Ectoparasites of rodents in Suez governorate with special reference to fleas


Morsy, T.A.; Fayad, M.E.; Abou Shady, M.K.; Yousef, N.S.

Journal of the Egyptian Society of Parasitology 16(2): 457-468

1986


Rodents have been investigated for their possible ectoparasites in Suez governorate. They were prevalent the whole years particulaI'ly in Spring. Five species of rodents were identified : M. musculus, R. rattus, R. norvegicu.s, A. cahirinus and S. calurus. The ectoparasites were fleas (X. cheopis, P. irritans, C. felis, C. segnis and E. galUna.cca), lice (P. spinulosa) and ticks (R. sanguineus and Ilyalomma spp.). X. cheopis was the commonest flea. The role played by rodents and their arthropcdectoparasites in transmission of human and animal diseases wa-, discussed. It was concluded that rodents are the most dangerous animal reservoir for human and animal diseases.

Journal
of
the
Egyptian
Society
of
Parasitology,
vol.
16
no.
2,
1986.
ECTOPARASITES
OF
RODENTS
IN
SUEZ
GOVERNORATE
WITH
SPECIAL
REFERENCE
TO
FLEAS
By
TOSSON
A.
MORSY,
MOHAMED
E.
FAYAD,
,6,,BDEL
MAKSOUD
K.A.aBOU
SHADY
and
NEHAL
S.%.
YOUSEF
Department
of
Parasitology,
Faculty
of
Medicine
and
Ain
Shams
Research
and
Training
Center('
on
Veto
of
Diseases,
Ain
Slums
University,
Abbassia,
Cairo,
Egypt.
ABSTRACT
Rodents
have
been
investigated
for
their
possible
ectopara-
sites
in
Suez
governorate.
They
were
prevalent
the
whole
years
particularly
in
Spring.
Five
species
of
rodents
were
identified
:
M.
musculus,
R.
rattus,
R.
norvegicus,
A.
cahirinus
and
S.
calurus.
The
ectoparasites
were
fleas
(X.
cheopis,
P.
irritans,
C.
felis,
C.
segnis
and
E.
gallinacca),
lice
(P.
spinulosa)
and
ticks
(R.
sanguineus
and
Ilyalomma
spp.).
X.
cheopis
was
the
com-
monest
flea.
The
role
played
by
rodents
and
their
arthropod-
ectoparasites
in
transmission
of
human
and
animal
diseases
was.;
discussed.
It
was
concluded
that
rodents
are
the
most
dangerous
animal
reservoir
for
human
and
animal
diseases.
INTRODUCTION
Rodents
have
a
time
honoured
public
health
place
in
the
history
of
science.
In
addition
to
being
destructive
pests
they
Abstract
presented
in
the
sixth
International
Congress
of
Parasitology,
(ICOPA
VI)
Brisbane,
August
24-29,
1981,
Australia.
457
have
been
to
serve
as
either
carriers
or
reservoirs
for
a
number
of
zoonotic
human
and
animal
diseases
(Morsy
et
al,
1982)..
They
also
continued
to
hold
their
permanent
position
as
animals
for
use
in
the
laboratory
investigations
due
to
a
number
of
factors
such
as
their
low
cost,
small
space
required,
short
time-
span
of
generation
and
the
fact
that
they
can
be
easily
handlet
and
obtained.
Compared
with
the
wealth
of
new
knowledge.
added
within
the
last
few
decades
about
the
taxonomy
and
crea-
tions
of
various
rodents
(Massif,
19
44
et
seq)
little
that
is-
exact,
has
been
added
about
their
related
ectoparasite
vectors
in
Egypt.
Hence,
it
was
mainly
for
this
reason
that
the
authors
studied
the
ectoparasites
of
rodents
in
Suez
governorate.
MATERIAL
AND
METHODS
Area
of
the
study
:
Suez
governorate
has
a
unique
position
as
a
civilized
urban
centre,
which
thrived
very
long
before
Christ
and
has
been
always
acknowledged
by
many
historians.
