Skip to main content
Free AccessReview

A systematic review of cardiovascular risk factors in patients with traumatic spinal cord injury

Published Online:https://doi.org/10.1024/0301-1526/a000981

Summary:Objective: The main risk factors for cardiac events, and particularly for the development of atherosclerosis, are diabetes mellitus, arterial hypertension, dyslipidemia and smoking. Patients with a traumatic spinal cord injury (SCI) may present with autonomic nervous system dysfunction depending on their level of spinal cord injury. Studies have found a rise in cardiovascular mortality. A systematic review was conducted that focused on this patient group’s predisposition to vascular risk. Methods: We performed a PubMed and Cochrane database search. After applying specific search criteria, 42 articles were included in our analysis out of a total of 10,784 matches. The articles were selected with the aim of establishing cardiovascular risk factors in patients with traumatic spinal cord injury. Results: Patients with SCI are at an increased risk for peripheral artery disease even in the absence of cardiovascular risk factors. Major vascular changes to the arteries of patients with SCI include: a reduction in lumen size, increased vessel wall tension, higher vascular stiffness, an impaired reactive hyperemic response, and a lack of reduced vascular resistance. The findings for carotid atherosclerosis were inconclusive. This group of patients also has a higher disposition for diabetes mellitus, lipid metabolism disorders and coronary artery disease. Paraplegics are more likely to suffer from dyslipidemia, obesity and PAD, while tetraplegics are more likely to have diabetes mellitus. Conclusions: Patients with SCI are more likely to have cardiovascular risk factors and have cardiovascular disease compared to the normal population. Peripheral circulatory disorders are particularly common. Patients with SCI are now considered to be a new risk group for cardiovascular disease; however, large epidemiological studies are needed to verify in more detail the cardiovascular risk profile of this patient group.

References

  • 1 WHO. World Health Statistics reports 2019. Geneva: World Health Organization; 2019. [cited 2021 Jan 24]. Available from https://www.who.int/gho/publications/world_health_statistics/2019/EN_WHS_2019_Main.pdf?ua=1 First citation in articleGoogle Scholar

  • 2 Frank U, Nikol S, Belch J, Boc V, Brodmann M, Carpentier PH, et al. ESVM Guideline on peripheral arterial disease. Vasa. 2019;48(Suppl 102):1–79. https://doi.org/10.1024/0301-1526/a000834 First citation in articleAbstractGoogle Scholar

  • 3 WHO. Querschnittlähmung – Internationale Perspektiven 2014. Geneve:World Health Organization; 2014. [cited 2021 Jan 24]. Available from https://apps.who.int/iris/bitstream/handle/10665/94190/9783033046405_ger.pdf;jsessionid=0FEF8BF3B3E39E397BBBA08DF239CE1E?sequence=7 First citation in articleGoogle Scholar

  • 4 Imai K, Kadowaki T, Aizawa Y. Standardized indices of mortality among persons with spinal cord injury: accelerated aging process. Ind Health. 2004;42:213–8. https://doi.org/10.2486/indhealth.42.213 First citation in articleCrossref MedlineGoogle Scholar

  • 5 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;43:408–16. https://doi.org/10.1038/sj.sc.3101729 First citation in articleCrossref MedlineGoogle Scholar

  • 6 Chamberlain JD, Meier S, Mader L, von Groote PM, Brinkhof MWG. Mortality and longevity after a spinal cord injury: systematic review and meta-analysis. Neuroepidemiology. 2015;44:182–98. https://doi.org/10.1159/000382079 First citation in articleCrossref MedlineGoogle Scholar

  • 7 Chamberlain JD, Buzzell A, Gmünder HP, Hug K, Jordan X, Moser A, et al. Comparison of all-cause and cause-specific mortality of persons with traumatic rpinal cord injuries to the general swiss population: results from a national cohort study. Neuroepidemiology. 2019;52:205–13. https://doi.org/10.1159/000496976 First citation in articleCrossref MedlineGoogle Scholar

