Predictors of free-roaming domestic dogs’ contact network centrality and their relevance for rabies control

Warembourg C., Fournié G., Abakar M.F., Alvarez D., Berger-González M., Odoch T., Wera E., Alobo G., Carvallo E.T.L., Bal V.D., López Hernandez A.L., Madaye E., Maximiano Sousa F., Naminou A., Roquel P., Hartnack S., Zinsstag J., Dürr S.

Veterinary Public Health Institute, Vetsuisse Faculty, University of Bern, Bern, Switzerland; Royal Veterinary College, University of London, London, United Kingdom; Institut de Recherche en Elevage pour le Développement, N’Djaména, Chad; Universidad del Valle de Guatemala, Guatemala City, Guatemala; Swiss Tropical and Public Health Institute, Basel, Switzerland; College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, Kampala, Uganda; Kupang State Agricultural Polytechnic (Politeknik Pertanian Negeri Kupang), West Timor, Indonesia; Animal Health Division, Agricultural Department of Sikka Regency, Flores, Indonesia; Section of Epidemiology, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland


Abstract

Free roaming domestic dogs (FRDD) are the main vectors for rabies transmission to humans worldwide. To eradicate rabies from a dog population, current recommendations focus on random vaccination with at least 70% coverage. Studies suggest that targeting high-risk subpopulations could reduce the required vaccination coverage, and increase the likelihood of success of elimination campaigns. The centrality of a dog in a contact network can be used as a measure of its potential contribution to disease transmission. Our objectives were to investigate social networks of FRDD in eleven study sites in Chad, Guatemala, Indonesia and Uganda, and to identify characteristics of dogs, and their owners, associated with their centrality in the networks. In all study sites, networks had small-world properties and right-skewed degree distributions, suggesting that vaccinating highly connected dogs would be more effective than random vaccination. Dogs were more connected in rural than urban settings, and the likelihood of contacts was negatively correlated with the distance between dogs’ households. While heterogeneity in dog’s connectedness was observed in all networks, factors predicting centrality and likelihood of contacts varied across networks and countries. We therefore hypothesize that the investigated dog and owner characteristics resulted in different contact patterns depending on the social, cultural and economic context. We suggest to invest into understanding of the sociocultural structures impacting dog ownership and thus driving dog ecology, a requirement to assess the potential of targeted vaccination in dog populations. © 2021, The Author(s).


Journal

Scientific Reports

Publisher: Nature Research

Volume 11, Issue 1, Art No 12898, Page – , Page Count


Journal Link: https://www.scopus.com/inward/record.uri?eid=2-s2.0-85108147421&doi=10.1038%2fs41598-021-92308-7&partnerID=40&md5=b803d30ffdb0f3a4a8befb31800f591c

