Ectoparasites of dogs and cats in Albania


Xhaxhiu, D.; Kusi, I.; Rapti, D.; Visser, M.; Knaus, M.; Lindner, T.; Rehbein, S.

Parasitology Research 105(6): 1577-1587

2010


One hundred eighty-one dogs and 26 short-hair cats from suburban areas around Tirana, Albania were examined for ectoparasite infestation. The dogs were examined on several occasions from 2005 through 2009 representing three seasons: winter (December-February), spring (March-May), and summer (June-August); the cats were examined in late autumn (November). In addition, deep ear swab specimens of 30 dogs were examined for ear mites. The arthropod ectoparasite fauna of the dogs included two tick species (Rhipicephalus sanguineus and Ixodes ricinus), three mite species (Sarcoptes scabiei var. canis, Otodectes cynotis, and Demodex canis), three flea species (Ctenocephalides canis, Ctenocephalides felis, and Pulex irritans), and one louse species (Trichodectes canis). In the dogs, rates of infestation were 23.8% for R. sanguineus, 0.6% for I. ricinus, 4.4% for S. scabiei var. canis, 6.7% for O. cynotis, 0.6% for D. canis, 75.7% for C. canis, 5.0% for C. felis, 8.3% for P. irritans, and 6.6% for T. canis. Mixed infestation with two or three species of ectoparasites was recorded on 38.1% of the dogs. Fleas infested 75.7% dogs (geometric mean, 3.96; range, 1-80) and were observed in winter, spring, and summer with increasing prevalences of 64.3%, 75.9%, and 100%. Ticks parasitized 24.3% of the dogs (geometric mean, 0.41; range, 1-331). R. sanguineus ticks were recorded on 34.2% and 50% of the dogs examined in spring and summer, respectively, but were absent on the dogs during winter except for a single I. ricinus specimen observed. Prevalence of infestation with R. sanguineus, S. scabiei var. canis, C. felis, P. irritans, and T. canis did not differ between dogs < or = 6 months and dogs > 6 months of age; however, prevalence of infestation with C. canis was significantly (p < 0.01) higher in dogs > 6 months old. There was no difference between the sexes for the prevalences of infestation with those parasites. The examination of the cats revealed infestation with only one species of ectoparasite, C. felis (prevalence, 100%; geometric mean, 2.5; range, 1-9).

Parasitol
Res
(2009)
105:1577-1587
DOI
10.1007/s00436-009-1591-x
ORIGINAL
PAPER
Ectoparasites
of
dogs
and
cats
in
Albania
Dashamir
Xhaxhiu
Ilir
Kusi
Dhimiter
Rapti
Martin
Visser
Martin
Knaus
Thomas
Lindner
Steffen
Rehbein
Received:
15
July
2009
/Accepted:
30
July
2009
/Published
online:
19
August
2009
C
Springer-Verlag
2009
Abstract
One
hundred
eighty-one
dogs
and
26
short-hair
cats
from
suburban
areas
around
Tirana,
Albania
were
examined
for
ectoparasite
infestation.
The
dogs
were
examined
on
several
occasions
from
2005
through
2009
representing
three
seasons:
winter
(December—February),
spring
(March—May),
and
summer
(June—August);
the
cats
were
examined
in
late
autumn
(November).
In
addition,
deep
ear
swab
specimens
of
30
dogs
were
examined
for
ear
mites.
The
arthropod
ectoparasite
fauna
of
the
dogs
included
two
tick
species
(Rhipicephalus
sanguineus
and
Ixodes
ricinus),
three
mite
species
(Sarcoptes
scabiei
var.
canis,
Otodectes
cynotis,
and
Demodex
canis),
three
flea
species
(Ctenocephalides
canis,
Ctenocephalides
felis,
and
Pulex
irritans),
and
one
louse
species
(Trichodectes
canis).
In
the
dogs,
rates
of
infestation
were
23.8%
for
R.
sanguineus,
0.6%
for
I.
ricinus,
4.4%
for
S.
scabiei
var.
canis,
6.7%
for
0.
cynotis,
0.6%
for
D.
canis,
75.7%
for
C.
canis,
5.0%
for
D.
Xhaxhiu
I.
Kusi
IClinika
Veterinare,
Bulevardi
Gjergj
Fishta,
Kulla
II
Jeshile,
Ap.
3,
Tirana,
Albania
D.
Rapti
Universiteti
Bujqesor,
Fakulteti
i
Mjeksise
Veterinare,
Koder
ICamez,
Tirana,
Albania
M.
Visser
M.
ICnaus
S.
Rehbein
(M)
Merial
GmbH,
ICathrinenhof
Research
Center,
Walchenseestr.
8-12,
83101
Rohrdorf,
Germany
e-mail:
T.
Lindner
IDT
Biologika
GmbH,
Am
Pharmapark,
06861
Dessau-RoBlau,
Germany
C.
felis,
8.3%
for
P
irritans,
and
6.6%
for
T
canis.
Mixed
infestation
with
two
or
three
species
of
ectoparasites
was
recorded
on
38.1%
of
the
dogs.
Fleas
infested
75.7%
dogs
(geometric
mean,
3.96;
range,
1-80)
and
were
observed
in
winter,
spring,
and
summer
with
increasing
prevalences
of
64.3%,
75.9%,
and
100%.
Ticks
parasitized
24.3%
of
the
dogs
(geometric
mean,
0.41;
range,
1-331).
