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Two-dimensional HPLC coupled to ICP-MS and electrospray ionisation (ESI)-MS/MS for investigating the bioavailability in vitro of arsenic species from edible seaweed

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Abstract

Edible seaweed consumption is a route of exposure to arsenic. However, little attention has been paid to estimate the bioaccessibility and/or bioavailability of arsenosugars in edible seaweed and their possible degradation products during gastrointestinal digestion. This work presents first use of combined inductively coupled plasma mass spectroscopy (ICP-MS) with electrospray ionization tandem mass spectrometry (ESI-MS/MS) with two-dimensional HPLC (size exclusion followed by anion exchange) to compare the qualitative and quantitative arsenosugars speciation of different edible seaweed with that of their bioavailable fraction as obtained using an in vitro gastrointestinal digestion procedure. Optimal extraction conditions for As species from four seaweed namely kombu, wakame, nori and sea lettuce were selected as a compromise between As extraction efficiency and preservation of compound identity. For most investigated samples, the use of ammonium acetate buffer as extractant and 1 h sonication in a water bath followed by HPLC-ICP-MS resulted in 40–61% of the total As to be found in the buffered aqueous extract, of which 86–110% was present as arsenosugars (glycerol sugar, phosphate sugar and sulfonate sugar for wakame and kombu and glycerol sugar and phosphate sugar for nori). The exception was sea lettuce, for which the arsenosugar fraction (glycerol sugar, phosphate sugar) only comprised 44% of the total extracted As. Interestingly, the ratio of arsenobetaine and dimethylarsinic acid to arsenosugars in sea lettuce extracts seemed higher than that for the rest of investigated samples. After in vitro gastrointestinal digestion, approximately 11–16% of the total As in the solid sample was found in the dialyzates with arsenosugars comprising 93–120% and 41% of the dialyzable As fraction for kombu, wakame, nori and sea lettuce, respectively. Moreover, the relative As species distribution in seaweed-buffered extracts and dialyzates was found to be very similar. Collection of specific fractions from the size-exclusion column to be analysed using anion-exchange HPLC-ESI-MS/MS enabled improved chromatographic selectivity, particularly for the less retained arsenosugar (glycerol sugar), facilitating confirmation of the presence of arsenosugars in seaweed extracts and dialyzates. Using this approach, the presence of arsenobetaine in sea lettuce samples was also confirmed.

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References

  1. Rupérez P (2002) Mineral content of edible marine seaweeds. Food Chem 79:23

    Article  Google Scholar 

  2. Romarís-Hortas V, García-Sartal C, Barciela-Alonso MC, Moreda-Piñeiro A, Bermejo-Barrera P (2010) Characterization of edible seaweed harvested on the Galician coast (Northwestern Spain) using recognition techniques and major and trace elements data. J Agric Food Chem 58:1986

    Article  Google Scholar 

  3. Dawczynski C, Schäfer U, Leiterer M, Jahreis G (2007) Nutritional and toxicological importance of macro, trace, and ultra-trace elements in algae food products. J Agric Food Chem 55:10470

    Article  CAS  Google Scholar 

  4. Borak J, Hosgood HD (2007) Seafood arsenic: implications for human risk assessment. Regul Toxicol Pharmacol 47:204

    Article  CAS  Google Scholar 

  5. Francesconi KA, Kuehnelt D (2002) Arsenic compounds in the environment. Environ Chem Arsenic 51

  6. Rose M, Lewis J, Langford N, Baxter M, Origgi S, Barber M, MacBain H, Thomas K (2007) Arsenic in seaweed—forms, concentration and dietary exposure. Food Chem Toxicol 45:1263

    Article  CAS  Google Scholar 

  7. Almela C, Clemente MJ, Vélez D, Montoro R (2006) Total arsenic, inorganic arsenic, lead and cadmium contents in edible seaweed sold in Spain. Food Chem Toxicol 44:1901

