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Iatrogenic Creutzfeldt-Jakob disease and its neurosurgical implications
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latrogenic Creutzfeldt-Jakob disease and its neurosurgical implications
D. C. G. G. G.
A . S i m p s o n 1 MS FRACS L. M a s t e r s 2 MD O h l r i c h 3 MD QId FRACP FRCP P u r d i e 4 FRACP S t u a r t s FRACS A. E. G. Tannenberg 6 FRCPA XDepartment of Neurosurgery, Women's and Children's Hospital, Adelalde,~Department of Pathology, University of Melbourne, 4Department of Neurology, The Queen Elizabeth Hospital, Woodville, Departments of 3Neurology and 5Neurosurgery, Royal Brisbane Hospital, Brisbane, 6Department of Pathology, Mater Misericordiae Public Hospitals, South Brisbane, Australia.
Creutzfeldt-Jakob (CJD) disease has been reported after the insertion of dural homografts. Two Australian cases of CJD, both following posterior fossa craniotomies done in 1982, are reported; the incubation periods were 5 and 12 years. It seems highly probable that the association is causal. CJD infective agents (prions) are resistant to many previously accepted means of sterih'sation and it is postulated that cadaver dural material was either derived from subjects with CJD, or was contaminated during preparation. In Australia the use of dural homografts in neurosurgery was abandoned in 1987; as the mean incubation period (determined from a world-wide review) has been about 65 months, it is now hoped that this cause of CJD will not recur in the Australian population, although it is premature to state this with confidence. However, precautions against case-to-case transmission remain necessary, and guidelines for this purpose should be enforced in theatre practice and in organ donations. Journal of Clinical Neuroscience 1996, 3(2): 118-123
Keywords:
© Pearson Professional 1996
Creutzfeldt-Jakob disease, Cadaveric dural hornografts, Prion
Introduction Creutzfeldt-Jakob disease (CJD) is a transmissible spongiform encephalopathy, one of a group of h u m a n and animal diseases in which the infecting agents, t e r m e d prions, have properties that distinguish them from other forms o f microbial life. In particular, prions have b e e n shown to be resistant to many procedures intended to secure sterilisation. CJD is usually seen as a sporadic disease affecting the elderly; it is sometimes familial, when there is invariably evidence of a genetic mutation in the PRNP gene coding for the prion protein (PrP). Unhappily, CJD may also be iatrogenic. 1 Case-to-case transmission of CJD by a corneal graft was r e p o r t e d in 1974. 2 In 1977 Bernoulli et al3 r e p o r t e d two cases o f CJD in which the infecting agent was evidently transmitted by implanted depth electrodes. In 1985 reports appeared of transmission by injections of h u m a n pituitary growth h o r m o n e derived from cadavers. In 1987 Penar and Prichard 4 r e p o r t e d a case of CJD occurring 19 months after the use of Lyodura®, a proprietary dural homograft; similar reports have followed. We r e p o r t two additional cases, one o f which has
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already b e e n briefly reported; 5 they are believed to be the first r e c o r d e d in Australia. We also consider the implications of these cases in neurosurgical practice.
Case reports
Case 1 A 56-year-old meat worker presented in 1982 with a complaint o f increasing deafness over a 2 year period. Computerised tomography (CT) showed an enhancing mass in the right cerebellopontine angle, which was consistent with an acoustic neurinoma. Subsequently this t u m o u r and its capsule were resected; during operation the seventh nerve was divided. At the e n d of the operation the dura was closed with the aid of a Lyodura® graft. T h e resected t u m o u r was confirmed as a schwannoma. One m o n t h later a hypoglossal-facial nerve anastomosis was p e r f o r m e d . Five years (58 months) after the initial surgery the patient presented with a 2 week history o f dizzy spells,
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deteriorating memory, blurred vision with transient diplopia and disorientation. He had been normal on review 5 months previously. On examination, there was severe impairment of memory, nystagmus and gait ataxia. CT scan and examination of the cerebrospinal fluid (CSF) were normal. His mental state deteriorated, and over the course of some weeks he became mute and eventually unable to obey commands. There was marked generalised extrapyramidal rigidity and bilateral pyramidal tract signs. Myoclonic jerks were also noted. A clinical diagnosis of CJD was made and electroencephalography (EEG) strongly supported this diagnosis with periodic complexes on a background of diffuse slow activity. He continued to deteriorate and eventually died in a vegetative state 7 weeks after the o n s e t of neurological deterioration and 5 years after the initial m m o u r removal and insertion of Lyodura® graft. An autopsy was performed. T h e immediate cause of death was acute b r o n c h o p n e u m o n i a and acute pulm o n a r y thromboembolism. The brain weighed 1420 g and appeared normal macroscopically. Histological examination confirmed the diagnosis of CJD with widespread spongiform change in cerebral and cerebellar cortex with variable mild to moderate neuronal loss and mild gliosis. The topographical distribution of these changes is d o c u m e n t e d in Table 1. There was no accenmarion of the changes in the brainstem. An unusual feature was the presence of numerous neuritic and diffuse plaques throughout the cerebral cortex. These were uniformly ~ A 4 amyloid positive on immunostaining and were accompanied by an amyloid angiopathy. No neurofibrillary tangles were identified. This case was reported in 1989. 5 Case
2
A 14-year-old boy presented in 1982 with diplopia and marked papilloedema. CT showed a large posterior fossa mmour, partly cystic, which proved to be a benign astrocytoma. It was removed completely, together with its lining. There was tonsillar herniation, and to allow full decompression, an insert of Lyodura® was used to close
the dural defect. Recovery was smooth and there were no residual disabilities. Twelve years later the patient became unsteady on his feet and noticed clumsiness in the upper limbs. He also noted blurred vision and occasional double vision. When seen 4.5 months after the onset of these symptoms he also complained of urinary frequency and slurred speech. Direct questioning elicited complaints of hyperphagia and emotional lability. There was no relevant family history. On examination there was marked gait ataxia, speech was dysarthric, and m o o d suggested frontal lobe impairment, with lack of insight and emotional lability. Eye movements were full without nystagmus, but horizontal saccadic movements were jerky. Power in the limbs was preserved, but there was mild incoordination in the upper limbs and significant ataxia in the legs. EEG showed non-specific slowing of cerebral rhythms. CT and magnetic resonance imaging (MRI) showed no evidence of mmour recurrence. Cerebrospinal fluid (CSF) analysis at this stage showed no specific abnormalities. The ataxia steadily worsened, and a generalised body tremor became evident. A second EEG done 6 m o n t h s after onset of symptoms again showed some slowing of cerebral rhythms, but no periodic complexes. Speech and swallowing worsened, and there was terminal anarthria, dysphagia and declining intellectual function. Myoclonic jerks were recorded during the last fortnight before death, which took place nearly 13 years after tumour removal and 9 months after the onset of symptoms. Autopsy was not performed. Blood examination, courtesy of Dr Paul Brown (Laboratory of Central Nervous System Disorders, National Institute of Neurological Disorders and Stroke, Bethesda, MD USA), showed the PRNP codon 129 genotype to be homozygous for methionine. CSF analysis showed the presence of 130/131 protein spot on 2D gel analysis, and this was considered to confirm the clinical diagnosis of iatrogenic Creutzfeldt-Jakob disease.
