Antenatal diagnosis and management of fetal megacystis and lower urinary tract obstruction
Fontanella, Federica
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Publication date: 2019
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Fontanella, F. (2019). Antenatal diagnosis and management of fetal megacystis and lower urinary tract obstruction. University of Groningen.
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bladder in the second and third
trimester of pregnancy
F. Fontanella, H. Groen, R. Smidt, L. Duin and C.M. Bilardo
abstract
Objective: To use 3D ultrasound images to construct reference values for fetal normal
urinary bladder size and volume between 15 and 35 weeks of gestation.
Methods: This was a prospective cross-sectional study carried out from 2016 to 2017 at the
University Medical Centre Groningen, the Netherlands. Singleton pregnancies in absence of fetal abnormalities were included in the study between 15 and 35 weeks’ gestation. All ultrasound examinations were performed by a trained sonographer. During each scan, lasting approximately 40-60 minutes, at least three 3D volumes of the urinary bladder were obtained for each fetus. Fetal bladder volume was calculated offline by the automatic volume calculation (AVC) tool and the manual virtual organ computer-aided analysis (VOCAL) technique, with 30° rotation angles. Postnatal data were reviewed, and only live-born children without congenital anomalies were kept in the study.
results: A 3D ultrasound sweep of the fetal bladder was obtained every 20 minutes in 225
pregnant women between 15 and 35 weeks of gestation. A total of 1238 measurements of urinary bladder volume (BV) and largest bladder diameter (LBD) were obtained. Urinary BV was successfully measured by the semi-automatic SonoAVC tool in 123 cases (55%) and by VOCAL method in all cases. There was no significant correlation between measurements obtained by SonoAVC and by VOCAL technique (r = 0.37). A linear relationship was observed between LBD and GA (r2: 0.78 for the largest LBD and 0.76 for the mean LBD), while a
polynomial regression line was fitted for the BV according to GA. Gestational age based normal ranges for the largest and mean LBD and bladder volume (BV) were constructed.
Conclusions: This normative data will be useful to establish if a bladder is pathologically
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Introduction
The function of the bladder is storing urine at low pressure and expelling it periodically via coordinated and sustained contractions (1). Neurogenic bladder dysfunctions, lower urinary tract obstruction (LUTO) or vesico-ureteral reflux can prejudice this function during fetal life and alter the physiological bladder filling and voiding process. When one of these conditions is suspected prenatally, it is crucial for the differential diagnosis and prognosis to objectively assess if the bladder size falls within normal ranges and to reproducibly triage an eventual pathological bladder enlargement (2)(3)(4).
Fetal bladder is standardly assessed at the first trimester scan, when the normal longitudinal bladder diameter measures less than 7 mm (5). However, beyond the 14th week
of gestation, although the assessment of bladder filling is part of every standard ultrasound examination (6)(7), a clear cut-off for defining normal or enlarged bladder size is lacking. Since the 1970s, hourly fetal urine production throughout gestation has been studied by using both 2D and 3D US (8)(9)(10)(11)(12)(13)(14)(15), showing that urinary production and bladder capacity progressively increase during gestation (16). However, all these studies have failed to report reference ranges and growth charts for fetal urinary bladder size beyond 14 weeks’ gestation. This means that currently the diagnosis of an enlarged bladder is largely based on a subjective judgment, rather than on objective parameters defining a normal or pathological bladder distension.
Main objective of the study was therefore to fill this gap and to construct charts of fetal bladder volume (BV) and longitudinal bladder diameter (LBD) from 15to 35 weeks of pregnancy.
Methods
A cross-sectional prospective study was carried out from May 2016 to October 2017 at the University Medical Center Groningen. Pregnant women with a viable singleton uncomplicated pregnancy and with an accurate gestational-age assessment were recruited from the 15th week of gestation age until 35 weeks’ gestation. Exclusion criteria were:
multiple pregnancies, fetal congenital abnormalities -detected either before or after birth-, and the use of medications or maternal diseases that could potentially affect fetal growth or diuresis (diabetes mellitus, smoking, hypertensive disorders). Postnatal data were collected in order to exclude neonates with abnormalities of pathological conditions at birth.
A trans-abdominal US scan was performed only once for each patient by a trained operator (FF) using either a Voluson E8 or E10 system (GE Voluson TM Healthcare, Zipf,
urinary bladder were collected.
