Skip to main content
Top
Published in: Cardiovascular Diabetology 1/2018

Open Access 01-12-2018 | Original investigation

Comparing the inflammatory profiles for incidence of diabetes mellitus and cardiovascular diseases: a prospective study exploring the ‘common soil’ hypothesis

Authors: Xue Bao, Yan Borné, Linda Johnson, Iram Faqir Muhammad, Margaretha Persson, Kaijun Niu, Gunnar Engström

Published in: Cardiovascular Diabetology | Issue 1/2018

Login to get access

Abstract

Background

Chronic low-grade inflammation and associated insulin resistance and metabolic abnormalities have been proposed as ‘common soil’ for diabetes mellitus (DM) and cardiovascular disease (CVD). This paper aimed to investigate the inflammatory profiles of DM and CVD and to distinguish their shared and specific markers.

Methods

Based on the Malmö Diet and Cancer cohort, total and differential leukocyte counts were measured in 25,969 participants without previous DM or CVD and were studied in relation to incident DM (mean follow-up 17.4 ± 5.58 years) and incident CVD (i.e., coronary events, including fatal and nonfatal myocardial infarction, or stroke); mean follow-up 17.7 ± 5.46 years, using multivariable Cox regression models. Furthermore, plasma concentrations of another seven inflammatory markers were examined in relation to incident DM and incident CVD in a sub-cohort of 4658 participants. The associations of each inflammatory marker with incident DM versus incident CVD were compared using the Lunn–McNeil competing risks approach. In sensitivity analyses, those who developed both DM and CVD during follow-up were excluded.

Results

After adjustment for conventional risk factors, total and differential leukocyte counts, orosomucoid, and C-reactive protein were associated with an increased risk of both DM and CVD. Neutrophil to lymphocyte ratio, ceruloplasmin, alpha1-antitrypsin and soluble urokinase plasminogen activator receptor predicted increased risk of CVD but not DM, while haptoglobin and complement C3 showed the opposite pattern. In competing risks analyses, lymphocyte count and complement C3 had stronger associations with risk of DM than with risk of CVD (p for equal associations = 0.020 and 0.006). The reverse was true for neutrophil to lymphocyte ratio (p for equal associations = 0.025). Results were consistent in sensitivity analyses.

