EUS FNA of Altered Left Adrenal Gland Morphology Suggests Amending CT and PET-CT Attenuation Threshold Values That Predict Malignancy

Ferga C. Gleeson, Allison J. Clapp, Robert C. Murphy, Jonathan E. Clain, Prasad G. Iyer, Elizabeth Rajan, Mark D. Topazian, Kenneth K. Wang, Michael J. Levy

Department of Radiology, Mayo Clinic College of Medicine, Rochester, USA.
Division of Gastroenterology and Hepatology, Mayo Clinic College of Medicine, Rochester, USA.

DOI: 10.4236/jct.2012.36133                

Abstract

Introduction: In the setting of an extra-adrenal malignancy, it is a recognized clinical challenge to try and distinguish a benign adrenal mass from a metastatic deposit. Current non-invasive diagnostic tools for adrenal gland evaluation include CT, MRI, PET and PET-CT. Diagnostic interpretative error can occur as evaluations rarely have complete cytologic or histologic correlation for concordance purposes. Aims: To establish the performance characteristics of non-contrast CT attenuation values (Hounsfield units-HU) and the optimal PET-CT maximum standard uptake value (SUV_max) for predicting adrenal malignancy when correlated with adrenal gland endoscopic ultrasound fine needle aspiration (EUS FNA) cytology results. Methods: A prospectively maintained EUS database was reviewed to identify consecutive patients who underwent a left adrenal gland FNA. Non-contrast CT attenuation values and SUV_max scores were calculated. EUS FNA cytology results were used as the reference standard for determining the presence of benign versus malignant adrenal gland status. Results: Sixty-two patients (69 ± 11 years) underwent adrenal EUS FNA, 34 (54.8%) of whom had a clinically suspected or established extra-adrenal malignancy. Non-invasive imaging was suggestive of abnormal adrenal morphology or altered PET-CT FDG activity in 45 (72.6%) patients. Elevated attenuation values (≥10 HU) by non-enhanced CT had a sensitivity and specificity of 100% and 34.6%, respectively. The SUV_max for malignant altered morphology was significantly higher than that for benign lesions [(8.5 ± 3.1 vs 3.3 ± 0.7; (p = 0.0001)]. ROC curve analysis indicated that an optimum cutoff SUV_max of ≥4.1 (AUC 0.92) yielded the best power distinction for malignancy with a sensitivity and specificity of 89% and 100%. Conclusion: When evaluating altered adrenal morphology by non-invasive methods, the performance characteristics of elevated CT attenuation values are suboptimal. But by adopting a SUV_max cut-off value of ≥4.1 could potentially improve such characteristics to detect malignancy.

Keywords

Altered Adrenal Morphology; Endoscopic Ultrasound Fine Needle Aspiration; Unenhanced CT Attenuation Value; PET Standardized Uptake Value

