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86 Miedema and Rangnekar
Chapter 9 / Gastric Tumors 87
9
Surgical Management of Gastric Tumors
Robert C. G. Martin, MD
and Martin S. Karpeh, JR., MD
CONTENTS
INTRODUCTION
PATIENT SELECTION
TOTAL GASTRECTOMY
COMPLICATIONS
PARTIAL GASTRECTOMY
COMPLICATIONS
SUMMARY
REFERENCES
INTRODUCTION
Gastric cancer remains the second most common cancer in the world, with an estimated 1 million new cases annually (1). During this same time period, deaths from
gastric cancer will approach 840,000.
The risk factors for gastric cancer have been well documented to include a diet high
in salt and smoked foods, gender (male), as well as atrophic gastritis. Race (AfricanAmerican) and low socioeconomic status are commonly associated with a higher prevalence of gastric cancer, but are probably not independent risk factors. Helicobacter
pylori (H. pylori) gastric infection is currently the most heavily studied potential carcinogen for gastric cancer. This association of H. pylori with gastric cancer is primarily
based on epidemiological, and prospective follow-up data that demonstrates an increased
risk of gastric cancer in patients who have H. pylori infections. The risk is estimated to
be about 0.5% per year. Individuals who have had prior gastrectomy also have been
reported to have a greater incidence of so-called gastric stump cancer. New data suggests
that H. pylori related gastric ulcers, but not duodenal ulcers, are associated with gastric
cancers. The appearance of gastric stump cancer occurs 15 yr or more after the primary
resection, with an overall risk that is 0 to 5 times higher than in individuals without
previous gastric resections.
A family history of gastric cancer diagnosed at an early age (< 40 yr old) and/or a
known history of Hereditary Non-polyposis Colon Cancer (HNPCC) have also been
demonstrated to increase the risk of gastric cancer in future generations. These cri-
From: Clinical Gastroenterology: An Internist's Illustrated Guide to Gastrointestinal Surgery
Edited by: George Y. Wu, Khalid Aziz, and Giles F. Whalen © Humana Press Inc., Totowa, NJ
87
88 Martin and Karpeh
teria define a population of patients who have a greater risk of developing carcinoma
of the stomach.
PATIENT SELECTION
The primary therapy for gastric cancer is surgical resection. The type of surgical
resection depends primarily on the location of the primary lesion, the size of the primary
lesion, and the overall stage of disease at presentation. Advances in computed tomography (CT), endoscopy staging, as well as greater use of laparoscopy have allowed both
the surgeon and the gastroenterologist to tailor treatment based on the stage of disease.
Laparoscopy remains the single most sensitive means of detecting peritoneal and small
hepatic metastases.
A greater awareness of upper-gastrointestinal (GI) tract cancers, increased use of
endoscopy, as well as the increasing ability to identify subtle signs of gastric mucosal
cancers, have resulted in a greater number of patients being diagnosed at an earlier
stage of disease. Patients with small (< 3 cm) mucosal (T1a) lesions (Table 1 and 2)
favorable endoscopic appearance (flat and no ulceration), and well-differentiated histology can be effectively treated with endoscopic mucosal resection (EMR) (2). This
technique has been applied with increasing frequency in Japan for the treatment of
favorable mucosal lesions.
The two most common techniques for gastric EMR are the grasp-and-pull and the cupand-suction method (3). The grasp-and-pull technique utilizes a double-channel endoscope, and after careful marking of the planned margins of resection, the submucosa is
injected with saline or sodium hyaluronate to raise the submucosal from the muscularis.
The raised lesion is then grasped and pulled into the channel, and a snare is placed at the
base of the lesion. The mucosa is then resected and the margins are then carefully
evaluated to ensure complete resection.
