1034638 research-article2021 JVA0010.1177/11297298211034638The Journal of Vascular AccessMario et al. Original research article JVA The Journal of Vascular Access The Journal of Vascular Access Current role of ultrasound in 2021, Vol. 22(1S) 56­–62 © The Author(s) 2021 hemodialysis access evaluation Article reuse guidelines: https://doi.org/10.1177/11297298211034638 sagepub.com/journals-permissions DOI: 10.1177/11297298211034638 journals.sagepub.com/home/jva Meola Mario1 , Jose Ibeas2 and Jan Malik3 Abstract Physical examination (PE) is considered the backbone before vascular access (VA) placement, during maturation period and for follow-up. However, it may be inadequate in identifying suitable vasculature, mainly in comorbid patients, or in detecting complications. This review highlights the advantages of ultrasound imaging to manage VA before placement, during maturation and follow-up. Furthermore, it analyses the future perspectives in evaluating early and late VA complications thank to the availability of multiparametric platforms, point of care of ultrasound, and portable/ wireless systems. Technical improvements and low-cost systems should favor the widespread ultrasound-based VA surveillance programs. This significant turning point needs an adequate training of nephrologists and dialysis nurses and the standardization of exams, parameters, and procedures. Keywords Vascular access, B-Mode and pulsed wave Doppler, vascular access surveillance, ultrasound instrumentation, point of care of ultrasound Date received: 7 January 2020; accepted: 5 July 2021 Introduction at bedside, operating, and hemodialysis rooms. Thus, the question is why US, now considered as the fifth pillar of Correct management of native arteriovenous fistula (AVF) physical semiotics, should not be systematically used in or arteriovenous grafts requires specific knowledge and VA management. expertise and a multidisciplinary team approach. Early This monothematic issue aims to update the role of the referral of uremic patients to a nephrologist—usually con- US in VA. It suggests the widespread use of Point-Of- sidered the vascular access (VA) coordinator—is the main- Care Ultrasound (POCUS) with miniaturized, portable stay to increase fistula placement, to ensure a correct and handheld devices using an imaging program in preopera- multidisciplinary approach, reduce the primary failure tive mapping, maturation period, and VA surveillance to rate, and improve the cumulative VA patency.1 avoid the major complications. In other words, it is time Before VA creation, patients’ presurgical assessment to add the insonation as the fifth pillar of the VA has been based on physical examination (PE) for a long examination. time, and phlebography was the gold-standard imaging.2,3 Currently, ultrasound (US) and pulsed wave Doppler (PWD) are the first-line imaging for VA management.4–6 1 Institute of Life sciences, Department of Internal Medicine, Sant’Anna Safety, availability, and reliability are the main advantages School of Advanced Studies, University of Pisa, Pisa, Italy of ultrasound modalities. 2 Nephrology Department, Parc Taulí University Hospital, Parc Taulí Therefore, non-invasive imaging impact has remarka- Research and Innovation Institute (I3PT), Autonomous University of bly increased in the last years because most AVF with an Barcelona, Barcelona, Spain 3 Center for Vascular Access, General University Hospital, First Faculty inflow or outflow stenosis can be treated with percutane- of Medicine, Charles University, Prague, Czech Republic ous transluminal angioplasty (PTA) to increase long-term survival.2,7 Meanwhile, US platforms have dramatically Corresponding author: Meola Mario, Institute of Life sciences, Department of Internal improved since the 1990s, when the first reports in VA Medicine, Sant’Anna School of Advanced Studies, University of Pisa, imaging were published. Both multiparametric top-line Via Roma 45, Pisa 56100, Italy. systems and portable or pocket-sized systems can be used Email: mario.meola@unipi.it Mario et al. 57 Table 1. Physical and B-Mode/PWD findings of arteries related to arteriovenous fistula prior to access placement. Diagnosis/test Physical examination B-Mode and PWD Normal No information IMT, PWV, PSV >25–30 cm/s in radial artery, >40–50 cm/s in brachial artery Blood flow rate >40–50 