Ann. N.Y. Acad. Sci.

ISSN 0077-8923

A N N A L S O F T H E N E W Y O R K A C A D E M Y O F SC I E N C E S
Special Issue: Global Perspectives on Esophageal Diseases
CONCISE REVIEW

Cancer of the gastroesophageal junction: a diagnosis,

classification, and management review
Mickael Chevallay,1 Elfriede Bollschweiler,2 Servarayan M. Chandramohan,3
Thomas Schmidt,4 Oliver Koch,5 Giovanni Demanzoni,6 Stefan Mönig,1 and William Allum7
1
Visceral Surgery Department, Geneva University Hospital, Genève, Switzerland. 2 Department of Visceral and Vascular
Surgery, University of Cologne, Cologne, Germany. 3 Department of Surgical Gastroenterology and Center of Excellence for
Upper Gastro Intestinal Surgery, Madras Medical College and Rajiv Gandhi Government General Hospital, Chennai, India.
4
Department of General, Visceral and Transplantation Surgery, University Hospital Heidelberg, Heidelberg, Germany.
5
Department of Surgery, Paracelsus Medical University, Salzburg, Austria. 6 Department of General Surgery, University of
Verona, Verona, Italy. 7 Department of Surgery, Royal Marsden Hospital, London, UK
Address for correspondence: Professor Stefan Mönig, Visceral Surgery Department, Geneva University Hospital, Rue
Gabrielle-Perret-Gentil 4, 1205 Genève, Switzerland. Stefan.Moenig@hcuge.ch

Management of gastroesophageal junction (GEJ) adenocarcinoma is a controversial topic. The rising incidence of this
cancer requires a clear consensus to ensure proper management. Application of oncological principles for tumors of
the esophagus or stomach is not possible because of comparative differences in the biology of GEJ adenocarcinoma,
leading to different therapeutic options. Staging work-up with endoscopy, endosonography, and PET is essential to
inform the choice of neoadjuvant treatment and surgical approach to GEJ adenocarcinoma. Surgery remains the
only curative treatment and should be undertaken in specialized centers.
Keywords: esophagectomy; minimally invasive; FLOT

