Tumor Localization for Laparoscopic Colorectal Surgery

Yong Beom Cho Æ Woo Yong Lee Æ Hae Ran Yun ÆWon Suk Lee Æ Seong Hyeon Yun Æ Ho-Kyung Chun

Published online: 30 May 2007

� Societe Internationale de Chirurgie 2007

Abstract

Background Because palpating colonic tumors during

laparoscopy is impossible, the precise location of a tumor

must be identified before operation. The aim of this study

was to evaluate the accuracy of various diagnostic methods

that are used to localize colorectal tumors and to propose

an adequate localization protocol for laparoscopic colo-

rectal surgery.

Methods A total of 310 patients underwent laparoscopy-

assisted colectomy between April 2000 and March 2006.

We investigated if the locations of the tumors that were

estimated preoperatively were consistent with the actual

locations according to the operation.

Results All the tumors were correctly localized and re-

sected. Altogether, 203 patients had complete endoscopic

reports available. Colonoscopy was inaccurate for tumor

localization in 23 cases (11.3%). In total, 104 patients (33.5%)

underwent barium enema; five tumors (4.8%) were not visu-

alized, and three tumors were incorrectly localized. Another

group of 94 patients (30.3%) underwent computed tomogra-

phy (CT) colonography, which identified 91 of 94 lesions

(96.8%). Finally, 96 patients (31.0%) underwent endoscopic

tattooing; 2 patients (2.1%) did not have tattoos visualized

laparoscopically and required intraoperative colonoscopy to

localize their lesions during resection. Dye spillage was found

in six patients intraoperatively, but only one patient experi-

enced clinical symptoms. Intraoperative colonoscopy was

performed in four patients; two of the four were followed by

endoscopic tattooing, and the other two underwent intraop-

erative colonoscopy for localization. All lesions were cor-

rectly localized by intraoperative colonoscopy. The accuracy

of tumor localization was as follows: colonoscopy (180/203,

88.7%), barium enema (97/104, 93.3%), CT colonography

(89/94, 94.7%), endoscopic tattooing (94/96, 97.9%), and

intraoperative colonoscopy (4/4, 100%).

Conclusions With a combination of methods, localization

of tumors for laparoscopic surgery did not seem very dif-

ferent from that during open surgery. Preoperative endo-

scopic tattooing is a safe, highly effective method for

localization. In the case of tattoo failure, intraoperative

colonoscopy can be used for accurate localization.

Precise localization of tumors is a critical aspect of the

minimally invasive approach to colorectal surgery. The

inability to palpate colonic tumors makes it difficult for

surgeons to locate lesions during laparoscopic surgery [1].

Some investigators have reported removing the wrong

segment of the colon during laparoscopic colorectal sur-

gery [2]. Therefore, an effective localization method is

essential for solving this technical problem. Colonoscopy,

barium enema or computed tomography (CT) colonogra-

phy, endoscopic tattooing, and intraoperative colonoscopy

can be used in the appropriate clinical situation to localize

colonic lesions precisely. The purpose of this study was to

evaluate the accuracy of the various methods we have used

to localize tumors and to propose adequate guidelines for

localization during laparoscopic colorectal surgery.

Patients and methods

Between April 2000 and March 2006, a total of 310 patients

underwent laparoscopic surgery for colorectal tumors.

Y. B. Cho � W. Y. Lee (&) � H. R. Yun �W. S. Lee � S. H. Yun � H.-K. Chun

Department of Surgery, Samsung Medical Center,

Sungkyunkwan University School of Medicine, Ilwon-dong 50,

Gangnam-gu, Seoul 135-710, South Korea

e-mail: lwy555@smc.samsung.co.kr

123

World J Surg (2007) 31:1491–1495

DOI 10.1007/s00268-007-9082-7

Those patients who had familial adenomatous polyposis or

who underwent stoma creation alone for palliative purposes

were excluded from this study. The patients were operated

on for both premalignant and malignant diseases of the

colon and rectum (17 adenomas, 293 adenocarcinomas). All

of the patients underwent laparoscopic resection of a bowel

segment (4 ileocecectomies, 64 right hemicolectomies, 2

transverse colon resections, 14 left hemicolectomies, 180

anterior resections, 43 low anterior resections, 1 subtotal

colectomy, and 2 abdominoperineal resections).

We evaluated the accuracy of diagnostic methods that

comprised colonoscopy, barium enema or CT colonogra-

phy, endoscopic tattooing, and intraoperative colonoscopy.

Accuracy was defined as the percent of the estimated

locations that matched the actual operative location. The

large intestine was divided into eight segments from the

rectum to the cecum, and lesion localization was ascribed

to one of these locations.

