INTRODUCTION
Emerging research is substantiating the negative health effects associated with long bouts of sitting (14,16,23–25 ). A number of cardiometabolic and inflammatory risk biomarkers have been linked to this sedentary behavior (i.e., sitting), including increased waist circumference, glucose, insulin, triglycerides, and the inflammatory marker, C-reactive protein (14–16,23,32 ). This new wave of research suggests that more frequent bouts of low-intensity, short-duration physical activity/movement spread across the day (i.e., standing, moving around), in conjunction with a reduction in sitting time, could have profound health benefits for the general population (24,32 ).
The growing awareness of the significant health consequences associated with long bouts of sitting behavior is a major concern for people with physical disabilities. Population-based data reflect higher rates of physical inactivity in people with disabilities compared with the general population (2 ). In addition to adults with disabilities (10 ), our research indicated that higher rates of obesity were present in youth with disabilities (26 ). Consequently, physical inactivity and obesity increase the risk of negative health outcomes in those with disabilities.
As people with disabilities age, a steep reduction in daily energy expenditure may result when individuals transition from use of a manual wheelchair, cane, or braces for community and household ambulation to a power wheelchair. This can occur when individuals are no longer capable of performing physically demanding tasks such as walking with an assistive aid or pushing their own wheelchair because of overuse or repetitive stress injuries that elicit high levels of pain or fatigue, often referred to as secondary conditions and associated with a primary disability (8,9 ). Among younger disabled populations (i.e., people born with a disability or those acquiring a disability early in life), new secondary health conditions (e.g., pain, fatigue, injury, weight gain) (4,8,9,33 ) may require greater reliance on power wheelchairs or scooters in place of manual wheelchairs or other assistive devices to maintain community ambulation. Although these devices have enormous benefits in terms of maintaining physical independence and community engagement, an unrecognized but noticeable decline in daily energy expenditure may result from over-reliance on them.
The growing volume of research on the cardiometabolic and inflammatory risk factors associated with high rates of sitting behavior (15,24 ) is a substantial concern for people with disabilities. One major health outcome associated with extremely low rates of physical activity and increased sedentary (sitting) behavior is deconditioning (34 ). Deconditioning is associated with disuse-induced changes in muscle and bone leading to a cluster of cardiometabolic and musculoskeletal risk factors that predispose individuals to high rates of physical decline and disease risk (5,21 ). Although deconditioning can affect all populations across the lifespan, in people with physical disabilities who have difficulty standing or walking, it is an even greater concern because of the limited opportunities to engage in low-level daily energy expenditure (e.g., standing and moving around). In this article, we provide a conceptual framework for understanding how disability-associated conditions lead to high rates of physical inactivity, which in turn result in an accelerated physical decline in people with disabilities. We end the article with a novel approach for increasing energy expenditure in this population across the spectrum of physical activity through the use of technologies that promote and encourage greater movement-related behaviors across the day.
HIGH-RISK SEDENTARY BEHAVIOR IN PEOPLE WITH DISABILITIES
Our recent work noted that people with disabilities, in general, are likely to perform a lower amount of unstructured physical activity across the day related to work and household activity (29 ). In fact, people with disabilities also are more likely to spend much of their day in sedentary behavior (i.e., sitting) (11 ). Impairments associated with neuromuscular disabilities (e.g., joint pain, paralysis, paresis, balance disorders, sensory impairments, spasticity) may limit opportunities to engage in common forms of physical activity and lead to higher levels of sedentary behavior (i.e., sitting) (4,8,21,34 ). Furthermore, the unemployment and underemployment rates among people with disabilities are substantially higher than those in nondisabled populations (17 ), increasing the risk of prolonged sitting behavior in the home (i.e., less movement-related behaviors associated with preparing for, and getting to and from, work). Although people without disabilities commonly engage in frequent, brief, and intermittent bouts of low-intensity physical activity across the day (e.g., standing, moving around, taking the stairs, doing interior and exterior housework, walking the dog) and have continuous access to walking, people with neuromuscular disabilities who use a wheelchair for mobility or have disability-related impairments are limited or restricted in similar opportunities for spontaneous (e.g., standing, moving around) and structured (e.g., walking) activity and, therefore, substantially spend more time in sedentary behavior (22 ).
