Cited by 5,021Liver Disease Diagnosis and TreatmentLiver Disease and TransplantationHepatitis C virus research

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Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection†‡

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Sterling, Richard K., Lissen, Eduardo, Clumeck, Nathan, Sola, Ricard, Correa, Mendes Cassia, Montaner, Julio, S. Sulkowski, Mark, Torriani, Francesca J., Dieterich, Doug T., Thomas, David L., Messinger, Diethelm, Nelson, Mark·2006·Hepatology

DOI 10.1002/hep.21178

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Abstract

Liver biopsy remains the gold standard in the assessment of severity of liver disease. Noninvasive tests have gained popularity to predict histology in view of the associated risks of biopsy. However, many models include tests not readily available, and there are limited data from patients with HIV/hepatitis C virus (HCV) coinfection. We aimed to develop a model using routine tests to predict liver fibrosis in patients with HIV/HCV coinfection. A retrospective analysis of liver histology was performed in 832 patients. Liver fibrosis was assessed via Ishak score; patients were categorized as 0-1, 2-3, or 4-6 and were randomly assigned to training (n = 555) or validation (n = 277) sets. Multivariate logistic regression analysis revealed that platelet count (PLT), age, AST, and INR were significantly associated with fibrosis. Additional analysis revealed PLT, age, AST, and ALT as an alternative model. Based on this, a simple index (FIB-4) was developed: age ([yr] x AST [U/L]) / ((PLT [10(9)/L]) x (ALT [U/L])(1/2)). The AUROC of the index was 0.765 for differentiation between Ishak stage 0-3 and 4-6. At a cutoff of <1.45 in the validation set, the negative predictive value to exclude advanced fibrosis (stage 4-6) was 90% with a sensitivity of 70%. A cutoff of >3.25 had a positive predictive value of 65% and a specificity of 97%. Using these cutoffs, 87% of the 198 patients with FIB-4 values outside 1.45-3.25 would be correctly classified, and liver biopsy could be avoided in 71% of the validation group. In conclusion, noninvasive tests can accurately predict hepatic fibrosis and may reduce the need for liver biopsy in the majority of HIV/HCV-coinfected patients.

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Declining Morbidity and Mortality among Patients with Advanced Human Immunodeficiency Virus Infection
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Bédossa, P., Dargère, D., & Paradis, V. (2003) · Hepatology · doi:10.1016/j.hep.2003.09.022 · Cited by 2,370
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Liver Biopsy
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APRI and FIB-4 in the evaluation of liver fibrosis in chronic hepatitis C patients stratified by AST level
Yen, Y., Kuo, F., Kee, K., Chang, K., Tsai, M., Hu, T., Lu, S., Wang, J., Hung, C., & Chen, C.-H. (2018) · PLoS ONE · doi:10.1371/journal.pone.0199760 · Cited by 64
Wisteria floribunda agglutinin positive human Mac‐2‐binding protein as a predictor of hepatocellular carcinoma development in chronic hepatitis C patients
Tamaki, N., Kurosaki, M., Kuno, A., Korenaga, M., Togayachi, A., Gotoh, M., Nakakuki, N., Takada, H., Matsuda, S., Hattori, N., et al. (2015) · Hepatology Research · doi:10.1111/hepr.12466 · Cited by 63
Association of liver steatosis and fibrosis with clinical outcomes in patients with SARS-CoV-2 infection (COVID-19)
López-Méndez, I., Aquino-Matus, J., Gall, S. M., Prieto-Nava, J., Juárez-Hernández, E., Uribe, M., & Castro-Narro, G. (2020) · Annals of Hepatology · doi:10.1016/j.aohep.2020.09.015 · Cited by 58
Liver Fibrosis Index FIB‐4 Is Associated With Mortality in COVID‐19
Li, Y., Regan, J., Fajnzylber, J. M., Coxen, K., Corry, H., Wong, C., Rosenthal, A., Atyeo, C. G., Fischinger, S., Gillespie, E., et al. (2020) · Hepatology Communications · doi:10.1002/hep4.1650 · Cited by 65
“(10) FIB-4 was calculated using the following formula(6):”
BackgroundMethodInfluential
Fibrosis-4 Index Reflects Right Ventricular Function and Prognosis in Heart Failure with Preserved Ejection Fraction
Nakashima, M., Sakuragi, S., Miyoshi, T., Takayama, S., Kawaguchi, T., Kodera, N., Akai, H., Koide, Y., Otsuka, H., Wada, T., et al. (2021) · ESC Heart Failure · doi:10.1002/ehf2.13317 · Cited by 65
“The fibrosis-4 index (FIB-4 index) was reported as a simple index to evaluate liver fibrosis.(7) The FIB-4 index is calculated from four parameters: age, aspartate aminotransferase (AST),”
BackgroundMethod
Higher Enhancement Intrahepatic Nodules on the Hepatobiliary Phase of Gd-EOB-DTPA-Enhanced MRI as a Poor Responsive Marker of Anti-PD-1/PD-L1 Monotherapy for Unresectable Hepatocellular Carcinoma
Aoki, T., Nishida, N., Ueshima, K., Morita, M., Chishina, H., Takita, M., Hagiwara, S., Ida, H., Minami, Y., Yamada, A., et al. (2021) · Liver Cancer · doi:10.1159/000518048 · Cited by 63
Obesity Modifies the Performance of Fibrosis Biomarkers in Nonalcoholic Fatty Liver Disease
Qadri, S. U., Ahlholm, N., Lønsmann, I., Pellegrini, P., Poikola, A., Luukkonen, P. K., Porthan, K., Juuti, A., Sammalkorpi, H. E., Penttilä, A. K., et al. (2021) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgab933 · Cited by 63
Circulating TREM2 as a noninvasive diagnostic biomarker for NASH in patients with elevated liver stiffness
Chandran, V. I., Wernberg, C. W., Lauridsen, M. M., Skytthe, M. K., Bendixen, S. M., Larsen, F. T., Hansen, C. D., Grønkjær, L. L., Siersbæk, M. S., Caterino, T. D., et al. (2022) · Hepatology · doi:10.1002/hep.32620 · Cited by 64
“We then compared the diagnostic accuracy of different classifications of NASH (NAS > 4, at‐risk NASH, and strict NASH) to other noninvasive test markers involved in NAFLD diagnosis such as FibroScan‐aspartate aminotransferase (FAST) score,[26] Fibrosis‐4 (FIB‐4),[27] Forns index,[28] aspartate aminotransferase (AST)/a…”
Method
Steatotic Liver Disease: Metabolic Dysfunction, Alcohol, or Both?