doi: 10.1038/s41598-021-92308-7

Issn: 20452322

Type: All Open Access, Gold, Green


References

Bouli, F.P.N.O., Awah-Ndukum, J., Mingoas, K.J.P., Tejiokem, M.C., Tchoumboue, J., Dog demographics and husbandry practices related with rabies in Cameroon (2020) Trop. Anim. Health Prod., 52, pp. 979-987. , PID: 31741308; Van Kesteren, F., Dog ownership, dog behaviour and transmission of Echinococcus spp. in the Alay Valley, southern Kyrgyzstan (2013) Parasitology, 140, pp. 1674-1684. , PID: 23985326; Pulczer, A.S., Jones-Bitton, A., Waltner-Toews, D., Dewey, C.E., Owned dog demography in Todos Santos Cuchumatán, Guatemala (2013) Prev. Vet. Med., 108, pp. 209-217. , PID: 22906504; Czupryna, A.M., Ecology and demography of free-roaming domestic dogs in rural villages near serengeti national park in Tanzania (2016) PLoS ONE, 11, pp. 1-24. , COI: 1:CAS:528:DC%2BC2sXhsFelu7bK; Ratsitorahina, M., Dog ecology and demography in Antananarivo, 2007 (2009) BMC Vet. Res., 5, pp. 1-7; Muthiani, Y., Traoré, A., Mauti, S., Zinsstag, J., Hattendorf, J., Low coverage of central point vaccination against dog rabies in Bamako, Mali (2015) Prev. Vet. Med., 120, pp. 203-209. , PID: 25953653; Touihri, L., Zaouia, I., Elhili, K., Dellagi, K., Bahloul, C., Evaluation of mass vaccination campaign coverage against rabies in dogs in Tunisia (2011) Zoonoses Public Health, 58, pp. 110-118. , COI: 1:STN:280:DC%2BC3M7nvFWluw%3D%3D, PID: 20042063; Matter, H.C., Wandeler, A.I., Neuenschwander, B.E., Harischandra, L.P.A., Meslin, F.X., Study of the dog population and the rabies control activities in the Mirigama area of Sri Lanka (2000) Acta Trop., 75, pp. 95-108. , COI: 1:STN:280:DC%2BD3c7ntVartg%3D%3D, PID: 10708011; Gsell, A.S., Domestic dog demographic structure and dynamics relevant to rabies control planning in urban areas in Africa: The case of Iringa, Tanzania (2012) BMC Vet. Res., 8, p. 236. , PID: 23217194; Kayali, U., Coverage of pilot parenteral vaccination campaign against canine rabies in N’Djaména, Chad (2003) Bull. World Health Organ., 81, pp. 739-744. , COI: 1:STN:280:DC%2BD2c%2FlvFyktg%3D%3D, PID: 14758434; Durr, S., Effectiveness of dog rabies vaccination programmes: Comparison of owner-charged and free vaccination campaigns (2009) Epidemiol. Infect., 137, pp. 1558-1567. , COI: 1:STN:280:DC%2BD1MnislaqtA%3D%3D, PID: 19327197; Hossain, M., A survey of the dog population in rural Bangladesh (2013) Prev. Vet. Med., 111, pp. 134-138. , PID: 23590964; Sudarshan, M.K., Mahendra, B.J., Narayan, D.H., A community survey of dog bites, anti-rabies treatment, rabies and dog population management in Bangalore city (2001) J. Commun. Dis., 33, pp. 245-251. , COI: 1:STN:280:DC%2BD3s%2Flt1Khuw%3D%3D, PID: 12561501; Cafazzo, S., Valsecchi, P., Bonanni, R., Natoli, E., Dominance in relation to age, sex, and competitive contexts in a group of free-ranging domestic dogs (2010) Behav. Ecol., 21, pp. 443-455; Majumder, S.S., To be or not to be social: Foraging associations of free-ranging dogs in an urban ecosystem (2014) Acta Ethol., 17, pp. 1-8; Bonanni, R., Cafazzo, S., (2014) The Social Organisation of A Population of Free-Ranging Dogs in A Suburban Area of Rome: A Reassessment of the Effects of Domestication on Dogs’ Behaviour, , https://doi.org/10.1016/B978-0-12-407818-5.00003-6, The Social Dog, Behavior and Cognition (Elsevier; Hampson, K., Estimating the global burden of endemic canine rabies (2015) PLoS Negl. Trop. Dis., 9, pp. 1-20; Singh, R., Rabies—Epidemiology, pathogenesis, public health concerns and advances in diagnosis and control: A comprehensive review (2017) Vet. Q., 37, pp. 212-251. , PID: 28643547; Zinsstag, J., Vaccination of dogs in an African city interrupts rabies transmission and reduces human exposure (2017) Sci. Transl. Med., 