Obesity Surgery

, Volume 25, Issue 3, pp 477–485 | Cite as

Epicardial and Pericardial Fat in Type 2 Diabetes: Favourable Effects of Biliopancreatic Diversion

  • Ana Carolina Junqueira Vasques
  • José Carlos Pareja
  • José Roberto Mattos Souza
  • Ademar Yamanaka
  • Maria da Saúde de Oliveira
  • Fernanda Satake Novaes
  • Élinton Adami Chaim
  • Francesca Piccinini
  • Chiara Dalla Man
  • Claudio Cobelli
  • Bruno Geloneze
Original Contributions



Ectopic fat is often identified in obese subjects who are susceptible to the development of type 2 diabetes mellitus (T2DM). The ectopic fat favours the decrease in insulin sensitivity (IS) and adiponectin levels. We aimed to evaluate the effect of biliopancreatic diversion (BPD) on the accumulation of ectopic fat, adiponectin levels and IS in obese with T2DM.

Materials and Methods

A nonrandomised controlled study was performed on sixty-eight women: 19 lean-control (23.0 ± 2.2 kg/m2) and 18 obese-control (35.0 ± 4.8 kg/m2) with normal glucose tolerance and 31 obese with T2DM (36.3 ± 3.7 kg/m2). Of the 31 diabetic women, 20 underwent BPD and were reassessed 1 month and 12 months after surgery. The subcutaneous adipose tissue, visceral adipose tissue, epicardial adipose tissue and pericardial adipose tissue were evaluated by ultrasonography. The IS was assessed by a hyperglycaemic clamp, applying the minimal model of glucose.


One month after surgery, there was a reduction in visceral and subcutaneous adipose tissues, whereas epicardial and pericardial adipose tissues exhibited significant reduction at the 12-month assessment (p < 0.01). Adiponectin levels and IS were normalised 1 month after surgery, resembling lean-control values and elevated above the obese-control values (p < 0.01). After 12 months, the improvement in IS and adiponectin was maintained, and 17 of the 20 operated patients exhibited fasting glucose and glycated haemoglobin within the normal range.


After BPD, positive physiological adaptations occurred in grade I and II obese patients with T2DM. These adaptations relate to the restoration of IS and decreased adiposopathy and explain the acute (1 month) and chronic (12 months) improvements in the glycaemic control.


Epicardial adipose tissue Obesity Type 2 diabetes mellitus Biliopancreatic diversion surgery Hyperglycaemic clamp Insulin sensitivity 



The funds were provided by the Sao Paulo Research Foundation—FAPESP, grants n. 2008/09451-7 and n. 2008/07312-0.

Conflict of Interest

The authors Ana Carolina Junqueira Vasques, José Carlos Pareja, José Roberto Mattos Souza, Ademar Yamanaka, Maria da Saúde de Oliveira, Fernanda Satake Novaes, Élinton Adami Chaim, Francesca Piccinini, Chiara Dalla Man, Claudio Cobelli and Bruno Geloneze declare that they have no conflict of interest reported.

“All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.”