This
is
owing
to
its
distinguished
situation
on
the
isthmus
carrying
its
name.
Suez
has
been
an
important
port
of
sale
for
merchant
ships,
a
haven
for
pilgrims
and
an
age-long
crossing
point
for
human
movements.
During
the
Pharaonic
and
Ptolemic
eras,
the
city
retained
its
importance
especially
after
the
digging
of
the
canal
which
joined
the
Red
Sea
with
the
River
Nile.
The
isthmus
of
Suez,
low,
sandy
and
scentily
vegetated
neck
of
land
connecting
the
Nile
Valley
with
Sinai,
contains
Lake
Timsah
and
great
and
little
bitter
lakes
which
are
connected
and
traversed
by
the
Suez
Canal.
Trapping
and
examination
of
rodents
:
rodents
were
trap-
ped
alive
from
different
areas.
For
seasonal
activity,
rodents
were
collected
from
2
fixed
stations
:
(a)
the
custom
area
and
(b)
Hai
El
Arbeen.
In
each
time
about
fifty
wire
box
traps
were
distributed
in
the
evening
just
before
sunset
both
indoor
and
outdoor
and
collected
the
early
morning.
The
process
of
collec-
-
458
Lion
v,.•as
carried
out
once
a
month
over
61
,
2
year
1935.
Every
trap
was
enclosed
in
separate
white
bag
to
avoid
exchange
of
.ectoparasites.
Dead
rodents
were
considered
only
for
the
rodent
density
when
calculating
the
flea
index.
Living
rodents
were
anaesthetized
with
ether
and
identified
by
species
_and
sex.
The
.arthropod-ectoparasites
were
carefully
collected.
The
method
was
essentially
the
same
as
described
by
Morsy
et
.
al
(1982:).
For
the
identification
of
rodents
the
keys
given
by
Osborn
and
Helmy
(1980)
and
Morsy
et
al
(1981)
were
followed.
For
the
identification
of
arthropod-ecteparasites;
the
keys
given
by
Soulsby
(1978),
Imins
(1934)
and
Hoogstraal
(1956,
65)
were
RESULTS
The
collected
rodents
were
identified
as
:
(1)
Mus
musculus
praetextus
(2)
Rattus
rattus
(3)
Rattus
norvegicus
(4)
Acomys
cahirinus
and
Sekeetamys
calurus.
The
collected
arthropod-ectoparasites
of
rodents
were
iden-
tified
as
:
(1)
Xenopsylla
cheopis,
(2)
Pulex
irritans,
(3)
Echid-
nophaga
gallinacca,
(4)
Ctenocephalides
fells,
(5)
Ctenopsyllus
segnis,
(6)
Polyplax
spinulosa,
(7)!
Rhipicephalus
sanguineus
and
(8)
Hyalomma
spp
The
results
are
shown
in
table
(1,
2,
3,
4
&
5).
DISCUSSION
In
the
present
study,
the
collections
of
rodents
yielded
676
rats
belonging
to
five
types.
These
were
:
Mus
musculus
(169),
Rattus
rattus
(229),
Rattus
nr4rvegicus
(240),
Acomys
CCatilinUS
(34)
and
Sekcctcniys
calunts
(4).
On
the
other
hand,
80.5%
of
the
collected
rodents
from
the
custom
area
(El.
Gomrok)
and
19.5%
were
from
Hai
El
Arbeen
(down
town).
Rifaat
et
al
(1981)
in
Port
Said
governorate,
reported
that
about
SO%
of
their
rodents
wel:c
caught
clowa
town..
But,
Ivlorsy
et
al
(1931)
in
Alexandria
governorate,
men-
-
459
tioned
that
75%
of
the
rodents
they
collected
were
from
the-
custom
area
(El
Gomi
ok).
