Sports Rehabilitation and Injury Prevention Edited by Paul Comfort

5 Tendons Dr. Stephen Pearson University of Salford, Greater Manchester Introduction Basic tendon anatomy and physiology Tendons are an important link in the locomotor sys- Tendon gross structure can be described as either tem, enabling muscle forces to be utilised to perform sheet like or rounded. Some tendinous structures complex movements and actions. As such, their char- may be a combination of both, with the tendon acteristics can affect the ability to generate appropri- being more rounded in the mid portion and tending ate forces when attempting, for example, fine motor to resemble sheet-like fascia at their attachments tasks, or indeed those tasks requiring high rates of (aponeuroses) with the adjoining muscle. Within force development. In order to be able to respond the tendon there is a structure consisting of closely to these demands, the tendon is designed to be both packed collagen molecules, which are assembled rigid enough to enable efficient transfer of forces into fibrils, fibres, fibre bundles or sub fascicles, from muscle to bone, but also compliant enough to fascicles and tertiary fibre bundles (see Figure 5.1). allow storage of energy for later use. This arrangement of collagens into a hierarchical structure enables the tendon to resist tensile loading It is because of these diverse requirements on and ensures that there is minimal risk of catastrophic the tendon that they are frequently at risk of injury, rupture. Each fibre bundle is wrapped with a layer both acutely where perhaps force has been applied of connective tissue called the endotenon; blood in an unusual or inappropriate fashion, or chron- vessels, nerves and lymphatic elements can pass ically where micro damage has accumulated over through this layer to supply the tendon. The tendon time leading to trauma. is covered by an outer layer of connective tissue called the epitenon; this is contiguous with the layer This chapter will outline the tendon physiology below (endotenon). Most tendons are then covered from a molecular level to gross tissue level and how with a looser outer layer paratenon; this tissue is this relates to its function and its subsequent me- lined with synovial cells and allows for tendon chanical properties. The tendon characteristics are movement or gliding. then put in context of the action of muscle and ulti- mately the ability to produce functional force. Next, Tendon consists of tendon cells (fibroblasts) that tendon injury will be discussed in context of its use lie in longitudinal rows and are elongated cells ex- both from an acute and also chronic perspective. tending within the tendon structure and communi- The ability of the tendon to regenerate and opti- cate via gap junctions within the three-dimensional mal or appropriate healing strategies will also be put space of the tendon. Also there is the extracellular into a context and illustrated by appropriate by case matrix (ECM) that forms the scaffold for the tendon studies. Sports Rehabilitation and Injury Prevention Edited by Paul Comfort and Earle Abrahamson C 2010 John Wiley & Sons, Ltd

80 TENDONS Primary Secondary Tertiary Tendon fiber bundle fiber bundle fiber bundle (subfascicle) (fascicle) Collagen fiber Collagen fibril Endoterion Epiterion Figure 5.1 Arrangement of collagen fibres and covering layers in the tendon structure. Reproduced, with permission, from Kannus, P. (2000). Structure of the tendon connective tissue. Scand. J. Med. Sci. Sports. 10:312–320. (p. 313) © 2000 John Wiley & Sons Ltd. and which consists of a range of collagens (I, II, ables the tendon to maintain its structural integrity. III, V, VI, IX and XI), proteoglycans and water (see It has been suggested that forces generated end to Table 5.1 for relative proportions of components). end along the tendon are transferred along it by the matrix in shear connecting along the length of the The largest proportion of collagen contained in discontinuous collagen fibres (Ker 1999). tendon is type I, this lends strength to the tendon structure, whereas, the proteoglycans gives the ten- Components called integrins, which are described don its viscoelastic properties. as heterodimeric transmembrane proteins, form cell surface receptors that connect the tendon ECM to It is now well known that tendon is a metabolically the cytoskeleton. Thus these are part of the adhesion active tissue and adapts readily to influences such as complex, forming adhesion foci complexes at the mechanical loading and unloading (Heinemeier et al. cell membrane and are thought to be involved in the 2009). This can be understood as a dynamic mecha- complex signalling processes resulting in modifica- nism responding to feedback signalling via mechan- tions of structural proteins. These molecules when otransduction pathways in an attempt to optimise the activated for example via mechanical stress, can ini- tissue characteristics to its function. Previous work tiate chemical signalling cascade processes, such as has shown that tendon adapts to loading by modify- tyrosine phosphorylation, nuclear factor transcrip- ing its mechanical properties and dimensions. Sim- tion factor (NF-kB), mitogen activated protein ki- ilarly it has been observed that tendon mechanical nase (MAPK) pathway activation, either directly or properties such as compliance are increased with un- as part of the process involving other growth factors loading due to regulation of structural proteins, i.e. (see Figure 5.2). Another ECM molecule that is re- collagens. In line with this is the observation that ceiving some attention is tenascin C; this is also seen tendon elastic properties are associated with the at- to be up regulated with mechanical stimulus and is tached muscle (Muraoka et al. 2005) in that a muscle a ligand for integrin. The actual role of tenascin in that is able to generate large force will generally be tendon tissue is as yet not clear, but may involve attached to a tendon that has adapted to cope with actions related to tissue remodelling and general these forces. maintenance of the intercellular structures enabling gliding of bordering collagen bundles (Riley et al. The mechanisms of how the tendon responds to 1996). mechanical signals at a cellular level are still not well understood but are thought to involve the transduc- How integrins sense strain is not clear, in that tion of mechanical stressors via the ECM. The ECM although conformational changes are seen when forms the substrate for the anchoring of cells and en-

FUNCTIONAL ASPECTS OF TENDON 81 Table 5.1 Components of tendon tissue and relative constituent proportion (taken from Ker 2002). Reprinted, with permission, from Burgess KE, Pearson SJ, Breen L, Onambe´le´ GN. (2009). Tendon structural and mechanical properties do not differ between genders in a healthy community-dwelling elderly population. J Orthop Res. 2009 Jun;27(6):820–5. (p. 823) © Elsevier Water Wet mass (%) Dry mass (%) Collagen: total 65b, 53–70e, 75g, 60j 50a, 76b,c, 99.7d, 60–85e, 65–80f Type I 67g, 65h Type III 10.0b, 3.5c, 1.8g, 0h Type VI 2.0d Elastic fibers 2e, 1–2f Hyaluronan 0.01f, 0.09g, 0.10h Other proteins: total 4.6j Sulfated proteoglycans Decorin 1.0j Biglycan ‘Half the decorin amount’d Aggrecan ‘Little’i Other glycoprotein COMP 1.0i Anorganic <0.2f This list is indented only to give an indication of the main extracellular components. Other proteins which might be relevant, but for which I have not found quantitative data include tenascin-C, the small proteoglycans biglycan, fibromodulin, and lumican and the glycoproteins undulin and PRELP (Proline arginine-rich end leucine-rich repeat protein). Abbreviation: COMP = cartilage oligomeric matrix protein. aBank et al. (1999): human supraspinatus and biceps brachii. bBirch et al. (1999): horse forelimb superficial digital flexor. cBirch et al. (1999): horse forelimb deep digital flexor. dDerwin et al. (2001): mouse tail. eElliott (1965): general review. fKannus (2000): general review, giving ranges. gRiley et al. (1994): human supraspinatus. hRiley et al. (1994): human biceps. iSmith et al. (1997): horse. jVogel and Meyers (1999): bovine forelimb deep digital flexor. forces are applied and ligands bind, other possible dons may also experience compressive and shear strain sensing mechanisms may involve a link forces. For example, tendon can glide over bony ar- between the calcium channel responses to stretch eas to allow moment arms to be utilised, potentially (reviewed in Chiquet 1999). Calcium channels are increasing torque transmitted via the tendon. The observed to open transiently for a relatively short tensile properties of tendon allow for its capacity period with stretch, this response is seen to be down to resist rupture under normal loading conditions. regulated by interfering with the integrins (Chen Tendon is described as having viscoelastic qualities. and Grinnell 1995). These properties enable the tendon to act both as a damper to reduce potentially damaging high forces, Functional aspects of tendon but also as a storage medium for energy generated during movement. Tendon is sited between the muscle and bone and acts to transmit forces generated by the muscle to It is usual to describe the tendon response to load- the bone to enable movement. The forces experi- ing in terms of strain (percentage change of length enced by tendons are usually tensile, although due from rest) and stress (force per unit area). A typical to their arrangements with the bony anatomy, ten- stress–strain curve for human tendon can be seen in Figure 5.3.

82 TENDONS growth factor stretch stretch receptor EOM integrin PKC ras MAPKKK MAPKK IKK MAPK IκB MAPK NF κB eg. AP -1 NF κB Figure 5.2 Schematic diagram showing possible signalling pathways for the up regulation of collagen synthesis viaStress (MPa) mechanosensitive pathways (from Chiquet 1999). Reprinted, with permission, from Chiquet, M. (1999). Regulation of extracellular matrix gene expression by mechanical stress. Matrix Biology. 18:417–426. © Elsevier (p. 422) 45 40 35 30 Male Female 25 20 15 10 5 0 0 5 10 15 20 Strain (%) Figure 5.3 Stress–strain curve for elderly males and females (mean age 72 yrs) (Burgess et al. 2009b). Reproduced, with permission, from Burgess KE, Pearson SJ, Breen L, Onambe´le´ GN. (2009). Tendon structural and mechanical properties do not differ between genders in a healthy community-dwelling elderly population. J Orthop Res. 2009 Jun;27(6):820–5. (p. 823) (C) 2009 John Wiley & Sons Ltd.

FUNCTIONAL ASPECTS OF TENDON 83 Stress (N/mm2) Macroscopic failure Rupture Physiological range ‘toe’ Linear region Microscopic region failure Straighten Strain fibers (%) Crimped fibers Figure 5.4 Diagram showing elongation properties of tendon with progressive loading. Low load region (toe) shows characteristic greater strain than linear region, with subsequent plastic region leading to rupture. With respect to the strain, tendon has the charac- jected to approximately 12.2 kN during actions such teristics of larger strain at low load, due in part to the as competitive weightlifting (Zernicke et al.1977), crimp structure of the collagen fibrils, and a linear but under normal circumstances there is a relatively region where strain is proportional to stress, beyond large margin of safety. This is perhaps best illustrated this point the tendon starts to become plastic in that by considering the tendons involved in locomotion, it takes on a new resting length when the load is such as the Achilles; it has been determined that this removed. If stress is continued to be applied then ul- structure may experience forces in the order of 7 kN timately tendon rupture will result (see Figure 5.4). during running (Komi et al. 1992), this equates to ap- Tendons with less crimp have been observed to fail proximately 8.5 times body mass for an individual of before those with a more pronounced tendon crimp mass 80 kg. This may be even greater during actions pattern (Wilmink et al. 1992). This may be reflective such as long jump or triple jumping and has been of the mechanical connections between the collagen reported to be in the order of 9 kN during jumping fibrils and the ECM or some qualitative differences (Komi 1990). in the collagen structure. However, with regard to tendinous damage, it is Regarding the ultimate tensile stress for tendon more likely generally that tendons suffer what is tissue, a conservative limit has been suggested of termed fatigue damage resulting from repeated load- 100 MPa (Bennett et al. 1986). However Johnson ing cycles (see section on Chronic tendon injury). et al. (1994) examined human patellar tendons and estimated that the ultimate tensile strength was 65 ± Tendon has been shown to become damaged 15 MPa for young subjects. at strain values approximating 15% (Sta¨ubli et al. 1999), although these values have been previously Ker (2002) discusses ‘stress for life’, where a reported to be as high as 30% (Haut and Pawlison functional stress is determined from the ratios of 1990). A functional design aspect of tendon to help the tendon to the muscle cross-sectional area (csa) limit damage is that of the ability of the tendon fasci- and the product of the maximal isometric stress de- cles to slide with respect to each other whilst simulta- veloped by the muscle (0.3 MPa, Wells 1965), with neously transmitting forces along the tendon length. ranges from 8–100 MPa, but more normally approx- With respect to strain, it has previously been shown imating 13 MPa. It can be seen then that in certain that there are qualitative differences between male circumstances a tendon may be subjected to stress ands female tendon, with females having greater which may be nearing its rupture limit, for exam- compliance in comparison to males (Onambele et al. ple the patellar tendon has been reported to be sub- 2007). Similarly previous work has reported that in

