#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Factors influencing subclinical atherosclerosis in patients with biopsy-proven nonalcoholic fatty liver disease


Autoři: Taeang Arai aff001;  Masanori Atsukawa aff001;  Akihito Tsubota aff002;  Tadamichi Kawano aff001;  Mai Koeda aff003;  Yuji Yoshida aff003;  Tomohide Tanabe aff001;  Tomomi Okubo aff003;  Korenobu Hayama aff001;  Ai Iwashita aff001;  Norio Itokawa aff003;  Chisa Kondo aff001;  Keiko Kaneko aff001;  Chiaki Kawamoto aff001;  Tsutomu Hatori aff004;  Naoya Emoto aff005;  Etsuko Iio aff006;  Yasuhito Tanaka aff006;  Katsuhiko Iwakiri aff001
Působiště autorů: Division of Gastroenterology and Hepatology, Nippon Medical School, Tokyo, Japan aff001;  Core Research Facilities for Basic Science, Research Center for Medical Sciences, The Jikei University School of Medicine, Tokyo, Japan aff002;  Division of Gastroenterology, Nippon Medical School Chiba Hokusoh Hospital, Inzai, Japan aff003;  Division of Pathology, Nippon Medical School Chiba Hokusoh Hospital, Inzai, Japan aff004;  Division of Endocrinology, Nippon Medical School Chiba Hokusoh Hospital, Inzai, Japan aff005;  Department of Virology and Liver Unit, Nagoya City University Graduate School of Medicinal Sciences, Nagoya, Japan aff006
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224184

Souhrn

Although the presence of nonalcoholic fatty liver disease (NAFLD) is known to be related to subclinical atherosclerosis, the relationship between the severity of NAFLD and subclinical atherosclerosis is not clear. This study aimed to clarify the factors related to subclinical arteriosclerosis, including the histopathological severity of the disease and PNPLA3 gene polymorphisms, in NAFLD patients. We measured brachial-ankle pulse wave velocity (baPWV) as an index of arterial stiffness in 153 biopsy-proven NAFLD patients. The baPWV values were significantly higher in the advanced fibrosis group than in the less advanced group (median, 1679 cm/s vs 1489 cm/s; p = 5.49×10−4). Multiple logistic regression analysis revealed that older age (≥55 years) (p = 8.57×10−3; OR = 3.03), hypertension (p = 1.05×10−3; OR = 3.46), and advanced fibrosis (p = 9.22×10−3; OR = 2.94) were independently linked to baPWV ≥1600 cm/s. NAFLD patients were categorized into low-risk group (number of risk factors = 0), intermediate-risk group (= 1), and high-risk group (≥2) based on their risk factors, including older age, hypertension, and biopsy-confirmed advanced fibrosis. The prevalence of baPWV ≥1600 cm/s was 7.1% (3/42) in the low-risk group, 30.8% (12/39) in the intermediate-risk group, and 63.9% (46/72) in the high-risk group. Non-invasive liver fibrosis markers and scores, including the FIB-4 index, NAFLD fibrosis score, hyaluronic acid, Wisteria floribunda agglutinin positive Mac-2-binding protein, and type IV collagen 7s, were feasible substitutes for invasive liver biopsy. Older age, hypertension, and advanced fibrosis are independently related to arterial stiffness, and a combination of these three factors may predict risk of arteriosclerosis in NAFLD patients.

Klíčová slova:

Fibrosis – Hypertension – Medical risk factors – Liver fibrosis – Fatty liver – Biopsy – Steatosis – Atherosclerosis


Zdroje

1. Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016; 64: 73–84. doi: 10.1002/hep.28431 26707365

2. Hashimoto E, Tokushige K. Prevalence, gender, ethnic variations, and prognosis of NASH. J Gastroenterol. 2011; 46: 63–9. doi: 10.1007/s00535-010-0311-8 20844903

3. Farrell GC, Larter CZ. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology. 2006; 43: S99–S112. doi: 10.1002/hep.20973 16447287

4. Taniai M, Hashimoto E, Tobari M, Kodama K, Tokushige K, Yamamoto M, et al. Clinicopathological investigation of steatohepatitic hepatocellular carcinoma: A multicenter study using immunohistochemical analysis of adenoma-related markers. Hepatol Res. 2018; 48: 947–955. doi: 10.1111/hepr.13203 30058778

5. Le MH, Devaki P, Ha NB, Jun DW, Te HS, Cheung RC, et al. Prevalence of non-alcoholic fatty liver disease and risk factors for advanced fibrosis and mortality in the United States. PLoS One. 2017; 27: e0173499. doi: 10.1371/journal.pone.0173499 PMID: 28346543

