The role of fascia in creating distinctive compartments for muscles and in acting as an ectoskeleton for their attachment
The unyielding character of the deep fascia enables it to serve as a means of containing and separating groups of muscles into relatively well-defined spaces called ‘compartments’. The deep fascia integrates these compartments and transmits load between them. As the compartmentalizing role of deep fascia is a function it performs in conjunction with the associated bones and intermuscular septa (Fig. 1), the compartments are sometimes called osteofascial compartments. Each segment of the limbs (e.g. arm, forearm, thigh, leg or foot) has its own characteristic compartments separating functional groups of muscles with distinctive embryological origins, blood and nerve supplies. The compartments are generally named according to their position (anterior, posterior, medial, lateral, etc.) or the actions of their contained muscles (flexors, extensors, evertors, adductors, etc.).
The fascial intermuscular septa are often attached to periosteum, and as these two structures share the same developmental origin, it means that fascia rarely makes contact with bone without also attaching to it (Grant, 1948). It is not surprising therefore that fascial entheses have been implicated in overuse injuries – e.g. medial tibial stress syndrome (Bouche & Johnson, 2007). These authors have suggested that the tenting effect of tendons associated with eccentric muscle contraction in the posterior compartment of the leg increases the tensile load on the deep fascia. This is ultimately relayed to the fascial attachment site on the tibial crest. Bouche & Johnson (2007) reported a linear relationship between tension of any one (or all) of the tendons involved and strain levels in the tibial fascia. Simple inspection of cadaveric specimens in which muscle contraction has been simulated by pulling on the tendons with a pneumatic actuator, shows clear evidence of fascial tenting. The authors point out that (1) eccentric contraction of the implicated muscles is increased when exercising on hard surfaces to promote shock dissipation and that individuals with marked foot pronation also have increased eccentric contractions; (2) both running on hard ground and over-pronation are known risk factors for medial tibial stress syndrome (‘shin splints’). Their fascial theory is supported by the common finding of inflammatory changes in the crural fascia of patients with shin splints.
Where deep fascia and intermuscular septa partition muscles, they may also serve for their attachment and this makes such fascia particularly thick (Grant, 1948). One of the most influential anatomists of the 20th century, Professor Frederic Wood Jones, coined the term ‘ectoskeleton’ to capture the idea that fascia could serve as a significant site of muscle attachment – a ‘soft tissue skeleton’ complementing that created by the bones themselves (Wood Jones, 1944). It is clearly related to the modern-day concept of ‘myofascia’ that is popular with manual therapists and to the idea of myofascial force transmission within skeletal muscle, i.e. the view that force generated by skeletal muscle fibres is transmitted not only directly to the tendon, but also to connective tissue elements inside and outside the skeletal muscle itself (Huijing et al. 1998; Huijing, 1999). Several authors have commented on the extent to which muscles attach to fascia as well as bone and on how this has been overlooked in the past. Thus Kalin & Hirsch (1987) found that only eight of the 69 interossei muscles they studied in the feet of dissecting room cadavers had attachments that were limited to bone. In the vast majority of cases the muscles had extensive attachments to ligaments and fascia that effectively link the muscles together to promote their contraction as a co-ordinated unit. A similar point is made by Chang & Blair (1985) in relation to the attachments of adductor pollicis. These authors described prominent attachments of its transverse head to fascia covering the palmar interossei that had not been recorded previously. As the palmar interossei and adductor pollicis are supplied by the same nerve and are both adductors of the thumb (Mardel & Underwood, 1991), it is likely that fascial interconnections promote their coordinated activity.
An interesting implication of recognizing the existence of fascial routes of force transmission is that in muscles with tendons at both ends, the forces within these tendons may be unequal (Huijing & Baan, 2001a). Furthermore, as Huijing et al. (2003) point out, what are generally taken to be morphologically discrete muscles from an anatomical perspective, cannot be considered isolated units controlling forces and moments. One can even extend this idea to embrace the concept that agonists and antagonists are mechanically coupled via fascia (Huijing, 2007). Thus Huijing (2007) argues that forces generated within a prime mover may be exerted at the tendon of an antagonistic muscle and indeed that myofascial force transmission can occur between all muscles of a particular limb segment.
It is intriguing to note that Huijing et al. (2003) follow Wood Jones's (1944) lead and liken compartment-forming fascia to a skeleton. Indeed, they suggest that one of the functions of myofascial force transmission is to stiffen this skeleton and hence augment its function. Whether surgery to this ‘skeleton’ (notably fasciotomies undertaken to reduce intracompartmental pressure – see below) changes the force-generating capacity of limb muscles is a valid question that does not seem to have been addressed, although Huijing & Baan (2001b) report significant changes in the forces generated by muscles in the anterior compartment of the rat leg following fasciotomy. Furthermore, as neighbouring muscles can be strongly attached to each other by extramuscular connective tissue, it may well be that the tenotomies favoured by some surgeons in the treatment of tennis elbow affect the force transmission of neighbouring muscles in way that has not been thoroughly explored.
