Stomach cancer surgery: Difference between revisions
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* Tumor size <20 mm in diameter | * Tumor size <20 mm in diameter | ||
* Differentiated intestinal histology | * Differentiated intestinal histology | ||
In most trials, there are no differences in outcome between the surgical and the endoscopic treatment. | In most trials, there are no differences in outcome between the surgical and the endoscopic treatment.<ref name="pmid16301028">{{cite journal| author=Etoh T, Katai H, Fukagawa T, Sano T, Oda I, Gotoda T et al.| title=Treatment of early gastric cancer in the elderly patient: results of EMR and gastrectomy at a national referral center in Japan. | journal=Gastrointest Endosc | year= 2005 | volume= 62 | issue= 6 | pages= 868-71 | pmid=16301028 | doi=10.1016/j.gie.2005.09.012 | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=16301028 }}</ref> | ||
==== Standard criteria for endoscopic resection: ==== | ==== Standard criteria for endoscopic resection:<ref name="pmid27664260">{{cite journal| author=Smyth EC, Verheij M, Allum W, Cunningham D, Cervantes A, Arnold D et al.| title=Gastric cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. | journal=Ann Oncol | year= 2016 | volume= 27 | issue= suppl 5 | pages= v38-v49 | pmid=27664260 | doi=10.1093/annonc/mdw350 | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=27664260 }}</ref><ref name="pmid24914327">{{cite journal| author=Bollschweiler E, Berlth F, Baltin C, Mönig S, Hölscher AH| title=Treatment of early gastric cancer in the Western World. | journal=World J Gastroenterol | year= 2014 | volume= 20 | issue= 19 | pages= 5672-8 | pmid=24914327 | doi=10.3748/wjg.v20.i19.5672 | pmc=4024776 | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=24914327 }}</ref> ==== | ||
1) Confined to the mucosa | 1) Confined to the mucosa | ||
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4) Without ulcer or ulcer scar | 4) Without ulcer or ulcer scar | ||
5) Without venous or lymphatic involvement | 5) Without venous or lymphatic involvement | ||
'''Expansion of the criteria''' to involve more tumors eligible for endoscopic resection was suggested by japanese centers and these criteria include | '''Expansion of the criteria''' to involve more tumors eligible for endoscopic resection was suggested by japanese centers and these criteria include:<ref name="pmid23023388">{{cite journal| author=Lee JH, Choi MG, Min BH, Noh JH, Sohn TS, Bae JM et al.| title=Predictive factors for lymph node metastasis in patients with poorly differentiated early gastric cancer. | journal=Br J Surg | year= 2012 | volume= 99 | issue= 12 | pages= 1688-92 | pmid=23023388 | doi=10.1002/bjs.8934 | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=23023388 }}</ref> | ||
* Differentiated type without ulceration, and mucosal tumors of any size | * Differentiated type without ulceration, and mucosal tumors of any size | ||
* Differentiated type, with ulceration, and mucosal tumors less than 30 mm | * Differentiated type, with ulceration, and mucosal tumors less than 30 mm | ||
* Undifferentiated type, without ulceration, and mucosal tumors 20 mm in size or smaller | * Undifferentiated type, without ulceration, and mucosal tumors 20 mm in size or smaller | ||
In a Japanese report of 131 patients with differentiated mucosal early gastric cancer less than 2 cm, the 5- and 10-year overall survival rates were 84 and 64 percent, respectively. The disease-specific survival rates at both 5- and 10-year follow-up were 99 percent | In a Japanese report of 131 patients with differentiated mucosal early gastric cancer less than 2 cm, the 5- and 10-year overall survival rates were 84 and 64 percent, respectively. The disease-specific survival rates at both 5- and 10-year follow-up were 99 percent. | ||
==== Methods of endoscopic resection ==== | ==== Methods of endoscopic resection<ref name="pmid26317585">{{cite journal| author=Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T, Repici A, Vieth M, De Ceglie A et al.| title=Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. | journal=Endoscopy | year= 2015 | volume= 47 | issue= 9 | pages= 829-54 | pmid=26317585 | doi=10.1055/s-0034-1392882 | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=26317585 }}</ref> ==== | ||
* Endoscopic mucosal resection (EMR): The lesion, together with the surrounding mucosa, is lifted by submucosal injection of saline and removed using a high-frequency steel snare. | * Endoscopic mucosal resection (EMR): The lesion, together with the surrounding mucosa, is lifted by submucosal injection of saline and removed using a high-frequency steel snare. | ||
* Endoscopic submucosal dissection (ESD): The mucosa surrounding the lesion is circumferentially incised using a high-frequency electric knife | * Endoscopic submucosal dissection (ESD): The mucosa surrounding the lesion is circumferentially incised using a high-frequency electric knife | ||
* ESD is more likely to result in complete resection of early gastric cancer | * ESD is more likely to result in complete resection of early gastric cancer | ||
* ESD requires more procedure time and endoscopic skill | * ESD requires more procedure time and endoscopic skill | ||
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===== '''Bleeding''' ===== | ===== '''Bleeding''' ===== | ||
* Bleeding was observed in 30 percent of cases. | * Bleeding was observed in 30 percent of cases.<ref name="pmid22402983">{{cite journal| author=Nishide N, Ono H, Kakushima N, Takizawa K, Tanaka M, Matsubayashi H et al.| title=Clinical outcomes of endoscopic submucosal dissection for early gastric cancer in remnant stomach or gastric tube. | journal=Endoscopy | year= 2012 | volume= 44 | issue= 6 | pages= 577-83 | pmid=22402983 | doi=10.1055/s-0031-1291712 | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=22402983 }}</ref> | ||
