Venous sinus stenting lowers the intracranial pressure in patients with idiopathic intracranial hypertension

Abstract

Aims
We report the cerebrospinal fluid opening pressure (CSF-OP) measurements obtained before and after venous sinus stenting (VSS) in 50 patients with idiopathic intracranial hypertension.

Methods
The CSF-OP was measured with a spinal tap 3 months before and 3 months after treatment. All data were prospectively collected and included patient demographics, weight (kg), body mass index (BMI), acetazolamide daily dosage (mg), procedural details, complications, venous sinus pressures (mm Hg), trans-stenotic pressure gradient (mm Hg), transverse sinus symmetry, and type of venous sinus stenosis.

Results
The average pretreatment CSF-OP was 37 cm H2O (range 25–77) and the average post-treatment CSF-OP was 20.2 cm H2O (range 10–36), with an average reduction of 16.8 cm H2O (P<0.01). The post-treatment CSF-OP was less than 25 cm H2O in 40/50 patients. The average acetazolamide daily dose decreased from 950 mg to 300 mg at the time of 3-month follow-up (P<0.01). No patient required an increase in acetazolamide dose 3 months after VSS. The average weight before treatment was 95.4 kg with an average BMI of 35.41. There was an average increase in body weight of 1.1 kg at the 3-month follow-up with an average increase in BMI of 0.35 (P=0.03).

Conclusions
We provide evidence that there is a significant decrease in CSF-OP in patients with idiopathic intracranial hypertension 3 months after VSS, independent of acetazolamide usage or weight loss.

Full text

1
PatsalidesA, etal. J NeuroIntervent Surg 2018;0:1–5. doi:10.1136/neurintsurg-2018-014032
ORIGINAL RESEARCH
Venous sinus stenting lowers the intracranial pressure
in patients with idiopathic intracranialhypertension
Athos Patsalides,1 Cristiano Oliveira,2,3 Jessica Wilcox,2 Kenroy Brown,1
Kartikey Grover,4 Yves Pierre Gobin,1 Marc J Dinkin2,3
Clinical neurology
To cite: PatsalidesA,
OliveiraC, WilcoxJ, etal.
J NeuroIntervent Surg Epub
ahead of print: [please
include Day Month Year].
doi:10.1136/
neurintsurg-2018-014032
1Division of Interventional
Neuroradiology, Department
of Neurological Surgery, Weill
Cornell Medine, New York, USA
2Department of Neurology,
Weill Cornell Medicine, New
York, USA
3Department of Ophthalmology,
Weill Cornell Medicine, New
York, USA
4Department of Medical
Statistics, Weill Cornell
Medicine, New York, USA
Correspondence to
Dr Athos Patsalides, Division of
Interventional Neuroradiology,
Department of Neurological
Surgery, Weill Cornell Medine,
New York, NY 10065, USA;
atp9002@ med. cornell. edu
Received 1 May 2018
Accepted 10 May 2018
ABSTRACT
Aims We report the cerebrospinal fluid opening
pressure (CSF-OP) measurements obtained before and
after venous sinus stenting (VSS) in 50 patients with
idiopathic intracranial hypertension.
Methods The CSF-OP was measured with a spinal
tap 3 months before and 3 months after treatment. All
data were prospectively collected and included patient
demographics, weight (kg), body mass index (BMI),
acetazolamide daily dosage (mg), procedural details,
complications, venous sinus pressures (mm Hg), trans-
stenotic pressure gradient (mm Hg), transverse sinus
symmetry, and type of venous sinus stenosis.
Results The average pretreatment CSF-OP was
37 cm H2O (range 25–77) and the average post-
treatment CSF-OP was 20.2 cm H2O (range 10–36),
with an average reduction of 16.8 cm H2O (P<0.01).
The post-treatment CSF-OP was less than 25 cm H2O
in 40/50 patients. The average acetazolamide daily
dose decreased from 950 mg to 300 mg at the time of
3-month follow-up (P<0.01). No patient required an
increase in acetazolamide dose 3 months after VSS. The
average weight before treatment was 95.4 kg with an
average BMI of 35.41. There was an average increase in
body weight of 1.1 kg at the 3-month follow-up with an
average increase in BMI of 0.35 (P=0.03).
Conclusions We provide evidence that there is
a significant decrease in CSF-OP in patients with
idiopathic intracranial hypertension 3 months after VSS,
independent of acetazolamide usage or weight loss.
