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Malignancies with Low Fluorodeoxyglucose Uptake at PET/CT: Pitfalls and Prognostic Importance Robert R. Flavell, MD, PhD, David M. Naeger, MD, Carina Mari Aparici, MD, Randall A. Hawkins, MD, PhD, Miguel H. Pampaloni, MD, PhD, Spencer C. Behr, MD Department of Radiology and Biomedical Imaging, University of California, San Francisco. Corresponding author: Spencer C. Behr, MD, [email protected], 415-3534889, 505 Parnassus Ave, San Francisco, CA, 94143. Presentation NME124, RSNA 2014, Awarded Certificate of Merit Dr. Flavell acknowledges an RSNA research fellow grant, a Society of Nuclear Medicine and Molecular ImagingEducational Research Foundation Mitzi & William Blahd, MD, pilot grant, and NIH 5T32EB001631-10 for funding. All authors have disclosed no relevant relationships. Presentation Background Fluorine 18 fluorodeoxyglucose (FDG) positron emission tomography (PET) is commonly used for staging and restaging of many solid tumors.

However, not all tumors take up high levels of FDG, which may cause challenges in scan interpretation. In some tumors, the level of metabolic activity has prognostic importance. In other tumors, uptake of FDG is inversely correlated with uptake of another radiotracer (the flip-flop phenomenon). Presentation Objectives Review common malignancies with low-level uptake of FDG on PET images. Understand the prognostic importance of highlevel FDG uptake in hepatocellular carcinoma (HCC), lymphoma, and prostate cancer. Review the flip-flop phenomenon, in which uptake of FDG is inversely correlated with uptake of another radiotracer. Learning Objectives

By the end of this presentation, the reader will be able to: 1. Identify which malignancies commonly have low-level FDG metabolic activity. 2. List tumors in which the presence of high-level FDG avidity carries poor prognostic importance. 3. Discuss the prognostic importance of the flipflop phenomenon in thyroid and neuroendocrine cancers. Malignancies with Low FDG Uptake FDG uptake correlates with glycolysis levels and is generally much higher than that of normal tissues in many common malignancies including lung, breast, and colon cancer. Other tumor subtypes may have low-level uptake, including renal cell cancer, mucinous tumors, and low-grade adenocarcinoma spectrum lesions in the lungs.

Malignancies with Low FDG Uptake: Possible Causes of Poor FDG Uptake Tumor causes: More indolent tumor type, with lower glycolysis resulting in lower FDG uptake Tumors with low cellularity (mucinous neoplasms) Small tumor size with partial volume effect; lesions smaller than 0.51.0 cm are not reliably detected Patient causes: Hyperglycemia Diabetes

Postprandial scan Malignancies with Low FDG Uptake: Technical Considerations Tumors with low FDG avidity could be obscured by poor patient preparation, including postprandial or hyperglycemic scans. Traditionally, lesions smaller than 1 cm are thought to be below the threshold for detection with PET. Recent improvements in technique, such as time-of-flight PET and optimized reconstruction technologies, enable detection of subcentimeter lesions.1 1

Postprandial FDG PET image. Koopman et al. J Nucl Med Tech, 2015 Malignancies with Low FDG Uptake: Mucinous Neoplasms FDG PET is insensitive for detection of mucinous adenocarcinoma (one study found 59% sensitivity1). Mean standardized uptake value (SUV) is 3.4 for ovarian mucinous neoplasms.2 Magnetic resonance (MR) imaging or contrast material enhanced computed tomography (CT) is preferred.

Berger et al. AJR, 2000 2 Tanizaki et al. Int J Gynecol Cancer, 2014 1 CT (left) and PET/CT (right) images in a 46-year-old woman with mucinous adenocarcinoma of the appendix (arrow) (maximum SUV [SUVmax], 3.0). Malignancies with Low FDG Uptake: Mucinous Neoplasms PET/CT images in a 31-year-old woman with widespread peritoneal mucinous adenocarcinoma (arrow), with low FDG avidity in both lesions (SUV max of 1.7 for pelvic and perihepatic lesions). Malignancies with Low FDG Uptake: Renal Cell Cancer, Primary Tumor Detection hampered by clearance of FDG in the renal

collecting system. One study found 60% sensitivity and 100% specificity of FDG uptake for renal cell cancer.1 Mean SUV for primary renal cell carcinoma (RCC) is 2.6.2 CT (left) and PET/CT (right) images in a 51-year-old woman with RCC (arrow) without FDG uptake above background (SUVmax, 4.9). 1 Kang et al. J Urol, 2004 2 Lee et al. Nucl Med Mol Imag, 2014 Malignancies with Low FDG Uptake: Renal Cell Cancer, Primary Tumor CT (top left) and PET/CT (bottom left, right) images in a 95-year-old man with RCC (arrow) without detectable FDG uptake above background (SUVmax, 2.9).

