Characterizing Rabies Epidemiology in Remote Inuit ...

EcoHealth DOI: 10.1007/s10393-014-0923-1

Ó 2014 International Association for Ecology and Health

Original Contribution

Characterizing Rabies Epidemiology in Remote Inuit ´ bec, Canada: A ‘‘One Health’’ Communities in Que Approach Cećile Aenishaenslin,1,2 Audrey Simon,1,2 Taya Forde,3 Andre´ Ravel,1,2 Jean-François Proulx,4 Christine Fehlner-Gardiner,5 Isabelle Picard,6 and Denise Be´langer1,2 1

Groupe international ve´te´rinaire, Faculte´ de me´decine ve´te´rinaire, Universite´ de Montreál, 3200 Sicotte, C.P. 5000, Saint-Hyacinthe, QC J2S 7C6, Canada 2 Groupe de recherche en épide´miologie des zoonoses et sante´ publique, Faculte´ de me´decine ve´te´rinaire, Universite´ de Montreál, 3200 Sicotte, C.P. 5000, Saint-Hyacinthe, QC J2S 7C6, Canada 3 Faculty of Veterinary Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary, AB T2N 4N1, Canada 4 Nunavik Regional Board of Health and Social Services, C.P. 900, Kuujjuaq, QC J0M 1C0, Canada 5 Centre of Expertise for Rabies, Canadian Food Inspection Agency (CFIA), 3851 Fallowfield Road, Ottawa, ON K2H 8P9, Canada 6 Ministe`re de l’Agriculture des Peˆcheries et de l’Alimentation du Que´bec (MAPAQ), 200 chemin Sainte-Foy, Que´bec, QC G1R 4X6, Canada

Abstract: Rabies is endemic throughout arctic areas including the region of Nunavik, situated north of the 55th parallel of Que´bec, Canada, and raises public health concerns. The aim of this paper is to provide a descriptive overview of the temporal and regional distributions of three important components of arctic rabies in Nunavik from 1999 to 2012, following a ‘‘One Health’’ approach: animal rabies tests and confirmed cases, dog vaccination, and human consultations for potential rabies exposures. Forty-four cases of rabies, involving mainly arctic and red foxes, were confirmed in animals during this period. The mean number of dogs vaccinated per 1,000 inhabitants was highly variable and lower in the Hudson region than the Ungava region. 112 consultations for potential rabies exposure were analyzed, of which 24 were exposure to a laboratory confirmed rabid animal. Children less than 10 years of age were the age group most commonly exposed. The median time between potential exposure and administration of the first post-exposure prophylaxis dose was four days. This study confirms that the risk of human exposure to rabid animals in Nunavik is present and underlines the need to follow a ‘‘One Health’’ approach to prevent rabies in humans in similar contexts worldwide. Keywords: Arctic, dog, fox rabies, one health, wildlife, zoonoses

INTRODUCTION Rabies is endemic throughout most parts of the Arctic, including northern Canada (north of 60°N), Greenland,

Correspondence to: Cećile Aenishaenslin, e-mail: [email protected]

Svalbard, and northern regions of the former Soviet Union (Tabel et al. 1974; Mørk and Prestrud 2004; Orpetveit et al. 2011) and is caused by a unique variant of the rabies virus referred to as the arctic rabies virus variant (ARVV). Several studies report that ARVV is not limited to Arctic regions, rather, related variants are widely dispersed throughout the

