REVIEW EDITORIAL For reprint orders, please contact: [email protected]
Advantages of staging laparoscopy in gastric cancer: they are so obvious that they are not evident “...in the era of tailored treatment, the basis of optimized therapies is the correct evaluation of tumor spread and exact staging...” Stefano Rausei*,1, Laura Ruspi1, Alberto Mangano1, Georgios D Lianos2, Federica Galli1, Luigi Boni1, Dimitrios H Roukos2 & Gianlorenzo Dionigi1 Gastric cancer is the second most common cause of cancer death and it often presents in an advanced stage at the time of diagnosis. As treatment strategies are different for metastatic and locally advanced disease, the importance of an accurate preoperative staging is evident, especially in the era of tailored treatment. Although several improvements in radiologic imaging have occurred, extraserosal invasion, nodal involvement, peritoneal carcinomatosis and small liver metastases still are unexpected findings at the time of laparotomy. Abdominal ultrasound has a good sensitivity in detecting liver metastases with an accuracy around 53 and 76% [1] , but its sensitivity significantly decreases (20%) for lesions 1 cm [2] . Finally, FDG-PET has a low resolution (4–5 mm), which limits its sensitivity in defining both nodal involvement and primary tumor depth [4] .
Staging laparoscopy is a minimally invasive surgical approach performed in order to evaluate the intra-abdominal involvement of disease and it is indicated in patients who have gastric cancer with no distant metastases detected on optimal pre-operative imaging. This technique enables the de visu appreciation of intraabdominal organs on their surface areas. What is more, it facilitates the bioptic harvesting, it allows free peritoneal fluid withdrawal for cytologic examination (mandatory according to the new TNM edition [5]) and it enables the use of laparoscopic ultrasounds, which has been shown to potentially further increase the accuracy of T and M parameter definition [6–9] . Technically, this minimally invasive technique is carried out during general anesthesia. It can also be performed immediately before gastrectomy. The patient position is supine (we usually perform a peri-umbilical open technique approach to the abdominal cavity). A 10‐mm trocar is introduced under the umbilical scar in order to access the abdominal cavity. Additionally, a 30° scope is introduced in order to get a clear and wide de visu assessment of the supramesocolic region. The ‘inverted TNM mode’ should be applied when this surgical procedure is performed [10] . In particular, any potential ascitic fluid must be totally harvested for immediate
KEYWORDS
• gastric cancer • multimodal treatment • neoadjuvant chemotherapy • peritoneal carcinomatosis • staging
laparoscopy
“Gastric cancer is the second most common cause of cancer death and it often presents in an advanced stage at the time of diagnosis.”
1st Division of General Surgery, Department of Human Morphology & Surgical Sciences, Insubria University Varese-Como, Italy 2 Department of General Surgery, Ioannina University Hospital, Centre for Biosystems & Genomic Network Medicine, Ioannina University, Ioannina, Greece *Author for correspondence: [email protected] 1
10.2217/FON.14.283 © 2015 Future Medicine Ltd
Future Oncol. (2015) 11(3), 369–372
part of
ISSN 1479-6694
369
Editorial Rausei, Ruspi, Mangano et al.
“Complications of staging laparoscopy globally occur with a low incidence and among them the most frequent ones are intra-abdominal organ iatrogenic damages, hemorrhage and infective processes.”
