Biological Trace Element Research

, Volume 179, Issue 1, pp 79–90 | Cite as

Comparative Analysis on the Effect of Plantago Species Aqueous Extracts on Tissue Trace Element Content in Rats

  • Evgenia R. Gatiatulina
  • Olga N. Nemereshina
  • Joanna Suliburska
  • Tejo Prakash Nagaraja
  • Anastasia A. Skalnaya
  • Alexandr A. Nikonorov
  • Anatoly V. Skalny
  • Alexey A. Tinkov


The primary objective of this study is to assess the influence of water extracts of Plantago major L., Plantago lanceolata L., and Plantago maxima Juss. ex Jacq. leaves on tissue trace element content in healthy adult Wistar rats. Twenty-eight female Wistar rats consumed pure drinking water or one of the three aqueous extracts of Plantago for 1 month. The extracts and liver, serum, hair, and adipose tissue of the rats were examined for trace element contents using inductively coupled plasma mass spectrometry. The aqueous extracts of Plantago species contained significant levels of trace elements, which were highest in P. lanceolata and P. major. The administration of every extract led to an increase in V and Si levels in the rats. At the same time, the consumption of P. lanceolata aqueous extract resulted in the accumulation of toxic elements (As, Pb) in the rats’ tissues. Despite the rather high concentration of heavy metals in the P. major leaf extract, its administration did not result in the accumulation of these elements. In turn, P. maxima extract induced a significant decrease in the tissue levels of Al, Cr, I, Li, and Mn in the rats. The beneficial effect of the P. major and P. maxima preparations may be at least partially associated with the increased supply of essential trace elements, whereas the use of P. lanceolata may be harmful due to the possibility of heavy metal overexposure.


Plantago Vanadium Silicon Adipose tissue Metals 


Compliance with Ethical Standards

The investigation protocol was approved by the local ethics committee. All animal studies were performed in accordance with the ethical standards laid down in the US guidelines (NIH Publication no. 85-23, amended in 1985).

Conflict of Interest

The authors declare that they have no conflict of interest.


This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.


