVA) were used as appropriate to test parametric data. The Wilcoxon signed ranks matched pairs test was used for testing changes over time within the groups. The Mann-Whitney U test was used to compare the groups. A p value of less than 0.05 was taken as significant. The study was powered to observe significant differences in relief of angina but not in the other variables.
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Results
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Thirty-seven patients were referred for inclusion in the study. Nine were excluded because of impaired left ventricular function (EF < 30%), five were still considered suitable for CABG surgery, one was too large to fit into the MRI scanner, one had asthma, and one declined to enter the study. As seen in Table 1,
the demographic data of the subjects randomized to TMR and TS were similar. The mean number of channels per patient in the TMR group was 42 ± 11. Eight patients had all three walls of the left ventricle lased, one had the lateral and inferior walls lased, and the remaining patient only had the inferior wall lased.
Clinical outcome
There was no mortality perioperatively in either group; however, two patients died at 22 and 25 months following surgery in the TS group. Two patients in the TMR group and one in the TS group had atrial fibrillation in the postoperative period that was controlled by antiarrhythmic medical therapy. Patients in the TMR group had a longer stay in hospital than patients in the TS group (6.7 ± 4.2 vs 3.6 ± 1.7 days; p < 0.05). No Horner's syndrome was encountered in the TS group.
As shown in Table 2,
the CCS angina score improved in the TS and TMR groups at 6 months after surgery although the improvement was greater in the TMR group than in the TS group. However, by 42 months angina class returned to presurgery values in the TS group and slightly deteriorated in the TMR group. The New York Heart Association (NYHA) class and the EuroQol scores were similar in both groups before surgery and there was no significant improvement with either of the two treatments at any time during the follow-up. As shown in Table 3,
the TMR patients reported a significant improvement in seven out of the nine categories in SF-36 scores compared to improvement in only one of the categories in the TS group at 6 months follow-up: however, most of the reported benefit was lost at 42 months follow-up. Figure 1
demonstrates improvement in exertional capacity and angina stability categories of the Seattle Angina Questionnaire in the TMR group but not in the TS group at 6 months and, although the reported exertional capacity was preserved 42 months later, the benefit on angina stability had disappeared and the disease perception score had worsened. During follow-up there were 4 readmissions because of unstable angina in the TS group and another 2 in the TMR group, one because of atrial flutter at 9 weeks that required electrical cardioversion and one because of unstable angina.
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Fig 1. The SAQ scores before surgery and 6 and 42 months after surgery in the (A) TS group (white bars = baseline score; hatched bars = 6 months after TS; black bars = 42 months after TS) and in the (B) TMR group (white bars = baseline score; hatched bars = 6 months after TMR; black bars = 42 months after TMR). *p < 0.05 versus preoperative mean value. (SAQ = Seattle Angina Questionnaire; TMR = transmyocardial revascularization; TS = thoracic sympathectomy.)
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Exercise tolerance test
The Bruce protocol was attempted by 15 patients (TS = 7; TMR = 8) while the other 5 were unable to exercise for the following reasons: 3 had limiting arthritis in their lower limbs; 1 was waiting for surgical correction of a femoral aneurysm; and 1 patient in the TS group refused to have the 6 months follow-up test. Although this study was not powered to assess differences in exercise tolerance, this was unchanged in the TS group but it tended to improve in the TMR patients, a difference that failed to achieve statistical significance (Table 2).
Magnetic resonance imaging
Seventeen patients completed MRI follow-up. Two patients were withdrawn from the TS group; one because of claustrophobia and one because of angina at rest before commencing the test. One patient from the TMR group withdrew because of intolerance to adenosine. There was no significant difference between the two groups in hemodynamic variables such as heart rate, systolic, diastolic, and mean blood pressure at rest or with adenosine infusion.
Satisfactory images for quantitative perfusion analysis were obtained in all 17 patients. Table 4
shows that there was no significant difference in perfusion at rest or on stress between the three groups and between preoperative and postoperative values within each group. No improvement in perfusion was seen with either intervention by qualitative assessment of the images (data not shown). In particular, evaluation of the subendocardial layer revealed no change in distribution of myocardial blood flow.
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Comment
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This study directly compares the degree of angina relief obtained with TMR and with cardiac TS. It also investigates the effect of the two interventions on myocardial perfusion. The study has shown that TMR causes greater short-term angina relief than TS but that this effect may be transient and does not seem to be associated with detectable improvement in myocardial perfusion using MRI. These results warrant further discussion.
