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Published in: European Journal of Clinical Microbiology & Infectious Diseases 2/2013

01-02-2013 | Article

Association of torque teno virus (TTV) and torque teno mini virus (TTMV) with liver disease among patients coinfected with human immunodeficiency virus and hepatitis C virus

Authors: M. García-Álvarez, J. Berenguer, E. Álvarez, M. Guzmán-Fulgencio, J. Cosín, P. Miralles, P. Catalán, J. C. López, J. Ma Rodríguez, D. Micheloud, Ma Á. Muñoz-Fernández, S. Resino

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 2/2013

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Abstract

Torque teno virus (TTV) and torque teno mini virus (TTMV) have been potentially related to liver diseases. The aim of the study was to quantify TTV and TTMV in human immunodeficiency virus (HIV)/hepatitis C virus (HCV)-coinfected patients to study the relationship between the TTV and TTMV viral loads and the severity of liver disease. We carried out a cross-sectional study in 245 patients coinfected with HIV and HCV (HIV/HCV-group), 114 patients monoinfected with HIV (HIV-group), and 100 healthy blood donors (Control-group). Plasma samples were tested for TTV and TTMV by quantitative real-time polymerase chain reaction (PCR). The prevalences of TTV and TTMV infections in the HIV/HCV-group and the HIV-group were significantly higher than the Control-group (p < 0.05). Furthermore, TTV and TTMV coinfections were found in 92.2 % (226/245) in the HIV/HCV-group, 84.2 % (96/114) in the HIV-group, and 63 % (63/100 %) in the Control-group (p ≤ 0.05). HIV/HCV-coinfected patients with HIV viral load ≥50 copies/mL and patients with severe activity grade had the highest viral loads of TTV and TTMV (p ≤ 0.05). HIV/HCV-coinfected patients with high TTV load (>2.78 log copies/μL) had increased odds of having advanced fibrosis or severe necroinflammatory activity grade in the liver biopsy. Moreover, HIV/HCV-coinfected patients with high TTMV load (>1.88 log copies/μL) had decreased odds of having no/minimal fibrosis and no/mild activity grade, and increased odds of having a high fibrosis progression rate. In conclusion, TTV and TTMV might play a role in the development of liver disease in immunodeficiency patients, such as the patients coinfected with HIV and HCV.
Literature
1.
go back to reference Nishizawa T, Okamoto H, Konishi K, Yoshizawa H, Miyakawa Y, Mayumi M (1997) A novel DNA virus (TTV) associated with elevated transaminase levels in posttransfusion hepatitis of unknown etiology. Biochem Biophys Res Commun 241(1):92–97PubMedCrossRef Nishizawa T, Okamoto H, Konishi K, Yoshizawa H, Miyakawa Y, Mayumi M (1997) A novel DNA virus (TTV) associated with elevated transaminase levels in posttransfusion hepatitis of unknown etiology. Biochem Biophys Res Commun 241(1):92–97PubMedCrossRef
2.
go back to reference Takahashi K, Iwasa Y, Hijikata M, Mishiro S (2000) Identification of a new human DNA virus (TTV-like mini virus, TLMV) intermediately related to TT virus and chicken anemia virus. Arch Virol 145(5):979–993PubMedCrossRef Takahashi K, Iwasa Y, Hijikata M, Mishiro S (2000) Identification of a new human DNA virus (TTV-like mini virus, TLMV) intermediately related to TT virus and chicken anemia virus. Arch Virol 145(5):979–993PubMedCrossRef
3.
go back to reference Huang LY, Øystein Jonassen T, Hungnes O, Grinde B (2001) High prevalence of TT virus-related DNA (90%) and diverse viral genotypes in Norwegian blood donors. J Med Virol 64(3):381–386PubMedCrossRef Huang LY, Øystein Jonassen T, Hungnes O, Grinde B (2001) High prevalence of TT virus-related DNA (90%) and diverse viral genotypes in Norwegian blood donors. J Med Virol 64(3):381–386PubMedCrossRef
4.
