 |
| About Bioline | All Journals | Testimonials | Membership | News |
|
||||||
|
||||||
Indian Journal of Surgery, Vol. 65, No. 4, July-Aug, 2003, pp. 339-343 Review Article Conservative surgery in cancer of the stomach and the current status of lymph node dissections Mallika Tewari, Priya Hazra,* Anurag Dixit, H. S. Shukla The Division of Surgical Oncology, Institute of Medical Sciences, Banaras Hindu University, Varanasi 221005 and
*Department of Surgery, AIIMS, New Delhi, India.
Paper Received: March 2002. Paper Accepted: November 2002. Source of Support: Nil Key Words: Stomach cancer, Conservation surgery. How to cite this article: Tewari M, Hazra P, Dixit A, Shukla HS. Conservative surgery in cancer of the stomach and the current status of lymph node dissections. Indian J Surg 2003;65:336-43. Code Number: is03067 Introduction Partial gastrectomy, as described by Polya in 1911 has been practised widely.1 However, a recommendation for more radical operation was given by McNeer et al2 after their review of 92 postmortem examinations following partial gastrectomy for gastric cancer. In half the cases they found recurrence in the gastric remnant and therefore advised radical total gastrectomy with partial pancreatectomy and splenectomy. However, a study at Mayo Clinic analysing the long-term results following total gastrectomy in 170 cases, in which 78 % had involved nodes, showed a five-year survival of only 18 %.3 Only 10 % of the patients with a malignant lesion in the distal part of the stomach lived for five years. These results indicated that total gastrectomy was not the operation of choice for all gastric carcinomas. There is extensive literature on all aspects of gastric cancer. There is a trend indicating an increase of proximal tumours of diffuse type and a decrease in the incidence of stage IV cancers.4 Copious literature of surgical treatment of cancer of the stomach is available from Japan and the western world. A new category of early gastric cancer (EGC) has emerged as a result of aggressive surveillance in Japanese populations. EGC is defined histologically when the lesion is confined to the mucosa and submucosa.5 With early access endoscopy, EGC is diagnosed much more frequently.5-7 The revised classification of gastric cancer (GC) of the Japanese Gastric Cancer Association8 has recognized different macroscopic types. The endoscopic macroscopic type of lesion and level of submucosal involvement, as assessed by gastric sonography (sm1: superficial invasion, sm2: deep invasion), are reliable indicators (predictors) of regional lymph node involvement.9 However, the overall diagnostic accuracy of staging the T (primary tumour) category using endoscopic ultrasound (EUS) is only 85 %.9 The use of EUS is hampered by the problem of over- or under-staging.11 It is often difficult, especially in ulcerated GC, to differentiate between carcinoma and inflamed surrounding soft tissue and fibrosis.10 Furthermore, EUS is unable to detect micro-invasive cancer.12 The effectiveness of EUS is strongly dependent upon the training and experience of the investigator, but EUS is superior to CT scan in the determination of the overall T category (CT has a 15-42 % accuracy in staging).13-15 The diagnostic accuracy for the determination of N (nodal involvement) is reported to be 65-87 % (as compared to 25-68 % of CT scan).11 Only lymph nodes in close proximity to the gastric wall are revealed by EUS. Nodes that are invaded but not enlarged cannot be detected. Overall, EUS appears to be more accurate than percutaneous ultrasound or CT for evaluating N stage in EGC.10 There is an increasing frequency of the diagnosis of EGC in Japan (5-40% in 10 years)16 and excellent survival on conservative therapy (90-100 % 5-year survival). This has led to the belief that mass screening and differences in diagnostic criteria are the attributing factors. The criterion for EGC is invasion not deeper than the submucosa. Japanese pathologists give more importance to nuclear characteristics rather than invasiveness alone as criteria for diagnosing EGC. Improper sampling or sectioning of biopsy specimens and ramification of glands may make diagnosis of invasion difficult. What western pathologists would consider adenoma or dysplasia, the Japanese would label as EGC (elevated and flat type). Indeed, most such lesions progress to frank carcinoma over a period of time and sometimes without an intervening period of high-grade dysplasia. The Japanese technique for an early and accurate diagnosis of EGC17 has the merit of wider application. Surgical treatment of EGC Local endogastric ablation or removal, or wedge resection as against D1 or D2 lymph node dissection is done on tumours that are unlikely to spread to regional lymph nodes. Kim10 reported that the incidence of lymph node metastasis is 15.7 % in EGC. Even from western series, data indicate that risk of regional lymph node spread is increased when EGC invades the submucosa deeply19 (3-5 % against 16-25 % for mucosal versus submucosal cancers).20-24 At present, nodal dissection is not required for the following types of EGC:25 1. Papillary or tubular histology 2. EGC (II a) <= 2 cm or EGC (II c) <= 1 cm 3. No ulcerative change 4. Mucosal cancer There are four types of surgical procedures for EGC: 1. Endoscopic mucosal resection (EMR) The Japanese have popularized EMR for mucosal cancer.26 This approach involves submucosal injection of adrenaline with saline to elevate the lesion and complete mucosal resection. Takekoshi et al27 reported a series of 308 endoscopic resections for EGC. Forty-four patients had residual or recurrent lesion after EMR. All recurrences were again resected. In experienced hands, EMR is a suitable alternative to gastrectomy for favourable EGC. However, tumours invading the submucosa are not appropriate for endoscopic resection.28 These are to be treated by D2 dissection.29 EMR is also difficult in tumours of cardia. Cap-fitted endoscopes may be helpful for such lesions.30 Laser irradiation in addition to EMR is useful in reducing recurrences in high-risk groups.31 The disadvantage of laser therapy is the lack of resected specimen for histological evaluation. 2. Laparo-endoluminal resection22 This technique is an alternative to EMR, suited for lesions on the posterior wall of the stomach and fundus. Its use for benign mucosal lesions and early superficial gastric cancer has been reported in selected patients.32 However, it is unsuitable for lesions requiring full-thickness resection because it necessitates carbon dioxide insufflation of the stomach. 3. Trans-gastro-stomal endoscopic surgery First described by Yamashita et al, 23 it is useful for posterior wall lesions, and because it avoids the need for carbon dioxide insufflation, it is suitable for mucosectomies and full thickness excisions. 4. Laparoscopic gastric resection: (totally laparoscopic assisted and hand-assisted) 24 Laparoscopic wedge resection without lymphadenectomy may be adequate for small superficial lesions situated on the anterior wall close to the lesser curvature without significant submucosal involvement. Laparoscopic D1 gastrectomy seems ideal for EGC >3.0 cm with submucosal invasion (sm2). However, the reported data are limited, and any conclusions on the efficacy and safety are premature. Thus for EGC there exists a controversy in the choice of surgery, especially when the submucosa is invaded, as the accuracy of preoperative detection (CT, MRI, EUS) and value of sentinel node biopsy / intra-operative prediction of lymph node involvement remains low, especially in assessing micro-metastases and micro involvement of nodes. Locally advanced GC The optimal surgical resection for potentially curable advanced GC (involving the muscularis propria), varies between total to subtotal gastrectomy (SG) and D1-D2-D3 levels of lymph node dissections. The extent of gastric resection should provide optimal clearance with minimal attendant morbidity. Some surgeons favour total gastrectomy (TG) as an adequate treatment, while others believe that SG, where a safe proximal resection margin can be guaranteed, is an ideal procedure. GC of the distal part of the stomach is universally treated by SG. But for neoplasms located in the proximal area of the stomach and for multifocal lesions the application of proximal gastrectomy (PG) or limited resection is not the standard. Older (retrospective) data suggest that chances of survival are better with TG as compared with SG,34 however, the current evidence is not corroborative. Amongst the three prospective studies,35-37 the French Association for surgical research35 and the Norwegian Stomach Cancer Trial,38,46 did not show survival advantage based on extent of surgical resection. However, several retrospective studies demonstrated that DG offered a significantly better survival advantage over TG.39 Long-term consequences of gastrectomy procedures (TG, PG and DG) showed that subtotal DG or PG have advantages in the early postoperative period, at 3-6 months after gastrectomy, with respect to immunological assessment. This suggests a better chance of long-term survival. If the surgical margin is free of cancer, it is useful to avoid total resection of the stomach; this maintains immunological competence after resection of stomach.40 The risk of recurrence in gastric remnant following partial gastric resection exists theoretically. Preoperative detection of synchronous lesions and regular endoscopic surveillance for metachronous lesions can help in early detection of such cancers. But such cancers usually develop over 10 years after initial curative surgery (CS) and bile reflux has been proposed as an important predisposing factor. Considering the poor 5-year survival in advanced GC, at present such lesions result only in a theoretical dilemma. Analysis of risk factors for surgical treatment in the Dutch GC trial41 and by Sasako et al78,84 revealed that splenectomy