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1
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Bazie MM, Sanou M, Djigma FW, Compaore TR, Obiri-Yeboah D, Kabamba B, Nagalo BM, Simpore J, Ouédraogo R. Genetic diversity and occult hepatitis B infection in Africa: A comprehensive review. World J Hepatol 2024; 16:843-859. [PMID: 38818293 PMCID: PMC11135261 DOI: 10.4254/wjh.v16.i5.843] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/14/2023] [Revised: 02/06/2024] [Accepted: 04/15/2024] [Indexed: 05/22/2024] Open
Abstract
BACKGROUND Occult hepatitis B infection (OBI) is a globally prevalent infection, with its frequency being influenced by the prevalence of hepatitis B virus (HBV) infection in a particular geographic region, including Africa. OBI can be transmitted through blood transfusions and organ transplants and has been linked to the development of hepatocellular carcinoma (HCC). The associated HBV genotype influences the infection. AIM To highlight the genetic diversity and prevalence of OBI in Africa. METHODS This systematic review followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines and involved a comprehensive search on PubMed, Google Scholar, Science Direct, and African Journals Online for published studies on the prevalence and genetic diversity of OBI in Africa. RESULTS The synthesis included 83 articles, revealing that the prevalence of OBI varied between countries and population groups, with the highest prevalence being 90.9% in patients with hepatitis C virus infection and 38% in blood donors, indicating an increased risk of HBV transmission through blood transfusions. Cases of OBI reactivation have been reported following chemotherapy. Genotype D is the predominant, followed by genotypes A and E. CONCLUSION This review highlights the prevalence of OBI in Africa, which varies across countries and population groups. The study also demonstrates that genotype D is the most prevalent.
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Affiliation(s)
- Michee M Bazie
- Department of Medicine, Transmissible Diseases Laboratory, Université Joseph KI-ZERBO, Ouagadougou 0000, Burkina Faso
| | - Mahamoudou Sanou
- Department of Medicine, Transmissible Diseases Laboratory, Université Joseph KI-ZERBO, Ouagadougou 0000, Burkina Faso
| | - Florencia Wendkuuni Djigma
- Department of Biochemistry and Microbiology, Molecular Biology and Genetics Laboratory, University Joseph KI-ZERBO, Ouagadougou 0000, Burkina Faso.
| | - Tegwinde Rebeca Compaore
- Infectious and parasitic disease Laboratory, Health Sciences Research Institute, IRSS/CNRST, National Center for Scientific and Technological Research, Ouagadougou 0000, Burkina Faso
| | - Dorcas Obiri-Yeboah
- Department of Microbiology and Immunology, School of Medical Sciences, University of Cape Coast, PMB, Cape Coast 0000, Ghana
| | - Benoît Kabamba
- Department of Clinical Biology, Virology Laboratory, Cliniques Universitaires Saint Luc, Université Catholique de Louvain, Bruxelles 0000, Belgium
| | | | - Jacques Simpore
- Department of Biochemistry and Microbiology, Molecular Biology and Genetics Laboratory, University Joseph KI-ZERBO, Ouagadougou 0000, Burkina Faso
| | - Rasmata Ouédraogo
- Department of Medicine, Transmissible Diseases Laboratory, Université Joseph KI-ZERBO, Ouagadougou 0000, Burkina Faso
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Sobajo OA, George UE, Osasona OG, Eromon P, Aborisade OY, Ajayi OD, Folarin OA, Komolafe IOO. Seroprevalence, co-infection and risk of transmission of Hepatitis B and D virus among hospital attendees in two South-western states in Nigeria. J Immunoassay Immunochem 2023; 44:133-146. [PMID: 36369932 DOI: 10.1080/15321819.2022.2141578] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/13/2022]
Abstract
Infection with both Hepatitis B (HBV) and D (HDV) virus causes more severe liver damage than HBV alone. Superinfections among chronic HBV infected cohorts often lead to HDV persistence with rapid progression to cirrhosis, necessitating continuous surveillance to determine their prevalence and relative contribution to liver pathology. A cross-sectional study among hospital outpatients in Ekiti and Osunstates was conducted using random sampling technique. Blood samples were collected from 410 participants and tested for HBV serological markers. All samples positive for HBsAg samples were tested for Hepatitis D virus antigen (HDAg), serum anti-HDV IgM, and serum anti-HDV IgG using enzyme-linked immunosorbent assay kits. The prevalence of HBV infection among the 410 samples was 12.4% (CI 9.5-15.9). Past HBV exposure was detected in 120 (29.2%), while 147(35.8%) were susceptible to HBV infection. Among the HBsAg positive individuals, 9.8% were hepatitis D antigen (HDAg) positive, while 3.9% and 1.9% were positive for IgG anti-HDV and IgM anti-HDV, respectively. Risk factors associated with HBV infections in this study were multiple sexual partners and sharing of sharp objects. Our investigation has verified the endemicity of HBV in Nigeria and revealed that HBV- HDV co-infection is highly prevalent in south-west Nigeria.
