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Open access Original research

Association of the British Athletic

Muscle Injury Classification and
anatomic location with return to full
training and reinjury following
hamstring injury in elite football
Ricky Shamji ‍ ‍,1,2 Steven L J James,3,4 Rajesh Botchu,3,4 Kent A Khurniawan,4
Gurjit Bhogal,1,2 Alison Rushton4,5

To cite: Shamji R, James SLJ, ABSTRACT

Botchu R, et al. Association SUMMARY
Background The relationship between hamstring
of the British Athletic Muscle
muscle injuries (HMIs) that involve the intramuscular
Injury Classification and What are the new findings?
anatomic location with return tendon and prolonged recovery time and increased reinjury
►► Hamstring muscle injuries (HMIs) extending into the
to full training and reinjury rate remains unclear in elite footballers.
intramuscular tendon, categorised as British Athletic
following hamstring injury Objective To determine the association of time to return
muscle injury ‘c’ on MRI, are associated with longer
in elite football. BMJ Open to full training (TRFT) and reinjury of HMIs using the British
Sport & Exercise Medicine time to return to full training and increased reinjury
Athletic Muscle Injury Classification (BAMIC) and specific
2021;7:e001010. doi:10.1136/ rate of elite-­level players in English football.
anatomical injury location in elite-­level football players.
bmjsem-2020-001010 ►► Most of the HMIs to the biceps femoris with reinjury
Methods The electronic medical records of all players at
were seen at the distal musculotendinous T junction
an English Premier League club were reviewed over eight
(DMTJ) involving both the long and short heads on
Accepted 16 April 2021 consecutive seasons. All players who sustained an acute
MRI.

copyright.
HMI were included. Two experienced musculoskeletal
radiologists independently graded each muscle using the How might it impact on clinical practice in the
BAMIC, categorised each injury location area (proximal vs future?
middle vs distal third and proximal vs distal tendon) and ►► HMI patterns, beyond intramuscular tendon involve-
reported second muscle involvement. TRFT and reinjury ment, such as location and second muscle injury
were recorded. warrants consideration for clinicians managing elite-­
Results Out of 61 HMIs, the intramuscular tendon level football players.
(BAMIC ‘c’) was involved in 13 (21.3%). HMI involving ►► The recognition of DMTJ of the biceps femoris inju-
the intramuscular tendon (‘c’) had a mean rank TRFT of ries may be important in elite-­level football.
© Author(s) (or their
36 days compared with 24 days without involvement
employer(s)) 2021. Re-­use (p=0.013). There were 10 (16.4%) reinjuries with a
permitted under CC BY-­NC. No significant difference of 38.5% reinjury rate in the group prolonged absence with a high risk of rein-
commercial re-­use. See rights with intramuscular tendon injury (‘c’) and 12.5% in the jury.1 2 Hamstring reinjury rates are reported
and permissions. Published by group without (p=0.031). TRFT and reinjury involving a
BMJ.
to be between 14% and 63%.2 Furthermore,
second muscle was statistically significantly higher than
1 Ekstrand et al3 recently reported that HMIs
Medical Department, Aston Villa without. Most of the HMIs to the biceps femoris with
FC, Birmingham, UK reinjury (5 out of 9) were in the distal third section related
have increased by 4% annually in mens
2
Centre for Musculoskeletal to the distal tendon site involving both the long and short professional football since 2001. Medical
Medicine, Royal Orthopaedic head. teams face pressure to make an accurate
Hospital, Birmingham, UK diagnosis and identify important prognostic
3 Conclusion TRFT in HMI involving the intramuscular
Imaging Department,
tendon (‘c’) of the Biceps femoris is significantly longer factors for return to play in the shortest time
Royal Orthopaedic Hospital,
Birmingham, UK with significantly higher reinjury rate compared with possible while still ensuring that the risk of
4
School of Sport, Exercise injuries without, in elite football players. The finding that injury reoccurrence is minimal.
and Rehabilitation Sciences, most reinjures of the biceps femoris occurring in the distal HMIs involving the intramuscular tendon
University of Birmingham, third muscle at the distal tendon site, involving both the have been associated with prolonged recovery
Birmingham, UK long and short head, merits further investigation. time and a higher reinjury rate in professional
5
School of Physical Therapy,
University of Western Ontario, athletes.4–8 Pollock et al6 9 used their validated
London, Ontario, Canada British Athletics Muscle Injury Classification
(BAMIC) which distinguishes anatomical
Correspondence to
INTRODUCTION site (‘a’: myofascial; ‘b’: musculotendinous
Dr Ricky Shamji; Hamstring muscle injuries (HMIs) in elite junction or ‘c’: intramuscular tendon) and
r​ icky.​shamji@​avfc.​co.​uk football are common and may result in a injury severity (grading 0–4) based on MRI

