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Holgado A, León X, Quer M, Camacho V, Fernández A. Association between maximum standarised uptake value (SUV) and local control in patients with oropharyngeal carcinoma treated with radiotherapy. ACTA OTORRINOLARINGOLOGICA ESPANOLA 2023; 74:211-218. [PMID: 37149130 DOI: 10.1016/j.otoeng.2022.05.001] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/06/2022] [Accepted: 05/19/2022] [Indexed: 05/08/2023]
Abstract
OBJECTIVE To analyse the prognostic ability of the maximum standardised uptake value (SUVmax) on local disease control in patients with oropharyngeal carcinoma treated with radiotherapy. MATERIAL AND METHODS Retrospective study of 105 patients with oropharyngeal carcinomas treated with radiotherapy, including chemo- and bio-radiotherapy, and who had a PET-CT scan prior to the start of treatment. RESULT Patients with a SUVmax value higher than 17.2 at the primary tumour site had a significantly higher risk of local recurrence. The 5-year local recurrence-free survival for patients with SUVmax less than or equal to 17.2 (n = 71) was 86.5% (95% CI 78.2-94.7 %), and for patients with SUVmax greater than 17.2 (n = 34) it was 55.8% (95% CI 36.0-75.6 %) (P = 0.0001). This difference in local control was maintained regardless of patients' HPV status. Specific survival was similarly lower for patients with a SUV greater than 17.2. The 5-year specific survival for patients with SUVmax greater than 17.2 was 39.5% (95% CI: 20.6-58.3 %), significantly shorter than that of patients with SUVmax equal to or less than 17.2, which was 77.3% (95% CI: 66.9-87.6 %) (P = 0.0001). CONCLUSIONS Patients with oropharyngeal carcinomas treated with radiotherapy with a SUVmax greater than 17.2 at the level of the primary tumour site had a significantly higher risk of local recurrence.
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Affiliation(s)
- Anna Holgado
- Servicio de Otorrinolaringología-->, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain
| | - Xavier León
- Servicio de Otorrinolaringología-->, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain; Centro de Investigación Biomédica en Red de Bioingeniería, Biomateriales y Nanomedicina (CIBER-BBN), Madrid, Spain; UVIC-->, Universitat Central de Catalunya, Vic, Spain.
| | - Miquel Quer
- Servicio de Otorrinolaringología-->, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain; Centro de Investigación Biomédica en Red de Bioingeniería, Biomateriales y Nanomedicina (CIBER-BBN), Madrid, Spain
| | - Valle Camacho
- Servicio de Medicina Nuclear-->, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain
| | - Alejando Fernández
- Servicio de Medicina Nuclear-->, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain
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Lin Fracp P, Holloway L, Min Franzcr M, Lee Franzcr M, Fowler Franzcr A. Prognostic and predictive values of baseline and mid-treatment FDG-PET in oropharyngeal carcinoma treated with primary definitive (chemo)radiation and impact of HPV status: review of current literature and emerging roles. Radiother Oncol 2023; 184:109686. [PMID: 37142128 DOI: 10.1016/j.radonc.2023.109686] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/29/2022] [Revised: 04/16/2023] [Accepted: 04/24/2023] [Indexed: 05/06/2023]
Abstract
BACKGROUND AND PURPOSE This study provides a review of the literature assessing whether semiquantitative PET parameters acquired at baseline and/or during definitive (chemo)radiotherapy ("prePET" and "iPET") can predict survival outcomes in patients with oropharyngeal squamous cell carcinoma (OPC), and the impact of human papilloma virus (HPV) status. MATERIAL AND METHODS A literature search was carried out using PubMed and Embase between 2001 to 2021 in accordance with PRISMA. RESULTS The analysis included 22 FDG-PET/CT studies1-22, 19 pre-PET and 3 both pre-PET and iPET14,18,20,. The analysis involved 2646 patients, of which 1483 are HPV-positive (17 studies: 10 mixed and 7 HPV-positive only), 589 are HPV-negative, and 574 have unknown HPV status. Eighteen studies found significant correlations of survival outcomes with pre-PET parameters, most commonly primary or "Total" (combined primary and nodal) metabolic tumour volume and/or total lesional glycolysis. Two studies could not establish significant correlations and both employed SUVmax only. Two studies also could not establish significant correlations when taking into account of the HPV-positive population only. Because of the heterogeneity and lack of standardized methodology, no conclusions on optimal cut-off values can be drawn. Ten studies specifically evaluated HPV-positive patients: five showed positive correlation of pre-PET parameters and survival outcomes, but four of these studies did not include advanced T or N staging in multivariate analysis1,6,15,22, and two studies only showed positive correlations after excluding high risk patients with smoking history7 or adverse CT features22. Two studies found that prePET parameters predicted treatment outcomes only in HPV-negative but not HPV-positive patients10,16. Two studies found that iPET parameters could predict outcomes in HPV-positive patients but not prePET parameters14,18. CONCLUSION The current literature supports high pre-treatment metabolic burden prior to definitive (chemo)radiotherapy can predict poor treatment outcomes for HPV-negative OPC patients. Evidence is conflicting and currently does not support correlation in HPV-positive patients.
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Affiliation(s)
- Peter Lin Fracp
- Department of Nuclear Medicine and PET, Liverpool Hospital, Liverpool, NSW, Australia; South Western Sydney Clinical School, University of New South Wales, NSW, Australia; School of Medicine, Western Sydney University, NSW, Australia.
| | - Lois Holloway
- South Western Sydney Clinical School, University of New South Wales, NSW, Australia; School of Medicine, Western Sydney University, NSW, Australia; Cancer Therapy Centre, Liverpool Hospital, Liverpool, NSW, Australia; Ingham Institute of Applied Medical Research, Liverpool, NSW, Australia
| | - Myo Min Franzcr
- Department of Radiation Oncology, Sunshine Coast University Hospital, Queensland, Australia; Faculty of Science, Health, Education and Engineering, University of Sunshine Coast, Queensland, Australia
| | - Mark Lee Franzcr
- South Western Sydney Clinical School, University of New South Wales, NSW, Australia; Cancer Therapy Centre, Liverpool Hospital, Liverpool, NSW, Australia
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Asociación entre el standarized uptake value (SUV) máximo y el control local en pacientes con carcinoma de orofaringe tratados con radioterapia. ACTA OTORRINOLARINGOLOGICA ESPANOLA 2022. [DOI: 10.1016/j.otorri.2022.05.004] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/18/2022]
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Noor A, Mair M, Cook L, Bolt H, Cheriyan S, Woods CM, Hopkins J, Ooi EH. Prognostic Value of
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F‐Fluoro‐Deoxyglucose‐Positron Emission Tomography Volumetric Parameters in Human Papillomavirus‐Related Oropharyngeal Squamous Cell Carcinoma. Laryngoscope 2022. [DOI: 10.1002/lary.30362] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/03/2022] [Revised: 07/15/2022] [Accepted: 08/08/2022] [Indexed: 11/06/2022]
Affiliation(s)
- Anthony Noor
- Department of Otolaryngology, Head and Neck Surgery Flinders Medical Centre Bedford Park South Australia Australia
| | - Manish Mair
- Department of Otolaryngology, Head and Neck Surgery John Hunter Hospital Newcastle New South Wales Australia
| | - Lachlan Cook
- Department of Otolaryngology, Head and Neck Surgery Flinders Medical Centre Bedford Park South Australia Australia
- Flinders Health and Medical Research Institute, College of Medicine and Public Health Flinders University Adelaide South Australia Australia
| | - Harrison Bolt
- Department of Otolaryngology, Head and Neck Surgery Flinders Medical Centre Bedford Park South Australia Australia
| | - Sanith Cheriyan
- Department of Otolaryngology, Head and Neck Surgery Flinders Medical Centre Bedford Park South Australia Australia
| | - Charmaine M. Woods
- Department of Otolaryngology, Head and Neck Surgery Flinders Medical Centre Bedford Park South Australia Australia
- Flinders Health and Medical Research Institute, College of Medicine and Public Health Flinders University Adelaide South Australia Australia
| | - James Hopkins
- Department of Medical Imaging Flinders Medical Centre Bedford Park South Australia Australia
| | - Eng H. Ooi
- Department of Otolaryngology, Head and Neck Surgery Flinders Medical Centre Bedford Park South Australia Australia
- Flinders Health and Medical Research Institute, College of Medicine and Public Health Flinders University Adelaide South Australia Australia