So,
it
may
be
concluded
that
nie
increase
in
the
rodent
populations
in
some
Egyptian
gover-
norates
may
be
due
to
the
continuous
invasions
of
the
ports•
from
abroad.
Also.
in
Poland
(Wegner
and
Pizyborowski.
1959)
and
in
Korea
(Attn
and
Soh,
1973)
the
increase
in
the
rodent
population
was
attributed
to
the
outer
invasion
from
abroad.
Table
1
:
The
seasonal
activity
and
flea
index
in
the
custom
area
and
Hai
El
Arbo.en
during
the
year
198b.
The
custom
area
Hai
El
Arbeen
Month
Rat
No.
Flea
No.
Flea
index
Rat
No.
Flea
No.
Flea
January
23
6
0.26
14
3
0.21
February
49
13
0.26
18
5
0.27
March
60
55
0.91
17
4
0.23
April
88
100
1.13
22
20
0.90
May
115
102
0.88
23
19
0.82
June
69
59
0.85
11
7
GM
July
44
34
0.77
8
4
0.50
August
24
17
0.70
4
1
0.25
September
25
20
0.80
4
3
0.75
October
24
12
0.85
3
2
0.66
Ncvember
25
16
0.64
5
3
0.60
December
8
3
0.37
3
2
0.66
Total
544
437
0.80
132
73
0
55
Table
2
:
The
total
number
of
ectoparasites
collected
on
rodents
Ectoparasite
No.
infested
rat
infestation
per
cent
Fleas
510
482/676
71.3%
Lice
30
11/676
1.62%
Ticks
41
39/676
5.76%
460
Table
3
:
The
flea
index
in
the
custom
area
(El
Gomrok)
,Season
Rat
No,
No.
infested
Flea
No.
Flea
index
Spring
272
245
261
0.95
Summer
93
64
71
0.76
Autumn
47
30
31
0.65
Winter
132
67
74
0.56
Total
544
406
437
0.80
Table
4
:
The
flea
index
in
Hai
El
Arbeen
(down
town)
Season
Rat
No.
No.
infested
Flea
No.
Flea
index
Spring
56
42
46
0.82
Summer
16
8
4
0.50
Autumn
11
7
7
0.63
Winter
49
19
12
0.24
Total
132
76
73
0.55
Table
5
:
The
flea
index
of
the
different
species
of
fleas
Flea
Flea
No.
Prevalence
Flea
index
X.
cheopis
399
78.2%
0.59
P.
irritans
26
5.09%
0.04
E.
gallinacea
21
4.11%
0.03
C.
felis
60
11.7%
0.08
C.
segnis
4
0.78%
0,01
On
the
other
hand,
the
most
common
rat
was
Betas
nor-
vegicus
(35.5%).
This
was
followed
by
Eattus
rattus
(33.9%),
Mus
muscu/us
(25%)
and
Aecnnys
caltirinus
(5%).
The
lowest
number
of
collected
rats
was
0.61%
for
Sekeetamys
calurus.
The
461
first
four
rodents
are
considered
(Morsy
et
al,
81
&
8;)
as
com-
mensal
ones.
The
last
one,
Sekeetamys
is
a
wild
rodent
(Osborn
and
Helmy,
1980).
So,
the
commonest
rodent
was
liatM,y
nor-
vegicus.
This
may
be
ascribed
due
to
the
invasion
from
abroad
through
the
ports,
and
to
its
aggressive
nature
as
it
attains-
its
predominance
by
the
elimination
of
other
commensal
species.
This
phenomenon
was
not
only
found
in
Suez
governorate
but.
also
in
Port
Said
(Rifaat
et
al,
1981),
in
Alexandria
(Morsy
et
al,
1984),
in
Poland,
(Wegner
and
Pizyborowski
1959),
and
in
Korea
(Attn
and
Soli,
1973).
In
Ismailia
governorate,
the
commonest
rat
was
1?.
norvegicus
(73,7%)
followed
by
R.
rattus
(25.9%)
and
M.
musculus.