Shamji R, et al. BMJ Open Sp Ex Med 2021;7:e001010. doi:10.1136/bmjsem-2020-001010 1

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measurements within muscle or tendon, to carry out a

retrospective study of HMIs in track and field athletes. Box 1 MRI thigh protocol parameters
They found BAMIC grade ‘c’ injuries took significantly MRI thigh protocol
time to return to full training (TRFT) and had a reinjury ►► t1 stir sag: FOV 420 mm, matrix resolution 320×320, 5 mm slice
rate of up to 63% compared with myofascial and muscu- thickness.
lotendinous injury. Given that clinical examination alone ►► t1 coronal: FOV 400, matrix resolution 384×384, 5 mm slice
is unable to discriminate the presence of intramuscular thickness.
tendon involvement, MRI is needed in professional ►► t1 stir axial: FOV 220, matrix resolution 320×320, 6 mm slice
sport.10 thickness.
The first prospective study of 70 HMIs by van der ►► pd axial: FOV 220, matrix resolution 384×384, 6 mm slice thickness.
Made et al11 has put this increased TRFT and reinjury ►► pd axial fs: FOV 220, matrix 320×320, 6 mm slice thickness.
association with intramuscular tendon involvement into
doubt. Their study of athletes from various sports does
not support the notion that injuries involving the tendon Participants
are significantly more serious. They demonstrated that All first team male players under contract across eight
return to play was only slightly over a week longer for competitive seasons (English Premier League 2011–
HMIs involving the intramuscular tendon vs those that 2016 and The English Football League Championship
are not (30.2±10.8 vs 22.2±7.4 days) and conclude that its 2016–19) were eligible; including all injuries reported
clinical relevance for the individual athlete is limited. between August 2011 and June 2019, with acute pain
Other hamstring injury patterns may also be important. to the posterior thigh, tenderness on hamstring palpa-
Entwisle et al12 describe the distal musculotendinous tion, contraction or function and an MRI examination
T junction (DMTJ) of the biceps femoris where the performed within 7 days of injury. Direct muscle contu-
opposing anterolateral aspect of the long head and the sions were excluded based either on clinical presentation
posterolateral aspect of the short head form the musculo- or imaging appearances.
tendinous junction which appears as a T-­shaped structure.
They report higher reinjury rates involving this DMTJ of Data sources
biceps femoris muscle in their cross-­sectional study of 106 A retrospective review was performed of: injury date, age
injuries in Australian Football players. The reinjury rate of player at time of injury, clinical diagnosis, TRFT, MRI

copyright.
was 54%, with 86% of subsequent injuries being the same scan date and injury recurrence to the same hamstring
or of higher grade than the index injury. muscle during rehabilitation (exacerbation before
Differences in study design, sporting demands and TRFT) or within 3 months of TRFT. Consistent with
failure to recognise distinct clinical entities such as the the Pollock et al6 retrospective study, a recurrence was
DMTJ, may contribute to the contrasting reports of recorded if the player sustained an acute, sudden exac-
HMI studies. The purpose of this study was to determine erbation of hamstring pain during exercise, followed
whether HMIs graded according to the BAMIC were asso- by worsening of clinical tests and requiring cessation of
ciated with delayed time to return to full training (TRFT) current activity of rehabilitation or training for greater
and higher recurrence rates in elite male football players. than 48 hours. Recurrence was categorised as yes/no.
The study also aimed to assess other hamstring anatom- All MRI examinations were performed using a 1.5T MRI
ical locations (proximal vs middle vs distal and proximal scanner (Siemens MAGNETOM Aera) using the same
vs distal tendon) that may be associated with delayed MRI thigh protocol at the same imaging centre (box 1).
TRFT and higher recurrence rates in elite male football
players. Our working hypothesis was that HMIs involving Bias
the intramuscular tendon and injuries involving the A retrospective review of each MRI was independently
distal biceps femoris are associated with longer TRFT and performed by two fellowship trained musculoskel-
higher reinjury rate. etal radiologists according to BAMIC using the same
protocol (Pollock et al). If the HMI affected ≥1 muscle,
METHODS the muscle with the most extensive pathology deter-
Design mined by the injury details was considered the primary
Retrospective observational cohort study to measure the injured muscle.14 Any discrepancies were discussed and
association between multiple exposures (BAMIC grade, consensus reached regarding classification. MRI data
muscle affected) and outcomes (TRFT, recurrence rate). collected included: scan date, primary muscle affected,
The study was designed and reported according to the second muscle affected, BAMIC (anatomical location
Strengthening the Reporting of Observational studies in and injury extent) and location (figure 1). All rehabil-
Epidemiology statement.13 itation was provided by the Club’s medical team and
guided by its philosophy of progressive, functional and
Setting strength-­based rehabilitation alongside graduated func-
Data were collected from one English Premier League tional drills and running, limited by pain. The transition
club through an electronic medical record system. process to full team training was gradual and integrated

