Inflammatory Markers and Risk of Developing Type 2 Diabetes in Women
Abstract
We conducted a prospective, nested, case-control study of inflammatory markers as predictors of type 2 diabetes among 32,826 women who provided blood samples in 1989 through 1990 in the Nurses’ Health Study. Among women free of diabetes, cardiovascular disease, or cancer at baseline, 737 had developed diabetes by 2000. Control women (n = 785) were selected matched on age, fasting status, race, and BMI for cases in the top BMI decile. Baseline levels of tumor necrosis factor (TNF)-α receptor 2, interleukin (IL)-6, and C-reactive protein (CRP) were significantly higher among case than control subjects (all P ≤ 0.001). After adjusting for BMI and other lifestyle factors, all three biomarkers significantly predicted diabetes risk; the odds ratios (ORs) comparing extreme quintiles were 1.64 (95% CI 1.10–2.45) for TNF-αR2, 1.91 (1.27–2.86) for IL-6, and 4.36 (2.80–6.80) for CRP (P for trend <0.001 for all biomarkers). In a multivariate model simultaneously including the three biomarkers, only CRP levels were significantly associated with risk of diabetes (OR comparing extreme quintiles of CRP = 3.99, P for trend <0.001). These data support the role of inflammation in the pathogenesis of type 2 diabetes. Elevated CRP levels are a strong independent predictor of type 2 diabetes and may mediate associations of TNF-αR2 and IL-6 with type 2 diabetes.
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The metabolic syndrome is associated with a state of chronic, low-grade inflammation.
“Recently, this syndrome has been noted to be associated with a state of chronic, low-grade inflammation.47,48”
From Diagnosis and Management of the Metabolic Syndrome: An American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement (2005) · cites this paper as [47]
Cites
Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin
(2002) · New England Journal of Medicine · doi:10.1056/nejmoa012512 · Cited by 19,011 · see citing works
Tuomilehto, J., Lindström, J., Eriksson, J. G., Valle, T. T., Hämäläinen, H., Ilanne-Parikka, P., Keinänen-Kiukaanniemi, S., Laakso, M., Louheranta, A., Rastas, M., et al. (2001) · New England Journal of Medicine · doi:10.1056/nejm200105033441801 · Cited by 10,873 · cited 1× · see citing works
“Lifestyle interventions such as exercise and weight loss are effective in lowering CRP and other inflammatory markers (43,44) and in preventing type 2 diabetes in subjects with impaired glucose tolerance (45,46).”
BackgroundReport of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus
The Expert Committee on the Diagnosis and Classification of Diabetes Mellitus* (2002) · Diabetes Care · doi:10.2337/diacare.25.2007.s5 · Cited by 10,320 · see citing works
Adipose Expression of Tumor Necrosis Factor-α: Direct Role in Obesity-Linked Insulin Resistance
Hotamisligil, G. S., Shargill, N. S., & Spiegelman, B. M. (1993) · Science · doi:10.1126/science.7678183 · Cited by 7,518 · see citing works
Acute-Phase Proteins and Other Systemic Responses to Inflammation
Gabay, C., & Kushner, I. (1999) · New England Journal of Medicine · doi:10.1056/nejm199902113400607 · Cited by 6,734 · see citing works
Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus
The Expert Committee on the Diagnosis and Classification of Diabetes Mellitus (1997) · Diabetes Care · doi:10.2337/diacare.20.7.1183 · Cited by 6,220 · see citing works
Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men
Ridker, P. M., Cushman, M., Stampfer, M. J., Tracy, R. P., & Hennekens, C. H. (1997) · New England Journal of Medicine · doi:10.1056/nejm199704033361401 · Cited by 5,504 · see citing works
Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance.
National Diabetes Data Group (1979) · Diabetes · doi:10.2337/diab.28.12.1039 · Cited by 4,909 · see citing works
C-Reactive Protein, Interleukin 6, and Risk of Developing Type 2 Diabetes Mellitus
Pradhan, A. D. (2001) · JAMA · doi:10.1001/jama.286.3.327 · Cited by 4,433 · see citing works
Reproducibility and validity of a semiquantitative food frequency questionnaire
WILLETT, W. C., SAMPSON, L., STAMPFER, M. J., ROSNER, B., BAIN, C., WITSCHI, J., HENNEKENS, C. H., & SPEIZER, F. E. (1985) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a114086 · Cited by 4,274 · see citing works
Hotamisligil, G. S., Arner, P., Caro, J. F., Atkinson, R. L., & Spiegelman, B. M. (1995) · Journal of Clinical Investigation · doi:10.1172/jci117936 · Cited by 3,543 · see citing works
Diet, lifestyle, and the risk of type 2 diabetes mellitus in women.
