SDHD GENE MUTATIONS: LOOKING BEYOND HEAD AND NECK TUMORS
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1 Case Report SDHD GENE MUTTIONS: LOOKING EYOND HED ND NECK TUMORS Sushma Kadiyala, MD 1,2* ; Yasmin Khan, MD 1,2* ; Valeria de Miguel, MD 3* ; Megan N. Frone, MS, CGC 4 ; Fiemu Nwariaku, MD 5 ; Jennifer Rabaglia, MD 5 ; Stacey Woodruff, MD 6 ; Elizabeth E. King, MD 7 ; Sumitha S. Hathiramani, MD 8 ; Karel Pacak, MD, PhD 9 ; Hans K. Ghayee, DO 1,2 STRCT Objective: Succinate dehydrogenase complex, subunit D (SDHD) gene mutations are most commonly associated with head and neck paragangliomas. We describe a pair of cases with early-onset, bilateral pheochromocytoma (PCC) and paraganglioma (PGL) syndrome associated with SDHD mutation. Methods: We describe 2 cases of hereditary, earlyonset, bilateral PCC/PGL syndrome associated with SDHD mutation. Results: oth cases presented under the age of 30 with bilateral PCC and PGL with SDHD mutations. Case 1 is a female who was initially diagnosed with hypertension and later work-up revealed elevated norepinephrine levels. Positron emission tomography coupled with computed *These authors contributed equally. Submitted for publication June 21, 2017 ccepted for publication ugust 23, 2017 From the 1 Departiment of Internal Medicine, Division of Endocrinology and Metabolism, University of Florida, Gainesville, Florida, 2 Malcolm Randall V Medical Center, Gainesville, Florida, 3 Endocrinology Unit, Hospital Italiano de uenos ires, uenos ires, rgentina, 4 Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, ethesda, Maryland, 5 Department of Surgery, University of Texas Southwestern Medical Center, Dallas, Texas, 6 Department of Surgery, John. urns School of Medicine, University of Hawaii, Honolulu, Hawaii, 7 Endocrine ssociates of Dallas, Dallas, Texas, 8 Departiment of Internal Medicine, Division of Endocrinology and Metabolism, V North Texas Healthcare System, Dallas, Texas, and 9 Section on Medical Neuroendocrinology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, ethesda, Maryland. ddress correspondence to Dr. Hans K. Ghayee, University of Florida and Malcom Randall V Medical Center, Division of Endocrinology, Diabetes and Metabolism, 1600 Southwest rcher Road, Gainesville, FL hans.ghayee@medicine.ufl.edu. DOI: /EP CR To purchase reprints of this article, please visit: tomography showed avid uptake of fluorodeoxyglucose by the right adrenal gland, the organ of Zuckerkandl, and the left carotid bifurcation. Surgical resection was performed and resulted in normalization of her catecholamines. Case 2 is a male who similarly presented with hypertension and elevated norepinephrine levels. Imaging revealed head, neck, and abdominal PGL. He underwent staged adrenalectomies and abdominal PGL resection. Gene sequencing and deletion/duplication analysis revealed that case 1 had an exon 2 deletion in her SDHD gene and case 2 had a frameshift mutation resulting in a stop codon in exon 3 in his SDHD gene. Conclusion: While SDHD mutations are primarily thought to result in silent head and neck tumors, our cases indicate that they should also be considered in the evaluation of functional, bilateral adrenal PCC in young patients. (CE Clinical Case Rep. 2018;4:e186-e190) bbreviations: FDG = fluorodeoxyglucose; PCC = pheochromocytoma; PGL = paraganglioma; SDHD = succinate dehydrogenase complex, subunit D gene; VHL = von Hippel-Lindau INTRODUCTION Pheochromocytomas (PCCs) are catecholamineproducing tumors arising from the chromaffin cells in the adrenal medulla. Paragangliomas (PGLs), on the other hand, are derived from extra-adrenal sympathetic and parasympathetic chain paraganglia, including the head and neck (1). Unlike PCCs, head and neck PGLs typically do not produce catecholamines. There are approximately 20 genes known to be associated with PCC/PGL (2). The most well-known susceptibility syndromes where these tumors may be found include e186 CE CLINICL CSE REPORTS Vol 4 No. 3 May/June 2018
