ArticlePDF Available

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

Authors:
Kim Reuter at Franklin Scholars
Kim Reuter
  • Franklin Scholars
Marni LaFleur at University of San Diego
Marni LaFleur
Tara A Clarke at North Carolina State University
Tara A Clarke
Melissa Schaefer Seaboch at Salt Lake Community College
Melissa Schaefer Seaboch
Download full-text PDF
Read full-text
Download citation

Abstract

Non-human primates harbor zoonotic pathogens including the ra- bies virus (Rabies lyssavirus). Though the chances of rabies trans- mission from primates is low, guidelines currently recommend a post-exposure prophylaxis for unvaccinated persons. In Madagas- car, 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 ex- amine 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 treat- ment 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 high- lights the lack of data and publications regarding the public health implications of human-lemur contact in Madagascar.
Content uploaded by Kim Reuter
Author content
All content in this area was uploaded by Kim Reuter on Aug 19, 2018
Content may be subject to copyright.
Reuter, K. E., Clarke, T. A., LaFleur, M. and Schaefer, M. S. 2018. Rabies in primates: are aggressive pet
lemurs a risk to humans? Madagascar Conservation & Development 13, 1: xx–xx.
http://dx.doi.org/10.4314/mcd.v13i1.9 Supplementary material
SM 1
Table S1. The primary and secondary sources from which IPM data were collected, including information on
the information source, the year(s) for which this source provided information, and the type of
information taken from this source. In the results, we indicate which source provided information
by referencing the Source Code (first column of the table).
Source
Code
Source
Date range of
information
Type of information/data
A
Coulanges et al. 1974
1898–1958;
1954–1973
Number of lemurs tested for rabies in Madagascar (and number that
tested positive for rabies; data also presented for other animals).
B
Jennings 2009
1901–1910
Number of patients treated nationally; number of patients treated in
Antananarivo
C
Institut Pasteur de
Madagascar 1961
1960
Number of patients treated nationally; number of patients treated in
Antananarivo; number of patients exposed to rabies from lemurs
D
Morvan et al. 1993
1959–1991
Number of lemurs tested for rabies in Madagascar (and number that
tested positive for rabies; data also presented for other animals).
E
Zeller et al. 1999
1994–1998
Number of lemurs tested for rabies in Madagascar (and number that
tested positive for rabies; data also presented for other animals);
number of patients treated nationally; number of patients treated in
Antananarivo; number of patients exposed to rabies from lemurs;
characteristics of the lemurs suspected of transmitting rabies
F
Reynes et al. 2011
2005–2010
Number of lemurs tested for rabies in Madagascar (and number that
tested positive for rabies; data also presented for other animals).
G
Institut Pasteur de
Madagascar 2006
2006
Number of patients treated nationally; number of patients treated in
Antananarivo; number of patients exposed to rabies from lemurs;
characteristics of the lemurs suspected of transmitting rabies
H
Institut Pasteur de
Madagascar 2007
2007
Number of patients treated nationally; number of patients treated in
Antananarivo; number of patients exposed to rabies from lemurs;
characteristics of the lemurs suspected of transmitting rabies
I
Institut Pasteur de
Madagascar 2008
2008
Number of patients treated nationally; number of patients treated in
Antananarivo; number of patients exposed to rabies from lemurs;
characteristics of the lemurs suspected of transmitting rabies
J
Institut Pasteur de
Madagascar 2009
2009
Number of patients treated in Antananarivo; number of patients
exposed to rabies from lemurs; characteristics of the lemurs suspected
of transmitting rabies
K
Institut Pasteur de
Madagascar 2010
2010
Number of patients treated nationally; number of patients treated in
Antananarivo; number of patients exposed to rabies from lemurs;
characteristics of the lemurs suspected of transmitting rabies
L
Institut Pasteur de
Madagascar 2011
2011
Number of patients treated nationally; number of patients treated in
Antananarivo; number of patients exposed to rabies from lemurs;
characteristics of the lemurs suspected of transmitting rabies
M
Institut Pasteur de
Madagascar 2012
2012
Number of patients treated nationally; number of patients treated in
Antananarivo; number of patients exposed to rabies from lemurs;
characteristics of the lemurs suspected of transmitting rabies
N
Institut Pasteur de
Madagascar 2015
2014
Number of patients treated nationally; number of lemurs tested for
rabies in Madagascar (and number that tested positive for rabies; data
also presented for other animals)
O
Institut Pasteur de
Madagascar 2016
2015
Number of patients treated nationally; number of lemurs tested for
rabies in Madagascar (and number that tested positive for rabies; data
also presented for other animals)
P
Institut Pasteur de
Madagascar 2017
2016
Number of patients treated nationally; number of lemurs tested for
rabies in Madagascar (and number that tested positive for rabies; data
also presented for other animals)
Reuter, K. E., Clarke, T. A., LaFleur, M. and Schaefer, M. S. 2018. Rabies in primates: are aggressive pet
lemurs a risk to humans? Madagascar Conservation & Development 13, 1: xx–xx.