Discussion
The unique biology of prion infections presents neurosurgical problems which can be discussed in several contexts. Table 1 Histopathological findings in case 1 Site
Spongiform change
Gliosis
Neuronal loss
Frontal c o r t e x Insular c o r t e x Temporal c o r t e x Parietal cortex Calcarine cortex Hippocampus Entorhinal c o r t e x Putamen C a u d a t e nucleus Thalamus M a m i l l a r y bodies O l f a c t o r y nerve Midbrain Cerebellum Medulla
+ ++ ++ + ++ ++ + + ± colliculi + -
+ + + + ++ + ± + -
+ + ++ + ++ + ± + + -
-
J.
Duraplasty
with
homografts
In 1958 Campbell et al 6 described experiences with freeze-dried h u m a n dura mater, the material being obtained from the US Navy tissue bank. In the same issue of the Journal ofNeurosurgery,Sharkey et al7 also reported on the use of lyophilised cadaver dura, and mentioned its use in hernial repairs. The dura was sterilised by ethylene oxide, and was commercially available. Further favourable reports followed. Koos8 reported on 75 paediatric cases, treated with lyophilised dura in Vienna. In these cases the homografts were apparently prepared by the German firm B Braun Melsungen AG under the proprietary name Lyodura®; sterilisation was by gamma irradiation. Another German firm, Lyofil-PfrimmerGmbH of Erlangen,
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Clinical studies also marketed cadaver dura mater u n d e r the name o f Tutoplast®; this was dehydrated with organic solvents and sterilised by gamma irradiation. In 1971, Abbott and Dupree 9 reported on 170 patients, using dura from the US Navy tissue bank. Sterilisation was effected by liquid ethylene, liquid betapropiolactone, or radiation. The use of cadaver dura mater became widespread, and in 1972 Lyodura® received product recognition in Australia. By 1987 Braun had sold more than 'one half million packages of Lyodura throughout the world'. TMIn that year Cantore et al aI reported on the use of h u m a n dura mater prepared in the La Sapienza Department of Neurosciences, Rome. The dura was sterilised by gamma rays and stored in alcohol; the long term results in 804 cases treated between 1967 and 1984 were considered to be very satisfactory. In 1978 Gibbs et all2 directed attention to the difficulties in destroying the infective particles now known as prions by ionising irradiation. In 1985, reports were published of CJD evidently due to the use of h u m a n pituitary growth h o r m o n e s obtained from autopsies. In May 1985 such h o r m o n e s were withdrawn from use in the UK, USA, Australia and many other countries. This raised the possibility that lyophilised h u m a n dura mater might also transmit CJD. Enquiries were made at that time to Braun, Melsungen, who confirmed awareness of the inefficacy of gamma irradiation alone, but believed that the additional treatment o f cadaver dura for 24 h by 10% sodium peroxide 'had the property of destroying the disulphide bridges' in the prions, so destroying their infective capacity (J. Krause & G. Meil, personal communication, 1985). However, some 16 months later, Penar and Prichard 4 reported the case of a 28-year-old woman who developed encephalopathic symptoms 19 months after the use o f Lyodura® in a cranial operation for cholesteatoma. Biopsy showed changes considered to justify the diagnosis of CJD. The US Food and Drug Administration (FDA) issued a warning against the possibility of such transmission by listed batches of Lyodura®. The case had been notified to one of us (DAS) early in February 1987, by the courtesy ofDrs C.J. Gibbs and D.C. Gajdusek of NINDS, who were aware of earlier concern about this possibility in Australia. A general warning was issued to Australian and New Zealand neurosurgeons through the Neurosurgical Society of Australasia. The Commonwealth Department of Health was also notified, and import permits for hitherto recognised proprietary dural homografts were withdrawn. It was realised that cases receiving dural homografts before this date might be at risk, but it was h o p e d that the rarity of CJD in the general community would make transmission a rare event. Unhappily, this proved not to be the case. In 1989, a second case was reported from Dunedin, New Zealand; 1~ other reports have followed, and to date (May 1995) some 25 cases are on record worldwide, 14-2I not all published (R.G. Will, personal communication). In the great majority, the dural homografts were identified as Lyodura®, although a non-commercial source was identified in one Italian case. 17 Can cadaver dural homografts now be used u n d e r any circumstances? In 1990 the US Neurological Diseases
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Creutzfeldt-Jakob disease Panel o f the FDA concluded that h u m a n cadaveric dural homografts might be used if provided by a tissue bank using acceptable d o n o r screening procedures. 22A recent publication by the American Association of Neurological Surgeons mentions the use o f lyophilised dural homografts as an acceptable procedure. 2s Australian neurosurgeons have felt reluctant to return to this admittedly very convenient means of dural repair, and in the USA misgivings have recently been expressed. 24
Case-to-case transmission Mention has been made o f the cases r e c o r d e d by Bernoulli et al, 3 in which transmission was clearly effected by electrodes which had b e e n contaminated by use in a case of CJD despite supposed sterilisation with 70% alcohol and formaldehyde vapour. Transmission from the electrodes to a chimpanzee was later demonstrated35 It is likely that this is not the only r e c o r d e d example of case-to-case transmission in neurosurgical operations. In 1960 Nevin et a126 r e p o r t e d on eight cases of CJD, three of which had u n d e r g o n e neurosurgical operations of different types in two hospitals. In 1979 Masters et a127 drew attention to this association and suggested the possibility of case-to-case transmission. Will and Matthews 28 later reviewed theatre operation lists from these hospitals and confirmed that there was a temporal proximity between the use of the theatres for diagnostic procedures o n cases o f proven CJD and the operative procedures later followed by CJD in 3 patients originally suffering from a meningioma, a brain abscess and an obsessional neurosis. Foncin et al29 also briefly r e p o r t e d possible operative case-to-case transmission, and other probable cases have been identified27 This strong circumstantial evidence underlines the n e e d for great caution when a case o f CJD must u n d e r g o any surgical procedure, and similar caution may be justified in cases with a history o f a CJD risk factor (see below).
