Sex dimorphism in the distribution of adipose tissue and its influence on proinflammatory adipokines and cardiometabolic profiles in motor complete spinal cord injury

References

• Gorgey AS, Dolbow DR, Dolbow JD, Khalil RK, Castillo C, Gater DR. Effects of spinal cord injury on body composition and metabolic profile - part I. J Spinal Cord Med 2014;37:693–702. doi: 10.1179/2045772314Y.0000000245
   PubMed Web of Science ®Google Scholar
• Farkas GJ, Gater DR. Neurogenic obesity and systemic inflammation following spinal cord injury: a review. J Spinal Cord Med 2017:1–10.
   PubMed Web of Science ®Google Scholar
• White UA, Tchoukalova YD. Sex dimorphism and depot differences in adipose tissue function. Biochim Biophys Acta 2013;1842(3):377–92. doi: 10.1016/j.bbadis.2013.05.006
   PubMed Web of Science ®Google Scholar
• Fuente-Martín E, Argente-Arizón P, Ros P, Argente J, Chowen JA. Sex differences in adipose tissue: It is not only a question of quantity and distribution. Adipocyte 2013;2(3):128–34. doi: 10.4161/adip.24075
   PubMedGoogle Scholar
• Mauvais-Jarvis F. Sex differences in metabolic homeostasis, diabetes, and obesity. Biol Sex Differ. 62015.
   Google Scholar
• Jung UJ, Choi M-S. Obesity and its Metabolic Complications: The Role of Adipokines and the Relationship between Obesity, Inflammation, Insulin Resistance, Dyslipidemia and Nonalcoholic Fatty Liver Disease. Int J Mol Sci 2014;15:6184–223. doi: 10.3390/ijms15046184
   PubMed Web of Science ®Google Scholar
• Spinal Cord Injury (SCI) 2016 Facts and Figures at a Glance. J Spinal Cord Med 2016;39(4):493–4. doi: 10.1080/10790268.2016.1210925
   PubMed Web of Science ®Google Scholar
• Curtin CM, Suarez PA, Di Ponio LA, Frayne SM. Who are the women and men in Veterans Health Administration's current spinal cord injury population? J Rehabil Res Dev 2012;49(3):351–60. doi: 10.1682/JRRD.2010.11.0220
   PubMed Web of Science ®Google Scholar
• Gorgey AS, Mather KJ, Poarch HJ, Gater DR. Influence of motor complete spinal cord injury on visceral and subcutaneous adipose tissue measured by multi-axial magnetic resonance imaging. J Spinal Cord Med 2011;34:99–109. doi: 10.1179/107902610X12911165975106
   PubMed Web of Science ®Google Scholar
• Gorgey AS, Gater DR. Regional and relative adiposity patterns in relation to carbohydrate and lipid metabolism in men with spinal cord injury. Appl Physiol Nutr Metab 2011;36:107–14. doi: 10.1139/H10-091
   PubMed Web of Science ®Google Scholar
• Neto FR, Lopes GH. Body composition modifications in people with chronic spinal cord injury after supervised physical activity. J Spinal Cord Med 2011;34(6):586–93. doi: 10.1179/2045772311Y.0000000038
   PubMed Web of Science ®Google Scholar
• Gorgey AS, Mather KJ, Gater DR. Central adiposity associations to carbohydrate and lipid metabolism in individuals with complete motor spinal cord injury. Metab Clin Exp 2011;60:843–51. doi: 10.1016/j.metabol.2010.08.002
   PubMed Web of Science ®Google Scholar
• 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. doi: 10.1093/ajcn/87.3.600
   PubMed Web of Science ®Google Scholar
• Kullberg J, Brandberg J, Angelhed JE, Frimmel H, Bergelin E, Strid L, et al. Whole-body adipose tissue analysis: comparison of MRI, CT and dual energy X-ray absorptiometry. Br J Radiol 2009;82(974):123–30. doi: 10.1259/bjr/80083156
   PubMed Web of Science ®Google Scholar
• Clasey J, Gater D. Body Composition Assessment in Adults with Spinal Cord Injury. Top Spinal Cord Inj Rehabil 2007;12:8–19. doi: 10.1310/sci1204-8
   Google Scholar
• Gorgey AS, Farkas GJ, Dolbow DR, Khalil RE, Gater DR. Gender Dimorphism in Central Adiposity May Explain Metabolic Dysfunction After Spinal Cord Injury. Pm r 2017.
   Google Scholar
• Gater DR. Obesity after spinal cord injury. Phys Med Rehabil Clin N Am 2007;18:333–51. doi: 10.1016/j.pmr.2007.03.004
   PubMedGoogle Scholar
• Katsareli EA, Dedoussis GV. Biomarkers in the field of obesity and its related comorbidities. Expert Opin Ther Targets 2014;18:385–401. doi: 10.1517/14728222.2014.882321
   PubMed Web of Science ®Google Scholar
• You T, Arsenis NC, Disanzo BL, Lamonte MJ. Effects of exercise training on chronic inflammation in obesity : current evidence and potential mechanisms. Sports Med 2013;43(4):243–56. doi: 10.1007/s40279-013-0023-3
   PubMed Web of Science ®Google Scholar
• Makki K, Froguel P, Wolowczuk I. Adipose Tissue in Obesity-Related Inflammation and Insulin Resistance: Cells, Cytokines, and Chemokines. Int Sch Res Notices 2013;2013:e139239.
