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\begin{document}

\title{Motion corrected fetal body MRI provides reliable 3D lung volumes in
normal and abnormal fetuses}



\author[1]{Joseph Davidson}%
\author[2]{Alena Uus}%
\author[2]{Alexia Egloff Collado}%
\author[2]{Milou Van Poppel}%
\author[2]{Jacqueline Matthew}%
\author[1]{Johannes Steinweg}%
\author[2]{Maria Deprez}%
\author[3]{Michael Aertsen}%
\author[4]{Jan Deprest}%
\author[2]{Mary Rutherford}%
\affil[1]{Evelina London Children's Hospital}%
\affil[2]{King's College London School of Biomedical Engineering and Imaging Sciences}%
\affil[3]{Universitaire Ziekenhuizen Leuven}%
\affil[4]{Center for Surgical Technologies}%


\vspace{-1em}



  
  \date{May 25, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
Abstract Objective:Evaluate deformable slice-to-volume registration
(DSVR) to calculate 3D-segmented total lung volume (TLV) in fetuses with
congenital diaphragmatic hernia, congenital lung lesions and healthy
controls, with comparison to 2D-manual segmentation. Design:Pilot study
Setting:Regional fetal medicine referral centre Sample:Fetal MRIs
performed for clinical indications (abnormal cases) or as research
participants (healthy controls) Methods:Sixteen MRI datasets of fetuses
(22-32 weeks GA). Diagnosis: CDH(n=5), CPAM(n=2), CDH with BPS(n=1) and
healthy control(n=8). DSVR was used for reconstruction of 3D isotropic
(0.85 mm) volumes of fetal body followed by semi-automated lung
segmentation. The resulting 3D TLV were compared to the traditional
2D-based volumetry, and a normogram of DSVR-derived fetal lung volumes
from 100 cases was produced. Main Outcome Measures:Concordance with
2D-volumetry assessed with Bland-Altman analysis, results of
segmentations presented visually. Observed/Expected values were
calculated for abnormal cases based upon the normogram.
Results:DSVR-derived TLV values have high correlation with the 2D-based
measurements but with a consistently lower volume; bias -1.44cm3 {[}95\%
limits: -2.6 to -0.3{]} with improved resolution able to exclude hilar
structures even in severe motion corruption or in cases of lung
hypoplasia. Conclusions:Application of DSVR for fetal MRI provides a
solution for analysis of motion corrupted scans and does not suffer from
the interpolation error inherent in 2D-segmentation as per current
clinical practice. It increases information content of acquired data in
terms of visualising organs in 3D space and quantification of volumes,
which we believe will have important value for counselling and surgical
planning. Keywords:Fetal MRI; congenital diaphragmatic hernia; CPAM;
lung volume%
\end{abstract}%



\sloppy


\textbf{Motion corrected fetal body MRI provides reliable 3D lung
volumes in normal and abnormal fetuses}

Joseph Davidson\textsuperscript{1,2,3}\selectlanguage{ngerman}§, Alena Uus\textsuperscript{4}§,
Alexia Egloff \textsuperscript{5}, Milou van Poppel
\textsuperscript{4,6}, Jacqueline Matthew \textsuperscript{4}, Johannes
Steinweg \textsuperscript{4,6}, Maria Deprez\textsuperscript{4}, Michael
Aertsen\textsuperscript{7}, Jan Deprest\textsuperscript{2,8,9}, Mary
Rutherford \textsuperscript{5}

1. Department of Paediatric Surgery, Evelina Children's Hospital,
London, United Kingdom

2. Elizabeth Garrett Anderson Institute of Women's Health, University
College London, London, United Kingdom

3. GOS-UCL Institute of Child Health, London, United Kingdom

4. Biomedical Engineering Department, School of Biomedical Engineering
and Imaging Sciences, King's College London, London, United Kingdom

5. Centre for the Developing Brain, School of Biomedical Engineering and
Imaging Sciences, King's College London, London, United Kingdom

6. Department of Congenital Heart Disease, Evelina Children's Hospital,
London, United Kingdom

7. Department of Imaging and Pathology, Clinical Department of
Radiology, University Hospitals KU Leuven, Leuven, Belgium.

