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Rossotti R, Merli M, Mazzarelli C, De Carlis RM, Travi G, Vecchi M, Viganò R, Lauterio A, Raimondi A, Belli LS, De Carlis LG, Puoti M. Similar survival but higher and delayed hepatocellular carcinoma recurrence in HIV-positive compared to negative cirrhotics undergoing liver transplantation. Dig Liver Dis 2023; 55:268-275. [PMID: 35644890 DOI: 10.1016/j.dld.2022.05.001] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/13/2021] [Revised: 05/04/2022] [Accepted: 05/05/2022] [Indexed: 02/01/2023]
Abstract
BACKGROUND Liver transplantation (LT) represents the best therapeutic option for hepatocellular carcinoma (HCC) and end-stage liver disease (ESLD). Although HIV infection does not seem to lower survival rates, HCV and HCC recurrence appear more harmful. AIMS To compare the overall survival after LT; evaluate the impact of anti-HCV direct-acting agents (DAA); assess the rate of HCC recurrence in HIV-positive and negative patients. METHODS Subjects with HCV/HBV infection who underwent LT for HCC or ESLD from 2012 to 2019 were retrospectively evaluated. RESULTS Study population included 299 individuals, 31 (10.4%) were HIV-positive. Overall mortality was similar (16.1% versus 19.0%, p = 0.695). HCC recurrence was observed in 6 HIV-positive (19.4%) and in 17 negative subjects (6.3%, p = 0.022). Time to relapse was 831 days in HIV-positive and 315 days in negative patients (p = 0.046). Cox model found a significant role for HIV in univariate analysis but, after adjusting for variables, extra-hepatic tumor was the only factor associated to recurrence (aHR 56.379, p < 0.001). CONCLUSIONS Post-LT survival improved after DAA availability and HIV has no impact on mortality. A higher and delayed rate of HCC recurrence was observed in co-infected individuals: surveillance protocols should be strengthened along time in this population.
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Affiliation(s)
- Roberto Rossotti
- Department of Infectious Diseases, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy.
| | - Marco Merli
- Department of Infectious Diseases, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy
| | - Chiara Mazzarelli
- Hepatology and Gastroenterology Unit, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy
| | - Riccardo Maria De Carlis
- Department of General Surgery and Transplantation, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy
| | - Giovanna Travi
- Department of Infectious Diseases, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy
| | - Marta Vecchi
- Department of Infectious Diseases, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy
| | - Raffaella Viganò
- Hepatology and Gastroenterology Unit, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy
| | - Andrea Lauterio
- Department of General Surgery and Transplantation, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy
| | - Alessandro Raimondi
- Department of Infectious Diseases, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy
| | - Luca Saverio Belli
- Hepatology and Gastroenterology Unit, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy
| | - Luciano Gregorio De Carlis
- Department of General Surgery and Transplantation, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy; School of Medicine, University of Milan-Bicocca, Milan, Italy
| | - Massimo Puoti
- Department of Infectious Diseases, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy; Hepatology and Gastroenterology Unit, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy; Department of General Surgery and Transplantation, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy; School of Medicine, University of Milan-Bicocca, Milan, Italy
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Roland ME, Barin B, Huprikar S, Murphy B, Hanto DW, Blumberg E, Olthoff K, Simon D, Hardy WD, Beatty G, Stock PG. Survival in HIV-positive transplant recipients compared with transplant candidates and with HIV-negative controls. AIDS 2016; 30:435-44. [PMID: 26765937 DOI: 10.1097/qad.0000000000000934] [Citation(s) in RCA: 16] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/30/2022]
Abstract
OBJECTIVES To evaluate the impact of liver and kidney transplantation on survival in HIV-positive transplant candidates and compare outcomes between HIV-positive and negative recipients. DESIGN Observational cohort of HIV-positive transplant candidates and recipients and secondary analysis comparing study recipients to HIV-negative national registry controls. METHODS We fit proportional hazards models to assess transplantation impact on mortality among recipients and candidates. We compared time to graft failure and death with HIV-negative controls in unmatched, demographic-matched, and risk-adjusted models. RESULTS There were 17 (11.3%) and 46 (36.8%) deaths among kidney and liver recipients during a median follow-up of 4.0 and 3.5 years, respectively. Transplantation was associated with survival benefit for HIV-infected liver recipients with model for end-stage liver disease (MELD) greater than or equal 15 [hazard ratio (HR) 0.1; 95% confidence interval (CI) 0.05, 0.01; P < 0.0001], but not for MELD less than 15 (HR 0.7; 95% CI 0.3, 1.8; P = 0.43) or for kidney recipients (HR 0.6; 95% CI 0.3, 1.4; P = 0.23). In HIV-positive kidney recipients, unmatched and risk-matched analyses indicated a marginally significant HR for graft loss [1.3 (P = 0.07) and HR 1.4 (P = 0.052)]; no significant increase in risk of death was observed. All models demonstrated a higher relative hazard of graft loss or death in HIV-positive liver recipients; the absolute difference in the proportion of deaths was 6.7% in the risk-matched analysis. CONCLUSION Kidney transplantation should be standard of care for well managed HIV-positive patients. Liver transplant in candidates with high MELD confers survival benefit; transplant is a viable option in selected candidates. The increased mortality risk compared with HIV-negative recipients was modest. TRIAL REGISTRATION ClinicalTrials.Gov; NCT00074386; http://clinicaltrials.gov/.
