Advances in Biological Chemistry, 2011, 1, 103-108
doi:10.4236/abc.2011.13012 Published Online November 2011 (http://www.SciRP.org/journal/abc/ ABC
).
Published Online November 2011 in SciR es. http://www.scirp.org/journal/ABC
Compatibility of Biomphalaria glabrata and B. alexandrina
snails to infection with an egyptian strain of Schistosoma
mansoni through two cycles in the experimental final host
Momeana Bayoumi Mahmoud
Environmental Research e s and Medical Malacology Department, Theodor Bilharz Research Institute, Giza, Egypt.
Email: gibriel2003@gmail.com
Received 24 September 2011; revised 29 October 2011; accepted 8 November 2011.
ABSTRACT
The infection rate and cercarial production from B.
glabrata, in comparison with B. alexandrina snails,
post their exposure to S. mansoni miracidia of an E-
gyptian strain after two cycles in albino-mice was
studies.The results indicated that infection rate of B.
glabrata with the Egyptian strain of S. mansoni was
less than that of B. alexandrina snails On the other
hand infected B. glabrata exhibited a longer life span
and a higher number of shedding cercariae, It was
also, noticed that in the first cycle mice infected with S.
mansoni cercariae shed from infected B. alexandrina
snails, the mean number of worms recovered from
infected mice was approximately twice that in mice
infected with cercariae shed from infected B. glabrata
snails The same observation was recorded from the
mean number of ova/g liver tissue from infected mice.
In the second cycle the same observation was re-
corded as first cycle suppression in the infection rate
of B. glabrata than that B. alexandrina. Also, longer
prepatent period and life span Also, mice infection as
the number of worms per infected mouse by cercariae
shed from B. alexandrina snails was approximately
2.5 times that of mice infected by cercariae shed from
B. glabrata being 29.3 and 12.5 worms/mouse.The
results also indicated that the egg laying capacity of B.
glabrata was higher than that B. alexandrina, It is
concluded from this work that infectivity of S. man-
soni cercariae shed from B. glabrata snails after two
cycles of mice infection and used to infect the experi-
mental final host was less than that of cercariae shed
from infected B. alexandrina snails. This may declare
a low compatibility o f B. glabrata snails with the Egy-
ptian strain of S. mansoni in comparison with B. al-
exandrina snails. However, this conclusion needs more
passages of mice infection with cercariae to have pre-
cise data and conclusions.
Keywords: Biomphalaria alexandrina; B. Glabrata;
Schistosom a m ansoni; Compatibility
1. INTRODUCTION
Schistosomiasis is one of the major health problems in
many developing countries [1]. The prevalence of this
parasite in human population depends on the number of
infected snails in an area. The specificity of parasite-host
interactions has received great attention by parasitolo-
gists and evolutionary biologists [2].
It was known till 1996 that B. alexandrina is the only
planorbid species acting as the intermediate host of
Schistosoma mansoni in Egypt. This snail was widely
distributed now along the Nile Delta and valley. Re-
cently, B. glabrata the intermediate host of S. mansoni in
the New world, has been reported from natural freshwa-
ter habitats in Egypt [3]. The authors collected the snail
population from many water courses of irrigation and
drainage systems in Qalyoubia and Kafr El-Sheikh Go-
vernorates.
In trematode-snail interactions, which are generally
regarded as highly specific [4], compatibility patterns of
species or strains of parasites and hosts have been used
for phylogenetic studies as well as for investigations of
parasite-host convolu tion on a local scale [5], Especially
in medically relevant blood flukes. Snail compatib ility is
also a topic of practical importance for epidemiological
surveys and development of biological control methods.
This is the reason why most work on snail compatibility
and the snail’s internal defense system against trematode
infections was performed with S. mansoni [6]. Host snails
of the genus Bomphalaria respond with humoral and
cellular mechanisms to S. mansoni sporocysts [7]. It was
recently demonstrated by selection experiments under
laboratory conditions with different snail lines that, in
the system S. mansoni, B. glabrata, compatibility char-
acteristics seem to be inherited with resistance being
dominant over susceptib ility [4,8].
M. B. Mahmoud / Advances in Biological Chemistry 1 (2011) 103-108
104
In fact, we found that an Egyptian (laboratory) strain
of S. mansoni discriminated between its host snail B.
alexandrina and other species and strains, already during
approach and after contac [9,10].
