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10.1245/ASO.2005.03.044
Annals of Surgical Oncology 12:111-116 (2005)
© 2005 Society of Surgical Oncology
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Original Article

Relationship Between Pathologic T-Stage and Nodal Metastasis After Preoperative Chemoradiotherapy for Locally Advanced Rectal Cancer

Salvatore Pucciarelli, MD1, Carlo Capirci, MD2, Urso Emanuele, MD1, Paola Toppan, MD1, Maria Luisa Friso, MD3, Gian Maria Pennelli, MD4, Giovanni Crepaldi, MD2, Lara Pasetto, MD5, Donato Nitti, MD1 and Mario Lise, MD1

1 Clinica Chirurgica II, Dipartimento di Scienze Oncologiche e Chirurgiche, Universitá di Padova, Padova, Italy
2 Servizio di Radioterapia and Oncologia Medica, Ospedale Civile di Rovigo, Italy
3 Divisione di Radioterapia, Azienda Ospedaliera di Padova, Padova, Italy
4 Istituto di Anatomia Patologica, Dipartimento di Scienze Oncologiche e Chirurgiche, Universitá di Padova, Padova, Italy
5 Divisione di Oncologia Medica, Azienda Ospedaliera di Padova, Padova, Italy

Correspondence: Address correspondence and reprint requests to: Salvatore Pucciarelli, MD; E-mail: puc{at}unipd.it.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: We investigated the relationship between pathologic T-stage and mesorectal metastases after preoperative chemoradiotherapy (CRT) for clinical stage II to III rectal carcinoma.

Methods: The records of consecutive patients with clinical stage II to III carcinoma of the mid or low rectum who underwent surgery after CRT were reviewed. Indications for preoperative CRT were cancer up to 11 cm from the anal verge, Eastern Cooperative Oncology Group performance status of 0 to 2, age 18 to 75 years, and clinical tumor-node-metastasis stage II or III.

Results: The study group consisted of 235 patients (148 men and 87 women; median age, 61 years). The pretreatment tumor-node-metastasis stage was as follows: I, n =1; II, n =96; and III, n = 138. Radiotherapy was delivered at a median dose of 50.4 Gy. A pathologic complete response on the rectal wall was found in 24% of patients, and nodal metastases were found in 20% of patients. According to the pT stage, the rate of node positivity was 2% for pT0, 15 % for pT1, 17 % for pT2, 38 % for pT3, and 33% for pT4 cases. At multivariate analysis, the best model for predicting pathologic node involvement included young age, positive pretreatment N status, and pT status. On considering pT stage alone, the odds ratio was in the region of 10 for pT1/2 and >20 for pT3/4 patients.

Conclusions: In patients with pT0 after preoperative CRT for clinical stage II to III mid or low rectal cancer, the risk of nodal metastases is very low. More conservative surgery (local excision) may be considered in these cases.

Key Words: Rectal cancer • Surgery • Radiotherapy • Chemotherapy • Adjuvant treatment


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Preoperative chemoradiotherapy (CRT) is now considered one of the standard treatment modalities for locally advanced rectal cancer. The potential advantages of preoperative CRT are both downsizing and downstaging of the tumor. A pathologic complete response (pCR) after this approach has been found in 4% to 44% of cases.1–5 Although a clear trend toward a better outcome has been reported for "responder" compared with "nonresponder" patients, 6–8 factors involved in tumor response and the effect of pCR on outcome are still a matter of debate. Moreover, tumor response can affect surgical treatment, allowing a higher percentage of sphincter-saving procedures and, for patients with a clinical complete response, even more conservative approaches. Encouraging results in terms of local recurrence and survival have been reported with either observation9 or a nonradical approach (i.e., transanal full-thickness local excision).10,11 The main concern regarding the observational approach is related to the wide discrepancy between clinical and pCR rates. Residual tumor is found at histology in up to 75% of cases considered complete responses at digital rectal examination and proctoscopy.12 The rationale for the nonradical approach is based on the assumption that, after preoperative CRT, the risk of residual cancer in the mesorectum is very low. However, this issue has been poorly investigated. The aim of this study was therefore to evaluate, in a large series of patients, the relationship between pathologic T-stage and lymph node status and factors that predict pathologic lymph node status after preoperative CRT.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patient Selection
A review was made of the records of 248 consecutive patients with locally advanced primary carcinoma of the mid or low rectum who, from 1994 to 2003, underwent surgery after CRT. Pretreatment staging included clinical history and physical examination, proctos copy with or without colonoscopy, chest radiograph, liver and transrectal ultrasound, pelvic computed tomography, and carcinoembryonic antigen assessment. At preradiation staging, lymph nodes >5 mm were considered positive.11,13 Patients who underwent local excision (n = 4) after preoperative CRT or non–5-fluorouracil (5-FU)–based CRT (n = 5) and those without reliable data on histopathology or the preoperative CRT regimen used (n=4) were excluded from the study. The study group thus comprised the remaining 235 patients.

