Ann Thorac Surg 2004;77:2066-2070
© 2004 The Society of Thoracic Surgeons
Original article: cardiovascular
Oxygen pressure measurement during grip exercise reveals exercise intolerance after radial harvest
Susumu Manabe, MDa,
Noriyuki Tabuchi, MD, PhDa*,
Masaaki Toyama, MDb,
Tomoya Yoshizaki, MDa,
Masanori Kato, MDb,
Haisong Wu, MD, PhDb,
Mitsuhisa Kotani, MDb,
Makoto Sunamori, MD, PhDa
a Department of Cardiothoracic Surgery, Graduate School of Medicine, Tokyo Medical and Dental University, Tokyo, Japan
b Department of Cardiac Surgery, Kameda Medical Center, Tokyo and Chiba, Japan
Accepted for publication October 10, 2003.
* Address reprint requests to Dr Tabuchi, Department of Cardiothoracic Surgery, Graduate School of Medicine, Tokyo Medical and Dental University, Yushima 1-5-45, Bunkyo-ku, Tokyo 113-8519, Japan
e-mail: n-tabu.tsrg{at}tmd.ac.jp
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Abstract
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BACKGROUND: Exercise intolerance of the hand after harvest of the radial artery is not well understood, although mild reductions of blood flow to the hand are reported. To ascertain its prevalence, patient symptoms implying potential exercise intolerance were evaluated by measuring transcutaneous oxygen pressure of the hand during grip exercise. For ascertaining predictive values, we verified ulnar flow reserve measured by Doppler ultrasonography before the harvest of radial artery.
METHODS: Forty patients whose radial artery was harvested for coronary bypass graft, were interviewed and tested 1 year after operation, and their preoperative ultrasonographic data compared.
RESULTS: Five patients (12.5%) had mild symptoms implying exercise intolerance. Exercise tests revealed severe decreases in tissue oxygenation in 7 patients (17.5%), but in accordance with symptoms (p = 0.0018). Tissue oxygenation in the operated hand was lower than in the nonoperated even in asymptomatic patients (p = 0.0011). Preoperative Doppler echography revealed that ulnar arteries of symptomatic patients were smaller (p = 0.0019) and carried lower blood flows during manual compression of the radial artery (p = 0.0004) compared with those of asymptomatic patients. Smaller ulnar arteries (less than 1.4 mm/m2) with poor flow reserves (less than 60 mL · min–1 · m–2 during radial compression) appear to indicate risks for exercise intolerance (p = 0.0004).
CONCLUSIONS: More than 10% of patients after harvest of radial arteries had mild symptoms implying exercise-intolerance, which accorded with abnormal tissue oxygenation during grip exercise. Work habits of patients should be considered in radial harvest decisions, especially if preoperative Doppler echography indicates lower flow reserves for the ulnar artery.
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Introduction
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The use of the radial artery (RA) as a coronary bypass graft is gaining acceptance because of its superior patency rate [1–3]. Severe hand ischemia after RA harvest is rare but annoying once it occurs, and thus has been much investigated [4, 5]. In contrast, the presence of exercise intolerance is not so extensively reported on. Although clinical significance was not clearly indicated, the presence of mild flow insufficiencies after harvest of RA has been pointed out in different analyses [6, 7]. Careful follow-up interviews of postoperative patients might reveal the presence of exercise intolerance, but an objective evaluation under an ascertained degree of exercise is essential to support even modest patient complaints. Recently it was demonstrated that the measurement of transcutaneous oxygen pressure (TcPO2) combined with exercise was a sensitive and objective way of assessing ischemia in iliac arteries [8]. Analysis of TcPO2 during hand exercise has also suggested the presence of hand ischemia during exercise, although the severity of complaints among the patients was not extensively analyzed [9]. To predict hand ischemia before RA harvest, an earlier study of ours indicated that a good marker was a low flow reserve of the ulnar artery, which is represented by preoperative ulnar blood flow during manual compression of the radial artery [10]. To demonstrate and evaluate the prevalence of exercise intolerance after RA harvest, and to investigate its relation with the flow reserve of the ulnar artery, symptoms were collated from face-to-face interviews and evaluated by TcPO2 measurement during grip exercise in 40 patients at 1 year after RA harvest during coronary bypass surgery, and compared with preoperative Doppler ultrasonography data.
