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British Journal of Radiology (2006) 79, 572-577
© 2006 British Institute of Radiology
doi: 10.1259/bjr/25287790
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PET/CT detects abdominal wall and port site metastases of colorectal carcinoma

E Goshen, MD 1 T Davidson, MD 2 D Aderka, MD 3 and S T Zwas, MD 1

Departments of 1 Nuclear Medicine, 2 Radiology and 3 Oncology, The Chaim Sheba Medical Center, Tel-Hashomer and Sackler School of Medicine, Tel Aviv University, Israel


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 Conclusion
 References
 
Abdominal wall metastases from colorectal cancer (CRC) may be resected with curative results. Such lesions, often indicators of additional intra-abdominal lesions, may appear in surgical scars, stomas and port site metastases after laparoscope-assisted surgery (LAS). Post-operative changes, primarily surgical scars, alter local physical findings making early detection of small lesions challenging. The purpose of this study was to retrospectively evaluate the contribution of PET/CT to the diagnosis of recurrent colorectal cancer in the post-operative abdominal wall. 120 patients were referred for PET/CT with suspected recurrent CRC based on clinical, radiological or laboratory findings. All underwent whole body PET/CT imaging. 12 of these 120 (10%), were found to have abdominal wall lesions. A total of 16 abdominal wall lesions were detected, located to surgical scars, stomas, drain and laparoscope ports. Additional findings on PET/CT in this group included liver metastases, intra-abdominal lesions and retroperitoneal lymph node involvement. In general, the patients in this small group were young with high grade tumours presenting in advanced stages. In conclusion, PET/CT appears to be a sensitive tool for the diagnosis of abdominal wall recurrence of CRC. The accuracy of localization afforded by the fused functional and anatomic images makes PET/CT a likely tool for diagnosing abdominal wall lesions, including port site metastases of other aetiologies.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 Conclusion
 References
 
Disease recurrence in the abdominal wall from a primary colorectal cancer is a poorly studied and little understood phenomenon. Aggressive resection of disease restricted to the abdominal wall and associated adherent viscera can result in local disease control with little morbidity and no mortality [1], yet abdominal wall metastases are often indicators of recurrent intra-abdominal cancer. Certainly, the timely diagnoses of abdominal wall lesions and possible concomitant intra-abdominal disease are crucial to optimize patient management.

Positron emission tomography (PET) with 18F-FDG allows functional imaging of malignant tissue. The well-documented mechanism of FDG uptake is based on increased glucose metabolism and increased expression of glucose transporters in malignant cells as compared with normal tissue. Thus, the metabolic rate of suspicious lesions as determined from PET can be used to define the presence and extent of active disease. While the sensitivity of dedicated PET has consistently been reported to be in the range of 85–100% for the detection of recurrent colorectal lesions the lack of anatomical detail affects image interpretation and remains a major limitation of PET. The combined PET/CT technique now helps overcome this drawback by providing fused images of functional PET and anatomic CT studies. The almost synchronous image acquisition and exact co-registration of anatomical and metabolic data improves the anatomic localization of PET abnormalities and reduces the number of equivocal PET interpretations [2–4]. PET/CT imaging has been found to increases the accuracy and certainty of locating lesions in colorectal cancer with a consequent improvement in staging and restaging accuracy from 78% to 89% [5].

This report describes the use of PET/CT in the detection of abdominal wall lesions, including port site metastases from colorectal carcinoma.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 Conclusion
 References
 
This was a retrospective evaluation of positive PET scans. Patients referred for PET/CT with a diagnosis of colorectal cancer were listed in a prospective database beginning 01/2004. Review of this database (10/2004) indicated 120 patients, 12 of whom (3 female, 9 male, aged 42–73 years, average 57 years) were found to have recurrent disease in the abdominal wall. The study population consisted of these 12 patients, who underwent 13 PET/CT scans. Primary disease was located in caecum (n = 3), transverse colon (n = 2), sigma (n = 4) and rectum (n = 3). All presented initially with advanced disease (all T3 or T4 according to TNM classification), and 10 of the 12 had moderate to poor tumour differentiation (1 was well differentiated, 1 unknown). Only 5 of the 12 had documented initial lymph node involvement. Three patients had intestinal perforations, yet there was no evidence of peritoneal spread at surgery. Three had liver metastases at presentation. All were reported to have clean surgical margins. Of the 12 patients, 8 had originally undergone open laparotomy, and 4 had laparoscope-assisted surgery (LAS). One patient (pt #4) had both LAS and open surgery, and also underwent two PET scans. The clinical data of these patients are summarized in Table 1Go.


