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World J Gastroenterol. Oct 14, 2014; 20(38): 13692-13704
Published online Oct 14, 2014. doi: 10.3748/wjg.v20.i38.13692
Improving the outcomes in gastric cancer surgery
Juul JW Tegels, Michiel FG De Maat, Karel WE Hulsewé, Anton GM Hoofwijk, Jan HMB Stoot
Juul JW Tegels, Michiel FG De Maat, Karel WE Hulsewé, Anton GM Hoofwijk, Jan HMB Stoot, Department of Surgery, Orbis Medical Center, 6130 MB Sittard, The Netherlands
Michiel FG De Maat, Department of Surgery, Maastricht University Medical Center, 6211 LK Maastricht, The Netherlands
Karel WE Hulsewé, Anton GM Hoofwijk, Jan HMB Stoot, Department of Surgery, Atrium Medical Center, 6461 AL Heerlen, The Netherlands
Author contributions: Stoot JHMB was invited and designed the outline of the paper; Tegels JJW wrote the first and final draft of the paper; De Maat MFG, Hulsewé KWE, Hoofwijk AGM and Stoot JHMB made writing contributions and extensively reviewed the manuscript.
Correspondence to: Juul JW Tegels, MD, Department of Surgery, Orbis Medical Centre, PO Box 5500, 6130 MB Sittard, The Netherlands.
Telephone: +31-88-4597777 Fax: +31-88-4597975
Received: December 28, 2013
Revised: February 8, 2014
Accepted: May 29, 2014
Published online: October 14, 2014


Gastric cancer remains a significant health problem worldwide and surgery is currently the only potentially curative treatment option. Gastric cancer surgery is generally considered to be high risk surgery and five-year survival rates are poor, therefore a continuous strive to improve outcomes for these patients is warranted. Fortunately, in the last decades several potential advances have been introduced that intervene at various stages of the treatment process. This review provides an overview of methods implemented in pre-, intra- and postoperative stage of gastric cancer surgery to improve outcome. Better preoperative risk assessment using comorbidity index (e.g., Charlson comorbidity index), assessment of nutritional status (e.g., short nutritional assessment questionnaire, nutritional risk screening - 2002) and frailty assessment (Groningen frailty indicator, Edmonton frail scale, Hopkins frailty) was introduced. Also preoperative optimization of patients using prehabilitation has future potential. Implementation of fast-track or enhanced recovery after surgery programs is showing promising results, although future studies have to determine what the exact optimal strategy is. Introduction of laparoscopic surgery has shown improvement of results as well as optimization of lymph node dissection. Hyperthermic intraperitoneal chemotherapy has not shown to be beneficial in peritoneal metastatic disease thus far. Advances in postoperative care include optimal timing of oral diet, which has been shown to reduce hospital stay. In general, hospital volume, i.e., centralization, and clinical audits might further improve the outcome in gastric cancer surgery. In conclusion, progress has been made in improving the surgical treatment of gastric cancer. However, gastric cancer treatment is high risk surgery and many areas for future research remain.

Key Words: Gastric cancer, Laparoscopic surgery, Risk assessment, Surgical outcome, Postoperative care

Core tip: In gastric cancer surgery comorbidities, nutritional status and geriatric frailty should be assessed to judge surgical risks in preoperative assessment. Improving postoperative recovery by laparoscopic surgery has improved outcomes for these patients. Enhanced recovery after surgery and fast-track programs should aim to further improve recovery after surgery. Advances have been made, however many areas for future research and improvement remain.

Citation: Tegels JJ, De Maat MF, Hulsewé KW, Hoofwijk AG, Stoot JH. Improving the outcomes in gastric cancer surgery. World J Gastroenterol 2014; 20(38): 13692-13704

Gastric cancer constitutes a major health problem worldwide and is one of the leading causes of cancer-related deaths. In the United States gastric cancer compromises only 2% (25500 cases) of all new cancer cases yearly. In South Korea it is the leading form of cancer constituting 20.8% of malignant neoplasms. The number of deaths due to gastric cancer has decreased from 774000 in 1990 to 755000 in 2010 worldwide. It remains however the second leading cause of cancer death after lung cancer[1]. Prognosis of gastric cancer is relatively poor with an overall five-year survival rate for gastric cancer in the United States between 1999 and 2005 of 27%[2]. For localized disease 5-year survival rate was 63%, but only 23% of all gastric cancer cases were diagnosed at this stage[2]. In 2008 gastric cancer was responsible for a disability-adjusted life-year (DALY) rate of 241 per 100000 for males and 146 per 100000 in females worldwide, which is 9.8% and 6.3% of total cancer related DALY-rates respectively[3].

Surgery is the mainstay of treatment for gastric malignancy. In European and other Western countries gastric cancer surgery is regarded to be high risk surgery and there are major differences in outcome between countries[4]. Therefore, knowledge to improve the outcome of gastric cancer treatment is of great importance. As with all operations perioperative planning of this type of surgery is crucial for the clinical outcome of treatment, not only in terms of morbidity but also in functional recovery and hospital stay. Many efforts have been made to improve outcome after surgery for these patients in pre-, intra- and postoperative stage of treatment. Not only surgical efforts have been implemented, medical oncology has also contributed a great deal with neoadjuvant and adjuvant chemotherapeutic regimens for example. However, these advances are beyond the scope of this review.

This paper will provide a structured review of current literature that deals with advances in surgical care for gastric cancer patients in the preoperative-, intra-operative- and postoperative stage. Literature will be discussed this order. MEDLINE database was searched using appropriate search terms for each of the discussed themes. Most relevant and recent literature was used to complete this review. Search terms used for each paragraph are given in Table 1. Lastly, advances in organization of surgical care will be discussed.

Table 1 MEDLINE search terms used per section.
SectionMEDLINE search termsLimits
Introduction"Cancer", "Mortality", "Global Burden of Disease", "Cancer statistics", "Gastric cancer", "Disability adjusted life years"Language: English
Time period: 2005-2014
Advances in preoperative care
Risk assessment"Risk assessment", "ASA classification", "peri operative risk", "Charlson Comorbidity Index", "Gastric cancer", "obesity", "complications", "previous abdominal surgery"Language: English
Time period: 2005-2014
Nutritional status"Malnutrition", "screening tool", "Surgery", "Gastric cancer"Language: English
Time period: 2005-2014
Sarcopenia"Gastric cancer", "Sarcopenia", "Surgery"Language: English
Time period: 2005-2014
Frailty"Fraily surgery", "Complications", "Gastric cancer"Language: English
Time period: 2005-2014
Prehabilitation"Prehabilitation", "Cancer"Language: English
Time period: 2005-2014
Staging laparoscopy and was cytology"Gastric cancer", "Staging laparoscopy", "peritoneal cytology", "Hyperthermic Intreperitoneal Chemotherapy"Language: English
Time period: 2005-2014
Advances in intra-operative care
Laparoscopic surgery (introduction)"Gastrectomy", "Gastric cancer", "Laparoscopy"Language: English
Time period: 1990-2000
Laparoscopic surgery"Gastrectomy", "Gastric cancer", "Laparoscopy"Language: English
Time period: 2005-2014
Article type: Review
Lymph node dissection"D2 resection", "Gastric cancer", "Nodal dissection", "Bursectomy"Language: English
Time period: 1995-2014
Article type: Clinical Trial
Reconstruction technique"Distal gastrectomy", "Gastric cancer", "Reconstruction", "Billroth", "Reconstruction"Language: English
Time period: 2005-2014
Intra-operative feeding jejunostomy placement"Gastric cancer", "feeding jejunostomy", "morbidity"Language: English
Time period: 2005-2014
Advances in postoperative care
Detection and treatment of anastomotic leakage"Gastrectomy", "anastomotic leak", "risk factors", "gastric cancer", "covered stent"Language: English
Time period: 2005-2014
ERAS and Fast-track programs"Gastric cancer", "ERAS", "Fast track", "Oral feeding", "Gastrectomy"Language: English
Time period: 2005-2014
Advances in organization of care: centralization and audits"Case load" or "hospital volume", "gastric cancer", "gastrectomy"Language: English
Time period: 2005-2014

Surgical morbidity in gastric cancer surgery is reported to be as high as 39%[5]. In addition, complications after curative surgery for gastric cancer have a negative effect on overall and disease specific survival[6]. Therefore much effort should be made in preventing morbidity and mortality. Needles to say, the preferential moment to assess the risk of morbidity and mortality is during preoperative work-up. Gastric cancer patients in Western countries constitute a group that is especially frail to surgical treatment due to the condition in which patients usually present at time of diagnosis. An example is the reported rate of malnutrition as high as 85%[7]. The on average poor physical state and advanced age as well as disease stage contributes to poorer outcomes in Western countries as compared to Eastern countries such as Japan and South Korea where nationwide screening programs exist to diagnose gastric cancer at an early stage[8].

