18F-FDG-PET glucose hypometabolism pattern in patients with epileptogenic hypothalamic hamartoma

Chao Lu, Kailiang Wang, Fei Meng, Yihe Wang, Yongzhi Shan, Penghu Wei, Guoguang Zhao

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Front. Med. ›› 2021, Vol. 15 ›› Issue (6) : 913-921. DOI: 10.1007/s11684-021-0874-1
RESEARCH ARTICLE

18F-FDG-PET glucose hypometabolism pattern in patients with epileptogenic hypothalamic hamartoma

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Abstract

Epileptogenic hypothalamic hamartoma is characterized by intractable gelastic seizures. A systematic analysis of the overall brain metabolic pattern in patients with hypothalamic hamartoma (HH) could facilitate the understanding of the epileptic brain network and the associated brain damage effects of HH. In this study, we retrospectively evaluated 27 patients with epileptogenic HH (8 female patients; age, 2–33 years) by using 18F-fluorodeoxyglucose-positron emission tomography. The correlations among tomography result, seizure type, sex, and structural magnetic resonance imaging were assessed. Whole metabolic patterns and voxel-based morphometry findings were assessed by group analysis with healthy controls. Assessment of the whole metabolic pattern in patients with HH revealed several regional metabolic reductions in the cerebrum and an overall metabolic reduction in the cerebellum. In addition, areas showing hypometabolism in the neocortex were more widely distributed ipsilaterally than contralaterally to the HH. Reductions in glucose metabolism and gray matter volume in the neocortex were predominant ipsilateral to the HH. In conclusion, the glucose hypometabolism pattern in patients with epileptogenic HH involved the neocortex, subcortical regions, and cerebellum. The characteristics of glucose hypometabolism differed across seizure type and sex. Reductions in glucose metabolism and structural changes may be based on different mechanisms, but both are likely to occur ipsilateral to the HH in the neocortex. We hypothesized that the dentato-rubro-thalamic tract and cerebro-ponto-cerebellar tract, which are responsible for intercommunication between the cerebral cortex, subcortical regions, and cerebellar regions, may be involved in a pathway related to seizure propagation, particularly gelastic seizures, in patients with HH.

Keywords

hypothalamic hamartoma / gelastic seizure / fluorodeoxyglucose-positron emission tomography / voxel-based morphometry

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Chao Lu, Kailiang Wang, Fei Meng, Yihe Wang, Yongzhi Shan, Penghu Wei, Guoguang Zhao. 18F-FDG-PET glucose hypometabolism pattern in patients with epileptogenic hypothalamic hamartoma. Front. Med., 2021, 15(6): 913‒921 https://doi.org/10.1007/s11684-021-0874-1