9, p. eaaf6984. , PID: 29263230; Kumarapeli, V., Awerbuch-Friedlander, T., Human rabies focusing on dog ecology—A challenge to public health in Sri Lanka (2009) Acta Trop., 112, pp. 33-37. , PID: 19540826; Mindekem, R., Cost description and comparative cost efficiency of post-exposure prophylaxis and canine mass vaccination against rabies in N’Djamena, Chad (2017) Front. Vet. Sci., 4, p. 38. , PID: 28421186; Zinsstag, J., Transmission dynamics and economics of rabies control in dogs and humans in an African city (2009) Proc. Natl. Acad. Sci. U. S. A., 106, pp. 14996-15001. , COI: 1:CAS:528:DC%2BD1MXhtFGnurbK, PID: 19706492; (2018) WHO expert consultation on rabies, , World Health Organization—Technical Report Series; Hampson, K., Synchronous cycles of domestic dog rabies in sub-Saharan Africa and the impact of control efforts (2007) Proc. Natl. Acad. Sci., 104, pp. 7717-7722. , COI: 1:CAS:528:DC%2BD2sXlslahtro%3D, PID: 17452645; Vial, F., Cleaveland, S., Rasmussen, G., Haydon, D.T., Development of vaccination strategies for the management of rabies in African wild dogs (2006) Biol. Conserv., 131, pp. 180-192; Laager, M., The importance of dog population contact network structures in rabies transmission (2018) PLoS Negl. Trop. Dis., 12, pp. 1-18; Hudson, E.G., Brookes, V.J., Ward, M.P., Dürr, S., Using roaming behaviours of dogs to estimate contact rates: The predicted effect on rabies spread (2019) Epidemiol. Infect., 147. , PID: 30869048; Wilson-Aggarwal, J.K., High-resolution contact networks of free-ranging domestic dogs Canis familiaris and implications for transmission of infection (2019) PLoS Negl. Trop. Dis., 13, pp. 1-19; Flores-Ibarra, M., Estrella-Valenzuela, G., Canine ecology and socioeconomic factors associated with dogs unvaccinated against rabies in a Mexican city across the US-Mexico border (2004) Prev. Vet. Med., 62, pp. 79-87. , PID: 15156995; Dürr, S., Dhand, N.K., Bombara, C., Molloy, S., Ward, M.P., What influences the home range size of free-roaming domestic dogs? (2017) Epidemiol. Infect., 145, pp. 1339-1350. , PID: 28202088; Hudson, E.G., Brookes, V.J., Dürr, S., Ward, M.P., Domestic dog roaming patterns in remote northern Australian indigenous communities and implications for disease modelling (2017) Prev. Vet. Med., 146, pp. 52-60. , PID: 28992928; Hudson, E.G., Brookes, V.J., Dürr, S., Ward, M.P., Modelling targeted rabies vaccination strategies for a domestic dog population with heterogeneous roaming patterns (2019) PLoS Negl. Trop. Dis., 13, pp. 1-15; Brookes, V.J., VanderWaal, K., Ward, M.P., The social networks of free-roaming domestic dogs in island communities in the Torres Strait, Australia (2018) Prev. Vet. Med.; Warembourg, C., Comparative study of free-roaming domestic dog management and roaming behavior across four countries: Chad, Guatemala, Indonesia and Uganda (2021) Front. Vet. Sci., 8, p. 617900. , PID: 33748208; Warembourg, C., Estimation of free-roaming domestic dog population size: Investigation of three methods including an Unmanned Aerial Vehicle (UAV) based approach (2020) PLoS ONE, 15, pp. 1-24. , COI: 1:CAS:528:DC%2BB3cXnvVGksr8%3D; Wey, T., Blumstein, D.T., Shen, W., Jordán, F., Social network analysis of animal behaviour: a promising tool for the study of sociality (2008) Anim. Behav., 75, pp. 333-344; Humphries, M.D., Gurney, K., Network ‘small-world-ness’: A quantitative method for determining canonical network equivalence (2008) PLoS ONE, 3. , PID: 18446219, COI: 1:CAS:528:DC%2BD1cXmt1WjsLs%3D; Christley, R.M., French, N.P., Small-world topology of UK racing: The potential for rapid spread of infectious agents (2010) Equine Vet. J., 35, pp. 586-589; Amaral, L.A.N., Scala, A., Barthe, M., Classes of small-world networks (2000) Proc. Natl. Acad. Sci. U. S. A., 