Changes in Components of Metabolic Syndrome after Antiviral Eradication in Hepatitis C Virus Infection
Abstract
:1. Introduction
2. Material and Methods
2.1. Patients
2.2. Clinical and Laboratory Assessment
2.3. FibroScan® 520 Compact Model Measurements
2.4. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- World Health Organization. Global Hepatitis Report; World Health Organization: Geneva, Switzerland, 2017; Available online: https://www.who.int/hepatitis/publications/global-hepatitis-report2017/en/ (accessed on 6 July 2021).
- Chang, M.-L. Metabolic alterations and hepatitis C: From bench to bedside. World J. Gastroenterol. 2016, 22, 1461–1476. [Google Scholar] [CrossRef]
- De Andrade, V.G.; Yamashiro, F.D.S.; Oliveira, C.V.; Kurozawa, L.L.; Moreira, A.; Silva, G.F. Increase of Lipids during HCV Treatment: Virus Action or Medication? Arq. De Gastroenterol. 2018, 55, 184–187. [Google Scholar] [CrossRef] [PubMed]
- Corey, K.E.; Kane, E.; Munroe, C.; Barlow, L.L.; Zheng, H.; Chung, R.T. Hepatitis C virus infection and its clearance alter circulating lipids: Implications for long-term follow-up. Hepatology 2009, 50, 1030–1037. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Meissner, E.G.; Lee, Y.-J.; Osinusi, A.; Sims, Z.; Qin, J.; Sturdevant, D.; McHutchison, J.; Subramanian, M.; Sampson, M.; Naggie, S.; et al. Effect of sofosbuvir and ribavirin treatment on peripheral and hepatic lipid metabolism in chronic hepatitis C virus, genotype 1–infected patients. Hepatology 2015, 61, 790–801. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tarantino, G.; Conca, P.; Sorrentino, P.; Ariello, M. Metabolic factors involved in the therapeutic response of patients with hepatitis C virus-related chronic hepatitis. J. Gastroenterol. Hepatol. 2006, 21, 1266–1268. [Google Scholar] [CrossRef] [PubMed]
- Bressler, B.L.; Guindi, M.; Tomlinson, G.; Heathcote, J. High body mass index is an independent risk factor for nonresponse to antiviral treatment in chronic hepatitis C. Hepatology 2003, 38, 639–644. [Google Scholar] [CrossRef]
- Schlevogt, B.; Deterding, K.; Port, K.; Kirschner, J.; Sollik, L.; Mix, C.; Manns, M.P.; Cornberg, M.; Wedemeyer, H. Weight gain after IFN-free cure of chronic hepatitis C: A potential concern? J. Hepatol. 2016, 64, S750. [Google Scholar] [CrossRef]
- Nomura, H.; Miyagi, Y.; Tanimoto, H.; Kawano, A.; Yamashita, N. Weight Loss during Telaprevir-based Triple Therapy due to Telaprevir-induced Appetite Loss. Intern. Med. 2014, 53, 2567–2573. [Google Scholar] [CrossRef] [Green Version]
- El Kassas, M.; Alboraie, M.; Naguib, M.; Omar, H.; El Tahan, A.; Moaz, I.; Abdellah, M.; Ezzat, S.; Wifi, M.N.; Sherief, A.F.; et al. A significant upsurge of body mass index in patients with chronic hepatitis C successfully treated with direct-acting antiviral regimens. Turk. J. Gastroenterol. 2019, 30, 708–713. [Google Scholar] [CrossRef]
- Do, A.; Esserman, D.A.; Krishnan, S.; Lim, J.K.; Taddei, T.H.; Hauser, R.G.; Tate, J.P.; Re, V.L.; Justice, A.C. Excess Weight Gain After Cure of Hepatitis C Infection with Direct-Acting. J. Gen. Intern. Med. 2020, 35, 2025–2034, Erratum in J. Gen. Intern. Med. 2020, 35, 3140. [Google Scholar] [CrossRef]
