The role of staging laparoscopy in oesophagogastric cancers

EJSO 33 (2007) 988e992

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The role of staging laparoscopy in oesophagogastric cancers G.W. de Graaf a, A.A. Ayantunde a, S.L. Parsons a, J.P. Duffy b, N.T. Welch a,* a

Department of Surgery, Nottingham City Hospital, Hucknall Road, Nottingham NG5 1PB, UK b Department of Thoracic Surgery, Nottingham City Hospital, Nottingham, UK Accepted 8 January 2007 Available online 7 March 2007

Abstract Aims: Selection of patients for treatment of oesophagogastric cancers rests on accurate staging. Laparoscopy has become a safe and effective staging tool in upper gastrointestinal cancers because of its ability to detect small peritoneal and liver metastases missed by imaging techniques. The aim of this study was to evaluate the role of staging laparoscopy (SL) in determining resectability of oesophagogastric cancers. Methods: A review of 511 patients with oesophagogastric cancers referred to our centre during a 7-year period was performed. Four hundred and sixteen of them assessed to have resectable tumours after preoperative staging with CT and/or ultrasound underwent SL. The main outcome measure was the number of patients in whom laparoscopy changed treatment decision. Results: Staging laparoscopy changed treatment decision in 84 cases (20.2%): locally advanced disease in 17, extensive lymph node disease in four and distant metastases (liver and peritoneum) in 63 cases. The sensitivity of laparoscopy for resectability was 88%. Eighty-one percent of patients who had combined CT scan and EUS were resectable at surgery compared with 65% of those who had CT scan alone (statistically significant with P-value < 0.05). Of those patients deemed resectable by SL 8.1% were found to be unresectable at laparotomy, 16 with locally advanced disease and 11 with metastases. Conclusion: Staging laparoscopy avoided unnecessary laparotomy in 20.2% of our patients and was most useful in adenocarcinoma, distal oesophageal, GOJ and gastric cancers and probably not necessary in lesions of the upper two-third of the oesophagus. Ó 2007 Published by Elsevier Ltd. Keywords: Oesophagogastric cancer; Staging laparoscopy; Imaging techniques; Laparotomy; Neoadjuvant chemotherapy

Introduction Oesophageal cancer is the eighth leading cause of malignancy and the sixth leading cause of death from cancer worldwide. There has also been an alarming rise in the incidence and prevalence of the adenocarcinoma of the oesophagogastric junction in the Western world.1,2 Gastric cancer is the sixth leading cause of malignancy and the eighth leading cause of death from cancer.3 Upper gastrointestinal cancer spreads rapidly, especially to the locoregional lymph nodes and by transcoelomic route to the peritoneal cavity. Peritoneal and other metastatic spreads are crucial prognostic factors in upper gastrointestinal cancers as no cure is possible and patient survival is limited.4,5 Peritoneal spread is the most frequently observed site of * Corresponding author. Tel.: þ44 01159691169x34589; fax: þ44 01158405821. E-mail address: [email protected] (N.T. Welch). 0748-7983/$ - see front matter Ó 2007 Published by Elsevier Ltd. doi:10.1016/j.ejso.2007.01.007

recurrence in gastric and lower oesophageal cancer following attempted curative resection and this arises from transcoelomic dissemination of malignant cells shed from the primary tumour.6 Radical surgical resection is the only curative treatment for patients with oesophagogastric cancers and is the first choice treatment in patients with early stages. The role of neoadjuvant chemotherapy has been recently suggested for patient with locally advanced disease so as to downstage the tumours and make them resectable at a later date.7 However, its roles and its benefits are still being evaluated with different combinations in several multicentric clinical trials. Most patients with oesophagogastric cancers have advanced and inoperable disease at the time of diagnosis8,9 and therefore careful selection is important in the surgical management of oesophagogastric cancers which is usually based mainly on both the patient and tumour characteristics. Accurate preoperative staging is vital to patient selection for treatment. The objectives of cancer staging are to

