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Impact of Weight Loss on Inflammatory Proteins and Their Association With the Insulin Resistance Syndrome in Morbidly Obese Patients
Abstract
Objective— Obesity is closely linked to the insulin resistance syndrome (IRS), type 2 diabetes, and cardiovascular disease, the primary cause of morbidity and mortality in these patients. Elevated levels of C-reactive protein (CRP) and interleukin-6 (IL-6), indicating chronic subclinical inflammation, have been associated with features of the IRS and incident cardiovascular disease. Methods and Results— We studied the cross-sectional and longitudinal relation of CRP, IL-6, and tumor necrosis factor-α (TNF-α) with features of the IRS in 37 morbidly obese patients with different stages of glucose tolerance before and 14 months after gastric surgery. Weight loss after gastric surgery induced a significant shift from diabetes (37% vs 3%) to impaired glucose tolerance (40% vs 33%) and normal glucose tolerance (23% vs 64%). The baseline concentration of IL-6 was correlated with TNF-α ( r =0.59, P <0.01) and CRP ( r =0.44, P <0.05) levels. TNF-α, IL-6, and CRP were significantly correlated with insulin resistance estimated by the homeostatic model assessment ( r =0.48, P <0.05; r =0.56, P <0.01; and r =0.35, P <0.05, respectively). Concentrations of CRP and IL-6 decreased after weight loss (median, 8.6 and interquartile range, 2.7/14.5 vs 2.5 and 1.2/4.1 mg/L; P <0.006, and 5.13 and 2.72/12.15 vs 3.95 and 1.97/5.64 pg/mL, P <0.02, respectively), whereas serum levels of TNF-α remained unchanged (8.6 and 6.3/18.8 vs 11.7 and 5.8/17.2 pg/mL; NS.). Multiple regression analysis revealed that the decrease in insulin resistance remained independently and significantly correlated with the decrease in IL-6 concentrations ( P <0.01) and the decrease in body mass index with the decrease in CRP ( P <0.05), respectively. Conclusions— Weight loss in morbidly obese patients induces a significant decrease of CRP and IL-6 concentrations in association with an improvement of the IRS.
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BackgroundObesity-Related Oxidative Stress: the Impact of Physical Activity and Diet Manipulation
Huang, C., McAllister, M. J., Slusher, A. L., Webb, H. E., Mock, J. T., & Acevedo, E. O. (2015) · Sports Medicine - Open · doi:10.1186/s40798-015-0031-y · Cited by 166
“, gastric bypass surgery) in previously obese men and women has been shown to decreases oxidative stress and vital inflammatory markers, such as IL-6, C-reactive protein, and TNF-α, suggesting that weight loss independently can reduce oxidative stress and inflammation [84, 85].”
BackgroundEffects of Bariatric Surgery on Glucose Homeostasis and Type 2 Diabetes
Bradley, D. P., Magkos, F., & Klein, S. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.07.114 · Cited by 154
Del Prato, S., Felton, A.-M., Munro, N., Nesto, R., Zimmet, P., & Zinman, B. (2005) · International Journal of Clinical Practice · doi:10.1111/j.1742-1241.2005.00674.x · Cited by 150
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“Multiple regression analysis reveals that the decrease in postoperative insulin resistance after surgery is independently associated with a decrease in interleukin-6 concentrations.(77) At 6 months after surgery, there is also an increase in the production of interferongamma, IL-12, and IL-18 that is associated with a…”
BackgroundJellema, A., Plat, J., & Mensink, R. P. (2004) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.2004.01414.x · Cited by 144
Obesity-related cognitive impairment: The role of endothelial dysfunction
Buie, J. N. J., Watson, L. S., Smith, C. J., & Sims‐Robinson, C. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104580 · Cited by 138
Akram, Z., Abduljabbar, T. S., Hassan, M. I. A., Javed, F., & Vohra, F. (2016) · Disease Markers · doi:10.1155/2016/4801418 · Cited by 136
“Weight management in obese subjects has shown a reduction in systemic inflammatory burden as expressed by lower levels of serum cytokines [47, 48].”
BackgroundPapaetis, G. S., Papakyriakou, P., & Panagiotou, T. N. (2015) · Archives of Medical Science · doi:10.5114/aoms.2015.52350 · Cited by 143
“Plasma IL-6 concentrations were also associated with an increase of NEFAs and C-reactive protein (CRP) levels [48].”
BackgroundInflammation, Insulin Resistance, and Adiposity
Kriketos, A. D., Greenfield, J. R., Peake, P. W., Furler, S. M., Denyer, G. S., CHARLESWORTH, J. A., & Campbell, L. V. (2004) · Diabetes Care · doi:10.2337/diacare.27.8.2033 · Cited by 126
“In a weightloss study, the decrease in CRP levels after gastric surgery was related to the decrease in BMI but not to the change in insulin sensitivity (39).”