- Sasso, M.; Beaugrand, M.; de Ledinghen, V.; Douvin, C.; Marcellin, P.; Poupon, R.; Sandrin, L.; Miette, V. Controlled Attenuation Parameter (CAP): A Novel VCTE™ Guided Ultrasonic Attenuation Measurement for the Evaluation of Hepatic Steatosis: Preliminary Study and Validation in a Cohort of Patients with Chronic Liver Disease from Various Causes. Ultrasound Med. Biol. 2010, 36, 1825–1835. [Google Scholar] [CrossRef] [PubMed]
- Vuppalanchi, R.; Siddiqui, M.S.; Van Natta, M.L.; Hallinan, E.; Brandman, D.; Kowdley, K.; Neuschwander-Tetri, B.A.; Loomba, R.; Dasarathy, S.; Abdelmalek, M.; et al. Performance characteristics of vibration-controlled transient elastography for evaluation of nonalcoholic fatty liver disease. Hepatology 2018, 67, 134–144. [Google Scholar] [CrossRef] [Green Version]
- Sadeghi, A.; Amiri, R.; Akbarpour, E.; Mirminachi, B.; Sharifi, A.; Merat, S. Changes in liver fibrosis in patients with chronic hepatitis C after successful direct-acting antiviral therapy. Int. J. Clin. Pract. 2021, 75, e14145. [Google Scholar] [CrossRef] [PubMed]
- Kobayashi, N.; Iijima, H.; Tada, T.; Kumada, T.; Yoshida, M.; Aoki, T.; Nishimura, T.; Nakano, C.; Takata, R.; Yoh, K.; et al. Changes in liver stiffness and steatosis among patients with hepatitis C virus infection who received direct-acting antiviral therapy and achieved sustained virological response. Eur. J. Gastroenterol. Hepatol. 2018, 30, 546–551. [Google Scholar] [CrossRef]
- Bansal, N. Prediabetes diagnosis and treatment: A review. World J. Diabetes 2015, 6, 296–303. [Google Scholar] [CrossRef] [PubMed]
- American Diabetes Association. Standards of medical care in diabetes—2014. Diabetes Care 2014, 37 (Suppl. 1), S14–S80. [Google Scholar] [CrossRef] [Green Version]
- Huang, P.L. A comprehensive definition for metabolic syndrome. Dis. Model. Mech. 2009, 2, 231–237. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karlas, T.; Petroff, D.; Sasso, M.; Fan, J.G.; Mi, Y.Q.; de Lédinghen, V.; Kumar, M.; Lupsor-Platon, M.; Han, K.H.; Cardoso, A.C.; et al. Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J. Hepatol. 2017, 66, 1022–1030. [Google Scholar] [CrossRef]
- Castéra, L.; Vergniol, J.; Foucher, J.; Le Bail, B.; Chanteloup, E.; Haaser, M.; Darriet, M.; Couzigou, P.; de Lédinghen, V. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology 2005, 128, 343–350. [Google Scholar] [CrossRef]
- Shousha, H.I.; Abdelaziz, R.A.; Azab, S.M.; Khairy, M.; Afifi, S.A.; Mehrez, M.I.; Eshra, M.A.; Abdelrahim, A.Y. Effect of treatment with direct acting antivirals on body mass index and hepatic steatosis in chronic hepatitis C. J. Med. Virol. 2018, 90, 1099–1105. [Google Scholar] [CrossRef]
- André, P.; Komurian-Pradel, F.; Deforges, S.; Perret, M.; Berland, J.L.; Sodoyer, M.; Pol, S.; Bréchot, C.; Paranhos-Baccalà, G.; Lotteau, V. Characterization of Low- and Very-Low-Density Hepatitis C Virus RNA-Containing Particles. J. Virol. 2002, 76, 7040–7048. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Meunier, J.-C.; Russell, R.S.; Engle, R.E.; Faulk, K.N.; Purcell, R.H.; Emerson, S.U. Apolipoprotein C1 Association with Hepatitis C Virus. J. Virol. 2008, 82, 9647–9656. [Google Scholar] [CrossRef] [Green Version]
