Review JVA The Journal of Vascular Access The Journal of Vascular Access 2021, Vol. 22(1S) 63–70 The role of Doppler ultrasonography ª The Author(s) 2020 in vascular access surveillance— Article reuse guidelines: sagepub.com/journals-permissions controversies continue DOI: 10.1177/1129729820928174 journals.sagepub.com/home/jva Jan Malik1,2 , Carlo Lomonte3, Mario Meola4 , Cora de Bont5 , Robert Shahverdyan6, Joris I Rotmans7 , Francois Saucy8, Tamara Jemcov9,10 and Jose Ibeas11 Abstract Chronic hemodialysis therapy required regular entry into the patient’s blood stream with adequate flow. The use of arteriovenous fistulas and grafts is linked with lower morbidity and mortality than the use of catheters. However, these types of accesses are frequently affected by stenoses, which decrease the flow and lead to both inadequate dialysis and access thrombosis. The idea of duplex Doppler ultrasound surveillance is based on the presumption that in-time diagnosis of an asymptomatic significant stenosis and its treatment prolongs access patency. Details of performed trials are con- flicting, and current guidelines do not support ultrasound surveillance. This review article summarizes the trials performed and focuses on the reasons of conflicting results. We stress the need of precise standardized criteria of significant access stenosis and the weakness of the metaanalyses performed. Keywords Hemodialysis, hemodialysis vascular access, ultrasonography, arteriovenous fistula, arteriovenous graft Date received: 19 December 2019; accepted: 17 April 2020 1 Center for Vascular Access, General University Hospital and First Faculty of Medicine, Charles University, Prague, Czech Republic 2 Introduction 3rd Department of Internal Medicine, General University Hospital and First Faculty of Medicine, Charles University, Prague, Czech Republic 3 Only few other hemodialysis access topics are more pas- Division of Nephrology, Miulli General Hospital, Acquaviva delle Fonti, sionately debated as ultrasound surveillance. The invention Italy 4 Institute of Life Sciences, Sant’Anna of Advanced Studies and of arteriovenous fistulas (AVFs) and arteriovenous grafts Department of Internal Medicine, Pisa University, Pisa, Italy (AVGs) as vascular access for hemodialysis considerably 5 Vascular Laboratory, Bravis Hospital, Bergen op Zoom, The decreased patients’ morbidity and mortality. The patency Netherlands 6 of AVFs and AVGs is being threatened mostly by the Vascular Access Clinic, Asklepios Clinic Barmbek, Hamburg, Germany 7 development of a stenosis, which can lead to access dys- Department of Internal Medicine, Leiden University Medical Center, The Netherlands function, inadequate dialysis, and/or access thrombosis. 8 Service of Vascular Surgery, Department of Heart and Vessels, The latter represents an acute risk of access abandonment, University Hospital, Lausanne, Switzerland 9 and its therapy is more complicated and painful and cost- Department of Nephrology, Clinical Hospital Centre Zemun, Belgrade, lier than the treatment of a (significant) stenosis. It seems, Serbia 10 School of Medicine, University of Belgrade, Belgrade, Serbia therefore, logical that treating significant stenoses before 11 Nephrology Department, Parc Taulı́ University Hospital, Parc Taulı́ thrombosis occurs should be beneficial. However, it Research and Innovation Institute (I3PT), Autonomous University of remains unclear when the risk of acute thrombosis due to Barcelona, Barcelona, Spain stenosis is high enough to justify the preemptive interven- tion. Moreover, the definition of a hemodynamically sig- Corresponding author: Jan Malik, 3rd Department of Internal Medicine, General University nificant stenosis varies between centers. Hospital and First Faculty of Medicine, Charles University, U nemocnice Stenosis is a vessel narrowing that could cause signifi- 1, 128 08 Prague, Czech Republic. cant pressure drop and flow volume decrease, but also Email: jan.malik@vfn.cz 64 The Journal of Vascular Access 22(1S) trigger mechanisms of thrombosis due to endothelial cell Table 1. Complex criteria of a significant vs borderline denudation and both platelet and von Willebrand factor stenosis—according to Malik et al.13 and Ishii et al.14 activation in the case of very high shear stress (*flow Significant Borderline velocity).1,2 The presence of a stenosis can be detected by routine physical examination and/or by signs of dys- Main criteria function that manifest themselves during the dialysis ses- Diameter reduction by >50% Peak systolic velocity increase >2–3 sion (monitoring). Such stenoses are clinically significant Additional criteria (1): and include edema anatomically distal to the venous ste- Residual diameter <1.9–2.0 mm No additional nosis, prolonged bleeding, needling problems, fall of flow Flow volume decrease by >25%a) criterion volume, decrease of dialysis dose due to higher recircula- Flow volume <600 mL/min for AVGs, <500 tion, and so forth. However, the accuracy of clinical diag- mL/min for AVFs nosis of a stenosis depends on the stenosis location, on If only the main criteria are present, the stenosis