Abstract
Purpose
Oncology patients undergoing positron emission tomography/computed tomography (PET/CT) occasionally show discrete adrenal [18F]-fluorodeoxyglucose (FDG) uptake without an associated nodule on CT, leaving the clinician uncertain about the need to proceed with biopsy or surgical referral. This study aimed to identify the prevalence of this radiological finding and to evaluate the effectiveness of FDG uptake values in risk stratification for adrenal metastasis.
Methods
From 2014 to 2015, oncology patients who underwent FDG-PET/CT and demonstrated elevated FDG uptake in the adrenal gland without discrete nodularity on cross-sectional imaging were included in a retrospective cohort analysis. Clinical records and FDG-PET/CT scans were reviewed for clinicopathological data, follow-up data, SUVmax (highest SUV of either adrenal gland), and SUVratio (SUVmax/background liver uptake). A receiver operating characteristic analysis was conducted to evaluate the associations between SUV values and the progression to adrenal metastasis.
Results
Of 3040 oncology patients who underwent FDG-PET/CT scans, 92 (3.0%) showed elevated adrenal uptake without associated mass. From the final study cohort of 66 patients with comprehensive follow-up data, 5 patients (7.6%) developed evidence of adrenal metastasis. At SUVmax < 3.25 (AUC = 0.757) and SUVratio < 1.27 (AUC = 0.907), 34.8% and 60.6% of patients could be excluded with 100% negative predictive value, respectively.
Conclusions
Thresholds of SUVmax and SUVratio identified a significant proportion of patients who did not develop adrenal metastasis. In oncology patients who demonstrate increased adrenal FDG uptake without a discrete lesion on FDG-PET/CT, quantitative uptake values may be useful in selecting those not at risk of developing adrenal metastatic disease.
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References
Mao JJ, Dages KN, Suresh M, Bancos I. Presentation, disease progression and outcomes of adrenal gland metastases. Clin Endocrinol (Oxf). 2020. https://doi.org/10.1111/cen.14268.
Liu B, Mo C, Wang W, Ye J, Jiang C, Xie X et al (2020) Treatment outcomes of percutaneous radiofrequency ablation versus adrenalectomy for adrenal metastases: a retrospective comparative study. J Endocrinol Invest 43(9):1249–1257. https://doi.org/10.1007/s40618-020-01212-w
Lam KY, Lo CY (2002) Metastatic tumours of the adrenal glands: a 30-year experience in a teaching hospital. Clin Endocrinol (Oxf) 56(1):95–101. https://doi.org/10.1046/j.0300-0664.2001.01435.x
Ramsingh J, O’Dwyer P, Watson C (2019) Survival outcomes following adrenalectomy for isolated metastases to the adrenal gland. Eur J Surg Oncol 45(4):631–634. https://doi.org/10.1016/j.ejso.2019.01.006
Hatano K, Horii S, Nakai Y, Nakayama M, Kakimoto KI, Nishimura K (2020) The outcomes of adrenalectomy for solitary adrenal metastasis: a 17-year single-center experience. Asia Pac J Clin Oncol 16(2):e86–e90. https://doi.org/10.1111/ajco.13078
Solaini L, Ministrini S, Tomasoni M, Merigo G, Gaverini G, Bertoloni GP et al (2015) Adrenalectomy for metastasis: long-term results and predictors of survival. Endocrine 50(1):187–192. https://doi.org/10.1007/s12020-015-0596-8
Tomasini P, Garcia ME, Greillier L, Paladino C, Sebag F, Barlesi F (2017) Adrenal surgery for oligometastatic tumors improves survival in selected cases. J Visc Surg 154(2):87–91. https://doi.org/10.1016/j.jviscsurg.2016.08.007
Drake FT, Beninato T, Xiong MX, Shah NV, Kluijfhout WP, Feeney T et al (2019) Laparoscopic adrenalectomy for metastatic disease: retrospective cohort with long-term, comprehensive follow-up. Surgery 165(5):958–964. https://doi.org/10.1016/j.surg.2018.11.008