- Graf, C.; Welzel, T.; Bogdanou, D.; Vermehren, J.; Beckel, A.; Bojunga, J.; Friedrich-Rust, M.; Dietz, J.; Kubesch, A.; Mondorf, A.; et al. Hepatitis C Clearance by Direct-Acting Antivirals Impacts Glucose and Lipid Homeostasis. J. Clin. Med. 2020, 9, 2702. [Google Scholar] [CrossRef]
- Shimizu, K.; Soroida, Y.; Sato, M.; Hikita, H.; Kobayashi, T.; Endo, M.; Sato, M.; Gotoh, H.; Iwai, T.; Tateishi, R.; et al. Eradication of hepatitis C virus is associated with the attenuation of steatosis as evaluated using a controlled attenuation parameter. Sci. Rep. 2018, 8, 7845. [Google Scholar] [CrossRef] [Green Version]
- Goossens, N.; Negro, F. Is genotype 3 of the hepatitis C virus the new villain? Hepatology 2014, 59, 2403–2412. [Google Scholar] [CrossRef] [PubMed]
- Townsend, K.; Meissner, E.G.; Sidharthan, S.; Sampson, M.; Remaley, A.T.; Tang, L.; Kohli, A.; Osinusi, A.; Masur, H.; Kottilil, S. Interferon-Free Treatment of Hepatitis C Virus in HIV/Hepatitis C Virus-Coinfected Subjects Results in Increased Serum Low-Density Lipoprotein Concentration. AIDS Res. Hum. Retroviruses 2016, 32, 456–462. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mauss, S.; Berger, F.; Wehmeyer, M.H.; Ingiliz, P.; Hueppe, D.; Lutz, T.; Simon, K.G.; Schewe, K.; Rockstroh, J.K.; Baumgarten, A.; et al. Effect of Antiviral Therapy for HCV on Lipid Levels. Antivir. Ther. 2017, 21, 81–88. [Google Scholar] [CrossRef]
- Singh, S.; Facciorusso, A.; Loomba, R.; Falck-Ytter, Y.T. Magnitude and Kinetics of Decrease in Liver Stiffness After Antiviral Therapy in Patients With Chronic Hepatitis C: A Systematic Review and Meta-analysis. Clin. Gastroenterol. Hepatol. 2018, 16, 27–38.e4. [Google Scholar] [CrossRef] [Green Version]
- Noureddin, M.; Khoyilar, C.; Palmer, S. MRI, CT Scan, and Ultrasound in the Diagnosis of Nonalcoholic Fatty Liver Disease. J. Clin. Gastroenterol. 2015, 49, 351–352. [Google Scholar] [CrossRef]
- Noureddin, M.; Wong, M.M.; Todo, T.; Lu, S.C.; Sanyal, A.J.; Mena, E.A. Fatty liver in hepatitis C patients post-sustained virological response with direct-acting antivirals. World J. Gastroenterol. 2018, 24, 1269–1277. [Google Scholar] [CrossRef]
- Shiratori, Y.; Imazeki, F.; Moriyama, M.; Yano, M.; Arakawa, Y.; Yokosuka, O.; Kuroki, T.; Nishiguchi, S.; Sata, M.; Yamada, G.; et al. Histologic Improvement of Fibrosis in Patients with Hepatitis C Who Have Sustained Response to Interferon Therapy. Ann. Intern. Med. 2000, 132, 517–524. [Google Scholar] [CrossRef] [PubMed]
- Trifan, A.; Stratina, E.; Rotaru, A.; Stafie, R.; Zenovia, S.; Nastasa, R.; Huiban, L.; Sfarti, C.; Cojocariu, C.; Cuciureanu, T.; et al. Changes in Liver Steatosis Using Controlled Attenuation Parameter among Patients with Chronic Hepatitis C Infection Treated with Direct-Acting Antivirals Therapy Who Achieved Sustained Virological Response. Diagnostics 2022, 12, 702. [Google Scholar] [CrossRef] [PubMed]
- Morales, A.L.; Junga, Z.; Singla, M.B.; Sjogren, M.; Torres, D. Hepatitis C eradication with sofosbuvir leads to significant metabolic changes. World J. Hepatol. 2016, 8, 1557–1563. [Google Scholar] [CrossRef]
- Endo, D.; Satoh, K.; Shimada, N.; Hokari, A.; Aizawa, Y. Impact of interferon-free antivirus therapy on lipid profiles in patients with chronic hepatitis C genotype 1b. World J. Gastroenterol. 2017, 23, 2355–2364. [Google Scholar] [CrossRef] [Green Version]
