5,154
Views
41
CrossRef citations to date
0
Altmetric
Reviews

Major emerging vector-borne zoonotic diseases of public health importance in Canada

, , , , &
Pages 1-7 | Received 27 Jan 2015, Accepted 06 May 2015, Published online: 25 Jan 2019

Abstract

In Canada, the emergence of vector-borne diseases may occur via international movement and subsequent establishment of vectors and pathogens, or via northward spread from endemic areas in the USA. Re-emergence of endemic vector-borne diseases may occur due to climate-driven changes to their geographic range and ecology. Lyme disease, West Nile virus (WNV), and other vector-borne diseases were identified as priority emerging non-enteric zoonoses in Canada in a prioritization exercise conducted by public health stakeholders in 2013. We review and present the state of knowledge on the public health importance of these high priority emerging vector-borne diseases in Canada. Lyme disease is emerging in Canada due to range expansion of the tick vector, which also signals concern for the emergence of human granulocytic anaplasmosis, babesiosis, and Powassan virus. WNV has been established in Canada since 2001, with epidemics of varying intensity in following years linked to climatic drivers. Eastern equine encephalitis virus, Jamestown Canyon virus, snowshoe hare virus, and Cache Valley virus are other mosquito-borne viruses endemic to Canada with the potential for human health impact. Increased surveillance for emerging pathogens and vectors and coordinated efforts among sectors and jurisdictions will aid in early detection and timely public health response.

Introduction

Zoonoses are infections or infectious diseases transmissible under natural conditions from vertebrate animals to humans and involve a wide range of causal agents including: viruses, bacteria, parasites, fungi, and prions. Emerging zoonoses are defined as newly recognized diseases or those that have increased in incidence or expanded their geographic, host, or vector range. Zoonoses comprise approximately 60% of all known infectious diseases, while 75% of emerging infectious agents are zoonotic.Citation1

The complex ecology of zoonotic infections poses both a challenge to, and opportunities for, surveillance and control. Transmission of zoonotic pathogens occurs through direct human–animal contact, arthropod vectors, inhalation of infectious drops or aerosolized pathogens in the environment, or through ingestion of contaminated food or water. The resulting infection in a susceptible host may be inapparent or manifest, with the latter causing disease. Enteric zoonoses are those that cause gastrointestinal illness, such as Salmonellosis, Campylobacter, and Giardia infections, and are generally transmitted through contaminated food or water, while the category of ‘non-enteric zoonoses’ is a catch-all grouping of diseases that can be divided generally into vector-borne diseases (such as Lyme disease, West Nile virus (WNV), plague), directly transmitted zoonoses (such as Brucellosis, rabies, influenza, and Hantaviruses), environmentally mediated zoonoses (such as Anthrax, Echinococcosis, Leptospirosis), and food-borne parasitic infections (such as Toxoplasmosis, Trichinellosis), although some may have more than one pathway of transmission.

The rate of zoonotic disease emergence has increased markedly since the 1940s as indicated by the increasing incidence of emerging infectious disease events, even after controlling for increasing infectious disease reporting effect.Citation1 This trend is likely due to a combination of demographic changes, land-use alterations, urbanization, increased travel and trade, agricultural practices, encroachment into animal habitat, and possibly also increased awareness.Citation1,Citation2

Ongoing global environmental and socioeconomic changes may create favorable conditions for emergence and transmission of vector-borne diseases in Canada by: (i) the import of vectors and pathogens exotic to Canada through international movements and their subsequent establishment here as has happened in the past with malaria and WNVCitation3 and could occur in the future with Rift Valley fever, Japanese encephalitis, and chikungunya;Citation4,Citation5 (ii) the northward spread of vector-borne pathogens from endemic areas in the USA as has recently happened with Lyme disease and eastern equine encephalitis; and (iii) the re-emergence or resurgence of endemic vector-borne diseases such as WNV, snowshoe hare virus (SSHV), and Jamestown Canyon virus (JCV), which may occur due to changes to their geographic range and ecology driven by environmental changes such as climate change.Citation6,Citation7

Similar environmental and socioeconomic changes (e.g. climate change, and land use changes due to urbanization and agricultural expansion) may impact on wildlife populations that serve as reservoirs of zoonotic diseases, altering the dynamics of transmission amongst natural reservoir hosts, changing the geographic footprint of endemic areas, and altering the likelihood of animal–human transmission (a.k.a. ‘spillover’).

Recognizing the potential need for multi-sector and multi-jurisdictional coordination, we review the state of knowledge on the public health importance of key emerging vector-borne zoonoses in Canada.

Rationale for the review focus

Selection of priority diseases presented in our review was based on the results of a prioritization exercise that was conducted with public health stakeholders across Canada in 2013. The prioritization exercise aimed to assess diseases of public health significance with the highest risk of emergence or re-emergence in Canada: (i) those known to be present in Canada with potential to expand in incidence, impact, or geographic range; (ii) those with potential to arrive from the USA (through range expansion); or (iii) those with potential to be introduced via international travel or trade; with an emphasis on the first group (). A detailed description of the prioritization exercise is outside of the scope of this paper, but we provide a brief summary here as context for disease selection in our review.

Table 1 Non-enteric zoonotic diseases of high-risk of emergence in Canada: 24 diseases included in a prioritization exercise by provincial and territorial public health stakeholders in Canada in 2013

Technical experts from provincial and territorial ministries of health-, agriculture- and/or environment-provided professional perspectives on non-enteric zoonoses for their respective jurisdiction. Methods and criteria for the selection of zoonoses of priority were adapted from Vorou et al. (2008) and are described in detail elsewhere.Citation8 Briefly, each participating jurisdiction (n = 10; includes nine provinces and one territory) completed a questionnaire to assess each pathogen/disease on the basis of six criteria (indices) of disease emergence. The questions asked respondents to assess a pre-defined list of pathogens () according to three internationally accepted indices defining disease emergence (scored as yes/no) and three indices of public health capacity (scored as high/medium/low): (i) increased incidence in humans in the last five years; (ii) increased geographic range (either newly detected in a given jurisdiction in the last five years, or an endemic agent detected in a novel geographic area in a given jurisdiction in the last two years); (iii) detection of the pathogen in novel animal species in the last two years (for endemic agents in a given jurisdiction); (iv) absence of any current animal or vector surveillance systems; (v) necessity for inter-sectoral collaboration in surveillance (between public health and animal health organizations); and (vi) necessity for inter-jurisdictional collaboration in research, surveillance, diagnostic testing, or communication/education. An overall positive index was scored when three or more jurisdictions provided a positive answer for the corresponding pathogen and index. Pathogens with three or more positive indices were identified as high priority. A series of round table discussions was held to discuss the results of the survey and to reach expert consensus on priority non-enteric zoonoses in Canada.

