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Published in: Obesity Surgery 1/2012

01-01-2012 | Basic Science Research

Only C-Reactive Protein, but not TNF-α or IL6, Reflects the Improvement in Inflammation after Bariatric Surgery

Authors: Eva Pardina, Roser Ferrer, Juan Antonio Baena-Fustegueras, Joaquín Rivero, Albert Lecube, Jose Manuel Fort, Víctor Vargas, Roberto Catalán, Julia Peinado-Onsurbe

Published in: Obesity Surgery | Issue 1/2012

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Abstract

Background

Increased C-reactive protein (CRP) levels strongly predict inflammatory diseases such as obesity and tissue damage. We wanted to study the CRP in plasma and tissue in morbidly obese patients before and after surgery and relate it with the expression of interleukin-6 (IL-6) and tumor necrosis factor-α (TNF-α) in tissues.

Methods

We analyzed CRP concentration in plasma, adipose and liver, and the expression of IL-6 and TNF-α, in those tissues, in 34 morbidly obese patients before and 1, 6 and 12 months after gastric bypass.

Results

Morbidly obese had a greater amount of CRP in plasma (3 times) and tissues (21, 5 and 7 times more in liver, subcutaneous adipose tissue (SAT) and visceral adipose tissue (VAT), respectively) than control subjects. The expression of IL-6 in SAT showed a similar profile to plasma and SAT CRP in both obese patients and after weight loss, despite no significant correlation was found. We were only able to detect IL-6 in the liver of a subset of patients. The expression of TNF-α after surgery showed a no significant slight tendency to decrease in SAT with weight loss, but in the liver, we did not observe any change.

