Diabetes Metab J.  2012 Aug;36(4):285-292. 10.4093/dmj.2012.36.4.285.

Influence of Visceral Adiposity on Cardiovascular Autonomic Neuropathy in Patients with Type 2 Diabetes Mellitus

• Jang EH
• Kim NY
• Park YM
• Kim MK
• Baek KH
• Song KH
• Lee KW
• Kwon HS

• KMID: 2174426
• DOI: http://doi.org/10.4093/dmj.2012.36.4.285

Abstract

BACKGROUND
The aim of this study was to investigate the influences of visceral adiposity on cardiovascular autonomic neuropathy (CAN) in patients with type 2 diabetes mellitus.
METHODS
Two hundred eleven patients with type 2 diabetes participated in this study. Anthropometric and metabolic parameters were measured, and the visceral fat area was assessed using computed tomography. CAN was diagnosed using a cardiovascular reflex test. We analyzed the correlation between the visceral fat area and each parameter in this test.
RESULTS
The mean age, body mass index (BMI), and duration of diabetes of the study population were 60+/-14 years (mean+/-standard deviation), 25.1+/-4.2 kg/m2, and 12.3+/-8.9 years, respectively. The visceral fat area showed positive correlations with age, BMI, waist circumference, and subcutaneous fat area. There was no statistically significant difference in the cardiovascular reflex test outcome between genders. Univariate linear regression analysis showed that an increased visceral fat area diminished good heart rate response to a Valsalva maneuver (R2=4.9%, P=0.013 in an unadjusted model), but only in women. This statistical association was preserved after adjusting for age and BMI (R2=9.8%, P=0.0072).
CONCLUSION
The results of this study suggest that visceral adiposity contributes to an autonomic imbalance to some degree, as demonstrated by the impaired cardiovascular reflex test among women with type 2 diabetes.

Keyword

Cardiovascular autonomic neuropathy; Diabetes mellitus, type 2; Intra-abdominal fat; Obesity

MeSH Terms

Adiposity
Body Mass Index
Diabetes Mellitus, Type 2
Female
Heart Rate
Humans
Intra-Abdominal Fat
Linear Models
Obesity
Reflex
Subcutaneous Fat
Valsalva Maneuver
Waist Circumference

Figure

• 

  Fig. 1 Comparison of cardiovascular reflex tests outcome according to visceral fat area (VFA). (A) Male (n=82). (B) Female (n=129).

Reference

1. Maser RE, Lenhard JM, DeCherney SG. Cardiovascular autonomic neuropathy: the clinical significance of its determination. Endocrinologist. 2000. 10:27–33.

2. Boulton AJ, Vinik AI, Arezzo JC, Bril V, Feldman EL, Freeman R, Malik RA, Maser RE, Sosenko JM, Ziegler D. American Diabetes Association. Diabetic neuropathies: a statement by the American Diabetes Association. Diabetes Care. 2005. 28:956–962.

3. Gerritsen J, Dekker JM, TenVoorde BJ, Kostense PJ, Heine RJ, Bouter LM, Heethaar RM, Stehouwer CD. Impaired autonomic function is associated with increased mortality, especially in subjects with diabetes, hypertension, or a history of cardiovascular disease: the Hoorn Study. Diabetes Care. 2001. 24:1793–1798.

4. Maser RE, Mitchell BD, Vinik AI, Freeman R. The association between cardiovascular autonomic neuropathy and mortality in individuals with diabetes: a meta-analysis. Diabetes Care. 2003. 26:1895–1901.

5. Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, Lauria G, Malik RA, Spallone V, Vinik A, Bernardi L, Valensi P. Toronto Diabetic Neuropathy Expert Group. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care. 2010. 33:2285–2293.

6. Jellis CL, Stanton T, Leano R, Martin J, Marwick TH. Usefulness of at rest and exercise hemodynamics to detect subclinical myocardial disease in type 2 diabetes mellitus. Am J Cardiol. 2011. 107:615–621.

7. Low PA, Benrud-Larson LM, Sletten DM, Opfer-Gehrking TL, Weigand SD, O'Brien PC, Suarez GA, Dyck PJ. Autonomic symptoms and diabetic neuropathy: a population-based study. Diabetes Care. 2004. 27:2942–2947.

8. Toyry JP, Niskanen LK, Mantysaari MJ, Lansimies EA, Uusitupa MI. Occurrence, predictors, and clinical significance of autonomic neuropathy in NIDDM. Ten-year follow-up from the diagnosis. Diabetes. 1996. 45:308–315.

9. Perciaccante A, Fiorentini A, Paris A, Serra P, Tubani L. Circadian rhythm of the autonomic nervous system in insulin resistant subjects with normoglycemia, impaired fasting glycemia, impaired glucose tolerance, type 2 diabetes mellitus. BMC Cardiovasc Disord. 2006. 6:19.

10. Grassi G, Seravalle G, Cattaneo BM, Bolla GB, Lanfranchi A, Colombo M, Giannattasio C, Brunani A, Cavagnini F, Mancia G. Sympathetic activation in obese normotensive subjects. Hypertension. 1995. 25(4 Pt 1):560–563.

