Diagnosis Please
Note: This copy is for your personal non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, contact us at www.rsna.org/rsnarights.
Case 204: Nonketotic Hyperglycemiainduced Hemiballism-Hemichorea1
Adriano M. Priola, MD Dario Gned, MD Andrea Veltri, MD Sandro M. Priola, MD
Part one of this case appeared 4 months previously and may contain larger images. Published online 10.1148/radiol.14120840 Content codes: Radiology 2014; 271:304–308 1 From the Department of Diagnostic Imaging, San Luigi Gonzaga Hospital, University of Torino, Regione Gonzole 10, 10043 Orbassano, Turin, Italy. Received April 14, 2012; revision requested June 7; revision received July 8; accepted July 26; final version accepted August 11. Address correspondence to A.M.P. (e-mail: [email protected]).
Conflicts of interest are listed at the end of this article. q RSNA, 2014
304
History
An 87-year-old white woman presented to our emergency department with a 2-day history of involuntary movements of the right upper and lower extremities. The movements increased with action, decreased with relaxation, and disappeared during sleep. The patient’s medical history included diabetes mellitus type 2, congestive heart failure, and hypertension. No history of parkinsonism or other neurologic disorders was reported. Furthermore, the patient had no prior history of dopamine antagonist or estrogen medication use. At admission, she was fully alert and oriented. A physical examination revealed her muscle tone and strength were normal on both sides; however, she reported transient weakness in the right limbs. There was no evidence of sensory impairment, and cranial nerves were normal. The deep tendon reflexes were symmetrically hypoactive. Her skin was pink, warm, and dry. Laboratory tests revealed poorly controlled diabetes mellitus, with a fasting blood glucose level of 410 mg/dL (22.8 mmol/L) and a hemoglobin A1C level of 18.0%. The urine examination was negative for ketones. Shortly after admission, the patient’s blood sugar was controlled with insulin; this led to a steady correction of glycemia in the subsequent days. At admission, the patient underwent unenhanced brain computed tomography (CT) (Fig 1). Magnetic resonance (MR) imaging of the brain was performed 2 days later (Fig 2). After she was discharged from the hospital, the involuntary movements progressively decreased over the next few weeks until they disappeared. Two months later, follow-up unenhanced brain CT (not shown) showed the absence of abnormal findings.
Imaging Findings Unenhanced CT of the head revealed slight and homogeneous increased attenuation in the left lentiform nucleus (Fig 1a, 1b). By using narrow window width and slightly higher center settings, there was markedly increased conspicuity of left lenticular nucleus hyperattenuation (Fig 1c, 1d). MR imaging of the brain performed 2 days after onset of hemiballism-hemichorea revealed abnormally strong hyperintense signal in the posterior portion of the left putamen on T1-weighted images
(Fig 2a) and isointensity on T2-weighted images (Fig 2b). Diffusion-weighted images revealed normal signal intensity in the left putamen (Fig 2c). Follow-up unenhanced brain CT performed 2 months later showed that the abnormal hyperattenuated lesion in the left lenticular nucleus had completely resolved (not shown).
Discussion Hemiballism-hemichorea is a rare hyperkinetic movement disorder characterized by continuous involuntary movements of
radiology.rsna.org n Radiology: Volume 271: Number 1—April 2014
DIAGNOSIS PLEASE: Nonketotic Hyperglycemia-induced Hemiballism-Hemichorea
Figure 1
Figure 1: (a, b) Unenhanced brain CT scans obtained with standard settings (window width, 80 HU; window center, 20 HU) show faint and homogeneous hyperattenuation of the left lentiform nucleus (arrow) and a few lacunae in the right putamen and globus pallidus. (c, d) With variable soft-copy settings (window width, 15 HU; window center, 40 HU) chosen to accentuate the gray and white matter interface, the subtle abnormality of the left putamen is markedly enhanced (arrows).
an entire limb or of multiple limbs on one side of the body. These movements are irregular, of variable amplitude, and poorly patterned, usually involving the arm and leg together (1). The acute onset of hemiballism-hemichorea is caused by focal lesions in contralateral basal ganglia, particularly the striatum;
however, two cases of hemiballism caused by ipsilateral lesions have been described (1). Ischemic or hemorrhagic stroke represents the most common cause of disease; nonketotic hyperglycemia is the next most common cause (1–3). Hemiballism-hemichorea associated with hyperglicemia was first report-
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ed by Bedwell in 1960. He described the case of a 65-year-old woman with hemiballism that resolved as the blood-glucose abnormality was corrected, only to recur episodically as the patient experienced lapses in diabetic control (1,2). Subsequently, other authors observed advanced age of onset and female predominance, especially in Asian subjects (1–4). Although this syndrome usually occurs in elderly patients with diabetes, it could also be an initial manifestation of diabetes (3). The pathophysiology of hemiballism-hemichorea triggered by hyperglycemia is controversial and poorly understood. In a few histopathologic studies, researchers have found gliosis, gemistocyte accumulation, and selective loss of neurons, with out evidence of hemorrhage or infarction (5–7). Characteristic MR and CT findings in the basal ganglia have been docu mented in almost all cases of hemiballismhemichorea associated with hyperglycemia (1–9). High-attenuation changes involving the contralateral basal ganglia are common at head CT, although CT scans have been normal in some cases (1). Brain MR imaging typically shows T1 hyperintensity and T2 hypointensity in the basal ganglia contralateral to the movements, although T2 isointensity has been described in one-third of cases and was present in this patient (4). The putamen is more frequently involved than other basal ganglia. Similar to other researchers (5,6), we found a mismatch between the size of lesions detected on CT scans and the size of lesions detected on T1-weighted MR images, suggesting that two different pathophysiologic mechanisms underlie the CT and T1-weighted MR imaging findings (6). Various theories have been proposed to explain the imaging findings, including acute infarct, petechial hemorrhage, myelinolysis, calcium deposition, decreased synthesis of g-aminobutyric acid and acetylcholine secondary to metabolic changes, or injury secondary to hyperviscosity and vasogenic edema (1–6). Petechial hemorrhage with blood-brain barrier breakdown in the striatum has been suggested as the most plausible mecha305
DIAGNOSIS PLEASE: Nonketotic Hyperglycemia-induced Hemiballism-Hemichorea
Priola et al
Figure 2
Figure 2: (a) Axial T1-weighted MR image (repetition time msec/echo time msec, 597/15) of the brain at admission shows an area of increased signal intensity involving the posterior left putamen (arrow). Foci of minute cystic remote infarcts and dilated Virchow-Robin spaces in the basal ganglia are seen on both sides of the brain. (b) Axial T2-weighted MR image (701/23) shows isointensity of the left putamen in the same area as in a. (c) Axial diffusion-weighted (2900/65) MR image shows no abnormal signal intensity changes in the left putamen.
