ORIGINAL ARTICLE

pISSN 2288-6575 • eISSN 2288-6796

https://doi.org/10.4174/astr.2018.94.3.135
Annals of Surgical Treatment and Research

The optimal surgical resection approach for T2

gallbladder carcinoma: evaluating the role of surgical
extent according to the tumor location
Tae Jun Park1,2, Keun Soo Ahn1, Yong Hoon Kim1, Tae-Seok Kim1, Jung Hee Hong3, Koo Jeong Kang1
1
Department of Surgery, Keimyung University Dongsan Medical Center, Keimyung University School of Medicine, Daegu, Korea
2
Department of Surgery, Andong Medical Group Hospital, Andong, Korea
3
Department of Radiology, Keimyung University Dongsan Medical Center, Keimyung University School of Medicine, Daegu, Korea

Purpose: The clinical behavior of T2 gallbladder cancer varies among patients. The aims of this study were to identify
prognostic factors for survival and recurrence, and to determine the optimal surgical strategy for T2 gallbladder cancer.
Methods: We conducted a retrospective analysis of 78 patients with T2 gallbladder cancer who underwent surgical
resection for gallbladder cancer.
Results: Twenty-eight patients (35.9%) underwent simple cholecystectomy and 50 (64.1%) underwent extended
cholecystectomy. Among 56 patients without LN metastasis (n = 20) or unknown LN status (no LN dissection, n = 36), the
5-year disease-free survival rates were 81.6%, and 69.8% (P = 0.080). In an analysis according to tumor location, patients
with tumors located on the hepatic side (n = 36) had a higher recurrence rate than patients with tumors located on the
peritoneal side only (n = 35) (P = 0.043). On multivariate analysis, R1 resection and lymph node metastasis were significant,
independent prognostic factors for poor disease-free and overall survival.
Conclusion: R0 resection and LN dissection are an appropriate curative surgical strategy in patients with T2 gallbladder
cancer. Tumors located on the hepatic side show worse prognosis than tumors located on the peritoneal side only, hepatic
resection should be considered.
[Ann Surg Treat Res 2018;94(3):135-141]

Key Words: Gallbladder neoplasms, Surgery

INTRODUCTION 72%–100% in earlier studies [2-5] and simple cholecystectomy

is considered to be an adequate surgical approach for T1
Gallbladder cancer is the most frequent malignant neoplasm gallbladder cancer [6]. Meanwhile, the prognosis of T3 and T4
of the biliary tract. Unfortunately, the prognosis of gallbladder gallbladder cancer with serosal involvement and invasion into
cancer, except for early-stage cancer, is very poor. The depth of adjacent organs or main vessels is still very dismal with 5-year
tumor invasion and lymph node (LN) metastasis were reported survival rates of <20% [2,7]. As compared with T1, T3, and T4
to be the most important prognostic factors for gallbladder gallbladder cancer, the prognosis of T2 gallbladder cancer is very
cancer [1]. T1 carcinoma confined to the lamina propria (T1a) heterogeneous and is difficult to predict. Moreover, T2 was the
or muscle layer (T1b) had favorable 5-year survival rates of most common T stage of gallbladder cancer in several studies

Received May 29, 2017, Revised July 14, 2017, Accepted August 3, 2017 Copyright ⓒ 2018, the Korean Surgical Society
Corresponding Author: Koo Jeong Kang cc Annals of Surgical Treatment and Research is an Open Access Journal. All
Department of Surgery, Keimyung University Dongsan Medical Center, articles are distributed under the terms of the Creative Commons Attribution Non-
Keimyung University School of Medicine, 56 Dalseong-ro, Jung-gu, Daegu Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which
41931, Korea permits unrestricted non-commercial use, distribution, and reproduction in any
Tel: +82-53-250-7655, Fax: +82-53-250-7322 medium, provided the original work is properly cited.
E-mail: [email protected]
ORCID code: https://orcid.org/0000-0003-1385-8308

