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Journal of Pediatric Urology (2018) 14, 277.e1e277.

e6

Is the renal pyramidal thickness a good


predictor for pyeloplasty in postnatal
hydronephrosis?

Amr Hodhod a,b, John-Paul Capolicchio a, Roman Jednak a,


a
Hadeel Eid c, Abd El-Alim El-Doray b, Mohamed El-Sherbiny a
Department of Pediatric
Surgery, Montreal Children’s
Hospital, McGill University, Summary Results
Montreal, Quebec, Canada The total included cases were 155 patients (165
units). One hundred and fourteen units had grade 3
b
Department of Urology, Objectives hydronephrosis and 51 units had grade 4 hydro-
Faculty of Medicine, Menoufia We evaluated the feasibility and value of renal py- nephrosis. Fifty-two cases (55 units) underwent
University, Al Minufya, Egypt ramidal thickness (PT) as a predictor of pyeloplasty pyeloplasty. The median follow-up period was 37.6
in high-grade postnatal hydronephrosis. months. PT measurement was reliable (ICC Z 0.94).
c
Pediatric Radiology Division, Univariate analysis revealed that SFU grading, APD,
Montreal Children’s Hospital, PT, T1/2, and MAG-3 curves were associated with
McGill University, Montreal, Patients and methods surgery. Multivariate analysis showed that PT was a
Quebec, Canada We retrospectively reviewed the charts of patients single independent predictor for pyeloplasty.
who presented with postnatal hydronephrosis from PT  3 mm had 98.1% sensitivity and 89.7% speci-
Correspondence to: A. Hodhod, 2008 to 2013. Included cases had grade 3 or 4 ficity in predicting pyeloplasty.
Department of Pediatric hydronephrosis. We included only units diagnosed as
Surgery, McGill University, The
ureteropelvic junction obstruction. Gender, later- Discussion
Montreal Children’s Hospital,
Room B04.2916.1 GLEN, 1001
ality, hydronephrosis side, renogram data, and PT is the first portion of renal parenchyma that is
Boulevard Décarie, Montréal, follow-up data were recorded. Two investigators affected in high-grade hydronephrosis. Moreover, it
Quebec H4A 3J1, Canada, Tel.: reviewed all patients’ ultrasounds images. We changes little over the first 9 years of life. PT mea-
þ1 4514 412 4384 measured PT and pelvic anteroposterior diameter surement in hydronephrosis was not previously
(APD) in the last ultrasound before surgery. For evaluated. We found that PT was easily measured in
amr.hodhod@mail.mcgill.ca those managed conservatively, measurements were most kidneys with high negative predictive value.
(A. Hodhod) obtained from the ultrasound with worst hydro- The PT value as an indicator for pyeloplasty should
nephrosis. PT was measured in supine position in the undergo extensive assessment by other institutions
Keywords middle third of the sagittal plane (Figure). We with different protocols.
Hydronephrosis; Pelvi-ureteric
assessed the reliability of PT measurement using the
junction obstruction;
Ultrasonography
intraclass correlation coefficient (ICC). Univariate Conclusion
and multivariate analyses were used to correlate the Being a slowly growing part of the parenchyma, PT
collected parameters to pyeloplasty incidence. can be a good measurable parameter to predict
Received 17 July 2017
Accepted 15 January 2018
Receiver operating characteristic curve was used to pyeloplasty. Measurement of PT in hydronephrosis is
Available online 20 March 2018 evaluate the cutoff value of PT that predicts reliable. PT  3 mm can predict pyeloplasty with
pyeloplasty. 98.1% sensitivity and 89.7% specificity.

Figure Measurement of the renal pyramidal thickness.

https://doi.org/10.1016/j.jpurol.2018.01.025
1477-5131/ª 2018 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved.
277.e2 A. Hodhod et al.