increased morbidity and it is a high relative risk for hospital death, more so when SG with D2 dissection was performed. Ischaemia of the gastric remnant due to proximal ligation of left gastric artery in D2 dissection along with ligation of short gastric vessels during splenectomy can explain the adverse effects of splenectomy in D2 SG. It is recommended that if splenectomy is unavoidable due to injury during D2 dissection, TG should be performed regardless of the location of the primary tumour42,43 to avoid ischaemia which also occurs due to intramural vascular damage of the gastric stump when linear staplers are used for side-to-side gastro-jejunostomy (GJ). Subclinical pancreatic juice leakage, infection and method of reconstruction are other factors determining morbidity and mortality.44 There is an increase in the incidence of proximal gastric cancer.29 Poor prognosis of proximal gastric cancers45 is due to the advanced stage of presentation. The current TNM classification understages these tumours, as it does not take into account the partly retroperitoneal location of the proximal stomach. Involvement of mediastinal nodes is seen in 8.7 % cases having 1-2 cm of oesophageal invasion and in 15.9 % cases with > 4 cm invasion. Para-aortic node metastasis is seen in cases with even 1cm invasion. Thus D4 lymphadenectomy is preferable to D2 in carcinoma of the cardia.63 Carcinoma of the proximal one-third of the stomach has a worse prognosis than distal gastric lesions.47-49 TG has been the procedure of choice for proximal cancer. Review of the prospective gastric database28 at Memorial Sloan-Kettering Cancer Center from July 1985 to August 1995 revealed that mortality for PG and TG were not significantly different. The 5-year survival rate for PG was 43 % and for TG 41%. The recurrence-free interval after surgery was similar after both TG and PG. However, the results of the Norwegian Stomach Cancer Trial38 revealed postoperative mortality of 16% for PG, 8% for TG, 10% for SG, and 7% for DG. Factors significantly related to postoperative complications included advancing age, male gender, lack of antibiotic prophylaxis, and addition of splenectomy. Several series have reported 4-18% operative mortality after TG, and anastomotic leak is responsible for up to 50% of these operative deaths.50-52 Functional results after TG are worse than after DG.53-55 The quality of life (QOL) never reaches above preoperative level after TG whereas after SG and DG, patients have better QOL as compared to preoperative levels.40,56 The ability to completely dissect paracardial lymph nodes is not related to the extent of gastric resection.57 Thus TG should not be the first option in patients in whom a 6-cm gross proximal margin can be obtained with a subtotal resection.58 To improve the QOL of patients undergoing gastrectomy, conservative procedures such as (a) pylorus preserving gastrectomy with or without anterior seromuscular flap to aid dissection of pyloric nodes without damaging vagal fibers (b) preservation of lower oesophageal sphincter to prevent gastro-oesophageal reflux and (c) various methods of pouch reconstructions, have been proposed.59,60 A new paradigm for early stage I & II stomach cancer is laparoscopic gastric resection.9 D1 gastrectomy (total or antral) is eminently feasible through the laparoscopic or laparoscopic-assisted approach. D2 gastrectomy has also been performed laparoscopically. The largest reported series is by Azagra et al61 nine D1 and three D2 total gastrectomies have been reported. It is difficult to draw any conclusion from this limited early experience. There is concern regarding the quality of extended lymphadenectomy and the possibility of dissemination of this tumour, especially when the serosa of the stomach is involved.
Combined resection of adjacent organs
Survival benefit from resection of neighbouring organs, varying from local excision of adjacent organs to left upper abdominal evisceration when invaded by primary tumour, has been reported.62-64 On the contrary, the benefit of combined resection to achieve lymph node dissection is doubtful. A pancreas preserving TG (PPTG) has become a standard procedure for D2 TG in Japan.65 PPTG is technically more demanding than TG with pancreatico-splenectomy (TGPG).66 Ultrasonic dissectors have been found to be useful in pancreas and spleen preserving TG with radical lymphadenectomy.67 The results from MRC68 and Dutch trials41 indicate that pancreatico-splenectomy should not be a part of D2 resections. The consensus in literature is that prophylactic splenectomy increases morbidity and mortality without an apparent survival benefit.69-71 According to Okajima et al87 the indications for splenectomy are a) direct invasion into the pancreas or spleen b) metastasis to nodes along the splenic artery, and c) immunological demands i.e. preserve in stages I, II and III, and resect in stage IV.73,74 However, recent studies indicate that morbidity following