A prospective multicenter study on selfexpandable metallic stents as a bridge tosurgery for malignant colorectal obstructionin Japan: efficacy and safety in 312 patients
Shuji Saito, Shuntaro Yoshida, Hiroyuki
Isayama, Takeaki Matsuzawa, Toshio
Kuwai, Iruru Maetani, Mamoru
Shimada, Tomonori Yamada, et al.
Surgical Endoscopy
And Other Interventional Techniques
Official Journal of the Society ofAmerican Gastrointestinal andEndoscopic Surgeons (SAGES) andEuropean Association for Endoscopic
Surgery (EAES)ISSN 0930-2794
Volume 30
Number 9
Surg Endosc (2016) 30:3976-3986
DOI 10.1007/s00464-015-4709-5

1 23

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Author's personal copy
Surg Endosc (2016) 30:3976–3986
DOI 10.1007/s00464-015-4709-5

and Other Interventional Techniques

A prospective multicenter study on self-expandable metallic stents
as a bridge to surgery for malignant colorectal obstructionin Japan: efficacy and safety in 312 patients
Shuji Saito1 • Shuntaro Yoshida2 • Hiroyuki Isayama3 • Takeaki Matsuzawa4 •Toshio Kuwai5 • Iruru Maetani6 • Mamoru Shimada7 • Tomonori Yamada8 •Masafumi Tomita9 • Koichi Koizumi10 • Nobuto Hirata11 • Hideki Kanazawa12 •Toshiyuki Enomoto13 • Hitoshi Sekido14 • Yoshihisa Saida13
Received: 17 April 2015 / Accepted: 24 November 2015 / Published online: 18 December 2015
Ó Springer Science+Business Media New York 2015

Abstract
Background Endoscopic stenting with a self-expandable
metallic stent (SEMS) is a widely accepted procedure formalignant colonic obstruction. The Colonic Stent Safe
Procedure Research Group conducted the present
prospective feasibility study.
Methods Our objectives were to estimate the safety andfeasibility of SEMS placement as a bridge to surgery (BTS)
for malignant colorectal obstruction. We conducted aprospective, observational, single-arm, multicenter clinical
trial from March 2012 to October 2013. Each patient was

Presented at the SAGES 2015 Annual Meeting, April 15–18, 2015,
Nashville, Tennessee.

treated with an uncovered WallFlex enteral colonic stent.
Patients were followed up until discharge after surgery.
Results A total of 518 consecutive patients were enrolled
in this study. The cohort intended for BTS consisted of 312
patients (61 %), and the stent could be released in 305
patients. Technical and clinical success rates were 98 and
92 %, respectively. Elective surgery was performed in 297
patients, and emergency surgery was performed in eightpatients for the treatment of complications. The overall
preoperative complication rate was 7.2 %. Major complications, including perforation, occurred in 1.6 %, persistentcolonic obstruction occurred in 1.0 %, and stent migration
occurred in 1.3 % patients. The median time from SEMS tosurgery was 16 days. Silent perforations were observed in
1.3 %. Open and laparoscopic surgery was performed in& Shuji Saito
shusaito@jb3.so-net.ne.jp

8

Department of Gastroenterology, Japanese Red Cross Nagoya
Daini Hospital, Nagoya, Japan

1

Division of Surgery, Gastrointestinal Center, Yokohama
Shin-Midori General Hospital, 1726-7 Tokaichiba-cho,
Midori-ku, Yokohama 226-0025, Japan

9

Department of Surgery, Kishiwada Tokushukai Hospital,
Kishiwada, Japan

10

2

Department of Endoscopy and Endoscopic Surgery, Graduate
School of Medicine, University of Tokyo, Tokyo, Japan

Department of Gastroenterology, Tokyo Metropolitan Cancer
and Infectious Disease Center Komagome Hospital, Tokyo,
Japan

3

Department of Gastroenterology, Graduate School of
Medicine, University of Tokyo, Tokyo, Japan

11

Department of Gastroenterology, Kameda Medical Center,
Kamogawa, Japan

4

Department of Digestive Tract and General Surgery, Saitama
Medical Center, Saitama Medical University, Moroyama,
Japan

12

Department of Surgery, National Hospital Organization
Sagamihara Hospital, Sagamihara, Japan

13

5

Department of Gastroenterology, National Hospital
Organization Kure Medical Center and Chugoku Cancer
Center, Kure, Japan

Department of Surgery, Toho University Ohashi Medical
Center, Tokyo, Japan

14

Department of Surgery, National Hospital Organization
Yokohama Medical Center, Yokohama, Japan

6

Division of Gastroenterology and Hepatology, Department ofInternal Medicine, Toho University Ohashi Medical Center,
Tokyo, Japan

7

Department of Surgery, Moriguchi Keijinkai Hospital,
Moriguchi, Japan123

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Surg Endosc (2016) 30:3976–3986

121 and 184 patients, respectively. The tumor could beresected in 297 patients. The primary anastomosis rate was
92 %. The rate of anastomotic leakage was 4 %, and theoverall stoma creation rate was 10 %. The median durationof hospitalization following surgery was 12 days. Overall
postoperative morbidity and mortality rates were 16 and
0.7 %, respectively.
Conclusions This largest, multicenter, prospective study
demonstrates the feasibility of SEMS placement as a BTS
for malignant colorectal obstruction. SEMS serves as a safeand effective BTS with acceptable stoma creation andcomplication rates in patients with acute malignant colonicobstruction.
Keywords Colon and rectal cancer  Intestinal
obstruction  Self-expandable metallic stent  Bridge tosurgery  Multicenter study  Prospective cohort study
Colorectal cancer (CRC) is one of the most common cancers worldwide [1] and the second most common cancer inJapan [2]. At the time of diagnosis, 8–13 % of patients with
CRC present with acute colonic obstruction [3–5]. Conventionally, patients with malignant large bowel obstruction receive emergency surgery. These patients have a pooroutcome as morbidity and postoperative mortality rates arehigher [6], rates of resection and curative resection arelower, and long-term survival is poorer than that in patients
admitted electively [7, 8].
Tejero et al. reported using a self-expandable metallic
stent (SEMS) as a bridge to surgery (BTS) in patients withcolonic obstruction in 1994 [9]. In Japan, in 1996, Saida
et al. [10] reported using SEMS as BTS in patients with
obstructing CRC. Thereafter, a number of studies haveshown that endoscopic stent procedures with SEMS prior
to elective surgery represent relatively simple and safe
alternatives to conventional emergency surgery [11–16].
Preoperative SEMS placement can prevent high-risk
emergency surgery and makes it possible to increase primary anastomosis and decrease stoma creation [17].
Additionally, SEMS gives the physician an opportunity toperform medical resuscitation, optimization of comorbid
disorders, bowel preparation, tumor staging, and preoperative total colonic examination for synchronous proximal
lesions [15, 16]. Although preoperative stent insertion has
such advantages, some stent-related complications, such as
perforation, stent migration, and re-obstruction, have beenreported [18]. Perforation may lead to an increased risk ofperitoneal carcinomatosis and septic and life-threatening
conditions [19–22]. If the perforation rate is low, the risk ofsepsis or peritoneal carcinomatosis is not increased.
Colonic SEMS placement as a bridge to elective surgery isuseful as a standard treatment for malignant colonic

