Ann Thorac Surg 2006;81:1700-1707
© 2006 The Society of Thoracic Surgeons
Original article: Cardiovascular
Long-Term Palmar Microcirculation After Radial Artery Harvesting: An Observational Study
Karsten Knobloch, MD
*
,
a
,
b
,
*
,
Sandra Tomaszek, MS
*
,
a
,
Artur Lichtenberg, MD
a
,
Matthias Karck, MD, PhD
a
,
Axel Haverich, MD, PhD
a
a Thoracic and Cardiovascular Surgery, Medical School Hannover, Hannover, Germany
b Trauma Surgery, Medical School Hannover, Hannover, Germany
Accepted for publication December 7, 2005.
* Address correspondence to Dr Knobloch, Trauma Surgery, Hannover Medical School, Carl-Neuberg-Str 1, Hannover 30625, Germany (Email: kknobi{at}yahoo.com).
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Abstract
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BACKGROUND: The aim of this study was to assess palmar microcirculation in a long-term follow-up after radial artery harvesting for coronary revascularization.
METHODS: One hundred fourteen patients (100 male; aged 61.7 ± 6.7 years; preoperative New York Heart Association 2.3 ± 0.6, ejection fraction 61.4% ± 13.9%) were included after undergoing elective coronary revascularization using the radial artery of the nondominant forearm with a nonpathologic Allen's test. Superficial and deep tissue oxygen saturation (SO2), postcapillary venous filling pressure (rHb), capillary blood flow, and capillary blood flow velocity were determined at a mean 25 ± 5 months after surgery using a combined laser Doppler spectrophotometry system.
RESULTS: At 2-mm tissue depth, there was a small, but significant, decrease of 3% of superficial SO2 at the thumb and the thenar eminence (D1: 75.3% ± 8.9% versus 77.6% ± 9.7%, p = 0.003; thenar: 71.5% ± 10.5% versus 73.2% ± 8.2%, p = 0.027). Deep palmar SO2 was changed significantly at 5 of 7 positions by 3%. Deep postcapillary venous filling pressure (8 mm) was significantly increased by 9% only at the fingertip of the fifth finger (112.4 ± 49.7 versus 103.0 ± 25.0, p = 0.033), while superficial capillary blood flow decreased by 13% at only 1 of 7 positions at the hypothenar eminence (242.0 ± 153.6 versus 275.6 ± 169.2, p = 0.009). Overall, only 2 of 56 positions exceeded a given threshold of 5% change of microcirculation. No clinical signs of malperfusion were found (postoperative New York Heart Association 1.1 ± 0.4, p < 0.05), and no patient was impaired in daily palmar motor activity.
CONCLUSIONS: Long-term objective evaluation of superficial and deep palmar microcirculation confirms that radial artery harvesting for coronary revascularization does not compromise palmar microcirculation.
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Introduction
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In 1971, Carpentier and associates [1] first described the use of the radial artery as a source for coronary artery bypass graft harvesting. The advantages of the radial artery as a graft source are the ease of harvesting, a low propensity for wound infection, a larger diameter than other arterial grafts, and a thick, muscular wall that facilitates the construction of a coronary anastomosis. Radial artery grafts provide excellent long-term patency. A randomized controlled trial in a total number of 561 patients found a 1-year angiography radial occlusion rate of 8.2% whereas for the saphenous vein, this was 13.6% [2]. Ten-year patency rates of 92% for the radial artery and 98% of the left internal thoracic artery have been reported in an observational study [3]. However, histologic studies [4] of distal and proximal radial artery specimens taken during coronary revascularization revealed the predictive factors for intimal hyperplasia of the radial artery graft to be age greater than 50 years (1.052), cigarette smoking (14.073), and arterial hypertension (2.777).
