2001;71:117-121 Ann Thorac SurgPierre Pagé and Louis P. Perrault

Olivier Chavanon, Michel Carrier, Raymond Cartier, Yves Hébert, Michel Pellerin, aortocoronary bypass surgery?

Increased incidence of acute ascending aortic dissection with off-pump

http://ats.ctsnetjournals.org/cgi/content/full/71/1/117on 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 © 2001 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 6, 2013 ats.ctsnetjournals.orgDownloaded from

Increased Incidence of Acute Ascending AorticDissection With Off-Pump Aortocoronary BypassSurgery?Olivier Chavanon, MD, Michel Carrier, MD, Raymond Cartier, MD, Yves Hebert, MD,Michel Pellerin, MD, Pierre Page, MD, and Louis P. Perrault, MD, PhDDepartment of Surgery, Research Center, Montreal Heart Institute, Montreal, Quebec, Canada

Background. An apparent increase in the incidence ofacute ascending aortic dissection following off-pumpcoronary artery bypass grafting (OPCAB) led us to assessretrospectively the rate and circumstances of this compli-cation in our institution on a consecutive series of pa-tients undergoing aortocoronary bypass performed withand without extracorporeal circulation (ECC).

Methods. A retrospective analysis of acute ascendingaortic dissections complicating coronary artery bypassgrafting surgery in 3,031 patients in our institution sinceApril 1, 1995, was performed using the database of theMontreal Heart Institute.

Results. There was a greater frequency of hypertensionin the OPCAB group. Iatrogenic acute aortic dissection

occurred in 3 patients among 308 operated on withoutECC (0.97%) and 1 patient among 2,723 operated onunder ECC (0.04%). This difference was statistically sig-nificant (p < 0.00001).

Conclusions. The risk of aortic dissection may beincreased in OPCAB. Careful manipulation of the aortawith a single side-clamping and a control of the arterialpressure should be used to minimize aortic trauma.High-risk patients should undergo CABG without side-clamping of the aorta or CABG with ECC to prevent thisredoubtable complication of myocardial revascularization.

(Ann Thorac Surg 2001;71:117–21)© 2001 by The Society of Thoracic Surgeons

Iatrogenic acute aortic dissection (IAAD) is a rare butpotentially fatal complication of coronary artery by-

pass grafting surgery. Its frequency is about 0.12% ofcases after open heart surgery with extracorporeal circu-lation (ECC) [1–3], and can occur intraoperatively or laterduring the postoperative hospitalization or after dis-charge [4]. With the new trend of minimally invasivecardiac surgery, and the regained interest for off-pumpcoronary artery bypass grafting (OPCAB) sparked byrecent advances in myocardial stabilization, a number ofoperative conditions have been modified. An apparentincrease in the incidence of acute ascending aortic dis-section following OPCAB led us to assess retrospectivelythe rate and circumstances of this complication in our in-stitution, on a consecutive series of patients undergoingaortocoronary bypass performed with and without ECC.

Patients and Methods

A retrospective analysis of acute ascending aortic dissec-tions complicating coronary artery bypass grafting sur-gery in 3,031 patients in our institution from April 1, 1995,to April 1997 was performed using the joint anesthesiolo-gy–surgery database of the Montreal Heart Institute.OPCAB was started in September 1996.

Revascularization With ECCAll ECC were performed under moderate hypothermia(33°C to 34°C) using the usual technique for CABGsurgery. After performing distal anastomosis anddeclamping the aorta, proximal anastomosis were per-formed with a beating heart using a Beck clamp, placedwhile decreasing the ECC flow to 500 mL/min which wasrepeated at the time of side and cross-clamping and un-clamping. Proximal anastomoses were done using 5-0polypropylene.

Off-Pump Coronary Artery BypassIn the early experience, patients were selected accordingto specific anatomic criteria: primary surgery, vesselsgreater than 1.5 mm in diameter. With increasing expe-rience, indications were broadened to most patients,including the circumflex artery territory providing therewere no intramyocardial arteries. The operative tech-nique has been previously described [5, 6]. Briefly, amechanical stabilizer system was used with the pressure-fixation concept. Patient positioning and pharmacologicmanagement using either intravenous nitroglycerin infu-sion or vasopressor drugs, allowed stabilization of hemo-dynamics during positioning of the heart for anastomo-ses. The left internal mammary artery was grafted to theleft anterior descending coronary artery (LAD) in themajority of patients (Table 1). Proximal anastomoseswere performed in the same manner as with ECC exceptno decrease of arterial pressure was induced at the time

Accepted for publication May 9, 2000.

