Current status and molecular epidemiology of rabies virus from different hosts and regions in Malawi.
Journal
Archives of virology
ISSN: 1432-8798
Titre abrégé: Arch Virol
Pays: Austria
ID NLM: 7506870
Informations de publication
Date de publication:
12 Jan 2023
12 Jan 2023
Historique:
received:
06
06
2022
accepted:
21
10
2022
entrez:
11
1
2023
pubmed:
12
1
2023
medline:
14
1
2023
Statut:
epublish
Résumé
Although rabies is endemic in Malawi, there have been no studies in which rabies virus was systematically investigated and characterized in multiple animal hosts in that country. In order to provide molecular epidemiological data on rabies virus in Malawi, 683 suspected rabies case reports from 2008 to 2021 were examined, and 46 (dog = 40, cow = 5, and cat = 1) viable rabies-positive brain samples archived at the Central Veterinary Laboratory (CVL), Lilongwe, Malawi, were analyzed genetically. The results showed an increase in the submission of brain samples from 2008 to 2010, with the highest number of submissions observed in 2020. Of the 683 case reports analyzed for the period under review, 38.1% (260/683) (CI: 34.44 - 41.84) were confirmed by direct fluorescent antibody test. Among the confirmed cases, 65.4% (170/260) (CI: 59.23 - 71.09) were canine rabies. Further, phylogenetic analysis revealed that sequences from different animal hosts clustered together within the Africa 1b lineage, suggesting that the strains circulating in livestock are similar to those in domestic dogs. This finding supports the hypothesis that canine rabies is spilling over to livestock and emphasizes the need for further studies to provide data for effective control of rabies in Malawi.
Identifiants
pubmed: 36631547
doi: 10.1007/s00705-022-05635-z
pii: 10.1007/s00705-022-05635-z
pmc: PMC9834359
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
61Subventions
Organisme : Japan Agency for Medical Research and Development
ID : JP21wm0125008
Informations de copyright
© 2023. The Author(s).
Références
International Committee on Taxonomy of Viruses. https://ictv.global/taxonomy/taxondetails?taxnode_id=202101733 . Accessed 26 Aug 2022
World Health Organization (2018) WHO expert consultation on rabies third report. World Health Organization. https://apps.who.int/iris/handle/10665/272364 . License: CC BY-NC-SA 3.0 IGO. Accessed 5 Sept 2022
Lembo T, Hampson K, Kaare MT, Ernest E, Knobel D, Kazwala RR, Haydon DT, Cleaveland S (2010) The feasibility of canine rabies elimination in Africa: dispelling doubts with data. PLoS Negl Trop Dis 4:e626. https://doi.org/10.1371/journal.pntd.0000626
doi: 10.1371/journal.pntd.0000626
pmcid: 2826407
Knobel DL, Cleaveland S, Coleman PG, Fèvre EM, Meltzer MI, Miranda MEG, Shaw A, Zinsstag J, Meslin FX (2005) Re-evaluating the burden of rabies in Africa and Asia. Bull World Health Organ 83:360–368
pmcid: 2626230
Hampson K, Coudeville L, Lembo T, Sambo M, Kieffer A, Attlan M, Barrat J, Blanton JD, Briggs D, Cleaveland S, Costa P, Freuling CM, Hiby E, Knopf L, Leanes F, Meslin FX, Metlin A, Miranda ME, Müller T, Nel LH, Recuenco S, Rupprecht CE, Schumacher C,Taylor L, Vigilato MA, Zinsstag J, Dushoff J (2015) Global alliance for rabies control partners for rabies prevention. Estimating the global burden of endemic canine rabies. PLoS Negl Trop Dis 9:e0003709. https://doi.org/10.1371/journal.pntd.0003709