Hu, F. B., Manson, J. E., Stampfer, M. J., Colditz, G., Liu, S., Solomon, C. G., & Willett, W. C. (2001) · New England Journal of Medicine · doi:10.1056/nejmoa010492 · Cited by 2,901 · see citing works
Self-citationClinical application of C-reactive protein for cardiovascular disease detection and prevention
Ridker, P. M. (2003) · Circulation · doi:10.1161/01.cir.0000053730.47739.3c · Cited by 2,513 · see citing works
Elevated C-reactive protein levels in overweight and obese adults
Visser, M. (1999) · JAMA · doi:10.1001/jama.282.22.2131 · Cited by 2,494 · see citing works
Yudkin, J. S., Stehouwer, C. D. A., Emeis, J. J., & Coppack, S. W. (1999) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.19.4.972 · Cited by 2,465 · see citing works
Chronic Subclinical Inflammation as Part of the Insulin Resistance Syndrome
Festa, A., D’Agostino, R., Howard, G., Mykkänen, L. M., Tracy, R. P., & Haffner, S. M. (2000) · Circulation · doi:10.1161/01.cir.102.1.42 · Cited by 2,363 · see citing works
Body Weight and Mortality among Women
Manson, J. E., Willett, W. C., Stampfer, M. J., Colditz, G. A., Hunter, D. J., Hankinson, S. E., Hennekens, C. H., & Speizer, F. E. (1995) · New England Journal of Medicine · doi:10.1056/nejm199509143331101 · Cited by 2,005 · see citing works
Self-citationImpact of Overweight on the Risk of Developing Common Chronic Diseases During a 10-Year Period
Field, A. E., Coakley, E. H., Must, A., Spadano, J. L., Laird, N., Dietz, W. H., Rimm, E., & Colditz, G. A. (2001) · Archives of Internal Medicine · doi:10.1001/archinte.161.13.1581 · Cited by 1,694 · see citing works
Esposito, K., Pontillo, A., Di Palo, C., Giugliano, G., Masella, M., Marfella, R., & Giugliano, D. (2003) · JAMA · doi:10.1001/jama.289.14.1799 · Cited by 1,511 · see citing works
Inflammatory Cytokines and the Risk to Develop Type 2 Diabetes
Spranger, J., Kroke, A., Möhlig, M., Hoffmann, K., Bergmann, M. M., Ristow, M., Boeing, H., & Pfeiffer, A. F. H. (2003) · Diabetes · doi:10.2337/diabetes.52.3.812 · Cited by 1,493 · see citing works
Tumor Necrosis Factor α: A Key Component of the Obesity-Diabetes Link
Hotamışlıgil, G. S., & Spiegelman, B. M. (1994) · Diabetes · doi:10.2337/diab.43.11.1271 · Cited by 1,344 · see citing works
Pickup, J. C., Mattock, M. B., Chusney, G. D., & Burt, D. J. (1997) · Diabetologia · doi:10.1007/s001250050822 · Cited by 1,241 · see citing works
Festa, A., D’Agostino, R., Tracy, R. P., & Haffner, S. M. (2002) · Diabetes · doi:10.2337/diabetes.51.4.1131 · Cited by 1,057 · see citing works
Is Type II diabetes mellitus a disease of the innate immune system?
Pickup, J. C., & Crook, M. A. (1998) · Diabetologia · doi:10.1007/s001250051058 · Cited by 1,040 · see citing works
Low-Grade Systemic Inflammation and the Development of Type 2 Diabetes
Duncan, B. B., Schmidt, M. I., Pankow, J. S., Ballantyne, C. M., Couper, D., Vigo, A., Hoogeveen, R., Folsom, A. R., & Heiss, G. (2003) · Diabetes · doi:10.2337/diabetes.52.7.1799 · Cited by 1,036 · see citing works
Hu, F. B., Sigal, R. J., Rich-Edwards, J. W., Colditz, G. A., Solomon, C. G., Willett, W. C., Speizer, F. E., & Manson, J. E. (1999) · JAMA · doi:10.1001/jama.282.15.1433 · Cited by 914 · see citing works
Self-citationFreeman, D. J., Norrie, J., Sattar, N., Neely, R. D. G., Cobbe, S. M., Ford, I., Isles, C., Lorimer, A. R., Macfarlane, P. W., McKillop, J. H., et al. (2001) · Circulation · doi:10.1161/01.cir.103.3.357 · Cited by 844 · see citing works
Carey, V. J., Walters, E. E., Colditz, G. A., Solomon, C. G., Willet, W. C., Rosner, B. A., Speizer, F. E., & Manson, J. E. (1997) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a009158 · Cited by 827 · see citing works
Self-citationIs obesity an inflammatory condition?
Das, U. N. (2001) · Nutrition · doi:10.1016/s0899-9007(01)00672-4 · Cited by 799 · see citing works
Freeman, D. J., Norrie, J. D., CASLAKE, M. J., Gaw, A., Ford, I., Lowe, G. D. O., O’Reilly, D. S. J., Packard, C. J., Sattar, N. A., & for the West of Scotland Coronary Prevention Study Group (2002) · Diabetes · doi:10.2337/diabetes.51.5.1596 · Cited by 720 · see citing works
The expression of TNF alpha by human muscle. Relationship to insulin resistance.
Saghizadeh, M., Ong, J. M., Garvey, W. T., Henry, R. R., & Kern, P. A. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118504 · Cited by 717 · see citing works
Manson, J. E. (1991) · Archives of Internal Medicine · doi:10.1001/archinte.1991.00400060077013 · Cited by 675 · see citing works
Self-citationMicrovascular and macrovascular reactivity is reduced in subjects at risk for type 2 diabetes.