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King JT, Perkal MF, Rosenthal RA, Gordon AJ, Crystal S, Rodriguez-Barradas MC, Butt AA, Gibert CL, Rimland D, Simberkoff MS, Justice AC. Thirty-day postoperative mortality among individuals with HIV infection receiving antiretroviral therapy and procedure-matched, uninfected comparators. JAMA Surg 2015; 150:343-51. [PMID: 25714794 DOI: 10.1001/jamasurg.2014.2257] [Citation(s) in RCA: 32] [Impact Index Per Article: 3.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/08/2023]
Abstract
IMPORTANCE Antiretroviral therapy (ART) has converted human immunodeficiency virus (HIV) infection into a chronic condition, and patients now undergo a variety of surgical procedures, but current surgical outcomes are inadequately characterized. OBJECTIVE To compare 30-day postoperative mortality in patients with HIV infection receiving ART with the rates in uninfected individuals. DESIGN, SETTING, AND PARTICIPANTS Retrospective analysis of nationwide electronic medical record data from the US Veterans Health Administration Healthcare System, October 1, 1996, to September 30, 2010. Common inpatient surgical procedures were grouped using the Healthcare Cost and Utilization Project Clinical Classification System to match HIV-infected and uninfected patients in a 1:2 ratio. Data on 1641 patients with HIV infection receiving combination ART who were undergoing inpatient surgery were compared with data on 3282 procedure-matched, uninfected comparators. Poisson regression models of 30-day postoperative mortality were adjusted for procedure year, age, Charlson Comorbidity Index score, hemoglobin level, albumin level, HIV infection, CD4 cell count, and HIV-1 RNA level. MAIN OUTCOMES AND MEASURES All-cause 30-day postoperative mortality. RESULTS The most common procedures in both groups were cholecystectomy (10.5%), hip arthroplasty (10.5%), spine surgery (9.8%), herniorrhaphy (7.4%), and coronary artery bypass grafting (7.0%). In patients with HIV infection, CD4 cell distributions were 80.0% with 200/μL or more, 16.3% with 50/μL to 199/μL, and 3.7% with less than 50/μL; 74.1% of patients with HIV infection had undetectable HIV-1 RNA. Human immunodeficiency virus infection was associated with higher 30-day postoperative mortality compared with the mortality in uninfected patients (3.4% [56 patients]) vs 1.6% [53]); incidence rate ratio [IRR], 2.11; 95% CI, 1.41-3.17; P < .001). CD4 cell count was inversely associated with mortality, but HIV-1 RNA provided no additional information. After adjustment, patients with HIV infection had increased mortality compared with uninfected patients at all CD4 cell count strata (≥500/μL: IRR, 1.92; 95% CI, 1.02-3.60; P = .04; 200-499/μL: IRR, 1.89; 95% CI, 1.20-2.98; P = .01; 50-199/μL: IRR, 2.66; 95% CI, 1.29-5.47; P = .01; and <50/μL: IRR, 6.21; 95% CI, 3.55-10.85; P < .001). Hypoalbuminemia (IRR, 4.35; 95% CI, 2.78-6.81; P < .001) and age in decades (IRR, 1.47; 95% CI, 1.23-1.76; P < .001) were also strongly associated with mortality. CONCLUSIONS AND RELEVANCE Current postoperative mortality rates among individuals with HIV infection who are receiving ART are low and are influenced as much by hypoalbuminemia and age as by CD4 cell status. Human immunodeficiency virus infection and CD4 cell count are only 2 of many factors associated with surgical outcomes that should be incorporated into surgical decision making.
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Affiliation(s)
- Joseph T King
- Section of Neurosurgery, Department of Surgery, Veterans Affairs (VA) Connecticut Healthcare System, West Haven2Department of Neurosurgery, Yale University School of Medicine, New Haven, Connecticut
| | - Melissa F Perkal
- Section of General Surgery, Department of Surgery, VA Connecticut Healthcare System, West Haven4Department of Surgery, Yale University School of Medicine, New Haven, Connecticut
| | - Ronnie A Rosenthal
- Section of General Surgery, Department of Surgery, VA Connecticut Healthcare System, West Haven4Department of Surgery, Yale University School of Medicine, New Haven, Connecticut
| | - Adam J Gordon
- Department of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania6Department of Medicine, VA Pittsburgh Healthcare System, Pittsburgh, Pennsylvania7Division of Infectious Diseases, Department of Medicine, University of Pittsbur
| | - Stephen Crystal
- Center for Health Services Research on Pharmacotherapy, Chronic Disease Management, and Outcomes, Rutgers University, New Brunswick, New Jersey
| | - Maria C Rodriguez-Barradas
- Section of Infectious Diseases, Department of Medicine, Michael E. DeBakey VA Medical Center, Houston, Texas10Department of Medicine, Baylor College of Medicine, Houston, Texas
| | - Adeel A Butt
- Department of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania6Department of Medicine, VA Pittsburgh Healthcare System, Pittsburgh, Pennsylvania7Division of Infectious Diseases, Department of Medicine, University of Pittsbur
| | - Cynthia L Gibert
- Section of Infectious Diseases, Medical Service, VA Medical Center, Washington, DC12Department of Medicine, George Washington University School of Medicine and Health Sciences, Washington, DC
| | - David Rimland
- Division of Infectious Diseases, Department of Medicine, Atlanta VA Medical Center, Atlanta, Georgia14Division of Infectious Diseases, Department of Medicine, Emory University School of Medicine, Atlanta, Georgia
| | - Michael S Simberkoff
- Section of Infectious Diseases, Department of Medicine, VA New York Harbor Healthcare System, New York, New York16Section of Infectious Diseases, Department of Medicine, New York University School of Medicine, New York
| | - Amy C Justice
- Section of General Internal Medicine, Department of Medicine, VA Connecticut Healthcare System, West Haven18Section of General Internal Medicine, Department of Medicine, Yale University School of Medicine, New Haven, Connecticut