2 Shamji R, et al. BMJ Open Sp Ex Med 2021;7:e001010. doi:10.1136/bmjsem-2020-001010

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Open access

able to accommodate for the small anticipated sample

size characteristic of elite sport populations (small
numbers anticipated in cells of contingency tables). The
null hypotheses were as follows:
H0—There is no association between TRFT and
BAMIC.
H0—There is no association between recurrence and
BAMIC.
H0—There is no association between TRFT, recur-
rence and injured muscle characteristics.
Additional descriptive analysis, not incorporated in
BAMIC, explored anatomical injury location (proximal,
middle, distal third from the sagittal and coronal images)
of specific muscles and tendon (proximal, distal) involved
(figure 1). In contrast to Pollock et al,6 linear and logistic
regression analyses were not used as assumptions for
testing were not met (linearity of variables, multivariate
normality, multicollinarity, inadequate sample size). The
level of significance was set at p<0.05. All analyses were
performed using IBM SPSS Statistics, V.26.

Ethical considerations
Written authorisation and permission to access data was
agreed by the Football Club. Participant data were stored
under an allocated personal number with no identifying
features (eg, date of birth). To ensure that no participant
can be identified, data are presented in an unattributable
format or at an aggregate level. Data are confidentially

copyright.
and securely stored for 10 years in line with research
governance procedures.

Patient involvement
No players were involved in the conduct of the study.

RESULTS
Figure 1 A schematic diagram of the left hamstring
Participants
muscle divided into proximal, middle and distal third
Thirty-­six elite football players were included with a
areas. It demonstrates the combined, approximate, free
and intramuscular tendon lengths of the proximal and median (IQR; range) age of 25 (6; range 18–36) years.
distal biceps femoris and semitendinosus muscle. The Twelve participants experienced ≥2 separate HMIs.
semimembranosus tendons are not illustrated.
Descriptive data
There were 61 HMIs from the 36 players. Median (IQR;
to coach-­
led sessions with TRFT recorded following range) TRFT following HMI was 18 (14; 2–103) days. The
consensus between clinicians. most common muscle injured was biceps femoris (n=40)
(table 1).
Statistical methods
Data were analysed consistent with Pollock et al6 as BAMIC of injuries
far as possible to enable comparison. Applying a Table 2 details the TRFT as median (IQR, range) for each
quasi-­experimental design, the relationship between BAMIC. Reinjury is presented as a percentage for each
independent (BAMIC) and dependent variables (TRFT, classification. Out of 61 HMI, n=13 (21.3%) are BAMIC
recurrence) was evaluated using the Kruskal-­Wallis (for ‘c’ (intramuscular tendon) injuries.
continuous TRFT outcome data) and Fisher’s exact test
(for two nominal variables for example, second muscle BAMIC and TRFT
injured yes/no). For analysis of anatomic site (a–c) 0 There was a statistically significant difference in TRFT
injuries were excluded as they represent normal MRIs for BAMIC (χ2=20.03, p=0.006, df=7) with a mean rank
for a, and either normal or characteristic MRIs for TRFT of 16 days for BAMIC 0a, 23 days BAMIC 0b, 12
delayed onset muscle soreness for b. All tests were non-­ days BAMIC 1a, 29 days BAMIC 1b, 23 days BAMIC 2a, 37
parametric taking into account the nature of the BAMIC days BAMIC 2b, 46 days BAMIC 2c and 33 days BAMIC
(not ordinal/ratio level data). Fischer’s exact test was 3c There were only three injuries with BAMIC grade 3c.

