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(The FASEB Journal. 2006;20:874-881.)
© 2006 FASEB

Vitreous cryopreservation maintains the viscoelastic property of human vascular grafts

Raj R. Thakrar*,1, Vishal P. Patel*,1, George Hamilton{dagger}, Barry J. Fuller* and Alexander M. Seifalian*,2

* Biomaterials and Tissue Engineering Centre, Academic Division of Surgical and Interventional Sciences, University College London, UK; and

{dagger} Vascular Biology Unit, Royal Free Hampstead NHS Trust, London, UK

2Correspondence: University College London, Rowland Hill St., London NW3 2PF, UK. E-mail: a.seifalian{at}medsch.ucl.ac.uk


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Assess the effects of cryopreservation (cryo) and vitrification (vitro) on the viscoelastic properties of blood vessels. Human external Iliac artery vessels were harvested from liver organ donors (n=8). In each case the vessel was segmented into 3 equal parts, which were randomly placed in one of 3 categories: Fresh (stored in 4°C UW for 6 h), Cryo (Placed in 10% Dulbecco’s modified Eagle medium (DMEM) and slowly frozen to –196°C), or Vitro (Placed in 40% DMEM and rapidly cooled to –196°C). A pulsatile flow circuit was used to perfuse arterial segments at physiological pulse pressure and flow. Intraluminal pressure was measured using a Millar Mikro-tip catheter transducer, and vessel wall motion was determined with duplex ultrasonography coupled with a novel echo-locked vessel wall tracking system. Diametrical compliance (DC), Petersons elastic modulus (Ep), and stiffness index (ß) were then calculated for each of the three groups over 3 mean pressure ranging from 40 to 80 mmHg. The change in the viscous component of arterial wall (lag phase angle, {theta}) was calculated from hysteresis plots. No significant changes were observed in the elastic properties of fresh and vitrified vessels (P>0.05 for each of DC, Ep, and ß). Similarly, variation in the wall viscosity between fresh and vitrified vessels appeared to be nonsignificant ({theta}=12.60±4.04 vs. 17.60±1.14, respectively). In contrast, statistical analysis of results obtained for cryopreserved vessels to the fresh vessels showed significant reduction in elastic parameter values. There was also a significant increase in the phase angle {theta} of the cryopreserved vessels ({theta}=24.30±6.32; P<0.001) compared with fresh vessel. Results suggest that vitrification maintains both elastic and viscous components of the mechanical properties of vascular grafts, which is positively correlated with their functional patency. In contrast, damage caused during cryopreservation significantly affects the overall tensile strength and elasticity of the vessel (i.e., Ep and ß), the dynamic properties (DC), and appears to significantly affect the viscous component of the vessel wall ({theta}), which is likely reduce the patency of the graft for transplantation purposes.—Thakrar, R. R., Patel, V. P., Hamilton, G., Fuller, B. J., Seifalian, A. M. Vitreous cryopreservation maintains the viscoelastic property of human vascular grafts.


Key Words: vessel wall • vitrification • vascular grafting • allograft


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
ORGAN TRANSPLANTATION, including cardiovascular bypass grafting, is a widely used method in reconstructive surgeries. The superiority of autogenous veins in reconstructive procedures is well recognized (2) . This is primarily due to the fact that the risk of rejection associated with antigen-antibody mismatch may be eliminated. Also the process of harvesting and transplanting the vessel is almost instantaneous, reducing the concentration of damage associated with storage of tissue in cold ischemia. However, an inadequate supply of these veins in patients has resulted in surgeons having to use alternative techniques (3) . A number of such vascular grafts are available, but studies of these materials indicate the inability of these prosthetic vessels to sufficiently match the functional properties of autogenous vessels, especially relating to the biomechanical properties (4) .

Similarly, the use of allografts has been suggested as an alternative source of blood vessels for vascular tissue engineering. A key advantage associated with the use of allografts is the fact that they are relatively more abundant than autografts and more likely to possess adequate biomechanical properties to function efficiently in the recipient. Conversely, there are common problems associated with the use of this technique, primarily being an increased risk of disease transmission between individuals. Further, Oschner and co-workers researched the use of such grafts and identified that rejection was a common occurrence in patients (5) .

