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10.1245/s10434-006-9171-0
Annals of Surgical Oncology 14:462-469 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Prognostic Significance of Circumferential Resection Margin Following Total Mesorectal Excision and Adjuvant Chemoradiotherapy in Patients with Rectal Cancer

Seung Hyuk Baik, MD1, Nam Kyu Kim, MD1, Young Chan Lee, MD1, Hoguen Kim, MD2, Kang Young Lee, MD1, Seung Kook Sohn, MD1 and Chang Hwan Cho, MD1

1 Department of Surgery, Yonsei University College of Medicine, Seoul, South Korea
2 Department of Pathology, Yonsei University College of Medicine, Seoul, South Korea

Correspondence: Address correspondence and reprint requests to: Nam Kyu Kim, MD, 134 Shincheondong, Seodaemun-ku 120-752, Seoul, South Korea; E-mail: namkyuk{at}yumc.yonsei.ac.kr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background: This study was designed to evaluate the prognostic value of circumferential resection margin (CRM) in rectal cancer patients who underwent curative resection with adjuvant chemoradiotherapy (CRT).

Methods: We studied 504 patients who underwent total mesorectal excision with adjuvant CRT for rectal cancer between 1997 and 2001. The patients were divided into two groups: a negative CRM group (CRM > 1 mm) and a positive CRM group (CRM ≤ 1 mm). The survival rates, local recurrence rates, and systemic recurrence rates were compared between groups.

Results: The negative CRM group had 460 patients and the positive CRM group had 44 patients. The 5-year local and systemic recurrence rates were 11.3 and 25.3%, respectively, in the negative CRM group and 35.2 and 60.8% in the positive CRM group, respectively. The cancer-specific 5-year survival rates for the two groups were 72.5 and 26.9% (P < .001), respectively. CRM was found to be an independent prognostic factor by multivariate analyses which were adjusted for known outcome predictors (P < .001).

Conclusion: Oncological outcome for patients in the positive CRM group is less favorable than for those in the negative CRM group. Adjuvant CRT is not a definite treatment modality that can be used to compensate for a positive CRM following TME and adjuvant CRT in patients with TNM stage II or III rectal cancer.

Key Words: Circumferential resection margin • Total mesorectal excision • Rectal cancer • Adjuvant chemoradiotherapy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Local recurrences are extremely painful and further salvage surgery has limited success in a rectal cancer patients. Conventional rectal surgery, either by abdominoperineal resection or low anterior resection, is associated with a high local recurrence rate.1–3

In 1979, the procedure now known as a total mesorectal excision (TME) was introduced.4 This procedure was developed with an awareness of the importance of complete excision of the rectal proper fascia surrounding the mesorectum using direct visualization. TME is now generally accepted as the surgical procedure of choice. Heald et al.5 and Enker et al.6 reported low local recurrence rates in patients with rectal cancer after TME. However, as rates of 5–10% have been reported, local recurrence after TME still remains an important problem.6–8 Salvage operations for recurrent rectal cancer is technically very difficult and the oncological outcomes are unfavorable. Thus, to reduce local recurrence rates after TME, radiotherapy has been given either pre- or post-operatively.9,10

From the many known prognostic factors for rectal cancer after TME, tumor involvement of the circumferential resection margin (CRM) appears to be a strong prognostic factor for local or systemic recurrences and survival after surgery.11–13 The CRM is prognostically significant and neoadjuvant radio-therapy has a beneficial effect in patients with inadequate CRM.14 However, previous studies have not discussed in detail the oncological results in relation to the positive CRM in patients who underwent adjuvant chemoradiotherapy (CRT). Therefore, the aim of this study was to compare the oncological significance of positive and negative CRM in patients who underwent adjuvant CRT.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Between 1 January 1997 and 31 December 2001, 696 patients underwent curative resections for rectal cancer in Severance Hospital at the Yonsei University College of Medicine. Curative resections were defined as those in which the surgeon was confident that all macroscopic tumors had been removed and those in which there was no evidence of metastatic spread during the operation or on preoperative computed tomography (CT), or magnetic resonance images (MRI) of other body sites. For pre-operative staging, all patients were evaluated using CT scans, pelvic MRIs, and transrectal ultrasonographies (TRUS).

Patients with TNM cancer stages15 I, IV (147 patients) and patients who underwent neoadjuvant chemoradiation (45 patients) were excluded from this analysis (Fig. 1Go). The clinicopathological data from these patients were accumulated prospectively and the data of final study group were analyzed. This study was approved by the institutional review board of our hospital.


