838180

research-article2019
JVA0010.1177/1129729819838180The Journal of Vascular AccessDistefano et al.

Original research article

JVA The Journal of
Vascular Access

The Journal of Vascular Access

Arteriovenous fistula and pre-surgery

1­–7
© The Author(s) 2019
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https://doi.org/10.1177/1129729819838180
DOI: 10.1177/1129729819838180

exercise on endothelial function journals.sagepub.com/home/jva

Giulio Distefano1, Luca Zanoli2, Antonio Basile1,

Pasquale Fatuzzo2 and Antonio Granata3

Abstract
Background: The success of the construction of an arteriovenous fistula for haemodialysis is related to the vascular
function of the vessels involved in the anastomosis, with particular reference to radial artery distensibility after reactive
hyperaemia test and to the fall of resistance index. Only few studies have evaluated the impact of exercise protocols
on the endothelial and morphological characteristics of the vessels of the upper limb with inconclusive results. In this
pilot longitudinal study, we aimed to evaluate the impact of a standardized exercise protocol on the haemodynamic and
resistive index of the arteries of the upper limb of uraemic patients.
Methods: A total of 17 uraemic patients planned to construct arteriovenous fistula at the distal third of the forearm
were enrolled and followed up for 30 days. All patients performed repeated handgrips for 30 min/day. The arterial
parameters were detected before and after an ischaemic stress of 5 min and radial and brachial artery flow-mediated
dilation was evaluated as well as radial artery resistance index.
Results: Pre-exercise measurements of radial artery diameter and resistance index and brachial artery diameter were
not modified by 30 days hand physical exercise, whereas the post-exercise haemodynamic were improved. Consequently,
flow-mediated dilation of the radial artery was improved (21% ± 14% vs 30% ± 19%; p = 0.03) and resistance index of the
radial artery was reduced (p = 0.02).
Conclusion: Exercise has beneficial effects on endothelial function of the radial artery by resistive index and, potentially,
on the outcome of the arteriovenous fistula. Further studies with larger sample size are needed to confirm our preliminary
data.

Keywords
Resistive index, arterio-venous fistula, physical exercise, arterial stiffness

Date received: 30 July 2018; accepted: 24 February 2019

Introduction
According to the NFK KDOQI Guidelines,1 the arterio- 1Radiology I Unit, Department of Medical, Surgical Sciences and
venous fistula (AVF), constructed with native vessels at Advanced Technologies, Catania University Hospital, University of
the distal third of the forearm, represents the first-choice Catania, Catania, Italy
vascular access in patients with end-stage renal disease 2Nephrology, Department of Clinical and Experimental Medicine,

(ESRD). The possibility to construct correctly a vascular University of Catania, Catania, Italy
3UOC Nephrology and Dialysis, ‘St. Giovanni di Dio’ Hospital,
access requires the careful examination of the vessels’ can-
Agrigento, Italy
didate to the anastomosis. The incidence of primary fail-
ures is significantly lower when the choice of vessels is Corresponding author:
Giulio Distefano, Radiology I Unit, Department of Medical, Surgical
guided by the echo colour Doppler (ECD) evaluation.2
Sciences and Advanced Technologies, Catania University Hospital,
Several morphological parameters related to endothelial University of Catania, Via Santa Sofia 78, 95100 Catania, Italy.
function, such as the vessel diameter, flow rate, Email: [email protected]
2 The Journal of Vascular Access 00(0)

