Prognostic Value of Sarcopenia and Metabolic Parameters of 18F-FDG-PET/CT in Patients with Advanced Gastroesophageal Cancer
Abstract
:1. Introduction
2. Materials and Methods
2.1. Imaging Acquisition
2.2. Image Analysis and Sarcopenia Measurements
2.3. Statistical Analysis
3. Results
3.1. Baseline Characteristics of the Study Cohort
3.2. Image Analysis and Sarcopenia Measurements
3.3. Analysis on Survival Prognostication
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2021, 71, 209–249. [Google Scholar] [CrossRef]
- Siegel, R.L.; Miller, K.D.; Fuchs, H.E.; Jemal, A. Cancer statistics, 2022. CA Cancer J. Clin. 2022, 72, 7–33. [Google Scholar] [CrossRef]
- Lund, O.; Hasenkam, J.M.; Aagaard, M.T.; Kimose, H.H. Time-related changes in characteristics of prognostic significance in carcinomas of the oesophagus and cardia. Br. J. Surg. 1989, 76, 1301–1307. [Google Scholar] [CrossRef]
- Kwon, H.R.; Pahk, K.; Park, S.; Kwon, H.W.; Kim, S. Prognostic value of metabolic information in advanced gastric cancer using preoperative 18F-FDG PET/CT. Nucl. Med. Mol. Imaging 2019, 53, 386–395. [Google Scholar] [CrossRef]
- Han, S.; Kim, Y.J.; Woo, S.; Suh, C.H.; Lee, J.J. Prognostic value of volumetric parameters of pretreatment 18F-FDG PET/CT in esophageal cancer: A systematic review and meta-analysis. Clin. Nucl. Med. 2018, 43, 887–894. [Google Scholar] [CrossRef]
- Cruz-Jentoft, A.J.; Baeyens, J.P.; Bauer, J.M.; Boirie, Y.; Cederholm, T.; Landi, F.; Martin, F.C.; Michel, J.P.; Rolland, Y.; Schneider, S.M.; et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on sarcopenia in older people. Age Ageing 2010, 39, 412–423. [Google Scholar] [CrossRef] [Green Version]
- Fearon, K.; Strasser, F.; Anker, S.D.; Bosaeus, I.; Bruera, E.; Fainsinger, R.L.; Jatoi, A.; Loprinzi, C.; MacDonald, N.; Mantovani, G.; et al. Definition and classification of cancer cachexia: An international consensus. Lancet Oncol. 2011, 12, 489–495. [Google Scholar] [CrossRef]
- Yip, C.; Goh, V.; Davies, A.; Gossage, J.; Mitchell-Hay, R.; Hynes, O.; Maisey, N.; Ross, P.; Gaya, A.; Landau, D.; et al. Assessment of sarcopenia and changes in body composition after neoadjuvant chemotherapy and associations with clinical outcomes in oesophageal cancer. Eur. Radiol. 2014, 24, 998–1005. [Google Scholar] [CrossRef]
- Sheetz, K.H.; Zhao, L.; Holcombe, S.A.; Wang, S.C.; Reddy, R.M.; Lin, J.; Orringer, M.B.; Chang, A.C. Decreased core muscle size is associated with worse patient survival following esophagectomy for cancer. Dis. Esophagus 2013, 26, 716–722. [Google Scholar] [CrossRef] [Green Version]
- Elliott, J.A.; Doyle, S.L.; Murphy, C.F.; King, S.; Guinan, E.M.; Beddy, P.; Ravi, N.; Reynolds, J.V. Sarcopenia: Prevalence, and impact on operative and oncologic outcomes in the multimodal management of locally advanced esophageal cancer. Ann. Surg. 2017, 266, 822–830. [Google Scholar] [CrossRef]