   Google Scholar
• Bajzar L. Thrombin activatable fibrinolysis inhibitor and an antifibrinolytic pathway. Arterioscler Thromb Vasc Biol 2000;20(12):2511–8. doi: 10.1161/01.ATV.20.12.2511
   PubMed Web of Science ®Google Scholar
• Manns PJ, McCubbin JA, Williams DP. Fitness, inflammation, and the metabolic syndrome in men with paraplegia. Arch Phys Med Rehabil 2005;86:1176–81. doi: 10.1016/j.apmr.2004.11.020
   PubMed Web of Science ®Google Scholar
• Krause JS, DiPiro ND, Saunders LL, Newman SD, Banik NL, Park S. Allostatic Load and Spinal Cord Injury: Review of Existing Research and Preliminary Data. Top Spinal Cord Inj Rehabil 2014;20:137–46. doi: 10.1310/sci2002-137
   PubMedGoogle Scholar
• Hansen D, Dendale P, Beelen M, Jonkers RAM, Mullens A, Corluy L, et al. Plasma adipokine and inflammatory marker concentrations are altered in obese, as opposed to non-obese, type 2 diabetes patients. Eur J Appl Physiol 2010;109:397–404. doi: 10.1007/s00421-010-1362-5
   PubMed Web of Science ®Google Scholar
• Roytblat L, Rachinsky M, Fisher A, Greemberg L, Shapira Y, Douvdevani A, et al. Raised Interleukin-6 Levels in Obese Patients. Obes Res 2000;8:673–5. doi: 10.1038/oby.2000.86
   PubMedGoogle Scholar
• Maruyama Y, Mizuguchi M, Yaginuma T, Kusaka M, Yoshida H, Yokoyama K, et al. Serum leptin, abdominal obesity and the metabolic syndrome in individuals with chronic spinal cord injury. Spinal Cord 2008;46:494–9. doi: 10.1038/sj.sc.3102171
   PubMed Web of Science ®Google Scholar
• Kirshblum SC, Burns SP, Biering-Sorensen F, Donovan W, Graves DE, Jha A, et al. International standards for neurological classification of spinal cord injury (Revised 2011). J Spinal Cord Med 2011;34:535–46.
   Google Scholar
• Doherty JG, Burns AS, O'Ferrall DM, Ditunno JF, Jr. Prevalence of upper motor neuron vs lower motor neuron lesions in complete lower thoracic and lumbar spinal cord injuries. J Spinal Cord Med 2002;25(4):289–92. doi: 10.1080/10790268.2002.11753630
   PubMedGoogle Scholar
• Ross R, Rissanen J. Mobilization of visceral and subcutaneous adipose tissue in response to energy restriction and exercise. Am J Clin Nutr 1994;60(5):695–703. doi: 10.1093/ajcn/60.5.695
   PubMed Web of Science ®Google Scholar
• Ross R, Rissanen J, Hudson R. Sensitivity associated with the identification of visceral adipose tissue levels using waist circumference in men and women: effects of weight loss. Int J Obes Relat Metab Disord 1996;20(6):533–8.
   PubMed Web of Science ®Google Scholar
• Ross R, Rissanen J, Pedwell H, Clifford J, Shragge P. Influence of diet and exercise on skeletal muscle and visceral adipose tissue in men. J Appl Physiol (1985) 1996;81(6):2445–55. doi: 10.1152/jappl.1996.81.6.2445
   PubMed Web of Science ®Google Scholar
• Gorgey AS, Wells KM, Austin TL. Adiposity and spinal cord injury. World J Orthop 2015;6:567–76. doi: 10.5312/wjo.v6.i8.567
   PubMed Web of Science ®Google Scholar
• Shuster A, Patlas M, Pinthus JH, Mourtzakis M. The clinical importance of visceral adiposity: a critical review of methods for visceral adipose tissue analysis. Br J Radiol. 85 2012. p. 1–10. doi: 10.1259/bjr/38447238
   PubMed Web of Science ®Google Scholar
• Gorgey AS, Harnish CR, Daniels JA, Dolbow DR, Keeley A, Moore J, et al. A report of anticipated benefits of functional electrical stimulation after spinal cord injury. J Spinal Cord Med 2012;35:107–12.