nism (3). However, MR findings suggest that petechial hemorrhage cannot be responsible for the lesions since if the striatal T1 hyperintensity represents methemoglobin (at the subacute stage of hemorrhage), T2 hyperintensity should also be present; this was not the case in this patient or in most previously reported cases (6). Other authors proposed that the high-signal-intensity lesions on T1-weighted MR images could be related to manganese accumulation in gemistocytes, which would result from an increase in the activity of manganese superoxide dismutase. This enzyme induction in gemistocytes (reactive astrocytes containing a rich protein content that usually appear during acute injury but later gradually shrink) can be triggered by multiple stimuli, including brain ischemia and hyperglycemia (8,9). Hence, the authors assumed that the acute putaminal dysfunction secondary to hyperglycemic or hyperosmolar insult could be associated with some degree of Wallerian degeneration of the internal white matter of the putamen with gemistocyte accumulation. Protein desiccation occurring in the course of Wallerian degeneration 306
could explain the CT hyperattenuation and the T1-weighted MR imaging pattern (9). The differential consideration for nonketotic hyperglycemia-induced hemiballism-hemichorea must include conditions related to clinical presentation and CT and MR imaging appearance. In regard to the clinical presentation, many diseases other than nonketotic hyperglycemia can manifest with the acute development of hemiballism-hemichorea. The most frequent condition is represented by ischemic or hemorrhagic stroke followed by complications of human immunodeficiency virus infection (1), vasculitis, central nervous system lupus, mass lesions, multiple sclerosis, thyrotoxicosis, and pharmacologic therapy (ie, anticonvulsants, levodopa, oral contraceptives, and neuroleptics) (2). However, in this patient, the characteristic CT and MR findings and the medical history, including laboratory values, make all these diagnoses unlikely. In regard to MR features, other causes of T1weighted hyperintense basal ganglia lesions are to be considered. Indeed, the typical T1-weighted MR imaging characteristic of hyperglycemic hemiballism-
hemichorea is not specific to this condition and can be observed in other toxic, metabolic, or degenerative disorders. The most frequent condition is chronic hepatic encephalopathy (4), followed by manganese toxicity during longterm parenteral nutrition (10), post–cardiac arrest encephalopathy, hypoglycemic coma, hypothyroidism, mild focal ischemia or chronic changes due to hypoxia, neurofibromatosis, Fahr disease or abnormal calcium metabolism, Wilson disease, and carbon monoxide poisoning (7). All these conditions usually involve basal ganglia on both sides of the brain converse to hyperglycemic hemiballismhemicorea; however, a few cases of bilateral increased T1 signal intensity within the striatum have been reported in patients with hemiballism-hemichorea associated with hyperglycemia (6). Moreover, patients with hemiballismhemichorea not related to hyperglycemia have a different presentation compared with this patient, and these conditions largely can be excluded on the basis of patient history and laboratory findings. Furthermore, in patients with hepatocerebral disease and manganese toxicity, the changes are seen mostly in the
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DIAGNOSIS PLEASE: Nonketotic Hyperglycemia-induced Hemiballism-Hemichorea
globus pallidus in contrast to hyperglycemia-related chorea-ballism where the putamen is the most consistent focus, as in this case (7). In patients developing hemiballismhemichorea secondary to nonketotic hyperglycemia, the clinical course is usually favorable, and the symptoms tend to resolve spontaneously with normaliza tion of hyperglycemia within hours, days, or weeks (1,4). Thus, normalization of glucose is the primary therapy, along with long-term diabetic control (4). However, 20% of patients have some persisting hemichorea-hemiballism for more than 3 months, although it is typically much milder than that at presentation. In these cases, pharmacologic therapy has a role in improving symptoms (1). In addition, striatal hyperintensity of basal ganglia is reversible after cessation of choreic and ballistic movements with complete resolution on CT and MR images within 2–11 months, although imaging resolution is slower than the clinical course (1,6). In summary, recognition of this unique clinicoradiologic manifestation with its peculiar CT and MR appearance is essential to select the correct therapy and avoid drugs to treat the clinical aspects of this syndrome when it is caused by hyperglycemia. Furthermore, vigilance for this cause of hemichorea-hemiballism is important, since the movement disorder may be the presentation of potentially dangerous underlying hyperglycemia. Disclosures of Conflicts of Interest: A.M.P. No relevant conflicts of interest to disclose. D.G. No relevant conflicts of interest to disclose. A.V. No relevant conflicts of interest to disclose. S.M.P. No relevant conflicts of interest to disclose.
References 1. Postuma RB, Lang AE. Hemiballism: revisiting a classic disorder. Lancet Neurol 2003; 2(11):661–668. 2. Hawley JS, Weiner WJ. Hemiballismus: current concepts and review. Parkinsonism Relat Disord 2012;18(2):125–129. 3. Lin JJ, Lin GY, Shih C, Shen WC. Presentation of striatal hyperintensity on T1-weighted MRI in patients with hemiballism-hemichorea caused by non-ketotic hyperglycemia: re-
port of seven new cases and a review of literature. J Neurol 2001;248(9):750–755. 4. Oh SH, Lee KY, Im JH, Lee MS. Chorea associated with non-ketotic hyperglycemia and hyperintensity basal ganglia lesion on T1-weighted brain MRI study: a metaanalysis of 53 cases including four present cases. J Neurol Sci 2002;200(1-2):57–62. 5. Ohara S, Nakagawa S, Tabata K, Hashimoto T. Hemiballism with hyperglycemia and striatal T1-MRI hyperintensity: an autopsy report. Mov Disord 2001;16(3):521–525. 6. Shan DE, Ho DM, Chang C, Pan HC, Teng MM. Hemichorea-hemiballism: an explanation for MR signal changes. AJNR Am J Neuroradiol 1998;19(5):863–870. 7. Lai PH, Tien RD, Chang MH, et al. Choreaballismus with nonketotic hyperglycemia in primary diabetes mellitus. AJNR Am J Neuroradiol 1996;17(6):1057–1064. 8. Chu K, Kang DW, Kim DE, Park SH, Roh JK. Diffusion-weighted and gradient echo magnetic resonance findings of hemichoreahemiballismus associated with diabetic hyperglycemia: a hyperviscosity syndrome? Arch Neurol 2002;59(3):448–452. 9. Wintermark M, Fischbein NJ, Mukherjee P, Yuh EL, Dillon WP. Unilateral putaminal CT, MR, and diffusion abnormalities secondary to nonketotic hyperglycemia in the setting of acute neurologic symptoms mimicking stroke. AJNR Am J Neuroradiol 2004;25(6): 975–976. 10. Mirowitz SA, Westrich TJ, Hirsch JD. Hyperintense basal ganglia on T1-weighted MR images in patients receiving parenteral nutrition. Radiology 1991;181(1):117–120.
