Gen Thorac Cardiovasc Surg DOI 10.1007/s11748-014-0381-2

ORIGINAL ARTICLE

Optimal surgical management for esophagogastric junction carcinoma Tatsuo Matsuda • Hiroya Takeuchi • Shinichi Tsuwano • Rieko Nakamura Tsunehiro Takahashi • Norihito Wada • Hirofumi Kawakubo • Yoshiro Saikawa • Tai Omori • Yuko Kitagawa



Received: 3 December 2013 / Accepted: 7 February 2014 Ó The Japanese Association for Thoracic Surgery 2014

Abstract Objectives Esophagogastric junction carcinoma incidence is increasing worldwide. However, surgical strategies for this cancer remain controversial. This study aimed to clarify the optimal surgical strategy for esophagogastric junction carcinoma. Methods We retrospectively reviewed a database of 68 consecutive patients with esophagogastric junction carcinoma [Japanese classification of gastric carcinoma (Nishi’s definition): adenocarcinoma, N = 53; squamous cell carcinoma, N = 15] who underwent curative surgical resection at Keio University Hospital between January 2000 and September 2008. Results In both adenocarcinoma and squamous cell carcinoma, most lymph node metastases were located in the lesser curvature area. Mediastinal lymph node metastasis was observed in 4 patients (7.5 %) with adenocarcinoma and 7 patients (46.7 %) with squamous cell carcinoma. No patient presented with lymph node metastases in the pyloric region. The therapeutic value of extended lymph node dissection was 0, except for lymph node station numbers 1, 2, 3, 4sa, 7, and 110. Extended lymph node dissection in the lesser curvature area showed a high therapeutic value. The para-aortic lymph node was the most frequent nodal recurrence site. All patients with tumor centers located below the esophagogastric junction Presented at the 65th Annual Scientific Meeting of The Japanese Association for Thoracic Surgery. T. Matsuda  H. Takeuchi (&)  S. Tsuwano  R. Nakamura  T. Takahashi  N. Wada  H. Kawakubo  Y. Saikawa  T. Omori  Y. Kitagawa Department of Surgery, Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan e-mail: [email protected]

(N = 37) did not develop mediastinal lymph node metastasis or recurrence. Conclusions Proximal gastrectomy through a transhiatal approach may be the optimal surgical strategy for esophagogastric carcinoma. Mediastinal lymph node dissection through a thoracic approach seems unnecessary, particularly when the tumor center is located below the esophagogastric junction. To confirm the necessity of para-aortic nodal dissection, further studies are required. Keywords Esophagogastric junction carcinoma  Nishi’s definition  Surgical management

Introduction The incidence of esophagogastric junction (EGJ) adenocarcinoma is increasing in developed countries, [1–3] including Japan; therefore, the surgical management for this condition is of considerable interest [4–7]. EGJ carcinomas develop along the border between the mediastinum and abdomen and can metastasize to both cavities. The optimal extent of mediastinal and abdominal lymph node dissection remains controversial. The occurrence of EGJ carcinoma metastasis to mediastinal lymph nodes is reported to range from 7 to 40 % [8–14]. Therefore, prophylactic mediastinal nodal dissection appears necessary. However, mediastinal node dissection through a thoracic approach can increase morbidity and markedly reduce the quality of life after surgery. In Western countries, EGJ carcinoma primarily presents as adenocarcinoma; therefore, the Siewert classification of EGJ adenocarcinoma has been accepted [15]. In contrast, squamous cell carcinoma (SCC) of the EGJ is often observed in Japan. Therefore, the Japanese classification of

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metastases were calculated for each nodal station, irrespective of lymph node metastasis for other stations.

gastric carcinoma (Nishi’s definition) of the EGJ is used in Japan [16] and describes EGJ carcinomas as tumors with epicenters within 2 cm of the EGJ, irrespective of histological type. We hypothesized that mediastinal nodal dissection through the thoracic approach did not improve the prognosis of patients with EGJ carcinoma, and that we could perform minimally invasive surgery with adequate radical oncological resection through the transhiatal approach. In this study, to clarify the optimal surgical management, we retrospectively reviewed the medical records of patients with EGJ carcinoma (according to Nishi’s definition) who received surgical resection.

Statistical analyses were performed using SPSS statistical software (version 20; SPSS Inc., Chicago, IL, USA). Clinical and pathological variables were analyzed using the Pearson’s Chi square and Mann–Whitney U tests. Multivariate logistic regression analysis was performed to identify the risk factor for mediastinal lymph node metastasis. Differences were considered to be statistically significant at p values of \0.05.

