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. Author manuscript; available in PMC: 2024 Feb 22.
Published in final edited form as: Neonatology. 2023 Feb 22;120(2):185–195. doi: 10.1159/000526794

MRI based evaluation of anatomy and outcomes prediction in infants with esophageal atresia

Kaitlyn T Marks 1, Nara S Higano 2,3,4, Meera Kotagal 5, Jason C Woods 2,3,4,6, Paul S Kingma 1,2,6
PMCID: PMC10118939  NIHMSID: NIHMS1868079  PMID: 36812903

Abstract

Introduction:

There is currently no validated diagnostic modality to characterize the anatomy and predict outcomes of tracheal esophageal defects, such as esophageal atresia (EA) and tracheal esophageal fistulas (TEF). We hypothesized that ultra-short echo-time MRI would provide enhanced anatomic information allowing for evaluation of specific EA/TEF anatomy and identification of risk factors that predict outcome in infants with EA/TEF

Methods:

In this observational study, 11 infants had pre-repair ultra-short echo-time MRI of the chest completed. Esophageal size was measured at the widest point distal to the epiglottis and proximal to the carina. Angle of tracheal deviation was measured by identifying the initial point of deviation and the farthest lateral point proximal to the carina.

Results:

Infants without a proximal TEF had a larger proximal esophageal diameter (13.5±5.1mm vs. 6.8±2.1mm, p=0.07) when compared to infants with a proximal TEF. The angle of tracheal deviation in infants without a proximal TEF was larger than infants with a proximal TEF (16.1±6.1° vs. 8.2±5.4°, p=0.09) and controls (16.1±6.1° vs. 8.0±3.1°, p=0.005). An increase in the angle of tracheal deviation was positively correlated with duration of post-operative mechanical ventilation (Pearson r=0.83, p<0.002) and total duration of post-operative respiratory support (Pearson r=0.80, p=0.004).

Discussion/Conclusion:

These results demonstrates that infants without a proximal TEF have a larger proximal esophagus and a greater angle of tracheal deviation which is directly correlated with the need for longer post-operative respiratory support. Additionally, these results demonstrate that MRI is a useful tool to assess the anatomy of EA/TEF.

Keywords: Esophageal atresia, tracheal esophageal fistula, magnetic resonance imaging, tracheomalacia

Introduction

Tracheal esophageal defects (TEDs) occur in 1 in 2,500–4,500 live births. Esophageal atresia (EA) and tracheal esophageal fistulas (TEF) occur when there is partial or complete disruption in the continuity of the esophagus with or without a connection to the trachea. There are six anatomic classifications of EA/TEF: Types A is an isolated EA without the presence of a TEF, Type B is an EA with a proximal TEF, Type C is an EA with a distal TEF, Type D is an EA with both proximal and distal TEFs, Type E or H-Type is an isolated TEF and Type F is congenital esophageal stenosis without an atresia or a fistula (Figure 1a) [1, 2].

Figure 1.

Figure 1.

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Anatomy of Esophageal atresia/tracheal esophageal fistula. (a) Illustration of the Gross Classification of the different anatomic subtypes of EA/TEF. UTE MR images were segmented using two different software programs, (a) AMIRA and (b) ITK-SNAP, to generate 3D reconstructions of the infants’ airway and esophagus. Segmentations were then used to measure (c) proximal esophageal size and angle of tracheal deviation.

Despite many advances in the care of patients with EA/TEFs, there is currently no validated diagnostic modality to characterize the specific anatomy prior to surgical repair [3]. Currently, the only diagnostic imaging routinely obtained is a chest x-ray showing a coiled nasogastric tube in the proximal esophageal pouch [1]. This information suggests the presence of a TED but provides very limited information regarding the specific anatomy of an EA/TEF, its effect on the infants’ airway, and the gap length between the proximal and distal esophageal pouches. These anatomic details significantly impact the clinical course of infants with TEDs [4–9].

