Original Article
Transmission of Rabies Virus from an Organ Donor to Four Transplant Recipients
N Engl J Med 2005; 352:1103-1111March 17, 2005
- Abstract
Background
In 2004, four recipients of kidneys, a liver, and an arterial segment from a common organ donor died of encephalitis of an unknown cause.
Methods
We reviewed the medical records of the organ donor and the recipients. Blood, cerebrospinal fluid, and tissues from the recipients were tested with a variety of assays and pathological stains for numerous causes of encephalitis. Samples from the recipients were also inoculated into mice.
Results
The organ donor had been healthy before having a subarachnoid hemorrhage that led to his death. Encephalitis developed in all four recipients within 30 days after transplantation and was accompanied by rapid neurologic deterioration characterized by agitated delirium, seizures, respiratory failure, and coma. They died an average of 13 days after the onset of neurologic symptoms. Mice inoculated with samples from the affected patients became ill seven to eight days later, and electron microscopy of central nervous system (CNS) tissue demonstrated rhabdovirus particles. Rabies-specific immunohistochemical and direct fluorescence antibody staining demonstrated rabies virus in multiple tissues from all recipients. Cytoplasmic inclusions consistent with Negri bodies were seen in CNS tissue from all recipients. Antibodies against rabies virus were present in three of the four recipients and the donor. The donor had told others of being bitten by a bat.
Conclusions
This report documenting the transmission of rabies virus from an organ donor to multiple recipients underscores the challenges of preventing and detecting transmission of unusual pathogens through transplantation.
Media in This Article
Figure 1
The Clinical Course of Four Recipients of Rabies-Infected Tissue or Organs.Figure 2
Axial Fluid-Attenuated Inversion Recovery MRI Scan Showing Profound Signal Abnormalities within the Bilateral Frontal and Temporal Lobes, Hippocampi, Basal Ganglia, and Medulla in Patient 2.Article Activity
- Article
Rabies is an acute encephalitis caused by viruses in the genus Lyssavirus, family Rhabdoviridae, that is nearly uniformly fatal in unvaccinated hosts. Although the virus is present in animal reservoirs, infection in humans is rare in the United States, with only two cases reported in 20031,2 and no more than six cases reported in any year in the past decade.3 The primary mode of transmission is through the bite of an infected animal, most commonly a bat in the United States.4 Although transmission of rabies virus from corneal transplants has previously been described,5 to our knowledge, no cases ascribed to organ or vascular-tissue transplants have been reported.
In May 2004, physicians at a hospital in Texas diagnosed encephalitis in three recipients of a liver and two kidneys from a common organ donor. It was later discovered that encephalitis also developed in a fourth patient, who had received a vascular graft from the same donor during liver transplantation. All four patients became progressively obtunded, lapsed into coma, and died within 50 days after transplantation. The initial diagnostic evaluation revealed no cause of the encephalitis, and assistance was sought from the Centers for Disease Control and Prevention (CDC) and the Texas Department of State Health Services. We report the results of this investigation.
Case Reports
Transplant Recipients
In May 2004, encephalitis was diagnosed in three recipients of a liver and two kidneys (Patients 2, 3, and 4 in Figure 1Figure 1
The Clinical Course of Four Recipients of Rabies-Infected Tissue or Organs.) from a common organ donor. In all three patients, signs and symptoms of altered mental status and progressively worsening encephalitis developed within 30 days after transplantation. Major clinical events and immunosuppressive medications are summarized in Figure 1. All patients had rapid neurologic deterioration characterized by agitated delirium and seizures. Respiratory failure requiring intubation developed within 48 hours after the onset of neurologic symptoms. Examination of cerebrospinal fluid from the three patients showed pleocytosis, with an average of 18 cells per cubic millimeter (range, 7 to 35), and elevated protein levels (mean, 135 mg per deciliter; range, 17 to 331). Neurologic imaging in the week after the onset of symptoms showed no evidence of an acute cerebral process. Magnetic resonance imaging (MRI) performed later in the course of illness demonstrated diffuse signal abnormalities, most often in the temporal lobes, basal ganglia, brain stem, and hippocampi on T2-weighted and fluid-attenuated inversion recovery images (Figure 2Figure 2Axial Fluid-Attenuated Inversion Recovery MRI Scan Showing Profound Signal Abnormalities within the Bilateral Frontal and Temporal Lobes, Hippocampi, Basal Ganglia, and Medulla in Patient 2.). There was minimal enhancement after the administration of gadolinium. The patients died an average of 13 days after the onset of neurologic symptoms (range, 7 to 23).Organ Donor
Four days before death, the organ donor was seen twice at an emergency department for nausea, vomiting, and difficulty swallowing. He was subsequently admitted to another hospital with altered mental status requiring intubation. Physical examination revealed a temperature of 38.1°C (100.5°F) and fluctuating blood pressures, including systolic measurements of more than 200 mm Hg. On admission, a urine toxicology screen was positive for cocaine and marijuana, and computed tomography of the brain demonstrated a subarachnoid hemorrhage. The hemorrhage progressed, and the neurologic symptoms, including seizures and coma, worsened. The patient was declared brain-dead within four days after presentation. Donor-eligibility screening and testing performed by an organ-procurement organization, including a review of premortem blood, urine, and sputum bacterial cultures, did not detect any signs or symptoms of infection precluding solid-organ donation. The patient's kidneys, lungs, and liver were removed for transplantation; in addition, iliac arteries were harvested for potential use in vascular reconstruction during the liver transplantation. In part because of the positive toxicology result, nonorgan tissues (e.g., tendons) were not removed. During contact investigations conducted after the rabies diagnoses were made, friends of the donor indicated he had reported being bitten by a bat.
Methods
Clinical and Epidemiologic Review
Medical records of the donor and infected transplant recipients were reviewed to characterize clinical courses and diagnostic evaluations. After the laboratory diagnosis of rabies infection in the three organ recipients, case finding was performed to search for other possible cases. Hospital autopsy records on patients with encephalitis were reviewed for pathological findings consistent with the presence of rabies. Also, charts of patients who had been on the same floor as a patient with rabies and who had also had a lumbar puncture or neurology consultation for altered mental status were examined for documented clinical findings consistent with the presence of rabies. Procedures for organ recovery and handling were also reviewed.
