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10.1245/ASO.2006.04.042
Annals of Surgical Oncology 13:397-404 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Improved Staging With Pretreatment Positron Emission Tomography/Computed Tomography in Low Rectal Cancer

Susan L. Gearhart, MD1, Deborah Frassica, MD2, Ron Rosen, MD3, Michael Choti, MD1, Richard Schulick, MD1 and Richard Wahl, MD3

1 Department of Surgery, Johns Hopkins Medical Institution, Blalock 656, 600 North Wolfe Street, Baltimore, Maryland 21287
2 Department of Radiation Oncology, Johns Hopkins Medical Institution, Baltimore, Maryland 21287
3 Department of Radiology, Johns Hopkins Medical Institution, Baltimore, Maryland 21287

Correspondence: Address correspondence and reprint requests to: Susan L. Gearhart, MD; E-mail: sdemees1{at}jhmi.edu.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: 18F-Fluorodeoxyglucose (FDG)-positron emission tomography (PET) and computed tomography (CT) are widely accepted in the evaluation for metastatic or recurrent rectal cancer. Only spiral CT and transrectal ultrasonography (TRUS) are routinely used in the initial evaluation of primary rectal cancer. We wished to determine whether PET/CT could provide additional information in patients undergoing standard evaluation for primary rectal cancer.

Methods: Thirty-seven patients (mean age, 58 years; range, 26–90 years) with a previously untreated rectal cancer underwent TRUS or magnetic resonance imaging, spiral CT, and FDG-PET/CT. The tumor location (low, ≤6 cm; mid, 7–10 cm; or high, ≥10 cm) and carcinoembryonic antigen level were recorded. Discordant findings between spiral CT and FDG-PET/CT were confirmed by histological analysis or imaging follow-up.

Results: FDG-PET/CT identified discordant findings in 14 patients (38%), and this resulted in upstaging of 7 patients (50%) and downstaging of 3 patients (21%). Although node-positive disease on TRUS/magnetic resonance imaging was associated with discordant FDG-PET/CT findings, this was not statistically significant. Discordant PET/CT findings were significantly more common in patients with a low rectal cancer than in those with mid or high rectal cancer (13 vs. 1; P = .0027). The most common discordant finding was lymph node metastasis (n = 7; 50%). Histological confirmation of discordant FDG-PET/CT findings was performed in seven patients, and in no case did FDG-PET/CT prove to be inaccurate. Discordant PET/CT findings resulted in a deviation in the proposed treatment plan in 27% of patients (n = 10).

Conclusions: FDG-PET/CT frequently yields additional staging information in patients with low rectal cancer. Improved accuracy of pretreatment imaging with FDG-PET/CT will allow for more appropriate stage-specific therapy.

Key Words: Rectal cancer • Positron emission tomography • Computed tomography • Neoadjuvant therapy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
According to the American Cancer Society, the relative rate of 5–year survival from colorectal cancer has increased over the past three decades from 49% in 1976 to 62% in 1998. The estimated 2005 relative 5- year survival rate for all stages of colorectal cancer is 64%.1 In optimizing the treatment of colorectal cancer, appropriate staging of the disease is essential. The current modalities used for the initial staging of colorectal cancer include digital rectal examination, spiral computed tomography (CT), magnetic resonance imaging (MRI), and endorectal ultrasound. For local staging of rectal cancer, endorectal ultrasound and MRI with a pelvic coil provide an accuracy of 82% in bowel wall invasion (T staging) and approximately 70% in lymph node (N) metastasis.2 Although limited in the evaluation of local pelvic disease, the accuracy of spiral CT for metastatic lesions >1 cm approaches 85%.3

Recently, 18F-fluorodeoxyglucose (FDG)-positron emission tomography (PET) has been shown to have a complementary role in the detection of local recurrence and distant metastatic colorectal cancer. Specifically, FDG-PET has aided in the differentiation of tumoral and nontumoral masses found on other imaging modalities, especially in the setting of an increasing serum tumor marker such as carcinoembryonic antigen (CEA). The accuracy of FDG-PET for pelvic recurrences ranges from 74% to 96%, and for metastatic disease to the lung and liver, it ranges from 93% to 99%.4,5 Even-Sapir et al.6 reported that the accuracy of FDG-PET for locally recurrent and metastatic colorectal cancer improved significantly when a simultaneous CT was performed. More recently, FDG-PET/CT has been used to monitor the clinical response of tumors to chemoradiation. The reported accuracy of FDG-PET/CT in determining responsiveness in these modalities was 80%.7,8

