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Published as doi: 10.1096/fj.07-096586.
 (The FASEB Journal. 2008;22:2084-2089.)
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Tissue engineering of a hybrid bypass graft for coronary and lower limb bypass surgery

S. T. Rashid*, B. Fuller*, G. Hamilton{dagger} and A. M. Seifalian*,1

* Biomaterial and Tissue Engineering Centre (BTEC), Royal Free and University College Medical School, University College London, London, UK; and

{dagger} Vascular Unit, Royal Free Hampstead National Health Service Trust, London, UK

1Correspondence: Biomaterials and Tissue Engineering Centre, Academic Division of Surgical and Interventional Sciences, University College London, Rowland Hill Street, London NW3 2PF, UK. E-mail: a.seifalian{at}ucl.ac.uk


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Tissue-engineered blood vessels have largely relied on inelastic scaffolds or biological solutions with uncertain long-term in vivo durability. In this report we present for the first time a hybrid tissue-engineered bypass graft consisting of an elastic scaffold of compliant poly(carbonate-urea)urethane (CPU), incorporated with human smooth muscle cells (SMCs) and endothelial cells (ECs) from the same human source. Human vascular SMCs and ECs were extracted from umbilical cord vessels. The effect of shear stress preconditioning on cell retention on the hybrid bypass graft was investigated under pulsatile arterial flow conditions. Retention of ECs seeded onto CPU precoated with SMCs was significantly improved by a period of shear stress preconditioning, especially when the stress incrementally increased. This is probably because the mechanical stimuli orient cells and increase the release of matrix proteins and attachment factors. The stage is now set for developing a hybrid graft for in vivo studies.—Rashid, S. T., Fuller, B., Hamilton, G., and Seifalian, A. M. Tissue engineering of a hybrid bypass graft for coronary and lower limb bypass surgery.


Key Words: compliance • polyurethanes • shear stress • smooth muscle cell • endothelial cell


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
ATHEROSCLEROSIS OF THE ARTERIES is the largest cause of mortality and morbidity in the Western world (1) . When occluded vessels are not amenable to angioplasty or stenting, the only option is surgical bypass of coronary artery and lower-limb vessels. The preferred bypass material is the patient’s own arteries or veins, but in approximately one-third of patients this source proves inadequate or unsuitable (2) . Prosthetic materials such as polyethylene terephthalate (Dacron) and expanded polytetrafluoroethylene (ePTFE), especially when the vessel diameter is under 5 mm, have lower patency and higher infection rates (3 , 4) .

The two important causes of the high failure rates in current commercially available prosthetic grafts are, first, mechanical failings, such as compliance mismatch between viscoelastic native artery and stiff prosthetic graft (5 6 7) , and, second, biological failings, including absence of antithrombogenic properties and living, responsive tissue adaptive to changes in the local environment (8) .

In an attempt to improve this situation, research has focused on three strategies: 1) developing newer types of prosthetic material, 2) making the existing prosthetic materials more natural by lining the lumen of the graft with endothelial cells (ECs), and 3) growing completely new vascular conduits from autogenous material, using tissue-engineering techniques.

Our laboratory has developed a graft made of a compliant poly(carbonate-urea)urethane (CPU), which has a honeycomb structure that allows it to maintain compliance similar to that of human artery (9) and pulsatile flow in vivo through a mechanism of wall compression that accommodates increases in volume without the need for external dilation. The graft has undergone in vitro degradation tests and has been implanted in a dog model for 36 months, demonstrating very high biostability (10 11 12) . This graft is already in use as an arteriovenous (A-V) fistula for hemodialysis access and is undergoing a phase I clinical trial as a peripheral vascular bypass graft (10) . CPU has been shown to have superior ability to attach ECs, which can be further improved by prelining the graft with attachment factors such as collagen and fibronectin (9 , 13 14 15) .

