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      Active and Passive Surveillance and Phylogenetic Analysis of Borrelia burgdorferi Elucidate the Process of Lyme Disease Risk Emergence in Canada

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          Abstract

          Background

          Northward expansion of the tick Ixodes scapularis is driving Lyme disease (LD) emergence in Canada. Information on mechanisms involved is needed to enhance surveillance and identify where LD risk is emerging.

          Objectives

          We used passive and active surveillance and phylogeographic analysis of Borrelia burgdorferi to investigate LD risk emergence in Quebec.

          Methods

          In active surveillance, we collected ticks from the environment and from captured rodents. B. burgdorferi transmission was detected by serological analysis of rodents and by polymerase chain reaction assays of ticks. Spatiotemporal trends in passive surveillance data assisted interpretation of active surveillance. Multilocus sequence typing (MLST) of B. burgdorferi in ticks identified likely source locations of B. burgdorferi.

          Results

          In active surveillance, we found I. scapularis at 55% of sites, and we were more likely to find them at sites with a warmer climate. B. burgdorferi was identified at 13 I. scapularis–positive sites, but infection prevalence in ticks and animal hosts was low. Low infection prevalence in ticks submitted in passive surveillance after 2004—from the tick-positive regions identified in active surveillance—coincided with an exponential increase in tick submissions during this time. MLST analysis suggested recent introduction of B. burgdorferi from the northeastern United States.

          Conclusions

          These data are consistent with I. scapularis ticks dispersed from the United States by migratory birds, founding populations where the climate is warmest, and then establishment of B. burgdorferi from the United States several years after I. scapularis have established. These observations provide vital information for public health to minimize the impact of LD in Canada.

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          A spatial scan statistic.

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            Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada.

            We used an Ixodes scapularis population model to investigate potential northward spread of the tick associated with climate change. Annual degree-days >0 degrees C limits for I. scapularis establishment, obtained from tick population model simulations, were mapped using temperatures projected for the 2020s, 2050s and 2080s by two Global Climate Models (the Canadian CGCM2 and the UK HadCM3) for two greenhouse gas emission scenario enforcings 'A2'and 'B2' of the Intergovernmental Panel on Climate Change. Under scenario 'A2' using either climate model, the theoretical range for I. scapularis establishment moved northwards by approximately 200 km by the 2020s and 1000 km by the 2080s. Reductions in emissions (scenario 'B2') had little effect on projected range expansion up to the 2050s, but the range expansion projected to occur between the 2050s and 2080s was less than that under scenario 'A2'. When the tick population model was driven by projected annual temperature cycles (obtained using CGCM2 under scenario 'A2'), tick abundance almost doubled by the 2020s at the current northern limit of I. scapularis, suggesting that the threshold numbers of immigrating ticks needed to establish new populations will fall during the coming decades. The projected degrees of theoretical range expansion and increased tick survival by the 2020s, suggest that actual range expansion of I. scapularis may be detectable within the next two decades. Seasonal tick activity under climate change scenarios was consistent with maintenance of endemic cycles of the Lyme disease agent in newly established tick populations. The geographic range of I. scapularis-borne zoonoses may, therefore, expand significantly northwards as a consequence of climate change this century.
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              Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe.

              The genetic polymorphism of Borrelia burgdorferi and Borrelia afzelii, two species that cause Lyme borreliosis, was estimated by sequence typing of four loci: the rrs-rrlA intergenic spacer (IGS) and the outer-membrane-protein gene p66 on the chromosome, and the outer-membrane-protein genes ospA and ospC on plasmids. The major sources of DNA for PCR amplification and sequencing were samples of the B. burgdorferi tick vector Ixodes scapularis, collected at a field site in an endemic region of the north-eastern United States, and the B. afzelii vector Ixodes ricinus, collected at a similar site in southern Sweden. The sequences were compared with those of reference strains and skin biopsy isolates, as well as database sequences. For B. burgdorferi, 10-13 alleles for each of the 4 loci, and a total of 9 distinct clonal lineages with linkage of all 4 loci, were found. For B. afzelii, 2 loci, ospC and IGS, were examined, and 11 IGS genotypes, 12 ospC alleles, and a total of 9 linkage groups were identified. The genetic variants of B. burgdorferi and B. afzelii among samples from the field sites accounted for the greater part of the genetic diversity previously reported from larger areas of the north-eastern United States and central and northern Europe. Although ospC alleles of both species had higher nucleotide diversity than other loci, the ospC locus showed evidence of intragenic recombination and was unsuitable for phylogenetic inference. In contrast, there was no detectable recombination at the IGS locus of B. burgdorferi. Moreover, beyond the signature nucleotides that specified 10 IGS genotypes, there were additional nucleotide polymorphisms that defined a total of 24 subtypes. Maximum-likelihood and parsimony cladograms of B. burgdorferi aligned IGS sequences revealed the subtype sequences to be terminal branches of clades, and the existence of at least three monophyletic lineages within B. burgdorferi. It is concluded that B. burgdorferi and B. afzelii have greater genetic diversity than had previously been estimated, and that the IGS locus alone is sufficient for strain typing and phylogenetic studies.
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                Author and article information

                Journal
                Environ Health Perspect
                Environmental Health Perspectives
                National Institute of Environmental Health Sciences
                0091-6765
                1552-9924
                July 2010
                27 April 2010
                : 118
                : 7
                : 909-914
                Affiliations
                [1 ] Centre for Food-Borne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, Saint-Hyacinthe, Québec, Canada
                [2 ] Groupe de recherche en épidémiologie des zoonoses et santé publique, Faculté de médecine vétérinaire, Université de Montréal, Québec, Canada
                [3 ] Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom
                [4 ] Zoonoses and Special Pathogens Division, Public Health Agency of Canada, National Microbiology Laboratory, Winnipeg, Manitoba, Canada
                [5 ] Laboratoire de santé publique du Québec, Institut national de santé publique du Québec, Québec, Canada
                [6 ] Direction des risques biologiques et santé au travail, Institut national de santé publique du Québec, Québec, Canada
                Author notes
                Address correspondence to N.H. Ogden, Centre for Food-borne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, 3200 Sicotte, C.P. 5000, Saint-Hyacinthe, Québec, J2S 7C6, Canada. Telephone: (450) 773-8521 Ext. 18604. Fax: (450) 778-8120. Email: nicholas_ogden@ 123456phac-aspc.gc.ca

                The authors declare they have no actual or potential competing financial interests.

                Article
                ehp-118-909
                10.1289/ehp.0901766
                2920908
                20421192
                f73ed205-c86b-4b95-9f8b-73f3413b4516
                This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original DOI.
                History
                : 1 December 2009
                : 25 March 2010
                Categories
                Research

                Public health
                lyme disease,ixodes scapularis,climate change,environment,borrelia burgdorferi,emergence
                Public health
                lyme disease, ixodes scapularis, climate change, environment, borrelia burgdorferi, emergence

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