    Article  CAS  Google Scholar 

  8. Feldmann J, Krupp EM (2011) Critical review or scientific opinion paper: arsenosugars—a class of benign arsenic species or justification for developing partly speciated arsenic fractionation in foodstuffs? Anal Bioanal Chem 399:1735

    Article  CAS  Google Scholar 

  9. Francesconi KA, Kuehnelt D (2004) Determination of arsenic species: a critical review of methods and applications, 2000–2003. Analyst 129:373

    Article  CAS  Google Scholar 

  10. Niegel C, Matysik F (2010) Analytical methods for the determination of arsenosugars—a review of recent trends and developments. Anal Chim Acta 657:83

    Article  CAS  Google Scholar 

  11. Almela C, Laparra JM, Velez D, Barberá R, Farré R, Montoro R (2005) Arsenosugars in raw and cooked edible seaweed: characterization and bioaccessibility. J Agric Food Chem 53:7344

    Article  CAS  Google Scholar 

  12. Gamble BM, Gallagher PA, Shoemaker JA, Wei X, Schwegel CA, Creed JT (2002) An investigation of the chemical stability of arsenosugars in simulated gastric juice and acidic environments using IC-ICP-MS and IC-ESI-MS/MS. Analyst 127:781

    Article  CAS  Google Scholar 

  13. Moreda-Pineiro J, Moreda-Piñeiro A, Romarís-Hortas V, Moscoso-Perez C, Lopez-Mahia P, Muniategui-Lorenzo S, Bermejo-Barrera P, Prada-Rodríguez D (2011) In-vivo and in-vitro testing to assess the bioaccessibility and the bioavailability of arsenic, selenium and mercury species in food samples. Trends Anal Chem 30:324

    Article  CAS  Google Scholar 

  14. Feldmann J (2000) Metabolism of arsenic from seaweed by man and animals: speciation in body fluids using liquid chromatography inductively coupled plasma mass spectrometry. Trace Elem Man Anim 10:165–168 (Proc Int Symp)

    Google Scholar 

  15. Hsueh YM, Hsu MK, Chiou HY, Yang MH, Huang CC, Chen CJ (2002) Urinary arsenic speciation in subjects with or without restriction from seafood dietary intake. Toxicol Lett 133:83

    Article  CAS  Google Scholar 

  16. Le XC, Cullen WR, Reimer KJ (1994) Human urinary arsenic excretion after one-time ingestion of seaweed, crab, and shrimp. Clin Chem 40:617

    CAS  Google Scholar 

  17. Le XC, Ma M, Lai VW (1999) Exposure to arsenosugars from seafood ingestion and speciation of urinary arsenic metabolites. In: Abernathy CO, Calderon RL, Chappell WR (eds) Arsenic exposure and health effects. Elsevier, London, pp 69–79, Proc Int Conf, 3rd

    Google Scholar 

  18. Reimer KJ, Cullen WR, Koch I, Lai VM, Sylvester S (2006) Arsenic bioaccessibility, metabolism and excretion following ingestion of traditional Chinese medicine. In: Abstracts of papers, 231st ACS National Meeting, Atlanta, GA, USA, 26–30 March 2006 (ENVR)

  19. Newcombe C, Raab A, Williams PN, Deacon C, Haris PI, Meharg AA, Feldmann J (2010) Accumulation or production of arsenobetaine in humans. J Environ Monit 12:832

    Article  CAS  Google Scholar 

  20. Van Hulle M, Zhang C, Schotte B, Mees L, Vanhaecke F, Vanholder R, Zhang XR, Cornelis R (2004) Identification of some arsenic species in human urine and blood after ingestion of Chinese seaweed Laminaria. J Anal At Spectrom 19:58

    Article  Google Scholar 

  21. Raml R, Raber G, Rumpler A, Bauernhofer T, Goessler W, Francesconi KA (2009) Individual variability in the human metabolism of an arsenic-containing carbohydrate, 2′,3′-dihydroxypropyl 5-deoxy-5-dimethylarsinoyl-β-d-riboside, a naturally occurring arsenical in seafood. Chem Res Toxicol 22:1534

