Physiological changes in the ageing foot

CHAPTER

Physiological changes in the ageing foot

The foot undergoes significant structural and functional changes with advancing age. While many of these changes merely reflect the physiological alterations in tissues elsewhere in the body, some changes are more pronounced than those that occur in other body regions, while others are unique to the highly specialised loadbearing structures of the foot. Indeed, it has been argued that careful assessment of the older foot can provide useful clinical insights into systemic conditions yet to be clearly manifested elsewhere.1 The following chapter reviews the body of literature pertaining to age-related changes of the foot in relation to the integumentary system, the soft tissue structures, the peripheral vascular and sensory systems, the skeletal system and the muscular system, and discusses the functional implications of these changes.

CHAPTER CONTENTS Integumentary system 13 Epidermis and dermis 14 Nails 15 Functional implications 15 Plantar soft tissues 15 Peripheral vascular system 16 Arteries 16 Capillaries 17 Veins 17 Functional implications 17 Peripheral sensory system 17 Functional implications 18 Skeletal system 18 Bone 18 Joints 18 Tendon and ligament 19 Functional implications 20 Muscular system 20 Age-related changes in muscle tissue Ankle muscles 21 Foot muscles 21 Functional implications 22 Summary 22 References 22

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INTEGUMENTARY SYSTEM 20

The integumentary system consists of the skin, nails and subcutaneous tissues. The primary functions of this system are to provide a barrier between the body and its surrounding environment, to provide sensory information and to assist in the regulation of body temperature. Normal ageing is known to affect the structure and function of each of the components of the integumentary system, which often manifest as characteristic changes to the appearance of the foot.2 These changes are summarised in Table 2.1 and are described in more detail in the following section.

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PHYSIOLOGICAL CHANGES IN THE AGEING FOOT

Table 2.1 Summary of major age-related physiological changes to the integumentary system Age-related changes

Implications

Skin ↓ production and turnover of keratinocytes ↓ density of sweat glands ↓ number of Langerhans cells ↓ number of dermal collagen and elastin fibres ↑ thickness and stiffness of dermal collagen fibres ↓ capillary loops in papillary dermis

↑ ↑ ↓ ↑ ↑

Nails ↓ nail growth rate (up to 50% reduction) ↑ nail plate thickness Plantar soft tissues Distortion and rupture of septa ↓ compressibility ↑ stiffness ↑ energy dissipation

EPIDERMIS AND DERMIS The skin of the sole of the foot has several unique features. Most notably, plantar skin is hairless and, although it contains a high density of eccrine sweat glands, it has no sebaceous glands.3 The plantar epidermis is considerably thicker (approximately 1.5 mm thick, compared to 0.1 mm in other regions of the body) and demonstrates a pattern of ridges that assist in generating sufficient friction when standing and walking barefoot. The plantar dermis is approximately 3 mm thick and is penetrated by adipose tissue, which provides resilience to shear stresses.3,4 Plantar skin is also highly adaptable, as evidenced by the considerably thicker epidermis and dermis observed in people who do not wear shoes.5 Because of this adaptability, it is sometimes difficult to delineate age-related changes from the effects of weightbearing activity and footwear. Advancing age is associated with several significant changes to the structure and function of the skin at both the epidermal and dermal levels.2,6–9 The thickness of the epidermis does not change appreciably with age;10 however, the dermal–epidermal junction becomes flattened, which may give the impression of atrophy.11 In the foot, there may be an increase in epidermal thickness due to thickening of the stratum corneum associated with plantar calluses.12 The shape and size of epidermal keratinocytes becomes more variable, and the rate of production and turnover of

dryness of skin → fissuring and hyperkeratosis risk of infection wound healing wound dehiscence bruising

