Maximum standardized uptake value on FDG‑PET predicts survival in stage I non‑small cell lung cancer following carbon ion radiotherapy

Shirai,Katsuyuki; Abe,Takanori; Saitoh,Jun‑Ichi; Mizukami,Tatsuji; Irie,Daisuke; Takakusagi,Yosuke; Shiba,Shintaro; Okano,Naoko; Ebara,Takeshi; Ohno,Tatsuya; Nakano,Takashi

doi:10.3892/ol.2017.5952

Maximum standardized uptake value on FDG‑PET predicts survival in stage I non‑small cell lung cancer following carbon ion radiotherapy

Authors:
- Katsuyuki Shirai
- Takanori Abe
- Jun‑Ichi Saitoh
- Tatsuji Mizukami
- Daisuke Irie
- Yosuke Takakusagi
- Shintaro Shiba
- Naoko Okano
- Takeshi Ebara
- Tatsuya Ohno
- Takashi Nakano
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Affiliations: Gunma University Heavy Ion Medical Center, Maebashi, Gunma 371‑8511, Japan, Department of Radiation Oncology, Gunma Prefectural Cancer Center, Ota, Gunma 373‑8550, Japan
Published online on: March 29, 2017 https://doi.org/10.3892/ol.2017.5952
Pages: 4420-4426

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Abstract

The present study (University Hospital Medical Information Network study no. UMIN000003797) aimed to evaluate whether the maximum standardized uptake value (SUVmax) of pretreatment 18F‑fluorodeoxyglucose‑positron emission tomography (FDG‑PET) is prognostic factor for stage I non‑small cell lung cancer (NSCLC) treated with carbon ion radiotherapy (C‑ion RT). Patients treated between June 2010 and June 2013 at Gunma University Heavy Ion Medical Center (Maebashi, Japan) on a prospective protocol were included in the present study. Patients with T1a‑b and T2a NSCLC were treated with C‑ion RT at a dose of 52.8 Gy [relative biological effectiveness (RBE)] and 60.0 Gy (RBE), respectively, in four fractions. Prior to treatment, all patients underwent FDG‑PET, in which the SUVmax of primary tumors was evaluated. Local control, progression‑free survival (PFS), and overall survival (OS) were calculated. A total of 45 patients were analyzed and the median follow‑up period was 28.9 months. The 2‑year local control, PFS and OS rates for all patients were 93, 78 and 89%, respectively. The mean SUVmax of primary tumors was 5.5, and patients were divided into higher (≥5.5) and lower (<5.5) SUVmax groups. The 2‑year PFS rates were 61 and 89% for the higher and lower SUVmax groups, respectively (P=0.01), and the 2‑year OS rates for the higher and lower SUVmax groups were 76 and 96%, respectively (P=0.01). The higher SUVmax group exhibited a significantly worse PFS and OS compared with the lower SUVmax group; however, the SUVmax was not associated with the local control rate. In total, 2 patients (4%) experienced grade 2 or 3 radiation pneumonitis, with their symptoms improved through conservative treatment. No patients experienced any grade 4 or 5 toxicities. The results of the present study indicate that pretreatment SUVmax is a prognostic indicator for outcomes in patients with stage I NSCLC treated with C‑ion RT.

