Associations of C-Reactive Protein With Measures of Obesity, Insulin Resistance, and Subclinical Atherosclerosis in Healthy, Middle-Aged Women
Open accessAbstract
Abstract —Obesity, the insulin resistance syndrome, and atherosclerosis are closely linked and may all be determinants of an increased acute-phase response. In this study, we examined the relationship of C-reactive protein (CRP) with measures of obesity, variables of the insulin resistance syndrome, and intima-media thickness of the common carotid arteries in 186 healthy, middle-aged women selected from the general population. Associations were assessed by regression analysis. CRP was strongly associated with body mass index (BMI) and waist circumference. CRP was also associated with other variables of the insulin resistance syndrome, including blood pressure, insulin, high density lipoprotein cholesterol, triglycerides, apolipoprotein A1 (inversely), plasminogen activator inhibitor-1 antigen, and tissue-type plasminogen activator antigen. Associations between CRP and the variables of the insulin resistance syndrome disappeared after controlling for BMI but remained significant for plasminogen activator inhibitor-1 antigen only. The association of CRP with common carotid artery intima-media thickness was weak and limited to ever-smokers. BMI explained 29.7% of the variance of CRP, whereas common carotid artery intima-media thickness explained only 3.7%. The results of this population-based study indicate that adiposity is strongly associated with CRP in healthy, middle-aged women. In this population, BMI accounted for the relationship between CRP and other variables of the insulin resistance syndrome. Further studies should determine whether losing weight ameliorates the inflammatory state.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Slightly elevated serum levels of C-reactive protein (IL-6-dependent) are closely interrelated with insulin resistance.
“This is confirmed by studies that describe a close interrelation of slightly elevated serum levels of C-reactive protein (IL-6-dependent) and a key element of the energy re-allocation program, namely insulin resistance [9,10].”
From Interaction of the endocrine system with inflammation: a function of energy and volume regulation (2014) · cites this paper as [9]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Friedewald, W. T., Levy, R. I., & Fredrickson, D. S. (1972) · Clinical Chemistry · doi:10.1093/clinchem/18.6.499 · Cited by 32,423 · see citing works
Matthews, D. R., Hosker, J. P., Rudenski, A. S., Naylor, B. A., Treacher, D. F., & Turner, R. C. (1985) · Diabetologia · doi:10.1007/bf00280883 · Cited by 31,502 · see citing works
The pathogenesis of atherosclerosis: a perspective for the 1990s
Ross, R. (1993) · Nature · doi:10.1038/362801a0 · Cited by 10,618 · 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
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
Baumann, H., & Gauldie, J. (1994) · Immunology Today · doi:10.1016/0167-5699(94)90137-6 · Cited by 2,907 · 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
Self-citationThe Prognostic Value of C-Reactive Protein and Serum Amyloid A Protein in Severe Unstable Angina
Liuzzo, G., Biasucci, L. M., Gallimore, J. R., Grillo, R. L., Rebuzzi, A. G., Pepys, M. B., & Maseri, A. (1994) · New England Journal of Medicine · doi:10.1056/nejm199408183310701 · Cited by 2,354 · see citing works
Common Carotid Intima-Media Thickness and Risk of Stroke and Myocardial Infarction
Bots, M. L., Hoes, A. W., Koudstaal, P. J., Albert Hofman, D., & Grobbee, D. E. (1997) · Circulation · doi:10.1161/01.cir.96.5.1432 · Cited by 2,333 · see citing works