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Material and methods
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Protocol and study patients
After obtaining informed consent, 40 patients (35 men and 5 women; mean age, 64.5 ± 9.1 years) were enrolled in the study and underwent a coronary bypass grafting operation using a RA graft. The technique of radial artery harvesting used has been described in previous reports [1, 2]: The radial artery was harvested as a pedicle accompanying veins and surrounding tissue. The use of electrical diathermy was kept to a minimum by using a surgical clip (LT100; Ethicon Inc, Cincinnati, OH). Ultrasonic coagulating shears (Harmonic Scalpel; Ethicon Endo-Surgery, Cincinnati, OH) were not used. Special care was taken to preserve the recurrent branch of the radial artery at the proximal end. Skin incisions were made no further than 2 cm proximal to the wrist crease. Patients with severe heart failure, unstable angina pectoris, peripheral vascular disease and renal dysfunction were excluded from the study group. Our institute has a practice of restricting the harvest of RA to the nondominant hands with negative Allen test. Working styles of patients have not been considered restrictively as exclusion criteria. Before operation, Doppler ultrasonography study was performed, and at 1 year after the operation patients were interviewed and underwent a grip exercise test.
Interview
A single investigator performed face-to-face interviews with all patients using an oral type questionnaire. Symptoms were admitted as significant only when there was a significant change between preand postoperation. Symptoms associated with exercise of the hand in their daily life activities after RA harvest were classified as follows: (1) asymptomatic group: no symptoms; (2) symptomatic group A: mild symptoms implying hand ischemia such as dullness, fatigue, or weakness of the hand during exercise; and (3) symptomatic group B: clear symptoms indicating hand ischemia such as pain, or cyanosis of the hand during exercise.
Doppler ultrasonography
Measurements were conducted on a 7.5-MHz linear transducer (SSA-380A; Toshiba, Tokyo, Japan) as performed previously [10]. For preoperative assessment, the internal diameter and mean velocity of the RA and ulnar artery at the wrist were recorded. Further, the mean velocity of the ulnar artery during compression of the radial artery was also measured, while the examiner digitally compressed the patient's radial artery at the wrist. For postoperative assessment in all patients, only the ulnar artery was examined. Two skilled examiners made all measurements in an air-conditioned room. The same examiner performed the preoperative and postoperative measurements in each patient. Before the measurements were taken, the patient was asked to lie down on the examining table for 10 minutes. As was described previously [10], blood flow volume was calculated using the following equation: Blood flow volume = (internal diameter/2)2 X 
X mean flow velocity. The mean flow velocity was calculated by machine after measuring the area under the spectral Doppler trace divided by time. After that, the values were converted to per body surface area.
Grip exercise test
The TcPO2 of the hand was measured during grip exercise as described previously [9]. In brief, hand exercise was achieved by keeping the hand gripped against the fixed resistance of a rolled cuff of a sphygmomanometer inflated at 100 mm Hg. During 5 minutes of exercise and after 2 minutes of rest, TcPO2 was measured by a commercially available probe (TCM-30 Radiometer; Copenhagen, Denmark) applied on the anatomic snuff-box. A stress test was conducted for both arms of all study patients. The decreased rate of oxygen pressure was expressed as the minimum value of the pressure during exercise divided by the starting value.
Statistical analysis
Results are expressed as means ± standard deviation. Difference in TcPO2 during grip exercise test was analyzed by repeated-measures analysis of variance (ANOVA). Other differences between the two means were compared by the Mann-Whitney test. Fisher's exact probability test was used to analyze differences in probability. All p values less than 0.05 were considered significant.
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Results
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Hand ischemic symptoms in daily life
Among the 40 patients who had their radial artery harvested, 5 (12.5%) were classified in the symptomatic group A. Their symptoms comprised hand fatigue when carrying a heavy bag in 4 patients, awareness of reduced grasping power in 2, and dullness of the thumb during hand exercise in 1. No patient was classified into symptomatic group B, with clear complaints indicating severe ischemia such as pain, or cyanosis during hand exercise. The other 35 patients (87.5%) were classified in the asymptomatic group. Therefore, the analysis was achieved by comparisons between the two groups, the symptomatic group A and the asymptomatic group. As for other complications that can be associated with radial harvesting, no patients suffered from wound infection or dehiscence. Three patients in the asymptomatic group experienced numbness in the forearm, and 1 patient in the symptomatic group suffered from slight paresthesia.
TcPO2 during grip exercise test
To demonstrate the general effect of radial harvest on oxygenation of the hand during exercise, TcPO2 in the operated and nonoperated hands was compared in all patients (Fig 1).
The TcPO2 in the nonoperated hand increased gradually during exercise. In contrast, the mean TcPO2 in the operated hand was lower than that in the nonoperated hand during exercise (repeated-measures ANOVA, p = 0.011) and declined further in the postexercise phase (Fig 1). If compared between the two groups with and without symptoms, TcPO2 in symptomatic group A showed a constant decline during exercise followed by a further decline during postoperative resting, which appears characteristic of ischemia (Fig 2).