Concerns about reduced palmar blood flow after radial artery harvesting have been previously raised. Methods to assess forearm and palmar blood flow include forearm plethysmography [5] or technetium-99m albumin scans [6] and the clinical Allen test. Pulse volume recording plethysmography as a semiquantitative measurement found an overall decrease of digital blood flow after radial artery harvesting 7 days postoperatively in 24 patients predominantly in the first two fingers [7], which is concordant with findings by flow index differences calculated by photoelectric plethysmography [8].
Palmar microcirculation has been studied using a combined laser Doppler spectrophotometry system, the Oxygen to See (O2C) system (O2C OXYGEN TO SEE; LEA Medizintechnik, Giessen, Germany) system in a small initial patient group (n = 15) preoperatively and at the second postoperative day, revealing no significant differences in tissue oxygen saturation, postcapillary venous filling pressures, and capillary blood flow at 2- and 8-mm tissue depths [9]. However, the small patient group and the limited postoperative observation period for the assessment of microcirculation prompted us to examine whether radial artery harvesting changes the palmar microcirculation over the long term. We studied 114 patients, 25 months after radial artery harvesting for coronary revascularization (CABG), using detailed spatial analysis of palmar microcirculation at 14 positions at each hand using the real-time quantitative laser Doppler spectrophotometry system O2C.
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Patients and Methods
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Patients' Characteristics
One hundred fourteen patients (100 male; aged 61.7 ± 6.7 years; preoperative New York Heart Association status 2.3 ± 0.6 and ejection fraction 61.4% ± 13.9%; Table 1) participated in the study after informed consent. The Institutional Review Board approval had been given about the study by the local Ethics Committee in Hannover Medical School, Germany, in July 2004 before the study. Every person participated after further individual written consent. All patients had elective coronary revascularization because of coronary artery disease using the radial artery as either a free or T graft additionally to the left internal thoracic artery. Exclusion criteria included emergency revascularization, Raynaud's disease, evident palmar malperfusion or signs of ischemia before the radial artery harvesting, and a pathologic Allen test. The CABG procedure time was 212 ± 57 minutes, aortic cross-clamp time was 49 ± 24 minutes, and extracorporeal circulation time was 89 ± 42 minutes. Mean stay on the intensive care unit was 1.8 ± 3.5 days. Patient cardiovascular risk factors and postoperative physical activity are documented in Table 1. All radial artery grafts were harvested using the same technique from a forearm incision using an electric scalpel using a pedicle technique. Minimally invasive harvesting or radial skeletonized techniques were not used in this cohort. All grafts were perfused with papaverin solution to prevent early vasospasm, and all patients received diltiazem (90 mg twice a day) for at least 14 days to prevent radial artery vasospasm during the immediate postoperative period. The majority of radial arteries were used in the T-graft technique (73.9%), with 24.2% as a free graft and 1.4% as a jump graft.
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Table 1. Characteristics of the 114 Patients Undergoing Radial Artery Harvesting for Coronary Revascularization in This Study
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Power Analysis
Regarding different patient risk factors such as arterial hypertension, lipid disorders, body mass index, and sport activities, we performed a detailed power analysis to determine the number of patients needed to reach a significant difference (
= 0.050, two-sided test, power 80%), which is depicted in Table 2.
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Table 2. Power Analysis to Determine Total Number of Patients Needed and Number for Each Group to Get Significant Differences at D1 Microcirculation Regarding the Microcirculatory Variables Tissue Oxygen Saturation (SO2), Postcapillary Venous Filling Pressure (rHb), Capillary Blood Flow (Flow), and Capillary Blood Flow Velocity (Velocity)
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All palmar perfusion examinations were conducted 25 ± 5.3 months after radial artery harvest and were performed by the same experienced examiner with the O2C system under identical conditions in an ambient light room after equilibration. Seven identical positions on both hands (harvesting side of the radial artery and corresponding nonoperated side) were defined—the palmar side of each fingertip (D1-D5), and the thenar and hypothenar eminence—and measurements were conducted on the sitting patient with the arm in a stable resting position.