370
cytologic examination and prior to any surgical steps, approximately 200–300 ml of saline solution is introduced into the abdominal cavity. Subsequently, some specimens for cytologic assessment are aspirated from the upper-left quadrant, from the pelvic region and from the region under the liver. The visceral and parietal peritoneal surfaces are systematically assessed in order to exclude any macroscopic potential malignant localization. Any oncologically suspected areas should be investigated by biopsy. Notably, both ovaries should be inspected in order to exclude potential Krukemberg lesions. What is more, the omental, diaphragmatic and hepatic surfaces are carefully assessed. A 5‐mm trocar must be additionally inserted in a midline location to get full operational control of the small intestine, of the gastric parenchyma and the left hepatic lobe. Of note, setting the surgical table at an angle enables movement of the abdominal organs to gain a better surgical approach to the gastric region. The celiac and perigastric lymph nodes are de visu assessed in the liver hilum area, along the lesser and greater gastric curvature and along the hepato-gastric ligament. Given that the N parameter staging is currently debated, in some situations, a bioptic specimen of a single lymph node can be essential in order to evaluate the best therapeutic strategy to be applied (not for an accurate N staging, strictly depending on the number of metastatic nodes). This could be useful when node involvement is highly suspected at preoperative imaging, but there is not any de visu extra-serosal invasion evidence of the primary tumor during the video-laparoscopic investigation. Tumors of the anterior gastric wall can be inspected without manipulation. A third further 5-/10‐mm trocar could be introduced at the right of the midline. This port potentially facilitates the exploration of the lesser sac via a small incision of the Bouchet lamina (a region without vessels in the gastrocolic ligament). This additional surgical maneuver is useful when a posteriorly located fixity is suspected or in case of cancer origin from the posterior wall. The surgical time of such a procedure is approximately 20 min (30 min in case of lesser sac exploration). As a matter of fact, multimodal imaging integrated with explorative laparoscopy may implement the staging accuracy (reported to range from 89 to 100% [6,10] ), modifying clinical staging in almost 60% of patients with treatment implications in almost half of the cases [11] .
Future Oncol. (2015) 11(3)
In our experience we performed laparoscopic staging in all the patients who did not present CT signs of distant metastases. This approach changed therapeutic strategy in 30% of patients otherwise addressed to immediate surgery. In particular, for 91 consecutive patients with gastric adenocarcinoma prospectively observed, we systematically planned CT scan and laparoscopic staging. A total of 15 patients (16%) were revealed with certain or suspected metastatic disease. In particular, 13 patients with liver metastases or peritoneal carcinomatosis were addressed to palliative therapy. Among the 15 patients, we included a patient with CT finding of enlarged para-aortic lymph nodes and another one with C4 finding at peritoneal lavage fluid exam. As for the other 76 patients, 28 (37%) were considered T1-T2N0 and were treated with surgical resection. The remaining 48 patients (63%) were considered patients with locally advanced gastric cancer. Thirty-three patients in this group (69%) directly received surgical treatment because they were considered not fit for preoperative therapy for symptoms, comorbidities or nonacceptance of preoperative chemotherapy, while seven patients (15%) were considered unresectable for T4b tumors. Hence, eight patients with locally advanced gastric cancer have been recruited in a preoperative chemotherapy protocol. Specifically, benefits of staging laparoscopy are intimately related to the avoidance of unnecessary (for indication or timing) surgery: in fact, the accuracy of this diagnostic modality leads to discriminate patients who may immediately undergo surgery from those with metastatic disease or who should receive a presurgical treatment, with a consequent better allocation of resources, as well as a postoperative hospital stay clearly shorter than that after an explorative laparotomy. As an example, a patient with a cT3–4 gastric cancer and no evidence of distant metastases at CT scan can undergo a neoadjuvant treatment. Neoadjuvant therapy has shown to have a compliance rate better than that of postoperative chemotherapy, and its results in terms of downstaging and, consequently, in curative resection are well known [12,13] ; anyway, in order to have satisfactory results, correct indications and accurate patient selection are mandatory. Conversely, another patient may have a positive cytology on the fluid withdrawn or a clear peritoneal carcinomatosis at staging laparoscopy,
