Skip to main content
Erschienen in:

Open Access 24.10.2023 | Correspondence

Risk of chronic traumatic encephalopathy in rugby union is associated with length of playing career

verfasst von: William Stewart, Michael E. Buckland, Bobak Abdolmohammadi, Andrew J. Affleck, Victor E. Alvarez, Shannon Gilchrist, Bertrand R. Huber, Edward B. Lee, Donald M. Lyall, Christopher J. Nowinski, Emma R. Russell, Thor D. Stein, Catherine M. Suter, Ann C. McKee

Erschienen in: Acta Neuropathologica | Ausgabe 6/2023

download
DOWNLOAD
print
DRUCKEN
insite
SUCHEN
Hinweise

Supplementary Information

The online version contains supplementary material available at https://​doi.​org/​10.​1007/​s00401-023-02644-3.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
There is concern over late, adverse brain health outcomes associated with contact sports participation, with high neurodegenerative disease risk reported in studies of former American football [3, 8], soccer [9, 16] and rugby union players [15]. In parallel, autopsy studies of former athletes from a range of contact sports describe a frequent finding of chronic traumatic encephalopathy (CTE), a neuropathology uniquely associated with prior history of traumatic brain injury (TBI) and repetitive head impact (RHI) exposure [7, 1214]. Among contact sports, rugby union (hereafter ‘rugby’) is documented as having high risk of concussion/mild TBI, with reported injury rates ranging 4.1 concussions/1000 player hours at community level [2] to 22.2 concussions/1000 player hours in professional rugby [4]. Nevertheless, despite its popularity, with a reported 8.46 million active participants globally [20], there have been relatively few case descriptions of CTE in former rugby players [7, 17, 18]. To address this, we collated and analyzed neuropathological data from autopsy brain examinations on individuals with rugby as primary sport exposure submitted to three international brain banks with specific interest in contact sport and brain health.
Case records of the Understanding Neurologic Injury and Traumatic Encephalopathy Brain Bank (UNITE; Boston University School of Medicine, US), the Glasgow TBI Archive (GTBI; University of Glasgow, UK) and the Australian Sports Brain Bank (ASBB; Royal Prince Alfred Hospital and University of Sydney, Australia) were surveyed to identify case donations in which primary sport exposure was recorded as ‘rugby union’. Each archive employs standardized procedures for case accrual, clinical history acquisition and tissue processing, with neuropathological evaluations conducted blind to demographic and clinical information and employing established, consensus protocols for assessment of neurodegenerative disease pathologies, including CTE [1, 11, 13]. For the purposes of this study, existing archive datasets were interrogated to extract relevant demographic information (age at death, sex), sports exposure history (years duration of rugby participation, position played [dichotomized as forward or back], highest level of participation [dichotomized as amateur or elite (encompassing representative international and/or professional)], other contact sport exposure) and principal neuropathological findings.
In total, 31 cases where primary sports exposure was documented as rugby union were identified within contributing research brain banks: 16 cases from UNITE; 8 from GTBI; and 7 from ASBB. Among these, mean age at death was 60.4 years (standard deviation [SD] 21.7 years; range 17–95 years), with all but 1 (3%) case male. Reported rugby career length averaged 18.3 years (SD 10.0 years; range 2–35 years), with an equal number of forward and backs, where information on player field position was available. Twenty-three (74%) played rugby exclusively as amateurs, with 8 (26%) reaching elite (representative/ professional) level and 19 of 29 (66%) reporting history of prior TBI with loss of consciousness and/or history of concussion.
Regarding neuropathological findings, CTE was present in 21 of 31 (68%) brains of former rugby players examined, a majority of whom (13/21; 62%) played solely at amateur level. Among cases with CTE, 14 were typical of low-stage CTE pathology, 7 high stage [1]. No notable differences were observed between players with or without CTE in respect of age at death, participation in other contact sports, history of drug or alcohol use disorder, whole brain weight at autopsy, prevalence of septum pellucidum abnormalities (Table 1) or wider neuropathologies assessed (Supplementary Table 1). However, players with CTE typically had longer rugby playing careers than those without CTE. Indeed, adjusted for age at death, a dose–response relationship was evident between career length and the presence of CTE at autopsy, with each additional year of play associated with an approximately 14% increase in CTE risk (relative risk ratio 1.138; 95% confidence interval 1.015–1.277; P = 0.027; multinomial logistic regression). While history of TBI with loss of consciousness and/or concussion was common among cases with CTE, this was not significantly different to prevalence among cases without CTE.
Table 1
Demographic and primary neuropathological findings
 
