Rabies in primates: are aggressive pet lemurs a risk to humans?

Authors

  • Kim E. Reuter Conservation International, Gabarone
  • Tara A. Clarke Duke University, and Lemur Love Inc. Durham, NC
  • Marni LaFleur University of California San Diego, and Lemur Love Inc., San Diego, CA
  • Melissa S. Schaefer University of Utah, and Salt Lake City Community College Salt Lake City, UT

Keywords:

rabies, lemur, non-human primates, pet trade, public health, disease transmission

Abstract

Non-human primates harbor zoonotic pathogens including the rabies virus (Rabies lyssavirus). Though the chances of rabies transmission from primates is low, guidelines currently recommend a post-exposure prophylaxis for unvaccinated persons. In Madagascar, lemurs have been described as carriers of the rabies virus, but a discussion about the risk of rabies transmission to humans from lemurs, particularly in the context of in-country ownership of lemurs, has not been studied. We use qualitative and quantitative data collected from household surveys (n = 271 interviewees who had seen a pet lemur across 12 urban towns), web-based surveys (n = 229), and the literature (publications using data collected by the Institute Pasteur of Madagascar over the last century) to examine the context in which the rabies virus could be transmitted from lemurs to humans. Though only a few wild and pet lemurs in Madagascar have tested positive for rabies, post-exposure treatment is sometimes also sought out following aggressive incidents with lemurs. Many interviewees (22 ± 6%, mean ± 95% confidence interval CI) across 12 towns indicated that pet lemurs they had seen, had a history of aggression. Some lemur owners appear to be aware that their pets could transmit the rabies virus and seek veterinary care to prevent this. The public health burden of rabies is relatively low in Madagascar and despite some anecdotes in the literature, it appears that lemurs are rarely the source of rabies when humans become infected. However, this case study highlights the lack of data and publications regarding the public health implications of human-lemur contact in Madagascar.

 

Résumé

Les primates non-humains hébergent des pathogènes zoonotiques incluant le virus de la rage (Rabies lyssavirus). Bien que les risques de transmission de la rage par les primates soient faibles, les lignes directrices recommandent actuellement une prophylaxie post-exposition pour les personnes non vaccinées. À Madagascar, les lémuriens ont été décrits comme porteurs du virus de la rage, mais une discussion sur le risque de transmission de la rage à l'Homme par les lémuriens, en particulier dans le contexte de la propriété locale des lémuriens, n'a pas été étudiée. Nous utilisons des données qualitatives et quantitatives collectées à partir d'enquêtes auprès des foyers (n = 271 interviewés ayant vu un lémurien dans 12 villes), des enquêtes en ligne (n = 229) et de la littérature (publications utilisant des données collectées par l'Institut Pasteur de Madagascar au cours du siècle dernier) pour examiner le contexte dans lequel le virus de la rage pourrait être transmis par les lémuriens aux humains. Bien que seuls quelques lémuriens sauvages et animaux de compagnie à Madagascar aient été testés positifs à la rage, un traitement post-exposition est parfois également recherché suite à des agressions par des lémuriens. De nombreuses personnes interrogées (22 ± 6%, moyenne ± Intervalle de confiance IC à 95%) dans 12 villes ont indiqué que les animaux de compagnie qu'ils avaient vus avaient des antécédents d'agression. Quelques propriétaires de lémuriens semblent être conscients que leurs animaux de compagnie peuvent transmettre le virus de la rage et demander des soins vétérinaires pour éviter cela. La rage constitue une charge relativement faible pour la santé publique à Madagascar et malgré quelques anecdotes dans la littérature, il semble que les lémuriens soient rarement la source de la rage lorsque les humains sont infectés. Cependant, cette étude de cas souligne le manque de données et de publications concernant les implications / conséquences du contact entre humains et lémuriens sur la santé publique à Madagascar.

References

Andriamandimby, S. F., Héraud, J. M., Ramiandrasoa, R., Ratsitorahina, M., Rasambainarivo, J. H., et al. 2013. Surveillance and control of rabies in La Reunion, Mayotte, and Madagascar. Veterinary Research 44: #77. <https://doi.org/10.1186/1297-9716-44-77>

Barrett, M. A. 2011. Understanding Environmental and Anthropogenic Drivers of Lemur Health in Madagascar: the Importance of a One Health Perspective. Unpubl. Doctoral Dissertation. Duke University, Durham. <https://dukespace.lib.duke.edu/dspace/handle/10161/3885>

Bradt, H. 2007. Madagascar: the Bradt travel guide. Bradt Travel Guides Ltd., U.K.

