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Interact CardioVasc Thorac Surg 2006;5:433-438. doi:10.1510/icvts.2005.116665
© 2006 European Association of Cardio-Thoracic Surgery
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ESCVS article - Experimental

Neurological damage after radial artery harvesting in coronary surgery: a direct measure{star}

Guillermo Reyesa,*, Alfredo Trabab, Lidia Lópezc, Ángel Pintod, Juan Duartea and José Luis Vallejod

a Department of Cardiovascular Surgery, Hospital Universitario La Princesa, c/Diego de León 62. 28006 Madrid, Spain
b Department of Neuroelectrophysiology, Hospital General Universitario Gregorio Marañón, Madrid, Spain
c Department of Neurology, Hospital General Universitario Gregorio Marañón, Madrid, Spain
d Department of Cardiovascular Surgery, Hospital General Universitario Gregorio Marañón, Madrid, Spain

Received 15 July 2005; received in revised form 18 April 2006; accepted 20 April 2006

{star} Presented at the 53rd International Congress of the European Society for Cardiovascular Surgery, Ljubljana, Slovenia, June 2–5, 2004.

*Corresponding author. Guillermo Reyes Copa, C/Escalinata 19 5° izq, 28013 Madrid, Spain. Tel.: +34 913 202556, 34 915 411254; fax: +34 915 868369.

E-mail address: guillermo_reyes_copa{at}yahoo.es (G. Reyes).


   Abstract
Top
 Abstract
1. Background
 2. Materials and methods
 3. Results
 4. Discussion
 References
 
Background: The incidence of neurological complications in the forearm after radial artery harvesting varies in the literature, ranging from 2% to more than 50%. Also, the areas affected and the type of neurological complications differ a lot. Peripheral nerve injuries may be divided into three types: neuroapraxia (conduction block that recovers within 3 months), axonotmesis (recovers 1 ml/day) and neurotmesis (needs surgery for recovering). We decided to perform a neuroelectrophysiological study, before and after surgery, in peripheral nerves of the forearm to find out the real incidence and the type of lesion after radial artery harvesting. Methods: Fifteen consecutive patients whose RA was going to be harvested were selected. Emergency patients, patients with severe liver or renal dysfunction were excluded. A complete neuroelectrophysiological study was performed in the median, ulnar and radial nerve. The amplitude was measured to check mielina status, whereas with the latency and nerve velocity conduction (NVC) we checked the axonal integrity. An electromyogram was also performed in the forearm muscles. A neurological clinical exploration was also performed. All these tests were performed before surgery and two weeks and two months after surgery. Results: Median nerve: A significant decrease in the amplitude that improved over time was registered. This decrease was observed in the motor and sensitive part of the nerve. No changes were observed regarding latency or NVC. Ulnar nerve: A decrease in the amplitude of the sensitive part of the nerve was observed (11.7–9.2–10.4 µV; P=0.006). No changes were observed regarding latency or NVC. Radial nerve: A statistical trend decrease observed regarding NVC of the sensitive part of the nerve branch was found (50.9 m/s vs. 47.1 m/s vs. 47.2 m/s; P=0.10). The electromyogram found no alterations. Clinically, three patients presented sensitive disorders in the median nerve territory and one of these also complained of sensitive disorders in the radial territory. Another patient referred dysesthesias in the ulnar nerve territory. All patients with the exception of one were asymptomatic two months after surgery. Conclusions: Although only a few patients refer symptoms, most patients suffer changes in the peripheral nerves of the forearm (especially in the sensitive part) after RA harvesting. In our study the median nerve and the sensitive part of the ulnar and radial nerve were affected. These changes were temporary, affecting mainly the axon. All these data suggest neuroapraxia as the main peripheral nerve type lesion. We think that physicians and patients must be aware of this.

Key Words: Coronary artery bypass surgery; Neurologic injury; Arteries


   1. Background
Top
 Abstract
 1. Background
2. Materials and methods
 3. Results
 4. Discussion
 References
 
The radial artery (RA) was first used in 1973 by Carpentier and colleagues [1], but it was not until Acar and others [2] discovered the excellent patency in a number of Carpentier early series, that the RA was of great interest to many surgeons. Since then, many papers have focused on the role of the RA in coronary surgery [3,4]. Several complications after RA harvesting have been described. Hand ischemia after RA harvest is a rare event [3]. Other problems like infections or hematomas usually are reported with a low incidence [5–7]. However, the incidence of neurological alterations in the forearm after RA harvesting is higher. Although some authors report an incidence less than 10%, this incidence is above 50% in many papers [5,7,8]. In the literature, the nerves affected and the types of neurological alteration vary. The median nerve, the superficial branch of the radial nerve and the lateral cutaneous nerve are most of the nerves that seem to be affected after radial artery harvesting in the literature. Different types of sensitive and motor disorders have been described in these nerves [6,9,10]. However, the real cause of these alterations is not well known.