Treatment
Criteria used for giving preoperative CRT were (1) biopsy-proven adenocarcinoma up to 11 cm from the anal verge; (2) preoperative stage T3/4, node-positive disease, or both; (3) age ≤75 years; and (4) an Eastern Cooperative Oncology Group performance status of 0 to 2. Although all patients received external beam radiotherapy (RT) with concomitant 5-FU–based chemotherapy followed by surgery with a curative intent, various therapeutic regimens were used in relation to the study period, the enrollment of patients in clinical trials, and differences in chemotherapy regimens administered by the referring oncologists.

Chemoradiation
External beam RT was delivered in fractions of 1.5 to 1.8 Gy/day by using the three-field or box technique. 5-FU, as a single drug or in combination with others (leucovorin, carboplatin, or oxaliplatin), was administered by bolus or continuous venous infusion (CVI). In most cases, two standard regimens were used during the study period: (1) Initially, 5 -FU was administered by bolus (5-FU 350 mg/m2/day) with a low-dose leucovorin bolus (10 mg/m2/day) for 5 days on days 1 to 5 and 29 to 33 together with RT (45 Gy in 25 fractions). (2) More recently, 5-FU was administered by CVI (225–300 mg/m2/day) throughout RT, which was delivered at doses of 50.4 Gy in 28 fractions. More details on the RT techniques are given elsewhere.2 Although we advocate routine postoperative chemotherapy (usually four to six cycles of 5-FU 375 mg/m2/day and leucovorin 100 mg/m2/day; bolus on days 1 to 5 every 28 days) irrespective of the pathologic stage, in several cases adjuvant chemotherapy was not administered.

Surgery
Surgery was planned 6 to 8 weeks after completion of preoperative CRT, and standard total mesorectal excision was usually performed. The surgical technique is described elsewhere.2,14 As a rule, the inferior mesenteric artery was divided at its origin, an d standard lymphadenectomy was performed. The mesorectum was completely removed by using sharp dissection in the avascular planes between the fascia propria and parietal tissue under direct vision.

Assessment of Pathologic Response
Most surgical specimens were assessed with the protocol of Quirke et al.15 Moreover, a single pathologist who was unaware of outcomes reviewed most of the pathologic archival material and reported findings according to the American Joint Committee on Cancer tumor-node-metastasis classification.16 A pCR was defined as the absence of viable tumor cells at histology of the surgical specimen, and pure acellular mucin was considered "no residual tumor."17

Follow-Up
Patients were examined at routine follow-up examinations (3, 6, 1 2, and 18 months after surgery and then yearly). At each follow-up visit, the carcinoembryonic antigen level was determined, and liver ultrasound and sigmoidoscopy were performed. A chest radiograph and colonoscopy were performed yearly. Recurrence in the pelvis was considered local, and recurrence outside the pelvis was considered distant.

Statistical Analysis
The associations between categorical variables were analyzed with {chi}2 or Fisher’s exact tests, as appropriate, and associations with continuous variables were analyzed by using the Kruskal-Wallis test. To find independent factors predictive of pathologic lymph node status, multivariate analysis was performed by using logistic regression analysis and the stepwise procedure. A P value of <=.05 was considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient and Tumor Characteristics
The study group consisted of 235 patients (148 men and 87 women; median age at surgery, 61 years; range, 31–81 years). The median distance of the tumor from the anal verge was 6 cm (range, 1–11 cm). The pretreatment cT stage was as follows: 2, n = 11 (4.7%); 3, n = 186 (79.1%); and 4, n = 37 (15.7%). The cT stage was not available in one case (.4%). Lymph nodes were staged as negative in 96 (40.9%) cases and positive in 139 (59.1%). The pretreatment tumor-node-metastasis stage was as follows: I, n = 1 (.4%); II, n = 96 (40.9%); and III, n = 138 (58.7%).

