Epidemiological and molecular characterization of HBV and HCV infections in HIV-1-infected inmate population in Italy: a 2017-2019 multicenter cross-sectional study.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
09 09 2023
09 09 2023
Historique:
received:
14
03
2023
accepted:
31
08
2023
medline:
11
9
2023
pubmed:
10
9
2023
entrez:
9
9
2023
Statut:
epublish
Résumé
HBV/HCV co-infection is common in HIV-1-infected prisoners. To investigate the characteristics of HIV co-infections, and to evaluate the molecular heterogeneity of HIV, HBV and HCV in prisoners, we carried-out a multicenter cross-sectional study, including 65 HIV-1-infected inmates enrolled in 5 Italian detention centers during the period 2017-2019. HIV-1 subtyping showed that 77.1% of inmates were infected with B subtype and 22.9% with non-B subtypes. Italian nationals were all infected with subtype B (93.1%), except two individuals, one infected with the recombinant form CRF72_BF1, and the other with the HIV-1 sub-subtype A6, both previously not identified in inmates of Italian nationality. Non-Italian nationals were infected with subtype B (52.6%), CRFs (36.8%) and sub-subtypes A1 and A3 (5.2%). HIV variants carrying resistance mutations to NRTI, NNRTI, PI and InSTI were found in 7 inmates, 4 of which were never exposed to the relevant classes of drugs associated with these mutations. HBV and/or HCV co-infections markers were found in 49/65 (75.4%) inmates, while 27/65 (41.5%) showed markers of both HBV and HCV coinfection. Further, Italian nationals showed a significant higher presence of HCV markers as compared to non-Italian nationals (p = 0.0001). Finally, HCV phylogenetic analysis performed in 18 inmates revealed the presence of HCV subtypes 1a, 3a, 4d (66.6%, 16.7% and 16.7%, respectively). Our data suggest the need to monitor HIV, HBV and HCV infections in prisons in order to prevent spreading of these viruses both in jails and in the general population, and to implement effective public health programs that limit the circulation of different genetic forms as well as of viral variants with mutations conferring resistance to treatment.
Identifiants
pubmed: 37689795
doi: 10.1038/s41598-023-41814-x
pii: 10.1038/s41598-023-41814-x
pmc: PMC10492787
doi:
Types de publication
Multicenter Study
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
14908Informations de copyright
© 2023. Springer Nature Limited.
Références
Dolan, K. et al. Global burden of HIV, viral hepatitis, and tuberculosis in prisoners and detainees. The Lancet 388, 1089–1102 (2016).
doi: 10.1016/S0140-6736(16)30466-4
Dolan, K. et al. HIV in prison in low-income and middle-income countries. Lancet Infect. Dis. 7, 32–41 (2007).
pubmed: 17182342
doi: 10.1016/S1473-3099(06)70685-5
Babudieri, S. B. et al. Correlates of HIV, HBV, and HCV infections in a prison inmate population: Results from a multicentre study in Italy. J. Med. Virol. 76, 311–317 (2005).
pubmed: 15902712
doi: 10.1002/jmv.20375
Maggiorella, M. T. et al. Italian network for HIV characterization. High HIV-1 diversity in immigrants resident in Italy (2008–2017). Sci. Rep. 10, 3226 (2020).
pubmed: 32094387
pmcid: 7039940
doi: 10.1038/s41598-020-59084-2
Lai, A. et al. Changing patterns in HIV-1 non-B clade prevalence and diversity in Italy over three decades. HIV Med. 11, 593–602 (2010).
pubmed: 20408891
doi: 10.1111/j.1468-1293.2010.00832.x
Ciccozzi, M. et al. HIV-1 non-B subtypes in Italy: A growing trend. New Microbiol. 5, 377–386 (2012).
Lorenzin, G. et al. Prevalence of non-B HIV-1 subtypes in North Italy and analysis of transmission clusters based on sequence data analysis. Microorganisms. 23;8(1), 36 (2019).
