Bovine spongiform encephalopathy (BSE) cases born after the total feed ban

Abstract Sixty bovine spongiform encephalopathy (BSE) cases of Classical or unknown type (BARB‐60 cases) were born after the date of entry into force of the EU total feed ban on 1 January 2001. The European Commission has requested EFSA to provide a scientific opinion on the most likely origin(s) of these BARB‐60 cases; whether feeding with material contaminated with the BSE agent can be excluded as the origin of any of these cases and, if so, whether there is enough scientific evidence to conclude that such cases had a spontaneous origin. The source of infection cannot be ascertained at the individual level for any BSE case, including these BARB‐60 cases, so uncertainty remains high about the origin of disease in each of these animals, but when compared with other biologically plausible sources of infection (maternal, environmental, genetic, iatrogenic), feed‐borne exposure is the most likely. This exposure was apparently excluded for only one of these BARB‐60 cases. However, there is considerable uncertainty associated with the data collected through the field investigation of these cases, due to a time span of several years between the potential exposure of the animal and the confirmation of disease, recall difficulty, and the general paucity of documented objective evidence available in the farms at the time of the investigation. Thus, feeding with material contaminated with the BSE agent cannot be excluded as the origin of any of the BARB‐60 cases, nor is it possible to definitively attribute feed as the cause of any of the BARB‐60 cases. A case of disease is classified as spontaneous by a process of elimination, excluding all other definable possibilities; with regard to the BARB‐60 cases, it is not possible to conclude that any of them had a spontaneous origin.

[1]  J. Hope,et al.  Is there a decline in bovine spongiform encephalopathy cases born after reinforced feed bans? A modelling study in EU member states , 2017, Epidemiology and Infection.

[2]  N. Speybroeck,et al.  Chronic wasting disease (CWD) in cervids , 2017, EFSA journal. European Food Safety Authority.

[3]  A. Adkin,et al.  Assessing the sensitivity of European surveillance for detecting BSE in cattle according to international standards. , 2016, Preventive veterinary medicine.

[4]  R. Will,et al.  Ten‐year follow‐up of two cohorts with an increased risk of variant CJD: donors to individuals who later developed variant CJD and other recipients of these at‐risk donors , 2016, Vox sanguinis.

[5]  R. Girones,et al.  An assessment of the long-term persistence of prion infectivity in aquatic environments. , 2016, Environmental research.

[6]  M. Simmons,et al.  Evidence of scrapie transmission to sheep via goat milk , 2016, BMC Veterinary Research.

[7]  A. Aguzzi,et al.  The Priority position paper: Protecting Europe's food chain from prions , 2016, Prion.

[8]  J. Collinge,et al.  Iatrogenic CJD due to pituitary-derived growth hormone with genetically determined incubation times of up to 40 years , 2015, Brain : a journal of neurology.

[9]  M. D. Di Bari,et al.  Further characterisation of transmissible spongiform encephalopathy phenotypes after inoculation of cattle with two temporally separated sources of sheep scrapie from Great Britain , 2015, BMC Research Notes.

[10]  C. Soto,et al.  Grass plants bind, retain, uptake, and transport infectious prions. , 2015, Cell reports.

[11]  Claudia Paoletti,et al.  Food and feed safety assessment: the importance of proper sampling. , 2015, Journal of AOAC International.

[12]  Kim H Esbensen,et al.  Distributional assumptions in food and feed commodities- development of fit-for-purpose sampling protocols. , 2015, Journal of AOAC International.

[13]  M. Simmons,et al.  Phenotype Shift from Atypical Scrapie to CH1641 following Experimental Transmission in Sheep , 2015, PloS one.

[14]  G. Murdoch,et al.  Genetics of Prion Disease in Cattle , 2015, Bioinformatics and biology insights.

[15]  H. Simmons,et al.  Persistence of ovine scrapie infectivity in a farm environment following cleaning and decontamination , 2014, Veterinary Record.

[16]  A. Molesworth,et al.  Investigation of Variant Creutzfeldt-Jakob Disease Implicated Organ or Tissue Transplantation in the United Kingdom , 2014, Transplantation.

[17]  N. Neumann,et al.  Biodegradation of prions in compost. , 2014, Environmental science & technology.

[18]  T. Selhorst,et al.  Case-control study on the risks of BSE infections in Northern Germany. , 2013, Berliner und Munchener tierarztliche Wochenschrift.