To date, three current approaches to tissue preservation exist. The first is storage of the tissue at hypothermic temperatures. This is currently the standard method used for short-term storage of organs during transplantation. One of the main problems associated with this technique of preservation is the short period before significant concentration of cellular injury occurs (6) .

A second preservation technique has been proposed that involves freezing and thawing of tissues at cryogenic temperatures. This technique has been successfully applied to individual cells in which cryopreserved human hematopoietic stem cells were observed to retain engraftment potential (7) .

Vitrification is an alternative process of long-term subzero preservation of tissues and whole organs (8) . The process involves converting an aqueous solution by use of high concentrations of cryoprotectants into an amorphous solid at low temperatures, such that when the liquid is cooled down it may be taken below its melting point without producing ice crystal growth. Restriction of ice crystal growth results in reduced structural and molecular damage. However, the key problem associated with vitrification of tissues is that approximately half the water within the tissue must be replaced by the vitrification solute (9) .

The key advantage of cryopreservation and vitrification as techniques for tissue preservation is the fact that deep subzero temperatures are thought to allow long-term storage. This has the potential to allow long-term banking of blood vessels for elective use in reconstructive and vascular surgery.

As mentioned earlier, vascular grafting is an important feature of vascular and transplant surgery and has become an increasingly common feature of tissue engineering. Such procedures may be successfully applied to bypass graft such as coronary artery. Appreciation of the overall effects of preservation on the mechanical properties of blood vessels is vitally important: it is these properties that influence blood flow through organs, and it is well known that changes in the mechanical properties of blood vessels occur with hypertension and disease processes such as atherosclerosis (10) . Studies of pharmacological responses of blood vessels to cryopreservation or vitrification (8 ,11) have been made using tissue rings; in vivo grafting experiments have also been reported (12 ,13) . However, to our knowledge there are no other reports on the effects of these different preservation techniques on mechanical properties of large vessel segments.

The essential mechanical properties of blood vessels may be categorized into one of two groups: elastic and viscous properties. Whereas elastic properties represent a time invariant component of the arterial wall structure, viscoelasticity refers also to the time variant component, which is primarily due to the viscosity exhibited by the biological structures that make up the vessel (14 ,15) .

The aim of our study was to assess the viscoelastic properties of human arterial blood vessels after cryopreservation and vitrification as an indication of their subsequent suitability for allograft application.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Elastic indices
The arterial elastic properties and indices are well described: Petersen’s elastic modulus (Ep) is defined (16) as:

Formula
Where D and P are diameter and pressure, and s and d denote systole and diastole, respectively. The inverse of Petersen’s elastic modulus is known as the diametrical or cross-sectional compliance (DC) and is given by the equation:

Formula
They measure the fractional change rather than the absolute change in the viscoelastic properties of the artery. This provides a means by which arteries of varying diameters can be compared. The stiffness index (ß) has been shown to be less dependent on the arterial blood pressure than the elastic modulus (17) , and is given by the equation:

Formula
In this study, we computed all three indices to assess the elastic properties of the arteries to avoid bias toward any of the parameters.

Viscous indices
The viscous component of the viscoelastic properties of arteries is a component of the dynamic elastic modulus (E) (18) and is the viscous retarding force, derived from the imaginary part of incremental elastic modulus as:

Formula
where {eta} is the coefficient of viscosity and {omega} is the angular velocity. When considering the artery, as the pressure within the tube is increased the radius begins to change. However, the change in radius (strain) lags behind the pressure (force) change. This lag is described by the phase angle ({theta}). When strain is plotted against force, a hysteresis loop results (see Fig. 4A ). As indicated in the equation below, the phase angle {theta} can be calculated from the ration of the separation, a, between the ascending and descending limbs at midcycle, where {Delta}F is the total excursion.

Formula


Figure 4
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  		Figure 4. A Typical hysteresis loop for one cardiac cycle obtained from fresh artery (A); summery of viscous component of arterial wall computed from hysteresis loop (B), *P < 0.001; $P > 0.05.

