Volume 41 Number 1, January/February 2004
Pages 1 — 8
The relationship between energy expenditure and lean tissue in monozygotic twins discordant for spinal cord injury
William A. Bauman, MD; Ann M. Spungen, EdD; Jack Wang, MS; Richard N. Pierson, Jr, MD
Department of Veterans Affairs (VA) Rehabilitation Research and Development Center of Excellence, Spinal Cord Damage Research Center, and Medical, Spinal Cord Injury, and Research Services, VA Medical Center, Bronx, NY; Departments of Medicine and Rehabilitation Medicine, Mount Sinai Medical Center, New York, NY; Body
Composition Unit, Columbia University-St. Luke's/Roosevelt Hospital Center, New York, NYAbstract — Energy expenditure and fat-free mass (FFM), as well as the relationships between these parameters, were investigated in thirteen pairs of monozygotic twins discordant for SCI. Basal energy expenditure (BEE) and resting energy expenditure (REE) were determined by indirect calorimetry. Measurements for FFM and fat mass were obtained by dual-energy x-ray absorptiometry. Total body potassium was determined by a 4-Pi whole-body counting chamber. Values are expressed as mean ± standard deviation. BEE and REE of the twins with SCI were significantly less than those of the able-bodied co-twins (1387 ± 268 vs. 1660 ± 324 kcal/d, p < 0.005, and 1682 ± 388 vs. 1854 ± 376 kcal/d, p < 0.05, respectively). Regardless of the group, direct and highly significant relationships were evident between BEE or REE and FFM or TBK. In summary, twins with SCI had lower energy expenditure than their able-bodied co-twins. Regardless of paralysis, direct linear relationships existed between energy expenditure and measures of lean mass.Key words: energy expenditure, fat-free mass, paraplegia, spinal cord injury, total body potassium.
Abbreviations: BCM = body cell mass, BEE = basal energy expenditure, DXA = dual-energy x-ray absorptiometry, FECO2 = fraction of mixed expired carbon dioxide, FEO2 = fraction of mixed expired oxygen, FFM = fat-free mass, FM = fat mass, IGF-I = insulin-like growth factor-I, IPD = intrapair difference, pBEE = predicted basal energy expenditure, REE = resting energy expenditure, SCI = spinal cord injury, SD = standard deviation, TBK = total body potassium, VCO2 = carbon dioxide production, VO2 = oxygen consumption.This material was based on work supported in part by the Spinal Cord Research Foundation (SCRF), the Eastern Paralyzed Veterans Association (EPVA), the Bronx Department of Veterans Affairs Medical Center, and the Mount Sinai School of Medicine.Address all correspondence to William A. Bauman, MD, Professor of Medicine; Director, Spinal Cord Damage Research Center, Room 1E-02, VA Medical Center, 130 West Kingsbridge Road, Bronx, NY 10468; 718-584-9000, ext. 5428; fax: 718-733-5291; email: wabauman@earthlink.net.INTRODUCTIONPersons with chronic spinal cord injury (SCI) have been reported to have a reduction in metabolic rate [1,2]. Lean tissue is the most metabolically active body tissue, and muscle mass, a predominant component of lean tissue, appears to be lost over time in those with SCI at a rate exceeding that of the able-bodied population [3,4]. The loss of lean tissue and associated energy expenditure changes in persons with chronic SCI would be expected to have profound implications on carbohydrate and lipid metabolism, as well as an impact on cardiovascular risk [5-8]. The ability to gauge accurately the reduction in energy expenditure in a person with chronic paraplegia is limited because of the relatively large variance in energy requirements known to be present in the general population. With the use of a monozygotic twin model discordant for SCI, an indirect but fairly convincing appraisal of the individual reductions in energy expenditure and losses of lean body tissue, as well as their interrelationships, may be assessed.
METHODSSubjectsThirteen pairs of monozygotic twins discordant for SCI were recruited by referral from their physicians for study (Table 1). Nine pairs were males and four were females (Table 2). Of the co-twins with SCI, 11 had paraplegia and 2 had tetraplegia; all were nonambulatory. The twins with SCI were in good health without comorbidities at the time of study. The duration of injury ranged from 3 to 26 years (Table 2). Genetic testing for zygosity was performed in all pairs at six independent, highly polymorphic loci (Lifecodes, Stamford, CT). All 13 pairs were found to be strongly consistent with monozygosity, with a probability of being nonidentical of 1 in 4,096. Institutional Review Board approvals from the Veterans Affairs Medical Center, Bronx, NY, and the Mount Sinai School of Medicine, New York, NY, were obtained before the study began. The subjects were provided with verbal and written information about the study, and written consent was obtained.
