World J Surg (2007) 31:1491 1495 DOI 10.1007/s00268-007-9082-7 Tumor Localization for Laparoscopic Colorectal Surgery Yong Beom Cho Æ Woo Yong Lee Æ Hae Ran Yun Æ Won Suk Lee Æ Seong Hyeon Yun Æ Ho-Kyung Chun Published online: 30 May 2007 Ó Société 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 colorectal surgery. Methods A total of 310 patients underwent laparoscopyassisted 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 resected. 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 visualized, and three tumors were incorrectly localized. Another group of 94 patients (30.3%) underwent computed tomography (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 experienced clinical symptoms. Intraoperative colonoscopy was performed in four patients; two of the four were followed by 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 endoscopic tattooing, and the other two underwent intraoperative colonoscopy for localization. All lesions were correctly 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 different from that during open surgery. Preoperative endoscopic 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 surgery [2]. Therefore, an effective localization method is essential for solving this technical problem. Colonoscopy, barium enema or computed tomography (CT) colonography, 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.
1492 World J Surg (2007) 31:1491 1495 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 colonography, 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 inserted tangentially in the submucosa around the lesion and radially at the four corners. To analyze the value of endoscopic tattooing compared to the other conventional methods, 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 underwent 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 colonoscopy in all 310 patients. Of them, 203 patients had complete endoscopic reports available. The regional distribution of neoplasms was as follows: cecum (n = 7), ascending colon (n = 23), hepatic flexure (n = 12), transverse 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 localization (Table 1). The accurate localization rate of preoperative 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 follows: 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 lesions (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 tools Procedure 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
World J Surg (2007) 31:1491 1495 1493 accurate localization rate of CT colonography was 94.7% (89/94). Endoscopic tattooing A total of 96 of the 310 patients (31.0%) underwent tattooing 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 follows: 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 intraoperative 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 Table 2 Pathoanatomic data of the patients Parameter Tattooed group (n = 87) Nontattooed group (n = 206) 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 p 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 complication. 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 colonscopies 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 increasing 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 diagnosed 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
1494 World J Surg (2007) 31:1491 1495 nonpalpable lesions. Piscatelli et al. [6] reported that colonoscopy 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 retrospective evaluation of barium enema examinations, the investigators found sensitivities of 71% to 95% for colorectal 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 enema may not be helpful for lesion localization. In these instances, preoperative endoscopic tattooing or intraoperative colonoscopy can be performed. Additionally, the correlation between radiologic imaging and the intraoperative 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 demonstrated that its performance exceeds that of the barium enema procedure, and it approaches that of optical colonoscopy 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 enema. CT colonography has been replacing the barium enema 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 polyps can be precisely localized by colonic tattooing. The tattoo persists for a long time, which enables the subsequent 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- Fig. 1 Localization guidelines for laparoscopic colorectal surgery. s/p: status postoperatively right colon colonoscopy transverse colon ~ rectum CT CT colonography/barium enema CT CT colonography/barium enema visible invisible small flat tumor s/p polypectomy T3 stage endoscopic tattooing endoscopic tattooing operation if invisible if invisible operation intraoperative colonoscopy
World J Surg (2007) 31:1491 1495 1495 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]. Intraoperative 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 tattooing should be performed for precise localization. Conclusions With the combination of various methods, localization of tumors for laparoscopic surgery did not seem much different 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, intraoperative colonoscopy can be used for localization. References 1. Holzman MD, Eubanks S (1997) Laparoscopic colectomy: prospects and problems. Gastrointest Endosc Clin N Am 7:525 539 2. Wexner SD, Cohen SM, Ulrich A, et al. (1995) Laparoscopic colorectal surgery are we being honest with our patients? Dis Colon Rectum 38:723 727 3. Lacy AM, Garcia-Valdecasas JC, Delgado S, et al. (2002) Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet 359:2224 2229 4. Color (2004) A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 350:2050 2059 5. Vignati P, Welch JP, Cohen JL (1994) Endoscopic localization of colon cancers. Surg Endosc 8:1085 1087 6. Piscatelli N, Hyman N, Osler T (2005) Localizing colorectal cancer by colonoscopy. Arch Surg 140:932 935 7. Rex DK, Rahmani EY, Haseman JH, et al. (1997) Relative sensitivity of colonoscopy and barium enema for detection of colorectal cancer in clinical practice. Gastroenterology 112:17 23 8. Brady AP, Stevenson GW, Stevenson I (1994) Colorectal cancer overlooked at barium enema examination and colonoscopy: a continuing perceptual problem. Radiology 192:373 378 9. Fletcher RH (2000) The end of barium enemas? N Engl J Med 342:1823 1824 10. Frager DH, Frager JD, Wolf EL, et al. (1987) Problems in the colonoscopic localization of tumors: continued value of the barium enema. Gastrointest Radiol 12:343 346 11. Winawer SJ, Stewart ET, Zauber AG, et al. (2000) A comparison of colonoscopy and double-contrast barium enema for surveillance after polypectomy: National Polyp Study Work Group. N Engl J Med 342:1766 1772 12. Pickhardt PJ, Choi JR, Hwang I, et al. (2003) Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults. N Engl J Med 349:2191 2200 13. Feingold DL, Addona T, Forde KA, et al. (2004) Safety and reliability of tattooing colorectal neoplasms prior to laparoscopic resection. J Gastrointest Surg 8:543 546 14. McArthur CS, Roayaie S, Waye JD (1999) Safety of preoperation endoscopic tattoo with India ink for identification of colonic lesions. Surg Endosc 13:397 400 15. Fu KI, Fujii T, Kato S, et al. (2001) A new endoscopic tattooing technique for identifying the location of colonic lesions during laparoscopic surgery: a comparison with the conventional technique. Endoscopy 33:687 691 16. Nizam R, Siddiqi N, Landas SK, et al. (1996) Colonic tattooing with India ink: benefits, risks, and alternatives. Am J Gastroenterol 91:1804 1808 17. Botoman VA, Pietro M, Thirlby RC (1994) Localization of colonic lesions with endoscopic tattoo. Dis Colon Rectum 37:775 776 18. Kim SH, Milsom JW, Church JM, et al. (1997) Perioperative tumor localization for laparoscopic colorectal surgery. Surg Endosc 11:1013 1016 Acknowledgments The authors thank Jee Hye Kim and Ji-Eun Sim for their assistance with data collection.