  • 8 Lidal IB, Snekkevik H, Aamodt G, Hjeltnes N, Stanghelle JK, Biering-Sørensen F. Mortality after spinal cord injury in Norway. J Rehabil Med. 2007;39:145–51. https://doi.org/10.2340/16501977-0017 First citation in articleCrossref MedlineGoogle Scholar

  • 9 Rabadi MH, Mayanna SK, Vincent AS. Predictors of mortality in veterans with traumatic spinal cord injury. Spinal Cord. 2013;51:784–8. https://doi.org/10.1038/sc.2013.77 First citation in articleCrossref MedlineGoogle Scholar

  • 10 Cragg JJ, Noonan VK, Krassioukov A, Borisoff J. Cardiovascular disease and spinal cord injury: results from a national population health survey. Neurology. 2013;81:723–8. https://doi.org/10.1212/WNL.0b013e3182a1aa68 First citation in articleCrossref MedlineGoogle Scholar

  • 11 Boot CR, Groothuis JT, Van Langen H, Hopman MT. Shear stress levels in paralyzed legs of spinal cord-injured individuals with and without nerve degeneration. J Appl Physiol. 2002;92:2335–40. https://doi.org/10.1152/japplphysiol.00340.2001 First citation in articleCrossref MedlineGoogle Scholar

  • 12 Bell JW, Chen D, Bahls M, Newcomer SC. Altered resting hemodynamics in lower-extremity arteries of individuals with spinal cord injury. J Spinal Cord Med. 2013;36:104–11. https://doi.org/10.1179/2045772312Y.0000000052 First citation in articleCrossref MedlineGoogle Scholar

  • 13 Bell JW, Chen D, Bahls M, Newcomer SC. Evidence for greater burden of peripheral arterial disease in lower extremity arteries of spinal cord-injured individuals. Am J Physiol Heart Circ Physiol. 2011;301:H766–72. https://doi.org/10.1152/ajpheart.00507.2011 First citation in articleCrossref MedlineGoogle Scholar

  • 14 Olive JL, Dudley GA, McCully KK. Vascular remodeling after spinal cord injury. Med Sci Sports Exerc. 2003;35:901–7. https://doi.org/10.1249/01.MSS.0000069755.40046.96 First citation in articleCrossref MedlineGoogle Scholar

  • 15 Yeung JJ, Kim HJ, Abbruzzese TA, Vignon-Clementel IE, Draney-Blomme MT, Yeung KK, et al. Aortoiliac hemodynamic and morphologic adaptation to chronic spinal cord injury. J Vasc Surg. 2006;44:1254–65. https://doi.org/10.1016/j.jvs.2006.08.026 First citation in articleCrossref MedlineGoogle Scholar

  • 16 de Groot PC, Bleeker MW, van Kuppevelt DH, van der Woude LH, Hopman MT. Rapid and extensive arterial adaptations after spinal cord injury. Arch Phys Med Rehabil. 2006;87:688–96. https://doi.org/10.1016/j.apmr.2006.01.022 First citation in articleCrossref MedlineGoogle Scholar

  • 17 Thijssen DHJ, de Groot PC, van den Bogerd A, Veltmeijer M, Cable NT, Green DJ, et al. Time course of arterial remodelling in diameter and wall thickness above and below the lesion after a spinal cord injury. Eur J Appl Physiol. 2012;112:4103–9. https://doi.org/10.1007/s00421-012-2400-2 First citation in articleCrossref MedlineGoogle Scholar

  • 18 Mizushima T, Tajima F, Aoki S, Yamamoto M, Ogata H. Carotid artery flow volume and velocity by duplex sonography in men with chronic low thoracic and lumbar spinal cord injury. Arch Phys Med Rehabil. 2005;86:517–20. https://doi.org/10.1016/j.apmr.2004.06.066 First citation in articleCrossref MedlineGoogle Scholar

