Concurrent infections of Fasciola, Schistosoma and Amphistomum spp. in cattle from Kafue and Zambezi river basins of Zambia.
ABSTRACT This study investigated interactions among Fasciola gigantica, Schistosoma spp. and Amphistomum spp. concurrent natural infections in Zambian cattle, based on egg and worm counts. In the abattoir 315 cattle were screened for worms of F. gigantica in the liver, Schistosoma spp. in mesenteric veins and/or Amphistomum spp. in the rumen. One hundred and thirty-three (42.2%) of the abattoir-examined cattle harboured one, two or all three trematodes. Of 133 cattle, 50 were randomly selected for worm and egg counts. The mean numbers (+/- SD) of Amphistomum, Schistosoma and Fasciola were 622.08 (+/- 97.87), 33.68 (+/- 7.44) and 19.46 (+/- 4.58), respectively. A total of 32% harboured all the three trematodes, 66% had F. gigantica and Amphistomum spp. infections, 52% had Schistosoma spp. and Amphistomum spp. infections while 32% had F. gigantica and Schistosoma infections. A positive correlation (P = 0.014) was found between F. gigantica and Amphistomum worm burdens. There were no correlations between Amphistomum and Schistosoma worm burdens and between F. gigantica and Schistosoma worm burdens. It may be concluded that there is no significant cross-protection among these trematodes in cattle in endemic areas.
Article: The Antischistosomal Activity of Fasciola gigantica and Schistosoma mansoni Eggs is Influenced by Saponin Extracted from Atriplex nummularia[show abstract] [hide abstract]
ABSTRACT: The objective of the present study was to evaluate the antischistosomal, biochemical and humoral immune response of Fasciola gigantica and Schistosoma mansoni eggs homogenate influenced with or without saponin extracted from Atriplex nummularia. The work was extended to study the histopathological picture of the liver before and after challenge. Total worms reduction recorded 57.14, 80.95 and 42.85% in immunized mice with Fasciola egg homogenate (50µg/100µl PBS/mouse), Fasciola egg homogenate influenced by saponin (50µg/100µl PBS/mouse) and saponin alone (50µg/100µl PBS/mouse), respectively. Immunized groups with Schistosoma egg antigen and Schistosoma egg antigen influenced by saponin showed reduction in total worms by 47.61, 52.38%, respectively. In conclusion, immunization with Fasciola gigantica egg homogenate possesses promising antischistosomal properties with an immunomodulatory response to saponin. Heterologous homogenate had antischistosomal activity more than homologous homogenate. In addition, heterologous homogenate influenced with saponin had more antischistosomal activity than its homologous homogenate. Moreover, Fasciola gigantica egg homogenate had an immunoprophylactic effects by increasing the IgM and IgG levels against Schistosoma egg antigen. [Journal of American Science. 2010;6(8):368-381]. (ISSN: 1545-1003).American Journal of Science 01/2010; · 2.72 Impact Factor
Article: The Nexus between Bovine Tuberculosis and Fasciolosis Infections in Cattle of the Kafue Basin Ecosystem in Zambia: Implications on Abattoir Surveillance.[show abstract] [hide abstract]
ABSTRACT: Bovine tuberculosis (bTB) and fasciolosis are important but neglected diseases that result in chronic infections in cattle. However, in Zambia, these diseases are mainly diagnosed at abattoirs during routine meat inspection. Albeit the coinfection status, these diseases have been reported as nothing more than normal separate findings without an explanatory phenomena. Forthwith, we formulated this study to assess the possible association of the two diseases in a known high prevalence area on the Kafue basin ecosystem. Of the 1,680 animals screened, 600 (35.7%; 95% CI 33.4%-38%) and 124 (7.4%; 95% CI 6.1%-8.6%) had fasciolosis and tuberculous lesions; respectively, whilst 72 had both fasciola and tuberculous lesions representing 12% (95% CI 9.4%-14.6%) and 58.1% (95% CI; 49.3%-66.7%) of the total positives for fasciola and tuberculosis, respectively. Jaundice was seen in 304 animals, 18.1% (95% CI; 16.3%-19.9%) and was significantly correlated to fasciolosis (r = 0.59, P < 0.0001). A significant association (χ(2) = 76.2, df = 1, and P < 0.0001) was found between fasciolosis and tuberculous lesions. Simple logistic regression intimated fasciolosis as a strong predictor for tuberculous lesions with animals that had fasciola being five times more likely to have tuberculous lesions (odds ratio = 4.8, 95% CI: 3.3-7.0). This study indicates that transmission and spatial risk factors of communicable and noncommunicable diseases such as bTB and fasciolosis can be correlated in an ecosystem such as the Kafue flats.Veterinary medicine international. 01/2012; 2012:921869.