The cup-and-suction method requires only a single-channel endoscope. After marking the margins, the lesion is raised with a submucosal injection. A clear cap is attached
to the end of the scope and the lesion is then aspirated into the cup with the placement
of a snare at the base of the lesion. The aspiration is then released, allowing for evaluation
of the lesion to ensure the snare encompasses the entire margin, and the lesion is then
resected. Again, careful evaluation after resection is indicated to ensure the lesion is
superficial and that all margins were excised.
This trend in treating patients with early gastric cancer with minimally invasive techniques originated from studies demonstrating that mucosal cancer with the earlier favorable characteristics have a very low incidence of lymph node metastasis. Patients with
small mucosal lesions demonstrating these favorable histologic characteristics have
been found to have a lymph node metastasis rate of 0% to 5% (4–8).
The treatment of more invasive early gastric cancer (T1b) has also been redefined
to take advantage of the benefits of laparoscopic approaches to resect the primary with
an adequate dissection of the perigastric N1 nodes. In the case of large (> 4.5 cm)
poorly differentiated tumors invading into the submucosa, the risk of N2 nodal involvement is sufficiently high to include these nodes in the resection (7–10). We
perform a D2 lymphadenectomy in the latter scenario case because cure is still possible
for T1 tumors with N2 nodes (7,8).
More invasive cancers, defined by endoscopic ultrasound as invading the muscularis
mucosa or deeper, which continues to be the most common presentation in Western
Chapter 9 / Gastric Tumors 89
Table 1
TMN Classification for Gastric Cancer
Primary tumor (T) Regional lymph nodes (N) Distant metastasis (M)
TX: Primary tumor cannot NX: Regional lymph node(s) MX: Distant metastasis
be assessed cannot be assessed cannot be assessed
T0: No evidence of primary N0: No regional lymph node M0: No distant metastasis
metastasis tumor
Tis: Carcinoma in situ: N1: Metastasis in 1 to 6 lymph M1: Distant metastasis
Intraepithelial tumor nodes
without invasion of
lamina propria
T1: Invasion lamina propria/ N2: Metastasis in 7 to 15
submucosa lymph nodes
T2: Invasion muscularis N3: Metastasis in more than 15
propria/subserosa regional lymph nodes
T3: Penetrates serosa w/o
invasion of adjacent
structures
T4: Invades adjacent structures
Table 2
Staging of Gastric Cancer
Stage 0: Tis N0 M0
Stage IA: T1 N0 M0
Stage IB: T1 N1 M0
T2 N0 M0
Stage II: T1 N2 M0
T2 N1 M0
T3 N0 M0
Stage IIIA: T2 N2 M0
T3 N1 M0
T4 N0 M0
Stage IIIB: T3 N2 M0
Stage IV: T4 N1,2 M0
Any T N3
Any T Any N M1
centers, should be treated with a formal resection and adequate lymph node dissection.
Recent changes in the American Joint Committee on Cancer (AJCC) staging guideline
have mandated that a minimum of 15 lymph nodes must be removed and examined
(Table 1). A recent report from Memorial Sloan Kettering Cancer Center (MSKCC)
Department of Surgery have emphasized the importance of adhering to these requirements for accurate nodal staging (9,10). This has placed greater emphasis on achieving
an adequate lymphadenectomy to standardize staging worldwide. The presence of
lymph node metastases is a powerful prognostic factor. The more complete the lymph
node dissection, the better the staging. With accurate staging, sound decisions regarding the need for postoperative adjuvant therapy can be made. The scope of a D1 lymphadenectomy or an extended D2 lymphadenectomy has been well described (Fig. 1).
90
90 Martin and Karpeh
Fig. 1. The defined lymph nodes for resection of gastric lesions within the distal, middle, and proximal stomach. (A) Proximal stomach: paraesophageal, left gastric, hepatic artery, celiac, suprapyloric, and infrapyloric, splenic arery, splenic hilum. (B) Middle stomach: left gastric, hepatic
artery, celiac, left cardia, splenic arery, splenic hilum. (C) Distal stomach: left gastric, hepatic artery, celiac, right cardia.
