Macrochanges to tissues associated with the chronic phase of SCI and relevant to the risk for PUs and DTIs typically include increases in body weight and fat mass, bone shape adaptation, muscle atrophy, and increase in IMF, as well as disuse-induced skin adaptation and changes to the macro- and microvasculature. These changes and their impact on the structural and functional anatomy of the buttocks are depicted in Figure 1.
Body weight. The literature presents considerable evidence demonstrating a tendency for major weight gain during the first year after a SCI. A retrospective chart review study25 in a US Department of Veterans Affairs SCI Unit (N = 85) showed the body mass index of two out of three patients increases to overweight or obesity levels within this timeframe. It appears the majority of patients are unable to adequately decrease their caloric intake to match their lower level of activity and metabolic caloric needs. This can result in a weight gain of 1.3 to 1.8 kg per week for SCI patients undergoing rehabilitation (shown in 22 patients in their early rehabilitation phase),26 which occurs after the initial weight loss of 5.3 to 9.1 kg these patients experience shortly after the acute SCI due to hypercatabolism; nutrient deficiencies such as albumin, carotene, transferrin, ascorbate, thiamine, folate, and copper typically are documented at 2 weeks post injury.27 This weight change infers the size of the buttocks and weight of the trunk are changing over time and typically start to increase after the first few weeks post acute injury, which has implications for sitting. Elsner and Gefen28 and Sopher et al29 investigated the biomechanical consequences of this gradual weight gain on deformations in the gluteal muscles during sitting. It could be hypothesized that a high body (or trunk) mass may lead to a greater risk for PUs, particularly DTIs, due to the increase in compressive forces from the ITs on overlying deep soft tissues in the buttocks. Conversely, it is possible the extra body fat associated with overweight or obesity may reduce the risk for PUs by providing enhanced subcutaneous cushioning that redistributes high IP. The Elsner and Sopher computer simulation studies28,29 clearly and consistently showed being overweight, particularly when co-existing with muscle atrophy (which is typical in SCI as well), contributes to a state of elevated deformations in the glutei, which may increase the likelihood of PUs in general and DTI in particular in the overweight SCI population. However, ongoing changes to the surface shape and size of the buttocks, as well as to internal anatomy (eg, thickness of fat tissue layers) in the SCI population in terms of the prescribed cushion also should be considered, but research addressing this specific problem still is lacking.
Skeletal changes. Bone adaptation due to disuse in SCI is clearly documented in the literature; primary adaptations include demineralization of epiphyses and thinning of the diaphyseal cortical walls below the injury level, with greater severe bone loss occurring in individuals with tetraplegia.30,31 Biomechanically, the bone loss is promoted by the absence of muscular loading via tendons, which is the primary stimulus for bone mass homeostasis in the able-bodied.32,33 In Giangregorio et al’s34 case study of two pairs of twins, where one of the twins suffered a SCI (at 7 years old, more than 20 years before the data collection), the authors used computed tomography to measure volumetric bone mineral density (BMD) and bone geometry and found lower BMD in the hip, distal femur, proximal tibia, and (to a lesser extent) in the spine of the SCI twins. Lower moments of inertia were evident at the mid-femur and calf of the SCI twins, indicating cortical bone loss. Studying twins makes a powerful comparison because it eliminates the potential effects of age and genetics. Small cohort prospective studies35 using dual X-ray absorptiometry, peripheral quantitative computerized tomography, and biomechanical test methods have demonstrated these catabolic changes in bone mass and shape occur within 2 years of the SCI, bone loss is more severe in tetraplegia than in paraplegia, large variability exists with respect to anatomical site and across individuals, and gender-dependent differences also may exist.36 The consequences of lower BMD and thinner cortical tissues are (after several years) more fragile bones that, much like in metabolic syndromes, tend to break as a result of non-traumatic loading, including when transferring to and from a wheelchair.30 Specifically with respect to sitting, Linder-Ganz et al12 used MRI scans of seated SCI subjects and found shape adaptations of the ITs, which tend to flatten in SCI patients, possibly due to the chronic exposure to the sitting loads coupled with the ongoing loss of cortical bone mass. The Linder-Ganz data12 revealed 1.8-times greater radii of curvature of the ITs in the SCI patient group with respect to the controls. Hence, ideally, a sitting solution should consider the ITs are gradually changing shape (typically flattening) in a SCI patient, which inevitably affects the load transfer from the weight-bearing ITs to the overlying soft tissues in the seated buttocks.
