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The effect of storage solutions on endothelial function and saphenous vein graft patency

  • Ismail Bouhout
  • Walid Ben Ali
  • Louis Paul PerraultEmail author
Review Article
  • 20 Downloads

Abstract

Vein graft failure is a complex mechanism that can be triggered immediately after surgical harvesting. Storage solutions have a major role in preventing endothelial cell damage during harvesting. While normal saline is still widely used, buffered solutions seem to better preserve endothelial integrity and function. This review aims to summarize the current literature surrounding vein graft storage solutions.

Keywords

Vein graft Preservation solution Coronary artery bypass 

Introduction

Despite the widespread use of arterial conduits, saphenous vein grafts (SVG) are used in approximately 90% of patients undergoing coronary artery bypass grafting (CABG) surgery to target the right coronary or the circumflex coronary arteries [1, 2]. However, half of the SVGs are occluded 10 years after surgery and of those still patent, 50% show marked atherosclerotic changes [3, 4, 5]. The resulting vein graft failure is associated with long-term adverse events after surgical revascularization [3]. Multiple factors may influence endothelial and vascular wall integrity during the intraoperative period including the condition of the vein itself, excessive manipulation, overdistension, and type of preservation solution used during warm ischemia. Interestingly, a survey conducted in 90 US centers showed a particular heterogeneity in the use of preservation solution with 29% using normal saline, 27% autologous blood, and 40% buffered solutions [6]. Despite two decades of debate, the best solution that preserves endothelial function and improves long-term SVG patency remains undetermined. The mechanism of vein graft failure, SVG preservation solutions, and their impact on graft patency will be discussed in this review.

Vein graft failure

Vein graft failure is the result of a complex physiopathological process that is dependent on endothelial integrity, development of intimal hyperplasia (IH), and atherosclerosis [7].

Early SVG failure is mainly due to the endothelial dysfunction and damage. During harvesting, manual handling and pressure distension could result in extensive damage to the endothelial layers. The endothelium denudation and exposition of the sub-endothelial matrix lead to the coagulation cascade activation and subsequently to thrombus formation.[8, 9, 10] Indeed, thrombosis-mediated graft failure is an early event responsible for 10–15% of vein graft failure (VGF) within the first month after CABG [11]. Many harvesting approaches have been proposed to mitigate the damage of endothelium layers. The no-touch technique (NT) consists of harvesting the vein with surrounding tissue and pedicle as well as avoidance of vein distention. The NT has been associated with a higher short- and long-term SVG patency rate while increasing the risk of wound complications. Endoscopic saphenous vein harvesting (ESVH) has emerged as minimally invasive technique that reduces wound pain and infection in patients undergoing CABG surgery. In a histological and immunohistochemical evaluation of SVG, harvested with closed tunnel, ESVH technique showed superiority in terms of endothelial layer preservation when compared to open harvesting. Similarly, Lamm et al. [12] studied endothelial integrity using electron microscopy following ESVH with continuous graft infusion from the heart-lung machine. This technique showed a better endothelial integrity when compared to conventional harvesting and preservation in a crystalloid solution. In contrast, Lopes et al. [13] have reported higher rates of vein-graft failure at 12 to 18 months in patients who underwent ESVH compared to patients undergoing open vein harvesting.

The ischemic-reperfusion injuries occurring in the first hours following surgery expose the SVG to oxidative stress [14]. In addition, the early endothelial dysfunction leads to a decrease in the nitric oxide (NO) production which impairs graft vasorelaxation and inducts a pro-inflammatory state [15]. Furthermore, the injured endothelial cells express adhesion proteins and selectins that promote the inflammatory response. In order to prevent the ischemic-reperfusion injury, preservation solutions after SVG harvesting aim to protect endothelial integrity.

