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Erschienen in: Diabetologia 7/2010

01.07.2010 | Article

Non-alcoholic fatty liver disease is independently associated with an increased prevalence of chronic kidney disease and retinopathy in type 1 diabetic patients

verfasst von: G. Targher, L. Bertolini, M. Chonchol, S. Rodella, G. Zoppini, G. Lippi, L. Zenari, E. Bonora

Erschienen in: Diabetologia | Ausgabe 7/2010

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Abstract

Aims/hypothesis

Non-alcoholic fatty liver disease (NAFLD) is associated with an increased prevalence of chronic kidney disease (CKD) and retinopathy in patients with type 2 diabetes. Information on this issue is lacking for type 1 diabetes. We evaluated whether NAFLD is associated with increased prevalence of retinopathy and CKD in type 1 diabetic patients.

Methods

All type 1 diabetic patients (n = 202) who regularly attended our diabetes clinic and did not have any clinical evidence of cirrhosis or other secondary causes of chronic liver disease were studied. Main study measures were detection of NAFLD (by patient history and liver ultrasound), diabetic retinopathy (diagnosed by ophthalmoscopy) and CKD (defined as abnormal albuminuria or estimated GFR of ≤60 ml min−1 1.73 m−2).

Results

The age- and sex-adjusted prevalence of diabetic retinopathy (53.2 vs 19.8%) and CKD (37.8 vs 9.9%) was markedly higher in patients with NAFLD than in those without (p < 0.0001). In multivariate logistic regression analysis, NAFLD was associated with prevalent retinopathy (adjusted OR 3.31, 95% CI 1.4–7.6, p = 0.005) or CKD (adjusted OR 3.90, 95% CI 1.5–10.1, p = 0.005). These associations were independent of age, sex, diabetes duration, HbA1c, medication use and presence of the metabolic syndrome.