Disuse-induced muscle atrophy. Atrophy of skeletal muscle tissues is a well-known consequence of SCI. The atrophy occurs below the injury level and at the muscle fiber scale. It includes thinning of the fibers, reduction in the numbers of slow-twitch fibers, and an increase in fast-twitch fibers, which start as early as 4 to 6 weeks after the acute injury (inter-patient variations are considerable).37 The progressive process lasts at least several months and stabilizes between 1 and 6 years after the acute stage, with substantial variations across individuals. The lack of neuromuscular activity leads to microvascular changes as well, which generally cause a reduced oxidative capacity and a greater risk for deformation-induced ischemia.
At the macroscopic scale, the denervation causes rapid muscle wasting. In a group of patients with incomplete SCI (ie, where damage to the spinal cord was not absolute), muscular cross-sectional area in the thighs decreased by one third 6 weeks after the acute injury, and this was accompanied by more than doubling of the IMF contents.38 In Giagregorio et al’s twin study,34 the averages of the cross-sectional areas of the thigh and calf muscles in the SCI twins were as low as approximately 30% of the values for their non-SCI twins. As could be expected, the extent of loss of skeletal muscle tissues depends on whether the spinal cord lesion is incomplete or complete. For example, at a mean time of 13 months from an acute incomplete injury, a reduction of 24% to 31% (tibialis anterior and quadriceps femoris muscles, respectively) was reported in Shah et al’s39 MRI study in 17 people, with a weak correlation with respect to use of a wheelchair. In Castro et al’s study,40 where muscle biopsies were taken from 12 patients at 6, 11, and 24 weeks after a complete SCI, it was shown that complete spinal cord lesions can lead to muscle mass loss twice that found in the Shah et al39 study of incomplete injuries.
Based on supine pelvic computed tomography scans with contrast in 10 able-bodied and 10 participants with SCI, Wu and Bogie41 recently reported gluteal muscle atrophy is relatively greater at the level of the ITs, which highlights the need to especially protect that region by means of a cushion during wheelchair sitting. Lastly, it should be noted muscle atrophy also occurs with normal aging, partly due to neurological and endocrinal changes and partly due to cachexia and the reduced physical activity.42 Accordingly, as a SCI patient ages, the disuse-induced muscle atrophy is superimposed with the aging-related atrophy.
Tissue composition and mechanical behavior.
Muscle/fat. IMF normally functions as dynamic adipose storage depots that are close to muscle fibers and hence accessible for muscular metabolism. These depots can expand when lipids are available, and they tend to increase in non-SCI overweight or obese individuals (the percentage of IMF typically assessed in humans using MRI).43 In able-bodied individuals, the normal IMF level is 1% to 2% of the total fat stored in the body.44 In SCI patients, IMF can increase progressively up to three to four times the healthy levels; after 8 to 10 years of denervation, the adipose tissues are nearly one third of the area in some muscle biopsies.38,45 Using computational modeling, Sopher et al21 demonstrated how internal muscle tissue loads under the ITs are elevated during sitting by the increase in IMF contents, implying the more severe the IMF, the higher the risk for a DTI. The authors explained the rise in skeletal muscle loads observed with the increasing IMF contents by the greater intramuscular shear stresses at interfaces between muscle and IMF tissues. Wu and Bogie41 reported the IMF depots are not homogeneously distributed across SCI muscles but tend to concentrate proximally (so gluteal tissues near the ITs are prone to have excess IMF), and also that high IMF levels correlated with a history of severe and/or repeated PUs, which supports and complements the Sopher21 study. Wu and Bogie41 emphasized skeletal muscle quality and particularly IMF levels in the glutei need to be assessed in SCI individuals because they are an important measure of the risk for severe PUs, keeping in mind the IMF contents evolve and tend to accumulate with time after the acute injury.
From a biomechanical perspective, the build-up of IMF acts to decrease the effective stiffness of the glutei fat tissues (from animals) tested in vitro are less stiff than skeletal muscle.46,47 Computer simulations48 have shown this phenomenon gives rise to greater deformations in the glutei under a given body weight. In other words, the decrease in stiffness of the glutei due to the progressing increase in IMF contents causes the glutei to gradually bear greater sustained deformations, which then increases the risk for PUs and DTIs in particular, even if the patient does not become substantially heavier.
