Biological Trace Element Research

, Volume 189, Issue 1, pp 267–276 | Cite as

Trace Element Uptake and Accumulation in the Medicinal Herb Hypericum perforatum L. Across Different Geolithological Settings

  • Gianmaria Bonari
  • Fabrizio Monaci
  • Francesco Nannoni
  • Claudia Angiolini
  • Giuseppe ProtanoEmail author


The worldwide growing interest in traditional medicines, including herbal medicines and herbal dietary supplements, has recently been accompanied by concerns on quality and safety of this type of health care. The content of nutritional and potentially toxic elements in medicinal plants is of paramount interest as it may vary remarkably according to different environmental and ecophysiological factors. In this study, the concentrations of essential and non-essential trace elements—Co, Cr, Cu, Ni, Sr, and Zn—were determined in the roots and aerial parts of the worldwide distributed and economically important medicinal herb Hypericum perforatum L. (St. John’s wort) and in its growing substrate. Most of the analyzed trace elements varied considerably in the plant parts according to edaphic conditions and soil geochemistry. However, uptake and retention in H. perforatum compartments of Co, Cr, and Ni, which markedly differentiated the investigated soils, were controlled by excluding mechanisms of the plant. Despite this, the Ni concentrations in the aerial parts, commonly used in herbal preparations, of H. perforatum plants from serpentine soils were not insignificant in relation to eventual human consumption. Good practice to assure the herbal product quality of H. perforatum collected from the wild cannot ignore the thorough understanding of the geolithological and geochemical features of the harvesting areas.


Trace elements Hypericum perforatum L. Uptake Bioaccumulation Translocation Medicinal plants 



The authors thank Debora Barbato, Marco Biagioli, Luca Paoli, Neha Shukla, and Andrea Vannini for their useful suggestions and beneficial discussions in the early stage of this study. We are grateful to two anonymous reviewers for their insightful comments on the paper which have substantially improved the final version of the manuscript.