CTE
N = 21
No CTE
N = 10
P
Demographic information
Mean age at death
61.7 years
57.8 years
0.710*
(standard deviation) [range]
(17.5)[23–94]
(29.7)[17–95]
Sex
  
NA
 Male
21
9
 Female
0
1
Years rugby participation
21.5 years
12.1 years
0.031*
(standard deviation) [range]
(8.1)[8–35}
(10.9)[2–15]
 
Position
  
NA
 Unknown
7
8
 Forward
7
1
 Back
7
1
Highest participation level
  
NA
 Amateur
13
10
 Elite
8
0
 
Other contact sports
  
1.000**
 None
12
6
 American football
5
2
 Boxing
3
0
 Soccer
2
1
 Ice Hockey
2
0
 Rugby league
1
0
 Wrestling
0
1
TBI with LOC and/or concussion
  
0.083**
 Unknown
0
2
 None
5
5
 Yes
16
3
Alcohol use disorder
  
1.000**
 Unknown
5
4
 No
9
4
 Yes
7
2
Drug use disorder
  
0.120**
 Unknown
6
4
 No
12
2
 Yes
3
4
Neuropathology findings
Mean brain weight
1353 g
1321 g
0.677*
(standard deviation)[range]
(208 g)[1030–1680 g]
(186 g) [1060–1449 g]
Septum pellucidum
  
0.422**
 Not available
1
1
 Intact
7
5
 Cavum/fenestrated
13
4
CTE
  
NA
 None
0
10
 Low stage
14
0
 High stage
7
0
CTE chronic traumatic encephalopathy, LOC loss of consciousness, NA not assessed as data insufficient and/or inappropriate for analysis, TBI traumatic brain injury. *Student’s t test. **Fisher’s exact with data dichotomized as feature present versus absent
An acknowledged limitation of this study is that our case series represents a convenience sample of brains donated for research evaluation. Nevertheless, our observation that CTE pathology is present in around two-thirds of former rugby union players examined is in line with experience reporting neuropathological findings in other series of former contact sports athletes, including former American footballers and soccer players [7, 13]. Notably, a majority of our cases played solely at amateur level, including those with CTE. First played in the nineteenth century, rugby remained an amateur sport until 1995 when professionalism was permitted. With an average age among our cohort around 60 years, it is perhaps not surprising that the majority are defined as amateur. Intriguingly, some observers suggest that contact sport-related late adverse brain health outcomes might be restricted solely to professional athletes [5]. In respect of CTE, at least, our data suggest that level of participation does not protect against development of this neurodegenerative pathology.
In contrast, among this case series, there was clear association between length of rugby playing career and risk of CTE, which was independent of age at death. Again, this is in line with observations among several contact sports demonstrating longer playing careers associated with increased risk of a neurodegenerative disease diagnosis [3, 16] and, independently, with increased risk of CTE pathology [610]. These data would be consistent with risk resulting from cumulative exposure to a factor associated with sport. To date, the only recognized risk factor for development of CTE is TBI and/or RHI exposure. Rugby union is recognized as having a notably high risk of concussion compared to wider contact sports [19], with risk at professional level increasing over the past 20 years [4].
In summary, in this convenience sample of research brain donations from former rugby union players, we found clear evidence of CTE pathology in around two-thirds of cases. Further, risk of CTE was directly associated with length of rugby playing career, interpreted as a surrogate for head impact exposure. These data reinforce concern around adverse brain health outcomes among former contact sports athletes and add to evidence in support of calls to reduce exposure to repetitive head impacts and risk of traumatic brain injury in training and in match play across all sports.

