Harvested white-tailed deer as sentinel hosts for early establishing Ixodes scapularis populations and risk from vector-

borne zoonoses in southeastern Canada

Bouchard, C.1, Leighton, P.1, Beauchamp, G. 1, Nguon, S.2, Trudel, L.3, Milord, F.2, Lindsay, L.R.4, Bélanger, D.1, Ogden, N.H.1,5

1

Groupe de recherche en épidémiologie des zoonoses et santé publique, Faculté de médecine

vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec, Canada

2

Direction des risques biologiques et de la santé au travail, Institut national de santé publique du

Québec, Montréal, Québec, Canada

3

Laboratoire de santé publique du Québec, Institut national de santé publique du Québec, Sainte-

Anne-de-Bellevue, Québec, Canada

4

Zoonotic Diseases and Special Pathogens, Public Health Agency of Canada, National Microbiology

Laboratory, Winnipeg, Manitoba, Canada

5

Zoonoses Division, Centre for Food-borne, Environmental and Zoonotic Infectious Diseases, Public

Abstract

Due to recent establishment of the tick Ixodes scapularis Say in southeastern Canada, tick-borne

zoonoses (Lyme disease, human granulocytotropic anaplasmosis and human babesiosis) are of

growing concern for public health. Using white-tailed deer culled in southwestern Quebec during

2007-2008, we investigated whether hunter-killed deer could act as sentinels for early establishing I.

scapularis tick populations and for tick-borne disease risk. Accounting for environmental

characteristics of the site of culling, and demographic variables of culled deer (i.e. age and sex) we

investigated whether tick infestation levels of deer could identify locations of known tick populations

detected in active surveillance, and/or presumed tick populations detected by passive surveillance.

We also used spatial cluster analyses to identify spatial patterns of tick infestation of deer and

occurrence of tick-borne zoonoses infection in ticks collected from the deer. Adult I. scapularis ticks

were found on 15% of the 583 deer examined. Adult male deer had the greatest number of adult I.

scapularis (nearly 90% of the ticks collected). Overall, 3%, 15% and 0% of the ticks collected were

PCR-positive for Borrelia burgdorferi, Anaplasma phagocytophilum and Babesia microti, respectively.

Our statistical analyses suggest that sex and age of deer, temperature, precipitation and an index of

tick dispersion by migratory birds were significantly associated with I. scapularis infestation levels.

Cluster analysis identified significant clusters of deer carrying ticks PCR-positive for A.

phagocytophilum, and for deer carrying 2 or more I. scapularis. Our study suggests that hunter-killed

deer may be effective as sentinels for emerging areas of tick-borne anaplasmosis. They may have

limited use as sentinels for early emerging I. scapularis tick populations and emerging Lyme disease

risk.

Keywords: Ixodes scapularis, Anaplasma phagocytophilum, Borrelia burgdorferi, white-tailed deer, environmental factors, public health

Introduction

Ixodes scapularis Say9 is the vector of a number of tick-borne zoonoses including Borrelia burgdorferi

sensu stricto (Borrelia burgdorferi Johnson, Schmidt, Hyde, Steigerwaldt & Brenner), Anaplasma

phagocytophilum Dumler, Barbet, Bekker, Dasch, Palmer, Rikihisa & Rurangirwa and Babesia microti

Franca which cause Lyme disease, human granulocytotropic anaplasmosis (HGA) and human

babesiosis, respectively (Thompson et al. 2001). I. scapularis ticks are expanding their geographic

range northwards into southeastern and south central Canada (Ogden et al. 2009, Ogden et al. 2010,

Bouchard et al. 2011, Leighton et al. 2012) and the diseases transmitted by I. scapularis represent a

dynamic and emerging public health challenge in Canada (Ogden et al. 2005). I. scapularis is a host

generalist parasitizing several species such as rodents, birds, medium and large sized mammals and

reptiles (Tsao 2009).

However, the positive correlation between I. scapularis abundance and white-tailed deer (Odocoileus

virginianus) density is well documented in eastern North America (Wilson et al. 1988, Wilson et al.

1990, Magnarelli et al. 1993, Magnarelli et al. 1995, Ginsberg and Zhioua 1999, Rand et al. 2003). This

is to be expected as white-tailed deer are the principal hosts for adult I. scapularis ticks (Piesman and

Spielman 1979, Wilson et al. 1990). Since deer are essential to stable I. scapularis populations, they

could give an accurate estimate of tick population distribution (Keefe et al. 2009). In addition,

hunter-harvested deer may be very useful sentinels for tick and tick-borne zoonoses surveillance

programs because of their availability and the fact that they provide tick samples from privately

In addition, white-tailed deer are considered reservoirs of A. phagocytophilum (Massung et al. 2005).

However, they are thought reservoir incompetent (and zooprophylactic by clearing infection from

feeding ticks) for B. burgdorferi (Loken et al. 1985, Telford et al. 1988, Lacombe et al. 1993) and may

also be refractory to infection with B. microti (Piesman et al. 1979).

In southeastern and south central Canada new I. scapularis populations and foci of tick-borne

zoonoses are emerging at present (Ogden et al. 2010, Bouchard et al. 2011, Leighton et al. 2012) as

they are in other parts of North America (Hamer et al. 2010) likely driven in part by abiotic factors

(Ogden et al. 2010, Estrada-Peña et al. 2001, Randolph, 2004) and there is a need to develop

methods of surveillance to identify where these areas of risk to public health are emerging (Koffi et

al. 2012). Such methods should aim to be flexible to detect other tick species (e.g. Amblyomma

americanum) that may also emerge in the future.

In this study, we evaluated the use of harvested white-tailed deer as sentinel hosts for adult ticks as

an early indicator of newly establishing populations of ticks and tick-borne zoonoses, that may be

useful for surveillance purposes, in a region in southwestern Quebec where considerable field studies

and surveillance activity have already taken place to act as a “gold standard” for the existence of tick

populations (Ogden et al. 2010). We investigated deer demography (age and sex) as well as

environmental (habitat and climate) factors as determinants of tick infestation levels (tick count per

deer; refer hereafter by tick infestation levels). Adjusting for relevant significant factors we then

assessed to what extent tick infestation levels of hunter-killed deer were influenced by known spatial

distributions of tick populations obtained from data of active and passive surveillance conducted in

deer-carried ticks could identify locations where transmission cycles of tick-borne zoonoses are

becoming established.