  • 19 Miyatani M, Masani K, Oh PI, Miyachi M, Popovic MR, Craven C. Pulse wave velocity for assessment of arterial stiffness among people with spinal cord injury: a pilot study. J Spinal Cord Med. 2009;32:72–8. https://doi.org/10.1080/10790268.2009.11760755 First citation in articleCrossref MedlineGoogle Scholar

  • 20 Huang SC, Wong MK, Lien HY, Tang SFT, Fu TC, Lin Y, et al. Systemic vascular resistance is increased and associated with accelerated arterial stiffening change in patients with chronic cervical spinal cord injury. Eur J Phys Rehabil Med. 2013;49:41–9. First citation in articleMedlineGoogle Scholar

  • 21 Miyatani M, Szeto M, Moore C, Oh PI, McGillvary CF, Craven BC. Exploring the associations between arterial stiffness and spinal cord impairment: A cross-sectional study. J Spinal Cord Med. 2014;37:556–64. https://doi.org/10.1179/2045772314Y.0000000261 First citation in articleCrossref MedlineGoogle Scholar

  • 22 Miyatani M, Alavinia SM, Szeto M, Moore C, Craven BC. Association between abnormal arterial stiffness and cardiovascular risk factors in people with chronic spinal cord injury. Eur J Prev Cardiol. 2017;24:552–8. https://doi.org/10.1177/2047487316687426 First citation in articleCrossref MedlineGoogle Scholar

  • 23 Currie KD, Hubli M, MacDonald MJ, Krassioukov AV. Associations between arterial stiffness and blood pressure fluctuations after spinal cord injury. Spinal Cord. 2019;57:1057–63. https://doi.org/10.1038/s41393-019-0316-y First citation in articleCrossref MedlineGoogle Scholar

  • 24 Matos-Souza JR, Pithon KR, Ozahata TM, Gemignani T, Cliquet AJ, Nadruz WJ. Carotid intima-media thickness is increased in patients with spinal cord injury independent of traditional cardiovascular risk factors. Atherosclerosis. 2009;202:29–31. https://doi.org/10.1016/j.atherosclerosis.2008.04.013 First citation in articleCrossref MedlineGoogle Scholar

  • 25 Matos-Souza JR, Pithon KR, Ozahata TM, Oliveira RT, Teo FH, Blotta MH, et al. Subclinical atherosclerosis is related to injury level but not to inflammatory parameters in spinal cord injury subjects. spinal cord. 2010;48:740–4. https://doi.org/10.1038/sc.2010 First citation in articleCrossref MedlineGoogle Scholar

  • 26 Hoskin JD, Miyatani M, Craven BC. Quality reporting of carotid intima-media thickness methodology. Current state of the science in the field of spinal cord injury. J Spinal Cord Med. 2018;41:479–89. https://doi.org/10.1080/10790268.2017.1301622 First citation in articleCrossref MedlineGoogle Scholar

  • 27 La Favor JD, Hollis BC, Mokshagundam SL, Olive JL. Serum hsCRP and visfatin are elevated and correlate to carotid arterial stiffness in spinal cord-injured subjects. Spinal Cord. 2011;49:961–6. https://doi.org/10.1038/sc.2011.56 First citation in articleCrossref MedlineGoogle Scholar

  • 28 Gibson AE, Buchholz AC, Ginis KAM, SHAPE-SCI Research Group. C-reactive protein in adults with chronic spinal cord injury: increased chronic inflammation in tetraplegia vs paraplegia. Spinal Cord. 2008;46:616–21. https://doi.org/10.1038/sc.2008.32 First citation in articleCrossref MedlineGoogle Scholar

  • 29 Wang TD, Wang YH, Huang TS, Su TC, Pan SL, Chen SY. Circulating levels of markers of inflammation and endothelial activation are increased in men with chronic spinal cord injury. J Formos Med Assoc. 2007;106:919–28. https://doi.org/10.1016/S0929-6646(08)60062-5 First citation in articleCrossref MedlineGoogle Scholar