Chapter 9 / Gastric Tumors 91
The mean number of nodes evaluated by the pathologist at MSKCC was 14 following
a D1 (limited) lymphadenectomy, 18 for D1+ (resecting some N2 nodes), and 26 for the
standard D2 (extended). The D2 lymphadenectomy satisfies all staging requirements
and can be done safely in experienced hands by avoiding pancreaticosplenectomy
(11,12). The D2 lymphadenectomy has not resulted in better overall survival in the
randomized data (13). Follow-up data from the Dutch trial presented at the 4th International Gastric Cancer Congress in April 2000, suggested that for node-positive patients, there is a survival advantage following a D2 dissection for the subset of T2N1
and T3N2 gastric cancer patients. A similar observation was made in 1998 by the
German Gastric Cancer Study Group (14,15). A reasonable minimum approach to the
lymphadenectomy would be to ensure that all perigastric nodes adjacent to the primary
(D1) are removed and extending that to include the left gastric artery nodes for all
advanced cancers. Taking the left gastric artery at its origin removes the site where N2
lymph node involvement is most frequently located (16).
This chapter will review the technical aspects of a proper surgical resection for
gastric cancer.
TOTAL GASTRECTOMY
The first successful total gastrectomy (TG) for cancer was performed in 1897, 16 yr
after Billroth’s historic pylorectomy, by Swiss surgeon Carl Schlatter. This procedure
involves removing the entire stomach from the distal esophagus to the proximal duodenum. TG is performed in many major medical centers for the treatment of gastric cancer.
The primary indications for TG is to obtain a minimum of a 5-cm proximal margin for
large tumors or the body, fundus and /or cardia of the stomach, or with tumors growing
in a diffuse pattern (linitis plastica). The proximal margin length is best determined and
should be recorded at the initial endoscopy. This is particularly important for lesions
arising from the lesser curve.
After diagnostic endoscopy, a CT of the abdomen must be done to rule out the presence of metastatic disease, and to evaluate the possible extent of resection. The presence
of metastatic disease is a relative contraindication to performing a TG because most
patients can be palliated with chemotherapy.
After removing the entire stomach, reconstruction with the proximal jejunum creating
a Roux-en-Y limb (Fig. 2) is the most commonly performed technique. Common variations seen with reconstruction involve the construction of a jejunal pouch. Improvements in oral intake and better weight gain have been attributed to using a pouch. There
have been at least six randomized controlled trials evaluating various surgical reconstruction techniques following total gastrectomy (17–22), and no clear conclusion can
be drawn regarding the optimal reconstruction technique. These trials suffer from either
small sample size, varied use of nonstandard quality of life indexes, and/or they lack
appropriate controls. Efforts continue to design simple, effective, and physiologic means
of reconstructing the GI tract.
Postoperative radiographic evaluation (Fig. 3) is commonly performed to rule out an
anastomotic leak (Fig. 4) between the fifth and seventh postoperative day. Because
clinical signs will usually precede a clinically significant anastomotic leak in most
instances, a gastrografin swallow can be used selectively to confirm clinical suspicion.
92 Martin and Karpeh
Fig. 2. Common reconstruction technique with a Roux-en-Y limb. After total gastrectomy jejunal
pouch is constructed and connected to esophagus.
COMPLICATIONS
The more common major perioperative complications seen after total gastrectomy
are pneumonia and leakage of the anastomosis. Anastomotic leakage is seen more
frequently following an esophageal anastomosis than gastrojejunostomy because the
esophagus lacks the strength of a serosa. In a review of 724 patients seen at MSKCC
who underwent resection that required an esophageal anastomosis, the overall leak rate
was 7%. Other major complications include cardiac dysrhythmias, pulmonary embolism, or bleeding.