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  		Table 1. Demographic and clinical data

 
All 12 patients presented at follow-up with clinical, radiological or laboratory findings suggestive of recurrent disease. Four patients were referred for PET/CT due to palpable masses, one had intestinal obstruction, one had CT findings suggestive of local recurrence and the remaining six were referred for PET/CT due to marker elevation. Patient #4 was referred both times due to palpable abdominal lesions.

The interval between initial surgical procedures and PET/CT for suspected recurrence in this group ranged between 4 months and 37 months, the average being 15 months. The indications for scan and intervals from surgery are presented in Table 2Go, together with PET/CT results.


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  		Table 2. Scan indications, recurrence time and PET/CT findings

 
PET/CT imaging protocol
All patients were imaged with a Gemini PET/CT Imaging System (Philips Co., USA) which provides three-dimensional acquisition, processing and display of CT, PET and PET/CT images, with 6.0 mm PET spatial resolution and a dual slice MX800 EXP CT scanner. Whole body PET/CT imaging was performed in fasting patients (4–6 h) following intravenous administration of 370 MBq (10 mCi) of 18F-FDG. Neither oral nor intravenous contrasts were administered. After a 60 min uptake period, during which patients were instructed to rest silently, images were acquired. First, a CT surview, (30 mA, 120 kVp, FOV 500 mm, length of scan 1.0–1.5 m with a speed of 100 mm s–1 and a spatial resolution of 1 mm) was performed from the orbital level to the level of the proximal thigh. This was followed by a dual slice CT (50 mAs per slice, 120 kVp, with a slice thickness of 6.5 mm, length of scan according to result of surview, with a bed speed of 20 mm s–1, rotation time of 0.75 s and a pitch of 1.5, and FOV of 600 mm). Finally, the acquisition of PET emission images was performed (2–3 min per bed position of 8.4 cm). The total acquisition time, accumulating between 100 and 150 million useful events, varied between 25 min and 35 min per patient. The CT data were used for attenuation correction of PET emission images. Non-attenuated data was reconstructed after scan acquisition was completed. Reconstruction of attenuation corrected data was executed concurrently. The lower limit of resolution of the PET system used is 0.45 cm.

Image interpretation
Both attenuation corrected and non-attenuation corrected scans were coregistered with the CT for interpretation using Syntegra (Version 2.0j, Philips) software. All studies were visually interpreted independently by individual physicians from the two specialties (Nuclear Medicine and Diagnostic Radiology). Studies were interpreted for PET alone and for combined PET/CT data. The low-dose non-enhanced CT data was used only in conjunction with PET data. Comparisons between the CT data and PET regarding contributions in the specific clinical context reported here were not made.

Evaluation of accuracy and statistical analysis
Results from combined PET/CT data were validated by comparison with concurrent contrast-enhanced CT, histopathological findings and at least 3 months of clinical follow-up. The contrast-enhanced CT scans used for comparison were not performed in our department, and were provided by the patients. PET/CT findings were interpreted on both lesion and patient levels, and determined to be true-positive (presence of cancer), or false-positive (increased FDG uptake unrelated to cancer). As the patients were selected on the basis of a positive PET result, there can be no meaningful assessment of true or false negatives.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 Conclusion
 References
 
A total of 16 abdominal wall lesions were detected in 13 scans performed in 12 patients. Three patients had 2 lesions each (pts 6, 11 and 4 who had 3 sites in 2 scans). The lesions ranged in size from 1.0–5x7 cm, with most (9/16) measured less than 1.5 cm. Intensity of 18F-FDG uptake was variable, yet the majority of lesions (10/16) had intense 18F-FDG avidity. The least uptake was observed in the smallest lesions.

All lesions were noted from PET findings and were subsequently localized anatomically by CT. Seven findings were localized to mid-abdominal surgical scars (1/7 in the site of a hernia), four localized to laparoscope insertion sites, two were in stomas and three in sites of surgical drains (1/3 in a hepatic drain site). The non-enhanced CT findings generally depicted heterogeneous nodular lesions, described as soft tissue masses with ill defined borders located near muscle. In some cases, fat infiltration was observed adjacent to the soft tissue mass, consistent with post-operative changes. No increased uptake of 18F-FDG was observed in any such region of fat infiltration. The abdominal lesions were divided nearly equally between open-surgery scars and drain/LAP sites. The lesions depicted essentially the same functional and anatomical characteristics (demonstrated in Figure 1Go). There were no suspicious findings on CT which were undetected by PET (no negative PET scans), and no CT findings which were below the resolution of the PET. All abdominal wall lesions were previously unreported.


