Pattern of failure	Dutch D1/D2 trial^1,²	US Intergroup 0116³
Local	Gastric bed, anastomosis, regional lymph nodes	Gastric bed, anastomosis, residual stomach
Regional	Peritoneal carcinomatosa	Liver, lymph nodes, peritoneal carcinomatosa
Distant	Liver, lung, ovary and other organs	Outside the peritoneal cavity

Metastatic pathway

Lymphatic spread

Lymphatic spread is the most common mode of dissemination in gastric cancer. Lymph node metastasis is histologically proven in 10% of T1 tumours, and the rate increases as the invasion deepens, up to 80% of T4a tumours.^4,⁵

The lymphatic drainage system from the stomach has been well demonstrated in lymphography studies (Fig. 7.1). Unlike other parts of the digestive tract, the stomach has multidimensional mesenteries that contain dense lymphatic networks. Cancer cells can flow out of the stomach through any of these routes and by way of the nearby perigastric nodes, to reach the nodes around the coeliac artery. They then enter the para-aortic nodes and finally flow into the thoracic duct and systemic circulation. Systemic metastasis can occur via this route. In particular, bone marrow carcinomatosis occurs most frequently in cases with extensive nodal disease.^6,⁷

Figure 7.1 Lymphography of the stomach. Courtesy of K. Maruyama.

The stomach has the largest number of ‘regional lymph nodes’ of any organ in the human body. After a total gastrectomy with D2 lymphadenectomy, more than 40 lymph nodes can usually be collected with careful retrieval. Of the malignant tumours listed in the UICC/TNM classification,⁸ stomach cancer requires the largest number of nodes to be removed as a minimal requirement to allow a pN0 diagnosis (16 nodes) and the largest number of positive nodes for the highest N category (pN3b, 16 or more positive nodes).This suggests that lymphatic metastasis from gastric cancer may remain in the dense lymphatic filters for some time and that patients with nodal metastasis can still be cured by adequate dissection.

Peritoneal spread

Peritoneal metastasis is the most common type of failure after radical surgery for gastric cancer.⁹ Once the tumour penetrates the serosal surface (T4a), cancer cells may be scattered in the peritoneal space. They can be implanted in the gastric bed or any part of the peritoneal cavity and subsequently cause intestinal obstruction or ascites. Peritoneal metastasis is much more common in diffuse-type cancers than the intestinal type¹⁰ and later causes peritonitis carcinomatosa, a characteristic recurrent pattern of gastric cancer, which is relatively uncommon in colorectal adenocarcinomas that are mostly of the intestinal type.

Peritoneal lavage cytology is a sensitive test for this metastasis. Almost all patients with positive cytology subsequently develop peritoneal recurrence even after macroscopically curative surgery. In the UICC/TNM 7th edition,⁸ positive cytology (‘cy+’) has been included in the definition of pM1.

In general, surgery has no curative role in treating this mode of spread. However, in some exceptional cases where a small number of peritoneal metastases exist in the upper abdomen but peritoneal cytology is negative, complete removal of these visible nodules may bring cure.

Peritoneal metastasis is refractory to systemic chemotherapy. Intraperitoneal chemotherapy with or without hyperthermia is being vigorously tested in various centres. Some promising results have been reported,¹¹ but the evidence is not yet compelling.

The concept of radical gastric cancer surgery

Surgery plays an essential role in the curative treatment of gastric cancer. Although radical surgery has been attempted in many centres worldwide, it is Japanese surgeons who have been at the forefront of the practice of radical gastric resection and lymphadenectomy.

Gastric cancer surgery in Japan

The incidence of gastric cancer in Japan is among the highest in the world. Approximately 100 000 new cases are diagnosed every year, accounting for 11% of all cases in the world.¹⁶ The age- standardised incidence, however, has been rapidly decreasing as in other countries in the world, probably due to the decreasing infection of Helicobacter pylori. The peak incidence was in the 1950s (male 71, female 37 per 10⁵ population), the time when the mass screening programme was planned and the basic style of radical D2 gastrectomy was proposed (for reference, the incidences in 2010 were 12.4 and 7.1 respectively).

The Japanese Research Society for Gastric Cancer (JRSGC) was founded in 1962 and the nationwide registry started using a new documentation system, the General Rules for Gastric Cancer in Surgery and Pathology. This just preceded the UICC’s publication of the TNM classification for gastric cancer.

The General Rules (the English name was later changed to the Japanese Classification of Gastric Carcinoma) played a key role in the standardisation of surgery and pathology for gastric cancer in Japan. Detailed clinicopathological information, especially on lymph node metastasis, was prospectively collected from a large number of institutions and the optimal extent of lymphadenectomy was eagerly sought. The concept of ‘lymph node groups’ was established and the dissection of group 1 and 2 nodal stations was proposed as the standard radical surgery, which Japanese surgeons almost blindly accepted and followed.

This concept has never been tested in a randomised trial in Japan. As D2 gastrectomy is safely performed with good results in the country, Japanese surgeons think it unethical even to plan a trial in which half of the patients should undergo surgery that they consider inferior (D1).

Development of gastric cancer surgery in the West

The Japanese documentation system and excellent treatment results influenced the Western concept of radical surgery for gastric cancer. Some surgeons visited Japanese institutions to convince themselves of the feasibility and efficacy of the technique and have successfully reproduced the results in the West.^17,¹⁸ However, most non-specialist surgeons could not overcome their scepticism and were reluctant to practise this aggressive surgery in their patients. An important obstacle is the difficulty in directly comparing the results between Japan and the West due to the following two issues.

Different staging systems

The UICC and the AJCC unified their TNM staging system in their fourth edition in 1985. The N category in that edition was defined according to the anatomical location of the involved lymph nodes: metastasis in the perigastric nodes within 3 cm of the primary tumour was staged as N1, metastasis in the other perigastric nodes and those along the named branches of the coeliac artery as N2. Although the Japanese definitions of nodal groups 1 and 2 were different, as detailed later, the basic concept of the two systems was similar in that the anatomical location of the involved lymph nodes determined the N category. Thus, the treatment results of tumours staged by the two different systems were able to be compared, neglecting minor differences.

In 1997 the UICC/AJCC adopted the numerical N category in the fifth edition, and the Japanese classification and the TNM classification became totally distinct systems. The Japanese results were able to be expressed using the new TNM system because the number of positive nodes in each case was also recorded, but the reverse was impossible because the anatomical data were no longer available in the West. Japanese surgeons and pathologists continued to use their system as the primary staging method, thus sticking to the surgical significance of lymph node anatomy, and they use the TNM system only when they write English papers. On the other hand, Western surgeons’ interest in lymphadenectomy may have diminished because the N category was determined regardless of the extent of lymphadenectomy.

Different disease hypotheses

A hypothesis that gastric cancer in the West may be a different disease to that in Japan prevails and prevents positive discussion to advance optimal treatment for gastric cancer patients on a global level. In the studies biologically analysing and comparing surgical specimens, no evidence has been shown to support the hypothesis.^19,²⁰ The following are the currently discussed differences.

Proximal location: It has been repeatedly highlighted that Western gastric cancers are predominantly located in the proximal stomach while Japanese tumours are found mostly in the distal stomach. This might suggest that these are different diseases. However, this needs careful consideration.

Adenocarcinoma of the lower oesophagus and the oesophagogastric junction is one of the most rapidly increasing malignant tumours in the West, especially among white males.²¹ This trend, together with the rapid decrease of distal gastric cancers, makes it plausible that Western gastric cancer arises mostly in the proximal stomach. However, the lower oesophageal adenocarcinoma is a new, distinct disease with a different aetiology and contrasting patient backgrounds,²² and therefore should be considered separately from ‘classical’ gastric cancer. In the three large-scale Western surgical trials, the Dutch D1/D2,¹ the British MRC D1/D2²³ and United States INT0116 studies,³ the proportion of proximal third tumours was 10.3%, 30.5% and 19.5% respectively, and was not significantly different from that (19.1%) in the Japanese D2/D3 study²⁴ (Fig. 7.2). This suggests that, as far as surgically targeted gastric cancers are concerned, tumour location is not largely different between the West and Japan. The apparent predominance of proximal tumours in the West may be a simple reflection of the mixture of different diseases, i.e. increasing oesophageal and decreasing gastric adenocarcinomas.