Late SVG graft failure is mainly mediated by intimal hyperplasia (IH) and atherosclerosis development. In the arterialization process, endothelial integrity plays a crucial role in the ability of vein grafts to adapt quickly to hemodynamic forces, shear stress, and radial wall stresses in a high-pressure and a pulsatile arterial system [16]. The loss of the balance between vascular pro- and anti-inflammatory factors leads to the production of cytokines (IL-2, IL-10) and growth factors (PDGF, IFF-1). This promotes migration and proliferation of smooth muscle cells (SMC) in the intima layer leading to IH [17]. This process starts 1 week following surgery and peaks at 4–6 weeks postoperatively. Venous metallic external stents (VEST™) have been hypothesized to mitigate the risk of IH by avoiding SMC migration to the intima. Taggart et al. [18] evaluated stented SVG with an angiography study 1 year after CABG surgery. They reported an SVG patency improvement and a reduction of IH. In the SAVE RITA trial, Kim et al. [19] have investigated the potential benefit of NO continuous production by an internal mammary artery (ITA) anastomosed to the SVG. The angiographic patency of the saphenous vein composite graft was non-inferior to a composite graft using the left and right ITAs up to 1 year of follow-up.

The initial endothelial damage is the main pathophysiological process that triggers the development of SVG atherosclerosis. The pathogenesis of atherosclerosis involves vessel wall inflammation, oxidative stress cellular proliferation, fibrous plaque formation, and continuous endothelial damage.

Intraoperative storage solution

The optimal intraoperative storage solution

Storage solutions are aiming to reduce ischemic-reperfusion injuries and to preserve endothelial integrity in order to limit the risk of SVG failure. The acid-base homoeostasis has been hypothesized to explain the limited result reported with heparinized 0.9% normal saline (NS) and autologous heparinized blood (AHB) [20, 21, 22, 23]. Indeed, Biswas et al. [24] showed that cell viability was maintained at a physiological pH (7.4), diminished at pH = 8.0, and was completely lost at pH = 6.0. Buffered solutions offer a physiological pH and are more resistant to changes in pH due to added buffers. The composition of these solutions is summarized in (Table 1). The only study that examined the clinical benefit of buffered solutions is a sub-analysis of the Project of Ex-vivo Vein Graft Engineering via Transfection (PREVENT) IV trial. Harskamp et al. [5] compared rates of VGF and long-term clinical outcomes in 3014 CABG patients whose SVGs had been stored in NS, buffered saline, or AHB. One-year VGF rates were far lower in the buffered saline than in the saline group (graft-level odds ratio 0.63; 95% IC [0.49–0.79], P < 0.001] or the blood group [graft-level odds ratio 0.62; 95% IC [0.46–0.83], P < 0.001]. Buffered saline solution was associated with lower 5-year risk of death, myocardial infarction, or repeat revascularization than with saline or blood, without reaching statistical significance [hazard ratio 0.81; 95% IC [0.64–1.02], p = 0.08 and 0.81; 95% IC [0.63–1.03], p = 0.09, respectively]. Potential confounding factors such as solution temperature, distension pressure, storage duration, and coronary artery anatomy were not documented. In vivo and ex vivo studies reporting results with buffered solutions are summarized in (Table 2).
Table 1

Available saphenous vein graft preservation solutions

Solutions

pH

Osmolarity (mOsm/L)

Na+ (mmol/L)

Cl (mmol/L)

K+ (mmol/L)

Mg2+ (mmol/L)

Ca2+ (mmol/L)

SO42− (mmol/L)

HCO3− (mmol/L)

Other components

Standard solutions

 0.9% NS

4.5–7.0

308

154

154

None

 AHB

7.4

280–310

140

110

5

2

2

None

Buffered solutions

 GALA

7.4

309

142–156

145

5.8–6

0.89–1

0.95–1

0.5

4

Glutathione, L-ascorbic acid, L-arginine, glucose

 TiProtec™

7.0 at 20 °C

305

16

103.1

93

8

0.05

α-ketoglutarate, aspartate, N-acetylhistidine, glycine, alanine, tryptophan, sucrose, glucose, deferoxamine, 3,4-dimethoxy-N-methyl-benzohydroxamic acid

 UWS

7.4

360

27

 

125

5

5

Lactobionic acid, adenosine, allopurinol, raffinose, glutathione, polyhydroxyethyl starch

 He solution

7.4

147

156

4

2.3

0.2 mL of 8.4%

Verapamil hydrochloride, glyceride trinitrite, heparin

 Plasma-Lyte

7.4

294

140

98

5

1.5

Acetate Gluconate

 HTK

7.4 at 4 °C

310

15

50

9

4

0.015

Histidine,α-ketoglutarate, Tryptophane, mannitol

AHB autologous heparinized blood, GALA gluthatione, ascorbic acid, L-arginine, HTK histidine-tryptophan-ketoglutarate, NS normal saline, UWS University of Wisconsin solution

Table 2

In vivo and ex vivo studies reporting results of buffered preservation solutions

Study

Design

Key endpoints

Catinella et al. 1982 [20]

SVG of patients undergoing CABG bathed in:

 -AHB

 -Buffered saline

SVG integrity evaluated by electron microscopic study

SVG patency assessed by angiography at 10 days

Higher VGF rate in the AHB group at 10 days [20 vs 7%, p < 0.01]

Endothelial cell desquamation and severe venous smooth muscle cell spam in the AHB group.

