Ann Thorac Surg 2008;85:891-894. doi:10.1016/j.athoracsur.2007.10.064
© 2008 The Society of Thoracic Surgeons
Original Articles: Cardiovascular
No Late Ulnar Artery Atheroma After Radial Artery Harvest for Coronary Artery Bypass Surgery
Alistair George Royse, MBBS, MDa,b,*,
Greg S. Changa,
Danielle M. Nicholas, BSa,
Colin F. Royse, MBBS, MDa,b
a Cardiovascular Therapeutics Unit, Department of Pharmacology, The University of Melbourne, Parkville, Australia
b Royal Melbourne Hospital, Parkville, Melbourne, Australia
Accepted for publication October 18, 2007.
* Address correspondence to Prof Alistair George Royse, Department of Pharmacology, Faculty of Medicine, The University of Melbourne, Parkville, Victoria 3052, Australia (Email: alistair.royse{at}unimelb.edu.au).
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Abstract
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Background: Radial artery harvest for coronary artery surgery leads to chronically elevated blood flow in the remaining ulnar artery. This study examined the ulnar artery for evidence of increased atherosclerosis compared with the contralateral ulnar artery where the radial artery had not been harvested.
Methods: Patients were enrolled at least seven years after unilateral radial artery harvest. Anatomical and flow data were acquired using a high-frequency ultrasound probe. Maximal forearm blood flow was measured after repeated hand grip with concurrent brachial artery occlusion to induce forearm ischemia.
Results: Eighty five patients, 71 males at age 71 ± 9 years (43 to 88) were assessed at 8.4 ± 1.0 years (7.2 to 11.1). There was no patient with ulnar artery atheroma on either side. Mild ulnar calcification was present in four patients bilaterally. The ulnar diameter after radial artery harvest was greater (2.8 ± 0.5 vs 2.4 ± 0.4 mm; p < 0.001), as was flow at rest (111 ± 64 vs 59 ± 41 mL/min; p < 0.001). However, the brachial artery flow was not different between the two sides at rest (169 ± 90 vs 176 ± 87 mL/min; p = 0.060) or after ischemic exercise (714 ± 294 vs 753 ± 315 mL/min; p = 0.485).
Conclusions: At an average of eight years after radial artery harvest, the remaining ulnar artery does not have evidence of increased atheroma and the maximal forearm blood flow is preserved.
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Introduction
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Use of the radial artery as a coronary artery bypass graft has increased over the past ten years, after publication by Acar and colleagues in 1992 [1]. At our institution, 85% to 90% of patients undergoing coronary artery bypass surgery have received a radial artery during the past ten years. This has enabled total arterial revascularization to be achieved in most patients [2].
A chronic increase in the ulnar artery flow occurs, consequent on harvesting the radial artery [3]. There have been two reports from Gaudino and colleagues [4, 5] suggesting that ulnar artery atherosclerosis may occur after radial artery harvest. It would be of great concern if the majority of patients undergoing coronary artery bypass surgery were to suffer forearm or hand ischemia many years later.
A minor degree of medial calcification is relatively common in the radial artery, with more extensive calcification being relatively uncommon [6, 7]. However, these changes are distinct from intimal plaques, which reflect atherosclerotic pathophysiology, and are quite easily differentiated by ultrasound interrogation. The aim of the study was to investigate whether chronically elevated ulnar artery flow after radial artery harvest would lead to increased ulnar artery atherosclerosis in the late period of at least seven years postoperative.
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Patients and Methods
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Patients with unilateral radial artery harvest at least seven years before were identified from the investigating surgeon’s database as a single surgeon and single institution experience. During this time, radial artery use by the surgeon was in more than 95% of patients and for the institution, more than 80% [2]. Before harvesting, the Allen test was used and there were no episodes of hand ischemia after harvest. The University of Melbourne Human Research Ethics Committee approved the study and informed written consent was obtained. Exclusions included bilateral radial artery harvest, inability to independently attend the University research facility; and remote locality making transportation difficult. The patients were assessed using high-frequency ultrasound imaging examining anatomical and flow characteristics of brachial, radial, and ulnar arteries on both sides, in short and long axis at baseline, and after forearm ischemic exercise testing.
A 13 MHz linear array probe was used (HFL38-6MHz, SonoSite MicroMaxx, Sonosite Inc, Bothell, WA). Images were stored to digital media and offline analysis was performed by two independent observers using ProSolv Cardiovascular Analyzer software (Problem Solving Concepts Inc, Indianapolis, IN). Blood flow was calculated from the cross-sectional diameter of the vessel (intima to intima; Fig 1), the velocity time integral of the spectral Doppler trace (Fig 2), and the heart rate [3]. Pulsed-wave Doppler spectral velocity was acquired from the long axis view, with a sweep speed at 50 mm/second and at least three consecutive cardiac cycles recorded. The appearance of medial calcification (Fig 3) is easily differentiated from that of atheroma, where there is intimal thickening and plaque formation.