Congratulations to the 187 individuals and 11 resident groups that submitted the most likely diagnosis (nonketotic hyperglycemia-induced hemiballism/ hemichorea) for Diagnosis Please, Case 204. The names and locations of the individuals and resident groups, as submitted, are as follows:
Individual responses Rifat F. Abdi, MD, Dhahran, Saudi Arabia Osamu Abe, MD, PhD, Itabashi-ku, Tokyo, Japan Gholamali Afshang, MD, Tinley Park, Ill Tahleel Altaf, MBBS, MD, Srinagar, Jammu and Kashmir, India Canan Altay, MD, Izmir, Turkey Albert J. Alter, MD, PhD, Blanchardville, Wis Nabil F. Ammouri, MD, Zahle, Lebanon Ruslan Asadov, MD, Istanbul, Turkey Debora C. Azevedo, Sao Paulo, Brazil Christopher W. Bailey, DO, Morgantown, WVa
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Dean E. Baird, MD, Potomac, Md Kenneth F. Baliga, MD, Rockford, Ill Thomas J. Barloon, MD, Iowa City, Iowa Dhiraj Baruah, MD, Wauwatosa, Wis Rupert Bauer, MD, Holzminden, Germany Manon N. Braat, MD, Nieuwegein, the Netherlands Eric L. Bressler, MD, Minnetonka, Minn Douglas C. Brown, MD, Virginia Beach, Va Ian A. Burgess, MD, North Sydney, New South Wales, Australia Jose Antonio Camilo Machado, Sr, MD, Goiania, Goias, Brazil Tirso Cascajares Murillo, MD, Hermosillo, Sonora, Mexico Phillip M. Cheng, MD, MS, Culver City, Calif Michael H. Childress, MD, Washington, DC Christopher Chu, MBBS, FRANZC, Sydney, New South Wales, Australia Ming-Tsung Chuang, MD, Kaohsiung City, Taiwan Carla Conceicao, MD, Lisboa, Portugal Marco A. Cura, MD, Highland Park, Tex Anil K. Dasyam, MD, Pittsburgh, Pa Marc G. De Baets, MD, Collina d'Oro, Ticino, Switzerland Peter de Baets, MD, Damme, Belgium Kristof De Meerleer, MD, Sint Blasius Boekel-Zwalm, Belgium Eduardo P. de Oliveira, Sao Jose do Rio Preto, São Paulo, Brazil Lucas M. DeJohn, DO, Wyomissing, Pa Mustafa K. Demir, MD, Istanbul, Turkey Thaworn Dendumrongsup, MD, Songkhla, Thailand Ivan M. Dequesada, MD, Atlanta, Ga Carlos R. Deragopyan, MD, Buenos Aires, Argentina Mark T. DiMarcangelo, DO, MSc, Cherry Hill, NJ Dionisios Drakopoulos, MD, Palaio Faliro, Athens, Greece Richard N. Edelstein, MD, Ocean Ridge, Fla Seyed A. Emamian, MD, PhD, Rockville, Md Pedro Erthal Vianna, Rio de Janeiro, Brazil Francis T. Flaherty, MD, Ridgefield, Conn Enrique Flores, MD, Santa Cristina, Oleiros, A Coruna, Spain Reza Forghani, MD, PhD, Cote-saint-Luc, Quebec, Canada Akira Fujikawa, MD, Tokyo, Japan Ram P. Galwa, MD, Fredericton, New Brunswick, Canada Mark G. Goldshein, MD, Andover, Mass Alvaro Gomez Naar, MD, Salta Capital, Salta, Argentina Wataru Gonoi, MD, PhD, Bunkyo-ku, Tokyo, Japan Maria A. Gosein, MBBS, FRCR, Santa Cruz, Trinidad And Tobago Manu S. Goyal, MD, MSc, Saint Louis, Mo Alex Grande Astorquiza, MD, Vigo, Pontevedra, Spain Pramod K. Gupta, MD, Plano, Tex Akifumi Hagiwara, MD, Tokyo, Japan
307
DIAGNOSIS PLEASE: Nonketotic Hyperglycemia-induced Hemiballism-Hemichorea
Osamu Hasegawa, MD, Koriyama, Fukushima, Japan D. C. Heasley, Jr, MD, Dallas, Tex Christoph Hefel, Feldkirch, Austria Yuusuke Hirokawa, MD, Kyoto, Japan Nerea Hormaza, MD, Barakaldo, Bizkaia, Spain Sodai Hoshiai, MD, Tsukuba, Ibaraki, Japan Alberto C. Iaia, MD, Wilmington, Del Noriatsu Ichiba, MD, Otsu, Shiga, Japan Takashi Ikeuchi, Moriyama, Shiga, Japan Akitoshi Inoue, MD, Otsu, Shiga, Japan Richard N. Irion, MD, Murray, Utah Janaranjan Jalli, DMRD, MD, Vizag, India Sharada Jayagopal, MD, East Williston, NY Vishwanath V. Joshi, Jr, MBBS, Mysore, Karnataka, India Kenji Kachi, MD, Tsuchiura, Ibaraki, Japan Shinichi Kan, MD, PhD, Yokohama, Japan Koki Kato, MD, Utsunomiya, Tochigi, Japan Yasushi Kawata, MD, Yurihonjo City, Akita, Japan Shanigarn Keoplung, MD, Muang Nonthaburi, Nonthaburi, Thailand Patrick Kiely, MBBCh, Limerick, Ireland Takao Kiguchi, MD, Niigata, Japan Takuji Kiryu, MD, PhD, Gifu, Japan Osamu Kizu, MD, Ohtsu, Japan Mitchell A. Klein, MD, Mequon, Wis Mehmet Kocak, MD, Chicago, Ill Masamichi Koyama, MD, PhD, Tokyo, Japan Richard E. Krauthamer, MD, Rolling Hills, Calif John J. Krol, MD, Lexington, Ky Kemmei Kuramoto, MD, Tachikawa, Tokyo, Japan Yoshihisa Kurosaki, MD, Setagaya-ku, Tokyo, Japan Ryo Kuwahara, MD, Kyoto, Nakagyogu, Japan Mario A. Laguna, MD, Milwaukee, Wis Rupakumar Lakshminarayanan, MBBS, MD, Madurai, Tamilnadu, India Michael Laucella, MD, Fort Salonga, NY Chee Hwee Lee, MD, Taipei, Taiwan Stefanie Lee, Toronto, Ontario, Canada David A. Lisle, MBBS, Brisbane, Queensland, Australia Rafael M. Loureiro, MD, Sao Paulo, Brazil Mark D. Mamlouk, MD, Foster City, Calif Stephen V. Manghisi, MD, Closter, NJ Satoshi Matsushima, MD, Tokyo, Japan Edward J. Mauch, MD, Harrison Township, Mich Brian McNamee, MD, Coeur d’Alene, Idaho Albert Mendelson, MD, Northbrook, Ill Mehran Midia, MD, Burlington, Ontario, Canada Manabu Minami, MD, PhD, Yokohama, Japan Kenichi Mizuki, MD, Hamamatsu-shi, Shizuokaken, Japan Jose Mondello, MD, Buenos Aires, Argentina