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1	Nakamura K, Ukawa S, Okada E, Hirata M, Nagai A, Yamagata Z, Ninomiya T, Muto K, Kiyohara Y, Matsuda K, et al: Characteristics and prognosis of Japanese male and female lung cancer patients: The BioBank Japan Project. J Epidemiol. 27:S49–S57. 2017. View Article : Google Scholar : PubMed/NCBI
2	Palma D, Visser O, Lagerwaard FJ, Belderbos J, Slotman BJ and Senan S: Impact of introducing stereotactic lung radiotherapy for elderly patients with stage I non-small-cell lung cancer: A population-based time-trend analysis. J Clin Oncol. 28:5153–5159. 2010. View Article : Google Scholar : PubMed/NCBI
3	Timmerman R, Paulus R, Galvin J, Michalski J, Straube W, Bradley J, Fakiris A, Bezjak A, Videtic G, Johnstone D, et al: Stereotactic body radiation therapy for inoperable early stage lung cancer. JAMA. 303:1070–1076. 2010. View Article : Google Scholar : PubMed/NCBI
4	Onishi H, Shirato H, Nagata Y, Hiraoka M, Fujino M, Gomi K, Karasawa K, Hayakawa K, Niibe Y, Takai Y, et al: Stereotactic body radiotherapy (SBRT) for operable stage I non-small-cell lung cancer: Can SBRT be comparable to surgery? Int J Radiat Oncol Biol Phys. 81:1352–1358. 2011. View Article : Google Scholar : PubMed/NCBI
5	Kanai T, Endo M, Minohara S, Miyahara N, Koyama-ito H, Tomura H, Matsufuji N, Futami Y, Fukumura A, Hiraoka T, et al: Biophysical characteristics of HIMAC clinical irradiation system for heavy-ion radiation therapy. Int J Radiat Oncol Biol Phys. 44:201–210. 1999. View Article : Google Scholar : PubMed/NCBI
6	Schulz-Ertner D and Tsujii H: Particle radiation therapy using proton and heavier ion beams. J Clin Oncol. 25:953–964. 2007. View Article : Google Scholar : PubMed/NCBI
7	Ando K and Kase Y: Biological characteristics of carbon-ion therapy. Int J Radiat Biol. 85:715–728. 2009. View Article : Google Scholar : PubMed/NCBI
8	Miyamoto T, Baba M, Sugane T, Nakajima M, Yashiro T, Kagei K, Hirasawa N, Sugawara T, Yamamoto N, Koto M, et al: Carbon ion radiotherapy for stage I non-small cell lung cancer using a regimen of four fractions during 1 week. J Thorac Oncol. 2:916–926. 2007. View Article : Google Scholar : PubMed/NCBI
9	Miyamoto T, Baba M, Yamamoto N, Koto M, Sugawara T, Yashiro T, Kadono K, Ezawa H, Tsujii H, Mizoe JE, et al: Curative treatment of Stage I non-small-cell lung cancer with carbon ion beams using a hypofractionated regimen. Int J Radiat Oncol Biol Phys. 67:750–758. 2007. View Article : Google Scholar : PubMed/NCBI
10	Iwata H, Murakami M, Demizu Y, Miyawaki D, Terashima K, Niwa Y, Mima M, Akagi T, Hishikawa Y and Shibamoto Y: High-dose proton therapy and carbon-ion therapy for stage I non-small cell lung cancer. Cancer. 116:2476–2485. 2010.PubMed/NCBI
11	Shirai K, Nakagawa A, Abe T, Kawahara M, Saitoh J, Ohno T and Nakano T: Use of FDG-PET in radiation treatment planning for thoracic cancers. Int J Mol Imaging. 2012:6095452012. View Article : Google Scholar : PubMed/NCBI
12	Lardinois D, Weder W, Hany TF, Kamel EM, Korom S, Seifert B, von Schulthess GK and Steinert HC: Staging of non-small-cell lung cancer with integrated positron-emission tomography and computed tomography. N Engl J Med. 348:2500–2507. 2003. View Article : Google Scholar : PubMed/NCBI
13	Pieterman RM, van Putten JW, Meuzelaar JJ, Mooyaart EL, Vaalburg W, Koëter GH, Fidler V, Pruim J and Groen HJ: Preoperative staging of non-small-cell lung cancer with positron- emission tomography. N Engl J Med. 343:254–261. 2000. View Article : Google Scholar : PubMed/NCBI
14	Lammering G, de Ruysscher D, van Baardwijk A, Baumert BG, Borger J, Lutgens L, van den Ende P, Ollers M and Lambin P: The use of FDG-PET to target tumors by radiotherapy. Strahlenther Onkol. 186:471–481. 2010. View Article : Google Scholar : PubMed/NCBI
15	Dooms C, Verbeken E, Stroobants S, Nackaerts K, De Leyn P and Vansteenkiste J: Prognostic stratification of stage IIIA-N2 non-small-cell lung cancer after induction chemotherapy: A model based on the combination of morphometric-pathologic response in mediastinal nodes and primary tumor response on serial 18-fluoro-2-deoxy-glucose positron emission tomography. J Clin Oncol. 26:1128–1134. 2008. View Article : Google Scholar : PubMed/NCBI
16	Mac Manus MP, Hicks RJ, Matthews JP, Wirth A, Rischin D and Ball DL: Metabolic (FDG-PET) response after radical radiotherapy/chemoradiotherapy for non-small cell lung cancer correlates with patterns of failure. Lung Cancer. 49:95–108. 2005. View Article : Google Scholar : PubMed/NCBI
17	Huang W, Zhou T, Ma L, Sun H, Gong H, Wang J, Yu J and Li B: Standard uptake value and metabolic tumor volume of ¹⁸F-FDG PET/CT predict short-term outcome early in the course of chemoradiotherapy in advanced non-small cell lung cancer. Eur J Nucl Med Mol Imaging. 38:1628–1635. 2011. View Article : Google Scholar : PubMed/NCBI