R.
sanguineus
ticks
were
recorded
on
34.2%
and
50%
of
the
dogs
examined
in
spring
and
summer,
respectively,
but
were
absent
on
the
dogs
during
winter
except
for
a
single
I.
ricinus
specimen
observed.
Prevalence
of
infestation
with
R.
sanguineus,
S.
scabiei
var.
canis,
C.
felis,
P.
irritans,
and
T
canis
did
not
differ
between
dogs
<6
months
and
dogs
>6
months
of
age;
however,
prevalence
of
infestation
with
C.
canis
was
significantly
(p<0.01)
higher
in
dogs
>6
months
old.
There
was
no
difference
between
the
sexes
for
the
prevalences
of
infestation
with
those
parasites.
The
examina-
tion
of
the
cats
revealed
infestation
with
only
one
species
of
ectoparasite,
C.
felis
(prevalence,
100%;
geometric
mean,
2.5;
range,
1-9).
Introduction
In
many
areas
of
the
world,
fleas
(Siphonaptera)
and
hard
ticks
(Ixodidae)
are
considered
the
most
common
and
most
important
external
parasites
infesting
dogs
and
cats.
Studying
the
species
infesting
ticks
and
fleas
of
dogs
and
cats
is
important
for
several
reasons.
Infestation
with
these
ectoparasites
can cause
in
considerable
discomfort
and
dermatological
reactions
as
they
affect
their
hosts
directly
by
feeding
blood
and
cause
dermatitis
and
other
allergic
reactions.
Ticks,
after
mosquitoes,
are
the
second
most
important
arthropods
that
may
transmit
pathogens
like
viruses,
bacteria
including
rickettsiae,
protozoa,
and
filarial
4Z
Springer
1578
Parasitol
Res
(2009)
105:1577-1587
nematodes
to
other
animals
and
humans.
While
ticks
are
notorious
as
vectors
of
disease
agents,
fleas
can
also
transmit
pathogens,
such
as
the
agents
of
flea-born
rickettsioses,
and
can
serve
as
intermediate
hosts
of
some
species
of
cestodes.
Different
species
of
ticks
and
fleas
may
infest
dogs
and
cats
in
different
geographical
regions.
These
geographical
differences
may
influence
the
risk
of
arthropod-borne
disease
agents
and
parasite
transmission,
not
only
between
animals
but
also
between
animals
and
humans,
and
they
may
have
implications
for
the
measures
used
to
control
these
ectoparasites.
Scarce
information
is
available
on
the
parasites
of
dogs
from
Albania,
and
in
most
cases,
it
dates
back
to
papers
published
in
the
1960s
and
1970s
(Moskvin
1958;
Danielova
1960;
Prokopi6
1960;
RosickST
and
Gjini
1960;
RosickST
et
al.
1960;
Luli
1963;
Gina
1973;
Gina
and
Kastrati
1974;
Gina
et
al.
1975;
Adhami
and
Murati
1977),
except
for
some
recent
reports
on
canine
arthropod-borne
diseases,
and
in
particular
leishmaniosis,
because
of
its
association
to
human
visceral leishmaniosis
(Kero
and
Xinxho
1998;
Cicko
et
al.
1999;
Sotira
2000;
Cani
et
al.
2001;
Dhamo
et
al.
2006;
Lazri
et
al.
2008).
As
the
ectoparasites
of
dogs
in
Albania
were
not
studied
since
the
1970s,
this
paper
reports
the
results
of
the
identification
of
arthropod
parasites
collected
from
dogs
and
cats
in
Tirana,
Albania
from
2005
through
2009.
Materials
and
methods
In
total,
181
dogs
(179
mixed
breed
dogs,
one
Pitbull
cross,
and
one
German
shepherd;
71
males,
one
male
castrated,
109
females;
approximately
2
months
to
10
years
old:
111<6
months,
70>6
months),
and
26
short-hair
cats
(ten
males,
16
females;
approximately
3
months
to
8
years
old)
from
suburban
areas
of
Tirana
were
examined
for
ectoparasite
infestation
at
the
Institute
of
Veterinary
Research
Tirana,
the
Veterinary
Faculty
of
the
Tirana
Agricultural
University,
or
a
private
small
animal
veterinary
practice
in
Tirana.
The
dogs
were
examined
on
several
occasions
which
were
blocked
to
three
seasons:
winter
(December—February),
70
dogs;
spring
(March—May),
79
dogs;
and
summer
(June—August),
32
dogs;
the
cats
were
examined
in
late
autumn
(November).
The animals
were
examined
for
ectoparasite
infestation
by
a
body
search,
and
the
whole
body
was
combed
with
a
stainless
steel
fine-toothed
flea
comb
(Zakson
et
al.
1995).
Ticks
were
manually
removed
and
collected
together
with
any
fleas
and
lice
in
the
comb.
For
the
32
dogs
examined
in
the
summer
season,
the
ectoparasite
load
for
ticks
and
fleas
was
determined
by
a
whole
body
comb;
however,
only
up
to
five
specimens
each
of
ticks
and
fleas
were
collected
for
identification
from
the
dogs.
The
ticks,
fleas,
and
lice
41?!
Springer
removed
from
the
animals
were
stored
in
70%
ethanol
until
they
were
identified.
When
lesions
suspicious
of
mite
infestation
(characterized
by
scaling,
scores,
dermal
encrus-
tations,
and
hair
loss)
were
observed
during
the
body
search,
scrapings
were
taken
from
the
altered
skin.
