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Annals of Surgical Oncology 8:519-524 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

A Pilot Study of Preoperative Chemoradiotherapy for Resectable Gastric Cancer

Andrew M. Lowy, MD, Barry W. Feig, MD, Nora Janjan, MD, Tyvin A. Rich, MD, Peter W. T. Pisters, MD, Jaffer A. Ajani, MD and Paul F. Mansfield, MD

From the Departments of Surgical Oncology (BWF, PWTP, PFM), Digestive Diseases (JAA), and Radiation Therapy (TAR), The University of Texas, M.D. Anderson Cancer Center, Houston, Texas; and the Department of Surgical Oncology (AML), University of Cincinnati, Cincinnati, Ohio.

Correspondence: Address correspondence and reprint requests to: Paul F. Mansfield, MD, Department of Surgical Oncology, Box 106, The University of Texas, M.D. Anderson Cancer Center, 1515 Holcombe Boulevard, Houston, TX 77030; Fax: 713-792-0722; E-mail: pmansfie{at}notes.mdacc.tmc.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The goals of this study were to assess the feasibility and toxicity of a regimen of preoperative chemoradiotherapy, surgery, and intraoperative radiotherapy in the treatment of patients with potentially resectable gastric cancer. A secondary objective was to assess pathologic response to chemoradiotherapy in the treated tumors.

Methods: Twenty-four patients were entered in the protocol. Treatment regimen consisted of 45 Gy of external beam radiotherapy with concurrent 5-FU given as a continuous infusion at a dose of 300 mg/m2. Patients were restaged 4–6 weeks after chemoradiotherapy and then underwent surgical resection and intraoperative radiotherapy to a dose of 10 Gy.

Results: Twenty-three patients (96%) completed chemoradiotherapy in accordance with the study protocol. Nineteen (83%) of 23 patients who completed chemoradiotherapy underwent surgical resection with D2 lymphadenectomy. Four patients (17%) had progressive disease and were not resected. The morbidity and mortality rates were 32% and 5%, respectively. Of the resected patients, two (11%) had complete pathologic responses while 12 (63%) had pathologic evidence of significant treatment effect.

Conclusions: Preoperative chemoradiotherapy for gastric cancer can be delivered safely and is well tolerated. The rate of surgical complications is consistent with that of other recently reported prospective trials of gastrectomy alone. Preoperative chemoradiotherapy resulted in significant pathologic responses in the majority of treated tumors, and complete pathologic responses were achieved in some patients.

Key Words: Preoperative chemoradiotherapy • Gastric cancer


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Despite its declining incidence in the United States during this century, gastric cancer remains a worldwide health problem.1 In Western series, less than half of the patients present with localized disease, and of those who undergo surgical resection, 70% recur.2 While the high incidence of peritoneal and liver metastases is well recognized, patterns of failure studies have repeatedly demonstrated local-regional recurrence to be a significant problem as well. In published series of reoperation, autopsy, and clinical follow-up, local-regional recurrence after surgical resection has been reported to range from 24% to 54%.3–5

In an attempt to improve local control, several groups have investigated postoperative external beam radiation (EBRT) or intraoperative radiation therapy (IORT), with varying results.6–11 The use of chemoradiotherapy in the neoadjuvant or preoperative setting has been widely applied to the treatment of esophageal and rectal carcinoma; however, it has not been evaluated in gastric cancer. Its beneficial results and its theoretical benefits for these other tumor types have been discussed in detail elsewhere.12,13 Perhaps the most salient argument for its investigation in the treatment of gastric cancer therapy preoperatively is the greater likelihood that patients would be able to tolerate the treatment before, rather than after, an operation as significant as gastrectomy. Due to the nature of gastric surgery, many patients experience a prolonged postoperative recovery, often with additional weight loss and fatigue. As such, significant delays in initiation of postoperative adjuvant chemotherapy and radiation are common.14 As many as one-third of the patients do not recover quickly enough to tolerate adjuvant therapy in a timely fashion. In addition, despite surgical resection, roughly 10% to 15% of patients with locally advanced gastric cancer (T3 or greater) will rapidly develop distant metastatic disease and thus never really benefit from a resection. For these reasons, we believe that administration of chemoradiotherapy in the neoadjuvant setting should be investigated.