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Livia T. Morais, MD, Boston, Mass Tiago N. Morato, MD, Brasilia, Distrito Federal, Brazil Matthew A. Morgan, MD, Philadelphia, Pa Toshio Moritani, MD, PhD, Iowa City, Iowa Takaki Murata, MD, Sendai, Japan Kyoko Nagai, MD, Yokohama, Japan Kazuyoshi Nakamura, MD, Yokkaichi, Mie, Japan Tammam N. Nehme, MD, Mattawan, Mich Tuan Duc Nguyen, MD, Ski, Norway Hironori Nishibori, MD, Minokamo City, Gifu, Japan Tomokazu Nishiguchi, MD, PhD, Osaka, Japan Mizuki Nishino, MD, Boston, Mass Hiroshi Nobusawa, MD, PhD, Ota, Tokyo, Japan Roque Oca, MD, Vigo, Pontevedra, Spain Hugo J. Paladini, MD, Buenos Aires, Argentina Vishal Panchal, San Francisco, Calif Ioannis E. Papachristos, MD, Agrinio, Greece Narendrakumar P. Patel, MD, Newburgh, NY Satish D. Patel, MD, Shavertown, Pa Suresh K. Patel, MD, Chicago, Ill Aruna R. Patil, MD, FRCR, Bangalore, Karnataka, India Yeliz Pekcevik, Izmir, Turkey John M. Plotke, MD, Naperville, Ill Rubem Pochaczevsky, MD, Bronx, NY Gerhardus J. Potgieter, MBChB, Stafford Heights, Australia Elias Primetis, MD, Athens, Greece Daniel C. Rappaport, MD, Toronto, Ontario, Canada Ryan P. Rebello, MD, Dundas, Ontario, Canada Mathieu H. Rodallec, MD, Paris, France Hugo Rodriguez Requena, MD, Madrid, Spain Stefan Roosendaal, MD, PhD, Amsterdam, the Netherlands Akihiko Sakata, MD, Kyoto, Japan Meir H. Scheinfeld, MD, Suffern, NY Steven M. Schultz, MD, Fort Worth, Tex Stephen D. Scotti, MD, Edina, Minn Anthony J. Scuderi, MD, Johnstown, Pa Matthew P. Shapiro, MD, Charlottesville, Va Hideki Shima, MD, Narita, Chiba, Japan Taro Shimono, MD, Osaka, Japan Ichiro Shirouzu, MD, Tokyo, Japan Paul J. Shogan, MD, Clarksville, Tenn Ho L. Sie, MD, Henderson, Nev Achint K. Singh, MD, San Antonio, Tex Shakti P. Singh, MD, Delhi, India David F. Sobel, MD, La Jolla, Calif Evan G. Stein, MD, PhD, New York, NY Jorge O. Suarez, MD, Bogota, Colombia Hongliang Sun, MD, Beijing, China Frank R. Tamura, MD, Fresno, Calif Eliko Tanaka, MD, Yokohama, Japan Takashi Tanaka, MD, Okayama, Japan Bisher Tarabishy, MD, West Bloomfield, Mich
Satoshi Tatsuno, MD, Ichikawa, Chiba, Japan Douglas L. Teich, MD, Brookline, Mass Yasuyo Teramura, MD, Tokorozawa, Saitama, Japan Christina Theoret, MD, Saskatoon, Saskatchewan, Canada Eugene Tong, MD, Austin, Tex Ulysses S. Torres, MD, Sao Paulo, Brazil Meric Tuzun, MD, Ankara, Turkey Atsushi Uehara, Niigata, Japan Piet K. Vanhoenacker, MD, Moorsel, Belgium Alexander Vidershayn, MD, Brooklyn, NY Joao Carlos C. Vilhena, MD, Sao Paulo, Brazil Pier Carlo Villani, MD, Bari, Italy Ainhoa Viteri, MD, Bilbao, Biscay, Spain Christopher P. Vittore, MD, Belvidere, Ill Lynne Voutsinas, MD, Staten Island, NY Garrett L. Walworth, MD, Milford, Mich Haruo Watanabe, MD, Gifu, Japan Hsu-Huei Weng, MD, PhD, Chia-Yi County, Taiwan Jeffrey H. West, MD, Jacksonville, Fla Noritaka Yamakawa, Kyoto, Japan Tatsuya Yamamoto, MD, Yoshida-gun, Fukui, Japan Toshihide Yamaoka, MD, Kyoto, Japan Koji Yamashita, MD, PhD, Fukuoka, Japan Koichiro Yasaka, MD, Tokyo, Japan Kurata Yasuhisa, MD, Kobe, Hyogo, Japan Hajime Yokota, MD, Chiba, Japan Rika Yoshida, MD, Utsunomiya, Tochigi, Japan Satoru Yoshida, MD, PhD, Muroran, Hokkaido, Japan Kaneko You, Gifu, Japan Carlos A. Zamora, MD, PhD, Lutherville, Md Yi Cheng Zhou, MD, Wuhan, Hub, China Ahmed Zidan, MD, Barcelona, Spain
Resident group responses ICESP Residents, Sao Paulo, Brazil Mater Dei Hospital Radiology Residents, Malta Mie University Hospital Radiology Residents, MD, Tsu, Mie, Japan Prince of Songkla University Radiology Residents, Songkla, Thailand Thomas Jefferson University Radiology Residents, Philadelphia, Pa Tsukuba University Hospital Radiology Residents, Tsukuba, Ibaraki, Japan University of Pennsylvania Radiology Residents, Philadelphia, Pa UTHSC at San Antonio Radiology Residents, MD, San Antonio, Tex University of Washington Radiology Residents, MD, Seattle, Wash Virginia Commonwealth University Radiology Residents, Richmond, Va Yale University Radiology Residents, New Haven, Conn
radiology.rsna.org n Radiology: Volume 271: Number 1—April 2014
Note: This copy is for your personal non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, contact us at www.rsna.org/rsnarights.
