Surg Endosc DOI 10.1007/s00464-009-0466-7
Transanal endoscopic microsurgery for rectal tumors: experience at Korea’s National Cancer Center Woon Kyung Jeong Æ Ji Won Park Æ Hyo Seong Choi Æ Hee Jin Chang Æ Seung-Yong Jeong
Received: 20 October 2008 / Accepted: 13 March 2009 Ó Springer Science+Business Media, LLC 2009
Abstract Background Transanal endoscopic microsurgery (TEM) is a minimally invasive alternative to transanal excision, enabling complete local excision of selected benign or malignant rectal tumors. This study aimed to determine the surgical and oncologic results for rectal tumors excised by TEM. Methods From November 2001 to October 2007, 45 patients underwent TEM for excision of adenoma (13 patients), carcinoid tumor (6 patients), and carcinoma (26 patients). The patients included 27 men and 18 women with a median age of 52 years (range, 22–72 years). Results The median tumor distance from the anal verge was 7 cm (range, 3–15 cm), and the median tumor size was 17 mm (range, 2–60 mm). There was no procedure-related morbidity or mortality. However, one patient with rectal carcinoma died of lung cancer during the follow-up period. Of 13 patients with adenomas, 1 patient (7.7%, 1/13) experienced local recurrence 5 months after surgery. No recurrence occurred for six patients with carcinoid tumors. Histologic examination of the carcinomas showed pathologic tumor (pT) stage 0 (ypT0) in 2 patients, pT1 in 17 patients (including ypT1 in 1 patient), pT2 in 6 patients, and pT3 in 1 patient. Immediate salvage surgery was performed for five patients (19%, 5/26). During a median follow-up W. K. Jeong J. W. Park H. S. Choi H. J. Chang Center for Colorectal Cancer, Research Institute and Hospital, National Cancer Center, Goyang, Korea
period of 37 months (range, 5–72 months), one patient (3.8%, 1/26) experienced local recurrence. The overall and disease-free 5-year survival rates for patients with carcinoma were 96.2% and 88.5%, respectively. Conclusions The TEM procedure is a safe and appropriate surgical treatment option for benign rectal tumors. With strict patient selection, it is oncologically safe for early-stage rectal carcinomas. Keywords Local excision Rectal tumor Transanal endoscopic microsurgery
Transanal endoscopic microsurgery (TEM) is a minimally invasive surgical technique that Buess introduced in 1983 as an alternative to conventional transanal excision (TAE) [1]. Conventional TAE has the limitations of poor visualization, accessibility only to the lower rectum, and high rates of local recurrence [2, 3]. The TEM procedure enables full-thickness tumor excision with an adequate resection margin under magnified view and access to the upper rectum or even to the distal sigmoid colon. It also provides lower rates of positive resection margin and recurrence than TAE [4]. Despite these advantages, TEM is not widely used in Korea due to the cost of equipment and the additional training required. This study aimed to present our experience with TEM for rectal tumors and to determine the morbidity and long-term results.
W. K. Jeong e-mail:
[email protected]
Materials and methods S.-Y. Jeong (&) Department of Surgery, Seoul National University College of Medicine, 101 Daehangno, Jongno-gu, Seoul 110-744, Korea e-mail:
[email protected]
From November 2001 to October 2007, 45 patients underwent TEM for rectal tumor at the Center for
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Colorectal Cancer, National Cancer Center, Korea. The data were collected retrospectively from electronic medical records. The patients included 27 men and 18 women with a median age of 52 years (range, 22–72 years). All the patients underwent preoperative evaluation including history taking, digital rectal examination, routine laboratory tests including complete blood cell count and liver function test, chest radiography, colonoscopy, tumor biopsy, and pathologic examination. The level of preoperative serum carcinoembryonic antigen (CEA) was measured for patients with carcinoma or tumor suspicious of carcinoma. Preoperative tumor staging was performed by colonoscopy and/or transrectal ultrasonography (TRUS) and/or magnetic resonance imaging (MRI). The treatments delivered before TEM included colonoscopic polypectomy and endoscopic mucosal resection for eight patients each. Neoadjuvant chemoradiotherapy was performed for three patients with clinical T3 tumors. For benign rectal adenoma, the indication for TEM included tumors unsuitable for endoscopic removal. The indications for rectal carcinoid tumor included tumors smaller than 10 mm and those with an incomplete resection margin after endoscopic resection. For rectal carcinoma, the indications included invasion to the level of the submucosa (T1), good or moderate differentiation, no lymphovascular invasion, and size smaller than 40 mm. The TEM procedure was performed for one patient with a T2 rectal lesion and concomitant advanced primary lung cancer, and for 3 patients with T3 lesions who refused radical resection after neoadjuvant chemoradiotherapy. Informed consent was obtained from all patients after an explanation regarding the procedure, indications, and potential complications such as bleeding, perforation, temporary incontinence, and the risk of local recurrence and distant metastasis. The indications for salvage surgery after TEM included invasion deeper than the submucosal layer, poor differentiation, mucinous carcinoma, lymphovascular invasion, and positive resection margin. The presence of tumor at the resection margin was defined as a positive resection margin. The development of tumor at or near the previous TEM site was defined as a local recurrence.
