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10.1245/ASO.2006.02.007
Annals of Surgical Oncology 13:919-926 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Level of Fluorodeoxyglucose Uptake Predicts Risk for Recurrence in Melanoma Patients Presenting With Lymph Node Metastases

Esther Bastiaannet, MSc1, Otto S. Hoekstra, MD, PhD2, Wim J. G. Oyen, MD, PhD3, Piet L. Jager, MD, PhD4, Theo Wobbes, MD, PhD5 and Harald J. Hoekstra, MD, PhD1

1 Department of Surgical Oncology, Groningen University Medical Center and University of Groningen, P.O. Box 30.001, 9700 RB Groningen, The Netherlands
2 Nuclear Medicine & PET Research, VU University Medical Center Amsterdam, Amsterdam, The Netherlands
3 Department of Nuclear Medicine, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
4 Nuclear Medicine & PET Center, Groningen University Medical Center, Groningen, The Netherlands
5 Department of Surgical Oncology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands

Correspondence: Address correspondence and reprint requests to: Harald J. Hoekstra, MD, PhD; E-mail: h.j.hoekstra{at}chir.umcg.nl.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The incidence of malignant melanoma has increased. Identification of additional prognostic factors may allow the development of individualized strategies. This multivariate analysis was undertaken to evaluate the potential role of the standard uptake value (SUV) in predicting disease-free and overall survival in melanoma patients with lymph node metastases.

Methods: All melanoma patients with palpable lymph node metastases who where referred for a fluorodeoxyglucose positron emission tomography scan were eligible. The SUV in the lymph node metastasis was calculated. Data were analyzed (Kaplan-Meier), and differences in cumulative survival and the disease-free rate were assessed (log-rank test). Univariate and multivariate analyses (Cox proportional hazard model) were performed to determine independent prognostic factors.

Results: There was no statistical difference in survival for the 38 patients with a high or low SUVmean (P = .11). However, a significant difference was found in disease-free survival (P = .03). Ulceration of the primary melanoma (P = .023) was an independent predictor of survival. For the disease-free survival, multivariate Cox regression showed adjuvant radiation (P = .001), localization of the primary melanoma (P = .017), and a high SUVmean (P = .009) as independent prognostic factors.

Conclusions: Disease-free survival of melanoma patients was prolonged in those with a low SUVmean value (P = .03) in their lymph node metastasis, as compared with those with a high SUVmean. However, this difference was not found for overall survival. In multivariate analysis, high SUVmean was an independent prognostic factor (P = .009) for disease-free survival. Prospective research should determine whether patients with a high FDG uptake in melanoma lymph node metastases could benefit from adjuvant radiation treatment or chemotherapy.

Key Words: Fluorodeoxyglucose-Positron emission tomography • Standard uptake value • Melanoma • Lymph node metastases • Survival • Disease-free survival


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Cutaneous melanoma is among the malignant tumors with the most rapidly increasing incidence rates in white populations.1 In 2000, the incidence in The Netherlands was 14 per 100,000, which is an increase of 38% compared with 1990; this represents the highest increase of the 10 most common cancers in The Netherlands. As a result of increased awareness and surveillance, melanoma is now diagnosed at an earlier stage of disease. Nevertheless, some patients with melanoma still present with or experience recurrence with locoregional metastases (American Joint Committee on Cancer stage III). Surgical excision of the primary tumor and a therapeutic lymph node dissection remain the standard of care for these patients.

Many melanoma patients with lymph node metastases die as a consequence of distant metastases, usually in less than 3 years, despite lymph node dissection with a curative intent. Locoregional recurrences (stage III) are often difficult to treat, and treatment may result in substantial morbidity, such as ulceration and disfigurement. The number of node metastases, the size of metastatic nodes, extracapsular extension, the number of involved nodal basins, and ulceration of the primary tumor are the most significant prognostic factors in stage III melanoma patients.1–9 However, patients with the same clinicopathologic parameters can still have a different outcome of treatment, regional control, and survival. Identification of additional prognostic factors may allow the development of individualized strategies that may lead to improved results.

