A New Perspective in Comparing Injuries Caused by Short-Duration External and Internal Forces in Saphenous Vein


  • Emine Seyma Denli Yalvac Department of Cardiovascular Surgery, Göztepe Education and Research Hospital, Istanbul Medeniyet University, Istanbul, Turkey
  • Alev Cumbul Department of Histology and Embryology,Yeditepe University, Istanbul, Turkey
  • Unal Uslu Department of Histology and Embryology, Faculty of Medicine, Göztepe Education and Research Hospital, Istanbul Medeniyet University, Istanbul, Turkey
  • Erdem Soztutar Department of Anatomy, Faculty of Medicine, Yeditepe University, Istanbul, Turkey
  • Edibe Bilisli Department of Anatomy, Faculty of Medicine, Yeditepe University, Istanbul, Turkey
  • Naci Balak Department of Neurosurgery, Göztepe Education and Research Hospital, Istanbul Medeniyet University, Istanbul, Turkey https://orcid.org/0000-0002-2395-0004




Background: Great saphenous vein (GSV) graft failure is one of the major reasons for repeat bypass grafting. A comparison of the effects of simultaneous, short-duration, externally squeezing and internally distending forces on the same segment of ex-vivo human GSV has not yet been published, although similar studies have compared the experimental injury of different ex-vivo human veins.

Methods: Approximately 8-cm-long segments of GSV were harvested from each of the 15 patients. For each specimen, one end of the vein piece was occluded at a distance of 1 cm with an external cross-clamp for 5 min and the other end was similarly occluded at a distance of 1 cm by an endoluminal balloon. The middle sections of the veins, which were not occluded by any means, were taken as the control group. Two histologists, who were blinded to the groups, graded the hematoxylin and eosin (H&E) and Weigert-Van Gieson (WVG) stained sections semi-quantitatively and performed the
histomorphometric measurements.

Results: The result of the histopathological evaluation of the intima layer showed that the microscopic scoring of lesions in the balloon group was significantly higher than that in the clamp and control groups (5.16 ± 1.32, 3.83 ± 0.75, and 1.00 ± 1.09, respectively, P < .001). In the adventitia layer, this level of scoring increased more in the clamp group than in the balloon and control groups (5.16 ± 1.16, 3.00 ± 0.89, and 0.16 ± 0.40, respectively, P < .001).

Conclusion: Both the endoluminal balloon and external clamp techniques have harmful effects on the vein wall. Studying different kind of forces on different veins cannot provide us with reliable comparisons.


Acland RD. 1980. Microsurgery practice manual. St Louis: The C.V. Mosby Company. pp 65-69.

Alrawi SJ, Balaya F, Raju R, Cunningham Jr J, Acinapura A. 2001. A comparative study of endothelial cell injury during open and endoscopic saphenectomy: an electron microscopic evaluation. Heart Surg Forum 4:120-7.

Babin-Ebell J, Gimpel-Henning K, Sievers HH, Scharfschwerdt M. 2010. Influence of clamp duration and pressure on endothelial damage in aortic cross-clamping. Interact Cardiovasc Thorac Surg 10:168-71.

Bourassa MG, Campeau L, Lesperance J, Grondin CM. 1982. Changes in grafts and coronary arteries after saphenous vein aortocoronary bypass surgery: results at repeat angiography. Circulation 65:90-7.

Cook RC, Crowley CM, Hayden R, et al. 2004. Traction injury during minimally invasive harvesting of the saphenous vein is associated with impaired endothelial function. J Thorac Cardiovasc Surg 127:65-71.

Davies M, Hagen P-O. 2011. Reprinted article: Pathophysiology of vein graft failure: a review. Eu J Vasc Endovasc Surg 42:S19-29.

Donaldson MC, Mannick JA, Whittemore AD. 1992. Causes of primary graft failure after in situ saphenous vein bypass grafting. J Vasc Surg 15:113-18; discussion 118-120.