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Rosen BS, Wilkie JR, Sun Y, Ibrahim M, Casper KA, Miller JE, Chotchutipan T, Stucken CL, Bradford C, Prince MEP, Rosko AJ, Malloy KM, McLean SA, Chinn SB, Shuman AG, Spector ME, Swiecicki PL, Worden FP, Shah JL, Schonewolf CA, Chapman CH, Eisbruch A, Mierzwa ML. CT and FDG-PET radiologic biomarkers in p16+ oropharyngeal squamous cell carcinoma patients treated with definitive chemoradiotherapy. Radiother Oncol 2020; 155:174-181. [PMID: 33069764 DOI: 10.1016/j.radonc.2020.10.006] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/26/2020] [Revised: 10/01/2020] [Accepted: 10/03/2020] [Indexed: 11/28/2022]
Abstract
PURPOSE To assess associations between imaging biomarkers from standard of care pre-treatment CT and FDG-PET scans and locoregional (LR) and distant metastatic (DM) recurrences in patients with p16+ oropharyngeal squamous cell carcinoma (OPSCC) treated with definitive chemoradiotherapy (CRT). METHODS An institutional database from a single NCI-designated cancer center identified 266 patients with p16+ OPSCC treated with definitive CRT in our department from 2005 to 2016 with evaluable pre-treatment FDG-PET scans. Quantitative SUV metrics and qualitative imaging metrics were determined from FDG-PET and CT scans, while clinical characteristics were abstracted from the medical record. Associations between clinical/imaging features and time to LR (TTLRF) or DM (TTDMF) failure and overall survival (OS) were assessed using univariable Cox regression and penalized stepwise regression for multivariable analyses (MVA). RESULTS There were 27 LR and 32 DM recurrences as incident failures. Imaging biomarkers were significantly associated with TTLRF, TTDMF and OS. FDG-PET metrics outperformed CT and clinical metrics for TTLRF, with metabolic tumor volume being the only significant feature selected on MVA: C-index = 0.68 (p = 0.01). Radiographic extranodal extension (rENE), positive retropharyngeal nodes (RPN+), and clinical stage were significant on MVA for TTDMF: C-index = 0.84 (p < 0.001). rENE, group stage, and RPN+ were significant on MVA for OS: C-index = 0.77 (p < 0.001). CONCLUSIONS In the largest study to date of uniformly treated patients with CRT to evaluate both pretreatment CT and FDG-PET, radiographic biomarkers were significantly associated with TTLRF, TTDMF and OS among patients with p16+ OPSCC treated with CRT. CT metrics performed best to predict TTDMF, while FDG-PET metrics showed improved prediction for LRRFS. These metrics may help identify candidates for treatment intensification or de-escalation of therapy. STATEMENT OF TRANSLATIONAL RELEVANCE Pre-treatment imaging features from standard-of-care PET/CT imaging show promise for predicting long-term outcomes following HPV-associated oropharynx cancer (HPV-OPC) therapy. This study comprehensively characterizes qualitative and quantitative pre-treatment imaging metrics associated with time to pattern-specific failure in a cohort of 266 patients treated uniformly with definitive chemoradiation. Multivariate analysis (MVA) for time to locoregional failure (TTLRF), time to distant metastatic failure (TTDMF), and overall survival (OS) was performed. FDG-PET metrics outperformed CT and clinical metrics for TTLRF. CT radiographic extranodal extension, positive retropharyngeal nodes, and stage strongly predicted TTDMF (combined C-index = 0.84, log rank p < 0.001). Number of smoking pack-years complemented clinical and imaging features only in patients without radiographic extranodal extension or positive retropharyngeal nodes. Time to pattern-specific failure is important for guiding treatment de-escalation strategies, which intend to reduce treatment-related toxicity in patients with relatively long expected survival times. This study suggests that PET/CT features should play a crucial role in future de-escalation trials and management of HPV-OPC patients.
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Affiliation(s)
- Benjamin S Rosen
- Department of Radiation Oncology, Michigan Medicine, Ann Arbor, United States.
| | - Joel R Wilkie
- Department of Radiation Oncology, Michigan Medicine, Ann Arbor, United States
| | - Yilun Sun
- Department of Radiation Oncology, Michigan Medicine, Ann Arbor, United States; Department of Biostatistics, University of Michigan, Ann Arbor, MI, Uninet States
| | - Mohannad Ibrahim
- Department of Radiology, Division of Neuroradiology, Michigan Medicine, Ann Arbor, United States
| | - Keith A Casper
- Department of Otolaryngology-Head and Neck Surgery, Michigan Medicine, Ann Arbor, United States
| | - Jessa E Miller
- Department of Head and Neck Surgery, UCLA, Los Angeles, United States
| | - Thong Chotchutipan
- Department of Radiation Oncology, Chulabhorn Hospital, HRH Princess Chulabhorn College of Medical Science, Chulabhorn Royal Academy, Bangkok, Thailand
| | - Chaz L Stucken
- Department of Otolaryngology-Head and Neck Surgery, Michigan Medicine, Ann Arbor, United States
| | - Carol Bradford
- Department of Otolaryngology-Head and Neck Surgery, Michigan Medicine, Ann Arbor, United States
| | - Mark E P Prince
- Department of Otolaryngology-Head and Neck Surgery, Michigan Medicine, Ann Arbor, United States
| | - Andrew J Rosko
- Department of Otolaryngology-Head and Neck Surgery, Michigan Medicine, Ann Arbor, United States
| | - Kelly M Malloy
- Department of Otolaryngology-Head and Neck Surgery, Michigan Medicine, Ann Arbor, United States
| | - Scott A McLean
- Department of Otolaryngology-Head and Neck Surgery, Michigan Medicine, Ann Arbor, United States
| | - Steven B Chinn
- Department of Otolaryngology-Head and Neck Surgery, Michigan Medicine, Ann Arbor, United States
| | - Andrew G Shuman
- Department of Otolaryngology-Head and Neck Surgery, Michigan Medicine, Ann Arbor, United States
| | - Matthew E Spector
- Department of Otolaryngology-Head and Neck Surgery, Michigan Medicine, Ann Arbor, United States
| | - Paul L Swiecicki
- Department of Internal Medicine, Michigan Medicine, Ann Arbor, United States; U.S. Department of Veterans Affairs, VA Center for Clinical Management Research, Ann Arbor, United States
| | - Francis P Worden
- Department of Internal Medicine, Michigan Medicine, Ann Arbor, United States
| | - Jennifer L Shah
- Department of Radiation Oncology, Michigan Medicine, Ann Arbor, United States
| | | | - Christina H Chapman
- Department of Radiation Oncology, Michigan Medicine, Ann Arbor, United States; U.S. Department of Veterans Affairs, VA Center for Clinical Management Research, Ann Arbor, United States
| | - Avraham Eisbruch
- Department of Radiation Oncology, Michigan Medicine, Ann Arbor, United States
| | - Michelle L Mierzwa
- Department of Radiation Oncology, Michigan Medicine, Ann Arbor, United States
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Qian DC, Magliocca KR, Aiken AH, Baugnon KL, Brandon DC, Stokes WA, McDonald MW, Patel MR, Baddour HM, Kaka AS, Steuer CE, Saba NF, Shin DM, Beitler JJ. Outcomes and Predictive Value of Post-adjuvant Therapy PET/CT for Locally Advanced Oral Squamous Cell Carcinoma. Laryngoscope 2020; 130:E850-E857. [PMID: 32057110 DOI: 10.1002/lary.28509] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/20/2019] [Revised: 12/23/2019] [Accepted: 01/07/2020] [Indexed: 11/08/2022]
Abstract
OBJECTIVES/HYPOTHESIS For locally advanced oral squamous cell carcinoma (OSCC) treated by surgery and adjuvant therapy, consensus has yet to be reached on whether the optimal time to initiate surveillance positron emission tomography/computed tomography (PET/CT) scan is before or after adjuvant therapy. In this study, we characterize the utility of PET/CT scans obtained 3 months after adjuvant therapy. STUDY DESIGN PET/CT scans were obtained for 220 patients with stage III, IVA, or IVB OSCC who underwent resection followed by adjuvant radiotherapy or chemoradiotherapy. METHODS Using the Neck Imaging Reporting and Data System, PET/CT scans were dichotomized as suspicious (primary or neck category ≥3, or distant lesion present) versus nonsuspicious. We then computed differences in locoregional progression, distant progression, and overall survival; positive predictive value (PPV), negative predictive value (NPV), sensitivity, and specificity; and success rate of salvage. RESULTS Sixty-seven patients (30%) had suspicious PET/CT scans, which were significantly associated with local failure (hazard ratio [HR] 14.0, 95% confidence interval [CI] 7.3-26.6), distant failure (HR 18.4, 95% CI 9.6-35.3), and poorer overall survival (HR 9.5, 95% CI 5.0-17.9). Overall PPV, locoregional PPV, NPV, sensitivity, and specificity were 85%, 79%, 73%, 58%, and 92%, respectively. Among those with biopsy-confirmed progression, 37 patients (65%) underwent salvage therapy; four (11%) were without evidence of disease at last follow-up. CONCLUSIONS For locally advanced OSCC, PET/CT scan 3 months after adjuvant therapy is strongly predictive of disease recurrence and survival, demonstrating improved performance over postoperative imaging in previous studies. Following a suspicious post-adjuvant therapy PET/CT scan, cure of locoregional recurrence is possible but unlikely. LEVEL OF EVIDENCE 4 Laryngoscope, 2020.