go back to reference Takahashi K, Hoshino H, Ohta Y, Yoshida N, Mishiro S (1998) Very high prevalence of TT virus (TTV) infection in general population of Japan revealed by a new set of PCR primers. Hepatol Res 12:233–239CrossRef Takahashi K, Hoshino H, Ohta Y, Yoshida N, Mishiro S (1998) Very high prevalence of TT virus (TTV) infection in general population of Japan revealed by a new set of PCR primers. Hepatol Res 12:233–239CrossRef
5.
go back to reference Okamoto H (2009) History of discoveries and pathogenicity of TT viruses. Curr Top Microbiol Immunol 331:1–20PubMedCrossRef Okamoto H (2009) History of discoveries and pathogenicity of TT viruses. Curr Top Microbiol Immunol 331:1–20PubMedCrossRef
6.
go back to reference Davidson F, MacDonald D, Mokili JLK, Prescott LE, Graham S, Simmonds P (1999) Early acquisition of TT virus (TTV) in an area endemic for TTV infection. J Infect Dis 179(5):1070–1076PubMedCrossRef Davidson F, MacDonald D, Mokili JLK, Prescott LE, Graham S, Simmonds P (1999) Early acquisition of TT virus (TTV) in an area endemic for TTV infection. J Infect Dis 179(5):1070–1076PubMedCrossRef
7.
go back to reference Ball JK, Curran R, Berridge S, Grabowska AM, Jameson CL, Thomson BJ, Irving WL, Sharp PM (1999) TT virus sequence heterogeneity in vivo: evidence for co-infection with multiple genetic types. J Gen Virol 80(Pt 7):1759–1768PubMed Ball JK, Curran R, Berridge S, Grabowska AM, Jameson CL, Thomson BJ, Irving WL, Sharp PM (1999) TT virus sequence heterogeneity in vivo: evidence for co-infection with multiple genetic types. J Gen Virol 80(Pt 7):1759–1768PubMed
8.
go back to reference Sugiyama K, Goto K, Ando T, Mizutani F, Terabe K, Kawabe Y, Wada Y (1999) Route of TT virus infection in children. J Med Virol 59(2):204–207PubMedCrossRef Sugiyama K, Goto K, Ando T, Mizutani F, Terabe K, Kawabe Y, Wada Y (1999) Route of TT virus infection in children. J Med Virol 59(2):204–207PubMedCrossRef
9.
go back to reference Simmonds P, Davidson F, Lycett C, Prescott LE, MacDonald DM, Ellender J, Yap PL, Ludlam CA, Haydon GH, Gillon J, Jarvis LM (1998) Detection of a novel DNA virus (TTV) in blood donors and blood products. Lancet 352(9123):191–195PubMedCrossRef Simmonds P, Davidson F, Lycett C, Prescott LE, MacDonald DM, Ellender J, Yap PL, Ludlam CA, Haydon GH, Gillon J, Jarvis LM (1998) Detection of a novel DNA virus (TTV) in blood donors and blood products. Lancet 352(9123):191–195PubMedCrossRef
10.
go back to reference Shibayama T, Masuda G, Ajisawa A, Takahashi M, Nishizawa T, Tsuda F, Okamoto H (2001) Inverse relationship between the titre of TT virus DNA and the CD4 cell count in patients infected with HIV. AIDS 15(5):563–570PubMedCrossRef Shibayama T, Masuda G, Ajisawa A, Takahashi M, Nishizawa T, Tsuda F, Okamoto H (2001) Inverse relationship between the titre of TT virus DNA and the CD4 cell count in patients infected with HIV. AIDS 15(5):563–570PubMedCrossRef
11.
go back to reference Christensen JK, Eugen-Olsen J, Sorensen M, Ullum H, Gjedde SB, Pedersen BK, Nielsen JO, Krogsgaard K (2000) Prevalence and prognostic significance of infection with TT virus in patients infected with human immunodeficiency virus. J Infect Dis 181(5):1796–1799PubMedCrossRef Christensen JK, Eugen-Olsen J, Sorensen M, Ullum H, Gjedde SB, Pedersen BK, Nielsen JO, Krogsgaard K (2000) Prevalence and prognostic significance of infection with TT virus in patients infected with human immunodeficiency virus. J Infect Dis 181(5):1796–1799PubMedCrossRef
12.