  1. 1.
    World Health Organization (2013) WHO Traditional Medicine Strategy 2014–2023Google Scholar
  2. 2.
    Arceusz A, Radecka I, Wesolowski M (2010) Identification of diversity in elements content in medicinal plants belonging to different plant families. Food Chem 120:52–58CrossRefGoogle Scholar
  3. 3.
    Bertoli A, Cirak C, Teixeira da Silva JA (2011) Hypericum species as sources of valuable essential oils. Med Aroma Plant Sci Biotech 5:29–47Google Scholar
  4. 4.
    Leśniewicz A, Jaworska K, Zyrnicki W (2006) Macro- and micro-nutrients and their bioavailability in polish herbal medicaments. Food Chem 99:670–679CrossRefGoogle Scholar
  5. 5.
    Korkmaz K, Kara SM, Özkutlu F, Akgün M, Coşge Şenkal B (2017) Profile of heavy metal and nutrient elements in some Sideritis species. Indian J Pharm Educ 51:s209–s212CrossRefGoogle Scholar
  6. 6.
    Haidu D, Párkányi D, Moldovan RI, Savii C, Pinzaru I, Dehelean C, Kurunczi L (2017) Elemental characterization of Romanian crop medicinal plants by neutron activation analysis. J Anal Methods Chem 2017:9748413CrossRefGoogle Scholar
  7. 7.
    Zeiner M, Juranović Cindrić I, Požgaj M, Pirkl R, Šilić T, Stingeder G (2015) Influence of soil composition on the major, minor and trace metal content of Velebit biomedical plants. J Pharm Biomed Anal 106:153–158CrossRefGoogle Scholar
  8. 8.
    Zeiner M, Juranović Cindrić I (2017) Review—trace determination of potentially toxic elements in (medicinal) plant materials. Anal Methods 9:1550–1574CrossRefGoogle Scholar
  9. 9.
    McCutcheon A (2017) On adulteration of Hypericum perforatum. Botanical Adulterants Bulletin 1:1–9Google Scholar
  10. 10.
    Barnes J, Anderson LA, Phillipson JD (2001) St John’s wort (Hypericum perforatum L.): a review of its chemistry, pharmacology and clinical properties. J Pharm Pharmacol 53:583–600CrossRefGoogle Scholar
  11. 11.
    Crockett S, Robson N (2011) Taxonomy and chemotaxonomy of the genus Hypericum. Med Aroma Plant Sci Biotech 5:1–13Google Scholar
  12. 12.
    Kabelitz L (2005) Quality of herbal drugs and their preparations: critical criteria and management. Acta Hortic 679:83–96CrossRefGoogle Scholar
  13. 13.
    Agapouda A, Booker A, Kiss T, Hohmann J, Heinrich M, Csupor D (2017) Quality control of Hypericum perforatum L. analytical challenges and recent progress. J Pharm Pharmacol.
  14. 14.
    Bertoli A, Çirak C, Seyis F (2018) Hypericum spp. volatile profiling and the potential significance in the quality control of new valuable raw material. Microchem J 136:94–100CrossRefGoogle Scholar
  15. 15.
    Booker A, Agapouda A, Frommenwiler DA, Scotti F, Reich E, Heinrich M (2018) St John’s wort (Hypericum perforatum) products—an assessment of their authenticity and quality. Phytomedicine 40:158–164CrossRefGoogle Scholar
  16. 16.
    Chizzola R, Lukas B (2006) Variability of the cadmium content in Hypericum species collected in eastern Austria. Water Air Soil Pollut 170:331–343CrossRefGoogle Scholar
  17. 17.
    Helmja K, Vaher M, Püssa T, Orav A, Viitak A, Levandi T, Kaljurand M (2011) Variation in the composition of the essential oils, phenolic compounds and mineral elements of Hypericum perforatum L. growing in Estonia. Nat Prod Res 25:496–510CrossRefGoogle Scholar
  18. 18.
    Pavlova D, Karadjova I, Krasteva I (2015) Essential and toxic element concentrations in Hypericum perforatum. Aust J Bot 63:152–158CrossRefGoogle Scholar
  19. 19.
    Tokalıoğlu Ş (2012) Determination of trace elements in commonly consumed medicinal herbs by ICP-MS and multivariate analysis. Food Chem 134:2504–2508CrossRefGoogle Scholar
  20. 20.
    Owen JD, Kirton SB, Evans SJ, Stair JL (2016) Elemental fingerprinting of Hypericum perforatum (St John’s wort) herb and preparations using ICP-OES and chemometrics. J Pharm Biomed Anal 125:15–21CrossRefGoogle Scholar
  21. 21.
    Pavlova D, Karadjova I (2013) Toxic element profiles in selected medicinal plants growing on serpentines in Bulgaria. Biol Trace Elem Res 156:288–297CrossRefGoogle Scholar
  22. 22.