Energy ExpenditureOxygen consumption (VO2) and carbon dioxide production (VCO2) were measured via indirect calorimetry with the use of a mixing chamber with dilution technology [9]. A metabolic cart (SensorMedics Corp., Yorba Linda, CA) was used to measure indirect calorimetry by analyzing the exhaled air from the subject for fractions of mixed expired oxygen and carbon dioxide (FEO2 and FECO2, respectively). Before each patient was tested, barometric pressure was measured and the metabolic cart calibrated. The dilution technique involves the use of a high-flow pump to draw air past the face of the subject through a loose-fitting mask [9]. As the subject breathed into this stream of air, the exhaled air was pulled into a 7 L mixing chamber. The total minute ventilation was set by the flow rate for the pump, which was governed by the fraction of carbon dioxide in the expired air. The ratio of room air to expired air was approximately 4:1; this ratio allowed for an FECO2 of 0.005 to 0.01 under normal resting breathing conditions. Although the pump was designed to adjust automatically for hyperventilation and hypoventilation, all subjects were rested for a minimum of 30 min and instructed to remain calm before and during data collection.
Basal energy expenditure (BEE), by our definition, was the energy expended by an individual when initially waking in the morning while lying supine in bed at normal body and ambient temperatures after at least a 12 h fast. Resting energy expenditure (REE) was defined as the energy expended by an individual when seated at least 4 h post-prandial at normal body and ambient temperatures. Predicted basal energy expenditure (pBEE) was determined by the Harris-Benedict equations [10]. The percentage of predicted energy expenditure (%pEE) was calculated as follows: %pEE = measured EE (mEE)/pEE × 100. All data were collected in a steady-state condition, defined as less than ±5-percent fluctuation in VO2 and VCO2 for 5 consecutive minutes. Equations for the following are as referenced: minute ventilation [11], VO2 (mL/min) [12], VCO2 (mL/min) [12], BEE (kcal/d) [13], REE (kcal/d) [13], pBEE (kcal/d) [10].
Body CompositionDual-energy x-ray absorptiometry (DXA) was used to determine fat-free mass (FFM) (kg), including bone. DXA was performed using a total-body scanner (model DPX, Lunar Radiation, Madison, WI) by standard methods [14-17]. The subjects were asked to lie on a table, and whole-body scanning was performed with a congruent beam of stable dual-energy radiation at 40 and 70 keV. The radiation passed through the patient from below while the differential absorption was measured above. The ratio of absorption between the two x-rays of different energies was linearly related to the FFM tissue compartment. The procedure for scanning was about 30 min. DXA provides a three-compartment partition of the body: bone mineral, fat mass (FM), and FFM. The precision and accuracy of DXA for soft tissue has been reported to be 99 percent with <1-percent error [18].
Total body potassium (TBK) was determine by the use of a 4-Pi whole-body counting chamber [19]. Subjects were placed on a stretcher and inserted into the chamber for 9 min. The radioisotope 40K occurs naturally as a trace element mixed with 39K. Potassium, the predominant cation in the body cell mass (BCM), can be measured by the highly sensitive whole-body counting chamber. TBK (mEq) is almost exclusively in the BCM compartment (95 to 98%) and has been shown to be a useful indicator of the quality and quantity of the lean tissue mass [19]. The 40K/39K ratio is constant and known at 0.0018, providing a marker for the TBK [20]. The measurement has a precision of ±4 percent [19]. TBK includes the combined 40K contribution from skeletal muscle and viscera, and this measurement has been referred to as BCM.
Statistical AnalysesThe results are expressed as mean ± standard deviation of the mean. Paired t-tests were performed to determine significant differences within the pairs. Intrapair difference (IPD) scores (paralyzed twin-able-bodied twin) were calculated within the twin pairs for BEE. Linear regression analyses were used to determine the relationship between energy expenditure (BEE or REE) with measures of FFM or TBK, as well as the relationship between BEE and duration of injury.
