Quantitative Ultrasound for Measuring Obstructive Severity

in Children with Hydronephrosis

Juan J. Cerrolaza,* Craig A. Peters,* Aaron D. Martin, Emmarie Myers,
Nabile Safdar and Marius George Linguraru
From Sheikh Zayed Institute for Pediatric Surgical Innovation (JJC, CAP, ADM, EM, MGL), and Division of Urology and
Pediatrics (CAP, ADM), Childrens National Health System, and Departments of Radiology and Pediatrics, School of
Medicine and Health Science, George Washington University (MGL), Washington, D.C., and Department of Radiology
and Imaging Sciences, Emory University School of Medicine, Atlanta, Georgia (NS)

Purpose: We define sonographic biomarkers for hydronephrotic renal units that

Abbreviations
can predict the necessity of diuretic nuclear renography.
and Acronyms
Materials and Methods: We selected a cohort of 50 consecutive patients with
D dimensional
hydronephrosis of varying severity in whom 2-dimensional sonography and
diuretic mercaptoacetyltriglycine renography had been performed. A total of DR diuretic renography
131 morphological parameters were computed using quantitative image analysis HI hydronephrosis index
algorithms. Machine learning techniques were then applied to identify ultra- LOG logistic regression analysis
sound based safety thresholds that agreed with the t1/2 for washout. A best fit MAG3 mercaptoacetyltriglycine
model was then derived for each threshold level of t1/2 that would be clinically QI quantitative imaging
relevant at 20, 30 and 40 minutes. Receiver operating characteristic curve
SFU Society for Fetal Urology
analysis was performed. Sensitivity, specificity and area under the receiver
operating characteristic curve were determined. Improvement obtained by the SVM support vector machine
quantitative imaging method compared to the Society for Fetal Urology grading US ultrasound
system and the hydronephrosis index was statistically verified.
Accepted for publication October 18, 2015.
Results: For the 3 thresholds considered and at 100% sensitivity the specificities No direct or indirect commercial incentive
of the quantitative imaging method were 94%, 70% and 74%, respectively. Cor- associated with publishing this article.
responding area under the receiver operating characteristic curve values were The corresponding author certifies that, when
applicable, a statement(s) has been included in
0.98, 0.94 and 0.94, respectively. Improvement obtained by the quantitative the manuscript documenting institutional review
imaging method over the Society for Fetal Urology grade and hydronephrosis board, ethics committee or ethical review board
index was statistically significant (p <0.05 in all cases). study approval; principles of Helsinki Declaration
were followed in lieu of formal ethics committee
Conclusions: Quantitative imaging analysis of renal sonograms in children approval; institutional animal care and use
with hydronephrosis can identify thresholds of clinically significant washout committee approval; all human subjects provided
written informed consent with guarantees of
times with 100% sensitivity to decrease the number of diuretic renograms in up
confidentiality; IRB approved protocol number;
to 62% of children. animal approved project number.
Supported by a grant from the government of
Abu Dhabi.
Key Words: biological markers, hydronephrosis, kidney, * Correspondence: Sheikh Zayed Institute for
technetium Tc 99m mertiatide, ultrasonography Pediatric Surgical Innovation, Childrens National
Health System, 111 Michigan Ave., NW Washing-
ton, D.C. 20010 (e-mail: jcerrola@childrensnational.
org, crpeters@childrensnational.org).

ULTRASOUND is the mainstay of imag- developed a semiautomatic quantita-

ing for pediatric hydronephrosis
yet is limited by its subjectivity and
lack of apparent correlation with
functional imaging modalities.1 To
improve the clinical usefulness of
sonography for hydronephrosis, we
tive imaging analysis algorithm to
objectively describe hydronephrosis
and to define ultrasound based
thresholds of obstruction below
which diuretic renography can be
safely avoided.2 Quantitative imaging