In work that we conducted in our laboratory, we found that in a sample of women with disabilities, the average time spent sitting, lying down, and sleeping was 18 h·d−1 and approximately one (17%) of six study participants was sitting, lying down, and sleeping 24 h·d−1 (31 ). Unpublished data (Rimmer JH and Liu Y, 2001) from our laboratory highlight the advanced decline in cardiorespiratory fitness in adults with physical disabilities. The data shown in Figure 1 are compared with norm-referenced data published by the American College of Sports Medicine (3 ) classified by age group. In every instance, people with neuromuscular disabilities fell significantly below the average values for adults without disabilities. No study participant with a disability reached the 10th percentile or lowest cardiorespiratory fitness category compared with the norm-referenced value. These data support the findings of our recently published systematic review on exercise training in adults with disabilities, in which the majority of studies reported very low fitness reserves in various subgroups of adults with disabilities (28 ).
Figure 1: Data on subjects with disabilities from the Center on Health Promotion Research for Persons with Disabilities (Each
dot represents one participant) compared to norm-referenced data published by the American College of Sports Medicine (
3 ) and classified by age group.
The substantial reduction in physical activity reported in people with disabilities is exacerbated by five key concomitants of disability: (a) the perception of needing to conserve energy to avoid fatigue may prompt limited activity; (b) assistive technologies (including power mobility devices) further substantially can reduce daily energy expenditure; (c) persistent stereotypes about disability and lack of awareness concerning the risks of inactivity continue to lead family members, health care providers, and personal assistants to be overprotective of people with disabilities; (d) persistent issues of access to the built environment (e.g., exercise facilities, exercise equipment, parks, recreation areas) make it extremely difficult to obtain regular bouts of indoor and outdoor physical activity based on our on-site assessments of health clubs and fitness facilities (30 ); and (e) opportunities to perform task-related activities such as housekeeping, doing exterior house or yard work, walking the dog, and gardening, are limited or not possible because of disability-related impairments or because of certain secondary conditions (pain, fatigue, and obesity) that limit or restrict opportunities to be physically active (18,33 ).
DISABILITY-ASSOCIATED LOW ENERGY EXPENDITURE DECONDITIONING SYNDROME
We propose that a certain percentage (and in some cases, a significant percentage) of the decline in physiological and musculoskeletal functioning observed in people with neuromuscular disabilities is related to a substantial reduction in energy expenditure leading to the clinical presentation of disability-associated low-energy expenditure deconditioning syndrome (DALEEDS) (Fig. 2 ). DALEEDS offers one possible explanation for the accelerated decline in health and function observed in younger populations of people with neuromuscular disabilities. It also can serve as an entry point for seeking underlying etiologies and be used as a basis for comparison against other hypotheses.
Figure 2: Conceptual model of Disability-Associated Low Energy Expenditure Deconditioning Syndrome (DALEEDS). IDALs, instrumental activities of daily living.
At the top of the model are the personal and environmental contributors (i.e., antecedents) to physical inactivity, which aligns with the World Health Organization’s International Classification of Functioning, Disability and Health (ICF) (36). The ICF emphasizes that both personal and environmental factors impact body functions and structures, activities, and participation and that changes to any of these domains may result in higher or lower levels of physical activity participation in people with disabilities (27 ). Personal antecedents indirectly increase physical inactivity (shown by the dashed line vs solid line, which represents a direct association) through the following: (a) impairments associated with a disability (e.g., paralysis, spasticity, balance, muscle weakness, cognition); (b) secondary conditions (e.g., pain, fatigue, depression, weight gain); (c) employment status (unemployment, underemployment, or nonemployment); and (d) “other” factors including medications and their associated side effects (e.g., weight gain, fatigue), the natural aging process, overprotection (i.e., fear of injury), and hospitalization. (Note: personal antecedents in our DALEEDS model should not be confused with personal factors in the ICF, which includes characteristics not related to the health condition such as sex, race, age, lifestyle, social background, education, occupation, and psychological characteristics.) Environmental antecedents also indirectly influence rates of physical inactivity. Inaccessible indoor and outdoor recreational facilities, lack of accessible home and commercial fitness equipment, and poorly designed communities (e.g., narrow or damaged sidewalks, no sidewalks, poor mixed-use land, limited accessible transportation) have a negative impact on being able to participate successfully and consistently in community leisure and fitness activities.
