Spatial and temporal dynamic analysis of rabies: A review of current methodologies

Rabies continues to be one of the deadliest, high risk diseases worldwide, posing a severe threat to public health. The lack of human-to-human transmission means that the spread of rabies is not significantly affected by the distribution of humans or migra- tion. Thus, the spatiotemporal dynamic of cases in both wild and domestic animals is an important issue that can result in human cases. This paper gives an overview of the methodologies for the spatial and temporal dynamic analysis of this disease. It introduces the most representative research progress of spatial aggregation, dynamic transmission, spatiotemporal distribution, epidemiologi- cal analysis and application of modelling in the study of rabies transmission in recent years. This overview should be useful for investigating the spatial and temporal dynamics of rabies, as it could help understanding the spread of cases as well as contribute to the development of better prevention and control strategies in ecology and epidemiology.

Abdrakhmanov SK, Beisembayev KK, Кorennoy FI, Yessembekova GN, Кushubaev DB, Кadyrov AS, 2016. Revealing spatio-temporal patterns of rabies spread among various categories of animals in the Republic of Kazakhstan, 2010-2013. Geospat Health 11:199-205. DOI: https://doi.org/10.4081/gh.2016.455

Alegria-Moran R, Miranda D, Barnard M, Parra A, Lapierre L, 2017. Characterization of the epidemiology of bat-borne rabies in Chile between 2003 and 2013. Prev Vet Med 143:30-38. DOI: https://doi.org/10.1016/j.prevetmed.2017.05.012

Anselin L, 1995. Local indicators of spatial association-LISA. Geogr Anal 27:93-115. DOI: https://doi.org/10.1111/j.1538-4632.1995.tb00338.x

Arias-Orozco P, Bástida-González F, Cruz L, Villatoro J, Espinoza E, Zárate-Segura PB, Recuenco S, 2018. Spatiotemporal analysis of canine rabies in El Salvador: Violence and poverty as social factors of canine rabies. PLoS One 13:e0201305. DOI: https://doi.org/10.1371/journal.pone.0201305

Bárcenas-Reyes I, Nieves-Martínez DP, Cuador-Gil JQ, Loza-Rubio E, González-Ruiz S, Cantó-Alarcón GJ, Milián-Suazo F, 2019. Spatiotemporal analysis of rabies in cattle in central Mexico. Geospat Health 14:247-253. DOI: https://doi.org/10.4081/gh.2019.805

Beran GW 1994. Rabies and infections by rabies-related viruses. Handbook of zoonoses. CRC press.

Biek R, Henderson JC, Waller LA, Rupprecht CE, Real LA, 2007. A high-resolution genetic signature of demographic and spatial expansion in epizootic rabies virus. PNAS 104:7993-7998. DOI: https://doi.org/10.1073/pnas.0700741104

Binder K, Heermann D, Roelofs L, Mallinckrodt AJ, Mckay S, 1993. Monte Carlo simulation in statistical physics. Computers in Physics 7:156-157. DOI: https://doi.org/10.1063/1.4823159

Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A, Heled J, Jones G, Kühnert D, De Maio N, 2019. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comp Biol 15:e1006650. DOI: https://doi.org/10.1371/journal.pcbi.1006650

Bourhy H, Nakouné E, Hall M, Nouvellet P, Lepelletier A, Talbi C, Watier L, Holmes EC, Cauchemez S, Lemey P, 2016. Revealing the micro-scale signature of endemic zoonotic disease transmission in an African urban setting. PLoS Path 12:e1005525. DOI: https://doi.org/10.1371/journal.ppat.1005525

Bouslama Z, Belkhiria JA, Turki I, Kharmachi H, 2020. Spatio-temporal evolution of canine rabies in Tunisia, 2011–2016. Prev Vet Med 185:105195. DOI: https://doi.org/10.1016/j.prevetmed.2020.105195

Breslow N, 1970. A generalized Kruskal-Wallis test for comparing K samples subject to unequal patterns of censorship. Biometrika 57:579-594. DOI: https://doi.org/10.1093/biomet/57.3.579

