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Contributors
M. Asunción Acosta Unidad de Cirugia Esofago-gàstrica, Hospital Universitario de Gran
Canaria “Dr. Negrìn”, Las Palmas, Gran Canaria, Spain
María Elia Pérez Aguirre Department of Surgery, Hospital Clínico San Carlos, Madrid,
Spain
Isaías Alarcón Unit of Innovation in Minimally Invasive Surgery, University Hospital Virgen
del Rocío, University of Sevilla, Sevilla, Spain
Sonia Fernandez Ananin Gastrointestinal Surgical Unit, Department of Surgery, Hospital
Sant Pau, Autonomous University of Barcelona, Barcelona, Spain
Luca Arru Department of General and Minimally Invasive Surgery, CHL, Luxembourg City,
Luxembourg
Juan Santiago Azagra Department of General and Minimally Invasive Surgery(Laparoscopy
& Robotic), Centre Hospitalier de Luxembourg (CHL), L-1210 Luxembourg, Luxembourg
Barbara A. J. Bastiaansen Department of Gastroenterology and Hepatology, Amsterdam
University Medical Center, University of Amsterdam, Amsterdam, The Netherlands
Felix Berlth Department of Surgery, Division of Gastrointestinal Surgery, Seoul National
University Hospital, Seoul, Korea;
Department of General, Visceral and Cancer Surgery, University Hospital of Cologne, Cologne,
Germany
Paulo A. Bertulucci Department of Upper GI Surgery, Americas Medical City Hospital, Rio
de Janeiro, Brazil
Ronald L. A. W. Bleys Department of Anatomy, University Medical Center Utrecht, Utrecht,
The Netherlands
Roel Bolckmans Virginia Commonwealth University Hospitals, Richmond, VA, USA
Ivo A. M. J. Broeders Meander Medisch Centrum, Amersfoort and University of Twente,
Enschede, The Netherlands
Marcos Bruna Department of Surgery, Hospital Universitario y Politécnico La Fé, Valencia,
Spain
Benjamin Cadiere Department of Gastrointestinal Surgery, European School of Laparoscopic
Surgery, Saint-Pierre University Hospital, Université Libre de Bruxelles, Brussels, Belgium
Guy-Bernard Cadiere Service de Chirurgie Digestive, UMC Saint-Pierre, Bruxelles,
Belgium
Miguel A. Cuesta Department of Surgery. Amsterdam UMC, Amsterdam, The Netherlands
Hiroyuki Daiko Department of Esophageal Surgery, National Cancer Center Hospital,
Tokyo, Japan
xiii
xiv Contributors
Bernard Dallemagne L’Hopital and IRCAD, Strasbourg, France
Antonio Talvane Torres de Oliveira Department of Upper GI Surgery, Americas Medical
City Hospital, Rio de Janeiro, Brazil
Ismael Diez del Val Department of Surgery, Hospital Universitario Basurto, Bilbao, Spain
Paul Fockens Department of Gastroenterology and Hepatology, Amsterdam University
Medical Center, University of Amsterdam, Amsterdam, The Netherlands
Hitoshi Fujiwara Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural
University of Medicine (KPUM), Kyoto, Japan
Michel Gagner Department of Surgery, Hopital du Sacre Coeur, Montreal, QC, Canada
Suzanne S. Gisbertz Department of Surgery, Amsterdam University Medical Center,
Amsterdam, The Netherlands
Martine Goergen Department of General and Minimally Invasive Surgery (Laparoscopy &
Robotic), Centre Hospitalier de Luxembourg (CHL), L-1210 Luxembourg, Luxembourg
Won Ho Han Department of Cancer Control and Population Health, National Cancer Center
Graduate School of Cancer Science and Policy & Center for Gastric Cancer, National Cancer
Center, Ilsandonggu, Goyang, Republic of Korea
Jacques Himpens CHIREC Delta Hospital, Brussels, Belgium
Woo Jin Hyung Department of Surgery, Yonsei University College of Medicine, Seoul,
Republic of Korea
Francisco Javier Ibañez Department of General and Minimally Invasive Surgery
(Laparoscopy & Robotic), Centre Hospitalier de Luxembourg (CHL), L-1210 Luxembourg,
Luxembourg
Noriyuki Inaki Department of Digestive and General Surgery, Juntendo University Urayasu
Hospital, Urayasu, Japan