INTRODUCTION
Since the first reported case in 2002, venous sinus
stenting (VSS) has gained increased acceptance as
a minimally invasive surgical option for patients
with idiopathic intracranial hypertension (IIH)
and significant cerebral venous sinus stenosis
(CVSS). The objective of VSS is to alleviate
significant stenosis typically found at the trans-
verse–sigmoid sinus junction, thereby reducing
intracranial pressure (ICP) and alleviating the
symptoms of IIH.
Despite the overall positive clinical results of
VSS reported in the literature, pre- and post-treat-
ment ICP has been documented in only a minority
of cases. More specifically, only four studies in the
literature documented cerebrospinal fluid opening
pressure (CSF-OP) by lumbar puncture (LP) before
and after treatment, if not in all, at least in the
majority of patients.1–4 Two other groups reported
measurements obtained from an ICP monitor that
was implanted before and after the stenting proce-
dure.5 6
As the VSS procedure has not yet been evalu-
ated in randomized controlled or sham procedure
trials, our group believes that objective data such
as CSF-OP are necessary, both for selecting patients
for treatment and also to demonstrate a successful
treatment effect as this treatment continues to be
evaluated. In this paper we report the CSF-OP
measurements obtained before and after treatment
in our patient cohort.
METHODS
This analysis was approved by our institution’s IRB.
Patient population
Sixty-three patients who met the criteria for diag-
nosis of IIH were treated with VSS in our insti-
tution from January 2012 to June 2017. Our
protocol required a 3-month post-stenting LP for
CSF-OP measurements. Of the 63 patients, 50 had
both pre- and post-treatment LP with CSF-OP
measurements and they constitute the cohort of
this analysis. Of the 13 subjects excluded from the
analysis, seven refused a post-treatment LP due to
a history of symptomatic CSF leak from a prior
procedure. Among these seven patients, four had
papilledema that resolved after VSS and three
had symptomatic improvement with resolution of
pulsatile tinnitus and headaches (no papilledema).
One patient did not have a recent pretreatment LP
but did have papilledema that resolved. Finally,
five patients had not reached the 3 month mark by
the time of the analysis and their follow-up LP was
still pending.
The VSS procedural details have been described
in previous publications from our group.4 A
minimum CSF-OP of 25 cm H2O before the proce-
dure was necessary for VSS. Briefly, the VSS proce-
dure requires dual antiplatelet therapy with aspirin
and clopidogrel, initiated 1 week before the proce-
dure and continuing for 1 month post-procedure,
with continued aspirin monotherapy for 5 more
months. Thus, at the time of post-stenting LP the
patients were on aspirin only. A catheter venogram
under local anesthesia was performed to obtain
venous sinus pressure measurements through a
microcatheter positioned in the superior sagittal,
transverse, and sigmoid sinuses and the jugular
bulb. A trans-stenotic gradient of ≥8 mm Hg was a
prerequisite for stenting. The stent placement was
performed under general anesthesia.
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Clinical neurology
Data collection
All data were prospectively collected and included patient
demographics, weight (kg), body mass index (BMI), acetazol-
amide daily dosage (mg), procedural details, complications,
venous sinus pressures (mm Hg), trans-stenotic pressure gradient
(mm Hg), transverse sinus symmetry, and type of venous sinus
stenosis.
CSF-OP
The CSF-OP was measured via a fluoroscopy-guided LP. The
majority of the LP procedures (82/100) were performed in
the left lateral decubitus position, whereas the remainder were
performed in the prone position. The pretreatment CSF-OP was
measured within 3 months before VSS. The post-treatment assess-
ment took place 3 months after VSS and included a contrast-en-
hanced MR venogram (MRV) followed by LP with CSF-OP. The
daily dosage of acetazolamide (mg) was documented at the time
of pre- and post-treatment LP. Following VSS, the acetazolamide
dosage was decreased when there was evidence of improvement
in papilledema, visual dysfunction, and presenting symptoms.
Body weight (kg) and BMI were also collected at the time of pre-
and and post-stenting LP.
Type of cerebral venous sinus stenosis
The type of venous sinus stenosis was documented with pretreat-
ment MRV and catheter venography. Extrinsic stenosis was
defined as a long segment stenosis with obtuse margins, whereas
intrinsic stenosis was defined as a short segment stenosis with
acute margins and focal filling defect in the venous sinus lumen.
