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01-12-2015 | Original Contribution

Higher plasma lipopolysaccharide concentrations are associated with less favorable phenotype in overweight/obese men

Authors: Ana Paula Boroni Moreira, Raquel Duarte Moreira Alves, Tatiana Fiche Salles Teixeira, Viviane Silva Macedo, Leandro Licursi de Oliveira, Neuza Maria Brunoro Costa, Josefina Bressan, Maria do Carmo Gouveia Peluzio, Richard Mattes, Rita de Cássia Gonçalves Alfenas

Published in: European Journal of Nutrition | Issue 8/2015

Abstract

Purpose

Lipopolysaccharide (LPS) from the outer membrane of gram-negative bacteria might be an inflammation trigger in adipose tissue. It has recently been proposed that there is a link between adipose tissue distribution and blood LPS. However, the number of studies on this topic is scarce, and further investigation in humans is required. In this study, we explored the association between plasma LPS concentrations and body fat distribution, as well as the biochemical parameters that may indicate the presence of metabolic disorders.

Methods

Sixty-seven young adult men with body mass index of 26–35 kg/m² were evaluated. Anthropometry, body composition and body fat distribution, blood pressure, energy expenditure, physical activity level, dietary intake, and biochemical parameters were assessed.

Results

Men with median plasma LPS ≥ 0.9 EU/mL presented higher sagittal abdominal diameter, trunk fat percentage, and android fat percentage, and mass, insulin and alanine aminotransferase concentrations, homeostasis model assessment of insulin resistance (HOMA-IR), and beta cell dysfunction (HOMA-B) than those with lower plasma LPS. LPS correlated positively with the trunk fat percentage, and android fat percentage, and mass, insulin, aspartate aminotransferase, alanine aminotransferase, and alkaline phosphatase concentrations, as well as HOMA-IR and HOMA-B.

Conclusion

Our results suggest that a higher plasma LPS concentration is associated with a less favorable phenotype as characterized by higher central adiposity, higher values of HOMA-IR, and beta cell function impairment in overweight/obese men.

Vázquez-Vela MEF, Torres N, Tovar AR (2008) White adipose tissue as endocrine organ and its role in obesity. Arch Med Res 39:715–728CrossRef

Virtue S, Vidal-Puig A (2008) It’s not how fat you are, it’s what you do with it that counts. PLoS Biol 6:e237CrossRef

Montague CT, O’Rahilly S (2000) The perils of portliness: causes and consequences of visceral adiposity. Diabetes 49:883–888CrossRef

Lupattelli G, De Vuono S, Boni M, Helou R, Raffaele Mannarino M, Rita Roscini A, Alaeddin A, Pirro M, Vaudo G (2013) Insulin resistance and not BMI is the major determinant of early vascular impairment in patients with morbid obesity. J Atheroscler Thromb 20:924–933CrossRef

Ding S, Lund PK (2011) Role of intestinal inflammation as an early event in obesity and insulin resistance. Curr Opin Clin Nutr Metab Care 14:328–333CrossRef

Shanik MH, Xu Y, Skrha J, Dankner R, Zick Y, Roth J (2008) Insulin resistance and hyperinsulinemia: is hyperinsulinemia the cart or the horse? Diabetes Care 31:S262–S268CrossRef

Reaven GM (1991) Insulin resistance and compensatory hyperinsulinemia: role in hypertension, dyslipidemia, and coronary heart disease. Am Heart J 121(4 Pt 2):1283–1288CrossRef

Klöting N, Fasshauer M, Dietrich A, Kovacs P, Schön MR, Kern M, Stumvoll M, Blüher M (2010) Insulin-sensitive obesity. Am J Physiol Endocrinol Metab 299:E506–E515CrossRef

Ledoux S, Coupaye M, Essig M, Msika S, Roy C, Queguiner I, Clerici C, Larger E (2010) Traditional anthropometric parameters still predict metabolic disorders in women with severe obesity. Obesity 18:1026–1032CrossRef

10.

Könner AC, Brüning JC (2011) Toll-like receptors: linking inflammation to metabolism. Trends Endocrinol Metab 22:16–23CrossRef

11.

Brook JS, Lee JY, Finch SJ, Balka EB, Brook DW (2013) Physical factors, personal characteristics, and substance use: associations with obesity. Subst Abus 34:273–276CrossRef

12.

