Skeletonized radial artery grafting: improved angiographic results

2002;73:1880-1887 Ann Thorac SurgAtsushi Amano, Akihito Takahashi and Hitoshi Hirose

Skeletonized radial artery grafting: improved angiographic results

http://ats.ctsnetjournals.org/cgi/content/full/73/6/1880on the World Wide Web at:

The online version of this article, along with updated information and services, is located

Print ISSN: 0003-4975; eISSN: 1552-6259. Southern Thoracic Surgical Association. Copyright © 2002 by The Society of Thoracic Surgeons.

is the official journal of The Society of Thoracic Surgeons and theThe Annals of Thoracic Surgery

by on June 12, 2013 ats.ctsnetjournals.orgDownloaded from

http://ats.ctsnetjournals.org/cgi/content/full/73/6/1880

http://ats.ctsnetjournals.org

Skeletonized Radial Artery Grafting: ImprovedAngiographic ResultsAtsushi Amano, MD, Akihito Takahashi, MD, and Hitoshi Hirose, MD, FICSDepartment of Cardiovascular Surgery, Showa University Northern Yokohama Hospital, Kanagawa, Department ofCardiovascular Surgery, Kobari General Hospital, and Department of Cardiovascular Surgery, Shin-Tokyo Hospital, Chiba, Japan

Background. The radial artery has been used for coro-nary artery bypass grafting (CABG) but its early angio-graphic results were relatively inferior to that of theinternal mammary artery, most likely due to spasm of thegraft. To avoid vasospasm we harvested the radial arteryusing a skeletonized technique and spasm was com-pletely reversed before use. The graft patency of theskeletonized radial artery was compared with the radialartery graft harvested as a pedicle.

Methods. A total of 112 patients underwent isolatedCABG using a pedicled radial artery between September1, 1999, and August 31, 2000 (group P), and a total of 131patients with a skeletonized radial artery between Sep-tember 1, 2000, and August 31, 2001 (group S). Anultrasonic scalpel (Harmonic Scalpel; Ethicon Endo-Surgery, Cincinnati, OH) was used for skeletonizationand removing satellite veins and surrounding tissue.

CABG was performed by the standard technique. Peri-operative results were prospectively collected and com-pared between the two groups. Early angiographic re-sults performed within 3 months were also compared.

Results. There were two hospital deaths in group S.Major complications were observed in 11 (8.4%) in groupS and 3 (2.7%) in group P (p � not significant [NS]). Nonewere related to the radial artery graft. Angiography wasobtained in 96 patients of group S and 76 patients ingroup P and revealed that the stenosis free graft patencyrate of group S (138 of 143, 96.5%) was superior to that ofgroup P (73 of 86, 84.9%) with p < 0.005.

Conclusions. Skeletonization of the radial artery withthe ultrasonic scalpel is safe and contributes to reducingthe incidence of early graft stenosis.

(Ann Thorac Surg 2002;73:1880–7)© 2002 by The Society of Thoracic Surgeons

Coronary artery bypass grafting (CABG) using arterialgrafts is receiving increased attention since the

long-term patency rate of arterial grafts is reported to besuperior to saphenous vein grafts [1]. The internal mam-mary arteries (IMAs) are the most frequently used arte-rial conduits and their patency rates are reported to be90% or better even 10 years after surgery [1, 2]. Studieshave shown that bilateral internal mammary artery graft-ing could provide better event-free rates than single IMAgrafting in selected patients [1, 3]. The graft patency ofthe right internal mammary artery (RIMA) is reported tobe similar to that of the left internal mammary artery(LIMA) [2]. These RIMA and LIMA are considered to bethe first and second choices of arterial conduit in mostCABG cases: the third choice remains controversial.Previously, we published our data of radial artery bypassgrafting [4]. The 3-year patency rate of radial arterybypass in that series was 81.3% but graft stenosis orstring signs were observed in 12.2% at early angiographyand 12.6% at late. Some of this graft stenosis was consid-ered to be related to graft spasm. Severe graft spasm mayresult in hypoperfusion syndrome. To prevent early graft

spasm a modification of the harvesting technique of theradial artery was considered.

The skeletonized harvesting technique was firstadopted for IMA grafting [5]. Skeletonization of the IMAincreased the length of the graft and increased the freeflow and its caliber size compared with the pedicled graft[6]. Early angiographic results of skeletonized IMA graft-ing were favorable and graft spasm was not induced byskeletonization itself [7, 8]. Considering the favorablefacts of skeletonized IMA grafting we began to harvestthe radial artery using the skeletonized technique inSeptember 2000. We report here our 1-year clinical ex-perience of skeletonized radial artery grafting, which wascompared with pedicled radial artery grafting.