Cleaveland S, Ferve E, Kaare M, Coleman P (2002) Estimating human rabies mortality in the United Republic of Tanzania from dog bite injuries. Bull World Health Organ 80:304–310
pmcid: 2567765
Mtui-Malamsha N, Sallu R, Mahiti GR, Mohamed H, OleNeselle M, Rubegwa B, Swai ES, Makungu S, Otieno EG, Lupindu AM, Komba E, Mdegela R, Assenga JA, Bernard J, Marandu W, Warioba J, Makondo Z, Chang’a J, Mramba F, Nonga H, Killewo J, Kafeero F, Makonnen YJ, Rivas AL, Fasina FO (2019) Ecological and epidemiological findings associated with zoonotic rabies outbreaks and control in Moshi, Tanzania, 2017–2018. Int J Environ Res Public Health 16:2816. https://doi.org/10.3390/ijerph16162816
Lunney M, Fèvre SJS, Stiles E, Ly S, San S, Vong S (2012) Knowledge, attitudes and practices of rabies prevention and dog bite injuries in urban and peri-urban provinces in Cambodia, 2009. Int Health 4:4–9. https://doi.org/10.1016/j.inhe.2011.12.001
doi: 10.1016/j.inhe.2011.12.001
Wunner HW (1994) Rabies virus. In: Mckendall RR, Stroop WG (eds) Handbook of neurovirology. Marcel Dekker Inc., New York, pp 455–462
Rose JK, Whitt MA (2001) Rhabdoviridae: the viruses and their replication. Lippincott-Raven Publishers, Philadelphia, pp 1221–1224
Tordo N, Poch O, Ermine A, Keith G, Rougeon F (1986) Walking along the rabies genome: is the large G-L intergenic region a remnant gene? Proc Natl Acad Sci USA 83:3914–3918. https://doi.org/10.1073/pnas.83.11.3914
doi: 10.1073/pnas.83.11.3914
pmcid: 323635
Patton JT, Davis NL, Wertz GW (1984) N protein alone satisfies the requirement for protein synthesis during RNA replication of vesicular stomatitis virus. J Virol 49:303–309
doi: 10.1128/jvi.49.2.303-309.1984
pmcid: 255465
Hyun BH, Lee KK, Kim IJ, Lee KW, Park HJ, Lee OS, An SH, Lee JB (2005) Molecular epidemiology of rabies virus isolates from South Korea. Virus Res. https://doi.org/10.1016/j.virusres.2005.06.004
doi: 10.1016/j.virusres.2005.06.004
Yamagata J, Ahmed K, Khawplod P, Mannen K, Xuyen DK, Loi HH, Dung NV, Nishizono A (2007) Molecular epidemiology of rabies in Vietnam. Microbiol Immunol 51:833–840. https://doi.org/10.1111/j.1348-0421.2007.tb03979.x
doi: 10.1111/j.1348-0421.2007.tb03979.x
Susetya H, Sugiyama M, Inagaki A, Ito N, Mudiarto G, Minamoto N (2008) Molecular epidemiology of rabies in Indonesia. Virus Res 135(1):144–149
doi: 10.1016/j.virusres.2008.03.001
Muleya W, Namangala B, Mweene A, Zulu L, Fandamu P, Banda D, Kimura T, Sawa H, Ishii A (2012) Molecular epidemiology and a loop-mediated isothermal amplification method for diagnosis of infection with rabies virus in Zambia. Virus Res 163:160–168. https://doi.org/10.1016/j.virusres.2011.09.010
doi: 10.1016/j.virusres.2011.09.010
Muleya W, Chambaro HM, Sasaki M, Gwenhure LF, Mwenechanya R, Kajihara M, Saasa N, Mupila Z, Mori-Kajihara A, Qiu Y, Kangwa E, Mweene A, Namangala B, Takada A, Sawa H (2019) Genetic diversity of rabies virus in different host species and geographic regions of Zambia and Zimbabwe. Virus Genes 55:713–719. https://doi.org/10.1007/s11262-019-01682-y
doi: 10.1007/s11262-019-01682-y