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confirm the diagnosis of malignancy and to determine the extent of the disease which in turn helps in choosing the treatment modality. It helps to determine which group of patients will benefit from curative surgery and which ones will not be cured by this treatment modality. Staging of oesophagogastric cancers was not precise for several years until the introduction of CT scan and endoscopic ultrasound (EUS). CT scan is the main staging tool in oesophagogastric cancer and it evaluates both the primary and possible distant metastases. However, CT scan is inaccurate in the evaluation of peritoneal disease, small metastases in lymph nodes and other sites. Buenaventura and Luketich10 indicated that CT scan is inaccurate in more than 40% of cases with no obvious metastatic disease detected in spite of the presence of spread either in the peritoneum, lymph nodes or liver. EUS is sensitive for detecting the depth of tumour invasion, because of its ability to image the gastrointestinal wall layers and surrounding structures and is said to be sensitive in detecting local, perigastric and celiac axis nodes11,12 but is a poor indicator of distant metastatic disease.13 The use of the diagnostic staging laparoscopy was introduced to further complement other staging modalities and histologically document metastatic disease. Staging laparoscopy is an acceptable and safe technique and is more sensitive and accurate than CT scan, conventional ultrasound scan or EUS for the detection of hepatic and peritoneal metastases.6,14e17 It allows further assessment of the primary tumour and its local invasion and can detect small lesions of the peritoneum, lymph node and liver by direct visualisations which are not identifiable by CT scan or other imaging modalities.16,18e22 It is known that without the use of staging laparoscopy, diagnosis of small peritoneal, lymph node and hepatic diseases are frequently met as unexpected findings at laparotomy in patients hitherto considered to have localised resectable disease by preoperative imaging modalities.23,24 The two major benefits of diagnostic staging laparoscopy for patients with an upper gastrointestinal tumour are the prevention of unnecessary laparotomy thereby avoiding its associated morbidity and/or mortality and help in identifying patients with locally advanced disease who might benefit from neoadjuvant therapy.25 Unnecessary laparotomy carries a 3% chance of significant mortality and morbidity especially in locally advanced or metastatic disease.26 Staging laparoscopy is indicated for patients with localised disease in the absence of distant metastasis on CT or ultrasound scans and where there is intention for curative surgery. There is no basis for staging laparoscopy in patients with advanced or metastatic disease already diagnosed by imaging technique. The accurate extent of local tumour invasion cannot usually be fully evaluated in all cases by laparoscopic means and is therefore not the primary goal for staging laparoscopy.27 The aim of this study was to examine the role and accuracy of diagnostic laparoscopy in detecting metastasis and

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local tumour invasion during staging of patients with upper gastrointestinal cancers. Its ability in predicting curative resectability in oesophagogastric cancers is also presented. We set out to see whether staging laparoscopy significantly change the treatment decision chosen based on preoperative imaging techniques. Patients and methods A retrospective review of 511 patients with oesophagogastric cancers referred to our centres [Queen Medical Centre (QMC) and Nottingham City Hospital (NCH), England] during a 7-year period (January 1997 and December 2003) was performed. Four hundred and sixteen of these patients who had preoperative staging by imaging techniques and were assessed to be fit for surgery and resectable underwent staging laparoscopy to assess resectability of the tumour. Relevant medical notes, imaging results and MDT decision relating to the cases were reviewed and their data collected. Patients were excluded from staging laparoscopy or attempted curative resection if they were unfit for surgery, had metastasis or locally advanced disease on CT scan and/or abdominal ultrasound or refused surgery. Staging laparoscopy Staging laparoscopy was performed under GA and in some cases followed immediately by definitive curative resection if the disease was assessed to be resectable. The procedure was done usually as a day case a week before intended definitive surgery. Laparoscopy was done through a standard 10-mm umbilical port using a 0 laparoscope (Olympus OTV-S2 chip camera, Olympus Optical Company Limited, Tokyo, Japan) and a 5-mm epigastric port with CO2 pneumoperitoneum and involved careful and thorough inspection of primary tumour and adjacent structure including lymphovascular network, the diaphragm, liver, peritoneum, greater omentum, the pelvis and sometime lesser sac. Biopsies of any suspicious or visible metastatic lesion were taken for histological confirmation. Once the disease was assessed by the laparoscopist as advanced evidenced by extensive locally invasive disease or presence of intraperitoneal or liver metastases, curative intention was abandoned and patient was entered into the palliative care pathway. Staging laparoscopy and surgical resection were performed by anyone of five surgeons all using technique as described previously agreed on the standard of staging laparoscopy and criteria for tumour resectability. Statistical analysis The data of only the 416 patients who underwent staging laparoscopy were analysed using SPSS version 11.5 software (SPSS, Inc., Chicago, IL). The main outcome measure was the proportion of patients whose treatment decision was changed by staging laparoscopy and unnecessary

