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Surgical resection for hepatic metastasis from gastric cancer: a multi-institution study

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Oncotarget. 2017; 8:71147-71153. https://doi.org/10.18632/oncotarget.16705

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Ailin Song, Xiaofeng Zhang, Feng Yu, Debang Li, Wenyu Shao, Yanming Zhou _

Abstract

Ailin Song1, Xiaofeng Zhang2, Feng Yu3, Debang Li4, Wenyu Shao5 and Yanming Zhou6

1Department of General Surgery, Second Hospital of Lanzhou University, Lanzhou, China

2Department of Special Treatment, Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, Shanghai, China

3Department of Hepatobiliary Surgery, the 101th Hospital of Chinese PLA, Wuxi, China

4Department of General Surgery, First Hospital of Lanzhou University, Lanzhou, China

5Department of Liver Surgery, First Affiliated Hospital of Nanjing Medical University, Nanjing, China

6Department of Hepatobiliary and Pancreatovascular Surgery, First Affiliated Hospital of Xiamen University, Xiamen, China

Correspondence to:

Yanming Zhou, email: zhouymsxy@sina.cn

Keywords: gastric cancer, liver metastases, hepatectomy, prognosis

Received: January 02, 2017     Accepted: March 21, 2017     Published: March 30, 2017

ABSTRACT

Background: The beneficial effect of surgical resection for hepatic metastasis from gastric cancer (HMGC) remains elusive. This study was conducted to analyze surgical outcomes of HMGC and determine the prognostic factors associated with survival.

Results: The in-hospital mortality rate was zero, and the overall morbidity rate was 56%. The overall 1-, 3-, and 5-year survival rate after surgery was 87.5%, 47.6%, and 21.7%, respectively, with a median survival time of 34.0 months. Multiple liver metastases (hazard ratio [HR] =1.998; 95% confidence interval [CI] = 1.248-3.198; P = 0.004) and ≥ T3 stage of the primary gastric cancer (HR = 2.065; 95% CI = 1.201–3.549; P = 0.009) were independent prognostic determinants in the multivariate analysis.

Materials and Methods: Data on surgical resection of 96 patients with HMGC at six institutions in China were analysed retrospectively. Prognostic factors were assessed by multiple stepwise regression analysis using the Cox model.

Conclusions: Surgical resection for HMGC is feasible and beneficial to long-term survival in selected patients.


Surgical resection for hepatic metastasis from gastric cancer: a multi- institution study | Song | Oncotarget

INTRODUCTION

It was reported that about 14% gastric cancer patients developed hepatic metastasis, and more than 30% gastric cancer patients developed metachronous liver metastasis after surgical resection of the primary gastric cancer [1]. Although previous studies [232] reported that hepatectomy may provide an opportunity of long-term survival in these patients (Table 1), most of these studies were conducted on the single-institution basis including no more than 50 cases, and therefore the beneficial effect of hepatectomy are not well-defined. The objective of this study was to analyze the outcome of surgical resection of hepatic metastasis from gastric cancer (HMGC) and determine prognostic factors associated with survival in a relatively large multi-institution cohort of patients.

Table 1: Literature overview of outcomes following hepatectomy for metastatic gastric cancer

Reference

Year

Country

Study interval

No. of patients

Mortality (%)

3-year OS (%)

5-year OS (%)

MST (months

Ambiru et al. [2]

2001

Japan

1975–1999

48

0

18

12

Imamura et al. [3]

2001

Japan

1990–1997

17

0

22

0

Okano et al. [4]

2002

Japan

1986–1999

19

0

34

34

Zacherl et al. [5]

2002

Austria

1980–1999

15

6.7

14.3

0

8.8

Sakamoto et al. [6]

2003

Japan

1985–2001

22

5

38

38

21

Shirabe et al. [7]

2003

Japan

1979–2001

36

0

26

26

Adam et al. [8]

2006

France

1983–2004

64

27

15

Sakamoto et al. [9]

2007

Japan

1990–2005

37

0

11

31

Cheon et al. [10]