Preventing morbidity is becoming especially important since multidisciplinary treatment schedules are becoming standard in gastric cancer. Deterioration of general condition or delay because of required rehabilitation time due to serious adverse events (e.g., abdominal sepsis due to anastomotic leakage requiring long-term Intensive Care Unit treatment) may disqualify a patients for his/her treatment.

Surgical risk assessment

Surgical risk assessment can be complex. Several risk scores have been introduced. A globally used risk-score is the American Society of Anesthesiologists (ASA)-Physical status and was first introduced in 1941[9]. To the best knowledge of the authors, ASA physical status as a risk factor has not been extensively investigated in gastric cancer surgery. ASA-physical status is only a component of the overall risk assessment. Moreover, it might also subject to interpretation by the assessor. Different ASA classifications may be ascribed by different assessors depending on which factors are taken into account[9]. The ASA classification as an instrument is also a non-specific. Moreover, it is just a momentary status, without any clues to improve its figure in the future. By definition each cancer patient is having systemic disease and only therefore already ASA 2-classification. Practical applicability of this classification remains a challenge not only in daily practice but also in clinical research. Therefore new classifications have been developed.

The Charlson comorbidity index (CCI) was established as a method for classifying comorbid conditions that determine risks of mortality[10]. CCI was later identified and validated in a surgical setting for prediction of mortality risk in patients undergoing complex gastrointestinal surgery[11]. It was shown in octo- and nonogenarians who underwent radical gastrectomies that these elderly patients had higher morbidity and mortality rates, and this was associated with CCI ≥ 5[12]. Cancer specific survival was comparable to younger patients[12]. In another cross-sectional study the only independent factor predicting for mortality was the presence of comorbidity not age[13]. In contrast, a German study which included 139 gastric cancer patients did not find a significant correlation between CCI and the occurrence of morbidity and mortality postoperatively[14]. In multivariate analysis age was found as an independent factor for postoperative events.

Several patient factors associated with an impaired outcome after gastric cancer surgery have been reported over the years. In a series of 118 laparoscopic total gastrectomies, male gender was independently associated with postoperative morbidity[15]. Overweight patients [i.e., body mass index (BMI) > 25 kg/m2] are at an increased risk of complications; this was shown in a large prospective series of 1853 patients[16]. This showed increased complication rate (47.9% vs 35.8%, P < 0.001). Obese patients especially had more anastomotic leakages (11.8% vs 5.4%) and wound infections (8.9% vs 4.7%). Several other studies have also shown the association between higher BMI and increased postoperative morbidity[17-19]. Although no valid explanation for this finding is reported; it is suggested that in open and laparoscopic surgery, obesity is associated with more technical difficulties[20].

A history of upper abdominal surgery is not a contraindication for laparoscopic gastrectomy. In a series of 22 cases with previous upper abdominal surgery (PUAS) no differences were found for operative time, blood loss or conversion to open surgery when compared to patients without a history PUAS[21]. In a larger series of 50 patients with a history of laparotomy similar results were obtained for laparoscopic assisted gastrectomies[22]. Also, when compared to open surgery in patients with PUAS laparoscopic gastrectomy was performed with comparable postoperative outcome[21].

The literature fairly uniformly states that age should not be factored in clinical decision making, rather comorbid conditions and general condition are far more important factors predicting adverse outcomes. It remains challenging to adequately assess a patient’s general condition and decide what factors exclude a patient from surgical treatment. Therefore, we discuss some of the features that are crucial to take into account during preoperative work-up.

Nutritional status

Gastric cancer patients are at a high risk for malnutrition and 30% to 38% of patients are reported to have > 10% weight loss in past six months[23]. A misbalance between energy expenditure and nutritional supplementation is the fundamental physiologic derangement leading to cancer-induced weight loss. Tumor related causes of malnutrition include early satiety and obstruction, but also tumor induced metabolic alterations[7]. Malnutrition is associated with increased morbidity and mortality after gastric cancer surgery[7]. It is highly important to thoroughly screen patients for malnutrition as interventions can be done to preoperatively improve nutritional status and subsequently surgical outcome. Both malnourishment and weight loss are associated with poor clinical outcome after surgery[24].

Questionnaires: An easy and non-invasive tool to estimate the patient’s physical and/or mental condition preoperatively is the use of questionnaires. Several questionnaires have been developed to identify patients at risk for malnutrition. The Short Nutritional Assessment Questionnaire (SNAQ) and Malnutrition Universal Screening Tool (MUST) scores are commonly used nutritional screening tools in surgical patients (Table 2)[25,26]. These questionnaires accurately screen for malnutrition and are obligatory in some Western countries as a part of governmental health care quality programs[27,28]. Although it is easy to apply, evidence for the value of nutritional screening tools to predict postoperative outcome in gastric cancer surgery is scarce. It has been shown that screening for nutritional risk in gastric cancer surgery patients using Nutritional Risk Screening 2002 (NRS 2002) is helpful. Increased scores are associated with more complications and increased length-of-stay[29]. A recently published study in which SNAQ was used to evaluate risks of adverse postoperative events after gastric cancer surgery showed that SNAQ ≥ 1 was associated with increased severe complications (i.e., Clavien-Dindo grade ≥ 3a, 35.7% vs 17.7%, P = 0.02) and in-hospital mortality (OR = 5.1, 95%CI: 1.01-23.8, P = 0.04)[30]. The detection of nutritional depletion is important, especially with neo-adjuvant therapies potentially further compromising the nutritional and metabolic status[31]. Questionnaires are subjective methods to assess nutritional status and therefore methods to objectively measure a patient’s condition might improve outcomes.

Table 2 Malnutrition universal screening tool and short nutritional assessment questionnaire, screening tools for detecting malnutrition.
Step 1 Body mass index
> 200
< 18.52
Step 2 Unintentional weight loss past 3-6 mo
< 5%0
> 10%2
Step 3 Acute disease effect
If patient is acutely ill and there has been or is likely to be no nutritional intake for > 5 d2
Did you lose weight unintentionally?
More than 6 kg in past 6 mo3
More than 3 kg in past 3 mo2
Did you experience a decreased appetite over the last month?
Did you use supplemental drinks or tube feeding over the last month?

Sarcopenia, or the decrease of muscle tissue, is a part of the cachexia syndrome[7]. Presence of sarcopenia has been shown to affect short-term postoperative outcome with increased morbidity and mortality rates in patients undergoing liver resection for colorectal liver metastases[32]. It also predicts adverse long-term outcome in liver and pancreas surgery for malignancy[33,34]. The method for measuring sarcopenia in these studies was to calculate the total muscle or psoas muscle cross-sectional area using a specialized software package (e.g., OsiriX5.5.2, open-source software) on computed tomography (CT) imaging on a set level (e.g., at level of spinous process of lumbar vertebra L3). This could also be a useful method in gastric cancer patients as they all have preoperative staging CT-imaging of the abdomen. But as far as the authors are aware no literature on this subject exists to date. Other objective parameters such as lowered preoperative serum albumin levels have been identified as risk factors for postoperative complications after surgery for gastrointestinal carcinomas[35,36]. But the latter risk factors remain under debate as some authors dispute the role of malnutrition and lowered serum albumin levels as risk factors for impaired outcome after gastric cancer surgery[37].

For future research it is important to establish objective screening tools to detect malnutrition in surgical patients and whether these results are related to perioperative outcomes. More importantly, studies need to be done to establish whether correction of nutritional status results in improved outcome.


In Western countries gastric cancer is a disease of the elderly, and therefore geriatric aspects have an important role in these patients. Frailty is defined as a state of increased vulnerability towards stressors in older individuals, leading to increased risk of developing adverse health outcomes. Geriatric frailty is considered by Fried et al[38] to be a clinical syndrome in which three of following five aspects are present. These are: unintentional weight loss (10 lbs in the past year), self-reported exhaustion, weakness (grip strength), slow walking speed, and low physical activity. Methods for assessing frailty are numerous. They range from a comprehensive geriatric assessment, which often employs the use of multiple questionnaires and short physical tests (e.g., 4-m walk test, grip strength measurement), to using specific frailty questionnaires (e.g., Edmonton frail scale).