Staufer, K., & Stauber, R. E. (2023) · Biomedicines · doi:10.3390/biomedicines11082108 · Cited by 63
“NAFLD fibrosis score (NFS), using a combination of the parameters of age, fasting glucose, body mass index (BMI), platelet count, albumin, and AST/ALT ratio [66], as well as fibrosis-4 index (FIB-4), including age, AST, ALT, and platelet count [67], are among the most widely used noninvasive tests.”
Method
Prognostic performance of the two-step clinical care pathway in metabolic dysfunction-associated steatotic liver disease
Yip, T. C., Lee, H. W., Lin, H., Tsochatzis, E. A., Petta, S., Bugianesi, E., Yoneda, M., Zheng, M., Hagström, H., Boursier, J., et al. (2025) · Journal of Hepatology · doi:10.1016/j.jhep.2025.01.014 · Cited by 63
Combination HBV therapy is linked to greater HBV DNA suppression in a cohort of lamivudine-experienced HIV/HBV coinfected individuals
Matthews, G. V., Seaberg, E. C., Dore, G. J., Bowden, S., Lewin, S. R., Sasadeusz, J. J., Marks, P., Goodman, Z. D., Philp, F. H., Tang, Y., et al. (2009) · AIDS · doi:10.1097/qad.0b013e32832b43f2 · Cited by 63
“Two methods of noninvasive fibrosis assessment using serum biochemical algorithms, the AST to platelet ration index (APRI) score [15] and FIB4 score [16], were calculated on all patients.”
Method
Mean platelet volume is increased in chronic hepatitis C patients with advanced fibrosis
Pürnak, T., Ölmez, Ş., Torun, S., Efe, C., Sayılır, A., Özaslan, E., Tenlik, İ., Kalkan, İ. H., Beyazıt, Y., & Yüksel, O. (2012) · Clinics and Research in Hepatology and Gastroenterology · doi:10.1016/j.clinre.2012.03.035 · Cited by 63
Assessment of Intestinal Failure Associated Liver Disease according to different diagnostic criteria
Sasdelli, A. S., Agostini, F., Pazzeschi, C., Guidetti, M., Lal, S., & Pironi, L. (2018) · Clinical Nutrition · doi:10.1016/j.clnu.2018.04.019 · Cited by 63
Liver elastography, comments on EFSUMB elastography guidelines 2013
Cui, X. (2013) · World Journal of Gastroenterology · doi:10.3748/wjg.v19.i38.6329 · Cited by 62
An elevated FIB-4 score predicts liver cancer development: A longitudinal analysis from 29,999 patients with NAFLD
Loosen, S. H., Kostev, K., Keitel, V., Tacke, F., Roderburg, C., & Luedde, T. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2021.08.030 · Cited by 62
Updated recommendations for the management of metabolic dysfunction–associated steatotic liver disease (MASLD) by the Latin American working group
Díaz, L. A., Arab, J. P., Idalsoaga, F. J., Perelli, J., Vega, J. A., Dirchwolf, M., Carreño, J., Samith, B., Valério, C. M., Moreira, R. O., et al. (2025) · Annals of Hepatology · doi:10.1016/j.aohep.2025.101903 · Cited by 72
“The FIB-4 score, which combines age, AST, ALT, and platelet count, is one of the most widely used NITs to estimate liver ﬁ brosis [84].”
Assessment of fibrosis in chronic liver diseases
Zhou, K., & Lu, L. (2009) · Journal of Digestive Diseases · doi:10.1111/j.1751-2980.2008.00356.x · Cited by 62
Serial measurement of Wisteria floribunda agglutinin positive Mac-2-binding protein is useful for predicting liver fibrosis and the development of hepatocellular carcinoma in chronic hepatitis C patients treated with IFN-based and IFN-free therapy
The Ochanomizu Liver Conference Study Group, Nagata, H., Nakagawa, M., Nishimura‐Sakurai, Y., Asano, Y., Tsunoda, T., Miyoshi, M., Kaneko, S., Goto, F., Otani, S., et al. (2016) · Hepatology International · doi:10.1007/s12072-016-9754-1 · Cited by 62
“A fibrosis 4 (Fib-4) index and aspartate aminotransferase (AST)-to-platelet ratio index (APRI) were also calculated as reported before [11, 12].”
Method
New Concepts on Pathogenesis and Diagnosis of Liver Fibrosis; A Review Article
Ebrahimi, H., Naderian, M., & Sohrabpour, A. A. (2016) · Middle East Journal of Digestive Diseases · doi:10.15171/mejdd.2016.29 · Cited by 61
Molecular profiling of subclinical inflammatory lesions in long-term surviving adult liver transplant recipients
Londoño, M., Souza, L. N., Lozano, J. J., Miquel, R., Abraldeṣ, J. G., Llovet, L., Quaglia, A., Rimola, A., Navasa, M., & Fueyo, A. S. (2018) · Journal of Hepatology · doi:10.1016/j.jhep.2018.04.012 · Cited by 62
“Indirect fibrosis scores (APRI and FIB4) were calculated using the standard formulas at the time of inclusion and at the last follow-up [12,13].”