C. Aenishaenslin et al.

Northern Hemisphere as far as southern Asia, where it circulates in dogs and wild canids such as red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) (Mansfield et al. 2006; Nadin-Davis et al. 2007; Kuzmin et al. 2008). In the far north, the arctic fox (Vulpes lagopus) is considered to be the main reservoir of ARVV; however, the red fox is another important reservoir species in regions further south (Rosatte 1988), and striped skunks (Mephitis mephitis) harbor a similar variant in Southwestern Ontario (Nadin-Davis et al. 2006). Considering the broad geographic range of ARVV, several other species could enable this variant to circulate (Mansfield et al. 2006). Little is known about the epidemiology of rabies caused by ARVV, and particularly, there are some important knowledge gaps regarding how this zoonotic viral agent spreads among the reservoir hosts and persists in arctic fox populations for which the densities are considerably lower than those required to maintain the virus in red foxes populations in Europe (Mørk and Prestrud 2004). According to Anderson et al. (1981), the density of red foxes has to be at least 1.0 fox per km2 to allow an epizootic to occur through a population, but fox rabies has survived in Canada where fox densities were 0.5). Between 1999 and 2011, 3–16 animals (median = 7) from Nunavik were sent annually for rabies testing and 0–8 animals (median = 2) were annually positive (Table 1) with some variation between the Hudson and the Ungava regions (Fig. 2). The number of submissions and positive results increased in both regions in Nunavik in late 2011 and early 2012: over the 5-month period between November 1st 2011 and March 31st 2012, 20 animals were submitted, 15 (75%) of which were rabies positive. On a monthly basis between 1999 and 2011, over two thirds of all rabid animals (23 of

33) were detected between the months of December and May, with a peak of seven cases in March (data not shown). Dogs were the most frequent animal species submitted for rabies testing (61% of all animals tested), but relatively few of them (15%) were positive (Table 2). Conversely, 77% of all wild animals submitted for testing were positive (Table 2). Red foxes accounted for 41% (18/44), and arctic foxes for 27% (12/44) of all positive samples. The two-dimensional map resulting from the MCA accounted for most (70%) of the inertia (or variance) in the data (Fig. 3). Years are not shown because it added little to the map. Along the first axis, the map shows a marked opposition between ‘‘contact: none’’, ‘‘positive test results’’ and the wild species, especially red foxes, on the right side and ‘‘negative test results’’ and ‘‘dog’’ on the left side, illustrating the finding that most wild animals submitted did not have domestic animal or human contact and were positive, whereas the submitted dogs mostly tested negative. On the second axis, no possible groupings are obvious; nevertheless, there might be differences between arctic foxes and wolves, between ‘‘contact: unknown’’ and of other type, and between March–May and September–November, possibly with more submissions of wolves during the March–May period.

Dog Vaccination Between January 1st 1999 and March 31st 2012, a total of 6,243 rabies vaccines was administered to dogs by the MAPAQ program in the 14 villages, ranging from 238 to 832 dogs vaccinated per year (annual median = 517, annual median in Hudson = 253, min = 0, max = 302, annual median in Ungava = 295, min = 170, max = 570). Hudson villages were not visited in 2006 and in 2008 because of technical constraints. No animal vaccinations were conducted by MAPAQ veterinarians between January and March 2012. The number of dogs vaccinated per 1,000 inhabitants was highly variable (Fig. 2) and significantly lower in the Hudson region (median = 41.4) than the Ungava region (median = 63.3) (Mann–Whitney test; P < 0.001). This difference is not due to the absence of vaccination in the Hudson region in 2006 and 2008 (still significantly lower in the Hudson (median = 42.9) than the Ungava region (median = 64.2) without considering these 2 years (Mann-Whitney test; P = 0.002)). In Ungava, the lowest number of dogs vaccinated against rabies per 1,000 inhabitants occurred in 2009 with 36.4. In the same year, two dogs were diagnosed with rabies in this region. The low number of cases does not allow for statistical inference

Characterizing Rabies Epidemiology in Remote Inuit Communities in Que´bec

Table 1. Dogs vaccinated against rabies, animal rabies cases, rabies diagnostic tests performed, and human consultation for potential exposure to rabies in Nunavik from January 1999 to March 2012. Year

1999

2000

2001

2002

2003

2004

2005

2006

2007

2008

2009

2010

2011

Region

Hudson Ungava Total Hudson Ungava Total Hudson Ungava Total Hudson Ungava Total Hudson Ungava Total Hudson Ungava Total Hudson Ungava Total Hudson Ungava Total Hudson Ungava Total Hudson Ungava Total Hudson Ungava Total Hudson Ungava Total Hudson Ungava Total

