Review Article
Esophageal Atresia: State of the Art in Translating
Experimental Research to the Bedside
Nicholas E. Bruns1 Ian C. Glenn1 Todd A. Ponsky2
1 Department of General Surgery, Cleveland Clinic, Cleveland,
Ohio, United States
2 Division of Pediatric General and Thoracic Surgery, Cincinnati
Children’s Hospital, Cincinnati, Ohio, United States
Eur J Pediatr Surg
Abstract Long-gap esophageal atresia is one of the most challenging diseases in the field of
Keywords pediatric surgery. There is no optimal therapy, and thus many potential therapies and
► esophageal atresia techniques are being actively explored, both in animal models and in neonates. This
► tracheoesophageal article will review the available experimental treatment options with a focus on novel
fistula techniques.
► esophageal
lengthening
► esophageal
replacement
Introduction
Esophageal atresia (EA) is a congenital disorder in which the
esophagus is in discontinuity. EA and tracheoesophageal
fistula (TEF) have multiple configurations and are believed
to be a spectrum of anomalies. There are multiple classifica-
tion systems, but for the purposes of this article, descriptive
names will be used to prevent confusion. The incidence of EA
is estimated to be 3.5 in 10,000 live births.1 EA without TEF
(pure EA, gross type A) accounts for 7% of EA.2 Typically, the
upper (proximal) esophageal pouch is dilated and terminates
at the level of the azygous vein and the distal pouch is
frequently short, making primary anastomosis difficult.
There is no consensus for the definition of a long gap, but
criteria have been proposed using measurements in centi-
meters, number of vertebral bodies, or merely the inability to
perform an anastomosis.3 Surgical repair has been associated
with a leak rate of 16% and a stricture rate of 35%.4 As long-
gap EA is the most challenging subtype of EA, it represents
the subtype with the most room for improvement when
Nicholas E. Bruns's ORCID is https://orcid.org/0000-0001-9607-
0633.
received
June 20, 2019
accepted after revision
June 25, 2019
Address for correspondence Nicholas E. Bruns, MD, Department of
General Surgery, Cleveland Clinic, 9500 Euclid Avenue, Cleveland,
OH 44195-5243, United States (e-mail: nickebruns@gmail.com).
Downloaded by: Boston University. Copyrighted material.
considering current mainstream therapies. This article will
focus on discussing research avenues in regard to treatment
of pure EA.
The American Pediatric Surgery Association released
guidelines in 2019 which recommended delayed repair for
treatment of long-gap EA.3 Surgical treatment of pure EA
usually starts with laryngoscopy to assess for a proximal TEF,
gastrostomy tube placement, and delayed reconstruction.
With delay of up to several months, the gap size has been
shown to decrease.5 Numerous techniques have been de-
scribed for lengthening, anastomosing, or reconstructing the
esophagus (►Table 1). This article will discuss novel techni-
ques for dealing with long-gap EA that have been employed
in animals and/or humans, with an emphasis on techniques
that have evolved in the last 10 to 20 years. Techniques such
as bougienage, electromagnetic bougienage, myotomy,
thread-and-olive technique, and extrathoracic esophageal
elongation (EEE) will not be discussed in great detail in
this article.6–9
Animal Model
Numerous animal models have been used to study the
esophagus for the purpose of investigating novel techniques
© Georg Thieme Verlag KG DOI https://doi.org/
Stuttgart · New York 10.1055/s-0039-1693992.
ISSN 0939-7248.
Esophageal Atresia Bruns et al.

