Advertisement

Bariatric surgery improves lipoprotein profile in morbidly obese patients by reducing LDL cholesterol, apoB, and SAA/PON1 ratio, increasing HDL cholesterol, but has no effect on cholesterol efflux capacity

Published:October 25, 2017DOI:https://doi.org/10.1016/j.jacl.2017.10.007

      Highlights

      • The effects of bariatric surgery on lipid profile in obese patients were evaluated.
      • Bariatric surgery has favorable effects on triglycerides, low-density lipoprotein cholesterol, and apolipoprotein (apo) B.
      • Surgery also increases high-density lipoprotein cholesterol and apoA1 and reduces apoB/apoA1 ratio and SAA1/PON1 ratio.
      • No changes in macrophage cholesterol efflux capacity was observed.

      Background

      Bariatric surgery has been shown to reduce cardiovascular events and cause-specific mortality for coronary artery disease in obese patients. Lipoprotein biomarkers relating to low-density lipoprotein (LDL), high-density lipoprotein (HDL), their subfractions, and macrophage cholesterol efflux have all been hypothesized to be of value in cardiovascular risk assessment.

      Objectives

      The objective of this study was to examine the effect of a lifestyle intervention followed by bariatric surgery on the lipid profile of morbidly obese patients.

      Methods

      Thirty-four morbidly obese patients were evaluated before and after lifestyle changes and then 1 year after bariatric surgery. They were compared with 17 lean subjects. Several lipoprotein metrics, serum amyloid A (SAA), serum paraoxonase-1 (PON1), and macrophage cholesterol efflux capacity (CEC) were assessed.

      Results

      Average weight loss after the lifestyle intervention was 10.5% and 1 year after bariatric surgery was 33.9%. The lifestyle intervention significantly decreased triglycerides (TGs; −28.7 mg/dL, P < .05), LDL cholesterol (LDL-C; −32.3 mg/dL, P < .0001), and apolipoprotein B (apoB; −62.9 μg/mL, P < .001). Bariatric surgery further reduced TGs (−36.7 mg/dL, P < .05), increased HDL cholesterol (+12 mg/dL, P < .0001), and reductions in LDL-C and apoB were sustained. Bariatric surgery reduced large, buoyant LDL (P < .0001), but had no effect on the small, dense LDL. The large HDL subfractions increased (P < .0001), but there was no effect on the smaller HDL subfractions. The ratio for SAA/PON1 was reduced after the lifestyle intervention (P < .01) and further reduced after bariatric surgery (P < .0001). Neither the lifestyle intervention nor bariatric surgery had any effect on CEC.