84 TENDONS response to acute stretch females shown larger de- Short Long creases in tendon stiffness in contrast to males, this may have implications where stretching is used as Force part of a warm up (Burgess et al. 2009a). This may re- flect differences in the collagen content and/or com- Muscle length position between males and females. These gender differences do not seem to be retained in elderly Figure 5.5 Length–tension relationship for skeletal tendon, however (Burgess et al. 2009b), possibly re- muscle. flecting the changing hormonal influences on tendon being less disparate between the genders with age force development are required, tendon compliance and more similarities in lifestyle. could be seen as potentially detrimental to optimal performance. At the levels of loading seen routinely, ten- don may suffer micro damage at levels of strain The mechanical properties of the tendon, in par- seen normally, that is below 10%, leading to ac- ticular the stiffness, can also be seen to potentially cumulated deterioration in tendon (see section on affect the characteristics of muscle contraction. A Chronic tendon injury). Normal ranges of strain un- muscle’s contractile ability in part is described by der conditions of maximal isometric contraction for its length tension curve, by which the number of human tendon structures are within the ranges of elements that generate muscle force (cross bridges) 6–14%. The range of normalised elasticity (Young’s are increased or decreased dependant on the muscle modulus) for tendon is approximately 0.8–2 GPa. length (see Figure 5.5). Here it can be seen that if This property represents the normalised (corrected the tendon is compliant and stretches under load, the for differences in tendon length and cross section) muscle will shorten, and this could affect its ability stiffness of the tissue and is the gradient of the stress- to generate force. As can be seen from Figure 5.5, strain curve. if the muscle is starting from a position near maxi- mal force and the tendon stretches, the muscle will As tendons are also elastic they tend to stretch shorten moving down the force generating curve. when muscle contraction takes place. If, for exam- ple, the external load is very heavy, then as the mus- The position where the tendon attaches to bone cle contracts the tendon may stretch initially, the can have functional implications. A muscle can only action of the tendon here could be thought of as sim- extend or shorten over a given range; the points at ilar to a spring being stretched and energy stored. which tendon attaches to the bone can thus affect the This may be functionally important, an example of movement of the limb to which the muscle–tendon this could be where an athlete is sprinting or jump- complex is attached. This can be seen to be useful ing and the tendon is being subjected to stretch- from a functional standpoint where for example shortening cycles. This enables the movement to be force is preferred over range of movement and visa carried out with higher efficiency than if the tendon versa (see Figure 5.6 for example). Here, where the did not stretch and then shorten, in that the tendon tendon attaches closer to the joint centre of rotation is initially storing energy during the stretch, to be as in Figure 5.6A, the limb being affected can released during the shortening or recoil period. It move further for a given muscle shortening than has been reported that tendon has the ability to re- where the tendon attaches further from the rotation turn ∼93% of its stored energy during the recoil centre (Figure 5.6B). This is at a cost of reduced phase, the rest being lost as heat energy (Alexander torque generating ability. 2002). This particular property of tendon is perhaps useful where for example cyclical movements are Tendon injury and its management being carried out with changes in kinetic and poten- tial energy or to increase the power component as Tendon injury can be debilitating in so far as a dam- in jumping. The tendon can act to help smooth out aged tendon will likely reduce the capacity for trans- these changes and store some of the energy as elas- fer of forces via the muscle to the bone. This has tic strain energy to be returned to the system when obvious implications for a range of activities ranging required, reducing the overall work required for the muscles (i.e. running). However, where high rates of

ACUTE TENDON INJURY 85 changes to tendon (see Table 5.2 for descriptors, taken from Wang et al. 2006). With regard to acute tendon injuries, although a number of these could be identified due to extrinsic factors, such as direct contact with external body, or accidental unaccustomed loading such as extreme A B shear, the majority of acute tendon injuries show prior predisposing factors. These potentially con- tributory factors can be thought of as chronic inflam- matory or accumulative degenerative conditions and may be undetected prior to the acute trauma. Figure 5.6 Differences in limb range of movement with Acute tendon injury tendon attachment. A: Tendon attaches closer to joint cen- tre of rotation. B: Tendon attaches further from centre of Immediate tendon injury rotation than A. This can be perhaps best described as either complete from normal everyday movement to elite level ath- rupture of the tendinous structure or partial rupture. letic performances where perhaps high levels of Complete rupture will be self-evident and accompa- force and rates of force development are prerequisite. nied by loss of function, pain and swelling usually following the incident. On inspection it may be ob- Injury to the tendon can be characterised as acute vious that rupture has occurred in that a gap may resulting in either a catastrophic rupture or a less ma- be seen where the tendon would normally be. More jor tear of the tendon tissue. Alternatively the tendon specific diagnosis of rupture can be carried out using may suffer chronic pathological changes which may imaging techniques, such as ultrasound (see Figure be inflammatory or not even detectable. These fac- 5.7) or magnetic resonance imaging. Tendon injuries tors can affect the tendon at numerous sites along of this nature tend to be unilateral and of those re- its length. There appears to be no set consensus ported for the achilles, 75% were related specifically on description for the degenerative or pathological to sport (Jozsa et al. 1989 cited in Leppilahti and Orava 1998). The tendons mostly seen to be suffer- ing rupture are those bearing higher functional loads, such as the achilles and patellar tendons. Site of Table 5.2 Description for degeneration or pathological changes in tendon Term Description Reference Tendinitis or tendonitis Inflammation of the tendon Clancy et al. (1976); Almekinders and Temple (1998); Curwin and Stanish (1984); Tendinosis Asymptomatic tendon Schepsis and Leach (1987) degeneration Tendinopathy Puddu et al. (1976); Ja¨rvinen et al. (1997) Generic description for tendon Paratenonitis disorders Khan et al. (2002); Maffulli et al. (1998) Peritendinitis Spontaneous tendon rupture Inflammation of the paratenon Maffulli et al. (1998); Jozsa and Kannus (1997) Inflammation of the peritendon Maffulli et al. (1998); Jozsa and Kannus (1997) Partial rupture Tendon rupture without any Kannus and Jozsa (1991) Enthesopathy predisposing symptoms Karlsson et al. (1992); Karlsson et al. (1991) Incomplete tendon tear Maffulli et al. (1998); Kvist (1991) Tendon-bone junction disorders

86 TENDONS Figure 5.7 Saggital view of achilles tendon rupture in- (2007) demonstrated qualitative differences between dicated by arrows (from imaging consultant.com). male and female tendons in young adults with fe- males having more compliant structures. Whether tendon rupture has also been previously suggested this would result in a tendon more likely to be in- to be associated with hypovascular regions of the jured is not clear, however, if the two tendon struc- tendon. For example, achilles tendon ruptures typi- tures have similar strain limits it might be suggested cally occur 2–6 cm proximal to the insertion site at that for a given force the female tendon would be the calcaneus. This area along with the insertion site more likely to undergo permanent deformation and is also known to be poorly supplied with blood (Carr subsequent damage. and Norris 1989; Niculescu and Matusz 1988). More recently it has been reported that certain Causes classes of drugs, including antibiotics (flouroquino- lines) and corticosteroids, can affect the collagen There are a number of factors which are thought to tissue directly, leading to weakened structures that be responsible for acute tendon injury. These factors may rupture under high loading conditions (Sode can be separated into intrinsic and extrinsic factors. et al. 2007). The mechanism by which flouroquino- lines are thought to increase the risk of tendon injury A sudden, large force or torque applied through is linked to the increased activation of metallopro- the tendon, perhaps at an oblique angle could result teinase, a regulator of collagen degradation. in a partial or complete tear. How this force or torque presents may be due to either environmental factors – There has been suggested association between an- incorrect or accidental placement of the limbs in con- abolic steroids use and tendon injury. Of the studies text of the surface, abnormal surface conditions – carried out in animal models there have been reports and/or neural control mechanism failure, which may of morphological changes to the collagen structures. be accompanied by inappropriate muscle balance. In humans, however, this has not been shown. Evans But it is also suggested that in a number of acute in- et al. (1998) examined tendon tissue from individu- juries to the tendon, prior predisposing pathological als who had self-administered anabolic steroids for factors may have been present. Here, when strenu- between 1 and 10 years. Subsequent light and elec- ous activity is routinely carried out it is possible that tron microscopy analysis of the tendon indicated cumulative damage may occur leading to a catas- no differences from normal. There is some initial trophic failure of the tissue (Ja¨rvinen et al. 2001). case study evidence to suggest there is an associ- The mechanisms underlying this will be discussed ation between steroid use and tendon rupture. One in more detail in section on Chronic tendon injury. such case involved an individual presenting with a relatively rare case of bilateral quadriceps tendon It has been reported that males present with ten- rupture, which was subsequently suggested to be as- don injuries more often than females, however, it is sociated with the earlier intake of anabolic steroids not clear if this is due to more participation in sport (Liow and Tavares 1995). Regarding the mechanism by males and thus more exposure to risk of injury responsible for injury with the intake of steroids, it (Clayton and Court-Brown 2008). Onambele et al. may be that as the ability to generate high forces increases due to the anabolic effects on muscle, the tendon simply cannot keep pace with this increased ability and therefore succumbs to injury. Previously, Unverferth and Olix (1973) showed, in a number of cases involving athletes who had received localised corticoid steroid injection of the tendon, that there was an association with the use of corticosteroid and subsequent tendon rupture. A series of experiments on animal tendons led them to suggest this may have been due to resultant dis- ruption of the tendon collagen matrix, and this was aligned with a reduced modulus of elasticity for those tendons.

CHRONIC TENDON INJURY 87 Recent evidence has indicated that there may be a morphological adaptation of the tendon tissue (see link between certain specific gene polymorphisms Table 5.3 for characteristics of tendon pathologies). and tendon injury. Mokone et al. (2005, 2006), A more general and suitable clinical term that does showed a relationship between the COL5A1 and not attempt to describe the pathologies associated tenascin C gene and achilles tendon injury rates. with the condition has been suggested as “tendinopa- These genes can be seen to be important to the struc- thy” (Mafulli et al. 1998). tural integrity of tendon as the COL5A1 gene is known to code for collagen structural components, Causes whereas the tenascin C gene encodes for the extracel- lular matrix component tenascin C. This component Tendinopathy can be directly associated with the is understood to be involved with the transmission volume or intensity of tendon loading and this can of forces throughout the tendon and is a component be modified by other factors such as age, gender that is upregulated in response to mechanical load- (Astro¨m et al. 1998; Riley et al. 2001), body mass, ing, suggesting a role in tendon remodelling. disease and oral contraceptives in females (Holmes and Lin 2006). Where loading is inappropriate the With respect to the optimal method for repair tendon may suffer continual minor damage from and subsequent rehabilitation treatment of tendon which the tendon is not able to recover for any num- ruptures, no consensus exists. Although there is in- ber of reasons, leading to eventual clinical signs of creasing evidence to suggest that where the individ- injury or damage. As a mechanism for ‘non-coping’ uals are relatively active and able, surgery may be tendons, the vasculature supplying the tendon may advantageous, providing better functional capacity have a part to play. Here the blood supply is required over non-operative options (Schepsis et al. 2002); to provide requisite healing components as part of whereas, for those who are more sedentary, less in- the process. If this system is not able to carry out vasive non-operative treatments may be advocated. this task optimally the tendon may not recover from The following case study illustrates the use of a re- the trauma. Previously poorly perfused tendon tissue cent methodology to aid in the repair of a ruptured has been linked with spontaneous tendon ruptures rotator cuff tendon. Here a patient underwent surgery (Yepes et al. 2008). Interestingly though, tendinopa- involving the use of a “cascade membrane” to knit thy shows hypervascularisation of the tendon with- the tendon and accelerate healing. The membrane out an associated healing response, this contrast is consisted of a thin layer of autologous fibre saturated difficult to explain and may be indicative of break- in platelets, the idea being that platelets are responsi- down of the cascade system responsible for normal ble for the production of growth factors responsible healing. This increased vascularisation has been re- for promoting healing. Here the membrane provided ported to be responsible for the pain associated with both mechanical strength to allow connection of the tendinopathy (Alfredson et al. 2003). Recently, re- tendon ends and an environment for optimal heal- searchers have suggested that insertional overuse in- ing. After surgery the patient was immobilised for a juries may be characterised by compressive forces period of four weeks and a standard rotator cuff re- rather than tensile loading. Here the suggestion is habilitation protocol carried out. MRI examination that the change from tensile to compressive loading of the repair after six months indicated a complete at the tendon origin during knee flexion could result and robust repair of the ruptured tendon (Maniscalco in adaptations of the tendon structure making it more et al. 2008). susceptible to injury (Johnson et al. 1996; Hamilton and Purdam 2004). However, recently a study in- Chronic tendon injury vestigating the aetiology of patellar jumper’s knee reported that forces present at the patellar origin site Definitions were in fact tensile in nature, showing that patellar strain increased with loading but also that tendon There are a number of definitions for chronic ten- strain increased with decreased patellar-patellar ten- don pathological changes generally associated with don angle (Lavagnino et al., 2008). The minimal increased tendon usage, these range from terms to patellar-patellar tendon angle was also shown to co- describe degeneration and the failing of the healing incide with predictions of knee angle for maximal response, to those used to describe inflammation and