Caballero, A. E., Arora, S., Saouaf, R., Lim, S. C., Smakowski, P., Park, J. Y., King, G. L., LoGerfo, F. W., Horton, E. S., & Veves, A. (1999) · Diabetes · doi:10.2337/diabetes.48.9.1856 · Cited by 647 · see citing works
Pickup, J. C., & Williams, G. H. (1991) · Cited by 573 · see citing works
The Relation of Markers of Inflammation to the Development of Glucose Disorders in the Elderly
Barzilay, J. I., Abraham, L., Heckbert, S. R., Cushman, M., Kuller, L. H., Resnick, H. E., & Tracy, R. P. (2001) · Diabetes · doi:10.2337/diabetes.50.10.2384 · Cited by 543 · see citing works
Ramipril and the Development of Diabetes
Yusuf, S. (2001) · JAMA · doi:10.1001/jama.286.15.1882 · Cited by 541 · see citing works
Han, T. S., Sattar, N. A., Williams, K., González‐Villalpando, C., Lean, M. E. J., & Haffner, S. M. (2002) · Diabetes Care · doi:10.2337/diacare.25.11.2016 · Cited by 514 · see citing works
C-Reactive Protein as a Predictor for Incident Diabetes Mellitus Among Middle-aged Men
Thorand, B., Löwel, H., Schneider, A. L. C., Kolb, H., Meisinger, C., Fröhlich, M., & Köenig, W. (2003) · Archives of Internal Medicine · doi:10.1001/archinte.163.1.93 · Cited by 370 · see citing works
Tumor necrosis factor alpha: a key component of the obesity-diabetes link
Hotamışlıgil, G. S., & Spiegelman, B. M. (1994) · Diabetes · doi:10.2337/diabetes.43.11.1271 · Cited by 354 · see citing works
Inflammatory Markers, Adiponectin, and Risk of Type 2 Diabetes in the Pima Indian
Krakoff, J. A., Funahashi, T., Stehouwer, C. D. A., Schalkwijk, C. G., Tanaka, S., Matsuzawa, Y., Kobes, S., Tataranni, P. A., Hanson, R. L., Knowler, W. C., et al. (2003) · Diabetes Care · doi:10.2337/diacare.26.6.1745 · Cited by 334 · see citing works
Vermes, E., Ducharme, A., Bourassa, M. G., Lessard, M., White, M., & Tardif, J.-C. (2003) · Circulation · doi:10.1161/01.cir.0000054611.89228.92 · Cited by 248 · see citing works
Do atherosclerosis and type 2 diabetes share a common inflammatory basis?
Pradhan, A. (2002) · European Heart Journal · doi:10.1053/euhj.2001.3052 · Cited by 214 · see citing works
C-Reactive Protein Is Independently Associated With Fasting Insulin in Nondiabetic Women
Pradhan, A. D., Cook, N. R., Buring, J. E., Manson, J. E., & Ridker, P. M. (2003) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000065636.15310.9c · Cited by 211 · see citing works
Self-citationTan, K. C. B., Chow, W.-S., Tam, S., Ai, V. H. G., Lam, C. H. L., & Lam, K. S. L. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.2.8249 · Cited by 202 · see citing works
O’Driscoll, G., GREEN, D. J., Maiorana, A., Stanton, K. G., Colreavy, F. B., & Taylor, R. R. (1999) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(99)00065-0 · Cited by 173 · see citing works
Chu, N., Spiegelman, D. L., Hotamışlıgil, G. S., Rifai, N., Stampfer, M. J., & Rimm, E. B. (2001) · Atherosclerosis · doi:10.1016/s0021-9150(00)00755-3 · Cited by 138 · see citing works
Self-citationEffect of transport conditions on the stability of biochemical markers in blood.
Hankinson, S. E., London, S. J., Chute, C. G., Barbieri, R. L., Jones, L. A., Kaplan, L., Sacks, F. M., & Stampfer, M. J. (1989) · Clinical Chemistry · doi:10.1093/clinchem/35.12.2313 · Cited by 137 · see citing works
Chu, N.-F., Spiegelman, D. L., Rifai, N., Hotamışlıgil, G. S., & Rimm, E. B. (2000) · International Journal of Obesity · doi:10.1038/sj.ijo.0801361 · Cited by 57 · see citing works
Self-citationManns, P. J., Williams, D. P., Snow, C. M., & Wander, R. C. (2003) · American Journal of Human Biology · doi:10.1002/ajhb.10117 · Cited by 47 · see citing works
Is Type 2 Diabetes Mellitus a Vascular Condition?
