Environmental Science and Pollution Research

, Volume 25, Issue 35, pp 35464–35470 | Cite as

Effects of tapeworm infection on absorption and excretion of zinc and cadmium by experimental rats

  • Vladislav SloupEmail author
  • Ivana Jankovská
  • Jiřina Száková
  • Jan Magdálek
  • Simon Sloup
  • Iva Langrová
Research Article


The main objective of this study was to determine how rat tapeworms affect the excretion of zinc and cadmium through rat feces. Male rats (Rattus norvegicus var. alba) were divided into four groups, and the experiment was conducted over a 6-week period. The control groups (00; 0T) were provided with a standard ST-1 rodent mixture and received 10.5 mg of Zn/week. Groups P0 and PT were fed a mixture supplemented with the hyperaccumulating plant Arabidopsis halleri at a dosage of 123 mg Zn/week and 2.46 mg Cd/week. Groups 0T and PT were infected with the rat tapeworm (Hymenolepis diminuta). Fecal samples were collected 24 h post exposure. Zinc and cadmium concentrations in rat feces were analyzed using inductively coupled plasma optical emission spectrometry. Tapeworm presence decreased the amount of metals excreted through the feces of the host throughout the entire experiment, with the exception of 1 week (control group). No statistically significant differences between zinc excretion rates in the control groups (00 and 0T) were detected at any time throughout the experiment. A statistically significant difference between zinc excretion rates (p < 0.05) in the exposed groups (P0 and PT) was detected in 2 of the 6 monitored weeks. Group PT excreted significantly less cadmium (p < 0.01) than group P0 did in three of the 6 weeks. Overall, our results indicate that tapeworms are able to influence the excretion of metals by their host. Tapeworms accumulate metals from intestinal contents. It is not clear whether tapeworms carry out this process before the host tissues absorb the metals from the intestines or the tapeworms accumulate metals excreted from the body of the host back to the intestines. Most likely, it is a combination of both phenomena.


Zinc Cadmium Tapeworm Excretion Feces Rat Hyperaccumulators 



The authors gratefully acknowledge Brian Kavalir for his proofreading services.

Funding information

This study was supported by the University-wide internal grant agency of the Czech University of Life Sciences Prague (CIGA), project no. 20182005.