88 TENDONS Table 5.3 Characteristics of tendon pathologies (from Xu and Murrell 2008). Reprinted, with permission, from Xu, Y and Murrell, G. (2008). The basic science of tendinopathy. Clin. Orthop. Relat. Res. 466:1528–1538. (p. 1529). © The Association of Bone and Joint Surgeons Tendon Macroscopic Ultrasound/doppler Light microscope Electron microscope category imaging r Brilliant white r Organised parallel r Dense collagen fibre Normal r Parallel r Firm texture collagen fibres structure hyperechoic r Uniform fibre diameter r Regular fibre r Spindle shaped and alignment structure tenocytes r Angulation of collagen r Parallel nucleus fibres arrangement r Heterogeneity of collagen Tendinopathic r Grey/brown r Localised widening r Disorganised tendon r Thin disorganised r Hypoechoic areas diameters and r Irregular structures collagen fibres r Loss of aligned nuclei r Neovascularisation r Increased vascular ingrowth r Increases in proteoglycans and glycosaminoglycans knee loading (60◦ ) (Pflum et al. 2004). Hence, here Although inflammation is common to injury, it is it can be seen that either deep knee flexion, high generally thought that tendinopathy is not associated loading or a combination of both could predispose with inflammation. In that tendons generally present the tendon to injury where the architecture of the as painful and histological degenerative changes are tendon–bone connection could cause increased lo- evident such as increased cellularity and rounded calised tendon strain. cells rather than elongated or striated cells, along with ECM remodelling, which includes reductions A common response to injury or damage is in- in total collagen (Riley et al. 1994). flammation; hence the molecular markers of inflam- mation can be used to identify potential damage. Diagnosis of tendinopathy would include the tak- Tendon responds differentially to cyclical loading ing of patient history to determine if pain was present or strain. A previous study examined the effects of and for how long. The characteristics of pain are also strain on tendon expression of inflammatory me- considered, that is present only after activity, present diators. Where strains were relatively low, that is during but not sufficient to interfere with the activ- approximating 4%, no deleterious effects on ten- ity, present during activity lasting into period after don were shown; however, with strains of 8% activity ceases and sufficient to interfere with activ- up-regulation of genes associated with inflamma- ity, or ultimately total tendon failure may present. A tion (COX-2, MMP-1 and prostaglandin E2) were visual inspection can be made of the kinematics of noted (Yang et al. 2005). This study suggests then the segments to identify any irregular aspects. As- that moderate load or strain may be appropriate sessment of the affected site may reveal swelling, for tendon homeostasis, whereas, higher loading tenderness and nodularity or crepitus. Other valid can lead to damage, which may accumulate if tools used are the Victorian Institute of Sport As- frequent. sessment Questionnaire (VISA) for the patellar or a

KEY POINTS AND SUMMARY 89 variant of this for the achilles (Visentini et al. 1998; with tendon having an oxygen consumption of ap- Robinson et al. 2001). Imaging techniques allow for proximately 13% of skeletal tissue (Zernicke et al. the quantification of the tendinopathologies, and typ- 1977). This results in a much slower healing pro- ically ultrasound or magnetic resonance imaging is cess than would be evident with higher metabolic used to determine tendon anomalies. Linear ultra- rates. This less adequate metabolic process is partly sound probes with a frequency range of between 7.5 due to the limited blood supply to the tendon tissue. and 15 MHz are able to spatially resolve superficial Subsequent to injury there are distinct but overlap- tissue to less than 0.1 mm (Martinoli et al. 1993). Ul- ping healing responses, the early phase is delineated trasound imaging has been utilised to describe three by inflammation, next the secondary phase involves different levels of tendinopathy: (1) normal tendon synthesis and is termed remodelling, followed by the image, (2) enlarged tendon area, and (3) hypoechoic final stage where refinement of the tissue takes place area to tendon (Archambault et al. 1998). MRI is a and is appropriately termed the modelling phase. very useful imaging methodology, in part because of its high spatial and contrast resolution, and is Cytokines, in particular neutrophils are associated able to generate 3D images of the tendon structures; with initiation of the inflammatory phase, vascular however, it is still relatively expensive and operator permeability is increased and damaged material intensive in contrast to ultrasound imaging. is removed via phagocytosis, with monocytes and macrophages invading the damage site within the Treatment first 24 hours. These mechanistic responses also bring about initiation of angiogenesis and tenocyte Treatment of tendinopathy can be by a number of proliferation and migration to the damage site, different methods. which results in increased type III collagen synthe- sis. During the remodelling stage, which is evident As tendinopathy has been associated with after the first two days or so, type III collagen increased vascularisation and also pain, a previous synthesis continues to increase, with the peak study examined the therapeutic value of utilising a occurring during this phase. Next, after a number sclerosing agent (Polidocanol) in order to try and of weeks there is a down regulation of collagen reduce the localised vascularisation. O¨ hberg and production, during weeks 6–10 there is a gradual Alfredson (2002) reported that the use of Poli- change in the new tissue from cellular to fibrous. It docanol in 10 patients presenting with achilles is during this ‘consolidation’ stage that the collagen tendinosis resulted in 8 out of 10 patients showing fibres align to the direction of stress. With time there improvements in the condition and reductions in is a gradual reduction in both the tenocyte activity vascularisation of the affected areas. and vascularisation of the tendon tissue injury site. In addition, during this period there is a changeover A case study is presented here for a 35-year-old from predominantly type III collagen production to tennis player complaining of pain at the flexor carpi type I. After a period of approximately 10 weeks the ulnaris tendon site. The use of a sclerosing agent remaining fibrous tissue begins to be modified into was applied based on the finding of neovasculari- tendon tissue that is scar-like, this process continues sation of the injury site. Polidocanol (1.5 ml) was for up to one year and is sometimes referred to as injected to the site of neovascularisation, guided by the maturation phase. power and laser doppler spectrophotometry. This ini- tial treatment reduced the neovascularisation by ap- Key points and summary proximately 25%. Further treatment after a short rest was in the form of eccentric resistance loading (Ther- Tendon is a highly adaptive structure capable of cop- abands) of the forearm for a period of 12 weeks (6 × ing with varying demands put on it. 15 repetitions day−1) after which the patient reported no incidence of wrist pain (Knobloch et al. 2007). The viscoelastic nature of tendons modifies the muscle output potential and enables the efficient stor- Tendon healing age and release of energy. Tendons by nature have a much lower metabolic The mechanisms by which tendons “sense” me- rate than associated tissue such as skeletal muscle, chanical loading are still not well understood but may involve proteins that connect the tendon ECM to the cytoskeleton. These proteins may somehow be

90 TENDONS connected via stretch sensitive ion channels to enable pre-injury levels of activity, or conservative, which signalling events leading to collagen synthesis. usually results in fewer complications such as infec- tions. There is currently no consensus on the best Injury to tendon can be categorised as acute or form of treatment, either repair or rehabilitation. chronic. Where acute injury occurs it is suggested However, there are a number of recent developments that predisposing factors are present in many cases. that show promise. Overuse injuries can be described as chronic References tendon injuries and fall into the description for tendinopathies. Alexander, R.M. (2002) Tendon elasticity and muscle function. Comparative Biochemistry and Physiology, Clinical diagnosis of tendinopathies involves Part A, Molecular and Integrative Physiology 133 (4), manual and visual elements. Pain may or may not 1001–11. be present, but changes to the tendon may include swelling, crepitus, tenderness, and or nodularity. Alfredson, H., Ohberg, L. and Forsgren, S. (2003) Is vasculo-neural ingrowth the cause of pain in chronic Imaging has been utilised to help diagnose Achilles tendinosis? An investigation using ultrasonog- tendinopathy, both US and MRI are able to identify raphy and colour Doppler, immunohistochemistry, and stages associated with tendinopathic changes, such diagnostic injections. Knee Surgery Sports Traumatol- as enlargement of the tendon and hypoechogenic ar- ogy and Arthroscopy. 11 (5), 334–338. eas to the tendon. Almekinders, L.C. and Temple, J.D. (1998) Etiology, di- Treatments of acute and/or chronic tendon injuries agnosis, and treatment of tendonitis: an analysis of the are dependant on site of injury, activity levels or literature. Medicine and Science in Sports and Exer- expectations of patient, the specific tendon injured cise, 30 (8), 1183–1190. and the grade of injury. Archambault, J.M., Wiley, J.P., Bray, R.C., Verhoef, M., Many treatments involving pharmacological in- Wiseman, D.A. and Elliott, P.D. (1998) Can sonog- tervention are available, for example NSAIDS have raphy predict the outcome in patients with achillo- been used with some degree of success to reduce dynia? Journal of Clinical Ultrasound, 26 (7), 335– swelling and symptoms of tendinopathy. More re- 339. cently, sclerosing injections have been utilised with good results to reduce the neovascularisation seen in Astro¨m, M. (1998) Partial rupture in chronic achilles some cases (described in earlier section). It remains, tendinopathy. A retrospective analysis of 342 cases. however, that no one treatment is a best option where Acta Orthopaedica Scandinavica 69 (4), 404– non-invasive conservative treatments are advocated. 407. Where surgery is advocated there are again many Bennett, M.B., Ker, R.F., Dimery, N.J. and Alexan- different methodologies present to repair tendon, this der, R.M. (1986) Mechanical properties of various chapter has presented a recent development whereby mammalian tendons. Journal of Zoology, 209, 537– growth factors are encouraged within the repair by 548. use of a patch saturated with platelets. Rehabilita- tion of the tendon following either acute or chronic Burgess, K.E., Graham-Smith, P. and Pearson, S.J. (2009) injury involves a period of rest or immobilisation Effect of acute tensile loading on gender-specific ten- followed by a gradual, progressive development of don structural and mechanical properties. Journal of strengthening and mobilising exercises. Recently ec- Orthopaedic Research, 27 (4), 510–516. centric exercise has been advocated as a particularly useful adjunct to successful rehabilitation of tendon Burgess, K.E., Pearson, S.J., Breen, L. and Onambe´le´, injuries; suggested mechanisms for this include high G.N. (2009) Tendon structural and mechanical prop- frequency oscillation of force during loading (Rees erties do not differ between genders in a healthy et al. 2008). community-dwelling elderly population. Journal of Orthopaedic Research, 27 (6), 820–825. In conclusion, tendon injury is a complex, mul- tifaceted issue. Injury can be cumulative or sudden Carr, A.J. and Norris, S.H. (1989) The blood supply of and can appear suddenly without any precognition the calcaneal tendon. The Journal of Bone and Joint of a problem. Repair of tendon can take the form Surgery, 71 (1), 100–101. of surgery, which tends to have a better outcome in terms of functionality and time taken to get back to Chen, B.M. and Grinnell, A.D. (1995) Integrins and modu- lation of transmitter release from motor nerve terminals by stretch. Science 269 (5230), 1578–1580.

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6 Pathophysiology of ligament injuries Dror Steiner Chartered Osteopath As ligaments injuries are common both in athletes Ligaments are made up primarily of type I col- and the general public, this chapter’s aim is to famil- lagen, with normally 1–2% oelastic fibre (Frank iarise the reader with the anatomy, physiology and 1996). During ligaments’ healing, type III colla- pathology of ligamentous structure and function, and gen levels increase and this is the reason for the then progress on to the healing process of ligamen- weakening of ligaments at that point (Frank et al. tous structures. Later on, this chapter will illustrate 1987). Ligaments, such as ligamentum flavum and this process by introducing two of the most common ligament nuchae, have a different structure with a ligamentous injuries and their available treatments. higher content of elastic fibre, which allows recoil and saves muscular energy moving the spine back Introduction to the anatomical position from flexion (Yong-Hing and Reilly 1976). Ligaments of the skeletal system are dense connec- tive tissues that attach bones across a joint. Liga- Like other connective tissues, ligaments have a ments play an important role in the neuro-muscular hierarchal structure (Figure 6.1). system by providing joints’ stability and sending sensory feedback to the central nervous system with Each ligament is built by multiple fascicle units. information about stress, tension, joints’ motion, Each fascicle carries the collagen fibrils and fibrob- stretch and pain (Riemann and Lephart 2002a). lasts cells in longitudinal lines and encapsulates them in a loose connective tissue called endoliga- Anatomy ment. Fascicles are separate enough to allow shear- ing movements occurring at different joint’s position Fibroblasts are the cells that reside in ligaments (Frank 1996). The entire ligament is covered with a producing both the matrix and the collagen fibre. vascular epiligament, a loose connective tissue that Fibroblasts are arranged in longitudinal rows paral- does not undergo much tension during the ligament’s lel to the fibres and communicate with each other by tightness (Ian et al. 2002). a gap junction, a mechanism that is poorly under- stood (Chi et al. 2005). The enthesis is the insertion of a ligament to the nearby bone and has a special arrangement The matrix is composed of proteoglycans and col- (Figure 6.2). This is where the collagen fibres fan-out lagen fibres. In ligaments the most common proteo- and are attached diagonally to bones via the perios- glycan is decorin, which strengthens the links be- teum. This arrangement helps in dissipate the liga- tween collagen fibres (Ilic et al. 2005). ment stress more evenly to the bone during different joint’s position (Benjamin et al. 2006). Sports Rehabilitation and Injury Prevention Edited by Paul Comfort and Earle Abrahamson C 2010 John Wiley & Sons, Ltd