Deep
ear
swab
specimens
were
obtained
from
both
ears
from
30
of
the
70
dogs
sampled
during
the
winter
season
and
examined
for
the
presence
of
ear
mites.
For
identification
and
determination
of
sex
using
a
binocular
microscope,
the
ticks,
fleas,
and
lice
were
cleared
in
10%
potassium
hydroxide.
Skin
scrapings
and
ear
swabs
were
placed
in
10%
potassium
hydroxide
and
gently
heated
to
macerate
scales,
crusts,
and
hair
or
aural
material.
Thereafter,
the
material
was
centrifuged,
and
the
sediment
was
microscopically
examined
for
mites.
Ectoparasites
were
identified
using
descriptions
and/or
keys
(Jancke
1938;
Peus
1938;
Babos
1964;
Hiepe
and
Ribbeck
1982;
Estrada-Pefta
et
al.
2004).
The
following
parasitological
parameters
were
evaluated:
percentage prevalence
(proportion
of
hosts
infested
with
an
ectoparasite
taxon),
intensity
(arithmetic
mean
count
of
ectoparasites
of
a
taxon
on
infested
hosts),
and
abundance
(geometric
mean
count
of
ectoparasites
of
a
taxon
on
examined
hosts;
Bush
et
al.
1997).
Chi-squared
tests
were
used
to
compare
the
prevalence
of
ectoparasite
infestation
between
the
dogs'
ages
and
sexes.
To
determine
significant
association
for
seasonality
of
collection
and
infestation
rates
for
dogs,
chi-squared
test
for
3
x2
contingency
table
was
used.
Ectoparasite
intensity
was
compared
using
the
Mann—
Whitney
U
test
for
two
independent
groups
and
the
Kruskal—
Wallis
test
for
multiple
comparisons.
Results
Total
prevalence
and
intensity
of
external
parasite
infesta-
tion
recorded
by
body
search
including
whole
body
comb
and
examination
of
skin
scrapings
from
suspicious
skin
areas
are
given
in
Table
1.
Using
these
techniques,
arthropod
ectoparasites
were
found
on
143
dogs
(79.0%)
and
26
cats
(100%).
Two
species
each
of
ticks,
Rhipicephalus
sanguineus
(adults
and
nymphs)
and
Ixodes
ricinus
(one
adult
female);
and
mites,
Sarcoptes
scabiei
var.
canis
and
Demodex
canis;
three
species
of
fleas,
namely
Ctenocephalides
canis,
Ctenocephalides
felis,
and
Pulex
irritans;
and
one
biting
louse,
Trichodectes
canis,
were
identified
on
the
dogs.
Only
one
species
of
flea,
C.
felis,
was
recorded
on
the
cats.
In
addition,
examination
of
ear
swabs
obtained
from
30
dogs
during
the
winter
season
revealed
the
presence
of
ear
mites,
Otodectes
cynotis,
in
two
dogs
which
did
not
carry
any
other
ectoparasite.
The
most
common
ectoparasites
were
fleas
which
were
recorded
on
137
dogs
(75.7%)
and
on
all
cats,
with
total
Parasitol
Res
(2009)
105:1577-1587
1579
Table
1
Prevalence
and
intensity
of
ectoparasite
species
on
dogs
and
cats
with
either
single
or
mixed-species
infestation
Body
search
including
whole
body
comb
and
examination
of
skin
scrapings
Dogs
(n=181)
Cats
(n=26)
Prevalence
total
(%)
Intensity,
AM
(range)
$
Abundance,
GM"
Prevalence
total
(%)
Intensity,
AM
(range)
Abundance
GM
R.
sanguineus
I
ricinus
43
(23.8)
1
(0.6)
Total
ticks
44
(24.3)
11.5
(1-331)
0.41
S.
scabiei
var.
canis
8
(4.4)
D.
canis
1
(0.6)
C.
canis
137
(75.7)
C.
felis
9
(5.0)
26
(100)
P
irritans
15
(8.3)
Total
fleas
137
(75.7)
12.0
(1-80)
3.96
26
(100)
2.9
(1-9)
2.5
T
canis
12
(6.6)
AM
arithmetic
mean,
GM
geometric
mean
a
Infested
animals
b
All
animals
individual
flea
counts
ranging
from
one
to
80
in
the
dogs
and
from
one
to
nine
in
the
cats.
In
the
dogs,
C.
canis
was
the
predominant
species
identified
on
any
flea-infested
dog,
while
C.
felis
and
P.
irritans
were
recorded
occasionally
only
as
single
specimens
and
concurrently
with
C.
canis.
Apart
from
one
dog
carrying
331
R.
sanguineus
ticks,
individual
tick
counts
ranged
from
one
to
18.
A
total
of
69
(38.1%)
dogs
were
infested
with
two
(29.8%)
or
three
(8.3%)
species
of
ectoparasites.
R.
sanguineus
plus
C.
canis
infestation
was
the
most
common
combination
(Table
2).
Rates
of
infestation
with
R.
sanguineus,
S.
scabiei
var.
canis,
C.
felis,
P.
irritans,
and
T
canis
was
not
different
(p>0.1)
between
dogs
<6
months
and
dogs
>6
months
of
age;
however,
the
rate
of
infestation
with
C.
canis
was
significantly
(p<0.01)
higher
in
dogs
>6
months
old.
There
was
no
difference
(p>0.1)
between
the
sexes
for
the
rates
of
infestation
with
those
parasites
(Table
3).
