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10.1245/ASO.2006.04.010
Annals of Surgical Oncology 13:547-556 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Local Recurrence After Transanal Endoscopic Microsurgery for Rectal Polyps and Early Cancers

Sabha Ganai, MD, Prathima Kanumuri, MD, Roshni S. Rao, MD and Albert I. Alexander, MD

Department of Surgery, Baystate Medical Center/Tufts University School of Medicine, 759 Chestnut Street, Springfield, Massachusetts 01199

Correspondence: Address correspondence and reprint requests to: Sabha Ganai, MD; E-mail: sabha.ganai{at}bhs.org.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Transanal endoscopic microsurgery (TEM) allows for local excision of rectal neoplasms with greater exposure than transanal excision and less morbidity than transabdominal approaches. This study examines the implications of the procedure with respect to predictors of recurrence.

Methods: We performed a retrospective analysis of 144 consecutive TEMs from 1993 to 2004.

Results: The study comprises 107 patients presenting for TEM with benign disease and 32 patients with cancer. Patients had a mean age of 64 ± 14 (SD) years. TEM was performed for recurrent lesions in 17% of cases. Pathologic classification of the lesions after TEM was benign adenoma in 45%, adenoma with high-grade dysplasia (HGD) in 17%, cancer in 33%, and other in 4%. Complications occurred in 10%, and local recurrence occurred in 15% of patients. Median follow-up was 44 months, with a median time to recurrence of 14 months. Positive margins did not influence lesion recurrence. Recurrence of cancers correlated with the depth of tumor invasion (P < .05). On multivariate analysis, independent predictors of recurrence were lesion size and the presence of HGD within adenomas (P < .05). Five-year neoplastic recurrence probabilities were 11% for benign adenomas, 35% for adenomas with HGD, and 20% for cancers (P = .31); invasive recurrence probabilities were 0% for benign adenomas, 15% for adenomas with HGD, and 13% for cancers (P < .05).

Conclusions: Close endoscopic follow-up is warranted after TEM for both benign and malignant disease, with special attention to lesions with HGD. TEM can be performed safely for early rectal cancer with careful patient selection.

Key Words: Rectal cancer • Rectal adenoma • Transanal endoscopic microsurgery • Transanal local excision • Dysplasia


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Local excision of rectal neoplasms is well described as an alternative to abdominoperineal resection (APR) and anterior resection in selected patients, with fewer postoperative complications and operative mortality.1 Historically, local excision has included transanal,2 transsacral,3 and transsphincteric4 approaches. Transanal endoscopic microsurgery (TEM) is a minimally invasive technique that allows greater exposure and facility in the management of proximal disease than traditional local excision, with a shorter operative time and less morbidity than the radical surgical procedures.5 This study examined the outcomes of local excision with TEM in the management of benign and early malignant rectal lesions.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A retrospective review was conducted on patients undergoing TEM at Baystate Medical Center in Springfield, MA, between November 1993 and October 2004. A single surgeon (A.I.A.) performed the procedure, using TEM as the exclusive technique of local excision of sessile lesions of the rectosigmoid colon. Preoperative diagnostic work-up included history, clinical examination, colonoscopy, and rigid sigmoidoscopy. The preoperative pathologic diagnosis was indicated by endoscopic biopsy and/or endorectal ultrasonographic depth of invasion. Bowel preparation and topical estrogen cream for women were administered before surgery.

The TEM operative technique was conducted as previously described6,7 with patients under general anesthesia by using a 20-cm-long operating rectoscope (Richard Wolf, Knittlingen, Germany) fixed by a Martin arm. Carbon dioxide insufflation was used. Lesions were excised circumferentially with at least 10-mm macroscopic margins via either partial-thickness excision (mucosectomy) or full-thickness excision to perirectal fat. The defects were closed transversely by using absorbable suture secured by a clip.