  1. 1.
    Samuelsen AB (2000) The traditional uses, chemical constituents and biological activities of Plantago major L. A review J Ethnopharmacol 71(1):1–21PubMedGoogle Scholar
  2. 2.
    Zhou Q, Lu W, Niu Y, Liu J, Zhang X, Gao B, Akoh CC, Shi H, Yu L (2013) Identification and quantification of phytochemical composition and anti-inflammatory, cellular antioxidant, and radical scavenging activities of 12 Plantago species. J Agric Food Chem 61(27):6693–6702CrossRefPubMedGoogle Scholar
  3. 3.
    Nemereshina ON, Tinkov AA, Gritsenko VA, Nikonorov AA (2015) Influence of Plantaginaceae species on E. coli K12 growth in vitro: possible relation to phytochemical properties. Pharm Biol 53(5):715–724CrossRefPubMedGoogle Scholar
  4. 4.
    Filipović-Trajković R, Ilić ZS, Šunić L, Andjelković S (2012) The potential of different plant species for heavy metals accumulation and distribution. J Food Agric Environ 10(1):959–964Google Scholar
  5. 5.
    Petrova S, Velcheva I, Yurukova I, Berova M (2014) Plantago lanceolata L. as a biomonitor of trace elements in an urban area. Bulg J Agric Sci 20:325–326Google Scholar
  6. 6.
    Tinkov AA, Nemereshina ON, Suliburska J, Gatiatulina ER, Regula J, Nikonorov AA, Skalny AV (2016) Comparative analysis of the trace element content of the leaves and roots of three Plantago species. Biol Trace Elem Res 173(1):225–230CrossRefPubMedGoogle Scholar
  7. 7.
    Fraga CG (2005) Relevance, essentiality and toxicity of trace elements in human health. Mol Asp Med 26(4):235–244CrossRefGoogle Scholar
  8. 8.
    Gonçalves S, Romano A (2016) The medicinal potential of plants from the genus Plantago (Plantaginaceae). Ind Crop Prod 83:213–226CrossRefGoogle Scholar
  9. 9.
    Yoshida T, Rikimaru K, Sakai M, Nishibe S, Fujikawa T, Tamura Y (2013) Plantago lanceolata L. leaves prevent obesity in C57BL /6 J mice fed a high-fat diet. Nat Prod Res 27(11):982–987CrossRefPubMedGoogle Scholar
  10. 10.
    Tinkov AA, Nemereshina ON, Popova EV, Polyakova VS, Gritsenko VA, Nikonorov AA (2014) Plantago maxima leaves extract inhibits adipogenic action of a high-fat diet in female Wistar rats. Eur J Clin Nutr 53(3):831–842CrossRefGoogle Scholar
  11. 11.
    Wiernsperger N, Rapin J (2010) Trace elements in glucometabolic disorders: an update. Diabetol Metab Syndr 2(70):1–9Google Scholar
  12. 12.
    Tinkov AA, Popova EV, Polyakova VS, Kwan OV, Skalny AV, Nikonorov AA (2015) Adipose tissue chromium and vanadium disbalance in high-fat fed Wistar rats. J Trace Elem Med Biol 29:176–181CrossRefPubMedGoogle Scholar
  13. 13.
    Maevskij PF (2014) Flora of the middle part of the European part of Russia. 11 ed., MoscowGoogle Scholar
  14. 14.
    Cruz BH, Díaz-Cruz JM, Ariño C, Esteban M (2000) Heavy metal binding by tannic acid: a voltammetric study. Electroanalysis 12(14):1130–1137CrossRefGoogle Scholar
  15. 15.
    Yoneda S, Nakatsubo F (1998) Effects of the hydroxylation patterns and degrees of polymerization of condensed tannins on their metal-chelating capacity. J Wood Chem Tech 18(2):193–205CrossRefGoogle Scholar
  16. 16.
    Khokhar S, Apenten RKO (2003) Iron binding characteristics of phenolic compounds: some tentative structure–activity relations. Food Chem 81(1):133–140CrossRefGoogle Scholar
  17. 17.
    Brune M, Rossander L, Hallberg L (1989) Iron absorption and phenolic compounds: importance of different phenolic structures. Eur J Clin Nutr 43(8):547–557PubMedGoogle Scholar
  18. 18.
    Taty-Costodes VC, Fauduet H, Porte C, Delacroix A (2003) Removal of Cd (II) and Pb (II) ions, from aqueous solutions, by adsorption onto sawdust of Pinus sylvestris. J Hazard Mater 105(1):121–142CrossRefPubMedGoogle Scholar
  19. 19.
    Hurrell RF, Reddy M, Cook JD (1999) Inhibition of non-haem iron absorption in man by polyphenolic-containing beverages. Br J Nutr 81(04):289–295PubMedGoogle Scholar
  20. 20.
    Glahn RP, Wortley GM, South PK, Miller DD (2002) Inhibition of iron uptake by phytic acid, tannic acid, and ZnCl2: studies using an in vitro digestion/Caco-2 cell model. J Agric Food Chem 50(2):390–395CrossRefPubMedGoogle Scholar
  21. 21.
    Afsana K, Shiga K, Ishizuka S, Hara H (2004) Reducing effect of ingesting tannic acid on the absorption of iron, but not of zinc, copper and manganese by rats. Biosci Biotechnol Biochem 68(3):584–592CrossRefPubMedGoogle Scholar
  22. 22.
    Haddadian K, Haddadian K, Zahmotkash H (2014) A review of Plantago plant. Indian J Tradit Knowl 13(4):681–685Google Scholar
  23. 23.
    Bronco S, Cappelli C, Monti S (2006) Characterization of supramolecular polyphenol-chromium (III) clusters by molecular dynamics simulations. J Phys Chem B 110(26):13227–13234CrossRefPubMedGoogle Scholar
  24. 24.
    Thoma V, Tampouris K, Petrou AL (2008) Kinetics and mechanism of the reaction between chromium (III) and 3, 4-dihydroxy-phenyl-propenoic acid (caffeic acid) in weak acidic aqueous solutions. Bioinorg Chem Appl 624583. doi:10.1155/2008/624583
  25. 25.