Angiogenesis and myocardial perfusion after TMR
Laser-created channels are soon occluded [24] and the initial concept, that improvement in angina after TMR relates to increased blood flow directly from the ventricular cavity into the ischemic myocardium through the created channels [25, 26], has been abandoned. Although some animal studies have failed to demonstrate an increase in regional blood flow after TMR when microspheres were used [27, 28], other studies have shown that TMR increases myocardial perfusion using nuclear imaging [8, 29]. This has led to the speculation that angiogenesis may be the underlying mechanism for the clinical benefit of TMR. However, with some exceptions [3, 7] most clinical studies [4, 25, 30] including ours, have shown absence of significant changes in myocardial perfusion in spite of the improvement in angina. The controversy is further fueled by the clinical difficulties on the measurement of myocardial perfusion and by the fact that different lasers generate different degrees of angiogenesis and efficacy of myocardial perfusion [31].
It is also possible that the failure to observe an increase in myocardial perfusion by TMR in clinical studies is the result, at least in part, of the inability for the diseased epicardial coronary arteries to increase blood supply. If this is the case, then it may be argued that the clinical effect of TMR is the result of a better blood distribution rather than a detectable increase in blood flow. In this connection, Cooley and co-workers [25] have reported a 20% increase in the ratio of subendocardial to subepicardial perfusion in laser-treated areas as assessed by computer-aided positron emission tomography after 12-month follow-up. Since the spatial resolution of MRI is superior to that of scintigraphy, we were able to evaluate the effects of TMR and TS on subendocardial perfusion. However, no improvements in the distribution (transmural vs subendocardial) or nature (reversible vs fixed) of any preoperative perfusion deficits were identified following either TMR or TS. Thus, this theory remains speculative.
Cardiac denervation
The superficial location of sympathetic fibers in the epicardium of the left ventricle [32] and the belief that perception of anginal pain is conveyed by afferent sympathetic fibers [33], together with the immediate relief of angina after TMR and the evidence that TS ameliorates angina [11], led to the proposition that the effect of TMR may be mediated by sympathetic cardiac denervation. It has been reported that TMR induces sympathetic denervation in the dog [9] and also in humans [10] but this concept has been disputed [34, 35]. The present study has shown that the degree of angina relief by TS is less than that obtained with TMR, suggesting that cardiac denervation may not be the only mechanism explaining the improvement of angina by TMR. However, it should be clarified that in our study, unilateral left thoracic sympathectomy was performed and that this alone may not have been sufficient to achieve complete cardiac denervation.
Placebo effect
The failure to demonstrate an improvement in objective variables in our study may suggest that a placebo effect is the cause of the improvement in symptoms observed in patients treated with TMR. This is an issue that will not be resolved until blind studies with proper controls for the TMR treatment are carried out. The use of such controls would be ethically unacceptable in surgical studies. It is worth noting that a presentation at the American College of Cardiology meeting (2001) by M Leon, on percutaneous direct myocardial revascularization using Biosense DMR laser with a blinded placebo group (the DIRECT trial), suggested a very strong placebo effect. However, the BELIEF study, presented at the American Heart Association scientific sessions meeting in the same year in which the Ho:YAG laser was percutaneously used in a blinded fashion, demonstrated a significant improvement of angina symptoms compared to sham procedure.
Clinical implications
It is clear from this study and from the literature that although TMR is an effective short-term therapy for the relief of angina and the improvement of the quality of life of patients with diffuse coronary artery disease who cannot receive angioplasty or bypass graft surgery, its efficacy is limited and most patients remain with some degree of angina. This clinical benefit is partly lost by 42 months follow-up suggesting that the improvement may be transient, although recent studies have reported the effectiveness of TMR up to five years [36]. An important question is whether the effectiveness of TMR can be increased and maintained by a better understanding and exploitation of its mechanism of action. Our study, although including a small number of patients in whom MRI was performed only at 6 months postoperatively, suggests that improvement in myocardial perfusion might not be the mechanism. Equally, the fact that TS does not offer as good symptom relief as TMR may suggest that cardiac denervation is probably not the mechanism of action either.
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Acknowledgments
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We wish to thank Professor Peter W. Jones, Dean of the Faculty of Natural Sciences and Professor of Statistics, Department of Mathematics, Keele University, UK, for his assistance with the statistical analysis.
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M. Galinanes
Invited commentary
Ann. Thorac. Surg.,
August 1, 2007;
84(2):
573 - 573.
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Abstract
Introduction