For the measurement of the urinary bladder volume (BV), 3D sweeps of the lower fetal abdomen were taken, digitally stored and subsequently analyzed with the 4D View software (GE VolusonTM Healthcare, Zipf, Austria). The BV was calculated by using two methods:
Sono automatic volume calculation (SonoAVC) and manual Virtual Organ Computer-aided Analysis (VOCAL), drawing the contours of the fluid filled area at every 30º of rotation (Figure 1). Additionally, the longitudinal bladder diameter (LBD) was measured manually on the multiplanar 3D image, corrected to the exact mid-sagittal plane, by placing one caliper on the inner border of the bladder wall at the upper pole (bladder dome) and the other on the inner border of the lower pole (bladder neck). A single trained operator measured manually the LBD and drew the contours of the bladder.For the study design, patient selection and statistical method, the guidelines from Altman and Chitty (1993) and by Ioannou et al (2011) were followed. The measurements were modeled against the gestational age and reference charts were constructed. Polynomial regression models were fitted to the mean and standard deviation (SD) of each measurement as functions of gestational age.
The study was authorized by the Medical Ethics Committee in Groningen (dossier number NL54636.042.15).
Figure 1. 3D sweeps of fetal pelvis with manual Virtual Organ Computer-aided Analysis of bladder
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results
A total of 225 pregnant women at different gestation age participated once into the study (Table 1). BV and LBD were measured at 20 minutes’ interval. In 56 cases, the scan lasted less than 40 minutes and the third US measurement was not performed. In total, 1238 measurements were obtained.
table 1. Gestational age distribution of the study population.
GA N % 15 12 5,3 16 11 4,9 17 13 5,8 18 9 4,0 19 10 4,4 20 15 6,7 21 17 7,6 22 15 6,7 23 19 8,4 24 16 7,1 25 12 5,3 26 13 5,8 27 7 3,1 28 14 6,2 29 9 4,0 30 9 4,0 31 6 2,7 32 5 2,2 33 5 2,2 34 4 1,8 35 4 1,8 Total 225 100
The BV was measured by using both the SonoAVC and the VOCAL method. The SonoAVC tool was successful in identifying and calculating the BV in 123 (55%). In the remaining 102 cases (45%) where the SonoAVC failed to semi-automatically identify and calculate the BV, this was only calculated by the Vocal method. In the 123 cases with volume measured by both SonoAVC or VOCAL, the bladder measurements differed by 3% (mean difference 6 cm3) and a significant correlation was not found (r = 0.37).
The three volumes, from the largest to the smallest were used to visually reconstruct bladder dynamics (fi gure 2). During a span of 40 minutes, fetal voiding was visually observed in all cases and the BV decreased of minimal one-third of its maximal volume within a mean period of 32 minutes (within 32.0, 29.5and 32.4 minutes in the gestational age windows between 15-21 week, 22-26 weeks, and 27-35 weeks, respectively).
Figure 2. Dynamics of fetal micturition between 28 and 35 weeks (red line), between 21 and 27 weeks
(green line), and between 15 – 20 weeks (blue line): for each category, the mean of the maximal, medial and minimal bladder volume during the US examination has been calculated.
Gestational age based reference size and growth charts were reported for: mean BV (table 2a), largest BV (table 2b), mean LBD (table 2c) and largest LBD (table 2d). A linear relation was observed between LBD and GA (r2: 0.78 for the largest LBD and 0.76 for the mean LBD),
while a polynomial regression line was fi tted for the BV according to GA (fi gures 3-5).
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Figure 4. Largest fetal bladder volume (max BV, mm) and gestational age (weeks)
Figure 5. Mean longitudinal diameter (cm3)and gestational age (weeks).
Discussion
This study reports normograms for the longitudinal bladder diameter and bladder volume from 15throughout 35weeks of gestation. These are, to our knowledge, the first normative data enabling the definition of a normal bladder size during the second and third trimester of pregnancy.
Cut-offs of normal bladder size have long been known in the first trimester of pregnancy (2). However, LUTO, posterior urethral valves, VUR or neurogenic bladder dysfunctions are more frequently suspected later in pregnancy, when bladder size assessment has already proved valuable for predicting prognosis (2)(3)(17). So far, previous studies have reported the hourly urinary fetal production (HUFP) throughout gestation without reporting on the size of the urinary bladder(18)(12)(14).The lack of normative data on urinary bladder size has represented a major issue, in particular for the definition of megacystis in the second and third-trimester of pregnancy (19).
table 2. Fitted centiles of the largest longitudinal diameter (largest LBD, mm; 2d), mean longitudinal
bladder diameter (mean LBD, mm; 2c), largest bladder volume (BV, cm3; 2b) and mean bladder volume
(BV, cm3; 2a) for exact gestational week between 15 and 35 weeks of gestational age (GA).