is borderline and ree- vascular access and patient’s characteristics (depth, flow valuation is indicated within 6–8 weeks. Significant stenoses are indicated volume, vein branching, and compliance), and highly on to correction. a the experience of the hemodialysis unit team, which is not Flow volume decrease by >25% if the previous value was <1000 mL/min. always optimal.3,4 In a recent study by Castro et al.,5 the clinical suspicion on AVF stenosis was not confirmed in There is a general agreement that clinically significant 27% of cases. Some stenoses remain clinically asympto- stenoses should be treated. In these cases, DUS can help to matic, which explains at least part of the “sudden” throm- identify the location of the stenosis, which is important for bosis that develops without any warning signs. All these the appropriate puncture site during the percutaneous pro- reasons led to the development of surveillance techniques. cedure. A debate continues about the indication of asymp- Surveillance is defined as the periodic evaluation of the tomatic stenoses diagnosed by any imaging method. We vascular access by using diagnostic tests that may involve believe that only the usage of strict diagnosis criteria could special instrumentation and staff and for which an abnor- justify the ultrasound surveillance. mal test result suggests the presence of dysfunction.6 The rationale of surveillance is based on the hypothesis that corrective intervention of an identified progressive stenosis Stenosis definition by DUS (such as percutaneous transluminal angioplasty (PTA)) can prevent complete occlusion of AVF/AVG and prolong Several criteria have been used for the description of a access lifespan.7 Besides regular access flow volume mea- significant stenosis by DUS. surement using dilutional techniques, Doppler ultrasono- graphy (DUS), is the most investigated and used method. Percentage of diameter reduction The main advantage of DUS is its ability to provide non- Percentage of diameter reduction is the oldest morpholo- invasive, precise, and reproducible data on the morphology gical assessment of a stenosis, used not only in DUS, but and flow dynamics of the arteriovenous access.8 However, also in angiography. The main problem of this criterion is a number of trials have been published, and the data about that the outflow veins have typically irregular lumen, so DUS surveillance benefits were conflicting.9–13 In the there is frequently no reference segment for the estimation absence of precise standardized definition of a significant of stenosis percentage in AVFs. Moreover, many stenoses stenosis or adequate level of experience, DUS (but also are asymmetric, and then the estimated severity of the angiography) could be an operator-dependent method and, stenosis depends on the direction from which it is viewed. indeed, the indication to preemptive therapy (¼ significant Stenosis visualization in two perpendicular directions stenosis) differed from study to study. The absence of strict could lessen this limitation. Nevertheless, it is diameter ultrasound diagnostic criteria of an asymptomatic stenosis narrowing in B-mode (and in color Doppler), which turns could explain the lack of surveillance benefit in some trials, the attention of the examiner to the particular vessel seg- and we describe them in detail below and in Table 1. ment. Percentage of stenosis (>50%) was used as the single Moreover, the technology of DUS has improved consider- criterion of significance in some trials.9–11 Using only this ably since the first reports of AVF/AVG ultrasound exam- criterion is unreliable because B-mode does not always ination and (negative) trials of surveillance, and its delineate low-echogenic structures, such as intimal hyper- improvement is an ongoing process. The higher working plasia, degenerative venous valves, or recent thrombosis. frequency of the ultrasound probes provide better axial spatial resolution, and the higher frame rate corresponds to the higher temporal resolution. Moreover, the size of the Peak systolic velocity ultrasound devices has decreased considerably, which led Peak systolic velocity (PSV) increase in comparison to a to their easier transportation even to the patients’ beds and non-stenosed segment is another widely used criterion.8–13 hemodialysis chairs. The velocity increase is caused by the stenosis itself and by Malik et al. 65 Figure 1. Correct orientation of the Doppler angle in the vas- Figure 2. Flow volume measurement in the graft. cular lumen. The flow volume calculation is based on the following formula: Qa The cosinus of the Doppler angle is a part of the equation ¼ pr2  TAMEAN, where r is the radius of the examined graft transforming the Doppler frequency shift into the velocity. and TAMEAN is the time-averaged mean velocity inside. The Therefore, it should be always the same for the follow-up. Man- latter is an integral value during the heart cycle of the average ufacturers set it usually to 60 . velocity layer (flow velocity is the fastest in the middle and the slowest along the vascular wall). TAMEAN must not be replaced