Hepatitis delta infection among persons living with HIV in Europe

doi:10.1111/liv.15519

. 2023 Apr;43(4):819-828.

doi: 10.1111/liv.15519. Epub 2023 Jan 21.

Hepatitis delta infection among persons living with HIV in Europe

Collaborators, Affiliations

Collaborators

for EuroSIDA and SHCS:
I Abela, K Aebi-Popp, A Anagnostopoulos, M Battegay, E Bernasconi, D L Braun, H C Bucher, A Calmy, M Cavassini, A Ciuffi, G Dollenmaier, M Egger, L Elzi, J Fehr, J Fellay, H Furrer, C A Fux, A Hachfeld, B Hasse, H H Hirsch, M Hoffmann, I Hösli, M Huber, L Kaiser, O Keiser, T Klimkait, R D Kouyos, H Kovari, G Martinetti, B Martinez de Tejada, C Marzolini, K J Metzner, N Müller, J Nemeth, D Nicca, P Paioni, G Pantaleo, M Perreau, A Rauch, P Schmid, R Speck, M Stöckle, P Tarr, A Trkola, G Wandeler, S Yerly, A Harxhi, M Losso, M Kundro, B Schmied, R Zangerle, I Karpov, A Vassilenko, V M Mitsura, D Paduto, N Clumeck, S De Wit, M Delforge, E Florence, L Vandekerckhove, V Hadziosmanovic, J Begovac, L Machala, D Jilich, D Sedlacek, G Kronborg, T Benfield, J Gerstoft, O Kirk, C Pedersen, I S Johansen, L Ostergaard, L Wiese, L N Nielsen, K Zilmer, Jelena Smidt, Nakkusosakond Siseklinik, I Aho, J-P Viard, K Lacombe, C Pradier, E Fontas, C Duvivier, J Rockstroh, O Degen, C Hoffmann, H J Stellbrink, C Stefan, J Bogner, G Fätkenheuer, N Chkhartishvili, H Sambatakou, G Adamis, N Paissios, J Szlávik, M Gottfredsson, E Devitt, L Tau, D Turner, M Burke, E Shahar, L M Wattad, H Elinav, M Haouzi, D Elbirt, A D'Arminio Monforte, G Guaraldi, R Esposito, I Mazeu, C Mussini, F Mazzotta, A Gabbuti, A Lazzarin, A Castagna, N Gianotti, M Galli, A Ridolfo, V Uzdaviniene, R Matulionyte, T Staub, R Hemmer, Marc van der Valk, J Trajanovska, D H Reikvam, A Maeland, J Bruun, B Knysz, B Szetela, M Inglot, E Bakowska, R Flisiak, A Grzeszczuk, M Parczewski, K Maciejewska, B Aksak-Was, M Beniowski, E Mularska, E Jablonowska, J Kamerys, K Wojcik, I Mozer-Lisewska, B Rozplochowski, A Zagalo, K Mansinho, F Maltez, R Radoi, C Oprea, D Gusev, T Trofimova, I Khromova, E Kuzovatova, E Borodulina, E Vdoushkina, J Ranin, J Tomazic, J M Miro, J M Miró, M Laguno, E Martinez, F Garcia, J L Blanco, M Martinez-Rebollar, J Mallolas, P Callau, J Rojas, A Inciarta, S Moreno, S Del Campo, B Clotet, A Jou, R Paredes, J Puig, J M Llibre, J R Santos, P Domingo, M Gutierrez, G Mateo, M A Sambeat, J M Laporte, P Novak, A Thalme, A Sönnerborg, J Brännström, L Flamholc, K Kusejko, D Braun, M Cavassini, A Calmy, H Furrer, M Battegay, P Schmid, A Kuznetsova, J Mikhalik, M Sluzhynska, A Milinkovic, A M Johnson, S Edwards, A Phillips, M A Johnson, A Mocroft, C Orkin, A Winston, A Clarke, C Leen, I Karpov, M Losso, J Lundgren, J Rockstroh, I Aho, L D Rasmussen, P Novak, G Wandeler, C Pradier, N Chkhartishvili, R Matulionyte, C Oprea, J D Kowalska, J Begovac, J M Miró, G Guaraldi, R Paredes, G Wandeler, R Paredes, L Peters, L Peters, J F Larsen, B Neesgaard, N Jaschinski, O Fursa, D Raben, D Kristensen, A H Fischer, S K Jensen, T W Elsing, M Gardizi, A Ahmed, A Mocroft, A Phillips, J Reekie, A Cozzi-Lepri, A Pelchen-Matthews, A Roen, E S Tusch, W Bannister