post-ischaemic resistance indexes (RI) and radial artery Humans. All the enrolled patients provided their informed
distensibility, are also associated with AVF survival.3 In consent to the processing of personal data and inclusion in
patients with ESRD, endothelial function is frequently the protocol.
impaired.4 As reported previously by other authors, inter-
ventions that increase the diameter and flow of vessels
Protocol
before the construction of the AVF can improve the out-
come,5 as well as physical exercise is correlated with an All the instrumental data were collected in the morning.
improvement in the local reactivity of vascular endothe- All the participants were studied in a quiet room with a
lium probably through the promotion of NO release.6,7 It controlled temperature of 22°C ± 1°C after 15 min of
has been found that physical activity is able to improve the recumbent rest. In each subject, a non-invasive haemody-
endothelial function even in healthy humans.8 It is known namic study was performed by an expert operator blinded
that the increase of mechanical forces (shear stress) and to the clinical data and therapy. A second operator, blinded
local perfusion are responsible for the phosphorylation of to the haemodynamic examination, collected the clinical
the primary activation site of the NOS named S-11779 and data using a standardized questionnaire.
that repeated contractions of the hand are associated with
phosphorylation of S-1177, with significant increase in the
Haemodynamic examination
bioavailability of NO and consequent vasodilatory effect.9
However, only a few studies have been conducted to eval- All patients underwent a non-invasive haemodynamic
uate the impact of exercise on the vessels candidates for study at baseline (T0) and at the end of follow-up (T1).
AVF. Therefore, in this pilot study our primary aim was to The following measurements were performed: flow of the
test whether an exercise protocol can improve the endothe- brachial artery, diameter of the brachial artery proximal to
lial function of the arterial vessels of the candidate limb for the origin of the radial artery, radial artery diameter at the
AVF construction. In case of an improvement of the distal third and radial artery RI.
endothelial function after hand grip exercise, results of this In accordance with the ACC Guidelines for the evalua-
study will allow the identification of possible confounding tion of the flow-mediated dilation (FMD),11 the sleeve of a
factors and the calculation of the sample size of a multi- manual aneroid sphygmomanometer was placed on the
centre study. patient’s arm and inflated to a pressure of 200 mmHg (or in
any case > 50 mmHg of the systolic blood pressure) and
maintained for 5 min. Measurements of the radial and bra-
Methods chial artery diameter were performed immediately before
Study design the induction of the ischaemic stimulus and 30–60 s after
5 min of ischaemia. RI were calculated at the distal third of
We conducted a pilot longitudinal study with a follow-up the radial artery after 5 min of ischaemia.
of 30 days. Brachial blood pressure measurements were performed
in the contralateral arm using an oscillometer device
(Dinamap ProCare 100; GE Healthcare, Milwaukee, WI,
Setting and participants
USA) and the arithmetic mean of three consecutive meas-
Sequential patients with ESRD were enrolled at the urements was used. The ultrasound examination of the
Nephrology and Dialysis Unit of the San Giovanni di Dio vessels was performed with a Siemens Acuson S 3000
Hospital in Agrigento from May 2017 to April 2018 and platform (Siemens Healthcare, Erlangen, Germany) and a
randomized to the treatment or placebo group. high-resolution (8 mHz) linear array probe, a maximum
The following eligibility criteria have been adopted: scanning depth limited to 3 cm from the transducer mem-
ambulatory or hospitalized patients with ESRD brane, focused proximal to the posterior wall of the vessel.
(eGFR < 15 mL/min/1.73 m2 on at least two occasions For the evaluation of the vessel diameter of the arteries of
90 days apart; bilateral intrarenal RI > 0.80 as indicator of the upper limb, pre- and post-ischaemia screenshots were
possible endothelial dysfunction and irreversible renal taken, and the measurements were performed. In our labo-
damage)10 and candidates for AVF construction for haemo- ratory, the intra and intersession coefficients of variation of
dialysis with native vessels at the distal third of the non- arterial vessels diameter are 5.2% and 7.9%, respectively.
dominant upper limb. We have excluded patients with All the vessels were studied in longitudinal section, the
osteotendinous or neurological lesions that compromise brachial arteries proximal to the antecubital fossa and the
the motility of the studied limb, severe peripheral vascu- radial arteries to the third distal.
lopathy, class III–IV NYHA cardiac failure and diabetes. Each subject was given verbal and written information
The study protocol conformed to the ethical guidelines about the physical exercise programme. The prescribed
of the 1975 Declaration of Helsinki and was previously physical exercise was the following: to tighten and to
approved by the local Ethics Committee on Research on release a ball for 10 min three times a day with the hand of
Distefano et al. 3

Table 1. Main clinical characteristics of the studied population.

All patients Radial FMD improvement during follow-up p-value

No Yes
n=5 n = 12
Age, years 67 (12) 72 (7) 64 (11) 0.14
Male sex, % 88 100 83 0.33
Body mass index, kg/m2 23.8 (8.5) 21.4 (12.1) 20.8 (10.8) 0.92
Total cholesterol, mg/dL 158 (49) 167 (49) 149 (49) 0.49
C-reactive protein, mg/L 12.5 (21.7) 15.9 (19.8) 13.7 (26.8) 0.87
Serum glucose, mg/dL 94 (17) 101 (19) 91 (16) 0.27
Smoking, % 24 20 33 0.58
Dyslipidaemia, % 65 60 75 0.54

FMD: flow-mediated dilation.

Data are reported as mean ± standard deviation or percentage, as appropriate.

Table 2. Haemodynamic measurement during follow-up.