future science group
Advantages of staging laparoscopy in gastric cancer negatively affecting any real curative possibility. In other words, for any surgeon it should be advisable at least to attempt to clarify any staging doubts derived from the low reliability of the imaging techniques. Otherwise a (wrongly selected) patient could have a poor outcome and, undoubtedly, the risk to negatively affect the interpretation of neoadjuvant efficacy is very high. This already occurred even more in the previous randomized controlled trials on perioperative chemotherapy [12,13] . Furthermore, in resectable T1–T2N0M0 gastric cancer, staging laparoscopy might confirm the extent of the disease and it can be quickly converted into operative surgery, both videolaparoscopic or open gastrectomy. Considering the various multimodal approaches to gastric cancer and the possibilities of a preoperative treatment, it is evident that laparoscopic exploration of the abdominal cavity can also be useful in restaging patients after neoadjuvant treatment, allowing the preliminary discrimination of responders from nonreponders [14] . In addition, staging laparoscopy has also been proposed as a diagnostic tool for detection of early recurrence of gastric cancer, showing again a higher accuracy than CT scan and PET in detecting peritoneal seeding, which is a common pattern of recurrence in gastric cancer patients [15] . Complications of staging laparoscopy globally occur with a low incidence and among them the most frequent ones are intra-abdominal organ iatrogenic damages, hemorrhage and infective processes. Of note, to our knowledge no procedure-related deaths have been reported so far. What is more, no adverse oncologic effects have been demonstrated [6] . The higher accuracy rate of staging laparoscopy may therefore avoid an References 1
2
Semelka RC, Martin DR, Balci C et al. Focal liver lesions: comparison of dual phase CT andmultisequence multiplanar MR imaging including dymamic gadolinium enhancement. J. Magn. Reson. Imaging 13, 397–401 (2001). Kinkel K, Lu Y, Both M et al. Detection of hepatic metastase from cancer of the gastrointestinal tract by using non-invasive imaging methods (US, CT, MR imaging, PET): a meta-analysis. Radiology 224, 748–756 (2002).
future science group
Editorial
unnecessary laparotomy, with its possible related complications, longer operating room time and longer hospital stay, with a consequent delay in the beginning of adjuvant treatment. Despite the demonstrated benefits of staging laparoscopy, the compliance of surgeons for this management approach in clinical practice is unclear [16] . Unfortunately, laparoscopic staging is not widely adopted and it still has some limitations: as no morphologic criterion to define a lymph node as metastatic has been proven, nodal involvement may be underestimated; a frozen section of enlarged nodes should be taken, and this increases the cost of the procedure. In conclusion, in the era of tailored treatment, the basis of optimized therapies is the correct evaluation of tumor spread and exact staging; since this cannot always be defined by traditional imaging, surgeons should get used to offering staging laparoscopy in patients with a gastric cancer (especially if >cT1) with no evidence of distant metastases, if no contraindications to laparoscopic surgery exist. It is true that no level 1 evidence has been proven for staging laparoscopy, but it is unquestionable that robust evidence is unlikely to be acquired in the future considering the obvious and convincing advantages of this staging modality. Financial & competing interests disclosure The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending or royalties. No writing assistance was utilized in the production of this manuscript.
3
Makino T, Fujiwara Y, Takiguchi S et al. Preoperative T staging of gastric cancer by multi-detector row computed tomography. Surgery 149(5), 672–679 (2011).
7
Anderson DN, Campbell S, Park KG. Accuracy of laparoscopic ultrasonography in the staging of upper gastrointestinal malignancy. Br. J. Surg. 83, 1424–1428 (1996).
4
Kwee RM, Kwee TC. Imaging in local staging of gastric cancer: a systematic review. J. Clin. Oncol. 25(15), 2107–2116 (2007).
8
5
Edge SB, Byrd DR, Compton CC et al. AJCC Cancer Staging Manual (7th Edition). Springer, New York, NY, USA (2011).
Finch MD, John TG, Garden OJ, Allan PL, Paterson-Brown S. Laparoscopic ultrasonography for staging gastroesophageal cancer. Surgery 121, 10–17 (1997).
9
Richards DG. Endoscopic ultrasound in the staging of tumours of the esophagus and gastro-esophageal junction. Ann. R. Coll. Surg. Engl. 82, 311–317 (2000).
