Should the internal thoracic artery be skeletonized?

2004;77:2238-2246 Ann Thorac SurgArjuna Weerasinghe, Brian Glenville and Roberto Casula

Thanos Athanasiou, Mary-Clare Crossman, George Asimakopoulos, Ashok Cherian, Should the internal thoracic artery be skeletonized?

http://ats.ctsnetjournals.org/cgi/content/full/77/6/2238located on the World Wide Web at:

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

Print ISSN: 0003-4975; eISSN: 1552-6259. Southern Thoracic Surgical Association. Copyright © 2004 by The Society of Thoracic Surgeons.

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

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hould the Internal Thoracic Artery Bekeletonized?

hanos Athanasiou, MD, PhD, Mary-Clare Crossman, MRCS,eorge Asimakopoulos, FRCS, Ashok Cherian, MD, Arjuna Weerasinghe, FRCS,rian Glenville, FRCS, and Roberto Casula, FECTS

he National Heart and Lung Institute, Imperial College of Science, Technology and Medicine, Department of Cardiothoracic
urgery, St Mary’s Hospital, London, United Kingdom
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raditionally, the internal thoracic artery is harvested aspedicle. In contemporary cardiac surgical practice, how-ver, certain surgeons practice the internal thoracic ar-ery-skeletonization technique. A systematic review oflinical studies reporting on the use of skeletonizednternal thoracic arteries (SKT-ITA) has not yet beenerformed. The primary aim of this review article is to
xamine comprehensively the entire body of evidence
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egarding the use of SKT-ITA. In particular, we aimed tonalyze the effects of skeletonization on sternal bloodupply, wall damage and blood flow in the harvestedessel, postoperative graft patency, and clinical outcome.dvantages and disadvantages of the skeletonization

echnique are highlighted and discussed.(Ann Thorac Surg 2004;77:2238–46)

© 2004 by The Society of Thoracic Surgeons

he left internal thoracic artery (LITA) is widely ac-cepted as a superior conduit in coronary artery

ypass (CABG) procedures. More recently, the use ofilateral internal thoracic arterial (BITA) grafts has beenemonstrated to be more beneficial in comparison toingle internal thoracic artery (ITA) with regard to sur-ival, freedom from repeat angioplasty or reoperation [1,]. It has been suggested that revascularization by usingITA specifically on the left coronary system can poten-

ially improve clinical outcome [3, 4]. The most seriousbjection to the use of BITA has been an increased risk ofound complications [5]. Advocates of ITA skeletoniza-

ion postulate that this technique reduces sternal devas-ularization and wound healing problems, and may po-entially increase the number of arterial anastomoses peratient by increasing the length of the ITA [6].Traditionally, most ITA grafts are harvested as a pedi-

le. The skeletonized internal thoracic artery (SKT-ITA)ay be defined as the arterial conduit that has been

issected from all surrounding tissues, the accompany-ng veins, fascia, lymphatics, adipose tissue, and chestall. The technique leaves the adventitia as the outerost layer of the harvested conduit.The concept of skeletonization is not new. The tech-

ique was more described in detail by Keeley in 1987 [7].systematic review of clinical studies reporting on the

se of SKT-ITAs has not yet been performed. The pri-ary aim of this review article is to examine comprehen-

ively the entire body of evidence regarding the use ofhe SKT-ITAs. In particular, we aimed to analyze infor-

ation related to the effects of skeletonization on sternallood supply, wall damage and blood flow in the har-

ddress reprint requests to Dr Athanasiou, Cardiothoracic Surgery, 70 St.

ested vessel, postoperative graft patency, and clinicalutcome.

aterial and Methods

iterature Searchliterature search (MEDLINE) of studies reporting on

he use of SKT-ITAs, published between 1965 and 2003,as performed. The following keywords were used:

skeletonized internal thoracic artery,” “internal thoracicrtery and free flow,” and “bilateral skeletonized internalhoracic arteries.” Internal mammary artery was taken toe synonymous with internal thoracic artery throughout.rticles were also identified by using the function “re-

ated articles” in PubMed.