Trøseid M, Nestvold TK, Rudi K, Thoresen H, Nielse EW, Lappegard KT (2013) Plasma lipopolysaccharide is closely associated with glycemic control and abdominal obesity: evidence from bariatric surgery. Diabetes Care 36:3627–3632CrossRef

13.

Moreira APB, Teixeira TFS, Ferreira AB, Peluzio MCG, Alfenas RCG (2012) Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia. Br J Nutr 108:801–809CrossRef

14.

Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmée E, Cousin B, Sulpice T, Chamontin B, Ferrières J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56:1761–1772CrossRef

15.

Muccioli GG, Naslain D, Backhed F, Reigstad CS, Lambert DM, Delzenne NM, Cani PD (2010) The endocannabinoid system links gut microbiota to adipogenesis. Mol Syst Biol 6:392CrossRef

16.

Wang L, Li L, Ran X, Long M, Zhang M, Tao Y, Luo X, Wang Y, Jiao Y, Mao X, Ren J (2013) Lipopolysaccharides reduce adipogenesis in 3T3-L1 adipocytes through activation of NF-κB pathway and downregulation of AMPK expression. Cardiovasc Toxicol 13:338–346CrossRef

17.

Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS (2006) TLR4 links innate immunity and fatty acid—induced insulin resistance. J Clin Investig 116:3015–3025CrossRef

18.

Mehta NN, McGillicuddy FC, Anderson PD, Hinkle CC, Shah R, Pruscino L, Tabita-Martinez J, Sellers KF, Rickels MR, Reilly MP (2010) Experimental endotoxemia induces adipose inflammation and insulin resistance in humans. Diabetes 59:172–181CrossRef

19.

Liang H, Hussey SE, Sanchez-Avila A, Tantiwong P, Musi N (2013) Effect of lipopolysaccharide on inflammation and insulin action in human muscle. PLoS One 8:e63983CrossRef

20.

Pussinen PJ, Havulinna AS, Lehto M, Sundvall J, Salomaa V (2011) Endotoxemia is associated with an increased risk of incident diabetes. Diabetes Care 34:392–397CrossRef

21.

Miller MA, McTernan PG, Harte AL, Silva NF, Strazzullo P, Alberti KG, Kumar S, Cappuccio FP (2009) Ethnic and sex differences in circulating endotoxin levels: a novel marker of atherosclerotic and cardiovascular risk in a British multi-ethnic population. Atherosclerosis 203:494–502CrossRef

22.

Devaraj S, Dasu MR, Park SH, Jialal I (2009) Increased levels of ligands of toll-like receptors 2 and 4 in type 1 diabetes. Diabetologia 52:1665–1668CrossRef

23.

Creely SJ, McTernan PG, Kusminski CM, Fisher FM, Da Silva NF, Khanolkar M, Evans M, Harte AL, Kumar S (2007) Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am J Physiol Endocrinol Metab 292:E740–E747CrossRef

24.

Calori G, Lattuada G, Piemonti L, Garancini MP, Ragogna F, Villa M, Mannino S, Crosignani P, Bosi E, Luzi L, Ruotolo G, Perseghin G (2011) Prevalence, metabolic features, and prognosis of metabolically healthy obese italian individuals: the cremona study. Diabetes Care 34:210–215CrossRef

25.

Vasques ACJ, Rosado LEFPL, Rosado GP, Ribeiro RCL, Franceschini SCC, Geloneze B, Priore SE, Oliveira DR (2009) Habilidade de indicadores antropométricos e de composição corporal em identificar a resistência à insulin. Arq Bras Endocrinol Metab 53:72–79CrossRef

26.

Valdez R, Seidell JC, Ahn YI, Weiss KM (1993) A new index of abdominal adiposity as an indicator of risk for cardiovascular disease. A cross-population study. Int J Obes Relat Metab Disord 17:77–82

27.

Kahn HS, Austin H, Williamson DF, Arensberg D (1996) Simple anthropometric indices associated with ischemic heart disease. J Clin Epidemiol 49:1017–1024CrossRef

28.

World Health Organization (2001) Food and nutrition technical report series: human energy requirements. WHO, Joint FAO/WHO/UNU Expert Consultation, Rome

29.

Pardini R, Matsudo SMM, Araújo T, Matsudo V, Andrade E, Braggion C, Andrade D, Oliveira L, Figueira Júnior A, Raso V (2001) Validação do questionário internacional de nível de atividade física (IPAQ-versão 6): estudo piloto em adultos jovens brasileiros. Rev Bras Ciên Mov 9:45–51

30.