Introduction by Kadioglu [7]. PT was measured in the middle third of the


sagittal renal ultrasonic images that were captured in su-
Many studies have evaluated the prediction value of ultra- pine position, as the distance between the cup of calyx and
sound parameters regarding the surgical intervention and the base of pyramid. To get the most accurate measure-
renal function [1e3]. Renal parenchymal thinning was ment, we selected the sagittal images that showed mostly
considered as a subjective parameter to define the severity all pyramids. Further, we chose the one with maximal
of hydronephrosis [4e6]. diameter of the mid-renal pyramid. We considered PT in a
However, in addition to its subjectivity, the parenchymal non-visualized pyramid, in all renal sagittal images, with
thickness essentially changes with age that makes its clin- very thin parenchyma as 0 mm. Moreover, we measured PT
ical application difficult especially in bilateral hydro- of the contralateral kidneys if not included in the diseased
nephrosis [7]. The pyramidal thickness (PT) changes little group.
over the first nine years of life, which makes it superior to Moreover, APD was measured at the mid-renal trans-
the parenchymal thickness [7]. verse plane of the renal pelvis in the supine position.
Multiple classification systems were used to define Mercaptoacetyltriglycine 3 (MAG-3) was indicated for all
various grades of antenatal hydronephrosis (ANH) patients with SFU grade 4. Patients with SFU grade 3 had
[4e6,8,9]. PT is the first portion of renal parenchyma that is MAG-3 when hydronephrosis was bilateral high grade, in a
affected in high-grade hydronephrosis [7]. Using PT to single kidney or worsening in subsequent ultrasounds. We
define the hydronephrosis severity, regarding ureteropelvic recorded MAG-3 data regarding the differential renal func-
junction obstruction (UPJO) has not been reported before. tion (DRF), post-Furosemide radioisotope T1/2 washout and
We tried to prove the feasibility and reliability of PT curve type. When the T1/2 was <10 min, non-obstructive
measurement in hydronephrosis. The renal pyramid grows renogram was considered. In cases of T1/2 > 10 min, we
slowly during the first years of life. Owing to its proximity to reviewed the renal washout percentage to exclude
the calyx, it is the first part of the renal parenchyma to be obstruction. Renogram curve types were obstructive or not
affected by the increase of intracalyceal pressure. So, we obstructive. Obstructive curve was considered when
hypothesized that PT measurement can be utilized to continuously rising or slow down sloping without adequate
assess the need for pyeloplasty. We evaluated PT as a washout (<50%) in response to furosemide, otherwise the
predictor for pyeloplasty compared with other possible curve was considered to be non-obstructive [10].
predictors such as anteroposterior diameter (APD), Society We reviewed the hydronephrosis outcome regarding the
for Fetal Urology (SFU) grading, and renogram findings. surgical intervention throughout the follow-up period.