Affiliations

¹ Department of Infectious Diseases, Bern University Hospital, Inselspital, University of Bern, Bern, Switzerland.
² Stichting HIV Monitoring, Department of Infectious Diseases, Public Health Service of Amsterdam, Amsterdam, the Netherlands.
³ Department of Infectious Diseases, Karolinska University Hospital, Stockholm, Sweden.
⁴ Department of Clinical Microbiology, Rigshospitalet, Copenhagen, Denmark.
⁵ Institute for Infectious Diseases, Faculty of Medicine, University of Bern, Bern, Switzerland.
⁶ Department of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, Zurich, Switzerland.
⁷ Institute of Medical Virology, University of Zurich, Zurich, Switzerland.
⁸ Department of Medicine I, University Hospital Bonn, Bonn, Germany.
⁹ Centre for Clinical Research, Epidemiology, Modelling and Evaluation (CREME), Institute for Global Health, UCL, London, UK.
¹⁰ Rigshospitalet, University of Copenhagen, Centre of Excellence for Health, Immunity and Infections (CHIP), Copenhagen, Denmark.
¹¹ Institute of Social and Preventive Medicine, University of Bern, Bern, Switzerland.

PMID: 36625770
DOI: 10.1111/liv.15519

Free article

Hepatitis delta infection among persons living with HIV in Europe

Charles Béguelin et al. Liver Int. 2023 Apr.

Free article

. 2023 Apr;43(4):819-828.

doi: 10.1111/liv.15519. Epub 2023 Jan 21.

