Journal of Bodywork & Movement Therapies (2016) 20, 377e387

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FASCIA SCIENCE AND CLINICAL APPLICATIONS: MUSCLE ARCHITECTURE

FASCIA SCIENCE AND CLINICAL APPLICATIONS: MUSCLE ARCHITECTURE

Fascial hierarchies and the relevance of

crossed-helical arrangements of collagen to
changes in the shape of muscles*
Graham Scarr, CBiol., FRSB., FLS., DO*

60 Edward Street, Stapleford, Nottingham, NG9 8FJ, UK

Received 27 October 2014; received in revised form 5 September 2015; accepted 30 September 2015

KEYWORDS Summary Muscles are composite structures consisting of contractile myofibres surrounded
Collagen; by complex hierarchies of collagen-reinforced fascial sheaths. They are essentially flexible cyl-
Crossed-helix; inders that change in shape, with the particular alignment of collagen fibres within their myo-
Crossed-ply; fascial walls reflecting the most efficient distribution of mechanical stresses and coordinating
Epimysium; these changes. However, while the functional significance of this crossed-helical fibre arrange-
Fascia; ment is well established in other species and in different parts of the body, relatively little
Helix; attention has been given to this within the fascia of humans; and the relevance of this geomet-
Muscle; ric configuration to muscles and surrounding fascial tissues is described.
Myofascia; ª 2015 Elsevier Ltd. All rights reserved.
Pennation;
Perimysium

Introduction et al., 2012). Once dismissed as a packing tissue of little

The fascia
The importance of the fascia to normal function has been
recognized by ‘hands-on’ practitioners for more than a
century (Still, 1899; Findley and Shalwala, 2013) but it
is only recently that it has emerged as a significant
contributor to mainstream orthopaedic knowledge (Schleip
*
The author is an independent researcher with no funding or
institutional affiliation, and there are no conflicts of interest.
* Tel.: þ44 115 9491753.
E-mail address: gscarr3@ntlworld.com.
consequence, the fascia is now recognized as a continuous
interconnected network that permeates and envelops
almost every part of the body and is now taking its rightful
place at the ‘top table’ of anatomical and physiological
research.
The term ‘fascia’ refers to dense planar tissue sheets
such as the ‘deep’ or ‘investing’ fascia (fascia profunda),
septa, aponeuroses, joint and organ capsules, the epimy-
sium that surrounds muscles; and the softer ‘superficial’
fascia beneath the skin, the intra-muscular endomysium
that surrounds individual muscle fibres; and perimysium
that surrounds bundles of these fibres. It also includes the
dura mater, periosteum, neurovascular sheaths and
abdominal mesentery etc, and is continuous with ‘non-

http://dx.doi.org/10.1016/j.jbmt.2015.09.004
1360-8592/ª 2015 Elsevier Ltd. All rights reserved.
 378
fascial’ densifications in the form of ligaments, tendons
(Benjamin, 2009; Schleip et al., 2012), periosteum and
bone (Aaron, 2012).
The internal structure of these fascial sheets consists of
an extra-cellular matrix (ECM) containing highly hydrated
proteoglycan complexes (‘ground substance’) and a variety
of cells and interlinked fibres (Gillies and Lieber, 2011), and
is continuous with the ECM that surrounds virtually every
cell in the body. A fibrillar collagen and elastin network also
FASCIA SCIENCE AND CLINICAL APPLICATIONS: MUSCLE ARCHITECTURE
encloses proteoglycan ‘microvacuoles’, which surround and
blend with tendons, aponeuroses, skin, nerves and blood
vessels etc so that at the microscopic level there is no
distinct boundary between where one ends and another
begins (Guimberteau, 2005, 2012).
Unfortunately, it is this anatomical continuity and the
pervasiveness of fascial tissues at every size scale that has
confounded anatomists over the centuries and maintained
this connective tissue matrix as the “Cinderella of ortho-
pedic science” (Schleip et al., 2012 p xv); but a new and all
encompassing classification system based on density and
fibre alignment is now able to relate them all together in a
useful way (Schleip et al., 2012 p xvii). The myofascia is
then just a fibrous specialization that is intimately con-
nected with muscle, and the crossed-helical orientation of
collagen fibres within it and the surrounding fascia play
important functional roles that deserve wider recognition.
The fascia
Myofascia
The myofascia is traditionally classified into three different
regions (Turrina et al., 2013), which together form a hier-
archical network of fibrous tubes or sheaths enclosing
smaller tubes within them, and is continuous with ‘higher-
level’ fascial tubes (compartments) that surround groups of
muscles, the limbs and entire body (Fig. 1). Although some
Figure 1 Schematic diagrams of (a) a transverse section of muscle showing the general hierarchical arrangement of myofascial
‘tubes’ surrounding the myofibres (not to scale); (b) transverse section of the human thigh showing the ‘higher-level’ fascial tubes
consisting of muscle septa and the deep ‘investing’ fascia surrounding individual muscles and the entire limb. Reproduced with
modifications from Scarr (2014) Handspring.
