Open Access

An overview of AVF maturation and endothelial dysfunction in an advanced renal failure

Renal Replacement Therapy20173:42

https://doi.org/10.1186/s41100-017-0123-x

Received: 13 March 2017

Accepted: 25 July 2017

Published: 2 October 2017

Abstract

Life expectancy in patient with established kidney failure is considerably shortened with worsening quality of life. Through the provision of renal replacement therapy, survival and quality of life of advanced renal disease patients can be markedly improved. Haemodialysis and peritoneal dialysis are the treatment modalities in patients with end-stage renal disease. The efficiency of haemodialysis treatment relies on the functional status of vascular access. Vascular access and its related problems represent the main factors that determine a rise in the rate of incidence of the disease among haemodialysis patients and, consequently, a rise in the healthcare expenses. Arteriovenous fistula is the most efficient method, as it has a low risk of infection and mortality, and can ensure long-term functional access. However, maturation of an arteriovenous fistula is a complex process and is not well understood; significant numbers of arteriovenous fistula fail to develop sufficiently prior to their use for haemodialysis due to either lack of vessel maturation or spontaneous thrombosis. There are multiple blood markers and human factors that contribute to the maturation of fistula. Endothelial function is one of the most important determinants of arteriovenous fistula maturation. Early fistula failure is usually due to thrombosis which can be triggered by haematoma, by low flow rates resulting from low blood pressure, or by a hypercoagulable state. Impairment of endothelial function is associated with decreased arterial remodelling and final venous lumen diameter. Arteriovenous fistula anastomoses need early proliferation of endothelial cells to restore the barrier, permeability, and biochemical monitoring roles of endothelial cells in managing vascular repair, local thrombosis, neointimal hyperplasia, and inflammation. The purpose of this review was to discuss the maturation of AVF and endothelial dysfunction.

Keywords

End-stage kidney disease Renal replacement therapy Haemodialysis Arteriovenous fistula Endothelial dysfunction

Background

Chronic kidney disease (CKD) is a critical condition with considerable public health implications. The global mean (95%CI) CKD prevalence in five stages was 13.4% (11.7–15.1%) and stages 3–5 was 10.6% (9.2–12.2%) [1]. In 2014, the number of adult patients starting renal replacement therapy (RRT) in the UK was 7411 equating to an incidence rate of 115 pmp, compared with 109 pmp in 2013 [2]. There are a number of factors, which have to be taken into account when deciding the usage of RRT in patients suffering from advanced renal disease, such as evaluation of electrolyte and acid-base balance, intravascular volume, uraemia, dietary needs, haemodynamic status, urine output, and the pathology of the disease in each individual case. The benefits of RRT have to be compared with the possible hazards of surgical intervention, such as bleeding caused by anticoagulants, as well as all types of complications that accompany the central venous access. Many patients with chronic kidney disease are still unknown, because the serum creatinine fails to identify decreasing kidney function, especially in women and old individuals [3, 4]. According to the Quality and Outcomes Framework, the diagnosis of chronic kidney disease and improvement of treatments will be mediated by the introduction of estimated glomerular filtration rate (eGFR) reporting, as well as by the preservation of patient records required of all the UK general practitioners [5].

Dialysis and transplantation provide alternative ways of taking over the work of advanced renal disease patients. The most efficient form of therapy for advanced renal disease patients is a kidney transplant. However, haemodialysis is the next best option. The efficiency of haemodialysis treatment relies on a functional status of vascular access (VA). According to the National Institute for Health and Clinical Excellence Guidelines [6], VA and its related problems represent the main factors that determine a rise in the rate of incidence of the disease among haemodialysis patients and, consequently, a rise in the healthcare expenses. To ensure that the dialysis therapy can be efficiently undertaken, all patients need a fully developed fistula that is appropriate for the process of cannulation. Arteriovenous fistula (AVF) is the most efficient method, as it has a low risk of infection and mortality, and can ensure long-term functional access [7, 8]. Unfortunately, significant numbers of AVF fail to develop sufficiently prior to their use for haemodialysis due to either lack of vessel maturation or spontaneous thrombosis [9].

It is likely that one of the most important determinants of AVF maturation is the ability of the inflow artery and the outflow vein to respond to the increased blood flow that occurs upon anastomosis of the artery and vein [10]. AVF maturation is the ability of the inflow artery and the outflow vein to respond to the increased blood flow that occurs upon anastomosis of the artery and vein. A healthy response to the anastomosis is an increase in blood flow and corresponding increase in shear stress [11] which stimulates the endothelial cells to release nitric oxide (NO) and other vasodilatory substances [12]. The main purpose of this review was to discuss the maturation of AVF and endothelial dysfunction in an advance kidney disease.