* A tumor size of more than 4 cm is a risk factor for acute bleeding and antithrombotic drug therapy is a risk factor for delayed bleeding. | * A tumor size of more than 4 cm is a risk factor for acute bleeding and antithrombotic drug therapy is a risk factor for delayed bleeding. | ||
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===== '''Perforation''' ===== | ===== '''Perforation''' ===== | ||
* Perforation rate for ESD is 4.5 percent, compared with 1.0 percent for EMR | * Perforation rate for ESD is 4.5 percent, compared with 1.0 percent for EMR.<ref name="pmid19621730">{{cite journal| author=Abe Y, Inamori M, Iida H, Endo H, Akiyama T, Yoneda K et al.| title=Clinical characteristics of patients with gastric perforation following endoscopic submucosal resection for gastric cancer. | journal=Hepatogastroenterology | year= 2009 | volume= 56 | issue= 91-92 | pages= 921-4 | pmid=19621730 | doi= | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=19621730 }}</ref> | ||
* Tumor location in the upper stomach and size more than 2 cm have been associated with an increased risk of perforation with ESD | * Tumor location in the upper stomach and size more than 2 cm have been associated with an increased risk of perforation with ESD. | ||
* Treatment of a perforation is endoscopic clipping, open or laparoscopic surgery in case of failed clipping | * Treatment of a perforation is endoscopic clipping, open or laparoscopic surgery in case of failed clipping. | ||
==== Curative resection ==== | ==== Curative resection ==== | ||
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==== '''Managing noncurative resection''' ==== | ==== '''Managing noncurative resection''' ==== | ||
* There is no standard approach for managing these patients noncurative resection. Gastrectomy has been recommended especially for tumors associated with a higher risk for lymph node metastases. | * There is no standard approach for managing these patients noncurative resection. Gastrectomy has been recommended especially for tumors associated with a higher risk for lymph node metastases. | ||
* Gastrectomy with removal of perigastric lymph nodes is recommended for such patients | * Gastrectomy with removal of perigastric lymph nodes is recommended for such patients. | ||
* Seven percent of patients who had gastrectomy and lymph node dissection after noncurative endoscopic resection for early gastric cancer had lymph node metastasis after that. | * Seven percent of patients who had gastrectomy and lymph node dissection after noncurative endoscopic resection for early gastric cancer had lymph node metastasis after that. | ||
==== '''Positive margins management''' ==== | ==== '''Positive margins management''' ==== | ||
* Patients with only positive '''lateral margins''' can be managed with further endoscopic therapy rather than surgery. Almost 90 percent of lateral psotitve margins were followed endoscopically with no recurrences. | * Patients with only positive '''lateral margins''' can be managed with further endoscopic therapy rather than surgery. Almost 90 percent of lateral psotitve margins were followed endoscopically with no recurrences. | ||
* Patients with positive '''vertical margins''', submucosal invasion, or lymphovascular invasion, are treated by surgery. | * Patients with positive '''vertical margins''', submucosal invasion, or lymphovascular invasion, are treated by surgery. | ||
==== Local recurrence after EMR/ESD ==== | ==== Local recurrence after EMR/ESD ==== | ||
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==== Non-curative surgery ==== | ==== Non-curative surgery ==== | ||
* '''Palliative surgery:''' Palliative gastrectomy or gastrojejunostomy is selected depending on the resectability of the primary tumor and surgical risks to relieve symptoms such as bleeding or obstruction. Gastrojejunostomy has been reported to result in superior function compared to simple gastrojejunostomy | * '''Palliative surgery:''' Palliative gastrectomy or gastrojejunostomy is selected depending on the resectability of the primary tumor and surgical risks to relieve symptoms such as bleeding or obstruction. Gastrojejunostomy has been reported to result in superior function compared to simple gastrojejunostomy. | ||
* '''Reduction surgery:''' Reduction surgery aims to prolong survival or to delay the onset of symptoms by reducing tumor volume. | * '''Reduction surgery:''' Reduction surgery aims to prolong survival or to delay the onset of symptoms by reducing tumor volume. | ||
=== Surgeries for gastric cancer === | === Surgeries for gastric cancer === | ||
* '''Total gastrectomy''': Total resection of the stomach '''including the cardia''' and pylorus | * '''Total gastrectomy''': Total resection of the stomach '''including the cardia''' and pylorus | ||
* '''Distal gastrectomy:''' Stomach resection including the pylorus. The '''cardia is preserved''' | * '''Distal gastrectomy:''' Stomach resection including the pylorus. The '''cardia is preserved''' | ||
* '''Pylorus-preserving gastrectomy''': Stomach resection preserving the upper third of the stomach and the pylorus along with a portion of the antrum | * '''Pylorus-preserving gastrectomy''': Stomach resection preserving the upper third of the stomach and the pylorus along with a portion of the antrum | ||
* '''Proximal gastrectomy''': Stomach resection including the cardia (esophagogastric junction). The pylorus is preserved | * '''Proximal gastrectomy''': Stomach resection including the cardia (esophagogastric junction). The pylorus is preserved | ||
* '''Segmental gastrectomy:''' Circumferential resection of the stomach preserving the cardia and pylorus | * '''Segmental gastrectomy:''' Circumferential resection of the stomach preserving the cardia and pylorus | ||
* '''Local resection'''. | * '''Local resection'''. | ||
* '''Non-resectional surgery''' (bypass surgery, gastrostomy, jejunostomy) | * '''Non-resectional surgery''' (bypass surgery, gastrostomy, and jejunostomy) | ||
