Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Clinical Studies and Practice

Effect of bariatric surgery on microvascular dysfunction associated to metabolic syndrome: a 12-month prospective study

Abstract

Objective:

To prospectively evaluate the effect of weight loss after bariatric surgery on microvascular function in morbidly obese patients with and without metabolic syndrome (MetS).

Methods:

A cohort of morbidly obese patients with and without MetS was studied before surgery and after 12 months of surgery. Healthy lean controls were also examined. Microvascular function was assessed by postocclusive reactive hyperemia (PORH) at forearm skin evaluated by laser Doppler flowmetry (LDF). Cutaneous vascular conductance (CVC) was calculated from laser-Doppler skin blood flow and blood pressure. Regression analysis was performed to assess the contribution of different clinical, metabolic and biochemical parameters to microvascular function.

Results:

Before surgery, 62 obese patients, 39 with MetS and 23 without MetS, and 30 lean control subjects were analyzed. The absolute area under the hyperemic curve (AUCH) CVC of PORH was significantly decreased in obese patients compared with lean control subjects. One year after surgery, AUCH CVC significantly increased in patients free of MetS, including patients that had MetS before surgery. In contrast, AUCH CVC did not significantly change in patients in whom MetS persisted after surgery. Stepwise multivariate regression analysis showed that only changes in HDL cholesterol (HDL-C) and oxidized LDL (oxLDL) independently predicted improvement of AUCH after surgery. These two variables together accounted for 40.9% of the variability of change in AUCH CVC after surgery.

Conclusions:

Bariatric surgery could significantly improve microvascular dysfunction in obese patients, but only in patients free of MetS after surgery. Improvement of microvascular dysfunction is strictly associated to postoperative increase in HDL-C levels and decrease in oxLDL levels.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1

Similar content being viewed by others

References

  1. Stapleton PA, James ME, Goodwill AG, Frisbee JC . Obesity and vascular dysfunction. Pathophysiology 2008; 15: 79–89.

    Article  CAS  Google Scholar 

  2. de Jongh RT, Serne EH, IJ RG, de Vries G, Stehouwer CD . Impaired microvascular function in obesity: implications for obesity-associated microangiopathy, hypertension, and insulin resistance. Circulation 2004; 109: 2529–2535.

    Article  Google Scholar 

  3. De Boer MP, Meijer RI, Wijnstok NJ, Jonk AM, Houben AJ, Stehouwer CD et al. Microvascular dysfunction: a potential mechanism in the pathogenesis of obesity-associated insulin resistance and hypertension. Microcirculation 2012; 19: 5–18.

    Article  CAS  Google Scholar 

  4. Roustit M, Cracowski JL . Assessment of endothelial and neurovascular function in human skin microcirculation. Trends Pharmacol Sci 2013; 34: 373–384.

    Article  CAS  Google Scholar 

  5. Roustit M, Cracowski JL . Non-invasive assessment of skin microvascular function in humans: an insight into methods. Microcirculation 2012; 19: 47–64.

    Article  Google Scholar 

  6. Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K et al. Bariatric surgery: a systematic review and meta-analysis. Jama 2004; 292: 1724–1737.

    Article  CAS  Google Scholar 

  7. Sjostrom L, Lindroos AK, Peltonen M, Torgerson J, Bouchard C, Carlsson B et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med 2004; 351: 2683–2693.

    Article  Google Scholar 

  8. Sjostrom L, Narbro K, Sjostrom CD, Karason K, Larsson B, Wedel H et al. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med 2007; 357: 741–752.

    Article  Google Scholar 

  9. Vest AR, Heneghan HM, Agarwal S, Schauer PR, Young JB . Bariatric surgery and cardiovascular outcomes: a systematic review. Heart 2012; 98: 1763–1777.

    Article  Google Scholar 

  10. Rossi M, Nannipieri M, Anselmino M, Pesce M, Muscelli E, Santoro G et al. Skin vasodilator function and vasomotion in patients with morbid obesity: effects of gastric bypass surgery. Obes Surg 2011; 21: 87–94.

    Article  Google Scholar 

  11. Lind L, Zethelius B, Sundbom M, Eden Engstrom B, Karlsson FA . Vasoreactivity is rapidly improved in obese subjects after gastric bypass surgery. Int J Obes (Lond) 2009; 33: 1390–1395.