    Poonkuzhali K, Manivannan M, Palvannan T (2013) Assessing the chelating ability of Aerva lanata: adsorption of chromium from tannery effluent and its toxicity measurement. J Water Chem Techno 35(3):133–138CrossRefGoogle Scholar
  26. 26.
    Haslam E (1996) Natural polyphenols (vegetable tannins) as drugs: possible modes of action. J Nat Prod 59(2):205–215CrossRefPubMedGoogle Scholar
  27. 27.
    Vidé J, Virsolvy A, Romain C, Ramos J, Jouy N, Richard S, Cristol JP, Gaillet S, Rouanet JM, Watts DL (1990) The nutritional relationships of manganese. J Orthomol Med 5(4):219–222Google Scholar
  28. 28.
    Fraile AL, Flynn A (1992) The absorption of manganese from polyphenol-containing beverages in suckling rats. Int J Food Sci Nutr 43(3):163–168CrossRefGoogle Scholar
  29. 29.
    Kolesnikov MP, Gins VK (2001) Forms of silicon in medicinal plants. Appl Biochem Microbiol 37(5):524–527CrossRefGoogle Scholar
  30. 30.
    Van Dyck K, Van Cauwenbergh R, Robberecht H, Deelstra H (1999) Bioavailability of silicon from food and food supplements. Fresenius J Anal Chem 363(5–6):541–544CrossRefGoogle Scholar
  31. 31.
    Brnić M, Wegmüller R, Zeder C, Senti G, Hurrell RF (2014) Influence of phytase, EDTA, and polyphenols on zinc absorption in adults from porridges fortified with zinc sulfate or zinc oxide. J Nutr 144(9):1467–1473CrossRefPubMedGoogle Scholar
  32. 32.
    Edel AL, Kopilas M, Clark TA, Aguilar F, Ganguly PK, Heyliger CE, Pierce GN (2006) Short-term bioaccumulation of vanadium when ingested with a tea decoction in streptozotocin-induced diabetic rats. Metabolism 55(2):263–270CrossRefPubMedGoogle Scholar
  33. 33.
    Sanchez-Gonzalez C, Bermudez-Peña C, Trenzado CE, Goenaga-Infante H, Montes-Bayon M, Sanz-Medel A, Llopis J (2012) Changes in the antioxidant defence and in selenium concentration in tissues of vanadium exposed rats. Metallomics 4(8):814–819CrossRefPubMedGoogle Scholar
  34. 34.
    Gruzewska K, Michno A, Pawelczyk T, Bielarczyk H (2014) Essentiality and toxicity of vanadium supplements in health and pathology. J Physiol Pharmacol 65(5):603–611PubMedGoogle Scholar
  35. 35.
    Tinkov AA, Sinitskii AI, Popova EV, Nemereshina ON, Gatiatulina ER, Skalnaya MG, Skalny AV, Nikonorov AA (2015) Alteration of local adipose tissue trace element homeostasis as a possible mechanism of obesity-related insulin resistance. Med Hypotheses 85(3):343–347CrossRefPubMedGoogle Scholar
  36. 36.
    Seale AP, de Jesus LA, Park MC, Kim YS (2006) Vanadium and insulin increase adiponectin production in 3T3-L1 adipocytes. Pharmacol Res 54(1):30–38CrossRefPubMedGoogle Scholar
  37. 37.
    Kawabe K, Yoshikawa Y, Adachi Y, Sakurai H (2006) Possible mode of action for insulinomimetic activity of vanadyl (IV) compounds in adipocytes. Life Sci 78(24):2860–2866CrossRefPubMedGoogle Scholar
  38. 38.
    Oberleas D (2011) Diabetes type II, a new perspective. Trace Elem Electroly 28(1):52–55CrossRefGoogle Scholar
  39. 39.
    Tinkov AA, Popova EV, Gatiatulina ER, Skalnaya AA, Yakovenko EN, Alchinova IB, Karganov MY, Skalny AV, Nikonorov AA (2016) Decreased adipose tissue zinc content is associated with metabolic parameters in high fat fed Wistar rats. Acta Sci Pol Technol Aliment 15(1):99–105. doi:10.17306/J.AFS.2016.1.10 CrossRefPubMedGoogle Scholar
  40. 40.
    Vidé J, Virsolvy A, Romain C, Ramos J, Jouy N, Richard S, Cristol JP, Gaillet S, Rouanet JM (2015) Dietary silicon-enriched spirulina improves early atherosclerosis markers in hamsters on a high-fat diet. Nutrition 31(9):1148–1154CrossRefPubMedGoogle Scholar
  41. 41.
    Arner E, Forrest AR, Ehrlund A, Mejhert N, Itoh M, Kawaji H, Lassmann T, Laurencikiene J, Rydén M, Arner P, FANTOM Consortium (2014) Ceruloplasmin is a novel adipokine which is overexpressed in adipose tissue of obese subjects and in obesity-associated cancer cells. PLoS One 9(3):e80274CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Chojnacka K, Zielińska A, Górecka H, Dobrzański Z, Górecki H (2010) Reference values for hair minerals of polish students. Environ Toxicol Pharmacol 29(3):314–319CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Evgenia R. Gatiatulina
    • 1
    • 2
  • Olga N. Nemereshina
    • 1
  • Joanna Suliburska
    • 3
  • Tejo Prakash Nagaraja
    • 4
  • Anastasia A. Skalnaya
    • 5
  • Alexandr A. Nikonorov
    • 1
    • 6
  • Anatoly V. Skalny
    • 6
    • 7
    • 8
    • 9
  • Alexey A. Tinkov
    • 1
    • 6
    • 7
    • 8
  1. 1.Orenburg State Medical UniversityOrenburgRussia
  2. 2.South Ural State Medical UniversityChelyabinskRussia
  3. 3.Poznan University of Life SciencesPoznanPoland
  4. 4.School of Energy and EnvironmentThapar UniversityPatialaIndia
  5. 5.Lomonosov Moscow State UniversityMoscowRussia
  6. 6.Orenburg State UniversityOrenburgRussia
  7. 7.RUDN UniversityMoscowRussia
  8. 8.Yaroslavl State UniversityYaroslavlRussia
  9. 9.All-Russian Research Institute of Medicinal and Aromatic Plants (VILAR)MoscowRussia

Personalised recommendations