The Journal of Maternal-Fetal & Neonatal Medicine

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Stomach position versus liver-to-thoracic volume ratio in left-sided congenital diaphragmatic hernia Anne-Gaël Cordier, Mieke M. Cannie, Lucie Guilbaud, Jocelyne De Laveaucoupet, Jéléna Martinovic, Dorota Nowakowska, Malgorzata MilejskaLewandowska, Carlota Rodó, Benjamin Viaris de Lesegno, Carmela Votino, Marie-Victoire Senat, Jacques C. Jani & Alexandra Benachi To cite this article: Anne-Gaël Cordier, Mieke M. Cannie, Lucie Guilbaud, Jocelyne De Laveaucoupet, Jéléna Martinovic, Dorota Nowakowska, Malgorzata Milejska-Lewandowska, Carlota Rodó, Benjamin Viaris de Lesegno, Carmela Votino, Marie-Victoire Senat, Jacques C. Jani & Alexandra Benachi (2015) Stomach position versus liver-to-thoracic volume ratio in leftsided congenital diaphragmatic hernia, The Journal of Maternal-Fetal & Neonatal Medicine, 28:2, 190-195, DOI: 10.3109/14767058.2014.906576 To link to this article: https://doi.org/10.3109/14767058.2014.906576

Accepted author version posted online: 24 Mar 2014. Published online: 25 Apr 2014.

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http://informahealthcare.com/jmf ISSN: 1476-7058 (print), 1476-4954 (electronic) J Matern Fetal Neonatal Med, 2015; 28(2): 190–195 ! 2014 Informa UK Ltd. DOI: 10.3109/14767058.2014.906576

ORIGINAL ARTICLE

Stomach position versus liver-to-thoracic volume ratio in left-sided congenital diaphragmatic hernia Anne-Gae¨l Cordier1, Mieke M. Cannie2,3, Lucie Guilbaud1, Jocelyne De Laveaucoupet4, Je´le´na Martinovic5, Dorota Nowakowska6, Malgorzata Milejska-Lewandowska7, Carlota Rodo´8, Benjamin Viaris de Lesegno9, Carmela Votino10, Marie-Victoire Senat11, Jacques C. Jani10, and Alexandra Benachi1 1

Department of Obstetrics, Gynecology and Reproductive Medicine, Centre Maladies Rares, Hernie de Coupole Diaphragmatique, Hoˆpital Antoine Be´cle`re, APHP, Universite´ Paris Sud, Paris, France, 2Department of Radiology, University Hospital Brugmann, Brussels, Belgium, 3Department of Radiology, UZ Brussel, Vrije Universiteit Brussel, Brussels, Belgium, 4Department of Radiology and 5Department of Foetopathology, Hoˆpital Antoine Be´cle`re, APHP, Universite´ Paris Sud, Paris, France, 6Department of Fetal-Maternal Medicine and Gynecology, Research Institute Polish Mother’s Memorial Hospital, Medical University of Lodz, Lodz, Poland, 7Department of Obstetrics and Gynaecology, Municipal Hospital, Ruda Slaska, Poland, 8 Department of Obstetrics, Hospital Universitari Vall d’Hebron, Universitat Autonoma de Barcelona, Barcelona, Spain, 9Department of Obstetrics, Gynecology and Reproductive Medicine, CHU de Caen-FEH, Caen Cedex, France, 10Department of Obstetrics and Gynaecology, University Hospital Brugmann, Brussels, Belgium, and 11Department of Obstetrics and Gynecology, Hoˆpital Kremlin Biceˆtre, APHP, Universite´ Paris Sud, Paris, France Abstract

Keywords

Objective: To describe a new grading method for stomach position (SP) in fetuses with left-sided congenital diaphragmatic hernia (L-CDH) using ultrasound and to correlate SP to liver position and to liver-to-thoracic cavity volume ratio (LiTR) using magnetic resonance imaging. Methods: SP were graded at the level of the 4-chamber view as following: grade 1-to-4 for stomach not visualised, visualised anteriorly at the apex of the heart, stomach showing abdominal structures anteriorly and stomach with its larger part posterior to the level of the atrial-ventricular heart valves, respectively. The LiTR was calculated and correlated to SP using the Mann–Whitney U test. Results: Seventy-four fetuses were included. Median LiTR for grade 1 SP was 0% and was not different from median LiTR for grade 2 SP (0%, p ¼ NS). Median LiTR for grade 3 SP was 14.9% and was significantly higher than for grade 2 SP (p50.001). Similarly, median LiTR for grade 4 SP was 20.7% and was significantly higher than for grade 3 SP (p50.05). When SP was grade 1 or 2, liver was intra-abdominal in 21 (84%) out of 25 fetuses while it was always intrathoracic for SP 3 or 4. Conclusion: In L-CDH, SP as described represents a simple indirect measurement of intrathoracic position and quantification of liver.