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Affiliation(s)
- David C Qian
- Department of Radiation Oncology, Winship Cancer Institute of Emory University, Atlanta, Georgia, USA
| | - Kelly R Magliocca
- Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Atlanta, Georgia, USA
| | - Ashley H Aiken
- Department of Radiology and Imaging Sciences, Emory University School of Medicine, Atlanta, Georgia, USA
| | - Kristen L Baugnon
- Department of Radiology and Imaging Sciences, Emory University School of Medicine, Atlanta, Georgia, USA
| | - David C Brandon
- Department of Radiology and Imaging Sciences, Emory University School of Medicine, Atlanta, Georgia, USA
| | - William A Stokes
- Department of Radiation Oncology, Winship Cancer Institute of Emory University, Atlanta, Georgia, USA
| | - Mark W McDonald
- Department of Radiation Oncology, Winship Cancer Institute of Emory University, Atlanta, Georgia, USA
| | - Mihir R Patel
- Department of Otolaryngology, Emory University School of Medicine, Atlanta, Georgia, USA
| | - Harry M Baddour
- Department of Otolaryngology, Emory University School of Medicine, Atlanta, Georgia, USA
| | - Azeem S Kaka
- Department of Otolaryngology, Emory University School of Medicine, Atlanta, Georgia, USA
| | - Conor E Steuer
- Department of Hematology and Medical Oncology, Winship Cancer Institute of Emory University, Atlanta, Georgia, USA
| | - Nabil F Saba
- Department of Hematology and Medical Oncology, Winship Cancer Institute of Emory University, Atlanta, Georgia, USA
| | - Dong M Shin
- Department of Hematology and Medical Oncology, Winship Cancer Institute of Emory University, Atlanta, Georgia, USA
| | - Jonathan J Beitler
- Department of Radiation Oncology, Winship Cancer Institute of Emory University, Atlanta, Georgia, USA.,Department of Otolaryngology, Emory University School of Medicine, Atlanta, Georgia, USA.,Department of Hematology and Medical Oncology, Winship Cancer Institute of Emory University, Atlanta, Georgia, USA
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Moan JM, Amdal CD, Malinen E, Svestad JG, Bogsrud TV, Dale E. The prognostic role of 18F-fluorodeoxyglucose PET in head and neck cancer depends on HPV status. Radiother Oncol 2019; 140:54-61. [DOI: 10.1016/j.radonc.2019.05.019] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/17/2019] [Revised: 05/13/2019] [Accepted: 05/15/2019] [Indexed: 11/25/2022]
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nab-Paclitaxel-based induction chemotherapy followed by cisplatin and radiation therapy for human papillomavirus-unrelated head and neck squamous-cell carcinoma. Med Oncol 2019; 36:93. [PMID: 31595355 DOI: 10.1007/s12032-019-1318-5] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/23/2019] [Accepted: 09/23/2019] [Indexed: 12/11/2022]
Abstract
In patients with locally advanced human papillomavirus (HPV)-unrelated head and neck squamous-cell carcinoma (HNSCC), cisplatin and radiation therapy (CisRT) resulted in a local-regional recurrence (LRR) rate of 35%, progression-free survival (PFS) of 49%, and overall survival (OS) of 60%. We, and others, showed that nab-paclitaxel is an active agent in metastatic and locally advanced HNSCC. The aim of this report was to assess the efficacy of nab-paclitaxel-based induction chemotherapy and CisRT in HPV-unrelated HNSCC. We performed a retrospective single-institution analysis of patients treated with nab-paclitaxel-based chemotherapy and CisRT. Key inclusion criteria included stage III-IV HPV-unrelated HNSCC. Induction chemotherapy included nab-paclitaxel and cisplatin (AP), AP + 5-fluorouracil (APF), or APF + Cetuximab (APF-C). Endpoints included LRR, overall relapse, PFS, and OS. Thirty-eight patients were the subject of this analysis. Patient characteristics included median age 59 years (IQR: 54-64) and smoking history in 36 patients (95%). Primary tumor sites included larynx/hypopharynx (27), p16 negative oropharynx (10), and oral cavity (1). Most patients had bulky disease: 82% T3-4 (n = 31) and 74% N2b-3 (n = 28). Median follow-up was 44 months (IQR: 23-59). The three-year LRR rate was 16% (95% confidence interval [CI] 7-34) and the overall relapse rate was 22% (95% CI 11-41). The three-year PFS was 64% (95% CI 46-77) and OS was 72% (95% CI 54-84). Among patients with HPV-unrelated HNSCC, nab-paclitaxel-based induction chemotherapy and CisRT resulted in a lower-than-expected rate of LRR and more favorable PFS and OS compared to historical results with CisRT.
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How Effective Are Noninvasive Tests for Diagnosing Malignant Peripheral Nerve Sheath Tumors in Patients with Neurofibromatosis Type 1? Diagnosing MPNST in NF1 Patients. Sarcoma 2019; 2019:4627521. [PMID: 31354382 PMCID: PMC6636541 DOI: 10.1155/2019/4627521] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/20/2019] [Accepted: 05/30/2019] [Indexed: 12/21/2022] Open
Abstract
Background Distinguishing between benign and malignant peripheral nerve sheath tumors (MPNSTs) in neurofibromatosis 1 (NF1) patients prior to excision can be challenging. How can MPNST be most accurately diagnosed using clinical symptoms, magnetic resonance imaging (MRI) findings (tumor size, depth, and necrosis), positron emission tomography (PET) measures (SUVpeak, SUVmax, SUVmax tumor/SUVmean liver, and qualitative scale), and combinations of the above? Methods. All NF1 patients who underwent PET imaging at our institution (January 1, 2007–December 31, 2016) were included. Medical records were reviewed for clinical findings; MR images and PET images were interpreted by two fellowship-trained musculoskeletal and nuclear medicine radiologists, respectively. Receiver operating characteristic (ROC) curves were created for each PET measurement; the area under the curve (AUC) and thresholds for diagnosing malignancy were calculated. Logistic regression determined significant predictors of malignancy. Results Our population of 41 patients contained 34 benign and 36 malignant tumors. Clinical findings did not reliably predict MPNST. Tumor depth below fascia was highly sensitive; larger tumors were more likely to be malignant but without a useful cutoff for diagnosis. Necrosis on MRI was highly accurate and was the only significant variable in the regression model. PET measures were highly accurate, with AUCs comparable and cutoff points consistent with prior studies. A diagnostic algorithm was created using MRI and PET findings. Conclusions MRI and PET were more effective at diagnosing MPNST than clinical features. We created an algorithm for preoperative evaluation of peripheral nerve sheath tumors in NF1 patients, for which additional validation will be indicated.
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Gouw ZAR, La Fontaine MD, van Kranen S, van de Kamer JB, Vogel WV, van Werkhoven E, Sonke JJ, Al-Mamgani A. The Prognostic Value of Baseline 18F-FDG PET/CT in Human Papillomavirus–Positive Versus Human Papillomavirus–Negative Patients With Oropharyngeal Cancer. Clin Nucl Med 2019; 44:e323-e328. [DOI: 10.1097/rlu.0000000000002531] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/25/2022]
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11
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Ishihara T, Kitajima K, Suenaga Y, Ejima Y, Komatsu H, Otsuki N, Nibu KI, Kiyota N, Takahashi S, Sasaki R. [18F]Fluorodeoxyglucose uptake by positron emission tomography predicts outcomes for oropharyngeal and hypopharyngeal cancer treated with definitive radiotherapy. NAGOYA JOURNAL OF MEDICAL SCIENCE 2018; 79:27-36. [PMID: 28303058 PMCID: PMC5346617 DOI: 10.18999/nagjms.79.1.27] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Indexed: 11/30/2022]
Abstract
This study evaluated the prognostic significance of the maximum standardized uptake value of the primary site (pSUVmax) in 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) scans of patients with oropharyngeal or hypopharyngeal cancer who were treated using definitive radiotherapy. The study included 86 patients who were primarily treated with radiotherapy for oropharyngeal or hypopharyngeal cancer. Sixty-nine patients underwent concurrent chemotherapy. The associations between pre-treatment pSUVmax and treatment outcomes were evaluated. The most appropriate pSUVmax cut-off value for predicting disease-free survival (DFS) and local control (LC) was selected using receiver operating characteristic (ROC) curves. The median follow-up time for surviving patients was 60 months, while the median survival time in the entire patient cohort was 55 months. A pSUVmax cut-off value of 9.0 showed the best discriminative performance. Five-year OS and DFS rates were 65.9% and 60.0%, respectively. In univariate analyses, pSUVmax (p = 0.009), T-stage (p = 0.001), N-stage (p = 0.039), and clinical stage (p = 0.017) were identified as significant prognostic predictors for DFS. The multivariate analysis did not identify any statistically significant factors, but the association between pSUVmax and DFS was borderline significant (p = 0.055). Interestingly, pSUVmax was predictive of local controllability in T1–T2 disease (p = 0.024), but there was no significant association for T3–T4 disease (p = 0.735). In this study, pSUVmax was predictive of DFS and LC in patients with oropharyngeal or hypopharyngeal cancer that was treated with definitive radiotherapy. pSUVmax was strongly associated with LC in T1–T2 disease.
