Content uploaded by Bjorn Olsen
Author content
All content in this area was uploaded by Bjorn Olsen on Apr 21, 2015
Content may be subject to copyright.
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.
REFERENCES
Arthur, DR. British Ticks. London: Butterworths; 1963.
Bunikis, J, Garpmo, U, Tsao, J, Berglund, J, et al. Sequence
typing reveals extensive strain diversity of the Lyme
borreliosis agents Borrelia burgdorferi in North America
and Borrelia afzelii in Europe. Microbiology 2004;
150:1741–1755.
BORRELIA IN THE ARCTIC
455
Comstedt, P, Bergstrom, S, Olsen, B, Garpmo, U, et al.
Migratory passerine birds as reservoirs of Lyme bor-
reliosis in Europe. Emerg Infect Dis 2006; 12:1087–
1095.
Gylfe, A, Olsen, B, Strasevicius, D, Marti Ras, N, et al. Iso-
lation of Lyme disease Borrelia from puffins (Fratercula
arctica) and seabird ticks (Ixodes uriae) on the Faeroe Is-
lands. J Clin Microbiol 1999; 37:890–896.
Olsen, B, Jaenson, TG, Noppa, L, Bunikis, J, et al. A Lyme
borreliosis cycle in seabirds and Ixodes uriae ticks. Na-
ture 1993; 362:340–342.
Olsen, B, Duffy, DC, Jaenson, TG, Gylfe, A, et al. Trans-
hemispheric exchange of Lyme disease spirochetes by
seabirds. J Clin Microbiol 1995; 33:3270–3274.
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.
Stanek, G, O’Connell, S, Cimmino, M, Aberer, E, et al. Eu-
ropean Union Concerted Action on Risk Assessment in
Lyme Borreliosis: clinical case definitions for Lyme bor-
reliosis. Wien Klin Wochenschr 1996; 108:741–747.
Tsao, JI, Wootton, JT, Bunikis, J, Luna, MG, et al. An eco-
logical approach to preventing human infection: vacci-
nating wild mouse reservoirs intervenes in the Lyme
disease cycle. Proc Natl Acad Sci USA 2004; 101:
18159–18164.
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.
456