Noninvasive assessment of liver disease severity in patients with nonalcoholic fatty liver disease (NAFLD) and type 2 diabetes

Grazia Pennisi¹, Marco Enea¹, Vincenzo Falco², Guruprasad P Aithal^{3

4}, Naaventhan Palaniyappan^{3

4}, Yusuf Yilmaz⁵, Jerome Boursier^{6

7}, Christophe Cassinotto⁸, Victor de Lédinghen⁹, Wah Kheong Chan¹⁰, Sanjiv Mahadeva¹⁰, Peter Eddowes^{3

4}, Philip Newsome^{3

4}, Thomas Karlas¹¹, Johannes Wiegand¹¹, Vincent Wai-Sun Wong¹², Jörn M Schattenberg^{13

14}, Christian Labenz^{13

14}, Won Kim¹⁵, Myoung Seok Lee¹⁵, Monica Lupsor-Platon¹⁶, Jeremy F L Cobbold¹⁷, Jian-Gao Fan¹⁸, Feng Shen¹⁸, Katharina Staufer^{19

20}, Michael Trauner¹⁹, Rudolf Stauber²¹, Atsushi Nakajima²², Masato Yoneda²², Elisabetta Bugianesi²³, Ramy Younes²³, Silvia Gaia²³, Ming-Hua Zheng^{24

25}, Calogero Cammà^{1

2}, Quentin M Anstee^{26

27}, Ferenc E Mózes²⁸, Michael Pavlides^{17

28}, Salvatore Petta^{1

2}

Affiliations

¹ Sezione di Gastroenterologia, PROMISE, University of Palermo, Italy.
² Department of Economics and Statistics, University of Palermo, Palermo, Italy.
³ NIHR Nottingham Biomedical Research Centre (BRC), Nottingham University Hospitals NHS Trust and the University of Nottingham, Nottingham, UK.
⁴ Nottingham Digestive Diseases Centre, Translational Medical Sciences, School of Medicine, University of Nottingham, Nottingham, UK.
⁵ Department of Gastroenterology, School of Medicine, Recep Tayyip Erdogan University, Rize, Turkey.
⁶ Hepato-Gastroenterology Department, Angers University Hospital, Angers, France.
⁷ HIFIH Laboratory, UPRES EA3859, Angers University, Angers, France.
⁸ Department of Diagnostic and Interventional Radiology, Saint-Eloi Hospital, University Hospital of Montpellier, Montpellier, France.
⁹ Hepatology Unit, University Hospital Bordeaux and INSERM U-1053, Bordeaux University, Pessac, France.
¹⁰ Department of Medicine, Faculty of Medicine, University of Malaya, Malaysia.
¹¹ Department of Oncology, Gastroenterology, Hepatology, Pulmonology and Infectious Diseases, University Hospital Leipzig, Leipzig, Germany.
¹² Department of Medicine and Therapeutics, Faculty of Medicine, The Chinese University of Hong Kong.
¹³ Department of Internal Medicine I, University Medical Center of the Johannes Gutenberg-University, Mainz, Germany.
¹⁴ Cirrhosis Center Mainz (CCM), University Medical Center of the Johannes Gutenberg-University, Mainz, Germany.
¹⁵ Division of Gastroenterology and Hepatology, Department of Internal Medicine, Seoul National University College of Medicine, Seoul Metropolitan Government Boramae Medical Center, Seoul, Korea.
¹⁶ Department of Medical Imaging, Iuliu Hatieganu, University of Medicine and Pharmacy, Regional Institute of Gastroenterology and Hepatology "Prof. Dr. Octavian Fodor", Cluj-Napoca, Romania.
¹⁷ Translational Gastroenterology Unit, University of Oxford, Oxford, UK.
¹⁸ Department of Gastroenterology, Xinhua Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China.
¹⁹ Division of Gastroenterology & Hepatology, Department of Internal Medicine III, Medical University of Vienna, Austria.
²⁰ Division of Transplantation, Department of General Surgery, Medical University of Vienna, Austria.
²¹ Division of Gastroenterology and Hepatology, Department of Internal Medicine, Medical University of Graz, Austria.
²² Department of Gastroenterology and Hepatology, Yokohama City University School of Medicine, Yokohama, Japan.
²³ Division of Gastroenterology and Hepatology, Department of Medical Sciences, University of Turin, Italy.
²⁴ Department of Hepatology, MAFLD Research Center, the First Affiliated Hospital of Wenzhou Medical University, Wenzhou, China.
²⁵ Key Laboratory of Diagnosis and Treatment for The Development of Chronic Liver Disease in Zhejiang Province, Wenzhou, China.
²⁶ Translational and Clinical Research Institute, Faculty of Medical Sciences, Newcastle University, Newcastle upon Tyne, Tyne and Wear, UK.
²⁷ Newcastle NIHR Biomedical Research Center, Newcastle upon Tyne Hospitals NHS Trust, Newcastle upon Tyne, Tyne and Wear, UK.
²⁸ Radcliffe Department of Medical Sciences, Cardiovascular Medicine, University of Oxford, Oxford, UK.

