Keywords
football - muscle injuries - muscle pain - ultrasound - elastosonography
Introduction
Muscular injuries are very frequent in sports, especially in football.[1]
[2]
[3]
[4] The diagnosis of muscular injuries is clinical and mostly based on history of injury
mechanism and symptoms and on physical examination. An accurate diagnosis supported
by objective instrumental data is crucial to select the proper treatment, to prevent
future damage and to allow an early return to play in accordance with the biological
healing time.
Despite considered complementary studies, musculoskeletal ultrasound (US), elastosonography
(USE), and magnetic resonance imaging (MRI) can assess diagnosis and prognosis more
significantly than the clinical examination.[5]
[6]
[7] In 2012, Mueller-Wohlfahrt et al[8] published a new classification focusing on muscle pain, related or not to the presence
of a lesion, using clinical examination, US and MRI.
The USE allows excellent follow-up assessment of muscle and tendon injuries by demonstrating
the recovery of elasticity in the injured areas. However, no previous studies investigated
the diagnostic value of USE in acute muscle and tendon injuries.
The objective of this study was to investigate the ability of USE to discriminate
the different grades of muscular injuries by comparison with standard US and by correlation
with the clinical classification of muscular pain. Our hypothesis was that USE could
provide additional information and therefore allow for a better assessment of muscle
injuries than the standard US.
Methods
In the period between August 2014 and May 2016 (two football seasons), we conducted
a nonrandomized prospective cohort study on a population of young male professional
athletes belonging to the under-17 football club (Ancona 1905). The team has been
monitored by the same medical team belonging to the Orthopaedic Clinic of Ospedali
Riuniti, Ancona. Only players who did not have muscle injuries before the beginning
of the research were included in the study. If a player had joined or left the team
during the season, the resulting data were adjusted considering the number of days
he was observed. The study was approved by the loca Institutional Review Board and
all the athletes signed an informed consent to enter the study.
Injury recording followed the guidelines for injury definitions and data collection
procedures in studies on soccer injuries provided by Fédération Internationale de
Football Association (FIFA)—Medical Assessment and Research Centre (F-MARC). The injury
criteria adopted in this study followed the definition of time loss provided by the
Medical Committee of Union of European Football Associations: “an injury that occurred
during a scheduled training session or match that caused absence from the next training
session or match.” Injuries were recorded by the rehabilitative team of the club,
who was trained to use the F-MARC form at the beginning of the season. The injury
event was recorded immediately after it occurred, and the team's physiotherapists
recorded the match and training hours. Injuries were then classified either as “requiring
medical attention,” as “time loss” when causing the player to miss training or competition,
as “early recurrence” if occurring within 2 months from the return to play and as
“late recurrence” if occurring from 2 to 12 months from the return to play.
Injuries were described as frequency and percentage according to location, type, mechanism,
recurrence, and whether they occurred with or without contact. The incidence of injury
during matches and training was reported as the number of injuries per 1,000 hours
played. Injury recording considered the moment at which the injury occurred (match
or training), as well as severity, location, type, mechanism, and recurrence.
Injury severity was classified according to the number of days lost by the player
between the day of the injury and the return to full participation in team training,
and the availability to be selected to play; it was classified as follows: minimal
(1–5 days), mild (6–10 days), moderate (11–28 days), and severe (>28 days).[8]
[9] The number and severity of injuries were calculated as ratio with the number of
days that each player was monitored. Since a player could enter or leave the team
during the study, this normalization procedure was chosen to consider differences
of monitoring time of the players in the quantity and severity (lost days) of injuries.
Location of injury was defined according to the following categories: head/neck, upper
limbs, trunk, and lower limbs.
The type of injury was classified as fracture/bone stress, joint (nonbone)/ligament,
muscle/tendon, contusions, laceration/skin injury, and others.[8]
The mechanism of injury was classified as traumatic (i.e., resulting from a specific
and identifiable event) or overuse (i.e., caused by repeated microtraumas, even without
a simple and identifiable event).
As for muscle injuries, muscle pain was classified, after a physical examination,
according to the classification of Mueller-Wohlfahrt et al[8] ([Table 1]). Physical examination evaluated the location of spontaneous pain, tenderness to
palpation of the concerned muscle, the presence of muscle hypertonicity, functional
impairment, decreased muscle strength, increased harmed muscle volume, subcutaneous
swelling, and the presence of subcutaneous ecchymosis, if any.
