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10.1245/ASO.2005.08.001
Annals of Surgical Oncology 12:561-569 (2005)
© 2005 Society of Surgical Oncology
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Original Article

Fusion Image of Positron Emission Tomography and Computed Tomography for the Diagnosis of Local Recurrence of Rectal Cancer

Hiroki Fukunaga, MD1, Mitsugu Sekimoto, MD, PhD1, Masataka Ikeda, MD, PhD1, Ichiro Higuchi, MD1, Masayoshi Yasui, MD1, Iwao Seshimo, MD1, Osamu Takayama, MD1, Hirofumi Yamamoto, MD, PhD1, Masayuki Ohue, MD, PhD1, Mitsuaki Tatsumi, MD, PhD2, Jun Hatazawa, MD, PhD2, Masakazu Ikenaga, MD, PhD3, Tsunehiko Nishimura, MD, PhD4 and Morito Monden, MD, PhD1

1 Department of Surgery and Clinical Oncology (E2), Graduate School of Medicine, Osaka University, 2-2 Yamadaoka Suita, Kinetics (D9), Osaka 565-0871, Japan
2 Department of Nuclear Medicine and Tracer Kinetics (D9), Graduate School of Medicine, Osaka University, 2-2 Yamadaoka, Suita, Osaka 565-0871, Japan
3 Department of Surgery, Osaka National Hospital, 2-1-14 Hoenzaka, Chuo-ku, Osaka 540-0006, Osaka, Japan
4 Department of Radiology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kajii, Kawaramachi-Hirokoji, Kamigyo, Kyoto 602-8566, Japan

Correspondence: Address correspondence and reprint requests to: Mitsugu Sekimoto, MD, PhD; E-mail: sekimoto{at}surg2.med.osaka-u.ac.jp.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The aim of this study was to evaluate the clinical and therapeutic value of digital fusion image (FI) of positron emission tomography (PET) using 18F-fluorodeoxy glucose and computed tomography (CT) in patients who were suspected of having a local recurrence of rectal cancer.

Methods:: Forty-two patients (32 men and 10 women; mean age, 61.4 years, range, 40–79 years) with a suspicion of local recurrence after curative resection of rectal cancer were prospectively recruited and underwent 18F-fluorodeoxy glucose-PET and CT. The FI was reconstructed with a commercially available digital software program, T-B Fusion. Wilcoxon signed rank test was used to compare FI with CT alone or PET alone.

Results: FI yielded a correct diagnosis in 39 (93%) of 42 patients, whereas CT alone and PET alone did so in 33 (79%) and 37 (88%) patients, respectively. FI had better diagnostic accuracy than CT alone (P = .0138) and PET alone (P = .0156). Overall, FI altered patient management in 11 (26.2%) patients on the basis of additional information, including differentiation of the tumor from the postoperative scar in 6 patients, exact anatomical location in 3 patients, and both in 2 patients.

Conclusions: FI has a potential clinical value in the treatment of suspected local recurrence of rectal cancer.

Key Words: PET • CT • Fusion image • Local recurrence of rectal cancer


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Local recurrence of rectal cancer is still a critical issue in the management of primary advanced rectal cancer. It is reported that approximately one third of rectal cancer patients undergoing curative radical resection will develop local recurrence.1 Local control and survival are possible for patients with isolated pelvic recurrence after extended radical operations, such as total pelvic exenteration and adjuvant chemotherapy. Wanebo et al.2 reported that local recurrence of rectal cancer can be resected safely with an expectation of long-term survival of 33%. Suzuki et al.3 reported that the 3-year survival rate for patients with curative R0 resection was 57%, but that for patients with R1 or R2 resection was only 26%. Therefore, early diagnosis of local recurrence is crucial to permit potentially curative reoperation.

In practice, however, many patients have tumors that require extended radical operations. Therefore, it is of clinical importance to differentiate recurrent tumor from postoperative scar after the diagnosis of local recurrence, for appropriate surgical planning. Conventional imaging modalities, including computed tomography (CT) and magnetic resonance imaging (MRI), are used to distinguish tumor from scar. However, CT is not specific for the detection of local recurrence, and its detection rate ranges from 69% to 95%.4–6 Furthermore, MRI is another frequently used modality, but the ability of T2-weighted images to differentiate tumors from scar tissue is questionable.7,8