Data were abstracted from hospital and office medical records supplemented by prospectively collected tumor registry records. Further detail on polyp positional analysis with this data set has been reported.8 The presence of lesion at the margin of specimen, including cautery at the margin, was classified as a positive margin. Mucinous histological characteristics, poor differentiation, and lymphatic and/or vascular invasion were classified as high-risk pathology. Characterization of an upstaged pathologic diagnosis was based on an increase in severity of dysplasia or depth of invasion between the preoperative diagnosis and final pathology after excision by TEM. Local recurrence was defined as the presence of a neoplastic lesion in proximity to the site of previous TEM on follow-up colonoscopy or rigid sigmoidoscopy. Classification as adenocarcinoma included lesions with intramucosal carcinoma (Tis) and invasive carcinomas to the levels of the submucosa (T1), muscularis propria (T2), and perirectal tissues (T3). Conversions and pathology other than adenoma, adenocarcinoma, or carcinoid were excluded from follow-up analysis.

Statistical analysis was conducted with EpiInfo (Centers for Disease Control and Prevention, Atlanta, GA). Means are listed along with their standard deviations; medians are listed with their interquartile range (IQR). Statistical significance was determined with an {alpha} of .05 by using two-tailed P values. Nonparametric statistical analysis was performed by using {chi}2 and Mann-Whitney rank-sum tests. Kaplan-Meier analysis was used for determination of actuarial recurrence and survival probabilities, with use of the log-rank test for comparisons between groups. Cox proportional hazards analysis was used for the determination of age-adjusted cumulative survival rates. Multivariate analysis for independent predictors of recurrence and survival was performed in a Cox proportional hazards model with stepwise inclusion of variables: those with a minimum absolute normal statistic (z) were removed sequentially until only statistically significant independent variables of association remained. Hazard ratios, 5-year recurrence rates, and survival probabilities are listed with their 95% confidence intervals (CI). Actuarial recurrence rates did not include patients who underwent immediate radical surgery (e.g., for T3 disease). Actuarial survival rates comprised all patients with neoplastic disease, including those who underwent salvage surgery for recurrence. The study methodology received approval by the Baystate Medical Center Institutional Review Board (protocol 04–191).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Operative Characteristics
In the study period, 144 TEMs were attempted on 139 patients (Table 1Go). Patients had a mean age of 64 ± 14 (SD) years (range, 29–92 years), with a male:female ratio of 1.09. The preoperative diagnosis was adenoma in 109 (76%) cases, adenocarcinoma in 28 (19%), carcinoid tumor in 4 (3%), and other in 3 (2%). Endoscopic ultrasonography was used in 10 (36%) patients with a preoperative diagnosis of adenocarcinoma. Management of recurrent disease after prior piecemeal polypectomy or transanal excision was performed for 23 (21%) of 109 adenomas and 3 (11%) of 28 adenocarcinomas. The final pathologic diagnosis was adenoma in 90 (63%), adenocarcinoma in 44 (31%), carcinoid tumor in 4 (3%), and other in 6 (4%). Overall, the final pathologic diagnosis was unchanged in 107 (74%) cases (Table 1Go).


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  		TABLE 1. Pathologic classification of cases presenting for TEM by preoperative and final diagnosis
 
Lesions classified as "other" before surgery included an anastomotic stricture (from prior anterior resection) managed by neodymium–yttrium:aluminum:garnet laser ablation and stricturoplasties using TEM, and a fistula secondary to Crohn’s disease was managed by an intraluminal advancement flap using TEM. Patients classified as "other" after surgery also included those with a final pathological diagnosis of hemorrhoidal disease, endometriosis, and submucosal abscess. These patients were excluded from follow-up analysis.

Lesions were located at a distance of 9.3 ± 4.9 cm from the dentate line, with an average maximal dimension of 3.1 ± 1.4 cm. The median operative time for full-thickness and partial-thickness excisions was 82 minutes (IQR, 58–120 minutes), with a median hospital length of stay of 29 hours (IQR, 25–31 hours). Positive margins were noted in 13 (9%) specimens; only 1 of these represented a positive deep margin, which occurred in a patient with T3 disease on final pathologic analysis.

Full-thickness excision was completed in 94 (65%) cases. Mucosectomy was performed in 35 (24%) cases, primarily in proximal lesions to avoid peritoneal entry; this was reflected by a significant difference in the distance of lesions by depth of excision (partial thickness, 11.9 ± 4.7 cm; full thickness, 7.6 ± 3.5 cm; P < .0001). Conversion to low anterior resection occurred in eight (6%) cases secondary to difficult access to the lesion and lack of progress. Conversion to local transanal excision by the technique of Parks and Stuart9 occurred in two cases (1%) secondary to proximity to the anal verge and difficulty maintaining pneumorectum. Conversion to snare polypectomy was performed on one lesion that was noted to be pedunculated during TEM. Conversion to fine-needle aspiration occurred in one patient and confirmed lymph node metastasis; this was followed by APR by the primary surgeon.