6
Chang L, Stefanidis D, Richardson WS et al. The role of staging laparoscopy for intraabdominal cancers: an evidence-based review. Surg. Endosc. 23, 231–241 (2009).
10 D’Ugo DM, Pende V, Persiani R et al.
Laparoscopic staging of gastric cancer:
www.futuremedicine.com
371
Editorial Rausei, Ruspi, Mangano et al. an overview. J. Am. Coll. Surg. 196(6), 965–974 (2003). 11 Blackshaw GRJC, Barry JD, Edwards P,
Allison MC, Thomas GV, Lewis WG. Laparoscopy significantly improve the perceived preoperative stage of gastric cancer. Gastric Cancer 6, 225–229 (2003). 12 Cunningham D, Allum WH, Stenning SP
et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N. Engl. J. Med. 355, 11–20 (2006).
372
13 Ychou M, Boige V, Pignon JP et al.
Perioperative chemotherapy compared with surgery alone for resectable gastroesophageal adenocarcinoma: an FNCLCC and FFCD multicenter Phase III trial. J. Clin. Oncol. 29, 1715–1721 (2011). 14 Cardona K, Zhou Q, Gonen M et al. Role of
repeat staging laparoscopy in locoregionally advanced gastric or gastroesophageal cancer after neoadjuvant therapy. Ann. Surg. Oncol. 20, 548–554 (2013).
Future Oncol. (2015) 11(3)
15 Shim JH, Yoo HM, Lee HH et al. Use of
laparoscopy as an alternative to computed tomography (CT) and positron emission tomography (PET) scans for the detection of recurrence in patients with gastric cancer: a pilot study. Surg. Endosc. 25, 3338–3344 (2011). 16 Karanicolas PJ, Elkin EB, Jacks LM et al.
Staging laparoscopy in the management of gastric cancer: a population-based analysis. J. Am. Coll. Surg. 213(5), 644–652 (2011).
future science group
Advantages of staging laparoscopy in gastric cancer: they are so obvious that they are not evident “...in the era of tailored treatment, the basis of optimized therapies is the correct evaluation of tumor spread and exact staging...” Stefano Rausei*,1, Laura Ruspi1, Alberto Mangano1, Georgios D Lianos2, Federica Galli1, Luigi Boni1, Dimitrios H Roukos2 & Gianlorenzo Dionigi1 Gastric cancer is the second most common cause of cancer death and it often presents in an advanced stage at the time of diagnosis. As treatment strategies are different for metastatic and locally advanced disease, the importance of an accurate preoperative staging is evident, especially in the era of tailored treatment. Although several improvements in radiologic imaging have occurred, extraserosal invasion, nodal involvement, peritoneal carcinomatosis and small liver metastases still are unexpected findings at the time of laparotomy. Abdominal ultrasound has a good sensitivity in detecting liver metastases with an accuracy around 53 and 76% [1] , but its sensitivity significantly decreases (20%) for lesions 1 cm [2] . Finally, FDG-PET has a low resolution (4–5 mm), which limits its sensitivity in defining both nodal involvement and primary tumor depth [4] .
Staging laparoscopy is a minimally invasive surgical approach performed in order to evaluate the intra-abdominal involvement of disease and it is indicated in patients who have gastric cancer with no distant metastases detected on optimal pre-operative imaging. This technique enables the de visu appreciation of intraabdominal organs on their surface areas. What is more, it facilitates the bioptic harvesting, it allows free peritoneal fluid withdrawal for cytologic examination (mandatory according to the new TNM edition [5]) and it enables the use of laparoscopic ultrasounds, which has been shown to potentially further increase the accuracy of T and M parameter definition [6–9] . Technically, this minimally invasive technique is carried out during general anesthesia. It can also be performed immediately before gastrectomy. The patient position is supine (we usually perform a peri-umbilical open technique approach to the abdominal cavity). A 10‐mm trocar is introduced under the umbilical scar in order to access the abdominal cavity. Additionally, a 30° scope is introduced in order to get a clear and wide de visu assessment of the supramesocolic region. The ‘inverted TNM mode’ should be applied when this surgical procedure is performed [10] . In particular, any potential ascitic fluid must be totally harvested for immediate
KEYWORDS
• gastric cancer • multimodal treatment • neoadjuvant chemotherapy • peritoneal carcinomatosis • staging
laparoscopy
“Gastric cancer is the second most common cause of cancer death and it often presents in an advanced stage at the time of diagnosis.”
