|Year : 2011 | Volume
| Issue : 6 | Page : 376-382
|Metabolic syndrome frequency in inflammatory bowel diseases
Elif Yorulmaz1, Gupse Adali1, Hatice Yorulmaz2, Celal Ulasoglu1, Guralp Tasan1, Ilyas Tuncer1
1 Department of Gastroenterology, Goztepe, Training and Research Hospital, Istanbul, Turkey
2 Department of Nursing, Halic University School of Nursing, Istanbul, Turkey
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|Date of Submission||06-Feb-2011|
|Date of Acceptance||23-Jun-2011|
|Date of Web Publication||5-Nov-2011|
| Abstract|| |
Background/Aim: Metabolic syndrome (MetS) is a clinical condition characterized by central obesity, elevated triglycerides, low-high density lipoproteins, impaired fasting glucose, and hypertension. There is insufficient data on the prevalence of MetS in patients with inflammatory bowel disease (IBD). This study sought to determine the prevalence of MetS in a Turkish cohort of patients with IBD and the association between insulin resistance (IR) and the MetS parameters, in this population. Patients and Methods: A total of 177 patients over 18 years of age (62 with Crohn's disease (CD) and 115 with ulcerative colitis (UC)) were enrolled in the study. The presence of at least three criteria of the International Diabetes Federation (IDF) was accepted for the diagnosis of MetS. The Homeostasis Model Assessment (HOMA) was used to determine IR. HOMA values < 1 were considered normal and values > 2.5 indicated a high probability of IR. Results: MetS frequency was higher in patients n=34 (29.5%) with UC than in patients n=11 (17.7%) with CD (P < 0.01). MetS was detected in 12 of the 117 patients (10.3%) with IBD, under 45 years of age, and in 33 of 60 patients (55%) over 45 years of age. HOMA value in n=31 patients (27%) with UC was > 2.5. Body mass index, insulin (P < 0.001), waist circumference, fasting plasma glucose, leukocyte count (P < 0.01), triglycerides, C-reactive protein, and uric acid values (P < 0.05) were significantly higher in UC patients with IR than those without IR. Conclusion: Frequent occurrence of MS with increasing age in IBD, particularly in UC, showed the importance of early diagnosis and treatment of cardiovascular disease risk factors in the long-term follow-up of these diseases.
Keywords: Inflammatory bowel disease, insulin resistance, metabolic syndrome, obesity
|How to cite this article:|
Yorulmaz E, Adali G, Yorulmaz H, Ulasoglu C, Tasan G, Tuncer I. Metabolic syndrome frequency in inflammatory bowel diseases. Saudi J Gastroenterol 2011;17:376-82
|How to cite this URL:|
Yorulmaz E, Adali G, Yorulmaz H, Ulasoglu C, Tasan G, Tuncer I. Metabolic syndrome frequency in inflammatory bowel diseases. Saudi J Gastroenterol [serial online] 2011 [cited 2019 Nov 17];17:376-82. Available from: http://www.saudijgastro.com/text.asp?2011/17/6/376/87177
Metabolic syndrome (MetS) is defined as abdominal obesity, elevated blood pressure, glucose intolerance, and atherogenic dyslipidemia. Recognition of this syndrome is important in that it represents a prothrombotic and proinflammatory process.  inflammatory bowel disease (IBD) is comprised of two major disorders, ulcerative colitis (UC) and Crohn's disease (CD). These disorders have distinct pathological and clinical characteristics. The pathogenesis of these diseases remains poorly understood.  Type 2 diabetes mellitus (T2DM) and cardiovascular disease (CVD) may affect the disease course and prognosis in patients with IBD. Increased mortality has not been observed in the population-based studies. [3-8] Bernstein et al.,  reported an increased risk of cardiac artheroembolic disease in IBD. Obesity is known to increase the risk of developing colorectal cancer, , a serious concern for IBD patients with longstanding disease, who are already at risk for developing colorectal cancer. , Obesity may also influence disease activity in IBD patients. , Recent evidence suggests that in CD, hypertrophied mesenteric adipose tissue contributes to increased disease activity and development of complications. ,,, In this study we sought to determine the prevalence of MetS in patients with IBD, as well as the association between IR and the MetS parameters in this population.