Complications
Intraoperative complications included eight (6%) conversions to anterior resection, nine (6%) cases of peritoneal entry, one (<1%) equipment failure, one (<1%) difficult extubation, and two (1%) position changes. Peritoneal breach was managed during surgery by primary closure of the defect and did not necessitate conversion to open anterior resection. Postoperative complications included urinary retention in seven patients (5%), abdominal or rectal pain in two (1%), bleeding in two (1%), fluid overload in two (1%), suture line dehiscence in two (1%), perirectal abscess in one (<1%), and stricture in one (<1%). Overall, complications occurred in 10% of patients who completed formal TEM. There were no deaths related to the technique.

Among the patients with bleeding, one required a return to the operating room for urgent treatment. Among the patients with postoperative suture line dehiscence, one presented for excision of a recurrent villous adenoma with high-grade dysplasia (HGD) that recurred as an adenoma with HGD 9 months after TEM, despite negative margins. The patient also developed a rectal stricture and underwent a concurrent rectal dilation and transanal excision. Six years after TEM, the patient developed another recurrence at the surgical site and underwent a Kraske proctectomy,3 followed by APR after pathologic diagnosis of invasive cancer. The patient was alive at 115 months following initial TEM.

Among the patients with peritoneal breach, one had moderately differentiated T1 cancer on preoperative and final pathologic analysis. This patient developed a perirectal abscess 1 month after surgery. Endoscopy 15 months later confirmed an invasive recurrence, which was managed with neoadjuvant radiotherapy and APR (T3N1). The patient was alive 35 months after the initial TEM.

Management and Outcomes
Table 2Go summarizes the lesion characteristics, management, and local recurrence for 127 patients who completed formal TEM with a pathologic diagnosis of adenoma, adenocarcinoma, or carcinoid. The median follow-up was 44 months (IQR, 23–74 months). Metachronous lesions were discovered in 14 (17%) of 82 patients with adenoma and 3 (7%) of 41 patients with adenocarcinoma. Open or laparoscopic segmental colonic resection for metachronous or synchronous colonic polyps was performed in four (5%) patients with adenoma and two (5%) patients with cancer. Sigmoid colectomy for diverticular disease was performed in two (2%) patients with adenoma and one (2%) patient with adenocarcinoma.


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  		TABLE 2. Characteristics and outcomes of lesions excised by TEM (n = 127)
 
Neoplastic local recurrence occurred in 12 (15%) of 82 adenomas and 6 (15%) of 41 adenocarcinomas (Table 3Go). Invasive local recurrence occurred in 2 (2%) of 82 adenomas and 4 (10%) of 41 adenocarcinomas. The median time until recurrence was 14 months (IQR, 12–46 months) for adenomas and 15 months (IQR, 13–18 months) for adenocarcinomas. Depth of invasion was related to the likelihood of invasive local recurrence (P = .04). Lesions ≥4 cm had a higher rate of recurrence (27% vs. 10%; P = .02). Among index lesions that were adenomas, prior lesion recurrence after formal polypectomy or transanal excision was significantly associated with the risk of recurrence (32% vs. 10%; P = .02). Only one case of recurrence occurred from a lesion that had positive margins; this patient had HGD on initial pathologic analysis that recurred as an adenoma with HGD. All benign recurrences without HGD were amenable to primary colonoscopic resection.


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  		TABLE 3. Characteristics of index lesions that developed neoplastic recurrence (n = 18)
 
Actuarial recurrence and survival probabilities at 5 years are reported in Table 4Go. No statistical difference was seen in overall neoplastic recurrence rates for adenoma and cancers (18% vs. 20% at 5 years; P = .76; Fig. 1Go). Five-year invasive recurrence rates were 0% for adenomas without HGD, 15% for adenomas with HGD, and 13% for adenocarcinomas (P = .01). After multivariate analysis, independent predictors of recurrence were HGD within adenomas (hazard ratio, 4.1; 95% CI, 1.3–13.4; P = .02) and the maximal dimension of the lesion (hazard ratio, 1.7 cm–1; 95% CI, 1.2–2.3 cm–1; P = .005). A history of recurrence of the index lesion after prior formal polypectomy or transanal excision approached significance as a predictor of recurrence (hazard ratio, 2.7; 95% CI, 1.0–7.6; P = .05).