Figure 1
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  		Figure 1. (a) Non enhanced CT demonstrates small irregularity in right anterior abdominal wall. (b) Attenuation-corrected PET image demonstrates focus of increased uptake of 18F-FDG in corresponding site in abdominal wall. The additional focus of intra-abdominal uptake on the right is due to physiological uptake in the ureter. (c) Fused PET/CT image yields functional and anatomic information.

 
Concomitant disease was present in 9 of 12 patients. The PET/CT findings demonstrated additional sites of active disease in 11 of 13 scans as follows: retroperitoneal lymphadenopathy (n = 1), intra-abdominal spread (n = 2), liver metastasis (n = 3) and local recurrence (n = 4), including repeated findings twice in pt #4. Findings from PET/CT are summarized in Table 2Go.

All PET/CT findings in this group were interpreted as true-positive, i.e. consistent with presence of cancer. Two abdominal wall lesions (pts #5 and #12) were highly suspicious clinically, while all other occult sites of abdominal wall and local recurrences were validated histologically.

The patient profile from the data of this small group included young age (8/12 below 60 years of age, of whom 5 were in their 50s), advanced disease at presentation (8/12 patients T3; 3/12 patients T4, and 1 unknown), with tumour differentiation being mostly moderate to poor.


   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
Conclusion
 References
 
Changes in tumour metabolism precede morphologic changes, and the functional information obtained from PET is therefore essentially independent of tumour location and size. The additional anatomic information provided by the CT contributed to the localization and characterization of lesions, thereby increasing the accuracy of the PET diagnoses. Overall, PET scanning has been reported to be contributory in the initial staging as well as in the evaluation of recurrent colorectal carcinomas. Recent works have reported the successful use of FDG-PET for the assessment of tumour aggressiveness, staging of disease, evaluation of treatment response, and the detection of recurrent disease [6]. While abdominal wall lesions and port site metastases are well documented entities, to the best of our knowledge the use of PET or PET/CT specifically addressing their diagnostic contribution has not been previously described.

Abdominal wall recurrences have been reported to occur in approximately 60% of patients with advanced colorectal cancer [7]. The importance of early and accurate diagnosis of such recurrence is not only in the localization of disease, allowing resection with curative intent, but also in the fact that abdominal wall metastases are often indicators of recurrent intra-abdominal cancer [7]. In the small study group evaluated here in fact, all but three patients (9/12 patients, in 11/13 scans) had additional sites of active disease. In three patients the additional sites were previously diagnosed by CT (in two patients referred for evaluation of palpable masses, and one with obstruction on previous CT) whereas previously unsuspected sites of disease were disclosed in another six patients. This finding is particularly striking as it was observed in the asymptomatic patients referred for evaluation due to elevated markers. In this subgroup, the lack of disease documentation on their previous CT was, in fact, the reason for referral to PET. When dividing our population into subgroups according to indication for the scan, this was also the largest subgroup.

Abdominal wall lesions, long recognized in surgical scars and stomas, have received renewed attention due to the recognition of port site metastases in patients following laparoscopic colorectal resections [1]. Although beneficial to the patient in the immediate post-operative period, the initial descriptions of port site lesions had put the adequacy of laparoscopic-assisted colectomy for tumour under question [8]. The incidence of port site metastases, however, is now recognized to be close to the incidence of wound metastases after open surgery [9]. Clinical evidence indicates that wound recurrence rates are 0.60% and 0.85% for open and laparoscopic colon cancer operations, respectively [10]. The group investigated here was derived from a larger group of 120 patients with suspected recurrent CRC, yet no evaluation of the entire population was performed, particularly regarding initial surgical procedure. Interestingly, however, the limited results in this small group indicate the abdominal lesions to be divided nearly equally between open-surgery scars and trocar/LAP sites. Excluding the two lesions localized to stomas, of the remaining lesions, half (7/16) were in incision sites from open surgery, and half (7/16) in trocar and laparoscope insertion sites. The lesions were essentially the same functionally and anatomically, and differed, in fact, only by location.