97, pp. 11149-11152. , COI: 1:CAS:528:DC%2BD3cXnsF2rt7g%3D, PID: 11005838; Telesford, Q.K., Joyce, K.E., Hayasaka, S., Burdette, J.H., Laurienti, P.J., The ubiquity of small-world networks (2011) Brain Connect., 1, pp. 367-375. , PID: 22432451; Dürr, S., Ward, M.P., Development of a novel rabies simulation model for application in a non-endemic environment (2015) PLoS Negl. Trop. Dis., 9. , PID: 26114762, COI: 1:CAS:528:DC%2BC1cXlsFOmtLg%3D; Davlin, S.L., VonVille, H.M., Canine rabies vaccination and domestic dog population characteristics in the developing world: A systematic review (2012) Vaccine, 30, pp. 3492-3502. , PID: 22480924; Atuman, Y.J., Ogunkoya, A.B., Adawa, D.A.Y., Nok, A.J., Biallah, M.B., Dog ecology, dog bites and rabies vaccination rates in Bauchi State, Nigeria (2014) Int. J. Vet. Sci. Med., 2, pp. 41-45; Schildecker, S., Dog ecology and barriers to canine rabies control in the Republic of Haiti, 2014–2015 (2017) Transbound. Emerg. Dis., 64, pp. 1433-1442. , COI: 1:STN:280:DC%2BC2s7gvFKksA%3D%3D, PID: 27313170; Watts, D., Strogatz, S., Collective dynamics of networks (1998) Nature, 393, pp. 440-442. , COI: 1:CAS:528:DyaK1cXjs1Khsrk%3D, PID: 9623998; Kiss, I.Z., Green, D.M., Kao, R.R., The network of sheep movements within Great Britain: Network properties and their implications for infectious disease spread (2006) J. R. Soc. Interface, 3, pp. 669-677. , PID: 16971335; Büttner, K., Krieter, J., Traulsen, A., Traulsen, I., Static network analysis of a pork supply chain in Northern Germany—Characterisation of the potential spread of infectious diseases via animal movements (2013) Prev. Vet. Med., 110, pp. 418-428. , PID: 23462679; Acosta-Jamett, G., Cleaveland, S., Cunningham, A.A., Bronsvoort, B.M.D.C., Demography of domestic dogs in rural and urban areas of the Coquimbo region of Chile and implications for disease transmission (2010) Prev. Vet. Med., 94, pp. 272-281. , COI: 1:STN:280:DC%2BC3c3hsFCnsg%3D%3D, PID: 20096943; Ortega-Pacheco, A., A Survey of dog populations in urban and rural areas of Yucatan, Mexico (2007) Anthrozoos, 20, pp. 261-274; Mustiana, A., Owned and unowned dog population estimation, dog management and dog bites to inform rabies prevention and response on Lombok Island, Indonesia (2015) PLoS ONE, 10, pp. 1-15. , COI: 1:CAS:528:DC%2BC2MXhvFKnurnK; Wallace, R.M.L., The impact of poverty on dog ownership and access to canine rabies vaccination: Results from a knowledge, attitudes and practices survey, Uganda 2013 (2017) Infect. Dis. Poverty, 6, pp. 1-22; Atuman, Y.J., Dog ecology, dog bites and rabies vaccination rates in Bauchi State, Nigeria Dog ecology, dog bites and rabies vaccination rates in Bauchi State, Nigeria (2019) Int. J. Vet. Sci. Med., 2, pp. 41-45; O’Neill, H.M.K., Durant, S.M., Woodroffe, R., What wild dogs want: Habitat selection differs across life stages and orders of selection in a wide-ranging carnivore (2020) BMC Zool., 5, pp. 1-11; Hudson, E.G., Dhand, N., Dürr, S., Ward, M.P., A survey of dog owners in remote northern Australian indigenous communities to inform rabies incursion planning (2016) PLoS Negl. Trop. Dis., 10, pp. 1-18. , COI: 1:CAS:528:DC%2BC1cXmtVKmsLo%3D; Turner, D.C., Waiblinger, E., Meslin, F.