Method
Real life Egyptian experience of efficacy and safety of Simeprevir/Sofosbuvir therapy in 6211 chronic HCV genotype IV infected patients
Eletreby, R., Elakel, W., Said, M., El‐Kassas, M., Seif, S. M., Elbaz, T. M., Raziky, M. E., Rehim, S. A., Zaky, S., Fouad, R., et al. (2016) · Liver International · doi:10.1111/liv.13266 · Cited by 61
Performance of non-invasive fibrosis scores in non-alcoholic fatty liver disease with and without morbid obesity
Drolz, A., Wolter, S., Wehmeyer, M. H., Piecha, F., Horvatits, T., Wiesch, J. S. Z., Lohse, A. W., Mann, O., & Kluwe, J. (2021) · International Journal of Obesity · doi:10.1038/s41366-021-00881-8 · Cited by 61
Noninvasive serum biomarkers for liver fibrosis in NAFLD: current and future
Reinson, T., Buchanan, R. M., & Byrne, C. D. (2022) · Clinical and Molecular Hepatology · doi:10.3350/cmh.2022.0348 · Cited by 69
Association of Visceral Fat Obesity, Sarcopenia, and Myosteatosis with Non-Alcoholic Fatty Liver Disease without Obesity
Kim, H., Bae, S., Lee, M. J., Kim, E. H., Park, H., Kim, H. S., Cho, Y. K., Jung, C. H., Lee, W. J., & Choe, J. (2023) · Clinical and Molecular Hepatology · doi:10.3350/cmh.2023.0035 · Cited by 63
“good diagnostic performance for detecting significant liver fibrosis (26).”
Background
Racial and ethnic differences and the role of unfavorable social determinants of health across steatotic liver disease subtypes in the United States
Ochoa‐Allemant, P., Marrero, J. A., & Serper, M. (2023) · Hepatology Communications · doi:10.1097/hc9.0000000000000324 · Cited by 62
“[24] We also obtained the fibrosis-4 score and NAFLD fibrosis score as described, [25,26] considering the optimized cutoffs for patients aged ≥ 65 years.”
Method
Lipid-based insulin-resistance markers predict cardiovascular events in metabolic dysfunction associated steatotic liver disease
Colantoni, A., Bucci, T., Cocomello, N., Angelico, F., Ettorre, E., Pastori, D., Lip, G. Y. H., Ben, M. D., & Baratta, F. (2024) · Cardiovascular Diabetology · doi:10.1186/s12933-024-02263-6 · Cited by 65
“The study protocol has been previously described elsewhere [25].”
Method
KASL clinical practice guidelines for noninvasive tests to assess liver fibrosis in chronic liver disease
Kim, M. N., Han, J. W., An, J., Kim, B. K., Jin, Y., Kim, S., Lee, M., Lee, H. A., Cho, Y., Kim, H. Y., et al. (2024) · Clinical and Molecular Hepatology · doi:10.3350/cmh.2024.0506 · Cited by 65
Management of chronic hepatitis B infection
Sundaram, V., & Kowdley, K. V. (2015) · BMJ · doi:10.1136/bmj.h4263 · Cited by 61
FibroScan used in street‐based outreach for drug users is useful for hepatitis C virus screening and management: a prospective study
Foucher, J., Reiller, B., Jullien, V., Léal, F., Cesare, E. S. D., Merrouche, W., Delile, J., & de Lédinghen, V. (2009) · Journal of Viral Hepatitis · doi:10.1111/j.1365-2893.2008.01050.x · Cited by 61
Prevalence and predictors of liver steatosis and fibrosis in unselected patients with HIV mono-infection
Lombardi, R., Sambatakou, H., Mariolis, I., Cokkinos, D. D., Papatheodoridis, G., & Tsochatzis, E. A. (2016) · Digestive and Liver Disease · doi:10.1016/j.dld.2016.08.117 · Cited by 61
DOT-C: A cluster randomised feasibility trial evaluating d irectly o bserved an t i-H C V therapy in a population receiving opioid substitute therapy from community pharmacy
Radley, A., Tait, J., & Dillon, J. F. (2017) · International Journal of Drug Policy · doi:10.1016/j.drugpo.2017.05.042 · Cited by 62
Multimorbidity and polypharmacy in diabetic patients with NAFLD
Patel, P. J., Hayward, K. L., Rudra, R., Horsfall, L. U., Hossain, F., Williams, S., Johnson, T., Brown, N. N., Saad, N., Clouston, A. D., et al. (2017) · Medicine · doi:10.1097/md.0000000000006761 · Cited by 61
“Patients were eligible to be included in the study if they had a diagnosis of type 2 diabetes defined using standard criteria,[17] NAFLD, and an indeterminate or high score on the FIB4[18]http://gihep.com/calculators/hepatology/fibrosis-4-score/) or NAFLD fibrosis scores[19] (http://www.nafldscore.com/).”
Background
Patient-Reported Symptoms Over 48 Weeks Among Participants in Randomized, Double-Blind, Phase III Non-inferiority Trials of Adults with HIV on Co-formulated Bictegravir, Emtricitabine, and Tenofovir Alafenamide versus Co-formulated Abacavir, Dolutegravir, and Lamivudine
Wohl, D. A., Clarke, A. E., Maggiolo, F., Garner, W., Laouri, M., Martin, H., & Quirk, E. K. (2018) · Patient · doi:10.1007/s40271-018-0322-8 · Cited by 61
“The FIB-4 score, computed using age, platelet count, and aspartate and alanine transaminase values, provides an estimate of the degree of liver fibrosis in HIV and hepatitis C virus co-infected patients [29].”
Method
Higher mortality among lean patients with non-alcoholic fatty liver disease despite fewer metabolic comorbidities
Wijarnpreecha, K., Li, F., Lundin, S. K., Suresh, D., Song, M. W., Tao, C., Chen, V. L., & Lok, A. S. F. (2023) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.17424 · Cited by 61
Magnetic resonance elastography plus Fibrosis‐4 versus FibroScan–aspartate aminotransferase in detection of candidates for pharmacological treatment of NASH‐related fibrosis
Tamaki, N., Imajo, K., Sharpton, S. R., Jung, J., Kawamura, N., Yoneda, M., Valasek, M. A., Behling, C. A., Sirlin, C. B., Nakajima, A., et al. (2021) · Hepatology · doi:10.1002/hep.32145 · Cited by 60
Noninvasive assessment of liver fibrosis and its clinical significance in nonalcoholic fatty liver disease
Tamaki, N., Kurosaki, M., Huang, D. Q., & Loomba, R. S. (2022) · Hepatology Research · doi:10.1111/hepr.13764 · Cited by 62
“FIB‐4 is composed of age, aspartate aminotransferase (AST), alanine aminotransferase (ALT), and platelets.(16) NFS is composed of age, body mass index (BMI), impaired fasting glucose/diabetes, AST, ALT, platelets, and albumin.”
