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EJSO xx (2017) 1e7 www.ejso.com

Incidental detection of colorectal lesions by FDG PET/CT


scans in melanoma patients
Christopher J. Young a,b,*, Assad Zahid a, Ian Choy a,
John F. Thompson b,c, Robyn P.M. Saw b,c
a
Department of Colorectal Surgery, Royal Prince Alfred Hospital, Camperdown, NSW, Australia
b
Discipline of Surgery, The University of Sydney, Sydney, NSW, Australia
c
Melanoma Institute Australia, The University of Sydney, Sydney, NSW, Australia
Accepted 7 September 2017
Available online - - -

Abstract
Background: Increased use of PET/CT scans in oncology patients has raised detection of Colorectal incidentalomas (CIs). The frequency
and diagnostic outcomes of identifying these lesions in melanoma patients have not previously been studied. This studies primary objective
was to determine the prevalence of CIs found on PET/CT scans in melanoma patients. The secondary objectives were to correlate the PET/
CT findings with the pathology found at colonoscopy, and identify which patients were referred for colonoscopy.
Methods: A retrospective analysis of patients identified from the prospectively collected research database of Melanoma Institute Australia.
2509 patients with melanoma underwent PET/CT scans between 2001 and 2013. The prevalence of CIs, the correlation of lesions, and the
survival of patients who underwent colonoscopy versus patients who did not were analyzed.
Results: The prevalence of CIs in melanoma patients who had PET/CT scans was 3.2%. Forty-five of the 81 (56%) patients with CIs un-
derwent colonoscopy. Of these, premalignant or malignant disease was found in 58%. Patients with previous metastatic melanoma were
significantly less likely to be referred for colonoscopy. Patients undergoing colonoscopy had significantly better survival, as did those
without previous distant metastases before the CIs were found, and those without any metastases at the time the CIs were found. These
factors were not significant on multivariate analysis.
Conclusion: The prevalence of incidental colorectal lesions identified on PET/CT scans in melanoma patients was found to be equivalent to
that in the general cancer population. Patients undergoing colonoscopy had better survival than those who did not.
Ó 2017 Elsevier Ltd, BASO ~ The Association for Cancer Surgery, and the European Society of Surgical Oncology. All rights reserved.

Keywords: Melanoma; FDG-PET; Colorectal lesions; Incidental; Surveillance

Introduction (PET) and low dose Computed Tomography (CT) PET/CT


scan is often used in the assessment and staging of many
Melanoma is an aggressive malignancy with the poten- types of cancer [2,3]. PET/CT imaging has also been shown
tial for metastasis to any organ system. While there is no to be useful in cancer surveillance for the detection of
role for routine imaging studies in patients with AJCC stage recurrent or metastatic disease [4e6]. Colorectal incidenta-
I and II disease, patients with stage III disease (clinically lomas (CIs) are unexpected colorectal findings detected on
positive lymph nodes or a pathologically positive sentinel imaging studies performed for other reasons [7]. The
lymph node (SLN)), often undergo extensive imaging increased use of PET/CT scans in oncology patients has
studies [1]. led to a corresponding increase in the number of CIs iden-
With high rates of sensitivity and specificity, an [18F] tified [7,8]. Incidental FDG uptake on these PET/CT scans
Fluorodeoxyglucose (FDG) Positron Emission Tomography has been reported as nodular-focal, nodular-multifocal,
segmental, or diffuse [9]. While segmental and diffuse up-
* Corresponding author. RPAH Medical Centre, Suite 415, 100 Carillon take patterns have been shown to be associated with a low
Avenue, Newtown NSW 2042, Australia. risk of malignancy, focal and multifocal nodular patterns
E-mail address: cyoungnsw@aol.com (C.J. Young).

http://dx.doi.org/10.1016/j.ejso.2017.09.012
0748-7983/Ó 2017 Elsevier Ltd, BASO ~ The Association for Cancer Surgery, and the European Society of Surgical Oncology. All rights reserved.