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Affiliation(s)
- Takeaki Ishihara
- Division of Radiation Oncology, Kobe University Graduate School of Medicine, Kobe, Japa
| | - Kazuhiro Kitajima
- Department of Radiology, Hyogo College of Medicine, Nishinomiya, Japan
| | - Yuko Suenaga
- Department of Radiology, Hyogo College of Medicine, Nishinomiya, Japan
| | - Yasuo Ejima
- Division of Radiation Oncology, Kobe University Graduate School of Medicine, Kobe, Japa
| | - Hirokazu Komatsu
- Department of Otolaryngology-Head and Neck Surgery, Kobe University Graduate School of Medicine, Kobe, Japan
| | - Naoki Otsuki
- Department of Otolaryngology-Head and Neck Surgery, Kobe University Graduate School of Medicine, Kobe, Japan
| | - Ken-Ichi Nibu
- Department of Otolaryngology-Head and Neck Surgery, Kobe University Graduate School of Medicine, Kobe, Japan
| | - Naomi Kiyota
- Division of Medical Oncology/Hematology, Kobe University Graduate School of Medicine, Kobe, Japan
| | - Satoru Takahashi
- Department of Radiology, Hyogo College of Medicine, Nishinomiya, Japan
| | - Ryohei Sasaki
- Division of Radiation Oncology, Kobe University Graduate School of Medicine, Kobe, Japa
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Survival for HPV-positive oropharyngeal squamous cell carcinoma with surgical versus non-surgical treatment approach: A systematic review and meta-analysis. Oral Oncol 2018; 86:121-131. [DOI: 10.1016/j.oraloncology.2018.09.018] [Citation(s) in RCA: 25] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/01/2018] [Revised: 09/10/2018] [Accepted: 09/14/2018] [Indexed: 02/07/2023]
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Floberg JM, DeWees TA, Chin RI, Garsa AA, Dehdashti F, Nussenbaum B, Oppelt PJ, Adkins DR, Gay HA, Thorstad WL. Pretreatment metabolic tumor volume as a prognostic factor in HPV-associated oropharyngeal cancer in the context of AJCC 8th edition staging. Head Neck 2018; 40:2280-2287. [DOI: 10.1002/hed.25337] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/10/2017] [Revised: 01/30/2018] [Accepted: 05/03/2018] [Indexed: 12/31/2022] Open
Affiliation(s)
- John M. Floberg
- Washington University School of Medicine, Department of Radiation Oncology; St Louis MO
| | - Todd A. DeWees
- Mayo Clinic, Department of Biomedical Statistics and Informatics Scottsdale; AZ
| | - Re-I Chin
- St Louis University School of Medicine; St Louis MO
| | - Adam A. Garsa
- Keck School of Medicine of University of Southern California, Department of Radiation Oncology; Los Angeles CA
| | - Farrokh Dehdashti
- Washington University School of Medicine, Mallinckrodt Institute of Radiology Division of Nuclear Medicine; St Louis MO
| | | | - Peter J. Oppelt
- Washington University School of Medicine, Department of Internal Medicine, Division of Oncology; St Louis MO
| | - Douglas R. Adkins
- Washington University School of Medicine, Department of Internal Medicine, Division of Oncology; St Louis MO
| | - Hiram A. Gay
- Washington University School of Medicine, Department of Radiation Oncology; St Louis MO
| | - Wade L. Thorstad
- Washington University School of Medicine, Department of Radiation Oncology; St Louis MO
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14
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Suzuki-Shibata S, Yamamoto Y, Yoshida T, Mizoguchi N, Nonaka T, Kubota A, Narimatsu H, Miyagi Y, Kobayashi T, Kaneta T, Inoue T. Prognostic value of volumetric FDG PET/CT parameters in patients with oral tongue squamous cell carcinoma who were treated by superselective intra-arterial chemoradiotherapy. Jpn J Radiol 2017; 35:740-747. [PMID: 29039110 DOI: 10.1007/s11604-017-0686-z] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/22/2017] [Accepted: 09/25/2017] [Indexed: 11/29/2022]
Abstract
PURPOSE This study aimed to evaluate the predictive and prognostic value of FDG PET/CT-based volumetric parameters in patients with oral tongue squamous cell carcinoma (OTSCC) treated by superselective intra-arterial chemoradiotherapy (IA-CRT). METHODS We conducted a retrospective study including 33 patients with biopsy-proven OTSCC between May 2007 and February 2016. All of the patients were treated by IA-CRT. Pretreatment SUVmax and metabolic tumor volume (MTV) of the primary tumor were measured. The SUV thresholds of 2.5 and 5.0 were used. Progression-free survival (PFS) and overall survival (OS) were chosen as endpoints to evaluate prognosis. Univariate and multivariate analyses were performed to assess the potential independent effect of FDG PET/CT parameters. RESULTS The median follow-up for surviving patients was 40.7 months (range 6.0-107.5 months). In univariate and multivariate analyses, SUVmax and MTV (5.0) were independent prognostic factors for PFS. In univariate analysis, SUVmax failed to predict OS. MTV (5.0) was a significant prognostic factor for OS, but multivariate analysis failed to show statistical independence because it could not exclude the possibility of an artifact due to N stage. CONCLUSIONS FDG PET/CT-based volumetric parameters may be significant prognostic markers for survival of patients with OTSCC who are treated by IA-CRT.
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Affiliation(s)
- Satoko Suzuki-Shibata
- Department of Diagnostic and Interventional Radiology, Kanagawa Cancer Center, 2-3-2 Nakao, Asahi-Ku, Yokohama, Kanagawa, 241-8515, Japan.
| | - Yayoi Yamamoto
- Department of Diagnostic and Interventional Radiology, Kanagawa Cancer Center, 2-3-2 Nakao, Asahi-Ku, Yokohama, Kanagawa, 241-8515, Japan
| | - Tetsuo Yoshida
- Department of Diagnostic and Interventional Radiology, Kanagawa Cancer Center, 2-3-2 Nakao, Asahi-Ku, Yokohama, Kanagawa, 241-8515, Japan
| | - Nobutaka Mizoguchi
- Department of Radiation Oncology, Kanagawa Cancer Center, 2-3-2 Nakao, Asahi-Ku, Yokohama, Kanagawa, 241-8515, Japan
| | - Tetsuo Nonaka
- Department of Radiation Oncology, Kanagawa Cancer Center, 2-3-2 Nakao, Asahi-Ku, Yokohama, Kanagawa, 241-8515, Japan
| | - Akira Kubota
- Department of Head and Neck Surgery, Kanagawa Cancer Center, 2-3-2 Nakao, Asahi-Ku, Yokohama, Kanagawa, 241-8515, Japan
| | - Hiroto Narimatsu
- Cancer Preservation and Control Division, Kanagawa Cancer Center Research Institute, 2-3-2 Nakao, Asahi-Ku, Yokohama, Kanagawa, 241-8515, Japan
| | - Yohei Miyagi
- Molecular Pathology and Genetics Division, Kanagawa Cancer Center Research Institute, 2-3-2 Nakao, Asahi-Ku, Yokohama, Kanagawa, 241-8515, Japan
| | - Toshiaki Kobayashi
- Kanagawa Cancer Center Research Institute, 2-3-2 Nakao, Asahi-Ku, Yokohama, Kanagawa, 241-8515, Japan
| | - Tomohiro Kaneta
- Department of Radiology, Yokohama City University School of Medicine, 3-9 Fukuura, Kanazawa-Ku, Yokohama, Kanagawa, 236-0004, Japan
| | - Tomio Inoue
- Department of Radiology, Yokohama City University School of Medicine, 3-9 Fukuura, Kanazawa-Ku, Yokohama, Kanagawa, 236-0004, Japan
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15
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Folkert MR, Setton J, Apte AP, Grkovski M, Young RJ, Schöder H, Thorstad WL, Lee NY, Deasy JO, Hun Oh J. Predictive modeling of outcomes following definitive chemoradiotherapy for oropharyngeal cancer based on FDG-PET image characteristics. Phys Med Biol 2017; 62:5327-5343. [PMID: 28604368 PMCID: PMC5729737 DOI: 10.1088/1361-6560/aa73cc] [Citation(s) in RCA: 39] [Impact Index Per Article: 4.9] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/23/2022]
Abstract
In this study, we investigate the use of imaging feature-based outcomes research ('radiomics') combined with machine learning techniques to develop robust predictive models for the risk of all-cause mortality (ACM), local failure (LF), and distant metastasis (DM) following definitive chemoradiation therapy (CRT). One hundred seventy four patients with stage III-IV oropharyngeal cancer (OC) treated at our institution with CRT with retrievable pre- and post-treatment 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) scans were identified. From pre-treatment PET scans, 24 representative imaging features of FDG-avid disease regions were extracted. Using machine learning-based feature selection methods, multiparameter logistic regression models were built incorporating clinical factors and imaging features. All model building methods were tested by cross validation to avoid overfitting, and final outcome models were validated on an independent dataset from a collaborating institution. Multiparameter models were statistically significant on 5 fold cross validation with the area under the receiver operating characteristic curve (AUC) = 0.65 (p = 0.004), 0.73 (p = 0.026), and 0.66 (p = 0.015) for ACM, LF, and DM, respectively. The model for LF retained significance on the independent validation cohort with AUC = 0.68 (p = 0.029) whereas the models for ACM and DM did not reach statistical significance, but resulted in comparable predictive power to the 5 fold cross validation with AUC = 0.60 (p = 0.092) and 0.65 (p = 0.062), respectively. In the largest study of its kind to date, predictive features including increasing metabolic tumor volume, increasing image heterogeneity, and increasing tumor surface irregularity significantly correlated to mortality, LF, and DM on 5 fold cross validation in a relatively uniform single-institution cohort. The LF model also retained significance in an independent population.