11. Laitinen T, Lindstrom J, Eriksson J, Ilanne-Parikka P, Aunola S, Keinanen-Kiukaanniemi S, Tuomilehto J, Uusitupa M. Cardiovascular autonomic dysfunction is associated with central obesity in persons with impaired glucose tolerance. Diabet Med. 2011. 28:699–704.

12. Hernandez-Ono A, Monter-Carreola G, Zamora-Gonzalez J, Cardoso-Saldana G, Posadas-Sanchez R, Torres-Tamayo M, Posadas-Romero C. Association of visceral fat with coronary risk factors in a population-based sample of postmenopausal women. Int J Obes Relat Metab Disord. 2002. 26:33–39.

13. Nicklas BJ, Penninx BW, Ryan AS, Berman DM, Lynch NA, Dennis KE. Visceral adipose tissue cutoffs associated with metabolic risk factors for coronary heart disease in women. Diabetes Care. 2003. 26:1413–1420.

14. Indulekha K, Anjana RM, Surendar J, Mohan V. Association of visceral and subcutaneous fat with glucose intolerance, insulin resistance, adipocytokines and inflammatory markers in Asian Indians (CURES-113). Clin Biochem. 2011. 44:281–287.

15. Miyazaki Y, Glass L, Triplitt C, Wajcberg E, Mandarino LJ, De-Fronzo RA. Abdominal fat distribution and peripheral and hepatic insulin resistance in type 2 diabetes mellitus. Am J Physiol Endocrinol Metab. 2002. 283:E1135–E1143.

16. Valensi P, Paries J, Attali JR. French Group for Research and Study of Diabetic Neuropathy. Cardiac autonomic neuropathy in diabetic patients: influence of diabetes duration, obesity, and microangiopathic complications: the French multicenter study. Metabolism. 2003. 52:815–820.

17. Baumgartner RN. Body composition in healthy aging. Ann N Y Acad Sci. 2000. 904:437–448.

18. Feldman EL, Stevens MJ, Thomas PK, Brown MB, Canal N, Greene DA. A practical two-step quantitative clinical and electrophysiological assessment for the diagnosis and staging of diabetic neuropathy. Diabetes Care. 1994. 17:1281–1289.

19. van der Kooy K, Seidell JC. Techniques for the measurement of visceral fat: a practical guide. Int J Obes Relat Metab Disord. 1993. 17:187–196.

20. Kang SM, Ko KS, Ko SH, Kwon HS, Kim JH, Park TS, Won JC, Lee JM, Lee JH, Chun SW, Cha BY. Korean Diabetic Neuropathy Study Group. Management of diabetic neuropathy. 2011. 3rd ed. Seoul: Korean Diabetes Association;39–42.

21. Wieling W, Schatz IJ. The consensus statement on the definition of orthostatic hypotension: a revisit after 13 years. J Hypertens. 2009. 27:935–938.

22. Examination Committee of Criteria for 'Obesity Disease' in Japan, Japan Society for the Study of Obesity. New criteria for 'obesity disease' in Japan. Circ J. 2002. 66:987–992.

23. Matsuzawa Y, Shimomura I, Nakamura T, Keno Y, Tokunaga K. Pathophysiology and pathogenesis of visceral fat obesity. Diabetes Res Clin Pract. 1994. 24:Suppl. S111–S116.

24. Voulgari C, Psallas M, Kokkinos A, Argiana V, Katsilambros N, Tentolouris N. The association between cardiac autonomic neuropathy with metabolic and other factors in subjects with type 1 and type 2 diabetes. J Diabetes Complications. 2011. 25:159–167.

25. Vinik AI, Maser RE, Ziegler D. Autonomic imbalance: prophet of doom or scope for hope? Diabet Med. 2011. 28:643–651.

26. Kreier F, Fliers E, Voshol PJ, Van Eden CG, Havekes LM, Kalsbeek A, Van Heijningen CL, Sluiter AA, Mettenleiter TC, Romijn JA, Sauerwein HP, Buijs RM. Selective parasympathetic innervation of subcutaneous and intra-abdominal fat: functional implications. J Clin Invest. 2002. 110:1243–1250.

27. Lee SH, Ha HS, Park YJ, Lee JH, Yim HW, Yoon KH, Kang MI, Lee WC, Son HY, Park YM, Kwon HS. Identifying metabolically obese but normal-weight (MONW) individuals in a nondiabetic Korean population: the Chungju Metabolic disease Cohort (CMC) study. Clin Endocrinol (Oxf). 2011. 75:475–481.

28. Witte DR, Tesfaye S, Chaturvedi N, Eaton SE, Kempler P, Fuller JH. EURODIAB Prospective Complications Study Group. Risk factors for cardiac autonomic neuropathy in type 1 diabetes mellitus. Diabetologia. 2005. 48:164–171.

29. Yufu K, Takahashi N, Okada N, Wakisaka O, Shinohara T, Nakagawa M, Hara M, Yoshimatsu H, Saikawa T. Gender difference in baroreflex sensitivity to predict cardiac and cerebrovascular events in type 2 diabetic patients. Circ J. 2011. 75:1418–1423.

30. May O, Arildsen H. Long-term predictive power of simple function tests for cardiovascular autonomic neuropathy in diabetes: a population-based study. Acta Diabetol. 2011. 48:311–316.