Parenchymal thinning in SFU grade 4 is not objectively Pyeloplasty was indicated when DRF < 40% with impaired
well defined. In the current study, we provided a feasible drainage (T1/2 > 20 min) or deterioration of the renal
alternative measurement that would help in defining sur- function > 10% on follow up renogram study. Moreover,
gically important parenchymal thinning. surgery was indicated in cases of high-grade worsening
hydronephrosis on follow-up ultrasound or symptomatic
hydronephrosis. These indications are similar to that of the
Patients and methods SFU recommendations [11]. Otherwise, conservative man-
agement was considered. Patients who underwent conser-
Local ethics approval was obtained (#14-256-ped.). vative management were followed up every 3e6 months.
We retrospectively reviewed patients’ charts who pre- When worsening hydronephrosis was detected, MAG-3 was
sented with antenatal hydronephrosis (ANH) from January performed. Patients with improving hydronephrosis were
2008 till December 2013. All included patients presented followed at longer intervals.
with ANH in the first year of life and had SFU grade 3 or 4 According to our institutional post-pyeloplasty protocol,
initially diagnosed as isolated hydronephrosis. We excluded patients had their first ultrasound study within the first 3
cases associated with posterior urethral valve (PUV), months postoperatively then after 3e4 months. The fre-
vesico-ureteric reflux (VUR), ureterocele, vesicoureteric quency of further follow-up was decided by the surgeon. PT
junction obstruction (VUJO), and neurogenic bladder. was remeasured post pyeloplasty by reviewing post-
Moreover, we excluded patients with UPJO of non- operative ultrasound images during short-term follow up.
functioning kidneys. For renal units with preoperative PT > 0 mm, the per-
We recorded the patients’ personal data regarding the age centage of PT change (DPT%) was calculated using the
and gender. Laterality and side of hydronephrosis were also following formula:
collected. Two investigators (A.H.) and (H.E.) reviewed all
patients’ ultrasound images. This review was blinded to sur-
gical need and outcome. The last ultrasound before surgery ½postoperative PT  preopertive PT  100
was reviewed. Otherwise, for units managed conservatively, :
preopative PT
the ultrasound with worst hydronephrosis was reviewed.
Postnatal hydronephrosis was graded using the SFU system. When the preoperative PT Z 0, we calculated the PT
We collected only renal units with SFU grade 3 or 4. SFU grade change (DPT) according to the following formula: post-
3 was defined as dilated renal pelvis and all renal calyces with operative PT e preoperative PT.
normal parenchyma while SFU grade 4 was considered as Postoperative hydronephrosis status was assessed by
grade 3 but with parenchymal thinning [5]. comparing hydronephrosis grade pre- and postoperatively
Thereafter, PT was measured. The method and in- according to the SFU system [5]. Thereafter, downgraded
terpretations of PT measurement were applied as described was defined was “improved hydronephrosis” and the term
Pyramidal thickness as a predictor for pyeloplasty 277.e3