ml/min in brachial artery Atherosclerosis, wall No information Number, extension, nature of plaques (lipoid, pathologies (age-related, fibro-sclerotic, calcific), lumen diameter (>2 mm), diabetes, CKD, connective single or multiple stenosis (PSV, DV, spectral tissue disorders) broadening, aliasing) Pulse examination Quality score (normal, diminished, Spectral curve morphology (high resistance flow), Corrigan pulse, absent) systolic/diastolic ratio, RI, PWV Segmental blood pressure Differential pressure between arms Stenosis of right subclavian artery at the origin measurement >20 mmHg (subclavian stenosis) (PSV, DV, spectral broadening, aliasing) Indirect signs of stenosis on the left side Patency of palmar arch Allen test Allen test modified with PWD Reactive hyperaemia test (RI <0.70) Congenital anomalies No information Bifurcation’s anomalies of brachial artery course anomalies of radial and ulnar artery PWD: pulsed wave Doppler; CKD: chronic kidney disease; IMT: intimal medial thickness; PSV: peak systolic velocity; DV: diastolic velocity; RI: resis- tive index; PWV: pulse wave velocity. Table 2. Physical and B-mode/PWD examination of vein related to arteriovenous fistula prior to access placement. Diagnosis/test Physical examination B-Mode and PWD Cephalic, basilic, and median Vein course on the forearm and Anomalies, course, luminal diameter (>2.5 mm), deep and antecubital veins anatomy arm surface is not always evident distance from the artery, length of straight segment for also using a blood pressure cuff cannulation, continuity with arm, and central veins inflated at 40–50 mmHg Anatomy of median antecubital and perforating vein Collaterals and valve apparatus Wall quality Distensibility (venous filling Variation of luminal diameter (25%–50%) after placing time test; dilation after placing tourniquet or blood pressure cuff inflated at 40–50 mmHg tourniquet or blood pressure Centripetal, continuous low-resistance flow cuff inflated at 40–50 mmHg) Absence of obstruction and fibrosis Stenosis and fibrosis Central vein patency No information Absence of arterial-like accelerations in the sampled trait “W” spectral modulation in the subclavian and jugular vein Congenital anomalies No information Variations of anatomy Presence of cephalic vein side branches referred to as accessory veins Objectives and accuracy of physical flow and fistula patency.9 A systolic rough, discontinu- examination ous, gunshot-like bruit or the onset of a discontinuous, pneumatic drill-like pulsatility or the disappearance of The National Kidney Foundation—Kidney Disease the thrill along the draining vein are all direct signs of Outcomes Quality Initiative (NKF-K/DOQI) guidelines stenosis. Collateral veins or aneurysms reinforce the sus- 2006 have already pointed out the pivotal role of clinical picion of stenosis.10 history and PE before VA creation.4 Physical examina- Palpatory findings associated with juxta-anastomotic tion should evaluate both arterial and venous patency venous stenosis include hyper-pulsatility at the anastomo- (Tables 1 and 2).8 sis site, systolic-only thrill perception, and abrupt pulse Physical findings of a mature AVF are related to hemo- disappearance across the stenosis site. In addition, flow dynamic changes due to by-pass implantation, fall of diversion in collateral veins is often visible and palpable. peripheral resistance, and evidence of turbulent flow in Complications of mature AVF can be detected with PE.10 the anastomotic site. Blood by-pass causes a palpable Two well-known tests, the arm elevation and pulse augmen- thrill on AVF and a bruit or “swishing” sound at ausculta- tation test, may easily detect outflow and inflow complica- tion. Both these signs indicate arterial and venous blood tions, but they are poorly applicable in AVG. Palpatory 58 The Journal of Vascular Access 22(1S) Table 3. Physical and B-Mode/CD/PWD findings of early and late AVF stenosis. Features Physical examination B-Mode and PWD Normal Thrill. Very prominent, continuous only at the Artery diameter >4 mm and vein diameter >6 mm anastomosis Flow rate of brachial artery >600–800 ml/min. Pulse. Soft and easily compressible Absence of arterial-like acceleration-point in draining Bruit. Low pitch, continuous, systo-diastolic vein and tributary artery No thrombosis or myxoid valve Juxta-anastomotic Strong