Aida Pérez Jiménez Department of Surgery, Hospital Universitario Puerta del Sur, Móstoles,
Madrid, Spain
Young-Woo Kim Department of Cancer Control and Population Health, National Cancer
Center Graduate School of Cancer Science and Policy & Center for Gastric Cancer, National
Cancer Center, Ilsandonggu, Goyang, Republic of Korea
Takahiro Kinoshita Gastric Surgery Division, National Cancer Center Hospital East,
Kashiwa, Japan
Bastiaan Klarenbeek Department of Surgery, Radboudumc Hospital, Nijmegen, The
Netherlands
Hirotaka Konishi Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural
University of Medicine (KPUM), Kyoto, Japan
Kenji Kudou Department of Surgery, Institute of Gastroenterology, Tokyo Women’s Medical
University, Sinjuku-ku, Japan
In Gyu Kwon Department of Surgery, Gangnam Severance Hospital, Yonsei University
College of Medicine, Seoul, Republic of Korea
Croider Franco Lacerda Department of Upper GI Surgery, Americas Medical City Hospital,
Rio de Janeiro, Brazil
Francisco Lopez Bernal Unit of Innovation in Minimally Invasive Surgery, University
Hospital Virgen del Rocío, University of Sevilla, Sevilla, Spain
Carlos Loureiro González Department of Surgery, Hospital Universitario Basurto, Bilbao,
Spain
xvContributors
Misha Luyer Gastro-Intestinal and Oncological Surgery, Catharina Hospital, Eindhoven, The
Netherlands
Silviu T. Makkai-Popa Department of General and Minimally Invasive Surgery, CHL,
Luxembourg City, Luxembourg
J. Caetano Marchesini Department of Endoscopy, Medical School of Mario Covas Hospital
and Bariatric Surgery of Sirio Libanés Hospital, Sao Paulo, Brazil
Fernando Mingol Navarro Department of Surgery, Esophageal Surgery Unit, Hospital
Universitario y Politécnico La Fé, Valencia, Spain
Salvador Morales-Conde Unit of Innovation in Minimally Invasive Surgery, University
Hospital Virgen del Rocío, University of Sevilla, Sevilla, Spain
Carlos Moreno-Sanz Department of General and Digestive Surgery, Hospital General La
Mancha Centro, Alcazar de San Juan, Ciudad Real, Spain
Kousuke Narumiya Department of Surgery, Institute of Gastroenterology, Tokyo Women’s
Medical University, Sinjuku-ku, Japan
Salvador Navarro Soto Department of Surgery, Parc Taulí, Sabadell, Barcelona, Spain
Grard Nieuwenhuijzen Gastro-Intestinal and Oncological Surgery, Catharina Hospital,
Eindhoven, The Netherlands
Harushi Osugi Department of Surgery, Institute of Gastroenterology, Tokyo Women’s
Medical University, Sinjuku-ku, Japan
Eigo Otsuji Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural
University of Medicine (KPUM), Kyoto, Japan
Beniamino Pascotto Department of General and Minimally Invasive Surgery(Laparoscopy
& Robotic), Centre Hospitalier de Luxembourg (CHL), L-1210 Luxembourg, Luxembourg
Jaime Ponce CHI Memorial Hospital, Chattanooga, TN, USA
Carmen Balague Ponz Gastrointestinal Surgical Unit, Department of Surgery, Hospital Sant
Pau, Autonomous University of Barcelona, Barcelona, Spain
José A. Ramírez Clinica San Roque, Las Palmas de Gran Canaria, Gran Canaria, Spain
Rishindra M. Reddy Department of Surgery, Section of Thoracic Surgery, University of
Michigan, Ann Arbor, MI, USA
Camiel Rosman Department of Surgery, Radboudumc Hospital, Nijmegen, The Netherlands
Jelle P. Ruurda Department of Surgical Oncology, University Medical Center Utrecht,
Utrecht, The Netherlands
Andrés Sánchez-Pernaute Department of Surgery, Hospital Clínico San Carlos, Madrid,
Spain
Atsushi Shiozaki Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural
University of Medicine (KPUM), Kyoto, Japan
André J. P. M. Smout Department of Gastroenterology and Hepatology, Amsterdam
University Medical Center, University of Amsterdam, Amsterdam, The Netherlands
Eduardo M. Targarona Gastrointestinal Surgical Unit, Department of Surgery, Hospital
Sant Pau, Autonomous University of Barcelona, Barcelona, Spain