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laparotomy was avoided. The percentage change in treatment decision and reasons for such change were determined for tumour histology and location subgroups. Accuracy of diagnostic laparoscopy in staging oesophagogastric cancer and percentage change in treatment decision was calculated and compared with preoperative imaging for each subgroup of cancer. Accuracy of CT scan and laparoscopic staging in predicting resectability was compared with the surgical resectability by calculating the diagnostic sensitivity and efficacy as measures of accuracy. Chi-square test of significance was used to compare resectability between those who had CT scan alone and those who had combined CT and EUS, and P-value < 0.05 was considered as significant. Results Demographics A total of 511 patients with oesophageal and gastric cancers were seen during the 7-year period and 416 underwent staging laparoscopy with success rate of 98.3%. The failure rate was due to the presence of adhesion from previous abdominal surgery limiting adequate laparoscopic inspection and staging in seven patients. There was no morbidity or mortality relating to staging laparoscopy recorded in this series. There were 308 males and 108 females with sex ratio of 2.9:1. Median age was 68 years (30e87). The location and distribution of the cancers are shown in Table 1. Preoperative imaging techniques Three hundred and eighty-five patients had a standard CT scan of chest and abdomen following oral and intravenous contrast while the remaining 31 patients had only abdominal ultrasound scan in the earlier days. Only 48 patients had Table 1 Distribution of cancer by site and change in treatment by staging laparoscopy based on tumour site Tumour subsite

Total

Change

Percentage

Proximal oesophagus Middle oesophagus Distal oesophagus Middle and distal oesophagus Gastroesophageal junction Cardia Middle stomach Antrum Cardia and middle Cardia/middle/antrum Middle and antrum Total oesophagus and cardia Total stomach Overall

2 26 164 3 64 48 36 47 7 8 11 307 109 416

0 0 28 1 11 8 13 7 4 6 6 48 36 84

0.0 0.0 17.1 33.3 17.2 16.7 36.1 14.9 57.1 75.0 54.5 15.6 33.0 20.2

Note: adenocarcinoma (n ¼ 375); squamous cell carcinoma (n ¼ 33); high grade dysplasia (n ¼ 3); and others [gastric lymphomas, melanoma and GIST (n ¼ 5)].

combined CT scan and endoscopic ultrasound (Hitachi EUB-525 ultrasound scanner, using a PL26-7.5 MHz probe through an IT240 Endoscope under sedation with 2e5 mg of IV midazolam). The sensitivity and efficacy of preoperative CT for resectability were 66% and 67%, respectively. Eighty-one percent of patients who had combined CT scan and EUS were resectable at surgery compared with 65% of those who had CT scan alone and the difference is statistically significant with P-value < 0.05. Staging laparoscopy Three hundred and thirty-two (79.8%) patients who underwent staging laparoscopy were deemed to have operable disease and hence proceeded to laparotomy while 84 had inoperable disease. Staging laparoscopy therefore avoided unnecessary laparotomy in 20.2% of cases. Of these patients 63 (75.0%) had metastases involving peritoneum and liver either singly or in combination, 17 (20.2%) patients had locally advanced disease (local disease that involves either structures that cannot themselves be resected or disease that cannot be wholly resected) and four (4.8%) patients had extensive lymph node involvement (Table 2). The sensitivity and specificity of staging laparoscopy for resectability were 88% and 100%, respectively. Staging laparoscopy was most useful in patients with adenocarcinoma, distal oesophageal, GOJ and gastric tumours with percentage change in treatment decision of 21.9%, 17.1%, 17.2% and 28.0%, respectively (Tables 1 and 3). One patient with long multifocal squamous cell carcinoma involving the middle and lower thirds of the oesophagus had change in treatment by laparoscopy because of extensive involvement of the right gastric artery and celiac axis nodal masses. The other patient with gastric lymphoma was shown to have extensive disease with liver and peritoneal metastases at staging laparoscopy. Laparoscopy predicted curative resection in 332 patients but a total of 305 patients eventually had curative surgery. Unresectability was found at laparotomy in 27/332 (8.1%) of patients who had successful laparoscopy and judged to be resectable with distribution shown in Table 4. These false negatives represent failure rate of staging laparoscopy in this series. The breakdown of the failure rate with different tumour site is as shown in Table 5.

Table 2 Reasons for change in treatment after staging laparoscopy (n ¼ 84)

Locally advanced disease Extensive lymph node disease Metastases Liver Peritoneal Liver and peritoneal

Frequency

Percentage

17 4 63 13 45 5

20.2 4.8 75.0

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Table 3 Change in treatment by staging laparoscopy based on tumour histology (n ¼ 84)

Table 5 Failure rates of staging laparoscopy by site (n ¼ 27) Location

Frequency

Percentage

Histology subtype

Total

Change

Percentage

Squamous cell carcinoma Adenocarcinoma High grade dysplasia Others

33 375 3 5

1 82 0 1

3.0 21.9 0.0 20.0

Middle oesophagus Distal oesophagus Middle and distal oesophagus Gastro-oesophageal junction Cardia Antrum Whole stomach