The prioritization exercise identified vector-borne diseases, in particular Lyme disease and other emerging tick-borne diseases, and WNV and other emerging mosquito-borne diseases, as top emerging non-enteric zoonotic disease priorities. Rabies and zoonotic influenza were also identified as high priorities in this exercise; however, these non-vector-borne pathogens are outside the scope of this paper and may be the subject of a future review.

A systematic review was conducted to determine the state of knowledge in Canada on the emerging vector-borne diseases identified as priorities by public health stakeholders. A literature search was performed in consultation with Health Canada Library services to identify published articles from five databases, including MEDLINE, CAB Abstracts, Agricola, EMBASE, and Global Health. A keyword search was performed for English or French language articles published between January 2008 and September 2013 using the following terms: disease name or pathogen name or zoono* or vectorborn* or mosquitoborn* or tickborn* or ‘disease vector’ and Canada or province/territory name. Titles and abstracts were reviewed and subjected to screening using pre-defined inclusion and exclusion criteria, and full article text was reviewed where necessary to confirm inclusion or exclusion. Forward and backward reference tracking approaches were applied to key documents meeting the inclusion criteria to identify additional relevant articles. Articles were included if they related to the epidemiology of the identified priority vector-borne diseases; their human health impact in Canada; geographic range; surveillance, diagnostic testing, and public health awareness/education. Articles were excluded if they related primarily to therapeutics and/or treatment, vaccine development, and/or vaccine safety. More than 450 publications were identified, including research articles, case reports, reviews, and conference proceedings. One hundred eight documents met the inclusion criteria and were retained for full review.

Emerging vector-borne zoonoses in Canada

Emerging vector-borne zoonoses in Canada are caused by a number of bacteria and viruses transmitted to humans by the bite of an infected tick (e.g. Lyme disease – Borrelia burgdorferi) or mosquito (e.g. WNV).

Lyme disease

Lyme disease, caused by the spirochete B. burgdorferi, is an emerging vector-borne disease in Canada due to the northward expansion of the geographic range of the tick vector Ixodes scapularis in southern Canada.Citation9,Citation10 Lyme disease is a multisystem disorder characterized by three clinical stages: early, disseminated, and late Lyme disease.Citation11 Early diagnosis and treatment are needed to prevent more severe disseminated and late Lyme disease, which may present with neurological, cardiac or joint involvement.Citation12

The reported incidence of human Lyme disease cases in Canada is low but increasing. The range of some vector ticks is expanding faster than had been predictedCitation9 and in the eastern portions of this expanding range is generally followed within three–five years by the invasion of tick-borne pathogens such as B. burgdorferi.Citation13 Risk of exposure to infected western blacklegged ticks (I. pacificus) is relatively low and incidence of Lyme disease in British Columbia (BC) is stable. In contrast, significant risk exists or is emerging across the range of I. scapularis, with the exception, for now, of Alberta, Saskatchewan, and Prince Edward island; populations of infected ticks are established in southern parts of Manitoba, Ontario, and Quebec, and in certain locations in New Brunswick and Nova Scotia.Citation11,Citation14,Citation15,Citation16,Citation17,Citation18,Citation19,Citation20,Citation21

Climate change is anticipated to accelerate the geographic spread and intensity of transmission of Lyme disease in Canada.Citation10 The progressive pattern of Lyme risk emergence is consistent with an association with warming temperatures, and I. scapularis tick population establishment has been shown to be driven by temperature suitability at provincial and national scales. Additionally, there is a low risk of Lyme disease being contracted almost anywhere in CanadaCitation22 due to the transport of infected ticks over large geographic distances by migratory birds.Citation23,Citation24,Citation25,Citation26

Lyme disease has been nationally notifiable in Canada since 2009 and has also been nationally notifiable in the USA since 1991. Through a combination of increased transmission risk, but also possibly increased awareness, human cases of Lyme disease reported in Canada have increased dramatically, from 64 cases in 2005 to nearly 700 cases in 2013 (PHAC, unpublished data), although there may be considerable underreporting of this disease, e.g. an estimated 40% underreporting of Lyme disease cases in BC in 1997–2008.Citation27 In the USA, over 30 000 probable and confirmed cases of Lyme disease are reported each year to the Center for Disease Control and Prevention, with the majority of cases in the North Central and Northeastern states (Connecticut, Delaware, Maryland, Massachusetts, Minnesota, New Jersey, New York, Pennsylvania, Rhode island, and Wisconsin) (http://www.cdc.gov/lyme/stats/index.html), although recent reports from Center for Disease Control and Prevention suggest considerable under-reporting occurs and that 300 000 cases a year is a more realistic incidence.

Studies on the genetic diversity,Citation28,Citation29 population structure,Citation30 ecology,Citation31 and dynamicsCitation32 of the Lyme disease system will help to improve our understanding of the risk of this disease in Canada and inform development of appropriate public health action for surveillance, diagnosis, prevention, and controlCitation12,Citation33,Citation34 and help to improve public and physician awareness.Citation35,Citation36,Citation37,Citation38,Citation39,Citation40

Other tick-borne diseases

Other tick-borne diseases of importance in Canada include human granulocytic anaplasmosis (HGA) (Anaplasma phagocytophilum), human babesiosis (Babesia microti) Powassan encephalitis caused by Powassan virus and Borrelia miyamotoi infection, which are all transmitted by Ixodes ticks.Citation41 Pathogens transmitted by other tick species also occur in Canada and include Rocky Mountain spotted fever (Rickettsia rickettsii) transmitted primarily by the Rocky Mountain wood tick (Dermacentor andersoni), tularaemia (Francisella tularensis) transmitted by the American dog tick (Dermacentor variabilis) and the rabbit tick (Haemaphysalis leporispalustris), and relapsing fever (Borrelia hermsii) which is transmitted by soft-bodied (Ornithodoros) ticks in southern BC. In addition, Colorado tick fever, caused by the Colorado tick fever virus,Citation42 has been isolated from Dermacentor andersoni ticks in BC and Alberta.Citation43 Finally, a new pathogenic Ehrlichia species has recently been detected in patients and blacklegged ticks in Minnesota and WisconsinCitation44 and further research is required in order to define the ecology of this newly recognized species and its variants in Canada and elsewhere in North America.

