transmission of human immunodeficiency virus and hepatitis c virus through liver transplantation

ORIGINAL ARTICLE

Transmission of Human Immunodeficiency Virusand Hepatitis C Virus Through LiverTransplantationJoseph Ahn and Stanley M. CohenSection of Hepatology, Rush University Medical Center, Chicago, IL

In November 2007, a liver transplant recipient was confirmed to have human immunodeficiency virus (HIV) and hepatitis C(HCV) infection after the organ procurement agency notified our institution that the donor has been HIV and HCV positive. Wereviewed medical records and the collected blood sample results for HIV and HCV testing. A 66 year old female withnonalcoholic steatohepatitis cirrhosis underwent liver transplantation. The donor was a male who had sex with men whoreceived multiple blood transfusions during resuscitation. Preoperative testing for HIV and HCV antibodies were negative forboth donor and recipient. Ten months later, HIV and HCV were identified with nucleic acid testing in the recipient and in thestored donor sera. This is the first reported case of HIV transmission from solid organ transplantation in 20 years, and the firstever reported case of simultaneously transmitted HIV and HCV. The current case represents a high risk donor withnewly-acquired HIV and HCV who transmitted the diseases during the window period of the infections. In this era of organshortages one option would be avoidance of any high-risk donor organs. Another option would be to continue the use of suchorgans with appropriate informed consent, acknowledging the limitations of current screening tests for HIV and HCV. Thisreport should serve as a wake-up call to the transplant community to consider revamping organ donor screening for HIV andHCV using nucleic acid testing as well as reconsidering the ongoing use of high-risk donors. Liver Transpl 14:1603-1608,2008. © 2008 AASLD.

Received January 23, 2008; accepted April 14, 2008.

See Editorial on 564

The transmission of human immunodeficiency virus(HIV) through solid organ transplantation is extremelyrare. The last documented case occurred in 1987.1 Wepresent a case of HIV and hepatitis C virus (HCV) infec-tion transmitted through the transplantation of an in-fected liver graft.

CASE REPORT

Because of the sensitive nature of this case, some re-cipient demographics have been omitted. A 66-year-oldfemale with diabetes and obesity presented with cirrho-sis, ascites, and hepatic encephalopathy. There was no

history of alcohol use, intravenous drug use, bloodtransfusions, or tattoos. Testing for viral hepatitis, au-toimmune hepatitis, biliary cirrhosis, and hereditaryliver diseases was negative. An HCV antibody test withthe Ortho HCV version 3.0 enzyme-linked immunosor-bent assay (Ortho-Clinical Diagnostics, Raritan, NJ), anHCV-RNA test with the Abbott real-time HCV assay(Abbott Molecular, Inc., Des Plaines, IL), and an HIVantibody test with the HIV-1/HIV-2 recombinant DNAenzyme immunoassay (EIA; Abbott Laboratories, Ab-bott Park, IL) were negative in November 2006. Thepatient was listed for orthotopic liver transplantation(OLT) and required repeat hospitalizations for hepaticencephalopathy while awaiting OLT. Her last pre-OLTModel for End-Stage Liver Disease score was 19.

A donor liver was offered in January 2007 from a

Abbreviations: CDC, Centers for Disease Control; CMV, cytomegalovirus; EIA, enzyme immunoassay; FHF, fulminant hepatic failure;HAART, highly active antiretroviral therapy; HCV, hepatitis C virus; HIV, human immunodeficiency virus; HTLV-III, human T-lymphotropic virus type III; NAT, nucleic acid testing; OLT, orthotopic liver transplantation; OPO, organ procurement organization.Address reprint requests to Joseph Ahn, 1725 W. Harrison Ave, Suite 158, Chicago, IL. Telephone: 312-942-8910; FAX: 312-563-3938;E-mail: [email protected]

DOI 10.1002/lt.21534Published online in Wiley InterScience (www.interscience.wiley.com).

LIVER TRANSPLANTATION 14:1603-1608, 2008

© 2008 American Association for the Study of Liver Diseases.