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obstruction because SEMS intervention resulted in morefavorable rates of permanent stoma, primary anastomosis,
and overall complications [23, 24].
To accurately evaluate the advantages and risks of
SEMS, proper stent placement is required. However, todate, SEMS placement studies with quality control information have not been performed. Furthermore, in Japan,
the safety and efficacy of SEMS placement are unclear
because until 2011, colonic SEMS was used only in clinicalresearch [10, 25, 26]. In 2012, this procedure was coveredby the National Health Insurance in Japan. Even underthese circumstances, the Colonic Stent Safe Procedure
Research Group affiliated with the Japan Gastroenterological Endoscopy Society was organized to provide
instructions regarding safety procedures for placement ofcolonic stents [27].
The present study is the largest prospective, multicenter
feasibility study of colonic SEMS as a BTS for acuteobstructive CRC. The aim of this study was to investigate
the outcomes of SEMS as a BTS for obstructive CRC interms of treatment details, short-term adverse events, andproportion of patients with stoma.

Materials and methods
Patients
This prospective, observational, single-arm, multicenter
clinical trial was conducted from March 2012 to October
2013 [28]. The study was registered with the University
Hospital Medical Information Network Clinical Trial
Registry (UMIN000007953). Before study start-up, a Website [27] was launched and the standard methods of SEMS
placement based on previously published data were proclaimed [10, 15, 25]. The Colonic Stent Safe Procedure
Research Group held a workshop to discuss the tips andtricks of SEMS placement. More than 140 doctors participated in the meeting, and several experienced doctors
presented their experience in developing safe SEMS
placement procedures. A summary was subsequently
uploaded on the Web site [27]. Before the introduction of
SEMS in each institute, we requested each member topromote cooperation among endoscopists and surgeons to
prepare for the possibility of adverse events.
Patients with acute colorectal obstruction or symptomatic strictures secondary to malignant neoplasms wereenrolled in the study. The goal was not to change the usual
treatment practice of the investigator or the center. Patientswere treated as per usual medical practices.
Forty-six facilities (14 academic centers and 32 community hospitals) participated in the study. Institutional

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review board approval was obtained for patient enrollment
prior to the start of the study. Each patient gave consent toundergo the procedure and registration of patient clinicaldata. Participating institutions registered all patients withacute colorectal obstructions managed using the WallFlex
enteral colonic stent (Boston Scientific Corporation, Natick, MA, USA) until completion of the study. Registration
was completed online through the Web site before or
immediately after the procedure. Patients with primarytumors receiving operation for resection were classified as‘‘BTS,’’ whereas patients for whom surgery was notscheduled were classified as ‘‘palliative.’’ All clinical data
were prospectively collected. Patients undergoing stenting
as a BTS were followed up until discharge after surgery.
Inclusion criteria
A criterion for enrollment was large bowel obstruction as
diagnosed by abdominal X-ray, colonoscopy, or computed
tomography (CT) scan. Patients with colorectal obstruction
secondary to malignant neoplasms were included in theregistry. Only patients with no previous colonic stenting
were included in the registry.
Exclusion criteria
Exclusion criteria included previous colonic stent placement, enteral ischemia, suspected or impending perforation,
intraabdominal abscess/perforation, severe inflammatorychanges around the tumor, contraindication to endoscopic
treatment, and any use of the stent other than those specifically outlined in indications for use.
Evaluation of obstruction symptoms
To assess oral intake levels and abdominal symptoms
before and after the procedure, we constructed a scoring
system similar to the one used for eating state assessment
in patients with malignant gastric outlet obstruction [29].
The ColoRectal Obstruction Scoring System (CROSS)
assigns a point score based on the patient’s oral intake level(Table 1): CROSS 0, requiring continuous decompression;

Table 1 The ColoRectal
Obstruction Scoring System

CROSS 1, no oral intake; CROSS 2, liquid or enteralnutrient intake; CROSS 3, soft solids, low residue, and full
diet with symptoms of stricture; and CROSS 4, soft solids,
low residue, and full diet without symptoms of stricture.
Stent device and procedure
Each patient was treated with an uncovered WallFlex
enteral colonic stent (Boston Scientific Corporation, Natick, MA, USA) with midbody and proximal flange diameters of 22/27 and 25/30 mm, respectively, and lengths of
6, 9, and 12 cm. SEMS placement was performed as presented in the pre-introduction publicity announcement. The
details of standard procedures for SEMS placement were
described on the Web site as a brief guideline [27]. Accessacross the stricture was established using a guidewire, anda contrast tube was inserted into the proximal lumen. The
length of the stricture was fluoroscopically measured using
a contrast agent, and the number of stents required to crossthe stricture was determined. To maintain good visualization of the tumor orifice, biopsy immediately before SEMS
placement was not recommended because the tumor orifice
becomes obscure due to bleeding. To identify the stricture
location, intraluminal or extraluminal marking with anendoscopic clip, lipiodol, or a radiopaque marker was
performed at the discretion of endoscopists. Stricture
dilatation before stent placement was generally forbidden.
Outcome measures
We examined the patients undergoing surgery for resection
after SEMS placement as a BTS. BTS was defined asscheduled elective surgery, independent of the time
between SEMS insertion and surgery. Technical success
was defined as accurate SEMS placement with adequate
stricture coverage on the first attempt without any adverse
events. Clinical success of a BTS was defined as thedecompression and relief of obstructive symptoms until
surgery without any stent-related complications and without
the need for endoscopic re-intervention or emergency surgery. The following conditions were considered to be procedure-related adverse events: perforation, re-obstruction,