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Stock PG, Terrault NA. Human immunodeficiency virus and liver transplantation: Hepatitis C is the last hurdle. Hepatology 2015; 61:1747-54. [PMID: 25292153 DOI: 10.1002/hep.27553] [Citation(s) in RCA: 14] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/21/2014] [Accepted: 09/11/2014] [Indexed: 01/16/2023]
Affiliation(s)
- Peter G Stock
- Departments of Surgery and Medicine, University of California San Francisco, San Francisco, CA
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Castells L, Rimola A, Manzardo C, Valdivieso A, Montero JL, Barcena R, Abradelo M, Xiol X, Aguilera V, Salcedo M, Rodriguez M, Bernal C, Suarez F, Antela A, Olivares S, Del Campo S, Laguno M, Fernandez JR, de la Rosa G, Agüero F, Perez I, González-García J, Esteban-Mur JI, Miro JM. Pegylated interferon plus ribavirin in HIV-infected patients with recurrent hepatitis C after liver transplantation: a prospective cohort study. J Hepatol 2015; 62:92-100. [PMID: 25127748 DOI: 10.1016/j.jhep.2014.07.034] [Citation(s) in RCA: 20] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/10/2014] [Revised: 07/22/2014] [Accepted: 07/28/2014] [Indexed: 12/19/2022]
Abstract
BACKGROUND & AIMS The aim of this study was to evaluate the results of treatment with pegylated interferon and ribavirin for the recurrence of hepatitis C after liver transplantation in HCV/HIV-coinfected patients. METHODS This was a prospective, multicentre cohort study, including 78 HCV/HIV-coinfected liver transplant patients who received treatment for recurrent hepatitis C. For comparison, we included 176 matched HCV-monoinfected patients who underwent liver transplantation during the same period of time at the same centres and were treated for recurrent hepatitis C. RESULTS Antiviral therapy was discontinued prematurely in 56% and 39% (p = 0.016), mainly because of toxicity (22% and 11%, respectively; p=0.034). Sustained virological response (SVR) was achieved in 21% of the coinfected patients and in 36% of monoinfected patients (p = 0.013). For genotype 1, SVR rates were 10% and 33% (p = 0.002), respectively; no significant differences were observed for the other genotypes. A multivariate analysis based on the whole series identified HIV-coinfection as an independent predictor of lack of SVR (OR, 0.17; 95% CI, 0.06-0.42). Other predictors of SVR were donor age, pretreatment HCV viral load, HCV genotype, and early virological response. SVR was associated with a significant improvement in survival: 5-year survival after antiviral treatment was 79% for HCV/HIV-coinfected patients with SVR vs. 43% for those without (p = 0.02) and 92% vs. 60% in HCV-monoinfected patients (p < 0.001), respectively. CONCLUSIONS The response to pegylated interferon and ribavirin was poorer in HCV/HIV-coinfected liver recipients, particularly those with genotype 1. However, when SVR was achieved, survival of coinfected patients increased significantly.
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Affiliation(s)
- Lluis Castells
- Hospital Vall d'Hebrón, Universitat Autónoma de Barcelona, Barcelona, Spain; CIBEREHD, Barcelona, Spain
| | - Antoni Rimola
- CIBEREHD, Barcelona, Spain; Hospital Clinic-IDIBAPS, University of Barcelona, Barcelona, Spain
| | | | | | | | - Rafael Barcena
- Hospital Universitario Ramón y Cajal-IRYCIS, Madrid, Spain
| | | | - Xavier Xiol
- Hospital de Bellvitge-IDIBELL, University of Barcelona, L'Hospitalet de Llobregat, Barcelona, Spain
| | | | | | | | - Carmen Bernal
- Hospital Universitario Virgen del Rocío, Sevilla, Spain
| | | | - Antonio Antela
- Hospital Universitario de Santiago de Compostela, La Coruña, Spain
| | | | | | | | - José R Fernandez
- Hospital de Cruces, University of the Basque Country, Bilbao, Spain
| | | | - Fernando Agüero
- Hospital Clinic-IDIBAPS, University of Barcelona, Barcelona, Spain
| | - Iñaki Perez
- Hospital Clinic-IDIBAPS, University of Barcelona, Barcelona, Spain
| | | | - Juan I Esteban-Mur
- Hospital Vall d'Hebrón, Universitat Autónoma de Barcelona, Barcelona, Spain; CIBEREHD, Barcelona, Spain
| | - Jose M Miro
- Hospital Clinic-IDIBAPS, University of Barcelona, Barcelona, Spain.
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6
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Miro J, Agüero F, Duclos-Vallée JC, Mueller N, Grossi P, Moreno A. Infections in solid organ transplant HIV-infected patients. Clin Microbiol Infect 2014; 20 Suppl 7:119-30. [DOI: 10.1111/1469-0691.12754] [Citation(s) in RCA: 23] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/11/2022]
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Congly SE, Doucette KE, Coffin CS. Outcomes and management of viral hepatitis and human immunodeficiency virus co-infection in liver transplantation. World J Gastroenterol 2014; 20:414-424. [PMID: 24574710 PMCID: PMC3923016 DOI: 10.3748/wjg.v20.i2.414] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/24/2013] [Revised: 10/22/2013] [Accepted: 11/05/2013] [Indexed: 02/06/2023] Open
Abstract
Liver transplantation for human immunodeficiency virus (HIV) positive patients with viral hepatitis co-infection is increasingly offered in many North American and European liver transplant centers. Prior studies have demonstrated acceptable post-transplant outcomes and no increased risk of HIV complications in patients co-infected with hepatitis B virus (HBV). However, liver transplantation in HIV positive patients with hepatitis C virus (HCV) has poorer outcomes overall, requiring careful selection of candidates. This review aims to summarize the published literature on outcomes after transplant in HIV patients with HBV or HCV related end-stage liver disease and recommendations for management. In particular the pre-transplant factors impacting outcomes in HCV/HIV co-infected candidates and importance of multidisciplinary management will be discussed.