Figure 7.2 Proportion of the primary tumour location in prospective trials of gastric cancer surgery.

Patient factor: Western patients with gastric cancer are on average 10 years older, much more likely to be obese and more frequently have comorbidities, especially of cardiovascular diseases, than their Japanese counterparts.²⁵ Although this does not mean that the disease is different, it certainly affects surgical process and outcomes. In particular, obesity hampers the completion of extended lymphadenectomy for gastric cancer, even in specialist Japanese centres. It has been shown to be an independent risk factor for postoperative morbidity.²⁶

Role of radical surgery in Western practice

Due to the decreased incidence and the technically demanding therapeutic requirements, gastric cancer in the West is today considered as a disease that should be treated in specialist centres. Several studies have shown relationships between the hospital/surgeon volume of gastric cancer treatment and operative mortality.²⁷ Given the accelerated ‘proximal shift’ of the disease and the increasing surgical risks in Western patients, the trend of centralisation will further progress.

Although solid evidence of extended lymphadenectomy is yet to be established, D2 gastrectomy without splenectomy or pancreatectomy was officially recommended by the European Society of Medical Oncology in 2009.²⁸ The NCCN guidelines for gastric cancer in the USA also recommend D2 for potentially curable gastric cancer with the condition that experienced surgeons perform it in specialist cancer centres.²⁹ However, as the possible benefit of this extensive surgery could be easily offset by the increased mortality, careful selection of patients is important even in specialist centres. There is an increasing move towards tailoring operations, taking not only the stage of the disease but also patient-related factors into account.

Summary

There are large differences between Japan and the West in incidence, staging system, tumour location and patient factors. Consequently, the concept of radical surgery has developed separately in Japan and the West. Today in the West, gastric cancer is considered as a disease to be treated by specialists, preferably with D2 lymphadenectomy without splenectomy.

Principles of radical gastric cancer surgery

Extent of gastric resection

The primary objective of gastric cancer surgery is to adequately excise the primary lesion with clear longitudinal and circumferential margins. Selection of gastrectomy depends on the tumour location and the mode of infiltration in the stomach wall. Preoperative diagnosis should focus on this, and careful assessment of lateral tumour spread is indispensable.

Resection margins

Proximal resection margin is the main determinant in selecting a total or distal gastrectomy. During surgery for T2 or deeper tumours, the resection line should be determined with a sufficient margin from the palpable edge of the tumour. A 5-cm margin has traditionally been recommended.³⁰ In some guidelines, even 8 cm is recommended for diffuse-type tumours,³¹ but this would necessitate most tumours of the gastric body requiring a total gastrectomy or oesophagogastrectomy.

According to Japanese treatment guidelines,³² a 5-cm margin is recommended for tumours showing an infiltrative growth pattern with indistinct borders or diffuse-type histology, but 3 cm is usually sufficient for those showing an expansive growth pattern with grossly distinct borders, for which the histology is most frequently of the intestinal type.

For gastric cancers invading the oesophagus, a 5-cm margin is not necessarily required, but frozen section examination of the resection line is desirable to ensure an R0 resection.

In cT1 tumours, lateral mucosal extension should be preoperatively detected or excluded by stepwise biopsy, and placing clips on the negative border is helpful to accurately resect impalpable lesions.

Type of gastrectomy

Common types of gastrectomy for gastric cancer are as follows.

Total gastrectomy: This involves removal of the whole stomach including the cardia (oesophagogastric junction) and the pylorus. It is indicated for tumours arising at or invading the proximal stomach.

Distal (subtotal) gastrectomy: This involves removal of the stomach including the pylorus but preserving the cardia. Two-thirds or more of the stomach is usually removed for gastric cancer. It is indicated for middle or lower third tumours with sufficient resection margins mentioned above.

Proximal gastrectomy: This involves removal of the stomach including the cardia but preserving the pylorus. It is indicated for proximal tumours with or without oesophageal invasion, where more than half of the distal stomach can be preserved.

Other resections for T1 tumours: Pylorus-preserving gastrectomy (PPG) is indicated for T1 tumours in the gastric body having negligible possibility of metastasis to the peripyloric lymph nodes. About a 3-cm pyloric cuff with the right gastric artery is preserved.

Segmental gastrectomy is a circumferential resection of a small part of the stomach preserving the cardia and pylorus. Local resection is a non-circumferential resection of the stomach wall. These resections are not considered as a standard cancer treatment and may be indicated for small T1 tumours in patients with high operative risks.

Total gastrectomy ‘de principe’ for distal cancers: Some European surgeons have argued that all cancers of the stomach, even those in the distal third, should be treated by total gastrectomy. This principle is based on the experience of frequent involvement of proximal resection margin and consequent anastomotic local recurrence. Theoretically, total gastrectomy ensures more certain negative margins and sufficient lymphadenectomy. In addition, the possible occurrence of multicentric cancer in the gastric stump can be prevented. On the other hand, total gastrectomy is associated with a higher operative morbidity and mortality, increased risk of long-term nutritional problems and impaired quality of life as compared to distal gastrectomy.

Randomised trials comparing total and distal gastrectomies in distal gastric cancer failed to show the survival benefit for total gastrectomy.³³

The policy of total gastrectomy de principe should be abandoned for the following reasons:

1. Provided the rules on safe margins of resection listed above are adhered to, a positive proximal resection margin is rare. If the margins are still positive, this usually indicates an aggressive and extensive malignancy and the resection line involvement will not be a major determinant of prognosis.

2. The lymph nodes that can be removed only by total gastrectomy, station nos. 2 (left cardia), 4sa (upper greater curve), 10 (splenic hilum) and 11d (distal splenic artery), are seldom involved in distal gastric cancers. If they are involved, again this indicates an aggressive malignancy and extended surgery would not alter survival outcome.

3. The incidence of second primary cancer in the gastric stump is low. Long-term surveillance by endoscopy may detect a new lesion that can be removed by endoscopic submucosal dissection.

Lymphadenectomy

Lymph node metastasis is the most common mode of spread in gastric cancer. Histological nodal metastasis has been proven in 80% of T4a/T4b tumours, and even T1 tumours have a 10% probability of lymph node metastasis (T1a 3%, T1b 18%).^4,⁵ Unlike hepatic and other distant metastases, lymph node metastasis from gastric cancer can be surgically removed for potential cure as long as it is confined to the regional area.The optimal extent of lymphadenectomy, however, has been controversial.

Lymph node groups in the former Japanese classifications

Japanese surgeons and pathologists have extensively investigated the distribution of lymph node metastasis. They have recorded it using standardised anatomical station numbers (Fig. 7.3). They then classified the stations into three groups, basically according to the incidence of metastasis (N groups 1–3). As the pattern of lymph node metastasis varies with the location of the primary tumour, N groups 1–3 were separately defined depending on the primary tumour location. These numbers of nodal groups were also used to express the grade of nodal disease (N1–3) and the extent of lymphadenectomy (D1–3), e.g. cancer with metastasis to a node in the second group was designated as N2, and complete dissection of up to the second group nodes was defined as D2.

Figure 7.3 Station numbers of lymph nodes around the stomach. Modified from the Japanese classification of gastric carcinoma, 3rd English edn.³⁹ ACM, A. colica media; AGB, Aa. gastrica breves; AGES, A. gastroepiploica sinistra; AHC, A. hepatica communis; AJ, A. jejunalis; APIS, A. phrenic inferior sinistra; TGC, truncus gastrocolicus; VCD, V. colica dextra; VCDA, V. colica dextra accessoria; VCM: V. colica media; VGED, V. vastroepiploica dextra; VJ:V. jejunalis; VL, V. lienalis; VMS, V. mesenterica superior; VP, V. portae; VPDSA, V. pancreaticoduodenalis inferior anterior.

