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Molecular evidence of tick-transmitted

infections in dogs and cats in the United
Kingdom
S. E. Shaw, S. H. Binns, R. J. Birtles, M. J. Day, R. Smithson, M. J. Kenny

PCR analysis was used to determine the prevalence of tick-transmitted infections in 120 systemically ill dogs
and 60 cats recruited over a period of three months from 52 veterinary practices in the UK. The animals had
not travelled outside the UK and had one or more of the following clinical criteria: acute or recurrent pyrexia,
anaemia and/or thrombocytopenia, polyarthritis/muscle pain, splenomegaly/lymphadenopathy, and
intraocular inflammation with systemic signs. Blood samples from the animals were tested for the presence
of DNA from Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum by using simple PCR targeting.
B burgdorferi sensu lato was detected in five dogs and two cats, and A phagocytophilum was detected in
one dog and one cat. These results provide the first molecular evidence of naturally occurring B burgdorferi
sensu lato infection in cats in the UK and confirm that A phagocytophilum infection is present in cats. There
were no statistically significant associations between the infections and the clinical signs shown by the dogs
and cats.

THE expansion of domestic housing and recreation into rural may also warn of the risk of human exposure to A phagocy-
and sylvatic environments, together with the apparent effects tophilum.
of climate change, have resulted in increased interest in vec- Serological and PCR assays (particularly when routine cul-
tor-transmitted infections in general, and tick-transmitted ture is difficult) can provide complementary information on
infections in particular (Patz and others 2000). Companion the epidemiology and pathogenesis of bacterial infections.
dogs and cats in the UK are commonly infested with Ixodes Serological assays play a major role in prevalence studies, but
ricinus and Ixodes hexagonus ticks (Ogden and others 2000), PCR assays can detect active infection and characterise the
but there is little information about the extent to which they infectious agent more specifically. In both Borrelia and
may be infected with the major Ixodes-transmitted pathogens, Anaplasma species infections, persistent antibody production
Borrelia burgdorferi sensu lato (B burgdorferi) and Anaplasma and recurrent exposure make correlation of serology with
(previously Ehrlichia) phagocytophilum. clinical signs difficult.
Veterinary Record (2005) Serological surveys for B burgdorferi infection have indi- The aims of this study were to determine the prevalence of
157, 645-648 cated a prevalence of 4·5 to 11 per cent in dogs (May and oth- active B burgdorferi and A phagocytophilum infections in a
ers 1991, Liu and others 1988) and 4·8 per cent in cats (May group of systemically ill companion dogs and cats by using
S. E. Shaw, BVSc, MSc, and others 1994). In continental northern Europe, dogs are PCR tests, and to determine whether there was any association
DECVIM, DACVIM, commonly seropositive to B burgdorferi, and chronic mus- between the infections and the clinical signs associated with
FACVSc, MRCVS, culoskeletal and/or neurological signs compatible with bor- them in other European countries.
M. J. Day, BSc, BVMS, PhD, reliosis and associated with high or rising antibody titres to
FASM, DECVP, MRCPath, B burgdorferi have been reported (McKenna and others 1995,
FRCVS, Hovius and others 2000). In contrast, in the UK, reports of MATERIALS AND METHODS
M. J. Kenny, BSc, PhD, dogs with disease associated with evidence of exposure to
School of Clinical B burgdorferi are uncommon (May and others 1990), and Recruitment of veterinary practices and animals
Veterinary Science, seropositivity is difficult to correlate with clinical signs (May Veterinary practices were recruited from many parts of the UK
University of Bristol, and others 1991). Although there is serological evidence of (Fig 1) by using direct mailing, and their enrolment in the
Langford House, B burgdorferi infection in cats in Europe, no naturally occur- study was confirmed by fax. Fifty-two practices were enrolled,
Langford, Bristol ring active infection has been reported. 30 of which had taken part in a previous study of the species
BS40 5DU In dogs, granulocytic ehrlichiosis characterised by acute of ticks attached to dogs and cats (Ogden and others 2000).
S. H. Binns, MA, VetMB, fever, weakness, lameness and thrombocytopenia caused by One hundred and twenty dogs and 60 cats, 12 months of
MSc, PhD, MRCVS, A phagocytophilum is well recognised in many northern age or older and with a current vaccination history (up to five
Centre for Epidemiology European countries, and almost 17 per cent of Swedish dogs dogs and five cats from each of the practices), were recruited
and Risk Analysis, are seropositive (Egenvall and others 1997). A single case of between August and October 2001. A clinical history was
Veterinary Laboratories A phagocytophilum infection has been reported in a European available for each animal, including information on the envi-
Agency – Weybridge, domestic cat (Bjöersdorff and others 1999). A phagocy- ronment in which the animal was housed and exercised.
New Haw, Addlestone, tophilum infection is well recognised in ruminants, deer and Animals that had travelled outside the UK were excluded. Each
Weybridge KT15 3NB rodents in the UK (Ogden and others 1998), but its prevalence animal had one or more of the clinical signs previously asso-
R. J. Birtles, BSc, PhD, in domestic dogs and cats is unknown and there are no vali- ciated with tick-transmitted diseases in other European coun-
Department of Veterinary dated serological methods available for these species in the tries: recurrent pyrexia, acute-onset pyrexia with weakness
Pathology, University of UK. However, dogs with compatible clinical signs and intra- and lethargy, anaemia and/or thrombocytopenia, polyarthri-
Liverpool, Leahurst, neutrophilic inclusions (Clark and others 1996), or with com- tis and/or muscle pain, splenomegaly and/or lymphaden-
Neston, Cheshire patible clinical signs and the presence of A phagocytophilum opathy, and intraocular inflammation with systemic signs. In
CH64 7TE DNA, have been reported in the UK (Shaw and others 2001). all cases no specific causes had been determined for these clin-
R. C. Smithson, BVetMed, Both B burgdorferi and A phagocytophilum are human ical signs.
MRCVS, pathogens and their presence in domestic pets may affect
Merial Animal Health, human health. Although dogs and cats are considered to be Collection of blood samples
Sandringham House, accidental hosts, companion dogs have been shown to be sen- Samples of anticoagulated blood (1 ml in EDTA) taken from
Harlow, Essex CM19 5TG tinels for human borreliosis (Goossens and others 2001) and samples submitted for diagnostic purposes from each animal

