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First Record of Lyme Disease Borrelia in the Arctic

Authors:

Abstract

The epidemiology and ecology of Lyme disease is very complex, and its reported geographical distribution is constantly increasing. Furthermore, the involvement of birds in long distance dispersal and their role as reservoir hosts is now well established. In this study, we have shown that sea birds in the Arctic region of Norway carry Ixodes uriae ticks infected with Lyme disease Borrelia garinii spirochetes. Interestingly, DNA sequencing showed that these isolates are closely related to B. garinii previously isolated from birds, as well as from clinical specimens in northern Europe.
VECTOR-BORNE AND ZOONOTIC DISEASES
Volume 7, Number 3, 2007
© Mary Ann Liebert, Inc.
DOI: 10.1089/vbz.2006.0644
Short Report
First Record of Lyme Disease Borrelia in the Arctic
CHRISTER LARSSON,
1
PÄR COMSTEDT,
1
BJÖRN OLSEN,
2
and SVEN BERGSTRÖM
1
ABSTRACT
The epidemiology and ecology of Lyme disease is very complex, and its reported geographical distribution is con-
stantly increasing. Furthermore, the involvement of birds in long distance dispersal and their role as reservoir
hosts is now well established. In this study, we have shown that sea birds in the Arctic region of Norway carry
Ixodes uriae ticks infected with Lyme disease Borrelia garinii spirochetes. Interestingly, DNA sequencing showed
that these isolates are closely related to B. garinii previously isolated from birds, as well as from clinical speci-
mens in northern Europe. Key Words: Borrelia—Lyme disease—Ixodes uriae—Ticks—Zoonosis—Arctic—Birds—
Common guillemot—Uria aalge. Vector-Borne Zoonotic Dis. 7, 00–00.
453
INTRODUCTION
L
YME DISEASE
is a tick-borne zoonosis caused
by the Borrelia burgdorferi sensu lato (s.l)
species: B. burgdorferi, B. garinii, and B. afzelii.
Several symptoms are indistinct and tick ex-
posure or a stay in a tick endemic area are im-
portant factors for physicians to diagnose Lyme
disease (Stanek et al. 1996).
While terrestrial B. burgdorferi s.l vectors such
as I. ricinus, I. persulcatus, and I. scapularis live
in temperate regions, the seabird tick Ixodes
uriae thrives in bird colonies in polar and tem-
perate regions of both hemispheres. In previ-
ous studies, I. uriae ticks collected from several
locations worldwide were found to carry Bor-
relia (Olsen et al. 1993, 1995). Although spe-
cialized to bird colonies, these ticks may attack
mammals such as grazing sheep and humans
when given the opportunity. Hence, I. uriae is
a potential vector of human and livestock Lyme
borreliosis (Arthur 1963).
In the present study, we report the presence
of Borrelia in I. uriae ticks collected on the
Varanger peninsula in arctic Norway situated
at 70°N. This is the northernmost finding of this
pathogen ever reported. Since bird colonies are
frequently visited by tourists and scientists,
awareness of Borrelia and the potential occur-
rence of Lyme disease in the arctic, outside its
general habitat, is essential.
METHODS
Collection of ticks
Ixodes uriae from nesting common guillemots
(Uria aalge), Brünnich’s guillemots (Uria
lomvia), razorbills (Alca torda), and puffins
1
Department of Molecular Biology, Umeå University, Umeå, Sweden.
2
Department of Infectious Diseases, Umeå University, Umeå, and Section for Zoonotic Ecology and Epidemiology,
Department of Biology and Environmental Science, Kalmar University, Kalmar, Sweden.
(Fratercula arctica) were collected in Hornøya,
(70°37N 31°10E) on the Varanger peninsula in
northern Norway.
DNA sequencing and phylogenetic analysis
To examine ticks for the presence of Borrelia,
DNA was extracted and screened by real-time
polymerase chain reaction (PCR) as previously
described (Tsao et al. 2004). If positive, the phy-
logenetic status was determined by partial se-
quencing of the intergenic spacer (IGS) region
between the rrs (16S) and rrl (23S) as previously
described (Bunikis et al. 2004). Sequences of 492
bp were compared to those of other B. garinii
isolates from various sources by ClustalW
(www.ebi.ac.uk). Novel IGS variants were de-
posited in GenBank.