Annals of Surgical Treatment and Research 135

 Annals of Surgical Treatment and Research 2018;94(3):135-141

[5,7,8]. Therefore, further improvements in the overall survival resection. If the depth of invasion was uncertain, additional
rate of gallbladder cancer could be achieved by improving the procedures or closure without extended resection were selected
survival of patients with T2 gallbladder cancer. on a case-by-case basis. For patients who initially underwent
There is a hope for long-term survival only in the case of simple cholecystectomy, additional extended resection was
complete resection and if there are no residual tumor cells. The performed after confirming the patient’s histopathological
recently published National Comprehensive Cancer Network findings.
guidelines and American Joint Committee on Cancer (AJCC) We intentionally performed extended cholecystectomy, at
Cancer Staging Manual (7th edition) recommend extended least, in patients with T2 gallbladder cancer. However, if the
cholecystectomy including both LN dissection and hepatic patient refused to undergo additional extended resection by
resection. However, the extent of extended cholecystectomy has open laparotomy or had severe comorbidities, even if extended
not been defined and the adequate surgical resection approach resection was necessary on the basis of the pathologic findings
for T2 gallbladder cancer is still debated. after simple cholecystectomy, the patient was very carefully
The aims of this retrospective study were to identify followed up without additional procedures.
prognostic factors for survival and recurrence, and to determine Bile duct resection was performed if the tumor was located
an adequate surgical strategy for T2 gallbladder cancer, focusing at the infundibulum or near the cystic duct. Partial hepatic
on the role of hepatic resection. resection (wedge resection or S4b and S5 resection) was done
if the tumor was located in the liver bed. Typically, regional
METHODS LN dissection (Nos. 8, 12, 13) was performed and aortocaval
LN dissection was considered for selected patients who had
This was a retrospective study and approved by the suspicious finding in preoperative radiologic studies.
Institutional Review Board of Keimyung University Dongsan The following microscopic characteristics were evaluated:
Medical Center (approval number: 2016-01-040-001) with differentiation, the presence of lymphovascular and perineural
agreement exemption for informed consent. invasion, LN metastasis, and margin status. R0 resection was
Between December 2000 and August 2012, 165 patients with defined as margin-negative resection in the pathologic report
gallbladder cancer underwent complete resection at a tertiary and the absence of grossly residual tumors, LN enlargement,
hospital in Daegu, Korea. Of these, 78 patients (47.2%) had pT2 and distant metastasis in the operative and radiologic findings.
gallbladder cancer. R1 resection was performed in 4 patients R1 resection was defined as the presence of residual tumor cells
and R0 resection in 74 patients. The following preoperative under microscopy. R2 resection was defined as the presence
demographic and clinical characteristics were retrospectively of a macroscopic residual tumor, but there were no R2 cases
obtained from the patients’ medical records: age, sex, types of among the 78 patients with T2 gallbladder cancer. Cancer stage
operative procedure, tumor markers, operation time, need for was evaluated according to the AJCC Cancer Staging Manual (7th
transfusion, postoperative complications, hospital stay, and edition).
mode of recurrence. The location of the tumor was defined The surgical outcomes and prognostic factors were
based on preoperative radiologic images, mostly CT scan. retrospectively evaluated based on these factors. Statistical
Hepatic side gallbladder cancer was defined when tumor was analysis was performed using IBM SPSS ver. 18.0 (IBM Co.,
located within gallbladder bed attached to the liver. Tumor Armonk, NY, USA). The survival time was calculated from
located only the free serosa side of gallbladder was classified as the date of surgery to the date of death or the last follow-up.
peritoneal side gallbladder cancer. If extent of tumor included Disease-free survival was calculated from the date of surgery to
both peritoneal and hepatic side, it was categorized as hepatic the date of recurrence. Survival was analyzed using the Kaplan-
side cancer. Meier method, and variables were compared using the log-rank
To avoid confusion regarding the surgical terms, we used the test. Multivariable regression analysis was performed using
following definitions. Radical cholecystectomy was defined the Cox proportional hazards model to identify independent
as all procedures beyond simple cholecystectomy. Extended prognostic factors for survival. P-values of <0.05 were
cholecystectomy was defined as simple cholecystectomy with considered statistically significant.
LN dissection and hepatic resection of S4b and S5 or gallbladder
bed resection with a 2- to 3-cm margin. Laparoscopic RESULTS
resection was performed if T1 cancer was suspected based
on the patient’s preoperative radiological findings. After General characteristics of patients
cholecystectomy, the specimen was sent for frozen sectioning. The demographic characteristics and perioperative data,
If the tumor invaded perimuscular connective tissue, the including the types of surgical procedures, are shown in Table
procedure was converted to open surgery for extended 1. Among 78 patients with T2 stage gallbladder, 32 (28.2%)