0022-5347/16/1954-1093/0 http://dx.doi.org/10.1016/j.juro.2015.10.173
THE JOURNAL OF UROLOGY
2016 by AMERICAN UROLOGICAL ASSOCIATION EDUCATION AND RESEARCH, INC.
Vol. 195, 1093-1099, April 2016
Printed in U.S.A.
www.jurology.com j 1093
1094 QUANTITATIVE ULTRASOUND FOR PEDIATRIC HYDRONEPHROSIS
techniques rely on analysis of digital images and
creation of normative models of shape and appear-
ance to which a test case is compared. The test case
can then be defined, based on probability, as being
within a specific range of values different from the
norm. By using machine learning to correlate pat-
terns of hydronephrosis with the diuretic renog-
raphy parameters, in this case t1/2 washout, the
correlation between structure and function can be
defined and used to categorize subsequent test
cases. With the primary goal being to identify ul-
trasound derived thresholds of safety for hydro-
nephrotic renal units where diuretic renography
can be avoided based on washout times, we applied
quantitative imaging techniques to a cohort of
pediatric patients with varying degrees of hydro-
nephrosis in whom routine ultrasonography and
diuretic renography had been performed. The
quantitative imaging algorithm was then assessed
as a predictor of the washout parameters of diuretic
renography.
Currently the most widely used instrument for
grading hydronephrosis sonographically is the SFU
system,3 although it is not universally accepted as
useful.4,5 Shapiro6 and Venkatesan7 et al proposed a
quantitative measure of hydronephrosis severity,
the HI, defined as the ratio of the collecting system
area to the total area of the collecting system
and renal parenchyma. However, the practical use
of this index remains unclear.8 While different cli-
nicians use differing thresholds for selecting pa-
tients in whom to perform DR and for defining
clinically significant obstruction, it would seem
valuable to perform DR only in those in whom it is
likely to reveal clinically relevant parameters for
intervention or close followup.
We hypothesized that hydronephrosis can be
objectively quantified sonographically using mod-
ern imaging analysis, and that there is a correla-
tion between degree of hydronephrosis and
severity of obstruction as measured by DR. This
correlation likely is not linear, but demonstrates
a threshold of dilatation above which clinically
significant drainage abnormalities are detectable
on DR. If this relationship can be defined, then
quantitative assessment of degree of hydro-
nephrosis on US could be used to selectively iden-
tify which patients have more severe obstruction
(by DR parameters) and should undergo DR, and
which patients have less severe hydronephrosis
and should forgo DR.
MATERIALS AND METHODS
Study Population
Under an internal review board approved protocol we
retrospectively selected 50 consecutive patients (32 males
and 18 females) with hydronephrosis who had undergone
concurrent renal 2-D ultrasound and DR (MAG3 scan).
Mean patient age was 9.6 months (median 4.0, range 0 to
168). Of the cases 21 were left sided, 29 were right sided
and 8 were bilateral. Cases involving vesicoureteral
reflux, ureterovesical junction obstruction, ureterocele
or hydroureter/megaureter were excluded to avoid con-
founding factors. Ultrasound acquisition was performed
using the Philips iU22 (C2-9-D transducer) and GE
Logiq E9 (C8-5 transducer) scanners between July 2012
and January 2013. Images were identified that contained
the closest to a full coronal view that included the renal
pelvis and calyces. MAG3 scan was performed using a
standardized method described previously.9,10 All pa-
tients underwent DR based on clinician preference, and
no study was postoperative.
Quantitative Imaging Analysis
Manual segmentation of the renal parenchyma and col-
lecting system was performed to create a cohort for pro-
gram calibration and algorithm development. This was
accomplished by manually drawing the best line around
the perimeter of the renal parenchyma and the collecting
system (using the ITK-Snap Medical Image Segmentation
Tool, http://www.itk-snap.org), excluding the extrarenal
pelvis. The intrarenal pelvis was defined as the area
falling within a line drawn around the hilar curve of the
parenchyma (fig. 1). All segmentations were reconciled
with 2 observers (pediatric radiologist and urologist) and
submitted for QI analysis. The same cohort underwent
grading using the SFU classification by a pediatric radi-
ologist and a pediatric urologist.
A total of 131 morphological parameters were
computed (fig. 2 and supplementary table, http://jurology.
com/). These descriptors can be intuitively grouped into
3 categories, ie size, geometric shape and curvature. Size
descriptor parameters describe the size of the collecting
system and renal parenchyma, such as relative area
(eg HI) and perimeter, depth of calyces, and thickness of
parenchyma. Geometric shape descriptor parameters
include such factors as circularity ratio, eccentricity of the
circumscribed ellipse and convexity. Curvature de-
scriptors are parameters that describe the local curvature
of the structures under analysis (ie kidney and collecting
system).11
These quantitative shape features were used as po-
tential predictive variables to evaluate the diagnostic
performance of 2 different supervised classification
models, the LOG12 and SVM with nonlinear kernel.13
Both approaches have been widely used in the field of
computer-aided diagnosis with satisfactory results.14
These 2 classification approaches were applied to the
test cohort to compute US based specific thresholds to
identify patients with a t1/2 above different thresholds,
ie 20, 30 and 40 minutes, since not all clinicians agree
as to the clinically relevant DR thresholds. These cutoffs
represent commonly used clinical thresholds.15 The
design parameters of the model were adjusted to maxi-
mize the sensitivity of detecting severe cases of hydro-
nephrosis, that is no case with t1/2 above the threshold
was misclassified. A best fit model was then derived for
each threshold using optimal morphological parameters
 QUANTITATIVE ULTRASOUND FOR PEDIATRIC HYDRONEPHROSIS 1095