Treatment
Patients received RT at 11 radiotherapy departments, but 221 (94%) of 235 received RT at two institutions. Likewise, surgical procedures were performed at 15 surgical units, but 151 (64%) of 235 patients underwent surgery at a single institution. External beam RT was delivered at a median dose of 50.4 Gy (range, 40–60 Gy); 177 (75%) patients received >50 Gy. 5-FU, administered by bolus in 60 (26%) patients and by CVI in 175 (74%) patients, was the only drug given in 140 (60%) cases; in the remaining 95 (40%) patients, it was associated with leucovorin, carbopla tin, and oxaliplatin in 50 (21%), 19 (8%), and 26 (11%) cases, respectively. The median interval between the completion of CRT and surgery was 51 days (range, 9–136 days). A sphincter-saving procedure was performed in 198 (84%) cases: low anterior resection with colorectal (n = 158; 67%) or coloanal (n = 36; 15%) anastomosis and Hartmann’s procedure (n = 4; 2%). The remaining 37 (15%) patients underwent abdominoperineal resection. Surgery was considered radical in 212 (90%) patients. Resections were considered nonradical in 23 cases: 16 patients with unsuspected distant metastases and 3 with macroscopic and 4 with microscopic residual tumor. One hundred six (45%) patients received postoperative adjuvant chemotherapy.

Factors Predictive of Positive Pathologic Lymph Node Status
Of the 235 cases included in the study, 151 were assessed with a standardized protocol,15 and 148 of these were reviewed by 1 pathologist. The mean number of lymph nodes retrieved from the surgical specimen was 9 (range, 0–38). A statistically significant association was found between positive lymph node status at histology and the following variables: age (P = .038), interval between completion of CRT and surgery (P = .039), and pT stage (P < .001).

The mean age was 58.6 years for patients with positive lymph nodes and 61.7 years for those with negative lymph nodes. The mean interval between completion of preoperative CRT and surgery was 50.3 and 57 days in lymph node–positive and lymph node–negative patients, respectively. A pCR was found in 56 patients (23.8%). The distribution of the remaining cases was as follows: pT1, n = 13 (5.5%); pT2, n = 83 (35.3%); pT3, n = 74 (31.5%); and pT4, n = 9 (3.8%). Overall, mesorectal lymph node metastases were found in 48 (20.4%) patients. According to the pT stage, the percentages for node positivity were 1.8% for pT0 (n = 56), 15.4 % for pT1 (n = 13), 16.9 % for pT2 (n = 83), 37.8 % for pT3 (n = 74), and 33.3% for pT4 (n = 9) (Table 1Go). Pathologic tumor-node-metastasis stage was as follows: 0 (pCR), n = 55 (23.4%); I, n = 78 (33.2%); II, n = 47 (20%); III, n = 40 (17%); and IV, n = 15 (6.4%).


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  		TABLE 1. Relationship between pathologic T-stage and N-stage in 235 cases
 
At multivariate analysis, the best model for predicting pathologic lymph node involvement included age, clinical pretreatment N-status, and pT status (Table 2Go). Young patients with pretreatment positive nodes and a higher pathologic T-stage had a greater probability of harboring metastatic mesorectal lymph nodes. Regarding pT stage, the odds ratio was approximately 10 for pT1 and pT2 patients and was >20 for pT3 and pT4 patients.


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  		TABLE 2. Factors predictive of lymph node involvement at multivariate logistic regression analysis and stepwise procedures
 
Outcome
The median follow-up was 28 months (range, 0–114 months). Among 212 patients who underwent radical surgery, recurrences were found in 25 (11.8%) patients; 22 recurrences were distant, and 3 (1.4%) were local and distant. Six of the 25 recurrences occurred in pT0 patients, and 1 of the 3 local recurrences was found in the 1 patient with a pT0N1 stage. Data on overall survival were available in 234 cases: 188 patients were alive and disease free, 10 were alive with disease, and 36 had died (3 after surgery, 27 of cancer-related causes, and 6 of other causes). Because follow-up was short and the number of events small (recurrences and deaths), survival curves were not estimated.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Radical surgery with either abdominoperineal resection or low anterior resection remains the standard treatment for most patients with mid or low rectal cancer. However, it is associated with significant mortality and morbidity. A large multicentric study conducted with the total mesorectal excision technique reported a mortality rate of 3.3%, an overall morbidity rate of 41%, and a reintervention rate of 13.6%.18 Moreover, urinary dysfunction occurs in 10% to 70% of patients, sexual dysfunction in 13% to 70%, and anastomotic leakage in 5% to 17%.14,19–23 Full-thickness transanal local excision, a much less invasive surgical option, incurs no mortality and negligible morbidity and is now considered an acceptable surgical alternative for T1 rectal adenocarcinoma that measures <4 cm, is well or moderately well differentiated, and has no lymphovascular invasion or mucinous aspects.24 In view of the high risk of lymph node metastases in the mesorectum, full-thickness transanal local excision is considered a nonradical surgical procedure and is contraindicated for T1 lesions with poor prognostic indicators and for pT2–4 tumors. In rectal cancer patients not given neoadjuvant therapy, the risk of nodal metastasis increases with T-stage, ranging from 0% to 12% for pT1, 12 % to 28% for pT2, and 36% to 79% for pT3/4 tumors.25–28