    Article  CAS  Google Scholar 

  12. Williams IL, Chowienczyk PJ, Wheatcroft SB, Patel AG, Sherwood RA, Momin A et al. Endothelial function and weight loss in obese humans. Obes Surg 2005; 15: 1055–1060.

    Article  Google Scholar 

  13. Brethauer SA, Heneghan HM, Eldar S, Gatmaitan P, Huang H, Kashyap S et al. Early effects of gastric bypass on endothelial function, inflammation, and cardiovascular risk in obese patients. Surg Endosc 2011; 25: 2650–2659.

    Article  Google Scholar 

  14. Gokce N, Vita JA, McDonnell M, Forse AR, Istfan N, Stoeckl M et al. Effect of medical and surgical weight loss on endothelial vasomotor function in obese patients. Am J Cardiol 2005; 95: 266–268.

    Article  Google Scholar 

  15. Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C . Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 2004; 109: 433–438.

    Article  Google Scholar 

  16. Gastrointestinal surgery for severe obesity: National Institutes of Health Consensus Development Conference Statement. Am J Clin Nutr 1992; 55: 615S–619S.

  17. Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults. Executive Summary of The Third Report of The National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, And Treatment of High Blood Cholesterol In Adults (Adult Treatment Panel III). Jama 2001; 285: 2486–2497.

    Article  Google Scholar 

  18. Friedewald WT, Levy RI, Fredrickson DS . Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972; 18: 499–502.

    CAS  Google Scholar 

  19. Jimenez-Morales AI, Ruano J, Delgado-Lista J, Fernandez JM, Camargo A, Lopez-Segura F et al. NOS3 Glu298Asp polymorphism interacts with virgin olive oil phenols to determine the postprandial endothelial function in patients with the metabolic syndrome. J Clin Endocrinol Metab 2011; 96: E1694–E1702.

    Article  CAS  Google Scholar 

  20. Fleiss J . The Design and Analysis of Clinical Experiments. John Wiley & Sons: New York, 1986.

    Google Scholar 

  21. Donald AE, Charakida M, Cole TJ, Friberg P, Chowienczyk PJ, Millasseau SC et al. Non-invasive assessment of endothelial function: which technique? J Am Coll Cardiol 2006; 48: 1846–1850.

    Article  CAS  Google Scholar 

  22. Harris RA, Padilla J, Hanlon KP, Rink LD, Wallace JP . Reproducibility of the flow-mediated dilation response to acute exercise in overweight men. Ultrasound Med Biol 2007; 33: 1579–1585.

    Article  Google Scholar 

  23. Faul F, Erdfelder E, Lang AG, Buchner A . G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 2007; 39: 175–191.

    Article  Google Scholar 

  24. Samuel I, Mason EE, Renquist KE, Huang YH, Zimmerman MB, Jamal M . Bariatric surgery trends: an 18-year report from the International Bariatric Surgery Registry. Am J Surg 2006; 192: 657–662.

    Article  Google Scholar 

  25. Serne EH, de Jongh RT, Eringa EC, IJ RG, Stehouwer CD . Microvascular dysfunction: a potential pathophysiological role in the metabolic syndrome. Hypertension 2007; 50: 204–211.

    Article  CAS  Google Scholar 

  26. Levy BI, Schiffrin EL, Mourad JJ, Agostini D, Vicaut E, Safar ME et al. Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus. Circulation 2008; 118: 968–976.

    Article  Google Scholar 

  27. Tibirica E, Matheus AS, Nunes B, Sperandei S, Gomes MB . Repeatability of the evaluation of systemic microvascular endothelial function using laser doppler perfusion monitoring: clinical and statistical implications. Clinics (Sao Paulo) 2011; 66: 599–605.

    Google Scholar 

  28. Yvonne-Tee GB, Rasool AH, Halim AS, Rahman AR . Reproducibility of different laser Doppler fluximetry parameters of postocclusive reactive hyperemia in human forearm skin. J Pharmacol Toxicol Methods 2005; 52: 286–292.

    Article  CAS  Google Scholar 

  29. Agarwal SC, Allen J, Murray A, Purcell IF . Comparative reproducibility of dermal microvascular blood flow changes in response to acetylcholine iontophoresis, hyperthermia and reactive hyperaemia. Physiol Meas 2010; 31: 1–11.

    Article  Google Scholar 

  30. Roustit M, Blaise S, Millet C, Cracowski JL . Reproducibility and methodological issues of skin post-occlusive and thermal hyperemia assessed by single-point laser Doppler flowmetry. Microvasc Res 2010; 79: 102–108.