Introduction introduced in 1987 a system separating GEJ tumors

into three types based on the relationship of the epi-
The junction between the esophagus and the
center of the tumor to the endoscopic location of
stomach can be defined in two ways: anatomically
the GEJ. Tumors with an epicenter 2–5 cm above
with the diaphragmatic hiatus or histologically with
the GEJ were considered type I or distal esophageal
the transition between the esophageal squamous
tumors, those within 2 cm (above or below) of the
epithelium to the gastric glandular cells. This
GEJ were type II or true GEJ tumors, and those with
histological transition renders the mucosa of the
an epicenter 2–5 cm distal to the GEJ were type III
lower esophagus and the gastroesophageal junction
or subcardial tumors (Fig. 1). Preoperative assess-
(GEJ) particularly vulnerable to the damaging
ment of the tumor location according to the Siew-
effect of gastric acid reflux with an increased risk
ert classification and the estimation of the length
of neoplasia and malignant transformation. The
of esophageal and gastric invasion are essential for
incidence of GEJ adenocarcinoma (AC) is rising and
planning the surgical approach.
management should be standardized. Oncological
The Siewert classification has implications for
principles, which are established for cancer of
lymph node spread. Type I tumors predominantly
the esophagus or the stomach, cannot be simply
metastasize to the paraesophageal nodes in the lower
applied to junctional cancers because of specific
mediastinum and into the upper abdominal lymph
pathological features of the latter. In the Western
nodes. More than 15% of the patients also demon-
world, patients with early stages of junctional
strate positive nodes higher in the mediastinum (at
cancers are rare; the majority are diagnosed at an
the tracheal bifurcation) and in the upper medi-
advanced stage with poor prognosis.
astinum. Type III tumors predominantly involve
Classification abdominal nodes, similar to gastric cancer. Type
II cancers spread to both posterior mediastinal and
In an effort to classify GEJ cancers and allow abdominal nodes including lesser curve, left gastric
comparison of treatment results, Siewert et al.1 artery, and coeliac axis.
doi: 10.1111/nyas.13954
Ann. N.Y. Acad. Sci. xxxx (2018) 1–7 
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Cancer of the gastroesophageal junction
Figure 1. Siewert and Nishi classification for esophagogastric
junction tumor.
Since 2016, the TNM (tumor, lymph node,
metastasis) Classification of Malignant Tumors
(9th and 10th editions) defines junctional cancer
as all tumors in which the center is found 2 cm
proximal or distal to the junction. Cancers involving
the GEJ and with an epicenter within the proximal
2 cm of the cardia (Siewert types I/II) are staged
as esophageal. Cancers whose epicenter is more
than 2 cm distal from the GEJ are staged using the
stomach cancer TNM staging, even if the GEJ is
involved.
Incidence
The incidence of esophageal carcinomas is rising
worldwide. An analysis of 43 cancer registries from
Europe, Australia, the United States, and Canada by
Bollschweiler et al.2 showed that the incidence of
AC of the esophagus has been rising rapidly in the
last 20 years (Fig. 2). The only exceptions to date are
the countries of Eastern Europe. A similar analysis
of 42 registries in 12 countries showed an expected
increase of esophageal AC between 2005 and 2030
in all studied countries.3
Diagnosis and staging
The main symptoms in patients with GEJ tumors
are dysphagia and weight loss. However, many have
a long history of reflux which is often dismissed as
in significant. Upper esophagogastroduodenoscopy
2 Ann. N.Y. Acad. Sci. xxxx (2018) 1–7 
Chevallay et al.
Table 1. Staging and proposed treatment of GEJ tumors
Staging Proposed treatment
T1a N0 Endoscopic resection
T1b N0 Surgery
T1bN1–T4a Perioperative therapy and surgery
T4b and metastatic disease Systemic/palliative therapy
(EGD) is the diagnostic examination of choice and
has largely replaced contrast radiology. EGD allows
precise location of the tumor, including determin-
ing the Siewert type, as well as enabling biopsies
for histological diagnosis. Endoscopic ultrasonog-
raphy (EUS) evaluates local invasion and regional
lymph node involvement. The accuracy of EUS can
be limited by the fact that tumor ulceration can be
difficult to differentiate from inflammatory change,
and depth of invasion is not well correlated with the
extent of lymphadenopathy.4
The aim of staging is to determine the most
appropriate therapeutic option (Table 1). The prin-
cipal tools for staging are computed tomogra-
phy (CT), EGD with echoendoscopy (EUS), and
positron emission tomography/CT (PET/CT). Two
retrospective studies have assessed the accuracy
of these staging modalities. Grotenhuis et al.5
compared the histopathological findings from 50
patients who had AC of the GEJ and underwent
esophagectomy with the Siewert type and N-stage
determined preoperatively by EGD/echoendoscopy
(EUS) and CT. Overall accuracy in predicting tumor
location according to the Siewert classification was
70% for EGD/EUS and 72% for CT. The radiol-
ogist was able to classify type II tumors correctly
more often than the endoscopist (53%) although
the accuracy for type I tumors was lower (77%).
Another retrospective study by Pedrazzani et al.6
with 115 patients compared EGD and EGD/EUS for
the determination of the Siewert classification. The
Siewert type was correctly assigned in 72.5% and
64.8% of the cases in EGD/EUS and EGD groups,
respectively. In both groups, the sensitivity was high
for type I and type II tumors, while some difficul-
ties were encountered in classifying type III (distin-
guishing from type II and type III tumors). This is
probably due to the imprecise results in the evalua-
tion of gastric invasion. In particular, the specificity
in classifying type II tumors by endoscopy alone was
C 2018 New York Academy of Sciences.
Chevallay et al.
Figure 2. Incidence of esophageal adenocarcinoma from 1975 to 1995. Adapted from Ref. 2.
extremely low (70.8% versus 44.0% in EGD/EUS
and EGD groups, respectively).
The evaluation of distant lesions by CT of the
thorax, abdomen, and pelvis is directed to assess
regional lymph node metastasis, as well as disease
in the liver, lungs, and retroperitoneal lymph nodes.
The sensitivity and specificity of detection of distant
metastasis by CT are 52% and 91%, respectively.
PET/CT can be added to the primary staging
modality for evaluation of metastatic disease and
increase sensitivity by 15–20%.7 Some histologic
subtypes, in particular noncohesive tumor (signet-
ring cell carcinoma), accumulate contrast less
readily which limits PET/CT in these cases.8 A
cross-sectional imaging can also be limited in the
detection of small volume peritoneal metastasis
which is preferably identified by laparoscopy.
Management
Nutrition
Nutritional consultation is an essential part of the
evaluation of these patients who are often mal-
nourished before the start of neoadjuvant treat-
ment or surgery. If oral feeding with nutritional
supplements is not possible, enteral nutrition with
jejunostomy should be considered; it is better tol-
erated than endoscopically placed nasojejunal tube
feeding. Percutaneous endoscopic gastrostomy has
Ann. N.Y. Acad. Sci. xxxx (2018) 1–7 
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Cancer of the gastroesophageal junction
been advocated9 but can be a risk to the blood supply
of the gastric conduit.
Surgical treatment
Endoscopy can be therapeutic in early tumors
(Tis, T1a) with endoscopic mucosal or submucosal
resection. Such patients often have associated Bar-
rett’s esophagus with columnar cell change, which
requires ablation, for example, by radiofrequency
ablation.
The surgical approach to junctional cancers is
controversial; there is no consensus. Although the
Siewert classification describes the topographical
location of GEJ cancers, in practice precise local-
ization can be difficult to assess endoscopically for
bulky tumors. This is particularly problematical for
type II lesions. Since the aim of surgical resection
is to achieve a clear margin both macroscopically
and microscopically (R0), careful preoperative
assessment of the extent of esophageal and gastric
involvement is crucial. This assessment will deter-
mine the most appropriate surgical procedure for
the tumor for en bloc resection. This is essential
because survival is influenced by margin involve-
ment. In a retrospective study of 1602 patients,
5-year survival was 43.2% for negative margin,
versus 11% for positive margin.10 Most experts
recommend esophagogastrectomy for Siewert I
tumors11 and total gastrectomy for type III tumors.
3
Cancer of the gastroesophageal junction Chevallay et al.