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

31.

Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419CrossRef

32.

Alberti KG, Zimmet P, Shaw J, IDF Epidemiology Task Force Consensus Group (2005) The metabolic syndrome: a new worldwide definition. Lancet 366:1059–1062CrossRef

33.

Item F, Konrad D (2012) Visceral fat and metabolic inflammation: the portal theory revisited. Obes Rev 13:30–39CrossRef

34.

Messier V, Karelis AD, Prud’homme D, Primeau V, Brochu M, Rabasa-Lhoret R (2010) Identifying metabolically healthy but obese individuals in sedentary postmenopausal women. Obesity 18:911–917CrossRef

35.

Lam YY, Mitchell AJ, Holmes AJ, Denyer GS, Gummesson A, Caterson ID, Hunt NH, Storlien LH (2011) Role of the gut in visceral fat inflammation and metabolic disorders. Obesity 19:2113–2120CrossRef

36.

Abbasi F, Blasey C, Reaven GM (2013) Cardiometabolic risk factors and obesity: does it matter whether BMI or waist circumference is the index of obesity? Am J Clin Nutr 98:637–640CrossRef

37.

Clemente-Postigo M, Queipo-Ortuño MI, Murri M, Boto-Ordoñez M, Perez-Martinez P, Andres-Lacueva C, Cardona F, Tinahones FJ (2012) Endotoxin increase after fat overload is related to postprandial hypertriacylglycerolemia in morbidly obese patients. J Lipid Res 53:973–978CrossRef

38.

Cornier M-A, Després J-P, Davis N, Grossniklaus DA, Klein S, Lamarche B, Lopez-Jimenez F, Rao G, St-Onge MP, Towfighi A, Poirier P (2011) Assessing adiposity: a scientific statement from the american heart association. Circulation 124:1996–2019CrossRef

39.

Despres J-P, Lemieux I (2006) Abdominal obesity and metabolic syndrome. Nature 444:881–887CrossRef

40.

Yu R, Kim CS, Kwon BS, Kawada T (2006) Mesenteric adipose tissue-derived monocyte chemoattractant protein-1 plays a crucial role in adipose tissue macrophage migration and activation in obese mice. Obesity 14:1353–1362CrossRef

41.

Lee RP, Lin NT, Chao YF, Linn CC, Harn HJ, Chen HI (2007) High-density lipoprotein prevents organ damage in endotoxemia. Res Nurs Health 30:250–260CrossRef

42.

Manco M, Putignani L, Bottazzo GF (2010) Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr Rev 31:817–844CrossRef

43.

Tuin A, Huizinga-Van der Vlag A, van Loenen-Weemaes AM, Meijer DK, Poelstra K (2006) On the role and fate of LPS-dephosphorylating activity in the rat liver. Am J Physiol Gastrointest Liver Physiol 290:G377–G385CrossRef

44.

Coimbra R, Porcides RD, Melbostad H, Loomis W, Tobar M, Hoyt DB, Wolf P (2005) Nonspecific phosphodiesterase inhibition attenuates liver injury in acute endotoxemia. Surg Infect 6:73–85CrossRef

45.

Bates JM, Akerlund J, Mittge E, Guillemin K (2007) Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in response to the gut microbiota. Cell Host Microbe 2:371–382CrossRef

46.

Schromm AB, Brandenburg K, Loppnow H, Zähringer U, Rietschel ET, Carroll SF, Koch MHJ, Kusumoto S, Seydel U (1998) The charge of endotoxin molecules influences their conformation and IL-6-inducing capacity. J Immunol 161:5464–5471

Title: Higher plasma lipopolysaccharide concentrations are associated with less favorable phenotype in overweight/obese men
Authors: Ana Paula Boroni Moreira
Raquel Duarte Moreira Alves
Tatiana Fiche Salles Teixeira
Viviane Silva Macedo
Leandro Licursi de Oliveira
Neuza Maria Brunoro Costa
Josefina Bressan
Maria do Carmo Gouveia Peluzio
Richard Mattes
Rita de Cássia Gonçalves Alfenas
Publication date: 01-12-2015
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Nutrition / Issue 8/2015
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI: https://doi.org/10.1007/s00394-014-0817-6

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