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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.
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: xxxx.
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
18981958;
19541973
Number of lemurs tested for rabies in Madagascar (and number that
tested positive for rabies; data also presented for other animals).
B
Jennings 2009
19011910
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
19591991
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
19941998
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
20052010
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: xxxx.
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: xxxx.
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: 149179. 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: xxxx.
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, 18991910. Social History
of Medicine 22, 2: 263282. <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: 58.
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:
19941998. Proceedings of the Southern and Eastern African Rabies Group/World Health Organization
Meeting in Entebbe, Uganda 2931 March, 1999, pp 5862. Éditions Fondation Marcel Mérieux, Lyon,
France. Available at
<https://pdfs.semanticscholar.org/ab2b/dbb344be3ca72feed01ef73aca78d772a288.pdf>
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Madagascar: the Bradt travel guide. Bradt Travel Guides Ltd
  • H Bradt
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  • J L Brown
  • A D Yoder
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