splenectomy rather than immunosuppression is the cause for decreased survival after splenectomy.75 Pancreatectomy increases the rate of intra-abdominal sepsis.76 Use of prophylactic drains, particularly in the left subphrenic space and drainage of the distal cut end of the pancreas into a segment of bowel have been proposed as methods to reduce sepsis after pancreatectomy.90 Lymph node dissection for locally advanced curable GC The role of radical lymphadenectomy in the operative treatment of gastric adenocarcinoma remains controversial. Much better results of surgical treatment for this disease and long-term survival are constantly reported from Japan and some western centres with D2 resection78-80 than from the western world. The difference may be because of firstly a different inherent biology of GC in Japan from that in the west and secondly, technical factors such as the small and thin-built physique of Japanese patients as compared to their western counterparts that make lymphadenectomy technically easier. Japanese surgeons may, in addition, be more technically adept at extended lymphadenectomy because they frequently perform the operation.81 Retrospective classification of TNM categories in Japanese patients, differences in description of curative resection, different surgical procedures and variations in postoperative treatment modalities,77 have also been thought to contribute to this difference. Surgical and pathological stage migration, non-compliance and contamination confounds comparisons of survival rates between Japan and the West.82,83 The calculated value of stage migration on survival effect is as follows: 1a 1%, 1b 2%, 2 7%, 3a 15%, and 3b - 15%. The lymphatic drainage of the stomach is extensive, and distinct anatomical groups of lymph nodes have been defined according to their relationship to the stomach and its blood supply.18 The Japanese staging system extensively classifies 18 lymph node regions into 4 N categories depending on their relation to the primary tumour and anatomical location.1 Resection of the stomach and the surrounding lymph nodes in Japan is described as R-0, R-1, R-2, R-3 and R-4. An R-0 resection indicates a gastrectomy with incomplete resection of the N1 (perigastric) nodes, R-2, R-3, and R-4 resections involve progressive complete removal of all the nodes through N2, N3, and N4 respectively.81 At a meeting of WHO on GC held in Munich in 1993, the classification revolving around R for residual tumours was suggested by Maruyama.81 He suggested that the lymph node status be designated D. Thus, there would be R0 (no residual tumour), R1 (microscopic evidence of residual tumour after surgery) and R2 (macroscopic evidence of residual tumour).85 However, the exact lymph node groups to be resected in a D1 or greater operation differ somewhat according to the location of the primary tumour.33,81 Radical gastrectomy (RG) aiming at R0 resection is proven to be the best treatment, whether an extended lymph node dissection (ELND) is carried out or not. Certainly, the wider the lymph node dissection, the more accurate the staging, which leads to an apparent increased survival rate for several stages after extended dissection. Bunt91,92 demonstrated this phenomenon using stage-specific survival rates of GC patients.72,82 A retrospective analysis of a large number of advanced GC cases showed a high incidence of lymph node metastasis and good prognosis for those having metastasis even to second tier nodes78 following D2 dissection. In the situation where no alternative therapy can control lymph node metastasis, surgical resection seems to be the only means to control local extension of the disease. This paper showed the benefit of extended dissection without using any stratification by stage, thus circumventing the stage migration phenomenon. Another approach to circumvent stage migration was proposed by Sasako et al.96 They proposed multiplication of the incidence of metastasis and percentage 5-year survival rate of patients with metastasis for each station. For advanced cancers, considerable debate continues as to whether the routine use of an extensive en bloc resection of second-echelon lymph nodes (D2 dissection) is superior to limited lymphadenectomy of the perigastric lymph nodes (D1 dissection). Four prospective randomized trials36,41,68,79 have now been completed on this subject. Dent et al57,58 reported the first prospective randomized trial of D1versus D2 gastrectomy from Cape Town, South Africa. No difference in 5-year survival rates was found. The second randomized prospective trial comparing D1 SG to D3 TG was reported from Hong Kong.36 Median survival was significantly shorter in those undergoing D1 dissections. These trials lacked statistical power owing to small sample sizes. In the late 1980s, two randomized control trials were started in the UK68 and the Netherlands41 to assess if ELND has any therapeutic advantage in GC. The short-term results reported in 