4 5 1 8 7 1 1

14.8 18.5 3.7 29.7 25.9 3.7 3.7

Discussion The overall prognosis of patients with oesophageal and gastric cancers remains poor in spite of availability of new chemotherapeutic drugs useful in either neoadjuvant or adjuvant settings. Surgical therapy remains the only cure for oesophagogastric cancers and patients must be adequately staged and selected in order to benefit maximally from this treatment. Multimodal staging techniques are the key to adequate patient selection and planning therapy to minimise unnecessary intervention and patient discomfort. The conventional staging modalities like X-rays, CT/ ultrasound scans and endoscopic ultrasound, however, do not always reliably detect unresectable disease and have been found to be inaccurate in some cases. As high as 30e45% of peritoneal and hepatic metastases have been reported missed by CT scan and other preoperative imaging techniques.28,29 Laparoscopy has become a staging tool in the management of upper gastrointestinal cancers in the last decade because of its ability to detect small peritoneal and liver metastases otherwise readily missed by other imaging techniques. Its accuracy at predicting resectability in upper gastrointestinal tumours has been reported to be as 90e100% in published series and has been shown to prevent unnecessary surgery in 5e64% of patients depending on the type of tumour.29,30 Many authors have demonstrated the accuracy of staging laparoscopy in detecting occult peritoneal, hepatic and even lymph node metastases. It is a safe technique associated with low risk of complication and usually done as a day case.29,31e34 Staging laparoscopy allows more detailed assessment of the tumour looking for serosal involvement, local invasion, peritoneal cavity, liver omentum and lymph nodes. It affords the opportunity to accurately stage the cancer and select patient appropriately either for curative or palliative surgical resection, neoadjuvant therapy or for non-surgical palliative care pathway. The real benefit to the patient is sparing them of unnecessary laparotomy with its associated Table 4 Reasons for nonresectability at laparotomy (n ¼ 27) Factor

Frequency

Locally advanced disease Metastases Peritoneal Liver Coeliac lymph nodes Other

16 11 3 4 3 1

morbidity and mortality and also correctly identifies some of them that may benefit from other therapy. Our series prevented unnecessary surgery in 20.2% of the patients. Krasna et al.31 reported that laparoscopy gave better information about local tumour invasion and peritoneal metastasis than CT scan and EUS combined. In our series, combined CT scan and EUS is a better prediction of tumour resectability than CT scan alone 81% versus 65% with P-value < 0.05. We therefore recommend use of combined CT scan and EUS for routine staging of upper gastrointestinal cancers especially those of oesophageal origin. Vickers and Alderson32 noted that combining these two imaging techniques may improve preoperative staging but EUS is generally poor in predicting neoplastic nodal involvement below the diaphragm and is not generally very useful in staging gastric cancer. Endoscopic ultrasound has been shown to accurately assess the T stage but its accuracy in assessing N stage is questionable.28,35 There is an increasing interest in the use of laparoscopic ultrasound for staging of the oesophagogastric cancers though it is yet to be widely accepted.16,36,37 This technique has added advantage of better resolution, characterisation and biopsy of liver and lymph node metastases. The role of laparoscopic peritoneal lavage as part of the staging modalities has been previously stressed.6 We have added peritoneal lavage cytology to staging laparoscopy by saline washing to further enhance our staging technique. There are reports that staging laparoscopy is probably not very useful in oesophageal cancer especially the upper twothird lesions.29,32 This study confirmed what other authors have observed in that none of our patients with upper twothird lesions had their treatment decision changed by staging laparoscopy. Only one patient with long multifocal squamous cell carcinoma involving the middle and lower thirds of the oesophagus had change in treatment by laparoscopy because of extensive involvement of the right gastric artery and celiac axis nodal masses. This we believe was because of the lesion in the lower third of the oesophagus. We then wonder whether there is any justification for routine use of staging laparoscopy in the management of the upper twothird oesophageal cancers. Several investigators have submitted that the more distal the tumour in the oesophagus, the greater the risk and likelihood of intra-abdominal metastases.17,18,22 Our series showed that staging laparoscopy is most useful in patients with adenocarcinoma, distal oesophageal, GOJ and gastric tumours with percentage change in

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treatment decision of 21.9%, 17.1%, 17.2% and 28.0%, respectively. Some authors have questioned the routine use of laparoscopy in staging oesophagogastric cancers because of its associated, all be it relatively low, immediate morbidity and mortality, potential delay in definitive treatment, possible dissemination of tumour cells during biopsy and port-sites metastases.38,39 We have not encountered such problems in our practice. Siewert39 affirmed that beyond any doubt, staging laparoscopy constitutes a step forward in surgical methodologies and contributes to improved preoperative staging especially by detecting peritoneal spread. Staging laparoscopy has a useful role in the management of patients with oesophagogastric cancers by complementing other staging investigations and this procedure prevented unnecessary laparatomy in one-fifth of our patients. We found it to be most useful in patients with adenocarcinoma, distal oesophageal, GOJ and gastric cancers and less useful in squamous cell carcinoma and the cancer of the upper two-third of the oesophagus because of the lymphatic spread anatomy.

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