Our laboratory is in the process of developing a hybrid graft that consists of a CPU, smooth muscle cells (SMCs), and ECs sourced from the same patient. We have previously demonstrated that SMC attachment and retention to the CPU can be enhanced with an attachment factor and the use of "preconditioning," respectively (16) .

Preconditioning occurs when a vascular construct is exposed in vitro to pulsatile flow and pressure. This approach has been shown to enhance cell proliferation, tissue formation, and mechanical properties in a variety of tissue-engineered vascular constructs and specifically enhances EC retention, viability, and morphology (17 18 19) . Some evidence also indicates that incremental increases in the shear stress during preconditioning is superior to constant low shear stress (20) . Furthermore, studies have shown that EC attachment can be enhanced by lining synthetic grafts with SMCs first (21) .

In this study we describe the further development of a hybrid tissue-engineered graft using CPU as a scaffold with incorporation of SMCs and ECs. Therefore, the aims of this study were to source both SMCs and ECs from the same human vessel and examine the effect on EC retention of different shear stress preconditioning techniques.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Material chemistry and manufacture of CPU
The chemistry and manufacture of this graft have been published (22) . Briefly, dry polycarbonate polyol was placed in a 250 ml reaction flask equipped with a mechanical stirrer and nitrogen inlet. The polyol was heated to 60°C, and then 9.1 g of flake 4,4'-methylene bisphenyl isocyanate (MDI) was added and reacted with the polyol, under nitrogen, to form a prepolymer. Dry dimethylacetamide (100 g) was added slowly to the prepolymer to form a solution. Chain extension of the prepolymer was performed by the drop-wise addition of a mixture of ethylenediamine and diethylamine in dry dimethylacetamide. After completion of the chain extension, butanol in 2 g of dimethylacetamide was added to the polymer solution. The CPU polymers were then extruded via low temperature cast coagulation. This methodology allows the graft structure to mimic the compliance of the host artery. CPU can, therefore, be manufactured to reflect the variations in arterial compliance across disease states, age groups, and arterial sites. This work was performed in collaboration with Credent Ltd, Wrexham, UK.

Extraction of SMCs and ECs
A combined extraction procedure to extract both ECs and SMCs from the same vessel was developed from previously established methodologies. EC extraction from human umbilical vein used the well-established cannulation method (23) , following a previously described in-house protocol (14) . Similarly, human umbilical vein and arterial SMCs were extracted using a novel enzymatic extraction process developed in-house (16 , 24) . The collagenase was from Roche Diagnostics GmbH (Roche Applied Science, Nonnenwald, Penzberg, Germany). All other chemicals were from the Sigma-Aldrich Company Ltd. (Gillingham, Dorset, UK).

Preconditioning experiments
For both experiments, CPU segments were first lined with 1 x 105 SMC/cm2 and preconditioned at low shear stress for 1 wk in a flow circuit setup, as described previously (16) . The effect of both constant and incremental preconditioning on EC retention was then assessed. Extracted ECs were radiolabeled as per our previously described protocol, using 111In-oxine (Amersham International, Amersham, Bucks, UK) at 1.8 MBq/106 cells (25) . After this procedure, radiolabeled ECs were again seeded onto the CPU lengths at 1 x 105 EC/cm2, rotated for a period of 1 h, and left for a day in static culture to allow cell attachment.

Static vs. constant preconditioning
Half the grafts were left in static culture while the other half were preconditioned in the flow circuit at low shear stress (1–2 dyne/cm2). In both experiments, the grafts were incubated at 37°C and 5% CO2.

After 2 h, all the grafts were put into a pulsatile flow circuit under arterial flow and pressure, with a consequent high shear stress (25 dyne/cm2); dynamic scintigraphy images were acquired using a gamma camera as per the method previously described (14 , 16) . Briefly, radioactivity from the 111In-oxine-labeled cells was measured using a gamma camera scanner linked to an image-processing system. The initial 6 images were each acquired over 5 min, with 22 subsequent images acquired over a 15-min span and used to generate time-activity curves corrected for background, spontaneous indium leakage, and isotope decay (half-life of 111In=68 h). Cell attachment (CA) with respect to time was calculated from the following equation:

Formula
where tn is time (min), t0 is the time point immediately before exposure to full arterial shear flow on the gamma camera, and CPMG and CPMB are counts per minute over the region of interest area on graft and background, respectively, computed from analysis of dynamic scintigraphy images. Grafts were perfused for 8 h.