ata Extraction and Validation of the Studieshe endpoints of interest were mortality, major in-ospital morbidity, long-term follow–up, and angio-raphic patency following SKT-BITA or LITA harvesting.tudies of SKT-LITA and BITA are tabulated (Tables 14). Care was taken to avoid inclusion articles reportingn the same patient populations. Studies were excludedhen both values (mean and standard deviation of theean) for the free flow of ITA in each group were not

eported or when results involved less than 10 ITAs inither group. The following information was extractedrom each study: first author, year of publication, studyopulation characteristics, study design (prospective,andomized, retrospective or other), selection criteriand exclusion criteria, number of patients operated onith each technique, timing of free flow measurement,

nd method of vasodilating agent used (Table 5). We alsossessed the validity of the studies identified taking into
onsideration the source and the strength of the evidence
0003-4975/04/$30.00doi:10.1016/j.athoracsur.2003.10.041

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2239Ann Thorac Surg REVIEW ATHANASIOU ET AL2004;77:2238–46 SHOULD THE INTERNAL THORACIC ARTERY BE SKELETONIZED?

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y using the grading system of the US Preventive Ser-ices Task Force [8]. Accordingly, Grade A for strength ofhe evidence is awarded when there is “good evidence toupport the recommendation,” Grade B when there isfair evidence,” and Grade C when there is “insufficientvidence for or against.”

tatistical Analysistatistical analysis was carried out by using the weightedean difference (WMD) as the summary statistic. In

able 1. Mortality and Major Morbidity After Use of Skeleton

uthor andeference Year

Number ofSKT-BITA

OperativeMortality AMI

albut et al [26] 1990 1087 29 222.7% 2%

ical et al [27] 1996 560 9 171.6% 3%

alafiore et al [6] 1999 842 18 62.1% 0.7%

evni et al [28] 2003 1000 34 103.4% 1%

im et al [29] 2002 223 3 41.3% 1.8%

onacchi et al [30] 2001 114 3 42% 3%

rapas et al [31] 2003 590 6 21% �1% �

auvage et al [32] 2003 150 4 13.2% 0.8%

MI � acute myocardial infarction; ARDS � airway respiratory dishoracic Artery; CVA � cerebrovascular event; LCO � cardiac ouf operation; SI � sternal infection; SKT � skeletonized; TIA

able 2. Mortality and Morbidity After Use of Skeletonized L

uthors andeference Year

Number ofSKT-LITA

OperativeMortality AMI L

ohen et al [19] 1999 10 NR NR

endler et al [34] 2001 576 12 92% 1%

eja et al [33] 1999 70 1 51.4% 7.1%

artier et al [37] 2002 200 3 71.5% 3.4%

akami et al [36] 2002 45 0 NR0%

igami et al [15] 2001 200 1 20.5% 1%

alpoth et al [35] 1996 10 0 00% 0%

MI � acute myocardial infarction; ARDS � airway respiratory divent; LCO � cardiac output; LITA � left internal thoracic artery
peration; SI � sternal infection; SKT � skeletonized; TIA � transi

igure 1, squares indicate point estimates of treatmentffect (WMD), with the size of the square representinghe weight attributed to each study and 95% confidencentervals indicated by horizontal bars. The diamondepresents the summary from the pooled studies with5% confidence intervals. The point estimate is consid-red statistically significant at the p less than 0.05 level ifhe 95% confidence interval does not include the verticalar. Analysis was conducted using the Review Manager,ersion 4.1 (The Cochrane Collaboration, Software Up-

BITA

Morbidity

diacNeurological

CVA/TIARespiratory

ARDSRenalARF

WoundSIArrythmias

NR 20 35 NR 191.8% 3.2% 1.7%

NR 6 9 NR 61.1% 1.6% 1.1%

NR 10 16 18 141.2% 1.9% 2.1% 1.7%

NR 12 NR NR 221.6% 2.2%

27 0 NR 2 312.1% 0% 0.9% 1.3%14 2 NR 7 212.7% 1% 6% 1%88 0 NR NR 115% 0% �1%

NR NR NR NR 97.2%

syndrome; ARF � acute renal failure; BITA � Bilateral InternalNR � non-recorded; Operative Mortality � death within 30 days

sient ischemic attack.