Hu, F. B., & Stampfer, M. J. (2003) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000094360.38911.71 · Cited by 44 · see citing works
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Grundy, S. M., Cleeman, J. I., Daniels, S. R., Donato, K. A., Eckel, R. H., Franklin, B. A., Gordon, D. J., Krauss, R. M., Savage, P. J., Smith, S. C., et al. (2005) · Circulation · doi:10.1161/circulationaha.105.169404 · Cited by 11,961 · see citing works
Muscle as an Endocrine Organ: Focus on Muscle-Derived Interleukin-6
Pedersen, B. K., & Febbraio, M. A. (2008) · Physiological Reviews · doi:10.1152/physrev.90100.2007 · Cited by 2,388 · see citing works
The Role of Vitamin D and Calcium in Type 2 Diabetes. A Systematic Review and Meta-Analysis
Pittas, A. G., Lau, J., Hu, F. B., & Dawson‐Hughes, B. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-0298 · Cited by 2,020 · see citing works
Self-citationCellular senescence and the senescent secretory phenotype: therapeutic opportunities
Tchkonia, T., Zhu, Y., van Deursen, J., Campisi, J., & Kirkland, J. L. (2013) · Journal of Clinical Investigation · doi:10.1172/jci64098 · Cited by 1,774 · see citing works
Risk factors for periodontal disease
Genco, R. J., & Borgnakke, W. S. (2013) · Periodontology 2000 · doi:10.1111/j.1600-0757.2012.00457.x · Cited by 1,257 · see citing works
Ding, E. L., Song, Y., Malik, V. S., & Liu, S. (2006) · JAMA · doi:10.1001/jama.295.11.1288 · Cited by 1,354 · see citing works
Diabetes mellitus and periodontitis: a tale of two common interrelated diseases
Lalla, E., & Papapanou, P. N. (2011) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2011.106 · Cited by 1,063 · see citing works
Melamed, S., Shirom, A., Toker, S., Berliner, S., & Shapira, I. (2006) · Psychological Bulletin · doi:10.1037/0033-2909.132.3.327 · Cited by 943 · see citing works
Inflammatory markers in population studies of aging
Singh, T., & Newman, A. B. (2010) · Ageing Research Reviews · doi:10.1016/j.arr.2010.11.002 · Cited by 866 · see citing works
Inflammatory Markers and Risk of Type 2 Diabetes
Wang, X., Bao, W., Liu, J., OuYang, Y.-Y., Wang, D., Rong, S., Xiao, X., Shan, Z.-L., Zhang, Y., Yao, P., et al. (2013) · Diabetes Care · doi:10.2337/dc12-0702 · Cited by 820 · see citing works
Interleukin-6 Signaling and Anti-Interleukin-6 Therapeutics in Cardiovascular Disease
Ridker, P. M., & Rane, M. A. (2021) · Circulation Research · doi:10.1161/circresaha.121.319077 · Cited by 715 · see citing works
Interleukin-6 in Aging and Chronic Disease: A Magnificent Pathway
Maggio, M. G., Guralnik, J. M., Longo, D. L., & Ferrucci, L. (2006) · The Journals of Gerontology Series A · doi:10.1093/gerona/61.6.575 · Cited by 687 · see citing works
Akash, M. S. H., Rehman, K., & Liaqat, A. (2018) · Journal of Cellular Biochemistry · doi:10.1002/jcb.26174 · Cited by 690 · see citing works
Ridker, P. M., Wilson, P. W. F., & Grundy, S. M. (2004) · Circulation · doi:10.1161/01.cir.0000132467.45278.59 · Cited by 645 · see citing works
Antar, S. A., Ashour, N. A., Sharaky, M. M., Khattab, M., Ashour, N. A., Zaid, R. T., Roh, E. J., Elkamhawy, A., & Al-Karmalawy, A. A. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115734 · Cited by 749 · see citing works
Effect of exercise training on chronic inflammation
Beavers, K. M., Brinkley, T. E., & Nicklas, B. J. (2010) · Clinica Chimica Acta · doi:10.1016/j.cca.2010.02.069 · Cited by 592 · see citing works
Kell, D. B. (2009) · BMC Medical Genomics · doi:10.1186/1755-8794-2-2 · Cited by 554 · see citing works
Aune, D., Norat, T., Romundstad, P., & Vatten, L. J. (2013) · European Journal of Epidemiology · doi:10.1007/s10654-013-9852-5 · Cited by 539 · see citing works
Effective and viable mind-body stress reduction in the workplace: A randomized controlled trial.
Wolever, R. Q., Bobinet, K. J., McCabe, K., Mackenzie, E. R., Fekete, E., Kusnick, C. A., & Baime, M. (2012) · Journal of Occupational Health Psychology · doi:10.1037/a0027278 · Cited by 539 · see citing works
Kristiansen, O. P., & Mandrup-Poulsen, T. R. (2005) · Diabetes · doi:10.2337/diabetes.54.suppl_2.s114 · Cited by 525 · see citing works
Bjermo, H., Iggman, D., Kullberg, J., Dahlman, I., Johansson, L., Persson, L., Berglund, J., Pulkki, K., Basu, S., Uusitupa, M., et al. (2012) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.030114 · Cited by 490 · see citing works
Comorbidities in Chronic Obstructive Pulmonary Disease
Chatila, W. M., Thomashow, B. M., Minai, O. A., Criner, G. J., & Make, B. J. (2008) · Proceedings of the American Thoracic Society · doi:10.1513/pats.200709-148et · Cited by 477 · see citing works
Liu, C., Feng, X., Li, Q., Wang, Y., Li, Q., & Hua, M. (2016) · Cytokine · doi:10.1016/j.cyto.2016.06.028 · Cited by 470 · see citing works
Development and Validation of an Empirical Dietary Inflammatory Index
Tabung, F. K., Smith‐Warner, S. A., Chavarro, J. E., Wu, K., Fuchs, C. S., Hu, F. B., Chan, A. T., Willett, W. C., & Giovannucci, E. L. (2016) · Journal of Nutrition · doi:10.3945/jn.115.228718 · Cited by 477 · see citing works
Self-citationThe InterAct Consortium (2015) · Diabetologia · doi:10.1007/s00125-015-3585-9 · Cited by 469 · see citing works
Dietary pattern, inflammation, and incidence of type 2 diabetes in women
Schulze, M. B., Hoffmann, K., Manson, J. E., Willett, W. C., Meigs, J. B., Weikert, C., Heidemann, C., Colditz, G. A., & Hu, F. B. (2005) · American Journal of Clinical Nutrition · doi:10.1093/ajcn.82.3.675 · Cited by 462 · see citing works
Self-citationRole of innate and adaptive immunity in obesity-associated metabolic disease
McLaughlin, T., Ackerman, S. E., Shen, L., & Engleman, E. G. (2017) · Journal of Clinical Investigation · doi:10.1172/jci88876 · Cited by 444 · see citing works
Diagnosis and management of the metabolic syndrome
Grundy, S. M., Cleeman, J. I., Daniels, S. R., Donato, K. A., Eckel, R. H., Franklin, B. A., Gordon, D. J., Krauss, R. M., Savage, P. J., Smith, S. C., et al. (2005) · Current Opinion in Cardiology · doi:10.1097/01.hco.0000200416.65370.a0 · Cited by 434 · see citing works
Monocytes from type 2 diabetic patients have a pro-inflammatory profile
Giulietti, A., van Etten, E., Overbergh, L., Stoffels, K., Bouillon, R., & Mathieu, C. (2007) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2006.10.007 · Cited by 400 · see citing works
An immune origin of type 2 diabetes?