Similarly,
the
pre-dominance
of
R.
norvegicus
in
the
coastal
zones
of
Egypt
and
its
invasion
to
the
adjoining
areas
were
reported
by
Rifaat
et
al
(1981),
Mandi
et
al
(1971)
and
Morsy
et
al
(1980,
82),
However,
one
cannot
neglect
that
the
environmental
conditions
prevailing
in
any
area
as
the
abundance
of
garbage,
poor
sanitary
conditions...
etc
are
comparatively
more
favourable
for
the
flourishing
of
rodents.
Regarding
other
species,
1?.
rattus
was
common
in
Hai
El
Arbeen
than
in
the
custom
area
(150
&
77
respectively).
This
species
is
more
common
in
the
Nile
Valley
particularly
the
Delta
and
in
the
coastal
towns
(Wassif
1944,
Rifaat
et
al
1981,
and
Morsy
et
al
1980.
81,
82).
This
species
lives
in
urban
as
well
as
rural
areas
and
feeds
mainly
on
seeds,
vegetables
and
the
likes
(Morsy
et
al,
1980).
The
former
species
R.
norvegicus
feeds
o
protein
diet
rich
in
fats
as
meat,
fish
and
even
small
rodents
-
and
birds.
Mita
musculus
is
more
or
less
distributed
all
over
Egypt.
It
is
more
or
less
a
typical
indoor
rodent
(Mandi
et
al
1971).
Acomys
cahirinus
although
considered
as
commensal
rodent,
yet
it
is
not
widely
distributed
as
the
other
species
of
rodents.
It
has
been
recorded
in
the
Nile
Valley
and
Suez
Canal
zone
(Mandi
et
al,
1971)
and
rarely
in
Alexandria
(Morsy
et
al,
1984).
Recently,
this
species
was
recorded
in
North
Sinai
(Shoukry
et
al,
1986).
Sekeetamys
caturus
is
more
or
less
a
wild
rat.
In
the
present
study,
it
was
caught
in
the
periphery
of
Hai
El
Arbeen.
This
district
is
under
reconstruction.
Perhaps
462
this
rat
was
brought
with
the
materials
used
for
construction
.as
it
is
known
to
live
in
the
desert
area
of
Suez
governorate
(Osborn
and
Helmy,
1980).
Rodents
were
prevalent
the
whole
year
in
both
the
custom
.area
and
Hai
El
Arbeen.
However
the
trap
index
was
0.91
in
the
custom
area
and
0.22
in
Hai
El
Arbeen.
This
trap
index
was
more
or
less
low
when
compared
with
other
areas
in
Suez
Canal
Zone.
It
was
1.5
in
the
custom
area
and
2,5
down
town
in
Port
Said
(Rifa
at
et
al,
1981)
and
about
one
in
some
areas
in
Ismailia
(Morsy
et
al,
1982).
In
the
custom
area
of
Suez,
the
trap
index
ranged
between
2.3
in
May
to
0.1
in
December.
In
Hai
El
Arbeen,
the
trap
index
ranged
between
0.4
in
May
to
0.06
in
December.
On
the
other
hand,
rodents
were
most
pre-
valent
in
Spring.
The
least
number
of
rodent
was
collected
in
Autumn.
This
low
trap
index
in
Suez
governorate
may
be
at-
tributed
to
the
human
population
density
and
the
regular
con-
trol
measures
carried
out
by
the
Public
Health
Authorities
in
Suez
governorate.
The
fact
that
Suez
is
the
main
port
for
pil-
grims
and
oil
products
may
also
account
for
this
low
rodent's
prevalence.
Regarding
ectoparasites,
not
all
the
collected
rodents
were
infested.
In
the
custom
area,
406
out,
of
544
rodents
(74.6%)
were
infested.
In
Hai
El
Arbeen,
76
out
of
132
rodents
(55.3%)
were
infested.
