Is there utility for fluorine-18-fluorodeoxyglucose positron-emission tomography scan before surgery in breast cancer? A 15-year overall survival analysis

Justine Perrin, Karim Farid, Hilde Van Parijs, Olena Gorobets, Vincent Vinh-Hung, Nam P Nguyen, Navid Djassemi, Mark De Ridder, Hendrik Everaert, Justine Perrin, Karim Farid, Hilde Van Parijs, Olena Gorobets, Vincent Vinh-Hung, Nam P Nguyen, Navid Djassemi, Mark De Ridder, Hendrik Everaert

Abstract

Background: The prognostic value of preoperative fluorine-18-fluorodeoxyglucose positron-emission tomography (18F-FDG PET) scan for determining overall survival (OS) in breast cancer (BC) patients is controversial.

Aim: To evaluate the OS predictive value of preoperative PET positivity after 15 years.

Methods: We performed a retrospective search of the Universitair Ziekenhuis Brussel patient database for nonmetastatic patients who underwent preoperative PET between 2002-2008. PET positivity was determined by anatomical region of interest (AROI) findings for breast and axillary, sternal, and distant sites. The prognostic role of PET was examined as a qualitative binary factor (positive vs negative status) and as a continuous variable [maximum standard uptake value (SUVmax)] in multivariate survival analyses using Cox proportional hazards models. Among the 104 identified patients who received PET, 36 were further analyzed for the SUVmax in the AROI.

Results: Poor OS within the 15-year study period was predicted by PET-positive status for axillary (P = 0.033), sternal (P = 0.033), and combined PET-axillary/sternal (P = 0.008) nodes. Poor disease-free survival was associated with PET-positive axillary status (P = 0.040) and combined axillary/sternal status (P = 0.023). Cox models confirmed the long-term prognostic value of combined PET-axillary/sternal status [hazard ratio (HR): 3.08, 95% confidence interval: 1.42-6.69]. SUVmax of ipsilateral breast and axilla as continuous covariates were significant predictors of long-term OS with HRs of 1.25 (P = 0.048) and 1.54 (P = 0.029), corresponding to relative increase in the risk of death of 25% and 54% per SUVmax unit, respectively. In addition, the ratio of the ipsilateral axillary SUVmax over the contralateral axillary SUVmax was the most significant OS predictor (P = 0.027), with 1.94 HR, indicating a two-fold relative increase of mortality risk.

Conclusion: Preoperative PET is valuable for prediction of long-term survival. Ipsilateral axillary SUVmax ratio over the uninvolved side represents a new prognostic finding that warrants further investigation.

Keywords: Breast surgery; Long-term prognosis; Overall survival; Positron-emission tomography scan; Preoperative workup; Restricted mean survival time.

Conflict of interest statement

Conflict-of-interest statement: The authors declare that they have no financial relationships to disclose.

©The Author(s) 2022. Published by Baishideng Publishing Group Inc. All rights reserved.

Figures

Figure 1
Figure 1
Anatomical regions of interest. Free-hand three-dimensional non-overlapping anatomical regions of interest (AROI) volumes drawn on the PET scan workstation for the right breast (red), right axilla-supraclavicular nodal area (blue), left breast (green), left axilla-supraclavicular (orange), and sternal-mediastinal area (purple). Viewing planes are indicated by crosshairs.
Figure 2
Figure 2
Overall survival according to fluorine-18-fluorodeoxyglucose positron-emission tomography status in anatomical regions of interest. A: Breast; B: Axillary; C: Distant; D: Sternal; E: Any axillary, sternal or distant; F: Any axillary or sternal.
Figure 3
Figure 3
Disease-free survival according to fluorine-18-fluorodeoxyglucose positron-emission tomography status in anatomical regions of interest. A: Breast; B: Axillary; C: Distant; D: Sternal; E: Any axillary, sternal or distant; F: Any axillary or sternal.