The center of the model describes the physiological effects of DALEEDS. Physical inactivity leads to a decline in skeletal muscle strength and muscle mass (i.e., sarcopenia) and an increase in fat mass (i.e., obesity). Building on clinical consensus that skeletal muscle-related declines in strength and exercise tolerance, accommodated by increases in fat mass, lead to dysregulated energetics, we hypothesize that these physiological changes can be ordered into one of two pathways: Pathway 1, fitness decline; and Pathway 2, increase in cardiometabolic risk factors. We also hypothesize that either of these two pathways could become self-sustaining and act as independent contributors to the adverse health outcomes listed at the bottom of the figure and, in some cases, may even dominate the clinical presentation independent of its initial cause.
Physical inactivity increases the risk of sarcopenia and obesity, resulting in reduced resting and total energy expenditure. In Pathway 1, obesity and sarcopenia lead to a sequence of events that begins with reduced strength and aerobic fitness, leading to impaired balance, increased risk of falls, and advanced immobilization (less mobility across the day) (6 ). The cumulative effect of this deconditioning segment leads to reduced physical function expressed as a lower ability to complete various basic and instrumental activities of daily living (IADL, e.g., transfers, walking with a mobility aid (walker, cane, braces, crutches), pushing a wheelchair, grocery shopping, meal preparation) and a further increase in sedentary behavior (e.g., sitting) resulting in a decrease in total energy expenditure.
In Pathway 2, sarcopenia and obesity increase cardiometabolic risk factors (13 ). This includes reduced insulin sensitivity, hypertension, dyslipidemia, and increased inflammatory biomarkers (i.e., C-reactive protein). This cluster of risk factors leads to cardiovascular morbidity, which in turn increases sedentary behavior and the risk of heart attack or stroke. In both Pathways 1 and 2, the end result is reduced total energy expenditure, which creates a continuous cycle of health risk leading to metabolic/physiological changes that cause further advancements in physical decline across time.
DALEEDS falls along a continuum of severity, from an end-stage condition that directly occurs before a major injury or illness, to modest alterations in health, function, and participation that clinically are not apparent but, over time, have a cumulative effect. People with neuromuscular disabilities who have difficulty standing or are unable to stand or use the lower extremities for ambulation are at greatest risk for DALEEDS. Poorer health status leads to conservation of energy and higher rates of physical inactivity. High rates of physical inactivity lead to higher rates of obesity and sarcopenia (21 ).
Both Pathways 1 and 2 result in substantial negative health outcomes. Greater reliance on family members or personal assistance services is necessary to assist with activities of daily living (ADL) and IADL; treatment for cardiovascular morbidity, injury (e.g., falls), or secondary health conditions (e.g., pain) increases costly health care expenditures; reduced health and function limit community participation including employment opportunities; mental health issues including social isolation, anxiety, and depression from poorer health status and alterations in lifestyle (e.g., reduced employment); and the cumulative effects of these outcomes reduce overall quality of life.
Understanding the etiology of DALEEDS is essential for establishing criteria for screening and early recognition (21 ). If we assume DALEEDS develops along a continuum of severity, identifying optimal intervention points to reduce physical inactivity may prevent or mitigate the physiological and psychological consequences of DALEEDS. We provide three hypothetical case studies to illustrate how DALEEDS can develop in younger populations with various neuromuscular disabilities:
A 50-year-old man with a spinal cord injury enters the hospital with a Stage II pressure ulcer. He has gained 30 lb since his injury and had a 30% reduction in lean body mass shortly after his injury. He has lost significant amounts of strength and can no longer perform independent transfers or pressure relief (i.e., wheelchair pushups, which involve lifting his lower torso up from the seat of the chair). He sits in his wheelchair most of the day with little movement, activity, or energy expenditure.