Human blood vessel
Human external iliac arterial grafts were obtained from liver donor transplantations. All human vessels were obtained in accordance with local ethics committee standing orders regarding experimental use of discarded human tissues.

Flow circuit simulation of the human cardiovascular system
We have developed and validated a flow system capable of simulating in vitro the pulsatility, flow waveform including reverse flow, pressures, and degree of oxygenation and pH of physiological femoral and coronary artery circulation in vivo (see Fig. 1 ) (19) . The system was described earlier (20) . Briefly, the model consisted of a variable-speed electromagnetic centrifugal pump, flexible plastic tubing and reservoir, flow waveform conditioner (FWC), Maxima hollow fiber oxygenator supplied with 95% air/5% CO2, an outflow resistance, a 6 mm caliber tubular flow probe and Transonic Medical Flowmeter (TMF) system; a serial intraluminal pressure in the artery was identified at discrete sites along the vessel using a Miller Mikro Tip catheter transducer (Miller Instruments, Houston, TX, USA) introduced via a Y connection port. The circuit was circulated with perfusion solution that has been published (21) . This was warmed to body temperature (37°C) using a water jacket around the reservoir. Serial intraluminal pressure in the circuit was identified at discrete sites along the graft using a Miller Mikro Tip catheter transducer (Miller Instruments) introduced via a Y connection port.


Figure 1
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  		Figure 1. The flow circuit comprising a variable-speed electromagnetic centrifugal pump, flexible plastic tubing, fluid reservoir, and circulating solution oxygenated through a Maxima hollow fiber oxygenator with 95% air and 5% CO2. Automatic pH, pO2 and pCO2 controller. A flow waveform conditioner (FWC) sited in series with the circuit is used to generate arterial flow waveforms. This was constructed in-house and consisted of a solenoid connected to an electronic control box from which the frequency and duration of solenoid occlusion could be governed. Instantaneous flow rate is measured using the TMF system. Serial intraluminal pressure measurements can be made at discrete sites along the graft using a Millar Mikro-tip catheter transducer introduced via a Y-connection port. Graft radius, flow rate, and shear stress are determined using an ultrasound duplex (US) scanner with a wall tracking system (WTS). All outputs are fed into a computer.

Preservation technique
Upon retrieval of each vessel, the vessels were cut in three equal segments; initial storage involved placing the segment in 4°C UW solutions in ice for the period of transportation between the site of retrieval and arrival in laboratories. The vessels were then randomly allocated to one of the following preservation techniques. For storage at cryogenic temperatures, 1,2 propane diol was selected as cryoprotectant because it has one of the best glass-forming tendencies of the linear alcohols (an important factor for the vitrification experiments) and a low toxicity (22) . It is also used widely in traditional cryopreservation by slow cooling for a variety of cells.

1. Fresh: Upon retrieval, vessel segment was stored in 4°C University of Wisconsin (UW) solutions for 6.0 ± 0.5 h on ice, then tested.

2. Cryopreservation: Vessel segment was placed in 10% w/v 1,2 propanediol in DMEM solution for 20 min on ice after retrieval. This was then cooled slowly in a polypropylene tube surrounded by insulation in a mechanical freezer to –70°C (yielding an average cooling rate of –2°C/min (measured by thermocouple) and left overnight. Then the vessel was placed in liquid nitrogen, cooled to –196°C, and stored for less than 1 h before thawing and testing.

3. Vitrification: In this case the vessel segment was placed in 40% w/v 1,2 propanediol in DMEM solution for a period of 20 min on ice. The vessel was then rapidly cooled to –196°C by placing the tube in liquid nitrogen (with an average cooling rate of –40°C/min) and stored at this temperature overnight, before thawing and testing.

Thawing
After 24 h preservation, both cryopreserved and vitrified vessels had to be thawed before tests were carried out. In each case the vessels were removed from liquid nitrogen and placed in ice for ~5 min. They were then transferred to a 37°C water bath until all ice had melted and placed in fresh DMEM at room temperature for 20 min prior to testing.