Testing
R.
sanguineus
and
total
flea
counts
vs
host
age
revealed
no
difference
(p=0.686)
for
ticks
between
dogs
<6
months
and
dogs
>6
months
of
age
(geometric
mean
tick
counts
0.41
and
0.40,
respectively),
while
the
older
dogs
carried
significantly
(p<0.0001)
more
fleas
than
the
younger
ones
(geometric
mean
flea
counts
7.48
and
2.54,
respectively). There
was
no
difference
in
the
male
and
female
dogs'
R.
sanguineus
counts
(all
dogs:
p=0.281,
geometric
mean
tick
counts
0.52
and
0.33,
respectively;
dogs
>6
months:
p=0.207,
geometric
mean
tick
counts
0.52
and
0.31,
respectively)
and
total
flea
burdens
(all
dogs:
p=
0.636,
geometric
mean
flea
counts
3.70
and
4.15,
respec-
tively;
dogs
>6
months:
p=0.750,
geometric
mean
flea
counts
7.31
and
7.65,
respectively).
The
seasonality
of
the
ectoparasites
infesting
the
dogs
in
Tirana
is
given
in
Table
4.
Infestation
rates
for
R.
sanguineus
and
fleas
showed
a
significant
variation
among
seasons
of
collection
(p<0.001).
R.
sanguineus
ticks
were
recorded
on
34.2%
and
50%
of
the
dogs
examined
in
spring
and
summer,
respectively,
but
they
were
absent
in
winter.
Flea
infestation,
however,
was
observed
in
winter,
spring,
and
summer
with
increasing
prevalences
of
64.3%,
75.9%,
and
100%,
respec-
tively
(Fig.
1).
Using
the
score
described
by
Marchiondo
et
al.
(2007),
approximately
two
thirds
of
the
R.
sanguineus
infested
dogs
carried
a
low
level
infestation
of
up
to
three
ticks,
and
the
tick
load
of
one
sixth
each
of
the
dogs
was
moderate
(four
to
ten
ticks/animal)
or
high
(>10
ticks/animal).
Using
the
score
described
by
Marchiondo
et
al.
(2007)
to
categorize
the
infestation
level
of
fleas
on
dogs
and
cats,
42.4%
of
the
dogs
carried
a
low
level
infestation
of
up
to
five
fleas
each,
and
the
infestation
level
was
moderate
(six
to
20
fleas/animal)
and
high
(>20
fleas/animal)
in
37.2%
and
20.4%
of
the
dogs,
respectively.
Nearly
90%
of
the
cats
carried
a
low
level
flea
infestation,
and
the
remaining
cats
showed
a
moderate
level
of
infestation.
For
the
dogs,
infestation
level
scores
for
R.
sanguineus
and
fleas
in
relation
to
season
are
shown
in
Table
5
and
Fig.
2.
Similarly
to
prevalence,
geometric
mean
R.
sanguineus
and
flea
counts
of
the
dogs
varied
significantly
between
seasons
(Table
6).
A
total
of
956
fleas
were
collected
from
the
dogs
and
cats
examined
in
winter
plus
spring
or
autumn,
respectively.
4Z
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1580
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Table
2
Occurrence
of
mixed
ectoparasite
infestations
in
the
Mixed-species
ectoparasite
infestation
Prevalence,
total
(%)
[69
(38.1)]
dogs
from
Tirana
(n=181)
Three
species
R.
sanguineus+D.
canis+C.
canis
1
(0.6)
R.
sanguineus+C.
canis+C.
fells
4
(2.2)
R.
sanguineus+C.
canis+P.
irritans
3
(1.7)
R.
sanguineus+C.
canis+T.
canis
3
(1.7)
S.
scabiei
var.
canis+C.
canis+T.
canis
1
(0.6)
C.
canis+C.
felis+P.
irritans
1
(0.6)
C.
canis+C.
felis+T.
canis
1
(0.6)
C.
canis+P.
irritans+T.
canis
1
(0.6)
Two
species
R.
sanguineus+C.
canis
28
(15.5)
I
ricinus+C.
canis
1
(0.7)
S.
scabiei
var.
canis+C.
canis
6
(3.3)
C.
canis+C.
fells
4
(2.2)
C.
canis+P.
irritans
9
(5.0)
C.
canis+T.
canis
6
(3.3)
Sex
ratios
of
the
three
flea
species
were
female-biased
(Table
7).
Discussion
In
the
dogs
and
cats
from
Tirana,
nine
species
of
arthropod
ectoparasites
were
identified.
All
of
them
represent
com-
mon
parasites
of
canines
and
felines
in
many
areas
of
the
world,
but
only
R.
sanguineus,
I.
ricinus,
C.
canis,
and
P
irritans
had
been
previously
recorded
on
dogs
in
Albania
(RosickST
and
Gjini
1960;
RosickST
et
al.
1960;
Luli
1963;
Gina
1973;
Gina
and
Kastrati
1974;
Gina
et
al.
1975).
During
a
parasite
survey
conducted
by
researchers
from
the
former
Czechoslovak
Academy
of
Sciences
1958
in
Albania
(RosickST
1958,
1960),
Hippobosca
equina
was
collected
from
a
dog
in
Shkoder
(Danielova
1960).