Laboratory Methods
Formalin-fixed, paraffin-embedded tissue specimens, obtained at autopsy, were stained with hematoxylin and eosin and various immunohistochemical stains according to a method described previously.6 For immunohistochemical assays, 3-μm tissue sections were deparaffinized, rehydrated, and digested in proteinase K. Tissue sections were incubated for 60 minutes at room temperature with a hyperimmune rabbit antiserum or mouse ascitic fluid with reactivity to rabies virus. After sequential application of the appropriate biotinylated linked antibody, avidin–alkaline phosphatase complex, and naphthol fast-red substrate, sections were counterstained in Meyer's hematoxylin and mounted with the use of aqueous mounting medium. Serologic analyses, detection of viral antigen in tissue by means of fluorescence microscopy, and identification of rabies virus variants were performed as described previously.7,8 Controls included serum specimens from noninfected animals, tissues from humans with nonrabies encephalitides, and rabies-infected human tissues. Immunohistochemical assays for various other viral, rickettsial, and protozoan agents of encephalitis were also performed on tissues from recipients.
Vero E6 cells were inoculated with CSF and 10 percent tissue suspensions from three of the four rabies-infected recipients (Patients 2, 3, and 4). Suckling mice were inoculated intracranially and intraperitoneally with cerebrospinal fluid and 10 percent clarified homogenates of brain tissue, spinal cord, and kidney suspensions. Tissue cultures and suckling mice were observed daily for cytopathic effects and signs of illness, respectively. Tissues obtained from suckling mice that developed neurologic signs or died were fixed in 10 percent neutral buffered formalin or 2.5 percent buffered gluteraldehyde or were frozen for further evaluation. At 14 days, the Vero E6 cells were suspended in saline, fixed on glass slides, and tested for the presence of rabies virus antigen by means of a direct fluorescence antibody assay according to a previously described method.9 Immunohistochemical studies were performed as described above, and formalin-fixed tissues were embedded for examination by electron microscopy.
Results
Review of Transplantation Records
All organs obtained from the donor were transplanted; the lung recipient died of intraoperative complications. Iliac arteries from the donor were not used during the liver transplantation in Patient 2 and were placed in a sterile container and stored for potential use in subsequent transplantation procedures. One day after the organs were transplanted, the iliac-artery segment was retrieved and used to construct a vascular graft for another liver-transplant procedure (in Patient 1).
Rabies Case Finding
In addition to the three initial cases noted by physicians, autopsy review identified a fourth patient (Patient 1 in Figure 1) in whom progressive, fatal encephalitis had developed after liver transplantation. This patient had received the vascular segment from the rabies-infected donor. A review of the medical records of patients who had been on the same floor as a patient with rabies and who had had a lumbar puncture or neurology consultation for altered mental status revealed no further cases of encephalitis consistent with the presence of rabies.
Pathological Findings
Histopathological evaluation of tissues from all four rabies-infected transplant recipients demonstrated diffuse, predominantly lymphohistiocytic, infiltrates and microglial nodules involving the cerebrum, brain stem, cerebellum, and spinal cord. Cytoplasmic inclusions consistent with Negri bodies were identified throughout the central nervous system (CNS), particularly in the Purkinje cells of the cerebellum and in neurons of the frontal cortex, thalamus, hippocampus, midbrain, and pons (Figure 3AFigure 3
Histopathological Findings in Patient 4.). Lymphohistiocytic infiltrates involving the peripheral nerves, heart, and kidneys were also noted in some patients. Electron microscopy of the midbrain of Patient 4 demonstrated abundant rhabdovirus particles (Figure 3B). Intracytoplasmic rabies virus antigens were detected on immunohistochemical staining in neurons from multiple areas of the CNS (Figure 3C); in peripheral nerves of the transplanted kidneys, liver, and arterial graft (Figure 4Figure 4
Immunohistochemical Staining (Red) of Rabies Virus Antigens in Peripheral Nerves of the Liver (Panels A and B), Kidney (Panel C), and Arterial-Graft Transplants (Panel D).); and in renal tubular epithelium, smooth muscle, histiocytes, and vascular endothelium. No tissues were positive for enteroviruses, human herpesviruses 1 and 2, West Nile and other flaviviruses, eastern equine encephalomyelitis virus, lymphocytic choriomeningitis virus, Cache Valley virus, henipaviruses, measles virus, spotted fever and typhus group rickettsiae, Toxoplasma gondii, or Trypanosoma cruzi on immunohistochemical analysis. Direct fluorescence antibody staining also demonstrated rabies virus antigens in CNS tissues from all recipients.Serologic Analyses and Viral Identification
Antibodies (IgM and IgG) reactive to rabies virus were present in the donor's serum at the time of death. Antibodies were also present in three of the four recipients in samples obtained on postoperative days 35 and 36; both IgM and IgG antibodies were present in one kidney recipient (Patient 3) and the recipient of the donor's liver (Patient 2), whereas only IgG antibodies were present in the patient who received the arterial segment (Patient 1). Antigenic typing revealed a previously characterized rabies virus variant associated with bats.
Cell Culture and Mouse Inoculations
All suckling mice had neurologic abnormalities or had died seven to eight days after inoculation. Thin-section electron microscopy of CNS tissue demonstrated rhabdovirus particles, and IHC testing detected rabies virus antigens in mouse CNS tissues. Cultures of Vero E6 cells inoculated with brain, spinal cord, and kidney from a kidney recipient demonstrated rabies virus antigen on staining with DFA.