Haemodialysis

Progressive and permanent renal failure is most frequently treated with haemodialysis. RRT with haemodialysis does not provide true replacement of renal function. However, by removing waste solutes and excess body water and restoring biochemical and acid-base balance, haemodialysis has considerably improved the morbidity and mortality of end-stage renal disease (ESRD) patients. A suitable type of vascular access has to be created to establish a connection between the circulation system of the patient and the haemodialysis cycle, in order to provide haemodialysis in ESRD patients.

Vascular access problems represent the main determinant of morbidity among haemodialysis patients and put a considerable degree of financial pressure on the healthcare sector [13, 14]. Successful haemodialysis depends on the provision of safe, efficient, and durable vascular access. Establishing and maintaining effective vascular access is a demanding process for both patients and renal services. These demands are set to increase in response to an RRT population that is becoming increasingly dependent on haemodialysis, whilst also increasing in population size, age, and co-morbidity. Vascular access can be divided into three categories: arteriovenous fistula, central venous catheter (CVC) and arteriovenous graft (AVG).

Of these, CVCs are used temporarily to provide vascular access for haemodialysis whilst the patient awaits creation or maturation of an AVF or AVG or because no suitable options for permanent vascular access are available [15]. AVF is considered to provide the best long-term functional vascular access, with a reduced risk of thrombosis or infection, and is the most cost-effective [16]. There are logistical hurdles to this late presentation to renal services, fitness for surgery, suitable peripheral vascular anatomy, delays due to primary or secondary access failure, and slow rates of AVF maturation.

Konner et al. [17] had also obtained a high success rate (70–90%) of native AVF construction in their study on a randomized sample of ESRD patients. Despite the fact that it is not without its problems, the arteriovenous fistula offers better quality access for dialysis as it has a long-lasting primary patency rate, avoids the need for other numerous procedures, and has the most reduced rates of morbidity and mortality among all types of vascular access [18].

Endothelial function

The endothelium is the largest organ in the body consisting of endothelial cells lining every blood vessel. Adults possess enough endothelial cells that cover a surface area of approximately 1 to 7 m2, with a total weight of around 1 kg and a total quantity of 1013–6078 individual cells [19]. In healthy subjects, vascular endothelium has many functions: it can identify hormonal stimuli (vasoactive substances) as well as mechanical stimuli (pressure and shear stress). Endothelial cells regulate inflammation, cell proliferation, coagulation, and vascular tone due to their output of a number of compounded substances [20]. Endothelium produced vasodilatory materials such as C-type natriuretic peptide, various endothelium-derived hyperpolarising elements, prostacyclin, and NO, whereas vasoconstrictor materials are reactive oxygen species, thromboxane A2, angiotensin II, and endothelin-1 [21]. In addition, there are a number of inflammatory regulators, such as nuclear factor-kB, vascular cell adhesion molecule-1, E-selectin, NO, and intercellular adhesion molecule-1 which play an integral part of endothelial function.

Gresele et al. reported that fibrinogen, prostacyclin, thromboxane A2, plasminogen activator inhibitor-1, NO, tissue factor inhibitor, von Willebrand factor, and plasminogen activator act as modulators for haemostasis [22]. Permeability, inflammation, coagulation, cell adhesiveness, and vascular tone are among the variety of local blood vessel operations modulated by endothelium. In medium to large arteries, healthy endothelial cells contribute to the prevention of atherosclerosis by inhibiting platelet activation, limiting the entry of cells and lipids into the vessel wall, and maintaining a non-proliferative and biochemically inactive intima [23].

Endothelial dysfunction

Endothelial dysfunction occurs when there is an imbalance between the vasoconstricting and vasodilating products (produced directly or indirectly by the endothelium) [24]. Endothelial cell dysfunction can be caused by multiple factors such as genetics, advance glycation end products, hyperglycaemia, high blood cholesterol, hypertension, obesity, diabetes, and smoking [25]. It is associated with higher aggregation of platelets and anticoagulant properties; decreased production of NO; higher secretion of cytokines, chemokines, or adhesion molecules; and increased reactive oxygen species production from the endothelium [26]. Furthermore, individuals suffering from chronic kidney failure exhibit endothelial cell dysfunction. There is also a link between metabolic changes to nitric oxide synthase (NOS) and chronic kidney disease [27, 28]. NOS is available to endothelial cells in two types of isoform: inducible and constitutive or iNOS and cNOS, respectively [29]. Physiological vascular dilation is significantly affected by the constitutive isoform. In patients with advanced renal disease, decreased NO production from cNOS has been observed as a mechanism leading to impaired endothelium-dependent vasodilation in uraemia [30]. Furthermore, Passauer et al.’s research found a correlation between reduced NO production and reduced endothelium-based vasodilation in dialysis patients [31]. The major features of endothelial dysfunction are recapped in Table 1.
Table 1