Diaphragmatic hernia, magnetic resonance imaging, stomach grading, stomach position, quantification of liver

Introduction Congenital diaphragmatic hernia (CDH) is a relatively common abnormality, with an incidence of 1 in 2500 live births [1]. In Europe, prenatal ultrasound detection rates reveal up to 60% of cases and under such conditions, the postnatal mortality rate remains high [2]. In isolated cases, postnatal mortality can vary between 15 and 50%, especially when population-based studies are considered [3–5]. Some authors have reported an apparent improvement in postnatal survival rates, probably related to the hidden mortality of the disease. However, selected centers with a high case load of CDH per year report an increase in survival rates Address for correspondence: Jacques Jani, MD, PhD, Department of Obstetrics and Gynecology, Fetal Medicine and Treatment Unit, University Hospital Brugmann, Place A. Van Gehuchten 4, 1020 Brussels, Belgium. Tel: +32 2 477 3631. Fax: + 32 2 477 2932. E-mail: [email protected]

History Received 2 January 2014 Accepted 16 March 2014 Published online 25 April 2014

that can be attributable to improvements in postnatal management [6,7]. CDH is one of the few congenital diseases that could be potentially amenable to prenatal surgery. However, the key for success in fetal intervention is the adequate selection of cases [8–10]. So far, the most extensively studied prediction method is the determination of intrathoracic liver position [11–15] and the measurement of the area of the contralateral lung as obtained in a transverse section of the fetal thorax, expressed as a ratio to the fetal head circumference (LHR) [11,16–29]. The fetal LHR is used as an indirect measurement of lung volume to predict postnatal outcome. Intrathoracic position of the liver is more easily evaluated prenatally by magnetic resonance imaging (MRI) than by prenatal ultrasound due to the difference in tissue contrast between the liver and other intrathoracic structures such as the lungs [30]. Furthermore, intrathoracic quantification of liver herniation has only been described on MRI and seems

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to be a very promising predictive marker of postnatal survival in CDH [13,31,32]. Intrathoracic liver quantification has never previously been described using prenatal ultrasound. That is probably due to the difficulty in distinguishing between liver, bowels and lungs, all with nearly the same echogenicity. In contrast, the stomach is an anechogenic structure, very easy to recognize on ultrasound. In a large number of left-sided CDH, the stomach is in an intrathoracic position and is often used as an indirect sign for a CDH diagnose. We hypothesized that in left-sided CDH, describing the stomach position in relation to the heart could be used as a simple indirect marker of intrathoracic liver position and/or liver quantification.

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a supine hypotension syndrome, with a combined six-channel phase-array body and spine coil positioned over the lower pelvic area. The MR protocol consisted of T2-weighted images. Geometric parameters of the T2-weighted images according to the machine used have been described previously [33,34]. T2-weighted imaging was obtained using a singleshot Half-Fourier turbo spin echo (HASTE) sequence in orthogonal transverse, coronal and sagittal planes according to the fetal orientation. No breath hold was requested of the patient. In each center, the radiologist adjusted the field of view and the number of sections and image orientation for each fetus as required for optimal measurement of lung volumes. Sequences that were degraded by fetal motion were repeated with the same parameters.

Materials and methods Study subjects and design This was a retrospective study conducted at the Hoˆpital Antoine Be´cle`re, Universite´ Paris Sud, Paris, France, Hoˆpital Kremlin-Bice`tre, Universite´ Paris Sud, Paris, France and the University Hospital Brugmann, Brussels, Belgium. During the study period from November 2008 to October 2012, we reviewed all fetuses with CDH assessed in the fetal medicine units of each of the participating centers. The following cases were excluded: right-sided CDH (n ¼ 27), bilateral CDH (n ¼ 5) and missing data (n ¼ 74). In total, 74 fetuses with left-sided CDH with a fetal MRI available were included. Among these 74 fetuses, 27 had prenatal fetoscopic endoluminal tracheal occlusion (FETO), 41 were expectantly managed and six underwent termination of pregnancy due to associated anomalies. The study was approved by the Local Ethics Committee and the need for written patient consent was waived. Prenatal ultrasound examination All prenatal ultrasound examinations were carried out using transabdominal sonography (RAB 4-8L probe, Voluson 730 Expert or E8; GE Medical Systems, Milwaukee, WI) by a fetal medicine specialist. Stomach position was graded on the same image sections used for the LHR measurement, thus in a transverse section of the fetal chest demonstrating the four-chamber view of the heart. We graded the stomach position as follows: grade 1 for the stomach not visualized, grade 2 for stomach visualized anteriorly at the apex of the heart, with no structures between the stomach and the apex, grade 3 for stomach showing abdominal structures anteriorly and posteriorly where the larger part was still anterior as compared to the atrial-ventricular heart valves, and grade 4 for stomach with its larger part posterior to the level of the atrial-ventricular heart valves (Figure 1). The LHR was obtained using the longest axis method. Furthermore, in every case the observed LHR was divided by the appropriate normal mean for gestational age and multiplied by 100 to derive the observed to expected (O/E) LHR and expressed as a percentage [29]. MR examination MR was performed on a clinical 1.5 T whole-body unit. Patients were positioned in a left-lateral position to prevent