Positron emission tomography (PET) using 18F-fluorodeoxy glucose (FDG) has emerged as a promising diagnostic modality in pelvic recurrence of rectal cancer; it detects the glycolytic activity of tumor cells.9–11 FDG-PET can potentially improve patient selection for surgery and hence may have a positive effect on treatment outcome. However, FDG-PET provides imprecise information on the exact location of focal abnormalities. Thus, even if the results of PET and CT are visually correlated, the precise location of lesions is sometimes difficult to determine. In a preliminary report, we described the construction and superimposition of PET images on CT images and demonstrated the usefulness of this fusion image (FI) for the diagnosis and operational planning of local recurrence of rectal cancer.12 The integrated PET/CT images have a promising value in the field of oncology.13–15

We recently developed software that can automatically generate a PET/CT FI. This study was conducted to determine the usefulness of FI for the detection of local recurrence of rectal cancer and to determine whether its use could influence surgical management.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study Population
Between April 2000 and May 2003, the Department of Surgery and Clinical Oncology, Graduate School of Medicine, Osaka University prospectively performed CT scanning and whole-body FDG-PET scanning in 44 consecutive patients with clinically suspected local recurrence of rectal cancer after curative resection. This study was approved by the institutional review board, and written informed consent was obtained before patients entered the study. Patients with underlying inflammatory bowel disease and diabetes were excluded because of potential diagnostic overlap with PET. In those 44 patients, 2 patients were excluded from the analysis; 1 had bladder cancer, and the other died during follow-up without confirmation of diagnosis. Thus, 42 patients (32 men and 10 women; mean age, 61.4 years; range, 40–79 years) were enrolled in this study. Of the 42 patients, 9 underwent surgery and were followed up in our department. The remaining patients underwent surgery and were followed up in other hospitals and then referred to our department for PET evaluation. Patients were referred because of CT/MRI findings suggestive of recurrence (n = 22), local symptoms (such as pain) suggestive of recurrence (n = 13), or increased levels of carcinoembryonic antigen (n = 7).

Follow-Up of Patients and Diagnosis Confirmation
Of 42 patients, pathologic confirmation was obtained by operation with curative intent in 17 patients and by biopsy specimens in 4 patients. The diagnosis of the other 21 patients was confirmed by clinical and radiological follow-up examinations (Table 1Go). The median follow-up period was 35.5 months (range, 12.5–45.2 months) for patients with a final diagnosis of postoperative change. The median time interval between the primary operation and the CT and PET scan was 24 months (range, 5–111.6 months).


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  		TABLE 1. Characteristics of 42 patients
 
Computed Tomography
All patients underwent CT of the abdomen and pelvis (Light Speed; General Electric, Milwaukee, WI) with intravenous administration of contrast material before PET studies (Omnipaque 300; Winthrop-Breon Laboratories, New York, NY). CT scans were obtained with 2.5-mm-thick axial planes in the upper portion of the abdomen and pelvis. The matrix size was 512 x 512, and the pixel size was .67 x .67 mm. Results of CT were reported by one senior radiologist with special interest in pelvic imaging who was blinded to the results of both PET and FI reading. Recurrence was evaluated, and the extent of pelvic recurrence was recorded when recurrence was suspected. The presence of other metastases was also recorded.

18F-Fluorodeoxy Glucose Positron Emission Tomography
FDG-PET was performed with a PET scanner, the Headtome V (Shimadzu Co., Kyoto, Japan), which has 32 rings and simultaneously produces 63 slices, each 3.125 mm thick, along a 20-cm longitudinal field. The matrix size was 128 x 128, with a pixel size of 4 x 4 mm. After at least 4 hours of fasting, 370 MBq of FDG was administered intravenously. One hour later, transmission and emission images were obtained simultaneously. The bladder was continuously flushed via a triple-lumen catheter with 1000 mL of saline. PET scans were evaluated qualitatively by one nuclear physician and one surgeon familiar with the local recurrence of rectal cancer and pelvic anatomy without the knowledge of CT results. Recurrence was recorded. The PET images were retrospectively evaluated quantitatively by means of standard uptake value (SUV). A region of interest was placed over the most intense areas of FDG accumulation to minimize any partial volume effect. SUV was calculated as follows:


Formula

Image Fusion Method
To enable digital fusion of the images, we used a commercially available digital software program (T-B Fusion; Shimadzu). The software automatically adjusted the pixel size. After the fusion area was selected manually on the transmission image according to the body shape, the fit image in the ordered area was registered according to the fusion algorithm based on minimizing the intensity difference on an image workstation. Then, automatically, the emission image corresponding to the transmission image was displayed transparently on the CT image. When necessary, fine adjustment was performed manually.

