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.

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Concurrent infections of Fasciola,
Schistosoma and Amphistomum spp. in
cattle from Kafue and Zambezi river basins
of Zambia
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
Merelbeke, Belgium:
Nationalestraat 155, B-2000, Antwerp, Belgium
2Clinical Studies
3Department of Parasitology, Faculty of
4Prince Leopold Institute of Tropical Medicine,
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 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.
Introduction
Trematode
helminth diseases hampering the productivity of dom-
esticatedruminantsworldwide(Vercruysse&Claerebout,
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
Fasciolaspeciesinconcurrentinfectionshasbeenobserved
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
Schistosoma and
*Fax: þ 260-01-291190
E-mail: miyabe@yahoo.com
Journal of Helminthology (2008) 82, 373–376 doi:10.1017/S0022149X08054904

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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
interactions.
Materials and methods
Study area
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-
infected cattle.
Parasitological examinations
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).
Worm counts
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).
Statistical analysis
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.
Results
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.
Worm burdens
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
Fasciola gigantica
Schistosoma spp.
Amphistomum spp.
1–176
1–186
2–2974
19.46 ^ 4.58
33.68 ^ 7.44
622.08 ^ 97.87
374
J. Yabe et al.

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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).
Discussion
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
recordeda stronger
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
production.
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
trematode populations,
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
375

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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.
Acknowledgements
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.
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