Guideline Approaches for Cardioendocrine Disease Surveillance and Treatment Following Spinal Cord Injury

Abstract

Purpose of Review

Persons with spinal cord injuries (SCI) commonly experience individual risks and coalesced health hazards of the cardiometabolic syndrome (CMS). This review will examinethe role of exercise and nutritional intervention as countermeasures to these disease risks.

Recent Findings

The CMS hazards of overweight/obesity, insulin resistance, hypertension, and dyslipidemia are strongly associated with physical deconditioning and are common after SCI. Both the CMS diagnosis and physical deconditioning worsen the prognosis for all-cause cardiovascular disease occurring early after SCI. Evidence supports a therapeutic role for physical activity after SCI as an effective countermeasure to these risks and often represents the first-line approach to CMS abatement. This evidence is supported by authoritative systematic reviews and associated guidelines that recommend specific activities, frequencies, and activities of work. In many cases, the most effective exercise programming uses more intense periods of work with limited rest. As SCI is also associated with poor dietary habits, including excessive energy intake and saturated fat consumption, more comprehensive lifestyle management incorporating both exercise and nutrition represents a preferred approach for overall health management.

Summary

Irrespective of the interventional strategy, improved surveillance of the population for CMS risks and encouraged incorporation of exercise and nutritional management according to recent population-specific guidelines will most likely play an important role in the preservation of activity, optimal health, and independence throughout the lifespan.

Cardioendocrine Disease

The Cardiometabolic Syndrome (CMS)

The CMS—also known as “syndrome X,” insulin resistance syndrome, Reaven’s syndrome, and metabolic syndrome—is a coalescing of cardiovascular, renal, metabolic, pro-thrombotic, and inflammatory health risks [1]. Figure 1 shows the general health indicators and component risks for the CMS. Co-occurrence of three (or more) of the following health risks typically defines the CMS: abdominal (central) obesity, hypertension, insulin resistance, and dyslipidemia, the latter as either hypertriglyceridemia or low high-density lipoproteinemia. When so co-expressed, these risks are recognized as a distinct disease entity by the American Society of Endocrinology, American Heart Association (AHA), International Diabetes Federation (IDF), NIH National Heart Lung Blood Institute (NIH-NHLBI), and the World Health Organization (WHO) [2]. While the definitions for CMS shown in Table 1 have yet to be harmonized entirely [3], it is consistently recognized that any coalescing of risk factors worsens a cardiovascular disease (CVD) prognosis. In particular, a CMS diagnosis increases the odds of developing atherosclerotic disease, heart failure, and diabetes and poses a health risk equivalent to that of either type 2 diabetes or existing coronary disease. CMS is currently reported in 22.9% of the U.S. adult population [4] and is increasing at a rate that resembles a pandemic of communicable diseases.

Fig. 1
figure1

Cardioendocrine health risks

Table 1 Commonly used guideline definitions for the CMS

Prevalence and Causes of CMS After SCI

CMS develops from a mismatch between daily energy intake and energy expenditure [5], making persons with SCI a high-risk target for the disorder. The principal metabolic abnormality of the syndrome is insulin resistance, while the unified cause ensues excessive body adipose mass associated with visceral and ectopic fat depots. Combined “overweight” and “obesity” in persons with chronic SCI describes 60–80% of the population [6, 7], with the most common period for gain in body mass occurring at 2–7 months after completion of post-injury rehabilitation [8, 9]. Not surprisingly, the component risks of CMS are not equally weighted, with sarcopenic obesity [10]—a highly prevalent finding after SCI [11,12,13,14,15]—appearing to be the most powerful progenitor, followed by insulin resistance.

Beyond the characteristic findings of sarcopenic obesity and insulin resistance, all-cause disorders of the integrated cardioendocrine system have been reported in persons with SCI since the early 1980s [16,17,18] and are thought to hasten cardiovascular-related morbidity and mortality [15, 19,20,21]. The genesis of these disorders is primarily attributed to CMS risk factors observed in the non-disabled population, although reported at a significantly elevated prevalence after SCI [6]. These risks include widely cited atherogenic dyslipidemia with low levels of the cardioprotective high-density lipoprotein cholesterol (HDL-C), [22,23,24,25,26,27] dyslipidemia attributed to immobilization-related physical deconditioning [28], and frequently associated with sarcopenia [29] and diminished resting energy expenditure [30, 31]. Otherwise, inadequate caloric expenditure by lowered daily resting energy expenditure and physical activity energy expenditure is thought to increase body fat mass, which is considered a sine qua non of CMS after SCI [32, 33].

Non-Guideline CMS Risks of Sedentary Lifestyle and Imprudent Nutrition After SCI

While physical deconditioning per se is not included among the five component risks of CMS, it is linked with and considered a significant cause of, obesity, insulin resistance, hypertension, and dyslipidemia [15, 34]. The same can be assumed for a hypercaloric diet relative to daily need [8, 35]. Several factors point to physical deconditioning after SCI as a significant contributor to a CMS diagnosis. First, the SCI population was long ago identified at the lowest end of the human fitness continuum, making physical deconditioning suspect as a cause for CMS-related risks [23, 36,37,38]. Second, a common finding after SCI is a low HDL-C, [22, 24, 39] which is strongly linked with low levels of cardiorespiratory fitness in persons without disability [40,41,42]. Third, barriers to exercise participation are common after SCI and may include either self-imposed obstacles to exercise participation or those associated with legitimate physical barriers to exercise, lack of adapted exercise equipment, limited professional assistance, societal mores, and financial limitations [43,44,45,46,47].

In addition to physical inactivity, CMS in humans is strongly influenced by dietary habits and nutritional status [48]. The latter may be significantly altered after SCI due to changes in the metabolic milieu (e.g., loss of metabolically active tissue), physical barriers (e.g., access to food shopping and grocery store shelving), environment (e.g., institutional food), functional challenges (e.g., difficulties encountered in preparing food), and social factors (e.g., food provided as comfort by family/friends) [49]. As persons with SCI living in what has been termed an “obesogenic environment,” [49] this reality and other factors combine to make lifelong healthy nutrition habits all the more challenging.

With respect to nutritional intake, data reported since 2008 indicate that men with SCI consume 500–600 fewer kilocalories than the ∼ 2600 kcal standard for men in the general population [8, 50], while caloric intake for women with SCI is about the same or slightly (∼ 100 kcal) lower than the expected intake of ∼ 1800 kcal [51, 52]. However, data comparing resting energy expenditure and average daily caloric ingestion still identify a surplus intake of ∼ 300–500 kcal per day [52,53,54]. Although this excess intake may seem inconsequential, even a small, sustained caloric excess will eventually lead to weight gain, pathogenic lipid profiles, impaired glycemic control, disease, and increased mortality. More precise data on total caloric expenditure relative to total energy expenditure are thus needed to fashion specific dietary recommendations for persons with SCI and emphasize the need for better matching of caloric intake and expenditure as a primary goal of a healthy post-SCI lifestyle [55, 56].

Despite a lower total daily energy intake than the general population, many studies also report that persons with SCI consume relatively more dietary fat than is recommended [8, 35, 51, 52, 57, 58]. In particular, saturated fat intakes are at the high end of, or exceed the recommended limit (typically < 10% of total calories) [8, 35, 57, 58], although may decline with the passage of time [59]. High-fat intake is commonly associated with weight gain, and in particular, high dietary levels of saturated fat adversely affect metabolic profiles and chronic disease outcomes [60, 61]. There is also evidence for a direct relationship between high-fat intake and serum triglycerides (TGs) after SCI [59], as well as elevated body mass index [39]. The high-fat gain may also worsen a reported exaggerated postprandial lipemia in persons with SCI, [62, 63] in which remnant lipoproteins from delayed metabolism of dietary TGs may accelerate the transfer of TG-rich lipoproteins in the vascular wall and hasten atherogenesis [64].