Table 1 Nonoperative and operative techniques for long-gap esophageal atresia

Technique Study population Author

Lengthening for delayed anastomosis
Botulinum toxin A injection Pig,23 human,24 rabbit15 Larsen et al,23 Ellebæk et al,24 Usui and Ono15
Bougienage Human Hays et al,20 Mahour et al,21 de Lorimier and Harrison6
Magnetic bougienage Human Hendren and Hale7,49
Traction sutures Human Foker et al,25,26 van der Zee et al28
Extrathoracic elongation Human Kimura and Soper29
Lower pouch hydrostatic distention Human Vogel et al31
Bioabsorbable spring Pig Sullins et al17
Lengthening and immediate anastomosis
Transluminal thread with olives Human Rehbein and Schweder,33 Sauer and Kurz8
Magnetic compression anastomosis Human,22,34,35 Pig10 Zaritzky et al,22,34 Ellebaek et al,35 Bruns et al10
Esophageal replacement
Colon Human German and Waterston,42 Esteves et al43
Stomach Human Heimlich and Winfield,40 Anderson and Randolph,41
Spitz,37 Spitz et al,38 Ure et al39

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Small bowel Human Ring et al,44 Bax and Van Renterghem,45
Bax and van der Zee,46 Saitua et al47
Scaffold Rat,16 pig11 Urbani et al,16 Jensen et al11

for EA. These include pig,10–14 rabbit,12,15 and rat.16 In our
experience, we found the pig to be an optimal model due to
the ease of handling, anatomic similarity to humans, and
downward facing snout to reduce aspiration risk.12 As aspi-
ration can be a major issue impacting the survival models
when facing esophageal discontinuity, there have been mul-
tiple attempts at maintaining a form of esophageal continui-
ty. These include a bifurcated esophageal model,13
esophageal bypass loop,14 and creation of a distal esophageal
pouch in parallel to a esophagogastric anastomosis.17
Mechanical Lengthening Techniques
With the exception of the bioengineered scaffolds and inter-
position grafts, all techniques rely on esophageal stretch. The
effect of stretch at the microscopic and/or molecular level is
poorly understood. When evaluated in rats, increased esoph-
ageal tension led to increased cholinergic responses in
smooth muscle as well as increased electrical response in
skeletal muscle and decreased relaxation to serotonin, indi-
cating impaired motility.18 In a separate study of esophageal
stretching in rats, histology showed thinning of the mucosa
and muscle when compared with the control.19 There was
uniform elongation and increased cell proliferation as indi-
cated by an increased Ki-67 positive ratio.
Bougienage
Preoperative bougienage has been described by several
authors.6,20,21 Proximal bougienage was described by Hays
et al and Mahour et al. De Lorimier and Harrison are credited
with the first description of both proximal and distal bou-
gienage in which over a 2- to 10-week period combined with
intraoperative circular myotomy, a successful anastomosis,
was achieved.6
Electromagnetic Bougienage
In 1975, Hendren and Hale reported the use of electromag-
netic bougienage in two infants to obtain esophageal length-
ening and delayed primary anastomosis.7 The concept of
combining this technique with magnetic compression anas-
tomosis was not performed until Zaritzky et al did so in 2009,
which will be discussed later in this article.22
Botulinum Toxin A (BoTox) Injection
It has been postulated that by inducing muscle relaxation
with intramural botulinum toxin A (BoTox) injection, esoph-
ageal tissue could significantly elongate with stretch. Larsen
et al studied the effect of on esophageal lengthening as a
potential adjunct for treatment of long-gap EA.23 Twenty-
four piglets were randomized to intramural esophageal
BoTox injection or saline injection. One hour later, the
esophagus was removed en bloc and analyzed in a stretch-
tension device. There was significantly more esophageal
elongation in the test group (84%) than in the control group
(65%).
Usui and Ono published the use of a series of intramural
esophageal BoTox injection to promote decreased tension on
rabbits.15 Twenty rabbits had a 1.5-cm cervical esophageal
resection followed by immediate esophageal anastomosis
with injection of BoTox (experimental group) or saline
(control group). Of the six rabbits in each group that