go back to reference Okamoto H, Nishizawa T, Ukita M (1999) A novel unenveloped DNA virus (TT virus) associated with acute and chronic non-A to G hepatitis. Intervirology 42(2–3):196–204PubMedCrossRef Okamoto H, Nishizawa T, Ukita M (1999) A novel unenveloped DNA virus (TT virus) associated with acute and chronic non-A to G hepatitis. Intervirology 42(2–3):196–204PubMedCrossRef
13.
go back to reference Focosi D, Maggi F, Albani M, Macera L, Ricci V, Gragnani S, Di Beo S, Ghimenti M, Antonelli G, Bendinelli M, Pistello M, Ceccherini-Nelli L, Petrini M (2010) Torquetenovirus viremia kinetics after autologous stem cell transplantation are predictable and may serve as a surrogate marker of functional immune reconstitution. J Clin Virol 47(2):189–192PubMedCrossRef Focosi D, Maggi F, Albani M, Macera L, Ricci V, Gragnani S, Di Beo S, Ghimenti M, Antonelli G, Bendinelli M, Pistello M, Ceccherini-Nelli L, Petrini M (2010) Torquetenovirus viremia kinetics after autologous stem cell transplantation are predictable and may serve as a surrogate marker of functional immune reconstitution. J Clin Virol 47(2):189–192PubMedCrossRef
14.
go back to reference Kaufmann GR, Elzi L, Weber R, Furrer H, Giulieri S, Vernazza P, Bernasconi E, Hirschel B, Battegay M; Swiss HIV Cohort Study (2011) Interruptions of cART limits CD4 T-cell recovery and increases the risk for opportunistic complications and death. AIDS 25(4):441–451PubMedCrossRef Kaufmann GR, Elzi L, Weber R, Furrer H, Giulieri S, Vernazza P, Bernasconi E, Hirschel B, Battegay M; Swiss HIV Cohort Study (2011) Interruptions of cART limits CD4 T-cell recovery and increases the risk for opportunistic complications and death. AIDS 25(4):441–451PubMedCrossRef
15.
go back to reference Madsen CD, Eugen-Olsen J, Kirk O, Parner J, Kaae Christensen J, Brasholt MS, Ole Nielsen J, Krogsgaard K (2002) TTV viral load as a marker for immune reconstitution after initiation of HAART in HIV-infected patients. HIV Clin Trials 3(4):287–295PubMedCrossRef Madsen CD, Eugen-Olsen J, Kirk O, Parner J, Kaae Christensen J, Brasholt MS, Ole Nielsen J, Krogsgaard K (2002) TTV viral load as a marker for immune reconstitution after initiation of HAART in HIV-infected patients. HIV Clin Trials 3(4):287–295PubMedCrossRef
16.
go back to reference Okamoto H, Ukita M, Nishizawa T, Kishimoto J, Hoshi Y, Mizuo H, Tanaka T, Miyakawa Y, Mayumi M (2000) Circular double-stranded forms of TT virus DNA in the liver. J Virol 74(11):5161–5167PubMedCrossRef Okamoto H, Ukita M, Nishizawa T, Kishimoto J, Hoshi Y, Mizuo H, Tanaka T, Miyakawa Y, Mayumi M (2000) Circular double-stranded forms of TT virus DNA in the liver. J Virol 74(11):5161–5167PubMedCrossRef
17.
go back to reference Okamoto H, Nishizawa T, Kato N, Ukita M, Ikeda H, Iizuka H, Miyakawa Y, Mayumi M (1998) Molecular cloning and characterization of a novel DNA virus (TTV) associated with posttransfusion hepatitis of unknown etiology. Hepatol Res 10(1):1–16CrossRef Okamoto H, Nishizawa T, Kato N, Ukita M, Ikeda H, Iizuka H, Miyakawa Y, Mayumi M (1998) Molecular cloning and characterization of a novel DNA virus (TTV) associated with posttransfusion hepatitis of unknown etiology. Hepatol Res 10(1):1–16CrossRef
18.
