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Ann Thorac Surg 2002;73:803-808
© 2002 The Society of Thoracic Surgeons


Original article: cardiovascular

Morbidity after procurement of radial arteries in diabetic patients and the elderly undergoing coronary revascularization

V. Seenu Reddy, MDa, Samir M. Parikh, MDa, Davis C. Drinkwater, Jr, MD*a, Amy Lo, MDa, Thomas P. Rauth, BSa, Rosemary M. Moleskia, Paul A. Chang, BSa

a Department of Cardiac and Thoracic Surgery, Vanderbilt University Medical Center, Nashville, Tennessee, USA

* Address reprint requests to Dr Drinkwater, 2986 The Vanderbilt Clinic, 1301 22nd Ave S, Nashville, TN 37232-5734, USA
e-mail: davis.drinkwater{at}mcmail.vanderbilt.edu

Presented at the Forty-seventh Annual Meeting of the Southern Thoracic Surgical Association, Marco Island, FL, Nov 9–11, 2000.


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Discussion
 References
 
Background. The use of radial arteries for coronary revascularization is increasing. There remain concerns regarding alteration of upper extremity function after radial artery procurement. This study evaluates the functional morbidity in higher risk patients.

Methods. Between April 1997 and September 1999, 374 patients underwent unilateral or bilateral radial artery procurement. A questionnaire was used to evaluate symptoms related to motor and sensory function and changes in appearance after radial artery harvest.

Results. Two hundred eighty-nine patients were successfully interviewed. The average age was 63 years. Median follow-up was 9.5 months (range, 2 to 23 months). No patient suffered limb loss. Altered gross and fine motor function, residual pain, paresthesias, numbness, pallor, swelling, and altered temperature sensation were compared among diabetic patients, patients older than 70 years, and patients without these characteristics.

Conclusions. Radial artery procurement for elective coronary revascularization can be done with minimal serious morbidity in higher risk patients. The most common symptoms were numbness and paresthesia. Despite the finding of greater residual pain in diabetic patients, we do not believe the use of radial artery conduits is contraindicated in these patients.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Discussion
 References
 
The use of radial arteries (RA) as a conduit for coronary artery bypass grafting procedures is increasing since recent reports have described good patency rates and flow characteristics when compared with saphenous veins [1, 2]. The resurgence in the use of RA grafts has also been accompanied by various reports of morbidity associated with the harvesting of RA [3]. Limb ischemia, wound infections, and paresthesias have been reported as occasional complications in patients undergoing RA harvesting [4].

Saphenous vein harvesting has long been associated with a myriad of complications, especially in those patients who are obese or have diabetes [5, 6]. The overall functional morbidity with RA harvesting has not been well described. The purpose of this study was to review the major and minor morbidity rates during the midterm and later-term period after RA harvesting. Furthermore, we compared the rates of morbidity for elderly and diabetic patients, who are traditionally considered at higher risk, with patients lacking these characteristics.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Discussion
 References
 
All patients undergoing elective coronary artery bypass grafting with the use of RA conduits with or without a concomitant cardiac procedure were included in this study. Included were patients who also underwent concomitant saphenous vein or cephalic vein harvesting. Patients undergoing redo coronary artery bypass grafting procedures were included as well. Excluded were patients who underwent emergency coronary artery bypass grafting procedures or patients with low preoperative ejection fraction, deemed to be less than 40% by preoperative imaging. These patients with a low ejection fraction were excluded to create a more uniform pool of patients and to minimize differences caused by variances in tissue perfusion. Patients with a preoperative history of diabetes, whether controlled by oral hypoglycemic agents or insulin administration, were relegated to the diabetic group (DM). Patients older than 70 years at the time of operation were placed in the elderly group (> 70). A subset of patients who were both elderly and diabetic were analyzed separately (Both). The remainder of patients (Non) consisted of younger nondiabetic patients.