RESULTSThe characteristics of the subjects for the SCI and able-bodied twin groups are shown in Table 1. Twins with SCI had a significantly lower body weight, body mass index, and body surface area than the able-bodied twins. FFM and TBK were lower in twins with SCI than in non-SCI co-twins (FFM: 45.6 ± 10.0 vs. 55.5 ± 11.9 kg, p < 0.0005; TBK: 2,534 ± 911 vs. 3,515 ± 916 mEq, p = 0.01). Total FM was similar in the SCI and non-SCI twins (19.8 ± 11.8 vs. 19.3 ± 8.8 kg), but because of the reduction in lean tissue, the ratios of FM to FFM and FM to TBK were lower in the SCI compared to the non-SCI twins (0.35 ± 0.15 vs. 0.436 ± 0.22, p = 0.08, and 8 ± 4 vs. 6 ± 2 g/mEq, p = 0.01, respectively). After application of the Harris-Benedict equation for age, height, weight, and gender, the predicted basal energy expenditure was significantly reduced in the twins with SCI (Table 3) [10]. The twins with SCI had a significantly lower percentage of predicted BEE than the able-bodied twins (85 ± 13 vs. 96 ± 11%; p < 0.05). The actual measured energy expenditure (BEE or REE) was significantly lower in the twins with SCI compared to the non-SCI twins. However, the energy expenditure per kilogram of body weight (BEE/kg or REE/kg) was not significantly different between the SCI and non-SCI groups (Table 3). There were significant linear correlations between FFM with BEE or REE (Figure 1) and TBK with BEE or REE (Figure 2). There was no significant difference in the increment of BEE or REE to either measure of lean tissue in the SCI compared with the able-bodied twins. An inverse trend was noted between the IPD scores for BEE and duration of injury (R = -0.44, p < 0.14).
Persons with SCI have body compositional changes that are similar to those reported in the elderly, with loss of lean tissue and relatively increased adiposity [21,22], although the anthropometrical distribution of muscle mass may differ. In an identical twin study, with one co-twin in each pair having SCI, Spungen et al. reported a loss of lower-limb muscle mass that was continuous and directly correlated with duration of injury [4]. Strong correlations between altered body composition and the level of SCI have been observed, with successively higher, more complete spinal cord lesions associated with decreased FFM and body cell mass [23]. In this study, the loss of lean body tissue in twins with SCI with similar absolute FM to their non-SCI co-twins results in a relative increase in the ratio of body fat to lean tissue in twins with SCI compared with non-SCI co-twins.
The dramatic muscle atrophy in patients with acute SCI is clearly related to the degree of paralysis and immobilization. The etiology for the apparent accelerated loss of muscle mass in those with chronic SCI is less certain. However, similar to that which occurs with advancing age, persons with SCI have shown a reduction in endogenous anabolic hormones, testosterone and growth hormone. Although the literature is conflicting concerning serum testosterone concentrations in persons with SCI [14,24-29], there are undoubtedly subsets of men with relative or absolute androgen deficiency, with several etiologies possible in the SCI population [30-35]. Blunted release of growth hormone to provocative stimulation has been reported in subjects with SCI [36]. The average plasma insulin-like grown factor-I (IGF-I) level, the second messenger of growth hormone, was significantly lower in younger individuals with SCI [36], a finding confirmed by others [37]. A low IGF-I level has been reported to have functional significance in persons with post poliomyelitis syndrome [38] and may be relevant to the activities of daily living in other disabled populations.
In a study of 241 monozygotic and 228 dizygotic twin pairs that examined the relationship between physical activity and total body or abdominal fat, physical activity predicted lower generalized and central adiposity in middle-aged women [39]. The influence of physical activity in those who were susceptible to adiposity also demonstrated a significant salutary effect of physical activity [39]. Behavioral factors were studied as predictors of weight gain in 12,669 adult Finns [40]. The prevalence of obesity was inversely associated with physical activity, as well as other sociodemographic factors. Parity and caloric intake predicted weight gain in women [40]. In another study in 436 female twins, no significant relationship was found between recent dietary fat consumption and total or abdominal adiposity, after controlling for genetic and some environmental factors [41].