References

    1. Global Burden of Disease Cancer Collaboration, Fitzmaurice C, Akinyemiju TF, Al Lami FH, Alam T, Alizadeh-Navaei R, Allen C, Alsharif U, Alvis-Guzman N, Amini E, Anderson BO, Aremu O, Artaman A, Asgedom SW, Assadi R, Atey TM, Avila-Burgos L, Awasthi A, Ba Saleem HO, Barac A, Bennett JR, Bensenor IM, Bhakta N, Brenner H, Cahuana-Hurtado L, Castañeda-Orjuela CA, Catalá-López F, Choi JJ, Christopher DJ, Chung SC, Curado MP, Dandona L, Dandona R, das Neves J, Dey S, Dharmaratne SD, Doku DT, Driscoll TR, Dubey M, Ebrahimi H, Edessa D, El-Khatib Z, Endries AY, Fischer F, Force LM, Foreman KJ, Gebrehiwot SW, Gopalani SV, Grosso G, Gupta R, Gyawali B, Hamadeh RR, Hamidi S, Harvey J, Hassen HY, Hay RJ, Hay SI, Heibati B, Hiluf MK, Horita N, Hosgood HD, Ilesanmi OS, Innos K, Islami F, Jakovljevic MB, Johnson SC, Jonas JB, Kasaeian A, Kassa TD, Khader YS, Khan EA, Khan G, Khang YH, Khosravi MH, Khubchandani J, Kopec JA, Kumar GA, Kutz M, Lad DP, Lafranconi A, Lan Q, Legesse Y, Leigh J, Linn S, Lunevicius R, Majeed A, Malekzadeh R, Malta DC, Mantovani LG, McMahon BJ, Meier T, Melaku YA, Melku M, Memiah P, Mendoza W, Meretoja TJ, Mezgebe HB, Miller TR, Mohammed S, Mokdad AH, Moosazadeh M, Moraga P, Mousavi SM, Nangia V, Nguyen CT, Nong VM, Ogbo FA, Olagunju AT, Pa M, Park EK, Patel T, Pereira DM, Pishgar F, Postma MJ, Pourmalek F, Qorbani M, Rafay A, Rawaf S, Rawaf DL, Roshandel G, Safiri S, Salimzadeh H, Sanabria JR, Santric Milicevic MM, Sartorius B, Satpathy M, Sepanlou SG, Shackelford KA, Shaikh MA, Sharif-Alhoseini M, She J, Shin MJ, Shiue I, Shrime MG, Sinke AH, Sisay M, Sligar A, Sufiyan MB, Sykes BL, Tabarés-Seisdedos R, Tessema GA, Topor-Madry R, Tran TT, Tran BX, Ukwaja KN, Vlassov VV, Vollset SE, Weiderpass E, Williams HC, Yimer NB, Yonemoto N, Younis MZ, Murray CJL, Naghavi M. Global, Regional, and National Cancer Incidence, Mortality, Years of Life Lost, Years Lived With Disability, and Disability-Adjusted Life-Years for 29 Cancer Groups, 1990 to 2016: A Systematic Analysis for the Global Burden of Disease Study. JAMA Oncol. 2018;4:1553–1568.
    1. Miladinova D. Molecular Imaging in Breast Cancer. Nucl Med Mol Imaging. 2019;53:313–319.
    1. Jeong YJ, Kang DY, Yoon HJ, Son HJ. Additional value of F-18 FDG PET/CT for initial staging in breast cancer with clinically negative axillary nodes. Breast Cancer Res Treat. 2014;145:137–142.
    1. Liu Y. Role of FDG PET-CT in evaluation of locoregional nodal disease for initial staging of breast cancer. World J Clin Oncol. 2014;5:982–989.
    1. Ulaner GA, Castillo R, Wills J, Gönen M, Goldman DA. 18F-FDG-PET/CT for systemic staging of patients with newly diagnosed ER-positive and HER2-positive breast cancer. Eur J Nucl Med Mol Imaging. 2017;44:1420–1427.
    1. Vinh-Hung V, Everaert H, Lamote J, Voordeckers M, van Parijs H, Vanhoeij M, Verfaillie G, Fontaine C, Vees H, Ratib O, Vlastos G, De Ridder M. Diagnostic and prognostic correlates of preoperative FDG PET for breast cancer. Eur J Nucl Med Mol Imaging. 2012;39:1618–1627.
    1. Diao W, Tian F, Jia Z. The prognostic value of SUVmax measuring on primary lesion and ALN by 18F-FDG PET or PET/CT in patients with breast cancer. Eur J Radiol. 2018;105:1–7.
    1. Wen W, Xuan D, Hu Y, Li X, Liu L, Xu D. Prognostic value of maximum standard uptake value, metabolic tumor volume, and total lesion glycolysis of positron emission tomography/computed tomography in patients with breast cancer: A systematic review and meta-analysis. PLoS One. 2019;14:e0225959.