Self-citationThompson, S. G., Kienast, J., Pyke, S., Haverkate, F., & van de Loo, J. C. W. (1995) · New England Journal of Medicine · doi:10.1056/nejm199503093321003 · Cited by 1,819 · see citing works
Atherosclerosis: Basic Mechanisms
Berliner, J. A., Navab, M., Fogelman, A. M., Frank, J. S., Demer, L. L., Edwards, P. A., Watson, A. D., & Lusis, A. J. (1995) · Circulation · doi:10.1161/01.cir.91.9.2488 · Cited by 1,726 · see citing works
Production of C-reactive protein and risk of coronary events in stable and unstable angina
Haverkate, E., Thompson, S. G., Pyke, S., Gallimore, J. R., & Mark B Pepys Group (1997) · The Lancet · doi:10.1016/s0140-6736(96)07591-5 · Cited by 1,511 · 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 1,287 · 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
Relation of C-Reactive Protein and Coronary Heart Disease in the MRFIT Nested Case-Control Study
Kuller, L. H., Tracy, R. P., Shaten, J., & Meilahn, E. N. (1996) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a008963 · Cited by 1,098 · see citing works
Steel, D. M., & Whitehead, A. S. (1994) · Immunology Today · doi:10.1016/0167-5699(94)90138-4 · Cited by 1,034 · see citing works
Mendall, M. A., Patel, P., Ballam, L., Strachan, D. P., & Northfield, T. C. (1996) · BMJ · doi:10.1136/bmj.312.7038.1061 · Cited by 847 · see citing works
Tracy, R. P., Lemaitre, R. N., Psaty, B. M., Ives, D. G., Evans, R. W., Cushman, M., Meilahn, E. N., & Kuller, L. H. (1997) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.17.6.1121 · Cited by 836 · see citing works
How good a marker is insulin level for insulin resistance?
Laakso, M. (1993) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a116768 · Cited by 726 · see citing works
Gupta, S., Leatham, E. W., Carrington, D., Mendall, M. A., Kaski, J. C., & Camm, A. J. (1997) · Circulation · doi:10.1161/01.cir.96.2.404 · Cited by 705 · see citing works
Patel, P., Mendall, M. A., Carrington, D., Strachan, D. P., Leatham, E., Molineaux, N., Levy, J., Blakeston, C., Seymour, C. A., Camm, A. J., et al. (1995) · BMJ · doi:10.1136/bmj.311.7007.711 · Cited by 592 · see citing works
Tracy, R. P., Psaty, B. M., Macy, E., Bovill, E. G., Cushman, M., Cornell, E. S., & Kuller, L. H. (1997) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.17.10.2167 · Cited by 539 · see citing works
Reproducibility of In Vivo Carotid Intima-Media Thickness Measurements
Kanters, S. D. J. M., Algra, A., van Leeuwen, M. S., & Banga, J.-D. (1997) · Stroke · doi:10.1161/01.str.28.3.665 · Cited by 365 · see citing works
Juhan-Vague, I., Thompson, S. G., & Jespersen, J. (1993) · Arteriosclerosis and Thrombosis A Journal of Vascular Biology · doi:10.1161/01.atv.13.12.1865 · Cited by 326 · see citing works
Solid phase radioimmunoassays for human C-reactive protein
Shine, B. S. F., de Beer, F. C., & Pepys, M. B. (1981) · Clinica Chimica Acta · doi:10.1016/0009-8981(81)90005-x · Cited by 320 · see citing works
Cabana, V. G., Siegel, J. N., & Sabesin, S. M. (1989) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)38390-5 · Cited by 307 · see citing works
Nieto, F. J., Adam, E., Sorlie, P. D., Farzadegan, H., Melnick, J. L., Comstock, G. W., & Szklo, M. (1996) · Circulation · doi:10.1161/01.cir.94.5.922 · Cited by 303 · see citing works
Katsuki, A., Sumida, Y., Murashima, S., Murata, K., Takarada, Y., Ito, K., Fujii, M., Tsuchihashi, K., Goto, H., Nakatani, K., et al. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.3.4618 · Cited by 301 · see citing works
Lipids, lipoproteins, and apoproteins in serum during infection.