Guidelines for Addressing CMS Risks After SCI

Given the well-documented CMS risks after SCI and the lack of a unified treatment strategy for its composite and individualized risks, the Consortium for Spinal Cord Medicine recently convened an expert panel to develop Guidelines for Identification and Management of Cardiometabolic Risk after Spinal Cord Injury [65]. These guidelines (from now on the “PVA Guidelines”), and others will form the basis for the remaining information presented in this monograph.

Definition and Surveillance of CMS

The PVA Guidelines [65] recommend the use of the AHA definition for determining CMS in persons with SCI (Table 2). As waist circumference is not a validated proxy for obesity in SCI, the PVA Guideline assumed definitions of obesity as: (a) > 22% body fat when using 3- or 4-compartment modeling or (b) BMI ≥ 22 kg/m2. Table 3 identifies timing for post-injury surveillance and periodic follow-up for the CMS diagnosis and component risks.

Table 2 PVA Guideline definition of the CMS
Table 3 Guidelines for testing of CMD and its five component risks at discharge from rehabilitation and follow-up

Lifestyle Intervention

While physical activity has established benefits as a countermeasure to excessive energy intake, some persons with SCI cannot effectively balance energy intake and expenditure with physical activity alone. Some are limited by their level of injury [66] and overuse injuries [67, 68] as well as other documented barriers to exercise [43, 45, 69, 70]. Based on the existing evidence and appreciating that energy expenditure from upper-body physical activity rarely compensates for excessive caloric intake, nutritional modification may represent a favored target for obesity management and CMS prevention in individuals with SCI. The panel does not recommend a single nutritional plan but notes success in weight loss using the Mediterranean diet in the Diabetes Prevention Program [71, 72], and the DASH Diet, which may be more useful for hypertension management [73, 74]. The Healthy Mediterranean-Style Pattern is also adapted from the Healthy U.S.-Style Pattern, modifying amounts recommended from some food groups to reflect eating patterns that have been associated with positive health outcomes in studies of Mediterranean-style diets.

To date, prospective evaluation of weight loss programs in the SCI population has been limited. Weight loss programs designed for the non-disabled population may not be appropriate for the specific health [20, 55, 56, 75] and nutritional needs [8, 35, 49] of the SCI population. A pilot study of a weight loss program consisting of education on nutrition, exercise, and behavioral modification in individuals with chronic SCI who were overweight or obese resulted in weight loss and improvements in dietary intake [76]. This study utilized the time-calorie displacement diet, which emphasizes large intakes of high bulk, low energy-density foods, such as fruits and vegetables, high-fiber grains, and cereals. It also emphasized a moderate intake of high energy-density foods, such as meats, cheeses, sugars, and fats (Table 4).

Table 4 Risk targets for management of CMS through primary lifestyle intervention using nutrition and exercise

Physical Activity and Exercise in the Lifestyle Plan

Chronic spinal cord injury (SCI) increases morbidity and mortality associated with cardiovascular [77] and metabolic diseases [78], and in persons without SCI the established risk factors for these conditions are effectively managed by engaging in regular physical activity [79,80,81]. However, the evidence is less clear for persons with SCI, who have a range of additional physiological perturbations and barriers to physical activity, which ultimately influence adaptive responses. These issues are, in part, summarized in the Disability-Associated Low Energy Expenditure Deconditioning Syndrome (DALEEDS) model [82], including a range of disability-associated personal and environmental barriers as antecedents to deconditioning, but also accelerated physiological deconditioning in response to physical inactivity. Of particular note, persons with SCI experience a loss of innervation to skeletal muscle, resulting in a rapid and dramatic loss of previously healthy muscle mass below the level of the lesion [83], particularly among larger muscles of the lower limb.

These post-injury adaptations lead to substantial reductions in total energy expenditure, characterized by reductions in both resting metabolic rate [84] and, importantly, a reduction in physical activity energy expenditure [85]. Indeed, persons with SCI appear to perform little or no physical activity [86,87,88,89], which is likely a cause of the higher prevalence of cardiometabolic disease in this population [90, 91]. Cross-sectional studies conducted ~ 20 years ago [25, 92] placed persons with chronic SCI near the lowest end of the human physical activity and fitness spectrum. These findings were recently reaffirmed using validated objective measures of physical activity energy expenditure [85] and physical fitness [93].

Among other health organizations, the WHO has produced general physical activity guidelines for humans, recommending at least 150 min/week of moderate-intensity aerobic activity (or 75 min/week of vigorous-intensity aerobic activity), plus muscle-strengthening activities twice per week [94]. However, WHO recognize that these guidelines were not specifically tailored to the SCI population, stating that: “These recommendations can be applied to adults with disabilities. However, they may need to be adjusted based on individual exercise capacities and specific health risks or limitations.” Disappointingly, studies of people with SCI were excluded from the systematic reviews underpinning these public health physical activity guidelines (e.g. [95],). Consequently, the potential risks of SCI-specific adverse events, including upper-limb over-use injuries [96], skin breakdown [97], autonomic dysreflexia [98], and hyperthermia [99], were not considered in the design of the exercise guideline. Furthermore, these guidelines did not account for the perceived psychosocial and environmental barriers to engaging in physical activity, particularly the access-related barriers, which are unique to persons with disabilities [43, 69]. Coupled with the traditional hindrances of time, knowledge, and motivation, this further complicates both prescription implementation and robust exercise compliance [46, 100]. Given the specific risks and barriers to exercise among persons with SCI and the fact that more than two million people currently live with SCI worldwide, it is a public health priority to develop evidence-based physical activity guidelines for the prevention of cardiometabolic diseases in this population.

One of the significant challenges to this ambition has been the lack of high quality randomized controlled trials to provide a robust empirical evidence base. Notably, the first significant attempt to conduct a systematic review of the available evidence [101] concluded that: “Evidence is insufficient to determine whether exercise improves carbohydrate and lipid metabolism disorders among adults with SCI.” Several years later, despite significant remaining reservations about the quality of the evidence, Martin Ginis and colleagues [102] were able to generate physical activity guidelines. The recommendation was that adults with SCI should engage in: (i) at least 20 min of moderate-vigorous intensity aerobic activity, twice per week and (ii) strength training exercise (3 × 8–10 reps) of each major muscle group, twice per week. However, these guidelines were predominantly aimed at enhancing physical fitness, noting that: “… although the link between fitness and improved health (through risk factor modification) may appear intuitive, the consensus panel felt that there was insufficient evidence to justify PA recommendations related to reducing disease risk.” Given the substantial contributions to the relevant literature since this time, we provide an overview of the current evidence and the latest consensus on physical activity and exercise guidelines.

Unfortunately, the selection of practical exercise activities for persons with SCI is somewhat limited (i.e., upper-extremity exercise), and the consequences of imprudent exercise can be more severe than those experienced by persons without a disability. It is therefore essential to identify exercise activities that reduce risks of physical dysfunction and all-cause cardiometabolic disease while not increasing injury risks or hastening musculoskeletal deterioration. There is clear evidence that upper-extremity moderate-intensity continuous training (MICT) exercise improves cardiorespiratory fitness, and that the magnitude of increase depends on the level of spinal lesion and training stimulus [103,104,105]. However, the role of exercise in reducing cardiometabolic component risk factors in persons with SCI is less clear. In an attempt to assess the efficacy of the 2011 physical activity guidelines for improving cardio-endocrine risks in persons with SCI [102], Totosy de Zepetnik and colleagues [106] conducted a randomized controlled trial. During this 16-week training study, the intervention group completed ≥ 20 min of moderate-vigorous aerobic exercise (rating of perceived exertion 3–6 on a 10-point scale) and 3 × 10 repetitions of upper-body strengthening exercises (50–70% one repetition maximum) two times per week. Despite good adherence, following the physical activity guidelines was insufficient to improve many markers of CMS risk. These findings are in contrast to some other studies, which demonstrate that as little as 20 min of moderate-intensity exercise, performed three times weekly, in persons with SCI, improves plasma high-density lipoprotein (HDL) concentrations [104]. Further studies have also reported ~ 10% increases in HDL and a 26% decrease in low-density lipoprotein (LDL) concentration, with trends for non-significant decreases in plasma total cholesterol and TG concentrations following 3 months of vigorous intensity armcrank ergometry when conducted three times per week for 45 min at ~ 75% HRmax [107, 108]. Interestingly, a more recent randomized clinical trial (RCT) revealed significant and clinically meaningful effects on fasting insulin sensitivity when persons with paraplegia performed 4 × 45-min moderate-intensity (60–65% peak oxygen uptake (VO2peak)) arm-crank exercise sessions per week for 6 weeks [105]. This study concluded that, while the intervention was able to enhance indices of hepatic insulin sensitivity, there was no effect on markers of peripheral insulin sensitivity. It seems clear from these studies that, in order to observe significant effects on cardiometabolic component risks, the absolute volume (135–180 min per week) and intensity (60–70% VO2peak) of MICT has to be substantially higher than previously recommended. This finding is probably not surprising given the relatively small muscle mass involved in upper body exercise and the somewhat limited potential to stimulate disturbances in whole-body hemodynamic or metabolic homeostasis.