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8
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Dannhorn E, O’Beirne JP. Liver transplantation for HIV/HCV coinfection: where is the controversy? Future Virol 2013. [DOI: 10.2217/fvl.13.51] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/21/2022]
Abstract
Liver transplantation (LT) is an accepted mode of treatment for patients with chronic liver disease. Historically, patients with HIV were excluded from LT programs, but with the introduction of highly effective antiretroviral regimens, HIV is no longer a contraindication. LT outcomes for some liver diseases in HIV-positive patients are equivalent to those observed in non-HIV-positive patients. This is not the case for patients coinfected with HIV and HCV, however, where results at 5 years have led to suggestions that LT for coinfection should be abandoned. This article examines the role of LT for HIV/HCV and identifies groups of patients where transplantation is associated with good outcomes. We believe that the application of existing knowledge to patient selection and organ allocation could improve outcomes further, and with the advent of directly acting antivirals for HCV, LT for HIV/HCV coinfection will no longer be controversial.
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Affiliation(s)
| | - James P O’Beirne
- UCL Institute of Liver & Digestive Health, Royal Free Hospital, Pond Street, Hampstead, London, UK
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Terrault NA, Roland ME, Schiano T, Dove L, Wong MT, Poordad F, Ragni MV, Barin B, Simon D, Olthoff KM, Johnson L, Stosor V, Jayaweera D, Fung J, Sherman KE, Subramanian A, Millis JM, Slakey D, Berg CL, Carlson L, Ferrell L, Stablein DM, Odim J, Fox L, Stock PG. Outcomes of liver transplant recipients with hepatitis C and human immunodeficiency virus coinfection. Liver Transpl 2012; 18:716-26. [PMID: 22328294 PMCID: PMC3358510 DOI: 10.1002/lt.23411] [Citation(s) in RCA: 164] [Impact Index Per Article: 12.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/31/2022]
Abstract
Hepatitis C virus (HCV) is a controversial indication for liver transplantation (LT) in human immunodeficiency virus (HIV)-infected patients because of reportedly poor outcomes. This prospective, multicenter US cohort study compared patient and graft survival for 89 HCV/HIV-coinfected patients and 2 control groups: 235 HCV-monoinfected LT controls and all US transplant recipients who were 65 years old or older. The 3-year patient and graft survival rates were 60% [95% confidence interval (CI) = 47%-71%] and 53% (95% CI = 40%-64%) for the HCV/HIV patients and 79% (95% CI = 72%-84%) and 74% (95% CI = 66%-79%) for the HCV-infected recipients (P < 0.001 for both), and HIV infection was the only factor significantly associated with reduced patient and graft survival. Among the HCV/HIV patients, older donor age [hazard ratio (HR) = 1.3 per decade], combined kidney-liver transplantation (HR = 3.8), an anti-HCV-positive donor (HR = 2.5), and a body mass index < 21 kg/m(2) (HR = 3.2) were independent predictors of graft loss. For the patients without the last 3 factors, the patient and graft survival rates were similar to those for US LT recipients. The 3-year incidence of treated acute rejection was 1.6-fold higher for the HCV/HIV patients versus the HCV patients (39% versus 24%, log rank P = 0.02), but the cumulative rates of severe HCV disease at 3 years were not significantly different (29% versus 23%, P = 0.21). In conclusion, patient and graft survival rates are lower for HCV/HIV-coinfected LT patients versus HCV-monoinfected LT patients. Importantly, the rates of treated acute rejection (but not the rates of HCV disease severity) are significantly higher for HCV/HIV-coinfected recipients versus HCV-infected recipients. Our results indicate that HCV per se is not a contraindication to LT in HIV patients, but recipient and donor selection and the management of acute rejection strongly influence outcomes.
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Affiliation(s)
| | | | | | | | | | | | | | | | | | | | | | | | | | | | | | | | | | | | | | - Laurie Carlson
- University of California San Francisco, San Francisco, CA
| | - Linda Ferrell
- University of California San Francisco, San Francisco, CA
| | | | - Jonah Odim
- National Institute of Allergy and Infectious Diseases, Bethesda, MD
| | - Lawrence Fox
- National Institute of Allergy and Infectious Diseases, Bethesda, MD
| | - Peter G. Stock
- University of California San Francisco, San Francisco, CA
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10
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Grossi PA, Costa AN, Fehily D, Blumberg EA, Kuehnert MJ, Fishman JA, Ison MG, Lattes R, Kotton CN, Lilleri D, Kabanova A, Lanzavecchia A, Gerna G, Razonable RR, Comoli P, Zecca M, Basso S, Ginevri F, Grossi A, Schena FP, Rimola A, Burra P, De Martin E, Rodriguez-Castro KI, Fagiuoli S, Pasulo L, Bruno R, Andreone P, Loggi E, Arena F, Rossolini GM, Sganga G, Cozza V. Infections and organ transplantation: new challenges for prevention and treatment--a colloquium. Transplantation 2012; 93:S4-S39. [PMID: 22374265 DOI: 10.1097/tp.0b013e3182481347] [Citation(s) in RCA: 23] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/06/2023]
Affiliation(s)
- Paolo A Grossi
- Infectious Diseases Department, University of Insubria, Varese, ISMETT-UPMC Palermo, National Center for Transplantation, Rome, Italy.