| Patients and Methods|| |
A total of 177 patients, followed due to IBD diagnosis, aged 18 years and older (62 with CD, 28 women and 34 men, 36.7 ± 13.8 years of age; 115 with UC, 49 women and 66 men, 43.9 ± 13.5 years of age) were enrolled in the study. The study protocol was approved by the Local Ethics Committee (approval date and number: 02-06-2009, No: 57). The patients with known malignancy, thyroid disease, those receiving hormone replacement therapy, corticosteroids in the past six months, pregnant, with abdominal mass, ascites, chronic obstructive pulmonary disease (COPD), liver cirrhosis, Stage 3 - 4 cardiac failure or chronic renal failure were excluded.
Diagnosis of MetS
Patients with MetS, have been defined by the International Diabetes Federation (IDF) criteria. These criteria were based on the presence of central obesity (waist circumference ≥ 94 cm for men and ≥ 80 cm for women) and two or more of the following; blood pressure ≥130 / 85 mmHg (or treatment of previously diagnosed hypertension), fasting plasma glucose (FPG) ≥100 mg / dl (or previously diagnosed T2DM), raised triglycerides level ≥150 mg / dl (or specific treatment for this lipid abnormality), and reduced high density lipoprotein cholesterol (HDL-C) cholesterol < 40 mg / dl in males and <50 mg / dl in females (or specific treatment for this lipid abnormality). 
Sitting blood pressure measurements were performed with conventional mercury sphygmomanometers in both arms after at least 10 minutes of rest, using the Korotkoff Phase I and Phase V sounds. A second measurement was performed in the arm with a higher reading. The average systolic and diastolic blood pressure (SBP and DBP) measurements were calculated with the measurements at least three minutes apart. Waist circumference was measured at the smallest circumference between the rib cage and anterior superior iliac spine iliac crest, with the subject in the standing position and during slight expiration. Body mass index (BMI) was calculated using the Quetlet index (weight / height 2, kg/m 2 ). 
The venous blood samples, taken after 12 hours of overnight fasting, were centrifuged (2500 rpm) and the sera were separated. Glucose, uric acid, total cholesterol (total-C), HDL-C, low-density lipoprotein cholesterol (LDL-C), and triglycerides were measured with enzymatic methods. Insulin was measured using an electrochemiluminescence immunoassay (ECLIA) (Roche E170). Insulin sensitivity was determined by Homeostasis Model Assessment (HOMA-IR). 
HOMA values < 1 were considered normal and values > 2.5 indicated a high probability of IR.
Data were evaluated by the SPSS 15.0 statistical analysis software using Chi square, t-test, one way analysis of variance, Tukey test, and the Pearson correlation analysis.
| Results|| |
One-hundred seventy seven patients with IBD were enrolled in this study, 115 (65%) with UC, and 62 (35%) with CD. The mean age of the patients with UC was 43.93 ± 13.59 years and the mean age of the patients with CD was 36.74 ± 13.88 years; 42.6% of the UC patients (n=49) were female (mean age 40.56 ± 12.79), 57.4% of the UC patients (n=66) were male (mean age 46.32 ± 14.39), 45.2% of the CD patients (n=28) were female (mean age 40.29 ± 14.55), and 54.8% of the CD patients (n=34) were male (mean age 33.82 ± 12.79). No significant difference was found between the duration of IBD, gender, and frequency of MetS (P > 0.05). Details of patient characteristics are shown in [Table 1]. MetS frequency was significantly higher in UC patients n=34 (29.5%) compared to CD patients n= 11 (17.7%) (P < 0.01). Comparison of patients in terms of the MetS criteria count is depicted in [Table 2] and [Figure 1].
|Table 1: Demographic, clinical and laboratory characteristics of patients with IBD|
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|Table 2: Statistical difference between groups in terms of MetS criteria count|
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|Figure 1: Comparison of patients with UC and CD in terms of the MetS criteria count|
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MetS was confirmed in 12 of the 117 (10.3%) IBD patients, under 45 years of age, and in 33 of the 60 (55%) patients over 45 years of age (P < 0.001) [Table 3]. Cigarette smoking was significantly higher in CD patients compared to UC patients (P < 0.001). However, among the groups there was no difference in terms of alcohol usage.