EA/TEF’s are associated with high rates of both short-term and long-term morbidity including but not limited to anastomotic strictures requiring frequent endoscopic dilations, dysphagia, tracheomalacia, aspiration pneumonia, chronic cough, and anastomotic leaks leading to increased risk of sepsis, mediastinitis and pneumothorax [4–8]. The estimation of the esophageal gap length by a fluoroscopic gap study or intra-operative vertebral body measurements is currently the best predictor of outcome in patients with EA/TEF but it is invasive and does not always correlate to the clinical course [10, 11]. A few studies have evaluated the use of pre-operative computerized tomography scanning in cases of suspected EA/TEFs. While these studies have demonstrated success in identifying the anatomy of the TED and defining the esophageal gap length, they have also shown that computerized tomography scans expose infants to a significant amount of ionizing radiation indicating that the risks may outweigh the benefits [12–15].

Multiple studies have demonstrated that magnetic resonance imaging (MRI) provides useful information for pre-surgical planning in infants with congenital heart disease without radiation exposure [16–18]. The Neonatal Intensive Care Unit (NICU) at Cincinnati Children’s Hospital Medical Center is equipped with an innovative, small footprint 1.5T MRI system which allows for convenient and controlled imaging of critically ill infants without the risks associated with transporting them off the unit. Preliminary studies done using this novel MRI scanner have demonstrated that MRI could be a useful tool for evaluation of non-cardiac neonatal pathology and congenital anomalies including TEDs [19–23]. Additionally, the use of an ultra-short echo-time (UTE) MRI protocol allows infants to be free breathing and non-sedated while capturing images that provide sufficient evaluation of structures within the thoracic cavity secondary to reduced sensitivity to cardiac and respiratory motion as well as an increased signal to noise ratio [24].

We, therefore, hypothesized that UTE MRI would provide enhanced anatomic information allowing for identification of the specific EA/TEF anatomy, determination of the size of the proximal esophagus and the resulting effect on airway anatomy in infants with TEDs.

Methods

Study population

In this prospective observational cohort study, the study population included all patients with a known TED admitted to the NICU at Cincinnati Children’s Hospital Medical Center from January 1, 2016 to January 31, 2019. A total of 39 patients with TEDs were eligible for our study. Of those, 13 consented for participation and all 13 infants were evaluated by MRI. Eight patients in the NICU at Cincinnati Children’s Hospital Medical Center with no known clinical airway or esophageal pathology who were born at greater than 34 weeks gestational age were enrolled to serve as the control group for our TED population (Table 1). The study was approved by the Cincinnati Children’s Hospital Medical Center Institutional Review Board (IRB2018–8330c) and informed written consent was obtained from all participants. Per the approved IRB protocol, the clinical team was informed of the results of the MRI if there was an incidental finding that would impact clinical care such as the presence of an abdominal mass; otherwise, the results of the study portion of the MRI were not available to the clinical team.

Table 1.

Demographic comparison of study participants (n=22).

Variable EA/TEF Infants (N = 14) Control Infants (N = 8)
Gender
 Male 8 (57.1%) 2 (25%)
 Female 6 (42.9%) 6 (75%)
Gestational Age (weeks) 37.9 ± 2.4 36.2 ± 1.6 p = 0.1
Birth weight (grams) 2754 ± 765 2602 ± 303 p = 0.6
TED Subtype
 EA/TEF Type A 3 (21.5%)
 EA/TEF Type B 1 (7.1%)
 EA/TEF Type C 7 (50%)
 EA/TEF Type D 0 (0%)
 EA/TEF Type E 2 (14.3%)
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Image acquisition

All magnetic resonance (MR) images were acquired in a novel, small footprint 1.5T MRI scanner (GE Healthcare, Waukesha, WI) optimized for neonatal imaging located within the NICU at Cincinnati Children’s Hospital Medical Center. Study participants were not sedated for image acquisition and all images were obtained while participants were free breathing.

