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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 2  |  Issue : 3  |  Page : 196-202

Prognostic value of 18F-fluorodeoxyglucose-positron emission tomography/computed tomography scan volumetric parameters in head-and-neck cancer patients after treatment


1 Pediatric Respiratory Diseases Research Center, National Research Institute of Tuberculosis and Lung Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran
2 Chronic Respiratory Diseases Research Center, National Research Institute of Tuberculosis and Lung Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran
3 Lung Transplantation Research Center, National Research Institute of Tuberculosis and Lung Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran
4 Telemedicine Research Center, National Research Institute of Tuberculosis and Lung Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Date of Web Publication6-Sep-2018

Correspondence Address:
Dr. Abtin Doroudinia
Department of Radiology, PET-CT Unit, Masih Daneshvari Hospital, Niyavaran, Dar Abaad, Tehran
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/bbrj.bbrj_75_18

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  Abstract 


Background: A few studies have evaluated the predictive value of fluorodeoxyglucose-positron emission tomography/computed tomography (PET/CT) in patients with head-and-neck squamous cell carcinoma (HNSCC). Methods: We performed a retrospective study on 32 HNSCC patients, undergoing PET/CT after completion of planned treatment. The PET/CT volumetric parameters measured separately for primary tumor site and nodal or distant metastases. The primary outcome measure of the study was overall survival. Results: There was significant difference between alive and dead patients regarding some of volumetric parameters. Univariate and multivariate Cox regression analyses demonstrated association between metabolic tumor burdens with survival outcome. There was also significant difference in time to survival between patients with metastatic metabolic tumor burden and metastatic total lesion glycolysis (TLG) above and below 50th percentile. Conclusion: PET/CT volumetric parameters including metabolic tumor burden and TLG are significant prognostic markers for overall survival of patients with primary HNSCC after treatment.

Keywords: Head-and-neck squamous cell carcinoma, metabolic tumor volume, overall survival, standardized uptake value, total lesion glycolysis


How to cite this article:
Karam MB, Doroudinia A, Goodarzi SB, Kaghazchi F, Koma AY, Mehrian P, Alizadeh N. Prognostic value of 18F-fluorodeoxyglucose-positron emission tomography/computed tomography scan volumetric parameters in head-and-neck cancer patients after treatment. Biomed Biotechnol Res J 2018;2:196-202

How to cite this URL:
Karam MB, Doroudinia A, Goodarzi SB, Kaghazchi F, Koma AY, Mehrian P, Alizadeh N. Prognostic value of 18F-fluorodeoxyglucose-positron emission tomography/computed tomography scan volumetric parameters in head-and-neck cancer patients after treatment. Biomed Biotechnol Res J [serial online] 2018 [cited 2018 Sep 22];2:196-202. Available from: http://www.bmbtrj.org/text.asp?2018/2/3/196/240710




  Introduction Top


Head-and-neck cancer is the sixth most common type of cancer, representing about 6% of all cancer cases and accounting for estimated 650,000 new cancer cases and 350,000 cancer deaths worldwide each year.[1] Cancers of the head and neck arise from the mucosal lining of the oral cavity, oropharynx, hypopharynx, larynx, sinonasal tract, and nasopharynx. By far, the most common histological type is squamous cell carcinoma (SCC), accounting for 95% of cases.[2],[3] The clinical presentation of these lesions, their treatment, and prognosis are highly variable. They will depend on the tumor type, histological variant, and grade and are influenced by many clinical factors.[3],[4],[5] Up to 50% of head-and-neck SCC (HNSCC) patients will experience recurrence or residual disease even after therapy with curative intent.[6] The majority of recurrences occur within 3 years of completion of treatment.[7],[8] The overall 5-year survival for all stages is approximately 60%.[3]

Over the past decade, 18F-fluorodeoxyglucose-positron emission tomography/computed tomography (18F-FDG-PET/CT) has evolved as a valuable imaging modality for staging, treatment response evaluation, and surveillance for recurrence in patients with many human solid tumors.[9],[10],[11],[12],[13],[14],[15],[16] Studies have shown that FDG-PET/CT is highly sensitive and specific in the posttreatment setting.[2],[17],[18] In many HNSCC studies, PET/CT markers (standardized uptake value [SUV] and volumetric parameters) have been identified as valuable imaging biomarkers to assess treatment response and long-term survival.[3],[14],[19],[20],[21]

The purpose of our study was to establish the prognostic value of the volumetric FDG-PET parameters in head-and-neck cancer patients after treatment.