Since its first edition published in 1962, the Japanese Classification of Gastric Carcinoma (JCGC) has undergone periodic revisions, and each time the definitions of the lymph node groups have been slightly modified. The Dutch and MRC D1/D2 trials were conducted using the N and D (‘R’ at that time) definitions of the 11th edition of the JCGC ³⁴ (Table 7.2), while the Taipei D1/D3 trial³⁵ and the Japanese D2/D3 trial²⁴ used the 12th edition,³⁶ in which the lymph nodes were grouped from N1 to N4. In the 13th edition,³⁷ the nodal grouping was completed, with four groups (N1–3 and ‘M’) in five categories of the primary tumour location (Table 7.3). This definition was based on the ‘dissection efficiency index’ of each lymph node station,³⁸ calculated using the incidence of metastasis and survival data of a large number of patients. As compared to the 11th edition, D2 lymphadenectomy defined in the 13th edition required more extensive dissection, e.g. for distal third tumours, station nos. 11p, 12a and 14v were included as N2 nodes.

Table 7.2

Lymph node groups used in the Dutch and MRC D1/D2 trials (Japanese classification, 11th edn)

A, lower third; M, middle third; C, upper third.

^*Resection or non-resection of these nodes does not affect the D number.

^†These nodes should be excised if the primary tumour site is the MC. If the primary tumour site is MA or M, removal is optional.

^‡In proximal gastrectomy, non-resection of these nodes does not affect the D number.

Table 7.3

Lymph node grouping in the 13th edition of the Japanese classification

Tumour location: L, lower third, M, middle third; U, upper third; + E, oesophageal invasion. Lymph node category: ‘M’, distant metastasis.

Outside Japan, it is widely believed that Japanese N1 nodes are perigastric and N2 nodes are those along the coeliac artery and its branches. Although this expression roughly reflects the nodal groups, it is apparently incorrect in terms of the original concept of grouping based on the primary tumour location. The misunderstanding seems to be due to the over-complicated definitions of the JCGC. In the latest 14th edition (third English edition ³⁹), the traditional nodal grouping system has been abandoned, and the simplified ‘D’ has been defined according to the type of gastrectomy (Fig. 7.4).

Figure 7.4 (a) Definitions of lymphadenectomy (D) in total gastrectomy. (b) Definitions of lymphadenectomy (D) in distal gastrectomy. Modified from Japanese gastric cancer treatment guidelines 2010 (ver. 3).³²

New definition of lymphadenectomy

The new ‘D’ definitions in the Japanese Treatment Guidelines ³² are simple, practical and mostly compatible with those in the 13th edition, with only some exceptions. D1, D1 + and D2 (D3 is no longer included) are defined for the two major types of gastrectomy, total and distal, regardless of the tumour location. It should be noted that the lymph nodes along the left gastric artery (no. 7), which used to be classified as N2 for tumours in any location, are now included in the D1 category for any type of gastrectomy. This is based not only on the previously mentioned efficacy index analysis, but also on the view that surgery for gastric carcinoma should as a minimum include the division of the left gastric artery at its origin.

The JGCA recommends that non-early, potentially curable gastric cancer should be treated by D2 lymphadenectomy. D1 or D1 + should be considered as an option for T1 tumours. In a poor-risk patient or under circumstances where D2 cannot be safely performed, D1 + can be a substitute for D2.

D2 lymphadenectomy – evidence

D2 lymphadenectomy is the gold standard for potentially curable advanced gastric cancer in Japan and Korea, while general surgeons in the West have been reluctant to adopt this radical approach.

In Japan, the benefits of D2 over less extensive dissections have never been tested in a randomised study. Instead, D2 was compared with more extensive surgery, D2 plus para-aortic nodal dissection (PAND), in a well-designed, multicentre randomised controlled trial (RCT).²⁴ This confirmed that D2 and D2 + PAND were performed with low operative mortality (0.8%) by specialist surgeons,⁴⁰ but failed to show a survival benefit of PAND. They have abandoned this super-extended lymphadenectomy as a means of prophylaxis, but they still never consider that D2 may not be superior to D1. A single institutional RCT in Taipei showed a significant survival benefit of D2/3 over D1,³⁵ and this is so far the only RCT that showed superiority of extended lymphadenectomy for gastric cancer.

In the West, where D0/D1 was the standard, D2 was tested as an experimental treatment in two large RCTs.^1,²³ In both trials, D2 was associated with higher morbidity and mortality than D1, and no significant survival benefit of D2 was shown.

In these trials, total gastrectomy in the D2 arm was performed with pancreatosplenectomy, which caused high morbidity and mortality. Despite these negative results for D2, the Dutch group continued the follow-up of the patients for 15 years and finally published remarkable results.¹² They compared the recurrence of gastric cancer in both arms on the basis of autopsy findings and found a significantly lower rate of gastric cancer death in D2 than in D1 patients. They concluded the study by stating that D2 should be performed as potentially curative surgery for gastric cancer.

There are several non-randomised observational studies in Europe that suggest benefits of extended lymphadenectomy, and today the guidelines officially recommend D2 lymphadenectomy without splenectomy by experienced surgeons.²⁸

Number of lymph nodes and extent of lymphadenectomy

In the Western literature, the definition of extent of lymphadenectomy for gastric cancer is often ambiguous. The number of retrieved lymph nodes is sometimes used as a surrogate for ‘D’, e.g. extended lymphadenectomy means retrieval of 25 or more nodes.⁴¹ This is a useful method to retrospectively assess the volume of lymphadenectomy in a gastrectomy where anatomical information of dissected lymph nodes is unavailable.

Generally the more extensive the surgery is, the more lymph nodes are retrieved. However, the number of retrieved nodes in a gastrectomy specimen is influenced by other factors as well:

1. Who picked up the nodes from which condition of the specimen for what goal. More nodes are retrieved when a surgeon tries to pick up as many nodes as possible in a fresh specimen than when a pathologist picks up swollen nodes from a formalin-fixed specimen up to the minimal requirement number.

2. Disease stage. In advanced disease with multiple lymph node metastases, the nodes are hard and easily recognised, even if they are small.

3. Patient factor. In obese patients, the lymph nodes are not easily recognised.

Thus, it should be kept in mind that the number of retrieved lymph nodes is a combination of the surgery and pathological handling, and does not necessarily reflect the extent of lymphadenectomy. Surgeons should plan and perform lymphadenectomy according to anatomical extent rather than to fulfil an aim of removing 25 or more nodes.

Bursectomy

Bursectomy is the complete removal of the lesser sac (omental bursa) that consists of the lesser/greater omenta, the anterior sheet of the transverse mesocolon and the pancreatic sheath. It is performed in potentially curative gastrectomy for T4a tumours penetrating the serosa of the posterior gastric body with the aim of removing possible cancer seeding inside the bursa.

Its impact on survival is yet to be established, but it does increase morbidity related to pancreatic fistula, and it is no longer a standard procedure even in Japan. A small RCT suggested its survival benefits ⁴² and a new RCT recruiting 1000 patients is active in Japan.

Splenectomy

Embryologically the spleen and the body of the pancreas arise in the dorsal mesentery of the foregut, sharing the vessels and lymphatics with the stomach, and in gastric cancer surgery these two may be removed together with the stomach as a total mesogastric excision. Indeed, a total gastrectomy with distal pancreatectomy and splenectomy (DP + S) enables complete en bloc resection without touching or incising the tumour of the stomach.

On the other hand, all clinical studies have shown that splenectomy or DP + S significantly increases operative morbidity and in the West, mortality, without obvious survival benefit.43–45 Today splenectomy or DP + S for gastric cancer is avoided in most countries. However, this needs some consideration.

Proximal gastric cancer may metastasise to the splenic hilar nodes (no. 10) via the gastrosplenic ligament (no. 4sa) and/or the left gastroepiploic lymphatics (no. 4sb). The incidence of no. 10 metastasis increases up to 25–30% when the tumour invades the greater curvature of the upper gastric body.³⁸ These can be completely cleared by splenectomy, and up to 25% of the patients having positive no. 10 nodes survive more than 5 years. Total gastrectomy with splenectomy can be performed by specialist surgeons without increasing mortality.⁴⁰ In this situation the author advocates gastrectomy with splenectomy.