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Affiliation(s)
- Oguntope A Sobajo
- Department of Biological Sciences, Faculty of Natural Sciences, Redeemer's University, Ede, Nigeria.,African Centre of Excellence for Genomics of Infectious Diseases, Redeemer's University, Ede, Nigeria.,Department of Biological Sciences, Afe Babalola University, Ado-Ekiti, Nigeria
| | - Uwem E George
- Department of Biological Sciences, Faculty of Natural Sciences, Redeemer's University, Ede, Nigeria.,African Centre of Excellence for Genomics of Infectious Diseases, Redeemer's University, Ede, Nigeria
| | - Oluwadamilola G Osasona
- Department of Biological Sciences, Faculty of Natural Sciences, Redeemer's University, Ede, Nigeria.,African Centre of Excellence for Genomics of Infectious Diseases, Redeemer's University, Ede, Nigeria
| | - Philomena Eromon
- African Centre of Excellence for Genomics of Infectious Diseases, Redeemer's University, Ede, Nigeria
| | - Olamide Y Aborisade
- Haematology and Blood Transfusion Service Department, UNIOSUN Teaching Hospital, Osogbo, Nigeria
| | - Oluwafemi D Ajayi
- Department of Medical Laboratory Science, Afe Babalola University, Ado-Ekiti, Nigeria
| | - Onikepe A Folarin
- Department of Biological Sciences, Faculty of Natural Sciences, Redeemer's University, Ede, Nigeria.,African Centre of Excellence for Genomics of Infectious Diseases, Redeemer's University, Ede, Nigeria
| | - Isaac O O Komolafe
- Department of Biological Sciences, Faculty of Natural Sciences, Redeemer's University, Ede, Nigeria
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3
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Ondigui JLN, Kenmoe S, Kengne-Ndé C, Ebogo-Belobo JT, Takuissu GR, Kenfack-Momo R, Mbaga DS, Tchatchouang S, Kenfack-Zanguim J, Fogang RL, Menkem EZ, Kame-Ngasse GI, Magoudjou-Pekam JN, Bowo-Ngandji A, Goumkwa NM, Esemu SN, Ndip L, Essama SHR, Torimiro J. Epidemiology of occult hepatitis B and C in Africa: A systematic review and meta-analysis. J Infect Public Health 2022; 15:1436-1445. [PMID: 36395668 PMCID: PMC7613883 DOI: 10.1016/j.jiph.2022.11.008] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/06/2022] [Revised: 11/04/2022] [Accepted: 11/08/2022] [Indexed: 11/13/2022] Open
Abstract
BACKGROUND Occult hepatitis B (OBI) and C (OCI) infections lead to hepatic crises including cases of liver cirrhosis and even hepatocellular carcinoma (HCC). OBI and OCI also pose a significant problem of their transmissibility. This study aimed to assess the overall prevalence of OBI and OCI in the African continent, a region highly endemic for classical hepatitis B and C viruses. METHODS For this systematic review and meta-analysis, we searched: PubMed, Web of Science, African Journal Online and African Index Medicus for published studies on the prevalence of OBI and OCI in Africa. Study selection and data extraction were performed by at least two independent investigators. Heterogeneity (I²) was assessed using the χ² test on the Cochran Q statistic and H parameters. Sources of heterogeneity were explored by subgroup analyses. This study was registered in PROSPERO, with reference number CRD42021252772. RESULTS We obtained 157 prevalence data for this meta-analysis, from 134 studies for OBI prevalence; 23 studies on OCI prevalence, and a single study on the OBI case fatality rate. The overall estimate for the prevalence of OBI was 14.8% [95% CI = 12.2-17.7] among 18579 participants. The prevalence of seronegative OBI and seropositive OBI was 7.4% [95% CI = 3.8-11.8] and 20.0% [95% CI = 15.3-25.1] respectively. The overall estimate for the prevalence of OCI was 10.7% [95% CI = 6.6-15.4] among 2865 participants. The pooled prevalence of seronegative OCI was estimated at 10.7% [95%CI = 4.8-18.3] and that of seropositive OCI at 14.4% [95%CI = 5.2-22.1]. In Sub-group analysis, patients with malignancies, chronic hepatitis C, and hemodialysis had a higher OCI prevalence. While those with malignancies, liver disorders, and HIV positive registered highest OBI prevalence. CONCLUSION This review shows a high prevalence of OBI and OCI in Africa, with variable prevalence between countries and population groups.
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Affiliation(s)
- Juliette Laure Ndzie Ondigui
- Department of Microbiology, The University of Yaounde I, Yaounde, Cameroon; Molecular Biology Laboratory, Chantal Biya International Reference Centre for AIDS Research (CIRCB), Yaounde, Cameroon
| | - Sebastien Kenmoe
- Department of Microbiology and Parasitology, University of Buea, Buea, Cameroon.
| | - Cyprien Kengne-Ndé
- Epidemiological Surveillance, Evaluation and Research Unit, National AIDS Control Committee, Douala, Cameroon
| | - Jean Thierry Ebogo-Belobo
- Medical Research Centre, Institute of Medical Research and Medicinal Plants Studies, Yaounde, Cameroon
| | - Guy Roussel Takuissu
- Centre for Food, Food Security and Nutrition Research, Institute of Medical Research and Medicinal Plants Studies, Yaounde, Cameroon
| | - Raoul Kenfack-Momo
- Department of Biochemistry, The University of Yaounde I, Yaounde, Cameroon
| | | | | | | | | | | | - Ginette Irma Kame-Ngasse
- Medical Research Centre, Institute of Medical Research and Medicinal Plants Studies, Yaounde, Cameroon
| | | | - Arnol Bowo-Ngandji
- Department of Microbiology, The University of Yaounde I, Yaounde, Cameroon
| | - Nadège Mafopa Goumkwa
- Molecular Biology Laboratory, Chantal Biya International Reference Centre for AIDS Research (CIRCB), Yaounde, Cameroon
| | | | - Lucy Ndip
- Department of Microbiology and Parasitology, University of Buea, Buea, Cameroon
| | | | - Judith Torimiro
- Molecular Biology Laboratory, Chantal Biya International Reference Centre for AIDS Research (CIRCB), Yaounde, Cameroon
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Kajogoo VD, Swai SS, Gurung S. Prevalence of occult hepatitis B among HIV-positive individuals in Africa: A systematic review and meta-analysis. SAGE Open Med 2022; 10:20503121211072748. [PMID: 35127096 PMCID: PMC8808011 DOI: 10.1177/20503121211072748] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/27/2021] [Accepted: 12/20/2021] [Indexed: 12/16/2022] Open
Abstract
The prevalence of hepatitis B virus among HIV-seropositive individuals is believed to be high, and yet the disease remains neglected in many areas of the continent. Little is known about occult hepatitis in HIV individuals. This review assessed occult hepatitis B infection and its prevalence in the different regions of the African continent. It also determines its prevalence in the HIV population which is endemic in the region. Studies were searched from the Cochrane, google scholar, PubMed/Medline, and African Journals online. Authors included cross-sectional studies, case controls, and cohorts, from 2010 to January 2021, following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses and Participants, Interventions, Comparisons, Outcomes, and Study design frameworks to develop the search strategy. All studies had participants who were HIV-positive, covering different regions of the continent. Risk ratio was used to measure effect size, and Stata 14 software was used for analysis. Eleven studies met the eligibility criteria, with 2567 participants. Overall prevalence of occult hepatitis B was 11.2%. Regional prevalence was 26.5% for the south, 11% for the north, 9.1% for the east, and 8.5% for the western region. Approximately 10% of HIV-seropositive individuals were co-infected with occult hepatitis B virus. Regionally, the prevalence was highest in the southern region and lowest in the west. The prevalence of occult HBV infection was compared between the southern region and the other regions. It was higher in the south compared to the east (risk ratio = 0.87, 95% confidence interval (0.83–0.91)). It was also higher in the south compared to the north (risk ratio = 0.82, 95% confidence interval (0.79–0.85)), and it was also higher in the south compared to the west (risk ratio = 0.85, 95% confidence interval (0.82–0.87)). Public health measures and interventions are required to raise awareness, increase prevention, and reduce spread of the disease. More evidence-based studies need to be carried out.