go back to reference Kao JH, Chen W, Chen PJ, Lai MY, Chen DS (2000) TT virus infection in patients with chronic hepatitis B or C: Influence on clinical, histological and virological features. J Med Virol 60(4):387–392PubMedCrossRef Kao JH, Chen W, Chen PJ, Lai MY, Chen DS (2000) TT virus infection in patients with chronic hepatitis B or C: Influence on clinical, histological and virological features. J Med Virol 60(4):387–392PubMedCrossRef
19.
go back to reference Charlton M, Adjei P, Poterucha J, Zein N, Moore B, Therneau T, Krom R, Wiesner R (1998) TT-virus infection in North American blood donors, patients with fulminant hepatic failure, and cryptogenic cirrhosis. Hepatology 28(3):839–842PubMedCrossRef Charlton M, Adjei P, Poterucha J, Zein N, Moore B, Therneau T, Krom R, Wiesner R (1998) TT-virus infection in North American blood donors, patients with fulminant hepatic failure, and cryptogenic cirrhosis. Hepatology 28(3):839–842PubMedCrossRef
20.
go back to reference Ikeda H, Takasu M, Inoue K, Okamoto H, Miyakawa Y, Mayumi M (1999) Infection with an unenveloped DNA virus (TTV) in patients with acute or chronic liver disease of unknown etiology and in those positive for hepatitis C virus RNA. J Hepatol 30(2):205–212PubMedCrossRef Ikeda H, Takasu M, Inoue K, Okamoto H, Miyakawa Y, Mayumi M (1999) Infection with an unenveloped DNA virus (TTV) in patients with acute or chronic liver disease of unknown etiology and in those positive for hepatitis C virus RNA. J Hepatol 30(2):205–212PubMedCrossRef
21.
go back to reference Tokita H, Murai S, Kamitsukasa H, Yagura M, Harada H, Takahashi M, Okamoto H (2002) High TT virus load as an independent factor associated with the occurrence of hepatocellular carcinoma among patients with hepatitis C virus-related chronic liver disease. J Med Virol 67(4):501–509PubMedCrossRef Tokita H, Murai S, Kamitsukasa H, Yagura M, Harada H, Takahashi M, Okamoto H (2002) High TT virus load as an independent factor associated with the occurrence of hepatocellular carcinoma among patients with hepatitis C virus-related chronic liver disease. J Med Virol 67(4):501–509PubMedCrossRef
22.
go back to reference Zein NN, Arslan M, Li H, Charlton MR, Gross JB Jr, Poterucha JJ, Therneau TM, Kolbert CP, Persing DH (1999) Clinical significance of TT virus infection in patients with chronic hepatitis C. Am J Gastroenterol 94(10):3020–3027PubMedCrossRef Zein NN, Arslan M, Li H, Charlton MR, Gross JB Jr, Poterucha JJ, Therneau TM, Kolbert CP, Persing DH (1999) Clinical significance of TT virus infection in patients with chronic hepatitis C. Am J Gastroenterol 94(10):3020–3027PubMedCrossRef
23.
go back to reference Moriyama M, Matsumura H, Shimizu T, Shioda A, Kaneko M, Miyazawa K, Miyata H, Tanaka N, Uchida T, Arakawa Y (2001) Histopathologic impact of TT virus infection on the liver of type C chronic hepatitis and liver cirrhosis in Japan. J Med Virol 64(1):74–81PubMedCrossRef Moriyama M, Matsumura H, Shimizu T, Shioda A, Kaneko M, Miyazawa K, Miyata H, Tanaka N, Uchida T, Arakawa Y (2001) Histopathologic impact of TT virus infection on the liver of type C chronic hepatitis and liver cirrhosis in Japan. J Med Virol 64(1):74–81PubMedCrossRef
24.