↑ time required to treat nail infections ↑ rate of re-infection ↑ peak pressures under forefoot → metatarsalgia Development of plantar heel pain

keratinocytes may reduce to only 50% of that of a young person.13 Because of this delay in turnover time, the moisture content of keratinocytes is reduced, which, combined with the reduction in sweat gland density,14 contributes to the dry, scaly appearance of elderly skin.7,8 Langerhans cells, which play an important role in the immune function of the epidermis, decrease dramatically with age,15 resulting in a reduced rate of sensitisation to microorganisms.16 In contrast to the epidermis, the dermis undergoes a significant reduction in thickness due to a marked loss of collagen fibres.17 The collagen fibres that remain become thicker and stiffer and undergo a haphazard cross-linking process.7,18 Elastin fibres, which provide the skin with its elasticity, decrease in number and become fragmented.19,20 These processes alter the mechanical properties of the skin, leading to increased fragility and loss of elastic recoil. Dermal macrophages and mast cells, which provide the second line of immune defence after epidermal Langerhans cells, reduce in number with advancing age, lowering the speed and intensity of the inflammatory response to infection.16 Another factor that contributes to the impaired inflammatory response in older people is the agerelated decline in cutaneous microvascular function. Older people exhibit a significant reduction in the number of capillary loops in the papillary dermis, increased porosity of endothelial cells and a thickened

Integumentary system

basement membrane, all of which contribute to a less efficient superficial blood supply.13,21–23 It has been demonstrated that a 70-year-old may have up to 40% less blood supply to the skin than a 20-year-old,24 and these age-related changes appear to be particularly pronounced in the lower limb. One of the most obvious manifestations of this change is a progressive reduction in skin surface temperature extending distally from the groin.25

NAILS Nails are comprised primarily of keratin produced by the nail matrix, with a small contribution from the underlying nail bed.26 Compared to fingernails, toenails are thicker (1.65 versus 0.60 mm) and have a slower linear growth rate (1 mm/month versus 3 mm/month).27,28 With advancing age, the rate of growth of the nails decreases by up to 50%,29,30 because of both a reduction in the turnover rate of keratinocytes and a reduction in size of the nail matrix itself. This process is particularly pronounced in toenails, possibly because of the greater age-related decline in blood supply to the feet compared to the hands.28 In addition to decreased rate of growth, the chemical composition, histology and structure and appearance of the nail plate changes with age. Older nails exhibit an increase in calcium and reduction in iron content, increased size of keratinocytes and degeneration of elastic tissues beneath the nail bed.28 The formation of longitudinal grooves and an overall increase in thickness (onychauxis), often leads to a marked loss of translucency,2,27 while periods of arrested growth due to periods of systemic illness may also manifest as transverse ridges known as Beau’s lines.27 These changes are exacerbated by the presence of arterial insufficiency and low-level chronic trauma from illfitting footwear.27,28

FUNCTIONAL IMPLICATIONS The physiological changes in the integumentary system that occur with ageing have important functional implications. As stated previously, the decreased water content of keratinocytes and decreased density of eccrine glands leads to an overall drying of the skin, which predisposes to the development of hyperkeratosis and fissuring. The reduction in epidermal and dermal immune function increases the risk of infection31 and the reduced rate of epidermal turnover may

increase the time required to successfully treat these infections.2 Wound healing is significantly delayed in older people, because of both a reduction in wound contraction (a direct result of collagen cross-linking and diminished elastin content of the dermis) and a reduced rate of epithelialisation and angiogenesis.32–34 Even if a wound successfully heals, the tensile strength at the wound site is diminished, which increases the likelihood of dehiscence. Subsequently, wounds in older people often require much longer periods of treatment and frequently recur. Bruising is also more likely to occur because of the decreased integrity of superficial blood vessels leading to leakage of red blood cells into the papillary dermis.2 Age-related changes in the structure and function of the nail have important implications for the management of fungal nail infections (onychomycosis), one of the most common foot problems in older people.35 Because of the reduction in nail growth rate and subsequent thickening of the nail plate, treatment of onychomycosis with either oral or topical agents may take considerably longer in older people and the possibility of reinfection is much higher.36

PLANTAR SOFT TISSUES The sole of the foot has highly specialised soft tissue structures in the heel and metatarsal head regions that are designed to absorb impact forces associated with weightbearing activities. Ageing is known to influence both the structure and function of these tissues and, although the literature is inconsistent, there is emerging evidence that these changes may be associated with the development of symptoms.