Conclusion

IL-6 in SAT, but not in liver, seems to be more closely related to plasma and tissue CRP than TNF-α in both obese patients and after weight loss. Plasma CRP protein perfectly reflects the decrease in inflammation and improves with weight loss in the tissues.
Literature
1.
go back to reference Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest. 2003;111(12):1805–12.PubMed Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest. 2003;111(12):1805–12.PubMed
2.
go back to reference Hirschfield GM, Pepys MB. C-reactive protein and cardiovascular disease: new insights from an old molecule. QJM. 2003;96(11):793–807.PubMedCrossRef Hirschfield GM, Pepys MB. C-reactive protein and cardiovascular disease: new insights from an old molecule. QJM. 2003;96(11):793–807.PubMedCrossRef
3.
go back to reference Danesh J, Collins R, Appleby P, et al. Association of fibrinogen, C-reactive protein, albumin, or leukocyte count with coronary heart disease: meta-analyses of prospective studies. JAMA. 1998;279(18):1477–82.PubMedCrossRef Danesh J, Collins R, Appleby P, et al. Association of fibrinogen, C-reactive protein, albumin, or leukocyte count with coronary heart disease: meta-analyses of prospective studies. JAMA. 1998;279(18):1477–82.PubMedCrossRef
4.
go back to reference Danesh J, Muir J, Wong YK, et al. Risk factors for coronary heart disease and acute-phase proteins. A population-based study. Eur Heart J. 1999;20(13):954–9.PubMedCrossRef Danesh J, Muir J, Wong YK, et al. Risk factors for coronary heart disease and acute-phase proteins. A population-based study. Eur Heart J. 1999;20(13):954–9.PubMedCrossRef
5.
go back to reference Frohlich M, Imhof A, Berg G, et al. Association between C-reactive protein and features of the metabolic syndrome: a population-based study. Diabetes Care. 2000;23(12):1835–9.PubMedCrossRef Frohlich M, Imhof A, Berg G, et al. Association between C-reactive protein and features of the metabolic syndrome: a population-based study. Diabetes Care. 2000;23(12):1835–9.PubMedCrossRef
6.
go back to reference Chambers JC, Eda S, Bassett P, et al. C-reactive protein, insulin resistance, central obesity, and coronary heart disease risk in Indian Asians from the United Kingdom compared with European whites. Circulation. 2001;104(2):145–50.PubMed Chambers JC, Eda S, Bassett P, et al. C-reactive protein, insulin resistance, central obesity, and coronary heart disease risk in Indian Asians from the United Kingdom compared with European whites. Circulation. 2001;104(2):145–50.PubMed
7.
go back to reference Ford ES. Body mass index, diabetes, and C-reactive protein among U.S. adults. Diabetes Care. 1999;22(12):1971–7.PubMedCrossRef Ford ES. Body mass index, diabetes, and C-reactive protein among U.S. adults. Diabetes Care. 1999;22(12):1971–7.PubMedCrossRef
8.
go back to reference McLaughlin T, Abbasi F, Lamendola C, et al. Differentiation between obesity and insulin resistance in the association with C-reactive protein. Circulation. 2002;106(23):2908–12.PubMedCrossRef McLaughlin T, Abbasi F, Lamendola C, et al. Differentiation between obesity and insulin resistance in the association with C-reactive protein. Circulation. 2002;106(23):2908–12.PubMedCrossRef
9.
go back to reference Cleland SJ, Sattar N, Petrie JR, et al. Endothelial dysfunction as a possible link between C-reactive protein levels and cardiovascular disease. Clin Sci (Lond). 2000;98(5):531–5.CrossRef Cleland SJ, Sattar N, Petrie JR, et al. Endothelial dysfunction as a possible link between C-reactive protein levels and cardiovascular disease. Clin Sci (Lond). 2000;98(5):531–5.CrossRef
10.
11.
go back to reference Lagrand WK, Visser CA, Hermens WT, et al. C-reactive protein as a cardiovascular risk factor: more than an epiphenomenon? Circulation. 1999;100(1):96–102.PubMed Lagrand WK, Visser CA, Hermens WT, et al. C-reactive protein as a cardiovascular risk factor: more than an epiphenomenon? Circulation. 1999;100(1):96–102.PubMed
12.
go back to reference Fried SK, Bunkin DA, Greenberg AS. Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid. J Clin Endocrinol Metab. 1998;83(3):847–50.PubMedCrossRef Fried SK, Bunkin DA, Greenberg AS. Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid. J Clin Endocrinol Metab. 1998;83(3):847–50.PubMedCrossRef
13.