Endoscopic tattooing was performed with India ink. It

was done with a standard sclerotherapy needle that was in-

serted tangentially in the submucosa around the lesion and

radially at the four corners. To analyze the value of endo-

scopic tattooing compared to the other conventional meth-

ods, 293 patients diagnosed with adenocarcinoma were

classified into two groups: the tattooed group (n = 87) and the

nontattooed group (n = 206). The pathoanatomical variables

of both groups were analyzed, and the following documents

were reviewed: preoperative colonoscopy reports, radiology

reports, operative records, and pathology reports.

The quantitative variable results were expressed as the

mean ± SD, and they were compared between groups using

Student’s t-test. Group comparisons were calculated using

the chi-squared test. Statistical analyses were performed

using the SPSS 11.5 statistical software package (SPSS,

Chicago, IL, USA).

Results

The 310 patients who were included in this study under-

went laparoscopic colectomy; none of the operations was

converted to open surgery. All the tumors were correctly

localized, and there was no incorrect colonic segment

resection.

Colonoscopy

The entire colon was examined preoperatively by colo-

noscopy in all 310 patients. Of them, 203 patients had

complete endoscopic reports available. The regional dis-

tribution of neoplasms was as follows: cecum (n = 7),

ascending colon (n = 23), hepatic flexure (n = 12), trans-

verse colon (n = 7), splenic flexure (n = 4), descending

colon (n = 11), sigmoid colon (n = 121), and rectum (n =

18). Of the 203 patients, 23 (11.3%) had erroneous local-

ization (Table 1). The accurate localization rate of preop-

erative colonoscopy was 88.7% (180/203).

Barium enema/CT colonography

Among the 310 patients, 104 (33.5%) underwent barium

enema. The anatomic distribution of tumors was as fol-

lows: cecum (n = 3), ascending colon (n = 13), hepatic

flexure (n = 2), transverse colon (n = 5), splenic flexure (n =

2), descending colon (n = 2), sigmoid colon (n = 69), and

rectum (n = 8). Five tumors (4.8%) were not visualized by

barium enema. Among the 99 tumors that were identified

by barium enema, 97 were correctly localized, and 2 were

incorrectly localized (Table 1). The accuracy rate of

localization with using barium enema was 93.3% (97/104).

Altogether, 94 of the 310 patients (30.3%) underwent

CT colonography. The regional distribution of neoplasms

was as follows: ascending colon (n = 9), hepatic flexure (n

= 5), transverse colon (n = 1), splenic flexure (n = 1),

descending colon (n = 5), sigmoid colon (n = 63), and

rectum (n = 10). CT colonography identified 91 of 94 le-

sions (96.8%). Three lesions were missed; one tumor was

in the splenic flexure, one was in the descending colon, and

one was in the rectum. In total, 89 of 91 tumors were

correctly localized on CT colonography, and 2 were

incorrectly localized; one tumor was in the hepatic flexure,

and the other was in the descending colon (Table 1). The

Table 1 Localization errors

according to the diagnostic toolsProcedure No. of patients Estimated location Operative location

Colonoscopy 7 Ascending colon Hepatic flexure

2 Sigmoid Descending colon

3 Sigmoid Rectum

11 Rectum Sigmoid

Barium enema 1 Hepatic flexure Transverse colon

1 Ascending colon Transverse colon

CT colonography 1 Ascending colon Hepatic flexure

1 Sigmoid Descending colon

1492 World J Surg (2007) 31:1491–1495

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accurate localization rate of CT colonography was 94.7%

(89/94).

Endoscopic tattooing

A total of 96 of the 310 patients (31.0%) underwent tat-

tooing and subsequent colorectal resection. The average

time between tattooing and resection was 6 days (range 0–

46 days). The anatomic distribution of tumors was as fol-

lows: cecum (n = 1), ascending colon (n = 7), hepatic

flexure (n = 4), transverse colon (n = 4), splenic flexure (n =

3), descending colon (n = 7), sigmoid colon (n = 64), and

rectum (n = 6).

The tattoos were visualized intraoperatively, and they

accurately localized the neoplasm in 94 of 96 patients

(97.9%). Two patients (2.1%) did not have the tattoos

visualized laparoscopically. These patients required intra-

operative colonoscopy to localize their lesions during

resection; both had sigmoid colon cancer.

The nontattooed group had a more advanced T stage and

a larger tumor size than the tattooed group (Table 2).