1st Division of General Surgery, Department of Human Morphology & Surgical Sciences, Insubria University Varese-Como, Italy 2 Department of General Surgery, Ioannina University Hospital, Centre for Biosystems & Genomic Network Medicine, Ioannina University, Ioannina, Greece *Author for correspondence: [email protected] 1
10.2217/FON.14.283 © 2015 Future Medicine Ltd
Future Oncol. (2015) 11(3), 369–372
part of
ISSN 1479-6694
369
Editorial Rausei, Ruspi, Mangano et al.
“Complications of staging laparoscopy globally occur with a low incidence and among them the most frequent ones are intra-abdominal organ iatrogenic damages, hemorrhage and infective processes.”
370
cytologic examination and prior to any surgical steps, approximately 200–300 ml of saline solution is introduced into the abdominal cavity. Subsequently, some specimens for cytologic assessment are aspirated from the upper-left quadrant, from the pelvic region and from the region under the liver. The visceral and parietal peritoneal surfaces are systematically assessed in order to exclude any macroscopic potential malignant localization. Any oncologically suspected areas should be investigated by biopsy. Notably, both ovaries should be inspected in order to exclude potential Krukemberg lesions. What is more, the omental, diaphragmatic and hepatic surfaces are carefully assessed. A 5‐mm trocar must be additionally inserted in a midline location to get full operational control of the small intestine, of the gastric parenchyma and the left hepatic lobe. Of note, setting the surgical table at an angle enables movement of the abdominal organs to gain a better surgical approach to the gastric region. The celiac and perigastric lymph nodes are de visu assessed in the liver hilum area, along the lesser and greater gastric curvature and along the hepato-gastric ligament. Given that the N parameter staging is currently debated, in some situations, a bioptic specimen of a single lymph node can be essential in order to evaluate the best therapeutic strategy to be applied (not for an accurate N staging, strictly depending on the number of metastatic nodes). This could be useful when node involvement is highly suspected at preoperative imaging, but there is not any de visu extra-serosal invasion evidence of the primary tumor during the video-laparoscopic investigation. Tumors of the anterior gastric wall can be inspected without manipulation. A third further 5-/10‐mm trocar could be introduced at the right of the midline. This port potentially facilitates the exploration of the lesser sac via a small incision of the Bouchet lamina (a region without vessels in the gastrocolic ligament). This additional surgical maneuver is useful when a posteriorly located fixity is suspected or in case of cancer origin from the posterior wall. The surgical time of such a procedure is approximately 20 min (30 min in case of lesser sac exploration). As a matter of fact, multimodal imaging integrated with explorative laparoscopy may implement the staging accuracy (reported to range from 89 to 100% [6,10] ), modifying clinical staging in almost 60% of patients with treatment implications in almost half of the cases [11] .