Frailty assessment is an emerging method to aid surgical risk assessment and it rapidly gaining evidence based support[39,40]. It has been shown that scores on the Edmonton frail scale (EFS) > 7, i.e., increased frailty, were associated with increased complications after non-cardiac surgery (OR = 5.02, 95%CI: 1.55-16.25)[39]. The association between frailty and adverse postoperative outcomes has also been shown in patients undergoing cardiac surgery[41] and patients undergoing various types of elective surgery[42]. Some use tools such as EFS or Hopkins Frailty Score which includes various tests with regards to cognition, ADL function and more (including laboratory tests such as serum albumin)[39,40]. Recently published results from a large prospective study with patients who underwent general, oncologic and urologic procedures confirmed these findings in a larger patient population (n = 189)[43]. They showed that “intermediately frail” or “frail” as judged by the Hopkins Frailty score was an independent predictor for complications. Another example of frailty assessment questionnaire is the Groningen frailty indicator[44]. This questionnaire was used in a retrospective study to evaluate frailty assessment as a predictor for adverse outcome after gastric cancer surgery. In this recent study, incorporating 180 patients, increased GFI was significantly associated with postoperative morbidity and in-hospital mortality[30].


A novel strategy for improving outcomes after surgery is by preoperatively correcting the reduced functional, nutritional, physical and neurophysiological state of patients: prehabilitation[45]. This type of intervention might prove to be especially beneficial in elderly patients because they are often compromised in these respects. Most available literature on prehabilitation concerns joint replacement surgery. A pilot study has been published that evaluates multimodality prehabilitation interventions in colorectal surgical patients[46]. This study uses a trimodal approach of preoperative exercise, nutritional intervention (dietary behavior counseling and protein supplementation) and anxiety reduction training (also aimed at increasing compliance of exercise and nutritional intervention). Multimodal approaches have yielded promising preliminary results such as better walking capacity in weeks after surgery and higher physical activity levels after surgery compared to controls[46,47]. Because in Western society gastric cancer is predominantly a disease of the elderly prehabilitation may provide a promising effort for improving outcomes in these patients in the future[48].

Staging laparoscopy and wash cytology

Preoperative staging laparoscopy improves detection of peritoneal metastases not otherwise detected by preoperative ultrasonography or CT imaging[49]. It can therefore prevent an unnecessary explorative laparotomy or change management in up to 60% of cases[50,51]. An expert panel concluded that a staging laparoscopy should be performed for reasons mentioned above, exceptions being early gastric cancer or known metastatic disease[52].

Also, during staging laparoscopy peritoneal wash cytology can be obtained to detect intraperitoneal free cancer cells (IFCC). This has been shown to be a predictor for early recurrence after curative intent surgery[53]. It is even a negative prognostic factor in patients with overt peritoneal metastases in patients with suspected serosal invasion with median survival times of 14.0 and 10.0 mo in patients without and with positive cytology respectively[54].

In patients with overt peritoneal metastases hyperthermic intraperitoneal chemotherapy (HIPEC) together with cytoreductive surgery has been considered as additional treatment. A recent review concluded that HIPEC was not beneficial for these patients[55]. Gastric cancer patients with IFCC may be suitable candidates for new treatment regimens such as neoadjuvant systemic and intraperitoneal chemotherapy before radical surgery are currently under investigation.


One of the most significant and fundamental developments in gastrointestinal surgery last decades has been the introduction of the laparoscopic technique. Large incisions are avoided and surgical trauma is minimized.

Laparoscopic surgery

Introduced in Asia in the early nineties, a laparoscopic approach was first implemented for the treatment of early gastric cancer (EGC)[56]. Early reports comparing open and laparoscopic surgery for EGC showed several advantages of the laparoscopic approach over conventional open surgery. These included, less intra-operative blood loss, less postoperative pain and shorter length-of-stay. Also serum markers indicating postoperative stress were lower, i.e., lower C-reactive protein (CRP) level on day 7, leukocyte count and interleukin-6 levels[57]. There were no significant differences in operation time, number of harvested lymph nodes and postoperative complications[57,58]. A review and meta-analysis evaluating randomized controlled trials (RCT’s) and high quality non-randomized controlled trials on laparoscopic vs open approach for distal gastrectomy for cancer showed that major complications and mortality rates were similar between procedures and concluded that the laparoscopic approach is safe[59]. However, the majority of patients had EGC and therefore comparison to a Western population case-mix is difficult. Results further showed additional benefits of fewer overall and minor complications, shorter length-of-stay (weighted mean difference, 3.6 d) and less blood loss[59]. Also, longer operation time and lower number of harvested lymph nodes was reported for laparoscopic gastrectomy. Several other reviews and meta-analyses have been published on this subject since (Table 3)[59-63]. The general conclusion of these studies is that laparoscopic approach offers improved recovery after surgery at no compromise of morbidity and mortality.

Table 3 Summary of recently published meta-analysis examining laparoscopic distal gastrectomy vs open distal gastrectomy for gastric cancer.
Ref.Trials included (n)Laparoscopic/open procedures (n)TumOR = characteristicsOperative time (min) (WMD)Blood loss (mL) (WMD)Harvested lymph nodes (WMD)Length-of-stay (WMD)Complication ratesMortality
Memon et al[62], 20084 RCT’s82/80EGC, GC+83 (P < 0.001)-104 (P = 0.02)-4.3 (P < 0.001)-3.3 d (P = 0.14)OR = 0.66 (P = 0.14)OR = 0.94 (P = 0.94)
Chen et al[60], 20096 RCT’s323/306EGC+87 (P < 0.001)-108 (P = 0.001)-4.9 (P < 0.001)-2.0 d (P = 0.14)RR = 0.61 (P = 0.01)Risk difference 0.01 (P = 0.32)
Kodera et al[61], 20106 RCT’s343/323EGC, GC+82 (P < 0.001)-118 (P < 0.001)-4.8 (P < 0.001)NAOR = 0.46 (P = 0.003)OR = 0.17 (P = 0.86)
Ohtani et al[63], 20115 RCT’s164/162EGC, GC+82 (P < 0.001)-122 (P < 0.001)-4.8 (P < 0.001)-2.5 d (P = 0.04)OR = 0.38 (P = 0.01)OR = 0.47 (P = 0.54)
Viñuela et al[59], 20126 RCT’s1658/1397ECG, GC+48.3 (P < 0.001)-118 (P < 0.001)-3.9 (P < 0.001)-3.6 (P < 0.001)OR = 0.59 (P < 0.001)OR = 0.64 (P = 0.39)
19 NRCT’s

Laparoscopic approach for performing a total gastrectomy for gastric cancer is technically more demanding and has therefore not gained as much widespread acceptance as the laparoscopic distal gastrectomy. A systematic review and meta-analysis by Chen et al[64] showed similar differences between laparoscopic assisted total gastrectomy and open total gastrectomy, i.e., longer operative time, shorter hospital stay, a decrease in medical complications and no difference in operative mortality. It included nine studies comprising 1221 patients (436 laparoscopic procedures and 758 open procedures), but none of the studies were RCT’s. All but one study included both EGC and advanced stage disease patients. Nevertheless, the authors concluded that laparoscopic approach for total gastrectomy can be performed safely and with improved outcome in experienced surgical centers[64].

As mentioned, most reported studies report on laparoscopic procedures for EGC. Laparoscopic approach for advanced stage disease has also been shown to be associated with shorter length-of-stay and less blood loss with comparable morbidity and mortality rates[65-67]. Also similar oncological outcomes are reported for laparoscopic surgery in advanced stage disease[68]. A systematic review and meta-analysis on distal gastrectomy for advanced gastric cancer concluded that further prospective controlled studies are needed for a comprehensive comparison.

A critical issue with the laparoscopic approach is oncological adequacy. The evidence for this is still sparse although a few report similar oncological outcomes for laparoscopic procedures at five years[65,66,69].

Lymph node dissection

Differences in treatment outcome between Asian and Western countries remain striking. The debate continues whether this is due to more extensive approach of lymph node dissection advocated by the Japanese Gastric Cancer Association. D2 lymphadenectomy has been shown increased survival in Chinese patients[70]. Initial results from randomized trials performed in the Netherlands and United Kingdom showed an increased morbidity and mortality rate in the D2 group and no survival benefit[71,72]. Fifteen-year follow-up results of the Dutch trial showed that D2 resection was associated with lower regional recurrence (22% in D1 resection and 12% in D2 resection) and gastric-cancer-related death[73]. They advocate a spleen preserving D2 procedure as a safer alternative. Later studies showed however that D2 resections can be performed safely in the West, they had low overall morbidity and mortality rates (3.0% after D1 and 2.2% after D2 gastrectomy, P = 0.722)[74]. Additional value of D3 dissection (dissection of hepatoduodenal ligament, superior mesenteric vein and retro-pancreatic area) is disputed. A prospective trial in Taiwan showed a slight 5-year survival benefit for D3 resections 59.5% compared to 53.6% in D1 gastrectomy patients (P = 0.041)[70]. Para-aortic nodal dissection was shown to be performed safely in addition to D2 dissection but failed to show a 5-year benefit[75,76].