Conclusions/interpretation

Our findings suggest that ultrasound-diagnosed NAFLD is associated, independently of several confounding factors, with a higher prevalence of CKD and retinopathy in type 1 diabetic individuals.
Literatur
1.
2.
Zurück zum Zitat de Alwis NMW, Day CP (2008) Nonalcoholic fatty liver disease: the mist gradually clears. J Hepatol 48(Suppl 1):S104–S112PubMed de Alwis NMW, Day CP (2008) Nonalcoholic fatty liver disease: the mist gradually clears. J Hepatol 48(Suppl 1):S104–S112PubMed
3.
Zurück zum Zitat Kotronen A, Yki-Järvinen H (2008) Fatty liver: a novel component of the metabolic syndrome. Arterioscler Thromb Vasc Biol 28:27–38CrossRefPubMed Kotronen A, Yki-Järvinen H (2008) Fatty liver: a novel component of the metabolic syndrome. Arterioscler Thromb Vasc Biol 28:27–38CrossRefPubMed
4.
Zurück zum Zitat Targher G, Marra F, Marchesini (2008) Increased risk of cardiovascular disease in non-alcoholic fatty liver disease: causal effect or epiphenomenon? Diabetologia 51:1947–1953CrossRefPubMed Targher G, Marra F, Marchesini (2008) Increased risk of cardiovascular disease in non-alcoholic fatty liver disease: causal effect or epiphenomenon? Diabetologia 51:1947–1953CrossRefPubMed
5.
Zurück zum Zitat Misra VL, Khashab M, Chalasani N (2009) Nonalcoholic fatty liver disease and cardiovascular risk. Curr Gastroenterol Rep 11:50–55CrossRefPubMed Misra VL, Khashab M, Chalasani N (2009) Nonalcoholic fatty liver disease and cardiovascular risk. Curr Gastroenterol Rep 11:50–55CrossRefPubMed
6.
Zurück zum Zitat Targher G, Bertolini L, Rodella S et al (2008) Non-alcoholic fatty liver disease is independently associated with an increased prevalence of chronic kidney disease and proliferative/laser-treated retinopathy in type 2 diabetic patients. Diabetologia 51:444–450CrossRefPubMed Targher G, Bertolini L, Rodella S et al (2008) Non-alcoholic fatty liver disease is independently associated with an increased prevalence of chronic kidney disease and proliferative/laser-treated retinopathy in type 2 diabetic patients. Diabetologia 51:444–450CrossRefPubMed
7.
Zurück zum Zitat Mohamed Q, Gillies M, Wong TY (2007) Management of diabetic retinopathy: a systematic review. JAMA 298:902–916CrossRefPubMed Mohamed Q, Gillies M, Wong TY (2007) Management of diabetic retinopathy: a systematic review. JAMA 298:902–916CrossRefPubMed
8.
Zurück zum Zitat Rossing P (2006) Prediction, progression and prevention of diabetic nephropathy. The Minkowski Lecture 2005. Diabetologia 49:11–19CrossRefPubMed Rossing P (2006) Prediction, progression and prevention of diabetic nephropathy. The Minkowski Lecture 2005. Diabetologia 49:11–19CrossRefPubMed
9.
Zurück zum Zitat Targher G, Bertolini L, Padovani R et al (2007) Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patients. Diabetes Care 30:1212–1218CrossRefPubMed Targher G, Bertolini L, Padovani R et al (2007) Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patients. Diabetes Care 30:1212–1218CrossRefPubMed
10.
Zurück zum Zitat Stevens LA, Coresh J, Greene T, Levey AS (2006) Assessing kidney function—measured and estimated glomerular filtration rate. N Engl J Med 354:2473–2483CrossRefPubMed Stevens LA, Coresh J, Greene T, Levey AS (2006) Assessing kidney function—measured and estimated glomerular filtration rate. N Engl J Med 354:2473–2483CrossRefPubMed
11.
Zurück zum Zitat American Diabetes Association (2010) Standards of medical care in diabetes—2010. Diabetes Care 33(Suppl 1):S11–S61CrossRef American Diabetes Association (2010) Standards of medical care in diabetes—2010. Diabetes Care 33(Suppl 1):S11–S61CrossRef
12.