Preoperative Duplex and Allen’s test
Patients during this study period underwent either a preoperative duplex ultrasound of both forearms to assess RA and ulnar arterial dominance or codominance. During the course of the study, we evolved our technique to minimize the need for duplex scanning and began to use a modified Allen’s test in the preoperative holding area or on the operating table using pulse oximetry of the middle finger to obtain digital saturations. Patients deemed to have radial dominant flow or with inadequate saturations (< 96% or change of > 4% from baseline) with RA compression were deemed unsuitable candidates for RA harvesting given the increased risk of hand ischemia. Duplex scanning is currently reserved for those patients in whom adequate digital saturations are unobtainable or in whom a more precise delineation of conduit adequacy is required.

Radial artery harvest technique
The details of harvesting the RA have been extensively reported elsewhere [7, 8]. The technique used at our institution favors sharp dissection and minimal use of the electrocautery, especially in the region of the radial nerve. Gentle handling of the conduit and the surrounding tissues is emphasized. We also avoid skeletonization of the artery and generally harvest it with approximately 1 cm or more of associated fascia and muscle tissue. Branches are identified and ligated with silk ligature. The wound is closed in layers, and the skin is reapproximated with subcuticular absorbable suture. The harvest site is usually closed without a drain and is wrapped in a compressive dressing that is removed on postoperative day 2. The patient is given specific instructions regarding wound care and extremity elevation. Several patients underwent cephalic vein procurement in addition to RA extraction. Although these patients were included in the study, no subset analysis of outcomes for this group was conducted because of the small number.

Follow-up questionnaire
A multipart follow-up questionnaire was designed and modeled after similar questionnaires used for follow-up studies (Fig 1). The questionnaire recorded a patient’s response in a bimodal fashion to simplify data collection and analysis. Most questions consisted of yes or no answers. This questionnaire was developed at our institution and is therefore a nonvalidated questionnaire. The broad areas queried included hand and arm function, appearance, and sensation. Specifically, a patient’s hand and arm preference preoperatively and postoperatively for gross motor tasks was assessed. Activities such as writing, using scissors, eating, and lifting were used as examples to elucidate whether the patient had to changed handedness as a result of the RA harvesting. No formal neurovascular testing was conducted as a part of this follow-up.



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Fig 1. Questionnaire for radial artery harvesting follow-up.

 
Regarding function, patients were asked whether they had noted any loss of arm or hand function or whether there was a change in perceived strength in the arm or hand. Fine motor function was queried in term of fine movement tasks such as handling coins or writing. Patients were also asked about the appearance of the limb from which the RA had been harvested. Specifically, patients were asked about any residual extremity edema and the presence of hand pallor.

Follow-up clinic visits and phone interviews
Patients all had routine postoperative follow-up in the cardiothoracic surgical clinic. These patients were examined in the clinic by the senior author in the study. All patients who had undergone RA harvesting were called at some point during the intermediate and late postoperative period. Trained personnel in the cardiac surgery department and the authors conducted the telephone interviews. Patients were contacted during the dates of the study period, and the time of follow-up varied from patient to patient. The responses generated were for that particular patient at the time of interview. We did not depend on patients’ recollections of prior time periods. There was no formal repeat interview conducted as a component of this study. The standardized questionnaire was used to record responses. Patients who had wound infections or other acute problems with their harvest site were not excluded from later-term follow-up. The proportion of patients successfully contacted represents the proportion that met the criteria of intermediate and late intervals from the time of operation to the time of follow-up.

Statistical methods
The {chi}2 test was used to identify significant differences between proportions. A p value of less than 0.05 was deemed to be statistically significant. SPSS 8.0 for Win95/NT (SPSS, Chicago, IL) and MS Excel for Windows (Microsoft Corp, Redmond, WA) were used for data analysis and the {chi}2 test.