Figure 1. 2-D ultrasound slice selection and segmentation. A, selected slice containing whole longitudinal section of kidney.
B, consensus manual delineation of renal parenchyma and collecting system.

and SVM or LOG to categorize the renal units and
severity of obstruction.
To compare this QI method to the current SFU grading
system in selecting cases where DR was to be performed,
we compared SFU grade 3 and above or only SFU grade 4
as the criterion for performing DR. Sensitivity and spec-
ificity were determined, as well as ROC curve analysis
with AUC calculation. A similar assessment was made
using the previously described HI. The proposed frame-
work was implemented in MATLAB, using a 64-bit
2.8 GHz processor, with an average execution time of
12 seconds per case.
Statistical Analysis
The cohort data were used to assess the performance
of the QI algorithm described previously,2 using leave-
one-out cross-validation methodology.16 From the 131
morphological features computed for each case an optimal
subset of predictive variables was selected for each t1/2
threshold using the feature selection technique proposed
by Cai et al.17 The significance of the improvement ob-
tained by the QI method over the SFU grade and HI was
statistically verified using the McNemar test.18 Addi-
tionally the interobserver variance for SFU grading was
assessed using the Fleiss kappa statistic.
In the absence of previous studies that related to this
topic to provide an estimation of the expected effect
we performed a retrospective power analysis using a
2-tailed t-test over the output probability provided by the
classifiers, SVM and LOG (significance level 0.05).
Effect sizes were calculated using the Hedges formulation
for means differences.19
RESULTS
The retrospective power analysis of the cohort of
50 patients provided a power value of greater than
0.99 in all instances. SFU grades ranged from 1 to 4
(median 3). Median differential uptake on MAG3
scan was 48% (range 14% to 100%). Median t1/2 was
17 minutes (range 3 to greater than 120). Differen-
tial uptake was less than 40% in 7 patients and less
than 30% in 3. All patients with differential uptake
less than 30% would have been identified with a t1/2
threshold of 30 minutes or greater. Two patients
with differential uptake less than 40% and greater
than 30% had washout times of less than 20 min-
utes (table 1), suggesting a nonobstructive cause of
the reduced uptake.
The best performance of the QI method was ob-
tained by means of the SVM classification system
for thresholds of 20 and 30 minutes, while LOG
provided better performance for a threshold of
40 minutes. Because the design parameters of the
model were defined to maximize the sensitivity of
detecting cases of hydronephrosis over a specified

Figure 2. Morphological descriptors of renal unit. Sample illustrates morphological descriptors considered as potential predictive
features of hydronephrosis severity. ab, eccentricity of circumscribed ellipse. Pmax, maximum parenchymal thickness. Pmin,
minimum parenchymal thickness. PKMAmax, kidney medial axis and point of maximum curvature. PKMAleft, left axis of kidney.
PKMAright, right axis of kidney. Arrows indicate curvature measures of collecting system and kidney surface. Relative area of
collecting system and parenchyma is shown.
1096 QUANTITATIVE ULTRASOUND FOR PEDIATRIC HYDRONEPHROSIS