The use of FDG-PET/CT in the initial evaluation of rectal cancer has primarily been reserved for further characterization of lesions identified in the lung or liver on preoperative CT imaging. However, given the accuracy of FDG-PET/CT, this study was undertaken to further define the utility of PET/CT imaging in the initial evaluation of primary rectal cancer.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
From January 2003 to January 2005, 37 patients with previously untreated, biopsy-proven adenocarcinoma of the rectum were identified from the Johns Hopkins Colorectal Cancer Database. This is a Johns Hopkins Medical Institution Review Board–approved database to study outcomes from colorectal cancer. This study evaluated the use of FDG-PET/CT in patients who were being considered for multidisciplinary treatment of their rectal cancer. Patients with early tumors not at risk for sphincter loss and patients with known metastatic disease were excluded. Furthermore, patients already undergoing therapy were excluded.

At the time of initial evaluation, all tumors were staged locally by using transrectal ultrasonography (TRUS) or MRI of the pelvis with an endorectal coil. All TRUS examinations were performed by a single investigator. TRUS was performed with the patient in the left lateral position. A 10-MHz crystal on an ultrasound probe (model 1846; Bruel and Kjaer, Marlboro, MA) was inserted into the anorectum, advanced above the tumor, and slowly withdrawn. The tumor within the rectum was evaluated for the distance from the anal verge, the degree of bowel wall invasion (T stage), and for lymph node metastasis within the mesorectum (N stage). Tumors were then classified as low (≤6 cm), mid (7–10 cm), or high (≥10 cm). Consistency among clinical studies regarding the classification of tumors into low, mid, or high rectal lesions is lacking. The classification used in this study is based on the location of the three valves of Houston at 7, 10, and 12 cm from the anal verge. These valves serve as an additional endoscopic technique for determining the distance of the tumor from the anal verge. All patients underwent a standard spiral CT of the chest, abdomen, and pelvis for evaluation of distal metastasis. Stages were reported by using the tumor-node-metastasis classification according to the AJCC Cancer Staging Manual.9

PET/CT Imaging
Patients undergoing FDG-PET combined with noncontrast CT (FDG-PET/CT) at our institution were instructed to fast 4 hours before the beginning of the examination. A blood glucose level was checked in patients with diabetes. The study was not performed if the blood glucose level exceeded 150 mg/dL. Initially, the patients were injected with 15 to 20 mCi of FDG intravenously. The patients were then asked to drink oral CT contrast lacking glucose with a 13% barium concentration. Scanning from the skull base to the mid thigh was then performed with the GE Discovery LS PET/CT system (GE Medical Systems, Milwaukee, WI). Simultaneous noncontrast CT images were obtained generally at 140 kV, 80 mA, and .8 seconds per CT rotation, with a pitch of 6 and a table speed of 22.5 mm/sec.

Image Interpretation
Images were interpreted at a workstation where images could be displayed with or without attenuation correction for PET with a registered noncontrast CT. Positive findings were determined and qualified by an experienced nuclear medicine physician. The findings on FDG-PET/CT were compared with conventional spiral CT findings. All images were reported initially independently. Questionable areas on either FDG-PET/CT or spiral CT that were amenable to biopsy underwent CT, ultrasound-guided fine-needle aspiration, or surgical excision. Further evaluation for discordant findings included other forms of confirmatory imaging, including MRI, follow-up spiral CT, or PET/CT.