Address reprint requests to Dr Perrault, Research Center, Montreal HeartInstitute, 5000 Belanger St E, Montreal, Quebec, Canada H1T 1C8; e-mail:lpperrau@icm.umontreal.ca.

© 2001 by The Society of Thoracic Surgeons 0003-4975/01/$20.00Published by Elsevier Science Inc PII S0003-4975(00)02136-6

by on June 6, 2013 ats.ctsnetjournals.orgDownloaded from

of application of the side-clamp or when declamping forthe first 100 patients, then systemic pressure reduction to100 mm Hg was done in the following 208 patients. In theinitial experience, distal and proximal anastomosis weredone sequentially for each saphenous vein graft (SVG)necessitating multiple periods of side-clamping for mul-tiple SVG.

StatisticsResults are expressed as mean 6 standard deviation. Forcategorical variables, groups were compared using thePearson’s x2 test. For continuous variables, the Fisher’sexact test was used.

Results

Demographic data are presented in Table 1. There wereno statistically significant differences between the 2groups except for history of stroke and number of grafts.Postoperative results are presented in Table 2.

IAAD occurred in 3 patients among 308 operated onwithout ECC (0.97%) and 1 patient among 2,723 operatedon under ECC (0.04%). This difference was statisticallysignificant ( p , 0.00001). Operative data and outcome ofIAAD are summarized in Tables 3 and 4. In all cases, 2SVG were performed, and proximal anastomoses usedseparate periods of aortic side-clamping, except in case 1.In this case, because of a dilated ascending aorta, aY-graft was performed to minimize the trauma becauseof aortic side-clamping. Aortic dissection (AD) occurredintraoperatively in 2 cases (cases 2 and 4), and weretreated by immediate aortic replacement with a Dacron

Table 1. Preoperative Data

Variable

Group I,with ECC(n 5 2723)

Group II,OPCAB

(n 5 308)p

Value

Age (y) 62.6 6 9.6 63.5 6 9.9 0.1Male/female (%) 77.2/22.8 75.6/24.4 0.5Diabetes (%) 22.6 20.5 0.3Smoking history (%) 28.7 24.0 0.1History of stroke (%) 6.4 9.7 0.02Low ejection fraction (, 40%) 43.2 45.8 0.3Ejection fraction (%) 53.8 6 14 54.1 6 15 0.7Hypertension (%) 49.5 55.2 0.058Pulmonary disease (%) 7.9 8.1 0.8% mammary artery used 93.8 94.2 0.06No. of grafts 2.8 6 0.7 2.4 6 0.7 0.0001

EEC 5 extracorporeal circulation; OPCAB 5 off-pump coronary ar-tery bypass grafting.

Table 2. Postoperative Data

Variable

Group I,with ECC

(n 5 2,723)

Group II,OPCAB

(n 5 308)p

Value

IABP (%) 3.0 2.9 0.9% infarct (CK-MB . 100 U) 5.4 5.5 0.9Pressor support (. 24 h) (%) 7.5 6.8 0.1Reentry for bleeding (%) 4.8 3.9 0.4Hospital death (%) 2.1 2.6 0.5Length of stay (days) 7.2 6 5.5 6.9 6 7.1 0.3

CK-MB 5 creatine kinase-MB fraction; EEC 5 extracorporeal circu-lation; IABP 5 intraaortic balloon pump; OPCAB, off-pump coro-nary artery bypass grafting.