The UTE MR images of the chest were segmented to generate 3D reconstructions of the infants’ airway and esophagus by a single operator using MIRA (Thermo Fischer Scientific) and ITK-SNAP (Figure 1b–d)[25]. Esophageal diameter was measured at the widest point distal to the epiglottis and proximal to the carina. Esophageal cross-sectional area was measured at the widest point distal to the epiglottis and proximal to the carina. Additionally, the angle of tracheal deviation from midline was measured by identifying the initial point of deviation and the farthest lateral point proximal to the carina using the AMIRA segmentations (Figure 1d).

The size of the proximal esophagus was compared to the anatomic classification of the EA/TEF as defined intra-operatively, the diagnosis of esophageal dysmotility as identified on a video swallow study or esophageal contrast study, the development of an anastomotic stricture, and the need for esophageal dilations during the first year of life. The angle of tracheal deviation from midline was compared to the total duration of post-operative respiratory support, duration of post-operative mechanical ventilation, highest peak inspiratory pressure, duration of postoperative non-invasive ventilation, and duration of post-operative supplemental oxygen.

Statistical analysis

The continuous variables (i.e. the size of the proximal esophagus, and the angle of tracheal deviation) were confirmed to be normally distributed, summarized as means, and compared using a Student t test. For evaluations using multiple measurements (i.e. total post-operative ventilator days versus angle of tracheal deviation), a Pearson correlation coefficient was calculated with a corresponding p value. All statistical calculations were performed using Microsoft Excel. A p value of 0.05 was considered statistically significant.

Results

A total of 13 enrolled infants were enrolled in the study, eight infants had pre-repair UTE MRI of the chest completed. Three infants had both pre-repair and post-repair UTE MRI of the chest completed. Two infants had only post-repair UTE MRI of the chest completed and therefore were excluded from the study due to lack of necessary information needed to make appropriate comparisons.

Size of the proximal esophagus

To determine if proximal esophageal size was influenced by the presence of a proximal TEF, esophageal size was examined relative to the presence or absence of a proximal TEF. Infants without a proximal TEF (Gross types A&C, n = 8) had a trend towards a larger proximal esophageal diameter when compared to infants with a proximal TEF (Gross types B&E, n = 3, 13.5±5.1mm vs. 6.8±2.1mm, p = 0.07). Proximal esophageal area in infants without a proximal TEF was larger when compared to infants with a proximal TEF but again this difference did not reach statistical significance (103.2±62.3mm2 vs. 19.4±8.7mm2, p = 0.06). Esophageal diameter was significantly larger in infants with a proximal TEF (6.8±2.1mm vs. 3.4±2.1mm, p = 0.05) and infants without a proximal TEF (13.5±5.1mm vs. 3.4±2.1mm, p < 0.001) when either group was independently compared to controls (Figure 2a). Additionally, esophageal area was significantly larger in infants without a proximal TEF when compared to controls (103.2±62.3mm2 vs. 8.9±6.4mm2, p < 0.001) but there was no statistically significant difference when comparing proximal esophageal area in infants with a proximal TEF to controls (19.4±8.7mm2 vs. 8.9±6.4mm2, p = 0.06) (Figure 2b).

Figure 2:

Figure 2:

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The absence of a proximal TEF is associated with a larger proximal esophagus. To determine if proximal esophageal size was influenced by the presence of a proximal TEF, esophageal size was examined relative to the presence or absence of a proximal TEF. Infants without a proximal TEF included those with Gross Types A&C (n=8). Infants with a proximal TEF included those with Gross Types B&E (n=3). Infants without tracheal or esophageal pathology served as controls. (a) Infants without a proximal TEF had a larger proximal esophageal diameter when compared to infants with a proximal TEF (p=0.07). Controls had a significantly smaller esophageal diameter compared to infants with a proximal TEF and infants without a proximal TEF (p<0.05). Error bars represent standard error of the mean. (b) Proximal esophageal area in infants without a proximal TEF was larger when compared to infants with a proximal TEF (p=0.06). Esophageal area was significantly larger in infants without a proximal TEF when compared to controls (p=0.001) but there was no statistically significant difference when comparing proximal esophageal area in infants with a proximal TEF to controls (p=0.06). Error bars represent standard error of the mean.