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Affiliation(s)
| | - Sylivia Sarah Swai
- School of public health, Muhimbili University of health and Allied Sciences (MUHAS), Dar es Salaam, Tanzania
| | - Sanyukta Gurung
- Department of Clinical Physiology, Maharajgunj Medical Campus, Tribhuvan University Teaching Hospital, Institute of Medicine, Maharajgunj, Nepal
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Osasona OG, Adewale-Fashoro O, Olumade TJ, Oguzie J, George U, Ariyo OE, Oguntoye OO. Comparative serologic profiles of hepatitis B Virus (HBV) between HIV/HBV co-infected and Hbv mono-infected patients in Ile-Ife, Nigeria. J Immunoassay Immunochem 2021; 42:633-647. [PMID: 34029499 DOI: 10.1080/15321819.2021.1924197] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/11/2023]
Abstract
Hepatitis B virus (HBV) infects about 2 billion people globally and accounts for mortality of about 800,000 from liver cirrhosis and hepatocellular carcinoma. Sub-Saharan Africa accounts for 70% of the Human Immunodeficiency Virus (HIV) global burden. HIV/HBV co-infection results in the early development of HBV complications, alterations of serological biomarkers of HBV. Two hundred and fifty patients with HIV/AIDS were screened for HBV and 20 (8%) were identified. The same number of HBV mono-infected individuals were recruited into the study and subsequently, HBV serological profiles which include HBsAg, HBsAb, HBeAg, HBeAb, HBcAbIgM, and HBcAbIgG were assayed using HBV ELISA kits. Mean age of patients in the HBV/HIV cohort was 45.5 years while the HBV mono-infected infected cohort was 30.5 years. The majority of the HBV/HIV co-infected individuals were females (85%). The frequency of HBeAg among HIV/HBV co-infected cohort was 25% and 15% for HBV mono-infected, while the frequency of HBeAb was higher (60%) among the cohort of HBV/HIV co-infected patients in comparison with the HBV mono-infected cohorts (50%). Two patients among the HIV/HBV co-infected cohort have the isolated anti-HBcAg serologic pattern. The study broadened the available evidence of comparative serologic profiles of Hepatitis B virus between cohorts of HBV/HIV co-infected individuals and HBV mono-infected patients in Nigeria.
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Affiliation(s)
- Oluwadamilola Gideon Osasona
- African Centre of Excellence for Genomics of Infectious Diseases, Redeemers University, Ede, Nigeria.,Department of Biological Sciences, Redeemers University, Ede, Nigeria.,Hospitals Management Board, Ado-Ekiti, Nigeria
| | | | - Testimony J Olumade
- African Centre of Excellence for Genomics of Infectious Diseases, Redeemers University, Ede, Nigeria.,Department of Biological Sciences, Redeemers University, Ede, Nigeria
| | - Judith Oguzie
- African Centre of Excellence for Genomics of Infectious Diseases, Redeemers University, Ede, Nigeria.,Department of Biological Sciences, Redeemers University, Ede, Nigeria
| | - Uwem George
- African Centre of Excellence for Genomics of Infectious Diseases, Redeemers University, Ede, Nigeria.,Department of Biological Sciences, Redeemers University, Ede, Nigeria
| | - Olumuyiwa Elijah Ariyo
- Department of MedicineInfectious Diseases and Tropical Medicine Unit, Federal Teaching Hospital, Ido-Ekiti, Nigeria
| | - Oluwatosin Oluwagbenga Oguntoye
- Department of MedicineInfectious Diseases and Tropical Medicine Unit, Federal Teaching Hospital, Ido-Ekiti, Nigeria.,Department of Medicine, Ekiti State University, Ado-Ekiti, Nigeria
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6
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Malagnino V, Cerva C, Cingolani A, Ceccherini-Silberstein F, Vergori A, Cuomo G, Perno CF, Puoti M, d'Arminio Monforte A, Cozzi-Lepri A, Andreoni M, Sarmati L. HBcAb Positivity Increases the Risk of Severe Hepatic Fibrosis Development in HIV/HCV-Positive Subjects From the ICONA Italian Cohort of HIV-Infected Patients. Open Forum Infect Dis 2020; 8:ofaa566. [PMID: 33447635 PMCID: PMC7781466 DOI: 10.1093/ofid/ofaa566] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/16/2020] [Accepted: 11/11/2020] [Indexed: 11/13/2022] Open
Abstract
Background The aim of this study was to investigate the impact of anti-HBc (HBcAb) positivity on the progression of liver fibrosis (Fibrosis-4 score >3.25) in the Italian cohort of HIV-infected individuals naïve to antiretroviral treatment (ICONA). Methods All patients with FIB-4 <3.25 at baseline were evaluated prospectively: 6966 people with HIV (PWH) were screened and classified based on hepatitis B virus (HBV) and hepatitis C virus (HCV) serology. Results Patients who were HBcAb+/HCV-/HBs antigen (HBsAg)- and HCV+/HBcAb+/HBsAg- or HBsAg+/HBcAb+/HCV- had CD4+ cell counts below the nadir and significantly higher prevalence of AIDS diagnosis at baseline than the other groups (P < .0001). A Cox regression model adjusted for age, HIV transmission mode, country of birth, and alcohol consumption showed a higher relative risk (HR) of progression to FIB-4 >3.25 in HCV+/HBcAb+/HBsAg- patients (HR, 7.2; 95% CI, 3 8–13.64). Conclusions HBcAb+ contributes to liver damage in HIV+/HCV+/HBcAb+/HBsAg- subjects. A careful monitoring for signs of previous HBV infection is needed in this kind of patients.
