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Is the tapeworm able to affect tissue Pb-concentrations in white rat?

Published online by Cambridge University Press:  06 February 2014

ZUZANA ČADKOVÁ ,
DANIELA MIHOLOVÁ ,
JIŘINA SZÁKOVÁ ,
PETR VÁLEK ,
IVANA JANKOVSKÁ  and
IVA LANGROVÁ
ZUZANA ČADKOVÁ*
Affiliation:
Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 957, Prague 6, 165 21, Czech Republic
DANIELA MIHOLOVÁ
Affiliation:
Department of Chemistry, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 957, Prague 6, 165 21, Czech Republic
JIŘINA SZÁKOVÁ
Affiliation:
Department of Agroenvironmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 957, Prague 6, 165 21, Czech Republic
PETR VÁLEK
Affiliation:
Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 957, Prague 6, 165 21, Czech Republic
IVANA JANKOVSKÁ
Affiliation:
Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 957, Prague 6, 165 21, Czech Republic
IVA LANGROVÁ
Affiliation:
Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 957, Prague 6, 165 21, Czech Republic
*
* Corresponding author. Department of Zoology and Fisheries, FAFNR, CULS Prague; Kamycka 957, Prague 6, 165 21, Czech Republic. E-mail: [email protected]
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Summary

The effect of gastrointestinal helminths on Pb accumulation in the host body is ambiguous. A laboratory experiment with Rattus norvegicus/Hymenolepis diminuta model was conducted to determine Pb toxicokinetics in a terrestrial host-parasite system. The ET-AAS or ICP–OES techniques were used to determine Pb concentrations (CPb) in both tapeworms and host tissues (kidney, liver, bone, testes, muscle and intestinal wall). Concerning the entire host-parasite system, the highest CPb were detected in H. diminuta. Rat kidneys and bone were the only two tissues whose mean Pb levels were lower in parasitized animals than they were in non-infected subjects after both levels of exposure. At low Pb exposure, parasitization slightly changed the Pb toxicokinetics in the host body. However, with respect to tissue at the same exposure level, no significant differences were detected between the parasitized and non-parasitized animals and no significant correlations were found between CPb in tapeworms and those of host tissues. The results of this study indicate that H. diminuta does not protect rat from elevated Pb exposure even if tapeworm accumulates a higher portion of ingested Pb dose compared with that of the most Pb-loaded host soft tissue. The portion of Pb dose accumulated in H. diminuta correlates positively with parasite biomass.

Keywords

Hymenolepis diminutatissue Pb levelsPb oral exposurebioaccumulationPb toxicokineticsheavy metalsbioconcentration factor
Type
Research Article
Information
Parasitology , Volume 141 , Issue 6 , May 2014 , pp. 826 - 836
Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Azmat, R., Fayyaz, S., Kazi, N., Mahmood, S. J. and Uddin, F. (2008). Natural bioremediation of heavy metals through nematode parasite of fish. Biotechnology 7, 139–143. doi: 10.3923/biotech.2008.139.143.Google Scholar
Barton, J. C., Conrad, M. E., Harrison, L. and Nuby, S. (1978 a). Effects of calcium on the absorption and retention of lead. Journal of Laboratory and Clinical Medicine 91, 366–376.Google Scholar
Barton, J. C., Conrad, M. E., Nuby, S. and Harrison, L. (1978 b). Effects of iron on the absorption and retention of lead. Journal of Laboratory and Clinical Medicine 92, 536–547.Google Scholar
Baruš, V., Tenora, F. and Kračmár, S. (2000). Heavy metal (Pb, Cd) concentrations in adult tapeworms (Cestoda) parasitizing birds (Aves). Helminthologia 37, 131–136.Google Scholar
Baudrimont, M. and De Montaudouin, X. (2007). Evidence of an altered protective effect of metallothioneins after cadmium exposure in the digenean parasite-infected cockle (Cerastoderma edule). Parasitology 134, 237–245. doi: 10.1017/S0031182006001375.Google Scholar