1995 by the Dutch group and in 1996 by the British group showed significantly worse results for D2 dissection in terms of postoperative mortality and morbidity. Long-term results could not show any significant difference in survival between the two treatment arms. However, such prospective randomized controlled trials cannot be conducted in Japan due to the general consensus regarding the benefits of ELND and the resulting ethical implications. Pancreatico-splenectomy was routinely performed as a part of D2 dissection in both the trials. The question whether D2 resection without pancreatico-splenectomy is better than standard D1 resection could not be answered by the results of these trials. Despite efforts made to ensure quality control in the Dutch trials of the two types of lymph node dissection, both non-compliance (not removing all lymph node stations) and contamination (removing more than was indicated) occurred, thus blurring the distinction between the two operations.86 Following the evaluation of 389 patients in 63 participating hospitals, Bunt et al83 noted 84% non-compliance in R1 and R2 resections respectively. Minor non-compliance (<3 node stations) was seen more commonly in R1 where as major non-compliance was seen in R2. Moderate contamination was present in both groups, however contamination was more common by Japanese surgeon. Investigations regarding the causes for such protocol deviation led to the following possible explanations.86 Lack of a learning curve in these trials also reflects an adequate experience during the whole trial period.86,87 1. Number of nodes per station 2. Clarity of anatomical situation 3. Location of stations 4. Local convention of gastrectomy 5. Technical considerations to allow en bloc dissection The survival advantage of D2 dissection over D1 is estimated as 10-15% in each stage, but becomes minimal if postoperative management and preoperative patient selection strongly affects the results of surgical treatment.29 It is now generally agreed that gastrectomy for advanced GC with curative intent is no longer a procedure for general hospitals88 and only hospitals performing more than 20-30 curative gastrectomies each year should treat GC patients. A prospective audit has revealed a learning curve of 18-24 months and 15 procedures before a plateau is reached.94 Multidisciplinary team approach in specialist centres and performance of D2 gastrectomy by specialists rather than general surgeons can help improve the results.89 Advancing age (>80 years), Borrmann type IV cancers, linitis plastica, presence of free intraperitoneal cells as demonstrated by peritoneal wash cytology, distant nodal metastasis and haematogenous metastatis remain the limits of radicality and palliative resections are better than palliation without resections in all such conditions.90, 91 In summary, the D2 operation is a systematic approach towards the removal of the high-risk lymph nodes. Most retrospective single-centre reports indicate that the routine use of extended lymphadenectomy for potentially curable GC can be performed safely. Four published prospective randomized trials have not shown a survival advantage for the D2 lymph node dissection and do not support the routine use of extended D2 gastrectomy. A modified D2 operation avoiding pancreatico-splenectomy will provide superior staging information and may avoid the added morbidity and mortality with additional organ resection. The advanced stage of disease at surgery in most patients remains the key determinant of survival. If there is survival benefit of D2 lymphadenectomy, it is limited to those with few lymph node metastases. Acknowledgement The authors are grateful to Miss Anjita Pandey for the preparation of this paper. References 1. Rosin RD. Tumors of the stomach. In: Zinner MJ, Schwartz SI, Ellis H, et al, editors. Maingot's Abdominal Operation, 10th edn. Prentice Hall International 1997. Vol 1. pp. 1009-11. 2. McNeer G, Berg JW. The clinical behavior and management of primary malignant lymphoma of the stomach. Surgery 1951;46:829. 3. Scott HW, Adkins RB, Sawyer JL. Results of an aggressive surgical approach to gastric carcinoma during a 23 years period. Surgery 1985;97:57. 4. Borch K, Jonsson B, Tarpila E, Franzen T, Berglund J, Kullman E, et al. Changing pattern of histological type, location stage, and outcome of surgical treatment of gastric carcinoma. Br J Surg 2000:87:618-26. 5. Kajitani T. The general rules for the gastric cancer study in surgery and pathology. Part I. Clinical classification. Jpn J Surg 1981;11:127-39. 6. Hallissey MT, Allum WH, Jewkes AJ, Ellis DJ, Fielding JW. Early detection of gastric cancer. BMJ 1990:513-5. 7. Sue Ling HM. Detection and treatment of early cancer in the West Gastric. Cancer 1998;1:8-9. 8. Hikoi Y, Nakane Y, Yamamoto M. Surgical strategy for early gastric cancer. Br J Surg 1990;77:1330-4. 