Sarmati, L. & Malagnino, V. HBV infection in HIV-driven immune suppression. Viruses 11, 1077 (2019).
pubmed: 31752284
pmcid: 6893694
doi: 10.3390/v11111077
Merchante, N., Jiménez-Saenz, M. & Pineda, J. A. Management of HCV-related end-stage liver disease in HIV-coinfected patients. AIDS Rev. 9, 131–139 (2007).
pubmed: 17982938
Kim, H. N. et al. Treatment of HCV in Persons with HIV Coinfection. Hepatitis C Online. https://www.hepatitisc.uw.edu/go/key-populations-situations/treatment-hiv-coinfection/core-concept/all . Last updated: February 17th (2021).
Moron- Lopez, S. et al. Short-term treatment with interferon alfa diminishes expression of HIV-1 and reduces CD4+ T-cell activation in patients coinfected with HIV and hepatitis C virus and receiving antiretroviral therapy. J. Infect. Dis. 213(6), 1008–12 (2016).
pubmed: 26525407
doi: 10.1093/infdis/jiv521
Curry, M. P. HIV and hepatitis C virus: Special concerns for patients with cirrhosis. J. Infect. Dis. 207, 40–44 (2013).
doi: 10.1093/infdis/jis763
Platt, L. et al. Prevalence and burden of HBV co-infection among people living with HIV: A global systematic review and meta-analysis. J. Viral Hepat. 27, 294–315 (2019).
pubmed: 31603999
pmcid: 7383613
doi: 10.1111/jvh.13217
Platt, L., Easterbrook, P., Gower, E., McDonald, B. & Sabin, K. Prevalence and burden of HCV co-infection in people living with HIV: A global systematic review and meta-analysis. Lancet Infect. Dis. 16, 797–808 (2016).
pubmed: 26922272
doi: 10.1016/S1473-3099(15)00485-5
Bick, J. A. Infection control in jails and prisons. Clin. Infect. Dis. 45, 1047–1055 (2007).
pubmed: 17879924
doi: 10.1086/521910
Falla, A. M. et al. Hepatitis B/C in the countries of the EU/EEA: A systematic review of the prevalence among at-risk groups. BMC Infect. Dis. 18, 79 (2018).
pubmed: 29433454
pmcid: 5809955
doi: 10.1186/s12879-018-2988-x
Ahmadi Gharaei, H. et al. The global and regional prevalence of hepatitis C and B co-infections among prisoners living with HIV: A systematic review and meta-analysis. Infect. Dis. Poverty 10, 93 (2021).
pubmed: 34210349
pmcid: 8252262
doi: 10.1186/s40249-021-00876-7
Sagnelli, E. et al. Blood born viral infections, sexually transmitted diseases and latent tuberculosis in italian prisons: A preliminary report of a large multicenter study. Eur. Rev. Med. Pharmacol. Sci. 16, 2142–2146 (2012).
pubmed: 23280032
Stasi, C., Silvestri, C., Fanti, E., Di Fiandra, T. & Voller, F. Prevalence and features of chronic viral hepatitis and HIV coinfection in Italian prisons. Eur. J. Intern. Med. 34, 21–22 (2016).
doi: 10.1016/j.ejim.2016.04.020
Pontali, E. et al. Treatment with direct-acting antivirals in a multicenter cohort of HCV-infected inmates in Italy. Int. J. Drug Policy 59, 50–53 (2018).
pubmed: 29986272
doi: 10.1016/j.drugpo.2018.06.017
Zuccaro, O. et al. Clinical, epidemiological and virological features of acute hepatitis B in Italy. Infection 43, 431–441 (2015).
pubmed: 25697541
doi: 10.1007/s15010-015-0747-0
Coppola, N. et al. Factors affecting the changes in molecular epidemiology of acute hepatitis B in a Southern Italian area. J. Viral Hepat. 17, 493–500 (2010).
