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Ann Thorac Surg 2004;78:1614-1621
© 2004 The Society of Thoracic Surgeons

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Original article: cardiovascular

Histopathology and Morphometry of Radial Artery Conduits: Basic Study and Clinical Application

^a Departments of Cardiothoracic and Vascular Surgery, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
^b Department of Cardiology, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
^c Department of Pathology, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
^d Department of Biostatistics, Cardiothoracic Centre, All India Institute of Medical Sciences, New Delhi, India

Accepted for publication March 8, 2004.

^* Address reprint requests to Dr Chowdhury, Department of Cardiothoracic and Vascular Surgery, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
ujjwalchow{at}rediffmail.com

	Abstract

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
BACKGROUND: The purpose of this study was to determine the pathohistology, morphometry, and risk factors for the development of intimal hyperplasia, calcification, and arteriosclerosis in the radial artery and to compare the morphometry of the distal and proximal radial arteries.

METHODS: A total of 190 proximal and distal radial artery specimens obtained from patients who underwent myocardial revascularization were exposed to histopathologic and morphometric analysis. The severity of disease was evaluated on the basis of the percentage of luminal narrowing, intimal thickness index, and intima-to-media ratio.

RESULTS: Sixty-two proximal (32.6%) and 22 distal (11.5%) radial artery segments were indicated as histologically normal. Morphometric analysis (Z test) revealed a lesser degree of intimal hyperplasia and luminal narrowing in the proximal segments compared with the distal segments (p < 0.001). The incidence of intimal hyperplasia, medial calcification, and arteriosclerosis in the distal radial arteries was 76.3%, 6.3%, and 5.78%, respectively. Using multivariate logistic regression, we have identified three significant predictors for intimal hyperplasia. Expressed as an odds ratio with a 95% confidence interval, these included (i) age greater than 50 years (1.052; 1.000–1.106, p = 0.052), (ii) smoking (14.073; 5.293–37.414, p = 0.000), and (iii) hypertension (2.777; 1.171–6.583, p = 0.020). Factors associated with an increased likelihood of medial calcification and arteriosclerosis included a history of smoking, diabetes, hypercholesterolemia, peripheral arterial disease, and chronic renal failure (p < 0.05).

CONCLUSIONS: The great majority of radial artery conduits indicate preexisting intimal hyperplasia mostly affecting the distal portion. Therefore in cases of longer diseased segments of radial arteries, the discarded segments should be the distal end. Care should be taken when selecting radial artery as a conduit in myocardial revascularization, particularly in elderly males, diabetics, smokers, hypertensive patients, and in those with associated peripheral vascular disease.

	Introduction

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Excellent long-term results of the internal mammary artery as a graft for coronary artery bypass surgery have encouraged a search for other reliable arterial conduits for total arterial revascularization. Such conduits include the radial artery, gastroepiploic artery, inferior epigastric artery, splenic artery, and subscapular artery [1–6]. Despite resurgence in the popularity of the radial artery as a conduit for coronary artery bypass graft, little is known about the prevalence of preexisting disease in this vessel [4–6]. The purpose of this investigation was to elucidate specific sites of pathohistologic changes of radial artery conduits in relation to risk factors in patients undergoing coronary artery bypass grafting, and to compare the morphometry of the distal and proximal radial arteries.

	Material and Methods

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Patient Characteristics
Institutional review board approval for radial artery harvest was granted in January 1996. Between February 1996 and June 2002, 780 patients who underwent coronary artery bypass grafting at the All India Institute of Medical Sciences (New Delhi, India) indicated radial artery as one of the conduits. Of these, 190 radial artery specimens (both proximal and distal segments left after use) from 160 unselected patients undergoing myocardial revascularization during the last 2 years were exposed to histopathological and morphometric analysis. Age at operation ranged from 28–72 years (mean ± standard deviation [SD] = 54.1 ± 11.36 years). 37.5% of patients were below 50 years of age (Fig 1). There were 120 men (75%) and 40 women (25%). Tables 1–4 summarize the clinical features that were investigated as risk factors in this study population. Patients with hypercholesterolemia exhibited serum cholesterol levels greater than 250 mg/dl and those with chronic renal failure exhibited serum creatinine levels greater than 2.5 mg/dl. None of the patients with chronic renal failure were on preoperative dialysis. As per institutional policy radial arteries are not used as bypass conduits in patients on dialysis.