Santoli et al. 1993 [32]

Human SVG harvested using the no touch technique

Electron microscopic comparative analysis of the effects of:

 -AHB

 -NS with papaverine

 -UWS

Severe endothelial cell loss and mural edema/necrosis at 30 min and 5 h in the AHB group.

Preserved endothelial integrity with NS but intracellular edema in 20% of cases

Preserved endothelial integrity with the UWS solution.

Sanchez et al.[21] 1994

Canine and human SVG immerged in:

 -Plasma-lyte

 -NS containing norepinephrine

Isometric-tension recording compared

Plasma-lyte completely relaxed the SVG within 20 min, while veins remained partially constricted with NS.

Cavallari et al. 1997 [29]

Canine external jugular and common femoral vein segments preserved in:

 -NS

 -AHB

 -UWS

Endothelial integrity and maximum contractile response measure at 45 min and 24 h

Endothelial integrity and maximal contractile response preserved in the UWS group when compared to standard preservation solutions.

Hickethier et al. 1999 [22]

Human SVG incubated for 45 min in:

 -NS

 -M-199

Endothelial damage evaluated by electron microscopy

Greater endothelial cell destruction in the NS group [55 vs 26% at 45 min]

Schaeffer et al. [37] 1999

Rabit carotid arteries perfused by:

 -NS

 -Ringer’s lactate

 -St Thomas’ solution

 -HTK

Endothelial permeability by measuring peroxidase accumulation

The HTK solution resulted in the better endothelial preservation.

Kown et al. 2001 [23]

Rabbit internal jugular treated intraluminally for 5 min with:

 -NS

 -L-arginine solution

And grafted in the contralateral carotid artery.

Rabbits were killed after 28 days

Garft score for intima/media ratio NO production were measured.

Greatest neointimal proliferation in the NS group.

Higher NO level in the L-arginine solution.

Thatte et al. 2003 [43]

Human SVG stored for 60 min in:

 -NS

 -AHB

 -GALA

Endothelial cell structural viability, calcium mobilization, and nitric oxide generation were measured

Greater cell integrity maintenance in the GALA group [76–100%] at 24 h

Calcium mobilization and NO production increased at 5 h in the GALA group and not detectable in the NS and AHB groups at 3 h.

Weiss et al. 2009 [9]

Human SVG stored in:

 -NS

 -NS + albumin

 -AHB

 -HTK

The HTK solution failed to maintain cell integrity.

Wilbring et al. 2013 [40]

Human SVG stored for 24 and 96 h in:

 -NS

 -TiProtec

Vessel wall function evaluated ex-vivo

The endothelium-dependant vasodilation abolished in the NS group and preserved in the TiProtec group at 96 h.

Wise et al. 2014 [35]

Human SVG placed for 1 h in:

 -NS

 -UWS

 -Plasma-lyte

Graft contractility measured

Reduced KCl induced contractility in the NS group when compared to UWS.

Harskamp et al. 2014 [5]

Human VGF immerged in:

 -NS

 -AHB

 -Buffered saline

One-year angiographic VGF and 5-year rates of death, myocardial infarction, and subsequent revascularization were determined.

1 year VGF rates were lower in the buffered solutions than in the saline group [graft-level odds ratio 0.63, p < 0.001] or the blood group (graft-level odds ratio 0.62, p < 0.001)

5 years HR ratios for death, myocardial infarction and repeat revascularization was 0.81 (buffered saline versus AHB/NS)

AHB autologous heparinized blood, GALA gluthatione, ascorbic acid, L-arginine, HTK histidine-tryptophan-ketoglutarate, HR hazard ratio, NO nitric oxide, NS normal saline, UWS University of Wisconsin solution, VGF vein graft failure

Heparinized 0.9% normal saline

Normal saline is the most used preservation solution. It contains 40 U/mL of heparin, 154 mmol/L of sodium chloride, has a pH of 5, and is hypertonic [308 mOsm/L]. Studies comparing NS to other preservation solutions have shown a reduction in SVG vascular tension and a marked endothelium-dependant vasodilation function decrease even after a short-term storage [< 90 min] [25, 26, 27, 28, 29, 30]. In addition, preservation of SVG on NS has demonstrated an extensive endothelial cell damage [28, 29, 31].