RESULTS
I. uriae ticks were collected from a bird
colony in the Barents Sea. In total, four differ-
ent Borrelia strains were obtained. By partial se-
quencing of the IGS, all isolates were identified
as B. garinii. Two strains, Var3 and Var4 (Gen-
Bank EF190484 and EF190485), were found
in one tick each. One strain, Var2 (GenBank
EF190483), was found in two ticks, and the last
strain, Var1 (GenBank EF190482), was found in
three individual ticks. All Borrelia-positive ticks
were collected from common guillemots except
for one of the Var1 strains, which was obtained
from a tick found on one of the authors. Ticks
were collected also from other bird species, but
only ticks from or near common guillemots car-
ried Borrelia. However, the sample size (less
LARSSON ET AL.
454
T
ABLE
1. C
OMPARISON OF
492 IGS N
UCLEOTIDES FROM
V
ARANGER
B.
GARINII
V
AR
1-4
TO
S
TRAINS
P
REVIOUSLY
I
SOLATED FROM
V
ARIOUS
S
OURCES
ClustalW
Varanger alignment
group Strain Source Location Environment score (%)
Var1 Far01 I. uriae feeding on puffin Faroe Island Auk colony 100
Var3 DQ307375 I. ricinus feeding on Sweden Migrating; caught by 99
european robin bird ringers
Var3 Bio56002 Human skin biopsy Sweden 98
a
Var2 Bio56056 Human skin biopsy Sweden 98
Var2 DQ307376 I. ricinus feeding on Sweden Migrating; caught by 98
tree pipit bird ringers
Var3 DQ307374 I. ricinus feeding on Sweden Migrating; caught by 98
trush nightingale bird ringers
Var4 DQ307375 I. ricinus feeding on Sweden Migrating; caught by 97
european robin bird ringers
Var4 DQ307374 I. ricinus feeding on Sweden Migrating; caught by 97
trush nightingale bird ringers
Var4 Bio56002 Human skin biopsy Sweden 95*
Var3 Bio56016 Human skin biopsy Sweden 95
Var2 Bio56016 Human skin biopsy Sweden 95
Var4 Bio56016 Human skin biopsy Sweden 95
Var2 DQ307373 I. ricinus feeding on Sweden Migrating; caught by 95
tree pipit bird ringers
Var3 DQ307373 I. ricinus feeding on Sweden Migrating; caught by 95
tree pipit bird ringers
Var4 DQ307373 I. ricinus feeding on Sweden Migrating; caught by 95
tree pipit bird ringers
Var3 IP90 I. persulcatus Russia 40
Var4 IP90 I. persulcatus Russia 40
Var2 IP90 I. persulcatus Russia 38
Var1 IP90 I. persulcatus Russia 38
a
488 bases of IGS were used for sequence comparison.
Only similarities of 95% or more are shown. B. garinii IP90 is included as an example of a less related strain.
than 50) from these other bird species was too
small to allow conclusions from this observa-
tion.
The IGS of these Varanger samples
(Var1–Var4) were compared to sequences of
other B. garinii strains, both published and un-
published. By phylogenetic analysis (Table 1),
the Var1 IGS sequence was found to be identi-
cal to strains previously isolated from I. uriae
feeding on puffins in the Faroe Islands (Gylfe
et al. 1999).
The Var2 and Var3 sequences from Varanger
were highly similar both to clinical samples
from Lyme disease patients in southern Swe-
den and to bacteria isolated from ticks feeding
on migratory passerine birds in the same area
(Comstedt et al. 2006). The Varanger strains
show strong similarities to B. garinii strains
found in the sea bird tick I. uriae, in I. ricinus
feeding on passerine birds, and to human clin-
ical isolates in northern Europe (Table 1). This
indicates transmission of Borrelia between dif-
ferent ecological niches.
DISCUSSION
Lyme disease borreliae are mainly associated
with temperate regions, but have also been
found in birds and ticks collected in colder cli-
mates such as the Antarctic, in the Faroe Is-
lands, Iceland, Alaska, and New Foundland
(Olsen et al. 1995, Smith et al. 2006). In this re-
port we demonstrate the presence of Borrelia in
ticks collected in an arctic bird colony, making
this the first report of Borrelia above the Arctic
Circle. Due to a small sample size, we cannot
draw conclusions about the prevalence of Bor-
relia among ticks in this region, although 5% is
a rough estimate.