After thawing of each blood vessel, each artery was placed in the flow circuit and measurements of the vessel wall movements were carried out over a range of intraluminal blood pressures as described below. Note that in each case the artery under study was immersed in a saline bath at 37°C.

Measurement of vessel wall movement
The change is vessel wall diameter with respect to each cardiac cycle was measured at discrete sites along the graft. Measurements were taken along the saggital plane at 90° to the vessel wall. In each case three measurements were taken at different points along each vessel at respective blood pressures.

The segments of the graft were scanned through the use of a duplex color-flow ultrasonography system (Pie 350; Pie Medical Systems, Maastricht, The Netherlands). This system has been successfully used for in vivo and in vitro measurement of viscoelastic properties of vessel (23) . This technique uses radio frequency to automatically track movement of the anterior and posterior arterial walls, and hence gives values for the overall distension over a period of time.

A 7.5 MHz linear array probe was immersed in the saline bath directly above the vessel to be investigated. The M-mode cursor was positioned midway along the test segment for the first reading, then displaced equidistant on either side of the midpoint for the second and third measurements.

The data recorded by the ultrasound was transferred to a personal computer (Wall Tracking System, WTS) for real-time display of the displacement waveforms of distension of artery walls (Fig. 2 ). These measurements were made using a constant pulse pressure over a range of mean physiological blood pressures (Table 1 ).


Figure 2
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  		Figure 2. Vessel distension detected with ultrasound wall tracking system and pressure with Millar Mikro-tip catheter transducer from circuit in Fig. 1 .


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  		Table 1. Summary of hemodynamic parametersa

Data analysis and statistical methods
The WTS was used to identify overall displacement of the vascular wall at each respective blood pressure. The results obtained over a 4 s cycle were then transferred to a spreadsheet such that the relative displacements were tabulated against their respective blood pressures (i.e., systolic pressure and the corresponding distension at this pressure was identified as was the diastolic pressure and corresponding diastolic distension). Using these values, diametrical compliance (DC) together with Peterson’s elastic modulus (Ep) and stiffness index (ß) were calculated. Hysteresis analysis was also applied to one vessel to appreciate quantitatively the overall effects of cryopreservation and vitrification on the viscosity of the blood vessels.

In each case, each vessel was sampled three times and an average value of each index was obtained at the relative blood pressures. A comparison of the DC, Ep, ß, and phase angle {theta} of cryopreserved and vitrified vessels with those of the fresh samples was carried out using 1-way ANOVA and the Bonferroni test.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
A summary of elastic parameters (Ep, ß) values for fresh, cryopreserved, and vitrified vessel segments with respect to each mean pressure is provided in Table 2 . Figure 3 depicts the variation of compliance at mean pressures 40–80 mmHg for fresh, cryopreserved, and vitrified vessel segments. As one would expect, arterial compliance was observed to behave nonlinearly in response to increased pressure.


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  		Table 2. Petersen’s elastic modulus, stiffness values for three mean pressures at 40, 60, and 80 mmHg, with peak pressure of 60 mmHga


Figure 3
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  		Figure 3. Diametrical compliance (DC) vs. mean pressure curves for fresh arteries and arteries post cryopreservation or vitrification. Curves were generated using nonlinear regression (single-phase exponential decay fit).

Table 3 summarizes the outcome of subsequent Bonferroni post-testing for each mean pressure, the compliance (DC), Peterson’s elastic modulus (Ep), and stiffness index (ß) values for fresh arteries and arteries preserved using cryopreservation or vitrification techniques. There were no significant differences between the (DC), (Ep), and (ß) values of fresh and vitrified arteries at the three (40, 60, 80 mmHg) mean pressures. However, a comparison of the same parameters between fresh and cryopreserved vessels revealed significant differences between the two vessel types at all three pressures.