Waist circumference values of UC patients were significantly higher, both in male (P < 0.01) and female patients (P < 0.05), than in the CD patients. In the UC patients, SBP and DBP (P < 0.001), BMI, total-C, LDL-C levels (P < 0.01), and HOMA levels (P < 0.05) were significantly higher than in CD patients. There was a positive correlation between BMI and waist circumference in male patients with UC and MetS criteria 3 and above (n=22) (P < 0.01), and in female patients (n=12) (P < 0.05).
The Homeostasis Model Assessment (HOMA) value was ≥ 2.5 in n= 31 of the UC patients (27%) and in 16.1% of the CD patients (n=10). 24.5% (n=12) of the female and 28.8% (n=19) of the male UC patients had IR. 21.4% (n=6) of the female and 11.8% (n=4) of the male CD patients had IR. UC patients with IR had significantly higher BMI, insulin (P < 0.001), FPG, leukocyte count, waist circumference (P < 0.01), triglycerides, C-reactive protein (CRP), and uric acid levels compared to patients without IR (P < 0.05). Comparison of UC patients with IR and without IR is shown in [Table 4].
C-reactive protein and leukocyte counts of patients were significantly high in CD patients (P < 0.01). In CD patients, BMI, FPG, leukocyte count (P < 0.05), and insulin values (P< 0.001) were higher in patients with ≥ 2.5 HOMA value. HDL-C values of female CD patients without IR were significantly higher than female patients with IR (P < 0.05).
| Discussion|| |
MetS is a major worldwide health problem and is a risk factor for CVD and T2DM.  MetS increases the risk of cardiovascular morbidity thrice, morbidity three times, mortality two times and T2DM five times. The reason for the increased incidence and prevalence of MetS in children can be attributed to the obesity epidemic in this population. ,
MetS prevalence increases with abdominal obesity and is approximately 27% in the United States, 13% in France, 31 - 40% in Pakistan, 33 - 29% in Turkey, and 40% in India. ,
Similar to many western populations, abdominal obesity and MetS prevalence are increasing in Turkey as well. In Turkey, MetS prevalence was 33.0% and 38.8%. , In a study carried out by the Metabolic Syndrome Association (METSAR), MetS prevalence was found to be 33.9% and it was 40% in women and 28% in men. Prevalence was 6.7% in the age group of 20 - 29 years and 43.5% in the age group of 60 - 69 years. MetS was 53% in coronary heart patients.  Even as prevalence increases with age and BMI, it decreases with increasing educational level and physical activity. It is also more frequently found in women. 
There is a lack of data on the prevalence of MetS in patients with IBD. In a study reported in Japan, there was no difference in the prevalence in MetS in IBD patients compared to the general population over the age of 40 years.  This study found that MetS was more common in IBD patients with advancing age.
Higher MetS frequency in IBD patients, over 45 years of age, enrolled in the study could be explained by the addition of a long-term inflammatory effect to the current risk factors.
The etiology of IBD is unknown, but the condition seems to be the result of a combination of environmental, genetic, and immunological factors, where an uncontrolled immune response within the intestine leads to inflammation in genetically predisposed individuals.  Dysfunctions of the intestinal immune system and cross-reactivity against host epithelial cells have been implicated as major mechanisms by which inflammation occurs. 