Table 1 Postoperative outcomes for rectal tumors according to histologic type
Final diagnosis (n)
Adenoma (n = 13) Carcinoid tumor (n = 6) Carcinoma (n = 26)
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Results The median tumor distance from the anal verge was 7 cm (range, 3–15 cm), and the median tumor size was 17 mm (range, 2–60 mm). The median surgical duration was 75 min (range, 30–265 min). The median postoperative hospital stay was 7 days (range, 2–16 days). The postoperative pathologic diagnosis was adenoma for 13 patients (28.9%), carcinoid tumor for 6 patients (13.3%), and carcinoma for 26 patients (57.8%). Comparison of the pre- and postoperative diagnoses showed that two patients with a diagnosis of tubulovillous adenoma by preoperative biopsy had carcinoma at the postoperative histologic examination. In the cases of carcinoid tumor and carcinoma, the histologic diagnosis did not differ between the pre- and postoperative pathologies. The pre- and postoperative diagnoses were identical for 43 (95.5%) of the 45 patients. There was no procedure-related morbidity or mortality. However, one patient with rectal carcinoma died of lung cancer during the follow-up period. A positive resection margin was documented for 7 (15.6%) of the 45 patients, adenoma for 3 of the patients, carcinoid tumor for 2 of the patients, and carcinoma for 2 of the patients. The postoperative outcomes for rectal tumors according to the histologic types are listed in Table 1. Among the 13 adenomas, the final histologic examination confirmed 4 histologic types: tubular (n = 2, 15.4%), tubulovillous (n = 3, 23.1%), villous (n = 7, 53.8%), and serrated (n = 1, 7.7%) adenoma. During a median follow-up period of 42 months (range, 1–63 months), local recurrence had developed for one patient (7.7%, 1/13) with an incomplete margin 5 months after surgery. Because of its large size (35 mm) and the possibility of malignant potential, the recurrent tumor was treated with radical surgery (anterior resection). Both the primary and recurrent tumors showed the same histologic features of tubulovillous adenoma. No lymph node metastasis was noted. Among the six cases of carcinoid tumor, histologic examination showed no residual tumor in the excised specimens of four patients who underwent endoscopic mucosal resection (EMR) before TEM. Of the two patients (33.3%) who underwent TEM as an initial therapy, one had a T1 lesion and a positive resection margin in the specimen
Tumor size (mm) median (range)
Positive resection margin n (%)
Duration of follow-up months (range)
Local recurrence n (%) 1 (7.7)
19 (4–60)
3 (23.1)
42 (1–63)
10.5 (5–16)
2 (33.3)
41 (13–66)
0
15 (2–35)
3 (11.5)
37 (5–72)
1 (3.8)
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resected by TEM. The other patient had a tumor larger than 10 mm (16 mm), and further resection was recommended but subsequently refused by the patient. During a median follow-up period of 41 months (range, 13–66 months), there was no recurrence in any patient with carcinoid tumor. Among the 26 carcinomas, there were no mucinous or poorly differentiated tumors. A positive resection margin was noted in three patients (11.5%). Histologic examination of the carcinomas showed pathologic tumor (pT) stage 0 in 2 patients, pT1 in 17 patients, pT2 in 6 patients, and pT3 in 1 patient. Two patients with pT0 lesions and one patient with a pT1 lesion had received neoadjuvant chemoradiotherapy before TEM. Of the 17 patients with submucosal (SM) carcinoma (pT1), 3 had SM1, 4 had SM2, 4 had SM3, and 6 had an invasion of unknown depth. The patients with SM1 lesions and unknown SM status were observed without any further treatment. Those who had SM2 (n = 3) and SM3 (n = 4) lesions refused further treatment. One of the four patients with a SM2 lesion underwent salvage surgery due to a positive resection margin. Immediate salvage surgery was performed for five patients (19%, 5/26) (Table 2). Of these, one patient with a single metastatic regional lymph node after salvage surgery experienced the development of right external iliac lymph node metastasis 28 months after salvage surgery. The