Conclusions

The results indicated substantial similarities in the inflammatory profiles associated with DM and CVD. However, there are also significant differences. These findings may help discriminate between individuals at elevated risk of DM and those at elevated risk of CVD, which is a prerequisite for targeted therapies.
Appendix
Available only for authorised users
Literature
1.
go back to reference Collaboration Emerging Risk Factors. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet. 2010;375(9733):2215–22.CrossRef Collaboration Emerging Risk Factors. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet. 2010;375(9733):2215–22.CrossRef
2.
go back to reference D’Agostino RB Jr, Hamman RF, Karter AJ, Mykkanen L, Wagenknecht LE, Haffner SM. Insulin Resistance Atherosclerosis Study I. Cardiovascular disease risk factors predict the development of type 2 diabetes: the insulin resistance atherosclerosis study. Diabetes Care. 2004;27(9):2234–40.CrossRefPubMed D’Agostino RB Jr, Hamman RF, Karter AJ, Mykkanen L, Wagenknecht LE, Haffner SM. Insulin Resistance Atherosclerosis Study I. Cardiovascular disease risk factors predict the development of type 2 diabetes: the insulin resistance atherosclerosis study. Diabetes Care. 2004;27(9):2234–40.CrossRefPubMed
3.
go back to reference Odegaard AO, Jacobs DR Jr, Sanchez OA, Goff DC Jr, Reiner AP, Gross MD. Oxidative stress, inflammation, endothelial dysfunction and incidence of type 2 diabetes. Cardiovasc Diabetol. 2016;15:51.CrossRefPubMedCentralPubMed Odegaard AO, Jacobs DR Jr, Sanchez OA, Goff DC Jr, Reiner AP, Gross MD. Oxidative stress, inflammation, endothelial dysfunction and incidence of type 2 diabetes. Cardiovasc Diabetol. 2016;15:51.CrossRefPubMedCentralPubMed
4.
go back to reference Stern MP. Diabetes and cardiovascular disease. The “common soil” hypothesis. Diabetes. 1995;44(4):369–74.CrossRefPubMed Stern MP. Diabetes and cardiovascular disease. The “common soil” hypothesis. Diabetes. 1995;44(4):369–74.CrossRefPubMed
5.
go back to reference Shu L, Chan KHK, Zhang G, Huan T, Kurt Z, Zhao Y, Codoni V, Tregouet DA, Cardiogenics C, Yang J, et al. Shared genetic regulatory networks for cardiovascular disease and type 2 diabetes in multiple populations of diverse ethnicities in the United States. PLoS Genet. 2017;13(9):e1007040.CrossRefPubMedCentralPubMed Shu L, Chan KHK, Zhang G, Huan T, Kurt Z, Zhao Y, Codoni V, Tregouet DA, Cardiogenics C, Yang J, et al. Shared genetic regulatory networks for cardiovascular disease and type 2 diabetes in multiple populations of diverse ethnicities in the United States. PLoS Genet. 2017;13(9):e1007040.CrossRefPubMedCentralPubMed
6.
go back to reference Moreno-Viedma V, Amor M, Sarabi A, Bilban M, Staffler G, Zeyda M, Stulnig TM. Common dysregulated pathways in obese adipose tissue and atherosclerosis. Cardiovasc Diabetol. 2016;15(1):120.CrossRefPubMedCentralPubMed Moreno-Viedma V, Amor M, Sarabi A, Bilban M, Staffler G, Zeyda M, Stulnig TM. Common dysregulated pathways in obese adipose tissue and atherosclerosis. Cardiovasc Diabetol. 2016;15(1):120.CrossRefPubMedCentralPubMed
7.
go back to reference Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol. 2011;11(2):98–107.CrossRefPubMed Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol. 2011;11(2):98–107.CrossRefPubMed
8.
go back to reference Ruparelia N, Chai JT, Fisher EA, Choudhury RP. Inflammatory processes in cardiovascular disease: a route to targeted therapies. Nat Rev Cardiol. 2017;14(3):133–44.CrossRefPubMed Ruparelia N, Chai JT, Fisher EA, Choudhury RP. Inflammatory processes in cardiovascular disease: a route to targeted therapies. Nat Rev Cardiol. 2017;14(3):133–44.CrossRefPubMed
9.
go back to reference Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120(16):1640–5.CrossRefPubMed Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120(16):1640–5.CrossRefPubMed
10.
11.