Metatarsal pads The plantar tissues of the forefoot serve numerous functions, including anchoring the skin to the underlying bony architecture of the foot, protecting underlying flexor tendons, blood vessels and nerves, and attenuating both vertical and shear forces applied during gait.37 The latter function is achieved by specialised pads of fat cells under each metatarsal head confined by retinacula extending from the dermis to the sides of each flexor tendon sheath.4 The metatarsal pads progressively decrease in thickness from the first to fifth metatarsal heads38–40 and undergo compression of 10–15% when standing40 and up to 46% during gait.41

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PHYSIOLOGICAL CHANGES IN THE AGEING FOOT

Although atrophy of metatarsal padding is frequently observed in older people, no studies have confirmed this finding using imaging techniques. Furthermore, no histological studies have been undertaken to ascertain whether ageing is associated with a breakdown of the connective tissues of the plantar forefoot. However, comparisons of the mechanical properties of metatarsal pads in young and older people by Hsu et al42 and Wang et al38 have demonstrated that older pads demonstrate greater stiffness, dissipate more energy when compressed and are slower to recover after the load is removed, all of which are likely to impair the ability of the forefoot to attenuate forces when walking.

Heel pad The heel pad consists of a 13–21 mm thick layer of connective tissue, the deepest portion of which is firmly adhered to the plantar periosteum of the calcaneus by a series of dense fibrous septa containing closely packed fat cells.4 In response to loading, these fat cells flow within the individual chambers, and it is this mechanism, along with the elastic properties of the septa themselves, that provides the heel pad with its shock attenuation capability.43 Evaluations of cadaver heel pads indicate that, with advancing age, the collagen fibres within the septa increase in number and size and appear more fragmented. As a result, the septa may become distorted and rupture, leading to a leakage of fat cells.44 However, this process does not lead to an overall decrease in the unloaded thickness of the heel pad; indeed, there is some evidence that older heel pads are slightly thicker than those of younger people.45–47 Rather, the functionally important age-related differences relate to how the heel pad responds to applied loads. Kinoshita et al48 used a drop-testing apparatus that applied a 5 kg mass to the heels of 10 young and 20 older people at two impact velocities. At the faster impact velocity (0.94 m/s), the older heel pads demonstrated less deformation and greater energy dissipation. In a study using ultrasound measurements of the heel pad in response to vertical loading, Hsu et al46 found that, while the unloaded heel pads of older people were slightly thicker, they demonstrated less compressibility than the younger subjects when a 3 kg load was applied. Evaluation of stress–strain curves indicated that older subjects’ heel pads were also slightly stiffer and dissipated more energy.

Functional implications The functional implications of the changes in plantar soft tissues associated with ageing are unclear. While atrophy of the metatarsal fat pads has been suggested to be a contributing factor to the development of forefoot pain, a recent study using ultrasound measurements found no differences in the thickness of metatarsal pads in those with and without metatarsalgia.49 However, it is likely that the mechanical properties of the fat pads are more relevant than their thickness, as it has been shown that the peak pressure under the metatarsal heads during gait is greater in people with forefoot symptoms.50 Similarly, while research findings related to the role of heel pad thickness in the development of heel pain are equivocal,51–53 it appears that painful heel pads are less compressible and dissipate more energy.51,53 Further studies utilising dynamic measurements of plantar soft tissues are therefore required to confirm the suspected association between ageing soft tissues and foot pain.

