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Asian Cardiovasc Thorac Ann 2007;15:486-492
© 2007 Asia Publishing EXchange Ltd


ORIGINAL CONTRIBUTIONS

Age Deteriorates Palmar Microcirculation Following Radial Artery Harvesting

Karsten Knobloch, PhD, Sandra Tomaszek, MD1, Axel Haverich, PhD1, Peter M Vogt, PhD

Plastic, Hand and Reconstructive Surgery
1 Thoracic and Cardiovascular Surgery, Hannover Medical School, Hannover, Germany

For reprint information contact: Karsten Knobloch, PhD Tel: 49 511 532 8849 Fax: 49 511 532 8890 email: kknobi{at}yahoo.com, Plastic, Hand and Reconstructive Surgery, Hannover Medical School, Carl-Neuberg-Str. 1, 30625 Hannover, Germany.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The effect of age as a risk factor for deterioration of palmar microcirculation after radial artery harvesting for coronary revascularization is unknown. In 114 patients aged 61.7 ± 6.7 years undergoing radial artery harvesting, superficial and deep tissue oxygen saturation, postcapillary venous filling, and capillary blood flow were determined using a combined laser Doppler spectrophotometry system 25 ± 5 months after surgery. Superficial and deep oxygen saturation at the harvested thenar eminence decreased with age. In the nondonor hand, oxygen saturation declined in the first and second digits. Postcapillary venous filling pressure in both thenars increased with age. It was concluded that neurological complications do not correlate with age. Palmar tissue oxygen saturation, palmar capillary blood flow, and blood velocity decrease, while postcapillary venous filling pressure significantly increases with age. Radial artery harvesting for coronary revascularization does not compromise palmar microcirculation to the same extent as age. A cut-off value of ≤ 67 years was determined by microcirculatory assessment; beyond this, significant deterioration of palmar microcirculation is more likely to occur.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Radial artery (RA) grafts used in coronary artery bypass grafting (CABG) provide excellent long-term patency.1,2 A randomized controlled trial in 561 patients found a 1-year angiographic RA occlusion rate of 8.2%, while for saphenous vein grafts it was 13.6%.3 Ten-year patency rates of 92% for RA grafts and 98% for the left internal thoracic artery have been reported.4 However, histological studies of distal and proximal RA specimens (mean age, 54 ± 11 years; range, 28–72 years) taken during CABG revealed the predictive factors for intimal hyperplasia of the RA graft to be age > 50 years, cigarette smoking, and arterial hypertension.5 Age as a risk factor for endothelial dysfunction is acknowledged, but to what extent age might interfere with the microcirculation is unknown. Furthermore, no recommendations regarding a cut-off age for RA harvesting have been established. Other risk factors such as smoking and menopause have been shown to affect the microcirculation.6 The number of cardiovascular risk factors correlates significantly with the duration of reactive hyperemia determined by plethysmography in men and women.7 Palmar microcirculation has been studied in a small patient group preoperatively and on the 2nd postoperative day, revealing no significant differences in tissue oxygen saturation, postcapillary venous filling pressure, and capillary blood flow at 2 and 8-mm tissue depths, and also in a long-term perspective study using detailed spatial analysis of palmar microcirculation.8,9 Based on these results, and given the lack of quantitative data, we sough to determine the effect of age on palmar microcirculation in patients undergoing CABG.


    PATIENTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Approval for the study was obtained from the ethics committee of Hannover Medical School, and every subject give written consent. All patients had elective CABG because of coronary artery disease, using the RA as either a free graft or a T-graft with the left internal thoracic artery. Exclusion criteria included emergency revascularization, Raynaud’s disease, evident palmar malperfusion or signs of ischemia prior to RA harvesting, and a pathologic Allen test. The 114 enrolled patients were divided into 4 age groups as shown in Table 1Go which lists the cardiovascular risk factors and perioperative data. All RA grafts were harvested by the same pedicle technique from a forearm incision, using an electric scalpel. Minimally invasive harvesting or skeletonized techniques were not used. All grafts were perfused with papaverine solution to prevent early vasospasm, and all patients received diltiazem (90 mg twice daily) for at least 14 days to prevent RA vasospasm during the immediate postoperative period. The RA was used as a T-graft in the majority of cases (73.9%).


