1. Top of page
  2. Abstract
  3. Introduction
  4. Existing Nonbiological Arteriovenous Grafts
  5. Biological Alternatives
  6. Conclusion
  7. References

The vast majority of arteriovenous grafts (AVG) have been constructed using expanded polytetrafluoroethylene (ePTFE). While ePTFE grafts have the advantage of being relatively inexpensive and easy to manufacture, distribute, ship, and store, their primary patency rates are disappointing when compared with the native AVF. Though use of arteriovenous fistulas (AVF) in the United States has increased substantially, approximately 25% of hemodialysis patients continue to use AVG as their vascular access. We present here a comprehensive review of biological grafts and their use in hemodialysis vascular access. In this review, we discuss the use of synthetics and then explore the evolution of biological grafts over the past 20 years, their clinical impact, and future challenges in widespread clinical use in hemodialysis patients. Provided are in depth descriptions of currently used nonbiological arteriovenous grafts and the recent approaches in increasing the patency of synthetic grafts. Recent technological advances using tissue-engineered AVGs have shown promise for patients receiving hemodialysis and their potential to provide an attractive, viable option for vascular access have been discussed.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Existing Nonbiological Arteriovenous Grafts
  5. Biological Alternatives
  6. Conclusion
  7. References

The National Kidney Foundation’s Kidney Disease Outcomes Quality Initiative (KDOQI) recommends the autogenous arteriovenous fistula (AVF) as the preferred form of vascular access in hemodialysis patients (1,2). A synthetic arteriovenous graft (AVG) is placed when patients cannot support the creation of an AVF. Catheters are also used for hemodialysis, typically as a temporary bridge device while waiting for a functional permanent access. The most recent 2011 data show that the AVG was the vascular access in 19.8% of prevalent hemodialysis patients in the United States, a marked reduction from 37.8% reported at the end of 2003 (3). Despite this reduction, catheter usage remains high (20.5%), and overall access maintenance costs remain high as well. Indeed, vascular access-related costs account for 1.5% of the United States Center for Medicare and Medicaid Services (CMS) budget, which amounts to approximately $2 billion per year.

For the past 40 years, the vast majority of AVGs have been constructed using expanded polytetrafluoroethylene (ePTFE). While ePTFE grafts have the advantage of being relatively inexpensive and easy to manufacture, distribute, ship, and store, their primary patency rates are disappointing when compared with the native AVF (4,5). The patency of commonly used grafts is independent of the manufacturer and generally more than 50% of the currently placed AVGs require intervention within 12 months (6,7). AVGs as well as other small diameter synthetic conduits, such as lower limb bypass grafts, are plagued by failures related to neointimal hyperplasia, surgical experience, anastmotic technique, infections, and thrombosis

The primary differences between native vessels and synthetic grafts that may contribute to loss of patency are lack of a functional endothelium, compliance mismatch, and inflammatory reactions that can trigger hyperproliferation of the surrounding tissue (8). Preemptive percutaneous transluminal balloon angioplasty (PTA), as well as thrombectomy, is commonly used to maintain and restore blood flow (9). Stent grafts (stent with embedded graft material) may offer more sustained patency at the site of stenosis, but long-term results for patency of the access circuit are not known (10,11). There is therefore an urgent need for new solutions to improve the outcomes of AV access. Recent advances in the use of biological grafts may provide improved outcomes (12). In this review, we briefly discuss the use of synthetics and then explore the evolution of biological grafts over the past 20 years, their clinical impact, and future challenges in widespread clinical use in hemodialysis patients.

Existing Nonbiological Arteriovenous Grafts

  1. Top of page
  2. Abstract
  3. Introduction
  4. Existing Nonbiological Arteriovenous Grafts
  5. Biological Alternatives
  6. Conclusion
  7. References

Table 1 summarizes the most commonly used synthetic grafts. Infection rates of synthetic AVG are 4- to 5-fold higher than those of AVFs (13,14). Synthetic materials are susceptible to infection because they provide an ideal surface for the adhesion of micro-organisms. Grafts can become infected either during the implant procedure or secondarily as the result of seeding with micro-organism during needle insertion from either the skin or an endogenous source. Once attached to a synthetic surface, a biofilm forms and encapsulation in the perigraft space can prevent effective phagocytosis (15). When antibiotics fail, excision of the infected graft is often necessary.