PERIPHERAL VASCULAR SYSTEM ARTERIES The arterial wall consists of three layers. The innermost layer, the intima, is composed of endothelial cells, which provide a smooth surface for the passage of blood, supported by a meshwork of collagen and elastin fibres. The middle layer (media) of large arteries consists mostly of elastin and provides vessels with the ability to expand and contract in response to changes in blood flow volume. In contrast, the media of small arteries is largely made up of smooth muscle. The outermost layer (adventitia) is primarily loose connective tissue, which assists in flexibly anchoring the vessel to surrounding structures. A summary of age-related changes in the peripheral vascular system is provided in Table 2.2. Normal ageing does not appear to affect the structure or function of the adventitia; however, considerable changes take place in the intima of all vessels and the media of large arteries. For reasons that are still unclear, the size and shape of endothelial cells become more irregular, and the overall thickness of the intima and media increases as a result of collagen cross-linking and invasion of smooth muscle cells.54–56 Elastin fibres in the media of large arteries break down and stiffen, result-

Peripheral sensory system

Table 2.2 Summary of major age-related physiological changes to the peripheral vascular system Age-related changes

Implications

↑ collagen cross-linking ↑ thickness of intima and media ↑ stiffness of arterial walls ↑ capillary wall thickness → reduced blood flow ↓ diameter of veins

↓ skin temperature ↑ risk of peripheral arterial disease ↑ risk of venous insufficiency

Development of perforator vein incompetence

ing in a reduction in elastic recoil, a reduction in overall flow and an elevation in blood pressure.57 These age-related changes appear to be most pronounced in the lower limb. For example, pulse transmission times (a measure of arterial stiffness) decrease by 1.6 ms/year in the toes compared to 0.6 ms/year in the fingers58 and vasodilation in response to occlusion decreases by 7% per decade in the calf compared to 4% per decade in the forearm.59

CAPILLARIES Capillaries are often less than 1 mm in length and consist of a single layer of endothelial cells supported by a basement membrane. The primary role of capillaries is the exchange of oxygen from red blood cells to surrounding tissues and absorption of waste material. With advancing age, capillaries become even narrower and their porous walls increase in thickness, because of basement membrane thickening and collagen deposition.60 As a result of these changes, ageing is associated with an overall reduction in capillary blood flow, particularly in the lower limb.61,62

VEINS Veins have the same basic structure as small arteries but are larger in diameter and exhibit considerably thinner walls. Relatively little is known about the effects of age on the microstructure of veins and no studies have directly evaluated the effect of age on structure and function of foot veins. However, the diameter of the femoral veins has been shown to

decrease slightly from the age of 60 years and the velocity of blood flow within them steadily declines from the age of 50 years.63 Advancing age is also significantly associated with perforator vein incompetence,64 which may result from the accumulation of collagen fibres around valves.

FUNCTIONAL IMPLICATIONS The overall decline in peripheral vascular function in older people clearly manifests in the foot. Even in the absence of overt vascular disease, many older people complain of cold feet and exhibit dry, flaky skin, particularly on the dorsum of the foot and the toes. As stated in the section on the integumentary system, peripheral vascular changes contribute to delayed wound healing and increased risk of infection. Furthermore, although the development of peripheral arterial disease is multifactorial, age itself has been shown to be an independent risk factor, with an approximate twofold increase in risk for every 10-year increase in age.65 Age is also an independent risk factor for conditions associated with venous insufficiency, such as varicose veins66,67 and venous ulcers,68 which commonly affect the foot and ankle.

PERIPHERAL SENSORY SYSTEM The key components of the peripheral sensory system are the sensory neurons, which consist of a nerve cell body, branch-like extensions called dendrites and an elongated axon that extends from the nerve cell body, and a range of sensory receptors, which are located in the skin and detect a range of stimuli, including vibration, pressure and temperature.69 In particular, the glabrous skin on the sole of the foot contains large populations of mechanoreceptors capable of detecting the site, velocity and acceleration of mechanical stimuli.69–71 A summary of age-related changes in the peripheral sensory system is provided in Table 2.3. With advancing age, there is a generalised decline in the size and number of axons, and the myelin sheaths surrounding the axons undergo significant deterioration, leading to a reduction in nerve conduction velocity.72 Merkel discs and free nerve endings are not affected by age; however, Meissner and Pacinian corpuscles considerably reduce in density and the receptors that remain exhibit a number of morphological alterations.73 As a

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PHYSIOLOGICAL CHANGES IN THE AGEING FOOT