A 35-year-old woman with multiple sclerosis has high levels of fatigue and mild depression. She stops going to her local fitness center because she does not want to be around other people and reduces her regular walks from 5 to 2 d·wk–1 . As shown in Pathway 1, over time, her strength, aerobic fitness, and flexibility decline, leading to poorer balance and osteopenia, precipitating a serious fall. To prevent future falls, she begins using a manual wheelchair for community ambulation, which leads to higher rates of immobilization, further decline in physical function (e.g., performing IADL), and increased cardiovascular morbidity. This leads to greater amounts of sedentary behavior and lower total energy expenditure.
An 18-year-old college student with spastic diplegia (cerebral palsy) enrolls in her first year of college. She is starting to have significant pain in her lower extremities and decides to use a power wheelchair to get around campus. Her walking is limited to household ambulation. At her next doctor’s visit, she learns that she has a cluster of cardiometabolic risk factors (Pathway 2) including high blood cholesterol, decreased insulin sensitivity, and mild hypertension, which increases her risk of cardiovascular morbidity. Increased sedentary behavior and lower total energy expenditure lead to higher rates of obesity and further health risks.
ADDRESSING DALEEDS IN PEOPLE WITH DISABILITIES
The majority of the exercise intervention research targeting adults with disabilities has focused on increasing participation in what we term fitness-oriented activities (FOA), which generally involve moderate-to-vigorous physical activity typically sustained for relatively short periods (i.e., 15–30 min). Emerging evidence (25 ) suggests that participation in moderate-to-vigorous physical activity alone may not be sufficient to ensure health benefits if the individual spends prolonged periods in sedentary behavior. This presents an interesting and viable approach for health improvement in people with neuromuscular disabilities who have limited access to organized, structured fitness activities.
The time spent in vigorous intensity activity has been proven not to be related to the total energy expenditure in the general population (35 ). The emphasis on moderate- to high-intensity activity levels makes it a particularly dubious strategy for addressing DALEEDS. A more productive approach may be to identify effective strategies for increasing energy expenditure across the spectrum of physical activity. To illustrate the potential of such an approach, consider our pyramid of physical activity energy expenditure shown in Figure 3 . We classified movement and activity into four broad categories of intensity as defined by the level of energy expended per unit of time spent in various types of activities. We consider the area under each category in the pyramid to reflect a broad estimate of the relative amount of time the average person spends in these activities in a typical month. It is customary for a person, with or without disabilities, to spend more time performing lower intensity activity across the day with only small amounts of time in higher intensity activities (35 ).
Figure 3: Energy expenditure pyramid.
The category at the top of the pyramid is the FOA, which requires moderate-to-high levels of energy expenditure for relatively brief duration. The next two levels include activities requiring energy expenditure in the light-to-moderate range of energy expenditure and include: leisure-time physical activity (LTPA) and task-specific activity (TSA). LTPA typically includes activities not performed at a high intensity or not having fitness-enhancing purposes. Examples include social dancing, gardening, bowling, golf (without a power cart), and leisure bicycling (vs higher-intensity cycling for fitness). TSA includes activities typically referred to as ADL, such as personal care (e.g., hygiene, dressing), and IADL, such as housework (e.g., cleaning, preparing meals). Other examples of TSA include outdoor household activity (e.g., yard work, exterior house maintenance), routine errands (e.g., shopping, banking), and employment-related activity (e.g., commuting, attending meetings, visiting with colleagues).
At the base of the pyramid is a catch-all category referred to as nonexercise activity thermogenesis (19 ). These activity and movement patterns include a wide range of low energy expenditure behaviors such as fidgeting, finger/foot tapping, stretching (in the common sense vs more structured flexibility exercise), rocking, and other idiosyncratic behaviors. People who might be described as restless can expend a regular, continuous number of kilocalories (kcal) over the course of the day. These low-energy, but frequent or continuous, movements accumulate across the day and can contribute significantly to total daily energy expenditure (19 ). Because many of these movements usually are performed in a sitting position, they are ideal for individuals who use manual or power wheelchairs.