Table 1
Classification of muscle disorders according to Mueller-Wohlfahrt et al[8]
|
A. Indirect muscle disorder/injury
|
Functional muscle disorder
|
Type 1: Overexertion-related muscle disorder
|
Type 1A: Fatigue-induced muscle disorder
Type 1B: Delayed-onset muscle soreness (DOMS)
|
|
Type 2: Neuromuscular muscle disorder
|
Type 2A: Spine-related neuromuscular Muscle disorder
Type 2B: Muscle-related neuromuscular Muscle disorder
|
|
Structural muscle injury
|
Type 3: Partial muscle tear
|
Type 3A: Minor partial muscle tear
Type 3B: Moderate partial muscle tear
|
|
Type 4: (Sub)total tear
|
Subtotal or complete muscle tear Tendinous avulsion
|
|
B. Direct muscle injury
|
Contusion
|
|
|
|
Laceration
|
|
|
All athletes were evaluated in the hours following the trauma/onset of pain (from
6 to a maximum of 72 hours) using a diagnostic US system (Philips iU22; Philips Healthcare,
Bothell, Washington, United States) and classified according to Mueller-Wohlfahrt
et al if one or more clinical or instrumental parameters experienced any change, by
differentiating functional disorders from structural injuries.
Musculoskeletal US and USE examination were performed by two radiologists experienced
in musculoskeletal US. The USE was performed with free-hand technique giving to the
US transducer rhythmic manual compressions on tissues under examination. A rectangular
region of interest (ROI) was used to represent the entire structure into consideration.
For the feedback, the images obtained from at least three compression/relaxation cycles
were recorded, using the intermediate images in the compression phase of each cycle
since the initial and final images are inaccurate.
The athletes were evaluated again clinically and by musculoskeletal US and USE after
7, 15, and 30 days from the date of trauma/onset of pain. Anechogenic areas of edema
or USE red areas, indicating higher tissue elasticity related to the edema or hematoma,
were highlighted.
A transducer was used to obtain specific information in USE imaging. By exerting low
pressure with the transducer in the ROI, it was possible to determine a proportional
correlation between pressure and deformation. The size of the ROI determined by the
examiner should exceed 5 mm all around the explored lesion ([Fig. 1]).
Fig. 1 3b injury of the medial head of the gastrocnemius in a professional 17-year-old football
player. US and USE performed at 48 hours (A) and 15 days (B) after trauma. US, ultrasound; USE, elastosonography.
Results
Thirty-seven male athletes were initially evaluated. Two athletes were excluded due
to a previous injury. During the season, three new athletes joined the team, and no
one suffered musculoskeletal injuries. In addition, four athletes left the team during
the season and consequently were not followed up for the entire period. At the end
of data collection, 34 athletes were examined, with an average age of 17.2 years ([Table 2]).
Table 2
Baseline characteristics of study population
|
Height (cm)
|
178.57 ± 5.65
|
|
Weight (kg)
|
64.36 ± 6.48
|
|
Body mass index (kg/m2)
|
20.20 ± 3.82
|
|
No. of matches
|
56 (26 + 30)
|
|
No. of training sessions
|
318 (150 + 168)
|
|
Match hours
|
70.2 (31.2 + 39)
|
|
Training hours
|
683.7 (330 + 369.6)
|
Overall, 318 team-training sessions (683.7 training hours) and 56 matches (70.2 match
hours) were recorded during the study period. Seventy injuries were documented in
19 players (54.3%). All injuries were “medical attention injuries.” Injury incidences
were 38.7 and 12.8 for match and training injuries, respectively. Forty-eight injuries
(71.6%) led to “time loss,” and incidences for match and training were 27.3 and 8.6
per 1,000 hours, respectively.
Traumatic injuries represented 38.6% of all injuries and the remaining were noncontact
injuries due to overuse, fatigue induced, or other clinical causes. The majority of
injuries (73%) affected lower extremities. Muscle/tendon injuries were the most common
type of injury (49%), followed by fracture/bone/stress (17%) ([Fig. 2]). Furthermore, there were three muscle reinjuries (8.8%) due to overuse; of these,
two were early and one was late recurrence. The most frequent locations of muscle
injuries were hamstrings in 11 cases (32%), triceps in 9 (26%), quadriceps in 7 (21%),
anterior and lateral calf in 4 (12%), and adductors in 3 (9%).
Fig. 2 Classification of injuries according to the type of injury.
All muscle injuries were time loss injuries, of which 41% (14 athletes) resulted in
minimal absence (5 days or less). The remaining 20 injuries (59%) resulted in absence
of more than 6 days. Of these, 12 (35%) were classified as mild (6–10 days), 4 (12%)
as moderate (11–28 days), and 4 (12%) as severe (>28 days).
At the first clinical assessment, 23 muscle disorders were classified as functional
pain, while the remaining 11 were classified as structural pain (8 due to indirect
trauma and 3 due to a direct trauma).