Zurück zum Zitat Sattar N, Gaw A, Scherbakova O et al (2003) Metabolic syndrome with and without C-reactive protein as a predictor of coronary heart disease and diabetes in the West of Scotland Coronary Prevention Study. Circulation 108:414–419CrossRefPubMed Sattar N, Gaw A, Scherbakova O et al (2003) Metabolic syndrome with and without C-reactive protein as a predictor of coronary heart disease and diabetes in the West of Scotland Coronary Prevention Study. Circulation 108:414–419CrossRefPubMed
13.
Zurück zum Zitat Girman CJ, Rhodes T, Mercuri M, 4S Group and the AFCAPS/TexCAPS Research Group et al (2004) The metabolic syndrome and risk of major coronary events in the Scandinavian Simvastatin Survival Study (4S) and the Air Force/Texas Coronary Atherosclerosis Prevention Study (AFCAPS/TexCAPS). Am J Cardiol 93:136–141CrossRefPubMed Girman CJ, Rhodes T, Mercuri M, 4S Group and the AFCAPS/TexCAPS Research Group et al (2004) The metabolic syndrome and risk of major coronary events in the Scandinavian Simvastatin Survival Study (4S) and the Air Force/Texas Coronary Atherosclerosis Prevention Study (AFCAPS/TexCAPS). Am J Cardiol 93:136–141CrossRefPubMed
14.
Zurück zum Zitat Wilkinson CP, Ferris FL, Klein RE, Global Diabetic Retinopathy Project Group et al (2003) Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology 110:1677–1682CrossRefPubMed Wilkinson CP, Ferris FL, Klein RE, Global Diabetic Retinopathy Project Group et al (2003) Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology 110:1677–1682CrossRefPubMed
15.
Zurück zum Zitat Joseph AE, Saverymuttu SH, al-Sam S, Cook MG, Maxwell JD (1991) Comparison of liver histology with ultrasonography in assessing diffuse parenchymal liver disease. Clin Radiol 43:26–31CrossRefPubMed Joseph AE, Saverymuttu SH, al-Sam S, Cook MG, Maxwell JD (1991) Comparison of liver histology with ultrasonography in assessing diffuse parenchymal liver disease. Clin Radiol 43:26–31CrossRefPubMed
16.
Zurück zum Zitat Saadeh S, Younossi ZM, Remer EM et al (2002) The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology 123:745–750CrossRefPubMed Saadeh S, Younossi ZM, Remer EM et al (2002) The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology 123:745–750CrossRefPubMed
17.
Zurück zum Zitat Mehta SR, Thomas EL, Bell JD, Johnston DG, Taylor-Robinson SD (2008) Non-invasive means of measuring hepatic fat content. World J Gastroenterol 14:3476–3483CrossRefPubMed Mehta SR, Thomas EL, Bell JD, Johnston DG, Taylor-Robinson SD (2008) Non-invasive means of measuring hepatic fat content. World J Gastroenterol 14:3476–3483CrossRefPubMed
18.
Zurück zum Zitat Targher G, Bertolini L, Poli F et al (2005) Nonalcoholic fatty liver disease and risk of future cardiovascular events among type 2 diabetic patients. Diabetes 54:3541–3546CrossRefPubMed Targher G, Bertolini L, Poli F et al (2005) Nonalcoholic fatty liver disease and risk of future cardiovascular events among type 2 diabetic patients. Diabetes 54:3541–3546CrossRefPubMed
19.
Zurück zum Zitat Targher G, Bertolini L, Rodella S et al (2007) Nonalcoholic fatty liver disease is independently associated with an increased incidence of cardiovascular events in type 2 diabetic patients. Diabetes Care 30:2119–2121CrossRefPubMed Targher G, Bertolini L, Rodella S et al (2007) Nonalcoholic fatty liver disease is independently associated with an increased incidence of cardiovascular events in type 2 diabetic patients. Diabetes Care 30:2119–2121CrossRefPubMed
20.
Zurück zum Zitat Thorn LM, Forsblom C, Fagerudd J, FinnDiane Study Group et al (2005) Metabolic syndrome in type 1 diabetes. Association with diabetic nephropathy and glycemic control (the FinnDiane study). Diabetes Care 28:2019–2024CrossRefPubMed Thorn LM, Forsblom C, Fagerudd J, FinnDiane Study Group et al (2005) Metabolic syndrome in type 1 diabetes. Association with diabetic nephropathy and glycemic control (the FinnDiane study). Diabetes Care 28:2019–2024CrossRefPubMed
21.