Materials and methods

Results

Patients and methods

Clinical parameters and pathological findings of patients

We retrospectively reviewed a database of 68 consecutive patients with EGJ carcinoma who underwent curative surgical resection at Keio University Hospital (Tokyo, Japan) between January 2000 and September 2008. EGJ carcinoma was defined according to the Japanese classification of gastric carcinoma (Nishi’s definition) [16]. The EGJ was defined according to the level of macroscopic caliber change of the resected esophagus and stomach, and the area extending from 2 cm above to 2 cm below the EGJ was designated as the EGJ area. Tumors with epicenters in this area were designated as EGJ carcinomas, irrespective of histological type. We performed tumor staging according to the Union for International Cancer Control, seventh edition, tumor-nodemetastasis (TNM) classification of esophageal cancer, and the number of regional lymph node stations was categorized according to the Japanese classification of gastric carcinoma. Analysis of overall survival comprised all causes of death, including those due to unrelated causes. Patient data were evaluated on the basis of age, gender, tumor size, distance between the tumor center and the EGJ, distance from the distal tumor border to the EGJ, distance from the proximal tumor border to the EGJ, surgical methods, perioperative chemotherapy, staging, and recurrence patterns. Therapeutic value of lymph node dissection The therapeutic value of extended lymph node dissection was estimated by multiplying the incidence of metastasis and the 5-year overall survival rate in patients with lymph node metastases for each station [17]. The frequency of metastasis was calculated by dividing the number of patients with lymph node metastases for each station by the number of those in whom that station was dissected. The 5-year overall survival rates in patients with lymph node

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Statistical analysis

The clinical parameters and pathological findings of patients are shown in Table 1. Of 68 patients, 53 presented with adenocarcinoma and 15 with SCC. Although no significant differences were observed in age, gender, neoadjuvant therapy, or adjuvant therapy between the 2 groups, the surgical procedures varied. The transhiatal approach was used more often in patients with adenocarcinoma (86.7 %) than in those with SCC (20.0 %). Lower esophagectomy was primarily performed in patients with adenocarcinoma (94.3 %), as only 40.0 % of patients with SCC underwent this procedure. In patients with adenocarcinoma, total gastrectomy (45.2 %) and proximal gastrectomy (49.0 %) were common, whereas partial gastrectomy with gastric tube reconstruction was often used in patients with SCC (60.0 %). No patient underwent subtotal esophagectomy with total gastrectomy. The tumor centers and proximal tumor borders in patients with SCC were more often located on the oral side as compared with those in patients with adenocarcinoma. Patients with SCC had significantly deeper tumors, higher frequency of lymph node metastases, and more advanced tumor staging than patients with adenocarcinoma. We evaluated the 5-year overall survival rates according to the tissue type. As shown in Fig. 1, the 5-year overall survival rate was 54.7 % in patients with adenocarcinoma and 40.0 % in patients with SCC. No significant difference in overall survival according to the tissue type was observed (p = 0.509). Distribution of lymph node metastasis and therapeutic value of lymph node dissection Figure 2 shows the distribution of nodal metastases to each lymph node station. In patients with both

Gen Thorac Cardiovasc Surg Table 1 Clinical parameters and pathological findings of patients

Total (N = 68)

Adenocarcinoma (N = 53)

SCC (N = 15)

p value

Age (years), mean ± SD

64.5 ± 13.5

65.3 ± 12.2

65.2 ± 7.6

0.608

Gender (M/F)

55/13

45/8

10/5

0.233

Surgical procedure Approach (THA/RTA/LTA)

49/15/4

46/5/2

3/10/2

\0.001

Esophagectomy (subtotal/lower)

12/56

3/50

9/6

\0.001

Gastrectomy [total/proximal/partial (gastric tube)]

29/27/12

24/26/3

5/1/9

\0.001

Splenectomy (±) Neoadjuvant therapy (±)

11/57 11/57

10/43 7/46

1/14 4/11

0.257 0.211

Adjuvant therapy (±)