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  		Table 3. Outcome of analysis of variance comparison of diametrical compliance (DC) together with Peterson’s elastic modulus (Ep) and stiffness index (ß) for fresh (F) arteries and arteries preserved using vitrification (V) or cryopreservation (C) techniques with post-Bonferroni analysis

Figure 4 A displays an example of the change in internal vessel diameter with respect to incremental increases in pressure. The changes in pressure cause nonlinear vessel distension that depends on the pressure itself, producing a hysterisis curve. The area within the loop of course is the energy dissipated due to the viscoelasticity of the vessel wall.

Mean values of the phase angle ({theta}) calculated from the hysterisis curves were 12.60 ± 4.04, 24.30 ± 6.32, and 17.6 ± 1.04 for fresh, cryopreserved, and vitrified vessel segments, respectively. There was a significant increase in ({theta}) as shown in Fig. 4B with cryopreserved vessel segment when compared with fresh vessel segments, but no significant increase in ({theta}) with the vitrified vessel segments.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This study addresses the overall effects of cryopreservation and vitrification on the viscoelastic properties of the human external iliac artery. Viscoelasticity, as the name suggests, is a generalization of the concepts of viscosity and elasticity. In a purely elastic body the application of a tension instantaneously produces a certain deformation, which disappears instantaneously once the tension is removed. In contrast, in viscoelastic bodies a finite period is required to reach the state of deformation consequent to the application of the tension. This delay is due to the presence of viscous phenomena.

The viscous behavior of the arterial wall is attributed primarily to smooth muscle cells (24) and may also be a reflection of the 3-dimensional network formed by muscular elastin and collagen fibers; hence, damage caused especially by intracellular ice formation in smooth muscle cells as well as fragmentation to elastin and collagen fibers will affect the viscosity of the artery.

The state of the components of the extracellular matrix is another factor that requires consideration. Changes in the fibrous components of the vessel (i.e., elastin and collagen) have been related to the elasticity of the vessel (25) .

So far, studies of artery wall mechanics contain the obvious, but at times misleading, assumption that the physical laws governing vessel wall mechanics are those strictly related to a purely elastic body, and so fail to address the viscous component to the vessel wall (13 , 26) .

Therefore, we wanted to assess the effects of cryopreservation and vitrification on the viscoelastic properties of the external iliac artery by assessment of both elastic and viscous indices. The results obtained from the various experiments carried out found variation in both elastic and viscoelastic properties caused by the two preservation techniques.

The technique of cryopreservation involves freezing of the vessel segments at cryogenic temperature after exposure to a cryoprotectant solution (11) . During the process of cryopreservation of blood vessels, the next major step after cooling of the vessel to subzero temperatures is the formation of ice at some point within the system. To ensure a successful outcome of this process of cryopreservation, the biological material must have the capacity to withstand cumulative strains generated during the change in state from physiological body temperatures to –196°C (as anticipated in liquid nitrogen) (27) .

Formation of ice occurs preferentially in the extracellular region of the vessel. Upon freezing, the vessel may be considered as two main compartments. While the extracellular space within the vessel represents the first of these, the individual cells make up the second. When ice forms in the cryosystem, there exists a point where solid and liquid phases coexist as crystals and free solution (residual solution). As cooling progresses, the fraction of ice gradually increases. This results in an increase in solute concentration. The consequence of this increase is the movement of water out of the surrounding cells due to osmotic imbalance. This in turn results in a reduction in cell volume and cytoplasmic cell dehydration. The concentration of osmotic stress has been correlated to the size of the overall cell (28) such that smaller cells such as erythrocytes are likely to suffer a reduced concentration of stress compared with larger cells such as mammalian oocytes.

Alternative stresses other than osmotic imbalance may also be applied to cells after freezing. These include damage to cell membranes due to overcrowding, which occurs as a result of interactions between charged surface layers after close contact (29) . Movement of ice within the solution that is being frozen also gives rise to a phenomenon referred to as the electrical effect (30) , resulting in further damage to the cell membrane. This involves the generation of an electrical field at the ice-solute interface (the Workman-Reynolds effect) and contributes to stresses imposed on the biological material.