G. Scarr
authors consider that the myofascia should no longer be
considered as a collection of ‘tubes’ or ‘sheaths’, as it is
really a “three-dimensional matrix that is continuous
throughout the entire organ” (Purslow and Delage, 2012 p
5) and “tremendously complex compared with other con-
nective tissues” (Gillies and Lieber, 2011 p 318), a com-
parison with crossed-helical ‘tubes’ in other parts of the
body and in different species suggests that an appreciation
of this pattern is important to furthering our understanding
of muscle mechanics (Clark and Cowey, 1958; Kier and
Smith, 1985).
Endomysium
The endomysium is a delicate tissue that surrounds indi-
vidual muscle fibres (myofibres) and links them all within a
continuous honeycomb arrangement that extends laterally
across each fascicle and over the entire length of the
muscle (Purslow and Trotter, 1994; Nishimura et al., 1996)
(Fig. 2). It consists of a basement membrane that covers
the sarcolemma (plasma membrane) and contains mostly
type IV collagen, and a thicker felt-like reticular layer of
collagen fibres of predominantly types III, V and VI with only
small amounts of type I.
This network forms an intimate connection with the
myofibril and enables the transfer of contractile force
(Huijing, 2012a; Turrina et al., 2013), and because the
tubular wall of this endomysial sheath is shared between
adjacent myofibres, the tensional force generated by
contraction can be efficiently transmitted to adjacent
tubes through what is described as trans-laminar shear
(Purslow and Trotter, 1994; Purslow, 2002). Even the ter-
minations of serially arranged myofibres, which are often
staggered by about a quarter of their length with respect to
adjacent myofibres, must transmit their force in the same
way (Gaunt and Gans, 1992; Sharafi and Blemker, 2011) as
this endomysial network is the only structure that contin-
uously links them all together within a fascicle (Purslow,
2010; Turrina et al., 2013). Such lateral load sharing
Fascial hierarchies and the relevance of crossed-helical arrangements of collagen
Figure 2 Transverse sections of bovine muscle viewed under
SEM showing a) the endomysial network (arrows) surrounding
individual myofibres, and a thickened region of perimysium
(arrowhead); b) higher power view of endomysial ‘tubes’
showing the shared walls (arrow) between myofibres. (Myofi-
bres removed after digestion with NaOH). Reproduced from
Trotter and Purslow (1992) Wiley with permission.
maintains a uniform strain throughout the tissue and is
transversely isotropic (Passerieux et al., 2006; Sharafi and
Blemker, 2010; Chaudhry et al., 2012) as well as enabling
muscles to grow and repair damaged sarcomeres without
loss of force transfer through the contractile column
(Purslow, 2010).
While the endomysium ultimately transmits the
tensional force generated by myofibre contraction to the
tendons (Turrina et al., 2013), it is also “very compliant to
tensile forces acting within the plane of the network and.
can easily deform to follow the length and diameter
changes of muscle fibers in contracting and relaxing mus-
cles” (Purslow and Delage, 2012 p 7), making this highly
nonlinear elastic material a key component in muscle
flexibility (Meyer and Lieber, 2011).
Perimysium
The perimysium, however, is a much more complex myo-
fascial tissue and one with key functions that remain un-
resolved, with collagen types I, III, IV, V, VI, XII and XIV
predominating and large variations in thickness, fibre size,
orientation and attachment adding to this complexity
379
(Passerieux et al., 2006; Gillies and Lieber, 2011). The
perimysium is continuous with the outer epimysium and
tendons at either end of the muscle, and has direct at-
tachments to both myofibres and their endomysial sheaths
(Purslow, 2010; Gillies and Lieber, 2011).
Although both endomysial and perimysial tissues are
regarded as qualitatively similar across different species
such as bovines, porcines, murines and humans etc (Rowe,
1981), variations do occur between them and in different
FASCIA SCIENCE AND CLINICAL APPLICATIONS: MUSCLE ARCHITECTURE
muscles within the body, and can complicate detailed
comparisons. Several levels of organization have been
described, including the larger fascicles that bundle groups
of myofibres (10e100) and their endomysium together
(Fig. 1a), to the smaller fascicles that arise from them and
subdivide into successively smaller bundles (Purslow, 2010;
Chaudhry et al., 2012). Terms such as ‘primary’ and ‘sec-
ondary’ fascicles, however, will not be mentioned further
as they relate to relative size and are used inconsistently in
the literature. In contrast to the endomysium, micro-
mechanical modelling shows that the behaviour of peri-
mysial fascicles is transversely anisotropic to changes in
shape (Sharafi and Blemker, 2010).