Baseline Follow-up p-value

Pre-exercise Post-exercise Pre-exercise Post-exercise Repeated- Bonferroni multiple

measures comparison test
A B C D ANOVA
Radial artery
Diameter, mm 1.87 ± 0.48 2.25 ± 0.56 1.99 ± 0.55 2.53 ± 0.56 <0.001 A ≠ B; C ≠ D; B ≠ D
RI 1.15 ± 0.09 0.88 ± 0.06 1.14 ± 0.08 0.84 ± 0.07 <0.001 A ≠ B; C ≠ D
Brachial artery
Diameter, mm 4.26 ± 0.62 4.97 ± 0.67 4.31 ± 0.65 4.98 ± 0.72 <0.001 A ≠ B; C ≠ D

RI: resistance index; ANOVA: analysis of variance.

Data are reported as mean ± standard deviation.

the non-dominant limb, daily for 30 consecutive days; Results

each patient was equipped with the same polyurethane
foam ball 7 mm in diameter (Artengo TB 600, Oxylane, Clinical characteristics of the studied population
Italy) and instructed to perform the maximum joint excur- A total of 17 patients (15 M and 2 F) were enrolled and fol-
sion with the hand while squeezing the ball. All the devices lowed-up for 30 days. Mean age was 67 ± 12 years (range
used were of the same model and purchased at the same 46–80 years), and body mass index was 23.8 ± 8.5 kg/m2.
time from the same supplier. Adherence to physical exer- Main characteristics of the studied population are summa-
cise was assessed by telephone interviews during follow- rized in Table 1.
up and, on site, during T0 and T1 visits.
Haemodynamic measurements
Statistical analysis Main haemodynamic measurements of the studied popula-
Data were analysed with NCSS 2007 and PASS 11 soft- tion are summarized in Table 2. T0: brachial artery diameter
ware (Gerry Hintze, Kaysville, UT, USA). Continuous was 4.26 ± 0.62 mm at rest and 4.97 ± 0.67 mm after 5 min
variables were presented as means (standard deviations), of ischaemia; radial artery diameter was 1.87 ± 0.48 mm at
and categorical variables were presented as percentages. rest and 2.25 ± 0.56 mm after 5 min of ischaemia.
Clinical and haemodynamic variables were compared T1: after 1 month of physical exercise, brachial artery
using analysis of variance (ANOVA) test for repeated diameter was 4.31 ± 0.65 mm at rest and 4.98 ± 0.72 mm
measurements. A two-tailed p-value < 0.05 was consid- after 5 min of ischaemia whereas radial artery diameter
ered statistically significant. was 1.99 ± 0.55 mm at rest and 2.53 ± 0.56 mm after 5 min
The authors had full access to the data and they take full of ischaemia. Consequently, FMD of the radial artery
responsibility for its integrity. All the authors have read increased from 21% ± 14% to 30% ± 19% (p = 0.03;
and agreed on the article as written. Figure 1) and RI of the radial artery drops from 0.88 ± 0.07
4 The Journal of Vascular Access 00(0)

Figure 1. Radial artery diameter after 5 min of ischaemia at T0 Figure 3. Brachial artery diameter after 5 min of ischaemia at
and T1. T0 and T1.

endothelial dysfunction.3 In this regard, we have previ-

ously reported in another district that, in presence of
reduced flow, muscular artery diameter is reduced accord-
ingly.17 Muscular contraction is a stimulus to increase the
flow and the consequent cutting forces in relation to local
metabolic needs, and it has recently been determined in
humans that a standardized physical exercise is able to
modify locally the bioavailability of nitric oxide resulting
from increased expression of NO synthetize.5
In the literature, there are only few experiences regard-
ing the impact of physical exercise on haemodynamic
parameters of the vessels of the upper limb, with nonhomo-
geneous results.18–24 The studies analysed are characterized
by small sample sizes, short follow-up and inhomogeneous
outcomes; only three of these studies reported a control
Figure 2. Radial artery resistance index after 5 min of
ischaemia at T0 and T1. group.18,22,23 Leaf et al.18 demonstrated that isometric exer-
cise increases the diameter of the cephalic vein, without
certain evidence on the long-term outcome of FAV con-
to 0.84 ± 0.07 (p = 0.02; Figure 2) whereas FMD of the struction. Uy et al.19 described a significant increase in the
brachial artery remains almost unchanged (17% ± 9% vs diameter of the cephalic vein after 8 weeks of isometric
16% ± 7%; p = 0.50; Figure 3) after 1 month of physical exercise, but identical results were also observed in the
exercise. Patients with an improvement of radial FMD at contralateral limb in the absence of valid justification.
the end of follow-up are slightly younger (p = 0.14) and Salimi et al.20 described a significant increase in the diam-
with a slightly lower serum glucose (p = 0.27) (Table 1) eter, flow and wall thickness of the AVF venous branch
than those with no improvement of radial FMD. compared to controls and had a significantly higher matura-
tion rate of vascular access in 2 weeks. Kong et al.21 com-
pared two different types of exercise to evaluate any
Discussion differences in diameter of the cephalic vein, flow, muscle
There is a tight interaction between the cardiovascular and strength and limb circumference; at the end of 4 weeks the
renal systems in patients with chronic kidney disease.12 In diameter of the cephalic vein was increased by an average
these patients, endothelial function is frequently impaired.4 of 30% and 33.5% in the two groups, a statistically signifi-
It is now recognized that there is a correlation between the cant difference with respect to baseline values. Rodriguez-
diameter of the radial artery and the success rate of the Moran et al.,22 evaluating the characteristics of the radial
AVF construction13–15 and that the FMD is correlated with artery in the first study found in the literature, highlighted
the artery distensibility after construction of the vascular that there was no benefit in recommending a specific exer-
anastomosis;16 high RI (>0.7) is considered a negative cise to patients with AVF (patients enrolled in the experi-
prognostic factor being correlated with a severe picture of mental arm n = 20). Rus et al.6 described, after an 8-week
Distefano et al. 5