Although a number of observational studies have demonstrated a lack of survival benefit or even a negative prognostic effect of splenectomy,^43,⁴⁴ these are all heavily biased, retrospective comparisons and cannot advocate spleen preservation. Medium-sized RCTs were conducted in Chile⁴⁶ (N = 187) and Korea⁴⁷ (N = 207) to compare total gastrectomy (TG) and TG + splenectomy (TGS). In both studies, TGS did not increase operative mortality by experienced surgeons, and although the 5-year survival rate of TGS was higher than that of TG, the difference was not statistically significant. They concluded that splenectomy was not justified. These are negative studies, but are still unconvincing.

In a multicentre RCT conducted in Japan,⁴⁸ 503 patients with proximal gastric cancer were randomised to receive TG or TGS during a curative operation, and are currently being followed up until the final survival analysis with complete 5-year results, which is scheduled in 2014. The TGS showed higher operative morbidity (23.6%) than TG (16.7%), but similar mortality (0.4% vs. 0.8%).⁴⁹

In the meantime, the JGCA treatment guidelines recommend splenectomy in a curative total gastrectomy for a T2–T4 tumour invading the greater curvature.³²

A spleen-preserving no. 10 dissection is feasible in thin patients. It is, however, technically demanding, and thorough anatomical knowledge of the splenic vessels is essential.

Distal pancreatectomy

Distal pancreatectomy and splenectomy (DP + S) used to be a part of D2 gastrectomy for proximal gastric cancer regardless of the presence or absence of pancreatic invasion of the tumour, and actually was performed in the Dutch and British D1/D2 trials.^1,²³ The aim of the routine use of this aggressive procedure was complete dissection of the lymph nodes along the splenic artery (nos. 11p and 11d) and those in the splenic hilum (no. 10).

However, DP + S is associated with high operative morbidity including pancreatic leakage and abscess formation, even in specialist Japanese centres.⁵⁰ Since the technique of complete dissection of no. 11 nodes without pancreatectomy has been established,⁵¹ DP + S is currently indicated only for tumours directly invading the pancreas.

It is of note that pathological assessment in apparent T4b cases shows that the adhesion to the other organ is often inflammatory rather than neoplastic.¹³ In order to avoid unnecessary DP + S in ambiguous cases, it may be worthwhile surgically separating the adhesion without DP + S, paying special attention not to injure the pancreatic parenchyma.

Extended resections

The goal of surgery for potentially curable gastric cancer is to achieve R0 resection by standard gastrectomy with sufficient resection margin and adequate lymphadenectomy. Some tumours may exceed this range but still be resectable. In such cases, extended resection should be considered.

En bloc resection of involved adjacent organs

Proximal gastric cancer may invade the distal pancreas, necessitating pancreatosplenectomy as discussed above. Middle to distal third gastric cancer may invade and penetrate the transverse mesocolon. When the invasion involves major colic vessels then partial colectomy may be necessary for en bloc resection.

When a distal tumour invades the pancreatic head or extends to the duodenum for a long distance intramurally, a pancreatoduodenectomy may enable en bloc tumour resection. However, this operation is rarely indicated because such tumours are frequently associated with other non-curative factors such as peritoneal disease. Although some case series from high-volume centres suggest survival benefit in R0 resection, the selection criteria are difficult to define.⁵²

Tumours penetrating the anterior wall of the stomach may invade the lateral segment of the liver, and can usually be removed by partial liver excision without segmentectomy.

Extended lymphadenectomy

The role of extended lymphadenectomy exceeding D2 is ambiguous. Prophylactic para-aortic nodal dissection did not improve the survival of standard D2 in a large-scale Japanese RCT ²⁴ and has been abandoned in Japan.

An Italian group of surgeons are still performing this surgery, aimed at improving the prognosis of patients.⁵³

The retropancreatic lymph nodes (no. 13) are not regional nodes of gastric cancer and the prognosis of patients with positive no. 13 nodes is extremely poor. However, for distal tumours invading the duodenum, no. 13 nodes are considered as regional nodes according to the TNM rules, and indeed some patients with a pyloric cancer invading the duodenum survive after dissection of positive no. 13 nodes.⁵⁴

Resection of liver metastases

Unlike for colorectal cancer, liver resection for gastric cancer is rarely indicated. In the literature, only some case series from Japanese high-volume centres suggest possible survival benefit in selected cases.^55,⁵⁶ In Koga et al.’s study,⁵⁶ for example, of 5520 patients who underwent gastric cancer surgery during a 20-year period, 121 (2.2%) had synchronous liver metastases and 126 (2.3%) developed metachronous ones, and only 42 patients underwent liver resection, of whom eight had survived more than 5 years at the time of analysis. In these reports, the authors’ proposals for selection criteria of liver resection are not consistent. They mostly agree that liver resection should be considered for solitary liver tumours without other non-curative factors.

Summary

Radical surgery for gastric cancer consists of a gastric resection with adequate margins and systematic lymphadenectomy. Total gastrectomy ‘de principe’ should be abandoned. The Japanese Association has totally renovated and simplified the definition of D2, which has the potential to be the world standard. More extended surgery including combined resections of the involved organs shows no evidence of improving survival, but may become necessary for R0 resection on an individual case basis.

Technique of gastric resection with D2 lymphadenectomy

Incision

An upper midline incision is used for resection of non-cardia gastric cancer. For a bulky proximal tumour, especially in an obese patient, an inverted T-shaped or a bilateral subcostal incision is useful.

For a proximal gastric cancer invading the oesophagus, either transhiatal (TH) or left thoracoabdominal (LTA) approach is selected. LTA provides excellent exposure of the paracardiac area and lower mediastinum, but is associated with an increased morbidity. A Japanese randomised trial compared TH and LTA for Siewert type 2 and 3 gastric cancer invading the oesophagus within 3 cm and showed no survival improvement but increased morbidity in LTA approach.⁵⁷

Intraoperative staging

The sensitivity and specificity of diagnostic imaging to stage gastric cancer is not sufficient to allow preoperative selection of optimal treatments. Surgical exploration or staging laparoscopy provides information on the T and M categories, especially on peritoneal metastasis. However, even by careful intraoperative palpation and inspection, lymph node metastasis cannot be accurately staged. Sentinel node diagnosis is not yet reliable due to the complicated lymphatic network around the stomach. Therefore, for radical gastrectomy, a systematic lymphadenectomy should always be considered unless the tumour is diagnosed as T1.

Procedure of D2 lymphadenectomy

Distal gastrectomy

Kocherisation: Mobilisation of the duodenum facilitates a safe and smooth procedure for the subsequent infrapyloric lymphadenectomy. The assistant should hold the descending portion of the duodenum to stretch the parietal peritoneum. The peritoneum close to the duodenum should be incised and the incision extended along the duodenum. The assistant should then ‘roll up’ the duodenum and proceed to the back of the pancreatic head, staying close to the posterior pancreatic fascia, and mobilise the pancreatic head. The para-aortic area should be palpated and, if suspicious nodes exist, they should be sampled.

Omentectomy: Though omentectomy is not necessarily a part of D2 dissection, it is usually performed for T3/T4 tumours to remove possible tumour spread into the omenta. The omentum is removed from the right side of the transverse colon and the duodenum. It is then dissected along the transverse colon toward the lower pole of the spleen.

When omentectomy is omitted in D2 gastrectomy, the incision line of the omentum should be at least 3 cm away from the right gastroepiploic arcade so that the no. 4d lymph nodes along the arcade are completely dissected.

Division of left gastroepiploic vessels: At the lower splenic hilum and the pancreatic tail, the left gastroepiploic artery (LGEA) arises from the end of the splenic artery, sometimes as a branch of the lower polar splenic artery. The LGEA and the vein of the same name should be ligated and then cut. As the lymph nodes along the LGEA (no. 4sb) are rarely metastatic from distal gastric tumours, the dissection does not have to include the trunk of this artery. However, tumours in the gastric body, especially those located on the greater curvature, may metastasise to the splenic hilar nodes (no. 10) via no. 4sb. The LGEA should be dissected at the origin in these cases.

On the greater curve of the stomach, there is usually some avascular area between the first branch of the LGEA and the short gastric arteries, and this will be a landmark of the upper limit of dissection in distal gastrectomy.