Transverse sinus symmetry
The pattern of venous outflow from the superior sagittal sinus to
the transverse sinuses was documented using pretreatment MRV
and catheter venogram at the time of stenting. As reported in
a previous publication from our group, a co-dominant system
was considered when the transverse sinuses were symmetric with
<3 mm difference in maximal diameter on MRV. A unilateral
dominant system was considered when there was absence of one
transverse sinus (ie, aplastic) or asymmetric transverse sinuses
with >3 mm difference in maximal diameter (hypoplastic).7
Procedural parameters
During catheter venography and with the patient under local
anesthetic only, the following parameters were recorded: pres-
sure in the superior sagittal sinus and trans-stenotic gradient
(difference between the proximal transverse and distal sigmoid
sinus.
Statistical analysis
Descriptive statistics were made for all variables of interest in
the statistical analysis. Q–Q plots were used to plot residuals for
the three variables (weight, CSF-OP, and acetazolamide usage)
before and after treatment as a test of normality. A paired t-test
was used to examine significant differences before and after
treatment in these three variables. To assess statistical correlation
between superior sagittal sinus pressure, trans-stenotic gradient,
and pre-stenting CSF-OP, Pearson correlation coefficients were
calculated and P value obtained. The change in CSF-OP (ie,
difference in CSF-OP before and after stenting) was measured
as an absolute change, relative change (%), and as a binary indi-
cator by assessing whether or not the post-treatment CSF-OP
was <25 mm H2O. The Pearson correlation test was used for
assessing the statistical correlation between the absolute and
relative changes of CSF-OP with superior sagittal sinus pressure
and trans-stenotic gradient. An unpaired t-test was conducted
to investigate statistical differences between absolute and rela-
tive changes of CSF-OP against the pattern of venous outflow
(co-dominant versus unilateral) and type of stenosis (intrinsic
versus extrinsic). Fisher’s exact test was used to investigate the
association between the categorical indication of post-treat-
ment CSF-OP <25 cm H2O and the pattern of venous outflow
(co-dominant versus unilateral) and type of stenosis (intrinsic
versus extrinsic). An unpaired t-test was used to investigate
statistically significant differences between the categorical indi-
cation of post-treatment CSF-OP <25 mm H2O with the param-
eters superior sagittal sinus pressure and trans-stenotic gradient.
To assess whether acetazolamide usage was decreased in both
intrinsic and extrinsic types of stenosis, the paired non-para-
metric Mann–Whitney U test was used separately for both
groups. An unpaired Mann–Whitney U test was conducted to
investigate differences in acetazolamide requirement after treat-
ment between intrinsic and extrinsic types of stenosis. Similarly,
to assess differences in usage before and after VSS between
co-dominant and unilateral groups, a paired Mann–Whitney U
test was used separately for both groups. Also, to find differences
in post acetazolamide usage between co-dominant and unilateral
groups, an unpaired Mann–Whitney U test was conducted.
RESULTS
We report the results from 50 patients with IIH who underwent
VSS and had CSF-OP measurements before and 3 months after
treatment (47 women and 3 men; age range 7–59 years). Twen-
ty-nine patients (58%) had extrinsic stenosis and 21 had intrinsic
stenosis (42%). The stent was placed in the right lateral (trans-
verse and sigmoid) sinus in 37 patients and the left lateral sinus
in 13 patients (74% and 26%, respectively). No patient was
treated with bilateral lateral sinus stenting. Although there were
no neurological complications, one patient developed a retro-
peritoneal hematoma from the femoral artery puncture site that
was managed with observation, without any need for transfusion
or surgery. Another patient had a ruptured ovarian cyst 4 days
post-stenting that may have been related to the dual antiplatelet
therapy. There was no occurrence of in-stent stenosis or throm-
bosis. No patient required alternative surgical treatment (VSS,
CSF shunt, or therapeutic LP) up to the 3-month follow-up
mark.