8. Clinical Department of Obstetrics and Gynaecology, University
Hospitals Leuven, Leuven, Belgium

9. Academic Department of Development and Regeneration, Cluster Woman
and Child, KU Leuven, Leuven, Belgium

§ contributed equally to this manuscript



\textbf{Abstract}

Objective: To evaluate deformable slice-to-volume registration (DSVR) to
calculate 3D-segmented total lung volume (TLV) in fetuses with
congenital diaphragmatic hernia, congenital lung lesions and healthy
controls, with comparison to 2D-manual segmentation. To establish
normogram of TLV calculated by DSVR in health control fetuses.

Design: Pilot study

Setting: Single regional fetal medicine referral centre

Sample:Fetal MRIs performed for clinical indications (abnormal cases) or
as research participants (healthy controls)

Methods: Sixteen MRI datasets of fetuses (22-32 weeks GA). Diagnosis:
CDH(n=6, one with coexisting BPS), CPAM(n=2), and healthy controls(n=8).
DSVR was used for reconstruction of 3D isotropic (0.85 mm) volumes of
the fetal body followed by semi-automated lung segmentation. The
resulting 3D TLV were compared to the traditional 2D-based volumetry,
and abnormal cases referenced to a normogram produced from 100 normal
fetuses whose TLV was calculated by DSVR.

Main Outcome Measures: Concordance with 2D-volumetry assessed with
Bland-Altman analysis, results of segmentations presented visually.
Observed/Expected values were calculated for abnormal cases based upon
the normogram.

Results: DSVR-derived TLV values have high correlation with the 2D-based
measurements but with a consistently lower volume; bias
-1.44cm\textsuperscript{3} {[}95\% limits: -2.6 to -0.3{]} with improved
resolution able to exclude hilar structures even in severe motion
corruption or in cases of very low lung volumes. lung hypoplasia.

Conclusions: Application of DSVR for fetal MRI is beneficial for the
analysis of motion corrupted scans and does not suffer from the
interpolation error inherent in currently applied 2D-segmentation as per
current clinical practice. It increases information content of acquired
data in terms of visualising organs in 3D space and quantification of
volumes, which we believe will improve counselling and surgical
planning.

Keywords\textbf{:} Fetal MRI; congenital diaphragmatic hernia;
congenital lung lesion; congenital pulmonary airway malformation;
bronchopulmonary sequestration; lung volume



\textbf{Introduction}

The antenatal work-up of fetal thoracic anomalies increasingly includes
fetal MRI in recent years. Fetal MRI aids in cases of diagnostic
uncertainty by detailed delineation of soft tissues within the fetal
chest, differentiating lung, bowel and liver more easily than
ultrasound\textsuperscript{1}, helping in the assessment of congenital
diaphragmatic hernia (CDH) and congenital lung lesions (CLL, including
congenital pulmonary airway malformation {[}CPAM{]} and bronchopulmonary
sequestration {[}BPS{]}). The currently standardised prognostic markers
for CDH and CPAM are the observed/expected Lung Head Ratio (O/E
LHR,\textsuperscript{2}) and the CPAM volume ratio
(CVR,\textsuperscript{3}), both measured by ultrasound. Both of these
metrics utilise single plane measurements of aspects of the fetal chest
to extrapolate volumes. Although these metrics are valid surrogates for
total lung volume (TLV, \textsuperscript{4}), generation of such values
may have inherent intra- and inter-operator
variability\textsuperscript{5}. Discrepancies between 2D ultrasound and
MRI-derived TLV measurements have been shown to be principally related
to the failure to account for the contribution of the ipsilateral
lung\textsuperscript{6}. Furthermore, ultrasound-based imaging struggles
with maternal habitus and fetal positioning, as well as extremes of
liquor volume. 3D ultrasound lung volume measurements have been shown to
be more difficult than by MRI, mainly because the most hypoplastic lung
cannot be properly visualized\textsuperscript{7}. High volume fetal
medicine centres have suggested that MRI-calculated lung volumes may be
a more accurate predictor of survival but that has not been formally
proven\textsuperscript{8}, however there is no standardised methodology
for the use of MRI in these cases which limits the compilation of large
datasets necessary for further study\textsuperscript{9}.