View larger version (20K): [in this window] [in a new window]   Fig 1. Age distribution of 160 patients undergoing coronary artery bypass grafting (study group).

Histopathological Analysis
The arterial segments were processed and paraffin blocks were created. Sections 4–5 µm thick were cut. Four to eight consecutive sections were analyzed per segment of the artery. The sections were stained with hematoxylin-eosin. Verhoeff–Van Gieson elastin stain was used as necessary. A pathologist blinded to the clinical data examined the slides. In this study three methods were used to evaluate the degree of intimal thickening and arteriosclerosis: (1) percentage of luminal narrowing, (2) intimal thickness index (ITI), and (3) intima-to-media ratio (IMR). The severity of disease was calculated from the most severely diseased section using the following formulas: percentage of luminal narrowing = 100 x intimal area/internal elastic lamina area, ITI = intimal area/medial area, and IMR = width of intima at maximal intimal thickness/width of media at maximal intimal thickness.

Morphometric Evaluation
Morphometric evaluation was accomplished by a computerized image analysis system that was comprised of the following: (1) research light microscope (Model B-50; Olympus Corp, Tokyo, Japan), (2) 12-bit digital camera (Media Cybernetics Corp, Silver Spring, MD), (3) personal computer with 43 GB hard disc drive and 32 MB SD RAM (Model PCXBV-LB; Digital Equipment Corp, Maynard, MA) and (4) image pro-plus analysis software (Media Cybernetics Corp, Silver Spring, MD).

For morphometric analysis, hematoxylin-eosin stained sections were used. The sections were screened and fields were selected. The field indicating the maximum intimal thickening was captured at the magnification of 4x. The intimal thickening and medial thickness were measured using the image pro-plus software and the values were expressed in micrometers. The specimens were then graded as follows (adopted from Kobayashi and colleagues) [8]: grade 0 = intima-to-media ratio less than or equal to 0.25, grade 1 = intima-to-media ratio greater than 0.25 but less than or equal to 0.5, grade 2 = intima-to-media ratio greater than 0.5 but less than or equal to 0.75, grade 3 = intima-to-media ratio greater than 0.75, grade 4 = lumen completely obliterated by thickening or thrombosis or both.

The grade was increased by one if the lesion was diffuse indicating that the intimal thickening included greater than 50% of the cross-sectional circumference. For each specimen the grade was derived from that section with the most advanced disease.

Microscopic Morphology of the Radial Artery: Normal and Diseased
The radial artery is a muscular vessel with a thin intima where the intimal endothelial cells seem flattened and are aligned along the long axis of the artery. The intima is very thin and directly rests on the internal elastic lamina [9]. Vessels were recorded as normal if there was no cellular or stromal tissue between the endothelium and the internal elastic lamina (Fig 2A). Vessels with any fibromyointimal proliferation between the endothelium and internal elastic lamina were recorded as indicating intimal hyperplasia (Fig 2B). An atherosclerotic lesion was defined by the presence of intimal lipid lying free as cholesterol clefts or in aggregates of foamy macrophages. Any atherosclerotic lesion present was categorized according to the histologic classification of arteriosclerosis set forth by the American Heart Association [10]. Atherosclerosis was differentiated from arteriosclerosis which is essentially an age-related degenerative process involving the peripheral arteries characterized by intimal thickening along with medial fibrosis [9, 10]. Intimal thickening is a nonspecific term used to designate variants in normal intimal histology as well as different types of pathologic lesions mentioned above [9, 10]. Medial calcification was recorded if present.