exercise protocol, an increase in radial artery diameter and function is altered in diabetic patients24,25 and may suggest
brachial artery FMD compared to baseline values in hae- that even a mild increase in serum glucose could be associ-
modialysis patients; the authors concluded that these ated with endothelial dysfunction. The ongoing multicen-
improvements in the characteristics of the forearm vessels tre study will test this hypothesis.
could support the advisability of this exercise prior to the Finally, FMD was slightly and negatively related to age
preparation of the FAV (patients enrolled in the experimen- (p = 0.14). If confirmed in larger studies, this finding could
tal arm n = 14). Kumar et al.,5 after prescribing an exercise suggest that the improvement of the endothelial function
protocol very similar to ours, described a slight but signifi- of the radial artery after physical exercise could be higher
cant increase in radial and brachial artery diameter and in young subjects and in those who have a better glycae-
cephalic vein in the trained arm without changes in the con- mic control.
trol arm (patients enrolled in the experimental arm n = 23).
Oder et al.23 evaluated the impact of physical exercise on
Limitations
the diameter of the newly created AVF constructed with
native vessels and found that squeezing a rubber ball causes This study has several limitations. First, despite the num-
acute vessel dilation but did not define the long-term out- ber of subjects included in this study is in line with that of
come. The studies evaluated are inhomogeneous for patient the other studies reported in the literature, the small sam-
characteristics, for evaluated parameters (some authors ple size and the selection criteria have not allowed us to
have analysed arterial vessels, others studied veins) and for generalize the results of this work and to perform subgroup
follow-up duration, and the reduced samples do not allow analyses.
to generalize the results. We have found that in all the pro- This is a small pilot study. Therefore, further data of
tocols in the literature, the duration of the exercise was dif- larger studies could be necessary to fully justify the
ferent, while only in one study the force necessary for the hypothesis, the scientific rationale and the conclusions of
execution of the physical exercise was clearly quantified.23 this study. However, the objective of this pilot study was to
These limits can partly explain the lack of homogeneity of generate hypotheses and to furnish data for the calculation
the results. of the sample size of a multicentre trial. Second, we have
From these analyses, there is no clear indication of the studied only the arterial function. It remains to be clarified
appropriateness of prescribing a specific exercise to urae- whether physical exercise was associated with an improve-
mic patients. ment of the function of the veins. Future multicentre pro-
In our pilot study, we evaluated the FMD response of spective trial could solve this question. Third, adherence to
the upper limb arteries after a standardized exercise proto- physical exercise was assessed by telephone interviews
col for the preparation of a construction AVF with native during follow-up and, on site, during T0 and T1 visits.
vessels in the uraemic patient. We reported that physical Therefore, we cannot exclude that adherence to physical
exercise is associated with an improvement of the endothe- exercise could be lower than reported. Finally, diabetics
lial function evaluated with the modification of the radial and patients with severe CHF were excluded from this
artery diameter and RI, while no significant changes were study. These subjects represent a growing fraction of real-
reported in the brachial artery. This result could suggest world dialysis population. Further and larger studies could
that the ‘hand-grip’ exercise affects only the muscles of the be needed to test the effect of local physical exercise on
forearm. On the other hand, it may mean that this type of FMD in patients with diabetes and severe CHF.
exercise is not useful in improving the endothelial function
of patients in whom a proximal fistula construction is pro-
Perspectives
grammed in the brachial artery. Further studies are needed
to confirm these hypotheses. Moreover, considering that Classically, an ECD ultrasound examination and, in
the bioavailability of nitric oxide is correlated with the selected cases, an arteriography are usually performed
increase, even if intermittent, of shear stress,9 we hypoth- before AVF construction. Our results suggest that a stand-
esize that the significant changes of radial artery diameter ardized physical exercise protocol before the evaluation of
and RI found in our patients after physical exercise could vascular function could be included. In this setting, a para-
be due to the increase in shear stress and the consequent metric contrast-enhanced ultrasound (CEUS) examina-
local improvement of the endothelial function. It remains tion26 pre- and post-exercise could be tested to better
to be clarified whether the increase of radial artery diame- characterize the vascular function of these subjects. Future
ter and the reduction of RI is maintained over time. Larger multicentre prospective trial could test this hypothesis.
studies with a longer follow-up are needed to solve this
question.
Conclusion
We found that serum glucose was slightly lower in
responders than in non-responders. These data are in In this pilot study, we investigated the impact of physical
agreement with several studies reporting that endothelial exercise on the endothelial function of peripheral arterial
6 The Journal of Vascular Access 00(0)