Issues related t o clinical and radiological diagnosis Awareness of CJD is facilitated by a history o f a risk factor such as the administration of h u m a n pituitary h o r m o n e s before 1985, or a homograft duraplasty done before 1987. It may be possible to narrow the risk periods more precisely; it seems likely that, with one exception, TM all cases of CJD attributed to duraplasty u n d e r w e n t operation in the period 1981-1986. It also appears that in the great majority of cases Lyodura® was employed, and it may be possible to exonerate duraplasties p e r f o r m e d with other commercial homografts, though no d o u b t some reservations should be made in such exonerations. However, a sporadic case of CJD could present after an unrelated neurosurgical procedure, while iatrogenic cases could for some reason present without a history o f a risk factor. T h e clinical symptomatology of sporadic CJD is well known. Iatrogenic CJD is typically seen in m u c h younger patients, although this of course depends on the age at exposure to the source of prion infection. T h e incubation period is long, especially for CJD complicating the
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use o f h u m a n pituitary h o r m o n e s where Brown et al] give a range of 4-30 years. Shorter incubation periods have been r e c o r d e d after dural implantation, the range being 16 months - 12 years (case 2 in this report) and the mean approximately 65 months. Iatrogenic CJD also tends to have a somewhat different clinical picture. Presentation with cerebellar ataxia is common, dementia less usual in the early stages, and myoclonic jerks are seen as a rule only in the late stages. The characteristic EEG abnormalides are typically seen late or never. In all these features, our case 2 is characteristic of the cerebellar type of iatrogenic CJD. However, there are cases o f CJD after supratentorial duraplasty which take a different course, with features suggesting early local spread to cerebral cortex. Thus, the second case r e p o r t e d by Esmonde et all8 presented with micropsia, metamorphopsia, and dyslexicdysgraphic symptoms, followed by dysphasia; since the duraplasty was originally p e r f o r m e d to replace a leftsided petrous meningioma it is tempting to suppose that the portal o f prion entry may d e t e r m i n e the nature of the first clinical symptoms. T h e same association appears evident in the case r e c o r d e d by Masullo et al, 14 since in this case a right temporal duraplasty was later followed by a left temporal h e m i a n o p i a and hemiparesis. However, ataxia was an early symptom in one case o f supratentorial duraplasty, 2] and conversely, our case 1 showed early dementia after an infratentorial duraplasty. To establish the diagnosis, it will be necessary to exclude r e c u r r e n c e of the disease for which operation was first p e r f o r m e d . This done, the clinical findings and their relentless course may be sufficient. Confirmation by CSF analysis was of great value in our case 2, but the identification o f the 130/131 protein spot by 2D gel electrophoresis requires specialised expertise, and is not yet widely available. Cerebral biopsy is now r e c o m m e n d e d only when a treatable condition has to be excluded. Autopsy is always desirable.
Theatre precautions In 1994 the Australian National Health & Medical Research Council (NH&MRC) set up a Working Party u n d e r the chairmanship of one of us (CLM) to prepare guidelines on patient m a n a g e m e n t and infection controlP ° This Working Party considered the circumstances in which CJD might be transmitted, and identified two groups o f patients with different risk levels:
Group 1: high risk patients This group includes: 1) patients with proven or suspected CJD; 2) asymptomatic carriers o f pathogenic mutations associated with a familial history of CJD or the allied condition Gerstmann-Str/iussler-Scheinker syndrome (GSS) ; and 3) all members o f a family with CJD/GSS in whom the PrP genotype is u n d e t e r m i n e d or unknown.
Group 2: low risk patients This group includes: 1) any patient with undiaguosed progressive neurological illness with or without dementia; 2)
all members of a family in which there is a strong family history o f undiagnosed d e m e n t i a / n e u r o l o g i c a l illnesses; 3) recipients o f h u m a n pituitary growth h o r m o n e s and gonadotrophins; and 4) recipients of dura mater grafts or persons with a record o f intracranial neurosurgical operations in Australia prior to 1987. We suggest that transdural spinal procedures should be considered to be at risk, since Lyodura® has been used for spinal duraplasty. We also suggest that the risk period in Australia should be from 1972, when permission was given to i m p o r t L y o d u r a ® , to 1989, since some neurosurgeons may not have accepted the evidence of a single case r e p o r t as a contraindication. For patients who u n d e r w e n t operations overseas, n o risk period can be set and the n e u r o s u r g e o n responsible should be contacted. It will be evident that the s e c o n d group is broadly inclusive, and the considerations set out above suggest that it should be possible to narrow the last category o f persons seen to be at risk on neurosurgical grounds. However, this r e p o r t provides a good basis for infection control. It is important to note that the Working Party concluded that normal autoclaving (121°C at 101 kPa), ultraviolet or gamma irradiation, glutaraldehyde, boiling, dry heat, ethylene oxide, acetone, and alcohols are not effective in sterilising material or instruments contaminated by prions. To eliminate prion contamination of surgical instruments the r e p o r t r e c o m m e n d e d gravity or porous load autoclaving to 134°C at 203 kPa. Where chemical sterilisation is needed, immersion for at least 1 h o u r in 1-2 molar sodium hydroxide was r e c o m m e n d e d . However, Taylor et aP 1f o u n d that this p r o c e d u r e did not completely inactivate tissue from bovine spongiform encephalopathy, although sodium hypochlorite was f o u n d to do so. These authors r e c o m m e n d e d exposure for 1 h o u r to a solution of sodium hypochlorite yielding 20,000 p p m o f available chlorine. Present knowledge suggests that n o m e t h o d o f chemical sterilisation will guarantee safety against contamination. Disposable instruments should be used as m u c h as possible, and in high-risk cases, all instruments should be destroyed. This last r e c o m m e n d a t i o n reflects UK guidelines, and has been criticised; s2 nevertheless, it is in accordance with general concepts of the extreme difficulty in eliminating prion contamination. Precautions against case-to-case transmission are also relevant in designing protocols to safeguard staff in the theatre, in the ward, and in the laboratory. Berger and David ~ list reports of CJD in a neurosurgeon, a pathologist, and two histopathology technicians; the case of the n e u r o s u r g e o n has been r e p o r t e d in detail by Schoene et alp4 Weber et al35 have added the case of an orthopaedic surgeon who contracted CJD 20 years after a prolonged period of work involving handling dura mater and sending it to a commercial organisation that sold dura mater preparations later held responsible for CJD transmission. In these cases the evidence for occupational infection is only circumstantial; however, the cases provide additional emphasis to the recommendations on safety precautions.
