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Surgical Treatment of
Localized Gastric Cancer
JOHN I. LEW, MD
MITCHELL C. POSNER, MD
Theodor Billroth performed the first successful gastric resection (a distal subtotal gastrectomy for stomach cancer) in 1881.1 Billroth operated on a 43-yearold woman with gastric outlet obstruction caused by
pyloric carcinoma. Despite tolerating the surgical
procedure well and having a benign hospital course,
the patient died of recurrent gastric cancer 14 months
later. Nevertheless, the new surgical technique
proved to be a great success for Billroth, whose clinic
would later report 257 gastric resections for stomach
cancer in 1894.2 In 1889, Mikulicz began to espouse
lymph node dissection in addition to gastrectomy and
(if required) distal pancreatectomy for the treatment
of gastric cancer.3 In 1898, Charles B. Brigham performed the first successful gastric resection in the
United States, a total gastrectomy, on a 66-year-old
woman using a Murphy button in the reconstruction
phase of the operation, to help create an esophagoduodenal anastomosis.4 The contributions of these
surgeons and others in the late nineteenth century
provided the cardinal foundations for current surgical
management of patients with gastric cancer.
Resection remains the only potentially curative
treatment for localized gastric cancer. The basic surgical approach for stomach cancer that is amenable
to potential cure has essentially remained the same
since Billroths time. In the early 1940s, Coller and
colleagues recommended radical resection, including
regional lymphadenectomy, for all gastric cancers
since lymph node metastasis could be insidious and
because identification of the correct resection plane
is difficult.5 However, other contemporaries were not
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Figure 131.
Figure 132.
253
254
Figure 133.
Figure 134.
Figure 135.
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256
with localized disease, to optimize palliative treatment in those patients with incurable disease, and to
minimize morbidity and mortality. Currently, no
therapeutic modalities except resection provide any
possibility for cure of stomach cancer. Therefore, it is
of paramount importance to determine those patients
who are suitable for curative resection and those
patients who are not. This assessment is performed
both preoperatively and at the time of surgery.
The location of the primary tumor and its pattern
of spread determine the selection of the most appropriate operative procedure for gastric cancer. The
stomach has been divided into thirds for classification.7 The proximal third consists of the gastroesophageal junction and extends to the fundus. Such
tumors of the gastroesophageal junction have
recently been classified into three types, based
solely on topographic and anatomic criteria8 (Table
131). The middle third of the stomach includes the
body of the stomach and extends from the fundus to
the incisura angularis of the lesser curvature. The
distal third of the stomach consists of the pyloric
antrum and originates from the incisura angularis to
the pylorus. Although there is some controversy
regarding which surgical procedure to apply, in general, proximal-third tumors that include the gastric
cardia require a total gastrectomy, with resection of
up to 10 cm of distal esophagus. Likewise, large
tumors of the middle third and fundus of stomach
are treated by total gastrectomy. Distal-third and
small midcorpus tumors, however, are treated surgically with a radical (75 to 85%) subtotal gastrectomy
(Figure 136).7,9,10
Past studies have suggested that the incidence of
proximal gastric cancers has risen over the years
while that of distal gastric cancers has decreased.11,12
This shift from distal tumors to proximal tumors
Type II
Type III
Figure 136.
257
detect carcinomatosis with diffuse peritoneal seeding, malignant ascites, and pelvic metastasis.
Although the stomach, perigastric nodes, and such
distant sites as the liver and lung are visualized, up
to 50% of patients will be found to have gross disease (missed by preoperative CT) at the time of
laparotomy.1719 Endoscopic ultrasonography is
more accurate than CT for determining lymph node
involvement in the perigastric region. The advantages of EUS reside with its ability to visualize all
layers of the gastric wall, perigastric lymph nodes,
and surrounding tissues. Since CT is able to identify distant metastatic sites (eg, liver, lungs, and
ovaries), CT and EUS are considered complementary tests. Studies with pathologic specimens have
shown EUS to be very accurate in determining
depth of invasion and lymph node involvement.20,21
The overall accuracy for tumor staging ranges from
80 to 90%. The diagnostic accuracy of EUS in
determining nodal status ranges from 70 to 90%.