go back to reference Sattar N, McConnachie A, Shaper AG, Blauw GJ, Buckley BM, de Craen AJ, Ford I, Forouhi NG, Freeman DJ, Jukema JW, et al. Can metabolic syndrome usefully predict cardiovascular disease and diabetes? Outcome data from two prospective studies. Lancet. 2008;371(9628):1927–35.CrossRefPubMed Sattar N, McConnachie A, Shaper AG, Blauw GJ, Buckley BM, de Craen AJ, Ford I, Forouhi NG, Freeman DJ, Jukema JW, et al. Can metabolic syndrome usefully predict cardiovascular disease and diabetes? Outcome data from two prospective studies. Lancet. 2008;371(9628):1927–35.CrossRefPubMed
12.
go back to reference Everett BM, Donath MY, Pradhan AD, Thuren T, Pais P, Nicolau JC, Glynn RJ, Libby P, Ridker PM. Anti-inflammatory therapy with canakinumab for the prevention and management of diabetes. J Am Coll Cardiol. 2018;71:2392–401.CrossRefPubMed Everett BM, Donath MY, Pradhan AD, Thuren T, Pais P, Nicolau JC, Glynn RJ, Libby P, Ridker PM. Anti-inflammatory therapy with canakinumab for the prevention and management of diabetes. J Am Coll Cardiol. 2018;71:2392–401.CrossRefPubMed
13.
go back to reference Tenenbaum A, Fisman EZ. Mirroring the CANTOS revolution: is anti-inflammatory therapy for diabetes just around the corner? Cardiovasc Diabetol. 2017;16(1):91.CrossRefPubMedCentralPubMed Tenenbaum A, Fisman EZ. Mirroring the CANTOS revolution: is anti-inflammatory therapy for diabetes just around the corner? Cardiovasc Diabetol. 2017;16(1):91.CrossRefPubMedCentralPubMed
14.
go back to reference Ridker PM, Everett BM, Thuren T, MacFadyen JG, Chang WH, Ballantyne C, Fonseca F, Nicolau J, Koenig W, Anker SD, et al. Antiinflammatory therapy with canakinumab for atherosclerotic disease. N Engl J Med. 2017;377(12):1119–31.CrossRefPubMed Ridker PM, Everett BM, Thuren T, MacFadyen JG, Chang WH, Ballantyne C, Fonseca F, Nicolau J, Koenig W, Anker SD, et al. Antiinflammatory therapy with canakinumab for atherosclerotic disease. N Engl J Med. 2017;377(12):1119–31.CrossRefPubMed
15.
go back to reference Fizelova M, Jauhiainen R, Kangas AJ, Soininen P, Ala-Korpela M, Kuusisto J, Laakso M, Stancakova A. Differential associations of inflammatory markers with insulin sensitivity and secretion: the prospective METSIM study. J Clin Endocrinol Metab. 2017;102(9):3600–9.CrossRefPubMedPubMedCentral Fizelova M, Jauhiainen R, Kangas AJ, Soininen P, Ala-Korpela M, Kuusisto J, Laakso M, Stancakova A. Differential associations of inflammatory markers with insulin sensitivity and secretion: the prospective METSIM study. J Clin Endocrinol Metab. 2017;102(9):3600–9.CrossRefPubMedPubMedCentral
16.
go back to reference Greenberg AS, Obin MS. Obesity and the role of adipose tissue in inflammation and metabolism. Am J Clin Nutr. 2006;83(2):461S–5S.CrossRefPubMed Greenberg AS, Obin MS. Obesity and the role of adipose tissue in inflammation and metabolism. Am J Clin Nutr. 2006;83(2):461S–5S.CrossRefPubMed
17.
go back to reference Gillum RF, Mussolino ME, Madans JH. Counts of neutrophils, lymphocytes, and monocytes, cause-specific mortality and coronary heart disease: the NHANES-I epidemiologic follow-up study. Ann Epidemiol. 2005;15(4):266–71.CrossRefPubMed Gillum RF, Mussolino ME, Madans JH. Counts of neutrophils, lymphocytes, and monocytes, cause-specific mortality and coronary heart disease: the NHANES-I epidemiologic follow-up study. Ann Epidemiol. 2005;15(4):266–71.CrossRefPubMed
18.
go back to reference Horne BD, Anderson JL, John JM, Weaver A, Bair TL, Jensen KR, Renlund DG, Muhlestein JB. Intermountain Heart Collaborative Study G. Which white blood cell subtypes predict increased cardiovascular risk? J Am Coll Cardiol. 2005;45(10):1638–43.CrossRefPubMed Horne BD, Anderson JL, John JM, Weaver A, Bair TL, Jensen KR, Renlund DG, Muhlestein JB. Intermountain Heart Collaborative Study G. Which white blood cell subtypes predict increased cardiovascular risk? J Am Coll Cardiol. 2005;45(10):1638–43.CrossRefPubMed
19.
