Rabies Prof. Dr Anthony R. Fooks




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Rabies

Prof. Dr Anthony R. Fooks

Veterinary Laboratories Agency (Weybridge), Rabies and Wildlife Zoonoses Group, Department of Virology,

New Haw, Addlestone, Surrey KT15 3NB, United Kingdom

Tel.: (+44-1932) 35.78.40, Fax: (+44-1932) 35.72.39

t.fooks@vla.defra.gsi.gov.uk, website: www.vla.gov.uk

Summary of general activities related to the disease

1. Test(s) in use/or available for the specified disease at your laboratory


Test

For


Specificity

Total

Fluorescent Antibody Test (FAT)

Antigen detection

RABV and other lyssaviruses

1,182

Rabies Tissue Culture Inoculation Test (RTCIT)

Virus isolation

RABV and other lyssaviruses

332

Mouse Inoculation Test

Virus isolation

RABV and other lyssaviruses

66

Reverse-transcriptase Polymerase Chain Reaction (RT-PCR)


RNA detection

RABV and other lyssaviruses (validated for genotypes 1-7)

77

Sequencing


Genotype differentiation

RABV and other lyssaviruses (validated for genotypes 1-7)

200

Fluorescent Antibody Virus Neutralisation Test (FAVN)


Antibody titration

RABV

12,424

2. Production and distribution of diagnostic reagents

2.1 Reagents produced for the specified disease / infection

A panel of monoclonal antibodies is available for the diagnosis of rabies strains. There were no requests in 2007.



2.2 The supply of other reagents and technology transfer

We have supplied rabies virus isolates, reagents, advice or protocols to a number of research and diagnostic units including:



  • Pasteur Institute, Novi Sad, Serbia

  • Madras Veterinary College, India

  • FLI, Wusterhausen, Germany

  • Ivanovsky Institute, Moscow, Russian Federation

  • University of Cambridge, Cambridge, UK

  • Thomas Jefferson University, Philadelphia, USA

  • BioBest, Scotland, UK

  • University College London, UK

2.3 Diagnostic samples

Diagnostic samples / virus isolates were received from a number of sources.



Diagnostic samples / viruses received

Collaborator

Country

Samples

Dr P Burr

Scotland

1 classical rabies virus isolate (Asian strain)

Dr S Stankov

Serbia

145 brain samples (61 positive RABV / gt 1 isolates)

Dr Yahia Beik

Sudan

7 rabies vaccine strains / 18 brain samples (14 positive RABV / gt 1 isolates)

Prof C Tu

China

22 bat brain samples (all samples tested negative)

Dr. G Eberle

Namibia

100 brain samples (94 positive RABV / gt 1 isolates)

Dr D David

Israel (ex. Egypt)

4 brain samples (4 positive RABV / gt 1 isolates)

Dr P Gunawardena

Sri Lanka

6 brain samples (6 positive RABV / gt 1 isolates)

Dr C Nwosuh

Nigeria

60 brain samples (testing in progress)

Dr D Ezeokoli

West Indies

24 brain samples (testing in progress)

Activities specifically related to the mandate
of OIE Reference Laboratories


3. International harmonisation and standardisation of methods for diagnostic testing or the production and testing of vaccines

3.1 Antibody Titration – proficiency testing for serological testing of blood from dogs / cats

The VLA has successfully participated in bi-annual FAVN proficiency schemes, organised by Afssa Nancy, France.



3.2 Antibody Titration – proficiency testing for serological testing of blood from bats

The VLA has provided a QA proficiency scheme for the detection of neutralising antibodies to bat variants of rabies virus, particularly the European Bat Lyssaviruses (EBLV-1 and -2). Two additional European laboratories (including the VLA) participated in the proficiency scheme.