de Buron, I., James, E., Riggs-Gelasco, P., Ringwood, A. H., Rolando, E. and Richardson, D. (2009). Overview of the status of heavy metal accumulation by helminths with a note on the use of in vitro culture of adult acanthocephalans to study the mechanisms of bioaccumulation. Neotropical Helminthology 3, 101–110.Google Scholar
Dwinell, M. B., Bass, P., Schaefer, D. M. and Oaks, J. A. (1997). Tapeworm infection decreases intestinal transit and enteric aerobic bacterial populations. American Journal of Physiology. Gastrointestinal and Liver Physiology 273, G480–G485.Google Scholar
Jankovska, I., Langrova, I., Bejcek, V., Miholová, D., Vadlejch, J. and Petrtyl, M. (2008). Heavy metal accumulation in small terrestrial rodents infected by cestodes or nematodes. Parasite 15, 581–588.Google Scholar
Jankovská, I., Miholová, D., Langrová, I., Bejček, V., Vadlejch, J., Kolihová, D. and Šulc, M. (2009). Influence of parasitism on the use of small terrestrial rodents in environmental pollution monitoring. Environmental Pollution 157, 2584–2586. doi: 10.1016/j.envpol.2009.04.008.Google Scholar
Jankovska, I., Vadlejch, J. and Szakova, J. (2010 a). Experimental studies on the lead accumulation in the cestode Moniezia expansa (Cestoda: Anoplocephalidae) and its final host (Ovis aries). Ecotoxicology 19, 928–932. doi: 10.1007/s10646-010-0474-3.Google Scholar
Jankovska, I., Miholova, D., Bejcek, V., Vadlejch, J., Sulc, M., Száková, J. and Langrová, I. (2010 b). Influence of parasitism on trace element contents in tissues of red fox (Vulpes vulpes) and its parasites Mesocestoides spp. (Cestoda) and Toxascaris leonina (Nematoda). Archives of Environmental Contamination and Toxicology 58, 469–477. doi: 10.1007/s00244-009-9355-2.Google Scholar
Jankovska, I., Miholova, D., Lukesova, D., Kalous, L., Válek, P., Romočuský, Š., Vadlejch, J., Petrtýl, M., Langrová, I. and Čadková, Z. (2012). Concentrations of Zn, Mn, Cu and Cd in different tissues of perch (Perca fluviatilis) and in perch intestinal parasite (Acanthocephalus lucii) from the stream near Prague (Czech Republic). Environmental Research 112, 83–85. doi: 10.1016/j.envres.2011.11.003.CrossRefGoogle Scholar
Jirsa, F., Leodolter-Dvorak, M., Krachler, R. and Frank, C. (2008). Heavy metals in the nase, Chondrostoma nasus (L. 1758), and its intestinal parasite Caryophyllaeus laticeps (Pallas 1781) from Austrian rivers: bioindicative aspects. Archives of Environmental Contamination and Toxicology 55, 619–626. doi: 10.1007/s00244-008-9154-1.Google Scholar
Khaleghzadeh-Ahangar, H., Malek, M. and McKenzie, K. (2011). The parasitic nematodes Hysterothylacium sp. type MB larvae as bioindicators of lead and cadmium: a comparative study of parasite and host tissues. Parasitology 138, 1400–1405. doi: 10.1017/S0031182011000977.CrossRefGoogle ScholarPubMed
MacKenzie, K., Williams, H. H., Williams, B., McVicar, A. H. and Siddall, R. (1995). Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in Parasitology 35, 85–144.Google Scholar
Mader, P., Száková, J. and Miholová, D. (1998). Classical dry ashing of biological and agricultural materials. Part II. Losses of analytes due to their retention in an insoluble residue. Analusis 26, 121–129. doi: 10.1051/analusis:1998121.Google Scholar
Malek, M., Haseli, M., Mobedi, I., Ganjali, M. R. and Mackenzie, K. (2007). Parasites as heavy metal bioindicators in the shark Carcharhinus dussumieri from the Persian Gulf. Parasitology 134, 1053–1056. doi: 10.1017/S0031182007002508.Google Scholar
Mettrick, d. f. (1971). Hymenolepis-diminuta–pH changes in rat intestinal contents and worm migration. Experimental Parasitology 29, 386–401. doi: 10.1016/0014-4894(71)90048-8.Google Scholar
Morrison, J. N. and Quarterman, J. (1987). The relationship between iron status and lead absorption in rats. Biological Trace Element Research 14, 115–126. doi: 10.1007/BF02795602.Google Scholar
Nachev, M., Zimmermann, S., Rigaud, T. and Sures, B. (2010). Is metal accumulation in Pomphorhynchus laevis dependent on parasite sex or infrapopulation size? Parasitology 137, 1239–1248. doi: 10.1017/S0031182010000065.Google Scholar