Table 1.   Common synthetic grafts implanted as arteriovenous access in hemodialysis patients
NameKey elementsAdvantagesDisadvantagesComment
  1. ePTFE, expanded polytetrafluoroethylene.

ePTFE Low porosity (<30 μm internodal distance) High Porosity (>45 μm internodal distance)Expanded teflon material into node and fiber structureThe most common graft used in hemodialysis vascular accessNot suitable for early cannulation. Stenosis at the vein-graft anastmosis is the most common cause of thrombosisAlthough porosity conventionally was defined on the basis of distance between nodes (inter nodal distance), the actual dimension of voids is defined by spaces between the fibrils
Fibrillar polyurethanePolyurethanePorosity, elasticity, and ease of handling and suitable for early cannulation. Blood surface events similar to woven Dacron than ePTFELacks spaces that allow blood vessels to reach through the entire wall thicknessPreferred when immediate or early cannulation is desired. Not suitable for anastmosis to small veins. Poor patency when anastmosed in a loop configuration
Foamy polyurethanePolyurethaneBlood surface layer more pronounced than on ePTFE and thicker pannusDegree of ingrowth is more pronounced than fibrillar typePreferred when immediate or early cannulation is desired

In addition to ePTFE, polyurethane is used for prosthetic grafts. This material has the benefit of early postoperative cannulation, often within the first 24 hours (16), possibly allowing for complete catheter avoidance in patients who present acutely with a need for dialysis. This leads to considerable cost savings and decreased morbidity associated with central catheter use. However, the polyurethane graft is limited by its increased propensity toward kinking, a steep learning curve for surgeons, and the inability to use Doppler ultrasound for early blood flow monitoring (17).

Regardless of the type of synthetic graft used, this kind of prosthesis lacks a functional endothelium and is unable to be endothelialized in vivo. Unlike in large diameter grafts, lack of a functional endothelium may be a major contributor to failure in small-diameter applications (18). Endothelial cells (ECs) create a nonthrombogenic layer associated with reduced clotting and thrombosis as well as downstream cellular activity that may prevent distal stenosis. Early results with perivascular allogeneic ECs suggest a decrease in venous outflow stenosis, indicating that the lack of a functional endothelium is a key shortcoming of synthetic AVG’s (19).

A number of approaches have been explored to improve the patency of synthetic grafts (Table 2). In 1987, Zilla reported seeding endothelial cells into the lumen of polytetrafluroethylene grafts used for lower limb bypass, creating a functional endothelial lining (20). Further studies showed improved patency in these grafts over ePTFE alone. Although the risk of an inflammatory response and the subsequent hyperplasia associated with the implant of synthetic material is not eliminated, this novel hybrid approach is credited with being a forerunner to modern cardiovascular tissue engineering.

Table 2.   Recent approaches in increasing the patency of synthetic grafts
Author, publication yearTechnique usedResultsComment
  1. PTFE, polytetrafluoroethylene graft.

  2. Exxcel – Boston Scientific, Oakland, NJ; Tex graft, Stretch Gore – Gore and associates, Flagstaff, AZ.

Davidson et al. [45] 2009Heparin-bound ePTFE grafts (= 83)compared with 67 control ePTFE grafts in hemodialysis patientsAt 12 months clot-free survival was 78% for heparin-bonded grafts and 58% for the ePTFE group (< 0.007)Heparin-bonded grafts group had higher percentage of upper arm grafts compared with ePTFE group (66% vs. 43%< 0.003)
Paulson et al. [46] 2012Sirolimus eluted COLL-R wraps (= 13) in hemodialysis (12 patients) patients and followed up for 24 months12- and 24-month primary unassisted patency was 76% and 38%, respectively. Thrombosis was 0.37 per patient-yearNo control arm is a major limitation of the study
Lee et al. [47] 2006 Kelly et al. [48] 2006 Kohler et al. [49] 2007PaclitaxelInhibits NIH in sheep, porcine AV ePTFE graft modelsDid not translate it to human subjects
Ko et al. [50] 2004Yarn wrapNo improvement in patency in yarn wrapped grafts PPR at 1 year 51% 2 year, 36%Prospective study compared Exxcel yarn PTFE vs. Gore-Tex stretch PTFE grafts
Hiltunen et al. [51] 2000Adenovirus-mediated VEGF–C gene transferNot tested as dialysis access. Preliminary results show technical feasibilityPhase 3 results were suspended
Nugent et al. [52,53] 2002,2007 Lawson et al. [54] 2008Endothelial cell wrapIn porcine models, beneficial effect on patency is shownGel foam wraps in porcine models done by Nugent Technical feasibility shown with vascugel wrap in hemodialysis patients by Lawson
Luo et al. [55] 2005β-Adrenergic receptor kinase inhibition of G protein signalNot implanted in dialysis patients.No data in dialysis patients
Burke et al. [56] 2008Recombinant elastase PRT-201Phase 2 study results showed technical feasibility, improved patency, and safetyPhase2 b results are awaited
Christi et al. [57] 2011Autologous adipose tissue grafts with Glitazones increasing release of adiponectinStudies conducted in Porcine models onlyNo human studies conducted