  Methods Top


Patient characteristics

This is a retrospective study approved by the Institutional Review Board and the need for written informed consent was obtained. Inclusion criteria included pathologically proven HNSCC, treated with either means of surgery, radiotherapy, and chemotherapy, and referred for FDG-PET/CT subsequently for treatment outcome assessment within 6–12 months after completion of treatment.[22]

The study group comprised 32 patients; 22 male (68.8%) and 10 female (31.2%); mean age of 53.2 ± 15.8 years, referred for FDG-PET/CT at our institution between January 2013 and March 2015 [Table 1]. All patients had been followed clinically by the end of March 2017. Mean follow-up time after FDG-PET/CT scanning was 31.9 ± 10.3 months. However, mean follow-up time after diagnosis of HNSCC was 53.9 ± 24.7 months.
Table 1: Patients characteristics

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Review of patients' medical records demonstrated that treatment regimen included 93.8% chemotherapy, 96.9% radiotherapy, and 43.7% surgery.

The chemotherapy regimen was variable and included either concurrent chemotherapy (n = 22) or induction chemotherapy followed by concurrent chemotherapy (n = 8). Chemotherapy agents included cisplatin, taxotere, 5-fluorouracil or cisplatin, and cetuximab. The radiation therapy regimen was also variable and on average included a total dosage of 60 Gy that was given in 30 fractions at a dose of 200 cGy per fraction over a course of 45 days. Surgical treatment was planned with curative intent in all occasions including; partial or total glossectomy (28.1%), total laryngectomy (9.4%), radical parotidectomy (3.1%), and radical tonsillectomy (3.1%). Radical or modified radical neck dissection had also been performed in these patients according to the characteristics of primary tumor.

Patient follow-up and outcome

Data collection included patient age, gender, overall stage at presentation; treatment received; and mortality data at last follow-up. Overall mortality was determined from either hospital medical records or contact with the patient him/herself or close relatives in case he/she had deceased. Time to overall survival was measured from the date of the original diagnosis of head and neck carcinoma (HNSCC) to the last follow-up in patients who were still alive or to the date of death for patients who had deceased. For all patients, including those who deceased, the mean length of follow-up was 53.9 ± 24.7 months and the median length of follow-up was 50 months (interquartile range [IQR], 38–61 months).

Positron emission tomography/computed tomographyprotocol

All PET/CT imaging were acquired using a Discovery 690 VCT (GE Healthcare, Milwaukee, USA) that is equipped with 64-slice CT (LightSpeed VCT). All patients fasted for at least 4–6 h before 18F-FDG-PET scanning and whole-blood glucose concentration was <150 mg/dl before 18F-FDG administration. Patients were injected with 4.5 MBq/Kg of FDG and the mean uptake time was 60 ± 10 min. All patients were scanned using a dedicated head and neck protocol as part of the standard clinical protocol. First, patients were scanned from the skull vertex to mid-thigh and scan time was set as 2 min per bed position. Dedicated head and neck images were acquired subsequently with the arms down and scan time was set as 3.0 min per bed position.

The ordered-subsets expectation maximization algorithm was used to reconstruct all PET images. All PET data were reconstructed with and without CT-based attenuation correction. Helical CT images were obtained with a matrix of 512 × 512. Beam collimation was 10 mm with a pitch of 1.0. Table speed was 10 mm/rotation and the slice thickness was 0.75 mm; 120 kV and 350 mAs were used.

Positron emission tomography/computed tomography image analysis

All PET/CT studies were electronically retrieved and reviewed on a 4.5 ADW GE workstation jointly by a board-certified nuclear medicine and radiologist with official PET/CT fellowship certification. The readers were blinded to clinical outcome. PET, CT, and fused PET/CT images were displayed in axial, coronal, and sagittal planes. The relevant imaging volumetric parameters were the maximum SUV (SUVmax), mean SUV (SUVmean), metabolic tumor volume (MTV), and total lesion glycolysis (TLG). All parameters were measured for each primary site (T), lymph nodal metastasis (N), and distant metastasis (M). MTV was defined as the tumor volume with FDG uptake segmented by a gradient-based method. Once the ROI was segmented, SUVmax, SUV mean, and MTV were automatically calculated by the ADW software. The TLG was calculated manually by multiplication of MTV and SUVmean of each lesion. We further calculated the total tumor burden (total MTV and total TLG) by combining the volumetric data from the primary tumor site, lymph node metastasis, and distant metastasis.

Statistical analysis

Central tendencies are presented as mean ± SD or as median (interquartile range-IQR) when data were skewed or as frequency and percentage for categorical variables. ROC analysis was performed for identifying the optimum thresholds. We presented survival as Kaplan-Meir survival curves with analysis performed using the Mantel-Cox log-rank test and Gehan–Breslow–Wilcoxon Test. Cox univariate and multivariate analyses were performed to adjust for important prognostic factors. A Mann-Whitney U test was performed to compare distribution of parameters between those who survived and those who deceased. We used the SPSS 20 (IBM) statistical packages for all analyses, and all hypothesis tests are two-sided with a significance level of 0.05.


