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Published in: European Journal of Nuclear Medicine and Molecular Imaging 2/2012

01-02-2012 | Original Article

Brain hypermetabolism in amyotrophic lateral sclerosis: a FDG PET study in ALS of spinal and bulbar onset

Authors: Angelina Cistaro, Maria Consuelo Valentini, Adriano Chiò, Flavio Nobili, Andrea Calvo, Cristina Moglia, Anna Montuschi, Silvia Morbelli, Dario Salmaso, Piercarlo Fania, Giovanna Carrara, Marco Pagani

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 2/2012

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Abstract

Purpose

To identify the neurobiological traits of amyotrophic lateral sclerosis (ALS) and to elucidate functional differences between ALS of spinal and bulbar onset. We hypothesized that glucose metabolism distribution might vary between groups.

Methods

The study groups comprised 32 patients with ALS of either bulbar (n = 13) or spinal (n = 19) onset and 22 subjects as controls. They were investigated by [18F]fluorodeoxyglucose (FDG) positron emission tomography (FDG PET), comparing the patient groups with each other and with the controls by statistical parametric mapping.

Results

Highly significant relative increases in glucose metabolism distribution were found in the group comprising all 32 ALS patients as compared with the controls in the bilateral amygdalae, midbrain, pons and cerebellum. Relative hypermetabolism was also found in patients with spinal onset as compared with the controls in the right midbrain. In patients with bulbar onset compared with the controls and with patients with spinal onset, large relatively hypometabolic areas were found in the bilateral frontal cortex, right insula, anterior cingulate, precuneus and inferior parietal lobe. Patients with spinal onset had significantly higher scores in a neuropsychological test assessing verbal fluency compared with patients with bulbar onset.