FI Readings
Two experienced oncologists with expertise in PET, but who were blinded to the clinical information and without knowledge of CT- and PET-alone results, evaluated all FIs independently. FIs were evaluated with five images. In these five images, FDG-PET images were superimposed on CT images with five grades of transparency: 0%, 25%, 50%, 75%, and 100%. To interpret the FI, sagittal, coronal, and transaxial images were prepared. When the diagnosis was different between the two observers, the final decision was determined after discussion.

Clinical Effect of FI Findings on Surgical Treatment and Management
Clinical management decisions were made first by one specialized surgeon on the basis of CT and PET findings. Afterward, the indication for surgical intervention was reconsidered by the surgeon with full knowledge of CT, PET, and FI. Changes in the therapeutic management before and after the results of the FI were compared, and the clinical usefulness of FI was evaluated.

Statistical Analysis
Statistical analysis was performed with SAS software, version 8.2 (SAS Institute, Cary, NC). To identify any improvements in the accuracy of the diagnosis of the local recurrence associated with the use of FI, the diagnosis of local recurrence by each imaging method was assessed by means of a score ranging from 0 to 3, as has been reported.13 Briefly, score 0 indicates incorrect findings, score 1 represents equivocal but incorrect findings, score 2 indicates correct but equivocal findings, and score 3 indicates correct findings. Wilcoxon signed rank test was used to compare FI with the other imaging methods. Because score 0 and score 1 were both incorrect, we combined them in the analysis and assigned them a score of 0. To address the problem of multiple comparisons, Bonferroni’s correction was applied, and P values <.025 were considered significant. All P values are two sided.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
All 42 patients with presumed local recurrence of rectal cancer were imaged with conventional CT scans and PET scans, and FIs were reconstructed. Table 1Go shows the patient characteristics, final diagnosis and confirmation of diagnosis, and treatment. Table 2Go shows the diagnostic accuracy of the three imaging modalities. Thirty-three of 42 patients were classified correctly (scores 2 and 3) by CT alone, and 9 classifications were incorrect (scores 0 and 1). Of the nine cases classified incorrectly, seven patients had local recurrence. Of the seven patients who had local recurrence, CT alone could not detect the abnormality in four patients; it diagnosed postoperative change in two patients and abscess in one. In the other two patients who did not have local recurrence, CT alone diagnosed recurrence. Compared with CT alone, FI provided additional information in seven of nine patients who had been diagnosed incorrectly and led to the correct diagnosis. The additional information consisted of the exact location of local recurrence in five patients and of no tumor radionuclide uptake in two patients (Table 3Go). The exact location of recurrence included the presacral area in one patient, the rectal stump in one, and lateral pelvic lymph nodes in three. Three of those five patients underwent operation, and the other two patients received chemotherapy. In the two patients with no FDG uptake, CT raised suspicion of a local recurrence, but FI did not. Finally, two patients did not undergo operation because FI results were negative, and follow-up showed no progression of the lesions, thus making malignancy unlikely. However, FI could not diagnose local recurrence correctly in two patients because of small-volume disease and overlap with urinary tract activity. In those two patients, radiological follow-up confirmed local recurrence 4 and 12 months after the initial diagnosis.


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  		TABLE 2. Diagnostic accuracy of the imaging methods
 

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  		TABLE 3. Results of CT, PET, and FI for discrepant results
 
Thirty-seven patients were classified correctly by PET alone, and five were classified incorrectly. All five patients had local recurrence, but radionuclide uptake was not detected in three patients, and tumor radionuclide uptake could not be differentiated from urinary tract activity in two patients. All nine patients without local recurrence were correctly diagnosed by PET alone (no false-positive cases). Compared with PET alone, FI provided information on the exact location of lesions in two of five patients who had been diagnosed incorrectly. In the other three patients, two could not be diagnosed correctly even with these three modalities. In the other patient (case 15), the initial CT showed a suspicion of local recurrence, whereas PET was negative. Surgery was postponed, but a CT taken 2 months later confirmed local recurrence by tumor growth, and the patient underwent operation. PET alone also detected extrapelvic disease in four patients: one patient with thyroid cancer, two patients with liver metastasis, and one patient with lung metastasis.

