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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Most tests of Fe status are affected in response to subclinical inflammation and infections.
“Most tests of Fe status, however, are affected in response to subclinical inflammation and infections (690 -692) .”
From Dietary factors and low-grade inflammation in relation to overweight and obesity (2011) · cites this paper as [692]
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“32 Studies over the past decade have shown that the storage and release of FFAs by adipose tissue are not its only function.”
The Role of Cytokines in Non-Alcoholic Fatty Liver Disease
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“Most cytokine research on obesity-related diseases has centered on IL-6, which was among the first cytokines to be implicated as a predictor or pathogenetic marker of IR and cardiovascular disease. Concentrations of IL-6 decrease in parallel with weight loss and improvement of IR in patients undergoing bariatric surge…”
BackgroundChapter 21 Interleukin‐6 and Insulin Resistance
Kim, J., Bachmann, R. A., & Chen, J. (2009) · Vitamins & Hormones · doi:10.1016/s0083-6729(08)00621-3 · Cited by 224 · see citing works
“…than within a prediabetic cohort (Kocak et al., 2007), while a study of morbidly obese patients given gastric surgery demonstrated a significant shift from diabetic or impaired glucose tolerance to normal glucose tolerance along with a significant decrease in serum IL-6 levels (Kopp et al., 2003).”
The role of interleukin‐6 in insulin resistance, body fat distribution and energy balance
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Obstructive Sleep Apnea, Insulin Resistance, and Steatohepatitis in Severe Obesity
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“Our findings confirm those of previous studies demonstrating similar marked elevations of serum CRP levels in severely obese individuals (12, 15).”
BackgroundResultInflammatory markers and particulate air pollution: characterizing the pathway to disease
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Proinflammatory Cytokines in Obesity: Impact of Type 2 Diabetes Mellitus and Gastric Bypass
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“In contrast, the absence of changes in these inflammatory cytokines has been recently reported in very active, weightlosing patients induced by a very low calorie diet (43) or bariatric surgery (21, 22), suggesting a role of the metabolic stress of relative starvation in the inflammatory response (44).”
BackgroundKapiotis, S., Holzer, G., Schaller, G., Haumer, M., Widhalm, H., Weghuber, D., Jilma, B., Röggla, G., Wolzt, M., Widhalm, K., et al. (2006) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000245795.08139.70 · Cited by 205 · see citing works
Effect of weight loss on some serum cytokines in human obesity: increase in IL-10 after weight loss
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“In another study, a decrease in IL-6 significantly correlated with a decrease in TNF-α after weight loss in morbidly obese patients [18].”
BackgroundAshrafian, H., Toma, T., Rowland, S. P., Harling, L., Tan, A., Efthimiou, E., Darzi, A. W., & Athanasiou, T. (2014) · Obesity Surgery · doi:10.1007/s11695-014-1533-2 · Cited by 196 · see citing works
“Bariatric/ metabolic surgery may significantly reduce the concentration of both IL-6 and CRP [49], as well as improving insulin resistance [50].”
BackgroundFerrannini, E., & Mingrone, G. (2009) · Diabetes Care · doi:10.2337/dc08-1762 · Cited by 187 · see citing works
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“It should be noted that weight loss following gastric surgery has been associated with decreased CRP levels together with an increase in insulin sensitivity, although those changes were not directly related (50).”
BackgroundKopp, H., Krzyżanowska, K., Möhlig, M., Spranger, J., Pfeiffer, A. F. H., & Schernthaner, G.-H. (2005) · International Journal of Obesity · doi:10.1038/sj.ijo.0802983 · Cited by 189 · see citing works
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Dekker, M. J., Lee, S., HUDSON, R. W., Kilpatrick, K., Graham, T. E., Ross, R., & Robinson, L. E. (2007) · Metabolism · doi:10.1016/j.metabol.2006.10.015 · Cited by 176 · see citing works
Pareek, M., Schauer, P. R., Kaplan, L. M., Leiter, L. A., Rubino, F., & Bhatt, D. L. (2018) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2017.12.014 · Cited by 181 · see citing works
“Both C-reactive protein and interleukin-6 levels decrease considerably, in parallel with the increased insulin sensitivity (78).”