Mark I. van Berge Henegouwen Department of Surgery, Amsterdam University Medical
Center, Amsterdam, The Netherlands
xvi Contributors
Donald. L. van der Peet Department of Surgery, Amsterdam UMC, Amsterdam, The
Netherlands
Pieter C. van der Sluis Department of Surgical Oncology, University Medical Center Utrecht,
Utrecht, The Netherlands
Richard van Hillegersberg Department of Surgical Oncology, University Medical Center
Utrecht, Utrecht, The Netherlands
Teus J. Weijs Department of Anatomy, University Medical Center Utrecht, Utrecht, The
Netherlands
Bas L. A. M. Weusten Department of Gastroenterology and Hepatology, St. Antonius
Hospital, Nieuwegein, The Netherlands
Han-Kwang Yang Department of Surgery, Division of Gastrointestinal Surgery, Seoul
National University Hospital, Seoul, Republic of Korea
Natan Zundel Department of Surgery, FIU Herbert Wertheim College of Medicine, Jackson
North Medical Center, Miami, FL, USA
Surgical Anatomy of the Esophagus
Teus J. Weijs and Ronald L. A. W. Bleys
1
1.1 Introduction
Many regard the esophagus as merely a “food pipe”
through which food traverses the gap between the pharynx
and the stomach [1]. However surgeons regard it as an elusive organ; situated central in the body it traverses neck,
thorax, and abdomen, surrounded by many vital structures
in near proximity. This chapter maps the highlights of the
surgical anatomy of the esophagus, from its composition,
attachments, topography, blood supply, and lymphatics to
relevant structures lying nearby.
1.2 Composition
The wall of the esophagus is formed by an inner layer of
mucosa, surrounded by layers of submucosa, muscularis,
and finally adventitia.
The esophageal mucosa is composed of squamous cell
epithelium. Its transition into the columnar epithelium of
the stomach can be visualized as a zig-zag line; the z-line.
The muscularis consists of an outer layer of longitudinally oriented muscle fibers and an inner layer of circularly
oriented muscle fibers. This is opposite to the pharynx,
where the circular muscle fibers form the outer layer.
Therefore at the level of the cricoid cartilage, where the
pharynx continuous into the esophagus, the orientation of the
muscle fibers is rearranged (Fig. 1.1). Here two weak spots
emerge posteriorly, which are prone to the development of
T. J. Weijs · R. L. A. W. Bleys (*)
Department of Anatomy, University Medical Center Utrecht,
Utrecht, The Netherlands
e-mail: R.L.A.W.Bleys@umcutrecht.nl
T. J. Weijs
e-mail: t.j.weijs@gmail.com
diverticula; Killian’s area, above the cricopharyngeus, and
Laimer’s area, below the cricopharyngeus.
The passage of the esophagus through the thorax, where
the pressure is subatmospheric, requires sphincters at both
ends to prevent continuous swallowing of air and saliva,
and regurgitation of stomach content. The function of upper
esophageal sphincter in the neck is exerted by the distal part
of the inferior pharyngeal constrictor, which is distinguishable and is called the cricopharyngeus (Fig. 1.1). The lower
esophageal sphincter is not a clearly distinct muscle but
rather a physiological sphincter. This is composed of the
local esophageal circular muscle fibers just below the level
of the diaphragm that is able to exert a higher pressure. This
action is reinforced by the right crus of the diaphragm which
envelopes the esophagus at this location and acts as an external sphincter (Fig. 1.2a and b) [2]. Other factors which con-
tribute to closure of the gastro-esophageal junction are the
intra-abdominal course of the last part of the esophagus, the
mucosal rosette, and the oblique muscle fibers of the stomach
which contribute to the cardiac notch and flap-valve of Hill.
Finally the adventitia consists of loose connective tissue,
which facilitates movement.
