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Ann Thorac Surg 2001;71:148-151
© 2001 The Society of Thoracic Surgeons


Original article: cardiovascular

The impact of chronic renal failure on atherosclerosis of the internal thoracic arteries

Masashi Ura, MDa, Ryuzo Sakata, MDa, Yoshihiro Nakayama, MDa, Yoshio Arai, MDa, Mitsuhiko Kitaoka, MDb, Hiroyoshi Fukui, MDc

a Department of Cardiovascular Surgery, Kumamoto Central Hospital, Kumamoto City, Japan
b Department of Pathology, Kumamoto Central Hospital, Kumamoto City, Japan
c Department of Nephrology, Kumamoto Central Hospital, Kumamoto City, Japan

Accepted for publication May 2, 2000.

Address reprint requests to Dr Ura, Department of Cardiothoracic Surgery, St. George Hospital, Gray St, Kogarah NSW 2217, Australia
e-mail: masashiura{at}hotmail.com


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. Little is known about the impact of renal failure on atherosclerotic changes in the internal thoracic artery (ITA).

Methods. A total of 20 consecutive patients on chronic dialysis who underwent coronary artery bypass grafting (CABG) during April 1998 through September 1999 were investigated. The 20 control patients were selected from the same interval to rigorously match risk factors. Atherosclerosis of the ITA collected from each patient was analyzed using the subjective evaluation proposed by Kay and colleagues.

Results. There were no cases of greater than 25% atherosclerotic luminal narrowing among a total of 35 ITA specimens from dialysis patients. The degree of atherosclerosis was not significantly different from that of the specimens from matched patients (p = 0.18). No calcification was found in ITA grafts either microscopically or macroscopically. The number of elastic lamellae, an index of the elasticity of the ITA graft, was not significantly different from those obtained from the matched patients. Analysis of preoperative coronary angiography revealed that coronary calcification was significantly more frequent in dialysis patients (15 patients, 75%) than in matched patients (p < 0.05). By analysis of postoperative angiography in dialysis patients, no evidence of atherosclerotic changes was found in 28 opacified ITAs. In addition, despite the presence of calcification in the native coronary, no calcification was evident along the entire length of the ITAs.

Conclusions. This study revealed the minimal impact of chronic renal failure on atherosclerotic changes in the ITA. The results of this study support the continued use of ITA grafting in dialysis patients.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Coronary artery bypass grafting (CABG) in long-term renal dialysis patients presents a surgical challenge because of patients’ susceptibility to infection, accelerated atherosclerosis and calcification involving the coronary arteries and other systemic vessels, and these conditions’ associated comorbidity [13]. Dialysis patients also commonly have poor quality saphenous veins. With the expectation of improvement of early and late results by using disease-free conduits for revascularization, we have extensively used arterial grafts, including the bilateral internal thoracic artery (ITA) and gastroepiploic artery, in renal dialysis patients [3]. Numerous studies have revealed the high resistance of the ITA to atherosclerotic changes [49]. Kay and colleagues [4] reported that significant atherosclerotic narrowing was seen in 9 patients (4.2%) among 215 ITA segments studied and that the degree of incipient atherosclerosis correlated positively with age, hypertension, diabetes mellitus, and peripheral vascular disease. Numerous follow-up angiographic studies have also demonstrated the excellent performance of the ITA over the long term [5, 6]. The aim of this study was to clarify the impact of the presence of renal failure on atherosclerotic changes in the ITA.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
A total of 20 consecutive patients on chronic dialysis who underwent CABG during April 1998 and September 1999 were investigated.

The patients consisted of 18 men and 2 women with a mean age of 66.4 ± 5.9 years (range 54 to 78 years). Patient characteristics and operative procedures are summarized in Table 1. Preoperatively, 18 patients were maintained on hemodialysis and 2 were on continuous ambulatory peritoneal dialysis. The mean duration of dialysis was 6.7 ± 2.0 years. The 20 control patients were selected during the same interval to rigorously match for risk factors such as hypertension, diabetes mellitus, hyperlipidemia, extent of coronary artery disease, age, gender, and arteriosclerosis obliterans (Table 1).


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Table 1. Preoperative Characteristics of Patients

 
Pathologic studies
The remnants of the distal segments of ITA collected from each patient were fixed in formalin, embedded in paraffin blocks, and sectioned every 5 mm. Sections were stained with hematoxylin and eosin and elastica Van Gieson. Atherosclerosis of the ITA was analyzed using the subjective evaluation proposed by Kay and colleagues [4], comprising a scale of 0 to 4 (0 = normal, 1 = minimal disease, 2 = < 25% luminal narrowing, 3 = 25% to 50% luminal narrowing, and 4 = > 50% luminal narrowing). A greater than 25% luminal narrowing was regarded as significant atherosclerosis. The maximum scale of atherosclerosis among the sectioned segments in each individual was compared between the dialysis patients and the matched patients.