go back to reference Lorenzo C, Hanley AJ, Haffner SM. Differential white cell count and incident type 2 diabetes: the insulin resistance atherosclerosis study. Diabetologia. 2014;57(1):83–92.CrossRefPubMed Lorenzo C, Hanley AJ, Haffner SM. Differential white cell count and incident type 2 diabetes: the insulin resistance atherosclerosis study. Diabetologia. 2014;57(1):83–92.CrossRefPubMed
20.
go back to reference Madjid M, Awan I, Willerson JT, Casscells SW. Leukocyte count and coronary heart disease: implications for risk assessment. J Am Coll Cardiol. 2004;44(10):1945–56.CrossRefPubMed Madjid M, Awan I, Willerson JT, Casscells SW. Leukocyte count and coronary heart disease: implications for risk assessment. J Am Coll Cardiol. 2004;44(10):1945–56.CrossRefPubMed
21.
go back to reference Rana JS, Boekholdt SM, Ridker PM, Jukema JW, Luben R, Bingham SA, Day NE, Wareham NJ, Kastelein JJ, Khaw KT. Differential leucocyte count and the risk of future coronary artery disease in healthy men and women: the EPIC-Norfolk Prospective Population Study. J Intern Med. 2007;262(6):678–89.CrossRefPubMed Rana JS, Boekholdt SM, Ridker PM, Jukema JW, Luben R, Bingham SA, Day NE, Wareham NJ, Kastelein JJ, Khaw KT. Differential leucocyte count and the risk of future coronary artery disease in healthy men and women: the EPIC-Norfolk Prospective Population Study. J Intern Med. 2007;262(6):678–89.CrossRefPubMed
22.
go back to reference Wheeler JG, Mussolino ME, Gillum RF, Danesh J. Associations between differential leucocyte count and incident coronary heart disease: 1764 incident cases from seven prospective studies of 30,374 individuals. Eur Heart J. 2004;25(15):1287–92.CrossRefPubMed Wheeler JG, Mussolino ME, Gillum RF, Danesh J. Associations between differential leucocyte count and incident coronary heart disease: 1764 incident cases from seven prospective studies of 30,374 individuals. Eur Heart J. 2004;25(15):1287–92.CrossRefPubMed
23.
go back to reference Zhang H, Yang Z, Zhang W, Niu Y, Li X, Qin L, Su Q. White blood cell subtypes and risk of type 2 diabetes. J Diabetes Complications. 2017;31(1):31–7.CrossRefPubMed Zhang H, Yang Z, Zhang W, Niu Y, Li X, Qin L, Su Q. White blood cell subtypes and risk of type 2 diabetes. J Diabetes Complications. 2017;31(1):31–7.CrossRefPubMed
24.
go back to reference Engström G, Hedblad B, Eriksson KF, Janzon L, Lindgarde F. Complement C3 is a risk factor for the development of diabetes: a population-based cohort study. Diabetes. 2005;54(2):570–5.CrossRefPubMed Engström G, Hedblad B, Eriksson KF, Janzon L, Lindgarde F. Complement C3 is a risk factor for the development of diabetes: a population-based cohort study. Diabetes. 2005;54(2):570–5.CrossRefPubMed
25.
go back to reference Muscari A, Antonelli S, Bianchi G, Cavrini G, Dapporto S, Ligabue A, Ludovico C, Magalotti D, Poggiopollini G, Zoli M, et al. Serum C3 is a stronger inflammatory marker of insulin resistance than C-reactive protein, leukocyte count, and erythrocyte sedimentation rate: comparison study in an elderly population. Diabetes Care. 2007;30(9):2362–8.CrossRefPubMed Muscari A, Antonelli S, Bianchi G, Cavrini G, Dapporto S, Ligabue A, Ludovico C, Magalotti D, Poggiopollini G, Zoli M, et al. Serum C3 is a stronger inflammatory marker of insulin resistance than C-reactive protein, leukocyte count, and erythrocyte sedimentation rate: comparison study in an elderly population. Diabetes Care. 2007;30(9):2362–8.CrossRefPubMed
26.
go back to reference Manjer J, Carlsson S, Elmstahl S, Gullberg B, Janzon L, Lindstrom M, Mattisson I, Berglund G. The Malmo Diet and Cancer Study: representativity, cancer incidence and mortality in participants and non-participants. Eur J Cancer Prev. 2001;10(6):489–99.CrossRefPubMed Manjer J, Carlsson S, Elmstahl S, Gullberg B, Janzon L, Lindstrom M, Mattisson I, Berglund G. The Malmo Diet and Cancer Study: representativity, cancer incidence and mortality in participants and non-participants. Eur J Cancer Prev. 2001;10(6):489–99.CrossRefPubMed
27.