European Journal of Pediatric Surgery


Fig. 1 Traction suture technique. (Reproduced with permission from
Foker et al. 26)
survived, there was a lower rate of anastomotic stricture and
fibrosis in the BoTox group. There was no difference in wall
thickness and no muscle fracturing. The authors concluded
that BoTox may have contributed to better anastomotic
healing due to less tension.
Transmural BoTox injection has been applied to a single
child with long-gap EA with success.24 These above studies
suggest that there is need for ongoing clinical trial in humans
to elicit if these findings in animal models will pan out to
measurable outcomes in neonates.
Traction Sutures
In 1997, Foker et al described a technique of using internal
and/or external traction sutures through a thoracotomy to
obtain primary anastomosis in four patients (►Fig. 1).25 They
subsequently published a series of 63 consecutive children
with long-gap EA over a 20-year period.26 The results were
promising but have been difficult to reproduce. High-reso-
lution ultrasound was later used to compare the effects of
traction on esophageal structure in EA. By comparing 15
children who required traction to obtain primary anastomo-
sis versus eight children who did not require traction, it was
found that there was no significant difference in the thick-
Fig. 2 Thoracoscopic traction suture technique. (Reproduced with permission from van der Zee et al. 28)
Esophageal Atresia Bruns et al.
ness of the muscularis propria, mucosa, and submucosa in
both the upper and lower pouches.27
More recently, van der Zee et al applied thoracoscopy to
this technique in 10 children with successful anastomosis in
eight children in 2015.28 Specifically, the technique included
thoracoscopic mobilization of both esophageal pouches and
placement of transthoracic traction sutures on both esoph-
ageal ends (►Fig. 2). In the two failures, one patient had no
esophageal growth initially, and the traction sutures pulled
through the distal esophagus. They ultimately underwent
jejunal interposition. The other patient had two perforations
related to Replogle tube insertion and underwent gastric
pull-up. Beyond the introduction of thoracoscopy, there has
been no further revision to this technique. As indicated by
this later experience, there may be issues with controlling
tension and prevention of sutures pulling through resulting
in esophageal perforation.
Extrathoracic Esophageal Elongation
In 1994, Kimura and Soper described a single case of multi-
stage EEE.29 The procedure consisted of proximal esopha-
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gostomy and gastrostomy tube followed by serial elongations
of the esophagostomy down the chest wall until, ultimately, a
mediastinal esophago-esophageal anastomosis could be per-
formed. In the first patient, there were satisfactory results. In
the largest published series of EEE which included 15
patients, 12 were successfully completed. Of those, two
developed esophageal dysmotility and five developed gas-
troesophageal reflux.30 Since the original description, there
has been little modification to the technique.
Lower Pouch Hydrostatic Distention
Mechanical elongation of the distal pouch has been explored
as a potential area of intervention. Vogel et al in 2006
described a technique to stimulate distal pouch growth via
intermittent pressurization by means of a surgically placed
indwelling balloon catheter in a neonate (►Fig. 3).31 The
patient ultimately had a successful anastomosis and good
long-term outcome. There have been no further published
European Journal of Pediatric Surgery
Esophageal Atresia Bruns et al.
Fig. 3 Lower pouch hydrostatic distention technique for elongation
of the distal pouch. (Reproduced with permission from Vogel et al. 31)
trials with this technique. It would be valuable to compare
against a control group to elicit the efficacy of this therapy.
Spring
Bioabsorbable springs have been implemented in experi-
ments to lengthen the bowel as a potential therapy for short
bowel syndrome through the process of distraction entero-
genesis.32 Sullins et al described a technique of attaching a
biodegradable polycaprolactone spring device in the distal
pouch as a potential therapy for long-gap EA.17 In six mini-
pigs, the distal esophagus was transected 2 cm proximal to
the gastro-esophageal junction and the proximal pouch was
anastomosed to the stomach to restore continuity. The spring
Fig. 4 Bioabsorbable spring technique for elongation of the distal pouch with pre- (A) and postprocedural (B) images. (Reproduced with
permission from Sullins et al. 17)
European Journal of Pediatric Surgery
device was secured inside the distal pouch (►Fig. 4). After
4 weeks, the distal pouch length increased from 1.9 to
4.5 cm. When comparing lengthened to native esophagus,
there was no difference in thickness of muscularis mucosa or
muscularis propria, or in the number of myenteric or sub-
mucosal ganglia. Lengthened esophagus showed mild to
moderate superficial inflammation and fibrosis. Remaining
unanswered questions include the function the of the
stretched distal pouch and whether the histological findings
will have any clinical significance.
Combined Lengthening and Anastomotic Techniques
Transluminal Thread and Olive
First described by Rehbein and Schweder, this technique
used tension from a thread and olive to stretch the esophagus
together and ultimately perform pressure-induced anasto-
mosis.33 The thread was passed endoscopically (anterograde
through to oropharynx and retrograde from a gastrostomy),
which had potential as a minimally invasive technique.
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However, issues included pulling through of the device and
bronchial injury during endoscopic insertion of the thread,
and this technique has been largely abandoned.8
Magnetic Compression Anastomosis
Magnetic techniques have been proposed because the mag-
nets can achieve esophageal elongation as well as anastomo-
sis formation. A theoretical benefit of a sutureless, magnetic
compression anastomosis is that since it leaves no foreign
material, it could have an improved leak or stricture rate
compared with conventional sutured anastomosis. Other
than the need for gastrostomy tube placement, these tech-
niques can avoid the morbidity of thoracic surgery.
Zaritzky et al described 9 children, 6 with pure EA and 3
with EA with distal TEF with prior surgical ligation of the
TEF, who were treated with magnetic compression