In
Albania,
14
species
of
ixodid
ticks
belonging
to
the
genera
Ixodes,
Dermacentor,
Haemaphysalis,
Hyalomma,
Rhipicephalus
(Rhipicephalus),
and
Rhipicephalus
(Boophilus)
were
recorded
in
the
past
parasitizing
cattle,
water
buffalo,
sheep,
goats,
horses,
donkeys,
dogs,
rodents,
wild
birds,
and/or
reptiles
(Enigk
1947;
eernST
and
RosickST
1960;
RosickST
et
al.
1960;
Luli
1963;
Gina
1973, 1983;
Gina
and
Kastrati
1974;
Gina
et
al.
1975;
Zanaj
et
al.
2002)
or
collected
from
the
vegetation (Christova
et
al.
2003;
Lika
and
Bench°li
2004).
In
addition,
the
description
of
fowl
spirochetosis
in
Albania
(Carpano
1938)
suggests
the
presence
of
the
vector,
argasid
ticks.
R.
sanguineus
and
I.
ricinus
have
been
found
on
dogs
in
Albania
in
earlier
surveys:
R.
sanguineus
on
dogs
in
Tirana
and
in
the
districts
of
Shkoder
and
Saranda
and
I.
ricinus
on
dogs
in
the
city
and
district
of
Tirana
(RosickST
et
al.
1960;
Luli
1963;
Gina
1973;
Gina
and
Kastrati
1974).
Table
3
Prevalence
of
ectoparasite
infestation
in
relation
to
age
and
sex
of
the
dogs
(n=181)
Ectoparasite
Prevalence,
total
(%)
Age
Significance
(chi-square
test;
p)
Sex
a
Significance
(chi-square
test;
p)
<6months
>6months
Male
Female
(n=111)
(n=70)
(n=71)
(n=109)
R.
sanguineus
25
(22.5)
18
(25.7)
>0.1
19
(26.8)
23
(21.1)
>0.1
S.
scabiei
var.
canis
7
(6.3)
1
(1.4)
>0.1
3
(4.2)
5
(4.6)
>0.1
C.
canis
75
(67.6)
62
(88.6)
<0.01
51
(71.8)
85
(78.0)
>0.1
C.
fells
5
(4.5)
4
(5.7)
>0.1
5
(7.0)
4
(3.7)
>0.1
P.
irritans
10
(9.0)
5
(7.1)
>0.1
3
(4.2)
12
(11.0)
>0.1
T
canis
9
(8.1)
3
(4.3)
>0.1
5
(7.0)
6
(5.5)
>0.1
a
One
male
castrated
dog
excluded
from
analysis
41?!
Springer
Fig.
1
Prevalence
of
Rhipicephalus
sanguineus
and
flea
infestation
of
dogs
in
Tirana
Preva
lence
o
f
In
fes
ta
t
ion
(
%)
100
-
40
-
20
80
60-
Parasitol
Res
(2009)
105:1577-1587
1581
Table
4
Seasonal
occurrence
of
ectoparasites
on
dogs
Season
(number
of
dogs
examined)
Dogs
infested
with
different
parasites,
total
(%)
R.
sanguineus
S.
scabiei
var.
canis
C.
canis
C.
fells
P
irritans
Total
fleas
T
canis
Winter
(n=70)
0
6
(8.6)
45
(64.3)
3
(4.3)
7
(10.0)
45
(64.3)
3
(4.3)
Spring
(n=79)
27
(34.2)
1
(1.3)
60
(75.9)
2
(2.5)
8
(10.1)
60
(75.9)
1
(1.3)
Summer
(n=32)
16
(50)
1
(3.1)
32
(100)
4
(12.5)
0
32
(100)
8
(25.0)
R.
sanguineus,
a
three-host
tick
with
endophilous
behavior,
is
a
typical
representative
of
the
ixodid
tick
fauna
of
the
Mediterranean
basin
area.
This
species,
as
well
as
the
exophilous,
a
more
cold-tolerant
but
desiccation-vulnerable
I.
ricinus,
have
been
recorded
on
dogs
and
ungulates
in
several
countries
of
the
southern
Balkan
peninsula
apart
from
Albania:
Greece
(Enigk
1947;
Papadopoulos
et
al.
1996;
Jensen
2003;
Papazahariadou
et
al.
2003;
Pavlidou
et
al.
2008),
the
former
Yugoslav
Macedonia
(Schulze
1918;
Oswald
1938;
Angelovskii
1957),
Kosovo
(Mekuli
1959;
Heneberg
et
al.
1968;
Milutinovio
et
al.
1997;
Fournier
et
al.
2003),
Montenegro
(Petrovih
and
Borhogki
1955;
Tomagevih
1962),
Serbia
(Kulisic
et
al.
2000;
Milutinovio
and
Radulovio
2002;
Pavlovio
et
al.
2002),
Bosnia
and
Herzegovina
(Omeragio
et
al.
2003;
Omeragio
2008),
and
littoral
Croatia
(Cvetanovio
1956;
Mika66
1965;
Tovornik
and
Vesenjak-Hirjan
1988,
1989).
These
ticks
can
feed
on
a
wide
range
of
hosts;
however,
all
stages
of
R.
sanguineus
are
primarily
associated
with
dogs
(Dantas-Torres
2008).
Cases
of
human
parasitism
by
R.
sanguineus
and
I.
ricinus
have
been
reported
from
southeastern
Europe
too,
i.e.,
from
Bosnia
and
Herzegovina,
Kosovo,
and
Greece
(Fournier
et
al.
2003;
Omeragio
2008;
Chaligiannis
et
al.
2009).