WHO. Expert: consultation on rabies, first report. WHO technical report series 2005; No. 931. World Health Organization. http://www.who.int/rabies/931/en/index.html
Ngoepe E, Fehlner-Gardiner C, Wandeler A, Sabeta C (2014) Antigenic characterisation of lyssaviruses in South Africa. Onderstepoort J Vet Res 81:1–9. https://doi.org/10.4102/ojvr.v81i1.711
doi: 10.4102/ojvr.v81i1.711
Markotter W, Coertse J (2018) Bat lyssaviruses. Revue scientifique et technique (International Office of Epizootics) 37(2):385–400. https://doi.org/10.20506/rst.37.2.2809
Coertse J, Grobler CS, Sabeta CT, Seamark E, Kearney T, Paweska JT, Markotter W (2020) Lyssaviruses in Insectivorous Bats, South Africa, 2003–2018. Emerg Infect Dis 26(12):3056–3060. https://doi.org/10.3201/eid2612.203592
doi: 10.3201/eid2612.203592
pmcid: 7706942
Kissi B, Tordo N, Bourhy H (1995) Genetic polymorphism in rabies virus nucleoprotein gene. Virology 209:526–537
doi: 10.1006/viro.1995.1285
Bourhy H, Reynes JM, Dunham EJ, Dacheux L, Larrous F, Huong VTQ, Xu G, Yan J, Miranda MEG, Holmes EC (2008) The origin and phylogeography of dog rabies virus. J Gen Virol 89:2673–2681. https://doi.org/10.1099/vir.0.2008/003913-0
doi: 10.1099/vir.0.2008/003913-0
David D, Hughes GJ, Yakobson BA, Davidson I, Un H, Aylan O, Kuzmin IV, Rupprecht CE (2007) Identification of novel canine rabies virus clades in the Middle East and North Africa. J Gen Virol 88:967–980. https://doi.org/10.1099/vir.0.82352-0
doi: 10.1099/vir.0.82352-0
Talbi C, Holmes EC, de Benedictis P, Faye O, Nakouné E, Gamatié D, Diarra A, Elmamy BO, Sow A, Adjogoua EV, Sangare O, Dundon WG, Capua I, Sall AA, Bourhy H (2009) Evolutionary history and dynamics of dog rabies virus in western and central Africa. J Gen Virol 90:783–791. https://doi.org/10.1099/vir.0.007765-0
doi: 10.1099/vir.0.007765-0
Johnson N, McElhinney LM, Ali YH, Saeed IK, Fooks AR (2004) Molecular epidemiology of canid rabies in Sudan: evidence for a common origin of rabies with Ethiopia. Virus Res 104:200–205. https://doi.org/10.1016/j.virusres.2004.04.006
doi: 10.1016/j.virusres.2004.04.006
Lembo T, Haydon DT, Velasco-Villa A, Rupprecht CE, Packer C, Brandão PE, Kuzmin IV, Fooks AR, Barrat J, Cleaveland S (2007) Molecular epidemiology identifies only a single rabies virus variant circulating in complex carnivore communities of the Serengeti. Proc Biol Sci 274:2123–2130. https://doi.org/10.1098/rspb.2007.0664
doi: 10.1098/rspb.2007.0664
pmcid: 2279181
Kuzmin IV, Orciari LA, Arai YT, Smith JS, Hanlon CA, Kameoka Y, Rupprecht CE (2003) Bat lyssaviruses (Aravan and Khujand) from Central Asia: phylogenetic relationships according to N, P and G gene sequences. Virus Res 97:65–79. https://doi.org/10.1016/S0168-1702(03)00217-X
doi: 10.1016/S0168-1702(03)00217-X
Pharande RR, Majee SB, Gaikwad SS, Moregoankar SD, Bannalikar A, Doiphode A, Gandge R, Dighe D, Ingle S, Mukherjee S (2021) Evolutionary analysis of rabies virus using the partial nucleoprotein and glycoprotein gene in Mumbai region of India. J Gen Virol 102:3. https://doi.org/10.1099/jgv.0.001521 . (Epub 2021 Feb 5. PMID: 33544071)
doi: 10.1099/jgv.0.001521