pubmed: 19780943
Sagnelli, E., Sagnelli, C., Pisaturo, M., Macera, M. & Coppola, N. Epidemiology of acute and chronic hepatitis B and delta over the last 5 decades in Italy. World J. Gastroenterol. 20, 7635–7643 (2014).
pubmed: 24976701
pmcid: 4069292
doi: 10.3748/wjg.v20.i24.7635
Quaranta, M. G. et al. Clinical features and comorbidity pattern of HCV infected migrants compared to native patients in care in Italy: A real-life evaluation of the PITER cohort. Dig. Liver Dis. 53, 1603–1609 (2021).
pubmed: 33893040
doi: 10.1016/j.dld.2021.03.020
Babudieri, S. et al. HIV e infezioni correlate negli Istituti Penitenziari Italiani: Note di epidemiologia e di organizzazione sanitaria. Ann. Ist Super. Sanità 39, 251–257 (2003).
pubmed: 14587225
Dell’Isola, S. et al. Detention and incompatibility of HIV patients in Italy. Ann. Ist Super. Sanità 49, 332–333 (2013).
pubmed: 24334775
Hemelaar, J. et al. Global and regional epidemiology of HIV-1 recombinants in 1990–2015: A systematic review and global survey. Lancet HIV 7, 772–781 (2020).
doi: 10.1016/S2352-3018(20)30252-6
Hemelaar, J. et al. Country level diversity of the HIV-1 pandemic between 1990 and 2015. J. Virol. 95, e01580-e1620 (2020).
pubmed: 33087461
pmcid: 7944450
doi: 10.1128/JVI.01580-20
Bbosa, N., Kaleebu, P. & Ssemwanga, D. HIV subtype diversity worldwide. Curr. Opin. HIV AIDS 14, 153–160 (2019).
pubmed: 30882484
doi: 10.1097/COH.0000000000000534
Longo, B. et al. HIV-1 diversity among inmates of Italian Prisons. J. Med. Virol. 80, 1689–1694 (2008).
pubmed: 18712824
doi: 10.1002/jmv.21275
Sanarico, N. et al. Correlates of infection and molecular characterization of blood-borne HIV, HCV, and HBV infections in HIV-1 infected inmates in Italy: An observational cross-sectional study. Medicine (Baltimore) 95, e5257 (2016).
pubmed: 27858889
doi: 10.1097/MD.0000000000005257
Pessôa, R., De Freitas Carneiro Proietti, A. B., Busch, M. P. & Sanabani, S. S. Identification of a novel HIV-1 circulating recombinant form (CRF72_BF1) in deep sequencing data from blood donors in Southeastern Brazil. Genome Announc. 2, e00386-14 (2014).
pubmed: 24926043
pmcid: 4056286
doi: 10.1128/genomeA.00386-14
Abidi, S.H. et al. Origin and evolution of HIV-1 subtype A6. Plos One. 16 (2021).
Giovanetti, M., Ciccozzi, M., Parolin, C. & Borsetti, A. Molecular epidemiology of HIV-1 in African countries: A comprehensive overview. Pathogens 9(12), 1072 (2020).
pubmed: 33371264
pmcid: 7766877
doi: 10.3390/pathogens9121072
Pessoa, R. et al. Deep sequencing of HIV-1 near full-length proviral genomes identifies high rates of BF1 recombinants including two novel circulating recombinant forms (CRF) 70_BF1 and a disseminating 71_BF1 among blood donors in Pernambuco, Brazil. PLOS ONE 9, 11 (2014).
doi: 10.1371/journal.pone.0112674
Cañada, J. E. et al. Identification of a new HIV-1 BC intersubtype circulating recombinant form (CRF108_BC) in Spain. Viruses 13, 93 (2021).
pubmed: 33445523
pmcid: 7826730
doi: 10.3390/v13010093
Kim, M. H. et al. HIV antiretroviral resistance mutations among antiretroviral treatment-naive and -experienced patients in South Korea. AIDS Res. Hum. Retrovir. 29, 1617–1620 (2013).