- Levolger, S.; van Vugt, J.L.A.; de Bruin, R.W.F.; Ijzermans, J.N.M. Systematic review of sarcopenia in patients operated on for gastrointestinal and hepatopancreatobiliary malignancies. Br. J. Surg. 2015, 102, 1448–1458. [Google Scholar] [CrossRef]
- Pamoukdjian, F.; Bouillet, T.; Lévy, V.; Soussan, M.; Zelek, L.; Paillaud, E. Prevalence and predictive value of pre-therapeutic sarcopenia in cancer patients: A systematic review. Clin. Nutr. 2017, 37, 1101–1113. [Google Scholar] [CrossRef]
- Makiura, D.; Ono, R.; Inoue, J.; Kashiwa, M.; Oshikiri, T.; Nakamura, T.; Kakeji, Y.; Sakai, Y.; Miura, Y. Preoperative sarcopenia is a predictor of postoperative pulmonary complications in esophageal cancer following esophagectomy: A retrospective cohort study. J. Geriatr. Oncol. 2016, 7, 430–436. [Google Scholar] [CrossRef] [Green Version]
- Hinzpeter, R.; Mirshahvalad, S.A.; Kulanthaivelu, R.; Ortega, C.; Metser, U.; Liu, Z.A.; Elimova, E.; Wong, R.K.S.; Yeung, J.; Jang, R.W.-J.; et al. Prognostic Value of [18F]-FDG PET/CT Radiomics Combined with Sarcopenia Status among Patients with Advanced Gastroesophageal Cancer. Cancers 2022, 14, 5314. [Google Scholar] [CrossRef]
- Derstine, B.A.; Holcombe, S.A.; Ross, B.E.; Wang, N.C.; Su, G.L.; Wang, S.C. Skeletal muscle cutoff values for sarcopenia diagnosis using T10 to L5 measurements in a healthy US population. Sci. Rep. 2018, 8, 11369. [Google Scholar] [CrossRef] [Green Version]
- R Core Team. R: A Language and Environment for Statistical Computing; Foundation for Statistical Computing: Vienna, Austria, 2020. [Google Scholar]
- Cruz-Jentoft, A.J.; Sayer, A.A. Sarcopenia. Lancet 2019, 393, 2636–2646. [Google Scholar] [CrossRef]
- Martin, L.; Birdsell, L.; MacDonald, N.; Reiman, T.; Clandinin, M.T.; McCargar, L.J.; Murphy, R.; Ghosh, S.; Sawyer, M.B.; Baracos, V.E. Cancer cachexia in the age of obesity: Skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J. Clin. Oncol. 2013, 31, 1539–1547. [Google Scholar] [CrossRef]
- Joglekar, S.; Nau, P.N.; Mezhir, J.J. The impact of sarcopenia on survival and complications in surgical oncology: A review of the current literature. J. Surg. Oncol. 2015, 112, 503–509. [Google Scholar] [CrossRef] [Green Version]
- Tan, B.H.; Birdsell, L.A.; Martin, L.; Baracos, V.E.; Fearon, K.C. Sarcopenia in an overweight or obese patient is an adverse prognostic factor in pancreatic cancer. Clin. Cancer Res. 2009, 15, 6973–6979. [Google Scholar] [CrossRef] [Green Version]
- Gu, W.-S.; Fang, W.-Z.; Liu, C.-Y.; Pan, K.-Y.; Ding, R.; Li, X.-H.; Duan, C.-H. Prognostic significance of combined pretreatment body mass index (BMI) and BMI loss in patients with esophageal cancer. Cancer Manag. Res. 2019, 11, 3029–3041. [Google Scholar] [CrossRef] [Green Version]
- Baracos, V.; Arribas, L. Sarcopenic obesity: Hidden muscle wasting and its impact for survival and complications of cancer therapy. Ann. Oncol. 2018, 29, ii1–ii9. [Google Scholar] [CrossRef]