The ‘walls’ of these perimysial fascicles consist primarily
of two or more layers containing large flattened cables or
bundles of wavy (crimped) collagen type I fibres, which are
oriented parallel to the myofibres in the region of the
myotendinous junction but generally curve around the
fascicle wall with an oblique angle (Passerieux et al., 2007).
The cables are generally aligned at an angle of w55
relative to the myofibre axis in resting muscle, and each
alternating layer is oriented differently so that the tubular
wall appears as a crossed-ply network with the cables
spaced at regular intervals and parallel to each other
(Gillies and Lieber, 2011; Purslow, 2010). In addition, thin
strips of perimysial tissue extend laterally from the smaller
fascicle walls and pass between the myofibres (Passerieux
et al., 2007) with the collagen fibres aligned in both fel-
ted and criss-cross arrangements (Rowe, 1981) (Fig. 3). The
points of intersection between these oriented collagen fi-
bres then give rise to branching plexuses that ultimately
connect to the surface of adjacent myofibres (and their
endomysium) through perimysial junctional plates (PJP’s)
spaced at regular intervals along their length (Passerieux
et al., 2006). The PJP’s are attached to the sarcolemma
and transfer tensional forces between them through spe-
cific transmembrane proteins such as integrins, which
interact with the inner cytoskeleton and contribute to the
mechanosensing and regulatory abilities of each cell (Wang
et al., 2009; Brown et al., 2012; Ingber et al., 2014).
Although the tensile properties of the perimysium are
similar to those of the endomysium, the fascicle ‘walls’ are
much thicker and there is plenty of evidence to show that
the perimysium is also involved in myofascial force trans-
mission (Passerieux et al., 2007; Purslow and Delage, 2012 p
10), but a transfer of forces by trans-laminar shear within
the shared walls of each fascicle seems improbable.
Purslow and Delage (2012 p 8) explained that “de-
formations caused by shear through its thickness would be
of orders of magnitude greater than in the endomysium,
and so perimysium would represent a rather sloppy and
inefficient force transmission pathway at physiologically-
relevant muscle lengths”.
 380
FASCIA SCIENCE AND CLINICAL APPLICATIONS: MUSCLE ARCHITECTURE
Figure 3 A lateral view of a sheet of perimysium overlying
two muscle fibres (asterisks) shows bundles of collagen
fibres (double arrows) arranged in a crossed-ply arrangement
with crimping in some of the fibres and a more delicate
felt-like network of finer collagen fibrils. (Sheep
semitendinosus  1700). Reproduced from Rowe (1981)
Elsevier with permission.
Schmalbruch (1985) cites an earlier model proposed by
Feneis (1935) where the perimysium provides “neutral”
connections between adjacent fascicles and enables them
to slide past each other and facilitate changes in muscle
shape during contraction (Purslow, 2010). As all fan-
shaped, fusiform and pennate muscles increase in width
when contracting (Lieber and Fridén, 2000; Azizi et al.,
2008), any consequent changes in the angle that myofi-
bres make with their tendinous/aponeurotic connections
at either end (<34 in human gastrocnemius muscle,
Kawakami et al., 1998) means that some sort of sliding
element within the muscle is necessary in order to
accommodate this (Purslow, 2002) (Fig. 4). Purslow (1989)
found that collagen fibres lie within the plane of the
crossed-ply perimysial layers and do not run through the
thickness of the inter-fascicular walls, which supports the
model whereby the septal walls between adjacent fasci-
cles can act as “neutral displacement membranes” that
facilitate sliding during changes in shape (Feneis, 1935;
Schmalbruch, 1985).
In the example given (Fig. 4) the muscle fibres and
tendon sheets form a parallelogram, with the length of the
myofibres being 60e70% of the muscle belly length, so that
shortening the myofibres shortens the muscle by about
33% and increases the collective diameters of the myofibre
bundles (fascicles) by about 20% (Schmalbruch, 1985). As
muscles maintain a constant volume during contraction, so
the cross-sectional area of the muscle fibres must in-
crease, and similar changes in fascicle length have also
been observed more recently in human gastrocnemius
(38e25 mm, a change of 34%) (Kawakami et al., 1998) and
other muscles (Fukunaga et al., 1997; Purslow, 2002).