Both
R.
sanguineus
and
I.
ricinus
have
been
implicated
as
vectors
for
a
range
of
pathogens
in
Europe
with
some
of
them
causing
zoonoses
with
the
potential
to
cause
considerable
public
health
problems
(Estrada-Peria
and
Jongejan
1999;
Shaw
et
al.
2001;
Parola
2004;
Parola
et
al.
2005;
Brouqui
et
al.
2007;
Rovery
et
al.
2008).
The
presence
of
several
of
those
tick-borne
disease
agents
in
Albania
has
been
proven
through
serological
surveys
or
direct
detection
of
the
antigens
in
hosts
or
ticks,
e.g.,
tick-borne
encephalitis
and
Mediterranean
spotted
fever
(Bardog
et
al.
1959;
Gina
et
al.
1986;
Eltari
et
al.
1993;
Berxholi
et
al.
1995;
Christova
et
al.
2003),
granulocytic
anaplasmosis,
canine
monocytic
ehrli-
chiosis,
babesiosis,
and
hepatozoonosis
(Christova
et
al.
2003;
Petrovec
et
al.
2003;
Dhamo
et
al.
2006;
Hamel
et
al.
2008;
Lazri
et
al.
2008).
The
tick
numbers
observed
on
the
dogs
from
Tirana
were
consistent
with
the
R.
sanguineus
counts
reported
from
Greece,
including
the
reporting
of
rare
cases
of
infestation
with
several
hundreds
of
ticks
(Papadopoulos
et
al.
1996;
Papazahariadou
et
al.
2003).
Although
our
sampling
allows
only
limited
conclusions
as
to
the
seasonality
of
tick
infestation,
comparable
to
observations
in
previous
studies
from
Albania
(Luli
1963;
Gina
1973),
littoral
Croatia
(Cvetanovio
1956;
Mika6i6
1965),
Bosnia
and
Herzegovina
(Omeragio
2008),
and
Greece
(Papadopoulos
et
al.
1996;
Pavlidou
et
al.
2008),
R.
sanguineus
was
present
in
spring
and
summer
with
increasing
prevalence
and
absent
in
winter
when
I.
ricinus
was
seen.
A
similar
seasonal
pattern
of
the
two
species
of
ticks
has
been
reported
from
central
Italy
(Stella
et
al.
1988;
Principato
et
al.
1989).
Not
surprisingly,
no
ticks
were
found
on
the
cats
which
originated
from
the
same
area
as
the
dogs
but
were
examined
in
November.
In
general,
the
domestic
cat
belongs
to
the
range
of
hosts
which
is
rarely
parasitized
Winter
Spring
Summer
Winter
Spring
Summer
Rhipicephalus
sanguineus
Total
Fleas
4
Z
Springer
1582
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Res
(2009)
105:1577-1587
Table
5
Infestation
intensity
of
Rhipicephalus
sanguineus
and
fleas
on
dogs
in
relation
to
season
Season
(number
of
dogs
examined)
Prevalence
of
infestation
level
according
to
Marchiondo
et
al.
(2007),
total
(%)
Rhipicephalus
sanguineus
Fleas
0
Low
Moderate
High
0
Low
Moderate
High
(1-3)
(4-10)
(>10)
(1-5)
(6-20)
(>20)
Winter
(n=70)
70
(100)
0 0
0
25
(35.7)
23
(32.9)
16
(22.9)
6
(8.6)
Spring
(n=79)
52
(65.8)
19
(24.0)
7
(8.9)
1
(1.3)
19
(24.1)
35
(44.3)
22
(27.8)
3
(3.8)
Summer
(n=32)
16
(50)
10
(31.3)
0
6
(18.7)
0 0
13
(40.6)
19
(59.4)
by
R.
sanguineus,
especially
in
the
presence
of
dogs
(Dantas-Torres
2008).
However,
cases
of
parasitism
have
been
recorded
in
Italy
(Sobrero
and
Manilla
1988;
Manfredi
et
al.
1999).
To
the
best
of
our
knowledge,
there
is
no
specific
data
regarding
infestation
of
cats
with
ticks
from
the
Balkan
countries.
In
western
Europe
and
Hungary,
however,
cats
were
reported
parasitized
by
I.
ricinus
(predominating
species),
Ixodes
hexagonus,
and
Ixodes
canisuga,
including
cases
of
R.
sanguineus
parasitism
of
cats
in
Spain
and
France
(Liebisch
et
al.
1985;
Supperer
and
Hinaidy
1986;
Comely
and
Schultz
1992;
Raschka
et
al.
1994;
Farkas
and
Foldvari
2001;
Larsen
et
al.
2001;
Losson
et
al.
2003;
Zenner
and
Drevon
2003;
Asensi
2007;
Nijhof
et
al.
2007).
In
contrast
to
the
infestation
with
ticks,
the
flea
fauna
of
domestic
animals
in
the
countries
of
southern
part
of
the
Balkan
peninsula
is
much
less
well
documented.
C.
canis
and
P.
irritans
were
observed
on
dogs
and
P.
irritans
on
goats
in
Albania
(RosickST
and
Gjini
1960).
An
earlier
paper
from
the
former
Yugoslavia
(Wagner
1939)
reported
the
frequent
occurrence
of
C.
canis
and
C.
felis
on
dogs
and
cats,
respectively,
and
also
mentioned
the
occasional
occurrence
of
C.
felis
on
dogs.
In
Bosnia
and
Herzegovina,
C.
canis
was
identified
on
dogs
and
C.
felis
on
cats
100
_c
3
fa
c
8
p c
id
.