Despite 50 years of research with new biomaterials, mechanical design, surface modifications, and interventional strategies, AVGs still have dramatically reduced primary and secondary patency rates compared with AVF. Recent advances with biological materials may provide a promising alternative to these synthetic approaches (12).

Biological Alternatives

  1. Top of page
  2. Abstract
  3. Introduction
  4. Existing Nonbiological Arteriovenous Grafts
  5. Biological Alternatives
  6. Conclusion
  7. References

The small-diameter tissue-engineered vascular graft has long been hailed as the “holy grail” of vascular tissue engineering (21,22). Figure 1 summarizes the key historical research time points in the development of biological grafts. Limitations of prior research studies in animal models have been summarized in Box 1. Four basic approaches have been employed toward reaching this goal: (i) xenogeneic or allogeneic conduits, (ii) cell seeded bioresorbable scaffolds, (iii) creation of vascular grafts with autologous cells in vivo, and (iv) Scaffold-free creation of blood vessels in vitro utilizing tissue engineering by self-assembly (TESA).


Figure 1.  History of research and development in vascular grafts.

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Table Box 1..   Limitations of research studies of synthetic grafts in animals [REF]
1. Inappropriate animal models were used that missed the clinical relevance
2. Transanastmotic endothelialization rather than transmural or blood borne endothelialization was studied
3. A majority of studies examined the role of mid-graft endothelialization using short graft lengths and long implantation periods. These grafts were therefore fully endothelialized at the time of explantation
4. In older (senescent) animal models and in human subjects, progressive inhibition occurs for transmural ingrowth compared with younger (juvenile) animals, which often allow complete transmural endothelialization
5. Animal models did not simulate the flow conditions of grafts implanted in humans
6. Transarterial endothelialization rates for a given animal model are unknown and comparing one animal model with the other is imprecise

Xenogeneic or Allogeneic Conduits (Bovine Mesenteric Vein, Cryopreserved Femoral Vein, and Bovine Carotid Artery)

Xenogeneic conduits have been explored as an alternative to synthetic grafts. Composed of bovine mesenteric veins, bovine carotid arteries, or human cryopreserved femoral veins, glutaraldehyde cross-linking and gamma-irradiation render harvested bovine vessels resistant to host rejection and degradation, and the presence of elastin within the graft leads to improved compliance as compared with ePTFE (23).

Although patency rates are comparable to ePTFE, the use of bovine mesenteric vein grafts (ProCol) and cryopreserved femoral veins are limited by their low overall mechanical strength and increased rate of pseudo aneurysms. However, there is no significant difference in infection rates (24–28). Bovine carotid arteries, when used as AVGs, have a higher incidence of rupture when they become infected and more variable cumulative patency rates, ranging from 21% to 86% at 1 year and from 45% to 76% at 2 years (29,30). More recently, improved results have been reported (31). Furthermore, a xenogeneic graft is 3–6 times more expensive than ePTFE. Cumulatively, these commercially available products have failed to make a significant impact beyond niche applications.