Strong VE, D’Angelica M, Tang L, Prete F, Gönen M, Coit D et al (2007) Laparoscopic adrenalectomy for isolated adrenal metastasis. Ann Surg Oncol 14(12):3392–3400. https://doi.org/10.1245/s10434-007-9520-7
Duh QY (2007) Laparoscopic adrenalectomy for isolated adrenal metastasis: the right thing to do and the right way to do it. Ann Surg Oncol 14(12):3288–3289. https://doi.org/10.1245/s10434-007-9569-3
Kumar R, Xiu Y, Yu JQ, Takalkar A, El-Haddad G, Potenta S et al (2004) 18F-FDG PET in evaluation of adrenal lesions in patients with lung cancer. J Nucl Med 45(12):2058–2062
Watanabe H, Kanematsu M, Goshima S, Kondo H, Kawada H, Noda Y et al (2013) Adrenal-to-liver SUV ratio is the best parameter for differentiation of adrenal metastases from adenomas using 18F-FDG PET/CT. Ann Nucl Med 27(7):648–653. https://doi.org/10.1007/s12149-013-0730-8
Sung YM, Lee KS, Kim BT, Choi JY, Chung MJ, Shim YM et al (2008) (18)F-FDG PET versus (18)F-FDG PET/CT for adrenal gland lesion characterization: a comparison of diagnostic efficacy in lung cancer patients. Korean J Radiol 9(1):19–28. https://doi.org/10.3348/kjr.2008.9.1.19
Kim SJ, Lee SW, Pak K, Kim IJ, Kim K (2018) Diagnostic accuracy of (18)F-FDG PET or PET/CT for the characterization of adrenal masses: a systematic review and meta-analysis. Br J Radiol 91(1086):20170520. https://doi.org/10.1259/bjr.20170520
Park HH, Park DS, Kweon DC, Lee SB, Oh KB, Lee JD et al (2011) Inter-comparison of 18F-FDG PET/CT standardized uptake values in Korea. Appl Radiat Isot 69(1):241–246. https://doi.org/10.1016/j.apradiso.2010.09.011
Kumar V, Nath K, Berman CG, Kim J, Tanvetyanon T, Chiappori AA et al (2013) Variance of SUVs for FDG-PET/CT is greater in clinical practice than under ideal study settings. Clin Nucl Med 38(3):175–182. https://doi.org/10.1097/RLU.0b013e318279ffdf
Lee JR, Madsen MT, Bushnel D, Menda Y (2000) A threshold method to improve standardized uptake value reproducibility. Nucl Med Commun 21(7):685–690. https://doi.org/10.1097/00006231-200007000-00013
Schomburg A, Bender H, Reichel C, Sommer T, Ruhlmann J, Kozak B et al (1996) Standardized uptake values of fluorine-18 fluorodeoxyglucose: the value of different normalization procedures. Eur J Nucl Med 23(5):571–574. https://doi.org/10.1007/bf00833394
Lodge MA (2017) Repeatability of SUV in Oncologic (18)F-FDG PET. J Nucl Med 58(4):523–532. https://doi.org/10.2967/jnumed.116.186353
Evans PD, Miller CM, Marin D, Stinnett SS, Wong TZ, Paulson EK et al (2013) FDG-PET/CT characterization of adrenal nodules: diagnostic accuracy and interreader agreement using quantitative and qualitative methods. Acad Radiol 20(8):923–929. https://doi.org/10.1016/j.acra.2013.02.010
Pitts A, Ih G, Wei M, Dhall D, Nissen NN, Waxman A et al (2013) Clinical utility of FDG-PET for diagnosis of adrenal mass: a large single-center experience. Hormones (Athens) 12(3):417–427. https://doi.org/10.1007/bf03401307
Hammarstedt L, Thilander-Klang A, Muth A, Wängberg B, Odén A, Hellström M (2013) Adrenal lesions: variability in attenuation over time, between scanners, and between observers. Acta Radiol 54(7):817–826. https://doi.org/10.1177/0284185113482688
Thomas AJ, Habra MA, Bhosale PR, Qayyum AA, Ahmed K, Vicens R et al (2018) Interobserver agreement in distinguishing large adrenal adenomas and adrenocortical carcinomas on computed tomography. Abdom Radiol (NY) 43(11):3101–3108. https://doi.org/10.1007/s00261-018-1603-3
Xu B, Gao J, Cui L, Wang H, Guan Z, Yao S et al (2012) Characterization of adrenal metastatic cancer using FDG PET/CT. Neoplasma 59(1):92–99. https://doi.org/10.4149/neo_2012_012
Metser U, Miller E, Lerman H, Even-Sapir E (2007) Benign nonphysiologic lesions with increased 18F-FDG uptake on PET/CT: characterization and incidence. AJR Am J Roentgenol 189(5):1203–1210. https://doi.org/10.2214/ajr.07.2083