5
c)
a)
c
ro
c
fq
80
60
5
40
N
03
7
X)
Cr
:o
cx
12
20
LL
Cc
0
0
1-3
4-10
>10
ticks
0
1-3
4-10
>10
ticks
0
1-3
4-10
>10
ticks
Winter
Spring
Summer
100
_c
§
80
0
a)
e
c
a1
0
g
60
40
CD
Cr
20
U_
0
0
1-5
6-20
>20
fleas
0
1-5
6-20
>20
fleas
0
1-5
6-20
>20
fleas
Winter
Spring
Summer
Fig.
2
Levels
of
infestation
with
Rhipicephalus
sanguineus
and
fleas
of
dogs
according
to
the
score
described
by
Marchiondo
et
al.
4?!
Springer
Parasitol
Res
(2009)
105:1577-1587
1583
Table
6
Abundance
of
Rhipicephalus
sanguineus
and
fleas
on
dogs
in
relation
to
season
Parasite
Season
Infestation
Significance
(ICruskal—Wallis
test;
p)
Prevalence
Range
Abundance
(geometric
mean)
Winter
0%
Oa
Rhipicephalus
sanguineus
Spring
34.2%
0-15
0.53b
<0.0001
Summer
50%
0-331
1.40b
Winter
64.3%
0-80
2.49a
Fleas
Spring
75.9%
0-37
2.70a
<0.0001
Summer
100%
8-62
21.28b
Values
with
different
letters
were
significantly
different
at
p<0.05
(Omeragio
et
al.
2003).
In
a
recent
study
from
western
Romania,
the
most
common
flea
in
both
dogs
and
cats
was
C.
fells,
followed
by
C.
canis
and
P.
irritans
(Morariu
et
al.
2006).
Examination
of
dogs
and
cats
in
Greece
revealed
the
presence
of
four
species
of
fleas:
C.
canis,
C.
felis,
P.
irritans,
and
Xenopsylla
cheopis
were
recorded
on
dogs
and
C.
felis
and
C.
canis
on
cats
(one
case
of
a
mixed
infestation;
Haralampides
1978;
Koutinas
et
al.
1995;
Christodoulopoulos
et
al.
2006).
Despite
being
not
as
prominent
as
in
the
dogs
from
Tirana,
C.
canis
was
more
prevalent
than
C.
felis
in
the
dogs
examined
in
Greece.
Although
still
not
well
understood,
our
findings
support
observations
from
several
regions
throughout
Europe
and
elsewhere
that
the
higher
frequency
of
C.
canis
is
usually
associated
with
inhabiting
rural
settings,
living
in
kennels,
or
being
kept
outdoors,
in
contrast
to
dogs
from
residential
habitats.
Thus,
the
prevalence
rate
may
be
less
dependent
upon
the
general climatic
conditions
than
upon
habitats
(Piotrowski
and
Polomska
1975;
Haarlem
and
Kristensen
1977;
Kristensen
et
al.
1978;
Muller
and
Kutschmann
1985;
Muller
1986;
Koutinas
et
al.
1995;
Rudziriska
and
Sulgostowska
1996;
Alcaino
et
al.
2002;
Durden
et
al.
2005;
Gracia
et
al.
2008).
While
X
cheopis
and
P.
irritans
were
collected
just
from
one
dog
each
by
Koutinas
et
al.
(1995),
the
latter
species
was
observed
more
frequently
than
C.
canis
by
Christodoulopoulos
et
al.
(2006)
who
examined
dogs
in
64
farms
in
central
and
southern
Greece
that
had
a
history
of
P.
irritans
infestation
in
their
goats
(Christodoulopoulos
and
Theodoropoulos
2003).
P.
irritans
has
the
potential
to
cause
severe
infestations
in
dogs
and
man
(Gracia
et
al.
2000;
Knoppe
et
al.
2003).
Although
occurring
in
small
numbers
only,
P.
irritans
was
the
second
most
prevalent
species
of
flea
on
the
dogs
from
Tirana
recovered
from
8.3%
of
all
dogs
examined
or
10.9%
of
the
flea-positive
dogs.
P.
irritans
infestation
was,
therefore,
higher
than
the
findings
reported
in
most
other
surveys
in
Europe
where
this
flea
was
recorded
(Haarlem
and
Kristensen
1977;
Kristensen
et
al.
1978;
Muller
and
Kutschmann
1985;
Muller
1986;
Hinaidy
1991;
Koutinas
et
al.
1995;
Beck
et
al.
2006;
Morariu
et
al.
2006;
Bond et
al.
2007;
Gracia
et
al.
2008)
apart
from
the
prevalences
reported
by
Baker
and
Hatch
(1972)
in
Ireland
(24%),
Piotrowski
and
Polomska
(1975)
in
Poland
(22%),
and
by
Christodoulopoulos
et
al.
(2006)
who
examined
dogs
in
farms
with
a
history
of
P.
irritans
infestation
in
their
goats
in
Greece
(40.7%).
The
mean
flea
burden
of
the
dogs
from
Tirana
was
comparable
to
the
flea
load
reported
in
a
study
from
Poland
(Piotrowski
and
Polomska
1975)
but
higher
than
the
densities
observed
in
surveys
of
dogs
in
Denmark,
Germany,
and
France
(Haarlem
and
Kristensen
1977;
Muller
and
Kutschmann
1985;
Bourdeau
and
Blumstein
1995;
Franc
et
al.