2 SDHD Mutation and Pheochromocytoma, CE Clinical Case Rep. 2018;4(No. 3) e187 von Hippel-Lindau (VHL) disease, neurofibromatosis type 1, and multiple endocrine neoplasia type 2. Rare mutations in the MYC-associated factor X (3) and transmembrane protein 127 (4) genes have also been described in this pathogenesis. More commonly, hereditary PCC/PGL syndromes have also been associated with mutations in one of the succinate dehydrogenase complex subunits (5-7). With the exception of the succinate dehydrogenase subunit gene mutation, most other succinate dehydrogenase gene family mutations, such as assembly factor 2 (F2) and subunits, C, and D (SDHD), are considered to result primarily in non-secretory PGLs found in the head and neck. We present two unique cases of SDHD mutation associated with catecholamine-producing bilateral adrenal PCC and head/neck PGL, reaffirming that SDHD mutation may no longer be considered a non-secretory head and neck tumor CSE REPORT Case 1 24-year-old female was referred for evaluation of a right-adrenal incidentaloma. This was incidentally found on a computed tomography scan for evaluation of back pain in the emergency room after a motor vehicle accident. The scan revealed a right-adrenal tumor measuring 3.0 cm 2.6 cm. Her blood pressure in the emergency room was 194/113 mm Hg and her pulse was 79 beats per minute. Review of systems was significant for hypertension, vertigo, heart palpitations, and headaches that had developed several weeks prior to admission. Results of the biochemical evaluation demonstrated plasma metanephrines were <0.20 nmol/l (normal range is <0.50 nmol/l), plasma normetanephrine was 12 nmol/l (normal range is <0.9 nmol/l), 24-hour urine norepinephrine excretion was 618 μg (normal range is 15 to 80 μg per 24 hours), 24-hour urine epinephrine excretion was <1.5 μg (normal range is 0 to 20 μg per 24 hours), and 24-hour urine dopamine excretion was 336 μg (normal range is 65 to 400 μg per 24 hours). Positron emission tomography scan revealed a fluorodeoxyglucose (FDG)-avid, right-adrenal mass compatible with PCC, 2 foci of FDG activity within the organ of Zuckerkandl, and a focus of FDG activity at the leftcarotid bifurcation (Fig. 1 and 2). fter adequate medical preparation with alpha-adrenergic blockade, she underwent successful right adrenalectomy and resection of the PGL located in the region of the organ of Zuckerkandl. Her blood pressure and plasma normetanephrine normalized postoperatively. Resection of the left-carotid body PGL was also performed several months later. Interestingly, the patient revealed prior history of a left-adrenal PCC at age 11 with an elevated blood pressure of 200/100 mm Hg diagnosed during a sports physical. She underwent left adrenalectomy at that time with subsequent normalization in blood pressure until the upcoming weeks prior to presentation. No genetic testing was performed at that time. The patient was not aware of any significant family history of PGL or PCC. Given the patient s history of bilateral, early-onset PCC with elevated normetanephrine, genetic testing was performed. The sequencing and deletion/duplication analysis of the full VHL gene was normal. Full gene sequencing and multiplex ligationdependent probe amplification of the SDH, SDHC, and SDHD genes were then performed. This testing revealed a deletion of exon 2 in SDHD, confirming a diagnosis of hereditary PCC/PGL syndrome in the patient. Case 2 29-year-old man, initially diagnosed with sustained hypertension 5 years prior, was found to have bilateral Fig. 1. Positron emission tomography scan of case 1 demonstrating a fluorodeoxyglucose-avid right-adrenal mass consistent with pheochromocytoma in both coronal () and transverse () views.