Determination of Microcirculation Noninvasively
A combined laser-Doppler and flowmetry system (O2C system; LEA Medizintechnik) was used in this study to evaluate microcirculation at two distinct tissue depths, 2 and 8 mm, noninvasively. The optical method for measuring both blood flow by laser-Doppler technique and hemoglobin oxygenation and hemoglobin concentration in tissue by spectrometric techniques has been described in detail elsewhere [10]. The determination of hemoglobin and the principle of blood flow measurement are combined in the O2C system. The local oxygen supply parameters, blood flow, oxygen saturation of hemoglobin SO2 (%), and amount of local hemoglobin rHb are recorded by an optical fiber probe (LEA Medizintechnik).
Laser Doppler Flowmetry
The tissue is illuminated with coherent laser light of 830 nm wavelength and 30 mW from a laser diode through a fiber optic light guide. Backscattered light is collected by the same probe, and frequency shifted light extracted by a heterodyne light beating technique. The power-spectral density of shifted light is a linear function of the average velocity of moving cells within the tissue. As laser Doppler flowmetry detects all moved particles of certain velocity, it measures blood flow.
Measurement of Volume
Laser Doppler perfusion measurements can increase sampling depth by using near-infrared laser light and changing detector geometry. In the near-infrared range, a mathematical model for measurements of skin blood oxygenation estimated a fiber separation of 400 to 800 µm for the blood sample. A measurement depth of 3.4 mm was shown with a fiber separation of 6 mm with fiber diameter of 3 mm.
Tissue Spectrophotometry
Light of the visible range is irradiated into tissue using a glass fiber probe, and the backscattered spectrum is measured over the range from 500 to 630 nm by the same probe. Light penetrates the tissue and is partly absorbed, reflected, and scattered. The main light absorber, hemoglobin, changes its absorption characteristics with oxygen saturation. Fully oxygenated hemoglobin has two absorption peaks at 542 and 577 nm, deoxygenated blood has one at 556 nm. By fitting measured spectra with spectra of known oxygen saturation, the oxygen saturation of the microvessel blood is calculated with appropriate algorithms of the additional absorption by other tissue chromophores like melanin and cytochrome. Measured spectra are further influenced by the path length of photons through tissue. Different tissue models have been used in the past to simulate the path of a photon through tissue, to determine multiple scattering influences on absorbance spectra. Here, a modified diffusion approximation to the transport equation is used, and includes changes in the complete spectra to estimate scattering, so absolute oxygen saturation values can be calculated. Information is mainly gathered from small arteries, capillaries, and venules, as light entering vessels larger than 100 µm is completely absorbed [11]. As 85% of the hemoglobin is in the capillary-venous compartment of the microcirculation, measurements with the spectrophotometer reflect mainly the capillary-venous oxygen saturation.
Oxygen saturation of hemoglobin is calculated in percent SO2, which is an absolute measure. The local amount of hemoglobin is calculated in relative units rHb (rAU), processed from the spectral absorption of the hemoglobin. The hemoglobin amount (rHb) is measured by the sum of absorption at all wavelengths ("area under the curve") and is corrected by the characteristic differences in absorption; fully oxygenated blood absorbs about 15% more than deoxygenated blood. As with hemoglobin measurement, volume change is measured. The hemoglobin values are relative values and reflect the filling of vessels or vessel density per catchment volume.
The O2C system is a combined laser Doppler spectrophotometry system and has been validated in vivo in humans in clinical conditions such as cardiac surgery in measuring the sternal microcirculation after harvesting of the pedicled left internal thoracic artery [12], and orthopedic surgery [13, 14]. The intraobserver reliability of the laser Doppler in the O2C system has been established with a 5% intrasubject variability, indicating that the laser Doppler is a reliable method for assessing tissue perfusion under standardized test conditions [15].
Statistics
The data are presented as mean and standard deviation for continuous variables or number and percentages for dichotomous variables. Paired t tests were conducted to compare microcirculation SO2, rHb, flow, and velocity in the operated hand and the nonoperated hand, and a p value less than 0.05 was considered to indicate significance. The general linear model with multivariate testing was applied to control the results for the measured difference between both hands. For the latter, a p value in the Wilks-Lambda score of less than 0.05 was considered to be of significance. The SPSS statistical software package 12.0 OG for Windows (SPSS, Chicago, Illinois) was used for statistical analysis.