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Papers & Articles

were sent, with the owner’s consent, to the Acarus Laboratory,

Department of Clinical Veterinary Science, University
of Bristol, within 24 to 48 hours of collection; they were
labelled with a number identifying the animal and the prac-
tice. On arrival at the laboratory, the samples were frozen at
–80°C.

DNA extraction and PCR analyses

B burgdorferi was detected by using primers BSL F and BSL R
to target the ospA gene, giving an amplicon size of approxi-
mately 300 base pairs (bp) (Demaerschalck and others 1995).
For A phagocytophilum, a species-specific PCR amplifying a
619 bp fragment of the 16S rRNA gene was used (Engvall and
others 1996). It had been shown that both PCR assays could
detect fewer than five organisms per sample or 1250 organ-
isms/ml. The analyses were performed in duplicate. Positive
controls for the A phagocytophilum PCR assay were blood sam-
ples from a confirmed case of bovine infection, and positive
controls for the B burgdorferi PCR assay were cultured
B burgdorferi sensu stricto. Negative controls consisted of
water and DNA extracted from animals shown by PCR to be
negative for the organisms.
DNA was extracted from 200 µl of blood by using a stan-
dard silica cartridge method (QIAamp DNA mini kit; Qiagen)
according to the manufacturer’s protocol. The DNA was eluted
in 100 µl of elution buffer and 2 µl of the extracted DNA was
used in each PCR assay. The amplicons were isolated by
agarose gel electrophoresis and visualised by UV illumination
of ethidium bromide-stained gels. In order to confirm the
species of bacteria present in any positive sample, the ampli-
fied DNA was purified (Nucleo-Spin Extract; Machery Nagel)
and sequenced using the same primers as for the PCR
(GRI-genomics). The DNA sequences obtained were compared
with sequences lodged in GenBank by using the BLAST pro-
gram.
0 50 100 km
Statistical analysis
The results were analysed by using EpiInfo 2000 (Centers for
Disease Control and Prevention). The potential association
of each group of clinical signs with the PCR-detected infection
was examined by using Fisher’s exact test. An alpha-level of
0·05 was used.
FIG 1: Geographical distribution of the veterinary practices that took part in the study