4. Preparation and supply of international reference standards for diagnostic tests or vaccines

None


5. Research and development of new procedures for diagnosis and control

5.1 Development of a canine adenovirus vector expressing the rabies virus glycoprotein

Several recombinant rabies vaccines have been developed for dogs. However, seldom have these vaccines been assessed or used in cats. In this collaborative trial, we report the experimental immunization of a recombinant canine adenovirus-rabies vaccine, CAV-2-E3Δ-RGP, in cats. Thirty cats were inoculated with the recombinant vaccine intramuscularly, orally and intranasally. Safety and efficacy studies were undertaken using the fluorescent antibody virus neutralization (FAVN) test and evaluated. Results showed that this recombinant vaccine is safe for cats as demonstrated by the three different routes of administration. The vaccine stimulated an efficient humoral response in the vaccinated cats when 108.5 PFU/ml of the recombinant vaccine was injected intramuscularly in a single dose. The neutralizing antibody level increased above 0.5 IU/ml at 4 weeks after the vaccination. The mean antibody level ranged from 0.96±0.26 to 4.47±1.57 IU/ml among individuals, and the antibody levels were elicited for at least 12 months. After this period, the immunized cats survived the challenge of CVS-24 and an obvious anemnestic and protective immune response was stimulated after the challenge. The immune response occurred later than the inactivated vaccine and the overall antibody level in the vaccinated cats was lower, but it was sufficient to confer protection of cats against infection. This demonstrated that a single, intramuscular dose of CAV-2-E3Δ-RGP stimulated a long-lasting protective immune response in cats and suggested that CAV-2-E3Δ-RGP could be considered as a potential rabies vaccine candidate for cats [Hu et al., 2007].



5.2 Antigenic characterization of yeast-expressed lyssavirus nucleoproteins

In a collaborative study, the entire authentic nucleoprotein (N protein) encoding sequences of RABV, EBLV-1 and EBLV-2 were expressed in yeast, Saccharomyces cerevisiae, at high level. Purification of recombinant N proteins by caesium chloride gradient centrifugation resulted in yields between 14-17, 25-29 and 18-20 mg/L of induced yeast culture for RABV, EBLV-1 and EBLV-2, respectively. The purified N proteins evaluated by negative staining electron microscopy revealed nucleocapsid-like structures resembling those isolated from native virions. The antigenic conformation of the N proteins was investigated by their reactivity with monoclonal antibodies (mAbs) directed against different lyssaviruses. The reactivity pattern of each mAb was virtually identical between immunofluorescence assay with virus-infected cells and ELISA and dot blot assay using the corresponding recombinant N proteins. These observations lead us to conclude that yeast-expressed lyssavirus N proteins share antigenic properties with naturally expressed virus protein. These recombinant proteins have the potential for use as components of serological assays for lyssaviruses [Kucinskaite et al., 2007].



Publications

  1. Hu, R., Liu, Y., Zhang, S., Zhang, F. and A.R. Fooks. (2007). Experimental immunization of cats with a recombinant rabies-canine adenovirus vaccine elicits a long-lasting neutralizing antibody response against rabies. Vaccine 25(29); 5301-7.

  2. Kucinskaite, I., Juozapaitis, M., Serva, A., Zvirbliene, A., Johnson, N., Staniulis, J., Fooks, A.R., Müller, T., Sasnauskas, K. and R. Ulrich. (2007). Antigenic characterization of yeast-expressed lyssavirus nucleoproteins. Virus Genes 35(3); 521-9.

6. Collection, analysis and dissemination of epizootiological data relevant to international disease control

6.1 Evidence for trans-border movement of rabies by wildlife reservoirs between countries in the Balkan peninsular

Rabies remains endemic in a number of reservoir species throughout southeast Europe. To investigate the relationship between rabies viruses within this region we have compared rabies virus nucleoprotein sequence data from a diverse panel of rabies samples from Bulgaria with available data from countries in the Balkan Peninsula. This analysis provided a first description of rabies isolates in Bulgaria and suggested that there was evidence for wildlife-mediated movement of rabies with countries to the west of Bulgaria including Serbia and Bosnia-Montenegro but no evidence for a link with rabies foci in Turkey. We speculated that natural barriers such as the Balkan mountains may play a significant role in constraining the southerly spread of rabies in southeast Europe [Johnson et al., 2007a].