View larger version (77K): [in this window] [in a new window]   Fig 2. Photomicrographs from a representative section of radial artery from the same patient. (A) The proximal end of the harvested conduit. (B) The distal end of the harvested conduit. (Note: The thin intima [black arrows] with flattened intimal endothelial cells is aligning along the long axis of the artery in the proximal segment. The distal end indicates moderate intimal hyperplasia [I] with fibrosis and mild luminal compromise [L] [hematoxylin & eosin stain].)

A multivariate forward stepwise logistic regression model was used to identify independent risk factors of intimal hyperplasia. Selection of independent variables was a forward stepwise method with a critical probability value of 0.15 and 0.10 for variable inclusion and exclusion, respectively. A p value less than 0.05 was considered significant in the final model.

Logistic regression was used to represent medial calcification and arteriosclerosis in the radial artery using the same ten risk factors that were used for the evaluation of intimal hyperplasia through the "Enter" method. There were few events regarding medial calcification and arteriosclerosis in this study population and data analyses did not reveal any variable with statistical significance. Hence the multivariate data for the above parameters are not presented. Two-tailed probability was used for all the statistical tests.

	Results

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Histopathology and Risk Factor Analysis
PROXIMAL SPECIMENS
Sixty-two proximal radial artery segments (32.6%) were indicated as histologically normal (Fig 2A). One-hundred twenty-seven specimens (66.8%) exhibited intimal thickening with mild luminal compromise (< 30%). In 76 patients the intimal thickening was concentric with hyalinization of the media, whereas the remainder exhibited an eccentric thickening involving only part of the intima.

DISTAL SPECIMENS
Twenty-two distal radial artery segments (11.5%) were histologically normal, whereas the remaining specimens revealed intimal thickening with luminal compromise (Fig 2B). Tables 1–4 summarize the OR for potential clinical risk factors regarding intimal hyperplasia, medial calcification, and arteriosclerosis. Analysis of each selected categorical variable is subsequently discussed.

INTIMAL HYPERPLASIA
The overall incidence of intimal hyperplasia with regard to the radial arteries was 76.3%. Assessed using univariate analysis, an age greater than 50 years, male gender, a history of smoking, hypertension, diabetes, hypercholesterolemia, peripheral arterial disease, and chronic renal failure were independent risk factors (p < 0.05). By multivariate logistic regression, accounting for the effects of other factors, we identified only three significant predictors for intimal hyperplasia (Table 2). Expressed as OR with a 95% confidence interval (CI), these included (i) age greater than 50 years (OR 1.052; 95% CI: 1.000–1.106, p = 0.052), (ii) a history of smoking (OR 14.073; 95% CI: 5.293–37.414, p = 0.000), and (iii) hypertension (OR 2.777; 95% CI: 1.171–6.583, p = 0.020) (Tables 1, 2).

MEDIAL CALCIFICATION
Evidence of medial calcification was exhibited by 6.3% of the distal radial artery specimens. The incidence of medial calcification of the distal radial artery segments was higher in smokers, hypertensive patients, diabetics, patients with hypercholesterolemia, patients with peripheral arterial disease, and patients with chronic renal failure (p < 0.05) (Table 3).

One patient in this series exhibited a radial artery harvested but not used as a conduit, as the specimen revealed palpable thickening and extensive calcification. Histopathological examination the distal segment indicated near total occlusion of the lumen by intimal proliferation. Proximal segment indicated focal intimal thickening with myointimal proliferation and there was no luminal compromise (< 5%).

ARTERIOSCLEROSIS
Histologic evidence of arteriosclerosis was exhibited by 5.78% of the radial artery specimens. All the atherosclerotic lesions were of type III (preatheroma) in severity. Arteriosclerosis was only predicted by (i) age greater than 50 years, (ii) a history of smoking, (iii) diabetes, (iv) hypercholesterolemia, (v) peripheral arterial disease, and (vi) chronic renal failure (p < 0.05). Male gender, hypertension, obesity, and positive family history did not exert any influence on the atherosclerotic disease process (Table 4).