Clearly, there are far more opportunities for increasing daily energy expenditure if intervention efforts consider the full spectrum of daily activities across a 16 to 17-hour period of wakefulness. Relatively small increases in participation levels in all categories of physical activity can result in increases in overall energy expenditure (20,35 ) lowering the risk of DALEEDS. Furthermore, the growing evidence base on the physiological effects of sitting behavior (25 ) suggests that distributing lower intensity physical activity throughout the waking hours may be more beneficial than engaging in higher intensity physical activity for a relatively brief duration and being sedentary much of the day. Interventions that produce modest reductions in time spent in sedentary behaviors, even through low intensity activity, have the potential to increase energy expenditure (20 ) and alter energy balance if the increase in expenditure is not offset by a compensatory increase in energy intake.
VIRTUAL EXERCISE ENVIRONMENTS: A GATEWAY TO PURPOSE-DRIVEN PHYSICAL ACTIVITY
With the technologies that are available today and those emerging in the near future, the opportunity to create more interactive exercise environments (with high-definition computer or TV screens and an internet-based connection) holds promise for increasing physical activity participation among people with neuromuscular disabilities. Many individuals with disabilities have limited access to the more enjoyable types of physical activity such as team and individual sports (e.g., golf, tennis, basketball, swimming, jogging, skiing), leisure (e.g., skiing, camping, gardening), and TSA (e.g., shopping in indoor malls). We believe that providing them with similar opportunities in a virtual world could have strong appeal for many people with disabilities who have limited access to these types of activities.
To build a more robust system that provides people with disabilities multiple opportunities to be regularly active across the day, physical activity must have immediate and sustainable end points. Although the distal end point associated with physical activity as a way to stabilize or improve health will attract a small number of end users, the larger percentage of people with and without disabilities who are low adherers to exercise will need other motivating factors.
A central facet in promoting more frequent and longer bouts of physical activity in various populations, and in our case, people with disabilities, first is to identify the reasons why people engage in physical activity. We believe there are six essential reasons why people participate in physical activity: Social interaction, Enjoyment, Learning, Exploration, Competition, and Task completion (SELECT) (1,12 ). In younger populations where most of the physical activity revolves around sports or leisure, participation is associated with enjoyment, social interaction, and competition. In other less competitive groups, hiking, cycling, and walking (e.g., mall shopping) are the main “thoroughfares” for physical activity because of their enjoyment, social interaction, and exploration, which includes the discovery of new places with friends (e.g., trails, bike paths, roads) or identifying and/or purchasing new products (e.g., shopping at a mall). People who enjoy visiting museums, libraries, and places (e.g., new cities, neighborhoods) primarily do so to learn, in addition to exploration, enjoyment, and social interaction. For a large percentage of the population, physical activity is performed for task completion, including work-related activity, cleaning the home, walking the dog, or completing an exercise routine to maintain or improve health. Many people who use cardiovascular exercise machines in gyms and fitness centers often find ways to distract themselves by watching TV, listening to music, or reading because they do not perceive the exercise routine as having any of the other SELECT features besides task completion. Having a broader understanding of what motivates someone to engage in physical activity (SELECT) is an important element for designing technology-based systems that promote higher levels of energy expenditure (i.e., physical activity).
From Virtual Reality to Virtual Exercise Environments
Virtual reality (VR) implementations can be categorized by the extent to which the person experiencing it feels a part of it. An effective VR experience causes the user to suspend disbelief and respond to the virtual environment as he or she would to a natural environment. In VR terms, this is called immersion. Immersion ranges from an experience similar to getting involved in a television show, to the interactive experience of a video game, and at the most advanced level, to a full environment that allows multisensory exploration and experience. The sense of immersion is enhanced by environmental features that approximate real world experiences, such as high resolution three-dimensional images and surround sound. A fully immersive and interactive virtual environment produces a sensation of telepresence — the feeling that the user actually is in the virtual world. The user can explore and even interact with the environment that distinguishes the VR experience from more passive user experiences, such as watching a movie or television show.