1998;
Beck
et
al.
2006;
Gilles
et
al.
2008a,
b).
Similar
to
other
studies
from
southern
regions
of
Europe
with
a
milder,
warmer
climate
(Koutinas
et
al.
1995;
Rinaldi
et
al.
2007;
Gracia
et
al.
2008),
our
data
from
Albania
indicate
flea
infestations
of
dogs
occurring
year
Table
7
Fleas
recovered
from
the
dogs
(n=149)
and
cats
(n=26)
during
winter
plus
spring
or
autumn,
respectively
Total
number
of
fleas
collected
(male,
female)
Percentage
of
total
Sex
ratio:
male/female
Dogs
C.
canis
859
(199,
660)
97.6
1/3.32
C.
fells
5
(2,
3)
0.6
1/1.50
P.
irritans
16
(7,
9)
1.8
1/1.29
Cats
C.
fells
76
(26,
50)
100
1/1.92
4Z
Springer
1584
Parasitol
Res
(2009)
105:1577-1587
round.
However,
as
observed
more
distinctly
in
European
regions
with
temperate
climates
(Piotrowski
and
Polomska
1975;
Rudziriska
and
Sulgostowska
1996;
Beck
et
al.
2006),
phenology
of
prevalence
and
intensity
of
flea
infestation
seem
to
be
correlated
to
the
seasonality
of
environmental
conditions.
Consistent
with
all
prior
reports
of
feline
pulicosis,
the
species
of
flea
most
abundant
by
far
throughout
Europe
irrespective
of
the
history
of
the
cats
or
environmental
conditions
was
the
cat
flea,
C.
felis,
while
the
other
species
observed
(i.e.,
Archaepsylla
erinacei,
Ceratophyllus
gallinae,
Ceratophyllus
garei,
C.
canis,
Ctenophthalmus
assimilis,
Hystrichopsylla
talpae,
Monopsyllus
sciurorum,
Nosopsyllus
fasciatus,
P.
irritans,
Spilopsyllus
cuniculi,
Typhloceras
poppei,
and
X
cheopis)
were
recorded
much
less
frequently
(Niak
1972;
Beresford-Jones
1974, 1981;
Haarlem
and
Kristensen
1977;
Haralampides
1978;
Kristensen
et
al.
1978;
Liebisch
et
al.
1985;
Kral
1986;
Supperer
and
Hinaidy
1986;
Zarzere
1988;
Canestri
Trotti
et
al.
1990;
Hinaidy
1991;
Kalvelage
and
Munster
1991;
Raschka
et
al.
1994;
Bourdeau
and
Blumstein
1995;
Chesney
1995;
Koutinas
et
al.
1995;
Wall
et
al.
1997;
Clark
1999;
Cadiergues
et
al.
2000;
Visser
et
al.
2001;
Beck
et
al.
2006;
Morariu
et
al.
2006;
Asensi
2007;
Bond
et
al.
2007;
Gilles
et
al.
2008a,
b).
The
mean
flea
burden
of
the
cats
from
Tirana
was
comparable
to
the
mean
flea
load
reported
in
recent
surveys
of
cats
in
France
and
Germany
(Cadiergues
et
al.
2000;
Beck
et
al.
2006;
Gilles
et
al.
2008a,
b).
The
female-biased
sex
ratio
in
the
flea
species
parasitizing
dogs
and
cats
observed
in
this
study
is
a
common
feature
which
has
been
observed
in
numerous
other
surveys
(e.g.,
Piotrowski
and
Polomska
1975;
Muller
1986;
Hinaidy
1991;
Bourdeau
and
Blumstein
1995;
Chesney
1995;
Rudziriska
and
Sulgostowska
1996;
Franc
et
al.
1998;
Alcaino
et
al.
2002;
Durden
et
al.
2005;
Rinaldi
et
al.
2007).
While
both
ticks
and
fleas
on
dogs
and
cats
received
significant
attention
for
several
reasons
in
the
recent
years,
much
less
is
known
about
the
prevalence
of
other
canine
and
feline
ectoparasites
in
general.
Based
on
a
review
of
the
available
data
on
the
epidemiology
of
ectoparasites
of
dogs
and
cats
in
Europe,
it
was
concluded
that
the
countries
"of
the
Balkan
peninsula
are
the
most
poorly
covered"
(Piotrowski
1979).
Apart
from
the
studies
on
ticks
and
fleas
mentioned
before,
only
a
few
other
papers
reporting
about
other
ectoparasitic
infestations
of
dogs
and
cats
in
Greece,
Bosnia
and
Herzegovina,
Croatia,
Slovenia,
and
Romania
have
been
published
(e.g.,
Haralampides
1978;
Sabolio
1997;
Sotiraki
et
al.
2001;
Omeragio
et
al.
2003;
Dara
-
bu
2003;
Rataj
et
al.
2004),
which
emphasizes
the
need
for
more
surveys
in
order
to
address
this
lack
of
basic
epidemiological
information.
Documentation
of
parasite
fauna
through
survey
and
inventory
is
the
first
step
in
defining
the
relationship
of
endemic
parasites
and
their
potential
and
real
impact
on
domestic
animals
and
humans.
The
present
results,
including
the
implications
of
transmission
of
pathogens
by
ticks
and
fleas,
suggest
that
further
studies
should
be
conducted
in
Albania,
especially
to
estimate
the
potential
risk
of
relevant
arthropod
borne
diseases.
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