- Kudou, K.; Saeki, H.; Nakashima, Y.; Edahiro, K.; Korehisa, S.; Taniguchi, D.; Tsutsumi, R.; Nishimura, S.; Nakaji, Y.; Akiyama, S.; et al. Prognostic significance of sarcopenia in patients with esophagogastric junction cancer or upper gastric cancer. Ann. Surg. Oncol. 2017, 24, 1804–1810. [Google Scholar] [CrossRef]
- Koch, C.; Reitz, C.; Schreckenbach, T.; Eichler, K.; Filmann, N.; Al-Batran, S.E.; Götze, T.; Zeuzem, S.; Bechstein, W.O.; Kraus, T.; et al. Sarcopenia as a prognostic factor for survival in patients with locally advanced gastroesophageal adenocarcinoma. PLoS ONE 2019, 14, e0223613. [Google Scholar] [CrossRef] [Green Version]
- Sato, S.; Kunisaki, C.; Suematsu, H.; Tanaka, Y.; Miyamoto, H.; Kosaka, T.; Yukawa, N.; Tanaka, K.; Sato, K.; Akiyama, H.; et al. Impact of sarcopenia in patients with unresectable locally advanced esophageal cancer receiving chemoradiotherapy. In Vivo 2018, 32, 603–610. [Google Scholar]
- Deng, H.-Y.; Zha, P.; Peng, L.; Hou, L.; Huang, K.-L.; Li, X.-Y. Preoperative sarcopenia is a predictor of poor prognosis of esophageal cancer after esophagectomy: A comprehensive systematic review and meta-analysis. Dis. Esophagus 2018, 32, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Paireder, M.; Asari, R.; Kristo, I.; Rieder, E.; Tamandl, D.; Ba-Ssalamah, A.; Schoppmann, S.F. Impact of sarcopenia on outcome in patients with esophageal resection following neoadjuvant chemotherapy for esophageal cancer. Eur. J. Surg. Oncol. 2017, 43, 478–484. [Google Scholar] [CrossRef]
- Siegal, S.R.; Dolan, J.P.; Dewey, E.N.; Guimaraes, A.R.; Tieu, B.H.; Schipper, P.H.; Hunter, J.G. Sarcopenia is not associated with morbidity, mortality, or recurrence after esophagectomy for cancer. Am. J. Surg. 2018, 215, 813–817. [Google Scholar] [CrossRef]
- Saeki, H.; Nakashima, Y.; Kudou, K.; Sasaki, S.; Jogo, T.; Hirose, K.; Edahiro, K.; Korehisa, S.; Taniguchi, D.; Nakanishi, R.; et al. Neoadjuvant chemoradiotherapy for patients with cT3/nearly T4 esophageal cancer: Is sarcopenia correlated with postoperative complications and prognosis? World J. Surg. 2018, 42, 2894–2901. [Google Scholar] [CrossRef]
- Grotenhuis, B.A.; Shapiro, J.; van Adrichem, S.; de Vries, M.; Koek, M.; Wijnhoven, B.P.; van Lanschot, J.J. Sarcopenia/muscle mass is not a prognostic factor for short-and long-term outcome after esophagectomy for cancer. World J. Surg. 2016, 40, 2698–2704. [Google Scholar] [CrossRef] [Green Version]
- Sergi, G.; Trevisan, C.; Veronese, N.; Lucato, P.; Manzato, E. Imaging of sarcopenia. Eur. J. Radiol. 2016, 85, 1519–1524. [Google Scholar] [CrossRef]
- Kitajima, K.; Nakajo, M.; Kaida, H.; Minamimoto, R.; Hirata, K.; Tsurusaki, M.; Doi, H.; Ueno, Y.; Sofue, K.; Tamaki, Y.; et al. Present and future roles of FDG-PET/CT imaging in the management of gastrointestinal cancer: An update. Nagoya J. Med. Sci. 2017, 79, 527–543. [Google Scholar] [CrossRef]