Acknowledgements

This work is supported by funding from: the National Institute of Neurological Disorders and Stroke of the National Institutes of Health (Award Nos. R01NS092398, R01NS094003, R01NS038104, U54NS115322, U01NS086659, U01NS093334, U54NS115266, R01NS078337, and R56NS078337); National Institute on Aging (Award Nos. AG057902, AG06348 and supplement 0572063345); US Department of Veterans Affairs (CX00135 to Dr. McKee and CX001038 to Dr. Stein); The Concussion Legacy Foundation; The Andlinger Foundation; and an NHS Research Scotland Career Researcher Fellowship (WS). The ASBB is supported by Sydney Local Health District and unrestricted philanthropic donations.

Declarations

Conflict of interest

The authors declare no competing interests.

Ethics approval

The Glasgow TBI Archive has specific Research Ethics Committee approval as a Research Tissue Bank (ref 22/WS/0168). The Australian Sports Brain Bank has ethical approval granted by the Sydney Local Health District Human Research Ethics Committee, Royal Prince Alfred Hospital (ref: X23-0073).
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://​creativecommons.​org/​licenses/​by/​4.​0/​.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Unsere Produktempfehlungen

e.Med Interdisziplinär

Kombi-Abonnement

Jetzt e.Med zum Sonderpreis bestellen!

Für Ihren Erfolg in Klinik und Praxis - Die beste Hilfe in Ihrem Arbeitsalltag

Mit e.Med Interdisziplinär erhalten Sie Zugang zu allen CME-Fortbildungen und Fachzeitschriften auf SpringerMedizin.de.

e.Med Neurologie & Psychiatrie

Kombi-Abonnement

Mit e.Med Neurologie & Psychiatrie erhalten Sie Zugang zu CME-Fortbildungen der Fachgebiete, den Premium-Inhalten der dazugehörigen Fachzeitschriften, inklusive einer gedruckten Zeitschrift Ihrer Wahl.

e.Med Neurologie

Kombi-Abonnement

Mit e.Med Neurologie erhalten Sie Zugang zu CME-Fortbildungen des Fachgebietes, den Premium-Inhalten der neurologischen Fachzeitschriften, inklusive einer gedruckten Neurologie-Zeitschrift Ihrer Wahl.