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Affiliation(s)
| | | | | | | | | | | | | | - Massimo Puoti
- ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy
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Nnakenyi ID, Uchechukwu C, Nto-ezimah U. Prevalence of hepatitis B and C virus co-infection in HIV positive patients attending a health institution in southeast Nigeria. Afr Health Sci 2020; 20:579-586. [PMID: 33163019 PMCID: PMC7609124 DOI: 10.4314/ahs.v20i2.5] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/17/2022] Open
Abstract
BACKGROUND The health of people living with HIV/AIDS becomes progressively worse when co-infected with hepatitis B virus (HBV) and hepatitis C virus (HCV), resulting in shortened life span. The modes of transmission of HIV, HBV and HCV are similar. OBJECTIVE To determine the prevalence of HBV and HCV co-infection in HIV patients. METHOD This was a retrospective study of serology test results for hepatitis B surface antigen (HBsAg) and antibodies to HCV (anti-HCV) of HIV positive patients registered from 2008-2013 (6years) at the University of Nigeria Teaching Hospital. Adult patients with confirmed HIV seropositivity were included. Ethical approval was obtained and confidentiality of the patient information was maintained. Laboratory records were reviewed to obtain HBsAg, anti-HCV, and CD4 T-lymphocyte results. Prevalence was determined by the number of positive results over total number of patients tested. Chi-square test was used to determine relationships and p<0.05 was considered to be statistically significant. RESULTS 4663 HIV patient records were included comprising 3024 (65%) females and 1639 (35%) males. Serology results showed 365/4663 (7.8%) tested HBsAg-positive only; 219/4663 (4.7%) tested anti-HCV-positive only; and 27/4663 (0.58%) tested both HBsAg and anti-HCV-positive. Correlation of age and sex were statistically significant with HBV and HCV (p<0.05) but not CD4 count (p>0.05). CONCLUSION HBV co-infection was more prevalent than HCV, and triple infection was also observed. Screening for these viral infections in the HIV population is necessary for early identification to enable appropriate, holistic management of these patients.
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Affiliation(s)
- Ifeyinwa Dorothy Nnakenyi
- University of Nigeria Nsukka, Department of Chemical Pathology
- University of Nigeria Teaching Hospital, Department of Chemical Pathology
- Corresponding author: Ifeyinwa Dorothy Nnakenyi, University of Nigeria Nsukka, Department of Chemical Pathology; University of Nigeria Teaching Hospital, Department of Chemical Pathology. ,
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Calux SJ, Silva VCM, Compri AP, Lemos MF, Santos APDT, Oba IT, Mendes-Correa MCJ, Moreira RC. Hepatitis B: Prevalence and occult infection in HIV-infected patients. Rev Soc Bras Med Trop 2020; 53:e20180533. [PMID: 31994654 PMCID: PMC7083387 DOI: 10.1590/0037-8682-0533-2018] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/13/2018] [Accepted: 09/05/2019] [Indexed: 01/04/2023] Open
Abstract
INTRODUCTION HBV and HIV have identical transmission routes. The aim of this study was to determine the prevalence of HBV in HIV patients and to detect the presence of occult HBV infection. METHODS All samples were tested for serology markers and using qPCR. RESULTS This study included 232 individuals, out of which 36.6% presented with HBV markers and 11.8% presented with HBsAg or HBV-DNA, including 3 patients that showed OBI. CONCLUSIONS We observed a high prevalence of HBV among HIV patients. In addition, the results suggest that OBI can occur in patients with serological profiles that are indicative of past infection. Therefore, the application of molecular tests may enable the identification of infections that are not evident solely based on serology.
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Affiliation(s)
- Samira Julien Calux
- Laboratório de Hepatites Virais, Centro de Virologia, Instituto Adolfo Lutz, São Paulo, SP, Brasil
| | | | - Adriana Parise Compri
- Laboratório de Hepatites Virais, Centro de Virologia, Instituto Adolfo Lutz, São Paulo, SP, Brasil
| | | | | | - Isabel Takano Oba
- Laboratório de Hepatites Virais, Centro de Virologia, Instituto Adolfo Lutz, São Paulo, SP, Brasil
| | | | - Regina Célia Moreira
- Laboratório de Hepatites Virais, Centro de Virologia, Instituto Adolfo Lutz, São Paulo, SP, Brasil
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9
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Tajik Z, Bokharaei-Salim F, Ghorbani S, Keyvani H, Esghaei M, Monavari SH, Ataei-Pirkooh A, Garshasbi S, Donyavi T, Fakhim A. Detection of HBV genome in the plasma and peripheral blood mononuclear cells of Iranian HBsAg negative patients with HIV infection: occult HBV infection. Arch Virol 2018; 163:1559-1566. [PMID: 29476259 DOI: 10.1007/s00705-018-3740-y] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/30/2017] [Accepted: 12/28/2017] [Indexed: 01/05/2023]
Abstract
The presence of hepatitis B virus (HBV) DNA in the absence of traceable hepatitis B surface antigen (HBsAg) in the plasma specimen of patients is defined as occult HBV infection (OBI). This study aimed to detect HBV-DNA in the plasma and peripheral blood mononuclear cells (PBMCs) of Iranian HBsAg negative patients with human immunodeficiency virus (HIV) infection. This cross-sectional study was conducted on 172 patients with HIV infection from September 2015 to August 2017. The patients were tested for serological parameters (HBsAg, HBcAb, HBeAg and HBeAb) against HBV infection. Moreover, they were tested for HBV viral load (using COBAS TaqMan 48 Kit, Roche, USA) in plasma and the presence of the HBV genome in PBMC specimens using real-time PCR. The mean age of the patients was 35.4 ± 13.4 years. Of the 172 studied patients, 109 (63.4%) were male. In this study, 151 (87.8%) patients were negative for HBsAg, 111 (64.5%) patients were negative for all HBV infection serological markers, 9 (5.2%) patients were only positive for HBsAg and 29 (16.9%) patients were only positive for HBcAb. Moreover, five (3.3%) patients with HBsAg negative had OBI (in the plasma sample of four patients and PBMC specimens of all five patients, HBV-DNA was detected). The present study revealed that 3.3% of the patients with HIV infection had occult HBV infection. Presumably, designing prospective studies to identify this infection in patients with HIV infection is informative and valuable.