Peripheral nerve lesions can be classified into three types. (1) Neuroapraxia is the more benign lesion. It is a conduction block without anatomical disruption of the nerve and always recovers within three months. (2) Axonotmesis represents a transaction of axons without disruption of epineurum or other supporting tissues. It recovers at a rate of axonal regeneration (1 mm per day). (3) Neurotmesis implies transaction of the entire nerve and must be repaired to allow axonal regeneration [11]. Different components of the nerve can be damaged: the myelin, the axon or both. Peripheral nerve lesions can be tested with a neuroelectrophysiological study. Several aspects can be measured with this study. As a general rule, the amplitude of the nerve represents the axonal condition, and the latency and nerve velocity conduction represent the myelin condition. Muscle conditions can be studied with an electromyogram.

For a better understanding of the neurological alterations in the forearm after RA harvesting, we performed a complete neuroelectrophysiological and neuroclinical study in a group of patients whose RA was going to be used in coronary artery bypass grafting in order to see how the forearm nerves are affected.


   2. Materials and methods
Top
 Abstract
 1. Background
 2. Materials and methods
3. Results
 4. Discussion
 References
 
2.1. Design of the study

A prospective observational study was performed in a tertiary hospital. Starting in January 2002, 15 consecutive patients whose RA was going to be used in CABG surgery were selected. Our policy is to use the RA as a graft in CABG surgery in all patients under 70 years whenever possible. The viability of the RA was tested with the modified Allen test and with the Eco-Doppler Allen test. Exclusion criteria for this study were: emergency patients, patients requiring other than isolated CABG surgery, patients that could not be carried to the neuroelectrophysiological department and patients with previous trauma in the forearm. In order to avoid interference with residual neurological alterations in extremities caused by an earlier stroke, patients with a previous history of cerebrovascular disease were also excluded. Consent was required from every patient. This study was approved by the Ethical Committee of the hospital.

2.2. Neurological study

A complete clinical neurological and neuroelectrophysiological study was performed in every patient before the surgery and twice after surgery (two weeks and two months after surgery).

2.2.1. Clinical neurological study
A clinical neurological study was performed by an expert in clinical neurology. In the three studies the following parameters were measured in the radial, ulnar and median nerve:

A complete neurological study was also performed in the first exploration before surgery in order to exclude any general neurological disorder that could affect the forearm.

2.2.2. Neuroelectrophysiological study
All studies were performed by the same expert in neuroelectrophysiology. The ulnar, radial and median nerves were studied. Motor nerve conduction was performed using cutaneous electrodes to register the compound muscle action potential (CMAP). Subdermic electrodes were employed for the sensitive conduction to register the sensitive action nerve potentials (SENP). Orthodromic conduction was employed in the second and third median nerve fingers and in the fifth ulnar finger, whereas antidromic conduction was employed in the radial nerve. The motor conduction of nerves was analyzed with the nerve velocity conduction (NVC), distal latency and CMAP amplitude. The sensitive component of nerves was measured with the NVC and sensitive nerve potential action (PANS) amplitude. The sensitive part of the median nerve is represented by the second and third finger whereas the motor part is represented by the elbow and carpo CMAP. The sensitive part of the ulnar nerve is represented by the fifth finger and the motor part is represented by the elbow and carpo CMAP. The superficial branch of the radial nerve is the sensitive part of the radial nerve.

An electromyogram was also performed in the following muscles: abductor pollicis brevis, abductor digiti minimi and extensor indicis. To evaluate individual motor units within muscles a needle electrode was used for this purpose. For grounding, a plate electrode was placed on the same extremity.

2.3. Surgical technique

The technique of coronary artery bypass grafting has been described previously elsewhere [12]. The RA was removed from the non-dominant arm. A technique similar to that described by Reyes and colleagues [13] was used, with emphasis on minimal touch and minimal diathermy. The distal end of the RA was clipped allowing it to pulsate against its occluded end. Then the proximal end was cut and the artery examined. Later on, the RA was dilated in situ with an intraluminal ejection of 4 ml of a 1-mM solution of papaverine with a mixture of 50% blood and Ringer's lactate solution. The RA was then stored in a bath of papaverine and saline solution. Hemostasis was checked and the subcutaneous tissues closed with a continuous absorbable suture. The skin was closed with staples and a crepe bandage was applied. The arm was then placed by the side of the torso using a drape. The left internal thoracic artery and the saphenous vein were harvested when needed. Heparin was given after all grafts were harvested and after the arm wound was closed. Left internal mammary artery (IMA) was sutured to the left anterior descending coronary artery. RA was sutured to any other coronary artery as surgeon criteria.