Morbidity

diacNeurological

CVA/TIARespiratory

ARDSRenalARF

WoundSIArrythmias

NR 1 NR NR 110% 10%

NR 9 NR NR 81% 1%

NR NR NR NR 00%

NR NR NR NR 21%

NR NR NR NR 12%

NR 4 NR NR 02% 0%

NR 0 0 0 00% 0% 0% 0%

syndrome; ARF � acute renal failure; CVA � cerebrovascularNR � non-recorded; Operative Mortality � death within 30 days of

ized

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ent ischemic attack.



Table 3. Angiographic Patency and Follow-Up After Use of Skeletonized BITA

Author andReference Year

Numberof

SKT-BITA

Postoperative Angiographic PatencyOutpatient Follow-Up

Number ofPatients

UnderwentAngiography

AngiographicPatency

Number ofPatients

FollowedUp as

Outpatient

Length ofFollow-Up(months)

ActuarialSurvival

ActualSurvival

Event-FreeSurvival

(% asymptomaticpatients of those

followed up)

Number ofPatients

RequiringReintervention

Galbut et al [26] 1990 1087 53 (4%) 84.9%–92.1% (53 months) 1041 39 (1–17 years) 80% � 3.2% (10 years) 92.2% 90.6% 16 (1.6%)60% � 5% (15 years)

Bical et al [27] 1996 560 104 (19.8%) 97.9% (10 days) 540 29 � 20 NR 95.9% 90.6% 2 (0.36%)95.2% (22 months)

Calafiore et al [6] 1999 842 133 (15.8%) 98.2% (�30 days) 822 16.3 � 11 96.4% � 0.8% 95.4% 95.4% 4 (0.48%)96.8% (7.6 � 2.3 months)

Pevni et al [28] 2003 650 41 (6.3%) 95.4% (23 � 6 months) 631 23 � 6 94.8% (1 year) NR 97.5% 15 (2.3%)92.5% (3 years)

Kim et al [29] 2002 223 218 (97.7%) 98.1%–99% NR NR NR NR NR NRSauvage et al [32] 2003 125 32 (25.6%) 85%–87% (7.4 years) 100% 117.6 61.6 (10 years) 85.6% 85% (9.1 years) 109 (90%)

BITA � bilateral internal thoracic artery; NR � not recorded; SKT � skeletonized.

Table 4. Angiographic Patency and Follow-Up After Use of Skeletonized LITA

Author andReference Year

Number ofSKT-LITA

Postoperative Angiographic PatencyOutpatient Follow-Up

Number ofPatients

UnderwentAngiography

AngiographicPatency

Number ofPatients

Followed Upas Outpatient

Length ofFollow-Up(months)

ActuarialSurvival

ActualSurvival

Event-FreeSurvival

(% asymptomaticpatients of those

followed up)

Number ofPatients

RequiringReintervention

Huddleston et al [38] 1986 222 222 (100%) 55.1% (120 months) NR NR NR NR NR NRHigami et al [15] 2001 200 188, 1 month (94%) 99.5% (1 month) 200 14.8 � 6.1 NR 98% 100% 0 (0%)

20, 1 year (10%) 100% (1 year)

LITA � left internal thoracic artery; NR � not recorded; SKT � skeletonized.

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ate, Oxford, United Kingdom). Sensitivity analysis waserformed by reanalyzing the data using different statis-

ical approaches (eg, using a random effects model in-tead of a fixed effect model) and by funnel plots tovaluate asymmetry [9].

nternal Thoracic Artery: Anatomy, Physiologynd Harvesting Techniqe

natomy and Physiology of the ITAhe ITA originates bilaterally from the inferior aspect of

he first part of the subclavian artery. It passes down-ards posterior to the brachiocephalic vein and medial to

he scalenus anterior muscle. Its further route is lateral tohe border of the sternum until the sixth intercostal spacehere it divides into the superior epigastric and the mus-

ulophrenic arteries. The ITA is accompanied by two venaeomitantes. It provides collateral blood flow to the ster-um by giving off the perforating arteries, that originate

rom the anterior aspect of the ITA, and connect with thentercostal arteries or by giving off intercostal arteriesirectly to the sternum. Several anatomic variations of

hese two main types have been identified [10]. It iseasonable to suggest that harvesting of the ITA is moreikely to impair sternal blood supply when this is pro-ided by intercostal arteries arising directly from the ITA.

able 5. Studies Comparing Free Flow of ITA Harvested as Pe

uthor andeference Year

PED/SKTNumber of

Patients TOS

hoi et al [40] 1996 14/23 Nonrandomizedeja et al [33] 1999 70/287 Nonrandomizedoera et al [22]b 1993 15/5 Nonrandomizedalpoth et al [35] 1996 10/10 Randomizedendler et al [39] 1999 40/40 Nonrandomized

Matching criteria: 1 � age; 2 � sex; 3 � body surface area; 4 � surge

eight; b Excluded from the meta-analysis.