Zurück zum Zitat Pambianco G, Costacou T, Orchard TJ (2007) The prediction of major outcomes of type 1 diabetes: a 12-year prospective evaluation of three separate definitions of the metabolic syndrome and their components and estimated glucose disposal rate. The Pittsburgh Epidemiology of Diabetes Complications Study Experience. Diabetes Care 30:1248–1254CrossRefPubMed Pambianco G, Costacou T, Orchard TJ (2007) The prediction of major outcomes of type 1 diabetes: a 12-year prospective evaluation of three separate definitions of the metabolic syndrome and their components and estimated glucose disposal rate. The Pittsburgh Epidemiology of Diabetes Complications Study Experience. Diabetes Care 30:1248–1254CrossRefPubMed
22.
Zurück zum Zitat Kilpatrick ES, Rigby AS, Atkin SL (2007) Insulin resistance, the metabolic syndrome, and complication risk in type 1 diabetes: “double diabetes” in the Diabetes Control and Complications Trial. Diabetes Care 30:707–712CrossRefPubMed Kilpatrick ES, Rigby AS, Atkin SL (2007) Insulin resistance, the metabolic syndrome, and complication risk in type 1 diabetes: “double diabetes” in the Diabetes Control and Complications Trial. Diabetes Care 30:707–712CrossRefPubMed
23.
Zurück zum Zitat Prati D, Taioli E, Zanella A et al (2002) Updated definitions of healthy ranges for serum alanine aminotransferase levels. Ann Intern Med 137:1–10PubMed Prati D, Taioli E, Zanella A et al (2002) Updated definitions of healthy ranges for serum alanine aminotransferase levels. Ann Intern Med 137:1–10PubMed
24.
Zurück zum Zitat Mofrad P, Contos MJ, Haque M et al (2003) Clinical and histological spectrum of nonalcoholic fatty liver disease associated with normal ALT values. Hepatology 37:1286–1292CrossRefPubMed Mofrad P, Contos MJ, Haque M et al (2003) Clinical and histological spectrum of nonalcoholic fatty liver disease associated with normal ALT values. Hepatology 37:1286–1292CrossRefPubMed
25.
Zurück zum Zitat Ratziu V, Imbert-Bismut F, Messous D, Poynard T (2004) The elusiveness of “normal” ALT in fatty liver. Hepatology 39:1172CrossRefPubMed Ratziu V, Imbert-Bismut F, Messous D, Poynard T (2004) The elusiveness of “normal” ALT in fatty liver. Hepatology 39:1172CrossRefPubMed
26.
Zurück zum Zitat Targher G, Chonchol M, Bertolini L et al (2008) Increased risk of CKD among type 2 diabetics with nonalcoholic fatty liver disease. J Am Soc Nephrol 19:1564–1570CrossRefPubMed Targher G, Chonchol M, Bertolini L et al (2008) Increased risk of CKD among type 2 diabetics with nonalcoholic fatty liver disease. J Am Soc Nephrol 19:1564–1570CrossRefPubMed
27.
Zurück zum Zitat Targher G, Kendrick J, Smits G, Chonchol M (2010) Relationship between elevated serum gamma-glutamyltransferase concentrations and chronic kidney disease in the United States population. Findings from the National Health and Nutrition Examination Survey 2001–2006. Nutr Metab Cardiovasc Dis. doi:10.1016/j.numecd.2009.05.012 PubMed Targher G, Kendrick J, Smits G, Chonchol M (2010) Relationship between elevated serum gamma-glutamyltransferase concentrations and chronic kidney disease in the United States population. Findings from the National Health and Nutrition Examination Survey 2001–2006. Nutr Metab Cardiovasc Dis. doi:10.​1016/​j.​numecd.​2009.​05.​012 PubMed
28.
Zurück zum Zitat Targher G, Bosworth C, Kendrick J, Smits G, Lippi G, Chonchol M (2009) Relationship of serum bilirubin concentrations to kidney function and albuminuria in the United States adult population. Findings from the National Health and Nutrition Examination Survey 2001–2006. Clin Chem Lab Med 47:1055–1062CrossRefPubMed Targher G, Bosworth C, Kendrick J, Smits G, Lippi G, Chonchol M (2009) Relationship of serum bilirubin concentrations to kidney function and albuminuria in the United States adult population. Findings from the National Health and Nutrition Examination Survey 2001–2006. Clin Chem Lab Med 47:1055–1062CrossRefPubMed