Increased uptake in stoma sites is frequently observed and well recognized. Physiological intestinal uptake is generally mild, but may be more increased if compounded by inflammation, complicating scan interpretation. Anatomic localization of the uptake by CT, and particularly the definition of soft tissue changes (nodular lesions, or infiltration) surrounding the stoma, allows clearer diagnoses with greater confidence when tumour is suspected. The retrospective evaluation of all post-operative CT images helps to discern physiological findings from pathology, including inflammatory changes (subcutaneous fat infiltration, or fluid collections suggestive of abscess).

Two tumours in stoma were demonstrated, and later pathologically proven, in the small group reported here. In both cases (pts 5 and 6) the uptake of 18F-FDG in the stoma was intense, yet could have been confused with inflammation. In these cases the additional anatomic information provided by the CT served to differentiate the findings from physiological uptake and inflammatory changes. The intensely increased 18F-FDG uptake, which was localized to ill-defined soft tissue masses in the abdominal wall surrounding the stoma, allowed for the diagnosis of viable tumour.

This is not a report on all CRC patients referred for PET/CT, but rather a retrospective evaluation of 12 patients with abdominal wall lesions. Only two patients presented with stoma lesions. No remarkable findings were noted in stoma sites in the remainder of the group (data not presented). As this is a report on the 12 patients with positive scans, there is also no information regarding the incidence of inflammatory uptake in stoma in the overall CRC population evaluated.

This report does not attempt to compare the contribution of PET/CT with that of CT in the context of abdominal wall lesions. Certainly, if abdominal wall lesions are large enough to be detected on conventional CT, and considering the high prevalence of concomitant disease in the presence of abdominal wall metastases, PET/CT may even be non-contributory and not cost-effective. Certainly, if the lesions, particularly intra-abdominal findings, are discovered (and duly reported) from CT, the PET may be unnecessary as curative options are limited. Our population was comprised of patients who presented at follow-up with clinical, radiological or laboratory findings suggestive of recurrent disease. Four patients were referred for PET/CT for evaluation of palpable masses, one had intestinal obstruction, one had equivocal CT findings suggestive of recurrence. The remaining six were referred for PET/CT due to marker elevation in the presence of "normal" CT.

Interestingly, while all abdominal wall lesions were at least 1 cm in size, and could have been identified on the concurrent contrast-enhanced CT, this was not the case. Unfortunately, missed diagnoses occurred. The PET consistently elucidated equivocal findings, and yielded "hot-spots" which easily directed attention to underlying lesions. The point which cannot be overstressed is that PET "shines the light" on small, sometimes overlooked, findings.

Port sites and open wounds are at equal risk of tumour implantation, with wound implantation affected mostly by the stage of the tumour and the operative techniques [10]. While our group is of limited size, and a complete demographic evaluation of the entire population (120 patients with suspected recurrent CRC) was not performed, a patient profile can be outlined. In general, the patients who developed abdominal wall recurrences were mostly young, and presented initially with advanced disease of moderate–poor differentiation. The general population (120 patients) from which this subgroup was derived includes patients in all age groups referred for evaluation, regardless of the stage of CRC at presentation. As such, this subgroup, with its relative homogeneity, is not representative of the entire population. While none were reported to have intra-abdominal dissemination at surgery, local spread of microscopic disease could not be excluded, particularly in two patients (pts #1 and 11, who presented initially with abscess, and peritonitis, respectively). As expected, the abdominal wall lesions were indistinguishable clinically whether they resulted in patients after open surgery or developed in port sites after laparoscope-assisted procedures.

The average time interval between resection of primary tumour and PET/CT diagnosis of recurrence was 15 months in this group (ranging 4–37 months). This is in keeping with anecdotal reports of abdominal wall recurrences. A case of a port site recurrence of colonic adenocarcinoma with diffuse peritoneal carcinomatosis was reported 1 month after laparoscopic-assisted right hemicolectomy, suggesting that intraperitoneal dissemination and tumour implantation on surgical wounds may have been the principal mechanism of recurrence after laparoscopic surgery [9]. In another case reported, a drain-site tumour recurrence was diagnosed 2 years after right colon resection for adenocarcinoma of the ascending colon [11].