Early atherosclerosis is a clinical feature common to several inflammatory and immunological diseases, in which atherothrombotic complications represent one of the most important causes of mortality and morbidity.  Parameters such as inflammation, and IR, which are considered clinical markers of early atherosclerosis, are accepted as predictors of cardiovascular events. ,
A number of prospective studies indicate that those with CVD and impaired glucose metabolism have a significantly greater cardiovascular morbidity and mortality compared to those with normal glucose metabolism.  IR and hyperinsulinemia are considered the primary events that lead to atherosclerosis.  The role of insulin in the development of atherosclerosis could be direct - through the stimulation of vascular smooth muscle cell proliferation and arterial wall lipid deposition, or indirect - through promoting the development of hypertension and dyslipidemia. , Bregenzer et al. reported an increase in IR in CD.  Capristo et al. , however, found that glucose uptake in IBD was similar to that in the control group.  In our study, the HOMA value above or equal to 2.5 was found in 27% and 16.1% of UC and CD, respectively. The UC patients with IR had significantly higher BMI, insulin, FPG, leukocyte count, TG, CRP, uric acid levels, and WC values compared to patients without IR. BMI, FPG, leukocyte count, and insulin levels of the CD patients were high in those with HOMA values ≥ 2.5. HDL levels of female CD patients without IR were significantly higher compared to female CD patients with IR.
Often referred to as central or abdominal obesity, periomental or visceral excess fat is a component of MetS and is associated with the increase of CVD risk. Central obesity hyperinsulinemia is associated with clinical conditions such as IR, diabetic dyslipidemia, hypertension, albuminuria, and proinflammatory-prothrombotic proinflammatory and prothrombotic. , In a study where obese young women were enrolled, there was a correlation between waist circumference and both plasma insulin and IR.  Lifestyle changes to prevent CVD were expected to reduce not only the risk of CVD, but also the risk of dysplasia and colorectal cancer development in IBD patients. ,,, Furthermore, a case report suggested that reducing body weight might also contribute to decreasing disease activity in UC.  Holtmann et al.,  recently showed improved outcomes in UC patients treated with azathioprine, with a lower BMI maintained under,  suggesting the benefit of body weight control in IBD patients. In our study, a positive correlation between BMI and waist circumference was established in male and female UC patients, with MetS criteria count ≥3. The BMI of UC and CD patients with IR was significantly higher compared to patients without IR. Furthermore, the waist circumference values of female and male UC patients with IR were significantly high compared to the female and male UC patients without IR.
Chronic inflammation is related to both MetS and future CVD. In recent years, markers of systemic inflammation and certain components of the hemostatic system have been found to predict atherosclerotic risk. CRP was found to be independently associated with body weight, IR, and SBP. White blood cell count and fibrinogen were associated with obesity and IR. 
C-Reactive protein is an inflammatory marker and is produced in the liver by the stimulation of cytokines generated at IL-1, IL-6, and TNF-alpha. The association between MetS and CRP is related to the release of cytokines through the adipose tissue. IR can cause elevated levels of CRP release and this effect is similar to the effect of insulin on the hepatic acute phase protein synthesis.  Festa et al. revealed that chronic subclinical inflammation is a part of the IR syndrome.  Fröhlich et al. determined high levels of CRP and IL-6 in patients with MetS. 
The strong association between CRP levels and IR determined by the HOMA-IR formulation was revealed in a study evaluating the relationship between CRP level as an inflammatory marker and other CVD risk factors, which comprised of 1025 subjects aged between 35 and 60 years, without any known health condition.  Chronic activation of the innate immune system may also underlie the formation of MetS, and chronic inflammation can explain the formation of T2 DM and CVD as well.  The serum CRP level correlates with the BMI and the waist-to-hip ratio in both non-diabetes and patients with T2 DM  In our study, the CRP and leukocyte levels of UC patients with IR were significantly higher than those in patients without IR. In patients with CD, the leukocyte count was higher in those with HOMA value > 2.5. There was no difference between the BMI and waist circumference or CRP and leukocyte values in male and female patients with UC.