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11
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Miró JM, Blanes M, Norman F, Martín-Dávila P. Infections in solid organ transplantation in special situations: HIV-infection and immigration. Enferm Infecc Microbiol Clin 2012; 30 Suppl 2:76-85. [DOI: 10.1016/s0213-005x(12)70086-1] [Citation(s) in RCA: 11] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/21/2022]
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12
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Moreno A, Cervera C, Fortún J, Blanes M, Montejo E, Abradelo M, Len O, Rafecas A, Martín-Davila P, Torre-Cisneros J, Salcedo M, Cordero E, Lozano R, Pérez I, Rimola A, Miró JM. Epidemiology and outcome of infections in human immunodeficiency virus/hepatitis C virus-coinfected liver transplant recipients: a FIPSE/GESIDA prospective cohort study. Liver Transpl 2012; 18:70-81. [PMID: 21898772 DOI: 10.1002/lt.22431] [Citation(s) in RCA: 40] [Impact Index Per Article: 3.1] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
Information about infections unrelated to acquired immunodeficiency syndrome (AIDS) in human immunodeficiency virus (HIV)-infected liver recipients is scarce. The aims of this study were to describe the prevalence, clinical characteristics, time of onset, and outcomes of bacterial, viral, and fungal infections in HIV/hepatitis C virus (HCV)-coinfected orthotopic liver transplant recipients and to identify risk factors for developing severe infections. We studied 84 consecutive HIV/HCV-coinfected patients who underwent liver transplantation at 17 sites in Spain between 2002 and 2006 and were followed until December 2009. The median age was 42 years, and 76% were men. The median follow-up was 2.6 years (interquartile range = 1.25-3.53 years), and 54 recipients (64%) developed at least 1 infection. Thirty-eight (45%) patients had bacterial infections, 21 (25%) had cytomegalovirus (CMV) infections (2 had CMV disease), 13 (15%) had herpes simplex virus infections, and 16 (19%) had fungal infections (7 cases were invasive). Nine patients (11%) developed 10 opportunistic infections with a 44% mortality rate. Forty-three of 119 infectious episodes (36%) occurred in the first month after transplantation, and 53 (45%) occurred after the sixth month. Thirty-six patients (43%) had severe infections. Overall, 36 patients (43%) died, and the deaths were related to severe infections in 7 cases (19%). Severe infections increased the mortality rate almost 3-fold [hazard ratio (HR) = 2.9, 95% confidence interval (CI) = 1.5-5.8]. Independent factors for severe infections included a pretransplant Model for End-Stage Liver Disease (MELD) score >15 (HR = 3.5, 95% CI = 1.70-7.1), a history of AIDS-defining events before transplantation (HR = 4.0, 95% CI = 1.9-8.6), and non-tacrolimus-based immunosuppression (HR = 2.5, 95% CI = 1.3-4.8). In conclusion, the rates of severe and opportunistic infections are high in HIV/HCV-coinfected liver recipients and especially in those with a history of AIDS, a high MELD score, or non-tacrolimus-based immunosuppression.
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Affiliation(s)
- Asunción Moreno
- Hospital Clínic-Institut d'Investigacions Biomèdiques August Pi i Sunyer, Universitat de Barcelona, Barcelona
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13
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Cherian PT, Alrabih W, Douiri A, Quaglia A, Heneghan MA, O'Grady J, Rela M, Heaton ND. Liver transplantation in human immunodeficiency virus-infected patients: procoagulant, but is antithrombotic prophylaxis required? Liver Transpl 2012; 18:82-8. [PMID: 22006832 DOI: 10.1002/lt.22449] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
Liver transplantation (LT) for human immunodeficiency virus (HIV)-positive recipients with end-stage liver disease has become an accepted practice. However, because these patients are increasingly being recognized as prothrombotic, we reviewed their posttransplant thrombotic complications. Because morphological changes might be responsible in part for this prothrombotic state, we also conducted a histopathological review of explants from HIV-positive patients. Between 1990 and 2010, 24 of 3502 recipients (including 23 adults) were HIV-positive at LT. These patients and their postoperative courses were reviewed with a particular focus on vascular complications, risk factors, and outcomes. Another patient in whom HIV was detected 12 years after LT was also examined. Among the 24 HIV-positive LT recipients (17 males and 22 whole liver grafts; median age = 40 years), 5 developed arterial complications [including 3 cases of hepatic artery thrombosis (HAT), 1 case of generalized arteriopathy (on angiography), and 1 case of endoarteritis (on histological analysis)]. Multiple arterial anastomoses were performed in 8 of the 24 recipients, and HAT occurred twice within this anastomosis group. The outcomes of the 3 patients with HAT included retransplantation, biliary stenting for ischemic cholangiopathy followed by retransplantation, and observation only. In addition, 5 separate venous thrombotic events were detected in the 24 recipients during this period. Moreover, the delayed-HIV recipient developed delayed HAT and subsequently ischemic cholangiopathy and was being assessed for retransplantation at the time of this writing. In conclusion, the prothrombotic state associated with combined HIV and liver disease is a cause of morbidity after LT: 8 of the 24 recipients (33%) in this series suffered vascular thrombotic complications. There is a potential increase in the risk of HAT: the rate for the HIV-positive cohort was higher than the rate for historical HIV-negative controls [12% versus 3.2%, P = 0.016 (Fisher's exact test)]. The minimization of complex arterial reconstruction, coagulopathy screening, and risk-adapted antithrombotic chemoprophylaxis appear to be reasonable precautions.