go back to reference Zia E, Melander O, Bjorkbacka H, Hedblad B, Engström G. Total and differential leucocyte counts in relation to incidence of stroke subtypes and mortality: a prospective cohort study. J Intern Med. 2012;272(3):298–304.CrossRefPubMed Zia E, Melander O, Bjorkbacka H, Hedblad B, Engström G. Total and differential leucocyte counts in relation to incidence of stroke subtypes and mortality: a prospective cohort study. J Intern Med. 2012;272(3):298–304.CrossRefPubMed
28.
go back to reference Hedblad B, Nilsson P, Janzon L, Berglund G. Relation between insulin resistance and carotid intima-media thickness and stenosis in non-diabetic subjects. Results from a cross-sectional study in Malmo, Sweden. Diabet Med. 2000;17(4):299–307.CrossRefPubMed Hedblad B, Nilsson P, Janzon L, Berglund G. Relation between insulin resistance and carotid intima-media thickness and stenosis in non-diabetic subjects. Results from a cross-sectional study in Malmo, Sweden. Diabet Med. 2000;17(4):299–307.CrossRefPubMed
29.
go back to reference Borne Y, Muhammad IF, Lores-Motta L, Hedblad B, Nilsson PM, Melander O, de Jong EK, Blom AM, den Hollander AI, Engström G. Complement C3 associates with incidence of diabetes, but no evidence of a causal relationship. J Clin Endocrinol Metab. 2017;102(12):4477–85.CrossRefPubMed Borne Y, Muhammad IF, Lores-Motta L, Hedblad B, Nilsson PM, Melander O, de Jong EK, Blom AM, den Hollander AI, Engström G. Complement C3 associates with incidence of diabetes, but no evidence of a causal relationship. J Clin Endocrinol Metab. 2017;102(12):4477–85.CrossRefPubMed
30.
go back to reference Muhammad IF, Borne Y, Hedblad B, Nilsson PM, Persson M, Engström G. Acute-phase proteins and incidence of diabetes: a population-based cohort study. Acta Diabetol. 2016;53(6):981–9.CrossRefPubMedCentralPubMed Muhammad IF, Borne Y, Hedblad B, Nilsson PM, Persson M, Engström G. Acute-phase proteins and incidence of diabetes: a population-based cohort study. Acta Diabetol. 2016;53(6):981–9.CrossRefPubMedCentralPubMed
31.
go back to reference Eugen-Olsen J, Andersen O, Linneberg A, Ladelund S, Hansen TW, Langkilde A, Petersen J, Pielak T, Moller LN, Jeppesen J, et al. Circulating soluble urokinase plasminogen activator receptor predicts cancer, cardiovascular disease, diabetes and mortality in the general population. J Intern Med. 2010;268(3):296–308.CrossRefPubMed Eugen-Olsen J, Andersen O, Linneberg A, Ladelund S, Hansen TW, Langkilde A, Petersen J, Pielak T, Moller LN, Jeppesen J, et al. Circulating soluble urokinase plasminogen activator receptor predicts cancer, cardiovascular disease, diabetes and mortality in the general population. J Intern Med. 2010;268(3):296–308.CrossRefPubMed
32.
go back to reference Enhorning S, Sjogren M, Hedblad B, Nilsson PM, Struck J, Melander O. Genetic vasopressin 1b receptor variance in overweight and diabetes mellitus. Eur J Endocrinol. 2016;174(1):69–75.CrossRefPubMedCentralPubMed Enhorning S, Sjogren M, Hedblad B, Nilsson PM, Struck J, Melander O. Genetic vasopressin 1b receptor variance in overweight and diabetes mellitus. Eur J Endocrinol. 2016;174(1):69–75.CrossRefPubMedCentralPubMed
33.
go back to reference Hammar N, Alfredsson L, Rosen M, Spetz CL, Kahan T, Ysberg AS. A national record linkage to study acute myocardial infarction incidence and case fatality in Sweden. Int J Epidemiol. 2001;30(Suppl 1):S30–4.CrossRefPubMed Hammar N, Alfredsson L, Rosen M, Spetz CL, Kahan T, Ysberg AS. A national record linkage to study acute myocardial infarction incidence and case fatality in Sweden. Int J Epidemiol. 2001;30(Suppl 1):S30–4.CrossRefPubMed
34.
go back to reference Delpierre C, Lauwers-Cances V, Datta GD, Lang T, Berkman L. Using self-rated health for analysing social inequalities in health: a risk for underestimating the gap between socioeconomic groups? J Epidemiol Community Health. 2009;63(6):426–32.CrossRefPubMed Delpierre C, Lauwers-Cances V, Datta GD, Lang T, Berkman L. Using self-rated health for analysing social inequalities in health: a risk for underestimating the gap between socioeconomic groups? J Epidemiol Community Health. 2009;63(6):426–32.CrossRefPubMed
