Omentin changes following bariatric surgery and predictive links with biomarkers for risk of cardiovascular disease

Marc Lapointe, Paul Poirier, Julie Martin, Marjorie Bastien, Audrey Auclair, Katherine Cianflone, Marc Lapointe, Paul Poirier, Julie Martin, Marjorie Bastien, Audrey Auclair, Katherine Cianflone

Abstract

Background: Although no receptor has yet been identified, changes in circulating levels of the adipokine designated as Omentin have been demonstrated in obesity and related comorbidities such as cardiovascular disease, insulin resistance, metabolic syndrome and chronic inflammation.

Methods: Changes in Omentin levels at 1 and 5 days and 6 and 12 months in response to biliopancreatic diversion with duodenal switch bariatric surgery were evaluated, specifically to investigate if changes preceded gain of insulin sensitivity.

Results: Pre-operative plasma Omentin was not different between men (n = 18) vs women (n = 48), or diabetic status but correlated with body mass index (BMI). Altogether, Omentin increased as early as 24-h post-surgery, with changes maintained up to 1-year. Fifty-nine percent of subjects increased Omentin >10% by 24-H following surgery (OmentinINC p < 0.0001), while 18% of subjects decreased (OmentinDEC p < 0.0001), with changes maintained throughout one-year. These two groups had comparable age, sex distribution, diabetes, BMI, waist circumference and fat mass, however OmentinDEC had elevated levels of cardiovascular risk markers; homocysteine (p = 0.019), NT-proBNP (p = 0.006) and total bilirubin (p = 0.0001) while red blood cell (RBC) count was lower (p = 0.0005) over the one-year period. Omentin levels at 1-DAY also correlated with immune parameters (white blood cell count, % neutrophil, % monocytes, % lymphocytes).

Conclusion: OmentinDEC at 1 day following surgery may be a marker of cardiovascular "at-risk" group before weight loss or insulin sensitivity restoration.

Figures

Figure 1
Figure 1
Circulating Omentin levels and correlations in preoperative state. Fasting Omentin levels in the preoperative state were measured in all subjects. A: Fasting Omentin levels separated based on sex and presence/absence of diabetes. Results are given as mean ± SEM. B and C: Correlation (Spearman) of Omentin levels to lymphocyte counts and circulating acylation stimulating protein (ASP).
Figure 2
Figure 2
Fasting pre-operative and post-operative Omentin levels. A: Fasting levels of Omentin were measured pre-operative, and at 1 day, 5 days, 6 months and 12 months post-operatively. Results are presented as average ± SEM with analysis by ANOVA vs pre-operative levels. B: Pre-operative and 1 day levels of Omentin are given individually for subjects separated based on >10% increase (OmentinINC), >10% decrease (OmentinDEC), and no change in Omentin (neutral = OmentinNEU). C: Percent Omentin change across all time points is given for the OmentinINC (solid line) and the OmentinDEC (dotted line) group. Results are presented as average ± SEM with analysis by 2-way ANOVA. Significance is presented as *p < 0.05, **p < 0.01 and ***p < 0.001.
Figure 3
Figure 3
Pre-operative and post-operative results for cardiovascular risk factors presented for groups based on OmentinINCand OmentinDEC. Preoperative and postoperative results are presented for homocysteine (A), NT-proBNP (B), total bilirubin (C) and red blood cell counts (D) for the OmentinINC (solid line) and OmentinDEC (dotted line) groups over one year follow-up. Results are expressed as average ± SEM with analysis by 2-way ANOVA, significance for groups difference is indicated with post-hoc comparisons indicated: *** p < 0.001.