Kolb, H., & Mandrup-Poulsen, T. (2005) · Diabetologia · doi:10.1007/s00125-005-1764-9 · Cited by 394 · see citing works
Dietary pattern, inflammation, and incidence of type 2 diabetes in women
Schulze, M. B., Hoffmann, K., Manson, J. E., Willett, W. C., Meigs, J. B., Weikert, C., Heidemann, C., Colditz, G. A., & Hu, F. B. (2005) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/82.3.675 · Cited by 457 · see citing works
Self-citationWhat Does Minor Elevation of C-Reactive Protein Signify?
Kushner, I., Rzewnicki, D., & Samols, D. R. (2006) · The American Journal of Medicine · doi:10.1016/j.amjmed.2005.06.057 · Cited by 372 · see citing works
Mirza, S., Hossain, M., Mathews, C., Martinez, P., Pino, P., Gay, J. L., Rentfro, A., McCormick, J. B., & Fisher-Hoch, S. P. (2012) · Cytokine · doi:10.1016/j.cyto.2011.09.029 · Cited by 358 · see citing works
Pancreatic β-cell dysfunction in type 2 diabetes: Implications of inflammation and oxidative stress
Dludla, P. V., Mabhida, S. E., Ziqubu, K., Nkambule, B. B., Mazibuko-Mbeje, S. E., Hanser, S., Basson, A. K., Pheiffer, C., & Kengne, A. P. (2023) · World Journal of Diabetes · doi:10.4239/wjd.v14.i3.130 · Cited by 352 · see citing works
Probiotics in prevention and treatment of obesity: a critical view
Kobyliak, N. M., Conte, C., Cammarota, G., Haley, A. P., Štyriak, I., Gašpar, Ľ., Fusek, J., Rodrigo, L., & Kružliak, P. (2016) · Nutrition & Metabolism · doi:10.1186/s12986-016-0067-0 · Cited by 359 · see citing works
Ma, Y., Hébert, J. R., Li, W., Bertone‐Johnson, E. R., Olendzki, B. C., Pagoto, S., Tinker, L. F., Rosal, M. C., Ockene, I. S., Ockene, J. K., et al. (2008) · Nutrition · doi:10.1016/j.nut.2008.04.005 · Cited by 343 · see citing works
Toker, S., Shirom, A., Shapira, I., Berliner, S., & Melamed, S. (2005) · Journal of Occupational Health Psychology · doi:10.1037/1076-8998.10.4.344 · Cited by 340 · see citing works
Periodontal Disease and Incident Type 2 Diabetes
Demmer, R. T., Jacobs, D. R., & Desvarieux, M. (2008) · Diabetes Care · doi:10.2337/dc08-0026 · Cited by 336 · see citing works
Carbone, S., Buono, M. G. D., Ozemek, C., & Lavie, C. J. (2019) · Progress in Cardiovascular Diseases · doi:10.1016/j.pcad.2019.08.004 · Cited by 333 · see citing works
Alam, S., Hasan, M. K., Neaz, S., Hussain, N., Hossain, M. F., & Rahman, T. (2021) · Diabetology · doi:10.3390/diabetology2020004 · Cited by 326 · see citing works
Bharadwaj, U., Kasembeli, M. M., Robinson, P., & Tweardy, D. J. (2020) · Pharmacological Reviews · doi:10.1124/pr.119.018440 · Cited by 314 · see citing works
“…cells, leading to further release of proinflammatory cytokines, such as IL-6, from recruited inflammatory cells, such as macrophages (Pradhan et al., 2001; Hu et al., 2004; Wunderlich et al., 2013), which exacerbates unintended immune responses contributing to the pathology (Wensveen et al., 2015).”