    Article  CAS  Google Scholar 

  31. Stiefel P, Moreno-Luna R, Vallejo-Vaz AJ, Beltran LM, Costa A, Gomez L et al. Which parameter is better to define endothelial dysfunction in a test of postocclusive hyperemia measured by laser-Doppler flowmetry? Coron Artery Dis 2012; 23: 57–61.

    Article  Google Scholar 

  32. Kruger A, Stewart J, Sahityani R, O’Riordan E, Thompson C, Adler S et al. Laser Doppler flowmetry detection of endothelial dysfunction in end-stage renal disease patients: correlation with cardiovascular risk. Kidney Int 2006; 70: 157–164.

    Article  CAS  Google Scholar 

  33. Yamamoto-Suganuma R, Aso Y . Relationship between post-occlusive forearm skin reactive hyperaemia and vascular disease in patients with Type 2 diabetes—a novel index for detecting micro- and macrovascular dysfunction using laser Doppler flowmetry. Diabet Med 2009; 26: 83–88.

    Article  CAS  Google Scholar 

  34. Rossi M, Bradbury A, Magagna A, Pesce M, Taddei S, Stefanovska A . Investigation of skin vasoreactivity and blood flow oscillations in hypertensive patients: effect of short-term antihypertensive treatment. J Hypertens 2011; 29: 1569–1576.

    Article  CAS  Google Scholar 

  35. Galle J, Hansen-Hagge T, Wanner C, Seibold S . Impact of oxidized low density lipoprotein on vascular cells. Atherosclerosis 2006; 185: 219–226.

    Article  CAS  Google Scholar 

  36. Tran-Dinh A, Diallo D, Delbosc S, Varela-Perez LM, Dang QB, Lapergue B et al. HDL and endothelial protection. Br J Pharmacol 2013; 169: 493–511.

    Article  CAS  Google Scholar 

  37. Garrido-Sanchez L, Garcia-Almeida JM, Garcia-Serrano S, Cardona I, Garcia-Arnes J, Soriguer F et al. Improved carbohydrate metabolism after bariatric surgery raises antioxidized LDL antibody levels in morbidly obese patients. Diabetes Care 2008; 31: 2258–2264.

    Article  CAS  Google Scholar 

  38. Persegol L, Verges B, Foissac M, Gambert P, Duvillard L . Inability of HDL from type 2 diabetic patients to counteract the inhibitory effect of oxidised LDL on endothelium-dependent vasorelaxation. Diabetologia 2006; 49: 1380–1386.

    Article  CAS  Google Scholar 

  39. Matsuda Y, Hirata K, Inoue N, Suematsu M, Kawashima S, Akita H et al. High density lipoprotein reverses inhibitory effect of oxidized low density lipoprotein on endothelium-dependent arterial relaxation. Circ Res 1993; 72: 1103–1109.

    Article  CAS  Google Scholar 

  40. Duffy D, Rader DJ . Update on strategies to increase HDL quantity and function. Nat Rev Cardiol 2009; 6: 455–463.

    Article  Google Scholar 

  41. Matsuo Y, Oberbach A, Till H, Inge TH, Wabitsch M, Moss A et al. Impaired HDL function in obese adolescents: Impact of lifestyle intervention and bariatric surgery. Obesity (Silver Spring) 2013; 21: E687–E695.

    Article  CAS  Google Scholar 

  42. Cracowski JL, Gaillard-Bigot F, Cracowski C, Sors C, Roustit M, Millet C . Involvement of cytochrome epoxygenase metabolites in cutaneous postocclusive hyperemia in humans. J Appl Physiol 2013; 114: 245–251.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Funding for this study was provided by the Andalusian Regional Ministry of Health (PI-0269/2008). We thank Rocío Infante-Fontán for technical assistance with biochemical analyses. We also thank Francisco J Tinahones and José Manuel Fernández Real for critical review of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to A Leal-Cerro or D A Cano.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Additional information

Supplementary Information accompanies this paper on International Journal of Obesity website

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martín-Rodríguez, J., Cervera-Barajas, A., Madrazo-Atutxa, A. et al. Effect of bariatric surgery on microvascular dysfunction associated to metabolic syndrome: a 12-month prospective study. Int J Obes 38, 1410–1415 (2014). https://doi.org/10.1038/ijo.2014.15

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2014.15

Keywords

This article is cited by

Search

Quick links