The primary objective of this study was to assess the feasibility and toxicity of a regimen of 5-FU-based chemoradiotherapy followed by surgical resection. A second objective was to assess pathologic response in the treated tumors.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients were eligible for this Institutional Review Board approved prospective study if they had biopsy-proven gastric adenocarcinoma with at least a T2 lesion (or a bulky tumor if endoscopic ultrasound could not be performed) or evidence of malignant perigastric adenopathy if the primary tumor were staged as T1. They could not have evidence of distant disease (distant nodal, peritoneal, hepatic, or other) nor history of prior abdominal radiation. Patients were required to have a Karnofsky score >70; absolute neutrophil count >2000 cells/mm3; bilateral kidney function with a creatinine <1.6 mg/dl; age >17; be free from active infection; could not be pregnant; and had to sign a study-specific consent form. Pretreatment staging included complete physical examination, chest x-ray, abdominal and pelvic CT scan (chest was included for proximal lesions), endoscopic ultrasound (EUS), and laparoscopy. During laparoscopy, peritoneal washings were obtained and a feeding jejunostomy was placed to improve the nutritional status prior to planned resection. Patients with positive peritoneal washings in the absence of visible peritoneal disease were eligible for protocol entry. During the duration of the 13-month study, a total of 156 patients with gastric adenocarcinoma were seen at our institution (including patients with stage IV disease).

The treatment regimen consisted of 45 Gy of EBRT delivered in 25 fractions over 5 weeks through AP/PA portals with kidney shielding as needed. Concurrent continuous infusion 5-FU was given at a dose of 300 mg/m2 daily Monday through Friday for the duration of the radiation treatments. A 25% dose reduction was planned for any patient whose toxicity reached grade 3. Toxicity from chemoradiotherapy for the most common types are typically graded as seen in Table 1.


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  		TABLE 1. Grading of common toxicities of chemoradiation
 
Radiation ports encompassed the primary tumor with a margin of 3 cm as well as the celiac lymph node basins(Fig. 1). Patients were then restaged with CT scans and physical examination 4–6 weeks later and underwent gastrectomy, including a spleen-preserving D2 lymphadenectomy. All patients who had a gastric resection also received 10 Gy of intraoperative radiotherapy to the gastric bed and paraaortic nodes. IORT was delivered via a 7- to 8-cm beveled cone to a penetration depth of 1 cm.



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  		FIG. 1. Planning film demonstrating a representative treatment field for preoperative radiation in a patient with a carcinoma of the gastric body.

 
Pathologic response was assessed by examining serial hematoxylin and eosin sections as previously described.15,16 A complete pathologic response was defined as the absence of viable tumor cells in the treated primary and lymph nodes. A partial pathologic response was defined as <10% viable tumor cells seen on serial sections from the primary tumor.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Demographics
There were 25 patients entered into the study, with one patient registered in error prior to his laparoscopy (during which he was found to have distant disease and was therefore ineligible) and thus did not receive treatment on this protocol. Therefore, there were 24 patients evaluable (15 males, 9 females) with a mean age of 61 years (range 24–76). Most patients had locally advanced tumors based on CT and EUS staging. EUS staging revealed 16 of 20 patients had T3 or T4 lesions. EUS was not completed in four patients due to technical reasons. In addition, most patients also had poor prognosis lesions based on grade and tumor location. Eighteen had grade 3 tumors and twelve had either proximal lesions or linitis plastica(Table 2).


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  		TABLE 2. Tumor characteristics prior to chemoradiation
 
Of the 24 patients entered, only one failed to complete chemoradiotherapy. This patient had presented 4 weeks earlier with an upper gastrointestinal bleed. After 2 days of chemoradiotherapy, he developed recurrent bleeding and was taken directly to surgery. No patient required hospital admission during treatment, though two patients were seen in the emergency room, treated, and released during therapy. Four patients were found to have distant disease on restaging: two developed liver metastases, one was found to have peritoneal metastases, and the fourth developed a malignant pleural effusion.