vessels in the uraemic patient. With the limits of the with end-stage renal disease. Blood Purif 2003; 21(6):
reduced sample size, the adopted exercise protocol seems 389–394.
to improve haemodynamic parameters in response to 7. Katz SD, Yuen J, Bijou R, et al. Training improves endothe-
ischaemia, such as FMD and RI of the radial artery. This lium-dependent vasodilation in resistance vessels of patients
with heart failure. J Appl Physiol (1985) 1997; 82(5): 1488–
improvement may have potential beneficial effects on the
1492.
outcome of the AVF. However, further studies are needed
8. Casey DP, Ueda K, Wegman-Points L, et al. Muscle
to confirm these hypotheses. contraction induced arterial shear stress increases
endothelial nitric oxide synthase phosphorylation in
Author Contributions humans. Am J Physiol Heart Circ Physiol 2017; 313(4):
All authors meet the ICMJE Recommendations for authorship H854–H859.
credit. G.D. has contributed substantially to acquisition and anal- 9. Zhang QJ, McMillin SL, Tanner JM, et al. Endothelial nitric
ysis of data and drafting the work; L.Z. has contributed substan- oxide synthase phosphorylation in treadmill-running mice:
tially to the conception and design of the work, interpretation of role of vascular signalling kinases. J Physiol 2009; 587(Pt
data and revising the work critically for important intellectual 15): 3911–3920.
content; A.B. has contributed substantially to revising the work 10. Granata A, Zanoli L, Clementi S, et al. Resistive intrare-
critically for important intellectual content; P.F. has contributed nal index: myth or reality? Br J Radiol 2014; 87(1038):
substantially to interpretation of data and revising the work criti- 20140004.
cally for important intellectual content; A.G. has contributed sub- 11. Corretti MC, Anderson TJ, Benjamin EJ, et al. Guidelines
stantially to the design of the work, interpretation of data and for the ultrasound assessment of endothelial-dependent
revising the work critically for important intellectual content. All flow-mediated vasodilation of the brachial artery: a report
authors have read and approved the manuscript and agree to be of the International Brachial Artery Reactivity Task Force.
accountable for all aspects of the work in ensuring that questions J Am Coll Cardiol 2002; 39(2): 257–265.
related to the accuracy or integrity of any part of the work are 12. Granata A, Clementi A, Virzi GM, et al. Cardiorenal syn-
appropriately investigated and resolved. All authors have con- drome type 4: from chronic kidney disease to cardiovascular
tributed equally. impairment. Eur J Intern Med 2016; 30: 1–6.
13. Parmar J, Aslam M and Standfield N. Pre-operative radial
arterial diameter predicts early failure of arteriovenous fis-
Declaration of conflicting interests
tula (AVF) for haemodialysis. Eur J Vasc Endovasc Surg
The author(s) declared no potential conflicts of interest with 2007; 33(1): 113–115.
respect to the research, authorship and/or publication of this 14. Silva MB Jr, Hobson RW II, Pappas PJ, et al. A strategy
article. for increasing use of autogenous hemodialysis access pro-
cedures: impact of preoperative noninvasive evaluation. J
Funding Vasc Surg 1998; 27(2): 302–307.
15. Wong V, Ward R, Taylor J, et al. Reprinted article ‘Factors
The author(s) received no financial support for the research,
associated with early failure of arteriovenous fistulae for
authorship and/or publication of this article.
haemodialysis access’. Eur J Vasc Endovasc Surg 2011;
42(Suppl. 1): S48–S54.
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