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Results
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Superficial and Deep Palmar Tissue Oxygen Saturation
At 2-mm tissue depth, there was a small, but significant decrease of 3% in total of superficial palmar tissue oxygen saturation at the thumb (D1) and the thenar eminence (thenar) of the operated hand in comparison with the nonoperated hand (D1: 75.3% ± 8.9% versus 77.6% ± 9.7%, p = 0.003; thenar: 71.5% ± 10.5% versus 73.2% ± 8.2%, p = 0.027; Fig 1A; Table 3). However, the sensitivity of the method for noninvasive determination of tissue oxygen saturation has a stated range of 3% to 5%, so the significance may be marginal. Superficial palmar tissue oxygenation in the second, third, fourth, and fifth finger, and at the hypothenar eminence were not significantly different on the operated and the nonoperated hand 25 months after radial artery harvesting.
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Fig 1. (A) Tissue oxygen saturation (OxSat) at the thenar (Th) at 2 mm at the operated (radial artery harvesting) versus the nonoperated side (p = 0.027); and (B) at the thenar (Th) at 8 mm at the operated (radial artery harvesting) versus the nonoperated side (p = 0.004).
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Table 3. Mean Values of Microcirculation (Tissue Oxygen Saturation, Relative Postcapillary Filling Pressures [rHb], Capillary Blood Flow and Capillary Blood Flow Velocity at 2- and 8-mm Tissue Depths) 25 ± 5 Months After Radial Artery Harvesting for Coronary Revascularization (n = 114) at Fingertips D1/2/3/4/5, Thenar, and Hypothenar on Operated Hands (First Number) and Nonoperated (Second Number) Hands
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Deep palmar oxygen saturation was significantly changed at five of the seven positions. At both the thenar and the hypothenar, deep palmar oxygen saturation was slightly, but significantly, decreased by 3% (thenar: 73.9% ± 8.0% versus 76.6% ± 9.0%, p = 0.004; hypothenar: 82.8% ± 8.5% versus 85.7% ± 8.5%, p = 0.0001). In contrast to those measurements, we found a small, but significant increase of as much as 2% of deep tissue oxygen saturation at the fingertips of the index finger (D2), the third finger (D3), and the fourth finger (D4) in comparison of the operated and the nonoperated hand (D2: 91.1 ± 7.1 versus 89.2 ± 8.5, p = 0.005; D3: 90.8 ± 7.6 versus 89.3 ± 8.1, p = 0.014; D4: 90.7 ± 8.0 versus 89.4 ± 8.0, p = 0.027; Fig 1B). While these variations of deep palmar oxygen saturation of 3% or less are within the estimated measurement resolution of the method, they seem not to reflect clinical relevant real long-term changes of palmar microcirculation associated with radial artery harvesting.
Superficial and Deep Postcapillary Venous Filling Pressures
Superficial postcapillary venous filling pressures at 2-mm tissue depth were not significantly changed in 114 patients 25 months after surgery at any of the five fingertips, the thenar, and the hypothenar (Fig 2A). Deep postcapillary venous filling pressures at 8-mm tissue depth were significantly increased by 9% at the fingertip of the fifth finger on the operated side relative to the nonoperated side (112.4 ± 49.7 versus 103.0 ± 25.0, p = 0.033), while no significant changes between the operated and the nonoperated hand were found at the thenar, the first, second, third, fourth finger, or the hypothenar (Fig 2B).
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Fig 2. Postcapillary venous filling pressures (rHb) at the operated versus the nonoperated side 25 months after radial artery harvesting, with no significant difference among 114 patients at the first finger (D1) at either (A) 2-mm tissue depth or (B) 8-mm tissue depth.