As a consequence of this evidence and observations in non-injured humans, there has been considerable interest in the efficacy of alternative forms of higher intensity upper-body exercise (i.e., high-intensity interval training, HIIT) for persons with SCI [109]. The primary rationale for HIIT is that it allows a higher volume of vigorous-intensity exercise to be accrued in a single exercise session. When compared to light- and moderate-intensity continuous exercise training, vigorous-intensity physical activity is more effective in reducing the risk of cardiovascular [110, 111] and all-cause mortality [112,113,114] in non-injured humans. There is also mounting evidence from studies in non-SCI cohorts that HIIT promotes superior peripheral [115] and whole-body physiological adaptations [116, 117], which would be of specific value in overcoming the numerous training limitations for persons with SCI. While a wide range of HIIT protocols have been described in the literature, the terminology proposed by Weston et al. [118], is particularly helpful, where HIIT protocols adopt exercise intensities between 80 and 100% of V̇O2 peak and those protocols using “all-out” efforts, or efforts > 100% V̇O2 peak are referred to as “sprint interval training” (SIT). It is relatively simple to deliver such a training stimulus via upper-limb armcrank exercise for persons with SCI. Indeed, early indications are that persons with SCI experienced greater enjoyment with HIIT and SIT protocols compared with MICT [119]. Further robust studies into the efficacy of HIIT for reducing cardiometabolic component risks in the fasted and post-prandial states are underway (e.g. [120],) and are necessary to confirm the benefits of HIIT in persons with SCI.

Resistance exercise training is now also universally recommended in exercise guidelines, adopted for use by persons with a disability [65]. Resistance training offers the potential to both prevent and treat shoulder pain [121] while improving or maintaining transfer and propulsion independence. One of the earliest studies to assess the efficacy of upper-body resistance training in men with incomplete low thoracic spinal lesions had a particular emphasis on developing triceps strength (for elbow extension during crutch walking) was undertaken for 7 weeks. In addition to the expected gains in triceps brachii strength, significant increases in V̇O2max were also observed following training [122]. These findings have since been confirmed in more recent studies in persons with SCI [123, 124], stimulating interest in the efficacy of resistance training and mixed-modality training protocols for enhancing cardiometabolic biomarkers. Indeed, strength and aerobic improvements can both be obtained using a “circuit resistance training” (CRT, Fig. 2) approach to integrating cardiorespiratory and resistance training exercise [125, 126]. Interestingly, this same circuit protocol was later shown to be effective at improving the atherogenic lipid profile of persons with paraplegia [127]. More recently, this circuit resistance protocol has been adapted for use by persons with tetraplegia, for whom both increased strength and endurance were reported when 6 months of training was accompanied by immediate post-exercise whey protein supplementation [128], a technique used to enhance glycogen replenishment following exercise carbohydrate and amino acid depletion [129]. The circuit resistance training (CRT) protocol has also been made compatible for home and community integration by use of elastic bands [130] and has been recommended by the American Physical Therapy Association as part of their Physical Fitness for Special Populations Program for Individuals with SCI.

Fig. 2
figure2

Images of a participant completing the various elements of the circuit resistance training (CRT) protocol: a arm crank ergometry, b military press, c horizontal row, d pectoralis (“pec”) dec, e preacher curl, f wide grip latissimus pull-down, and g seated dip

To summarize, comprehensive physical activity guidelines to enhance cardiometabolic component risks for persons with SCI were recently updated and published by several authorities [65, 131, 132]. Reassuringly, these latest recommendations have considerable commonality, promoting both cardiorespiratory exercise and resistance exercise training, as well as highlighting the importance of avoiding inactivity. Quite rightly, the Consortium for Spinal Cord Medicine Clinical Practice Guideline [65] emphasizes the importance of higher volumes (150 min per week) and higher frequencies (up to 5 days per week) of exercise for delaying the progression of cardiometabolic disorders. Further research is beginning to demonstrate the benefits for specific forms of higher intensity armcrank ergometry and mixed-mode resistance exercise, and it is likely that these activities will inform the development of future iterations of exercise guidelines. Given the limited impact of upper-body MICT on physiological responses and physical activity energy expenditure, conditioned adults with SCI should be encouraged to accrue their weekly exercise dose by engaging in higher intensity forms of intermittent upper-body exercise (e.g., higher intensity interval training (HIIT)), including continuous resistance training (CRT).

Other Interventions for CMS Risks

Secondary Management: Pharmacotherapy

While comprehensive lifestyle intervention is the primary approach for CMS control, a failure to satisfy targets using the combination of exercise conditioning and nutritional control then defaults to pharmacotherapy as secondary management (Table 5). These approaches address individual risk components of the CMS, and in most instances, selection of a therapeutic agent for the PVA Guideline was made by guideline approaches and good medical practices adopted for the non-disabled population (Table 5). For example, hypertension pharmacotherapy in the PVA Guidelines was based upon the Eighth Joint National Committee (JNC 8) evidence-based guideline for the management of high blood pressure [134]. Control for dysglycemia was consistent with the ADA standards of medical care for type 2 diabetes [133]. The sole area where medicines were not recommended was for treatment of obesity, where available agents have not been systematically tested for safety and tolerance in the SCI population, risks may outweigh potential benefits, and drug interactions with other prescription and non-prescription medicines may be hazardous. The latter was specifically cited for the potential risk of serotonin syndrome

Table 5 Risk targets and first-line recommendations for management of CMS using pharmacotherapy

.

Bariatric Surgery

Bariatric surgery has become a routine, yet still aggressive approach for clinical management of morbid obesity. However, limited study has systematically tested the safety and effectiveness of bariatric surgery in persons with SCI, and while several case reports have described the procedures [135,136,137], inadequate information has documented perioperative or post-operative risks that are unique to the population. Further, guidelines for determining bariatric surgery candidacy in non-disabled individuals have limited relevance for the SCI population [138, 139] and do not address the complex needs/risks including post-operative mobility and activities of daily living deficits. Otherwise, risks of neurogenic bradycardia, neurogenic hypotension, adapted myocardial atrophy, circulatory hypokinesis, autonomic dysreflexia, neurogenic restrictive and obstructive lung disease, neurogenic bladder and bowel, neurogenic skin, sarcopenia, osteopenia/osteoporosis, and spasticity are noted in the PVA Guideline [65].

Conclusions

An alarming number of individuals with SCI develop component risks for CMS at some point within their lifespan, the two most serious of which are sarcopenic obesity and insulin resistance. For many individuals with SCI, exercise offers an effective strategy for attenuation of these risks, with a benefit favored by the adoption of more intensive activity. The value of this exercise in CMS/CVD management may be less useful for individuals with higher levels of injury where functional sympathectomy has been sustained. In these individuals, when combined with balanced, calorie-regulated nutrition, the two modifications constitute a lifestyle intervention that favors a best-practice appropriate for disease management. When lifestyle intervention is ineffective for risk reduction, both pharmacotherapy and bariatric surgery become options for CMS risk abatement, but may also be accompanied by unique risks and variable benefits for the SCI population.