2008

Korea

1995–2005

41

3

31.7

20.8

17

Morise et al. [11]

2008

Japan

1989–2004

18

0

27

27

13

Thelen et al. [12]

2008

Germany

1988–2002

24

4.2

22

15

10

Ueda et al. [13]

2009

Japan

1991–2005

15

0

60

60

Makino et al. [14]

2010

Japan

1992–2007

16

0

46.4

37.1

38.3

Tsujimoto et al. [15]

2010

Japan

1980–2007

17

0

37.5

31.5

34

Dittmar et al. [16]

2012

Germany

1995–2009

15

0

54

27

48

Garancini et al. [17]

2012

Italy

1998–2007

21

0

31

19

11

Miki et al. [18]

2012

Japan

1995–2009

25

42.8

36.7

33.4

Schildberg et al.19]

2012

Germany

1972–2008

31

6

25

13

14

Takemur et al. [20]

2012

Japan

1993–2011

64

0

50

37

34

Wang et al. [21]

2012

China

2003–2008

30

0

16.7

16.7

11

Baek et al. [22]

2013

Korea

2003-2010

12

0

39

39

31

Chen et al. [23]

2013

China

2007–2012

20

0

20

22.3

Qiu et al. [24]

2013

China

1998–2009

25

0

70.4

29.4

38

Komeda et al. [25]

2014

Japan

2000–2012

24

0

40.1

40.1

22.3

Wang et al. [26]

2014

China

1996–2008

35

0

17.9

10.3

14

Kinoshita et al. [27]

2015

Japan

1990–2010

256

1.6

77.3

41.9

31.1

Shinohara et al. [28]

2015

Japan

1995–2010

19

0

31.7

31.7

27

Tiberio et al. [29]

2015

Italy

1997–2011

53

14

9.3

13

Oki et al. [30]

2016

Japan

2000–2010

94

51.4

42.3

40.8

Tiberio et al. [31]

2016

Italy

1990–2013

105

0.9

20.3

13.1

14.6

Markar et al. [32]

2017

UK

1997–2012

78

10.3

42

31

Abbreviations: MST = median survival time; OS = overall survival.

RESULTS

Patient characteristics

The study group included 72 (75%) men and 24 (25%) woman with a median age of 63 (range 32–78) years. Of these, 59 (61.5%) patients presented with synchronous liver metastases and 37 (38.5%) presented with metachronous liver metastases. In the latter group, the median interval between gastrectomy and hepatectomy for hepatic metastasis was 8.7 months (range, 4–32 months). Forty-two (43.7%) patients presented with solitary lesions, and 54 (56.3%) had multiple lesions. Ninety-one (94.8%) patients achieved curative resection. Fifty-eight (60.4%) patients received adjuvant therapy after hepetectomy.

Results of surgical resection

There was no intra- or postoperative mortality. A total of 63 complications occurred in 46 patients (47.9%), of whom 11 (11.4%) patients had major morbidities (Clavien-Dindo ≥ 3a).

During the median follow-up period of 33 months, 77 (80.2%) patients experienced recurrences. The most frequently site of recurrence was the liver (n = 45, 58.4%), followed by the lymph node (n = 11, 14.3%), peritoneum (n = 8, 10.3%), and lung (n = 8, 10.3%). Details of the recurrences were unknown in 5 cases (6.5%). Only 3 (6.7%) of the 45 patients with liver recurrences underwent re-hepatectomy.

The 1-, 3- and 5-year overall survival (OS) rate of the entire cohort of patients after surgery was 87.5%, 47.6% and 21.7%, respectively, with a median survival time of 34.0 months (Figure 1). Several factors were found to be associated with poor prognosis in univariate analysis (Table 2). Multiple liver metastases (hazard ratio [HR] = 1.998; 95% confidence interval [CI] = 1.248–3.198; P = 0.004) and ≥ T3 stage of the primary gastric cancer (HR = 2.065; 95% CI = 1.201–3.549; P = 0.009) were independent prognostic determinants, as shown by multivariate analysis.

Cumulative overall survival for patients who underwent resection for hepatic metastasis from gastric cancer.