Endoscopic ultrasonography not only detects malignant lymph nodes by size but also by shape, homogeneity, and hypoechogenicity of the lymph node
and by tumor proximity.20,21 Recent technologic
advances allow EUS-guided tissue sampling of
lymph nodes. One limitation, however, is the ability
of EUS to detect lymph nodes that are > 3 cm from
the gastric wall. More recently, laparoscopic ultrasonography (LUS) has been a valuable modality for
identifying missed metastases to the liver and peritoneum and may prove more accurate in detecting
lymph node metastasis and tumor stage.22
Although highly accurate, EUS will not necessarily change the overall surgical approach to gastric
cancer. This diagnostic modality, however, may be
useful in identifying patients who are candidates for
preoperative chemotherapy and radiotherapy trials.
We routinely use CT and endoscopy (with or without ultrasonography) as part of our preoperative
staging work-up in patients with gastric cancer.
SURGICAL MANAGEMENT
Preoperative Preparation
After the decision for surgery has been made, the
preoperative preparation should include optimization of cardiac and respiratory status. Patients
should be typed and screened, in case blood transfusion during surgery is necessary. Patients with gastric cancer often have an increased pH and bacterial
colonization of the stomach and therefore have a
higher risk for wound infection. At the time of intubation, a single dose of a first-generation cephalosporin should be given to cover such common organisms as Streptococcus viridans, Streptococcus
fecalis, Escherichia coli, Clostridium species, and
Bacteroides species.23
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For patients with gastric cancer who have significant weight loss (> 15% of predisease body weight)
and low serum albumin (< 2.9 mg/dL), some surgeons advocate preoperative nutrition support.24 If
such patients can tolerate preoperative nasoenteral
tube feedings, this route of delivery is preferred. In
patients with obstructing gastric cancer, hospitalization for preoperative total parenteral nutrition (TPN)
may benefit those who have severe malnutrition.24
However, for patients with mild or moderate malnutrition, the role of preoperative TPN is limited, and
this nutritional support may actually prolong overall
STAGING
CT
EUS
Preoperative preparation
Comorbidity (eg, cardiac, pulmonary)
Nutritional status
Metastatic disease
(eg, liver)
Metastatic disease
Laparoscopy
Palliative therapy
Surgical
Nonsurgical
Confined to stomach
Exploratory laparotomy
Unresectable
2 to metastatic disease
Resectable disease
Surgical resection
Total gastrectomy for proximal
and midbody tumors
Subtotal gastrectomy for distal
and small midbody tumors
Node negative ()
Postoperative follow-up
History and physical examination
Imaging studies (eg, CT)
Figure 137.
Postoperative adjuvant
therapy (chemoradiotherapy)
Clinical trials
An algorithm for the management of gastric cancer. (CT = computed tomography; EUS = endoscopic ultrasonography.)
259
determine whether there is direct invasion into adjacent structures such as the pancreas. If no liver metastasis or peritoneal seeding has occurred, gastrectomy
should be performed with curative intent.
Total Gastrectomy
260
Figure 1310.
Figure 1311.
Figure 1312.
device.
261
After the removal of the specimen and after diseasefree margins are confirmed histologically, a Rouxen-Y end-to-side esophagojejunostomy is performed. A 28 EEA anvil is placed into the lumen of the
divided esophagus, and the purse-string suture is
262
tied (Figures 1318 and 1319). Once this is accomplished, the jejunum is divided distal to the ligament
of Treitz, with a GIA stapler. The jejunum is mobilized, and its mesenteric blood supply is examined to
confirm that it is intact. The divided distal loop of
jejunum is then brought up through an opening in
the mesocolon just left of the middle colic vessels.
This retrocolic approach enables the jejunal limb to
reach the end of the esophagus in a tension-free
manner. The jejunal staple line is removed, and an
EEA instrument is placed into the jejunum. The trocar from the EEA is brought through the side of the
jejunum, and the instrument is then attached to the
anvil, closed, and fired (Figure 1320). The EEA is
opened, slightly rotated, and then removed. The
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opened end of the jejunal limb is closed with a TA30 stapler. The nasogastric tube is then passed
beyond the anastomosis (Figure 1321). To examine
for air leaks, air is insufflated with the esophagojejunal anastomosis submerged under sterile saline.