    1. Royston P, Parmar MK. Restricted mean survival time: an alternative to the hazard ratio for the design and analysis of randomized trials with a time-to-event outcome. BMC Med Res Methodol. 2013;13:152.
    1. Nielsen MH, Berg M, Pedersen AN, Andersen K, Glavicic V, Jakobsen EH, Jensen I, Josipovic M, Lorenzen EL, Nielsen HM, Stenbygaard L, Thomsen MS, Vallentin S, Zimmermann S, Offersen BV Danish Breast Cancer Cooperative Group Radiotherapy Committee. Delineation of target volumes and organs at risk in adjuvant radiotherapy of early breast cancer: national guidelines and contouring atlas by the Danish Breast Cancer Cooperative Group. Acta Oncol. 2013;52:703–710.
    1. van Buuren S. Multiple imputation of discrete and continuous data by fully conditional specification. Stat Methods Med Res. 2007;16:219–242.
    1. Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc. 1958;53:457–481.
    1. Therneau TM, Grambsch PM. Modeling survival data: extending the Cox model New York, NY Springer-Verlag 2000.
    1. Royston P, Sauerbrei W. A new measure of prognostic separation in survival data. Stat Med. 2004;23:723–748.
    1. R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing 2020; R version 3.6.3.
    1. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti Iii A. American Joint Committee on Cancer. AJCC Cancer Staging Manual Seventh Edition. New York, Dordrecht, Heidelberg, London: Springer, 2010.
    1. Cleemput I, Dargent G, Poelmans J, Camberlin C, Van den Bruel A, Ramaekers D. HTA Positron Emission Tomography in Belgium. KCE Reports. Brussels: Belgian Health Care Knowledge Centre (KCE), 2005.
    1. Wahl RL, Jacene H, Kasamon Y, Lodge MA. From RECIST to PERCIST: Evolving Considerations for PET response criteria in solid tumors. J Nucl Med. 2009;50 Suppl 1:122S–150S.
    1. Cooper KL, Harnan S, Meng Y, Ward SE, Fitzgerald P, Papaioannou D, Wyld L, Ingram C, Wilkinson ID, Lorenz E. Positron emission tomography (PET) for assessment of axillary lymph node status in early breast cancer: A systematic review and meta-analysis. Eur J Surg Oncol. 2011;37:187–198.
    1. Groheux D, Giacchetti S, Espié M, Vercellino L, Hamy AS, Delord M, Berenger N, Toubert ME, Misset JL, Hindié E. The yield of 18F-FDG PET/CT in patients with clinical stage IIA, IIB, or IIIA breast cancer: a prospective study. J Nucl Med. 2011;52:1526–1534.
    1. Humbert O, Berriolo-Riedinger A, Riedinger JM, Coudert B, Arnould L, Cochet A, Loustalot C, Fumoleau P, Brunotte F. Changes in 18F-FDG tumor metabolism after a first course of neoadjuvant chemotherapy in breast cancer: influence of tumor subtypes. Ann Oncol. 2012;23:2572–2577.
    1. Bos R, van Der Hoeven JJ, van Der Wall E, van Der Groep P, van Diest PJ, Comans EF, Joshi U, Semenza GL, Hoekstra OS, Lammertsma AA, Molthoff CF. Biologic correlates of (18)fluorodeoxyglucose uptake in human breast cancer measured by positron emission tomography. J Clin Oncol. 2002;20:379–387.
    1. Groheux D, Hindié E, Delord M, Giacchetti S, Hamy AS, de Bazelaire C, de Roquancourt A, Vercellino L, Toubert ME, Merlet P, Espié M. Prognostic impact of (18)FDG-PET-CT findings in clinical stage III and IIB breast cancer. J Natl Cancer Inst. 2012;104:1879–1887.
    1. Jo I, Zeon SK, Kim SH, Kim HW, Kang SH, Kwon SY, Kim SJ. Correlation of Primary Tumor FDG Uptake with Clinicopathologic Prognostic Factors in Invasive Ductal Carcinoma of the Breast. Nucl Med Mol Imaging. 2015;49:19–25.