Itano et al [12] reported on a patient who developed two subcutaneous metastases at two trocar sites. Multiple lesions in the abdominal wall, as observed in three of our patients (pt # 6, #11 and #4) are, therefore, also in keeping with the literature. While the patient group is too small to allow statistical evaluation, the fact that three out of 12 patients had multiple abdominal wall lesions is an interesting observation which may warrant further investigation and should, perhaps, be taken into consideration during follow-up of patients undergoing such procedures.

Of special interest is the lesion detected in the insertion site of a hepatic drain (pt #12). While a similar finding has been previously described, the occurrence is rare. A previous case has been reported in the literature of a colon carcinoma metastasizing to a port site following laparoscopic cholecystectomy has been reported. That case too was of an advanced tumour at the time of diagnosis, in an immunosuppressed patient, who developed clinical recurrence within 3 months of her procedure [13].

Previous reports of abdominal wall metastases after laparoscopic procedures for colorectal cancer have suggested the finding to be anecdotal [12–14]. In our group, however, 12 of 120 (10%) of those initially referred for investigation of suspected recurrent CRC had PET/CT findings consistent with abdominal wall lesions. Excluding the two lesions localized to stomas, of the remaining lesions half (7/16) were in incision sites from open surgery and half (7/16) in trocar and laparoscope insertion sites. This appears to be in keeping with large-scale studies that have shown the actual rate of port site metastasis to be similar to that observed in open surgery [12]. Furthermore, PET/CT disclosed concomitant findings in the vast majority (75%) of our, albeit small, group.

PET/CT is frequently indicated for the restaging of disease in CRC patients prior to metastasectomy. As limited disease is considered operable with curative intent, the scan is performed with hopes of demonstrating only limited disease, thereby allowing the planned surgery to proceed. While the presence of additional findings may contraindicate surgery, abdominal wall and port site metastases per se should not serve as contraindications, but, rather, should be considered for resection as well. The combined findings should be taken into consideration when planning treatment and the presence of a resectable abdominal wall lesion should not exclude surgery as an option.


   Conclusion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Conclusion
References
 
Although preventive measures have been proposed [9], it seems likely that abdominal wall lesions, including port site metastases, will continue to present diagnostic challenges. A well-documented complication after laparoscopic resection of intra-abdominal malignancies, port site metastases have been reported in various other clinical settings including breast cancer [15], gallbladder and bile duct cancer [16, 17], renal cell carcinoma [18], pancreatic cancer [19], upper gastrointestinal tract cancers [20] and gynaecological tumours including ovarian, cervical and endometrial cancer [21–23].

The metabolic images provided by PET scanning appear to have a high positive predictive value regarding the detection of abdominal wall metastases from colorectal cancer. The implementation of PET/CT will likely allow detection, characterization and anatomic localization of such occult lesions, as well as the diagnosis of additional concomitant lesions, in other clinical settings as well.

Received for publication August 10, 2005. Revision received November 1, 2005. Accepted for publication November 24, 2005.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Conclusion
 References
 

  1. Koea JB, Lanouette N, Paty PB, Guillem JG, Cohen AM. Abdominal wall recurrence after colorectal resection for cancer. Dis Colon Rectum 2000;43:628–32.[Medline]
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  8. Jacquet P, Averbach AM, Jacquet N. Abdominal wall metastasis and peritoneal carcinomatosis after laparoscopic-assisted colectomy for colon cancer. Eur J Surg Oncol 1995;21:568–70.[Medline]
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  12. Itano O, Watanabe T, Jinno H, Suzuki F, Baba H, Otaka H. Port site metastasis of sigmoid colon cancer after a laparoscopic sigmoidectomy: report of a case. Surg Today 2003;33:379–82.[Medline]
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  16. Nakagawa S, Tada T, Furukawa H, Abe M, Hatakeyama K. Late-type recurrence at the port site of unexpected gallbladder carcinoma after a laparoscopic cholecystectomy: report of a case. Surg Today 2000;30:853–5.[Medline]
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  18. Iwamura M, Tsumura H, Matsuda D, Kurosaka S, Yoshida K, Baba S. Port site recurrence of renal cell carcinoma following retroperitoneoscopic radical nephrectomy with manual extraction without using entrapment sac or wound protector. J Urol 2004;171:1234–5.[Medline]
  19. Jorgensen JO, McCall JL, Morris DL. Port site seeding after laparoscopic ultrasonographic staging of pancreatic carcinoma. Surgery 1995;117:118–9.[CrossRef][Medline]
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