Future Oncol. (2015) 11(3)
In our experience we performed laparoscopic staging in all the patients who did not present CT signs of distant metastases. This approach changed therapeutic strategy in 30% of patients otherwise addressed to immediate surgery. In particular, for 91 consecutive patients with gastric adenocarcinoma prospectively observed, we systematically planned CT scan and laparoscopic staging. A total of 15 patients (16%) were revealed with certain or suspected metastatic disease. In particular, 13 patients with liver metastases or peritoneal carcinomatosis were addressed to palliative therapy. Among the 15 patients, we included a patient with CT finding of enlarged para-aortic lymph nodes and another one with C4 finding at peritoneal lavage fluid exam. As for the other 76 patients, 28 (37%) were considered T1-T2N0 and were treated with surgical resection. The remaining 48 patients (63%) were considered patients with locally advanced gastric cancer. Thirty-three patients in this group (69%) directly received surgical treatment because they were considered not fit for preoperative therapy for symptoms, comorbidities or nonacceptance of preoperative chemotherapy, while seven patients (15%) were considered unresectable for T4b tumors. Hence, eight patients with locally advanced gastric cancer have been recruited in a preoperative chemotherapy protocol. Specifically, benefits of staging laparoscopy are intimately related to the avoidance of unnecessary (for indication or timing) surgery: in fact, the accuracy of this diagnostic modality leads to discriminate patients who may immediately undergo surgery from those with metastatic disease or who should receive a presurgical treatment, with a consequent better allocation of resources, as well as a postoperative hospital stay clearly shorter than that after an explorative laparotomy. As an example, a patient with a cT3–4 gastric cancer and no evidence of distant metastases at CT scan can undergo a neoadjuvant treatment. Neoadjuvant therapy has shown to have a compliance rate better than that of postoperative chemotherapy, and its results in terms of downstaging and, consequently, in curative resection are well known [12,13] ; anyway, in order to have satisfactory results, correct indications and accurate patient selection are mandatory. Conversely, another patient may have a positive cytology on the fluid withdrawn or a clear peritoneal carcinomatosis at staging laparoscopy,
future science group
Advantages of staging laparoscopy in gastric cancer negatively affecting any real curative possibility. In other words, for any surgeon it should be advisable at least to attempt to clarify any staging doubts derived from the low reliability of the imaging techniques. Otherwise a (wrongly selected) patient could have a poor outcome and, undoubtedly, the risk to negatively affect the interpretation of neoadjuvant efficacy is very high. This already occurred even more in the previous randomized controlled trials on perioperative chemotherapy [12,13] . Furthermore, in resectable T1–T2N0M0 gastric cancer, staging laparoscopy might confirm the extent of the disease and it can be quickly converted into operative surgery, both videolaparoscopic or open gastrectomy. Considering the various multimodal approaches to gastric cancer and the possibilities of a preoperative treatment, it is evident that laparoscopic exploration of the abdominal cavity can also be useful in restaging patients after neoadjuvant treatment, allowing the preliminary discrimination of responders from nonreponders [14] . In addition, staging laparoscopy has also been proposed as a diagnostic tool for detection of early recurrence of gastric cancer, showing again a higher accuracy than CT scan and PET in detecting peritoneal seeding, which is a common pattern of recurrence in gastric cancer patients [15] . Complications of staging laparoscopy globally occur with a low incidence and among them the most frequent ones are intra-abdominal organ iatrogenic damages, hemorrhage and infective processes. Of note, to our knowledge no procedure-related deaths have been reported so far. What is more, no adverse oncologic effects have been demonstrated [6] . The higher accuracy rate of staging laparoscopy may therefore avoid an References 1
2
Semelka RC, Martin DR, Balci C et al. Focal liver lesions: comparison of dual phase CT andmultisequence multiplanar MR imaging including dymamic gadolinium enhancement. J. Magn. Reson. Imaging 13, 397–401 (2001). Kinkel K, Lu Y, Both M et al. Detection of hepatic metastase from cancer of the gastrointestinal tract by using non-invasive imaging methods (US, CT, MR imaging, PET): a meta-analysis. Radiology 224, 748–756 (2002).