Figure 1: Cumulative overall survival for patients who underwent resection for hepatic metastasis from gastric cancer.

Table 2: Univariate analysis of prognostic factors for overall survival

Variables

Number

MST (months)

P-value

Gender

 Male

72

40

0.714

 Female

24

28

Age

 ≥ 65

51

36

0.739

 < 65

45

34

T stage of gastric cancer

 < T3

47

46

0.007

 ≥ T3

59

24

Lymph node status of gastric cancer

 N0-N1

28

45

0.015

 N2-N3

68

30

Histologic grade of gastric cancer

 Well-moderate

62

42

0.032

 Poorly

34

29

Histologic type of gastric cancer

 Intestinal

61

44

0.058

 Diffuse

12

17

Type of gastrectomy

 Total gastrectomy

33

22

0.373

 Subtotal gastrectomy

63

40

Timing of hepatic metastasis

 Synchronous

59

43

0.167

 Metachronous

37

33

Type of hepatectomy

 Major (≥ 3 segments)

35

34

0.456

 Minor (< 3 segments)

61

36

Curative resection

 Yes

91

39

0.031

 No

5

27

Maximum hepatic metastasis size

 < 5 cm

71

44

0.069

 ≥ 5 cm

25

28

Number of metastases

 Solitary

42

42

0.021

 Multiple

54

29

Distribution of liver metastases

 Unilobar

57

41

0.394

 Bilobar

29

32

Morbidity

 Yes

46

40

0.237

 No

50

31

Adjuvant chemotherapy

 Yes

58

42

0.172

 No

38

35

Abbreviations: MST = median survival time.

DISCUSSION

Although solid clinical evidence exists to support surgical resection as the optimal option for the treatment of colorectal liver metastasis (CLM), data evaluating the postoperative outcome of HMGC are limited and controversial (Table 1). This may be explained by the fact that most patients with HMGC presented with multiple lobar metastases, gross peritoneal dissemination, extensive lymph node metastases, distant metastasis, or direct invasion to other organs at time of diagnosis, and therefore were considered unamenable to surgery [5]. It was reported that patients with potentially resectable HMGC treated with systemic chemotherapy had a median survival of 5.5 months, and the number of 3-year survivors was zero [23]. A systematic review of 870 patients from 23 studies performed by Petrelli and colleagues in 2015 demonstrated that resection of HMGC was associated with a 22-month median survival and a 23.8% 5-year OS rate [33]. A similar systematic review was published by Markar et al in 2016, which included 991 patients and come to similar conclusions, with a median 5-year OS of 27% [34]. In accordance with these two reports, the present study also confirmed the benefit of surgical resection for HMGC in achieving long-term survival in a relatively large cohort of patients drawn from multi-centers in China. The 5-year OS rate after surgery was 21.7% with a median survival time of 34.0 months.

Safety is an important concern in such an aggressive management strategy. Hepatic resection of metachronous liver disease is technically demanding because of intra-abdominal adhesions caused by previous surgery. Synchronous resection of the HMGC and primary tumor may be associated with increased post-operative complications. However, in the present study and previous reports, resection could be safely performed with acceptable operative mortality and morbidity [1928]. It should be noted that this favourable outcome may be attributed to careful selection of patients with limited disease, as reflected by major hepatectomy is not performed frequently [27]. In addition, patients with HMGC usually had no underlying cirrhosis, a factor associated with a high risk of postoperative liver failure because of the limited regenerative capacity of the liver remnant.

Multivariate analysis in our series disclosed that multiple liver metastases and ≥ T3 stage of the primary gastric cancer were independent prognostic determinants. These data may have important implications in helping select patients for surgical resection. There is evidence that postoperative complications, especially major complications, have a negative impact on long-term survival after oncological surgery [35]. Immunosuppression secondary to septic complications may increase the growth of occult micrometastasis, and some complications may make patients unfit for adjuvant therapy or delay the time interval. However, we did not find that OS was significantly reduced in patients with complications in our study. The fact that there were only 11.4% of patients with major complications in current study, it is possible that failure to detect a clinically significant difference represents a type-II error.

