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TRADITION AND MODERNITY IN VETERINARY MEDICINE, 2020, vol. 5, No 1(8): 29–32
HEAVY METALS ACCUMULATION IN THE SYSTEM RATTUS
NORVEGICUS – HYMENOLEPIS DIMINUTA FROM INDUSTRIAL AREA IN
BULGARIA
Ivelin Vladov, Veselin Nanev, Margarita Gabrashanska
Institute of Experimental Morphology, Pathology and Anthropology with Museum, Bulgarian
Academy of Sciences, Sofia, Bulgaria
E-mail: iepparazit@yahoo.com
ABSTRACT
Rat intestinal parasites have attracted great interest as bioindicators for environmental quality since they
can bioconcentrate several heavy metals to much higher concentrations than the tissues of the hosts. Our aim
was to assess the potential of the cestode Hymenolepis spp. as a bioindicator for heavy metal pollution in an
industrial area of the town of Maglizh, Bulgaria. The level of Zn, Mn, Cu, Pb and Cd was detected in the livers
of rats and in the cestode. A bioconcentration factor (BF), Concentration parasite/Concentration liver, was de-
termined.
A high BF was observed for Cd, Pb and Mn. The results revealed that Hymenolepis spp. has much great
ability to bioaccumulate heavy metals compared with their final hosts. Therefore, the system Rattus norvegicus-
Hymenоlepis spp. could be a very useful tool for environmental monitoring of the terrestrial areas.
Key words: heavy metals, rat, Hymenolepis spp.
Introduction
The helminths may act as bioindicators of pollution with heavy metals in their environment.
A high accumulation potential of different parasite taxa were identified as useful sentinels for chem-
ical pollution. Parasites are often able to take up metals at much higher levels and can bioconcentrate
pollutants presented in very low concentrations in the environment (Sures et al, 2017). Many studies
have showed that fish acanthocephalans, cestodes and nematodes have high capacity to accumulate
Cu, Pb, Cd and Mn (Sures et al, 1999, Gabrashanska and Nedeva, 1996). Few studies have been
done on the bioaccumulation of heavy metals in helminths from terrestrial animals (Sures et al, 2017;
Jankovska et al. 2008). Some endoparasites in mammals have the capacity to accumulate toxic met-
als much higher than their hosts living in polluted areas (Lotfy et al, 2013). The widespread wild
rats are frequently infected with cestodes which are the most abundant gastrointestinal parasites
(Teimoori et al. 2014). The common host-parasite system Rattus norvegicus/ Hymenolepis diminuta
was used in our study on the pollutants in an industrial area.
Our aim was to assess the potential of the cestode Hymenolepis spp. as a bioindicator for heavy
metal pollution in an industrial area of the town of Maglizh, Bulgaria. The level of Zn, Mn, Cu, Pb
and Cd was detected in the livers of rats and in the cestode. A bioconcentration factor (BF) (Con-
centration parasite/Concentration liver) was determined.
Materials and methods
Collection of rats and isolation of cestode. 21 adult rats (Rattus norvegicus) were captured
using traps placed in the selected area near the town of Maglizh, Bulgaria. Rats infected only with
cestodes (12 numbers) and those without any parasites (6 numbers) were investigated. The rest rats
30 Ivelin Vladov, Veselin Nanev, Margarita Gabrashanska
were with a mixed infection and were excluded from the study. Their livers were removed and stud-
ied for heavy metal content. The most abundant endohelminth in the captured rats was Hymenolepis
diminuta (Cestoda). The levels of Zn, Mn, Cd, Cu and Pb were determined in the liver of rats (in-
fected with H. diminuta and non-infected) and in the tissue of H. diminuta. Metal analysis was done
by ICP – OES Prodigy 7 Teledyne Leeman Labs, USA. The bioconcentration factor of heavy metals
in helminths was calculated according to the formula proposed by Sures et al (1999). A bioconcen-
tration factor (BF) – Concentration parasite/Concentration liver was used.