  1. 1.
    Bays HE. Adiposopathy is “sick fat” a cardiovascular disease? J Am Coll Cardiol. 2011;57:2461–73.CrossRefPubMedGoogle Scholar
  2. 2.
    Nolan CJ, Damm P, Prentki M. Type 2 diabetes across generations: from pathophysiology to prevention and management. Lancet. 2011;378:169–81.CrossRefPubMedGoogle Scholar
  3. 3.
    Britton KA, Fox CS. Ectopic fat depots and cardiovascular disease. Circulation. 2011;124:e837–41.CrossRefPubMedGoogle Scholar
  4. 4.
    Wajchenberg BL, Giannella-Neto D, da Silva ME, et al. Depot-specific hormonal characteristics of subcutaneous and visceral adipose tissue and their relation to the metabolic syndrome. Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme 2002;34:616–21.Google Scholar
  5. 5.
    Iacobellis G, Malavazos AE, Corsi MM. Epicardial fat: from the biomolecular aspects to the clinical practice. Int J Biochem Cell Biol. 2011;43:1651–4.CrossRefPubMedGoogle Scholar
  6. 6.
    Chen X, Jiao Z, Wang L, et al. Roles of human epicardial adipose tissue in coronary artery atherosclerosis. J Huazhong Univ Sci Technol Med Sci. 2010;30:589–93.CrossRefPubMedGoogle Scholar
  7. 7.
    Standards of medical care in diabetes--2012. Diabetes Care 2012;35:dc12–s011.Google Scholar
  8. 8.
    Dixon JB, Zimmet P, Alberti KG, et al. Bariatric surgery: an IDF statement for obese Type 2 diabetes. Arq Bras Endocrinol Metabol. 2011;55:367–82.CrossRefPubMedGoogle Scholar
  9. 9.
    Dixon JB, le Roux CW, Rubino F, et al. Bariatric surgery for type 2 diabetes. Lancet. 2012;379(9833):2300–11.CrossRefPubMedGoogle Scholar
  10. 10.
    Buchwald H, Estok R, Fahrbach K, et al. Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med. 2009;122(3):248–56.CrossRefPubMedGoogle Scholar
  11. 11.
    Mari A, Manco M, Guidone C, et al. Restoration of normal glucose tolerance in severely obese patients after bilio-pancreatic diversion: role of insulin sensitivity and beta cell function. Diabetologia. 2006;49(9):2136–43.CrossRefPubMedGoogle Scholar
  12. 12.
    Scopinaro N, Adami GF, Papadia FS, et al. The effects of biliopancreatic diversion on type 2 diabetes mellitus in patients with mild obesity (BMI 30–35 kg/m2) and simple overweight (BMI 25–30 kg/m2): a prospective controlled study. Obes Surg. 2011;21(7):880–8.CrossRefPubMedGoogle Scholar
  13. 13.
    Guidone C, Manco M, Valera-Mora E, et al. Mechanisms of recovery from type 2 diabetes after malabsorptive bariatric surgery. Diabetes. 2006;55(7):2025–31.CrossRefPubMedGoogle Scholar
  14. 14.
    Executive summary: standards of medical care in diabetes--2012. Diabetes Care 2012;35(Suppl 1):S4–S10Google Scholar
  15. 15.
    Scopinaro N, Gianetta E, Civalleri D, et al. Bilio-pancreatic bypass for obesity: II. Initial experience in man. Br J Surg. 1979;66(9):618–20.CrossRefPubMedGoogle Scholar
  16. 16.
    Ribeiro-Filho FF, Faria AN, Azjen S, et al. Methods of estimation of visceral fat: advantages of ultrasonography. Obes Res. 2003;11(12):1488–94.CrossRefPubMedGoogle Scholar
  17. 17.
    Iacobellis G, Assael F, Ribaudo MC, et al. Epicardial fat from echocardiography: a new method for visceral adipose tissue prediction. Obes Res. 2003;11(2):304–10.CrossRefPubMedGoogle Scholar
  18. 18.
    Iacobellis G. Epicardial and pericardial fat: close, but very different. Obesity (Silver Spring). 2009;17(4):625.CrossRefGoogle Scholar
  19. 19.
    Mitrakou A, Vuorinen-Markkola H, Raptis G, et al. Simultaneous assessment of insulin secretion and insulin sensitivity using a hyperglycemia clamp. J Clin Endocrinol Metab. 1992;75(2):379–82.PubMedGoogle Scholar
  20. 20.
    Cobelli C, Caumo A, Omenetto M. Minimal model SG overestimation and SI underestimation: improved accuracy by a Bayesian two-compartment model. Am J Physiol. 1999;277(3 Pt 1):E481–8.PubMedGoogle Scholar
  21. 21.
    Gaborit B, Jacquier A, Kober F, et al. Effects of bariatric surgery on cardiac ectopic fat: lesser decrease in epicardial fat compared to visceral fat loss and no change in myocardial triglyceride content. J Am Coll Cardiol. 2012;60(15):1381–9.CrossRefPubMedGoogle Scholar
  22. 22.
    Willens HJ, Byers P, Chirinos JA, et al. Effects of weight loss after bariatric surgery on epicardial fat measured using echocardiography. Am J Cardiol. 2007;99(9):1242–5.CrossRefPubMedGoogle Scholar
  23. 23.
    Greco AV, Mingrone G, Giancaterini A, et al. Insulin resistance in morbid obesity: reversal with intramyocellular fat depletion. Diabetes. 2002;51(1):144–51.CrossRefPubMedGoogle Scholar
  24. 24.
    Capurso C, Capurso A. From excess adiposity to insulin resistance: the role of free fatty acids. Vascul Pharmacol. 2012;57(2–4):91–7.CrossRefPubMedGoogle Scholar
  25. 25.
    Vasques AC, Souza JR, Yamanaka A, et al. Sagittal abdominal diameter as a marker for epicardial adipose tissue in premenopausal women. Metabolism. 2013;62(7):1032–6.CrossRefPubMedGoogle Scholar
  26. 26.
    Salani B, Briatore L, Andraghetti G, et al. High-molecular weight adiponectin isoforms increase after biliopancreatic diversion in obese subjects. Obesity. 2006;14(9):1511–4.CrossRefPubMedGoogle Scholar
  27. 27.
    Salinari S, Bertuzzi A, Asnaghi S, et al. First-phase insulin secretion restoration and differential response to glucose load depending on the route of administration in type 2 diabetic subjects after bariatric surgery. Diabetes Care. 2009;32(3):375–80.CrossRefPubMedCentralPubMedGoogle Scholar
  28. 28.
    Lima MM, Pareja JC, Alegre SM, et al. Acute effect of Roux-en-Y gastric bypass on whole-body insulin sensitivity: a study with the euglycemic-hyperinsulinemic clamp. J Clin Endocrinol Metab. 2010;95(8):3871–5.CrossRefPubMedGoogle Scholar
  29. 29.
    Laferrere B. Diabetes remission after bariatric surgery: is it just the incretins? Int J Obes. 2011;35(3):143.Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Ana Carolina Junqueira Vasques
    • 1
    • 2
  • José Carlos Pareja
    • 2
    • 3
  • José Roberto Mattos Souza
    • 4
  • Ademar Yamanaka
    • 2
  • Maria da Saúde de Oliveira
    • 2
  • Fernanda Satake Novaes
    • 2
  • Élinton Adami Chaim
    • 3
  • Francesca Piccinini
    • 5
  • Chiara Dalla Man
    • 5
  • Claudio Cobelli
    • 5
  • Bruno Geloneze
    • 2
  1. 1.School of Applied Sciences (FCA)State University of Campinas, UNICAMPLimeiraBrazil
  2. 2.Laboratory of Investigation on Metabolism and Diabetes (LIMED), Gastrocentro, Faculty of Medical SciencesState University of Campinas, UNICAMPCampinasBrazil
  3. 3.Diabetic Surgery Unit, Department of SurgeryState University of Campinas, UNICAMPCampinasBrazil
  4. 4.Department of Cardiology, Faculty of Medical SciencesState University of Campinas, UNICAMPCampinasBrazil
  5. 5.Department of Information EngineeringUniversity of PadovaPadovaItaly

Personalised recommendations