PB � cardiopulmonary bypass; MAP � mean arterial pressure; PEype of study.

ig 1. Meta-analysis of studies comparing free flow of ITA harvestedary from the pooled studies showing that the weighted mean differe

n comparison to the pedicled conduit. (CI � confidence interval; ITA
eviation; SKT-ITA � skeletonized ITA.)

here is, however, absence of clinical proof for thisssumption.The layers of the wall of the ITA are common to most

essels: the tunica intima, tunica media, and tunicadventitia. The tunica intima contains endothelial cellsesting on a basal lamina. The tunica media consistshiefly of smooth muscle cells and is separated from theunica intima by the internal elastic lamina. The tunicadventitia gradually becomes continuous with the envel-ping connective tissue and contains vasa vasorum and

ymphatics. The ITA, however, is not thought to beeliant on vasa vasorum. Luminal diffusion can reach aange of 350 to 600 �m [11] and the thickest part of theedia measures approximately 150 �m. It is likely that

he ITA does not suffer if the vasa vasorum are disruptedy skeletonization.

hich Harvesting Technique Should Be Preferred?arvesting of skeletonized ITA is time consuming and

equires higher level of surgical precision in comparisono pedicled conduit [12, 13]. There is a learning curve-ffect related to the factor-surgeon. Cautery should besed on a low setting and kept away from the ITA.xposure of the ITA after standard median sternotomy isy dissection of loose areolar tissue and pleural reflec-

ions posterior to the sternum. The vessel is teased away

d Versus Skeletonized Conduit

hingriaa Timing of Free Flow Measurement

Application ofPapaverine atthe Time of

Measurement

On CPB, MAP � 50–55 mm Hg Spray,6,7 On CPB On flow 2.2 L*min�1*m�2 Soaked swab

Before CPB On normal SP SprayBefore CPB Soaked swabBefore CPB MAP � 70 mm Hg Intraluminal

� number of distal anastomoses; 6 � angina status; 7 � diabetes; 8 �

pedicled; SKT � skeletonized; SP � systemic pressure; TOS �

dicled or skeletonized conduit. The diamond represents the sum-MD) of the ITA flow is 32.88 mls/min in favor of the skeletonized

ternal thoracic arteries; PED-ITA � pedicled ITA; SD � standard

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2242 REVIEW ATHANASIOU ET AL Ann Thorac SurgSHOULD THE INTERNAL THORACIC ARTERY BE SKELETONIZED? 2004;77:2238–46

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rom the chest wall, accompanying veins, fascia, lym-hatics and adipose tissue using a cold cautery tip orcissors. Forceps should not touch the ITA directly.ranches are divided between two metallic clips usingcissors. Throughout dissection, dilute papaverine isprayed onto the internal mammary artery to preventessication and counteract spasm.Studies detailing the long-term follow-up of patency

nd outcome after harvesting the SKT-ITA by electrocau-erization are lacking. Yoshida and coworkers [14] usedight and electron microscopy, in a canine model, toemonstrate that monopolar cauterization was moreommonly associated with intimal corrugation as com-ared with bipolar cauterization. Higami and colleagues

15] described an ultrasonic scalpel method for ITAarvesting. Two hundred patients underwent SKT-ITAarvesting using the ultrasonic scalpel and were exam-

ned for early angiographic patency at 1 month. Patencyf 99.7% of LITAs and 100% of RITAs was demonstrated.imited follow-up of 20 patients (34 ITAs) demonstrated00% patency at 1 year. Bolotin and associates [16] testedhe safety of robotic ITA skeletonization in dogs. Skele-onized harvesting technique was not associated withistologic or functional ITA damage although roboticallyarvested SKT-ITA required more operative time [16].