Epidemiological studies have demonstrated that the incidence rates for diabetes mellitus decline as energy expenditure and regular exercise increase [42,43]. Leisure time activity was inversely correlated to the development of type 2 diabetes mellitus in 5,990 male alumni of the University of Pennsylvania [42]. Each 500 kcal increment in energy expenditure was associated with a 6-percent reduction in the age-adjusted risk of diabetes [42]. In a prospective study of 21,271 physicians who were participating in the Physicians' Health Study, exercise appeared to reduce the risk of developing diabetes mellitus, even after adjusting for body mass index [43]. Whether a decrement in basal energy needs per se, as was the case in our study, will influence the risk for diabetes mellitus, has not been addressed in the literature. However, the obvious need to encourage increased activity-related energy expenditure in persons with disability who have a propensity for the development of diabetes is certainly supported by the above epidemiological studies [42,43]. Of note, the protective effect of physical activity was greatest in those who were at highest risk for the development of diabetes mellitus [42].
If appetite is not diminished and energy requirements are reduced, the result will inevitably be weight gain and obesity. We are not aware of any studies that specifically address satiety after an individual has sustained a SCI. Increased relative or absolute adiposity has certainly been reported for persons with chronic SCI, with unfavorable metabolic consequences [44,45]. Appetite regulation and measures of satiety remain necessary and provocative areas of future investigation in individuals with disability-including, but not limited to, those with SCI.
Related to these adverse body composition changes and reductions in energy requirements, individuals with SCI have a pattern of metabolic changes that is atherogenic. In persons with SCI, there have been reported adverse lipid changes [46,47], a reduction in metabolic rate [1], glucose intolerance, and insulin resistance [5,47,48]. The "multiple metabolic syndrome" has been well appreciated to increase risk of premature cardiovascular disease in the able-bodied population and would be expected to be at least equally deleterious in those with SCI [7,8,48-54].
CONCLUSIONIn this study of monozygotic twins who are discordant for SCI, a clear reduction in energy expenditure has been demonstrated after chronic paralysis. Without regard to injury status, the reduction in energy needs is directly related to lean tissue: the greater the reduction in lean tissue, the greater the reduction in energy expenditure. There appears to be an inverse relationship, albeit not reaching significance, between energy expenditure and duration of injury. Although this study was performed in twins discordant for SCI, our findings may be generalized to persons with various disabilities that limit mobility and/or reduce muscle mass, and who will be expected to have similar reductions in energy requirements. Once again, if there is a reduction in energy needs, the appropriate exercise and dietary interventions should be considered.
ACKNOWLEDGMENTSThe authors wish to thank the Spinal Cord Research Foundation (SCRF) for funding our grant, entitled "The Influence of SCI on Metabolism: An Analysis of Identical Twins." The Eastern Paralyzed Veterans Association (EPVA), under the direction, guidance, and wisdom of Mr. James J. Peters, provided us with its unwavering support that permitted us to accomplish this study. The Bronx Veterans Affairs Medical Center and the Mount Sinai School of Medicine also supported this work.