A side-to-side jejunojejunostomy 40 cm from the
esophagojejunostomy completes the Roux-en-Y
reconstruction and re-establishes alimentary continuity beyond the ligament of Treitz (Figure 1322).
The side-to-side anastomosis is performed with a
GIA stapler introduced into the antimesenteric sides
of the jejunum. The enteroenterotomy is then closed
with a TA-60 stapler. The jejunum is anchored to the
margins of the mesocolon opening, which must be
closed to avoid internal herniation, with interrupted
Figure 1316. After the stomach and esophagus are mobilized, an automatic purse-string
applier is placed about 6 to 10 cm above the
gastroesophageal junction.
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3-0 silk sutures. At this time, a needle catheter feeding jejunostomy is placed just past the enteroenterostomy and is secured to the abdominal wall with
3-0 silk sutures.
Subtotal Gastrectomy
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selection of patients suitable for curative or palliative resection. Furthermore, the study demonstrated
that a positive cytologic test is a significant prognostic factor for survival.
Laparoscopic techniques are useful for confirming the absence or presence of incurable disease.
Laparoscopy allows easy access to intra-abdominal
structures for biopsy and for determining local
resectability, thereby avoiding unnecessary high-risk
surgical procedures. Furthermore, laparoscopic peritoneal-lavage cytology may play an important role in
staging, evaluating, and classifying patients with
gastric cancer for appropriate treatment. This
approach may be especially valuable in the diagnosis of occult abdominal M1 disease missed by standard ultrasonography or CT. For all of the above reasons, we routinely perform laparoscopy prior to
attempting curative gastric resection.
SURGICAL ISSUES IN GASTRIC CANCER
Extended Lymph Node Dissection
The role of extended lymphadenectomy for gastric
cancer is a controversial issue that continues to
receive much attention. Radical lymph node dissection was embraced as an integral part of gastrectomy procedures, based on an initial report from
Japan that demonstrated a survival benefit for
patients with serosal or involved regional lymph
nodes who underwent D2 lymphadenectomy.32 The
Japanese have made significant contributions to the
classification of regional lymph nodes, which is
essential to the understanding of extended lymph
node resection. The Japanese staging of lymph node
involvement is different from the American Joint
Committee on Cancer (AJCC) system in that it
describes four major nodal groups (N1 to N4) that
comprise 16 separate locations of nodal tissue.
Group 1 (N1) nodes are located closest to the primary tumor and within the perigastric tissue along
the greater and lesser curvature of the stomach.
Group 2 (N2) nodes are found along the major vessels from the celiac axis, including the common
hepatic, splenic, and left gastric arteries. Group 3
(N3) nodes are located at the celiac axis, near the
origin of the superior mesenteric artery, near the
nonrandomized study, Japanese patients who underwent D3 resection had a 5-year survival rate of
21.4%, compared to 10.0% for those patients who
underwent D2 resection for N2 gastric cancer.35
Other studies from Japan reported 5-year survival
rates approaching 50% in node-positive patients
after extended lymphadenectomy.36
These impressive survival outcomes from Japan
have not been reliably reproduced in Western reports
and have undoubtedly contributed to the controversy
over whether or not extended lymphadenectomy confers a survival advantage. A more aggressive surgical
approach involving a total gastrectomy with en bloc
resection of adjacent organs with standard extended
lymphadenectomy is believed by Japanese surgeons
to be the main reason for such good stage-specific
survival. Other factors that may explain such results
include the younger age of Japanese patients, less comorbidity in this population, earlier detection due to
mass screening programs, and stage migration
(described below). Finally, there may exist the possibility that gastric cancers in Japan are inherently different from gastric cancers in other Western countries and that the Japanese have developed a less
aggressive form of the intestinal type of disease.
In the last two decades, D2 resections have
become more commonplace in Western countries.
Nonrandomized studies from Germany, Norway,
and the United States have reported postoperative
morbidity rates of around 30%, mortality rates
between 4 and 5%, and 5-year survival rates
between 26.3 and 47% for D2 resections3739 (Table
133). This variability in outcome is probably due to
the varied definitions of D2 resections.