-X., Benefits of the human–dog relationship (2013) Dogs, Zoonoses and Public Health, pp. 13-23; Bhattacharjee, D., Sau, S., Bhadra, A., Free-ranging dogs understand human intentions and adjust their behavioral responses accordingly (2018) Front. Ecol. Evol., 6, pp. 1-9. , COI: 1:CAS:528:DC%2BC1MXhsVenu73L; Bhattacharjee, D., Sau, S., Das, J., Bhadra, A., Free-ranging dogs prefer petting over food in repeated interactions with unfamiliar humans (2017) J. Exp. Biol., 220, pp. 4654-4660. , PID: 29038310; Bhattacharjee, D., Free-ranging dogs show age related plasticity in their ability to follow human pointing (2017) PLoS ONE, 12, pp. 1-17. , COI: 1:CAS:528:DC%2BC1cXnsV2js7c%3D; Bhattacharjee, D., Sau, S., Bhadra, A., Bolder together-response to human social cues in groups of free-ranging dogs (2020) Behaviour, 157, pp. 363-384; Villatoro, F.J., Sepúlveda, M.A., Stowhas, P., Silva-Rodríguez, E.A., Urban dogs in rural areas: Human-mediated movement defines dog populations in southern Chile (2016) Prev. Vet. Med., 135, pp. 59-66. , PID: 27931930; Colombi, D., Poletto, C., Nakouné, E., Bourhy, H., Colizza, V., Long-range movements coupled with heterogeneous incubation period sustain dog rabies at the national scale in Africa (2020) PLoS Negl. Trop. Dis., 14. , PID: 32453756; Miklósi, Á., Turcsán, B., Kubinyi, E., The personality of dogs (2014) Soc. Dog Behav. Cogn.; Kubinyi, E., Turcsán, B., Miklósi, Á., Dog and owner demographic characteristics and dog personality trait associations (2009) Behav. Process., 81, pp. 392-401; Siniscalchi, M., Stipo, C., Quaranta, A., ‘Like owner, like dog’: Correlation between the owner’s attachment profile and the owner–dog bond (2013) PLoS ONE, 8. , COI: 1:CAS:528:DC%2BC3sXhsleqt77I, PID: 24205235; Ley, J.M., Bennett, P.C., Coleman, G.J., A refinement and validation of the Monash Canine Personality Questionnaire (MCPQ) (2009) Appl. Anim. Behav. Sci., 116, pp. 220-227; Eken Asp, H., Fikse, W.F., Nilsson, K., Strandberg, E., Breed differences in everyday behaviour of dogs (2015) Appl. Anim. Behav. Sci., 169, pp. 69-77; Dias, R.A., Size and spatial distribution of stray dog population in the University of São Paulo campus, Brazil (2013) Prev. Vet. Med., 110, pp. 263-273. , PID: 23273378; Bombara, C.B., Dürr, S., Machovsky-Capuska, G.E., Jones, P.W., Ward, M.P., A preliminary study to estimate contact rates between free-roaming domestic dogs using novel miniature cameras (2017) PLoS ONE, 12, pp. 1-16. , COI: 1:CAS:528:DC%2BC1cXnsV2jtrk%3D; Heurtefeux, K., Valois, F., Is RSSI a good choice for localization in wireless sensor network? (2012) In Proc.—Int. Conf. Adv. Inf. Netw. Appl. AINA, pp. 732-739. , https://doi.org/10.1109/AINA.2012.19; Fielding, H.R., Timing of reproduction and association with environmental factors in female free-roaming dogs in southern India (2021) Prev. Vet. Med., 187, p. 105249. , COI: 1:STN:280:DC%2BB3svnsFajsw%3D%3D, PID: 33418515; Hampson, K., Rabies exposures, post-exposure prophylaxis and deaths in a region of endemic canine rabies (2008) PLoS Negl. Trop. Dis., 2. , PID: 19030223; Brookes, V.J., Dürr, S., Ward, M.P., Rabies-induced behavioural changes are key to rabies persistence in dog populations: Investigation using a network-based model (2019) PLoS Negl. Trop. Dis., 13, pp. 1-19; Croft, D.P., Madden, J.R., Franks, D.W., James, R., Hypothesis testing in animal social networks (2011) Trends Ecol. Evol., 26, pp. 502-507. , PID: 21715042; Gordon, R.A., (2015) Regression Analysis for the Social Sciences, , Routledge; Mollentze, N., Biek, R., Streicker, D.G., The role of viral evolution in rabies host shifts and emergence (2014) Curr. Opin. Virol., 8, pp. 68-72. , PID: 25064563; Dekker, D., Krackhardt, D., Snijders, T.A.B., Sensitivity of MRQAP tests to collinearity and autocorrelation conditions (2007) Psychometrika, 72, pp. 563-581. , PID: 20084106; (2020) R: A Language and Environment for Statistical Computing; Paradis, E., Schliep, K., ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R (2019) Bioinformatics, 35, pp. 526-528. , COI: 1:CAS:528:DC%2BC1MXitVWgs7%2FL, PID: 30016406; Le, S., Josse, J., Husson, F., FactoMineR: An R package for multivariate analysis (2008) J. Stat. Softw., 25, pp. 1-18; Butts, C.T.S., Tools for Social Network Analysis (2019) R Package Version, 2, p. 5

Indexed by Scopus

Leave a Comment