The TcPO2 of the symptomatic patients was lower than that of the asymptomatic group during and after exercise (repeated-measures mixed design ANOVA, p = 0.026). The decrease of TcPO2 during exercise in each patient is shown in Figure 3.
Seven patients (17.5%) experienced a considerable drop (more than 10%) of TcPO2 during exercise and this had a significant correlation to their ischemic symptoms (p = 0.0018).
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Fig 1. General effects of radial harvest on transcutaneous oxygen pressure (TcPO2). Mean values of TcPO2 are compared during 5 minutes of grip exercise followed by 2 minutes of rest in hands with (open triangles) and without (closed triangles) harvest of the radial artery, in all patients. Error bar indicates standard deviation. *Significant difference between groups (repeated-measures ANOVA, p = 0.011).
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Fig 2. Transcutaneous oxygen pressure (TcPO2) in symptomatic patients in comparison with asymptomatic patients. Mean values of TcPO2 in the hand after harvest of the radial artery are compared during 5 minutes of grip exercise followed by 2 minutes of rest in patients in the symptomatic group A (open circles) and in those in the asymptomatic group (closed circles). Error bar indicates standard deviation. *Significant difference between the groups (repeated-measures mixed design ANOVA, p = 0.026).
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Fig 3. Variation of transcutaneous oxygen pressure (TcPO2) decrease in each patient. Decrease of TcPO2 during grip exercise is presented in each patient in the symptomatic group A and the asymptomatic group. Decrease is defined as the minimum value of TcPO2 during exercise divided by the starting value. The line indicates 10% decrease of TcPO2. *Significant difference between groups (p < 0.05).
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Doppler ultrasonography
Before RA harvest, the forearm territory was supplied with an average blood flow of 103.0 ± 34.4 mL · min–1 · m–2 through two major arteries (RA: 53.6 ± 24.8 mL · min–1 · m–2, and ulnar artery: 49.6 ± 16.8 mL · min–1 · m–2). After RA harvest, the blood flow through the remaining major artery, the ulnar artery, to the forearm territory showed a 20.5% decrease on average (81.9 ± 36.3 mL · min–1 · m–2, p = 0.011), which was almost comparable and predictable from the preoperative ulnar flow during the manual compression of the RA (76.0 ± 25.6 mL · min–1 · m–2; Y = 0.443 X + 46.4, r2 = 0.159, p = 0.0194). Patients in symptomatic group A had smaller ulnar diameters than those in the asymptomatic group (1.24 ± 0.06 versus 1.51 ± 0.19 mm/m2, p = 0.0034) and lower preoperative ulnar flows during compression of the RA (40.5 ± 12.3 vs 81.0 ± 22.9 mL · min–1 · m–2, p = 0.0004; Fig 4).
Ulnar flows during RA compression were correlated with ulnar diameter (Y = 96.9 X –67.1, r2 = 0.547, p < 0.01). Hand ischemia appears to be predictable from lower ulnar flow during compression if less than 60 mL · min–1 · m–2 (p = 0.0004) and from a smaller internal diameter of ulnar artery of less than 1.4 mm/m2 (p = 0.002).
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Fig 4. Ulnar artery diameter and flow reserve in each patient. Internal diameter and blood flow of the ulnar artery during compression of the radial artery in preoperative Doppler studies are shown for each patient in the symptomatic group A (open circles) and the asymptomatic group (closed circles). The line indicates 1.4 mm of internal diameter and 60 mL/min of blood flow in the ulnar artery during compression of the radial artery. Ulnar flows during radial artery compression correlate with ulnar diameter (y = 96.9, x –67.1, r2 = 0.547, p < 0.01).
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Comment
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Our careful face-to-face interviews to the patients revealed that modest symptoms implying exercise intolerance were present in more than 10% of patients in the year after RA harvest. To our surprise, however, no ischemic symptoms were recorded in most patients in the symptomatic group during routine follow-ups in the out-patient clinic, probably because any of their vague or minor symptoms did not seriously affect their daily life activities. Some patients in the symptomatic group unconsciously adopted an attitude to life that did not require frequent use of the hand after RA harvest. Infrequent symptoms they might have had were recalled during discussions in interviews. Therefore, most symptoms collated in the present study could possibly have been overlooked or considered as of nonischemic origin in most of the conventional surveys [1, 11]. However, their modest symptoms clearly matched the typical decrease of TcPO2 in the hand during grip exercise as suggested previously [12]. Grip exercise is a hard activity, keeping a fist against a pressure of 100 mm Hg for 5 minutes [9]. Therefore, abnormal results obtained in this test would not always represent a limitation of daily life. Among the 5 symptomatic patients in our series, only a fisherman involved in heavy manual labor had recognized that RA harvest was a possible cause of his symptoms. Therefore, if hand activity is high for a patient in daily life, even a mild insufficiency of blood flow could possibly affect quality of life. Another concern is whether this exercise intolerance is a temporary phenomenon after RA harvest or is it long-lasting. Although we did not have long-term data, Serrichio and associates [9] documented that the mild flow reduction to the hand persists in 5 years after RA harvest.