Table 1. Cases by category
No. Cases
1
T /2 threshold:
20 Mins or greater
30 Mins or greater
40 Mins or greater
SFU grade:
2 14
3 18
4 18
DR parameter, no case with t1/2 above the threshold
was misclassified (100% sensitivity).
For the 3 thresholds considered, ie 20, 30 and
40 minutes, and at 100% sensitivity the specificities
of the method were 94%, 70% and 74%, respectively.
Compared to using the SFU grading system to select
patients for MAG3 scan (table 2) or the HI, this
approach provides greater specificity while main-
taining maximum sensitivity.
Figure 3 illustrates the ROC curves for the
quantitative imaging, SFU and hydronephrosis
index techniques for selecting patients with t1/2
greater than 30 minutes. Using either hydro-
nephrosis index or SFU grading system showed an
AUC of 0.78, which was significantly less robust
than the 0.94 AUC using the SVM based quantita-
tive imaging method (p <0.001 and p 0.04,
respectively). Similar results were obtained for
washout threshold values of 20 and 40 minutes.
Quantitative imaging performed significantly better
than hydronephrosis index (p <0.001 for either
threshold) and significantly better than the SFU
grading system (p <0.001 for t1/2 of 20 minutes and
p 0.05 for t1/2 of 40 minutes). The interobserver
reliability for SFU grading between a pediatric
radiologist and a pediatric urologist revealed a
Fleiss kappa statistic of 0.378, indicating fair
agreement.20
Table 3 outlines the potential reduction in
MAG3 scanning using the QI method, compared to
that obtained using SFU grade when an SFU grade
of 3 or 4 was used to refer patients for MAG3 im-
aging. For the 3 different t1/2 thresholds under
19
study the QI algorithm maximizes the reduction
14 in MAG3 scan within the total cohort, while no
8 critical case with severe obstruction was missed.
DISCUSSION
Using the QI algorithm with machine learning in
pediatric patients with hydronephrosis, US can be
used to predict which patients will have clinically
relevant increased washout times on DR. Applying
this technique to children with hydronephrosis,
particularly those with prenatally diagnosed dis-
ease, could safely decrease the need for invasive and
ionizing DR. Clinicians would be able to select
thresholds of safety that they find acceptable.
These results have several potentially useful
implications. These observations demonstrate that
renal structure and function, specifically drainage,
are related. Being able to use ultrasound images to
infer functional data would offer decreased inva-
siveness, complexity and cost, with no reduction in
safety and acceptable reduction in accuracy.
This system appears to be a useful clinical tool to
determine which patients would benefit from DR
over using the SFU scoring system alone. While this
approach does not eliminate the need for DR, it
permits more specific application of a costly, com-
plex, semi-invasive imaging test with radiation
exposure. Application of this modality would be
most useful in infants with prenatally detected
hydronephrosis, in whom there remains controversy
regarding the need for imaging beyond the post-
natal US. There are currently no clearly defined
guidelines based on objective metrics or clinical
outcomes that aid in the selection of patients for DR.
Of course, interpretation of the DR remains
controversial, as is the decision regarding the need
and timing for surgical intervention. This study

Table 2. QI vs SFU grade or HI to identify washout time thresholds in patients with hydronephrosis

% Sensitivity (95% CI) % Specificity (95% CI) % Pos Predictive Value (95% CI) % Accuracy (95% CI) % AUC (95% CI)
1
T /2 greater than 20 mins:
QI (SVM) 100 (82e100) 94 (79e99) 90 (70e99) 96 (86e99) 98 (92e100)
SFU grade 2 100 (82e100) 0 (0e11) 38 (25e53) 38 (25e53) 74 (57e83)
HI 100 (82e100) 52 (33e70) 56 (38e73) 70 (55e82) 77 (58e86)
T1/2 greater than 30 mins:
QI (SVM) 100 (77e100) 70 (52e84) 56 (35e75) 78 (64e88) 94 (83e98)
SFU grade 3 100 (77e100) 39 (23e56) 39 (23e56) 56 (41e70) 78 (62e86)
HI 100 (77e100) 47 (30e64) 42 (25e61) 62 (47e75) 78 (55e88)
T1/2 greater than 40 mins:
QI (LOG) 100 (63e100) 74 (58e86) 42 (20e66) 78 (64e88) 94 (81e98)
SFU grade 3 100 (63e100) 33 (20e50) 22 (10e39) 44 (30e59) 88 (56e90)
HI 100 (63e100) 62 (46e76) 33 (16e55) 68 (53e80) 80 (46e93)

For each case (t1/2 greater than 20, 30 or 40 minutes) SFU grade that resulted in 100% sensitivity was used. Optimized threshold of HI was used for prediction of t1/2 greater
than 20, 30 or 40 minutes. Accuracy equals true positive true negative/total positive total negative. Due to limited number of cases, exact 95% confidence interval is
provided (using binomial distribution).
 QUANTITATIVE ULTRASOUND FOR PEDIATRIC HYDRONEPHROSIS 1097