    1. Pritchard KI, Julian JA, Holloway CM, McCready D, Gulenchyn KY, George R, Hodgson N, Lovrics P, Perera F, Elavathil L, O'Malley FP, Down N, Bodurtha A, Shelley W, Levine MN. Prospective study of 2-[¹⁸F]fluorodeoxyglucose positron emission tomography in the assessment of regional nodal spread of disease in patients with breast cancer: an Ontario clinical oncology group study. J Clin Oncol. 2012;30:1274–1279.
    1. Fisher B, Slack NH, Bross ID. Cancer of the breast: size of neoplasm and prognosis. Cancer. 1969;24:1071–1080.
    1. Dehbi HM, Royston P, Hackshaw A. Life expectancy difference and life expectancy ratio: two measures of treatment effects in randomised trials with non-proportional hazards. BMJ. 2017;357:j2250.
    1. Adunlin G, Cyrus JW, Dranitsaris G. Correlation between progression-free survival and overall survival in metastatic breast cancer patients receiving anthracyclines, taxanes, or targeted therapies: a trial-level meta-analysis. Breast Cancer Res Treat. 2015;154:591–608.
    1. Harrell FE Jr, Lee KL, Mark DB. Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996;15:361–387.
    1. Yoo J, Kim BS, Chung J, Yoon HJ. Clinical value of delayed 18F-FDG PET/CT for predicting nipple-areolar complex involvement in breast cancer: A comparison with clinical symptoms and breast MRI. PLoS One. 2018;13:e0203649.
    1. Perani D. FDG PET and cognitive symptoms of dementia. Clin Transl Imaging. 2013;1:247–260.
    1. Boellaard R, Delgado-Bolton R, Oyen WJ, Giammarile F, Tatsch K, Eschner W, Verzijlbergen FJ, Barrington SF, Pike LC, Weber WA, Stroobants S, Delbeke D, Donohoe KJ, Holbrook S, Graham MM, Testanera G, Hoekstra OS, Zijlstra J, Visser E, Hoekstra CJ, Pruim J, Willemsen A, Arends B, Kotzerke J, Bockisch A, Beyer T, Chiti A, Krause BJ European Association of Nuclear Medicine (EANM) FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur J Nucl Med Mol Imaging. 2015;42:328–354.
    1. Cerci JJ, Linardi CC, Pracchia LF, Junior JS, Trindade E, Delbeke D, Cerci RJ, Carr R, Meneghetti JC, Buccheri V. 2-[18F]-fluoro-2-desoxy-D-glucose positron emission tomography initial staging impacts on survival in Hodgkin lymphoma. World J Radiol. 2013;5:484–490.
    1. Siddiqui F, Yao M. Application of fluorodeoxyglucose positron emission tomography in the management of head and neck cancers. World J Radiol. 2014;6:238–251.
    1. Awan MJ, Siddiqui F, Schwartz D, Yuan J, Machtay M, Yao M. Application of positron emission tomography/computed tomography in radiation treatment planning for head and neck cancers. World J Radiol. 2015;7:382–393.
    1. Detry O, Govaerts L, Deroover A, Vandermeulen M, Meurisse N, Malenga S, Bletard N, Mbendi C, Lamproye A, Honoré P, Meunier P, Delwaide J, Hustinx R. Prognostic value of (18)F-FDG PET/CT in liver transplantation for hepatocarcinoma. World J Gastroenterol. 2015;21:3049–3054.
    1. Abuodeh Y, Naghavi AO, Ahmed KA, Venkat PS, Kim Y, Kis B, Choi J, Biebel B, Sweeney J, Anaya DA, Kim R, Malafa M, Frakes JM, Hoffe SE, El-Haddad G. Prognostic value of pre-treatment F-18-FDG PET-CT in patients with hepatocellular carcinoma undergoing radioembolization. World J Gastroenterol. 2016;22:10406–10414.
    1. Lee JW, Lee MS, Chung IK, Son MW, Cho YS, Lee SM. Clinical implication of FDG uptake of bone marrow on PET/CT in gastric cancer patients with surgical resection. World J Gastroenterol. 2017;23:2385–2395.
    1. Kitajima K, Miyoshi Y, Sekine T, Takei H, Ito K, Suto A, Kaida H, Ishii K, Daisaki H, Yamakado K. Harmonized pretreatment quantitative volume-based FDG-PET/CT parameters for prognosis of stage I-III breast cancer: Multicenter study. Oncotarget. 2021;12:95–105.

Source: PubMed

Sponsors en medewerkers

Medische omstandigheden

Geneesmiddelinterventies

3
Abonneren