Azizi et al. (2008) showed that changes in the pennate
angle of muscle fibres (wild turkey) “decrease a muscle’s
output force but increase output velocity by allowing
the muscle to function at a higher gear ratio (muscle ve-
locity/fiber velocity)”, and that “muscle-shape changes
G. Scarr
Figure 4 Schematic drawing of a pennate muscle showing
how contraction of the myofibre bundles leads to an increase in
their diameter and change in pennation angle q with shortening
of the muscle (not to scale) (re-drawn after Schmalbruch,
1985). Schmalbruch (1985) describes a model by Feneis
(1935) that proposes that the septal walls between adjacent
fascicles (perimysium) act like neutral displacement mem-
branes that enable the myofibre bundles to slide relative to
each other and change shape. The ‘neutral connecting threads’
change their alignment relative to the longitudinal axis of the
fascicles but remain the same with respect to the tendon
sheets (see text).
act as an automatic transmission system allowing a
pennate muscle to shift from a high gear [1:1.4] during
rapid contractions to low gear [1:1] during forceful con-
tractions”, thus modulating muscle performance during
mechanically diverse functions. However, their use of
the term “rotation” to describe these changes in orien-
tation of contracting myofibres (Fig. 4) is perhaps unfor-
tunate as any perceived axis of rotation is a virtual
contrivance.
While Schmalbruch’s (1985) description of Feneis (1935)
model also includes “neutral connecting threads” that
cross multiple perimysial fascicles as “large collagen
bundles. arranged parallel to the tendons and obliquely
to the muscle fibres. and hence do not resist movement
of the fascicles”, so the alignment of these threads in this
example (Fig. 4) suggest that these fibres may actually be
part of the epimysium (see below).
Epimysium
The epimysium is an even thicker myofascial tissue that
covers the entire muscle and is continuous with the peri-
mysium lying beneath, and tendons at either end, as well
as other fascial structures that surround it (Turrina et al.,
2013) (Fig. 1). Collagen cables of type I fibres are also
crimped and even larger in diameter and generally form
the same crossed-ply arrangement in resting fusiform
muscles of 55 relative to the myofibre axis (Purslow,
2010; Gillies and Lieber, 2011). However, the myofibres
within pennate muscles are themselves arranged at an
Fascial hierarchies and the relevance of crossed-helical arrangements of collagen
angle to the collective direction of tension generation,
and the arrangement of collagen fibres within these and
some other muscles can be parallel to the long axis and
form a dense surface layer that functions as a surface
tendon (Benjamin, 2009; Purslow, 2010).
The main functions of the epimysium are thus the
transmission of tensional forces (Huijing, 2012b; Turrina
et al., 2013) and containment of the muscle during
contraction (Passerieux et al., 2007), but high levels of
hyaluronic acid associated with proteoglycans in the outer
epimysial layers also enable the muscle surface to slide
with respect to adjacent structures (McCombe et al.,
2001). Although some epimysial surfaces are tightly
bound to the deep fascia, the sliding ability of many
others is facilitated by thin septal sheets and interposed
loose connective tissues, which enable the muscle and
surrounding tissues to accommodate to the changes in
shape that occur during contraction (Stecco and Stecco,
2012a,b). However, it may be that this ‘sliding’ is at
least partly due to structural rearrangements within
mutually linked collagen fibres and proteoglycans at both
‘fibrillar’ and molecular levels, and related to the micro-
vacuolar system described by Guimberteau (2005, 2012);
and ‘shear-linkage’ type connections of the endomysium
(Purslow, 2002) rather than a true shear (Levin and Martin,
2012 p 139).
Although the myofascia has been classified into these
distinct regions for the purpose of description, the struc-
tural complexity that unites them all into a functional unit
also enables the efficient transfer of tensional force to
other fascial tissues that surround the epimysium (Maas
and Sandercock, 2010; Huijing, 2012b).
The fascial tissues associated with muscle
These include the inter-muscular fascial septa that connect
adjacent muscles within a group; and the extra-muscular
fasciae that merge with the deep fascia (fascia profunda),
interosseal membranes and periosteum, and the neuro-
vascular sheaths that enclose the nerves and vessels sup-
plying the muscle (Fig. 1b). The deep, or ‘investing’, fascia
is a tough tissue that surrounds and contains groups of
muscles (compartments) and is continuous with aponeuro-
ses (McCombe et al., 2001; Stecco and Stecco, 2012a,b) and
the overlying ‘superficial’ fascia that lies beneath the skin
(Benjamin, 2009; Abu-Hijleh et al., 2012); and all are
involved in the transfer of tension (Maas and Sandercock,
2010; Huijing, 2012b), with the loose fibre network of the
superficial layer contributing to its flexibility (Iatridis et al.,
2003).