“non-improved hydronephrosis” was considered for units


Table 1 Patient demographics.
with the same or upgraded hydronephrosis.
Our primary outcome was to study the feasibility of PT Number Percentage
measurement in hydronephrosis. Moreover, our secondary Gender
outcome was to assess the usefulness of PT in prediction of Male 124 80
pyeloplasty. Female 31 20
SPSS 20 was used for recording patients’ data and sta- Laterality
tistical analysis. The intraclass correlation coefficient (ICC) Unilateral 77 49.7
was used to test the inter-rater reliability (0.7 indicates Bilateral 78 50.3
good reliability). Internal consistency was tested using Side
Cronbach’s alpha (0.7 indicates robust consistency Right 40 24.2
without redundancy). For better evaluation of PT, average Left 125 75.8
PT was used [(PT measured by investigator 1 þ PT measured SFU grade
by investigator 2)/2]. Univariate and multivariate analyses Grade 3 114 69.1
were done using Cox regression. Univariate analysis was Grade 4 51 30.9
used to correlate patients’ gender, laterality, the SFU
grading system, average PT, APD, and MAG-3 findings
regarding pyeloplasty. Gender, laterality, SFU grading, and
type of MAG-3 curve were considered categorical variables. We were not able to measure PT in six out of 165 renal units
PT, APD, T1/2, and DRF were considered continuous vari- (3.6%) because of inadequate ultrasonic images. The median
ables. PT for units that underwent pyeloplasties (preoper- PT was 3.5 mm (range 0e7 mm). Average PT was considered
ative PT) and those managed conservatively was compared 0 mm in 17 renal units with sever parenchymal thinning. The
with the contralateral side. ICC was 0.94 for diseased group, and for the control group the
Furthermore, multivariate analysis was done for pa- ICC was 0.89. Cronbach’s alpha was 0.97 for the diseased
rameters with p < 0.1. Multicollinearity was evaluated for group and 0.94 for the control group (Table 2).
parameters found to be significant in the univariate analysis Ninety-eight out of 155 patients (63.2%) with 106 units
using linear regression model. Value of variance inflation had MAG-3 renograms. Thirty-nine out of 98 patients (40%)
factor (VIF) > 5 indicated a multicollinearity problem.
Receiver operating characteristic (ROC) curve was used
to evaluate the cut-off value of average PT that predicts
pyeloplasty. Moreover, Spearman’s rank correlation test Table 2 PT measurement reliability by both investigators.
was used to determine the correlation between the T1/2 Parameter Observer 1 Observer 2
and PT. The KruskaleWallis test was used to evaluate DPT% Diseased group
in relation to the postoperative status of hydronephrosis. A Units measured (%) 161/165 159/165
p-value  0.05 was defined as significant. (97.6) (96.4)a
Median PT (range)
All units (range) 3.6 (0e7) 3.5 (0e7)
Results Pyeloplasty units 1.6 (0e3.2) 1.8 (0e3.4)
Conservatively 4.4 (1e7) 4.3 (2e7)
Of 626 cases with ANH, 256 cases were considered as SFU managed units
grade 3 or grade 4. We excluded three cases with PUV, 28 Units with PT equals 0 18 17
cases with VUR, 30 cases with non-obstructing megaureter, Intraclass correlation coefficient
seven cases with vesicoureteric junction obstruction, and All units 0.95
six cases with neurogenic bladder. Moreover, we excluded Pyeloplasty units 0.92
21 cases with missed follow-up during conservative man- Conservatively 0.91
agement and six patients considered non-functioning by managed units
renogram. Cronbach’s alpha
Total eligible cases were 155 patients (165 units). Pa- All units 0.97
tients’ demographics are presented in Table 1. Of 78 cases Pyeloplasty units 0.96
with bilateral hydronephrosis only 10 patients (12.8%) had Conservatively 0.94
bilateral grade 3 or 4 while the others (87.2%) had one unit managed units
with grade 3 or grade 4 and hydronephrosis of lower grade Control group
on the contralateral side. Units measured (%) 141/145 140/145
The median age at presentation is 0.5 months (97.3) (96.5)a
(0.03e11.6). Median PT (range) 6.2 (5e7) 6.3 (5e7)
Included ultrasound measurements were obtained at a Intraclass correlation 0.89
median age of 3.3 months (0.1e48.3). The median age of coefficient
measurements for patients who underwent pyeloplasties Cronbach’s alpha 0.94
was 4.9 months (0.1e48.3) and 2.5 months (0.2e14.1) for
PT Z pyramidal thickness.
those who were managed conservatively (p Z 0.001). a
All units that investigator 1 was not able to measure were
The median APD for all renal units was 13 mm (range
included in the units that investigator 2 could not measure.
3.5e47 mm).
277.e4 A. Hodhod et al.