Another xenogeniec approach was reported by Ketharnathan et al. in 1980. This biosynthetic device was composed of glutaraldehyde-tanned bovine collagen grown around polyester mesh templates and then implanted underneath the muscle of adult male sheep. After a period of 12–14 weeks, these grafts, called Omniflow, were implanted in a canine model (32). In a study of the Omniflow and Omniflow II grafts, 720 hemodialysis accesses were compared (429 AVFs, 291 AVGs and 59 Omniflow/Omniflow II grafts). One-year primary patency rates were 70% for AVFs, 41% for ePTFE grafts, and 54% for the Omniflow grafts (33). In addition, the Omniflow grafts also had a low infection rate of 2% (34). A more recent study by Palumbo et al., has demonstrated primary patency rates of 80% at 1 year and a similarly low infection rate (35).

Bioresorbable Scaffolds

While biological vessels derived from allogeneic or xenogeneic tissues have failed to make a significant clinical impact, advances in cell culture techniques have introduced the possibility of a lab grown vessel, as first seen in Eugene Bell’s work in the 1980s. A pioneer in cardiovascular tissue engineering, Bell created the first tissue-engineered blood vessel by casting a mixture of collagen and vascular cells into a tubular mold. Although the vessels exhibited low bust strengths and had to be reinforced through the use of a Dacron sleeve, this visionary work set the stage for the field of cardiovascular tissue engineering.

Mechanical strength is one of the most important attributes of a functional arterial vascular graft. Many biological approaches have struggled to produce grafts with the required strength to perform clinically as they have been plagued by late-stage aneurysmal failure. As a result, tissue engineers have focused their efforts on the use of bioresorbable materials to provide initial strength and structure. Tubular constructs created from these scaffold materials are then seeded with autologous cells to produce a tubular vascular graft. As the graft matures after implantation, the scaffold is broken down and replaced with biological material. However, this process is highly dependent on the polymer design (material, porosity, and geometry), indication for use, local mechanical environment, as well as other patient-specific factors. Furthermore, long-term mechanical strength and patency of the graft are reliant on the delicate balance between resorption of the biodegradable material by the body and deposition of new extracellular matrix. Thus, even if adequately strong tissue-engineered blood vessels can be built, achieving the appropriate design that is applicable to all patient populations and indications is a complex and serious challenge.

Despite numerous complexities, there have been several successful advances with the scaffold model. In 2001, Shin’oka reported the implantation of a tissue-engineered blood vessel, created by seeding autologous bone marrow cells into a porous biodegradable scaffold composed of a copolymer of l-lactide and β-caprolactone (36). The graft was used to reconstruct the pulmonary artery and as a cavopulmonary connection graft in young patients. Although these grafts were implanted in a low-pressure system and therefore not directly applicable for vascular access, this was a major advancement and Shin’oka is credited with the first human use of a tissue-engineered blood vessel. In 2005, the same group reported results of grafts prepared with a shorter incubation period of 4 days (37). Using an approach that evolved out of the same laboratory, Niklason and colleagues reported promising preclinical results with a tissue-engineered vascular graft intended for hemodialysis access. These grafts have been placed in baboons for at least 6 months and 12 months in dogs and they are being prepared for initial clinical use (12,38).

Nieponice introduced a novel method for seeding cells into synthetic scaffolds in 2008. A rotational vacuum seeding device was used to seed large numbers of muscle-derived stem cells into a biodegradable bilayered elastomeric scaffold, mimicking the natural structure of a blood vessel. The fibrous outer layer of the scaffold, created by a process called electrospinning, provided mechanical strength for the construct. The internal layer was extremely porous and readily infiltrated by cells. Bench-top mechanical testing showed that the resulting graft had properties similar to that of the coronary artery, although the model has not yet been used clinically, and it is unclear if there will be an inflammatory response to the synthetic scaffold.

Creation of Vascular Grafts with Autologous Cells In Vivo

Eliminating the use of exogenous biomaterials to create a completely biological graft may decrease the risk of rejection secondary to chronic inflammation. Directing cells to produce a scaffold to provide the necessary mechanical strength and structure would eliminate the immune response caused by an exogenous scaffold material or the byproducts of its breakdown.

Inspired by the pioneering work of Sparks in the late 1960s, researchers including Campbell experimented with vascular graft production in vivo by implanting various kinds of tubing into the peritoneum and pleural cavities in multiple animal models. After several weeks, the tubes became encapsulated by layers of myofibroblasts, collagen, and mesothelium. These tissues were explanted and the tube was removed from the inside of the explant. This created a tubular piece of tissue that was then reimplanted into the animal’s carotid artery to function as a vascular graft with relatively good patency (39,40).

