Rodents as reservoir of zoonotic intestinal helminths in Suez Canal Zone with the possible immunological changes


el Gindy, M.S.; Morsy, T.A.; Bebars, M.A.; Sarwat, M.A.; Arafa, M.A.; Salama, M.M.

Journal of the Egyptian Society of Parasitology 17(1): 259-273

1987


1320 rodents captured in Port Said, Ismailia and Suez Governorates, Egypt, were examined for helminths: Echinostoma callawayensis and Schistosoma mansoni (eggs in the liver) were each found in one Arvicanthis niloticus from Ismailia. Taenia taeniaeformis metacestodes were found in A. niloticus, Rattus rattus, R. norvegicus and Acomys cahirinus; Andrya neotomae, Hymenolepis nana and H. diminuta were also found. The nematodes were Syphacia obvelata (in R. rattus, R. norvegicus) and S. muris (in R. rattus only), Aspiculuris tetraptera (in Arvicanthis niloticus and R. norvegicus) and Protospirura muricola (in R. rattus, R. norvegicus and A. niloticus). The acanthocephalan Moniliformis moniliformis was also found. The role of rodents as reservoirs of zoonotic intestinal helminths is discussed. IgE, IgM and IgA levels were generally raised above normal in infected rodents.

Journal
of
the
Egyptian
Society
of
Parasitology,
vol.
17
No.
1,
1987.
_
RODENTS
AS
RESERVOIR
OF
ZO
'
ONOTIC
INTESTINAL
.
HELMINTIIS
IN
SUEZ
CANAL
ZONE
WITH
THE
POSSIBLE
IMMUNOLOGICAL
CHANGES
By
MOHAMED
S.
EL
GINDY,
TOSSON
A.
MORSY,
MOHAMED
A.
BEBARS,
MOHAMED
A.
SARWAT,
MAGDY
A.S.
ARAFA
and
MAGDY
M.I.
SALAMA
Departments
of
Parasitology;
Faculty
of
Medicine,
Ain
Shams
University,
Abbassia,
Cairo
ABSTRACT
Rodent
populations
have
bden
investigated
in
the
Suez
.
Canal
Zone
for
their
types
and
helminthic
endoparasites.
Eleven
worms
belonging
to
Trematoda
(2),
Cestoda
(4),
Nematoda
(4)
and
Acanthocephala
(1)
were
identified.
The
commonest
worm
was
Hymenolepis
diminuta,
followed
by
Aspiculuris
tetraptera
and
Andrya
neotomae.
The
least
prevalent
worm
was
Echinos-
toma
callawayensis.
Of
interest
was
the
detection
of
Schista-
soma
mansoni
eggs
in
the
liver.
The
zoonotic
importance
of
these
worms
was
discussed.
Immunoglobulins
levels
were
found
increased
than
the
value
of
the
reference
serum.
INTRODUCTION
In
the
last
few
years,
rodent
populations
markedly
increas-
ed
in
many
Egyptian
governorates,
particularly
in
Suez
Canal.
Zone
(Morsy
et
al,
1981,
82,
86
and
Shoukry
et
al,
1986).
Pre-
vious
works
have
shown
that
they
act
as
reservoir
hosts
for
many
parasitic
diseases
as
H.
diminuta,
T.
spiralis,
L.
major
259
and
E.
histolytica
(Morsy
et
al,
1981,
82
&
84),
bacterial
diseases
as
plague,
fungus
as
histoplasmosis,
rickettsial
as
murine
typhms
and
spirochetes
as
endemic
relapsing
(Abdon
and
Samaan,
1962).
The
aim
of
this
work
was
to
study
thd
species
of
rodents
and
their
role
as
reservoirs
of
zoonotic
intestinal
helminths.
MATERIAL
AND
METHODS
Altogether
1320
rodents
have
been
collected
from
Port
Said,
Ismailia
and
Suez
Governorates.
For
details
please
refer
to
Morsyi
et
al.
(1981,
82).
The
rodents
were
narcotised
with
chloroform
or
ether
fol-
lowed
by
the
identification
by
sex
and
species.