Please cite this article in press as: Young CJ, et al., Incidental detection of colorectal lesions by FDG PET/CT scans in melanoma patients, Eur J Surg
Oncol (2017), http://dx.doi.org/10.1016/j.ejso.2017.09.012
2 C.J. Young et al. / EJSO xx (2017) 1e7

have been associated with actual lesions, either benign, pre- colonoscopy. This study was approved by the MIA research
malignant, or malignant [9]. review board.
Previous studies have examined the occurrence of All PET/CT scans were performed at nationally ac-
benign and malignant CIs in cancer patients undergoing credited diagnostic radiology centers. Incidental colorectal
PET/CT scans [7], however the optimal management of lesions were defined, as in previous studies, as 1) FDG-avid
these patients remains unclear. Of the cancer patients lesions identified in a location that would not be an ex-
with findings suggesting a second primary malignancy, pected endpoint for a particular primary malignancy, 2)
less than 50% had a further evaluation for various reasons persistent activity in a distant site when the primary tumor
including low clinical suspicion, lack of patient follow-up or similar lesions had resolved or become significantly less
or advanced primary malignancy [10,11]. However, it has FDG-avid, or 3) incidental findings in sites not expected on
been proposed that even though PET/CT is associated the basis of the reason for ordering the PET/CT [13]. Any
with a high false positivity rate, patients with positive re- variations of uptake such as focal, segmental or diffuse
sults should be investigated [12e14]. In fact, multiple were reported by the radiologists and any concerns for sus-
studies have found that 71e86% of CIs were associated picious lesions were reported and further investigated.
with abnormalities found on colonoscopy [15e18] While We were unable to review the patients’ previous history
many of these reports discuss the issues regarding follow- of colonoscopy or fecal occult blood tests. There is a na-
up and clinical decision making when CIs are found tional fecal occult blood test screening program
[5,6,14], few of them provided management strategies for commencing at age 50 in Australia, but not a screening co-
incidental PET lesions found on PET/CT scans [13]. lonoscopy program.
One limitation of these previous studies is that their find-
ings were based on a broad range of oncology patients who Statistical analysis
underwent PET/CT scans. Moreover, there is no common
consensus as to what the best management practices should Continuous data were expressed as the mean  standard
be when CIs are detected on PET/CT scans for melanoma deviation (SD), or medians, as appropriate. Differences in
patients [14]. Given that melanoma patients present unique continuous variables were evaluated with Student’s t-test.
challenges in staging and management, a specific study of Categorical data were compared by the Fisher’s exact test
incidental PET/CT colorectal lesions in this patient popula- or Pearson’s chi-squared test, as appropriate.
tion was undertaken. Overall survival curves were constructed using the
To guide optimal management of melanoma patients Kaplan-Meier (K-M) method and compared by the log-
with incidental PET lesions, this study sought to determine rank test. Cox’s proportional hazard regression model
the frequency of incidental colorectal lesions found on with stepwise comparisons was used to analyze indepen-
PET/CT scans in melanoma patients, to identify which pa- dent prognostic factors. All analyses were performed in
tients were referred for colonoscopy, and to identify which IBM SPSS Statistics version 24.0 software package. A p-
factors, including age, gender and the presence or not of value <0.05 was considered significant.
metastatic disease influenced referrals.
Further objectives of this study were to provide a Results
descriptive account of the current management of mela-
noma patients with CIs and to compare the survival of pa- Between 2001 and 2013, 2509 of 16,755 melanoma pa-
tients who underwent colonoscopy with patients who did tients whose details were recorded in the MIA database
not. (15.0%) had PET/CT scans as part of their initial investiga-
tion for metastatic disease or routine surveillance of high-
risk disease. CIs were identified in 81 of the 2509 patients
Patients and methods (3.2%) (Fig. 1).
Of these 81 patients who were found to have a CI, 45
Patient population (56%) proceeded to undergo a colonoscopy and were in
the Colonoscopy Group (CG), while 36 (44%) were in
A total of 2509 patients with melanoma who underwent the non-Colonoscopy Group (NCG). The demographic
a PET/CT scan from 2001 to 2013 were identified from the data, primary tumor characteristics at the time of initial
Melanoma Institute Australia (MIA) database. This mela- melanoma presentation, and details regarding evidence of
noma research database is the largest global melanoma previous metastatic disease and at the time the CIs were
database. Patients who had CIs on their PET/CT were found is outlined in Table 1.
then identified and their clinical records examined in Of the 45 patients in the CG, the mean time to colonos-
further detail. Information extracted from the database copy after the CI had been identified on PET/CT was
and patient hospital records included what, if any, follow- 42.5  46.7 days. Of the 45 patients, 8 (18%) had a malig-
up was undertaken, whether or not a colonoscopy was per- nant colonic lesion. All 8 of these tumors were adenocarci-
formed, the results of the colonoscopy, and follow-up after nomas. Eighteen patients (40%) had premalignant lesions

Please cite this article in press as: Young CJ, et al., Incidental detection of colorectal lesions by FDG PET/CT scans in melanoma patients, Eur J Surg
Oncol (2017), http://dx.doi.org/10.1016/j.ejso.2017.09.012
C.J. Young et al. / EJSO xx (2017) 1e7 3

Fig. 1. Patient analysis flowchart. PET/CT ¼ [18F] Fluorodeoxyglucose Positron emission tomography/Computed Tomography.