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Table 1. Demographics and perioperative characteristics of Table 2. Clinicopathological characteristics of patients with T2
patients with T2 gallbladder cancer (n = 78) gallbladder cancer (n = 78)

Variable Value Variable Value

Sex, male:female (n) 32:46 Tumor size (mm) 25.0 (3.0–90.0)

Age (yr), median (range) 69 (44–87) Tumor location
CA 19-9 (>37 U/mL) 20 (25.6) Hepatic side 5 (6.4)
Incidental findings 10 (12.8) Peritoneal side 35 (44.9)
Type of surgery Both 31 (39.7)
Chole 28 (35.9) Undetermined 7 (9.0)
Chole + LND 22 (28.2) Tumor location within the gallbladder
Chole + LND + BDR 3 (3.8) Fundus and/or body 58 (74.4)
Chole + LND + HR 18 (23.1) Infundibulum to neck 12 (15.4)
Chole + LND + BDR +HR 6 (7.7) Cystic duct 3 (3.8)
Chole + LND + PPPD 1 (1.3) Diffuse 5 (6.4)
Laparoscopy/open surgery 24 (30.8):54 (69.2) Histology
Morbidities 9 (11.5) Adenocarcinoma 72
Deaths 0 (0) Papillary adenocarcinoma 4
Signet ring cell carcinoma 1
Values are presented as number (%) unless indicated.
Papillary carcinoma 1
Chole, cholecystectomy; LND, lymph node dissection; BDR, bile
duct resection; HR, hepatic resection; PPPD, pylorus preserving Differentiation
pancreaticoduodenectomy. WD 14 (17.9)
MD, PD 58 (74.4)
R1 status 4 (5.1)
were men and 46 (71.8%) were women, and the mean age was Lymphovascular invasion 29 (37.2)
68.3 years (range, 44–87 years). Twenty-eight patients (35.9%) Perineural invasion 24 (30.8)
Lymph node metastasis 20 (25.6)
underwent simple cholecystectomy and 50 patients (64.1%)
AJCC stage
underwent extended cholecystectomy. One patient underwent X 28 (35.9)
pancreaticoduodenectomy because the tumor cells had spread II 30 (38.5)
into the distal bile duct from cystic duct cancer. Twenty- IIIB 19 (24.4)
four patients (30.8%) underwent laparoscopic surgery and 54 IVB 1 (1.3)
patients (69.2%) underwent open surgery. Nine surgery-related Values are presented as median (range), number, or number (%)
complications (11.5%) occurred. Bile leakage was found in 3 WD, well differentiated; MD, moderately differentiated; PD,
patients, delayed gastric emptying in 3 patients, and bleeding in poorly differentiated; AJCC, American Joint Committee on
Cancer.
1 patient. There were no intraoperative deaths.