Healthy and dysfunctional endothelium

Healthy endothelium

Endothelial dysfunction

Vasodilatory (↑NO, ↑PGI2)

Impaired vasodilation (↓NO, ↓PGI2)

Decrease oxidative stress, ↓uric acid

Increase oxidative stress (↑ nitrotyrosine and uric acid)

Anticoagulant (↓PAI-1, vWF, P-selectin)

Procoagulant (↑PAI-1, vWF, P-selectin)

Rise in endothelial progenitor cells and decrease molecular markers of damage (circulating endothelial cells, microparticles)

Decrement in endothelial progenitor cells and increase molecular markers of damage (circulating endothelial cells, microparticles)

Anti-inflammatory biomarkers (↓sICAM, sVCAM, E-selectin, CRP, TNF-alpha, IL-6, MCP-1)

Pro-inflammatory biomarkers (↑sICAM, sVCAM, E-selectin, CRP, TNF-alpha, IL-6, MCP-1)

CRP C-reactive protein, IL-6 interleukin-6, NO nitric oxide, PAI-1 plasminogen activator inhibitor 1, PGI2 prostacyclin, sICAM soluble intercellular adhesion molecule, sVCAM soluble vascular cell adhesion molecule, TNF-α tumour necrosis factor alpha, vWF von Willebrand factor

Endothelial dysfunction is also associated with increased oxidative stress and inflammatory changes that play a role in the development and progression of atherosclerosis in the early stages, while they increase the vulnerability of fully developed plaques facilitating their rupture [32]. There are many techniques used to assess endothelial function. These techniques can be either invasive or non-invasive. In invasive techniques, vasoactive agents are delivered via intra-arterial infusion, whilst the response is measured with high-resolution ultrasound or strain gauge plethysmography. In addition, intravascular infusions of vasoactive stimulants can be combined with intravascular ultrasound.

Non-invasive techniques includes ultrasound and magnetic resonance imaging flow-mediated dilatation, salbutamol-mediated endothelial function measured by pulse wave analysis or pulse contour analysis, and peripheral arterial tonometry [33, 34]. Ultrasound flow-mediated dilatation of the brachial artery is the most widely used in clinical research, and it is currently considered a standard for a non-invasive assessment of conduit artery endothelial function [35].

Endothelium dysfunction and AVF maturation

Early fistula failure is usually due to thrombosis which can be triggered by haematoma, by low flow rates resulting from low blood pressure, or by a hypercoagulable state [36]. On the other hand, progressive neointimal hyperplasia in the venous outflow system can lead to stenosis, which can cause late thrombosis of haemodialysis AVF [37, 38]. Arteriovenous fistula anastomoses need swift proliferation of endothelial cells to restore the barrier, permeability, and biochemical monitoring roles of endothelial cells in managing vascular repair, local thrombosis, neointimal hyperplasia, and inflammation [39]. Because the migration and proliferation of endothelial cells are restricted by uraemia, and because uraemia causes abnormal vascular remodelling, neointimal hyperplasia can sometimes be found at the point of anastomosis of VA [40, 41]. This results in primary access failure and ineffective dialysis [42]. A recent study suggested that microvascular endothelial function as measured using peripheral arterial tonometry may be useful as a predictor of AVF maturation and function [10]. Patients who had impaired flow-mediated dilation (FMD) with a median value of 5.0% (3–9) did not find any difference between the patients with successful and/or unsuccessful AVF [10]. The finding of impaired endothelial function in this CKD cohort is similar to what others have shown using both venous occlusion plethysmography techniques [43], and FMD [44]. Owens et al. [45] determined FMD among 25 CKD patients prior to AVF creation and found very similar values (5.8 ± 1.0%). Study explored the correlation between baseline FMD and subsequent change in the diameter of the artery and vein at 3 months after AVF creation and found a positive correlation.

Erdem et al. discovered that during haemodialysis, turbulent flow, intraluminal pressure, and regular needle insertion caused endothelial damage, which led to haemostatic activation in AVF [46]. Wakefield et al.’s study indicated that thrombus development and blood clotting could be stimulated by higher levels of factor V, plasminogen activator inhibitor-1, tissue factor, and von Willebrand factor, as secreted by a dysfunctional venous endothelium [47]. Furthermore, a dysfunctional venous endothelium favours the interactions with circulating tissue factor-bearing microparticles, further triggering localized blood clotting activation [48].

