Brain glucose metabolism and gray matter volume in retired professional soccer players: a cross-sectional [<sup>18</sup>F]FDG-PET/MRI study

Aranha, Mateus Rozalem; Coutinho, Artur Martins; Carneiro, Camila de Godoi; Pastorello, Bruno Fraccini; Studart Neto, Adalberto; Guariglia, Carla Cristina; Tsunemi, Miriam Harumi; Moreira, Everton Luis Santos; Ianof, Jéssica Natuline; Anghinah, Renato; Nitrini, Ricardo; Cerri, Giovanni Guido; Fortea, Juan; Buchpiguel, Carlos Alberto; Leite, Claudia Costa

doi:10.1055/S-0043-1768666

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Original Article • Arq. Neuropsiquiatr. 81 (5) • 2023 • https://doi.org/10.1055/S-0043-1768666 linkcopy

Brain glucose metabolism and gray matter volume in retired professional soccer players: a cross-sectional [¹⁸F]FDG-PET/MRI study

Metabolismo glicolítico cerebral e volume de substância cinzenta em jogadores de futebol profissionais aposentados: um estudo transversal de [¹⁸F]FDG-PET/RM

Authorship SCIMAGO INSTITUTIONS RANKINGS

Background Professional soccer athletes are exposed to repetitive head impacts and are at risk of developing chronic traumatic encephalopathy.

Objective To evaluate regional brain glucose metabolism (rBGM) and gray matter (GM) volume in retired soccer players (RSPs).

Methods Male RSPs and age and sex-matched controls prospectively enrolled between 2017 and 2019 underwent neurological and neuropsychological evaluations, brain MRI and [18F]FDG-PET in a 3.0-Tesla PET/MRI scanner. Visual analysis was performed by a blinded neuroradiologist and a blinded nuclear physician. Regional brain glucose metabolism and GM volume were assessed using SPM8 software. Groups were compared using appropriate statistical tests available at SPM8 and R.

Results Nineteen RSPs (median [IQR]: 62 [50–64.5] years old) and 20 controls (60 [48–73] years old) were included. Retired soccer players performed worse on mini-mental state examination, digit span, clock drawing, phonemic and semantic verbal fluency tests, and had reduced rBGM in the left temporal pole (pFDR = 0.008) and the anterior left middle temporal gyrus (pFDR = 0.043). Semantic verbal fluency correlated with rBGM in the right hippocampus, left temporal pole, and posterior left middle temporal gyrus (p ≤ 0.042). Cray matter volume reduction was observed in similar anatomic regions but was less extensive and did not survive correction for multiple comparisons (pFDR ≥ 0.085). Individual [18F]FDG-PET visual analysis revealed seven RSPs with overt hypometabolism in the medial and lateral temporal lobes, frontal lobes, and temporoparietal regions. Retired soccer players had a higher prevalence of septum pellucidum abnormalities on MRI.

Conclusion Retired soccer players had reduced rBCM and CM volume in the temporal lobes and septum pellucidum abnormalities, findings possibly related to repetitive head impacts.

Keywords:
Soccer; Brain Injuries, Traumatic; Chronic Traumatic Encephalopathy; Positron-Emission Tomography; Magnetic Resonance Imaging

			Retired soccer players (19, male)	Controls (20, male)	p-value
Demographics (years, median; IQR)	Age (years old)		62; 50–64.5	60; 48–73	0.527^a
Demographics (years, median; IQR)	Education		14; 11–15	15; 11.8–16	0.035^a
Septum pellucidum abnormalities (% of participants)	Cavum Septum Pellucidum		68	15	0.001^b
	Cavum Vergae		37	20	0.243^b
	Fenestration of Cavum Septum Pellucidum		32	0	0.006^b
Brain atrophy (visual rating) (median; IQR)	Global cortical atrophy (Pasquier) scale		1; 0–1	1; 0–2	0.136^a
	Medial temporal lobe atrophy (Scheltens) scale		0; 0–1	0;0–0.125	0.446^a
	Posterior atrophy (Koedam) scale		0; 0–1	0; 0–1	0.543^a
	Anterior cingulate atrophy scale		0; 0–0.5	0; 0–1	0.414^a
	Orbitofrontal atrophy scale		0; 0–0	0; 0–0	0.964^a
	Anterior-temporal atrophy scale		0; 0–0	0; 0–1	0.471^a
	Frontoinsular atrophy scale		0; 0–0	0; 0–0.25	0.730^a
White matter FLAIR hyperintensities (visual rating and quantification) (median; IQR)	Fazekas scale		1; 0–1	1; 0–1	0.666^a
	Volume of white matter FLAIR hyperintensities^d		5.7; 2.4–32.5	2.7; 1.5–18.1	0.224^a
Neuropsychological evaluation	MMSE total score (median; IQR)		27; 25.5–29	29; 28.8–30	0.003^a
	Clock drawing test (median; IQR)		9; 9–10	10; 9–10	0.036^a
	Semantic verbal fluency test (animals) (mean ± SD)		15.7 ± 4.4	20.8 ± 4.8	0.002^c
	Phonemic verbal fluency test total score* (mean ± SD)		35.3 ± 11.5	42.6 ± 9.6	0.040^c
	Digit span test total score* (mean ± SD)		8.3 ± 2.1	11.5 ± 3.9	0.005^c
	Figure memory test	Naming (median; IQR)	10; 10–10	10; 10–10	1.000^a
		Incidental memory (mean ± SD)	6.5 ± 2.4	6.0 ± 2.1	0.467^c
		Immediate memory (median; IQR)	8; 7–9	8; 7–9	1.000^a
		Learning (median; IQR)	9; 8–10	9; 8–10	0.609^a
		Delayed recall (median; IQR)	9; 7–9	9; 8–9.3	0.437^a
		Recognition (median; IQR)	10; 9.5–10	10; 10–10	0.094^a
Clinical evaluation	History of traumatic brain injury		11 (58%)	0	<0.001^c
	Psychiatric symptoms		6 (31%)	2 (10%)	0.171^b
	Subjective cognitive complaints		2 (10%)	5 (25%)	0.447^b
	Arterial systemic hypertension		4 (21%)	6 (30%)	0.562^b
	Type 2 diabetes		2 (10%)	2 (10%)	0.920^b

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[TFN1] Abbreviations: IQR, interquartile range; MMSE, Mini-Mental State Examination; SD, standard deviation.

Notes: ^aMann-Whitney U test. ^bChi-squared test. ^ct-test for independent samples. ^dVolume of WM FLAIR hyperintensities measured with Lesion Segmentation Tool toolbox for SPM 8 software (threshold = 0.30). Data with normal distribution are expressed as mean ± SD and data with non-normal distribution are expressed as median; IQR. *One control (with normal MMSE, naming, incidental memory, immediate memory, learning, delayed recall, and recognition scores) had missing values on the Digits Span and Phonemic Verbal Fluency Tests.

Brain glucose metabolism and gray matter volume in retired professional soccer players: a cross-sectional [18F]FDG-PET/MRI study

Metabolismo glicolítico cerebral e volume de substância cinzenta em jogadores de futebol profissionais aposentados: um estudo transversal de [18F]FDG-PET/RM

Brain glucose metabolism and gray matter volume in retired professional soccer players: a cross-sectional [¹⁸F]FDG-PET/MRI study

Metabolismo glicolítico cerebral e volume de substância cinzenta em jogadores de futebol profissionais aposentados: um estudo transversal de [¹⁸F]FDG-PET/RM