(adenomatous polyps), 3 (7%) had benign lesions including With the absence of information regarding why patients
diverticula and colitis, and 16 (36%) had normal were referred for colonoscopy, the presence of metastatic
colonoscopies. disease in PET/CT scans performed before the discovery
The mean age at the time of initial primary melanoma of the CI did shed some light on the clinical pathway of
diagnosis was 60.5 years in the CG and 58.0 years in the melanoma patients. In the CG, 7 (16%) had evidence of
NCG (p ¼ 0.904). The mean age at the time of identifica- previous distant metastatic disease, while in the NCG, 20
tion of the CI was 63.8 years in the CG and 62.2 years in (56%) had evidence of previous distant metastatic disease
the NCG (p ¼ 0.888). The mean time from the initial diag- (p < 0.001). Similarly, we found that in the CG, 13
nosis of melanoma to the time of diagnosis of a CI by PET/ (29%) of patients had evidence of any previous metastatic
CT scan for all 81 patients was 4.4 years, while the average disease (regional, in transit or distant), compared with 28
time to diagnosis of a CI was 3.0 years in the CG and 3.7 (78%) in the NCG (p < 0.001).
years in the non-colonoscopy group (p ¼ 0.186). Survival curves were calculated for CG and NCG pa-
There was no significant relationship between gender tients (Fig. 2). Overall, the 81 patients had a median sur-
and colonoscopy group, with 8 (18%) women in the CG vival of 20.0 months and a mean survival of 31.5  3.8
and 9 (25%) women in the NCG (p ¼ 0.584). months. The mean survival time for patients in the CG
When comparing the presence of metastatic disease, as was 38.0  5.6 months and for patients in the NCG was
identified on PET/CT scans, 23 (51%) of patients in the 23.47  4.1 months (p ¼ 0.026) Univariate analysis also re-
CG had evidence of distant metastatic disease found at vealed a significant effect on survival for the presence of
the time of the CI, and 25 (69%) of patients in the NCG any metastases (in transit, nodal or distant) at the time
(p ¼ 0.115). Similarly, we found that in the CG, 32 the CI was found, and if there had been any previous distant
(71%) of patients had evidence of any metastatic disease metastases found. While these differences were significant
(regional, in transit or distant), compared with 28 (78%) on univariate analysis, the effects were not significant on
in the NCG (p ¼ 0.612). multivariate analysis (Table 2).

Please cite this article in press as: Young CJ, et al., Incidental detection of colorectal lesions by FDG PET/CT scans in melanoma patients, Eur J Surg
Oncol (2017), http://dx.doi.org/10.1016/j.ejso.2017.09.012
4 C.J. Young et al. / EJSO xx (2017) 1e7

Table 1
Clinicopathological factors for Colonoscopy Group (CG) and non-Colonoscopy Group (NCG) patients who had Colorectal incidentalomas (CIs) found on
PET/CT.
CG (n ¼ 45) NCG (n ¼ 36) P value between groups
Demographic data
Gender (male/female) 8/37 9/27 0.584
Age (years) at primary melanoma (PM) diagnosis 60.5  15.4 58.1  15.3 0.472
Age (years) at time of CIs found on PET/CT 63.8  13.7 62.2  14.4 0.609
Time (years) between PM diagnosis and CIs 3.0  4.6 3.7  6.6 0.591
Primary melanoma data
Location of tumor
Occult 5 (11%) 6 (17%) c2 [6] ¼ 6.2, p ¼ 0.406
Head 5 (11%) 7 (19%)
Neck 2 (3%) 4 (4%)
Thorax 14 (31%) 7 (19%)
Abdomen 2 (4%) 2 (6%)
Upper extremity 8 (18%) 2 (6%)
Lower extremity 9 (20%) 8 (22%)
2009 AJCC Stage
I 8 (18%) 10 (28%) c2 [3] ¼ 1.2, p ¼ 0.756
II 18 (40%) 13 (36%)
III 15 (33%) 10 (28%)
IV 4 (9%) 3 (8%)
Clark Level
1 0 (0%) 1 (3%) c2 [4] ¼ 4.8, p ¼ 0.310
2 1 (2%) 1 (3%)
3 5 (11%) 7 (19%)
4 24 (53%) 11 (31%)
5 9 (20%) 4 (11%)
Unknown 6 (13%) 12 (33%)
Average thickness (mm) 4.2  4.0 3.2  3.2 0.274
Ulceration (Yes/No) 13/32 10/26 1.0, FET
Mitosis/mm2 7.7  6.6 5.7  4.4 0.200
Metastatic disease (MD) data
Distant MD at time CIs found (Yes/No) 23/22 25/11 0.115, FET
Intransit/nodal/distant MD at time CIs found (Yes/No) 32/13 28/8 0.612, FET
Previous distant MD before CIs found (Yes/No) 7/38 20/16 <0.001, FET
Previous intransit/nodal/distant MD before CIs found (Yes/No) 13/32 28/8 <0.001, FET
FET (Fisher’s exact tests).