3 e188 SDHD Mutation and Pheochromocytoma, CE Clinical Case Rep. 2018;4(No. 3) C Fig. 2. Positron emission tomography scan of case 1 showing fluorodeoxyglucose activity within the transverse view of the organ of Zuckerlandl (), transverse view of the left carotid body (), and coronal view of the left carotid body (C), consistent with paraganglioma. PCC during a hospitalization for hypertensive urgency. iochemically, he had a noradrenergic profile. Specifically, 24-hour urine results included norepinephrine excretion of μg (reference range is 0 to 100 μg per 24 hours) and epinephrine excretion of 23.7 μg (reference range is 0 to 8.5 μg per 24 hours). The sizes of his PCC tumors were 5.0 cm on the right and 2.4 cm on the left side. Computed and positron emission tomography scans also showed bilateral carotid body PGLs and increased FDG activity of the adrenal and retrocaval PGL (Fig. 3). fter the evaluation was complete, a right adrenalectomy was performed. Several years later, he underwent a left adrenalectomy along with retrocaval PGL resection and right nephrectomy. His sister had a neck PGL, however no other family history of PCC/ PGL was found. Considering this family history of PGL syndrome, genetic testing was performed and revealed a frameshift mutation resulting in a stop codon in exon 3 in the SDHD gene. DISCUSSION We describe 2 patients with early-onset, bilateral, adrenal PCC and PGL with molecular characterization consistent with SDHD mutations. t least one third of patients with PCC/PGL are known to have an inherited germline mutation (8). The most common of these are associated with germline mutations in the succinate dehydrogenase family of genes, including its 4 subunits. This membrane complex converts succinate to fumarate in the Krebs cycle. n inactivating mutation in the succinate dehydrogenase gene family causes decreased or complete absence of succinate dehydrogenase enzyme activity, resulting in an accumulation of succinate and disruption of electron transport with generation of reactive oxygen species resulting in accelerated cell proliferation and tumor development (9). The accumulation of succinate and other oncometabolites in tumors caused by succinate dehydrogenase gene family mutations have also been illustrated to have a key role in regulating the stability of hypoxia-inducible factor α. When hypoxia-inducible factor α is unstable, a cascade of downstream events lead to tumorigenesis (9). One such condition is PGL syndrome type 1, resulting from inactivating mutations in the SDHD gene (7). Clinically, the principles associated with loss of succinate dehydrogenase activity has helped to advance imaging modalities such as positron emission and computed tomography scans for the detection of succinate dehydrogenase-associated tumors (10,11). In most reports, the mean age at initial presentation is around 30 years (12,13). oth of our patients first presented with hypertension prior to the age of 25 years and disease prior to age 30 (Table 1). Cascon et al (14) have also described SDHD mutations in PCCs found in young patients, however such reports are limited (14). ilateral PCCs are more commonly known to be associated with multiple endocrine neoplasia type 2 protooncogene and VHL gene mutations. Our cases are unique as the patients presented with adrenal PCCs and carotid bifurcation PGLs with the SDHD mutation (Table 1). In at least one of the cases, testing for VHL gene mutation was performed due to the noradrenergic phenotype. When that proved to be negative, further testing for genes associated with noradrenergic activity revealed the SDHD mutation. New opportunities in genetic testing have been moving
4 SDHD Mutation and Pheochromocytoma, CE Clinical Case Rep. 2018;4(No. 3) e189 C Fig. 3. Computed and positron emission tomography scans of case 2 demonstrating left-adrenal pheochromocytoma and right-renal hilum paraganglioma ( and C) and carotid body paragangliomas ( and C). Table 1 Patient Characteristics Case 1 Case 2 Gender Female Male Hypertension diagnosis ge 11 ge 24 PCC location Size of PCC PGL location Left (unilateral initially) age 11, right adrenal PCC age 24 Right 3.0 cm Left (unknown) Carotid body Organ of Zuckerkandl Plasma metanephrine <0.20 nmol/l (reference range <0.50 nmol/l) ilateral at age 29 Right 5.0 cm Left 2.4 cm Carotid bifurcations Retrocaval PGL iochemistry Plasma normetanephrine 12 nmol/l (reference range <0.9 nmol/l) 24-hr urine norepinephrine 618 μg (reference range μg/24 hr) 24-hr urine epinephrine <1.5 μg (reference range 0-20 μg/24 hour) 24-hr urine norepinephrine μg (reference range μg/24 hour) 24-hr urine epinephrine 23.7 μg (reference range μg/24 hour) Treatment 24-hr urine dopamine 336 μg (reference range μg/24 hour) Left adrenalectomy (age 11) Right adrenalectomy and PGL resection at the organ of Zuckerkadl and left carotid body (age 24) Right adrenalectomy (age 31) Left adrenalectomy, retrocaval PGL, and right nephrectomy (age 39) Genetic mutation SDHD, exon 2 deletion SDHD, (c.217 dup (Ser73LysFx134)) Family history None Sister had neck PGL bbreviations: PCC = pheochromocytoma; PGL = paraganglioma; SDHD = succinate dehydrogenase subunit D gene.