    Decandia FA, Lazzarotto A, Liotta D (2001) Structural features of southern Tuscany, Italy. Ofioliti 26:287–300Google Scholar
  23. 23.
    Buckley YM, Briese DT, Rees M (2003) Demography and management of the invasive plant species Hypericum perforatum. II Construction and use of an individual-based model to predict population dynamics and the effects of management strategies. J Appl Ecol 40:494–507CrossRefGoogle Scholar
  24. 24.
    Robson N (2002) Studies in the genus Hypericum L. (Guttiferae) 4(2). Section 9. Hypericum sensu lato (part 2): subsection 1. Hypericum series 1. Hypericum. Bulletin of the Natural History Museum: Botany 32:61–123Google Scholar
  25. 25.
    Fox LR, Ribeiro SP, Brown VK, Masters GJ, Clarkeet IP (1999) Direct and indirect effects of climate change on St John’s wort, Hypericum perforatum L. (Hypericaceae). Oecologia 120:113–122CrossRefGoogle Scholar
  26. 26.
    Maron JL, Elmendorf SC, Vilà M (2007) Contrasting plant physiological adaptation to climate in the native and introduced range of Hypericum perforatum. Evolution 61:1912–1924CrossRefGoogle Scholar
  27. 27.
    Rauret G, Lòpez-Sànchez JF, Sahuquillo A, Rubio R, Davidson C, Ure A, Quevauviller P (1999) Improvement of the BCR three step sequential extraction procedure prior to the certification of new sediment and soil reference materials. J Environ Monit 1:57–61CrossRefGoogle Scholar
  28. 28.
    Hendershot WH, Douquette M (1986) A simple barium chloride method for determining cation exchange capacity and exchangeable cations. Soil Sci Soc Am J 50:605–608CrossRefGoogle Scholar
  29. 29.
    Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 34:29–38CrossRefGoogle Scholar
  30. 30.
    Angiolini C, Bonari G, Frignani F, Iiriti G, Nannoni F, Protano G, Landi M (2015) Ecological patterns of morphological variation in Italian populations of Romulea bulbocodium (Iridaceae). Flora 214:1–10CrossRefGoogle Scholar
  31. 31.
    Yoon J, Cao X, Zhou Q, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464CrossRefGoogle Scholar
  32. 32.
    Li HF, Gray C, Mico C, Zhao FJ, McGrath SP (2009) Phytotoxicity and bioavailability of cobalt to plants in a range of soils. Chemosphere 75:979–986CrossRefGoogle Scholar
  33. 33.
    Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals. Springer, NYCrossRefGoogle Scholar
  34. 34.
    Giandon P, Garlato A, Ragazzi F (2010) Valori di fondo di metalli e metalloidi nei suoli del Veneto [Background values of metals and metalloids in soils of Veneto region]. ARS 127:14–19, article in ItalianGoogle Scholar
  35. 35.
    Kabata-Pendias A, Pendias H (2011) Trace elements in soils and plants. CRC Press, Boca RatonGoogle Scholar
  36. 36.
    Reimann C, de Caritat P (1998) Trace elements in the environment. Springer Verlag, BerlinGoogle Scholar
  37. 37.
    Geneva M (2010) Metal uptake by Saint John’s wort (Hypericum perforatum L.) grown on industrially polluted soil. Proceedings of 6th Conference on Aromatic and Medicinal Plants of Southeast European Countries. April 18–22, 2010 Antalya, TurkeyGoogle Scholar
  38. 38.
    Radanovic D, Antic-Mladenovic S, Jakovljevic M (2002) Influence of some soil characteristics on heavy metal content in Hypericum perforatum L. and Achillea millefolium. Acta Hortic 576:295–301CrossRefGoogle Scholar
  39. 39.
    Schneider M, Marquard R (1996) Aufnahme und Akkumulation von cadmium und weiterer Schwermetalle bei Hypericum perforatum L. und Linum usitatissimum L. [Investigations on reception and accumulation of cadmium in Hypericum perforatum (St. John’s wort) and Linum usitatissimum L. (linseed)] Z Arznei- Gewürzpfla 1:111−116, article in GermanGoogle Scholar
  40. 40.
    Jones JB (2012) Plant nutrition and soil fertility manual, second edition. Taylor & Francis, CRC Press, Boca RatonCrossRefGoogle Scholar
  41. 41.
    Markert B (1992) Establishing of ‘reference plant’ for inorganic characterization of different plant species by chemical fingerprinting. Water Air Soil Pollut 64:533–538CrossRefGoogle Scholar
  42. 42.