The distinctions between these different types of fas-
cia can thus be rather tenuous at the microscopic level, as
they are interlinked with each other, and the same named
tissue can vary in its structural organization and func-
tionality depending on where it appears in the body
(Benjamin, 2009; Stecco and Stecco, 2012a,b). While
collagen fibre alignments in the deep fascia have been
noted as lying parallel with the muscles (McCombe et al.,
2001; Benjamin, 2009), Benetazzo et al. (2011) noted
the mean angle between crossed-fibre orientations in
human thoraco-lumbar and crural fascia as 78 , which
381
indicates an average fibre angle of 39 relative to the body
axis.
The helical tube
All these tissues contribute to the highly complex and
continuous structural network that extends from the
inner cellular cytoskeleton, plasma membrane, endomy-
sial sheath, perimysial fascicules and epimysium to the
FASCIA SCIENCE AND CLINICAL APPLICATIONS: MUSCLE ARCHITECTURE
tendons and surrounding fascia, muscles and bone; with
each region playing its own specialized part in the transfer
of tension. The descriptions of myofascial tissues as
‘tubes’ naturally follows from their cross-sectional ap-
pearances; and the higher-level fascial tubes surrounding
groups of muscles, the entire limb and body wall are
similar (Figs. 1 and 2), with the orientations of collagen
fibres within their walls having an important functional
role.
The ‘walls’ of the perimysium and epimysium are
distinct in that they frequently contain two crossed-ply
sets of collagen cables aligned at about 55 (relative to
the long axis in resting fusiform muscles) (Fig. 3), while
the apparently isotropic orientation of collagen fibres
within the endomysium appears to be random but collec-
tively has a (numbers-weighted) mean alignment of about
59 (Purslow and Trotter, 1994). All these angles increase
with muscle contraction and become more aligned with its
transverse, or circumferential, plane and when the muscle
is stretched the angles decrease as the fibres become
aligned towards the main direction of tension, indicating
that the collagen fibres are mechanically linked with each
other (Purslow, 1989; Chaudhry et al., 2012). The partic-
ular alignments of collagen fibres within the walls of these
tubes can thus not be considered incidental but a
contributor to the mechanics of muscle function, which
can be simply analysed if the crossed-ply sets of collagen
are considered as left- and right-handed helixes, or spirals
(Fig. 5).
Crossed-ply helixes
In 1958, Clarke and Cowey showed that changes in
the relative length and diameter of certain nemertean
and turbellarian worms were controlled by the particular
alignment and geometric configuration of tensioned
fibres within their body walls. In essence, the inextensible
fibres were constrained by the crossed-helical geometry
surrounding the pressurized body tube and enabled it
to maintain a constant volume throughout changes in
shape; and this basic hydrostatic model has now
become entrenched as a design principle in biomechanics
(Wainwright, 1988; Shadwick, 2008; Kier, 2012).
A crossed-helical tube that is shortened will cause the
fibre angles to increase (relative to the tube axis) while one
that is extended in length will cause them to decrease; and
in both cases, the tension within the fibres becomes greater
as the tube shape moves away from its central resting po-
sition (Purslow, 1989; Goriely and Tabor, 2013) (Fig. 6). The
optimum shape that balances both longitudinal and
circumferential stresses is when the fibres are at an angle
of w55 , i.e. these fibre orientations are reflecting the
 382
FASCIA SCIENCE AND CLINICAL APPLICATIONS: MUSCLE ARCHITECTURE
Figure 5 Schematic drawings of crossed-helixes showing how
a shortened tube (a) causes the fibre angles to increase
(relative to the tube axis); b) a lengthened tube decreases the
fibre angles; and (c) a ‘resting’ tube with fibre angles of w55
balances both longitudinal and circumferential fibre stresses
(not to scale).
Figure 6 Graph showing the relationship between changes in
length and diameter for a constant volume tube with crossed-
helical fibres (helixes not to scale). Re-drawn with modifica-
tions from Kier and Smith (1985).
most efficient distribution of mechanical stresses and
coordinating the changes in shape of the tube, as well as
providing a system of elastic energy storage that assists in
returning the tube to its resting state (Fig. 6) (Clark and
Cowey, 1958).
G. Scarr
The muscular tube
The tensioned fibres actually follow the course of geo-
desics, or the shortest line between two points on the
surface of a curve, and the theoretical relationship be-
tween fibre angle and volume is relatively simple for a tube
with circular cross-section (Fig. 7a). Muscles, however,
maintain an almost constant volume during contraction and
elongation, with Baskin and Paolini (1966) finding variations
in frog sartorius muscle of less than 0.006 cm3 per 100 g of
muscle (Rana, ex-vivo), but the graph is still relevant if the
cross-section of the tube is an ellipse, or non-circular,
where changes in the fibre-angle follow a horizontal line
(b) within the boundaries of the curve (a) (Clark and Cowey,
1958).