RESULTS
DISCUSSION
Five of the 120 dogs and two of the 60 cats were positive for
B burgdorferi, and one dog and one cat were positive for Only a few animals with tick-transmitted pathogens were
A phagocytophilum. No co-infections with B burgdorferi and detected, but they were distributed widely throughout the UK
A phagocytophilum were detected. All the amplicons obtained and had access to habitats ranging from suburban gardens to
from the Borrelia PCR reactions had DNA sequences consistent upland moor, illustrating the variety of habitats in which
with B burgdorferi. However, the quality of the amplified DNA, companion animals and their owners may be exposed to ticks
and the region of the gene sequenced, made it possible to infected with B burgdorferi or A phagocytophilum.
identify the infecting genospecies unambiguously. The ampli- Four per cent of the samples were positive for active
cons from samples positive for A phagocytophilum had DNA B burgdorferi infection, a proportion consistent with the
sequences that were identical to those of A phagocytophilum prevalence of exposure to the organism reported by Liu and
(Genbank AY082656). others (1988) and May and others (1991, 1994). However,
The geographical distribution of the positive cases and the because spirochaetes are more easily detectable by PCR in the
clinical signs associated with them are shown in Table 1. The blood in the early stages of infection than after tissue locali-
positive dogs lived in suburban areas but had access to upland sation has occurred, the PCR analysis of peripheral blood
and/or woodland habitats, and the positive cats lived in sub- samples may have underestimated the prevalence of infection
urban areas and had access to garden, parkland or industrial (Demaerschalck and others 1995). The study was conducted
wasteland. during late summer and autumn, when I ricinus nymphs and
There were too few positive cases for a separate analysis for adults are reported to be active in the UK. Self-limiting infec-
each pathogen, and all the cases that were positive for either tions resulting from the spring peak of tick activity may there-
B burgdorferi or A phagocytophilum in either dogs or cats were fore not have been detected (Gray 1991, Randolph and others
therefore combined for analysis. Fisher’s exact test showed 2002), but chronic persistent infections that have been asso-
that there was no significant association between the infec- ciated with borreliosis in dogs would have been detected
tions detected by PCR and any particular clinical syndrome (McKenna and others 1995, Hovius and others 2000). Less is
in the dogs or cats (Tables 2, 3). known of the biology of I hexagonus, particularly in relation

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TABLE 1: Historical and clinical information for the three cats and six dogs that were PCR TABLE 2: Numbers and percentages of the 60 cats with
positive for Anaplasma phagocytophilum or Borrelia burgdorferi sensu lato different clinical syndromes and the numbers that were PCR
positive for Anaplasma phagocytophilum or Borrelia
Animal PCR positive Location Clinical syndrome
burgdorferi sensu lato
Cat B burgdorferi Enniskillen, Fermanagh Chronic recurrent fever, renal disease Number (%) Number
Cat B burgdorferi Swindon, Wiltshire Chronic recurrent fever, weight loss Clinical syndrome of cats positive
Cat A phagocytophilum Scarborough, North Yorkshire Acute fever, weakness, lethargy
Dog A phagocytophilum Frome, Somerset Bleeding from surgical site, Recurrent pyrexia 39 (65) 2
splenomegaly Acute pyrexia, weakness, lethargy 20 (33·3) 1
Dog B burgdorferi Edinburgh, Lothian Chronic recurrent fever, Anaemia, thrombocytopenia 7 (11·7) 0
lymphadenopathy, splenomegaly Polyarthritis and/or muscle pain 6 (10) 0
Dog B burgdorferi Biggin Hill, Kent Uveitis, ocular disease Splenomegaly and/or lymphadenopathy 6 (10) 0
Dog B burgdorferi Broadway, Gloucestershire Chronic recurrent fever, lethargy Intraocular inflammation with systemic signs 3 (5) 0
Dog B burgdorferi Swindon, Wiltshire Acute fever, lethargy, weakness
Dog B burgdorferi Scarborough, North Yorkshire Acute fever, lethargy, weakness