Brockwell PJ, Davis RA 2002. Introduction to time series and forecasting, Springer. DOI: https://doi.org/10.1007/b97391

Brookes VJ, Gill G, Singh C, Sandhu B, Dhand N, Singh B, Gill J, Ward M, 2018. Exploring animal rabies endemicity to inform control programmes in Punjab, India. Zoonoses Public Health 65:e54-e65. DOI: https://doi.org/10.1111/zph.12409

Brunker K, Lemey P, Marston DA, Fooks AR, Lugelo A, Ngeleja C, Hampson K, Biek R, 2018a. Landscape attributes governing local transmission of an endemic zoonosis: Rabies virus in domestic dogs. Mol Ecol 27:773-788. DOI: https://doi.org/10.1111/mec.14470

Brunker K, Nadin-Davis S, Biek R, 2018b. Genomic sequencing, evolution and molecular epidemiology of rabies virus. Rev Sci Tech 37:401-408. DOI: https://doi.org/10.20506/rst.37.2.2810

Cavalcante KKDS, Florêncio CMGD, Moreno JDO, Correia FGS, Alencar CH, 2019. Post-exposure human rabies prophylaxis: spatial patterns of inadequate procedures in Ceará-Brazil, 2007 to 2015. Rev Soc Bras Med Trop 53:e20190247. DOI: https://doi.org/10.1590/0037-8682-0247-2019

Clark PJ, Evans FC, 1954. Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35:445-453. DOI: https://doi.org/10.2307/1931034

De Andrade FA, Gomes MN, Uieda W, Begot AL, Ramos ODS, Fernandes ME, 2016. Geographical analysis for detecting high-risk areas for bovine/human rabies transmitted by the common hematophagous bat in the Amazon region, Brazil. PLoS One 11:e0157332. DOI: https://doi.org/10.1371/journal.pone.0157332

Dellicour S, Rose R, Pybus OG, 2016. Explaining the geographic spread of emerging epidemics: a framework for comparing viral phylogenies and environmental landscape data. BMC Bioinformatics 17:1-12. DOI: https://doi.org/10.1186/s12859-016-0924-x

Dhand NK, Ward MP, 2012. Anthropogenic and environmental risk factors for rabies occurrence in Bhutan. Prev Vet Med 107:21-26. DOI: https://doi.org/10.1016/j.prevetmed.2012.05.003

Dos Santos AJF, Ferreira JM, Baptista F, Alexandrino B, Da Silva MaG, Gomes JEC, Júnior JPV, Tavares RM, De Sousa Almeida K, 2022. Statistical analysis between 2006 and 2019 and forecast of rabies in cattle from 2020 to 2022 in Tocantins State (Brazil), by using the R Studio software. Epidemiol Infect 150:1-7. DOI: https://doi.org/10.1017/S0950268822000553

Drummond AJ, Rambaut A, 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:1-8. DOI: https://doi.org/10.1186/1471-2148-7-214

Eckardt M, Freuling C, Müller T, Selhorst T, 2015. Spatio-temporal analysis of fox rabies cases in Germany 2005-2006. Geospat Health 10:313. DOI: https://doi.org/10.4081/gh.2015.313

Elliot P, Wakefield JC, Best NG, Briggs DJ 2000. Spatial epidemiology: methods and applications, Oxford University Press. DOI: https://doi.org/10.1093/acprof:oso/9780198515326.001.0001

Escobar L, Restif O, Yung V, Favi M, Pons D, Medina-Vogel G, Infection, 2015. Spatial and temporal trends of bat-borne rabies in Chile. Epidemiol Infect 143:1486-1494. DOI: https://doi.org/10.1017/S095026881400226X

Feng Y, Wang Y, Xu W, Tu Z, Liu T, Huo M, Liu Y, Gong W, Zeng Z, Wang W, 2020. Animal rabies surveillance, China, 2004–2018. Emerging Infect Dis 26:2825. DOI: https://doi.org/10.3201/eid2612.200303

Fooks AR, Banyard AC, Horton DL, Johnson N, Mcelhinney LM, Jackson AC, 2014. Current status of rabies and prospects for elimination. Lancet 384:1389-1399. DOI: https://doi.org/10.1016/S0140-6736(13)62707-5