29.
Zurück zum Zitat Ryu S, Chang Y, Kim DI, Kim WS, Suh BS (2007) Gamma-glutamyltransferase as a predictor of chronic kidney disease in nonhypertensive and nondiabetic Korean men. Clin Chem 53:71–77CrossRefPubMed Ryu S, Chang Y, Kim DI, Kim WS, Suh BS (2007) Gamma-glutamyltransferase as a predictor of chronic kidney disease in nonhypertensive and nondiabetic Korean men. Clin Chem 53:71–77CrossRefPubMed
30.
Zurück zum Zitat Lee DH, Jacobs DR, Gross M, Steffes M (2005) Serum gamma-glutamyltransferase was differently associated with microalbuminuria by status of hypertension and diabetes: the Coronary Artery Risk development in Young Adults (CARDIA) study. Clin Chem 51:1185–1191CrossRefPubMed Lee DH, Jacobs DR, Gross M, Steffes M (2005) Serum gamma-glutamyltransferase was differently associated with microalbuminuria by status of hypertension and diabetes: the Coronary Artery Risk development in Young Adults (CARDIA) study. Clin Chem 51:1185–1191CrossRefPubMed
31.
Zurück zum Zitat Targher G, Chonchol M, Miele L, Zoppini G, Pichiri I, Muggeo M (2009) Nonalcoholic fatty liver disease as a contributor to hypercoagulation and thrombophilia in the metabolic syndrome. Semin Thromb Hemost 35:277–287CrossRefPubMed Targher G, Chonchol M, Miele L, Zoppini G, Pichiri I, Muggeo M (2009) Nonalcoholic fatty liver disease as a contributor to hypercoagulation and thrombophilia in the metabolic syndrome. Semin Thromb Hemost 35:277–287CrossRefPubMed
32.
Zurück zum Zitat Edens MA, Kuipers F, Stolk RP (2009) Non-alcoholic fatty liver disease is associated with cardiovascular disease risk markers. Obes Rev 10:412–419CrossRefPubMed Edens MA, Kuipers F, Stolk RP (2009) Non-alcoholic fatty liver disease is associated with cardiovascular disease risk markers. Obes Rev 10:412–419CrossRefPubMed
33.
Zurück zum Zitat Yoneda M, Mawatari H, Fujita K et al (2007) High-sensitivity C-reactive protein is an independent clinical feature of nonalcoholic steatohepatitis (NASH) and also of the severity of fibrosis in NASH. J Gastroenterol 42:573–582CrossRefPubMed Yoneda M, Mawatari H, Fujita K et al (2007) High-sensitivity C-reactive protein is an independent clinical feature of nonalcoholic steatohepatitis (NASH) and also of the severity of fibrosis in NASH. J Gastroenterol 42:573–582CrossRefPubMed
34.
Zurück zum Zitat Thuy S, Ladurner R, Volynets V et al (2008) Nonalcoholic fatty liver disease in humans is associated with increased plasma endotoxin and plasminogen activator inhibitor 1 concentrations and with fructose intake. J Nutr 138:1452–1455PubMed Thuy S, Ladurner R, Volynets V et al (2008) Nonalcoholic fatty liver disease in humans is associated with increased plasma endotoxin and plasminogen activator inhibitor 1 concentrations and with fructose intake. J Nutr 138:1452–1455PubMed
35.
Zurück zum Zitat Wieckowska A, Papouchado BG, Li Z, Lopez R, Zein NN, Feldstein AE (2008) Increased hepatic and circulating interleukin-6 levels in human nonalcoholic steatohepatitis. Am J Gastroenterol 103:1372–1379CrossRefPubMed Wieckowska A, Papouchado BG, Li Z, Lopez R, Zein NN, Feldstein AE (2008) Increased hepatic and circulating interleukin-6 levels in human nonalcoholic steatohepatitis. Am J Gastroenterol 103:1372–1379CrossRefPubMed
Metadaten
Titel
Non-alcoholic fatty liver disease is independently associated with an increased prevalence of chronic kidney disease and retinopathy in type 1 diabetic patients
verfasst von
G. Targher
L. Bertolini
M. Chonchol
S. Rodella
G. Zoppini
G. Lippi
L. Zenari
E. Bonora
Publikationsdatum
01.07.2010
Verlag
Springer-Verlag
Erschienen in
Diabetologia / Ausgabe 7/2010
Print ISSN: 0012-186X
Elektronische ISSN: 1432-0428
DOI
https://doi.org/10.1007/s00125-010-1720-1

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