The present study aims to study the compatibility of B.
glabrata snails to infection with an Egyptian strain of S.
mansoni which is very important from the epidemiol-
ogical point of view and draws the attention to the pos-
sible role of this snail (B. glabrata) may play in schisto-
somiasis in Egypt.
2. MATERIALS AND METHODS
2.1. Snails
The snails used in the present study, Biomphalaria alex-
andrina and B. glabrata, were obtained from the Schisto-
some Biological Supply Centre (SBSC), Theodor Bilharz
Research Institute (TBRI). B. glabrata snails were col-
lected from some foci in the irrigation canals at Qalyoubia
Governorate [3], transferred to laboratory examined for
natural trematode infection, negative and healthy ones
were maintained under laboratory conditions [1 1].
2.2. Snails Infection
S. mansoni miracidia of the Egyptian strain were obtained
from SBSC. B. alexandrina and B. glabrata snails used
for infection were almost the same size (4 mm - 5 mm)
and individually exposed to miracidia (10 miracidia/snail)
for 24 hrs after miracidial exposure, snails were main-
tained in dechlorinated water at 24˚C ± 1˚C then from 20
days post exposure, samples from surviving snails were
microscopically examined for sporocysts. The other sur-
viving snails were examined to cercarial shedding after 30
days post miracidial exposure by exposing each snail in 2
ml water for 3 hrs to 100 watt filament lamp, 40 cm far at
26˚C ± 1˚C. Positive snails were isolated, marked and
re-exposed for cercarial shedding twice weekly. The cer-
cariae emerged from each positive snail were counted and
recorded. The prepatent period, infection rate, periodic
cercarial production and life span of infected snails were
determined for each species.
2.3. Fecund ity of B. alex andrina and B. glabr at a
For each snail species three replicates were used each of
10 snails (5 mm - 8 mm)/L the aquaria were provided
with thin plastic sheets for egg deposition. The snails
were fed blue-green algae (Nostoc muscorum) and dried
lettuce leaves. The egg clutches were weekly collected
and eggs were counted and recorded.
2.4. Animals Infections
Laboratory bred albino mice in this study were obtained
from SBSC cercariae shed from infected B. alexandrina
snails were used to infect a group of 6 mice and those
shed from B. glabrata were used to infect another 6 mice
group. The infection was done by the tail immersion
method (100 cercariae/mouse [11] and 4 mice non-in-
fected act as a control.
2.5. Parasitological Investigations
Worm load and distribution were studied in infected
mice by perfusion (hepatic and intestinal) method and
the number of eggs was counted per g tissue [12]. The S.
mansoni eggs from mice infected with cercariae shed
from B. alexandrina snails were hatched to miracidia
that used to infect clean groups of B. alexandrina and
B.glabrata snails. The same re-exposure of snail to mi-
racidia was followed by miracidia hatched from S. man-
soni eggs obtained from mice infected with cercariae
shed from B. glabrata snails. This technique of re-ex-
posure of snail to miracidia was repeated after another
passage of mice infection with cercariae shed from the
first passage of infect i on.
2.6. Student’s t-Test
Student’s t-Test and chi-square test [13] were used in
comparing the means and rates of experimental group
statistically.
3. RESULTS AND DISCUSSION
3.1. First Cycle
Laboratory produced snails B. alexandrina and B. gla-
brata were exposed to S. mansoni miracidia individually
(10 miracidia/snail). The result indicated that after 20
days from exposure to miracidia the survival rate of B.
glabrata significantly higher (96%) than B. alexandrina
(76%). Crushing ten snails from each species to examine
for sporocyst revealed that positive snails of B. alexan-
drina was 8 snails, however only one snail positive of B.
glabrata.
The present results showed that there are significant
differences between B. alexandrina and B. glabrata in-
fected with S. mansoni from Egypt, in the tested pa-
rameters (survival rate, infection rate, prepatent period,
cercarial production, duration of shedding and life span
of infected snails).
From Ta ble 1 the results indicated that after 34 days
from miracidial exposure the survival rate of B. glabrata
was higher about 70% compared to 46% of B. alexan-
drina with significant difference (p < 0.001). These re-
sults agree with [7,14], they found that a reduction in th e
survival rate of infected B. alexandrina compared to in-
fected B. glabrata snails through the prepatent period.