Background
The Accuracy of Noninvasive Methods in Predicting the Development of Hepatocellular Carcinoma and Hepatic Decompensation in Patients With Chronic Hepatitis B
Chon, Y. E., Jung, E. S., Park, J. Y., Kim, D. Y., Ahn, S. H., Han, K., Chon, C. Y., Jung, K. S., & Kim, S. U. (2012) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e31825079f1 · Cited by 60
Late diagnosis of hepatitis C virus infection in the Chronic Hepatitis Cohort Study (CHeCS): Missed opportunities for intervention
Moorman, A. C., Xing, J., Ko, S. C., Rupp, L. B., Xu, F., Gordon, S. C., Lü, M., Spradling, P. R., Teshale, E. H., Boscarino, J. A., et al. (2014) · Hepatology · doi:10.1002/hep.27365 · Cited by 60
Liver fibrosis: the 2017 state of art
Caviglia, G. P., Rosso, C., Fagoonee, S., Saracco, G. M., & Pellicano, R. (2017) · Panminerva Medica · doi:10.23736/s0031-0808.17.03359-6 · Cited by 62
Transient Elastography (FibroScan) Performs Better Than Non-Invasive Markers in Assessing Liver Fibrosis and Cirrhosis in Autoimmune Hepatitis Patients
Guo, L., Zheng, L., Hu, L., Zhou, H., Yu, L., & Liang, W. (2017) · Medical Science Monitor · doi:10.12659/msm.907300 · Cited by 60
“These non-invasive markers can detect cirrhosis in chronic viral hepatitis and nonalcoholic fatty liver disease (NAFLD) [14,15]; however, their ability to detect the early liver fibrosis stages and cirrhosis of AIH patients is still uncertain.”
Background
Serum autotaxin levels are correlated with hepatic fibrosis and ballooning in patients with non-alcoholic fatty liver disease
Fujimori, N., Umemura, T., Kimura, T., Tanaka, N., Sugiura, A., Yamazaki, T., Joshita, S., Komatsu, M., Usami, Y., Sano, K., et al. (2018) · World Journal of Gastroenterology · doi:10.3748/wjg.v24.i11.1239 · Cited by 61
Incidence, aetiology and related comorbidities of cirrhosis: a Swedish population-based cohort study
Vaz, J., Eriksson, B., Strömberg, U., Buchebner, D., & Midlöv, P. (2020) · BMC Gastroenterology · doi:10.1186/s12876-020-01239-6 · Cited by 59
A risk prediction model for hepatocellular carcinoma after hepatitis B surface antigen seroclearance
Yang, H., Bae, S. H., Nam, H., Lee, H. L., Lee, S. W., Yoo, S. H., Song, M. J., Kwon, J. H., Nam, S. W., Choi, J. Y., et al. (2022) · Journal of Hepatology · doi:10.1016/j.jhep.2022.03.032 · Cited by 59
Effect of dapagliflozin on liver and pancreatic fat in patients with type 2 diabetes and non-alcoholic fatty liver disease
Shi, M., Zhang, H., Wang, W., Zhang, X., Liu, J., Wang, Q., Wang, Y., Zhang, C., Guo, X., Qiao, Q., et al. (2023) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2023.108610 · Cited by 65
Use of transient elastography (FibroScan®) for the noninvasive assessment of portal hypertension in HIV/HCV-coinfected patients
Sánchez‐Conde, M., Miralles, P., Bellón, J. M., Rincón, D., Ramírez, M., Gutiérrez, I., Ripoll, C., López, J. C., Cosín, J., Clemente, G., et al. (2010) · Journal of Viral Hepatitis · doi:10.1111/j.1365-2893.2010.01371.x · Cited by 59
Noninvasive Measurements Predict Liver Fibrosis Well in Hepatitis C Virus Patients After Direct-Acting Antiviral Therapy
Huang, R., Rao, H., Yang, M., Gao, Y., Wang, J., Jin, Q., Ma, D., & Wei, L. (2019) · Digestive Diseases and Sciences · doi:10.1007/s10620-019-05886-y · Cited by 59
Machine Learning Prediction of Liver Stiffness Using Clinical and T2-Weighted MRI Radiomic Data
He, L., Li, H., Dudley, J. A., Maloney, T., Brady, S. L., Somasundaram, E., Trout, A. T., & Dillman, J. R. (2019) · American Journal of Roentgenology · doi:10.2214/ajr.19.21082 · Cited by 58
Nonalcoholic Fatty Liver Disease in Patients with Type 2 Diabetes: Screening, Diagnosis, and Treatment
Ciardullo, S., Vergani, M., & Perseghin, G. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12175597 · Cited by 63
“The most validated and applied are the FIB-4 [37] (based on AST, ALT, age, and platelet count) and the NAFLD Fibrosis Score [38] (NFS, based on AST, ALT, age, platelet count, BMI, and diabetes/impaired glucose tolerance).”