On the basis of the aforementioned retrospective
data, four randomized studies comparing D1 to D2
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Morbidity
(%)
558
29
78
1,529
n = sample size.
Mortality
(%)
D2 Gastrectomy
5-Yr Survival
(%)
Morbidity
(%)
Mortality
(%)
5-Yr Survival
(%)
5.2
51.2
1,096
30.6
46.6
37
13.0
30.0
105
30.0
47.0
30.0
695
26.3
270
D2 Gastrectomy
Morbidity
(%)
Mortality
(%)
5-Yr Survival
(%)
22
22
0.0
69
21
43.0
0.0
67
25
0.0
45
30
58.6
3.3
35
200
28
6.5
35
200
46.0
13.0
33
380
25
4.0
45
331
43.0
10.0
47
Morbidity
(%)
Mortality
(%)
5-Yr Survival
(%)
n = sample size.
*Study involved extended D3 resections vs. D1 resections.
there was no 5-year survival advantage for D2 resections. Thus, the adopted practice of D2 resection for
Western patients with N1 gastric cancers warrants
reconsideration as this surgical approach is associated with higher postoperative morbidity and mortality rates and no apparent survival benefit.
Extent of Gastric Resection
For proximal gastric tumors, surgical management
remains controversial in regard to the extent of gastric
and esophageal resection and in regard to the optimal
surgical approach. The options include performing a
total gastrectomy through a transabdominal approach
versus performing a proximal gastrectomy through an
Ivor Lewis or transabdominal approach. In general,
proximal tumors often have an advanced presentation
and have a poorer prognosis than distal tumors. In one
report, a survival advantage and a lower recurrence
rate have been shown for patients with stage I and II
disease of the proximal stomach who undergo a radical total gastrectomy with esophagojejunal anastomosis.44 This procedure can be accomplished with minimal morbidity and a mortality of < 5%.45 The
advantages of total gastrectomy when compared to
proximal gastrectomy include the increased probability of achieving negative histologic distal margins and
the relative ease of complete perigastric lymph node
removal. Furthermore, total gastrectomy with Rouxen-Y reconstruction for proximal gastric lesions also
precludes the possibility of alkaline reflux esophagitis that is frequently associated with disabling symptoms after proximal subtotal gastrectomy. However, in
a recent study of 391 patients with proximal gastric
cancers, the extent of resection did not affect the longterm outcome.46 The report concluded that both total
and proximal gastrectomy could equally be safely
accomplished and that they had similar times for
recurrence, similar recurrence rates, and similar 5year survival rates.
Midbody lesions account for approximately 15 to
30% of all gastric cancers, and these tumors tend to
remain asymptomatic until they are locally advanced.
Although the decision to perform a radical total gastrectomy versus a subtotal gastrectomy (75 to 85%)
remains controversial, most midstomach tumors are
large and invade adjacent structures that may require
a radical total gastrectomy or an extended total gastrectomy (en bloc splenectomy and distal pancreatectomy) to achieve negative margins. In a comparative
study, there were no convincing data regarding the
superiority of one procedure over another.47 This
finding may reflect the fact that the majority of
patients in the study had stage III and IV disease and
that no surgical procedure was therefore likely to
have a favorable impact on survival. The lowest local
recurrence rate (16%) was achieved in patients who
underwent extended total gastrectomy. Overall, these
data suggest that tumor biology, rather than the
extent of gastrectomy, dictates the eventual outcome.
Approximately 35% of all remaining gastric cancers occur in the distal third of the stomach. These
lesions are detected earlier than the more proximal
lesions in the stomach because they have the tendency
to cause symptoms of gastric outlet obstruction even
when relatively small. For distal gastric cancers, radical subtotal gastrectomy is the surgical procedure of
choice. This operation requires the resection of
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272
273
Stage Migration
41/52
(79%)
II
15/30
(50%)
III
21/68
(31%)
Overall 5-yr
survival rate 77/150
(52%)
Group B
26/28
2/2
13/22
13/21
2/9
21/68
(93%)
(100%)
(59%)
(62%)
(22%)
(31%)
26/28
(93%)
II
15/23
(65%)
III
36/99
(36%)
77/150
(52%)
274
ation, chemotherapy, or both yielded no survival benefit when compared to surgical resection alone.