39-year-old male who had sustained head trauma. Hehad received multiple transfusions during resuscita-tion. The donor’s risk assessment questionnaire wasanswered by a close family friend. The donor had noknown history of hemophilia, viral hepatitis, HIV, priortransfusions, tattoos, intravenous drug use, or incar-cerations. He was a male who had sex with men. He hadpreviously tested negative for HIV. As part of predona-tion testing, both pretransfusion and posttransfusionblood samples were tested for HCV antibody with Ab-bott HCV EIA 2.0 (Abbott Laboratories) and for HIVantibody with HIV-1/HIV-2 recombinant DNA EIA (Ab-bott Laboratories) and found to be negative. A biopsy ofthe donor liver revealed mild steatosis.

The transplant surgeon accepted the donor liver. Thedonor heart and kidneys were accepted by other insti-tutions in Chicago, IL. Informed consent was obtainedwith a standard consent form from the recipient’s sonas the patient was encephalopathic. The patient under-went OLT, and the explant revealed nonalcoholic ste-atohepatitis with cirrhosis. No induction therapy withthymoglobulin or OKT3 was used. The patient was dis-charged on tacrolimus and corticosteroids on postop-erative day 8. The postoperative course was compli-cated by intermittently elevated liver enzymes, andmultiple liver biopsies suggested acute rejection andsubsequent biliary obstruction requiring therapeuticendoscopic retrograde cholangiopancreatography anda surgical bile duct revision. No findings were seen tosuggest an obvious diagnosis of HCV or HIV.

In November 2007, the local organ procurement or-ganization (OPO) notified our institution of the possibil-ity that the donor of the liver graft had been HIV-posi-tive and HCV-positive. Our institution was not providedwith the specific details that led to the follow-up testing,but later we learned from media reports that the heartand kidney recipients from the same donor (at otherinstitutions in Chicago, IL) had become HIV-positiveand HCV-positive by nucleic acid testing (NAT). For thisreason, our patient was tested for HIV and HCV. HCVantibody was negative, but HCV-RNA with the Abbottreal-time HCV assay (Abbott Molecular) was greaterthan 5,000,000 IU/mL. HIV-1 antibody was positivewith HIV-RNA greater than 500,000 copies/mL by theVersant HIV-1 RNA 3.0 branched DNA assay (BayerDiagnostics, Norwood, MA). The CD4 count was 34cells/mm3. The patient and her family were informed ofthe diagnoses by the transplant surgeons in their out-patient clinic. As expected, the patient and her familywere quite distraught. The patient became very de-pressed, and this condition subsequently worsenedover the remainder of her clinical course. She was re-ferred to the infectious disease clinic for evaluation andmanagement of her HIV.

Despite the low CD4 count, there were no overt man-ifestations of acquired immune deficiency syndrome atthe time of diagnosis. The patient was started on highlyactive antiretroviral therapy (HAART) with efavirenz,emtriva, and tenofovir. She was also started on prophy-laxis with sulfamethoxazole and trimethoprim, valgan-ciclovir, and azithromycin. Tacrolimus doses were de-

creased after the initiation of HAART and were adjustedto standard levels. The CD4 count increased to 112cells/mm3 5 weeks later. However, HAART was subse-quently held because of the patient’s clinical deteriora-tion with development of urosepsis, cytomegalovirusviremia, and acute renal failure. Extensive workup in-cluding endoscopic retrograde cholangiopancreatogra-phy, liver biopsy, and computed tomography scans ofthe entire body were most significant for multiple ring-enhancing lesions in the brain and subdural hemato-mas. Despite aggressive therapy, the patient expired atthe end of January 2008 (1 year post-OLT).

DISCUSSION

Transmission of HIV through solid organ transplanta-tion is extremely rare, with only sporadic case reportspublished1-8 (see Table 1). Most cases involved kidneytransplants prior to 1985, when HIV antibody donorscreening was implemented by the Public Health Ser-vice.9 The last reported case occurred in 1987.1 Sincethat time, more than 420,000 organ transplants havebeen performed in the United States.10 We report thefirst case of HIV transmitted by solid organ transplantin 20 years and the first case ever reported of simulta-neous HIV and HCV transmission.