different from SFU selection using grades 3 and 4,

which we have shown performs significantly less
well than the QI approach presented in this report
(p <0.05 for all t1/2 thresholds). The criterion for the
study by Dias et al was need for pyeloplasty based
on nonstandard criteria, rather than defining a
threshold for more precise imaging.22
Several investigators have measured renal
parenchymal area to assess renal status in ves-
icoureteral reflux and hydronephrosis,23,24 and
recently in posterior urethral valves.25 Renal
parenchymal volume has been measured using 3-D
ultrasound to permit estimation of relative func-
tion.26 These approaches have focused primarily on
renal function rather than severity of obstruction
yet indicate the potential usefulness of ultrasound
in estimating relative renal function.
Figure 3. ROC curves for quantitative imaging (SVM and LOG
To our knowledge, this is the first study to relate
methods), SFU grading and hydronephrosis index methods renal morphological features from US with clinical
for selecting patients with t1/2 greater than 30 minutes. Sens., parameters of DR. In a previous study proposed
sensitivity. Spec., specificity. Acc., accuracy. by Kim et al a clinical cohort of 46 patients was
evaluated.5 However, no study of the power of the
proposed HI as a meaningful indicator of renal
cannot answer those questions, but it can provide function was presented. We used a data cohort of
more objective criteria from ultrasonographic 50 patients, which provided a retrospective power
imaging that could support prospective studies of value of greater than 0.99.
congenital obstruction. There are several limitations to this pilot study
Objective prediction of clinically significant that will be addressed in future research. Despite
hydronephrosis in children has been an ongoing the satisfactory power value provided by the post
challenge. Erickson et al reported that SFU grade 3 hoc power analysis, the number of patients may
has never been associated with reduced differential be relatively small for a condition that is as het-
uptake in pediatric kidneys.21 However, the erogeneous as hydronephrosis. Even so, the errors
dividing line between SFU grades 3 and 4 is not noted are small, and if the parameters are
clearly defined or reproducible.4 A recent report by conservatively defined, there is less risk of an
Dias et al presented the use of renal pelvic dilata- error of omission (ie missing detection of a patient
tion as highly predictive of the need for surgical with an increased t1/2). The current methodology
intervention, based on decreased function on requires hand drawn segmentation. While this is
dimercaptosuccinic acid scanning and not DR.22 not difficult, it is tedious and requires some
This approach used fetal and postnatal ante- training, and represents a potential source of
roposterior diameter of the renal pelvis, with interobserver variability. Ultimately the goal is to
thresholds of 18 mm for fetal and 16 mm for post- develop an automatic segmentation algorithm,27,28
natal measures. This approach was not statistically which would permit rapid evaluation of an image
to yield a hydronephrosis score that would be
available to the clinician for further decision
Table 3. Decrease in MAG3 scanning possible using QI vs SFU making.
grade
This study does not assess the potential of using
Threshold QI SFU Grade 3 SFU Grade 4 this methodology for clinical followup. It is unknown
1
T /2 greater than 20 mins: if the US parameters remain consistent or reflect
No. MAG3 scans 21 36 18 alterations in either direction as hydronephrosis
% Reduction from cohort 58 28 64 evolves. Hafez29 and Ross30 et al observed that
% Missed critical cases 0 5 42
1
T /2 greater than 30 mins: increasing hydronephrosis is indicative of obstruc-
No. MAG3 scans 25 36 18 tion. However, not all obstructed kidneys exhibit
% Reduction from cohort 50 28 64 increasing dilatation on followup, and it is unknown
% Missed critical cases 0 0 29
1
T /2 greater than 40 mins: if persisting hydronephrosis is safe. It remains to be
No. MAG3 scans 19 36 18 seen if QI may be able to more readily identify these
% Reduction from cohort 62 28 64 patients. That area is the subject of an ongoing
% Missed critical cases 0 0 13
study.
1098 QUANTITATIVE ULTRASOUND FOR PEDIATRIC HYDRONEPHROSIS

CONCLUSIONS renograms performed by up to 62%, depending on

We have demonstrated the potential clinical use- selection criteria used. While diuretic renography
fulness of a semiautomated means of quantitating remains the gold standard, the described technique
ultrasonographic images of hydronephrotic kidneys. has the potential to simplify and enhance our care of
This approach can decrease the number of diuretic children with hydronephrosis.

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EDITORIAL COMMENT

This report is a promising contribution to the hydronephrosis with regard to a conservative

never ending discussion among pediatric urolo- approach, followup and indications for surgical
gists about the proper diagnosis of congenital intervention. The semiquantitative approach, based
 QUANTITATIVE ULTRASOUND FOR PEDIATRIC HYDRONEPHROSIS
on ultrasonographic images, may lead to more
objective and, perhaps most importantly, reproduc-
ible results of diagnosis and outcome measures.
So far, semiquantitative US has been related to
t1/2 on MAG3 renography, a quite controversial
parameter, especially in younger children and in-
fants. To some extent, this method is observer
dependent but the same is the case in assessment
1099
of renography. Future studies will hopefully give us
the potential to assess differential renal function
using 3-D quantitative imaging as a noninvasive
tool without the exposure to radiation.
L. Henning Olsen
Department of Urology, Section of Pediatric Urology
Aarhus University Hospital
Aarhus, Denmark