Statistical Analysis
Statistical analysis was performed by using Prism software (Graphpad Inc., San Diego, CA). Chisquare analysis was used to compare differences in tumor level and stage with discordant PET/CT findings. The Mann-Whitney test was used to compare CEA levels between patients with and without discordant CT findings.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Patient Characteristics
Of the 37 patients included in this study, there were 11 women and 26 men with an average age of 58 years (range, 26–90 years). All patients underwent local staging procedures with either TRUS (n = 31) or pelvic MRI with an endorectal coil (n = 6) at the Johns Hopkins Medical Institutions. MRI with a pelvic coil was performed when TRUS could not be performed because of significant narrowing of the rectal lumen from the tumor. Full-body intravenous contrast CT was performed in 69% of patients (n = 22) at an outside institution, whereas 81% of patients (n=30) underwent FDG-PET/CT at our institution. The interval between contrast CT and FDG-PET/CT was <1 month in 34 patients. In the three patients in whom the interval was>1 month, one patient had an MRI of the abdomen performed within a 1-month interval, and two patients had a delay in further radiological imaging secondary to unrelated health problems. In the patient with an additional MRI scan, neither the MRI nor the CT scan achieved imaging low enough to evaluate the femoral nodes. For this reason, this case was considered a discordant finding of femoral node metastasis. Seven patients had already obtained a FDG-PET/CT at an outside institution before their initial evaluation, and the outside interpretation was used. FDG-PET/CT was administered without complications to all participants. The initial study on one patient had to be postponed secondary to an increased blood glucose level.

Discordant FDG-PET/CT Findings
Initial evaluation with conventional methods of staging for rectal cancer demonstrated that 81% of patients had stage II or III disease. However, three patients had stage IV disease based initially on conventional CT imaging (Table 1Go). These three patients included two patients with enlarged inguinal lymph nodes and one with a liver lesion, all pointing toward metastatic disease. The use of FDG-PET/CT identified discordant findings when compared with conventional spiral full-body CT in 38% of patients (n = 14). This resulted in downstaging of all three patients previously classified as having stage IV disease. Discordant findings also resulted in upstaging of 19% of patients (n = 7; Table 2Go). The most common discordant finding was lymph node metastasis (Fig. 1Go; n = 7; 50%) Other discordant findings included an additional colonic neoplasm, abnormal endometrial enhancement, and additional liver lesions. Histological confirmation was obtained in 50% of discordant FDG-PET/CT findings by either fine-needle aspiration (n = 3) or surgical excision (n = 4). In patients who underwent histological confirmation, in no case did FDG-PET/CT prove to be inaccurate in its findings. The remaining seven patients did not have accessible lesions for biopsy or refused biopsy (n=1), and follow-up or alternative imaging was performed. Follow-up or alternative imaging included a repeat PET/CT or spiral CT to evaluate for changes in the identified abnormality or MRI imaging.


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  		TABLE 1. Pretreatment staging for low versus mid and high rectal cancers by using standard techniques (computed tomography, transrectal ultrasonography, and pelvic magnetic resonance imaging)
 

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  		TABLE 2. Final pretreatment staging for low versus mid and high rectal cancers by using standard techniques with the addition of positron emission tomography/computed tomography
 

Figure 1
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  		FIG. 1. (A) Positron emission tomography (PET)/computed tomographic (CT) imaging demonstrates a primary rectal lesion and a right internal iliac node (arrow). (B) On the same scan, a right inguinal node also demonstrates increased activity (arrow).

 
Tumor Location, uTN Stage, CEA Level, and Discordant PET/CT Findings
In this patient population, 62% of the patients (n = 23) had a low adenocarcinoma of the rectum. The remaining 38% of patients had mid and high rectal cancers (n = 12 and 2, respectively). Discordant FDG-PET/CT findings were significantly more common among patients with low rectal cancers than those with mid or high cancers (n = 13 vs. 1; P = .0027). The one patient with a high rectal cancer and discordant findings on FDG-PET/CT had evidence of mesorectal lymph node metastasis. This patient had Leriche syndrome and had undergone a limited TRUS examination secondary to multiple enlarged mesorectal vessels. Node-positive disease on TRUS/MRI was seen in 71% (n = 10) of patients with discordant FDG-PET/CT findings and in 48% (n = 11) of patients without discordant findings. Although a trend was evident between higher local stage and discordant FDG-PET/CT findings, this did not reach statistical significance (Table 3Go). Pretreatment CEA levels were not available for two patients. The mean CEA level for patients with and without discordant FDG-PET/CT findings was not significantly different (11 ng/mL [95% confidence interval, 2.7 to 19.3 ng/mL] and 23.5 ng/mL [95% confidence interval, –8.15 to 55 ng/mL], respectively).