References

  1. 1.

    Despres JP, Lemieux I, Bergeron J, Pibarot P, Mathieu P, Larose E, et al. Abdominal obesity and the metabolic syndrome: contribution to global cardiometabolic risk. Arterioscler Thromb Vasc Biol. 2008;28(6):1039–49.

    CAS  PubMed  Google Scholar 

  2. 2.

    Castro JP, El-Atat FA, McFarlane SI, Aneja A, Sowers JR. Cardiometabolic syndrome: pathophysiology and treatment. Curr Hypertens Rep. 2003;5(5):393–401.

    PubMed  Google Scholar 

  3. 3.

    Mancia G, Bombelli M, Facchetti R, Casati A, Ronchi I, Quarti-Trevano F, et al. Impact of different definitions of the metabolic syndrome on the prevalence of organ damage, cardiometabolic risk and cardiovascular events. J Hypertens. 2010;28(5):999–1006.

    CAS  PubMed  Google Scholar 

  4. 4.

    Beltrán-Sánchez H, Harhay MO, Harhay MM, McElligott S. Prevalence and trends of metabolic syndrome in the adult US population, 1999–2010. J Am Coll Cardiol. 2013;62(8):697–703.

    PubMed  PubMed Central  Google Scholar 

  5. 5.

    Bremer AA, Mietus-Snyder M, Lustig RH. Toward a unifying hypothesis of metabolic syndrome. Pediatrics. 2012;129(3):557–70.

    PubMed  PubMed Central  Google Scholar 

  6. 6.

    Nash MS, Tractenberg RE, Mendez AJ, David M, Ljungberg IH, Tinsley EA, et al. Cardiometabolic syndrome in people with spinal cord injury/disease: guideline-derived and non-guideline risk components in a pooled sample. Arch Phys Med Rehabil. 2016;97:1696–705.

    PubMed  Google Scholar 

  7. 7.

    Weaver FM, Collins EG, Kurichi J, Miskevics S, Smith B, Rajan S, et al. Prevalence of obesity and high blood pressure in veterans with spinal cord injuries and disorders: a retrospective review. Am J Phys Med Rehabil. 2007;86(1):22–9.

    PubMed  Google Scholar 

  8. 8.

    Groah SL, Nash MS, Ljungberg IH, Libin A, Hamm LF, Ward E, et al. Nutrient intake and body habitus after spinal cord injury: an analysis by sex and level of injury. J Spinal Cord Med. 2009;32(1):25–33.

    PubMed  PubMed Central  Google Scholar 

  9. 9.

    Groah SL, Nash MS, Ward EA, Libin A, Mendez AJ, Burns P, et al. Cardiometabolic risk in community-dwelling persons with chronic spinal cord injury. J Cardiopulm Rehabil Prev. 2011;31(2):73–80.

    PubMed  Google Scholar 

  10. 10.

    Pelletier CA, Miyatani M, Giangregorio L, Craven BC. Sarcopenic obesity in adults with chronic spinal cord injury: a cross-sectional study. Arch Phys Med Rehabil. 2016;97:1931–7.

    PubMed  Google Scholar 

  11. 11.

    Gorgey AS, Gater DR Jr. Prevalence of obesity after spinal cord injury.TOP Spinal Cord Inj Rehabil. 2007;12(4):1–7.

    PubMed  PubMed Central  Google Scholar 

  12. 12.

    Buchholz AC, Bugaresti JM. A review of body mass index and waist circumference as markers of obesity and coronary heart disease risk in persons with chronic spinal cord injury. Spinal Cord. 2005;43(9):513–8.

    CAS  PubMed  Google Scholar 

  13. 13.

    Gater DR Jr. Obesity after spinal cord injury. Phys Med Rehabil Clin N Am. 2007;18(2):333–51 vii.

    PubMed  Google Scholar 

  14. 14.

    Nash MS, Gater DR. Exercise to reduce obesity in SCI. Top Spinal Cord Inj Rehabil. 2007;12(4):76–93.

    Google Scholar 

  15. 15.

    Kressler J, Cowan RE, Bigford GE, Nash MS. Reducing cardiometabolic disease in spinal cord injury. Phys Med Rehabil Clin N Am. 2014;25(3):573–604 viii.

    PubMed  Google Scholar 

  16. 16.

    Bauman WA, Spungen AM, Raza M, Rothstein J, Zhang RL, Zhong YG, et al. Coronary artery disease: metabolic risk factors and latent disease in individuals with paraplegia. Mt Sinai J Med. 1992;59(2):163–8.

    CAS  PubMed  Google Scholar 

  17. 17.

    Cowan RE, Nash MS. Cardiovascular disease, SCI and exercise: unique risks and focused countermeasures. Disabil Rehabil. 2010;32(26):2228–36.

    PubMed  Google Scholar 

  18. 18.

    Cowan RE, Nash MS. Cardiovascular disease, SCI and exercise: unique risks and focused countermeasures. 2010;32(26):2228–36.

  19. 19.

    Bauman WA, Spungen AM. Coronary heart disease in individuals with spinal cord injury: assessment of risk factors. Spinal Cord. 2008;46(7):466–76.

    CAS  PubMed  Google Scholar 

  20. 20.

    Banerjea R, Sambamoorthi U, Weaver F, Maney M, Pogach LM, Findley T. Risk of stroke, heart attack, and diabetes complications among veterans with spinal cord injury. Arch Phys Med Rehabil. 2008;89(8):1448–53.

    PubMed  Google Scholar 

  21. 21.

    Nash MS, Cowan RE. Cardiovascular risk and exercise after spinal cord injuries. In: Spinal cord medicine, vol. 2010. New York: Demos Publications; 2010. p. 848–58.

    Google Scholar 

  22. 22.

    Bauman WA, Spungen AM, Zhong YG, Rothstein JL, Petry C, Gordon SK. Depressed serum high density lipoprotein cholesterol levels in veterans with spinal cord injury. Paraplegia. 1992;30(10):697–703.

    CAS  PubMed  Google Scholar 

  23. 23.

    Brenes G, Dearwater S, Shapera R, LaPorte RE, Collins E. High density lipoprotein cholesterol concentrations in physically active and sedentary spinal cord injured patients. Arch Phys Med Rehabil. 1986;67(7):445–50.

    CAS  PubMed  Google Scholar 

  24. 24.

    Nash MS, Mendez AJ. A guideline-driven assessment of need for cardiovascular disease risk intervention in persons with chronic paraplegia. Arch Phys Med Rehabil. 2007;88(6):751–7.

    PubMed  Google Scholar 

  25. 25.

    Bauman WA, Adkins RH, Spungen AM, Herbert R, Schechter C, Smith D, et al. Is immobilization associated with an abnormal lipoprotein profile? Observations from a diverse cohort. Spinal Cord. 1999;37(7):485–93.

    CAS  PubMed  Google Scholar 

  26. 26.

    Bauman WA, Adkins RH, Spungen AM, Kemp BJ, Waters RL. The effect of residual neurological deficit on serum lipoproteins in individuals with chronic spinal cord injury. Spinal Cord. 1998;36(1):13–7.

    CAS  PubMed  Google Scholar 

  27. 27.

    Bauman WA, Spungen AM. Disorders of carbohydrate and lipid metabolism in veterans with paraplegia or quadriplegia: a model of premature aging. Metabolism. 1994;43(6):749–56.

    CAS  PubMed  Google Scholar 

  28. 28.

    Dallmeijer AJ, van der Woude LH, van Kamp GJ, Hollander AP. Changes in lipid, lipoprotein and apolipoprotein profiles in persons with spinal cord injuries during the first 2 years post-injury. Spinal Cord. 1999;37(2):96–102.