It is known that there is a relationship among elevated serum uric acid levels, CVD, hypertension, MetS, coronary artery disease, cerebrovascular disease, vascular dementia, pre-eclampsia, and kidney disease.  In subjects with high MetS risk, uric acid is thought to be the determinative variable for the development of T2DM.  In the eight-year prospective study by Kekalainen et al.,  it was found that while dyslipidemia, HT, and uric acid levels were associated with IR; hypertension and very-low-density lipoprotein cholesterol were associated with impaired first phase insulin secretion. In IR patients, plasma uric acid concentrations were higher due to the decrease of uric acid renal clearance. Nonetheless, the plasma uric acid level was not a very sensitive indicator of IR. Normal uric acid levels did not necessarily mean insulin sensitivity.  In our study, the uric acid levels of UC patients with IR were significantly higher than those without IR.
| Conclusions|| |
MetS is a preventable, but poorly recognized chronic inflammatory disease with high prevalence and usually treated inadequately. Insulin resistance is an important parameter in the relationship between MetS and CVD. Although, due to insufficient comparable worldwide data, this study may conclude the importance of MetS and IR in IBD patients. In terms of prevention of cardiovascular morbidity and mortality and avoiding colorectal cancer, strategies toward preventable risk factors that will increase insulin sensitivity, such as, weight control, normalizing lipid levels, and blood pressure, seem to be important issues in IBD treatment.
| Acknowledgments|| |
Prior to investigation, all patients and their families had been given verbal explanations and had signed informed consent forms meeting all institutional and ethic guidelines, explicitly detailing the method and goal of the study. Financial support was obtained from the research fund of our hospital. All authors had full access to the data and had the final responsibility of taking the decision to submit the manuscript. The preliminary results of this study have been accepted as an abstract by the ECCO Congress (Dublin 2011) of European Crohn's and Colitis Organization.
| References|| |
|1.||Grundy SM. Metabolic syndrome: Connecting and reconciling cardiovascular and diabetes worlds. J Am Coll Cardiol 2006;47:1093-100. |
|2.||Sartor RB. Mechanisms of disease: Pathogenesis of Crohn's disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 2006;3:390-407. |
|3.||Winther KV, Jess T, Langholz E, Munkholm P, Binder V. Survival and cause-specific mortality in ulcerative colitis: Follow-up of a population-based cohort in Copenhagen County. Gastroenterology 2003;125:1576-82. |
|4.||Jess T, Gamborg M, Munkholm P, Sorensen TI. Overall and causespecific mortality in ulcerative colitis: Meta-analysis of population-based inception cohort studies. Am J Gastroenterol 2007;102:609-17. |
|5.||Hoie O, Schouten LJ, Wolters FL, Solberg IC, Riis L, Mouzas IA, et al. Ulcerative colitis: no rise in mortality in a European-wide population based cohort 10 years after diagnosis. Gut 2007;56:497-503. |
|6.||Jess T, Winther KV, Munkholm P, Langholz E, Binder V. Mortality and causes of death in Crohn's disease: follow-up of a population-based cohort in Copenhagen County, Denmark. Gastroenterology 2002;122:1808-14. |