Gabriele-Rivet V, Arsenault J, Brookes VJ, Fleming PJ, Nury C, Ward MP, 2020. Dingo density estimates and movements in equatorial Australia: Spatially explicit mark–resight models. Animals 10:865. DOI: https://doi.org/10.3390/ani10050865

Gabriele-Rivet V, Ward MP, Arsenault J, London D, Brookes VJ, 2021. Could a rabies incursion spread in the northern Australian dingo population? Development of a spatial stochastic simulation model. PLoS Negl Trop Dis 15:e0009124. DOI: https://doi.org/10.1371/journal.pntd.0009124

Geary RC, 1954. The contiguity ratio and statistical mapping. The Incorporated Statistician 5:115-146. DOI: https://doi.org/10.2307/2986645

Getis A, Ord JK 2010. The analysis of spatial association by use of distance statistics. Perspectives on spatial data analysis. Springer. DOI: https://doi.org/10.1111/j.1538-4632.1992.tb00261.x

Gong W, Jiang Y, Za Y, Zeng Z, Shao M, Fan J, Sun Y, Xiong Z, Yu X, Tu C, 2010. Temporal and spatial dynamics of rabies viruses in China and Southeast Asia. Virus Res 150:111-118. DOI: https://doi.org/10.1016/j.virusres.2010.02.019

Guerra MA, Curns AT, Rupprecht CE, Hanlon CA, Krebs JW, Childs JE, 2003. Skunk and raccoon rabies in the eastern United States: temporal and spatial analysis. Emerging Infect Dis 9:1143. DOI: https://doi.org/10.3201/eid0909.020608

Guo D, Yin W, Yu H, Thill J-C, Yang W, Chen F, Wang D, 2018a. The role of socioeconomic and climatic factors in the spatio-temporal variation of human rabies in China. BMC Infect Dis 18:1-13. DOI: https://doi.org/10.1186/s12879-018-3427-8

Guo D, Zhou H, Zou Y, Yin W, Yu H, Si Y, Li J, Zhou Y, Zhou X, Magalhães RJS, 2013. Geographical analysis of the distribution and spread of human rabies in China from 2005 to 2011. PLoS One 8:e72352. DOI: https://doi.org/10.1371/journal.pone.0072352

Guo D, Zhu Y, Yin W, 2018b. OSCAR: a framework to integrate spatial computing ability and data aggregation for emergency management of public health. GeoInformatica 22:383-410. DOI: https://doi.org/10.1007/s10707-017-0308-z

Hampson K, Coudeville L, Lembo T, Sambo M, Kieffer A, Attlan M, Barrat J, Blanton JD, Briggs DJ, Cleaveland S, 2015. Estimating the global burden of endemic canine rabies. PLoS Negl Trop Dis 9:e0003709. DOI: https://doi.org/10.1371/journal.pntd.0003709

Hassine TB, Ali MB, Ghodhbane I, Said ZB, Hammami S, 2021. Rabies in Tunisia: a spatio-temporal analysis in the region of CapBon-Nabeul. Acta Tropica 216:105822. DOI: https://doi.org/10.1016/j.actatropica.2021.105822

Heeney J, 2006. Zoonotic viral diseases and the frontier of early diagnosis, control and prevention. J Intern Med 260:399-408. DOI: https://doi.org/10.1111/j.1365-2796.2006.01711.x

Hemachudha T, Laothamatas J, Rupprecht CE, 2002. Human rabies: a disease of complex neuropathogenetic mechanisms and diagnostic challenges. Lancet Neurol 1:101-109. DOI: https://doi.org/10.1016/S1474-4422(02)00041-8

Hikufe EH, Freuling CM, Athingo R, Shilongo A, Ndevaetela E-E, Helao M, Shiindi M, Hassel R, Bishi A, Khaiseb S, 2019. Ecology and epidemiology of rabies in humans, domestic animals and wildlife in Namibia, 2011-2017. PLoS Negl Trop Dis 13:e0007355. DOI: https://doi.org/10.1371/journal.pntd.0007355