6.2 Epidemiology of bat rabies in Germany

Rabies in European bats was first reported from Germany in 1954. In concordance with Denmark and The Netherlands, Germany has reported one of the highest numbers (N = 187) of European bat lyssavirus (EBLV)-positive cases in bats in Europe (1954-2005). So far only the two lineages of EBLV-1 (genotype 5), a and b, have been detected. Although only 50% of the rabies positive bats have been identified by species, the Serotine bat (Eptesicus serotinus) is the bat species most frequently infected. Single rabies cases have also been detected in a further five indigenous bat species. In a collaborative study, we showed that there was evidence for a significant bias in the frequency of bat rabies cases in the north of Germany with an endemic cluster in the north-western most low-lying plain parts adjacent to The Netherlands and Denmark [Müller et al., 2007].



6.3 Identification of European bat lyssavirus isolates with short genomic insertions

In a related report confirms the presence of the closely related EBLV-1b in southern Germany, a group previously reported from the Netherlands, France and Spain. Furthermore, two of three German EBLV-1b isolates contain a 6 base pair insertion within the 3’ untranslated region (UTR) of the nucleoprotein gene. This feature was shared with a third EBLV-1b isolate from a region of France adjacent to the French-German border. Further investigation revealed a two base pair insertion in a single isolate of EBLV-2 at the same genomic location. Although the length of the nucleoprotein gene 3’ UTRs do vary between lyssavirus genotypes, such insertions have not been recorded within genotypes and could be the result of duplications within the nucleoprotein mRNA transcript polyadenylation signal [Johnson et al., 2007b].



6.4 Comparative analysis of the full genome sequence for European Bat Lyssavirus type-1 and type-2 with other lyssaviruses and evidence for a conserved transcription termination and polyadenylation motif in the G-L 3’-nontranslated region

We reported the first full-length genomic sequences for European bat lyssavirus type-1 (EBLV-1) and type-2 (EBLV-2) [Marston et al., 2007]. The EBLV-1 genomic sequence was derived from a virus isolated from a Serotine bat in Hamburg, Germany in 1968 and the EBLV-2 sequence derived from a virus isolate from a human case of rabies that occurred in Scotland in 2002. A long distance PCR strategy was used to amplify the open-reading frames (ORFs), followed by standard and modified RACE (rapid amplification of cDNA ends) techniques to amplify the 3’ and 5’ ends. The lengths of each complete viral genome for EBLV-1 and EBLV-2 were 11,966 and 11,930 base-pairs respectively and follow the standard rhabdovirus genome organisation of five viral proteins. Comparison with other lyssavirus sequences demonstrates variation in degrees of homology, with the genomic termini showing a high degree of complementarity. The N-protein was the most conserved, both intra- and intergenotypically, followed by the L-, M- and G- with the P-protein being the most variable. In addition, we have shown that both EBLVs utilise a conserved transcription termination and polyadenylation motif, approximately 50 nucleotides upstream of the L gene start methionine. All available lyssavirus sequences to date, including the EBLVs, use the second TTP site with the exception being Pasteur Virus (PV) and PV-derived isolates. This observation may explain differences in pathogenicity between lyssavirus strains, dependent on the length of the untranslated region, which might affect transcriptional activity and RNA stability.



6.5 Phylogenetic comparison of rabies viruses from disease outbreaks on the Svalbard Islands

We investigated a retrospective source of rabies in the Svarlbard Islands [Johnson et al., 2007c]. In 1980, a wildlife epizootic of rabies occurred on the previously rabies-free Svalbard Islands. Repeated outbreaks in the arctic fox (Alopex lagopus) occurred on the Islands over the following two decades. Phylogenetic characterisation of four viruses isolated from infected arctic foxes from the Islands from three separate outbreaks suggested that the source of these epizootics could have been migration of this species from the Russian mainland.