PMID: 36924031
DOI: 10.1097/HEP.0000000000000351

Meta-Analysis

Noninvasive assessment of liver disease severity in patients with nonalcoholic fatty liver disease (NAFLD) and type 2 diabetes

Grazia Pennisi et al. Hepatology. 2023.

. 2023 Jul 1;78(1):195-211.

doi: 10.1097/HEP.0000000000000351. Epub 2023 Mar 17.

Authors

Affiliations

¹ Sezione di Gastroenterologia, PROMISE, University of Palermo, Italy.
² Department of Economics and Statistics, University of Palermo, Palermo, Italy.
³ NIHR Nottingham Biomedical Research Centre (BRC), Nottingham University Hospitals NHS Trust and the University of Nottingham, Nottingham, UK.
⁴ Nottingham Digestive Diseases Centre, Translational Medical Sciences, School of Medicine, University of Nottingham, Nottingham, UK.
⁵ Department of Gastroenterology, School of Medicine, Recep Tayyip Erdogan University, Rize, Turkey.
⁶ Hepato-Gastroenterology Department, Angers University Hospital, Angers, France.
⁷ HIFIH Laboratory, UPRES EA3859, Angers University, Angers, France.
⁸ Department of Diagnostic and Interventional Radiology, Saint-Eloi Hospital, University Hospital of Montpellier, Montpellier, France.
⁹ Hepatology Unit, University Hospital Bordeaux and INSERM U-1053, Bordeaux University, Pessac, France.
¹⁰ Department of Medicine, Faculty of Medicine, University of Malaya, Malaysia.
¹¹ Department of Oncology, Gastroenterology, Hepatology, Pulmonology and Infectious Diseases, University Hospital Leipzig, Leipzig, Germany.
¹² Department of Medicine and Therapeutics, Faculty of Medicine, The Chinese University of Hong Kong.
¹³ Department of Internal Medicine I, University Medical Center of the Johannes Gutenberg-University, Mainz, Germany.
¹⁴ Cirrhosis Center Mainz (CCM), University Medical Center of the Johannes Gutenberg-University, Mainz, Germany.
¹⁵ Division of Gastroenterology and Hepatology, Department of Internal Medicine, Seoul National University College of Medicine, Seoul Metropolitan Government Boramae Medical Center, Seoul, Korea.
¹⁶ Department of Medical Imaging, Iuliu Hatieganu, University of Medicine and Pharmacy, Regional Institute of Gastroenterology and Hepatology "Prof. Dr. Octavian Fodor", Cluj-Napoca, Romania.
¹⁷ Translational Gastroenterology Unit, University of Oxford, Oxford, UK.
¹⁸ Department of Gastroenterology, Xinhua Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China.
¹⁹ Division of Gastroenterology & Hepatology, Department of Internal Medicine III, Medical University of Vienna, Austria.
²⁰ Division of Transplantation, Department of General Surgery, Medical University of Vienna, Austria.
²¹ Division of Gastroenterology and Hepatology, Department of Internal Medicine, Medical University of Graz, Austria.
²² Department of Gastroenterology and Hepatology, Yokohama City University School of Medicine, Yokohama, Japan.
²³ Division of Gastroenterology and Hepatology, Department of Medical Sciences, University of Turin, Italy.
²⁴ Department of Hepatology, MAFLD Research Center, the First Affiliated Hospital of Wenzhou Medical University, Wenzhou, China.
²⁵ Key Laboratory of Diagnosis and Treatment for The Development of Chronic Liver Disease in Zhejiang Province, Wenzhou, China.
²⁶ Translational and Clinical Research Institute, Faculty of Medical Sciences, Newcastle University, Newcastle upon Tyne, Tyne and Wear, UK.
²⁷ Newcastle NIHR Biomedical Research Center, Newcastle upon Tyne Hospitals NHS Trust, Newcastle upon Tyne, Tyne and Wear, UK.
²⁸ Radcliffe Department of Medical Sciences, Cardiovascular Medicine, University of Oxford, Oxford, UK.