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Notification of risk from dural homografts Should all recipients o f Lyodura® a n d o t h e r dural h o m o grafts be notified that they are at risk o f this lethal disease, as was d o n e to the recipients of h u m a n pituitary h o r m o n e s ? In the UK, the D e p a r t m e n t of Health in 1993 decided n o t to a t t e m p t to do this, on the grounds that the risks were remote, that individuals would n o t know whether or not they were at risk, a n d that records would often be incomplete or destroyed? 6 A further consideration is the possibility that hospital records m i g h t be misleading, in that operation notes m i g h t state or imply that Lyodura® was used, when in reality some o t h e r preparation of lyophilised d u r a m a t e r was employed. These a r g u m e n t s may be valid; however, it is desirable for n e u r o s u r g e o n s who have used dural homografts to review their records to identify patients who are at risk if this is possible. Blood banks and tissue banks may well reject as donors any person t h o u g h t to be at risk, and a person so rejected will obviously be entitled to a full explanation a n d a p p r o p r i a t e counselling. Received26 September 1995 Accepted for publication 6 October 1995
Correspondence and offprint requests: D. A. Simpson MS FRACS Department of Neurosurgery Women's and Children's Hospital Adelaide Australia 5006 Phone: 61 8 204 7230 Fax: 61 8 204 6575
References 1. Brown P, Preece MA, Will RG. 'Friendly fire' in medicine: hormones, homografts, and Creutzfeldt-Jakob disease. Lancet 1992; 340: 24-27. 2. Duffy P, WolfJ, Collins G, DeVoe AG, Streeten B, Cowen D. Possible person-to-person transmission of CreutzfeldJakob disease (letter). N EnglJ Med 1974; 290: 692-693. 3. Bernoulli C, Siegfried J, Baumgartner G e t al. Danger of accidental person-to-person transmission of CreutzfeldtJakob disease by surgery (letter). Lancet 1977; 1: 478-479. 4. Penar PL, PrichardJW. Jakob-Creutzfeldt disease associated with cadaveric dura (letter). J Neurosurg 1987; 67: 149. 5. Anon. A case of Creutzfeldt-Jakob disease associated with a human dura mater graft. Communicable Disease Intelligence 1989; 89: 7-8. 6. CampbellJB, Bassett CAL, RobertsonJW. Clinical use of freeze-dried human dura mater. J Neurosurg 1958; 15: 207-214. 7. Sharkey PC, Usher FC, Robertson RCL, Pollard C. Lyophilized human dura mater as a dural substitute. J Neurosurg 1958; 15: 193-206. 8. Koos W. Erfahrungen mit der Transplantation homologer, lyophilisierter Dura in der Kinderneurochirurgie. Melsunger Medizinische Mitteilungen 1969; 43: 39-47. 9. Abbott WM, Dupree EL. Clinical results of lyophilized human cadaver dura transplantation. J Neurosurg 1971; 34: 770-773. 10. Otto D. Jakob-Creutzfeldt disease associated with cadaveric dura (Response).J Neurosurg 1987 67: 149.
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Creutzfeldt-Jakob disease 11. Cantore G, Guidetti B, Delfini R. Neurosurgical use of human dura mater sterilized by gamma rays and stored in alcohol; long term results.J Neurosurg 66: 93-95, 1987. 12. Gibbs CJ, Gajdusek DC, Latarjet R. Unusual resistance to ionizing radiation of the viruses of kuru, CreutzfeldtJakob disease, and scrapie. Proc Natl Acad Sci, USA 1978; 75: 6268-6270. 13. Nisbet TJ, MacDonaldson I, Bishara SN. Creutzfeldt-Jakob disease in a second patient who received a cadaver dura mater graft. JAMA 1989; 261: 1118. 14. Masullo C, Pocchiari M, Macchi G, Alema G, Piazzi G, Panzera MA. Transmission of Creutzfeldt-Jakob disease by dural cadaveric graft (letter) J Neurosurg 1989; 71: 954-955. 15. Miyashita K, Inuzuka T, Kondo H e t al Creutzfeldt-Jakob disease following cadaver dura mater graft. Neurology 1991; 41: 940-941. 16. Willison HJ, Gale AN, McLaughlinJE. Creutzfeldt-Jakob disease following dura mater graft (letter). J Neurol Neurosurg Psychiatry 1991; 54: 940. 17. Pocchiari M, MasuUo C, Salvatore M, Genuardi M, Galgani S. Creutzfeldt-Jakob disease after non-commercial dura mater graft. Lancet 1992; 340: 614-615. 18. Esmonde T, Lueck CJ, Symon L, Duchen LW, Will RG. Creutzfeldt-Jakob disease and lyophilised dura mater grafts: report of two cases. J Neurol Neurosurg Psychiatry 1993; 56: 999-1000. 19. Martinez-Lage JF, Poza M, SolaJ et al. Accidental transmission of Creutzfeldt-Jakob disease by dural cadaveric grafts. J Neurol Neurosurg Psychiatry 1994; 57: 1091-1094. 20. Lane KL, Brown P, Howell DN et al. Creutzfeldt-Jakob disease in a pregnant woman with an implanted dura mater graft. Neurosurgery 1994; 34: 73%740. 21. Yamada S, Aiba T, Endo Y, Hara M, Kitamoto T, TateishiJ. Creutzfeldt-Jakob disease transmitted by a cadaveric dura mater graft. Neurosurgery 1994; 34: 740-744. 22. Gummerlock MK, Kaufman HH, Narayan RK. FDA panel discussion on cadaver dura.J Neurosurg 1990; 73: 310. 23. Duhaime A-C, Sutton LN. Delayed sequelae of pediatric head injury. In: Complications and sequelae of head injury. Barrow DL (ed). American Association of Neurological Surgeons. Park Ridge. 1992 p 175. 24. Black PMcL. Dural graft associated with CJD (comment). Neurosurgery 1994; 34: 739. 