BackgroundInflammatory Process in Type 2 Diabetes: The Role of Cytokines
ALEXANDRAKI, K., PIPERI, C., KALOFOUTIS, C., SINGH, J., ALAVERAS, A., & KALOFOUTIS, A. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1372.039 · Cited by 309 · see citing works
Nazmi, A., & Victora, C. G. (2007) · BMC Public Health · doi:10.1186/1471-2458-7-212 · Cited by 291 · see citing works
Samaras, K., Botelho, N. K., Chisholm, D. J., & Lord, R. V. (2009) · Obesity · doi:10.1038/oby.2009.443 · Cited by 287 · see citing works
DNA damage response and metabolic disease
Shimizu, I., Yoshida, Y., Suda, M., & Minamino, T. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.10.008 · Cited by 286 · see citing works
Cytokines and abnormal glucose and lipid metabolism
Shi, J., Fan, J., Su, Q., & Yang, Z. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00703 · Cited by 282 · see citing works
Whole-Grain, Bran, and Cereal Fiber Intakes and Markers of Systemic Inflammation in Diabetic Women
Qi, L., van Dam, R. M., Liu, S., Franz, M., Mantzoros, C., & Hu, F. B. (2006) · Diabetes Care · doi:10.2337/diacare.29.02.06.dc05-1903 · Cited by 261 · see citing works
Self-citationChronic Obstructive Pulmonary Disease, Asthma, and Risk of Type 2 Diabetes in Women
Rana, J. S., Mittleman, M. A., Sheikh, J. K., Hu, F. B., Manson, J. E., Colditz, G. A., Speizer, F. E., Barr, R. G., & Camargo, C. A. (2004) · Diabetes Care · doi:10.2337/diacare.27.10.2478 · Cited by 267 · see citing works
Self-citationRajpathak, S. N., Gunter, M. J., Wylie‐Rosett, J., Ho, G., Kaplan, R. C., Muzumdar, R. H., Rohan, T. E., & Strickler, H. D. (2009) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.919 · Cited by 263 · see citing works
Diabetes Mellitus-Associated Vascular Impairment
Tousoulis, D., Παπαγεωργίου, Ν., Androulakis, E. S., Siasos, G., Latsios, G., Tentolouris, K. N., & Stefanadis, C. (2013) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2013.03.089 · Cited by 263 · see citing works
Genetic Variation, C-Reactive Protein Levels, and Incidence of Diabetes
Dehghan, A., Kardys, I., de Maat, M. P. M., Uitterlinden, A. G., Sijbrands, E. J. G., Bootsma, A. H., Stijnen, T., Albert Hofman, D., Schram, M. T., & Witteman, J. C. M. (2007) · Diabetes · doi:10.2337/db06-0922 · Cited by 258 · see citing works
López‐García, E., van Dam, R. M., Qi, L., & Hu, F. B. (2006) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/84.4.888 · Cited by 257 · see citing works
Self-citationRelation of C-Reactive Protein to Abdominal Adiposity
Brooks, G. C., Blaha, M. J., & Blumenthal, R. S. (2010) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2010.02.017 · Cited by 255 · see citing works
Ranneh, Y., Ali, F., Akim, A. M., Hamid, H. A., Khaza’ai, H., & Fadel, A. (2017) · Applied Biological Chemistry · doi:10.1007/s13765-017-0285-9 · Cited by 258 · see citing works
Social relationships, sleep quality, and interleukin-6 in aging women
Friedman, E. M., Hayney, M. S., Love, G. D., Urry, H. L., Rosenkranz, M. A., Davidson, R. J., Singer, B. H., & Ryff, C. D. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509281102 · Cited by 247 · see citing works
Adverse childhood experiences and risk of type 2 diabetes: A systematic review and meta-analysis
Huang, H., Yan, P., Shan, Z., Chen, S., Li, M., Luo, C., Gao, H., Hao, L., & Liu, L. (2015) · Metabolism · doi:10.1016/j.metabol.2015.08.019 · Cited by 239 · see citing works
Abell, S. K., de Courten, B. V., Boyle, J. A., & Teede, H. J. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms160613442 · Cited by 243 · see citing works
Tataranni, P. A., & Ortega, E. (2005) · Diabetes · doi:10.2337/diabetes.54.4.917 · Cited by 239 · see citing works
Brown, T. T., Tassiopoulos, K., Bosch, R. J., Shikuma, C. M., & McComsey, G. A. (2010) · Diabetes Care · doi:10.2337/dc10-0633 · Cited by 236 · see citing works
Tuomisto, K., Jousilahti, P., Sundvall, J., Pajunen, P., & Salomaa, V. V. (2006) · Thrombosis and Haemostasis · doi:10.1160/th05-08-0571 · Cited by 231 · see citing works
Shankar, A., Sun, L.-P., Klein, B., Lee, K. E., Muntner, P., Nieto, F., Tsai, M., Cruickshanks, K., Schubert, C., Brazy, P., et al. (2011) · Kidney International · doi:10.1038/ki.2011.283 · Cited by 209 · see citing works
Chapter 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
Association of Oxidative Stress, Insulin Resistance, and Diabetes Risk Phenotypes
Meigs, J. B., Larson, M. G., Fox, C. S., Keaney, J. F., Vasan, R. S., & Benjamin, E. J. (2007) · Diabetes Care · doi:10.2337/dc07-0817 · Cited by 220 · see citing works
Self-citationHeidemann, C., Hoffmann, K., Spranger, J., Klipstein‐Grobusch, K., Möhlig, M., Pfeiffer, A. F. H., & Boeing, H. (2005) · Diabetologia · doi:10.1007/s00125-005-1743-1 · Cited by 220 · see citing works
Bakker, G. C., van Erk, M. J., Pellis, L., Wopereis, S., Rubingh, C. M., Cnubben, N. H., Kooistra, T., van Ommen, B., & Hendriks, H. F. (2010) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.28822 · Cited by 252 · see citing works
Sedentary Time and Markers of Chronic Low-Grade Inflammation in a High Risk Population
Henson, J. J., Yates, T. E., Edwardson, C. L., Khunti, K. K., Talbot, D. C. S., Gray, L. J., Leigh, T. M., Carter, P., & Davies, M. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078350 · Cited by 219 · see citing works