Case 204: Nonketotic Hyperglycemiainduced Hemiballism-Hemichorea1
Adriano M. Priola, MD Dario Gned, MD Andrea Veltri, MD Sandro M. Priola, MD
Part one of this case appeared 4 months previously and may contain larger images. Published online 10.1148/radiol.14120840 Content codes: Radiology 2014; 271:304–308 1 From the Department of Diagnostic Imaging, San Luigi Gonzaga Hospital, University of Torino, Regione Gonzole 10, 10043 Orbassano, Turin, Italy. Received April 14, 2012; revision requested June 7; revision received July 8; accepted July 26; final version accepted August 11. Address correspondence to A.M.P. (e-mail: [email protected]).
Conflicts of interest are listed at the end of this article. q RSNA, 2014
304
History
An 87-year-old white woman presented to our emergency department with a 2-day history of involuntary movements of the right upper and lower extremities. The movements increased with action, decreased with relaxation, and disappeared during sleep. The patient’s medical history included diabetes mellitus type 2, congestive heart failure, and hypertension. No history of parkinsonism or other neurologic disorders was reported. Furthermore, the patient had no prior history of dopamine antagonist or estrogen medication use. At admission, she was fully alert and oriented. A physical examination revealed her muscle tone and strength were normal on both sides; however, she reported transient weakness in the right limbs. There was no evidence of sensory impairment, and cranial nerves were normal. The deep tendon reflexes were symmetrically hypoactive. Her skin was pink, warm, and dry. Laboratory tests revealed poorly controlled diabetes mellitus, with a fasting blood glucose level of 410 mg/dL (22.8 mmol/L) and a hemoglobin A1C level of 18.0%. The urine examination was negative for ketones. Shortly after admission, the patient’s blood sugar was controlled with insulin; this led to a steady correction of glycemia in the subsequent days. At admission, the patient underwent unenhanced brain computed tomography (CT) (Fig 1). Magnetic resonance (MR) imaging of the brain was performed 2 days later (Fig 2). After she was discharged from the hospital, the involuntary movements progressively decreased over the next few weeks until they disappeared. Two months later, follow-up unenhanced brain CT (not shown) showed the absence of abnormal findings.
Imaging Findings Unenhanced CT of the head revealed slight and homogeneous increased attenuation in the left lentiform nucleus (Fig 1a, 1b). By using narrow window width and slightly higher center settings, there was markedly increased conspicuity of left lenticular nucleus hyperattenuation (Fig 1c, 1d). MR imaging of the brain performed 2 days after onset of hemiballism-hemichorea revealed abnormally strong hyperintense signal in the posterior portion of the left putamen on T1-weighted images
(Fig 2a) and isointensity on T2-weighted images (Fig 2b). Diffusion-weighted images revealed normal signal intensity in the left putamen (Fig 2c). Follow-up unenhanced brain CT performed 2 months later showed that the abnormal hyperattenuated lesion in the left lenticular nucleus had completely resolved (not shown).
Discussion Hemiballism-hemichorea is a rare hyperkinetic movement disorder characterized by continuous involuntary movements of
radiology.rsna.org n Radiology: Volume 271: Number 1—April 2014
DIAGNOSIS PLEASE: Nonketotic Hyperglycemia-induced Hemiballism-Hemichorea
Figure 1
Figure 1: (a, b) Unenhanced brain CT scans obtained with standard settings (window width, 80 HU; window center, 20 HU) show faint and homogeneous hyperattenuation of the left lentiform nucleus (arrow) and a few lacunae in the right putamen and globus pallidus. (c, d) With variable soft-copy settings (window width, 15 HU; window center, 40 HU) chosen to accentuate the gray and white matter interface, the subtle abnormality of the left putamen is markedly enhanced (arrows).
an entire limb or of multiple limbs on one side of the body. These movements are irregular, of variable amplitude, and poorly patterned, usually involving the arm and leg together (1). The acute onset of hemiballism-hemichorea is caused by focal lesions in contralateral basal ganglia, particularly the striatum;
however, two cases of hemiballism caused by ipsilateral lesions have been described (1). Ischemic or hemorrhagic stroke represents the most common cause of disease; nonketotic hyperglycemia is the next most common cause (1–3). Hemiballism-hemichorea associated with hyperglicemia was first report-
Radiology: Volume 271: Number 1—April 2014 n radiology.rsna.org
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ed by Bedwell in 1960. He described the case of a 65-year-old woman with hemiballism that resolved as the blood-glucose abnormality was corrected, only to recur episodically as the patient experienced lapses in diabetic control (1,2). Subsequently, other authors observed advanced age of onset and female predominance, especially in Asian subjects (1–4). Although this syndrome usually occurs in elderly patients with diabetes, it could also be an initial manifestation of diabetes (3). The pathophysiology of hemiballism-hemichorea triggered by hyperglycemia is controversial and poorly understood. In a few histopathologic studies, researchers have found gliosis, gemistocyte accumulation, and selective loss of neurons, with out evidence of hemorrhage or infarction (5–7). Characteristic MR and CT findings in the basal ganglia have been docu mented in almost all cases of hemiballismhemichorea associated with hyperglycemia (1–9). High-attenuation changes involving the contralateral basal ganglia are common at head CT, although CT scans have been normal in some cases (1). Brain MR imaging typically shows T1 hyperintensity and T2 hypointensity in the basal ganglia contralateral to the movements, although T2 isointensity has been described in one-third of cases and was present in this patient (4). The putamen is more frequently involved than other basal ganglia. Similar to other researchers (5,6), we found a mismatch between the size of lesions detected on CT scans and the size of lesions detected on T1-weighted MR images, suggesting that two different pathophysiologic mechanisms underlie the CT and T1-weighted MR imaging findings (6). Various theories have been proposed to explain the imaging findings, including acute infarct, petechial hemorrhage, myelinolysis, calcium deposition, decreased synthesis of g-aminobutyric acid and acetylcholine secondary to metabolic changes, or injury secondary to hyperviscosity and vasogenic edema (1–6). Petechial hemorrhage with blood-brain barrier breakdown in the striatum has been suggested as the most plausible mecha305
DIAGNOSIS PLEASE: Nonketotic Hyperglycemia-induced Hemiballism-Hemichorea
Priola et al
Figure 2
Figure 2: (a) Axial T1-weighted MR image (repetition time msec/echo time msec, 597/15) of the brain at admission shows an area of increased signal intensity involving the posterior left putamen (arrow). Foci of minute cystic remote infarcts and dilated Virchow-Robin spaces in the basal ganglia are seen on both sides of the brain. (b) Axial T2-weighted MR image (701/23) shows isointensity of the left putamen in the same area as in a. (c) Axial diffusion-weighted (2900/65) MR image shows no abnormal signal intensity changes in the left putamen.
