INTRODUCTION

Several randomized controlled trials and meta-analysis have shown that laparoscopic colorectal surgery is associated with a better postoperative pain control, faster recovery of the intestinal transit and a shorter hospital stay compared to open surgery ^{1) (2) (3}. However, one of the limitations of minimally invasive surgery is decreased tactile sensitivity, which makes it difficult to identify small neoplasms ^{4) (5}. In such cases, several techniques have been proposed to facilitate intraoperative identification of these lesions. Currently, the most commonly used technique is preoperative endoscopic tattooing ⁶. This is an effective and safe procedure with a precision for the localization of the lesion between 70-100% ⁷.

Current recommendations for tattooing colonic neoplasms are not very specific. In 2013 the SAGES (Society of American Gastrointestinal and Endoscopic Surgeons) evidence-based guidelines for the laparoscopic resection of curable colon and rectal cancer recommended marking all small lesions without clearly specifying their size ⁸. On the other hand, a recent systematic review by Acuna et al. ⁹ suggested tattooing all lesions located in the transverse and left colon. In some cases the indication for marking the neoplasm is made by the endoscopist during the diagnostic colonoscopy, depending on the size and location of the lesion. In other cases the indication is made later by the surgeon, therefore the endoscopy must be repeated ¹⁰. Moreover, in a high percentage of patients in whom the preoperative tattooing has been performed, it is possible to identify the neoplasia during the laparoscopic examination without marking. Unnecessary marking incurs a higher cost ¹¹, discomfort for the patient, a longer procedure time and in some cases, may hamper the subsequent surgical procedure.

On the basis of these observations, the objective of this study was to establish endoscopic criteria for the selection of patients that require a tattoo during the diagnostic colonoscopy, avoiding a repeat preoperative endoscopy and unnecessary markings.

METHODS

RESULTS

One hundred and twenty patients with colonic neoplasms tattooed and operated by laparoscopy were included in the study (80 patients retrospectively and 40 prospectively). The mean age was 68 ± 12 years. The most frequent endoscopic localization of the neoplasia was the sigmoid colon followed by the ascending colon, in 59 (49%) and 29 (24%) patients, respectively. Other neoplasms were located in the transverse colon in 15 patients, the upper rectum in 10 and in the descending colon in 7 patients.

Table 1 shows the classification of neoplasms according to the endoscopic criteria described previously. More than half of the neoplasms were described as polypoids and/or occupied less than half of the circumference. The neoplasms were tattooed during the diagnostic endoscopy in 92 (77%) patients, whereas a second colonoscopy was needed to mark the lesion in the remaining 28 (23%) cases. There were no complications related to the tattooing technique. However, there were two complications related to the colonoscopy, one perforation and one post-polypectomy hemorrhage (1.6%). The median time between tattooing and surgery was 40 (22-59) days.

Table 1 Classification of neoplasms 

Table 2 shows the intraoperative characteristics of the tattoo and the surgical procedures performed. The tattoo was not visualized in 6 patients (5%). The tumor was subsequently identified during laparoscopy in 5 cases and an intra-operative colonoscopy was necessary in the final case. The location of the neoplasia was the ascending-transverse colon in 4 cases and the rectosigmoid junction and upper rectum in 2 cases. Ninety-seven (81%) of the lesions were identified as adenocarcinomas and 23 (19%) were identified as adenomas by anatomopathological analysis.

Table 2 Characteristics of intraoperative marking and surgical procedures 

There was a discrepancy between the location described by the endoscopist and that observed by the surgeon during the laparoscopy in 10 cases. Three of the neoplasms endoscopically located in the sigmoid colon were found to be in the rectum and 2 in the descending colon. Of the 3 neoplasms endoscopically located in the descending colon, 2 were found in the sigma and one in the transverse colon. Two neoplasms described by the endoscopist in the ascending and transverse colon were found by the surgeon in the transverse colon and ascending colon, respectively. Table 3 shows the endoscopic characteristics of the neoplasms according to the established criteria and whether they were identified during laparoscopy independently of the tattoo. In these cases, marking is unnecessary.

Table 3 Endoscopic characteristics and identification of the neoplasm during the laparoscopy procedure 

The location of the neoplasms during surgery, whether by endoscopic tattooing or by direct visualization by the surgeon, was possible in 119 (99%) cases. Fifteen stenosing neoplasms and 36 of 37 neoplasms that occupied more than half of the circumference could have been identified by the surgeon without the tattoo (98%). Whereas only 9 of 42 polypoid neoplasms and 8 out of 26 neoplasms occupying less than 50% of the circumference were identified intra-operatively without marking (25%). This difference was statistically significant (p = 0.0001). Based on the proposed endoscopic criteria, an identification rate of 98% by laparoscopy could be achieved when only tattooing those neoplasms described endoscopically as polypoids and those occupying less than 50% of the circumference.