After the flow circuit data were collected, segments of grafts were sent for analysis using scanning electron microscopy (SEM). Six grafts comprised each experiment.

Constant vs. incremental preconditioning
The above experiment was repeated, but this time by comparing constant-but-low preconditioning over a week with incremental preconditioning, whereby after 3 days the shear stress was increased by increasing the flow in the circuit. To increase the flow, the circuit was set up with the modification enabling splitting of flow shown in Fig. 1 .


Figure 1
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  		Figure 1. Splitting flow circuit. By clamping and unclamping the lower arm of the flow circuit, flow can be varied through the upper arm between half and full flow.

For the first 3 days, the arm without bioreactors was clamped to ensure identical flow throughout all bioreactors. Then, after 3 days, the clamp was removed and the flow was doubled. Therefore, those bioreactors in the split part of the circuit received constant flow and shear stress (1–2 dyne/cm2), but those bioreactors positioned after the two arms of the split in the circuit had reunited then had doubled flow and shear stress. After 1 wk, the circuit was again set up with arterial flow, pressure, and shear stress (25 dyne/cm2), with cell retention again measured dynamically on a gamma camera.

After completion of the shear flow experiment, the grafts were sent for SEM visualization of the surface. Each group of the experiment consisted of 5 grafts.

Data analysis and statistical methods
Data are presented with mean ± SD. For each of the preconditioning experiments, the initial values of absolute radioactive levels between the two groups of preconditioned grafts were compared using the 2-tailed t test. For the time activity–retention data, at each time point the two groups were compared using the Mann-Whitney test. Furthermore, the two curves were then compared using a 2-way ANOVA.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Preconditioning experiments
Before exposure of the cells to the high shear force of arterial pulsatile blood flow, no significant difference was found in cell retention, as determined by radioactivity levels between the two groups of grafts in either experiment.

Static vs. constant preconditioning
Figure 2 shows that, on commencement of the pulsatile flow circuit, the percentage of original radioactivity was significantly lower in the static grafts (82.2±3.1) compared with the preconditioned grafts (91.0±3.8) after 150 min (P=0.0286; Mann-Whitney). At the end of the study period of 8 h, the values had barely begun to plateau for both the static and preconditioned groups. However, a significant difference was found between the final percentage values, with a mean of 45.6 ± 2.3 for the static group and 67.4 ± 4.0 for the preconditioned group (P=0.0286; Mann-Whitney). The two curves were significantly different (P=0.0005; 2-way ANOVA). The r2 values for the lines of best fit are 0.9711 for the static group and 0.8910 for the constant preconditioning group. Figure 3 shows SEM images of the two groups, reflecting the greater cell coverage for the constant preconditioning group compared to the static group.


Figure 2
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  		Figure 2. Effect of preconditioning on EC retention to CPU. All values are means ± SD; n = 6.


Figure 3
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  		Figure 3. SEM images of SMC–EC CPU grafts: preconditioned (A) and static (B); x220. Scale bars = 100 µm.

Constant vs. incremental preconditioning
Figure 4 shows that, on commencement of the pulsatile flow circuit, the percentage of original radioactivity was significantly lower in the constantly preconditioned grafts (64.2±7.7) compared with the incrementally preconditioned grafts (76.8±1.5) after 255 min (P=0.0159; Mann-Whitney). At the end of the study period of 8 h, the values had begun to plateau for both groups. However, a significant difference was noted between the final percentage values, with a mean of 56.8 ± 8.9 for the constant group and 71.8 ± 2.7 for the incrementally preconditioned group (P=0.0159; Mann-Whitney). The two curves were significantly different (P=0.0014; 2-way ANOVA). The r2 values for the lines of best fit are 0.5158 for the constant group and 0.8256 for the incremental group. Figure 5 shows an SEM image of the cells on an incrementally preconditioned graft, with good cell coverage of the graft.