Conclusion

This large FDG PET investigation provided unprecedented evidence of relatively increased metabolism in the amygdalae, midbrain and pons in ALS patients as compared with control subjects, possibly due to local activation of astrocytes and microglia. Highly significant relative decreases in metabolism were found in large frontal and parietal regions in the bulbar onset patients as compared with the spinal onset patients and the controls, suggesting a differential metabolic and neuropsychological state between the two conditions.
Literature
1.
go back to reference Brooks BR, Miller RG, Swash M, Munsat TL. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2000;1:293–9.PubMedCrossRef Brooks BR, Miller RG, Swash M, Munsat TL. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2000;1:293–9.PubMedCrossRef
2.
go back to reference Chiò A, Mora G, Calvo A, Mazzini L, Bottacchi E, Mutani R, et al. Epidemiology of ALS in Italy: a 10-year prospective population-based study. Neurology. 2009;72:725–31.PubMedCrossRef Chiò A, Mora G, Calvo A, Mazzini L, Bottacchi E, Mutani R, et al. Epidemiology of ALS in Italy: a 10-year prospective population-based study. Neurology. 2009;72:725–31.PubMedCrossRef
3.
go back to reference Leigh PN, Kew JJM, Goldstein LH, Brooks DJ. The cerebral lesions in amyotrophic lateral sclerosis: new insights from pathology and functional brain imaging. In: Rose C, editor. Amyotrophic lateral sclerosis from Charcot to the present and into the future. London: Smith-Gordon; 1994. p. 191–209. Leigh PN, Kew JJM, Goldstein LH, Brooks DJ. The cerebral lesions in amyotrophic lateral sclerosis: new insights from pathology and functional brain imaging. In: Rose C, editor. Amyotrophic lateral sclerosis from Charcot to the present and into the future. London: Smith-Gordon; 1994. p. 191–209.
4.
go back to reference Talbot PR, Goulding PJ, Lloyd JJ, Snowden JS, Neary D, Testa HJ. Inter-relation between ‘classic’ motor neuron disease and frontotemporal dementia: neuropsychological and single photon emission computed tomography study. J Neurol Neurosurg Psychiatry. 1995;58:541–7.PubMedCrossRef Talbot PR, Goulding PJ, Lloyd JJ, Snowden JS, Neary D, Testa HJ. Inter-relation between ‘classic’ motor neuron disease and frontotemporal dementia: neuropsychological and single photon emission computed tomography study. J Neurol Neurosurg Psychiatry. 1995;58:541–7.PubMedCrossRef
5.
go back to reference Geser F, Brandmeir NJ, Kwong LK, Martinez-Lage M, Elman L, McCluskey L, et al. Evidence of multisystem disorder in whole-brain map of pathological TDP-43 in amyotrophic lateral sclerosis. Arch Neurol. 2008;65:636–41.PubMedCrossRef Geser F, Brandmeir NJ, Kwong LK, Martinez-Lage M, Elman L, McCluskey L, et al. Evidence of multisystem disorder in whole-brain map of pathological TDP-43 in amyotrophic lateral sclerosis. Arch Neurol. 2008;65:636–41.PubMedCrossRef
6.
go back to reference Gallassi R, Montagna P, Morreale A, Lorusso S, Tinuper P, Daidone R, et al. Neuropsychological, electroencephalogram and brain computed tomography findings in motor neuron disease. Eur Neurol. 1989;29:115–20.PubMedCrossRef Gallassi R, Montagna P, Morreale A, Lorusso S, Tinuper P, Daidone R, et al. Neuropsychological, electroencephalogram and brain computed tomography findings in motor neuron disease. Eur Neurol. 1989;29:115–20.PubMedCrossRef
7.
go back to reference Ludolph AC, Langen KJ, Regard M, Herzog H, Kemper B, Kuwert T, et al. Frontal lobe function in amyotrophic lateral sclerosis: a neuropsychologic and positron emission tomography study. Acta Neurol Scand. 1992;85:81–9.PubMedCrossRef Ludolph AC, Langen KJ, Regard M, Herzog H, Kemper B, Kuwert T, et al. Frontal lobe function in amyotrophic lateral sclerosis: a neuropsychologic and positron emission tomography study. Acta Neurol Scand. 1992;85:81–9.PubMedCrossRef
8.