Concurrent infections of Fasciola,
Schistosoma and Amphistomum spp. in
cattle from Kafue and Zambezi river basins
J. Yabe1*, I.K. Phiri2, A.M. Phiri2, M. Chembensofu1, P. Dorny3,4
and J. Vercruysse3
1Paraclinical Studies Department, School of Veterinary Medicine, The
University of Zambia, PO Box 32379, Lusaka, Zambia:
Department, School of Veterinary Medicine, The University of Zambia,
PO Box 32379, Lusaka, Zambia:
Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820
Nationalestraat 155, B-2000, Antwerp, Belgium
3Department of Parasitology, Faculty of
4Prince Leopold Institute of Tropical Medicine,
This study investigated interactions among Fasciola gigantica, Schistosoma spp.
and Amphistomum spp. concurrent natural infections in Zambian cattle, based on
egg and worm counts. In the abattoir 315 cattle were screened for worms of
F. gigantica in the liver, Schistosoma spp. in mesenteric veins and/or Amphistomum
spp. in the rumen. One hundred and thirty-three (42.2%) of the abattoir-
examined cattle harboured one, two or all three trematodes. Of 133 cattle, 50
were randomly selected for worm and egg counts. The mean numbers (^ SD) of
Amphistomum, Schistosoma and Fasciola were 622.08 (^ 97.87), 33.68 (^ 7.44) and
19.46 (^ 4.58), respectively. A total of 32% harboured all the three trematodes,
66% had F. gigantica and Amphistomum spp. infections, 52% had Schistosoma spp.
and Amphistomum spp. infections while 32% had F. gigantica and Schistosoma
infections. A positive correlation (P ¼ 0.014) was found between F. gigantica and
Amphistomum worm burdens. There were no correlations between Amphistomum
and Schistosoma worm burdens and between F. gigantica and Schistosoma worm
burdens. It may be concluded that there is no significant cross-protection among
these trematodes in cattle in endemic areas.
helminth diseases hampering the productivity of dom-
2001). Fasciola gigantica, Schistosoma mattheei and Amphis-
tomum spp. are the most common trematodes in Zambia
(De Bont et al., 1994; Phiri et al., 2006a). Mixed infections
with different trematode species are common since
infectionsare economically important
they share the same intermediate snail host and/or
similar transmission sites (Pfukenyi et al., 2005; Keyyu
et al., 2006; Phiri et al., 2006a).
Heterologous resistance between
in several experimental and farm animals (Hillyer, 2005).
Previous reports have demonstrated that F. hepatica and
Schistosoma mansoni cross-protect against each other in
mice, causing a reduction in worm burden and/or egg-
producing capacity (Hillyer, 1984). Likewise, cattle
infected with Schistosoma bovis were shown to acquire an
enhanced resistance to challenge Fasciola spp. infection
*Fax: þ 260-01-291190
Journal of Helminthology (2008) 82, 373–376 doi:10.1017/S0022149X08054904
and vice versa (Haroun & Hillyer, 1986; Yagi et al., 1986).