They
werd
then
dissected,
the
abdominal
and
pleural
cavities
were
examined.
for
any
helminth
parasites
and
the
organs
of
internal
viscera
were
isolated
in
separate
petri-dishes
to
be
examined
for
parasites
in
normal
saline
solution.
Each
organ
was
opened
by
a
fine
scissor
and
left
in
normal
saline
solution
for
few
minutes
with
occasional
shaking.
Hel-
Ininth
parasites
were
picked
up
using
a
fine
pasteur
nipette
or
fine
brush.
If
they
were
strongly
attached
to
the
host
organs,
they
would
be
left
in
the
refrigerator
for
an
hour,
after
which
they
lost
their
grasp
and
were
easily
collected.
If
not,
the
internal
surface
of
the
respective
organ
was
cleaned
by
a
fine
brush
for
detaching
the
parasites.
Specimens
according
to
their
type
were
relaxed,
fixed,
stained,
dehydrated
and
mounted.
Quantitative
determination
of
immunoglobulins:
Blood
sam-
ples
were
taken
directly
from
the
heart
by
disposable
sterile
'syringe.
Blood
was
allowed
to
settle
(27°C),
at
room
tem-
perature
for
about
1/2
an
hour.
Sera
were
separated
by
centri-
fugation
at
3000
r.p.m.
for
about
15
minutes.
Separated
sera
were
collected
in
small
sterile
bottles
and
stored
in
deep
freeze
-at
—20
0
C.
Before
estimation
separated
sera
were
thawed
and
260
estimation
of
immunoglobulins
levels
was
done
by
immunodif-
fusion
method.
(a)
Agar
preparation
:
(1)
To
100
ml
of
barbiturate
buffer
of
pH
8.6
and
ionic
strength
0.02
(containing
0.02%
NaN
3
)
add
2
gm
of
special
Noble
Agar
(Difco).
(2)
The
sus-
pension
was
stirred
on
a
boiling
water
bath
until
dissolved,
and
distilled
water
was
added
to
replace
looses
due
to
evaporation.
The
gel
was
filled
in
well
stoppered
test
tubes,
which
were
stored
for
several
weeks
at
37°C.
(b)
Agar-antiserum
mixture
preparation
:
Antisera
of
rat
were
supplied
from
Miles-Made
products
for
canine
immuno-
assay.
These
were
antisera
of
IgG
(H
&
L)
*
(the
host
was
rabbit),
antisera
of
-
IgM
(the
host
was
goat),
and
antisera
of
IgA
(the
host
was
rabbit).
(1)
The
required
amount
of
soli-
dified
2%
agar
gel
was
melted
on
a
boiling
water
bath
and
cooled
to
55°C.
A
suitable
dilution
of
antiserum
(in
barbiturate
buffer)
was
warmed
to
55°C
and
mixed
at
equal
volumes
with
the
molted
agar.
(2)
The
mixture
was
thoroughly
stirred
(avoid
bubbling)
by
means
of
pipette
preheated
to
55°C
in
water
bath.
The
antiserum-agar
mixture
was
then
poured
without
delay
on
55°C
heated
microscopic
slides
using
55°C
heated
pipette.
(C)
Immuno-diffusion
plate
preparation
:
(1)
In
this
work,
we
used
microscopic
slides.
To
each
slide,
about
a
ml
of
antiserum-agar
mixture
were
added.
The
slides
were
left
until
the
mixture
had
solidified
(after
15
minutes).
(2)
Circular
wells
were
punched
out
of
the
gel
at
a
distance
of
10
mm
intervals
using
a
pasteui
pipette
and
small
parts
of
gel
cut
out
by
the
pipette
were
removed
by
suction.
*
Rat
immunoglobulin
reference
serum
was
prepared
from
a
large
serum
pool
from
outbred
adult
male
and
female
Wistar
and
Sprague
Dawley
rats.
Ail
sera
were
from
normal
healthy
animals.
This
reference
serum
was
supplied
as
liquid
serum
preserved
with
0.1%
sodium
azide.
Its
immunocrlobulin
were
determined
by
repeated
(RID)
radial
immunodiffusion.
(*
=
Miles-Made
Products).
Values
for
the
rat
reference
serum
(m7%1
.
00
ml)
are
:
IgG
=
1320
IgM
=
131
IgA
=
24.3.