Infrapyloric node dissection (no. 6): In distal gastric cancers, a precise dissection of no. 6 lymph nodes is essential because they are most frequently involved and the dissection of positive nodes can still bring cure.

The (second) assistant should hold the transverse colon and gently stretch the mesocolon. The middle colic vein should be identified and pursued, to the approach of the gastrocolic venous junction point (Fig. 7.5). Identify the accessory right colic vein (ARCV), right gastroepiploic vein (RGEV), gastrocolic trunk and the anterior superior pancreaticoduodenal vein (ASPDV). The middle colic vein usually drains directly into the superior mesenteric vein (SMV).

Figure 7.5 Infrapyloric veins and lymph nodes. ASPDV, anterior superior pancreaticoduodenal vein.

The RGEV should be ligated and cut prior to its junction with the ASPDV. A small vein draining from the pancreas to the RGEV should be carefully cauterised. When no. 6 nodes are grossly metastatic, dissection of the nodes in front of the SMV (no. 14v) should be considered.

Then, the gastric antrum should be pulled up and the gastroduodenal artery (GDA) identified between the duodenum and the pancreas. The GDA is exposed distally as far as the origin of the right gastroepiploic artery (RGEA) (Fig. 7.6). The infrapyloric artery arises either from the GDA or from the RGEA. The RGEA and the infrapyloric artery should be ligated and cut together or separately at their origin.

Figure 7.6 Branches of the common hepatic artery and lymph node numbers. CHA, common hepatic artery; GDA, gastroduodenal artery; LGA, left gastric artery; PDA, pancreaticoduodenal artery; RGA, right gastric artery; SA, splenic artery.

The GDA should be pursued proximally to its origin from the common hepatic artery (CHA). A large, flat lymph node (no. 8a) usually covers the CHA. The peritoneum covering this node at its right edge is opened and the surface of the CHA exposed. Using this procedure, no. 5 (suprapyloric) and no. 8a nodes are separated. A gauze is placed to the right of the no. 8a node, which will serve as a landmark of the correct layer in the subsequent suprapyloric dissection.

Suprapyloric nodes dissection (no. 5) and transection of the duodenum: The assistant pulls down the pylorus and the duodenum to stretch the suprapyloric area. The right gastric artery (RGA) and the superior duodenal arteries (SDAs) are identified and the serosa between them incised. The previously placed gauze is encountered, protecting the GDA and CHA.

The SDA arising from the GDA and/or the proper hepatic artery (PHA) is cut. The origin of the RGA and the right gastric vein that runs just close to the artery and drains into the portal vein is then exposed. The RGA and vein together are ligated and cut to dissect no. 5 nodes. The anterior peritoneum of the hepatoduodenal ligament is removed to expose the PHA for subsequent no. 12a dissection.

The duodenum is transected using a linear stapler, and the staple line sutured with seromuscular stitches.

Exposure of the oesophageal hiatus: The assistant pulls down the stomach to stretch the lesser omentum. It is incised close to the liver, and the incision extended toward the right cardia. The accessory left hepatic artery is sometimes encountered and can be dissected. If it is large and replaces the proper left hepatic artery then it should be preserved. In this case, the division of the left gastric artery needs special attention, as described later.

At the upper end of the lesser omentum, the peritoneum covering the right diaphragmatic crus is excised to enter the oesophageal hiatus. The crus is exposed towards the coeliac artery, which will be helpful for later dissection around the coeliac axis.

Dissection of the upper border of the pancreas (nos. 8a, 9, 11p and 12a): This is the core of D2 lymphadenectomy. The nerve tissue surrounding the major arteries in this area does not have to be removed in lymphadenectomy for gastric cancer because the lymphatic tissue between the nerve and the arterial adventitia is sparse and the perineural infiltration at this level is very rare.

The assistant should gently pull down the pancreas and expose the field of dissection. The peritoneal covering is incised along the upper border of the pancreas and the vascular structures (CHA, splenic artery (SpA), left gastric vein (LGV), etc.) broadly identified. The lymphadenectomy should be started at the no. 8a nodes that have already been exposed. There are small vessels between no. 8a nodes and the pancreatic parenchyma, which may require ligature or coagulation. The surface of the CHA should be exposed towards the coeliac axis until the root of the SpA appears. The LGV often drains to the splenic vein across the CHA, and is ligated and cut.

Then a change of direction is necessary and the CHA should be exposed towards the hepatoduodunal ligament. The lymph nodes are dissected along the PHA (no. 12a), exposing the left side of the portal vein.

The dissection then turns back towards the coeliac artery behind the CHA. The LGV draining to the portal vein is most frequently encountered at this point and is ligated and cut. The lymph nodes on the right side of the coeliac artery are then dissected.

The bifurcation of the coeliac artery (to the CHA and SpA) is identified, and the anterior surface of the coeliac artery is exposed until the left gastric artery (LGA) appears, surrounded by thick nerve fibres.The LGA sometimes arises very close to the aorta. The LGA is ligated (usually double) and cut at the origin. The surface of the diaphragmatic crus exposed previously is encountered, and the dissection of no. 9 lymph nodes is completed by removing lymphatic tissue in this area.

The left side of the coeliac artery is not easy to expose because, unlike the right side that can be accessed directly from the free peritoneal surface, the left side is covered by complicated fusion of the retropancreatic fascia and the parietal peritoneum.

When the accessory left hepatic artery arising from the LGA is to be preserved, the LGA should not be ligated but dissected at the origin, which exposes its trunk longitudinally until the origin of the ‘proper’ LGAs (usually two) appear. These are ligated and dissected to leave the arterial arcade from the coeliac artery to the left liver exposed.

The SpA originating from the coeliac artery immediately passes behind the pancreas, then reappears on the upper border of the pancreas and winds towards the spleen (Fig. 7.7). The left side of the coeliac artery and the proximal part of the SpA are dissected. In distal gastrectomy for distal tumours, dissection around the proximal 4–5 cm of the artery is sufficient. Note that there are lymphatic channels from the infrapyloric no. 6 area to the splenic artery nodes crossing the surface of the pancreas, and the no. 11p nodes often have metastases from pyloric tumors (Fig. 7.1).

Figure 7.7 Splenic artery and its branches. CHA, common hepatic artery; LGA, left gastric artery.

Dissection of the upper lesser curvature nodes (nos. 1 and 3a): The lymph nodes along the lesser curve (no. 3) are most frequently involved with tumours of the gastric body, and therefore complete removal is essential. The assistant should pull down the stomach. The lesser omental surface is lifted and incised close to the gastric wall, and then peeled away towards the cardia. The anterior trunk of the vagal nerve is cut and the left cardia nodes (no. 1) dissected. The posterior vagal trunk is then cut and the stomach reflected. Complete the no. 1 and 3 dissection by removing the lymphatics on the posterior aspect of the cardia.

Total gastrectomy

Most aspects of D2 lymphadenectomy in total gastrectomy are common to those in distal gastrectomy. Additional procedures are as follows.

Dissection of the upper greater curvature nodes (nos. 2 and 4sa): Following the division of the LGEA at its origin, the upper stomach is raised to inspect the splenic hilum from inside the lesser sac. The wall of the left bottom of the lesser sac is the dorsal gastric mesentery, which connects the upper greater curve of the stomach, the spleen, and the pancreatic body and tail. The gastrosplenic ligament is part of the dorsal mesentery.

The winding SpA and its terminal branches are broadly identified. The gastrosplenic ligament should be held and kept tense. The ligament is dissected close to the spleen, dividing the short gastric vessels towards the superior pole of the spleen. The peritoneal fusion at the back of the gastric fundus is then incised and the upper stomach mobilised from the abdominal wall.

The left paracardiac area has arterial supply from either the oesophagocardiac branch of the left subphrenic artery or the left cardiac branch of the LGA. Lymphatic flow from this area can directly reach the left para-aortic network.

Dissection along the distal splenic artery (no. 11d) and splenic hilum (no. 10): Following the 11p dissection, the procedure is continued along the SpA towards the spleen. The winding SpA gives off several branches to both the pancreas and the stomach (Fig. 7.7). The great pancreatic artery, though not so large as its name suggests, is an important blood supply to the pancreatic tail. The caudal pancreatic artery arises near the splenic hilum. These pancreatic branches are preserved.