Level of oral intake

Score

Requiring continuous decompression0

No oral intake

1

Liquid or enteral nutrient intake

2Soft solids, low residue, and full diet with symptoms of stricturea

3Soft solids, low residue, and full diet without symptoms of stricture

4aSymptoms of stricture include abdominal pain/cramps, abdominal distension, nausea, vomiting, constipation, and diarrhea, which are related to gastrointestinal transit

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stent migration, infection/fever, abdominal pain, andtenesmus. Perforation was diagnosed by clinical symptoms
and radiological examination or intraoperative findings.
Postprocedural adverse events were distinguished by theonset time: up to 7 days of stent placement, from 7 days
after stent placement up to 14 days, from 14 days after
stent placement up to 21 days, and from 21 days after stentplacement. Silent perforation, in which the stent was
intraoperatively exposed in the abdominal cavity without
preoperative symptoms, was not regarded as a complication. Patients undergoing stenting were followed up until
discharge from hospital. Evaluation of surgical outcomes
took into account the ability to perform elective surgery asplanned with or without the need for a diverting stoma.
Complications and length of hospitalization after surgery
were also recorded.
Statistical analysis
Continuous variables were presented as medians (range).
Statistical calculations were performed using SPSS version
8.0.2 (SPSS, Chicago, IL, USA).

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Results
A flowchart of the patient registry is shown in Fig. 1. A
total of 518 consecutive patients were enrolled in the study.
Five patients were excluded because of loose stenosis
identified by colonoscopy (n = 3), adhesive small bowel
obstruction (n = 1), and placement of another type of
SEMS (n = 1). The remaining 513 patients were the perprotocol cohort. The intention of treatment was a BTS in
312 patients (61 %) and palliative in 201 patients.
Baseline characteristics
Of the 312 BTS patients, 177 (57 %) were males, and the
median (range) age was 71 (35–94) years. Of the 312
patients, 296 (95 %) patients presented with acute colonicobstructive symptoms and the remaining 16 patients did
not have any stricture-related symptoms. Primary CRC was
reported in 98 % of the patients, and the remaining fivepatients had either locally recurrent CRC (n = 2), extracolonic cancer (n = 1), or benign lesions pathologically
proven after surgery (n = 2). The tumor was located in theFig. 1 Patient analysis
flowchart. BTS bridge to surgery

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Surg Endosc (2016) 30:3976–3986

left colon in 76 % of the patients, in the rectum in 4 % of
the patients, and proximal to the splenic flexure in 21 % of
the patients. At postoperative staging, 72 % of the patients
had localized CRC without metastatic disease, whereas
28 % of the patients had distant metastasis (Table 2).
Technical success
Successful SEMS insertion was achieved in 305 patients(technical success rate 97.8 %). Technical failure occurredin seven patients because of our inability to endoscopicallyvisualize the tumor in one case, inability to pass a guidewire in three cases, and perforation by the guidewire inthree cases (Table 3). These patients were included in theassessment of safety but were excluded from the assessment of effectiveness. Seven out of the 305 (2.3 %)patients required two stents in the first attempt. Six of theseseven patients had a single stricture, whereas one patient
Table 2 Characteristics of 312 patients who had self-expandable
metallic stent insertion as a bridge to surgery (BTS) for malignant
colorectal obstruction%

No. of patientsa

Age, median (range), years

71b(35–94)c

Sex
Male

57

177

Female43

135

Patient characteristics

CROSS before stent placement
0

37

114

1

30

93

2

13

41

3

13

42

4

7

22

Rectum4

11

Lt. sided colon

76

236

Rt. sided colon

21

65

98
0.6

307
2

Tumor characteristics
Stenosis/tumor localization

Etiology of colorectal obstruction
Primary colorectal cancer
Locally recurrent colorectal cancer
Other extrinsic origin

0.3

1

Benign lesion

0.6

2

Localized

72

225

With distant metastasis

28

87

CROSS ColoRectal Obstruction Scoring System, Lt. sided colon
rectosigmoid junction, sigmoid colon, descending colon, and splenic
flexure, Rt. sided colon transverse colon, ascending colon, and ileocecal junction
Unless otherwise indicated, b median, c range

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Clinical success as a BTS
All patients received follow-ups until discharge. In twopatients, obstructive colitis that occurred before stenting
worsened, and emergency surgery was performed. Adverse
events were recorded in 22 (7.2 %) patients (Table 5). A
total of 24 patients were categorized as clinical failure. If
technical errors were excluded, the clinical success rate
was 92.1 %. Emergency surgery was performed in eightpatients for the treatment of complications (n = 6) orobstructive colitis (n = 2); the details and outcomes ofthese patients are summarized in Table 5. In the cases of
emergency surgery, Hartmann’s resection was performedin three cases and resection of the tumor with primaryanastomosis without diverting stoma was performed in fivecases. Major procedural complications related to stentplacement included perforation in 1.6 % (n = 5) (Tables 5,6). One patient presented with abdominal emergency
2 days after stent insertion, and a blowout perforation in
the cecum was identified at acute laparotomy. One patient
had tumor perforation and underwent acute surgery 2 days
after stent insertion. One patient had perforation of theappendix with primary tumor invasion and underwent
acute surgery 2 days after stent insertion. Two patients had
perforation from the edge of the stent flare and underwent
emergency surgery 5 and 19 days after initial stent insertion, respectively. In both these patients, the stents that had
been used were 9 cm long and had a 22/27-mm body/flarediameter. Other major complications included persistentcolonic obstruction in three (1.0 %) patients, stent migration in four (1.3 %) patients, and sepsis due to obstructive
colitis in one (0.3 %) patient who underwent emergency
surgery. Minor complications included fever (n = 4),
tenesmus (n = 3), and stool impaction (n = 1). Patientswith stool impaction underwent endoscopic cleaning next
day of stent insertion.
Elective BTS

Tumor spreadinga

had a double stricture. Of the total of 312 stents, the mostcommonly used stent length was 6 cm (n = 204, 65.2 %),but in 101 (32.4 %) patients, a 9-cm-long stent was
selected. The most commonly used stent diameter was the
22/27-mm body/flare diameter (n = 287, 92.0 %)(Table 4). In only six (2.0 %) patients, the stricture wasdilated before stent placement using a balloon.