Material and Methods

PatientsBetween September 1, 1999, and August 31, 2001, a totalof 243 consecutive patients underwent isolated CABGusing the radial artery at Shin-Tokyo Hospital Cardio-vascular Group (Shin-Tokyo Hospital, Kobari GeneralHospital and Yokohama City Northern Hospital). In theearly half of the study period the radial artery washarvested routinely as a pedicle graft and in the late halfas a skeletonized graft. Between September 1, 1999, andAugust 31, 2000, 112 patients underwent CABG using a

Accepted for publication Feb 5, 2002.

Address reprint requests to Dr Hirose, Department of CardiovascularSurgery, Kobari General Hospital 29-1 Yokouchi, Noda City, Chiba278-8501, Japan; e-mail: [email protected].

© 2002 by The Society of Thoracic Surgeons 0003-4975/02/$22.00Published by Elsevier Science Inc PII S0003-4975(02)03559-2



pedicle radial artery (group P) and between September 1,2000, and August 31, 2001, 131 patients using a skeleton-ized radial artery (group S).

Technique of Radial Artery HarvestingRadial artery harvest was avoided in patients with renaldysfunction or patients with a positive Allen test. Theradial artery was harvested from the nondominant handin most cases.

The pedicle radial artery harvest was performed in theusual manner described previously [4]. Briefly, a skinincision was made from the wrist to the midantecubitalfossa. The brachioradialis muscle was retracted laterallyalong its entire length. The radial artery was immobilizedwith the satellite veins, covering fascia, and the sur-rounding adipose tissue. The branches of the radialartery were clipped and divided at just distal to thesatellite veins. Electrocautery to the radial artery or itsbranches was avoided. After transection of the distal endof the radial artery, it was cannulated and diluted milri-none was slowly injected. The proximal end was thentransected at the level of the bifurcation. The harvestedpedicle was preserved in warm papaverine solution.

Skeletonization of the radial artery was performedusing an ultrasonic scalpel (Harmonic Scalpel, dissect-ing-hook type; Ethicon Endo-Surgery, Cincinnati, OH).The fascia covering the radial artery and satellite veinswas dissected longitudinally using a metzenbaum. Thespace between the satellite vein and the radial artery wascarefully dissected using the ultrasonic scalpel. The re-moval of excessive tissue around the radial artery wasfacilitated by the cavitations ability of the ultrasonicscalpel, using it to sweep over the radial artery. This wascarried out quickly and the contact time of the ultrasonicscalpel and the radial artery was about 0.2 second toavoid damage to the vessel (“quick touch” method). Inthis way the main trunk of the radial artery was quicklyskeletonized. The branches of the radial artery were alsocontrolled 1 mm distal to main trunk, inside of thesatellite veins, with the ultrasonic scalpel, applying theblunt side of the blade perpendicular to the branches ata distance of at least 1.0 mm from the main trunk. In 3seconds the branch divided spontaneously with a proteincoagulum. The hook inside the blade was not used tocontrol a branch, otherwise the branch is often cut beforethe protein coagulum was made, which might result inincomplete hemostasis. After all the branches were con-trolled diluted papaverine was sprayed onto the graft toreverse vasospasm. Further dissection of the adventitiawas continued using micro-scissors (Fig 1). The vaso-spasm was further reversed by injecting diluted milri-none intraluminally through the distal end of the graft.Mild gentle pressure was applied during intraluminalinjection. After the complete reverse of vasospasm, theproximal end of the graft was transected. The harvestedradial artery was preserved in warm papaverine solutionuntil use.

CABGAfter harvesting of the appropriate grafts CABG wasperformed under cardiopulmonary bypass with normo-thermia (36°C) or under off-pump beating-heart. Theselection of off-pump CABG was individualized [9].

The target of the LIMA was primarily the left anteriordescending artery. If the RIMA was used for the bypassto the left anterior descending artery, the LIMA wasanastomosed to the diagonal or the circumflex artery.The gastroepiploic artery was used for revascularizationof the distal right coronary artery. Thus most of the radialartery was used for revascularization of the branches ofthe circumflex artery or main trunk of the right coronaryartery. When arteriosclerosis of the aorta was expected,the radial artery was used as a composite Y-graft usuallymade with the LIMA. The proximal diameter of the radialartery was measured just before the proximalanastomosis.

For the prophylaxis of perioperative vasospasm calci-um-channel blockers such as nicorandil or diltiazemwere administered systemically. An intravenous infusionof diltiazem (1 ug � kg�1 � min�1) or nicorandil (0.5 ug �kg�1 � min�1) was started after the induction of generalanesthesia and continued until the second postoperativeday. Oral diltiazem 180 mg/d or nicorandil 15 mg/d wasthen given for at least 1 year. Anticoagulation was startedon postoperative day 2 with aspirin 81 mg/d and di-pyridamole 75 mg/d.