http://dx.doi.org/10.4314/mcd.v13i1.9 Supplementary material
SM 2
Table S2. The number and percent of animals that tested positive for the rabies virus in tests conducted by
the Institut Pasteur de Madagascar IPM (samples typically sent to IPM by veterinarians). These
lemurs were tested by the IPM because the animals were suspected as being rabies virus
carriers (i.e. a human receiving PEP treatment from IPM indicated that the specific animal was
the reason for seeking treatment). * cf. Table S1; † As per Coulanges et al. (1974), it was noted
that no lemurs had been found to be positive for rabies between 1954 and 1973 and that,
therefore, 6 or 7 of these earlier ‘positive’ tests likely were incorrect, as they were all made by one
observer during 1910 and 1913. Therefore, these data were considered inaccurate by Coulanges
et al. (1974).
Number
of years
in
range
Total
number of
animals
tested
Number
of lemurs
tested
Percent (%) of lemurs
tested
Number of dogs
Comments
Source*
positive
positive/year
tested
% tested
positive
61
N.D.
45
15.5% †
0.25%
N.D.
N.D.
A
20
1 672
33
0%
0%
1 313
42%
A
33
2 953
47
0%
0%
2 481
57%
D
5
427
26
3.80%
0.76%
347
69%
E
6
450
10
0%
0%
353
54%
F
1
96
0
N/A
N/A
77
49%
G
1
77
3
0%
0%
56
57%
The lemurs tested
were from the city
of Antananarivo and
Ambohidratrimo
H
1
73
5
0%
0%
47
26%
Four lemurs were
from Antananarivo
and one lemur was
from Tôlanaro
I
1
63
0
N/A
N/A
49
53%
J
1
45
0
N/A
N/A
39
51%
K
1
117
1
0%
0%
98
69%
Lemur was from
Antananarivo
L
1
140
0
N/A
N/A
129
80%
M
1
86
0
N/A
N/A
65
58%
N
1
59
0
N/A
N/A
48
N.D.
O
1
125
0
N/A
N/A
103
75%
P
Reuter, K. E., Clarke, T. A., LaFleur, M. and Schaefer, M. S. 2018. Rabies in primates: are aggressive pet
lemurs a risk to humans? Madagascar Conservation & Development 13, 1: xx–xx.
http://dx.doi.org/10.4314/mcd.v13i1.9 Supplementary material
SM 3
Table S3. Information collected from patients about whether the lemur in question (i.e. the lemur which
caused a person to receive PEP treatment at IPM) was a wild or pet lemur, as well as what
happened to the lemur in question. Descriptions of lemurs are translated from the French
language directly from IPM reports (noting that the IPM reports provided no further information
about how lemurs were categorized into these different descriptions). † The data for 2008 and
2009 are identical despite being reported in two different IPM annual reports. It is unlikely that
these numbers would be exactly the same across two years; therefore, the information for one of
the years is probably incorrect.