==== Determination of gastric resection ==== | ==== Determination of gastric resection ==== | ||
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==== Selection of the surgery ==== | ==== Selection of the surgery ==== | ||
* The standard surgical procedure for clinically node-positive | * The standard surgical procedure for clinically node-positive or T2-T4a tumors is total or distal gastrectomy. | ||
* Distal gastrectomy is selected when a satisfactory proximal resection margin can be obtained. | * '''Distal gastrectomy:''' It is selected when a satisfactory proximal resection margin can be obtained. | ||
* Pancreatic invasion by tumor requiring | * '''Pancreaticosplenectomy''': Pancreatic invasion by tumor requiring necessitates total gastrectomy regardless of the tumor location. | ||
* Total gastrectomy with splenectomy should be considered for tumors that are located along the greater curvature and harbor metastasis to no. 4 lymph nodes, even if the primary tumor could be removed by distal gastrectomy. | * '''Total gastrectomy with splenectomy''': It should be considered for tumors that are located along the greater curvature and harbor metastasis to no. 4 lymph nodes, even if the primary tumor could be removed by distal gastrectomy. | ||
* For adenocarcinoma located on the proximal side of the esophagogastric junction | * '''Esophagectomy and proximal gastrectomy''' should be considered for For adenocarcinoma located on the proximal side of the esophagogastric junction. | ||
* | * '''T1N0 tumors''': the following types of gastric resection can be considered according to tumor location: | ||
* Pylorus-preserving gastrectomy: for tumors in the middle portion of the stomach with the distal tumor border at least 4 cm proximal to the pylorus. | * '''Pylorus-preserving gastrectomy''': for tumors in the middle portion of the stomach with the distal tumor border at least 4 cm proximal to the pylorus. | ||
* Proximal gastrectomy: for proximal tumors where more than half of the distal stomach can be preserved | * '''Proximal gastrectomy''': for proximal tumors where more than half of the distal stomach can be preserved. | ||
=== Lymph nodes resection === | === Lymph nodes resection === | ||
* One of the most controversial areas in the surgical management of gastric cancer is the optimal extent of lymph node dissection. | * One of the most controversial areas in the surgical management of gastric cancer is the optimal extent of lymph node dissection.<ref name="pmid11147594">{{cite journal| author=Noguchi Y, Yoshikawa T, Tsuburaya A, Motohashi H, Karpeh MS, Brennan MF| title=Is gastric carcinoma different between Japan and the United States? | journal=Cancer | year= 2000 | volume= 89 | issue= 11 | pages= 2237-46 | pmid=11147594 | doi= | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=11147594 }}</ref> | ||
* The draining lymph nodes for the stomach have been meticulously divided into 16 stations by Japanese surgeons; stations 1 to 6 are perigastric, and the remaining 10 are located adjacent to major vessels, behind the pancreas, and along the aorta | * The draining lymph nodes for the stomach have been meticulously divided into 16 stations by Japanese surgeons; stations 1 to 6 are perigastric, and the remaining 10 are located adjacent to major vessels, behind the pancreas, and along the aorta.<ref name="pmid21573743">{{cite journal| author=Japanese Gastric Cancer Association| title=Japanese classification of gastric carcinoma: 3rd English edition. | journal=Gastric Cancer | year= 2011 | volume= 14 | issue= 2 | pages= 101-12 | pmid=21573743 | doi=10.1007/s10120-011-0041-5 | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=21573743 }}</ref> | ||
'''D1 lymphadenectomy''' | |||
* It refers to a limited dissection of only the perigastric lymph nodes. It is indicated for T1N0 tumors other than the above. A D1 lymphadenectomy is indicated for T1a tumors that do not meet the criteria for EMR/ ESD and for T1bN0 tumors that are histologically of differentiated type and 1.5 cm or smaller in diameter. | |||
'''D2 lymphadenectomy''' | |||
* It is an extended lymph node dissection, includes removal of nodes along the hepatic, left gastric, celiac, and splenic arteries, as well as those in the splenic hilum (stations 1 to 11). It is indicated for potentially curable T2-T4 tumors as well as T1N+ tumors. A D2 lymphadenectomy should be performed whenever nodal involvement is suspected. | |||
'''D3 dissection''' | |||
* It is a superextended lymphadenectomy. The surgery includes D2 lymphadenectomy plus the removal of nodes within the porta hepatis and periaortic regions.<ref name="pmid18669424">{{cite journal| author=Sasako M, Sano T, Yamamoto S, Kurokawa Y, Nashimoto A, Kurita A et al.| title=D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer. | journal=N Engl J Med | year= 2008 | volume= 359 | issue= 5 | pages= 453-62 | pmid=18669424 | doi=10.1056/NEJMoa0707035 | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=18669424 }}</ref> | |||
=== Miscellaneous procedures === | === Miscellaneous procedures === | ||
'''Vagal nerve preservation''' | '''Vagal nerve preservation<ref name="pmid27342689">{{cite journal| author=Japanese Gastric Cancer Association| title=Japanese gastric cancer treatment guidelines 2014 (ver. 4). | journal=Gastric Cancer | year= 2017 | volume= 20 | issue= 1 | pages= 1-19 | pmid=27342689 | doi=10.1007/s10120-016-0622-4 | pmc=5215069 | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=27342689 }}</ref>''' | ||
It is reported that preservation of the hepatic branch of the anterior vagus and/or the celiac branch of the posterior vagus contributes to improving postoperative quality of life through reducing post-gastrectomy gallstone formation, diarrhea and/or weight loss. In case of PPG, the hepatic branch should be preserved to maintain the pyloric function. | It is reported that preservation of the hepatic branch of the anterior vagus and/or the celiac branch of the posterior vagus contributes to improving postoperative quality of life through reducing post-gastrectomy gallstone formation, diarrhea and/or weight loss. In case of PPG, the hepatic branch should be preserved to maintain the pyloric function. | ||