nism (3). However, MR findings suggest that petechial hemorrhage cannot be responsible for the lesions since if the striatal T1 hyperintensity represents methemoglobin (at the subacute stage of hemorrhage), T2 hyperintensity should also be present; this was not the case in this patient or in most previously reported cases (6). Other authors proposed that the high-signal-intensity lesions on T1-weighted MR images could be related to manganese accumulation in gemistocytes, which would result from an increase in the activity of manganese superoxide dismutase. This enzyme induction in gemistocytes (reactive astrocytes containing a rich protein content that usually appear during acute injury but later gradually shrink) can be triggered by multiple stimuli, including brain ischemia and hyperglycemia (8,9). Hence, the authors assumed that the acute putaminal dysfunction secondary to hyperglycemic or hyperosmolar insult could be associated with some degree of Wallerian degeneration of the internal white matter of the putamen with gemistocyte accumulation. Protein desiccation occurring in the course of Wallerian degeneration 306
could explain the CT hyperattenuation and the T1-weighted MR imaging pattern (9). The differential consideration for nonketotic hyperglycemia-induced hemiballism-hemichorea must include conditions related to clinical presentation and CT and MR imaging appearance. In regard to the clinical presentation, many diseases other than nonketotic hyperglycemia can manifest with the acute development of hemiballism-hemichorea. The most frequent condition is represented by ischemic or hemorrhagic stroke followed by complications of human immunodeficiency virus infection (1), vasculitis, central nervous system lupus, mass lesions, multiple sclerosis, thyrotoxicosis, and pharmacologic therapy (ie, anticonvulsants, levodopa, oral contraceptives, and neuroleptics) (2). However, in this patient, the characteristic CT and MR findings and the medical history, including laboratory values, make all these diagnoses unlikely. In regard to MR features, other causes of T1weighted hyperintense basal ganglia lesions are to be considered. Indeed, the typical T1-weighted MR imaging characteristic of hyperglycemic hemiballism-
hemichorea is not specific to this condition and can be observed in other toxic, metabolic, or degenerative disorders. The most frequent condition is chronic hepatic encephalopathy (4), followed by manganese toxicity during longterm parenteral nutrition (10), post–cardiac arrest encephalopathy, hypoglycemic coma, hypothyroidism, mild focal ischemia or chronic changes due to hypoxia, neurofibromatosis, Fahr disease or abnormal calcium metabolism, Wilson disease, and carbon monoxide poisoning (7). All these conditions usually involve basal ganglia on both sides of the brain converse to hyperglycemic hemiballismhemicorea; however, a few cases of bilateral increased T1 signal intensity within the striatum have been reported in patients with hemiballism-hemichorea associated with hyperglycemia (6). Moreover, patients with hemiballismhemichorea not related to hyperglycemia have a different presentation compared with this patient, and these conditions largely can be excluded on the basis of patient history and laboratory findings. Furthermore, in patients with hepatocerebral disease and manganese toxicity, the changes are seen mostly in the
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globus pallidus in contrast to hyperglycemia-related chorea-ballism where the putamen is the most consistent focus, as in this case (7). In patients developing hemiballismhemichorea secondary to nonketotic hyperglycemia, the clinical course is usually favorable, and the symptoms tend to resolve spontaneously with normaliza tion of hyperglycemia within hours, days, or weeks (1,4). Thus, normalization of glucose is the primary therapy, along with long-term diabetic control (4). However, 20% of patients have some persisting hemichorea-hemiballism for more than 3 months, although it is typically much milder than that at presentation. In these cases, pharmacologic therapy has a role in improving symptoms (1). In addition, striatal hyperintensity of basal ganglia is reversible after cessation of choreic and ballistic movements with complete resolution on CT and MR images within 2–11 months, although imaging resolution is slower than the clinical course (1,6). In summary, recognition of this unique clinicoradiologic manifestation with its peculiar CT and MR appearance is essential to select the correct therapy and avoid drugs to treat the clinical aspects of this syndrome when it is caused by hyperglycemia. Furthermore, vigilance for this cause of hemichorea-hemiballism is important, since the movement disorder may be the presentation of potentially dangerous underlying hyperglycemia. Disclosures of Conflicts of Interest: A.M.P. No relevant conflicts of interest to disclose. D.G. No relevant conflicts of interest to disclose. A.V. No relevant conflicts of interest to disclose. S.M.P. No relevant conflicts of interest to disclose.
References 1. Postuma RB, Lang AE. Hemiballism: revisiting a classic disorder. Lancet Neurol 2003; 2(11):661–668. 2. Hawley JS, Weiner WJ. Hemiballismus: current concepts and review. Parkinsonism Relat Disord 2012;18(2):125–129. 3. Lin JJ, Lin GY, Shih C, Shen WC. Presentation of striatal hyperintensity on T1-weighted MRI in patients with hemiballism-hemichorea caused by non-ketotic hyperglycemia: re-
port of seven new cases and a review of literature. J Neurol 2001;248(9):750–755. 4. Oh SH, Lee KY, Im JH, Lee MS. Chorea associated with non-ketotic hyperglycemia and hyperintensity basal ganglia lesion on T1-weighted brain MRI study: a metaanalysis of 53 cases including four present cases. J Neurol Sci 2002;200(1-2):57–62. 5. Ohara S, Nakagawa S, Tabata K, Hashimoto T. Hemiballism with hyperglycemia and striatal T1-MRI hyperintensity: an autopsy report. Mov Disord 2001;16(3):521–525. 6. Shan DE, Ho DM, Chang C, Pan HC, Teng MM. Hemichorea-hemiballism: an explanation for MR signal changes. AJNR Am J Neuroradiol 1998;19(5):863–870. 7. Lai PH, Tien RD, Chang MH, et al. Choreaballismus with nonketotic hyperglycemia in primary diabetes mellitus. AJNR Am J Neuroradiol 1996;17(6):1057–1064. 8. Chu K, Kang DW, Kim DE, Park SH, Roh JK. Diffusion-weighted and gradient echo magnetic resonance findings of hemichoreahemiballismus associated with diabetic hyperglycemia: a hyperviscosity syndrome? Arch Neurol 2002;59(3):448–452. 9. Wintermark M, Fischbein NJ, Mukherjee P, Yuh EL, Dillon WP. Unilateral putaminal CT, MR, and diffusion abnormalities secondary to nonketotic hyperglycemia in the setting of acute neurologic symptoms mimicking stroke. AJNR Am J Neuroradiol 2004;25(6): 975–976. 10. Mirowitz SA, Westrich TJ, Hirsch JD. Hyperintense basal ganglia on T1-weighted MR images in patients receiving parenteral nutrition. Radiology 1991;181(1):117–120.