BackgroundBarrea, L., Marzullo, P., Muscogiuri, G., Di Somma, C., Scacchi, M., Orio, F., Aimaretti, G., Colao, A., & Savastano, S. (2018) · Nutrition Research Reviews · doi:10.1017/s0954422418000136 · Cited by 171 · see citing works
“Dietary modifications that lead to a reduction in postprandial glucose and hyperinsulinaemia could have important implications in improving fatty acid oxidation, promoting weight loss, and preventing further weight gain in women with PCOS((105)).”
BackgroundYou, T., Yang, R., Lyles, M. F., Gong, D., & Nicklas, B. J. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00419.2004 · Cited by 173 · see citing works
“Previous work has shown that glucose tolerance and insulin sensitivity are reduced in individuals with elevated circulating levels of inflammatory and thrombotic biomarkers (21, 29, 31, 38, 39).”
BackgroundClaycombe, K., Harkins, J. M., Chung, Y.-J., Penner, K. M., Pestka, J. J., North, C. M., & Moustaïd‐Moussa, N. (2004) · Journal of Nutrition · doi:10.1093/jn/134.10.2673 · Cited by 169 · see citing works
Lambert, M. A., DELVIN, E. E., Paradis, G., O’Loughlin, J. L., Hanley, J. A., & Levy, E. H. (2004) · Clinical Chemistry · doi:10.1373/clinchem.2004.036418 · Cited by 167 · see citing works
“The IL-6 concentration is increased in obesity (8, 33), and weight loss has been associated with significant decreases in IL-6 values in both adipose tissue and serum (15, 33) and with a decrease in plasma CRP concentrations (15, 34).”
BackgroundObesity, adipokines and neuroinflammation
Aguilar‐Valles, A., Inoue, W., Rummel, C. D., & Luheshi, G. N. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.12.023 · Cited by 166 · see citing works
“Furthermore, IL-6 serum concentrations are elevated in obese individuals and decrease in parallel with weight loss (Kopp et al., 2003; Moschen et al., 2011).”
BackgroundManco, M., Fernández‐Real, J. M., Equitani, F., Vendrell, J. J., Mora, M. E. V., Nanni, G., Tondolo, V., Calvani, M., Ricart, W., Castagneto, M., et al. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-0960 · Cited by 162 · see citing works
“Levels of TNF- did not decrease in short-term (34) and long-term patient follow-ups after bariatric surgery (6, 35), and in very active weightlosing patients (36).”
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 161 · see citing works
“, 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 153 · see citing works
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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 · see citing works
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 133 · see citing works
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“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 135 · see citing works
“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 · see citing works
“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 · see citing works
Inflammation and thrombosis in diabetes
Hess, K., & Grant, P. J. (2011) · Thrombosis and Haemostasis · doi:10.1160/ths10-11-0739 · Cited by 117 · see citing works
“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 · see citing works
“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 118 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
Effect of Weight Loss on Proinflammatory State of Mononuclear Cells in Obese Women
Sheu, W. H., Chang, T., Lee, W., Ou, H., Wu, C.-M., Tseng, L., Lang, H.-F., Wu, C., Wan, C., & Lee, I. (2008) · Obesity · doi:10.1038/oby.2008.37 · Cited by 112 · see citing works
“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 112 · see citing works
Self-citationAdipose tissue, inflammation and cardiovascular disease
Ikeoka, D., Mader, J. K., & Pieber, T. R. (2010) · Revista da Associação Médica Brasileira · doi:10.1590/s0104-42302010000100026 · Cited by 109 · see citing works
Thrombin generation in morbid obesity: significant reduction after weight loss
AY, L., KOPP, H. ‐., Brix, J., Ay, C., Quehenberger, P., Schernthaner, G.-H., Pabinger, I., & Schernthaner, G.-H. (2010) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2010.03766.x · Cited by 110 · see citing works
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 109 · see citing works
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 · see citing works
“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 · see citing works
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 102 · see citing works
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 101 · see citing works
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“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 · see citing works
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 98 · see citing works
“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 95 · see citing works
“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 96 · see citing works
Lifestyle intervention for prevention of diabetes: determinants of success for future implementation
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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 · see citing works
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 94 · see citing works
“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
- 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 › Epidemiology › 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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