11/57

8/45

3/12

0.649

Tumor length (mm), mean ± SD

40.4 ± 19.6

38.3 ± 20.1

47.6 ± 15.1

0.539

Location of tumor center from the EGJ (mm), mean ± SD

2.6 ± 11.8

6.8 ± 10.2

-11.2 ± 6.6

0.004

Location of proximal tumor border from the EGJ (mm), mean ± SD

-14.4 ± 16.4

-9.2 ± 13.5

-32.5 ± 11.7

0.01

Location of distal tumor border from the EGJ (mm), mean ± SD

20.0 ± 13.8

22.7 ± 14.1

10.7 ± 8.1

0.312

pT1

21

19

2

pT2

11

11

0

pT3

29

17

12

pT4

7

6

1

pN0

31

28

3

pN1

15

11

4

pN2

15

12

3

pN3

7

2

5

UICC stage Stage IA

18

18

0

Stage IB

6

6

0

Stage IIA

7

4

3

Stage IIB

6

5

1

Stage IIIA

8

6

2

Stage IIIB

9

7

2

Stage IIIC

14

7

7

Stage IV

0

0

0

Postoperative diagnosis pT factor

0.009

pN factor

THA abdominal-transhiatal approach, RTA right thoracoabdominal approach, LTA left thoracoabdominal approach, pT, pN factors tumor/ node (TNM) staging, UICC Union for International Cancer Control

adenocarcinoma and SCC, most lymph nodal metastases were located in the lesser curvature area, such as lymph node stations 1, 3, and 7. Mediastinal lymph node metastasis was observed in 4 patients with adenocarcinoma (7.5 %) and 7 patients with SCC (46.7 %). No patient presented with lymph node metastases in the pyloric region. Table 2 shows the therapeutic value of extended nodal dissection of each lymph node station. The 5-year overall survival rate in patients with lymph node metastases was 0 %, except for metastases for stations 1, 2, 3, 4sa, 7, and

0.005

\0.001

110. High therapeutic values were observed with extended lymph node dissection in the lesser curvature area, including stations 1, 3, and 7. Recurrence patterns Initial recurrence patterns are shown in Table 3. Of 68 patients, 22 (32.3 %) experienced relapse, and 30 recurrence sites were diagnosed as initial recurrence sites. Ten of 68 patients (14.7 %) showed nodal recurrence at one or more regions. Nodal recurrence more frequently involved

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the para-aortic lymph nodes (N = 5, 7.4 %) than the gastric (N = 3, 4.4 %) or mediastinal lymph nodes (N = 3, 4.4 %). All 3 patients with mediastinal lymph node recurrence presented with metastatic mediastinal lymph nodes at the time of surgery. No other recurrence was identified in 4 patients (80 %) with initial para-aortic lymph node recurrence. All 4 1.0 Adenocarcinoma N=43

0.8

Survival rate

5 years over all survival

0.6

54.7% SCC N=15

0.4

40.0%

0.2 Adenocarcinoma vs SCC , p=0.509 (Log-rank test)

0.0 0

1

2

3

4

5

Time after surgery (years)

Fig. 1 Overall survival after resection of EGJ carcinoma

Fig. 2 The distribution of lymph node (LN) metastases in 68 surgically treated patients (adenocarcinoma, N = 53; SCC, N = 15). Asterisks indicate the numbers of patients in whom lymph node metastases were detected for each indicated lymph node station. Thoracic lymph node station numbers. 105 Upper thoracic paraesophageal LNs, 106recL left recurrent nerve LNs, 106recR right recurrent nerve LNs, 108 middle thoracic paraesophageal LNs, 109 main bronchus LNs, 110 lower thoracic paraesophageal LNs, 111 supradiaphragmatic LNs. Abdominal lymph node station numbers. 1

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patients (adenocarcinoma, N = 2; SCC, N = 2) had advanced EGJ carcinoma. Tumor depth was T3 in 2 patients and T4 in 2 patients. All 4 patients had more than 4 metastatic lymph nodes pathologically. Mediastinal lymph node metastasis Mediastinal lymph node metastasis was observed in 11 patients (adenocarcinoma, N = 4; SCC, N = 7). Patients with SCC had a higher incidence of mediastinal lymph node metastasis as compared with patients with adenocarcinoma. Table 4 shows the clinical parameters and pathological findings of patients with and without mediastinal lymph node metastasis. Most patients (94.1 %) without mediastinal lymph node metastases underwent surgery through the transhiatal approach. The tumor centers and proximal tumor border of patients with mediastinal lymph node metastases were more often located on the oral side as compared with patients without mediastinal lymph node metastasis. In all patients, the tumor centers were located above the EGJ. We conducted multivariate analysis to identify the risk factor for mediastinal lymph node metastasis. As shown in

Right cardiac LNs. 2 left cardiac LNs, 3 LNs along the lesser curvature, 4sa left greater curvature LNs along the short gastric arteries, 7 LNs along the left gastric artery, 8a LNs along the common hepatic artery anterosuperior group, 9 LNs along the celiac artery, 10 LNs at the splenic hilum, 11p LNs along the proximal splenic artery, 19 infradiaphragmatic lymph nodes predominantly along the subphrenic artery, 20 paraesophageal LNs in the diaphragmatic esophageal hiatus