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  		TABLE 3. Characteristics of patients with and without discordant positron emission tomography/computed tomographic findings
 
Alteration in Treatment Plan
Alterations in treatment plans as a result of FDG-PET/CT findings occurred in 27% of patients (n=10; Table 4Go). Patients identified with metastasis to the distant pelvic lymph nodes proceeded with neoadjuvant therapy; however, it was recommended that the fields of radiotherapy include the diseased lymph node (Fig. 2Go). In the two patients with enlarged lymph nodes on conventional CT imaging, neither lymph node was FDG avid on FDG-PET/CT. This resulted in one patient proceeding with the planned operation with the addition of a lymph node biopsy for confirmation. The second patient underwent a confirmatory biopsy, which demonstrated the lack of metastatic disease, and then proceeded with the planned pelvic exenteration. One patient had a second primary tumor discovered on FDG-PET/CT which was found to be approximately 10 cm above the initial lesion. This lesion was missed on initial colonoscopic evaluation. Both lesions were removed at the time of operation. Final pathologic analysis revealed two separate cancers within the rectum and rectosigmoid. Finally, there were three additional patients with worrisome liver or lung lesions.


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  		TABLE 4. Discordant or additional PET/CT findings resulting in an alteration of patient management
 

Figure 2
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  		FIG. 2. (A) Standard radiation ports for the treatment of adenocarcinoma of the lower rectum. (B) Extended radiation ports for the inclusion of inguinofemoral lymph nodes.

 
The first patient had an outside FDG-PET/CT scan, and the results, which indicated that there was an FDG-avid lesion in the left lobe of the liver, were reported after neoadjuvant therapy had begun. A repeat FDG-PET/CT scan at the end of his neoadjuvant therapy demonstrated decreased activity in the left lobe of the liver and the primary lesion. At the time of operation, he underwent an abdominoperineal resection and excision of his left lobe lesion. The final pathologic analysis of the liver lesion demonstrated necrotic metastatic adenocarcinoma consistent with a treatment effect.

The second patient had a history of septic endocarditis and was found on spiral CT performed at our institution to have multiple cysts/lesions of the liver and lung. FDG-PET/CT was able to distinguish two to three suspicious liver lesions and no lung lesions. He had an asymptomatic primary tumor and was referred for systemic chemotherapy. He subsequently has undergone resection of his primary tumor, as well as his metastatic lesions, and is alive with no evidence of disease.

Finally, the third patient had a suspicious liver lesion on an outside CT scan that was not FDG avid on FDG-PET/CT. This lesion remains unchanged throughout neoadjuvant therapy, and the patient is >1 year out without any new findings within the liver on follow-up imaging.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
The 5-year relative survival rate for all stages of colorectal cancer has increased from 49% to 63% over the past three decades. This is thought to be secondary, in part, to improvements in screening.10,11 In addition, multimodality therapy for locally advanced disease is believed to be the preferred treatment modality in preventing local recurrence and improving survival from rectal cancer.12–15 For this reason, neoadjuvant and/or adjuvant chemoradiation is considered the standard of treatment for locally advanced (T3/4) or node-positive (N1/2) rectal cancer. Current accepted methods for preoperative staging of rectal cancer include TRUS, MRI, and spiral CT. In this article, we demonstrate the usefulness of FDG-PET/CT in the initial staging of rectal cancer, particularly low rectal cancers.

Our data demonstrated that FDG-PET/CT, when compared with conventional spiral full-body CT, demonstrated discordant findings in 38% of patients. These findings altered the initial stage and resulted in alterations in the initial treatment plan in 27% of patients. We attempted to confirm all discordant findings by fine-needle aspiration or excisional biopsy; however, many lesions were not amenable to biopsy. All biopsy results concurred with FDG-PET/CT findings. Our findings are consistent with the findings of others. Heriot et al.16 found that pretreatment FDG-PET resulted in an alteration of stage in 39% of patients and an alteration in treatment plan in 17% of patients. In Heriot’s study, 22% of new findings (n = 4) on FDG-PET were pelvic or paraortic lymphadenopathy. Only one patient had a confirmatory biopsy, and no mention of tumor location was made. In our study, iliac or inguinal/femoral lymphadenopathy composed 50% of discordant findings (n = 7), of which four patients underwent confirmatory biopsy either before or at the time of surgery. The higher percentage of patients with pelvic lymphadenopathy in our study may be the result of a significant number of lower rectal tumors or the use of combined-modality FDG-PET/CT.