2.4. Statistics

Descriptive statistics were used using the mean, median and standard deviation. Box plot was used to represent the quantitative variables and frequencies and percentages for categoric data. Neurological and neuroelectrophysiological data were measured using the Friedman test. Changes within the groups were considered statistically significant, when the P-value was <0.05. All analyses were done using Statistical Packages SPSS for Windows (11.5).


   3. Results
Top
 Abstract
 1. Background
 2. Materials and methods
 3. Results
4. Discussion
 References
 
3.1. Surgical results

Baseline clinical characteristics of patients are described in Table 1. Mean age was 60.7±9.5 years with a male/female ratio of 2:1. All patients were in sinus rhythm before surgery. Five interventions were performed off-pump. A complete revascularization was achieved in 11 patients (73%). The mean number of grafts performed was 2.9 per patient. Left IMA was sutured in all cases to the left anterior descending coronary artery. RA was sutured to the first diagonal in three cases, to a marginal branch in ten and in four cases to the right coronary artery. Kissing technique was used twice.


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  		Table 1 Baseline clinical characteristics of patients undergoing cardiac surgery and whose radial artery has been used as a graft (n=15)

 
Inotropes were needed in two patients and another two patients were re-explored for bleeding. Three patients suffered postoperative atrial fibrillation.

3.2. Neurological results

Neurological exploration was normal in all patients before surgery. After surgery two patients suffered dysesthesias and one patient hypoesthesisas in the median nerve territory. One of these patients also referred dysesthesias in the radial nerve territory. The two patients that complained of dysesthesias were asymptomatic in the last study.

Considering the ulnar nerve, one patient complained of dysesthesias in the fourth and fifth fingers. The patient was asymptomatic in the last study.

3.3. Neuroelectrophysiological results

Radial nerve: Table 2 shows the measures obtained from the radial nerve. Only a trend to a decrease in the superficial branch NVC was noted after surgery (P=0.10). This decrease recovered two months later.


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  		Table 2 Measures obtained in the radial nerve

 
Median nerve: In Table 3, we can see the measures obtained from the median nerve. One of the patients suffering dysesthesias did not attempt the last study. A decrease in the median nerve amplitude was registered. This was observed in both the motor and the sensitive part of the nerve. These changes recovered in the last study (Fig. 1).


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  		Table 3 Measures obtained in the median nerve

 

Figure 1
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  		Fig. 1. Boxplot showing median nerve amplitude in the second finger before and after surgery (P<0.0001).

 
Ulnar nerve: Table 4 represents the measures of this nerve. A transitory decrease in the sensitive part of the ulnar nerve amplitude can be seen after surgery (Fig. 2).


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  		Table 4 Measures obtained in the ulnar nerve

 

Figure 2
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  		Fig. 2. Boxplot showing ulnar nerve amplitude in the fifth finger before and after surgery (P=0.006).

 
The electromyogram exploration was completely normal before surgery. No alterations were observed after surgery in any muscle. The motor unit activity did not change after surgery in any of three muscles. No signs of muscle deterioration were observed.


   4. Discussion
Top
 Abstract
 1. Background
 2. Materials and methods
 3. Results
 4. Discussion
References
 
We performed a complete neuroelectrophysiological and neuroclinical study in patients whose RA was harvested for coronary surgery. We saw that neurological alterations in the forearm after surgery are quite common. A decrease in median nerve amplitude was detected. This decrease recovered over time. Also, a transitory decrease in the sensitive part of the ulnar nerve amplitude and in the radial nerve NVC was detected. This suggests that neuroapraxia is the type of nerve lesion caused after RA harvesting and that the axon may be the most affected part of the nerve.

The IMA has proved to have an excellent patency rate in a long-term follow up, achieving better results than the saphenous vein graft [14]. Since then the interest in artery grafts is growing. Among these grafts, the radial artery grafts have proved a very good patency rate in a short time follow up [15,16]. It is important to be aware of the local complications that can happen after radial artery harvesting. Ischemic problems are very rare [3] and the local complications such as infections or hematomas are not frequent [5–7]. However, the incidence of local neurological problems in the forearm is much higher.