-
RESULTS
The
worms
detected
by
autopsies
in
different
rodents
in
the
three
governorates
were
:
Trematoda
:
1.
Echinostoma
callawayensis
(Baker
and
Noll,
1915).
2.
Schistosoma
mansoni
(Sambon,
1907).
Cestoda
:
1.
Andrya
ncotomac
(Voge,
1946).
2.
Hymenolepis
diminuta
(Rudolphi,
1819,
Blanchard,
1891)..
3.
Hymenolepis
nana
(V.
Siebold,
1852
&
Blanchard,
1891).
4.
Taenia
taeniaeformis
(Batsch,
1786).
Nematoda
:
1.
Aspiculuris
tetrapetra
(Mitzsch,
1821).
2.
Syphacia
obvelata
(Rud.,
1802).
3.
Syphacia
muris
(Yamaguti,
1935).
4.
Protospirura
muricola
(Gedoelst,
1916).
Acanthoceph,ala
:
Moniliformis
moniliformis
(Bremser
1811
&
Travassos,
1915).
DISCUSSION
IgG,
IgM
and
IgA
were
more
or
less
increased
than
the
value
of
reference
serum.
However,
the
number
tested
was
not
enough
for
statistical
analysis.
Besides,
most
of
the
rodents
had
ectoparasites.
Rodents
were
dissected,
their
intestines
were
opened
and
worms
were
collected.
These
worms
were,
identified
and
clas-
sified
as
Trematoda,
Cestoda,
Nematoda
and
Archiacanthoce-
phala.
The
Trematodes
were
Echinostoma
callawayensis
and
262
--
Schistosoma
mansoni.
The
Cestodes
were
Andrya
neotomae,
Hymenolepis
diminuta.
Hymenolepis
nana
and
Taenia
taeniae-
formis
(Cyst
in
liver).
The
Nematodes
were
Aspiculuris
tetrap-
tra,
Byphacia
obvelata,
Syphacia
muris
and
Protospirura
muri-
cola.
The
Archiacanthocephala
was
Moniliformis
moniliformis.
Table
1
:
Quantitative
determination
of
immunoglobulins
in
rodents.
Rodent
1gG
Main
Standard
value
parasites
1320
mg/dl
=
6.3
1gM
Standard
value
131
mg/d1
0
.1
5.3
IgA
Standard
value
24.3
mg/dl
3.1
I
A.
niloticus
E.
callawaynis
1460
142
32
2
A.
niloticus
S.
mansont
1915
194
32
3
A.
nilottcus
A.
neotomae
1530
146
1lt
4
R.
rattus
A.
neotomae
1090
176
38
5
A.
niloticus
H.
diminuta
1530
153
6
,
..
6
R.
norvegicus
H.
diminuta
1340
156
48
7
R.
rattus
H.
diminuta
1680
152
5?
8
R.
norvegicus
H.
diminuta
1690
140
5S
9
R.•rattus
H.
nana
1520
156
36
10
R.
rattus
H.
nana
1490
176
4
2
11
R.
Maus
H.
nana
1610
180
48
12
.9
norvegicus
T.
taen.aeformn
1240
154
30
.13
R.
no.
_
.cus
T.
taentaeformis
1400
142
20
14
R.
t=r_vrgicus
T.
taentaeformts
1530
146
36
15
A.
nilottrIA
A.
tetraptera
1640
174
28
16
A.
nilottcus
A.
tetrapetra
1260
158
26
17
A.
nilvicus
t
etrapetra
1510
146
28
18
R.
norvegicus
S.
obvela
a
1480
156
30
19
R.
norvegicus
S.
obvelata
1530
160
3i
20
R.
rattus
S.
muris
1560
160
3
4
2i
R.
rattus
S.
muris
1910
192
32
22
R.
norvegicus
P.
muricola
1680
184
28
23
R.
norvegicus
P.
muncola
1550
146
28
24
R.
norvegicus
M.
rnontLiformus
1510
144
30
25
A.
nolottctis
-z•
M.
montliformts
1430
I.'
34
Regarding
Echinostoma
callawcfyensis,
3
worms
were
col-
lected
from
one
Arvicanthis
nitoticus
trapped
in
Ismailia.
Baker
263
--
et
al.