Hussain MH, Ward MP, Body M, Al-Rawahi A, Wadir AA, Al-Habsi S, Saqib M, Ahmed MS, Almaawali MG, 2013. Spatio-temporal pattern of sylvatic rabies in the Sultanate of Oman, 2006–2010. Prev Vet Med 110:281-289. DOI: https://doi.org/10.1016/j.prevetmed.2013.01.001

Kalthoum S, Guesmi K, Gharbi R, Baccar MN, Seghaier C, Zrelli M, Bahloul C, 2021. Temporal and spatial distributions of animal and human rabies cases during 2012 and 2018, in Tunisia. Vet Med Sci 7:686-696. DOI: https://doi.org/10.1002/vms3.438

Kanankege KS, Errecaborde KM, Wiratsudakul A, Wongnak P, Yoopatthanawong C, Thanapongtharm W, Alvarez J, Perez A, 2022. Identifying high-risk areas for dog-mediated rabies using Bayesian spatial regression. One Health 15:100411. DOI: https://doi.org/10.1016/j.onehlt.2022.100411

Kaplan C, Turner G, Warrell DA 1986. Rabies, the facts, Oxford University Press.

Karunanayake D, Matsumoto T, Wimalaratne O, Nanayakkara S, Perera D, Nishizono A, Ahmed K, 2014. Twelve years of rabies surveillance in Sri Lanka, 1999–2010. PLoS Negl Trop Dis 8:e3205. DOI: https://doi.org/10.1371/journal.pntd.0003205

Kermack WO, Mckendrick AG, 1927. A contribution to the mathematical theory of epidemics. Proc R Soc London 115:700-721. DOI: https://doi.org/10.1098/rspa.1927.0118

Knobel DL, Cleaveland S, Coleman PG, Fèvre EM, Meltzer MI, Miranda MEG, Shaw A, Zinsstag J, Meslin F-X, 2005. Re-evaluating the burden of rabies in Africa and Asia. Bull WHO 83:360-368.

Knox EG, Bartlett MS, 1964. The detection of space-time interactions. J R Stat Soc Ser C Appl Stat 13:25-30. DOI: https://doi.org/10.2307/2985220

Kulldorff M, 1997. A spatial scan statistic. Commun Stat Theory Methods 26:1481-1496. DOI: https://doi.org/10.1080/03610929708831995

Kulldorff M, Heffernan R, Hartman J, Assunçao R, Mostashari F, 2005. A space–time permutation scan statistic for disease outbreak detection. PLoS Med 2:e59. DOI: https://doi.org/10.1371/journal.pmed.0020059

Kulldorff M, Huang L, Pickle L, Duczmal L, 2006. An elliptic spatial scan statistic. Stat Med 25: 3929-3943. DOI: https://doi.org/10.1002/sim.2490

Laager M, Mbilo C, Madaye EA, Naminou A, Léchenne M, Tschopp A, Naïssengar SK, Smieszek T, Zinsstag J, Chitnis N, 2018. The importance of dog population contact network structures in rabies transmission. PLoS Negl Trop Dis 12:e0006680. DOI: https://doi.org/10.1371/journal.pntd.0006680

Lee J, Wong DW 2001. Statistical analysis with ArcView GIS, John Wiley & Sons.

Mchugh ML, 2013. The chi-square test of independence. Biochemia Medica 23:143-149. DOI: https://doi.org/10.11613/BM.2013.018

Mitmoonpitak C, Tepsumethanon V, Wilde H, 1998. Rabies in Thailand. Epidemiol Infect 120:165-169. DOI: https://doi.org/10.1017/S0950268897008601

Mogano K, Suzuki T, Mohale D, Phahladira B, Ngoepe E, Kamata Y, Chirima G, Sabeta C, Makita K, 2022. Spatio-temporal epidemiology of animal and human rabies in northern South Africa between 1998 and 2017. PLoS Negl Trop Dis 16:e0010464. DOI: https://doi.org/10.1371/journal.pntd.0010464