In recent years, preoperative CRT has been used increasingly often for locally advanced mid or low rectal cancer, and a pCR is achieved in up to 44% of cases.1–5 However, the effect of tumor response on both outcome and surgical treatment has been poorly investigated. Whatever the clinical response, radical abdominal surgery is still considered the standard procedure. However, for patients with a clinical complete response after CRT, some authors advocate an observational approach, 9 whereas others suggest that the full-thickness transanal local excision approach is appropriate.10,11 The rationale for these "alternative" approaches is based on the assumption that, after CRT, there is a close association between a clinical complete response and pCR and that the risk of mesorectal lymph node metastases is low in responders. However, the discrepancy between clinical complete response and pCR is great, ranging from 25% to 77%11,12; this suggests that the clinical evaluation of complete response by using the current staging methods is still inaccurate. Moreover, preoperative CRT induces many morphological modifications, and microscopic residual adenocarcinoma foci may be overlooked by the pathologist even if the surgical specimen is carefully evaluated. Thus, a low rate of positive nodes can be expected in multicentric retrospective studies. The overall rate for positive lymph nodes after preoperative CRT was 20% in our study. This is similar to the percentages of 24% and 25% reported by other authors.12,29 Moreover, in our series, the percentage of patients with positive lymph nodes was only 1.8% in those with a pCR on the rectal wall (pT0); this percentage was still low (3.5%) in the 148 cases that were evaluated by one pathologist using a standardized protocol.

These findings are comparable to those reported by Grann et al.30 and Theodoropoulos et al.3 but are different from those of other authors,12,29,31 who have reported percentages ranging from 9% to 16%. Our finding can be considered reliable in view of the standardized pathologic examination of the surgical specimen used and the number of lymph nodes retrieved. This seems appropriate in view of the facts that patients received preoperative CRT and that the review of 148 specimens was performed by one pathologist. However, histopathologic accuracy is only one variable; others with a potential effect on lymph node status are preoperative CRT regimens used, pretreatment stage (pretreatment N-stage was found to be an independent variable associated with pathologic N-status in our study), and the interval between completion of RT and surgery. In our study, pT stage was the stronger predictor of pathologic lymph node status at both univariate and multivariate analysis.

Our findings and those of other authors12,30 suggest that, be cause the risk of leaving mesorectal disease after CRT is too high for patients with residual tumor on the rectal wall, the use of nonradical surgical resection it is not justified in patients with pT1 to pT4 tumors. However, it seems justified to consider a nonradical surgical approach (full-thickness local excision) for patients with T0 lesions. Thus, full-thickness transanal excision should be considered primarily an excisional biopsy, an d, as yet, it is the only reliable method available to distinguish between patients with and without pCR after preoperative CRT.

In conclusion, in this large retrospective series of patients with locally advanced mid or low rectal cancer who received preoperative CRT, the main finding was a low rate of positive lymph node metastases (1 of 56; 1.8%) in cases with a pCR on the rectal wall (pT0). This finding may be the rationale for prospective trials investigating more conservative surgery for patients who are given preoperative CRT and who present a pCR on the rectal wall after full-thickness local excision.


   ACKNOWLEDGMENTS
 
The authors thank Alessandro Ambrosi for the statistical analysis and Sara Pearcey for her assistance with the English language.


   FOOTNOTES
 
Presented at the 57th Annual Cancer Symposium of the Society of Surgical Oncology, New York, New York, March 18–21, 2004.

Received for publication March 18, 2004. Accepted for publication October 1, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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