Anhänge

Supplementary Information

Below is the link to the electronic supplementary material.
Literatur
1.
Zurück zum Zitat Bieniek KF, Cairns NJ, Crary JF et al (2021) The second NINDS/NIBIB consensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy. J Neuropathol Exp Neurol 80:210–219PubMedPubMedCentral Bieniek KF, Cairns NJ, Crary JF et al (2021) The second NINDS/NIBIB consensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy. J Neuropathol Exp Neurol 80:210–219PubMedPubMedCentral
3.
Zurück zum Zitat Daneshvar DH, Mez J, Alosco ML et al (2021) Incidence of and mortality from amyotrophic lateral sclerosis in National Football League athletes. JAMA Netw Open 4:e2138801CrossRefPubMedPubMedCentral Daneshvar DH, Mez J, Alosco ML et al (2021) Incidence of and mortality from amyotrophic lateral sclerosis in National Football League athletes. JAMA Netw Open 4:e2138801CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat Iverson GL, Castellani RJ, Cassidy JD et al (2023) Examining later-in-life health risks associated with sport-related concussion and repetitive head impacts: a systematic review of case-control and cohort studies. Br J Sports Med 57:810–821CrossRefPubMed Iverson GL, Castellani RJ, Cassidy JD et al (2023) Examining later-in-life health risks associated with sport-related concussion and repetitive head impacts: a systematic review of case-control and cohort studies. Br J Sports Med 57:810–821CrossRefPubMed
6.
Zurück zum Zitat LeClair J, Weuve J, Fox MP et al (2022) Relationship between level of american football playing and diagnosis of chronic traumatic encephalopathy in a selection bias analysis. Am J Epidemiol 191:1429–1443CrossRefPubMedPubMedCentral LeClair J, Weuve J, Fox MP et al (2022) Relationship between level of american football playing and diagnosis of chronic traumatic encephalopathy in a selection bias analysis. Am J Epidemiol 191:1429–1443CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Lee EB, Kinch K, Johnson VE, Trojanowski JQ, Smith DH, Stewart W (2019) Chronic traumatic encephalopathy is a common co-morbidity, but less frequent primary dementia in former soccer and rugby players. Acta Neuropathol 138:389–399CrossRefPubMedPubMedCentral Lee EB, Kinch K, Johnson VE, Trojanowski JQ, Smith DH, Stewart W (2019) Chronic traumatic encephalopathy is a common co-morbidity, but less frequent primary dementia in former soccer and rugby players. Acta Neuropathol 138:389–399CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Lehman EJ, Hein MJ, Baron SL et al (2012) Neurodegenerative causes of death among retired National Football League players. Neurology 79:1970–1974CrossRefPubMedPubMedCentral Lehman EJ, Hein MJ, Baron SL et al (2012) Neurodegenerative causes of death among retired National Football League players. Neurology 79:1970–1974CrossRefPubMedPubMedCentral
9.
Zurück zum Zitat Mackay DF, Russell ER, Stewart K et al (2019) Neurodegenerative disease mortality among former professional soccer players. N Engl J Med 381:1801–1808CrossRefPubMedPubMedCentral Mackay DF, Russell ER, Stewart K et al (2019) Neurodegenerative disease mortality among former professional soccer players. N Engl J Med 381:1801–1808CrossRefPubMedPubMedCentral
10.
Zurück zum Zitat Mez J, Daneshvar DH, Abdolmohammadi B et al (2020) Duration of American football play and chronic traumatic encephalopathy. Ann Neurol 87:116–131CrossRefPubMed Mez J, Daneshvar DH, Abdolmohammadi B et al (2020) Duration of American football play and chronic traumatic encephalopathy. Ann Neurol 87:116–131CrossRefPubMed
11.
Zurück zum Zitat McKee AC, Cairns NJ, Dickson DW et al (2016) The first NINDS/NIBIB consensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy. Acta Neuropathol 131:75–86CrossRefPubMed McKee AC, Cairns NJ, Dickson DW et al (2016) The first NINDS/NIBIB consensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy. Acta Neuropathol 131:75–86CrossRefPubMed
13.
Zurück zum Zitat McKee AC, Stein TD, Huber BR et al (2023) Chronic traumatic encephalopathy (CTE): criteria for neuropathological diagnosis and relationship to repetitive head impacts. Acta Neuropathol 145:371–394CrossRefPubMedPubMedCentral McKee AC, Stein TD, Huber BR et al (2023) Chronic traumatic encephalopathy (CTE): criteria for neuropathological diagnosis and relationship to repetitive head impacts. Acta Neuropathol 145:371–394CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat McKee AC, Stern RA, Nowinski CJ et al (2013) The spectrum of disease in chronic traumatic encephalopathy. Brain 136:43–64CrossRefPubMed McKee AC, Stern RA, Nowinski CJ et al (2013) The spectrum of disease in chronic traumatic encephalopathy. Brain 136:43–64CrossRefPubMed
15.
Zurück zum Zitat Russell ER, Mackay DF, Lyall D, Stewart K, MacLean JA, Robson J et al (2022) Neurodegenerative disease risk among former international rugby union players. J Neurol Neurosurg Psychiatry 93:1262–1268CrossRefPubMed Russell ER, Mackay DF, Lyall D, Stewart K, MacLean JA, Robson J et al (2022) Neurodegenerative disease risk among former international rugby union players. J Neurol Neurosurg Psychiatry 93:1262–1268CrossRefPubMed
16.
Zurück zum Zitat Russell ER, Mackay DF, Stewart K et al (2021) Association of field position and career length with risk of neurodegenerative disease in male former professional soccer players. JAMA Neurol 78:1057–1063CrossRefPubMed Russell ER, Mackay DF, Stewart K et al (2021) Association of field position and career length with risk of neurodegenerative disease in male former professional soccer players. JAMA Neurol 78:1057–1063CrossRefPubMed
17.
Zurück zum Zitat Stewart W, McNamara PH, Lawlor B, Hutchinson S, Farrell M (2016) Chronic traumatic encephalopathy: a potential late and under recognized consequence of rugby union? QJM 109:11–15CrossRefPubMed Stewart W, McNamara PH, Lawlor B, Hutchinson S, Farrell M (2016) Chronic traumatic encephalopathy: a potential late and under recognized consequence of rugby union? QJM 109:11–15CrossRefPubMed
18.
Zurück zum Zitat Suter CM, Affleck AJ, Lee M, Pearce AJ, Iles LE, Buckland ME (2022) Chronic traumatic encephalopathy in Australia: the first three years of the Australian Sports Brain Bank. Med J Aust 216:530–531CrossRefPubMedPubMedCentral Suter CM, Affleck AJ, Lee M, Pearce AJ, Iles LE, Buckland ME (2022) Chronic traumatic encephalopathy in Australia: the first three years of the Australian Sports Brain Bank. Med J Aust 216:530–531CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Van Pelt KL, Puetz T, Swallow J, Lapointe AP, Broglio SP (2021) Data-driven risk classification of concussion rates: a systematic review and meta-analysis. Sports Med 51:1227–1244CrossRefPubMed Van Pelt KL, Puetz T, Swallow J, Lapointe AP, Broglio SP (2021) Data-driven risk classification of concussion rates: a systematic review and meta-analysis. Sports Med 51:1227–1244CrossRefPubMed
Metadaten
Titel
Risk of chronic traumatic encephalopathy in rugby union is associated with length of playing career
verfasst von
William Stewart
Michael E. Buckland
Bobak Abdolmohammadi
Andrew J. Affleck
Victor E. Alvarez
Shannon Gilchrist
Bertrand R. Huber
Edward B. Lee
Donald M. Lyall
Christopher J. Nowinski
Emma R. Russell
Thor D. Stein
Catherine M. Suter
Ann C. McKee
Publikationsdatum
24.10.2023
Verlag
Springer Berlin Heidelberg
Erschienen in
Acta Neuropathologica / Ausgabe 6/2023
Print ISSN: 0001-6322
Elektronische ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-023-02644-3