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Superficial and Deep Capillary Blood Flow
Superficial capillary blood flow determined noninvasively using the laser Doppler technique was found to be significantly decreased (by 13%) at only one of seven interrogation positions, the hypothenar eminence, with operated and nonoperated values of 242.0 ± 153.6 versus 275.6 ± 169.2 (p = 0.009; Fig 3A). Superficial capillary blood flow at the thenar, the first, second, third, fourth, and fifth fingers were not significantly different in the operated hands compared with the nonoperated hands. Deep capillary blood flow was found not be significantly different at all seven palmar positions 25 months after radial artery harvesting in 114 patients (Fig 3B).
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Fig 3. Capillary blood flow at the operated versus the nonoperated side 25 months after radial artery harvesting, with no significant difference among 114 patients at the first finger (D1) at (A) the 2-mm tissue depth and (B) the 8-mm tissue depth.
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Superficial and Deep Capillary Blood Flow Velocity
Palmar superficial capillary blood flow velocity measured at any position showed no significant difference in patients after radial artery harvesting. Deep capillary blood flow velocity was significantly different only in one of seven positions, the fingertip of the fifth finger of the radial artery harvested side. The harvested side had an increased deep capillary blood flow velocity of 3.5% (D5: 76.0 ± 17.7 versus 73.4 ± 18.4, p = 0.031), which, again, is barely greater than the resolution of the measuring method. Deep capillary blood flow at the thenar, the first, second, third, fourth finger, and the hypothenar showed no significantly different changes after harvesting.
Clinical Data on the 114 Patients
Capillary refill was within 2 s in 109 of 114 patients after radial artery harvesting, in 3 of 114 beyond 2 s, and in 2 of 114 not determined. Blood pressure on the radial harvested side (systolic 126 ± 15 mm Hg and diastolic 74 ± 10 mm Hg) was not significantly different from that on the unoperated hand (systolic 125 ± 14 mm Hg and diastolic 73 ± 10 mm Hg). Twenty-eight patients (25%) remained on calcium-channel blockers 25 months after radial artery harvesting, 70 patients remained on aspirin (61.4%), 33 on clopidogrel (28.9%), and 11 on phenprocoumon (9.6%) since their bypass operation.
Neurologic Complications
No patients had impaired hand function after radial artery harvesting. All 114 patients studied retained their motor skills such as piano playing, computer operation, writing, or performing sports such as tennis or volleyball at the same level as before the operation. Ninety-eight patients remained free of neurologic numbness at the harvested side, whereas 3 complained of numbness in the region of the medial cutaneus antebrachii nerve, and 8 complained of numbness in the region of the lateral cutaneus antebrachii nerve (Fig 4A). One hundred one patients did not complain of any hyposensitivty at the radial artery harvested side, but 2 complained of hyposensitivity in the lateral region of the cutaneous antebrachii nerve, 3 in the region of the radial nerve, and 6 in the medial or lateral region of the cutaneous antebrachii nerve (Fig 4B).
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Fig 4. (A) Distribution of numbness 25 ± 5 months after radial artery harvesting in coronary revascularization in 114 patients. (B) Distribution of hyposensibility 25 ± 5 months after radial artery harvesting in coronary revascularization in 114 patients.
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Comment
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Radial artery harvesting for coronary revascularization does not change overall measurements of palmar microcirculation at follow-up 26 months after surgery, and no physical impairment was reported regarding their daily palmar motor activity, such as piano playing, writing, typing, or performing racket sports such as tennis. However, small and significant differences of tissue oxygen saturation were detected at some positions on the radial harvested hands compared with the nonoperated hands. The superficial thumb and thenar tissue oxygen saturation was reduced 3% (p = 0.003, p = 0.027, respectively), indicating that collateral palmar flow compensates nearly completely for the absent radial artery, if this difference is not attributed to the resolution of the spectrophotometry system. Postcapillary venous filling pressures as well as capillary blood flow and capillary blood flow velocity have been found to be unchanged at seven of seven superficial or six of seven deep tissue positions. Interestingly, deep tissue oxygen saturation at the second to fourth fingertip on the nonoperated hands was less than the corresponding position on the radial artery harvested side (3% difference). Again, this could be explained as measurement artefact and related to the resolution of the spectrophotometer device.