'''Omentectomy''' | '''Omentectomy'''<ref name="pmid25436387">{{cite journal| author=Kim JY, Ha TK, le Roux CW| title=Metabolic effects of gastrectomy with or without omentectomy in gastric cancer. | journal=Hepatogastroenterology | year= 2014 | volume= 61 | issue= 134 | pages= 1830-4 | pmid=25436387 | doi= | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=25436387 }}</ref> | ||
Removal of the greater omentum is usually integrated in the standard gastrectomy for T3 | Removal of the greater omentum is usually integrated in the standard gastrectomy for T3 or deeper tumors. For T1/T2 tumors, the omentum more than 3 cm away from the gastroepiploic arcade may be preserved. | ||
'''Bursectomy''' | '''Bursectomy'''<ref name="pmid25704429">{{cite journal| author=Hirao M, Kurokawa Y, Fujita J, Imamura H, Fujiwara Y, Kimura Y et al.| title=Long-term outcomes after prophylactic bursectomy in patients with resectable gastric cancer: Final analysis of a multicenter randomized controlled trial. | journal=Surgery | year= 2015 | volume= 157 | issue= 6 | pages= 1099-105 | pmid=25704429 | doi=10.1016/j.surg.2014.12.024 | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=25704429 }}</ref> | ||
For tumors penetrating the serosa of the posterior gastric wall, bursectomy (removal of the inner peritoneal surface of the bursa omentalis) may be performed with the aim of removing microscopic tumor deposits in the lesser sac. There is no evidence that bursectomy reduces peritoneal or local recurrence, and it should be avoided in T1/T2 tumors to prevent injury to the pancreas and/or adjacent blood vessels. A small-scale randomized controlled trial recently suggested a survival benefit for bursectomy in T3/T4a tumors | For tumors penetrating the serosa of the posterior gastric wall, bursectomy (removal of the inner peritoneal surface of the bursa omentalis) may be performed with the aim of removing microscopic tumor deposits in the lesser sac. There is no evidence that bursectomy reduces peritoneal or local recurrence, and it should be avoided in T1/T2 tumors to prevent injury to the pancreas and/or adjacent blood vessels. A small-scale randomized controlled trial recently suggested a survival benefit for bursectomy in T3/T4a tumors. | ||
=== | === Options of local palliation=== | ||
Therapeutic options to control symptoms of local disease progression, such as nausea, pain, bleeding, and obstruction, include palliative surgical resection, surgical bypass (gastrojejunostomy), radiation therapy (RT), and endoscopic techniques. | Therapeutic options to control symptoms of local disease progression, such as nausea, pain, bleeding, and obstruction, include palliative surgical resection, surgical bypass (gastrojejunostomy), radiation therapy (RT), and endoscopic techniques. | ||
'''Palliative resection''' | '''Palliative resection''' | ||
Palliative gastrectomy should be reserved for extreme, highly symptomatic cases where less invasive methods cannot be used. | Palliative gastrectomy should be reserved for extreme, highly symptomatic cases where less invasive methods cannot be used.<ref name="pmid10791239">{{cite journal| author=Kikuchi S, Arai Y, Kobayashi N, Tsukamoto H, Shimao H, Sakakibara Y et al.| title=Is extended lymphadenectomy valuable in palliatively gastrectomized patients with gastric cancer and simultaneous peritoneal metastasis? | journal=Hepatogastroenterology | year= 2000 | volume= 47 | issue= 32 | pages= 563-6 | pmid=10791239 | doi= | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=10791239 }}</ref> | ||
two-year survival for chemotherapy alone versus gastrectomy plus chemotherapy was 32 versus 25 percent. | two-year survival for chemotherapy alone versus gastrectomy plus chemotherapy was 32 versus 25 percent. | ||
patients undergoing gastrectomy had a significantly higher incidence of several serious adverse events related to chemotherapy, including leucopenia, nausea, anorexia, and hyponatremia. | patients undergoing gastrectomy had a significantly higher incidence of several serious adverse events related to chemotherapy, including leucopenia, nausea, anorexia, and hyponatremia. | ||
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'''Gastrojejunostomy''' | '''Gastrojejunostomy''' | ||
Palliative gastrojejunostomy for gastric outlet obstruction associated with unresectable advanced gastric cancer can improve food intake | Palliative gastrojejunostomy for gastric outlet obstruction associated with unresectable advanced gastric cancer can improve food intake.<ref name="pmid9762890">{{cite journal| author=Ouchi K, Sugawara T, Ono H, Fujiya T, Kamiyama Y, Kakugawa Y et al.| title=Therapeutic significance of palliative operations for gastric cancer for survival and quality of life. | journal=J Surg Oncol | year= 1998 | volume= 69 | issue= 1 | pages= 41-4 | pmid=9762890 | doi= | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=9762890 }}</ref> | ||
palliative gastrojejunostomy for patients with metastatic gastric cancer is reserved for cases where less invasive methods cannot be used. | palliative gastrojejunostomy for patients with metastatic gastric cancer is reserved for cases where less invasive methods cannot be used. | ||
'''Endoscopic stent placement''' | '''Endoscopic stent placement''' | ||
For palliation of obstructive symptoms, endoscopic placement of a stent provides a less invasive alternative to surgery for symptom palliation and may possibly be more effective in symptom relief. | For palliation of obstructive symptoms, endoscopic placement of a stent provides a less invasive alternative to surgery for symptom palliation and may possibly be more effective in symptom relief.<ref name="pmid10905359">{{cite journal| author=Wu KL, Tsao WL, Shyu RY| title=Low-power laser therapy for gastrointestinal neoplasia. | journal=J Gastroenterol | year= 2000 | volume= 35 | issue= 7 | pages= 518-23 | pmid=10905359 | doi= | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=10905359 }}</ref> | ||