Another strategy for attempting to improve oncological outcome of gastric cancer surgery was to perform a bursectomy in addition to resection and lymphadenectomy for advanced stage gastric cancer. Several studies did not show a benefit of bursectomy[77,78]. But proponents of this technique argue that it may improve survival and should not be discarded as a futile technique[79]. A phase III trial is currently ongoing in Japan that will also evaluate the effectiveness of procedure (see: ).

Reconstruction technique

Roux-en-Y is the accepted standard technique for reconstructing bowel continuity after total gastrectomy. Billroth I and II reconstruction after distal gastrectomy have been the standard for a long time but are associated with increased rates of reflux symptoms and esophagitis[80]. Roux-en-Y reconstruction as an alternative after distal gastrectomy has been thoroughly investigated. Studies have shown beneficial outcomes in terms of less reflux symptoms and less gastric remnant gastritis[81,82]. These findings persist in long-term follow-up[83]. However, patients did not differ in terms of quality of life[84]. Morbidity and mortality were similar between Billroth I and Roux-en-Y technique, but the latter was associated with longer length-of-stay and discontinuance of food intake[85].

Intra-operative feeding jejunostomy placement

Routine intra-operative placement of feeding jejunostomy can potentially decrease malnutrition and improve tolerance of adjuvant chemotherapy[86]. A study with data from a prospectively maintained database including 132 patients showed no advantage of jejunostomy placement and increased complications associated with jejunostomy placement[87]. In a series of 73 patients who received jejunostomy placement, it was shown that 21 patients had jejunostomy specific complications (11 minor and 10 major)[88]. Therefore, routine jejunostomy placement is not recommended and should be reserved for selected patients.

Detection and treatment of anastomotic leakage

Anastomotic failure or leakage is an important complication of gastric surgery, potentially with detrimental consequences. Risk factors for anastomotic leakage have been identified in several studies. These include: older age (> 65 years), longer operating time, intra-operative errors, increased blood loss and comorbidities[89-91].

When leakage or associated intra-abdominal abscess is suspected clinically by positive peritoneal signs, fever and/or wound infection, further investigation using computed tomography should be prompted. If detected and leakage is minor it can be successfully managed with percutaneous drainage[92,93]. Some authors advocate the use of conservative management techniques for treating anastomotic leakage such as placement of a naso-jejunal tube combined with percutaneous drainage of abscess[94]. In this study this approach was associated with lower mortality rates compared to operative intervention. Therefore, reoperation is only required when conservative treatment is ineffective. When reoperation is carried out the anastomosis can be evaluated and if it is in a poor condition reconstruction can be carried out[95].

Endoscopic approach also offers a chance to assess the anastomosis site and endoscopic treatment options for leakage are available. Recent literature describes endoscopic approaches for the management of anastomotic leakage and different techniques can be applied[96]. The authors concluded that defects smaller than 2 cm in size could be successfully managed using endoscopy. Techniques include use of fibrosealant or Histoacryl and also stent insertion. Multiple studies report use of removable covered metal stents to treat anastomotic leaks with relatively good results[97,98]. Main advantage of this approach is that it enables evaluation the anastomosis without the need for invasive surgery. However, this technique requires a well trained and well equipped endoscopy department.

Enhanced recovery after surgery and fast-track programs

Enhanced recovery after surgery (ERAS) programs have been developed and implemented with great success in colorectal surgery[99]. All recommendations by ERAS society for colonic surgery (see also: ) can potentially be implemented in gastric cancer patients, i.e., early removal of urinary catheter, prevention of postoperative ileus, postoperative analgesia, and early mobilization and resumption of normal diet[100]. Important to note is that ERAS protocols not only include recommendations on postoperative care, but also preoperative measures (e.g., counseling) and intra-operative measures (e.g., avoidance of salt and water overload and use of short acting anesthetic agents). In recent years efforts have been made to develop, implement and evaluate the effect of similar programs in gastric cancer surgery. Studies on the timing of oral intake after gastrectomy for gastric cancer are sparse. Small studies that exist have evaluated early oral feeding as safe and feasible[101]. This study started liquid intake on days 1-2 and soft diet on postoperative day 3. Similar studies showed significant shorter hospital stay (e.g., 5.7 d vs 9.2 d) and earlier return of bowel function[102-104]. Although the strategies for early oral feeding were different, ranging from oral diet on day one to liquid diet on day two followed by soft diet from day three until discharge, their findings were that it is safe and potentially leads to shorter hospital-stay.

A randomized comparison between fast-track surgery and conventional care in gastric cancer patients (n = 45 and n = 47 respectively) showed less stress response in the fast-track surgery group[105]. This was measured by serum tumor necrosis factor-alfa, CRP and interleukin-6 levels. Also, fast-track patients had a shorter hospital stay and higher quality of life with no increase in complications. Yamada et al[106] compared ERAS (n = 91) with conventional care (n = 100) after gastrectomy and found that ERAS was associated with less postoperative pain and analgesics use. There was no difference in complication rates between ERAS and conventional care. They did not find a significant difference in mean length-of-stay.

Implementation of a fast-track or ERAS program was also investigated as an addition to laparoscopic procedures[107-109]. A consecutive series of 32 patients showed that it was safe and had similar postoperative results[107]. In addition, a randomized clinical trial with 22 fast-track and 22 conventional care patients showed a shorter length of stay for fast-track patients (5 d vs 8 d, P < 0.001) but no difference was noted for postoperative pain[108]. Chen Hu et al[109] found that the laparoscopic assisted procedure with the addition of a fast-track approach resulted in shortest length-of-stay.


In Western countries the incidence of gastric cancer is relatively low. Annual hospital volume can therefore be low in institutions in non-centralized regions. Centralization offers a chance to increase volumes in selected centers. Increased hospital volume leads to better treatment results in gastric cancer surgery[110]. More recent studies support this idea and show that increased volumes are associated with lower short-term mortality and improved survival[111,112]. Other literature suggests that hospital volume is not a determinant for disease-free survival or overall survival in gastric cancer surgery survivors (i.e., perioperative mortality excluded)[113]. Although the optimal number of procedures is not clearly defined in literature, expert panel based recommendations state that an annual volume of more than 15 for an institution and more than 6 for the individual surgeon are held to be appropriate[52]. They also state that the necessity of these volumes is undetermined.

In several countries clinical auditing has been initiated in various fields of surgery. It is considered an important tool for quality assessment and the identification of factors needing improvement. Furthermore, clinical audits provide a unique dataset for research as well. For gastric cancer surgery, a nationwide audit has been initiated in the Netherlands, the Dutch upper GI cancer audit (DUCA) ( ). The DUCA has become a performance index for gastric cancer surgeons as it was also adopted as a quality indicator for the health care inspectorate. It is expected that postoperative mortality and anastomotic leakage rates will decrease but few reports have been published in the Netherlands so far. From 2011 to 2012 30-d mortality decreased from 8.8% to 6.7% (see: ). Whether these improvements are directly related to the introduction of the audit has to be determined. At least, it can be stated that the DUCA has effectuated increased awareness of and insight in aspects of improvement.

Clinical audits have revealed several interesting findings with respect to postoperative complications. Hospitals with higher mortality rates had only slightly higher incidences of postoperative complications. But in high volume centers these patients with a serious complication had less chance dying than in high-mortality centers. This phenomenon is addressed as failure to rescue and was not only described for gastrectomy but also for other gastro-intestinal operations[114]. Data from the American College of Surgeons National Surgical Quality Improvement Program showed that although complication incidences did not vary between hospitals, mortality rates, largely contributed to death after major complications, significantly varied, indicating that timely recognition and treatment of complications deserves greater attention[115]. Future research should aim at identifying and improving the fundamental aspects causing failure to rescue.


