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ORIGINAL CONTRIBUTION

En Bloc Pancreaticoduodenectomy and Right


Colectomy in the Treatment of Locally Advanced
Colon Cancer
Ji Zhang, M.D. Jia-hua Leng, M.D. Hong-gang Qian, M.D.
Hui Qiu, M.D. Jian-hui Wu, M.D. Bo-nan Liu, M.D.
Cheng-peng Li, M.D. Chun-yi Hao, M.D.
Key Laboratory of Carcinogenesis and Translational Research, Ministry of Education, Department of Hepato-Pancreatic
Biliary Surgery, Beijing Cancer Hospital, Peking University Cancer Hospital & Institute, Beijing, China

BACKGROUD: Carcinoma of the right colon invading death occurred in 2 patients. The median hospital stay
the pancreas or duodenum is rare. Evidence of the was 22.5 days (range, 17.057.0 days). Inflammatory
indication, operative morbidity, and survival of en bloc adhesion was confirmed by pathologic examination in
pancreaticoduodenectomy and right colectomy for right only 1 patient. Eight patients (57%) did not have lymph
colon cancer invading adjacent organs is limited. node metastasis. The median follow-up time was 21
OBJECTIVE: The goal of this study was to investigate the months (range, 4276 months). Ten patients were alive
feasibility, safety, indication, and long-term results of at the time of their last scheduled follow-up. The overall
en bloc pancreaticoduodenectomy and right colectomy survival rates were 72% at 1 year and 60% at 2 years. No
in the treatment of locally advanced right-sided colon patient was lost to follow-up. Three patients developed
cancer. tumor recurrence. The outcomes are no worse than those
of the stage-matched patients without adjacent organ
DESIGN: This was a retrospective analysis of all inpatients involvement and are much better than those of the stage-
undergoing en bloc pancreaticoduodenectomy and right matched patients who underwent bypass surgery and
colectomy. Detailed data of these patients were assessed chemotherapy.
by a thorough review of medical charts.
LIMITATIONS: The number of patients in current studies
SETTINGS: The study was conducted using a hospital is limited.
database.
CONCLUSIONS: En bloc pancreaticoduodenectomy
PATIENTS: Fourteen patients who underwent en bloc and right colectomy can be performed safely with an
pancreaticoduodenectomy and right colectomy from acceptable morbidity and mortality rate in selected
January 1989 through December 2011 were included in patients with locally advanced right-side colon cancer.
the study. The long-term results are promising.
MAIN OUTCOME MEASURES: In-hospital complications,
mortality, and survival were the primary outcomes
measured. KEY WORDS: En bloc resection;
RESULTS: Major postoperative complications included Pancreaticoduodenectomy; Right-sided colon cancer.
delayed gastric empting (n = 7), class B pancreatic

L
fistula (n = 3), and bile leakage (n = 1). Postoperative ocally advanced colorectal tumors, that is, tumors
that infiltrate or adhere to adjacent organs without
distant metastases, represent 5.2% to 23.6% of all
Financial Disclosure: None reported. colorectal cancers at the time of presentation.17 Extended
or multivisceral resection to achieve R0 resection is the
Correspondence: Chun-yi Hao, M.D., No. 52 Fu-Cheng-Lu St, Beijing
100142, China. E-mail: drhaochunyi@163.com
treatment of choice. Right colon cancer invading adjacent
organs is rare, and even fewer series have described
Dis Colon Rectum 2013; 56: 874880 colon cancer with duodenal and/or pancreatic invasions.
DOI: 10.1097/DCR.0b013e3182941704 Because preoperative diagnosis is difficult, the situation
The ASCRS 2013 is often identified for the first time at surgery when the
874 Diseases of the Colon & Rectum Volume 56: 7 (2013)
Diseases of the Colon & Rectum Volume 56: 7 (2013) 875