Common esophageal complications

To assess the association of proximal esophageal size with common esophageal complications seen in patients with EA/TEFs. Proximal esophageal diameter (p = 0.06, Figure 3a) and area (p = 0.11, Figure 3b) were larger in infants who developed esophageal dysmotility when compared to those who did not, but this difference did not reach statistical significance. Proximal esophageal size was also compared to the presence of an anastomotic stricture (p = 0.5) and the number of esophageal dilations required in the first year of life (Pearson r = 0.05, p = 0.96) but there was no statistically significant difference.

Figure 3.

Figure 3.

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A larger proximal esophagus is associated with the development of esophageal dysmotility. To assess the impact of proximal esophageal size on common esophageal complications seen in patients with EA/TEF, proximal esophageal size was compared to the presence of esophageal dysmotility. Proximal esophageal area (p=0.11) and diameter (p=0.06) were larger in infants who had esophageal dysmotility when compared to those who did not, but this difference did not reach statistical significance. Error bars represent standard error of the mean.

Angle of tracheal deviation

To determine if the anatomic classification of the EA/TEF was associated with the anatomy of the infant’s airway, the angle of tracheal deviation from midline was evaluated based on the intraoperative definition of the EA/TEF anatomy. Comparison showed that the angle of tracheal deviation was greater in infants without a proximal TEF when compared to infants with a proximal TEF (16.1±6.1° vs. 8.2±5.4°, p = 0.09) and controls (16.1±6.1° vs. 8.0±3.1°, p = 0.005) (Figure 4).

Figure 4.

Figure 4.

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The absence of a proximal TEF is associated with a larger angle of tracheal deviation from midline. To evaluate the impact of EA/TEF subtype on airway anatomy, the angle of tracheal deviation from midline was evaluated based on the intraoperative definition of EA/TEF anatomy. The angle of tracheal deviation was larger in infants without a proximal TEF when compared to infants with a proximal TEF (p=0.09) and controls (p<0.005). Error bars represent standard error of the mean.

Post-operative respiratory support

To investigate if the angle of tracheal deviation from midline was associated with the post-operative respiratory course of infants with TEDs, the angle of tracheal deviation was compared to the duration and level of post-operative respiratory support. A greater angle of tracheal deviation was positively correlated with both a longer duration of total post-operative respiratory support (Pearson r = 0.80, p = 0.004, Figure 5a) as well as longer duration of post-operative mechanical ventilation (Pearson r = 0.83, p = 0.002, Figure 5b). Additionally, a greater angle of tracheal deviation was associated with a need for higher peak inspiratory pressures (Pearson r = 0.55, p = 0.10, Figure 5c) while mechanically ventilated but this association did not reach statistical significance.

Figure 5.

Figure 5.

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A greater angle of tracheal deviation is associated with greater post-operative respiratory support. To determine if the angle of tracheal deviation from midline impacted the post-operative respiratory course of infants with TEDs, the angle of tracheal deviation was compared to duration of post-operative respiratory support. (a) A greater angle of tracheal deviation was positively correlated with duration of total post-operative respiratory support (Pearson r=0.80, p=0.004). (b) A greater angle of tracheal deviation was positively correlated with duration of post-operative mechanical ventilation (Pearson r=0.83, p=0.002). (c) A greater angle of tracheal deviation was associated with a higher peak inspiratory pressures (Pearson r=0.55, p=0.10) but this association did not reach statistical significance.

To determine if there were significant differences in the relationship between tracheal deviation and post-operative respiratory in infants with different anatomic subtypes of TEDs the study participants were subcategorized by those without a proximal TEF (types A, B) and those with a proximal TEF (Type C). As seen in Figure 6, the correlation between tracheal deviation and both duration of post-operative mechanical ventilation (Pearson r = 0.89, p = 0.05 vs. Pearson r = 0.83, p = 0.04) and total duration of post-operative respiratory support (Pearson r = 0.93, p = 0.02 vs. Pearson r = 0.84, p = 0.03) was quite similar when comparing infants to those without a proximal TEF and those with a proximal TEF.