ata ReviewOW DOES SKELETONIZATION AFFECT BLOOD SUPPLY TO THE STER-

UM? (EVIDENCE GRADE A). A major factor in wound healings adequate blood supply. Sternal devascularization fol-owing pedicled internal mammary artery harvesting isell documented [17]. It seems that there is a higher riskf damaging the collateral blood supply of the sternumsternal/intercostal branches, sternal/perforatingranches and persistent posterior intercostal artery)hen the ITA is harvested as a wide pedicle [10]. Sternallood supply after skeletonization has been investigated

n a few studies. Lorberboym and colleagues [18] andohen and coworkers [19] produced similar studies that

ompared single photon emission computed tomographySPECT) of two sides of the sternum of patients pre- andost-CABG. Loberboym and colleagues [18] randomized3 patients in to either pedicled (12 patients) or skeleton-zed (11 patients) ITA harvesting. Results demonstratedignificantly reduced postoperative sternal vascularityfter harvesting as a pedicle. Cohen and coworkers [19]andomized LITA harvesting to either skeletonized (11atients) or pedicled (12 patients) technique and came toimilar conclusions. Parish and associates [20] used ra-ioactive microspheres to examine chest wall vascularityfter ITA harvesting in a canine model. They found atatistically significant reduction in residual blood flow tohe sternum after pedicled harvesting when comparedith skeletonized ITA [20].

OES SKELETONIZATION CAUSE DAMAGE TO THE HARVESTED ITA?

EVIDENCE GRADE C). Graft failure may be caused by damageo the vessel wall of the harvested conduit. Such injury

ay result in thrombus formation and graft occlusion.
audino and coworkers [21] used immunohistochemis- f

ry with light and electron microscopy to study the vesselall of harvested ITAs and compared the skeletonized

echnique with a pedicle method. Dissection with lowoltage bipolar electrocautery was employed. Examina-ion demonstrated no cases of vessel disruption, dissec-ion or macroscopically detectable thrombosis in eitherroup. Of note however, were two cases of microthrombidherent to the endothelial layer in the skeletonizedroup [21].In 1993, Noera and associates [22] used light micros-

opy to examine the ITA in 70 patients. Ten of these werekeletonized. No statistically significant difference wasound between harvesting techniques although thereas a tendency for skeletonized vessels to contain a

arger number of lesions in the endothelium, microscopicntimal dissection and detachment and also injuries tohe external elastic lamina [22].

Sasajima and coworkers [23] used light and electronicroscopy to examine SKT-ITA specimens harvested

sing bipolar cautery in six dogs. The contralateral ITAas used as a control. Segments of specimens were taken

t 3 and 12 weeks. Gross observation demonstrated nonjury or deformity after skeletonization and light mi-roscopy revealed no major differences in the vessel walletween control and skeletonized vessels. In a similartudy in dogs, Ueda and colleagues [24] demonstratedhat the expression of von Willebrand Factor and endo-helial nitric oxide synthase, as markers of endothelialamage, was similar in skeletonized and pedicled ITAs.keletonization, however, induced more neovasculariza-

ion in the adventitia [24].Recently, in a randomized study, Gaudino and associ-

tes [25] compared skeletonized and pedicled ITAs inerms of early vasoreactive profile. Pharmacologic stim-lation of the ITA was performed during postoperativengiogram on the second postoperative day, using anntraluminal infusion of serotonin and acetylcholine. Noifferences in vasoactive profile were identified betweenkeletonized and pedicled ITAs [25].

OES MORTALITY AND MORBIDITY IMPROVE BY THE USE OF SKT-

ITAS OR LITAS? (EVIDENCE GRADE C). The benefits of bilateralnternal mammary arterial grafting have been well doc-mented by many studies [1, 2]. With regard to SKT-ITAs or SKT-LITAs, short- to mid-term outcome alsoppears to be similar to those achieved with pedicledITA or LITA [6, 15, 19, 26–37]. Tables 1 and 2 demon-trate that postoperative complications, including cardiacomplications and sternal wound infections, after use ofilateral skeletonized conduits are consistently low andot offset by any increase in mortality. Only three studiesere randomized [19, 30, 35].