patient and surgeon might not be fully prepared for a Duodenal or pancreatic invasion was determined after lib-
surgical resection of such complexity. It may require eration of natural adherences to the colon. Once the resect-
complex and difficult surgical resolution that involves en ability was established, an RC was performed following the
bloc pancreaticoduodenectomy (PD) plus right colectomy standard technique. A stapled end-to-side ileocolic anas-
(RC),814 which pose surgical challenges. This may explain tomosis was routinely performed after the specimen was
the scarce information about this issue in the literature. removed. In all of the patients, PD was undertaken with
Most reports of this condition are solitary cases that are an antrectomy, and reconstruction was carried out with
included in large analyses of extended colonic resections an end-to-side pancreaticogastrostomy or pancreaticojeju-
at all sites.6,1519 Some studies enrolled patients who nostomy. A pancreatic duct stent was usually used in the
underwent RC plus partial duodenectomy. As a result, pancreaticojejunostomy. If the portal vein and/or superior
the evidence on the indication, operative morbidity, and mesenteric vein was involved, resection of the mesenteri-
survival of en bloc PD for right colon cancer invading coportal vein and an end-to-end anastomosis was carried
adjacent organs is limited. The present retrospective out, as reported previously.20 After completion of the re-
study reviewed 14 cases of en bloc PD and RC for locally section and reconstruction, rubber drains were placed near
advanced right colon cancer. the biliary and pancreatic anastomosis. The drains were
removed progressively from postoperative day 7. Paren-
teral antibiotics and octreotide acetate were administered
MATERIALS AND METHODS to all of the patients prophylactically. When the drain fluid
The study protocol was approved by the ethics committee turned cloudy with sediment before the abdominal drain
of the Beijing Cancer Hospital. We identified 531 patients was removed, a low-speed intermittent irrigation was
with primary right-sided colon cancer who underwent added until the drain fluid returned clear. No attempt to
radical RC with or without multivisceral resection at the separate the involved structures from the tumor was made
Beijing Cancer Hospital between January 1989 and De- during the operation. Finger fracture of the adhesions was
cember 2011 from a prospectively maintained operative avoided. The staging process was based on the TNM clas-
database and analyzed their records. Among them, 14 pa- sification proposed by the American Joint Committee of
tients underwent en bloc PD and RC because of direct in- Cancer (AJCC).21
volvement of the duodenum and/or pancreas wherein the A postoperative pancreatic fistula was defined accord-
cases were not suitable for a lesser procedure. ing to the International Study Group on Pancreatic Fistula
Computed tomography (CT) to determine local tu- Definition.22 Hence, a postoperative pancreatic fistula was
mor infiltration was routinely performed. Preoperative drained via an operatively placed drain (or a subsequently
colonoscopy and histopathological confirmation of the placed percutaneous drain) of any measurable volume of
diagnosis were performed in all of the patients. The pre- drain fluid on or after postoperative day 3 with an amylase
operative CEA levels were routinely tested in 12 patients. content >3 times the upper normal serum value. Delayed
Indications for surgery included primary lesions with gastric emptying was defined according to the consensus
or without direct extension to adjacent organs including definition of delayed gastric emptying after pancreatic
the pancreas and/or duodenum, as determined by preop- surgery suggested by the International Study Group of
erative imaging assessment, which could be radically re- Pancreatic Surgery.23 Intraabdominal abscess was defined
sected. The absence of medical comorbidities precluded as a pocket of infected fluid and pus located inside the ab-
the operation. PD combined with RC should only be con- dominal cavity.
sidered when there is no other method to achieve com- All of the patients were examined during the first 2
plete resection, and the surgical risk is acceptable. Patients postoperative years at 3-month intervals, during the third
with distant metastasis, high operative risk, or secondary to fifth years at 6-month intervals, and at least annually
involvement of the duodenum and/or pancreas rather thereafter. The patients were followed up according to a
than direct spread were excluded. Patients with secondary standard protocol, including physical examination, CEA
or recurrent tumors were not considered. Patients with lo- measurement, chest radiography, and abdominal ultra-
cal duodenal involvement that could be radically resected sound or CT, and then the patients were followed-up via
by partial duodenectomy were also excluded. annual colonoscopy exams at outpatient clinics.24
A CattellBraasch maneuver was initially performed. According to our search results, 47 stage-matched
An extended Kocher maneuver was then performed to fully patients with right-sided colon cancer without adjacent
mobilize the duodenum with an effort to palpate a clear organ involvement underwent radical surgery, whereas
plane between any tumor and the pulsation of the superior 7 stage-matched patients with right-sided colon cancer
mesenteric artery. The resectability of the tumor was eval- underwent bypass surgery and chemotherapy during the
uated after complete mobilization of the right colon and same period. Patient records were analyzed for outcome
duodenum by means of an extended Kocher maneuver. comparison.
876 ZHANG ET AL: PANCREATICODUODENECTOMY FOR COLON CANCER