Data CollectionThis study was conducted prospective manner. The in-stitutional ethics committee approved the skeletonizedradial grafting. The patients signed an informed consentbefore surgery. The following data were collected: pa-tient’s age, gender, cardiac profiles, preoperative riskfactors, graft material, surgical data, postoperative com-plications, and mortality. Outpatient follow-up was com-pleted by the referring cardiologists or hospital outpa-tient clinic. Cardiac events after discharge from hospitalwere reported. Myocardial infarction, angina, arrhythmiarequiring hospitalization, congestive heart failure requir-

Fig 1. The radial artery harvested with the skeletonized technique.

1881Ann Thorac Surg AMANO ET AL2002;73:1880–7 SKELETONIZED RADIAL ARTERY GRAFTING



ing hospitalization, coronary reintervention (percutane-ous transluminal coronary angioplasty [PTCA] with orwithout stent placement or redo-CABG), and suddendeath were counted as cardiac events. These follow-updata were compiled by October 31, 2001. The end pointswere patient death or the occurrence of one of thesecardiac events.

Angiographic ControlPostoperative angiographic control was obtained if thepatients agreed to the procedure. Most patients under-went postoperative angiography before discharge fromhospital but some patients underwent outpatient angiog-raphy within 3 months after surgery as per patientrequest. The quality of the anastomosis was gradedaccording to Fitzgibbon’s classification [10]. Briefly, gradeA stands for excellent graft patency, grade B for graftstenosis more than 50%, and grade O for occlusion.String sign, which was defined as a severe and extensivenarrowing of the whole body of the graft [11], wasclassified into grade B anastomosis.

Statistical AnalysisResults were expressed as mean � standard deviation.Statistical analysis was performed using Student’s t testfor continuous variables or �2 tests (Fisher’s exact tests ifn � 5) for categorical variables. A p value less than 0.05was considered significant. Postoperative patient survivaland event-free rates were calculated using the Kaplan-Meier method and compared with log-rank tests. Allstatistical analyses were performed using Statview ver-sion 5.0 (SAS Institute, Cary, NC).

Results

Patient DemographicsGroup S consisted of 131 patients (102 males and 29females with a mean age of 65.9 � 8.9 years), and groupP of 112 patients (80 men and 32 women with a mean ageof 65.8 � 8.9 years). The preoperative data are describedin Table 1. The two groups were not significantly different

Table 1. Preoperative Patient Demographics

Skeletonized(n � 131)

Pedicled(n � 112) p Value

Clinical characteristicsAge (years) 65.9 � 8.9 (33–90) 65.8 � 8.9 (34–86) NSAge over 75 years 20 15.3% 19 17.0% NSFemale sex 29 22.1% 32 28.6% NS

Cardiac profileUnstable angina 21 16.0% 19 17.0% NSAcute myocardial infarction 4 3.1% 4 3.6% NSPrevious myocardial infarction 82 62.6% 74 66.1% NSHistory of congestive heart failure 13 9.9% 17 15.2% NSPoor ejection function (� 40%) 13 9.9% 6 5.4% NSAtrial fibrillation 5 3.8% 2 1.8% NSRedo surgery 7 5.3% 5 4.5% NSEmergent surgery 8 6.1% 10 8.9% NS

Angiographic profileLeft main disease 25 19.1% 31 27.7% NSNumber of diseased vessels 28 � 0.4 (1–3) 2.8 � 0.4 (1–3) NSThree-vessel disease 100 76.3% 87 77.7% NS

Coronary risk factorsHypertension 85 64.9% 73 65.2% NSDiabetes 72 55.0% 54 48.2% NSInsulin user 22 16.8% 12 10.7% NSHyperlipidemia 58 44.3% 61 54.5% NSSmoking 60 45.8% 56 50.0% NSObesity 12 9.2% 17 15.2% NSFamily history 28 21.4% 17 15.2% NS

ComorbidityPeripheral vascular disease 12 9.2% 7 6.3% NSCerebral vascular accident 23 17.6% 17 15.2% NSChronic obstructive pulmonary disease 7 5.3% 3 2.7% NSCalcified ascending aorta 9 6.9% 10 8.9% NSRenal dysfunction 4 3.1% 4 3.6% NSHemodialysis 0 0.0% 0 0.0% NS

NS � not significant.

1882 AMANO ET AL Ann Thorac SurgSKELETONIZED RADIAL ARTERY GRAFTING 2002;73:1880–7



in terms of cardiac profile, angiographic profile, coronaryrisk factors, or preoperative comorbidities.

Operative ResultsOperative data are shown in Table 2. The mean numberof distal anastomoses was 3.7 � 1.0 in group S and 3.6 �0.9 in group P (p � NS). Off-pump CABG was morefrequently performed in group S than in group P. The useof the RIMA was significantly more frequent in group Sthan group P whereas the gastroepiploic artery andsaphenous vein were significantly more frequently usedin group P than group S. The total operation time wassignificantly shorter in group S than group P, reflecting

the number of cases in group S who underwent off-pumpCABG. The proximal diameter of the radial artery wassignificantly larger in group S (3.3 � 0.3 mm in group Sversus 3.1 � 0.3 mm in group P, p � 0.001). There were noincidences of radial artery dissection or injury duringgraft harvest in either group.