Because the number of elastic lamellae indicates the elasticity of the ITA graft [10], the number of elastic lamellae in the media of both ITAs was counted and recorded by an independent pathologist (M.K.). The segments 2 cm proximal to the bifurcation (left ITA) and precisely at the bifurcation (right and left ITAs) were used as reference points, allowing a comparison to be made between the dialysis patients and the matched patients.

Postoperative angiography
Early postoperative angiography was performed 2 to 3 weeks after surgery. All grafts were evaluated for occlusion, development of string signs, or presence of stenosis (flow limiting or stenosis of > 25% of the vessel diameter at any point along the body of the graft or at any anastomosis).

Statistical methods
Univariate testing of variables was performed using Fisher’s exact test on discrete variable comparisons. The Mann-Whitney U test was used for continuous variable comparisons. Only p values of less than 0.05 were considered significant. All analyses were performed using SAS version 6.12 statistical package (SAS Institute, Cary, NC).


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Pathologic studies
A total of 35 ITA specimens were collected from 20 patients. Of these, there were two specimens with degree 0 atherosclerosis, 30 with degree 1 atherosclerosis, and three with degree 2 atherosclerosis. There were no cases of degree 3 or 4 atherosclerosis. The degree of atherosclerosis was not significantly different from that in the specimens of 20 matched patients (p = 0.18). Also there was no significant difference of degree of atherosclerosis between right and left ITAs. No calcification was found in ITA grafts either microscopically or macroscopically (Table 2).


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Table 2. Pathologic Study of ITAs

 
The number of elastic lamellae, an index of the elasticity of the ITA graft, was 3.18 ± 1.33 in the segment 2 cm proximal to the bifurcation (left ITA) and was 2.29 ± 1.16 and 2.0 ± 1.3 in the segment containing the bifurcation (left and right ITA, respectively). These results were not significantly different from those obtained from the matched patients (p > 0.2).

Angiographic studies
Analysis of preoperative coronary angiography revealed that coronary calcification was significantly more frequent in dialysis patients (15 patients, 75%) than in matched patients (p < 0.05). In 9 dialysis patients (45%), calcification involved more than one coronary artery.

Postoperative selective angiography of ITAs was performed in 15 of 20 dialysis patients (75%). In 28 opacified ITAs, no evidence of atherosclerotic changes was found. Despite the presence of calcification in the native coronary, no calcification was evident along the entire length of the ITAs in dialysis patients. All grafts except one were completely patent except for one right ITA anastomosed to the circumflex artery through the transverse sinus, which showed 90% stenosis due to technical failure.


    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Calcification of the coronary arteries and the ascending aorta and poor quality saphenous veins are serious problems in long-term dialysis patients [3]. We have advocated the use of multiple arterial grafting to forestall these characteristic problems.

Numerous studies have revealed the high resistance of the ITA to atherosclerotic changes [49]. Kay and colleagues [4] reported significant atherosclerotic narrowing in 9 patients (4.2%) after an investigation of 215 ITA segments. The degree of incipient atherosclerosis correlated positively with age, hypertension, diabetes mellitus, and peripheral vascular disease [4]. Numerous follow-up angiographic studies have also demonstrated the excellent performance of the ITA over the long term [5, 6]. Information is still lacking on the influence of renal failure on atherosclerotic changes in the ITA. In our study, no severe atherosclerosis was found in the specimens obtained from renal patients undergoing CABG. Despite extensive calcification of the native coronary artery, no microscopic calcification was found in the ITA grafts. In addition, the elasticity of ITA conduits, as evaluated by the number of the elastic lamellae in the media, was not significantly different between renal dialysis patients and matched patients. These results suggest that the elasticity of ITA conduits was well preserved despite patient history of long-term dialysis. The study demonstrated the high resistance of the ITA to atherosclerotic changes, even in dialysis patients.

Sons and colleagues [7] conducted bilateral semiselective internal thoracic arteriography in 116 patients. They noted evidence of atherosclerotic change in 6.6% (15/227) of the opacified vessels in 11.1% (13/117) of the individuals investigated. Although all patients with atherosclerotic lesions in the ITA had coronary artery disease, no correlation could be found between coronary artery disease and internal thoracic atherosclerosis. However, peripheral vascular disease and hyperlipidemia were identified as predictors of atherosclerotic changes in the ITA.