Table 3. Patient Clinical Parameters and Operative Data During Coronary Artery Bypass Surgery

No. Age Gender Medical HistoryAnginaPectoris

CoronaryAngiogram

(%)EF(%) Operation ECC/OP

OperativeComments

AP DuringASC

(mm Hg)

1 70 M Hypertension;operation forAAA; carotidendarterectomy

Stable LAD: 100CX: 100RCA: 50

62 LIMA—LAD;SVG—D1;SVG—PDA;CX notgraftable

OP Dilated ascendingaorta (4.5-cmdiameter) Y-graft

90/50

2 56 M Hypertension;chronic renalfailure

Unstable LMC: 50LAD: 65CX: 75RCA: 60

57 LIMA—LAD;SVG—OM;SVG—RCA

OP 110/60

3 76 M Hypertension Stable LMS: 50LAD: 50D1: 60OM2: 80RCA: 100

82 LIMA—LAD;SVG—OM2;SVG—PDA

OP 2 Separate side-clamping

120/70

4 70 M Obesity; hemolyticanemia

Unstable LAD: 70OM2: 50PL: 55

35 LIMA—LAD;SVG—OM2;SVG—PL

ECC Thin and friableaorta, 2separate side-clamping

90

AAA 5 abdominal aortic aneurism; AP 5 arterial pressure; ASC 5 aortic side-clamping; CX 5 circumflex artery; D1 5 diagonalartery; ECC 5 extracorporeal circulation; EF 5 ejection fraction; LAD 5 left anterior descending artery; LIMA 5 left internal mammaryartery; LMC 5 left main coronary; LMS 5 left main stem artery; M 5 male; OM 5 obtuse marginal artery; OP 5 off-pump; PDA 5posterior descending artery; PL 5 posterolateral artery; RCA 5 right coronary artery; SVG 5 saphenous vein graft.

118 CHAVANON ET AL Ann Thorac SurgAORTIC DISSECTION WITH OPCAB 2001;71:117–21

by on June 6, 2013 ats.ctsnetjournals.orgDownloaded from

(C.R. Bard, Haverhill, MA) graft under cardiopulmonarybypass to which the SVG were anastomosed in a Y-graftmanner. Both patients were discharged and did well. Theside-clamping in the ECC patient was performed with ablood pressure of 90 mm Hg. In the 2 other patients(cases 1 and 3), aortic dissection occurred postoperativelyand had an unfavorable outcome. In patient 1, AD wasdiagnosed on postoperative day 13 and was promptlybrought to surgery, during which extreme operativedifficulties were encountered because of severe adhe-sions and inflammation. Repair with graft interpositionwas performed under circulatory arrest but weaning ofECC was not tolerated and the patient died of cardiacfailure. In patient 3, cardiorespiratory arrest occurred onpostoperative day 5, and AD was diagnosed on postmor-tem examination. In all cases, macroscopic lesions fromaortic side-clamping were present (Figs 1 and 2). In 3 ofthem, microscopic examinations were performed (Fig 3)(cases 2–4) and showed degeneration of the elastic la-mella in 2 cases (cases 2 and 4), and cystic medial necrosisin 1 (case 2) (Fig 4). Three patients had a history ofhypertension and 1 was associated with dilatation of theascending aorta at the time of surgery. In the otherpatient (case 4), the aorta was found to be friable at thetime of surgery.

Comment

The incidence of acute ascending aortic dissection fol-lowing heart surgery is low with a rate of about 0.12%[1–3]. Among 8,624 cardiac operations with ECC, 10patients presented with a IAAD, of whom 8 were afterCABG including 2 with concomitant valvular surgery [3].Intraoperative dissection was predominant over postop-erative occurrence [2–4]. Acute aortic dissection (AAD)can also occur later after the initial CABG [7, 8], althoughin some cases the mediastinum may be enlarged on thepostoperative chest x-ray film after CABG [9] as in one ofour patients. Prompt recognition and surgical repair areessential to achieve a successful outcome, although insome cases long-term survival without surgery has beenreported [10]. In most observations and in our series,predisposing factors can be identified such as a history ofhypertension [9], atherosclerosis of the aorta, thin dilatedaortic walls, cystic medial necrosis, or inherited disordersof connective tissue, as in spontaneous aortic dissection.In the case of IAAD, the surgical trauma is the maintrigger mechanism in conjunction with pathological con-ditions of the aorta that are often present in the popula-tion undergoing CABG surgery. Many manipulationsmay be the initiating point of the dissection [2, 11]: aorticcannulation; injury at the time of application of the

Table 4. Operative Data and Outcome of Iatrogenic Aortic Dissection

No. Date of AAD Diagnosis Treatment Outcome Comment

1 Postoperative (POD 13) CT-scan, TEE AAD around proximalanastomosis;“Inflammatorymagma,” adhesions111; repair underECC with CA (22°C)