The distal anastomosis of each graft is shown in Table3. The target of the radial artery graft was primarily thecircumflex artery in both groups. Sequential radial arterybypass was performed in 44 cases (33.6%) in group S and19 cases (17.0%) in group P (p � 0.005). CompositeY-grafts were used in 15 patients (11.5%) in group S and9 patients (9.4%) in group P, showing no significant

Table 2. Surgical Results

nSkeletonized

(n � 131)Pedicled(n � 112) p Value

Number of distal anastomosis 3.7 � 1.0 (1–7) 3.6 � 0.9 (2–6) NSOff-pump coronary artery bypass graft 109 83.2% 74 66.1% �0.005Bilateral internal mammary artery 69 52.7% 32 28.6% �0.0005Total arterial revascularization 117 89.3% 86 76.8% �0.01Complete revascularization 128 97.7% 111 99.1% NSSequential radial artery bypass 44 33.6% 19 17.0% �0.005Radial composite graft 15 11.5% 9 8.0% NSCoronary anastomosis time/vessel 12.9 � 1.9 (7–18) 10.6 � 2.2 (6–18) �0.0001Clamp time (minutes) 99 � 37 (55–193) 80 � 20 (48–129) �0.0001Pump time (minutes) 147 � 42 (93–247) 125 � 42 (77–252) �0.0005Operation time (minutes) 323 � 71 (185–520) 347 � 85 (165–675) �0.05Left internal mammary artery 126 96.2% 108 96.4% NSRight internal mammary artery 72 55.0% 35 31.3% �0.0005Radial artery 131 100.0% 112 100.0% NAGastroepiploic artery 56 42.7% 74 66.1% �0.0005Inferior epigastric artery 1 0.8% 0 0.0% NSSaphenous vein 12 9.2% 26 23.2% �0.005Blood transfusion 35 26.7% 19 17.0% �0.05

NS � not significant; NA � not applicable.

Table 3. Distribution of Distal Anastomoses

LAD Diagonal Circumflex RCA Total

SkeletonizedLeft internal mammary artery 114 (78.6%) 19 (13.1%) 12 (8.3%) 0 (0.0%) 145Right internal mammary artery 16 (23.2%) 26 (37.7%) 19 (27.5%) 8 (11.6%) 69Radial artery 3 (1.5%) 31 (15.8%) 115 (58.7%) 47 (24.0%) 196Gastroepiploic artery 0 (0.0%) 0 (0.0%) 6 (10.3%) 52 (89.7%) 58Inferior epigastric artery 0 (0.0%) 1 (100.0%) 0 (0.0%) 0 (0.0%) 1Saphenous vein 0 (0.0%) 0 (0.0%) 5 (33.3%) 10 (66.7%) 15Total 133 (27.5%) 77 (15.9%) 157 (32.4%) 117 (24.2%) 484 (100.0%)

PedicledLeft internal mammary artery 108 (86.4%) 14 (11.2%) 3 (2.4%) 0 (0.0%) 125Right internal mammary artery 8 (22.9%) 16 (45.7%) 8 (22.9%) 3 (8.6%) 35Radial artery 1 (0.8%) 19 (14.5%) 91 (69.5%) 20 (15.3%) 131Gastroepiploic artery 0 (0.0%) 0 (0.0%) 12 (14.8%) 69 (85.2%) 81Inferior epigastric artery 0 0 0 0 0Saphenous vein 0 (0.0%) 2 (7.1%) 14 (50.0%) 12 (42.9%) 28Total 117 (29.3%) 51 (12.8%) 128 (32.0%) 104 (26.0%) 400 (100.0%)

LAD � left anterior descending artery; RCA � right coronary artery.




difference. All composite Y-grafts were created with theLIMA. The remaining were anastomosed onto the as-cending aorta.

In-Hospital ResultsThe postoperative course is displayed in Table 4. Postop-erative intubation time, intensive care unit stay, andpostoperative stay were not significantly different be-tween the two groups. There were two deaths in theentire group. They were both in group S and were due topostoperative stroke. Major complications occurred in 11patients (8.4%) in group S and 3 patients (2.7%) in groupP, without significant difference. No hypoperfusion syn-drome was observed related to the radial artery graft.Perioperative myocardial infarction occurred in 2 cases ingroup S, both of which were attributed to native arteryspasm and the grafts appeared to be patent by coronaryangiography. No postoperative bleeding from the radialgraft was observed in either group. There were no armwound complications.