MR planimetry Planimetric measurements of liver volumes were all performed by a single trained operator (MC). Liver volumes were calculated on the T2 HASTE sequences in the transverse plane using the sequences that allowed complete imaging of liver without motion-induced artifacts. The areas of the liver were determined on each section by using free-form regions of interest (ROI) on PACS (Impax, Agfa-Gevaert, Mortsel, Belgium). The measured areas were added and multiplied by the slice thickness to determine a volume. The degree of intrathoracic liver herniation was measured by volumetry, using the xyphoid process and thoracic apex as a landmark. The ratio of the intrathoracic part of the liver to the thoracic cavity volume was calculated (LiTR) as previously described (Figure 2) [32]. Statistical analysis Inter-observer (AGC and JJ) and intra-observer variability (JJ, two evaluations with at least 1 month in between) were assessed for stomach position grading on 20 randomly chosen fetuses from the series of 74 fetuses, using the Kappa statistics for multiple raters (k) [35]. Kappa statistics is the index of choice for measuring observer agreement in categorical scales. A k value that approximated 1 denoted perfect agreement while a value that approximated 0 denoted agreement no better than that by chance. Guidelines for evaluating level of agreement were: 40.80 good, 0.60–0.80 moderate/fair, 50.60 poor [36]. These empirical guidelines are more stringent than the highly contested values originally reported by Landis and Koch [35,37]. Ultrasound determined stomach grading was correlated to LiTR at MRI, using the Mann–Whitney U test. Data were expressed in medians and ranges unless mentioned otherwise. Data were analyzed with statistical softwares SPSS, version 16.0 (SPSS Inc., Chicago, IL), MedCalc software, version 7.4 (Mariakerke, Belgium) and Excel, version 9.0 (Microsoft, Redmond, WA). A two-sided p value of less than 0.05 was considered statistically significant.

Results Fetuses were evaluated with ultrasound at a median gestational age of 27.3 (range: 20.6–37.6) weeks and with MRI at 27.4 (range: 21.3–37.6) weeks. At a median, the stomach grading was 3 (range: 1–4) and the O/E LHR 29.5% (range:

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Figure 1. Ultrasound images of fetuses with left-sided diaphragmatic hernia showing (a) a grade 1 stomach position at 33 weeks of gestation, (b) a grade 2 stomach position at 24 weeks of gestation, (c) a grade 3 stomach position at 23 weeks and 6 day of gestation and (d) a grade 4 stomach position at 25 weeks and 6 days of gestation.

10.3–89.4). Stomach position was grade 1 in 12 (16.2%) patients, grade 2 in 13 (17.6%) patients, grade 3 in 32 (43.3%) patients and grade 4 in 17 (23.0%) patients. At MRI, the LiTR was equal to 0 in 18 fetuses (24.3%) out of 74. For the remaining 56 fetuses, LiTR was at a median 15.5% (0.9–42.7). Overall inter-observer agreement for the grading of the stomach position was fair with a k value ¼ 0.661 (95% C.I. 0.404–0.918) and intra-observer agreement was good with a k value ¼ 0.861 (95% C.I. 0.678–1.044). Correlation between stomach position grading and LiTR In 74 fetuses, LiTR measurements were available. Median LiTR for grade 1 stomach position was equal to 0% and was not different from median LiTR for grade 2 stomach position (0%, p ¼ NS). Median LiTR for grade 3 stomach position was equal to 14.9% and was significantly higher than for grade 2 stomach position (p50.001). Similarly, median LiTR for grade 4 stomach position was equal to 20.7% and was significantly higher than for grade 3 stomach position (p50.05; Figure 3). When stomach position was grade 1 or 2, liver was intra-abdominal in 21 (84%) out of 25 fetuses.

For the remaining four fetuses liver was moderately intrathoracic with LiTR between 0.9 and 5.0%. For fetuses with grade 3 or 4 stomach position, the liver was always intrathoracic. There was only one case with stomach position graded as 4, while the liver was minimally herniated into the thorax with LiTR equal to 5.5%. In this case, the spleen was massively herniated into the thorax (Figure 4).