Mollentze N, Nel LH, Townsend S, Le Roux K, Hampson K, Haydon DT, Soubeyrand S, 2014. A Bayesian approach for inferring the dynamics of partially observed endemic infectious diseases from space-time-genetic data. Proc R Soc Ser B Biol Sci 281:20133251. DOI: https://doi.org/10.1098/rspb.2013.3251

Mondul AM, Krebs JW, Childs JE, 2003. Trends in national surveillance for rabies among bats in the United States (1993-2000). J Am Vet Med Assoc 222:633-639. DOI: https://doi.org/10.2460/javma.2003.222.633

Moran PA, 1950. Notes on continuous stochastic phenomena. Biometrika 37:17-23. DOI: https://doi.org/10.1093/biomet/37.1-2.17

Mshelbwala P, Weese S, Mamun A, Magalhaes R, 2020. Global spatial epidemiology of rabies: Systematic review and critical appraisal of methods. Int J Infect Dis 101:321. DOI: https://doi.org/10.1016/j.ijid.2020.09.839

Mulatti P, Ferrã N, Patregnani T, Bonfanti L, Marangon S, 2011. Geographical information systems in the management of the 2009-2010 emergency oral anti-rabies vaccination of foxes in north-eastern Italy. Geospat Health 5:217-226. DOI: https://doi.org/10.4081/gh.2011.174

Müller TF, Schröder R, Wysocki P, Mettenleiter TC, Freuling CM, 2015. Spatio-temporal use of oral rabies vaccines in fox rabies elimination programmes in Europe. PLoS Negl Trop Dis 9:e0003953. DOI: https://doi.org/10.1371/journal.pntd.0003953

Nahata KD, Bollen N, Gill MS, Layan M, Bourhy H, Dellicour S, Baele G, 2021. On the use of phylogeographic inference to infer the dispersal history of rabies virus: a review study. Viruses 13:1628. DOI: https://doi.org/10.3390/v13081628

Oliveira FaS, Castro RJS, De Oliveira JF, Barreto FM, Farias MPO, Marinho GLDOC, Dos Santos Soares MJ, Silva-Júnior A, Schwarz DGG, 2022. Geographical and temporal spread of equine rabies in Brazil. Acta Trop 227:106302. DOI: https://doi.org/10.1016/j.actatropica.2022.106302

Olugasa BO, Aiyedun J, Akingbogun AA, 2009. Identification of geographic risk factors associated with clinical human rabies in a transit city of Nigeria. Epizoot Anim Health West Afr 5:43-52.

Ord JK, Getis A, 1995. Local spatial autocorrelation statistics: distributional issues and an application. Geogr Anal 27:286-306. DOI: https://doi.org/10.1111/j.1538-4632.1995.tb00912.x

Ortega-Sánchez R, Bárcenas-Reyes I, Cantó-Alarcón GJ, Luna-Cozar J, E R-A, Contreras-Magallanes YG, González-Ruiz S, Cortez-García B, Milián-Suazo F, 2022. Descriptive and Time-Series Analysis of Rabies in Different Animal Species in Mexico. Front Vet Sci 9:800735. DOI: https://doi.org/10.3389/fvets.2022.800735

Oviedo-Pastrana ME, Oliveira CS, Capanema RO, Nicolino RR, Oviedo-Socarras TJ, Haddad JPA, 2015. Trends in animal rabies surveillance in the endemic state of Minas Gerais, Brazil. PLoS Negl Trop Dis 9:e0003591. DOI: https://doi.org/10.1371/journal.pntd.0003591

Polupan I, Bezymennyi M, Gibaliuk Y, Drozhzhe Z, Rudoi O, Ukhovskyi V, Nedosekov V, De Nardi M, 2019. An analysis of rabies incidence and its geographic spread in the buffer area among orally vaccinated wildlife in Ukraine from 2012 to 2016. Front Vet Sci 6:290. DOI: https://doi.org/10.3389/fvets.2019.00290

Polupan I, Bezymennyi M, Golik M, Drozhzhe Z, Nychyk S, Nedosekov V, 2017. Spatial and temporal patterns of enzootic rabies on the territory of Chernihiv oblast of Ukraine. J Vet Med Biotechnol Biosafety 6:31-36.