Compliance with ethical standards

All experiments with laboratory animals were conducted in compliance with the current laws of the Czech Republic Act No 246/1992 Coll. on the Protection of Animals against Cruelty.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abdulla M, Chmielnicka J (1989) New aspects on the distribution and metabolism of essential trace elements after dietary exposure to toxic metals. Biol Trace Elem Res 23:25–53. CrossRefGoogle Scholar
  2. Bayçu G, Gevrek-Kürüm N, Moustaka J, Csatári I, Rognes SE, Moustakas M (2017) Cadmium-zinc accumulation and photosystem II responses of Noccaea caerulescens to Cd and Zn exposure. Environ Sci Pollut Res 24:2840–2850. CrossRefGoogle Scholar
  3. Brand von T (1973) Biochemistry of parasites. Academic press, BethesdaGoogle Scholar
  4. Brody T (1998) Zinc and copper. Nutritional biochemistry. Academic Press, San DiegoGoogle Scholar
  5. Brown KH, Wuehler SE, Peerson JM (2001) The importance of zinc in human nutrition and estimation of the global prevalence of zinc deficiency. Food Nutr Bull 22:113–125. CrossRefGoogle Scholar
  6. Brožová A, Jankovská I, Miholová D, Scháňková Š, Truněčková J, Langrová I, Kudrnáčová M, Vadlejch J (2015) Heavy metal concentrations in the small intestine of red fox (Vulpes vulpes) with and without Echinococcus multilocularis infection. Environ Sci Pollut Res 22:3175–3179. CrossRefGoogle Scholar
  7. Brzóska MM, Moniuszko-Jakoniuk J (2001) Interactions between cadmium and zinc in the organism. Food Chem Toxicol 39:967–980. CrossRefGoogle Scholar
  8. Čadková Z, Száková J, Miholová D, Válek P, Pacáková Z, Vadlejch J, Langrová I, Jankovská I (2013) Faecal excretion dynamic during subacute oral exposure to different Pb species in Rattus norvegicus. Biol Trace Elem Res 152:225–232. CrossRefGoogle Scholar
  9. Cao J, Gao Z, Yan J, Li M, Su J, Xu J, Yan CHH (2016) Evaluation of trace elements and their relationship with growth and development of young children. Biol Trace Elem Res 171:270–274. CrossRefGoogle Scholar
  10. Chaney RL (2010) Trace elements in soils. In: Chaney RL (ed) Cadmium and zinc, School of Geography, Geology and the Environment. Kingston University, London, pp 409–439. CrossRefGoogle Scholar
  11. Chmielnicka J, Cherian MG (1986) Environmental exposure to cadmium and factors affecting trace-element metabolism and metal toxicity. Biol Trace Elem Res 10:243–262. CrossRefGoogle Scholar
  12. Chowdhury N, Singh R (1989) Distribution of zinc in parasitic helminths. J Helminthol 2:149–152. CrossRefGoogle Scholar
  13. Cikrt M, Tichý M (1974) Excretion of cadmium through bile and intestinal wall in rats. Br J Ind Med 31:134–139. CrossRefGoogle Scholar
  14. Das P, Samantaray S, Rout GR (1997) Studies on cadmium toxicity in plants: a review. Environ Pollut 98:29–36. CrossRefGoogle Scholar
  15. Decker CF, Byerrum RU, Hoppert CA (1957) A study of the distribution and retention of cadmium-115 in the albino rat. Arch Biochem 66:140–145CrossRefGoogle Scholar
  16. Elinder CG, Piscator M (1978) Cadmium and zinc relationships. Environ Health Perspect 25:129–132CrossRefGoogle Scholar
  17. Erdman JW Jr, MacDonald IA, Zeisel SH (2012) Present knowledge in nutrition, 10th edn. Wiley-Blackwell, Oxford, pp 1328CrossRefGoogle Scholar
  18. Ferguson LE, Gibson SR, Opare-Obisaw C, Ounpuu S, Lamba CH (1995) Dietary strategies for improving the zinc nutriture of rural, southern Malawian and Ghanaian children. Ecol Food Nutr 34:33–47. CrossRefGoogle Scholar
  19. Funk AE, Day FA, Brady FO (1987) Displacement of zinc and copper from copper-induced metallothionein by cadmium and by mercury: in vivo and ex vivo studies. Comp Biochem Physiol C Toxicol Pharmacol 86:1–6. CrossRefGoogle Scholar
  20. Godt J, Scheidig F, Grosse-Siestrup CH, Esche V, Brandenburg P, Reich A, Groneberg D (2006) The toxicity of cadmium and resulting hazards for human health. J Occup Med Toxicol 1(22):22. CrossRefGoogle Scholar
  21. Hesami R, Salimi A, Ghaderian SM (2018) Lead, zinc, and cadmium uptake, accumulation, and phytoremediation by plants growing around Tang-e Douzan lead–zinc mine, Iran. Environ Sci Pollut Res 25:8701–8714. CrossRefGoogle Scholar
  22. House WA, Welch RM, Van Campen DR (1982) Effect of phytic acid on the absorption, distribution, and endogenous excretion of zinc in rats. J Nutr 112:941–953. CrossRefGoogle Scholar
  23. Huguet S, Bert V, Laboudigue A, Barthès V, Isaure MP, Llorens I, Schat H, Sarret G (2012) Cd speciation and localization in the hyperaccumulator Arabidopsis halleri. Environ Exp Bot 82:54–65. CrossRefGoogle Scholar
  24. Isaure MP, Huguet S, Meyer CL, Castillo-Michel H, Testemale D, Vantelon D, Saumitou-Laprade P, Verbruggen N, Sarret G (2015) Evidence of various mechanisms of Cd sequestration in the hyperaccumulator Arabidopsis halleri, the non-accumulator Arabidopsis lyrata, and their progenies by combined synchrotron-based techniques. J Exp Bot 66:3201–3214. CrossRefGoogle Scholar