Discussion The data from this study demonstrates that in left-sided CDH, stomach grading at prenatal ultrasound as proposed in this study is a simple, reproducible method that is quite reliable for indirect evaluation of intrathoracic liver position. Furthermore, stomach grading as proposed in this study represent an indirect measurement of intrathoracic liver volume quantification as performed using MRI. A previous study published by Kitano et al. [38] described a 4-level grading system for stomach position; however, it was based on the proportion of stomach herniated into the thoracic cavity rather than on the position of the stomach in comparison to the heart [38]. The authors found that based on their grading system, stomach position positively correlated with postnatal outcome. They also found that there was an

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Figure 2. (a) T2-weighted single-shot turbo spin echo magnetic resonance image of a fetus with left-sided diaphragmatic hernia at 25 weeks of gestation in a sagittal view showing the landmark at the xyphoid process (arrow) for the first plane of measurement (—) and two other planes higher in the thorax (– – –) and (). (b), (c) and (d) Same fetus in an axial view at the level of the xyphoid process (b) as well as two levels higher in the thorax (c) and (d) with delineation of the liver (—) and the thoracic cavity (– – –).

Figure 3. Box plots of liver to thoracic cavity volume ratio (LiTR) in fetuses with left-sided diaphragmatic hernia for different grade stomach position showing a positive correlation between LiTR and stomach position grading between 2 and 4. Solid line within each box corresponds to median. Upper and lower bars of boxes correspond to first and third quartiles, respectively. Two vertical lines (whiskers) outside box extend to smallest and largest observations within 1.5 times interquartile range of quartiles (interquartile range extends from third quartile to first quartile). Squares are outliers.

inverse relationship between grade of stomach position and proportion of fetuses with intrathoracic liver herniation: all fetuses with grade 0 had intra-abdominal liver, while 91% of fetuses with grade 3 had intrathoracic liver. In their multiple logistic regressions they showed that stomach position and liver position are independently predictive of

intact discharge failure. Unfortunately, they failed to include gestational age at delivery, birth-weight and gestation corrected LHR, all factors known to influence postnatal survival in CDH. Quantification of intrathoracic liver was first introduced by Walsh et al. [13] who described a single dimension method to quantify intrathoracic liver herniation. The liver/diaphragm ratio was obtained at MR imaging in a study with 43 expectantly managed and isolated CDH fetuses. The liver/ diaphragm ratio was calculated by using the distances from the superior aspect of the liver and the diaphragmatic remnant to the apex of the chest and unlike lung volumes, was predictive of postnatal outcome. In a later study by Kitano et al. [31] and in only 10 fetuses with isolated left-sided CDH and intrathoracic liver, the liver/diaphragm ratio was calculated and showed that non-survivors tended to have a larger part of the liver in the thorax, although this did not reach statistical significance probably because the study was underpowered [31]. Recently and using MRI, we described volumetric quantification of liver herniation into the thoracic cavity and showed in a series of 40 expectantly managed CDH fetuses that the liver to thoracic volume ratio of LiTR is independent of relative lung volume, predictive of postnatal survival [32]. While volumetric quantification of intrathoracic liver needs a certain expertise, the stomach is easily seen on prenatal ultrasound and the grading system as proposed in this study is reliable and represents indirect measurement of liver position and quantification in left-sided CDH. One the other hand, this marker is likely to be reliable in typical posterolateral types of hernias but less reliable for other types

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Figure 4. (a) T2-weighted single-shot turbo spin echo magnetic resonance image of a fetus with left-sided diaphragmatic hernia at 28 weeks and 3 days of gestation in (a) an axial plane showing a stomach (St) pushed posterior, classified as grade 4 on ultrasound with minimal liver herniation. Instead, there was complete herniation of the spleen (Sp) explaining the discrepancy between ultrasound grading and liver to thoracic volume ratio. (b) Same fetus in a coronal plane. H: heart; Bo: bowels.

of CDH. In fact, diaphragmatic hernias include posterolateral hernias commonly referred to as Bochdalek hernias, Morgagni and other anterior hernias, and rarely, central hernias. The posterolateral type is the most common and comprises approximately 80–90% of all CDH [39]. It is often accompanied by herniation of the stomach, intestines, liver and/or spleen into the chest cavity. It is likely that with anterior types of hernia where the liver first herniates, the configuration of different abdominal organs are changed, thus making the value of stomach position less reliable in the prediction of intrathoracic liver herniation. Our study had a limitation. We did not study if the use of this stomach grading system is predictive of postnatal survival. In fact, 41 fetuses out of the 74 included in this study were expectantly managed; however, our series is biased since expectantly managed fetuses had for the most part a good prognosis while fetuses with poor prognosis mostly underwent FETO. On the other hand, our main purpose was first to describe this new marker before undergoing predictive studies. In conclusion, in left-sided CDH stomach position as described in this study represents a simple indirect measurement of intrathoracic position and quantification of the liver. The extent to which stomach position would show to be independent of O/E LHR predictive of postnatal outcome remains to be determined in future studies.

Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of this article.

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