CSF-OP
The average pretreatment CSF-OP was 37 cm H2O (range
25–77) and the average post-treatment CSF-OP was 20.2 cm
H2O (range 10–36), with an average reduction of 16.8 cm H2O
(P<0.01)Table 1. The post-treatment CSF-OP was <25 cm H2O
in 40/50 patients. The most significant change was 50 cm H2O
(27 cm H2O after treatment from 77 cm H2O before treatment),
which was documented in a patient with fulminant presenta-
tion and severe papilledema that resolved after stenting. Three
out of the 50 patients in our series did not show any reduction
in CSF-OP. One patient who experienced initial improvement
in symptoms and resolution of papilledema returned the week
before the 3-month LP with recurrent headaches; the CSF-OP
had slightly increased (29 cm H2O from 28 cm H2O) and MRV
demonstrated a new stenosis adjacent to the stent. The patient
was subsequently treated with a second VSS procedure and had
significant reduction of CSF-OP at follow-up (21 cm H2O). The
second patient had the same CSF-OP before and after VSS and
did not experience symptomatic improvement. The third patient
had the same CSF-OP before and after VSS but at the time of
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PatsalidesA, etal. J NeuroIntervent Surg 2018;0:1–5. doi:10.1136/neurintsurg-2018-014032
Clinical neurology
follow-up was off acetazolamide; this patient required serial
large volume spinal taps and 1 g acetazolamide daily prior to
venous stenting.
Acetazolamide
The average acetazolamide daily dose decreased from 950 mg to
300 mg at the time of 3-month follow-up (P<0.01). No patient
required an increase in acetazolamide dose 3 months after VSS.
Thirty-five of the 50 patients (70%) had discontinued acetazol-
amide by the time of the 3-month follow-up assessment.
Weight loss
The average weight before treatment was 95.4 kg with an average
BMI of 35.41. There was an average increase in body weight of
1.1 kg at the 3-month follow-up with an average increase in BMI
of 0.35 (P=0.03). Twenty-one patients (42%) had weight gain
>1 kg (range 1–13.6 kg), whereas 10 patients (20%) had a body
weight loss of >1 kg (range 1–5.9 kg) and 19 patients (38%)
maintained the same body weight (within 1 kg).
Procedural parameters
There was a statistically significant linear correlation between
the pressure in the superior sagittal sinus and the trans-stenotic
gradient with the pretreatment CSF-OP (P<0.001 and Pearson
correlation coefficient 0.46 and 0.49, respectively). There was
no statistically significant correlation between the pressure in
the superior sagittal sinus and the absolute or relative changes
in post-stenting CSF-OP or the categorical indicator (<25 cm
H2O). There was no statistically significant correlation between
the trans-stenotic gradients and the absolute and relative changes
in post-stenting CSF-OP or the categorical indicator (<25 cm
H2O).
Extrinsic versus intrinsic stenosis
There were 29 patients (58%) with extrinsic stenosis and 21
patients (42%) with intrinsic stenosis. At the 3-month follow-up
assessment, the patients with extrinsic stenosis showed a 44%
mean reduction in CSF-OP (from 37.34 to 20.93 cm H2O)
whereas the patients with intrinsic stenosis showed a 47% reduc-
tion of ICP (from 36.48 to 19.29 cm H2O). The mean absolute
change and percent change in CSF-OP did not differ between
the extrinsic and intrinsic groups, nor was the rate of improve-
ment to <25 cm H2O.
At the 3-month follow-up there was a 62% decrease in the
daily dosage of acetazolamide among patients with extrinsic
stenosis compared with an 81% decrease in daily dosage of the
medication among patients with intrinsic stenosis. Similarly,
62% of patients with extrinsic stenosis and 80% of patients
with intrinsic stenosis did not require any acetazolamide at 3
months. Both intrinsic (P<0.01) and extrinsic (P<0.01) groups
showed a statistically significant decrease in acetazolamide usage
(paired Mann–Whitney U test). However, acetazolamide usage
after treatment failed to show a statistically significant difference
between the intrinsic and extrinsic types of stenosis (P=0.13).
Unilateral dominant versus co-dominant transverse venous
sinuses
There were 31 patients with a unilateral dominant pattern
(62%) and 19 patients with a co-dominant system (38%). There
was no statistically significant difference in the degree of abso-
lute, percent, or categorical change (CSF-OP <25 cm H2O)
between the unilateral dominant and co-dominant groups. Both
the unilateral dominant (P<0.01) and co-dominant (P<0.01)
groups showed a statistically significant decrease in acetazol-
amide usage. Acetazolamide usage after treatment, on the other
hand, failed to show a statistically significant difference between
unilateral dominant and co-dominant groups (P=0.67).
