See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/340075059

A Histoarchitectural Approach to Skeletal Muscle Injury: Searching for a

Common Nomenclature

Article in Orthopaedic Journal of Sports Medicine · March 2020

DOI: 10.1177/2325967120909090

CITATIONS READS

32 1,471

13 authors, including:

Ramon Balius Marc Blasi

Generalitat de Catalunya University of Barcelona
88 PUBLICATIONS 1,113 CITATIONS 29 PUBLICATIONS 225 CITATIONS

SEE PROFILE SEE PROFILE

Carles Pedret Xavier Alomar

Clínica Diagonal. Barcelona Hospital de la Santa Creu i Sant Pau
75 PUBLICATIONS 997 CITATIONS 72 PUBLICATIONS 2,267 CITATIONS

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Human glabrous skin innervation View project

Study of new therapeutic approaches for skeletal muscle injury View project

All content following this page was uploaded by José A Vega on 24 March 2020.

The user has requested enhancement of the downloaded file.

 Consensus Statement

A Histoarchitectural Approach
to Skeletal Muscle Injury
Searching for a Common Nomenclature
Study Group of the Muscle and Tendon System from the Spanish Society of Sports
Traumatology*†

In recent years, different classifications for muscle injuries have been proposed based on the topographic location of the injury
within the bone-tendon-muscle chain. We hereby propose that in addition to the topographic classification of muscle injuries, a
histoarchitectonic (description of the damage to connective tissue structures) definition of the injury be included within the
nomenclature. Thus, the nomenclature should focus not only on the macroscopic anatomy but also on the histoarchitectonic
features of the injury.
Keywords: muscle injuries; sport injuries; extracellular matrix; connective tissue; muscle injury anatomy

Skeletal muscle is composed of skeletal muscle cells and the collagen molecules, proteoglycans, and noncollagenous
surrounding connective tissue distributed in a highly orga- extracellular matrix proteins such as laminin, fibronectin,
nized manner. Naturally, this organ is supplied by small and other adhesion molecules.37 For clinical applications,
vessels, capillaries, and nerves and also contains a variable the concept of the extracellular matrix of skeletal muscle is
number of cells from the immune system.14,17 Skeletal mus- usually simplified; it is considered simply as the connective
cle cells are cylindrical and striated multinucleated cells tissue structure that surrounds the muscle and is crucial
called myofibers due to their elongated shape, and their for the mechanical integrity of the tissue. This connective
main function is to generate contractile forces for locomo- structure is also known by the global term fascia.1
tion.30 Connective tissue has its own cells: fibroblasts. The fibrous collagen networks are arranged in 3 differen-
Depending on where it is located in the muscle, this con- tiated layers in the muscle belly: endomysium, perimysium,
nective tissue shows marked differences in the composition and epimysium.1,14 The endomysium surrounds each indi-
and specific distribution of the extracellular matrix mole- vidual myofiber and is composed mainly of collagen types I,
cules. These variable features make it more or less orga- III, and V.16 The perimysium surrounds several fascicles of
nized with variable flexibility, thereby carrying out myofibers and is composed mainly of collagen types I and
different yet highly specific functions within the III. The epimysium surrounds the entire muscle and is also
muscle.15,17 Thus, the extracellular matrix plays a key role composed mainly of collagen types I and III. Beyond these 3
in maintaining the structure and organization of muscle structures, type IV collagen is mainly expressed in the basal
fibers, is highly integral to force transmission, and is essen- membrane of the myofiber.19 These 3 structures make up
tial for the proper regeneration following injury.14,22,24,38 what is known as the myofascial junction (MFJ) between
Furthermore, the extracellular matrix generates biochem- muscle and fascia or the myotendinous junction (MTJ)
ical signals that regulate myogenesis and modulate various between muscle and tendon, which mainly has structural
growth factors.6,13,39 function but may also have a mechanical function.5
In terms of cell biology, the extracellular matrix of mus- The aponeuroses have a direct connective continuum
cle consists of 3-dimensional networks made of different with the MFJ via the perimysium.14 Histologically, the
perimysium joins the aponeurosis at the ends of the muscle
fascicles, facilitating the overall functional unity of the
*Address correspondence to Ramon Balius, MD, PhD, Consell Català
skeletal muscle between the MFJ and the tendons them-
de l’Esport, Generalitat de Catalunya, Av. dels Paı̈sos Catalans, 12, 08950
Esplugues de Llobregat, Barcelona, Spain (email: ramonbaliusmatas@ selves (Figure 1).
gmail.com). In a muscle injury, a myoconnective junction (MCJ) is
†
All authors are listed in the Authors section at the end of this article. always involved. This MCJ can be located in a myotendi-
Final revision submitted January 10, 2020; accepted January 10, 2020. nous junction (MTJ) when the lesion affects an aponeurosis
The Orthopaedic Journal of Sports Medicine, 8(3), 2325967120909090
or a tendinous expansion attached to muscle fiber or when
DOI: 10.1177/2325967120909090 it involves an MFJ, that is, when the muscle fiber is
ª The Author(s) 2020 attached to the epimysium or perimysium.