In our study 4 patients out of 15 (26%) complained of neurological alterations in the forearm after surgery. Three of them suffered sensitive disorders in the median nerve and one in the ulnar nerve. However, the neuroelectrophysiological studies have shown that alterations in the forearm nerves after surgery are much more frequent.

The median nerve is one of the most affected nerves. We have seen a decrease in the median nerve amplitude in both the sensitive and motor part of the nerve. This suggests mainly a transitory alteration of the axons. This is supported by the fact that clinically, in our study and in the literature, most patients recovered over time. The only patient that complained of symptoms two months after surgery did not present a recovery in his median nerve amplitude. This suggests that this patient had axonotmesis as a nerve lesion.

The median nerve is very close to the radial artery near the wrist. At this point local edema or hematoma can cause an extrinsical compression of the nerve, simulating a tunnel carpian syndrome. Alterations in median nerve have been noticed by other authors [10].

Regarding the ulnar nerve a decrease in the sensitive part of the nerve amplitude was noted. This decrease also improved over time, suggesting that neuroapraxia is also the type of nerve lesion produced in the ulnar nerve. Only one patient complained of sensitive disorders in the ulnar nerve territory. This patient was asymptomatic in the third study. The ulnar nerve and radial artery are quite separate in the forearm. It is not very frequent to find patients with alterations in the ulnar territory in the literature. The findings of our study might be due to the position of the arm in theater.

One patient complained of alterations in the forearm in the radial territory. We detected a statistical tendency decrease in the superficial branch nerve velocity conduction (P=0.10). We think that this is due to our small size sample. Sensitive alterations affecting the radial nerve territory are common in the literature and some authors have reported that the superficial branch of the radial nerve is affected after RA harvesting [9,10].

In this study, the electromyogram was normal in every patient. Motor disorders are also reported in the literature [10,17]. Although we did not find any patient complaining of motor alterations, a decrease in the motor part of the median nerve was registered. However, these alterations seem not to be important enough to cause alterations in the muscle itself (electromyogram was normal). All these data suggest that even when some patients may complain of motor disorders, the muscle itself seems to be unaffected. Interestingly enough, a similar study has been published recently by Ikizler et al. [18]. They also performed a nerve conduction study in patients undergoing CABG surgery with RA conduits. They found a modest deceleration in neurological conduction of the forearm nerves. However, these changes did not reach statistical difference. In our study statistical differences were found in several measures. Even if removal of RA does not lead to any major neurological hand complication, it is logical to think that these nerves may be somehow affected. The methods employed for the measuring of nerve conduction may be slightly different thus explaining the differences between our study and the Ikizler paper.

It is not easy to determine the real cause for these alterations. Considering our results, it is very possible that an indirect mechanism, like local edema, nerve manipulation or external compression, may be the main causes. We think that this happens particularly in the distal part of the median nerve where there is little room for the nerve. After these findings, we have decided in our practice to finish the incision 3–4 cm before the wrist in order to avoid these alterations.

In our study every radial artery was harvested following standard techniques [13]. Some authors have reported a lower incidence of neurological alterations following endoscopic radial harvesting [19]. Further neuroelectrophysiological studies will be necessary to confirm this.

Limitations of the study are based on the reduced number of patients included in this study. A neuroelectrophysiological study causes moderate discomfort in patients; therefore, the minimum number of patients is required. Also, a decrease in the superficial branch of the radial nerve NVC would have probably been confirmed with more patients. Some authors have reported, in some patients, alterations in the lateral cutaneous nerve [6,9]. The study of this nerve would have complicated the neuroelectrophysiological study. Also, this nerve is anatomically related to the superficial branch of the radial nerve and it is very likely that both nerves may be affected in the same manner.

In conclusion, peripheral nerves in the forearm suffer alterations and alter radial artery harvest. A transitory decrease in median nerve amplitude is seen affecting both the sensitive and motor part of the nerve. Similar changes were obtained in the sensitive part of the ulnar nerve and in the superficial branch of the radial nerve. Clinical alterations are less common. Patients and physicians must be aware of this.