DISCUSSION
While VSS has become increasingly popular as a minimally
invasive surgical treatment for IIH, high quality and objec-
tive data are necessary to validate its efficacy. As patients with
IIH are often polysymptomatic with a psychological compo-
nent, we wanted to report objective reproducible data and
explore whether the reduction in CSF-OP could be related to
other confounding factors such as acetazolamide usage and/or
weight loss. In what is to our knowledge the largest series of
IIH patients with CSF-OP measurements before and after VSS,
we demonstrate a statistically significant 45% mean reduction
in ICP 3 months after VSS, despite a statistically significant
reduction in acetazolamide usage and an increase in BMI in the
majority of patients.
Our results corroborate those published in prior series showing
a meaningful reduction of CSF-OP after VSS and support the role
of VSS as an effective surgical treatment for CVSS. Donnet et al
showed a mean reduction in CSF-OP of 24.2 cm H2O 3 months
after VSS in 10 patients.1 In a previous publication from our
group, we demonstrated a 20 cm H2O reduction 3 months after
VSS in 13 patients (these patients were also included in the
present analysis).4 The differences in mean reduction of CSF-OP
are most likely related to the number of patients included in the
earlier reports, to the average pretreatment ICP, and the degree
of acetazolamide usage post-treatment.
Others have shown an immediate reduction of ICP using ICP
monitors implanted at the time of stenting. Liu et al demonstrated
an immediate reduction of 27 cm H2O at the time of stenting in
10 patients, with an additional reduction of 10.8 cm H2O over-
night.6 Similarly, Matloob et al showed an immediate decrease
in ICP post-stenting in 9/10 patients, with a mean reduction of
7.8 cm H2O that was sustained for at least 24 hours.5 Although
complications of ICP monitors following stenting have not been
reported in the literature, we felt that implanting an ICP monitor
at the time of stenting could result in hemorrhage in the setting
of antiplatelet agents and intraprocedural anticoagulation.
Table 1 Changes in cerebrospinalfluid opening pressure (CSF-OP)and acetazolamide usage 3 months after venous sinus stenting(VSS)
CSF-OP (cm H2O) Acetazolamide (mg)
Pre VSS Post VSS Decrease (%) Pre VSS Post VSS Decrease (%)
All (n=50) 36.98 20.24 16.74 (45) 950 300 650 (68)
Ex (n=29) 37.34 20.93 16.41 (44) 1086.2 413.79 672.41 (62)
In (n=21) 36.48 19.29 17.19 (47) 761.90 142.86 619.04 (81)
Ex, extrinsic venous sinus stenosis;In, intrinsic venous sinus stenosis.
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4PatsalidesA, etal. J NeuroIntervent Surg 2018;0:1–5. doi:10.1136/neurintsurg-2018-014032
Clinical neurology
Intrinsic stenoses are anatomically fixed narrowed regions
of the sinus, and in some cases may act as a primary mediator
of the pathophysiology of IIH. Conversely, extrinsic stenoses
improve with ICP reduction and are therefore not felt to be an
isolated cause of IIH. It has been hypothesized, however, that an
initial elevation in ICP due to other factors such as recent weight
gain compresses the sinus at a vulnerable location, leading to
secondary venous hypertension and ultimately an even greater
elevation in ICP, since the CSF drains into the sinuses through
the arachnoid granulations. The additional increase in ICP
results in further venous sinus stenosis and a positive feed-
back loop ensues,8 ultimately resulting in a more severe disease
presentation. With this difference in mind, we hypothesized
that VSS of an intrinsic stenosis would lead to a greater reduc-
tion in ICP than extrinsic stenosis. Indeed, in a previous report
from our group4 we observed a trend (non-statistically signifi-
cant) towards a greater reduction of ICP in the intrinsic stenosis
group. This observation was not confirmed in this larger series,
likely reflecting the fact that CVSS—whether it is extrinsic or
intrinsic—is probably just one factor that interacts with others to
result in IIH. Indeed, since intrinsic stenoses are often the result
of longstanding anomalies, the advent of IIH at a given time of
life must reflect the addition of some new contributing factor
such as weight gain.
We did find that the need for acetazolamide was reduced
in the intrinsic stenosis group, both in terms of absolute daily
dosage and of the proportion of patients who stopped the medi-
cation completely within 3 months after treatment, but these
differences were not statistically significant. Perhaps the number
of patients is still not adequate to achieve statistical significance.