Results
The results for the level of heavy metals in rats (non-infected or infected with H. diminuta)
and tapeworm are presented in graph (microg/g)
T he r esu lts fo r th e le ve l o f h ea vy m eta ls in r ats
(no n -in fe cted o r infe cte d w it h H . d im in uta )
L o g 1 0
N o n - in f e c te d In f e c te d H y m e no le p is
d im in u ta
0.1
1
10
100
1000 C d
Mn
Pb
Zn
C u
The average concentration of the above metals in the studied host-parasite system was in de-
scending order as follows:
Non-infected rats Zn > Cu > Pb > Mn > Cd
Infected rats Zn > Cu > Pb > Mn > Cd
H. diminuta Zn > Pb > Cu > Mn > Cd
The BFs were as follows Zn – 2.01; Cu – 1.39; Pb – 2.30; Cd – 1.21; Mn – 2.32.
Taking in consideration that cestodes are more abundant in terrestrial mammals than are acan-
thocephalans (and thus potentially more useful in passive as well as active biomonitoring) we opted
for a common animal rat and its common tapeworm H. diminuta to be used in our study. Tapeworms
decreased only the level of Cu, Pb and Zn. The tapeworm can accumulate Pb, Zn and Mn in high
extend. The effect of the tapeworm presence on the bioaccumulation some heavy metals in the host
tissue liver can serve as an important tool in monitoring environmental pollution.
Heavy metals accumulation in the system rattus norvegicus – hymenolepis diminuta … 31
Discussion
The present results revealed there were significant differences in the levels of studied metals
between infected and non-infected rats well as between cestodes and their hosts. The concentration
of Cd, Pb, Zn, were lower in the non-infected rats compared with infected. The content of Mn was
similar in the infected and un-infected hosts. The concentration of Cd, Pb, Zn, Mn were signifi-
cantly higher in cestodes than those in their host. These findings may indicate the possibility of the
cestodes Hymenolepis diminuta can accumulate some metals and are suitable species as bioindica-
tors for environmental pollution with the metals. Our results are agreed with those of previous stud-
ies (Sures et al 2017, Cadkova et al. 2014; Jankovska et al. 2008; Gabrashanska and Nedeva 1996).
The mechanism whereby cestode-infected animals accumulate less heavy metals than parasite-free
ones is not known. It may be due to their lower metabolic activities or due to a fact that the tape-
worms and acanthocephalus (Cestoda and Acanthocephala) are lacking digestive tracts and using
their teguments for absorbing substances from the host digestive tract (Jankovska et al. 2008).
The higher bioaccumulation factors in heavy metals exposed tapeworms observed in our study
are in good agreement with the previous field studies (Jankovska et al. 2008). The studies showed
elevated tapeworm BF-s in animals living in polluted areas (Cadkova et al.2014). Our studies sup-
port the hypothesis that cestodes with a relatively large absorbance surface have reached high BF-s.
It is known that cestodes take up bile salts produced in the liver through the hepatic intestinal
cycle and use them for their eggs formation (Jankovska et al. 2008). According Sures (2003) and
Jankovska et al (2008) the mechanism which enables cestodes to absorb metals from the host intes-
tinal lumen is the presence of bile acids, forming organo-metallic complexes, that are easily absorbed
by the worms due to their lipophilicity.