Figure 4
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  		Figure 4. Effect of variations in preconditioning on EC retention to CPU. All values are means ± SD; n = 5.


Figure 5
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  		Figure 5. SEM image of SMC-EC CPU graft: incrementally preconditioned CPU; x160. Scale bar = 125 µm.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
We have demonstrated the feasibility of developing a hybrid graft composed of a compliant scaffold with human SMCs and ECs harvested from the same vessel. Much work in the literature shows that cells simply wash off grafts when exposed to pulsatile flow and the high pressures of the arterial circulation. It is known, though, that mechanical stress orients cells and the extracellular matrix (ECM) both in vitro or in vivo (26 27 28 29 30) . Pulsatile blood flow results in a mechanical stimulation composed of hydrostatic pressure, tangential shear stress, and circumferential stretch relaxation (30 , 31) . ECs, because of their contact with flowing blood or medium, are exposed to all three forces (31 , 32) . Furthermore, exposure to shear stress has been shown to enhance EC attachment, retention, and differentiation, as well as being a critical factor in the biological regulatory function of ECs (33 34 35) . Both shear stress and cyclic strain increase EC proliferation and the production of ECM molecules such as collagen and fibronectin (31 , 36) . SMC proliferation also is enhanced by shear stress (37) .

We used these principles in the flow circuit developed in-house to precondition CPU grafts lined with cells at pulsatile subarterial pressures and flows. Using 111In radiolabeling of cells and following the radioactivity dynamically of grafts on a gamma camera, it was established that preconditioning significantly improves cellular retention once the cells on grafts are exposed to full arterial pressures and flow rates. This benefit can occur with as little as 2 h of preconditioning, although this time period means that after 8 h at arterial pressures and flows, a plateau level of cell retention was not established, which suggests that preconditioning needs to be done for longer in order to be truly effective in the long term. This finding is indeed demonstrated by the second flow circuit experiment, with constant preconditioning achieving a plateau level after a week-long preconditioning time. This can be explained by the fact that cell attachment occurs in four overlapping stages, beginning with cell attachment, which occurs within seconds to minutes. This allows cells to withstand gentle shear forces, without which cells could easily be rinsed off a surface. Then cells flatten as the cell membrane spreads to take its characteristic shape. Third, actin is organized into microfilament bundles, also known as stress fibers. Finally focal adhesions or contacts areformed, consisting of clustered integrins and other transmembrane, membrane-associated, and cytosolic molecules, which link ECM molecules to the cell’s actin cytoskeleton (38) . It is notable that previous studies have shown that a layer of SMCs itself enhances the retention of ECs (21 , 39) .

Furthermore, a regimen of incrementally increasing preconditioning and shear stress further enhances the retention of ECs when exposed to full arterial pressures and flow rates. This finding concurs with other studies in the literature showing that incremental preconditioning enhances retention of cells more than constant preconditioning at low shear stress (20) . It seems that such a regimen is better at preparing the attached cells for the disruption caused by full arterial pressures and flows. By gently increasing the shear stress and cyclic strain, cells can develop the ECM and adhesion molecules required to attach to each other and the scaffold surface without succumbing to the detachment forces of circulating medium.

Studies have also shown that exposure of tissue-engineered vessels to the mechanical stimulation of pulsatile flow increases mechanical strength of the constructs, as measured by parameters such as burst pressure (18 , 19 , 40 41 42) . This point is critical if implanted vessels are to avoid aneurysmal dilation and ultimate rupture once exposed to long-term arterial blood pressures. The optimum conditions for the preconditioning are still to be defined, but some propose that the ideal for tissue-engineered vessels may actually be fetal conditions (43) , where the high pulse rate (165 beats per minute) has been shown to enhance collagen deposition and ECM turnover (44) .