1960
1998
2006
2007
2008 †
2009 †
2010
Number of patients thought to have been exposed
to the rabies virus from lemurs
7
93
30
97
36
36
23
Wild lemur
Free roaming lemur (location unknown)
N.D
N.D
23
60
13
13
11
Free roaming lemur (still alive), unknown owner
N.D
N.D
0
6
1
1
2
Pet lemur
Pet lemur, with known owner
N.D
N.D
7
23
21
21
10
Pet lemur (location unknown)
N.D
N.D
0
1
0
0
0
Pet lemur killed
N.D
N.D
0
1
1
1
0
Pet lemur died of the disease
N.D
N.D
0
6
0
0
0
Source (cf. Table S1)
C
E
G
H
I
J
K
REFERENCES
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. Available at <https://bit.ly/2LNPsAX>
Institut Pasteur de Madagascar. 1961. Rapport sur le fonctionnement de l'Institut Pasteur de Madagascar en
1960. Archives de Institute Pasteur de Madagascar, Antananarivo, Madagascar.
Institut Pasteur de Madagascar. 2006. Rapport d’Activités 2006. Institute Pasteur de Madagascar,
Antananarivo, Madagascar. Available at <http://www.pasteur.mg/publication/rapport-dactivites-2006/>
Institut Pasteur de Madagascar. 2007. Rapport d'Activités 2007. Institut Pasteur de Madagascar, Antananarivo,
Madagascar. Available at <http://www.pasteur.mg/publication/rapport-dactivites-2007/>
Institut Pasteur de Madagascar. 2008. Rapport d’Activités 2008. Institute Pasteur de Madagascar,
Antananarivo, Madagascar. Available at <http://www.pasteur.mg/publication/rapport-dactivites-2008/>
Institut Pasteur de Madagascar. 2009. Rapport d’Activités 2009. Institute Pasteur de Madagascar,
Antananarivo, Madagascar. Available at <http://www.pasteur.mg/publication/rapport-dactivites-2009/>
Institut Pasteur de Madagascar. 2010. Rapport d’Activités 2010. Institute Pasteur de Madagascar,
Antananarivo, Madagascar. Available at <http://www.pasteur.mg/publication/rapport-dactivites-2010/>
Institut Pasteur de Madagascar. 2011. Rapport d’Activités 2011. Institute Pasteur de Madagascar,
Antananarivo, Madagascar. Available at <http://www.pasteur.mg/publication/rapport-dactivites-2011/>
Reuter, K. E., Clarke, T. A., LaFleur, M. and Schaefer, M. S. 2018. Rabies in primates: are aggressive pet
lemurs a risk to humans? Madagascar Conservation & Development 13, 1: xx–xx.
http://dx.doi.org/10.4314/mcd.v13i1.9 Supplementary material
SM 4
Institut Pasteur de Madagascar. 2012. Rapport d’Activités 2012. Institute Pasteur de Madagascar,
Antananarivo, Madagascar. Available at <http://www.pasteur.mg/publication/rapport-dactivites-2012/>
Institut Pasteur de Madagascar. 2015. Rapport d’Activités 2014. Institute Pasteur de Madagascar,
Antananarivo, Madagascar. Available at <http://www.pasteur.mg/publication/rapport-dactivites-2014/>
Institut Pasteur de Madagascar. 2016. Rapport d'Activités 2015. Institute Pasteur de Madagascar,
Antananarivo, Madagascar. Available at <http://www.pasteur.mg/publication/rapport-dactivites-2015/>
Institut Pasteur de Madagascar. 2017. Rapport d'Activités 2016. Institute Pasteur de Madagascar,
Antananarivo, Madagascar. Available at <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>
Morvan, J. M., Rakoto-Andrianarivelo, M., Randriamihoatra, S. & Roux, J. 1993. Situation de l’endémie
rabique a Madagascar. Archives de l’Institut Pasteur de Madagascar 60, 1–2: 5–8.