Histopathological results resection were 64.9% at 3 years and 62.6% at 5 years. The sites
The clinicopathological outcomes are shown in Table 2. The of recurrence or distant metastasis were regional LN metastasis
mean tumor diameter was 28.4 mm (range, 3–90 mm). The in 13 patients, distant LN metastasis in 1 patient, and lung
tumor was located on the peritoneal side in 35 patients, on metastases in 2 patients. Hepatic metastases were found in
the hepatic side in 5 patients, and involved both sides in 31 6 patients (27.2%); liver resection was performed in 3 and
patients. The tumor was located in the fundus and/or body not in the other 3. Eighteen patients died because of disease
of the gallbladder in 58 patients (74.4%), the infundibulum to recurrence (Fig. 1). The overall survival rates of the 78 patients
neck in 12 patients (15.3%), the cystic duct in 3 patients (3.8%), were 70.9% at 3 years and 64.6% at 5 years.
and the entire gallbladder wall in 5 patients (6.4%). The tumor The 5-year disease-free survival rates of patients with and
was classified as well differentiated in 14 patients (17.9%), without LN metastasis were 81.8% and 34.7%, respectively (P =
moderately differentiated in 49 patients (62.8%), and poorly 0.020) (Fig. 1A). Patients who underwent R0 resection (n = 74)
differentiated in 8 patients (10.2%). R0 resection was achieved showed significant better disease-free survival than patients
in 74 patients and R1 resection was achieved in 4 patients. who underwent R1 resection (n = 4) (P = 0.003) (Fig. 1B).
The disease-free survival rate was similar in patients who
Long-term survival according to pathological factors underwent simple cholecystectomy and radical cholecystectomy,
During the follow-up period of 45.4 months, 22 patients with 5-year survival rates of 66.5% and 59.5%, respectively (P =
(28.2%) experienced disease recurrence. The disease-free 0.838) (Fig. 2A). Among 56 patients without LN metastasis (N0
survival rates among the 78 patients who underwent surgical after LN dissection, n = 20) or unknown LN status (Nx due to

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 Annals of Surgical Treatment and Research 2018;94(3):135-141

A B

Fig. 1. (A) The 5-year disease-free survival rates of patients with (N1) and without (N0) lymph node metastasis were 81.8%
and 34.7%, respectively (P = 0.020). (B) Patients who underwent R0 resection (n = 74) showed significant better disease-free
survival than patients who underwent R1 resection (n = 4) (P = 0.003).

Fig. 2. (A) The disease-free survival rate was similar in patients who underwent simple cholecystectomy (simple) and radical
cholecystectomy (radical), with 5-year survival rates of 66.5% and 59.5%, respectively (P = 0.838). (B) Between 56 patients
without lymph node (LN) metastasis (N0 after lymph node dissection, n = 20) or unknown LN status (NX due to no lymph
node dissection, n = 36), the 5-year disease-free survival rates were 81.6%, and 69.8% (P = 0.080) in patients who underwent
LN dissection or not, respectively.

no LN dissection, n = 36), the 5-year disease-free survival rates Disease-free survival was not affected by the tumor location
were 81.6%, and 69.8% (P = 0.080) in patients who underwent in the gallbladder (i.e., fundus, body, infundibulum, and cystic
LN dissection or not, respectively (Fig. 2B). Disease recurrence duct).
was found in 2 patients (10.0%) with LN dissection and in 11
patients (30.5%) without LN dissection. Prognostic factors for disease-free survival and
overall survival
Survival according to tumor location The results of the univariate analyses of the clinicopatho­
In a subgroup analysis according to tumor location, patients logical characteristics of pT2 gallbladder cancer are shown in
with tumors located on the hepatic side (n = 36, hepatic side Table 3. Univariate analyses showed that R1 resection, absence
+ both hepatic and peritoneal side) had a higherer recurrence of LN metastasis (P = 0.020), lymphovascular invasion, and
rate than patients with tumors located on the peritoneal side tumor stage were significant prognostic factors for poor disease-
only (n = 35) (P = 0.043) (Fig. 3A). However, in patients with free and overall survival. In addition, the multivariable analyses
tumors on the hepatic side, liver resection did not affect long- showed that R1 resection and LN metastasis were significant
term survival (P = 0.846) (Fig. 3B). and independent prognostic factors for poor disease-free and

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 Tae Jun Park, et al: Surgical extent of T2 gallbladder cancer

Fig. 3. Analysis according to the tumor location. (A) Patients with tumors located on the hepatic side (n = 36, hepatic side +
both hepatic and peritoneal side) had a higherer recurrence rate than patients with tumors located on the peritoneal side only (n
= 35) (P = 0.043). (B) In patients with tumors on the hepatic side, liver resection did not affect long-term survival (P = 0.846).