    CAS  PubMed  Google Scholar 

  29. 29.

    Spungen AM, Wang J, Pierson RN, Bauman WA. Soft tissue body composition differences in monozygotic twins discordant for spinal cord injury. J Appl Physiol. 2000;88(4):1310–5.

    CAS  PubMed  Google Scholar 

  30. 30.

    Buchholz AC, Pencharz PB. Energy expenditure in chronic spinal cord injury. Curr Opin Clin Nutr Metab Care. 2004;7(6):635–9.

    PubMed  Google Scholar 

  31. 31.

    Monroe MB, Tataranni PA, Pratley R, Manore MM, Skinner JS, Ravussin E. Lower daily energy expenditure as measured by a respiratory chamber in subjects with spinal cord injury compared with control subjects. Am J Clin Nutr. 1998;68(6):1223–7.

    CAS  PubMed  Google Scholar 

  32. 32.

    Emmons RR, Garber CE, Cirnigliaro CM, Kirshblum SC, Spungen AM, Bauman WA. Assessment of measures for abdominal adiposity in persons with spinal cord injury. Ultrasound Med Biol. 2011;37(5):734–41.

    PubMed  Google Scholar 

  33. 33.

    Inskip J, Plunet W, Ramer L, Ramsey JB, Yung A, Kozlowski P, et al. Cardiometabolic risk factors in experimental spinal cord injury. J Neurotrauma. 2010;27(1):275–85.

    PubMed  Google Scholar 

  34. 34.

    Nash MS, Cowan RE, Kressler J. Evidence-based and heuristic approaches for customization of care in cardiometabolic syndrome after spinal cord injury. J Spinal Cord Med. 2012;35(5):278–92.

    PubMed  PubMed Central  Google Scholar 

  35. 35.

    Levine AM, Nash MS, Green BA, Shea JD, Aronica MJ. An examination of dietary intakes and nutritional status of chronic healthy spinal cord injured individuals. Paraplegia. 1992;30(12):880–9.

    CAS  PubMed  Google Scholar 

  36. 36.

    Dearwater SR, LaPorte RE, Robertson RJ, Brenes G, Adams LL, Becker D. Activity in the spinal cord-injured patient: an epidemiologic analysis of metabolic parameters. Med Sci Sports Exerc. 1986;18(5):541–4.

    CAS  PubMed  Google Scholar 

  37. 37.

    LaPorte RE, Adams LL, Savage DD, Brenes G, Dearwater S, Cook T. The spectrum of physical activity, cardiovascular disease and health: an epidemiologic perspective. Am J Epidemiol. 1984;120(4):507–17.

    CAS  PubMed  Google Scholar 

  38. 38.

    LaPorte RE, Brenes G, Dearwater S, Murphy MA, Cauley JA, Dietrick R, et al. HDL cholesterol across a spectrum of physical activity from quadriplegia to marathon running. Lancet. 1983;1(8335):1212–3.

    CAS  PubMed  Google Scholar 

  39. 39.

    Zlotolow SP, Levy E, Bauman WA. The serum lipoprotein profile in veterans with paraplegia: the relationship to nutritional factors and body mass index. J Am Paraplegia Soc. 1992;15(3):158–62.

    CAS  PubMed  Google Scholar 

  40. 40.

    Halle M, Berg A, Baumstark M, Keul J. Association of physical fitness with LDL and HDL subfractions in young healthy men. Int J Sports Med. 1999;20(7):464–9.

    CAS  PubMed  Google Scholar 

  41. 41.

    Franks PW, Ekelund U, Brage S, Wong M-Y, Wareham NJ. Does the association of habitual physical activity with the metabolic syndrome differ by level of cardiorespiratory fitness? Diabetes Care. 2004;27(5):1187–93.

    PubMed  Google Scholar 

  42. 42.

    Carnethon MR, Gulati M, Greenland P. Prevalence and cardiovascular disease correlates of low cardiorespiratory fitness in adolescents and adults. Jama. 2005;294(23):2981–8.

    CAS  PubMed  Google Scholar 

  43. 43.

    Cowan RE, Nash MS, Anderson KD. Exercise participation barrier prevalence and association with exercise participation status in individuals with spinal cord injury. Spinal Cord. 2013;51(1):27–32.

    CAS  PubMed  Google Scholar 

  44. 44.

    Ginis KA, Latimer AE, Arbour-Nicitopoulos KP, Buchholz AC, Bray SR, Craven BC, et al. Leisure time physical activity in a population-based sample of people with spinal cord injury part I: demographic and injury-related correlates. Arch Phys Med Rehabil. 2010;91(5):722–8.

    PubMed  Google Scholar 

  45. 45.

    Scelza WM, Kalpakjian CZ, Zemper ED, Tate DG. Perceived barriers to exercise in people with spinal cord injury. Am J Phys Med Rehabil. 2005;84(8):576–83.

    PubMed  Google Scholar 

  46. 46.

    Vissers M, van den Berg-Emons R, Sluis T, Bergen M, Stam H, Bussmann H. Barriers to and facilitators of everyday physical activity in persons with a spinal cord injury after discharge from the rehabilitation centre. J Rehabil Med. 2008;40(6):461–7.

    PubMed  Google Scholar 

  47. 47.

    Cowan RE, Nash MS, Anderson KD. Exercise participation barrier prevalence and association with exercise participation status in individuals with spinal cord injury. Spinal Cord. 2013;51(1):27–32.

    PubMed  Google Scholar 

  48. 48.

    Liu L, Nunez AE. Cardiometabolic syndrome and its association with education, smoking, diet, physical activity, and social support: findings from the Pennsylvania 2007 BRFSS Survey. J Clin Hypertens. 2010;12(7):556–64.

    Google Scholar 

  49. 49.

    Feasel SGS. The impact of diet on cardiovascular disease risk in individuals with spinal cord injury. Top Spinal Cord Inj Rehabil. 2009;14(3):56–68.

    Google Scholar 

  50. 50.

    U.S. Department of Agriculture and U.S. Department of Health and Human Services. Dietary guidelines for Americans. 7th ed. Washington, DC: Government Printing Office; 2010. p. 112.

    Google Scholar 

  51. 51.

    Walters JL, Buchholz AC, Martin Ginis KA. Evidence of dietary inadequacy in adults with chronic spinal cord injury. Spinal Cord. 2009;47(4):318–22.

    CAS  PubMed  Google Scholar 

  52. 52.

    Perret C, Stoffel-Kurt N. Comparison of nutritional intake between individuals with acute and chronic spinal cord injury. J Spinal Cord Med. 2011;34(6):569–75.

    PubMed  PubMed Central  Google Scholar 

  53. 53.

    Aquilani R, Boschi F, Contardi A, Pistarini C, Achilli MP, Fizzotti G, et al. Energy expenditure and nutritional adequacy of rehabilitation paraplegics with asymptomatic bacteriuria and pressure sores. Spinal Cord. 2001;39(8):437–41.

    CAS  PubMed  Google Scholar 

  54. 54.

    Lee BY, Agarwal N, Corcoran L, Thoden WR, Del Guercio LR. Assessment of nutritional and metabolic status of paraplegics. J Rehabil Res Dev. 1985;22(3):11–7.

    CAS  PubMed  Google Scholar 

  55. 55.

    Bigford GE, Brooks L, Burns-Drecq P, Kappy C, Kreger K, Munoz R, et al. A populationrelevant lifestyle-intensive intervention for diabetes prevention after SCI. Top Spinal Cord Inj Rehabil. 2013:1.

  56. 56.

    Bigford GE, Brooks L, Burns-Drecq P, Kappy C, Kreger K, Munoz R, et al. Therapeutic lifestyle intervention after paraplegia significantly reduces component markers of cardiometabolic risk. Top Spinal Cord Inj Rehabil. 2014;20(S1):43.