|7.||Wolters FL, Russel MG, Sijbrandij J, Schouten LJ, Odes S, Riis L, et al. Disease outcome of inflammatory bowel disease patients: General outline of a Europewide population-based 10-year clinical follow-up study. Scand J Gastroenterol Suppl 2006;243:46-54. |
|8.||Wolters FL, Russel MG, Sijbrandij J, Schouten LJ, Odes S, Riis L, et al. Crohn's disease: Increased mortality 10 years after diagnosis in a Europe-wide population based cohort. Gut 2006;55:510-8. |
|9.||Bernstein CN, Wajda A, Blanchard JF. The incidence of arterial thromboembolic diseases in inflammatory bowel disease: A population-based study. Clin Gastroenterol Hepatol 2008;6:41-5. |
|10.||Giovannucci E, Ascherio A, Rimm EB, Colditz GA, Stampfer MJ, Willett WC. Physical activity, obesity, and risk for colon cancer and adenoma in men. Ann Intern Med 1995;122:327-34. |
|11.||Martinez ME, Giovannucci E, Spiegelman D, Hunter DJ, Willett WC, Colditz GA. Leisure-time physical activity, body size, and colon cancer in women. Nurses' Health Study Research Group. J Natl Cancer Inst 1997;89:948-55. |
|12.||Gillen CD, Walmsley RS, Prior P, Andrews HA, Allan RN. Ulcerative colitis and Crohn's disease: A comparison of the colorectal cancer risk in extensive colitis. Gut 1994;35:1590-2. |
|13.||Ekbom A, Helmick C, Zack M, Adami HO. Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med 1990;323:1228-33. |
|14.||Blain A, Cattan S, Beaugerie L, Carbonnel F, Gendre JP, Cosnes J. Crohn's disease clinical course and severity in obese patients. Clin Nutr 2002;21:51-7. |
|15.||Hass DJ, Brensinger CM, Lewis JD, Lichtenstein GR. The impact of increased body mass index on the clinical course of Crohn's disease. Clin Gastroenterol Hepatol 2006;4:482-8. |
|16.||Peyrin-Biroulet L, Chamaillard M, Gonzalez F, Beclin E, Decourcelle C, Antunes L, et al. Mesenteric fat in Crohn's disease: A pathogenetic hallmark or an innocent bystander? Gut 2007;56:577-83. |
|17.||Karmiris K, Koutroubakis IE, Kouroumalis EA. The emerging role of adipocytokines as inflammatory mediators in inflammatory bowel disease. Inflamm Bowel Dis 2005;11:847-55. |
|18.||Yamamoto K, Kiyohara T, Murayama Y, Kihara S, Okamoto Y, Funahashi T, et al. Production of adiponectin, an anti-inflammatory protein, in mesenteric adipose tissue in Crohn's disease. Gut 2005;54:789-96. |
|19.||Desreumaux P, Ernst O, Geboes K, Gambiez L, Berrebi D, Muller-Alouf H, et al. Inflammatory alterations in mesenteric adipose tissue in Crohn's disease. Gastroenterology 1999;117:73-81. |
|20.||Alberti KG, Zimmet P, Shaw J. IDF Epidemiology Task Force Consensus Group. The metabolic syndrome - a new worldwide definition. Lancet 2005;366:1059-62. |
|21.||Maggio CA, Pi-Sunyer FX. The prevention and treatment of obesity. Application to type 2 diabetes. Diabetes Care 1997;20:1744-66. |
|22.||Haffner SM, Kennedy E, Gonzalez C, Stern MP, Miettinen H. A prospective analysis of the HOMA model. The Mexico City Diabetes Study. Diabetes Care 1996;19:1138-41. |
|23.||Ekelund U, Anderssen S, Andersen LB, Riddoch CJ, Sardinha LB, Luan J, et al. Prevalence and correlates of the metabolic syndrome in a population-based sample of European youth. Am J Clin Nutr 2009;89:90-6. |
|24.||Misra A, Khurana L The Metabolic Syndrome in South Asians: Epidemiology, Determinants, and Prevention. Meta Syndr Relat Disord 2009;7:497-514. |
|25.||Bener A, Zirie M, Musallam M, Khader YS, Al-Hamaq AO. Prevalence of metabolic syndrome according to adult treatment panel ýýý and ýnternational diabetes federation criteria: A population-based study. Metab Syndr Relat Disord 2009;7:221-9. |