BackgroundLongitudinal effects of systemic inflammation markers on periodontitis
Pink, C., Kocher, T., Meisel, P., Dörr, M., Markus, M. R. P., Jablonowski, L., Grotevendt, A., Nauck, M. A., & Holtfreter, B. (2015) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12473 · Cited by 121
Inflammation and thrombosis in diabetes
Hess, K., & Grant, P. J. (2011) · Thrombosis and Haemostasis · doi:10.1160/ths10-11-0739 · Cited by 117
“In general, life style intervention, particularly weight loss results in a decrease in inflammatory proteins (196, 197), thereby improving insulin resistance and the pro-thrombotic milieu.”
BackgroundHeutling, D., Schulz, H., Nickel, I., Kleinstein, J., Kaltwaßer, P., Westphal, S., Mittermayer, F., Wolzt, M., Krzyżanowska, K., Randeva, H. S., et al. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-0842 · Cited by 117
“Chronic subclinical inflammation is closely related to obesity, and a BMI reduction results in a decrease of inflammatory markers (54, 55).”
BackgroundSelf-citationReinehr, T., Stoffel‐Wagner, B., Roth, C. L., & Andler, W. (2005) · Metabolism · doi:10.1016/j.metabol.2005.03.022 · Cited by 119
Defective regulation of adipose tissue autophagy in obesity
Nuñez, C. E. C., Rodrigues, V. S., Gomes, F. S., de Moura, R. F., Victorio, S. C. D. S., Bombassaro, B., Chaim, É. A., Pareja, J. C., Geloneze, B., Velloso, L. A., et al. (2013) · International Journal of Obesity · doi:10.1038/ijo.2013.27 · Cited by 117
Makary, M. A., Clark, J. M., Shore, A. D., Magnuson, T. H., Richards, T., Bass, E. B., Dominici, F., Weiner, J. P., Wu, A. W., & Segal, J. B. (2010) · Archives of Surgery · doi:10.1001/archsurg.2010.150 · Cited by 115
“The use of this intervention has increased 200% during the past 5 years, but studies of its effect on type 2 diabetes and costs are limited.(6,8,9) Our objective was to determine the impact of bariatric surgery on the use of diabetes medication and on total health care costs.”
BackgroundInteractive Effect of Obesity Indexes on Cognition
Jeong, S., Nam, H., Son, M.-H., Son, E.-J., & Cho, K.-H. (2004) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000082659 · Cited by 113
Effect of Weight Loss on Proinflammatory State of Mononuclear Cells in Obese Women
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“In this study, weight reduction, even though limited in magnitude, had a beneficial effect on metabolic and inflammatory responses in obese subjects (9,10).”
BackgroundElevated Fetuin-A Concentrations in Morbid Obesity Decrease after Dramatic Weight Loss
Brix, J. M., Stingl, H., Höllerl, F., Schernthaner, G.-H., Kopp, H.-P., & Schernthaner, G. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-0148 · Cited by 113
Self-citationAdipose tissue, inflammation and cardiovascular disease
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Thrombin generation in morbid obesity: significant reduction after weight loss
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Self-citationEffects of long-term exercise and diet intervention on plasma adipokine concentrations
Rokling-Andersen, M. H., Reseland, J. E., Veierød, M. B., Anderssen, S. A., Jacobs, D. R., Urdal, P., Jansson, J., & Drevon, C. A. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.5.1293 · Cited by 110
The usefulness of circulating adipokine levels for the assessment of obesity-related health problems
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Metabolic surgery and obstructive sleep apnoea: the protective effects of bariatric procedures
Ashrafian, H., le Roux, C. W., Rowland, S. P., Ali, M., Cummin, A. R., Darzi, A., & Athanasiou, T. (2012) · Thorax · doi:10.1136/thx.2010.151225 · Cited by 106
“Analysis by multiple regression has shown that the reduction in postoperative insulin resistance after surgery is independently associated with a decrease in IL-6 concentrations.(86) TNFa was reduced in one study of patients undergoing liposuction(87) (which does not offer long-term metabolic or weight loss effects) a…”
BackgroundTussing‐Humphreys, L. M., Nemeth, E., Fantuzzi, G., Freels, S., Holterman, A. L., Galvani, C., Ayloo, S., Vitello, J., & Braunschweig, C. (2010) · Obesity · doi:10.1038/oby.2009.490 · Cited by 105
Emerging Role of Mast Cells and Macrophages in Cardiovascular and Metabolic Diseases
Xu, J., & Shi, G. (2012) · Endocrine Reviews · doi:10.1210/er.2011-0013 · Cited by 105
Liver-spleen axis in nonalcoholic fatty liver disease
Tarantino, G., Citro, V., & Balsano, C. (2021) · Expert Review of Gastroenterology & Hepatology · doi:10.1080/17474124.2021.1914587 · Cited by 107
Miller, G. D., Nicklas, B. J., & Loeser, R. F. (2008) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2007.01636.x · Cited by 105
“Data from several cross-sectional studies, including the National Health and Nutrition Examination Survey and the Nurses Health Study, revealed that a diet higher in saturated and trans fatty acids is associated with higher levels of inflammatory markers, including CRP, IL-6, and TNFa.38 Total amount of dietary fat ca…”
BackgroundInfluentialSöndergaard, H. P., Hansson, L.-O., & Theorell, T. (2004) · Clinica Chimica Acta · doi:10.1016/j.cccn.2003.12.019 · Cited by 98
Dvořáková-Lorenzová, A., Suchánek, P., Havel, P. J., Stávek, P., Karasová, L., Valenta, Z., Tintěra, J., & Poledne, R. (2006) · Metabolism · doi:10.1016/j.metabol.2005.09.010 · Cited by 97
“Decreases in hsCRP concentrations after weight reduction have been documented in 4 other recently published interventional studies [9,11-13].”