Several potential mechanisms exist for the transmis-sion of HIV through organ transplantation, as shown inTable 1. These include testing of donors in the windowperiod between the time of exposure and the develop-ment of a positive HIV antibody, dilution of the donor’sserum by extensive transfusions, inappropriate timingof pretransplant HIV testing (in the case of living-re-lated transplant), inability to await the HIV test results,and false-negative HIV antibody tests. The time periodfrom HIV exposure to the development of HIV antibod-ies is approximately 22 days, but it can range up to 6months.11,12 By standard antibody testing, the patientsare HIV-negative, but they are still potentially infec-tious. The use of individual donor NAT allows the de-tection of HIV infection prior to antibody seroconver-sion, reducing this window period by approximately50% to 75%.13,14

In 1994, the Centers for Disease Control (CDC) issuedguidelines addressing donor screening, testing, and ex-clusion, as well as recipient testing, for prevention ofHIV transmission through organ transplantation.15 Ta-ble 2 lists the suggested donor exclusion criteria. Basedon the available data, the guidelines did not recom-mend the use of p24 antigen testing or NAT for HIV-RNA. The guidelines did note that these donors could beconsidered if “the risk to the recipient of not performingthe transplant is deemed to be greater than the risk ofHIV transmission and disease.” In those cases, in-formed consent was deemed essential. Posttransplanttesting of all solid organ recipients of high-risk donorsfor HIV was suggested but not mandated.

HCV transmission through transplantation has alsobeen described. The New England Organ Bank in 1991identified 29 recipients (19 kidneys, 6 hearts, and 4livers) of HCV-positive donor organs.16 Non-A–non-B

1604 AHN AND COHEN

LIVER TRANSPLANTATION.DOI 10.1002/lt. Published on behalf of the American Association for the Study of Liver Diseases

hepatitis developed in 48% of the recipients, with HCVconfirmed in 92% of those cases. Similar to HIV trans-mission, HCV transmission through transplantationhas also been documented during the 8- to 10-weekHCV window period.17 The conclusion from these stud-ies and from a CDC review was that NAT would havedetected the HCV infection prior to the transplants.18

The process of organ acquisition involves notificationof the local OPO of potential donor organs. They com-plete a risk assessment questionnaire to identify high-

risk donors as outlined in Table 2 according to the CDCguidelines.15 The OPO performs standard serologictesting, including pretransfusion and posttransfusiontesting for blood typing, HIV-1/HIV-2 antibodies byEIA, HCV antibody by EIA, hepatitis B surface antigenand hepatitis B core antibody, cytomegalovirus anti-body, and Epstein-Barr virus antibody as well as rapidplasma reagin screening. A plasma dilution worksheetis also completed to identify donors at increased risk offalse-negative testing from hemodilution. Current sero-

TABLE 1. Cases of HIV Transmission Through Solid Organ Transplantation

ReferenceYear of

OccurrenceYear ofReport

OrganTransplanted

Donor RiskFactor Donor HIV status

RecipientDemographics Recipient Outcome

1 1987 1989 Kidney(living-

related)

Homosexualmale

Negative EIAantibody 8 months

prior to donation.Found to be HIV

antibody positive onpostdonation

testing.

26-year-oldmale

Developed a mononucleosis-likeinfection 7 days post-

transplant. HIV seroconversion57 days post-transplant.

2 1986 1988 Liver Unknown Positive EIAantibody test, but

test results were notwaited for because

of FHF in recipient.

16-year-oldmale

HIV antibodies found 3 dayspost-transplant. Developed

acute HIV infection syndromeand aplastic anemia. Died 49

days post-transplant3 1985 1992 Heart Unknown Negative by 2

separate EIAantibody tests.

Retrospective testingof donor splenictissue confirmed

HIV.

55-year-oldmale

HIV antibodies positive by EIA(but negative on western blot)

found 8 months post-transplant. Had developed

herpes zoster, thrush,Pneumocystis carinii

pneumonia, CMV retinitis, andcerebritis. Died 10 months

post-transplant. Subsequenttesting on stored donor serum

revealed positive HIV-1 p24antigen.