S THERE ANY EVIDENCE THAT EARLY AND LATE ANGIOGRAPHIC

ATENCY OF SKT-BITAS IS SUPERIOR TO PED-BITAS? (EVIDENCE

RADE C). Nine previous publications reported postopera-ive angiographic findings in patients who underwentABG with SKT-BITA or LITA (Tables 3 and 4) [6, 15,6–29, 32, 38, 39]. Postoperative angiography was per-
ormed to investigate suspected recurrence of symptoms


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nd included only a small minority of the patients.igures demonstrated levels of patency that were similaro patency rates for PED-ITA. Survival figures, bothctuarial and actual were also satisfactory. The differingengths of follow-up periods between studies make ac-urate comparison of the figures difficult. It is worthoting that no prospective randomized trial has beenublished comparing angiographic patency of SKT-ITAersus PED-ITA.

S THE FREE FLOW OF THE SKELETONIZED ITA SUPERIOR IN COMPAR-

SON TO PEDICLED ITA? (EVIDENCE GRADE B). We conducted aeta-analysis of studies including at least 20 patients andeasuring free blood flow of the ITA after division (at

ero distal resistance) and before the anastomosis to theoronary target [22, 33, 35, 39, 40]. Details of the studiesdentified are summarized in Table 5. Volume of free flownto a beaker from skeletonized ITA was measured. Theesults depicted in Figure 1 indicate better free flow fromkeletonized vessels as compared with those harvested as

pedicle with a WMD of 32.88, and 95% confidencentervals of 29.51 to 36.25. No significant heterogeneityas identified between studies and funnel plot did not

xhibit any asymmetry. Important drawbacks of thiseta-analysis was the fact that numbers of patients in

ach group were not identical and that four out of the fivetudies were not randomized.

In a large retospective study, short-term and long-termutcome of skeletonized and pedicled ITAs were as-essed in 814 patients [38]. Findings demonstrated thateither free flow before grafting nor harvesting tech-ique bore any relation to graft patency in the long-term.wo other studies [35, 36] measured intraoperatively

ransit time flow after grafting was completed. The firsttudy revealed significantly greater intraoperative flow inhe SKT group in comparison to the PED group. Thisifference was not identified in the second study. Furthertudies with longer-term follow-up would be importantdditions to the literature in this area.

OES SKELETONIZATION AFFECT CLINICAL OUTCOME IN DIABETIC

ATIENTS? (EVIDENCE GRADE C). CABG is the treatment ofhoice for coronary artery disease in diabetic patients41], although the LITA is regarded as the superior graftor long-term function [1]. When both ITAs are used, theisk of sternal wound complications in diabetic patients isncreased 4- to 20-fold [42, 43]. Wendler and coworkers34] investigated 576 patients who underwent completerterial revascularization using a skeletonized LITA andither RITA or radial artery. Of these patients, 174 wereiabetic. Obesity, female sex, triple vessel disease, and

mpairment of left ventricular function were more fre-uent in the diabetic group. The incidence of BITA useas similar in the two groups (20% and 21%) and thereas no significant difference in mortality or morbidity

44].In a retrospective analysis, Uva and colleagues [45]

xamined 207 diabetic patients who underwent eitherKT-BITA (n � 74) or single skeletonized ITA (n � 133)
arvesting. The SKT-BITA group had fewer females, r

ewer emergency operations, and younger patients. Per-aps as a result, mortality was statistically greater in theingle ITA group. Total numbers of postoperative com-lications were similar between the two groups.A more recent study by Lev-Ran and associates [46]

xamined the feasibility of SKT-BITAs in insulin-treatediabetic patients undergoing CABG. The comparisonetween the two ITAs and one ITA group revealed thatternal wound infection was not significantly higher (4%s 2.7%) and in a multivariate analysis the use of twoTAs was found to have a protective effect in cardiacelated event-free survival. Interpretation of this result isather problematic because most surgeons would regardn infection sternal wound infection rate of 4% asnacceptable.

OES SKELETONIZATION AFFECT CLINICAL OUTCOME IN THE EL-

ERLY? (EVIDENCE GRADE C). Kramer and coworkers [47] ad-ressed the question of whether skeletonizing the ITAeduces morbidity in the elderly. This study investigated03 patients 70 years old and older who underwentABG using skeletonized BITAs. Mortality of 2.6% and

ternal wound infection rate of 2% compared favorablyith reported outcomes after single ITA harvesting.urevitch and colleagues [48] retrospectively studied the

ffect of age on outcome in 634 patients undergoingABG with skeletonized BITA. Older age was not asso-

iated with increased mortality or morbidity [48].