      Conclusions

      Lifestyle intervention followed by bariatric surgery in 34 morbidly obese patients showed favorable effects on TGs, LDL-C, and apoB. HDL cholesterol and apoA1 was increased, apoB/apoA1 ratio as well as SAA/PON1 ratio reduced, but bariatric surgery did not influence CEC.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Clinical Lipidology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • World Health Organization
        Obesity and Overweight - Fact Sheet.
        2016 (Available at:) (Accessed May 2017)
        • Centers for Disease Control and Prevention
        Childhood Obesity Facts.
        2016 (Available at:) (Accessed May 2017)
        • Beamish A.J.
        • Olbers T.
        • Kelly A.S.
        • Inge T.H.
        Cardiovascular effects of bariatric surgery.
        Nat Rev Cardiol. 2016; 13: 730-743
        • Poirier P.
        • Giles T.D.
        • Bray G.A.
        • et al.
        Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss.
        Arterioscler Thromb Vasc Biol. 2006; 26: 968-976
        • Adams T.D.
        • Mehta T.S.
        • Davidson L.E.
        • Hunt S.C.
        All-cause and cause-specific mortality associated with bariatric surgery: a review.
        Curr Atheroscler Rep. 2015; 17: 74
        • Ridker P.M.
        LDL cholesterol: controversies and future therapeutic directions.
        Lancet. 2014; 384: 607-617
        • Carmena R.
        • Duriez P.
        • Fruchart J.C.
        Atherogenic lipoprotein particles in atherosclerosis.
        Circulation. 2004; 109: III2-III7
        • Nikolic D.
        • Katsiki N.
        • Montalto G.
        • Isenovic E.R.
        • Mikhailidis D.P.
        • Rizzo M.
        Lipoprotein subfractions in metabolic syndrome and obesity: clinical significance and therapeutic approaches.
        Nutrients. 2013; 5: 928-948
        • St-Pierre A.C.
        • Ruel I.L.
        • Cantin B.
        • et al.
        Comparison of various electrophoretic characteristics of LDL particles and their relationship to the risk of ischemic heart disease.
        Circulation. 2001; 104: 2295-2299
        • Rohatgi A.
        • Khera A.
        • Berry J.D.
        • et al.
        HDL cholesterol efflux capacity and incident cardiovascular events.
        N Engl J Med. 2014; 371: 2383-2393
        • Gebhard C.
        • Rhainds D.
        • Tardif J.C.
        HDL and cardiovascular risk: is cholesterol in particle subclasses relevant?.
        Eur Heart J. 2015; 36: 10-12
        • Du X.-M.
        • Kim M.-J.
        • Hou L.
        • et al.
        HDL particle size is a critical determinant of ABCA1-mediated macrophage cellular cholesterol export.
        Circ Res. 2015; 116: 1133-1142
        • Mackness M.
        • Mackness B.
        Human paraoxonase-1 (PON1): gene structure and expression, promiscuous activities and multiple physiological roles.
        Gene. 2015; 567: 12-21
        • Han C.Y.
        • Tang C.
        • Guevara M.E.
        • et al.
        Serum amyloid A impairs the antiinflammatory properties of HDL.
        J Clin Invest. 2016; 126: 796
        • Kotani K.
        • Yamada T.
        • Gugliucci A.
        Paired measurements of paraoxonase 1 and serum amyloid A as useful disease markers.
        Biomed Res Int. 2013; 2013: 481437
        • Trøseid M.
        • Nestvold T.K.
        • Rudi K.
        • et al.
        Plasma lipopolysaccharide is closely associated with glycemic control and abdominal obesity: evidence from bariatric surgery.
        Diabetes Care. 2013; 36: 3627-3632
        • Nestvold T.K.
        • Nielsen E.W.
        • Lappegård K.T.
        Bariatric surgery reduces risk factors for development of type 2 diabetes mellitus in morbidly obese, nondiabetic patients.
        Metab Syndr Relat Disord. 2013; 11: 441-446
        • Chang S.H.
        • Stoll C.R.
        • Song J.
        • Varela J.E.
        • Eagon C.J.
        • Colditz G.A.
        The effectiveness and risks of bariatric surgery: an updated systematic review and meta-analysis, 2003-2012.
        JAMA Surg. 2014; 149: 275-287
        • Garcia-Sanchez C.
        • Posadas-Romero C.
        • Posadas-Sanchez R.
        • et al.
        Evolution of lipid profiles after bariatric surgery.
        Obes Surg. 2012; 22: 609-616
        • Huang H.
        • Kasumov T.
        • Gatmaitan P.
        • et al.
        Gastric bypass surgery reduces plasma ceramide subspecies and improves insulin sensitivity in severely obese patients.
        Obesity (Silver Spring). 2011; 19: 2235-2240
        • Hofso D.
        • Nordstrand N.
        • Johnson L.K.
        • et al.
        Obesity-related cardiovascular risk factors after weight loss: a clinical trial comparing gastric bypass surgery and intensive lifestyle intervention.
        Eur J Endocrinol. 2010; 163: 735-745
        • Kligman M.D.
        • Dexter D.J.
        • Omer S.
        • Park A.E.
        Shrinking cardiovascular risk through bariatric surgery: application of Framingham risk score in gastric bypass.
        Surgery. 2008; 143: 533-538
        • Williams D.B.
        • Hagedorn J.C.
        • Lawson E.H.
        • et al.
        Gastric bypass reduces biochemical cardiac risk factors.
        Surg Obes Relat Dis. 2007; 3: 8-13
        • Huerta S.
        • Li Z.
        • Anthony T.
        • Livingston E.H.
        Feasibility of a supervised inpatient low-calorie diet program for massive weight loss prior to RYGB in superobese patients.
        Obes Surg. 2010; 20: 173-180
        • Tzotzas T.
        • Filippatos T.D.
        • Triantos A.