9. Schlemper RJ, Itabashi M, Kato Y, Lewin KJ, Riddell RH, Shimoda T, et al. Differences in diagnostic criteria for gastric carcinoma between Japanese and Western pathologists. Lancet 1997;349:1725-9. 10. Kim JP, Hur YS, Yang HK. Lymph node metastasis as a significant prognostic factor in early gastric cancer: analysis of 1136 early gastric cancer. Ann Surg Oncol 1995;2:308-13. 11. Lisborg PH, Jatzko GR, Denk H, Klimpfinger MH, Stettner HM. Long term survival analysis of gastric cancer limited to the submucosa. J Gastroenterol 1997;35:663-8. 12. Ohta H, Noguchi Y, Takagi K, Nishi M, Kajitani T, Kato Y. Early gastric carcinoma with special reference to macroscopic classification. Cancer 1987;60:1099-106. 13. Takahashi T, Kodama M, Kida K, et al. Lymphnode dissection for early gastric cancer Geka-Shinryoh 1983;25:163-8. 14. Suzuki H, Endo M, Suzuki S, et al. Surgical treatment for early gastric cancer. Jpn J Gastroenterol Surg 1984;17:1517-76. 15. Nashimoto A, Tanaka S, Miyashita K, Sasaki K, Muto T, Soga J. Clinicopathological study for early gastric cancer. J Jpn Surg Sec 1988;89:1780-8. 16. Oohara T. Rational view of reduced radical gastectomy for early gastric cancers. Jpn J Gastroenterol Surg 1991;24:167-71. 17. Yokota T, Saito T, Teshima S, Kikuchi S, Kunii Y, Yamauchi H. Lymphnode metastasis in early gastric cancer: How can surgeons perform limited surgery? Int Surg 1998;83:287-90. 18. Hiki Y, Shimao H, Mieno H, Sakakibara Y, Kobayashi N, Saigenji K. Modified treatment of early gastric cancer. Evaluation of endoscopic treatment of early gastric cancers with respect to treatment indication groups. World J Surg 1995;19:517-22. 19. Korenaga D, Orita H, Maekawa S, Maruoka A, Sakai K, Ikeda T, et al. Pathological appearance of the stomach after endoscopic mucosal resection for early gastric cancer. Br J Surg 1997;84: 1563-6. 20. Takekoshi T, Baba Y, Ota H, Kato Y, Yanagisawa A, Takagi K, et al. Endoscopic resection of early gastric carcinoma: results of retrospective analysis of 308 cases. Endoscopy 1994;26:352. 21. Takeshita K, Tani M, Inoue H, Saeki I, Honda T, Kando F, et al. A new method of endoscopic mucosal resection of neoplastic lesions in the stomach. Its technical features and results. Hepato gastro enterology 1997;44:1602-11. 22. Ohashi S. Laparoscopic intraluminal (intra-gastric) surgery for early gastric cancer. Surg Endosc 1999;9:161-71. 23. Yamashita Y, Maekewa T, Sakai T, Shirakusa T. Transgastrostomal endoscopic surgery for early gastric carcinoma and submucosal tumor. Surg Endosc 1999;13:361-4. 24. Cuschieri A. Laparoscopic gastric resection. Surg Clin North Am 2000;80:1269-84. 25. McNeer G, Bowden L, Booner RJ, McPeak CJ. Elective total Gastrectomy for cancer for the stomach; end results. Ann Surg 1974;180:252-6. 26. Costello CB, Taylor TV, Torrance B. Personal experience in the surgical management of carcinoma of the stomach. Br J Surg 1977;64:47-51. 27. Yamada E, Miyaishi S, Nakazato H, Kato K, Kito T, Takagi H, et al. The surgical treatment of cancer of the stomach Int Surg 1980;65:387-99. 28. Suzuki H, Endo M, Nakayama K. A review of the five year survival rate and clinicopathologic factors in stomach cancer treated by surgery alone. Int Adv Surg Oncol 1983;6:271. 29. Gall GP, Hermanek P. New aspects in the surgical treatment of gastric carcinoma: A comparative study of 1636 patients operated between 1969 and 1982. Eur J Surg Oncol 1985;11:219. 30. Maruyama K, Okabayshi K, Kinoshita T. Progress in gastric cancer surgery in Japan and its limits of radicality. World J Surg 1987;11:418-25. 31. Gennari L, Bozzetti F, Bonfanti G, Morabito A, Bufalino R, Doci R, et al. Subtotal versus total gastrectomy for cancer of the lower two third of the stomach: a new approach to an old problem. Br J Surg 1986;73:534-8. 32. Shiu MH, Perrotti M, Brennan MF. Adenocarcinoma of the stomach: a multivariate analysis of clinical pathologic treatment factors. Hepato gastro-enterology 1989;36:7. 33. Msika S, Chastang C, Houry S, Lacaine F, Huguier M. Lymph node involvement as the only prognostic factor in curative resected gastric carcinoma. A multi variate analysis. World J Surg 1989;13:118-23. 34. Allum WH, Powell DJ, McComkey CC, Fielding JW. Gastric cancer: a 25 year review. Br J Surg 1989;76:535-40. 35. Breaux JR, Bringaze W, Chappuis C, Cohn I Jr. Adenocarcinoma of the stomach: a review of 35 years and 1,710 cases. World J Surg 1990;14:580-6. 36. Meyer HJ, Johne J, Wilke H, Pichlmayr R. Surgical treatment of gastric Cancer. Retrospectime survey of 1704 operated cases with special reference to total gastrectomy as the operation of choice. Semi Surg Oncol 1991;7:356-64. 37. Nakamura K, Ueyama T, Yao T, Xuan ZX, Ambe K, Adachi Y, et al. Pathology & prognosis of gastric carcinoma: findings in 10,000 patients who underwent primary gastrectomy. Cancer 1992;70:1030-7. 38. Stipa S, Digrorgio A, Ferri M, Bottti C. Results of curative gastrectomy for carcinoma. J Am Coll Surg 1994;179:567-72. 39. Pacelli F, Doglietto GB, Bellantone R, Alfieri S, Sgadari A, Crucitti F. Extensive versus limited lymphnode dissection for gastric cancer. A comparative study of 320 patients. Br J Surg 1993;80:1153-6. 