Virtual exercise environments (VEE) have the potential to develop compelling immersive augmentations using stationary exercise equipment to navigate through the “environment.” The goal is to target as many SELECT components as possible to reach the broadest audience of nonparticipants. In the case of social interaction, which often is the most challenging aspect of promoting physical activity in people with neuromuscular disabilities because of limited options to engage in mutually satisfying activities (i.e., walking, cycling, tennis) at an equivalent intensity or duration, the geographic distance between people becomes irrelevant when they meet on an internet-based platform. Both the disabled and nondisabled participant can explore a virtual space remotely using different exercise devices (e.g., the disabled person could be using an arm cycle ergometer to explore the VEE, whereas the nondisabled member could be walking on a treadmill or using a stationary cycle. All manner of engaging locations (actual and/or animated) could be presented as a VEE.
In our rehabilitation engineering research center (www.rectech.org ), we have focused on low-cost solutions that integrate with many existing exercise machines in an effort to make the system readily available to all users. In developing these systems, there is a need to address both the quality of the visual and physical interaction on systems that use commodity hardware and, thus, are available potentially to everyone. The basic technology is a high-quality video sequence of a trail or other environment, which is played back according to how fast the user moves on the exercise machine. The video can be displayed on devices ranging from high-end head-mounted displays or multiple large format TVs (Fig. 4 ) to improve immersion, down to a basic computer monitor with an inexpensive tabletop ergometer (Fig. 5 ).
Figure 4: Large format panoramic virtual exercise environment (VEE) with Matrix Krankcycle and three high-definition monitors. Photo courtesy of Jane Mulligan.
Figure 5: Basic virtual exercise environment (VEE) with computer monitor and PCGamerBike. Photo courtesy of Jane Mulligan.
Recorded VEE
The goal of our laboratory work is to provide people with neuromuscular disabilities an equivalent experience as the general population in accessing indoor and outdoor settings that are considered desirable places to visit (e.g., parks, trails, museums, streets, shopping malls) because of one or more SELECT features. The VEE offers a rich visual world to make exercising at home engaging as well as convenient. Going forward, we plan to focus on video content from two general environments that will promote low- to moderate-intensity physical activity:
Shopping mall: recordings from indoor environments, such as malls and stores, which encourage low-intensity activity and relatively short exercise circuits (Fig. 6 ).
City street: recordings of interesting street scenes from a variety of cities (e.g., the French Quarter as shown in Fig. 7 ) that will offer longer duration activity.
Figure 6: Mall shopping (flower store) virtual exercise environment (VEE) circuit. Photo courtesy of Jane Mulligan.
Figure 7: Street life (downtown New Orleans) virtual exercise environment (VEE) circuit. Photo courtesy of Jane Mulligan.
A user could arrange with a friend to meet and explore the space at a specific time (social interaction, enjoyment, learning and exploration ), or the user could choose to go to the virtual environment alone to learn (e.g., museum), explore new merchandise (e.g., mall), or to view interesting architecture (e.g., French Quarter). Users also can speak to each other via voice or text if they choose. “Walking” through the VEE can be performed with an arm ergometer or other type of exercise equipment that is attached to the playback system as the person moves through the space. In the virtual world, each person’s activity makes them move where they wish to explore. If they stop the physical activity they stop moving, which makes the activity meaningful and functional to the context.
CONCLUSION
A variety of social, economic, and environmental barriers continue to keep people with neuromuscular disabilities in the low to very low levels of daily energy expenditure, increasing their risk of DALEEDS and reducing their overall health and well-being. People with neuromuscular disabilities need greater access to purpose-driven physical activity (SELECT) that provides them with opportunities to be active across the day. As we work towards providing greater access to all forms of indoor and outdoor activity for people with disabilities, VEE hold great promise in providing people with disabilities an intermediate source of opportunities to engage in physical activity for a number of SELECT reasons that will ensure greater adherence over time.
This work was supported by the National Institute on Disability and Rehabilitation Research, Rehabilitation Engineering Center on Interactive Exercise Technologies and Exercise Physiology for People with Disabilities, Grant no. H133E070029.
All authors certify that there is no conflict of interest with any financial organization regarding the material discussed in the manuscript.
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