  Results Top


The mean age (±SD) of our patients was 53.2 ± 15.8 years. [Table 1] illustrates the patients characteristics. Eighteen (56.3%) patients had American Joint Commission on Cancer stage IV cancer at the time of initial diagnosis and underwent no surgical intervention. The follow-up time from confirmed pathologic diagnosis was 53.9 ± 24.7 months. The follow-up time from the date of performing PET/CT was 31.9 ± 10.3 months.[23] By the end of follow-up time, 25 (78.1%) patients were still alive and 7 (21.9%) patients had deceased. The median length of follow-up for the study population from the time of diagnosis was 50 months (IQR, 38–61 months).[23] The volumetric FDG-PET/CT parameters in our study included; SUVmax, SUVmean, MTV and TLG which were calculated separately for primary tumor site (T), lymph node metastases (N), and distant metastases (M). Illustrative cases are provided in [Figure 1] and [Figure 2].
Figure 1: Deceased patient from widely metastatic disease with high volumetric parameters

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Figure 2: Deceased patient from recurrent disease and high volumetric parameters

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The most common primary tumor sites were the tongue (50.0%), nasopharynx (28.1%), and the larynx (9.4%). The primary tumor sites are summarized in [Table 1]. On the posttreatment PET/CT, there was no evidence of residual or recurrent FDG-avid disease at primary tumor site in 10 (31.3%) patients. PET/CT detected increased metabolic activity in primary tumor site in 22 (68.7%) patients. Mean values (±SD) for volumetric PET/CT parameters for primary tumor site are summarized in [Table 2].
Table 2: Patients positron emission tomography/computed tomography volumetric data mean values

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Regarding regional lymph node metastasis only 10 (31.3%) patients demonstrated increased metabolic activity on PET/CT. The most common lymph node station for metastatic lymph nodes includes jugulodigastric (level IIA/B) lymph nodes (28.1%). Mean values (±SD) for volumetric PET/CT parameters for regional lymph nodes are summarized in [Table 2].

Eighteen (56.3%) patients demonstrated evidence of distant metastatic disease on PET/CT images. The most common sites for distant metastasis were lungs (25.0%) and bones (15.6%). Mean values (±SD) for volumetric PET/CT parameters for distant metastases are summarized in [Table 2].

Values of MTV and TLG were finally calculated for the whole body including T, N, and M volumetric data. Mean values (±SD) for total MTV and total TLG were 50.25 (±78.48) and 227.95 (±328.76), respectively.

Comparison of FGD-PET/CT volumetric data in alive and deceased patients, considering mean values and IQR (Mann–Whitney U-test) [Table 3], demonstrated statistically significant difference between the two groups for M. MTV (P = 0.013), M. TLG (P = 0.013), total MTV (P = 0.00), and total TLG (P = 0.001).
Table 3: Mann-Whitney U-test demonstrating significance of positron emission tomography/computed tomography volumetric data. Statistically significant results are highlighted in yellow

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Univariate and multivariate Cox regression models

Age, gender, FDG metabolic parameters of primary tumor site (T. SUVmax, T. SUVmean, T. MTV, and T. TLG), lymph nodal metastasis (N. SUVmax, N. SUVmean, N. MTV, and N. TLG), distant metastasis (M. SUVmax, M. SUVmean, M. MTV, and M. TLG), and total tumor (total MTV and total TLG) were included in the univariate and multivariate Cox regression models for overall survival outcome.[24] In univariate statistical analyses, when stratified by overall survival status at the end of follow-up time; metastasis TLG (P = 0.009) and total MTV (P = 0.003) were significantly associated with overall survival outcome [Table 4].
Table 4: Univariate Cox regression analysis. Statistically significant results are highlighted in yellow

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We further studied the M. TLG and total MTV with exploratory multivariate models (forward stepwise) to identify whether the univariate results were an artifact due to possible confounding variables. We evaluated the association between M. TLG and outcome [Table 5] while controlling for each covariate individually. M. TLG remained significantly independent prognostic factor (P = 0.009) associated with overall survival when adjusted for age, gender, and FDG volumetric metabolic parameters.
Table 5: Multivariate Cox regression analysis (forward stepwise). Statistically significant results are highlighted in yellow

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Receiver operating characteristic analysis

Receiver operating characteristic (ROC) curves were performed to evaluate the accuracy of M. MTV, M. TLG, total MTV, and total TLG. These variables had been recognized to be significantly different in Mann–Whitney U-test [Table 3] to differentiate alive and deceased cases.

In ROC analysis for M. MTV variable (area under the curve [AUC]: 0.883, 95% confidence interval [CI], 0.689–1.00, P = 0.013), the median value was 10.38.