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Affiliation(s)
- Michael R. Folkert
- Department of Radiation Oncology, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
| | - Jeremy Setton
- Department of Radiation Oncology, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
| | - Aditya P. Apte
- Department of Medical Physics, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
| | - Milan Grkovski
- Department of Medical Physics, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
| | - Robert J. Young
- Department of Radiology, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
| | - Heiko Schöder
- Department of Radiology, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
| | - Wade L. Thorstad
- Department of Radiation Oncology, Washington University School of Medicine, St. Louis, MO 63110, USA
| | - Nancy Y. Lee
- Department of Radiation Oncology, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
| | - Joseph O. Deasy
- Department of Medical Physics, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
| | - Jung Hun Oh
- Department of Medical Physics, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
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16
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Cacicedo J, Fernandez I, Del Hoyo O, Navarro A, Gomez-Iturriaga A, Pijoan JI, Martinez-Indart L, Escudero J, Gomez-Suarez J, de Zarate RO, Perez JF, Bilbao P, Rades D. Prognostic value of maximum standardized uptake value measured by pretreatment 18F-FDG PET/CT in locally advanced head and neck squamous cell carcinoma. Clin Transl Oncol 2017; 19:1337-1349. [PMID: 28540535 DOI: 10.1007/s12094-017-1674-6] [Citation(s) in RCA: 19] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/24/2016] [Accepted: 05/12/2017] [Indexed: 11/24/2022]
Abstract
PURPOSE/OBJECTIVES To evaluate the prognostic impact of maximum standardized uptake value (SUVmax) in patients with locally advanced head and neck squamous cell carcinoma (HNSCC) undergoing pretreatment [F-18] fluoro-D-glucose-positron emission tomography/computed tomography (FDG PET/CT) imaging. MATERIALS/METHODS Fifty-eight patients undergoing FDG PET/CT before radical treatment with definitive radiotherapy (±concomitant chemotherapy) or surgery + postoperative (chemo)radiation were analyzed. The effects of clinicopathological factors (age, gender, tumor location, stage, Karnofsky Performance Status (KPS), and treatment strategy) including primary tumor SUVmax and nodal SUVmax on overall survival (OS), disease-free survival (DFS), locoregional control (LRC), and distant metastasis-free survival (DMFS) were evaluated. Kaplan-Meier survival curves were generated and compared with the log-rank test. RESULTS Median follow-up for the whole population was 31 months (range 2.3-53.5). Two-year OS, LRC, DFS and DMFS, for the entire cohort were 62.1, 78.3, 55.2 and 67.2%, respectively. Median pretreatment SUVmax for the primary tumor and lymph nodes was 11.85 and 5.4, respectively. According to univariate analysis, patients with KPS < 80% (p < 0.001), AJCC stage IVa or IVb vs III (p = 0.037) and patients undergoing radiotherapy vs surgery (p = 0.042) were significantly associated with worse OS. Patients with KPS < 80% (p = 0.003) or age ≥65 years (p = 0.007) had worse LRC. The KPS < 80% was the only factor associated with decreased DFS (p = 0.001). SUVmax of the primary tumor or the lymph nodes were not associated with OS, DFS or LRC. The KPS < 80% (p = 0.002), tumor location (p = 0.047) and AJCC stage (p = 0.025) were associated with worse cancer-specific survival (CSS). According to Cox regression analysis, on multivariate analysis KPS < 80% was the only independent parameter determining worse OS, DFS, CSS. Regarding LRC only patients with IK < 80% (p = 0.01) and ≥65 years (p = 0.01) remained statistically significant. Nodal SUVmax was the only factor associated with decreased DMFS. Patients with a nodal SUVmax > 5.4 presented an increased risk for distant metastases (HR, 3.3; 95% CI 1.17-9.25; p = 0.023). CONCLUSIONS The pretreatment nodal SUVmax in patients with locally advanced HNSCC is prognostic for DMFS. However, according to our results primary tumor SUVmax and nodal SUVmax were not significantly related to OS, DFS or LRC. Patients presenting KPS < 80% had worse OS, DFS, CSS and LRC.
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Affiliation(s)
- J Cacicedo
- Radiation Oncology Department, Cruces University Hospital (University of the Basque Country)/Biocruces Health Research Institute, c/Plaza de Cruces s/n, 48903, Barakaldo, Bizkaia (Basque Country), Spain.
| | - I Fernandez
- Nuclear Medicine Department, Cruces University Hospital, Barakaldo, Spain
| | - O Del Hoyo
- Radiation Oncology Department, Cruces University Hospital (University of the Basque Country)/Biocruces Health Research Institute, c/Plaza de Cruces s/n, 48903, Barakaldo, Bizkaia (Basque Country), Spain
| | - A Navarro
- Radiation Oncology Department, Hospital Duran i Reynals (ICO) Avda, Gran Via de L´Hospitalet, 199-203, Hospitalet de Llobregat, 08908, Barcelona, Spain
| | - A Gomez-Iturriaga
- Radiation Oncology Department, Cruces University Hospital (University of the Basque Country)/Biocruces Health Research Institute, c/Plaza de Cruces s/n, 48903, Barakaldo, Bizkaia (Basque Country), Spain
| | - J Ignacio Pijoan
- Clinical Epidemiology Unit, Cruces University Hospital/Biocruces Health Research Institute, Barakaldo, Spain.,CIBER de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
| | - L Martinez-Indart
- Clinical Epidemiology Unit, Cruces University Hospital/Biocruces Health Research Institute, Barakaldo, Spain
| | - J Escudero
- Clinical Epidemiology Unit, Cruces University Hospital/Biocruces Health Research Institute, Barakaldo, Spain
| | - J Gomez-Suarez
- Otolaryngology Department, Cruces University Hospital, c/Plaza de Cruces s/n, 48903, Barakaldo, Vizcaya (Basque Country), Spain
| | - R Ortiz de Zarate
- Medical Physics and Radioprotection Department, Cruces University Hospital/Biocruces Health Research Institute, Vizcaya, Spain
| | - J Fernando Perez
- Medical Physics and Radioprotection Department, Cruces University Hospital/Biocruces Health Research Institute, Vizcaya, Spain
| | - P Bilbao
- Radiation Oncology Department, Cruces University Hospital (University of the Basque Country)/Biocruces Health Research Institute, c/Plaza de Cruces s/n, 48903, Barakaldo, Bizkaia (Basque Country), Spain
| | - D Rades
- Department of Radiation Oncology, University of Lübeck, Ratzeburger Allee 160, 23562, Lübeck, Germany
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17
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Cacicedo J, Navarro A, Del Hoyo O, Gomez-Iturriaga A, Alongi F, Medina JA, Elicin O, Skanjeti A, Giammarile F, Bilbao P, Casquero F, de Bari B, Dal Pra A. Role of fluorine-18 fluorodeoxyglucose PET/CT in head and neck oncology: the point of view of the radiation oncologist. Br J Radiol 2016; 89:20160217. [PMID: 27416996 DOI: 10.1259/bjr.20160217] [Citation(s) in RCA: 35] [Impact Index Per Article: 3.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/06/2023] Open
Abstract
Squamous cell carcinoma is the most common malignant tumour of the head and neck. The initial TNM staging, the evaluation of the tumour response during treatment, and the long-term surveillance are crucial moments in the approach to head and neck squamous cell carcinoma (HNSCC). Thus, at each of these moments, the choice of the best diagnostic tool providing the more precise and larger information is crucial. Positron emission tomography with fluorine-18 fludeoxyglucose integrated with CT (18F-FDG-PET/CT) rapidly gained clinical acceptance, and it has become an important imaging tool in routine clinical oncology. However, controversial data are currently available, for example, on the role of 18F-FDG-PET/CT imaging during radiotherapy planning, the prognostic value or its real clinical impact on treatment decisions. In this article, the role of 18F-FDG-PET/CT imaging in HNSCC during pre-treatment staging, radiotherapy planning, treatment response assessment, prognosis and follow-up is reviewed focusing on current evidence and controversial issues. A proposal on how to integrate 18F-FDG-PET/CT in daily clinical practice is also described.