Autologous heparinized blood

Autologous heparinized blood may mitigate the endothelial damage seen with the NS. However, the real benefit of AHB as a preservation solution over the NS remains debated. Indeed, Gundry et al. [31] showed that SVG immersed in a warm AHB resulted in less endothelial damage when compared to warm NS. While both solutions showed a similar endothelial preservation at 4 °C, cold saline was associated with mural edema. In an in vitro and in vivo study, Bush et al. [27] assessed endothelial function by measuring the production of prostacyclin metabolites. While the AHB was associated with a preserved biochemical function when compared to NS in the pre-arterialization phase, this difference disappears after arterialization of the graft. In another study, AHB better preserved endothelial integrity when compared to NS, as assessed by measuring endothelium-dependent relaxation factors. In contrast, other studies [28, 29, 32, 33, 34] failed to find any significant superiority of AHB over saline in preserving graft function. In terms of pro-thrombotic state prevention, Weiss et al. [9] concluded that endothelium-dependent anticoagulant activities were similarly abolished when vein grafts were immerged in AHB or NS preservation solutions.

The University of Wisconsin preservation solution

The objectives of this solution are to maintain an osmotic concentration by inert metabolites [raffinose and lactobionic acid), to prevent cellular edema by using colloids [hydroxyethyl starch], and to provide an antioxidant effect [glutathione]. In an in vitro human study, [32] SVG stored in the University of Wisconsin preservation solution (UWS) showed a preserved endothelial integrity at 30 min and 5 h. Similarly, Cavallari et al. [29] evaluated functional and morphological canine vein grafts stored in the UWS solution, compared to NS and AHB. The endothelial integrity and maximum contractile were preserved with the UWS solution while these were reduced in SVG stored in AHB and NS solutions. Wise et al. [35] compared in vitro human SVG contractility after preservation in UWS and NS solutions. While there was no difference in terms of endothelial-independent relaxation between the two solutions, the endothelial-dependent relaxation induced by potassium chloride was reduced in NS and preserved in the UWS group.

Histidine-tryptophan-ketoglutarate solutions

The HTK solutions buffer the extracellular space by means of the histidine, stabilize membranes using the tryptophan, and protect against reactive oxygen species damage by using ketoglutarate which is an energy substrate for anaerobic metabolism. This solution is a low viscosity and low potassium crystalloid preservation solution with osmolarity slightly higher than the intracellular space [310 mOsm/L]. Weiss et al. [9] showed that endothelial layer integrity was lost after 2 h in human SVGs stored in HTK. Similarly, human SVG had worse endothelial and SMC function when preserved in the HTK solution versus the UWS solutions [36]. In contrast, Schaeffer et al. [37] have assessed endothelial permeability by measuring peroxidase accumulation in the subendothelial space of rabbit carotid arteries perfused by different solutions [NS, Ringer’s lactate, St Thomas’s solution and HTK]. The HTK solution resulted in better endothelial preservation.

TiProtec™

This solution is an N-acetylhistidine-buffered storage solution consisting of a low concentration of sodium [16 M] enriched with potassium [93 M], N-acetylhistidine [30 M], glycine [10 M], and the iron chelator defetoxamine. Garbe et al. [38] evaluated several parameters of human internal mammary rings preserved in a cold solution of TiProtec for up to 25 days. The authors reported that TriProtec better preserved endothelium-dependant and independent relaxation when compared to HTK and NS solutions. Similarly, Veres et al. [39] reported better vasorelaxation in rat aorta preserved in TiProtect for 2 h when compared to those stored in saline or HTK. More importantly, Wilbring et al. [40] recently compared SVG preservation in the TiProtec versus the NS solution4. Saphenous vein grafts immersed in the TiProtec solution had a better vessel wall contraction and endothelial-dependant vasodilation.