This open-access article is published and distributed under the Creative Commons Attribution - NonCommercial - No Derivatives License (https://creativecommons.org/
licenses/by-nc-nd/4.0/), which permits the noncommercial use, distribution, and reproduction of the article in any medium, provided the original author and source are
credited. You may not alter, transform, or build upon this article without the permission of the Author(s). For article reuse guidelines, please visit SAGE’s website at
http://www.sagepub.com/journals-permissions.

1
2 Study Group of the Muscle and Tendon System from SETRADE The Orthopaedic Journal of Sports Medicine

Figure 1. Outline of the global functional unit of skeletal muscle. A connective continuum is seen from the endomysium to the
tendon-aponeurosis via the union of the perimysium to the aponeurosis.

TABLE 1 differentiated at the level of gross anatomy (in the dissec-

Injuries to the Myoconnective Junctiona tion room or in the operating theater).5 The weakest part of
the bone-tendon-muscle chain in adults is the MCJ. Inju-
Injury of the peripheral MCJ (MTJ-MFJ continuum) ries can be located at 2 levels (the peripheral MCJ and the
Injury of the MTJ internal or central MCJ) if the muscle contains internal
Tendinous (or aponeurotic) injury fascia structure.
Myotendinous (or myoaponeurotic) injury
Muscle (or intramuscular) injury
Injury of the MFJ Peripheral MCJ Injuries
Without rupture of the epimysium
With rupture of the epimysium Peripheral MCJ injuries mainly affect the MTJ (ie, the
Injury of the internal or central MCJ muscle-aponeurosis [or tendon] interface). These are
Tendinous (or aponeurotic) injury the most common types of injury in the hamstring ten-
Myotendinous (or myoaponeurotic) injury
don, the posterior aponeurosis of the rectus femoris,
Muscle (or intramuscular) injury
and the medial head of the gastrocnemius (ie, tennis
a
MCJ, myoconnective junction; MFJ, myofascial junction; MTJ, leg). In addition, the areas adjacent to the MTJ can be
musculotendinous junction. affected at varying distances, specifically in the peri-
mysium and epimysium (ie, in the nearby MFJ). This
type of injury can occur proximal to the posterior apo-
NOMENCLATURE OF MUSCLE INJURIES BASED neurosis of the rectus femoris, at the level of its
ON ANATOMY: OPTIMIZING THE TOPOGRAPHIC epimysium.
LEVEL OF INJURY Classically, injuries that occur in the periphery of a mus-
cle tend to be called myofascial injuries. Indirect MFJ inju-
Different classifications for muscle lesions have been ries are infrequent because myotendinous injuries in the
proposed based on the topographic location of the muscle periphery are often erroneously interpreted as myo-
lesion7,26,28,34 but without accurate identification of its fascial injuries. Myofascial injuries are usually produced by
level. All indirect muscle injuries occur in MCJs, either traction of the epimysium-perimysium from a proximal
at the tendinous aponeurotic level in the MTJ or in the aponeurosis, which can break it or damage its connection
MFJ (epimysium, perimysium). To distinguish injuries to the muscle fiber.
to the MCJ, we divide the injuries into 2 main cate-
gories: MTJ and MFJ injuries (Table 1). We propose Central MCJ Injuries
that an MCJ is always involved in a skeletal muscle
injury. The affected MCJ can be located either in an Internal or central MCJ injuries are those affecting the
MTJ (the lesion affects an aponeurosis or a tendinous central tendon. These injuries are the intramuscular
expansion attached to muscle fibers) or in the MFJ, homolog of peripheral MCJ injuries except that they are
when the injury involves muscle fiber and their perimy- surrounded on all surfaces by muscle fascicles and the
sium and/or epimysium. corresponding perimysium. The main difference between
Although MCJs may be similar to the MTJ from a the 2 is that the internal or central MCJ lacks the char-
histological point of view, their macroscopic appearance is acteristic external lining of the muscle (epimysium). Typ-
determined by their thicknesses (tendon > aponeurosis > ical examples of this type of injury are those of the
myofascia).5 Thus, the 2 opposite end components of the indirect tendon of the rectus femoris and those of the
continuum between an MTJ and the MFJ can be clearly central tendon of the soleus.
The Orthopaedic Journal of Sports Medicine Histoarchitectural Approach to Skeletal Muscle Injury 3