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>
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. Available at
<https://pdfs.semanticscholar.org/ab2b/dbb344be3ca72feed01ef73aca78d772a288.pdf>
ResearchGate has not been able to resolve any citations for this publication.
Surveillance and control of rabies in La Reunion, Mayotte, and Madagascar
Article
Full-text available
  • Sep 2013
  • VET RES
: Mayotte and La Reunion islands are currently free of animal rabies and surveillance is performed by the French Human and Veterinary Public Health Services. However, dog rabies is still enzootic in Madagascar with 4 to 10 confirmed human cases each year. The number of antirabies medical centres in Madagascar is still scarce to provide easy access to the local population for post-exposure rabies prophylaxis. Furthermore, stray dog populations are considerable and attempts to control rabies by mass campaigns of dog vaccination have not received sufficient attention from the national health authorities. To address these challenges, an expanded program to control rabies needs to be initiated by the Malagasy authorities.
View
Laboratory Surveillance of Rabies in Humans, Domestic Animals, and Bats in Madagascar from 2005 to 2010
Article
Full-text available
  • Jan 2011
Background. Rabies virus (RABV) has circulated in Madagascar at least since the 19th century. Objectives. To assess the circulation of lyssavirus in the island from 2005 to 2010. Materials and Methods. Animal (including bats) and human samples were tested for RABV and other lyssavirus using antigen, ribonucleic acid (RNA), and antibodies detection and virus isolation. Results. Half of the 437 domestic or tame wild terrestrial mammal brains tested were found RABV antigen positive, including 54% of the 341 dogs tested. This percentage ranged from 26% to 75% across the period. Nine of the 10 suspected human cases tested were laboratory confirmed. RABV circulation was confirmed in 34 of the 38 districts sampled. No lyssavirus RNA was detected in 1983 bats specimens. Nevertheless, antibodies against Lagos bat virus were detected in the sera of 12 among 50 Eidolon dupreanum specimens sampled. Conclusion. More than a century after the introduction of the vaccine, rabies still remains endemic in Madagascar.
View
Illegal captive lemurs in Madagascar: Comparing the use of online and in-person data collection methods
Article
  • Feb 2016
Although it is illegal to capture, sell, and trade lemurs, the live capture of lemurs in Madagascar is ongoing and may have impacted over 28,000 lemurs between 2010 and 2013. Only one study has examined this trade and did so using in-person interviews in northern Madagascar. The current study sought to expand this existing dataset and examine the comparability of online surveys to more traditional on-location data collection methods. In this study, we collected data through a web-based survey resulting in 302 sightings of 685 captive lemurs. We also collected data from 171 hotel and 43 restaurant websites and social media profiles. Survey submissions included sightings of 30 species from 10 genera, nearly twice as many species as identified via the in-person interviews. Lemur catta, Varecia variegata, and Eulemur fulvus were the most common species sighted in captivity. Captive lemurs were reported in 19 of Madagascar's 22 administrative regions and most were seen in urban areas near their habitat ranges. This represents a wider geographic distribution of captive lemurs than previously found through in-person interviews. The online survey results were broadly similar to those of the in-person surveys though greater in species and geographic diversity demonstrating advantages to the use of online surveys. The online research methods were low in cost (USD 100)comparedtoon−locationdatacollection(USD100) compared to on-location data collection (USD 12,000). Identified disadvantages included sample bias; most of the respondents to the online survey were researchers and many captive sightings were near study sites. The results illustrate the benefits of incorporating a social science approach using online surveys as a complement to traditional fieldwork. Am. J. Primatol. © 2016 Wiley Periodicals, Inc.