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	C. Davenport, A. Liew, B. Doherty, et al., “The Prevalence of Adrenal Incidentaloma in Routine Clinical Practice,” Endocrine, Vol. 40, No. 1, 2011, pp. 80-83. doi:10.1007/s12020-011-9445-6
[2]	S. Bovio, A. Cataldi, G. Reimondo, et al., “Prevalence of Adrenal Incidentaloma in a Contemporary Computerized Tomography Series,” Journal of Endocrinological Investigation, Vol. 29, No. 4, 2006, pp. 298-302.
[3]	M. Terzolo, A. Stigliano, I. Chiodini, et al., “Italian Association of Clinical Endocrinologists. AME Position Statement on Adrenal Incidentaloma,” European Journal of Endocrinology, Vol. 164, No. 6, 2011, pp. 851-870. doi:10.1530/EJE-10-1147
[4]	G. W. Boland, M. A. Blake, P. F. Hahn and W. W. Mayo-Smith, “Incidental Adrenal Lesions: Principles, Techniques, and Algorithms for Imaging Characterization,” Radiology, Vol. 249, No. 3, 2008, pp. 756-775. doi:10.1148/radiol.2493070976
[5]	E. M. Remer, N. Obuchowski, J. D. Ellis, T. W. Rice, D. J. Adelstein and M. E. Baker, “Adrenal Mass Evaluation in Patients with Lung Carcinoma: A Cost-Effectiveness Analysis,” American Journal of Roentgenology, Vol. 174, 2000, pp. 1033-1039.
[6]	F. E. Nwariaku, J. Champine, L. T. Kim, S. Burkey, G. O’keefe and W. H. Snyder III, “Radiologic Characterization of Adrenal Masses: The Role of Computed Tomography—Derived Attenuation Values,” Surgery, Vol. 130, No. 6, 2001, pp. 1068-1071. doi:10.1067/msy.2001.119189
[7]	A. H. Hamrahian, A. G. Ioachimescu, E. M. Remer, et al., “Clinical Utility of Noncontrast Computed Tomography Attenuation Value (Hounsfield Units) to Differentiate Adrenal Adenomas/Hyperplasias from Nonadenomas: Cleveland Clinic Experience,” Journal of Clinical Endocrinology & Metabolism, Vol. 90, No. 2, 2005, pp. 871-877. doi:10.1210/jc.2004-1627
[8]	G. W. Boland, M. J. Lee, G. S. Gazelle, E. F. Halpern, M. M. McNicholas and P. R. Mueller, “Characterization of Adrenal Masses Using Unenhanced CT: An Analysis of the CT Literature,” American Journal of Roentgenology, Vol. 171, No. 1, 1998, pp. 201-204.
[9]	S. H. Park, M. J. Kim, J. H. Kim, J. S. Lim and K. W. Kim, “Differentiation of Adrenal Adenoma and Nonadenoma in Unenhanced CT: New Optimal Threshold Value and the Usefulness of Size Criteria for Differentiation,” Korean Journal of Radiology, Vol. 8, No. 4, 2007, pp. 328-335. doi:10.3348/kjr.2007.8.4.328
[10]	M. A. Eloubeidi, K. R. Black, A. Tamhane, I. A. Eltoum, A. Bryant and R. J. Cerfolio, “A Large Single-Center Experience of EUS-Guided FNA of the Left and Right Adrenal Glands: Diagnostic Utility and Impact on Patient Management,” Gastrointestinal Endoscopy, Vol. 71, No. 4, 2010, pp. 745-753. doi:10.1016/j.gie.2009.10.022
[11]	Y. M. Sung, K. S. Lee, B. T. Kim, et al., “(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 Journal of Radiology, Vol. 9, No. 1, 2008, pp. 19-28. doi:10.3348/kjr.2008.9.1.19
[12]	U. Metser, E. Miller, H. Lerman, G. Lievshitz, S. Avital and E. Even-Sapir, “18F-FDG PET/CT in the Evaluation of Adrenal Masses,” Journal of Nuclear Medicine, Vol. 47, No. 1, 2006, pp. 32-37.
[13]	M. Nakajo, M. Nakajo, Y. Kajiya, et al., “A Black Adrenal Adenoma Difficult to be Differentiated from a Malignant Adrenal Tumor by CT, MRI, Scintigraphy and FDG PET/CT Examinations,” Annals of Nuclear Medicine, Vol. 25, No. 10, 2011, pp. 812-817. doi:10.1007/s12149-011-0535-6
[14]	S. Chong, K. S. Lee, H. Y. Kim, et al., “Integrated PET-CT for the Characterization of Adrenal Gland Lesions in Cancer Patients: Diagnostic Efficacy and Interpretation Pitfalls,” Radiographics, Vol. 26, No. 6, 2006, pp. 1811-1824. doi:10.1148/rg.266065057
[15]	M. Okada, T. Shimono, Y. Komeya, et al., “Adrenal masses: The Value of Additional Fluorodeoxyglucose-Positron Emission Tomography/Computed Tomography (FDG-PET/CT) in Differentiating between Benign and Malignant Lesions,” Annals of Nuclear Medicine, Vol. 23, No. 4, 2009, pp. 349-354. doi:10.1007/s12149-009-0246-4