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Affiliation(s)
- Zahra Tajik
- HIV Laboratory of National Center, Iran University of Medical Sciences, Tehran, Iran
| | - Farah Bokharaei-Salim
- HIV Laboratory of National Center, Iran University of Medical Sciences, Tehran, Iran. .,Department of Virology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran.
| | - Saied Ghorbani
- Department of Virology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
| | - Hossein Keyvani
- Department of Virology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
| | - Maryam Esghaei
- Department of Virology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
| | | | - Angila Ataei-Pirkooh
- Department of Virology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
| | - Saba Garshasbi
- HIV Laboratory of National Center, Iran University of Medical Sciences, Tehran, Iran
| | - Tahereh Donyavi
- HIV Laboratory of National Center, Iran University of Medical Sciences, Tehran, Iran
| | - Atousa Fakhim
- Department of Architectural Engineering, Faculty of Engineering, Islamic Azad University, South Tehran Branch, Tehran, Iran
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10
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Akintule O, Olusola B, Odaibo G, Olaleye D. Occult HBV Infection in Nigeria. ARCHIVES OF BASIC AND APPLIED MEDICINE 2018; 6:87-93. [PMID: 29963604 PMCID: PMC6022766] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Subscribe] [Scholar Register] [Indexed: 06/08/2023]
Abstract
Occult hepatitis B virus infection (OBI) is manifested by presence of HBV-DNA in the absence of detectable Hepatitis B surface antigen (HBsAg) with or without anti-HBV antibodies. Hence it is a potential threat in blood transfusion medicine. This study was carried out to determine the prevalence of OBI as well as evaluate the effectiveness of using Hepatitis B surface antigen (HBsAg) marker alone in the diagnosis of HBV infection among HBsAg negative blood donors in Ilorin, Nigeria. A purposive sampling, including samples from 206 already donated and prescreened blood units from HBsAg negative from apparently healthy volunteer blood donors at the General Hospital Blood Transfusion Centre, Ilorin, Nigeria, were collected for further laboratory analysis for this study. Five millilitres of blood was collected and plasma sample tested for the presence of HBsAg using a commercially available ELISA kit. In addition, Polymerase Chain Reaction (PCR) was used for molecular detection of HBV DNA in each of the samples. Data was analyzed using descriptive statistics, Chi square at p = 0.05. Of the 206 HBsAg Micropoint® rapid kits pre-screened seronegative samples collected from the blood transfusion centre, 8 (3.9%) samples were positive for the presence of HBsAg when retested using ELISA in the laboratory. Eighteen of the 206 samples (8.7%) were HBV-DNA positive by a semi-nested PCR technique giving an OBI rate of 8.7%. Out of the 18 HBV-DNA positive samples, 17 (4.4%) were from males and only one (5.6%) was from a female donor. Analysis of the 18 HBV DNA positive samples using genotype specific primers into genotype A and Non-A showed that 15 (83.3%) were HBV genotype A, while 2 (11.1%) were genotypes other than A (Non-A), one (5.6%) sample had mixed genotypes (A & non-A). A prevalence of 8.7% OBI found in this study indicates substantial risk of post transfusion HBV infection in the study area in Nigeria. Hence, the need to include HBV DNA detection in the routine blood screening that is, using Nucleic Acid Testing (NAT) technique for transfusion safety in the country.
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Affiliation(s)
- O.A. Akintule
- Department of Virology, College of Medicine, University of Ibadan, Nigeria
| | - B.A. Olusola
- Department of Virology, College of Medicine, University of Ibadan, Nigeria
| | - G.N. Odaibo
- Department of Virology, College of Medicine, University of Ibadan, Nigeria
| | - D.O. Olaleye
- Department of Virology, College of Medicine, University of Ibadan, Nigeria
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Ryan K, Anderson M, Gyurova I, Ambroggio L, Moyo S, Sebunya T, Makhema J, Marlink R, Essex M, Musonda R, Gaseitsiwe S, Blackard JT. High Rates of Occult Hepatitis B Virus Infection in HIV-Positive Individuals Initiating Antiretroviral Therapy in Botswana. Open Forum Infect Dis 2017; 4:ofx195. [PMID: 29062862 PMCID: PMC5641381 DOI: 10.1093/ofid/ofx195] [Citation(s) in RCA: 28] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/08/2017] [Accepted: 09/12/2017] [Indexed: 12/16/2022] Open
Abstract
Background Hepatitis B surface antigen (HBsAg)–negative but hepatitis B virus (HBV) DNA-positive infection—known as occult hepatitis B infection (OBI)—occurs in 1% to >15% of HIV-positive individuals in the United States and South Africa, respectively. However, there are no data on OBI from Botswana, a country known to be hyperendemic for chronic HBV infection and to have a significant HIV burden. Methods Two hundred seventy-two adults enrolled in an HIV treatment study of tenofovir/emtricitabine as the nucleoside backbone who were previously determined to be HBsAg negative were tested for HBV DNA at baseline and 1 year after initiation of highly active antiretroviral therapy (HAART). Results HBV DNA was detected in 72 of 272 (26.5%). Six individuals (8.3%) had HBV DNA levels greater than 200 IU/mL, and the highest viral load was 3280 IU/mL. Of 65 participants with OBI evaluated at 12 months after initiating HAART, only 1 (1.5%) had detectable HBV DNA. Conclusions Occult HBV infection is quite common in HIV-infected patients in Botswana, although its impact on the course of HIV disease progression is unknown. The suppression of occult HBV DNA levels by tenofovir/emtricitabine suggests an effective therapeutic option, although the long-term suppressive abilities remain unstudied.