Human granulocytic anaplasmosis

Due to recent establishment of the blacklegged tick, I. scapularis, in southeastern and south central Canada, HGA and babesiosis are of growing concern for public health.Citation45 The rickettsial bacteria that cause HGA has been detected in 15% of ticks collected from hunter-caught deer in a study in Quebec in 2007Citation45 (although genotypes in deer may not be pathogenic in humansCitation46). The infection has also been found in dogs in SaskatchewanCitation47 as well as in horses in SaskatchewanCitation48 and Nova Scotia,Citation49 while no dogs showed evidence of exposure to A. phagocytophilum in a study in remote communities along the Central and North coasts of BC.Citation50 The seropositivity of dogs to A. phagocytophilum antigens was assessed in Canada in 2010, and positives were found in only four provinces: Saskatchewan, Manitoba, Ontario, and Quebec; the provinces with the highest canine seroprevalence for A. phagocytophilum were Manitoba and Saskatchewan.Citation51

HGA is not a nationally notifiable disease in Canada and very few human cases have been recorded in Canada, with the first locally acquired case reported in Alberta in 2009Citation52 and another in a US traveler to Manitoba in 2010.Citation53 In the USA, human and canine infections with A. phagocytophilum have been reported in the Pacific northwest, the upper midwest, and the northeastern and mid-Atlantic USA, and most human cases occur in Minnesota, Wisconsin, New York state, New Jersey, and Connecticut,Citation53 suggesting that expansion from the USA may further drive the emergence of this tick-borne disease in Canada. HGA has been a nationally notifiable disease in the USA since 1998, facilitating tracking of the expanding geographic range of this infection south of the border.Citation47

Babesiosis

Babesiosis, caused by the protozoan parasite Babesia microti, has recently been identified in ticks in Canada and has caused one endemic case from Manitoba.Citation54 It is emerging in the USA, and there is a risk of transmission via blood transfusion.Citation55 In North America, over 70 cases of transfusion-transmitted babesiosis (one from Ontario, Canada) and nine associated deaths were reported up to 2008, mostly from the USA.Citation56 Risk assessment for this emerging tick-borne disease involves the monitoring of the tick vectors and the pathogens they carry, in addition to any reports of human infections that may arise in Canada.

West Nile virus

Of the five zoonotic mosquito-borne viruses currently or recently endemic to Canada, WNV is the best known. WNV is transmitted from birds to humans via the bite of an infected mosquito and is transmissible through blood transfusion and tissue and organ transplantation.Citation57 In North America, mosquitoes of the genus Culex are the most common vectors.Citation58 Most human infections cause no illness, while about 20% suffer from WN fever, and less than 1% experience severe neurological disease including meningitis and encephalitis.Citation59,Citation60

Between 2002 and 2012, 5339 human WNV cases were reported in Canada, including 980 (18.4%) cases with neurological symptoms and 73 (1.4%) deaths associated with WNV infection (http://www.phac-aspc.gc.ca/wnv-vwn/), and since 1999 there have been over 30 000 confirmed WNV cases in the USA;Citation61 however, these values under-represent the true infection rates as most infected individuals remain asymptomaticCitation59 or do not seek medical attention. The long-term consequences of WNV neuroinvasive disease include acute flaccid paralysis and other neurological sequelae, often resulting in a poor physical and mental prognosis for patients,Citation62 particularly those with comorbid conditions.Citation63 In a study including 156 WNV patients from four Canadian provinces, physical and mental outcome measures were found to normalize within approximately one year in patients with West Nile non-neuroinvasive disease, while patients with neuroinvasive disease took slightly longer to recover.Citation63 However, more recent studies indicate that long-term effects and chronic manifestations resulting from WNV neurological infections are significant public health issues that require increased attention.Citation64

WNV is now endemic to southern Canada from Alberta to Quebec and has been detected in BC since 2009.Citation65,Citation66,Citation67,Citation68 Culex tarsalis, the main vector of WNV in western Canada, has been found as far north as Yellowknife, Northwest territories in 2010Citation69,Citation70; the main vectors of WNV in eastern Canada belong to the Culex pipiens complex.Citation71,Citation72 While WNV is currently restricted to southern latitudes, the presence of WNV vector mosquitoes as far north as Yellowknife indicates the need for systematic surveillance of arthropod vectors, because a warming climate has the potential to favor the spread of competent vectors and pathogens further north.Citation70

The intensity of WNV activity has varied greatly among years and appears associated with a range of ecological factors affecting mosquito and bird population parameters,Citation14,Citation73,Citation74 with the first epidemic associated with the initial invasion of WNV into wild reservoir and vector populations in 2001/2002 in Ontario and Quebec, and 2002/2003 in the Prairies, and then epidemic ‘re-emergence’ events in 2007 in the Prairies and in 2012 in Ontario and Quebec. Certainly the 2007 epidemic in the prairie provinces was associated with a combination of unusual weather events (a particularly warm winter of 2006 followed by a particularly warm and wet spring of 2007) that drove unprecedented abundance of Cx. tarsalis mosquitoes.Citation75 Increasingly variable weather, which can drive epidemic re-emergence of endemic mosquito-borne diseases, is anticipated with climate change.Citation76 Two serological studies conducted in Canada in 2003 provide insights into the levels of population exposure following the initial WNV outbreaks in Ontario and the Prairies. A household-based seroprevalence survey in southern Ontario found 3.1% (n = 1505) of respondents tested positive for WNV IgG with confirmation by plaque reduction neutralization test; the ratio of severe illness (meningitis or encephalitis) to asymptomatic or mild cases was 1:85.Citation77 In a region of Saskatchewan with the highest incidence of WNV in the 2003 outbreak, the seroprevalence of WNV was almost 10% (n = 501), with significantly higher seropositivity in rural areas (16.8%) compared to urban areas (3.2%).Citation78 Similarly, serological surveys conducted in areas of intense WNV transmission in the USA have reported low prevalence of antibodies to WNV in human populations, indicating that additional epidemic outbreaks of human disease from WNV can be expected in the future when the abundance of human-biting, infected mosquitoes reaches critical levels.Citation68

In recent years, considerable research has been conducted on WNV molecular characterization,Citation79,Citation80,Citation81 vector studies, and WNV ecology,Citation82,Citation83,Citation84,Citation85,Citation86,Citation87,Citation88 public risk behavior and health-care provider knowledge,Citation89,Citation90,Citation91 and risk factor analysis and predictive modeling.Citation92,Citation93,Citation94,Citation95,Citation96 Data from these studies will help to inform public health action for human, vector, and animal surveillance,Citation97,Citation98 diagnosis,Citation99,Citation100,Citation101,Citation102 and prevention and control, including messaging.Citation103,Citation104,Citation105 For example, public health managers could use prediction maps, which are based on animal or human information and developed from annual early season meteorological information, to guide ongoing decisions about when and where to focus intervention strategies for WNVCitation106 as a complement to public health preparedness. Ongoing disease modeling research may further enable the development of weather-generated forecasting tools for WNV risk that could be used in decision support systems for interventions such as mosquito control and enhanced public awareness of imminent increased risk of WNV infection.Citation107,Citation108