Figure 2. Three different central tendon injuries of the rectus femoris according to their tendinous gap. Sagittal and axial
T2-weighted fat-saturated magnetic resonance imaging scans of (A) a transversal tendon gap (arrows), (B) a longitudinal tendon
gap (split, arrows), and (C) a mixed tendon gap: longitudinal (arrows) and transversal (arrowheads).

HISTOLOGICAL NOMENCLATURE OF
MUSCLE INJURIES: OPTIMIZING THE
HISTOARCHITECTURE OF THE INJURY

To understand the behavior of a muscle injury, provide an

accurate prognosis, and understand why some injuries
recur, one needs take into account not only the anatomic
and topographic location but also the type and level of his-
toarchitectural involvement (ie, degree of damage to con-
nective tissue structure) (Table 1). Two injuries in exactly
the same topographic location and with the same treatment
can heal differently depending on the degree of the damage
to the connective tissue component (ie, the extent of dam- Figure 3. Myotendinous injury located in the anterior aponeu-
age to its extracellular matrix).5 rosis of the soleus (arrows). (A) Sagittal and (B) axial
Injuries of either MCJ—peripheral or central-internal— T2-weighted fat-saturated magnetic resonance imaging
may have different degrees of histoarchitectural involve- scans. The aponeurosis is affected focally by small retraction
ment. In this work, we have updated the nomenclature of the muscle fiber.
with respect to that in a previous report5 through broad
discussions and have ultimately reached a consensus with
Muscle (Intramuscular) Injuries
more authors. Thus, we can define different types of injury
depending on their histoarchitecture. Muscle injuries occur in the interface between the perimy-
sium and the fiber or muscle fascicle to which it is attached
Tendinous (Aponeurotic) Injuries but with no direct involvement of the tendon or aponeuro-
sis, as the rupture occurs at a distance from them. These
Tendinous injuries have direct aponeurotic involvement, injuries are generally secondary to traction at a distance
with an observable gap in the tendinous tissue. In turn, this from an aponeurosis or tendon. In these cases, the injury is
gap can have different orientations, such as transversal, lon- usually called intramuscular, although, in fact, the MCJ is
gitudinal (in splits), or mixed orientation. Retraction of the also involved (Figure 4).
muscle fibers is observed only when a transverse gap is pre-
sent. Similarly, fibrous repair secondary to a transverse rup- Myofascial Injuries (Injuries in the MFJ)
ture is greater than that following longitudinal rupture, and
thus, these injuries have a greater chance of reinjury. In The affected MFJ is located in the peripheral MCJ and may
short, it is essential to assess the type of rupture to guide or may not damage the epimysium. If the epimysium is
prognosis and assess the risk of reinjury (Figure 2). intact, bleeding occurs in the muscle and is limited by the
epimysial fascia (Figure 5). If the epimysium breaks, the
Myotendinous (Myoaponeurotic) Injuries edema and fluid migrate along the intermuscular planes;
because the epimysium is composed of a variable amount of
Myotendinous injuries are located at the interface between loose connective tissue20 that has marked distensibility, it
the aponeurosis and the fiber or muscle fasciculus (and its is deformed by the bleeding itself. Clinically, these injuries
corresponding perimysium). In this type of injury, the ten- are very well tolerated and even may go unnoticed.
don or aponeurosis is affected either focally by small muscle The healing time of an injury is always longer if the injury
fiber tears or by major tears that produce a muscle gap but affects the tendon-aponeurotic structures. Although mag-
not a tendinous gap (Figure 3). netic resonance imaging (MRI) assessment of the muscle fiber
4 Study Group of the Muscle and Tendon System from SETRADE The Orthopaedic Journal of Sports Medicine