An enhanced resistance against F. hepatica and F. gigantica
after primary infection with S. bovis has been described in
cattle (Sirag et al., 1981; Yagi et al., 1986) and sheep
(Monrad et al., 1981). Similarly, a primary infection of
F. gigantica in calves resulted in enhanced resistance to
challenge S. bovis, with a 94.2% reduction in worm count
(Yagi et al., 1986). These findings imply that these two
trematodes may be susceptible to the same or similar
immune responses (Spithill et al., 1999) and may have
common antigens (Rodriguez-Osorio et al., 1993).
Studies on concurrent naturally acquired infections of
Fasciola, Schistosoma and Amphistomum in cattle are lacking.
Since concurrent trematode infections may influence the
epidemiology of individual fluke populations, it was
desirable to study the dynamics of these trematode
infections and their relationships in cattle in endemic
areas. Therefore, objectives of this study were to deter-
mine the occurrence and extent of concurrent F. gigantica,
Schistosoma spp. and Amphistomum spp. infections in
free-ranging cattle in Zambia, and to investigate their
Materials and methods
This study was carried out at Turn Pike abattoir, located
60 km south of Lusaka. The local cattle came from areas
where worm control is not routinely practised. A total of
315 cattle presented for slaughter were examined from
June 2005 to July 2006 for worms of F. gigantica in the liver,
Schistosoma spp. in mesenteric blood veins, and Amphis-
tomum spp. in the rumen. Worm and faecal egg counts
were determined from 50 randomly selected trematode-
Fasciola and Amphistomum eggs were detected and
quantified by the sieving and sedimentation technique
as described by Taira et al. (1983). Schistosoma faecal
egg counts were determined using a modification of
the concentration technique by Lawrence (1970). Each
Schistosoma egg counted represented 10 eggs per gram
(De Bont et al., 1995).
The intestine was isolated and mesenteries were spread
out for thorough examination of mesenteric veins for
schistosomes. The rumen was opened and washed lightly
with tap water to expose amphistomes. Schistosomes
were counted in situ in the abattoir, while amphistomes
were picked from the mucosa of the whole rumen using
tissue forceps, and counted. Sharp incisions were made
on the liver surface, through major bile ducts and into the
parenchyma to expose liver flukes. To determine liver
fluke burden, liver dissections were done as described by
Phiri et al. (2006b).
Data of faecal egg counts (EPG) and worm counts from
sampled animals were log transformed (count þ1) to
stabilize variances. Trematode frequencies were calcu-
lated using SPSS version 11.0 for Windows (SPSS
Institute, Chicago, Illinois, USA). Chi-square was used
to determine differences in worm burdens and faecal egg
counts among the three trematodes. Pearson’s correlation
coefficient and linear regression were used to determine
and describe relationships among the three trematodes.
A significant relationship was denoted by a P value of
less than 0.05.
Of 315 cattle presented for slaughter, 133 were positive
for at least one trematode infection. From these, 50
animals were randomly selected for further studies.
Coproscopy (n ¼ 50)
On coproscopic examination, 58% were positive for
fascioliasis, 76% for amphistomiasis, 22% for schistoso-
miasis and 20% were positive for Schistosoma miracidia.
Faecal egg counts varied throughoutthe study period, but
ranged from 0 to 95 with a mean (^ SEM) of 8.02 ^ 2.23
for F. gigantica, 0–90 with a mean (^ SEM) of 7.0 ^ 2.42
for Schistosoma species and 0–183 with a mean (^ SEM)
of 17.7 ^ 4.49 for Amphistomum species. A positive
correlation (r ¼ 0.560, P , 0.001) was obtained between
F. gigantica and Amphistomum EPG.
At meat inspection, 68% of the 50 randomly selected
trematode-infected cattle were positive for fascioliasis,
56% for schistosomiasis and 92% were positive for
amphistomiasis. The range of individual worm burdens
was wide and there were variations in worm burdens
among the three trematodes (table 1). Heavy worm
burdens characterized Amphistomum infections, of which
48% of the Amphistomum infected cattle (n ¼ 46) har-
boured more than 500 amphistomes. Low worm burdens
characterized Schistosoma infections, of which 68% of the
Schistosoma infected cattle (n ¼ 28) harboured fewer than
100 worms in the mesenteric blood vessels.