Table 2.3 Summary of major age-related physiological changes to the peripheral sensory system Age-related changes

Implications

↓ size and number of axons → ↓ nerve conduction velocity Deterioration of myeline sheaths ↓ density of Meissner and Pacinian corpuscles

↓ tactile and vibration sensitivity ↓ proprioception and kinaesthesia ↓ balance ↓ walking speed and stability ↑ risk of falls ↑ likelihood of undetected tissue damage

result of changes in receptor structure and function, ageing is associated with significant reductions in tactile sensitivity,74–77 spatial acuity78–81 and vibration sense,74,77,82–85 and these changes are particularly pronounced in the lower limb compared to the upper limb.79,82,86 Proprioception (the ability to detect the position of body parts) and kinaesthesia (the ability to detect movement of body parts) rely partly on skin receptors but also on Golgi tendon organs and receptors in muscle spindles.87 As with other mechanoreceptive abilities, ageing is associated with significant decline in proprioception and kinaesthesia in the sagittal plane of the knee76,88–91 and the sagittal92–95 and frontal plane96 of the ankle.

FUNCTIONAL IMPLICATIONS When standing and walking, the sole of the foot provides the only direct contact with the ground and therefore provides important sensory information about the supporting surface.97 Furthermore, ankle proprioception plays an important role in maintaining balance when walking on irregular terrain. Subsequently, age-related changes in peripheral sensation are associated with deficits in balance 98–103 and walking speed,104,105 and reduced peripheral sensation is an important risk factor for falls.106,107 Loss of plantar sensation in older people may also result in pressure from ill-fitting footwear or foreign bodies within the shoe being undetected, leading to tissue damage and ulceration.108

SKELETAL SYSTEM BONE Bone cells produce two types of tissue: cortical bone, which consists of long tubes of bone matrix (called osteons) forming the outer layer of the bone, and trabecular bone, an irregular matrix that forms the central core of the bone. Cortical bone comprises approximately 90% of the skeleton and is found primarily in long bones. Both types of bone are in a continuous process of remodelling, because of a coupling between bone formation by osteoblasts and bone resorption by osteoclasts. This process enables bone to respond to changing mechanical and metabolic demands.109 A summary of age-related changes in the skeletal system is provided in Table 2.4. Age-related changes in the physiology and biochemistry of bone cells are complex and only partly understood; however, it is thought that ageing primarily affects the structure and function of bone marrow, from which cellular precursors to osteoblasts and osteoclasts are formed. This results in reduced osteoblastic activity, and subsequently the amount of bone formed is not equivalent to the amount of bone resorbed.110 Bone mass therefore undergoes a characteristic trajectory throughout the lifespan, with steady increases in bone density throughout adolescence, a plateau between the third and fifth decade and a progressive decline thereafter.111 In men, age-related bone loss occurs at a rate of approximately 5% per decade,112,113 whereas women experience a more rapid loss (approximately 10% per decade) from the onset of menopause.114 From the age of 75 years, bone loss slows to approximately 3% per decade.112–114 Possibly in response to these changes in bone density, older people’s bones (both cortical and cancellous) also demonstrate a higher proportion of microfractures.115

JOINTS Although the alignment and morphology of lower limb joints differ considerably depending on their function, the basic structure is essentially the same. Each of the bones comprising the joint is covered with a thin layer of articular cartilage. The space between the bones, the joint cavity, is lined by a synovial membrane, which secretes synovial fluid, enabling smooth movement of one bone over the other. Encasing the synovial membrane is the joint capsule, which consists of strong but flexible collagen

Skeletal system

Table 2.4 Summary of major age-related physiological changes to the skeletal system Age-related changes

Implications

Bone ↓ osteoblastic activity ↓ bone density

↑ risk of osteoporosis ↑ risk of traumatic and insufficiency fractures

Joints ↑ collagen cross-linking of cartilage ↓ water content of cartilage ↑ stiffness of synovial membrane and joint capsule ↓ production of synovial fluid