Positron emission tomography (PET) allows an assessment of tumor physiology by determining the uptake of radiolabeled tracers.10 Fluorodeoxyglucose (FDG) is a radiolabeled glucose analogue that is taken up by cells through the glucose transporter. It is subsequently phosphorylated intracellularly by hexokinase and trapped in the cells. FDG distribution within the body is thus a measure of glucose metabolism, which is increased in cancer cells.11 Several studies have shown the value of FDG-PET in melanoma patients. A systematic review and meta-analysis revealed that FDG-PET is accurate for the detection of distant and regional lymph node metastases.12 For regional staging, subgroup analysis showed a better accuracy of FDG-PET in stage III melanoma compared with stage I and II disease.

To assess the degree of FDG accumulation, the standardized uptake value (SUV) is a popular index in different cancers. Studies in breast cancer, head and neck carcinoma, pancreatic cancer, lung cancer, and sarcoma showed that patients with high FDG uptake had a significantly lower disease-free and overall survival. The SUVmean and SUVmax turned out to be significant prognostic factors in several univariate and multivariate analyses.13–20 However, studies have also been published in which the SUV had no prognostic value with respect to disease-free or overall survival.18,21

Although FDG-PET has adequate sensitivity and specificity in staging melanoma, no study has focused on the prognostic value of FDG uptake in melanoma patients.22–26 By using retrospective data, this analysis was undertaken to evaluate the potential role of the SUV in predicting disease-free and overall survival in melanoma patients with lymph node metastases.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
All melanoma patients with palpable lymph node metastases who were referred for FDG-PET to Groningen University Medical Center or Radboud University Nijmegen Medical Centre from 1999 to 2004 were eligible for this study. In all patients, the lymph node metastases had to be cytologically proven and untreated before FDG-PET. Patients were included in the study if FDG-PET could be evaluated with the provided software and if they had a lymph node dissection after the FDG-PET. The medical records of these patients were reviewed, and the following information was retrieved: age, sex, treatment, FDG-PET result, interval from the occurrence of the primary melanoma, characteristics of the primary melanoma (localization, Breslow thickness, and ulceration), and characteristics of the lymph node metastases (localization, extranodal growth, and number of lymph nodes). We recorded the number of days of follow-up and, if a patient died or experienced disease recurrence, the days until death (primary end point) or until recurrence (secondary end point). Follow-up was the same for all patients; physical examination in the 1st year every 3 months, in the 2nd year every 4 months, in the 3rd to 5th year every 6 months, and in the 6th to 10th year once a year, with a chest radiograph every year. PET and computed tomographic scans were performed only if there was a suspicion for recurrence according to the physical examination or chest radiograph. Tumor recurrence events could be recurrence in the lymph nodes or metastatic disease and had to be cytologically or histologically proven.

Positron Emission Tomography
In Nijmegen, FDG was obtained commercially from Mallinckrodt Medical, Petten, The Netherlands. In Groningen, FDG was synthesized on site according to Hamacher et al.27 by an automated synthesis module. Before PET imaging, patients were instructed to fast for at least 6 hours, after which FDG was injected intravenously. Patients were instructed to drink 1 L of water before imaging, to stimulate FDG excretion. Whole-body imaging was performed in the two- or three-dimensional mode, with emission scans of 4 to 10 minutes per bed position, starting 1 hour after the injection of FDG. In Nijmegen, a dedicated, rotating half-ring PET scanner (ECAT-ART; Siemens AG, Erlangen, Germany) was used for data acquisition from 1999 to 2001; thereafter, an ECAT EXACT (Siemens/CTI) was used. In Groningen, an ECAT 951/31 or an ECAT HR+ scanner (Siemens/CTI) was used for data acquisition. Data were iteratively reconstructed (ordered subsets expectation maximization). In both centers, FDG-PET was read by using a computer display. All clinical information was available when reading the FDG-PET scans.

Standard Uptake Value
The SUV depends on the amount of injected radioactivity, the patient’s weight, and the calibration factor of the camera and is calculated according to the following formula:


Formula

Three-dimensional regions of interest were placed semiautomatically by using a dedicated software program over the tumor on multiple slices, by using a threshold of 70% of the maximum pixel value within the tumor. The SUVmean and SUVmax in the lymph node metastasis were calculated; SUVmean reflects the mean value over all voxels, and SUVmax reflects the maximum SUV value in the tumor. If there was more than one metastasis in the lymph node basin, the lesion with the most intense uptake was chosen.

Data Analysis
The relationships between SUV and patient characteristics were assessed by Student’s t-test or analysis of variance, as appropriate. Patients were divided into two groups according to the SUVmean and SUVmax for the survival analysis. In the absence of an established cutoff point, we chose the median SUVmean and median SUVmax.