Nineteen patients underwent resection. There was one histologically positive duodenal margin in a patient with linitis plastica. This patient had a thickened duodenum at laparotomy, and biopsies were taken in an attempt to prove disease beyond the planned point of transection; however, all returned without evidence of disease. On final pathology, the true nature of her disease was evident, and, in retrospect, this complication was an error in judgment to resect. The remaining 18 patients had margin-negative resections. Eleven patients had total gastrectomy, six underwent subtotal gastrectomy, and two patients had an esophagogastrectomy.

Treatment Toxicity
There was relatively minimal toxicity associated with this treatment regimen. One patient required a dose reduction of the 5-FU for grade 3 diarrhea/mucositis. A second patient required a break in therapy, coupled with a dose reduction for treatment of a pulmonary embolism and fatigue. All other patients completed the entire course of chemoradiotherapy in the prescribed time without significant complication. The most common toxicities were mucositis, diarrhea, and nausea.

Major postoperative complications occurred in six patients (32%)(Table 3). Three patients developed pneumonia. There were two anastomotic leaks after total gastrectomy, of which one was subclinical and required no therapeutic intervention. The other patient with an anastomotic leak developed an intra-abdominal abscess as did another patient in whom a leak could not be documented. There were two duodenal stump leaks, one in the patient with linitis plastica mentioned above. The other leak occurred in a patient after subtotal gastrectomy and is presumed to have been technical in origin. One postoperative death occurred in a patient who suffered a witnessed aspiration and subsequent cardiac arrest on postoperative day 3.


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  		TABLE 3. Morbidity and mortality
 
Treatment Response
Of the 19 resected patients, 2 (11%) had complete pathologic responses, and 12 (63%) had partial responses (Fig. 2). Among the partial responders, there were three patients with only a single 1-mm focus of residual carcinoma. In five patients (27%), there was either minor or no evidence of treatment effect.



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  		FIG. 2. Photomicrographs of a gastric adenocarcinoma pre- (top panel) and posttreatment (bottom panel) with chemoradiotherapy. Note the presence of extensive necrosis and stromal fibrosis present following treatment.

 
One potential concern regarding radiotherapy is the impact on nodal harvest. A comparison was made between the 19 resected patients in this study and similar time period patients treated on preoperative chemotherapy protocols and undergoing similar resections by the same surgeons. Both the median (13 vs. 24) and mean (12.3 vs. 23) number of pathologically evaluated nodes were less (P < .003) in the patients receiving chemoradiotherapy.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The dismal prognosis for most patients with gastric adenocarcinoma has prompted the evaluation of multimodality therapy. In most cases, locoregional recurrence of gastric cancer does not usually result in patient morbidity as significant as seen with recurrent rectal or esophageal cancer. Nonetheless, the gastric bed and regional nodal basins are a frequent site of treatment failure that must be reduced if we are to improve survival rates for patients with gastric cancer. While adjuvant radiotherapy has been a mainstay in the treatment of other gastrointestinal neoplasms, its potential role in the treatment of gastric cancer is less considered. Neoadjuvant approaches are particularly attractive because they allow for assessment of pathologic response in the treated tumor and are generally associated with much higher compliance rates than postoperative therapy. The current study clearly demonstrates that preoperative chemoradiotherapy can be delivered relatively safely.

Four patients were found to have interval disease progression upon restaging. None of the four required laparotomy or endoscopic procedures for palliation. In most patients, the decision to resect a patient with stage IV disease is an arbitrary one and is colored by the thought of expectant palliation. Many patients with advanced disease do not benefit from such an intervention, and none of these four patients suffered an unnecessary resection.

The 11% complete pathologic response rate in this trial was less than that seen after chemoradiotherapy for esophageal or rectal cancer but greater than that seen in patients with pancreatic cancer.17–20 It is possible that other radiation sensitizers such as Taxol, cisplatin, or Gemcitabine, used alone or in combination with 5-FU, may yield improved pathologic responses. These or other specific regimens could be the topic of future investigations. Certainly the pathologic response rate of 73% in resected patients is evidence that chemoradiotherapy has significant activity in the treatment of gastric cancer.