   ACKNOWLEDGMENTS
 
S.T.R. received grants from Freemedic Ltd., UCL.

Received for publication September 3, 2007. Accepted for publication December 6, 2007.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. World Health Organization (1999) World Health Organization: The World Health Report 1999 World Health Organization Geneva, Switzerland. 1-1-1999
  2. Kannan, R. Y., Salacinski, H. J., Butler, P. E., Hamilton, G., Seifalian, A. M. (2005) Current status of prosthetic bypass grafts: a review. J. Biomed. Mater. Res. B Appl. Biomater. 74,570-581[Medline]
  3. Bennion, R. S., Williams, R. A., Stabile, B. E., Fox, M. A., Owens, M. L., Wilson, S. E. (1985) Patency of autogenous saphenous vein versus polytetrafluoroethylene grafts in femoropopliteal bypass for advanced ischemia of the extremity. Surg. Gynecol. Obstet. 160,239-242[Medline]
  4. Abbott, W. M., Callow, A., Moore, W., Rutherford, R., Veith, F., Weinberg, S. (1993) Evaluation and performance standards for arterial prostheses. J. Vasc. Surg. 17,746-756[CrossRef][Medline]
  5. Greenwald, S. E., Berry, C. L. (2000) Improving vascular grafts: the importance of mechanical and haemodynamic properties. J. Pathol. 190,292-299[CrossRef][Medline]
  6. Salacinski, H. J., Goldner, S., Giudiceandrea, A., Hamilton, G., Seifalian, A. M., Edwards, A., Carson, R. J. (2001) The mechanical behavior of vascular grafts: a review. J. Biomater. Appl. 15,241-278[Abstract/Free Full Text]
  7. Thakrar, R. R., Patel, V. P., Hamilton, G., Fuller, B. J., Seifalian, A. M. (2006) Vitreous cryopreservation maintains the viscoelastic property of human vascular grafts. FASEB J. 20,874-881[Abstract/Free Full Text]
  8. Parikh, S. A., Edelman, E. R. (2000) Endothelial cell delivery for cardiovascular therapy. Adv. Drug. Deliv. Rev. 42,139-161[CrossRef][Medline]
  9. Tai, N. R., Salacinski, H. J., Edwards, A., Hamilton, G., Seifalian, A. M. (2000) Compliance properties of conduits used in vascular reconstruction. Br. J. Surg. 87,1516-1524[CrossRef][Medline]
  10. Seifalian, A. M., Salacinski, H. J., Tiwari, A., Edwards, A., Bowald, S., Hamilton, G. (2003) In vivo biostability of a poly(carbonate-urea)urethane graft. Biomaterials 24,2549-2557[CrossRef][Medline]
  11. Tiwari, A., Salacinski, H., Seifalian, A. M., Hamilton, G. (2002) New prostheses for use in bypass grafts with special emphasis on polyurethanes. Cardiovasc. Surg. 10,191-197[CrossRef][Medline]
  12. Salacinski, H. J., Tai, N. R., Carson, R. J., Edwards, A., Hamilton, G., Seifalian, A. M. (2002) In vitro stability of a novel compliant poly(carbonate-urea)urethane to oxidative and hydrolytic stress. J. Biomed. Mater. Res. 59,207-218[CrossRef][Medline]
  13. Stansby, G., Berwanger, C., Shukla, N., Schmitz-Rixen, T., Hamilton, G. (1994) Endothelial seeding of compliant polyurethane vascular graft material. Br. J. Surg. 81,1286-1289[CrossRef][Medline]
  14. Giudiceandrea, A., Seifalian, A. M., Krijgsman, B., Hamilton, G. (1998) Effect of prolonged pulsatile shear stress in vitro on endothelial cell seeded PTFE and compliant polyurethane vascular grafts. Eur. J. Vasc. Endovasc. Surg. 15,147-154[CrossRef][Medline]