40. Roder JD, Bottcher K, Siewert JR, Busch R, Hermanek P, Meyer HJ. German Gastric carcinoma study group. Prognostic factors in gastric carcinoma results of the German gastric carcinoma study 1992. Cancer 1993;72:2089-97. 41. Lisborg P, Jatzko G, Horn M, Neumann HJ, Muller M, Stettner H, et al. Radical surgery (R2 resection) for gastric cancer a multi variate analysis. Scand J Gastroenterol 1994;29:1024-8. 42. Kockerling F, Reck T, Gall FP. Extended gastrectomy who benefits World J Surg 1995;19:541-5. 43. Jatzko GP, Lisborg PH, Denk H, Klimpfinger M, Stettner HM. A 10 yr. experience with Japanese type lymph node dissection for gastric cancer outside of Japan. Cancer 1995;76:1302-12. 44. Gouzi JL, Hugnier M, Fagiez PL, Launois B, Flamant Y, Lacaine F, et al. Total vs subtotal gastrectomy for adeno- carcinoma of the gastric antrum. Ann Surg 1989;209:162-6. 45. Viste A, Haugstvedt T, Eide GE, Soreide O and the Norwegian member stomach cancer trial members. Post op complications and mortality after surgery for gastric cancer. Ann Surg 20:7-13. 46. Haugstvedt TK, Viste A, Eide GE. Members of the Norwegian stomach cancer trial. Norwegian multicentre study of survival & prognostic factors in patients undergoing curative resection for gastric carcinoma. Br J Surg 1988;80:975. 47. Guadagni S, Reed PI, Johnston BJ, De Bernardinis G, Catarci M, Valenti M, et al. Early gastric cancer follow up after gastrectomy in 159 patients. Br J Surg 1993;80:325-8. 48. Robertson CS, Chung SCS, Woods SDS, et al. Prospective randomised trial comparing R, subtotal gastrectomy and R3 total gastrectomy for antral cancer. Ann Surg 1994;229:176. 49. Bonenkamp JJ, Songun I, Hermans J, Sasako M, Welvaart K, Plukker JT, et al. Randomized comparison of morbidity after D1& D2 dissection for gastric cancer in 996 Dutch patients. Lancet 1995;345:745-8. 50. Cuschieri A, Fayers P, Fielding J, Craven J, Bancewicz J, Joypaul V, et al. Post-operative morbidity and mortality after D1 & D2 resections for gastric cancer: preliminary results of the MR with randomized controlled surgical trial. Lancet 1996;347:995-9. 51. Bozzetti F, Marubini E, Bonfanti G, Miceli R, Piano C, Crose N, et al. Total versus subtotal gastrectomy surgical morbidity and mortality rates in a multicentre, Italian randomized trial. Ann Surg 1997;226:613-20. 52. Kodama Y, Sugimachi K, Soejima K, Matsusaka T, Inokuchi K. Evaluation of extensive lymph node dissection for carcinoma of the stomach. World J Surg 1981;5:241-8. 53. Sawai K, Takahashi T, Suzuki H. New trends in surgery for gastric cancer in Japan. J Surg Oncol 1994;56:221-6. 54. Volpe CM, Koo J, Miloro SM, Driscoll DL, Nava HR, Douglass HO Jr. The effect of extended lymphadenectomy on survival in patients with gastric Adeno carcinoma. J Am Coll Surg 1995;181:56-64. 55. Baba H, Maehara Y, Inutsuka S, Takeuchi H, Oshiro T, A dachi Y, et al. Effectiveness of extended lymphadenectomy in non-curative gastrectomy. Am J Surg 1995;169:261-4. 56. Adachi Y, Mori M, Maehara Y, Kitano S, Sugimachi K. Prognostic factors of node negative gastric carcinoma. Univariate and multi variate analysis. J Am Coll Surg 1997;184:373-7. 57. Dent DM, Madden MV, Price SK. Randomized comparison of R1 & R2 gastrectomy for gastric carcinoma. Br J Surg 1988;75:110-2. 58. Dent DM, Madden MV, Price SK. Controlled trials and R1/ R2 controversy in the management of gastric carcinoma. Surg. Oncol North Am 1993;2:443. 59. Siewert JR, Battcher K, Roder JD, Busch R, Hermanek P, Meyer HJ. German gastric carcinoma study group. Prognostic relevance of systematic lymph node dissection in gastric carcinoma. Br J Surg 1993;80:1015-8. 60. Wanebo HJ, Kennedy BJ, Winchester DP, Fremgen A, Stewart AK. Gastric carcinoma: Does lymph node dissection alter survival. J Am Coll Surg 1996;183:616-24. 61. Iwata K, Ogoshi K, Tajima T, et al. Long-term, consequences of Gastrectomy procedures in gastric cancer patients. Annals of Cancer Research and Therapy 2000;8:97-111. 62. Chareton B, Lauden S, Manganas D, et al. Prospective randomized trails comparing Bilroth I and Bilroth II procedures for carcinoma of the gastric antrum. J Am Coll Surg 1993;183:191-4. 63. Harrison LE, Karpech MS, Brennan MF. Proximal gastric cancer resected via a transabdominal - only approach. Results and comparisons to distal adenocarcinoma of the stomach. Ann Surg 1997;225:678. 64. Maehara Y, Moriguchi S, Kakeji Y, Orita H, Haraguchi M, Korenaga D, et al. Prognostic factors in adenocarcinoma in upper one-third of the stomach. Surg Gynecol Obstet 1991;173:223-6. 65. Butter JA, Dubrow TJ, Trezana Y, Klassen M, Nejdl RJ. Total Gastrectomy in the treatment of advanced gastric cancer. Am J Surg 1989;158:602-5. 66. Kwaura Y, Mori Y, Nakajima H, Iwa T. Total Gastrectomy with left oblique abdominothoracic approach for gastric cancer involving esophagus. Arch Surg 1988;123:514-8. 