The Heterogeneity, Distribution, and Environmental Associations of Borrelia burgdorferi Sensu Lato, the Agent of Lyme Borreliosis, in Scotland

Marianne C James, Lucy Gilbert, Alan S Bowman, Ken J Forbes

Research output: Contribution to journalArticle

20 Citations (Scopus)
5 Downloads (Pure)

Abstract

Lyme borreliosis is an emerging infectious human disease caused by the Borrelia burgdorferi sensu lato complex of bacteria with reported cases increasing in many areas of Europe and North America. To understand the drivers of disease risk and the distribution of symptoms, which may improve mitigation and diagnostics, here we characterize the genetics, distribution, and environmental associations of B. burgdorferi s.l. genospecies across Scotland. In Scotland, reported Lyme borreliosis cases have increased almost 10-fold since 2000 but the distribution of B. burgdorferi s.l. is so far unstudied. Using a large survey of over 2200 Ixodes ricinus tick samples collected from birds, mammals, and vegetation across 25 sites we identified four genospecies: Borrelia afzelii (48%), Borrelia garinii (36%), Borrelia valaisiana (8%), and B. burgdorferi sensu stricto (7%), and one mixed genospecies infection. Surprisingly, 90% of the sequence types were novel and, importantly, up to 14% of samples were mixed intra-genospecies co-infections, suggesting tick co-feeding, feeding on multiple hosts, or multiple infections in hosts. B. garinii (hosted by birds) was considerably more genetically diverse than B. afzelii (hosted by small mammals), as predicted since there are more species of birds than small mammals and birds can import strains from mainland Europe. Higher proportions of samples contained B. garinii and B. valaisiana in the west, while B. afzelii and B. garinii were significantly more associated with mixed/deciduous than with coniferous woodlands. This may relate to the abundance of transmission hosts in different regions and habitats. These data on the genetic heterogeneity within and between Borrelia genospecies are a first step to understand pathogen spread and could help explain the distribution of patient symptoms, which may aid local diagnosis. Understanding the environmental associations of the pathogens is critical for rational policy making for disease risk mitigation and land management.

Original languageEnglish
Article number129
JournalFrontiers in public health
Volume2
DOIs
Publication statusPublished - 28 Aug 2014

Fingerprint

Borrelia burgdorferi Group
Lyme Disease
Scotland
Borrelia burgdorferi
Birds
Borrelia
Mammals
Ticks
Coinfection
Emerging Communicable Diseases
Ixodes
Genetic Heterogeneity
Policy Making
North America
Ecosystem
Bacteria

Cite this

The Heterogeneity, Distribution, and Environmental Associations of Borrelia burgdorferi Sensu Lato, the Agent of Lyme Borreliosis, in Scotland. / James, Marianne C; Gilbert, Lucy; Bowman, Alan S; Forbes, Ken J.

In: Frontiers in public health, Vol. 2, 129, 28.08.2014.

Research output: Contribution to journalArticle

@article{e02b9885cdb44ca69d63e512f7367f8e,
title = "The Heterogeneity, Distribution, and Environmental Associations of Borrelia burgdorferi Sensu Lato, the Agent of Lyme Borreliosis, in Scotland",
abstract = "Lyme borreliosis is an emerging infectious human disease caused by the Borrelia burgdorferi sensu lato complex of bacteria with reported cases increasing in many areas of Europe and North America. To understand the drivers of disease risk and the distribution of symptoms, which may improve mitigation and diagnostics, here we characterize the genetics, distribution, and environmental associations of B. burgdorferi s.l. genospecies across Scotland. In Scotland, reported Lyme borreliosis cases have increased almost 10-fold since 2000 but the distribution of B. burgdorferi s.l. is so far unstudied. Using a large survey of over 2200 Ixodes ricinus tick samples collected from birds, mammals, and vegetation across 25 sites we identified four genospecies: Borrelia afzelii (48{\%}), Borrelia garinii (36{\%}), Borrelia valaisiana (8{\%}), and B. burgdorferi sensu stricto (7{\%}), and one mixed genospecies infection. Surprisingly, 90{\%} of the sequence types were novel and, importantly, up to 14{\%} of samples were mixed intra-genospecies co-infections, suggesting tick co-feeding, feeding on multiple hosts, or multiple infections in hosts. B. garinii (hosted by birds) was considerably more genetically diverse than B. afzelii (hosted by small mammals), as predicted since there are more species of birds than small mammals and birds can import strains from mainland Europe. Higher proportions of samples contained B. garinii and B. valaisiana in the west, while B. afzelii and B. garinii were significantly more associated with mixed/deciduous than with coniferous woodlands. This may relate to the abundance of transmission hosts in different regions and habitats. These data on the genetic heterogeneity within and between Borrelia genospecies are a first step to understand pathogen spread and could help explain the distribution of patient symptoms, which may aid local diagnosis. Understanding the environmental associations of the pathogens is critical for rational policy making for disease risk mitigation and land management.",
author = "James, {Marianne C} and Lucy Gilbert and Bowman, {Alan S} and Forbes, {Ken J}",
note = "Genospecies controls were obtained from the laboratory of Dr. Muriel Cornet at the Institut Pasteur, Paris. We thank Bob Furness for collecting ticks from passerine birds, Steph Vollmer for processing the samples from one site, E. Packer, A. Wiebe, J. Low, E. Stephen, and J. Arthur for help collecting ticks, Kenny Raey for laboratory assistance, and Jackie Potts for statistical advice. Marianne C. James was funded by a Biotechnology and Biological Sciences Research Council (BBSRC) Doctoral Training Grant with CASE support from the Macaulay Development Trust awarded to Alan S. Bowman and Lucy Gilbert. Lucy Gilbert was supported by the Scottish Government’s Rural and Environment Science and Analytical Services Division (RESAS).",
year = "2014",
month = "8",
day = "28",
doi = "10.3389/fpubh.2014.00129",
language = "English",
volume = "2",
journal = "Frontiers in public health",
issn = "2296-2565",
publisher = "Frontiers Media S.A.",