Figure 1
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  		FIG. 1. Flow chart of the selection process for the study group. CRM, circumferential resection margin; TME, total mesorectal excision; TNM, tumor, lymph node, metastasis.

 
Patients underwent adjuvant CRT as recommended by the National Institute of Health Consensus Conference in 1990.16 Chemotherapy based on 5-FU (450 mg/m2 for 5 days) and leucovorin (20 mg/m2 for 5 days) was given intravenously each month with six cycles. Radiation therapy was performed after the second chemotherapy treatment and consisted of 5,400 cGY delivered (as 6 MV/ 10 MV dual photon linear accelerator) in 30 fractions of 180 cGY each, five times weekly to the pelvis, with individually shaped portals and using a four-field box technique.

Clinical follow-up data were obtained from our institute’s colorectal cancer database. Patients were followed up at 3 months intervals during the first 3 years, at 6 months intervals from the fourth and fifth years and thereafter annually for life. Medical histories, physical examinations, and blood tests with serum carcinoembryonic antigen were performed. Digital rectal examination was performed on all out-patients for detecting local recurrences. CT and whole body bone scan were checked every year. Local tumor recurrences or systemic tumor recurrences were identified clinically by tissue diagnosis, where possible, or by CT or MRI. Positron emission tomography was used where possible.

All patients underwent surgery which was performed by qualified colorectal surgeons in our institute in accordance to the TME principle. Mobilization of the rectum was performed with sharp dissection by direct visualization so that the visceral pelvic fascia, which enclosed the mesorectum, was kept intact. TME was defined as the transection of the rectum at the level of the pelvic floor with the entire mesorectum intact. This procedure was performed for patients with mid and distal rectal cancer. For tumors in the upper rectum, transection of the rectum and mesorectum 4–5 cm below the lower border of the tumor was performed following sharp perimesorectal dissection.

Pathological data was collected on all 504 patients and was reviewed for stage, adjacent organ involvement, the reporting pathologists’ comments on CRM involvement, and the shortest distance between the CRM and the tumor. Standardized pathology examinations were performed by one pathologist. The CRM were identified as described by Quirke et al.17 The minimum distance between the tumor and CRM, which was a distance of 1 mm or less, was taken as tumor involvement with the CRM, as de-fined previously.17,18 The CRM of the freshly received specimen was stained using the Davidson Marking System (Bradley Product, Inc., USA) and subsequently fixed for 48 h. Dissection consisted of slicing 5–10 mm serial sections of the whole tumor and the surrounding mesorectum in the transverse plane. The primary slice which contained the most lateral spread was selected for CRM measurement. The shortest distance between the CRM and the tumor was measured on a pathology slide (haematoxylin and eosin (H&E) stain, 20 times) with a micrometer. The distance was measured from the microscopically lateral portion of the tumor to the stained CRM (Fig. 2Go). We then divided the patients into two groups: "the negative CRM group" (CRM > 1 mm) and "the positive CRM group" (CRM ≤ 1 mm) according to the shortest distance between the CRM and the tumor. Clinical characteristics and oncological results were then investigated according to the groups.


Figure 2
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  		FIG. 2. Pathological measurement of the distance between the tumor and the circumferential resection margin. The distance was 350 µm (H&E stain, 20x) in (A) and 700 µm (H&E stain, 20x) in (B).

 
Data was analyzed using the SPSS package (Statistical Product and Service Solutions 11.5 for Windows, SPSS Inc., Chicago, IL, USA). Two-tailed {chi}2 tests for categorical variables and two-tailed Student’s t-tests for continuous variables were used for statistical comparisons of patient characteristics between the positive CRM group and the negative CRM group. Recurrence and survival curves between the two groups were calculated and compared using the Kaplan–Meier method and log-rank test, respectively. Univariate analysis of clinicopathological factors upon recurrence and survival were assessed with the log-rank test. All statistically significant factors found by univariate analysis were then used in the multivariate analysis. This analysis was conducted by a Cox proportional hazards model with a forward selection of variables to determine the prognostic value of the CRM. Statistically significant factors in the Cox analysis were expressed as a hazard ratio and a 95% CI. P values of ≤.05 were considered to be statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
Patients’ Characteristics
Out of all 504 patients, 460 patients (285 males and 175 females) were in the negative CRM group, 44 patients (26 males and 18 females) were in the positive CRM group (P = .709). The mean age within each group was 57.8 years (range, 22–87 years) and 58.0 years (range, 27–87 years) (P = .902) for the negative and positive CRM groups, respectively. In addition, the mean follow-up periods were 45.0 months (range, 1.1–88.7 months) and 35.8 months (range, 4.8–83.4 months) (P = .003) for the negative and positive CRM groups, respectively. Other clinicopathological characteristics of the patients are described in Table 1Go.