TABLE 1. Patient characteristics


Patient Age, y Sex Site of colon cancer Comorbidity Preoperative CEA level, ng/mL
A 56 F HF Hypertension 2.68
B 62 F HF - 6.01
C 46 M HF Hypertension 13.43
D 76 F HF Chronic hepatitis 1.64
E 39 M HF - 59.16
F 69 M HF Anemia 4.60
G 45 F HF - 7.65
H 47 M ASC - 5.04
I 46 M HF - 4.64
J 48 M HF Diabetes mellitus NA
K 54 M HF - 3.71
L 48 F ASC - NA
M 58 M HF - 5.21
N 59 F ASC - 188.91
ASC = ascending colon; F = female; HF: hepatic flexure; M = male; NA = not applicable.

RESULTS abdominal abscess formation. No patient had an ileocolic,


gastrojejunal, or jejunojejunal anastomotic leak. The me-
Fourteen patients, including 6 women and 8 men, with dian hospital stay was 22.5 days (range, 17.057.0 days).
advanced right-sided colon cancer involving the pancreas This was much longer than that reported by Western au-
or duodenum underwent en bloc PD and RC at our hos- thors because of the Chinese social insurance system. Nine
pital between 1989 and 2011. The median age was 51 years patients received adjuvant chemotherapy, 6 with modi-
(range, 3976 years). Sites of the primary cancer were the fied FOLFOX 6; 1 with FOLFOX 4; 1 with folinic acid,
ascending colon (n = 3) and hepatic flexure (n = 11). The fluorouracil, plus irinotecan hydrochloride; and 1 with
demographics and tumor location are outlined in Table1. capecitabine plus oxaliplatin treatment. The treatment,
Eight patients had anemia and 6 had abdominal pain perioperative course, and outcome are listed in Table2.
at presentation. Other prominent symptoms were abdom- The median follow-up time was 21 months (range,
inal distension (n = 4), palpable fixed mass (n = 4), altera- 4276 months). During this period, 2 patients died from
tion of bowel habits (n = 4), history of significant weight recurrence. Ten patients were alive by their last scheduled
loss (n = 4), and vomiting (n = 3). One patient (patient F) follow-up. No patient was lost to follow-up. Three patients
underwent laparotomy and ileocolostomy followed by 1 (21%) developed recurrence. Among them, 2 patients (pa-
cycle of chemotherapy (regimen unknown) at a local hos- tients B and D) died from a recurrence and 1 remained
pital. The patient was recommended to our hospital for alive. Three patients survived >5 years after surgery, in-
further treatment. Another patient (patient G) received 6 cluding 1 patient surviving >23 years. The overall survival
cycles of modified folinic acid, fluorouracil, plus oxalipla- rates were 72% at 1 year and 60% at 2 years. During the
tin (FOLFOX) treatment at a local hospital after the diag- same period, 47 stage-matched (T4bNxM0) patients with
nosis had been established and was then transferred to our right-sided colon cancer without adjacent organ involve-
hospital. ment underwent radical surgery. The overall survival rates
The median operative time was 360 minutes (range, were 76% at 1 year, 58% at 2 years, and 26% at 5 years.
270600 minutes), and the median blood loss was 400mL Seven stage-matched patients with right-sided colon can-
(range, 200800mL). One patient (patient N) had associ- cer underwent bypass surgery and chemotherapy. Only 1
ated infiltration of the right kidney and had an en bloc ne- patient was alive by the last scheduled follow-up. The me-
phrectomy. Major postoperative complications occurred dium survival time was 5 months.
in 9 patients (64%) with delayed gastric empting being Direct invasion to the duodenum and/or pancreas
the most common complication (4 grade A and 3 grade head was confirmed histologically in 13 patients. Among
B). Eight patients developed pancreatic fistulas (5 grade A them, 3 patients developed fistula formation between their
and 3 grade B) according to the International Study Group colon and duodenum. Only 1 patient had inflammatory
on Pancreatic Fistula Definition.22 Two patients devel- adhesions. Pathologic examination demonstrated poorly
oped intra-abdominal abscesses. Both of them underwent differentiated adenocarcinoma (n = 5), moderately
pancreaticogastrostomy. Pancreatic fistula was the cause differentiated adenocarcinoma (n = 7), well-differentiated
of the abscesses. They were all successfully treated dur- adenocarcinoma (n = 1), and mucinous adenocarcinoma
ing their primary hospital stay. Two patients (14%) died with signet-ring cell carcinoma (n = 1). All of the tumors
postoperatively, 1 with pneumonia and septic shock and had clear resection margins (R0). According to the AJCC
another with delayed post-PD arterial bleeding after intra- cancer staging system,21 8 patients (57%) were staged
Diseases of the Colon & Rectum Volume 56: 7 (2013) 877