metastatic nodes were excised by laparotomy, and histologic examination showed the involvement of three lymph nodes. Of the three patients with T2 lesions who did not undergo salvage surgery, one had concomitant lung cancer and two refused salvage surgery. One of the two latter patients (3.8%, 1/26) received adjuvant radiotherapy but experienced local recurrence 47 months after TEM. The recurrent lesion was treated by ultralow anterior resection. The pathologic stage was pT4N0. The tumor had invaded the posterior wall of the vagina. As mentioned earlier, one patient (3.8%, 1/26) experienced local recurrence after TEM. One of the five patients
who underwent salvage surgery experienced metastasis to the right external iliac lymph node. The overall and disease-free 5-year survival rates for the patients with carcinoma were 96.2% and 88.5%, respectively.
Discussion The TEM procedure is widely used in Europe and the United States and widely reported. In Korea, however, TEM has been performed only at two hospitals, including our institution [5]. A major obstacle to the use of TEM in clinical practice in Korea is that the medical cost of this procedure is not covered by the National Health Insurance Program of Korea despite the high cost of TEM equipment and the need for a high level of surgical skill. The TEM procedure is indicated for benign and malignant rectal tumors [6, 7]. Previous studies reported local recurrence rates of 0% to 15% for adenoma after TEM [6– 15]. The rate for local recurrence after excision of adenoma in the current study was 7.7%, which is comparable with rates reported in the literature. Complete excision of adenoma and tumor clearance at the resection margin are essential for preventing local recurrence. McCloud et al. [16] reported that a positive resection margin or a fragmented specimen results in a significantly higher rate of recurrence. Moore et al. [4] compared TEM and TAE for rectal tumors and reported that TEM was more likely than TAE to yield clear resection margins (90% vs. 71%) and a nonfragmented specimen (94% vs. 65%). The recurrence rate for TEM (5%) was lower than for TAE (27%). Kinoshita et al. [17] reported no recurrence after performing TEM for 27 patients with carcinoid tumor. No tumors showed lymphovascular invasion, and the deep and lateral margins were free of tumor. The authors suggested that TEM may be an effective surgical option for complete removal of residual tumors in patients with a microscopic positive margin after endoscopic polypectomy. In the current study, two patients with a positive resection margin
Table 2 Characteristics and outcomes for patients who underwent salvage surgery Patient Postoperative stage Resection margin Lymphovascular invasion Salvage surgery Pathologic stage Tumor
Lymph node (metastasis/total)
1
T2
Positive
Positive
LAR
No residual tumor N0 (0/19)
2
T2
Negative
Positive
LAR
No residual tumor N0 (0/13)
3
T2
Positive
Positive
LAR
T3
4
T3
Negative
Positive
LAR
No residual tumor N1 (1/12)
5
T1 (SM2)
Positive
Positive
LAR
No residual tumor N0 (0/13)
N0 (0/18)
LAR low anterior resection, T1 tumor invades the submucosa, T2 tumor invades the muscularis propria, T3 tumor invades through the muscularis propria into the subserosa, N0 no regional lymph node metastasis, N1 metastasis in 1–3 regional lymph nodes, SM2 tumor invades the middle third of the submucosa
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but no lymphovascular invasion had no recurrence during the follow-up period. For four patients with a positive resection margin after EMR, treatment with TEM achieved complete resection margins. Studies comparing radical surgery with TEM for T1 rectal cancer demonstrate no significant difference in recurrence or 5-year survival rate between the two approaches [5, 18]. The TEM procedure has some benefits over radical surgery. It offers the opportunity to save the sphincter and has a lower morbidity rate. For T1 rectal cancer with favorable histologic features, TEM is an accepted standard therapy [6, 9]. However, TEM with curative intent for T2 and T3 rectal cancer is limited due to the high risk of lymph node