In
Port
Said
city,
the
percentage
of
infested
rodents
was
79.2%
and
in
the
custom
area
57.9%
(Rifaat
et
al,
19
5
31).
While
in
Ismailia
governorate,
the
percentage
of
infested
rodents
was
32.3%
(Morsy
et
al,
1982).
This
may
be
attributed
to
the
fact
that
both
Port
Said
and
Suez
are
among
the
impor-
tant
Egyptian
ports.
In
the
present
study,
three
groups
of
arthropod-ectopara
-
sites
were
identified
on
the
collected
rodents.
These
were
fleas,
biting
lice
and
ticks.
The
commonest
ectoparasites
were
fleas,
which
represented
90.6%
of
the
detected
ectoparasites,
lice
-
represented
2.1%
and
ticks
represented
7.3%.
Regarding
fleas,
five
species
(Xenopsylla,
Pulex,
Ctenoce-
-
463
phalidcs,
Ctenopsyllus
and
Echidnophaga)
were
detected.
These.
fleas
are
respectively
ectoparasites
of
rat,
man,
cat,
mouse
and
pouitry.
Each
flea
has
its
preferred
host
or
related
group
of
hosts.
However,
the
host-parasite
relationship
by
its
true
mean-
ing
is
not
absolute
and
fleas
pass
from
one
host
to
another
(Morsy
et
al,
1982).
Most
rat
fleas
for
examples
feed
on
several
kinds
of
animals
and
even
man
(Rumreich
and
Wynn,
1945).
In
Dakahlia
governorate,
El
Kholy
(1971)
identified
Xenopsylla,_
Bu.lex,
Echidnophaga,
Ctcnocephallus,
(=
Ctenocephalides)
and
Leptopsylla
(=
Ctenopsylla)
as
ectoparasites
on
R.
norvcgicus,.
R.
rattus,
M,
musculus
and
A.
chirinus.
Rifaat
et
al
(1981)
in
Port
Said
governorate,
and
Morsy
et
al
(1982)
in
Ismailia
gover-
norate,
identified
Xenopsylla,
Pulex
and
Ctcnocephat!ides
and
Ctenopsyllus
as
ectoparasites
of
rodents.
No
doubt,
the
absence
of
host
parasite
relationship
in
group
of
fleas
has
its
epidemio-
logical
importance
in
the
transmission
of
plague
and
murine
typhus
fever
as
well
as
other
bacterial,
viral
and
parasitic
diseases.
The
most
common
species
of
fleas
were
Xenopsylla
cheopis
(78.2%)
followed
by
Ctenoccphalides
felis
(11
8%
),
Pu!ex
irritans
(5.1%),
Echidnophaga
gallinacca
(4.1%)
and
lastly
Ctenopsyllus
segnis
(0.8%).
In
all
works
done
by
Mandi
et
al
(1971),
El
Kholy
(1971),
Rifaat
et
al
(1981)
and
Morsy
et
al
(1980,
81,
82)
the
commonest
ectoparasites
of
rodents
wag
Xenopsylla
cheopis.
The
rat
louse
(Polyplax
spinulosa)
was
detected
on
R.
norvcgicus
(4).
and
M.
musculus
(7).
This
species
was
identified
as
an
ectoparasite
of
commensal
rodents
in
Dakhalia
gover-
norate
(El
Kholy,
1971)
and
Ismailia
governorate
(Morsy
et
al,
1982).
Polyplax
spinulosa
may
transmit
rickettsiae
of
murine
typhus
(:Moser
et
al,
1931)
or
plague
and
tularemia
(Faust
et
al,
1978)
from
rat
to
rat.
But,
it
is
not
known
to
feed
on
man
(Soulsby,
-1978).