    Google Scholar 

  57. 57.

    Tomey KM, Chen DM, Wang X, Braunschweig CL. Dietary intake and nutritional status of urban community-dwelling men with paraplegia. Arch Phys Med Rehabil. 2005;86(4):664–71.

    PubMed  Google Scholar 

  58. 58.

    Sabour H, Javidan AN, Vafa MR, Shidfar F, Nazari M, Saberi H, et al. Calorie and macronutrients intake in people with spinal cord injuries: an analysis by sex and injury-related variables. Nutrition. 2012;28(2):143–7.

    CAS  PubMed  Google Scholar 

  59. 59.

    Moussavi RM, Ribas-Cardus F, Rintala DH, Rodriguez GP. Dietary and serum lipids in individuals with spinal cord injury living in the community. J Rehabil Res Dev. 2001;38(2):225–33.

    CAS  PubMed  Google Scholar 

  60. 60.

    Hooper L, Summerbell CD, Thompson R, Sills D, Roberts FG, Moore HJ, et al. Reduced or modified dietary fat for preventing cardiovascular disease. Cochrane Database Syst Rev. 2012;5:CD002137.

    Google Scholar 

  61. 61.

    Schrauwen P, Westerterp KR. The role of high-fat diets and physical activity in the regulation of body weight. Br J Nutr. 2000;84(4):417–27.

    CAS  PubMed  Google Scholar 

  62. 62.

    Nash MS, DeGroot J, Martinez-Arizala A, Mendez AJ. Evidence for an exaggerated postprandial lipemia in chronic paraplegia. J Spinal Cord Med. 2005;28(4):320–5.

    PubMed  PubMed Central  Google Scholar 

  63. 63.

    Emmons RR, Garber CE, Cirnigliaro CM, Moyer JM, Kirshblum SC, Galea MD, et al. The influence of visceral fat on the postprandial lipemic response in men with paraplegia. J Am Coll Nutr. 2010;29(5):476–81.

    CAS  PubMed  Google Scholar 

  64. 64.

    Ellenbroek D, Kressler J, Cowan RE, Burns PA, Mendez AJ, Nash MS. Effects of prandial challenge on triglyceridemia, glycemia, and pro-inflammatory activity in persons with chronic paraplegia. J Spinal Cord Med. 2015;38(4):468–75.

    PubMed  Google Scholar 

  65. 65.

    Identification and management of cardiometabolic risk after spinal cord injury—clinical practice guideline for health care providers, 2018. 201. Available from: https://www.pva.org/CMSPages/GetFile.aspx?guid=f3c29b7e-e201-4392-b241-9933dc620e40.

  66. 66.

    Noreau L, Shephard RJ, Simard C, Pare G, Pomerleau P. Relationship of impairment and functional ability to habitual activity and fitness following spinal cord injury. Int J Rehabil Res. 1993;16(4):265–75.

    CAS  PubMed  Google Scholar 

  67. 67.

    Boninger ML, Dicianno BE, Cooper RA, Towers JD, Koontz AM, Souza AL. Shoulder magnetic resonance imaging abnormalities, wheelchair propulsion, and gender. Arch Phys Med Rehabil. 2003;84(11):1615–20.

    PubMed  Google Scholar 

  68. 68.

    Ballinger DA, Rintala DH, Hart KA. The relation of shoulder pain and range-of-motion problems to functional limitations, disability, and perceived health of men with spinal cord injury: a multifaceted longitudinal study. Arch Phys Med Rehabil. 2000;81(12):1575–81.

    CAS  PubMed  Google Scholar 

  69. 69.

    Cowan RE, Nash MS, Anderson-Erisman K. Perceived exercise barriers and odds of exercise participation among persons with SCI living in high-income households. Top Spinal Cord Inj Rehabil. 2012;18(2):126–7.

    PubMed  Google Scholar 

  70. 70.

    Kroll T, Kratz A, Kehn M, Jensen MP, Groah S, Ljungberg IH, et al. Perceived exercise self-efficacy as a predictor of exercise behavior in individuals aging with spinal cord injury. Am J Phys Med Rehabil. 2012;91(8):640–51.

    PubMed  Google Scholar 

  71. 71.

    The Diabetes Prevention Program (DPP). Description of lifestyle intervention. Diabetes Care. 2002;25(12):2165–71.

    Google Scholar 

  72. 72.

    Rubin RR, Fujimoto WY, Marrero DG, Brenneman T, Charleston JB, Edelstein SL, et al. The diabetes prevention program: recruitment methods and results. Control Clin Trials. 2002;23(2):157–71.

    PubMed  Google Scholar 

  73. 73.

    Moore TJ, Alsabeeh N, Apovian CM, Murphy MC, Coffman GA, Cullum-Dugan D, et al. Weight, blood pressure, and dietary benefits after 12 months of a web-based nutrition education program (DASH for health): longitudinal observational study. J Med Internet Res. 2008;10(4):e52.

    PubMed  PubMed Central  Google Scholar 

  74. 74.

    Steinberg D, Bennett GG, Svetkey L. The DASH diet, 20 years later. Jama. 2017;317(15):1529–30.

    PubMed  PubMed Central  Google Scholar 

  75. 75.

    Bauman WA, Zhong YG, Schwartz E. Vitamin D deficiency in veterans with chronic spinal cord injury. Metabolism. 1995;44(12):1612–6.

    CAS  PubMed  Google Scholar 

  76. 76.

    Chen Y, Henson S, Jackson AB, Richards JS. Obesity intervention in persons with spinal cord injury. Spinal Cord. 2006;44(2):82–91.

    CAS  PubMed  Google Scholar 

  77. 77.

    Garshick E, Kelley A, Cohen SA, Garrison A, Tun CG, Gagnon D, et al. A prospective assessment of mortality in chronic spinal cord injury. Spinal Cord. 2005;43(7):408–16.

    CAS  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Lai YJ, Lin CL, Chang YJ, Lin MC, Lee ST, Sung FC, et al. Spinal cord injury increases the risk of type 2 diabetes: a population-based cohort study. Spine J. 2014;14(9):1957–64.

    PubMed  Google Scholar 

  79. 79.

    Booth FW, Gordon SE, Carlson CJ, Hamilton MT. Waging war on modern chronic diseases: primary prevention through exercise biology. J Appl Physiol (1985). 2000;88(2):774–87.

    CAS  Google Scholar 

  80. 80.

    Kesaniemi YK, Danforth E Jr, Jensen MD, Kopelman PG, Lefebvre P, Reeder BA. Dose-response issues concerning physical activity and health: an evidence-based symposium. Med Sci Sports Exerc. 2001;33(6 Suppl):S351–8.

    CAS  PubMed  Google Scholar 

  81. 81.

    Haskell WL, Lee IM, Pate RR, Powell KE, Blair SN, Franklin BA, et al. Physical activity and public health: updated recommendation for adults from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc. 2007;39(8):1423–34.

    Google Scholar 

  82. 82.

    Rimmer JH, Schiller W, Chen MD. Effects of disability-associated low energy expenditure deconditioning syndrome. Exerc Sport Sci Rev. 2012;40(1):22–9.

    PubMed  Google Scholar 

  83. 83.

    Wilmet E, Ismail AA, Heilporn A, Welraeds D, Bergmann P. Longitudinal study of the bone mineral content and of soft tissue composition after spinal cord section. Paraplegia. 1995;33(11):674–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  84. 84.

    Liusuwan A, Widman L, Abresch RT, McDonald CM. Altered body composition affects resting energy expenditure and interpretation of body mass index in children with spinal cord injury. J Spinal Cord Med. 2004;27(Suppl 1):24–8.

    Google Scholar 

  85. 85.

    Nightingale TE, Williams S, Thompson D, Bilzon JLJ. Energy balance components in persons with paraplegia: daily variation and appropriate measurement duration. Int J Behav Nutr Phys Act. 2017;14(1):132.