metastasis [19]. Recurrence rates after TEM for adenocarcinoma are reported to range from 0% to 33% [6–14, 20]. The recurrence rates according to tumor stage are reported to be 0% to 19% for T1, 12% to 50% for T2, and 33% to 75% for T3 rectal cancer [11–14, 20]. The wide variation in recurrence rates among studies could be attributable to differences in the use of adjuvant therapy and diversity of patient cohorts. In the current study, the recurrence rates after TEM were for 0% for T1, 16.7% for T2, and 0% for T3 lesions. Of the six patients with T2 lesions, one patient who received adjuvant radiotherapy after refusing salvage surgery experienced local recurrence, whereas two patients who refused any further treatment did not. Pathologic stage T2 and T3 lesions have a high risk of lymph node metastasis that ranges from 17% to 50% [19]. The routine use of TEM for T2 and T3 lesions has a high possibility of retaining metastatic lymph nodes [10]. Radiotherapy after local excision of T2 and T3 lesions has been used previously to reduce tumor recurrence. However, the incidence of local failure did not decrease significantly (15–18%) [21, 22]. Three patients in the current study with clinical T3N0 tumors were treated with neoadjuvant chemoradiotherapy and downstaged. Postoperative pathology showed that two of the patients had a complete response, and one had a near complete response. None of these patients experienced recurrence during the follow-up period. Two were complete responders at 5 and 32 months, and one was a near complete responder at 54 months. Some investigators have suggested that local excision alone could be enough for patients with T2 and T3 rectal cancer who show a significant response after neoadjuvant chemoradiotherapy. Kim et al. [23] performed local excision for 26 patients with T2 and T3 rectal cancer after neoadjuvant chemoradiotherapy. Pathologic partial responses were achieved for 9 patients (35%) and complete responses for 17 patients (65%). One patient who refused abdominoperineal resection after a partial response experienced recurrence.
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Lezoche et al. [24] reported the results for 100 patients with small T2 and T3 N0 rectal tumors managed by TEM after preoperative radiotherapy. They reported the cumulative probability of local recurrence to be 5% and of distant recurrence to be 2% at 90 months. No recurrence occurred for any patients with tumors downstaged or reduced in size by more than 50% after radiotherapy. The cancer-specific survival rate during the 90-month follow-up period was 89%, and the overall survival rate was 72%. These results are comparable with those reported for conventional open or laparoscopic surgery [25, 26]. The complication rates for TEM are reported to range from 0% to 26% [7, 13, 15, 20]. In particular, the reported complication rates are 3% to 7% for adenoma and 0% to 28% for carcinoma [15]. There were no procedure-related complications in the current study. One of the most common complications described in previous reports was intraand postoperative hemorrhage. Conventional surgical instruments such as dissectors and graspers designed for TEM are either right- or lefthanded, and their tips do not rotate. In contrast, recent laparoscopic instruments have rotatable tips, and an all-inone type of laparoscopic dissector combined with suction and an irrigator can facilitate dissection with timely suction of fluid and smoke during the procedure. We have used both conventional TEM instruments and laparoscopic instruments. An ultrasonically activated scalpel for laparoscopy also was used in the current study, especially for excising tumors in the deep layers. This instrument also could have contributed to a reduction in intra- and postoperative hemorrhage. In conclusion, TEM is a safe and appropriate surgical treatment option for benign rectal tumors. With strict selection of patients, it is oncologically safe for early-stage rectal malignancy. Precise preoperative tumor staging is important in the selection of appropriate candidates for TEM.
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