96 PATHOPHYSIOLOGY OF LIGAMENT INJURIES Tertiary Endotenon tissue, ligaments are hypovascular and their blood fiber Primary supply is better closer to the bones’ attachments; the middle section is poorly supplied (Bray et al. 1996). bundle fiber bundle (subfascicle) The blood supply to ligaments may arrive from three places. The epiligament carries blood along Collagen the ligament, where blood vessels branch out to the fiber endoligament and inside the fascicles. A build up of tension in the ligament will reduce the amount of Epitenon Secondary Collagen blood circulating, but will recover at rest (Bray et al. fiber bundle fibril 1996). The periosteal blood supply supplies mostly (fascicle) the enthesis region of the ligament. The surrounding connective tissues such as fat, joint capsule or mus- Figure 6.1 Ligament structure. cles may carry some blood that collaterally supplies ligaments (Arnoczky 1985; Bray et al. 1996). One character of the fascicle is the “crimps” – a waviness of the fibrils. The crimps give the ligaments Following injury, the vascularity increases for its pseudo-elasticity and disappear once the ligament about 40 weeks while the ligament’s fibres become is stretched (Scott 2003). disorganised. The increased vascularity allows heal- ing. The final post-injury state is a reduced vascular- Many ligaments are attached to the joint capsule, ity (compare to the pre-injury level) with poor vessel tendons and other connective tissue and cannot be organisation in the scar tissue. Ligaments probably separated anatomically and functionally, hence the do not have the ability to keep the original vascu- common injuries where more than one tissue is lar organisation, causing reduced vascularity in the damaged. chronic healing stage, which may be the causes of higher level of reinjures. Blood supply Nerve supply The blood supply to ligaments deserves a special examination as in most cases it is the limiting factor Ligaments carry two types of sensory impulses to the in healing injured ligaments. Compared with other central nervous system: mechanoreceptor and pain. Midsubstance Composition A Collagen (60% dw) including type I (III, IV, V, VI, XII, XIV) Insertion B Proteoglycan (0.5% dw) including decorin, versican, lumican Glycoproteins (5% dw) including tenascin, COMP, elastin T C As above, but also includes: F collagen type II, IX, XI, aggrecan, biglycan CM Figure 6.2 The enthesis. Reprinted, with permission, from Nature Clinical Practice in Rheumatology (2008) 4, 82–89 doi: 10.1038/ncprheum0700 © Nature Publishing (2008)

PHYSIOLOGY 97 Mechanoreceptors signal mechanical events occur- ligamentous tension, which sends a corrupt sensory ring in the tissue and have an important role in the message to spinal muscles to contract continuously, coordinated motion pattern. Ruffini receptors are the causing those muscle to be in chronic tension and most common mechanoreceptors in ligaments and fatigue (Panjabi 2007). joint capsule, whilst the others are Pacinian, Golgi tendon organ-like and free nerve endings. All of Physiology these receptors allowing the central nervous system to assess the amount of stress joints undergo and ex- Ligaments have similar mechanical properties to ecute patterns of muscle contraction to help protect other connective tissues: viscoelasticity and stress- joints over stretching (Riemann and Lephart 2002b). strain (Norking and Levangie 2005). Following an injury both the peripheral and central The first mechanical property of a ligament is its nervous system undergo modifications. non-linear stress-strain relationship (see Figure 6.3). One study found that the post-injury instability of The stress-strain graph (Figure 6.3) demonstrates the anterior crutiate ligament is due, in part, to re- three regions: modelling of the central nervous system. The remod- elling is probably due to the habitual reduction of us- 1. Toe region - this is where the deformity (liga- age of that area (Valeriani et al. 1996). As ligaments ment length) is high while the force applied is become strained and torn so the nerves supply loses low. Anatomically, this is where the fibrils’ crimps a certain amount of receptors. This by itself can dam- slack begins to tighten. The toe region is where age the peripheral nervous system and prevent it from most ligaments are at rest. accurately suppling the central nervous system with a real-time sensation of what happened to the joint. 2. Linear region - this is where a stress build up creates a linear build up of strain or stretch to In any case, following an injury it is probably both the ligament. This region demonstrates ligaments the central and peripheral nervous systems that are during a normal joint’s movement. damaged and so supply corrupted sensory input to the central nervous system. This, in turn corrupts the 3. Failure region - this is where even a mild increased muscular contraction pattern (Riemann and Lephart stress to the ligament creates a large deformation 2002b). One author’s hypothesis is that some cases of as the ligament is overstretched or torn. back pain, for example, may originate from chronic 250.00 Linear Region Wield and Failure Region Top Region 200.00 150.00 100.00 .00 0.00 0.00 1.00 2.00 3.00 4.00 5.00 6.00 7.00 8.00 Deformation (mm) Figure 6.3 Stress-Strain graph. Reprinted from Mow, V.C. and Hayes, W.C. ‘Basic Orthopaedic Biomechanics’ (ISBN: 9780881677966) © 1991, Lippencott, Williams and Wilkins

98 PATHOPHYSIOLOGY OF LIGAMENT INJURIES Load Constant Load deformation the stress will be reduced. For example, Creep if a ligament will elongate during load, the stress will be reduced compared to a situation where the Deformation ligament will stay at a constant length. Time A The third viscoelastistic property is hysteresis (Figure 6.6). Under load, ligaments undergo Figure 6.4 Ligament creep. Reprinted from Mow, V.C. deformation that does not immediately return to and Hayes, W.C. ‘Basic Orthopaedic Biomechanics’ the original length after unloading the joint. The (ISBN: 9780881677966) © 1991, Lippencott, Williams difference between the length before loading and and Wilkins after unloading represents the amount of energy lost in the process. If, for example, the joint is loaded The stress-strain graph never perfectly occurs as and unloaded many times, the stress-strain curve the ligament also exhibits viscoelasticity property. would move to the right, showing an increase strain Viscoelasticity is a tendency of the tissue to to the same stress. stretch and return slowly to its normal form whilst dampening the shearing force. There are Figure 6.6 illustrates how loading a ligament many three viscoelasticity tissue behaviours: creep, stress- times in a short period can cause a strain or a tear if relaxation and hysteresis. there is not enough recovery time between the cycles. Creep is the tendency of slowly increasing the Normal changes to ligament through life ligament’s deformation under a load and the return to normal shape once the load is taken away (Fig- Ligaments exhibit adaptation to external and internal ure 6.4). For example, under a load the ligament changes. will slowly elongate, and then return to its original length once the load is taken away. The rate of creep The effect of exercise and long-term immobility increases at high temperature. to ligaments are known and directly relate to the property of collagen fibrils to increase its thickness in The second viscoelasticity property is stress relax- response to exercise and reduce thickness in response ation (Figure 6.5). This means that under a constant to immobility (Kannus et al. 1992). There are no differences between pre-puberty male and female ligamentous structure. However, following puberty females show an increased joint laxity (Quatman et al 2008). Before puberty the rate Deformation Loading Cycle 1 2 3 4... Constant Deformation Stress Stress Stress Relaxation Time B Strain Figure 6.5 Stress relaxation relationship in ligaments. Figure 6.6 Hysteresis. Reprinted from Mow, V.C. and Reprinted from Mow, V.C. and Hayes, W.C. ‘Basic Or- Hayes, W.C. ‘Basic Orthopaedic Biomechanics’ (ISBN: thopaedic Biomechanics’ (ISBN: 9780881677966) © 9780881677966) © 1991, Lippencott, Williams and 1991, Lippencott, Williams and Wilkins Wilkins

TREATMENT AND THE HEALING PROCESS 99 of anterior crutiate ligament (ACL) injury is equal Fascicle male to female, but the post-puberty injury rate is at least 3-fold higher in adolescent females (Agel Epiligament Endoligament et al. 2005). Normal The knee crutiate ligaments express the sex hor- ligament mone receptors for oestrogen, testosterone and re- laxin (Faryniarz et al. 2006). There is an increased Ligament risk of ACL strain during the pre-ovulation stages scar of menstrual cycle, where hormone levels change from a low to high level (Slauterbeck et al. 2002). Figure 6.7 The healing ligament and creating of a scar Due to different individual hormonal profiles during tissue. Reprinted from Mow, V.C. and Hayes, W.C. ‘Basic menstrual cycle there is a significant difference to Orthopaedic Biomechanics’ (ISBN: 9780881677966) © the amount of ligamentous laxity and risk of injury 1991, Lippencott, Williams and Wilkins (Shultz et al. 2006). and the gap becomes filled with scar tissue (Frank In the elderly there is an increase in joint capsule et al. 1992). Fibroblasts start producing scar tissue and ligaments laxity, which may be one of the rea- made by type III collagen. This collagen-type sons for the increase in incidents of osteoarthritis material creates a rapid, disorganised structure with (Rudolph et al. 2007). weaker cross links to fill the gap between the ligament’s edges quickly (Frank et al. 1987). Pathology Followed is the long remodelling period, which Pathological changes in ligaments may occur due can take months or even years as the matrix and col- to structural and functional failure. Any strain to lagen fibres are rearranged to have stronger bonds. a ligament may cause a long-term joint instability. There are agreed degrees of ligaments strain: 1st The healing process depends on few parameters: degree is mild, 2nd degree moderate and 3rd degree an isolated strain heals better than when it combines is a complete tear (Chen et al. 2008). with other tissue’s injury; the degree of the injury; certain ligaments heal better than others (such as the Following a strain, ligaments do not heal by pro- MCL compared with the ACL); and failure of the ducing an identical tissue; instead, a scar tissue is repair process can appear months post injury (Frank formed. The scar tissue presents with an uneven ma- et al. 1992). The viewpoints of the main two treat- trix, smaller in diameter collagen fibers, weaker col- ments are the immobility, long rest and braces versus lagen crosslinking and a limited creep (Figure 6.7). the sooner-than-later active treatment (see below). The blood circulation is also affected with a long- A systematic review finds no data to support term reduction in blood circulation to the scar tissue any benefits from using braces in sprained ligament (Bray et al. 1996). Although scar tissue is formed rel- (Pietrosimone et al. 2008). atively fast, there are still mechanical and chemical changes months and years after the injury, though it Another study found that early activity, rather never has a normal appearanceor function again, re- than long immobility, would make the healing time sulting in a high level of reoccurrences (Frank et al. 1999). Ankle sprains, for example, reoccur in 73% of all athletes (Yeung et al. 1994). As ligaments provide the proprioceptive sensory nerve supply to the central nervous system, any liga- ment injury may cause further problems in the neuro- muscular system. Treatment and the healing process Following a strain injury, the gap within the ligament fills with blood to start the inflammation phase. Fibroblasts proliferate, the ligaments revascularise

100 PATHOPHYSIOLOGY OF LIGAMENT INJURIES shorter, more complete and that the ligaments would Increased factors for sprain injuries are previous appear stronger (Woo et al. 1987; Frank et al. 1992). sprains, wearing shoes with air cells, being over- Immobility affects the ligament on a cellular level weight, not stretching before sports activities, in- with the fibroblasts appearing uneven. creased foot width and weak active eversion and dorsiflexion (Daniel et al. 2009). Immobilisation of For grades I–II a non-operative active treatment the sprained joint was found to be less effective than approach is the most common (Chen et al. 2008) active treatment (Kerkhoffs et al. 2001). and usually comprises rest (for a limited period), ice, compression and elevation (RICE), isometric and The most common treatment for grade I and II isotonic exercises and proprioceptive training. The during an acute sprained ankle is RICE (Cooke et al. rationale of using the RICE treatment is to reduce 2003). Early exercise, which includes dorsiflexion the inflammation during the acute phase. and plantarflexion range-of-motion exercises, and isometric and isotonic strength-training exercises are Proprioceptive training concentrates mostly on the recommended by many authors (Trevino et al. 1994; lower limb, in particularly post sprain in the ankle Lynch and Renstrom 1999; Safran et al. 1999). joint. The idea behind it is to maintain the propri- oceptive neural function by continuously using the Another treatment is balanced and coordina- joint in a challenged position. It has been found that tion training performed on the wobble board, even the use of unsupervised, home proprioceptive both as a treatment and preventative measurements exercises reduces the rate of reoccurance in atheletes (Mattacola and Dwyer 2002). It appears to halve the (Hupperets et al. 2009). reoccurrence of a sprained ankle ligament. This ex- ercise enhances the proprioceptive neural function of Another treatment method is exercise, which aims the central nervous system and reduce the response to improve the proprioceptive property of the dam- time of the peroneal and other muscles around the aged ligament and to strengthen the muscles sur- ankle joint to protect the ligaments from reinjury rounding the affected joint (Olsen et al. 2005). (McKeon and Hertel 2008). Examples of ligament injuries A meta-analysis found that for grade III sprain ankle the possibility of surgical ligament reconstruc- Lateral ankle sprain tion is controversial (Lynch and Renstrom 1999). This research found that only late ligament recon- The ankle joint is one of the most common sites struction appears to be better than a conservative of ligament injury with a higher reoccurrence rate treatment after all other treatment modalities fail to compared to other ligament strains (Hubbard and produce joint stability. Hicks-Little 2008). It occupies 0.6% of all cases in Accident and Emergency in the U.K., with higher Anterior crutiate ligament sprain rate of 1.3% in young girls (Bridgman et al. 2003). At 14%, ankle sprains are the most common acute sports ACL resists anterior tibial translation on the fe- injury (Fong et al. 2009) with 59% of reoccurrence mur and rotational motion at the knee joint. ACL (Yeung et al., 1994). can withstand multiple stresses and varying ten- sile strains at the same time, a property that is not The most common ligamentous injury is to the yet achieved with any ACL artificial reconstruc- lateral ankle, and to the anterior talofibular ligament tion (Duthon et al. 2006). Non-contact ACL injuries in particular (Daniel et al. 2009). can arise during deceleration and acceleration mo- tions, an excessive quadriceps contraction together The anterior talofibular ligament is the weakest with reduced hamstrings co-contraction, where the ankle joint ligament while limiting a relatively large knee internally rotated at or near full knee exten- inversion at the subtar joint (Attarian et al. 1985). sion (Shimokochi and Shultz 2008). In all of those position there is a higher force applies on the ACL. Lateral ankle injury happens mostly by an exces- ACL injury is more common in contact sports, with sive supination due to mechanical and/or functional the highest rate in footballers (Hootman et al. 2007). instability. Mechanical instability can arise due to The exact damage to the ligament will determine the certain muscular weaknesses, knee or other joint length of the healing process. For example, if the problems, or degenerative changes. Functional in- stability can arise from a lack of proprioception or coordination (Hertel 2002).