(1915)
named
and
described
E.
callawayensis
from
the
American
musk
rats
Fiber
xibethicus.
Beaver
(1937),
Bonne
et
al.
(1953),
Lie
(1963
a,b
and
1964)
suggested
that
"one
of
the
most
important
features
in
determining
the
species
of
adult
echinostomes
is
arrangement
of
the
collar
spines,
"While
Lice
et
al.
(1965)
pointed
out
that
species
diagnosis
of
echino-
stomes
by
adult
characteristics
only
may
be
misleading.
This
rodent
parasite
is
not
yet
recorded
in,
man.
The
second
trematode
recovered,
Schistosoma
mansoni
was
found
in
one
Arvicanthis
niloticus
trapped
in
Ismailia.
Kuntz
(1952)
discovered
S.
mansoni
in
a
gerbil
in
Egypt
and
empha-
sized
that
animals
might
play
a
part
in
the
transmission
of
bilharziasis
in
Africa
or
South
America.
During
the
past
ten
years
many
animals
have
been
examined
for
natural
schisto-
some
infections.
S.
mansoni
has
been
found
in
numerous
rodents
in
the
Congo,
in
South
Africa
and
in
East
Africa
(Koppisch.
1937).
In
the
present
study
the
eggs
were
elongated
with
pro-
liferation
of
the
endothelium
around
the
eggs
excluding
them
from
the
lumen.
Also
there
was
inflammatory
reaction
and
cellular
infiltration
of
mononuclear
and
polymorphnuclear
leu-
cocytes
and
eosinophils
around
eggs.
The
portal
tract
was
thickened
by
fibrous
tissue
containing
ova
and
inflammatory
reaction.
Regarding
the
pathology
in
the
liver,
Main
(1963)
s.tudied
the
bilharzial
granuloma
in
rodents
and
showed
an
elongated
egg
with
a
prominent
lateral
spina
covered
by
an
endothelium
lined
cavity,
surrounded
by
phagocytic
epithelioid
cells
and
occa-
sional
giant
cells.
An
outer
mantle
consisted
of
lymphocytes,
plasma
cells,
and
few
neutrophils
with
eosinophils
througtiout
the
layers.
Fibroblasts
of
various
stages
of
maturity
appeared
later
in
the
outermost
zones
of
the
granuloma.
Cheever
(1965)
defined
the
recently
formed
bilharzial
granuloma
as
that
con-
taining
Schistosoma
eggs
with
a
mature
structurally
intact
miracidium
or
that
with
recognizable
cellular
embryonic
rem-
nants.
Kloetzel
(1969)
described
the
mature
egg
as
that
which.
possesses
a
thick
linear
shell,
and
an
embryo
strongly
eosino-
philic
with
haematoxylin
and
eosin
stain.
—264--
,
.
Maniottr
(1973)
iri
Egypt,
repor
ted
that
3
,out
of
22
A.
iitilotieus
caught
from
El
Mansuriya,
Giza;
were
naturally
in-
fected
with
S.
mansonti
and
S:
lzaernatobiiim.
He
added
that
on
bx0riniental
work
this
animal
'can
serve
as
a
natural
reservoir
libht.'
In
Egypt
alsO
many
authoii
as
Mintz
(1952),
Fahmy
et
al.
(1971),
El
Nahal
et
al.
(1.60)
and
Moriy
et
al.
(1982)
reported
the
presence
of
the
billiarzial
worm
or
antibodies
against
them
in
some
species
of
rodents.
One
of
.
the
cestodes
recovered
was
'7'nenict
taeniae
fO?mis
(101.'
'cyst
iii
the
liver
of
Ar.
ntiloitilms
.
2.4%;
R.
izo
.
rimgticu,S
R
.
rattus
0.2%
and
Ada.
cahirinus
1.7
6
7
0
caught
froth
'the
three
goverrioratei.
The
cysfs
occurred'
in'
both
lobe's
of
the
livCi'riotiin
the
right
robe
as
'mentioned
by
Tyagi
and
.
Ailishia
(1978'
and
-
with:
no
hooklets
on
the
cuticle'
around
the
base
of
elvatiori,
its
reported
by
CiuSz
.
.
,
.