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Discussion
 References
 
Between April 1, 1997, and September 30, 1999, 374 consecutive patients underwent either primary or redo coronary artery revascularizations with procurement of the RA for use as a conduit. Of these, 289 (77%) patients were successfully interviewed either on the telephone or in person regarding their RA harvest site. During the study period, the RA was used in greater than 70% of patients; this percentage has increased at our institution. There were 210 men and 79 women in the interview group. The overall average age was 63 years (range, 36 to 90 years). There were 58 (20%) patients who had either insulin-dependent or non-insulin-dependent diabetes (DM group) documented in their preoperative assessment. These patients were also all younger than 70 years of age. There were 73 patients (25%) older than 70 years of age classified as elderly but nondiabetic (> 70 group). The average age of this subgroup was 74 years. An additional 20 patients (7%) had both characteristics (Both) of being elderly and diabetic. The remaining 138 (48%) patients comprise the Non group of patients who were neither elderly nor diabetic, with an average age of 58 years. All comparisons looked for statistically significant differences among the DM, greater than 70, or Both groups when compared with the Non group.

Table 1 summarizes the findings. In terms of gross motor function, 14% of the DM group, 11% of the greater than 70 group, 5% of the Both group, and 14% of the Non group reported some alteration in the postoperative period. There was a statistically significant difference between the Both and Non groups. Fine motor function similarly saw a difference only between the Non and Both groups although the elderly diabetic group actually had fewer complaints of gross and fine motor function. Paresthesia rates were no different for the DM, greater than 70, or Non groups but was significantly higher for the Both group with nearly 50% of these patients complaining of some degree of paresthesia, usually in the region of the radial nerve distribution. Numbness in the area of the forearm incision was also a common complaint but was only statistically higher for the comparison between the Both and Non groups. Fourteen (70%) patients of the Both group reported some residual numbness over the incision during the follow-up period. Pallor and altered temperature sensation were less frequently reported by patients, and there was no significant difference in these characteristics among the groups. Postoperative swelling by patient response was statistically higher for the Both group when compared with the Non group.


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Table 1. Percentage of Respondents in Each Group Reporting Positive Findings

 
When patients were asked for differences in arm or hand appearance in terms of perceived pallor, there was no difference among any of the groups. Of note, no report of hand pallor was associated with true hand ischemia or symptomatic vascular insufficiency. Residual pain, typically in the forearm or the region of the incision, was reported at higher rates in the DM group and in the Both group and was statistically higher when compared with the Non group.


    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Discussion
 References
 
There are numerous reports in the literature describing the complications resulting from RA harvesting for use as a bypass conduit [3, 9, 10]. Other groups have reported morbidity such as altered temperature sensation, change in hand strength, and paresthesias after RA harvesting as a part of forearm free flaps [11]. Despite these occasional complications, there has been a resurgence and a growth in the use of RA as a conduit for coronary revascularization since the first report in 1973 by Carpentier and colleagues [12] and the subsequent study by Acar and associates [13]. The concept and application of total arterial grafting as a revascularization strategy has also added to the increased use of RA. Finally, the morbidity associated with saphenous vein harvesting has been well documented and is frequently the only source of morbidity associated with any given patient’s postoperative course [5, 6].

This questionnaire-based study attempts to better define the morbidity associated with RA harvesting as reported by patients in the midterm and late postoperative period. Many of the calculated rates of morbidities are higher than those cited in previously published work [14, 15]. These findings are likely owing to several factors. Other authors have based morbidity calculation rates on formal neurovascular testing or have used stringent definitions of morbidity. We chose to include broad categories of morbidity, relied on patient’s perceptions of alterations from their preoperative status, and included both sensory as well as functional changes as categories of morbidity.

Regarding the specific findings of this study, it is interesting to note that there was no statistical difference in either gross or fine motor function among the DM, greater than 70, and Non groups. There was a statistical difference between the Both group and the Non group, but fewer elderly diabetic patients complained of alterations in motor function. This may be related to the small sample size of patients comprising the elderly diabetic group or the greater perception of changes in motor function in the younger nondiabetic patient whose average age was only 58 years.