go back to reference Alvarez do Barrio M, González Díez R, Hernández Sánchez JM, Oyonarte Gómez S (2005) Residual risk of transfusion-transmitted viral infections in Spain, 1997–2002, and impact of nucleic acid testing. Euro Surveill 10(2):20–22PubMed Alvarez do Barrio M, González Díez R, Hernández Sánchez JM, Oyonarte Gómez S (2005) Residual risk of transfusion-transmitted viral infections in Spain, 1997–2002, and impact of nucleic acid testing. Euro Surveill 10(2):20–22PubMed
25.
go back to reference Jacobs WH, Goldberg SB, Balint JA, Boyce HW, Browning TH, Cooper JN, Earnest DL, Friedman E, Greene M, Mellow MA, Pitt HA, Todaro JL; Patient Care Committee of the American Gastroenterological Association (1989) Statement on outpatient percutaneous liver biopsy. Dig Dis Sci 34(3):322–323PubMedCrossRef Jacobs WH, Goldberg SB, Balint JA, Boyce HW, Browning TH, Cooper JN, Earnest DL, Friedman E, Greene M, Mellow MA, Pitt HA, Todaro JL; Patient Care Committee of the American Gastroenterological Association (1989) Statement on outpatient percutaneous liver biopsy. Dig Dis Sci 34(3):322–323PubMedCrossRef
26.
go back to reference Bedossa P, Poynard T (1996) An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology 24(2):289–293PubMedCrossRef Bedossa P, Poynard T (1996) An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology 24(2):289–293PubMedCrossRef
27.
go back to reference Moen EM, Sleboda J, Grinde B (2002) Real-time PCR methods for independent quantitation of TTV and TLMV. J Virol Methods 104(1):59–67PubMedCrossRef Moen EM, Sleboda J, Grinde B (2002) Real-time PCR methods for independent quantitation of TTV and TLMV. J Virol Methods 104(1):59–67PubMedCrossRef
28.
go back to reference Biagini P, Gallian P, Touinssi M, Cantaloube JF, Zapitelli JP, de Lamballerie X, de Micco P (2000) High prevalence of TT virus infection in French blood donors revealed by the use of three PCR systems. Transfusion 40(5):590–595PubMedCrossRef Biagini P, Gallian P, Touinssi M, Cantaloube JF, Zapitelli JP, de Lamballerie X, de Micco P (2000) High prevalence of TT virus infection in French blood donors revealed by the use of three PCR systems. Transfusion 40(5):590–595PubMedCrossRef
29.
go back to reference Maggi F, Bendinelli M (2009) Immunobiology of the Torque teno viruses and other anelloviruses. Curr Top Microbiol Immunol 331:65–90PubMedCrossRef Maggi F, Bendinelli M (2009) Immunobiology of the Torque teno viruses and other anelloviruses. Curr Top Microbiol Immunol 331:65–90PubMedCrossRef
30.
31.
go back to reference Zhong S, Yeo W, Tang MW, Lin XR, Mo F, Ho WM, Hui P, Johnson PJ (2001) Gross elevation of TT Virus genome load in the peripheral blood mononuclear Cells of cancer patients. Ann N Y Acad Sci 945:84–92PubMedCrossRef Zhong S, Yeo W, Tang MW, Lin XR, Mo F, Ho WM, Hui P, Johnson PJ (2001) Gross elevation of TT Virus genome load in the peripheral blood mononuclear Cells of cancer patients. Ann N Y Acad Sci 945:84–92PubMedCrossRef
32.
go back to reference Touinssi M, Gallian P, Biagini P, Attoui H, Vialettes B, Berland Y, Tamalet C, Dhiver C, Ravaux I, De Micco P, De Lamballerie X (2001) TT virus infection: prevalence of elevated viraemia and arguments for the immune control of viral load. J Clin Virol 21(2):135–141PubMedCrossRef Touinssi M, Gallian P, Biagini P, Attoui H, Vialettes B, Berland Y, Tamalet C, Dhiver C, Ravaux I, De Micco P, De Lamballerie X (2001) TT virus infection: prevalence of elevated viraemia and arguments for the immune control of viral load. J Clin Virol 21(2):135–141PubMedCrossRef
33.