2a 2b
GA fitted centiles mean BV fitted centiles largest BV
5th 50th 95th SD 5th 50th 95th SD 15 0,00 0,69 1,99 0,66 0,00 0,85 2,10 0,64 16 0,00 0,55 1,46 0,46 0,00 0,69 1,66 0,50 17 0,00 0,45 1,06 0,31 0,00 0,57 1,33 0,39 18 0,00 0,39 0,79 0,21 0,00 0,53 1,13 0,31 19 0,10 0,39 0,68 0,15 0,03 0,55 1,08 0,27 20 0,18 0,46 0,73 0,14 0,14 0,67 1,20 0,27 21 0,24 0,60 0,96 0,18 0,27 0,89 1,52 0,32 22 0,29 0,82 1,36 0,27 0,41 1,23 2,05 0,42 23 0,34 1,15 1,95 0,41 0,57 1,70 2,83 0,58 24 0,40 1,58 2,75 0,60 0,76 2,32 3,87 0,79 25 0,49 2,13 3,77 0,84 0,98 3,09 5,21 1,08 26 0,62 2,81 5,01 1,12 1,24 4,05 6,85 1,43 27 0,79 3,64 6,49 1,45 1,55 5,20 8,84 1,86 28 1,02 4,62 8,22 1,84 1,91 6,55 11,19 2,37 29 1,33 5,77 10,21 2,27 2,34 8,14 13,93 2,96 30 1,72 7,10 12,48 2,74 2,83 9,96 17,09 3,64
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GA fitted centiles mean BV fitted centiles largest BV
5th 50th 95th SD 5th 50th 95th SD 31 2,21 8,62 15,04 3,27 3,40 12,05 20,69 4,41 32 2,81 10,35 17,90 3,85 4,06 14,41 24,76 5,28 33 3,53 12,30 21,07 4,47 4,81 17,07 29,32 6,25 34 4,40 14,49 24,58 5,15 5,67 20,04 34,41 7,33 35 5,41 16,92 28,42 5,87 6,63 23,34 40,04 8,52 2c 2d
GA fitted centiles mean LBD fitted centiles largest LBD
5th 50th 95th SD 5th 50th 95th SD 15 0,00 5,05 11,47 3,90 3,99 6,08 8,17 1,27 16 0,00 6,53 13,32 4,13 5,43 7,79 10,15 1,43 17 0,85 8,01 15,17 4,36 6,84 9,50 12,16 1,62 18 1,95 9,49 17,03 4,58 8,21 11,21 14,21 1,83 19 3,06 10,97 18,88 4,81 9,53 12,92 16,31 2,06 20 4,17 12,45 20,73 5,03 10,82 14,63 18,44 2,32 21 5,28 13,93 22,58 5,26 12,06 16,34 20,62 2,60 22 6,38 15,41 24,44 5,49 13,25 18,05 22,85 2,92 23 7,49 16,89 26,29 5,71 14,40 19,76 25,12 3,26 24 8,60 18,37 28,14 5,94 15,49 21,47 27,45 3,64 25 9,70 19,85 30,00 6,17 16,53 23,18 29,83 4,04 26 10,81 21,33 31,85 6,39 17,51 24,89 32,27 4,49 27 11,92 22,81 33,70 6,62 18,44 26,60 34,76 4,96 28 13,03 24,29 35,55 6,85 19,30 28,31 37,32 5,48 29 14,13 25,77 37,41 7,07 20,10 30,02 39,94 6,03 30 15,24 27,25 39,26 7,30 20,84 31,73 42,62 6,62 31 16,35 28,73 41,11 7,53 21,51 33,44 45,37 7,25 32 17,46 30,21 42,96 7,75 22,11 35,15 48,19 7,93 33 18,56 31,69 44,82 7,98 22,64 36,86 51,08 8,64 34 19,67 33,17 46,67 8,21 23,10 38,57 54,04 9,41 35 20,78 34,65 48,52 8,43 23,48 40,28 57,08 10,22 table 2. Continued 2a 2b
Thus far, the definition of megacystis beyond the first trimester has been heterogeneous including: a longitudinal bladder measurement above the 99th centile without referring
to any normative data (20); a fetal bladder reaching the umbilical cord insertion, or most commonly, a bladder failing to empty within 45 minutes (21). All these definitions lack an objective cut-off to define a physiological and pathological bladder distension and to allow reproducibility and consistency among the studies. Maizels et al. were the first in the literature to propose a mathematical formula to calculate the LBD according to GA, but only based on 39 normal bladders measurements between 15 and 40 weeks’ gestation (22). The study reported a linear relationship between GA and largest LBD and the calculated formula was LBD = GA – 5. We also found a linear relationship between LBD and GA, but with the following formula defining the mean physiological LBD: LBD = 1.48 * GA - 17.15.