Other mosquito-borne diseases

At least four other mosquito-borne viruses that cause human encephalitis are currently, or have been in recent years, present in Canada, including eastern equine encephalitis virus (EEEV), JCV, SSHV, and Cache Valley virus (CVV). However, the burden of illness associated with these viruses is unmeasured and unknown at present as these diseases are not nationally notifiable. Western equine encephalitis virus is also of historic importance in western Canada, with epidemics recorded every decade from the 1930s to the 1980s.Citation43 The health consequences of human infection with these mosquito-borne viruses range from mild febrile illness to severe neurological disease; the latter may result in long-term neurological sequelae or death. As with WNV, the endemic mosquito-borne viruses in Canada differ in their geographical distribution, which is influenced by the distributions of their main mosquito vector species, animal reservoir hosts, and of environmental conditions suitable for transmission.Citation109 Although data on incidence are not available, it is likely that the impact of many of these mosquito-borne viruses in Canada is considerably less than in the USA because of the temperature constraints that restrict transmission to limited periods of warmer months and may restrict the geographic occurrence of different vector species, particularly for EEEV. Nevertheless, sporadic arbovirus epidemics could result in severe illness in substantial numbers of persons in Canada.

California serogroup viruses

JCV and SSHV are mosquito-borne viruses belonging to the California serogroup (CSG) of bunyaviruses.Citation14,Citation110 JCV is widely distributed throughout North America; both SSHV and JCV were first identified as the causal agents of febrile and neurological illness in Canada during the late 1970s and 1980s; however, routine testing had not been conducted for almost 20 years.Citation111 Recently, enhanced testing for CSG virus-associated disease has resulted in the identification of new neuroinvasive and non-neuroinvasive cases associated with these bunyavirusesCitation111,Citation112 (Drebot et al., unpublished data). Widespread exposure to these viruses in wildlife populations in Canada has been demonstrated,Citation110 e.g. seroprevalence data suggest that up to 88% of deer along the south shore region of Nova Scotia have been infected by JCV.Citation113 There have been rare reports of human SSHV and JCV infection in Canada.Citation113,Citation114 Studies in northern Quebec have found up to 10% seroprevalence of CSG viruses in residents of local communities.Citation115 Analysis of sera collected from suspect WNV cases in Manitoba found that 25% of suspect WNV cases were seropositive for CSG viruses when tested for virus-specific antibody in 2010; of these a significant number of individuals also had IgM antibody to SSHV and/or JCV which correlates with possible cases of illness associated with these pathogens,Citation112 although persistent IgM and cross-reactivity among CSG antigens may pose a diagnostic challenge rendering attribution of acute neurological symptoms to these viruses difficult.Citation116,Citation117,Citation118 Importantly, such studies demonstrate that infection of Canadians with CSG viruses may be occurring, and suggest that SSHV and JCV may be contributing to an under recognized burden of disease during the mosquito season in Canada.Citation111

Eastern equine encephalitis virus

EEEV is found along the US gulf and Atlantic coasts, as well as in the US mid-West and in Canada, with human cases reported in at least 19 US states.Citation109 No autochthonous human cases of EEEV have been reported in Canada to date, although the vector of EEEV, Culiseta melanura, has been reported from Quebec, Ontario, Newfoundland, and Manitoba,Citation119 and the virus has caused periodic outbreaks in horses and exotic domestic bird populations (pheasants and emus) in Ontario and Quebec through the 2000s (e.g. http://www.omafra.gov.on.ca/english/livestock/horses/facts/09-047.htm#neurological). However, the recent increase in EEEV epizootic activity in Quebec and Nova Scotia since 2008, with an unprecedented number of equine cases (43 and 13, respectively) reported from localized regions of these provinces during the period 2008–2010, is indicative of an emerging disease.Citation120 The emergence of EEEV in eastern Canada likely relates to a similar, more extensive, EEEV epizootic that has been occurring in the northeastern USA since 2003, which is thought to coincide with the arrival of a novel genotype of EEEV, and has recently extended in range and intensity outside its historic geographic focus in central New York state.Citation121

Cache Valley virus

CVV has been documented to cause congenital defects in livestock but three cases of CVV-associated neurological disease in humans have been reported in the USA.Citation122,Citation123 While CVV, in common with CSG viruses in most jurisdictions, is not included in routine mosquito surveillance programs, CVV has been detected in mosquitoes in Alberta, Saskatchewan, Manitoba, and Ontario.Citation124 Human CVV disease is not nationally notifiable in Canada; however, serological studies of WNV suspect cases from Manitoba and Saskatchewan in 2009 identified probable CVV infections in 5%–16% of patients.Citation122 In 2012 and 2013, CVV infections in livestock were noted for the first time in OntarioCitation125 and QuebecCitation126 and were associated with lamb malformations in flocks of sheep.

Concluding remarks

A prioritization exercise was conducted by public health stakeholders in Canada that identified vector-borne diseases, including Lyme disease and WNV, among the highest priority emerging zoonoses of public health importance. Much is known about the ecological drivers of disease emergence, including climate change, habitat disruption, and population movements; yet fragmented surveillance systems across jurisdictions and the need for inter-sectoral coordination pose a challenge to the timely detection and response to these and other emerging and re-emerging diseases. Research on the ecology and public health impact of vector-borne diseases in Canada has resulted in increased diagnostic capacity and predictive ability to identify areas at risk of disease emergence. Further research is still needed, however, to fill critical knowledge gaps on the ecology and burden of these diseases, which in turn will assist in public health decision-making.

In addition to the priority emerging diseases reviewed here, there is a need for enhanced surveillance to detect other emerging diseases and those with potential for introduction through international travel and trade. While Canada records several hundred imported cases of malaria in international travelers each year, these have not resulted in local transmission despite the presence of competent vector species; the prevailing assumption is that malaria risk will remain negligible, although climate change impacts remain unclear.Citation3 However, several non-endemic mosquito-borne viruses may have the potential for either re-emergence or importation into Canada, including La Crosse virus and St Louis encephalitis virus which are both known in North America, and Rift Valley fever virus, Japanese encephalitis virus, Dengue virus, and Chikungunya virus, which have all recently expanded in global distribution.Citation4,Citation127

Given the rapid spread of tick vectors associated with the rise in tick-borne diseases such as Lyme disease in many parts of Canada, and the potential for climate-driven re-emergence of mosquito-borne diseases such as WNV, public health vigilance in Canada will benefit from a One Health approach that emphasizes multi-sectoral and multidisciplinary coordination among human and animal health stakeholders. A coordinated approach will enable the development of informed risk assessments and promote the early detection of and response to emerging infectious diseases of public health significance in Canada. Clinicians, laboratory medical practitioners, and public health officials should be aware of the risk of local infection with emerging vector-borne diseases in Canada, including those that may not be provincially or nationally notifiable.