2. Topographical anatomic level: peripheral MCJ or inter-

nal (or central) MCJ
3. Nominal anatomic level: specific name of the injured
structure according to international anatomic
terminology

In addition to this nomenclature, which is not a classifi-

cation, other important clinical details should be added,
such as the presence or absence of hematoma or the dis-
tance from the tendon insertion, which for some muscles is
known to be an important contributing factor for manage-
ment and prognosis.

ANALYSIS OF TYPICAL INJURIES

ACCORDING TO THE MODEL
Hamstring Tendons

The role of intramuscular tendon involvement is controver-

sial.35 Of the various prognostic factors implicated in inju-
ries of the common hamstring tendon, involvement of the
Figure 4. A case of intramuscular injury in the rectus femoris “free tendon” (distance from bony origin or insertion to the
(arrows). (A) Coronal and (B) sagittal T2-weighted fat- point where muscle tissue starts) is particularly important
saturated magnetic resonance imaging scans. This type of regarding return-to-play (RTP) time and risk of reinjury.2,3
injury entails no direct or indirect involvement of the tendon Another important factor is the distance from the injury to
or aponeurosis, even though the injury has actually been the origin of the hamstring, with shorter distances being
caused by the traction of a myoconnective junction, in this associated with longer RTP.3,12,32 This is consistent with our
case by the central tendon of the rectus femoris. proposed model for understanding muscle injuries. Tendon
injury has the worst prognosis21,28; the closer the injury
occurs to the tendon origin or insertion, the larger the con-
may predict regeneration in approximately 3 weeks,23,25 the nective tissue lesion. Other important prognostic factors,
repair takes considerably longer when the injury involves the although not as important as the ones mentioned above, are
tendon or aponeurosis.8,28,29 This highlights the need to the length of edema,9,31 its cross-sectional area,2,9,31,33 its
account for connective tissue or fascial involvement in the volume,2 and the degree of injury.11 These factors, combined
clinical assessment of the injury. Furthermore, injury can with information on location and histoarchitectural involve-
cause damage to all 3 levels of histoarchitectonic structures, ment, could help to determine the true prognosis of proximal
leading to an even more uncertain prognosis. hamstring injuries more accurately.
In previous reports, some authors have proposed that Injuries to the distal MTJ of the biceps femoris present a
injuries in the internal or central MCJ do not have a worse special clinical challenge due to its complex anatomic struc-
prognosis than those in the peripheral MCJ,36,37 which is ture and dual innervation to the short and long head of the
justified if the level and degree of histoarchitectural muscle.11 As the long and short head of the biceps femoris
involvement are taken into account rather than just the merge together at the distal MTJ, they form a T-shaped apo-
location (central or peripheral). Thus, some injuries of the neurosis. Injuries occurring in this region are demanding to
central MCJ without connective tissue damage or involve- treat; despite long rehabilitation times, the recurrence rates
ment (muscle injury or intramuscular injury) may have a are the highest among skeletal muscle injuries reported to
better prognosis than some peripheral injuries that do have date, as more than 50% of patients sustain reinjury.11
connective tissue damage or involvement. Because the maturation of scar tissue is a slow process, it has
been recommended that MRI be used to determine proper
scar maturation before RTP can be considered.11
Proposal to Standardize the Nomenclature
We can observe all 3 types of histoarchitectonic involve-
To standardize the nomenclature of muscle injuries according ment in the common hamstring tendon in daily clinical
to the model presented here, which we hope will facilitate practice: direct tendon involvement with gap (Figure 6A),
communication between professionals and ultimately lead to purely myotendinous injury without gap (Figure 6B), and
more accurate clinical diagnoses, we propose the following muscle injury produced by traction of the common tendon
requirements for describing muscle injuries: but without direct contact with it (Figure 6C). Comin et al8
used MRI to study gaps or fiber retractions in the central
1. Histoarchitectonic level: tendinous (or aponeurotic), tendon and found these factors to be associated with signif-
myotendinous (myoaponeurotic), muscle (or intramus- icantly longer RTP times than injuries without these fac-
cular), or myofascial injury tors. In this sense, an injury with a tendinous gap leads to
The Orthopaedic Journal of Sports Medicine Histoarchitectural Approach to Skeletal Muscle Injury 5