A similar process was also used by Sakai in 2007 in which a device composed of a tube with an attached “wing” was implanted into the peritoneal cavity (41). As the device became encapsulated, a cell sheet formed on the “wing.” This sheet was then rolled around the tube and reintroduced into the patient for further incubation. After the final incubation, the mature graft had thick walls with a high burst pressure of around 4000 mmHg.

Although the grafts created by Campbell and Sakai can be produced relatively quickly and are completely biological, the results have not yet been applied to a human model. Biological differences in healing mechanisms among species make the transition from animal models to humans difficult. Clinical trials with both models also require extremely invasive procedures and regulatory hurdles may limit their clinical feasibility.

Creation of Blood Vessels In Vitro by Tissue Assembly Without Use of Scaffolds

In 1998, L’Heureux reported the first in vitro creation of a tissue-engineered blood vessel using a completely biological method termed Tissue Engineering by Self-Assembly (TESA) (42). In initial research, the vessel was composed of distinct layers, specifically a functional endothelium, a medium of smooth muscle cells and an adventitia composed of fibroblasts. It was determined that presence of the smooth muscle layer had no effect on graft patency, despite the contractility that the layer contributed, and the smooth muscle cell layer was eliminated. Removal of the media layer markedly reduced the complexity of the graft. The production process became more streamlined as the need for multiple culture conditions and additional quality control measures was eliminated.

Production of the optimized graft began with fibroblasts harvested from a small skin biopsy to grow robust cellular sheets. These sheets were then rolled around a support mandrel, cultured to allow the layers to fuse, and then dried to form the internal membrane of the graft. A second sheet, the adventitia, was then rolled around this decellularized internal membrane and the two-ply construct was returned to culture. After a maturation time of 10 weeks, the lumen of the vessel was seeded with endothelial cells, harvested from a superficial vein biopsy, to create a three-layered vascular graft. The grafts produced by this method had supra-physiological burst pressures of around 3500 mmHg. Initial implantation studies performed in dog and rat models provided patency rates high enough for the translation to human trials. In 2006, the use of vessels created by a streamlined version of this technique was first reported in humans as AVGs for hemodialysis access. This represented the first human use of a tissue-engineered vascular graft in high-pressure arterial circulation (43).

In 2009, expanded results from the trial were reported (44). Patients who were not suitable candidates for creation of AVF with a history of access failure were recruited. Skin and small vein biopsies were taken from 10 participants in a minimally invasive outpatient procedure and used to produce living autologous grafts as previously described and implanted as AV-shunts (Fig. 2).


Figure 2.  Tissue engineered human blood vessel.

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Although some early graft failures were reported, they were the result of an immunological reaction to high levels of IgG found the bovine serum used in the culture of the graft. Reducing the level of this protein resulted in grafts with extremely encouraging long-term results. Even including the serum-related failures, overall, there was a 4.2-fold reduction in intervention rates relative to preoperative events in the 6 months prior to implantation with follow-up out to 3 years. More recently, the first implant of an allogeneic version of this graft was reported. Like the autologous cohort, with time points out to nearly 1 year, this allogeneic graft demonstrated a dramatic reduction in graft-related events relative to preoperative rates. This suggests that an off-the-shelf version, suitable for widespread clinical use, is a possibility (38).


  1. Top of page
  2. Abstract
  3. Introduction
  4. Existing Nonbiological Arteriovenous Grafts
  5. Biological Alternatives
  6. Conclusion
  7. References

Although existing synthetic arteriovenous grafts are relatively inexpensive and readily available, they have poor patency when compared with the native AVF. Alternative approaches, including xenogeneic grafts, bioresorbable scaffolds, and scaffold-free models have been studied, but have not achieved widespread clinical use due to various limitations. Recent technological advances using tissue-engineered AVGs have shown promise for patients receiving hemodialysis and may provide an attractive, viable option for vascular access.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Existing Nonbiological Arteriovenous Grafts
  5. Biological Alternatives
  6. Conclusion
  7. References
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