   Google Scholar
• Faul F, Erdfelder E, Buchner A, Lang AG. Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Methods 2009;41(4):1149–60. doi: 10.3758/BRM.41.4.1149
   PubMed Web of Science ®Google Scholar
• Tuck MK, Chan DW, Chia D, Godwin AK, Grizzle WE, Krueger KE, et al. Standard operating procedures for serum and plasma collection: early detection research network consensus statement standard operating procedure integration working group. J Proteome Res 2008;8(1):113–7. doi: 10.1021/pr800545q
   Web of Science ®Google Scholar
• 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 (1985) 2003;95:2398–407. doi: 10.1152/japplphysiol.00729.2002
   PubMed Web of Science ®Google Scholar
• Bauman WA, Adkins RH, Spungen AM, Waters RL. The effect of residual neurological deficit on oral glucose tolerance in persons with chronic spinal cord injury. Spinal Cord 1999;37(11):765–71. doi: 10.1038/sj.sc.3100893
   PubMed Web of Science ®Google Scholar
• Fryar CD, Gu Q, Ogden CL. Anthropometric reference data for children and adults: United States, 2007–2010. Vital Health Stat 2012(252):1–48.
   PubMedGoogle Scholar
• Piche ME, Lapointe A, Weisnagel SJ, Corneau L, Nadeau A, Bergeron J, et al. Regional body fat distribution and metabolic profile in postmenopausal women. Metabolism 2008;57(8):1101–7. doi: 10.1016/j.metabol.2008.03.015
   PubMed Web of Science ®Google Scholar
• Lizcano F, Guzmán G. Estrogen Deficiency and the Origin of Obesity during Menopause. Biomed Res Int 2014;2014. doi: 10.1155/2014/757461
   PubMedGoogle Scholar
• Munoz J, Derstine A, Gower BA. Fat distribution and insulin sensitivity in postmenopausal women: influence of hormone replacement. Obes Res 2002;10(6):424–31. doi: 10.1038/oby.2002.59
   PubMedGoogle Scholar
• Yuksel H, Odabasi AR, Demircan S, Koseoglu K, Kizilkaya K, Onur E. Effects of postmenopausal hormone replacement therapy on body fat composition. Gynecol Endocrinol 2007;23(2):99–104. doi: 10.1080/09513590601152177
   PubMed Web of Science ®Google Scholar
• Lombardi G, Mondaini N, Macchiarella A, Del Popolo G. Female sexual dysfunction and hormonal status in spinal cord injured (SCI) patients. J Androl 2007;28(5):722–6. doi: 10.2164/jandrol.106.002113
   PubMedGoogle Scholar
• Allan CA, Strauss BJ, Burger HG, Forbes EA, McLachlan RI. Testosterone therapy prevents gain in visceral adipose tissue and loss of skeletal muscle in nonobese aging men. J Clin Endocrinol Metab 2007;93(1):139–46. doi: 10.1210/jc.2007-1291
   PubMed Web of Science ®Google Scholar
• Ouchi N, Parker JL, Lugus JJ, Walsh K. Adipokines in inflammation and metabolic disease. Nat Rev Immunol 2011;11(2):85–97. doi: 10.1038/nri2921
   PubMed Web of Science ®Google Scholar
• Schmid A, Knöebber J, Vogt S, König D, Deibert P, Bültermann D, et al. Lipid Profiles of Persons With Paraplegia and Tetraplegia: Sex Differences. J Spinal Cord Med 2008;31(3):285–9. doi: 10.1080/10790268.2008.11760724
   PubMed Web of Science ®Google Scholar
• Yarar-Fisher C, Chen Y, Jackson AB, Hunter GR. Body mass index underestimates adiposity in women with spinal cord injury. Obesity (Silver Spring, Md) 2013;21:1223–5. doi: 10.1002/oby.20199
   PubMed Web of Science ®Google Scholar
• Paradis ME, Badellino KO, Rader DJ, Deshaies Y, Couture P, Archer WR, et al. Endothelial lipase is associated with inflammation in humans. J Lipid Res 2006;47(12):2808–13. doi: 10.1194/jlr.P600002-JLR200
   PubMed Web of Science ®Google Scholar
• Nadon GW, Little JA, Hall WE, O'Sullivan MO. A Comparison of the Oral and Intravenous Glucose Tolerance Tests in Non-Diabetic, Possible Diabetic and Diabetic Subjects. Can Med Assoc J 1964;91(26):1350–3.
   PubMed Web of Science ®Google Scholar
• Yarar-Fisher C, Chen YY, Jackson AB, Hunter GR. Body Mass Index Underestimates Adiposity in Women with Spinal Cord Injury. Obesity 2013;21(6):1223–5. doi: 10.1002/oby.20199
   PubMed Web of Science ®Google Scholar
• Beck LA, Lamb JL, Atkinson EJ, Wuermser L-A, Amin S. Body composition of women and men with complete motor paraplegia. J Spinal Cord Med 2014;37:359–65. doi: 10.1179/2045772313Y.0000000151
   PubMed Web of Science ®Google Scholar
• Mammi C, Calanchini M, Antelmi A, Cinti F, Rosano GM, Lenzi A, et al. Androgens and adipose tissue in males: a complex and reciprocal interplay. Int J Endocrinol 2012;2012. doi: 10.1155/2012/789653
   PubMed Web of Science ®Google Scholar
• Keustermans GC, Hoeks SB, Meerding JM, Prakken BJ, de Jager W. Cytokine assays: an assessment of the preparation and treatment of blood and tissue samples. Methods 2013;61(1):10–7. doi: 10.1016/j.ymeth.2013.04.005
   PubMed Web of Science ®Google Scholar