REFERENCES1. Mollinger LA, Spurr GB, El Ghatit AZ, Barboriak JJ, Rooney CB, Davidoff DD, et al. Daily energy expenditure and basal metabolic rates of patients with spinal cord injury. Arch Phys Med Rehabil 1985;66:420-26.2. Spungen AM, Bauman WA, Wang J, Pierson RN Jr. The relationship between total body potassium and resting energy expenditure in individuals with paraplegia. Arch Phys Med Rehabil 1993;73:965-68.3. Spungen AM, Wang J, Pierson RN Jr, Bauman WA. Soft tissue body composition differences in monozygotic twins discordant for spinal cord injury. J Appl Physiol 2000;88: 1310-15.4. Spungen AM, Adkins RH, Stewart CA, Wang J, Pierson RN, Waters RL, et al. Factors influencing body composition in persons with spinal cord injury: a cross-sectional study. J Appl Physiol 2003;95(6):2398-407.5. Bauman WA, Spungen AM. Disorders of carbohydrate and lipid metabolism in veterans with paraplegia or quadriplegia: a model of premature aging. Metabolism 1994;43:749-56.6. Bauman WA, Spungen AM. Endocrinology and metabolism after spinal cord injury. In: Kirshblum S, Campagnolo DI, DeLisa JA, editors. Spinal cord medicine. New York: Lippincott Publications; 2002. p. 164-80.7. Reaven GM. NIDDM, abnormal lipoprotein metabolism, and atherosclerosis. Metabolism 1987;36(Suppl 1):1-8.8. Lopez-Candales A. Metabolic syndrome X: a comprehensive review of the pathophysiology and recommended therapy. J Med 2001;32(5,6):283-300.9. Webb P, Troutman S Jr. An instrument for continuous measurement of oxygen consumption. J Appl Physiol 1970; 28:867-71.10. Harris JA, Benedict FG. Biometric studies of basal metabolism in man. Washington, DC: Carnegie Institution of Washington; 1919. Publication No. 279.11. Jones N. Clinical exercise testing. 3rd ed. Philadelphia: Saunders; 1988. p. 292-300.12. Consolazio C, Johnson R, Pecora L. Physiological measurement of metabolic function in man. New York: McGraw-Hill; 1963.13. De Weir JB. New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol (London) 1949;109:1-9.14. Wang YH, Huang TS, Lien IN. Hormone changes in men with spinal cord injuries. Amer J Phys Med Rehabil 1992; 71:328-32.15. Pierson RN Jr, Wang J, Heymsfield SB, Russell-Aulet M, Mazariegos M, Tierney M, et al. Measuring body fat: calibrating the rulers. Intermethod comparisons in 389 normal Caucasian subjects. Am J Physiol Endocrinol Metab 1991; 261:E103-8.16. Heysfield SB, Wang J, Heshka S, Kehayias JJ, Pierson RN Jr. Dual-photon absorptiometry: comparison of bone mineral and soft tissue mass measurements in vivo with established methods. Am J Clin Nutr 1989;49:1283-89.17. Mazess RB, Peppler WW, Gibbons M. Total body composition by dual-photon absorptiometry. Am J Nutr 1984;40: 834-39.18. Lukaski HC. Soft tissue composition and bone mineral status: evaluation by dual-energy x-ray absorptiometry. J Nutr 1993;123:438-43.19. Pierson RN Jr, Wang J, Colt EWD, Neumann P. Body composition measurements in normal man: potassium, saline and tritium spaces in 58 adults. J Chron Dis 1982;35:419-28.20. Bin Samat S, Green S, Beddoe AH. The activity of one gram of potassium. Phys Med Biol 1997;42:407-13.21. Spungen AM, Bauman WA, Wang J, Pierson RN Jr. Meas-urement of body fat in individuals with tetraplegia: a comparison of eight clinical methods. Paraplegia 1995;33: 402-8.22. Evans WJ. What is sarcopenia? J Geontol 1995;50A(Special Issue):5-8.23. Nulicek DN, Spurr GB, Barboriak JJ, Rooney CB, el Ghatit AZ, Bongard RD. Body composition of patients with spinal cord injury. Euro J Clin Nutri 1988;42:765-73.24. Bors E, Engle ET, Rosenquist RC, Holinger H. Fertility in paraplegic males: a preliminary report of endocrine studies. J Clin Endocrinol Metabol 1949;10:381-98.25. Naftchi NE, Via AT, Sell GH, Lowman EW. Pituitary-testicular axis dysfunction in spinal cord injury. Arch Phys Med Rehabil 1980;61:402-5.26. Nance P, Shears AH, Mivner ML, Nance M. Gonadal regulation in men with flaccid paraplegia. Arch Phys Med Rehabil 1987;66:757-59.27. Cook AW, Lyons HA. Urinary excretion of 17-ketosteroids in tetraplegic and paraplegic patients. US Armed Forces Med J 1950;1:538-85.28. Bauman WA, Spungen AM. Serum testosterone concentrations in a population of persons with spinal cord injury. Clin Endocrinol. Submitted for publication.29. Tsitouras PD, Zhong YG, Spungen AM, Bauman WA. Serum testosterone and growth hormone/insulin-like growth factor-I in adults with spinal cord injury. Horm Metab Res 1995;27:287-92.30. Rinieris P, Hatzimanolis J, Markianos M, Stefanis C. Effects of 4 weeks treatment with chlorpromazine and/or trihexyphenidyl on the pituitary-gonadal axis in male paranoid schizophrenics. Eur Arch Psychiatry