go back to reference Iwasaki Y, Kinoshita M, Oceda K, Takamiya K, Shiojima T. Cognitive impairment in amyotrophic lateral sclerosis and its relation to motor disabilities. Acta Neurol Scand. 1990;81:141–3.PubMedCrossRef Iwasaki Y, Kinoshita M, Oceda K, Takamiya K, Shiojima T. Cognitive impairment in amyotrophic lateral sclerosis and its relation to motor disabilities. Acta Neurol Scand. 1990;81:141–3.PubMedCrossRef
9.
go back to reference Kew JJM, Goldstein LH, Leigh PN, Abrahams S, Cosgrave N, Passingham RE, et al. The relationship between abnormalities of cognitive function and cerebral activation in amyotrophic lateral sclerosis. A neuropsychological and positron emission tomography study. Brain. 1993;116:1399–423.PubMedCrossRef Kew JJM, Goldstein LH, Leigh PN, Abrahams S, Cosgrave N, Passingham RE, et al. The relationship between abnormalities of cognitive function and cerebral activation in amyotrophic lateral sclerosis. A neuropsychological and positron emission tomography study. Brain. 1993;116:1399–423.PubMedCrossRef
10.
go back to reference Abrahams S, Leigh PN, Kew JJ, Goldstein LH, Lloyd CM, Brooks DJ. A positron emission tomography study of frontal lobe function (verbal fluency) in amyotrophic lateral sclerosis. J Neurol Sci. 1995;129(Suppl):44–6.PubMedCrossRef Abrahams S, Leigh PN, Kew JJ, Goldstein LH, Lloyd CM, Brooks DJ. A positron emission tomography study of frontal lobe function (verbal fluency) in amyotrophic lateral sclerosis. J Neurol Sci. 1995;129(Suppl):44–6.PubMedCrossRef
11.
go back to reference Abe K, Fujimura H, Toyooka K, Sakoda S, Yorifuji S, Yanagihara T. Cognitive function in amyotrophic lateral sclerosis. J Neurol Sci. 1997;148:95–100.PubMedCrossRef Abe K, Fujimura H, Toyooka K, Sakoda S, Yorifuji S, Yanagihara T. Cognitive function in amyotrophic lateral sclerosis. J Neurol Sci. 1997;148:95–100.PubMedCrossRef
12.
go back to reference Abrahams S, Goldstein LH, Suckling J, Ng V, Simmons A, Chitnis X, et al. Frontotemporal white matter changes in amyotrophic lateral sclerosis. J Neurol. 2005;252:321–31.PubMedCrossRef Abrahams S, Goldstein LH, Suckling J, Ng V, Simmons A, Chitnis X, et al. Frontotemporal white matter changes in amyotrophic lateral sclerosis. J Neurol. 2005;252:321–31.PubMedCrossRef
13.
go back to reference Andreadou E, Sgouropoulos P, Varelas P, Gouliamos A, Papageorgiou C. Subcortical frontal lesions on MRI in patients with motor neurone disease. Neuroradiology. 1998;40:298–302.PubMedCrossRef Andreadou E, Sgouropoulos P, Varelas P, Gouliamos A, Papageorgiou C. Subcortical frontal lesions on MRI in patients with motor neurone disease. Neuroradiology. 1998;40:298–302.PubMedCrossRef
14.
go back to reference Kato S, Hayashi H, Yagishita A. Involvement of the frontotemporal lobe and limbic system in amyotrophic lateral sclerosis: as assessed by serial computed tomography and magnetic resonance imaging. J Neurol Sci. 1993;116:52–8.PubMedCrossRef Kato S, Hayashi H, Yagishita A. Involvement of the frontotemporal lobe and limbic system in amyotrophic lateral sclerosis: as assessed by serial computed tomography and magnetic resonance imaging. J Neurol Sci. 1993;116:52–8.PubMedCrossRef
15.
go back to reference Peavy GM, Herzog AG, Rubin NP, Mesulam M-M. Neuropsychological aspects of dementia of motor neuron disease: a report of two cases. Neurology. 1992;42:1004–8.PubMed Peavy GM, Herzog AG, Rubin NP, Mesulam M-M. Neuropsychological aspects of dementia of motor neuron disease: a report of two cases. Neurology. 1992;42:1004–8.PubMed
16.
go back to reference Hudson AJ. Amyotrophic lateral sclerosis and its association with dementia, parkinsonism and other neurological disorders: a review. Brain. 1981;104:217–47.PubMedCrossRef Hudson AJ. Amyotrophic lateral sclerosis and its association with dementia, parkinsonism and other neurological disorders: a review. Brain. 1981;104:217–47.PubMedCrossRef
17.