MethodInfluential
Epidemiology and diagnosis of metabolic dysfunction-associated fatty liver disease
Fouad, Y. M., Alboraie, M. A. A., & Shiha, G. E.-S. (2024) · Hepatology International · doi:10.1007/s12072-024-10704-3 · Cited by 58
MAFLD Criteria Guide the Subtyping of Patients with Fatty Liver Disease
Huang, J., Ou, W., Wang, M.-F., Singh, M., Liu, Y., Liu, S., Wu, Y., Zhu, Y., Kumar, R., & Lin, S. (2021) · Risk Management and Healthcare Policy · doi:10.2147/rmhp.s285880 · Cited by 58
Change in serial liver stiffness measurement by magnetic resonance elastography and outcomes in NAFLD
Gidener, T., Dierkhising, R. A., Mara, K. C., Therneau, T. M., Venkatesh, S. K., Ehman, R. L., Yin, M., & Allen, A. M. (2023) · Hepatology · doi:10.1002/hep.32594 · Cited by 62
“FIB‐4 index was calculated as age (years) × AST (U/L)/(platelets [109/L] ×ALT1/2 [U/L]).[10] Cirrhosis was defined by the presence histologic evidence of stage 4 fibrosis on biopsy or cirrhotic morphology on imaging (surface nodularity, hypertrophy of the caudate lobe hypertrophy, right lobe atrophy) with evidence of…”
Method
Clinicopathological characteristics and diagnostic performance of Wisteria floribunda agglutinin positive Mac-2-binding protein as a preoperative serum marker of liver fibrosis in hepatocellular carcinoma
The Hepatitis Glyco-biomarker Study Group, Fujiyoshi, M., Kuno, A., Gotoh, M., Fukai, M., Yokoo, H., Kamachi, H., Kamiyama, T., Korenaga, M., Mizokami, M., et al. (2015) · Journal of Gastroenterology · doi:10.1007/s00535-015-1063-2 · Cited by 57
“FIB4 indices were calculated as follows: FIB4 index = age 9 AST level/[platelet count 9 (ALT level)] [20].”
Method
The risks of hepatocellular carcinoma development after HCV eradication are similar between patients treated with peg-interferon plus ribavirin and direct-acting antiviral therapy
Nagaoki, Y., Imamura, M., Aikata, H., Daijo, K., Teraoka, Y., Honda, F., Nakamura, Y., Hatooka, M., Morio, R., Morio, K., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0182710 · Cited by 57
Strengths and Limitations of the Veterans Aging Cohort Study Index as a Measure of Physiologic Frailty
Justice, A. C., & Tate, J. P. (2019) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2019.0136 · Cited by 58
Magnetic resonance elastography for prediction of long‐term progression and outcome in chronic liver disease: A retrospective study
Gidener, T., Yin, M., Dierkhising, R., Allen, A. M., Ehman, R. L., & Venkatesh, S. K. (2021) · Hepatology · doi:10.1002/hep.32151 · Cited by 59
A laboratory marker, FIB-4 index, as a predictor for long-term outcomes of hepatocellular carcinoma patients after curative hepatic resection
Toyoda, H., Kumada, T., Tada, T., Kaneoka, Y., & Maeda, A. (2015) · Surgery · doi:10.1016/j.surg.2014.10.022 · Cited by 57
Prevalence of hepatitis B and C viruses in HIV‐positive patients in China: a cross‐sectional study
Xie, J., Han, Y., Qiu, Z., Li, Y., Li, Y., Song, X., Wang, H., Thio, C. L., & Li, T. (2016) · Journal of the International AIDS Society · doi:10.7448/ias.19.1.20659 · Cited by 57
Non‐invasive fibrosis score for hepatitis delta
Lutterkort, G. L., Wranke, A., Yurdaydın, C., Budde, E., Westphal, M., Lichtinghagen, R., Stift, J., Bremer, B., Hardtke, S., Keskın, O., et al. (2016) · Liver International · doi:10.1111/liv.13205 · Cited by 57
Noninvasive markers for staging fibrosis in chronic delta hepatitis
Takyar, V. K., Surana, P., Kleiner, D. E., Wilkins, K. J., Hoofnagle, J. H., Liang, T. J., Heller, T., & Koh, C. (2016) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.13834 · Cited by 57
Improvement of Liver Fibrosis after Long-Term Antiviral Therapy Assessed by Fibroscan in Chronic Hepatitis B Patients With Advanced Fibrosis
Chon, Y. E., Park, J. Y., Myoung, S.-M., Jung, K. S., Kim, B. K., Kim, S. U., Kim, D. Y., Ahn, S. H., & Han, K. (2017) · The American Journal of Gastroenterology · doi:10.1038/ajg.2017.93 · Cited by 57
Application of the combined FibroMeter vibration‐controlled transient elastography algorithm in Chinese patients with non‐alcoholic fatty liver disease
Loong, T. C., Wei, J. L., Leung, J. C., Wong, G. L., Shu, S. S., Chim, A. M., Chan, A. W. H., Choi, P. C., Tse, Y., Chan, H. L., et al. (2016) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.13671 · Cited by 57
Tumor Fibroblast Growth Factor Receptor 4 Level Predicts the Efficacy of Lenvatinib in Patients With Advanced Hepatocellular Carcinoma
Yamauchi, M., Ono, A., Ishikawa, A., Kodama, K., Uchikawa, S., Hatooka, H., Zhang, P., Teraoka, Y., Morio, K., Fujino, H., et al. (2020) · Clinical and Translational Gastroenterology · doi:10.14309/ctg.0000000000000179 · Cited by 57
“The fibrosis-4 index of each case was calculated by using the formula (17): (age [years]3 aspartate aminotransferase [U/L])/([PLT (10(9)/L)]3 [alanine aminotransferase (U/L)]).”