Similarly, during ice formation a potential exists for damage to individual cells, interconnections with neighboring cells, and other extracellular structures such as smooth muscle cells and the epithelial layer (31) . Particular concern in cryopreserving tissues is the location of extracellular ice (32) . Even if cryopreservation is capable of recovering viable cells within the vascular graft, the growth of ice crystals may disrupt the matrix in of the vessel wall and even lead to fracturing (33) . This mechanical disruption seems a likely cause of the poor function of cryopreserved arteries in our current study, but more work is required to confirm this theory. However, support for this concept is available from other work (31) , where histological analysis of cryopreserved vessels identified some changes in the vascular wall, which included fragmentation of cells in the tunica media together with changes to the elastic lamina. The occurrence of such histological changes may be the basis of the significant variations observed in the viscoelastic properties between fresh and cryopreserved vessels in this study. However, histological assessment is of necessity a destructive procedure, with potential sampling error when using small biopsies. Dynamic measurement of viscoelastic properties could be developed as a nondestructive test of whole vessel performance after storage and before grafting.

So far consideration has been given to the formation of extracellular ice within the vessel. However, after ice nucleation in the extracellular compartment due to thermodynamic equilibrium, freezing of intracellular solution also occurs. The effects of such a process on the cell viability is dependent on the overall size of the crystals formed such that large crystals are more damaging than with small ice crystals (34) .

Vitrification is thought to be a relatively superior technique of preservation for tissues, and previous work has demonstrated the ability of vitrification protocols to preserve cellular physiological function in vascular grafts (35) . The process involves placing the tissue to be preserved in a much higher concentration of cryoprotectant and cooling rapidly. The high osmolality of the surrounding solution will promote rapid water loss from the intracellular cytosol of cells. As a result, ice formation, which is known to be destructive to cells and organs (29 ,33) , is eliminated, and instead both the intracellular solution and the extracellular mixture undergo a phase change to an amorphous state or "glassy" state. The vitrification mixture chosen in this study is very close to the minimal concentrations of propanediol required to achieve this glassy state (8 ,22) . Using this and the cooling rate we achieved, the sample remained transparent and glassy during cooling and storage but became opaque during warming, indicating the growth of some ice. Thus, the method can only be considered as quasi-vitrification, but from the results obtained it seems likely that this limited ice formation on warming was not sufficiently great to disrupt the mechanical properties of the blood vessels.

From our study, a comparison of the elastic parameters shows a significant difference between fresh and cryopreserved vessel segments but a nonsignificant difference in the elastic properties of fresh and vitrified vessels. This is also true for the phase change angle {theta}, where a significant increase was found representing an increase in vessel wall viscosity after cryopreservation. These results suggest that damage caused during cryopreservation significantly affects the overall tensile strength and elasticity of the vessel (i.e., Ep and ß), the dynamic properties (DC), and appears to affect the viscous component of the vessel wall ({theta}), which likely reduced the viability of the graft for transplantation purposes.

It has long been established that a mismatch between viscoelastic properties such as compliance between vascular prosthesis and its host vessel can be detrimental to the performance of the graft and can result in the loss of patency (36) . In addition, mismatch in the elastic properties of prosthetic grafts and the adjacent native vessel has been implicated in the etiology of anastomotic myointimal hyperplasia.

Whereas elastin and collagen are needed to keep the concentration of arterial stress stable, allowing cyclic elastic arterial stretching and recovery but preventing overdistension of the arterial wall, viscosity provides an indication of capacity to dissipate energy of wave pulse components from the pulsatile arterial flow. An optimal viscosity/elasticity ratio of arterial wall components is important in protecting the wall from the high oscillatory frequencies present in a pulsatile arterial blood flow (37) .

In summary, based on the findings from our study, emphasis may be placed on the need to preserve the mechanical properties of the blood vessel for viable allografting. As evident from the results obtained in this study, we propose that vitrification is a superior preservation technique in its ability to maintain the viscoelastic properties of the vascular graft. In contrast, a major limitation of cryopreservation for the preservation of vessel allografts is based on its inability to maintain both elastic and viscous components of the arterial wall.


   FOOTNOTES
 
1 These authors contributed equally to this work.

Received for publication October 28, 2005. Accepted for publication January 6, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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