The remaining dorsal mesentery connects the posterior aspect of the upper stomach and the splenic artery and vein, and includes the posterior gastric artery and vein. This artery usually arises in the middle of the SpA and nourishes the dorsal part of the cardia. It should be ligated and cut at the root. Cancers in the upper stomach, especially those located on the posterior wall, frequently metastasise to the SpA nodes through the lymphatic channels in this mesentery.

The dissection is sometimes dangerous owing to kinking of the artery. Appropriate traction by the second assistant is particularly helpful.

Splenectomy: Splenectomy is required when the tumour invades the tail of the pancreas and/or splenic hilum without other non-curative factors. It may also be indicated for complete dissection of no. 10 lymph nodes in tumours invading the greater curvature of the proximal stomach.

Mobilisation of the pancreas and spleen is started at the lower border of the pancreas. The bottom of the anterior sheet of the mesocolon is incised close to the pancreas. Several vessels arising from the pancreas to the anterior mesocolon (posterior epiploic arteries) should be cut.

The pancreatic body is lifted and entered behind the pancreas, leaving the retropancreatic fusion fascia to the retroperitoneal space. This is continued towards the spleen until the pancreatic tail is lifted. If the proper layer is entered, no vessels are encountered in this procedure.

The assistant should pull down the left kidney. The pancreatic tail is pulled up with the lower pole of the spleen. Then the parietal peritoneum behind the spleen can be visualised from its medial aspect. It is then incised and the spleen mobilised. This incision is continued towards the cardia, mobilising the whole dorsal mesentery from Gerota’s fascia covering the kidney and left adrenal gland.

When the pancreas and spleen have been totally mobilised, the surgeon moves to the left side of the patient to continue the procedure.

The assistant should hold the reversed spleen. Holding the tail of the pancreas in the left hand, the lymph nodes are dissected along the distal SpA. The SpA is double ligated and cut, then the vein, and the spleen removed from the pancreas.

When the pancreas is also removed for tumour invasion, the SpA is ligated and dissected as close to the root as possible. Then the vein is ligated and cut close to the resection line, and the pancreas transected.

Summary

D2 lymphadenectomy is a systematic, standardised, technically demanding procedure that necessitates thorough knowledge of the anatomy of major gastric arteries and veins.

Modified surgery for early gastric cancer

Lymph node metastasis from early gastric cancer

In undertaking D2 lymphadenectomy, almost all regional lymph nodes that may contain metastases are removed. In T1 tumours (early gastric cancer, EGC), lymph node metastasis is infrequent (about 10%) and mostly limited to the perigastric nodes.

Therefore, when the clinical diagnosis of EGC is reliable, D2 lymphadenectomy is not necessary, and the extent of gastric resection can also be reduced.

There is a clear correlation between the depth of tumour invasion and the incidence of lymph node metastasis in gastric cancer. This is true between any two adjacent T categories, and even in the same T1 category, mucosal (T1a) and submucosal (T1b) tumours show clearly different chances of metastasis. However, the reported incidence of lymph node metastasis from pT1 tumours has not been consistent.^5,⁵⁸ This is probably due to differences in the pathological process. In Japan the sectioning method of gastric cancer has been standardised by the Japanese Classification of Gastric Carcinomas,³⁹ and all lesions in the surgically resected specimens are sectioned at 5-mm intervals. With sectioning at wider intervals, or with only one or two central sectioning, the deepest invasion of a lesion can be overlooked and the T category would be under-staged. Then a group of tumours diagnosed as T1a may include some deeper ones having a greater chance of lymph node metastasis and the ‘incidence of lymph node metastasis from T1a’ will be reported as higher. With sectioning at smaller intervals, deeper invasion may be detected in a tumour and a diagnosis of deeper T category is given, resulting in a lower incidence of metastasis in more strictly staged T1a tumours.

On the other hand, lymph node retrieval and the sectioning method of the nodes will also change the results. By meticulous retrieval and multiple sectioning, the chance of detection of metastasis increases (by 20% according to one report ⁵⁹) and the incidence of metastasis in T1 tumours is reported as higher.

Considering these possibilities, the incidence of lymph node metastasis is broadly estimated to be 3% and 20% from T1a and T1b tumours respectively. It should be noted that once the tumour invades the proper muscle layer, the incidence increases up to 50%.³⁸

Limited lymphadenectomy

The Japanese treatment guidelines define D1 and D1 + lymphadenectomy for tumours clinically diagnosed as T1. Since most metastasis from T1 is limited to the perigastric nodes and no. 7 and 8a nodes, D1 is sufficient to remove all possibly positive nodes. The problem is that the preoperative diagnosis of T1 is not always accurate: even for endoscopists who have diagnosed more than 100 ECGs, more than 10% of tumours they diagnose as T1 are pathologically T2 or deeper.⁶⁰ Surgeons should always bear this in mind and be ready to perform D2 whenever deeper invasion is suspected during surgery.

Pylorus-preserving gastrectomy (PPG) (Fig. 7.8)

PPG was originally developed as surgery for peptic ulcer disease,⁶¹ but due to its excellent functional results it is currently applied for selected cases of EGC. A short cuff (usually 3 cm) of the pyloric antrum is preserved together with the pyloric branch of the anterior vagal nerve and the infrapyloric artery. The upper gastric remnant should be large enough to function as a reservoir. For these restrictions, the dissection of no. 1 and 5 nodes is incomplete compared to standard distal gastrectomy. Therefore, PPG is indicated for middle gastric tumours that have very low possibility of metastasis to these nodes, i.e. clinical T1N0 in the middle portion of the stomach with the distal tumour border at least 4 cm proximal to the pylorus.

Figure 7.8 Pylorus-preserving gastrectomy for early gastric cancer in the middle gastric body.

The quality of life after PPG is superior to that after distal gastrectomy. Low incidence of early and late dumping syndromes, low incidence of iron-deficiency anaemia and less body weight loss are reported.^62,⁶³ These are attributable to less rapid gastric emptying and prolonged acid contact of dietary iron. On the other hand, some patients suffer from early satiety and reflux due to malfunction of the pylorus and/or too small gastric remnant.

With careful selection of the cases, the oncological results are excellent and not at all inferior to standard distal gastrectomy.

Local tumour resection based on sentinel lymph node diagnosis

If the sentinel lymph nodes from a small gastric cancer are accurately detected and their negativity can be confirmed, gastrectomy can be omitted and local tumour resection is sufficient for cure. However, the lymphatic network surrounding the stomach is very complex and accurate identification of the sentinel nodes is not easy. Several prospective studies have failed to detect the ‘lymph nodes that first receive metastasis’.⁶⁴ At present, this strategy still remains investigational.

Summary

Various less invasive or function-preserving surgeries have been developed for early cancers with good results. Indications for these treatments should be strictly confined to early cancers so as not to lose the chance of cure.

Reconstruction after gastric resection

A number of reconstruction methods have been proposed for gastrectomy. Each has advantages and disadvantages, and should be selected according to surgical and oncological conditions in each patient. The following points should be considered in selection:

1. Safety of surgery. In gastrectomy for advanced tumours (curative or palliative) or for patients having high operative risk, any procedure after removal of the tumour should be simple and safe, so as not to prolong the surgical time or increase the postoperative complications.

2. Possible local recurrence. In locally advanced tumours with wide serosal involvement and/or apparent nodal metastasis, gastric bed recurrence should be prepared for and a reconstruction with the least risk of obstruction should be selected.

3. Long-term quality of life. In gastrectomy with a high probability of cure, a reconstruction to maximise quality of life should be selected. Reflux of bile and alkaline duodenal juices into the oesophagus should be prevented. At the same time, long-term nutritional status should be considered.

Reconstruction after distal gastrectomy (Fig. 7.9)

While Roux-en-Y (R-Y) and Billroth II (B-II) reconstructions are widely used, Billroth I gastroduodenostomy (B-I) is also frequently employed in Eastern Asia.