Discussion
This report describes the transmission of rabies virus through the transplantation of solid organs and vascular material. Four patients who received transplants — three organs and one vascular segment — from a donor with unrecognized rabies infection subsequently died of rabies. The transmission of rabies from corneal transplants has been described previously.5
Rabies is seldom included in the differential diagnosis of encephalitis in the absence of a documented exposure or suggestive history.8,10 The symptoms in the cases reported here, including fever, changes in mental status, and autonomic instability, were, in retrospect, consistent with a diagnosis of rabies. However, the diagnosis was complicated by the absence of a history of exposure at presentation and by the number of other potential causes of illness in these immunosuppressed patients. A history of a bat bite in the donor was discovered during contact interviews only after rabies had been diagnosed, and the investigation initiated. The diagnosis in the donor was further complicated by the presence of a subarachnoid hemorrhage in the setting of hypertension and a positive toxicology screen for cocaine. It is not known whether rabies infection was the cause of the subarachnoid hemorrhage, since this finding has not been noted in previous reports.11-13
Signs of rabies developed in all four transplant recipients within 30 days after infection. According to previous reports, symptoms developed within 30 days after an animal bite in only 25 percent of patients.10 It is unknown whether the shorter incubation period in these patients was due to the immunosuppression, the route of transmission, or both. The effect of immunosuppression on rabies infection is currently not well understood. In reports of rabies transmission from corneal transplants in patients who were not immunosuppressed and did not receive postexposure prophylaxis, symptoms developed an average of 26 days after transplantation,14-17 suggesting that implantation of material from infected donors may lead to a shorter incubation period. Three of our patients presented with commonly described symptoms of tremors and changes in mental status, whereas the fourth presented with abdominal and flank pain, which may have been neuropathic, and changes in mental status occurred about 48 hours later. The rapidly progressive encephalitis, with death occurring an average of 13 days after the onset of symptoms, is consistent with the course in other reports.4
There is only one reported case of recovery from clinical rabies by a patient who had not received preexposure or postexposure prophylaxis against rabies.18 However, administration of postexposure prophylaxis with rabies immune globulin and vaccine is highly effective in preventing infection after exposure. In a previous report, administration of postexposure prophylaxis probably prevented infection in a patient who had received a cornea from a donor with rabies.19
This report and another, describing the transmission of West Nile virus through solid-organ transplantation,20 underscore the potential for transmission of unexpected infectious diseases through organ transplantation. Recognition and prevention of transplant-transmitted infections may be improved in various ways, including enhanced donor screening and testing, the development of standardized procedures related to storage and use of donor vascular segments, as well as methods to track their use or nonuse, and enhanced means of detection and diagnosis of illnesses in recipients.
To minimize the risk of transmitting infections during organ transplantation, the Organ Procurement and Transplantation Network (OPTN) has established standards that require organ-procurement organizations to assess the risks of infectious diseases through screening questions and blood testing for selected bloodborne viral pathogens and syphilis.21 Questions about potential exposure to rabies are generally not included, and laboratory testing for rabies infection is not performed. Organs can be procured from donors who are febrile, provided that the medical director of the organ-procurement organization and the transplantation physicians agree that the cause of the fever does not pose an unacceptable risk to the recipient. Given the growing importance of emerging and reemerging infectious diseases, the ability of general improvements in the donor-screening process, rather than disease-specific measures, to increase organ safety should be evaluated. A proposed revision of OPTN policies would expand the list of potentially transmittable diseases and conditions that clinicians should consider in determining a donor's eligibility.22 The revision emphasizes that when any of these conditions is known or suspected in a donor, this information should be conveyed immediately to the organ-procurement organization as well as to all transplantation centers that received organs from the donor.
The successful use of donor arterial conduits has been reported in liver transplantation23-26 and in the management of vascular complications in recipients of both hepatic transplants27,28 and renal transplants.29 As with organs, these vessel segments have the potential to transmit infection. A careful accounting of and an ability to track donated material, such as vessel conduits, are essential in efforts to link unexplained illnesses or deaths to a common organ donor and will increase the probability of quickly identifying all recipients who may be at risk from donor infections. Proposed revisions of the policies of both OPTN22 and the Joint Commission on Accreditation of Healthcare Organizations30 may help address the storage of vessel conduits and documentation of their use or nonuse.
Our investigation underscores the challenge in detecting and diagnosing infections that occur in recipients of organs or tissues from a common donor. The potential for disease transmission from a donor as a cause of illness or death may not be considered in the evaluation of an individual recipient. In this investigation, and in the previous report of the transmission of West Nile virus through transplantation, the ability to connect illnesses to a common organ donor was facilitated by the fact that multiple recipients were hospitalized at the same facility. Improved national detection of unexpected or serious outcomes among transplant recipients may facilitate the discovery of transplant-related transmission of emerging and unusual pathogens by allowing connections to common donors to be made. The ability to make retrospective diagnoses of infections in organ donors when unexplained deaths or illnesses occur in recipients is hampered by the limited availability of donor samples, particularly tissue; currently, only serum samples from organ donors are retained for any length of time. Investigations into possible transplantation-associated infections would be facilitated by the availability of selected, archived tissue samples from the donor and by autopsy reports and materials. An improved diagnostic ability may have important implications for other patients who received material from the donors and for contacts of the patients and donors.
As organ and tissue transplantation becomes more common, the potential risks of disease transmission may increase. Cases of transplantation-associated infections provide important opportunities to review practices in an attempt to enhance the safety of transplantation without affecting the organ supply. The Department of Health and Human Services, including the CDC, is working with other partners in the organ- and tissue-transplantation community to review donor-screening practices, the use of retained vascular segments, and surveillance of recipients for illness. Clinicians who care for organ-transplant recipients should continue to be aware of the potential for disease transmission through transplantation and the challenges in recognizing atypical presentations of infections in this immunosuppressed population. Clinicians should report unexpected outcomes or unexplained illnesses in transplant recipients to their local organ- and tissue-procurement organization.
We are indebted to the state health departments in Oklahoma and Alabama, to the Southwest Transplant Alliance, and to the staff of the Baylor University Medical Center for their assistance with this investigation.
Source Information
From the Divisions of Healthcare Quality Promotion (A.S., D.C., D.B.J.) and Viral and Rickettsial Diseases (M.J.K., C.R., T.G.K., C.D.P., J.G., W.-J.S., C.G., C.A.H., M.N., L.O., J.L., M.E.C., S.R.Z.), National Center for Infectious Diseases, and the Epidemic Intelligence Service Branch, Division of Applied Public Health Training, Epidemiology Program Office (A.L.), Centers for Disease Control and Prevention, Atlanta; Baylor University Medical Center, Dallas (E.C.B., W.L.S., B.F., W.H.E., E.Q.S., G.B.K.); and the Texas Department of State Health Services, Austin (J.Z.).
Members of the Rabies in Transplant Recipients Investigation Team are listed in the Appendix.