In total, 297 patients received elective resection. The
median time from SEMS insertion to surgery was 16 days
(interquartile range 12–24 days). Silent perforation (thestent was intraoperatively exposed in the abdominal cavity
without preoperative symptoms) was observed in four
(1.3 %) patients (Table 6). The overall perforation rate

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Table 3 Technical success andfailure rates%

No. of patients

Technical success rate

97.8

305

Technical failure rate

2.2

7Inability to pass the guidewire

1.0

3

Perforation by the guidewire

1.0

3Inability to endoscopically visualize the tumor

0.3

1

Table 4 Interventions before stent placement and stent placement
details
Stent procedure details%

No. of patients

Single stricture with one stent

97.7

298

Single stricture with two stents

2.0

6

Double strictures with two stents

0.3

1

Stricture no. and placed stent no.

Stent type (deployed stent number was 312)
6 cm length

65.4

204

9 cm length

32.4

101

12 cm length

2.2

7

22 mm diameter
25 mm diameter

92.0
8.0

287
25

consisting of technical perforation, procedure-related perforation, and silent perforation was 3.8 % (12/312). The
tumor could be resected in 290 patients (97.6 %). Open andlaparoscopic surgery was performed in 116 and 181
patients, respectively. The conversion rate from laparoscopic to open surgery was 10.5 % (19/181). There was nocorrelation between interval from stent insertion to surgery
or conversion from laparoscopic to open surgery. Resectionof the tumor with primary anastomosis was performed in
276 cases (93 %), which included covering stoma in ninecases and postoperative diverting stoma for anastomotic
leakage in two cases. Hartmann’s resection was performed
in 13 cases. Palliative colostomy only and palliative bypass
only were performed in six and two cases, respectively.
The overall stoma creation rate was 10.1 % (30/297), and89.9 % of the 297 patients were stoma free after surgery.
The overall postoperative morbidity rate was 17.7 %.
Anastomotic leakage of all grades occurred in 12 (4.3 %)of 279 patients with primary anastomosis. Two of these 12
patients underwent re-operation with stoma creation, andother patients were treated conservatively. There was nocorrelation between interval from stent insertion to surgery
and anastomotic leakage. Wound infection of all grades
occurred in 18 patients. Bowel obstruction of all grades
occurred in 15 patients, and two of the 15 patients underwent re-operation. Intraperitoneal abscess was observed inthree patients (Table 7). The median duration of hospitalization after surgery was 12 days (range 4–73). The overall
30-day mortality rate after technically successful SEMS
placement was zero, but the hospital postoperative mortality was 0.7 % (n = 2). These two patients died fromcancer progression.

Table 5 Clinical failure and occurrence of adverse events%

No. of patients

Time of occurrence*7 days

Clinical success rate

92.5

282

Clinical failure rate
Emergency surgery for obstructive colitis

7.8
0.6

24
2a

2

Adverse events

7.2

22

17

Perforation

1.6

5a

4

Sepsis0.3

1a1

Persistent obstruction

1.0

3

3

Migration

1.3

4

4

a

Fever

1.3

4

1

Tenesmus

1.0

3

3

Stool impaction

0.3

1

1

Acute appendicitis

0.3

1

1

14 days1

21 days

22 days

1

2

1

1

2

Emergency surgery was performed123

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Table 6 Characteristics in patients with perforation
Classification

Perforation cause

Age

Sex

Perforation time after
stent placement (days)

Tumor
site

Perforation
site

Surgery

Technical

Guidewire

68

F

0

S

S

Emergency

Technical

Guidewire

60

Technical

Guidewire

78

M

0

S

S

Emergency

M

0

S

S

Procedure-related

Proximal bowel (obstructive
colitis)86

Elective

F

2

A

C

Emergency

Procedure-related

Cancer

81

F

2

R

R

Emergency

Procedure-related

Infiltration of the cancer

67

M

2

C

V

Emergency

Procedure-related

Stent

80

F

5

RS

RS

Emergency

Silent perforation

Stent

63

F

8a

S

S

Elective

Silent perforation

Stent

68

M

16

S

S

Electivea

Procedure-related

Stent

71

M

19

S

S

Emergency

Silent perforation

Stent

84

F

20a

S

S

Elective

Silent perforation

Stent

85

F

30a

D

D

Elective

R rectum, RS rectosigmoid, S sigmoid colon, D descending colon, A ascending colon, C cecum, V vermiform appendixa

The time interval to elective operation (silent perforation was diagnosed during the surgery)

Discussion
In patients with acute colonic obstruction, emergency
surgical decompression has become mandatory as the traditional treatment option. It involves a defunctioning stoma
with or without primary resection of the obstructing tumor;
however, emergency operation is associated with highmorbidity and mortality rates, and a colostomy has an
impact on the quality of life [30]. Endoscopic placement of
SEMS is an effective alternative to surgical decompression
for colonic obstruction without emergency surgery. Furthermore, SEMS placement allows the treating physician toTable 7 Postoperativecomplications

All grade

Requiring re-operation%

No. of patients%

No. of patients

Overall

17.7

54

1.3

4

Anastomotic leakage

4.3a

12

0.7a

2

Intraperitoneal abscess

1.0

3
0.7

2

Wound infection

5.9

18

Bowel obstruction

4.9

15

Enterocolitis

1.0

3

Hemorrhagic gastric ulcer

0.3

1

Mesenteric panniculitis

0.3

1

Pulmonary complication

0.7

2

Sepsis0.3

1

Renal failure
Cerebral infarction

0.3
0.3

1
1

a

123

perform medical resuscitation, optimization of comorbid
disorders, bowel preparation, accurate tumor staging, andpreoperative total colonic examination to exclude synchronous proximal lesions [15, 16, 23, 24].
The present study is the largest prospective, multicenter
feasibility study on SEMS placement as a BTS for malignant colorectal obstruction. In Japan, colonic SEMS
placement was not covered by the National Health Insurance until January 2012. Appropriate SEMS placement
resulted in high technical and clinical success rates throughthe expertise offered by experienced doctors at the prestent placement meeting arranged to introduce the standard