- Estefan, S.; Brandão-Melo, C.E.; Silva, C.M.D.S.; Gomes, D.C.K.; Cardoso, P.; Costa, M.H.S. Metabolic Evaluation in Patients with Hepatitis C Treated with Direct Antiviral Agents. Front. Med. 2021, 8, 631600. [Google Scholar] [CrossRef]
- Ramcharran, D.; Wahed, A.S.; Conjeevaram, H.S.; Evans, R.W.; Wang, T.; Belle, S.H.; Yee, L.J. Associations between serum lipids and hepatitis C antiviral treatment efficacy. Hepatology 2010, 52, 854–863. [Google Scholar] [CrossRef] [Green Version]
- Qing, S.; Ji, D.; Li, B.; Li, F.; Wang, Y.; Niu, X.; Ling, B.; Meng, Y.; Lau, G.; Chen, G. Improvement of glucose and lipid metabolism with pegylated interferon-α plus ribavirin therapy in Chinese patients chronically infected with genotype 1b hepatitis C virus. Ann. Saudi Med. 2015, 35, 293–297. [Google Scholar] [CrossRef]
- Harrison, S.A.; Abdurakhmanov, D.; Shiffman, M.L.; Bakulin, I.; Mazur, W.; Rodriguez-Torres, M.; Silva, G.F.; Cheinquer, H.; Messinger, D.; Connell, E.V.; et al. Intensified peginterferon α-2a dosing increases sustained virologic response rates in heavy, high viral load hepatitis C genotype 1 patients with high low-density lipoprotein. J. Clin. Gastroenterol. 2013, 47, 271–279. [Google Scholar] [CrossRef]
- Loo, N.; Hanysak, B.; Mann, J.; Ramirez, R.; Kim, J.; Mitchell, R.; Van Frank, T.; Guerrero, R.; Hinojosa, K.; Christensen, K.; et al. Real-world observational experience with direct-acting antivirals for hepatitis C: Baseline resistance, efficacy, and need for long-term surveillance. Medicine 2019, 98, e16254. [Google Scholar] [CrossRef]
- Bassani, L.; Fernandes, S.A.; Raimundo, F.V.; Harter, D.L.; Gonzalez, M.C.; Marroni, C.A. Lipid profile of cirrhotic patients and its association with prognostic scores: A cross-sectional study. Arq. De Gastroenterol. 2015, 52, 210–215. [Google Scholar] [CrossRef]
- Habib, A.; Mihas, A.A.; Abou-Assi, S.G.; Williams, L.M.; Gavis, E.; Pandak, W.M.; Heuman, D.M. High-density lipoprotein cholesterol as an indicator of liver function and prognosis in noncholestatic cirrhotics. Clin. Gastroenterol. Hepatol. 2005, 3, 286–291. [Google Scholar] [CrossRef] [PubMed]
- Hashimoto, S.; Yatsuhashi, H.; Abiru, S.; Yamasaki, K.; Komori, A.; Nagaoka, S.; Saeki, A.; Uchida, S.; Bekki, S.; Kugiyama, Y.; et al. Rapid Increase in Serum Low-Density Lipoprotein Cholesterol Concentration during Hepatitis C Interferon-Free Treatment. PLoS ONE 2016, 11, e0163644. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- European Association for the Study of the Liver. EASL recommendations on treatment of hepatitis C 2016. J. Hepatol. 2017, 66, 153–194. [Google Scholar] [CrossRef] [PubMed]
Variables | Overall Cohort n, 132 |
---|---|
Age (years) | 61.17 ± 9.11 |
Females, n (%) | 85 (64.4) |
Weight(kg) | 79.12 ± 16.03 |
Height(cm) | 168.5 ± 9.69 |
Body mass index (kg/m2) | 27.12 ± 3.22 |
Underweight, n (%) | 3 (2.3) |
Lean subjects, n (%) | 42 (31.8) |
Overweight, n (%) | 53 (40.2) |
Obese, n (%) | 34 (25.7) |
Waist circumference, (cm) | 87.6 ± 14.1 |
Hypertension, n (%) | 68 (51.5) |
Diabetes, n (%) | 32 (24.2) |
Pre-diabetes, n (%) | 39 (32.5) |
Dyslipidemia, n (%) | 27 (20.4) |