Wood Jones (1944) was particularly intrigued by the ectoskeletal function of fascia in the lower limb. He related this to man's upright stance and thus to the importance of certain muscles gaining a generalized attachment to the lower limb when it is viewed as a whole weight-supporting column, rather than a series of levers promoting movement. He singled out gluteus maximus and tensor fascia latae as examples of muscles that attach predominantly to deep fascia rather than bone (Wood Jones, 1944). Viewing the deep fascia as an ectoskeleton emphasizes the importance of considering the responses of this tissue to distraction procedures designed to lengthen a limb segment. According to Wang et al. (2007), a lengthening rate of 1 mm day−1 in a rabbit model of distraction in which the tibia is ultimately increased in length by 20%, results in a corresponding re-modelling of the deep fascia. This ensures that the tensile forces operating in the fascia match the increasing length of the limb so that the fascia does not impede distraction.
Although gastrocnemius is strikingly lacking in any significant attachment to its overlying deep fascia (see above), it nevertheless gains extensive anchorage to a thick fascial sheet on its deep surface. As with any such well-developed aponeurosis on the surface of a muscle, this inevitably restricts the range of movement. Indeed, a surgical approach that has been advocated to improve the range of motion in cerebral palsy patients with an equinus deformity is to make a series of transverse incisions through this fascia (Saraph et al. 2000).
This ectoskeletal role of fascia is particularly obvious in relation to the intrinsic muscles of the foot and tibialis anterior in the upper part of the leg. The firm fascial attachments of tibialis anterior account for the longitudinal orientation of the fascial fibres at this site (i.e. parallel to the long axis of the muscle) and for the difficulty in making a clean dissection. In marked contrast, the deep fascia on the back of the leg covering the muscle bellies of gastrocnemius, does not serve for muscle attachment at all (Grant, 1948). This indicates the importance of this particular muscle belly to be able to move independently of its fascia during the powerful contractions that it performs in its weight-bearing capacity. Advantage is taken of the absence of muscle–fascia attachment in this location in the design of surgical interventions to augment calf size, either for purely aesthetic reasons or to correct a deformity resulting from illness (Niechajev, 2005). Silicone implants can be placed between the investing deep fascia covering gastrocnemius and the muscle itself (Niechajev, 2005).
The general thinness of the deep fascia covering the large, flat pectoral muscles in the chest is in line with the need for the thorax to expand and contract during breathing (Grant, 1948). In contrast, the deep fascia is particularly thick in the leg in line with its compartmentalizing and ectoskeletal roles. Strong intermuscular septa pass inwards from the deep fascia to fuse with the periosteum of the tibia and fibula and create separate compartments for the dorsiflexor, peroneal and plantarflexor muscles (Fig. 1). The anterior compartment houses the dorsiflexor muscles (which include tibialis anterior, discussed above) and is of particular clinical significance in relation to compartment syndrome. This is a painful and potentially limb-threatening condition that occurs when pressure builds up within the space that is limited by the tough and unyielding deep fascia impairing blood flow. It can occur as a result of sudden trauma (e.g. a haematoma) or as a consequence of overuse. The resulting muscle ischaemia may require an emergency fasciotomy to reduce the pressure. If surgery is unduly delayed, serious systemic complications can arise, including renal failure (Mubarak & Owen, 1975). Anterior compartment syndrome is perhaps the best known, but compartment syndrome can occur elsewhere as well. From an anatomical perspective, it is worth remembering that the fascial compartments characterizing the hands and feet are small (matching the size of the muscles; Grant, 1948) and thus pressure can quickly build up from a haematoma and trigger a collapse of the local circulation.
The attachment of seemingly diverse muscles to a common fascia means that fascia is in a strategic position to co-ordinate muscle activity. This is not surprising bearing in mind the integrating role of the connective tissue sheaths within a given muscle, harnessing the activity of its muscle fibres into an integrated whole. In an influential paper, Vleeming et al. (1995) have highlighted the importance of the thoracolumbar fascia in integrating the activity of muscles traditionally regarded as belonging to the lower limb, upper limb, spine or pelvis and whose action is thus often considered in that territory alone. They have argued that a common attachment to the thoracolumbar fascia means that the latter has an important role in integrating load transfer between different regions. In particular, Vleeming et al. (1995) have proposed that gluteus maximus and latissimus dorsi (two of the largest muscles of the body) contribute to co-ordinating the contralateral pendulum like motions of the upper and lower limbs that characterize running or swimming. They suggest that the muscles do so because of a shared attachment to the posterior layer of the thoracolumbar fascia. Others, too, have been attracted by the concept of muscle-integrating properties of fascia. Thus Barker et al. (2007) have argued for a mechanical link between transversus abdominis and movement in the segmental neutral zone of the back, via the thoracolumbar fascia. They feel that the existence of such fascial links gives an anatomical/biomechanical foundation to the practice in manual therapy of recommending exercises that provoke a submaximal contraction of transversus abdominis in the treatment of certain forms of low back pain. Stecco et al. (2007a,b, 2008) have also given us further examples of how fascia in the upper limb links numerous different muscles together. They suggest that a basal level of tension that is loaded onto the fascia by flexor and extensor muscles alike, contributes to myofascial continuity and possibly activates specific patterns of proprioceptors associated with the fascia.