stenting may achieve a better quality of life compared with other forms of palliation | stenting may achieve a better quality of life compared with other forms of palliation. | ||
In a review of two randomized trials of endoscopic stenting versus palliative gastrojejunostomy, there were no statistically significant differences between the two procedures in terms of efficacy or complications | In a review of two randomized trials of endoscopic stenting versus palliative gastrojejunostomy, there were no statistically significant differences between the two procedures in terms of efficacy or complications.<ref name="pmid17559659">{{cite journal| author=Jeurnink SM, van Eijck CH, Steyerberg EW, Kuipers EJ, Siersema PD| title=Stent versus gastrojejunostomy for the palliation of gastric outlet obstruction: a systematic review. | journal=BMC Gastroenterol | year= 2007 | volume= 7 | issue= | pages= 18 | pmid=17559659 | doi=10.1186/1471-230X-7-18 | pmc=1904222 | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=17559659 }}</ref> | ||
'''Endoscopic laser therapy''' | '''Endoscopic laser therapy''' | ||
Laser photocoagulation can be effective, particularly for large tumors with diffuse bleeding | Laser photocoagulation can be effective, particularly for large tumors with diffuse bleeding. | ||
An alternative that is being used increasingly is argon plasma coagulation. | An alternative that is being used increasingly is argon plasma coagulation.<ref name="pmid8751226">{{cite journal| author=Freitas D, Gouveia H, Sofia C, Cabral JP, Donato A| title=Endoscopic Nd-YAG laser therapy as palliative treatment for esophageal and cardial cancer. | journal=Hepatogastroenterology | year= 1995 | volume= 42 | issue= 5 | pages= 633-7 | pmid=8751226 | doi= | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=8751226 }}</ref> | ||
=== Reconstruction after gastrectomy === | === Reconstruction after gastrectomy === | ||
'''Total gastrectomy''' | '''Total gastrectomy''' | ||
* Roux-en-Y esophagojejunostomy | * Roux-en-Y esophagojejunostomy<ref name="pmid26379405">{{cite journal| author=Xiao JW, Liu ZL, Ye PC, Luo YJ, Fu ZM, Zou Q et al.| title=Clinical comparison of antrum-preserving double tract reconstruction vs roux-en-Y reconstruction after gastrectomy for Siewert types II and III adenocarcinoma of the esophagogastric junction. | journal=World J Gastroenterol | year= 2015 | volume= 21 | issue= 34 | pages= 9999-10007 | pmid=26379405 | doi=10.3748/wjg.v21.i34.9999 | pmc=4566393 | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=26379405 }}</ref> | ||
* Jejunal interposition | * Jejunal interposition | ||
* Double tract method | * Double tract method | ||
'''Distal gastrectomy''' | '''Distal gastrectomy''' | ||
* Billroth I gastroduodenostomy | * Billroth I gastroduodenostomy<ref name="pmid26895918">{{cite journal| author=Byun C, Cui LH, Son SY, Hur H, Cho YK, Han SU| title=Linear-shaped gastroduodenostomy (LSGD): safe and feasible technique of intracorporeal Billroth I anastomosis. | journal=Surg Endosc | year= 2016 | volume= 30 | issue= 10 | pages= 4505-14 | pmid=26895918 | doi=10.1007/s00464-016-4783-3 | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=26895918 }}</ref> | ||
* Billroth II gastrojejunostomy | * Billroth II gastrojejunostomy | ||
* Roux-en-Y gastrojejunostomy | * Roux-en-Y gastrojejunostomy | ||
* Jejunal interposition | * Jejunal interposition | ||
'''Pylorus-preserving gastrectomy''' | '''Pylorus-preserving gastrectomy'''<ref name="pmid25243417">{{cite journal| author=Song P, Lu M, Pu F, Zhang D, Wang B, Zhao Q| title=Meta-analysis of pylorus-preserving gastrectomy for middle-third early gastric cancer. | journal=J Laparoendosc Adv Surg Tech A | year= 2014 | volume= 24 | issue= 10 | pages= 718-27 | pmid=25243417 | doi=10.1089/lap.2014.0123 | pmc= | url=https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=25243417 }}</ref> | ||
* Gastro-gastrostomy | * Gastro-gastrostomy | ||
* Proximal gastrectomy | * Proximal gastrectomy | ||
Revision as of 21:16, 13 November 2017
Editor-In-Chief: C. Michael Gibson, M.S., M.D. [1]Associate Editor(s)-in-Chief: Parminder Dhingra, M.D. [2]
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Overview
Surgery is the mainstay of treatment for stomach cancer.
Surgical management of early gastric cancer
Early gastric cancer is an invasive gastric cancer that invades no more than the submucosa whatever the lymph node metastasis condition (T1 and any N)
Endoscopic resection is suggested for:
- Patients without suspected lymph node involvement
- Tumor size <20 mm in diameter
- Differentiated intestinal histology
In most trials, there are no differences in outcome between the surgical and the endoscopic treatment.[1]
Standard criteria for endoscopic resection:[2][3]
1) Confined to the mucosa
2) Smaller than 2 cm for superficially elevated type lesions
3) Smaller than 1 cm for the flat and depressed type lesions
4) Without ulcer or ulcer scar
5) Without venous or lymphatic involvement
Expansion of the criteria to involve more tumors eligible for endoscopic resection was suggested by japanese centers and these criteria include:[4]
- Differentiated type without ulceration, and mucosal tumors of any size
- Differentiated type, with ulceration, and mucosal tumors less than 30 mm
- Undifferentiated type, without ulceration, and mucosal tumors 20 mm in size or smaller
In a Japanese report of 131 patients with differentiated mucosal early gastric cancer less than 2 cm, the 5- and 10-year overall survival rates were 84 and 64 percent, respectively. The disease-specific survival rates at both 5- and 10-year follow-up were 99 percent.