The smaller tissue oxygen saturation at the midportion of the fingers was not associated with an increased capillary blood flow from the collateral ulnar artery or from the interosseus artery or with significant changes in postcapillary venous filling pressures. Therefore, despite the significant differences of 3% detected in this study, these changes might be explained by the resolution of the O2C system, quoted as intrasubject variability of 5%. Therefore, as all changes were less than 3%, except the 13% increase of the deep postcapillary venous filling pressure at the fingertip of the fifth finger, it is reasonable to conclude that radial artery harvesting does not result in disturbed microcirculation 25 months after surgery.
The significance of this study relates to the large number of patients (n = 114), the long-term follow-up (25 months), and the quantitative assessment of microcirculation using a novel noninvasive laser Doppler spectrophotometry method. These data are concordant with pulse volume recording plethysmography and 39 ± 3 months of follow-up, which demonstrated in a small patient group (n = 15) that radial artery harvesting decreased distal blood flow immediately after operation but that this flow recovers [16].
Limitations
We used a conventional pedicled surgical harvesting technique for the radial artery in this study performed by different surgeons in one cardiothoracic department, so the surgical expertise of different cardiothoracic surgeons was not controlled. However, radial graft perfusion using papaverin was the same in all patients as was the postoperative administration of a calcium-channel blocker (diltiazem) for 14 days to prevent vasospasm. Additionally, this study used the nonoperated hand as a control, with assumed normal circulation. That may not have been universally valid and may explain the few aberrant results.
Novel harvesting techniques, such as the minimally invasive radial artery harvesting technique [17], were not evaluated in this study, and these results cannot be extrapolated to this patient group. It could be hypothesized that skeletonized radial artery harvesting techniques[18] might influence postcapillary venous filling pressures, but that would require further study.
The combined laser Doppler spectrophotometry system incorporated in the O2C system has a reported intrasubject variability of 5%. Therefore, even significant changes of microcirculation of 3% or less might be within the measurement resolution of the system. Despite this, only 2 of 56 measures exceeded the 5% threshold in 114 patients: the 9% increase of postcapillary venous filling pressure at the deep fingertip of the fifth finger and the 13% decrease of superficial capillary blood flow at the hypothenar eminence, neither of which had clinical signs of malperfusion.
In summary, long-term superficial and deep palmar microcirculation changed only slightly regarding tissue oxygen saturation, postcapillary venous filling pressures, capillary blood flow, and capillary blood flow velocity in 114 patients 26 months after radial artery harvesting for coronary revascularization without clinical relevant signs of malperfusion or any deterioration of palmar motor function.
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The Society of Thoracic Surgeons Policy Action Center
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The Society of Thoracic Surgeons (STS) is pleased to announce a new member benefit—the STS Policy Action Center, a website that allows STS members to participate in change in Washington, DC. This easy, interactive, hassle-free site allows members to:
- • Personally contact legislators with one's input on key issues relevant to cardiothoracic surgery
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- • Research the proposed policies that help—or hurt— one's practice
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This website is now available at www.sts.org/takeaction.
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Footnotes
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* Both authors contributed equally to this work. 
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References
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- Desai ND, Cohen EA, Nayloer CD, Fremes SE, Radial Artery Patency Study Investigators A randomized comparison of radial-artery and saphenous-vein coronary bypass grafts N Engl J Med 2004;351:2302-2309.[Abstract/Free Full Text]
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- Knobloch K, Lichtenberg A, Pichlmaier M, Tomaszek S, Krug A, Haverich A. Palmar microcirculation following harvesting of the radial artery in coronary revascularisation Ann Thorac Surg 2005;79:1026-1030.[Abstract/Free Full Text]
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Abstract
Introduction