Several RCTs and case series comparing these methods have been published with inconsistent results. A recent meta-analysis suggests that R-Y shows some clinical advantages over the other two methods.⁶⁵

Figure 7.9 Reconstructions after distal gastrectomy. (a) Billroth I. (b) Billroth II isoperistaltic. (c) Roux-en-Y. (d) Roux-en-Y (hand-sewing). (e) Roux-en-Y (stapler).

Roux-en-Y

Indication: Advantages of R-Y over B-I are absence of duodenal juice reflux, safe anastomosis with very low leak rate, and low risk of obstruction at gastric bed recurrence. Weak points include loss of easy endoscopic access to the duodenal papilla and possible nutritional problems due to non-physiological food passage, though no clear evidence has proven this. R-Y procedure involves jejunum and this may cause adhesive obstruction or internal hernia in the future. So-called ‘Roux-en-Y syndrome’, characterised by chronic abdominal pain and nausea that are aggravated by meals and associated with malnutrition, used to be reported mainly after ulcer surgery, but has not been observed as a serious problem lately.

R-Y reconstruction is applicable for most distal gastrectomies. The following are particularly good indications:

1. tumours involving the gastric body for which the remnant stomach after resection is small;

2. patients who suffer from reflux esophagitis before surgery;

3. patients with high operative risks for whom anastomotic leak must be prevented;

4. locally advanced disease with high risk of gastric bed recurrence.

In special patients with biliary tract problems or duodenal pathological conditions that require endoscopic access or follow-up, B-I reconstruction might be considered.

Procedure: The duodenum is transected using a linear-type stapler and many surgeons add covering seromuscular stitches. The jejunum 20–30 cm distal to the Treiz ligament is divided and the jejunal limb is pulled up either via the ante- or retrocolic route. In T4a/T4b tumours that have a significant risk of local recurrence involving the mesocolon, the antecolic route is preferred. Gastrojejunostomy is achieved either by stapler or hand-sewing; different anastomotic sites and jejunal directions are selected accordingly (Fig. 7.9d,e). The jejunojejunostomy is made 40 cm distal to the gastrojejunostomy. The mesentery holes are closed to prevent internal hernia.

When the retrocolic route is selected, the gastrojejunostomy site should be pulled down below the mesocolon and be fixed to it to prevent torsion or obstruction of the jejunal limb in the narrow space above the mesocolon.

Billroth I

Indication and procedure: Advantages of B-I over R-Y are physiological food passage, simple anastomosis without jejunal manipulation, and preserved endoscopic access to the duodenal papilla. B-I is useful for distal tumours at an early stage for which a relatively large proximal stomach can be preserved and recurrence is not thought likely. Weak points of B-I are duodenal juice reflux, possible anastomotic leak and possible obstruction at recurrence. Thus, B-I should be avoided in cases with high operative risks, small remnant stomach, preoperative presence of oesophageal reflux or locally advanced disease.

Gastroduodenostomy is made either by hand-sewing or using a circular stapler. When the anastomotic tension is high, Kocher’s mobilisation of the duodenum is useful to reduce it.

Reconstruction after total gastrectomy (Fig. 7.10)

R-Y is the standard reconstruction after total gastrectomy. It is simple, safe and gives relatively good functional results. Weak points are early satiety due to lack of reservoir and consequent long-term malnutrition. Careful dietetic surveillance and education is essential.

Figure 7.10 Reconstructions after total gastrectomy. (a) Roux-en-Y. (b) Double tract Roux-en-Y. (c) Jejunal interposition.

Roux-en-Y

Indication: There is virtually no contraindication for R-Y. In rare cases where endoscopic access to the duodenum needs to be maintained for biliary tract problems, a jejunoduodenostomy is added at about 30–40 cm from oesophagojejunostomy (double-tract R-Y, Fig. 7.10b).

Procedure: The jejunum is transected 20–30 cm from the Treiz ligament. Either the ante- or retrocolic route is selected according to the criteria mentioned in the section on distal gastrectomy. The retrocolic pathway provides the shortest route and the least tension on the limb mesentery, especially in obese patients with a large omental residue.

Jejunal vessels are carefully prepared so that the mesentery tension is reduced, preserving the blood supply to the anastomotic site.

Oesophagojejunostomy is undertaken using a circular stapler. A 25-mm anvil is applicable in most cases. A larger size can be selected in patients with large oesophagus and jejunum.

Jejunojejunostomy is performed 40–50 cm below the oesophageal anastomosis. A shorter limb may cause reflux and a longer one may be disadvantageous from a nutritional viewpoint. In the double tract method, jejunojejunostomy is made 20 cm distal to the jejunoduodenostomy.

Jejunal interposition

This method is employed to maintain the physiological food passage to the duodenum.

However, there is no solid evidence that this reconstruction has long-term nutritional advantage over standard R-Y.

The length of the interposed jejunum can be shorter (20–30 cm) than the jejunal limb in R-Y, probably because the jejunal juice can flow down the natural route without reflux.

Pouch formation

Various operations were devised to increase the reservoir capacity of the jejunum, with inconsistent results: some patients eat remarkably well but some others suffer from severe stasis or regurgitation.

Pouch formation does not significantly increase morbidity or extend the operation time, while patients with pouch have better food intake and improved quality of life. The technique is expected to be standardised in the near future.

The pouch technique has been improved, and a recent meta-analysis of 13 RCTs comparing R-Y or jejunal interposition with and without pouch showed some clinical advantages for a pouch reconstruction.⁶⁶

Reconstruction after proximal gastrectomy (Fig. 7.11)

Jejunal interposition

Indication: The original method was described by Merendino and Dillard in 1955 for reflux disease.⁶⁷ The interposed isoperistaltic jejunum prevents gastric juice reflux to the oesophagus, and strangely anastomotic ulcers do not appear. This reconstruction method is applicable to proximal gastrectomy for small tumours of the oesophagogastric junction in which resection of the oesophagus and stomach can be minimal. Note that even a short segment of the interposed jejunum could cause early dumping syndrome due to rapid food inflow.

Figure 7. 11 Jejunal interposition after proximal gastrectomy. (a) Jejunal interposition. (b) Oesophagojejunostomy. (c) Jejunogastrostomy. (d) Post operative Gastrografin swallow. Modified from Katai H, Sano T, Fukagawa T et al. Prospective study of proximal gastrectomy for early gastric cancer in the upper third of the stomach. Br J Surg 2003; 90:850–3.

Procedure: A short segment jejunum (10–15 cm) is used and anastomosed to the anterior wall ⁶⁸ (Fig. 7.11). Pyloroplasty is usually made. It is not necessary when the anterior trunk and the hepatic branch of the vagal nerve are preserved.

Oesophagogastrostomy

Indication: Although this is a simple and safe reconstruction after proximal gastrectomy, some patients suffer from severe reflux oesophagitis and cannot quit medication. This is indicated for proximal gastrectomy in which the abdominal oesophagus is preserved. Reconstruction after lower oesophagectomy using a gastric tube is described in Chapter 5.

Procedure: Oesophagogastrostomy is performed on the anterior wall of the remnant stomach, usually using a circular stapler. A hand-sewing method is not very difficult, and the soft opening of the anastomosis instead of the fixed ring of the stapler seems to function as a protector for the reflux. Many surgeons add some extra stitches between the oesophagus and the stomach to prevent reflux.

Summary

There is no single best reconstruction method after gastrectomy. Priority should be given to safety for poor risk patients, and to function for those with high possibility of cure. Roux-en-Y, following both distal and total gastrectomy, could be the first choice. Pouch formation seems to improve quality of life, and its procedure is expected to be standardised.

Early postoperative complications

Two major complications after gastrectomy for cancer are anastomotic leak and pancreatic fistula. They cause abdominal abscess, peritonitis, sepsis or massive haemorrhage. Complications are more common in total gastrectomy and extended lymphadenectomy than in distal gastrectomy and limited lymphadenectomy respectively. Most prospective studies have shown that splenectomy and distal pancreatectomy significantly increase postoperative morbidity and mortality. Close management by experienced surgeons, especially for pancreatic fistula, is essential to avoid mortality.