Raghavan RK, Hanlon CA, Goodin DG, Davis R, Moore M, Moore S, Anderson GA, 2016. Bayesian spatiotemporal pattern and eco-climatological drivers of striped skunk rabies in the North Central Plains. PLoS Negl Trop Dis 10:e0004632. DOI: https://doi.org/10.1371/journal.pntd.0004632

Real LA, Henderson JC, Biek R, Snaman J, Jack TL, Childs JE, Stahl E, Waller L, Tinline R, Nadin-Davis S, 2005. Unifying the spatial population dynamics and molecular evolution of epidemic rabies virus. PNAS 102:12107-12111. DOI: https://doi.org/10.1073/pnas.0500057102

Rees EE, Pond BA, Tinline RR, Bélanger D, 2013. Modelling the effect of landscape heterogeneity on the efficacy of vaccination for wildlife infectious disease control. J Appl Ecol 50:881-891. DOI: https://doi.org/10.1111/1365-2664.12101

Saleh AY, Medang SA, Ibrahim AO. Rabies outbreak prediction using deep learning with long short-term memory. International Conference of Reliable Information and Communication Technology, 2019. Springer, 330-340. DOI: https://doi.org/10.1007/978-3-030-33582-3_32

Seetahal JF, Sanchez-Vazquez MJ, Vokaty A, Carrington CV, Mahabir R, Adesiyun AA, Rupprecht CE, 2019. Of bats and livestock: The epidemiology of rabies in Trinidad, West Indies. Vet Microbiol 228:93-100. DOI: https://doi.org/10.1016/j.vetmic.2018.11.020

Skellam JG, 1952. Studies in statistical ecology: I. Spatial pattern. Biometrika 39:346-362. DOI: https://doi.org/10.1093/biomet/39.3-4.346

Smith D, Waller L, Russell C, Childs J, Real L, 2005. Assessing the role of long-distance translocation and spatial heterogeneity in the raccoon rabies epidemic in Connecticut. Prev Vet Med 71:225-240. DOI: https://doi.org/10.1016/j.prevetmed.2005.07.009

Smith DL, Lucey B, Waller LA, Childs JE, Real LA, 2002. Predicting the spatial dynamics of rabies epidemics on heterogeneous landscapes. PNAS 99:3668-3672. DOI: https://doi.org/10.1073/pnas.042400799

Song M, Tang Q, Rayner S, Tao X-Y, Li H, Guo Z-Y, Shen X-X, Jiao W-T, Fang W, Wang J, 2014. Human rabies surveillance and control in China, 2005–2012. BMC Infect Dis 14:1-9. DOI: https://doi.org/10.1186/1471-2334-14-212

Talbi C, Lemey P, Suchard MA, Abdelatif E, Elharrak M, Jalal N, Faouzi A, Echevarría JE, Vazquez Moron S, Rambaut A, 2010. Phylodynamics and human-mediated dispersal of a zoonotic virus. PLoS Path 6:e1001166. DOI: https://doi.org/10.1371/journal.ppat.1001166

Thanapongtharm W, Suwanpakdee S, Chumkaeo A, Gilbert M, Wiratsudakul A, 2021. Current characteristics of animal rabies cases in Thailand and relevant risk factors identified by a spatial modeling approach. PLoS Negl Trop Dis 15:e0009980. DOI: https://doi.org/10.1371/journal.pntd.0009980

Tobler WR, 1970. A computer movie simulating urban growth in the Detroit region. Econ Geogr 46:234-240. DOI: https://doi.org/10.2307/143141

Touihri L, Zaouia I, Elhili K, Dellagi K, Bahloul C, 2011. Evaluation of mass vaccination campaign coverage against rabies in dogs in Tunisia. Zoonoses Public Health 58:110-118. DOI: https://doi.org/10.1111/j.1863-2378.2009.01306.x

Twabela AT, Mweene AS, Masumu JM, Muma JB, Lombe BP, Hankanga C, 2016. Overview of animal rabies in Kinshasa Province in the Democratic Republic of Congo. PLoS One 11:e0150403. DOI: https://doi.org/10.1371/journal.pone.0150403