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Affiliation(s)
- Kathleen Ryan
- University of Cincinnati College of Medicine, Cincinnati, Ohio
| | - Motswedi Anderson
- Botswana Harvard AIDS Institute Partnership, Gaborone, Botswana.,Department of Biological Sciences, University of Botswana, Gaborone, Botswana
| | - Ivayla Gyurova
- University of Cincinnati College of Medicine, Cincinnati, Ohio
| | | | - Sikhulile Moyo
- Botswana Harvard AIDS Institute Partnership, Gaborone, Botswana.,Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, Massachusetts
| | - Teresa Sebunya
- Department of Biological Sciences, University of Botswana, Gaborone, Botswana
| | - Joseph Makhema
- Botswana Harvard AIDS Institute Partnership, Gaborone, Botswana.,Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, Massachusetts
| | - Richard Marlink
- Botswana Harvard AIDS Institute Partnership, Gaborone, Botswana.,Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, Massachusetts
| | - Max Essex
- Botswana Harvard AIDS Institute Partnership, Gaborone, Botswana.,Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, Massachusetts
| | - Rosemary Musonda
- Botswana Harvard AIDS Institute Partnership, Gaborone, Botswana.,Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, Massachusetts
| | - Simani Gaseitsiwe
- Botswana Harvard AIDS Institute Partnership, Gaborone, Botswana.,Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, Massachusetts
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12
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Olotu AA, Oyelese AO, Salawu L, Audu RA, Okwuraiwe AP, Aboderin AO. Occult Hepatitis B virus infection in previously screened, blood donors in Ile-Ife, Nigeria: implications for blood transfusion and stem cell transplantation. Virol J 2016; 13:76. [PMID: 27150469 PMCID: PMC4859058 DOI: 10.1186/s12985-016-0533-3] [Citation(s) in RCA: 18] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/17/2016] [Accepted: 04/25/2016] [Indexed: 12/18/2022] Open
Abstract
BACKGROUND Hepatitis B virus (HBV) transmission through blood transfusion is reduced by screening for hepatitis B surface antigen (HBsAg). However this method cannot detect the presence of occult hepatitis B virus infection. This study sought to determine the prevalence of occult hepatitis B virus infection among blood donors in Ile-Ife, Nigeria. For the first time in Nigeria we employed an automated real-time PCR- method to investigate the prevalence of occult HBV in blood donors. METHODS Blood donors screened with HBsAg immunochromatographic rapid test kits at the blood transfusion units of two hospitals and found to be negative were recruited into the study. Questionnaires to elicit risk factors for HBV infection were administered and then 10 ml of blood was collected from each donor. Plasma samples obtained from these HBsAg negative blood donors were screened again for HBsAg using an enzyme-linked immunosorbent assay (ELISA) method, and those found negative were screened for the presence of total antibody to the HBV core antigen (anti-HBc) using ELISA method. Those positive to anti-HBc were then tested for HBV DNA, using an automated real-time PCR method. RESULTS Five hundred and seven blood donors found HBsAg negative by immunochromatographic rapid test kits at both blood transfusion units, were tested for HBsAg using ELISA and 5 (1 %) were HBsAg positive. The 502 found negative were tested for anti-HBc and 354 (70.5 %) were found positive implying previous exposure to HBV and 19 (5.4 %) of the 354 anti-HBc positive had HBV DNA signifying occult HBV infection. No risk factors were found to be associated with the presence of HBV DNA among those who tested positive. CONCLUSION Occult HBV infection exists in blood donors in Ile-Ife, Nigeria and the use of HBsAg alone for screening prospective donors will not eliminate the risk of HBV transmission in blood transfusion or stem cell transplantation.
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Affiliation(s)
- Amadin A Olotu
- Department of Medical Microbiology and Parasitology, Bowen University/Bowen University Teaching Hospital, P.O. Box 15, Ogbomoso, Oyo State, Nigeria.
| | - Adesola O Oyelese
- Department of Medical Microbiology and Parasitology, Obafemi Awolowo University Teaching Hospitals Complex, Ile-Ife, Nigeria
| | - Lateef Salawu
- Department of Haematology and Blood Transfusion, Obafemi Awolowo University Teaching Hospitals Complex, Ile-Ife, Nigeria
| | | | | | - Aaron O Aboderin
- Department of Medical Microbiology and Parasitology, Obafemi Awolowo University Teaching Hospitals Complex, Ile-Ife, Nigeria
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13
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Sood A, Pangotra C, Manrai M. Prevalence of occult hepatitis B infection in patients visiting tertiary care hospital. Med J Armed Forces India 2016; 72:140-144. [PMID: 27257324 PMCID: PMC4878925 DOI: 10.1016/j.mjafi.2016.02.006] [Citation(s) in RCA: 8] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/19/2015] [Accepted: 02/18/2016] [Indexed: 02/08/2023] Open
Abstract
BACKGROUND To study the prevalence of occult hepatitis B virus infection (OBI) in a tertiary care hospital. METHODS 50 HBsAg negative individuals, each amongst blood donors, alcohol dependence syndrome (ADS), alcoholic cirrhotics, hepatitis C virus (HCV)/cryptogenic cirrhotics, end-stage renal disease (ESRD) on maintenance haemodialysis for one year, all malignancies prior to chemotherapy and HIV positive patients were evaluated for anti-HBc total antibody, and blood hepatitis B virus (HBV) DNA amplification in those tested positive. RESULTS A total of 60/369 (16.2%) individuals were anti-HBc total positive, 13/50 (26%) of HCV/cryptogenic cirrhotics, 13/52 (25%) of HIV positive, 10/50 (20%) of patients with malignancy, 10/51 (19.6%) and 7/59 (11.9%) of alcoholic cirrhotics and ADS respectively had intermediate prevalence, while, blood donors 5/55 (9.1%), ESRD patients 2/52 (3.8%) had low prevalence. 12 patients (20% of all anti-HBc total positive cases) were HBV DNA positive, 5 HCV cirrhotics (10% of total HCV/cryptogenic), 4 HIV positive (7.69%), 1 each of ADS (1.69%), alcoholic cirrhotics (1.96%) and malignancy group (2%). Blood donors and ESRD patients were negative for HBV DNA. CONCLUSION HBV DNA amplification may under diagnose OBI and anti-HBc total positivity may be a better surrogate marker. Nucleic acid testing of blood donors, however is preferred, especially in high endemic areas. OBI must be looked for in cirrhotics, HIV infection, and patients with cancers prior to chemotherapy, as they may contribute to morbidity in them.