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Affiliation(s)
- Jon Cacicedo
- 1 Radiation Oncology Department, Cruces University Hospital/Biocruces Health Research Institute, Barakaldo, Spain.,2 Grupo Español de Oncología Radioterápica en Cabeza y Cuello (GEORCC)
| | - Arturo Navarro
- 3 Radiation Oncology Department, Hospital Duran i Reynals (ICO) Avda, Gran Via de L´Hospitalet, Hospitalet de Llobregat, Barcelona, Spain
| | - Olga Del Hoyo
- 1 Radiation Oncology Department, Cruces University Hospital/Biocruces Health Research Institute, Barakaldo, Spain
| | - Alfonso Gomez-Iturriaga
- 1 Radiation Oncology Department, Cruces University Hospital/Biocruces Health Research Institute, Barakaldo, Spain
| | - Filippo Alongi
- 4 Radiation Oncology Department, Sacro Cuore-Don Calabria Hospital, Verona, Italy
| | - Jose A Medina
- 2 Grupo Español de Oncología Radioterápica en Cabeza y Cuello (GEORCC).,5 Radiation Oncology Department, Hospital Universitario Virgen de la Victoria, Malaga, Spain
| | - Olgun Elicin
- 6 Radiation Oncology Department, Inselspital, Bern University Hospital, Bern, Switzerland
| | - Andrea Skanjeti
- 7 Nuclear Medicine Department, Hospices Civils de Lyon, Université Claude Bernard Lyon 1, Lyon, France
| | - Francesco Giammarile
- 7 Nuclear Medicine Department, Hospices Civils de Lyon, Université Claude Bernard Lyon 1, Lyon, France
| | - Pedro Bilbao
- 1 Radiation Oncology Department, Cruces University Hospital/Biocruces Health Research Institute, Barakaldo, Spain
| | - Francisco Casquero
- 1 Radiation Oncology Department, Cruces University Hospital/Biocruces Health Research Institute, Barakaldo, Spain
| | - Berardino de Bari
- 8 fESTRO Radiation Oncology, Centre Hospitalier Universitaire Vaudois (CHUV), Lausanne, Switzerland
| | - Alan Dal Pra
- 6 Radiation Oncology Department, Inselspital, Bern University Hospital, Bern, Switzerland
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18
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Min M, Lin P, Liney G, Lee M, Forstner D, Fowler A, Holloway L. A review of the predictive role of functional imaging in patients with mucosal primary head and neck cancer treated with radiation therapy. J Med Imaging Radiat Oncol 2016; 61:99-123. [DOI: 10.1111/1754-9485.12496] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/07/2015] [Accepted: 06/11/2016] [Indexed: 12/14/2022]
Affiliation(s)
- Myo Min
- Cancer Therapy Centre; Liverpool Hospital; Liverpool New South Wales Australia
- South Western Clinical School; University of New South Wales; Sydney New South Wales Australia
- Ingham Institute of Applied Medical Research; Liverpool New South Wales Australia
| | - Peter Lin
- South Western Clinical School; University of New South Wales; Sydney New South Wales Australia
- Department of Nuclear Medicine and Positron Emission Tomography; Liverpool Hospital; Liverpool New South Wales Australia
- University of Western Sydney; Sydney New South Wales Australia
| | - Gary Liney
- Cancer Therapy Centre; Liverpool Hospital; Liverpool New South Wales Australia
- South Western Clinical School; University of New South Wales; Sydney New South Wales Australia
- Ingham Institute of Applied Medical Research; Liverpool New South Wales Australia
- Centre for Medical Radiation Physics; University of Wollongong; Wollongong New South Wales Australia
| | - Mark Lee
- Cancer Therapy Centre; Liverpool Hospital; Liverpool New South Wales Australia
- South Western Clinical School; University of New South Wales; Sydney New South Wales Australia
| | - Dion Forstner
- Cancer Therapy Centre; Liverpool Hospital; Liverpool New South Wales Australia
- South Western Clinical School; University of New South Wales; Sydney New South Wales Australia
- Ingham Institute of Applied Medical Research; Liverpool New South Wales Australia
| | - Allan Fowler
- Cancer Therapy Centre; Liverpool Hospital; Liverpool New South Wales Australia
| | - Lois Holloway
- Cancer Therapy Centre; Liverpool Hospital; Liverpool New South Wales Australia
- South Western Clinical School; University of New South Wales; Sydney New South Wales Australia
- Ingham Institute of Applied Medical Research; Liverpool New South Wales Australia
- Centre for Medical Radiation Physics; University of Wollongong; Wollongong New South Wales Australia
- Institute of Medical Physics; School of Physics; University of Sydney; Sydney New South Wales Australia
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19
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Yabuki K, Sano D, Shiono O, Arai Y, Takahashi H, Chiba Y, Tanabe T, Nishimura G, Takahashi M, Taguchi T, Kaneta T, Hata M, Oridate N. Prognostic significance of metabolic tumor volume in patients with piriform sinus carcinoma treated by radiotherapy with or without concurrent chemotherapy. Head Neck 2016; 38:1666-1671. [DOI: 10.1002/hed.24488] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/12/2016] [Revised: 02/27/2016] [Accepted: 03/17/2016] [Indexed: 11/08/2022] Open
Affiliation(s)
- Kenichiro Yabuki
- Department of Otorhinolaryngology, Head and Neck Surgery; Yokohama City University School of Medicine; Yokohama Japan
| | - Daisuke Sano
- Department of Otorhinolaryngology, Head and Neck Surgery; Yokohama City University School of Medicine; Yokohama Japan
| | - Osamu Shiono
- Department of Otorhinolaryngology, Head and Neck Surgery; Yokohama City University School of Medicine; Yokohama Japan
| | - Yasuhiro Arai
- Department of Otorhinolaryngology, Head and Neck Surgery; Yokohama City University School of Medicine; Yokohama Japan
| | - Hideaki Takahashi
- Department of Otorhinolaryngology, Head and Neck Surgery; Yokohama City University School of Medicine; Yokohama Japan
| | - Yoshihiro Chiba
- Department of Otorhinolaryngology, Head and Neck Surgery; Yokohama City University School of Medicine; Yokohama Japan
| | - Teruhiko Tanabe
- Department of Otorhinolaryngology, Head and Neck Surgery; Yokohama City University School of Medicine; Yokohama Japan
| | - Goshi Nishimura
- Department of Otorhinolaryngology, Head and Neck Surgery; Yokohama City University School of Medicine; Yokohama Japan
| | - Masahiro Takahashi
- Department of Otorhinolaryngology, Head and Neck Surgery; Yokohama City University School of Medicine; Yokohama Japan
| | - Takahide Taguchi
- Department of Otorhinolaryngology, Head and Neck Surgery; Yokohama City University School of Medicine; Yokohama Japan
| | - Tomohiro Kaneta
- Department of Radiology; Yokohama City University School of Medicine; Yokohama Japan
| | - Masaharu Hata
- Department of Oncology; Yokohama City University Graduate School of Medicine; Yokohama Japan
| | - Nobuhiko Oridate
- Department of Otorhinolaryngology, Head and Neck Surgery; Yokohama City University School of Medicine; Yokohama Japan
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20
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Min M, Lin P, Lee M, Shon IH, Lin M, Forstner D, Tieu MT, Chicco A, Bray V, Fowler A. 18F-FDG PET-CT performed before and during radiation therapy of head and neck squamous cell carcinoma: Are they independent or complementary to each other? J Med Imaging Radiat Oncol 2016; 60:433-40. [PMID: 26868588 DOI: 10.1111/1754-9485.12439] [Citation(s) in RCA: 17] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/26/2015] [Accepted: 12/28/2015] [Indexed: 11/30/2022]
Abstract
INTRODUCTION The aims of this study are to evaluate the prognostic value of metabolic parameters derived from (18) F-FDG PET-CT performed before definitive radiation therapy (RT) (prePET) in patients with mucosal primary head and neck squamous cell carcinoma (MPHNSCC) and to assess the additive prognostic values of FDG PET-CT performed during RT (iPET). METHODS One hundred patients with MPHNSCC treated with radical RT underwent staging prePET and iPET performed during the third week of treatment. The maximum standardized uptake value (SUVmax ), metabolic tumour volume (MTV) and total lesional glycolysis (TLG) of primary tumour were analysed for both prePET and iPET, and results were correlated with loco-regional recurrence-free survival (LRFS), disease-free survival (DFS), metastatic failure-free survival (MFFS) and overall survival (OS), using Kaplan-Meier analysis. Optimal cut-offs (OC) for prePET and iPET were derived from Receiver Operating Characteristic curves. Patients with metabolic parameters above/below the individual OC of prePET as well as iPET (i.e. combined prePET and iPET (comPET)) were evaluated against their outcomes. RESULTS Median age was 61 years (range 39-81), median follow-up of 20 months (range 4-70, mean 27), and AJCC 7th Edition clinical stage II, III and IV were 8, 24 and 68 patients respectively. Metabolic values below individual OC in comPET were found to be associated with statistically significant improvements (P < 0.05) in DFS, LRFS and OS. In addition, patients with SUVmax above the OC in comPET were associated with worse MFFS (P = 0.011) and confirmed on both univariate (P = 0.019) and multivariate analyses (P = 0.04). CONCLUSION Addition of iPET significantly improves the prognostic values of all three metabolic parameters and can potentially be used in future adaptive local and systemic therapy trials.