In terms of paresthesias and numbness, there was again no difference among patients who were either elderly or diabetic when compared with their younger, nondiabetic cohort. Paresthesias and numbness in the region of the incision were, however, among the most frequently cited complaints by patients. Paresthesias were almost exclusively relegated to the region of the anatomic "snuff box" and areas of the extremity supplied by the radial nerve. Unlike the report by Arons and colleagues [3], none of our patients experienced permanent or debilitating dysesthesias. In general, the paresthesias in the region of the cutaneous radial nerve distribution tended to improve with time, but further time course study would be needed to document significant interval changes. Inasmuch as our follow-ups were not conducted in a repetitive manner at specific postoperative intervals (eg, 3, 6, 9 months), a time-related analysis is not feasible. We also note that there is a learning curve associated with the extraction of the RA and that standardization of technique with adherence to gentle tissue handling, minimization of electrocautery, and avoidance of skeletonization of the vessel can greatly affect overall results [16]. The modified Allen’s test using pulse oximetry appears to be an adequate preoperative assessment in almost every case. Although using the nondominant arm as the initial procurement site is recommended, with an all-arterial revascularization strategy the removal of both RA was required and well tolerated.

Numbness was a common complaint among all of the study groups and was reported at a particularly high rate by the elderly diabetic patient. Numbness occurred almost exclusively over the incision site and was included as a category in this study because it is a common concern among patients. Furthermore, numbness over an upper extremity scar may be more noticed than numbness over similar incisions over the sternum, abdomen, or lower extremity and therefore lead to higher rate of complaints by patients. Slower nerve regeneration, healing, and underlying neuropathy may explain the significantly higher rates of paresthesias and numbness reported by the elderly diabetic patient group.

With respect to changes in appearance such as postoperative swelling and hand pallor, there were no differences among the groups except with regard to swelling. The elderly diabetic patient group had higher rates of continued postoperative extremity edema when compared with the younger nondiabetic group. Our data did not allow time course analysis that might elucidate whether this improves with time. The higher rates of swelling in the elderly diabetic group may be caused by slower tissue healing or possible alterations in lymph drainage. Typically, most reported swelling improved with extremity elevation and did not interfere in the other categories such as motor function. Pallor of the extremity, or more commonly the hand, was reported by 14% to 20% of patients. There was no significant difference among groups, and none of these patients had pallor that was indicative of limb claudication, limb ischemia, or clinical vascular insufficiency. Of note, the patients in this study all underwent preoperative vascular duplex scanning to evaluate the patency and dominance or codominance of the ulnar artery. Thus, residual pallor may be a transient finding while the ulnar artery and the distributive palmar branches compensate for absent radial flow.

The presence of residual pain was the primary significant positive finding in this study. Both the DM and the Both groups had significantly higher rates of residual pain when compared with the Non group during the follow-up period. Typically, patients reported residual pain in the forearm and in the region overlying the incision. The pain was not characteristic of claudication. Furthermore, patients did not report limitations in their activity or extremity use because of the presence of residual pain. The gross and fine motor function responses reveal that these were unaffected by the presence of residual pain in these same groups. Diabetic neuropathy may play a role in the higher rates of residual pain reported by these patient subsets.

In summary, there is renewed interest in the use of RA conduits for coronary revascularization, and we anticipate that the choice of this conduit will continue to increase as total arterial revascularization gains popularity. Accompanied with this increased use is the potential for increased complications in the process of RA procurement. Meticulous attention to harvesting technique and standardization of the harvesting procedure should minimize these events. Newer techniques for removal of the RA such as endoscopic procurement and the use of cautery alternatives may further alter the rates or severity of postoperative complications [17, 18]. Furthermore, recognition of preoperative patient characteristics will allow for better counseling of patients with regard to what to expect in the postoperative period. The rates of saphenous vein harvesting complications have been widely reported, and most of us recognize that some of the most frequent complaints in the postoperative setting are related to saphenous vein harvesting.