Discussion Kei 2010 [16] reported an average time between PET/CT


and follow up colonoscopy of 1.3 months (41 days). Docu-
In this study the prevalence of CIs detected on PET/CT menting the time for patients to undergo follow up colonos-
scans performed in melanoma patients was 3.2%. This is copy can help establish standards for patient care.
similar to the prevalence of CIs in a meta-analysis by Tre- While the difference in the presence of in transit, nodal
glia [7] of 32 studies (totaling 89,061 patients) which found or distant metastatic disease in the CG, when compared
the pooled prevalence of CIs detected on PET/CT scans with the NCG group was not statistically significant, there
was 3.6% for all cancer types. While none of the studies was a significantly worse overall survival for patients with
identified in a literature review looked at melanoma pa- such metastases. Patients with previous melanoma metasta-
tients specifically, our results suggest that the prevalence ses were significantly less likely to be referred for colonos-
of CIs detected on PET/CT scans for melanoma patients copy, and those with previous distant metastases had a
is similar to the broader population of oncology patients. worse survival.
Of the 81 melanoma patients who were found to have a The survival analysis found that patients who under-
CI, 56% (45 patients) underwent colonoscopic assessment. went colonoscopy after a CI was found on PET/CT had
The risk of premalignant or malignant disease in our study a longer survival than patients who did not undergo a co-
was 58%, which is slightly less than the pooled risk of 68% lonoscopy. However, there may be no causal link between
for malignant or pre-malignant CIs calculated in Treglia’s colonoscopies and survival. Indeed, the analysis suggests
[7] meta-analysis. that patients who did not undergo a colonoscopy may
On average, patients underwent a colonoscopy 43 days have had significantly more advanced melanoma disease
after a CI was detected on a PET/CT scan. While very burden, so that further investigation of CI was considered
few studies, including the meta-analysis, looked at this, inappropriate.

Please cite this article in press as: Young CJ, et al., Incidental detection of colorectal lesions by FDG PET/CT scans in melanoma patients, Eur J Surg
Oncol (2017), http://dx.doi.org/10.1016/j.ejso.2017.09.012
C.J. Young et al. / EJSO xx (2017) 1e7 5

Fig. 2. The comparison of survival for melanoma patients with incidental colorectal lesions found on FDG PET/CT scan, 45 patients in the Colonoscopy
Group (CG) and 36 patients in the non-Colonoscopy Group (NCG).

While we were unable to determine from our data the melanoma should continue to receive colonoscopies like for
exact reasons why patients were or were not referred for the general population if the patient and diseases factors do
further investigation of their CI, our results suggest that not preclude it.
the prior presence of metastatic disease impacts whether Many previous studies have discussed the role of the
or not physicians choose to investigate CIs. treating specialist’s clinical judgment in deciding whether
There was a statistically significant difference regarding to investigate a CI found on a PET/CT scan and two points
metastatic burden between the CG and NCG at the time of of view are apparent. On the one hand, Agress et al. [6]
CI diagnosis. This may have influenced the need for further found that the referring physician was also focused on the
investigation due to multiple foci of disease. On reviewing primary disease and that often follow-up of the incidental
the PET scan reports, it was noted that in the colonoscopy PET finding was a relatively low priority. Wang et al.
group, all but one patient were reported to have a focally [11] and Beatty et al. [13] also found that follow-up evalu-
avid lesion in the colon while one was reported as diffuse. ation was not recommended except when confirmation of
In the non-colonoscopy group, patients were noted to have malignancy would significantly alter curative potential.
more disease burden elsewhere, however the reports of the Evens-Sapir et al. [5] declared that there was a direct asso-
colonic avid lesions were less defined, and some lesions re- ciation between the incentive of the referring physician to
ported as diffuse and hence non-specific. This may have evaluate a focal lesion and the decision of whether to treat
also impacted on referral for colonoscopy. There are the lesion if it was found to be malignant. These authors
many patient and disease factors with melanoma patients suggested that evaluation of CIs is not necessarily a high
that mitigate the focus or not on other disease entities. priority in the presence of metastatic disease. From this
But in general, we recommend that patients with metastatic perspective, one possible interpretation of our data would