Figure 6.

Figure 6.

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Tracheal deviation is an important determinant of post-operative respiratory status independent of specific anatomy. Infants without a proximal TEF included those with Gross Types A&C (n=8). Infants with a proximal TEF included those with Gross Types B&E (n=3). (a) The correlation between tracheal deviation and duration of post-operative mechanical ventilation was similar when comparing infants to those without a proximal TEF (Pearson r = 0.89, p = 0.05) and those with a proximal TEF (Pearson r = 0.83, p = 0.04). (b) The correlation between tracheal deviation and total duration of post-operative respiratory support was similar when comparing infants to those without a proximal TEF (Pearson r = 0.93, p = 0.02) and those with a proximal TEF (Pearson r = 0.84, p = 0.03).

To assess if other clinical factors influenced post-operative respiratory course of study participants, the level of post-operative respiratory support was compared to key surgical and clinical variables. All of the patients in this study had open repairs. 55% had a delayed repair defined as the first operation occurring at greater than 5 days of life. 73% achieved esophageal continuity with one surgical repair attempt. There was no significant difference in the duration of post-operative mechanical ventilation (10.8±13.7 days vs. 5.6±5.2 days, p = 0.44) or the total duration of post-operative respiratory support (19.7±19.1 days vs. 15.4±11.6 days, p = 0.43) in infants with delayed repair vs. those without a delayed repair. No infants had a major cardiac defect, while six of the eleven study participants had minor findings on echocardiography which included small atrial septal defects, small ventricular septal defects, mild pulmonic stenosis, a bicuspid aortic valve, a right aortic arch and an aberrant left subclavian. There was no significant difference in the duration of post-operative mechanical ventilation (8.7±13.6 days vs. 8.2±7.1 days, p = 0.95) or duration of total post operative respiratory (13.5±18.5 days vs. 22.8±10.8 days, p = 0.35) in infants with mild cardiac disease vs. those without cardiac disease.

Discussion

TEDs, specifically EA/TEFs, are associated with high rates of morbidity thought to be due to the primary congenital anomaly as well as the sequelae that follow surgical repair [4–8]. Despite many advances in the care of patients with EA/TEFs, there is currently no validated diagnostic modality to characterize the anatomy of the defect prior to surgical repair. Greater pre-operative information on EA/TEF anatomy would improve our understanding of the primary drivers of long-term morbidity in patients with EA/TEF and allow improved counseling of families regarding the risk for short- and long-term complications [1, 3]. This study demonstrates that UTE MRI is a useful tool to assess the anatomy of TEDs prior to surgical repair. Furthermore, this study presents objective evidence demonstrating the importance of characterizing the proximal esophageal pouch prior to surgical repair due its impact on dysmotility, tracheal deviation and the post-operative respiratory course in these infants.

Infants without a proximal TEF appear to have a larger proximal esophagus when compared to those with a proximal TEF. This finding suggests that the anatomic subtype of the EA/TEF, specifically the presence or absence of a proximal TEF, plays a crucial role in the size of the proximal esophagus and thus the long-term morbidity seen in these infants. We have two possible explanations that support this observation. First, the absence of a proximal TEF in the setting of an esophageal atresia is likely associated with a greater proximal esophageal size due to the absence of a drainage of accumulated amniotic fluid in the proximal pouch causing constant stretch and ultimately long-standing dilation (which may affect motility even post-repair). Second, it is also possible that the larger proximal esophageal size seen in infants without a proximal TEF develops secondary to underlying dysmotility and the lack of necessary peristalsis to clear the anatomic fluid proximally in utero.