|26.||Martinez MA, Puig JG, Mora M. Metabolic syndrome: Prevalence, associated factors, and C-reactive protein. Metab Clin Exp 2008;57:1232-40. |
|27.||Hydrie MZ, Shera AS, Fawwad A, Basit A, Hussain A. Prevalence of metabolic syndrome in urban Pakistan (Karachi): Comparison of newly proposed international diabetes federation and modified adult treatment panel III criteria. Metab Syndr Relat Disord 2009;7:119-24. |
|28.||Çizmecioðlu FM, Hatun ª, Kalaça S. Metabolic syndrome in obese Turkish children and adolescents: comparison of two diagnostic models. Tur J Pediatr 2008;50:359-65. |
|29.||Kozan O, Oguz A, Abaci A, Erol C, Ongen Z, Temizhan A, et al. Prevalence of the metabolic syndrome among Turkish adults. Eur J Clin Nutr 2007;61:548-53. |
|30.||Nagahori M, Hyun SB, Totsuka T, Okamoto R, Kuwahara E, Takebayashi T, et al. Prevalence of metabolic syndrome is comparable between inflammatory bowel disease patients and the general population. J Gastroenterol 2010;45:1008-13. |
|31.||Karlinger K, Gyorke T, Mako E, Mester A, Tarján Z. The epidemiology and the pathogenesis of inflammatory bowel disease. Eur J Radiol 2000;35:154-67. |
|32.||Yu Y, Sitaraman S, Gewirtz AT. Intestinal epithelial cell regulation of mucosal inflammation. Immunol Res 2004;29:55-68. |
|33.||Van Doornum S, McColl G, Wicks IP. Accelerated atherosclerosis. An extraarticular feature of rheumatoid arthritis? Arthritis Rheum 2002;46:862-73. |
|34.||Danesh J, Wheeler JG, Hirschfield GM, Eda S, Eiriksdottir G, Rumley A, et al. C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease. N Engl J Med 2004;350:1387-97. |
|35.||Bregenzer N, Hartmann A, Strauch U, Schölmerich J, Andus T, Bollheimer LC. Increased insulin resistance and beta cell activity in patients with Crohn's disease. Inflamm Bowel Dis 2006;12:53-6. |
|36.||Hu G, Qiao Q, Tuomilehto J, Eliasson M, Feskens EJ, Pyörälä K, et al. Plasma insulin and cardiovascularmortality in non-diabetic Europeanmen and women: A meta-analysis of data from eleven prospective studies. Diabetologia 2004;47:1245-56. |
|37.||Enas A, Garg A, Davidson MA, Nair VM, Huet BA, Yusuf S. Coronary heart disease and its risk factors in first generation immigrant Asian Indians to the United State of America. Indian Heart J 1996;48:343-53. |
|38.||Rantala AO, Paivansalo M, Kauma H, Lilja M, Savolainen MJ, Reunanen A, et al. Hyperinsulinemia and carotid atherosclerosis in hypertensive and control subjects. Diabetes Care 1998;21:1188-93. |
|39.||Frayn KN. Insulin resistance and lipid metabolism. Curr Opin Lipidol 1993;4:197-204. |
|40.||Capristo E, Mingrone G, Addolorato G, Greco AV, Gasbarrini G. Glucose metabolism and insulin sensitivity in inactive inflammatory bowel disease. Aliment Pharmacol Ther 1999;13:209-17. |
|41.||Lakka HM, Lakka TA, Tuomiletho J, Salonen JT. Abdominal obesity is associated with increased risk of acute coronary events in men. Eur Heart J 2002;23:706-13. |
|42.||McFarlane SI, Banerji M, Sowers JR. Insulin resistance and cardiovascular disease. J Clin Endocrinol Metab 2001;85:713-8. |
|43.||Maffeis C, Corciulo N, Livieri C, Rabbone I, Trifirò G, Falorni A, et al. Waist circumference as a predictor of cardiovascular and metabolic risk factors in obese girls. Eur J Clin Nutr 2003;57:566-72. |
|44.||Wolin KY, Yan Y, Colditz GA, Lee IM. Physical activity and colon cancer prevention: A meta-analysis. Br J Cancer 2009;100:611-6. |