25. Gibbs CJ, Asher DM, Kobrine A, Amyx HK, Sulima ME Gajdusek DC. Transmission of Creutzfeldt-Jakob disease to a chimpanzee by electrodes contaminated during neurosurgery. J Neurol Neurosurg Psychiatry 1994; 57: 75%658. 26. Nevin S, McMenemy WH, Behrman S, Jones DE Subacute spongiform encephalopathy - a subacute form of encephalopathy attributable to vascular dysfunction (spongiform cerebral atrophy). Brain 1960; 83: 519-564. 27. Masters CL, HarrisJO, Gajdusek DC et al. CreutzfeldtJakob disease: patterns of world-wide occurrence and the significance of familial and sporadic clustering. Ann Neurol 1979; 5: 177-188. 28. Will RG, Matthews WB. Evidence for case-to-case transmission of Creutzfeld-Jakob disease. J Neurol Neurosurg Psychiatry 1982; 45: 235-238. 29. FoncinJF, GachesJ, Cathala F et al. Transmission iatrog6ne interhumaine possible de maladie de Creutzfeldt-Jakob avec atteinte des grains du cervelet (abstract). Revue Neurol 1980; 136: 280. 30. National Health and Medical Research Council of Australia. Creutzfeldt-Jakob disease and other human transmissible encephalopathies: guidelines on patient management and infection control. 1996 (In press) 31. Taylor DM, Fraser H, McConnell I e t al. Decontamination studies with the agents of bovine spongiform encephalopathy and scrapie. Arch Virol 1994; 139: 313-326.
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32. Ayliffe GAJ. Surgical instruments and disease transmission. Lancet 1993; 341: 1098. 33. BergerJR, David NJ. Creutzfeldt-Jakob disease in a physician: a review of the disorder in health care workers. Neurology 1993; 43:205-206 and 2421 (letter) 34. Schoene WC, Masters CL, Gibbs cJ et al. Transmissible spongiform encephalopathy (Creutzfeldt-Jakob disease).
Atypical clinical and pathological findings. Arch Neurol 1981; 38:473-477. 35. Weber T, Tumani H, Holdorff B et al. Transmission of Creutzfeldt-Jakob disease by handling of dura mater (letter). Lancet 1993; 341: 123-124. 36. UK Department of Health, Spongiform encephalopathies and Creutzfeldt-Jakob disease. October 1993.
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latrogenic Creutzfeldt-Jakob disease and its neurosurgical implications
D. C. G. G. G.
A . S i m p s o n 1 MS FRACS L. M a s t e r s 2 MD O h l r i c h 3 MD QId FRACP FRCP P u r d i e 4 FRACP S t u a r t s FRACS A. E. G. Tannenberg 6 FRCPA XDepartment of Neurosurgery, Women's and Children's Hospital, Adelalde,~Department of Pathology, University of Melbourne, 4Department of Neurology, The Queen Elizabeth Hospital, Woodville, Departments of 3Neurology and 5Neurosurgery, Royal Brisbane Hospital, Brisbane, 6Department of Pathology, Mater Misericordiae Public Hospitals, South Brisbane, Australia.
Creutzfeldt-Jakob (CJD) disease has been reported after the insertion of dural homografts. Two Australian cases of CJD, both following posterior fossa craniotomies done in 1982, are reported; the incubation periods were 5 and 12 years. It seems highly probable that the association is causal. CJD infective agents (prions) are resistant to many previously accepted means of sterih'sation and it is postulated that cadaver dural material was either derived from subjects with CJD, or was contaminated during preparation. In Australia the use of dural homografts in neurosurgery was abandoned in 1987; as the mean incubation period (determined from a world-wide review) has been about 65 months, it is now hoped that this cause of CJD will not recur in the Australian population, although it is premature to state this with confidence. However, precautions against case-to-case transmission remain necessary, and guidelines for this purpose should be enforced in theatre practice and in organ donations. Journal of Clinical Neuroscience 1996, 3(2): 118-123
Keywords:
© Pearson Professional 1996
Creutzfeldt-Jakob disease, Cadaveric dural hornografts, Prion
Introduction Creutzfeldt-Jakob disease (CJD) is a transmissible spongiform encephalopathy, one of a group of h u m a n and animal diseases in which the infecting agents, t e r m e d prions, have properties that distinguish them from other forms o f microbial life. In particular, prions have b e e n shown to be resistant to many procedures intended to secure sterilisation. CJD is usually seen as a sporadic disease affecting the elderly; it is sometimes familial, when there is invariably evidence of a genetic mutation in the PRNP gene coding for the prion protein (PrP). Unhappily, CJD may also be iatrogenic. 1 Case-to-case transmission of CJD by a corneal graft was r e p o r t e d in 1974. 2 In 1977 Bernoulli et al3 r e p o r t e d two cases o f CJD in which the infecting agent was evidently transmitted by implanted depth electrodes. In 1985 reports appeared of transmission by injections of h u m a n pituitary growth h o r m o n e derived from cadavers. In 1987 Penar and Prichard 4 r e p o r t e d a case of CJD occurring 19 months after the use of Lyodura®, a proprietary dural homograft; similar reports have followed. We r e p o r t two additional cases, one o f which has
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already b e e n briefly reported; 5 they are believed to be the first r e c o r d e d in Australia. We also consider the implications of these cases in neurosurgical practice.