Weitere Artikel der Ausgabe 6/2023

Acta Neuropathologica 6/2023 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Neu im Fachgebiet Neurologie

Parkinson-Prodromi per Smartphone-App erkennen?

19.07.2024 Parkinson-Krankheit Nachrichten

Mithilfe einer Smartphone-App lassen sich möglicherweise stimmliche und sprachliche Veränderungen erfassen, die auf eine frühe Parkinsonerkrankung hindeuten könnten.

Multimodale Intervention verbessert Demenzrisikoprofil

18.07.2024 Demenz Nachrichten

Eine Auswertung der Studie AgeWell.de legt nahe, dass sich auch bei älteren Personen mit hoher Demenzgefahr das Risikoprofil durch Lebensstiländerungen verbessern lässt. Die stärksten Auswirkungen haben dabei eine Ernährungsumstellung und eine gute Blutdruckkontrolle.

Muskeln trainieren gegen Nervenschäden durch Chemotherapie

17.07.2024 Nebenwirkungen der Krebstherapie Nachrichten

Chemotherapien können die Nerven schädigen und damit die Lebensqualität von Betroffenen zusätzlich einschränken. Wer aber auf die richtige Art trainiert, kann das absolute Risiko für Neuropathien um bis zu 40% senken.

Herzrhythmusstörungen – neue Verfahren für langfristige Erfolge

16.07.2024 Vorhofflimmern Podcast

Prof. Markus Lerch wirft gemeinsam mit dem Herzspezialisten Prof. Gerd Hasenfuß aus Göttingen einen Blick auf neue Entwicklungen in der Diagnostik und Therapie von Herzrhythmusstörungen. Hören Sie in dieser Folge, warum fast jedes Vorhofflimmern therapiert werden sollte, wieso die Ablationsbehandlung auch bei Herzinsuffizienz gute Effekte zeigt und vor und nach welchen Medikamenten Sie ein EKG schreiben sollten.

Deutsche Gesellschaft für Innere Medizin

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.