3 1985 1992 Liver Unknown Negative by 2separate EIA

antibody tests.Retrospective testing

of donor splenictissue confirmed

HIV.

26-year-oldmale

Died from hepatic and renalfailure 24 days post-transplant.

Retrospective testing of storedsera showed positive HIV-1 p24

antigen.

3 1985 1992 Kidney Unknown Negative by 2separate EIA



HIV.

45-year-oldmale

Found to be HIV-positive at 17months post-transplant during

a dementia workup. Died 32months post-transplant.

3 1985 1992 Kidney Unknown Negative by 2separate EIA



HIV.

34-year-oldmale

Found to be HIV-positive 7months post-transplant. Hadalready lost the transplanted

kidney and was back ondialysis. Died because of

complications ofcardiomyopathy, pancreatitis,

and renal failure 14 monthspost-transplant.

4 1986 1987 Heart Multipleblood

transfusions(�50) prior to

death

Initial antibodytesting negative.

Found to be positiveon postdonation

testing.

Age andgender not

reported

Expired in the operating room.

4 1986 1987 Liver Multipleblood


death



testing.

Age notreported, male

Found to be HIV-positive at 3months post-transplant. No

HIV-related complicationsreported.

4 1986 1987 Kidney Multipleblood


death



testing.

Age notreported, male

Found to be HIV-positive at 2.5months post-transplant. No

HIV-related complicationsreported.

5 1984 1985 Kidney Hemophilia Unknown 42-year-oldmale

HTLV-III antibodies were found15 months post-transplant

during a workup for malaise,fever, and rash.

TRANSMISSION OF HIV AND HCV 1605


logic testing does not include NAT. The donor evalua-tion and risk assessment results are then provided tothe transplant center. The transplant surgeon has theoption of accepting or refusing the organ. If it is ac-cepted, the recipient is informed of the potential high-risk status of the donor. The recipient then has theoption to accept or decline the offer.

In light of this report, one solution would be avoidingthe use of any high-risk organs. However, with more

than 16,000 current OLT candidates on the waitinglist,10 a relatively constant number of OLTs being per-formed annually, and a substantial rate of waiting-listdeaths, this may not be the most appropriate choice.The dilemma of using high-risk donor organs requiresthe transplant center to balance the risk of furtherhepatic decompensation and death of the recipient ver-sus the very small but real risk of the transmission ofinfectious diseases. The potential recipient’s status

TABLE 1. (Continued)

ReferenceYear of

OccurrenceYear ofReport

OrganTransplanted

Donor RiskFactor

Donor HIVstatus

RecipientDemographics Recipient Outcome

5 1984 1985 Kidney Hemophilia Unknown 52-year-oldmale

HTLV-III antibodieswere found 16 months

post-transplant. Patientwas tested because of

the positive diagnosis inthe other kidney

recipient.6 1983 1987 Kidney Unknown Positive on

retrospectivetesting.

51-year-oldmale

Died from pneumonia16 days post-transplant.

No serum available fortesting.

6 1983 1987 Kidney Unknown Positive onretrospective

testing.

38-year-oldmale

HIV antibodies weredetected at 50 days

post-transplant. Patienthad been tested because

of fever, leukopenia,thrombocytopenia, and

adenopathy.6 1984 1987 Kidney Intravenous

drug useUnknown 28-year-old

maleHIV antibodies were

detected 56 days post-transplant. Patient hadbeen tested because of

fever, leukopenia,thrombocytopenia, and

acute splenomegaly.7 1984 1985 Kidney Intravenous


maleFever and leukopenia

occurred at 2 to 7 weekspost-transplant. HTLV-

III antibodies weredetected at 8 months

post-transplant.7 1984 1985 Kidney Intravenous


femaleFever and leukopenia





femaleFever and leukopenia





maleFever and leukopenia





femaleHTLV-III antibodieswere detected at 8

months post-transplant.Clinical course not

recorded.8 1982 1987 Kidney

(living-related)

Homosexualmale

Positive onretrospective

testing.