TABLE 2. Treatments and outcomes


Perioperative course
Blood
transfusion, Operative
Patient Operation EBL, mL units time, min LOS, d Complications Chemotherapy Survival, mo Status Cause of death
A PD+RC 300 2 390 30 PF(A), DGE - 63 Alive
B PD+RC 400 0 280 36 DGE, BF FOLFOX4 12 Dead Recurrence
C PD+RC 700 2 360 25 PF(A) FOLFOX6 60 Alive
D PD+RC 300 4 270 17 PF(A), DGE mFOLFOX6 10 Dead Recurrence
E PD+RC 500 0 360 23 PF(A) mFOLFOX6 48 Alive
F PD+RC 800 4 600 IAA - Dead PC
G PD+RC 300 1 325 18 - FOLFIRI 24 Alive
H PD+RC 400 0 410 PF(A), IAA - Dead PC
I PD+RC+PH 800 2 360 19 DGE mFOLFOX6 49 Alive
J PD+RC 500 4 315 22 PF(B), DGE, IAA mFOLFOX6 4 Alive
K PD+RC 200 6 420 22 PF(B), DGE mFOLFOX6 12 Alive
L PD+RC NA NA NA NA - NA 276 Alive
M PD+RC 400 6 500 24 DGE XELOX 18 Alive
N PD+RC+RN 300 0 420 21 - mFOLFOX6 13 Alive
BF = biliary fistula; DGE = delayed gastric emptying; EBL = estimated blood loss; FOLFIRI = folinic acid, fluorouracil, plus irinotecan hydrochloride; FOLFOX = folinic acid,
fluorouracil, plus oxaliplatin; IAA = intra-abdominal abscess; LOS = length of stay; m = modified; NA = not applicable; PC = postoperative complications; PD = pancreatico-
duodenectomy; PF = pancreatic fistula; PH = partial hepatectomy; RC = right colectomy; RN = right nephrectomy; XELOX = capecitabine plus oxaliplatin.

as N0, 2 as N1a, 1 as N1b, 2 as N2a, and 1 as N2b. The who underwent en bloc resection of the tumor and part
pathologic characteristics are outlined in Table3. of the duodenal wall with a negative margin, because the
complexity, morbidity, and mortality are incomparable
DISCUSSION between local resection of the duodenal wall and PD.
The feasibility of en bloc PD and RC in the treatment
Carcinoma of the right colon (CRC) invading the pan- of locally advanced CRC is controversial. CRC that
creas or duodenum is rare.2528 Only a few series have de- invades the adjacent pancreas and/or duodenum is often
scribed adjacent-organ resection.911,14,2531 In our study, 14 considered to be unresectable. One of the reasons is that
patients (2.6%) with advanced right-sided colon cancer such locally infiltrative tumors are generally believed to
involving the pancreas and/or duodenum who underwent be highly malignant. Actually, although all of the tumors
en bloc PD and RC were recognized from the 531 patients of this category are staged T4b, according to the AJCC
who underwent curative RC between 1989 and 2011. Pa- staging system, 21 The N staging of the cancer may not be
tients who had metastatic or recurrent lesions affecting the that advanced. According to the reports, 25% to 60% of
pancreas and/or duodenum were excluded. We also did CRCs that invade the adjacent pancreas or duodenum do
not include those patients with local duodenal infiltration not have lymph node metastasis.9,10,14,25,26 In our series, 8