By comparing DNA sequences of these iso-
lates to those of other B. garinii strains, we could
conclude that the IGS of B. garinii Var1 strains
is identical to those of strains from the Faroe
Islands (Table 1). Var2–Var4 exhibit close se-
quence relatedness to strains isolated from
Lyme disease patients in southern Sweden
(Table 1). The strains also show a high level of
similarity to bacteria found in I. ricinus ticks
collected from migrating passerine birds in the
same area. I. ricinus is the major vector of Lyme
disease in Europe and this suggests a flux of
bacteria not only geographically between sea
birds but also between the marine cycle of sea
birds and I. uriae, and the terrestrial cycle of I.
ricinus, passerines, small mammals, and hu-
mans. We believe the transfer between the ter-
restrial and marine Borrelia cycles occurs via
small mammals such as rodents visiting bird
colonies to feed, or by nesting passerines (Olsen
et al. 1993) in the colonies being fed on by I.
uriae. Transmission of bacteria between I. rici-
nus and sea birds is less likely due to their dif-
ferent ecological preferences. When taking tick
distribution into account, it is more likely that
the two tick species, I. ricinus and I. uriae, may
share the same geographical niches at lower al-
titudes.
We report a finding of B. garinii strains iso-
lated from sea bird-associated ticks bearing
nearly identical sequence similarity to human
clinical isolates. Altogether, these results chal-
lenge the grouping of B. garinii into “bird re-
lated” versus “mammal or human related”
strains. Our findings demonstrate a broader
geographic distribution of Borrelia than previ-
ously thought and highlight the importance of
birds, ticks and mammals in Borrelia ecology
and dispersal in regions including the Arctic.
ACKNOWLEDGMENTS
Pernilla Jatko is acknowledged for technical
assistance and Betty Guo for critically reading
the manuscript. This study was supported by
Formas, the Swedish Council for Environment,
Agricultural Sciences and Spatial Planning
(grant 23.0161), The Swedish Research Council
(grants 05489 and 07922), and the J.C. Kempe
Foundation.
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Address reprint requests to:
Dr. Sven Bergström
Department of Molecular Biology
Umeå University
SE-901 87 Umeå, Sweden
E-mail: sven.bergstrom@molbiol.umu.se
LARSSON ET AL.
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The Lyme disease spirochaete, Borrelia burgdorferi s.l., is the only Borrelia known to infect both mammals and birds. The main vertebrate reservoirs of B. burgdorferi are thought to be various small and intermediate size mammals, but the importance of birds as a reservoir has not been thoroughly explored. In the Northern and Southern Hemispheres the seabird tick, Ixodes uriae, is prevalent and closely associated with many species of colony-nesting marine birds. Here we report the presence of spirochaetes, demonstrated by immunofluorescent assay, by polymerase chain reaction and in culture, in I. uriae infesting razorbills on an island in the Baltic Sea. This island is free from mammals. The protein profile of the spirochaetes and the sequences of their flagellin and ospA genes are identical to those of the Lyme disease spirochaete, Borrelia burgdorferi s.l., previously isolated from I. ricinus on a nearby island. In biopsies from the foot web of razorbills, B. burgdorferi-specific DNA was detected after amplification by polymerase chain reaction. Our results suggest that birds play an important part in the maintenance of B. burgdorferi and that mammals may not be a prerequisite for its life cycle.
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Lyme disease is a zoonosis transmitted by ticks and caused by the spirochete Borrelia burgdorferi sensu lato. Epidemiological and ecological investigations to date have focused on the terrestrial forms of Lyme disease. Here we show a significant role for seabirds in a global transmission cycle by demonstrating the presence of Lyme disease Borrelia spirochetes in Ixodes uriae ticks from several seabird colonies in both the Southern and Northern Hemispheres. Borrelia DNA was isolated from I. uriae ticks and from cultured spirochetes. Sequence analysis of a conserved region of the flagellin (fla) gene revealed that the DNA obtained was from B. garinii regardless of the geographical origin of the sample. Identical fla gene fragments in ticks obtained from different hemispheres indicate a transhemispheric exchange of Lyme disease spirochetes. A marine ecological niche and a marine epidemiological route for Lyme disease borreliae are proposed.
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The EU Concerted Action on Risk Assessment in Lyme Borreliosis (EUCALB) has consulted other clinicians and scientists in Europe to produce case definitions of the principal manifestations of European Lyme borreliosis. These case definitions will not only be helpful in supporting its own research interests, but are also intended to assist other clinicians in appropriate management and to support further studies aimed at determining the full clinical spectrum of the disease. The case definitions were achieved after a series of meetings organised by EUCALB with other expert clinicians and scientists from twelve European countries. The definitions and the diagnostic criteria presented thus represent the consensus reached at these meetings. The proposed case definitions consider skin, nervous system, cardiac and musculoskeletal presentations and the role of laboratory investigation in supporting diagnosis.