38-year-oldfemale

Patient developed fevers,anorexia, Pneumocystis

carinii pneumonia,histoplasmosis, and

Kaposi’s sarcoma. Thepatient died 10 months

post-transplant. HIVantibodies were noted

on retrospective testing.

Abbreviations: CMV, cytomegalovirus; EIA, enzyme immunoassay; FHF, fulminant hepatic failure; HIV, humanimmunodeficiency virus; HTLV-III, human T-lymphotropic virus type III.

1606 AHN AND COHEN


needs to be evaluated with surrogate markers such asthe Model for End-Stage Liver Disease score and overallfunctional status. Each center should have its own pol-icies and procedures in place to deal with such donororgan offers. Although it is controversial, many centers,including our own, consider high-risk and other ex-tended criteria donors for their OLT recipients. This isespecially true in cities and regions with intense com-petition for donor organs, as illustrated in this case inwhich 3 separate transplant centers used organs fromthis high-risk donor. Since the development of thiscase, our center has instituted the use of a specificconsent form to be used in cases of high-risk donors.The patient and his or her family must understand thepotential consequences of using such an organ as wellas the potential consequences of declining the organand remaining on the waiting list.

An alternative solution would be the implementationof NAT as a prerequisite to organ donation. However,many variables, such as a delay in organ utilization andan increase in costs, must be considered. Using ourhospital laboratory as a reference, we found that themost rapid turnaround time for HIV antibody is 1 hourwith the OraQuick Advance HIV-1/2 antibody test(Orasure Technologies, Bethlehem, PA). The turn-around time is 24 hours for HIV-RNA NAT, 4 hours forHCV antibody, and 24 hours for HCV-RNA NAT. Giventhese turnaround times, the additional delay of waitingfor NAT would be impractical as donor organs showdeterioration of function with increasing ischemictimes, which translates into overall inferior graft andrecipient outcomes. The incremental cost associatedwith NAT would also be considerably higher.

As an example of a technique for decreasing infec-tious disease transmission, pooled NAT was imple-mented for screening blood donations in 1999 for HIVand HCV. While successfully decreasing the risk of

transmission of both viruses, NAT does not completelyeliminate the risk because donor testing can still occurduring the window period.19-23 NAT for blood donationsis estimated to prevent 5 cases of HIV transmission and56 cases of HCV transmission annually at an estimatedcost of more than $100 million annually, or $1.5 to 4.3million per quality-adjusted year of life.24,25

If and when similar cases of HIV transmissionthrough solid organ transplantation occur in the fu-ture, our recommendation would be an honest andforthright approach in relaying the information. Oneshould explain how such an event could have occurredand how the current screening tests are imperfect andlimited. Each transplant center will need to individual-ize the approach on the basis of its relationship with thepatient, but incorporating the support of social work-ers, psychologists/psychiatrists, and even clergy maybe appropriate. An infectious disease specialist shouldbe consulted to help manage the patient appropriately.Also, providing positive feedback on the improved out-comes of HIV patients in the era of HAART and in thesetting of OLT, including the existence of a NationalInstitutes of Health–supported multicenter HIV OLTstudy, may be beneficial to the patient.26-30

In conclusion, we present the first reported case ofHIV transmission from solid organ transplantation in20 years and the first ever reported case of simulta-neously transmitted HIV and HCV. These infectionswere undetected by current screening tests becauseboth infections were present in their respective windowperiods in a high-risk donor. In this era of organ short-ages, each transplant center will need to weigh therisk-benefit ratio of using high-risk donor organs. Oneoption would be avoidance of any high-risk donor or-gans. Another option would be to consider the use ofsuch organs. However, the recipient must be informedof the limitations of the current testing methods inidentifying donors with potential HIV and HCV in thewindow period, prior to giving consent. The current NATturnaround time is too slow for practical use, and pre-vention of future cases will require the development ofmore rapid NAT but at a high cost with a low yield.Ultimately, this report should serve as a wake-up call toour transplant community to consider revamping do-nor screening for HIV and HCV using NAT and to re-evaluate the ongoing use of high-risk donors for OLT.