Exercise intolerance after RA harvest might not have been paid due attention in the past, in contrast to the catastrophic severe ischemia accompanying resting pain and necrosis [4, 5]. To avoid severe ischemia after RA harvest, the Allen test used to be performed in most institutes to exclude patients at risk of ischemia [13], as was employed in the present protocol. After this preoperative selection of patients, the prevalence rate of severe hand ischemia is low at around 0.03% [1]. Additionally, RA harvest is usually restricted to the nondominant hand of nonmanual workers [13]. Therefore, the clinical significance of exercise intolerance has possibly remained obscured. However, with increasing use of RA harvesting there is a chance that this complication might increase, especially if radial artery is harvested from a dominant hand or if a patient returns to frequent or heavy manual labor after operation.
Analysis under exercise appears critical for identifying mild flow insufficiencies resulting in exercise intolerance. Other sensitive tests, such as photographic plethsmography [6] and isotope (Tc-99 m) tissue perfusion [7], have also revealed mild flow decrease after RA harvest. However, flow decreases measured at rest still remained within the physiologic range [6, 7] and their clinical significance vague [6, 7]. Analysis under exercise became feasible by the introduction of TcPO2 measurement [9, 12]. The TcPO2 is a measure of the oxygenation on the surface, not in muscle. As a variable gradient in oxygen diffusion might exist between them, the raw value from TcPO2 measurement performed at rest might not represent muscle ischemia with any sensitivity, and be greatly affected by both central (cardiovascular and pulmonary status) and local factors (skin temperature and metabolic activity, and diffusion conditions such as epidermal thickness and composition) [14]. If combined with exercise, however, the changing pattern of TcPO2 can accurately represent muscle ischemia by virtually minimizing the influences from variable gradients under the skin [9]. Additionally, observation of TcPO2 more than 7 minutes appears long enough to detect any ischemic change, even in the case of slow oxygen diffusion across subcutaneous tissue. Around 80% sensitivity and specificity in TcPO2 was documented for detecting the presence of arterial occlusive disease in the buttock [8], and an even higher accuracy was expected for diagnosis of muscle ischemia itself [8]. The characteristic pattern of ischemia is an initial decrease of TcPO2 during exercise followed by a further decrease in the postexercise phase [12], which could clearly differentiate the exercise-induced muscle ischemia from simple malperfusion by mechanical compression caused by contracted muscles maintaining a fist in 100 mm Hg. The severity of the 10% decrease of TcPO2, which we observed in most symptomatic patients, indicates leg ischemia as Fontaine class II [12].
Ulnar flow reserve is thought determined by the largeness and completeness of the vascular bed in the palmar arch connected to the ulnar artery [10]. In a previous study we demonstrated that ulnar flow reserve could be measured by the preoperative ulnar blood flow during compression of the radial artery, and that this correlates well with postoperative ischemic events and with positive results of Allen tests [10]. Many reports have documented the measurement of Doppler ultrasonography as a useful tool to predict hand ischemia after RA harvest [6, 7, 15], although the most sensitive way to use it still needs to be determined [16, 17]. The present study confirmed that the simple measurement of ulnar flow reserve by manual compression of the radial artery, and the diameter of the ulnar artery could predict hand ischemia after RA harvest.
Most of the symptoms carefully collated in the present study are modest and do not seem to seriously affect patient life styles. However, the symptoms were clearly supported by an objective evaluation using TcPO2 during exercise. As it is technically difficult to measure TcPO2 during grip exercise while the radial artery is manually compressed, measurement of the ulnar flow reserve appears a useful alternative to predict the risk of future exercise intolerance before an operation. If the lifestyle or the profession of the patient requires hand exercise above a certain severity, the decision for RA harvest should best be done based on the quality of the ulnar flow reserve. Further studies with a larger number of patients are waited to confirm the suggestions indicated by the present study.
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Acknowledgments
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We sincerely appreciate the technical help from Makoto Iwashima, Takafumi Yamasaki, and Kouwa Fukuyama at the Kameda Medical Center, and statistical advice from Dr Keiko Nakamura.
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References
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Abstract
Introduction