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Table 1. Characteristics of 114 Patients in 4 Age Groups Undergoing Radial Artery Harvesting for Coronary Revascularization
 
Palmar perfusion studies were conducted at 25 ± 5.3 months after RA harvest by the same experienced examiner using the O2C (oxygen to see) system (LEA Medizintechnik, Giessen, Germany) under identical conditions in ambient light after equilibration. Seven positions on both hands were defined: the palmar side of each fingertip (D1–D5), and the thenar and hypothenar eminences. Measurements were conducted with the patient seated with the arm in a stable resting position. The microcirculation was assessed noninvasively at 2 tissue depths: 2 and 8 mm. The optical methods for measuring blood flow by laser Doppler and hemoglobin oxygenation and concentration by spectrometry have been described elsewhere.10 The determination of hemoglobin and the principle of blood flow measurement are combined in the O2C system. Local oxygen supply parameters, blood flow, hemoglobin oxygen saturation (SO2), and relative hemoglobin concentrations were recorded by a fiberoptic probe. Local relative hemoglobin is determined by the amount of absorbed light; as hemoglobin is the strongest light absorber in tissue, the greater the amount of blood, the more light will be absorbed. The O2C system calculates the relative hemoglobin from the absorbed amount for the illuminated tissue volume, which gives a measurement of blood vessel filling (in arbitrary units). This measurement represents an amount of hemoglobin per tissue volume and is independent of vessel density, vessel lumen, and hemoglobin quantity in the blood. The O2C system is a combined laser Doppler spectrophotometry system that has been validated in vivo in humans under clinical conditions, such as measuring the sternal microcirculation after harvesting the pedicled left internal thoracic artery.11

Data are presented as mean ± standard deviation for continuous variables, or numbers and percentages for dichotomous variables. To determine the influence of age, data were correlated with age by either the Pearson or Spearman-rho method, depending on Gaussian distribution, and with age group by one-way analysis of variance (ANOVA). Paired t tests or the Wilcoxon test were conducted for each age group to compare microcirculation SO2, relative hemoglobin, and capillary flow in the hands on the donor and nondonor sides; a p value < 0.05 was considered to indicate significance. For intergroup comparison, the one-way ANOVA Scheffé post-hoc test was applied. To determine a cut-off level of age, the Mann-Whitney U test was used. A boxplot (also known as a box-and-whisker diagram) was used to depict the 5-number summary, which consists of the smallest observation, lower quartile, median, upper quartile, and largest observation; in addition, the boxplot indicates which observations, if any, are considered unusual, or outliers. SPSS statistical software package 13.0 for Windows (SPSS Inc., Chicago, IL, USA) was used for statistical analysis. Nonsignificant data were evaluated by power analysis; regarding the effect of age, SO2 and relative hemoglobin, flow power ranged between 60% and 80%.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Palmar tissue SO2 declined with age. At the 2-mm tissue depth, a significant influence of age was found in several positions (Table 2Go). Age had no significant influence on postcapillary venous filling pressure at 2-mm tissue depth, but at 8 mm, it increased with age (Table 3Go). The relative hemoglobin of the thenar eminences of both hands were significantly increased in intergroup comparisons (Figures 1Go and 2Go), but there was no significant difference in relative hemoglobin between donor and nondonor hands. As shown in Table 4Go and Figure 1CGo, superficial capillary blood flow determined noninvasively using the laser Doppler technique decreased with age; a significant influence of age was found in 8 of 14 positions. Deep capillary blood flow also decreased with age.


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Table 2. Tissue Oxygen Saturation (%) by Age Group
 

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Table 3. Postcapillary Venous Filling (in Arbitrary Units) by Age Group
 

Figure 1
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Figure 1. Superficial (2 mm) thenar microcirculation after radial artery harvesting, in relation to age. (A) Thenar tissue oxygen saturation (OxSat). (B) Thenar postcapillary venous filling pressure, measured as relative amount of hemoglobin (rHb). (C) Thenar capillary blood flow in arbitrary units (AU). The p values indicate the level of significance of the difference between the operated (OP) vs the non-operated (non-OP) side at each given age quartile.