Figure 5. A case of myofascial injury close to the proximal part of the posterior aponeurosis of the rectus femoris (arrows).
(A) Coronal, (B) sagittal, and (C) axial T2-weighted fat-saturated magnetic resonance imaging scans. In this case, since the
epimysium is intact, bleeding occurs in the muscle but is limited by the epimysial fascia.

Figure 6. Three different cases of common tendon injury of the biceps femoris. Coronal and axial T2-weighted fat-saturated
magnetic resonance imaging scans of (A) a tendinous rupture (arrow), (B) a myotendinous rupture (arrow), and (C) an intramuscular
rupture (arrow).
the retraction of the affected myofibers, and the time Central Tendon of the Soleus
required to repair the injured connective tissue results in
a longer duration before RTP. In a series of 100 calf injuries, Prakash et al29 observed that
Next, we provide a few representative examples from interruption of the muscle connective tissue resulted in a
common and clinically demanding skeletal muscle injuries. longer recovery time and a longer RTP time than injuries
6 Study Group of the Muscle and Tendon System from SETRADE The Orthopaedic Journal of Sports Medicine

Figure 7. Two different cases of central tendon injury of the soleus. (A) Axial T1-weighted and axial and sagittal T2-weighted fat-
saturated magnetic resonance imaging (MRI) scans of tendinous rupture. The arrows indicate the tendon gap in both T1-weighted
and T2-weighted images. (B) Axial T1-weighted and axial and sagittal T2-weighted fat-saturated MRI scans of myotendinous
rupture. The arrows indicate the integrity of the central tendon in both T1-weighted and T2-weighted images.

Figure 8. Five different cases of posterior aponeurosis injury. Sagittal and axial T2-weighted fat-saturated magnetic resonance
imaging scans of (A) a tendinous rupture (with posterior aponeurosis retracted), (B) a myotendinous rupture, (C) an intramuscular
rupture, (D) a myoaponeurotic rupture, and (E) a myofascial injury. (F) Scheme in relation to these injuries. The white solid arrows
indicate the posterior aponeurosis; the white and black dashed arrows indicate the injury.

that did not affect the central tendon of the soleus. in the peripheral MCJ.27,29 This rule also applies for the
Although no reported studies have focused only on injuries central tendon of the rectus femoris.4,10
of the central tendon of the soleus, it seems likely that a
central tendon injury with tendon gap (Figure 7A) will have Posterior Aponeurosis of the Rectus Femoris
a more complex progression than an injury in which the
connective structure is not damaged (Figure 7B). This According to Cross et al,10 injuries in the posterior periph-
should be taken into account when one is evaluating an eral MCJ of the rectus femoris have a faster RTP than those
injury to this muscle. In general, injuries affecting the ten- in the central MCJ of the central tendon. If the injury
don of the central MCJ entail a longer RTP time than those occurs in the distal part of the posterior aponeurosis, one
The Orthopaedic Journal of Sports Medicine Histoarchitectural Approach to Skeletal Muscle Injury 7