Dreifaldt M, Mannion JD, Bodin L, et al. 2013. The no-touch saphenous vein as the preferred second conduit for coronary artery bypass grafting. Ann Thorac Surg 96:105-11.

Eddleman C, Getch C, Bendok B, Batjer H. 2010. Saphenous vein grafts for high-flow cerebral revascularization. In Abdulrauf SI (ed): Cerebral Revascularization: Techniques in Extracranial-to-Intracranial Bypass Surgery. Elsevier Health Sciences, Philadelphia, pp 125-8.

Gabeler EE, Gussenhoven EJ, van Urk H, et al. 2002. A comparison of balloon injury models of endovascular lesions in rat arteries. BMC cardiovascular disorders Sep 27;2:16.

Hashmi SF, Krishnamoorthy B, Critchley WR, et al. 2015. Histological and immunohistochemical evaluation of human saphenous vein harvested by endoscopic and open conventional methods. Interact Cardiovasc Thorac Surg 20:178-85.

Horvath KD, Gray D, Benton L, Hill J, Swanstrom LL. 1998. Operative outcomes of minimally invasive saphenous vein harvest. Am J Surg 175:391-5.

Johnson JL, van Eys GJ, Angelini GD, George SJ. 2001. Injury induces dedifferentiation of smooth muscle cells and increased matrix-degrading metalloproteinase activity in human saphenous vein. Arterioscler Thromb Vasc Biol 21:1146-51.

Kaplan S, Bisleri G, Kılınç K, Çobanoğlu A, Öz MC. 2013. Effects of harvesting technique on endothelial inflammation and nitric oxide production in saphenous vein grafts. Türk Göğüs Kalp Damar Cerrahisi Dergisi 21:31-6.

Karabulut H, Karabulut O, Arbak S, et al. 1998. Endothelial damage in preparation of saphenous vein used as graft in coronary bypass surgery: Light and electron microscopic examination. [Koroner Bypass Cerrahisinde Greft Olarak Kullanılan Safen Veninin Hazırlanmasında endotel Hasarı: Işık ve Elektron Mikroskopik Inceleme]. Türk Kardiyol Dern Arş 26:416-424 [Turkish].

Karimi A, Navidbakhsh M, Kudo S. 2015. A comparative study on the mechanical properties of the healthy and varicose human saphenous vein under uniaxial loading. J Med Eng Technol 39:490-7.

Kopjar T, Dashwood MR. 2016. Endoscopic versus “no-touch” saphenous vein harvesting for coronary artery bypass grafting: a trade-off between wound healing and graft patency. Angiology 67:121-32.

Krayenbühl H. 1977. Comments on the history of external-internal anastomosis for cerebral ischemia. In Schmiedek P, Gratzl O, Spetzler RF. Microsurgery for Stroke. Springer-Verlag, New York, pp 3-7.

Kurdal AT, Ustundag N, Guven A, et al. 2009. Protection of saphenous vein graft from arterial pressure: an experimental study. Thorac Cardiovasc Surg 57:333-8.

Kwok MWT, Lau RHL, Underwood MJ. 2016. Coronary artery bypass surgery: on-pump and off-pump techniques. In Ţintoiu IC, Underwood MJ, Cook SP, Kitabata H, Abbas A (eds): Coronary Graft Failure: State of the Art. Springer International Publishing, Switzerland.

Manship LL, Moore WM, Bynoe R, Bunt TJ. 1985. Differential endothelial injury caused by vascular clamps and vessel loops. II. Atherosclerotic vessels. Am Surg 51:401-6.

Meng X, Mavromatis K, Galis ZS. 1999. Mechanical stretching of human saphenous vein grafts induces expression and activation of matrix-degrading enzymes associated with vascular tissue injury and repair. Experimental and molecular pathology 66:227-37.

Moritz A, Grabenwoger F, Raderer F, et al. 1993. Use of varicose veins as arterial bypass grafts. Cardiovasc Surg 1:508-12.

Neufang A, Espinola-Klein C, Savvidis S, et al. 2018. External polytetrafluoroethylene reinforcement of varicose autologous vein grafts in peripheral bypass surgery produces durable bypass function. J Vasc Surg 67:1778-87.