One of the most striking examples of how fascia links muscles together concerns the extensor muscles of the forearm in the region of the lateral epicondyle. Although standard anatomy texts often simplify the position greatly by saying that the extensor muscles attach to the common extensor origin, the reality is rather more complex. Clearly, the area of bone provided by the lateral epicondyle is insufficient to attach the numerous muscles on the back of the forearm that arise from the common extensor origin. What happens instead is that the muscles attach to each other in this region via fascia and by this means they can be crowded onto a limited surface of bone. This is well illustrated by the work of Briggs & Elliott (1985) who dissected 139 limbs, and found that extensor carpi radialis brevis (the muscle most commonly associated with tennis elbow) actually attached directly to the epicondylar region in only 29 cases. Much more frequently it was linked by fascia to extensor carpi radialis longus, extensor digitorum communis, supinator and the radial collateral ligament.
The circulatory-support function of deep fascia – the muscle pump phenomenon
An important function of deep fascia in the limbs is to act as a restraining envelope for muscles lying deep to them. When these muscles contract against a tough, thick and resistant fascia, the thin-walled veins and lymphatics within the muscles are squeezed and their unidirectional valves ensure that blood and lymph are directed towards the heart. Wood Jones (1944) contests that the importance of muscle pumping for venous and lymphatic return is one of the reasons why the deep fascia in the lower limb is generally more prominent than in the upper – because of the distance of the leg and foot below the heart. However, there is also a thick, inelastic fascia covering the scapular muscles above the level of the heart. This has a bearing on the high intramuscular pressure in supraspinatus that is implicated in shoulder pain and muscle isthemia (Jarvholm et al. 1988).
That the deep fascia is under tension from the contraction of its contained muscles is evident when it is punctured, for the muscle bulges through it (Le Gros Clark, 1945). The protrusions are known as fascial herniations and may merit a fasciotomy if muscle ischaemia is a risk (de Fijter et al. 2006). The anti-gravitational nature of the ‘muscle pump’ associated with the crural fascia is commonly mentioned in anatomy texts and has traditionally been reinforced to generations of medical students by the observation that long periods of standing still (e.g. as with soldiers on ceremonial duty) can cause blood to pool in the legs and feet, resulting in inadequate venous return and fainting. More recently, the emphasis has turned to deep vein thrombosis as a way of illustrating the importance of the muscle pump. The stagnancy of peripheral blood flow that comes from long periods of static posture (again linked to inadequate muscle activity) can lead to the formation of blood clots – which can be fatal. Understanding the role of fascia in the muscle-pumping actions of the lower limb depends on a sound understanding of the venous system. This is adequately covered in standard anatomy teaching texts and has also been addressed in a recent review article by Meissner et al. (2007). Briefly, a distinction is made between superficial and deep veins according to their relative position with respect to the deep fascia. The two sets of veins are linked by ‘perforating veins’ that penetrate the deep fascia, linking veins either side. All three sets of vessels have valves that prevent backflow and help to divide the hydrostatic column of blood into segments (Meissner et al. 2007). Valvular incompetence in the leg thus diminishes muscle pump function. Curiously, however, the perforating veins in the foot lack valves and thus do allow bidirectional flow. According to Meissner et al. (2007), the calf muscle pump is the most significant and has the largest capacitance, but is primed by muscle pumps in the foot. They view the influence of similar pumps in the thigh as being minimal.
On occasions, the deep fascia may have too severe a restraining influence on its contained muscles, so that they are in danger of inadequate perfusion because their vessels are occluded for prolonged periods. The outcome is known as a ‘compartment syndrome’ and can be acute or chronic. Acute compartment syndromes may be associated with trauma where there is bleeding within the compartment or may be elicited by a plaster-cast applied too tightly to a limb. Chronic compartment syndromes stem from an exercise-induced increase in intra-compartmental pressure that compromises normal neuromuscular function (Bourne & Rorabeck, 1989). The muscle ischaemia stemming from acute compartment syndrome can be limb- (and sometimes life-)threatening and represents a surgical emergency. The confining deep fascia must be cut to reduce the pressure. The urgency with which a fasciotomy needs to be performed in severe acute cases is indicated by the observation that significant necrosis can occur within 3 h (Vaillancourt et al. 2004). In mild cases of exercise-induced compartment syndrome, the pressure on the muscles may be reduced by applying ice.
In view of the importance of gravitational influences in accounting for the prominence of deep fascia in the leg, it might be surmised that fasciotomies would seriously impair the venous calf pumps. This is the conclusion of Bermudez et al. (1998) who caution that patients who have had fasciotomies are at risk of developing chronic venous insufficiency in the long term. This, however, contrasts with the earlier findings of Ris et al. (1993).