Mixed trematode infections were common, of which
32% of the 50 randomly selected trematode-infected cattle
harboured all three trematodes. Fasciola gigantica and
Amphistomum dual infections were the highest (34%)
while F. gigantica and Schistosoma dual infections were
the lowest (0%). Schistosoma and Amphistomum dual
Table 1. Fasciola gigantica, Schistosoma spp. and Amphistomum spp.
worm burdens in 50 randomly selected trematode-infected cattle
from the Kafue and Zambezi river basins of Zambia.
Trematode species Worm burden, rangeMean ^ SEM
19.46 ^ 4.58
33.68 ^ 7.44
622.08 ^ 97.87
J. Yabe et al.
infections were represented by 20%. Only 6% of sampled
animals had Amphistomum, 2% F. gigantica and 4%
Schistosoma single infections.
Interactions among trematodes
Apositive correlation(r2¼ 0.12,P ¼ 0.014)was
obtained between F. gigantica and Amphistomum worm
counts (fig. 1), and also between F. gigantica worm
burden and Amphistomum faecal egg counts (r2¼ 0.338,
P , 0.001).
There were no correlations (r2¼ 0.022, P ¼ 0.302)
between Amphistomum and Schistosoma worm burdens
and between F. gigantica and Schistosoma worm burdens
(r2¼ 0.015, P ¼ 0.390).
This study has revealed, for the first time, the presence
and extent of fascioliasis, schistosomiasis and amphi-
stomiasis concurrent infections in cattle in Zambia,
based on both egg and worm counts. Our observation
of concurrent F. gigantica and Amphistomum species
infections is in agreement with earlier reports in Zambia
(Phiri et al., 2006a) and elsewhere (Szmidt-Adjide et al.,
2000; Pfukenyi et al., 2005; Keyyu et al., 2006). This finding
demonstrates that interactive infections between these
two trematodes are mutually inclusive. Phiri et al. (2006a)
recorded a positive correlation (r2¼ 0.043) between
F. gigantica and Amphistomum species using faecal egg
counts.Our study, however,
correlation (r2¼ 0.120) between these two trematodes
using worm burdens. Worm burden may therefore be
a better parameter for determining the relationship
between these two trematodes than EPG, as pathophy-
siological changes in the host may result in fluctuations
in faecal egg outputs (Boray, 1969). Faecal egg counts
may also be influenced by the amount of faeces produced
per day, time of day of faecal sampling, low sensitivity of
coproscopic techniques and other factors. Moreover,
acquisition of immunity by cattle in chronic infections
may depress egg output (Bitakaramire, 1973).
Although an increase in F. gigantica worm burden
was associated with an increase in Amphistomum worm
burden, differences in their worm burdens could be due
to the density and uptake of the specific metacercariae
by the host and/or the specific development of metacer-
cariae in the definitive host (Szmidt-Adjide et al., 2000).
Despite scarcity of reports on economic effects of
amphistomiasis in cattle, the heterologous interaction
of Amphistomum and F. gigantica may compound the
economical effects of liver flukes to the livestock industry.
These effects could be induced by the combined patho-
logy caused by individual
especially by immature flukes in young animals.
Although Schistosoma and Amphistomum spp. co-joint
infections were common, there was no significant
relationship between these trematodes. This may be
attributed to possible simultaneous exposure of cattle to
both trematodes in endemic areas and other unknown
factors. Knowles & Jones (1989) observed that concurrent
Calicophoron microbothrium and Schistosoma bovis infection
might occur in the snail Bulinus tropicus, given that
B. tropicus is an intermediate host for both trematodes.
As a result of the above, it may be difficult to observe
the relationship between these trematodes in cattle in
endemic areas where both parasites may become esta-
blished in the definitive host at the same time.
