The musculoskeletal (MSK) changes are the most obvious external signs of aging, as most people have some wear and tear on this system as they age (Aldwin & Gilmer 2004). Changes in the MSK system after long-term SCI may lead to upper extremity pain (Waters et al. 1993), reduced strength due to muscle atrophy (Giangregorio & McCartney 2006), and an increased risk for fractures (Lazo et al. 2001). Hence, the complications associated with a degenerating MSK system hold serious implications in terms of functionality for the person aging with SCI.
In terms of bone health, peak bone mass is achieved by the age of 30 in the general population and then declines, but the rate of decline is affected by a number of factors such as age, gender, and lifestyle (e.g., smoking). Although the risk for osteoporosis and fracture are greater among post-menopausal women over the age of 65 in the general community (Goddard & Kleerekoper 1998), there is evidence for increased risk in the SCI population (Ingram et al. 1989; Garland et al. 1992; Lazo et al. 2001). After sustaining a SCI, there are several reports of bone loss occurring in the early months following injury (Garland et al. 1992). These losses are regional; areas rich in trabecular bone are demineralized to the greatest degree, with the distal femur and proximal tibia bones being the most affected, followed by the pelvis and arms (Garland et al. 2001a). However, there is some evidence that there is a continual loss of bone mass with time since injury (Demirel et al. 1998; Bauman et al. 1999), which suggests that a steady state of lower extremity bone mineral homeostasis is not reached (Craven et al. 2014). Assuming that the rate of bone loss in the aging SCI-population is similar to that of the non-disabled population, it is likely that the degree of osteoporosis will be much more severe since they will have less skeletal mass at the onset of typical age-related declines in bone mass (Waters et al. 1993).
As a result of bone loss associated with SCI, there is an increased risk for fracture (Garland et al. 2001a; Craven et al. 2014). After SCI, the most common areas at risk for fracture include the distal femur and proximal tibia, and are consistent with site-specific decreases in bone mineral density around the knee (Craven et al. 2014). The majority of fragility fractures occur following transfers or activities that involve minimal or no trauma (Ragnarsson & Sell 1981). Individuals with SCI are more at risk for osteoporosis if they are older, and the time since injury is longer (Lazo et al. 2001). However, it is BMD, and not age per se, that is the significant predictor for risk of fracture (Lazo et al. 2001). Interestingly, the BMD of the spine is often maintained or actually increases (Garland et al. 2001a; Sabo et al. 2001).
Although BMD of the spine after SCI does not appear to be affected by aging, there are other age-related changes to the spine. With age the spine undergoes degeneration, which may cause deformity or nerve root compression that produces symptoms of pain radiating into the extremities, loss of sensation and/or motor function (Waters et al. 1993). Age-related degenerative changes in the spine may severely impact individuals with SCI whose functional capacities are already limited (Waters et al. 1993). Long-term SCI is associated with scoliosis and/orCharcot spine (progressive destruction of the spine and surrounding ligament leading to major spinal instability) (Sobel et al. 1985; Park et al. 1994; Krause 2000; Vogel et al. 2002; Abel et al. 2003). Age at injury, however, may also play a role as there is some lower level evidence that the odds of developing curvature of the spine is lower in persons who are older when injured (Krause 2000).
There are a variety of musculoskeletal changes associated with aging. In the general population, there is degeneration in the joints of the upper and lower extremities, and common sites include the shoulder, knee, and hip (Waters et al. 1993). As well, muscle atrophy is inevitable with age, although the rate of decline varies from person to person (Loeser & Delbono 1999). These age-related changes may lead to joint pain, stiffness, restricted range of motion, or trauma (i.e. fracture) that would not typically occur in a younger person. As a result, independence when performing daily activities may be compromised due to restricted activities of daily living, mobility. Lack of mobility may also affect temperature regulation (Aldwin & Gilmer 2004).
In addition to bone loss (see section 2.2.1), persons with SCI experience muscle atrophy (Giangregorio & McCartney 2006), especially among muscles that are denervated from complete SCI (Lam et al. 2006). In the lower extremities, muscle degeneration typically occurs around the knee in those who are capable of ambulation but have persistent gait abnormalities, which in turn may generate pathologic forces at the knee (Waters et al. 1993). Although persons who primarily utilize wheelchairs rarely develop clinically significant degenerative problems in the lower extremities, they are more likely to have problems in the upper extremities due to overuse of muscles needed to push their wheelchairs, to transfer, and perform weight-shift maneuvers to prevent pressure ulcers (Waters et al. 1993).