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Affiliation(s)
- Myo Min
- Cancer Therapy Centre, Liverpool Hospital, Liverpool, New South Wales, Australia.,University of New South Wales, Liverpool, New South Wales, Australia.,Ingham Institute of Applied Medical Research, Liverpool, New South Wales, Australia
| | - Peter Lin
- University of New South Wales, Liverpool, New South Wales, Australia.,Department of Nuclear Medicine and PET, Liverpool Hospital, Liverpool, New South Wales, Australia.,University of Western Sydney, Liverpool, New South Wales, Australia
| | - Mark Lee
- Cancer Therapy Centre, Liverpool Hospital, Liverpool, New South Wales, Australia.,University of New South Wales, Liverpool, New South Wales, Australia
| | - Ivan Ho Shon
- University of New South Wales, Liverpool, New South Wales, Australia.,Department of Nuclear Medicine and PET, Liverpool Hospital, Liverpool, New South Wales, Australia.,University of Western Sydney, Liverpool, New South Wales, Australia
| | - Michael Lin
- University of New South Wales, Liverpool, New South Wales, Australia.,Department of Nuclear Medicine and PET, Liverpool Hospital, Liverpool, New South Wales, Australia.,University of Western Sydney, Liverpool, New South Wales, Australia
| | - Dion Forstner
- Cancer Therapy Centre, Liverpool Hospital, Liverpool, New South Wales, Australia.,University of New South Wales, Liverpool, New South Wales, Australia.,Ingham Institute of Applied Medical Research, Liverpool, New South Wales, Australia
| | - Minh Thi Tieu
- Department of Radiation Oncology, Calvary Mater Newcastle, Waratah, New South Wales, Australia.,University of Newcastle, Callaghan, New South Wales, Australia
| | - Andrew Chicco
- Department of Nuclear Medicine and PET, Liverpool Hospital, Liverpool, New South Wales, Australia
| | - Victoria Bray
- Cancer Therapy Centre, Liverpool Hospital, Liverpool, New South Wales, Australia
| | - Allan Fowler
- Cancer Therapy Centre, Liverpool Hospital, Liverpool, New South Wales, Australia
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21
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Vahle AK, Hermann S, Schäfers M, Wildner M, Kerem A, Öztürk E, Jure-Kunkel M, Franklin C, Lang S, Brandau S. Multimodal imaging analysis of an orthotopic head and neck cancer mouse model and application of anti-CD137 tumor immune therapy. Head Neck 2015; 38:542-9. [PMID: 25482887 DOI: 10.1002/hed.23929] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 12/03/2014] [Indexed: 11/06/2022] Open
Abstract
BACKGROUND Recent technical progress makes sophisticated noninvasive imaging methods available for murine models. For the first time, in this study, we applied fluorodeoxyglucose (FDG)-positron emission tomography (PET)-CT and FDG-PET-MRI to a murine orthotopic model of head and neck cancer immunotherapy. METHODS Tumor growth of floor of the mouth tumors was evaluated by multimodal small-animal imaging using FDG-PET-CT and FDG-PET-MRI. The immunotherapeutic effects of anti-CD137 antibody therapy were examined on body weight, tumor growth, and tumor-infiltrating immune cells in longitudinal imaging studies and immunohistochemical analyses. RESULTS Imaging revealed aggressive, fast-growing tumors without evidence of local or distant metastases. CD137 immunotherapy decreased tumor take and growth and stabilized body weight over time. A clear case of tumor regression was demonstrated by longitudinal PET-CT. CONCLUSION The murine model mimics the characteristics of head and neck cancer in humans and offers excellent opportunities to investigate immunomodulatory anticancer drugs. The CD137 antibody showed antitumor effects in some therapy-responsive mice.
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Affiliation(s)
- Anne-Kristin Vahle
- Department of Otorhinolaryngology, University Hospital Essen, Essen, Germany
| | - Sven Hermann
- European Institute for Molecular Imaging, University of Münster, Münster, Germany
| | - Michael Schäfers
- European Institute for Molecular Imaging, University of Münster, Münster, Germany.,Department of Nuclear Medicine, University Hospital Münster, Germany.,Cluster of Excellence EXC 1003 "CiM - Cells in Motion,", University of Münster, Münster, Germany
| | - Michael Wildner
- Department of Otorhinolaryngology, University Hospital Essen, Essen, Germany
| | - Alexander Kerem
- Department of Otorhinolaryngology, University Hospital Essen, Essen, Germany
| | - Ender Öztürk
- Department of Otorhinolaryngology, University Hospital Essen, Essen, Germany
| | | | - Cindy Franklin
- Department of Otorhinolaryngology, University Hospital Essen, Essen, Germany
| | - Stephan Lang
- Department of Otorhinolaryngology, University Hospital Essen, Essen, Germany
| | - Sven Brandau
- Department of Otorhinolaryngology, University Hospital Essen, Essen, Germany
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Prognostic Value of 18F-FDG PET/CT Metabolic Parameters in Metastatic Differentiated Thyroid Cancers. Clin Nucl Med 2015; 40:469-75. [DOI: 10.1097/rlu.0000000000000780] [Citation(s) in RCA: 22] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/26/2022]
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Schouten CS, Hakim S, Boellaard R, Bloemena E, Doornaert PA, Witte BI, Braakhuis BJM, Brakenhoff RH, Leemans CR, Hoekstra OS, de Bree R. Interaction of quantitative (18)F-FDG-PET-CT imaging parameters and human papillomavirus status in oropharyngeal squamous cell carcinoma. Head Neck 2015; 38:529-35. [PMID: 25352335 DOI: 10.1002/hed.23920] [Citation(s) in RCA: 18] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/04/2014] [Revised: 07/23/2014] [Accepted: 10/24/2014] [Indexed: 11/12/2022] Open
Abstract
BACKGROUND Patients with human papillomavirus (HPV)-positive oropharyngeal squamous cell carcinoma (SCC) have a better survival than with HPV-negative oropharyngeal SCC. An (18) F-fluorodeoxyglucose positron emission tomography-CT ((18) F-FDG-PET-CT) may also provide prognostic information. We evaluated glycolytic characteristics in HPV-negative and HPV-positive oropharyngeal SCC. METHODS Forty-four patients underwent pretreatment (18) F-FDG-PET-CT. Standardized uptake values (SUVs) and metabolic active tumor volumes (MATVs) were determined for primary tumors. HPV status was determined with p16 immunostaining, followed by high-risk HPV DNA detection on the positive cases. RESULTS Twenty-seven patients were HPV-positive (61.4%). Median MATV was 2.8 mL (range = 1.6-5.1 mL) for HPV-positive and 6.0 mL (range = 4.4-18.7 mL) for HPV-negative tumors (p < .001). SUV values are volume dependent (partial volume effect), therefore, MATV was included as covariate in multivariate analysis. In this multivariate analysis, the maximum SUV in HPV-positive tumors was 3.9 units lower than in HPV-negative tumors (p = .01). CONCLUSION The (18) F-FDG-PET-CT parameters are lower in HPV-positive than in HPV-negative patients. Low pretreatment SUV values in HPV-positive oropharyngeal SCC may be at least partly explained by HPV-induced tumor changes.