pulse and systolic thrill at the anastomosis Vein lumen diameter <2–3 mm venous stenosis Thrill disappearance downstream the point of Arterial-like accelerations (PSV >250–300 cm/s), stenosis spectral broadening, aliasing, and color bruit Development of accessory branches RI and S/D ratio Increase in tributary artery Blood flow-rate fall in tributary artery Strength of Pulse strength. Very strong = good inflow; Arterial calibre (>4–4.5 mm) arterial inflow weak = poor inflow Low-resistive flow pattern (IR <0.50; S/D ratio <1.5–2) AVF pulsatility = vein stenosis Brachial artery flow-rate >600–800 ml/min Inflow stenosis Qb stress test positive Arterial-like accelerations (PSV >250–300 cm/s), spectral broadening, aliasing, and color bruit (tributary artery or juxta-anastomotic tract) Slow of venous flow without systolic reinforcement Outflow stenosis Thrill very prominent at site of stenosis Collateral vein Pulse systolic knock Arterial-like accelerations (PSV >250–300 cm/s), High pitched, discontinuous, only systolic bruit spectral broadening, aliasing, and color bruit). When arm is elevated, distally to point of stenosis Fall of brachial flow-rate the vein distended, while proximal portion remain collapsed Aneurysm development upstream from venous stenosis (insertion needle) findings associated with juxta-anastomotic venous stenosis Practice (ERBP) guidelines on VA and KDOQI-2019 clini- include hyper-pulsatility at the anastomosis site, systolic- cal practice guideline revision for VA recommend a differ- only thrill perception, and abrupt pulse disappearance across ent approach.14,15 the stenosis site. Flow diversion in collateral veins is often In our opinion, PWD may play a pivotal role in every visible and palpable. The persistence of a palpable thrill in aspect of VA care and might be considered the first-line the anastomosis site after occlusion of the outflow vein is an imaging modality in patients needing a VA. PWD gives indirect sign of collateral circles patency. The physical both morphologic and functional data about upper limb examination can also detect complications of mature VA. arterial and venous vessels. This information is particularly Once again, the presence of a swollen arm with subcutane- useful in obese patients with diabetes mellitus and arterio- ous venous collaterals and draining vein aneurysms may sclerosis or in the elderly and pediatric population. In these suggest central vein stenosis. cases, calcified and noncompliant arteries and small scle- Nevertheless, B-Mode and PWD provide more details rotic veins that negatively affect the remodeling and matu- to understand VA morphological and functional changes ration rates can be easily detected using US modalities.16 (Table 3). Preoperative mapping Advantages of integrating PE with At US, the upper limb veins show a thin wall that com- US-based techniques pletely collapse with transducer compression, while their Physical examination may be incomplete for both VA diameter increases when a tourniquet is placed at the prox- planning and management. B-Mode and PWD help choose imal segment. Data that have to be evaluated before AVF the anastomotic site, improve pre-and postoperative sur- creation are veins depth, diameter, course and length, con- veillance, and indicate cannulation time, especially when genital anomalies, and fibrotic segments. Perforating vein PE is inconclusive (Tables 1 and 2).11 Some guidelines morphology and patency at the elbow should always be support the PWD usefulness in preoperative mapping and assessed. An increase >25% (or >50% in the most favora- suggest this imaging modality as a screening test to detect ble cases) in the vein diameter after application of a tour- stenosis and perform pre-emptive interventions to avoid niquet is a sign of normal vein wall elasticity (Table 2). VA loss.12,13 However, the new European Renal Best In upper limb veins, the spectral curve is continuous, Mario et al. 59 centripetal, and generates a blowing wind-like sound. remodeling, and dilation of the feeding artery and draining However, there is considerable variability in the normal vein. These parameters can be reliably calculated through venous waveforms due to breathing, right heart function, a US examination. A recent study suggests that fistula and blood volume.17 blood flow rates measured at the proximal