Modern clinical fetal MRI protocols (primarily based on single shot
turbo spin echo (ssTSE) sequence) allow fast acquisition of individual
2D slices that ``freeze'' fetal position in time. These slices have
sufficiently high image and contrast resolution for diagnostic purposes
in cases where fetal motion may previously have limited the information
available. However, the misalignment between individual slices leads to
corruption of volumetric information and loss of structural continuity
within a slice stack. Therefore, output MRI stacks are termed ``motion
corrupted''. In general, to achieve a sufficient coverage of fetal
visceral organs, clinical examinations require 3-6 MRI stacks acquired
under different orientations with respect to the fetal body. The degree
of motion corruption (misalignment of slices) can vary between the
stacks and normally depends on the gestational age, amount of amniotic
fluid, as well as fetal lie and mobility. It directly influences the
accuracy of the fetal lung volume assessment, which is based on 2D
slice-wise segmentation of motion-corrupted stacks followed by 3D
interpolation. Therefore, calculated TLV values might vary for different
stacks (from the same acquisition / the same subject) depending on the
amount of motion corruption and acquisition plane. This is considered
one of the limiting factors for MRI-based TLV assessment.

The recently proposed deformable slice-to-volume registration (DSVR)
method \textsuperscript{10} is used for reconstruction of
high-resolution (e.g., 0.8x0.8x0.8mm) isotropic 3D images of fetal body
from multiple low-resolution (e.g., 1.25x1.25x1.25mm) motion-corrupted
stacks. In DSVR method, one of the low-resolution stacks is selected as
an initial target space and it is then registered to each of the slices
using nonlinear free form deformation registration. This is followed by
super-resolution reconstruction (SR) of the 3D image from the registered
slices. The full pipeline includes 3 interleaved SR and SVR steps. The
resulting reconstructed images provide detailed 3D volumetric
information and can be reoriented in any plane.~This facilitates
accurate 3D segmentations of fetal lungs and other organs allowing
volumetric analysis.

In this work, we sought to explore how DSVR-derived lung volumes would
compare to those calculated by conventional manual 2D segmentation in
cases of fetal thoracic anomalies, with a comparison to normal control
cases.

\textbf{Methods}

\emph{Case Selection}

The investigated cohort for 2D vs. 3D TLV assessment included 8 cases
with abnormal lungs and 8 control cases from the iFIND project
{[}https://www.ifindproject.com{]} and clinical fetal cardiac MRI
databases. The abnormal cases included 6 cases of CDH (one with
concomitant BPS), and a further 2 cases of CLL (both CPAM). The eight
control cases were healthy control pregnancies and spanned approximately
the same gestational range as the abnormal cases (22-32 weeks
gestational age). In addition, 100 normal cases imaged as healthy
control participants for research purposes from 21-33 weeks gestational
age were used for the general assessment of 3D DSVR-derived fetal lung
volumetry growth chart. All datasets used in this research were
collected and processed subject to the informed consent of the
participants.

\emph{Data}

Each fetus was scanned using T2-weighted ssTSE sequence, producing
between 6 and 10 stacks in different planes, with varying degrees of
motion corruption. In all cases, images were acquired on an Ingenia 1.5
Tesla (Philips) system using T2w ssTSE: TR=15000ms, TE=80ms, voxel size
1.25x1.25mm, slice thickness 2.5mm and spacing 1.25mm. For the initial
16 study cases, 2D slice-wise segmentation of the fetal lungs was
performed in ITK-SNAP (http://www.itksnap.org) in the axial stack with
respect to the fetal trunk and a total fetal lung volume was calculated
using the conventional interpolation approach. These datasets also
underwent DSVR reconstruction to 0.85x0.85x0.85mm resolution using SVRTK
toolbox (https://github.com/SVRTK/SVRTK) and lung volumes were
calculated after automated 3D segmentation followed by manual refinement
in 3D Slicer (https://www.slicer.org). An example of one of the he
original 2D axial stacks affected by minor to moderate motion and the
corresponding 3D DSVR reconstruction are displayed side by side for
descriptive purposes in Figure 1 and Supplementary Video 1. The
processing of the additional 100 cases included reconstruction using the
standard DSVR pipeline \textsuperscript{10} followed by semi-automated
lung segmentation.