PMID: 36924031
DOI: 10.1097/HEP.0000000000000351

Abstract

Background and aims: We evaluated the diagnostic accuracy of simple, noninvasive tests (NITs) in NAFLD patients with type 2 diabetes (T2D).

Methods and results: This was an individual patient data meta-analysis of 1780 patients with biopsy-proven NAFLD and T2D. The index tests of interest were FIB-4, NAFLD Fibrosis Score (NFS), aspartate aminotransferase-to-platelet ratio index, liver stiffness measurement (LSM) by vibration-controlled transient elastography, and AGILE 3+. The target conditions were advanced fibrosis, NASH, and fibrotic NASH(NASH plus F2-F4 fibrosis). The diagnostic performance of noninvasive tests. individually or in sequential combination, was assessed by area under the receiver operating characteristic curve and by decision curve analysis. Comparison with 2278 NAFLD patients without T2D was also made. In NAFLD with T2D LSM and AGILE 3+ outperformed, both NFS and FIB-4 for advanced fibrosis (area under the receiver operating characteristic curve:LSM 0.82, AGILE 3+ 0.82, NFS 0.72, FIB-4 0.75, aspartate aminotransferase-to-platelet ratio index 0.68; p < 0.001 of LSM-based versus simple serum tests), with an uncertainty area of 12%-20%. The combination of serum-based with LSM-based tests for advanced fibrosis led to a reduction of 40%-60% in necessary LSM tests. Decision curve analysis showed that all scores had a modest net benefit for ruling out advanced fibrosis at the risk threshold of 5%-10% of missing advanced fibrosis. LSM and AGILE 3+ outperformed both NFS and FIB-4 for fibrotic NASH (area under the receiver operating characteristic curve:LSM 0.79, AGILE 3+ 0.77, NFS 0.71, FIB-4 0.71; p < 0.001 of LSM-based versus simple serum tests). All noninvasive scores were suboptimal for diagnosing NASH.

Conclusions: LSM and AGILE 3+ individually or in low availability settings in sequential combination after FIB-4 or NFS have a similar good diagnostic accuracy for advanced fibrosis and an acceptable diagnostic accuracy for fibrotic NASH in NAFLD patients with T2D.

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References

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Noninvasive assessment of liver disease severity in patients with nonalcoholic fatty liver disease (NAFLD) and type 2 diabetes

Affiliations

Noninvasive assessment of liver disease severity in patients with nonalcoholic fatty liver disease (NAFLD) and type 2 diabetes

Authors

Affiliations

Abstract

References

Publication types

MeSH terms

Substances

Grants and funding

LinkOut - more resources

Full Text Sources

Medical

Miscellaneous