Shamji R, et al. BMJ Open Sp Ex Med 2021;7:e001010. doi:10.1136/bmjsem-2020-001010 3

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Table 1 Descriptive data of the study participants and the

hamstring injuries
Descriptive
Variable value
Study participants 61
 Median age in years (IQR, range) 25 (6.00; 18–36)
 Players who sustained ≥2 HMI (n) 12 (2–7 injuries)
Total no of injuries by specific muscle* (%)  
 Biceps femoris n (%) 40 (65.6)
 Semitendinosus n (%) 7 (11.5)
 Semimembranosus n (%) 10 (16.4)
Figure 2 British Athletic Muscle Injury Classification of
Median TRFT in days (IQR, range) 18 (14.00; hamstring injuries and median (IQR; range) time (days) to
2–103) return to full training (TRFT).
Reinjury (%) 10 (16.4)
 Yes, reinjury 6 (9.8) There was also a statistically significant difference in
 Yes, exacerbation 4 (6.6) TRFT for anatomical site BAMIC (a–c) excluding grade
0 (χ2=12.68, p=0.002, df=2), with a mean rank TRFT of 12
*Note n=4 grade 0a injuries days for BAMIC ‘a’, 27 days BAMIC ‘b’ and 36 days BAMIC
HMI, hamstring muscle injury; TRFT, time to return to full training.
‘c’. In particular, it can be concluded that TRFT for HMIs
with intramuscular tendon involvement (anatomical site,
Figure 2 illustrates the relationship between BAMIC and ‘c’) was statistically significantly higher than HMIs with
TRFT. no intramuscular tendon involvement (sites ‘a’ and ‘b’)
BAMIC was explored further regarding grading and (χ2=6.16, p=0.013, df=1) with a mean rank TRFT of 24
anatomical sites within muscle (a,b or c) components days for no tendon involvement and 36 days for tendon
separately. There was a statistically significant difference involvement.
in TRFT for BAMIC severity (0–3) (χ2=11.52, p=0.009,

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df=3), with a mean rank TRFT of 19 days for BAMIC 0, Injured muscle, second muscle involvment and TRFT
25 days BAMIC 1, 39 days BAMIC 2 and 33 days BAMIC 3. There was a statistically significant difference in TRFT
for injured muscle (χ2=6,23, p=0.044, df=2), with a mean
rank TRFT of 18 days for semimembranosus, 27 days for
semitendinosus, and 32 days for biceps femoris (table 3).
Table 2 TRFT and reinjury rate of HMI according to British Fisher’s exact test enabled assessment of the differences of
Athletic Muscle Injury Classification BAMIC according to injured muscle. There was a signifi-
cant difference (χ2=39.60, p=0.000) between BAMIC and
British
Athletic
injured muscle.
Muscle Injury No of Median TRFT (IQR; Reinjury Only data for Biceps femoris HMIs were possible
Classification injuries range) days n (%) to analyse descriptively. Of the n=11 BAMIC 1b biceps
femoris (long head) HMIs, three were proximal, three
0a 4 8.00 (13.75; 5–22) N/A
were middle and five were distal third injuries. Of the
0b 4 13.00 (13.75; 7–22) 1 (25) n=10 2 b biceps femoris (long head) HMIs, four were
1a 6 8.00 (9.00; 2–14) 0 proximal, two were middle and four were distal third
1b 15 17.00 (12.00; 3–34) 1 (7) injuries. Of the n=10 2 c long head HMIs, two were prox-
2a 3 12.00 (*; 3–25) 0 imal, two were middle and six were distal third injuries;
with five distal third injuries involving the distal tendon
2b 16 22.00 (14.5; 6–39) 3 (19)
and four involving a second muscle—short head biceps
2c 10 37.00 (43.00; 8–103) 4 (40) femoris.
3a Twenty HMIs involved a second muscle (32.8%), of
3b which 75% (n=15) were injuries to biceps femoris. All
3c 3 15.00 (*; 9–63) 1 (33) grade 1 or above HMIs involving a second muscle were
BAMIC ‘b’ (musculotendinous junction) or ‘c’ (intra-
4
muscular tendon).
4c TRFT for HMIs with second muscle involvement was
Total 61 18.00 (14.00; 2–103) 10 (16) statistically significantly higher than HMIs with no second
*Not possible to calculate IQR (n=3) muscle involvement (χ2=19.161, p=0.000, df=1) with a
HMI, hamstring muscle injury; N/A, not available; TRFT, time to mean rank TRFT of 42 days for second muscle involve-
return to full training. ment and 22 days for none.