Gen Thorac Cardiovasc Surg Table 2 Therapeutic value of lymph node dissection Lymph node station

Incidence of metastasis (%)

#1

29.4 % (20/68)

35.0

#2

17.6 % (12/68)

8.3

1.4

#3 #4sa

23.5 % (16/68) 3.6 % (2/55)

43.7 100.0

10.3 3.6

#7

16.1 % (11/68)

27.2

4.3

#110

18.2 % (4/22)

25.0

4.5

Table 3 Initial recurrence pattern

5-year overall survival rate (%)

Estimated therapeutic value 10.3

Recurrence site

N = 22

Lymphatic

N = 10

Para-aortic

5

Gastric regional

3

Mediastinal

3

Cervical

2

Hematogenous

N = 11

Lung

6

Liver

5

Bone

2

Peritoneal

3

Esophageal

1

Table 5, when the tumor center from the EGJ was located on the esophageal side, the risk of mediastinal lymph node metastasis was significantly increased. In contrast, when the proximal tumor border from the EGJ was located on the esophageal side, the risk of mediastinal lymph node metastasis was not significantly reduced. In addition, histological type was not a significant risk factor for metastasis to mediastinal lymph nodes.

Discussion In this retrospective study, we reviewed the surgical outcomes of 68 patients with EGJ carcinoma according to Nishi’s definition. EGJ carcinoma was defined according to the Siewert classification of adenocarcinoma. However, in Japan, EGJ carcinoma has been historically defined according to Nishi’s definition, which includes both adenocarcinoma and SCC. This difference is supported by the higher incidence of SCC in Japan. However, surgical strategies for EGJ carcinoma remain controversial. The Japan Clinical Oncology Group (JCOG) conducted a multicenter randomized controlled trial in Japan (JCOG 9502) [18]. This trial assessed 165 patients with EGJ adenocarcinoma (Siewert type II, N = 95; Siewert type III,

N = 70) to compare the effects of the left thoracoabdominal approach (LTA) with those of the abdominal-transhiatal approach. The 5-year overall survival rates were 52.3 and 37.9 % in the transhiatal approach and LTA groups, respectively. The hazard ratio of death for the LTA vs. the transhiatal approach was 1.36. Morbidity was higher after the LTA than the transhiatal approach. Therefore, we concluded that the LTA was not justified for the treatment of type II or III EGJ adenocarcinoma if the length of esophageal invasion was B3 cm. These findings identified a consensus on the surgical strategy for EGJ carcinoma in Japan. However, the optimal surgical strategy for EGJ carcinoma has been discussed after the JCOG 9502 trial. Therefore, the optimal extent of lymph node dissection and the necessity of using the thoracic approach and total gastrectomy for EGJ carcinoma remain controversial. In the present study, we identified the distribution of lymph node metastasis and evaluated the therapeutic value of extended lymph node dissection. Our data showed that lymph node stations 1, 2, 3, and 7 had high rates of metastasis, and that no lymph node metastases were observed in the pyloric region. The therapeutic value of extended lymph node dissection was 0, except for lymph node stations 1, 2, 3, 4sa, 7, and 110. These results were almost identical to those of previous reports [4–7]. From these results, proximal gastrectomy through the transhiatal approach appears to be the minimally invasive surgery for the treatment of EGJ carcinoma, with adequate radical oncological resection. Other than lymph node station 110, which can be dissected through the transhiatal approach, the therapeutic value of extended mediastinal lymph node dissection was 0, and the metastasis rate was low. Thus, mediastinal lymph node dissection through the thoracic approach seems unnecessary and invasive. In addition, 37 patients had tumors with centers located below the EGJ, and all were free from mediastinal lymph node metastasis and recurrence (Table 4). According to the results of multivariate analysis, the location of the tumor center from the EGJ is a more important factor than histological type or location of proximal tumor border to predict the occurrence of mediastinal lymph node metastasis. Therefore, if the EGJ tumor center is located below the EGJ, the need for mediastinal lymph node dissection appears to be reduced. In our study, we investigated the initial recurrence patterns. We believed that the high recurrence rate of the para-aortic lymph node was of considerable importance to suggest an optimal surgical strategy. Following the results of the multicenter randomized controlled trial JCOG 9501, several hospitals, including ours, no longer perform para-aortic nodal dissection for EGJ carcinoma [19]. In this trial, treatment with D2 lymphadenectomy plus para-

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Gen Thorac Cardiovasc Surg Table 4 Clinical parameters and pathological findings of patients Mediastinal lymph node metastasis (?)