Such a tube would only have a circular cross-section
when it reached either of these two extremes, i.e. when
the fibres are under the greatest amount of tensional
stress, with the tube progressively flattening towards the
middle as the fibre angles approach 54.44 ; the angle where
tension is at a minimum, and circumferential and longitu-
dinal stresses are balanced (Clark and Cowey, 1958).
The constraining fibres
It should be recognized that the apparently continuous
collagen fibres that stretch between the ends of the
crossed-helical tubes shown in Figs. 5e7 are really graphic
representations of bundles of shorter collagen molecules/
fibrils that are cross-linked together and transfer tensional
forces between them (Avery and Bailey, 2008; Purslow,
2010).
Figure 7 Graph (a) showing the relationship between volume
and crossed-helical fibre angle for a tube with circular cross-
section, with maximum volume coinciding with the least
tensional stress in the fibres and an angle of 54.44 (middle
dotted line). The horizontal line (b) indicates the limits (an-
gles) of maximum contraction and elongation (dotted lines) for
a tube with constant volume, where the tube is long and thin at
lower fibre angles, and fat and short at high fibre angles (not to
scale), with the vertical position of this line on the volume axis
of the graph determining the relative amount of flattening
(ellipses) that occurs near the resting angle. Re-drawn with
modifications from Clark and Cowey (1958) and Wainwright
(1988).
Fascial hierarchies and the relevance of crossed-helical arrangements of collagen
Muscles generally have an elliptical or irregular cross-
section with considerable variation in shape in-vivo
(Fig. 1b) and normally operate in the near-horizontal part
of the curve shown in Fig. 6 and middle region of the hor-
izontal line in Fig. 7b and rarely, if ever, reach the extremes
of shape and fibre alignment shown (Purslow, 1989). It is
thus important to note that the ideal curves shown in these
figures are theoretical representations of the mechanical
behaviour of crossed-helical tubes with inextensible fibres,
while the wavy crimped collagen fibres in the perimysium
and epimysium (Fig. 3) can be stretched by an additional
five per cent of their length; and such tubes are likely to
behave differently (Clark and Cowey, 1958).
Purslow (1989) showed that the crimp angle (w39 in
resting muscle) contributes to the elasticity of individual
fibres and that this angle decreases (as tension in the fibres
increases) and they are straightened out during changes in
muscle length and shape. A correlation with changes in
sarcomere length (fusiform muscle in vitro) and crossed-
helical fibre angles (1.1 mm at w20 to 3.9 mm at w80 )
confirmed that the straightened fibres are acting as con-
straints to further increases in muscle length and circum-
ference, and that these particular angles corresponded
with a sudden and dramatic increase in the stiffness (0 e
w18 KPa) and ability of the perimysium to transfer signifi-
cant tensional forces (Purslow, 1989). However, these ex-
tremes are well beyond the normal range of living muscle,
which explains why they can change shape with ease.
Variations in angle
Variations in the resting fibre angles of a collagen-
reinforced tube would undoubtedly depend on its partic-
ular functional activities, such as in bovine semitendinosus
muscle where collagen fibres are generally aligned parallel
(0 ) to the long axis and cause it to act more as an epi-
tendon (Purslow, 2010), and in the deep fascia where they
can be arranged similarly (McCombe et al., 2001; Benjamin,
2009). While the arrangement of collagen fibres within the
epimysium of pennate muscles may be “parallel to the long
axis of the muscle and forms a dense surface layer that
functions as a surface tendon” (Purslow, 2010), the myofi-
bres are arranged at an angle to this, and there is some
gradation in collagen fibre angle as the myofascia transits
into functionally related tissues with different mechanical
properties. Passerieux et al. (2007) showed that oblique
perimysial fibres become more axially aligned with the
overall direction of muscle tension generation as they
approach the myotendinous junction (bovine flexor carpi
radialis). Tendons, however, are more complicated than is
generally recognized, with collagen fibres tending to form
complex plaits and spirals in both longitudinal and trans-
verse directions (Kannus, 2000); and in ligaments, their
complex myofascial connections and variable internal or-
ganization suggest a much more complex multi-axial
loading (Van der Wal, 2009).
A ubiquitous pattern
Crossed-helical winding and its functional significance
have been described in the body walls of squid (Johnsen
and Kier, 1993), amphibians (O’Reilly et al., 1997), eels
383
(Hebrank, 1980), fish, dolphins and whales (Pabst, 2000)
suggesting that a similar pattern is likely to occur
throughout the human. Indeed, the alignments of muscle
and investing fascial tissues that curve around the body
wall and limbs are also suggestive of helical arrangements,
if only in part (Benetazzo et al., 2011; Vleeming, 2012)
(Fig. 8); and Scarr (2013) also suggested an alternative
helical arrangement of collagen in the limbs of mammals,
although this remains unconfirmed.