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  		TABLE 4. Kaplan-Meier 5-year recurrence and survival probabilities for patients undergoing TEM
 

Figure 1
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  		FIG. 1. Recurrence-free probability by lesion pathology after local excision with transanal endoscopic microsurgery (P > .05).

 
Actuarial survival at 5 years was 93% for adenoma and 83% for adenocarcinoma (P = .11; Fig. 2Go). The age-adjusted 5-year cumulative survival was 94% for adenoma and 88% for adenocarcinoma. The cancer-specific mortality for adenocarcinoma was 9% at 5 years. After multivariate analysis, the only independent predictors of survival were age (hazard ratio, 1.1 per year; 95% CI, 1.0–1.2; P = .01) and sex (hazard ratio, 5.8; male vs. female; 95% CI, 1.2–27.5; P = .03).


Figure 2
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  		FIG. 2. Overall survival probability by lesion pathology after local excision with transanal endoscopic microsurgery (P > .05).

 
Cancer Outcomes
On final pathologic analysis, all patients with cancer had well or moderately well differentiated disease. The one T1 patient with mucinous histological characteristics underwent adjuvant chemoradiotherapy with 5-fluorouracil and is without evidence of disease after 79 months’ follow-up. The only T1 case with positive margins had moderate differentiation; this patient refused further treatment and is alive after 58 months. The one T1 patient with vascular invasion had a benign villous recurrence at the resection site after 14 months.

The two T1 benign recurrences include the aforementioned case and another patient with a tubular adenoma at the resection site excised at a 1-year follow-up colonoscopy, with no further disease at 59 months. The two T1 cancerous recurrences include the case of complicated peritoneal breach and abscess, as well as a case of well-differentiated T1 disease that recurred 24 months after TEM. This patient underwent APR for T3N0 disease and died of metastatic disease 2 years later.

Patients with T2 disease on final pathologic analysis were offered further treatment with adjuvant radiotherapy. The one patient with positive margins had moderate differentiation and lymphatic invasion; this patient received adjuvant radiotherapy and survived to 85 months after TEM. Another patient received chemoradiotherapy and remains disease free after 64 months. A third patient received radiotherapy but then experienced disease recurrence after 18 months; this patient proceeded to salvage APR and is alive at 26 months. The fourth patient received adjuvant chemoradiotherapy but experienced disease recurrence after 10 months. This patient went on to APR followed by intensity-modulated radiotherapy and is disease free at 38 months after TEM.

Patients with T3 disease were offered immediate radical surgical resection. One T3 patient with lymphatic invasion had chemoradiation before formal surgery and is alive at 17 months. Another patient had positive deep margins and mucinous histology and was confirmed to have lung metastasis on pulmonary lobectomy. This patient underwent APR (T3N1M1) followed by radiotherapy and had further evidence of metastatic disease at 60-month follow-up. Another patient with moderate differentiation underwent APR and is without evidence of disease at 123 months. A fourth T3 patient, despite positive margins, declined radical surgery secondary to age (88 years), choosing radiotherapy only, and remains without evidence of disease after 45 months. The fifth T3 patient proceeded to anterior resection and died of metastatic disease at 32 months.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Local excision of rectal tumors has evident benefits over transabdominal surgical approaches such as APR and anterior resection, including less morbidity; maintenance of anorectal, sexual, and bladder function; and less operative mortality.1,10 In the case of adenoma, it is difficult to argue against techniques that favor sphincter preservation. However, a curative resection for cancer necessitates adequate lymph node dissection to prevent associated recurrence of disease and the potential for decreased survival. Unfortunately, local excision renders an inability to adequately stage the patient because lymph nodes are not taken with the specimen. Careful patient selection is thus necessary to provide patients with a procedure with a satisfactory outcome according to oncological principles.