[19]  A. Adkin,et al.  A Quantitative Assessment of the Prion Risk Associated with Wastewater from Carcass‐Handling Facilities , 2013, Risk analysis : an official publication of the Society for Risk Analysis.

[20]  S. Cawthraw,et al.  Bovine spongiform encephalopathy: the effect of oral exposure dose on attack rate and incubation period in cattle – an update , 2012, BMC Research Notes.

[21]  A. Adkin,et al.  Model for the evaluation of different options for the monitoring of Transmissible Spongiform Encephalopathies in cattle in the European Union (C‐TSEMM) , 2012 .

[22]  G. Ru,et al.  A relevant long-term impact of the circulation of a potentially contaminated vaccine on the distribution of scrapie in Italy. Results from a retrospective cohort study , 2012, Veterinary Research.

[23]  R. Girones,et al.  Persistence of the bovine spongiform encephalopathy infectious agent in sewage. , 2012, Environmental research.

[24]  S. More,et al.  The epidemiology of bovine spongiform encephalopathy in the Republic of Ireland before and after the reinforced feed ban. , 2012, Preventive veterinary medicine.

[25]  J. W. Wilesmith,et al.  Case-control study of cases of bovine spongiform encephalopathy born after July 31, 1996 (BARB cases) in Great Britain , 2012, Veterinary Record.

[26]  O. Andréoletti,et al.  Classical Bovine Spongiform Encephalopathy by Transmission of H-Type Prion in Homologous Prion Protein Context , 2011, Emerging infectious diseases.

[27]  M. Simmons,et al.  Experimental bovine spongiform encephalopathy: detection of PrP(Sc) in the small intestine relative to exposure dose and age. , 2011, Journal of comparative pathology.

[28]  J. Pedersen,et al.  Fate of prions in soil: a review. , 2011, Journal of environmental quality.

[29]  M. Groschup,et al.  BSE infectivity in jejunum, ileum and ileocaecal junction of incubating cattle , 2011, Veterinary research.

[30]  Christopher J. Johnson,et al.  Meat and Bone Meal and Mineral Feed Additives May Increase the Risk of Oral Prion Disease Transmission , 2011, Journal of Toxicology and Environmental Health, Part A.

[31]  Claire A. Baker,et al.  Environmental Sources of Scrapie Prions , 2010, Journal of Virology.

[32]  J. Wilesmith,et al.  Descriptive epidemiological features of cases of bovine spongiform encephalopathy born after July 31, 1996 in Great Britain , 2010, Veterinary Record.

[33]  A. Aguzzi.  Prions of Humans and Animals , 2010 .

[34]  A. Chemeris,et al.  Polymorphism of the prion protein gene PRNP and risk of multiple sclerosis development in ethnic Russians from Bashkortostan , 2009, Russian Journal of Genetics.

[35]  P. Gatta.  review of the origin of bse , 2009 .

[36]  P. Burke.  Preliminary epidemiological analysis of BSE cases born after 2000 in Great Britain , 2009, Veterinary Record.

[37]  M. Pumarola,et al.  Assessing the presence of BSE and scrapie in slaughterhouse wastewater , 2008, Journal of applied microbiology.

[38]  J. Richt,et al.  BSE Case Associated with Prion Protein Gene Mutation , 2008, PLoS pathogens.

[39]  S. Bellworthy,et al.  Approaches to investigating transmission of spongiform encephalopathies in domestic animals using BSE as an example. , 2008, Veterinary research.

[40]  Christian Ducrot,et al.  Review on the epidemiology and dynamics of BSE epidemics. , 2008, Veterinary research.

[41]  S. Bellworthy,et al.  Pruritus is a common feature in sheep infected with the BSE agent , 2008, BMC veterinary research.

[42]  Y. Yoshikawa.  Epidemiological study on BSE outbreak in Japan. , 2008, The Journal of veterinary medical science.

[43]  J. Lumley.  The impact of Creutzfeldt-Jakob disease on surgical practice. , 2008, Annals of the Royal College of Surgeons of England.

[44]  T. Tsutsui,et al.  Milk Replacers and Bovine Spongiform Encephalopathy in Calves, Japan , 2008, Emerging infectious diseases.

[45]  T. Selhorst,et al.  Risk factors for BSE-infections in Lower Saxony, Germany. , 2008, Preventive veterinary medicine.

[46]  L. Leita,et al.  Direct Detection of Soil-Bound Prions , 2007, PloS one.

[47]  G. Ru,et al.  Epidemiological study of the decline of bse in Italy , 2007, Veterinary Record.