Inflammatory dietary pattern and risk of depression among women
Lucas, M., Chocano-Bedoya, P. O., Shulze, M. B., Mirzaei, F., O’Reilly, É. J., Okereke, O. I., Hu, F. B., Willett, W. C., & Ascherio, A. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.09.014 · Cited by 217 · see citing works
Self-citationElevated Levels of Interleukin-18 Predict the Development of Type 2 Diabetes
Thorand, B., Kolb, H., Baumert, J. J., Köenig, W., Chambless, L. E., Meisinger, C., Illig, T., Martin, S., & Herder, C. (2005) · Diabetes · doi:10.2337/diabetes.54.10.2932 · Cited by 216 · see citing works
C-reactive protein comes of age
Verma, S., Szmitko, P. E., & Ridker, P. M. (2005) · Nature Clinical Practice Cardiovascular Medicine · doi:10.1038/ncpcardio0074 · Cited by 210 · see citing works
Heidemann, C., Sun, Q., van Dam, R. M., Meigs, J. B., Zhang, C., Tworoger, S. S., Mantzoros, C. S., & Hu, F. B. (2008) · Annals of Internal Medicine · doi:10.7326/0003-4819-149-5-200809020-00005 · Cited by 208 · see citing works
Self-citationOxInflammation: From Subclinical Condition to Pathological Biomarker
Valacchi, G., Virgili, F., Cervellati, C., & Pecorelli, A. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00858 · Cited by 206 · see citing works
López‐Candales, A., Burgos, P. M. H., Hernández-Suárez, D. F., & Harris, D. A. (2017) · PubMed · Cited by 203 · see citing works
Blood pressure and risk of developing type 2 diabetes mellitus: The Women's Health Study
Conen, D., Ridker, P. M., Mora, S., Buring, J. E., & Glynn, R. J. (2007) · European Heart Journal · doi:10.1093/eurheartj/ehm400 · Cited by 203 · see citing works
Vitamin D and diabetes mellitus
Danescu, L. G., Levy, S., & Levy, J. (2008) · Endocrine · doi:10.1007/s12020-008-9115-5 · Cited by 200 · see citing works
Association of C-reactive protein with type 2 diabetes: prospective analysis and meta-analysis
Lee, C.-T., Adler, A., Sandhu, M. S., Sharp, S. J., Forouhi, N. G., Erqou, S. A., Luben, R., Bingham, S. A., Khaw, K., & Wareham, N. J. (2009) · Diabetologia · doi:10.1007/s00125-009-1338-3 · Cited by 201 · see citing works
Yokum, S., Ng, J., & Stice, E. M. (2011) · International Journal of Obesity · doi:10.1038/ijo.2011.175 · Cited by 199 · see citing works
Inflammation and the Incidence of Type 2 Diabetes
Bertoni, A. G., Burke, G. L., Owusu, J. A., Carnethon, M. R., Vaidya, D. M., Barr, R. G., Jenny, N. S., Ouyang, P., & Rotter, J. I. (2010) · Diabetes Care · doi:10.2337/dc09-1679 · Cited by 201 · see citing works
Liu, S. (2007) · Archives of Internal Medicine · doi:10.1001/archinte.167.15.1676 · Cited by 198 · see citing works
Phillips, C. M., Shivappa, N., Hébert, J. R., & Perry, I. J. (2018) · Nutrients · doi:10.3390/nu10081033 · Cited by 198 · see citing works
Adipokines and Risk of Type 2 Diabetes in Older Men
Wannamethee, S. G., Lowe, G. D. O., Rumley, A., Cherry, L., Whincup, P. H., & Sattar, N. A. (2007) · Diabetes Care · doi:10.2337/dc06-2416 · Cited by 194 · see citing works
Sun, S., Wang, K., Ma, K., Li, B. A. O., & Liu, H. (2019) · Chinese Journal of Natural Medicines · doi:10.1016/s1875-5364(19)30003-2 · Cited by 194 · see citing works
Marcos-Pérez, D., Sánchez-Flores, M., Proietti, S., Bonassi, S., Costa, S., Teixeira, J. P., Fernandez-Tajes, J. J., Pásaro, E., Laffón, B., & Valdiglesias, V. (2020) · GeroScience · doi:10.1007/s11357-020-00247-4 · Cited by 188 · see citing works
Qi, L., Cornelis, M. C., Kraft, P. L., Jensen, M. K., van Dam, R. M., Sun, Q., Girman, C. J., Laurie, C. C., Mirel, D. B., Hunter, D. J., et al. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq057 · Cited by 185 · see citing works
Self-citationObesity, inflammatory markers, and endometrial cancer risk: a prospective case–control study
Dossus, L., Rinaldi, S., Becker, S., Lukanova, A., Tjønneland, A. M., Olsen, A., Stegger, J. G., Overvad, K., Chabbert‐Buffet, N., Jiménez-Corona, A., et al. (2010) · Endocrine Related Cancer · doi:10.1677/erc-10-0053 · Cited by 186 · see citing works
Hemostatic Markers of Endothelial Dysfunction and Risk of Incident Type 2 Diabetes
Meigs, J. B., O’Donnell, C. J., Tofler, G. H., Benjamin, E. J., Fox, C. S., Lipinska, I., Nathan, D. M., SULLIVAN, L. M., D’Agostino, R. B., & Wilson, P. W. F. (2006) · Diabetes · doi:10.2337/diabetes.55.02.06.db05-1041 · Cited by 184 · see citing works
Self-citationBadawi, A. F. (2010) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmsott.s9089 · Cited by 224 · see citing works
Ye, X., Yu, Z., Li, H., Franco, O. H., Liu, Y., & Xu, L. (2007) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2007.01.065 · Cited by 177 · see citing works
Sex Differences in the Prediction of Type 2 Diabetes by Inflammatory Markers
Thorand, B., Baumert, J. J., Kolb, H., Meisinger, C., Chambless, L. E., Köenig, W., & Herder, C. (2007) · Diabetes Care · doi:10.2337/dc06-1693 · Cited by 173 · see citing works
Calcitriol blunts the deleterious impact of advanced glycation end products on endothelial cells
Talmor, Y., Golan, E., Benchetrit, S., Bernheim, J., Klein, O., Green, J., & Rashid, G. (2008) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00051.2008 · Cited by 169 · see citing works
What about non-alcoholic fatty liver disease as a new criterion to define metabolic syndrome?