4 Shamji R, et al. BMJ Open Sp Ex Med 2021;7:e001010. doi:10.1136/bmjsem-2020-001010

 Table 3 Injured muscle and specific location of injury according to British Athletic Muscle Injury classification (BAMIC)
Location injury
(proximal, middle or distal third of muscle and proximal or
BAMIC of injury Primaryinjured muscle n distal tendon involved if applicable) Second injured muscle Reinjury

0a n=4 Not applicable 4 Not applicable N N

0b Semimembranosus 1 Distal N N
Muscle n=4
Semitendinosus 3 Middle N N
Middle Semimembranosus N
Middle N Y
Biceps femoris 0      
1a Semimembranosus 2 Distal N N
Myofascial n=6
Distal N N
Semitendinosus 0      
Biceps femoris (LH) 4 Middle N N
Middle N N
Distal N N
Distal N N
1b Semimembranosus 3 Middle (prox tendon) Adductor magnus N
Muscle tendon junction n=15
Middle (prox tendon) N N
Distal (prox tendon) N N

Shamji R, et al. BMJ Open Sp Ex Med 2021;7:e001010. doi:10.1136/bmjsem-2020-001010

Semitendinosus 1 Prox (prox tendon) N N
Biceps femoris (LH) 11 Prox (prox tendon) N N
Prox (prox tendon) Semitendinosus N
Prox (distal tendon) Vastus medialis N
Middle (prox tendon) N N
Middle (prox tendon) N N
Middle (prox tendon) N N
Distal (prox tendon) N N
Distal (prox tendon) N N
Distal (distal tendon) N N
Distal (distal tendon) N N
Distal (distal tendon) N N
2a Semimembranosus 1 Distal N N
Myofascial n=3
Semitendinosus 0      
Biceps femoris (LH) 2 Middle N N
Distal N N

Continued
Open access

5
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 6
Table 3 Continued
Location injury
(proximal, middle or distal third of muscle and proximal or
BAMIC of injury Primaryinjured muscle n distal tendon involved if applicable) Second injured muscle Reinjury

2b Semimembranosus 3 Middle (prox tendon) N N

Open access

Muscle tendon junction n=16

Middle (prox tendon) Vastus lateralis N
Distal (prox tendon) N N
Semitendinosus 3 Prox (prox tendon) Biceps femoris (LH) N
Middle (prox tendon) Biceps femoris (LH) N
Distal (prox tendon) N N
Biceps femoris (LH) 10 Prox (prox tendon) N N
Prox (prox tendon) N N
Prox (prox tendon) Semitendinosus N
Prox (prox tendon) Vastus lateralis Y (Exac)
Middle (prox tendon) Semitendinosus Y
Middle (prox tendon) Semitendinosus Y
Distal (prox tendon) N N
Distal (distal tendon) N N
Distal (distal tendon) Biceps femoris (SH) N
Distal (distal tendon) Biceps femoris (SH) Y (Exac)
2c Semimembranosus 0      
Intramuscular tendon n=10
Semitendinosus 0      
Biceps femoris (LH) 10 Prox (prox tendon) N Y
Prox (prox tendon) Semitendinosus N
Middle and distal (prox tendon) Semitendinosus N
Middle and distal (prox tendon) N N
Distal (prox tendon) N N
Distal (distal tendon) N N
Distal (distal tendon) Biceps femoris (SH) N
Distal (distal tendon) Biceps femoris (SH) Y
Distal (distal tendon) Biceps femoris (SH) Y (Exac)
Distal (distal tendon) Biceps femoris (SH) Y (Exac)
3c Semimembranosus 0      
Intramuscular tendon n=3
Semitendinosus 0      
Biceps femoris (LH) 3 Middle (prox tendon) N N
Middle (prox tendon) N N
Distal (distal tendon) Biceps femoris (SH) Y

Exac, exacerbation during rehabilitation; LH, long head; N, none/no; SH, short head; Y, yes.