The denominator is 279 patients with primary anastomosis

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Surg Endosc (2016) 30:3976–3986

procedural details of SEMS placement as described on the
Web site [27, 28]. As a result, the technical and clinicalsuccess rates of stent placement in the present study weresimilar to those reported in previous reviews and comparable with those reported in the previous largest multicenterprospective study from the WallFlex Colonic RegistryGroup (technical success rate 98 % and clinical successrate 94 %) [31, 32]. Previously, three systematic reviews[14, 15, 18] evaluated and presented data on the efficacy
and safety of colorectal stents in 598, 1198, and 1785
patients, respectively. The reported rates of technical success were 92, 93.2, and 96.2 % (median), with clinicalsuccess rates of 85 % (as a BTS with technical failure notbeing excluded), 78.1 % (as a BTS), and 92 % (median),
respectively. In patients with total obstruction, stentplacement is challenging [33]. Because all consecutive
patients in whom SEMS insertion was attempted wereenrolled in the present study, patients without total
obstruction, such as those with CROSS 3 or 4, wereenrolled, and this situation may be reflected in the hightechnical success rate.
In the present study, the clinical perforation rate was
2.7 %. In a previous comprehensive prospective study, theclinical perforation rate within 30 days was reported as
3 % [31, 32]. The previous three systematic reviews [14,15, 18] reported the perforation rates of 4, 3.8, and 4.5 %(median), respectively. On the other hand, some randomized controlled studies and a comparative study reported
high perforation rates, such as 10–12.8 % [19, 34, 35]. In
the European Society of Gastrointestinal Endoscopy(ESGE) clinical guidelines, published in 2014 [36], it ismentioned that several studies have shown no differencesin outcomes (efficacy and safety) based on different stentdesigns. However, from both our study and the study fromthe WallFlex Colonic Registry Group, WallFlex enteralcolonic stents were used and the perforation rate is about
3 % [31, 32]. On the other hand, in one RCT with a highperforation rate, four-fifths of the stents were Wallstent(Boston Scientific, Natick, MA, USA) and one-fifth of thestents were WallFlex [19]. Therefore, we speculate thatstent design may be related to the perforation rate. Furthermore, we believe that the shorter WallFlex colonicstent, which is still longer than the length of the stricture, isbetter. In the present study, 65 % of the stents used were
6 cm long, and in both patients who had perforation fromthe edge of the stent flare, the stents used were 9 cm long.
However, with regard to the data of the study from the
WallFlex Colonic Registry Group, in 61.3 % of thepatients, a 9-cm-long stent was selected and stents of 6
and 12 cm length were less commonly used.
In the present study, four of the five postprocedural
perforations occurred within 5 days after stent placement;
the remaining patient had perforation from the edge of the

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stent flare 19 days after stent insertion (Table 6). Iversen
et al. reported that one of the four perforations occurred
18 days after SEMS insertion, whereas the remaining threepatients experienced perforation within 5 days after SEMS
placement [37]. Other adverse events occurring after morethan 7 days only included fever in three patients who hadelective surgery (Table 5). In the present study, the mediantime from SEMS insertion to surgery was 16 days. In the
ESGE clinical guidelines from 2014 [36], a time interval of
5–10 days till operation is suggested when SEMS is used
as a bridge to elective surgery in patients with potentiallycurable left-sided colon cancer (weak recommendation,
low-quality evidence). It was written in the commentary tothese guidelines that, theoretically, a longer interval([1 week) may allow for better recovery and better optimal nutritional status; however, this may increase the riskof stent-related complications and may compromise surgery by more local tumor infiltration and fibrosis. Practically, according to our data, a longer interval did notincrease the risk of stent-related complications and did notincrease anastomotic leakage or conversion from laparoscopic to open surgery. Therefore, we cannot identify any
optimal time interval till operation following stent placement as a BTS.
In the present study, up to 97.4 % of patients withtechnical success underwent an elective surgery, whereas
only 2.6 % required emergency surgery. As demonstrated
by several previous systematic reviews based on metaanalyses, SEMS intervention was associated with a higher
successful primary anastomosis rate, lower stoma creation
rate, and lower overall morbidity after surgery [16, 23, 24];
this was consistent with the observations in the present
study. Anastomotic leakage and postoperative mortality
were very low compared with several systematic reviews
and meta-analyses.
In the ESGE clinical guidelines from 2014 [36], it ismentioned that colonic SEMS placement as a bridge toelective surgery is not recommended as a standard treatment for symptomatic left-sided malignant colonicobstruction with strong recommendation, because of a highrisk of stent-related perforation. Follow-up data of theStent-in 2 trial also showed that the cumulative incidenceof overall recurrences in patients with clinical stent-related
perforation was significantly increased than in those who
underwent emergency surgery or stenting without perforation [38]. The long-term impact of silent perforation, in
which the edge of the stent was visible during the scheduled operation, is unknown. Silent perforation wasobserved in four (1.3 %) patients in the present study. Two
randomized clinical trials of SEMS as a BTS versus
emergency surgery reported that the silent perforation rate
among cases with successfully placed stents was 9 and
57 %, respectively. We speculate that these high silent