Congratulations to the 187 individuals and 11 resident groups that submitted the most likely diagnosis (nonketotic hyperglycemia-induced hemiballism/ hemichorea) for Diagnosis Please, Case 204. The names and locations of the individuals and resident groups, as submitted, are as follows:
Individual responses Rifat F. Abdi, MD, Dhahran, Saudi Arabia Osamu Abe, MD, PhD, Itabashi-ku, Tokyo, Japan Gholamali Afshang, MD, Tinley Park, Ill Tahleel Altaf, MBBS, MD, Srinagar, Jammu and Kashmir, India Canan Altay, MD, Izmir, Turkey Albert J. Alter, MD, PhD, Blanchardville, Wis Nabil F. Ammouri, MD, Zahle, Lebanon Ruslan Asadov, MD, Istanbul, Turkey Debora C. Azevedo, Sao Paulo, Brazil Christopher W. Bailey, DO, Morgantown, WVa
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Dean E. Baird, MD, Potomac, Md Kenneth F. Baliga, MD, Rockford, Ill Thomas J. Barloon, MD, Iowa City, Iowa Dhiraj Baruah, MD, Wauwatosa, Wis Rupert Bauer, MD, Holzminden, Germany Manon N. Braat, MD, Nieuwegein, the Netherlands Eric L. Bressler, MD, Minnetonka, Minn Douglas C. Brown, MD, Virginia Beach, Va Ian A. Burgess, MD, North Sydney, New South Wales, Australia Jose Antonio Camilo Machado, Sr, MD, Goiania, Goias, Brazil Tirso Cascajares Murillo, MD, Hermosillo, Sonora, Mexico Phillip M. Cheng, MD, MS, Culver City, Calif Michael H. Childress, MD, Washington, DC Christopher Chu, MBBS, FRANZC, Sydney, New South Wales, Australia Ming-Tsung Chuang, MD, Kaohsiung City, Taiwan Carla Conceicao, MD, Lisboa, Portugal Marco A. Cura, MD, Highland Park, Tex Anil K. Dasyam, MD, Pittsburgh, Pa Marc G. De Baets, MD, Collina d'Oro, Ticino, Switzerland Peter de Baets, MD, Damme, Belgium Kristof De Meerleer, MD, Sint Blasius Boekel-Zwalm, Belgium Eduardo P. de Oliveira, Sao Jose do Rio Preto, São Paulo, Brazil Lucas M. DeJohn, DO, Wyomissing, Pa Mustafa K. Demir, MD, Istanbul, Turkey Thaworn Dendumrongsup, MD, Songkhla, Thailand Ivan M. Dequesada, MD, Atlanta, Ga Carlos R. Deragopyan, MD, Buenos Aires, Argentina Mark T. DiMarcangelo, DO, MSc, Cherry Hill, NJ Dionisios Drakopoulos, MD, Palaio Faliro, Athens, Greece Richard N. Edelstein, MD, Ocean Ridge, Fla Seyed A. Emamian, MD, PhD, Rockville, Md Pedro Erthal Vianna, Rio de Janeiro, Brazil Francis T. Flaherty, MD, Ridgefield, Conn Enrique Flores, MD, Santa Cristina, Oleiros, A Coruna, Spain Reza Forghani, MD, PhD, Cote-saint-Luc, Quebec, Canada Akira Fujikawa, MD, Tokyo, Japan Ram P. Galwa, MD, Fredericton, New Brunswick, Canada Mark G. Goldshein, MD, Andover, Mass Alvaro Gomez Naar, MD, Salta Capital, Salta, Argentina Wataru Gonoi, MD, PhD, Bunkyo-ku, Tokyo, Japan Maria A. Gosein, MBBS, FRCR, Santa Cruz, Trinidad And Tobago Manu S. Goyal, MD, MSc, Saint Louis, Mo Alex Grande Astorquiza, MD, Vigo, Pontevedra, Spain Pramod K. Gupta, MD, Plano, Tex Akifumi Hagiwara, MD, Tokyo, Japan
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Osamu Hasegawa, MD, Koriyama, Fukushima, Japan D. C. Heasley, Jr, MD, Dallas, Tex Christoph Hefel, Feldkirch, Austria Yuusuke Hirokawa, MD, Kyoto, Japan Nerea Hormaza, MD, Barakaldo, Bizkaia, Spain Sodai Hoshiai, MD, Tsukuba, Ibaraki, Japan Alberto C. Iaia, MD, Wilmington, Del Noriatsu Ichiba, MD, Otsu, Shiga, Japan Takashi Ikeuchi, Moriyama, Shiga, Japan Akitoshi Inoue, MD, Otsu, Shiga, Japan Richard N. Irion, MD, Murray, Utah Janaranjan Jalli, DMRD, MD, Vizag, India Sharada Jayagopal, MD, East Williston, NY Vishwanath V. Joshi, Jr, MBBS, Mysore, Karnataka, India Kenji Kachi, MD, Tsuchiura, Ibaraki, Japan Shinichi Kan, MD, PhD, Yokohama, Japan Koki Kato, MD, Utsunomiya, Tochigi, Japan Yasushi Kawata, MD, Yurihonjo City, Akita, Japan Shanigarn Keoplung, MD, Muang Nonthaburi, Nonthaburi, Thailand Patrick Kiely, MBBCh, Limerick, Ireland Takao Kiguchi, MD, Niigata, Japan Takuji Kiryu, MD, PhD, Gifu, Japan Osamu Kizu, MD, Ohtsu, Japan Mitchell A. Klein, MD, Mequon, Wis Mehmet Kocak, MD, Chicago, Ill Masamichi Koyama, MD, PhD, Tokyo, Japan Richard E. Krauthamer, MD, Rolling Hills, Calif John J. Krol, MD, Lexington, Ky Kemmei Kuramoto, MD, Tachikawa, Tokyo, Japan Yoshihisa Kurosaki, MD, Setagaya-ku, Tokyo, Japan Ryo Kuwahara, MD, Kyoto, Nakagyogu, Japan Mario A. Laguna, MD, Milwaukee, Wis Rupakumar Lakshminarayanan, MBBS, MD, Madurai, Tamilnadu, India Michael Laucella, MD, Fort Salonga, NY Chee Hwee Lee, MD, Taipei, Taiwan Stefanie Lee, Toronto, Ontario, Canada David A. Lisle, MBBS, Brisbane, Queensland, Australia Rafael M. Loureiro, MD, Sao Paulo, Brazil Mark D. Mamlouk, MD, Foster City, Calif Stephen V. Manghisi, MD, Closter, NJ Satoshi Matsushima, MD, Tokyo, Japan Edward J. Mauch, MD, Harrison Township, Mich Brian McNamee, MD, Coeur d’Alene, Idaho Albert Mendelson, MD, Northbrook, Ill Mehran Midia, MD, Burlington, Ontario, Canada Manabu Minami, MD, PhD, Yokohama, Japan Kenichi Mizuki, MD, Hamamatsu-shi, Shizuokaken, Japan Jose Mondello, MD, Buenos Aires, Argentina