Remote ResultsAmong the survivors, postoperative follow-up was com-pleted in all patients. The follow-up period was signifi-cantly shorter in group S (0.7 � 0.3 years) than in groupP (1.6 � 0.3 years). During the follow-up period, cardiacevents occurred in 3 patients (2.3%) in group S and 7patients (6.3%) in group P, as shown in Table 5. A total of5 PTCA were performed; however, none were related tothe radial artery bypass. Actuarial event-free rates at 1year were 98.1% in group S and 98.2% in group P, whichwas not significantly different by log-rank tests. Duringthe same follow-up period there was 1 death in group Sand 1 death in group P, giving an actuarial 1-year survivalrate after surgery of 99.1% in group S and 100% in groupP, showing no significant difference.

Angiographic StudyAngiographic control (angiography performed within 3months of surgery) was obtained in 96 patients (73.3%)with 143 anastomoses of radial artery in group S with aninterval between surgery and angiography of 0.9 � 1.8months, and 76 patients (67.9%) with 96 anastomoses ingroup P at 1.2 � 1.5 months. There were 2 (1.4%) radialartery occlusions in group S and 1 (1.2%) in group P (p �NS). The graft patency rate (grade A�B) was 98.6% ingroup S and 98.8% in group P, showing no significantdifference. Grade B stenosis was observed in 3 anasto-moses (2.1%) in group S and 12 (14.0%) in group P (p �0.0014). Among grade B stenoses, string signs were ob-served in zero patients in group S and in 6 patients ingroup P (p � 0.005). Anastomotic stenoses were observed

Table 4. Postoperative Outcomes

Skeletonized(n � 131)

Pedicled(n � 112) p Value

Intubation (hours) 8.4 � 5 (3–41) 6.6 � 9.1 (1–92) NSIntensive care unit stay (days) 2.1 � 0.8 (1–5) 2.2 � 0.8 (1–6) NSPostoperative stay (days) 12.8 � 5.9 (6–51) 12.9 � 3.4 (7–27) NSMajor complication (patients) 11 8.4% 3 2.7% NS

Low-output syndrome 0 0.0% 1 0.9% NSPostoperative myocardial infarction 2 1.5% 0 0.0% NSRespiratory failure 2 1.5% 2 1.8% NSPneumonia 0 0.0% 0 0.0% NASevere arrhythmia 0 0.0% 0 0.0% NACerebral vascular accident 4 3.1% 0 0.0% NSReexploration for bleeding 0 0.0% 0 0.0% NAPostoperative hemodialysis 0 0.0% 0 0.0% NAMediastinitis 2 1.5% 0 0.0% NSOthers 1 0.8% 0 0.0% NS

Inhospital deaths 2 1.5% 0 0.0% NS

NS � not significant; NA � not applicable.

Table 5. Remote Results

Skeletonized Pedicled

Number of patients followed up 129/129 (100%) 112/112 (100%)Follow-up period (years) 0.7 � 0.3 1.6 � 0.3Total outpatient cardiac events 3 (2.3%) 7 (6.3%)

Angina 1 3PTCA 2 3Congestive heart failure 1 0Arrhythmia 0 1Sudden death 0 0Others 0 0

1-year event-free rate 98.1% 98.2%2-year event-free rate 93.3%Distant death 1 (0.8%) 1 (0.9%)

Cardiac death 0 (0%) 0 (0%)Noncardiac death 1 (0.8%) 1 (0.9%)

1-year survival rate 99.1% 100.0%2-year event-free rate 98.9%

PTCA � percutaneous transluminal coronary angiography.




in 3 anastomoses in group S and 6 in group P (p � NS).Grade A anastomosis (stenosis or occlusion free anasto-moses) comprised 138 (96.5%) in group S and 73 (84.9%)in group P (p � 0.0016; Table 6).

Comment

Carpentier and associates [12] first reported CABG usingthe radial artery in 1973. However, its initial results wereso poor that Carpentier concluded that the radial arteryshould have not be used because of the high frequency ofearly graft occlusion [12]. These unsuccessful resultswere mostly due to technical problems occurring whileharvesting the radial artery and a lack of knowledge ofthe mechanism of vasospasm. Histologically the radialartery is classified as a muscular artery, which is knownto be liable to vasospasm in comparison with the IMA [1].Vasospasm of the arterial graft may result in seriouspostoperative complications, such as hypoperfusion syn-drome. The clinical application of the radial artery wasnot established until 1992 when Acar and colleagues [11]reported a series of 104 patients who underwent radialartery grafting with an angiographic early radial graftpatency rate of 93.5%. These improved results wereattributed to the appropriate use of a pharmacologicantispasm agent such as a calcium-channel blocker andto the modification of the radial artery harvesting tech-nique. Acar [11] recommended that the radial arteryshould be dissected en-bloc together with its pedicle,including the two satellite veins and the surroundingadipose tissue. To reverse vasospasm, radial cannulationand the injection of diluted papaverine were performed.Buxton and colleagues [13] reported that the vasocon-stricitve response of the radial artery was suppressed bythe use of the phosphodiesterase inhibitor milrinone.Adopting this technical protocol, radial artery graftingwas revitalized. Numerous reports regarding radial ar-tery grafting were published [14, 15]. Pedicle harvestingincluding the adjacent veins and surrounding connectivetissue was considered to be standard for radial artery

grafting. A very recent report also supported the pedicleharvesting for fear of graft spasm [16] and skeletonizationof the radial artery was believed to be contraindicated.