    Kalny P, Wyderska S, Fijałek Z, Wroczyński P (2012) Determination of selected elements in different pharmaceutical forms of some Polish herbal medicinal products. Acta Pol Pharm Drug Res 69:279–283Google Scholar
  43. 43.
    Mihaljev Z, Zivkov-Balos M, Cupic Z, Jaksic S (2014) Levels of some microelements and essential heavy metals in herbal teas in Serbia. Acta Pol Pharm Drug Res 71:385–391Google Scholar
  44. 44.
    Yusuf M, Fariduddin Q, Hayat S, Ahmad A (2011) Nickel: an overview of uptake, essentiality and toxicity in plants. Bull Environ Contam Toxicol 86:1–17CrossRefGoogle Scholar
  45. 45.
    Augustsson ALM, Uddh-Söderberg TE, Hogmalm KJ, Filipsson MEM (2015) Metal uptake by homegrown vegetables—the relative importance in human health risk assessments at contaminated sites. Environ Res 138:181–190CrossRefGoogle Scholar
  46. 46.
    Lange B, van der Ent A, Baker AJM, Echevarria G, Mahy G, Malaisse F, Meerts P, Pourret O, Verbruggen N, Faucon MP (2017) Copper and cobalt accumulation in plants: a critical assessment of the current state of knowledge. New Phytol 213:537–551CrossRefGoogle Scholar
  47. 47.
    Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181CrossRefGoogle Scholar
  48. 48.
    Murch SJ, Haq K, Rupasinghe HPV, Saxena PK (2003) Nickel contamination affects growth and secondary metabolite composition of St. John’s wort (Hypericum perforatum L.). Environ Exp Bot 49:251–257CrossRefGoogle Scholar
  49. 49.
    World Health Organization (WHO) (2007) WHO guidelines for assessing quality of herbal medicines with reference to contaminants and residues. Switzerland, GenevaGoogle Scholar
  50. 50.
    Element Concentration Cadastre in Ecosystems (1994) Element Concentration Cadasters in Ecosystems (ECCE) progress report, presented at the 25th General Assembly of International Union of Biological Sciences (IUBS: Paris, France)Google Scholar
  51. 51.
    Barker AV, Pilbeam DJ (2016) Handbook of plant nutrition. CRC Press, Boca RatonGoogle Scholar
  52. 52.
    Sasmaz M, Sasmaz A (2017) The accumulation of strontium by native plants grown on Gumuskoy mining soils. J Geochem Explor 181:236–242CrossRefGoogle Scholar
  53. 53.
    Qi L, Qin X, Li FM, Siddique KH, Brandl H, Xu J, Li X (2014) Uptake and distribution of stable strontium in 26 cultivars of three crop species: oats, wheat, and barley for their potential use in phytoremediation. Int J Phytoremediat 17:264–271CrossRefGoogle Scholar
  54. 54.
    Wang X, Chen C, Wang J (2017) Phytoremediation of strontium contaminated soil by Sorghum bicolor (L.) Moench and soil microbial community-level physiological profiles (CLPPs). Environ Sci Pollut Res 24:7668–7678CrossRefGoogle Scholar
  55. 55.
    Moyen C, Roblin G (2010) Uptake and translocation of strontium in hydroponically grown maize plants, and subsequent effects on tissue ion content, growth and chlorophyll a/b ratio: comparison with Ca effects. Environ Exp Bot 68:247–257CrossRefGoogle Scholar
  56. 56.
    Savinkov A, Semioshkina N, Howard BJ, Voigt G (2007) Radiostrontium uptake by plants from different soil types in Kazakhstan. Sci Total Environ 373:324–333CrossRefGoogle Scholar
  57. 57.
    Kabata-Pendias A, Mukherjee A (2007) Trace elements from soil to human. Springer-Verlag, Berlin HeidelbergCrossRefGoogle Scholar
  58. 58.
    Moreno-Jiménez E, Peñalosa JM, Manzano R, Carpena-Ruiz RO, Gamarra R, Esteban E (2009) Heavy metals distribution in soils surrounding an abandoned mine in NW Madrid (Spain) and their transference to wild flora. J Hazard Mater 162:854–859CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Gianmaria Bonari
    • 1
  • Fabrizio Monaci
    • 2
  • Francesco Nannoni
    • 3
  • Claudia Angiolini
    • 2
  • Giuseppe Protano
    • 3
    Email author
  1. 1.Department of Botany and ZoologyMasaryk University Kotlarska 2BrnoCzech Republic
  2. 2.Department of Life SciencesUniversity of SienaSienaItaly
  3. 3.Department of Environmental, Earth and Physical SciencesUniversity of SienaSienaItaly

Personalised recommendations