pubmed: 23952717
pmcid: 3848436
doi: 10.1089/aid.2013.0184
Frentz, D. et al. Increase in transmitted resistance to non-nucleoside reverse transcriptase inhibitors among newly diagnosed HIV-1 infections in Europe. BMC Infect. Dis. 14, 407 (2014).
pubmed: 25047543
pmcid: 4223652
doi: 10.1186/1471-2334-14-407
Jiamsakul, A. et al. Transmitted drug resistance in recently infected HIV-positive Individuals from four urban locations across Asia (2007–2010)—TASER-S. AIDS Res. Ther. 12, 3 (2015).
pubmed: 25685169
pmcid: 4326480
doi: 10.1186/s12981-015-0043-1
Alexiev, I. et al. Low HIV-1 transmitted drug resistance in Bulgaria against a background of high clade diversity. J. Antimicrob. Chemother. 70, 1874–1880 (2015).
pubmed: 25652746
doi: 10.1093/jac/dkv011
Ndashimye, E., Reyes, P. S. & Arts, E. J. New antiretroviral inhibitors and HIV-1 drug resistance: More focus on 90% HIV-1 isolates?. FEMS Microbiol. Rev. 16(47), 1–22 (2023).
Pitman, M. C., Lau, J. S. Y., McMahon, J. H. & Lewin, S. R. Barriers and strategies to achieve a cure for HIV. Lancet HIV 5, e317–e328 (2018).
pubmed: 29893245
pmcid: 6559798
doi: 10.1016/S2352-3018(18)30039-0
Baxter, J. D. et al. Global HIV-1 transmitted drug resistance in the INSIGHT Strategic Timing of AntiRetroviral Treatment (START) trial. HIV Med. 16, 77–87 (2015).
pubmed: 25711326
pmcid: 4341921
doi: 10.1111/hiv.12236
Gupta, R. K. et al. HIV-1 drug resistance before initiation or re-initiation of first-line antiretroviral therapy in low-income and middle-income countries: A systematic review and meta-regression analysis. Lancet Infect. Dis. 18, 346–355 (2017).
pubmed: 29198909
doi: 10.1016/S1473-3099(17)30702-8
Bandera, A. et al. Phylogenies in ART: HIV reservoirs, HIV latency and drug resistance. Curr. Opin. Pharmacol. 48, 24–32 (2019).
pubmed: 31029861
doi: 10.1016/j.coph.2019.03.003
Chen, Q. et al. Deep-sequencing reveals broad subtype-specific HCV resistance mutations associated with treatment failure. Antivir. Res. 174, 104694 (2020).
pubmed: 31857134
doi: 10.1016/j.antiviral.2019.104694
Borghetti, A. et al. Transmitted drug resistance to NRTIs and risk of virological failure in naïve patients treated with integrase inhibitors. HIV Med. 22, 22–27 (2021).
pubmed: 32964671
doi: 10.1111/hiv.12956
Quashie, P. K. et al. Characterization of the R263K mutation in HIV-1 Integrase that confers low-level resistance to the second-generation Integrase strand transfer inhibitor Dolutegravir. J. Virol. 86, 2696–2705 (2012).
pubmed: 22205735
pmcid: 3302270
doi: 10.1128/JVI.06591-11
Garrido, C. et al. Broad phenotypic cross-resistance to elvitegravir in HIV-infected patients failing on raltegravir-containing regimens. Antimicrob. Agents Chemother. 56, 2873–2878 (2012).
pubmed: 22450969
pmcid: 3370736
doi: 10.1128/AAC.06170-11
Doyle, T. et al. Integrase inhibitor (INI) genotypic resistance in treatment-naive and raltegravir-experienced patients infected with diverse HIV-1 clades. J. Antimicrob. Chemother. 70, 3080–3086 (2015).