This study was funded by the Public Health Agency of Canada.

  • Jones KE, Patel NG, Levy MA et al.Global trends in emerging infectious diseases. Nature 2008; 451: 990–993.
  • Keesing F, Belden LK, Daszak P et al.Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 2010; 468: 647–652.
  • Berrang-Ford L, Maclean JD, Gyorkos TW, Ford JD, Ogden NH.Climate change and malaria in Canada: a systems approach. Interdiscip Perspect Infect Dis 2009; 2009: 385487.
  • Rolin AI, Berrang-Ford L, Kulkarni MA.The risk of Rift Valley fever virus introduction and establishment in the United States and European Union. Emerg Microbes Infect 2013; 2: e81.
  • Ogden NH, Milka R, Caminade C, Gachon P.Recent and projected future climatic suitability of North America for the Asian tiger mosquito Aedes albopictus. Parasit Vectors 2014; 7: 532.
  • Ogden NH, Mechai S, Margos G.Changing geographic ranges of ticks and tick-borne pathogens: drivers, mechanisms and consequences for pathogen diversity. Front Cell Infect Microbiol 2013; 3: 46.
  • Belanger D, Berry P, Bouchet V et al. Human Health in a Changing Climate: A Canadian Assessment of Vulnerabilities and Adaptive Capacity.Ottawa: Health Canada, 2008.Available at http://publications.gc.ca/collections/collection_2008/hc-sc/H128-1-08-528E.pdf (accessed 21 December 2014).
  • Vorou R, Mellou K, Dougas G et al. Selection of Zoonoses of Priority in the Episouth Countries: Final Report.Rome: the EpiSouth project, 2008.Available at http://www.episouth.org/outputs/wp8/WP8Report_Public_area_FINALE_REV_9-4-08.pdf (accessed 21 December 2014).
  • Leighton PA, Koffi JK, Pelcat Y, Lindsay LR, Ogden NH.Predicting the speed of tick invasion: an empirical model of range expansion for the Lyme disease vector Ixodes scapularis in Canada. J Appl Ecol 2012; 49: 457–464.
  • Ogden NH, St-Onge L, Barker IK et al.Risk maps for range expansion of the Lyme disease vector, Ixodes scapularis, in Canada now and with climate change. Int J Health Geogr 2008; 7: 24.
  • Ho K, Melanson M, Desai JA.Bell palsy in lyme disease-endemic regions of canada: a cautionary case of occult bilateral peripheral facial nerve palsy due to Lyme disease. CJEM 2012; 14: 321–324.
  • Halperin JJ, Lang B.Lyme disease in Canada: Q&A for paediatricians. Can J Infect Dis Med Microbiol 2009; 20: 42–44.
  • Ogden NH, Lindsay LR, Leighton PA.Predicting the rate of invasion of the agent of Lyme disease Borrelia burgdorferi. J Appl Ecol 2013; 50: 510–518.
  • Cimolai N, Cimolai T.Infections in the natural environment of British Columbia, Canada. J Infect Public Health 2008; 1: 11–26.
  • Russell C, Martin D, Pillai D, Kristjanson E, Lindsay L.P248 trends in blacklegged tick submissions and Lyme disease serology at Ontario Public Health Laboratories. Int J Antimicrob Agents 2009; 34: S104.
  • Bourré-Tessier J, Milord F, Pineau C, Vinet E.Indigenous Lyme disease in Quebec. J Rheumatol 2011; 38: 183.
  • Paterson J. Preparing Health Care Facilities for Climate Change.Halifax: Nova Scotia Department of Environment, 2013.Available at http://www.greenhealthcare.ca/climateresilienthealthcare/CCGHC-ResiliencyResourceGuide.pdf (accessed 21 December 2014).
  • JD S, Lee M, Fernando K, Jorgensen D, Durden L, Morshed M.Rapid introduction of Lyme disease spirochete, Borrelia burgdorferi sensu stricto, in Ixodes scapularis (Acari: Ixodidae) established at Turkey Point Provincial Park, Ontario, Canada. J Vector Ecol 2008; 33: 64–69.
  • Mak S, Morshed M, Henry B.Ecological niche modeling of lyme disease in British Columbia, Canada. J Med Entomol 2010; 47: 99–105.
  • Koffi JK, Leighton PA, Pelcat Y et al.Passive surveillance for I. scapularis ticks: enhanced analysis for early detection of emerging Lyme disease risk. J Med Entomol 2012; 49: 400–409.
  • Ogden NH, Bouchard C, Kurtenbach K et al.Active and passive surveillance and phylogenetic analysis of Borrelia burgdorferi elucidate the process of Lyme disease risk emergence in Canada. Environ Health Perspect 2010; 118: 909–914.
  • Sperling J, Middelveen M, Klein D, Sperling F.Evolving perspectives on lyme borreliosis in Canada. Open Neurol J 2012; 6: 94–103.
  • Lobato E, Pearce-Duvet J, Staszewski V et al.Seabirds and the circulation of Lyme borreliosis bacteria in the North Pacific. Vector Borne Zoonotic Dis 2011; 11: 1521–1527.
  • Ogden NH, Lindsay LR, Hanincová K et al.Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Appl Environ Microbiol 2008; 74: 1780–1790.
  • Scott JD, Anderson JF, Durden LA.Widespread dispersal of Borrelia burgdorferi-infected ticks collected from songbirds across Canada. J Parasitol 2012; 98: 49–59.
  • Scott JD, Lee M-K, Fernando K et al.Detection of Lyme disease spirochete, Borrelia burgdorferi sensu lato, including three novel genotypes in ticks (Acari: Ixodidae) collected from songbirds (Passeriformes) across Canada. J Vector Ecol 2010; 35: 124–139.
  • Henry B, Roth D, Reilly R et al.How big is the Lyme problem? Using novel methods to estimate the true number of Lyme disease cases in British Columbia residents from 1997 to 2008. Vector Borne Zoonotic Dis 2011; 11: 863–868.
  • Krakowetz CN, Lindsay LR, Chilton NB.Genetic diversity in Ixodes scapularis (Acari: Ixodidae) from six established populations in Canada. Ticks Tick Borne Dis 2011; 2: 143–150.
  • Ogden NH, Margos G, Aanensen DM et al.Investigation of genotypes of Borrelia burgdorferi in Ixodes scapularis ticks collected during surveillance in Canada. Appl Environ Microbiol 2011; 77: 3244–3254.