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Affiliation(s)
- A.K. Sood
- Senior Adviser (Medicine and Gastroenterology), Command Hospital (Western Command), C/O 56 APO, India
| | - Chetan Pangotra
- Graded Specialist (Medicine), 167 Military Hospital, C/O 56 APO, India
| | - Manish Manrai
- Classified Specialist (Medicine and Gastroenterologist), Army Hospital (R&R), Delhi Cantt 110010, India
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14
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Maldonado-Rodriguez A, Cevallos AM, Rojas-Montes O, Enriquez-Navarro K, Alvarez-Muñoz MT, Lira R. Occult hepatitis B virus co-infection in human immunodeficiency virus-positive patients: A review of prevalence, diagnosis and clinical significance. World J Hepatol 2015; 7:253-260. [PMID: 25729480 PMCID: PMC4342607 DOI: 10.4254/wjh.v7.i2.253] [Citation(s) in RCA: 18] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/29/2014] [Revised: 10/22/2014] [Accepted: 11/19/2014] [Indexed: 02/06/2023] Open
Abstract
The prevalence of human immunodeficiency virus (HIV) and hepatitis B virus (HBV) co-infection is high as they share similar mechanisms of transmission. The development and widespread use of highly sensitive tests for HBV diagnosis has demonstrated that a significant proportion of apparently healthy individuals with evidence of exposure to HBV continue to carry fully functional HBV DNA in their hepatocytes, a situation that predisposes them to the development of progressive liver disease and hepatocellular carcinoma. The presence of co-infections frequently influences the natural evolution of each of the participating infections present by either facilitating their virulence or competing for resources. Furthermore, the drugs used to treat these infections may also contribute to changes in the natural course of these infections, making the analysis of the impact of co-infection more difficult. The majority of studies has examined the impact of HIV on overt chronic hepatitis B, finding that co-infection carries an increased risk of progressive liver disease and the development of hepatocellular carcinoma. Although the effect of HIV on the natural history of occult hepatitis B infection (OBI) has not been fully assessed, all available data suggest a persisting risk of repeated flares of hepatitis and progressive liver disease. We describe studies regarding the diagnosis, prevalence and clinical significance of OBI in HIV-positive patients in this short review. Discrepancies in worldwide prevalence show the urgent need for the standardization of diagnostic criteria, as established by the Taormina statements. Ideally, standardized protocols for testing should be employed to enable the comparison of data from different groups. Additional studies are needed to define the differences in risk for OBI without HIV and in HIV-HBV co-infected patients with or without overt disease.
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15
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Bautista-Amorocho H, Castellanos-Domínguez YZ, Rodríguez-Villamizar LA, Velandia-Cruz SA, Becerra-Peña JA, Farfán-García AE. Epidemiology, risk factors and genotypes of HBV in HIV-infected patients in the northeast region of Colombia: high prevalence of occult hepatitis B and F3 subgenotype dominance. PLoS One 2014; 9:e114272. [PMID: 25462190 PMCID: PMC4252145 DOI: 10.1371/journal.pone.0114272] [Citation(s) in RCA: 16] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/18/2014] [Accepted: 11/09/2014] [Indexed: 12/18/2022] Open
Abstract
INTRODUCTION Chronic hepatitis B virus (HBV) infection is an increasing cause of morbidity and mortality in human immunodeficiency virus (HIV)-infected individuals. HIV-positive patients are commonly co-infected with HBV due to shared routes of transmission. OBJECTIVES Our aim was to determine the risk factors, prevalence, genotypes, and mutations of the Surface S gene of HBV, and occult hepatitis B infection (OBI) among patients infected with HIV in a northeastern Colombian city. METHODS A cross-sectional study was conducted with 275 HIV-positive patients attending an outpatient clinic in Bucaramanga, Colombia during 2009-2010. Blood samples were collected and screened for serological markers of HBV (anti-HBs, anti-HBc and HBsAg) through ELISA assay. Regardless of their serological profile, all samples were tested for the HBV S gene by nested-PCR and HBV genotypes were determined by phylogenetic inference. Clinical records were used to examine demographic, clinical, virological, immunological and antiretroviral therapy (ART) variables of HIV infection. RESULTS Participants were on average 37±11 years old and 65.1% male. The prevalence of HIV-HBV coinfection was 12% (95%CI 8.4-16.4) of which 3.3% had active HBV infection and 8.7% OBI. The prevalence of HIV-HBV coinfection was associated with AIDS stage and ART treatment. Sequence analysis identified genotype F, subgenotype F3 in 93.8% of patients and genotype A in 6.2% of patients. A C149R mutation, which may have resulted from failure in HBsAg detection, was found in one patient with OBI. CONCLUSIONS The present study found a high prevalence of HIV-HBV coinfection with an incidence of OBI 2.6-fold higher compared to active HBV infection. These findings suggest including HBV DNA testing to detect OBI in addition to screening for HBV serological markers in HIV patients.