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Fig 2. Velocity time integral after ischemic forearm exercise. The spectral Doppler trace with exercise showing prominent flow during diastole.
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Fig 3. Ulnar artery medial calcification. Calcification is noted within the wall of the artery by hyperechoic signals in the wall of the vessel, and acoustic shadowing and "comet-tail" artifact deep to the calcification. There is no intimal thickening or plaque formation that would suggest atheroma.
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Measurements were performed with the patient seated and in a warm room. The following measurements were performed: (1) two-dimensional imaging of the ulnar and radial arteries from the wrist to the brachial artery for atherosclerotic plaques; (2) arterial diameter and pulsed-wave Doppler spectral velocities (PWD) at rest for the ulnar and radial arteries 5 cm proximal to the flexor skin crease of the wrist, and the brachial artery in the antecubital fossa; and (3) brachial artery diameter and PWD after forearm exercise. Maximum forearm ischemia was induced by inflating a blood pressure cuff 20 mm Hg above systolic blood pressure and the patient rapidly clenching his or her fists until fatigue ensued with a minimum of one minute of exercise [3, 8]. Doppler data were acquired for maximal flow within the first 15 seconds after blood pressure cuff deflation. All measurements were an average of three cardiac cycles from two independent observers. In the case of ulnar and brachial arteries, the right (nonharvested) side was measured before the left (harvested) side.
Statistical Analysis
Data are presented as mean ± standard deviation. Analysis of the incidence of calcification was performed using the Fisher exact test. Comparisons of flow between sides and between baseline and maximal flow were performed using the paired-samples Student t test, SPSS version 14 (SPSS Inc, Chicago, IL). Statistical significance was defined as p less than 0.05.
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Results
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Eighty five patients were assessed, 71 males, at an age 70.6 ± 8.8 years (range, 43 to 88). The time after surgery was 8.4 ± 1.0 years (range, 7.2 to 11.1). Demographic data are presented in Table 1. The data for body mass index and body surface area approximated the normal distribution. Of note, 32% of patients were considered obese (body mass index >30). Previous smokers represented 55% of patients, and ongoing current smokers 12%.
No atheromatous plaques were detected in the ulnar or radial arteries. Ulnar artery medial calcification was present in four patients (Fig 3), though the distribution was equal between both forearms. In two of these four patients, calcification was also present in the remaining radial artery. Diameter and flow in the ulnar artery was significantly greater on the side where the radial artery had been harvested (see Table 2).
There was a small but statistically significant increase in size of the brachial artery on both sides with exercise, but a large increase in flow on both sides after exercise. At rest, the dimension of the brachial artery on the harvested side was slightly smaller (p < 0.001), but flow between these two sides was not significantly different (p = 0.060; Table 3). After ischemic exercise, the brachial artery dimensions on both sides were not different (p = 0.485), nor were the flows between sides (p = 0.310).
An additional flow assessment to the hand was made by measuring flow 5 cm proximal to the skin crease in the ulnar artery on the harvested side, and the addition of the ulnar and radial artery flows on the nonharvested side. These flows at rest were not different, being 117 ± 67 versus 113 ± 64 mL/minute on the harvested side (p = 0.447). Interobserver data are shown in Table 4. There was good agreement for all measurements performed.
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Comment
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This study examined 85 patients at 7 to 11 years after unilateral radial artery harvest for coronary artery bypass surgery. We found no atheroma in the ulnar arteries of these patients, either on the side where the radial artery had been harvested or on the side where the radial artery had not been harvested. This important finding confirms late freedom from accelerated atherosclerosis involving the remaining ulnar artery when the radial artery was used as a coronary artery bypass graft.
After radial artery harvest, the remaining ulnar artery increases in size, but the brachial artery does not. Flow in the ulnar artery is chronically elevated after radial artery harvest. Previous reports suggested that this chronic increase in the flow may lead to acceleration in atherosclerosis formation, potentially leading to late vascular impairment of the forearm or hand [4, 5]. Conversely, an increase in flow, and therefore shear stress on the ulnar artery intima, could theoretically lead to elevated nitric oxide production and so be protective against atheroma formation [9]. We found that there was no increase in atheroma of the ulnar artery after radial artery harvest.
These data are consistent with a previous report early after surgery, where there was preservation of maximal blood flow to the forearm after radial artery harvest [3, 10]. We also assessed the blood flow to the hand alone, where the measurements were taken 5 cm proximal to the wrist, distal to the forearm muscle branches. We found no difference in the blood flow of the ulnar artery on the harvested side, compared with the sum of the ulnar and radial artery flows on the nonharvested side. These data support the continued use of the radial artery as a conduit and coronary bypass surgery to achieve greater total arterial revascularization.