Appendix
The other members of the Rabies in Transplant Recipients Investigation Team are as follows: J.A. Comer, J. Dillaha, B. Flow, D. Johnson, J. McQuiston, M. J. Opatowsky, N. Pascoe, D. Perrotta, P. Rollin, D. Swerdlow, B. Tierney, J. D. Walker, F. Wilson, and P. Yager.
- References
References
1
First human death associated with raccoon rabies -- Virginia, 2003. MMWR Morb Mortal Wkly Rep 2003;52:1102-1103
Medline2
Human death associated with bat rabies -- California, 2003. MMWR Morb Mortal Wkly Rep 2004;53:33-35
Medline3
Cases of rabies in human beings in the United States, by circumstances of exposure and rabies virus variant, 1990-2001. (Accessed February 23, 2005, at http://www.cdc.gov/ncidod/dvrd/rabies/professional/publications/Surveillance/Surveillance01/Table2-01.htm.)
4
Bleck TP, Rupprecht CE. Rabies virus. In: Mandell GL, Bennett JE, Dolin R, eds. Principles and practice of infectious diseases. Philadelphia: Churchill Livingstone, 2000:1811-20.
5
Doe J . Human rabies prevention -- United States, 1999: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 1999;48:1-21[Erratum, MMWR Recomm Rep 1999;48:16, 2000;49:737.]6
Zaki SR ,Greer PW ,Coffield LM , et al. Hantavirus pulmonary syndrome: pathogenesis of an emerging infectious disease. Am J Pathol 1995;146:552-579
Web of Science | Medline7
Warner CK ,Zaki SR ,Shieh WJ , et al. Laboratory investigation of human deaths from vampire bat rabies in Peru. Am J Trop Med Hyg 1999;60:502-507
Web of Science | Medline8
Noah DL ,Drenzek CL ,Smith JS , et al. Epidemiology of human rabies in the United States, 1980 to 1996. Ann Intern Med 1998;128:922-930
Web of Science | Medline9
Protocol for postmortem diagnosis of rabies in animals by direct fluorescent antibody testing: a minimum standard for rabies diagnosis in the United States. (Accessed February 23, 2005, at http://www.cdc.gov/ncidod/dvrd/rabies/professional/publications/DFA_diagnosis/DFA_protocol-b.htm.)
10
Anderson LJ ,Nicholson KG ,Tauxe RV ,Winkler WG . Human rabies in the United States, 1960 to 1979: epidemiology, diagnosis, and prevention. Ann Intern Med 1984;100:728-735
Web of Science | Medline11
Esiri MM, Kennedy PGE. Virus diseases. In: Adams JH, Duchen LW, eds. Greenfield's neuropathology. 5th ed. New York: Oxford University Press, 1992:335-99.
12
Awasthi M ,Parmar H ,Patankar T ,Castillo M . Imaging findings in rabies encephalitis. AJNR Am J Neuroradiol 2001;22:677-680
Web of Science | Medline13
Mani J ,Reddy BC ,Borgohain R ,Sitajayalakshmi S ,Sundaram C ,Mohandas S . Magnetic resonance imaging in rabies. Postgrad Med J 2003;79:352-354
CrossRef | Web of Science | Medline14
Human-to-human transmission of rabies via corneal transplant -- Thailand. MMWR Morb Mortal Wkly Rep 1981;30:473-474
Medline15
Houff SA ,Burton RC ,Wilson RW , et al. Human-to-human transmission of rabies virus by corneal transplant. N Engl J Med 1979;300:603-604
Full Text | Web of Science | Medline16
Gode GR ,Bhide NK . Two rabies deaths after corneal grafts from one donor. Lancet 1988;2:791-791
CrossRef | Web of Science | Medline17
Human-to-human transmission of rabies via a corneal transplant -- France. MMWR Morb Mortal Wkly Rep 1980;29:25-26
18
Recovery of a patient from clinical rabies, Wisconsin 2004. MMWR Morb Mortal Wkly Rep 2004;53:1171-1173
Medline19
Sureau P ,Portnoi D ,Rollin P ,Lapresle C ,Lapresle C ,Chaouni-Berbich A . Prevention of inter-human rabies transmission after corneal graft. C R Seances Acad Sci III 1981;293:689-692
Medline20
Iwamoto M ,Jernigan DB ,Guasch A , et al. Transmission of West Nile virus from an organ donor to four transplant recipients. N Engl J Med 2003;348:2196-2203
Full Text | Web of Science | Medline21
Organ Procurement and Transplantation Network. Minimum procurement standards for an organ procurement organization. (Accessed February 23, 2005, at http://www.optn.org/policiesandbylaws.)
22
Organ Procurement and Transplantation Network Policy Proposal. (Accessed February 23, 2005, at http://www.unos.org/policiesAndBylaws/publicComment/pdfs/pubcommentProp_15.pdf.)
23
Zamboni F ,Franchello A ,Ricchiuti A ,Fop F ,Rizzetto M ,Salizzoni M . Use of arterial conduits as an alternative technique in arterial revascularization during orthotopic liver transplantation. Dig Liver Dis 2002;34:122-126
CrossRef | Medline24
Muralidharan V ,Imber C ,Leelaudomlipi S , et al. Arterial conduits for hepatic artery revascularization in adult liver transplantation. Transpl Int 2004;17:163-168
CrossRef | Web of Science | Medline25
Goldstein RM ,Secrest CL ,Klintmalm GB ,Husberg BS . Problematic vascular reconstruction in liver transplantation. I. Arterial. Surgery 1990;107:540-543
Web of Science | Medline26
Muiesan P ,Rela M ,Nodari F , et al. Use of infrarenal conduits for arterial revascularization in orthotopic liver transplantation. Liver Transpl Surg 1998;4:232-235
CrossRef | Medline27
Sellers MT ,Haustein SV ,McGuire BM , et al. Use of preserved vascular homografts in liver transplantation: hepatic artery aneurysms and other complications. Am J Transplant 2002;2:471-475
CrossRef | Web of Science | Medline28
Pinna AD ,Smith CV ,Furukawa H ,Starzl TE ,Fung JJ . Urgent revascularization of liver allografts after early hepatic artery thrombosis. Transplantation 1996;15:1584-1587
CrossRef | Web of Science29
Shames BD ,Odorico JS ,D'Alessandro AM ,Pirsch JD ,Sollinger HW . Surgical repair of transplant renal artery stenosis with preserved cadaveric iliac artery grafts. Ann Surg 2003;237:116-122
CrossRef | Web of Science | Medline30
Joint Commission on Accreditation of Healthcare Organizations. Proposed Tissue Storage and Issuance Standards. (Accessed February 23, 2005, at http://www.jcaho.org/accredited+organizations/hospitals/standards/field+reviews/tissue_fr_stds.htm.)