Metabolic syndrome, n (%) | 35 (26.5) |
Steatosis degree, n (%) | |
CAP < 248 dB/m, n (%) | 57 (43.2) |
CAP ≥ 248 dB/m, n(%) | 32 (24.2) |
CAP ≥ 268 dB/m, n (%) | 26 (19.7) |
CAP ≥ 280 dB/m, n (%) | 17 (12.9) |
CAP, dB/m | 233.27 ± 48.26 |
Fibrosis stage, n (%) | |
LSM < 5.6 kPa, n (%) | 18 (13.6) |
LSM ≥ 5.6 kPa, n (%) | 37 (28) |
LSM ≥ 7.1 kPa, n (%) | 16 (12.1) |
LSM ≥ 9.5 kPa, n (%) | 42 (31.8) |
LSM ≥ 12.5 kPa, n (%) | 19 (14.4) |
LSM, kPa | 8.94 ± 5.1 |
Variable | Pre-Treatment | Post-Treatment | p-Value |
---|---|---|---|
HGB (g/dL) | 12.91 ± 1.72 | 12.94 ± 1.58 | 0.644 |
Platelet count (G/L) | 176.73 ± 68.06 | 183.53 ± 66.43 | 0.721 |
Total bilirubin (mg/dL) | 1.19 ± 0.64 | 1.08 ± 0.55 | 0.532 |
AST (IU/L) | 36.83 ± 21.54 | 30.62 ± 23.61 | 0.097 |
ALT (IU/L) | 42.5 ± 25.21 | 35.23 ± 22.13 | 0.119 |
GGT (IU/L) | 90.4 ± 72.5 | 62.4 ± 46.3 | 0.038 |
Albumin(mg/dL) | 3.86 ± 0.72 | 4.01 ±0.67 | 0.058 |
Glucose(mg/dL) | 115.08 ± 34.9 | 109.26 ± 29.43 | 0.064 |
HbA1c (%) | 5.52 ± 0.65 | 5.41 ± 0.51 | 0.124 |
Total cholesterol (mg/dL) | 161.68 ± 31.6 | 177.01 ± 42.2 | 0.014 |
Triglycerides (mg/dL) | 135.7 ± 41.4 | 145.4± 47.2 | 0.026 |
LDL (mg/dL) | 114.05± 37.1 | 129. 32 ± 44.6 | 0.017 |
HDL (mg/dL) | 44.8 ± 12.9 | 43.95 ± 13.1 | 0.236 |
LSM (kPa) | 8.94 ± 5.1 | 8.02 ± 4.8 | 0.023 |
Fibrosis stage, n (%) | |||
F0, n (%) | 18 (13.6) | 25 (18.9) | |
F1, n (%) | 37 (28) | 42 (31.8) | |
F2, n (%) | 16 (12.1) | 19 (14.4) | |
F3, n (%) | 42 (31.8) | 34 (25.8) | |
F4, n (%) | 19 (14.4) | 12 (9.1) | |
CAP (dB/m) | 233.27 ± 48.26 | 259 ± 63.89 | <0.001 |
Steatosis degree, n (%) | |||
S0, n (%) | 57 (43.2) | 50 (37.9) | |
S1, n (%) | 32 (24.2) | 39 (29.5) | |
S2, n (%) | 26 (19.7) | 29 (22) | |
S3, n (%) | 17 (12.9) | 14 (10.6) |
Variable | Baseline | SVR12 | Post-SVR Evaluation | p-Value |
---|---|---|---|---|
BMI (kg/m2) | 27.11 ± 3.22 | 27.415 ± 3.03 | 28.04 ± 1.11 | 0.012 |
Waist circumference (cm) | 87.6 ± 13.1 | 87.9 ± 13.2 | 88.4 ± 13.6 | 0.031 |
Cholesterol (mg/dL) | 161.68 ± 31.6 | 168.23 ± 37.1 | 177.01 ± 42.2 | 0.014 |
LDL-cholesterol (mg/dL) | 114.05± 37.1 | 122.41 ± 34.3 | 129. 32 ± 44.6 | 0.07 |
Triglycerides (mg/dL) | 135.7 ± 41.4 | 133.48 ± 41.8 | 145.4 ± 47.2 | 0.026 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Trifan, A.; Cuciureanu, T.; Nastasa, R.; Stratina, E.; Zenovia, S.; Muzica, C.M.; Huiban, L.; Singeap, A.-M.; Chiriac, S.; Sfarti, C.; et al. Changes in Components of Metabolic Syndrome after Antiviral Eradication in Hepatitis C Virus Infection. Life 2023, 13, 534. https://doi.org/10.3390/life13020534
Trifan A, Cuciureanu T, Nastasa R, Stratina E, Zenovia S, Muzica CM, Huiban L, Singeap A-M, Chiriac S, Sfarti C, et al. Changes in Components of Metabolic Syndrome after Antiviral Eradication in Hepatitis C Virus Infection. Life. 2023; 13(2):534. https://doi.org/10.3390/life13020534
Chicago/Turabian StyleTrifan, Anca, Tudor Cuciureanu, Robert Nastasa, Ermina Stratina, Sebastian Zenovia, Cristina Maria Muzica, Laura Huiban, Ana-Maria Singeap, Stefan Chiriac, Catalin Sfarti, and et al. 2023. "Changes in Components of Metabolic Syndrome after Antiviral Eradication in Hepatitis C Virus Infection" Life 13, no. 2: 534. https://doi.org/10.3390/life13020534