Table 3. Univariate and multivariate analysis of prognostic factors for 5-year overall survival of patients with T2 gallbladder
cancer (n = 78)
Univariate analysis Multivariate analysis
Variable
% P-value RR Exp (95% CI) P-value

Age (yr) 0.943

≥65 (n = 57) 69.9
<65 (n = 21) 71.2
Sex 0.400
Male (n = 32) 72.9
Female (n = 46) 67.8
CA 19-9 (U/mL) 0.447
≥37 (n = 20) 69.8
<37 (n = 50) 77.5
Operation type 0.691
Simple (n = 28) 68.1
Radical (n = 50) 72.5
Resection status 0.001
R0 (n = 74) 77.2 1.000 Reference
R1 (n = 4) 0 39.170 2.471–67.603 0.009
Differentiation 0.387
WD (n = 14) 60.9
MD/PD (n = 58) 68.3
LN metastasis 0.020
No (n = 30) 48.5 1.000 Reference
Yes (n = 20) 76.4 9.456 1.098–87.445 0.041
Lymphovascular invasion 0.003
No (n = 40) 49.5
Yes (n = 29) 88.9
Perineural invasion 0.035
No (n = 42) 48.5
Yes (n = 24) 80.0
AJCC stage 0.049
II (n = 30) 76.4
IIIb/IVb (n = 20) 51.0

RR, relative risk; CI, confidence interval; WD, well differentiated; MD, moderately differentiated; PD, poorly differentiated; LN, lymph
node; AJCC, American Joint Committee on Cancer.

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 Annals of Surgical Treatment and Research 2018;94(3):135-141

overall survival (Table 3). results show that LN dissection is necessary in patients with T2
gallbladder cancer.
DISCUSSION Some recent studies have suggested that tumor location on
the hepatic side of the gallbladder is a significant prognostic
Because of its vague symptoms and aggressive clinical factor for poor survival [22,23]. Microscopic liver metastasis
behavior, most gallbladder cancer is at an advanced stage at is frequently detected in patients with T2 gallbladder cancer,
diagnosis. Therefore, the prognosis of gallbladder cancer is poor, and residual cancer cells were more frequently detected in the
and long-term survival is only realistic if it is detected early and gallbladder bed adjacent to the liver parenchyma after simple
complete surgical resection is performed [9]. The 5-year survival cholecystectomy in patients with tumors on the hepatic side
rate of T2 gallbladder cancer varied considerably in earlier [22,24]. Similar to our study, Shindoh et al. [22] reported that
studies, ranging from 29.3% to 78.3% [3,4,10,11]. In our study, the tumors located on the hepatic were associated with poor
5-year survival rate was 62.6%, consistent with that of earlier prognosis in patients with T2 cancer, but not in patients with
reports. T1 or T3 cancer. The need for hepatic resection of T2 gallbladder
Several clinicopathological factors were reported to affect cancer is still controversial [21]. Hepatic S4b and S5 resection
the prognosis of gallbladder cancer, including LN metastasis, or gallbladder bed resection with a 2- to 3-cm margin have
lymphatic invasion, vascular invasion, perineural invasion, been performed based on the fact that most of the cholecystic
differentiation grade, tumor-node-metastasis stage, and residual vein drains through segments 4 and 5 [25]. However, invasion
tumor status [4,10,12,13]. The results of the univariate analyses of gallbladder cancer into the gallbladder vein was reported
in our study yielded similar prognostic factors. However, only in just 0%–10% of all cases [26,27]. Furthermore, the most
R0 resection and LN metastasis were significant prognostic common event is direct invasion of the tumor into adjacent
factors for overall survival in the multivariable analysis. liver segments 4 and 5, which is classified as pT3. There was no
Extended cholecystectomy, including LN dissection and evidence of intrahepatic intravascular invasion in cases of gross
hepatic resection, was reported as a significant surgery- liver invasion of gallbladder cancer in an early study of the
related prognostic factor. In patients who undergo simple modes of spread, and vascular invasion is a relatively rare mode
cholecystectomy alone, the postoperative survival is dismal, of spread of gallbladder cancer [26]. Therefore, tumor location
with 5-year survival rates of 17%–40% reported [5,14,15]. Shirai on the hepatic side is clearly associated with poor prognosis.
et al. [5] conducted a retrospective analysis of 48 patients and Nevertheless, the benefit of hepatic resection of tumors located
found that radical resection of pT2 gallbladder cancer improved on the hepatic side remains unclear. Our study showed that
the 5-year survival rate from 40% to 90%. On the basis of these liver resection in patients located on the hepatic side did not
studies, the AJCC Cancer Staging Manual, 7th edition, and the affect long-term survival, similar to the study by Shindoh et
recently published guidelines of the Korean Association of HBP al. [22]. However, Lee et al. [23] reported that liver resection
Surgery recommend extended cholecystectomy with regional had a beneficial effect on long-term survival in patients with
LN dissection and en bloc hepatic resection in patients with T2 cancer located on the hepatic side but not in patients with
T2 gallbladder cancer. However, extended cholecystectomy was tumors located on the peritoneal side.
performed in just 13.4%–45.8% of patients with T2 gallbladder In conclusion, R0 resection and LN dissection are an
cancer in clinical practice [10,16,17]. Despite this inconsistency, appropriate curative surgical strategy in patients with T2
some studies have reported a favorable survival rate after gallbladder cancer. Although tumors located on the hepatic side
simple cholecystectomy [3], and we found a high 5-year overall show worse prognosis than tumors located on the peritoneal
survival rate of 66.5% in patients who underwent simple side, the need for hepatic resection should be evaluated in
cholecystectomy. Although survival was not significantly additional studies.
different (P = 0.080) between N0 and Nx patients (n = 56),
patients who underwent LN dissection showed favorable CONFLICTS OF INTEREST
survival relative to patients who did not undergo LN dissection
(Fig. 2B). The rate of LN metastasis in T2 gallbladder cancer was No potential conflict of interest relevant to this article was
reported to be as high as 63.4% [14,18-21], and considering LN reported.
metastasis is an independent significant prognostic factor, LN
dissection should be performed to achieve R0 resection if there
are no specific contraindications to this procedure. The present
study included 28 patients (35.9%) who underwent simple
cholecystectomy, and most of them were treated before the
policy for routine LN dissection was established. Therefore, our