Dog vaccination

Rabies cases

Rabies tests

Nb of villages visited

Nb of dogs vaccinated

Nb of dogs vaccinated per 1000 inhabitants

Dogs

Wildlifea

Total

Nb of tests (all species)

Proportion of tests positive (%)

6 7 13 6 5 11 6 7 13 6 7 13 7 7 14 6 6 12 6 7 13 0 2 2 7 7 14 0 5 5 5 6 11 6 6 12 6 6 12

93 290 383 123 191 314 256 296 552 301 406 707 273 378 651 302 215 517 262 570 832 0 282 282 253 296 549 0 238 238 102 170 272 89 295 384 262 300 562

17.5 67.3 39.8 23.1 44.4 32.6 48.1 68.7 57.3 49.3 86.8 65.6 44.7 80.9 60.4 49.4 46.0 47.9 42.9 121.9 77.2 0.0 60.3 26.1 41.4 63.3 50.9 0.0 50.9 22.1 16.7 36.4 25.2 14.6 63.1 35.6 42.9 64.2 52.1

0 0 0 1 0 1 0 0 0 0 0 0 1 0 1 0 0 0 0 0 0 0 2 2 0 0 0 0 0 0 0 2 2 0 0 0 1 0 1

4 0 4 0 1 1 2 1 3 2 0 2 2 0 2 0 3 3 1 0 1 0 0 0 1 0 1 0 1 1 0 2 2 0 0 0 2 5 7

4 0 4 1 1 2 2 1 3 2 0 2 3 0 3 0 3 3 1 0 1 0 2 2 1 0 1 0 1 1 0 4 4 0 0 0 3 5 8

5 4 9 3 3 6 11 1 12 4 3 7 3 1 4 3 12 15 3 0 3 3 4 7 3 2 5 1 4 5 1 6 7 0 5 5 8 8 16

80 0 44.4 33.3 33.3 33.3 18.2 100 25 50 0 28.6 100 0 75 0 25 20 33.3 – 33.3 0 50 28.6 33.3 0 20 0 25 20 0 66.7 57.1 – 0 0 37.5 62.5 50

Nb of consultations for potential exposureb (Confirmed exposures)

5 (0)

18 (13)

7 (0)

7 (1)

15 (3)

15 (0)

2 (1)

11 (1)

2 (0)

11 (2)

6 (1)

***

***


Table 1. continued Year

Region

Dog vaccination

Rabies cases

Rabies tests

Nb of Nb of dogs Nb of dogs Dogs Wildlifea Total Nb of tests Proportion villages vaccinated vaccinated (all species) of tests per 1000 visited positive (%) inhabitants 2012**

Total

Median

c

Hudson Ungava Total Hudson Ungava Total Hudson Ungava Total

– – – – – – – – –

– – – 2316 3927 6243 253 295 517

– – – – – – 41.4 63.3 47.9

1 2 3 4 6 10 0 0 0

6 1 7 20 14 34 1 0 2

7 3 10 24 20 44 1 1 2

7 4 11 55 57 112 3 4 7

100 75 90.9 43.6 35.1 39.3 – – –

Nb of consultations for potential exposureb (Confirmed exposures)

***

99 (22)

7 (1)

**Data reported here are only from January 1st to March 31st of 2012. ***Numbers of human consultations for 2010, 2011 and 2012 were not available at the time of writing. a Wildlife represents rabies cases identified in the following species: red foxes, arctic foxes and wolves. b Human data from 1996–1998 are not shown in this table. c Medians were calculated for the period 1999–2011, excluding 2012 for all items except for the number of human consultations, for which only 1999 to 2009 were included.

between dog vaccination and the occurrence of rabies in the dog population.