by TAMAX, which is the time velocity integral of the fastest the recirculation zone due to flow turbulence just behind the velocity only—using TAMAX would lead to significant overesti- stenosis. Sometimes it is expressed as a PSV ratio (PSR). mation of Qa. Pulse wave Doppler sample size should be wide AVG stenosis with PSR 2.0–2.9 had 50%–74% stenosis on enough to cover most of the vessel lumen because of the different angiography, and AVG stenosis with PSR  3.0 had 75% speeds of blood inside the vessel from the center to the wall. stenosis.12 The velocities should be always recorded by the same Doppler angle, which is usually set to 60 by the ultrasound manufacturers (Figure 1), but could be changed appropriately by the examiner. It should not exceed 60 . This is related to the formula that calculates the velocity, which includes the cosine of the angle in the numerator. Irregular (asymmetrical) stenoses cause higher pressure drop and velocity increase than symmetrical stenoses of the same area reduction.15 The velocity increase mirrors the pressure gradient caused by the stenosis according to the Bernoulli equation. This is because the outflow vein is softer or easily collapsible and anatomically proximal to a significant steno- sis during palpation or ultrasound evaluation. The use of absolute PSV values as the only criterion is confounding Figure 3. RD measurement. because the increase of PSV does not have the same signifi- There is excessive intimal hyperplasia in the outflow vein causing cance when it is or it is not associated to a drop of the flow rate the stenosis. By diameter reduction, this stenosis would be significant if compared with the left or right part of the vein. Nevertheless, the RD is 2.35 mm, so this stenosis was considered Flow volume (Qa) borderline, and soon, reevaluation (within 6–8 weeks) was indicated. Flow volume (Qa) is frequently considered as the function of the access and is obtainable during DUS examination. For precise values, it has to be measured in a straight vascular ischemia.17 In considering preemptive correction, studies segment free of stenoses. In AVFs, Qa is usually measured regarded stenoses as significant either at a flow volume in the brachial artery, supposing that the vast majority of the decrease by 20%–25% and/or at a cut-off value of <500– flow volume (>90%) enters the AVF. In AVGs, Qa is mea- 600 mL/min.13–14,18–20 However, the problem is that the sured directly in the graft close to its venous anastomosis actual Qa does not depend only on stenosis severity, but (Figure 2). Low values are linked to higher thrombosis risk16 also on the actual hydration status and blood pressure similar and to increased blood recirculation, with subsequent to and in relation with the cardiac output. Natural/physiolo- decrease of the dialysis dose—Kt/V (especially in the pop- gic variation of repeated Qa exceeds 20%.21 It is advisable ular high-flow regimes). On the contrary, high Qa could be to validate Qa values obtained by DUS with dilutional tech- detrimental for the heart or could be responsible for hand niques performed during hemodialysis. 66 The Journal of Vascular Access 22(1S) Residual diameter (RD) of the stenosis could be pre- in AVFs after their creation, although the optimal criteria cisely analyzed by the modern high quality ultrasound are discussed.31 devices (Figure 3).8 The cut-off value <2.0 mm was arbi- AVF/AVG thrombosis, however, can also develop not trarily set and confirmed clinically when used as a part of only because of stenosis progression, but also due to other the “complex stenosis criteria” in AVGs13,22,23 and vali- mechanisms, such as hypotension, dehydration, unwished dated against angiography.8 In AVFs, an Australian study outer compression during sleep, thrombophilia, and so showed that the RD < 2.7 mm was associated with 90% forth. Moreover, the aforementioned complex stenosis cri- sensitivity and 80% specificity of AVF dysfunction.18 teria cannot be used mechanically. One such example is a According to a recent study, RD < 2.5 mm is associated branched AVF—if an outflow vein stenosis is diagnosed, with lower Qa.24 Another current Japanese study with but Qa (measured in the brachial artery) is adequate and the AVFs determined the RD cut-off value to be <1.86 alternative outflow vein (branch) is suitable for hemodia- mm.14 As long as the stenosis is asymmetrical, it should lysis needling, the stenosis could be left without interven- be again visualized by two perpendicular views, and for the tion. Alternatively, when a decreased Qa is calculated, but diagnosis of a significant stenosis, the RD should be below there is no clear high-grade stenosis, it is worth to estimate the cut-off value in both.. patient’s hydration, for example, by the visualization of the The resistive index (RI) of the flow pattern in the feed- inferior vena cava diameter and collapsibility when the ing artery has been tested in several studies, and although it ultrasound device is equipped with abdominal or echocar- is used in the assessment of the transplanted kidney,25 the diography probes.32 Whole-body