Case reports
Case 1 A 56-year-old meat worker presented in 1982 with a complaint o f increasing deafness over a 2 year period. Computerised tomography (CT) showed an enhancing mass in the right cerebellopontine angle, which was consistent with an acoustic neurinoma. Subsequently this t u m o u r and its capsule were resected; during operation the seventh nerve was divided. At the e n d of the operation the dura was closed with the aid of a Lyodura® graft. T h e resected t u m o u r was confirmed as a schwannoma. One m o n t h later a hypoglossal-facial nerve anastomosis was p e r f o r m e d . Five years (58 months) after the initial surgery the patient presented with a 2 week history o f dizzy spells,
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deteriorating memory, blurred vision with transient diplopia and disorientation. He had been normal on review 5 months previously. On examination, there was severe impairment of memory, nystagmus and gait ataxia. CT scan and examination of the cerebrospinal fluid (CSF) were normal. His mental state deteriorated, and over the course of some weeks he became mute and eventually unable to obey commands. There was marked generalised extrapyramidal rigidity and bilateral pyramidal tract signs. Myoclonic jerks were also noted. A clinical diagnosis of CJD was made and electroencephalography (EEG) strongly supported this diagnosis with periodic complexes on a background of diffuse slow activity. He continued to deteriorate and eventually died in a vegetative state 7 weeks after the o n s e t of neurological deterioration and 5 years after the initial m m o u r removal and insertion of Lyodura® graft. An autopsy was performed. T h e immediate cause of death was acute b r o n c h o p n e u m o n i a and acute pulm o n a r y thromboembolism. The brain weighed 1420 g and appeared normal macroscopically. Histological examination confirmed the diagnosis of CJD with widespread spongiform change in cerebral and cerebellar cortex with variable mild to moderate neuronal loss and mild gliosis. The topographical distribution of these changes is d o c u m e n t e d in Table 1. There was no accenmarion of the changes in the brainstem. An unusual feature was the presence of numerous neuritic and diffuse plaques throughout the cerebral cortex. These were uniformly ~ A 4 amyloid positive on immunostaining and were accompanied by an amyloid angiopathy. No neurofibrillary tangles were identified. This case was reported in 1989. 5 Case
2
A 14-year-old boy presented in 1982 with diplopia and marked papilloedema. CT showed a large posterior fossa mmour, partly cystic, which proved to be a benign astrocytoma. It was removed completely, together with its lining. There was tonsillar herniation, and to allow full decompression, an insert of Lyodura® was used to close
the dural defect. Recovery was smooth and there were no residual disabilities. Twelve years later the patient became unsteady on his feet and noticed clumsiness in the upper limbs. He also noted blurred vision and occasional double vision. When seen 4.5 months after the onset of these symptoms he also complained of urinary frequency and slurred speech. Direct questioning elicited complaints of hyperphagia and emotional lability. There was no relevant family history. On examination there was marked gait ataxia, speech was dysarthric, and m o o d suggested frontal lobe impairment, with lack of insight and emotional lability. Eye movements were full without nystagmus, but horizontal saccadic movements were jerky. Power in the limbs was preserved, but there was mild incoordination in the upper limbs and significant ataxia in the legs. EEG showed non-specific slowing of cerebral rhythms. CT and magnetic resonance imaging (MRI) showed no evidence of mmour recurrence. Cerebrospinal fluid (CSF) analysis at this stage showed no specific abnormalities. The ataxia steadily worsened, and a generalised body tremor became evident. A second EEG done 6 m o n t h s after onset of symptoms again showed some slowing of cerebral rhythms, but no periodic complexes. Speech and swallowing worsened, and there was terminal anarthria, dysphagia and declining intellectual function. Myoclonic jerks were recorded during the last fortnight before death, which took place nearly 13 years after tumour removal and 9 months after the onset of symptoms. Autopsy was not performed. Blood examination, courtesy of Dr Paul Brown (Laboratory of Central Nervous System Disorders, National Institute of Neurological Disorders and Stroke, Bethesda, MD USA), showed the PRNP codon 129 genotype to be homozygous for methionine. CSF analysis showed the presence of 130/131 protein spot on 2D gel analysis, and this was considered to confirm the clinical diagnosis of iatrogenic Creutzfeldt-Jakob disease.
Discussion
The unique biology of prion infections presents neurosurgical problems which can be discussed in several contexts. Table 1 Histopathological findings in case 1 Site
Spongiform change
Gliosis
Neuronal loss
Frontal c o r t e x Insular c o r t e x Temporal c o r t e x Parietal cortex Calcarine cortex Hippocampus Entorhinal c o r t e x Putamen C a u d a t e nucleus Thalamus M a m i l l a r y bodies O l f a c t o r y nerve Midbrain Cerebellum Medulla
+ ++ ++ + ++ ++ + + ± colliculi + -
+ + + + ++ + ± + -
+ + ++ + ++ + ± + + -
-
J.
