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

Abstract

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). Gray 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 rBGM and GM volume in the temporal lobes and septum pellucidum abnormalities, findings possibly related to repetitive head impacts.

Resumo

Antecedentes Jogadores profissionais de futebol estão expostos a impactos cranianos repetitivos e ao risco de desenvolver encefalopatia traumática crônica.

Objetivo Avaliar o metabolismo glicolítico cerebral regional (MGCr) e o volume de substância cinzenta (vSC) em jogadores de futebol aposentados (JFAs).

Métodos Jogadores de futebol aposentados masculinos e controles pareados por idade e sexo foram incluídos prospectivamente entre 2017 e 2019. Foram realizadas avaliações neurológica e neuropsicológica, ressonância magnética (RM) e [18F]FDG-PET cerebrais (3.0-Tesla PET/RM). As imagens foram analisadas visualmente por um neurorradiologista e um médico nuclear cegos ao grupo de cada participante. O metabolismo glicolítico cerebral regional e o vSC foram avaliados através do programa SPM8. Os grupos foram comparados através de testes estatísticos apropriados disponíveis em SPM8 e R, de acordo com a distribuição e o tipo dos dados.

Resultados Dezenove JFAs (mediana [IIQ]: 62 [50–64.5] anos) e 20 controles (60 [48–73] anos) foram incluídos. Os JFAs tiveram pior desempenho no mini-exame do estado mental e nos testes de dígitos, desenho do relógio, fluência verbal e fluência semântica e apresentaram MGCr significativamente reduzido no polo temporal e no giro temporal médio anterior esquerdos. Fluência semântica (animais) apresentou correlação positiva com MGCr no hipocampo direito, no polo temporal esquerdo e no aspecto posterior do giro temporal médio esquerdo. Menor vSC foi observado nas mesmas regiões, porém este achado não sobreviveu à correção para comparações múltiplas. Análise individual do [18F]FDG-PET cerebral revelou sete JFAs com claro hipometabolismo nas faces medial e lateral dos lobos temporais, nos lobos frontais e nas regiões temporoparietais. Os JFAs apresentaram ainda maior prevalência de anormalidades do septo pelúcido.

Conclusão Os JFAs apresentam MGCr e vSC reduzidos nos lobos temporais, além de anormalidades do septo pelúcido, achados possivelmente relacionados a impactos cranianos repetitivos.

Keywords

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

Palavras-chave

Futebol - Lesões Encefálicas Traumáticas - Encefalopatia Traumática Crônica - Tomografia Por Emissão De Pósitrons - Imageamento Por Ressonância Magnética

Authors' Contributions

MRA, AMC: conceptualization, data curation, formal analysis, investigation, project administration, resources, software, visualization, writing – original draft, writing – review & editing, contributed equally to this work and shared first co-authorship; CGC: data curation, formal analysis, resources, software; BFP: data curation, investigation, project administration, resources, software; ASN, JNI: data curation, investigation, resources; CCG: investigation; MHT: formal analysis; ELSM: data curation, formal analysis; RA, RN: conceptualization, funding acquisition, methodology, resources, writing – review & editing; GGC: funding acquisition, methodology, resources, writing – review & editing; JF: writing – review & editing; CAB: conceptualization, funding acquisition, methodology, supervision, writing – review & editing; CCL: Conceptualization, funding acquisition, methodology, project administration, resources, supervision, writing – review & editing. All authors read and approved the manuscript, and all data were generated in-house and no paper mill was used.

Support

The present study was supported by funding from General Electric (GE Healthcare). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; or decision to submit for publication.

Publication History

Received: 16 September 2022

Accepted: 15 January 2023

Article published online:
31 May 2023

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