Authors

Collaborators

for EuroSIDA and SHCS:
I Abela, K Aebi-Popp, A Anagnostopoulos, M Battegay, E Bernasconi, D L Braun, H C Bucher, A Calmy, M Cavassini, A Ciuffi, G Dollenmaier, M Egger, L Elzi, J Fehr, J Fellay, H Furrer, C A Fux, A Hachfeld, B Hasse, H H Hirsch, M Hoffmann, I Hösli, M Huber, L Kaiser, O Keiser, T Klimkait, R D Kouyos, H Kovari, G Martinetti, B Martinez de Tejada, C Marzolini, K J Metzner, N Müller, J Nemeth, D Nicca, P Paioni, G Pantaleo, M Perreau, A Rauch, P Schmid, R Speck, M Stöckle, P Tarr, A Trkola, G Wandeler, S Yerly, A Harxhi, M Losso, M Kundro, B Schmied, R Zangerle, I Karpov, A Vassilenko, V M Mitsura, D Paduto, N Clumeck, S De Wit, M Delforge, E Florence, L Vandekerckhove, V Hadziosmanovic, J Begovac, L Machala, D Jilich, D Sedlacek, G Kronborg, T Benfield, J Gerstoft, O Kirk, C Pedersen, I S Johansen, L Ostergaard, L Wiese, L N Nielsen, K Zilmer, Jelena Smidt, Nakkusosakond Siseklinik, I Aho, J-P Viard, K Lacombe, C Pradier, E Fontas, C Duvivier, J Rockstroh, O Degen, C Hoffmann, H J Stellbrink, C Stefan, J Bogner, G Fätkenheuer, N Chkhartishvili, H Sambatakou, G Adamis, N Paissios, J Szlávik, M Gottfredsson, E Devitt, L Tau, D Turner, M Burke, E Shahar, L M Wattad, H Elinav, M Haouzi, D Elbirt, A D'Arminio Monforte, G Guaraldi, R Esposito, I Mazeu, C Mussini, F Mazzotta, A Gabbuti, A Lazzarin, A Castagna, N Gianotti, M Galli, A Ridolfo, V Uzdaviniene, R Matulionyte, T Staub, R Hemmer, Marc van der Valk, J Trajanovska, D H Reikvam, A Maeland, J Bruun, B Knysz, B Szetela, M Inglot, E Bakowska, R Flisiak, A Grzeszczuk, M Parczewski, K Maciejewska, B Aksak-Was, M Beniowski, E Mularska, E Jablonowska, J Kamerys, K Wojcik, I Mozer-Lisewska, B Rozplochowski, A Zagalo, K Mansinho, F Maltez, R Radoi, C Oprea, D Gusev, T Trofimova, I Khromova, E Kuzovatova, E Borodulina, E Vdoushkina, J Ranin, J Tomazic, J M Miro, J M Miró, M Laguno, E Martinez, F Garcia, J L Blanco, M Martinez-Rebollar, J Mallolas, P Callau, J Rojas, A Inciarta, S Moreno, S Del Campo, B Clotet, A Jou, R Paredes, J Puig, J M Llibre, J R Santos, P Domingo, M Gutierrez, G Mateo, M A Sambeat, J M Laporte, P Novak, A Thalme, A Sönnerborg, J Brännström, L Flamholc, K Kusejko, D Braun, M Cavassini, A Calmy, H Furrer, M Battegay, P Schmid, A Kuznetsova, J Mikhalik, M Sluzhynska, A Milinkovic, A M Johnson, S Edwards, A Phillips, M A Johnson, A Mocroft, C Orkin, A Winston, A Clarke, C Leen, I Karpov, M Losso, J Lundgren, J Rockstroh, I Aho, L D Rasmussen, P Novak, G Wandeler, C Pradier, N Chkhartishvili, R Matulionyte, C Oprea, J D Kowalska, J Begovac, J M Miró, G Guaraldi, R Paredes, G Wandeler, R Paredes, L Peters, L Peters, J F Larsen, B Neesgaard, N Jaschinski, O Fursa, D Raben, D Kristensen, A H Fischer, S K Jensen, T W Elsing, M Gardizi, A Ahmed, A Mocroft, A Phillips, J Reekie, A Cozzi-Lepri, A Pelchen-Matthews, A Roen, E S Tusch, W Bannister

Affiliations

¹ Department of Infectious Diseases, Bern University Hospital, Inselspital, University of Bern, Bern, Switzerland.
² Stichting HIV Monitoring, Department of Infectious Diseases, Public Health Service of Amsterdam, Amsterdam, the Netherlands.
³ Department of Infectious Diseases, Karolinska University Hospital, Stockholm, Sweden.
⁴ Department of Clinical Microbiology, Rigshospitalet, Copenhagen, Denmark.
⁵ Institute for Infectious Diseases, Faculty of Medicine, University of Bern, Bern, Switzerland.
⁶ Department of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, Zurich, Switzerland.
⁷ Institute of Medical Virology, University of Zurich, Zurich, Switzerland.
⁸ Department of Medicine I, University Hospital Bonn, Bonn, Germany.
⁹ Centre for Clinical Research, Epidemiology, Modelling and Evaluation (CREME), Institute for Global Health, UCL, London, UK.
¹⁰ Rigshospitalet, University of Copenhagen, Centre of Excellence for Health, Immunity and Infections (CHIP), Copenhagen, Denmark.
¹¹ Institute of Social and Preventive Medicine, University of Bern, Bern, Switzerland.