6.6 Molecular epidemiology identifies only a single rabies virus variant circulating in complex carnivore communities of the Serengeti

Understanding the extent to which multiple hosts contribute to the maintenance of distinct rabies virus variants in a single ecological system is fundamental for effective disease control. In a collaborative study, we used molecular phylogenetics to test whether distinct virus-host associations might occur in the species-rich carnivore community of the Serengeti ecosystem (northwestern Tanzania). Our analysis revealed a single major variant belonging to the group of southern Africa canid-associated viruses (Africa 1b) with a high degree of genetic relatedness among viruses isolated from a range of hosts with no evidence for species-specific grouping. A statistical parsimony analysis supported within- and between-species linkages suggesting intra- and interspecific transmission. Coalescent theory allows a root to be inferred that is consistently placed at nodes representing domestic dog sequences, whereas sequences recovered from other species were localized at the end of rabies virus transmission chains, suggesting transmission from domestic dogs to other species. This study emphasized the value of the analysis of genetic data for identifying transmission pathways [Lembo et al., 2007].



6.7 Molecular epidemiology of rabies in bat-eared foxes (Otocyon megalotis) in South Africa

In a collaborative study, rabies from wildlife hosts (principally the bat-eared fox, Otocyon megalotis) and domestic carnivore species were collected between 1980 and 2005 from a region of South Africa associated with endemic bat-eared fox rabies. We have studied the molecular epidemiology of bat-eared fox rabies by virtue of nucleotide sequence analyses of PCR amplicons specific to the variable G-L intergenic region as well as the conserved nucleoprotein gene of each of the rabies viruses in this South African panel. Although it was demonstrated that all of these viruses were very closely related, they could be segregated into two major phylogenetic groups. These data complement antigenic and surveillance data on rabies in this host species in South Africa. Most importantly our data support a hypothesis that the bat-eared fox independently maintains rabies cycles in specific geographical loci [Sabeta et al., 2007].


Publications


  1. Johnson, N., Fooks, A.R., Valchovski, R. and T. Müller. (2007a). Evidence for trans-border movement of rabies by wildlife reservoirs between countries in the Balkan peninsular. Veterinary Microbiology 120(1-2); 71-6.

  2. Müller, T., Johnson, N., Freuling, C.M., Vos, A., Fooks, A.R. and T. Selhorst. (2007). Epidemiology of bat rabies in Germany. Archives of Virology 152(2); 273-88.

  3. Johnson, N., Freuling, C., Marston, D.A., Tordo, N., Fooks, A.R. and T. Müller. (2007b). Identification of European bat lyssavirus isolates with short genomic insertions. Virus Research. 128(1-2); 140-3.

  4. Marston, D., McElhiney, L.M., Johnson, N., Müller, T., Conzelmann, K.K., Tordo, N. and A.R. Fooks. (2007). Comparative analysis of the full genome sequence for European Bat Lyssavirus type-1 and type-2 with other lyssaviruses and evidence for a conserved transcription termination and polyadenylation motif in the G-L 3’-nontranslated region. Journal of General Virology 88; 1302 – 1314.

  5. Johnson, N., Dicker, A., Mork, T., Marston, D., Fooks, A.R., Tryland, M., Fuglei, E. and T. Müller. (2007c). Phylogenetic comparison of rabies viruses from disease outbreaks on the Svalbard Islands. Vector-Borne and Zoonotic Diseases. 7(3); 457-460.

  6. Lembo, T., Haydon, D.T., Velasco-Villa, A., Rupprecht, C.E., Packer, C., Brandão, P.E., Kuzmin, I.E., Fooks, A.R., Barrat, J. and S. Cleaveland. (2007). Molecular epidemiology identifies only a single rabies virus variant circulating in complex carnivore communities of the Serengeti. Proc. Biol. Soc 274(1622); 2123-30.

  7. Sabeta, C., Mansfield K., McElhinney, L.M., Fooks., A.R. and L.H. Nel. (2007). Molecular epidemiology of rabies in bat-eared foxes (Otocyon megalotis) in South Africa. Virus Research. 129; 1-10.

7. Provision of consultant expertise to OIE or to OIE Member Countries

Reviewer for the OIE manual of Diagnostic Tests and Vaccines for Terrestrial animals: rabies. Co-editor of the book: ‘Towards the Elimination of Rabies in Eurasia’ (2008) B. Dodet, A.R. Fooks, T. Muller, N. Tordo (eds). OIE Publications.