TABLE 3. Pathologic findings


Staging Pathologic finding
Patient Site of adhesion T N M Tumor Margin Adhesion
A Du+Pa+Kid 4b 0 0 Moderately differentiated adenocarcinoma Negative Ca
B Du+Pa 4b 1a 0 Moderately differentiated adenocarcinoma with mucinous adenocarcinoma Negative Ca
C Du 4b 0 0 Moderately differentiated adenocarcinoma Negative Ca
D Du 4b 1b 0 Poorly differentiated neuroendocrine tumor Negative Ca
E Pa 4a 0 0 Mucinous adenocarcinoma with signet-ring carcinoma Negative In
F Pa 4b 2a 0 Moderately to poorly differentiated adenocarcinoma Negative Ca
G Du+Pa 4b 0 0 Moderately differentiated adenocarcinoma with mucinous adenocarcinoma Negative Ca
H Du+Pa 4b 0 0 Well-differentiated adenocarcinoma Negative Ca
I Pa+GB+Liv 4b 2a 0 Moderately differentiated adenocarcinoma Negative Ca
J Du+Liv 4b 0 0 Moderately differentiated adenocarcinoma Negative Ca
K Du+Pa 4b 0 0 Poorly differentiated adenocarcinoma Negative Ca
L Du 4b 0 0 Moderately differentiated adenocarcinoma Negative Ca
M Du 4b 1a 0 Moderately differentiated adenocarcinoma Negative Ca
N Du+Kid 4b 2b 0 Moderately differentiated adenocarcinoma with mucinous adenocarcinoma Negative Ca
Du = duodenum; Pa = pancreas; Kid = kidney; GB = gallbladder; Liv = liver; Ca = carcinomatous; In = inflammatory.
878 ZHANG ET AL: PANCREATICODUODENECTOMY FOR COLON CANCER