Surgical risk assessment is complex and difficult. In preoperative assessment of gastric cancer patients age should not be a criterion on which treatment decisions are be made. Rather, presence of comorbidities, nutritional status and geriatric frailty should be assessed and taken into account. Future studies should further determine the role geriatric frailty and nutritional status assessment has in the preoperative evaluation of gastric cancer surgery patients, especially in Western counties, as these patients are more often at an advanced age.

Improving postoperative recovery by using fast-track and ERAS protocols has yielded improved results. The timing of oral intake is still at debate, but early oral feeding (postoperative days 1-3) seems to be feasible and safe. Further studies have to verify this and investigate its effect on morbidity, length-of-stay and quality of life/patient satisfaction. Also optimal fast-track/ERAS programs have to be developed to further improve outcome and quality of care for these patients.

Introduction of laparoscopic surgery has improved short-term postoperative outcome for gastric cancer patients. Oncological safety remains an area of debate, but available literature suggest that oncological safety is not compromised.

In conclusion, although advances have been made in pre-, intra- and postoperative stage of gastric cancer surgery to improve the outcome of these patients, there still remain many areas for improvement and future research.


P- Reviewer: Nakayama Y, Zhu BS, Zielinski J S- Editor: Gou SX L- Editor: A E- Editor: Ma S