References

    1. Jaikanth C, Gurumurthy P, Cherian KM, Indhumathi T. Emergence of omentin as a pleiotropic adipocytokine. Exp Clin Endocrinol Diabetes. 2013;121:377–383. doi: 10.1055/s-0033-1345123.
    1. Schäffler A, Neumeier M, Herfarth H, Fürst A, Schölmerich J, Büchler C. Genomic structure of human omentin, a new adipocytokine expressed in omental adipose tissue. Biochim Biophys Acta. 2005;1732:96–102. doi: 10.1016/j.bbaexp.2005.11.005.
    1. Yang RZ, Lee MJ, Hu H, Pray J, Wu HB, Hansen BC, Shuldiner AR, Fried SK, McLenithan JC, Gong DW. Identification of omentin as a novel depot-specific adipokine in human adipose tissue: possible role in modulating insulin action. Am J Physiol Endocrinol Metab. 2006;290:E1253–E1261. doi: 10.1152/ajpendo.00572.2004.
    1. Kazama K, Usui T, Okada M, Hara Y, Yamawaki H. Omentin plays an anti-inflammatory role through inhibition of TNF-?-induced superoxide production in vascular smooth muscle cells. Eur J Pharmacol. 2012;686:116–123. doi: 10.1016/j.ejphar.2012.04.033.
    1. de Souza Batista CM, Yang RZ, Lee MJ, Glynn NM, Yu DZ, Pray J, Ndubuizu K, Patil S, Schwartz A, Kligman M, Fried SK, Gong DW, Shuldiner AR, Pollin TI, McLenithan JC. Omentin plasma levels and gene expression are decreased in obesity. Diabetes. 2007;56:1655–1661. doi: 10.2337/db06-1506.
    1. Shibata R, Ouchi N, Takahashi R, Terakura Y, Ohashi K, Ikeda N, Higuchi A, Terasaki H, Kihara S, Murohara T. Omentin as a novel biomarker of metabolic risk factors. Diabetol Metab Syndr. 2012;4:37. doi: 10.1186/1758-5996-4-37.
    1. Jialal I, Devaraj S, Kaur H, Adams-Huet B, Bremer AA. Increased chemerin and decreased omentin-1 in both adipose tissue and plasma in nascent metabolic syndrome. J Clin Endocrinol Metab. 2013;98:E514–E517. doi: 10.1210/jc.2012-3673.
    1. Liu R, Wang X, Bu P. Omentin-1 is associated with carotid atherosclerosis in patients with metabolic syndrome. Diabetes Res Clin Pract. 2011;93:21–25. doi: 10.1016/j.diabres.2011.03.001.
    1. Shibata R, Ouchi N, Kikuchi R, Takahashi R, Takeshita K, Kataoka Y, Ohashi K, Ikeda N, Kihara S, Murohara T. Circulating omentin is associated with coronary artery disease in men. Atherosclerosis. 2011;219:811–814. doi: 10.1016/j.atherosclerosis.2011.08.017.
    1. Yoo HJ, Hwang SY, Hong HC, Choi HY, Yang SJ, Seo JA, Kim SG, Kim NH, Choi KM, Choi DS, Baik SH. Association of circulating omentin-1 level with arterial stiffness and carotid plaque in type 2 diabetes. Cardiovasc Diabetol. 2011;10:103. doi: 10.1186/1475-2840-10-103.
    1. Pan HY, Guo L, Li Q. Changes of serum omentin-1 levels in normal subjects and in patients with impaired glucose regulation and with newly diagnosed and untreated type 2 diabetes. Diabetes Res Clin Pract. 2010;88:29–33. doi: 10.1016/j.diabres.2010.01.013.
    1. El-Mesallamy HO, El-Derany MO, Hamdy NM. Serum omentin-1 and chemerin levels are interrelated in patients with Type 2 diabetes mellitus with or without ischaemic heart disease. Diabet Med. 2011;28:1194–1200. doi: 10.1111/j.1464-5491.2011.03353.x.
    1. Moreno-Navarrete JM, Catalán V, Ortega F, Gómez-Ambrosi J, Ricart W, Frühbeck G: Fernández-Real JM. Circulating omentin concentration increases after weight loss. Nutr Metab (Lond) 2010;7:27. doi: 10.1186/1743-7075-7-27.