  • 30 Thijssen DHJ, Ellenkamp R, Kooijman M, Pickkers P, Rongen GA, Hopman MTE, et al. A causal role for endothelin-1 in the vascular adaptation to skeletal muscle deconditioning in spinal cord injury. Arterioscler Thromb Vasc Biol. 2007;27:325–31. https://doi.org/10.1161/01.ATV.0000253502.83167.31 First citation in articleCrossref MedlineGoogle Scholar

  • 31 Su TW, Chou TY, Jou HJ, Yang PY, Lin CL, Sung FC, et al. Peripheral arterial disease and spinal cord injury: a retrospective nationwide cohort study. Medicine. 2015;94:e1655. https://doi.org/10.1097/MD.0000000000001655 First citation in articleCrossref MedlineGoogle Scholar

  • 32 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;14:1957–64. https://doi.org/10.1016/j.spinee.2013.12.011 First citation in articleCrossref MedlineGoogle Scholar

  • 33 Cragg JJ, Noonan VK, Dvorak M, Krassioukov A, Mancini GBJ, Borisoff JF. Spinal cord injury and type 2 diabetes: results from a population health survey. Neurology. 2013;81:1864–8. https://doi.org/10.1212/01.wnl.0000436074.98534.6e First citation in articleCrossref MedlineGoogle Scholar

  • 34 LaVela SL, Weaver FM, Goldstein B, Chen K, Miskevics S, Rajan S, et al. Diabetes mellitus in individuals with spinal cord injury or disorder. J Spinal Cord Med. 2006;29:387–95. https://doi.org/10.1080/10790268.2006.11753887 First citation in articleCrossref MedlineGoogle Scholar

  • 35 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. Cardiopulm Rehabil Prev. 2011;31:73–80. https://doi.org/10.1097/HCR.0b013e3181f68aba First citation in articleCrossref MedlineGoogle Scholar

  • 36 La Fountaine M, Rivera DR, Radulovic M, Bauman WA. The hemodynamic actions of insulin are blunted in the sublesional microvasculature of healthy persons with spinal cord injury. Am J Phys Med Rehabil. 2013;92:127–35. https://doi.org/10.1097/PHM.0b013e31827d63ee First citation in articleCrossref MedlineGoogle Scholar

  • 37 Li J, Hunter GR, Chen Y, McLain A, Smith DL, Yarar-Fisher C. Differences in glucose metabolism among women with spinal cord injury may not be fully explained by variations in body composition. Arch Phys Med Rehabil. 2019;100:1061–7.e1. https://doi.org/10.1016/j.apmr.2018.08.191 First citation in articleCrossref MedlineGoogle Scholar

  • 38 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;89:1448–53. https://doi.org/10.1016/j.apmr.2007.12.047 First citation in articleCrossref MedlineGoogle Scholar

  • 39 Barry W, St. Andre JR, Evans CT, Sabharwal S, Miskevics S, Weaver FM, et al. Hypertension and antihypertensive treatment in veterans with spinal cord injury and disorders. Spinal Cord. 2013;51:109–15. https://doi.org/10.1038/sc.2012.122 First citation in articleCrossref MedlineGoogle Scholar

  • 40 Saunders LL, Clarke A, Tate DG, Forchheimer M, Krause JS. Lifetime prevalence of chronic health conditions among persons with spinal cord injury. Arch Phys Med Rehabil. 2015;96:673–9. https://doi.org/10.1016/j.apmr.2014.11.019 First citation in articleCrossref MedlineGoogle Scholar