    PubMed  PubMed Central  Google Scholar 

  86. 86.

    Washburn RA, Zhu W, McAuley E, Frogley M, Figoni SF. The physical activity scale for individuals with physical disabilities: development and evaluation. Arch Phys Med Rehabil. 2002;83(2):193–200.

    PubMed  Google Scholar 

  87. 87.

    Ginis KA, Arbour-Nicitopoulos KP, Latimer AE, Buchholz AC, Bray SR, Craven BC, et al. Leisure time physical activity in a population-based sample of people with spinal cord injury. Part II: activity types, intensities, and durations. Arch Phys Med Rehabil. 2010;91(5):729–33.

    PubMed  Google Scholar 

  88. 88.

    Tanhoffer RA, Tanhoffer AI, Raymond J, Johnson NA, Hills AP, Davis GM. Energy expenditure in individuals with spinal cord injury quantified by doubly labeled water and a multi-sensor armband. J Phys Act Health. 2015;12(2):163–70.

    PubMed  Google Scholar 

  89. 89.

    Tanhoffer RA, Tanhoffer AI, Raymond J, Hills AP, Davis GM. Exercise, energy expenditure, and body composition in people with spinal cord injury. J Phys Act Health. 2014;11(7):1393–400.

    PubMed  Google Scholar 

  90. 90.

    Blair SN. Physical inactivity: the biggest public health problem of the 21st century. Br J Sports Med. 2009;43(1):1–2.

    PubMed  Google Scholar 

  91. 91.

    Thyfault JP, Krogh-Madsen R. Metabolic disruptions induced by reduced ambulatory activity in free-living humans. J Appl Physiol (1985). 2011;111(4):1218–24.

    CAS  Google Scholar 

  92. 92.

    Washburn RA, Figoni SF. High density lipoprotein cholesterol in individuals with spinal cord injury: the potential role of physical activity. Spinal Cord. 1999;37(10):685–95.

    CAS  PubMed  Google Scholar 

  93. 93.

    Simmons OL, Kressler J, Nash MS. Reference fitness values in the untrained spinal cord injury population. Arch Phys Med Rehabil. 2014;95(12):2272–8.

    PubMed  Google Scholar 

  94. 94.

    World Health Organization. Global recommendations on physical activity for health. World Health Organization, 2010.

  95. 95.

    Warburton DE, Charlesworth S, Ivey A, Nettlefold L, Bredin SS. A systematic review of the evidence for Canada’s physical activity guidelines for adults. Int J Behav Nutr Phys Act. 2010;7(1):39.

    PubMed  PubMed Central  Google Scholar 

  96. 96.

    Requejo PS, Mulroy SJ, Haubert LL, Newsam CJ, Gronley JK, Perry J. Evidence-based strategies to preserve shoulder function in manual wheelchair users with spinal cord injury. Top Spinal Cord Inj Rehabil. 2008;13(4):86–119.

    Google Scholar 

  97. 97.

    Byrne D, Salzberg C. Major risk factors for pressure ulcers in the spinal cord disabled: a literature review. Spinal Cord. 1996;34(5):255–63.

    CAS  PubMed  Google Scholar 

  98. 98.

    Krassioukov A, Biering-Sørensen F, Donovan W, Kennelly M, Kirshblum S, Krogh K, et al. International standards to document remaining autonomic function after spinal cord injury. J Spinal Cord Med. 2012;35(4):201–10.

    PubMed  PubMed Central  Google Scholar 

  99. 99.

    Griggs KE, Price MJ, Goosey-Tolfrey VL. Cooling athletes with a spinal cord injury. Sports Med. 2015;45(1):9–21.

    PubMed  Google Scholar 

  100. 100.

    Rimmer JH, Riley B, Wang E, Rauworth A, Jurkowski J. Physical activity participation among persons with disabilities: barriers and facilitators. Am J Prev Med. 2004;26(5):419–25.

    PubMed  Google Scholar 

  101. 101.

    Carlson KF, Wilt TJ, Taylor BC, Goldish GD, Niewoehner CB, Shamliyan TA, et al. Effect of exercise on disorders of carbohydrate and lipid metabolism in adults with traumatic spinal cord injury: systematic review of the evidence. J Spinal Cord Med. 2009;32(4):361–78.

    PubMed  PubMed Central  Google Scholar 

  102. 102.

    Ginis KA, Hicks AL, Latimer AE, Warburton DE, Bourne C, Ditor DS, et al. The development of evidence-informed physical activity guidelines for adults with spinal cord injury. Spinal Cord. 2011;49(11):1088–96.

    PubMed  Google Scholar 

  103. 103.

    Cowell LL, Squires WG, Raven PB. Benefits of aerobic exercise for the paraplegic: a brief review. Med Sci Sports Exerc. 1986;18(5):501–8.

    CAS  PubMed  Google Scholar 

  104. 104.

    Hooker SP, Wells CL. Effects of low- and moderate-intensity training in spinal cord-injured persons. Med Sci Sports Exerc. 1989;21(1):18–22.

    CAS  PubMed  Google Scholar 

  105. 105.

    Nightingale TE, Walhin J-P, Thompson D, Bilzon JL. Impact of exercise on cardiometabolic component risks in spinal cord-injured humans. Med Sci Sports Exerc. 2017;49(12):2469–77.

    PubMed  PubMed Central  Google Scholar 

  106. 106.

    de Zepetnek JOT, Pelletier CA, Hicks AL, MacDonald MJ. Following the physical activity guidelines for adults with spinal cord injury for 16 weeks does not improve vascular health: a randomized controlled trial. Arch Phys Med Rehabil. 2015;96(9):1566–75.

    Google Scholar 

  107. 107.

    DiCarlo SE. Effect of arm ergometry training on wheelchair propulsion endurance of individuals with quadriplegia. Phys Ther. 1988;68(1):40–4.

    CAS  PubMed  Google Scholar 

  108. 108.

    Drory Y, Ohry A, Brooks ME, Dolphin D, Kellermann JJ. Armcrank ergometry in chronic spinal cord injured patients. Arch Phys Med Rehabil. 1990;71(6):389–92.

    CAS  PubMed  Google Scholar 

  109. 109.

    Nightingale TE, Metcalfe RS, Vollaard NB, Bilzon JL. Exercise guidelines to promote cardiometabolic health in spinal cord injured humans: time to raise the intensity? Arch Phys Med Rehabil. 2017;98(8):1693–704.

    PubMed  Google Scholar 

  110. 110.

    Moholdt T, Wisløff U, Nilsen TIL, Slørdahl SA. Physical activity and mortality in men and women with coronary heart disease: a prospective population-based cohort study in Norway (the HUNT study). Eur J Cardiovasc Prev Rehabil. 2008;15(6):639–45.

    PubMed  Google Scholar 

  111. 111.

    Wisløff U, Nilsen TI, Drøyvold WB, Mørkved S, Slørdahl SA, Vatten LJ. A single weekly bout of exercise may reduce cardiovascular mortality: how little pain for cardiac gain? ‘The HUNT study, Norway’. Eur J Cardiovasc Prev Rehabil. 2006;13(5):798–804.

    PubMed  Google Scholar 

  112. 112.

    Wen CP, Wai JPM, Tsai MK, Yang YC, Cheng TYD, Lee M-C, et al. Minimum amount of physical activity for reduced mortality and extended life expectancy: a prospective cohort study. Lancet. 2011;378(9798):1244–53.

    PubMed  Google Scholar 

  113. 113.

    Gebel K, Ding D, Chey T, Stamatakis E, Brown WJ, Bauman AE. Effect of moderate to vigorous physical activity on all-cause mortality in middle-aged and older Australians. JAMA Intern Med. 2015;175(6):970–7.

    PubMed  Google Scholar 

  114. 114.

    Samitz G, Egger M, Zwahlen M. Domains of physical activity and all-cause mortality: systematic review and dose–response meta-analysis of cohort studies. Int J Epidemiol. 2011;40(5):1382–400.