Shamji R, et al. BMJ Open Sp Ex Med 2021;7:e001010. doi:10.1136/bmjsem-2020-001010

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Table 4 Reinjury rate of HMI according to BAMIC site (a–c)

component only
BAMIC according to site
(a–c), excluding grade 0 No of injuries Reinjury n (%)
a 9 0
b 31 5 (16.1)
c 13 5 (38.5)
BAMIC, British Athletic Muscle Injury Classification; HMI,
hamstring muscle injury.

BAMIC and reinjury

Ten cases (16.4%) of HMI reinjury, included four cases
(40.0%) of HMI exacerbation before TRFT. Reinjury
rate involving the intramuscular tendon (‘c’) was 38.5%
(table 4). In comparison, reinjury without extension into
the intramuscular tendon (‘a’, ‘b’), excluding grade 0
injuries, was 12.5%.
Overall, there was no significant difference (χ2=10.38, Figure 3 Axial proton density fat suppressed MRI image of
p=0.083) within BAMIC according to reinjury. When an injury to the distal musculotendinous junction involving
looking at BAMIC regarding grade severity (0–4) and both the short head (BS) and long head (BL) of the biceps
site (a, b, c) components separately, there was a signifi- femoris. The semitendinosus (ST) and the semimembranosus
cant difference (χ2=8.52, p=0.024) within BAMIC severity (SM) is normal.
reinjury and (χ2=6.47, p=0.028) within BAMIC site classi-
fication according to reinjury. In particular, there was a
intramuscular tendon involvement on the TRFT seems
significant difference (χ2=5.64, p=0.031) between intra-
less clear across other studies. While it is not ideal to
muscular tendon (site ‘c’) vs no intramuscular tendon
compare medians with means, the trends are important
involvement (site ‘a’ and ‘b’) and reinjury.

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to discuss. Players with 2c and 3c injuries in this study
Injured muscle, second muscle and reinjury had a median TRFT of 37 days and 15 days, respectively.
There was no significant difference (χ2=2.94, p=0.368) In contrast, Pollock et al6 reported a mean TRFT of 27
between reinjury and injured muscle. There was a signif- days for 2c which increased to 84 days for 3c injuries.
icant difference (χ2=10.74, p=0.002) between a second The prospective study of van der Made et al11 did not use
muscle being involved (yes or no) and reinjury. BAMIC per se, but a comparison is possible as they did
There were sufficient data to descriptively analyse loca- report injuries according to the separate degrees of intra-
tion of injury for biceps femoris HMIs, with most injuries muscular tendon involvement. They report a mean TRFT
with reinjury involving the distal third section and distal of 24 days in the group equivalent to a BAMIC grade 2c
tendon site (n=5; 55.6%; n=1 2 b HMI, n=3 2 c HMI, n=1 and a mean TRFT of 25 days rising to 30 days, for addi-
3 c HMI). All five reinjuries involving this distal third tional signs of tendon waviness/loss of tension, which
section and distal tendon had evidence of injury to both would be classed as BAMIC grade 3c. It can, therefore, be
the long and short heads of biceps femoris. Notably, deduced that the median TRFT of 37 days for the BAMIC
three occurred before TRFT (ie, exacerbation during 2c injuries in this study are considerably higher than
rehabilitation) and represented three out of the four those seen in the other studies. With regards to BAMIC
exacerbations. 3c injuries, our median TRFT of 15 days, is closer to the
TRFT reported by van der Made et al,11 but considerably
DISCUSSION shorter to that reported by Pollock et al (84 days).6 It is
HMIs with any degree of intramuscular tendon involve- acknowledged however that there are low numbers of
ment are associated with increased TRFT (mean rank of BAMIC grade 3c injuries in this current study.
36 days with tendon involvement vs 24 days without) and The differences are multifactorial and require further
an increased risk of reinjury (38.5% reinjury with tendon evaluation beyond the extent of intramuscular tendon
involvement vs 12.5% without) in elite footballers. This involvement where there is a wide range of TRFT in both
study also highlights potential significance of injury to 2c (8–103 days) and 3c (9–63 days) injuries in our study.
the DMTJ of the biceps femoris. Anatomical injury location, which is not routinely catego-
rised by MRI classification beyond site within the muscle,
TRFT in HMI with intramuscular tendon involvement cannot differentiate all possible important clinical enti-
Similar to Pollock et al,6 this study shows that HMIs in elite ties which may result in the differences reported between
footballers extending into the tendon (‘c’) are associated studies. Entwisle et al12 have described the DMTJ of the
with an increased TRFT and reinjury rate. The degree of biceps femoris as a distinct clinical entity and report a

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varying degrees of intramuscular tendon injury reported

in studies.