These procedures enable both an R0 resection and

appropriate lymph node resection based on likely
lymph node spread.
For type II tumors, some advocate for esopha-
gogastrectomy, which allows access to both abdom-
inal and mediastinal lymph node stations, while
others recommend an extended total gastrectomy
with a transhiatal dissection of the posterior medi-
astinum. Studies have shown no oncological ben-
efit between esophagectomy and gastrectomy.12 A
retrospective study by Blank et al.13 compared 56
patients undergoing esophagogastrecomy, with 186
patients treated by transhiatal extended gastrec-
tomy. The results showed no significant difference
in R0 resection rates and number of resected lymph
nodes, though a better survival in the Ivor–Lewis Figure 3. Total gastrectomy with distal esophagectomy for
group. The rates of anastomotic leak have also been Siewert type III tumor.
reported to be higher in those undergoing extended
total gastrectomy, probably reflecting difficult access
via a transhiatal approach.14 nerve trauma in the Ivor–Lewis group (RR = 6.70,
95% CI: 3.09–14.55, P < 0.001).
Thoracoabdominal esophagectomy. The Ivor–
Lewis esophagogastrectomy consists of a combined Total gastrectomy with distal esophagectomy. In
abdominal and a thoracic approach. Intervention this procedure via an abdominal approach, a total
begins with either laparotomy or laparoscopy gastrectomy is performed with an extended lym-
to mobilize the stomach, conserving the right phadenectomy, harvesting perigastric nodes, coeliac
gastroepiploic artery as blood supply to act a trunk, splenic artery, hepatic artery, and lower medi-
conduit and an abdominal lymphadenectomy. astinal nodes. The distal esophagus is resected via
The procedure continues with either a right the diaphragmatic hiatus with access to the poste-
thoracotomy or thoracoscopy during which the rior mediastinum (Fig. 3), and a Roux-en-Y recon-
esophagus is resected and medistinal lymph nodes struction is generally made with esophagojejunal
are harvested. A high esophagogastric anastomosis anastomosis.
(above the azygos vein) is made; the advantage of
Minimally invasive techniques. The devel-
this approach is that it simplifies access for both a
opment of minimally invasive techniques for
thoracic and an abdominal lymphadenectomy, and
esophagectomy has a potential advantage to
it ensures a greater resection margin, which should
minimize morbidity. Most centers propose a
be above 5 cm and distal to the tumor.15
laparoscopic abdominal approach, with gastric
Thoracoabdominal esophagectomy with cervical mobilization and pull up of the stomach through the
anastomosis. The McKeown esophagectomy is a diaphragmatic hiatus. The thoracic phase includes
three-stage procedure and differs from the Ivor– either an open procedure (hybrid technique)17 or
Lewis technique with a higher anastomosis in the a thoracoscopic approach. A recently completed
neck. One of the potential advantages is easier man- French MIRO trial using the hybrid approach has
agement of any anastomotic leak. A meta-analysis reported reduced respiratory complications in the
by van Workum et al.16 compared total minimally hybrid group.18 Such evidence suggests that laparo-
invasive esophagectomy using the Ivor–Lewis and scopic mobilization is the preferred approach, irre-
McKeown procedures. The authors included five spective of Siewert type. Thus, both type I and type II
studies and concluded a higher incidence of anas- tumors should be treated by esophagogastrectomy.
tomotic leakage in the McKeown procedure (5.2% The extent of lymphadenectomy during esoph-
after McKeown esophagectomy and 4.7% after Ivor– agectomy should be adequate, as the number of
Lewis) and lower incidence of recurrent laryngeal lymph nodes removed is an independent predictor

4 Ann. N.Y. Acad. Sci. xxxx (2018) 1–7 

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Chevallay et al. Cancer of the gastroesophageal junction