Finally, FI provided additional information on 8 (19%) of 42 patients over CT or PET alone positively for accurate diagnosis of local recurrence of rectal cancer. On the other hand, FI negatively affected the diagnosis in one patient. Overall, FI provided more accurate information on the diagnosis of local recurrence of rectal cancer than did the other two imaging modalities. Statistically significant improvement was observed with FI compared with CT alone (P = .0138) and PET alone (P = .0156).

Influence of FI on Therapeutic Management
Because FI can provide more precise information on the anatomical location of disease, the results of FI could potentially influence the therapeutic management of local recurrence. We had five such patients in this series. In those five patients, either CT alone or PET alone indicated local recurrence, but patients could not be candidates for radical operation if FI did not show the exact anatomical location of local recurrence. Four patients underwent total pelvic exenteration, and one patient underwent local tumor resection. Figure 1Go shows patient 18, whose recurrent tumor was not detected by CT alone (Fig. 1AGo) but was clearly detected by FI (Fig. 1CGo). In Fig. 2Go, lateral pelvic lymph node metastasis was identified by FI and later resected (case 41), although CT alone could not detect the tumor and PET alone did not provide sufficient information for surgical planning. FI is also useful for differentiating between physiological FDG uptake and tumor. Accumulation of FDG within the bladder and bowel (Figs. 1BGo and 2BGo) is easily discriminated in the FI (Figs. 1CGo and 2CGo).


Figure 1
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  		FIG. 1. A 65-year-old man (patient 18) with a history of low anterior resection with the Hartmann procedure, with recurrence at the rectal stump. (A) Sagittal computed tomography does not show tumor, and a differential diagnosis cannot be made. (B) Corresponding sagittal positron emission tomography image shows focal increase of 18F-fluorodeoxy glucose uptake in the presacral area (arrowhead), suggesting tumor recurrence, but no precise anatomical information can be obtained. (C) Corresponding fusion image shows tumor recurrence at the rectal stump (arrow). (D) Resected specimen showing tumor recurrence (red circle). (E) Photomicrograph of the resected specimen confirms adenocarcinoma (stain, hematoxylin and eosin; original magnification, x200).

 

Figure 2
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  		FIG. 2. A 57-year-old woman (patient 41) with a history of abdominoperineal resection, with recurrence at the lateral pelvic lymph node. (A) Transaxial computed tomography does not show any abnormalities. (B) Corresponding axial positron emission tomography image demonstrates increased metabolic activity in the right presacral area (red circle). (C) Transaxial fusion image reveals right lateral pelvic lymph node recurrence (red circle). (D) Resected specimen showing tumor recurrence (area surrounded by red dots). (E) Photomicrograph of the resected specimen confirms adenocarcinoma (stain, hematoxylin and eosin; original magnification, x200).

 
Taken together, a clinical effect of FI findings on surgical treatment and management was evident in 11 (26.2%) patients. Three patients underwent radical operation after the precise anatomical location of the tumor was identified, and in six patients, the treatment was modified on the basis of correct diagnosis by FI. Two patients (patients 18 and 41) underwent surgery on the basis of both correct diagnosis and anatomical location with FI. In particular, the surgical plan was modified in 5 (27.8%) of 18 patients, who underwent operation because of the results of FI. However, we could not diagnose two patients correctly even with these three modalities because of small-volume disease and overlap with urinary tract uptake.

Quantitative Analysis of Suspected Local Recurrence of Rectal Cancer
Figure 3Go shows the individual and median SUV of true-positive cases (n=28), true-negative cases (n=9), and false-negative cases (n = 5). The median SUV of true-positive cases was 3.93 (range, 2.02–8.17), and that of true-negative cases was 1.34 (range, .73–2.06). SUVs of false-negative cases fell well within the range between true-negative and -positive cases (median, 2.14; range, 1.8–2.64).


Figure 3
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  		Fig. 3 Standard uptake value (SUV) of the region of interest in patients with suspected local recurrence of rectal cancer. Each bar represents the interquartile range, and the horizontal line within the bar represents the median value. To identify statistical difference among the three groups, the Kruskal-Wallis test was used. The Steel-Dwass test was then applied to compare between groups. *P < .001; **P = .017; ***P = .008. T, true positive; TN, true negative; F, false negative.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
PET scanning is a useful imaging modality for the detection of local recurrence of rectal cancer, particularly because it distinguishes between recurrence and postoperative fibrosis.9,16,17 Ito et al.9 and Strauss et al.17 reported its utility by semiquantitative analysis of FDG uptake. Keogan et al.11 demonstrated the usefulness of visual correlation of PET and CT or MRI in detecting local recurrence of rectal cancer. The image fusion method, with more precise anatomical information on the PET image, was then introduced, and its utility in maxillofacial carcinoma and thoracic malignancies has been reported.18,19 However, the usefulness of digital FI in the diagnosis of rectal cancer has not been studied. Our results with FI of PET and CT demonstrated that FI provided more accurate information on the diagnosis of local recurrence of rectal cancer than did the other two imaging modalities. Statistically, a significant improvement was observed in comparison with both CT alone (P = .0138) and PET alone (P = .0156).