Upper extremity pain is common in persons with long-term SCI, and most frequently affects the shoulder and wrist (Sie et al. 1992; Thompson & Yakura 2001; Waters & Sie 2001), and typically increases with duration of injury (Sie et al. 1992; Ballinger et al. 2000; Waters & Sie 2001). The prevalence of shoulder pain in SCI ranges between 30-100% (Curtis et al. 1999) and is likely a consequence of increased physical demands and overuse (Nichols et al. 1979; Pentland & Twomey 1991). It is unclear, however, if these findings are independent of treatment era effects or are related to environmental changes in mobility technology, accessibility, and rehabilitation practices (Adkins 2004).
Losses in strength and diminished joint capacity along with joint degeneration due to overuse can negatively impact functional ability, which makes maintaining high levels of independence difficult. Since persons with SCI are operating at a near-maximum capacity but have a low reserve capacity, declines in functionality may occur prematurely (Thompson & Yakura 2001).
In this section, 12 longitudinal studies, 1 mixed longitudinal/cross-sectional study and 23 cross-sectional studies on the musculoskeletal system after SCI are reviewed.
In general, the evidence supports the notion that the musculoskeletal system undergoes obvious external signs of premature aging except for a few areas. Many studies found that there was rapid bone loss, and particularly for the pelvis and lower limbs within the acute stage post-SCI (Garland et al. 1992; Biering-Sorensen et al. 1990; Wilmet et al. 1995; Dauty et al. 2000; de Bruin et al. 2000; Frey-Rindova et al. 2000; Garland et al. 2004; Frotzler et al. 2008, Dudley-Javoroski & Shields 2010; Dionyssiotis et al. 2011). Further, this loss may be greater for females with SCI (Garland et al. 2001b) and is evident in both bone mineral density (BMD; amount of matter per cubic centimeter of bones) and content (BMC; bone mass). Similarly, there are bone geometric changes (Finsen et al. 1992; de Bruin et al. 2000; Giangregorio et al. 2005) that occur, which may be independent of chronological age and YPI (Slade et al. 2005).
Some of the findings are mixed with regards to the duration of decline. One study found that bone mass continues to decline throughout the chronic phase (Finsen et al. 1992), whereas another study reporting a rapid loss with stabilization after approximately 2 years (Dudley-Javorski & Shields 2010). A cross-sectional study with AB controls (Eser et al. 2004) and a longitudinal analysis of the same cohort of persons with complete SCI (Frotzler et al. 2008) found that tibial and femoral bone geometry and density properties reach a new steady-state within 3-8 YPI, with the time frame depending on bone parameter and skeletal site.
The use of peripheral quantitative computed tomography (pQCT) is viewed as a superior approach for investigating changes in BMD and BMC compared to dual energy X-ray absorptiometry, DXA), but there are some unresolved issues with the use of this technology in people with SCI (Dudley-Javorski & Shields 2010). A mixed cross-sectional and longitudinal study by Dudley-Javorski & Shields (2010) who used two approaches for studying declines in BMD via pQCT found BMD values of their SCI subjects (n = 15) fell below the lowest range of control values (n = 10), suggesting that subjects lost an average of 1.7% BMD per month within the first two years post-SCI. However, their subjects (N=4) who were followed longitudinally starting at approximately 2 years demonstrated no BMD decline over time. There is a need to better understand anatomical variations related to bone adaptive processes in order to account for SCI-related bone losses (Rittweger et al. 2010). As such, further refinement into bone assessment are needed to help clarify some of the mixed findings noted in the literature.
There are also a number of other factors that contribute to bone loss post-SCI. For instance, endocrine changes may be contributing to the losses in bone density (Dauty et al. 2000; Szollar et al. 1998; Finsen et al. 1992; Vaziri et al. 1994; Bauman et al. 1995). It is thought that altered bone structure and microarchitecture due to SCI (de Bruin et al. 2000; Eser et al. 2004; Giangregorio et al. 2005; Kiratli et al. 2000; Slade et al. 2005; Frotzler et al. 2008) leads to impaired calcium and phosphate metabolism and the parathyroid hormone (PTH)-vitamin D axis (Finsen et al. 1992; Vaziri et al. 1994; Bauman et al. 1995; Szollar et al. 1998; Dauty et al. 2000). For instance, Bauman and colleagues (1995) noted that the reduction in the bioavailability of vitamin D in persons with SCI is similar to that found in AB elderly persons. These changes have been shown to contribute to premature onset of osteoporosis and increased risk for fracture in total and regional sites following SCI when compared to the AB population (Garland et al. 1992; Szollar et al. 1997a; Szollar et al. 1997b; Dauty et al. 2000; Kiratli et al. 2000; Garland et al. 2001b; Vlychou et al. 2003; Eser et al. 2004; Giangregorio et al. 2005; Frotzler et al. 2008, Dudley-Javoroski & Shields, 2010), which may be more related to YPI than chronological age (Bauman et al. 1999; Garland et al. 2001b).