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   References
Top
 Abstract
 1. Background
 2. Materials and methods
 3. Results
 4. 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; 16:111–121.[Medline]
  2. Acar C, Jebara VA, Portoghese M, Beyssen B, Pagny JY, Grare P, Chachques JC, Fabiani JN, Deloche A, Guermonprez JL. Revival of the radial artery for coronary artery bypass grafting. Ann Thorac Surg 1992; 54:652–659. discussion 659–660.[Abstract]
  3. Parolari A, Rubini P, Alamanni F, Cannata A, Xin W, Gherli T, Polvani GL, Toscano T, Zanobini M, Biglioli P. The radial artery: which place in coronary operation? Ann Thorac Surg 2000; 69:1288–1294.[Abstract/Free Full Text]
  4. Buxton B, Gaer J, Komeda M, Ruengsakulrach P. The road to complete arterial grafting for coronary artery disease. Int J Cardiol 1997; 62:1, S65–S70.
  5. Anyanwu AC, Saeed I, Bustami M, Ilsley C, Yacoub MH, Amrani M. Does routine use of the radial artery increase complexity or morbidity of coronary bypass surgery? Ann Thorac Surg 2001; 71:555–559. discussion 559–560.[Abstract/Free Full Text]
  6. Meharwal ZS, Trehan N. Functional status of the hand after radial artery harvesting: results in 3,977 cases. Ann Thorac Surg 2001; 72:1557–1561.[Abstract/Free Full Text]
  7. Saeed I, Anyanwu AC, Yacoub MH, Amrani M. Subjective patient outcomes following coronary artery bypass using the radial artery: results of a cross-sectional survey of harvest site complications and quality of life. Eur J Cardiothorac Surg 2001; 20:1142–1146.[Abstract/Free Full Text]
  8. Saeed I, Anyanwu AC, Yacoub MH, Amrani M. Subjective patient outcomes following coronary artery bypass using the radial artery: results of a cross-sectional survey of harvest site complications and quality of life. Eur J Cardiothorac Surg 2001; 20:1142–1146.[Abstract/Free Full Text]
  9. Royse AG, Royse CF, Shah P, Williams A, Kaushik S, Tatoulis J. Radial artery harvest technique, use and functional outcome. Eur J Cardiothorac Surg 1999; 15:186–193.[Abstract/Free Full Text]
  10. Denton TA, Trento L, Cohen M, Kass RM, Blanche C, Raissi S, Cheng W, Fontana GP, Trento A. Radial artery harvesting for coronary bypass operations: neurologic complications and their potential mechanisms. J Thorac Cardiovasc Surg 2001; 121:951–956.[Abstract/Free Full Text]
  11. Sunderland S. Nerve injuries and their repair: a critical appraisal 1991;New York: Churchill Livingstone.
  12. Dietl CA, Benoit CH. Radial artery graft for coronary revascularization: technical considerations. Ann Thorac Surg 1995; 60:102–109. discussion 109–110.[Abstract/Free Full Text]
  13. Reyes AT, Frame R, Brodman RF. Technique for harvesting the radial artery as a coronary artery bypass graft. Ann Thorac Surg 1995; 59:118–126.[Abstract/Free Full Text]
  14. Loop FD, Lytle BW, Cosgrove DM, Golding LA, Taylor PC, Stewart RW. Free (aorto-coronary) internal mammary artery graft. Late results. J Thorac Cardiovasc Surg 1986; 92:827–831.[Abstract]
  15. Tatoulis J, Royse AG, Buxton BF, Fuller JA, Skillington PD, Goldblatt JC, Brown RP, Rowland MA. The radial artery in coronary surgery: a 5-year experience – clinical and angiographic results. Ann Thorac Surg 2002; 73:143–147. discussion 147–148.[Abstract/Free Full Text]
  16. Buxton BF, Bellomo R, Gordon I, Hare DL. Radial versus right internal thoracic artery for myocardial revascularization. J Thorac Cardiovasc Surg 2004; 127:893–894. author reply 894–895.[Free Full Text]
  17. Grossebner M, Arifi A, Bourov Y, 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]
  18. Ikizler M, Ozkan S, Dernek S, Ozdemir C, Erdinc OO, Sevin B, Ozdemir G, Kural T. Does radial artery harvesting for coronary revascularization cause neurological injury in the forearm and hand. Eur J Cardiothorac Surg 2005; 28:420–424.[Abstract/Free Full Text]
  19. Patel AN, Henry AC, Hunnicutt C, Cockerham CA, Willey B, Urschel Jr HC. Endoscopic radial artery harvesting is better than the open technique. Ann Thorac Surg 2004; 78:149–153.[Abstract/Free Full Text]

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Murat Özeren
Interactive CardioVascular and Thoracic Surgery 2006 5: 438. [Full Text] [PDF]



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ICVTS on-line discussion A
Interactive CardioVascular and Thoracic Surgery, August 1, 2006; 5(4): 438 - 438.
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