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Affiliation(s)
- P Thomas Cherian
- Institute of Liver Studies, King's College Hospital, London, United Kingdom
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14
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Francoz C, Belghiti J, Castaing D, Chazouillères O, Duclos-Vallée JC, Duvoux C, Lerut J, Le Treut YP, Moreau R, Mandot A, Pageaux G, Samuel D, Thabut D, Valla D, Durand F. Model for end-stage liver disease exceptions in the context of the French model for end-stage liver disease score-based liver allocation system. Liver Transpl 2011; 17:1137-51. [PMID: 21695771 DOI: 10.1002/lt.22363] [Citation(s) in RCA: 59] [Impact Index Per Article: 4.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/07/2023]
Abstract
Model for End-Stage Liver Disease (MELD) score-based allocation systems have been adopted by most countries in Europe and North America. Indeed, the MELD score is a robust marker of early mortality for patients with cirrhosis. Except for extreme values, high pretransplant MELD scores do not significantly affect posttransplant survival. The MELD score can be used to optimize the allocation of allografts according to a sickest first policy. Most often, patients with small hepatocellular carcinomas (HCCs) and low MELD scores receive extra points, which allow them appropriate access to transplantation comparable to the access of patients with advanced cirrhosis and high MELD scores. In addition to patients with advanced cirrhosis and HCC, patients with a number of relatively uncommon conditions have low MELD scores and a poor prognosis in the short term without transplantation but derive excellent benefits from transplantation. These conditions, which correspond to the so-called MELD score exceptions, justify the allocation of a specific score for appropriate access to transplantation. Here we report the conclusions of the French consensus meeting. The goals of this meeting were (1) to identify which conditions merit MELD score exceptions, (2) to list the criteria needed for defining each of these conditions, and (3) to define a reasonable time interval for organ allocation for each MELD exception in the general context of organ shortages. MELD exceptions were discussed in an attempt to reconcile the concepts of transparency, equity, justice, and utility.
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Affiliation(s)
- Claire Francoz
- Departments of Hepatology, Beaujon Hospital, Clichy, France.
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15
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Vernadakis S, Sotiropoulos GC, Brokalaki EI, Esser S, Kaiser GM, Cicinnati VR, Beckebaum S, Paul A, Mathé Z. Long-term outcomes of liver transplant patients with human immunodeficiency virus infection and end-stage-liver-disease: single center experience. Eur J Med Res 2011; 16:342-8. [PMID: 21813377 PMCID: PMC3351986 DOI: 10.1186/2047-783x-16-8-342] [Citation(s) in RCA: 11] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/16/2023] Open
Abstract
Objective Orthotopic-liver-transplantation (OLT) in patients with Human-Immunodeficiency-Virus infection (HIV) and end-stage-liver-disease (ESDL) is rarely reported. The purpose of this study is to describe our institutional experience on OLT for HIV positive patients. Material and methods This is a retrospective study of all HIV-infected patients who underwent OLT at the University Hospital of Essen, from January 1996 to December 2009. Age, sex, HIV transmission-way, CDC-stage, etiology of ESDL, concomitant liver disease, last CD4cell count and HIV-viral load prior to OLT were collected and analysed. Standard calcineurin-inhibitors-based immunosuppression was applied. All patients received anti-fungal and anti-pneumocystis carinii pneumonia prophylaxis post-OLT. Results Eight transplanted HIV-infected patients with a median age of 46 years (range 35-61 years) were included. OLT indications were HCV (n = 5), HBV (n = 2), HCV/HBV/HDV-related cirrhosis (n = 1) and acute liver-failure (n = 1). At OLT, CD4 cell-counts ranged from 113-621 cells/μl, and HIV viral-loads from < 50-175,000 copies/ml. Seven of eight patients were exposed to HAART before OLT. Patients were followed-up between 1-145 months. Five died 1, 3, 10, 31 and 34 months after OLT due to sepsis and graftfailure respectively. Graft-failure causes were recurrent hepatic-artery thrombosis, HCV-associated hepatitis, and chemotherapy-induced liver damage due to Hodgkin-disease. One survivor is relisted for OLT due to recurrent chronic HCV-disease but non-progredient HIV-infection 145 months post-OLT. Two other survivors show stable liver function and non-progredient HIV-disease under HAART 21 and 58 months post-OLT. Conclusions OLT in HIV-infected patients and ESLD is an acceptable therapeutic option in selected patients. Long-term survival can be achieved without HIV disease-progression under antiretroviral therapy and management of the viral hepatitis co-infection.
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Affiliation(s)
- S Vernadakis
- Department of General, Visceral and Transplantation Surgery, University Hospital Essen, Hufelandstr. 55, 45122 Essen, Germany
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16
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Joshi D, O'Grady J, Taylor C, Heaton N, Agarwal K. Liver transplantation in human immunodeficiency virus-positive patients. Liver Transpl 2011; 17:881-90. [PMID: 21563295 DOI: 10.1002/lt.22329] [Citation(s) in RCA: 14] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/12/2022]
Abstract
With the successful introduction of combined antiretroviral therapy (cART), human immunodeficiency virus (HIV) is now regarded as a chronic illness with excellent long-term outcomes. However, chronic exposure to viral etiologies (ie, chronic hepatitis B and hepatitis C) and drug-induced toxicity secondary to cART have resulted in increasing rates of mortality and morbidity due to end-stage liver disease. HIV disease is no longer considered an absolute contraindication to liver transplantation (LT) by most transplant centers worldwide. Because the burden of liver disease in this cohort is likely to increase, this review addresses the key etiologies and the management strategies available for HIV-positive patients undergoing LT.