- Citing Articles (100)
Citing Articles
1
D. W. McKeown, R. S. Bonser, J. A. Kellum. (2012) Management of the heartbeating brain-dead organ donor. British Journal of Anaesthesia 108:suppl 1, i96-i107
CrossRef2
Sebastian B. Lucas, Sherif R. Zaki, Bernard C. Portmann. 2012. Other viral and infectious diseases and HIV-related liver disease. , 403-466.
CrossRef3
Raymund R. Razonable. (2011) Rare, unusual, and less common virus infections after organ transplantation. Current Opinion in Organ Transplantation 16:6, 580-587
CrossRef4
Rob Aalsburg, Perry Genderen. (2011) Rabiës. Critical Care
CrossRef5
Rajat Dhar, Theresa Human. (2011) Central Nervous System Complications After Transplantation. Neurologic Clinics 29:4, 943-972
CrossRef6
Theresa R. Harring, Christine A. O’Mahony, John A. Goss. (2011) Extended Donors in Liver Transplantation. Clinics in Liver Disease
CrossRef7
Danielle Bury, Neil Langlois, Roger W. Byard. (2011) Animal-Related Fatalities-Part II: Characteristic Autopsy Findings and Variable Causes of Death Associated with Envenomation, Poisoning, Anaphylaxis, Asphyxiation, and Sepsis. Journal of Forensic Sciencesno-no
CrossRef8
R. Rodríguez-Romo, L.E. Morales-Buenrostro, L. Lecuona, N. Escalante-Santillán, A. Velasco-Villa, I. Kuzmin, C.E. Rupprecht, C. De-Leo, J. Ramírez, J. Alberú. (2011) Immune response after rabies vaccine in a kidney transplant recipient. Transplant Infectious Disease 13:5, 492-495
CrossRef9
P. Wohlsein, W. Baumgärtner, H.H. Kreipe, A. Haverich, A. Hori, A.C. Stan. (2011) Übertragung von Tollwut durch Organtransplantation. Der Pathologe 32:5, 406-410
CrossRef10
Chintamani Atreya, Hira Nakhasi, Paul Mied, Jay Epstein, James Hughes, Marta Gwinn, Steven Kleinman, Roger Dodd, Susan Stramer, Mark Walderhaug, Peter Ganz, Raymond Goodrich, Clark Tibbetts, David Asher. (2011) FDA workshop on emerging infectious diseases: evaluating emerging infectious diseases (EIDs) for transfusion safety. Transfusion 51:8, 1855-1871
CrossRef11
M. G. Ison, E. Llata, C. S. Conover, J. J. Friedewald, S. I. Gerber, A. Grigoryan, W. Heneine, J. M. Millis, D. M. Simon, C.-G. Teo, M. J. Kuehnert, . (2011) Transmission of Human Immunodeficiency Virus and Hepatitis C Virus From an Organ Donor to Four Transplant Recipients. American Journal of Transplantation 11:6, 1218-1225
CrossRef12
Gregory I. Snell, Glen P. Westall. (2011) Selection and Management of the Lung Donor. Clinics in Chest Medicine 32:2, 223-232
CrossRef13
M. G. Ison, M. A. Nalesnik. (2011) An Update on Donor-Derived Disease Transmission in Organ Transplantation. American Journal of Transplantation 11:6, 1123-1130
CrossRef14
Raymund R Razonable. (2011) Management of viral infections in solid organ transplant recipients. Expert Review of Anti-infective Therapy 9:6, 685-700
CrossRef15
(2011) Potential Transmission of Viral Hepatitis Through Use of Stored Blood Vessels as Conduits in Organ Transplantation-Pennsylvania, 2009. American Journal of Transplantation 11:4, 863-865
CrossRef16
Laurent Dacheux, Hervé Bourhy. (2011) Le diagnostic de la rage. Revue Francophone des Laboratoires 2011:430, 33-40
CrossRef17
Kameel Mungrue, Ron Mahabir. (2011) The Rabies Epidemic in Trinidad of 1923 to 1937: An Evaluation with a Geographic Information System. Wilderness & Environmental Medicine 22:1, 28-36
CrossRef18
J. Scott Weese, Martha B. Fulford. 2011. Viral Diseases. , 241-274.
CrossRef19
Henry Wilde, Boonlert Lumlertdacha. 2011. Rabies Research in Resource—Poor Countries. , 449-455.
CrossRef20
Susan A Nadin-Davis. 2010. Rabies: Virus and Disease. .
CrossRef21
Mary Warrell. (2010) Rabies and African bat lyssavirus encephalitis and its prevention. International Journal of Antimicrobial Agents 36, S47-S52
CrossRef22
Rebecca Pellett Madan, Betsy C Herold. (2010) Viral infections in pediatric solid organ transplantation recipients and the impact of molecular diagnostic testing. Current Opinion in Organ Transplantation 15:3, 293-300
CrossRef23
Michele I. Morris, Staci A. Fischer, Michael G. Ison. (2010) Infections Transmitted by Transplantation. Infectious Disease Clinics of North America 24:2, 497-514
CrossRef24
Supaporn Wacharapluesadee, Thiravat Hemachudha. (2010) Ante- and post-mortem diagnosis of rabies using nucleic acid-amplification tests. Expert Review of Molecular Diagnostics 10:2, 207-218
CrossRef25
P. D. Griffiths. (2010) Transmission of swine influenza through organ transplantation. Reviews in Medical Virology 20:2, 65-67
CrossRef26
Carlos Franco-Paredes, Jesse T. Jacob, Alicia Hidron, Alfonso J. Rodriguez-Morales, David Kuhar, Angela M. Caliendo. (2010) Transplantation and tropical infectious diseases. International Journal of Infectious Diseases 14:3, e189-e196
CrossRef27
Peter M. Rabinowitz, Lisa A. Conti. 2010. Zoonoses. , 105-298.