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Affiliation(s)
- Charlotte S Schouten
- Department of Otolaryngology-Head and Neck Surgery, VU University Medical Center, Amsterdam, The Netherlands
| | - Sara Hakim
- Department of Otolaryngology-Head and Neck Surgery, VU University Medical Center, Amsterdam, The Netherlands
| | - R Boellaard
- Department of Radiology and Nuclear Medicine, VU University Medical Center, Amsterdam, The Netherlands
| | - Elisabeth Bloemena
- Department of Oral and Maxillofacial Surgery/Oral Pathology, VU University Medical Center/Academic Center for Dentistry Amsterdam (ACTA), Amsterdam, The Netherlands.,Department of Pathology, VU University Medical Center, Amsterdam, The Netherlands
| | - Patricia A Doornaert
- Department of Radiation Oncology, VU University Medical Center, Amsterdam, The Netherlands
| | - Birgit I Witte
- Department of Epidemiology and Biostatistics, VU University Medical Center, Amsterdam, The Netherlands
| | - Boudewijn J M Braakhuis
- Department of Otolaryngology-Head and Neck Surgery, VU University Medical Center, Amsterdam, The Netherlands
| | - Ruud H Brakenhoff
- Department of Otolaryngology-Head and Neck Surgery, VU University Medical Center, Amsterdam, The Netherlands
| | - C René Leemans
- Department of Otolaryngology-Head and Neck Surgery, VU University Medical Center, Amsterdam, The Netherlands
| | - Otto S Hoekstra
- Department of Radiology and Nuclear Medicine, VU University Medical Center, Amsterdam, The Netherlands
| | - Remco de Bree
- Department of Otolaryngology-Head and Neck Surgery, VU University Medical Center, Amsterdam, The Netherlands
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Yabuki K, Shiono O, Komatsu M, Sano D, Nishimura G, Takahashi M, Taguchi T, Inoue T, Oridate N. Predictive and prognostic value of metabolic tumor volume (MTV) in patients with laryngeal carcinoma treated by radiotherapy (RT) / concurrent chemoradiotherapy (CCRT). PLoS One 2015; 10:e0117924. [PMID: 25692986 PMCID: PMC4334911 DOI: 10.1371/journal.pone.0117924] [Citation(s) in RCA: 23] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/24/2014] [Accepted: 01/02/2015] [Indexed: 11/19/2022] Open
Abstract
Purpose To evaluate the predictive and prognostic value of pretreatment metabolic tumor volume (MTV) in patients with treated by radiotherapy (RT) or concurrent chemoradiotherapy (CCRT). Methods We reviewed the records of 118 patients with newly diagnosed laryngeal carcinoma, who had been treated by RT or CCRT. Pretreatment positron emission tomography (PET) was performed, and MTV values were obtained by contouring margins of standardized uptake value. Clinical factors and MTV were analyzed for their association with survival. Results Patients with residual disease showed a significantly higher MTV than those with a complete response (CR) after primary treatment. Univariate analysis showed that the patients with a high MTV had a significantly lower disease-free survival (DFS) (p < 0.001). Subsite (p = 0.010), T-stage (p < 0.001), nodal metastasis (p < 0.001) and clinical stage (p < 0.001) also correlated significantly with DFS. In the multivariate analysis, MTV and clinical stage were both found to be independent prognostic factors for DFS (p = 0.001, p = 0.034, respectively). The 3-year DFS for patients with a high MTV were significantly poorer than those with a low MTV (p < 0.001). Conclusions MTV of the primary tumor is a significant prognostic factor for DFS in patients with laryngeal carcinoma treated by RT or CCRT. The results imply that MTV could be an important factor when planning treatment and follow-up for patients with laryngeal carcinoma.
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Affiliation(s)
- Kenichiro Yabuki
- Department of Otorhinolaryngology and Head and Neck Surgery, Yokohama City University School of Medicine, Yokohama, Japan
- * E-mail:
| | - Osamu Shiono
- Department of Otorhinolaryngology and Head and Neck Surgery, Yokohama City University School of Medicine, Yokohama, Japan
| | - Masanori Komatsu
- Department of Otorhinolaryngology and Head and Neck Surgery, Yokohama City University School of Medicine, Yokohama, Japan
| | - Daisuke Sano
- Department of Otorhinolaryngology and Head and Neck Surgery, Yokohama City University School of Medicine, Yokohama, Japan
| | - Goshi Nishimura
- Department of Otorhinolaryngology and Head and Neck Surgery, Yokohama City University School of Medicine, Yokohama, Japan
| | - Masahiro Takahashi
- Department of Otorhinolaryngology and Head and Neck Surgery, Yokohama City University School of Medicine, Yokohama, Japan
| | - Takahide Taguchi
- Department of Otorhinolaryngology and Head and Neck Surgery, Yokohama City University School of Medicine, Yokohama, Japan
| | - Tomio Inoue
- Department of Radiology, Yokohama City University School of Medicine, Yokohama, Japan
| | - Nobuhiko Oridate
- Department of Otorhinolaryngology and Head and Neck Surgery, Yokohama City University School of Medicine, Yokohama, Japan
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18F-FDG PET/CT as a semiquantitative imaging marker in HPV-p16-positive oropharyngeal squamous cell cancers. Nucl Med Commun 2015; 36:16-20. [DOI: 10.1097/mnm.0000000000000208] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/01/2023]
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Abstract
In this review, we review the literature on the use of PET in radiation treatment planning, with an emphasis on describing our institutional methodology (where applicable). This discussion is intended to provide other radiation oncologists with methodological details on the use of PET imaging for treatment planning in radiation oncology, or other oncologists with an introduction to the use of PET in planning radiation therapy.
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Pak K, Cheon GJ, Nam HY, Kim SJ, Kang KW, Chung JK, Kim EE, Lee DS. Prognostic value of metabolic tumor volume and total lesion glycolysis in head and neck cancer: a systematic review and meta-analysis. J Nucl Med 2014; 55:884-90. [PMID: 24752671 DOI: 10.2967/jnumed.113.133801] [Citation(s) in RCA: 232] [Impact Index Per Article: 21.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/11/2013] [Accepted: 01/29/2013] [Indexed: 12/11/2022] Open
Abstract
UNLABELLED We conducted a comprehensive systematic review of the literature on volumetric parameters and a meta-analysis of the prognostic value of metabolic tumor volume (MTV) and total lesion glycolysis (TLG) in patients with head and neck cancer (HNC). METHODS A systematic search of MEDLINE and EMBASE was performed using the key words PET, head and neck, and volume. Inclusion criteria were (18)F-FDG PET used as an initial imaging tool; studies limited to HNC; patients who had not undergone surgery, chemotherapy, or radiotherapy before PET scans; and studies reporting survival data. Event-free survival and overall survival were considered markers of outcome. The impact of MTV or TLG on survival was measured by the effect size hazard ratio (HR). Data from each study were analyzed using Review Manager. RESULTS Thirteen studies comprising 1,180 patients were included in this study. The combined HR for adverse events was 3.06 (2.33-4.01, P < 0.00001) with MTV and 3.10 (2.27-4.24, P < 0.00001) with TLG, meaning that tumors with high volumetric parameters were associated with progression or recurrence. Regarding overall survival, the pooled HR was 3.51 (2.62-4.72, P < 0.00001) with MTV and 3.14 (2.24-4.40, P < 0.00001) with TLG. There was no evidence of significant statistical heterogeneity at an I(2) of 0%. CONCLUSION MTV and TLG are prognostic predictors of outcome in patients with HNC. Despite clinically heterogeneous HNC and the various methods adopted between studies, we can confirm that patients with a high MTV or TLG have a higher risk of adverse events or death.
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Affiliation(s)
- Kyoungjune Pak
- Department of Nuclear Medicine, Seoul National University Hospital, Seoul, Korea Department of Nuclear Medicine, Pusan National University Hospital, Busan, Korea Medical Research Institute, Pusan National University Hospital, Busan, Korea
| | - Gi Jeong Cheon
- Department of Nuclear Medicine, Seoul National University Hospital, Seoul, Korea Cancer Research Institute, Seoul National University Hospital, Seoul, Korea
| | - Hyun-Yeol Nam
- Department of Nuclear Medicine, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon, Korea
| | - Seong-Jang Kim
- Department of Nuclear Medicine, Pusan National University Hospital, Busan, Korea Medical Research Institute, Pusan National University Hospital, Busan, Korea
| | - Keon Wook Kang
- Department of Nuclear Medicine, Seoul National University Hospital, Seoul, Korea Cancer Research Institute, Seoul National University Hospital, Seoul, Korea
| | - June-Key Chung
- Department of Nuclear Medicine, Seoul National University Hospital, Seoul, Korea Cancer Research Institute, Seoul National University Hospital, Seoul, Korea
| | - E Edmund Kim
- WCU Graduate School of Concergence Science and Technology, Seoul National University College of Medicine, Seoul, Korea; and University of California at Irvine, Irvine, California
| | - Dong Soo Lee
- Department of Nuclear Medicine, Seoul National University Hospital, Seoul, Korea Cancer Research Institute, Seoul National University Hospital, Seoul, Korea WCU Graduate School of Concergence Science and Technology, Seoul National University College of Medicine, Seoul, Korea; and
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