1.3 Fixation
The esophagus is attached to the trachea by several connective tissue strands and to the diaphragm by
the phrenico-esophageal ligament (Fig. 1.2a) [3]. The
phrenico-esophageal ligament stabilizes the esophagus at
the level of the diaphragm, which is important to maintain
the synergy of the components of gastro-esophageal closure. This ligament wraps the gastro-esophageal junction
like a collar and is derived from the endothoracic and transversalis fascias which run above and below the diaphragm,
respectively. Furthermore the esophagus is attached to the
aorta by a thin layer of connective tissue which is called the
aorto-esophageal ligament (Fig. 1.3) [4].
© Springer Nature Switzerland AG 2021
M. Asunción Acosta et al. (eds.), Atlas of Minimally Invasive Techniques in Upper Gastrointestinal Surgery,
https://doi.org/10.1007/978-3-030-55176-6_1
1
2 T. J. Weijs and R. L. A. W. Bleys
a
b
Fig. 1.1 Structure of the upper esophagus. Transition zone from the
pharynx to the esophagus, where two weak spots emerge above and
below the cricopharyngeus (Killian and Laimer) Source: Pearson FG
et al. Esophageal surgery. 2nd ed. New York, Churchill Livingstone, 2002
1.4 Topography
In the neck, the esophagus courses caudally from the level
of the cricoid cartilage. It lies in the visceral compartment
which is anteriorly bounded by the strap muscles, laterally by the carotid sheaths and posteriorly by the alar fascia
(Fig. 1.4a and b) [5]. This compartment extends to the level
of the aortic arch. In the visceral compartment, the esophagus lies between the trachea and alar fascia. A thin layer of
connective tissue, the visceral fascia, envelops esophagus
and trachea. Of interest are the recurrent laryngeal nerves
that course lateral to the trachea and esophagus to the vocal
cords. Finally the thyroid gland is found anterior to the
trachea.
In the thorax, below the aortic arch, the esophagus
traverses the posterior mediastinum. This compartment
is bounded by the pericardium anteriorly, right pleura on
the right lateral side, left pleura and aorta on the left lateral side, and spine posteriorly (Fig. 1.5a–d). The poste-
rior mediastinum is further divided into a peri-esophageal
compartment and a para-aortic compartment by the aortoesophageal and aorto-pleural ligaments [6]. In the periesophageal compartment the esophagus, carinal lymph
nodes and vagus nerves are located. The para-aortic compartment contains the azygos vein and thoracic duct. The
Fig. 1.2 a. Schematic drawing of the gastro-esophageal junction
demonstrating two ways in which the endothoracic and transversalis
fascias may contribute to the phrenico-esophageal ligament. On the
right side, the endothoracic fascia fuses with the upper leaflet of the
transversalis fascia while on the left side they attach separately to the
esophagus. b. Mean distances in centimeters between an imaginary
horizontal line through the diaphragm and attachment points of the
fascial layers of the phrenico-esophageal ligament. It is demonstrated
that the upper part of the ligament is the longest part (From Apaydin
et al. [3]; with permission.)
para-aortic compartment is an extension of the potential
space between the alar fascia and the prevertebral fascia.
This space is known as “the danger space”, because retropharyngeal abscesses can quickly spread via this route to
the mediastinum[7].
In the abdomen, the esophagus traverses 1.5 cm of
the upper abdomen to end in the stomach. The abdominal
part of the esophagus is partially covered by peritoneum
whereas the other parts do not have a serous lining.
31 Surgical Anatomy of the Esophagus
a
b
Fig. 1.3 Illustration of the aorto-esophageal ligament, previously
named “meso-esophagus”. It is a bilayered connective tissue layer
with blood vessels coursing from the descending aorta to the esophagus. Abbreviations: ps: pericardial sac; lu: right lung; vp, right pulmonary vein; ca: carina and right bronchus; meso-oe: meso-oesophagus;
az: azygos vein; ao: aorta; oe: oesophagus (From Cuesta et al. [4];
with permission.)
1.5 Arteries and Veins
The cervical esophagus is supplied by branches of the inferior thyroid artery (Fig. 1.6a and b). The thoracic esopha-
gus is supplied by 1–2 branches of the bronchial arteries
and in 20% by a direct branch of an intercostal artery.