Human Exposure Between 1996 and 2009 inclusive, a total of 112 consultations for potential exposure to a rabid animal were recorded. In 41 (37%) of the 112 cases of potential exposure, the animal responsible was sent for analysis at CFIA and 24 (59%) of these were confirmed to be infected with ARVV (Table 3). Children under 10 years old represented 11 (50%) of the 22 confirmed cases of exposure to a rabid animal where age of the victim was known. Hudson was the main region of residence for both potential exposures (55%) and confirmed exposures (71%). Consultations for potential exposure were most frequently sought due to dog bites (68%). However, in cases where the animal was confirmed rabid, mucous membrane contamination was the most common type of exposure (50%), followed by dog bites (25%). Overall, 62 people (55%) started a PEP, and 46 of them (74%) completed it. All people who were exposed to a laboratory-confirmed rabid animal completed the PEP treatment. Time between potential exposure and consultation was variable (median time = 1.5 days, range = 0–23 days). Time between potential exposure and administration of the first

PEP dose was known for 47 of the 62 cases. Among these, 16 people (34%) received their first dose within 48 h of potential exposure. The median time between potential exposure and administration of the first PEP dose was 4 days (range = 0– 23 days). 54% (13 of the 24) confirmed cases of exposure to a rabid animal received their first dose after more than 14 days. For the 41 cases where the animal was sent for analysis, the time between exposure and reception of the diagnostic results ranged from 2 to 31 days, with a median delay of 7 days.

DISCUSSION This study is the first to describe the temporal and regional distributions of three important components of rabies surveillance and prevention in Nunavik: rabies tests and confirmed cases (January 1999–March 2012), dog vaccination (January 1999–March 2012), and human exposures (January 1996–December 2009).

Rabies Tests and Confirmed Animal Cases This study shows that samples are irregularly submitted to the CFIA for rabies diagnosis and that most of the samples submitted are from domestic dogs. This can be explained


Figure 2. Annual distribution of positive and negative samples tested by the Canadian Food Inspection Agency for the Nunavik region (a), and number of dogs vaccinated per 1,000 inhabitants by year in Hudson region (b) and Ungava region (c).

by the design of the passive surveillance system, which limits testing to suspect animals that have potentially exposed humans or domestic animals. Wild animals are less likely to enter into contact with humans, and exposure of domestic animals to wildlife may not always be recognized.

Furthermore, wild animals are less likely to be captured after a human or domestic animal contact. Hence, cases diagnosed through this system very likely represent an underestimation of the number of rabies cases in the region.


Table 2. Samples submitted for rabies diagnostic testing per species (January 1999–March 2012). Species

Nb tested

Nb positive

Percentage positive (%)a

Percentage of rabies cases (%)b

Dogs Red foxes Arctic foxes Wolves Total

68 20 18 6 112

10 18 12 4 44

14.7 90.0 66.7 66.7 39.3

22.7 40.9 27.3 9.1 100.0

a

% of positive samples among species-specific samples tested. % of all rabies cases for all species.

b

Figure 3. Map from the multiple correspondence analysis of the 112 rabies tests performed on animals in Nunavik, 1999–2012. It shows the relative position of the categories that describe the tested animals in terms of test results (spotted bubble positive or negative), the type of contact with humans the animal had [gray bubbles bite, other (no bite), none, unknown], the kind of animal (black bubbles artic fox, dog, red fox, wolf), the region (white bubbles Hudson or Ungava), and the trimester (dotted bubble December to February, March to

May, June to August, and September to November). The first and the second axes encompass 76% of the total inertia (synonymous of with variance for categorical variables) present in the multidimensional data set. The size of the bubbles is proportional to the number of animals within the category the bubble represents. Dark bold words indicate categories that contribute to axis 1 and dark underlined ones indicate categories that contribute to axis 2. Gray words indicate categories that provide no contribution to axis 1 and 2.