future science group
Editorial
unnecessary laparotomy, with its possible related complications, longer operating room time and longer hospital stay, with a consequent delay in the beginning of adjuvant treatment. Despite the demonstrated benefits of staging laparoscopy, the compliance of surgeons for this management approach in clinical practice is unclear [16] . Unfortunately, laparoscopic staging is not widely adopted and it still has some limitations: as no morphologic criterion to define a lymph node as metastatic has been proven, nodal involvement may be underestimated; a frozen section of enlarged nodes should be taken, and this increases the cost of the procedure. In conclusion, in the era of tailored treatment, the basis of optimized therapies is the correct evaluation of tumor spread and exact staging; since this cannot always be defined by traditional imaging, surgeons should get used to offering staging laparoscopy in patients with a gastric cancer (especially if >cT1) with no evidence of distant metastases, if no contraindications to laparoscopic surgery exist. It is true that no level 1 evidence has been proven for staging laparoscopy, but it is unquestionable that robust evidence is unlikely to be acquired in the future considering the obvious and convincing advantages of this staging modality. Financial & competing interests disclosure The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending or royalties. No writing assistance was utilized in the production of this manuscript.
3
Makino T, Fujiwara Y, Takiguchi S et al. Preoperative T staging of gastric cancer by multi-detector row computed tomography. Surgery 149(5), 672–679 (2011).
7
Anderson DN, Campbell S, Park KG. Accuracy of laparoscopic ultrasonography in the staging of upper gastrointestinal malignancy. Br. J. Surg. 83, 1424–1428 (1996).
4
Kwee RM, Kwee TC. Imaging in local staging of gastric cancer: a systematic review. J. Clin. Oncol. 25(15), 2107–2116 (2007).
8
5
Edge SB, Byrd DR, Compton CC et al. AJCC Cancer Staging Manual (7th Edition). Springer, New York, NY, USA (2011).
Finch MD, John TG, Garden OJ, Allan PL, Paterson-Brown S. Laparoscopic ultrasonography for staging gastroesophageal cancer. Surgery 121, 10–17 (1997).
9
Richards DG. Endoscopic ultrasound in the staging of tumours of the esophagus and gastro-esophageal junction. Ann. R. Coll. Surg. Engl. 82, 311–317 (2000).
6
Chang L, Stefanidis D, Richardson WS et al. The role of staging laparoscopy for intraabdominal cancers: an evidence-based review. Surg. Endosc. 23, 231–241 (2009).
10 D’Ugo DM, Pende V, Persiani R et al.
Laparoscopic staging of gastric cancer:
www.futuremedicine.com
371
Editorial Rausei, Ruspi, Mangano et al. an overview. J. Am. Coll. Surg. 196(6), 965–974 (2003). 11 Blackshaw GRJC, Barry JD, Edwards P,
Allison MC, Thomas GV, Lewis WG. Laparoscopy significantly improve the perceived preoperative stage of gastric cancer. Gastric Cancer 6, 225–229 (2003). 12 Cunningham D, Allum WH, Stenning SP
et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N. Engl. J. Med. 355, 11–20 (2006).
372
13 Ychou M, Boige V, Pignon JP et al.
Perioperative chemotherapy compared with surgery alone for resectable gastroesophageal adenocarcinoma: an FNCLCC and FFCD multicenter Phase III trial. J. Clin. Oncol. 29, 1715–1721 (2011). 14 Cardona K, Zhou Q, Gonen M et al. Role of
repeat staging laparoscopy in locoregionally advanced gastric or gastroesophageal cancer after neoadjuvant therapy. Ann. Surg. Oncol. 20, 548–554 (2013).
Future Oncol. (2015) 11(3)
15 Shim JH, Yoo HM, Lee HH et al. Use of
laparoscopy as an alternative to computed tomography (CT) and positron emission tomography (PET) scans for the detection of recurrence in patients with gastric cancer: a pilot study. Surg. Endosc. 25, 3338–3344 (2011). 16 Karanicolas PJ, Elkin EB, Jacks LM et al.
Staging laparoscopy in the management of gastric cancer: a population-based analysis. J. Am. Coll. Surg. 213(5), 644–652 (2011).
future science group