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perforation rates correlated with relatively low technicalsuccess rates of stent placement (70 and 47 %, respectively) or selective stent design [19, 34]. In the ESGE
guidelines, it is mentioned that potential concerns havebeen raised about impaired oncological outcomes after
SEMS placement in patients with potentially curable coloncancer, particularly following stent perforation.
Our study group discussed some RCTs and cohort
studies, which reported long-term outcomes after SEMS
insertion as a bridge to elective surgery and referred in the
ESGE guidelines [35, 38–41]. In the three studies with highperforation rates, oncological long-term outcomes were
unfavorable. Therefore, we speculate that technical failureof the stent placement affects the long-term outcome. Withno study having good evidence of setting the primary
endpoint of oncological outcomes, the conclusions of the
ESGE guidelines appear to be premature. The most recent
systematic review and meta-analysis evaluated long-term
outcomes of colonic stent as a BTS (n = 704) and emergency surgery (n = 432) for malignant large bowel
obstruction, in which main outcome measures were overall
survival (OS), disease-free survival (DFS), and recurrence[42]. This study suggests that SEMS insertion followed bysurgery has no adverse influence in terms of patient
oncological outcomes, including OS, DFS, and recurrence,compared with emergency surgery.
However, theoretically enforced radial dilatation by
SEMS suggests the possibility of increased risk of not only
perforation but also tumor manipulation that can induce
dissemination of cancer cells into the peritoneal cavity,
surrounding lymphatic vessels, and bloodstream [43, 44].
On the other hand, long-term outcomes of malignant colorectal obstruction may improve whether cases of postoperative morbidity are fewer by SEMS placement as abridge to elective surgery.
The current analysis has at least three limitations. First,
this was a non-randomized, single-arm study; therefore, acomparison of stent and surgical morbidity and mortality
could not be performed. Second, 20 % of the patients
without total obstruction categorized as CROSS 3 (13 %)or 4 (7 %) received a preventive stent procedure. Finally,
there are no data on long-term outcomes available yet. In
order to clarify the long-term outcomes of SEMS, patient
survival is currently being monitored.
To reveal the oncological long-term effects of colonic
SEMS as bridge to elective surgery, large-size randomized
controlled trials are warranted. However, for randomized
controlled studies of colonic SEMS as BTS versus emergency surgery, it will be difficult to recruit patients for an
emergency setting and to standardize the procedure of stentinsertion. In our group, procedures of SEMS placement for
malignant colorectal obstruction had been standardized
already. In future, our group is going to undertake a large-

123

Surg Endosc (2016) 30:3976–3986

size randomized controlled trial to reveal the oncologicaleffects of colonic stent placement.
Acknowledgments This study was conducted with Japan Gastroenterological Endoscopy Society funding support and the Colonic
Stent Safe Procedure Research Group membership dues.
Compliance with ethical standards
Disclosures Dr. Shuji Saito has received personal fees from Boston
Scientific Japan, Century Medical Inc; Dr. Shuntaro Yoshida hasreceived personal fees from Boston Scientific Japan, Century Medical
Inc and ZEON Co, Dr. Hiroyuki Isayama has received donations andpersonal fees from Boston Scientific Japan, Century Medical Inc andTaewoong Medical Devices Inc. Drs. Takeaki Matsuzawa, Toshio
Kuwai, and Mamoru Shimada have received personal fees from
Boston Scientific Japan; Dr. Iruru Maetani has received personal feesfrom Boston Scientific Japan, Century Medical Inc, Piolax Medical
Device Inc, and MC Medical Inc; Dr. Koichi Koizumi has received
personal fees from Century Medical Inc and Olympus Medical Systems Corp; and Dr. Yoshihisa Saida has received grants and personal
fees from Boston Scientific Japan, Century Medical Inc, and Olympus
Medical Systems Corp. Drs. Tomonori Yamada, Masafumi Tomita,
Nobuto Hirata, Hideki Kanazawa, Toshiyuki Enomoto, and Hitoshi
Sekido have no conflicts of interest or financial ties to disclose.

Appendix
The Colonic Stent Safe Procedure Research Group includes
the following members in addition to the authors.
Tatsuya Osuga, Aijinkai Takatsuki General Hospital,
Takatsuki, Japan; Masaki Kikkawa, Akita Red Cross
Hospital, Akita, Japan; Mitsuru Goto, Asahikawa Kosei
Hospital, Asahikawa, Japan; Shungo Endo, Fukushima
Medical University Aizu Medical Center, Aizu-wakamatsu, Japan; Sayo Kobayashi, Fukuyama City Hospital,
Fukuyama, Japan; Shigeru Yamagishi, Fujisawa City
Hospital, Fujisawa, Japan; Ken Konishi, Higashiosaka City
General Hospital, Higashiosaka, Japan; Masanori
Yoshimitsu, Hiroshima City Asa Hospital, Hiroshima,
Japan; Satoshi Ikeda, Hiroshima Prefectural Hospital,
Hiroshima, Japan; Rintaro Moroi, Iwate Prefectural Isawa
Hospital, Oshu, Japan; Michiaki Watanabe, Kawaguchi
Municipal Medical Center, Kawaguchi, Japan; Hirofumi
Kawamoto, Kawasaki Medical School, Okayama, Japan;
Hirotoshi Hasegawa, Keio University School of Medicine,Tokyo, Japan; Atsushi Yamauchi, Kitano Hospital, Osaka,
Japan; Fuminori Teraishi, Kochi Health Sciences Center,
Kochi, Japan; Kohei Takayasu, Kyorin University Hospital, Mitaka, Japan; Takahiro Horimatsu, Kyoto University
Hospital, Kyoto, Japan; Yoshinori Kushiyama, Matsue Red
Cross Hospital, Matsue, Japan; Hiroaki Naota, Matsusaka
Chuo General Hospital, Matsusaka, Japan; Takuya Yamaguchi, Mimihara General Hospital, Sakai, Japan; Shigenori Masaki, Miyanomori Memorial Hospital, Sapporo,
Japan; Taku Sakamoto, National Cancer Center Hospital,

Author's personal copy
Surg Endosc (2016) 30:3976–3986

Tokyo, Japan; Kazuhiro Watanabe, National Center for
Global Health and Medicine, Tokyo, Japan; Masafumi
Inomata, Oita University Faculty of Medicine, Oita, Japan;
Nobuya Obana, Osaki Citizen Hospital, Osaki, Japan;
Masayoshi Horimoto, Osaka Saiseikai Senri Hospital,
Suita, Japan; Rika Kyo, Saiseikai Yokohamashi-Nanbu
Hospital,Yokohama, Japan; Shinei Kudo, Showa University Northern Yokohama Hospital, Yokohama, Japan;
Yasushi Nakamura, Takano Hospital, Kumamoto, Japan;
Mitsunori Ushigome, Toho University Omori Medical
Center, Tokyo, Japan; Takeshi Ohki, Tokyo Women’s
Medical University, Tokyo, Japan; Hiroyuki Kato, Tokyo
Women’s Medical University Medical Center East, Tokyo,
Japan; Shiro Hayashi, Toyonaka Municipal Hospital,
Toyonaka, Japan; Tomio Hirakawa, Yao Tokushukai
General Hospital, Yao, Japan; and Kensuke Kubota,
Yokohama City University Hospital, Yokohama, Japan.