Overall, 39% of the submitted samples were positive (31% when excluding 2011 and 2012). This is comparable to the proportion of positive tests found previously in the Canadian territories throughout the arctic region, where 27% of the samples tested were found positive from 1999 to 2009 (CFIA 2012, unpublished data). In Alaska, United States, a proportion of positive samples of 14% was reported in 2011 (Blanton et al. 2012). The occurrence of rabies test submissions and confirmed rabies cases was not different in the Hudson and Ungava regions. In both

regions, the proportion of confirmed rabid animals was much higher for wild species than for domestic ones. Several studies have estimated the prevalence of rabies among trapped arctic foxes showing no behaviorial or clinical signs compatible with rabies in enzootic and epizootic periods. Prevalences of 0.3 to 3% in enzootic periods and up to 75% in epizootics have been reported (Secord et al. 1980; Prestrud et al. 1992; Ballard et al. 2001; Mørk et al. 2011). Although this study does not allow for prevalence to be evaluated, the high proportion of positive wild


Table 3. Description of human potential and confirmed exposures to rabies in Nunavik from 1996 to 2009.

Number of consultations

Age of the patient 0–9 10–19 20–29 30–39 40–49 50–59 60 and above Unspecified Region of residence Hudson Ungava Type of exposure Dog bites Fox bites Other bites Per skin contacts other than bite Mucous membrane Unspecified Type of intervention PEP completed PEP not completed No PEP Unspecified Time between exposure and consultation 14 days Unspecified Time between exposure and PEP administrationa 14 days Unspecified a

Potential exposures

Confirmed exposures

112

24 (21%)

Nb

%

Nb

%

41 13 9 13 6 5 3 22

36.6 11.6 8.0 11.6 5.4 4.5 2.7 19.6

11 2 3 2 3 1 0 2

45.8 8.3 12.5 8.3 12.5 4.2 0.0 8.3

61 51

54.5 45.5

17 7

70.8 29.2

76 6 2 7 18 3

67.9 5.4 1.8 6.3 16.1 2.7

6 1 0 4 12 1

25.0 4.2 0.0 16.7 50.0 4.2

46 16 41 9

41.1 14.3 36.6 8.0

24 0 0 0

100.0 0.0 0.0 0.0

32 17 10 7 10 8 14 14

28.6 15.2 8.9 6.3 8.9 7.1 12.5 12.5

2 0 0 1 6 1 13 1

8.3 0.0 0.0 4.2 25.0 4.2 54.2 4.2

8 8 4 3 7 3 14 15

12.9 12.9 6.5 4.8 11.3 4.8 22.6 24.2

1 1 0 1 3 3 13 2

4.2 4.2 0.0 4.2 12.5 12.5 54.2 0.1

Data presented for this variable describe the distribution of the subset of 62 cases of consultations where the patient started a PEP treatment (24 cases where confirmed exposure to rabies), as indicated in the summary of intervention above.


animals (up to 90% of red foxes submitted were positive for rabies) raises concerns about the extent of rabies infection in Nunavik wildlife and the risk of exposure associated with activities such as trapping and hunting. An increased risk of rabies exposure in northern trappers was also suggested by a previous study in Alaska, where a high rabies virus neutralizing antibody titre was found in one unvaccinated fox trapper (Follmann et al. 1994). In Inuvik, the area within the Northwest Territories where the majority of positive rabies cases have been detected, the disease follows a 4-year cycle (Mitchell and Kandola 2005). A 3–4-year cyclic occurrence of epizootics has also been noted in northern and western Alaska (Follmann et al. 1992; Mørk and Prestrud 2004; Kim et al. 2013). One hypothesis is that the epidemic cycle of rabies could follow the natural fluctuations in the fox population, with rabies peaks corresponding to high densities that shadow fluctuations in the density of prey species, especially small rodents (Hall and Mallory 1988). From January 1999 to December 2010, the number of rabies cases in Nunavik remained relatively constant (range 0–4 cases/ year), without evidence of cyclic peaks of cases. In contrast, the number of confirmed animal rabies cases increased in 2011 and early 2012 (n = 18) suggesting the emergence of an epizootic in the region. This is supported by the detection of 12 cases of rabies caused by ARVV in the neighboring region of Labrador in the first trimester of 2012 (CFIA 2012). Fourteen of the 2011–2012 Nunavik cases are wildlife cases and only one of these was associated with a human exposure, although eight were associated with a domestic animal exposure. In 2011 and 2012, observations of a larger number of wild animals presenting suspect behaviors near villages were reported by local residents; cases where there was no human or domestic animal contact were analyzed by CQSAS and subsequently confirmed by CFIA. These observations could suggest a higher prevalence of rabies in wildlife or alternatively, variations in wildlife behavior that brings them closer to villages, favoring that suspect animals are more easily seen, captured and sent for analysis by residents. Some studies have suggested that climate change may be linked to these behavior changes, by reducing prey availability for foxes in their natural habitats (decreasing rodent populations, and accessibility of marine mammals on the sea ice) (Kim et al. 2013). As a consequence, foxes could tend to seek food near human habitations. Moreover, the increase of animal testing during this period by CQSAS most probably contributed to a higher detection rate of rabies cases in wildlife.