Endoscopic tattooing was used when the tumor was less

than 2 cm in size and was below the T2 stage. For the

patients with T3 stage disease, nine patients underwent

endoscopic tattooing to ensure localization at the beginning

of tattooing. However, during the laparoscopic operation it

was not difficult to find the serosal change in these lesions

with the naked eye or to feel firmness of the colonic wall

by the touch sense from the instrument. Thereafter, the

authors did not perform endoscopic tattooing for T3

lesions, and the lesions were well identified without the

help of endoscopic tattooing.

The operative findings revealed that India ink spilled

intraperitoneally in six patients. The scattered ink stains

were found, but they did not hinder resection in any way.

Only one clinically significant complication was identified:

One patient developed fever and abdominal pain following

endoscopic injection of India ink. The patient was operated

on the next day, and he improved without any complica-

tion.

Intraoperative colonoscopy

Intraoperative colonoscopy was performed in four patients;

three of the patients had sigmoid tumors, and one had a

rectal lesion. As mentioned above, two patients’ colons-

copies were followed by endoscopic tattooing owing to

nonvisualization. In the other two patients, the tumors were

localized by performing intraoperative colonoscopy only.

Laparoscopic clips were applied to the serosal surface of

the bowel under intraoperative colonoscopy guidance.

Discussion

Laparoscopic approaches for colorectal tumor are increas-

ing in clinical practice owing to research evidence that has

demonstrated results comparable to those of conventional

surgery in terms of both survival and recurrence [3, 4].

Accurate preoperative localization is even more important

with the advent of minimally invasive laparoscopy-assisted

colectomy because the colon cannot be palpated during this

procedure, and there is the potential of removing the wrong

segment of bowel [2]. In this study, all the tumors were

correctly localized using various methods, and they were

successfully removed by laparoscopic surgery.

Colonoscopy is considered the procedure of choice for

patients with suspected colorectal disease and particularly

for the diagnosis and management of colonic polyps or

tumors. Colonoscopy can accurately localize lesions, but

its success is heavily dependent on the experience of the

endoscopist. Combining colonoscopy with fluoroscopy can

help overcome this obstacle, but fluoroscopy involves

radiation and requires special equipment in the endoscopy

office. In this study, all the patients underwent colonoscopy

and were diagnosed with colorectal neoplasms. Complete

records of the colonoscopy were available for only 203

patients because 107 patients had been previously diag-

nosed at other hospitals. The accuracy of colonoscopy for

localizing a tumor was 88.7% in this study. Vignati et al.

[5] reported a 14% error rate for preoperative endoscopic

localization that led to difficulty with intraoperative

localization in 4.8% of the cases, which was mainly due to

Table 2 Pathoanatomic data of the patients

Parameter Tattooed group

(n = 87)

Nontattooed group

(n = 206)

p

Age (years) 56.5 ± 10.8 56.3 ± 10.4 0.861

Sex (F/M) 29/58 90/116 0.099

T stage < 0.001

Tis 14 (16.1%) 13 (6.3%)

T1 47 (54.0%) 30 (14.6%)

T2 17 (19.5%) 35 (17.0%)

T3 9 (10.3%) 128 (62.1%)

Size of tumor (cm) 1.8 ± 1.4 4.2 ± 1.8 < 0.001

Location of tumor 0.009

Right colon 10 (11.5%) 47 (22.8%)

Transverse colon 3 (3.4%) 2 (1.0%)

Left colon 8 (9.2%) 5 (2.4%)

Sigmoid colon 60 (69.0%) 131 (63.6%)

Rectum 6 (6.9%) 21 (10.2%)

Proximal margin (cm) 9.8 ± 4.5 10.6 ± 5.1 0.244

Distal margin (cm) 6.0 ± 4.9 6.7 ± 5.6 0.290

World J Surg (2007) 31:1491–1495 1493

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nonpalpable lesions. Piscatelli et al. [6] reported that col-

onoscopy had a considerable error rate (21%) for localizing

colorectal cancer, especially when previous colorectal

procedures had been performed.

Barium enema has previously been the main modality

used to localize lesions for colorectal surgery. It is a readily

available procedure, and it accurately localizes anatomic

regions; however, it is operator-dependent [7]. In a retro-

spective evaluation of barium enema examinations, the

investigators found sensitivities of 71% to 95% for colo-

rectal cancer detection [8]. The sensitivity of barium enema

was 95.2% in our current study, and five tumors (4.8%)

were not identified. Although barium enema is a good

method for localizing exophytic and stenosing lesions, it is

less effective for localizing early or flat tumors [9]. In cases

where a polyp has already been removed, the barium en-

ema may not be helpful for lesion localization. In these

instances, preoperative endoscopic tattooing or intraoper-

ative colonoscopy can be performed. Additionally, the

correlation between radiologic imaging and the intraoper-

ative findings is not always easily established, especially in

the transverse and sigmoid colon [10].