go back to reference Dalakas MC, Hatazawa J, Brooks RA, Di Chiro G. Lowered cerebral glucose utilization in amyotrophic lateral sclerosis. Ann Neurol. 1987;22:580–6.PubMedCrossRef Dalakas MC, Hatazawa J, Brooks RA, Di Chiro G. Lowered cerebral glucose utilization in amyotrophic lateral sclerosis. Ann Neurol. 1987;22:580–6.PubMedCrossRef
18.
go back to reference Hatazawa J, Brooks RA, Dalakas MC, Mansi L, Di Ghiro G. Cortical moto-sensory hypometabolism in amyotrophic lateral sclerosis: a PET study. J Comput Assist Tomogr. 1988;12:630–6.PubMedCrossRef Hatazawa J, Brooks RA, Dalakas MC, Mansi L, Di Ghiro G. Cortical moto-sensory hypometabolism in amyotrophic lateral sclerosis: a PET study. J Comput Assist Tomogr. 1988;12:630–6.PubMedCrossRef
19.
go back to reference Le Forestier N, Maisonobe T, Spelle L, Lesort A, Salachas F, Lacomblez L, et al. Primary lateral sclerosis: further clarification. J Neurol Sci. 2001;185:95–100.PubMedCrossRef Le Forestier N, Maisonobe T, Spelle L, Lesort A, Salachas F, Lacomblez L, et al. Primary lateral sclerosis: further clarification. J Neurol Sci. 2001;185:95–100.PubMedCrossRef
20.
go back to reference Turner MR, Hammers A, Al-Chalabi A, Shaw CE, Andersen PM, Brooks DJ, et al. Cortical involvement in four cases of primary lateral sclerosis using [(11)C]-flumazenil PET. J Neurol. 2007;254:1033–6.PubMedCrossRef Turner MR, Hammers A, Al-Chalabi A, Shaw CE, Andersen PM, Brooks DJ, et al. Cortical involvement in four cases of primary lateral sclerosis using [(11)C]-flumazenil PET. J Neurol. 2007;254:1033–6.PubMedCrossRef
21.
go back to reference Claassen DO, Josephs KA, Peller PJ. The stripe of primary lateral sclerosis: focal primary motor cortex hypometabolism seen on fluorodeoxyglucose F18 positron emission tomography. Arch Neurol. 2010;67:122–5.PubMedCrossRef Claassen DO, Josephs KA, Peller PJ. The stripe of primary lateral sclerosis: focal primary motor cortex hypometabolism seen on fluorodeoxyglucose F18 positron emission tomography. Arch Neurol. 2010;67:122–5.PubMedCrossRef
22.
go back to reference Strong MJ, Grace GM, Freedman M, Lomen-Hoerth C, Woolley S, Goldstein LH, et al. Consensus criteria for the diagnosis of frontotemporal cognitive and behavioral syndromes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2009;10:131–46.CrossRef Strong MJ, Grace GM, Freedman M, Lomen-Hoerth C, Woolley S, Goldstein LH, et al. Consensus criteria for the diagnosis of frontotemporal cognitive and behavioral syndromes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2009;10:131–46.CrossRef
23.
go back to reference Bennett CM, Wolford GL, Miller MB. The principled control of false positives in neuroimaging. Soc Cogn Affect Neurosci. 2009;4:417–22.PubMedCrossRef Bennett CM, Wolford GL, Miller MB. The principled control of false positives in neuroimaging. Soc Cogn Affect Neurosci. 2009;4:417–22.PubMedCrossRef
24.
go back to reference Yatham LN, Liddle PF, Lam RW, Zis AP, Stoessl AJ, Sossi V, et al. Effect of electroconvulsive therapy on brain 5-HT2 receptors in major depression. Br J Psychiatry. 2010;196:474–9.PubMedCrossRef Yatham LN, Liddle PF, Lam RW, Zis AP, Stoessl AJ, Sossi V, et al. Effect of electroconvulsive therapy on brain 5-HT2 receptors in major depression. Br J Psychiatry. 2010;196:474–9.PubMedCrossRef
25.
go back to reference Lloyd CM, Richardson MP, Brooks DJ, Al-Chalabi A, Leigh PN. Extramotor involvement in ALS: PET studies with the GABA(A) ligand [(11)C]flumazenil. Brain. 2000;123:2289–96.PubMedCrossRef Lloyd CM, Richardson MP, Brooks DJ, Al-Chalabi A, Leigh PN. Extramotor involvement in ALS: PET studies with the GABA(A) ligand [(11)C]flumazenil. Brain. 2000;123:2289–96.PubMedCrossRef
26.
go back to reference Turner BJ, Lopes EC, Cheema SS. The serotonin precursor 5-hydroxytryptophan delays neuromuscular disease in murine familial amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2003;4:171–6.PubMedCrossRef Turner BJ, Lopes EC, Cheema SS. The serotonin precursor 5-hydroxytryptophan delays neuromuscular disease in murine familial amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2003;4:171–6.PubMedCrossRef