Gall11 has outlined four salient points that should be considered regarding local excision versus radical resection of rectal cancer: (1) the risk of lymph node metastasis, (2) the risk of local recurrence, (3) the risk of operative mortality, and (4) the risk of compromised anorectal function. It is critical to select patients at low risk of lymph node metastasis and recurrence to reap the benefits of the lower rate of morbidity and mortality associated with local excision. Lymph node metastasis has been reported in 3% to 17% of T1 cancers12–16 and is found in 52% of tumors <5 cm.16 Features that increase the risk of lymph node metastasis include poor differentiation, vascular invasion, and depth of invasion.17 Low-risk T1 lesions (well or moderately well differentiated and without lymphatic invasion) carry a 5% risk of lymph node metastasis, compared with 27% for high-risk lesions.11

In this study, we demonstrated the outcomes of treatment of neoplastic disease after local excision with TEM. Both adenomas and adenocarcinomas were included in the analysis to provide a comprehensive spectrum of the pathology addressed by TEM at our institution. Inherent in this study is a significant selection bias associated with referral patterns, lesion characteristics, and the premorbid conditions of the patients. Preoperative staging with endoscopic ultrasonography was also limited during the study interval; it was performed in only 36% of patients with a preoperative diagnosis of adenocarcinoma. This infrequent use may contribute to the discrepancies seen between preoperative and final diagnoses; despite this, two cases of submucosal invasion diagnosed by endoscopic ultrasonography were ultimately upstaged on final pathologic analysis.

In our series of adenomas, a selection bias was demonstrated for more severe disease, because TEM was performed on sessile lesions with villous or tubulovillous histological characteristics that were not amenable to primary colonoscopic excision. We can accurately classify all the adenomas in this series as advanced adenomas, as defined by the presence of HGD, size >1 cm, or appreciable villous tissue.18 Such lesions have an increased risk of invasion and are recommended for postexcision colonoscopy within 3 years rather than 5 years. Furthermore, sessile polyps >2 cm excised colonoscopically have been suggested to warrant follow-up colonoscopy in 3 to 6 months to ensure complete resection.19 Indeed, this series demonstrated a median time to recurrence that was <2 years, even with the benefit of resection in continuity (i.e., nonpiecemeal excision).

The Polyp Prevention Trial had 750 (40%) recurrences from 1889 baseline adenomas, and advanced adenomas comprised 16% of cases. Polyp size or HGD did not predict recurrence, which was related more to age, anatomical region, and villous histological characteristics.20 However, the National Polyp Study correlated HGD with size, villous component, and lesion multiplicity and suggested HGD as a marker for malignant potential.21 Multivariate analysis within our study confirmed HGD within adenoma and size as independent predictors of local failure. Furthermore, the analysis suggests a trend in which previously recurrent polyps contribute to a greater risk of subsequent recurrence. Close follow-up is warranted with such lesions.

In a review of endoscopic polypectomies (70% piecemeal) for colonic lesions >2 cm, persistence of the lesion at the first follow-up was 22%, with polyp recurrence rates of 0% to 55% and polypectomy complication rates of 1% to 9% (primarily bleeding).22 Polyp persistence was related to the size of the index lesion. Furthermore, among endoscopically excised sessile polyps >3 cm, 22% required management over three or more sessions.23 In comparison, our series of TEM had favorable outcomes, with a 16% 5-year recurrence probability for adenomas (15% crude rate for all adenomas excised).

TEM offers considerable technical advantages over transanal excision, with stereoscopic magnification, better instrumentation, and improved access to proximal lesions.24,25 Published studies on TEM outcomes report complication rates of 2% to 32% and recurrence rates of 0% to 15% for benign disease and 0% to 50% for malignant disease (Table 5Go).5,26–43 Unfortunately, these studies are heterogeneous, and many have follow-up data of short duration (mean, 29 months; range, 7–43 months). Table 6Go summarizes the composite complication and recurrence rates among these series and the present series.