Method
Liver stiffness by magnetic resonance elastography is associated with increased risk of cardiovascular disease in patients with non‐alcoholic fatty liver disease
Park, J. G., Jung, J., Verma, K. K., Kang, M. K., Madamba, E. V., Lopez, S. J., Yonan, A. Q., Liu, A. Y., Bettencourt, R., Sirlin, C. B., et al. (2021) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.16324 · Cited by 57
Direct and Indirect Effects of Heavy Alcohol Use on Clinical Outcomes in a Longitudinal Study of HIV Patients on ART
Kahler, C. W., Liu, T., Cioe, P. A., Bryant, V., Pinkston, M. M., Kojic, E. M., Onen, N., Baker, J. V., Hammer, J., Brooks, J. T., et al. (2017) · AIDS and Behavior · doi:10.1007/s10461-016-1474-y · Cited by 56
“Non-HIV biomarkers included indices of liver fibrosis, kidney function, and hemoglobin: We used FIB-4 to estimate the extent of liver fibrosis; FIB-4 incorporates aspartate aminotransferase, alanine aminotransferase, platelets, and age, and has both high negative and positive predictive values for the presence of adva…”
Method
CHI3L1 in the pathophysiology and diagnosis of liver diseases
Wang, S., Hu, M., Qian, Y.-S., Jiang, Z., Shen, L., Fu, L., & Hu, Y. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110680 · Cited by 57
Favorable effect of sodium–glucose cotransporter 2 inhibitor, dapagliflozin, on non‐alcoholic fatty liver disease compared with pioglitazone
Cho, K. Y., Nakamura, A., Omori, K., Takase, T., Miya, A., Yamamoto, K., Nomoto, H., Kameda, H., Taneda, S., Kurihara, Y., et al. (2020) · Journal of Diabetes Investigation · doi:10.1111/jdi.13457 · Cited by 58
Diabetes and metabolic dysfunction-associated fatty liver disease
Davis, T. M. E. (2021) · Metabolism · doi:10.1016/j.metabol.2021.154868 · Cited by 60
Distribution of FIB-4 index in the general population: analysis of 75,666 residents who underwent health checkups
Sugiyama, A., Kurisu, A., Bunthen, E., Ouoba, S., Ko, K., Rakhimov, A., Akita, T., Harakawa, T., Sako, T., Koshiyama, M., et al. (2022) · BMC Gastroenterology · doi:10.1186/s12876-022-02290-1 · Cited by 56
“FIB-4 index was principally developed by analyzing patients with an average age of 40 ± 7 years [12].”
Method
A Systematic Review of Metabolic Syndrome: Key Correlated Pathologies and Non-Invasive Diagnostic Approaches
Giangregorio, F., Mosconi, E., Debellis, M. G., Provini, S., Esposito, C., Garolfi, M., Oraka, S., KALOUDI, O., Mustafazade, G., Marín‐Baselga, R., et al. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13195880 · Cited by 67
“FIB-4 index is also associated with all-cause mortality of systemic chronic diseases such as rheumatoid arthritis [262], microscopic polyangiitis, granulo-matosis with polyangiitis [263], and chronic obstructive pulmonary disease [264].”
Background
Progression of Liver Fibrosis in HIV/HCV Co-Infection: A Comparison between Non-Invasive Assessment Methods and Liver Biopsy
Schmid, P., Bregenzer, A., Huber, M., Rauch, A., Jochum, W., Müllhaupt, B., Vernazza, P., Opravil, M., Weber, R. K., & Study, S. H. C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0138838 · Cited by 56
“45 (<F3) Standard [17] 100 (14/ 14) 55.”
Influential
Evaluation of seven noninvasive models in staging liver fibrosis in patients with chronic hepatitis B virus infection
Ma, J., Jiang, Y., & Gong, G. (2013) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0b013e32835cb5dd · Cited by 56
New noninvasive index for predicting liver fibrosis in Asian patients with chronic viral hepatitis
Wang, H., Peng, C., Lai, H., Su, W., Lin, C., Chuang, P., Chen, S., Chen, C., Hsu, W., & Huang, G. (2017) · Scientific Reports · doi:10.1038/s41598-017-03589-w · Cited by 56
Loss of Life Expectancy by 10 Years or More From Elevated Aspartate Aminotransferase: Finding Aspartate Aminotransferase a Better Mortality Predictor for All-Cause and Liver-Related than Alanine Aminotransferase
Xie, K., Chen, C.-H., Tsai, S.-P., Lu, P. J., Wu, H. M., Zeng, Y., Ye, Y., Tu, H., Wen, C., Huang, M., et al. (2019) · The American Journal of Gastroenterology · doi:10.14309/ajg.0000000000000332 · Cited by 56
Exploratory Analysis of Lenvatinib Therapy in Patients with Unresectable Hepatocellular Carcinoma Who Have Failed Prior PD−1/PD-L1 Checkpoint Blockade
Aoki, T., Kudo, M., Ueshima, K., Morita, M., Chishina, H., Takita, M., Hagiwara, S., Ida, H., Minami, Y., Tsurusaki, M., et al. (2020) · Cancers · doi:10.3390/cancers12103048 · Cited by 55
“HCV, hepatitis C virus; HBV, hepatitis B virus; NBNC, HBV and HCV negative; BCLC, Barcelona Clinic Liver Cancer; ALBI grade, albumin-bilirubin grade; FIB4, The fibrosis-4 (FIB-4) index was calculated as age (year) × AST (IU/L) / (platelet count (109/L) × √ALT (IU/L)) [38]; AST, aspartate aminotransferase; ALT, alanine…”
Non-Obese MAFLD Is Associated with Colorectal Adenoma in Health Check Examinees: A Multicenter Retrospective Study
Fukunaga, S., Nakano, D., Kawaguchi, T., Eslam, M., Ouchi, A., Nagata, T., Kuroki, H., Kawata, H., Hirohiko, A. B. E., Nouno, R., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115462 · Cited by 56
“FIB-4 index was calculated using age, serum levels of AST, ALT, and platelet count as previously described [39].”
Method
Noninvasive Assessment of Fibrosis in Patients with Nonalcoholic Fatty Liver Disease
Buzzetti, E., Lombardi, R., Luca, L. D., & Tsochatzis, E. A. (2015) · International Journal of Endocrinology · doi:10.1155/2015/343828 · Cited by 56
Clinical care pathway to detect advanced liver disease in patients with type 2 diabetes through automated fibrosis score calculation and electronic reminder messages: a randomised controlled trial
Zhang, X., Yip, T. C.-F., Wong, G. L.-H., Leow, W.-X., Liang, L. Y., Lim, L.-L., Li, G., Ibrahim, L., Lin, H., Lai, J. C. T., et al. (2023) · Gut · doi:10.1136/gutjnl-2023-330269 · Cited by 55
Transient versus two-dimensional shear-wave elastography in a multistep strategy to detect advanced fibrosis in NAFLD
Cassinotto, C., Boursier, J., Paisant, A., Guiu, B., Irles‐Depe, M., Canivet, C., Aube, C., & de Ledinghen, V. (2021) · Hepatology · doi:10.1002/hep.31655 · Cited by 55
Antiretroviral Therapy Reduces the Rate of Hepatic Decompensation Among HIV- and Hepatitis C Virus–Coinfected Veterans
ANDERSON, J. P., Tchetgen, E. J. T., Re, V. L., Tate, J. P., Williams, P. L., Seage, G. R., Horsburgh, C. R., Lim, J. K., Goetz, M. B., Rimland, D., et al. (2013) · Clinical Infectious Diseases · doi:10.1093/cid/cit779 · Cited by 55
“and categorized as described by Sterling et al [30].”