We also looked at differences in outcome between patients
with unilateral dominant versus co-dominant cerebral venous
outflow patterns. Despite a significant reduction in CSF-OP and
acetazolamide usage after stenting in both groups, there was no
difference in outcomes between the two groups. In a prior publi-
cation we have shown that, in cases of co-dominant pattern, the
majority of the venous outflow after stenting is via the stented
side (path of least resistance).7 Therefore, after stenting, both
groups functionally behave in the same fashion, which explains
the similar outcomes.
Limitations of the study
Our study was limited by the timing of the follow-up CSF-OP
measurement at 3 months after stenting. Our results do not tell
us about the speed of ICP reduction during those 3 months,
which is an important factor in ensuring that papilledema
resolves before permanent vision loss ensues. Since it has already
been demonstrated that the ICP decreases immediately after VSS
using ICP monitors, and since we could not perform LP within
the first 5 weeks while clopidogrel was still in effect, we opted to
perform the LP at 3 months to evaluate whether the immediate
reduction in ICP was sustained.
Another potential limitation of our study is the use of LP as
a means to assess ICP. Measurements derived this way might be
spurious owing to patient’s body habitus, anxiety, and position.
The alternative would be to use an ICP monitor before and after
stenting and document ICP changes over a longer period of
time and with positional changes and various activities. A recent
comparison of ICP monitoring and LP measurements performed
within the previous 6 months showed that only 2/17 patients
had high ICP when the ICP monitoring was utilized, whereas
all 17 had high ICP by LP.9 In another study ICP monitoring
did not show high ICP in 7/8 patients with high ICP by LP. The
authors did not report the time interval between LP and ICP
monitoring.10 From our review, there is no available study in the
literature comparing LP and ICP monitoring performed at the
same time, or at least a very close time interval. According to
current guidelines,11 12 the diagnosis of IIH requires demon-
stration of high ICP by LP. There is definitely a role for ICP
monitoring in complex cases, but the reality is that LP is widely
accepted for the diagnosis and management of IIH. In our study
we used LP under fluoroscopy before and after treatment, and
we feel that any errors of ICP measurements inherent to LP did
not affect the outcomes of this study.
Lastly, in the vast majority of patients the LP was performed in
the left lateral decubitus position, with only a few performed in
the prone position. A prospective study of 52 patients evaluated
for IIH showed no significant differences when CSF-OP was
measured in the prone versus the lateral decubitus position while
undergoing a fluoroscopy-guided LP,13 and we do not feel that
this change in positioning would have had a significant effect on
our results.
CONCLUSION
We have provided evidence that there is significant decrease in
CSF-OP in patients with IIH 3 months after VSS, independent of
acetazolamide usage or weight loss. As a high CSF-OP is a ‘sine
qua non’ for the diagnosis of IIH, and normalization of ICP is
an established treatment endpoint, the data we present in this
report are fundamental in supporting the beneficial role of VSS
as a therapeutic option in carefully selected patients with proven
IIH.
Contributors AP: Substantial contributions to the conception and design,
acquisition, analysis, and interpretation of data; guarantor of the paper. CO:
Substantial contributions to the conception and design; critical revision of the
manuscript for important intellectual content. JW: Acquisition of data. KB: Acquisition
of data. KG: Statistical analysis and interpretation. YPG: Substantial contributions
to the conception and design of the work; critical revision of the manuscript for
important intellectual content. MD: Substantial contributions to the conception
and design of the work; critical revision of the manuscript for important intellectual
content.
Funding KG: This work was supported by Clinical and Translational Science Center
at Weill Cornell Medical College grant number (1-UL1-TR002384-01).
Competing interests Dr Gobin is the founder, medical director and CEO of
Serenity Medical None declared.
Patient consent Not required.
Ethics approval Weill Cornell Medicine IRB.
Provenance and peer review Not commissioned; externally peer reviewed.
Data sharing statement Unprocessed data are available upon request from the
corresponding author.
Open Access This is an Open Access article distributed in accordance with the
Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which
permits others to distribute, remix, adapt, build upon this work non-commercially,
and license their derivative works on different terms, provided the original work
is properly cited and the use is non-commercial. See: http:// creativecommons. org/
licenses/ by- nc/ 4. 0/
© Article author(s) (or their employer(s) unless otherwise stated in the text of the
article) 2018. All rights reserved. No commercial use is permitted unless otherwise
expressly granted.
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