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7 Pathophysiology of skeletal injuries Sarah Catlow University College Plymouth St Mark & St John, Plymouth Introduction to adapt its structure to imposed loads has become known as Wolff’s Law: Skeletal injuries are common in sport, especially in contact sports, such as football and rugby, and in in- Wolff’s law: dividual sports such as skiing and gymnastics. This chapter provides an overview of the skeleton and its “states that bone responds to the stresses component parts. Special attention is paid to the pro- that are imposed upon it by rearranging its cess of bone formation or ossification and its unique initial architecture in the best way to with- implications for healing following skeletal injuries. stand stress (Porter 2008) The chapter further considers principles of rehabil- itation in relation to skeletal injury and pathology. Bones function as: The use of annotated diagrams and schema, within the chapter, further emphasise important processes r Protectors of vital organs – provides mechanical in skeletal organisation (Figure 7.1). protection for most of the body’s internal organs, The skeleton can be divided into two subgroups: thereby reducing the risk of injury to them 1. Axial skeleton – bones of the skull, vertebral col- r Supportive structures – the skeleton is the frame- umn, ribs and sternum work of the body it provides attachment for skele- 2. Appendicular skeleton – bones of the upper and tal muscles lower limbs. r Levers – the skeleton assists with movement Bone is a living, well-organised, vascular form of r Reservoirs for calcium and phosphorus – storage connective tissue. It is largely composed of an or- ganic protein, collagen, and an inorganic mineral, for minerals (calcium and phosphorus), which are hydroxyapatite, which combine to provide a me- released when needed into the blood chanical and supportive role in the body (Smith et al. 1983). Bone is a dynamic tissue that requires r Blood producing cells – develops red blood cells stress for normal development. The capacity of bone in the bone marrow. Sports Rehabilitation and Injury Prevention Edited by Paul Comfort and Earle Abrahamson C 2010 John Wiley & Sons, Ltd

106 PATHOPHYSIOLOGY OF SKELETAL INJURIES SPINAL COLUMN SKULL SPINAL COLUMN Cranium Cervical Cranium Vertebrae Atlas C1 C1 - C7 Mandible Cervical Mandible Thoracic Vertebrae Vertebrae Clavicle C1 - C7 Clavicle T1 - T12 Manubrium Scapula Scapula Thoracic Humerus Lumbar Sternum Vertebrae Ribs Vertebrae Ribs T1 - T12 L1 - L5 Ulna Humerus Lumbar Radius Sacrum Vertebrae Pelvis Coccyx Ulna L1 - L5 Radius Pelvis Sacrum Coccyx C ... M ... Carpals P ... Metacarpals Phalanges Femur Femur Patella Tibia Tibia Fibula Fibula AXIAL SKELETON APPENDICULAR SKELETON Tarsals Tarsals Calcaneus Metatarsals Metatarsals Phalanges Phalanges Figure 7.1 Components of the axial and appendicular skeletons (taken from Google images). Bone structure Compact bone There are primarily three types of bone, namely: Compact bone is the outer structure and provides woven, compact and cancellous (Figure 7.2). mechanical strength, while cancellous bone forms the inner structure and its function is the metabolic Woven bone unit of the bone (Figure 7.3). Compact bone is dense bone and surrounds the cancellous bone. Woven bone is normally remodelled and replaced The primary structural unit of compact bone is an with either compact or cancellous bone. Woven bone osteon, which is also known as a Haversian system. is found during embryonic development, during frac- Osteons consist of cylindrical shaped lamellar bone ture healing (callus formation), and in some patho- that surrounds longitudinally oriented vascular logical states, such as hyperparathyroidism and Pad- channels called Haverisan canals; horizontally get Disease (Recker et al. 1992).

BONE FORMATION AND GROWTH 107 Spongy of a joint where articular cartilage is present. It con- Bone sists of dense irregular connective tissue. The pe- riosteum is divided into a fibrous layer (outer) and Yellow an oseogenic layer (inner). The fibrous layer con- Marrow tains fibroblasts, while the oseogenic layer contains progenitor cells that develop into osteoblasts, which Compact are cells that form and repair bones. The perios- Bone teum has nociceptors nerve endings present and is sensitive to injury. It also provides nourishment by Figure 7.2 Illustrate the structure of bone (taken from providing the blood supply. It is attached to bone Google images). by strong collagenous fibres called Sharpey’s fibres, which extend to the outer circumferential and inter- oriented vascular channels, which are known as stitial lamellae. It also provides an attachment for Volkmann canals, connect adjacent osteons. muscles and tendons. Bone, including the marrow, periosteum, metaphysic, diaphysis and epiphysis are richly supplied with blood vessels. Studies by Shim et al. (1967) and Tothill and MacPherson (1986) re- ported that approximately 7% of the cardiac output is sent to the skeleton. Classification of bones Bones are usually classified according to their shape. Table 7.1 summarises the main categories of bones. Cancellous bone Bone formation and growth Cancellous (spongy) bone consists of spicules of Ossification is the name given to the formation bone enclosing cavities containing marrow (blood- of bone. There are three cells involved in bone forming cells). This type of bone is strong but the metabolism: spaces make it light and flexible. Cancellous bone is always covered and therefore protected by compact 1. Osteoblasts (bone forming cells) – mononuclear bone. In long bones, cancellous bone is found in the cells of mesenchymal origin. epiphysis (at the end of the long bone); in some it also extends down inside into the shaft. In all other 2. Osteoclasts (bone eating cells). bones, it forms the central mass of bone within a compact bone lining. 3. Osteocytes (cells of the matrix) – found in mature adult bone. In adults, 80% of the skeleton is compact bone. However, the relative proportions of compact and Signalling pathways between these cells help regu- cancellous bone vary in different parts of the skele- late the balance between bone formation and bone ton. For example, in the lumbar spine, cancellous reabsorption. bone accounts for about 70% of the total bone tissue, whereas in the femoral neck and radial diaphysis, it Osteoblasts are the bone-forming cells and they accounts for about 50% and 5%, respectively (Kanis originate from local mesenchymal stem cells (bone 1994; Einhorn 1996; Fleisch 1997). marrow stroma or connective tissue mesenchyme). These stem cells undergo proliferation and differen- Bone covering tiate to preosteoblasts and then to mature osteoblasts (Triffitt 1996). The plasma membrane of osteoblasts The periosteum is a membrane that lines the outer is rich in alkaline phosphatase, which enters the sys- surface of all bones, (Netter 1987) except in the area temic circulation. The plasma concentration of this

108 PATHOPHYSIOLOGY OF SKELETAL INJURIES Proximal Endosteum epiphysis Epiphysis line Compact bone Spongy bone Yellow (containing marrow red marrow) Periosteum Diaphysis Nutrient artery Compact bone Distal Medullary epiphysis cavity Periosteum Spongy bone Epiphysis line Figure 7.3 Structure of bone. enzyme is used as a biochemical marker of bone for- 1996). The mechanism of bone resorption involves mation. Osteocytes originate from osteoblasts em- the secretion of hydrogen ions and proteolytic bedded in the organic bone matrix, which subse- enzymes into the sub-osteoclastic resorbing com- quently become mineralised. They have numerous partment. The hydrogen ions dissolve the bone cell processes forming a network of thin canaliculi minerals, thereby exposing the organic matrix to the that connects them with active osteoblasts and flat proteolytic enzymes (Baron 1996; Teitelbaum et al., lining cells. Osteocytes probably play a role in the 1996). These enzymes, which include collagenases homeostasis of this extracellular fluid and in the lo- and cathepsins, are responsible for the breakdown cal activation of bone formation and/or resorption in of the organic matrix. response to mechanical loads (Nijweide et al. 1996). Bone metabolism is under constant regulation by Osteoclasts are giant cells containing 4–20 nuclei a host of hormonal and local factors. Three of the cal- that reabsorb bone. Osteoclastic reabsorption takes citropic hormones that most effect bone metabolism place at the cell/bone interface in a sealed-off are parathyroid hormone, vitamin D and calcitonin microenvironment (Baron 1996; Teitelbaum et al., (Table 7.2).

CARTILAGE 109 Table 7.1 Categorisation of bones Type of bone Function Long bones This type of bone functions as a lever Flat bones They have greater length than width and consist of a shaft and a variable number of endings Sesamoid bones Irregular bones (extremities) Short bones They are usually somewhat curved for strength Examples include femur, tibia, fibula, humerus, ulna and radius This type of bone has a broad surface for muscle attachment and is used for the protection of underlying organs Examples include cranial bones (protecting the brain), the sternum and ribs (protecting the organs in the thorax), and the scapulae. This type of bone develops in some tendons in locations where there is considerable friction, tension and physical stress. However their presence and quantity varies considerably from person to person Examples include patellae and under 1st metatarsal This type of bone has complicated shapes and so cannot be classified into any of the above (shape-based) categories. Their shapes are due to the functions they fulfil within the body e.g. providing major mechanical support for the body yet also protecting the spinal cord (in the case of the vertebrae) Examples include the vertebrae and some facial bones These types of bone are roughly cube-shaped and have approximately equal length and width Examples include ankle and wrist bones Cartilage These different forms of cartilage are distin- guished by their structure, elasticity, and strength. Cartilage is a non-vascular connective tissue that is divided, according to its minute structure, into: In general, cartilage is a tough, fibrous and blood vessel-free connective tissue that forms flexible link- r hyaline cartilage (articular) – covers joint surfaces ages, supporting structures and acts as a shock ab- r fibrocartilage – knee meniscus, vertebral discs sorber in joints such as the knee. r elastic cartilage – outer ear Hyaline (articular) cartilage is the most common type of cartilage. In addition to being found in artic- ulated joints, hyaline cartilage forms the majority of the skeleton of a fetus. Later in fetal development, Table 7.2 Hormones that most effect bone metabolism Hormone Description Parathyroid hormone Produced via the parathyroid glands, which are small endocrine glands in the neck Humans have four parathyroid glands, which are usually located behind the thyroid gland Vitamin D Increases the flow of calcium into the calcium pool Calcitonin Maintains body’s extracellular calcium pool level at a relatively constant level Osteoblasts are the only cells that have parathyroid hormone receptors Parathyroid hormone has antagonistic effects to those of calcitonin. Fat soluble molecule Stimulates intestinal and renal calcium binding proteins and facilitates active calcium transport Inhibits parathyroid hormone secretion Serves to inhibit calcium dependent cellular metabolic activity