  • 41 Sabour H, Javidan AN, Ranjbarnovin N, Vafa MR, Khazaeipur Z, Ghadri F, et al. Cardiometabolic risk factors in Iranians with spinal cord injury: analysis by injury-related variables. J Rehabil Res Dev. 2013;50:635–42. https://doi.org/10.1682/jrrd.2012.01.0020 First citation in articleCrossref MedlineGoogle Scholar

  • 42 Nash MS, Groah SL, Gater DR, Dyson-Hudson TA, Lieberman JA, Myers J, et al. Identification and management of cardiometabolic risk after spinal cord injury. J Spinal Cord Med. 2019;42:643–77. https://doi.org/10.1080/10790268.2018.1511401 First citation in articleCrossref MedlineGoogle Scholar

  • 43 Thayer JF, Sollers JJ, Clamor A, Koenig J, Hagglund KJ. The association of resting heart rate variability and 24-hour blood pressure variability in spinal cord injury. J Neurol Sci. 2016;361:52–9. https://doi.org/10.1016/j.jns.2015.12.017 First citation in articleCrossref MedlineGoogle Scholar

  • 44 Rosado-Rivera D, Radulovic M, Handrakis JP, Cirnigliaro CM, Jensen AM, Kirshblum S, et al. Comparison of 24-hour cardiovascular and autonomic function in paraplegia, tetraplegia, and control groups: Implications for cardiovascular risk. J Spinal Cord Med. 2011;34:395–403. https://doi.org/10.1179/2045772311Y.0000000019 First citation in articleCrossref MedlineGoogle Scholar

  • 45 Seabra-Garcez JD, Matos-Souza JR, Goulart D, Pithon KR, Abib E, Etchebehere M, et al. Ambulatory blood pressure is associated with subclinical atherosclerosis in spinal cord injury subjects. Int J Cardiol. 2012;154:89–90. https://doi.org/10.1016/j.ijcard.2011.10.055 First citation in articleCrossref MedlineGoogle Scholar

  • 46 Chen YK, Hung TKJ, Lin CC, Yen RF, Sung FC, Lee WY, et al. Increased risk of acute coronary syndrome after spinal cord injury: a nationwide 10-year follow-up cohort study. Int J Cardiol. 2013;168:1681–2. https://doi.org/10.1016/j.ijcard.2013.03.077 First citation in articleCrossref MedlineGoogle Scholar

  • 47 Akbal A, Kurtaran A, Selcuk B, Akyütz M. H-FABP, cardiovascular risk factors, and functional status in asymptomatic spinal cord injury patients. Herz. 2013;38:629–35. https://doi.org/10.1007/s00059-013-3779-1 First citation in articleCrossref MedlineGoogle Scholar

  • 48 Jörgensen S, Hill M, Lexell J. Cardiovascular risk factors among older adults with long-term spinal cord injury. PM R. 2019;11:8–16. https://doi.org/10.1016/j.pmrj.2018.06.008 First citation in articleCrossref MedlineGoogle Scholar

  • 49 Schmid A, Halle M, Stützle C, König D, Baumstark MW, Storch MJ, et al. Lipoproteins and free plasma catecholamines in spinal cord injured men with different injury levels. Clinical Physiology. 2000;20:304–10. https://doi.org/10.1046/j.1365-2281.2000.00263.x First citation in articleCrossref MedlineGoogle Scholar

  • 50 Laclaustra M, Van den Berg ELM, Hurtado-Roca Y, Castellote JM. Serum lipid profile in subjects with traumatic spinal cord injury. PLoS One. 2015;10: e0115522. https://doi.org/10.1371/journal.pone.0115522 First citation in articleCrossref MedlineGoogle Scholar

  • 51 Storch MJ, König D, Bültermann D, Blum A, Vogt S, Baumstark M, et al. Lipid profile in spinal cord-injured woman with different injury levels. Prev Med. 2005;40:321–5. https://doi.org/10.1016/j.ypmed.2004.06.006 First citation in articleCrossref MedlineGoogle Scholar