        • et al.
        Effects of a low-calorie diet associated with weight loss on lipoprotein-associated phospholipase A2 (Lp-PLA2) activity in healthy obese women.
        Nutr Metab Cardiovasc Dis. 2008; 18: 477-482
        • Mooradian A.D.
        • Haas M.J.
        • Wehmeier K.R.
        • Wong N.C.
        Obesity-related changes in high-density lipoprotein metabolism.
        Obesity (Silver Spring). 2008; 16: 1152-1160
        • Schofield J.D.
        • Liu Y.
        • Rao-Balakrishna P.
        • Malik R.A.
        • Soran H.
        Diabetes dyslipidemia.
        Diabetes Ther. 2016; 7: 203-219
        • Diffenderfer M.R.
        • Schaefer E.J.
        The composition and metabolism of large and small LDL.
        Curr Opin Lipidol. 2014; 25: 221-226
        • Kaur N.
        • Pandey A.
        • Negi H.
        • et al.
        Effect of HDL-raising drugs on cardiovascular outcomes: a systematic review and meta-regression.
        PLoS One. 2014; 9: e94585
        • Voight B.F.
        • Peloso G.M.
        • Orho-Melander M.
        • et al.
        Plasma HDL cholesterol and risk of myocardial infarction: a mendelian randomisation study.
        Lancet. 2012; 380: 572-580
        • Kontush A.
        HDL-mediated mechanisms of protection in cardiovascular disease.
        Cardiovasc Res. 2014; 103: 341-349
        • Marsche G.
        • Saemann M.D.
        • Heinemann A.
        • Holzer M.
        Inflammation alters HDL composition and function: implications for HDL-raising therapies.
        Pharmacol Ther. 2013; 137: 341-351
        • Hutchins P.M.
        • Heinecke J.W.
        Cholesterol efflux capacity, macrophage reverse cholesterol transport and cardioprotective HDL.
        Curr Opin Lipidol. 2015; 26: 388-393
        • Hafiane A.
        • Genest J.
        High density lipoproteins: measurement techniques and potential biomarkers of cardiovascular risk.
        BBA Clin. 2015; 3: 175-188
        • Movva R.
        • Rader D.J.
        Laboratory assessment of HDL heterogeneity and function.
        Clin Chem. 2008; 54: 788-800
        • Asztalos B.F.
        • Swarbrick M.M.
        • Schaefer E.J.
        • et al.
        Effects of weight loss, induced by gastric bypass surgery, on HDL remodeling in obese women.
        J Lipid Res. 2010; 51: 2405-2412
        • Woudberg N.J.
        • Goedecke J.H.
        • Blackhurst D.
        • et al.
        Association between ethnicity and obesity with high-density lipoprotein (HDL) function and subclass distribution.
        Lipids Health Dis. 2016; 15: 92
        • Rader D.J.
        • Alexander E.T.
        • Weibel G.L.
        • Billheimer J.
        • Rothblat G.H.
        The role of reverse cholesterol transport in animals and humans and relationship to atherosclerosis.
        J Lipid Res. 2009; 50 Suppl: S189-S194
        • Cuchel M.
        • Rader D.J.
        Macrophage reverse cholesterol transport: key to the regression of atherosclerosis?.
        Circulation. 2006; 113: 2548-2555
        • Sankaranarayanan S.
        • Kellner-Weibel G.
        • de la Llera-Moya M.
        • et al.
        A sensitive assay for ABCA1-mediated cholesterol efflux using BODIPY-cholesterol.
        J Lipid Res. 2011; 52: 2332-2340
        • Davidson W.S.
        • Heink A.
        • Sexmith H.
        • et al.
        The effects of apolipoprotein B depletion on HDL subspecies composition and function.
        J Lipid Res. 2016; 57: 674-686
        • James R.W.
        A long and winding road: defining the biological role and clinical importance of paraoxonases.
        Clin Chem Lab Med. 2006; 44: 1052-1059
        • Karlsson H.
        • Kontush A.
        • James R.W.
        Functionality of HDL: antioxidation and detoxifying effects.
        Handb Exp Pharmacol. 2015; 224: 207-228
        • Bhattacharyya T.
        • Nicholls S.J.
        • Topol E.J.
        • et al.
        Relationship of paraoxonase 1 (PON1) gene polymorphisms and functional activity with systemic oxidative stress and cardiovascular risk.
        JAMA. 2008; 299: 1265-1276
        • Tang W.H.
        • Hartiala J.
        • Fan Y.
        • et al.
        Clinical and genetic association of serum paraoxonase and arylesterase activities with cardiovascular risk.
        Arterioscler Thromb Vasc Biol. 2012; 32: 2803-2812
        • Oberbach A.
        • von Bergen M.
        • Bluher S.
        • Lehmann S.
        • Till H.
        Combined serum proteomic and metabonomic profiling after laparoscopic sleeve gastrectomy in children and adolescents.
        J Laparoendosc Adv Surg Tech A. 2012; 22: 184-188
        • Uzun H.
        • Zengin K.
        • Taskin M.
        • Aydin S.
        • Simsek G.
        • Dariyerli N.
        Changes in leptin, plasminogen activator factor and oxidative stress in morbidly obese patients following open and laparoscopic Swedish adjustable gastric banding.
        Obes Surg. 2004; 14: 659-665
        • Chevrier J.
        • Dewailly E.
        • Ayotte P.
        • Mauriege P.
        • Despres J.P.
        • Tremblay A.
        Body weight loss increases plasma and adipose tissue concentrations of potentially toxic pollutants in obese individuals.
        Int J Obes Relat Metab Disord. 2000; 24: 1272-1278
        • Williams P.T.
        • Zhao X.Q.
        • Marcovina S.M.
        • Otvos J.D.
        • Brown B.G.
        • Krauss R.M.
        Comparison of four methods of analysis of lipoprotein particle subfractions for their association with angiographic progression of coronary artery disease.
        Atherosclerosis. 2014; 233: 713-720