artery and in the Central vein waveform is multiphasic due to the modu- draining vein are comparable one to each other and with lations induced by breathing, central venous pressure vari- the values obtained by phase-contrast magnetic resonance ations during systole and diastole. This pattern provides an imaging if the measurements of vessels lumen diameter indirect sign of venous patency of proximal vessels with are accurate.22 However, a draining vein diameter <4 mm respect to the sampling point. For example, a phased wave- and a flow rate <500 ml/min are associated with a low form through the subclavian or jugular vein sampling probability of adequate maturation.23 After AVF creation, means that the proximal brachiocephalic trunk and supe- PWD measurements of blood flow rates at 2 weeks may be rior vena cava are not stenotic. In the preoperative setting, useful in the early identification of fistulas that are unlikely if the waveform pattern is flat and weak without any pha- to mature correctly.24 Flow rates calculated by PWD cor- sic modulations, phlebography, or second level imaging relate with the values measured with the US dilution should investigate a central venous occlusion of the bra- method (R2 = 0.83).25 chiocephalic vein or superior vena cava. Sonographic evaluation of venous anatomy is pivotal in Evaluation of early and late the choice of the anastomosis site. In adulthood, the effer- complications: B-mode and Doppler ent vein chosen for the anastomosis should have a diame- ter >2.0–2.5 mm, especially in patients with arterial wall criteria of stenosis damage and flow impairment due to age, atherosclerosis, Venous stenosis may be either an early or a late complica- and diabetes, because this condition is favorable both for tion of fistula, and it is the most common cause of access primary survival and success in the revision of malfunc- failure and dialysis inadequacy. The VA stenosis alters tioning AVF.18,19 regional hemodynamic and may causes access flow vol- On the arterial side, the main checkpoints are the bra- ume decline, followed by recirculation ⩾12%, reduction chial artery, brachial bifurcation, ulnar and radial arteries. of Kt/V ratio, high venous pressure (>200 mmHg), thrill The radial artery course should be carefully sampled to reduction, and post-dialytic bleeding.26,27 More proximal find the artery sites closest to the cephalic vein to create an outflow vein stenosis increases the venous pressure and anastomosis with a correct angle. This procedure reduces could lead to hand edema. In newly fistulas, the juxta- the risk of reactive neointimal hyperplasia. anastomotic stenosis in inflow or outflow is primarily The arterial parameters to be assessed are the diameter, caused by venous neointimal hyperplasia and inward vas- the extension of atheromatous plaques, the intimal-medial cular remodeling (venous constriction) stimulated by thickness, the spectral curve in rest conditions (peak sys- endothelial inflammatory-like pathways due to shear stress tolic velocity, mean or peak average velocity), and the variations. blood flow rate (Table 1). The optimal arterial diameter for PTA has become the current standard treatment of this creating an AVF is 2 mm, and the minimal blood flow vol- complication despite the stenosis relapses.28 Adequate sur- ume in the brachial artery is >50 ml/min, as it has been veillance with PWD imaging allows early diagnosis of the proved that a diameter <1.5 mm is associated with a higher venous stenosis and proper selection of the cases referred risk of access dysfunction and lack of arterial dilation.20,21 to procedure. Defining morphological and hemodynamic The superficial and deep palmar arches’ patency and criteria of stenosis at ultrasound is currently challenging perfusion of the distal circulation should be evaluated because of the lack of standardized values and procedures. by using the reactive hyperaemia test. The test is based The increase of the peak systolic velocity (PSV) and dias- on the spectral curve recorded in the radial artery in tolic velocity in stenotic segments (juxta-anastomotic and basal conditions, after fist closing for 2 min and imme- distal segment of the outflow vein in the native fistula, diately after fist opening. If significant vasodilation venous anastomosis of prosthetic graft), spectral