Duraplasty
with
homografts
In 1958 Campbell et al 6 described experiences with freeze-dried h u m a n dura mater, the material being obtained from the US Navy tissue bank. In the same issue of the Journal ofNeurosurgery,Sharkey et al7 also reported on the use of lyophilised cadaver dura, and mentioned its use in hernial repairs. The dura was sterilised by ethylene oxide, and was commercially available. Further favourable reports followed. Koos8 reported on 75 paediatric cases, treated with lyophilised dura in Vienna. In these cases the homografts were apparently prepared by the German firm B Braun Melsungen AG under the proprietary name Lyodura®; sterilisation was by gamma irradiation. Another German firm, Lyofil-PfrimmerGmbH of Erlangen,
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Clinical studies also marketed cadaver dura mater u n d e r the name o f Tutoplast®; this was dehydrated with organic solvents and sterilised by gamma irradiation. In 1971, Abbott and Dupree 9 reported on 170 patients, using dura from the US Navy tissue bank. Sterilisation was effected by liquid ethylene, liquid betapropiolactone, or radiation. The use of cadaver dura mater became widespread, and in 1972 Lyodura® received product recognition in Australia. By 1987 Braun had sold more than 'one half million packages of Lyodura throughout the world'. TMIn that year Cantore et al aI reported on the use of h u m a n dura mater prepared in the La Sapienza Department of Neurosciences, Rome. The dura was sterilised by gamma rays and stored in alcohol; the long term results in 804 cases treated between 1967 and 1984 were considered to be very satisfactory. In 1978 Gibbs et all2 directed attention to the difficulties in destroying the infective particles now known as prions by ionising irradiation. In 1985, reports were published of CJD evidently due to the use of h u m a n pituitary growth h o r m o n e s obtained from autopsies. In May 1985 such h o r m o n e s were withdrawn from use in the UK, USA, Australia and many other countries. This raised the possibility that lyophilised h u m a n dura mater might also transmit CJD. Enquiries were made at that time to Braun, Melsungen, who confirmed awareness of the inefficacy of gamma irradiation alone, but believed that the additional treatment o f cadaver dura for 24 h by 10% sodium peroxide 'had the property of destroying the disulphide bridges' in the prions, so destroying their infective capacity (J. Krause & G. Meil, personal communication, 1985). However, some 16 months later, Penar and Prichard 4 reported the case of a 28-year-old woman who developed encephalopathic symptoms 19 months after the use o f Lyodura® in a cranial operation for cholesteatoma. Biopsy showed changes considered to justify the diagnosis of CJD. The US Food and Drug Administration (FDA) issued a warning against the possibility of such transmission by listed batches of Lyodura®. The case had been notified to one of us (DAS) early in February 1987, by the courtesy ofDrs C.J. Gibbs and D.C. Gajdusek of NINDS, who were aware of earlier concern about this possibility in Australia. A general warning was issued to Australian and New Zealand neurosurgeons through the Neurosurgical Society of Australasia. The Commonwealth Department of Health was also notified, and import permits for hitherto recognised proprietary dural homografts were withdrawn. It was realised that cases receiving dural homografts before this date might be at risk, but it was h o p e d that the rarity of CJD in the general community would make transmission a rare event. Unhappily, this proved not to be the case. In 1989, a second case was reported from Dunedin, New Zealand; 1~ other reports have followed, and to date (May 1995) some 25 cases are on record worldwide, 14-2I not all published (R.G. Will, personal communication). In the great majority, the dural homografts were identified as Lyodura®, although a non-commercial source was identified in one Italian case. 17 Can cadaver dural homografts now be used u n d e r any circumstances? In 1990 the US Neurological Diseases
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Creutzfeldt-Jakob disease Panel o f the FDA concluded that h u m a n cadaveric dural homografts might be used if provided by a tissue bank using acceptable d o n o r screening procedures. 22A recent publication by the American Association of Neurological Surgeons mentions the use o f lyophilised dural homografts as an acceptable procedure. 2s Australian neurosurgeons have felt reluctant to return to this admittedly very convenient means of dural repair, and in the USA misgivings have recently been expressed. 24
Case-to-case transmission Mention has been made o f the cases r e c o r d e d by Bernoulli et al, 3 in which transmission was clearly effected by electrodes which had b e e n contaminated by use in a case of CJD despite supposed sterilisation with 70% alcohol and formaldehyde vapour. Transmission from the electrodes to a chimpanzee was later demonstrated35 It is likely that this is not the only r e c o r d e d example of case-to-case transmission in neurosurgical operations. In 1960 Nevin et a126 r e p o r t e d on eight cases of CJD, three of which had u n d e r g o n e neurosurgical operations of different types in two hospitals. In 1979 Masters et a127 drew attention to this association and suggested the possibility of case-to-case transmission. Will and Matthews 28 later reviewed theatre operation lists from these hospitals and confirmed that there was a temporal proximity between the use of the theatres for diagnostic procedures o n cases o f proven CJD and the operative procedures later followed by CJD in 3 patients originally suffering from a meningioma, a brain abscess and an obsessional neurosis. Foncin et al29 also briefly r e p o r t e d possible operative case-to-case transmission, and other probable cases have been identified27 This strong circumstantial evidence underlines the n e e d for great caution when a case o f CJD must u n d e r g o any surgical procedure, and similar caution may be justified in cases with a history o f a CJD risk factor (see below).
Issues related t o clinical and radiological diagnosis Awareness of CJD is facilitated by a history o f a risk factor such as the administration of h u m a n pituitary h o r m o n e s before 1985, or a homograft duraplasty done before 1987. It may be possible to narrow the risk periods more precisely; it seems likely that, with one exception, TM all cases of CJD attributed to duraplasty u n d e r w e n t operation in the period 1981-1986. It also appears that in the great majority of cases Lyodura® was employed, and it may be possible to exonerate duraplasties p e r f o r m e d with other commercial homografts, though no d o u b t some reservations should be made in such exonerations. However, a sporadic case of CJD could present after an unrelated neurosurgical procedure, while iatrogenic cases could for some reason present without a history o f a risk factor. T h e clinical symptomatology of sporadic CJD is well known. Iatrogenic CJD is typically seen in m u c h younger patients, although this of course depends on the age at exposure to the source of prion infection. T h e incubation period is long, especially for CJD complicating the
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use o f h u m a n pituitary h o r m o n e s where Brown et al] give a range of 4-30 years. Shorter incubation periods have been r e c o r d e d after dural implantation, the range being 16 months - 12 years (case 2 in this report) and the mean approximately 65 months. Iatrogenic CJD also tends to have a somewhat different clinical picture. Presentation with cerebellar ataxia is common, dementia less usual in the early stages, and myoclonic jerks are seen as a rule only in the late stages. The characteristic EEG abnormalides are typically seen late or never. In all these features, our case 2 is characteristic of the cerebellar type of iatrogenic CJD. However, there are cases o f CJD after supratentorial duraplasty which take a different course, with features suggesting early local spread to cerebral cortex. Thus, the second case r e p o r t e d by Esmonde et all8 presented with micropsia, metamorphopsia, and dyslexicdysgraphic symptoms, followed by dysphasia; since the duraplasty was originally p e r f o r m e d to replace a leftsided petrous meningioma it is tempting to suppose that the portal o f prion entry may d e t e r m i n e the nature of the first clinical symptoms. T h e same association appears evident in the case r e c o r d e d by Masullo et al, 14 since in this case a right temporal duraplasty was later followed by a left temporal h e m i a n o p i a and hemiparesis. However, ataxia was an early symptom in one case o f supratentorial duraplasty, 2] and conversely, our case 1 showed early dementia after an infratentorial duraplasty. To establish the diagnosis, it will be necessary to exclude r e c u r r e n c e of the disease for which operation was first p e r f o r m e d . This done, the clinical findings and their relentless course may be sufficient. Confirmation by CSF analysis was of great value in our case 2, but the identification o f the 130/131 protein spot by 2D gel electrophoresis requires specialised expertise, and is not yet widely available. Cerebral biopsy is now r e c o m m e n d e d only when a treatable condition has to be excluded. Autopsy is always desirable.