The long-term consequences of total gastrectomy are related to an inability to absorb
sufficient nutrition to gain weight. A large majority of patients undergoing total gastrectomy will lose between 5% and 10% of their overall body weight in the immediate
postoperative period (6–12 wk). The weight loss is multifactorial, but in part is related
to limited intake because of early satiety and/or increased losses from diarrhea. This can
be effectively treated with diet modifications of frequent small, high-calorie meals, and
avoiding fatty meals. Symptoms of fat intolerance can develop, which often respond to
pancreolipase supplementation.
Dumping syndrome, which is the rapid emptying of undigested food into the intestine
and small bowel immediately after a meal, can lead to nausea, emesis, bloating, and
diarrhea. Delayed symptoms, including weakness and perspiration, can occur approx 2–
4 h after a meal. The most effective therapy for dumping syndrome is a diet of small,
frequent meals that are low in simple carbohydrates, and the avoidance of drinking
liquids with meals. Antidiarrhea agents may also be useful.
Another complication following total gastrectomy is stricture formation at the
esophagojejunostomy anastomosis. This may arise after a small leak has healed second-
Chapter 9 / Gastric Tumors 93
Fig. 3. Normal gastrografin swallow after total gastrectomy.
arily. A tightly stapled or hand-sewn anastomosis or ischemia at the anastomosis can lead
to a stricture. Symptoms can present as dysphagia 1–6 wk following total gastrectomy.
Almost all of these strictures can be treated with endoscopic dilations. The number of
dilations is variable among patients, but two to three dilations are not uncommon.
A less common consequence of total gastrectomy is bile reflux. This can be effectively treated with Sucrafate. One of the primary reasons for this complication is construction of a short Roux-en-Y limb that is less than 45 cm in length. Creating a Roux-en-Y
limb of adequate length essentially eliminates this problem.
PARTIAL GASTRECTOMY
A partial gastrectomy for gastric cancer is performed either in the form of a proximal
subtotal gastrectomy or a distal subtotal gastrectomy. The proximal gastrectomy is a
procedure that has increased in frequency as the incidence of small early stage proximal gastric cancer increases. The decision to perform either of these procedures is
dependent on the location of the primary lesion. Early (T1b) gastric cancers and small
advanced lesions located in the proximal one-third of the stomach (Fig. 5) can be
treated with a proximal resection, provided that a generous gastric pouch remains.
Lesions located in the distal two-thirds of the stomach (Fig. 6) are often treated with
a distal subtotal resection.
94 Martin and Karpeh
Fig. 4. Anastomotic leak demonstrated on gastrografin swallow following total gastrectomy.
The preoperative radiographic evaluation for these patients is the same as for patients
who require a total gastrectomy, and consists of a CT of the abdomen to rule out metastatic disease and to evaluate the possible nodal involvement. Once metastatic disease
has been ruled out and the primary lesion can be resected with a partial gastrectomy, this
is performed with a gastrojejunostomy reconstruction (Fig. 7).
COMPLICATIONS
The types of perioperative complications with a proximal gastrectomy or distal gastrectomy have several similarities and differences. The primary difference between the
two types of partial gastrectomy (distal vs proximal) is the anastomotic leak rate. Patients
who have undergone a proximal gastrectomy have a much higher leak rate (11.5%)
compared with patients who have undergone a distal gastrectomy (< 1%) and has been
reported to be even higher than for a total gastrectomy. Proximal gastrectomy is reputedly associated with profound bile reflux. This is more related to the size of the gastric
remnant than simply the operation. With a patulous gastric remnant, and an anastomosis
that sits in the abdomen, much of the debilitating symptoms of bile reflux can be avoided.
Other common complications are related to pulmonary dysfunction following a major
abdominal surgery.
Chapter 9 / Gastric Tumors 95
Fig. 5. A proximal one-third gastric cancer.
Fig. 6. A primary gastric cancer of the antrum.
The long-term consequences of partial gastrectomy are related to impaired motility.
Impaired motility can present with poor emptying of the Roux-en-Y limb, which can lead
to early satiety or emesis. This dysmotility can be treated with prokinetic agents such as
Reglan or erythromycin with moderate success; the vast majority of patients will improve
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