Contextual factors
The type of sport (eg, football, sprinting, squash, rugby)
and level of participation for the athlete is also a key
consideration when comparing differences between
studies. Return to train is a continuum, paralleled with
recovery and rehabilitation.16 Some individuals will
return to full squad training earlier than other players
with similar injury classification. TRFT in team sports,
such as football, will vary according to position in team,
position on the field as well as other common contextual
circumstances such as upcoming competition, timing in
season and social and financial costs. Our study reports
TRFT in high elite level first team English football and
should therefore be considered more applicable to the
HMIs seen in this population.

Limitations
Our cohort includes professional level first team football
players only. While potentially increasing the external
validity and clinical relevance for similar football players
at this level, the lack of a sufficient number of injuries
within each category limits our statistical analyses. In
particular, there are a low number of BAMIC grade 3c vs
2c injuries. We are unable to comment on the importance
of intramuscular tendon injuries of the semimembra-

copyright.
nosus and semitendinosus as no ‘c’ injuries to these
Figure 4 Schematic diagram to demonstrate the sequential muscles were seen in our study. The clinicians involved in
axial anatomy of the distal musculotendinous junction of the decision for TRFT were not blinded to the MRI find-
the long (BL) and short (BS) head of the biceps femoris. The
ings although reference to the specific BAMIC was not
middle axial image shows the DMTJ as a T-­shaped structure.
DMTJ, distal musculotendinous T junction.
used by clinicians in the first four seasons of data collec-
tion. All images were acquired by a 1.5T MRI and greater
diagnostic accuracy might be achieved by 3.0T MRI.
reinjury rate of 54% in Australian football players. We
show increased reinjury at the distal biceps femoris CONCLUSION
related to the distal tendon, described and termed DMTJ This study provides evidence that HMIs in elite footbal-
by Entwisle et al,12 involving both the long and short head lers, involving the intramuscular tendon increases TRFT
(figure 3). This area of the biceps femoris has complex and risk of reinjury. The use of BAMIC can, therefore,
anatomy where two heads (long and short), with their provide useful information for the managing clinician.
different sites of origin and separate innervation, give However, this study shows that while knowledge of the
rise to opposing force vectors during contraction that intramuscular tendon involved in injury is helpful,
converge on and transmit through the DMTJ (figure 4).12 considering other anatomical entities may help refine
In this study, three out of four exacerbations during the wide range of TRFT seen with intramuscular tendon
graded rehabilitation occurred at this location and may involvement. We describe the potential importance of
suggest that a different approach, possibly beyond clin- recognising injury to the DMTJ of the biceps femoris
ical progression criteria are needed. Interval MRI may involving both the long and short heads.
be of value to monitor scar formation and maturation
of this aponeurotic, as opposed to a cord-­like, intramus- Twitter Ricky Shamji @p4exercise
cular tendon appearance seen at this location.12 Of note, Acknowledgements John Hartley, Rob Marshall and Steve Polley provided
intramuscular tendon appearance (aponeurotic, cord-­ invaluable insight during the process.
like) varies according to hamstring location, and between Contributors RS, AR and KAK were involved in the conception and design of
individuals, and with intramuscular tendon not behaving this study; RS and KAK were involved in the acquisition of data; RS, AR and SLJJ
like a free tendon functionally or when injured, the effect conducted the analyses; all authors were involved in interpretation of the data;
RS and AR prepared the first draft and all authors critically reviewed and revised
of the varying intramuscular tendon appearances are not this several times, with addition of important intellectual content; RS, RB and SLJJ
known.15 These factors warrant further study that may produced the illustrations; all authors gave final approval of the version to be
help us understand the wide range of TRFT seen with submitted.