Mediastinal lymph node metastasis (-)

p value

Histological type (adenocarcinoma/SCC)

4/7

49/8

\0.001

Age (years), mean ± SD

65.7 ± 9.5

64.6 ± 14.2

\0.914

Gender (M/F)

7/4

46/11

Approach (THA/RTA/ LTA)

1/9/1

Esophagectomy (subtotal/lower) Gastrectomy [total/ proximal/partial (gastric tube)] Splenectomy (±)

Table 5 Multivariate logistic regression analysis to identify the risk factor for mediastinal lymph node metastasis Variables

HR (95 % CI)

p value

Histological type (adenocarcinoma/SCC)

1.11 (0.15–7.83)

0.916

Tumor depth (pT1, pT2/pT3, pT4)

19.62 (1.23–312.7)

0.035

0.78 (0.63–0.95)

0.016

0.211

Location of tumor center from the EGJ (mm)

0.233

\0.001

Location of proximal tumor border from the EGJ (mm)

1.08 (0.95–1.23)

48/6/3

7/4

5/52

\0.001

The location from the EGJ defined the esophageal side as minus and defined the stomach side as plus

3/1/7

26/26/5

\0.001

0/11

11/46

0.112

Tumor length (mm), mean ± SD Location of tumor center from the EGJ (mm), mean ± SD

49.6 ± 15.7

39.4 ± 20.2

0.047

-11.5 ± 7.0

4.9 ± 10.8

\0.001

Location of tumor center (esophagus side/EGJ/ stomach side)

10/1/0

12/8/37

\0.001

Location of proximal tumor border from the EGJ (mm), mean ± SD

-31.7 ± 12.4

-11.8 ± 15.6

\0.001

Location of distal tumor border from the EGJ (mm), mean ± SD

11.5 ± 7.6

21.4 ± 14.1

0.01

Surgical procedure

pT tumor (TNM) staging

Postoperative diagnosis pT factor

0.052

pT1

1

20

pT2

0

11

pT3

8

21

pT4

2

5 \0.001

pN factor pN0

0

31

pN1 pN2

1 5

14 10

pN3

5

2 \0.001

UICC stage Stage IA

0

18

Stage IB

0

6

Stage IIA

0

7

Stage IIB

0

6

Stage IIIA

1

7

Stage IIIB

4

5

Stage IIIC

6

8

Stage IV

0

0

THA abdominal-transhiatal approach, RTA right thoracoabdominal approach, LTA left thoracoabdominal approach, pT, pN factors tumor/ node (TNM) staging, UICC Union for International Cancer Control

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aortic nodal dissection did not improve the overall survival rate in patients with curable gastric cancer as compared with D2 lymphadenectomy alone. Therefore, it is considered that the target of the trial was gastric cancer and not EGJ carcinoma. The benefit of para-aortic nodal dissection for EGJ carcinoma remains controversial. EGJ carcinomas are anatomically close to the para-aortic region and, clinically, lymph node metastases are often observed in this region. Siewert et al. [20] recommended dissections of the left retroperitoneal para-aortic and left renal hilum nodes in patients with enlarged nodes in these areas according to preoperative or intraoperative staging. As shown in Table 3, para-aortic lymph node recurrence was identified as the most frequent mode of lymph node recurrence, which is in accordance with the findings of a previous report [4]. Other recurrence was not identified in 4 patients (80 %) with initial para-aortic lymph node recurrence. Thus, if these patients underwent para-aortic nodal dissection, they may be recurrence free. We expect that a randomized controlled study will clarify the benefits of para-aortic nodal dissection for EGJ carcinoma. This study had some limitations. First, this study was retrospective. Second, the surgical strategy was determined by the surgeon; thus, various surgical procedures were included in this study. To strictly evaluate the therapeutic value of lymph node dissection, it is necessary to use a standard surgical procedure. In conclusion, proximal gastrectomy through the transhiatal approach with adequate radical oncological resection may be a minimally invasive surgical technique in EGJ carcinoma. Mediastinal lymph node dissection through the thoracic approach seems unnecessary, particularly if the tumor center is located below the EGJ. To confirm the necessity of para-aortic nodal dissection, further studies are required. Acknowledgments study.

The authors received no grant support for this

Gen Thorac Cardiovasc Surg Conflict of interest interest exists.

The authors have declared that no conflict of

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Optimal surgical management for esophagogastric junction carcinoma.

Esophagogastric junction carcinoma incidence is increasing worldwide. However, surgical strategies for this cancer remain controversial. This study ai...
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