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Xenotropic Murine Leukemia Virusrelated Virus COMMITTEE REPORT Xenotropic murine leukemia virus–related virus (XMRV) and blood transfusion: report of the AABB interorganizational XMRV task force_3012 654..661 Harvey G. Klein, Roger Y. Dodd, F.Blaine Hollinger, Louis M. Katz, Steven Kleinman, K. Kimberly McCleary, Robert H. Silverman, and Susan L. Stramer for the AABB Interorganizational Task Force on XMRV n October 2009, a report in the journal Science iden- AABB about informing donors, recipients, physicians, tified evidence of infection with the retrovirus xeno- and the general public regarding the risk of XMRV tropic murine leukemia virus–related virus (XMRV) transmission. in the blood of two-thirds of 101 patients diagnosed Iwith chronic fatigue syndrome (CFS) and in 3.7% of 218 healthy control subjects.1 This was not the first report of CHARACTERISTICS OF XMRV XMRV nor the first association of these viral sequences XMRV is a member of the Gammaretrovirus genus of the 2 with human tissue. However, because this study recov- Orthoretrovirinae subfamily of Retroviridae with high ered virus from lymphocytes, these findings raised con- sequence similarity to endogenous murine leukemia cerns anew about a possible pathologic role of XMRV and viruses.3 XMRV was so named because its envelope gene its potential transmission by blood transfusion. As a result was similar to that of xenotropic murine leukemia virus of this publication, in December 2009 the AABB (formerly (MLV), an endogenous MLV that infects cells from non- American Association of Blood Banks) established an mouse species including humans. Similar agents are Interorganizational Task Force composed of representa- found in a wide range of mammalian species and include tives of blood collectors, government agencies, and not- the porcine endogenous retrovirus, the feline leukemia for-profit organizations dedicated to CFS research and virus, the koala retrovirus, and the gibbon ape leukemia policy, supplemented with additional scientific consult- virus. Although XMRV has been portrayed by some as an ants. The Task Force was charged with reviewing the AIDS-like virus, this description is not accurate. Gam- available data on XMRV, recommending action to assess maretroviruses are much simpler than the complex and if necessary mitigate the risk of transmitting XMRV deltaviruses such as human T-lymphotropic virus (HTLV), through blood and cellular therapy products, and advising or the complex lentiviruses such as human immunodefi- ciency virus (HIV). The XMRV genome includes gag, pol, and env genes but no accessory or regulatory genes.3 As the name implies, XMRV is believed to have originated in ABBREVIATIONS: CFS = chronic fatigue syndrome; mice and is the first agent of its class to be identified in XMRV = xenotropic murine leukemia virus–related virus. humans; it likely evolved as a result of a recombination From the Department of Transfusion Medicine, National Insti- event between polytropic and xenotropic MLV. Its patho- tutes of Health, Bethesda, Maryland. genic potential in humans is unknown. Address reprint requests to: Harvey G. Klein, MD, Depart- The XMRV virions consist of an envelope, a nucleo- ment of Transfusion Medicine, Clinical Center RM 1C-711, capsid, and a nucleoid. The virions are spherical to pleo- National Institutes of Health, Bethesda MD 20892; e-mail: morphic and measure 80 to 100 nm in diameter. The [email protected]. genome is a dimer of linear, positive-sense, single- The views expressed do not necessarily represent the view stranded RNA, approximately 8300 nucleotides long. of the National Institutes of Health, the Department of Health XMRV is resistant to many of the antiretroviral drugs used and Human Services, or the U.S. Federal Government. to treat HIV-1 infection, but is sensitive to a subset of these Received for publication October 9, 2010; revision received inhibitors in vitro. The divergent drug sensitivity profiles October 25, 2010, and accepted October 25, 2010. of XMRV and HIV-1 are partially explained by specific doi: 10.1111/j.1537-2995.2010.03012.x amino acid differences in their respective protease, TRANSFUSION 2011;51:654-661. reverse transcriptase (RT), and integrase sequences.4 As 654 TRANSFUSION Volume 51, March 2011 XMRV AND BLOOD TRANSFUSION TESTING FOR XMRV Research studies on XMRV have employed a number of different assays including the polymerase chain reaction (PCR) assay (nested and real-time PCR) and fluorescence in situ hybridization for direct detection of the viral sequences; serologic assays for detection of circulating antibodies against XMRV include flow cytometry, Western blot and chemiluminescent immunoassays and enzyme- linked immunoassay techniques; immunohistochemical assays have been used for direct detection of viral pro- teins; and cell culture assays used for detection of infec- tious virus. It has been difficult to compare assay results from different laboratories due to differences in primer pair or antigen selection, assay reaction conditions, specimen type, and specimen preparation and storage conditions. Currently, commercial high-throughput assays