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Affiliation(s)
- Deepak Joshi
- Institute of Liver Studies, King's College Hospital, Denmark Hill, London, SE5 9RS, UK
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17
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Results of a newborn liver transplant program in the era of piggyback technique and extended donor criteria in Italy. Updates Surg 2011; 63:191-200. [DOI: 10.1007/s13304-011-0096-1] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/23/2011] [Accepted: 06/30/2011] [Indexed: 12/13/2022]
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18
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Sugawara Y, Tamura S, Kokudo N. Liver transplantation in HCV/HIV positive patients. World J Gastrointest Surg 2011; 3:21-28. [PMID: 21394322 PMCID: PMC3052410 DOI: 10.4240/wjgs.v3.i2.21] [Citation(s) in RCA: 9] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/19/2010] [Revised: 01/15/2011] [Accepted: 01/21/2011] [Indexed: 02/06/2023] Open
Abstract
Since the introduction of highly active antiretroviral therapy (HAART) in 1996 for human immunodeficiency virus (HIV)-infected patients, the incidence of liver diseases secondary to co-infection with hepatitis C has increased. Although data on the outcome of liver transplantation in HIV-infected recipients is limited, the overall results to date seem to be comparable to that in non-HIV-infected recipients. Liver transplant centers are now accepting HIV-infected individuals as organ recipients. Post-transplantation HIV replication is controlled by HAART. Hepatitis C re-infection of the liver graft, however, remains an important problem because cirrhotic changes of the liver graft may be more rapid in HIV-infected recipients. Interactions between the HAART components and immunosuppressive drugs influence drug metabolism and therefore meticulous monitoring of drug blood level concentrations is required. The risk of opportunistic infection in HIV-positive transplant patients seems to be similar to that in HIV-negative transplant recipients.
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Affiliation(s)
- Yasuhiko Sugawara
- Yasuhiko Sugawara, Sumihito Tamura, Norihiro Kokudo, Artificial Organ and Transplantation Division, Department of Surgery, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan
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19
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Trasplante hepático en pacientes con infección por VIH. GASTROENTEROLOGIA Y HEPATOLOGIA 2010; 33:660-9. [DOI: 10.1016/j.gastrohep.2010.01.007] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Received: 01/20/2010] [Accepted: 01/22/2010] [Indexed: 01/18/2023]
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20
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Coffin CS, Stock PG, Dove LM, Berg CL, Nissen NN, Curry MP, Ragni M, Regenstein FG, Sherman KE, Roland ME, Terrault NA. Virologic and clinical outcomes of hepatitis B virus infection in HIV-HBV coinfected transplant recipients. Am J Transplant 2010; 10:1268-75. [PMID: 20346065 PMCID: PMC3155863 DOI: 10.1111/j.1600-6143.2010.03070.x] [Citation(s) in RCA: 66] [Impact Index Per Article: 4.4] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/25/2023]
Abstract
Liver transplantation (LT) is the treatment of choice for end-stage liver disease, but is controversial in patients with human immunodeficiency virus (HIV) infection. Using a prospective cohort of HIV-hepatitis B virus (HBV) coinfected patients transplanted between 2001-2007; outcomes including survival and HBV clinical recurrence were determined. Twenty-two coinfected patients underwent LT; 45% had detectable HBV DNA pre-LT and 72% were receiving anti-HBV drugs with efficacy against lamivudine-resistant HBV. Post-LT, all patients received hepatitis B immune globulin (HBIG) plus nucleos(t)ide analogues and remained HBsAg negative without clinical evidence of HBV recurrence, with a median follow-up 3.5 years. Low-level HBV viremia (median 108 IU/mL, range 9-789) was intermittently detected in 7/13 but not associated with HBsAg detection or ALT elevation. Compared with 20 HBV monoinfected patients on similar HBV prophylaxis and median follow-up of 4.0 years, patient and graft survival were similar: 100% versus 85% in HBV mono- versus coinfected patients (p = 0.08, log rank test). LT is effective for HIV-HBV coinfected patients with complications of cirrhosis, including those who are HBV DNA positive at the time of LT. Combination HBIG and antivirals is effective as prophylaxis with no clinical evidence of HBV recurrence but low-level HBV DNA is detectable in approximately 50% of recipients.
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Affiliation(s)
- C S Coffin
- Department of Medicine, University of California San Francisco, San Francisco, CA, USA
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21
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Eisenbach C, Merle U, Stremmel W, Encke J. Liver transplantation in HIV-positive patients. Clin Transplant 2010; 23 Suppl 21:68-74. [PMID: 19930319 DOI: 10.1111/j.1399-0012.2009.01112.x] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/28/2023]
Abstract
Death from end-stage liver disease (ESLD) because of chronic hepatitis B and C has become an increasing problem in human immunodeficiency virus (HIV)-infected patients in the last years. This is mainly because of the dramatic decrease of HIV-related morbidity and mortality since the introduction of highly active antiretroviral therapy (HAART). Although the data on the outcome of liver transplantation in HIV-infected recipients with ESLD is limited, overall results seem comparable to non-HIV-infected recipients. Therefore, liver transplant centres around the world are increasingly accepting HIV-infected individuals as organ recipients. Post-transplantation control of HIV replication is achieved by continuing HAART. As in non-HIV-infected patients, hepatitis B virus recurrence is efficiently prevented by hepatitis B immunoglobulin and antiviral therapy. Re-infection of the allograft with hepatitis C virus, however, remains an important problem, and progress to allograft cirrhosis may even be more rapid than in HIV-negative patients. Interactions in drug metabolism between the HAART components and the immunosuppressive drugs are difficult to predict and require close monitoring of drug levels and dose adjustments. The complexity in this setting makes close cooperation between transplant surgeons, hepatologists, HIV-clinicians and pharmacologists mandatory. As experience on liver transplantation in HIV-infected individuals is still limited, to date results from large prospective trials addressing key issues are needed.