35.
go back to reference Khan FA, Zia E, Janzon L, Engström G. Incidence of stroke and stroke subtypes in Malmo, Sweden, 1990–2000: marked differences between groups defined by birth country. Stroke. 2004;35(9):2054–8.CrossRefPubMed Khan FA, Zia E, Janzon L, Engström G. Incidence of stroke and stroke subtypes in Malmo, Sweden, 1990–2000: marked differences between groups defined by birth country. Stroke. 2004;35(9):2054–8.CrossRefPubMed
36.
37.
go back to reference Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC Jr, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation. 2005;112(17):2735–52.CrossRefPubMed Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC Jr, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation. 2005;112(17):2735–52.CrossRefPubMed
38.
go back to reference Nilsson PM, Engström G, Hedblad B. The metabolic syndrome and incidence of cardiovascular disease in non-diabetic subjects–a population-based study comparing three different definitions. Diabet Med. 2007;24(5):464–72.CrossRefPubMed Nilsson PM, Engström G, Hedblad B. The metabolic syndrome and incidence of cardiovascular disease in non-diabetic subjects–a population-based study comparing three different definitions. Diabet Med. 2007;24(5):464–72.CrossRefPubMed
39.
go back to reference Wlazlo N, van Greevenbroek MM, Ferreira I, Feskens EJ, van der Kallen CJ, Schalkwijk CG, Bravenboer B, Stehouwer CD. Complement factor 3 is associated with insulin resistance and with incident type 2 diabetes over a 7-year follow-up period: the CODAM Study. Diabetes Care. 2014;37(7):1900–9.CrossRefPubMed Wlazlo N, van Greevenbroek MM, Ferreira I, Feskens EJ, van der Kallen CJ, Schalkwijk CG, Bravenboer B, Stehouwer CD. Complement factor 3 is associated with insulin resistance and with incident type 2 diabetes over a 7-year follow-up period: the CODAM Study. Diabetes Care. 2014;37(7):1900–9.CrossRefPubMed
40.
go back to reference Bao X, Xia Y, Zhang Q, Wu HM, Du HM, Liu L, Wang CJ, Shi HB, Guo XY, Liu X, et al. Elevated serum complement C3 levels are related to the development of prediabetes in an adult population: the Tianjin Chronic Low-Grade Systematic Inflammation and Health Cohort Study. Diabet Med. 2016;33(4):446–53.CrossRefPubMed Bao X, Xia Y, Zhang Q, Wu HM, Du HM, Liu L, Wang CJ, Shi HB, Guo XY, Liu X, et al. Elevated serum complement C3 levels are related to the development of prediabetes in an adult population: the Tianjin Chronic Low-Grade Systematic Inflammation and Health Cohort Study. Diabet Med. 2016;33(4):446–53.CrossRefPubMed
41.
go back to reference Gao X, Liu H, Ding G, Wang Z, Fu H, Ni Z, Ma J, Liu F, Fu Z. Complement C3 deficiency prevent against the onset of streptozotocin-induced autoimmune diabetes involving expansion of regulatory T cells. Clin Immunol. 2011;140(3):236–43.CrossRefPubMed Gao X, Liu H, Ding G, Wang Z, Fu H, Ni Z, Ma J, Liu F, Fu Z. Complement C3 deficiency prevent against the onset of streptozotocin-induced autoimmune diabetes involving expansion of regulatory T cells. Clin Immunol. 2011;140(3):236–43.CrossRefPubMed
42.
go back to reference Bykov I, Jauhiainen M, Olkkonen VM, Saarikoski ST, Ehnholm C, Junnikkala S, Vakeva A, Lindros KO, Meri S. Hepatic gene expression and lipid parameters in complement C3(−/−) mice that do not develop ethanol-induced steatosis. J Hepatol. 2007;46(5):907–14.CrossRefPubMed Bykov I, Jauhiainen M, Olkkonen VM, Saarikoski ST, Ehnholm C, Junnikkala S, Vakeva A, Lindros KO, Meri S. Hepatic gene expression and lipid parameters in complement C3(−/−) mice that do not develop ethanol-induced steatosis. J Hepatol. 2007;46(5):907–14.CrossRefPubMed
43.
go back to reference Nguyen QM, Srinivasan SR, Xu JH, Chen W, Hassig S, Rice J, Berenson GS. Elevated liver function enzymes are related to the development of prediabetes and type 2 diabetes in younger adults: the Bogalusa Heart Study. Diabetes Care. 2011;34(12):2603–7.CrossRefPubMedCentralPubMed Nguyen QM, Srinivasan SR, Xu JH, Chen W, Hassig S, Rice J, Berenson GS. Elevated liver function enzymes are related to the development of prediabetes and type 2 diabetes in younger adults: the Bogalusa Heart Study. Diabetes Care. 2011;34(12):2603–7.CrossRefPubMedCentralPubMed