Lung volumes from the 16 cases derived from 3D DSVR and the conventional
2D-based approach underwent pairwise Bland-Altmann comparison to assess
for bias in measurement. In cases of CLL, lesion volume was calculated
and is provided here in cm\textsuperscript{3} and as a proportion of
TLV. A normal curve (growth chart) for fetal lung volumes was generated
for 21-32 weeks GA range from 100 DSVR reconstructions , and this curve
was compared descriptively to the previously published MRI-generated
fetal lung volume normograms \textsuperscript{11,12}.

\textbf{Results}

The examples of 2D vs. 3D lung segmentations for 4 cases are depicted in
Figure 2; motion corruption of the axial-plane stack can clearly be
appreciated in the coronal plane, with the coronal section of the DSVR
shown alongside each case. DSVR was able to produce clear images even
from severely motion-corrupted stacks (Figure 2C) and the resultant
images can be examined in any plane and at a higher resolution than that
of the original input stack (Figure 1, Video 1). The resultant
segmentation of fetal lungs demonstrates a smooth outline, with normal
cases depicting sufficient detail even to appreciate the lingula (Figure
2A) or a systemic feeding vessel in cases of CLL (Figure 2B). Comparison
of the volumes generated from 2D and 3D segmentation is made in Figure
3; results correlated strongly, however a consistently lower measurement
was made with 3D segmentation (Bland-Altman: Bias
-1.44cm\textsuperscript{3} {[}95\% confidence limits -2.63 to -0.24{]}).
This was felt to be due to the enhanced ability to exclude structures of
the vascular hilum in 3D reconstructions, as well as an inherent
reduction in interpolation error.

Having defined the fidelity of DSVR-derived 3D TLV, we proceeded to
produce a normal curve based upon 100 healthy cases undergoing fetal MRI
as normal controls for research, presented in Figure 4. The
corresponding fitted TLV normogram has a high correlation with the
previously reported gestational TLV curves produced from conventional 2D
segmentation data by Cannie et al\textsuperscript{11} and Meyers et
al\textsuperscript{12}. The generated regression line had a similar
R\textsuperscript{2} (0.72) to those published and was subsequently used
to generate the ``Expected'' value for the depiction of
Observed:Expected total lung volume in the abnormal cases.

The manually segmented 2D lung volumes and corresponding DSVR lung
volumes are depicted graphically in Figure 5 with reference to the
DSVR-derived normal curve. Table 1 displays data calculated from anomaly
cases. CPAM lesion volumes were calculated from DSVR reconstructions and
are presented as a percentage of the remaining TLV; of note one case had
CDH and a BPS of the lung on the same side as the hernia, this case had
significantly smaller lesion volume related to lung volume.