Brown, J. L. and Yoder, A. D. 2015. Shifting ranges and conservation challenges for lemurs in the face of climate change. Ecology and Evolution 5, 6: 1131–1142. <https://doi.org/10.1002/ece3.1418>

Centers for Disease Control and Prevention. 2017. Health Information for Travelers to Madagascar. <https://wwwnc.cdc.gov/travel/destinations/traveler/none/madagascar> Accessed 21 May 2017.

Christiansen, A. H., Rodriguez, A. B., Nielsen, J. and Cowan, S. A. 2016. Should travellers to rabies-endemic countries be pre-exposure vaccinated? An assessment of post-exposure prophylaxis and pre-exposure prophylaxis given to Danes travelling to rabies-endemic countries 2000–12. Journal of Travel Medicine 23, 4: 1–6. <https://doi.org/10.1093/jtm/taw022>

Cleaveland, S. 1998. Epidemiology and control of rabies. The growing problem of rabies in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 2: 131–134. <https://doi.org/10.1016/S0035-9203(98)90718-0>

Coulanges, P., Rakotonirina-Randriambeloma, P.-J. and Brygoo, E.-R. 1974. La rage à Madagascar: vingt ans d’utilisation d’un vaccin antirabique phéniqué type fermi avec virulence résiduelle. Archives de l’Institut Pasteur de Madagascar 43: 149–179. <https://bit.ly/2LNPsAX>

Folb, J. E. and Cooke, R. P. 2006. Issues of human rabies immunoglobulin and vaccine: policy versus practice. Journal of Public Health 29, 1: 83–87. <https://doi.org/10.1093/pubmed/fdl079>

Girard, G. 1930. L’Institut Pasteur de Tananarive. Imprimerie Moderne de l’Emyrne, Antananarivo, Madagascar.

Gautret, P., Adehossi, E., Soula, G., Soavi, M.-J., Delmont, J., et al. 2010. Rabies exposure in international travelers: do we miss the target? International Journal of Infectious Diseases 14, 3: e243–e246. <https://doi.org/10.1016/j.ijid.2009.05.009>

Gautret, P., Blanton, J., Dacheux, L., Ribadeau-Dumas, F., Brouqui, P., et al. 2014. Rabies in nonhuman primates and potential for transmission to humans: a literature review and examination of selected French national data. PLOS Neglected Tropical Diseases 8, 5: e2863. <https://doi.org/10.1371/journal.pntd.0002863>

Health Protection Agency. 2013. Guidelines on Managing Rabies Post-Exposure Prophylaxis: January 2013. <http://www.hpa.org.uk/webc/HPAwebFile/HPAweb_C/1224745729371> Accessed 7 Feb 2013.

Institut Pasteur de Madagascar. 2007. Rapport d'Activités 2007. Institut Pasteur de Madagascar, Antananarivo, Madagascar. <http://www.pasteur.mg/publication/rapport-dactivites-2007/>

Institut Pasteur de Madagascar. 2016. Rapport d'Activités 2015. Institute Pasteur Madagascar, Antananarivo, Madagascar. <http://www.pasteur.mg/publication/rapport-dactivites-2015/>

Institut Pasteur de Madagascar. 2017. Rapport d'Activités 2016. Institute Pasteur Madagascar, Antananarivo, Madagascar. <http://www.pasteur.mg/publication/rapport-dactivites-ipm-2016/>

Jennings, E. T. 2009. Confronting rabies and its treatment in colonial Madagascar, 1899–1910. Social History of Medicine 22, 2: 263–282. <https://doi.org/10.1093/shm/hkp010>

Junge, R. E. and Sauther, M. L. 2006. Overview of the health and disease ecology of wild lemurs: conservation implications. In: Lemurs Ecology and Adaptation. L. Gould and M. L. Sauther (eds.), pp 423–440. Springer Science and Business Media, New York, NY, USA.

Le Brun, Y. & Randrianarison, A. 2014. Conseils sanitaires aux résidents ou expatriés à Madagascar. Consulat Général de France à Tananarive, Madagascar. <https://bit.ly/2LnRfR2>

Levinson, J., Bogich, T. L., Olival, K. J., Epstein, J. H., Johnson, C. K., Karesh, W. and Daszak, P. 2013. Targeting surveillance for zoonotic virus discovery. Emerging infectious diseases 19, 5: 743–747. <https://doi.org/10.3201/eid1905.121042>

Mease, L. E. and Baker, K. A. 2012. Monkey bites among US military members, Afghanistan, 2011. Emerging Infectious Diseases 18, 10: 1647–1649. <https://doi.org/10.3201/eid1810.120419>

Morvan, J. M., Rakoto-Andrianarivelo, M., Randriamihoatra, S. & Roux, J. 1993. Situation de l’endémie rabique à Madagascar. Archives de l’Institut Pasteur de Madagascar 60, 1–2: 5–8.