Malignancies with Low FDG Uptake: Renal Cell Cancer Metastases Although FDG PET is more sensitive for RCC metastasis than for primary tumor, some cases are still missed. One recent meta-analysis found a pooled 91% sensitivity and 88% specificity for PET/CT for detection of metastatic RCC.1 PET/CT images in a 77-year-old woman with low FDG avidity primary RCC (SUV max, 3.0) with hypermetabolic right ilium metastasis (SUVmax, 9.8). 1 Wang et al. Cancer Imaging, 2012 Malignancies with Low FDG Uptake: Renal Cell Cancer Metastases PET/CT image (left) in a 77-year-old woman with a history of metastatic RCC demonstrates low background levels of hypermetabolism in the pancreatic tail (SUVmax, 3.6). Subsequent T1-weighted gadolinium-enhanced fat-saturated abdominal

MR image (right) demonstrates an enhancing mass in the pancreatic tail (arrow), consistent with metastasis. Malignancies with Low FDG Uptake: Low-Grade Adenocarcinoma of the Lung Low-grade adenocarcinoma spectrum lesions (formerly called bronchoalveolar carcinoma or BAC) often demonstrate low or no FDG uptake. Previous studies have documented low sensitivity of FDG PET for detecting these lesions, ranging from 43% 60%.1,2 Average SUV is 1.2.3 Higashi et al. J Nucl Med, 1998

2 Heyneman and Patz. Lung Cancer, 2002, 261-266. 3 Aquino et al. Int J Mol Med, 2007 1 Low-grade adenocarcinoma spectrum lesions (arrow) typically present as ground-glass attenuation nodules, as on this CT image in a 75-year-old man. Malignancies with Low FDG Uptake: Low-Grade Adenocarcinoma of the Lung CT (left) and PET/CT (right) images in a 77-year-old man with a history of melanoma. A left upper-lobe ground-glassattenuation nodule (arrow) had slowly increased in size over multiple prior scans and is consistent with adenocarcinoma in situ (left). There was no definite FDG uptake above background (SUVmax, 0.8) (right).

Malignancies with Low FDG Uptake Low-grade pulmonary adenocarcinoma spectrum lesions Low-grade lymphomas, including mucosa-associated lymphoid tissue, chronic lymphocytic leukemia or small lymphocytic lymphoma, marginal zone lymphoma, peripheral T-cell lymphoma Renal cell cancer Prostate cancer Pancreatic cancer Mucinous neoplasms HCC Some soft-tissue sarcomas Thyroid cancer Neuroendocrine tumors Uterine malignancies Lobular breast cancer Teratoma Low-grade glioma

Prognostic Importance of FDG Uptake In many types of cancer, there is strong evidence that higher FDG uptake correlates with poor prognosis. Therefore, it is important to report the level of FDG uptake in cases of HCC, lymphoma, and prostate cancer. Prognostic Importance of FDG Uptake: HCC Less than liver = Well differentiated (SUVmax, 1.8) Equal to liver = Well to moderately differentiated

(SUVmax, 2.5) Greater than liver = Poorly differentiated (SUVmax, 4.8) Average liver SUV is 2.02.5 and can change on the basis of age, weight, and blood glucose level. 1 1 Groheux et al. Clin Nuc Med, 2013, 422-425 Prognostic Importance of FDG Uptake: HCC FDG PET uptake predicted poor response to radiation1 and transarterial chemoembolization.2 High FDG uptake predicts higher stage as well as presence of metastatic disease.3 High FDG uptake predicts recurrence after

liver transplantation.4 Huang et al. J Nucl Med, 2013, 1710-1716 2 Song et al. Eur J Nucl Med Mol Imag, 2013, 865-873 3 Pant et al. Nucl Med Comm, 2013, 749-757 4 Lee et al. Transpl Int, 2013, 50-60 1 Prognostic Importance of FDG Uptake: HCC 83% sensitivity for HCC metastatic disease,1 lesions often missed at CT CT (top) and PET/CT (bottom) images in a 58year-old man with supraclavicular node HCC metastasis (arrow) (SUVmax, 3.2).