The present results showed that B. glabrata was less
susceptible to in fection with Egyptian strain of S mansoni
than B. alexandrina being 8.6% and 78.3% respectivel y.
The infection rate was significantly much higher of
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M. B. Mahmoud / Advances in Biological Chemistry 1 (2011) 103-108
Copyright © 2011 SciRes.
105
ABC
Ta ble 1. Survival rate, infection rate, prepatent period, cercarial
production, duration of shedding and life span of infected B.
alexandrina and B. glabrata with S. manson i miracidia.
op B. alexandrina B. glabrata
Number of exposed snails to
miracidia of Egyptian strain
50 50
Number of survived snails at
first cercarial shedding
23 35
Survival rate 46% 70%
Number of infected snails 18 3
Infection rate 78.3% 8.6%
Prepatent period (days)
Range 34 - 53 59 - 61
Mean ± SD 37.5 ± 5.8 60.0 ± 1.0
Total number of cercariae 14731 11492
Range 21 - 2485 1888 - 7482
Mean ± SD 818.4 ± 720.8 3830.7 ± 316
Duration of cercarial
shedding (days)
Range 4 - 45 30 - 69
Mean ± SD 18.1 ± 11.2 43.3 ± 22.2
Life span (days)
Range 47 - 86 71 - 110
Mean ± SD 56.8 ± 9.1 97 ± 22.5
B.alexandrina than that of B.glabrata (p < 0.001). This
agrees with the previous findings of Files [15], Kuntz
[16] and Cridland [17] they found that the susceptibility
of B.glabrata to S mansoni from Egypt was very low
being 8% - 30% and 0%. The same conclusion was re-
corded by Yousif et al. [18]. They found that the infec-
tion rate of all Egyptian S. mansoni strains was signifi-
cantly higher in B. alexandrina than each of B. glabrata
and the hybrid snail. Also, Kalbe et al. [9] found that
infection rate of Brazilian sn ail B. glabrata with S. man-
soni Egyptian strain ranged between 12.3% and 18.7%
Bakry [7] found that infection rate of B. glabrata and B.
alexandrina from Domietta 8% and 16% respectively
were significantly less than tho se of B. alexandrina from
Fayoum and Giza (56% and 64%, respectively p <
0.001)
The results showed that the prepatent period of S.
mansoni in B. glabrata was significantly longer than in
B. alexandrina being 60 days and 37.5 days r espectively
(p < 0.001). This resu lt agrees with Yousif et al. [3] who
showed that B. glabrata has significantly longer incuba-
tion period than B. alexandrina being 33.45 days and 28
days respectively (p < 0.05) when exposed to laboratory
strain of S. mansni (SBSC) from Egypt.
The cercarial production of B. alexandrina was sig-
nificantly less (p < 0.001) than that of B. glabrata the
mean number of cercariae per snail of infected B. alex-
andrina was 818.4 cercariae/snail compared to mean
number of cercariae shed from infected B. glabrata was
3830.7 cercariae/snail.
The result agrees with Yousif et al. [18] who found
that cercarial production from B. alexandrina was lower
than those from B. glabrata and hybrid snail species post
their exposure to an Egyptian strain from SBSC. This
observation is in p arallel with that of Frandsen [19] who
found that B. glabrata infected with various strains of S.
mansoni from St. Lucia and the West Indies produced
variable numbers of cercariae. However Bakry [7] found
that the cercarial production of B. glabrata and B. alex-
andrina from Damietta was significantly lower than th at
of B. alexandrina from Fayoum and Giza.
The result indicated that the mean of duration of
shedding and life span of infected B. glabrata was
longer than of B. alexandrina infected snails being 43.3
and 97 days compared to 18.1 and 56.8 days respectiv ely
(p < 0.001). A similar result was observed by yousif et al.
[18] who found that duration of cercarial shedding from
B. alexandrina infected with S. mansoni from Egypt was
shorter than those of B. glabrata and hybrid snails.
Frandsen [19] who found that the longest duration of
cercarial production by B. glabrata, St.Lucia infected
with its local S. mansoni strain was 180 days.