- Mallet, R.; Modzelewski, R.; LeQuesne, J.; Mihailescu, S.; Decazes, P.; Auvray, H.; Benyoucef, A.; Di Fiore, F.; Vera, P.; DuBray, B.; et al. Prognostic value of sarcopenia in patients treated by Radiochemotherapy for locally advanced oesophageal cancer. Radiat. Oncol. 2020, 15, 116. [Google Scholar] [CrossRef]
- Li, Y.; Zschaeck, S.; Lin, Q.; Chen, S.; Chen, L.; Wu, H. Metabolic parameters of sequential 18F-FDG PET/CT predict overall survival of esophageal cancer patients treated with (chemo-) radiation. Radiat. Oncol. 2019, 14, 35. [Google Scholar] [CrossRef]
- Lee, S.; Choi, Y.; Park, G.; Jo, S.; Lee, S.S.; Park, J.; Shim, H.K. 18F-FDG PET/CT Parameters for predicting prognosis in esophageal cancer patients treated with concurrent chemoradiotherapy. Technol. Cancer Res. Treat. 2021, 20, 15330338211024655. [Google Scholar] [CrossRef]
- Pan, L.; Gu, P.; Huang, G.; Xue, H.; Wu, S. Prognostic significance of SUV on PET/CT in patients with esophageal cancer: A systematic review and meta-analysis. Eur. J. Gastroenterol. Hepatol. 2009, 21, 1008–1015. [Google Scholar] [CrossRef]
Characteristics | n = 128 |
---|---|
Age (mean ± SD; range) | 63.5 ± 11.7 (29–91) |
Sex | |
Females | 26 (20%) |
Male | 102 (80%) |
BMI (kg/m2) (mean ± SD) | 24.4 ± 4.9 |
Race | |
Asian | 11 (9%) |
Non-Asian | 117 (91%) |
Siewert Class | |
AEG 1: 35–39 cm | 27 (21%) |
AEG 2: 39–42 cm | 27 (21%) |
AEG 3: 42–45 cm | 15 (12%) |
Esophagus: <35 cm | 59 (46%) |
ECOG | |
0 | 28 (22%) |
1 | 73 (57%) |
≥2 | 27 (21%) |
Tumor Grade | |
G1-2 | 47 (37%) |
G3 | 51 (40%) |
GX | 30 (23%) |
T stage | |
T0-3 | 37 (29%) |
T4 | 8 (6%) |
TX | 83 (65%) |
N stage | |
N0 | 6 (5%) |
N1 | 113 (88%) |
N2 | 4 (3%) |
NX | 5 (4%) |
M stage | 128 (100%) |
Distant Lymph Nodes | 73 (57%) |
Lung/Pleura | 24 (19%) |
Liver | 43 (34%) |
Peritoneum | 16 (12%) |
Bone | 29 (23%) |
Brain | 2 (2%) |
Sarcopenia | 60 (47%; 82% males, 18% females) |
Metabolic Parameters | Mean (Range) |
---|---|
SUVmax | 15.4 (4.1–54.4) |
SUVmean | 8.4 (2.9–25.2) |
SUVpeak | 12.9 (3.3–45.7) |
SULmax | 11.5 (2.6–39.7) |
SULmean | 6.3 (1.9–18.4) |
SULpeak | 9.7 (2.3–33.3) |
Covariate | OS | PFS | ||
---|---|---|---|---|
HR (95%CI) | p-value | HR (95%CI) | p-value | |
Age | 1.02 (1.00, 1.04) | 0.017 | 1.01 (1.00, 1.03) | 0.14 |
Sex (male) | 0.90 (0.57, 1.43) | 0.65 | 1.00 (0.64, 1.57) | 0.99 |
Race (non-Asian) | 0.69 (0.36, 1.34) | 0.28 | 0.53 (0.27, 1.02) | 0.058 |
ECOG | <0.001 | <0.001 | ||
0–1 | Reference | Reference | ||
2–3 | 3.13 (1.96, 4.98) | 2.30 (1.46, 3.62) | ||
T stage | 0.47 | 0.27 | ||
T0-3 | Reference | Reference | ||
T4 | 1.05 (0.44, 2.55) | 0.70 (0.29, 1.68) | 0.42 | |
TX | 1.30 (0.84, 2.02) | 1.25 (0.83, 1.90) | 0.28 | |
Tumor Histology | 0.68 | 0.69 | ||
Adenocarcinoma | Reference | Reference | ||
Squamous cell carcinoma | 0.92 (0.61, 1.37) | 1.08 (0.74, 1.59) | ||
Tumor Grade | 0.77 | 0.86 | ||
G1-2 | Reference | Reference | ||
G3 | 0.92 (0.60, 1.41) | 0.91 (0.60, 1.37) | 0.64 | |
GX | 1.11 (0.67, 1.85) | 1.02 (0.63, 1.66) | 0.93 | |
M | 0.44 | 0.45 | ||
M1 | Reference | Reference | ||
M1a | 0.70 (0.27, 1.79) | 0.69 (0.29, 1.65) | 0.4 | |