Our results revealed that the concentration of some heavy metals in the infected hosts are lower
than those found in non-infected hosts. The high BF-s in Hymenolepis diminuta proposed that these
tapeworms have the ability to remediate some toxic metals from their hosts. Basing on the results
we conclude that some intestinal cestodes could be used as a bioremediation tool by absorbing the
heavy metals from their hosts as well as they be used as bioindicators of pollution in their environ-
ment. Data about the level of heavy metals in the surface water slightly exceed the limits of level of
Mn, Zn, Cd, Pb but not that of Cu in the studied area (Kovacheva et al. 2019). According the above
authors detected level of Zn was 0.106, of Cd - 0.118 and of Pb – 155 mg/l. The host -cestode
system Rattus norvegicus/ Hymenoleps diminuta reflected
Conclusion
Concentrations of heavy metals around a town located near to a plant were determined in sub-
web a host-parasite system Rattus norvegicus – Hymenoleps diminuta. A high ratio C parasite/C
host was indicative of acute pollutant exposure or long/chronic exposure of the pollutant correlated
with high concentration in both the host and parasite. Parasite infections have been attributed to
man-made impact and environmental changes in terrestrial habitat. The position of parasite as a
trophic consumer can infer details about the chemical state of the environment as a consequence of
food web biomagnifications. The host-helminth system wild rat/H. diminuta reflects the content of
heavy metals in the terrestrial environment and could be used as a bioindicator for heavy metal
pollution. The content of toxic metals is lower in the infected hosts. The high BF-s for Pb, Mn, Cd
and Zn indicates that even small amount of metals in the environment may result in significant
32 Ivelin Vladov, Veselin Nanev, Margarita Gabrashanska
uptake by the tapeworms. Despite the fact that almost of heavy metal values may not indicate a
severe risk of toxic effects on wildlife but after a long period of time could exert an impact on
individuals, communities and ecosystems in the studied area.
Aknowledgements
This work was financially supported by the Bulgarian Ministry of Education and Science, FNI,
DN14-7/2017.
References
1. Cadkova Z., Miholova D, Szakova J, Valeki P, Jankovska I, Langrova I. (2014). Is the tapeworm
able to affect Pb- concentration in white rat? Parasitology. 141. 826–836.
2. Gabrashanska M., I. Nedeva. (1996). Content of heavy metals in the system fish-cestodes. EMOP.
Parasitologia: 3858–61.
3. Jankovska I., LangrovaI, Bejcek V., Miholova D., Vadlejch J., Petrtyl M. (2008). Heavy metal ac-
cumulation small terrestrial rodents infected by cestodes and nematodes. Parasite. 15: 581–588.
4. Kovacheva A., I. Vladov, M. Gabrashanska, D. Rabadjieva, S. Tepavitcharova, R. Ilieva, V. Nanev.
(2019). Dynamics of trace metals in the system water-soil-low vegetation-small animals-parasites
in the Maglizh area. Bulgaria 7th International Symposium Federation of European Societies on
Trace Elements and Minerals (FESTEM) together with 35th Annual GMS Meeting, Potsdam, Ger-
many.
5. Lotfy W., M. Ezz, A. Hassan. (2013). Bioaccumulation of some heavy metals in the liver flukes
Fasciola hepatica and Fasciola gigantica. Iranian Journal of Parasitology. 8 (4): 552–558.
6. Sures B., Siddall R., Taraschewski H. (1999). Parasites as accumulation indicators of heavy metal
pollution. Parasitology Today. 15 (1): 16–21.
7. Sures B. (2003). Accumulation of heavy metals by intestinal helminthes in fish: an overview and
perspectiva. Parasitology. 126 (7): S53–S60.
8. Sures B. (2004). Environmental parasitology: relevancy of parasites in monitoringenvironmen-
tal pollution. Trends in Parasitology. 20 (4): 170-177.
9. Sures B., Nachev M., Selbach C., Marcogliese D. (2017). Parasite responses to pollution: what we
know and where we go in “Environment Parasitology”. Parasites and Vectors. 10: 65–83.
10. Teimoori S., Yaraghi A., Makki M., Shahbazi F., Nazmara S., Rokni M., Mesdaghinia A., Moghad-
dam A., Hosseini M., Rakhshanpour A., Mowlavi G. (2014). Heavy metal absorption capacity of
intestinal helminthes in urban rats. Iranian J of Public Health, 43 (3): 310–315.