Dietzschold B, Wunner WH, Wiktor TJ, Lopes AD, Lafon M, Smith CL, Koprowski H (1983) Characterization of an antigenic determinant of the glycoprotein that correlates with pathogenicity of rabies virus. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.80.1.70
doi: 10.1073/pnas.80.1.70
pmcid: 393311
Seif I, Coulon P, Rollin PE, Flamandl A (1985) Rabies virulence: effect on pathogenicity and sequence characterization of rabies virus mutations affecting antigenic site III of the glycoprotein. J Virol. https://doi.org/10.1128/JVI.53.3.926-934.1985
doi: 10.1128/JVI.53.3.926-934.1985
pmcid: 254728
Badrane H, Tordo N (2001) Host Switching in Lyssavirus History from the Chiroptera to the Carnivora Orders. J Virol 75:8096–8104. https://doi.org/10.1128/JVI.75.17.8096-8104.2001
doi: 10.1128/JVI.75.17.8096-8104.2001
pmcid: 115054
Guyatt K, Twin J, Davis P, Holmes E, Smith G, Smith I, Mackenzie J, Young PA (2003) Molecular epidemiological study of Australian bat lyssavirus. J Gen Virol 84:485–496. https://doi.org/10.1099/vir.0.18652-0
doi: 10.1099/vir.0.18652-0
Hyun BH, Lee KK, Kim IJ, Lee KW, Park HJ, Lee OS, An SH, Lee JB (2005) Molecular epidemiology of rabies virus isolates from South Korea. J Virus Res 114:113–125. https://doi.org/10.1016/j.virusres.2005.06.004
doi: 10.1016/j.virusres.2005.06.004
National Statistics Office (NSO) [Malawi]. 2018 Malawi population and housing census—main report. Zomba, Malawi, 2019. http://populationmalawi.org/wp1/wp-content/uploads/2019/10/2018-MalawiPopulation-and-Housing-Census-Main-Report-1.pdf . Accessed 25 Aug 2022
The World Bank, population, total Malawi 2020. [Internet]. https://data.worldbank.org/indicator/SP.POP.TOTL?locations=MW . Accessed 2 Dec 2021
Zimmer BL, Gamble L, Foster R, Kennedy N, Mayer D, Bailey JB, Lemon J, Langton J (2019) Assessment of the impact on paediatric rabies at Queen Elizabeth Central Hospital, Blantyre, Malawi, following a mass canine rabies vaccination programme. Int J Infect Dis 79:64. https://doi.org/10.1016/j.ijid.2018.11.165
doi: 10.1016/j.ijid.2018.11.165
Mallewa M, Fooks AR, Banda D, Chikungwa P, Mankhambo L, Molyneux E, Molyneux ME, Solomon T (2007) Rabies encephalitis in malaria-endemic area, Malawi, Africa. Emerg Infect Dis 13:136–139. https://doi.org/10.3201/eid1301.060810
doi: 10.3201/eid1301.060810
pmcid: 2725806
Sánchez-Soriano C, Gibson AD, Gamble L, Bailey JLB, Mayer D, Lohr F, Chikungwa P, Chulu J, Handel IG, Bronsvoort BMD, Mellanby RJ, Mazeri S (2020) Implementation of a mass canine rabies vaccination campaign in both rural and urban regions in southern Malawi. PLoS Negl Trop Dis 23(14):e0008004. https://doi.org/10.1371/journal.pntd.0008004
doi: 10.1371/journal.pntd.0008004
Burdon BJL, Gamble L, Gibson AD, Bronsvoort BMD, Handel IG, Mellanby RJ (2018) A rabies lesson improves rabies knowledge amongst primary school children in Zomba, Malawi. PLoS Negl Trop Dis. 12:e0006293. https://doi.org/10.1371/journal.pntd.0006293
doi: 10.1371/journal.pntd.0006293
Depani SJ, Kennedy N, Mallewa M, Molyneux EM (2012) Case report: evidence of rise in rabies cases in Southern Malawi—better preventative measures are urgently required. Malawi Med J 24:61–64
pmcid: 3576828
SEARG (2014) Rabies in Mozambique: update. https://www.who.int/rabies/epidemiology/Rabies_CP_Mozambique_09_2014.pdf . Accessed 10 Mar 2022