1.  Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380:2095-2128.  [PubMed]  [DOI]
2.  Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin. 2010;60:277-300.  [PubMed]  [DOI]
3.  Soerjomataram I, Lortet-Tieulent J, Parkin DM, Ferlay J, Mathers C, Forman D, Bray F. Global burden of cancer in 2008: a systematic analysis of disability-adjusted life-years in 12 world regions. Lancet. 2012;380:1840-1850.  [PubMed]  [DOI]
4.  Dikken JL, van Sandick JW, Allum WH, Johansson J, Jensen LS, Putter H, Coupland VH, Wouters MW, Lemmens VE, van de Velde CJ. Differences in outcomes of oesophageal and gastric cancer surgery across Europe. Br J Surg. 2013;100:83-94.  [PubMed]  [DOI]
5.  Bösing NM, Goretzki PE, Röher HD. Gastric cancer: which patients benefit from systematic lymphadenectomy? Eur J Surg Oncol. 2000;26:498-505.  [PubMed]  [DOI]
6.  Kubota T, Hiki N, Sano T, Nomura S, Nunobe S, Kumagai K, Aikou S, Watanabe R, Kosuga T, Yamaguchi T. Prognostic significance of complications after curative surgery for gastric cancer. Ann Surg Oncol. 2014;21:891-898.  [PubMed]  [DOI]
7.  Mariette C, De Botton ML, Piessen G. Surgery in esophageal and gastric cancer patients: what is the role for nutrition support in your daily practice? Ann Surg Oncol. 2012;19:2128-2134.  [PubMed]  [DOI]
8.  Bickenbach K, Strong VE. Comparisons of Gastric Cancer Treatments: East vs. West. J Gastric Cancer. 2012;12:55-62.  [PubMed]  [DOI]
9.  Fitz-Henry J. The ASA classification and peri-operative risk. Ann R Coll Surg Engl. 2011;93:185-187.  [PubMed]  [DOI]
10.  Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40:373-383.  [PubMed]  [DOI]
11.  Grendar J, Shaheen AA, Myers RP, Parker R, Vollmer CM, Ball CG, Quan ML, Kaplan GG, Al-Manasra T, Dixon E. Predicting in-hospital mortality in patients undergoing complex gastrointestinal surgery: determining the optimal risk adjustment method. Arch Surg. 2012;147:126-135.  [PubMed]  [DOI]
12.  Hsu JT, Liu MS, Wang F, Chang CJ, Hwang TL, Jan YY, Yeh TS. Standard radical gastrectomy in octogenarians and nonagenarians with gastric cancer: are short-term surgical results and long-term survival substantial? J Gastrointest Surg. 2012;16:728-737.  [PubMed]  [DOI]
13.  Pisanu A, Montisci A, Piu S, Uccheddu A. Curative surgery for gastric cancer in the elderly: treatment decisions, surgical morbidity, mortality, prognosis and quality of life. Tumori. 2007;93:478-484.  [PubMed]  [DOI]
14.  Lübke T, Mönig SP, Schneider PM, Hölscher AH, Bollschweiler E. [Does Charlson-comorbidity index correlate with short-term outcome in patients with gastric cancer?]. Zentralbl Chir. 2003;128:970-976.  [PubMed]  [DOI]
15.  Jeong O, Ryu SY, Zhao XF, Jung MR, Kim KY, Park YK. Short-term surgical outcomes and operative risks of laparoscopic total gastrectomy (LTG) for gastric carcinoma: experience at a large-volume center. Surg Endosc. 2012;26:3418-3425.  [PubMed]  [DOI]
16.  Bickenbach KA, Denton B, Gonen M, Brennan MF, Coit DG, Strong VE. Impact of obesity on perioperative complications and long-term survival of patients with gastric cancer. Ann Surg Oncol. 2013;20:780-787.  [PubMed]  [DOI]
17.  Kunisaki C, Makino H, Takagawa R, Sato K, Kawamata M, Kanazawa A, Yamamoto N, Nagano Y, Fujii S, Ono HA. Predictive factors for surgical complications of laparoscopy-assisted distal gastrectomy for gastric cancer. Surg Endosc. 2009;23:2085-2093.  [PubMed]  [DOI]
18.  Oh SJ, Hyung WJ, Li C, Song J, Rha SY, Chung HC, Choi SH, Noh SH. Effect of being overweight on postoperative morbidity and long-term surgical outcomes in proximal gastric carcinoma. J Gastroenterol Hepatol. 2009;24:475-479.  [PubMed]  [DOI]
19.  Kulig J, Sierzega M, Kolodziejczyk P, Dadan J, Drews M, Fraczek M, Jeziorski A, Krawczyk M, Starzynska T, Wallner G. Implications of overweight in gastric cancer: A multicenter study in a Western patient population. Eur J Surg Oncol. 2010;36:969-976.  [PubMed]  [DOI]
20.  Noshiro H, Shimizu S, Nagai E, Ohuchida K, Tanaka M. Laparoscopy-assisted distal gastrectomy for early gastric cancer: is it beneficial for patients of heavier weight? Ann Surg. 2003;238:680-685.  [PubMed]  [DOI]
21.  Tsunoda S, Okabe H, Obama K, Tanaka E, Akagami M, Kinjo Y, Sakai Y. Laparoscopic gastrectomy for patients with a history of upper abdominal surgery: results of a matched-pair analysis. Surg Today. 2014;44:271-276.  [PubMed]  [DOI]
22.  Nunobe S, Hiki N, Fukunaga T, Tokunaga M, Ohyama S, Seto Y, Yamaguchi T. Previous laparotomy is not a contraindication to laparoscopy-assisted gastrectomy for early gastric cancer. World J Surg. 2008;32:1466-1472.  [PubMed]  [DOI]
23.  Dewys WD, Begg C, Lavin PT, Band PR, Bennett JM, Bertino JR, Cohen MH, Douglass HO, Engstrom PF, Ezdinli EZ. Prognostic effect of weight loss prior to chemotherapy in cancer patients. Eastern Cooperative Oncology Group. Am J Med. 1980;69:491-497.  [PubMed]  [DOI]
24.  Correia MI, Waitzberg DL. The impact of malnutrition on morbidity, mortality, length of hospital stay and costs evaluated through a multivariate model analysis. Clin Nutr. 2003;22:235-239.  [PubMed]  [DOI]
25.  Lomivorotov VV, Efremov SM, Boboshko VA, Nikolaev DA, Vedernikov PE, Deryagin MN, Lomivorotov VN, Karaskov AM. Prognostic value of nutritional screening tools for patients scheduled for cardiac surgery. Interact Cardiovasc Thorac Surg. 2013;16:612-618.  [PubMed]  [DOI]
26.  Tu MY, Chien TW, Chou MT. Using a nutritional screening tool to evaluate the nutritional status of patients with colorectal cancer. Nutr Cancer. 2012;64:323-330.  [PubMed]  [DOI]
27.  Kruizenga HM, Seidell JC, de Vet HC, Wierdsma NJ, van Bokhorst-de van der Schueren MA. Development and validation of a hospital screening tool for malnutrition: the short nutritional assessment questionnaire (SNAQ). Clin Nutr. 2005;24:75-82.  [PubMed]  [DOI]
28.  van Venrooij LM, van Leeuwen PA, Hopmans W, Borgmeijer-Hoelen MM, de Vos R, De Mol BA. Accuracy of quick and easy undernutrition screening tools--Short Nutritional Assessment Questionnaire, Malnutrition Universal Screening Tool, and modified Malnutrition Universal Screening Tool--in patients undergoing cardiac surgery. J Am Diet Assoc. 2011;111:1924-1930.  [PubMed]  [DOI]
29.  Guo W, Ou G, Li X, Huang J, Liu J, Wei H. Screening of the nutritional risk of patients with gastric carcinoma before operation by NRS 2002 and its relationship with postoperative results. J Gastroenterol Hepatol. 2010;25:800-803.  [PubMed]  [DOI]
30.  Tegels JJ, de Maat MF, Hulsewé KW, Hoofwijk AG, Stoot JH. Value of geriatric frailty and nutritional status assessment in predicting postoperative mortality in gastric cancer surgery. J Gastrointest Surg. 2014;18:439-445; discussion 445-446.  [PubMed]  [DOI]
31.  Awad S, Tan BH, Cui H, Bhalla A, Fearon KC, Parsons SL, Catton JA, Lobo DN. Marked changes in body composition following neoadjuvant chemotherapy for oesophagogastric cancer. Clin Nutr. 2012;31:74-77.  [PubMed]  [DOI]
32.  Peng PD, van Vledder MG, Tsai S, de Jong MC, Makary M, Ng J, Edil BH, Wolfgang CL, Schulick RD, Choti MA. Sarcopenia negatively impacts short-term outcomes in patients undergoing hepatic resection for colorectal liver metastasis. HPB (Oxford). 2011;13:439-446.  [PubMed]  [DOI]
33.  Peng P, Hyder O, Firoozmand A, Kneuertz P, Schulick RD, Huang D, Makary M, Hirose K, Edil B, Choti MA. Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma. J Gastrointest Surg. 2012;16:1478-1486.  [PubMed]  [DOI]
34.  van Vledder MG, Levolger S, Ayez N, Verhoef C, Tran TC, Ijzermans JN. Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br J Surg. 2012;99:550-557.  [PubMed]  [DOI]
35.  Marrelli D, Roviello F, De Stefano A, Vuolo G, Brandi C, Lottini M, Pinto E. Surgical treatment of gastrointestinal carcinomas in octogenarians: risk factors for complications and long-term outcome. Eur J Surg Oncol. 2000;26:371-376.  [PubMed]  [DOI]
36.  Bozzetti F, Gianotti L, Braga M, Di Carlo V, Mariani L. Postoperative complications in gastrointestinal cancer patients: the joint role of the nutritional status and the nutritional support. Clin Nutr. 2007;26:698-709.  [PubMed]  [DOI]
37.  Pacelli F, Bossola M, Rosa F, Tortorelli AP, Papa V, Doglietto GB. Is malnutrition still a risk factor of postoperative complications in gastric cancer surgery? Clin Nutr. 2008;27:398-407.  [PubMed]  [DOI]
38.  Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56:M146-M156.  [PubMed]  [DOI]
39.  Dasgupta M, Rolfson DB, Stolee P, Borrie MJ, Speechley M. Frailty is associated with postoperative complications in older adults with medical problems. Arch Gerontol Geriatr. 2009;48:78-83.  [PubMed]  [DOI]
40.  Robinson TN, Eiseman B, Wallace JI, Church SD, McFann KK, Pfister SM, Sharp TJ, Moss M. Redefining geriatric preoperative assessment using frailty, disability and co-morbidity. Ann Surg. 2009;250:449-455.  [PubMed]  [DOI]