    1. Saremi A, Asghari M, Ghorbani A. Effects of aerobic training on serum omentin-1 and cardiometabolic risk factors in overweight and obese men. J Sports Sci. 2010;28:993–998. doi: 10.1080/02640414.2010.484070.
    1. Tan BK, Adya R, Farhatullah S, Lewandowski KC, O’Hare P, Lehnert H, Randeva HS. Omentin-1, a novel adipokine, is decreased in overweight insulin-resistant women with polycystic ovary syndrome: ex vivo and in vivo regulation of omentin-1 by insulin and glucose. Diabetes. 2008;57:801–808. doi: 10.2337/db07-0990.
    1. Poirier P, Cornier MA, Mazzone T, Stiles S, Cummings S, Klein S, McCullough PA, Ren Fielding C, Franklin BA. American heart association obesity committee of the council on nutrition, physical activity, and metabolism. Bariatric surgery and cardiovascular risk factors: a scientific statement from the American Heart Association. Circulation. 2011;123:1683–1701. doi: 10.1161/CIR.0b013e3182149099.
    1. Brethauer SA, Aminian A, Romero-Talamás H, Batayyah E, Mackey J, Kennedy L, Kashyap SR, Kirwan JP, Rogula T, Kroh M, Chand B, Schauer PR. Can diabetes be surgically cured? Long-term metabolic effects of bariatric surgery in obese patients with type 2 diabetes mellitus. Ann Surg. 2013;258:628–636.
    1. Sjöström L, Peltonen M, Jacobson P, Ahlin S, Andersson-Assarsson J, Anveden Å, Bouchard C, Carlsson B, Karason K, Lönroth H, Näslund I, Sjöström E, Taube M, Wedel H, Svensson PA, Sjöholm K, Carlsson LM. Association of bariatric surgery with long-term remission of type 2 diabetes and with microvascular and macrovascular complications. JAMA. 2014;311:2297–2304. doi: 10.1001/jama.2014.5988.
    1. Habib P, Scrocco JD, Terek M, Vanek V, Mikolich JR. Effects of bariatric surgery on inflammatory, functional and structural markers of coronary atherosclerosis. Am J Cardiol. 2009;104:1251–1255. doi: 10.1016/j.amjcard.2009.06.042.
    1. Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K, Schoelles K. Bariatric surgery: a systematic review and meta-analysis. JAMA. 2004;292:1724–1737. doi: 10.1001/jama.292.14.1724.
    1. Munkonda MN, Martin J, Poirier P, Carrington A, Biron S, Lebel S, Cianflone K. Acylation stimulating protein reduction precedes insulin sensitization after BPD-DS bariatric surgery in severely obese women. Nutr Diabetes. 2012;2:e41. doi: 10.1038/nutd.2012.13.
    1. 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.
    1. Hanusch-Enserer U, Hermann KM, Cauza E, Spak M, Mähr B, Dunky A, Rosen HR, Köller U, Prager R. Effect of gastric banding on aminoterminal pro-brain natriuretic peptide in the morbidly obese. Obes Res. 2003;11:695–698. doi: 10.1038/oby.2003.99.
    1. Görmüs U, Ozmen D, Ozmen B, Parildar Z, Ozdogan O, Mutaf I, Bayindir O. Serum N-terminal-pro-brain natriuretic peptide (NT-pro-BNP) and homocysteine levels in type 2 diabetic patients with asymptomatic left ventricular diastolic dysfunction. Diabetes Res Clin Pract. 2010;87:51–56. doi: 10.1016/j.diabres.2009.10.010.
    1. MacGowan GA, Neely D, Peaston R, Wrightson N, Parry G. Evaluation of NT-proBNP to predict outcomes in advanced heart failure. Int J Clin Pract. 2010;64:892–899. doi: 10.1111/j.1742-1241.2010.02388.x.