CT (top) and PET/CT (bottom) images in a 67-year-old woman with femoral HCC metastasis (arrow) (SUVmax, 4.3). 1 Sugiyama et al. J Gastroenterol, 2004;39:961-968 Prognostic Importance of FDG Uptake: Lymphoma Low-grade lymphomas typically demonstrate low FDG uptake.1 This is common in chronic lymphocytic leukemia, marginal zone lymphoma, and mucosa-associated lymphoid tissue.

PET/CT image in a 67-year-old woman with a history of chronic lymphocytic leukemia, with low FDG avidity pelvic and inguinal lymphadenopathy (SUVmax, 1.8). 1 Weiler-Sagie et al. J Nucl Med, 2010 Prognostic Importance of FDG Uptake: Lymphoma The presence of high FDG uptake in a patient with known low-grade lymphoma is suspicious for high-grade transformation (Richter transformation).

An SUVmax of 5 is accepted as a cutoff for concern for transformation.1 In general, high FDG uptake in lymphoma correlates with higher grade.2,3 Falchi et al. Blood, 2014 2 Noy et al. Ann Oncology, 2009, 508-512 3 Rodriguez et al. J Nucl Med, 1995, 1790-1796 1 PET/CT image in a 65-year-old woman with a history of chronic lymphocytic leukemia. Marked FDG uptake in the right inguinal lymph nodes (SUVmax, 10.1) is concerning for high-grade transformation. Excisional biopsy results

confirmed transformation to diffuse large B-cell lymphoma. Prognostic Importance of FDG Uptake: Lymphoma The Deauville criteria have been proposed as a method of following response to treatment, on the basis of uptake at FDG PET: 1 Deauville 1: No uptake Deauville 2: Uptake less than or equal to mediastinum Deauville 3: Uptake greater than mediastinum, less than or equal to liver Deauville 4: Uptake greater than liver Deauville 5: Uptake markedly higher than liver and/or new lesions Other authors have advocated using a quantitative approach of SUV measurement for predicting response, with a greater than 71% reduction in SUV being strongly correlated with treatment response. 2 Barrington et al. J Clin Oncology, 2014, 3048-3058 2 Rossi et al. J Nucl Med, 2014, 569-573

1 Prognostic Importance of FDG Uptake: Prostate Cancer Most cases of low-grade prostate cancer have little FDG uptake. 1 Mean SUV in lymph node metastases is 1.1 and 1.0 for local recurrences. 2 High-grade castrate-resistant prostate cancer can demonstrate increased FDG uptake, and higher SUV is associated with decreased survival. 3 Neuroendocrine-type prostate cancer has higher FDG avidity (average SUV, 4.5). 4 PET/CT images in a 66-year-old man with metastatic small cell prostate cancer with liver and mediastinal metastases (SUVmax, 11.1 and 13.2). Jadvar et al. J Nucl Med, 2013, 1195-1201 2 Fricke et al. Eur J Nucl Med Mol Imag, 2003 3 Jadvar, Eur J Nucl Med Mol Imag, 2013, S5-S10 4

Spratt et al. Prostate, 2014, 1153-1159 1 Prognostic Importance of FDG Uptake: Prostate Cancer Images in a 69-year-old man with a history of metastatic prostate cancer. FDG PET/CT images (left) demonstrate a sclerotic lesion without detectable hypermetabolism above background (SUVmax, 2.0). Corresponding image from an anterior projection bone scan and single-photon emission computed tomographic (SPECT) image (right) demonstrate an osteoblastic L5 metastasis (arrow). The Flip-Flop Phenomenon FDG uptake Receptor targeting

tracer uptake Poorly differentiated Aggressive phenotype Resistant to receptor-targeted therapy Well differentiated Indolent phenotype Express cell surface receptors Amenable to receptor-targeted therapy The flip-flop phenomenon is a rough correlation where FDG uptake is inversely correlated with uptake of another tracer, such as iodine 131 (131I) or indium 111 (111In) pentetreotide.1 Differentiated tumors resemble the normal underlying tissue, express cell surface receptors such as sodium-iodine symporter and somatostatin receptors, and take up 131 I or 111In pentetreotide, but dedifferentiated tumors lose this feature and become