 

Figure 2
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Figure 2. Deep (8 mm) thenar microcirculation after radial artery harvesting, in relation to age. (A) Thenar tissue oxygen saturation (OxSat). (B) Thenar postcapillary venous filling pressure, measured as relative amount of hemoglobin (rHb). (C) Thenar capillary blood flow in arbitrary units (AU). The p values indicate the level of significance of the difference between the operated (OP) vs the non-operated (non-OP) side at each given age quartile.

 

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Table 4. Capillary Blood Flow (in Arbitrary Units) by Age Group
 
A cut-off age of 67 years was calculated. Data of the 24 patients > 67 years were significantly worse than the 90 patients ≤ 67 years old, as illustrated by SO2 at 2 mm in the thenar eminence of the donor hand (66% ± 15% vs 73% ± 8%; p = 0.030), with capillary blood flow (in arbitrary units) at 2 mm (122 ± 122 vs 280 ± 180; p < 0.001) and at 8 mm (205 ± 135 vs 389 ± 173; p < 0.001); as well as for the nondonor hand (capillary blood flow at 2 mm: 168 ± 119 vs 293 ± 178; p = 0.002, and at 8 mm: 298 ± 168 vs 393 ± 163; p = 0.013).

Capillary refilling was < 2 sec in 109 patients (95.6%) after RA harvesting, > 2 sec in 3 (2.6%), and not determinable in 2 (1.8%). Capillary refilling was not significantly impaired with age in either hand. Normal capillary refilling (< 2 sec) in the RA donor side was found in 94.4% of the younger patient group (≤ 67 years) vs 100% of the older group ( p = 0.814), which was the same in the nondonor side (94.4% vs 100%). Blood pressure on the RA donor side (systolic 126 ± 15, diastolic 74 ± 10 mm Hg) was not significantly different from the nondonor side (systolic of 125 ± 14, diastolic 73 ± 10 mm Hg). There were 28 (25%) patients still on calcium-channel blockers 25 months after RA harvesting, 70 remained on aspirin (61.4%), 33 on clopidogrel (28.9%), and 11 on phenprocoumon (9.6%). No patient had impaired hand function after RA harvesting; all 114 retained their motor skills such as piano playing, computer operation, writing, or performing sports such as tennis or volleyball, at the same level. There was no difference between the older (> 67 years) and younger patients regarding differentiation of cold and hot, ability to form a fist, apposition of the thumb, or numbness, and we could not demonstrate any effect of advanced age on neurological deterioration after RA harvesting.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The major findings of this study were that palmar tissue oxygen saturation and palmar capillary blood flow decrease with age, while postcapillary venous filling pressure significantly increases with age, and a cut-off age of 67 years was determined, beyond which significant deterioration of the palmar microcirculation is likely to occur. Radial artery harvesting for coronary revascularization does not compromise palmar microcirculation to the same extent as age. Currently, no microcirculatory data are available regarding dependency on age. Neurological complications do not correlate with advanced age.

Palmar tissue oxygen saturation is the major indicator of palmar oxygen supply; a decline is related to limited metabolic function in the microcirculation, thus deteriorating palmar cell perfusion. A decline of tissue oxygen saturation is seen in ischemia, such as after supra-systolic compression of the forearm.9 Palmar capillary blood flow decreased significantly with increasing age. Thus perfusion is limited with progressing arteriosclerotic disease. Increased postcapillary venous filling pressures indicate deterioration of the clearance function of local metabolic endproducts from the capillary bed. This capillary venous congestion promotes venous stasis with consequent local thrombosis and/or possible inflammation. After pedicled harvesting of the left internal mammary artery, we could demonstrate a significant increase of retrosternal postcapillary venous filling pressures in line with a significant decrease of retrosternal oxygen saturation and capillary flow, which might promote deep retrosternal infections. On the other hand, modification of the harvesting technique to skeletonized harvesting of the mammary artery showed a beneficial effect on microcirculatory parameters, such as preserved low-level postcapillary venous filling pressures.