PMID: 36625770
DOI: 10.1111/liv.15519

Abstract

Background and aims: A high prevalence of hepatitis delta virus (HDV) infection, the most severe form of viral hepatitis, has been reported among persons living with HIV (PLWH) in Europe. We analysed data from a large HIV cohort collaboration to characterize HDV epidemiological trends across Europe, as well as its impact on clinical outcomes.

Methods: All PLWH with a positive hepatitis B surface antigen (HBsAg) in the Swiss HIV Cohort Study and EuroSIDA between 1988 and 2019 were tested for anti-HDV antibodies and, if positive, for HDV RNA. Demographic and clinical characteristics at initiation of antiretroviral therapy were compared between HDV-positive and HDV-negative individuals using descriptive statistics. The associations between HDV infection and overall mortality, liver-related mortality as well as hepatocellular carcinoma (HCC) were assessed using cumulative incidence plots and cause-specific multivariable Cox regression.

Results: Of 2793 HBsAg-positive participants, 1556 (56%) had stored serum available and were included. The prevalence of HDV coinfection was 15.2% (237/1556, 95% confidence interval [CI]: 13.5%-17.1%) and 66% (132/200) of HDV-positive individuals had active HDV replication. Among persons who inject drugs (PWID), the prevalence of HDV coinfection was 50.5% (182/360, 95% CI: 45.3%-55.7%), with similar estimates across Europe, compared to 4.7% (52/1109, 95% CI: 3.5%-5.9%) among other participants. During a median follow-up of 10.8 years (interquartile range 5.6-17.8), 82 (34.6%) HDV-positive and 265 (20.1%) HDV-negative individuals died. 41.5% (34/82) of deaths were liver-related in HDV-positive individuals compared to 17.7% (47/265) in HDV-negative individuals. HDV infection was associated with overall mortality (adjusted hazard ratio 1.6; 95% CI 1.2-2.1), liver-related death (2.9, 1.6-5.0) and HCC (6.3, 2.5-16.0).

Conclusion: We found a very high prevalence of hepatitis delta among PWID across Europe. Among PLWH who do not inject drugs, the prevalence was similar to that reported from populations without HIV. HDV coinfection was associated with liver-related mortality and HCC incidence.

Keywords: HCC; HIV; Hepatitis Delta; PLWH; prevalence.

PubMed Disclaimer

Cited by

Carcinogenicity of hepatitis D virus, human cytomegalovirus, and Merkel cell polyomavirus.
Karagas MR, Kaldor J, Michaelis M, Muchengeti MM, Alfaiate D, Argirion I, Chen X, Cunha C, Hantz S, Koljonen V, Laude HC, Lui WO, Nevels MM, O'Brien TR, Scheurer ME, Touze A, Wiemels JL, Benbrahim-Tallaa L, de Conti A, Facchin C, Madia F, Pasqual E, Wedekind R, Aguilera-Buenosvinos I, Clifford G, Deng X, Dongoran RA, Ezzemni S, Huang Y, Suonio E, Zhai Y, Mattock H, Schubauer-Berigan MK, Kunzmann AT. Karagas MR, et al. Lancet Oncol. 2025 Jun 26:S1470-2045(25)00403-6. doi: 10.1016/S1470-2045(25)00403-6. Online ahead of print. Lancet Oncol. 2025. PMID: 40587985 No abstract available.
Prevalence of Hepatitis D in People Living with HIV: A National Cross-Sectional Pilot Study.
Schinas G, Antonopoulou N, Vamvakopoulou S, Tsachouridou O, Protopapas K, Petrakis V, Petrakis EC, Papageorgiou D, Metallidis S, Papadopoulos A, Barbounakis E, Kofteridis D, Panagopoulos P, Lekkou A, Paliogianni F, Akinosoglou K. Schinas G, et al. Viruses. 2024 Jun 28;16(7):1044. doi: 10.3390/v16071044. Viruses. 2024. PMID: 39066206 Free PMC article.
Hepatitis Delta and Liver Disease Among People Living With Hepatitis B With or Without HIV Co-Infection in Senegal.
Wembulua BS, Le Gal F, Ndiaye O, Pandi MS, Akotia MK, Badiane AS, Hamouda P, Tine J, Ndiaye K, Béguelin C, Ngom NF, Wandeler G, Seydi M, Mena AR; SEN‐B. Wembulua BS, et al. Liver Int. 2025 Mar;45(3):e70026. doi: 10.1111/liv.70026. Liver Int. 2025. PMID: 39967446 Free PMC article.