  • 52 Paim LR, Schreiber R, Matos-Souza JR, Silva AA, Campos LF, Azevedo ER, et al. Oxidized low-density lipoprotein, matrix-metalloproteinase-8 and carotid atherosclerosis in spinal cord injured subjects. Atherosclerosis. 2013;231:341–5. https://doi.org/10.1016/j.atherosclerosis.2013.10.005 First citation in articleCrossref MedlineGoogle Scholar

  • 53 La Fountaine MF, Cirnigliaro CM, Hobson JC, Dyson-Hudson T, Kenna CM, Kirshblum SC. Etablishing a threshold to predict cardiovascular disease from the serum triglyceride and high-density lipoprotein concentrations in person with spinal cord injury. spinal cord. 2018;56:1051–8. https://doi.org/10.1038/s41393-018-0187-7 First citation in articleCrossref MedlineGoogle Scholar

  • 54 Huang TS, Wang YH, Chen SY. The relation of serum leptin to body mass index and to serum cortisol in men with spinal cord injury. Arch Phys Med Rehabil. 2000;81:1582–6. https://doi.org/10.1053/apmr.2000.9173 First citation in articleCrossref MedlineGoogle Scholar

  • 55 Jeon JY, Steadward RD, Wheeler GD, Bell G, McCargar L, Harber V. Intact sympathetic nervous system is required for leptin effects on resting metabolic rate in people with spinal cord injury. J Clin Endocrinol Metab. 2003;88:402–7. https://doi.org/10.1210/jc.2002-020939 First citation in articleCrossref MedlineGoogle Scholar

  • 56 Maruyama Y, Mizuguchi M, Yaginuma T, Kusaka M, Yoshida H, Yokoyma K, et al. Serum leptin, abdominal obesity and the metabolic syndrome in individuals with chronic spinal cord injury. Spinal Cord. 2008;46:494–9. https://doi.org/10.1038/sj.sc.3102171 First citation in articleCrossref MedlineGoogle Scholar

  • 57 Long YC, Kostovski E, Boon H, Hjeltnies N, Krook A, Widegren U. Differential expression of metabolic genes essential for glucose and lipid metabolism in skeletal muscle from spinal cord injured subjects. J Appl Physiol. 2011;110:1204–10. https://doi.org/10.1152/japplphysiol.00686.2010 First citation in articleCrossref MedlineGoogle Scholar

  • 58 Kannel WB, McGee DL. Update on some epidemiologic features of intermittent claudication: the Framingham Study. J Am Geriatr Soc. 1985;33:13–8. https://doi.org/10.1111/j.1532-5415.1985.tb02853.x First citation in articleCrossref MedlineGoogle Scholar

  • 59 American Spinal Injury Association [ASIA]. International Standards for Neurological Classification of SCI (ISNCSCI) Worksheet. Richmond, VA: The American Spinal Injury Association; 2019. [cited 2021 Feb 1]. Available from https://asia-spinalinjury.org/international-standards-neurological-classification-sci-isncsci-worksheet/ First citation in articleGoogle Scholar

  • 60 West CR, Alyahya A, Laher I, Krassioukov A. Peripheral vascular function in spinal cord injury: a systematic review. Spinal Cord. 2013;51:10–9. https://doi.org/10.1038/sc.2012.136 First citation in articleCrossref MedlineGoogle Scholar

  • 61 Heinen Y, Stegemann E, Sansone R, Benedens K, Wagstaff R, Balzer J, et al. Local association between endothelial dysfunction an intimal hyperplasia: relevance in peripheral arterial disease. J Am Hear Assoc. 2015;4:e001472. https://doi.org/10.1161/JAHA.114.001472 First citation in articleMedlineGoogle Scholar

  • 62 Lee ANX, Phillips AA, Krassioukov AV. Increased central arterial stiffness after spinal cord injury: contributing factors, implications, and possible interventions. J Neurotrauma. 2017;34:1129–40. https://doi.org/10.1089/neu.2016.4694 First citation in articleCrossref MedlineGoogle Scholar