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Livia T. Morais, MD, Boston, Mass Tiago N. Morato, MD, Brasilia, Distrito Federal, Brazil Matthew A. Morgan, MD, Philadelphia, Pa Toshio Moritani, MD, PhD, Iowa City, Iowa Takaki Murata, MD, Sendai, Japan Kyoko Nagai, MD, Yokohama, Japan Kazuyoshi Nakamura, MD, Yokkaichi, Mie, Japan Tammam N. Nehme, MD, Mattawan, Mich Tuan Duc Nguyen, MD, Ski, Norway Hironori Nishibori, MD, Minokamo City, Gifu, Japan Tomokazu Nishiguchi, MD, PhD, Osaka, Japan Mizuki Nishino, MD, Boston, Mass Hiroshi Nobusawa, MD, PhD, Ota, Tokyo, Japan Roque Oca, MD, Vigo, Pontevedra, Spain Hugo J. Paladini, MD, Buenos Aires, Argentina Vishal Panchal, San Francisco, Calif Ioannis E. Papachristos, MD, Agrinio, Greece Narendrakumar P. Patel, MD, Newburgh, NY Satish D. Patel, MD, Shavertown, Pa Suresh K. Patel, MD, Chicago, Ill Aruna R. Patil, MD, FRCR, Bangalore, Karnataka, India Yeliz Pekcevik, Izmir, Turkey John M. Plotke, MD, Naperville, Ill Rubem Pochaczevsky, MD, Bronx, NY Gerhardus J. Potgieter, MBChB, Stafford Heights, Australia Elias Primetis, MD, Athens, Greece Daniel C. Rappaport, MD, Toronto, Ontario, Canada Ryan P. Rebello, MD, Dundas, Ontario, Canada Mathieu H. Rodallec, MD, Paris, France Hugo Rodriguez Requena, MD, Madrid, Spain Stefan Roosendaal, MD, PhD, Amsterdam, the Netherlands Akihiko Sakata, MD, Kyoto, Japan Meir H. Scheinfeld, MD, Suffern, NY Steven M. Schultz, MD, Fort Worth, Tex Stephen D. Scotti, MD, Edina, Minn Anthony J. Scuderi, MD, Johnstown, Pa Matthew P. Shapiro, MD, Charlottesville, Va Hideki Shima, MD, Narita, Chiba, Japan Taro Shimono, MD, Osaka, Japan Ichiro Shirouzu, MD, Tokyo, Japan Paul J. Shogan, MD, Clarksville, Tenn Ho L. Sie, MD, Henderson, Nev Achint K. Singh, MD, San Antonio, Tex Shakti P. Singh, MD, Delhi, India David F. Sobel, MD, La Jolla, Calif Evan G. Stein, MD, PhD, New York, NY Jorge O. Suarez, MD, Bogota, Colombia Hongliang Sun, MD, Beijing, China Frank R. Tamura, MD, Fresno, Calif Eliko Tanaka, MD, Yokohama, Japan Takashi Tanaka, MD, Okayama, Japan Bisher Tarabishy, MD, West Bloomfield, Mich
Satoshi Tatsuno, MD, Ichikawa, Chiba, Japan Douglas L. Teich, MD, Brookline, Mass Yasuyo Teramura, MD, Tokorozawa, Saitama, Japan Christina Theoret, MD, Saskatoon, Saskatchewan, Canada Eugene Tong, MD, Austin, Tex Ulysses S. Torres, MD, Sao Paulo, Brazil Meric Tuzun, MD, Ankara, Turkey Atsushi Uehara, Niigata, Japan Piet K. Vanhoenacker, MD, Moorsel, Belgium Alexander Vidershayn, MD, Brooklyn, NY Joao Carlos C. Vilhena, MD, Sao Paulo, Brazil Pier Carlo Villani, MD, Bari, Italy Ainhoa Viteri, MD, Bilbao, Biscay, Spain Christopher P. Vittore, MD, Belvidere, Ill Lynne Voutsinas, MD, Staten Island, NY Garrett L. Walworth, MD, Milford, Mich Haruo Watanabe, MD, Gifu, Japan Hsu-Huei Weng, MD, PhD, Chia-Yi County, Taiwan Jeffrey H. West, MD, Jacksonville, Fla Noritaka Yamakawa, Kyoto, Japan Tatsuya Yamamoto, MD, Yoshida-gun, Fukui, Japan Toshihide Yamaoka, MD, Kyoto, Japan Koji Yamashita, MD, PhD, Fukuoka, Japan Koichiro Yasaka, MD, Tokyo, Japan Kurata Yasuhisa, MD, Kobe, Hyogo, Japan Hajime Yokota, MD, Chiba, Japan Rika Yoshida, MD, Utsunomiya, Tochigi, Japan Satoru Yoshida, MD, PhD, Muroran, Hokkaido, Japan Kaneko You, Gifu, Japan Carlos A. Zamora, MD, PhD, Lutherville, Md Yi Cheng Zhou, MD, Wuhan, Hub, China Ahmed Zidan, MD, Barcelona, Spain
Resident group responses ICESP Residents, Sao Paulo, Brazil Mater Dei Hospital Radiology Residents, Malta Mie University Hospital Radiology Residents, MD, Tsu, Mie, Japan Prince of Songkla University Radiology Residents, Songkla, Thailand Thomas Jefferson University Radiology Residents, Philadelphia, Pa Tsukuba University Hospital Radiology Residents, Tsukuba, Ibaraki, Japan University of Pennsylvania Radiology Residents, Philadelphia, Pa UTHSC at San Antonio Radiology Residents, MD, San Antonio, Tex University of Washington Radiology Residents, MD, Seattle, Wash Virginia Commonwealth University Radiology Residents, Richmond, Va Yale University Radiology Residents, New Haven, Conn
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