The
hard
ticks,
R.
sanguineus
and
Hyalomma
species
were
detected
mainly
on
Sekectamys,
Acomys
and
Ilattus
rattus,
R.
sanguineus
is
mainly
a
dog
tick,
but
it
has
been
recorded
on
rodents
by
many
authors
(Strivastara
and
Varma,
1964,
El
Kholy,
1971,
Rifaat
et
al,
1981
and
Morsy
et
al,
1982).
This:
464
species
of
tick
has
been
found
infected
with
the
Rickettsia
of
Rocky
Mountain
spotted
fever
in
North
and
South
America,
with
R.
conori
the
causal
agent
of
boutonneuse
or
Marseilles
fever,
South
African
tick
bite
fever
and
Indian
tick
typhus
(Manson-Bahr
and
Apted,
1982).
On
the
other
hand,
Ilyaloinma
species
is
the
vector
of
viral
haemorrhagic
fever
(Hoogstraal,
1956).
In
addition
to
diseases
transmission,
the
saliva
secre-
tions
of
certain
ticks,
when
introduced
into
human
skin
at
the
time
the
tick
takes
a
blood
meal
produce
systemic
toxaemia
(tick
paralysis).
Also
the
penetration
of
their
mouth
parts
into
the
skin
of
man,
produces
appreciable
pain
and
traumatic
injury
and
providing
opportunity
for
pyogenic
organisms
to
enter
human
body
(Faust
et
al,
1978).
In
the
studies
carried
out
by
El
Kholy
(1971),
Rifaat
et
al
(1981)
and
Morsy
et
al
(1982)
mites
were
detected
on
rodents.
But
in
the
present
study,
no
mites
were
detected
among
the
examined
rodents.
The
flea
indices
varied
in
the
different
months
in
both
the
custom
area
and
Hai
El
Arbeen.
In
the
custom
area,
the
highest
flea
index
was
reached
in
April
(1.13)
and
the
lowest
was
reached
in
January
and
February
(0.26).
In
Hai
El
Arbeen,
the
highest
flea
index
was
in
April
(0.90)
and
the
lowest
was
in
January
(0.21).
The
overall
flea
indices
were
0.80
in
the
custom
area
and
0.55
in
Hai
El
Arbeen.
Seasonally,
the
highest
flea
indices
were
in
Spring
(0.95
and
0.82)
in
both
the
custom
area
and
Hai
El
Arbeen.
The
lowest
flea
indices
were
in
Winter
(0.56
and
0.24)
in
both
areas.
Rifaat
et
al
(1981)
in
Port
Said,
found
the
highest
flea
indices
down
town
in
Autumn
and
the
lowest
in
Winter.
El
Kholy
(1971)
and
Morsy
et
al
(1982)
found
that
the
highest
flea
indices
were
recorded
in
Spring
and
the
lowest
in
Winter.
Again,
Rifaat
et
al
(1981)
added
that
there
was
no
statistical
difference
between
the
flea
indices
in
Autumn
and
Spring.
Cavanough
et
al
(1968)
in
Vietnam,
recorded
an
ap-
proximately
small
flea
index
during
the
wet
season
which
,
showed
a
great
increase
during
the
warm
season.
Stark
and
Miles
(1962)
attributed
the
seasonal
flea
index
to
their
life
cycle.
Amin
(1966)
reported
that
the
incidence
of
fleas
was
related
to
the
climatic
condition
and
it
was
less
affected
with'
the
size
of
the
rodent
host.
465
--
It
is
concluded
that
the
role
played
by
rodents
as
carriers
.or
reservoirs
of
diseases
is
far
from
negligible
particularly
in
tropical
and
subtropical
countries.
Besides,
one
should
not
ascrib
or
deny
pathogenic
properties
to
the
arthropods
found
on
hosts
other
than
man.
ACKNOWLEDGEMENT
This
study
was
partially
supported
by
Contract
'MIA
.'
=6V/NIH-NIAID/USAID.
Sincere
thanks
are
due
to
the
Public
Health
Authorities
of
Suez
Governorate
for
their
help
to
make
the
field
work
possible.
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4133