Methods of endoscopic resection[5]
- Endoscopic mucosal resection (EMR): The lesion, together with the surrounding mucosa, is lifted by submucosal injection of saline and removed using a high-frequency steel snare.
- Endoscopic submucosal dissection (ESD): The mucosa surrounding the lesion is circumferentially incised using a high-frequency electric knife
- ESD is more likely to result in complete resection of early gastric cancer
- ESD requires more procedure time and endoscopic skill
Side effects and complications:
Bleeding
- Bleeding was observed in 30 percent of cases.[6]
- A tumor size of more than 4 cm is a risk factor for acute bleeding and antithrombotic drug therapy is a risk factor for delayed bleeding.
- Bleeding treatment is injection therapy, electrocoagulation, ligation with a detectable snare, and endoscopic clipping.
Perforation
- Perforation rate for ESD is 4.5 percent, compared with 1.0 percent for EMR.[7]
- Tumor location in the upper stomach and size more than 2 cm have been associated with an increased risk of perforation with ESD.
- Treatment of a perforation is endoscopic clipping, open or laparoscopic surgery in case of failed clipping.
Curative resection
Criteria need to be fulfilled to consider endoscopic resection curative:
- En bloc resection
- Tumor size < 2 cm
- Histologically of differentiated type
- Staging of tumor < T1a
- Negative horizontal margin
- Negative vertical margin
- No lymphovascular infiltration
Any resection that does not satisfy any of the above criteria is considered non-curative.
Managing noncurative resection
- There is no standard approach for managing these patients noncurative resection. Gastrectomy has been recommended especially for tumors associated with a higher risk for lymph node metastases.
- Gastrectomy with removal of perigastric lymph nodes is recommended for such patients.
- Seven percent of patients who had gastrectomy and lymph node dissection after noncurative endoscopic resection for early gastric cancer had lymph node metastasis after that.
Positive margins management
- Patients with only positive lateral margins can be managed with further endoscopic therapy rather than surgery. Almost 90 percent of lateral psotitve margins were followed endoscopically with no recurrences.
- Patients with positive vertical margins, submucosal invasion, or lymphovascular invasion, are treated by surgery.
Local recurrence after EMR/ESD
Local mucosal recurrence after EMR/ESD for tumors that had fulfilled the absolute indication could be considered to meet the criteria for expanded indication and may be treated by another ESD.
Treatments after endoscopic resection
Treatments after curative resection
- Annual endoscopy with abdominal ultrasonography or CT scan follow-up is recommended.
- Helicobacter pylori should be examined and eradicated.
Treatment after non-curative resection
- Surgical treatment should be performed after non-curative resection such as endoscopic coagulation using a laser or argon-plasma coagulator.
Surgical management of invasive gastric cancer
Surgical eradication of a gastric tumor with resection of adjacent lymph nodes represents the best chance for long-term survival.
Types of gastric surgery
Curative surgery
- Standard gastrectomy: It is the principal surgical procedure performed with curative intent. It involves resection of at least two-thirds of the stomach with a D2 lymph node dissection. In the standard gastrectomy, two-thirds of the stomach is resected.
- Non-standard gastrectomy: In non-standard gastrectomy, the extent of gastric resection and/or lymphadenectomy is altered according to tumor stages.
- Modified surgery: The extent of gastric resection and lymphadenectomy is reduced compared to standard surgery.
- Extended surgery
- Gastrectomy with combined resection of adjacent involved organs
- Gastrectomy with extended lymphadenectomy exceeding D2
Non-curative surgery
- Palliative surgery: Palliative gastrectomy or gastrojejunostomy is selected depending on the resectability of the primary tumor and surgical risks to relieve symptoms such as bleeding or obstruction. Gastrojejunostomy has been reported to result in superior function compared to simple gastrojejunostomy.
- Reduction surgery: Reduction surgery aims to prolong survival or to delay the onset of symptoms by reducing tumor volume.
Surgeries for gastric cancer
- Total gastrectomy: Total resection of the stomach including the cardia and pylorus
- Distal gastrectomy: Stomach resection including the pylorus. The cardia is preserved
- Pylorus-preserving gastrectomy: Stomach resection preserving the upper third of the stomach and the pylorus along with a portion of the antrum
- Proximal gastrectomy: Stomach resection including the cardia (esophagogastric junction). The pylorus is preserved
- Segmental gastrectomy: Circumferential resection of the stomach preserving the cardia and pylorus
- Local resection.
- Non-resectional surgery (bypass surgery, gastrostomy, and jejunostomy)
Determination of gastric resection
- For T1 tumors, a gross resection margin of 2 cm should be obtained.
- Proximal margin of at least 3 cm is recommended for T2 or deeper tumors with an expansive growth pattern (types 1 and 2) and 5 cm for those with an infiltrative growth pattern (types 3 and 4).
- For tumors invading the esophagus, a 5-cm margin is not necessarily required, but frozen section examination of the resection line is desirable to ensure an R0 resection.
- When the tumor border is unclear, preoperative endoscopic marking by clips of the tumor border based on biopsy results will be helpful for decision making regarding the resection line.
Selection of the surgery
- The standard surgical procedure for clinically node-positive or T2-T4a tumors is total or distal gastrectomy.
- Distal gastrectomy: It is selected when a satisfactory proximal resection margin can be obtained.
- Pancreaticosplenectomy: Pancreatic invasion by tumor requiring necessitates total gastrectomy regardless of the tumor location.
- Total gastrectomy with splenectomy: It should be considered for tumors that are located along the greater curvature and harbor metastasis to no. 4 lymph nodes, even if the primary tumor could be removed by distal gastrectomy.
- Esophagectomy and proximal gastrectomy should be considered for For adenocarcinoma located on the proximal side of the esophagogastric junction.