Method
Inherited non-alcoholic fatty liver disease and dyslipidemia due to monoallelic ABHD5 mutations
Youssefian, L., Vahidnezhad, H., Saeidian, A. H., Pajouhanfar‎, S., Sotoudeh, S., Mansouri, P., Amirkashani, D., Zeinali, S., Levine, M. A., Peris, K., et al. (2019) · Journal of Hepatology · doi:10.1016/j.jhep.2019.03.026 · Cited by 55
Non-invasive tests of non-alcoholic fatty liver disease
Li, G., Zhang, X., Lin, H., Liang, L. Y., Wong, G. L., & Wong, V. W. (2022) · Chinese Medical Journal · doi:10.1097/cm9.0000000000002027 · Cited by 56
“FIB-4 consists of age, AST, ALT, and platelet count and was developed in CHC/human immunodeficiency virus (HIV) coinfected patients.([65]) A recent meta-analysis (based on 64 studies in 13,046 NAFLD patients) reported that FIB-4 had AUROC of 0.”
Background
Fontan‐associated liver disease
Hilscher, M. B., Wells, M. L., Venkatesh, S. K., Cetta, F., & Kamath, P. S. (2022) · Hepatology · doi:10.1002/hep.32406 · Cited by 55
Accuracy of Noninvasive Scoring Systems in Assessing Liver Fibrosis in Patients with Nonalcoholic Fatty Liver Disease: A Systematic Review and Meta-Analysis
Han, S., Choi, M., Lee, B., Lee, H. W., Kang, S. H., Cho, Y., Ahn, S. B., Song, D. S., Jun, D. W., Lee, J.-E., et al. (2022) · Gut and Liver · doi:10.5009/gnl210391 · Cited by 55
“First, the biggest limitation of this study is that it lacks new information compared to the existing meta-analysis related to FIB-4 or NFS.”
BackgroundMethodInfluential
The Association Between Proton Pump Inhibitor Exposure and Key Liver-Related Outcomes in Patients With Cirrhosis: A Veterans Affairs Cohort Study
Mahmud, N., Serper, M., Taddei, T. H., & Kaplan, D. E. (2022) · Gastroenterology · doi:10.1053/j.gastro.2022.03.052 · Cited by 55
Association between Noninvasive Fibrosis Markers and Chronic Kidney Disease among Adults with Nonalcoholic Fatty Liver Disease
Sesti, G., Fiorentino, T., Arturi, F., Perticone, M., Sciacqua, A., & Perticone, F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088569 · Cited by 60
“problems, several noninvasive scoring indexes have been developed by combining clinical and biochemical parameters that are useful to categorize subjects with NAFLD in subgroups at low and high risk of advanced fibrosis [33–37].”
Background
Comparison of non-invasive assessment to diagnose liver fibrosis in chronic hepatitis B and C patients
Stibbe, K. J. M., Verveer, C., Francke, J., Hansen, B. E., Zondervan, P. E., Kuipers, E. J., de Knegt, R. J., & van Vuuren, A. J. (2011) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365521.2011.574725 · Cited by 55
“Fib-4 was measured in the serum of all patients as follows: age(years) [AST(U/L)/platelets (10(9)/L) HALT(U/L)] [19].”
Method
Validation and comparison of simple noninvasive models for the prediction of liver fibrosis in chronic hepatitis C
Amorim, T. G. F., Staub, G. J., Lazzarotto, C., Silva, A. P., Manes, J., Ferronato, M. D. G., Shiozawa, M. B. C., Narciso-Schiavon, J. L., Dantas-Corrêa, E. B., & Schiavon, L. D. L. (2012) · Annals of Hepatology · doi:10.1016/s1665-2681(19)31410-3 · Cited by 55
The serum proteome of nonalcoholic fatty liver disease: A multimodal approach to discovery of biomarkers of nonalcoholic steatohepatitis
Miller, M. H., Walsh, S. V., Atrih, A., Huang, J. T.-J., Ferguson, M. A. J., & Dillon, J. F. (2014) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.12614 · Cited by 55
Transient elastography for the detection of hepatic fibrosis in HIV-monoinfected adults with elevated aminotransferases on antiretroviral therapy
Morse, C. G., McLaughlin, M. E., Proschan, M. A., Koh, C., Kleiner, D. E., Heller, T., & Kovacs, J. A. (2015) · AIDS · doi:10.1097/qad.0000000000000841 · Cited by 55
“The AST/platelet ratio index (APRI) [12], fibrosis-4 (FIB-4) [13], and non-alcoholic fatty liver disease fibrosis score (NAFLD-FS) [14] indices were calculated as noninvasive markers of fibrosis, using laboratory and clinical parameters at the time of study enrollment.”
MethodInfluential
Prospects in non-invasive assessment of liver fibrosis: Liquid biopsy as the future gold standard?