67. Paolini A, Tosato F, Cassese M, De Marchi C, Grande M, Paoletti P, et al. Total Gastrectomy in the treatment of adenocarcinoma of the cardia. Review of the results of 7834 resected patients. Am J Surg 1986;151:238-43. 68. Anderson TD, Maclntyre IM. Symptomatic out come following resection of gastric cancer. Surg Oncol 1995;4:35-40. 69. Santoro E, Garofalo A, Carlini M, Rinaldi G, Santoro E. Early and late results of 100 Consecutive total gastrectomies for cancer. Hepatogastroenterology 1994;41:489-96. 70. Bozzetti F. Total versus subtotal Gastrectomy in cancer of the distal stomach: facts and fantasy. Eur J Surg Oncol 1992;18:572-9. 71. Davies J, Johnston D, Seu-ling H, Young S, May J, Griffith J, et al. Total or subtotal gastrectomy for gastric carcinoma. A study of quality of life. World J Surg 1998;22:1048-55. 72. Huscher C, Chiodini S, Freni V, et al. Adequacy of paracardial dissection in subtotal versus total Gastrectomy. Br J Surg 1992;79:942 73. Kodama M, Koyama K, Chida T, Arakawa A, Tur G. Early post operative evaluation of pylorus preserving gastrectomy for gastric cancer. World J Surg 1995;19:456-61. 74. Isozaki H, Okajima K, Momura E, Ichinona T, Fujii K, Izumi N, et al. Post operative evaluation of pylorus preserving gastrectomy for early gastric cancer. Br J Surg 1996;83:266-9. 75. Hirai T, Saeki S, Matsuki K, Yamashita Y, Iwata T, Yoshimoto A, et al. Preservation of the lower esophageal sphincter during total gastrectomy for gastric cancer to prevent post operative reflux oesophagitis. Surg Today 1995;25:507-14. 76. Buhl K, Lehnert T, Schlag P, Herfarth C. Reconstruction after gastrectomy and quality of life. World J Surg 1995;19:558-63. 77. Azagra JS, Goergen M, De Simone P, Ibanez-Aguirre J. Minimally invasive Surgery for gastric cancer. Surg Endosc 1999;13:351-7. 78. Sasako M, Sano T, Kataai H, et al. Radical Surgery: In Sugimura T, Sasako M, editors. Gastric cancer. Oxford: Oxford Univesity Press; 1997. pp. 223-4. 79. Iriyama K, Ohsawa T, Tsuchibashi T, Noji M, Miki C, Ilunga K, Suzuki H.Results of combined resection of invaded organs in patients with potentially curable, advanced gastric cancer. Eur J Surg 1994;160:27-30. 80. Furukawa H, Hiratsuka M, Iwanaga T. A rational technique for surgical operation on Borrmann type 4 gastric carcinoma: left upper abdominal evisceration and Appleby's method. Br J Surg 1988;75:116-9. 81. Maruyama K, Sasako M, Kinoshita T, et al. Pancreas - preserving total Gastrectomy for proximal gastric cancer. Wold J Surg 1995;19:532-6. 82. Pacelli F, Doglietto GB, Alffien S, Carriero C, Malerba M, Crucitti P, et al. Avoiding pancreatic necrosis following pancreas preserving D3 lymphadenectomy for gastric cancer. Br J Surg 1998;85:125-6. 83. Uyama I, Ogiwara H, Takahara T, Kikuchi K, Iida S, Kubota T, et al. How I do it: spleen and pancreas preserving total gastrectomy with super extended lymphadenectomy including dissection of the paraaortic lymph nodes for gastric cancer. J Surg Oncol 1996;63:268-70. 84. Griffitth JP, Sue-ling HM, Martin I, Dixon MF, McMahon MJ, Axon AT, et al. Preservation of the spleen improves survival after radical surgery for gastric cancer. Gut 1995;36:684-90. 85. Otsuji E, Yamaguchi T, Sawai K, Ohara M, Takahashi T. End results of simultaneous splenectomy in patients undergoing total Gastrectomy for gastric cancer. Surgery 1996;120:40-4. 86. Wanebo HJ, Kennedy BJ, Winchester DP, Stewart AK, Fremgen AM. Role of splenectomy in gastric cancer surgery: adverse effect splenectomy on long term survival. J Am Coll Surg 1997;185:177-84. 87. Okajima K, Isozaki H. Splenectomy for treatment of gastric cancer. Japanese experience. World J Surg 1995;19:537-40. 88. Sugimachi K, Kodama Y, Okamura K, et al. Splenectomy in total gasrectomy. Syujitu 1982;36:337. 89. Toge T, Hamamoto S, Itagaki E, et al. Concavalin A induced and spontaneous suppressor cell activities in spleen cells from gastric cancer patient Cancer 1983;52:162. 90. Bollschwieler E, Boettcher K, Hoelscher AH, et al. Is the prognosis for Japanese and German patients with gastric cancer really different? Cancer 1993;74:2918-25. 91. Bunt AM, Hermans J, Boon MC, van de Velde CJ, Sasako M, Fleuren GJ et al. Evaluation of the extent of lymphadenectomy in a randomized trial of Western versus Japanese type surgery in gastric cancer. J Clin Oncol 1994;12:417-22. 92. Bunt AM, Hermans J, Smit VT, van de Velde CJ, Fleuren GJ, Bruijn JA. Surgical/pathological - stage migration confounds comparisons of gastric cancer survival rates between Japan and western countries. J Clin Oncol 1995;13:19-25. 93. Sasako M, Mc Culloch P, Kinoshita T, Maruyama K. Therapeutic value of lymph node dissection for gastric cancer: A new method of evaluation circumventing the stage migration effect. Br J Surg 1995;82:346-51. 94. Parikh D, Johnson M, Chagla L, Lowe D, McCulloch P. D2 gastrectomy: Lessons from a prospective audit of learning curve Br J Surg 1996;83:1595-8. © 2003 Indian Journal of Surgery. Also available online at http://www.indianjsurg.com |
| |||||||||