[16]	B. Xu, J. Gao, L. Cui, et al., “Characterization of Adrenal Metastatic Cancer Using FDG PET/CT,” Neoplasma, Vol. 59, No. 1, 2012, pp. 92-99. doi:10.4149/neo_2012_012
[17]	M. Perri, P. Erba, D. Volterrani, et al., “Adrenal Masses in Patients with Cancer: PET/CT Characterization with Combined CT Histogram and Standardized Uptake Value PET Analysis,” American Journal of Roentgenology, Vol. 197, No. 1, 2011, pp. 209-216. doi:10.2214/AJR.10.5342
[18]	N. C. Nguyen, A. Kaushik, M. K. Wolverson and M. M. Osman, “Is There a Common SUV Threshold in Oncological FDG PET/CT, at Least for Some Common Indications? A Retrospective Study,” Acta Oncologica, Vol. 50, No. 5, 2011, pp. 670-677. doi:10.3109/0284186X.2010.550933
[19]	M. J. Brady, J. Thomas, T. Z. Wong, K. M. Franklin, L. M. Ho and E. K. Paulson, “Adrenal Nodules at FDG PET/CT in Patients Known to Have or Suspected of Having Lung Cancer: A Proposal for an Efficient Diagnostic Algorithm,” Radiology, Vol. 250, No. 2, 2009, pp. 523-530. doi:10.1148/radiol.2502080219
[20]	S. Jana, T. Zhang, D. M. Milstein, C. R. Isasi and M. D. Blaufox, “FDG-PET and CT Characterization of Adrenal Lesions in Cancer Patients,” European Journal of Nuclear Medicine and Molecular Imaging, Vol. 33, No. 1, 2006, pp. 29-35. doi:10.1007/s00259-005-1915-8
[21]	C. Ansquer, S. Scigliano, E. Mirallié, et al., “18F-FDG PET/CT in the Characterization and Surgical Decision Concerning Adrenal Masses: A Prospective Multicentre Evaluation,” European Journal of Nuclear Medicine and Molecular Imaging, Vol. 37, No. 9, 2010, pp. 1669-1678. doi:10.1007/s00259-010-1471-8
[22]	I. Kayani, N. Avril, J. Bomanji, et al., “Sequential FDG-PET/CT as a Biomarker of Response to Sunitinib in Metastatic Clear Cell Renal Cancer,” Clinical Cancer Research, Vol. 17, No. 18, 2011, pp. 6021-6028. doi:10.1158/1078-0432.CCR-10-3309
[23]	M. Okada, T. Shimono, Y. Komeya, et al., “Adrenal Masses: The Value of Additional Fluorodeoxyglucose-Positron Emission Tomography/Computed Tomography (FDG-PET/CT) in Differentiating between Benign and Malignant Lesions,” Annals of Nuclear Medicine, Vol. 23, No. 4, 2009, pp. 349-354. doi:10.1007/s12149-009-0246-4
[24]	P. S. Duarte, H. Zhuang, P. Castellucci and A. Alavi, “The Receiver Operating Characteristic Curve for the Standard Uptake Value in a Group of Patients with Bone Marrow Metastasis,” Molecular Imaging and Biology, Vol. 4, No. 2, 2002, pp. 157-160. doi:10.1016/S1095-0397(01)00060-7
[25]	R. Hong, J. Halama, D. Bova, A. Sethi and B. Emami, “Correlation of PET Standard Uptake Value and CT Window-Level Thresholds for Target Delineation in CT-Based Radiation Treatment Planning,” International Journal of Radiation Oncology*Biology*Physics, Vol. 67, No. 3, 2007, pp. 720-726.
[26]	D. Wang, C. J. Schultz, P. A. Jursinic, et al., “Initial Experience of FDG-PET/CT Guided IMRT of Head-and-Neck Carcinoma,” International Journal of Radiation Oncology*Biology*Physics, Vol. 65, No. 1, 2006, pp. 143-151.
[27]	T. L. Ang, T. S. Chua, K. M. Fock, A. K. Tee, E. K. Teo and K. Mancer, “EUS-FNA of the Left Adrenal Gland Is Safe and Useful,” Annals Academy of Medicine Singapore, Vol. 36, No. 11, 2007, pp. 954-957.
[28]	U. Bodtger, P. Vilmann, P. Clementsen, E. Galvis, K. Bach and B. G. Skov, “Clinical Impact of Endoscopic Ultrasound-Fine Needle Aspiration of Left Adrenal Masses in Established or Suspected Lung Cancer,” Journal of Thoracic Oncology, Vol. 4, No. 12, 2009, pp. 1485-1489. doi:10.1097/JTO.0b013e3181b9e848
[29]	J. DeWitt, M. Alsatie, J. LeBlanc, L. McHenry and S. Sherman, “Endoscopic Ultrasound-Guided Fine-Needle Aspiration of Left Adrenal Gland Masses,” Endoscopy, Vol. 39, No. 1, 2007, pp. 65-71. doi:10.1055/s-2006-945042
[30]	M. A. Eloubeidi, S. Seewald, A. Tamhane, et al., “EUS-Guided FNA of the Left Adrenal Gland in Patients with Thoracic or GI Malignancies,” Gastrointestinal Endoscopy, Vol. 59, No. 6, 2004, pp. 627-633. doi:10.1016/S0016-5107(04)00296-2