Nachev, M., Schertzinger, G. and Sures, B. (2013). Comparison of the metal accumulation capacity between the acanthocephala Pomphorhynchus laevis and larval nematodes of the genus Eustrongylides sp. infecting barbel (Barbus barbus). Parasites and Vectors 6, 21. doi: 10.1186/1756-3305-6-21.Google Scholar
Nhi, T. T. Y., Mohd, S. N. A. and Faizah, S. H. (2013). Use of cestodes as indicator of heavy-metal pollution. Experimental Parasitology 133, 75–79. doi: 10.1016/j.exppara.2012.10.014.Google Scholar
Oros, M. and Hanzelova, V. (2009). Re-establishment of the fish parasite fauna in the Tisa River system (Slovakia) after a catastrophic pollution event. Parasitology Research 104, 1497–1506. doi: 10.1007/s00436-009-1356-6.Google Scholar
Oyoo-Okoth, E., Wim, A., Osano, O., Kraak, M. H. S., Ngure, V., Makwali, J. and Orina, P. S. (2010). Use of the fish endoparasite Ligula intestinalis (L., 1758) in an intermediate cyprinid host (Rastreneobola argentea) for biomonitoring heavy metal contamination in Lake Victoria, Kenya. Lakes & Reservoirs: Research & Management 15, 63–73.Google Scholar
Oyoo-Okoth, E., Admiraal, W., Osano, O., Kraak, M. H., Were-Kogogo, P. J., Gichuki, J., Ngure, V., Makwali, J. and Ogwai, C. (2012). Dynamics of metal uptake and depuration in a parasitized cyprinid fish (Rastrineobola argentea). Aquatic Toxicology 124, 34–40. doi: 10.1016/J.AQUATOX.2012.07.006.Google Scholar
Quadroni, S., Galassi, S., Capoccioni, F., Ciccotti, E., Grandi, G., De Leo, G. A. and Bettinetti, R. (2013). Contamination, parasitism and condition of Anguilla anguilla in three Italian stocks. Ecotoxicology 22, 94–108. doi: 10.1007/s10646-012-1006-0.Google Scholar
Retief, N. R., Avenant-Oldewage, A. and du Preez, H. (2006). The use of cestode parasites from the largemouth yellowfish, Labeobarbus kimberleyensis (Gilchrist and Thompson, 1913) in the Vaal Dam, South Africa as indicators of heavy metal bioaccumulation. Physics and Chemistry of the Earth 31, 840–847. doi: 10.1016/j.pce.2006.08.004.Google Scholar
Roepstorff, A. and Nansen, P. (1998). Epidemiology, Diagnosis and Control of Helminth Parasites of Swine. FAO Animal Health Manual, Rome, Italy.Google Scholar
Schludermann, C., Konecny, R., Laimgruber, S. and Sures, B. (2003). Fish macroparasites as indicators of heavy metal pollution in river sites in Austria. Parasitology 126S, S61–S69. doi: 10.1017/S0031182003003743.Google Scholar
Soliman, M. F. M. (2012). Heavy metal pollution across sites affecting the intestinal helminth communities of the Egyptian lizard, Chalcides ocellatus (Forskal, 1775). Environmental Monitoring and Assessment 184, 7677–7685. doi: 10.1007/s10661-012-2528-x.Google Scholar
StatSoft, Inc. (2009). STATISTICA (data analysis software system), version 9.0. http://www.statsoft.com.Google Scholar
Sures, B. (2004). Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology 20, 170–177. doi: 10.1016/j.pt.2004.01.014.Google Scholar
Sures, B. and Siddall, R. (1999). Pomphorhynchus laevis: the intestinal acanthocephalan as a lead sink for its fish host, chub (Leuciscus cephalus). Experimental Parasitology 93, 66–72. doi: 10.1006/expr.1999.4437.Google Scholar
Sures, B. and Siddall, R. (2001). Comparison between lead accumulation of Pomphorhynchus laevis (Palaeacanthocephala) in the intestine of chub (Leuciscus cephalus) and in the body cavity of goldfish (Carassius auratus auratus). International Journal for Parasitology 31, 669–673. doi: 10.1016/S0020-7519(01)00173-4.Google Scholar
Sures, B. and Siddall, R. (2003). Pomphorhynchus laevis (Palaeacanthocephala) in the intestine of chub (Leuciscus cephalus) as an indicator of metal pollution. International Journal for Parasitology 33, 65–70. doi: 10.1016/S0020-7519(02)00249-7.Google Scholar
Sures, B., Taraschewski, H. and Rokicki, J. (1997). Lead and cadmium content of two cestodes, Monobothrium wageneri and Bothriocephalus scorpii, and their fish hosts. Parasitology Research 83, 618–623. doi: 10.1007/s004360050307.Google Scholar