Data were analyzed by using the Kaplan-Meier method, and the differences in the cumulative survival rate and disease-free rate were assessed by using the log-rank test. Univariate and multivariate analyses (Cox proportional hazard model) were performed to determine independent prognostic predictors. All variables with P < .2 in the univariate analysis were entered in the multivariate analysis. All P values are two tailed and significant if P ≤ .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
FDG-PET and the medical records of 38 patients were reviewed. Twenty patients were male, and 18 were female; the mean age was 54 years (range, 28–86 years). Lymph node dissection was performed in all patients, of whom 35 showed no distant metastases on the FDG-PET scan. The median time from the primary melanoma to the presentation of the lymph node metastases was 289 days (range, 0–6117). The primary melanoma was located at the lower limb (47.4%), trunk (31.6%), head and neck (7.9%), unknown location (10.5%), and upper limb (2.6%). The lymph node metastases were located in the groin (52.6%), in the axilla (34.2%), and in the neck (13.2%). The median SUVmax was 6.0 (range, 1.0–20.6), and the median SUVmean was 5.2 (range, .9–16.7). The median follow-up time after FDG-PET scanning was 257 (range, 27–1813) days. At last follow-up, 25 patients were alive, and 13 had died as a result of melanoma metastases. In the follow-up period, 17 patients developed a recurrence.

Patient and melanoma characteristics and comparisons of SUVmax and SUVmean in each group are listed in Table 1Go. There were no significant differences in SUVmax or SUVmean for the different characteristics. For the survival analysis, patients were divided into two groups according to the median value of the SUVmax or SUVmean; these groups showed no difference in participation, and the SUVmean was used for further analysis. As shown in Fig. 1Go, there was no statistical difference in survival for patients with a high or low SUVmean (P = .11). However, as shown in Fig. 2Go, disease-free survival was significantly longer for patients with a low SUVmean (P = .03).


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  		TABLE 1. Standard uptake value (SUVmax and SUVmean) and patient or melanoma characteristics
 

Figure 1
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  		FIG. 1. Kaplan-Meier overall survival for patients with a high SUVmean or low SUVmean SUV, standard uptake value.

 

Figure 2
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  		FIG. 2. Kaplan-Meier disease-free survival for patients with a high SUVmean or low SUVmean. SUV, standard uptake value.

 
Univariate survival and disease-free survival analysis for various patient characteristics is shown in Table 2Go. The cumulative survival rate was significantly decreased in patients with the primary melanoma located on the head or with an unknown primary tumor location (P = .0005), although the numbers are too small to draw conclusions.


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  		TABLE 2. Univariate survival analysis
 
The cumulative disease-free survival rate was significantly decreased for patients who received no adjuvant radiation (P = .03), patients with the primary melanoma located on the head and neck, those with an unknown primary tumor location (P < .00005, although numbers were too small to draw conclusions), and patients with a high SUVmean (P = .03).

Because of possible interrelationships between prognostic factors, multivariate analysis was performed. All variables with P < .2 in the univariate analysis were entered in the multivariate analysis. For survival, these were localization of the primary melanoma, ulceration, localization of the lymph node metastases, extranodal growth, and SUVmean. For disease-free survival, these were sex, time from the primary melanoma, localization of the primary melanoma, recurrence or not, extranodal growth, adjuvant radiation, and SUVmean. Multivariate Cox regression for survival showed that ulceration of the primary melanoma (P = .023) was an independent predictor of survival. For the disease-free survival, multivariate Cox regression showed localization of the primary melanoma (P = .017, although there were too few patients to draw conclusions), adjuvant radiation (P = .001), and a high SUVmean (P = .009), with a hazard ratio of 8.2, as independent prognostic factors.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The prediction of disease-free and overall survival of patients with lymph node metastases of melanoma is usually based on the number of lymph nodes and extranodal growth. However, patients with the same clinicopathologic parameters can show differences in survival and disease-free rates. Identification of factors predictive of outcome in melanoma patients is of potential interest, because it may allow adjuvant therapy tailored to the characteristics of individual tumors.13

This study showed a difference in the disease-free survival (P = .03) in patients with high or low SUVmean values, although a statistical difference for survival was not found in these patients with lymph node metastases after surgery with a curative intent. Also, a high SUVmean value was an independent prognostic factor (P = .009) in the multivariate disease-free survival analysis.