had more than one renogram. The median age at renogram The median postoperative follow up period was 29
was 3.2 months (0.9e50 months). Fifty-one out of 106 units (6.3e98.4) months. Postoperative PT was measured in 41
(48.2%) had a non-obstructive curve, and 55 units (51.8%) out of 55 units (74.5%) at median postoperative time in-
had obstructive ones. The median DRF was 48% (17e68%) terval 7.6 months (6.1e9.4). We could not measure PT in 14
while the median T1/2 was 8.8 (1.8e650) minutes. units because the renal pyramids were not clearly defined
The median follow-up period for all cases was 37.6 within the parenchyma. The median DPT% was 69.6% (100
(12.5e102) months. to 358.3). Renal units with non-visualized PT (PT Z 0 mm;
Fifty-two patients with 55 out of total included renal 12/17 units, 70.6%) were improved with median
units (33.3%) underwent pyeloplasty. Thirty-three percent DPT Z 2.30 mm, one unit showed no improvement, and we
(18/55 units) were SFU grade 3 while 67% were grade 4 (37/ were not be able to define the renal pyramid within the
55 units). On the other hand, 110 units (66.7%) were remaining units. Hydronephrosis improvement was noted in
managed conservatively. Of the conservatively managed 38 out of 41 (92.7%) units and three units were not
units, 50% (55/110 units) were resolved while the others improved. One unit with non-improved hydronephrosis un-
were either improved or had the same hydronephrosis. derwent redo pyeloplasty and two units showed improve-
The median average PT for units that underwent pye- ment on subsequent ultrasounds. The renal unit that had
loplasty was 1.8 (0e3.2) mm while for resolved renal units redo pyeloplasty had a preoperative PT Z 1.5 mm and
on conservative management was 4.35 (2e7) mm. We postoperative PT Z 0. The status of hydronephrosis showed
measured the PT in 141 contralateral kidneys. We were not excellent association with DPT% (p Z 0.004). For the non-
able to measure the contralateral PT in five units. The defined pyramids, preoperative PT was 0 mm in 11 out of
median contralateral PT was 6.2 (5.8e7) mm. Twenty-seven 14 units (78.6%) because of significant thin parenchyma.
patients had contralateral SFU grade 2, grade 1 was diag-
nosed in 41, and the remaining patients had non-
hydronephrotic contralateral kidneys. The median contra- Discussion
lateral PT was 6.2 mm for those who had pyeloplasties or
were treated conservatively (p < 0.001 in both groups). The The renal pyramid is the first renal component that is
median APD for units undergoing pyeloplasty was 25 affected by hydronephrosis [7]. So, it can be a good
(13e47) mm. While for units with conservative manage- parameter to evaluate the hydronephrosis severity. We
ment, the median APD was 9.4 (3.5e20) mL. included only SFU grade 3 and 4 because pyeloplasty deci-
Univariate analysis revealed that SFU grade 4, APD, sion is made for considering these grades.
average PT, T1/2, and a MAG-3 obstructive curve had sig- Kadioglu [7] measured PT in healthy children. According
nificant relationships with pyeloplasty (Table 3). to his results, during the first year of life the mean PT is
Multivariate analysis (Table 3) showed that PT was a 6 mm while at the age of nine it is 7 mm; so, it was slightly
single independent predictor for pyeloplasty. The multi- changed within the first years of life. In comparison to the
collinearity statistics yielded a VIF value of 2.1 and 2.3 for whole parenchymal thickness, which was significantly
APD and PT respectively. This revealed non-problematic changed with age (9 mm at 1 year to 13.3 mm at 9 years)
multicollinearity. [7]. So, we used PT to evaluate hydronephrosis severity
The ROC curve was used to estimate the cut-off value of because it is easier to interpret than the whole paren-
average PT regarding the pyeloplasty incidence. The area chymal thickness.
under the curve (AUC) was 0.965 (Fig. 1). A cut-off value of PT measurement in hydronephrosis was not previously
3 mm had 98.1% sensitivity and 89.7% specificity regarding evaluated. We found that PT was easily measured in most
the need for surgery (positive predictive value kidneys. However, the feasibility of postoperative mea-
(PPV) Z 0.82.8 and negative predictive value (NPV) Z 0.99). surement was lesser as some renal pyramids were not easy
Moreover, there was a moderate correlation between T1/2 identified. Moreover, we measured the contralateral PT as
and average PT (r Z 0.58, p < 0.001). an internal control for those who underwent pyeloplasties

Table 3 Univariate and multivariate Cox regression analyses regarding pyeloplasty.


Parameters Univariate analysis Multivariate analysis
Hazard ratio (confidence interval) p Hazard ratio (confidence interval) p
Gender 0.846 (0.445e1.609) 0.61 e
Laterality 0.599 (0.33e1.086) 0.11 e
SFU Grade 3 0.207 (0.115e0.371) <0.001 0.976 (0.456e2.09) 0.6
Grade 4 1 1
PT 0.485 (0.4e0.584) <0.001 0.639 (0.481e0.849) 0.002
APD 1.067 (1.031e1.104) <0.001 1.03 (0.993e1.068) 0.12
MAG-3 T1/2 1.003 (1.003e1.005) 0.01 0.998 (0993e1.003) 0.42
DRF 0.992 (0.975e1.009) 0.339 e
Curve Obstructive 1 <0.001 1 0.07
Non-obstructive 0.14 (0.06e0.328) 0.484 (0.225e1.041)
APD Z pelvic anteroposterior diameter; DRF Z differential renal function; PT Z pyramidal thickness.
Pyramidal thickness as a predictor for pyeloplasty 277.e5