  • Margos G, Tsao JI, Castillo-Ramírez S et al.Two boundaries separate Borrelia burgdorferi populations in North America. Appl Environ Microbiol 2012; 78: 6059–6067.
  • Bouchard C, Beauchamp G, Nguon S et al.Associations between Ixodes scapularis ticks and small mammal hosts in a newly endemic zone in southeastern Canada: implications for Borrelia burgdorferi transmission. Ticks Tick Borne Dis 2011; 2: 183–190.
  • Wu X, Duvvuri VR, Lou Y, Ogden NH, Pelcat Y, Wu J.Developing a temperature-driven map of the basic reproductive number of the emerging tick vector of Lyme disease Ixodes scapularis in Canada. J Theor Biol 2013; 319: 50–61.
  • Kadkhoda K, Van Caeselle P, Smart G, Mar W.Evaluation of a new health canada-approved lyme immunoblot assay for confirmation of positive EIA screen results. Can J Infect Dis Med Microbiol 2011; 22: 26A.
  • Potok V, Fonseca K, Vayalumkal J.Case 1: Headache after a European vacation. Paediatr Child Health 2011; 16: 391–392.
  • Lowe A-M. [Lyme disease. A tick bite, no panic! Emerging zoonoses in Quebec]. Perspect Infirm 2011; 8: 25–27.French.
  • Sabourin G. [Lyme disease. The carrier tick has settled in Quebec]. Perspect Infirm 2009; 6: 18–19.French.
  • Makhani N, Morris SK, Page AV et al.A twist on Lyme: the challenge of diagnosing European Lyme neuroborreliosis. J Clin Microbiol 2011; 49: 455–457.
  • Henry B, Crabtree A, Roth D, Blackman D, Morshed M.Lyme disease: knowledge, beliefs, and practices of physicians in a low-endemic area. Can Fam Physician 2012; 58: e289–e295.
  • Ogden NH, Lindsay LR, Morshed M, Sockett PN, Artsob H.The rising challenge of Lyme borreliosis in Canada. Can Commun Dis Rep 2008; 34: 1–19.
  • Ogden NH, Artsob H, Lindsay LR, Sockett PN.Lyme disease: a zoonotic disease of increasing importance to Canadians. Can Fam Physician 2008; 54: 1381–1384.
  • Baggs EM, Stack SH, Finney-Crawley JR, Simon NPP.Peromyscus maniculatus, a possible reservoir host of Borrelia garinii from the Gannet Islands off Newfoundland and Labrador. J Parasitol 2011; 97: 792–794.
  • Romero JR, Simonsen KA.Powassan encephalitis and Colorado tick fever. Infect Dis Clin North Am 2008; 22: 545–559.
  • Artsob H.Arthropod-borne disease in Canada: A clinician’s perspective from the ‘Cold Zone’. Paediatr Child Health 2000; 5: 206–212.
  • Pritt BS, Sloan LM, Johnson DKH et al.Emergence of a new pathogenic Ehrlichia species, Wisconsin and Minnesota, 2009. N Engl J Med 2011; 365: 422–429.
  • Bouchard C, Leighton PA, Beauchamp G et al.Harvested white-tailed deer as sentinel hosts for early establishing Ixodes scapularis populations and risk from vector-borne zoonoses in southeastern Canada. J Med Entomol 2013; 50: 384–393.
  • Massung RF, Courtney JW, Hiratzka SL, Pitzer VE, Smith G, Dryden RL.Anaplasma phagocytophilum in white-tailed deer. Emerg Infect Dis 2005; 11: 1604–1606.
  • Cockwill KR, Taylor SM, Snead ECR et al.Granulocytic anaplasmosis in three dogs from Saskatoon, Saskatchewan. Can Vet J 2009; 50: 835–840.
  • Burgess H, Chilton NB, Krakowetz CN, Williams C, Lohmann K.Granulocytic anaplasmosis in a horse from Saskatchewan. Can Vet J 2012; 53: 886–888.
  • Uehlinger FD, Clancey NP, Lofstedt J.Granulocytic anaplasmosis in a horse from Nova Scotia caused by infection with Anaplasma phagocytophilum. Can Vet J 2011; 52: 537–540.
  • Bryan HM, Darimont CT, Paquet PC et al.Exposure to infectious agents in dogs in remote coastal British Columbia: Possible sentinels of diseases in wildlife and humans. Can J Vet Res 2011; 75: 11–17.
  • Villeneuve A, Goring J, Marcotte L, Overvelde S.Seroprevalence of Borrelia burgdorferi, Anaplasma phagocytophilum, Ehrlichia canis, and Dirofilaria immitis among dogs in Canada. Can Vet J 2011; 52: 527–530.
  • Parkins MD, Church DL, Jiang XY, Gregson DB.Human granulocytic anaplasmosis: first reported case in Canada. Can J Infect Dis Med Microbiol 2009; 20: e100–e102.
  • Mackowiak PA, Lagace-Wiens P.Neutrophilic Inclusions in a Hunter. Clin Infect Dis 2010; 51: 1102–1103.
  • Bullard J, Ahsanuddin AN, Perry AM et al.The first case of locally acquired tick-borne Babesia microti infection in Canada. Can J Infect Dis Med Microbiol 2014; 25: e87–e89.
  • Goldman R, O’Brien S, Scalia V, Fearon M.Monitoring for emerging risk of babesiosis in Canada. Vox Sang 2011; 101: 230.
  • Bigham M, Fearon M.Reducing the risk of transfusion-transmitted babesiosis. Transfus Med 2009; 19: 296–297.
  • Fearon M.West Nile story: the transfusion medicine chapter. Future Virol 2011; 6: 1423–1434.
  • Murray KO, Mertens E, Despres P.West Nile virus and its emergence in the United States of America. Vet Res 2010; 41: 67.
  • Téllez-Zenteno JF, Hunter G, Hernández-Ronquillo L, Haghir E.Neuroinvasive West Nile virus disease in Canada. The Saskatchewan experience. Can J Neurol Sci 2013; 40: 580–584.
  • Lanteri MC, Kaidarova Z, Peterson T et al.Association between HLA class I and class II alleles and the outcome of West Nile virus infection: an exploratory study. PLoS One 2011; 6: e22948.
  • Hofmeister EK.West Nile virus: North American experience. Integr Zool 2011; 6: 279–289.
  • Johnstone J, Hanna SE, Nicolle LE et al.Prognosis of West Nile virus associated acute flaccid paralysis: a case series. J Med Case Rep 2011; 5: 395.
  • Loeb M, Hanna S, Nicolle L et al.Prognosis after West Nile virus infection. Ann Intern Med 2008; 149: 232–241.
  • Sejvar JJ.Clinical manifestations and outcomes of West Nile virus infection. Viruses 2014; 6: 606–623.