  15. Salacinski, H. J., Punshon, G., Krijgsman, B., Hamilton, G., Seifalian, A. M. (2001) A hybrid compliant vascular graft seeded with microvascular endothelial cells extracted from human omentum. Artif. Organs 25,974-982[CrossRef][Medline]
  16. Rashid, S. T., Salacinski, H. J., Button, M. J., Fuller, B., Hamilton, G., Seifalian, A. M. (2004) Cellular engineering of conduits for coronary and lower limb bypass surgery: role of cell attachment peptides and pre-conditioning in optimising smooth muscle cells (SMC) adherence to compliant poly(carbonate-urea)urethane (MyoLink trademark) scaffolds. Eur. J. Vasc. Endovasc. Surg. 27,608-616[CrossRef][Medline]
  17. Hoerstrup, S. P., Zund, G., Sodian, R., Schnell, A. M., Grunenfelder, J., Turina, M. I. (2001) Tissue engineering of small caliber vascular grafts. Eur. J. Cardiothorac. Surg. 20,164-169[Abstract/Free Full Text]
  18. Niklason, L. E., Gao, J., Abbott, W. M., Hirschi, K. K., Houser, S., Marini, R., Langer, R. (1999) Functional arteries grown in vitro. Science 284,489-493[Abstract/Free Full Text]
  19. Niklason, L. E., Abbott, W., Gao, J., Klagges, B., Hirschi, K. K., Ulubayram, K., Conroy, N., Jones, R., Vasanawala, A., Sanzgiri, S., Langer, R. (2001) Morphologic and mechanical characteristics of engineered bovine arteries. J. Vasc. Surg. 33,628-638[CrossRef][Medline]
  20. Kaushal, S., Amiel, G. E., Guleserian, K. J., Shapira, O. M., Perry, T., Sutherland, F. W., Rabkin, E., Moran, A. M., Schoen, F. J., Atala, A., Soker, S., Bischoff, J., Mayer, J. E., Jr (2001) Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat. Med. 7,1035-1040[CrossRef][Medline]
  21. Yu, H., Dai, W., Yang, Z., Kirkman, P., Weaver, F. A., Eton, D., Rowe, V. L. (2003) Smooth muscle cells improve endothelial cell retention on polytetrafluoroethylene grafts in vivo. J. Vasc. Surg. 38,557-563[CrossRef][Medline]
  22. Edwards, A., Carson, R. J., Bowald, S., Quist, W. C. (1995) Development of a microporous compliant small bore vascular graft. J. Biomater. Appl. 10,171-187[Abstract/Free Full Text]
  23. Watkins, M. T., Sharefkin, J. B., Zajtchuk, R., Maciag, T. M., D'Amore, P. A., Ryan, U. S., Van Wart, H., Rich, N. M. (1984) Adult human saphenous vein endothelial cells: assessment of their reproductive capacity for use in endothelial seeding of vascular prostheses. J. Surg. Res. 36,588-596[CrossRef][Medline]
  24. Button, M., Barden, G., Fuller, B., Hamilton, G. (2002) Optimized extraction of smooth muscle cells from human vein for use in a tissue engineered vascular graft. Cardiovasc. Pathol. 11,39
  25. Giudiceandrea, A., Salacinski, H., Tai, N., Punshon, G., Hamilton, G., Seifalian, A. (2000) Development and evaluation of an ideal flow circuit: assessing the dynamic behavior of endothelial cell seeded grafts. J. Artif. Organs 3,16-24[CrossRef]
  26. Kobashi, T., Matsuda, T. (1999) Fabrication of compliant hybrid grafts supported with elastomeric meshes. Cell Transplant 8,477-488[Medline]
  27. Kobashi, T., Matsuda, T. (1999) Fabrication of branched hybrid vascular prostheses. Tissue Eng. 5,515-524[CrossRef][Medline]
  28. Hirai, J., Matsuda, T. (1996) Venous reconstruction using hybrid vascular tissue composed of vascular cells and collagen: tissue regeneration process. Cell Transplant 5,93-105[CrossRef][Medline]