Sharp SE, Gelfand MJ, Absalon MJ (2012) Altered FDG uptake patterns in pediatric lymphoblastic lymphoma patients receiving induction chemotherapy that includes very high dose corticosteroids. Pediatr Radiol 42(3):331–336. https://doi.org/10.1007/s00247-011-2228-7
Pinkerton E, Good P, Kindl K, Richard R, Fischer A, Hardy JR (2019) Quality use of medicines: oral corticosteroids in advanced cancer. Palliat Med 33(10):1325–1326. https://doi.org/10.1177/0269216319866647
Lim FMY, Bobrowski A, Agarwal A, Silva MF (2017) Use of corticosteroids for pain control in cancer patients with bone metastases: a comprehensive literature review. Curr Opin Support Palliat Care 11(2):78–87. https://doi.org/10.1097/spc.0000000000000263
Paulsen O, Klepstad P, Rosland JH, Aass N, Albert E, Fayers P et al (2014) Efficacy of methylprednisolone on pain, fatigue, and appetite loss in patients with advanced cancer using opioids: a randomized, placebo-controlled, double-blind trial. J Clin Oncol 32(29):3221–3228. https://doi.org/10.1200/jco.2013.54.3926
Paladino NC, Guérin C, Lowery A, Attard A, Essamet W, Slotema E et al (2018) Characterization of adrenocortical tumors by (18)F-FDG PET/CT: does steroid hormone hypersecretion status modify the uptake pattern? Surg Oncol 27(2):231–235. https://doi.org/10.1016/j.suronc.2018.04.003
Sastry P, Tocock A, Coonar AS (2014) Adrenalectomy for isolated metastasis from operable non-small-cell lung cancer. Interact Cardiovasc Thorac Surg 18(4):495–497. https://doi.org/10.1093/icvts/ivt526
Gao XL, Zhang KW, Tang MB, Zhang KJ, Fang LN, Liu W (2017) Pooled analysis for surgical treatment for isolated adrenal metastasis and non-small cell lung cancer. Interact Cardiovasc Thorac Surg 24(1):1–7. https://doi.org/10.1093/icvts/ivw321
Bradley CT, Strong VE (2014) Surgical management of adrenal metastases. J Surg Oncol 109(1):31–35. https://doi.org/10.1002/jso.23461
Castillo OA, Rodríguez-Carlin A, López-Vallejo J, Borgna V (2014) Complications associated with laparoscopic adrenalectomy: description and standardized assessment. Actas Urol Esp 38(7):445–450. https://doi.org/10.1016/j.acuro.2013.12.007
Strebel RT, Müntener M, Sulser T (2008) Intraoperative complications of laparoscopic adrenalectomy. World J Urol 26(6):555–560. https://doi.org/10.1007/s00345-008-0272-1
Heinrich DA, Adolf C, Holler F, Lechner B, Schneider H, Riester A et al (2019) Adrenal insufficiency after unilateral adrenalectomy in primary aldosteronism: long-term outcome and clinical impact. J Clin Endocrinol Metab 104(11):5658–5664. https://doi.org/10.1210/jc.2019-00996
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Study conception and design: Kluijfhout WP, Bongers PJ, Metser U, Veit-Haibach P, and Pasternak JD. Acquisition of data: Hsiao R, Kluijfhout WP, Bongers PJ, Verzijl R, Metser U, and Pasternak JD. Analysis and interpretation of data: Hsiao R, Chow A, Kluijfhout WP, Bongers PJ, Verzijl R, Metser U, Veit-Haibach P, and Pasternak JD. Drafting of manuscript: Hsiao R, Chow A, and Bongers PJ. Critical revision of manuscript: Hsiao R, Chow A, Bongers PJ, Verzijl R, Metser U, Veit-Haibach P, and Pasternak JD.
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This study was presented in part at the 39th Annual Meeting of the American Association of Endocrine Surgeons, Durham, NC.
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Hsiao, R., Chow, A., Kluijfhout, W.P. et al. The clinical consequences of functional adrenal uptake in the absence of cross-sectional mass on FDG-PET/CT in oncology patients. Langenbecks Arch Surg 407, 1677–1684 (2022). https://doi.org/10.1007/s00423-021-02379-3
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DOI: https://doi.org/10.1007/s00423-021-02379-3