[48]  Lourens Heres,et al.  Identification of the Characteristics and Risk Factors of the BSE Epidemic in the Netherlands , 2007, Risk analysis : an official publication of the Society for Risk Analysis.

[49]  C. Fischer,et al.  Functional relevance of DNA polymorphisms within the promoter region of the prion protein gene and their association to BSE infection , 2007, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[50]  E. Morignat,et al.  Case-control study on feed risk factors for BSE cases born after the feed ban in France. , 2007, Veterinary research.

[51]  F. Brülisauer,et al.  Evaluation of the effectiveness of selected measures against bovine spongiform encephalopathy (BSE) in Switzerland by use of the basic reproduction ratio R0. , 2007, Berliner und Munchener tierarztliche Wochenschrift.

[52]  J. Woolliams,et al.  Polymorphisms of the prion protein gene coding region in born-after-the-reinforced-ban (BARB) bovine spongiform encephalopathy cattle in Great Britain. , 2007, The Journal of general virology.

[53]  J. Wilesmith,et al.  Bovine spongiform encephalopathy: the effect of oral exposure dose on attack rate and incubation period in cattle. , 2007, The Journal of general virology.

[54]  L. Minati,et al.  Conversion of the BASE Prion Strain into the BSE Strain: The Origin of BSE? , 2007, PLoS pathogens.

[55]  L. Manuelidis.  A 25 nm virion is the likely cause of transmissible spongiform encephalopathies , 2007, Journal of cellular biochemistry.

[56]  H. Schwermer,et al.  Cases of bovine spongiform encephalopathy born in Switzerland before and after the ban on the use of bovine specified risk material in feed , 2007, Veterinary Record.

[57]  J. Wilesmith,et al.  Different prion disease phenotypes result from inoculation of cattle with two temporally separated sources of sheep scrapie from Great Britain , 2006, BMC veterinary research.

[58]  H. Schwarzenbacher,et al.  A major genetic component of BSE susceptibility , 2006, BMC Biology.

[59]  F. Conraths,et al.  Potential risk factors associated with bovine spongiform encephalopathy in cattle from Schleswig-Holstein, Germany. , 2006, Journal of veterinary medicine. B, Infectious diseases and veterinary public health.

[60]  D. Taylor,et al.  Inactivation of transmissible spongiform encephalopathy agents during the manufacture of dicalcium phosphate from bone , 2006, Veterinary Record.

[61]  D. Riesner,et al.  Prions in Humans and Animals , 2006 .

[62]  N. Gibbens.  Link between feed bins and BSE cases born after July 1996 , 2005, Veterinary Record.

[63]  A. Colchester,et al.  The origin of bovine spongiform encephalopathy: the human prion disease hypothesis , 2005, The Lancet.

[64]  Christian Ducrot,et al.  A spatio-temporal analysis of BSE cases born before and after the reinforced feed ban in France. , 2005, Veterinary research.

[65]  R. Morris,et al.  Area-level risks for BSE in British cattle before and after the July 1988 meat and bone meal feed ban. , 2005, Preventive veterinary medicine.

[66]  A. Ebringer,et al.  Bovine Spongiform Encephalopathy, Multiple Sclerosis, and Creutzfeldt‐Jakob Disease Are Probably Autoimmune Diseases Evoked by Acinetobacter Bacteria , 2005, Annals of the New York Academy of Sciences.

[67]  J. Spiropoulos,et al.  Pathogenesis of experimental bovine spongiform encephalopathy: preclinical infectivity in tonsil and observations on the distribution of lingual tonsil in slaughtered cattle , 2005, Veterinary Record.

[68]  Charles Weissmann,et al.  The state of the prion , 2004, Nature Reviews Microbiology.

[69]  D. Calavas,et al.  Molecular Analysis of the Protease-Resistant Prion Protein in Scrapie and Bovine Spongiform Encephalopathy Transmitted to Ovine Transgenic and Wild-Type Mice , 2004, Journal of Virology.

[70]  Christian Ducrot,et al.  Estimating the trend of the French BSE epidemic over six birth cohorts through the analysis of abattoir screening in 2001 and 2002. , 2004, Veterinary research.

[71]  L. Paisley,et al.  A quantitative assessment of the risk of transmission of bovine spongiform encephalopathy by tallow-based calf milk-replacer. , 2004, Preventive veterinary medicine.

[72]  L. Terry,et al.  Detection of disease-specific PrP in the distal ileum of cattle exposed orally to the agent of bovine spongiform encephalopathy , 2003, Veterinary Record.