Active surveillance of wild foxes would have been necessary to support the hypothesis of an actual epizootic of rabies.

Dog Vaccination This study suggests that there may be unequal vaccination coverage between the two regions of Nunavik, Ungava and Hudson, illustrated by the differences in the regional annual numbers of dogs vaccinated per 1,000 inhabitants. Unequal vaccination coverage may be due to differences in local participation in the MAPAQ vaccination program, as the MAPAQ veterinarians only visit the villages that submit a request for such services. However, this interpretation must be taken with caution. The number of dogs vaccinated per 1,000 inhabitants is an imperfect indicator of the vaccination coverage in the dog population as there might be differences in the number of dogs per inhabitant between these regions. Calculation of the percentage of dogs vaccinated within the total number of dogs should be used for comparisons if possible. The size of the dog population in Nunavik regions is unknown, and the real vaccination coverage could not be calculated for this study. As MAPAQ veterinarians subjectively report that there is no evidence of important differences in the number of dogs per inhabitant between both regions, this indicator (number of dogs vaccinated per 1,000 inhabitants) was used for comparisons. These observations underline that actions should be taken to ensure that the two regions are equally protected against potential exposure from rabid animals by building a good immunity in the dog populations. This study also reveals that there is a need for better dog population estimates in Nunavik, including better comprehension of the temporal and spatial variations of the dog populations in the different villages, including freeroaming dogs. Several villages practice sporadic free-roaming dog eradication when the dog populations reach a high density. It is therefore likely that the dog population size fluctuates within a year and from one year to another within villages. The isolated locations of the villages in Nunavik make the administration of preventive animal health services, including rabies vaccination, particularly challenging; temporal variations in the dog vaccination coverage can therefore have an impact on the risk of rabies exposure. In addition to dog vaccination, vaccination of foxes should be evaluated as a complementary method of rabies prevention in Nunavik. This is supported by the high proportion of rabies-positive wild animals found during the study period. Although Arctic rabies in red foxes has been controlled by wildlife vaccination (oral-baiting


vaccination or trap-vaccinate-release strategies) in other jurisdictions within a limited area, it presents some distinct challenges in a region as large as Nunavik (Mansfield et al. 2006; MacInnes et al. 2001), especially with regards to the sparse population of arctic foxes combined with the possible loss of efficiency of vaccines used in the field in arctic conditions (Mørk and Prestrud 2004). Lyophilized oral vaccines have produced adequate immunity of arctic foxes in captivity and were suggested as an alternative of liquid oral vaccines in frozen conditions (Follmann et al. 2004). A review of recent advances in wildlife rabies control techniques is available in Rosatte (2011).