The infected mice by cercariae of B. glabrata and cer-
cariae of B. alexandrina were dissected after 60 days
from exposure to cercariae by perfusion hepatic and in-
testine method. The worm were picked out and placed in
normal saline and counted. The number of ova/g tissue
liver was estimated (Ta ble 2) show that the number of
infected mice by cercariae of B. alexandrina was 5 mice
and the other infected with cercariae from B. glabrata
was 4 mice. From Tabl e 2 it was indicated that the low-
est number of worms was obtained from mice infected
with cercariae shed from B. glabrata snails being 38
worms compared to 85 worms obtained from mice in-
fected with cercariae shed from B. alexandrina. in the
first cycle the mean number of worms per infected
mouse with Schistosoma cercariae shed from B.
glabrata was reduced being 9.5 worms/mouse compared
to 17 worms/mouse infected with cercariae shed from B.
alexandrina. This result agrees with the previous find-
ings of Jourdane et al. [20] recorded a reduction in the
infectivity of Schistosome cercariae shed from B. gla-
brata infecte d wit h both S. manso ni and E. liei.
The mean number of ova cunt per g tissue liver of in-
fected mice with cercariae of B. glabrata decreased sig-
nificantly than that of infected mice by cercariae shed
ding from B. alexandrina being 771.8 compared to 1579
M. B. Mahmoud / Advances in Biological Chemistry 1 (2011) 103-108
106
Table 2. Total and mean number of worms in mice infected with S. mansoni cercariae from B. alexandrina and B. glabrata snails (the
first passage of mice infection).
Case (1) worm load/mouse infected by cercariae from
B. alexandrina
Case (1) worm load/mouse infected by cercariae from
B. glabrata Mice’ number
F M Couple Total F M couple Total
1
2
3
4
5
6
4
8
0
2
4
-ve
7
3
4
5
2
-ve
3
7
3
4
6
-ve
17
25
10
15
18
-ve
1
3
4
3
-ve
-ve
0
0
0
1
-ve
-ve
2
5
6
0
-ve
-ve
5
13
16
4
-ve
-ve
Total 18 21 23 85 11 1 13 38
Mean ± SD 3.6 ± 3.0 42 ± 1.9 4.6 ± 1.8 17 ± 5.4 2.8 ± 1.3 1 4.3 ± 2.1 9.5 ± 5.9
Mean of ova/g tissue live r 1579 ± 125.8 771.8 ± 99.9
F: Female, M: Male.
ova/g tissue. Warren & Peters [21] obtained adult worms
from mice exposed to 40 S. mansoni cercariae with only
10 minutes exposure period. Blumenthal & Jewsbury [22]
showed that increasing of cercarial age (2,3,6,8 and 10
hours) gave no effect on percentage worm recovery.
The present results showed that the number of ova re-
tained in the tissue of liver increased with the in crease of
number of worms. Similar relation was reported by
Kloetzel [23] an d Koura [24 ] who found that th e number
of retained eggs was always proportional to the worm
burden. On the contrary, Grove & Warren [25] stated
that with increasing worm burden, the number of eggs in
the liver per worm pair tended to decrease. The S. man-
soni eggs from mice infected in the first cycle with cer-
cariae shed from B. alexandrina snails were hatched to
miracidia that used to infect group 1) clean B. alexan-
drina and group 2) clean B. glabrata. Also, miracidia
hatched from eggs from mice infected with cercariae
shed from B. glabrata were used to infect group 3) clean
B. alexandri na and group 4) clean B. glabrata.
The first cycle: the present results showed that there
were no difference between the result of first cycle and
second cycle. The survival rate was higher in infected B.
glabrata than that of infected B. alexandrina. Also, the
infection rate was highest in group 1) being 66.7% com-
pared to 14.3% and 53.3% for group 2) and 3) while gr ou p
4) was the lowest infection rate being 10% (Table 3).
In the second cycle the mice infected by cercariae
shed from each group of snails infected, the number of
mice infected in each group was 5 mouse. From Table 4
the result indicated that the highest mean number of
worms/mouse was obtained from mice infected with
cercariae shed from B. alexandrina group 1) being 29.3
worms/mouse while the mice infected with cercariae
shed from snails in group 4) showed a low value, being
12.5 worms/mouse, with a reduction rate of 42.7% from
that group 1). This may indicate that infectivity of
Schistosoma cercariae of an Egyptian strain shed from B.
glabrata snails to albino mice was suppressed by succes-
sive passages of mice and snails infection with this para-
site strain. Also, the mean number of ova per g tissue of
liver in infected mice in group 1) was higher being 1504
compared to 670.5 ova/g in mice infected with cercariae
from snail group 4).