Parolari and coworkers [14] published a review ofradial artery grafting and demonstrated that the earlyradial graft patency rate was 98.1% (627 of 639) and thatthe perfect patency rate was 90.8% (474 of 522), reflectingthe graft occlusion found in 2.9% and graft stenosis in7.3%. Other reports also pointed out certain and consid-erable radial artery stenosis occurring in the early phaseafter surgery: 5.4% by Acar and colleagues [17], and 6.5%by Weinschelbaum and colleagues [18]. Radial arterygraft spasm affecting early graft stenosis wasemphasized.

The skeletonization technique was introduced into ourinstitute for IMA harvesting in early 2000. Skeletoniza-tion requires immobilization of the arterial trunk fromthe satellite veins and surrounding tissue. We wereinitially hesitant to adopt the skeletonization techniquedue to concerns about graft injury and vasospasm. How-ever, the application of an ultrasonic scalpel made theskeletonized graft harvest easier and safer. Dissection ofthe tissue planes and hemostasis of the branches wereadequately achieved by ultrasonic scalpel with minimumvasoconstriction.

The ultrasonic scalpel converts ultrasonic energy todenature tissue protein into a sticky coagulum that sealsblood vessels and bleeding tissue with less heat produc-tion than electrocautery [7, 19]. Higami and coworkers [7]reported that protein coagulum sealed the branch of theIMA without damaging the main trunk when the bladewas applied to the side branch at least 1 mm from themain trunk. Proper application of the ultrasonic scalpeldoes not injure the main trunk and achieves completehemostasis.

From the study of IMAs, skeletonization using ultra-sonic scalpel was found not to damage the endothelialfunction of the IMA. Choi and Lee [8] reported that theskeletonized IMA can deliver a higher blood flow thanthe pedicle IMA. The response to the intraluminally

Table 6. Postoperative Angiographic Results

Examined anastomosesby angiography

Skeletonized (96 Patients [73.3%]Examined)

Pedicled (76 Patients [67.9%]Examined)

p Value

Numberof Distal

AnastomosesGrade

BGrade

OGrade

A

Numberof Distal

AnastomosesGrade

BGrade

OGrade

A

Left internal mammaryartery

106 10 1 95 89.6% 80 7 0 73 91.3% NS

Right internal mammaryartery

53 4 0 49 92.5% 26 1 0 25 96.2% NS

Radial artery 143 3 2 138 96.5% 86 12 1 73 84.9% �0.005Gastroepiploic artery 41 3 1 37 90.2% 56 2 0 54 96.4% NSInferior epigastric artery 1 1 0 0 0.0% 0Saphenous vein 12 0 1 11 91.7% 19 0 0 19 100.0% NS

Interval between surgery and angiography was 0.9 � 1.8 months for skeletonized and 1.2 � 1.2 months for pedicled group. Grading of the anastomosisis according to Fitzgibbon’s criteria.

NS � not significant.




injected vasodilators was reported to be greater in theskeletonized graft than the pedicle graft [6]. Higher bloodflow through the bypass conduit is probably beneficialfor early postoperative coronary perfusion and it maydecrease the risk of hypoperfusion syndrome [15].

Considering the facts of skeletonized IMA grafting westarted to harvest the radial artery using an ultrasonicscalpel. Unlike electrocautery, graft spasm seldom occursby skeletonization using the ultrasonic scalpel. Dissec-tion between the radial artery and its satellite veins iswell performed using fragmentation mechanism. Tightadhesions, which are occasionally observed at the cath-eterization site, also can be dissected without injuring themain trunk of the radial artery. Even with extensivedissection along the radial artery, graft spasm was not amajor problem when the ultrasonic scalpel was used fordissection. Application of topical spray of papaverine andintraluminal injection of milrinone reverses vasospasmin the radial artery. Although skeletonized harvestingtakes a longer than pedicle harvesting, it had no influ-ence on the total operative time. We do not use electro-cautery for skeletonization of the radial artery, becausethe electrocautery causes heat injury which may result ingraft spasm. It would be interesting to see histologic orfunctional studies using animal models to support thehypothesis that skeletonization with the ultrasonic scal-pel is associated with lower trauma to the radial arterythan with the electrocautery.

Radial artery graft spasm rarely occurs under ourskeletonization protocol. No postoperative myocardialinfarction occurred in the territory of the radial graft. Theangiographic study successfully demonstrated the reduc-tion of string sign in the radial artery by use of ourskeletonization technique. We hypothesized that theseangiographical improvements were attributed to thecomplete reverse of vasoconstriction by removing allsurrounding tissue. The role of the adventitia should befurther analyzed in relation to the vasospasm. The angio-graphic follow-up of our series was extremely limited. Itis of great concern how the skeletonized radial arterygraft patency will progress in the remote follow-up.Furthermore, randomized study using the pedicle graftversus skeletonized graft is necessary to confirm ourinitial data.