[31]	M. A. Eloubeidi, L. P. Luz, D. R. Crowe, C. Snowden, D. E. Morgan and P. J. Arnoletti, “Bilateral Adrenal Gland Enlargement Secondary to Histoplasmosis Mimicking Adrenal Metastases: Diagnosis with EUS-Guided FNA,” Diagnostic Cytopathology, Vol. 38, No. 5, 2010, pp. 357-359.
[32]	N. C. Jhala, D. Jhala, M. A. Eloubeidi, et al., “Endoscopic Ultrasound-Guided Fine-Needle Aspiration Biopsy of the Adrenal Glands: Analysis of 24 Patients,” Cancer, Vol. 102, No. 5, 2004, pp. 308-314. doi:10.1002/cncr.20498
[33]	O. C. Schuurbiers, K. G. Tournoy, H. J. Schoppers, et al., “EUS-FNA for the Detection of Left Adrenal Metastasis in Patients with Lung Cancer,” Lung Cancer, Vol. 73, No. 3, 2011, pp. 310-315. doi:10.1016/j.lungcan.2010.12.019
[34]	H. Gerke, R. A. Robinson and P. Luo, “Diagnosis of Focal Metastasis to the Adrenal Gland by EUS-Guided Core Biopsy,” Gastrointestinal Endoscopy, Vol. 62, No. 3, 2005, pp. 469-471. doi:10.1016/S0016-5107(05)01578-6
[35]	E. B. Stelow, S. M. Debol, M. W. Stanley, S. Mallery, R. Lai and R. H. Bardales, “Sampling of the Adrenal Glands by Endoscopic Ultrasound-Guided Fine-Needle Aspiration,” Diagnostic Cytopathology, Vol. 33, No. 1, 2005, pp. 26-30. doi:10.1002/dc.20273
[36]	E. L. Artifon, A. M. Lucon, P. Sakai, et al., “EUS-Guided Alcohol Ablation of Left Adrenal Metastasis from Non-Small-Cell Lung Carcinoma,” Gastrointestinal Endoscopy, Vol. 66, No. 6, 2007, pp. 1201-1205. doi:10.1016/j.gie.2007.05.051
[37]	J. T. Lenert, C. C. Barnett Jr., A. P. Kudelka, et al., “Evaluation and Surgical Resection of Adrenal Masses in Patients with a History of Extra-Adrenal Malignancy,” Surgery, Vol. 130, No. 6, 2001, pp. 1060-1067. doi:10.1067/msy.2001.118369
[38]	L. Hammarstedt, A. Muth, H. A. Sigurjónsdóttir, E. Almqvist, B. W?ngberg and M. Hellstr?m, “On Behalf of the Adrenal Study Group of Western Sweden. Adrenal Lesions in Patients with Extra-Adrenal Malignancy— Benign or Malignant?” Acta Oncologica, Vol. 51, No. 2, 2012, pp. 215-221. doi:10.3109/0284186X.2011.608084
[39]	L. Yip, M. E. Tublin, J. A. Falcone, et al., “The Adrenal Mass: Correlation of Histopathology with Imaging,” Annals of Surgical Oncology, Vol. 17, No. 3, 2010, pp. 846-852. doi:10.1245/s10434-009-0829-2
[40]	J. M. Meier, A. Alavi, S. Iruvuri, et al., “Assessment of Age-Related Changes in Abdominal Organ Structure and Function with Computed Tomography and Positron Emission Tomography,” Seminars in Nuclear Medicine, Vol. 37, No. 3, 2007, pp. 154-172. doi:10.1053/j.semnuclmed.2007.02.001
[41]	D. Hellwig, T. P. Graeter, D. Ukena, et al., “18F-FDG PET for Mediastinal Staging of Lung Cancer: Which SUV Threshold Makes Sense?” Journal of Nuclear Medicine, Vol. 48, No. 11, 2007, pp. 1761-1766. doi:10.2967/jnumed.107.044362
[42]	A. S. Bryant, R. J. Cerfolio, K. M. Klemm and B. Ojha, “Maximum Standard Uptake Value of Mediastinal Lymph Nodes on Integrated FDG-PET-CT predicts Pathology in Patients with Non-Small Cell Lung Cancer,” Annals of Thoracic Surgery, Vol. 82, 2006, pp. 417-422. doi:10.1016/j.athoracsur.2005.12.047
[43]	K. J. Chang, R. A. Erickson and P. Nguyen, “Endoscopic Ultrasound (EUS) and EUS-Guided Fine-Needle Aspiration of the Left Adrenal Gland,” Gastrointestinal Endoscopy, Vol. 44, No. 5, 1996, pp. 568-572. doi:10.1016/S0016-5107(96)70010-X
[44]	J. M. Dumonceau, M. Polkowski, A. Larghi, et al., “Indications, Results, and Clinical Impact of Endoscopic Ultrasound (EUS)-Guided Sampling in Gastroenterology: European Society of Gastrointestinal Endoscopy (ESGE) Clinical Guideline,” Endoscopy, Vol. 43, No. 10, 2011, pp. 897-912. doi:10.1055/s-0030-1256754
[45]	C. J. Tyng, A. G. Bitencourt, E. B. Martins, P. N. Pinto and R. Chojniak, “Technical Note: CT-Guided Paravertebral Adrenal Biopsy Using Hydrodissection—A Safe and Technically Easy Approach,” British Journal of Radiology, 2011.