Fig. 5 Magnetic compression anastomosis technique using catheter-based magnets (A) inserted anterograde and retrograde (B and C).
(Reproduced with permission from Zaritzky et al. 34)
anastomosis.34 Catheter-based bullet-shaped magnets with
5-mm diameter (Cook Medical, Winston-Salem, North Car-
olina, United States) were used with the proximal catheter
introduced through the oropharynx and the distal catheter
through a gastrostomy (►Fig. 5). Eight of these patients
developed strictures requiring endoscopic dilations, one of
whom required stenting and another required surgical
revision. Of the six patients with long-term follow-up,
two have gastroesophageal reflux and three have esoph-
ageal dysmotility. Ellebaek et al provided a description of a
similar technique in a 2-month-old child with pure EA who
had already undergone gastrostomy tube and waited until
the gap was 5 mm.35 Magnetic compression anastomosis
was performed with similar 5-mm cylindrical magnets
attached to catheters that were aligned under fluoroscopy.
The anastomosis was formed in 5 days. The patient devel-
oped a stricture requiring balloon dilation.
Our group described an experience using the Magnamosis
device to form an anastomosis in a live porcine esophagus.10
Esophageal Atresia Bruns et al.
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The Magnamosis device consists of two donut-shaped rings
(Harrison rings) constructed with rare earth neodymium–
iron–boron ring magnets encased in medical grade polycar-
bonate (►Fig. 6). In this study, three anastomoses were
formed in five pigs. The study served as proof of concept of
forming an esophageal anastomosis and did not use a true EA
model with a long gap, removing the potential lengthening
ability from that trial. More investigation is required to
determine the elongation ability of the device.
For magnetic techniques to advance as a more popular
therapy, a design must be developed that leads to less
stricturing than currently available devices.
Esophageal Replacement Techniques
Stomach
Gastric transposition is currently the most common tech-
nique for esophageal replacement, likely due to its technical
ease, single anastomosis, and robust vascular supply.36 Spitz
European Journal of Pediatric Surgery
Esophageal Atresia Bruns et al.
Fig. 6 Magnamosis rings with donut of tissue after completion of a
magnetic compression anastomosis.
described gastric transposition in four infants with pure EA
in 1984.37 Since, Spitz published a series of 173 children who
underwent gastric transposition, majority for EA.38 There
was a 5.2% mortality rate, a 12% anastomotic leak rate, and an
anastomotic stricture rate of 19%. Laparoscopic gastric trans-
position was subsequently described by Ure et al in a single
patient with success.39
Gastric tube was first described by Heimlich and Winfield
in 1955, and Anderson and Randolph later applied gastric
tube for EA in children.40,41 It is less popular due to the need
for a large suture line and with an increased leak and
stricture rate.36
Colon
German and Waterston published a series of 32 patients who
underwent transverse colon interposition with long-term
follow-up with positive results.42 It is a technically more
challenging procedure and requires three anastomoses. In
2010, Esteves et al described a laparoscopic-assisted ap-
proach in a series of five children.43
Fig. 7 Polyurethane scaffold seeded with autologous cells on initial esophageal replacement (A) and at 3 weeks postprocedure on endoscopy