8. Provision of scientific and technical training to personnel from other OIE Member Countries

8.1 Training personnel from other countries in rabies diagnostic techniques.

  • Mr. Conrad Freuling Friedrich-Loeffler Institute, Germany

  • Dr. Panduka Gunawardena, Sri Lanka

  • Dr. Chee-Wee Lim National Authority for Veterinary Public Health and Animal Health, Singapore

  • Prof. Tu / Prof. Hu Changchun Veterinary Research Institute, China

9. Provision of diagnostic testing facilities to other OIE Member Countries

9.1 Collaboration with other WHO collaborating centres (national labs, other institutions or networks collaborating in the programme and activities):

We have continued to work closely with the OIE reference laboratory for Rabies Surveillance and Research at Wusterhausen (Germany). In addition, closer links have been made with the OIE reference laboratory for rabies at CDC, Atlanta, USA.



9.2 Official diagnostic services to other countries

None


10. Organisation of international scientific meetings on behalf of OIE or other international bodies

Organising committee and scientific steering group, 2nd International Conference on Rabies in Eurasia 2007, May 2007, Paris France.



11. Participation in international scientific collaborative studies

11.1 Pathogenesis of EBLV-2 in Daubenton’s bats

This study was undertaken in collaboration with the OIE reference laboratory for Rabies Surveillance and Research at Wusterhausen (Germany), the OIE reference laboratory for rabies at CDC, Atlanta, USA and a private company. Little is known on the anti-viral response to infection of both the natural and spill-over hosts, such as man, following exposure to European Bat Lyssavirus type 2 (EBLV-2). Furthermore, the mechanism of viral egress and transmission has not been firmly established. Like the closely related virus, classical rabies, the EBLV-2 virus is thought to be transmitted through the bite, infect sensory neurons and move rapidly to the brain. Following rapid virus replication, associated with initial clinical symptoms, the virus is then thought to move to peripheral tissue such as the salivary glands and a further infectious cycle can be initiated. However, this remains speculative and unstudied within appropriate experimental models. The objective of this study was to examine virus replication at critical points within the EBLV-2 life cycle using a number of in vivo (mouse, bat) and ex vivo (primary tissue) models. Simultaneously, the host response to infection will be examined to identify evidence of anti-viral activity or the initiation of an innate immune response.

This project has enabled the design of specific primers that enable detection and quantification of a range of EBLV and host (murine) RNA transcripts. This includeed all of the structural genes of EBLV-2 and innate immune response genes (interferons, toll-like receptors, cytokines and chemokines). A number of in vivo studies of EBLV infection in mice and bats (Eptesicus fuscus and Myotis daubentonii) have been completed or are ongoing. These have demonstrated the EBLV-2 is widely distributed within the infected host but highest levels remain in the CNS. Neuroinvasion with EBLV-2 led to a pronounced inflammatory response characterised by perivascular cuffing, lymphocyte infiltration and the upregulation of a range of inflammatory mediators and chemokines. Bats experimentally infected with EBLV-1 (E. fuscus) were suscptible to both intra-cranial (IC) and intra-muscular (IM) inoculation but not oral or intranasal exposure. The incubation period varied with the route of challenge (IC shorter than IM) and the dose (high dose 12 - 35 days; low dose 21 - 58 days). Only 2 bats challenged by the IM route developed an immune response. There was clear evidence of EBLV-1 excretion (PCR and virus isolation) within the saliva in bats experimentally challenged with virus (E. fuscus model). Virus was detected in the saliva of a single bat that survived to the end of the study (90 days). Virus is detectable in both the CNS and periphery but there is evidence that this is linked to the length of the incubation period. The study of EBLV-2 challenge in M. daubentonii is ongoing.

11.2 Virtual Archive of Lyssaviruses In collaboration with the OIE reference laboratory for Rabies Surveillance and Research at Wusterhausen Germany, the Lyssavirus Archives of VLA with those of Tubingen and Wusterhausen have been combined to create a large Virtual Collection of isolates. A joint or linked database is under development to provide access to isolate and partial sequence information.