Vascular stenosis of arteriovenous fistula is primarily the result of neointimal hyperplasia [49, 50]. The pathophysiology of neointimal hyperplasia consists of the presence of extracellular matrix deposition and proliferation, adherence, and migration of vascular smooth muscle cell (VSMC), which represents abnormal healing. Sung et al. [51] found that growth factors and cytokines act as semi-regulators for the changes to the VSMC response. Tumour necrosis factor-α stimulates the synthesis of other pro-inflammatory cytokines and adhesion molecules; it has a chemotactic activity for monocytes and stimulates migration and proliferation of VSMC.

The shear stress levels revert back to baseline due to these vascular reactions (Fig. 1). On the other hand, the activation of endothelial cells and proliferation, release of inflammatory and procoagulant substances, and alterations to cellular shape are all events that have been linked to reduction in shear stress and blood flow. This manifests as raised levels of neointimal hyperplasia and vascular constriction [52]. Furthermore, Dardik et al. [53] has revealed that vascular response seems to be significantly influenced by the exact type of shear stress. For instance, matrix metalloproteinase up-regulation, higher proliferation of cells, and a pro-inflammatory environment can be caused by oscillatory shear stress [54]. On the other hand, normal dilatation and endothelial stability are the outcomes of laminar shear stress [55].
Fig. 1

Vascular remodelling responses

Corpataux et al. [56] discovered that the fistula vein instantly deals with huge increase in blood flow following the creation of AVF. Additionally, there is an eventual thickening of the fistula vein wall and dilation of the venous lumen. This allows the fistula vein to effectively deliver sufficient blood for haemodialysis and be regularly needled for dialysis circulation. The next most significant hemodynamic factor that typically influence an AV fistula is the circumferential or transmural pressure. Transmural pressure is produced inside the blood vessel, and previous studies [57, 58] have shown that increase in transmural pressure lead to an activation of smooth muscle cells, higher levels of extracellular matrix elements, and raised production of cytokine. These pathways invariably lead to the thickening of blood vessel wall, which result in the reduction of transmural pressure which revert back to basal level.

Vanholder et al. [59] and Cardinal et al. [60] indicated that wound healing, migration, proliferation, viability, and other fundamental endothelial cells biological processes are restricted by the uraemic toxins found in the plasma of individuals with ESRD. This is particularly true at the site of haemodialysis vascular access. The failure of these EC processes has played a crucial role in vascular remodelling. According to Chitalia et al. [61], vascular remodelling is negatively impacted by EC dysfunction that is caused by uraemia. The result of this is vascular access failure and can be fatal to patients with ESRD since it is crucial to achieve vascular access for haemodialysis.

Certainly, endothelial cell function is also important, but the most important factor in maturation of AVF seems to be blood vessel selection and surgical technique. Blood vessel selection is one the most important factors in the maturation of AVF. The inadequate vessels used to construct AVFs have been identified as another cause of AVF failure. Zadeh et al. [62] conducted a cross-sectional study using a sample of 96 haemodialysis patients and found an association between the vein diameter and the success rate of fistula development. A vein diameter of <2.5 mm is supposed to be considered inadequate for formation of an AVF, particularly if measurements remain unchanged following the use of tourniquet [63].

Conclusion

The efficiency of haemodialysis treatment relies on a functional status of vascular access. AVF non-maturation is most commonly characterized by a juxta-anastomotic stenosis, a histological level such as aggressive neointimal hyperplasia at the juxta-anastomosis, and an absence of outward vascular remodelling. Currently, we have reasonable understanding of the mechanisms, pathways, pathology, and the pathogenesis of venous neointimal hyperplasia, and vascular stenosis leads to AVF non-maturation. The combination of advances in cellular and molecular pathobiology, biomaterials, and drug delivery techniques has resulted in many innovative therapies for neointimal hyperplasia. There is a need to identify the therapies that are best suited for clinical use in AVF dysfunction.

Abbreviations

AVF: 

Arteriovenous fistula

AVG: 

Arteriovenous graft

CKD: 

Chronic kidney disease

CVC: 

Central venous catheter

eGFR: 

Estimated glomerular filtration rate

ESRD: 

End-stage renal disease

FMD: 

Flow-mediated dilation

NO: 

Nitric oxide

NOS: 

Nitric oxide synthase

RRT: 

Renal replacement therapy

VA: 

Vascular access

VSMC: 

Vascular smooth muscle cell

Declarations

Acknowledgements

Not applicable.

Funding

No funding was obtained.

Availability of data and materials

Not applicable.

Authors’ contributions

MAS conceived the study and supervised the study. MAS and SA drafted the manuscript while DS and TC revised and reviewed the whole manuscript. All authors read and approved the final manuscript.

Ethics approval and consent to participate

Not applicable as a literature review.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

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Authors’ Affiliations

(1)
School of Health Sciences, Queen Margaret University
(2)
Diabetes and Endocrinology, James Cook University Hospital
(3)
Professional Faculties, University of Calgary

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