1 more glucose dependent and hypermetabolic. Feine et al. J Nucl Med, 1995, 14681472 Flip-Flop Phenomenon: Neuroendocrine Tumors In pentetreotide uptake results from somatostatin receptor expression and can be inversely correlated with FDG uptake. Average SUV of well-differentiated lesions is 2.9.1 Tumors that take up pentetreotide are amenable to therapy with octreotide. 111 1

Kayani et al. Cancer, 2008 Flip-Flop Phenomenon: Neuroendocrine Tumors Neuroendocrine tumors (as well as other neoplasms) have considerable intratumoral heterogeneity, which can provide important prognostic information.1 One study found an average of 54 months of progression-free survival in patients with positive pentetreotide uptake versus 3 months for those without.2 The same study found 3 months of progression-free survival in those with FDG uptake versus 72 months in those without. Yang et al. Am J Surg Path, 2011, 853-860 2 Bahri et al. J Nucl Med, 2014, 1786-1790

1 Flip-Flop Phenomenon: Neuroendocrine Tumors FDG PET/CT InInPentetreotide Pentetreotid 111 111 e Images in a 56-year-old woman with a history of renal cell cancer with an incidentally discovered carcinoid tumor. The presence of pentetreotide uptake and low FDG uptake (SUVmax, 1.2) is a favorable prognostic indicator.

Flip-Flop Phenomenon: Neuroendocrine Tumors In-Pentetreotide 111 18 F-FDG PET image (right) and frontal projection image from 111In pentetreotide scan (left) in a 28-year-old woman with a diffusely metastatic neuroendocrine tumor. Some metastases demonstrate high pentetreotide and low FDG uptake (liver mass, yellow arrow, SUVmax of 2.5), others demonstrate high uptake of both tracers (liver mass, blue arrow, SUVmax of 4.8), while others demonstrate low pentetreotide uptake and high FDG uptake (retroperitoneal lymph node, red arrow, SUVmax of 4.9). The presence of FDG avid, pentetreotide negative Flip-Flop Phenomenon:

Thyroid Cancer FDG uptake may be inversely correlated with sodiumiodide symporter expression, and therefore with iodine uptake, in patients with thyroid cancer.1,2 High FDG and low iodine uptake is associated with dedifferentiated tumor and poor prognosis.3 Patients with high iodine uptake may undergo treatment with 131I, whereas those without will not typically benefit from treatment. Patients with distant metastases with negative iodine scan findings and positive FDG uptake may be treated with tyrosine kinase inhibitors.4 Feine et al. J Nucl Med, 1996, 14681472 1 Feine et al. Nuklearmedizin, 1995, 127-134 3 Hong et al. Nuklearmedizin, 2013, 121-129 4

Busaidy and Cabanillas, J Thy Res, 2012 2 Flip-Flop Phenomenon: Thyroid CancerWhen to Use FDG versus Iodine Imaging I or 131I scan is preferred for differentiated thyroid cancers and can assist in treatment planning. PET/CT is useful in patients with papillary thyroid cancer with rising thyroglobulin level and negative iodine scan findings for detection of potentially curable disease.1 FDG PET/CT is also useful in all patients with selected histologic subtypes of thyroid cancer, including Hrthle cell, tall cell, and anaplastic thyroid cancers. 2 123

Schluter et al. J Nucl Med, 2001 2 Abraham and Schoder, Semin Nucl Med, 2011 1 Flip-Flop Phenomenon: Thyroid Cancer Images in a 45-year-old man with a history of metastatic papillary thyroid cancer. FDG PET/ CT image (left) demonstrates a hypermetabolic pulmonary metastasis (arrow) (SUVmax, 28.6). No uptake was seen on

post131I treatment scan (right). Note physiologic salivary gland uptake. These findings suggest tumor dedifferentiation and are associated with poor treatment response and poor prognosis. Flip-Flop Phenomenon: Thyroid Cancer Images in a 66-year-old man with a history of papillary thyroid cancer. FDG PET/CT image (left) demonstrates a mass inferior to the right hepatic lobe with low-level hypermetabolism (SUVmax, 1.5). SPECT/CT image (right) obtained after 131I treatment (150 mCi [5550 MBq]) demonstrates tracer uptake in the mass (arrow). These findings are associated with well-differentiated tumors and good treatment response.