(B) and after extrusion (C). (Reproduced from Jensen et al.11 )
European Journal of Pediatric Surgery
Small Bowel
Jejunal and ileal interposition grafts are the most technically
difficult procedures but may have the best long-term func-
tional outcomes.36 Ring et al described a series of staged
jejunal interpositions performed in 32 children in 1982.44
There were no reported failures of the graft to reach the
proximal pouch, no graft loss, and no mortalities. In 2007,
Bax et al published a series of 24 children who underwent
jejunal pedicle grafts as well as a case report of ileal pedicle
graft.45,46 Free jejunal graft has also been described47 in a
single patient.
Bioengineered Scaffolds
Tissue engineering is a novel method that may show promise
in EA management by stimulating the body’s intrinsic ability
to regenerate esophagus. Urbani et al described a layered
esophagus graft derived from acellular rat esophagus.16 By
combining a decellularized scaffold with patient-derived
cells, there is the potential to regenerate tissue defects.
The scaffold is bioengineered in a two-stage process that
recreates a muscularis externa with smooth muscle, fibro-
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blasts, and enteric nervous system followed by a multilay-
ered mucosa derived from epithelial precursors. The result is
a structurally organized and vascularized esophageal substi-
tute which may be an alternative to esophageal replacement
grafts.
Jensen et al developed a graft from a polyurethane scaffold
that was seeded with autologous cells.11 Porcine esophageal
epithelial cells or porcine amniotic fluid was cultured on the
graft in a bioreactor and then implanted in piglets as a 5-cm
esophageal interposition graft (►Fig. 7). By 21 days, the
scaffolds were extruded and demonstrated regeneration of
a complete tube. By 6 months, the tissue appeared as
complete epithelium. Grafts seeded with either cell type
demonstrated epithelial and muscle regeneration, and the
pigs were ultimately able to eat with the bioengineered
segment of esophagus. Application in neonates appears to
be the next step.
What Is on the Horizon?
There are several unanswered questions in the current under-
standing of EA and its existing therapies. The role of molecular
mechanisms is largely unknown when it comes to mechanical
lengthening.48 Furthermore, it is unclear whether mechanical

lengthening leads to new growth rather than stretch alone, and
how this potentially impacts inflammation, stricture forma-
tion, and motility. Finally, as tissue engineering is coming
closer to reality in neonates, questions regarding muscle
formation and function need to be addressed.
Conclusion
In the last decade, strides have been made in the develop-
ment of novel techniques for long-gap EA. BoTox injection
may prove to be a useful adjunct during anastomosis once
adequately studied in neonates. Magnetic compression anas-
tomosis has the potential to be a minimally invasive tech-
nique for long-gap EA if the current devices can be revised to
improve stricture rates. Among therapies untested in
humans, bioengineered scaffolds show the most promise,
although there is still the question of muscle formation and
function.
Conflict of Interest
Dr. Ponsky is the owner of Globalcast MD and consultant
for Conmed, outside the submitted work.
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