This study shows that although patient-reported rates of morbidity may be significant, that with respect to serious morbidity RA harvesting continues to be performed safely and is well tolerated. Moreover, there is no significant difference in the rates of morbidity among patients traditionally thought to be at higher risk for complications, such as the elderly or the diabetic patient. Of note, the combination of risk factors may contribute to higher rates of numbness, paresthesias, and residual pain, but these complaints may decrease over time. Furthermore, the presence of these complaints does not preclude the use of the RA as a conduit given that the majority of patients tolerate removal of the RA with the absence of serious complications. We believe that the continued use of RA conduits in both the elderly patient as well as the diabetic patient is warranted.


    Discussion
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Discussion
 References
 
DR ALAA Y. AFIFI (Albany, NY): I really enjoyed your presentation very much. It really is one of a few large series of patients that closely evaluated morbidity in the goal for complete arterial revascularization. I have a few questions.

In relation to the morbidity, especially paresthesias, the incidence that you demonstrated, more than 50%, seems like it is a much higher incidence than what we have seen in the literature. Typically 10% to 15% is what has been quoted in the past. This leads to the next question in terms of the specific technique of harvesting. One, are surgeons or physician assistants harvesting your radial artery for you? Two, what mode of visualization is used, typically loupes or nonloupes, to try to obviously spare the superficial radial and lateral antebrachial cutaneous nerves?

The next issue becomes the question of potential hematomas that develop. You have not identified any significant problems in terms of hematomas postoperatively, but that is something else of concern.

And the final point: we have seen in reports by many authors, in in vitro studies performed with nitrates being an ideal antispastic drug, and looking at the outstanding results of Hendrick Barner, MD, a recent article by Thoralf Sundt, MD, in the Annals of Thoracic Surgery has demonstrated no need for utilization of antispastic drugs and their use of the harmonic scalpel to minimize complications as opposed to a Bovie electrocautery.

If you could make some comments based on these questions. Thank you very much. Nice paper.

DR REDDY: Thank you for raising those very interesting points. With regard to your first question in terms of our rates of paresthesias and some of these rates of morbidity when compared with reports in the literature, I think this can be explained at least in part by the fact that this was a survey method, and I think patients are quite prone to report even minor changes in their preoperative status. In terms of the reports in the literature, many of them have brought patients back for formal neuromotor testing, and that of course we did not do here, and I think that certainly accounts for some of the difference that we are seeing.

In terms of the technique, you asked about who does the harvesting. At our institution we have physician assistants doing it as well as senior residents. I think the residents would wear loupes with the physician assistants rarely with the loupes.

In terms of the technique, I reviewed it a little bit. There is a learning curve with the harvesting of the radial artery, and we see, with this learning curve, certainly improvements in morbidity.

In terms of the storage of the conduit itself and the management of the conduit with systemic administration of vasodilators, at our institution we currently do store the conduit in a composition of blood and nitroglycerin. We are administering systemic vasodilators, specifically calcium-channel blockers; however, this question I think still has not been answered. In fact, in our basic science laboratories we have undertaken some ring studies to take pieces of radial artery ring, trying to elucidate better whether there is a difference in the spasticity of these vessels or in fact are there differences in the endothelial expression of inflammatory molecules in response to the various storage techniques.

DR THORALF SUNDT (St. Louis, MO): Is it my understanding you did not use the harmonic scalpel for harvesting the radial artery in this series, is that correct?

DR REDDY: That is correct, we did not use the harmonic scalpel.

DR SUNDT: Have you moved that direction at all and I wonder whether there is any difference in the morbidity in those two groups. We have moved entirely to using the harmonic scalpel in St. Louis.

DR REDDY: Certainly that, and the presentation last night talked about the use of harmonic scalpels. We have not at our institution done a cross comparison between the two techniques but I think that would certainly be interesting.

Afifi also asked about wound complications. This specific study did not look at wound complication rates and hematomas. Certainly these occur in a small percentage of patients and are typically managed in an outpatient setting.

DR MICHAEL C. MAXWELL (Charlotte, NC): My question is about the effect of the sternotomy and the sternal retraction on paresthesias in the hand. I wonder whether there is a component of brachial plexus stretch from the sternotomy and have you ever heard of anyone controlling for that and looking at patients who did not have radial arteries but did have a sternotomy?