In ROC analysis for M. TLG variable (AUC: 0.883, 95% CI, 0.705–1.00, P = 0.013), the median value was 50.48.

In ROC analysis for total MTV variable (AUC: 0.986, 95% CI, 0.952–1.00, P = 0.00), the median value was 20.825.

In ROC analysis for total TLG variable (AUC: 0.925, 95% CI, 0.822–1.00, P = 0.001), the median value was 84.29.

Kaplan–Meier survival curves

Overall survival curves were compared using the Mantel–Cox log-rank test and Gehan–Breslow–Wilcoxon test. A significant difference in time to survival was observed between patients with metastatic MTV above and below the optimum threshold of 10.38 mL (Mantel–Cox log-rank test, P = 0.018 and Gehan–Breslow–Wilcoxon test, P = 0.007, HR = 0.169) [Figure 3].
Figure 3: Kaplan-Meier curve demonstrating significance of metastatic metabolic tumor volume for survival with cutoff value of 10.38. Statistically significant results are highlighted in yellow

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A significant difference in time to survival was also observed between patients with metastatic TLG above and below the median threshold of 50.48 (Mantel–Cox log-rank test, P = 0.004 and Gehan–Breslow–Wilcoxon test, P = 0.006, HR = 0.130) [Figure 4].
Figure 4: Kaplan−Meier curve demonstrating significance of metastatic total lesion glycolysis for survival with cutoff value of 50.48. Statistically significant results are highlighted in yellow

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  Discussion Top


Our study demonstrated that metastatic metabolic tumor volume (M. MTV), metastatic total lesion glycolysis (M. TLG), total MTV, and total TLG are significantly different between alive and deceased patients from HNSCC after treatment.

However, in univariate Cox regression analysis, the difference was significant for M. TLG and total MTV. Further statistical analysis with multivariate Cox regression model (forward stepwise) demonstrated significance of M. TLG for overall survival.

ROC analysis and Kaplan–Meier survival curves demonstrated that M. MTV and M. TLG are significant prognostic factors in HNSCC patients after treatment. We were also able to find cutoff values with statistical significance for these variables. We demonstrated that cutoff values >10.38 mL for M. MTV and 50.48 for M. TLG are associated with significantly worse survival outcome.

Head and neck cancers are particularly challenging to physicians because resectability, age, performance status, and patient wishes in the overall management strategy should be considered. In addition, the cost of treatment is also a very important factor because most therapies may fail to provide overall survival benefit. The value of PET/CT in restaging of head and neck cancers including identifying the distant metastasis is already established.[25] Evaluation of primary tumor site, regional, and distant metastases after treatment can be potentially valuable to predict patient's prognosis and tailor potential treatment options.

Several studies have shown that baseline SUVmax,[26] MTV,[27],[28] and TLG [29] are significant independent prognostic factors for survival in HNSCC. A few studies also have evaluated posttreatment SUVmax [22],[30] and posttreatment MTV [21] for prediction of disease-free survival and overall survival. Wong et al.[30] suggested that for every one unit increase in posttreatment SUVmax, the relative risk of death increases by 14%. Similarly, Murphy et al.[21] suggested that an increase in posttreatment MTV of 21 cm3 measured by the threshold segmentation method was associated with an increased risk of death.

In this study, we selected patients with HNSCC, referred for PET/CT scan within 6–12 after completion of their treatment including surgery, radiotherapy, and chemotherapy. We considered 6–12-month time window to minimize the effect of posttreatment inflammatory changes on the subsequent PET/CT images. We investigated the FDG volumetric parameters as well as SUVmax and SUVmean and we correlated the patients' survival outcome with metabolic quantitative PET/CT data. Our results suggest that metastatic MTV and metastatic TLG are markers for prognosis in patients with HNSCC after treatment. The total MTV and total TLG were also significantly different between alive and deceased patients. Our study results are consistent with other reports supporting the value of MTV and TLG as prognostic markers.[31],[32],[33],[34]

This study has a few limitations, including its retrospective design, heterogeneous treatment regimen, and relatively small sample size of 32 patients. The findings require to be validated in a larger prospective study. Because of the small numbers within each clinical stage, we did not stratify patients within each stage.


  Conclusion Top


Our study suggests that MTV and TLG when measured for metastatic sites and also for the entire body are potential markers for overall survival in patients with HNSCC after treatment. Our results require further validation in larger studies.

Acknowledgments

This article has been extracted from the thesis written by Ms. Sheida Bashiri Goodarzi MD in School of Medicine, Shahid Beheshti University of Medical Sciences. This study is conducted with the help of our valuable colleagues in Departments of Nuclear Medicine, Radiology, and Biostatistics in Shahid Beheshti University of Medical Sciences, Tehran, Iran. We really appreciate their kind cooperation as well.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
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