Furthermore, between the level of the tracheal bifurcation and the diaphragm 4–5 small arteries branch from the
anterior side of the descending aorta to descend obliquely
to the esophagus. The abdominal esophagus is supplied by
branches of the left gastric artery and often (55%) branches
of the left inferior phrenic artery. Occasionally there is an
anastomosis between the left gastric artery and left inferior
phrenic artery, called Belsey’s artery. The esophageal arteries are connected by a dense uninterrupted network of arterioles located in the esophageal mucosa and submucosa,
which secures a good blood supply even when a large part
of the esophagus is mobilized [8–10].
The blood leaving the esophagus collects in a subepithelial plexus and a submucosal plexus. These plexus drain
through perforating veins into the peri-esophageal plexus
surrounding the esophagus. In the neck, these veins drain
into the inferior thyroid and vertebral veins. In the thorax,
the peri-esophageal plexus generally drains into the azygos
Fig. 1.4 a. The esophagus traversing the visceral compartment in
the neck. MR image. Abbreviations: Car: carotid artery; Esophagu:
esophagus; Jug: jugular vein; LCM: longus colli; Ln: lymph node;
SCM: sternocleidomastoid. b. Schematic drawing. Abbreviations: Car:
carotid artery; Eso: esophagus; Jug: jugular vein; LCM: longus colli
muscle; Ln: lymph node; Rln: recurrent laryngeal nerve; SCM: sternocleidomastoid; SCA: subclavian artery; V: vagus nerve; VA: vertebral
artery
and hemi-azygos veins. In the abdomen, the esophageal
plexus drains into the left gastric and inferior phrenic veins;
forming a well-known portal-caval anastomosis [11].
4 T. J. Weijs and R. L. A. W. Bleys
ab
a
b
d
c
Fig. 1.5 Photograph of a transverse section of the posterior mediastinum between the diaphragm and tracheal bifurcation (a) with a magnetic
resonance image of the same section (b), histology (c), and a schematic summary (d). For histology the Verhoef-Von Gieson stain was used
(elastin stained black-blue; collagen stained light red-pink). The black arrows indicate the aorto-esophageal ligament, the blue arrows indicate
the aorto-pleural ligament, the white arrows indicate the right and left pleural reflections and the red arrows indicate blood vessels. In the schematic drawing the green line represents the pleura, the yellow line represents pericardium and the black line the aorto-esophageal and aortopleural ligaments. Abbreviations: Av: azygos vein; Ln: lymph node; TD: thoracic duct; V: vagus nerve (From Weijs et al. [6]; with permission.)
Fig. 1.6 a. Arteries of the esophagus. Right view. Abbreviations: a: thyroid inferior artery; b: right bronchial artery; c: esophageal arteries and
d: branches from the left gastric artery and inferior phrenic artery. b. Arteries of the esophagus. Left view. a: left superior bronchial artery; b: left
inferior bronchial artery; c and d: 7th esophageal arteries from intercostal arteries
51 Surgical Anatomy of the Esophagus
1.6 Lymphatics
The lymph drainage of the esophagus is not segmentally
organized, in contrast to other parts of the intestines. There
is a dense submucosal network of lymphatic channels
which are predominantly oriented longitudinally [12]. From
here lymph channels traverse the esophageal wall to drain
into regional lymph nodes (deep cervical, mediastinal, left
gastric, and celiac) or directly into the thoracic duct (43%)
[13]. For this reason, lymph node metastasis of esophageal
a
cancer can quickly spread over a long distance from the primary tumor. Mediastinal lymph node stations are categorized following the system of the International Association
for the Study of Lung Cancer (Fig. 1.7a and b) or the
Japanese Society of Esophageal Cancer and abdominal
lymph node stations following the system of the Japanese
society for Gastric Cancer [14, 15]. The number of lymph
nodes that can be resected is very dependent on the large
interindividual variation, for example, the number of mediastinal lymph nodes varies from 11 up to 54 [16].