go back to reference Enkhmaa B, Shiwaku K, Anuurad E, et al. Prevalence of the metabolic syndrome using the Third Report of the National Cholesterol Educational Program Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (ATP III) and the modified ATP III definitions for Japanese and Mongolians. Clin Chim Acta. 2005;352(1–2):105–13.PubMedCrossRef Enkhmaa B, Shiwaku K, Anuurad E, et al. Prevalence of the metabolic syndrome using the Third Report of the National Cholesterol Educational Program Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (ATP III) and the modified ATP III definitions for Japanese and Mongolians. Clin Chim Acta. 2005;352(1–2):105–13.PubMedCrossRef
14.
go back to reference Standardization of anthropometric measurements: the Airlie (VA) Consensus Conference. Champaign, Human Kinetics Publishers. 1988. Standardization of anthropometric measurements: the Airlie (VA) Consensus Conference. Champaign, Human Kinetics Publishers. 1988.
15.
go back to reference Deurenberg P, Weststrate JA, Seidell JC. Body mass index as a measure of body fatness: age- and sex-specific prediction formulas. Br J Nutr. 1991;65(2):105–14.PubMedCrossRef Deurenberg P, Weststrate JA, Seidell JC. Body mass index as a measure of body fatness: age- and sex-specific prediction formulas. Br J Nutr. 1991;65(2):105–14.PubMedCrossRef
16.
go back to reference Bonora E, Micciolo R, Ghiatas AA, et al. Is it possible to derive a reliable estimate of human visceral and subcutaneous abdominal adipose tissue from simple anthropometric measurements? Metabolism. 1995;44(12):1617–25.PubMedCrossRef Bonora E, Micciolo R, Ghiatas AA, et al. Is it possible to derive a reliable estimate of human visceral and subcutaneous abdominal adipose tissue from simple anthropometric measurements? Metabolism. 1995;44(12):1617–25.PubMedCrossRef
17.
go back to reference Martinez Olmos MA, Bellido Guerrero D, Blay Cortés V. Métodos de valoración de la distribución de la grasa corporal en el paciente obeso. Rev Esp Obes. 2004;II(1):42–9. Martinez Olmos MA, Bellido Guerrero D, Blay Cortés V. Métodos de valoración de la distribución de la grasa corporal en el paciente obeso. Rev Esp Obes. 2004;II(1):42–9.
18.
go back to reference Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.PubMedCrossRef Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.PubMedCrossRef
19.
go back to reference Sabugal R, Robert MQ, Julve J, et al. Hepatic regeneration induces changes in lipoprotein lipase activity in several tissues and its re-expression in the liver. Biochem J. 1996;318(2):597–602.PubMed Sabugal R, Robert MQ, Julve J, et al. Hepatic regeneration induces changes in lipoprotein lipase activity in several tissues and its re-expression in the liver. Biochem J. 1996;318(2):597–602.PubMed
20.
go back to reference Anty R, Bekri S, Luciani N, et al. The inflammatory C-reactive protein is increased in both liver and adipose tissue in severely obese patients independently from metabolic syndrome, Type 2 diabetes, and NASH. Am J Gastroenterol. 2006;101(8):1824–33.PubMedCrossRef Anty R, Bekri S, Luciani N, et al. The inflammatory C-reactive protein is increased in both liver and adipose tissue in severely obese patients independently from metabolic syndrome, Type 2 diabetes, and NASH. Am J Gastroenterol. 2006;101(8):1824–33.PubMedCrossRef
21.
go back to reference Ouchi N, Kihara S, Funahashi T, et al. Reciprocal association of C-reactive protein with adiponectin in blood stream and adipose tissue. Circulation. 2003;107(5):671–4.PubMedCrossRef Ouchi N, Kihara S, Funahashi T, et al. Reciprocal association of C-reactive protein with adiponectin in blood stream and adipose tissue. Circulation. 2003;107(5):671–4.PubMedCrossRef
22.
go back to reference Khera A, McGuire DK, Murphy SA, et al. Race and gender differences in C-reactive protein levels. J Am Coll Cardiol. 2005;46(3):464–9.PubMedCrossRef Khera A, McGuire DK, Murphy SA, et al. Race and gender differences in C-reactive protein levels. J Am Coll Cardiol. 2005;46(3):464–9.PubMedCrossRef
23.
go back to reference Imhof A, Frohlich M, Loewel H, et al. Distributions of C-reactive protein measured by high-sensitivity assays in apparently healthy men and women from different populations in Europe. Clin Chem. 2003;49(4):669–72.PubMedCrossRef Imhof A, Frohlich M, Loewel H, et al. Distributions of C-reactive protein measured by high-sensitivity assays in apparently healthy men and women from different populations in Europe. Clin Chem. 2003;49(4):669–72.PubMedCrossRef