Intraoperative death Initial CABG postoperativeoutcome was uneventfulwith discharge on POD6; macroscopic lesion:tearing of aorta aroundthe SVG

2 Intraoperative afterfirst aortic side-clamping

Macroscopicperoperative

Aortic graftreplacement underfemoro-femoralECC (24°C); Y-SVGimplanted in aorticgraft

Uneventful withdischarge on POD7

Pathology: macroscopy 1.5-cm wide transverselaceration; microscopy:elastic degeneration withcystic medial necrosis

3 POD 5, day of planneddischarge

CRA; autopsy . . . Death Wide mediastinum on POchest roentgenogram;pathology: macroscopy:1.8-cm wide transverselaceration (Fig 3);microscopy: elasticlamella degeneration(Fig 4)

4 Intraoperative afterremoval of aorticside-clamp

Macroscopic;intraoperative

Aortic graftreplacement witharterial femoralcannulation afterunsuccessful repairattempt; Y-SVGimplanted in aorticgraft

Uneventful withdischarge on POD10

Pathology: macroscopy:transverse laceration ofaortic wall; microscopy:elastic lamelladegeneration withoutcystic medial necrosis

AAD 5 acute aortic dissection; CA 5 circulatory arrest; CABG 5 coronary artery bypass graft surgery; CRA 5 cardiorespiratoryarrest; CT 5 computed tomography; ECC 5 extracorporeal circulation; PO 5 postoperative; POD 5 postoperative day; SVG 5saphenous vein graft; TEE 5 transesophageal echocardiography.

119Ann Thorac Surg CHAVANON ET AL2001;71:117–21 AORTIC DISSECTION WITH OPCAB

by on June 6, 2013 ats.ctsnetjournals.orgDownloaded from

cross-clamp, or the side-clamp, creating an intimal tear;and direct injury during suturing of the graft to the aorta,or failure to obtain intima-to-intima approximation. Be-cause OPCABG does not necessitate cannulation andaortic cross-clamping, the risky manipulations are fromlateral clamping that may increase the risk of injurybecause of the pulsatile pattern of arterial pressure.Indeed, uncontrolled hypertension is a major risk factorin the occurrence of aortic clamp trauma [2]. Further-more, in conventional CABG, ECC allows the temporarydecrease in arterial pressure, which is nonpulsatile, to asafe threshold (50 mm Hg) while clamping the aorta,facilitating the placement of the clamp and diminishingthe likelihood of aortic clamp injury and slippage. Thisimportant maneuver is not as readily feasible duringOPCAB and lateral clamping may be hazardous whenpredisposing factors coexist. Consequently, decreasingthe arterial pressure at the time of application andremoval of the aortic side-clamp, with or without tempo-rary partial clamping of the inferior vena cava [12], andmaintaining a low systolic arterial pressure (about100 mm Hg) during the proximal anastomoses with phar-

macological agents may minimize the strain caused bythe clamp on the aorta. Another preventive measure,which may be useful even under ECC, includes the use ofa single side-clamping period for performance of proxi-mal anastomoses. Another alternative is to perform prox-imal anastomosis during a single cross-clamp period as isrecommended in reoperative CABG surgery. If multipleSVG are used in OPCAB, we now perform both proximalanastomoses after the first distal anastomosis using aSVG, then the second distal anastomosis is completed. Ifmore than two SVG grafts are necessary, Y-grafts withvenovenous anastomosis are performed with a running7-0 polypropylene suture.

Avoidance of the greater curvature of the aorta, aclassical site of dissection, for placement of the proximalanastomosis, and preference for the inner portion of theaorta after dissection of the aortopulmonary space, maydecrease the risk of complications. Sequential graftingmay also be used to decrease the number of proximalanastomosis. In high-risk situations where there is un-derlying disease of the aorta, the proximal anastomosiscan be performed on the brachiocephalic artery, or in aend-to-side manner to the internal mammary artery [13].Total arterial revascularization using bilateral pedicled

Fig 1. Intimal trauma after application of aortic sideclamp.

Fig 2. Aortic laceration at the site of proximal anastomosis resultingin aortic dissection and death on postoperative day 5 after off-pumpcoronary artery bypass.

Fig 3. Histological examination showing the laceration of the aorticwall in dissection of the ascending aorta after off-pump coronaryartery bypass surgery (Movat pentachrome stain, original magnifica-tion 3 10).