The vascular endothelium plays an important role in modulating vascular homeostasis, as it is a source of numerous vasorelaxing, antithrombotic, and antiproliferative mediators. In uremic patients awaiting arteriovenous fistula operations, the RA intima-media thickness was significantly thicker (0.41 ± 0.09 mm) compared to hypertensive (0.33 ± 0.05 mm) or healthy patients (0.25 ± 0.04), measured by high-resolution ultrasonography, which correlated significantly with the results of histological examinations in 43 uremic patients.12

Age alone has been shown to influence outcomes after CABG or valve surgery. Octogenarians undergoing cardiac surgery had more comorbidities and higher mortality than younger patients, even after controlling for 16 potential confounding variables, which is in line with the results of a New York study stating that age ≥ 80 years was an independent predictor of increased resource utilization, postoperative morbidity, and mortality.13 Coronary artery bypass grafting with extracorporeal circulation results in a dramatic drop in testosterone levels in men > 70 years old, a significant decline in insulin-like growth factor I in both sexes, and elevated serum cortisol levels.14 It was suggested that these hormonal changes may at least partially explain why the elderly need prolonged rehabilitation after CABG. From a financial point of view, hospital costs can be identified by length of stay in the intensive care unit.15 A recent multivariate analysis among 7,553 patients undergoing cardiac surgery found older age to be an independent predictor of prolonged ventilation, which is associated with significantly increased hospital mortality and costs as well as poor 5-year survival.16

Some limitations of this study must be mentioned. We used a conventional pedicled surgical harvesting technique employing electrocautery, which is believed to be superior to sharp dissection of the RA, in this study performed by different surgeons in one cardiothoracic department, so the surgical expertise of different cardiothoracic surgeons was not controlled. However, RA graft perfusion using papaverine was the same in all patients, as was the postoperative administration of a calcium-channel blocker (diltiazem) for 14 days to prevent vasospasm. A recent study found that RA contraction induced by rapid temperature changes could be blocked by glyceryl trinitrate, but not by phenoxybenzamine, while papaverine and calcium-channel blockers had only limited activity.17 The limited effects of papaverine and diltiazem are in line with a recent study from Turkey, where nitroglycerin was found to be the best agent to prevent RA spasm.18 However, accumulating data suggest that papaverine is not only of limited use, but also denudes the endothelium, which was not known prior the RA follow-up study in our Medical School.19 In addition, this study used the nondonor hand as a control, with normal circulation assumed. This may not have been universally valid and may explain the few aberrant results. Novel harvesting techniques, such as minimally invasive RA harvesting, were not evaluated in this study, and the results cannot be extrapolated to this patient group. It could be hypothesized that skeletonized RA harvesting techniques might influence postcapillary venous filling pressures, but this would require further study. The combined laser Doppler spectrophotometry system has a reported intra-subject variability of 5%.

It was concluded from this study that palmar tissue oxygen saturation and palmar capillary blood flow decrease, while postcapillary venous filling pressures significantly increase with age. Radial artery harvesting for coronary revascularization does not compromise palmar microcirculation to the same extent as age. Beyond 67 years old, significant deterioration of palmar microcirculation is likely to occur. Neurological complications do not correlate with advance age, so in patients ≤ 67 years, there seems to be no contraindication to the use of the radial artery for CABG.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Carpentier A, Guermonprez JL, Deloche A, Frechette C, DuBost C. The aorta-to-coronary radial artery bypass graft. A technique avoiding pathological changes in grafts. Ann Thorac Surg 1973;16:111–21.[Medline]

  2. Chowdhry TM, Loubani M, Galinanes M. Mid-term results of radial and mammary arteries as the conduits of choice for complete arterial revascularization in elective and nonelective coronary bypass surgery. J Card Surg 2005;20:530–6.[Medline]

  3. Desai ND, Cohen EA, Naylor 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;351:2302–9.[Abstract/Free Full Text]

  4. Possati G, Gaudino M, Prati F, Alessandrini F, Trani C, Glieca F, et al. Long-term results of the radial artery used for myocardial revascularization. Circulation 2003;108:1350–4.[Abstract/Free Full Text]