[73]  J. Wilesmith.  Preliminary epidemiological analyses of the first 16 cases of BSE born after iuly 31, 1996, in Great Britain , 2002, Veterinary Record.

[74]  S. Bellworthy,et al.  Distinction of scrapie phenotypes in sheep by lesion profiling. , 2002, Journal of comparative pathology.

[75]  R. Somerville,et al.  Characterization of Thermodynamic Diversity between Transmissible Spongiform Encephalopathy Agent Strains and Its Theoretical Implications* , 2002, The Journal of Biological Chemistry.

[76]  H. Narang.  A Critical Review of the Nature of the Spongiform Encephalopathy Agent: Protein Theory Versus Virus Theory 1 , 2002, Experimental biology and medicine.

[77]  S. Bellworthy,et al.  Differential diagnosis of infections with the bovine spongiform encephalopathy (BSE) and scrapie agents in sheep. , 2001, Journal of comparative pathology.

[78]  P. Gale,et al.  Towards a quantitative risk assessment for BSE in sewage sludge , 2001, Journal of applied microbiology.

[79]  H. Narang.  A Critical Review of Atypical Cerebellum-Type Creutzfeldt-Jakob Disease: Its Relationship to “New Variant” CJD and Bovine Spongiform Encephalopathy , 2001, Experimental biology and medicine.

[80]  M. Purdey.  Does an ultra violet photooxidation of the manganese-loaded/copper-depleted prion protein in the retina initiate the pathogenesis of TSE? , 2001, Medical hypotheses.

[81]  I. McGill.  Phillips report and the origin of BSE. , 2001, The Veterinary record.

[82]  M. Usher,et al.  The United Kingdom , 2001, Migration and Integration.

[83]  R. Morris,et al.  Temporal aspects of the epidemic of bovine spongiform encephalopathy in Great Britain: holding.associated risk factors for the disease , 2000, Veterinary Record.

[84]  M Purdey,et al.  Ecosystems supporting clusters of sporadic TSEs demonstrate excesses of the radical-generating divalent cation manganese and deficiencies of antioxidant co factors Cu, Se, Fe, Zn. Does a foreign cation substitution at prion protein's Cu domain initiate TSE? , 2000, Medical hypotheses.

[85]  S. Whatley,et al.  Phosmet induces up‐regulation of surface levels of the cellular prion protein , 1998, Neuroreport.

[86]  M. Purdey.  High-dose exposure to systemic phosmet insecticide modifies the phosphatidylinositol anchor on the prion protein: the origins of new variant transmissible spongiform encephalopathies? , 1998, Medical Hypotheses.

[87]  A. Ghani,et al.  Analysis of dam–calf pairs of BSE cases: confirmation of a maternal risk enhancement , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[88]  J. Wilesmith,et al.  A cohort study to examine maternally-associated risk factors for bovine spongiform encephalopathy , 1997, Veterinary Record.

[89]  T. Stockdale.  Are Bacterial Toxins Involved in the Aetiology of Transmissible Spongiform Encephalopathies? , 1997, Nutrition and health.

[90]  R. Curnow,et al.  Separating the environmental and genetic factors that may be causes of bovine spongiform encephalopathy. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[91]  M. Purdey.  The UK epidemic of BSE: slow virus or chronic pesticide-initiated modification of the prion protein? Part 1: Mechanisms for a chemically induced pathogenesis/transmissibility. , 1996, Medical hypotheses.

[92]  M. Purdey.  The UK epidemic of BSE: slow virus or chronic pesticide-initiated modification of the prion protein? Part 2: An epidemiological perspective. , 1996, Medical hypotheses.

[93]  I. Andersson,et al.  Soil ingestion in farm animals. A review , 1996 .

[94]  M. Richards,et al.  An investigation of risk factors for cases of bovine spongiform encephalopathy born after the introduction of the 'feed ban' , 1995, Veterinary Record.

[95]  N. Hunter,et al.  Frequencies of PrP gene variants in healthy cattle and cattle with BSE in Scotland , 1994, Veterinary Record.

[96]  H. Narang.  Evidence That Homologous ssDNA Is Present in Scrapie, Creutzfeldt‐Jakob Disease, and Bovine Spongiform Encephalopathy a , 1994, Annals of the New York Academy of Sciences.

[97]  J. Miller,et al.  Intracerebral transmission of scrapie to cattle. , 1994, The Journal of infectious diseases.