may observe a tendinous, myotendinous, or intramuscular Chile, Chile); Ricard Pruna, MD, PhD (FC Barcelona Med-
injury (Figure 8, A-C, respectively). If the injury is located ical Services, FIFA Medical Center of Excellence, Barce-
in the proximal part of the peripheral MCJ, this may affect lona, Spain); Jordi Ard èvol, MD, PhD (Department of
the posterior aponeurosis itself (myoaponeurotic injury) Orthopedic and Trauma Surgery, Hospital Asepeyo, Sant
(Figure 8D) and/or the epimysium (myofascial injury) prox- Cugat, Spain); Guillermo Álvarez, MD (AMS Centro
imal to it (Figure 8E). True myofascial injuries are those Médico del Ejercicio, Málaga, Spain); Javier de la Fuente,
that affect the epimysium only. In the peripheral MCJ of MD, PhD (Pakea Clinic of Mutualia, San Sebastián, Spain);
the rectus femoris, pure myofascial injuries are usually Tom ás Fern ández-Ja én, MD, PhD (Clı́nica CEMTRO,
located in the posterolateral area18 and are accompanied Madrid, Spain; Cátedra de Traumatologı́a del Deporte,
by interfascial hematoma. In routine clinical practice, this Facultad de Medicina, Universidad Católica de Murcia,
injury is very well-tolerated and can be a casual finding. Murcia, Spain); Tero A.H. Järvinen, MD, PhD (Faculty of
Medicine and Health Technologies, Tampere University,
Tampere, Finland; Department of Orthopedics & Trauma-
CONCLUSION tology, Tampere University Hospital, Tampere, Finland);
and Gil Rodas, MD, PhD (FC Barcelona Medical Services,
We propose that an exact description of the affected MCJ, FIFA Medical Center of Excellence, Barcelona, Spain).
together with knowledge of any histoarchitectural damage
to the connective tissue structures, improves our under-
standing of the clinical characteristics of the injured skele- REFERENCES
tal muscle. These rules, in turn, can be applied to all 1. Adstrum S, Hedley G, Schleip R, et al. Defining the fascial system.
skeletal muscle injuries. Considering clinical experience J Bodyw Mov Ther. 2017;21:173-177.
and evidence from published studies, we propose that when 2. Askling CM, Tengvar M, Saartok T, et al. Acute first-time hamstring
an injury in the MCJ has a tendon gap that is detectable by strains during high-speed running: a longitudinal study including clin-
MRI, the injury will heal more slowly and pose a greater ical and magnetic resonance imaging findings. Am J Sports Med.
2007;35:197-206.
risk of reinjury than would an injury without such a con-
3. Askling CM, Tengvar M, Saartok T, et al. Acute hamstring injuries in
nective tissue lesion. Similarly, the injury has a better prog- Swedish elite football: a prospective randomized controlled clinical
nosis if it is purely muscular or if it is myofascial but trial comparing two rehabilitation protocols. Br J Sports Med. 2013;
without clear involvement of the neighboring tendon (or 47:953-959.
aponeurosis). Moreover, all 3 types of histoarchitectonic 4. Balius R, Maestro A, Pedret C, et al. Central aponeurosis tears of the
involvement can co-occur in the same injury, and it is very rectus femoris: practical sonographic prognosis. Br J Sports Med.
2009;43:818-824.
difficult to make an accurate prognosis in these cases. How-
5. Balius R, Alomar X, Pedret C, et al. Role of the extracellular matrix in