M1b | 1.18 (0.77, 1.79) | 1.14 (0.76, 1.70) | 0.53 | |
Distant LN | 0.79 (0.54, 1.16) | 0.23 | 0.91 (0.63, 1.31) | 0.61 |
Lung/ Pleura | 1.06 (0.65, 1.73) | 0.8 | 1.09 (0.68, 1.73) | 0.73 |
Liver | 1.27 (0.85, 1.89) | 0.25 | 1.15 (0.78, 1.70) | 0.47 |
Peritoneum | 1.34 (0.78, 2.32) | 0.29 | 1.01 (0.58, 1.73) | 0.98 |
Bone | 1.67 (1.06, 2.63) | 0.028 | 1.61 (1.03, 2.51) | 0.038 |
Brain | 0.49 (0.07, 3.53) | 0.48 | 1.63 (0.40, 6.63) | 0.5 |
SUVmax | 0.99 (0.96, 1.01) | 0.33 | 1.00 (0.97, 1.02) | 0.86 |
SUVmean | 0.96 (0.91, 1.01) | 0.15 | 0.99 (0.94, 1.04) | 0.6 |
SUVpeak | 0.98 (0.95, 1.01) | 0.26 | 0.99 (0.96, 1.02) | 0.68 |
SULmax | 0.99 (0.96, 1.02) | 0.5 | 1.00 (0.97, 1.04) | 0.83 |
SULmean | 0.96 (0.89, 1.03) | 0.23 | 0.99 (0.92, 1.07) | 0.86 |
SULpeak | 0.98 (0.94, 1.02) | 0.4 | 1.00 (0.96, 1.04) | 0.99 |
BMI (kg/m2) | 0.97 (0.93, 1.02) | 0.21 | 0.98 (0.94, 1.02) | 0.3 |
SMI (cm2/m2) | 0.97 (0.95, 0.99) | 0.0075 | 0.97 (0.96, 0.99) | 0.011 |
Sarcopenia (yes) | 1.51 (1.03, 2.22) | 0.033 | 1.55 (1.07, 2.25) | 0.021 |
Covariate | OS | PFS | ||
---|---|---|---|---|
HR (95%CI) | p-Value | HR (95%CI) | p-Value | |
Age | 1.01 (0.99, 1.03) | 0.2 | ||
ECOG | <0.001 | <0.001 | ||
0–1 | reference | reference | ||
2–3 | 2.91 (1.75, 4.82) | 2.27 (1.43, 3.61) | ||
Bone | 0.01 | 0.019 | ||
No | reference | reference | ||
Yes | 1.84 (1.16, 2.94) | 1.71 (1.09, 2.69) | ||
SMI (cm2/m2) | 0.98 (0.96, 1.00) | 0.065 | 0.98 (0.96, 1.00) | 0.03 |
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Hinzpeter, R.; Mirshahvalad, S.A.; Kulanthaivelu, R.; Murad, V.; Ortega, C.; Metser, U.; Liu, Z.A.; Elimova, E.; Wong, R.K.S.; Yeung, J.; et al. Prognostic Value of Sarcopenia and Metabolic Parameters of 18F-FDG-PET/CT in Patients with Advanced Gastroesophageal Cancer. Diagnostics 2023, 13, 838. https://doi.org/10.3390/diagnostics13050838
Hinzpeter R, Mirshahvalad SA, Kulanthaivelu R, Murad V, Ortega C, Metser U, Liu ZA, Elimova E, Wong RKS, Yeung J, et al. Prognostic Value of Sarcopenia and Metabolic Parameters of 18F-FDG-PET/CT in Patients with Advanced Gastroesophageal Cancer. Diagnostics. 2023; 13(5):838. https://doi.org/10.3390/diagnostics13050838
Chicago/Turabian StyleHinzpeter, Ricarda, Seyed Ali Mirshahvalad, Roshini Kulanthaivelu, Vanessa Murad, Claudia Ortega, Ur Metser, Zhihui Amy Liu, Elena Elimova, Rebecca K. S. Wong, Jonathan Yeung, and et al. 2023. "Prognostic Value of Sarcopenia and Metabolic Parameters of 18F-FDG-PET/CT in Patients with Advanced Gastroesophageal Cancer" Diagnostics 13, no. 5: 838. https://doi.org/10.3390/diagnostics13050838
APA StyleHinzpeter, R., Mirshahvalad, S. A., Kulanthaivelu, R., Murad, V., Ortega, C., Metser, U., Liu, Z. A., Elimova, E., Wong, R. K. S., Yeung, J., Jang, R. W., & Veit-Haibach, P. (2023). Prognostic Value of Sarcopenia and Metabolic Parameters of 18F-FDG-PET/CT in Patients with Advanced Gastroesophageal Cancer. Diagnostics, 13(5), 838. https://doi.org/10.3390/diagnostics13050838