Computed tomography colonography is useful for

detecting not only the primary tumor but also synchronous

colon lesions, and it provides additional information

regarding regional and distant metastatic disease, the depth

of wall invasion, and the precise location of the lesion in

the colon prior to surgery. Published studies have demon-

strated that its performance exceeds that of the barium

enema procedure, and it approaches that of optical colo-

noscopy for detecting polyps and cancer [11, 12]. The

sensitivity of CT colonography for detecting tumors and

the accuracy for localization were 96.8% and 94.7%,

respectively; these values exceeded those for barium en-

ema. CT colonography has been replacing the barium en-

ema technique in recent years. The authors of this study

have not performed barium enema for localizing lesion

since January 2005.

Colonic tattooing with India ink represents a safe,

accurate, economical method to facilitate finding colonic

lesions intraoperatively. Colonoscopic tattoo injections can

be carried out either at the time of the initial colonoscopy

for an obviously malignant lesion or later for a completely

excised lesion that shows malignant histology. Small, flat

colonic malignancies or previously snared malignant pol-

yps can be precisely localized by colonic tattooing. The

tattoo persists for a long time, which enables the sub-

sequent surgical operation to be suitably scheduled. In

previous studies, the use of preoperative tattooing for

localizing colorectal lesions, using both conventional and

laparoscopic approaches, has been reported to be effective

in more than 90% of cases [13–15]. The accuracy of

endoscopic tattooing was 97.9% in this study, which was

consistent with the results of other investigators. The risk

of clinical complications has been stated to be less than

1%: There have been episodic reports of perforation, colon

abscess, or inflammatory pseudotumor with necrosis of the

perivisceral fat [16]. In our series, India ink was spilled

intraperitoneally in six patients, but only one patient

developed clinical symptoms. The patient was scheduled to

be operated on the day after endoscopic tattooing, and he

improved after the operation. No long-term complications

with tattooing have been reported. Botoman et al. [17]

described the only case of clinical complications associated

with the use of India ink for tattooing colonic lesions.

Accurate tattooing helps the laparoscopist avoid manipu-

CT colonography/barium enema

operation

invisible T3 stage

if invisible

colonoscopy

right colon transverse colon ~ rectum

CT

CT colonography/barium enema

endoscopic tattooing

intraoperative colonoscopy

small flat tumor s/p polypectomy

if invisible

visible

endoscopic tattooing

operation

CT

Fig. 1 Localization guidelines

for laparoscopic colorectal

surgery. s/p: status

postoperatively

1494 World J Surg (2007) 31:1491–1495

123

lating a cancer intraoperatively and aids the surgeon by

marking an appropriate margin of tissue for resection. The

authors experienced failure of tattoos to localize colorectal

lesions in two patients; therefore, using an appropriate

technique is important. There are various tinting methods,

but two-step ink injection, which includes injecting saline

before tattooing to form a submucosal bleb, is better than

the other techniques for tumor visualization; it also creates

fewer ink spillage problems [15].

Intraoperative colonoscopy is another method for

localizing a tumor during laparoscopic surgery. It is a

somewhat complex procedure that requires an experienced

endoscopist and specific instruments in the operating room.

It is essential to prevent intestinal distension due to the air

insufflated for the endoscopy procedure [18]. Intraopera-

tive colonoscopy with laparoscopic clipping applied to the

serosa just distal to the lesion can also be done.

We selected a proper localization method on the basis of

the following (Fig. 1). If the tumor is located at the right

colon based on the colonoscopy findings, and the site is

reaffirmed by CT or CT colonography (or barium enema),

further localization is unnecessary. However, if the tumor

is invisible on CT or CT colonography (or barium enema)

owing to previous polypectomy, endoscopic tattooing is

recommended for localization. If the tumor is placed distal

to the transverse colon and it is a T3 or T4 lesion according

to the CT or CT colonography (or barium enema) findings,

further localization is unnecessary. If the tumor is small or

invisible owing to previous polypectomy, endoscopic tat-

tooing should be performed for precise localization.

Conclusions

With the combination of various methods, localization of

tumors for laparoscopic surgery did not seem much dif-

ferent from that of open surgery. Colonoscopy is highly

sensitive for detecting colorectal tumors, yet it is associated

with a considerable incidence of erroneous localization.

Barium enema or CT colonography is of great value for

localizing tumors. Endoscopic tattooing seems the safest

and most effective method for localizing colonic lesions,

especially for such lesions as small, flat tumors or those at

polypectomy sites. In the event of tattoo failure, intraop-

erative colonoscopy can be used for localization.

Acknowledgments The authors thank Jee Hye Kim and Ji-Eun Sim

for their assistance with data collection.

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