Postoperative complications in this trial exceed those reported in most retrospective series; however, they are in keeping with recently reported complication rates in prospective trials of gastrectomy alone. The British MRC study21 found an in-hospital mortality rate of 13% and a morbidity rate of 46% after gastrectomy and D2 lymphadenectomy. The anastomotic leak rate was 13%. Similarly, Bonenkamp et al.22 reported a mortality rate of 10% and a morbidity rate of 43% with D2 lymphadenectomy in the Dutch randomized trial of D1 versus D2 lymphadenectomy. In that study, there was an anastomotic leak rate of 10%; 17% of the patients had complications of intra-abdominal infection, and 18% of the patients required reoperation. While the present study compares favorably with the studies mentioned above, we felt that the complication rate was too high. Partway through the study, a technical modification was made which seemed to significantly improve the leak problem. Initially, the feeding jejunostomy tube was placed through a minilaparotomy near the midline. The segment of bowel was the area that was subsequently brought up for anastomosis to the stomach remnant or esophagus. Unfortunately, this bowel was usually within the field of radiation. Thus, by placing the feeding tube (using T-fasteners) on the lateral abdominal wall away from the radiation field, this problem was avoided and the incidence of leaks diminished markedly. There were no anastomotic or duodenal stump leaks in the last eight patients treated on the present trial nor in the early experience in a follow-up Phase II trial currently in progress. Thus, we believe preoperative chemoradiotherapy should not result in any significant increase in leak rates over gastrectomy alone but, rather, that the 5% mortality and 32% morbidity rates in the present study primarily reflect the complexity of radical gastric surgery and a learning curve on the part of the surgeons. Certainly, if the location of the lesion permits, design of radiation fields to minimize radiation exposure to the duodenum and distal esophagus is warranted and may further reduce complications.

Although we were concerned that the operation may be more technically difficult due to reaction from the radiation, this turned out to be an insignificant issue. Any increase in difficulty of dissection was, at most, minimal. However, one finding of note is that the left lateral segment of the liver was typically within the radiation portal and this area did demonstrate fibrosis, though there was no clinical significance to this abnormality and no patient demonstrated any liver abnormalities from this.

There was little significant toxicity during chemoradiotherapy, and 96% of the patients completed treatment and 88% received the full doses of radiation and 5-FU in the time prescribed. This must be compared with the recently reported results (presented at American Society of Clinical Oncology) of the Intergroup Trial 0116 of adjuvant therapy in patients who have undergone potentially curative resection.23 In that study, roughly 35% of the patients could not complete therapy (secondary to their debilitated postgastrectomy state). If one considers that perhaps 30% of the patients weren’t even able to be entered into the study because of complications from gastrectomy or slow recovery (patients were required to begin therapy within 6 weeks), then only 46% (70% x 65%) of the patients who might benefit from an effective therapy can actually receive it. This underscores one of the major appeals of neoadjuvant therapy.

The pathologic evaluation of the resected specimen is an important prognostic factor. The potential impact of treatment such as this must be recognized and puts further emphasis on the need for accurate preoperative staging of patients being considered for neoadjuvant therapy trials. The only reported prospective randomized trial of neoadjuvant therapy in potentially resectable gastric cancer was from the Dutch Gastric Cancer Group.24 This was a relatively small number of patients (fewer than 30 in each arm), patients were not staged with laparoscopy, the chemotherapy used is no longer considered a preferred regimen, and radiotherapy was not used. Not surprisingly, this was a negative study. Neoadjuvant chemotherapy without radiation is continuing to be investigated aggressively for the treatment of gastric cancer. It appears that survival rates are excellent among patients who respond to chemotherapy.25 Regional nodal basins were a frequent site of failure among patients who recurred after neoadjuvant chemotherapy alone. Thus, it may be beneficial to add chemoradiotherapy to a regimen of systemic therapy to optimize locoregional disease control, and such studies are underway.

Longer follow-up of this cohort and the treatment of additional patients in a Phase II study are required to determine whether this treatment regimen will truly decrease locoregional recurrence and to determine if there is any impact on survival. Clearly, this treatment appears to be well tolerated, and a high proportion of patients are able to complete therapy as prescribed, thus warranting further investigation, particularly in light of the demonstration of efficacy of postoperative adjuvant chemoradiotherapy.

Received for publication May 17, 2000. Accepted for publication January 29, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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