Age of SCI onset, however, may be an influential factor on the extent of the decline in bone loss (Garland et al. 2001b; Kiratli et al. 2000; Szollar et al. 1997a). For instance, the findings by Szollar and colleagues (1997a) provide evidence that the BMD of persons with SCI are significantly lower than the AB population, but that YPI (i.e., older adults injured at a young age) may be more influential on BMD changes in specific areas (i.e. femoral and trochanter regions), although older males may not be as severely affected. Persons who were 60 years or older had comparable levels to their age-matched AB controls in their BMD whereas persons in the younger age categories had significant differences in their femoral regions at different intervals (Szollar et al. 1997a). For instance, younger adults with SCI (20-39 year olds) had significantly lower BMD at 1-5 YPI and at 10-19 YPI in the femoral regions of their neck and trochanter when compared to their AB controls, and the mid-age group (40-59 year olds) only had lower BMD at 10-19 YPI in the femoral neck and trochanter regions. These findings possibly allude to premature aging occurring at specific intervals post-injury, most notably in the first year, in the femoral region in younger persons with SCI, and are consistent with the other identified studies (Garland et al. 1992; Biering-Sorensen et al. 1990; de Bruin et al. 2005; Frey-Rindova et al. 2000; Wilmet et al. 1995; Chow et al. 1996; Szollar et al. 1997a; Szollar et al. 1997b; de Bruin et al. 2000; Kiratli et al. 2000; Eser et al. 2004; Frotzler et al. 2008). It may be that age-related factors become less important on changes in bone mass when an individual reaches a certain chronological age threshold (i.e. 60 years). At this point, other factors (i.e. immobilization) affecting bone mass may become more prominent. In general,all of these changes provide additional support that premature aging is occurring.
Gender also is an influential factor on bone loss. Garland and colleagues (2001b) provide evidence that women with a complete SCI incur a rapid bone loss in the knee, resulting in a BMD that is approximately 40% to 45% of the AB population, and that this loss is greater than the loss seen in males with comparable injuries. Unlike the findings by Szollar and colleagues (1997a), the pattern of bone loss of the hip was linear regardless of the age at the time of injury. The findings by Bauman and colleagues (1999), which used a cross-sectional monozygotic twin design, also shows evidence that duration of injury may be more closely associated to bone loss than current age. Although lifestyle habits such as smoking and alcohol intake were examined and found not to be significant, the sample in Bauman et al. (1999) study was quite small, and relatively young.
As well, a study by Slade and colleagues (2005) which compared bone loss at the knee between AB and SCI women who were pre- and post-menopausal concluded that although age and estrogen effects could not be independently discerned, it was unloading (lack of weight bearing) that resulted in the deterioration of trabeculae that occurs early post-injury. Given that SCI is less common in women, more studies are needed to further our understanding of the interaction between gender, SCI, and aging plays on bone loss.
Interestingly, the lumbar spine BMD of persons with SCI appears to increase with age regardless of YPI. Szollar and colleagues (1997a) interpreted this finding as either being representative of the lumbar spine becoming the primary weight-bearing region or that neuropathic osetorarthropathy (i.e. spectrum of bone andjoint destructive processes associated with neurosensory deficit) may have caused diffused increased radiodensity of the spinal column. The finding that BMD and BMC of the spine remains unaffected or increases is consistent with several other of the identified studies (Biering-Sorensen et al. 1990; Dauty et al. 2000; Chow et al. 1996; Garland et al. 2001b; Szollar et al. 1997b; Szollar et al. 1998), and are complementary to the findings by Catz and colleagues (1992). Based on their findings, Catz et al. (1992) concluded that an SCI injury does not accelerate the aging process of the lumbar spine, and that it may even prevent some expected spinal bone changes since no significant differences were detected between their group with SCI and their AB matched control group. However, they noted that a limitation of their study was that 10 years might be too short a duration to detect any significant effects. As well, the sample size was small and consisted of a heterogeneous group of spinal cord etiologies (i.e. non-traumatic). Finally, one study (Amsters & Nitz 2006) found that postural changes, such as thoracic kyphosis, might also be independent of age and YPI.