REFERENCES

1. Quarto M, Germinario C, Fontana A, Barbuti S. HIV trans-mission through kidney transplantation from a living do-nor. N Engl J Med 1989;320:1754.

2. Samuel D, Castaing D, Adam R, Saliba F, Chamaret S,Misset JL, et al. Fatal acute HIV infection with aplasticanaemia, transmitted by liver graft. Lancet 1988;1:1221-1222.

3. Simonds RJ, Holmberg SD, Hurwitz RL, Coleman TR, Bot-tenfield S, Conley LJ, et al. Transmission of human immu-nodeficiency virus type 1 from a seronegative organ andtissue donor. N Engl J Med 1992;326:726-732.

4. Centers for Disease Control. Human immunodeficiencyvirus infection transmitted from an organ donor screened

TABLE 2. Suggested Donor Exclusion Criteria

Laboratory and Medical Exclusionary Criteria

Positive HIV antibodyInability to test a donor’s HIV statusWorrisome signs or symptoms for the presence of HIVBehavior/History Exclusionary CriteriaMen having sex with men in the preceding 5 yearsUse of nonmedical injectable drugs in the preceding 5

yearsPersons with clotting disorders who have received

human-derived clotting factor concentratesPersons engaging in sex in exchange for money or

drugs in the preceding 5 yearsPersons having sex with any person described above

or with a high-risk or known/suspected HIV-positivepartner in the last year

Persons exposed to known or suspected HIV-infectedblood within the last year

Inmates of correctional facilities

Abbreviation: HIV, human immunodeficiency virus.

TRANSMISSION OF HIV AND HCV 1607


for HIV antibody—North Carolina. MMWR Morb MortalWkly Rep 1987;36:306-308.

5. Prompt CA, Reiss MM, Grillo FM, Kopstein J, Kraemer E,Manfro R, et al. Transmission of AIDS virus at renal trans-plantation. Lancet 1985;2:672.

6. Schwarz A, Hoffmann F, L’Age-Stehr J, Tegzess AM, Offer-mann G. Human immunodeficiency virus transmission byorgan donation. Transplantation 1987;44:21-24.

7. L’Age-Stehr J, Schwarz A, Offermann G, Langmaack H,Bennhold I, Niedrig M, Koch MA. HTLV-III infection inkidney transplant recipients. Lancet 1985;2:1361-1362.

8. Kumar P, Pearson JE, Martin DH, Leech SH, Buisseret PD,Bezbak HC, et al. Transmission of human immunodefi-ciency virus by transplantation of a renal allograft, withdevelopment of the acquired immunodeficiency syndrome.Ann Intern Med 1987;106:244-245.

9. Centers for Disease Control. Testing donors of organs,tissues, and semen for antibody to human T-lymphotro-phic virus type III/lymphoadenopathy-associated virus.MMWR Morb Mortal Wkly Rep 1985;34:294.

10. The Organ Procurement and Transplantation Network.Available at: http://www.optn.org/latestdata/rptdata-.asp. Accessed March 2008.

11. Busch MP, Lee LL, Satten GA, Henrard DR, Farzadegan H,Nelson KE, et al. Time course of detection of viral andserologic markers preceding human immunodeficiency vi-rus type 1 seroconversion: implications for screening ofblood and tissue donors. Transfusion 1995;35:91-97.

12. Horsburgh CR Jr, Ou C-Y, Jason J, Holmberg SD, LonginiIM Jr, Schable C, et al. Duration of human immunodefi-ciency virus infection before detection of antibody. Lancet1989;16:637-640.

13. Busch MP, Glynn SA, Stramer SL, Strong DM, Caglioti S,Wright DJ, et al. A new strategy for estimating risks oftransfusion-transmitted viral infections based on rates ofdetection of recently infected donors. Transfusion 2005;45:254-264.