He solution

The He preservation solution composition aims to provide a relaxation of the overdistended saphenous vein using rapid onset and long-acting vasodilators [glyceryl trinitrate and verapamil]. He et al. [41] reported that preservation and irrigation of SVG with their solution during harvesting resulted in relaxation of contraction induced by potassium or thromboxane for up to 2 h after harvesting.

Plasma-Lyte

The anionic composition and the lack of calcium of the solution result in a venous relaxation. Sanchez et al. [21] compared isometric-tension recording of canine and human SVG emerged in Plasma-lyte and NS containing norepinephrine. Plasma-lyte completely relaxed the SVG within 20 min, while veins remained partially constricted with NS. More recently, Wise et al. [42] compared porcine SVG harvested using a traditional technique [an unregulated distension, marking with traditional skin marker and preserved in heparinized NS] or an improved technique [a pressure-regulated distension, marking with brilliant FCF-based pen and preservation inPlasma-lyte] preparations. The improved approach was associated with better SMC and endothelial viability.

Glutathione-ascorbic L-arginin

This solution has an antioxidant effect offered by glutathione and L-ascorbic acid and induces nitric oxid [NO] production by the addition of arginine, a substrate for endothelial cell nitric oxide synthase. Therefore, the glutathione-ascorbic L-arginin (GALA) solution was hypothesized to result in better endothelial-dependent relaxation and cell viability preservation when compared to other preservation solutions. This has been investigated by Thatte et al. [43, 44] who compared human SVG preserved for up to 24 h at 21 °C in the GALA solution against other preservation solutions. The cell viability was maintained in the GALA group when compared to AHB and NS. In addition, vein segment structural analysis using a transmission microscopic evaluation revealed a preserved smooth cell with the GALA solution. Finally, vascular function assessed by calcium mobilization and NO production was maintained up to 5 h with the GALA while it was lost 3 h after preservation in NS and AHB. An ongoing randomized, double-blinded trial started in 2014 enrolled 119 patients undergoing CABG surgery and is aiming to compare storage of harvested SVG in the GALA solution versus heparinized NS [clinical trial protocol number: NCT02272582]. The primary endpoint is graft patency at 1 year after CABG using multi-detector computed tomography angiography. The follow-up is expected to be achieved in January 2018.

Future perspective

The best preservation solution has a physiologic PH and provides substrates for NO production. However, in the survey from Williams et al. [6] on 90 US centers, only 40% use buffered solutions in their routine CABGs, highlighting potential for practice improvement. Most of the available studies have used ex vivo parameters that were extrapolated as markers of endothelial dysfunction. Therefore, to achieve a broader adoption of buffered preservation solutions, studies looking to short- and long-term graft patency with these solutions are needed. In addition, other avenues should be explored in order to improve vein graft patency. Indeed, gene therapies primarily target the proliferative and inflammatory processes leading to IH [45, 46] and have shown favorable clinical outcomes in CABG patients [47, 48]. In addition, treatment of vein graft with monoxide of carbon has resulted in the inhibition of arterialized vein grafts intimal hyperplasia [49] and could be used as an adjunction to preservation solutions. Finally, though more complex, external stenting of SVG showed better lumen uniformity and reduced IH on follow-up angiography and intravenous ultrasound [18].

Conclusion

The saphenous vein graft failure is a complex mechanism that could be mitigated during harvesting. The best preservation solution preserves the structure and function of the graft endothelial during warm ischemia. The use of standard preservation solution, namely normal saline and autologous heparinized blood, has been found to be harmful to the endothelial integrity and potentially adverse clinical outcomes. Up to now, only small in vitro studies have demonstrated the superiority of buffered solutions over standard substrates. However, to determine the real benefit of these solutions, further clinical studies are needed.

Notes

Funding

No extramural funding was obtained for this work.

Compliance with ethical standards

Conflicts of interest

Louis Paul Perrault discloses a financial relationship with ClearFlow and Somahulation as a member of the scientific committee. All other authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Informed consent was not necessary for the review article.

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Copyright information

© Indian Association of Cardiovascular-Thoracic Surgeons 2018

Authors and Affiliations

  • Ismail Bouhout
    • 1
  • Walid Ben Ali
    • 1
  • Louis Paul Perrault
    • 1
    Email author
  1. 1.Department of Cardiovascular SurgeryMontreal Heart InstituteMontrealCanada

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