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Affiliation(s)
- Christoph Eisenbach
- Department of Internal Medicine IV, Gastroenterology, Hepatology and Infectious Diseases, University of Heidelberg, Heidelberg, Germany.
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22
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Huprikar S. Solid organ transplantation in HIV-infected individuals: an update. Rev Med Virol 2010; 19:317-23. [PMID: 19554551 DOI: 10.1002/rmv.620] [Citation(s) in RCA: 8] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/02/2023]
Abstract
In the era of highly active antiretroviral therapy (HAART), the survival of patients with HIV has improved. Increasing morbidity and mortality are now related to chronic liver and kidney disease. Transplantation in HIV patients has been reported for nearly two decades and outcomes have generally improved in the HAART era. This review summarises the published experiences with liver and kidney transplantation in HIV patients.
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Affiliation(s)
- Shirish Huprikar
- Department of Medicine, Mount Sinai School of Medicine, New York, NY 10029, USA.
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23
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Drapeau CMJ, Pan A, Bellacosa C, Cassola G, Crisalli MP, De Gennaro M, Di Cesare S, Dodi F, Gattuso G, Irato L, Maggi P, Pantaleoni M, Piselli P, Soavi L, Rastrelli E, Tacconelli E, Petrosillo N. Surgical site infections in HIV-infected patients: Results from an Italian prospective multicenter observational study. Infection 2009; 37:455-60. [DOI: 10.1007/s15010-009-8225-1] [Citation(s) in RCA: 14] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/28/2022]
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Singal AK, Anand BS. Management of hepatitis C virus infection in HIV/HCV co-infected patients: Clinical review. World J Gastroenterol 2009; 15:3713-24. [PMID: 19673011 PMCID: PMC2726448 DOI: 10.3748/wjg.15.3713] [Citation(s) in RCA: 38] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/06/2023] Open
Abstract
Nearly one fourth of individuals with human immunodeficiency virus (HIV) infection have hepatitis C virus (HCV) infection in the US and Western Europe. With the availability of highly active antiretroviral therapy and the consequent reduction in opportunistic infections, resulting in the prolongation of the life span of HIV-infected patients, HCV co-infection has emerged as a significant factor influencing the survival of HIV patients. Patients with HIV/HCV co-infection have a faster rate of fibrosis progression resulting in more frequent occurrences of cirrhosis, end-stage liver disease, and hepatocellular carcinoma. However, the mechanism of interaction between the two viruses is not completely understood. The treatment for HCV in co-infected patients is similar to that of HCV mono-infection; i.e., a combination of pegylated interferon and ribavirin. The presence of any barriers to anti-HCV therapy should be identified and eliminated in order to recruit all eligible patients. The response to treatment in co-infected patients is inferior compared to the response in patients with HCV mono-infection. The sustained virologic response rate is only 38% for genotype-1 and 75% for genotype-2 and -3 infections. Liver transplantation is no longer considered a contraindication for end-stage liver disease in co-infected patients. However, the 5 year survival rate is lower in co-infected patients compared to patients with HCV mono-infection (33% vs 72%, P = 0.07). A better understanding of liver disease in co-infected patients is needed to derive new strategies for improving outcome and survival.
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25
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Care of HIV patients with chronic hepatitis B: updated recommendations from the HIV-Hepatitis B Virus International Panel. AIDS 2008; 22:1399-410. [PMID: 18614862 DOI: 10.1097/qad.0b013e3282f8b46f] [Citation(s) in RCA: 113] [Impact Index Per Article: 6.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/07/2023]
Abstract
Nearly 10% of the estimated 36 million people having HIV worldwide suffer from chronic hepatitis B virus (HBV) infection. The advent of new antiviral agents against HBV and the recent availability of improved molecular diagnostic tools have revolutioned the management of HIV/HBV coinfected patients. The present study represents an update of the current knowledge about HBV/HIV coinfection and an intent to provide practical advise about how to give the best care to HIV-infected persons with chronic hepatitis B.
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26
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Samuel D, Weber R, Stock P, Duclos-Vallée JC, Terrault N. Are HIV-infected patients candidates for liver transplantation? J Hepatol 2008; 48:697-707. [PMID: 18331763 DOI: 10.1016/j.jhep.2008.02.009] [Citation(s) in RCA: 30] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/17/2023]
Affiliation(s)
- Didier Samuel
- INSERM U785, and Centre Hepato-Biliare, AP-HP Hôpital Paul Brousse, Villejuif, France.
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27
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Gupta S, Markham DW, Mammen PPA, Kaiser P, Patel P, Ring WS, Drazner MH. Long-term follow-up of a heart transplant recipient with documented seroconversion to HIV-positive status 1 year after transplant. Am J Transplant 2008; 8:893-6. [PMID: 18294349 DOI: 10.1111/j.1600-6143.2008.02154.x] [Citation(s) in RCA: 16] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/25/2023]
Abstract
Whether human immunodeficiency virus (HIV) should be an absolute contraindication to heart transplantation has been a topic of recent discussion. There is a paucity of data regarding the expected outcome of heart transplantation in a recipient who is HIV positive. Herein, we report the case and long-term follow-up of a woman who was found to have seroconverted to HIV positive status 1 year after transplant.
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Affiliation(s)
- S Gupta
- Division of Cardiology, Department of Internal Medicine, University Hospital-St. Paul, University of Texas Southwestern Medical Center, TX, USA
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