Theatre precautions In 1994 the Australian National Health & Medical Research Council (NH&MRC) set up a Working Party u n d e r the chairmanship of one of us (CLM) to prepare guidelines on patient m a n a g e m e n t and infection controlP ° This Working Party considered the circumstances in which CJD might be transmitted, and identified two groups o f patients with different risk levels:
Group 1: high risk patients This group includes: 1) patients with proven or suspected CJD; 2) asymptomatic carriers o f pathogenic mutations associated with a familial history of CJD or the allied condition Gerstmann-Str/iussler-Scheinker syndrome (GSS) ; and 3) all members o f a family with CJD/GSS in whom the PrP genotype is u n d e t e r m i n e d or unknown.
Group 2: low risk patients This group includes: 1) any patient with undiaguosed progressive neurological illness with or without dementia; 2)
all members of a family in which there is a strong family history o f undiagnosed d e m e n t i a / n e u r o l o g i c a l illnesses; 3) recipients o f h u m a n pituitary growth h o r m o n e s and gonadotrophins; and 4) recipients of dura mater grafts or persons with a record o f intracranial neurosurgical operations in Australia prior to 1987. We suggest that transdural spinal procedures should be considered to be at risk, since Lyodura® has been used for spinal duraplasty. We also suggest that the risk period in Australia should be from 1972, when permission was given to i m p o r t L y o d u r a ® , to 1989, since some neurosurgeons may not have accepted the evidence of a single case r e p o r t as a contraindication. For patients who u n d e r w e n t operations overseas, n o risk period can be set and the n e u r o s u r g e o n responsible should be contacted. It will be evident that the s e c o n d group is broadly inclusive, and the considerations set out above suggest that it should be possible to narrow the last category o f persons seen to be at risk on neurosurgical grounds. However, this r e p o r t provides a good basis for infection control. It is important to note that the Working Party concluded that normal autoclaving (121°C at 101 kPa), ultraviolet or gamma irradiation, glutaraldehyde, boiling, dry heat, ethylene oxide, acetone, and alcohols are not effective in sterilising material or instruments contaminated by prions. To eliminate prion contamination of surgical instruments the r e p o r t r e c o m m e n d e d gravity or porous load autoclaving to 134°C at 203 kPa. Where chemical sterilisation is needed, immersion for at least 1 h o u r in 1-2 molar sodium hydroxide was r e c o m m e n d e d . However, Taylor et aP 1f o u n d that this p r o c e d u r e did not completely inactivate tissue from bovine spongiform encephalopathy, although sodium hypochlorite was f o u n d to do so. These authors r e c o m m e n d e d exposure for 1 h o u r to a solution of sodium hypochlorite yielding 20,000 p p m o f available chlorine. Present knowledge suggests that n o m e t h o d o f chemical sterilisation will guarantee safety against contamination. Disposable instruments should be used as m u c h as possible, and in high-risk cases, all instruments should be destroyed. This last r e c o m m e n d a t i o n reflects UK guidelines, and has been criticised; s2 nevertheless, it is in accordance with general concepts of the extreme difficulty in eliminating prion contamination. Precautions against case-to-case transmission are also relevant in designing protocols to safeguard staff in the theatre, in the ward, and in the laboratory. Berger and David ~ list reports of CJD in a neurosurgeon, a pathologist, and two histopathology technicians; the case of the n e u r o s u r g e o n has been r e p o r t e d in detail by Schoene et alp4 Weber et al35 have added the case of an orthopaedic surgeon who contracted CJD 20 years after a prolonged period of work involving handling dura mater and sending it to a commercial organisation that sold dura mater preparations later held responsible for CJD transmission. In these cases the evidence for occupational infection is only circumstantial; however, the cases provide additional emphasis to the recommendations on safety precautions.
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Notification of risk from dural homografts Should all recipients o f Lyodura® a n d o t h e r dural h o m o grafts be notified that they are at risk o f this lethal disease, as was d o n e to the recipients of h u m a n pituitary h o r m o n e s ? In the UK, the D e p a r t m e n t of Health in 1993 decided n o t to a t t e m p t to do this, on the grounds that the risks were remote, that individuals would n o t know whether or not they were at risk, a n d that records would often be incomplete or destroyed? 6 A further consideration is the possibility that hospital records m i g h t be misleading, in that operation notes m i g h t state or imply that Lyodura® was used, when in reality some o t h e r preparation of lyophilised d u r a m a t e r was employed. These a r g u m e n t s may be valid; however, it is desirable for n e u r o s u r g e o n s who have used dural homografts to review their records to identify patients who are at risk if this is possible. Blood banks and tissue banks may well reject as donors any person t h o u g h t to be at risk, and a person so rejected will obviously be entitled to a full explanation a n d a p p r o p r i a t e counselling. Received26 September 1995 Accepted for publication 6 October 1995
Correspondence and offprint requests: D. A. Simpson MS FRACS Department of Neurosurgery Women's and Children's Hospital Adelaide Australia 5006 Phone: 61 8 204 7230 Fax: 61 8 204 6575
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32. Ayliffe GAJ. Surgical instruments and disease transmission. Lancet 1993; 341: 1098. 33. BergerJR, David NJ. Creutzfeldt-Jakob disease in a physician: a review of the disorder in health care workers. Neurology 1993; 43:205-206 and 2421 (letter) 34. Schoene WC, Masters CL, Gibbs cJ et al. Transmissible spongiform encephalopathy (Creutzfeldt-Jakob disease).
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