11.2 Susceptibility of sheep to European Bat Lyssavirus types 1 and -2 infection: A clinical pathogenesis study

In collaboration with the OIE reference laboratory for Rabies Surveillance and Research at Wusterhausen Germany, we have confirmed EBLV-1 and EBLV-2 susceptibility in sheep (Ovis ammon) following intracranial and peripheral (intramuscular) inoculation. Notably, mild clinical disease was observed in those exposed to virus via the intramuscular route. Following the intramuscular challenge, 75% of the animals infected with EBLV-1 and 100% of those that were challenged with EBLV-2 developed clinical signs of rabies and then recovered during the 94-day observation period. Disease pathogenesis also varied substantially between the two viruses. Infection with EBLV-1 resulted in peracute clinical signs, which are suggestive of motor neurone involvement. Antibody induction was observed and substantial inflammatrory infiltrate in the brain. In contrast, more antigen was detected in the EBLV-2 infected sheep brains but less inflammatory infiltrate and no virus neutralising antibody was evident. The latter involved a more protracted disease that was behaviour orientated. A high infectious dose was required to establish EBLV infection under experimental conditions (>5.0 logs/ml) but the infectious dose in field cases remains unknown. These data confirm that sheep are susceptible to infection with EBLV but that there is variability in pathogenesis including neuroinvasiveness that varies with the route of infection. This study suggests that inter-species animal-to-animal transmission of a bat variant of rabies virus to a terrestrial mammal host may be limited, and may not always result in fatal encephalitis.



Brookes, S.M., Klopfleisch, R., Müller, T., Healy, D.M., Teifke, J.P., Lange, E., Kliemt, J., Johnson, N., Johnson, L., Kaden, V., Vos, A. and A.R. Fooks. (2007). Veterinary Microbiology 125; 210-223.

12. Publication and dissemination of information relevant to the work of OIE (including list of scientific publications, internet publishing activities, presentations at international conferences)

  • Presentations at international conferences and meetings

  1. Advisory Board on Cat Diseases (ABCD), [invited speaker], Warsaw, Poland [June 2007]

  2. XVIII Rabies in The Americas (RITA), [speaker] Guanajuato, Mexico[Oct 2007]

  3. The Control and Prevention of Zoonoses from Science to Policy, [invited speaker], Glasgow, [Nov 2007]

  4. 5th International Conference on Emerging Zoonoses, [speaker] Limassol, Cyprus [Nov 2007]

  5. Society for Applied Microbiology (SFAM), Manchester Metropolitan University, UK [invited speaker] [April 2007]

  6. BSAVA Congress, Birmingham, UK [invited speaker] [April 2007]

  7. Health Protection 2007, University of Warwick UK [invited speaker] [Sept 2007]

  • Scientific publications in peer-reviewed journals

  1. Vos, A., Kaipf , I., Denzinger, A., Fooks, A.R., Johnson, N. and T. Müller. (2007). European Bat Lyssaviruses – an ecological enigma. Acta Chiropterologica 9(1); 283-296.

  2. Mallawa, M., Fooks, A.R., Banda, D., Chikungwa, P., Mankhambo, L., Molyneux, E., Molyneux, M.E. and T. Solomon. (2007). Rabies encephalitis in a malaria-endemic area of Malawi, Africa. Emerging Infectious Diseases 13(1); 136-139.

  3. Johnson, N., Fooks, A.R., Valchovski, R. and T. Müller. (2007). Evidence for trans-border movement of rabies by wildlife reservoirs between countries in the Balkan peninsular. Veterinary Microbiology 120(1-2); 71-6.

  4. Müller, T., Johnson, N., Freuling, C.M., Vos, A., Fooks, A.R. and T. Selhorst. (2007). Epidemiology of bat rabies in Germany. Archives of Virology 152(2); 273-88.