Recent development of inline PET/CT has improved diagnostic accuracy without visually correlating these two images by providing coregistered PET/CT images.20 Significant improvement in diagnostic accuracy was found in the staging of non–small-cell lung cancer in comparison with visual correlation of PET and CT images.13 Cohade et al.21 demonstrated the superiority of PET/CT over PET alone in the evaluation of colorectal cancer. Although the inline PET/CT will be the standard of reference in oncological imaging in the near future, those scanners are still quite expensive and not frequently available. Therefore, the software-based image fusion technique used in our study may provide relevant information concerning diagnosis and treatment decision making in patients with suspected local recurrence of rectal cancer. It is less expensive and easier to use. Because the PET and CT images were taken separately, it is impossible to eliminate respiratory movement when they are registered. However, in the pelvic area, there are many landmarks for coregistering PET and CT images, and artifacts due to respiratory movement are negligible because local recurrence is a fixed tumor.

Local recurrence of rectal cancer is a complex disease. The treatment consists of surgery, radio-therapy, chemotherapy, or a combination of these.22 Among these treatments, surgical resection remains the only potentially curative option in most patients.2,3 It is therefore important to select favorable candidates for radical operation. Saito et al.23 emphasized the importance of the pattern of recurrence, the area of invasion, and the presence of symptoms for successful curative operation. Wanebo et al.2 reported that patients with previous anterior resections or preoperative carcinoembryonic antigen levels <10 ng/mL had a favorable outcome. Taken together, it is apparent that patients with small tumors and adequate margins of resection have longer survival. In terms of early detection, PET is useful24 and is also useful in terms of providing anatomical information when it is combined with CT.20 In our series, in five patients (11.9%)—27.8% of patients who underwent curative resection—the treatment plan was altered on the basis of FI results; namely, the extent of tumor involvement was considered possible for curative resection on FI. This decision could not be made without FI. CT alone or PET alone is less powerful for the precise localization of recurrent tumors and their resectability.25–27

The clinical effect of FI on diagnosis or treatment decision making in this study was 26.2%. The frequency of patient management changes attributable to PET ranges from 20% to 61%.27–32 Flamen et al.32 reported that potential changes in therapeutic management were noted in 20% of their patients, and Kalff et al.31 demonstrated that the frequency of change of patient management attributable to PET was 59% in their prospective study. In comparison with those studies, the clinical effect of FI on patient management in our study is comparable if the patient population is limited to local recurrence.

PET still has limitations. The detectability of tumor by PET depends on tumor size and uptake of FDG; therefore, PET scans cannot detect small-volume disease and underestimate the extent of lesions measuring <1 cm in diameter.1,28 Bladder activity also remains a potential source of error in PET studies of the presacral area.33 In our series, we had five (11.9%) false-negative cases by PET alone, and two were correctly diagnosed with FI by provision of additional anatomical information. However, the other three patients could not receive a correct diagnosis even with FI because of small-volume disease in two and overlap with urinary tract activity in one. Therefore, a correct diagnosis cannot be obtained in some patients even with this modality. Serial imaging studies and tumor markers are very important in patients who are highly suspected of having local recurrence but without confirmation.

In conclusion, combined morphological (CT) and functional (PET) imaging improves the diagnosis of local recurrence of rectal cancer and helps surgical management of this critical disease as an integral part of treatment decision making, even if each modality cannot provide sufficient information. FI allows selection of patients with a higher chance of cure while avoiding unnecessary operation on patients with diffuse disease and no chance for improvement of survival. Therefore, FIs have a potential clinical value in the treatment of suspected local recurrence of rectal cancer, and now we routinely perform FI on all patients being evaluated for local recurrence.


   ACKNOWLEDGMENTS
 
The authors thank Dr. Tadaaki Yamada, Shionogi & Co., Ltd., Department of Biostatistics, for technical assistance regarding statistical analysis.

Received for publication August 2, 2004. Accepted for publication January 19, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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