Sures, B., Jurges, G. and Taraschewski, H. (1998). Relative concentrations of heavy metals in the parasites Ascaris suum (Nematoda) and Fasciola hepatica (Digenea) and their respective porcine and bovine definitive hosts. International Journal for Parasitology 28, 1173–1178. 10.1016/S0020–7519(98)00105-2.Google Scholar
Sures, B., Siddall, R. and Taraschewski, H. (1999 a). Parasites as accumulation indicators of heavy metal pollution. Parasitology Today 15, 16–22.Google Scholar
Sures, B., Steiner, W., Rydlo, M. and Taraschewski, H. (1999 b). Concentrations of 17 elements in the zebra mussel (Dreissena polymorpha), in different tissues of perch (Perca fluviatilis), and in perch intestinal parasites (Acanthocephalus lucii) from the subalpine lake Mondsee, Austria. Environmental Toxicology and Chemistry 18, 2574–2579. doi: 10.1897/1551-5028(1999)018<2574:COEITZ><2574:COEITZ>2.3.CO;2.Google Scholar
Sures, B., Jurges, G. and Taraschewski, H. (2000). Accumulation and distribution of lead in the archiacanthocephalan Moniliformis moniliformis from experimentally infected rats. Parasitology 121, 427–433. doi: 10.1017/S003118209900654X.Google Scholar
Sures, B., Grube, K. and Taraschewski, H. (2002). Experimental studies on the lead accumulation in the cestode Hymenolepis diminuta and its final host, Rattus norvegicus . Ecotoxicology 11, 365–368. doi: 10.1023/A:1020561406624.Google Scholar
Sures, B., Dezfuli, B. S. and Krug, H. F. (2003 a). The intestinal parasite Pomphorhynchus laevis (Acanthocephala) interferes with the uptake and accumulation of lead (Pb-210) in its fish host chub (Leuciscus cephalus). International Journal for Parasitology 33, 1617–1622. doi: 10.1016/S0020-7519(03)00251-0.Google Scholar
Sures, B., Scheible, T., Bashtar, A. R. and Taraschewski, H. (2003 b). Lead concentrations in Hymenolepis diminuta adults and Taenia taeniaeformis larvae compared to their rat hosts (Rattus norvegicus) sampled from the city of Cairo, Egypt. Parasitology 127, 483–487. doi: 10.1017/S0031182003003901.Google Scholar
Teodorova, S., Metcheva, R. and Topashka-Ancheva, M. (2003). Bioaccumulation and damaging action of polymetal industrial dust on laboratory mice Mus musculus alba – I. Analysis of Zn, Cu, Pb, and Cd disposition and mathematical model for Zn and Cd bioaccumulations. Environmental Pollution 91, 85–94. doi: 10.1016/S0013-9351(02)00013-0.Google Scholar
Torres, J., de Lapuente, J., Eira, C. and Nadal, J. (2004). Cadmium and lead concentrations in Gallegoides arfaai (Cestoda: Anoplocephalidae) and Apodemus sylvaticus (Rodentia: Muridae) from Spain. Parasitology Research 94, 468–470. doi: 10.1007/s00436-004-1232-3.Google Scholar
Torres, J., Peig, J., Eira, C. and Borrás, M. (2006). Cadmium and lead concentrations in Skrjabinotaenia lobata (Cestoda: Catenotaeniidae) and in its host, Apodemus sylvaticus (Rodentia: Muridae) in the urban dumping site of Garraf (Spain). Environmental Pollution 143, 4–8. doi: 10.1016/j.envpol.2005.11.012.Google Scholar
Torres, J., Foronda, P., Eira, C., Miquel, J. and Feliu, C. (2010). Trace element concentrations in Raillietina micracantha in comparison to its definitive host, the feral pigeon Columba livia in Santa Cruz de Tenerife (Canary Archipelago, Spain). Archives of Environmental Contamination and Toxicology 58, 176–182. doi: 10.1007/s00244-009-9352-5.Google Scholar
Torres, J., Eira, C., Miquel, J., Foronda, P. and Feliu, C. (2011). Cadmium and lead concentrations in Moniliformis moniliformis (Acanthocephala) and Rodentolepis microstoma (Cestoda), and in their definitive hosts, Rattus rattus and Mus domesticus in El Hierro (Canary Archipelago, Spain). Acta Parasitologica 56, 320–324. doi: 10.2478/s11686-011-0064-4.Google Scholar
Vidal-Martinez, V. M., Pech, D., Sures, B., Purucker, T. and Poulin, R. (2010). Can parasites really reveal environmental impact? Trends in Parasitology 26, 44–51. doi: 10.1016/j.pt.2009.11.001.Google Scholar