Fig 4. Microscopic examination showing aortic cystic degenerationof the elastic lamellae and smooth muscle cells with Movat penta-chrome staining in the ascending aorta in the same patient (originalmagnification 3 200).

120 CHAVANON ET AL Ann Thorac SurgAORTIC DISSECTION WITH OPCAB 2001;71:117–21

by on June 6, 2013 ats.ctsnetjournals.orgDownloaded from

mammary artery and gastroepiploic artery could be anideal alternative technique in such cases avoiding ma-nipulation of the aorta altogether [14]. When the aorta isthin or dilated, elective use ECC for CABG may bepreferable allowing performance of proximal anastomo-sis during a single aortic cross-clamp time, or may allowa complementary procedure on the aorta if required.Assessment of aortic disease with epicardial echographymay also be useful in diagnosing aortas at high risk ofdissection [15, 16].

When AAD occurs, establishment of the diagnosisintraoperatively is preferable and associated with a betterprognosis because it permits proceeding to immediaterepair by either interposition of a prosthesis [3] or localrepair as in 4 of 6 patients in Blakeman and coworkers’series [1] and in 11 of 20 cases in the report of Still andcolleagues [2]. Postoperatively, the diagnosis may besuspected by a persistently widened mediastinum, recur-rence of chest pain, peripheral ischemic changes or moresubtle visceral ischemic damage leading to a gradual riseof lactic acid and urea-creatinine ratio. Prompt trans-esophageal echocardiography allows confirmation of thediagnosis, avoids delays in therapeutic care, and guidessurgical strategy. Early postoperative AAD generally re-quires graft replacement of the ascending aorta [1]. Incase of late type A dissection, local repair was feasible inonly 2% of the cases in the series of Gillinov andassociates [8]. Patent vein grafts can be reattached withan “island flap” of ascending aorta to the prosthesis, or anew saphenous vein either interposed or as a new bypasscan be used [8]. Postoperative mortality ranges from 15%to 50% [2, 3, 8]. To avoid this high mortality rate, alter-native techniques have been proposed such as extra-anatomic bypass [17] or catheter fenestration with stent-ing, but some concerns remain about the evolution of thedissected ascending aorta.

LimitationsThe influence of the learning curve on this complicationcannot be ruled out. The small amount of events in bothgroups make absolute conclusions about the relationshipbetween OPCAB and an increased incidence of dissec-tion difficult to establish as does the lack of prospectivefollow-up. However, the careful statistical analysis of thisconsecutive cohort of patients spreads the underreport-ing bias across both groups. No dissections have beenidentified since the end of the study period which may beexplained by an increasing experience in modifying thesurgical technique (avoiding cross-clamping) in high-riskpatients and using precautions as mentioned above.

ConclusionAortic dissection after coronary artery bypass graftingsurgery maybe more frequent in OPCAB than with thetraditional technique under ECC. This suspicion shouldbe verified with a long-term follow-up study of patientsundergoing OPCAB along with the patency assessmentof graft performed with this technique. Meanwhile, at-tention should be given to technical details that mayinfluence the occurrence of IAAD. Careful manipulation

of the aorta with a single side-clamping and control of thearterial pressure should be used to minimize aortictrauma. Patients at risk for this complication shouldundergo alternative techniques without side-clamping ofthe aorta, or undergo CABG with ECC, to prevent thisredoubtable complication.

We thank Dr Andre Couturier for expert statistical analysis, andDr Tack Ki Leung for pathological examination of the specimens.

References

1. Blakeman BM, Pifarre R, Sullivan HJ, et al. Perioperativedissection of the ascending aorta: types of repair. J Card Surg1988;3:9–14.

2. Still RJ, Hilgenberg AD, Akins CW, Daggett WM, BuckleyMJ. Intraoperative aortic dissection. Ann Thorac Surg 1992;53:374–9.

3. Ruchat P, Hurni M, Stumpe F, Fischer AP, von Segesser LK.Acute ascending aortic dissection complicating open-heartsurgery: cerebral perfusion defines the outcome. Eur J Car-diothorac Surg 1998;14:449–52.

4. Murphy DA, Craver JM, Jones EL, et al. Recognition andmanagement of ascending aortic dissection complicatingcardiac surgical operations. J Thorac Cardiovasc Surg 1983;85:247–56.