110 PATHOPHYSIOLOGY OF SKELETAL INJURIES it is replaced by bone. The free surfaces of most hya- storage. Therefore, injuries to bone can compromise line cartilage (except that found in joints) are covered any of these functions and interrupt daily functions. by a layer of fibrous connective tissue known as peri- chondrium. The perichondrium is rich in a type of Bone fractures cell known as the fibroblast. Compositionally, hya- line cartilage is made of water (75% by weight), Fractures are potentially serious injuries, damaging collagen (10% by weight, mainly collagen type II), not only the bone but also the soft tissue in the sur- with the remainder being non-fibrous material, such rounding area (diagram of types of fractures are illus- as chondroitin sulphate and keratan sulphate. The trated in Figure 7.4) (Table 7.3). Although the bone collagen provides strength and makes hyaline car- tissue itself contains no nociceptors, bone fracture tilage resistant to compression. Also, the collagen can be very painful, due to (1) the breaking in the provides a means by which the cartilage can be an- continuity of the periosteum; (2) oedema of nearby chored to bone. soft tissues, caused by bleeding of torn periosteal blood vessels, evoking pressure pain; and (3) spasms Cartilage is a metabolically active tissue that under in muscles trying to hold bone fragments in place. normal conditions is maintained in a relatively slow state of turnover by a sparse population of chondro- The severity of a fracture depends on its location cytes distributed throughout the tissue (Naujok et al. and the damage done to the bone and tissue near 2008). it. Serious fractures can have dangerous complica- tions if not treated promptly; possible complications Common cartilage injuries include damage to blood vessels or nerves and in- fection of the bone (osteomyelitis) or surrounding It is well known that lesions which are confined to the tissue. hyaline cartilage alone have little or no capacity to heal (Naujoks et al. 2008). In general, the individual Clinical features of a fracture becomes symptomatic and a significant progression to osteoarthritis is possible (Lohmander 2003). The features of a fracture are many and varied, de- pending on the cause and nature of the injury. The Osteoarthritis (OA) is the most common form of clinical features are listed below: arthritis, which is a leading cause of physical disabil- ity, increased healthcare usage and impaired quality r pain of life (Felson 1990; Guccione et al. 1994). The term OA also applies particularly to the degeneration and r deformity excessive wear of cartilage. This condition develops and progresses with an increase in age. Epidemio- r oedema logical studies have demonstrated that participation in certain competitive sports increase the risk for r muscle spasm OA (Kujala et al. 1994; Buckwalter and Lane 1997). Moderate regular running has low, if any risk leading r abnormal movements to OA (Lane et al. 1993; Newton et al. 1997). Sport activities that appear to increase the risk for OA in- r loss of function clude those that demand high-intensity, acute, direct joint impact as a result of contact with other partic- r shock ipants, playing surfaces or equipment (Buckwalter and Lane 1997). r limitation of joint movement. Common skeletal injuries and Stress fractures their manifestation Stress related bone injuries have become common- As previously stated bone provides structural support place amongst the members of our increasingly ac- and protection, facilitating movement and mineral tive society and account for up to 10% of cases in a typical sport medicine practice (Jones et al. 1989)

COMMON SKELETAL INJURIES AND THEIR MANIFESTATION 111 Table 7.3 Types of bone fracture Type of fracture Description of fracture Compound (open) Occurs when the sharp ends of the broken bone protrude through the individual’s skin Closed Skin remains intact Depressed or fissured Occurs when a sharp localised blow depresses a segment of cortical bone below the level of Greenstick surrounding bone – example – fractured skull Seen in children – fracture is on one side of the bone but does not tear the periosteum of the Spiral Oblique opposite side Transverse This is caused by opposite rotator forces pulling on the bone Avulsion The fracture is oriented at an angle of ≥30 degrees to the axis of the bone The fracture is oriented at a right angle to the axis of the bone Comminuted The fracture is caused by a sudden muscle contraction, with the muscle pulling off the Stress portion of the bone The fracture involves multiple fracture fragments The fracture results from stresses repeated with excessive frequency to the bone Stress fractures occur in normal and abnormal Insufficiency fracture results from normal stress bones that have been subjected to repeated traumas applied to abnormal bone (Pentecost et al. 1964) (Figure 7.5). Other terms used to describe this injury that is weakened by an underlying disorder such as include crack fracture, pseudofracture, spontaneous osteoporosis, rheumatoid arthritis, osteomalacia or fracture and exhaustion fracture (Belkin 1980; Jones Paget’s disease (Stafford et al. 1986) et al. 1989). These fractures occur in weight-bearing and non-weight bearing bones. There are two gen- Fatigue fractures occur when normal bones are eral types of stress fractures, insufficiency fracture subjected to increased loads and repetitive stresses. and a fatigue fracture. None of these stresses is individually capable of pro- ducing a fracture, but combined they will lead to Greenstick Spiral Comminuted Transverse Compound Vertebral Compression Typical Bone Fractures Figure 7.4 Diagram illustrating common fractures.

112 PATHOPHYSIOLOGY OF SKELETAL INJURIES r Muscle fatigue ◦ Muscles provide shock absorption by taking the force away from the bone, thereby protecting it from fracture. As the muscle fatigues the stress is then transferred to the bone. Running is responsible for the greatest number of stress fractures (fatigue fractures). This occurs espe- cially when an individual: r demonstrates a poor training technique (changing intensity or duration) r anatomic and biomechanical factors, such as leg length discrepancy, external rotation of the hip, excessive pronation (Sullivan et al. 1984; Giladi et al., 1991) r poor footwear Figure 7.5 X ray of a stress fracture. Osteoporosis mechanical failure over time (Belkin 1980). It is not Osteopenia is not an injury but if left untreated can known or clear whether compressive, gravitational lead to the development of osteoporosis. Osteopenia or muscular forces are most responsible for fatigue is when the Bone mineral density (BMD) is lower fractures. Several mechanisms have been proposed: than normal but not low enough to be classed as osteoporosis. r Weight bearing Osteoporosis is an established and well-defined ◦ Weight bearing plays a role in some stress frac- disease that affects more than 75 million people tures. in Europe, Japan and the USA, and causes more than 2.3 million fractures annually in Europe and ◦ It is unlikely this mechanism is solely respon- the USA alone (WHO 2000). It is a systemic skele- sible for the development of a stress fracture. tal disease characterised by low bone density and This is supported by the fact that stress fractures micro-architectural deterioration of bone tissue with occur in both weight-bearing and non-weight a consequent increase in bone fragility (WHO 2000). bearing bones. Early osteoporosis is not usually diagnosed and re- mains asymptomatic; it does not become clinically r Muscle actions evident until fractures occur. Loss of bone density occurs with advancing age and rates of fracture in- ◦ Muscles may provide enough repetitive force to crease markedly with age, giving rise to significant create a stress fracture. This is a likely mecha- morbidity and some mortality (WHO 1994). nism for upper limb stress fractures. Osteoporosis is three times more common in ◦ With training muscle strengthens quicker than women than in men, partly because women have bone causing a mis-match that may lead to os- a lower peak bone mass and partly because of the seous fatigue failure (Daffner 1978) hormonal changes that occur at the menopause. Just after menopause the rate of bone mass loss in fe- males is up to 10 times faster than in men of the same age (Reginster et al. 2006). Oestrogens have an important function in pre- serving bone mass during adulthood, and bone loss

OSTEOPOROSIS 113 occurs as levels decline, usually from about the age (Gibson et al. 1999). However the effectiveness of of 50 years. Also women live longer than men (the a reduced training load (Warren et al. 2003) and 1994 revision of the United Nations (1995) global improved nutrition on the resumption of regular population estimates and projections) and therefore menses, and the consequent increase in BMD, sug- have greater reductions in bone mass. gests that energy balance is also implicated in the relationship between compromised bone health and According to the WHO diagnostic criteria, women menstrual dysfunction (Micklesfield et al. 2007). with bone density levels more than 2.5 standard de- Extensive reports confirm that female athletes who viations below the young adult reference mean are present with menstrual dysfunction have a lower considered to have osteoporosis (Kanis et al. 1994). BMD than amenorrhoeic athletes (Marcus et al. Individuals with bone density below this threshold 1985). Traditionally it has been accepted that the who also sustain a fracture meet the definition of reason for the decrease in BMD that accompanies “established or severe osteoporosis”. Among British menstrual dysfunction is chronic hypo-oestrogenism women aged 50–59 years, for example, the preva- (Micklesfield et al. 2007). However, the use of oral lence of osteoporosis (as defined by a WHO Study contraceptives and the restoration of regular menses Group) at the femoral neck of the hip is 4% and in these athletes have not been successful in revers- at any site is 15%. These figures rise to 48% and ing this bone loss (Mazess et al. 1991; Keen 1997; 70%, respectively, in women aged 80 years and over Micklesfield et al. 1998). Another mechanism may (WHO 2000) be responsible for the bone loss seen in athletes with menstrual dysfunction. This is confirmed by One mode of athletic activity, gymnastic training, Micklesfield et al. (2007) in a study that showed a invokes high impact loading strains on bone, which relationship between the occurrence of bone stress many have powerful osteogenic effects (Taaffe et al. injuries and disordered eating patterns, as well as a 1997). It has been reported that regional and to- high training load, this mechanism maybe more re- tal body density in competitive collegiate gym- lated to energy balance than to hypo-oestrogenism. nasts exceeds that of runners, swimmers and non- athletic women regardless of menstrual cycle status The osteoporosis risk factors are summarised (Myburgh et al. 1993). below: The Female Athlete r female sex The female triad is defined as a serious syndrome r premature menopause (Micklesfiled et al. 2007) consisting of three inter- related components: r age 1. disordered eating r primary or secondary amenorrhoea 2. amenorrhea r slight body build 3. osteoporosis. r primary and secondary hypogonadism in men The athletes most at risk are those participating in r Asian or Caucasian race sports in which success is determined by thinness and aesthetics (Micklesfiled et al. 2007). The link r previous fragility fracture between current and past menstrual dysfunction and potential deleterious effects on bone mineral density r glucocorticoid therapy has been thoroughly investigated in female athletes (Drinkwater et al. 1984; Marcus et al. 1985; Mick- r maternal history of hip fracture lesfiled et al. 1998; Miller et al. 2006) r low body weight Results of treatments for reversing bone loss in athletes with menstrual dysfunction, such as hor- mone replacement, have shown equivocal outcomes

114 PATHOPHYSIOLOGY OF SKELETAL INJURIES Fracture Healing Process Week 1 Weeks 2-3 Hematoma (or Inflammation) Soft Callus Weeks 4-16 Weeks 17 & Beyond Hard Callus Remodeling Figure 7.6 Fracture healing process. r cigarette smoking riencing growth, mechanical stress, microfractures r excessive alcohol consumption or breaks. About 20% of all bone tissue is replaced r prolonged immobilisation annually by the remodelling process. The total pro- r vitamin D deficiency cess takes about 4–8 months, and occurs continually r low dietary calcium intake. throughout our lives. The healing potential of bone is influenced by a variety of biochemical, biomechani- Healing re-modelling process during cal, cellular, hormonal and pathological mechanisms injury/rehabilitation (Kalfas 2001). Healthy bone remodelling occurs at many simulta- The first stage of bone healing is referred to as neous sites throughout the body where bone is expe- the inflammatory phase (also known as the granula- tion stage, fracture stage or clot phase). This stage has two parts to it: during the first part of this stage the surviving cells are sensitised to chemical mes- sengers that are involved in the healing process, this stage is completed within seven days. The sec- ond part, which lasts for about two weeks, is the

HEALING RE-MODELLING PROCESS DURING INJURY/REHABILITATION 115 development of a clot around the fracture site; this is arin, glucocorticoids) can affect calcium activity. Vi- not seen within stress fractures. After the clot has tamin D regulates calcium absorption and excretion, been formed, granulation tissue forms within the especially when calcium intake is low. space between the fracture fragments. This granu- lation tissue then activates macrophages. When calcium levels in the blood drop, parathy- roid hormone (PTH) is released. PTH causes calcium The second stage is known as the reparative phase to be released from the bones; this then raises the (callous stage), and can be divided into the soft cal- low calcium levels in the blood. Osteoporosis may lous and hard callous stages. During the soft callous result from chronically high levels of PTH (Groff stage the osteoblasts and chondrocytes within the and Gropper 2000). granulation tissue begins to make cartilage and wo- ven bone matrices. This newly formed callus begins Wolff's law and the effect it has on to mineralise after approximately a week. This min- bone healing eralisation concludes with the formation of a frac- ture/hard callus, this callus is detectable on X-rays When mechanical stresses are put on bone, the bone due to the calcium it contains. The creation and min- has the ability to adapt by changing size, shape and eralisation of the callus can take 4–16 weeks to com- structure. When optimal stress is placed on bone plete. there is a greater bone deposition than bone resorp- tion. This results in an increased bone density and a The third stage is called the remodelling phase hypertrophy of perosteal bone. (consolidation phase), In the remodelling phase the process may occur over months to years and consists Effect of NSAID's on fracture healing of restoring the fractured bone to its normal size, shape and strength (Kalfas 2001). Adequate strength Bone repair is a complex process initiated by injury usually develops by six months. and an inflammatory response. Prostaglandins me- diate inflammation, influence the balance of bone Effects on the bone healing process formation and resorption; processes that are essen- tial for new bone formation. NSAIDs inhibit cyclo- Nutrition oxygenases, which are essential for prostaglandin production (Dumont et al. 2000). It has been shown Calcium is far the most abundant mineral found that long-term excessive use of these medications within the body and contributes to the structure of may reduce normal bone healing (Placzek and Boyce teeth and bone (Thatcher et al. 2009) Calcium plays 2006). an important role in helping attain peak bone mass during bone development and preventing fractures in Conditions that have a negative effect later life. The daily recommended allowance of cal- cium intake is 800–1200 mg (Thatcher et al. 2009). The following list gives a range of conditions that Multiple factors can affect the bioactivity of calcium: have a negative effect on the bone healing process: r high-fat or high fibre diets can interfere with or r infection decrease the activity of calcium r poor reduction (poor realignment of fracture) r large doses of zinc supplementation or mega doses r loss of local blood supply due to injury of vitamin A can lower calcium bioactivity r vascular injury r high protein diets can decrease calcium reserves r failure to make callus (metabolic abnormalities) by increasing urinary excretion of calcium r formation of scar and fat tissue instead of callus (Placzek and Boyce 2006) In addition, alcohol consumption can decrease the absorption of calcium and various medications (hep-