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  		TABLE 1. Comparison of clinicopathological features according to CRM involvement
 
Recurrence and Survival
The 5-year local recurrence rate was 11.3% in the negative CRM group and 35.2% in the positive CRM group (P = .010) (Fig. 3Go). The 5-year systemic recurrence rate was 25.3% in the negative CRM group and 60.8% in the positive CRM group (P < .001) (Fig. 4Go). The cancer-specific 5-year survival rate was statistically different between the groups (P < .001). This rate was 72.5% in the negative CRM group and 26.9% in the positive CRM group (Fig. 5Go). In addition, the cancer-specific disease-free 5-year survival rate was 62.7% in the negative CRM group and 24.4% in the positive CRM group (P < .001) (Fig. 6Go).


Figure 3
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  		FIG. 3. Five-year local recurrence rates in the positive (35.2%, n = 44) and negative CRM groups (11.3%, n = 460).

 

Figure 4
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  		FIG. 4. Five-year systemic recurrence rates in the positive (60.8%, n = 44) and negative CRM groups (25.3%, n = 460).

 

Figure 5
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  		FIG. 5. Cancer-specific 5-year survival rates in the positive (26.9%, n = 44) and negative CRM groups (72.5%, n = 460).

 

Figure 6
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  		FIG. 6. Cancer-specific disease free 5-year survival rates in the positive (24.4%, n = 44) and negative CRM groups (62.7%, n = 460).

 
Clinicopathological Factors Affecting Oncological Outcomes
Table 2Go shows the clinicopathological factors for the cancer-specific 5-year survival rate, 5-year local recurrence rate, and 5-year systemic recurrence rate in all enrolled patients (n = 504). CRM, preoperative CEA levels, histology grade, and TNM stage were significant prognostic factors for 5-year cancer-specific survival and 5-year systemic recurrence. CRM, preoperative CEA levels, and TNM stage were significant prognostic factors for the 5-year local recurrence rate.


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  		TABLE 2. Univariate analysis of clinicopathological factors for cancer-specific 5-year survival rates, 5-year local recurrence rates, and 5-year systemic recurrence rates in 504 patients
 
In the Cox proportional hazard regression for multivariate analysis, CRM was identified as an independent prognostic factor for cancer-specific 5-year survival, local recurrence, and systemic recurrence (Tables 3Go–5GoGo).


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  		TABLE 3. Multivariate analysis of clinicopathological factors for cancer-specific 5-year survival rates
 

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  		TABLE 4. Multivariate analysis of clinicopathological factors for 5-year local recurrence rates
 

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  		TABLE 5. Multivariate analysis of clinicopathological factors for 5-year systemic recurrence rates
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
CRM involvement is a predisposing factor for high risk of both local and systemic recurrences.13,19 Studies by Quirke et al.17 and Adam et al.18 found that inadequate surgical excision, in which the tumor is seen at the CRM, correlates with a high risk of local recurrence and that CRM involvement often causes adjuvant CRT. However, the beneficial effect of adjuvant CRT on patients with a positive CRM has not been fully evaluated.

In this study, we show that tumor involvement in the CRM is an unfavorable prognostic factor and that adjuvant CRT does not appear to compensate for a positive CRM. In our study, the local recurrence rate was significantly high in patients with a positive CRM than a negative CRM, and multivariate analysis showed that CRM status was an independent prognostic factor for local recurrence in all patients who underwent adjuvant CRT.