References

[1]
Wagner K, Schulze-Bonhage A, Urbach H, Trippel M, Spehl TS, Buschmann F, Metternich B, Ofer I, Meyer PT, Frings L. Reduced glucose metabolism in neocortical network nodes remote from hypothalamic hamartomas reflects cognitive impairment. Epilepsia 2017; 58(Suppl 2): 41–49
CrossRef Pubmed Google scholar
[2]
Breningstall GN. Gelastic seizures, precocious puberty, and hypothalamic hamartoma. Neurology 1985; 35(8): 1180–1183
CrossRef Pubmed Google scholar
[3]
Wang D, Shan Y, Bartolomei F, Kahane P, An Y, Li M, Zhang H, Fan X, Ou S, Yang Y, Wei P, Lu C, Wang Y, Du J, Ren L, Wang Y, Zhao G. Electrophysiological properties and seizure networks in hypothalamic hamartoma. Ann Clin Transl Neurol 2020; 7(5): 653–666
CrossRef Pubmed Google scholar
[4]
Kahane P, Ryvlin P, Hoffmann D, Minotti L, Benabid AL. From hypothalamic hamartoma to cortex: what can be learnt from depth recordings and stimulation? Epileptic Disord 2003; 5(4): 205–217
Pubmed
[5]
Wu J, Xu L, Kim DY, Rho JM, St John PA, Lue LF, Coons S, Ellsworth K, Nowak L, Johnson E, Rekate H, Kerrigan JF. Electrophysiological properties of human hypothalamic hamartomas. Ann Neurol 2005; 58(3): 371–382
CrossRef Pubmed Google scholar
[6]
Mueller SG, Laxer KD, Cashdollar N, Buckley S, Paul C, Weiner MW. Voxel-based optimized morphometry (VBM) of gray and white matter in temporal lobe epilepsy (TLE) with and without mesial temporal sclerosis. Epilepsia 2006; 47(5): 900–907
CrossRef Pubmed Google scholar
[7]
Barron DS, Fox PM, Laird AR, Robinson JL, Fox PT. Thalamic medial dorsal nucleus atrophy in medial temporal lobe epilepsy: a VBM meta-analysis. Neuroimage Clin 2013; 2: 25–32
CrossRef Pubmed Google scholar
[8]
Labate A, Cerasa A, Gambardella A, Aguglia U, Quattrone A. Hippocampal and thalamic atrophy in mild temporal lobe epilepsy: a VBM study. Neurology 2008; 71(14): 1094–1101
CrossRef Pubmed Google scholar
[9]
Ponisio MR, Zempel JM, Day BK, Eisenman LN, Miller-Thomas MM, Smyth MD, Hogan RE. The role of SPECT and PET in epilepsy. AJR Am J Roentgenol 2021; 216(3): 759–768
CrossRef Pubmed Google scholar
[10]
Shang K, Wang J, Fan X, Cui B, Ma J, Yang H, Zhou Y, Zhao G, Lu J. Clinical value of hybrid TOF-PET/MR imaging-based multiparametric imaging in localizing seizure focus in patients with MRI-negative temporal lobe epilepsy. AJNR Am J Neuroradiol 2018; 39(10): 1791–1798
CrossRef Pubmed Google scholar
[11]
Vickery S, Hopkins WD, Sherwood CC, Schapiro SJ, Latzman RD, Caspers S, Gaser C, Eickhoff SB, Dahnke R, Hoffstaedter F. Chimpanzee brain morphometry utilizing standardized MRI preprocessing and macroanatomical annotations. eLife 2020; 9: e60136
CrossRef Pubmed Google scholar
[12]
Lamarche F, Job AS, Deman P, Bhattacharjee M, Hoffmann D, Gallazzini-Crépin C, Bouvard S, Minotti L, Kahane P, David O. Correlation of FDG-PET hypometabolism and SEEG epileptogenicity mapping in patients with drug-resistant focal epilepsy. Epilepsia 2016; 57(12): 2045–2055
CrossRef Pubmed Google scholar
[13]
Lagarde S, Boucekine M, McGonigal A, Carron R, Scavarda D, Trebuchon A, Milh M, Boyer L, Bartolomei F, Guedj E. Relationship between PET metabolism and SEEG epileptogenicity in focal lesional epilepsy. 2020; 47: 3130–3142
CrossRef Google scholar
[14]
Wei PH, An Y, Fan XT, Wang YH, Yang YF, Ren LK, Shan YZ, Zhao GG. Stereoelectroencephalography-guided radiofrequency thermocoagulation for hypothalamic hamartomas: preliminary evidence. World Neurosurg 2018; 114: e1073–e1078
CrossRef Pubmed Google scholar
[15]
Fenoglio KA, Wu J, Kim DY, Simeone TA, Coons SW, Rekate H, Rho JM, Kerrigan JF. Hypothalamic hamartoma: basic mechanisms of intrinsic epileptogenesis. Semin Pediatr Neurol 2007; 14(2): 51–59
CrossRef Pubmed Google scholar
[16]
Wang D, Shan Y, Bartolomei F, Kahane P, An Y, Li M, Zhang H, Fan X, Ou S, Yang Y, Wei P, Lu C, Wang Y, Du J, Ren L, Wang Y, Zhao G. Electrophysiological properties and seizure networks in hypothalamic hamartoma. Ann Clin Transl Neurol 2020; 7(5): 653–666
CrossRef Pubmed Google scholar
[17]
Ryvlin P, Ravier C, Bouvard S, Mauguire F, Le Bars D, Arzimanoglou A, Petit J, Kahane P. Positron emission tomography in epileptogenic hypothalamic hamartomas. Epileptic Disord 2003; 5(4): 219–227