  5. Marston, D., McElhiney, L.M., Johnson, N., Müller, T., Conzelmann, K.K., Tordo, N. and A.R. Fooks. (2007). Comparative analysis of the full genome sequence for European Bat Lyssavirus type-1 and type-2 with other lyssaviruses and evidence for a conserved transcription termination and polyadenylation motif in the G-L 3’-nontranslated region. Journal of General Virology 88; 1302 – 1314.

  6. Lembo, T., Haydon, D.T., Velasco-Villa, A., Rupprecht, C.E., Packer, C., Brandão, P.E., Kuzmin, I.E., Fooks, A.R., Barrat, J. and S. Cleaveland. (2007). Molecular epidemiology identifies only a single rabies virus variant circulating in complex carnivore communities of the Serengeti. Proc. Biol. Soc 274(1622); 2123-30.

  7. Hu, R., Liu, Y., Zhang, S., Zhang, F. and A.R. Fooks. (2007). Experimental immunization of cats with a recombinant rabies-canine adenovirus vaccine elicits a long-lasting neutralizing antibody response against rabies. Vaccine 25(29); 5301-7.

  8. Johnson, N., Freuling, C., Marston, D.A., Tordo, N., Fooks, A.R. and T. Müller. (2007). Identification of European bat lyssavirus isolates with short genomic insertions. Virus Research. 128(1-2); 140-3.

  9. Sabeta, C., Mansfield K., McElhinney, L.M., Fooks., A.R. and L.H. Nel. (2007). Molecular epidemiology of rabies in bat-eared foxes (Otocyon megalotis) in South Africa. Virus Research. 129; 1-10.

  10. Johnson, N., Dicker, A., Mork, T., Marston, D., Fooks, A.R., Tryland, M., Fuglei, E. and T. Müller. (2007). Phylogenetic comparison of rabies viruses from disease outbreaks on the Svalbard Islands. Vector-Borne and Zoonotic Diseases. 7(3); 457-460.

  11. Fooks, A.R. (2007). Rabies - the need for a 'one medicine' approach. The Veterinary Record 161; 289-290.

  12. Morris, J., Crowcroft, N.S., Fooks, A.R. Brookes, S.M. and N. Andrews. (2007). Rabies antibody levels in bat handlers in the United Kingdom: immune response before and after purified chick embryo cell rabies booster vaccination. Human Vaccines 3(5); 165-70.

  13. Harris, S., Mansfield, K., Marston, D., Johnson, N., Pajamo, K., O’Brien, N., Black, C., McElhinney, L.M. and A.R. Fooks. (2007). Isolation of a European bat lyssavirus type-2 from a Daubenton’s bat (Myotis daubentonii) in Shropshire, UK. The Veterinary Record 161(11); 384-386.

  14. Brookes, S.M., Klopfleisch, R., Müller, T., Healy, D.M., Teifke, J.P., Lange, E., Kliemt, J., Johnson, N., Johnson, L., Kaden, V., Vos, A. and A.R. Fooks. (2007). Susceptibility of sheep to European Bat Lyssavirus types 1 and -2 infection: A clinical pathogenesis study. Veterinary Microbiology 125; 210-223.

  15. Fooks, A.R. (2007). Rabies awareness. The Veterinary Record 161(12); 432.

  16. Kucinskaite, I., Juozapaitis, M., Serva, A., Zvirbliene, A., Johnson, N., Staniulis, J., Fooks, A.R., Müller, T., Sasnauskas, K. and R. Ulrich. (2007). Antigenic characterization of yeast-expressed lyssavirus nucleoproteins. Virus Genes. 35(3); 521-9.

  17. Kennedy, L.J., Lunt, M., Barnes, A., McElhinney, L., Fooks, A.R., Baxter, D.N. and W.E.R. Ollier. (2007). Factors influencing the antibody response of dogs vaccinated against rabies. Vaccine. 25(51); 8500-7.

  • Other communications

  1. Fooks, A.R. (2007). Rabies: current perspectives in an enlarged Europe. BSAVA Congress proceedings. pp. 70 - 71.

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Annual reports of OIE Reference Laboratories and Collaborating Centres, 2007


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