  25. Jackson MJ (1989) Physiology of zinc: general aspects. In: Mills CF (ed) Zinc in human biology. ILSI human nutrition reviews. Springer, London, pp 1–14. CrossRefGoogle Scholar
  26. Jankovská I, Miholová D, Bejček V, Vadlejch J, Šulc M, Száková J, Langrová I (2010a) Influence of parasitism on trace element contents in tissues of red fox (Vulpes vulpes) and its parasites Mesocestoides spp. (Cestoda) and Toxascaris leonina (Nematoda). Arch Environ Contam Toxicol 58:469–477. CrossRefGoogle Scholar
  27. Jankovská I, Langrová I, Bejček V, Miholová D, Vadlejch J, Petrtýl M (2010b) Heavy metal accumulation in small terrestrial rodents infected by cestodes or nematodes. Parasite 15:581–588. CrossRefGoogle Scholar
  28. Jankovská I, Vadlejch J, Száková J, Miholová D, Kunc P, Knížková I, Čadková Z, Langrová I (2010c) Experimental studies on the cadmium accumulation in the cestode Moniezia expansa (Cestoda: Anoplocephalidae) and its final host (Ovis aries). Exp Parasitol 126:130–134. CrossRefGoogle Scholar
  29. Jankovská I, Sloup V, Száková J, Langrová I, Sloup S (2016) How the tapeworm Hymenolepis diminuta affects zinc and cadmium accumulation in a host fed a hyperaccumulating plant (Arabidopsis halleri). Environ Sci Pollut Res 23:19126–19133. CrossRefGoogle Scholar
  30. Jankovská I, Sloup V, Száková J, Magdálek J, Nechybová S, Peřinková P, Langrová I (2018) How tapeworm infection and consumption of a Cd and Zn hyperaccumulating plant may affect Cu, Fe, and Mn concentrations in an animal — a plant consumer and tapeworm host. Environ Sci Pollut Res 25:4190–4196. CrossRefGoogle Scholar
  31. Jin T, Nordberg M, Frech W, Dumont X, Bernard A, Ye T, Kong Q, Wang Z, Li P, Lundström NG, Li Y, Nordberg GF (2002) Cadmium biomonitoring and renal dysfunction among a population environmentally exposed to cadmium from smelting in China (ChinaCad). BioMetals 15:397–410. CrossRefGoogle Scholar
  32. Kägi JHR (1991) Overview of metallothionein. Methods Enzymol 205:613–626. CrossRefGoogle Scholar
  33. Kelly EJ, Quaife CJ, Froelick GJ, Palmiter RD (1996) Metallothionein I and II protect against zinc deficiency and zinc toxicity in mice. J Nutr 126:1782–1790. CrossRefGoogle Scholar
  34. King JC, Shames DM, Woodhouse LR (2000) Zinc homeostasis in humans. J Nutr 130:1360–1366. CrossRefGoogle Scholar
  35. Klaassen CD, Kotsonis FN (1977) Biliary excretion of cadmium in the rat, rabbit, and dog. Toxicol Appl Pharmacol 41:101–112. CrossRefGoogle Scholar
  36. Lee DY, Prasad AS, Hydrick-Adair C, Brewer G, Johnson PE (1993) Homeostasis of zinc in marginal human zinc deficiency: role of absorption and endogenous excretion of zinc. J Lab Clin Med 122:549–556Google Scholar
  37. Milne DB, Canfield WK, Mahalko JR, Sandstead HH (1984) Effect of oral folic acid supplements on zinc, copper, and iron absorption and excretion. Am J Clin Nutr 39:535–539. CrossRefGoogle Scholar
  38. Petering HG (1979) Effect of cadmium and lead on copper and zinc metabolism. Trace Element Metab Anim Proc Int Symp 2Google Scholar
  39. Roohani N, Hurrell R, Kelishadi R, Schulin R (2013) Zinc and its importance for human health: an integrative review. J Res Med Sci 18:144–157Google Scholar
  40. Sarret G, Willems G, Isaure MP, Marcus MA, Fakra SC, Frérot H, Pairis S, Geoffroy N, Manceau A, Saumitou-Laprade P (2009) Zinc distribution and speciation in Arabidopsis halleri × Arabidopsis lyrata progenies presenting various zinc accumulation capacities. New Phytol 184:581–595. CrossRefGoogle Scholar
  41. Tang L, Qiu RL, Tang YT, Wang SZ (2014) Cadmium-zinc exchange and their binary relationship in the structure of Zn-related proteins: a mini review. Metallomics 6:1313–1323. CrossRefGoogle Scholar
  42. Winiarska-Mieczan A, Kwiecień M (2016) The effect of exposure to Cd and Pb in the form of a drinking water or feed on the accumulation and distribution of these metals in the organs of growing Wistar rats. Biol Trace Elem Res 169:230–236. CrossRefGoogle Scholar
  43. Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecology. CrossRefGoogle Scholar
  44. Zheng G, Zhong H, Guo Z, Wu Z, Zhang H, Wang C, Zhou Y, Zuo Z (2014) Levels of heavy metals and trace elements in umbilical cord blood and the tisk of adverse pregnancy outcomes: a population-based study. Biol Trace Elem Res 160:437–444. CrossRefGoogle Scholar
  45. Zhenli LH, Yanga XE, Stoffella PJ (2005) Trace elements in agro-ecosystems and impacts on the environment. J Trace Elem Med Biol 19:125–140. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural ResourcesCzech University of Life SciencesPrague 6, SuchdolCzech Republic
  2. 2.Department of Agroenvironmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural ResourcesCzech University of Life SciencesPrague 6, SuchdolCzech Republic

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