5. Cartier R. Systematic off-pump coronary artery revasculariza-tion: experience of 275 cases. Ann Thorac Surg 1999;68:1494–7.

6. Dagenais F, Perrault LP, Cartier R, et al. Beating heartcoronary artery bypass grafting: technical aspects and re-sults in 200 patients. Can J Cardiol 1999;15:867–72.

7. Yaku H, Fermanis GG, Macauley J, Horton DA. Dissection ofthe ascending aorta: a late complication of coronary arterybypass grafting. Ann Thorac Surg 1996;62:1834–5.

8. Gillinov AM, Lytle BW, Kaplon RJ, Casselman FP, Black-stone EH, Cosgrove DM. Dissection of the ascending aortaafter previous cardiac surgery: differences in presentationand management. J Thorac Cardiovasc Surg 1999;117:252–60.

9. Bopp P, Perrenoud JJ, Periat M. Dissection of ascendingaorta. Rare complication of aortocoronary venous bypasssurgery. Br Heart J 1981;46:571–3.

10. Horowitz RS, Kitchen JG III. Aortic dissection followingcoronary arterial bypass graft surgery. Chest 1981;80:749–51.

11. Connolly MW. Aortoatriocaval cannulation for cardiopul-monary bypass. In: Mora CT, ed. Cardiopulmonary bypass.Principles and techniques of extracorporeal circulation. NewYork: Springer-Verlag, 1995:257–63.

12. Dagenais F, Cartier R. Pulmonary hypertension during beat-ing heart coronary surgery: intermittent inferior vena cavasnaring. Ann Thorac Surg 1999;68:1094–5.

13. Peigh PS, DiSesa VJ, Collins JJ Jr, Cohn LH. Coronary bypassgrafting with totally calcified or acutely dissected ascendingaorta. Ann Thorac Surg 1991;51:102–4.

14. Calafiore AM, Teodori G, Di Giammarco G, et al. Multiplearterial conduits without cardiopulmonary bypass: earlyangiographic results. Ann Thorac Surg 1999;67:450–6.

15. Baribeau YR, Wesbrook BM. Intraoperative epicardial echo-cardiography. In: Izzat MB, Sanderson JE, St. John SuttonMG, eds. Echocardiography in adult cardiac surgery. Ox-ford, UK: ISIS Medical Media Ltd, 1999:223–9.

16. Wareing TH, Davila-Roman VG, Barzilai B, Murphy SF,Kouchoukos NT. Management of the severely atheroscle-rotic ascending aorta during cardiac operations. A strategyfor detection and treatment. J Thorac Cardiovasc Surg 1992;103:453–62.

17. Pappas D, Hines GL, Gennaro M, Hartman A. Delayediatrogenic aortic dissection from coronary bypass managedwith extraanatomic bypass. J Thorac Cardiovasc Surg 1998;115:947–9.

121Ann Thorac Surg CHAVANON ET AL2001;71:117–21 AORTIC DISSECTION WITH OPCAB

by on June 6, 2013 ats.ctsnetjournals.orgDownloaded from

2001;71:117-121 Ann Thorac SurgPierre Pagé and Louis P. Perrault

Olivier Chavanon, Michel Carrier, Raymond Cartier, Yves Hébert, Michel Pellerin, aortocoronary bypass surgery?

Increased incidence of acute ascending aortic dissection with off-pump

& ServicesUpdated Information

http://ats.ctsnetjournals.org/cgi/content/full/71/1/117including high-resolution figures, can be found at:

References http://ats.ctsnetjournals.org/cgi/content/full/71/1/117#BIBL

This article cites 15 articles, 12 of which you can access for free at:

Citations http://ats.ctsnetjournals.org/cgi/content/full/71/1/117#otherarticles

This article has been cited by 23 HighWire-hosted articles:

Subspecialty Collections

eryhttp://ats.ctsnetjournals.org/cgi/collection/minimally_invasive_surg

invasive surgeryMinimally http://ats.ctsnetjournals.org/cgi/collection/great_vessels

Great vesselsfollowing collection(s): This article, along with others on similar topics, appears in the

Permissions & Licensing

.healthpermissions@elsevier.comemail: 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 reprints@elsevier.com

For information about ordering reprints, please email:

by on June 6, 2013 ats.ctsnetjournals.orgDownloaded from