go back to reference Thom K, Petrik J (2007) Progression towards AIDS leads to increased torque teno virus and torque teno minivirus titers in tissues of HIV infected individuals. J Med Virol 79(1):1–7PubMedCrossRef Thom K, Petrik J (2007) Progression towards AIDS leads to increased torque teno virus and torque teno minivirus titers in tissues of HIV infected individuals. J Med Virol 79(1):1–7PubMedCrossRef
34.
go back to reference Mariscal LF, López-Alcorocho JM, Rodríguez-Iñigo E, Ortiz-Movilla N, de Lucas S, Bartolomé J, Carreño V (2002) TT virus replicates in stimulated but not in nonstimulated peripheral blood mononuclear cells. Virology 301(1):121–129PubMedCrossRef Mariscal LF, López-Alcorocho JM, Rodríguez-Iñigo E, Ortiz-Movilla N, de Lucas S, Bartolomé J, Carreño V (2002) TT virus replicates in stimulated but not in nonstimulated peripheral blood mononuclear cells. Virology 301(1):121–129PubMedCrossRef
35.
go back to reference Reiberger T, Ferlitsch A, Sieghart W, Kreil A, Breitenecker F, Rieger A, Schmied B, Gangl A, Peck-Radosavljevic M (2010) HIV-HCV co-infected patients with low CD4+ cell nadirs are at risk for faster fibrosis progression and portal hypertension. J Viral Hepat 17(6):400–409PubMedCrossRef Reiberger T, Ferlitsch A, Sieghart W, Kreil A, Breitenecker F, Rieger A, Schmied B, Gangl A, Peck-Radosavljevic M (2010) HIV-HCV co-infected patients with low CD4+ cell nadirs are at risk for faster fibrosis progression and portal hypertension. J Viral Hepat 17(6):400–409PubMedCrossRef
36.
go back to reference Thorpe J, Saeed S, Moodie EE, Klein MB; Canadian Co-infection Cohort Study (CTN222) (2011) Antiretroviral treatment interruption leads to progression of liver fibrosis in HIV-hepatitis C virus co-infection. AIDS 25(7):967–975PubMedCrossRef Thorpe J, Saeed S, Moodie EE, Klein MB; Canadian Co-infection Cohort Study (CTN222) (2011) Antiretroviral treatment interruption leads to progression of liver fibrosis in HIV-hepatitis C virus co-infection. AIDS 25(7):967–975PubMedCrossRef
37.
go back to reference Shang D, Lin YH, Rigopoulou I, Chen B, Alexander GJM, Allain JP (2000) Detection of TT virus DNA in patients with liver disease and recipients of liver transplant. J Med Virol 61(4):455–461PubMedCrossRef Shang D, Lin YH, Rigopoulou I, Chen B, Alexander GJM, Allain JP (2000) Detection of TT virus DNA in patients with liver disease and recipients of liver transplant. J Med Virol 61(4):455–461PubMedCrossRef
38.
go back to reference Bendinelli M, Pistello M, Maggi F, Fornai C, Freer G, Vatteroni ML (2001) Molecular properties, biology, and clinical implications of TT virus, a recently identified widespread infectious agent of humans. Clin Microbiol Rev 14(1):98–113PubMedCrossRef Bendinelli M, Pistello M, Maggi F, Fornai C, Freer G, Vatteroni ML (2001) Molecular properties, biology, and clinical implications of TT virus, a recently identified widespread infectious agent of humans. Clin Microbiol Rev 14(1):98–113PubMedCrossRef
39.
go back to reference Moriyama M, Matsumura H, Shimizu T, Shioda A, Kaneko M, Miyazawa K, Miyata H, Tanaka N, Uchida T, Arakawa Y (2001) Histopathologic impact of TT virus infection on the liver of type C chronic hepatitis and liver cirrhosis in Japan. J Med Virol 64(1):74–81PubMedCrossRef Moriyama M, Matsumura H, Shimizu T, Shioda A, Kaneko M, Miyazawa K, Miyata H, Tanaka N, Uchida T, Arakawa Y (2001) Histopathologic impact of TT virus infection on the liver of type C chronic hepatitis and liver cirrhosis in Japan. J Med Virol 64(1):74–81PubMedCrossRef
40.