Alvarez, C., & Ramos, A. (1986) · Clinical Chemistry · doi:10.1093/clinchem/32.1.142 · Cited by 285 · see citing works
Repression of interleukin‐6 gene expression by 17β‐estradiol:
Ray, P., Ghosh, S., Zhang, D.-H., & Ray, A. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)00487-0 · Cited by 254 · see citing works
SOME ATHEROGENIC CONCOMITANTS OF MENOPAUSE: THE FRAMINGHAM STUDY
Hjortland, M. C., McNamara, P., & Kannel, W. B. (1976) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a112228 · Cited by 243 · see citing works
Nilsson, J. Å., Jovinge, S. V., Niemann, A., Reneland, R., & Lithell, H. (1998) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.18.8.1199 · Cited by 200 · see citing works
Heinrich, J., Schulte, H., Schönfeld, R., Köhler, E., & Assmann, G. (1995) · Thrombosis and Haemostasis · doi:10.1055/s-0038-1653783 · Cited by 200 · see citing works
Hormonal control of regional fat distribution
Björntorp, P. A. (1997) · Human Reproduction · doi:10.1093/humrep/12.suppl_1.21 · Cited by 170 · see citing works
Reproducibility of carotid vessel wall thickness measurements. the rotterdam study
Bots, M. L., Mulder, P. G. H., Albert Hofman, D., van Es, G., & Grobbee, D. E. (1994) · Journal of Clinical Epidemiology · doi:10.1016/0895-4356(94)90196-1 · Cited by 136 · see citing works
Self-citationGauldie, J., Richards, C. D., Northemann, W., et al. (1989) · PubMed · Cited by 100 · see citing works
Bots, M. L., de Jong, P. T. V. M., Albert Hofman, D., & Grobbee, D. E. (1997) · Journal of Clinical Epidemiology · doi:10.1016/s0895-4356(97)00059-0 · Cited by 96 · see citing works
Self-citationGauldie, J., Richards, C. D., Northemann, W., et al. (1989) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1989.tb23998.x · Cited by 96 · see citing works
Tuck, C. H., Holleran, S., & Berglund, L. (1997) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.17.9.1822 · Cited by 81 · see citing works
'Curing' empty follicle syndrome
Ndukwe, G., Thornton, S. J., Fishel, S. B., et al. (1997) · Human Reproduction · doi:10.1093/humrep/12.1.21 · Cited by 81 · see citing works
C‐reactive Protein in Population Samples
Palosuo, T., Husman, T. M., Koistinen, J., & Aho, K. (1986) · Acta Medica Scandinavica · doi:10.1111/j.0954-6820.1986.tb02746.x · Cited by 78 · see citing works
DAVIS, C. E., Pająk, A., Rywik, S. L., Williams, D. H., Broda, G., Pażucha, T., & Ephross, S. A. (1994) · Annals of Epidemiology · doi:10.1016/1047-2797(94)90003-5 · Cited by 65 · see citing works
Highton, J., & Hessian, P. A. (1984) · Journal of Immunological Methods · doi:10.1016/0022-1759(84)90149-2 · Cited by 64 · see citing works
Insulin Resistance Syndrome and Fibrinolytic Activity: The Northern Sweden MONICA Study
Lindahl, B., Asplund, K., Eliasson, M., & Evrin, P. (1996) · International Journal of Epidemiology · doi:10.1093/ije/25.2.291 · Cited by 59 · see citing works
Mohamed‐Ali, V., Gould, M., Gillies, S., Goubet, S., Yudkin, J. S., & Haines, A. (1995) · Diabetologia · doi:10.1007/bf00402183 · Cited by 50 · see citing works
Aune, B., Øian, P., Omsjø, I. H., et al. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)90433-6 · Cited by 48 · see citing works
HDL cholesterol and the acute phase reaction following myocardial infarction and acute pancreatitis
Fahie‐Wilson, M. N., Mills, R., & Wilson, K. (1987) · Clinica Chimica Acta · doi:10.1016/0009-8981(87)90372-x · Cited by 35 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Yudkin JS, Stehouwer CDA, Emeis JJ, Coppack SW. Insulin resistance syndrome and endothelial damage: role of adipose tissue derived proin- flammatory cytokines. Arterioscler Thromb Vasc Biol. In press.
- Cushman M, Meilahn EN, Kuller LH, Psaty BM, Tracy RP. Hormone replacement therapy (HRT) and markers of hemostasis and inflammation in elderly women. [Abstract.]. Santa Fe, NM: 38th Annual Conference on Cardiovascular Disease Epidemiology and Prevention, March 18 -20, 1998; Circulation. 1998;97:814.