Hemostasis of the ultrasonic scalpel was adequate. Nopatients developed postoperative bleeding from the skel-etonized conduits. Care should be taken in selecting theangle of the blade when applying to the branch of theartery. Inadequate angle of the blade may cause imma-ture hemostasis. In addition venous bleeding may not bestopped with ultrasonic scalpel, as the venous wall hastoo small an amount of protein to create coagulum [7].

Extensively reversed vasospasm and a larger caliber ofthe graft makes the anastomosis easier. Sequential graft-ing is carried out more easily in the skeletonized graftthan the pedicle graft because the skeletonized graft hasno adventitia and a good length. The pedicled radialartery anastomosed to the mildly stenosed coronaryartery often showed a narrowing in early angiography,because of flow competition between the graft and the

native coronary artery [4]. Thus a mildly stenosed coro-nary artery used to be bypassed with the saphenous vein,accepting the risk of vein graft disease. However, in thissituation now we can use the skeletonized radial artery asa valveless, large-caliber conduit that can deliver highflow. In our study bypass to the mildly stenosed coronaryartery was performed in 13 patients (11.6%) in group Pand 30 patients (22.9%) in group S (p � 0.05). Among the13 radial grafts to the mildly stenosed coronary artery, 1developed string sign by the early angiography; however,no string signs were observed in the skeletonized group.To optimize the high blood flow through the radial arterygraft, proximal anastomosis of the radial artery graftshould be the ascending aorta rather than creating acomposite graft with the LIMA.

The harvested skeletonized radial graft appeared to belonger than the pedicle graft. In our study the length ofthe radial artery was not compared between the twogroups because the length of the skin incision wasmodified according to the condition of the radial artery.Skin incision can be shortened in the skeletonized groupcompared with the pedicle group. Furthermore the distalpart of the radial artery has often been injured byprevious coronary angiography or arterial blood pressuremonitoring. The skeletonized and lengthened radial ar-tery allows us to discard the distal portion of the radialartery. Calcification or focal arteriosclerosis was reportedto be present in about 5% of radial arteries [15]. Becausefocal arteriosclerosis in the graft may influence graftpatency, the graft should be examined carefully. Theskeletonized radial artery graft is easily accessed whetheror not arteriosclerosis is present. Any affected portion ofthe radial artery should not be used.

While we harvested the radial artery as a pedicle, thelength of the graft was sometimes shorter than we hadexpected. In that case a composite graft was made withthe LIMA to lengthen the radial artery. Flow competitionbetween the radial artery and the LIMA was a greatconcern [4]. Because the skeletonized technique allowsus to harvest the radial artery with sufficient length foraortocoronary bypass, frequency of the composite graft-ing has been reduced. The application of compositegrafts using the skeletonized radial artery is limited tohigh-risk patients for aortocoronary bypass, such as pa-tients with severe arteriosclerosis including aortic calci-fication. Another factor influencing decreased frequencyof the composite graft is the availability of the bilateralIMAs. During the period of radial skeletonization all theIMAs were harvested with skeletonized fashion. Skele-tonized harvesting of the IMA is reported to maintainvenous return from the sternum and to reduce theincidence of sternal wound problems even with bilateralIMA harvesting [20, 21]. Bilateral IMA harvesting wasincreased from 28.6% in the early phase of our study to52.7% to the late phase but the incidence of mediastinitiswas not increased.

SummaryAlthough skeletonized radial artery harvesting was notpreviously recommended, the accurate application of an




ultrasonic scalpel allowed us to safely harvest the skele-tonized radial artery. In the skeletonized radial artery,vasospasm was easily reversed. Skeletonized radial graft-ing contributes to a wider range of selection of graftingtechniques including sequential bypass or bypass to ahigh-flow and mildly stenosed coronary artery. The ini-tial angiographic findings of the skeletonized radial ar-tery grafts successfully showed reduction of string sign.No skeletonized grafting-related adverse effects wereobserved. The fate of the skeletonized grafts should befollowed up carefully.

References

1. Reardon MJ, Conklin LD, Reardon PR, Baldwin JC. Coronaryartery bypass conduits: review of current status. J CardiovascSurg (Torino) 1997;38:201–9.

2. Barner HB. Arterial grafting: techniques and conduits. AnnThorac Surg 1998;66:S2–5.

3. Lytle BW, Blackstone EH, Loop FD, et al. Two internalthoracic artery grafts are better than one. J Thorac Cardio-vasc Surg 1999;117:855–72.

4. Amano A, Hirose H, Takahashi A, Nagano N. Coronaryartery bypass grafting using the radial artery: mid-termresults in a Japanese institute. Ann Thorac Surg 2001;72:120–5.