broaden- appears in this last phase of the test and the spectral ing, and artifacts such as aliasing and perivascular color curve shows a low-resistance pattern (Resistive Index bruit are the typical signs of stenosis. <0.70), the test indicates patency of the palmar arches Arterial stenosis represents only 8% of all vascular and hand vessels. Consequently, the creation of an AVF access stenosis. It is associated with age-related diseases is at low risk of steal syndrome. The color sampling of and may be suspected when PSV values in the radial artery arteries and veins should be obtained using a 10°–20° are greater than 200 cm/s (compared with the upstream steering, while spectral analysis can be obtained using a segment of the vessel—PSV ratio >2–2.5).4,6 Conversely, 60° angle to standardize the results. the diagnosis of draining vein stenosis is more difficult. In After AVF implantation, the most accurate predictors of this case, a segmental increase in the PSV (>300 cm/s) in adequate access maturation are the blood flow volume, the vein is to be considered critical if the increase of PSV 60 The Journal of Vascular Access 22(1S) is associated with a reduction of blood flow rate in the bra- chial artery (<500 ml/m or fall of 25% in the last month when the blood flow rate is <1000 ml/min).5,6 PWD meas- urements compared to venography have shown an overall sensitivity ranging from 87% and 100% and specificity between 85% and 97%.28,29 Considering that PTA is the choice treatment for stenosis and obstruction of VA and that the costs related to the administration of repeated PTA and drug-eluting/coated balloon are elevated, more trials are needed to define parameters and indications of the therapeutic procedures. Point-of-care ultrasound revolution The concept of focused imaging increasingly influences current clinical practice. The physician has to focus only to few US key points instead of performing an extensive PWD examination. Point-Of-Care Ultrasound (POCUS) is the most known and promising application of focused imaging. It refers to the practice of trained medical profes- sionals using US to diagnose problems wherever a patient Figure 1. Wireless ultrasound probe. is treated, either in a modern hospital, an ambulance, or a remote place. Its benefits include the availability of a wider range of medical personnel than the one needed for a spe- mapping is still lacking. Moreover, the clinical contexts of cialized and extensive US examination. Therefore, this comparison between PE, comprehensive ultrasound, and procedure is very helpful in emergency settings where POCUS are multiple. They include preoperative mapping, prompt referral to a specialist is not always possible. The maturation period, VA surveillance, and follow-up to common belief that POCUS cannot replace extensive US detect early and late complications. POCUS could be examination is based on the bedside context, the lower implemented to detect early and late VA complications, but required level of examiner’s US proficiency, and the goal- it needs to be assessed through feasibility studies that are directed nature of the POCUS examination. still lacking to date. Consequently, specific measures are required to distin- guish the clinical context in which each kind of examina- Standardization of examination, tion should be performed (Figure 1).30 Focused imaging parameters, and procedures has found its utility in clinical practice by considering “insonation” as the fifth pillar of physical examination.31 In routine US management of VA, there are the same issues POCUS has properly and cost-effectively modified the present in all the subspecialties of sonography, especially workup of common clinical presentations.32 The improved regarding the lack of a standardized and shared protocol clinical outcomes using POCUS already justify the wide- for PWD examination and interpretation. However, a spread of US practice among nurses and non-specialists of nephrologist should always manage VA clinical process ultrasound imaging. The lack of specific training require- using PWD, from planning to follow-up, even if the skills ments further stimulates the use of POCUS since no required to obtain the best results are not limited to normal standardized teaching and assessment criteria are availa- specialist knowledge. A PWD operative protocol for VA