}

TY - JOUR

T1 - The Heterogeneity, Distribution, and Environmental Associations of Borrelia burgdorferi Sensu Lato, the Agent of Lyme Borreliosis, in Scotland

AU - James, Marianne C

AU - Gilbert, Lucy

AU - Bowman, Alan S

AU - Forbes, Ken J

N1 - Genospecies controls were obtained from the laboratory of Dr. Muriel Cornet at the Institut Pasteur, Paris. We thank Bob Furness for collecting ticks from passerine birds, Steph Vollmer for processing the samples from one site, E. Packer, A. Wiebe, J. Low, E. Stephen, and J. Arthur for help collecting ticks, Kenny Raey for laboratory assistance, and Jackie Potts for statistical advice. Marianne C. James was funded by a Biotechnology and Biological Sciences Research Council (BBSRC) Doctoral Training Grant with CASE support from the Macaulay Development Trust awarded to Alan S. Bowman and Lucy Gilbert. Lucy Gilbert was supported by the Scottish Government’s Rural and Environment Science and Analytical Services Division (RESAS).

PY - 2014/8/28

Y1 - 2014/8/28

N2 - Lyme borreliosis is an emerging infectious human disease caused by the Borrelia burgdorferi sensu lato complex of bacteria with reported cases increasing in many areas of Europe and North America. To understand the drivers of disease risk and the distribution of symptoms, which may improve mitigation and diagnostics, here we characterize the genetics, distribution, and environmental associations of B. burgdorferi s.l. genospecies across Scotland. In Scotland, reported Lyme borreliosis cases have increased almost 10-fold since 2000 but the distribution of B. burgdorferi s.l. is so far unstudied. Using a large survey of over 2200 Ixodes ricinus tick samples collected from birds, mammals, and vegetation across 25 sites we identified four genospecies: Borrelia afzelii (48%), Borrelia garinii (36%), Borrelia valaisiana (8%), and B. burgdorferi sensu stricto (7%), and one mixed genospecies infection. Surprisingly, 90% of the sequence types were novel and, importantly, up to 14% of samples were mixed intra-genospecies co-infections, suggesting tick co-feeding, feeding on multiple hosts, or multiple infections in hosts. B. garinii (hosted by birds) was considerably more genetically diverse than B. afzelii (hosted by small mammals), as predicted since there are more species of birds than small mammals and birds can import strains from mainland Europe. Higher proportions of samples contained B. garinii and B. valaisiana in the west, while B. afzelii and B. garinii were significantly more associated with mixed/deciduous than with coniferous woodlands. This may relate to the abundance of transmission hosts in different regions and habitats. These data on the genetic heterogeneity within and between Borrelia genospecies are a first step to understand pathogen spread and could help explain the distribution of patient symptoms, which may aid local diagnosis. Understanding the environmental associations of the pathogens is critical for rational policy making for disease risk mitigation and land management.

AB - Lyme borreliosis is an emerging infectious human disease caused by the Borrelia burgdorferi sensu lato complex of bacteria with reported cases increasing in many areas of Europe and North America. To understand the drivers of disease risk and the distribution of symptoms, which may improve mitigation and diagnostics, here we characterize the genetics, distribution, and environmental associations of B. burgdorferi s.l. genospecies across Scotland. In Scotland, reported Lyme borreliosis cases have increased almost 10-fold since 2000 but the distribution of B. burgdorferi s.l. is so far unstudied. Using a large survey of over 2200 Ixodes ricinus tick samples collected from birds, mammals, and vegetation across 25 sites we identified four genospecies: Borrelia afzelii (48%), Borrelia garinii (36%), Borrelia valaisiana (8%), and B. burgdorferi sensu stricto (7%), and one mixed genospecies infection. Surprisingly, 90% of the sequence types were novel and, importantly, up to 14% of samples were mixed intra-genospecies co-infections, suggesting tick co-feeding, feeding on multiple hosts, or multiple infections in hosts. B. garinii (hosted by birds) was considerably more genetically diverse than B. afzelii (hosted by small mammals), as predicted since there are more species of birds than small mammals and birds can import strains from mainland Europe. Higher proportions of samples contained B. garinii and B. valaisiana in the west, while B. afzelii and B. garinii were significantly more associated with mixed/deciduous than with coniferous woodlands. This may relate to the abundance of transmission hosts in different regions and habitats. These data on the genetic heterogeneity within and between Borrelia genospecies are a first step to understand pathogen spread and could help explain the distribution of patient symptoms, which may aid local diagnosis. Understanding the environmental associations of the pathogens is critical for rational policy making for disease risk mitigation and land management.

U2 - 10.3389/fpubh.2014.00129

DO - 10.3389/fpubh.2014.00129

M3 - Article

VL - 2

JO - Frontiers in public health

JF - Frontiers in public health

SN - 2296-2565

M1 - 129

ER -