Use of prophylactic drains after gastrectomy is controversial. There is no evidence that drains decrease postoperative complications or death.⁶⁹ Distal gastrectomy without intraoperative problems usually needs no drains. However, in total gastrectomy or extended D2 dissection along the upper border of the distal pancreas, a suction drain along the pancreas gives useful information on pancreatic fistula or early anastomotic leak.

Anastomotic leak

Most anastomotic leaks after gastrectomy occur at the oesophagojejunostomy. Possible causes are tissue ischaemia or tension on the anastomotic line. These should be avoided by careful preparation of the jejunal loop. Correct usage of the anastomotic circular stapler is also important. Covering stiches are usually unnecessary, but should be used when the continuity of the ‘doughnut’ of the resected oesophagus or jejunum is incomplete.

Early anastomotic leak occurring within 72 hours would be life threatening without proper management. It may present as septic episodes or contaminated drain discharge. Contrast swallow (Gastrografin) should be done whenever a leak is suspected. Drainage is crucial to treat anastomotic leakage. When a prophylactic drain has been appropriately placed and the leak is minor without evidence of local diffusion, a conservative treatment with fasting and adequate nutrition will suffice. When there is no drain or septic signs are evident, re-operation is strongly advised. Anastomotic failure can be repaired in some early cases, or at worst a drain can be placed close to the leak site. In either case, a feeding jejunostomy should be constructed.

The management of a delayed leak is controversial. Usually drains have already been removed and meals are started. The patient may have some difficulty in swallowing and, though perhaps being afebrile, blood tests suggest continuous inflammation. When a contrast study reveals only a minor leak, fasting and adequate nutrition will be sufficient. A naso-intestinal tube placed beyond the jejunojejunostomy may be useful for enteral feeding. If the patient is septic, a drain must be placed. Contrast-enhanced computed tomography will be helpful whether the intervention is achieved surgically or radiologically. Surgery at this point is technically difficult due to severe adhesions in the upper abdomen, but should be carried out when the abdominal infection is diffuse.

Duodenal stump leak

A properly stapled duodenal stump rarely leaks. However, stump leak occurs when the duodenal tissue is damaged or becomes ischaemic. There is no evidence that covering stiches reduce leak, but some surgeons use them. Duodenal stump leak may also occur when the intraduodenal pressure increases due to afferent limb obstruction or possibly unusually strong peristalsis.

A prophylactic drain that is placed near the stump gives good information. If its discharge contains bile, it is an indication for immediate re-operation. Re-closure of the stump is usually very difficult due to tissue inflammation. If there is a major defect, a Foley-type catheter can be placed in the duodenum with a plan to form a controlled fistula. When the leak is from a pinhole on the staple line, a suction drain is placed close to it and retrograde insertion of a duodenal decompression tube from the jejunum should be considered. Feeding jejunostomy is useful not only for nutrition but also for returning the suctioned duodenal content to the intestine. With good duodenal decompression, enteral feeding does not have to be stopped or reduced.

Pancreatic fistula

After D2 lymphadenectomy, pancreatic leak may occur even without pancreatectomy. It is more common when the pancreatic capsule has been removed as a part of bursectomy or the pancreas has been mobilised for splenectomy. Placement of a prophylactic suction drain along the upper border of the pancreas is recommended in these operations. Increased amylase content in the drain fluid on the first or second postoperative day is a useful marker to predict later development of pancreatic fistula. The fluid containing high amylase usually takes on a dark red (wine) colour. Suction drainage is also useful to prevent diffusion of pancreatic fluid and localise the fistula.

When the tail of the pancreas is resected, pancreatic leak is more common and drain placement is strongly recommended. A suction tube should be placed close to the stump via the shortest percutaneous route.

It is controversial as to whether the use of somatostatin analogues prevents pancreatic fistula. RCTs for pancreatic surgery showed inconsistent results, and meta-analyses did not support a positive effect.⁷⁰ No RCT has been conducted on this subject in gastrectomy.

When pancreatic leak occurs, the management should concentrate on prevention of infection and abscess control. Adequate drainage is essential and radiological intervention should be considered. Abscess drainage takes time and may require frequent adjustments of the drain tip. When the abscess is localised and surrounded by a solid wall, saline irrigation of the cavity will enhance healing.

Haemorrhage

Haemorrhage within the first few hours of surgery should be treated by early re-laparotomy. It must be remembered that drains can occlude with blood clot and the clinical suspicion of bleeding in a haemodynamically unstable patient is a sufficient indication to operate.

Secondary haemorrhage caused by intra-abdominal infection following anastomotic leak and/or pancreatic fistula is truly life threatening. A poorly drained abscess causes pseudo-aneurysm of a major artery (most frequently the splenic artery)and then causes massive haemorrhage. In the stage of pseudo-aneurysm, a small amount of bleeding may precede massive haemorrhage, which must not be overlooked. Immediate radiological intervention may detect an unruptured pseudo-aneurysm that can be embolised. Once massive bleeding occurs, immediate angiography again should first be considered because it not only provides the chance of embolisation but can also identify the bleeding point. In immediate re-laparotomy, the bleeding artery is sometimes difficult to identify or reach due to severe adhesion and/or inflammation.

Postsplenectomy infections

There is increasing evidence that splenectomy predisposes the patient to an increased risk of bacterial infections in both the early postoperative period and probably for the remainder of their life. Immediate prophylaxis with twice daily oral penicillin is now recommended for patients of all ages. The patient should also be immunised with vaccines against pneumococci, meningococcus and Haemophilus influenzae. If the splenectomy has been planned as part of a radical procedure these vaccines are most effective if administered preoperatively. The patient should have an annual influenza vaccine and an updated pneumococcal vaccine about every 3 years.

Late sequelae and complications

Side-effects and postprandial sequelae

No gastrectomised patient can eat in the same way he or she used to eat, at least during the first few postoperative months. Good dietary advice is essential and patients should understand what their stomach used to do and how they can cope with their status without part or all of their stomach. The author usually explains this as follows: ‘The stomach has three major functions:(1) it stores the food that has been swallowed; (2) it digests and dilutes it; and (3) it slowly pushes it out to the duodenum (taking many hours after a greasy meal). These functions help the small bowel to effectively absorb nutrients. When the stomach has been removed, it is necessary to change eating habits to help the small intestine to work as before: chew well, take time to have the next bite, and have frequent small meals.’

Patients should also be able to accept that their stomach will never come back, and that the lost stomach functions are compensated not by medicine but by an appropriate eating style. Additional specific advice from a dietician will help further.

Early dumping syndrome

Early dumping syndrome appears within 30 minutes after a meal, or even during a meal. The rapid filling of the proximal small intestine with hypertonic food leads to rapid movement of fluid from the extracellular fluid compartment into the gut, and also triggers a complex neurohumoral response. This produces various gastrointestinal and cardiovascular symptoms such as palpitation, bloating, cramping, diarrheoa and nausea, requiring some patients to lie down for an hour after each meal. Most patients with early dumping syndrome can be treated by appropriate dietary adaptation. In severe cases, however, quality of life is restricted and malnutrition can occur rapidly. Careful management involving an experienced dietician should be considered.

Late dumping syndrome or reactive hypoglycaemic attacks

Late dumping syndrome appears 2–3 hours after a meal, and is characterised by faintness, severe hunger, dizziness and cold sweating, which are symptoms of hypoglycaemia. Rapid inflow of carbohydrate to the jejunum causes oxyhyperglycaemia, which induces hyperinsulinemia followed by hypoglycemia. Glucagon-like peptide-1 (GLP-1) secreted from the proximal jejunal mucosa is thought to play some role in this hypersecretion of insulin.

Dietary adaptation is again the main treatment for late dumping syndrome. Patients are advised to decrease the carbohydrate load in their main meals and to take small amounts of carbohydrate between main meals. Those with frequent attacks should carry dextrose tablets to eat at the first sign of symptoms.

In a large-scale investigation into dumping syndrome after gastrectomy (N = 1153),⁷¹ early dumping syndrome was more commonly experienced than late dumping syndrome (68% vs. 38%) and the incidence varied according to the type of gastrectomy but not the postoperative period. Early and late dumping syndromes have different aetiologies and appear independently. During follow-up, a careful history should be taken and appropriate dietary advice should be given.