ever, the determination of scar tissue maturity by MRI muscle injuries: histoarchitectural considerations for muscle injuries.
might be helpful during follow-up to ascertain readiness Orthop J Sports Med. 2018;6:2325967118795863.
to RTP. 6. Blasi M, Blasi J, Domingo T, et al. Anatomical and histological study of
human deep fasciae development. Surg Radiol Anat. 2015;37:
571-578.
7. Chan O, Del Buono A, Best TM, et al. Acute muscle strain injuries: a
AUTHORS proposed new classification system. Knee Surg Sports Traumatol
Arthrosc. 2012;20:2356-2362.
Study Group of the Muscle and Tendon System from the 8. Comin J, Malliaras P, Baquie P, et al. Return to competitive play after
Spanish Society of Sports Traumatology; Ramon Balius, hamstring injuries involving disruption of the central tendon. Am J
MD, PhD (Consell Català de l’Esport, Generalitat de Cata- Sports Med. 2013;41:111-115.
lunya, Barcelona, Spain; Sports Medicine and Clı́nical 9. Connell DA, Schneider-Kolsky ME, Hoving JL, et al. Longitudinal
Ultrasound Department, Clı́nica Diagonal, Barcelona, study comparing sonographic and MRI assessments of acute and
healing hamstring injuries. AJR Am J Roentgenol. 2004;183:
Spain); Marc Blasi, MD (Department of Fundamental Care
975-984.
and Medical-Surgical Nursing, Faculty of Medicine and 10. Cross TM, Gibbs N, Houang MT, et al. Acute quadriceps muscle
Health Sciences, Bellvitge Campus, University of Barce- strains: magnetic resonance imaging features and prognosis. Am J
lona, Barcelona, Spain; Àrea d’Estructura i Funció del Cos Sports Med. 2004;32:710-719.
Humà, Facultat de Medicina i Ciències de la Salut, Univer- 11. Entwisle T, Ling Y, Splatt A, Brukner P, Connell D. Distal musculoten-
sitat Internacional de Catalunya, Barcelona, Spain); Carles dinous T junction injuries of the biceps femoris: an MRI case review.
Orthop J Sports Med. 2017;5(7):2325967117714998.
Pedret, MD, PhD (Sports Medicine Department, Clinica
12. Ekstrand J, Healy JC, Walden M, et al. Hamstring muscle injuries in
Creu Blanca, Barcelona, Spain; Sports Medicine and Clı́ni- professional football: the correlation of MRI findings with return to
cal Ultrasound Department, Clinica Diagonal, Esplugues play. Br J Sports Med. 2012;46:112-117.
de Llobregat, Spain); Xavier Alomar, MD, PhD (Clı́nica 13. Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a
Creu Blanca, Barcelona, Spain); José Peña-Amaro, MD, glance. J Cell Sci. 2010;123:4195-4200.
PhD (Department of Morphological Sciences, Histology 14. Gillies AR, Lieber RL. Structure and function of the skeletal muscle
Section, Faculty of Medicine, University of C órdoba, extracellular matrix. Muscle Nerve. 2011;44:318-331.
15. Grounds MD. Complexity of Extracellular Matrix and Skeletal Muscle
Maimónides Institute for Biomedical Research IMIBIC, Regeneration: Skeletal Muscle Repair and Regeneration. Dordrecht,
Córdoba, Spain); José A. Vega, MD, PhD (Department of the Netherlands: Springer Netherlands; 2008:269-302.
Morphology and Cell Biology, University of Oviedo, Spain; 16. Jakobsen JR, Mackey AL, Knudsen AB, et al. Composition and adap-
Faculty of Health Sciences, Autonomous University of tation of human myotendinous junction and neighboring muscle fibers
8 Study Group of the Muscle and Tendon System from SETRADE The Orthopaedic Journal of Sports Medicine