pubmed: 26311843
pmcid: 4613743
doi: 10.1093/jac/dkv243
De Francesco, M. A. et al. Prevalence of integrase strand transfer inhibitors resistance mutations in integrase strand transfer inhibitors-naive and -experienced HIV-1 infected patients: A single center experience. AIDS Res. Hum. Retrovir. 34, 570–574 (2018).
pubmed: 29631420
doi: 10.1089/aid.2018.0006
Alvarez, M. et al. Surveillance of transmitted drug resistance to integrase inhibitors in Spain: Implications for clinical practice. J. Antimicrob. Chemother. 74, 1693–1700 (2019).
pubmed: 30838386
doi: 10.1093/jac/dkz067
Lepik, K. J. et al. Emergent drug resistance with integrase strand transfer inhibitor-based regimens. AIDS 31, 1425–1434 (2017).
pubmed: 28375875
doi: 10.1097/QAD.0000000000001494
Van Herck, K., Leuridan, E. & Van Damme, P. Schedules for hepatitis B vaccination of risk groups: Balancing immunogenicity and compliance. Sex. Transm. Infect. 83, 426–432 (2007).
pubmed: 17911142
pmcid: 2598703
doi: 10.1136/sti.2006.022111
Stasi, C. et al. Screening for hepatitis B virus and accelerated vaccination schedule in prison: A pilot multicenter study. Vaccine 37, 1412–1417 (2019).
pubmed: 30733091
doi: 10.1016/j.vaccine.2019.01.049
Chang, J. J., Mohtashemi, N. & Bhattacharya, D. Significance and management of isolated hepatitis B core antibody (anti-HBc) in HIV and HCV: Strategies in the DAA era. Curr. HIV/AIDS Rep. 15, 172–181 (2018).
pubmed: 29572624
pmcid: 6039383
doi: 10.1007/s11904-018-0379-y
Wu, T., Kwok, R. M. & Tran, T. T. Isolated anti-HBc: The relevance of hepatitis B core antibody—A review of new issues. Am. J. Gastroenterol. 112, 1780–1788 (2017).
pubmed: 29087395
doi: 10.1038/ajg.2017.397
Stroffolini, T. et al. Hepatitis C virus infection among drug addicts in Italy. J. Med. Virol. 84, 1608–1612 (2012).
pubmed: 22930509
doi: 10.1002/jmv.23370
Gardini, I., Bartoli, M., Conforti, M., Mennini, F. S. & Marcellusi, A. Estimation of the number of HCV-positive patients in Italy. PLoS ONE 14, e0223668 (2019).
pubmed: 31671120
pmcid: 6822946
doi: 10.1371/journal.pone.0223668
Kondili, L. A. et al. Estimated prevalence of undiagnosed HCV infected individuals in Italy: A mathematical model by route of transmission and fibrosis progression. Epidemics 34, 100442 (2021).
pubmed: 33607538
doi: 10.1016/j.epidem.2021.100442
Schmidt, J., Blum, H. E. & Thimme, R. T-cell responses in hepatitis B and C virus infection: Similarities and differences. Emerg. Microbes Infect. 2, e15 (2013).
pubmed: 26038456
pmcid: 3630955
doi: 10.1038/emi.2013.14
Giuliani, R. et al. HCV micro-elimination in two prisons in Milan, Italy: A model of care. J. Viral Hepat. 27, 1444–1454 (2020).
pubmed: 32815623
doi: 10.1111/jvh.13376
Rodríguez-Tajes, S. et al. Significant decrease in the prevalence of hepatitis C infection after the introduction of direct acting antivirals. J. Gastroenterol. Hepatol. 35, 1570–1578 (2020).
pubmed: 31957902
doi: 10.1111/jgh.14984
Fiore, V. et al. Chronic viral hepatitis in the Italian prison setting: Prevalence, outcomes, literature needs and perspectives. Healthcare 9, 1186 (2021).
pubmed: 34574960
pmcid: 8467805
doi: 10.3390/healthcare9091186
Tresó, B. et al. Molecular epidemiology of hepatitis C virus genotypes and subtypes among injecting drug users in Hungary. Euro Surveill. 18, 20639 (2013).