↑ ↓ ↓ ↑

Tendon and ligament ↑ collagen fibril concentration, diameter and cross-linking ↓ water content of glycosaminoglycans ↑ lipid content

↑ risk of posterior tibial tendon dysfunction ↑ risk of tendon rupture when performing non-sporting activities

fibres, and binding the entire joint together are ligaments, which are also primarily composed of collagen fibres. Much of the research relating to age-related changes in joints has focused on cartilage, because of its role in the development of osteoarthritis. Cartilage is a dense connective tissue comprising cells (called chondrocytes) dispersed in a matrix of various types of collagen, proteoglycans and other matrix proteins, and water. The matrix provides cartilage with the ability to withstand compressive, tensile and shear forces generated during movement. Degradation of cartilage is a complex process influenced not only by age but also nutrition, individual mechanical joint characteristics and level of physical activity. Furthermore, it is difficult to delineate age-related changes from those associated with osteoarthritis. Nevertheless, several changes in articular cartilage do appear to be related to the ageing process. At the molecular level, there is a gradual reduction in the amount of chondroitin sulphate and oligosaccharides, and a corresponding increase in keratan sulphate.116 Collagen fibril width and cross-linking increase with age, and the water content decreases.117 Somewhat surprisingly, the cell content and thickness of articular cartilage does not appear to change appreciably with age,118 and joint surfaces in older people may be more congruent than those of younger people. The latter observation has been explained by the notion that some level of incongruence is a normal feature of a healthy joint, in order to provide access of synovial fluid to the cartilage and allow for controlled loading.

risk of osteoarthritis joint range of motion balance risk of falls

With ageing, this protective mechanism becomes less effective, and the joint may be in a state of constant loading.119 In addition to these changes in cartilage structure and function, ageing also results in a stiffening of the synovial membrane and a reduction in its ability to produce synovial fluid. As with ageing cartilage, there is a reduction in the amount of chondroitin sulphate in the synovial fluid,120 which may influence its viscosity. Collagen cross-linking also results in a shortening and stiffening of the joint capsule and supporting ligaments.121

TENDON AND LIGAMENT The primary function of tendons is to transmit muscle force to the skeletal system, whereas the function of ligaments is to bind bones together and restrict excessive movement. Despite this difference in function, the structure of tendons and ligaments is similar – both structures consist primarily of collagen fibrils embedded in a matrix of proteoglycans. Evaluating the effect of ageing on the structure of human tendons and ligaments, however, is inherently difficult because of the need to biopsy tissue. As a consequence, much of our knowledge regarding the biochemical and histological changes in these structures stems from animal models (most commonly rat tails or the Achilles tendons of rabbits), cadavers, or tendons and ligaments harvested from surgical cases.122 These investigations have revealed that advancing age results in significant increases in collagen fibril

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PHYSIOLOGICAL CHANGES IN THE AGEING FOOT

concentration123 and diameter,124 and increased spacing and cross-linking of collagen molecules,125 factors thought be indicative of non-enzymatic glycosylation. Non-collagenous components of tendon have also been shown to undergo changes with age, with decreases in the water content of glycosaminoglycans126 and increases in lipid content.127 A small number of studies have directly evaluated structural changes in the human Achilles tendon. Snow et al128 analysed gross anatomy and histological sections of Achilles tendons obtained from neonatal, young and old cadavers, and reported a progressive reduction in the number of fibres connecting the tendon to the plantar fascia with advancing age. In the older group, a band of periosteum clearly separated the insertion of the Achilles tendon and the plantar fascia. Using light and electron microscopy, Strocchi et al129 evaluated 15 cadaver Achilles tendons up to 87 years of age and reported that ageing was associated with a decrease in the diameter but an increase in the concentration of collagen fibrils. Similar results were reported by Sargon et al130 in 28 Achilles tendon specimens obtained from patients undergoing heel surgery. Finally, using magnetic resonance imaging, Magnusson et al131 demonstrated that older women have a larger Achilles tendon cross-sectional area than younger women, reflecting the age-related hypertrophy evident in animal studies.