CrossRef28
J. A. Fishman, . (2009) Introduction: Infection in Solid Organ Transplant Recipients. American Journal of Transplantation 9, S3-S6
CrossRef29
S. A. Fischer, R. K. Avery, . (2009) Screening of Donor and Recipient Prior to Solid Organ Transplantation. American Journal of Transplantation 9, S7-S18
CrossRef30
Michael G. Ison, Valentina Stosor. (2009) Transplantation of high-risk donor organs: a survey of US solid organ transplant center practices as reported by transplant infectious diseases physicians. Clinical Transplantation 23:6, 866-873
CrossRef31
, Veroniek S. M. Saegeman, Akila Chandrasekar, Marja J. Wijk, Hilde Beele, Monica M. Montenero, Aurora Navarro, Caroline Geyt, Arlinke G. Bokhorst, Deirdre Fehily, Ruth M. Warwick. (2009) EATB Donor Case Workshop 2007. Cell and Tissue Banking 10:4, 351-357
CrossRef32
Gregory I Snell, Glen P Westall. (2009) Donor selection and management. Current Opinion in Organ Transplantation 14:5, 471-476
CrossRef33
Andrea Julia Nigg, Pamela L Walker. (2009) Overview, Prevention, and Treatment of Rabies. Pharmacotherapy 29:10, 1182-1195
CrossRef34
M. G. Ison, J. Hager, E. Blumberg, J. Burdick, K. Carney, J. Cutler, J. M. DiMaio, R. Hasz, M. J. Kuehnert, E. Ortiz-Rios, L. Teperman, M. Nalesnik. (2009) Donor-Derived Disease Transmission Events in the United States: Data Reviewed by the OPTN/UNOS Disease Transmission Advisory Committee. American Journal of Transplantation 9:8, 1929-1935
CrossRef35
Susan L. Stramer, F. Blaine Hollinger, Louis M. Katz, Steven Kleinman, Peyton S. Metzel, Kay R. Gregory, Roger Y. Dodd. (2009) Emerging infectious disease agents and their potential threat to transfusion safety. Transfusion 49, 1S-29S
CrossRef36
Charles D. Boucek, Paul Phrampus, John Lutz, Thomas Dongilli, Nicholas G. Bircher. (2009) Willingness to perform mouth-to-mouth ventilation by health care providers: A survey. Resuscitation 80:8, 849-853
CrossRef37
Jay A. Fishman, D. Michael Strong, Matthew J. Kuehnert. (2009) Organ and tissue safety workshop 2007: advances and challenges. Cell and Tissue Banking 10:3, 271-280
CrossRef38
Minoru Tobiume, Yuko Sato, Harutaka Katano, Noriko Nakajima, Keiko Tanaka, Akira Noguchi, Satoshi Inoue, Hideki Hasegawa, Yoko Iwasa, Junichi Tanaka, Hiroyuki Hayashi, Sachiko Yoshida, Ichiro Kurane, Tetsutaro Sata. (2009) Rabies virus dissemination in neural tissues of autopsy cases due to rabies imported into Japan from the Philippines: Immunohistochemistry. Pathology International 59:8, 555-566
CrossRef39
Michael G. Ison. (2009) The Epidemiology and Prevention of Donor-Derived Infections. Advances in Chronic Kidney Disease 16:4, 234-241
CrossRef40
Parisa Ravanfar, Anita Satyaprakash, Rosella Creed, Natalia Mendoza. (2009) Existing antiviral vaccines. Dermatologic Therapy 22:2, 110-128
CrossRef41
Jun-Sun Park, Myung-Guk Han. (2009) General Features and Post-Exposure Prophylaxis of Rabies. Infection and Chemotherapy 42:1, 6
CrossRef42
Peter K. Linden. (2009) History of Solid Organ Transplantation and Organ Donation. Critical Care Clinics 25:1, 165-184
CrossRef43
Shimon Kusne. (2008) Regarding unexpected severe and life-threatening donor-transmitted viral infections and use of high-risk behavior donors. Liver Transplantation 14:11, 1564-1568
CrossRef44
AM Geretti, . (2008) British HIV Association guidelines for immunization of HIV-infected adults 2008. HIV Medicine 9:10, 795-848
CrossRef45
Natasha Halasa, Michael Green. (2008) Immunizations and infectious diseases in pediatric liver transplantation. Liver Transplantation 14:10, 1389-1399
CrossRef46
Shungo Yamamoto, Chihiro Iwasaki, Hiroshi Oono, Kiyoshi Ninomiya, Tadashi Matsumura. (2008) The First Imported Case of Rabies Into Japan in 36 Years: A Forgotten Life-Threatening Disease. Journal of Travel Medicine 15:5, 372-374
CrossRef47
E. Schmutzhard, B. Pfausler. (2008) Infektionen des ZNS beim immuninkompetenten Patienten. Der Nervenarzt 79:S2, 93-111
CrossRef48
Allan R. Tunkel, Carol A. Glaser, Karen C. Bloch, James J. Sejvar, Christina M. Marra, Karen L. Roos, Barry J. Hartman, Sheldon L. Kaplan, W. Michael Scheld, Richard J. Whitley. (2008) The Management of Encephalitis: Clinical Practice Guidelines by the Infectious Diseases Society of America. Clinical Infectious Diseases 47:3, 303-327
CrossRef49
Edwina J. Wright, Bruce J. Brew, Steve L. Wesselingh. (2008) Pathogenesis and Diagnosis of Viral Infections of the Nervous System. Neurologic Clinics 26:3, 617-633
CrossRef50
Alan C. Jackson. (2008) Rabies. Neurologic Clinics 26:3, 717-726
CrossRef51
Jesse D Blanton, Charles E Rupprecht. (2008) Travel vaccination for rabies. Expert Review of Vaccines 7:5, 613-620
CrossRef52
Mary J Warrell. (2008) Emerging aspects of rabies infection: with a special emphasis on children. Current Opinion in Infectious Diseases 21:3, 251-257
CrossRef53
F. Mattner, A. Kola, S. Fischer, T. Becker, A. Haverich, A. Simon, S. Suerbaum, P. Gastmeier, H. Weißbrodt, M. Strüber. (2008) Impact of Bacterial and Fungal Donor Organ Contamination in Lung, Heart–Lung, Heart and Liver Transplantation. Infection 36:3, 207-212