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8 Peripheral nerve injuries Elizabeth Fowler University of Salford, Greater Manchester Introduction fibres and groups of non-mylenated fibres are surrounded by three connective tissue layers; the This chapter aims to introduce the structure and endoneurium, the perineurium and the epineurium function of nerves and the neurological system, and (Topp and Boyd, 2006; Campbell 2008). the pathophysiology of common nerve injuries. The chapter also reviews some common nerve injuries, The innermost connective tissue layer is the their assessment and evidence based treatment. endoneurium, which is composed of longitudi- nally aligned collagen fibres and therefore, plays Anatomy of nerves an important role in protecting the axon from tensile forces (Butler 1991). Encompassing the The nervous system comprises of the central, endoneurial components, axon and Schwann cells autonomic and peripheral nervous systems (Gallant is the perineurium, the second layer of connective 1998) the latter of which consists of cranial nerves, tissue, whose primary responsibility is to act as a spinal nerves, peripheral nerves and peripheral com- primary barrier to external forces (Lundborg 1988). ponents of the autonomic nervous system (Gardner Collectively, all the contents surrounded by the and Bunge 1984). The neurone is the structural perineurium form what is known as a nerve fascicle unit of the nervous system and is responsible for (Topp and Boyd 2006). Collections of nerve fascicles conducting messages from one part of the body then form a nerve and these are surrounded by the to another (Marieb 1998). The basic unit of the outermost layer of connective tissue, the epineurium neurone is the axon, more commonly known as (Campbell 2008). The epineurium is regarded as the nerve fibre (Butler 1991) (Figure 8.1) and can the most resistant connective layer to tensile forces be either mylenated or non-mylenated. Mylenated (Sunderland 1978) as it surrounds, protects and axons are surrounded by a myelin sheath and have cushions the nerve fascicles (Butler 1991). Col- one Schwann cell per axon. The Schwann cell is fre- lectively all three connective tissue layers not only quently interrupted by nodes of Ranvier; a structure protect the axon, but are also structurally developed that allows impulses to be conducted from one node to cope with the tensile stresses and compressive to the next (Topp and Boyd 2006; Campbell 2008). forces nerves typically have to endure (Butler Non-mylenated fibres however, have several axons 1991). In everyday movements and postures, nerves associated with only one Schwann cell (Topp and are subjected to various mechanical stresses (Topp Boyd 2006; Campbell 2008). Individual mylenated and Boyd 2006), which can elongate, compress or increase strain within the nerve (Shacklock 1995). Sports Rehabilitation and Injury Prevention Edited by Paul Comfort and Earle Abrahamson C 2010 John Wiley & Sons, Ltd

120 PERIPHERAL NERVE INJURIES Dendrite Biological tissues, such as nerves, have an ideal Cell body physical stress range that they can tolerate to main- Axon tain homeostasis. This is called the “maintenance stress range” (Mueller and Maluf 2002). Stress lev- Myelin sheath els lower than the maintenance range decreases a tis- sue’s tolerance to physical stress; for example during Synapse immobilisation of a limb, muscle atrophy is a typical bi-product of being in a cast for a prolonged period Figure 8.1 Structure of nerves. of time. Contrastingly, when physical stresses are ex- ceedingly higher than the homeostatic stress range, The ability of the nervous system to withstand the associated tissues are unable to tolerate these and adapt to the mechanical stresses placed on it, is and any subsequent stresses and ultimately become essential to prevent injury (Shacklock 1995). Alter- injured (Mueller and Maluf 2002). ations in the physical stress to which a biological tis- sue is subjected, causes predictable responses within The mechanical stresses a nerve is subjected to are the tissue according to Mueller and Maluf’s (2002) not the only factor which must be taken into account Physical Stress Theory. Injury to tissues is caused with nerve injury as the nature of the surrounding by excessive physical stress via any of the following structures a nerve traverses or passes through must mechanisms: also be considered (Butler 1991). The nervous system is surrounded by and comes into contact 1. High magnitude stress applied to the tissue for with many different anatomical structures which a brief duration; spinal cord injury is a typical may be firm and unyielding, such as the radial nerve outcome from this mechanism of injury. in the spiral groove of the humerus, or soft, such as the tibial nerve in the posterior thigh musculature 2. Low magnitude stress applied for long duration or (Butler 1991). Additionally, anatomically narrow repetitively; an example of nerve injury from this passages through which the nerve must pass may particular mechanism of injury is Carpal Tunnel also predispose individual nerves to entrapment Syndrome at the wrist. neuropathies, such as the ulnar nerve in the cubital fossa of the elbow (Bencardino and Rosenberg 3. Moderate stress applied to a tissue many times. 2006). The extent of an injury to a nerve is dependant Cubital Tunnel Syndrome at the elbow, for exam- on the mechanism of injury, as traumatic injuries, ple in a javelin thrower, whereby repetitive high such as a gun-shot wound (i.e. high magnitude load forces are exerted through the elbow and con- stress), will significantly damage a nerve’s integrity, sequently the ulnar nerve, is an example (Mueller whilst a low magnitude stress, such as prolonged and Maluf 2002). intermittent compression over a long duration of time, will have less of an impact on the nerve. Nerve injuries were initially classified by Seddon (1943) based on the severity of the injury and the potential for reversibility of the condition (Bencardino and Rosenberg 2006). Classification of nerve injury Neurapraxia, axonotmesis and neurotmesis are the three categories of nerve injuries classified by Seddon (1943) each describing different degrees of injury to the nerve’s anatomical structures (Table 8.1). Neurapraxia is the most benign injury and typically results from compression and/or traction (Perlmutter and Apruzzese 1998; Bencardino and Rosenberg 2006). Pathologically, the nerve is

ASSESSMENT OF NERVE INJURY 121 Table 8.1 Classification and characteristics of nerve injury Classification Anatomical presentation Clinical presentation Prognosis Neuropraxia Segmental demylenation Slight motor loss Excellent Axontmesis Minimal sensory involvement Up to 12 week recovery Neurotmesis Loss of axonal continuity Substantial loss of motor, sensory Good Connective tissue intact Surgery may be required however Complete disruption of nerve and autonomic function Poor Significant muscle fibre atrophy Surgery is a necessity fibre and connective tissues Sensory loss Adapted from Seddon (1943). intact but is temporarily unable to transmit signals (Bencardino and Rosenberg 2006) and therefore (Campbell 2008) due to injury to the myelin about surgical intervention is often required in an attempt the nodes of Ranvier (Bencardino and Rosenberg to re-establish the continuity of the peripheral nerve 2006). Consequently, the clinical presentation is (Perlmutter and Apruzzese 1998). Avulsion of the that of motor loss, with little sensory involvement nerve, via stab wounds or gunshot, is a typical and little disturbance of sympathetic innervation example of neurontmesis; it is a rare occurrence in (Perlmutter and Apruzzese 1998). With remylena- sport. tion of the nerve, motor and sensory dysfunction will gradually be restored, usually within 12 weeks The majority of nerve injuries in sport will typi- (Novak and Mackinnon 2005; Bencardino and cally involve neurapraxia or axontmesis and there- Rosenberg 2006). The prognosis for neuropraxia fore prognosis for recovery is generally good. is excellent (Perlmutter and Apruzzese 1998) and complete recovery is expected (Novak and Assessment of nerve injury Mackinnon 2005). Neural and non-neural tissues should be assessed When there is loss of continuity of the axon and by the clinician in all patients presenting with pain myelin sheath, but the majority of the connective (Nee and Butler 2006) by means of a comprehensive tissue structure is maintained, the injury is classified subjective and physical examination. All the phys- as axonotmesis; the second classification (Seddon ical examination findings should complement and 1943). The endoneurium and Schwann sheath support the information obtained from the patient are preserved, but injury to the axon is evident, via subjective examination (Hall and Elvey 1999). accompanied with secondary Wallerian degenera- Nee and Butler (2006) proposed numerous clinical tion (Bencardino and Rosenberg 2006). A clinical features that may be evident in the subjective and finding of significant loss of motor, sensory and physical assessment of patients presenting with autonomic function distal to the injury site is evident peripheral neuropathic pain, such as complaints (Perlmutter and Apruzzese 1998). Neural regen- of tingling, burning and parasthesia in addition to eration will occur, but at a rate of approximately antalgic postures and movement impairments being 1mm per day and over-all the prognosis for recovery present. Motor or sensory losses, or both, may also is good (Novak and Mackinnon 2005). Stinger Syn- be evident in the assessment of patients presenting drome is also an example of axontmesis, particularly with nerve pain. However, when nerve injury is should the injury recur within a short period of suspected, the assessment of the integrity of the time. nerve is vital. The most severe peripheral nerve injury is referred Evaluation of the function of the muscles inner- to as neurontmesis and involves complete disruption vated by the injured nerve should be assessed via of the nerve trunk and connective tissue (axons, manual resistance testing to determine the motor endoneurial tube, Schwann sheath and epineurium) function of the nerve (Figure 8.2 and Table 8.2). (Campbell 2008). The prognosis for recovery is Likewise, the areas of innervation should be as- poor as there is no potential for nerve regeneration sessed via touch to assess the sensory function of the

122 PERIPHERAL NERVE INJURIES MYOTOMES Table 8.2 Myotomes of the upper and lower limb Myotomes of the Upper limb C5 C8 T1-12 Nerve root/nerve Cervical flexion T1-12 C7 C1 Cervical flexion C2 Cervical lateral flexion C3,4,5 C6 C3 Shoulder elevation S3,4,5 C4 Shoulder abduction C5 Elbow flexion L2 L2 T1 C6 Elbow extension C7 Thumb extension C8 Finger abduction T1 Myotomes of the Lower limb L3 Nerve root/nerve L1 L4 L2 Hip flexion S1 L3 Hip adduction L4 Knee extension L5 L5 Ankle dorsi-flexion S1 Great toe extension Figure 8.2 Myotomes. S2 Ankle plantar flexion Knee flexion injured nerve (Dahlin 2008) (Figure 8.3). Knowl- edge of the myotomes and dermatomes of the upper structure in the area in question, without moving the and lower extremities is important to conduct a thor- musculoskeletal tissues in the same region; a task ough assessment of the peripheral nervous system. attempted by structural differentiation during neuro- Nee and Butler (2006) also recommend incorporat- dynamic tests (Shacklock 1995). The concept behind ing neurodynamic tests into the physical assessment structural differentiation is to move a joint remote to to determine the mechanosensitivity of the nervous the area where the patient experiences symptoms; system. should this decrease or increase symptoms, neural involvement into patient symptoms should be sus- Neurodynamic testing pected. For example, in a patient presenting with posterior thigh pain, moving the head from cervi- Nerves slide and stretch during limb movements to cal flexion to extension during the slump test should allow for changes in nerve bed length (Babbage et al. have no effect on patient symptoms if the pain is of 2007) and whilst healthy nerves can tolerate strain a non-neural origin. However, should the clinician and compression, injured or inflamed nerves become suspect the sciatic nerve is a contributing factor to sensitive to mechanical stimuli and can inflict pain patient symptoms, moving the cervical spine from on movement (Bove et al. 2005). flexion to extension should decrease the pain and/or permit a further range of movement at the knee Neurodynamic tests were developed to evaluate joint. peripheral nerve sensitivity to movement and to infer underlying pathomechanics (Topp and Boyd 2006). Neurodynamic tests for the upper and lower ex- To determine if neural tissues contribute to the pa- tremities have been developed; each one intent on tient’s symptoms, it is important to move the neural identifying whether a specific nerve is contributing to the symptomatic patient. The termination of the movement during a neurodynamic test is dependant on whether the clinician wants to stop at the point

ASSESSMENT OF NERVE INJURY 123 Figure 8.3 Dermatomes. where resistance is experienced by the clinician Upper limb neurodynamic test with median (Shacklock 1995; Nee and Butler 2006) or to the nerve bias point where the patient reports onset of pain or sub- maximal pain (Coppieters et al. 2002). Three tests for In patients presenting with suspected median nerve the upper limb are described below, each focused on pathology whereby symptoms may be localised to examining the integrity of the three primary nerves the median nerve, such as carpal tunnel syndrome or in the upper extremity; the median, radial and ul- pronator tunnel syndrome, incorporating a neurody- nar nerves. For the lower limb, the slump test and namic test into the physical examination is essential straight leg raise tests will be illustrated. In-depth to determine if the nerve contributes to patient symp- and more detailed clinical neurodynamic tests have toms. To conduct this test, the patient lies supine on been presented by Shacklock (2005). the plinth with arms relaxed by the side of the body.