FUNCTIONAL IMPLICATIONS The functional implications of an ageing skeletal system are considerable. Changes in bone density are strongly linked to the development of osteoporosis, the prevalence of which increases exponentially with age.132 Although the most serious consequences of osteoporosis are vertebral, femoral and radius fractures, insufficiency fractures of the foot may also occur, most commonly in the metatarsals133–135 but also in the calcaneus136 and talus.137 Such fractures are frequently misdiagnosed and often lead to impaired mobility. Ageing is also a significant risk factor for osteoarthritis,138 which affects the first metatarsophalangeal joint of the foot in 44% of people over the age of 80 years.139 Changes in joint tissues may also be responsible for the reduced range of motion of lower extremity joints in older people. Several studies have shown that ankle dorsiflexion–plantarflexion range of motion reduces with age140–142 and Nigg et al141 have also noted a significant reduction in inversion–eversion and abduc-

tion–adduction motion of the ankle joint complex. Of particular note, women generally exhibited greater range of motion than men but also demonstrated greater reductions in ankle dorsiflexion and eversion with age. More recently, Scott et al143 showed that older people had significantly less range of motion at the ankle joint (36° versus 45°, using a weightbearing lunge test) and less passive range of motion the first metatarsophalangeal joint (56° versus 82°, measured non-weightbearing) compared to younger controls. Assessment of foot posture also indicated that older people had significantly flatter feet, as indicated by a higher foot posture index and arch index, and a reduction in the height of the navicular tuberosity. Reduction in joint range of motion in the foot is strongly associated with impaired balance and functional ability144,145 and increases the risk of falls,145,146 while the progressive flattening of the arch may predispose to the development of posterior tibial tendon dysfunction, a disorder in which the tendon becomes progressively weakened and elongated, resulting in a painful flatfoot deformity.147 There is also emerging evidence that restricted range of motion in the ankle joint may impair the function of the calf muscle pump, thereby contributing to the development of venous disorders of the lower limb.148,149 Finally, despite having a reduced overall risk of tendon rupture because of their reduced exposure to ballistic activities, older people have an increased risk of tendon rupture when performing non-sporting activities, possibly due to age-related increases in tendon stiffness.150,151

MUSCULAR SYSTEM AGE-RELATED CHANGES IN MUSCLE TISSUE Muscle fibres consist of elongated actin and myosin filaments encased in a tubular membrane. Broadly speaking, two types of fibre have been identified: type I fibres, which contract slowly and can stay contracted for long periods of time before fatiguing, and type II fibres, which contract more quickly but also fatigue more easily. One of the most characteristic features of advancing age is the inevitable reduction in the total mass of muscle fibres, often referred to as sarcopenia (adapted from the Greek, meaning ‘poverty of the flesh’).152,153 Muscle mass accounts for 40% of

Muscular system

Table 2.5 Summary of major age-related physiological changes to the muscular system Age-related changes

Implications

↓ total muscle mass ↓ muscle cross-sectional area ↓ size of Type II fibres Development of large, slow-twitch motor units

↓ ankle dorsiflexion and plantarflexion strength ↓ toe plantarflexion strength ↓ balance ↓ walking speed ↑ risk of falls

the total body weight of young people but this reduces to approximately 25% of total body weight in older people.154 This reduction in muscle mass is strongly correlated with the reduction in total muscle crosssectional area, which has been shown to decrease by approximately 40% between the ages of 20 and 60 years155 and involves reductions in both the size and number of muscle fibres.156,157 Although preliminary research suggested that age-related loss of muscle fibres specifically affected type II fibres, more recent evidence indicates that although ageing results in a reduction in the size of type II fibres,158,159 the relative proportion of type I and type II fibres is largely unaffected by age.153 However, ageing also results in motor unit remodelling, a process in which type II fibres are denervated and then reinnervated by collateral branches of type I fibres, resulting in the formation of large, slow-twitch motor units.153 A summary of these changes is provided in Table 2.5. Age-related changes in muscle composition result in significant reductions in muscle strength throughout the body. Comparisons in muscle strength between young and older people (most commonly the quadriceps muscles) generally report differences in strength in the order of 20–40% between the age of 30 and 80 years; however, people aged in their 90s may exhibit even larger reductions (50% or greater).152,160 Because young men generally exhibit greater strength than young women, their absolute reduction in strength associated with age is greater, although the relative loss is similar for both sexes. Because of the difficulties associated with conducting long-term prospective studies, the rate at which these changes occur is not fully understood; however, figures of 1–3% per year have been suggested.161,162