18	Berghmans T, Dusart M, Paesmans M, Hossein-Foucher C, Buvat I, Castaigne C, Scherpereel A, Mascaux C, Moreau M, Roelandts M, et al: Primary tumor standardized uptake value (SUVmax) measured on fluorodeoxyglucose positron emission tomography (FDG-PET) is of prognostic value for survival in non-small cell lung cancer (NSCLC): A systematic review and meta-analysis (MA) by the European Lung Cancer Working Party for the IASLC Lung Cancer Staging Project. J Thorac Oncol. 3:6–12. 2008. View Article : Google Scholar : PubMed/NCBI
19	Tashiro M, Ishii T, Koya J, Okada R, Kurosawa Y, Arai K, Abe S, Ohashi Y, Shimada H, Yusa K, et al: Technical approach to individualized respiratory-gated carbon-ion therapy for mobile organs. Radiol Phys Technol. 6:356–366. 2013. View Article : Google Scholar : PubMed/NCBI
20	National Cancer Institute, . Common Terminology Criteria for Adverse Events (CTCAE v4.0). https://ctep.cancer.gov/protocolDevelopment/electronic_applications/ctc.htmlNovember 14–2016
21	Coon D, Gokhale AS, Burton SA, Heron DE, Ozhasoglu C and Christie N: Fractionated stereotactic body radiation therapy in the treatment of primary, recurrent, and metastatic lung tumors: The role of positron emission tomography/computed tomography-based treatment planning. Clin Lung Cancer. 9:217–221. 2008. View Article : Google Scholar : PubMed/NCBI
22	Burdick MJ, Stephans KL, Reddy CA, Djemil T, Srinivas SM and Videtic GM: Maximum standardized uptake value from staging FDG-PET/CT does not predict treatment outcome for early-stage non-small-cell lung cancer treated with stereotactic body radiotherapy. Int J Radiat Oncol Biol Phys. 78:1033–1039. 2010. View Article : Google Scholar : PubMed/NCBI
23	Takeda A, Yokosuka N, Ohashi T, Kunieda E, Fujii H, Aoki Y, Sanuki N, Koike N and Ozawa Y: The maximum standardized uptake value (SUVmax) on FDG-PET is a strong predictor of local recurrence for localized non-small-cell lung cancer after stereotactic body radiotherapy (SBRT). Radiother Oncol. 101:291–297. 2011. View Article : Google Scholar : PubMed/NCBI
24	Chang JY, Liu H, Balter P, Komaki R, Liao Z, Welsh J, Mehran RJ, Roth JA and Swisher SG: Clinical outcome and predictors of survival and pneumonitis after stereotactic ablative radiotherapy for stage I non-small cell lung cancer. Radiat Oncol. 7:1522012. View Article : Google Scholar : PubMed/NCBI
25	Clarke K, Taremi M, Dahele M, Freeman M, Fung S, Franks K, Bezjak A, Brade A, Cho J, Hope A, et al: Stereotactic body radiotherapy (SBRT) for non-small cell lung cancer (NSCLC): Is FDG-PET a predictor of outcome? Radiother Oncol. 104:62–66. 2012. View Article : Google Scholar : PubMed/NCBI
26	Na F, Wang J, Li C, Deng L, Xue J and Lu Y: Primary tumor standardized uptake value measured on F18-Fluorodeoxyglucose positron emission tomography is of prediction value for survival and local control in non-small-cell lung cancer receiving radiotherapy: Meta-analysis. J Thorac Oncol. 9:834–842. 2014. View Article : Google Scholar : PubMed/NCBI
27	Goodgame B, Pillot GA, Yang Z, Shriki J, Meyers BF, Zoole J, Gao F, Dehdashti F, Patterson A, Siegel BA and Govindan R: Prognostic value of preoperative positron emission tomography in resected stage I non-small cell lung cancer. J Thorac Oncol. 3:130–134. 2008. View Article : Google Scholar : PubMed/NCBI
28	Nair VS, Krupitskaya Y and Gould MK: Positron emission tomography 18F-fluorodeoxyglucose uptake and prognosis in patients with surgically treated, stage I non-small cell lung cancer: A systematic review. J Thorac Oncol. 4:1473–1479. 2009. View Article : Google Scholar : PubMed/NCBI
29	Vesselle H, Schmidt RA, Pugsley JM, Li M, Kohlmyer SG, Vallires E and Wood DE: Lung cancer proliferation correlates with [F-18]fluorodeoxyglucose uptake by positron emission tomography. Clin Cancer Res. 6:3837–3844. 2000.PubMed/NCBI
30	van Baardwijk A, Dooms C, van Suylen RJ, Verbeken E, Hochstenbag M, Dehing-Oberije C, Rupa D, Pastorekova S, Stroobants S, Buell U, et al: The maximum uptake of (18)F-deoxyglucose on positron emission tomography scan correlates with survival, hypoxia inducible factor-1alpha and GLUT-1 in non-small cell lung cancer. Eur J Cancer. 43:1392–1398. 2007. View Article : Google Scholar : PubMed/NCBI
31	Satoh Y, Onishi H, Nambu A and Araki T: Volume-based parameters measured by using FDG PET/CT in patients with stage I NSCLC treated with stereotactic body radiation therapy: Prognostic value. Radiology. 270:275–281. 2014. View Article : Google Scholar : PubMed/NCBI
32	Salavati A, Borofsky S, Boon-Keng TK, Houshmand S, Khiewvan B, Saboury B, Codreanu I, Torigian DA, Zaidi H and Alavi A: Application of partial volume effect correction and 4D PET in the quantification of FDG avid lung lesions. Mol Imaging Biol. 17:140–148. 2015. View Article : Google Scholar : PubMed/NCBI