With regard to the upper extremities, the musculoskeletal system appears to decline with YPI (Siddall et al. 2003; Jensen et al. 2005; Akbar et al. 2010), with the incidence of shoulder pain increasing over time. However, the role of chronological age may also be influential (Lal 1998; Kivimäki & Ahoniemi 2008). The incidence of degenerative shoulder changes (Lal 1998) may be higher in persons who are older than 30 years and are less than 10 YPI, suggesting that degenerative changes may occur earlier than previously thought in persons with SCI.
In addition to the lumbar spine, there are other areas of the musculoskeletal system that are not negatively affected by aging. For instance, handgrip strength may increase with YPI in males with paraplegia relative to AB controls (Petrofsky & Laymon 2002). This may be due to the use of manual wheelchairs, as well as to age-related changes in muscle fibre composition, and/or to a reduction in intramuscular pressure (Petrofsky & Laymon 2002). As well, older males with paraplegia (45 years and older) may have comparable levels of upper extremity strength to AB controls (Pentland & Twomey 1994).
There is Level 4 evidence from 9 longitudinal studies (Biering-Sorensen et al. 1990; Garland et al. 1992; Wilmet et al. 1995; de Bruin et al. 2000; Frey-Rindova et al. 2000; Garland et al. 2004; de Bruin et al. 2005; Frotzler et al. 2008, Dudley-Javorski & Shields 2010) and Level 5 evidence from 15 studies (Chow et al. 1996; Szollar et al. 1997a; Szollar et al. 1997b; Szollar et al. 1998; Bauman et al. 1999; Dauty et al. 2000; Kiratli et al. 2000; Garland et al. 2001b; Vlychou et al. 2003; Eser et al. 2004; Giangregorio et al. 2005; Slade et al. 2005; Dudley-Javorski & Shields 2010; Rittweger et al. 2010; Dionyssiotis et al. 2011) that there is a rapid loss of bone in the hip and lower extremities following SCI.
There is Level 2 evidence (Frotzler et al. 2008) and Level 5 evidence (Eser et al. 2004) that tibial and femoral bone geometry and density properties reach a new steady-state within 3-8 year post injury, with the time frame depending on bone parameter and skeletal site.
There is Level 5 evidence from three studies (Szollar et al. 1997a; Szollar et al. 1998; Garland et al. 2001b) that older males and females with SCI may not experience as rapid of a decline in bone mass compared to AB controls.
There is Level 5 evidence from two studies (Bauman et al. 1999; Garland et al. 2001b) that year YPI may be more associated with bone loss after SCI than chronological age.
There is Level 5 evidence (Slade et al. 2005) that there are differences in bone geometric indices and in structural properties in the lower extremities of women with SCIcompared to the AB women.
There is Level 5 evidence from five studies (Finsen et al. 1992; Vaziri et al. 1994; Bauman et al. 1995; Szollar et al. 1998; Dauty et al. 2000) suggesting that there are impaired biochemical and bone markers in persons with SCI compared to AB controls that persons with SCI are at greater risk for fracture due to the premature development of osteoporosis.
There is Level 2 evidence from a longitudinal study with AB controls (Catz et al. 1992), Level 4 evidence from a longitudinal study (Biering-Sorensen et al. 1990), and Level 5 evidence from five studies (Chow et al. 1996; Szollar et al. 1997a; Szollar et al. 1997b; Szollar et al. 1998; Garland et al. 2001b) that premature aging does not occur in the lumbar spine after SCI. The possibility that the lumbar spine becomes the primary weight-bearing region, along with immobilization, may serve to protect age-related bone loss changes to this region.
There is Level 5 evidence (Amsters & Nitz 2006) that persons with SCI, regardless of age or YPI, had increased thoracic kyphosis compared to AB controls.
There is Level 5 evidence from two studies (Pentland & Twomey 1994; Petrofsky & Laymon 2002) that decreased hand grip strength does not occur in men with complete paraplegia and that continual wheelchair use may retard this aging process.
There is Level 5 evidence (Pentland & Twomey 1994) that upper limb pain in males with complete paraplegia who use manual wheelchairs may be attributed to longer YPI and not to chronological age.
There is Level 2 evidence from two longitudinal studies (Siddall et al. 2003; Jensen et al. 2005) showing that the incidence of shoulder pain increases over time in persons with SCI.
There is Level 2 evidence from a longitudinal study (Lal 1998) and Level 5 evidence (Kivimäki et al. 2008) that highlights chronological age having an important influence on developing shoulder pain.