27.
go back to reference Aquilonius SM, Jossan SS, Ekblom JG, Askmark H, Gillberg PG. Increased binding of 3H-L-deprenyl in spinal cords from patients with amyotrophic lateral sclerosis as demonstrated by autoradiography. J Neural Transm Gen Sect. 1992;89:111–22.PubMedCrossRef Aquilonius SM, Jossan SS, Ekblom JG, Askmark H, Gillberg PG. Increased binding of 3H-L-deprenyl in spinal cords from patients with amyotrophic lateral sclerosis as demonstrated by autoradiography. J Neural Transm Gen Sect. 1992;89:111–22.PubMedCrossRef
28.
go back to reference Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, Gutmann DH, et al. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci. 2008;11:251–3.PubMedCrossRef Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, Gutmann DH, et al. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci. 2008;11:251–3.PubMedCrossRef
29.
go back to reference Yu I, Inaji M, Maeda J, Okauchi T, Nariai T, Ohno T, et al. Glial cell-mediated deterioration and repair of the nervous system after traumatic brain injury in a rat model as assessed by positron emission tomography. J Neurotrauma. 2010;27:1463–75.PubMedCrossRef Yu I, Inaji M, Maeda J, Okauchi T, Nariai T, Ohno T, et al. Glial cell-mediated deterioration and repair of the nervous system after traumatic brain injury in a rat model as assessed by positron emission tomography. J Neurotrauma. 2010;27:1463–75.PubMedCrossRef
30.
go back to reference Marik J, Ogasawara A, Martin-McNulty B, Ross J, Flores JE, Gill HS, et al. PET of glial metabolism using 2-18F-fluoroacetate. J Nucl Med. 2009;50:982–90.PubMedCrossRef Marik J, Ogasawara A, Martin-McNulty B, Ross J, Flores JE, Gill HS, et al. PET of glial metabolism using 2-18F-fluoroacetate. J Nucl Med. 2009;50:982–90.PubMedCrossRef
31.
go back to reference Yokokura M, Mori N, Yagi S, Yoshikawa E, Kikuchi M, Yoshihara Y, et al. In vivo changes in microglial activation and amyloid deposits in brain regions with hypometabolism in Alzheimer’s disease. Eur J Nucl Med Mol Imaging. 2011;38:343–51.PubMedCrossRef Yokokura M, Mori N, Yagi S, Yoshikawa E, Kikuchi M, Yoshihara Y, et al. In vivo changes in microglial activation and amyloid deposits in brain regions with hypometabolism in Alzheimer’s disease. Eur J Nucl Med Mol Imaging. 2011;38:343–51.PubMedCrossRef
32.
go back to reference Fukumoto D, Hosoya T, Nishiyama S, Harada N, Iwata H, Yamamoto S, et al. Multiparametric assessment of acute and subacute ischemic neuronal damage: a small animal positron emission tomography study with rat photochemically induced thrombosis model. Synapse. 2011;65:207–14.PubMedCrossRef Fukumoto D, Hosoya T, Nishiyama S, Harada N, Iwata H, Yamamoto S, et al. Multiparametric assessment of acute and subacute ischemic neuronal damage: a small animal positron emission tomography study with rat photochemically induced thrombosis model. Synapse. 2011;65:207–14.PubMedCrossRef
33.
go back to reference Barros LF, Porras OH, Bittner CX. Why glucose transport in the brain matters for PET. Trends Neurosci. 2005;28:117–9.PubMedCrossRef Barros LF, Porras OH, Bittner CX. Why glucose transport in the brain matters for PET. Trends Neurosci. 2005;28:117–9.PubMedCrossRef
34.
go back to reference Magistretti PJ. Cellular bases of functional brain imaging: insights from neuron-glia metabolic coupling. Brain Res. 2000;886:108–12.PubMedCrossRef Magistretti PJ. Cellular bases of functional brain imaging: insights from neuron-glia metabolic coupling. Brain Res. 2000;886:108–12.PubMedCrossRef
35.
go back to reference Nehlig A, Coles J. Cellular pathways of energy metabolism in the brain: is glucose used by neurons or astrocytes? Glia. 2007;55:1238–50.PubMedCrossRef Nehlig A, Coles J. Cellular pathways of energy metabolism in the brain: is glucose used by neurons or astrocytes? Glia. 2007;55:1238–50.PubMedCrossRef
36.