View
Expert Review of Evidence Bases for Managing Monkey Bites in Travelers
Article
  • Jun 2015
  • J TRAVEL MED
The clinical problem discussed in this case report involves the management of an adolescent traveler bitten by a non-captive monkey in Southeast Asia. Treatment decisions and the state of evidence for or against are discussed. To assure successful clinical management of travelers who suffer injuries inflicted by nonhuman primates, clinicians should acquaint themselves with the potential threats and discuss current published recommendations with their patients prior to arriving at a treatment plan. Your patient is a 14-year-old high school student who just returned from a school-sponsored trip to Ko Phi-Phi, in Thailand. She is in your clinic because of a bite to her right hand by a crab-eating macaque monkey inflicted 2 days earlier near Monkey Beach. The bite broke the skin, but she immediately irrigated the wound under a nearby faucet for about 5 minutes. The wound does not look infected. She can move her hand normally and sensation is intact. She is afebrile and otherwise feels fine. She received three doses of rabies vaccine 2 years earlier, prior to moving to Thailand. What is your advice? A recent review from France looked at rabies transmission from nonhuman primates (NHPs) to humans.1 The report cites 159 rabies cases that occurred in NHPs, documented from 1960 to 2013 and 25 human rabies cases following NHP-caused injuries. The review cited data from 14 surveys and studies involving a total of 2000 travelers seeking care for rabies post-exposure prophylaxis (PEP). Nearly one third had been injured by monkeys. If representative of the experience of travelers, this high number of monkey injuries may differ from what occurs in local resident populations. For instance, in Thailand, a large Asian country with high rabies prevalence in feral and stray dogs, Bangkok's Thai Red Cross Animal Bite Clinic collected common animal bite statistics between 2008 … Corresponding Author: Nicholas J. Riesland, MD, Lake Forest Park, 3404 NE 163rd Street, Lake Forest Park, Seattle, WA 98155, USA. E-mail: nickriesland{at}gmail.com
View
Confronting Rabies and Its Treatments in Colonial Madagascar, 1899-1910
Article
  • Jul 2009
Rabies constituted a point of cultural tension and divergence over disease in late nineteenth-century, post-conquest Madagascar. The Pasteur Institute and colonial authorities ascribed an extraordinary importance to rabies, given the means at their disposal, and given the other epidemiological challenges facing them. Local peoples, in turn, met this expertise with some trepidation, and in some cases, outright defiance. This article considers, in turn, colonial health priorities, connections between Malagasy cures and Pasteurian remedies, as well as issues of accommodation, resistance and rumour in a colonial context.
View
View
Royal Society of Tropical Medicine and Hygiene meeting at Manson House, London, 20 March 1997. Epidemiology and control of rabies. The growing problem of rabies in Africa
Article
  • Mar 1998
Although rabies in Africa is relatively insignificant in terms of human mortality, the disease is still relevant because of the high costs of rabies prevention. Over the past 2 decades, demographic, economic and sociopolitical trends in Africa have increasingly favoured the persistence and spread of rabies, while limiting the effectiveness of control measures. Dog rabies predominates throughout most of Africa; the domestic dog is the principal reservoir host as well as the most important source of infection for people. However, wild-life rabies is increasingly a concern, both as a threat to endangered wildlife populations and because of the possible emergence of new maintenance hosts.
View
Understanding Environmental and Anthropogenic Drivers of Lemur Health in Madagascar: The Importance of a One Health Perspective. Unpubl. Doctoral Dissertation
  • Jan 2011
  • M A Barrett
Barrett, M. A. 201 1. Understanding Environmental and Anthropogenic Drivers of Lemur Health in Madagascar: The Importance of a One Health Perspective. Unpubl. Doctoral Dissertation. Duke University, Durham. Available at <https://dukespace.lib.duke.edu/dspace/handle/1 01 61 /3885>
Madagascar: the Bradt travel guide. Bradt Travel Guides Ltd
  • Jan 2007
  • H Bradt
Bradt, H. 2007. Madagascar: the Bradt travel guide. Bradt Travel Guides Ltd., U.K.
Shifting ranges and conservation challenges for lemurs in the face of climate change
  • 8
  • J L Brown
  • A D Yoder
Brown, J. L. and Yoder, A. D. 201 5. Shifting ranges and conservation challenges for lemurs in the face of climate change. Ecology and Evolution 5, 6: 1 1 31 -1 1 42. <https://doi.org/1 0.1 002/ece3.1 41 8>