Because we obtained our pathologic specimens from patients undergoing CABG, it was impossible to investigate the entire ITA grafts microscopically. However, Shelton and colleagues [5] reported a good correlation between the degree of narrowing, as estimated by angiographic and histologic measurements in both internal mammary artery grafts (d = 0.90), and that in saphenous vein grafts (d = 0.71). Thus we arteriographically evaluated the ITA grafts postoperatively. Selective arteriography revealed no significant or insignificant atherosclerotic changes in the ITA grafts in the renal dialysis patients studied. Although no definite conclusions can be obtained without long-term angiographic studies, most of the renal patients already had a long-term history of dialysis at the time of angiography, so excellent long-term patency of ITA grafts can be expected even in dialysis patients.

Although dialysis patients often show complications (specifically, calcification of the coronary arteries, aorta, and other peripheral arteries), our angiographic and histologic study revealed no sign of calcification in the ITA grafts. In dialysis patients with severe atherosclerosis and calcification precluding aortic cross clamping, coronary artery bypass grafting using in situ arterial grafts under ventricular fibrillation or on the beating heart would be the procedure of choice. However, considering the high frequency of coronary calcification in dialysis patients, the more secure anastomosis obtainable under ventricular fibrillation may be more appropriate in such situations. In fact, CABG under ventricular fibrillation was successfully performed in 4 patients in this series.

There may be some concern, however, about using the ITA in dialysis patients, whose immune systems and blood clotting systems are compromised and who often have associated comorbidity. Blakeman and colleagues [2] reported the results of internal mammary artery revascularization in patients on long-term renal dialysis. However, no wound healing problems occurred in either the 16 patients with saphenous vein grafts or the 10 patients with ITA grafts in combination with saphenous vein grafts. They concluded that the use of the internal mammary artery in patients on long-term renal dialysis does not adversely affect wound healing or increase blood loss in this subset of patients.

In our series, no wound healing problems occurred in either the 18 patients who underwent BITA grafting or the 2 patients who underwent single ITA grafting. Although our technique of harvesting ITA is the standard pedicled graft and not unique in any way, wound healing problems may be avoided by using an experienced surgical team that is able to avoid any electrocautery injury to the periost or cartilage.

In conclusion, this study revealed the minimal impact of chronic renal failure on atherosclerotic changes in the ITA. Despite the presence of calcification in the native coronary arteries and aorta that is characteristic of long-term dialysis patients, no calcification was found in the ITA grafts. The results of this study support the continued use of ITA grafting in dialysis patients, especially in individuals with calcified aorta and poor-quality saphenous veins.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Ko W., Kreiger K.H., Isom O.W. Cardiopulmonary bypass procedures in dialysis patients. Ann Thorac Surg 1993;55:677-684.[Abstract]
  2. Blakeman B.P., Sullivan H.J., Foy B.K., Sobotka P.A., Pifarré R. Internal mammary artery revascularization in the patient on long-term renal dialysis. Ann Thorac Surg 1990;50:776-778.[Abstract]
  3. Nakayama Y., Sakata R., Ura M., Miyamoto T. Coronary artery bypass grafting in dialysis patients. Ann Thorac Surg 1999;68:1257-1263.[Abstract/Free Full Text]
  4. Kay H.R., Korns M.E., Flemma R.J., Tector A.J., Lepley D., Jr Atherosclerosis of the internal mammary artery. Ann Thorac Surg 1976;21:504-507.[Abstract]
  5. Shelton M.E., Forman M.B., Virmani R., Bajaj A., Stoney W.S., Atkinson J.B. A comparison of morphologic and angiographic findings in long-term internal mammary artery and saphenous vein bypass grafts. J Am Coll Cardiol 1988;11:297-307.[Abstract]
  6. Loop F.D., Lytle B.W., Cosgrove D.M., et al. Influence of the internal-mammary-artery graft on 10-year survival and other cardiac events. N Engl J Med 1986;314:1-6.[Abstract]
  7. Sons H.J., Godehardt E., Kunert J., Losse B., Bircks W. Internal thoracic artery: prevalence of atherosclerotic changes. J Thorac Cardiovasc Surg 1993;106:1192-1195.[Abstract]
  8. Frazier B.L., Flemma R.J., Tector A.J., Korns M.E. Atherosclerosis involving the internal mammary artery. Ann Thorac Surg 1974;18:305-307.[Medline]
  9. Sisto T., Isola J. Incidence of atherosclerosis in the internal mammary artery. Ann Thorac Surg 1989;47:884-886.[Abstract]
  10. van Son J.A., Smedts F. Bifurcated ("Y") internal thoracic-coronary artery grafts. J Thorac Cardiovasc Surg 1993;106:945-946.[Medline]



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This Article
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