CrossRef54
Gaston De Serres, Frédéric Dallaire, Mathieu Côte, Danuta M. Skowronski. (2008) Bat Rabies in the United States and Canada from 1950 through 2007: Human Cases With and Without Bat Contact. Clinical Infectious Diseases 46:9, 1329-1337
CrossRef55
Cabot, Richard C.Harris, Nancy Lee, Shepard, Jo-Anne O., Rosenberg, Eric S., Cort, Alice M., Ebeling, Sally H.Peters, Christine C., Fishman, Jay A., Gonzalez, R. Gilberto, Branda, John A., . (2008) Case 11-2008. New England Journal of Medicine 358:15, 1604-1613
Full Text56
Naohide Takayama. (2008) Rabies: a preventable but incurable disease. Journal of Infection and Chemotherapy 14:1, 8-14
CrossRef57
Fishman, Jay A., . (2007) Infection in Solid-Organ Transplant Recipients. New England Journal of Medicine 357:25, 2601-2614
Full Text58
J. A. Fishman, M. A. Greenwald, M. J. Kuehnert. (2007) Enhancing Transplant Safety: A New Era in the Microbiologic Evaluation of Organ Donors?. American Journal of Transplantation 7:12, 2652-2654
CrossRef59
Jane D. Siegel, Emily Rhinehart, Marguerite Jackson, Linda Chiarello. (2007) 2007 Guideline for Isolation Precautions: Preventing Transmission of Infectious Agents in Health Care Settings. American Journal of Infection Control 35:10, S65-S164
CrossRef60
Anne M Anglim. (2007) Exotic donor-transmitted infections in solid-organ transplantation: can seemingly random events inform policy?. Current Opinion in Organ Transplantation 12:6, 591-603
CrossRef61
Toru Ikegami, Yuji Soejima, Akinobu Taketomi, Tomoharu Yoshizumi, Noboru Harada, Hideaki Uchiyama, Mitsuo Shimada, Yoshihiko Maehara. (2007) Explanted Portal Vein Grafts for Middle Hepatic Vein Tributaries in Living-Donor Liver Transplantation. Transplantation 84:7, 836-841
CrossRef62
F. Mattner, F. Bitz, M. Goedecke, A. Viertel, S. Kuhn, P. Gastmeier, L. Mattner, F. Biertz, A. Heim, C. Henke-Gendo, I. Engelmann, A. Martens, M. Strüber, T. F. Schulz. (2007) Adverse Effects of Rabies Pre- and Postexposure Prophylaxis in 290 Health-Care-Workers Exposed to a Rabies Infected Organ Donor or Transplant Recipients. Infection 35:4, 219-224
CrossRef63
Eun Jeong Kwak, Robin K Avery. (2007) Strategies for the prevention of infectious complications after renal transplantation. Current Opinion in Organ Transplantation 12:4, 362-370
CrossRef64
Su Wang, Craig Zinderman, Robert Wise, Miles Braun. (2007) Infections and human tissue transplants: review of FDA MedWatch reports 2001–2004. Cell and Tissue Banking 8:3, 211-219
CrossRef65
Hugo Bonatti, Robert Sawyer, Rolland C Dickson, Raymond Razonable, Timothy Schmitt, Julio Mendez, Nina Singh, Timothy Pruett. (2007) Transmission of viral disease to the recipient through the donor liver. Current Opinion in Organ Transplantation 12:3, 231-241
CrossRef66
Jan Bronnert, Henry Wilde, Veera Tepsumethanon, Boonlert Lumlertdacha, Thiravat Hemachudha. (2007) Organ Transplantations and Rabies Transmission. Journal of Travel Medicine 14:3, 177-180
CrossRef67
PD Griffiths. (2007) Transmission of viruses with human allografts. Reviews in Medical Virology 17:3, 147-149
CrossRef68
Frauke Mattner, Cornelia Henke‐Gendo, Andreas Martens, Christian Drosten, Thomas F. Schulz, Albert Heim, Sebastian Suerbaum, Sabine Kuhn, Juliane Bruderek, Petra Gastmeier, Martin Strueber. (2007) Risk of Rabies Infection and Adverse Effects of Postexposure Prophylaxis in Healthcare Workers and Other Patient Contacts Exposed to a Rabies Virus–Infected Lung Transplant Recipient • . Infection Control and Hospital Epidemiology 28:5, 513-518
CrossRef69
Saša Živković. (2007) Neuroimaging and Neurologic Complications after Organ Transplantation. Journal of Neuroimaging 17:2, 110-123
CrossRef70
Kenneth D. McMilin, Susmita Dasgupta. (2007) Allogeneic Transplantation and the Risk for Transmission of Genetic Disease: The Heritable Cancer Disorders. Stem Cells and Development 16:2, 191-212
CrossRef71
C. N. Kotton. (2007) Zoonoses in Solid-Organ and Hematopoietic Stem Cell Transplant Recipients. Clinical Infectious Diseases 44:6, 857-866
CrossRef72
P.R.A. Meylan, J.-D. Aubert, L. Kaiser. (2007) Influenza transmission to recipient through lung transplantation. Transplant Infectious Disease 9:1, 55-57
CrossRef73
Samson Wong, Susanna Lau, Patrick Woo, Kwok-Yung Yuen. (2007) Bats as a continuing source of emerging infections in humans. Reviews in Medical Virology 17:2, 67-91
CrossRef74
Matthew J. Kuehnert, Krista L. Yorita, Robert C. Holman, D. Michael Strong, . (2007) Human tissue oversight in hospitals: an AABB survey. Transfusion 47:2, 194-200
CrossRef75
K. Muhamuda, S.N. Madhusudana, V. Ravi, A. Desai. (2006) Presence of rabies specific immune complexes in cerebro-spinal fluid can help in ante-mortem diagnosis of human paralytic rabies. Journal of Clinical Virology 37:3, 162-167
CrossRef76
Thiravat Hemachudha, Supaporn Wacharapluesadee, Jiraporn Laothamatas, Henry Wilde. (2006) Rabies. Current Neurology and Neuroscience Reports 6:6, 460-468