In this study, few animals harboured both F. gigantica
and Schistosoma worms. Since both trematodes cause
significant liver pathology (Ferreras et al., 2000; Phiri
et al., 2006b), when one infection is established, it may
exclude the other from establishing. Almeida et al. (2003)
demonstrated that sheep vaccinated against rSm14 were
significantly protected against challenge infections with
F. hepatica metacercariae, and were completely free of
histopathological hepatic damage related to liver fluke
infections. Although the correlation coefficient between
the two trematodes in our study was negative, the
relationship was not significant (P ¼ 0.390). In experi-
mental studies, primary infection with Schistosoma or
Fasciola species in ruminants has been reported to
result in enhanced resistance to heterologous challenge
(Bushara et al., 1978; Sirag et al., 1981; Yagi et al., 1986;
Ferreras et al., 2000; Almeida et al., 2003). Our findings
however, were not conclusive, since this study was done
in naturally infected cattle from endemic areas with no
known duration of infections. It was not possible to
determine which trematode infected the host first, or the
sequence of subsequent infections. Possible simultaneous
exposure of cattle to both trematodes in endemic areas
could have contributed to our failure to assess the effects
of co-joint infections on their worm burdens and egg
In conclusion, for control programmes of trematodes to
be effective in endemic areas, their design must consider
the existence of concurrent infections. It is difficult to
conclude on the relationship among and between those
trematodes in natural infections. The number of cattle in
this study is relatively low, especially considering the
Fig. 1. Positive correlation (r2¼ 0.12) between Fasciola gigantica
and Amphistomum worm burdens in cattle from Kafue and
Zambezi river basins of Zambia.
Concurrent infections of Fasciola, Schistosoma and Amphistomum spp. in cattle
high trematode prevalence ratio in the study area.
Experimental studies on concurrent Fasciola and Amphis-
tomum, and Schistosoma and Amphistomum infections may
also give a clear explanation on interactions of these
trematodes in cattle.
We thank the VLIR-UNZA IUC Program for funding
this study and Professor S. Siziya for his assistance with
statistics and data analysis. Technical assistance by
Mr M. Masuku and Mr D.S. Banda is acknowledged.
We also thank the University of Zambia School of
Veterinary Medicine for facilitating this study and Turn
Pike abattoir management for their cooperation.
Almeida, M.S., Torloni, H., Lee-Ho, P., Villar, M.M.,
Taumaturgo, N., Simpson, A.J. & Tendler, M. (2003)
Vaccination against Fasciola hepatica infection using a
Schistosoma mansoni defined recombinant antigen,
Sm14. Parasite Immunology 25, 135–137.
Bitakaramire, P.K. (1973) Preliminary studies on the
immunization of cattle against fasciolosis using
gamma-irradiated metacercariae of Fasciola hepatica.
pp. 465–525 in Dalton, J.P. (Ed.) Fasciolosis. Wall-
ingford, UK, CABI Publishing.
Boray, J.C. (1969) Experimental fasciolosis in Australia.
Advances in Parasitology 7, 95–209.
Bushara, H.O., Hussein, M.F., Saad, A.M., Taylor, M.G.,
Dargie, J.D., Marshall, T.F. de C, & Nelson, G.S.
(1978)Immunization of calves against Schistosoma bovis
using irradiated cercaria or schistosomula of S. bovis.
Parasitology 77, 303–311.
De Bont, J., Vercruysse, J., Southgate, V.R., Rollinson, D.
& Kaukas, A. (1994) Cattle schistosomiasis in Zambia.
Journal of Helminthology 68, 295–299.
De Bont, J., Vercruysse, J., Sabbe, F., Southgate, V.R. &
Rollinson, D. (1995) Schistosoma mattheei infections in
cattle: changes associated with season and age.
Veterinary Parasitology 57, 299–307.
Perez-Martinez, C., Mizinska, Y., Romajo, V., Gonzalez-
Lanza, M.C., Escudero, A. & Garcia-Marin, J.F. (2000)
Histopathological and immunohistochemical study of
lambs experimentally infected with Fasciola hepatica and
Schistosoma bovis. Journal of Veterinary Medicine B 47,
Haroun, E.M. & Hillyer, G.V. (1986) Resistance to
fasciolosis – a review. Veterinary Parasitology 20, 63–93.