Cited by
Sorted by citations
Inflammation: the link between insulin resistance, obesity and diabetes
Dandona, P. (2004) · Trends in Immunology · doi:10.1016/j.it.2003.10.013 · Cited by 2,170 · see citing works
Klein, S., Burke, L. E., Bray, G. A., Blair, S., Allison, D. B., Pi-Sunyer, X., Hong, Y., & Eckel, R. H. (2004) · Circulation · doi:10.1161/01.cir.0000145546.97738.1e · Cited by 934 · see citing works
Early inflammation and dementia: A 25‐year follow‐up of the Honolulu‐Asia aging study
Schmidt, R., Schmidt, H., Curb, J. D., Masaki, K., White, L. R., & Launer, L. J. (2002) · Annals of Neurology · doi:10.1002/ana.10265 · Cited by 710 · see citing works
Roberts, W. L., Moulton, L., Law, T. C., Farrow, G., Cooper-Anderson, M., Savory, J., & Rifai, N. (2001) · Clinical Chemistry · doi:10.1093/clinchem/47.3.418 · Cited by 652 · see citing works
Liu, S., Manson, J. E., Buring, J. E., Stampfer, M. J., Willett, W. C., & Ridker, P. M. (2002) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/75.3.492 · Cited by 594 · see citing works
Weight Loss Reduces C-Reactive Protein Levels in Obese Postmenopausal Women
Tchernof, A., Nolan, A., Sites, C. K., Ades, P. A., & Poehlman, E. T. (2002) · Circulation · doi:10.1161/hc0502.103331 · Cited by 541 · see citing works
Body mass index and the risk of stroke in men
Kurth, T., Gaziano, J. M., Berger, K., Kase, C. S., Rexrode, K. M., Cook, N. R., Buring, J. E., & Manson, J. E. (2002) · Archives of Internal Medicine · doi:10.1001/archinte.162.22.2557 · Cited by 524 · see citing works
Kim, C.-S., Park, H.-S., Kawada, T., Kim, J.-H., Lim, D., Hubbard, N. E., Kwon, B.-S., Erickson, K. L., & Yu, R. (2006) · International Journal of Obesity · doi:10.1038/sj.ijo.0803259 · Cited by 511 · see citing works
The implication of obesity and central fat on markers of chronic inflammation: The ATTICA study
PANAGIOTAKOS, D., PITSAVOS, C., YANNAKOULIA, M., CHRYSOHOOU, C., & STEFANADIS, C. (2005) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2005.03.010 · Cited by 340 · see citing works
Association of high-sensitivity C-reactive protein with <i>de novo</i> major depression
Pasco, J. A., Nicholson, G. C., Williams, L. J., Jacka, F. N., Henry, M. J., Kotowicz, M. A., Schneider, H. G., Leonard, B. E., & Berk, M. (2010) · British Journal of Psychiatry · doi:10.1192/bjp.bp.109.076430 · Cited by 321 · see citing works
Heilbronn, L. K., Noakes, M., & Clifton, P. M. (2001) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.21.6.968 · Cited by 331 · see citing works
Inflammatory 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
Yoneda, M., Mawatari, H., Fujita, K., Iida, H., Yonemitsu, K., Kato, S., Takahashi, H., Kirikoshi, H., Inamori, M., Nozaki, Y., et al. (2007) · Journal of Gastroenterology · doi:10.1007/s00535-007-2060-x · Cited by 294 · see citing works
Nicklas, B. J. (2005) · Canadian Medical Association Journal · doi:10.1503/cmaj.1040769 · Cited by 259 · see citing works
Is Hypertension an Inflammatory Process?