FASCIA SCIENCE AND CLINICAL APPLICATIONS: MUSCLE ARCHITECTURE
Crossed-helical arrangements of collagen have also been
described in the walls of elastic arteries (Holzapfel, 2006),
the inter-vertebral disc (Hukins and Meakin, 2000), heart
(Buckberg, 2002), trachea, oesophagus (Carey, 1920a,b),
small intestines (Gabella, 1987) and embryonic notochord
(Koehl et al., 2000); and tubular organs that maintain
constant volume throughout changes in shape due to
crossed-helical arrangements of muscle and fascial tissue
have also been described in the tongues of mammals and
lizards, the arms and tentacles of cephalopods and the
trunks of elephants (Kier and Smith, 1985). The mechanical
principles that underlie the value of this ubiquitous pattern
in biology even contribute to the novelty of the ‘Chinese
finger trap’ toy and its effectiveness as a suture in gastro-
intestinal surgery (Song et al., 2008).
Considering the similarity between the theoretical fibre
angle that balances both longitudinal and circumferential
stresses (54.44 ), and the alignment of collagen fibres
within the myofascia of resting muscles and other biological
examples, it would seem that these geometric crossed-
helical arrangements are indeed contributing to the coor-
dination of changes in muscle shape. They would also
enable such tubes to bend smoothly without kinking and
resist torsional deformations, thus further demonstrating
the value of this particular arrangement to muscle me-
chanics (Wainwright, 1988 p 71; Etnier, 2003).
Discussion
Although collagen fibre angles quoted in the literature are
sometimes stated in relation to the transverse axis they
have been converted here relative to the longitudinal axis
Figure 8 Schematic diagrams showing the muscles and fascia
of the trunk twisting around the body wall and continuing into
the neck and limbs. Reproduced from Scarr (2014) Handspring.
 384
of the tube for comparison purposes. Biological helixes
are not continuous, like metal springs, but consist of mul-
tiple discrete components (fibres) arranged into these
particular geometric configurations because they are the
most efficient packing arrangement within a dynamic
environment (Pickett et al., 2000). The orientation of fibres
with respect to the longitudinal axis then distinguishes this
biological configuration from the continuous ‘helical angle’
that is perpendicular to it and as used in mechanical
FASCIA SCIENCE AND CLINICAL APPLICATIONS: MUSCLE ARCHITECTURE
engineering.
Simple hydrostat or integrated structure?
Crossed-helical configurations in biological tissues are
widely considered to be acting as hydrostats (Wainwright,
1988; Aspden, 1990; Kier, 2012; Goriely and Tabor, 2013;
Findley et al., 2015), where an incompressible fluid con-
tained within a tube is constrained by tensioned fibres in
the tube wall, but this seems to be far too simplistic on its
own when considering the high level of structural organi-
zation within muscle (Levin, 2014). Although an increase in
intra-muscular pressure as the result of lateral tissue
constraint would increase muscle stiffness and lead to
increased force production during active contraction
(Purslow, 2002), muscles are not like pressurized balloons
(Levin, 2002; Sharkey, 2015) and most of the water con-
tained within them is tightly bound to a wide diversity of
proteoglycan complexes that are cross-linked with the
collagen fibres (Gillies and Lieber, 2011).
While the measurement of normal intra-muscular pres-
sures during contraction (15e141 mm Hg) is notoriously
difficult (Hill, 1948; Ward et al., 2007; Aweid et al., 2012),
pressures of 6e12 mm Hg at rest (Aweid et al., 2012) may
be at least partly due to the passive muscle stiffness, or
intrinsic tension, that naturally occurs in muscle tissues in-
vivo (Schleip et al., 2006; Masi and Hannon, 2008).
Collagens are the main tension-bearing element within
ECM/fascial tissues and are aligned parallel to the local
tissue strain (Purslow, 2010) with the cells contained within
them also contributing to this tension (Tomasek et al.,
2002). Myofibroblasts generate significant tensional forces
due to the presence of smooth muscle-like actin filaments
within their cytoskeletons and transfer this into the sur-
rounding ECM through transmembrane proteins, and they
play an important role in tissue contracture during wound
healing and other fascial pathologies (Tomasek et al.,
2002). This contractile ability thus enables myofibroblasts
to contribute to the intrinsic tension/passive stiffness of
muscle and other tissues (Schleip et al., 2006), and perhaps
even assist in organizing or fine-tuning the crossed-helical
lattice as the most efficient distribution of tension. So,
while it has been assumed that the walls containing these
crossed-helical arrangements simply apply pressure against
the contents of a fluid filled bag during changes in shape, a
more complex picture emerges.