44.
go back to reference Mamane Y, Chung Chan C, Lavallee G, Morin N, Xu LJ, Huang J, Gordon R, Thomas W, Lamb J, Schadt EE, et al. The C3a anaphylatoxin receptor is a key mediator of insulin resistance and functions by modulating adipose tissue macrophage infiltration and activation. Diabetes. 2009;58(9):2006–17.CrossRefPubMedCentralPubMed Mamane Y, Chung Chan C, Lavallee G, Morin N, Xu LJ, Huang J, Gordon R, Thomas W, Lamb J, Schadt EE, et al. The C3a anaphylatoxin receptor is a key mediator of insulin resistance and functions by modulating adipose tissue macrophage infiltration and activation. Diabetes. 2009;58(9):2006–17.CrossRefPubMedCentralPubMed
45.
go back to reference Phieler J, Chung KJ, Chatzigeorgiou A, Klotzsche-von Ameln A, Garcia-Martin R, Sprott D, Moisidou M, Tzanavari T, Ludwig B, Baraban E, et al. The complement anaphylatoxin C5a receptor contributes to obese adipose tissue inflammation and insulin resistance. J Immunol. 2013;191(8):4367–74.CrossRefPubMed Phieler J, Chung KJ, Chatzigeorgiou A, Klotzsche-von Ameln A, Garcia-Martin R, Sprott D, Moisidou M, Tzanavari T, Ludwig B, Baraban E, et al. The complement anaphylatoxin C5a receptor contributes to obese adipose tissue inflammation and insulin resistance. J Immunol. 2013;191(8):4367–74.CrossRefPubMed
46.
go back to reference Muscari A, Bozzoli C, Puddu GM, Sangiorgi Z, Dormi A, Rovinetti C, Descovich GC, Puddu P. Association of serum C3 levels with the risk of myocardial infarction. Am J Med. 1995;98(4):357–64.CrossRefPubMed Muscari A, Bozzoli C, Puddu GM, Sangiorgi Z, Dormi A, Rovinetti C, Descovich GC, Puddu P. Association of serum C3 levels with the risk of myocardial infarction. Am J Med. 1995;98(4):357–64.CrossRefPubMed
47.
go back to reference Engström G, Hedblad B, Janzon L, Lindgarde F. Complement C3 and C4 in plasma and incidence of myocardial infarction and stroke: a population-based cohort study. Eur J Cardiovasc Prev Rehabil. 2007;14(3):392–7.CrossRefPubMed Engström G, Hedblad B, Janzon L, Lindgarde F. Complement C3 and C4 in plasma and incidence of myocardial infarction and stroke: a population-based cohort study. Eur J Cardiovasc Prev Rehabil. 2007;14(3):392–7.CrossRefPubMed
48.
go back to reference King R, Tiede C, Simmons K, Fishwick C, Tomlinson D, Ajjan R. Inhibition of complement C3 and fibrinogen interaction: a potential novel therapeutic target to reduce cardiovascular disease in diabetes. Lancet. 2015;385(Suppl 1):S57.CrossRefPubMed King R, Tiede C, Simmons K, Fishwick C, Tomlinson D, Ajjan R. Inhibition of complement C3 and fibrinogen interaction: a potential novel therapeutic target to reduce cardiovascular disease in diabetes. Lancet. 2015;385(Suppl 1):S57.CrossRefPubMed
49.
go back to reference Eriksson EE, Xie X, Werr J, Thoren P, Lindbom L. Direct viewing of atherosclerosis in vivo: plaque invasion by leukocytes is initiated by the endothelial selectins. FASEB J. 2001;15(7):1149–57.CrossRefPubMed Eriksson EE, Xie X, Werr J, Thoren P, Lindbom L. Direct viewing of atherosclerosis in vivo: plaque invasion by leukocytes is initiated by the endothelial selectins. FASEB J. 2001;15(7):1149–57.CrossRefPubMed
50.
go back to reference Naruko T, Ueda M, Haze K, van der Wal AC, van der Loos CM, Itoh A, Komatsu R, Ikura Y, Ogami M, Shimada Y, et al. Neutrophil infiltration of culprit lesions in acute coronary syndromes. Circulation. 2002;106(23):2894–900.CrossRefPubMed Naruko T, Ueda M, Haze K, van der Wal AC, van der Loos CM, Itoh A, Komatsu R, Ikura Y, Ogami M, Shimada Y, et al. Neutrophil infiltration of culprit lesions in acute coronary syndromes. Circulation. 2002;106(23):2894–900.CrossRefPubMed
51.