Conclusions Many common neoplasms have low FDG uptake, including renal cell cancer, mucinous neoplasms, and low-grade lung adenocarcinoma spectrum lesions. In many tumors, FDG uptake is associated with dedifferentiation and poor prognosis, including HCC, prostate cancer, and low-grade lymphoma. In neuroendocrine tumors and thyroid cancer, FDG uptake is associated with poor prognosis and can be inversely correlated with uptake of 131I and 111In pentetreotide, respectively. References

Abraham T, Schoder H. Thyroid cancer: indications and opportunities for positron emission tomography/computed tomography imaging. Semin Nucl Med 2011;41:121-138. Aquino SL, Halpern EF, Kuester, LB, Fischman AJ. FDG-PET and CT features of nonsmall cell lung cancer based on tumor type. Int J Molecular Med 2007;19:495-499. Bahri H, Laurence L, Edeline J, et al. High prognostic value of 18F-FDG PET for metastatic gastroenteropancreatic neuroendocrine tumors: a long-term evaluation. J Nucl Med 2014;55:1786-1790. Barrington SF, Mikhaeel NG, Kostakoglu L, et al. Role of imaging in the staging and response assessment of lymphoma: consensus of the International Conference on Malignant Lymphomas Imaging Working Group. J Clin Oncol 2014;32:3048-3058. Berger KL, Nicholson SA, Dehdashti F, Siegel BA. FDG PET evaluation of mucinous neoplasms: correlation of FDG uptake with histopathologic features. AJR Am J Roentgenol 2000;174:1005-1008. Busaidy NL, Cabanillas ME. Differentiated thyroid cancer: management of patients with radioiodine

nonresponsive disease. J Thyroid Res 2012;618985. Falchi L, Keating MJ, Marom EM, et al. Correlation between FDG/PET, histology, characteristics, and survival in 332 patients with chronic lymphoid leukemia. Blood 2014;123:2783-2790. Feine U, Lietzenmayer R, Hanke JP, Held J, Wohrle H, Muller-Schauenburg W. Fluorine-18-FDG and iodine131-iodide uptake in thyroid cancer. J Nucl Med 1996;37:1468-1472. Feine U, Lietzenmayer R, Hanke JP, Wohrle H, Mullerschauenburg W. (18)FDG whole-body PET in differentiated thyroid carcinoma: flipflop in uptake patterns of (18)FDG and I-131. Nuklearmedizin Nuclear Medicine 1995;34:127-134. References

Fricke E, Machtens S, Hofmann M, et al. Positron emission tomography with 11C-acetate and 18F-FDG in prostate cancer patients. Eur J Nucl Med Mol Imaging 2003;30:607-611. Groheux D, Delord M, Rubello D, Colletti PM, Nguyen ML, Hindie E. Variation of liver SUV on (18)FDG-PET/ CT studies in women with breast cancer. Clin Nucl Med 2013;38:422-425. Heyneman LE, Patz EF. PET imaging in patients with bronchioloalveolar cell carcinoma. Lung Cancer 2002;38:261-266. Higashi K, Ueda Y, Seki H, et al. Fluorine-18-FDG PET imaging is negative in bronchioloalveolar lung carcinoma. J Nucl Med 1998;39:1016-1020. Hong CM, Ahn BC, Jeong SY, Lee SW, Lee J. Distant metastatic lesions in patients with differentiated thyroid carcinoma: clinical implications of radioiodine and FDG uptake. Nuklearmedizin Nucl Med 2013;52:121129. Huang, WY, Kao CH, Huang WS, et al. 18F-FDG PET and combined 18F-FDG-contrast CT parameters as predictors of tumor control for hepatocellular carcinoma after stereotactic ablative radiotherapy. J Nucl Med 2013;54:1710-1716. Jadvar H. FDG PET in prostate cancer. PET Clin 2009;4:155-161. Jadvar H, Desai B, Ji L, et al. Baseline 18F-FDG PET/CT parameters as imaging biomarkers of overall survival