6. Angulo P, Kleiner DE, Dam-Larsen S, Adams LA, Bjornsson ES, Charatcharoenwitthaya P, et al. Liver Fibrosis, but No Other Histologic Features, Is Associated With Long-term Outcomes of Patients With Nonalcoholic Fatty Liver Disease. Gastroenterology. 2015; 149: 389–397. doi: 10.1053/j.gastro.2015.04.043 25935633

7. Hagström H, Nasr P, Ekstedt M, Hammar U, Stål P, Hultcrantz R, et al. Fibrosis stage but not NASH predicts mortality and time to development of severe liver disease in biopsy-proven NAFLD. J Hepatol. 2017; 67: 1265–1273. doi: 10.1016/j.jhep.2017.07.027 28803953

8. Adams LA, Lymp JF, St Sauver J, Sanderson SO, Lindor KD, Feldstein A, et al. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology. 2005; 129: 113–21. doi: 10.1053/j.gastro.2005.04.014 16012941

9. Lonardo A, Nascimbeni F, Targher G, Bernardi M, Bonino F, Bugianesi E, et al. AISF position paper on nonalcoholic fatty liver disease (NAFLD): Updates and future directions. Dig Liver Dis. 2017; 49: 471–483. doi: 10.1016/j.dld.2017.01.147 28215516

10. Oni ET, Agatston AS, Blaha MJ, Fialkow J, Cury R, Sposito A, et al. A systematic review: burden and severity of subclinical cardiovascular disease among those with nonalcoholic fatty liver; should we care? Atherosclerosis. 2013; 230: 258–67. doi: 10.1016/j.atherosclerosis.2013.07.052 24075754

11. Zhou YY, Zhou XD, Wu SJ, Fan DH, Van Poucke S, Chen YP, et al. Nonalcoholic fatty liver disease contributes to subclinical atherosclerosis: A systematic review and meta-analysis. Hepatol Commun. 2018; 2: 376–392. doi: 10.1002/hep4.1155 29619417

12. Gummesson A, Strömberg U, Schmidt C, Kullberg J, Angerås O, Lindgren S, et al. Non-alcoholic fatty liver disease is a strong predictor of coronary artery calcification in metabolically healthy subjects: A cross-sectional, population-based study in middle-aged subjects. PLoS One. 2018; 13: e0202666. doi: 10.1371/journal.pone.0202666 30133541

13. Sunbul M, Agirbasli M, Durmus E, Kivrak T, Akin H, Aydin Y, et al. Arterial stiffness in patients with non-alcoholic fatty liver disease is related to fibrosis stage and epicardial adipose tissue thickness. Atherosclerosis. 2014; 237: 490–3. doi: 10.1016/j.atherosclerosis.2014.10.004 25463079

14. Ozturk K, Uygun A, Guler AK, Demirci H, Ozdemir C, Cakir M, et al. Nonalcoholic fatty liver disease is an independent risk factor for atherosclerosis in young adult men. Atherosclerosis. 2015; 240: 380–6. doi: 10.1016/j.atherosclerosis.2015.04.009 25875390

15. Targher G, Bertolini L, Padovani R, Rodella S, Zoppini G, Zenari L, et al. Relations between carotid artery wall thickness and liver histology in subjects with nonalcoholic fatty liver disease. Diabetes Care. 2006; 29: 1325–30. doi: 10.2337/dc06-0135 16732016

16. Romeo S, Kozlitina J, Xing C, Pertsemlidis A, Cox D, Pennacchio LA, et al. Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nat Genet. 2008; 40: 1461–5. doi: 10.1038/ng.257 18820647

17. Sookoian S, Pirola CJ. Meta-analysis of the influence of I148M variant of patatin-like phospholipase domain containing 3 gene (PNPLA3) on the susceptibility and histological severity of nonalcoholic fatty liver disease. Hepatology. 2011; 53: 1883–94. doi: 10.1002/hep.24283 21381068

18. Koo BK, Joo SK, Kim D, Bae JM, Park JH, Kim JH, et al. Additive effects of PNPLA3 and TM6SF2 on the histological severity of non-alcoholic fatty liver disease. J Gastroenterol Hepatol. 2018; 33: 1277–1285. doi: 10.1111/jgh.14056 29193269

19. Petta S, Valenti L, Marchesini G, Di Marco V, Licata A, Cammà C, et al. PNPLA3 GG genotype and carotid atherosclerosis in patients with non-alcoholic fatty liver disease. PLoS One. 2013; 8: e74089. doi: 10.1371/journal.pone.0074089 24069270

20. Kawaguchi T, Sumida Y, Umemura A, Matsuo K, Takahashi M, Takamura T, et al. Genetic polymorphisms of the human PNPLA3 gene are strongly associated with severity of non-alcoholic fatty liver disease in Japanese. PLoS One. 2012; 7: e38322. doi: 10.1371/journal.pone.0038322 22719876