Lembo T, Hampson K, Haydon DT, Craft M, Dobson A, Dushoff J, Ernest E, Hoare R, Kaare M, Mlengeya T, Mentzel C, Cleaveland S (2008) Exploring reservoir dynamics: a case study of rabies in the Serengeti ecosystem. J Appl Ecol 45(4):1246–1257. https://doi.org/10.1111/j.1365-2664.2008.01468.x
doi: 10.1111/j.1365-2664.2008.01468.x
pmcid: 3303133
Mazeri S, Gibson AD, Meunier N, Bronsvoort BMD, Handel IG, Mellanby RJ, Gamble L (2018) Barriers of attendance to dog rabies static point vaccination clinics in Blantyre, Malawi. PLoS Negl Trop Dis 12:e0006159. https://doi.org/10.1371/journal.pntd.0006159
doi: 10.1371/journal.pntd.0006159
pmcid: 5783422
Kamolvarin N, Tirawatnpong T, Rattanasiwamoke R, Tirawatnpong S, Panpanich T, Hemachudha T (1993) Diagnosis of rabies by polymerase chain reaction with nested primers. J Infect Dis 167:207–210. https://doi.org/10.1093/infdis/167.1.207
doi: 10.1093/infdis/167.1.207
Tamura K, Stecher G, Peterson D, Peterson FA (2013) MEGA 6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
doi: 10.1093/molbev/mst197
pmcid: 3840312
Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol Biol Evol 9:678–687
Felsenstein J (1982) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
doi: 10.1111/j.1558-5646.1985.tb00420.x
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452 (pmid:19346325)
doi: 10.1093/bioinformatics/btp187
Scott T, Coetzer A, de Balogh K, Wright N, Nel L (2015) The Pan-African rabies control network (PARACON): a unified approach to eliminating canine rabies in Africa. Antivir Res 124:93–100. https://doi.org/10.1016/j.antiviral.2015.10.002
doi: 10.1016/j.antiviral.2015.10.002
Jarvis S (2016) One health. Aiming for elimination of dog-mediated human rabies cases by 2030. Vet Rec 178:86–87. https://doi.org/10.1136/vr.i51
doi: 10.1136/vr.i51
Edelsten RM (1995) Epidemiology and control of rabies in Malawi. Trop Anim Health Prod 27:155–163
doi: 10.1007/BF02248961
Department of Animal Health and Livestock Development, Ministry of Agriculture. National Livestock Development Policy, 2017–2022. 2017, Lilongwe, Malawi
Nel LH, Rupprecht CE (2007) Emergence of lyssaviruses in the Old World: the case of Africa. Curr Top Microbiol Immunol 315:161–193
Hirano S, Sato G, Kobayashi Y, Itou T, Luo RT, Liu Q, Jin NY, Xuan X (2010) Analysis of Chinese rabies virus isolates from 2003–2007 based on P and M protein genes. Acta Virol 54:91–98
doi: 10.4149/av_2010_02_91
Cohen C, Sartorius B, Sabeta C, Zulu G, Paweska J, Mogoswane M, Sutton C, Nel LH, Swanepoel R, Leman PA, Grobbelaar AA, Dyason E, Blumberg L (2007) Epidemiology and molecular virus characterization of re-emerging rabies, South Africa. Emerg Infect Dis 13:1879–1886. https://doi.org/10.3201/eid1312.070836
doi: 10.3201/eid1312.070836
pmcid: 2874428
World Health Organization WHO rabies epidemiology; 2012. http://www.who.int/entity/rabies/rabies_maps/en/index.html . Accessed 9 Dec 2021
Coetzer A, Coertse J, Makalo MJ, Molomo M, Markotter W, Nel LH (2017) Epidemiology of rabies in Lesotho: the importance of routine surveillance and virus characterization. Trop Med Infect Dis 2:30. https://doi.org/10.3390/tropicalmed2030030
doi: 10.3390/tropicalmed2030030
pmcid: 6082089