Muehlenbein, M. P. 2017. Primates on display: potential disease consequences beyond bushmeat. American Journal of Physical Anthropology 162, S63: 32–43. <https://doi.org/10.1002/ajpa.23145>

National Health Service. 2017. Rabies. Online, <http://www.nhs.uk/Conditions/Rabies/Pages/Introduction.aspx> Accessed 22 May 2017.

Reuter, K. E. and Schaefer, M. S. 2016. Captive conditions of pet lemurs in Madagascar. Folia Primatologica 87, 1: 48–63. <https://doi.org/10.1159/000444582>

Reuter, K. E. and Schaefer, M. S. 2017a. Motivations for the ownerships of captive lemurs in Madagascar. Anthrozoös 30, 1: 33–46. <https://doi.org/10.1080/08927936.2017.1270589>

Reuter, K. E. and Schaefer, M. S. 2017b. Illegal captive lemurs in Madagascar: comparing the use of online and in-person data collection methods. American Journal of Primatology 79, 11: e22541. <https://doi.org/10.1002/ajp.22541>

Reuter, K. E., Gilles, H., Wills, A. R. and Sewall, B. J. 2016. Live capture and ownership of pet lemurs in Madagascar: extent and conservation implications. Oryx 50, 2: 344–354. <https://doi.org/10.1017/S003060531400074X>

Reuter, K. E., Clarke, T. A., LaFleur, M., Ratsimbazafy, J., Holiniaina Kjelgaard, F., et al. 2018. Exploring the role of wealth and religion on the ownership of captive lemurs in Madagascar using qualitative and quantitative data. Folia Primatologica 89, 1: 81–96. <https://doi.org/10.1159/000477400>

Reynes, J. –M., Andriamandimby, S. F., Razafitrimo, G. M., Razainirina, J., Jeanmaire, E. M., et al. 2011. Laboratory surveillance of rabies in humans, domestic animals, and bats in Madagascar from 2005 to 2010. Advances in Preventive Medicine 2011: #727821. <http://dx.doi.org/10.4061/2011/727821>

Riesland, N. J. and Wilde, H. 2015. Expert review of evidence bases for managing monkey bites in travelers. Journal of Travel Medicine 22, 4: 259–262. <https://doi.org/10.1111/jtm.12214>

Tsiresy, R. 1995. Rabies in Madagascar. Proceeding of the SEARG International Symposium. Available online <http://searg.info/fichiers/articles/1995045047L.PDF> Accessed 21 May 2017.

United Nations. 2017.Population Division. World Population Prospects 2017. <https://esa.un.org/unpd/wpp/dataquery/> Accessed 20 May 2018.

Valenta, K., Gettinger-Larson, J. A., Chapman, C. A. and Farris, Z. J. 2016. Barking up the right tree: understanding local attitudes towards dogs in villages surrounding Ranomafana National Park, Madagascar can benefit applied conservation. Madagascar Conservation & Development 11, 2: 87–90. <http://dx.doi.org/10.4314/mcd.v11i2.4>

World Health Organization. 2010. Rabies vaccines. WHO position paper. Weekly Epidemiological Record 85, 32: 309–320. <http://www.who.int/wer/2010/wer8532/en/>

World Tourism Organization. 2014. International tourism, number of arrivals. <http://data.worldbank.org/indicator/ST.INT.ARVL?locations=MG> Accessed 21 May 2017.

Zeller, H. G., Rakoto-Andrianarivelo, M., Rakotonjanabelo, L. A. and Roux, J. F. 1999. Rabies in Madagascar: 1994–1998. Proceedings of the Southern and Eastern African Rabies Group/World Health Organization Meeting in Entebbe, Uganda 29–31 March, 1999, pp 58–62. Éditions Fondation Marcel Mérieux, Lyon, France. <https://bit.ly/2Lt1KT6>

Crowned lemur kept in captivity in Northern Madagascar. Eulemur coronatus. Pet Lemur. Madagascar Conservation & Development. Photo Kim Reuter

Published

19-12-2018

Issue

Section

Articles

Most read articles by the same author(s)