Boos, C., & Lip, G. (2006) · Current Pharmaceutical Design · doi:10.2174/138161206776843313 · Cited by 165 · see citing works
Interaction of the endocrine system with inflammation: a function of energy and volume regulation
Straub, R. H. (2014) · Arthritis Research & Therapy · doi:10.1186/ar4484 · Cited by 121 · see citing works
“This is confirmed by studies that describe a close interrelation of slightly elevated serum levels of C-reactive protein (IL-6dependent) and a key element of the energy re-allocation program, namely insulin resistance [9,10].”
BackgroundCo-morbidity in rheumatoid arthritis
Mikuls, T. R. (2003) · Best Practice & Research Clinical Rheumatology · doi:10.1016/s1521-6942(03)00041-x · Cited by 122 · see citing works
Inflammatory cardiovascular risk markers in women with hypopituitarism
Sesmilo, G., Miller, K. K., Hayden, D., & Klibanski, A. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.12.8087 · Cited by 97 · see citing works
Pihl, E., Zilmer, K., Kullisaar, T., Kairane, C., Mägi, A., & Zilmer, M. (2006) · International Journal of Obesity · doi:10.1038/sj.ijo.0803068 · Cited by 84 · see citing works
Heilbronn, L. K., & Clifton, P. M. (2002) · The Journal of Nutritional Biochemistry · doi:10.1016/s0955-2863(02)00187-0 · Cited by 80 · see citing works
Sick fat: the good and the bad of old and new circulating markers of adipose tissue inflammation
Barchetta, I., Cimini, F. A., Ciccarelli, G., Baroni, M. G., & Cavallo, M. G. (2019) · Journal of Endocrinological Investigation · doi:10.1007/s40618-019-01052-3 · Cited by 77 · see citing works
Atherosclerosis in women with endometriosis
Pretta, S., Remorgida, V., Abbamonte, L. H., Anserini, P., Ragni, N., Del Sette, M., Gandolfo, C., & Ferrero, S. (2007) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2006.04.015 · Cited by 44 · see citing works
- Authors
- Hak, A. E., Stehouwer, C. D. A., Bots, M. L., Polderman, K. H., Schalkwijk, C. G., Westendorp, I. C. D., Hofman, A., & Witteman, J. C. M.
- Affiliations
- University Medical Center Utrecht (NL)
- From the Department of Epidemiology and Biostatistics (A.E.H., M.L.B., I.C.D.W., A.H., J.C.M.W.), Erasmus University Medical School, Rotterdam; the Department of Internal Medicine (C.D.A.S., K.H.P.), University Hospital Vrije Universiteit and Institute for Cardiovascular Research Vrije Universiteit, Amsterdam; the Julius Center for Patient Oriented Research (M.L.B.), University Medical Center Utrecht, Utrecht; and the Department of Clinical Chemistry (C.G.S.), University Hospital Vrije Universiteit...
- Venue
- Arteriosclerosis, Thrombosis, and Vascular Biology
- Published
- 1999-08
- Volume
- 19
- Issue
- 8
- Pages
- 1986-1991
- ISSN
- 1079-5642 (ISSN-L)
- 1524-4636
- OpenAlex
- W2162483087
- Cited by
- 525
- References
- 47
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 6 · 2023: 5 · 2022: 7 · 2021: 15 · 2020: 6 · 2019: 4 · 2018: 6 · 2017: 10 · 2016: 13 · 2015: 12 · 2014: 17 · 2013: 14 · 2012: 19
- FWCI
- 21.67
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Arteriosclerosis Thrombosis and Vascular Biology (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion, other-oa)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, other-oa)
- RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek
- 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 › Surgery › Lipoproteins and Cardiovascular Health
- Keywords
- C-reactive protein, obesity, metabolic syndrome, subclinical atherosclerosis, carotid intima-media thickness, middle-aged women, body mass index, waist circumference, adiposity, acute phase response, plasminogen activator inhibitor-1, tissue plasminogen activator, smoking, inflammation
- MeSH terms
- Adult, Arteriosclerosis, Body Height, Body Weight, C-Reactive Protein, Female, Humans, Insulin Resistance, Middle Aged, Obesity, Smoking, Body Mass Index, Carotid Artery, Common, Tunica Intima, Tunica Media, Premenopause, Postmenopause
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review