    PubMed  Google Scholar 

  115. 115.

    MacInnis MJ, Zacharewicz E, Martin BJ, Haikalis ME, Skelly LE, Tarnopolsky MA, et al. Superior mitochondrial adaptations in human skeletal muscle after interval compared to continuous single-leg cycling matched for total work. J Physiol. 2017;595(9):2955–68.

    CAS  PubMed  Google Scholar 

  116. 116.

    Ramos JS, Dalleck LC, Tjonna AE, Beetham KS, Coombes JS. The impact of high-intensity interval training versus moderate-intensity continuous training on vascular function: a systematic review and meta-analysis. Sports Med. 2015;45(5):679–92.

    Google Scholar 

  117. 117.

    Jelleyman C, Yates T, O'Donovan G, Gray LJ, King JA, Khunti K, et al. The effects of high-intensity interval training on glucose regulation and insulin resistance: a meta-analysis. Obes Rev. 2015;16(11):942–61.

    CAS  PubMed  Google Scholar 

  118. 118.

    Weston KS, Wisløff U, Coombes JS. High-intensity interval training in patients with lifestyle-induced cardiometabolic disease: a systematic review and meta-analysis. Br J Sports Med. 2014;48(16):1227–34.

    PubMed  Google Scholar 

  119. 119.

    Astorino TA, Thum JS. Within-session responses to high-intensity interval training in spinal cord injury. Disabil Rehabil. 2018;40(4):444–9.

    PubMed  Google Scholar 

  120. 120.

    McMillan DWMJ, Jacobs KA, Mendez AJ, Nash MS, Bilzon JLJ. Influence of upper-body continuous, resistance or high intensity interval training (CRIT) on postprandial responses in persons with spinal cord injury: Study protocol for a randomised controlled trial. Trials (under review). 2018.

  121. 121.

    Nash MS, van de Ven I, van Elk N, Johnson BM. Effects of circuit resistance training on fitness attributes and upper-extremity pain in middle-aged men with paraplegia. Arch Phys Med Rehabil. 2007;88(1):70–5.

    PubMed  Google Scholar 

  122. 122.

    Nilsson S, Staff PH, Pruett ED. Physical work capacity and the effect of training on subjects with long- standing paraplegia. Scand J Rehabil Med. 1975;7(2):51–6.

    CAS  PubMed  Google Scholar 

  123. 123.

    Cooney MM, Walker JB. Hydraulic resistance exercise benefits cardiovascular fitness of spinal cord injured. Med Sci Sports Exerc. 1986;18(5):522–5.

    CAS  PubMed  Google Scholar 

  124. 124.

    Olenik LM, Laskin JJ, Burnham R, Wheeler GD, Steadward RD. Efficacy of rowing, backward wheeling and isolated scapular retractor exercise as remedial strength activities for wheelchair users: application of electromyography. Paraplegia. 1995;33(3):148–52.

    CAS  PubMed  Google Scholar 

  125. 125.

    Jacobs PL, Nash MS, Rusinowski JW. Circuit training provides cardiorespiratory and strength benefits in persons with paraplegia. Med Sci Sports Exerc. 2001;33(5):711–7.

    CAS  PubMed  Google Scholar 

  126. 126.

    Jacobs PL, Mahoney ET, Nash MS, Green BA. Circuit resistance training in persons with complete paraplegia. J Rehabil Res Dev. 2002;39(1):21–8.

    PubMed  Google Scholar 

  127. 127.

    Nash MS, Jacobs PL, Mendez AJ, Goldberg RB. Circuit resistance training improves the atherogenic lipid profiles of persons with chronic paraplegia. J Spinal Cord Med. 2001;24(1):2–9.

    CAS  PubMed  Google Scholar 

  128. 128.

    Kressler J, Burns PA, Betancourt L, Nash MS. Circuit training and protein supplementation in persons with chronic tetraplegia. Med Sci Sports Exerc. 2014;46(7):1277–84.

    CAS  Google Scholar 

  129. 129.

    Kerksick CM, Rasmussen CJ, Lancaster SL, Magu B, Smith P, Melton C, et al. The effects of protein and amino acid supplementation on performance and training adaptations during ten weeks of resistance training. J Strength Cond Res. 2006;20(3):643–53.

    PubMed  Google Scholar 

  130. 130.

    Nash MS, Jacobs PL, Woods JM, Clark JE, Pray TA, Pumarejo AE. A comparison of 2 circuit exercise training techniques for eliciting matched metabolic responses in persons with paraplegia. Arch Phys Med Rehabil. 2002;83(2):201–9.

    PubMed  Google Scholar 

  131. 131.

    Ginis KAM, van der Scheer JW, Latimer-Cheung AE, Barrow A, Bourne C, Carruthers P, et al. Evidence-based scientific exercise guidelines for adults with spinal cord injury: an update and a new guideline. Spinal Cord. 2018;56(4):308–21.

    Google Scholar 

  132. 132.

    van der Scheer JW, Ginis KAM, Ditor DS, Goosey-Tolfrey VL, Hicks AL, West CR, et al. Effects of exercise on fitness and health of adults with spinal cord injury: a systematic review. Neurology. 2017;89(7):736–45.

    PubMed  Google Scholar 

  133. 133.

    Chamberlain JJ, Herman WH, Leal S, Rhinehart AS, Shubrook JH, Skolnik N, et al. Pharmacologic therapy for type 2 diabetes: synopsis of the 2017 American Diabetes Association Standards of Medical Care in Diabetes Pharmacologic Therapy for Type 2 Diabetes. Ann Intern Med. 2017;166(8):572–8.

    PubMed  Google Scholar 

  134. 134.

    James PA, Oparil S, Carter BL, Cushman WC, Dennison-Himmelfarb C, Handler J, et al. 2014 evidence-based guideline for the management of high blood pressure in adults: report from the panel members appointed to the Eighth Joint National Committee (JNC 8). Jama. 2014;311(5):507–20.

    CAS  PubMed  Google Scholar 

  135. 135.

    Alaedeen DI, Jasper J. Gastric bypass surgery in a paraplegic morbidly obese patient. Obes Surg. 2006;16(8):1107–8.

    PubMed  Google Scholar 

  136. 136.

    Williams G, Georgiou P, Cocker D, Bonanomi G, Smellie J, Efthimiou E. The safety and efficacy of bariatric surgery for obese, wheelchair bound patients. Ann R Coll Surg Engl. 2014;96(5):373–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  137. 137.

    Wong S, Barnes T, Coggrave M, Forbes A, Pounds-Cornish E, Appleton S, et al. Morbid obesity after spinal cord injury: an ailment not to be treated? Eur J Clin Nutr. 2013;67(9):998–9.

    CAS  PubMed  Google Scholar 

  138. 138.

    Fried M, Yumuk V, Oppert J, Scopinaro N, Torres A, Weiner R, et al. Interdisciplinary European guidelines on metabolic and bariatric surgery. Obes Surg. 2014;24(1):42–55.

    CAS  PubMed  Google Scholar 

  139. 139.

    Mechanick JI, Youdim A, Jones DB, Garvey WT, Hurley DL, McMahon MM, et al. Clinical practice guidelines for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient—2013 update: cosponsored by American Association of Clinical Endocrinologists, the Obesity Society, and American Society for Metabolic & Bariatric Surgery. Obesity. 2013;21:S1.

    CAS  PubMed  Google Scholar 

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Nash, M.S., Bilzon, J.L.J. Guideline Approaches for Cardioendocrine Disease Surveillance and Treatment Following Spinal Cord Injury. Curr Phys Med Rehabil Rep 6, 264–276 (2018). https://doi.org/10.1007/s40141-018-0203-z

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Keywords

  • Cardioendocrine disease
  • Spinal cord injury
  • Nutrition
  • Exercise
  • Physical activity
  • Pharmacotherapy
  • Bariatrics