DR REDDY: We did not look at that specific issue. Again, in the patients who did report paresthesias and were evaluated in the clinic, typically the paresthesia was in the snuff box region or in the region of the radial nerve distribution as opposed to a brachial plexus distribution.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Discussion
 References
 

  1. Acar C., Ramsheyi A., Pagny, et al. The radial artery for coronary artery bypass grafting clinical and angiographic results at five years. J Thorac Cardiovasc Surg 1998;116:981-989.[Abstract/Free Full Text]
  2. Possati G., Gaudino M., Alessandrini F., et al. Midterm clinical and angiographic results of radial artery grafts used for myocardial revascularization. J Thorac Cardiovasc Surg 1998;116:1015-1021.[Abstract/Free Full Text]
  3. Arons J.A., Collins N., Arons M.S. Permanent nerve injury in the forearm following radial artery harvesting: a report of two cases. Ann Plast Surg 1999;43:299-301.[Medline]
  4. Trick W., Scheckler W.E., Tokars J.I., et al. Risk factors for radial artery harvest site infection following coronary artery bypass grafting surgery. Clin Inf Dis 2000;30:270-275.[Abstract/Free Full Text]
  5. Slaughter M.S., Olson M.M., Lee J.T., Jr, Ward H.B. A fifteen-year wound surveillance study after coronary artery bypass. Ann Thorac Surg 1993;56:1063-1068.[Abstract/Free Full Text]
  6. Wong S.W., Fernando D., Grant P. Leg wound infections associated with coronary revascularization. Aust NZ J Surg 1997;67:689-691.[Medline]
  7. Tatolis J., Buxton B.F., Fuller J.A., Royse A.G. The radial artery as a graft for coronary revascularization: techniques and follow-up. Adv Card Surg 1999;11:99-128.[Medline]
  8. Levine A.J., Graham T.R. Techniques in conduit harvesting. Hosp Med 1999;60:178-182.[Medline]
  9. Manasse E., Sperti G., Suma H., et al. Use of radial artery for myocardial revascularization. Ann Thorac Surg 1996;62:1076-1083.[Abstract/Free Full Text]
  10. Pola P., Serricchio M., Flore R., Manasse E., Favuzzi A., Possati G.F. Safe removal of the radial artery for myocardial revascularization: a Doppler study to prevent ischemic complications of the hand. J Thorac Cardiovasc Surg 1996;112:737-744.[Abstract/Free Full Text]
  11. Timmons M.J., Missotten F.E.M., Poole M.D., Davies D.M. Complications of radial forearm flap donor sites. Br J Plast Surg 1986;39:176-178.[Medline]
  12. Carpentier A., Guermonprez J., 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;16:111-121.[Abstract/Free Full Text]
  13. Acar C., Jebara V., Portoghese M., et al. Revival of the radial artery for coronary artery bypass grafting. Ann Thorac Surg 1992;54:652-659.[Abstract/Free Full Text]
  14. Grossbner M., Arifi A., Bourov G., Taylor G., Gray S., Ritchie A. No change in O2 saturation but measurable difference in thenar flexor power after radial artery harvest. Eur J Cardiothorac Surg 1999;16:160-162.[Abstract/Free Full Text]
  15. Serricchio M., Gaudino M., Tondi P., et al. Hemodynamic and functional consequences of radial artery removal for coronary artery bypass grafting. Am J Cardiol 1999;84:1353-1356.[Medline]
  16. Levine A.J., Graham T.R. Techniques in conduit harvesting. Hosp Med 1999;60:178-182.
  17. Genovesi M.H., Torillo L., Fonger J., Patel N., McCabe J.C., Subramanian V.A. Endoscopic radial artery harvest: a new approach. Heart Surg Forum 2001;4:223-225.[Medline]
  18. Wright C.B., Barner H.B., Gao A., et al. The advantages of the harmonic scalpel for the harvesting of radial arteries for coronary artery bypass. Heart Surg Forum 2001;4:226-230.[Medline]



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