References
1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011)
Global cancer statistics. CA Cancer J Clin 61:69–90
2. Matsuda A, Matsuda T, Shibata A, Katanoda K, Sobue T,
Nishimoto H, The Japan Cancer Surveillance Research Group(2013) Cancer incidence and incidence rates in Japan in 2008: astudy of 25 population-based cancer registries for the monitoringof cancer incidence in Japan (MCIJ) Project. Jpn J Clin Oncol
44:388–396
3. Winner M, Mooney SJ, Hershman DL, Feingold DL, Allendorf
JD, Wright JD, Neugut AI (2013) Incidence and predictors ofbowel obstruction in elderly patients with stage IV colon cancer:
a population-based cohort study. JAMA Surg 148:715–722
4. Jullumstro E, Wibe A, Lydersen S, Edna TH (2011) Colon cancer
incidence, presentation, treatment and outcomes over 25 years.
Colorectal Dis 13:512–518
5. Cheynel N, Cortet M, Lepage C, Benoit L, Faivre J, Bouvier AM(2007) Trends in frequency and management of obstructing
colorectal cancers in a well-defined population. Dis Colon Rectum 50:1568–1575
6. Iversen LH, Bülow S, Christensen IJ, Laurberg S, Harling H(2008) Danish Colorectal Cancer Group. Postoperative medical
complications are the main cause of early death after emergency
surgery for colonic cancer. Br J Surg 95:1012–1019
7. Cuffy M, Abir F, Audisio RA, Longo WE (2004) Colorectal
cancer presenting as surgical emergencies. Surg Oncol 13:149–
157
8. McArdle CS, Hole DJ (2004) Emergency presentation of colorectal cancer is associated with poor 5-year survival. Br J Surg
91:605–609
9. Tejero E, Mainar A, Fernández L, Tobı́o R, De Gregorio MA(1994) New procedure for the treatment of colorectal neoplastic
obstructions. Dis Colon Rectum 37:1158–1159
10. Saida Y, Sumiyama Y, Nagao J, Takase M (1996) Stent endoprosthesis for obstructing colorectal cancers. Dis Colon Rectum
39:552–555
11. Martinez-Santos C, Lobato RF, Fradejas JM, Pinto I, OrtegaDeballon P, Moreno-Azcoita M (2002) Self-expandable stent
before elective surgery vs. emergency surgery for the treatment ofmalignant colorectal obstructions: comparison of primary anastomosis and morbidity rates. Dis Colon Rectum 45:401–406

3985
12. ASGE Standards of Practice Committee, Harrison ME, Anderson
MA, Appalaneni V, Banerjee S, Ben-Menachem T, Cash BD,
Fanelli RD, Fisher L, Fukami N, Gan S, Ikenberry SO, Jain R,
Khan K, Krinsky ML, Maple JT, Shen B, Guilder TV, Baron TH,
Dominitz JA (2010) The role of endoscopy in the management ofpatients with known and suspected colonic obstruction andpseudo-obstruction. Gastrointest Endosc 71:669–679
13. Ansaloni L, Andersson RE, Bazzoli F, Catena F, Cennamo V, Di
Saverio S, Fuccio L, Jeekel H, Leppäniemi A, Moore E, Pinna
AD, Pisano M, Repici A, Sugarbaker PH, Tuech JJ (2010)
Guidelines in the management of obstructing cancer of the left
colon: consensus conference of the world society of emergency
surgery (WSES) and peritoneum and surgery (PnS) society.
World J Emerg Surg 5:29
14. Sebastian S, Johnston S, Geoghegan T, Torreggiani W, Buckley
M (2004) Pooled analysis of the efficacy and safety of self-expanding metal stenting in malignant colorectal obstruction. Am J
Gastroenterol 99:2051–2057
15. Khot UP, Lang AW, Murali K, Parker MC (2002) Systematic
review of the efficacy and safety of colorectal stents. Br J Surg
89:1096–1102
16. Cirocchi R, Farinella E, Trastulli S, Desiderio J, Listorti C,
Boselli C, Parisi A, Noya G, Sagar J (2013) Safety and efficacy ofendoscopic colonic stenting as a BTS in the management ofintestinal obstruction due to left colon and rectal cancer: a systematic review and meta-analysis. Surg Oncol 22:14–21
17. Cennamo V, Luigiano C, Coccolini F, Fabbri C, Bassi M, De
Caro G, Ceroni L, Maimone A, Ravelli P, Ansaloni L (2013)
Meta-analysis of randomized trials comparing endoscopic stenting and surgical decompression for colorectal cancer obstruction.
Int J Colorectal Dis 28:855–863
18. Watt AM, Faragher IG, Griffin TT, Rieger NA, Maddern GJ(2007) Self-expanding metallic stents for relieving malignant
colorectal obstruction: a systematic review. Ann Surg 246:24–30
19. van Hooft JE, Bemelman WA, Oldenburg B, Marinelli AW,
Lutke Holzik MF, Grubben MJ, Sprangers MA, Dijkgraaf MG,
Fockens P (2011) Colonic stenting versus emergency surgery foracute left-sided malignant colonic obstruction: a multicentre
randomised trial. Lancet Oncol 12:344–352
20. van Hooft JE, Fockens P, Marinelli AW, Bossuyt PM, Bemelman
WA (2006) Dutch stent-in study group. Premature closure of the
Dutch stent-in I study. Lancet 368:1573–1574
21. Tan KK, Zhang J, Liu JZ, Shen SF, Earnest A, Sim R (2009)
Right colonic perforation in an Asian population: predictors ofmorbidity and mortality. J Gastrointest Surg 13:2252–2259
22. Anwar MA, D’Souza F, Coulter R, Memon B, Khan IM, Memon
MA (2006) Outcome of acutely perforated colorectal cancers:
experience of a single district general hospital. Surg Oncol 15:
91–96
23. Tan CJ, Dasari BV, Gardiner K (2012) Systematic review andmeta-analysis of randomized clinical trials of self-expanding
metallic stents as a bridge to surgery versus emergency surgery
for malignant left-sided large bowel obstruction. Br J Surg
99:469–476
24. Huang X, Lv B, Zhang S, Meng L (2014) Preoperative colonicstents versus emergency surgery for acute left-sided malignant
colonic obstruction a meta-analysis. J Gastrointest Surg 18:584–
591
25. Saida Y, Sumiyama Y, Nagao J, Uramatsu M (2003) Long-term
prognosis of preoperative ‘‘bridge to surgery’’ expandable
metallic stent insertion for obstructive colorectal cancer: comparison with emergency operation. Dis Colon Rectum 46:S44–
S49
26. Yoshida S, Watabe H, Isayama H, Kogure H, Nakai Y, Yamamoto N, Sasaki T, Kawakubo K, Hamada T, Ito Y, Yashima Y,
Sasahira N, Hirano K, Yamaji Y, Tada M, Omata M, Koike K