bioimpedance spectro- results in AVFs and AVGs are not conclusive. Values scopy is frequently used in hemodialysis units for the above 0.6–0.7 indicated stenosis.26,27 The RI is defined assessment of hydration. by the following equation: RI ¼ (PSV  end diastolic velocity)/PSV. RI increases especially in juxtaanastomotic stenoses. Stenoses in AVFs Some centers and trials have used the complex criteria Anatomically distal AVF is the first access of choice. The of a significant stenosis, comprising the combination of more frequent upper extremity fistulas include radio- two main criteria (>50% diameter reduction þ PSR >3) cephalic, ulno-basilic and brachiocephalic fistulas, Gracz and at least one additional criterion (RD, flow volume fistula (median cubital vein attached to the brachial or radial decrease, or low Qa—see Table 1).28 AVG stenoses with artery), and transposed basilic vein. They have a long life- a lack of any additional criterion (¼ borderline stenoses) span, low risk of complications, and their use is associated possess low risk of thrombosis (ca. 1% during 6–8 weeks with the longest life expectancy.33 The main limitation of since the primary diagnosis).22 Only 54% of borderline AVFs is non-maturation, as up to 40%–60% of AVFs are AVF stenoses progressed into significant stenosis in the never suitable for hemodialysis without additional AVF pro- study by Castro et al.5 The complex stenosis criteria (Table cedures to34 facilitate maturation and the maturation rate of 1) have been developed for the “Watch and wait strategy.” AVFs is suggested as a surgical quality indicator.35 Many These criteria were used in the largest randomized trial factors responsible for these unsatisfactory early results have testing ultrasound surveillance and proving its benefit,13 been identified, and they lead to outflow vein or inflow but also in other trials.19,28 Unfortunately, the majority of artery stenoses. Early DUS can identify such stenosis and trials used only >50% diameter reduction as the only cri- provide an indication to percutaneous or surgical therapy— terion of stenosis.9–11 The second largest randomized con- so-called assisted maturation. 36,37 Later on, stenoses trolled trial (RCT) of ultrasound surveillance that did not develop mostly in the outflow vein close to the anastomosis prove its benefit used complex criteria, but included RD < in distal forearm AVFs and more proximally in the outflow 4.0 mm.29 The latter cut-off value is quite high and could vein (cephalic arch) in brachiocephalic AVFs.38 be found in many normally functioning AVFs/AVGs. The key question is this: can ultrasound surveillance provide reliable guidance for the clinician as to which ste- Stenoses in AVGs nosis should be treated and when? The identification of The most frequent AVGs are forearm—they begin at the such high-risk stenosis is based on the understanding of radial or brachial artery and are straight or curved and are stenosis pathophysiology and on their detailed morpholo- attached to the basilic vein. More proximal grafts originate gical and functional (Qa) evaluation.22 DUS enables com- at the brachial or even subclavian artery and are attached to plex evaluation of the stenosis significance, which was, the cephalic or subclavian vein. Lower extremity grafts are however, used only in a few published trials as mentioned created in the case of occluded central veins and are above. Moreover, DUS performed early after AVG cre- straight (between popliteal artery and some groin vein) or ation can also predict future risk of AVG abandonment and looped (femoral artery to femoral or great saphenous vein). thus select high-risk AVGs that could profit from the sur- AVGs have a higher rate of complications and a shorter veillance most.30 DUS is even more frequently performed lifespan than AVFs. Therefore, AVG is the vascular access Malik et al. 67 that is created and recommended especially in patients with Table 2. The use of DUS as answered by the VAS council and abandoned subcutaneous veins, with AVF non-maturation, board members. but also in elderly patients, thanks to AVG’s higher AVF AVG maturation rate.39 Unfortunately, no currently available graft is as good as Do you routinely perform/support ultrasound 75% 75% an AVF that matured without intervention. DUS performed examination after access creation? Do you perform/support duplex Doppler 100% 91% early after AVG creation can predict future complications ultrasound in the case of access problems and thus select patients who would profit more from ultra- (puncture difficulties, limb edema, decrease of sound surveillance.30 AVGs are generally more prone to dialysis dose . . . ?) later stenosis development than AVFs. The typical site of Do you check the access by ultrasound regularly? 55% 55% stenosis development is at the venous anastomosis and at Do you indicate PTA if a severe stenosis is found? 