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
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
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
Similar content being viewed by others
References
Stapleton PA, James ME, Goodwill AG, Frisbee JC . Obesity and vascular dysfunction. Pathophysiology 2008; 15: 79–89.
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.
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.
Roustit M, Cracowski JL . Assessment of endothelial and neurovascular function in human skin microcirculation. Trends Pharmacol Sci 2013; 34: 373–384.
Roustit M, Cracowski JL . Non-invasive assessment of skin microvascular function in humans: an insight into methods. Microcirculation 2012; 19: 47–64.
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.
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.
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.
Vest AR, Heneghan HM, Agarwal S, Schauer PR, Young JB . Bariatric surgery and cardiovascular outcomes: a systematic review. Heart 2012; 98: 1763–1777.
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.
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.
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.
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.
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.
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.
Gastrointestinal surgery for severe obesity: National Institutes of Health Consensus Development Conference Statement. Am J Clin Nutr 1992; 55: 615S–619S.
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.
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.
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.
Fleiss J . The Design and Analysis of Clinical Experiments. John Wiley & Sons: New York, 1986.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Galle J, Hansen-Hagge T, Wanner C, Seibold S . Impact of oxidized low density lipoprotein on vascular cells. Atherosclerosis 2006; 185: 219–226.
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.
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.
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.
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.
Duffy D, Rader DJ . Update on strategies to increase HDL quantity and function. Nat Rev Cardiol 2009; 6: 455–463.
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.
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.
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
Corresponding authors
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
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ijo.2014.15
Keywords
This article is cited by
-
Gastric Bypass Improves Microvascular Perfusion in Patients with Obesity
Obesity Surgery (2021)
-
Bile acid, glucose, lipid profile, and liver enzyme changes in prediabetic patients 1 year after sleeve gastrectomy
BMC Surgery (2020)
-
Short- and Long-Term Effects of Bariatric Surgery on Vascular Phenotype
Obesity Surgery (2019)
-
Microcirculatory Improvement Induced by Laparoscopic Sleeve Gastrectomy Is Related to Insulin Sensitivity Retrieval
Obesity Surgery (2018)
-
The Effects of Bariatric Surgery-Induced Weight Loss on Adipose Tissue in Morbidly Obese Women Depends on the Initial Metabolic Status
Obesity Surgery (2016)