Human Exposures Between 1996 and 2009, the overall number of human exposures to laboratory-confirmed rabid animals remained low in Nunavik, and generally varied between 0 and 3 cases annually, with one rare and unique event in 2000, where 13 people were exposed to a single rabid animal that presented a paralytic form of rabies. Half of the confirmed cases of potential exposure were children under 10 years old. Previous studies have shown that children tend to be bitten near the head more often than adults due to their size and that the incubation period of rabies can be shorter in this population (Wilde et al. 2003), making them a major risk group. Another preoccupying issue is the time between exposure and PEP administration found in this study (from 0 to 23 days, median of 4 days). For several cases, this period exceeded the recommendation of the Ministry of Health and Social Services of Que´bec (MSSS), which advocates a maximum delay of 48 h for such situations (MSSS 2012). This long median delay is not due to an inadequate treatment of potential exposure by local health professionals, who are well trained to efficiently manage cases of potential rabies exposure by administrating PEP; rather, it is dependent on the delay between exposure and consultation to the local health center (median of 4 days, when considering only people who started a PEP). When a rabies case is detected an investigation is conducted by public health professionals to identify people who were in contact with the rabid animal, including contacts with mucous membrane (for example, with dog saliva), to administer PEP, as was the case for the 2000 event. This protocol often leads to the identification of additional exposed individuals several days following the exposure. This protocol also explains the high proportion of this type of exposure (with mucous membranes) in the group of confirmed exposures. An ‘‘in depth’’ analysis of the context of exposure by a qualitative

analysis of medical files or by interviews with patients and with local health professionals would help to confirm and understand the reasons for these long delays between exposure and consultation, exposure and PEP administration, and exposure and reception of the animal rabies status. Despite the need for further information on human exposures, these observations on rabies exposure in children and its management (two thirds of the patients with a confirmed exposure to rabies received PEP more than 7 days after exposure) in Nunavik underline a major public health issue, and highlight the need to reinforce rabies prevention education within the population, specifically about routes of viral entry and the importance of a rapid consultation after contact with a suspect animal. Moreover, in order to cost-effectively manage potential rabies exposures (e.g., to allow discontinuation of PEP if the animal tests negative), the time between submission of a sample and reception of the diagnostic results should be reduced. If the isolated location of the Nunavik region makes this delay difficult to reduce, the implementation of a local laboratory for rabies testing might be considered. We recognize that the use of annual means to describe the distribution of PEP treatments in this case has important limitations. Nevertheless, for the purpose of comparisons, the mean annual rate of PEP in the Nunavik population based on the 46 completed PEP treatments from 1996 to 2009 can be estimated to be 30.5 PEP for 100,000 inhabitants (using the 2006 census for the human population), which is high when compared to the mean rate of 7.7 PEP per 100,000 inhabitants for Que´bec as a whole in 2005 (MSSS 2012). The Nunavik rate is also higher than rates reported from similar regions with endemic arctic rabies, such as in Alaska, where 7.42 PEP per 100,000 inhabitants was reported between 1975 and 1980 (Middaugh and Ritter 1982) and in the Northwest Territories, where a rate of 23.0 PPE per 100,000 people was described (Mitchell and Kandola 2005). Factors that could contribute to high rates of PEP administration in Nunavik include the rabies enzootic situation of the region which dictates rapid PEP administration when an exposure is suspected, the lengthy period between consultation and receipt of results from laboratory testing due to the remote location or a difficulty in verifying the immunization status of the dog in question. In summary, this study has shown that residents of Nunavik, and children in particular, are at risk of exposure to rabies, and that this risk could be increasing, as suggested by the 2011–2012 data. Hence, we recommend that a global approach be adopted for rabies prevention in Nunavik.


Prevention and control actions should follow the ‘‘One Health’’ model, with integrated actions toward public health, animal health and ecosystem health. More precisely, this study highlights the need to maintain and reinforce the dog vaccination program in this region, to enhance surveillance of rabies with a special emphasis on wildlife, to improve dog population estimates, to implement a perennial dog population control program, to evaluate the possibility of vaccinating wildlife against rabies in the region, and to improve education on rabies prevention and dog bites in the villages with a focus on children. The ‘‘One Health’’ approach leads to more comprehensive and efficient actions to tackle the gaps in rabies prevention and control in Nunavik, and should serve as a model for rabies prevention in similar contexts worldwide.

ACKNOWLEDGEMENTS The authors would like to acknowledge Michelle Dionne and Magaly Pe´pin from the ministe`re de l’Agriculture, des Peˆcheries et de l’Alimentation du Que´bec for putting together vaccination data, Manon Simard from the Nunavik Research Center for useful information on Nunavik regional characteristics, and staff from the CFIA Centre of Expertise for Rabies and CQSAS for the laboratory analyses.

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