Hillyer, G.V. (1984) Immunity to schistosomes using
heterologous trematode antigens. Veterinary Parasitology
Hillyer, G.V. (2005) Fasciola antigens as vaccines against
fasciolosis and schistosomiasis. Journal of Helminthology
Keyyu, J.D., Kassuku, A.A., Msaliwa, L.P., Monrad, J. &
Kyvsgaard, N.C. (2006) Cross-sectional prevalence
of helminth infections in cattle of traditional, small
scale and large scale dairy farms in Iringa district,
Knowles, R.J. & Jones, A. (1989) The influence of
Calicophoron microbothrium on the susceptibility of B.
tropicus to Schistosoma bovis. Parasitological Research 75,
Lawrence, J.A. (1970) Examination of ruminal faeces
for schistosome eggs. Rhodesia Veterinary Journal 1,
Monrad, J., Christensen, N.O., Nansen, P. & Frandsen, F.
(1981) Resistance to Fasciola hepatica in sheep harbour-
ing primary Schistosoma bovis infections. Journal of
Helminthology 55, 261–271.
Pfukenyi, D.M., Mukaratirwa, S., Willingham, A.L. &
Monrad, J. (2005) Epidemiological studies of amphis-
tome infections in cattle in the highveld and lowveld
communal grazing areas of Zimbabwe. Onderstepoort
Journal of Veterinary Research 72, 67–86.
Phiri, A.M., Phiri, I.K. & Monrad, J. (2006a) Prevalence
of amphistomiasis and its association with Fasciola
gigantica infections in Zambian cattle from communal
grazing areas. Journal of Helminthology 80, 65–68.
& Monrad, J. (2006b) Comparative fluke burden and
pathology in condemned and non-condemned cattle
livers from selected abattoirs in Zambia. Onderstepoort
Journal of Veterinary Research 73, 275–281.
Rodriguez-Osorio, M., Gomez-Garcia, Vi., Rojas-Gon-
zalez, J., Romajo-Martin, V., Manga-Gonzalez, Y. &
Gonzalez-Lanza, C. (1993) Resistance to Schistosoma
bovis in sheep induced by an experimental Fasciola
hepatica infection. Journal of Parasitology 72, 223–225.
Sirag, S.B., Christensen, N.O., Nansen, P., Monrad, J. &
Frandsen, F. (1981) Resistance of Fasciola hepatica in
calves harbouring primary patent Schistosoma bovis
infection. Journal of Helminthology 55, 63–70.
Spithill, T.W., Smooker, P.M. & Bruce, C.D. (1999)
Fasciola gigantica: Epidemiology, control, immunology
and molecular biology. pp. 465–525 in Dalton, J.P. (Ed.)
Fasciolosis. Wallingford, UK, CABI Publishing.
Szmidt-Adjide, V., Abrous, M., Adjide, C.C. & Drey-
fuss, G. (2000) Prevalence of Paramphistomum daubney
in central France. Veterinary Parasitology 87, 133–138.
Taira, R., Suzuki, K. & Boray, J.C. (1983) Detection and
quantification of Fasciola eggs in cattle using the Beads
technique. Japanese Journal of Veterinary Parasitology 32,
Vercruysse, J. & Claerebout, E. (2001) Treatment vs. non-
treatment of helminth infections in cattle: defining the
thresholds. Veterinary Parasitology 98, 195–214.
Yagi, A.I., Younis, S.A., Haroun, E.M., Gameel, A.A.,
Bushara, H.O. & Taylor, M.G. (1986) Studies on
heterologous resistance between Schistosoma bovis and
Helminthology 60, 55–59.
(Accepted 2 July 2008)
First Published Online 15 October 2008
q 2008 Cambridge University Press
J. Yabe et al.