are under development; validation of these assays will be critical for large-scale epidemiologic studies. At this stage of assay development, there are no FDA- licensed diagnostic or blood donor-screening assays. The U.S. Department of Health and Human Services has established the Blood XMRV Scientific Research Working Group to evaluate XMRV nucleic acid and anti- body assays, establish prevalence of XMRV in blood Fig. 1. Transmission electron microscope image of XMRV donors, determine if XMRV is transfusion-transmitted, courtesy of Dr John Hackett Jr. (Abbott Diagnostics, Abbott and if so, whether transfusions are associated with any Park, IL). recipient disease. As a first step, the Working Group has established analytical panels and evaluated the perfor- mance of its six participating laboratories in detecting XMRV nucleic acid in whole blood, peripheral blood an enveloped retrovirus, XMRV should be susceptible to mononuclear cells (PBMNCs), and plasma samples spiked heat, detergents, and many disinfectants. A photomicro- with known concentrations of a single XMRV isolate. The graph of XMRV virions is provided in Fig. 1. next step involves pilot clinical studies that will compare Although little is known about XMRV infectivity, results from whole blood, PBMNC specimens, and plasma tissue tropism, in vivo reservoirs, and persistence in to investigate methods of collection, processing, freezing, humans, preliminary information has been obtained from and other issues related to sample preparation and an animal model. Five rhesus macaques inoculated storage. These studies will allow preparation of clinical intravenously with XMRV developed transient, low-level panels to evaluate assay performance on pedigreed viremia between Day 4 and Day 21.5 Villinger et al. clinical samples including well-characterized negative reported at the First International Workshop on XMRV controls. Once assay methods are optimized at the partici- in September 2010 (http://www.virology-education.com/ pating laboratories, testing of coded panels of blood index.cfm/t/Workshop_material/vid/1A5D65BD-FB8B- samples obtained primarily from healthy blood donors 8AE1-5E10829372D080B4) that XMRV targeted CD4+ T and from CFS patients can be performed to determine the cells in lymphoid organs, macrophages in lungs, and epi- prevalence of XMRV sequences and seropositivity. thelial or interstitial cells in other organs. Animals sacri- ficed early showed evidence of viral replication in spleen, lung, lymph node, and prostate tissue. Two animals eutha- XMRV EPIDEMIOLOGY AND nized at 19 weeks after XMRV reinoculation showed wide DISEASE ASSOCIATIONS dissemination of XMRV DNA and RNA including in the gastrointestinal and reproductive tracts as well as in the Evidence of human infection with XMRV was first vaginal tissue of the one female animal. All three chroni- reported in 2006 when genome sequences from a previ- cally infected animals developed antibody responses to ously undescribed gammaretrovirus, XMRV were detected env and gag proteins by Western blot assays. No animal in a cohort of US men with localized prostate cancer developed evidence of illness more than 8 months after undergoing radical prostatectomy.2 The investigators pro- inoculation. posed that these men expressed a homozygous mutation Volume 51, March 2011 TRANSFUSION 655 KLEIN ET AL. TABLE 1. Comparison of published XMRV studies in patients with CFS + CFS patients (%) + Controls (%) Study criteria source Sample source Assays Patient selection Lombardi et al.1,a 68/101 (67) NAT 8/218 (3.7) 0/7 Activated PBMNC Nested PCR 25 patients Incline 9/18 (50) serology serology subjects plasma serology gag village NV and 76 Fukuda, Canadian undergoing routine culture sporadic cases in medical testing United States Erlwein et al.13 0/186 Fukuda NT PBMNCs Nested XMRV, MLV UK patients with PCR CFS Groom et al.14 0/142 NAT 1/28 0/395 NAT PBMNCs Real time- PCR env Two UK cohorts with serology Fukuda 25/395 (6.3) Viral neutralization CFS criteria serology; only 1/26 from a CFS patient Van Kuppeveld 0/32 NAT Sharpe 0/43 NAT matched PBMNCs Nested PCR (gag) Netherlands matched et al.15 neighborhood Real case-control study control time-PCR (int) Switzer et al.16 0/51 NAT, WB, 0/53 0/41 serology PBMNC plasma Nested PCR, WB, Survey-identified ELISA, IFA healthy US blood ELISA, IFA tested patients from Reeves 2005 donors in three labs Georgia and Wichita, KS Lo et al.18 32/37 (86.5) NAT 3/44 (6.8) MLV-like PBMNC plasma Nested PCR gag CFS cohort followed MLV-like virus virus US blood and env in Boston clinic Fukuda criteria donors Hong et al.17 0/65 Fukuda criteria 0/85 Chinese blood PBMNC plasma Multiplex RT-PCR; Chinese cohort of donors—65 RT-PCR CFS patients from healthy, 20 Peking Medical infected with HBV, College Hospital HCV, HIV, HTLV a [Correction added after online publication 14-Jan-2011. Nat and serology numbers have been updated.] (R462Q) of the antiviral enzyme RNase L rendering them XMRV has also been associated with CFS (also susceptible to infection by this virus and to its possible referred to as CFS-myalgic encephalitis), a debilitating oncogenic potential.
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