Pubmed
[18]
Yang YF, Wei PH, Meng F, An Y, Fan XT, Wang YH, Wang D, Ren LK, Shan YZ, Zhao GG. Glucose metabolism characteristics of extra-hypothalamic cortex in patients with hypothalamic hamartomas (HH) undergoing epilepsy evaluation: a retrospective study of 16 cases. Front Neurol 2021; 11: 587622
CrossRef Pubmed Google scholar
[19]
McCormick C, Protzner AB, Barnett AJ, Cohn M, Valiante TA, McAndrews MP. Linking DMN connectivity to episodic memory capacity: what can we learn from patients with medial temporal lobe damage? Neuroimage Clin 2014; 5: 188–196
CrossRef Pubmed Google scholar
[20]
Hu CY, Gao X, Long L, Long X, Liu C, Chen Y, Xie Y, Liu C, Xiao B, Hu ZY. Altered DMN functional connectivity and regional homogeneity in partial epilepsy patients: a seventy cases study. Oncotarget 2017; 8(46): 81475–81484
CrossRef Pubmed Google scholar
[21]
Mohan A, Roberto AJ, Mohan A, Lorenzo A, Jones K, Carney MJ, Liogier-Weyback L, Hwang S, Lapidus KAB. The significance of the default mode network (DMN) in neurological and neuropsychiatric disorders: a review. Yale J Biol Med 2016; 89(1): 49–57
Pubmed
[22]
Wang KL, Hu W, Liu TH, Zhao XB, Han CL, Xia XT, Zhang JG, Wang F, Meng FG. Metabolic covariance networks combining graph theory measuring aberrant topological patterns in mesial temporal lobe epilepsy. CNS Neurosci Ther 2019; 25(3): 396–408
CrossRef Pubmed Google scholar
[23]
Chassoux F, Artiges E, Semah F, Desarnaud S, Laurent A, Landré E, Gervais P, Devaux B, Helal OB. Determinants of brain metabolism changes in mesial temporal lobe epilepsy. Epilepsia 2016; 57(6): 907–919
CrossRef Pubmed Google scholar
[24]
Iannetti P, Spalice A, Raucci U, Atzei G, Cipriani C. Gelastic epilepsy: video-EEG, MRI and SPECT characteristics. Brain Dev 1997; 19(6): 418–421
CrossRef Pubmed Google scholar
[25]
Usami K, Matsumoto R, Sawamoto N, Murakami H, Inouchi M, Fumuro T, Shimotake A, Kato T, Mima T, Shirozu H, Masuda H, Fukuyama H, Takahashi R, Kameyama S, Ikeda A. Epileptic network of hypothalamic hamartoma: an EEG-fMRI study. Epilepsy Res 2016; 125: 1–9
CrossRef Pubmed Google scholar
[26]
Parvizi J, Anderson SW, Martin CO, Damasio H, Damasio AR. Pathological laughter and crying: a link to the cerebellum. Brain 2001; 124(9): 1708–1719
CrossRef Pubmed Google scholar
[27]
Elyas AE, Bulters DO, Sparrow OC. Pathological laughter and crying in patients with pontine lesions. J Neurosurg Pediatr 2011; 8(6): 544–547
CrossRef Pubmed Google scholar
[28]
Zhang L, Cao B, Wei QQ, Ou R, Zhao B, Yang J, Wu Y, Shang H. Pathological laughter and crying in multiple system atrophy with different subtypes: frequency and related factors. J Affect Disord 2021; 283: 60–65
CrossRef Pubmed Google scholar
[29]
Striano S, Striano P. Clinical features and evolution of the gelastic seizures-hypothalamic hamartoma syndrome. Epilepsia 2017; 58(Suppl 2): 12–15
CrossRef Pubmed Google scholar
[30]
Savic I, Engel J Jr. Structural and functional correlates of epileptogenesis—does gender matter? Neurobiol Dis 2014; 70: 69–73
CrossRef Pubmed Google scholar
[31]
Chételat G, Landeau B, Eustache F, Mézenge F, Viader F, de la Sayette V, Desgranges B, Baron JC. Using voxel-based morphometry to map the structural changes associated with rapid conversion in MCI: a longitudinal MRI study. Neuroimage 2005; 27(4): 934–946
CrossRef Pubmed Google scholar
[32]
Losey TE, Beeman SC, Ng YT, Kerrigan JF, Baxter LC. White matter density is increased in patients with hypothalamic hamartoma and multiple seizure types. Epilepsy Res 2011; 93(2–3): 212–215
CrossRef Pubmed Google scholar

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 81801288, 81871009, and 82030037)

Compliance with ethics guidelines

Chao Lu, Kailiang Wang, Fei Meng, Yihe Wang, Yongzhi Shan, Penghu Wei, and Guoguang Zhao declare that they have no conflicts of interest. All procedures were conducted in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000 (5). Informed consent was obtained from all patients for inclusion in the study.

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