A new model
The contraction of myofibres mechanically influences the
endomysium, perimysium and epimysium (as described
above) and leads to shortening of the entire muscle
because of their tensional continuity with each other and
the tendinous tissues at each end (Fig. 5). While the walls
G. Scarr
of these tubes have been widely considered as compressing
the contents of a constant-volume tube, they are already
under tension, and the collagen and proteoglycans mole-
cules within them are mechanically linked with each other
(Wess, 2008).
It has thus been suggested that structural rearrange-
ments, and moment by moment changes in the balance
between tensioned collagen fibres and compressed pro-
teoglycans at both fibrillar and molecular levels, and across
the myofascial hierarchy, also regulate the changes in
shape of muscle and that perhaps an equivalent mechanism
operates within the tubular hierarchy of surrounding fascial
tissues (Levin, 2014). This balance between tension and
compression acting within and between different tissues
has been considered in relation to tensegrity, a structural
design principle whose significance is increasingly recog-
nized in structural biology, but the reader is referred
elsewhere for further information (Levin, 2002; Ingber
et al., 2014; Scarr, 2014).
A brief summary
The endomysial sheath (tube) surrounding each myofibre
is shared with those adjacent to it and transmits the force
of contraction through trans-laminar ‘shear’, and ulti-
mately to the tendinous tissues at either end of the mus-
cle; and because this network forms a tight and seamless
connection that is continuous across the whole fascicle, its
behaviour is transversely isotropic to changes in shape
(Purslow and Trotter, 1994; Chaudhry et al., 2012). The
perimysium also forms a honey-comb like network (at a
higher size-scale) that extends across the entire muscle
and continues into the epimysium, with the larger fasci-
cles giving rise to smaller fascicles that subdivide into
successively smaller bundles and ultimately connect to the
endomysium and individual myofibres (Passerieux et al.,
2006; Purslow, 2010). However, the transverse anisotropy
of this perimysial network suggests that changes in muscle
diameter will not be the same in every direction (Sharafi
and Blemker, 2010), thus complicating the precise rela-
tionship between muscle length and diameter during
changes in shape. Although Schmalbruch (1985) descrip-
tion of the Feneis (1935) model includes “neutral
displacement membranes” within the walls of adjacent
perimysial sheets, and which enable the fascicles to slide
against each other during changes in muscle shape (Fig. 4),
confirmation of the details of this mechanism are still
needed.
Bundles of collagen fibres within the perimysium and
epimysium form crossed-helical arrangements that bal-
ance and coordinate the longitudinal and circumferential
stresses within the walls of these myofascial tubes during
changes in muscle shape; but more comparative details of
their alignments within fusiform, fan-shaped and pennate
muscles are needed. Myofascial hierarchies are inter-
connected and extremely complex, and much information
has been determined on two-dimensional tissue samples,
with relatively few attempts made to extrapolate them to
the behaviour of crossed-helical tubes; and although this
tubular perspective is itself a simplification, much is likely
to be gained from an understanding of these geometric
patterns.
Fascial hierarchies and the relevance of crossed-helical arrangements of collagen
Conclusion
Helixes spontaneously appear in self-organizing systems as
the most efficient way of organizing components of similar
size on the surface of a cylinder or tube (Pickett et al.,
2000). They are a common motif in protein construction
because they provide an energy-efficient solution to mo-
lecular close-packing (Snir and Kamien, 2005) and form a
structural model for coiled winding at multiple size scales
throughout the body (Scarr, 2011) and in a diverse group of
organisms (Kier and Smith, 1985). The formation of a helix
is based on simple geometric principles (Sadoc and Rivier,
2000; Pickett et al., 2000; Lord, 2002) and its persistence
is ensured because it is one of the most stable of structural
configurations. It is thus not surprising that a system of
crossed-helical tubes should predominate in compliant
biological tissues because this is one of the most efficient
ways of optimizing mechanical stresses within their walls
(Clark and Cowey, 1958; Wainwright, 1988; Kier, 2012).
The myofascia, as a fibrous specialization of fascial/ECM
tissues that surround and interpenetrate muscles is then a
complex hierarchy of helically-reinforced tubes contained
within larger tubes; and continuous with higher-level
fascial tubes that surround groups of muscles, the limbs
and entire body (Figs. 1 and 2). Bundles of collagen fibres
within the perimysium and epimysium form crossed-helical
configurations (Fig. 3) that balance longitudinal and
circumferential stresses and coordinate changes in muscle
shape during contraction and extension (Figs. 4e7), and
should thus be considered as an essential part of muscle
function.
Acknowledgements
I would like to thank Stephen Levin for his views on the
standard muscular hydrostat model and for questioning
whether a true shear (rather than an apparent one) really
occurs within normally functioning tissues; also to the
anonymous reviewer who rigorously questioned the as-
sumptions made and provided much-needed food for
thought.
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