8 Shamji R, et al. BMJ Open Sp Ex Med 2021;7:e001010. doi:10.1136/bmjsem-2020-001010

 BMJ Open Sport Exerc Med: first published as 10.1136/bmjsem-2020-001010 on 10 May 2021. Downloaded from http://bmjopensem.bmj.com/ on December 12, 2022 by guest. Protected by
Open access

Funding The authors have not declared a specific grant for this research from any hamstring and quadriceps muscle strains. Br J Sports Med
funding agency in the public, commercial or not-­for-­profit sectors. 2016;50:205–8.
6 Pollock N, Patel A, Chakraverty J, et al. Time to return to full training
Competing interests None declared. is delayed and recurrence rate is higher in intratendinous ('c') acute
Patient and public involvement Patients and/or the public were not involved in hamstring injury in elite track and field athletes: clinical application
the design, or conduct, or reporting, or dissemination plans of this research. of the British Athletics Muscle Injury Classification. Br J Sports Med
2016;50:305–10.
Patient consent for publication Not required. 7 Slavotinek JP, Verrall GM, Fon GT. Hamstring injury in athletes: using
MR imaging measurements to compare extent of muscle injury
Ethics approval Ethics committee of University of Birmingham.
with amount of time lost from competition. AJR Am J Roentgenol
Provenance and peer review Not commissioned; externally peer reviewed. 2002;179:1621–8.
8 Connell DA, Schneider-­Kolsky ME, Hoving JL, et al. Longitudinal
Data availability statement No data are available. All data are reported. study comparing sonographic and MRI assessments of acute and
Open access This is an open access article distributed in accordance with the healing hamstring injuries. AJR Am J Roentgenol 2004;183:975–84.
Creative Commons Attribution Non Commercial (CC BY-­NC 4.0) license, which 9 Pollock N, James SLJ, Lee JC, et al. British athletics muscle
permits others to distribute, remix, adapt, build upon this work non-­commercially, injury classification: a new grading system. Br J Sports Med
2014;48:1347–51.
and license their derivative works on different terms, provided the original work is
10 Crema MD, Guermazi A, Reurink G, et al. Can a clinical
properly cited, appropriate credit is given, any changes made indicated, and the examination demonstrate intramuscular tendon involvement
use is non-­commercial. See: http://c​ reativecommons.​org/​licenses/​by-​nc/​4.​0/. in acute hamstring injuries? Orthop J Sports Med
2017;5:232596711773343.
ORCID iD 11 van der Made AD, Almusa E, Whiteley R, et al. Intramuscular tendon
Ricky Shamji http://​orcid.​org/​0000-​0001-​8224-​8357 involvement on MRI has limited value for predicting time to return to
play following acute hamstring injury. Br J Sports Med 2018;52:83–8.
REFERENCES 12 Entwisle T, Ling Y, Splatt A, et al. Distal Musculotendinous T junction
1 Ekstrand J, Hägglund M, Waldén M. Epidemiology of muscle injuries injuries of the biceps femoris: an MRI case review. Orthop J Sports
in professional football (soccer). Am J Sports Med 2011;39:1226–32. Med 2017;5:232596711771499.
2 de Visser HM, Reijman M, Heijboer MP, et al. Risk factors of 13 von Elm E, Altman DG, Egger M, et al. The strengthening the
recurrent hamstring injuries: a systematic review. Br J Sports Med reporting of observational studies in epidemiology (STROBE)
2012;46:124–30. statement: guidelines for reporting observational studies. Lancet
3 Ekstrand J, Lee JC, Healy JC. MRI findings and return to play in 2007;370:1453–7.
football: a prospective analysis of 255 hamstring injuries in the UEFA 14 Hallén A, Ekstrand J. Return to play following muscle injuries in
elite Club injury study. Br J Sports Med 2016;50:738–43. professional footballers. J Sports Sci 2014;32:1229–36.
4 Comin J, Malliaras P, Baquie P, et al. Return to competitive play after 15 Brukner P, Cook JL, Purdam CR. Does the intramuscular tendon act
hamstring injuries involving disruption of the central tendon. Am J like a free tendon? Br J Sports Med 2018;52:1227–8.
Sports Med 2013;41:111–5. 16 Ardern CL, Glasgow P, Schneiders A, et al. 2016 consensus
5 Brukner P, Connell D. 'Serious thigh muscle strains': beware the statement on return to sport from the first world Congress in sports
intramuscular tendon which plays an important role in difficult physical therapy, Bern. Br J Sports Med 2016;50:853–64.

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