ANKLE MUSCLES As stated above, most studies addressing age-related differences in strength have examined quadriceps muscles; however, some have focused on ankle muscles. One of the earliest studies to assess age-associated changes in ankle muscle function was that of McDonagh et al,163 who compared ankle plantarflexor strength in young and older men and reported that the maximum voluntary contraction in older subjects was 20% weaker than in young subjects. A comparison of these results with those of arm flexor strength suggested that ankle plantarflexors were more significantly affected by advancing age. More recent investigations have largely confirmed these results. Vandervoort & McComas164 reported that the strength of ankle plantarflexor and dorsiflexor muscles declined with advancing age but the differences were most marked from late middle age onwards. VanSchaik et al165 reported that ankle dorsiflexion strength was significantly decreased in subjects aged 60–80 years compared to subjects aged 20–40 years. Similarly, Winegard et al166 compared ankle plantarflexor strength in subjects aged 20–91 years and found that strength significantly decreased with advancing age. Although considerable differences in study populations and methods used make direct comparisons of these investigations difficult, it can be concluded that older people exhibit between 30% and 60% of the ankle strength of younger people.152

FOOT MUSCLES Although it has long been suspected that ageing is associated with atrophy of intrinsic foot muscles, evidence to support such an assertion is scarce. Recent studies using magnetic resonance imaging in people with and without diabetes indicates significant reductions in the volume of ankle plantarflexors167 and intrinsic foot muscles168–170 associated with the disease. Given that many of the neuromuscular changes that occur in diabetes are similar to those of advancing age, it is likely that comparisons between healthy young and older people would reveal similar, but not as marked, differences in foot muscle volume. Only two studies have investigated age-related changes in the strength of foot muscles. Endo et al171 measured the force applied by the toes in 20 young and 20 older participants when instructed to place all their bodyweight on their forefoot while leaning forwards as far as possible. The results revealed that older participants generated 29% less force than younger

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PHYSIOLOGICAL CHANGES IN THE AGEING FOOT

participants. However, the contribution of ankle plantarflexor strength using this testing procedure cannot be discounted and it is likely that the amount of force applied by the toes was also influenced by balance ability. Furthermore, this approach is incapable of delineating between the strength of the hallux and the lesser toes. To address these issues, Menz et al172 used a pressure platform to measure toe plantarflexor strength in 40 young and 40 older participants while seated. The results indicated that older participants exhibited 32% less plantarflexion strength of the hallux and 27% less plantarflexion strength of the lesser toes compared to younger participants, and women exhibited 42% less hallux plantarflexor strength than men. However, sex did not influence lesser toe plantarflexor strength.

FUNCTIONAL IMPLICATIONS The key functional implication of an ageing muscular system is its effect on functional mobility in older people. Lower limb strength is strongly associated

with balance,98 walking speed105,173 and the ability to rise from a chair174 and, subsequently, loss of strength is a major contributor to falls175 and overall functional decline.176 However, there is solid evidence that agerelated loss of strength and its functional consequences can be partly prevented, and possibly partly reversed, by resistance training.153 Secondly, although several authors have suggested that atrophy and/or imbalance of foot muscles may be related to the development of hallux valgus177,178 and lesser toe deformities,169 the role of muscle weakness in the development of foot deformity remains unclear.

SUMMARY Normal ageing has a significant effect on the structure and function of the foot and these changes have considerable implications for the development of foot problems. A sound knowledge of these changes is essential for clinicians involved in the assessment and management of foot disorders in older people.

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