123

Author's personal copy
3986
(2013) Feasibility of a new self-expandable metallic stent forpatients with malignant colorectal obstruction. Dig Endosc
25:160–166
27. Colonic Stent Safe Procedure Research Group. http://www.colonstent.com/001_mainpage_en.html
28. Matsuzawa T, Ishida H, Yoshida S, Isayama H, Kuwai T, Maetani I, Shimada M, Yamada T, Saito S, Tomita M, Koizumi K,
Hirata N, Sasaki T, Enomoto T, Saida Y (2015) A Japaneseprospective multicenter study of self-expandable metallic stentplacement for malignant colorectal obstruction: short-term safety
and efficacy within 7 days of stent procedure in 513 cases.
Gastrointest Endosc 82:697–707
29. Adler DG, Baron TH (2002) Endoscopic palliation of malignant
gastric outlet obstruction using self-expanding metal stents:
experience in 36 patients. Am J Gastroenterol 97:72–78
30. Tekkis PP, Kinsman R, Thompson MR, Stamatakis JD, Association of Coloproctology of Great Britain I (2004) The Associationof Coloproctology of Great Britain and Ireland study of large
bowel obstruction caused by colorectal cancer. Ann Surg 240:
76–81
31. Jiménez-Pérez J, Casellas J, Garcı́a-Cano J, Vandervoort J,
Garcı́a-Escribano OR, Barcenilla J, Delgado AA, Goldberg P,
Gonzalez-Huix F, Vázquez-Astray E, Meisner S (2011) Colonicstenting as a bridge to surgery in malignant large-bowel
obstruction: a report from two large multinational registries. Am J
Gastroenterol 106:2174–2218
32. Meisner S, González-Huix F, Vandervoort JG, Goldberg P,
Casellas JA, Roncero O, Grund KE, Alvarez A, Garcı́a-Cano J,
Vázquez-Astray E, Jiménez-Pérez J (2011) Self-expandable
metal stents for relieving malignant colorectal obstruction: shortterm safety and efficacy within 30 days of stent procedure in 447
patients. Gastrointest Endosc 74:876–884
33. Baron TH (2010) Colonic stenting: a palliative measure only or abridge to surgery? Endoscopy 42:163–168
34. Pirlet IA, Slim K, Kwiatkowski F, Michot F, Millat BL (2011)
Emergency preoperative stenting versus surgery for acute leftsided malignant colonic obstruction: a multicenter randomized
controlled trial. Surg Endosc 25:1814–1821
35. Sabbagh C, Browet F, Diouf M, Cosse C, Brehant O, Bartoli E,
Mauvais F, Chauffert B, Dupas JL, Nguyen-Khac E, Regimbeau
JM (2013) Is stenting as ‘‘a bridge to surgery’’ an oncologicallysafe strategy for the management of acute, left-sided, malignant,123

Surg Endosc (2016) 30:3976–3986
colonic obstruction? A comparative study with a propensity scoreanalysis. Ann Surg 258:107–115
36. van Hooft JE, van Halsema EE, Vanbiervliet G, Beets-Tan RG,
DeWitt JM, Donnellan F, Dumonceau JM, Glynne-Jones RG,
Hassan C, Jiménez-Perez J, Meisner S, Muthusamy VR, Parker
MC, Regimbeau JM, Sabbagh C, Sagar J, Tanis PJ, Vandervoort
J, Webster GJ, Manes G, Barthet MA, Repici A (2014) Selfexpandable metal stents for obstructing colonic and extracoloniccancer: European Society of Gastrointestinal Endoscopy (ESGE)
Clinical Guideline. Gastrointest Endosc 80:747–761
37. Iversen LH, Kratmann M, Bøje M, Laurberg S (2011) Self-expanding metallic stents as bridge to surgery in obstructing colorectal cancer. Br J Surg 98:275–281
38. Sloothaak DAM, van den Berg MW, Dijkgraaf MGW, Fockens P,
Tanis PJ, van Hooft JE, Bemelman WA (2014) Oncologicaloutcome of malignant colonic obstruction in Dutch Stent-In 2
trial. Br J Surg 101:1751–1757
39. Tung KL, Cheung HY, Ng LW, Chung CC, Li MK (2013) Endolaparoscopic approach versus conventional open surgery in thetreatment of obstructing left-sided colon cancer: long-term follow-up of a randomized trial. Asian J Endosc Surg 6:78–81
40. Alcantara M, Serra-Aracil X, Falco J, Mora L, Bombardo J,
Navarro S (2011) Prospective, controlled, randomized study of
intraoperative colonic lavage versus stent placement in obstructive left-sided colonic cancer. World J Surg 35:1904–1910
41. Gorissen KJ, Tuynman JB, Fryer E, Wang L, Uberoi R, Jones
OM, Cunningham C, Lindsey I (2013) Local recurrence after
stenting for obstructing left-sided colonic cancer. Br J Surg
100:1805–1809
42. Matsuda A, Miyashita M, Matsumoto S, Matsutani T, Sakurazawa N, Takahashi G, Kishi T, Uchida E (2014) Comparison of
long-term outcomes of colonic stent as ‘‘bridge to surgery’’ andemergency surgery for malignant large-bowel obstruction: ameta-analysis. Ann Surg Oncol 22:497–504
43. Koch M, Kienle P, Sauer P, Willeke F, Buhl K, Benner A,
Lehnert T, Herfarth C, von Knebel Doeberitz M, Weitz J (2004)
Hematogenous tumor cell dissemination during colonoscopy forcolorectal cancer. Surg Endosc 18:587–591
44. Maruthachalam K, Lash GE, Shenton BK, Horgan AF (2007)
Tumour cell dissemination following endoscopic stent insertion.
Br J Surg 94:1151–1154