21. Seko Y, Sumida Y, Tanaka S, Mori K, Taketani H, Ishiba H, et al. Development of hepatocellular carcinoma in Japanese patients with biopsy-proven non-alcoholic fatty liver disease: Association between PNPLA3 genotype and hepatocarcinogenesis/fibrosis progression. Hepatol Res. 2017; 47: 1083–1092. doi: 10.1111/hepr.12840 27862719

22. Marchesini G, Day ChP, Dufour JF, Canbay A, Nobili V, Ratziu V, et al. EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. J Hepatol. 2016; 64: 1388–402. doi: 10.1016/j.jhep.2015.11.004 27062661

23. Bugianesi E, Rosso C, Cortez-Pinto H. How to diagnose NAFLD in 2016. J Hepatol. 2016; 65: 643–4. doi: 10.1016/j.jhep.2016.05.038 27401791

24. Nascimbeni F, Pais R, Bellentani S, Day CP, Ratziu V, Loria P, et al. From NAFLD in clinical practice to answers from guidelines. J Hepatol. 2013; 59: 859–71. doi: 10.1016/j.jhep.2013.05.044 23751754

25. Shimamoto K, Ando K, Fujita T, Hasebe N, Higaki J, Horiuchi M, et al. The Japanese Society of Hypertension Guidelines for the Management of Hypertension (JSH 2014). Hypertens Res. 2014; 37: 253–390. doi: 10.1038/hr.2014.20 24705419

26. Teramoto T, Sasaki J, Ishibashi S, Birou S, Daida H, Dohi S, et al. Executive summary of the Japan Atherosclerosis Society (JAS) guidelines for the diagnosis and prevention of atherosclerotic cardiovascular diseases in Japan -2012 version. J Atheroscler Thromb. 2013; 20: 517–23. doi: 10.5551/jat.15792 23665881

27. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985; 28: 412–9. doi: 10.1007/bf00280883 3899825

28. Suzuki A, Angulo P, Lymp J, Li D, Satomura S, Lindor K. Hyaluronic acid, an accurate serum marker for severe hepatic fibrosis in patients with non-alcoholic fatty liver disease. Liver Int. 2005; 25: 779–86. doi: 10.1111/j.1478-3231.2005.01064.x 15998429

29. Yoneda M, Mawatari H, Fujita K, Yonemitsu K, Kato S, Takahashi H, et al. Type IV collagen 7s domain is an independent clinical marker of the severity of fibrosis in patients with nonalcoholic steatohepatitis before the cirrhotic stage. J Gastroenterol. 2007; 42: 375–81. doi: 10.1007/s00535-007-2014-3 17530362

30. Ogawa Y, Honda Y, Kessoku T, Tomeno W, Imajo K, Yoneda M, et al. Wisteria floribunda agglutinin-positive Mac-2-binding protein and type 4 collagen 7S: useful markers for the diagnosis of significant fibrosis in patients with non-alcoholic fatty liver disease. J Gastroenterol Hepatol. 2018; 33: 1795–1803. doi: 10.1111/jgh.14156 29633352

31. Abe M, Miyake T, Kuno A, Imai Y, Sawai Y, Hino K, et al. Association between Wisteria floribunda agglutinin-positive Mac-2 binding protein and the fibrosis stage of non-alcoholic fatty liver disease. J Gastroenterol. 2015; 50: 776–84. doi: 10.1007/s00535-014-1007-2 25326152

32. Atsukawa M, Tsubota A, Okubo T, Arai T, Nakagawa A, Itokawa N, et al. Serum Wisteria floribunda agglutinin-positive Mac-2 binding protein more reliably distinguishes liver fibrosis stages in non-alcoholic fatty liver disease than serum Mac-2 binding protein. Hepatol Res. 2018; 48: 424–432. doi: 10.1111/hepr.13046 29274190

33. Sumida Y, Yoneda M, Hyogo H, Itoh Y, Ono M, Fujii H, et al. Validation of the FIB4 index in a Japanese nonalcoholic fatty liver disease population. BMC Gastroenterol. 2012; 12: 2. doi: 10.1186/1471-230X-12-2 22221544

34. Angulo P, Hui JM, Marchesini G, Bugianesi E, George J, Farrell GC, et al. The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD. Hepatology. 2007; 45: 846–54. doi: 10.1002/hep.21496 17393509

35. Van Bortel LM, Laurent S, Boutouyrie P, Chowienczyk P, Cruickshank JK, De Backer T, et al. Expert consensus document on the measurement of aortic stiffness in daily practice using carotid-femoral pulse wave velocity. J Hypertens. 2012; 30: 445–8. doi: 10.1097/HJH.0b013e32834fa8b0 22278144