There are no data in the literature concerning the relationship between SUV and survival or disease-free survival in melanoma patients. However, in head and neck cancer patients treated with radiotherapy, SUV was found to have potential value in predicting local control and disease-free survival.13 Similar to this study, no difference in overall survival was found. Consequently, high FDG uptake may be a useful parameter for identifying patients who may benefit from adjuvant systemic treatment. In another study of 143 patients with previously treated head and neck squamous cell carcinoma, SUV proved to be an independent predictor of relapse-free and overall survival in a multivariate proportional hazards model.11 Also, in sarcoma, the multivariate analyses showed that the SUVmax information was a statistically significant independent predictor of sarcoma patient survival and disease progression.20 One of the few prospective studies showed that a high uptake of FDG was associated with advanced disease and poor survival in patients with head and neck cancer.16

Studies in patients with pancreatic cancer, prostate cancer, and gastric cancer have shown that the SUV is an important prognostic factor.10,17,28,29 A systematic review showed good evidence that FDG uptake on PET had independent prognostic value in newly diagnosed non–small-cell lung cancer.30 Two studies did not observe this prognostic value of SUV. In 38 patients with primary non–small-cell lung cancer, the tumor FDG uptake did not independently predict the prognosis.18 Also, in a study of 40 patients with newly diagnosed cancer of the esophagus or gastroesophageal junction, SUV was not useful as an independent predictor of survival.21

FDG-PET is useful is distinguishing benign from malignant tumors in the diagnosis of different cancers. An accelerated rate of glucose transport and an increased rate of glycolysis are among the most characteristic biochemical markers of malignant transformation.17 FDG is a glucose analogue that is actively taken up by Glut-1 into the cell and phosphorylated by hexokinase during the first step of the glycolytic pathway. However, FDG cannot be further processed and becomes trapped within the cell.

Two meta-analyses reported an overall sensitivity of FDG-PET in detecting melanoma of 92% and 79%, with a overall specificity of 90% and 86%.12,31 These overall values indicate the potential benefits of using FDG-PET as a diagnostic management tool. Furthermore, in a study in 257 melanoma patients, it was found that FDG-PET had the highest value in staging patients with locoregional metastases for detection or exclusion of distant metastases; it changed surgical treatment in 37% of the patients.32 Predicting the response to treatment through the measurement of increased glucose metabolism, the uptake of FDG may be of potential value. In this study, we analyzed FDG uptake in the lymph node metastases of melanoma patients. Obviously, the effect of these findings is limited because of the retrospective design in a limited number of patients. However, this study can serve as the basis for a prospective study on the value of SUV in the disease-free survival and overall survival of melanoma patients with lymph node metastases (American Joint Committee on Cancer stage III).

Despite the advantage of calculating an SUV from a noninvasive pretreatment PET study, SUV values are subject to many sources of variability, such as the timing of PET acquisition after tracer injection, patient size, region of interest definition, partial volume, and image reconstruction.17,33–37 Although we realize that there is variation in the scanners (two-dimensional, three-dimensional, partial, and full ring scanners), our approach was based on the use of commercially available software to prevent different ways of calculating the SUVs in the two centers.

There is currently no consensus on the optimal methodology for objective quantitative measurement of FDG uptake.38 Regarding the SUV, no diagnostic threshold has been clearly established for distinguishing uptake in malignant or benign tissues, and in cancer cases, no cutoff has been established for defining subgroups of different prognosis.13 Additional prospective studies need to be performed to determine these values. Regarding the prognostic value of FDG-PET, the main question concerns the possible added value of FDG uptake intensity versus other known prognostic indicators.13 Current evidence suggests that the intensity of FDG uptake correlates less clearly with tumor burden than with biological aggressiveness.13 FDG uptake has been found to be associated with cell viability and particularly with cell proliferative activity.39–41

In conclusion, disease-free survival in patients with a high SUVmean is significantly lower than in patients with a low SUV. However, this difference is not reflected in differences in overall survival. In the multivariate analysis, a high SUVmean proved to be an independent prognostic factor for disease-free survival in melanoma patients with lymph node metastases. Prospective research should determine whether patients with a high FDG uptake in melanoma lymph node metastases could benefit from adjuvant radiation treatment or chemotherapy.

Received for publication February 8, 2005. Accepted for publication January 2, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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