Dove
(1950)
-
Saicrthat
Taentia
iaentiaeforthis
has
a
cosmo-
politan
distribution
and
infection
of
the
liver
with
those
laiime
is
p_common
infective
feature
of
rats
in
many
parts
of
the
world
particularly
U.S.A.
Also,
Morsy
et
al,.
(1981
and
1982)
detected
this
parasite
.
in
stray
cats
and
rodents
in
Cairo
and
Ismailia.
In
all
animal
hosts,
the
bladder
of
T.
taentiaeforrnis
appear
as
pear
shaped
.
single
sac
by
the
light,
microscope.
When
using
scanriing
electron
microscope
lateral
and
terminal
excre
,
tory
pores
were
seen
in
the
bladder
of
T.
taentiaeformtis
from
experimentally
infected
rat
.
(Jones,
et
al.,
1977).
Taentia
taenticreformis
is
a
normal
parasite
of
the
intestine
of
the
cat,
which,
becomes
infected
by
eating
rats
.harbouring
the
strobilocercus
stage.
A
single
human
infection
(probably
accidental)
has
been
recorded
in
Buenos
Aires,
.Argentina
in
a
five
year-old
child
(Faust
et
al.,
1976).
,
. .
Andrya
neotomae
(22)
was
collected
from
the
small
intes-
tine
of
ArvicanthiS
ntiloticui
7.2%
and
Rattus
rattus
6.7%
caught
in
Ismailia'
and
Port
Said.
In
the
present
study
TI.
dirnitiuta
(250)
was
recovered
froth
Ar.
triloticus
32.5%,
1?.
My-
vegicus
16.4%,
R.
rattus
1%
and
Aco.
cahirtinus
11.7%
Caught
.-265
from
the
three
governorates.
Tho
morphological
characteristics
of
H.
diminuta
(Weinland,
1858)
agreed
with
the
descriptions
of
both
Spassky
(1954)
and
Yamaguti
(1959)
dimenSions
of
cirrus
pouch
varied
from
one
author
to
another
due
to
age
of
segment
(Meggitt,
1927).
Mikhail
(1967)
classified
the
unarmed
rostellae
species
of
genus
Hymenolepis
according
to
the
position
of
testes
which
may
be
arranged
either
in
triangle
or
straight
line.
H.
diminuta
was
described
by
many
workers
from
rodents
in
Egypt
as
Meggitt
(1927),
Fahmy
(1961),
Mikhail
(1967),
Arafa
(1968),
Monib
(1980),
Azzazy
(1981),
and
Morsy
et
al.
(1982).
In
the
majority
of
the
mature
segments
examined,
there
are
three
testes
:
one
portal
and
two
aporal.
Only
Mikhail
(1967)
found
in
some
mature
segments
three
aporal
testes
and
less
frequently
one
poral
and
other
aporal.
Also,
he
described
the
mature
proglottides
of
one
specimen
in
which
no
testes
was
found
although
a
well
developed
ovary
and
vitelline
gland
were
present.
Regarding
infection
in
humans,
in
America,
H.
diminuta
was
recorded
from
the
southern
States
by
Clark
(1930)
;
Keller
(1931)
;
Keller
and
Leathers
(1936)
;
Smith
et
al.
(1953)
and
Ratliff
(1965).
In
Russia,
H.
diminuta
infection
in
man
was
recorded
by
Nitzulescu
et
al.
(1955)
and
Geller
(1956).
In
Egypt,
H.
diminuta
infection
(2%)
was
recorded
by
Chandler
(1961).
Arafa
(1968)
found
the
incidence
of
H.
diminuta
infec-
tion
in
Kharta
(Imbaba),
Cairo,
was
7.8%.
In
the
area
where
infected
rodents
were
caught,
not
a
single
human
case
was
detected
(El
Gindy
et
al,
1986).
Ten
H.
nana
were
collected
from
M.
musculus,
R.
rattus
and
Aco.
cahirinus
caught
in
the
3
governorates.
This
worm
was
found
not
to
be
an
uncommon
cestode
in
rodents
as
stated
by
Ruch
(1959)
and
Belding
(1965).
However,
it
was
recorded
in
rhesus
monkey
and
chimpanzee
(Bensen
et
al.