  • 63 Bloom O, Herman PE, Spungen AM. Systemic inflammation in traumatic spinal cord injury. Exp Neurol. 2020;325:113143. https://doi.org/10.1016/j.expneurol.2019.113143 First citation in articleCrossref MedlineGoogle Scholar

  • 64 Pearson TA, Mensah GA, Alexander RW, Anderson JL, Cannon RO 3rd, Criqui M, et al. Markers of inflammation and cardiovascular disease: application to clinical and public health practice: A statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation. 2003;107:499–511. https://doi.org/10.1161/01.cir.0000052939.59093.45 First citation in articleCrossref MedlineGoogle Scholar

  • 65 Eriks-Hoogland I, Hilfiker R, Baumberger M, Balk S, Stucki G, Perret C. Clinical assessment of obesity in persons with spinal cord injury: validity of waist circumference, body mass index, and anthropometric index. J Spinal Cord Med. 2011;34:416–22. https://doi.org/10.1179/2045772311Y.0000000014 First citation in articleCrossref MedlineGoogle Scholar

  • 66 Jones LM, Legge M, Goulding A. Healthy body mass index values often underestimate body fat in men with spinal cord injury. Arch Phys Med Rehabil. 2003;84:1068–71. https://doi.org/10.1016/s0003-9993(03)00045-5 First citation in articleCrossref MedlineGoogle Scholar

  • 67 Laughton GE, Buchholz AC, Ginis KAM, Goy RE for the SHAPE SCI Research Group. Lowering body mass index cutoffs better identifies obese persons with spinal cord injury. Spinal Cord. 2009;47:757–62. https://doi.org/10.1038/sc.2009.33 First citation in articleCrossref MedlineGoogle Scholar

  • 68 Pelletier CA, Miyatani M, Giangregorio L, Craven BC. Sarcopenic obesity in adults with spinal cord injury: A cross-sectional study. Arch Phys Med Rehabil. 2016;97:1931–7. https://doi.org/10.1016/j.apmr.2016.04.026 First citation in articleCrossref MedlineGoogle Scholar

  • 69 Farkas GJ, Gorgey AS, Dolbow DR, Berg AS, Gater DR. The influence of level of spinal cord injury on adipose tissue and its relationship to inflammatory adipokines and cardiometabolic profiles. J Spinal Cord Med. 2018;41:407–15. https://doi.org/10.1080/10790268.2017.1357918 First citation in articleCrossref MedlineGoogle Scholar

  • 70 Edwards LA, Bugaresti JM, Buchholz AC. Visceral adipose tissue and the ratio of visceral to subcutaneous adipose tissue are greater in adults with than in those without spinal cord injury, despite matching waist circumferences. Am J Clin Nutr. 2008;87:600–7. https://doi.org/10.1093/ajcn/87.3.600 First citation in articleCrossref MedlineGoogle Scholar

  • 71 Ravensbergen HJC, Lear SA, Claydon VE. Waist circumference is the best for obesity-related cardiovascular disease risk in individuals with spinal cord injury. J Neurotrauma. 2014;31:292–300. https://doi.org/10.1089/neu.2013.3042 First citation in articleCrossref MedlineGoogle Scholar

  • 72 Koyuncu E, Yüzer GFN, Yenigün D, Özgirgin N. The analysis of serum lipid levels in patients with spinal cord injury. J Spinal Cord Med. 2017;40:567–72. https://doi.org/10.1080/10790268.2016.1228286 First citation in articleCrossref MedlineGoogle Scholar

  • 73 Dalman RL, Harris EJ, Walker MT, Perkash I. Limb salvage surgery in spinal cord injury patients. Ann Vasc Surg. 1998;12:60–4. https://doi.org/10.1007/s100169900116 First citation in articleCrossref MedlineGoogle Scholar