go back to reference Siminiak T, Flores NA, Sheridan DJ. Neutrophil interactions with endothelium and platelets: possible role in the development of cardiovascular injury. Eur Heart J. 1995;16(2):160–70.CrossRefPubMed Siminiak T, Flores NA, Sheridan DJ. Neutrophil interactions with endothelium and platelets: possible role in the development of cardiovascular injury. Eur Heart J. 1995;16(2):160–70.CrossRefPubMed
52.
go back to reference Harlan JM, Killen PD, Harker LA, Striker GE, Wright DG. Neutrophil-mediated endothelial injury in vitro mechanisms of cell detachment. J Clin Invest. 1981;68(6):1394–403.CrossRefPubMedCentralPubMed Harlan JM, Killen PD, Harker LA, Striker GE, Wright DG. Neutrophil-mediated endothelial injury in vitro mechanisms of cell detachment. J Clin Invest. 1981;68(6):1394–403.CrossRefPubMedCentralPubMed
53.
go back to reference Chatzigeorgiou A, Karalis KP, Bornstein SR, Chavakis T. Lymphocytes in obesity-related adipose tissue inflammation. Diabetologia. 2012;55(10):2583–92.CrossRefPubMed Chatzigeorgiou A, Karalis KP, Bornstein SR, Chavakis T. Lymphocytes in obesity-related adipose tissue inflammation. Diabetologia. 2012;55(10):2583–92.CrossRefPubMed
54.
55.
go back to reference Wu H, Ghosh S, Perrard XD, Feng L, Garcia GE, Perrard JL, Sweeney JF, Peterson LE, Chan L, Smith CW, et al. T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation. 2007;115(8):1029–38.CrossRefPubMed Wu H, Ghosh S, Perrard XD, Feng L, Garcia GE, Perrard JL, Sweeney JF, Peterson LE, Chan L, Smith CW, et al. T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation. 2007;115(8):1029–38.CrossRefPubMed
56.
go back to reference Afari ME, Bhat T. Neutrophil to lymphocyte ratio (NLR) and cardiovascular diseases: an update. Expert Rev Cardiovasc Ther. 2016;14(5):573–7.CrossRefPubMed Afari ME, Bhat T. Neutrophil to lymphocyte ratio (NLR) and cardiovascular diseases: an update. Expert Rev Cardiovasc Ther. 2016;14(5):573–7.CrossRefPubMed
57.
go back to reference Guo X, Zhang S, Zhang Q, Liu L, Wu H, Du H, Shi H, Wang C, Xia Y, Liu X, et al. Neutrophil:lymphocyte ratio is positively related to type 2 diabetes in a large-scale adult population: a Tianjin Chronic Low-Grade Systemic Inflammation and Health cohort study. Eur J Endocrinol. 2015;173(2):217–25.CrossRefPubMed Guo X, Zhang S, Zhang Q, Liu L, Wu H, Du H, Shi H, Wang C, Xia Y, Liu X, et al. Neutrophil:lymphocyte ratio is positively related to type 2 diabetes in a large-scale adult population: a Tianjin Chronic Low-Grade Systemic Inflammation and Health cohort study. Eur J Endocrinol. 2015;173(2):217–25.CrossRefPubMed
58.
go back to reference Ryder E, Diez-Ewald M, Mosquera J, Fernandez E, Pedreanez A, Vargas R, Pena C, Fernandez N. Association of obesity with leukocyte count in obese individuals without metabolic syndrome. Diabetes Metab Syndr. 2014;8(4):197–204.CrossRefPubMed Ryder E, Diez-Ewald M, Mosquera J, Fernandez E, Pedreanez A, Vargas R, Pena C, Fernandez N. Association of obesity with leukocyte count in obese individuals without metabolic syndrome. Diabetes Metab Syndr. 2014;8(4):197–204.CrossRefPubMed
59.
go back to reference Lee CT, Harris SB, Retnakaran R, Gerstein HC, Perkins BA, Zinman B, Hanley AJ. White blood cell subtypes, insulin resistance and beta-cell dysfunction in high-risk individuals—the PROMISE cohort. Clin Endocrinol (Oxf). 2014;81(4):536–41.CrossRef Lee CT, Harris SB, Retnakaran R, Gerstein HC, Perkins BA, Zinman B, Hanley AJ. White blood cell subtypes, insulin resistance and beta-cell dysfunction in high-risk individuals—the PROMISE cohort. Clin Endocrinol (Oxf). 2014;81(4):536–41.CrossRef
Metadata
Title
Comparing the inflammatory profiles for incidence of diabetes mellitus and cardiovascular diseases: a prospective study exploring the ‘common soil’ hypothesis
Authors
Xue Bao
Yan Borné
Linda Johnson
Iram Faqir Muhammad
Margaretha Persson
Kaijun Niu
Gunnar Engström
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2018
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-018-0733-9

Other articles of this Issue 1/2018

Cardiovascular Diabetology 1/2018 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.