5. Higami T, Kozawa S, Asada T, Shida T, Ogawa K. Skeleton-ization and harvest of the internal thoracic artery with anultrasonic scalpel. Ann Thorac Surg 2000;70:307–8.

6. Wendler O, Tscholl D, Huang Q, Schafers HJ. Free flowcapacity of skeletonized versus pedicled internal mammaryartery grafts in coronary artery bypass grafts. Eur J Cardio-thorac Surg 1999;15:247–50.

7. Higami T, Maruo A, Yamashita T, Shida T, Ogawa K.Histologic and physiologic evaluation of skeletonized inter-nal thoracic artery harvesting with an ultrasonic scalpel.J Thorac Cardiovasc Surg 2000;120:1142–7.

8. Choi JB, Lee SY. Skeletonized and pedicled internal thoracicartery grafts: effect on free flow during bypass. Ann ThoracSurg 1996;61:909–13.

9. Amano A, Hirose H, Takahashi A, Nagano N. Off-pumpcoronary arterial bypass: mid-term results. Jpn J ThoracCardiovasc Surg 2001;49:67–78.

10. Fitzgibbon GM, Kafka HP, Leach AJ. Coronary bypass graftfate and patient outcome: angiographic follow-up of 5,065grafts related to survival and re-operation in 1,388 patientsduring 25 years. J Am Coll Cardiol 1996;28:616–26.

11. Acar C, Jebara VA, Portoghese M, et al. Revival of the radialartery for coronary artery bypass grafting. Ann Thorac Surg1992;54:652–60.

12. Carpentier A, Guermonprez JL, Deloche A, Frechette C, DuBost C. The aorta-to-coronary radial artery bypass graft. Atechnique avoiding pathological changes in grafts. AnnThorac Surg 1973;16:111–21.

13. Buxton B, Fuller J, Gaer J, et al. The radial artery as bypassgraft. Curr Opin Cardiol 1966;11:591–8.

14. Parolari A, Rubini P, Alamanni F, et al. The radial artery:which place in coronary operation? Ann Thorac Surg 2000;69:1288–94.

15. Buxton B, Windsor M, Komeda M, Gear J, Fuller J, Liu J. Howgood is the radial artery as a bypass graft? Cor Artery Dis1997;8:225–33.

16. Iaco AL, Teodori G, Di Giammarco G, et al. Radial artery formyocardial revascularization: long-term clinical and angio-graphic results. Ann Thorac Surg 2001;72:464–89.

17. Acar C, Ramsheyi A, Pagny JY, et al. The radial artery forcoronary artery bypass grafting: clinical and angiographicresults at five years. J Thorac Cardiovasc Surg 1998;116:981–9.

18. Weinschelbaum EE, Gabe ED, Macchia A, Smimmo R,Suarez LD. Total myocardial revascularization with arterialconduits: radial artery combined with internal thoracic ar-teries. J Thorac Cardiovasc Surg 1997;114:911–16.

19. Ohtsuka T, Wolf RK, Hiratzka LF, Wurnig P, Flege JB Jr.Thoracoscopic internal mammary artery harvest forMIDCAB using the harmonic scalpel. Ann Thorac Surg 1997;63:107–9.

20. Matsa M, Paz Y, Gurevitch J, et al. Bilateral skeletonizedinternal thoracic artery grafts in patients with diabetesmellitus. J Thorac Cardiovasc Surg 2001;121:668–74.

21. Calafiore AM, Vitolla G, Iaco AL, et al. Bilateral internalmammary artery grafting: midterm results of pedicled ver-sus skeletonized conduits. Ann Thorac Surg 1999;67:1637–42.




2002;73:1880-1887 Ann Thorac SurgAtsushi Amano, Akihito Takahashi and Hitoshi Hirose

Skeletonized radial artery grafting: improved angiographic results

& ServicesUpdated Information

http://ats.ctsnetjournals.org/cgi/content/full/73/6/1880including high-resolution figures, can be found at:

References http://ats.ctsnetjournals.org/cgi/content/full/73/6/1880#BIBL

This article cites 20 articles, 15 of which you can access for free at:

Citationshttp://ats.ctsnetjournals.org/cgi/content/full/73/6/1880#otherarticlesThis article has been cited by 15 HighWire-hosted articles:

Permissions & Licensing

[email protected]: orhttp://www.us.elsevierhealth.com/Licensing/permissions.jsp

in its entirety should be submitted to: Requests about reproducing this article in parts (figures, tables) or

Reprints [email protected]

For information about ordering reprints, please email:


http://ats.ctsnetjournals.org/cgi/content/full/73/6/1880

http://ats.ctsnetjournals.org/cgi/content/full/73/6/1880#BIBL

http://www.us.elsevierhealth.com/Licensing/permissions.jsp


Documents

Skeletonized radial artery grafting: improved angiographic results