    1. Ahluwalia N, Blacher J, Szabo de Edelenyi F, Faure P, Julia C, Hercberg S, Galan P. Prognostic value of multiple emerging biomarkers in cardiovascular risk prediction in patients with stable cardiovascular disease. Atherosclerosis. 2013;228:478–484. doi: 10.1016/j.atherosclerosis.2013.03.017.
    1. Humphrey LL, Fu R, Rogers K, Freeman M, Helfand M. Homocysteine level and coronary heart disease incidence: a systematic review and meta-analysis. Clin Proc. 2008;83:1203–1212. doi: 10.4065/83.11.1203.
    1. Cho HC. The relationship among homocysteine, bilirubin, and diabetic retinopathy. Diab Metab J. 2011;35:595–601. doi: 10.4093/dmj.2011.35.6.595.
    1. Tzotzas T, Evangelou P, Kiortsis DN. Obesity, weight loss and conditional cardiovascular risk factors. Obes Rev. 2011;12:e282–e289. doi: 10.1111/j.1467-789X.2010.00807.x.
    1. Biegus J, Zymlinski R, Sokolski M, Nawrocka S, Siwolowski P, Szachniewicz J, Jankowska EA, Banasiak W, Ponikowski P. Liver function tests in patients with acute heart failure. Pol Arch Med Wewn. 2012;122:471–479.
    1. Onat A, Can G, Örnek E, Çiçek G, Ayhan E, Dogan Y. Serum Y-glutamyltransferase: independent predictor of risk of diabetes, hypertension, metabolic syndrome, and coronary disease. Obesity (Silver Spring) 2012;20:842–848. doi: 10.1038/oby.2011.136.
    1. Giral P, Ratziu V, Couvert P, Carrié A, Kontush A, Girerd X, Chapman MJ. Plasma bilirubin and gamma-glutamyltransferase activity are inversely related in dyslipidemic patients with metabolic syndrome: relevance to oxidative stress. Atherosclerosis. 2010;210:607–613. doi: 10.1016/j.atherosclerosis.2009.12.026.
    1. Narumi T, Watanabe T, Kadowaki S, Kinoshita D, Yokoyama M, Honda Y, Otaki Y, Nishiyama S, Takahashi H, Arimoto T, Shishido T, Miyamoto T, Kubota I. Impact of serum omentin-1 levels on cardiac prognosis in patients with heart failure. Cardiovasc Diabetol. 2014;13:84. doi: 10.1186/1475-2840-13-84.
    1. Kataoka Y, Shibata R, Ohashi K, Kambara T, Enomoto T, Uemura Y, Ogura Y, Yuasa D, Matsuo K, Nagata T, Oba T, Yasukawa H, Numaguchi Y, Sone T, Murohara T, Ouchi N. Omentin prevents myocardial ischemic injury through AMPK- and Akt-dependent mechanisms. J Am Coll Cardiol. 2014;63:2722–33. doi: 10.1016/j.jacc.2014.03.032.
    1. Tsuji S, Uehori J, Matsumoto M, Suzuki Y, Matsuhisa A, Toyoshima K, Seya T. Human intelectin is a novel soluble lectin that recognizes galactofuranose in carbohydrate chains of bacterial cell wall. J Biol Chem. 2001;276:23456–23463. doi: 10.1074/jbc.M103162200.
    1. Caricilli AM, Saad MJ. Gut microbiota composition and its effects on obesity and insulin resistance. Curr Opin Clin Nutr Metab Care. 2014;17:312–318. doi: 10.1097/MCO.0000000000000067.
    1. Erejuwa OO, Sulaiman SA, Ab Wahab MS. Modulation of gut microbiota in the management of metabolic disorders: the prospects and challenges. Int J Mol Sci. 2014;15:4158–4188. doi: 10.3390/ijms15034158.
    1. Onat A, Can G. Enhanced proinflammatory state and autoimmune activation: a breakthrough to understanding chronic diseases. Curr Pharm Des. 2014;20:575–584. doi: 10.2174/138161282004140213145551.

Source: PubMed

3
Abonner