DISCUSSION

The results of this study suggest that it is possible to establish selective criteria for tattooing colonic neoplasms that reduce the number of unnecessary tattoos, while maintaining an identification percentage of almost 100%. The choice of simple endoscopic criteria facilitates the decision to perform a tattoo during the diagnostic colonoscopy, therefore decreasing the number of patients that require a second colonoscopy for marking the neoplasms. In this study, the frequency was 23%.

The identification of colonic neoplasms during surgery is particularly important when using a laparoscopic approach, as the marking error rate during diagnostic colonoscopy reaches 15% ^{9) (10) (11) (12) (13) (14).} In this study, the percentage of inaccurate location marking was only 8%. This may be due to the fact that all procedures in the present study were performed by endoscopists with a wide experience and who have performed over 1000 annual endoscopies. Colonoscopy is highly operator-dependent which explains the great variability reported in the frequency of inaccurate marked locations.

Different methods have been reported to facilitate the localization of colonic neoplasms during laparoscopic surgery. A barium enema identifies lesions of a large and medium size but small neoplasms are often difficult to identify. On the other hand, computed tomographic colonography can identify lesions greater than 1 cm with an adequate anatomical accuracy but with a considerable radiation index ^{15) (16)}. Endoscopic indocyanine green marking is a safe and effective method but has some limitations. Specific devices are required in the operating room to visualize this soluble dye and in some cases the marking is not visible during surgery 8 days after marking ¹⁷. Therefore, the technique of choice for the localization of colonic neoplasms treated by a laparoscopic approach is Spot(r) tattooing ^{13) (18}. In our series, the tattoo was visualized in the majority of patients and the mark made with Indian ink was not identified in only 6 (5%) cases. The endoscopic technique was the same and there was no difference with regard to the time between the tattooing procedure and surgery, therefore it is unlikely due to technical failure. The rates reach 30% in other series ⁵.

There are currently no specific recommendations with regard to the colonic tumors that should be tattooed by endoscopy. Quality guidelines in the detection and diagnosis of colorectal cancer endorsed by the European Commission recommend that all suspicious lesions regardless of size should be tattooed ¹⁹. Zafar et al. ²⁰ recommend that polyps greater or equal to 10 mm for endoscopic resection, regardless of the endoscopic appearance, should be tattooed due to the greater risk of malignancy. However, if all resected polyps are marked according to these criteria, this could create problems in a future colectomy. There may be several tattoos that could create confusion for the surgeon with regard to selecting the segment for surgical resection. The tattoo with Indian ink is permanent and therefore can be identified several years later ⁵.

In the absence of a consensus for the indications of tattooing colonic neoplasms, it is important to establish precise and simple marking criteria that can be applied during the diagnostic colonoscopy. A second endoscopy for marking is not a trivial matter in these patients; the rate was 23% in this series. In a study of almost 350 patients ¹⁰, a second colonoscopy was necessary in 40% of cases. A re-endoscopy is associated with a greater discomfort for the patient, a repeat mechanical bowel preparation and other associated risks such as colonic perforation (0.08% to 0.16%) ^{21) (22}. Moreover, this is associated with an unnecessary use of healthcare resources.

Morphological criteria to select neoplasms for a preoperative tattoo were analyzed in this study. The aim was to establish simple and easy to apply criteria based on the circumferential involvement of the intestinal wall and the appearance of the lesion. Post-polypectomy scars were excluded as tattooing is mandatory in these cases, even in open surgery. On the other hand, tattooing is not necessary for neoplasms located in the cecum and rectum as neoplasms in these locations can be easily localized. In the present series, 10 upper rectum neoplasms were included as they were found in the distal sigmoid colon at the time of the diagnostic endoscopy. We have retained these neoplasms in the analysis as the morphological description of these neoplasms could contribute to the establishment of selective endoscopic tattooing criteria.

On the other hand, the neoplasms were marked in all patients and the assessment of the surgeon may be biased. However, all surgeons that participated in the present study were specialists in colon and rectal surgery and appreciate the importance of a strict evaluation. The intra-operative location of colonic neoplasms may be more problematic and the surgery time prolonged and in some cases converted to open surgery if these criteria are not applied.

The results of the present study confirm that tattooing stenosing lesions is unnecessary as they are always clearly identified intra-operatively due to their large size. In addition, the majority of neoplasms occupying more than half of the circumference can be identified without marking. Therefore, only neoplasms with a polypoid morphology and those limited to less than half of the intestinal circumference should be tattooed, as these tumors cannot be identified by laparoscopic approach.

In conclusion, our results suggest that it is possible to establish simple and precise endoscopic criteria that allow a selective tattooing of lesions during a diagnostic endoscopy in patients with colonic neoplasms. These results should be prospectively validated in a larger cohort of patients.