Osgood MJ, Hocking KM, Voskresensky IV, et al. 2014. Surgical vein graft preparation promotes cellular dysfunction, oxidative stress, and intimal hyperplasia in human saphenous vein. J Vasc Surg 60:202-11.

Perek B. 2016. Early CABG Failure. In Ţintoiu I, Underwood M, Cook S, Kitabata H, Abbas A (eds): Coronary Graft Failure: State of the Art. Springer International Publishing, Switzerland, pp 131-8.

Pilmane M, Ozoliņa L, Ābola Z, et al. 2011. Growth factors, their receptors, neuropeptide-containing innervation, and matrix metalloproteinases in the proximal and distal ends of the esophagus in children with esophageal atresia. Medicina 47:453.

Pounds L, Killewich L. 2014. Venous physiology. In Cronenwett J, Johnston K (eds): Rutherford’s vascular surgery. Saunders Elsevier, Philadelphia, pp 150-62.

Rousou LJ, Taylor KB, Lu X-G, et al. 2009. Saphenous vein conduits harvested by endoscopic technique exhibit structural and functional damage. Ann Thorac Surg 87:62-70.

Sayers RD, Watt PA, Muller S, Bell PR, Thurston H. 1992. Endothelial cell injury secondary to surgical preparation of reversed and in situ saphenous vein bypass grafts. Eur J Vasc Surg 6:354-61.

Souza DS, Dashwood MR, Tsui JC, et al. 2002. Improved patency in vein grafts harvested with surrounding tissue: results of a randomized study using three harvesting techniques. Ann Thorac Surg 73:1189-95.

Stone D, Walsh D. 2014. Local complications: graft thrombosis. In Cronenwett J, Johnston K (eds): Rutherford’s vascular surgery. 8th edn. Saunders Elsevier, Philadelphia, pp 683-703.

Sumpio B, Chin J. 2014. Vessel wall biology. In Cronenwett J, Johnston K (eds): Rutherford’s vascular surgery. Saunders Elsevier, Philadelphia, pp 34-48.

Tajima H, Araki Y, Izumi T, et al. 2017. Coiling of a ruptured large internal carotid artery aneurysm via extracranial-intracranial saphenous vein bypass graft just after proximal ligation of the internal carotid artery. World neurosurgery 98:879. e871-79.

Wali MA, Dewan M, Eid RA. 2003. Histopathological changes in the wall of varicose veins. Int Angiol 22:188-93.

Wise ES, Hocking KM, Luo W, et al. 2016. Traditional graft preparation decreases physiologic responses, diminishes viscoelasticity, and reduces cellular viability of the conduit: A porcine saphenous vein model. Vasc Med 21:413-21.

Wise ES, Hocking KM, Evans BC, et al. 2017. Unregulated saphenous vein graft distension decreases tissue viscoelasticity. Perfusion 32:489-94.

Woodward LC, Antoniades C, Taggart DP. 2016. Intraoperative vein graft preservation: What is the solution? Ann Thoracic Surg 102:1736-46.

World Medical Association. 2013. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. Jama 310:2191.

Yaşargil M. 1967. Experimental small vessel surgery in the dog including patching and grafting of cerebral vessels and the formation of functional extra-intracranial shunts. In Donaghy R, Yaşargil M (eds): Micro-Vascular Surgery. Georg Thieme Verlag, Stuttgart, pp 87-126.

Yaşargil M, Krayenbuhl H, Jacobson J. 1970. Microsurgical arterial reconstruction. Surgery 67:221-33.



How to Cite

Denli Yalvac, E. S., Cumbul, A., Uslu, U., Soztutar, E., Bilisli, E., & Balak, N. (2019). A New Perspective in Comparing Injuries Caused by Short-Duration External and Internal Forces in Saphenous Vein. The Heart Surgery Forum, 22(2), E063-E069. https://doi.org/10.1532/hsf.2303