Lambrecht, J., Verhulst, S., Mannaerts, I., Reynaert, H., & van Grunsven, L. A. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.01.009 · Cited by 56
Overview of the Pathogenesis, Genetic, and Non-Invasive Clinical, Biochemical, and Scoring Methods in the Assessment of NAFLD
Kupčová, V., Fedelešová, M., Bulas, J., Kozmonová, P., & Turecký, L. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16193570 · Cited by 53
Direct comparison of the specialised blood fibrosis tests FibroMeterV2G and Enhanced Liver Fibrosis score in patients with non‐alcoholic fatty liver disease from tertiary care centres
Guillaume, M., Moal, V., Delabaudière, C., Zuberbuhler, F., Robic, M., Lannes, A., Métivier, S., Oberti, F., Gourdy, P., Fouchard‐Hubert, I., et al. (2019) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.15529 · Cited by 55
Effects of Metformin Exposure on Survival in a Large National Cohort of Patients With Diabetes and Cirrhosis
Kaplan, D. E., Serper, M., John, B. V., Tessiatore, K. M., Lerer, R., Mehta, R., Fox, R., Aytaman, A., Baytarian, M., Hunt, K., et al. (2021) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2020.08.026 · Cited by 41
Comparative effectiveness of the hepatitis C virus protease inhibitors boceprevir and telaprevir in a large U.S. cohort
Backus, L. I., Belperio, P. S., Shahoumian, T. A., Cheung, R. C., & Mole, L. A. (2013) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.12546 · Cited by 54
Retreatment efficacy and predictors of ledipasvir plus sofosbuvir to HCV genotype 1 in Japan
Akuta, N., Sezaki, H., Suzuki, F., Fujiyama, S., Kawamura, Y., Hosaka, T., Kobayashi, M., Kobayashi, M., Saitoh, S., Suzuki, Y., et al. (2016) · Journal of Medical Virology · doi:10.1002/jmv.24617 · Cited by 54
“25 was evaluated as advanced fibrosis [Sterling et al., 2006].”
Galectin-3 is related to right ventricular dysfunction in heart failure patients with reduced ejection fraction and may affect exercise capacity
Zaborska, B., Sygitowicz, G., Smarż, K., Pilichowska‐Paszkiet, E., & Budaj, A. (2020) · Scientific Reports · doi:10.1038/s41598-020-73634-8 · Cited by 54
Substantial gaps in evaluation and treatment of patients with hepatitis B in the US
Ye, Q., Kam, L. Y., Yeo, Y. H., Dang, N. H., Huang, D. Q., Cheung, R. C., & Nguyen, M. H. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2021.08.019 · Cited by 54
Antifibrotic effect and long‐term outcome of SGLT2 inhibitors in patients with NAFLD complicated by diabetes mellitus
Arai, T., Atsukawa, M., Tsubota, A., Mikami, S., Uojima, H., Yoshikata, K., Ono, H., Kawano, T., Yoshida, Y., Tanabe, T., et al. (2022) · Hepatology Communications · doi:10.1002/hep4.2069 · Cited by 54
“The FIB- 4 index was calculated to estimate the degree of liver fibrosis, as reported previously.[21] FIB- 4 index values of <1.”
Method
Non-linear association of baseline viral load with on-treatment hepatocellular carcinoma risk in chronic hepatitis B
Choi, W., Kim, G., Choi, J., Choi, G. H., Lee, Y. B., Sinn, D. H., & Lim, Y. (2023) · Gut · doi:10.1136/gutjnl-2023-330225 · Cited by 54
Prospective head-to-head comparison of non-invasive scores for diagnosis of fibrotic MASH in patients with type 2 diabetes
Castéra, L., Garteiser, P., Laouenan, C., Vidal-Trécan, T., Vallet‐Pichard, A., Manchon, P., Paradis, V., Czernichow, S., Roulot, D. M., Larger, É., et al. (2024) · Journal of Hepatology · doi:10.1016/j.jhep.2024.03.023 · Cited by 55

Authors: Sterling, R. K., Lissen, E., Clumeck, N., Sola, R., Correa, M. C., Montaner, J., S. Sulkowski, M., Torriani, F. J., Dieterich, D. T., Thomas, D. L., Messinger, D., & Nelson, M.
Affiliations: Virginia Commonwealth University (US)
James J. Peters VA Medical Center (US)
Centre Hospitalier Universitaire de Saint-Pierre (BE)
Universitat Autònoma de Barcelona (ES)
University of British Columbia (CA)
University of California San Diego (US)
Icahn School of Medicine at Mount Sinai (US)
Johns Hopkins University (US)
Chelsea and Westminster Hospital (GB)
Corresponding author: Sterling, Richard K.
ORCID: Sterling, Richard K.
Montaner, Julio
Torriani, Francesca J.
Thomas, David L.
Nelson, Mark
Venue: Hepatology
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2006-06
Volume: 43
Issue: 6
Pages: 1317-1325
ISSN: 0270-9139 (ISSN-L)
DOI: 10.1002/hep.21178
OpenAlex: W2064387090
Cited by: 5,021
References: 48
Citations by year: 2026: 497 · 2025: 523 · 2024: 523 · 2023: 490 · 2022: 492 · 2021: 494 · 2020: 390 · 2019: 333 · 2018: 239 · 2017: 210 · 2016: 204 · 2015: 158 · 2014: 92 · 2013: 83 · 2012: 67
FWCI: 29.41
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: doi.wiley.com/10.1002/tdm_license_1.1 (tdm, 3379 d)
Locations: Hepatology (publishedVersion)
PubMed (publishedVersion)
Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion)
Funders: National Institute on Drug Abuse (R01DA016078)
National Institute of Diabetes and Digestive and Kidney Diseases (K23DK064578)
Topics: Health Sciences › Medicine › Hepatology › Liver Disease Diagnosis and Treatment
Health Sciences › Medicine › Hepatology › Liver Disease and Transplantation
Health Sciences › Medicine › Hepatology › Hepatitis C virus research
Keywords: HIV/HCV coinfection, liver fibrosis, FIB-4, liver biopsy avoidance, platelet count, transaminases, international normalized ratio, Ishak score, fibrosis staging
MeSH terms: Age Factors, Biopsy, Needle, Blood Chemical Analysis, Diagnostic Tests, Routine, Female, Humans, Immunohistochemistry, Liver Cirrhosis, Liver Function Tests, Male, Predictive Value of Tests, Probability, Prognosis, Retrospective Studies, ROC Curve, Sensitivity and Specificity, Severity of Illness Index, Sex Factors, Reproducibility of Results, Cohort Studies, HIV Infections, Logistic Models, Disease Progression, Risk Assessment, Hepatitis C, Chronic

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Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection†‡

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