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Original Article
ABSTRACT
Background/Aim: Metabolic syndrome (MetS) is a clinical condition characterized by central obesity,
elevated triglycerides, lowhigh 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 Crohns 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.
Key Words: Inflammatory bowel disease, insulin resistance, metabolic syndrome, obesity
Received 06.02.2011, Accepted 23.06.2011
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.
Website: www.saudijgastro.com
Patient population
DOI: 10.4103/1319-3767.87177
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Metabolic syndrome in IBD
Diagnosis of MetS
Biochemical measurements
Statistical 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.
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).
50
0
1
2
3
4
5
40
30
20
10
0
UC
Crohn
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Yorulmaz, et al.
Ulcerative colitis
115
49/66
43.93 13.59
50.18 55.59
22 (19.1%)
16 (13.9%)
26.27 4.89
97.37 12.55
97.53 12.69
122.43 19.58
78.39 11.93
98.95 32
121.26 57.29
61.92 12.84
48.53 14.48
8.81 5.30
2.20 1.57
Crohns disease
62
28/34
36.74 13.88
47.71 70.16
29 (46.8%)
12 (19.4%)
23.67 5.18
89.82 15.97
90.47 10.74
111.13 20.96
71.45 12.78
91.87 17.04
121.15 63.47
56.04 15.56
51.12 14.93
7.34 5.39
1.69 1.27
P values
>0.05
>0.05
>0.05
<0.001
>0.05
< 0.01
<0.05
<0.01
<0.001
<0.001
>0.05
>0.05
>0.05
>0.05
>0.05
<0.05
BMI: Body mass index, SBP: Systolic blood pressure, DBP: Diastolic blood pressure, FPG: fasting plasma glucose, HOMA-IR: Homeostasis model assessment of
insulin resistance
0
29%
(n=18)
7.8%
(n=9)
n
%
n
%
Metabolic syndrome
Absent
Present
105
12
89.7
10.3
27
33
45
55
41.87
0.0001
MetS was detected in 10.3% of patients under 45 years of age and in 55% of
patients over 45 years of age (P<0.001).
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DISCUSSION
MetS is a major worldwide health problem and is a risk
factor for CVD and T2DM.[23] 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.[24,25]
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.[26,27]
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%.[26,28] 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.[29]
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.[25]
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Metabolic syndrome in IBD
IR+UC
31
12/19
48.32 13.01
52.97 51.28
29.85 5.75
105.75 10.217
104.74 15.369
128.06 23.72
80.97 14.45
114.74 57.07
140.94 69.62
59.83 14.295
45.00 13.760
15.38 5.27
5.06 1.36
IR-UC
P values
84
37/47
>0.05
42.31 13.51
<0.05
49.15 57.35
>0.05
24.95 3.79
94.65 12.136
94.62 10.254
120.36 17.52
77.44 10.79
93.12 10.07
114.00 50.58
62.59 12.473
49.96 14.675
6.39 2.55
4.47 1.43
<0.001
<0.01
<0.01
>0.05
>0.05
<0.01
<0.05
>0.05
>0.05
<0.001
<0.05
BMI: Body mass index, SBP: Systolic blood pressure, DBP: Diastolic blood
pressure, FPG: fasting plasma glucose, HDL-C: High density lipoprotein
cholesterol, WC: Waist circumference
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Yorulmaz, et al.
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 Crohns and Colitis Organization.
REFERENCES
1.
2.
3.
4.
5.
6.
7.
8.
9.
CONCLUSIONS
10.
11.
380
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Dhul Hijjah 1432H
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12.
13.
[Downloadedfreefromhttp://www.saudijgastro.comonMonday,September10,2012,IP:118.96.168.103]||ClickheretodownloadfreeAndroidapplicationforthis
journal
Metabolic syndrome in IBD
14. Blain A, Cattan S, Beaugerie L, Carbonnel F, Gendre JP, Cosnes J.
Crohns 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 Crohns 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 Crohns 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 Crohns 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 Crohns
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 and
nternational 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. izmeciolu FM, Hatun , Kalaa 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, Tarjn 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, Schlmerich J, Andus T,
Bollheimer LC. Increased insulin resistance and beta cell activity in
patients with Crohns disease. Inflamm Bowel Dis 2006;12:53-6.
36. Hu G, Qiao Q, Tuomilehto J, Eliasson M, Feskens EJ, Pyrl 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, Trifir 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 Crohns 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, DAgostino 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. Frhlich 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, dAgostino 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.
381
Volume 17, Number 6
Dhul Hijjah 1432H
November 2011
[Downloadedfreefromhttp://www.saudijgastro.comonMonday,September10,2012,IP:118.96.168.103]||ClickheretodownloadfreeAndroidapplicationforthis
journal
Yorulmaz, et al.
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.
382
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