The bladder volume can be assessed either by applying a mathematical formula for the three bladder diameters (longitudinal, antero-posterior and transverse) obtained by 2D US, or by directly calculating the volume on 3D pictures taking into account the true shape of the fetal bladder. Two major limitations can be envisaged with the first approach: first, the fact that the volume is calculated on an arbitrarily selected image, assumed to represent the maximal bladder size and (8) second, the difficulty of choosing an appropriate formula to calculate the BV from the bladder diameters. In fact, throughout the filling phase, the bladder shape changes from an ellipsoid to a super-ellipsoid, a virtually more cylindrical shape(8). Therefore, the use of a unique formula for estimating the bladder volume at different filling phases and GA it is not appropriate (23)(8). Both these limitations can be overcome by the use of a 3D US technique enabling accurate volume estimation, even in irregularly shaped or asymmetrical organs (24)(25)(26). Three D technique is at present the most accurate method (27) for calculating the BV and we therefore report charts and centiles for the 3D-measured fetal bladder volume.
After acquisition of a 3D image, different methods can be used to measure the volume of an organ, such as the rotational Virtual Organ Computer-aided AnaLysis ((VOCAL); GE Medical Systems, Zipf, Austria) or the automated segmentation tool for fluid-filled spaces Sono-AVC (GE Medical Systems). The Sono-AVC tool semi-automatically recognizes, traces and measures the fluid-filled structures in the 3D volume. This tool represents the easiest and quickest method in daily practice, however the volumes obtained on the same image with either SonoAVC and VOCAL setting in our cohort were not strictly correlated (r=0.037), and the SonoAVC method failed in recognizing the right structure in 45% of our cases. The VOCAL method has been previously used for measuring the BV by Peixoto-Filho et al. (27). The authors also investigated the inter- and intra-observer reliability by using 15 and 30° rotation steps calculation. Since an excellent correlation between the two measurements was found, the authors suggested to use 30° of rotation as this is significantly faster. This is why we adopted 30° rotational angle.
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As 3D technique is not universally available, we also propose reference ranges for LBD,based on 2D Images and therefore more easily applicable in daily practice.
In the present study, the 40-minutes period for the US examination resulted in the observation of a complete bladder cycle of filling and voiding in all fetuses. This confirms the results of Hata et al., which reported that the time needed for observing the bladder empty was approximately 30 minutes at 28 weeks, and 40 minutes at 35 weeks’ gestation (28). These and our results (figure 1), confirm that the capacity of the fetal bladder to store urine and empty changes and matures with advancing gestation, with a progressively increasing capacity and more complete emptying with advancing gestation (1).As we examined the fetuses for 40 minutes, the HUFP could not be calculated. However, the HUFP has been already reported in details by other studies, and recently by using 3D US scans (11)(29).
A strength of this study is its prospective and cross sectional design, in accordance to the best practice for constructing fetal reference charts (30)(31). Moreover, the US examinations were performed by the same operator (F.F.), and the contours of the urinary bladder and the LBD were all measured by another operator (R.S.) This should have limited any inter-operator bias.
In conclusion, we provide normograms for fetal bladder size during the second and third trimester of pregnancy. Future research is needed to validate these results and define an objective threshold for second and third-trimester megacystis.
appendix 1. Micturition dynamics between 15 – 20 weeks.
appendix 2. Micturition dynamics between 21 and 27 weeks
appendix 3. Micturition dynamics between 28 and 35 weeks.
Examination time (40 minutes)
Bladder volume 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8 2.0 2.2 2.4
Examination time (40 minutes)
Bladder volume 0 10 20 30 40 50
Examination time (40 minutes)
Bladder volume 0.0 0.5 1.0 1.5 2.0 2.5
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