5 e190 SDHD Mutation and Pheochromocytoma, CE Clinical Case Rep. 2018;4(No. 3) towards next generation sequencing (15-17). This was not performed on either of our patients since this was not available at the time of testing. Traditionally, SDHD mutation is associated with nonfunctional head and neck tumors, unlike our cases (7). There is evidence that individuals with PCC and germline SDHD mutations possess mutations in the 5 region of the SDHD gene. bout 50% of all germline SDHD mutations occur in the first 2 exons of the SDHD gene as well as the beginning of exon 3. When the 5 portion of the SDHD gene is disrupted, the ability of the succinate dehydrogenase enzyme complex to insert itself into the mitochondrial membrane is compromised, ultimately leading to a disassembly of complex II. Contrastingly, a missense mutation would not completely inactivate this complex (18). Eng et al (18) postulate that this is why 5 mutations seem to predispose to PCC whereas partial inactivation of the catalytic activity of the SDHD gene through missense mutations tends to lead to head and neck tumors. The SDHD mutations in both of our cases seem to follow the proposed hypothesis; in case 1 the deletion was located in the 5 location and in case 2 a frameshift mutation resulted in a stop codon. Eng et al (18) also note that truncating mutations, even after amino acid 63, would likely result in an inability of the enzyme complex to insert into the mitochondrial membrane. Further research is needed to understand this phenomenon. CONCLUSION Typically, noradrenergic adrenal PCC in a young patient leads to suspicion for disease linked to a VHL mutation. Similarly, abdominal noradrenergic PGLs are most suggestive of disease caused by succinate dehydrogenase subunit gene mutation. The unexpected association of bilateral PCCs with the SDHD mutation has important implications for the clinical management of PCC and PGL. Therefore, SDHD mutation analysis should no longer be limited to just head and neck PGLs but should be also considered in thoracic (19), abdominal, and pelvic PCCs and PGLs. DISCLOSURE Dr. King serves on the speakers bureau for and has received honoraria from Corcept Therapeutics. The other authors have no multiplicity of interest to disclose. REFERENCES 1. Taïeb D, Kaliski, oedeker CC, et al. Current approaches and recent developments in the management of head and neck paragangliomas. Endocr Rev. 2014;35: Ghayee HK, Vinik I, Pacak K, CE drenal Scientific Committee. Precision medicine in adrenal disorders: the next generation. Endocr Pract. 2017;23: Comino-Méndez I, Gracia-znárez FJ, Schiavi F, et al. Exome sequencing identifies MX mutations as a cause of hereditary pheochromocytoma. Nat Genet. 2011;43: Qin Y, Yao L, King EE, et al. Germline mutations in TMEM127 confer susceptibility to pheochromocytoma. Nat Genet. 2010;42: stuti D, Latif F, Dallol, et al. Gene mutations in the succinate dehydrogenase subunit SDH cause susceptibility to familial pheochromocytoma and to familial paraganglioma. m J Hum Genet. 2001;69: Niemann S, Müller U. Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat Genet. 2000;26: aysal E, Ferrell RE, Willett-rozick JE, et al. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science. 2000;287: Fishbein L, Leshchiner I, Walter V, et al. Comprehensive molecular characterization of pheochromocytoma and paraganglioma. Cancer Cell. 2017;31: Lussey-Lepoutre C, uffet, Gimenez-Roqueplo P, Favier J. Mitochondrial deficiencies in the predisposition to paraganglioma. Metabolites. 2017; Timmers HJ, Chen CC, Carrasquillo J, et al. Staging and functional characterization of pheochromocytoma and paraganglioma by 18F-fluorodeoxyglucose (18F-FDG) positron emission tomography. J Natl Cancer Inst. 2012;104: Garrigue P, odin-hullin, alasse L, et al. The evolving role of succinate in tumor metabolism: an 18F-FDG-based study. J Nucl Med. 2017;58: Karasek D, Shah U, Frysak Z, Stratakis C, Pacak K. n update on the genetics of pheochromocytoma. J Hum Hypertens. 2013;27: enn DE, Gimenez-Roqueplo P, Reilly JR, et al. Clinical presentation and penetrance of pheochromocytoma/paraganglioma syndromes. J Clin Endocrinol Metab. 2006;91: Cascon, Ruiz-Llorente S, Cebrian, et al. Identification of novel SDHD mutations in patients with phaeochromocytoma and/ or paraganglioma. Eur J Hum Genet. 2002;10: Sbardella E, Cranston T, Isidori M, et al. Routine genetic screening with a multi-gene panel in patients with pheochromocytomas. Endocrine In press. 16. Currás-Freixes M, Inglada-Pérez L, Mancikova V, et al. 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Accepted 5 June 2008 Published online 15 December 2008 in Wiley InterScience ( DOI: /hed.20930
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