b
Fig. 1.7 a. Lymphatic drainage. The aim of this figure is to show, from a surgical point of view (stations as seen during thoracolaparoscopic
esophagectomy in prone position.) the lymph node stations of the supracarinal area, and vagus nerve including recurrent laryngeal nerves and
the thoracic duct between the aorta and the azygos vein. Abbreviations: e: esophagus; dth: thoracic duct; rrln: right recurrent laryngeal nerve;
lrln: left recurrent laryngeal nerve; ao: aorta; tr: trachea; svc: superior vena cava; lsbra: left superior bronchial artery; libra: left inferior bronchial
artery; rbra: right bronchial artery; av: azygos vein; lb: left bronchus; rb: right bronchus; lv: left vagus nerve; rv: right vagus nerve; lpv: left
pulmonary vein; rpv: right pulmonary vein; R. Lung: right lung. (From Cuesta et al. [14]; Attribution 4.0 International [CC BY 4.0] https://crea-
tivecommons.org/licenses/by/4.0). b. Supracarinal lymph node stations to be resected during esophagectomy. Abbreviations: LN: lymph node;
R: right; L: left. c. Gastric lymph node stations according to the system of the Japanese Gastric Cancer Society. APIS: a. phrenica inferior sinistra; AGES: a. gastroepiploica sinistra; AGB: aa. gastricae breves; VGED: v. gastroepiploica dextra; VCDA: v. colica dextra accessoria; VCM: v.
colica media; VCD: v. colica dextra
6 T. J. Weijs and R. L. A. W. Bleys
The thoracic duct arises from multiple abdominal lymph
vessels. These courses cranially to merge in the thorax,
1.8 cm (IQR: − 0.4–2.4 cm) above the esophageal hiatus
(Fig. 1.7c) [17]. Caudally in the thorax, the thoracic duct is
located between esophagus and spine, just right to the midline. At the level of the azygos vein, it crosses to the left
side and eventually drains into the left venous angle. It is
important to note that the course of the thoracic duct is typical in only 40–60% of cases. The most important variations
are the location of drainage into the venous system and the
presence of (partially) duplicated systems.
1.7 Innervation
The esophagus is innervated by the vagus nerve and
branches of the sympathetic trunk. From the viewpoint of
esophageal surgery the vagus nerves are especially important. In their course close to the esophagus they have important branches that course through the previously mentioned
lymph node stations.
In the neck, the vagus nerves course distally in the
carotid sheath between the carotid artery and jugular vein.
In the superior mediastinum the right vagus nerve
passes anterior to the right subclavian artery. Just below the
right subclavian artery the right recurrent laryngeal nerve
branches off to curve dorsally and cranially around the
right subclavian artery. The left vagus nerve passes anterior
to the aortic arch. Just below the aortic arch, the left recurrent laryngeal nerve branches off to curve dorsally and cranially around the aortic arch, through the aorto-pulmonary
window (lymph node station #5) and then cranially, lateral
to the trachea (lymph node station, #4L). In their ascent to
the larynx, the recurrent laryngeal nerves may course next
to the esophagus, tracheo-esophageal sulcus, or trachea.
Near their entrance into the larynx there is less variation,
and both recurrent laryngeal nerves tend to course near
the tracheo-esophageal sulcus [18]. In their course to the
larynx, the recurrent laryngeal nerves have 8–14 branches
which course medially to innervate the trachea and proximal esophagus [19].
The right vagus nerve continues dorso-caudally to pass
dorsal to the right main bronchus. In the trajectory between
subclavian artery and right main bronchus (lymph node station #4R) a median of 3 vagus nerve branches arise which
form the right anterior pulmonary plexus (Fig. 1.8a and b)
[20]. This plexus is located just cranial to the right pulmonary artery and contains a small proportion (23%) of the
right lung innervation. Dorsally to the right main bronchus a median of 13 vagus nerve branches form the right
a
b
c
Fig. 1.8 Schematic drawings of the right posterior (a) and left pos-
terior (b) pulmonary vagus nerve plexuses as encountered during
transthoracic esophagectomy from a right lateral approach, including
a corresponding photograph (c). Abbreviations: A: azygos vein; Ao:
aorta; Oeso: esophagus; RLN: left recurrent laryngeal nerve; S, sympathetic trunk; T, trachea; V, vagus nerve. (From Weijs et al. [20]; with
permission.)