BackgroundResultDiabetes resolution and hyperinsulinaemia after metabolic Roux‐en‐Y gastric bypass
Ashrafian, H., Athanasiou, T., Li, J. V., Bueter, M., Ahmed, K., Nagpal, K., Holmes, E. C., Darzi, A. W., & Bloom, S. R. (2010) · Obesity Reviews · doi:10.1111/j.1467-789x.2010.00802.x · Cited by 102
“Multiple regression analysis has revealed that the decrease in insulin resistance after surgery is independently associated with a decrease in Interleukin-6 concentrations (132).”
BackgroundThe periodontal host response with diabetes
Nishimura, F., Iwamoto, Y., & Soga, Y. (2007) · Periodontology 2000 · doi:10.1111/j.1600-0757.2006.00171.x · Cited by 94
Lifestyle intervention for prevention of diabetes: determinants of success for future implementation
Roumen, C., Blaak, E. E., & Corpeleijn, E. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.2009.00181.x · Cited by 96
Salas‐Salvadó, J., Bulló, M., García‐Lorda, P., Figuerêdo, R. G., Castillo, D. D., Bonada, A., & Balanzá, R. (2006) · International Journal of Obesity · doi:10.1038/sj.ijo.0803348 · Cited by 93
Impact of bariatric surgery on oral health conditions: 6-months cohort study
de Moura‐Grec, P. G., Yamashita, J. M., Marsicano, J. A., Ceneviva, R., Leite, C. V. D. S., Brito, G. B., Brienze, S. L. A., & Peres, S. H. D. C. S. (2014) · International Dental Journal · doi:10.1111/idj.12090 · Cited by 92
Brock, C., Hansen, C. S., Karmisholt, J., Møller, H. J., Juhl, A. H., Farmer, A. D., Drewes, A. M., Riahi, S., Lervang, H. H., Jakobsen, P. E., et al. (2019) · British Journal of Clinical Pharmacology · doi:10.1111/bcp.14063 · Cited by 95
“Weight loss is considered as anti‐ inflammatory in itself, and it has previously been shown that substantially weight reduction in morbidly obese patients induces a significant decrease in IL‐6, whereas TNF‐α remains unaltered.(44) In this study, the average weight loss was only approximately 3 kg; however, this reduc…”
Background
Metadata
- Authors
- Kopp, H. P., Kopp, C. W., Festa, A., Krzyzanowska, K., Kriwanek, S., Minar, E., Roka, R., & Schernthaner, G.
- Affiliations
- Vienna General Hospital (AT)
- From the Department of Medicine 1 (H.P.K., A.F., K.K., G.S.), Rudolfstiftung Hospital; the Department of Medicine 2 (C.W.K., E.M.), General Hospital of Vienna; and the Department of Surgery 1 and Ludwig Boltzmann Institute for Endocrine Surgery (S.K., R.K.), Rudolfstiftung Hospital, Vienna, Austria.
- Venue
- Arteriosclerosis, Thrombosis, and Vascular Biology
- Published
- 2003-06
- Volume
- 23
- Issue
- 6
- Pages
- 1042-1047
- ISSN
- 1079-5642 (ISSN-L)
- 1524-4636
- OpenAlex
- W2102170193
- Cited by
- 427
- References
- 45
- Citations by year
- 2026: 9 · 2025: 8 · 2024: 10 · 2023: 14 · 2022: 9 · 2021: 10 · 2020: 10 · 2019: 13 · 2018: 17 · 2017: 10 · 2016: 6 · 2015: 24 · 2014: 24 · 2013: 25 · 2012: 15
- FWCI
- 20.21
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Arteriosclerosis Thrombosis and Vascular Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Universität Wien
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Surgery › Bariatric Surgery and Outcomes
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
- Keywords
- morbid obesity, weight loss, metabolic syndrome, C-reactive protein, interleukin-6, TNF-α, chronic inflammation, gastric bypass, bariatric surgery, impaired glucose tolerance, type 2 diabetes, HOMA, body mass index, glucose tolerance, cardiovascular risk factors, adipokines, adipose tissue inflammation, hepatic insulin resistance
- MeSH terms
- Adult, Blood Glucose, C-Reactive Protein, Cross-Sectional Studies, Diabetes Mellitus, Type 2, Female, Fibrinogen, Humans, Inflammation, Insulin, Insulin Resistance, Lipids, Longitudinal Studies, Male, Middle Aged, Obesity, Morbid, Tumor Necrosis Factor-alpha, Gastroplasty, Weight Loss, Interleukin-6, Body Mass Index
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