go back to reference Sioda A, Moriyama M, Matsumura H, Kaneko M, Tanaka N, Arakawa Y (2001) Clinicopathological features of serum TTV DNA-positive non-A-G liver diseases in Japan. Hepatol Res 21(2):169–180PubMedCrossRef Sioda A, Moriyama M, Matsumura H, Kaneko M, Tanaka N, Arakawa Y (2001) Clinicopathological features of serum TTV DNA-positive non-A-G liver diseases in Japan. Hepatol Res 21(2):169–180PubMedCrossRef
41.
go back to reference Masia G, Ingianni A, Demelia L, Faa G, Manconi PE, Pilleri G, Ciancio A, Rizzetto M, Coppola RC (2001) TT virus infection in Italy: prevalence and genotypes in healthy subjects, viral liver diseases and asymptomatic infections by parenterally transmitted viruses. J Viral Hepat 8(5):384–390PubMedCrossRef Masia G, Ingianni A, Demelia L, Faa G, Manconi PE, Pilleri G, Ciancio A, Rizzetto M, Coppola RC (2001) TT virus infection in Italy: prevalence and genotypes in healthy subjects, viral liver diseases and asymptomatic infections by parenterally transmitted viruses. J Viral Hepat 8(5):384–390PubMedCrossRef
42.
go back to reference Shieh B, Chang MJ, Ko WC, Chen EJ, Wu JC, Lee CF, Chang TT, Li C (2003) Effects of multiple virus coinfections on disease progression in HIV-positive patients. Intervirology 46(2):105–113PubMedCrossRef Shieh B, Chang MJ, Ko WC, Chen EJ, Wu JC, Lee CF, Chang TT, Li C (2003) Effects of multiple virus coinfections on disease progression in HIV-positive patients. Intervirology 46(2):105–113PubMedCrossRef
43.
go back to reference Hofer H, Aydin I, Neumueller-Guber S, Mueller C, Scherzer TM, Staufer K, Steindl-Munda P, Wrba F, Ferenci P (2011) Prevalence and clinical significance of GB virus type C/hepatitis G virus coinfection in patients with chronic hepatitis C undergoing antiviral therapy. J Viral Hepat 18(7):513–517PubMedCrossRef Hofer H, Aydin I, Neumueller-Guber S, Mueller C, Scherzer TM, Staufer K, Steindl-Munda P, Wrba F, Ferenci P (2011) Prevalence and clinical significance of GB virus type C/hepatitis G virus coinfection in patients with chronic hepatitis C undergoing antiviral therapy. J Viral Hepat 18(7):513–517PubMedCrossRef
44.
go back to reference Moriyama M, Matsumura H, Shimizu T, Shioda A, Kaneko M, Saito H, Miyazawa K, Tanaka N, Sugitani M, Komiyama K, Arakawa Y (2000) Hepatitis G virus coinfection influences the liver histology of patients with chronic hepatitis C. Liver 20(5):397–404PubMedCrossRef Moriyama M, Matsumura H, Shimizu T, Shioda A, Kaneko M, Saito H, Miyazawa K, Tanaka N, Sugitani M, Komiyama K, Arakawa Y (2000) Hepatitis G virus coinfection influences the liver histology of patients with chronic hepatitis C. Liver 20(5):397–404PubMedCrossRef
Metadata
Title
Association of torque teno virus (TTV) and torque teno mini virus (TTMV) with liver disease among patients coinfected with human immunodeficiency virus and hepatitis C virus
Authors
M. García-Álvarez
J. Berenguer
E. Álvarez
M. Guzmán-Fulgencio
J. Cosín
P. Miralles
P. Catalán
J. C. López
J. Ma Rodríguez
D. Micheloud
Ma Á. Muñoz-Fernández
S. Resino
Publication date
01-02-2013
Publisher
Springer-Verlag
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 2/2013
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-012-1744-1

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