Figure 1 Evaluation of the cutoff value of PT for prediction of pyeloplasty using the receiver operating characteristic curve with
the coordinates of the curve. Area under the curve interpretations: 0.90e1 Z excellent; 0.80e0.89 Z good; 0.70e0.79 Z fair;
0.60e0.69 Z poor; 0.50e0.59 Z fail.

or managed conservatively. There were significant differ- We did not exclude renal units with PT Z 0, as evalua-
ences in both groups; this indicated the early affection of tion of PT as a reliable and valid parameter was to be
PT in high-grade hydronephrosis. assessed by at least two investigators for all patients with
Many pyeloplasty predictors were previously evaluated. SFU grade 3 and 4. Otherwise, the agreement of non-
APD is the best predictor for surgical intervention in UPJO visualized PT (PT Z 0 mm) would not be assessed.
[1,2]. Mudrik-Zohar and colleagues [2] reported that the Post pyeloplasty, the renal parenchymal growth is more
parenchymal thickness is a good predictor of postnatal evident than APD reduction [15]. We found that DPT%
pyeloplasty especially if used as APD/parenchymal thick- post pyeloplasty is associated with hydronephrosis
ness ratio. Moreover in a recent prospective study, the APD improvement.
and DRF were considered the most independent predictors The preoperative non-assessed PT could be due to py-
for pyeloplasty [12]. In our study, only PT showed to be ramidal atrophy [16]. We supposed that PT could not be
associated significantly with pyeloplasty. assessed postoperatively due to absence of cortico-
All available grading systems classify ANH according to medullary differentiation secondary to previous atrophy or
the probability of complication or surgery [4e6,9]. SFU fibrosis. Despite the significant association between DPT%
grade 4 is just different from grade 3 by the presence of and postoperative hydronephrosis status, the percentage of
thin parenchyma [5]. However, SFU grade 4 is not a good non-defined PT (25.5%) may hinder its use as a good pre-
predictor of pyeloplasty [12]. The inter-rater reliability of dictor for improvement especially for units with thin pa-
grade 3 hydronephrosis is low [13]. This may be because the renchyma (grade 4).
parenchymal thinning is not clearly defined to differentiate Measurement of PT just before surgery or the worst
between grade 3 and grade 4 [14]. hydronephrosis for non-operative group reflects the time at
According to our results, PT is a good predictor for which the PT is maximally affected in both groups. Thus, it
pyeloplasty in high-grade hydronephrosis and DPT% is makes the comparison of PT regarding the surgical or con-
associated with postoperative hydronephrosis status. servative managements more justified. The trend of PT in
Moreover, it is correlated with post-furosemide T1/2. The both groups could be a further step in evaluating the PT
important factor to classify the hydronephrosis is to predict value in high-grade hydronephrosis management.
the probability of surgical intervention. High-grade hydro- Further studies are needed to evaluate agreement of PT
nephrosis was defined as hydronephrosis associated with measurement and its ability to predict surgical intervention
parenchymal thickness <50% regarding the measurement of for other causes of hydronephrosis according to the natural
a normal contralateral kidney [3,4]. However, it cannot be history. Furthermore, assess of PT utility in the term of
applied for patients with bilateral hydronephrosis. To definition of parenchymal thinning.
clearly define the parenchymal thinning, it necessitates The determination of the “need” for pyeloplasty re-
using a parameter that not changes significantly with the mains subjective. We presented our indications of pyelo-
first years of life. plasty that not all other practitioners would follow. The PT
277.e6 A. Hodhod et al.

value as an indicator for pyeloplasty should undergo detected pelvi-ureteric junction obstruction. Eur J Nucl Med
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