36. Kim HJ, Nam JS, Park JS, Cho M, Kim CS, Ahn CW, et al. Usefulness of brachial-ankle pulse wave velocity as a predictive marker of multiple coronary artery occlusive disease in Korean type 2 diabetes patients. Diabetes Res Clin Pract. 2009; 85: 30–4. doi: 10.1016/j.diabres.2009.03.013 19398141

37. Yambe M, Tomiyama H, Hirayama Y, Gulniza Z, Takata Y, Koji Y, et al. Arterial stiffening as a possible risk factor for both atherosclerosis and diastolic heart failure. Hypertens Res. 2004; 27: 625–31. doi: 10.1291/hypres.27.625 15750255

38. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005; 41: 1313–21. doi: 10.1002/hep.20701 15915461

39. Tomiyama H, Matsumoto C, Shiina K, Yamashina A. Brachial-Ankle PWV: Current Status and Future Directions as a Useful Marker in the Management of Cardiovascular Disease and/or Cardiovascular Risk Factors. J Atheroscler Thromb. 2016; 23: 128–46. doi: 10.5551/jat.32979 26558401

40. Salvi P, Ruffini R, Agnoletti D, Magnani E, Pagliarani G, Comandini G, et al. Increased arterial stiffness in nonalcoholic fatty liver disease: the Cardio-GOOSE study. J Hypertens. 2010; 28: 1699–707. doi: 10.1097/HJH.0b013e32833a7de6 20467324

41. Huang RC, Beilin LJ, Ayonrinde O, Mori TA, Olynyk JK, Burrows S, et al. Importance of cardiometabolic risk factors in the association between nonalcoholic fatty liver disease and arterial stiffness in adolescents. Hepatology. 2013; 58: 1306–14. doi: 10.1002/hep.26495 23703776

42. Huang Y, Bi Y, Xu M, Ma Z, Xu Y, Wang T, et al. Nonalcoholic fatty liver disease is associated with atherosclerosis in middle-aged and elderly Chinese. Arterioscler Thromb Vasc Biol. 2012; 32: 2321–6. doi: 10.1161/ATVBAHA.112.252957 22814750

43. Lee YJ, Shim JY, Moon BS, Shin YH, Jung DH, Lee JH, et al. The relationship between arterial stiffness and nonalcoholic fatty liver disease. Dig Dis Sci. 2012; 57: 196–203. doi: 10.1007/s10620-011-1819-3 21750929

44. Li N, Zhang GW, Zhang JR, Jin D, Li Y, Liu T, et al. Non-alcoholic fatty liver disease is associated with progression of arterial stiffness. Nutr Metab Cardiovasc Dis. 2015; 25: 218–23. doi: 10.1016/j.numecd.2014.10.002 25456154

45. Chen Y, Xu M, Wang T, Sun J, Sun W, Xu B, et al. Advanced fibrosis associates with atherosclerosis in subjects with nonalcoholic fatty liver disease. Atherosclerosis. 2015; 241: 145–50. doi: 10.1016/j.atherosclerosis.2015.05.002 25988358

46. Leite NC, Villela-Nogueira CA, Ferreira MT, Cardoso CR, Salles GF. Increasing aortic stiffness is predictive of advanced liver fibrosis in patients with type 2 diabetes: the Rio-T2DM cohort study. Liver Int. 2016; 36: 977–85. doi: 10.1111/liv.12994 26509555

47. Fargion S, Porzio M, Fracanzani AL. Nonalcoholic fatty liver disease and vascular disease: state-of-the-art. World J Gastroenterol. 2014; 20: 13306–24. doi: 10.3748/wjg.v20.i37.13306 25309067

48. Targher G, Day CP, Bonora E. Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med. 2010; 363: 1341–50. doi: 10.1056/NEJMra0912063 20879883

49. Wree A, Broderick L, Canbay A, Hoffman HM, Feldstein AE. From NAFLD to NASH to cirrhosis-new insights into disease mechanisms. Nat Rev Gastroenterol Hepatol. 2013; 10: 627–36. doi: 10.1038/nrgastro.2013.149 23958599

50. Di Costanzo A, D'Erasmo L, Polimeni L, Baratta F, Coletta P, Di Martino M, et al. Non-alcoholic fatty liver disease and subclinical atherosclerosis: A comparison of metabolically- versus genetically-driven excess fat hepatic storage. Atherosclerosis. 2017; 257: 232–239. doi: 10.1016/j.atherosclerosis.2016.12.018 28027788


Článok vyšiel v časopise

PLOS One


2019 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#