On subsequent evaluation (48 hours from injury), on the basis of clinical and US examination,
18 muscle pain were classified as fatigue-induced muscle disorder (FIMD, 1a), 4 as
delayed-onset muscle soreness (1b), 1 as spine-related neuromuscular disorder (2a),
2 as structural lesions (3a), 6 as 3b, and 3 as injuries from direct trauma ([Fig. 3]). The USE evaluations confirmed the clinical diagnosis and US findings. However,
areas of edema (red areas, indicating increased tissue elasticity related to the edema)
were identified in nine patients, who had been classified as FIMD (1a) ([Fig. 4]).
Fig. 3 Classification of muscle injuries according to Mueller-Wohlfahrt et al.[8] FIMD, fatigue-induced muscle disorder; MW, Mueller-Wohlfahrt.
Fig. 4 Longitudinal scanning of vastus medialis muscle. Indirect trauma in a 17-year-old
football player. (A) B-mode US shows no signs of edema or muscle injury. (B) USE shows red area (box) of soft tissue localized in the same area of the pain referred
by the athlete. US, ultrasound; USE, elastosonography.
Discussion
Muscle damage is defined as a lesion of muscle fibers without involvement of the extracellular
matrix, blood perfusion, and innervation. The amount of muscle tissue affected, the
extent, and location of the effusion define the severity of muscle trauma.[10]
[11]
[12]
[13]
[14]
Clinically, discerning 1a lesions from 3a lesions proves challenging, especially in
the early phase when blood extravasation could possibly be unnoticeable. In this case,
diagnosis should rely not only on the clinical features of the lesion but also on
US survey results, approximately 48 to 72 hours from the trauma.
Musculoskeletal US and USE are able to provide clinicians with adequate data about
muscle injury diagnosis. B-mode US does not play a large role in assessing elongations
and contractures because the absence of fiber lesions entails that there forms no
hematoma but only a moderate and diffuse intramuscular edema. USE measures tissue
deformation as a response to the application of an external force, the assumption
being that the deformation will be lower in rigid tissues, compared with elastic,
soft tissues.
Elastosonography is currently available in all US scanners. It is based on the principle
that a distinctive vibration is associated with the degree of elasticity of the tissue
being examined. The vibration, obtained by moderate tissue compression with the probe,
is translated by the software into a color map. Elastosonography allows excellent
follow-up assessment of muscle and tendon lesions by demonstrating the recovery of
elasticity in areas that have suffered injury.[15] Therefore, edema is not clearly depicted by US. On the contrary, USE could show
loss of elasticity of muscle component during compression, even in acute phase of
an indirect muscular trauma.
An early postinjury US 36 to 48 hours after the muscle trauma can provide helpful
information about any existing muscle structure problem, particularly in the presence
of hematoma or when the clinical examination indicates a functional disorder without
evidence of structural damage.[16]
In this study, USE showed areas of edema in nine lesions, which were negative at the
US examination and therefore classified as FIMD. Comparing these data with the recovery
time results, it can be highlighted that the players affected by these nine injuries
took more time to return to physical activity compared with others with injuries classified
into the same group.
We can therefore distinguish two subgroups within the FIMD group: one subgroup with
both US and USE negative, and another subgroup with negative US but positive USE (presence
of red colored areas), with the presence of edema areas not assessable with US. This
type of injury showed longer time of healing than the first type ([Fig. 5]). We may suppose that these injuries represent pre-3a-type injuries because of the
absence of confirmed structural injuries at US examination, as required by the Mueller-Wohlfahrt
et al's classification.[8] In this study, 50% of the lesions classified as 1a exhibited these characteristics.
These lesions were included in a group of “preinjury,” before 3a and within the group
of structural lesions, and they could be the prelude to a lesion because the presence
of edema and soft tissue represent an inflammatory condition and probably an existing
injury.
Fig. 5 Fifty per cent of the lesions classified as 1a exhibited characteristics of “ pretype-3
injuries” in terms of USE (red area) and of time loss and return to play. FIMD, fatigue-induced
muscle disorder; US, ultrasound; USE, elastosonography.
Our interpretation of this kind of injuries might be relevant for the treatment program
and for the outcome. Therefore, USE can be a valuable aid in the diagnosis and prognostic
evaluation of muscle injuries because it clarifies the staging of the lesion, defining
what is not perceptible with the simple B-mode US exam. USE allows for a better definition
of the acute phase and the degree of injury, particularly in 1a lesions. Through this
additional clinical information, it allows to improve the diagnosis and helps the
medical staff to plan a better functional recovery, targeted to the type of lesion.
Nonetheless, we conceive that the potential benefit of USE in the better definition
of muscle injuries should be deeply investigated in further studies before using it
routinely in sports traumatology.