24.
go back to reference Rifai N, Ridker PM. Population distributions of C-reactive protein in apparently healthy men and women in the United States: implication for clinical interpretation. Clin Chem. 2003;49(4):666–9.PubMedCrossRef Rifai N, Ridker PM. Population distributions of C-reactive protein in apparently healthy men and women in the United States: implication for clinical interpretation. Clin Chem. 2003;49(4):666–9.PubMedCrossRef
25.
go back to reference Badawi A, Klip A, Haddad P, et al. Type 2 diabetes mellitus and inflammation: prospects for biomarkers of risk and nutritional intervention. Diabetes, Metab Syndr Obes: Targets Ther. 2010;3(173):186. Badawi A, Klip A, Haddad P, et al. Type 2 diabetes mellitus and inflammation: prospects for biomarkers of risk and nutritional intervention. Diabetes, Metab Syndr Obes: Targets Ther. 2010;3(173):186.
26.
go back to reference Kern PA, Ranganathan S, Li CL, et al. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab. 2001;280(5):E745–51.PubMed Kern PA, Ranganathan S, Li CL, et al. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab. 2001;280(5):E745–51.PubMed
27.
go back to reference Muller S, Martin S, Koenig W, et al. Impaired glucose tolerance is associated with increased serum concentrations of interleukin 6 and co-regulated acute-phase proteins but not TNF-alpha or its receptors. Diabetologia. 2002;45(6):805–12.PubMedCrossRef Muller S, Martin S, Koenig W, et al. Impaired glucose tolerance is associated with increased serum concentrations of interleukin 6 and co-regulated acute-phase proteins but not TNF-alpha or its receptors. Diabetologia. 2002;45(6):805–12.PubMedCrossRef
28.
go back to reference Fain JN, Bahouth SW, Madan AK. Involvement of multiple signaling pathways in the post-bariatric induction of IL-6 and IL-8 mRNA and release in human visceral adipose tissue. Biochem Pharmacol. 2005;69(9):1315–24.PubMedCrossRef Fain JN, Bahouth SW, Madan AK. Involvement of multiple signaling pathways in the post-bariatric induction of IL-6 and IL-8 mRNA and release in human visceral adipose tissue. Biochem Pharmacol. 2005;69(9):1315–24.PubMedCrossRef
29.
go back to reference Clementi AH, Gaudy AM, van Rooijen N, et al. Loss of Kupffer cells in diet-induced obesity is associated with increased hepatic steatosis, STAT3 signaling, and further decreases in insulin signaling. Biochim Biophys Acta. 2009;1792(11):1062–72.PubMed Clementi AH, Gaudy AM, van Rooijen N, et al. Loss of Kupffer cells in diet-induced obesity is associated with increased hepatic steatosis, STAT3 signaling, and further decreases in insulin signaling. Biochim Biophys Acta. 2009;1792(11):1062–72.PubMed
30.
go back to reference Despres JP, Lemieux I, Pascot A, et al. Gemfibrozil reduces plasma C-reactive protein levels in abdominally obese men with the atherogenic dyslipidemia of the metabolic syndrome. Arterioscler Thromb Vasc Biol. 2003;23(4):702–3.PubMedCrossRef Despres JP, Lemieux I, Pascot A, et al. Gemfibrozil reduces plasma C-reactive protein levels in abdominally obese men with the atherogenic dyslipidemia of the metabolic syndrome. Arterioscler Thromb Vasc Biol. 2003;23(4):702–3.PubMedCrossRef
31.
go back to reference Curat CA, Wegner V, Sengenes C, et al. Macrophages in human visceral adipose tissue: increased accumulation in obesity and a source of resistin and visfatin. Diabetologia. 2006;49(4):744–7.PubMedCrossRef Curat CA, Wegner V, Sengenes C, et al. Macrophages in human visceral adipose tissue: increased accumulation in obesity and a source of resistin and visfatin. Diabetologia. 2006;49(4):744–7.PubMedCrossRef
Metadata
Title
Only C-Reactive Protein, but not TNF-α or IL6, Reflects the Improvement in Inflammation after Bariatric Surgery
Authors
Eva Pardina
Roser Ferrer
Juan Antonio Baena-Fustegueras
Joaquín Rivero
Albert Lecube
Jose Manuel Fort
Víctor Vargas
Roberto Catalán
Julia Peinado-Onsurbe
Publication date
01-01-2012
Publisher
Springer-Verlag
Published in
Obesity Surgery / Issue 1/2012
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-011-0546-3

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