Skin. As previously discussed, disuse adaptation of the skin secondary to SCI is analogous to the degenerative processes in bone and muscle. In a study in Turkey employing high-frequency ultrasound, Yalcin et al49 compared skin thickness in the buttocks of 32 SCI patients to 34 controls and found the skin was substantially thinner over the ITs and sacrum in the SCI group (although the skin of individuals with SCI can thicken at other anatomical sites). Thinning of the skin at the load-bearing sites of a seated body appears to occur together with stiffening of the remaining skin tissues. In a study conducted in South Korea using a noninvasive suction testing device in 48 male participants with chronic SCI and 48 age-matched healthy controls, Park et al50 demonstrated the skin was significantly less distensible in the SCI group (P <0.05). This change in the skin’s biomechanical behavior occurs in conjunction with, and as a result of, deficient vascular reactions, decreased fibroblast activity, and primarily higher collagen catabolism. The loss of stability of intermolecular collagen cross-links, which is evident in increased urinary excretion of the biochemical residues of the disintegrated collagen in SCI, occurs months before these patients develop visible PUs (demonstrated in analyses of 24-hour urine samples from 60 men with SCI who were followed-up prospectively in the US).51 These are all changes associated with the disuse of skin tissues. The Park et al50 study also reported the duration of the SCI had a substantial impact on the changes in distensibility, elasticity, and viscoelasticity — ie, biomechanical skin properties. Taking the Yalcin49 and Park50 studies together, the thinner and stiffer SCI skin tissues, particularly at the weight-bearing sites of sitting, must cause the mechanical stresses (eg, when a patient moves or is being moved) in the deformed SCI skin to increase. At the same time, the strength of the SCI skin should decrease due to the loss of the collagen cross-links at the material level and the loss of thickness of the skin structure.49-51 This places SCI patients at high risk for superficial (tension- and shear-related) PUs (in addition to DTI) as a direct result of these skin changes. Interestingly, although not as widely reported as the degenerative musculoskeletal changes in SCI previously described, these skin changes are progressive and develop from the time of the acute injury,50 much like the disuse-induced musculoskeletal changes.
Tissue perfusion. Autonomic impairments may lead to increased prevalence of cardiovascular abnormalities in SCI patients, which manifest in the macro- and microcirculation (the impaired microvascular reactivity in SCI is largely due to the sympathetic dysfunction over the cardiovascular system). With respect to macro-circulation, which was studied in a retrospective chart review,52 hypotension was found to occur more in patients with a high level SCI. Additionally, a meta-analysis53 showed individuals with a cervical SCI exhibit a lower resting systolic blood pressure in the seated versus a supine position. Literature reviews summarizing data from muscle biopsies further report a gradual pathological decrease in numbers and sizes of capillaries that feed muscle fibers in skeletal muscle tissue of SCI patients.54,55 The fewer, narrower capillaries in SCI make the deformed skeletal muscles more prone to ischemia, particularly during episodes of low blood pressures. Although ischemic damage in weight-bearing muscles is now recognized to occur subsequent to direct deformation damage,9 it should be taken into account that muscle tissue in the SCI population becomes more susceptible to ischemic damage with the time that elapses post acute injury, which is a consequence of the disuse-induced muscle atrophy. The author’s conclusion, based on the above findings, is that when adding the systemic cardiovascular impairments, a given level of sustained muscle deformations in the SCI patient causing obstructions of the intramuscular vasculature will trigger ischemia sooner than in non-SCI subjects. This is yet another reason why skeletal muscle deformation should be minimized, especially in seated SCI individuals.
Skin, like skeletal muscle, also pathologically adapts in structure and function to conditions of disuse. The reactive hyperemia (ie, the microvascular response to re-establishment of blood flow after a period of a reduced flow due to, for example, sustained tissue deformations) differs between SCI patients and healthy individuals. In a laser Doppler perfusion study,56 eight SCI patients experienced greater perfusion to the buttocks skin tissues following a period of pressure-induced obstruction of the skin vasculature than eight control subjects. This probably indicates the skin of SCI patients experiences more severe ischemic conditions when loaded compared to a healthy skin response to the same loading conditions. Hence, the above-mentioned studies suggest muscle, as well as the skin of SCI patients, undergoes micro- and macro-structural changes over time. These changes, together with systemic cardiovascular changes, eventually cause these tissues to become more sensitive to development of ischemia when sitting for prolonged periods.