pubmed: 24300886
doi: 10.2807/1560-7917.ES2013.18.47.20639
Salemovic, D. et al. Intravenous drug use - an independent predictor for HCV genotypes 3 and 4 infection among HIV/HCV co-infected patients. Arch. Med. Sci. 13, 652–658 (2017).
pubmed: 28507583
pmcid: 5420631
doi: 10.5114/aoms.2017.66022
Tyczyno, M., Halota, W., Nowak, W. & Pawlowska, M. Distribution of HCV genotypes in the populations of inmates in polish prison Potulice and patients hospitalised in Bydgoszcz. Hepat. Mon. 14, e14559 (2014).
pubmed: 24910703
pmcid: 4030260
doi: 10.5812/hepatmon.14559
Petruzziello, A. et al. Nine-year distribution pattern of hepatitis C virus (HCV) genotypes in Southern Italy. PLoS ONE 14, e0212033 (2019).
pubmed: 30785909
pmcid: 6382136
doi: 10.1371/journal.pone.0212033
Bon, I. et al. Genotypic resistance in plasma and peripheral blood lymphocytes in a group of naive HIV1 patients. J. Clin. Virol. 38, 313–320 (2007).
pubmed: 17306618
doi: 10.1016/j.jcv.2006.12.018
Kwon, E. H. et al. HIV-1 subtypes and drug resistance mutations among female sex workers varied in different cities and regions of the Democratic Republic of Congo. PLoS ONE 15, e0228670 (2020).
pubmed: 32045455
pmcid: 7012409
doi: 10.1371/journal.pone.0228670
Chew, C. B. et al. Assessment of drug resistance mutations in plasma and peripheral blood mononuclear cells at different plasma viral loads in patients receiving HAART. J. Clin. Virol. 33, 206–216 (2005).
pubmed: 15911442
doi: 10.1016/j.jcv.2004.11.006
Arias, A. et al. Sanger and next generation sequencing approaches to evaluate HIV-1 virus in blood compartments. Int. J. Environ. Res. Public Health 15, 1697 (2018).
pubmed: 30096879
pmcid: 6122037
doi: 10.3390/ijerph15081697
Manyana, S. et al. HIV-1 drug resistance genotyping in resource limited settings: Current and future perspectives in sequencing technologies. Viruses 13(6), 1125 (2021).
pubmed: 34208165
pmcid: 8230827
doi: 10.3390/v13061125
Fokam, J. et al. Performance evaluation of an in house human immunodeficiency virus type-1 protease-reverse transcriptase genotyping assay in Cameroon. Arch. Virol. 156, 1235–1243 (2011).
pubmed: 21465085
doi: 10.1007/s00705-011-0982-3
Giovanetti, M. et al. Analysis of HIV-1 integrase genotypes and polymorphisms among integrase inhibitors-based antiretroviral treatment naïve patients in South Sudan. J. Med. Virol. 94, 3320–3327 (2022).
pubmed: 35277871
doi: 10.1002/jmv.27713
Pybus, O. G. et al. Genetic history of hepatitis C virus in East Asia. J. Virol. 83, 1071–1082 (2009).
pubmed: 18971279
doi: 10.1128/JVI.01501-08
Hall, T. A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98 (1999).
Nei, M. & Kumar, S. Molecular Evolution and Phylogenetics (Oxford University Press, 2000).
doi: 10.1093/oso/9780195135848.001.0001
Bennett, D. E. et al. Drug resistance mutations for surveillance of transmitted HIV-1 drug-resistance: 2009 update. PLoS ONE 4, e4724 (2009).
pubmed: 19266092
pmcid: 2648874
doi: 10.1371/journal.pone.0004724
Wensing, A. M. et al. 2019 update of the drug resistance mutations in HIV-1. Top. Antivir. Med. 27, 111–121 (2019).
pubmed: 31634862
pmcid: 6892618