patients (57%) were staged as T4bN0M0 pathologically. we recommend for this procedure include the following:
These patients should be staged as IIC. Radical resection 1) no distant metastasis, 2) R0 resection being possible on
is possible for most of the patients at this stage. Another the basis of the preoperative examination, 3) the patients
reason is that en bloc PD plus RC poses a surgical condition being good enough to accept radical multivis-
challenge because of its complexity and the significant ceral resection, and 4) the surgical team being experienced
morbidity and mortality rates. Most surgeons believe enough to safely perform en bloc PD and RC. High-risk
that the risks of such a radical resection may outweigh patients (ie, elderly, malnourished patients or patients
the benefits. With the development of surgical skills with long-term anemia or severe comorbid disease) may
and perioperative care, postoperative mortality and not be good candidates for this procedure. Preoperative
morbidity rates of PD have recently fallen to acceptable evaluations (performance status and functional test of the
levels.3237 Many reports have revealed that en bloc PD vital organs) are highly recommended.
plus RC could be performed safely and produce good The mortality rate in our study was relatively higher
results.911,14,38,39 In our study, 8 patients developed than in similar studies. The main reason is that we were
pancreatic fistulas (5 grade A and 3 grade B), according not as experienced in managing post-PD complications
to the International Study Group on Pancreatic Fistula when 20 PDs were performed every year. The mortality
Definition,22 7 developed delayed gastric emptying, and rate dropped significantly in the past 5 years when 70 to
2 developed intraabdominal abscesses. Both of the 2 80 PDs were performed every year. Otherwise, most of
patients who developed abdominal abscesses underwent the correlating studies enrolled patients who underwent
pancreaticogastrostomy. Pancreatic fistula was the partial resection of the duodenal wall rather than PD,
cause of the abscesses. Most of the complications were which makes it impossible to compare certain parameters
successfully treated. Two patients (14%) died in the 30- between different studies.9,10,14,26,27,29 The limitation of the
day postoperative duration. When the PD volume in number of patients in current studies is another reason.
our hospital reached 70 per year, no postoperative death An extra postoperative death can alter the mortality rate.
happened in patients who underwent PD and RC. We Study on a larger scale is needed to provide more reliable
believe that postoperative mortality and morbidity rates results.
of PD and RC are acceptable in an experienced team. According to previous reports, the prognosis of pa-
No preoperative examination is reliable in distin- tients with CRC who accepted en bloc PD and RC is prom-
guishing between carcinomatous or inflammatory adhe- ising.10,14,25,30,41 In our series, 10 patients (71.4%) were still
sions. CT scan can only show the intimate relationship alive by their last scheduled follow-up. The overall sur-
between the tumor and adjacent structures. Barium en- vival rates were 72% at 1 year and 60% at 2 years. The
ema and duodenoscopy may identify some of the duo- outcomes are no worse than those of the stage-matched
denocolic fistulas. However, negative findings cannot patients without adjacent organ involvement. However, of
rule out malignant adhesions. In our series, all of the pa- the 7 stage-matched patients with right-sided colon cancer
tients accepted CT scans preoperatively. However, a CT who underwent bypass surgery and chemotherapy, only
scan can only demonstrate the thickness of the colonic 1 patient was alive by the last scheduled follow-up. The
wall and the close relationship between the tumor and medium survival was 5 months. Because the number of
adjacent duodenum and/or pancreas head. Three pa- patients is limited, definite conclusion on the basis of sta-
tients developed duodenocolic fistulas. One fistula was tistic analysis could not be drawn. Saiura et al25 reported
found by barium enema. The rest were revealed by post- long-term survival in 12 patients with advanced colon
operative pathologic examination. Even during surgical cancer after en bloc PD and RC. Palliative therapy could
exploration, it is still difficult to distinguish malignant not produce a comparable prognosis.10,39
adhesions from inflammatory adhesions.8,24,40 It is widely Three (25%) of 12 patients, not including those who
accepted that all adhesions between the adenocarcinoma died postoperatively, had recurrence. The recurrence rate
and neighboring organs should be assumed to be ma- in our study was relatively low compared with that in
lignant. When a right-sided colon cancer is staged T4b- most of the previous studies.10,14,17,2528,30,40,41 We believe
NxM0, as long as the patient is an appropriate candidate that selection bias can significantly influence the final
for a radical operation, en bloc multivisceral resection results. Because the number of patients was limited in
should be performed. all of the relevant studies, it is very difficult to make a
There are no widely accepted indications for en bloc definite conclusion. It has been widely recognized that
PD and RC in the treatment of locally advanced CRC. It staging, especially N staging, is a prominent prognostic
is generally accepted that en bloc multivisceral resection factor affecting survival.1,5,7,17,19 In our study, 8 patients
is appropriate when it can be performed with minimal (57.1%) did not present any compromised lymph nodes
added operative morbidity and mortality and with a re- (N0). Meanwhile, nearly half of the stage T4 CRC patients
alistic chance of long-term survival. The indications that (49.1%; n = 255) in our series did not have lymph node
Diseases of the Colon & Rectum Volume 56: 7 (2013) 879

metastasis. Our findings are consistent with some previous 3. Gall FP, Tonak J, Altendorf A, Kuruz U. Operative tactics and
reports suggesting that some CRCs may behave in a results in extensive operations for colorectal cancer [in Ger-
locally aggressive manner rather than causing lymphatic man]. Langenbecks Arch Chir. 1985;366:445450.
or hematogenous spread.9,10,14,25,26 En bloc resection can 4. Pittam MR, Thornton H, Ellis H. Survival after extended resec-
tion for locally advanced carcinomas of the colon and rectum.
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Ann R Coll Surg Engl. 1984;66:8184.
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may not reflect the true situation. First, it is likely that only surgical resection of locally advanced colorectal carcinoma.
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because patients who were rejected from surgical treat- carcinoma adherent to other organs: an efficacious treatment?
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