Of particular interest in this study was that discordant FDG-PET/CT findings were significantly more common among lower (≤6 cm from the anal verge) rectal cancers. In this subset of patients, the most common finding was the presence of inguinofemoral or iliac lymphadenopathy. It is well known that the lymphatic drainage of the lower rectum is directly into the systemic and the portal venous system. In reviewing the pathologic characteristics of 353 early rectal cancers, Nascimbeni et al.17 found that cancers in the lower third of the rectum had a higher propensity for lymph node metastasis (34%) as compared with cancers of the mid or upper rectum (11% vs. 8%, respectively). Furthermore, in a review of 189 locally advanced cancers of the lower rectum, Habr-Gama et al.18 demonstrated that these tumors overall had a worse prognosis. In this series, patients with locally advanced node-positive low rectal cancer treated with neoadjuvant chemoradiation and surgery had only a 28% 5-year disease-free survival. Furthermore, the local recurrence rate for pathologic node-positive low rectal cancer was 27.5%. These authors emphasized that the presence of lymph node metastasis in the pathologic specimen after neoadjuvant chemoradiation in this subgroup of patients was the most significant prognostic factor.

One of the established major causes of pelvic failure after the surgical management of rectal cancer is the lateral spread of tumor cells within the mesorectum not removed at the time of surgery.19,20 However, in this study, which consisted of >60% low rectal cancers, FDG-PET/CT identified five cases (13.5%) with nodal spread outside of the mesorectum to the inguinal/femoral or iliac lymph nodes that were not identified on conventional staging modalities. FDG-PET/CT also accurately determined the lack of lymph node metastasis in two patients with enlarged lymph nodes on spiral CT imaging. The management of FDG-avid pelvic lymph nodes identified on FDG-PET/CT or the effect of this finding on local recurrence and survival is not known. In this study, patients with rectal cancer and FDG-avid iliac, inguinal, or femoral lymph nodes were referred for neoadjuvant therapy with extended radiation fields. Others have proceeded with extended lymphadenectomy at the time of surgical resection of the primary tumor.21,22 Ciernik et al.23 demonstrated the usefulness of integration of radiation treatment planning with FDG-PET/CT. FDG-PET/CT allowed for better characterization of tissue structures of unknown significance adjacent to the tumor and provided better treatment volume delineation. The ability of radiotherapy to decrease the incidence of local recurrence after surgery for rectal cancer has led many to believe that high-dose radiotherapy may sterilize the pelvic sidewall lymphatics.24,25 Guillem et al.7 reported the utility of FDG-PET/CT in monitoring the clinical response of 15 patients with rectal cancer to neoadjuvant therapy. In Guillem’s study, a decrease in the standard uptake value intensity of the primary lesion on consecutive FDG-PET/CT scanning was associated with an improvement in disease-specific and recurrence-free survival. The effect of the findings of this study, particularly the pelvic lymphadenopathy, on local recurrence and survival after treatment for rectal cancer is not yet known.

Our data support the routine use of FDG-PET/CT in pretreatment staging of rectal cancer, particularly in patients with low rectal cancers. The use of FDG-PET/CT as an accurate adjunct in the management of rectal cancer may assist the clinician in several ways: (1) by eliminating additional procedures, such as biopsies of suspicious lesions on CT imaging that are not FDG avid; (2) by improving treatment field planning for radiotherapy; (3) and by assisting in routine follow-up of patients with treated rectal cancer. However, our findings are limited by a small sample size and a lack of consistency in imaging. Only 50% of our patients were able to undergo a confirmatory biopsy, and nearly 70% of our patients had their spiral CT scan performed at another institution. These limitations, however, may be difficult to overcome, and larger studies with the addition of intravenous contrast CT to FDG-PET imaging may provide additional information regarding the usefulness of FDG-PET/CT in the initial management of rectal cancer.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Discordant PET/CT findings were found to be significantly more common among lower rectal cancers than mid or high rectal cancers. Because of the high propensity of these tumors for lymph node metastasis, the enhanced ability of PET/CT to improve accuracy in initial staging will allow for more stage-specific therapy in the treatment of low rectal cancer. Further studies are needed to determine the effect of PET/CT findings on survival in rectal cancer.


   FOOTNOTES
 
Presented at the Annual Meeting of the Society of Surgical Oncology, Atlanta, Georgia, March 3–6, 2005.

Received for publication May 2, 2005. Accepted for publication September 16, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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