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This is the first report on the isolation of Lyme disease Borrelia from seabirds on the Faeroe Islands and the characteristics of its enzootic cycle. The major components of the Borrelia cycle include the puffin (Fratercula arctica) as the reservoir and Ixodes uriae as the vector. The importance of this cycle and its impact on the spread of human Lyme borreliosis have not yet been established. Borrelia spirochetes isolated from 2 of 102 sampled puffins were compared to the borreliae previously obtained from seabird ticks, I. uriae. The rrf-rrl intergenic spacer and the rrs and the ospC genes were sequenced and a series of phylogenetic trees were constructed. Sequence data and restriction fragment length polymorphism analysis grouped the strains together with Borrelia garinii. In a seroepidemiological survey performed with residents involved in puffin hunting on the Faeroe Islands, 3 of 81 serum samples were found to be positive by two commonly used clinical tests: a flagellin-based enzyme-linked immunosorbent assay (ELISA) and Western blotting. These three positive serum samples also had high optical density values in a whole-cell ELISA. The finding of seropositive Faeroe Islanders who are regularly exposed to I. uriae indicate that there may be a transfer of B. garinii by this tick species to humans.
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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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Many pathogens, such as the agents of West Nile encephalitis and plague, are maintained in nature by animal reservoirs and transmitted to humans by arthropod vectors. Efforts to reduce disease incidence usually rely on vector control or immunization of humans. Lyme disease, for which no human vaccine is currently available, is a commonly reported vector-borne disease in North America and Europe. In a recently developed, ecological approach to disease prevention, we intervened in the natural cycle of the Lyme disease agent (Borrelia burgdorferi) by immunizing wild white-footed mice (Peromyscus leucopus), a reservoir host species, with either a recombinant antigen of the pathogen, outer surface protein A, or a negative control antigen in a repeated field experiment with paired experimental and control grids stratified by site. Outer surface protein A vaccination significantly reduced the prevalence of B. burgdorferi in nymphal blacklegged ticks (Ixodes scapularis) collected at the sites the following year in both experiments. The magnitude of the vaccine's effect at a given site correlated with the tick infection prevalence found on the control grid, which in turn correlated with mouse density. These data, as well as differences in the population structures of B. burgdorferi in sympatric ticks and mice, indicated that nonmouse hosts contributed more to infecting ticks than previously expected. Thus, where nonmouse hosts play a large role in infection dynamics, vaccination should be directed at additional species.
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To define the role of birds as reservoirs and disseminators of Borrelia spirochetes, we characterized tick infestation and reservoir competence of migratory passerine birds in Sweden. A total of 1,120 immature Ixodes ricinus ticks were removed from 13,260 birds and assayed by quantitative polymerase chain reaction (PCR) for Borrelia, followed by DNA sequencing for species and genotype identification. Distributions of ticks on birds were aggregated, presumably because of varying encounters with ticks along migratory routes. Lyme borreliosis spirochetes were detected in 160 (1.4%) ticks. Borrelia garinii was the most common species in PCR-positive samples and included genotypes associated with human infections. Infestation prevalence with infected ticks was 5 times greater among ground-foraging birds than other bird species, but the 2 groups were equally competent in transmitting Borrelia. Migratory passerine birds host epidemiologically important vector ticks and Borrelia species and vary in effectiveness as reservoirs on the basis of their feeding behavior.
Borrelia garinii in seabird ticks (Ixodes uriae), Atlantic Coast
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Smith, RP, Muzaffar, SB, Lavers, J, Lacombe, EH, et al. Borrelia garinii in seabird ticks (Ixodes uriae), Atlantic Coast, North America. Emerg Infect Dis 2006; 12: 1909–1912.
Borrelia garinii in seabird ticks (Ixodes uriae)
  • R P Smith
  • Muzaffar
  • Sb
  • J Lavers
  • E H Lacombe
Smith, RP, Muzaffar, SB, Lavers, J, Lacombe, EH, et al. Borrelia garinii in seabird ticks (Ixodes uriae), Atlantic Coast, North America. Emerg Infect Dis 2006; 12: 1909-1912.
London: Butterworths
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Arthur, DR. British Ticks. London: Butterworths; 1963.