In the present study, cohorts of B. alexandrina and B.
glabrats snails were maintained for 4 weeks under stan-
dard laboratory conditions at a constant temperature
(25˚C + 1˚C) for comparing fecundity of both snail spe-
cies. B. glabrata snails showed a high survival rate (Lx)
of 93% compared to 66% of B. alexandrina. The net
reproduction rate of B. glabrata (Ro) was higher than
that of B. alexandrna after experimental observation
period (4 weeks) being 34.7 and 4.69, respectively (Ta-
ble 5). This observation is in accordance with that of
Yousif et al.[18] who recorded a high value of (Ro) for B.
glabrata in comparison with that of B. alexandrina
snails being 1265.9 and 145.3 respectively. However,
Sturrock [26] and Pointier et al. [27] attributed that dif-
ference to strain and type of feeding of the snails.
It is concluded from this work th at there is a low com-
patibility of B. glabrata snails with an Eg yptian strain of
S. mansoni in comparison with B. alexandrina snails. Ho-
wever, this conclusion needs more passages of mice infec-
tion with cercariae to have precise data and conclusions.
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M. B. Mahmoud / Advances in Biological Chemistry 1 (2011) 103-108 107
Table 3. Survival rate, infection rate, prepatent period, cercarial production, duration of shedding and life span of infected groups of
B. alexandrina and B. glabrata with S. mansoni miracidia from mice infected in the first cycle.
Survivorship at
1st shedding
Infection rateNumber of
groups and snail
species
% No.%
Prepatent period
(days)
Range
Mean ± SD
Total no of cercariae/snail
Mean ± SD
Duration of
shedding (days)
Range
Mean ± SD
Life span
(days)
Range
Mean ± SD
18 60 12 66.725 5931 5 - 31 35 - 66 1) B. alexandrina
1937.2 ± 417.4 15.5+10.1 44.4 ± 11.7
21 70 3 14.342 - 70 16264 5 - 40 47 - 110 2) B. glabrata
58 ± 14.4 5421.3 ± 1995.9 23.3+17.6 83.3 ± 32.2
15 50 8 53.325 - 31 5860 4 - 22 43 - 53 3) B. alexandrina
28.5 ± 2.9 732 ± 392.5 13.6 ± 7.2 47.8 ± 3.2
20 66.7 2 10 40 - 53 1255 5 - 14 45 - 70
9.5 ± 6 .4 57.5 ± 17.7 4) B. glabrata
46.5 ± 9.2 627.5 ± 62.9
Tabl e 4. Worm load per mouse infected with S. mansoni cercariae shed from snails of B. alexandrina and B. glabrata in the second
cycle.
Worm load/mouse Cercariae
shed fom snail
groups
No. of
survived mice
No. of
infected mice
F M CoupleTotal
Total no. of worms
Mean ± SD
Mean no of ova/g
tissue liver ± SD
(1) 3 3 10 9 6 31 88
15 6 3 27 29.3 ± 2.1 1504 ± 409.3
13 9 4 30
(2) 3 1 5 2 4 15 15 567
(3) 4 3 6 9 2 19 41
3 4 2 11 13.7 ± 4.6 773.7 ± 211.6
6 3 1 11
(4) 4 2 3 2 3 11 25
7 3 2 14 12.5 ± 2.1 670.5 ± 160. 5
Table 5. Survival rate (Lx) & fe cundity (Mx) of B. alexandrina and B. glabrata after four weeks of maintenance under standard labo-
ratory conditions.
B. alexandrina B. glabrata Observation period (weeks)
Lx Mx LxMx Lx Mx LxMx
1 1.00 1.2 1.2 1.00 10.5 10.5
2 0.90 1.1 0.99 1.00 10.2 10.2
3 0.73 1.7 1.2 0.96 8.37 8.1
4 0.66 1.9 1.3 0.93 6.42 5.9
Ro 4.69 34.7
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