Marijnen et al.14 reported that adjuvant RT in patients with a positive CRM did not lead to a reduction of the number of local recurrences when patients with and without adjuvant RT were compared. Our analysis compared patients who underwent adjuvant CRT with a positive CRM to patients who underwent the same therapy with a negative CRM. Our data was based on the 5-year local recurrence rate. Even though the method of analysis was different, our study showed the same results with the study by Marijnen et al.14; adjuvant RT could not compensate for a positive resection margin. However, in the study by Marijnen et al.,14 the results were based on the 2-year local recurrence rate and did not include an analysis determining whether the systemic recurrence rate and the survival rate would be different in patients with a positive CRM according to adjuvant RT. In our study, the 5-year systemic recurrence rate was higher in the positive CRM group than in the negative CRM group. The cancer-specific 5-year survival rate and cancer-specific disease-free 5-year survival rate in the negative CRM group was higher than in the positive CRM group. Moreover, the CRM status was an independent prognostic factor for systemic recurrence and survival by multivariate analysis. These results showed that adjuvant CRT could not compensate for a positive CRM in local, systemic recurrences rates and survival rates.

Sauer et al.20 reported that neoadjuvant CRT improved local control compared to adjuvant CRT. Neoadjuvant CRT has a potential advantage of curative surgery and sphincter preservation in patients with low-lying tumors. However, in a previous study,14 neoadjuvant RT had no beneficial effects for patients with positive CRMs and reduced local recurrences merely in patients with negative CRMs. In patients who underwent neoadjuvant RT for rectal cancer, a positive CRM was a result of neoadjuvant RT and surgery. Thus, a cancer deposit in a positive CRM could be the cause of local recurrence. We agree with these conclusions. According to this postulation, we thought that adjuvant CRT could be effective for controlling these remnant cancer deposits in patients with a positive CRM. However, our results show that adjuvant CRT does not appear to compensate for a positive CRM.

In this study, patients who had neoadjuvant CRT were excluded. Adjuvant CRT was applied to all enrolled patients. Therefore, we believe that neoadjuvant CRT was not a compounding factor in the comparison of oncological outcomes between groups. All patients underwent surgery according to the standard TME principle performed by colorectal surgeons at our institute, thus eliminating any factors involving the surgeon and incomplete excision.

A distance of ≤1 mm has been defined as CRM involvement in several studies13,17,18,21 and is generally accepted as the definition of a CRM involvement.22 Thus, our study is based on this definition, although Nagtegal et al.23 suggested that an increased risk was present when CRM was ≤2 mm.

In our study, the rate of positive CRM was 8.7% (44 of 504 cases). Our rate was similar to the rates reported in a series of studies by Cawthorn et al.12 (6.5%) and Wibe at al.13 (9.5%). However, the rate of positive CRMs in our study is lower than the rate reported by Quirke et al.,17 which found a positive CRM rate of 27% when the entire tumor was embedded and examined. In the same series, a positive CRM rate of 12% was found when only the single primary slice was examined. In our study, we also only examined the single primary slice. Quirke et al.17 discussed that the examination of a single slice underestimates lateral spread by 50%. However, the single slice technique that was used in our study is more practical to do as a routine technique of the pathological examination of rectal cancer specimens.

To improve oncological outcomes of patients with positive CRMs, alternative, new treatment agents such as anti-VEGF monoclonal antibodies and epidermal growth factor receptor inhibitors24 may be considered. Moreover, close follow-up of these patients may be necessary for the early detection of systemic recurrence and prompt salvage treatment. Recently, new MRI technology allows the relatively accurate determination of tumor invasion depth and the potential for CRM involvement.25–27 Thus, pre-operative MRI may have a prognostic value in rectal cancer. This scan may encourage surgeons to dissect the rectum more carefully with respect to a CRM and to perform a more radical surgery, including combined organ resection, in order to obtain a large enough CRM. Moreover, in patients with a narrow or positive CRM by preoperative MRI, preoperative radiation treatments such as short-term regimens of high-dose neoadjuvant radiotherapy28 or common adjuvant radiotherapy can be used selectively for a safe CRM.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
This study shows that the CRM is an important prognostic factor in TNM stage II or III rectal cancer patients who underwent TME and adjuvant CRT. The patients with a positive CRM reveal higher local and systemic recurrence rates and less favorable survival rates than patients with a negative CRM. Therefore, adjuvant CRT is not a definite treatment modality that can be used to compensate for a positive CRM following TME and adjuvant CRT in patients with TNM stage II or III rectal cancer.


   ACKNOWLEDGMENTS
 
This study was supported by a grant from the Korea Health 21 R&D Project, Ministry of Health & Welfare, Republic of Korea (0412-CR01-0704-0001).

Received for publication June 16, 2006. Accepted for publication June 26, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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