OES SKELETONIZATION AFFECT POSTOPERATIVE RESPIRATORY

OMPLICATIONS RATES? (EVIDENCE GRADE C). Postoperative re-piratory complications after CABG have been related toactors such as anesthesia, bypass time, use of ITA andurgical technique. The effect of skeletonized versusedicled ITA harvesting with or without pleurotomy wasddressed by two studies. Bonacchi and associates [30]tudied respiratory dysfunction after BITA harvesting.atients were randomized into the following groups: 82atients in the skeltonized group with closed pleura, 186atients in the pedicled group with open pleura, and 31atients in the skeletonized group with incidentallypened pleura. Postoperative respiratory complicationsere similar in the groups with open pleura regardless ofarvesting technique. Mechanical ventilation time wasignificantly higher in the groups with pleurotomy. Theedicled group had significantly greater numbers requir-

ng prolonged ventilation, unilateral pleural effusion,ostoperative thoracentesis, and atelectasis when com-ared with the skeletonized group [30]. In a small studyatsumoto and coworkers [49] demonstrated that reduc-

ion in forced vital capacity postoperatively was signifi-antly greater after pedicled ITA harvesting. Pleurotomytself did not appear to affect postoperative forced vitalapacity [49].

FFECT OF SKELETONIZATION IN POSTOPERATIVE BLOOD LOSS AND

TERNOTOMY-RELATED PAIN (EVIDENCE GRADE C). The effect ofkeletonization in postoperative blood loss was docu-ented in three comparative studies [6, 30, 37]. All three

eported a significant reduction in total blood loss post-



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peratively, but only the study by Calafiore and col-eagues [6] identified significant reduction in blood trans-usion requirements. A beneficial effect of skeletonizationn chest pain and analgesia requirements postopera-ively was found in two studies [19, 30].

OES SKELETONIZATION AFFECT MORTALITY AND MORBIDITY IN

FF-PUMP CORONARY ARTERY SURGERY? (EVIDENCE GRADE C). Usef skeletonized vessels in offpump coronary artery by-ass (OPCABG) procedures has been investigated inecent reports [29, 31, 37]. Cartier and coworkers [37]tudied 440 patients undergoing pedicled ITA harvestingnd 200 using skeletonization for OPCAB in a nonran-omized fashion. Groups were comparable for preoper-tive demographic characteristics except age: skeleton-zed patients were significantly older. BITAs werearvested more commonly in the skeletonized group

48% vs 27%). Mortality and morbidity were similaretween the two groups [37]. Kim and associates [29]tudied the use of skeletonized BITAs in OPCAB withifferent grafting arrangements and also found satisfac-

ory mortality and morbidity rates. Early postoperativeatency was 98.1% to 99% [29].

OES SKELETONIZATION OF THE ITA AFFECT THE INCIDENCE OF

OSTOPERATIVE HYPOPERFUSION SYNDROME? (EVIDENCE GRADE C).

ypoperfusion syndrome is a rare perioperative clinicalondition associated with low cardiac output, left ven-icular failure, and cardiac arrest. The major pathophy-ologic factor to ITA hypoperfusion is a disproportionetween ITA flow and myocardial demand due to severeenticular hypertrophy [51]. Takami and colleagues [36]eported that intraoperative measurement of flow with aransit-time flow meter is correlated with the diameter ofhe ITA just proximal to the anastomosis, and can besed as a quality control tool to identify patients at risk toevelop this condition. Previously published incidence ofse of intraaortic balloon pump perioperatively and oferioperative myocardial infarction (in comparativetudies) was comparable between pedicled and skeleton-zed groups [6, 30, 33–35].

omment

his review article aims to analyze previously publishediterature concerning the use of the ITA as a skeletonizedraft in patients undergoing CABG. Data, sternal bloodupply, wall damage, blood flow in the harvested vessel,ostoperative graft patency, and clinical outcome afterkeletonization, compared with the more commonly usededicled graft were the outcome points of the review.The performance of skeletonized conduits has been

ssessed in a number of retrospective trials. There isemarkable shortage of randomized trials investigating,n particular, the effects of LITA skeletonization. This isrobably due to the fact that the technique is used onlyy a minority of surgeons worldwide. Also, most of theey outcome variables of interest (mediastinitis rates,raft patency) would be expected to occur at very low
ates, thus necessitating a very large sample for statistical i

ower to be achieved. This would necessitate large mul-icenter studies.