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 Tae Jun Park, et al: Surgical extent of T2 gallbladder cancer

REFERENCES

1. Yamaguchi K, Chijiiwa K, Saiki S, Nishihara 11. Suzuki S, Yokoi Y, Kurachi K, Inaba K, Ota Surg 2011;148:e77-84.
K, Takashima M, Kawakami K, et al. Re­ S, Azuma M, et al. Appraisal of surgical 20. Goetze TO, Paolucci V. Benefits of reo­
trospective analysis of 70 operations for treatment for pT2 gallbladder carcinomas. peration of T2 and more advanced in­
gallbladder carcinoma. Br J Surg 1997; World J Surg 2004;28:160-5. cidental gallbladder carcinoma: analysis
84:200-4. 12. Chijiiwa K, Noshiro H, Nakano K, Okido of the German registry. Ann Surg 2008;
2. Ogura Y, Mizumoto R, Isaji S, Kusuda T, M, Sugitani A, Yamaguchi K, et al. Role 247:104-8.
Matsuda S, Tabata M. Radical operations of surgery for gallbladder carcinoma 21. Yokomizo H, Yamane T, Hirata T, Hifumi
for carcinoma of the gallbladder: present with special reference to lymph node M, Kawaguchi T, Fukuda S. Surgical
status in Japan. World J Surg 1991;15:337- metastasis and stage using western and treatment of pT2 gallbladder carcinoma:
43. Japanese classification systems. World J a reevaluation of the therapeutic effect
3. Kang CM, Lee WJ, Choi GH, Kim JY, Kim Surg 2000;24:1271-6. of hepatectomy and extrahepatic bile
KS, Choi JS, et al. Does "clinical" R0 have 13. Wakai T, Shirai Y, Yokoyama N, Ajioka Y, duct resection based on the long-term
validity in the choice of simple chole­ Watanabe H, Hatakeyama K. Depth of outcome. Ann Surg Oncol 2007;14:1366-
cystectomy for gallbladder carcinoma? J subserosal invasion predicts long-term 73.
Gastrointest Surg 2007;11:1309-16. survival after resection in patients with 22. Shindoh J, de Aretxabala X, Aloia TA, Roa
4. Kohya N, Miyazaki K. Hepatectomy of T2 gallbladder carcinoma. Ann Surg Oncol JC, Roa I, Zimmitti G, et al. Tumor location
segment 4a and 5 combined with extra- 2003;10:447-54. is a strong predictor of tumor progression
hepatic bile duct resection for T2 and 14. Chijiiwa K, Nakano K, Ueda J, Noshiro and survival in T2 gallbladder cancer: an
T3 gallbladder carcinoma. J Surg Oncol H, Nagai E, Yamaguchi K, et al. Surgical international multicenter study. Ann Surg
2008;97:498-502. treatment of patients with T2 gallbladder 2015;261:733-9.
5. Shirai Y, Yoshida K, Tsukada K, Muto T. carcinoma invading the subserosal layer. J 23. Lee H, Choi DW, Park JY, Youn S, Kwon
Inapparent carcinoma of the gallbladder. Am Coll Surg 2001;192:600-7. W, Heo JS, et al. Surgical strategy for T2
An appraisal of a radical second operation 15. Benoist S, Panis Y, Fagniez PL. Long- gallbladder cancer according to tumor