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  		TABLE 5. Published series of transanal endoscopic microsurgical outcomes for benign and malignant rectal disease
 

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  		TABLE 6. Composite rates of TEM outcomes from the present and published series5,26–43
 
Results from our patients with adenocarcinoma are similar to those in the TEM literature providing time-to-event analysis. Stipa et al.43 reported recurrence rates after TEM of 0% for Tis, 13% for T1, 17% for T2, and 50% for T3 disease, with respective 5-year survival rates of 100%, 92%, 75%, and 69%. In a study comparing TEM with radical surgery for stage I disease, complication rates of 5% vs. 48%, 5-year local recurrence rates of 4% vs. 0%, and 5-year cancer-free survival rates of 96% vs. 94% were obtained.33 Another study comparing TEM with radical surgery for T1 disease reported complication rates of 3% for TEM versus 18% for radical surgery; those classified as low risk had respective 5-year survival rates of 79% and 81%, whereas those with high risk had respective survival rates of 62% and 69%. Local recurrence after TEM occurred in 4% of patients with low-risk disease versus 33% of those with high-risk disease.30 The only prospective randomized trial for TEM versus anterior resection found early complications in 21% vs. 35% of patients and late complications in 8% vs. 23%.5 The TEM group had one local recurrence (4%), whereas the anterior resection group had one patient die from distant metastasis (4%); the 5-year survival probability was 96% for both groups.

A systematic review of 10 historical series of transanal local excision for rectal cancer demonstrated 5-year survival rates of 69%, cancer-specific 5-year survival rates of 94%, and local recurrence rates of 19%.10 In recent years, outcomes for local excision of T1 disease have been questioned, with local recurrence rates of 5% to 28% after follow-up of 33 to 72 months.14,44–51 Paty et al.51 reported actuarial local recurrence rates of 14% and survival of 92% at 5 years for T1 disease without adjuvant therapy. Madbouly et al.48 recently reported 5-year actuarial local recurrence of 29% and survival of 75% for T1 disease. Among T1 and T2 cancers <4 cm, the Cancer and Leukemia Group B and collaborators found 6-year recurrence and survival rates of 22% and 85%, respectively.52 In a comparison of local excision with oncological resection of low and mid rectal T1 cancers, Nascimbeni et al.50 demonstrated respective 5-year local recurrence rates of 7% vs. 3% and survival rates of 72% vs. 90%.

Mellgren et al.49 also compared patients undergoing local excision with radical surgery for T1 and T2 disease. They demonstrated respective 5-year local recurrence rates of 28% vs. 4%, 5-year overall survival rates of 69% vs. 82%, and 5-year cancer-specific survival rates of 90% vs. 92%. It seems that despite the higher rate of local recurrence attributed to local excision, recurrences may be dealt with by using salvage procedures that offer a similar overall survival benefit. However, their study did show a significant difference in survival for T2 tumors between local excision and radical surgery (65% vs. 81%). Transanal excision of T2 tumors has associated local failure rates of 28% to 47%.45,46,49,51 Although this study demonstrated no deaths within 5 years for T2 patients after adjuvant radiotherapy (n = 4), 50% required salvage therapy for local recurrence. Conclusions about T2 disease are uncertain because of heterogeneity in treatment, patient comorbidity, and low numbers, but with knowledge of the increased rate of lymph node metastasis in T2 disease, one can easily argue against performing local excision with a depth of invasion beyond the submucosal layer. Until further study on the role of neoadjuvant therapy in local excision proves a benefit, local excision of lesions advanced beyond submucosal invasion should not be performed with the intent to cure and should be reserved for patients with a high risk of operative morbidity and mortality.

In summary, TEM provides acceptable outcomes in the local management of benign and malignant disease, with a shorter operative time and hospital length of stay and fewer complications than radical surgery. In the case of cancer, TEM should be limited to small lesions with invasion up to the submucosal level. Close endoscopic follow-up is necessary for patients with both benign and malignant disease, especially for lesions with HGD. TEM should be limited to lesions <4 cm, with vigilance in the management of previously recurrent lesions. Pathologic criteria for a low risk of lymphatic metastasis (good or moderate differentiation, without lymphatic invasion, and without mucinous components) should be adhered to when the technique is performed for curative intent.


   ACKNOWLEDGMENTS
 
The authors thank Anne Krasnecky, Judi Bush, and Veronica Hilbert for their assistance in record acquisition, as well as Richard B. Arenas, MD, and Thomas G. Magill, MD, for many valuable discussions. Funding for the TEM apparatus (Richard Wolf, Knittlingen, Germany) was supported through the Marjory Sandowsky Cancer Research Grant.


   FOOTNOTES
 
Presented at the Society of Surgical Oncology, 58th Annual Cancer Symposium, Atlanta, Georgia, March 3–6, 2005.

Received for publication April 19, 2005. Accepted for publication October 12, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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