Table 2. Summary of different trials

Tumor of JOG
Studies proportion Intervention Survival R0 resection

MAGIC8 26% Chemotherapy Survival 5 years Nonavailable

perioperative 36% surgery +
chemotherapy
23% surgery alone
ACCORD9 75% Chemotherapy Survival 5 years 87% surgery +
perioperative 38% surgery + chemotherapy
chemotherapy 74% surgery alone
24% surgery alone
CROSS10 75% Radiochemotherapy Median survival 92% RCT + surgery
(RCT) neoadjuvant 49.4 months RCT 69% surgery alone
+ surgery
24 months surgery
alone
FLOT20 57% Chemotherapy Nonavailable 85% in the FLOT group
perioperative 74% in the ECF/ECX
group

of survival. To maximize the survival benefit,
according to one report, a minimum of 23 regional
lymph nodes must be removed.19 The current
German guidelines11 specify the standard of care
should be a two-field lymph node dissection in both
abdominal and thoracic stations.
GEJ tumors with small volume metastatic
disease (oligometastatic) are increasingly being con-
sidered for combined modality treatment, includ-
ing resection;20 however, these should be managed
within the context of clinical trials.
Neoadjuvant treatment
Multimodal treatment has become the standard of
care for locally advanced GEJ tumors because of high
rates of treatment failure after surgery alone. Neoad-
juvant treatments are intended to shrink the tumor
to achieve a higher rate of complete resection and
to eradicate circulating tumor cells. The majority
of scientific evidence relating to junctional tumors
is an extrapolation of studies designed for esoph-
agus or stomach cancers. All tumors staged with
serosa involvement (T3) or regional lymphadenopa-
thy (N1) should receive neoadjuvant treatment. For
tumors involving the muscularis propria (T2), the
role of neoadjuvant treatment should be discussed
with the patient.21
Two large randomized trials have established
the role of perioperative chemotherapy. The UK
MAGIC trial22 compared overall survival between
surgery alone and perioperative chemotherapy and
surgery; the study group had 13% better survival in
5 years. In a similar trial from France (ACCORD
trial)23 with a larger proportion of GEJ cancers,

Table 3. Therapeutic options according to the Siewert classification

Siewert
classification Definition Multimodal treatment Surgery

Type I 1–5 cm above the junction Radiochemotherapy or Thoracoabdominal esophagectomy

chemotherapy (Ivor–Lewis)
Type II 1 cm above to 2 cm under the Radiochemotherapy or Thoracoabdominal esophagectomy or
junction chemotherapy gastrectomy (negative margin resection is
mandatory)
Type III 2–5 cm under the junction Chemotherapy Total gastrectomy with distal esophagectomy

Ann. N.Y. Acad. Sci. xxxx (2018) 1–7 

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Cancer of the gastroesophageal junction
almost the same survival benefit of 14% for the
chemotherapy-treated patients was seen. Subse-
quent studies have shown similar results in the
recent FLOT trial, which reported a superior advan-
tage of a docetaxol-based regimen over the estab-
lished regimens used in MAGIC and ACCORD
trials.24,25
To improve locoregional control and improve
the rate of complete resection, the adding of
radiotherapy has also been studied. The reference
study for chemoradiotherapy is the Dutch CROSS-
trial,26 in which patients receiving a combination
of chemotherapy and radiotherapy before surgery
were compared with a surgery-alone group. The
resection rate with negative margin was greater in
the group with neoadjuvant treatment; overall sur-
vival was also greater in the neoadjuvant group (49.4
versus 24 months).
Each neoadjuvant treatment has its advantages
and disadvantages: radiochemotherapy allows
better locoregional control, compared with chemo-
therapy, which has a greater effect on systemic
metastasis. Table 2 summarizes the different stud-
ies. For locally advanced Siewert I and II tumors,
neoadjuvant radiochemotherapy is an option; for
Siewert III tumors perioperative chemotherapy
is preferred.22 However, comparison between
radiochemotherapy and chemotherapy alone has
yet to be undertaken; early results of ongoing trials
are awaited.27
Conclusion
Esophagogastric junction tumors are a subtype of
cancer for which the incidence is increasing in the
Western world. The location of the primary tumor
and the extent of lymph node involvement are the
bases for therapeutic decisions. Table 3 summarizes
the therapeutic options according to the Siewert
classification. Surgery is still the only curative
treatment and should be performed in specialized
centers. Minimally invasive surgical approaches
are showing results as good as traditional open
surgery. The frequency of locally advanced tumors
at the time of diagnosis indicates multimodal
management by either chemoradiotherapy or
chemotherapy.
Competing interests
The authors declare no competing interests.
6 Ann. N.Y. Acad. Sci. xxxx (2018) 1–7 
Chevallay et al.
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