The use of ultrasound to measure the diameter of small vessels has previously been validated by Kiserud and colleagues [11]. Flow using this Doppler principle has been validated with the following: steady state diffusion of umbilical cord in sheep [12]; invasive arterial and electromechanical assessment in human subclavian artery and aorta [13]; thermodilution in humans [14]; and invasive perivascular flow probes on the renal artery in the fetal lamb [15].
There are several limitations to the study. Flow was determined by a noninvasive ultrasound technology which is operator dependent. However, the errors are reduced by averaging three consecutive cardiac cycles and two independent observers. Potential error in sampling may occur where the Doppler cursor is not consistently placed in the same part of the vessel, as the velocity profile of blood is parabolic in shape; greatest in the center of the vessel and lowest near to the wall of the vessel. Maximal flow will decline after deflation of the blood pressure cuff, requiring the acquisition of data within 15 seconds.
At an average of eight years after radial artery harvest, the remaining ulnar artery does not have evidence of increased atheroma and the maximal forearm blood flow is preserved. This supports the continued use of radial artery for coronary revascularization.
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Acknowledgments
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We are grateful to Sonosite Australasia for the loan of the ultrasound equipment for the study, and to Vision Software Solutions Pty Ltd, Brisbane, QLD, Australia for the provision of Prosolv Cardiovascular Analyser software.
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References
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- Acar C, Jebara V, Portoghese M, et al. Revival of the radial artery for coronary artery bypass grafting Ann Thorac Surg 1992;54:652-659.[Abstract/Free Full Text]
- Royse A, Royse C, Shah P, Williams A, Kaushik S, Tatoulis J. Radial artery harvest technique, use and functional outcome Eur J Cardiothorac Surg 1999;15:186-193.[Abstract/Free Full Text]
- Royse AG, Royse CF, Maleskar A, Garg A. Harvest of the radial artery for coronary artery surgery preserves maximal blood flow of the forearm Ann Thorac Surg 2004;78:539-542.[Abstract/Free Full Text]
- Gaudino M, Glieca F, Luciani N, et al. Ten-year echo-Doppler evaluation of forearm circulation following radial artery removal for coronary artery bypass grafting Eur J Cardiothorac Surg 2006;29:71-73.[Abstract/Free Full Text]
- Gaudino M, Serricchio M, Tondi P, et al. Chronic compensatory increase in ulnar flow and accelerated atherosclerosis after radial artery removal for coronary artery bypass J Thorac Cardiovasc Surg Jul 2005;130:9-12.
- Ruengsakulrach P, Sinclair R, Komeda M, Raman J, Gordon I, Buxton B. Comparative histopathology of radial artery versus internal thoracic artery and risk factors for development of intimal hyperplasia and atherosclerosis Circulation 1999;100(19 suppl):II139-II144.[Medline]
- Chowdhury UK, Airan B, Mishra PK, et al. Histopathology and morphometry of radial artery conduits: basic study and clinical application Ann Thorac Surg 2004;78:1614-1621.[Abstract/Free Full Text]
- Ludbrook J. Collateral artery resistance in the human lower limb J Surg Res 1966;6:423-434.[Medline]
- Snow HM, Markos F, O’Regan D, Pollock K. Characteristics of arterial wall shear stress which cause endothelium-dependent vasodilatation in the anaesthetized dog J Physiol 2001;531(pt 3):843-848.[Abstract/Free Full Text]
- Chong WC, Ong PJ, Hayward CS, Collins P, Moat NE. Effects of radial artery harvesting on forearm function and blood flow Ann Thorac Surg 2003;75:1171-1174.[Abstract/Free Full Text]
- Kiserud T, Saito T, Ozaki T, Rasmussen S, Hanson MA. Validation of diameter measurements by ultrasound: intraobserver and interobserver variations assessed in vitro and in fetal sheep Ultrasound Obstet Gynecol 1999;13:52-57.[Medline]
- Galan HL, Jozwik M, Rigano S, et al. Umbilical vein blood flow determination in the ovine fetus: comparison of Doppler ultrasonographic and steady-state diffusion techniques Am J Obstet Gynecol 1999;181(5 pt 1):1149-1153.[Medline]
- Marcus RH, Korcarz C, McCray G, et al. Noninvasive method for determination of arterial compliance using Doppler echocardiography and subclavian pulse tracings. Validation and clinical application of a physiological model of the circulation. Circulation 1994;89:2688-2699.[Abstract/Free Full Text]
- Royse CF, Royse AG, Blake DW, Grigg LE. Measurement of cardiac output by transoesophageal echocardiography: a comparison of two Doppler methods with thermodilution Anaesth Intensive Care 1999;27:586-590.[Medline]
- Veille JC, Figueroa JP, Mueller-Heubach E. Validation of noninvasive fetal renal artery flow measurement by pulsed Doppler in the lamb Am J Obstet Gynecol 1992;167:1663-1667.[Medline]
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Abstract
Introduction