CrossRef77
Jodi M. Smith, Ruth A. McDonald. (2006) Emerging viral infections in transplantation. Pediatric Transplantation 10:7, 838-843
CrossRef78
Glyn N. Stacey, Fernando Cobo, Ana Nieto, Paloma Talavera, Lyn Healy, Ángel Concha. (2006) The development of ‘feeder’ cells for the preparation of clinical grade hES cell lines: Challenges and solutions. Journal of Biotechnology 125:4, 583-588
CrossRef79
F.M. Marty, R.H. Rubin. (2006) The persistent challenges of bacterial infections in the transplant recipient. Transplant Infectious Disease 8:3, 125-127
CrossRef80
S.L. Harris, S.M. Brookes, G. Jones, A.M. Hutson, P.A. Racey, J. Aegerter, G.C. Smith, L.M. McElhinney, A.R. Fooks. (2006) European bat lyssaviruses: Distribution, prevalence and implications for conservation. Biological Conservation 131:2, 193-210
CrossRef81
Juliana H. Chávez, Paulo C. Leal, Rosendo A. Yunes, Ricardo J. Nunes, Célia R.M. Barardi, Aguinaldo R. Pinto, Cláudia M.O. Simões, Carlos R. Zanetti. (2006) Evaluation of antiviral activity of phenolic compounds and derivatives against rabies virus. Veterinary Microbiology 116:1-3, 53-59
CrossRef82
James J Sejvar. (2006) The evolving epidemiology of viral encephalitis. Current Opinion in Neurology 19:4, 350-357
CrossRef83
Myrna R. Rosenfeld, Amy Pruitt. (2006) Neurologic Complications of Bone Marrow, Stem Cell, and Organ Transplantation in Patients With Cancer. Seminars in Oncology 33:3, 352-361
CrossRef84
Alan C. Jackson. (2006) Bat Rabies Virus Variants Causing Human Rabies. The Pediatric Infectious Disease Journal 25:6, 570
CrossRef85
Alan C Jackson. (2006) Rabies: new insights into pathogenesis and treatment. Current Opinion in Neurology 19:3, 267-270
CrossRef86
Thomas R. Howdieshell, Daithi Heffernan, Joseph T. Dipiro. (2006) Surgical Infection Society Guidelines for Vaccination after Traumatic Injury. Surgical Infections 7:3, 275-303
CrossRef87
Jennifer N. Post. (2006) Immunizations, neonatal jaundice and animal-induced injuries. Current Opinion in Pediatrics 18:3, 330-335
CrossRef88
Fischer, Staci A., Graham, Mary Beth, Kuehnert, Matthew J., Kotton, Camille N., Srinivasan, Arjun, Marty, Francisco M., Comer, James A., Guarner, Jeannette, Paddock, Christopher D., DeMeo, Dawn L., Shieh, Wun-Ju, Erickson, Bobbie R., Bandy, Utpala, DeMaria, Alfred Jr., Davis, Jeffrey P., Delmonico, Francis L., Pavlin, Boris, Likos, Anna, Vincent, Martin J., Sealy, Tara K., Goldsmith, Cynthia S., Jernigan, Daniel B., Rollin, Pierre E., Packard, Michelle M., Patel, Mitesh, Rowland, Courtney, Helfand, Rita F., Nichol, Stuart T., Fishman, Jay A., Ksiazek, Thomas, Zaki, Sherif R., the LCMV in Transplant Recipients Investigation Team. (2006) Transmission of Lymphocytic Choriomeningitis Virus by Organ Transplantation. New England Journal of Medicine 354:21, 2235-2249
Full Text89
Autumn Fiester. (2006) Casuistry and the moral continuum. Politics and the Life Sciences 25:1 & 2, 15-22
CrossRef90
Marek J. Nowicki, Claudia Chinchilla, Livier Corado, Lea Matsuoka, Rick Selby, Frank Steurer, Thomas Mone, Robert Mendez, Sali Aswad. (2006) Prevalence of Antibodies to Trypanosoma cruzi among Solid Organ Donors in Southern California: A Population at Risk. Transplantation 81:3, 477-479
CrossRef91
Surakit Pungpapong, Murli Krishna, Susan C. Abraham, Andrew P. Keaveny, Rolland C. Dickson, Raouf E. Nakhleh. (2006) Clinicopathologic findings and outcomes of liver transplantation using grafts from donors with unrecognized and unusual diseases. Liver Transplantation 12:2, 310-315
CrossRef92
J.A. Stockman. (2006) Transmission of Rabies Virus From an Organ Donor to Four Transplant Recipients. Yearbook of Pediatrics 2006, 280-282
CrossRef93
Francisco M. Marty, Robert H. Rubin. (2006) The prevention of infection post-transplant: the role of prophylaxis, preemptive and empiric therapy. Transplant International 19:1, 2-11
CrossRef94
F Cobo, C Cabrera, P Catalina, Á Concha. (2006) General safety guidances in stem cell bank installations. Cytotherapy 8:1, 47-56
CrossRef95
Marissa Wilck, Jay A Fishman. (2005) The challenges of infection in transplantation: donor-derived infections. Current Opinion in Organ Transplantation 10:4, 301-306
CrossRef96
John W. Krebs, Eric J. Mandel, David L. Swerdlow, Charles E. Rupprecht. (2005) Rabies surveillance in the United States during 2004. Journal of the American Veterinary Medical Association 227:12, 1912-1925
CrossRef97
(2005) Candid observations on the current status of xenotransplantation. Xenotransplantation 12:6, 428-431
CrossRef98
Shimon Kusne, Jerry Smilack. (2005) Transmission of rabies virus from an organ donor to four transplant recipients. Liver Transplantation 11:10, 1295-1297
CrossRef99
Georg Pauli. (2005) Tissue Safety in View of CJD and Variant CJD. Cell and Tissue Banking 6:3, 191-200
CrossRef100
(2005) Transmission of Rabies from an Organ Donor. New England Journal of Medicine 352:24, 2551-2552
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