41.  Lee DH, Buth KJ, Martin BJ, Yip AM, Hirsch GM. Frail patients are at increased risk for mortality and prolonged institutional care after cardiac surgery. Circulation. 2010;121:973-978.  [PubMed]  [DOI]
42.  Makary MA, Segev DL, Pronovost PJ, Syin D, Bandeen-Roche K, Patel P, Takenaga R, Devgan L, Holzmueller CG, Tian J. Frailty as a predictor of surgical outcomes in older patients. J Am Coll Surg. 2010;210:901-908.  [PubMed]  [DOI]
43.  Revenig LM, Canter DJ, Taylor MD, Tai C, Sweeney JF, Sarmiento JM, Kooby DA, Maithel SK, Master VA, Ogan K. Too frail for surgery? Initial results of a large multidisciplinary prospective study examining preoperative variables predictive of poor surgical outcomes. J Am Coll Surg. 2013;217:665-670.e1.  [PubMed]  [DOI]
44.  Schuurmans H, Steverink N, Lindenberg S, Frieswijk N, Slaets JP. Old or frail: what tells us more? J Gerontol A Biol Sci Med Sci. 2004;59:M962-M965.  [PubMed]  [DOI]
45.  Carli F, Zavorsky GS. Optimizing functional exercise capacity in the elderly surgical population. Curr Opin Clin Nutr Metab Care. 2005;8:23-32.  [PubMed]  [DOI]
46.  Li C, Carli F, Lee L, Charlebois P, Stein B, Liberman AS, Kaneva P, Augustin B, Wongyingsinn M, Gamsa A. Impact of a trimodal prehabilitation program on functional recovery after colorectal cancer surgery: a pilot study. Surg Endosc. 2013;27:1072-1082.  [PubMed]  [DOI]
47.  Mayo NE, Feldman L, Scott S, Zavorsky G, Kim do J, Charlebois P, Stein B, Carli F. Impact of preoperative change in physical function on postoperative recovery: argument supporting prehabilitation for colorectal surgery. Surgery. 2011;150:505-514.  [PubMed]  [DOI]
48.  Silver JK, Baima J. Cancer prehabilitation: an opportunity to decrease treatment-related morbidity, increase cancer treatment options, and improve physical and psychological health outcomes. Am J Phys Med Rehabil. 2013;92:715-727.  [PubMed]  [DOI]
49.  Gretschel S, Siegel R, Estévez-Schwarz L, Hünerbein M, Schneider U, Schlag PM. Surgical strategies for gastric cancer with synchronous peritoneal carcinomatosis. Br J Surg. 2006;93:1530-1535.  [PubMed]  [DOI]
50.  Mahadevan D, Sudirman A, Kandasami P, Ramesh G. Laparoscopic staging in gastric cancer: An essential step in its management. J Minim Access Surg. 2010;6:111-113.  [PubMed]  [DOI]
51.  Leake PA, Cardoso R, Seevaratnam R, Lourenco L, Helyer L, Mahar A, Law C, Coburn NG. A systematic review of the accuracy and indications for diagnostic laparoscopy prior to curative-intent resection of gastric cancer. Gastric Cancer. 2012;15 Suppl 1:S38-S47.  [PubMed]  [DOI]
52.  Coburn N, Seevaratnam R, Paszat L, Helyer L, Law C, Swallow C, Cardosa R, Mahar A, Lourenco LG, Dixon M. Optimal management of gastric cancer: results from an international RAND/UCLA expert panel. Ann Surg. 2014;259:102-108.  [PubMed]  [DOI]
53.  Bentrem D, Wilton A, Mazumdar M, Brennan M, Coit D. The value of peritoneal cytology as a preoperative predictor in patients with gastric carcinoma undergoing a curative resection. Ann Surg Oncol. 2005;12:347-353.  [PubMed]  [DOI]
54.  Lee SD, Ryu KW, Eom BW, Lee JH, Kook MC, Kim YW. Prognostic significance of peritoneal washing cytology in patients with gastric cancer. Br J Surg. 2012;99:397-403.  [PubMed]  [DOI]
55.  Roviello F, Caruso S, Neri A, Marrelli D. Treatment and prevention of peritoneal carcinomatosis from gastric cancer by cytoreductive surgery and hyperthermic intraperitoneal chemotherapy: overview and rationale. Eur J Surg Oncol. 2013;39:1309-1316.  [PubMed]  [DOI]
56.  Kitano S, Iso Y, Moriyama M, Sugimachi K. Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc. 1994;4:146-148.  [PubMed]  [DOI]
57.  Adachi Y, Shiraishi N, Shiromizu A, Bandoh T, Aramaki M, Kitano S. Laparoscopy-assisted Billroth I gastrectomy compared with conventional open gastrectomy. Arch Surg. 2000;135:806-810.  [PubMed]  [DOI]
58.  Kitano S, Shiraishi N, Kakisako K, Yasuda K, Inomata M, Adachi Y. Laparoscopy-assisted Billroth-I gastrectomy (LADG) for cancer: our 10 years’ experience. Surg Laparosc Endosc Percutan Tech. 2002;12:204-207.  [PubMed]  [DOI]
59.  Viñuela EF, Gonen M, Brennan MF, Coit DG, Strong VE. Laparoscopic versus open distal gastrectomy for gastric cancer: a meta-analysis of randomized controlled trials and high-quality nonrandomized studies. Ann Surg. 2012;255:446-456.  [PubMed]  [DOI]
60.  Chen XZ, Hu JK, Yang K, Wang L, Lu QC. Short-term evaluation of laparoscopy-assisted distal gastrectomy for predictive early gastric cancer: a meta-analysis of randomized controlled trials. Surg Laparosc Endosc Percutan Tech. 2009;19:277-284.  [PubMed]  [DOI]
61.  Kodera Y, Fujiwara M, Ohashi N, Nakayama G, Koike M, Morita S, Nakao A. Laparoscopic surgery for gastric cancer: a collective review with meta-analysis of randomized trials. J Am Coll Surg. 2010;211:677-686.  [PubMed]  [DOI]
62.  Memon MA, Khan S, Yunus RM, Barr R, Memon B. Meta-analysis of laparoscopic and open distal gastrectomy for gastric carcinoma. Surg Endosc. 2008;22:1781-1789.  [PubMed]  [DOI]
63.  Ohtani H, Tamamori Y, Noguchi K, Azuma T, Fujimoto S, Oba H, Aoki T, Minami M, Hirakawa K. Meta-analysis of laparoscopy-assisted and open distal gastrectomy for gastric cancer. J Surg Res. 2011;171:479-485.  [PubMed]  [DOI]
64.  Chen K, Xu XW, Zhang RC, Pan Y, Wu D, Mou YP. Systematic review and meta-analysis of laparoscopy-assisted and open total gastrectomy for gastric cancer. World J Gastroenterol. 2013;19:5365-5376.  [PubMed]  [DOI]
65.  Huscher CG, Mingoli A, Sgarzini G, Sansonetti A, Di Paola M, Recher A, Ponzano C. Laparoscopic versus open subtotal gastrectomy for distal gastric cancer: five-year results of a randomized prospective trial. Ann Surg. 2005;241:232-237.  [PubMed]  [DOI]
66.  Siani LM, Ferranti F, De Carlo A, Quintiliani A. Completely laparoscopic versus open total gastrectomy in stage I-III/C gastric cancer: safety, efficacy and five-year oncologic outcome. Minerva Chir. 2012;67:319-326.  [PubMed]  [DOI]
67.  Dulucq JL, Wintringer P, Stabilini C, Solinas L, Perissat J, Mahajna A. Laparoscopic and open gastric resections for malignant lesions: a prospective comparative study. Surg Endosc. 2005;19:933-938.  [PubMed]  [DOI]
68.  Park do J, Han SU, Hyung WJ, Kim MC, Kim W, Ryu SY, Ryu SW, Song KY, Lee HJ, Cho GS. Long-term outcomes after laparoscopy-assisted gastrectomy for advanced gastric cancer: a large-scale multicenter retrospective study. Surg Endosc. 2012;26:1548-1553.  [PubMed]  [DOI]
69.  Lee MS, Lee JH, Park do J, Lee HJ, Kim HH, Yang HK. Comparison of short- and long-term outcomes of laparoscopic-assisted total gastrectomy and open total gastrectomy in gastric cancer patients. Surg Endosc. 2013;27:2598-2605.  [PubMed]  [DOI]
70.  Wu CW, Hsiung CA, Lo SS, Hsieh MC, Chen JH, Li AF, Lui WY, Whang-Peng J. Nodal dissection for patients with gastric cancer: a randomised controlled trial. Lancet Oncol. 2006;7:309-315.  [PubMed]  [DOI]
71.  Bonenkamp JJ, Songun I, Hermans J, Sasako M, Welvaart K, Plukker JT, van Elk P, Obertop H, Gouma DJ, Taat CW. Randomised comparison of morbidity after D1 and D2 dissection for gastric cancer in 996 Dutch patients. Lancet. 1995;345:745-748.  [PubMed]  [DOI]
72.  Cuschieri A, Fayers P, Fielding J, Craven J, Bancewicz J, Joypaul V, Cook P. Postoperative morbidity and mortality after D1 and D2 resections for gastric cancer: preliminary results of the MRC randomised controlled surgical trial. The Surgical Cooperative Group. Lancet. 1996;347:995-999.  [PubMed]  [DOI]
73.  Songun I, Putter H, Kranenbarg EM, Sasako M, van de Velde CJ. Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol. 2010;11:439-449.  [PubMed]  [DOI]
74.  Degiuli M, Sasako M, Ponti A. Morbidity and mortality in the Italian Gastric Cancer Study Group randomized clinical trial of D1 versus D2 resection for gastric cancer. Br J Surg. 2010;97:643-649.  [PubMed]  [DOI]
75.  Sano T, Sasako M, Yamamoto S, Nashimoto A, Kurita A, Hiratsuka M, Tsujinaka T, Kinoshita T, Arai K, Yamamura Y. Gastric cancer surgery: morbidity and mortality results from a prospective randomized controlled trial comparing D2 and extended para-aortic lymphadenectomy--Japan Clinical Oncology Group study 9501. J Clin Oncol. 2004;22:2767-2773.  [PubMed]  [DOI]
76.  Sasako M, Sano T, Yamamoto S, Kurokawa Y, Nashimoto A, Kurita A, Hiratsuka M, Tsujinaka T, Kinoshita T, Arai K. D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer. N Engl J Med. 2008;359:453-462.  [PubMed]  [DOI]
77.  Kochi M, Fujii M, Kanamori N, Kaiga T, Mihara Y, Funada T, Tamegai H, Takayama Y, Yoshida N, Takayama T. D2 gastrectomy with versus without bursectomy for gastric cancer. Am J Clin Oncol. 2014;37:222-226.  [PubMed]  [DOI]