  5. Chowdhury UK, Airan B, Mishra PK, Kothari SS, Subramaniam GK, Ray R, et al. Histopathology and morphometry of radial artery conduits: basic study and clinical application. Ann Thorac Surg 2004;78:1614–22.[Abstract/Free Full Text]

  6. Bercovici B, Davis E. The effect of smoking and menopause on the small blood vessels. Microcirc Endothelium Lymphatics 1991;7:51–6.[Medline]

  7. Ishibashi Y, Takahashi N, Shimada T, Sugamori T, Sakane T, Umeno T, et al. Short duration of reactive hyperemia in the forearm of subjects with multiple cardiovascular risk factors. Circ J 2006;70:115–23.[Medline]

  8. Knobloch K, Lichtenberg A, Pichlmaier M, Tomaszek S, Krug A, Haverich A. Palmar microcirculation following harvesting of the radial artery in coronary revascularization. Ann Thorac Surg 2005;79:1026–30.[Abstract/Free Full Text]

  9. Knobloch K, Tomaszek S, Lichtenberg A, Karck M, Haverich A. Long-term palmar microcirculation after radial artery harvesting. An observational study. Ann Thorac Surg 2006;81:1700–7.[Abstract/Free Full Text]

  10. Frank KH, Kessler M, Appelbaum K, Dummler W. The Erlangen micro-lightguide spectrophotometer EMPHO I [Review]. Phys Med Biol 1989;34:1883–900.[Medline]

  11. Knobloch K, Lichtenberg A, Pichlmaier M, Mertsching H, Krug A, Klima U, et al. Microcirculation of the sternum following harvesting of the left internal mammary artery. Thorac Cardiovasc Surg 2003;51:255–9.[Medline]

  12. Ku YM, Kim YO, Kim JI, Choi YJ, Yoon SA, Kim YS, et al. Ultrasonographic measurement of intima-media thickness of radial artery in pre-dialysis uraemic patients: comparison with histological examination. Nephrol Dial Transplant 2006;21:715–20.[Abstract/Free Full Text]

  13. Scott BH, Seifert FC, Grimson R, Glass PS. Octogenarians undergoing coronary artery bypass graft surgery: resource utilization, postoperative mortality, and morbidity. J Cardiothorac Vasc Anesth 2005;19:583–8.[Medline]

  14. Maggio M, Ceda GP, De Cicco G, Cattadori E, Visioli S, Ablondi F, et al. Acute changes in circulating hormones in older patients with impaired ventricular function undergoing on-pump coronary artery bypass grafting. J Endocrinol Invest 2005;28:711–9.[Medline]

  15. Hekmat K, Raabe A, Kroener A, Fischer U, Suedkamp M, Geissler HJ, et al. Risk stratification models fail to predict hospital costs of cardiac surgery patients. Z Kardiol 2005;94:748–53.[Medline]

  16. Rajakaruna C, Rogers CA, Angelini GD, Ascione R. Risk factors for and economic implications of prolonged ventilation after cardiac surgery. J Thorac Cardiovasc Surg 2005;130:1270–7.[Abstract/Free Full Text]

  17. Oo AY, Conant AR, Chester MR, Dihmis WC, Simpson AW. Temperature changes stimulate contraction in the human radial artery and affect response to vasoconstrictors. Ann Thorac Surg 2007;83:126–32.[Abstract/Free Full Text]

  18. Nisanoglu V, Battaloglu B, Ozgur B, Eroglu T, Erdil N. Topical vasodilators for preventing radial artery spasm during harvesting for coronary revascularization: comparison of 4 agents. Heart Surg Forum 2006;9:E807–12.[Medline]

  19. Mayranpaa M, Simpanen J, Hess MW, Werkkala K, Kovanen PT. Arterial endothelial denudation by intraluminal use of papaverine-NaCl solution in coronary bypass surgery. Eur J Cardiothorac Surg 2004;25:560–6.[Abstract/Free Full Text]





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