Tarantino, G. (2013) · World Journal of Gastroenterology · doi:10.3748/wjg.v19.i22.3375 · Cited by 167 · see citing works
Sleep and cardiometabolic risk in children and adolescents
Quist, J. S., Sjödin, A. M., Chaput, J., & Hjorth, M. F. (2015) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2015.09.001 · Cited by 165 · see citing works
Inflammation, Coagulation, and the Pathway to Frailty
Kanapuru, B., & Ershler, W. B. (2009) · The American Journal of Medicine · doi:10.1016/j.amjmed.2009.01.030 · Cited by 163 · see citing works
Brunner, E. J., Mika Kivimaki, B., Witte, D. R., Lawlor, D. A., Smith, G. D., Cooper, J. A., Miller, M. A., Lowe, G. D. O., Rumley, A., Casas, J. P., et al. (2008) · PLoS Medicine · doi:10.1371/journal.pmed.0050155 · Cited by 161 · see citing works
Kim, M.-J., Lim, N.-K., Choi, S.-J., & Park, H. (2015) · Hypertension Research · doi:10.1038/hr.2015.72 · Cited by 163 · see citing works
Interrelationship between diabetes and periodontitis: Role of hyperlipidemia
Zhou, X., Zhang, W., Liu, X., Zhang, W., & Li, Y. (2014) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2014.11.008 · Cited by 157 · see citing works
The use of high-sensitivity assays for C-reactive protein in clinical practice
Musunuru, K., Kral, B. G., Blumenthal, R. S., Fuster, V., Campbell, C. Y., Gluckman, T. J., Lange, R. A., Topol, E. J., Willerson, J. T., Desai, M. Y., et al. (2008) · Nature Clinical Practice Cardiovascular Medicine · doi:10.1038/ncpcardio1322 · Cited by 153 · see citing works
Periodontal Infection, Systemic Inflammation, and Insulin Resistance
Demmer, R. T., Squillaro, A. I., Papapanou, P. N., ROSENBAUM, M. S., Friedewald, W. T., Jacobs, D. R., & Desvarieux, M. (2012) · Diabetes Care · doi:10.2337/dc12-0072 · Cited by 152 · see citing works
How the association between obesity and inflammation may lead to insulin resistance and cancer
Amin, M. N., Hussain, M. S., Sarwar, M. S., Moghal, M. M. R., Das, A., Hossain, M. Z., Chowdhury, J. A., Millat, M. S., & Islam, M. S. (2019) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2019.01.041 · Cited by 150 · see citing works
Roles of IL-6-gp130 Signaling in Vascular Inflammation
Hou, T., Tieu, B. C., Ray, S., Recinos, A., Cui, R., Tilton, R. G., & Brasier, A. R. (2008) · Current Cardiology Reviews · doi:10.2174/157340308785160570 · Cited by 149 · see citing works
Insulin-Like Growth Factor Axis and Risk of Type 2 Diabetes in Women
Rajpathak, S. N., He, M., Sun, Q., Kaplan, R. C., Muzumdar, R. H., Rohan, T. E., Gunter, M. J., Pollak, M., Kim, M., Pessin, J. E., et al. (2012) · Diabetes · doi:10.2337/db11-1488 · Cited by 148 · see citing works
Self-citation
- Authors
- Hu, F. B., Meigs, J. B., Li, T. Y., Rifai, N., & Manson, J. E.
- Affiliations
- Brigham and Women's Hospital (US)
- Harvard University (US)
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2004-03-01
- Volume
- 53
- Issue
- 3
- Pages
- 693-700
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- OpenAlex
- W2153214557
- Cited by
- 788
- References
- 51
- Citations by year
- 2026: 7 · 2025: 17 · 2024: 20 · 2023: 22 · 2022: 33 · 2021: 32 · 2020: 25 · 2019: 34 · 2018: 41 · 2017: 48 · 2016: 39 · 2015: 42 · 2014: 55 · 2013: 42 · 2012: 57
- FWCI
- 25.01
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Diabetes (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Cancer Institute (CA-87969, P01CA087969)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK058845, DK58845)
- Topics
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
- Health Sciences › Medicine › Oncology › Inflammatory Biomarkers in Disease Prognosis
- Keywords
- type 2 diabetes, inflammatory markers, C-reactive protein, interleukin-6, inflammation, diabetes risk prediction, women, Nurses' Health Study, body mass index
- MeSH terms
- Adult, Body Constitution, C-Reactive Protein, Diabetes Mellitus, Type 2, Female, Humans, Inflammation, Insulin, Menopause, Middle Aged, Risk Factors, Smoking, United States, Cohort Studies, Biomarkers, Antigens, CD, Interleukin-6, Body Mass Index, Receptors, Tumor Necrosis Factor, Receptors, Tumor Necrosis Factor, Type II
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