Wallace RM, Gilbert A, Slate D, Chipman R, Singh A, Wedd C, Blanton JD, 2014. Right place, wrong species: a 20-year review of rabies virus cross species transmission among terrestrial mammals in the United States. PLoS One 9:e107539. DOI: https://doi.org/10.1371/journal.pone.0107539

Ward MP, 2014. Rabies in the Dutch East Indies a century ago–a spatio-temporal case study in disease emergence. Prev Vet Med 114:11-20. DOI: https://doi.org/10.1016/j.prevetmed.2014.01.009

Wheeler DC, Waller LA, 2008. Mountains, valleys, and rivers: the transmission of raccoon rabies over a heterogeneous landscape. J Agric Biol Environ Stat 13:388-406. DOI: https://doi.org/10.1198/108571108X383483

Wilson ML, Bretsky PM, Cooper Jr GH, Egbertson SH, Van Kruiningen HJ, Cartter ML, 1997. Emergence of raccoon rabies in Connecticut, 1991-1994: spatial and temporal characteristics of animal infection and human contact. Am J Trop Med Hyg 57:457-463. DOI: https://doi.org/10.4269/ajtmh.1997.57.457

Yao H-W, Yang Y, Liu K, Li X-L, Zuo S-Q, Sun R-X, Fang L-Q, Cao W-C, 2015. The spatiotemporal expansion of human rabies and its probable explanation in mainland China, 2004-2013. PLoS Negl Trop Dis 9:e0003502. DOI: https://doi.org/10.1371/journal.pntd.0003502

Yin C-P, Zhou H, Wu H, Tao X-Y, Rayner S, Wang S-M, Tang Q, Liang G-D, 2012. Analysis on factors related to rabies epidemic in China from 2007–2011. Virol Sin 27: 132-143. DOI: https://doi.org/10.1007/s12250-012-3244-y

Yu J, Li H, Tang Q, Rayner S, Han N, Guo Z, Liu H, Adams J, Fang W, Tao X, 2012. The spatial and temporal dynamics of rabies in China. PLoS Negl Trop Dis 6:e1640. DOI: https://doi.org/10.1371/journal.pntd.0001640

Yu J, Xiao H, Yang W, Dellicour S, Kraemer MU, Liu Y, Cai J, Huang ZX, Zhang Y, Feng Y, 2020. The impact of anthropogenic and environmental factors on human rabies cases in China. Transbound Emerg Dis 67:2544-2553. DOI: https://doi.org/10.1111/tbed.13600

Zar JH 1999. Biostatistical analysis, Pearson Education India.

Zhang H-L, Zhang Y-Z, Yang W-H, Tao X-Y, Li H, Ding J-C, Feng Y, Yang D-J, Zhang J, He J, 2014. Molecular epidemiology of reemergent rabies in Yunnan Province, southwestern China. Emerging Infect Dis 20: 1433. DOI: https://doi.org/10.3201/eid2009.130440

Zhang J, Jin Z, Sun G-Q, Sun X-D, Ruan S, 2012a. Modeling seasonal rabies epidemics in China. Bull. Math. Biol. 74: 1226-1251. DOI: https://doi.org/10.1007/s11538-012-9720-6

Zhang J, Jin Z, Sun G-Q, Zhou T, Ruan S, 2011. Analysis of rabies in China: transmission dynamics and control. PLoS One 6:e20891. DOI: https://doi.org/10.1371/journal.pone.0020891

Zhang J, Jin Z, Sun G, Sun X, Ruan S, 2012b. Spatial spread of rabies in China. J Appl Anal Comput 2: 111-126. DOI: https://doi.org/10.11948/2012008

Zhou H, Vong S, Liu K, Li Y, Mu D, Wang L, Yin W, Yu H, 2016. Human rabies in China, 1960-2014: a descriptive epidemiological study. PLoS Negl Trop Dis 10:e0004874. DOI: https://doi.org/10.1371/journal.pntd.0004874

Zhu WY, Liang GD, 2012. Current status of canine rabies in China. Biomed Environ Sci 25:602-605.