ble to date. management is mandatory, however to date, it is still lack- Given the progressive diffusion of focused imaging, it ing. The European Federation of Societies for Ultrasound is appropriate to evaluate whether and how its use in clin- in Medicine and Biology (EFSUMB) has published the ical practice will affect VA planning and/or follow-up. minimum training recommendations for medical ultra- Evidence about POCUS use in VA management is still sound practice. However, there is no specific section on very poor; a recent study has shown a decreased primary VA management in the vascular appendix34 because data and secondary failure rate of AVF when the preoperative about VA ultrasound are recent and not always conclusive. mapping was performed with POCUS versus PE.33 Therefore, ultrasound societies’ standardization of US Investigations are ongoing to assess whether POCUS exams and procedures should be performed together with can improve vessel cannulation compared to “blind” multidisciplinary teams skilled in VA US management. PE-based cannulation. However, to our knowledge, a Examples of parameters requiring urgent standardization direct comparison with specialized and extensive US among practitioners include preoperative criteria for Mario et al. 61 assessing outflow vein stenosis, and algorithms for the postoperative assessment of dialysis access. J Ultrasound postoperative evaluation of the access flow rate. Med 2014; 33: 1321–1332. 7. Tordoir JHM, Zonnebeld N, van Loon MM, et al. Surgical and endovascular intervention for dialysis access matura- Conclusion tion failure during and after arteriovenous fistula surgery: review of the evidence. Eur J Vasc Endovasc Surg 2018; 55: An accurate PE in preoperative period and a continuous 240–248. VA follow-up during and after the maturation period 8. Woo K, Ulloa J, Allon M, et al. Establishing patient-specific should be coupled with PWD examination. In this mono- criteria for selecting the optimal upper extremity vascular thematic supplement, the role of ultrasound in the evalua- access procedure. J Vasc Surg 2017; 5: 1089–1103. tion of early and late complications of VA is extensively 9. Windus DW. Evaluation for vascular access dysfynction. considered. The prospective and future of US surveillance In: Nissenson AR and Fine RN (ed.) Handbook of dialysis are also analyzed, considering the technological advances therapy. 4th ed. Philadelphia, PA: Saunders–Elsevier, 2008, and the widespread use of US-based techniques. In the pp.37–48. next future, US-based surveillance will probably be the 10. Malovrh M. Postoperative assessment of vascular access. J routine procedure. The real challenge will be adequate Vasc Access 2014; 15(Suppl. 7): 10–14. 11. Aishwarya KC, Srinath MG, Desai SC, et al. Value of pre- training for nephrologists and dialysis nurses and the operative sonographic vascular evaluation of haemodialysis standardization of exams, parameters, and procedures. access in upperlimb. J Clin Diagn Res 2014; 8(12): RC06– RC10. Declaration of conflicting interests 12. Ibeas J, Roca-Tey R, Vallespín J, et al. Spanish clinical The author(s) declared no potential conflicts of interest with respect guidelines on vascular access for haemodialysis. Nefrologia to the research, authorship, and/or publication of this article. 2017; 37(Suppl, 1):1–191. 13. Schmidli J, Widmer M, Basile C, et al. Editor’s choice – Funding vascular access: 2018 clinical practice guidelines of the European society for vascular surgery (ESVS). Eur J Vasc The author(s) disclosed receipt of the following financial support Endovasc Surg 2018; 55: 757–818. for the research, authorship, and/or publication of this article: JM 14. Gallieni M, Hollenbeck M, Inston N, et al. Clinical practice is supported by the grant of the Agency of Health Research of the guideline on peri- and postoperative care of arteriovenous Czech Republic 17-31796A. fistulas and grafts for haemodialysis in adults. Nephrol Dial Transplant 2019; 34(Suppl. 2): ii1-ii42. ORCID iDs 15. Lok EC, Huber TS, Lee T, et al. KDOQI clinical practice guideline for vascular access: 2019 update. Am J Kidney Dis Meola Mario https://orcid.org/0000-0002-1330-2820 2020; 75: s1–s164. Jose Ibeas https://orcid.org/0000-0002-1292-7271 16. Farrington CA, Robbin ML, Lee T, et al. 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