[98]  B. Schreuder.  BSE agent hypotheses , 1994 .

[99]  J. Wilesmith,et al.  Epidemiology and control of bovine spongiform encephalopathy (BSE). , 1993, British medical bulletin.

[100]  T. Alper.  The scrapie enigma: insights from radiation experiments. , 1993, Radiation research.

[101]  E. Sulkowski.  Spontaneous conversion of PrPC to PrPSc , 1992, FEBS letters.

[102]  W D Hueston,et al.  Bovine spongiform encephalopathy: case-control studies of calf feeding practices and meat and bonemeal inclusion in proprietary concentrates. , 1992, Research in veterinary science.

[103]  J W Wilesmith,et al.  Bovine spongiform encephalopathy: epidemiological studies on the origin , 1991, Veterinary Record.

[104]  J. Ryan,et al.  Bovine spongiform encephalopathy: epidemiological studies , 1988, Veterinary Record.

[105]  M. Jeffrey,et al.  A novel progressive spongiform encephalopathy in cattle , 1987, Veterinary Record.

[106]  T. Alper.  Scrapie agent unlike viruses in size and susceptibility to inactivation by ionizing or ultraviolet radiation , 1985, Nature.

[107]  N. Speybroeck,et al.  Evaluation of the revision of the BSE monitoring regime in Croatia , 2016 .

[108]  T. Hald,et al.  EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards), 2014. Scientific Opinion on the scrapie situation in the EU after 10 years of monitoring and control in sheep and goats , 2014 .

[109]  P. Liberski,et al.  Human prion diseases: from Kuru to variant Creutzfeldt-Jakob disease. , 2012, Sub-cellular biochemistry.

[110]  Bovine Spongiform Encephalopathy and Spatial Analysis of the Feed Industry , 2009 .

[111]  L. Hansen,et al.  Short communication: Allele, genotype, and haplotype data for bovine spongiform encephalopathy-resistance polymorphisms from healthy US Holstein cattle. , 2008, Journal of dairy science.

[112]  R. Wiggins.  Prion Stability and Infectivity in the Environment , 2008, Neurochemical Research.

[113]  C. Ducrot,et al.  Milk yield, age at first calving, and the risk of BSE: an analysis at the farm level in France. , 2007, Preventive veterinary medicine.

[114]  C. Ettelaie,et al.  From rabies to transmissible spongiform encephalopathies: an immune-mediated microbial trigger involving molecular mimicry could be the answer. , 2007, Medical hypotheses.

[115]  H. Kretzschmar,et al.  Pathology and genetics of human prion diseases , 2006 .

[116]  C. Darcel.  Reflections on scrapie and related disorders, with consideration of the possibility of a viral aetiology , 2005, Veterinary Research Communications.

[117]  J. Frey.  Bovine Spongiform Encephalopathy: Are the Cows Mad or Full of Carbohydrates? , 2002, Clinical chemistry and laboratory medicine.

[118]  G. Horn,et al.  Review of the Origin of BSE , 2001 .

[119]  U. Braun,et al.  [182 offspring of cows with bovine spongiform encephalopathy (BSE) in Switzerland. 1. Clinical findings]. , 1998, Schweizer Archiv fur Tierheilkunde.

[120]  U. Braun,et al.  [182 offspring of cows with bovine spongiform encephalopathy (BSE) in Switzerland. 2. Epidemiology and pathological findings]. , 1998, Schweizer Archiv fur Tierheilkunde.

[121]  Marc Vandevelde,et al.  UNTERSUCHUNGEN AN 182 NACHKOMMEN VON AN BOVINER SPONGIFORMER ENZEPHALOPATHIE (BSE) ERKRANKTEN KUHEN IN DER SCHWEIZ. TEIL 2: EPIDEMIOLOGISCHE UND PATHO LOGISCHE BEFUNDE , 1998 .

[122]  J. Wilesmith.  Recent Observations on the Epidemiology of Bovine Spongiform Encephalopathy , 1996 .

[123]  G. Davies.  Origin of BSE. , 1996, The Veterinary record.

[124]  J. Aiken,et al.  PRP gene variability in the us cattle population , 1992 .

[125]  N. Hunter,et al.  Different forms of the bovine PrP gene have five or six copies of a short, G-C-rich element within the protein-coding exon. , 1991, The Journal of general virology.

[126]  W. S. Gordon.  Advances in veterinary research. , 1946, The Veterinary record.

[127]  The nature and cause of BSE , 2022 .