Percutaneous radiofrequency ablation (RFA) is generally accepted as a safe, effective and minimally invasive treatment for patients with CLM [36]. However, few studies have focused on RFA for HMGC. RFA may contribute to local control of single liver-only metastatic lesions [37]. No reliable data on the comparative therapeutic efficacy of RFA and hepatic resection for resectable HMGC are available at present, and therefore RFA should not be recommended as an alternative to surgical resection at this disease stage.

Recurrence following surgical resection of HMGC is common and mostly occurs in the remaining liver tissue. Repeat hepatectomy seems beneficial to patients with solitary intrahepatic recurrence [25, 27]. Unfortunately, very few patients are potential candidates for hepatic resection because of extensive metastases [27].

The efficacy of adjuvant chemotherapy after liver resection of HMGC remains unclear. Qiu et al. [24] reported that patients who received adjuvant chemotherapy had significantly better survival. However, our and other studies [9, 25, 27] were unable to confirm their conclusion. These different findings may be explained by differences in the regimens used, the timing and duration of cytotoxic agent administration, and patient selection between these studies. Unlike CLM, it seems impossible to test the clinical significance of adjuvant chemotherapy for HMGC in a prospective manner because of the rarity of candidates [27].

The study has some limitations, including the retrospective nature and possible bias in patient selection. More data are needed to further verify the conclusion of the present study.

In conclusion, this large-cohort study has demonstrated that surgical resection for HMGC is feasible and beneficial to long-term survival in selected patients.

MATERIALS AND METHODS

Patients

Included in this study were 96 patients who underwent surgical resection for HMGC between January 2001 and January 2012 in six medical institutions in China. The study was approved by the ethics committee of each contributing institution. Written informed consent forms were not required from the patients due to the retrospective approach of the study. In general, surgical resection of HMGC followed the following criteria: (1) curative resection (microscopic tumor removal based on the histopathologic evaluation) of the primary tumor and liver metastasis thought to be technically accessible; and (2) no sign of concomitant extrahepatic metastasis on preoperative imaging. Data were collected retrospectively by reviewing the medical records, including patient age and sex at hepatic resection; pathological characteristics of the primary gastric cancer and hepatic metastasis; and short- and long-term outcomes after surgery. Postoperative mortality was defined as any death occurring within 30 days of surgery or within the same hospital stay. Postoperative complications were defined as occurrence of any medical or surgical complication during the hospital stay and graded according to the Clavien-Dindo classification [38]. The primary tumor stage and regional lymph node status were classified according to the 7th edition of the International Union Against Cancer of gastric cancer [39]. The types of hepatectomy were classified in accordance with the Brisbane 2000 nomenclature [40].

Statistical analysis

Overall survival was determined by Kaplan-Meier analysis. Factors related to survival selected by univariate analysis with P < 0.05 were entered into a multivariate analysis using Cox proportional hazard regression model to determine the independent risk factors for survival. All statistical analyses were performed using SPSS for Windows (version 11.0; SPSS Institute, Chicago, IL, USA). P < 0.05 was considered statistically significant.

Abbreviations

HMGC: hepatic metastasis from gastric cancer; OS: overall survival; HR: hazard ratio; CI: confidence interval; CLM: colorectal liver metastasis; RFA: radiofrequency ablation.

Authors’ contributions

Conception/Design: Yanming Zhou. Provision of study materials or patients: Ailin Song, Xiaofeng Zhang, Feng Yu, Debang Li, Wenyu Shao,Yanmng Zhou. Collection and/or extract data: Ailin Song, Xiaofeng Zhang, Feng Yu, Debang Li, Wenyu Shao,Yanmng Zhou. Data analysis and statistical guidance: Ailin Song, Yanming Zhou. Final approval of the manuscript: Ailin Song, Xiaofeng Zhang, Feng Yu, Debang Li, Wenyu Shao,Yanmng Zhou

CONFLICTS OF INTEREST

The authors indicated no financial relationships.

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