TABLE 3: Numbers and percentages of the 120 dogs with

different clinical syndromes and the numbers that were PCR
positive for Anaplasma phagocytophilum or Borrelia
to companion animals, but all its stages are active during the burgdorferi sensu lato
autumn (Hillyard 1996).
The results provide the first molecular evidence of natu- Number (%) Number
Clinical syndrome of dogs positive
rally occurring B burgdorferi infection in cats. Cats are sus-
ceptible to experimental infection with the organism (Burgess Recurrent pyrexia 46 (38·3) 4
1992), and studies of archived feline sera from the USA and Acute pyrexia, weakness, lethargy 33 (27·5) 2
Europe have recorded a significant prevalence of antibody Anaemia, thrombocytopenia 15 (12·5) 1
Polyarthritis and/or muscle pain 26 (21·7) 0
titres against B burgdorferi (Magnarelli and others 1990, May Splenomegaly and/or lymphadenopathy 16 (13·3) 0
and others 1994, Linder and Bockel 1995). The results also Intraocular inflammation with systemic signs 5 (4·2) 1
provide the first molecular evidence of B burgdorferi infection
in dogs in the UK.
There has been little work to characterise the genospecies
of B burgdorferi infecting dogs in Europe, and none for to cause fever, lethargy and lameness with joint swelling
cats. Infections of dogs with Borrelia afzelli, Borrelia garinii, (Gibson and others 1995). There have been so few cats
B burgdorferi sensu stricto and Borrelia valaisiana, and co- reported with A phagocytophilum infection that no meaning-
infections involving several Borrelia species, have been iden- ful association with clinical signs is possible. Furthermore, the
tified in the Netherlands, Germany and Switzerland by PCR, immunosuppression in ill, tick-exposed dogs and cats may
in situ hybridisation and/or culture (Hovius and others 1999, result in the recrudescence of a previously asymptomatic
Leibisch and Leibisch 1999, Speck and others 2001). The B burgdorferi or A phagocytophilum infection (Straubinger
genospecies B afzelli, B garinii and B burgdorferi sensu stricto and others 1997, Egenvall and others 2000), thus complicat-
are important pathogens, and studies of their prevalence ing the clinical signs, diagnosis and outcome of a pre-existing
in the UK may provide further information on the risk to disease process. However, A phagocytophilum infection in
companion animals and their owners. All three Borrelia dogs has not been associated with an increased predisposition
genospecies have been identified in I ricinus ticks in Scotland to opportunistic infections, unlike the corresponding infec-
(Ling and others 2000). The annual incidence of Lyme disease tion in sheep (Larsen and others 1994) and in fatal human
in people in the UK is much lower than in France, Sweden and cases (Lepidi and others 2000). In dogs infected experimen-
Slovenia, and was estimated in 1998 to be 0·32 per 100,000 tally with A phagocytophilum, neutrophil phagocytosis and
of the population in England and Wales; however, reporting the intracellular killing of pathogens other than A phagocyto-
is voluntary and the incidence is considered to be increasing philum were not impaired (Lilliehöök and others 1999). A
(Smith and others 2000). case-control study of the prevalence of these infections in
The results also reveal A phagocytophilum infection in cats healthy and ill dogs and cats would help to establish whether
for the first time in the UK, a finding that is consistent with the there is any association between the infections and clinical
reports of A phagocytophilum infection in dogs in the UK disease.
(Clark and others 1996, Shaw and others 2001). Human Clinical borreliosis is better defined in human beings than
granulocytic ehrlichiosis caused by A phagocytophilum is well in companion animals owing to the pathognomonic clinical
recognised in many European countries, and a low level sign of erythema migrans; nevertheless, the correlation
of exposure has been identified in English farm workers between clinical disease in people in the UK and the prevalence
(Thomas and others 1998). However, no clinical illness in of B burgdorferi infection is still poor (Smith and others
people due to this infectious agent has yet been established in 2000). It is possible that some of the infection in both com-
the UK. The patterns of infection with A phagocytophilum in panion animals and people in the UK is due to the less path-
companion dogs and cats may provide further information ogenic genospecies B valaisiana, which is prevalent in
on the risk to their owners. populations of I ricinus ticks in the UK (Kurtenbach and oth-
There were no significant associations between the ers 1998). Characterisation of the Borrelia genospecies infect-
B burgdorferi or A phagocytophilum infections detected by PCR ing companion animals would allow more accurate diagnosis.
and any of the clinical syndromes suffered by the dogs and The results of this study suggest that there are low but
cats. However, there were few positive cases and it was not potentially significant levels of infection with tick-transmit-
possible to analyse the results for each pathogen separately. ted pathogens in companion animals in the UK, although their
It is recognised that the clinical signs associated with borreli- association with clinical disease remains unclear.
osis and granulocytic ehrlichiosis in dogs may not be pathog-
nomonic (Levy and Magnarelli 1992, Egenvall and others
1997), and the present results support this finding. There have ACKNOWLEDGEMENTS
been no descriptions of naturally occurring disease associated
with B burgdorferi infection in cats, but some experimental The authors thank all the veterinary practitioners for collect-
infections with B burgdorferi sensu stricto have been reported ing the blood samples. The study was funded by Merial

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Papers & Articles

Animal Health. The BLAST program is hosted by NCBI, DUMLER, J. S. (2000) Comparative pathology and immunohistology asso-
National Institutes of Health, USA (www.ncbi.nlm.nih.gov). ciated with clinical illness after Ehrlichia phagocytophila-group infections.
American Journal of Tropical Medicine and Hygiene 62, 29-37
LEVY, S. A. & MAGNARELLI, L. A. (1992) Relationship between development
of antibodies to Borrelia burgdorferi in dogs and the subsequent development
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Molecular evidence of tick-transmitted

infections in dogs and cats in the United
Kingdom
S. E. Shaw, S. H. Binns, R. J. Birtles, M. J. Day, R. C. Smithson and M. J.
Kenny

Veterinary Record 2005 157: 645-648

doi: 10.1136/vr.157.21.645

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