MORPHOMETRIC ANALYSIS
Figure 3 depicts the grading of cases based on the intima-to-media ratio. Sixty-two proximal (32.6%) and 22 distal radial artery segments (11.5%) exhibited an intima-to-media ratio of less than or equal to 0.25. Overall 25.7% of the proximal radial artery specimens and 44.2% of the distal radial artery specimens exhibited an intima-to-media ratio greater than 50% (Kobayashi's grade 2 and above) (Table 5, Fig 3).

View larger version (24K): [in this window] [in a new window]   Fig 3. Grading of radial artery specimens on the basis of intima-to-media ratio (n = 190). = proximal; = distal.

	Comment

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Evaluation of Disease Severity and Analyses of Risk Factors for Development of Intimal Hyperplasia, Calcification, and Arteriosclerosis
There is an obvious necessity for a bypass conduit to be relatively disease-free before implantation. Three arterial abnormalities were determined in this study population: intimal hyperplasia, medial calcification, and arteriosclerosis. Three methods were used to evaluate the propensity of in situ radial artery to develop intimal hyperplasia including arteriosclerosis: percentage of luminal narrowing, intimal thickness index, and intima-to-media ratio. Comparative morphometric analyses revealed a significantly smaller percentage of luminal narrowing, intimal thickness index, and intima-to-media ratios in the proximal segments compared with the distal segments [p < 0.001), (Table 5)].

The percentage of luminal narrowing is a measure of the severity of intimal thickening including arteriosclerosis. The area rather than the thickness of the intima is measured to allow accurate evaluation of eccentric or irregular disease. It is presumed to be a useful parameter for comparing intimal thickening in different vascular beds [4, 6, 8–11]. The intimal thickness index and the intima-to-media ratio are alternative methods for comparing intimal disease in different vascular beds [4–6, 8–11], as the intimal thickness index uses the area of intima and media rather than the width.

Several investigators have pointed out that the intima-to-media ratio should be used to compare the severity of arteriosclerosis in the same artery among different patients but should not be used to compare arteriosclerosis in two different arteries [8–11]. This method is likely to be more sensitive for the detection of atherosclerotic changes than the percentage of luminal occlusion because compensatory enlargement of the caliber of coronary arteries may preserve the luminal cross-sectional area in arteriosclerosis [6, 12].

Varying degrees of intimal hyperplasia occurred in 76.3% of distal radial artery specimens in this study population. An age greater than 50 years, a history of smoking, and hypertension were the only risk factors indicated for intimal hyperplasia with regard to multivariate analysis (Table 2). On the basis of a low correlation between the severity of radial artery pathology and other known coronary artery risk factors, it seems that some risk factors do not appreciably affect the development of intimal hyperplasia in the radial artery.

A radial artery that is heavily calcified poses technical difficulties intraoperatively apart from indicating a doubtful long-term patency [2, 3, 13]. Chronic renal failure and diabetes are known to predispose individuals to arterial calcification [2, 3, 9–11, 13]. In the present series medial calcification was present in 26.8% of patients with chronic renal failure (p = 0.00) and in 9.5% of patients with diabetes mellitus (p = 0.01). Medial calcification was only predicted by a history of smoking, hypertension, diabetes, hypercholesterolemia, peripheral arterial disease, and chronic renal failure ([p < 0.05], Table 3). A preoperative roentgenogram of the forearm and Doppler ultrasonography have been advocated to select only disease-free radial arteries and to avoid an unnecessary exploration of the forearm [3, 13].

Arteriosclerosis is essentially a chronic disease of elastic arteries and of large- and medium-sized muscular arteries. Intimal cells and medial smooth muscles interact with the serum constituents to produce fatty and fibrofatty plaques. These plaques tend to accumulate preferentially in the hyperplastic intima causing arteriosclerosis [9, 10]. It is conjectured that different arterial beds may exhibit different risk factors for the development of intimal hyperplasia and arteriosclerosis. In this series the incidence of arteriosclerosis in the radial artery was 5.78%. The prevalence of arteriosclerosis was probably underestimated in our study because only the distal ends were examined and arteriosclerosis is a segmental disease.