to heavy resistance training. Scand J Med Sci Sports. 2017;12: 29. Prakash A, Entwisle T, Schneider M, et al. Connective tissue injury in
1547-1559. calf muscle tears and return to play: MRI correlation. Br J Sports Med.
17. Jarvinen TA, Jarvinen TL, Kaariainen M, et al. Muscle injuries: biology 2018;52:929-933.
and treatment. Am J Sports Med. 2005;33:745-764. 30. Sambasivan R, Tajbakhsh S. Adult skeletal muscle stem cells. Results
18. Kassarjian A, Rodrigo RM, Santisteban JM. Current concepts in MRI Probl Cell Differ. 2015;56:191-213.
of rectus femoris musculotendinous (myotendinous) and myofascial 31. Schneider-Kolsky ME, Hoving JL, Warren P, et al. A comparison
injuries in elite athletes. Eur J Radiol. 2012;81:3763-3771. between clinical assessment and magnetic resonance imaging of
19. Kovanen V. Intramuscular extracellular matrix: complex environment acute hamstring injuries. Am J Sports Med. 2006;34:1008-1015.
of muscle cells. Exerc Sport Sci Rev. 2002;30:20-25. 32. Silder A, Sherry MA, Sanfilippo J, et al. Clinical and morphological
20. Langevin HM, Huijing PA. Communicating about fascia: history, pit- changes following 2 rehabilitation programs for acute hamstring strain
falls, and recommendations. Int J Ther Massage Bodywork. 2009;2: injuries: a randomized clinical trial. J Orthop Sports Phys Ther. 2013;
3-8. 43:284-299.
21. Macdonald B, McAleer S, Kelly S, Chakraverty R, Johnston M, Pol- 33. Slavotinek JP, Verrall GM, Fon GT. Hamstring injury in athletes: using
lock N. Hamstring rehabilitation in elite track and field athletes: apply- MR imaging measurements to compare extent of muscle injury with
ing the British Athletics muscle injury classification in clinical practice. amount of time lost from competition. AJR Am J Roentgenol. 2002;
Br J Sports Med. 2019;53(23):1464-1473. 179:1621-1628.
22. Mackey AL, Kjaer M. The breaking and making of healthy adult human 34. Valle X, Alentorn-Geli E, Tol JL, et al. Muscle injuries in sports: a new
skeletal muscle in vivo. Skelet Muscle. 2017;7:24. evidence-informed and expert consensus-based classification with
23. Mackey AL, Magnan M, Chazaud B, et al. Human skeletal muscle clinical application. Sports Med. 2017;47(7):1241-1253.
fibroblasts stimulate in vitro myogenesis and in vivo muscle regener- 35. Van der Made AD, Almusa E, Whiteley R, et al. Intramuscular tendon
ation. J Physiol. 2017;595:5115-5127. involvement on MRI has limited value for predicting time to return to
24. Mahdy MAA. Skeletal muscle fibrosis: an overview. Cell Tissue Res. play following acute hamstring injury. Br J Sports Med. 2018;52:83-88.
2019;375(3):575-588. 36. Van der Made AD, Almusa E, Reurink G, et al. Intramuscular tendon
25. Marotta M, Sarria Y, Ruiz-Roig C, et al. Laser microdissection-based injury is not associated with an increased hamstring reinjury rate within
expression analysis of key genes involved in muscle regeneration in 12 months after return to play. Br J Sports Med. 2018;52:1261-1266.
mdx mice. Neuromuscul Disord. 2007;17:707-718. 37. Velleman SG, Shin J, Li X, Song Y. Review: the skeletal muscle extra-
26. Mueller-Wohlfahrt H-W, Haensel L, Mithoefer K, et al. Terminology cellular matrix: possible roles in the regulation of muscle development
and classification of muscle injuries in sport: the Munich consensus and growth. Can J Anim Sci. 2012;92:1-10.
statement. Br J Sports Med. 2013;47:342-350. 38. Wang Z, Tang Z. Composition and function of extracellular matrix in
27. Pedret C, Rodas G, Balius R, et al. Return to play after soleus muscle development of skeletal muscle. In: Travascio F, ed. Composition and
injuries. Orthop J Sports Med. 2015;3:2325967115595802. Function of the Extracellular Matrix in the Human Body. Rijeka, Croa-
28. Pollock N, James SLJ, Lee JC, et al. British athletics muscle injury tia: InTech; 2016:25-43.
classification: a new grading system. Br J Sports Med. 2014;48: 39. Yue B. Biology of the extracellular matrix: an overview. J Glaucoma.
1347-1351. 2014;23:20-23.

View publication stats