go back to reference Abe K, Fujimura H, Toyooka K, Hazama T, Hirono N, Yorifuji S, et al. Single-photon emission computed tomographic investigation of patients with motor neuron disease. Neurology. 1993;43:1569–73.PubMed Abe K, Fujimura H, Toyooka K, Hazama T, Hirono N, Yorifuji S, et al. Single-photon emission computed tomographic investigation of patients with motor neuron disease. Neurology. 1993;43:1569–73.PubMed
37.
go back to reference Abrahams S, Leigh PN, Harvey A, Vythelingum GN, Grise D, Goldstein LH. Verbal fluency and executive dysfunction in amyotrophic lateral sclerosis (ALS). Neuropsychologia. 2000;38:734–47.PubMedCrossRef Abrahams S, Leigh PN, Harvey A, Vythelingum GN, Grise D, Goldstein LH. Verbal fluency and executive dysfunction in amyotrophic lateral sclerosis (ALS). Neuropsychologia. 2000;38:734–47.PubMedCrossRef
38.
go back to reference Abrahams S, Goldstein LH, Kew JJM, Brooks DJ, Lloyd CM, Frith CD, et al. Frontal lobe dysfunction in amyotrophic lateral sclerosis. A PET study. Brain. 1996;119:2105–20.PubMedCrossRef Abrahams S, Goldstein LH, Kew JJM, Brooks DJ, Lloyd CM, Frith CD, et al. Frontal lobe dysfunction in amyotrophic lateral sclerosis. A PET study. Brain. 1996;119:2105–20.PubMedCrossRef
39.
go back to reference Abrahams S, Goldstein LH, Al-Chalabi A, Pickering A, Morris RG, Passingham RE, et al. Relation between cognitive dysfunction and pseudobulbar palsy in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 1997;62:464–72.PubMedCrossRef Abrahams S, Goldstein LH, Al-Chalabi A, Pickering A, Morris RG, Passingham RE, et al. Relation between cognitive dysfunction and pseudobulbar palsy in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 1997;62:464–72.PubMedCrossRef
40.
go back to reference Pagani M, Dessi B, Morbelli S, Brugnolo A, Salmaso D, Piccini A, et al. MCI patients declining and not-declining at mid-term follow-up: FDG-PET findings. Curr Alzheimer Res. 2010;7:287–94.PubMedCrossRef Pagani M, Dessi B, Morbelli S, Brugnolo A, Salmaso D, Piccini A, et al. MCI patients declining and not-declining at mid-term follow-up: FDG-PET findings. Curr Alzheimer Res. 2010;7:287–94.PubMedCrossRef
41.
go back to reference Nobili F, Mazzei D, Dessi B, Morbelli S, Brugnolo A, Barbieri P, et al. Unawareness of memory deficit in amnestic MCI: FDG-PET findings. J Alzheimers Dis. 2010;22:993–1003.PubMed Nobili F, Mazzei D, Dessi B, Morbelli S, Brugnolo A, Barbieri P, et al. Unawareness of memory deficit in amnestic MCI: FDG-PET findings. J Alzheimers Dis. 2010;22:993–1003.PubMed
42.
go back to reference Del Sole A, Clerici F, Chiti A, Lecchi M, Mariani C, Maggiore L, et al. Individual cerebral metabolic deficits in Alzheimer’s disease and amnestic mild cognitive impairment: an FDG PET study. Eur J Nucl Med Mol Imaging. 2008;35:1357–66.PubMedCrossRef Del Sole A, Clerici F, Chiti A, Lecchi M, Mariani C, Maggiore L, et al. Individual cerebral metabolic deficits in Alzheimer’s disease and amnestic mild cognitive impairment: an FDG PET study. Eur J Nucl Med Mol Imaging. 2008;35:1357–66.PubMedCrossRef
43.
go back to reference Borghammer P, Cumming P, Aanerud J, Gjedde A. Artefactual subcortical hyperperfusion in PET studies normalized to global mean: lessons from Parkinson’s disease. Neuroimage. 2009;45:249–57.PubMedCrossRef Borghammer P, Cumming P, Aanerud J, Gjedde A. Artefactual subcortical hyperperfusion in PET studies normalized to global mean: lessons from Parkinson’s disease. Neuroimage. 2009;45:249–57.PubMedCrossRef
Metadata
Title
Brain hypermetabolism in amyotrophic lateral sclerosis: a FDG PET study in ALS of spinal and bulbar onset
Authors
Angelina Cistaro
Maria Consuelo Valentini
Adriano Chiò
Flavio Nobili
Andrea Calvo
Cristina Moglia
Anna Montuschi
Silvia Morbelli
Dario Salmaso
Piercarlo Fania
Giovanna Carrara
Marco Pagani
Publication date
01-02-2012
Publisher
Springer-Verlag
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 2/2012
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-011-1979-6

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