  • Morshed M, Tang P, Petric M et al.West Nile virus finally debuts in British Columbia 10 years after its introduction to North America. Vector Borne Zoonotic Dis 2011; 11: 1221–1224.
  • Muhamad M, Tang P, Petric M et al.West nile virus in british columbia 10 years after appearing in North America. Vector Borne Zoonotic Dis 2011; 11: 1221–1224.
  • Roth D, Henry B, Mak S et al.West Nile virus range expansion into British Columbia. Emerg Infect Dis 2010; 16: 1251–1258.
  • Artsob H, Gubler DJ, Enria DA et al.West Nile Virus in the New World: trends in the spread and proliferation of West Nile Virus in the Western Hemisphere. Zoonoses Public Health 2009; 56: 357–369.
  • Waeckerlin R, Cork S.Sampling considerations for Flavivirus arthropod vectors in Western Canada – making sense at a data collection level. Int J Infect Dis 2010; 14: e280.
  • Waeckerlin R, Swann J, Elkin B, Zuliani A, Cork S.Flavi and Bunyavirus mosquito vector distribution in North Western Canada. Int J Infect Dis 2012; 16: e449.
  • Andreadis TG.The contribution of Culex pipiens complex mosquitoes to transmission and persistence of West Nile Virus in North America. J Am Mosq Control Assoc 2012; 28: 137–151.
  • Reisen WK.The contrasting bionomics of Culex mosquitoes in western North America. J Am Mosq Control Assoc 2012; 28: 82–91.
  • Blitvich BJ.Transmission dynamics and changing epidemiology of West Nile virus. Anim Health Res Rev 2008; 9: 71–86.
  • Leighton FA.Wildlife Pathogens and Diseases in Canada. Canadian Biodiversity: Ecosystem Status and Trends 2010, Technical Thematic Report No. 7.Ottawa: Canadian Councils of Resource Ministers, 2011.Available at http://publications.gc.ca/collections/collection_2011/ec/En14-43-7-2011-eng.pdf (accessed 21 December 2014).
  • Chen CC, Jenkins E, Epp T, Waldner C, Curry PS, Soos C.Climate change and West Nile virus in a highly endemic region of North America. Int J Environ Res Public Health 2013; 10: 3052–3071.
  • Romero-Lankao P, Smith J, Davidson D et al.North America.In: Barros V, Field C, Dokken D et al. (eds) Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.Cambridge: Cambridge University Press, 2012: 1439–1498.
  • Loeb M, Elliott SJ, Gibson B, Fearon M, Nosal R, Drebot M et al.Protective behavior and West Nile virus risk. Emerg Infect Dis 2005; 11: 1433–1436.
  • Schellenberg TL, Anderson ME, Drebot MA et al.Seroprevalence of West Nile virus in Saskatchewan’s Five Hills Health Region. Can J Public Health 2006; 97: 369–373.
  • Lee M, Man S, Fernando K, Lo T, Tang P, QW.Molecular characterization of west nile virus strains from culex tarsalis in BC. Can J Infect Dis Med Microbiol 2010; 21: 29A–30A.
  • Holloway K, Fearon M, Scalia V et al.Identification and characterization of west nile virus genetic variants collected from canadian samples 2006-2008. Int J Antimicrob Agents 2009; 34: S18–S19.
  • Fearon M, Holloway K, Scalia V et al.West Nile viral load and genotype of viruses in Canadian blood donors during the 2006 and 2007 West Nile seasons. Transfus Med 2009; 19: 283.
  • Millins C, Reid A, Curry P et al.Evaluating the use of house sparrow nestlings as sentinels for West Nile virus in Saskatchewan. Vector Borne Zoonotic Dis 2011; 11: 53–58.
  • Russell C, Hunter FF.Influence of elevation and avian or mammalian hosts on attraction of Culex pipiens (Diptera: Culicidae) in southern Ontario. Can Entomol 2012; 142: 250–255.
  • Jackson M, Gow J, Evelyn M et al.Culex mosquitoes, West Nile virus, and the application of innovative management in the design and management of stormwater retention ponds in Canada. Water Qual Res J Canada 2009; 44: 103–110.
  • Dubé MC, Bird DM, Dibernardo A, Lindsay LR, Charest H.Prevalence of West Nile virus in wild American Kestrels (Falco sparverius) of southern Quebec, Canada. J Wildl Dis 2010; 46: 603–607.
  • Ludwig A, Bigras-Poulin M, Michel P.The analysis of crow population dynamics as a surveillance tool. Transbound Emerg Dis 2009; 56: 337–345.
  • Edillo F, Kiszewski A, Manjourides J et al.Effects of latitude and longitude on the population structure of Culex pipiens s.l., vectors of West Nile virus in North America. Am J Trop Med Hyg 2009; 81: 842–848.
  • Iranpour M, Lindsay LR, Dibernardo A.Development of three additional Culex species-specific polymerase chain reaction primers and their application in West Nile virus surveillance in Canada. J Am Mosq Control Assoc 2010; 26: 37–42.
  • Epp T, Waldner S, Wright J, Curry P, Townsend HG, Potter A.Characterizing the acceptability of a vaccine for West Nile virus by public health practitioners. Vaccine 2010; 28: 3423–3427.
  • Puterman E, DeLongis A, Lee-Baggley D, Greenglass E.Coping and health behaviours in times of global health crises: lessons from SARS and West Nile. Glob Public Health 2009; 4: 69–81.
  • Kiehn L, Murphy KE, Yudin MH, Loeb M.Self-reported protective behaviour against West Nile Virus among pregnant women in Toronto. J Obstet Gynaecol Can 2008; 30: 1103–1109.
  • Chen C-C, Epp T, Jenkins E, Waldner C, Curry PS, Soos C.Predicting weekly variation of Culex tarsalis (Diptera: Culicidae) West Nile virus infection in a newly endemic region, the Canadian prairies. J Med Entomol 2012; 49: 1144–1153.
  • Epp TY, Waldner CL, Berke O.Predicting geographical human risk of West Nile virus – Saskatchewan, 2003 and 2007. Can J Public Health 2009; 100: 344–348.
  • Berke O, Waller L.On the effect of diagnostic misclassification bias on the observed spatial pattern in regional count data – a case study using West Nile virus mortality data from Ontario, 2005. Spat Spatiotemporal Epidemiol 2010; 1: 117–122.