78.  Eom BW, Joo J, Kim YW, Bae JM, Park KB, Lee JH, Ryu KW, Kook MC. Role of bursectomy for advanced gastric cancer: result of a case-control study from a large volume hospital. Eur J Surg Oncol. 2013;39:1407-1414.  [PubMed]  [DOI]
79.  Fujita J, Kurokawa Y, Sugimoto T, Miyashiro I, Iijima S, Kimura Y, Takiguchi S, Fujiwara Y, Mori M, Doki Y. Survival benefit of bursectomy in patients with resectable gastric cancer: interim analysis results of a randomized controlled trial. Gastric Cancer. 2012;15:42-48.  [PubMed]  [DOI]
80.  Nomura E, Lee SW, Bouras G, Tokuhara T, Hayashi M, Hiramatsu M, Okuda J, Tanigawa N. Functional outcomes according to the size of the gastric remnant and type of reconstruction following laparoscopic distal gastrectomy for gastric cancer. Gastric Cancer. 2011;14:279-284.  [PubMed]  [DOI]
81.  Kojima K, Yamada H, Inokuchi M, Kawano T, Sugihara K. A comparison of Roux-en-Y and Billroth-I reconstruction after laparoscopy-assisted distal gastrectomy. Ann Surg. 2008;247:962-967.  [PubMed]  [DOI]
82.  Ishikawa M, Kitayama J, Kaizaki S, Nakayama H, Ishigami H, Fujii S, Suzuki H, Inoue T, Sako A, Asakage M. Prospective randomized trial comparing Billroth I and Roux-en-Y procedures after distal gastrectomy for gastric carcinoma. World J Surg. 2005;29:1415-120; discussion 1421.  [PubMed]  [DOI]
83.  Inokuchi M, Kojima K, Yamada H, Kato K, Hayashi M, Motoyama K, Sugihara K. Long-term outcomes of Roux-en-Y and Billroth-I reconstruction after laparoscopic distal gastrectomy. Gastric Cancer. 2013;16:67-73.  [PubMed]  [DOI]
84.  Takiguchi S, Yamamoto K, Hirao M, Imamura H, Fujita J, Yano M, Kobayashi K, Kimura Y, Kurokawa Y, Mori M. A comparison of postoperative quality of life and dysfunction after Billroth I and Roux-en-Y reconstruction following distal gastrectomy for gastric cancer: results from a multi-institutional RCT. Gastric Cancer. 2012;15:198-205.  [PubMed]  [DOI]
85.  Imamura H, Takiguchi S, Yamamoto K, Hirao M, Fujita J, Miyashiro I, Kurokawa Y, Fujiwara Y, Mori M, Doki Y. Morbidity and mortality results from a prospective randomized controlled trial comparing Billroth I and Roux-en-Y reconstructive procedures after distal gastrectomy for gastric cancer. World J Surg. 2012;36:632-637.  [PubMed]  [DOI]
86.  Wu Q, Yu JC, Kang WM, Ma ZQ. Short-term effects of supplementary feeding with enteral nutrition via jejunostomy catheter on post-gastrectomy gastric cancer patients. Chin Med J (Engl). 2011;124:3297-3301.  [PubMed]  [DOI]
87.  Patel SH, Kooby DA, Staley CA, Maithel SK. An assessment of feeding jejunostomy tube placement at the time of resection for gastric adenocarcinoma. J Surg Oncol. 2013;107:728-734.  [PubMed]  [DOI]
88.  Llaguna OH, Kim HJ, Deal AM, Calvo BF, Stitzenberg KB, Meyers MO. Utilization and morbidity associated with placement of a feeding jejunostomy at the time of gastroesophageal resection. J Gastrointest Surg. 2011;15:1663-1669.  [PubMed]  [DOI]
89.  Deguchi Y, Fukagawa T, Morita S, Ohashi M, Saka M, Katai H. Identification of risk factors for esophagojejunal anastomotic leakage after gastric surgery. World J Surg. 2012;36:1617-1622.  [PubMed]  [DOI]
90.  Migita K, Takayama T, Matsumoto S, Wakatsuki K, Enomoto K, Tanaka T, Ito M, Nakajima Y. Risk factors for esophagojejunal anastomotic leakage after elective gastrectomy for gastric cancer. J Gastrointest Surg. 2012;16:1659-1665.  [PubMed]  [DOI]
91.  Tsou CC, Lo SS, Fang WL, Wu CW, Chen JH, Hsieh MC, Shen KH. Risk factors and management of anastomotic leakage after radical gastrectomy for gastric cancer. Hepatogastroenterology. 2011;58:218-223.  [PubMed]  [DOI]
92.  Schurawitzki H, Karnel F, Stiglbauer R, Schimmerl S, Salomonowitz E. CT-guided percutaneous drainage and fluid aspiration in intensive care patients. Acta Radiol. 1992;33:131-136.  [PubMed]  [DOI]
93.  Lambiase RE, Deyoe L, Cronan JJ, Dorfman GS. Percutaneous drainage of 335 consecutive abscesses: results of primary drainage with 1-year follow-up. Radiology. 1992;184:167-179.  [PubMed]  [DOI]
94.  Lang H, Piso P, Stukenborg C, Raab R, Jähne J. Management and results of proximal anastomotic leaks in a series of 1114 total gastrectomies for gastric carcinoma. Eur J Surg Oncol. 2000;26:168-171.  [PubMed]  [DOI]
95.  Etoh T, Inomata M, Shiraishi N, Kitano S. Revisional surgery after gastrectomy for gastric cancer: review of the literature. Surg Laparosc Endosc Percutan Tech. 2010;20:332-337.  [PubMed]  [DOI]
96.  Kim YJ, Shin SK, Lee HJ, Chung HS, Lee YC, Park JC, Hyung WJ, Noh SH, Kim CB, Lee SK. Endoscopic management of anastomotic leakage after gastrectomy for gastric cancer: how efficacious is it? Scand J Gastroenterol. 2013;48:111-118.  [PubMed]  [DOI]
97.  Roy-Choudhury SH, Nicholson AA, Wedgwood KR, Mannion RA, Sedman PC, Royston CM, Breen DJ. Symptomatic malignant gastroesophageal anastomotic leak: management with covered metallic esophageal stents. AJR Am J Roentgenol. 2001;176:161-165.  [PubMed]  [DOI]
98.  Kwak HS, Lee JM, Jin GY, Han YM, Yang DH. Treatment of gastrojejunal anastomotic leak with a covered metallic stent. Hepatogastroenterology. 2003;50:62-64.  [PubMed]  [DOI]
99.  Gillissen F, Hoff C, Maessen JM, Winkens B, Teeuwen JH, von Meyenfeldt MF, Dejong CH. Structured synchronous implementation of an enhanced recovery program in elective colonic surgery in 33 hospitals in The Netherlands. World J Surg. 2013;37:1082-1093.  [PubMed]  [DOI]
100.  Gustafsson UO, Scott MJ, Schwenk W, Demartines N, Roulin D, Francis N, McNaught CE, MacFie J, Liberman AS, Soop M. Guidelines for perioperative care in elective colonic surgery: Enhanced Recovery After Surgery (ERAS®) Society recommendations. Clin Nutr. 2012;31:783-800.  [PubMed]  [DOI]
101.  Jo DH, Jeong O, Sun JW, Jeong MR, Ryu SY, Park YK. Feasibility study of early oral intake after gastrectomy for gastric carcinoma. J Gastric Cancer. 2011;11:101-108.  [PubMed]  [DOI]
102.  Hur H, Si Y, Kang WK, Kim W, Jeon HM. Effects of early oral feeding on surgical outcomes and recovery after curative surgery for gastric cancer: pilot study results. World J Surg. 2009;33:1454-1458.  [PubMed]  [DOI]
103.  Suehiro T, Matsumata T, Shikada Y, Sugimachi K. Accelerated rehabilitation with early postoperative oral feeding following gastrectomy. Hepatogastroenterology. 2004;51:1852-1855.  [PubMed]  [DOI]
104.  Hur H, Kim SG, Shim JH, Song KY, Kim W, Park CH, Jeon HM. Effect of early oral feeding after gastric cancer surgery: a result of randomized clinical trial. Surgery. 2011;149:561-568.  [PubMed]  [DOI]
105.  Wang D, Kong Y, Zhong B, Zhou X, Zhou Y. Fast-track surgery improves postoperative recovery in patients with gastric cancer: a randomized comparison with conventional postoperative care. J Gastrointest Surg. 2010;14:620-627.  [PubMed]  [DOI]
106.  Yamada T, Hayashi T, Cho H, Yoshikawa T, Taniguchi H, Fukushima R, Tsuburaya A. Usefulness of enhanced recovery after surgery protocol as compared with conventional perioperative care in gastric surgery. Gastric Cancer. 2012;15:34-41.  [PubMed]  [DOI]
107.  Grantcharov TP, Kehlet H. Laparoscopic gastric surgery in an enhanced recovery programme. Br J Surg. 2010;97:1547-1551.  [PubMed]  [DOI]
108.  Kim JW, Kim WS, Cheong JH, Hyung WJ, Choi SH, Noh SH. Safety and efficacy of fast-track surgery in laparoscopic distal gastrectomy for gastric cancer: a randomized clinical trial. World J Surg. 2012;36:2879-2887.  [PubMed]  [DOI]
109.  Chen Hu J, Xin Jiang L, Cai L, Tao Zheng H, Yuan Hu S, Bing Chen H, Chang Wu G, Fei Zhang Y, Chuan Lv Z. Preliminary experience of fast-track surgery combined with laparoscopy-assisted radical distal gastrectomy for gastric cancer. J Gastrointest Surg. 2012;16:1830-1839.  [PubMed]  [DOI]
110.  Meyer HJ. The influence of case load and the extent of resection on the quality of treatment outcome in gastric cancer. Eur J Surg Oncol. 2005;31:595-604.  [PubMed]  [DOI]
111.  Coupland VH, Lagergren J, Lüchtenborg M, Jack RH, Allum W, Holmberg L, Hanna GB, Pearce N, Møller H. Hospital volume, proportion resected and mortality from oesophageal and gastric cancer: a population-based study in England, 2004-2008. Gut. 2013;62:961-966.  [PubMed]  [DOI]
112.  Anderson O, Ni Z, Møller H, Coupland VH, Davies EA, Allum WH, Hanna GB. Hospital volume and survival in oesophagectomy and gastrectomy for cancer. Eur J Cancer. 2011;47:2408-2414.  [PubMed]  [DOI]
113.  Enzinger PC, Benedetti JK, Meyerhardt JA, McCoy S, Hundahl SA, Macdonald JS, Fuchs CS. Impact of hospital volume on recurrence and survival after surgery for gastric cancer. Ann Surg. 2007;245:426-434.  [PubMed]  [DOI]
114.  Ghaferi AA, Birkmeyer JD, Dimick JB. Hospital volume and failure to rescue with high-risk surgery. Med Care. 2011;49:1076-1081.  [PubMed]  [DOI]
115.  Ghaferi AA, Birkmeyer JD, Dimick JB. Variation in hospital mortality associated with inpatient surgery. N Engl J Med. 2009;361:1368-1375.  [PubMed]  [DOI]