73%a 73%a the adjacent part of the outflow vein. This is caused by the PTA: percutaneous transluminal angioplasty; AVF: arteriovenous fistula; formation of intimal hyperplasia after creation. AVG: arteriovenous graft. Percentage of “YES” is depicted. Cannulation-related stenoses could also develop in the a Half responded “only if symptomatic.” graft itself, especially when the areal puncture technique is applied instead of the recommended rope-ladder tech- metaanalyses are similar: Preemptive stenosis correction nique.40 In this case, the graft wall disruption and subse- of a functional arteriovenous access does not improve quent healing are responsible. Both development of intimal access longevity; although results for native AVF are pro- hyperplasia and puncture healing are slow-acting mechan- mising, existing evidence is insufficient to guide clinical isms, which give time for surveillance.22 practice and health policy. The board and council members of the Vascular Access Ultrasound surveillance in the guidelines Society were asked about their practice in DUS surveil- lance. The results are given in Table 2, and they illustrate Some published vascular access guidelines support DUS as the current uncertainty about the clinical value of vascular a screening tool for detecting stenosis and to perform pre- access surveillance. The results of the largest RCT evi- emptive interventions to prevent the loss of the AV access. denced the benefit of DUS surveillance and preemptive The Kidney Disease Outcomes Quality Initiative (KDOQI) therapy of carefully assessed stenoses.13 On the contrary, clinical practice guideline for vascular access, published in the metaanalyses had negative results.45,46 Nevertheless, 2006, recommended direct flow measurement and DUS as the number of patients included in the metaanalyses is preferred techniques that may be used in AVF surveillance scarce: six RCTs enrolled 612 patients with the primary and preemptive correction of luminal stenosis of >50% endpoint of thrombosis, and four RCTs enrolled 443 when the access flow rate is less than 600 mL/min in patients for access loss.47 Some of the studies included AVGs, and 400–500 mL/min in AVFs, even if the access prevalent patients, while others included solely incident is still able to provide adequate hemodialysis.41 patients at the time of access creation. The most important Recent Spanish guidelines have recommended DUS as differences were, however, in the definition of significant the first visualization method in the case of clinical suspi- stenosis that was indicated to percutaneous or surgical cion on access dysfunction or stenosis, and regarding sur- correction (Table 3). Performing a metaanalysis from so veillance, both DUS and dilution methods for AVFs but not different studies leads therefore to significant oversimpli- for AVGs.42 The European Society for Vascular Surgery fication. The final answer to whether to do or not to do guidelines also recommended DUS as a non-invasive tool DUS surveillance is therefore in including more patients to be the first line imaging method only in patients with with the use of the complex stenosis criteria and clear suspected vascular access dysfunction.43 The new Eur- indication criteria of percutaneous treatment, ideally in a opean Renal Best Practice (ERBP) guideline on AV access multicenter study with defined inclusion criteria and end- specifies that the evidence for surveillance of AVFs is points (thrombosis and cumulative patency). inconclusive and needs more research. In addition, they recommend not to perform routine surveillance of AVGs with access flow measurements or DUS.44 Perspective: is it the time to change the surveillance paradigm? Clinical trials on vascular access Although the guidelines are not favorable, the authors of surveillance this article are convinced that ultrasound should play a Current statements of the societies are based especially on pivotal role in the AVF/AVG management, as it is a precise the results of the metaanalyses.44,45 Their authors included and highly reproducible method in experienced hands. For all RCTs testing the benefit of DUS surveillance and pre- the greater distribution of AVF/AVG ultrasound imaging, emptive treatment of stenoses. The conclusions of both it is necessary to (1) standardize the examination 68 The Journal of Vascular Access 22(1S) Table 3. Duplex Doppler cut-off criteria of a significant AVG stenosis (used as the indication to angiography and intervention)—from the work by Malik et al.28 Diameter Residual Prolonged¼survival Trial first No of subjects reduction Peak velocity Qa Qa cut-off value diameter in ultrasound author US/control in B-mode increase decrease (mL/min) (mm) surveillance arm? Mayer et al.9 35/35 >50% – – – – Yes Lumsden et al.10 32/32 >50% – – – – No Ram et al.11 32/34 >50% – – – – No Robbin et al.29 65/61 >50% >2fold <500 <4.0 No Malik et al.13 97/92 >50% >2fold >25% <600 <2.0 Yes Qa ¼ access flow volume. technique, (2) define the technical demands of the ultra- 2. Remuzzi A and Ene-Iordache B. Novel paradigms for dia- sound devices, and (3) standardize the criteria of signifi- lysis vascular access: upstream hemodynamics and vascular cant stenosis in a well-controlled multicenter trial. remodeling in dialysis access stenosis. 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