  29. Ishibashi, K., Matsuda, T. (1994) Reconstruction of a hybrid vascular graft hierarchically layered with three cell types. ASAIO J. 40,M284-M290[Medline]
  30. Kanda, K., Matsuda, T. (1994) Mechanical stress-induced orientation and ultrastructural change of smooth muscle cells cultured in three-dimensional collagen lattices. Cell Transplant 3,481-492[Medline]
  31. Mills, I., Sumpio, B. E. (1999) Mechanical forces and cell differentiation. Zilla, P. Greisler, H. P. eds. Tissue Engineering of Vascular Prosthetic Grafts ,425-438 R. G. Landes Austin, Texas, USA.
  32. Tiwari, A., Salacinski, H. J., Punshon, G., Hamilton, G., Seifalian, A. M. (2002) Development of a hybrid cardiovascular graft using a tissue engineering approach. FASEB J. 16,791-796[Abstract/Free Full Text]
  33. Dardik, A., Liu, A., Ballermann, B. J. (1999) Chronic in vitro shear stress stimulates endothelial cell retention on prosthetic vascular grafts and reduces subsequent in vivo neointimal thickness. J. Vasc. Surg. 29,157-167[CrossRef][Medline]
  34. Fisher, A. B., Chien, S., Barakat, A. I., Nerem, R. M. (2001) Endothelial cellular response to altered shear stress. Am. J. Physiol. Lung Cell. Mol. Physiol. 281,L529-L533[Abstract/Free Full Text]
  35. Wu, M. H., Kouchi, Y., Onuki, Y., Shi, Q., Yoshida, H., Kaplan, S., Viggers, R. F., Ghali, R., Sauvage, L. R. (1995) Effect of differential shear stress on platelet aggregation, surface thrombosis, and endothelialization of bilateral carotid-femoral grafts in the dog. J. Vasc. Surg. 22,382-390[CrossRef][Medline]
  36. Davies, P. F. (1995) Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75,519-560[Abstract/Free Full Text]
  37. Shigematsu, K., Yasuhara, H., Shigematsu, H., Muto, T. (2000) Direct and indirect effects of pulsatile shear stress on the smooth muscle cell. Inter. Angio. 19,39-46
  38. LeBaron, R. G., Athanasiou, K. A. (2000) Extracellular matrix cell adhesion peptides: functional applications in orthopedic materials. Tissue Eng. 6,85-103[CrossRef][Medline]
  39. Yu, H., Wang, Y., Eton, D., Rowe, V. L., Terramani, T. T., Cramer, D. V., Starnes, V. A., Weaver, F. A. (2001) Dual cell seeding and the use of zymogen tissue plasminogen activator to improve cell retention on polytetrafluoroethylene grafts. J. Vasc. Surg. 34,337-343[CrossRef][Medline]
  40. Nerem, R. M. (2000) Tissue engineering a blood vessel substitute: the role of biomechanics. Yonsei Med. J. 41,735-739[Medline]
  41. Seliktar, D., Black, R. A., Vito, R. P., Nerem, R. M. (2000) Dynamic mechanical conditioning of collagen-gel blood vessel constructs induces remodeling in vitro. Ann. Biomed. Eng. 28,351-362[CrossRef][Medline]
  42. L'Heureux, N., Pâquet, S., Labbé, R., Germain, L., Auger, F. A. (1998) A completely biological tissue-engineered human blood vessel. FASEB J. 12,47-56[Abstract/Free Full Text]
  43. Stock, U. A., Vacanti, J. P. (2001) Cardiovascular physiology during fetal development and implications for tissue engineering. Tissue Eng. 7,1-7[CrossRef][Medline]
  44. Solan, A., Mitchell, S., Moses, M., Niklason, L. (2003) Effect of pulse rate on collagen deposition in the tissue-engineered blood vessel. Tissue Eng. 9,579-586[CrossRef][Medline]




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