When the findings from this study were compared to
experiences reported from 56 Japanese hospitals, a
higher incidence of stage I gastric cancer was noted
among patients from Japan (33.7%), compared to
patients from the United States (17.1%). The overall
survival rate of patients who underwent resection
was 19% in the United States, compared to 56.3% in
Japan. The stage-for-stage 5-year survival rate was
also better in Japan. The reasons for such discrepancy may be due to the understaging of patients in
the American series whereas in the Japanese series, a
more aggressive surgical approach to lymph node
dissection may have provided more accurate staging.
Although the results of surgery for gastric cancer in
the United States are less favorable than those
reported by the Japanese and by centers in other
Eastern countries, the report concluded that earlier
diagnosis and appropriate surgical technique for controlling locoregional disease are essential for optimizing outcomes.
In a subsequent study conducted by the American
College of Surgeons and the American Cancer Society, the demographics, grade, subsite, treatment, and
rate of survival of Japanese Americans were investigated to explain the international differences in
stage-stratified survival for gastric cancer patients.62
The stage-stratified 5-year and 10-year survival rates
based on the fifth edition of the AJCC staging system
were as follows, respectively: stage 1A, 78% and
65%; stage IB, 58% and 42%; stage II, 34% and
26%; stage IIIA, 20% and 14%; stage IIIB, 8% and
3%; and stage IV, 7% and 5%. The report revealed
that Japanese Americans had a superior stage-forstage survival, which was attributed partly to this
groups predilection for fewer proximal tumors, a
lower male-female ratio, and fewer adjacent-organ
resections. Furthermore, the fifth edition of the
AJCC system, which stages lymph nodes according
to number rather than location, proved to be a superior prognostic tool. Finally, the report asserted that
the consideration of proximal tumors as being
located at a separate disease site might improve the
current TNM staging system and concluded that surgical undertreatment of patients with gastric cancer
remains a problem in the United States.
275
rate of cure. In another study from the same institution, of 165 patients with early gastric cancer staged
as T1, the 5-year survival rate after surgical resection was 91% in those patients with negative nodes,
compared to 78% in those patients with positive
nodes.65 Although multivariate analysis showed that
nodal disease and tumors > 4.5 cm in size were associated with decreased survival, only the presence of
nodal disease predicted decreased survival. Moderately or well-differentiated tumors < 4.5 cm and limited to the mucosa had no incidence of nodal metastasis. The authors of the study concluded that early
gastric cancer patients with T1 tumors in the United
States have a prognosis that is as good as that of similar patients in Japan after surgical resection and that
favorable pathologic tumors should be considered
for limited resection without lymphadenectomy.
Current surgical treatment for early gastric cancer should therefore consist of subtotal gastrectomy
with regional lymph node dissection. Patients with
multifocal and proximal lesions should be treated
with total gastrectomy. Although extended lymphadenectomy for more advanced lesions remains
controversial, the majority of patients with early gastric cancers do well with limited lymphadenectomy,
and extended dissections may not be indicated. A
limited resection without lymphadenectomy may be
considered in patients with small T1 tumors who
have comorbid conditions that would put these
patients at prohibitive risk if subjected to a more formal and conventional gastrectomy.
In Japan, endoscopic treatment for early gastric
cancer has been evaluated in elderly or other poorrisk patients as well as in those patients who refuse
gastric resection. In one report, endoscopic therapy
in the form of laser ablation, multiple or strip biopsies, or chemical injections followed by careful
monitoring resulted in a disease-free survival rate of
close to 100%.66 The best results are obtained when
tumors are < 2 cm and less likely to be metastatic.
Patients with small elevated tumors found to be limited to the gastric mucosa by EUS evaluation are the
best candidates for endoscopic treatment.67 Although
short-term survival has been promising thus far in
poor-risk patients and in those who refuse gastrectomy, more experience with this minimally invasive treatment modality is needed before endo-
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