|45.||Botteri E, Iodice S, Bagnardi V, Raimondi S, Lowenfels AB, Maisonneuve P. Smoking and colorectal cancer: A meta-analysis. JAMA 2008;300:2765-78. |
|46.||Lascano CA, Soto F, Carrodeguas L, Szomstein S, Rosenthal RJ, Wexner SD. Management of ulcerative colitis in the morbidly obese patient: Is bariatric surgery indicated? Obes Surg 2006;16:783-6. |
|47.||Holtmann MH, Krummenauer F, Claas C, Kremeyer K, Lorenz D, Rainer O, et al. Significant differences between Crohn's disease and ulcerative colitis regarding the impact of body mass index and initial disease activity on responsiveness to azathioprine: results from a European multicenter study in 1,176 patients. Dig Dis Sci 2010;55:1066-78. |
|48.||Miranda PJ, DeFronzo RA, Califf RM, Guyton JR. Metabolic syndrome: Definition, pathophysiology, and mechanisms. Am Heart J 2005;149:33-45. |
|49.||Isomaa B. A major health hazard: The metabolic syndrome. Life Sci 2003;73:2395-411. |
|50.||Festa A, D'Agostino R Jr, Howard G, Mykkanen L, Tracy RP, Haffner SM. Chronic subclinical inflammation as part of the insulin resistance syndrome: The Insulin Resistance Atherosclerosis Study (IRAS). Circulation 2000;102:42-7. |
|51.||Fröhlich M, Imhof A, Berg G, Hutchinson WL, Pepys MB, Boeing H, et al. Association between C-reactive protein and features of the metabolic syndrome: A population-based study. Diabetes Care 2000;23:1835-9. |
|52.||Chambers JC, Eda S, Bassett P, Karim Y, Thompson SG, Gallimore JR, et al. C-reactive protein, insulin resistance, central obesity and coronary heart disease risk in Indian Asians from the United Kingdom compared with European whites. Circulation 2001;104:145-50. |
|53.||Festa A, d'Agostino R Jr, Williams K, Karter AJ, Mayer-Davis EJ, Tracy RP, et al. The relation of body fat mass and distribution to markers of chronic inflamation. Int J Obes Relat Metab Disord 2001;25:1407-15. |
|54.||Feig DI, Kang DH, Johnson RJ. Uric acid and cardiovascular risk. N Engl J Med 2008;359:1811-21. |
|55.||Chou P, Li CL, Wu GS, Tsai ST. Progression to type 2 diabetes among high risk groups in Kin-Chen, Kinmen. Diabetes Care 1998;21:1183-7. |
|56.||Kekalainen P, Sarlund H, Laakso M Long-term association of cardiovascular risk factors with impaired insulin secretion and insulin resistance. Metabolism 2000;49:1247-54. |
|57.||Facchini F, Chen YD, Hollenbeck CB, Reaven GM. Relationship between resistance to insulin-mediated glucose uptake, urinary uric acid clearance, and plasma uric acid concentration. JAMA 1991;266:3008-11. |
Department of Gastroenterology, Goztepe, Training and Research Hospital, Goztepe, Istanbul
Source of Support: None, Conflict of Interest: None
[Table 1], [Table 2], [Table 3], [Table 4]
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| ||Peluso, R. and Di Minno, M.N.D. and Iervolino, S. and Manguso, F. and Tramontano, G. and Ambrosino, P. and Esposito, C. and Scalera, A. and Castiglione, F. and Scarpa, R. |
| ||Clinical and Developmental Immunology. 2013; 2013(631408) |
||Epidemiology and disease burden of ulcerative colitis in Taiwan: A nationwide population-based study
| ||Chen, C.-Y. and Lee, K.-T. and Charles Tzu-Chi, L. and Lai, W.-T. and Huang, Y.-B. |
| ||Value in Health Regional Issues. 2013; 2(1): 127-134 |
||Primary care considerations in the management of Inflammatory Bowel Disease patients
| ||Manten, E. and Green, J.A. and Bartholomew, C. |
| ||Practical Gastroenterology. 2012; 36(4): 48-54 |