References

REFERENCES

1. Stockdale AJ, Kreuels B, Henrion MYR, et al. The global prevalence of hepatitis D virus infection: systematic review and meta-analysis. J Hepatol. 2020;73(3):523-532.
1. Chen HY, Shen DT, Ji DZ, et al. Prevalence and burden of hepatitis D virus infection in the global population: a systematic review and meta-analysis. Gut. 2019;68(3):512-521.
1. Kushner T, Serper M, Kaplan DE. Delta hepatitis within the veterans affairs medical system in the United States: prevalence, risk factors, and outcomes. J Hepatol. 2015;63(3):586-592.
1. Le Gal F, Brichler S, Sahli R, Chevret S, Gordien E. First international external quality assessment for hepatitis delta virus RNA quantification in plasma. Hepatology. 2016;64(5):1483-1494.
1. Koh C, Heller T, Glenn JS. Pathogenesis of and new therapies for hepatitis D. Gastroenterology. 2019;156(2):461-76 e1.

Publication types

Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

Substances

Actions

LinkOut - more resources

[1] Stockdale AJ, Kreuels B, Henrion MYR, et al. The global prevalence of hepatitis D virus infection: systematic review and meta-analysis. J Hepatol. 2020;73(3):523-532.

[2] Stockdale AJ, Kreuels B, Henrion MYR, et al. The global prevalence of hepatitis D virus infection: systematic review and meta-analysis. J Hepatol. 2020;73(3):523-532.

[3] Chen HY, Shen DT, Ji DZ, et al. Prevalence and burden of hepatitis D virus infection in the global population: a systematic review and meta-analysis. Gut. 2019;68(3):512-521.

[4] Chen HY, Shen DT, Ji DZ, et al. Prevalence and burden of hepatitis D virus infection in the global population: a systematic review and meta-analysis. Gut. 2019;68(3):512-521.

[5] Kushner T, Serper M, Kaplan DE. Delta hepatitis within the veterans affairs medical system in the United States: prevalence, risk factors, and outcomes. J Hepatol. 2015;63(3):586-592.

[6] Kushner T, Serper M, Kaplan DE. Delta hepatitis within the veterans affairs medical system in the United States: prevalence, risk factors, and outcomes. J Hepatol. 2015;63(3):586-592.

[7] Le Gal F, Brichler S, Sahli R, Chevret S, Gordien E. First international external quality assessment for hepatitis delta virus RNA quantification in plasma. Hepatology. 2016;64(5):1483-1494.

[8] Le Gal F, Brichler S, Sahli R, Chevret S, Gordien E. First international external quality assessment for hepatitis delta virus RNA quantification in plasma. Hepatology. 2016;64(5):1483-1494.

[9] Koh C, Heller T, Glenn JS. Pathogenesis of and new therapies for hepatitis D. Gastroenterology. 2019;156(2):461-76 e1.

[10] Koh C, Heller T, Glenn JS. Pathogenesis of and new therapies for hepatitis D. Gastroenterology. 2019;156(2):461-76 e1.

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

Hepatitis delta infection among persons living with HIV in Europe

Collaborators

Affiliations

Hepatitis delta infection among persons living with HIV in Europe

Authors

Collaborators

Affiliations

Abstract

Similar articles

Cited by

References

REFERENCES

Publication types

MeSH terms

Substances

LinkOut - more resources

Full Text Sources

Medical

Abstract

Similar articles

Cited by

References

REFERENCES

Publication types

MeSH terms

Substances

Related information

LinkOut - more resources

Full Text Sources

Medical