  • Pan L, Qin L, Yang SX, Shuai J.A neural network-based method for risk factor analysis of West Nile virus. Risk Anal 2008; 28: 487–496.
  • Custer B, Kamel H, Kiely NE, Murphy EL, Busch MP.Associations between West Nile virus infection and symptoms reported by blood donors identified through nucleic acid test screening. Transfusion 2009; 49: 278–288.
  • Epp T, Waldner C, Corrigan R, Curry P.Public health use of surveillance for West Nile virus in horses: Saskatchewan, 2003-2005. Transbound Emerg Dis 2008; 55: 411–416.
  • Higgins R, Hung S, Stewart T, Berry R, Hamid-Allie A, Mazzulli T.Human surveillance for West Nile meningoencephalitis infection in Ontario in 2007 and 2008. Int J Antimicrob Agents 2009; 34: S18.
  • O’Brien SF, Scalia V, Zuber E et al.West Nile virus in 2006 and 2007: the Canadian Blood Services’ experience. Transfusion 2010; 50: 1118–1125.
  • Sambol AR, Hinrichs SH.Evaluation of a new West Nile Virus lateral-flow rapid IgM assay. J Virol Methods 2009; 157: 223–226.
  • Pai A, Kleinman S, Malhotra K, Lee-Haynes L, Pietrelli L, Saldanha J.Performance characteristics of the Food and Drug Administration-licensed Roche Cobas TaqScreen West Nile virus assay. Transfusion 2008; 48: 2184–2189.
  • Tilley PAG, Fox JD, Lee B, Chui L, Preiksaitis J.Screening of organ and tissue donors for West Nile virus by nucleic acid amplification – a three year experience in Alberta. Am J Transplant 2008; 8: 2119–2125.
  • MacDonald N.West Nile virus in the context of climate change. Paediatr Child Health 2008; 13: 399–404.
  • Elliott SJ, Loeb M, Harrington D, Eyles J.Heeding the message? Determinants of risk behaviours for West Nile virus. Can J Public Health 2008; 99: 137–141.
  • Lowe AM. [West Nile virus. A record number of cases in Quebec in 2011]. Perspect Infirm 2012; 9: 49–50.French.
  • Epp TY, Waldner C, Berke O.Predictive risk mapping of West Nile virus (WNV) infection in Saskatchewan horses. Can J Vet Res 2011; 75: 161–170.
  • Wang J, Ogden NH, Zhu H.The impact of weather conditions on Culex pipiens and Culex restuans (Diptera: Culicidae) abundance: a case study in Peel Region. J Med Entomol 2011; 48: 468–475.
  • Bouden M, Moulin B, Gosselin P.The geosimulation of West Nile virus propagation: a multi-agent and climate sensitive tool for risk management in public health. Int J Health Geogr 2008; 7: 35.
  • Zacks M a, Paessler S.Encephalitic alphaviruses. Vet Microbiol 2010; 140: 281–286.
  • Goff G, Whitney H, Drebot MA.Roles of host species, geographic separation, and isolation in the seroprevalence of Jamestown Canyon and snowshoe hare viruses in Newfoundland. Appl Environ Microbiol 2012; 78: 6734–6740.
  • Makowski K, Dimitrova K, Andonova M, Drebot M.An overview of California serogroup virus diagnostics & surveillance in Canada in 2008. Int J Antimicrob Agents 2009; 34: S19.
  • Makowski K, Dimitrova K, Andonova M et al.The identification of probable cases of California serogroup virus infections in Manitoba in 2010. Can J Infect Dis Med Microbiol 2011; 22: 15A–16A.
  • Rasool N, Benstead T, Drebot M, Hatchette T.Jamestown Canyon Virus: a potential cause for acute inflammatory polyneuropathy? Neurology 2012; 78: 256.
  • Drebot MA.A laboratory confirmed case of Jamestown Canyon Virus encephalitis in a quebec resident with travel history to maine and new hampshire. Am J Trop Med Hyg 2012; 87: 280.
  • Campagna S, Lévesque B, Anassour-Laouan-Sidi E et al.Seroprevalence of 10 zoonotic infections in 2 Canadian Cree communities. Diagn Microbiol Infect Dis 2011; 70: 191–199.
  • Drebot M, Makowski K, Dimitrova K, Artsob H.IgM persistence in probable cases of California serogroup infection. Am J Trop Med Hyg 2010; 83: 263.
  • Makowski K, Dimitrova K, Andonova M, Drebot M.Assessing serological cross-reactivity among California serogroup viruses using an IgM ELISA platform. Can J Infect Dis Med Microbiol 2010; 21: 26A.
  • Makowski K, Dimitrova K, Andonova M, Van Caeseele P, Dawood M, Drebot M.IgM persistence: a diagnostic concern for identifying cases of California serogroup virus infection. Can J Infect Dis Med Microbiol 2010; 21: 26A–27A.
  • Iranpour M, Lindsay LR, Dibernardo A.Culiseta melanura (Diptera: Culicidae), a new record for the Manitoba mosquito fauna. Proc Entomol Soc Manitoba 2009; 65: 21–25.
  • Chénier S, Côté G, Vanderstock J, Macieira S, Laperle A, Hélie P.An eastern equine encephalomyelitis (EEE) outbreak in Quebec in the fall of 2008. Can Vet J 2010; 51: 1011–1015.
  • Kramer L, Jones S, Dupuis A, Maffei J, Oliver J, Howard J.Shift in dynamics in Eastern equine encephalitis virus activity in central New York. Am J Trop Med Hyg 2012; 87: 169–170.
  • Dimitrova K, Andonova M, Makowski K et al.Preliminary evidence of Cache Valley virus infections and associated human illness in western Canada in 2009. Can J Infect Dis Med Microbiol 2011; 22: 15A.
  • Nguyen NL, Zhao G, Hull R et al.Cache valley virus in a patient diagnosed with aseptic meningitis. J Clin Microbiol 2013; 51: 1966–1969.
  • Pabbaraju K, Ho KCY, Wong S et al.Surveillance of mosquito-borne viruses in Alberta using reverse transcription polymerase chain reaction with generic primers. J Med Entomol 2009; 46: 640–648.
  • Shapiro J, Brooks A, Menzies P et al.Cache Valley virus identified as a cause of malformed lambs in Ontario. AHL Newsl 2012; 16: 15.
  • MAPAQ.Birth defect cases in sheep caused by Cache Valley virus. Info-RAIZO 2013; 1: 1.
  • Weaver SC, Reisen WK.Present and future arboviral threats. Antiviral Res 2010; 85: 328–345.