Size, Flow, and Spasm of the Radial Artery
The radial artery exhibits many anatomic, surgical, and histologic advantages over other alternative arterial conduits [1–8, 11]. Failure of the radial artery graft is either caused by spasm or intimal hyperplasia [1–8, 11]. Radial artery exhibits a considerably thicker media containing a high density of smooth muscle cells as compared with the internal mammary and right gastroepiploic artery [4–6]. Presence of thicker media makes the anastomoses technically easier, but it also predisposes the artery to spasms and to a greater degree of ischemia especially in the outer layers of media. Van Son and associates reported a considerably greater number of discontinuities as well as a greater presence of smooth muscle cells in the internal elastic lamina of the radial artery as compared with the internal mammary and gastroepiploic artery [5]. These discontinuities in the internal elastic lamina stimulate early and progressive intimal hyperplasia [1–6, 9]. Alarmed by these drawbacks the use of the radial artery has been debated by several investigators [4–6].

Electrocautery injury could also be an important factor with regard to suboptimal results with arterial conduits. Over the years the ultrasonic Harmonic scalpel is emerging as a useful alternative to electrocautery with the advantage of fast, safe, spasm-free harvesting and minimal use of hemoclips for arterial branches [7].

Pathohistology and Patency of the Radial Artery Conduits
The long-term performance of radial artery grafts will determine whether this level of atherosclerotic disease translates to adverse clinical outcomes. A review of the literature indicates that this graft is performing quite well at midterm follow-up [1–3, 6, 7, 14, 15]. Previous reports from this center have documented an angiographic patency rate of 96.8% at a mean interval of 16.2 ± 5.1 months (range, 3–24 months) postoperatively [7]. Acar and colleagues determined 100% patency for radial artery graft (56 out of 56) in the early postoperative period ( < 2 weeks), but the patency decreased to 93.5% (29/31) on repeat angiogram after a mean follow-up of 9.2 months [2]. Coltharp cited a 51% occlusion rate of 61 radial artery grafts studied 7 days to 16.3 years postoperatively [14]. Calafiore and colleagues also reported a 94.1% (16 out of 17) angiographic patency at a mean interval of 0.5 months postoperatively [15]. These results support the finding that early occlusion is attributable to intimal hyperplasia, as the grafts that are patent at 5 years are likely to remain patent. There is general agreement that the incidence of intimal hyperplasia leading to graft occlusion can be substantially reduced by harvesting the radial artery together with its venae comitantes and by avoiding vigorous manual dilatation that was used in the previous series of patients. Instead relying on vasoactive drugs to combat the spasm is a more rational approach [1–7, 9].

Limitations of the Study
Arteriosclerosis is a segmental disease. Therefore the extent of disease in one section of a vessel may not necessarily represent the condition of the entire vessel. Multiple serial sections of the entire length of the artery may be the only way to solve this issue. We have attempted to deal with this limitation in two ways. Firstly we have studied a relatively large number of specimens and secondly we have obtained multiple histologic sections for each specimen. The most severely diseased segment was used for the purpose of grading.

Clinical Implications and Recommendations
Our findings indicate that the majority of radial artery conduits exhibit preexisting disease. An increased incidence of intimal hyperplasia of radial arteries was noted among elderly males, smokers, and hypertensive patients. Care should be taken when selecting radial artery as a conduit in myocardial revascularization, particularly in elderly males, diabetics, smokers, hypertensive patients, and in those with associated peripheral vascular disease.

Morphometric analysis revealed more severe pathologic changes of the distal radial artery segments as compared with the proximal segments. Therefore in cases of long segment diseased radial arteries, the discarded segment should be the distal end. The findings as presented in this study may indicate implications for long-term graft patency.

	Acknowledgments

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We thank Shankar Sharma for secretarial assistance.

	References

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 

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8. Kobayashi H, Kitamura S, Kawachi K, et al. A pathological and biochemical study of arteriosclerosis in the internal thoracic artery, a vessel commonly used as a graft in coronary artery bypass surgery. Surg Today. 1993;23:697–703[Medline]
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