\textbf{Discussion}

This study demonstrates that MRI of the fetal thorax can be processed by
3D DSVR reconstruction, and subsequent lung volumetry can be performed
with similar volumes generated to the 2D-manual segmentation derived
volumes currently used in clinical practice for O/E TLV assessment.
Furthermore, 3D lung segmentations potentially provide more accurate TLV
estimation since they minimise the errors on the conventional 2D-based
approach affected by the combination of misalignment of slices and
interpolation. The analysis of the quantitative comparison results as
well as the general visual inspection of 2D vs. 3D segmentations suggest
that using 3D DSVR-based TLV assessment may potentially resolve one of
the current limitations to the validity of MRI derived volumes in
predicting outcomes as reliably as LHR\textsuperscript{13}. This series
demonstrates that DSVR method provides the means for accurate
calculation of lung volumes for both normal and abnormal cases. This is
especially useful for CDH cases for more accurate evaluation of the
observed to expected lung volume ratios. The recent advances in image
processing methods reduce variability in
segmentation\textsuperscript{14}, further improving the reliability of
the volumetry results. We anticipate that MR based lung volumetry may
soon be validated as a reliable and more accurate prognostic indicator
than the current use of the LHR; since it would invariably more closely
predict true TLV. Furthermore, the ability to outline lesion volumes in
cases of CLL will likely produce a prognostic marker more faithful to
true lesion size than the currently utilised CVR where cross sectional
areas are utilised to estimate lesion volume relative to fetal size. The
consistency of such a method will certainly deliver on the recent plea
for consistency in prognostication of these cases\textsuperscript{9}. It
should be noted that although we have provided lesion volume
proportionate to TLV, it would be possible to segment any aspect of the
fetus and derive a corresponding volume ratio proportional to this as
well as the relative position of the organs (e.g., the degree of liver
herniation or position of the stomach in CDH cases)

Recently, it has also been demonstrated that DSVR reconstructed MRI
images may provide additional diagnostic information for complex fetal
anomalies\textsuperscript{1}. The illustrative cases included within
this dataset also show that DSVR will produce datasets that are more
accessible to the clinician by resolving motion corruption with a
resolution superior to that of the original input stacks. This will
certainly aid in prenatal counselling and planning of the operative
approach in neonatal thoracic surgery; the reliable depiction of
systemic feeding vessels in BPS, combined with US Doppler assessment may
reduce the reliance on early postnatal CT imaging \textsuperscript{15}.

Regarding longitudinal assessment of CDH or CLL, it should be recognised
that the repeated use of MRI is considerably more expensive, time
consuming and lengthy compared to an expert-performed ultrasound.
Therefore, we anticipate that there will continue to be a role for
ultrasound in the monitoring of such conditions to delivery. Indeed,
serial CVR assessment has recently been shown to be effective in
predicting a need for perinatal intervention in cases of
CLL\textsuperscript{16}.

\textbf{Conclusions}

This pilot study demonstrates the potential of a 3D reconstruction
platform such as DSVR in the analysis of the fetal lung, with an
emphasis on accuracy and reliability in image derived volumetry. We
anticipate that MR based lung volumetry may soon be validated as a
reliable and more accurate prognostic indicator than the current use of
the LHR.

Our current work focuses on deep learning methods in order to provide
reliable volumetric assessment for a wide range of anomalies as well as
optimisation of different MRI acquisition protocols. This will allow
integration of both DSVR and volumetry pipelines in different clinical
centres that employ fetal MRI on a regular basis.

\textbf{Acknowledgements}

The iFIND study, from which these cases are derived, was supported by a
Wellcome Trust IEH Award (102431). Research carried out at King's
College London is made possible by NIHR funding of the Biomedical
Research Centre; the views expressed here are those of the authors and
not necessarily those of the NHS, NIHR or DoH.

\textbf{Disclosure of Interest Statement}

None of the authors have any conflict of interest to declare.

\textbf{Author Contribution}

JD and MR designed the study, analysed and interpreted the data, drafted
the manuscript. AU designed the study, acquired the data, drafted the
manuscript. AE, MvP, JM, JS acquired data and provided critical review
of the manuscript. MD, MA, JD interpreted the data and provided critical
review of the manuscript. All authors approved the final version for
publication and agree to be accountable for all aspects of the work
presented here.

\textbf{Details of Ethics Approval}

This study received national ethics approvals through the NHS REC:
{[}07/H0707/105{]} in 2007 and {[}14/LO/1806{]} in 2014. All
participating pregnant women taking part consented for the use of their
imaging data in research.

\textbf{Funding Statement}

This study received no specific internal or external funding

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Available from: http://www.ncbi.nlm.nih.gov/pubmed/32622160\selectlanguage{english}
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\textbf{Hosted file}

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