124 PERIPHERAL NERVE INJURIES Keeping the head in a neutral position, the clinician Figure 8.5 Upper limb neurodynamic test with radial places a hand over the superior aspect of the shoul- nerve bias. der with the aim of depressing the shoulder as the test commences. The clinician then holds the pa- at 90◦ and the wrist and fingers in neutral. The clini- tient’s ipsilateral hand and places the glenohumeral cian then applies shoulder depression before moving joint in 90◦ abduction and 90◦ lateral rotation, the the elbow into extension and the wrist and fingers forearm in full supination and the wrist in exten- into flexion whilst internally rotating the gleno- sion. The clinician then supports the patient’s arm humeral joint. Finally, glenohumeral abduction is ap- on their thigh with the aim of preventing adduction plied and again the clinician ceases the movement at of the shoulder during the test. Once in this posi- the point of resistance or pain (Figure 8.5). To struc- tion, the clinician slowly extends the elbow to either turally differentiate, shoulder depression can be re- onset of resistance or pain (Figure 8.4). To struc- moved for distal symptoms, whilst moving the wrist turally differentiate, the clinician can either ask the from flexion to neutral may identify proximal lesions patient to execute contralateral side flexion of the (Shacklock 2005). head for distal symptoms or the wrist can be moved from extension into flexion for proximal symptoms Upper limb neurodynamic test with ulnar (Shacklock 2005). nerve bias Upper limb neurodynamic test with radial When symptoms are evident in the anatomical nerve bias pathway of the ulnar nerve or the lower trunk of In patients presenting with radial neuropathy such as the brachial nerve (Shacklock 2005), neurodynamic radial tunnel syndrome, the clinician requires a phys- testing specific to this nerve is important. The testing ical test which can be conducted to determine the sequence for an upper limb neurodynamic test with sensitivity of the nerve to stretch. To do this, a clinical ulnar nerve bias requires the patient to lie supine on test was developed to focus specifically on the radial the plinth, with the head in a neutral position and the nerve and is conducted as follows: the patient lies arms relaxed by the side of the body. The clinician supine with arms resting by the side of the body but in prepares for depression of the shoulder as for the a diagonal direction across the plinth. This allows the median nerve test. The patient’s shoulder joint is clinician to apply shoulder depression using the ante- abducted slightly whilst the elbow is maintained in rior aspect of their hip whilst conducting the test. The extension and the forearm slightly pronated. The patient’s starting position involves placing the elbow wrist and hand of the patient remains in a neutral position, following which, the clinician then com- Figure 8.4 Upper limb neurodynamic test with median mences the test by depressing the shoulder before nerve bias. applying extension to the wrist and fingers and pronation to the forearm. The elbow is then brought

ASSESSMENT OF NERVE INJURY 125 Figure 8.6 Upper limb neurodynamic test with ulnar Figure 8.7 Lower limb neurodynamic test: The slump nerve bias. test. into a flexed position; following which, the shoulder which the clinician applies dorsi-flexion to the ankle is gradually moved into an abducted position (Figure before slowly extending the knee to the point of 8.6). The clinician again uses a leg to support the resistance or pain. To structurally differentiate, the moving limb; thereby making the movement more release of cervical flexion and ankle dorsi-flexion fluid. Again once resistance or pain is experienced are used for distal and proximal lesions respectively. by the clinician or patient respectively, shoulder abduction ceases and the structural differentiation Lower limb neurodynamic test: the straight manoeuvre is applied; either contralateral cervical leg raise side flexion for distal symptoms or radial deviation for proximal symptoms (Shacklock 2005). The straight leg raise (SLR) is a similar neurody- namic test to the slump test, intent in evaluating Lower limb neurodynamic test: The the integrity of the lumbosacral trunk and plexus, slump test sciatic nerve and its expansion in the leg and foot (Shacklock 2005). The format for the SLR is as fol- The slump test is used to evaluate the dynamics of lows: the patient lies supine on the plinth with arms the central and peripheral nervous systems from the resting by the side of the body. The clinician uses one head, along the spinal cord and sciatic nerve tract hand to support the posterior calf, just proximal to and its extensions in the foot (Shacklock 2005). The the ankle joint; whilst the other hand is placed on the slump test should be a component of the clinical anterior aspect of the knee joint to ensure knee ex- examination in patients who present with spinal tension is maintained throughout. Maintaining this symptoms (Butler 1991) and/or spinal, pelvic and position, the clinician then begins to lift the leg off lower limb conditions whereby pain is experienced the bed, thereby conducting hip flexion, moving to in the neural distribution of the sciatic nerve and the point of resistance or patient pain. Following its extensions (Butler 1991; Shacklock 2005). To this the clinician then applies dorsi-flexion to the conduct the slump test, the patient is requested to ankle by way of structurally differentiating (Figure side on the plinth with the back of the knees to the 8.8). An increase in symptoms at this point indicates edge of the plinth and to “sag” the upper body, or a neural involvement in the patient’s condition. To bring their shoulder towards their hips, thereby re- ascertain whether the peroneal division of the sciatic sulting in thoracic flexion. The clinician then applies nerve is sensitive to stretch, whilst conducting the overpressure at C7 spinous process with the medial SLR, the clinician can plantar-flex and invert the an- aspect of the forearm (Figure 8.7). The patient is kle whilst moving the ankle into dorsi-flexion and ev- instructed to bring their chin to chest, following ersion emphasises the tibial nerve (Shacklock 2005).

126 PERIPHERAL NERVE INJURIES Figure 8.8 Lower limb neurodynamic test: the straight Figure 8.9 Sliding technique. leg raise. Neurodynamic tests as treatment tools counterbalance the elongation. For example, during the neurodynamic test with median nerve bias, in- A positive neurodynamic test is constituted by a stead of having the patient placed in the final testing reproduction or increase in symptoms during the position, with contralateral side flexion of the cer- test, which is subsequently decreased with the re- vical spine, the patient would move the elbow into moval of the structural differentiating manoeuvre extension whilst simultaneously moving the cervical (Maitland 1985); difference in responses between spine into ipsilateral side flexion (Figure 8.9). The limbs (Nee and Butler 2006); differences in avail- opposing technique is the “tensioning” technique, able range of motion (Coppieters et al. 2002; Nee which the same authors define as the elongation of and Butler 2006); or where there is structural dif- the nerve bed at two adjacent joints (Coppieters et al. ferentiation supporting a neurogenic source (Butler 2009) and again, referring back to the median nerve 2000). Whilst all the aforementioned tests have been test, would involve the patient actively extending the described from a diagnostic point of view, each of elbow whilst simultaneously side flexing the cervical these can be modified and incorporated into treat- spine into the contralateral direction (Figure 8.10). ment plans, should their inclusion as a treatment modality be warranted. Modified versions of the neu- Figure 8.10 Tensioning technique. rodynamic tests can be used in clinical practice in the treatment plan for peripheral nerve injuries and can be specific to each patient. The purpose of utilising neurodynamic tests as treatment tools is to minimise scarring and stretching of the nerve, and maintain or restore normal nerve excursion and function (Wehbe´ and Schlegel 2004). Two neural treatment techniques will be con- sidered in this chapter; sliding and tensioning techniques, the principle of which can be applied to any neurodynamic test and considered for use in the treatment plan for neuropathy patients. A “sliding” technique was defined by Coppieters et al. (2009), as a combination of movements that elongate the nerve bed at one joint, whilst simultaneously reducing nerve bed length at an adjacent joint, to

TREATMENT PLANS FOR NERVE INJURY 127 The sliding technique causes more longitudinal inflammation and restore nerve function. Brief excursion of a nerve than the tensioning technique treatment options will be provided in this section, (Coppieters et al. 2009), and therefore, from following the discussion of each specific injury. a clinical viewpoint, may be more suitable for highly irritable or acute neural conditions as it still Peripheral nerve injury encourages movement of the inflamed nerve, whilst limiting the strain placed on the nerve. A tensioning Neurological conditions are common in athletes technique, however, is proposed to induce higher (Dimberg and Burns 2005) often dependant on the tension within the nerve and therefore less excursion nature and intensity of the sporting activity (Toth (Coppieters et al. 2009) than a sliding technique 2009). A clinician may be confronted with signs and and can therefore be considered more aggressive symptoms of neurological injuries affecting various and possibly suitable for less irritable conditions. aspects of the nervous system, such as spinal nerve The clinician should therefore consider the imple- roots, peripheral nerve injuries or plexopathies. Pos- mentation of sliding or tensioning techniques into a sessing the ability to recognise and diagnose injuries treatment plan for the patient presenting with neural specific to sporting activities and then subsequently symptoms, with the former to be used in acute, to treat the injury, is vital to a clinician in sport (Toth irritable conditions and the latter technique for use 2009) to ensure a rapid return to play for the athlete. in the end stage of rehabilitation. The upper extremity is particularly vulnerable to Ultimately, neurodynamic tests can be modified nerve injury (Dahlin 2008) due to its high mobility and used in the treatment plan for the neuropathic pa- (Aldridge et al. 2001) and it is therefore unsurpris- tient and can also be incorporated into a home exer- ing that the brachial plexus is the most commonly cise programme (Kostopoulos 2004). Typical patient injured plexus in the body (Wilbourn 2007). The responses to neurodynamic tests as both a diagnos- brachial plexus is formed by the ventral rami of the tic and treatment tool, of which the patient should be spinal nerves C5 to T1, which enter the posterior aware, range from reporting feelings of “stretching”, cervical triangle between the scalene anterior and tissue tension, light numbness or a slight increase medius muscles (Pratt 2005). Superior, middle and of pain during the technique; all which should re- inferior nerve trunks of the brachial plexus are then duce or dissipate on cessation of the test or treatment formed by the C5–C6, C7 and C8–T1 nerve roots re- (Kostopoulos 2004). spectively (Reid and Trent 2002; Pratt, 2005). These trunks divide into anterior and posterior portions be- Treatment plans for nerve injury hind the clavicle whereby these divisions then unite to form lateral, medial and posterior cords which en- Immediately post-injury, inflammation occurs, ter the axilla (Reid and Trent 2002). The end result thereby rendering injured tissues less capable of of the brachial plexus is the formation of periph- tolerating stress compared to their pre-morbid level eral nerves which supply the upper limb (Pratt 2005) (Mueller and Maluf 2002). Nerve fibres become (Figure 8.11). The primary peripheral nerves which sensitive to stretch and low intensity pressure are subsequently discussed in this chapter are the following injury (Dilley et al. 2005). Therefore axillary nerve, long thoracic nerve, suprascapular the importance of protecting the tissues during this nerve, ulnar nerve, median nerve and radial nerve; acute inflammation stage from subsequent stress the anatomical locations of which can be viewed in cannot be underestimated (Mueller and Maluf 2002). Figure 8.12. Conservative treatment is the initial recommended strategy in numerous neuropathies not requiring Brachial plexus neuropathy urgent medical attention. Within this category of treatment, several authors suggest incorporating Stinger Syndrome non-steroidal anti-inflammatory drugs (NSAIDs), ice, rest, elimination of the aggravating activity, One of the most common brachial plexus neuropa- physical and manual therapy into the conservative thy is Stinger Syndrome (Hershman 1990), which treatment plan (McKean 2009; Shapiro and Preston is more common in young adults who participate in 2009); the primary aim of which is to decrease sport (Unlu et al. 2007) and particularly in contact

128 PERIPHERAL NERVE INJURIES sports (Wilbourn 2007). The superior trunk of the Brachial plexus brachial plexus (C5 and C6) is thought to be the structure injured in this syndrome (Aldridge et al. ADAM. 2001; Dimberg and Burns 2005; Wilbourn 2007). Tensile overload is one mechanism of injury for the Figure 8.11 The brachial plexus and its pathways. brachial plexus (Hershman 1990), whereby the head and shoulder of the symptomatic side have been forced in opposite directions to each other (Weinstein 1998; Dimberg and Burns 2005) thereby causing stretch and traction of the nerve. Alternatively, another mechanism of injury in Stinger Syndrome is where a compressive force forces the head and neck into the posterolateral corner, causing nerve root compression and thereby injuring the nerve (Weinstein 1998). Finally, injury to the brachial plexus can occur as the result of a direct blow to Snapped with HyperSnap-DX Brachial Plexus http://www.hyperionics.com Schema To longus colli and scalene muscles (C5, 6 Contribution from C4 Dorsal scapular nerve (C5) To phrenic nerve Dorsal ramus To subclavius muscle (C5, 6) C5 ventral Middle trunk ramus Superior trunk Suprascapular nerve (C5, 6) Anterior divisions C6 ventral ramus Lateral pectoral nerve (C5, 6, 7) C7 ventral ramus Lateral cord C8 ventral Posterior cord ramus Musculocutaneous T1 ventral nerve (C5, 6, 7) ramus Contribution from T2 1st intercostal nerve Axillary nerve Long thoracic nerve (C5, 6, 7) (C5, 6) Inferior trunk 1st rib Radial nerve (C5, 6, 7, 8, T1) Median nerve (C5, 6, 7, 8, Posterior divisions Ulnar Medial pectoral nerve (C8, T1) nerve (C7, Medial brachial cutaneous nerve Lower subscapular nerve (C5, 6) Medial antebrachial cutaneous nerve (C8, horacodorsal (middle subscapular) nerve (C6, 7, Medial cord Upper subscapular nerve (C5, 6) Figure 8.12 Pathways of the nerves for the upper limb