- T1N0 tumors: the following types of gastric resection can be considered according to tumor location:
- Pylorus-preserving gastrectomy: for tumors in the middle portion of the stomach with the distal tumor border at least 4 cm proximal to the pylorus.
- Proximal gastrectomy: for proximal tumors where more than half of the distal stomach can be preserved.
Lymph nodes resection
- One of the most controversial areas in the surgical management of gastric cancer is the optimal extent of lymph node dissection.[8]
- The draining lymph nodes for the stomach have been meticulously divided into 16 stations by Japanese surgeons; stations 1 to 6 are perigastric, and the remaining 10 are located adjacent to major vessels, behind the pancreas, and along the aorta.[9]
D1 lymphadenectomy
- It refers to a limited dissection of only the perigastric lymph nodes. It is indicated for T1N0 tumors other than the above. A D1 lymphadenectomy is indicated for T1a tumors that do not meet the criteria for EMR/ ESD and for T1bN0 tumors that are histologically of differentiated type and 1.5 cm or smaller in diameter.
D2 lymphadenectomy
- It is an extended lymph node dissection, includes removal of nodes along the hepatic, left gastric, celiac, and splenic arteries, as well as those in the splenic hilum (stations 1 to 11). It is indicated for potentially curable T2-T4 tumors as well as T1N+ tumors. A D2 lymphadenectomy should be performed whenever nodal involvement is suspected.
D3 dissection
- It is a superextended lymphadenectomy. The surgery includes D2 lymphadenectomy plus the removal of nodes within the porta hepatis and periaortic regions.[10]
Miscellaneous procedures
Vagal nerve preservation[11]
It is reported that preservation of the hepatic branch of the anterior vagus and/or the celiac branch of the posterior vagus contributes to improving postoperative quality of life through reducing post-gastrectomy gallstone formation, diarrhea and/or weight loss. In case of PPG, the hepatic branch should be preserved to maintain the pyloric function.
Omentectomy[12]
Removal of the greater omentum is usually integrated in the standard gastrectomy for T3 or deeper tumors. For T1/T2 tumors, the omentum more than 3 cm away from the gastroepiploic arcade may be preserved.
Bursectomy[13]
For tumors penetrating the serosa of the posterior gastric wall, bursectomy (removal of the inner peritoneal surface of the bursa omentalis) may be performed with the aim of removing microscopic tumor deposits in the lesser sac. There is no evidence that bursectomy reduces peritoneal or local recurrence, and it should be avoided in T1/T2 tumors to prevent injury to the pancreas and/or adjacent blood vessels. A small-scale randomized controlled trial recently suggested a survival benefit for bursectomy in T3/T4a tumors.
Options of local palliation
Therapeutic options to control symptoms of local disease progression, such as nausea, pain, bleeding, and obstruction, include palliative surgical resection, surgical bypass (gastrojejunostomy), radiation therapy (RT), and endoscopic techniques.
Palliative resection
Palliative gastrectomy should be reserved for extreme, highly symptomatic cases where less invasive methods cannot be used.[14]
two-year survival for chemotherapy alone versus gastrectomy plus chemotherapy was 32 versus 25 percent.
patients undergoing gastrectomy had a significantly higher incidence of several serious adverse events related to chemotherapy, including leucopenia, nausea, anorexia, and hyponatremia.
Gastrojejunostomy
Palliative gastrojejunostomy for gastric outlet obstruction associated with unresectable advanced gastric cancer can improve food intake.[15]
palliative gastrojejunostomy for patients with metastatic gastric cancer is reserved for cases where less invasive methods cannot be used.
Endoscopic stent placement
For palliation of obstructive symptoms, endoscopic placement of a stent provides a less invasive alternative to surgery for symptom palliation and may possibly be more effective in symptom relief.[16]
stenting may achieve a better quality of life compared with other forms of palliation.
In a review of two randomized trials of endoscopic stenting versus palliative gastrojejunostomy, there were no statistically significant differences between the two procedures in terms of efficacy or complications.[17]
Endoscopic laser therapy
Laser photocoagulation can be effective, particularly for large tumors with diffuse bleeding.
An alternative that is being used increasingly is argon plasma coagulation.[18]
Reconstruction after gastrectomy
Total gastrectomy
- Roux-en-Y esophagojejunostomy[19]
- Jejunal interposition
- Double tract method
Distal gastrectomy
- Billroth I gastroduodenostomy[20]
- Billroth II gastrojejunostomy
- Roux-en-Y gastrojejunostomy
- Jejunal interposition
Pylorus-preserving gastrectomy[21]
- Gastro-gastrostomy
- Proximal gastrectomy
- Esophagogastrostomy
- Jejunal interposition
- Double tract method
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| M0 | M1 | ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| T1 | T2,T3,T4A | T4B | |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| N0 | N1 | ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| T1a | T1b | ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| Differenitated,≤1.5cm | Differenitated,≤1.5cm | ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| H01 | H02 | H03 | H04 | ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| {{{ I01 }}} | {{{ I02 }}} | {{{I03}}} | {{{I04}}} | ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
References
- ↑ Etoh T, Katai H, Fukagawa T, Sano T, Oda I, Gotoda T; et al. (2005). "Treatment of early gastric cancer in the elderly patient: results of EMR and gastrectomy at a national referral center in Japan". Gastrointest Endosc. 62 (6): 868–71. doi:10.1016/j.gie.2005.09.012. PMID 16301028.
- ↑ Smyth EC, Verheij M, Allum W, Cunningham D, Cervantes A, Arnold D; et al. (2016). "Gastric cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up". Ann Oncol. 27 (suppl 5): v38–v49. doi:10.1093/annonc/mdw350. PMID 27664260.