The potential association of dysmotility with a dilated proximal pouch is supported by a large body of literature that demonstrates a high prevalence of dysphagia seen in patients with a repaired EA/TEF [26, 4, 5, 27, 6–8, 28]. Our work adds to this body of literature by objectively demonstrating a link between the anatomic subtype of EA/TEF and the presence of dysmotility. We demonstrate that EA/TEF infants both with and without a proximal TEF have a larger proximal esophageal size when compared to controls suggesting that all infants with EA/TEF have some degree of dysmotility. This dysmotility appears, however, to be greater in those infants without a proximal TEF based on direct but non-significant association between the degree of proximal esophageal size and the presence of esophageal dysmotility as identified on post-natal imaging. We do, however, recognize that the use of post-operative esophageal contrast and video swallow studies to identify the presence of dysmotility is imprecise.

Additionally, our work demonstrates that the presence or absence of a proximal TEF is associated with the degree tracheal deviation which appears to be a critical driver of the post-operative respiratory course seen in these infants. We believe that the presence of a dilated proximal esophageal pouch in infants without a proximal TEF functions as a space occupying lesion during development which alters the course of the trachea. As demonstrated in Figure 5, the degree of tracheal deviation from midline is strongly correlated to the duration of post-operative respiratory support and duration of mechanical ventilation. The ability to have this information pre-repair to guide timing of post-operative extubating and counsel families on the expected post-operative course would be invaluable. Furthermore, the similar correlations seen in our subgroup analysis of tracheal deviation in infants without a proximal TEF degree and those with proximal TEF suggest that the degree of proximal esophageal dilation might influence the post-operative course of these infants more than the specific anatomy of the TED. It would be beneficial to compare the angle of tracheal deviation as measured on pre-operative UTE MRI with that on post-operative UTE MRI to assess if this tracheal deviation is transient or long-standing. Additionally, it would be informative to follow a cohort of infants with EA/TEF into childhood to assess if the degree of tracheal deviation has a long-standing impact on respiratory function such as a predisposition to lower respiratory tract infections, aspiration pneumonia, chronic cough, and clinically significant tracheomalacia which are all long-term complications seen in patients with EA/TEFs [4–8].

The primary limitation of this study is that UTE MRI was performed on 11 of 39 eligible infants, limiting the statistical power of this study due to the small number of infants and introducing the possibility of selection bias. Despite the small sample size, many of our variables demonstrated a robust statistically significant result. In future studies, it would be ideal to standardize the time at which these infants underwent imaging to ensure that all infants have pre-repair imaging captured. Including infants with TEDs managed at multiple institutions would greatly increase the statistical power of this study, but the availability of NICU MRI may limit the application of our results at other institutions.

Conclusion:

In summary, this study suggests that the error that occurs in early tracheal/esophageal development resulting in a specific anatomy of the EA/TEF is crucial in determining the clinical course of these infants. Our work suggests that infants without a proximal TEF have a larger proximal esophagus and demonstrates the importance of the size of the proximal esophagus and resulting angle of tracheal deviation in the outcome of these patients. Additionally, these results demonstrate that UTE MRI is a useful tool to assess the anatomy of TEDs.

Funding sources:

NIH/NICHD P01 HD093363. The sponsor was not involved in the preparation of the data or manuscript

Abbreviations:

TED

tracheal esophageal defects

EA

esophageal atresia

TEF

tracheal esophageal fistula

MRI

magnetic resonance imaging

UTE

ultra-short echo-time

NICU

neonatal intensive care unit

Footnotes

Statement of Ethics

The research in this study complied with the guidelines for human studies and was conducted ethically in accordance with the World Medical Association Declaration of Helsinki. The study protocol was reviewed and approved by Cincinnati Children’s Hospital Medical Center Institutional Review Board, approval IRB 2018–8330C. All subjects (or their parent or legal guardian) gave written informed consent to participate in the study.

Conflict of interest disclosure: The authors have no conflicts of interest or disclosures to report. Kaitlyn Marks wrote the first draft of the manuscript. No honorariums or payments were given for preparation of the manuscript.

Data Availability Statement

All data generated or analysed during this study are included in this article. Further enquiries can be directed to the corresponding author.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

All data generated or analysed during this study are included in this article. Further enquiries can be directed to the corresponding author.

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