Please cite this article in press as: Young CJ, et al., Incidental detection of colorectal lesions by FDG PET/CT scans in melanoma patients, Eur J Surg
Oncol (2017), http://dx.doi.org/10.1016/j.ejso.2017.09.012
6 C.J. Young et al. / EJSO xx (2017) 1e7

Table 2
Survival analysis of prognostic factors by cox hazard model.
Univariate analysis P value Multivariate analysis P value
Odds ratio (95% CI) Odds ratio (95% CI)
Colonoscopy Group (Yes/No) 2.485 (1.117e5.531) 0.026 1.947 (0.812e4.670) 0.135
Gender (female/male) 1.330 (0.458e3.863) 0.600
Age at PM diagnosis (60/>60) 1.832 (0.828e4.054) 0.135
Age at CI find (64/>64) 1.848 (0.853e4.006) 0.120
Location of PM 0.838 (0.697e1.008) 0.061
2009 AJCC Stage of PM 1.341 (0.826e2.178) 0.235
Clark Level of PM 0.775 (0.447e1.342) 0.362
Ulceration of PM (Yes/No) 0.741 (0.341e1.613) 0.451
Distant MD at time CIs found (Yes/No) 0.566 (0.240e1.337) 0.194
IND MD at time CIs found (Yes/No) 0.286 (0.86e0.948) 0.041 0.337 (0.100e1.137) 0.080
Previous distant MD before CIs found (Yes/No) 0.420 (0.199e0.886) 0.023 0.639 (0.279e1.462) 0.289
Previous IND MD before CIs found (Yes/No) 0.435 (0.184e1.025) 0.057
PM ¼ primary melanoma, CI ¼ colorectal incidentaloma, MD ¼ Metastatic disease, IND¼Intransit/nodal/distant.

be that very few patients had colon cancer, and that follow- who underwent colonoscopy or did not undergo colonos-
up with colonoscopy may not be necessary. copy might be useful, though this may not be possible
However, alternatively, Pandit et al. [4] proposed that with the limited cohort numbers.
because of the high incidence of premalignant and malig- Melanoma can, in many cases, be an aggressive malig-
nant conditions identified as CIs, further diagnostic workup nancy. Routine PET/CT imaging during the management
was indicated. Kamel et al. [15] found that early detection of the disease has led to an increase of CI findings in these
of a second primary tumor did improve the overall survival patients. Some authors have suggested that colonoscopy is
outcome of patients and that colonoscopy was indicated. associated with an unnecessary risk and little or no benefit.
The results of Lee et al. [14] support the need for colono- However, given the rates of incidental malignant and prema-
scopic verification, while also emphasizing that cost, lignant lesions, we propose that colonoscopy is indicated in
procedure-related complications and clinical status, patient patients with suspicious lesions. Our results suggest that if
performance and the likely additional benefit of further CIs are identified in PET/CTs scans of patients with mela-
management should all be considered by the referring noma, a colonoscopy may have an impact on their survival.
physician before further screening. These authors suggested
that follow-up evaluation of CIs is indicated because of the Conflicts of interest
high incidence of premalignant and malignant conditions in
this population. We have no commercial interests and no sources of sup-
In melanoma patients, the issue of co-existing metastatic port to declare.
disease is particularly relevant given their extremely poor
prognosis. As the first group of studies indicated, a colonos-
copy would not be likely to benefit and could harm patients Acknowledgements
with advanced metastatic disease. However, given the high
rates of identifying malignant and premalignant lesions (com- No grant support needs to be declared.
bined 58%) in melanoma patients in this study, we suggest
that colonoscopy is indicated in most cases. In spite of the
aggressive nature of melanoma, our survival analysis demon-
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Please cite this article in press as: Young CJ, et al., Incidental detection of colorectal lesions by FDG PET/CT scans in melanoma patients, Eur J Surg
Oncol (2017), http://dx.doi.org/10.1016/j.ejso.2017.09.012
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Please cite this article in press as: Young CJ, et al., Incidental detection of colorectal lesions by FDG PET/CT scans in melanoma patients, Eur J Surg
Oncol (2017), http://dx.doi.org/10.1016/j.ejso.2017.09.012

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