in castrate-resistant metastatic prostate cancer. J Nucl Med 2013;54:1195-1201. Kang DE, White RL Jr, Zuger JH, Sasser HC, Teigland CM. Clinical use of fluorodeoxyglucose F 18 positron emission tomography for detection of renal cell carcinoma. J Urol 2004;171:1806-1809. References Kayani I, Bomanji JB, Groves A, et al. Functional imaging of neuroendocrine tumors with combined PET/CT using 68Ga-DOTATATE (DOTA-DPhe1,Tyr3-octreotate) and 18F-FDG. Cancer 2008;112:2447-2455. Koopman D, van Dalen JA, Lagerweij MC, et al. Improving the detection of small lesions using a state-ofthe-art time-of-flight PET/CT system and small-voxel reconstructions. J Nucl Med Technol 2015;43:21-27.

Lee H, Hwang KH, Kim SG, Koh G, Kim JH. Can initial (18)F-FDG PET-CT imaging give information on metastasis in patients with primary renal cell carcinoma? Nucl Med Mol Imaging 2014;48:144-152. Lee SD, Kim SH, Kim YK, et al. (18)F-FDG-PET/CT predicts early tumor recurrence in living donor liver transplantation for hepatocellular carcinoma. Transpl Int 2013;26:50-60. Noy A, Schoder H, Gonen M, et al. The majority of transformed lymphomas have high standardized uptake values (SUVs) on positron emission tomography (PET) scanning similar to diffuse large B-cell lymphoma (DLBCL). Ann Oncol 2009;20:508-512. Pant V, Sen IB, Soin AS. Role of (1)(8)F-FDG PET CT as an independent prognostic indicator in patients with hepatocellular carcinoma. Nucl Med Commun 2013;34:749-757. Rodriguez M, Rehn S, Ahlstrom H, Sundstrom C, Glimelius B. Predicting malignancy grade with PET in nonHodgkin's lymphoma. J Nucl Med 1995;36:1790-1796. Rossi C, Kanoun S, Berriolo-Riedinger A, et al. Interim 18F-FDG PET SUV max reduction is superior to visual analysis in predicting outcome early in Hodgkin lymphoma patients. J Nucl Med 2014;55:569-573. References

Schluter B, Bohuslavizki KH, Beyer W, Plotkin M, Buchert R, Clausen M. Impact of FDG PET on patients with differentiated thyroid cancer who present with elevated thyroglobulin and negative 131I scan. J Nucl Med 2001;42:71-76. Song MJ, Bae SH, Lee SW, et al. 18F-fluorodeoxyglucose PET/CT predicts tumour progression after transarterial chemoembolization in hepatocellular carcinoma. Eur J Nucl Med Mol Imaging 2013;40:865873. Spratt DE, Gavane S, Tarlinton L, et al. Utility of FDG-PET in clinical neuroendocrine prostate cancer. Prostate 2014;74:1153-1159. Sugiyama M, Sakahara H, Torizuka T, et al. 18F-FDG PET in the detection of extrahepatic metastases from hepatocellular carcinoma. J Gastroenterol 2004;39:961-968. Tanizaki Y, Kobayashi A, Shiro M, et al. Diagnostic value of preoperative SUVmax on FDG-PET/CT for the detection of ovarian cancer. Int J Gynecol Cancer 2014;24:454-460.

Wang HY, Ding HJ, Chen JH, et al. Meta-analysis of the diagnostic performance of [18F]FDG-PET and PET/CT in renal cell carcinoma. Cancer Imaging 2012;12:464-474. Weiler-Sagie M, Bushelev O, Epelbaum R, et al. (18)F-FDG avidity in lymphoma readdressed: a study of 766 patients. J Nucl Med 2010;51:25-30. Yang Z, Tang LH, Klimstra DS. Effect of tumor heterogeneity on the assessment of Ki67 labeling index in well-differentiated neuroendocrine tumors metastatic to the liver: implications for prognostic stratification. Am J Surg Pathol 2011;35:853-860.

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