14. Fiebig EW, Wright DJ, Rawal BD, Garrett PE, SchumacherRT, Peddada L, et al. Dynamics of HIV viremia and anti-body seroconversion in plasma donors: implications fordiagnosis and staging of primary HIV infection. AIDS2003;17:1871-1879.

15. Centers for Disease Control. Guidelines for preventingtransmission of human immunodeficiency virus throughtransplantation of human tissue and organs. MMWRRecomm Rep 1994;43:1-17.

16. Pereira BJG, Milford EL, Kirkman RL, Levey AS. Trans-mission of hepatitis C virus by organ transplantation.N Engl J Med 1991;325:454-460.

17. Tugwell BD, Patel PR, Williams IT, Hedberg K, Chai F,Nainan OV, et al. Transmission of hepatitis C virus toseveral organ and tissue recipients from an antibody-neg-ative donor. Ann Intern Med 2005;143:648-654.

18. Centers for Disease Control. Hepatitis C virus transmis-sion from an antibody-negative organ and tissue donor—United States, 2000-2002. MMWR Morb Mortal Wkly Rep2003;52:273-276.

19. Schreiber GB, Busch MP, Kleinman SH, Korelitz JJ. Therisk of transfusion-transmitted viral infections. N EnglJ Med 1996;334:1685-1690.

20. Lackritz EM, Satten GA, Aberle-Grasse J, Dodd RY, Rai-mondi VP, Janssen RS, et al. Estimated risk of transmis-sion of the human immunodeficiency virus by screenedblood in the United States. N Engl J Med 1995;333:1721-1725.

21. Dodd RY, Notari IV, Stramer SL. Current prevalence andincidence of infectious disease markers and estimatedwindow-period risk in the American Red Cross blood do-nor population. Transfusion 2002;42:975-979.

22. Phelps R, Robbins K, Liberti T, Machuca A, Leparc G,Chamberland M, et al. Window-period human immunode-ficiency virus transmission to two recipients by an adoles-cent blood donor. Transfusion 2004;44:929-933.

23. Schuttler CG, Caspari G, Jursch CA, Willems WR, GerlichWH, Schaefer S. Hepatitis C virus transmission by a blooddonation negative in nucleic acid amplification tests forviral RNA. Lancet 2000;355:41-42.

24. Jackson BR, Busch MP, Stramer SL, AuBuchon JP. Thecost-effectiveness of NAT for HIV, HCV, and HBV in whole-blood donations. Transfusion 2003;43:721-729.

25. Marshall DA, Kleinman SH, Wong JB, AuBuchon JP,Grima DT, Kulin NA, Weinstein MC. Cost-effectiveness ofnucleic acid test screening of volunteer blood donationsfor hepatitis B, hepatitis C, and human immunodeficiencyvirus in the United States. Vox Sang 2004;86:28-40.

26. Duclos-Vallee JC, Feray C, Sebagh M, Teicher E, Roque-Alfonso AM, Roche B, et al. Survival and recurrence ofhepatitis C after liver transplantation in patients coin-fected with human immunodeficiency virus and hepatitisC virus. Hepatology 2008;47:407-417.

27. Mindikoglu AL, Regev A, Magder LS. Impact of humanimmunodeficiency virus on survival after liver transplan-tation: analysis of United Network for Organ Sharing Da-tabase. Transplantation 2008;85:359-368.

28. Schreibmann I, Gaynor JJ, Jayaweera D, Pyrsopoulos N,Weppler D, Tzakis A, et al. Outcomes after orthotopic livertransplantation in 15 HIV-infected patients. Transplanta-tion 2007;84:697-705.

29. Samuel D, Weber R, Stock P, Duclos-Vallee JC, Terrault N.Are HIV-infected patients candidates for liver transplan-tation. J Hepatol 2008;48:697-707.

30. Roland ME, Barin B, Carlson L, Frassetto LA, Terrault NA,Hirose R, et al. HIV-infected liver and kidney transplantrecipients:1-and3-yearoutcomes.AmJTransplant2008;8:355-365.

1608 AHN AND COHEN


transmission of human immunodeficiency virus and hepatitis c virus through liver transplantation

Documents