1954
and
Middleton
et
al,
1964).
Grassi
(1887)
first
suggested
that
the
human
and
mice
strains
were
identical.
He
based
his
view
on
the
infection
of
one
out
of
6
children
who
were
fed
gravid
proglottids
of
the
parasite
of
rats.
266
Another
nematode
recovered
was
Aspiculuris
tetraptera
(25)
which
was
collected
from
the
caecum
and
colon
of
Ar.
niloticus
12%
and
R.
norvegicus
0.9%
trapped
from
the
3
governorates.
In
previous
studies
A.
tetraptera
worms
were
recovered
by
Meyers
et
.
al.
(1962)
from
M.
musculus,
R.
rattus.
and
Ar.
nilo-
ticus,
by
Fahmy
et
al.
(1971b)
from
R.
rattus,
by
Rifaat
et
al.
(1969a)
from
R.
rattus,
Rifaat
et
al.
(1969b)
from
small
mam-
mals
particularly
rodents,
by
Monib
(1980)
and
lastly
by
Azzazy
(1981)
but
no
description
was
given
by
any
of
these
authors.
Another
nematode
Protospirura
muricola
(6)
was
recover-
ed
from
the
stomach
of
R.
norvegicus
(0.6%),
Ar.
niloticus
(1.2,%)
and
R.
rattus
(0.3%)
trapped
in
Ismailia
and
Suez
governorates.
In
Egypt,
Meyers
et
al.
(1962)
recovered
P.
muri-
cola.
Mikhail
(1967)
recorded
it
from
M.
musculus
and
Aro.
cahirinus
and
reported
that
incidence
of
P.
muricola
in
both
hosts
was
20%
and
4%
respectively.
Fahmy
et
al.
(1971)
re-
ported
P.
muricola
from,
both
Aco.
cahirinus
and
M.
mudculus.
Ashour
(1980)
described
P.
muricola,
from
A
r.
niloticus,
R.
rattus.
R.
norvegicus,
Ace.
cr!h
4
rinus.
M.
muscului
and
Gerbillus
pyramidum.
Moniliformis
moniliformis
is
a
cosmopolitan
parasite
in
wild
Norway
and
black
rats
and
in
other
rodents
through
the
world
(Witenberg.
1964).
The
life
history
usually
involves
an
arthroped
(Periplaneta
americanus)
as
intermediate
host
in
which
larval
development
occurs
and
a
vertebrate
definitive
host
into
which
it
grows
to
the
adult
worm.
They
rarely
and
accidentally
infect
man
because
the
intermediate
hosts
(C,
elt-
roaches)
are
not
likely
to
be
ingested.
Besides
this
parasite
has
not
been
reported
in
commercially
or
laboratory
reared
rodents
(Flynn,
1973).
CONCLUSION
Rodents
populations
are
increasing
in
many
Egyptian
governorates
particularly
in
coastal
areas.
Eleven
species
of
268
worms
were
identified
in
their
alimentary
tract
and
tissues.
Of
great
interest
was
the
detection
of
S.
mansoni
egg(
in
the
liver
of
A.
niloticus.
Many
authors
detected
S.
mansoni
or
antibodies-
against
it.
However
the
detection
of
S.
mansoni
in
the
liver
has
its
own
epidemiological
meaning.
So,
one
can
say
that
rodents
play
a
very
important
role
in
human
Health
and
Wel-
fare.
It
is
not
surprizing to
say
that
they
are
the
first
human
enemy.
It
is
the
duty
of
the
Public
Health
Authorities
and'
people
as
well,
to
design
a
control
program
strategy
based
on
completd
understanding
of
"All
About.
Rodents".
ACKNOWLEDGEMENT
This
work
was
partially
supported
by
Research
Contract
No.
NOI
AI
22667
(NIH/NIAID
USAID)
between
Ain
Shams
-
University,
Research
and
Training
Center
on
Vectors
of
Diseases
and
National
Institutes
of
Health,
Bethesda,
MD
20892,
U.S.A.
Sincere
thanks
are
due
to
the
Public
Health
Authorities
in
Suez,
Ismailia
and
Port
Said
Governorates
for
their
help
to
make
the
field
work
possible.
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Three
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Tennessee
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