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Affiliation(s)
- Henry Bautista-Amorocho
- University of Santander (UDES), Bacteriology and Clinical Laboratory Program, Department of Health Sciences, CliniUDES Research Group, Laboratory for Biomedical and Biotechnological Research (LBBR) Bucaramanga, Santander, Colombia
- * E-mail:
| | - Yeny Zulay Castellanos-Domínguez
- University of Santander (UDES), Bacteriology and Clinical Laboratory Program, Department of Health Sciences, CliniUDES Research Group, Laboratory for Biomedical and Biotechnological Research (LBBR) Bucaramanga, Santander, Colombia
| | - Laura Andrea Rodríguez-Villamizar
- Industrial University of Santander (UIS), Department of Public Health, School of Medicine, Research Group on Demography, Public Health and Health Systems (GUINDESS), Bucaramanga, Santander, Colombia
| | - Sindi Alejandra Velandia-Cruz
- University of Santander (UDES), Bacteriology and Clinical Laboratory Program, Department of Health Sciences, CliniUDES Research Group, Laboratory for Biomedical and Biotechnological Research (LBBR) Bucaramanga, Santander, Colombia
| | - Jeysson Andrey Becerra-Peña
- University of Santander (UDES), Bacteriology and Clinical Laboratory Program, Department of Health Sciences, CliniUDES Research Group, Laboratory for Biomedical and Biotechnological Research (LBBR) Bucaramanga, Santander, Colombia
| | - Ana Elvira Farfán-García
- University of Santander (UDES), Bacteriology and Clinical Laboratory Program, Department of Health Sciences, CliniUDES Research Group, Laboratory for Biomedical and Biotechnological Research (LBBR) Bucaramanga, Santander, Colombia
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Zhang F, Zhu H, Wu Y, Dou Z, Zhang Y, Kleinman N, Bulterys M, Wu Z, Ma Y, Zhao D, Liu X, Fang H, Liu J, Cai WP, Shang H. HIV, hepatitis B virus, and hepatitis C virus co-infection in patients in the China National Free Antiretroviral Treatment Program, 2010-12: a retrospective observational cohort study. THE LANCET. INFECTIOUS DISEASES 2014; 14:1065-1072. [PMID: 25303841 DOI: 10.1016/s1473-3099(14)70946-6] [Citation(s) in RCA: 94] [Impact Index Per Article: 8.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/16/2022]
Abstract
BACKGROUND Hepatitis-related liver diseases are a leading cause of mortality and morbidity among people with HIV/AIDS taking combination antiretroviral therapy. We assessed the effect of hepatitis B virus (HBV) and hepatitis C virus (HCV) co-infection on HIV outcomes in patients in China. METHODS We did a nationwide retrospective observational cohort study with data from the China National Free Antiretroviral Treatment Program from 2010-11. Patients older than 18 years starting standard antiretroviral therapy for HIV who had tested positive for HBV and HCV were followed up to Dec 31, 2012. We used Kaplan-Meier analysis and Cox proportional hazard models to evaluate survival, and logistic regression models to estimate virological failure, immunological response, and retention in care. FINDINGS 33 861 patients with HIV met eligibility criteria. 2958 (8·7%) participants had HBV co-infection, 6149 (18·2%) had HCV co-infection, and 1114 (3·3%) had triple infection. All-cause mortality was higher in participants with triple infection (adjusted hazard ratio 1·90, 95% CI 1·53-2·37) and HCV co-infection (1·46, 1·25-1·70) than in those with HIV only, but not in those with HBV co-infection (1·06, 0·89-1·26). People with triple infection were also more likely to have virological failure (adjusted odds ratio [OR] 1·26, 95% CI 1·02-1·56) than were those with HIV only, whereas the difference was not significant for those with HBV co-infection (0·93, 0·80-1·10) or HCV co-infection (1·10, 0·97-1·26). No co-infection was significantly associated with a difference in CD4 cell count after 1 year of treatment. Loss to follow-up was more common among participants with triple infection (OR 1·37, 95% CI 1·16-1·62) and HCV co-infection (1·30, 1·17-1·45), but not HBV co-infection (0·93, 0·82-1·05), than among those with HIV only. INTERPRETATION Screening for viral hepatitis is important in individuals diagnosed as HIV positive. Effective management for viral hepatitis should be integrated into HIV treatment programmes. Long-term data are needed about the effect of hepatitis co-infection on HIV disease progression. FUNDING The National Center for AIDS/STD Control and Prevention, China Center for Disease Control and Prevention.
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Affiliation(s)
- Fujie Zhang
- National Center for AIDS/STD Control and Prevention, China Center for Disease Control and Prevention, Beijing, China; First Affiliated Hospital of China Medical University, Liaoning, China
| | - Hao Zhu
- Global AIDS Program, China Office, US Centers for Disease Control and Prevention, Beijing, China
| | - Yasong Wu
- National Center for AIDS/STD Control and Prevention, China Center for Disease Control and Prevention, Beijing, China
| | - Zhihui Dou
- National Center for AIDS/STD Control and Prevention, China Center for Disease Control and Prevention, Beijing, China
| | - Yao Zhang
- National Center for AIDS/STD Control and Prevention, China Center for Disease Control and Prevention, Beijing, China
| | - Nora Kleinman
- Global AIDS Program, China Office, US Centers for Disease Control and Prevention, Beijing, China; Association of Schools and Programs of Public Health, Washington, DC, USA
| | - Marc Bulterys
- Global AIDS Program, China Office, US Centers for Disease Control and Prevention, Beijing, China; Department of Defense HIV/AIDS Prevention Program, Naval Health Research Center, San Diego, CA, USA
| | - Zunyou Wu
- National Center for AIDS/STD Control and Prevention, China Center for Disease Control and Prevention, Beijing, China
| | - Ye Ma
- National Center for AIDS/STD Control and Prevention, China Center for Disease Control and Prevention, Beijing, China
| | - Decai Zhao
- National Center for AIDS/STD Control and Prevention, China Center for Disease Control and Prevention, Beijing, China
| | - Xia Liu
- National Center for AIDS/STD Control and Prevention, China Center for Disease Control and Prevention, Beijing, China
| | - Hua Fang
- National Center for AIDS/STD Control and Prevention, China Center for Disease Control and Prevention, Beijing, China
| | - Jing Liu
- First Affiliated Hospital of China Medical University, Liaoning, China
| | - Wei-Ping Cai
- Department of Infectious Diseases, Guang Zhou Eighth People's Hospital, Guangdong, China
| | - Hong Shang
- First Affiliated Hospital of China Medical University, Liaoning, China.
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