- ↑ Bollschweiler E, Berlth F, Baltin C, Mönig S, Hölscher AH (2014). "Treatment of early gastric cancer in the Western World". World J Gastroenterol. 20 (19): 5672–8. doi:10.3748/wjg.v20.i19.5672. PMC 4024776. PMID 24914327.
- ↑ Lee JH, Choi MG, Min BH, Noh JH, Sohn TS, Bae JM; et al. (2012). "Predictive factors for lymph node metastasis in patients with poorly differentiated early gastric cancer". Br J Surg. 99 (12): 1688–92. doi:10.1002/bjs.8934. PMID 23023388.
- ↑ Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T, Repici A, Vieth M, De Ceglie A; et al. (2015). "Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) Guideline". Endoscopy. 47 (9): 829–54. doi:10.1055/s-0034-1392882. PMID 26317585.
- ↑ Nishide N, Ono H, Kakushima N, Takizawa K, Tanaka M, Matsubayashi H; et al. (2012). "Clinical outcomes of endoscopic submucosal dissection for early gastric cancer in remnant stomach or gastric tube". Endoscopy. 44 (6): 577–83. doi:10.1055/s-0031-1291712. PMID 22402983.
- ↑ Abe Y, Inamori M, Iida H, Endo H, Akiyama T, Yoneda K; et al. (2009). "Clinical characteristics of patients with gastric perforation following endoscopic submucosal resection for gastric cancer". Hepatogastroenterology. 56 (91–92): 921–4. PMID 19621730.
- ↑ Noguchi Y, Yoshikawa T, Tsuburaya A, Motohashi H, Karpeh MS, Brennan MF (2000). "Is gastric carcinoma different between Japan and the United States?". Cancer. 89 (11): 2237–46. PMID 11147594.
- ↑ Japanese Gastric Cancer Association (2011). "Japanese classification of gastric carcinoma: 3rd English edition". Gastric Cancer. 14 (2): 101–12. doi:10.1007/s10120-011-0041-5. PMID 21573743.
- ↑ Sasako M, Sano T, Yamamoto S, Kurokawa Y, Nashimoto A, Kurita A; et al. (2008). "D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer". N Engl J Med. 359 (5): 453–62. doi:10.1056/NEJMoa0707035. PMID 18669424.
- ↑ Japanese Gastric Cancer Association (2017). "Japanese gastric cancer treatment guidelines 2014 (ver. 4)". Gastric Cancer. 20 (1): 1–19. doi:10.1007/s10120-016-0622-4. PMC 5215069. PMID 27342689.
- ↑ Kim JY, Ha TK, le Roux CW (2014). "Metabolic effects of gastrectomy with or without omentectomy in gastric cancer". Hepatogastroenterology. 61 (134): 1830–4. PMID 25436387.
- ↑ Hirao M, Kurokawa Y, Fujita J, Imamura H, Fujiwara Y, Kimura Y; et al. (2015). "Long-term outcomes after prophylactic bursectomy in patients with resectable gastric cancer: Final analysis of a multicenter randomized controlled trial". Surgery. 157 (6): 1099–105. doi:10.1016/j.surg.2014.12.024. PMID 25704429.
- ↑ Kikuchi S, Arai Y, Kobayashi N, Tsukamoto H, Shimao H, Sakakibara Y; et al. (2000). "Is extended lymphadenectomy valuable in palliatively gastrectomized patients with gastric cancer and simultaneous peritoneal metastasis?". Hepatogastroenterology. 47 (32): 563–6. PMID 10791239.
- ↑ Ouchi K, Sugawara T, Ono H, Fujiya T, Kamiyama Y, Kakugawa Y; et al. (1998). "Therapeutic significance of palliative operations for gastric cancer for survival and quality of life". J Surg Oncol. 69 (1): 41–4. PMID 9762890.
- ↑ Wu KL, Tsao WL, Shyu RY (2000). "Low-power laser therapy for gastrointestinal neoplasia". J Gastroenterol. 35 (7): 518–23. PMID 10905359.
- ↑ Jeurnink SM, van Eijck CH, Steyerberg EW, Kuipers EJ, Siersema PD (2007). "Stent versus gastrojejunostomy for the palliation of gastric outlet obstruction: a systematic review". BMC Gastroenterol. 7: 18. doi:10.1186/1471-230X-7-18. PMC 1904222. PMID 17559659.
- ↑ Freitas D, Gouveia H, Sofia C, Cabral JP, Donato A (1995). "Endoscopic Nd-YAG laser therapy as palliative treatment for esophageal and cardial cancer". Hepatogastroenterology. 42 (5): 633–7. PMID 8751226.
- ↑ Xiao JW, Liu ZL, Ye PC, Luo YJ, Fu ZM, Zou Q; et al. (2015). "Clinical comparison of antrum-preserving double tract reconstruction vs roux-en-Y reconstruction after gastrectomy for Siewert types II and III adenocarcinoma of the esophagogastric junction". World J Gastroenterol. 21 (34): 9999–10007. doi:10.3748/wjg.v21.i34.9999. PMC 4566393. PMID 26379405.
- ↑ Byun C, Cui LH, Son SY, Hur H, Cho YK, Han SU (2016). "Linear-shaped gastroduodenostomy (LSGD): safe and feasible technique of intracorporeal Billroth I anastomosis". Surg Endosc. 30 (10): 4505–14. doi:10.1007/s00464-016-4783-3. PMID 26895918.
- ↑ Song P, Lu M, Pu F, Zhang D, Wang B, Zhao Q (2014). "Meta-analysis of pylorus-preserving gastrectomy for middle-third early gastric cancer". J Laparoendosc Adv Surg Tech A. 24 (10): 718–27. doi:10.1089/lap.2014.0123. PMID 25243417.