Reduced damage of arterial branches supplying theternum is one of the theoretical advantages of skeleton-zation. Careful dissection with scissors or bipolar dia-hermy is the recommended method of skeletonizing theTA. With regard to sternal blood supply, studies dem-nstrated significantly lower sternal vascularity in pa-ients and animals undergoing harvesting of pedicled asompared to skeletonized conduits. There is no evidence,owever, that skeletonization is associated with lessostoperative sternal wound complications .Quality of the harvested vessel is a further important

ariable by which the technique of skeletonizationhould be judged. A small number of human and animaltudies reported no significant differences in the numberf vessel wall lesions between the two techniques. There

s a tendency, however, for skeletonised vessels to de-elop more vasa vasorum and to manifest microlesionsnd microthrombi, although the significance of this effectemains unknown. Blood flow of the conduit, both im-ediately after division of the distal end and after com-

letion of the anastomosis, appears to be better withkeletonization. The mechanism by which skeletoniza-ion might improve flow has not been ascertained. Oneheory is that skeletonization increases graft diameternd, therefore, decreases resistance [36]. Other contrib-tory factors may be that skeletonization facilitates theasodilating action of papaverine because topical papav-rine may reach more of the naked skeletonized internalammary than when it is hidden in a pedicle. The

linical and experimental studies reviewed above usedmall numbers of patients, limiting the power of statisti-al analysis. Despite better early flow, most of the studieseporting on long-term angiographic patency have beenerformed in small selected patient groups. They dem-nstrated similar levels of patency between skeletonizednd pedicled grafts. It should be noted that there is onlyne study by Sauvage and coworkers [32] that demon-trates patency rates of 85% to 87% for SKT-ITAs at aean of 7.4 years of follow-up in a cohort of 125 patients

ndergoing exclusive ITA grafting, with an impressiveverage of 3.9 grafts per patient without excluding high-isk patients (diabetics and obese). In this study freedomrom reintervention was 90.8% at a mean of 9.8 years.urthermore, mortality and major morbidity appears toe unaffected by the technique of single or bilateral ITAarvesting, both in low- and high-risk patient groups.ne exemption to this finding is postoperative lung

unction, which was demonstrated to be better afterkeletonization in two small randomized trials.

Potential advantages of the skeletonized ITA are thencreased length and diameter of the available conduit.his may result in a higher number of distal arterialnastomoses performed per patient. It is worth noting,owever, that there is no published study measuringbjectively length of the ITA before and after skeleton-

zation adjusting for length of the sternum, sex, height,nd weight of the patient. Increased length may be useful
n two situations. First, it may enable a sequential left ITA


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o be grafted to the left anterior descending and diagonalessels if indicated. The importance of such an arrange-ent is suggested by Huddleston and coworkers [38],ho propose the choice of conduit and the recipient graft

s the two factors that determine long-term patency.econdly, skeletonization of the right ITA grafting allows

t to reach distant target vessels, such as the distal leftnterior descending artery in cross-arrangement and theranches of the right coronary artery. This enables com-lex and complete arterial revascularization [13, 32, 50].nother potential advantage of skeletonization lies in the

mproved visualization of length, diameter, and vesseluality that it affords. The pulse of the conduit is alsoore easily assessed. An important disadvantage of

keletonization is that it comprises a technically demand-ng surgical technique, which may be time consumingnd necessitate retraining.In conclusion, we believe that there is limited pub-

ished literature on the use of skeletonized ITAs fororonary revascularization. It seems, however, that al-hough skeletonization may be technically demandingith an appreciable learning curve, it is a safe and useful

urgical technique for surgeons using the concept of totalrterial revascularization. Further research is required tovaluate any effect in postoperative morbidity and long-erm angiographic patency.

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2004;77:2238-2246 Ann Thorac SurgArjuna Weerasinghe, Brian Glenville and Roberto Casula

Thanos Athanasiou, Mary-Clare Crossman, George Asimakopoulos, Ashok Cherian, Should the internal thoracic artery be skeletonized?

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Should the internal thoracic artery be skeletonized?