Neurol Sci 1988; 237:189-93.31. Rinieris P, Hatzimanolis J, Markianos M, Stefanis C. Effects of treatment with various doses of halperidol on the pituitary-gonadal axis in male schizophrenic patients. Neuropsychobiology 1989;22:146-49.32. Calvo DJ, Campos MB, Calandra RS, Medina JH, Ritta MN. Effect of long term diazepam administration on testicular benzodiazepine receptors and steroidogenesis. Life Sci 1991;49:519-25.33. Sam AD 2nd, Sharma AC, Lee LY, Hales DB, Law WR, Ferguson JL, et al. Sepsis produces depression of testosterone and steroidogenic acute regulatory (StAR) protein. Shock 1999;11:298-301.34. Schroder J, Kahlke V, Stataubach KH, Zabel P, Stuber F. Gender differences in human sepsis. Arch Surg 1998;133: 1200-205.35. Brindley GS. Deep scrotal temperature and the effect on it of clothing, air temperature, activity, posture and paraplegia. Brit J Urol 1982;54:49-55.36. Bauman WA, Spungen AM, Flanagan S, Zhong YG, Alexander LR, Tsitouras PD. Blunted growth hormone response to intravenous arginine in subjects with a spinal cord injury. Horm Met Res 1994;26:149-53.37. Shetty K, Sutton CH, Mattson DE, Rudman D. Hyposomatomedinemia in quadriplegic men. Am J Med Sci 1993; 305:95-100.38. Rao U, Shetty KR, Mattson DE, Rudman IW, Rudman D. Prevalence of low plasm IGF-I in poliomyelitis survivors. J Am Geriatr Soc 1993;41:697-702.39. Samaras K, Kelly PJ, Chiano MN, Spector TD, Campbell LV. Genetic and environmental influences on total-body and central abdominal fat: the effect of physical activity in female twins. Ann Intern Med 1999;130(11):873-82.40. Rissanen AM, Heliovaara M, Knekt P, Reunanen A, Aromaa A. Determinants of weight gain and overweight in adult Finns. Eur J Clin Nutr 1991;45:419-30.41. Samaras K, Kelly PJ, Chiano MN, Spector TD, Campbell LV. Genes versus environment. The relationship between dietary fat and total and central abdominal fat. Diabetes Care 1998;21(12):2069-76.42. Helmrich SP, Ragland DR, Leung RW, Paffenbarger RS. Physical activity and reduced occurrence of NIDDM. N Engl J Med 1991;325:147-52.43. Manson JE, Nathan DM, Krolewski AS, Stampfer MJ, Willett WC, Hennekens CH. A prospective study of exercise and incidence of diabetes among US male physicians. JAMA 1992;268:63-67.44. Zhong YG, Levy E, Bauman WA. The relationships among serum uric acid, plasma insulin and serum lipoprotein levels in subjects with spinal cord injury. Horm Met Res 1995; 27:283-86.45. Maki KC. Associations between serum lipids and indicators of adiposity in men with spinal cord injury. Paraplegia 1995;33:102-9.46. 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;30:697-703.47. Bauman WA, Adkins RH, Spungen AM, Waters RL. The effect of residual neurological deficit on serum lipoproteins in individuals with chronic spinal cord injury. Spinal Cord 1998;36:13-17.48. Bauman WA, Adkins RH, Spungen AM. Carbohydrate and lipid metabolism in chronic spinal cord injury. J Spinal Cord Med 2001;24:266-77.49. Bauman WA, Raza M, Machac J. Tomograhic thallium201 myocardial perfusion imaging after intravenous dipyridamole in asymptomatic subjects with quadriplegia. Arch Phys Med Rehab 1993;74(7):740-44.50. Bauman WA, Raza M, Spungen AM, Machac J. Upper ergometry cardiac stress testing with thallium201 imaging in paraplegia. Arch Phys Med Rehabil 1994;75:946-50.51. Whiteneck GG, Charlifue SW, Frankel HL, Fraser MH, Gardner BP, Gerhart KA, et al. Mortality, morbidity, and psychosocial outcomes of persons spinal cord injured more than 20 years ago. Paraplegia 1992;30:617-30.52. Budoff MJ, Shariar A, Adkins RH, Yee F, Bakhsheshi H, Bauman WA. Coronary atherosclerosis in persons with spinal cord injury. J Spinal Cord Med 2000;23:170.53. Reaven GM. NIDDM, abnormal lipoprotein metabolism, and atherosclerosis. Metabolism 1987;36(Suppl 1):1-8.54. Hanley AJ, Karter AJ, Festa A, D'Agostino R Jr, Wagenknecht LE, Savage P, et al. Factor analysis of metabolic syndrome using directly measured insulin sensitivity: the Insulin Resistance Atherosclerosis Study. Diabetes 2002; 51(8):2642-47.Submitted for publication August 12, 2003. Accepted in revised form November 16, 2003.
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