after simple cholecystectomy. Ann Surg term results after curative resection for location. Ann Surg Oncol 2015;22:2779-
1992;215:326-31. carcinoma of the gallbladder. French 86.
6. Lee SE, Jang JY, Lim CS, Kang MJ, Kim University Association for Surgical 24. Endo I, Shimada H, Takimoto A, Fujii Y,
SW. Systematic review on the surgical Research. Am J Surg 1998;175:118-22. Miura Y, Sugita M, et al. Microscopic liver
treatment for T1 gallbladder cancer. World 16. Mayo SC, Shore AD, Nathan H, Edil B, metastasis: prognostic factor for patients
J Gastroenterol 2011;17:174-80. Wolfgang CL, Hirose K, et al. National with pT2 gallbladder carcinoma. World J
7. Miyakawa S, Ishihara S, Horiguchi A, trends in the management and survival Surg 2004;28:692-6.
Takada T, Miyazaki M, Nagakawa T. Biliary of surgically managed gallbladder 25. Yoshimitsu K, Honda H, K aneko K,
tract cancer treatment: 5,584 results from adeno c a rc i nom a o ver 15 ye a rs: a Kuroiwa T, Irie H, Chijiiwa K, et al.
the Biliary Tract Cancer Statistics Registry population-based analysis. J Gastrointest Anatomy and clinical importance of
from 1998 to 2004 in Japan. J Hepatobiliary Surg 2010;14:1578-91. cholecystic venous drainage: helical CT
Pancreat Surg 2009;16:1-7. 17. Kim DH, Kim SH, Choi GH, Kang CM, Kim observations during injection of contrast
8. Chan SY, Poon RT, Lo CM, Ng KK, Fan KS, Choi JS, et al. Role of cholecystectomy medium into the cholecystic artery. AJR
ST. Management of carcinoma of the and lymph node dissection in patients Am J Roentgenol 1997;169:505-10.
gallbladder: a single-institution experience with T2 gallbladder cancer. World J Surg 26. Fahim RB, McDonald JR, Richards JC,
in 16 years. J Surg Oncol 2008;97:156-64. 2013;37:2635-40. Ferris DO. Carcinoma of the gallbladder:
9. Sikora SS, Singh RK. Surgical strategies in 18. Shimada H, Endo I, Togo S, Nakano a study of its modes of spread. Ann Surg
patients with gallbladder cancer: nihilism A, Izumi T, Nakagawara G. The role of 1962;156:114-24.
to optimism. J Surg Oncol 2006;93:670-81. lymph node dissection in the treatment 27. Sons HU, Borchard F, Joel BS. Carcinoma
10. Choi SB, Han HJ, Kim CY, Kim WB, Song of gallbladder carcinoma. Cancer 1997;79: of the gallbladder: autopsy findings in
TJ, Suh SO, et al. Surgical outcomes and 892-9. 287 cases and review of the literature. J
prognostic factors for T2 gallbladder 19. Isambert M, Leux C, Métairie S, Paineau J. Surg Oncol 1985;28:199-206.
cancer following surgical resection. J Incidentally-discovered gallbladder cancer:
Gastrointest Surg 2010;14:668-78. When, why and which reoperation? J Visc

Annals of Surgical Treatment and Research 141