    Article  CAS  Google Scholar 

  22. Taebunpakul S, Liu C, Wright C, McAdam K, Heroult J, Braybrook J, Goenaga-Infante H (2011) Determination of total Arsenic and Arsenic speciation in tobacco products: from tobacco leaf and cigarette smoke. J Anal At Spectrom 26:1633

    Article  CAS  Google Scholar 

  23. García-Sartal C, Romarís-Hortas V, Barciela-Alonso MC, Moreda-Piñeiro A, Domínguez-González R, Bermejo-Barrera P (2011) Use of an in vitro digestion method to evaluate the bioaccessibility of arsenic in edible seaweed by inductively coupled plasma-mass spectrometry. Michrochemical J 98:91

    Article  Google Scholar 

  24. Montes-Bayon M, Meija J, LeDuc DL, Terry N, Caruso JA, Sanz-Medel A (2004) HPLC-ICP-MS and ESI-Q-TOF analysis of biomolecules induced in Brassica juncea during arsenic accumulation. J Anal At Spectrom 19:153

    Article  CAS  Google Scholar 

  25. Ouypornkochagorn S, Feldmann J (2010) Dermal uptake of arsenic through human skin depends strongly on its speciation. Environ Sci Technol 44:3972

    Article  CAS  Google Scholar 

  26. McSheehy S, Pohl P, Velez D, Spuznar J (2002) Multidimensional liquid chromatography with parallel ICP MS and electrospray MS/MS detection as a tool for the characterization of arsenic species in algae. Anal Bioanal Chem 372:457

    Article  CAS  Google Scholar 

  27. Corr JJ, Larsen EH (1996) Arsenic speciation by liquid chromatography coupled with ionspray tandem mass spectrometry. J Anal At Spectrom 11:1215

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank the Ministerio de Ciencia y Tecnología (Project number AGL-2006-11034) and Xunta de Galicia (Grupo de Referencia Competitiva 2007/000047-0) for financial support. They are also grateful to the seaweed-based industry ALGAMAR in Redondela (Pontevedra, Spain) for supplying dried and canned seaweed samples. The UK National Measurement Office is also acknowledged for funding, in part, this study. The authors thank Dr K. A. Francesconi from Karl-Franzens University in Austria for the kind donation of the algal extract. Cristina García Sartal thanks to the Fundation Segundo Gil-Dávila for a pre-doctoral grant.

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Authors and Affiliations

  1. Department of Analytical Chemistry, Nutrition and Bromatology, Faculty of Chemistry, University of Santiago de Compostela, Avenida das Ciencias, s/n. 15782, Santiago de Compostela, Spain

    Cristina Garcia-Sartal, María del Carmen Barciela-Alonso & Pilar Bermejo-Barrera

  2. LGC Limited, Queens Road, Teddington, Middlesex, TW11 OLY, UK

    Sutthinun Taebunpakul, Emma Stokes & Heidi Goenaga-Infante

  3. Department of Materials, Imperial College of Science, Technology and Medicine, South Kensington, London, SW7 2AZ, UK

    Sutthinun Taebunpakul

  4. National Institute of Metrology (Thailand), Klong 5, Klong Luang, Pathumthani, 12120, Thailand

    Sutthinun Taebunpakul

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  1. Cristina Garcia-Sartal
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  2. Sutthinun Taebunpakul
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  3. Emma Stokes
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  4. María del Carmen Barciela-Alonso
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  5. Pilar Bermejo-Barrera
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  6. Heidi Goenaga-Infante
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Correspondence to Heidi Goenaga-Infante.

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Published in the special paper collection on Elemental Imaging and Speciation in Plant Science with guest editors J. Feldmann and E. Krupp.

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Garcia-Sartal, C., Taebunpakul, S., Stokes, E. et al. Two-dimensional HPLC coupled to ICP-MS and electrospray ionisation (ESI)-MS/MS for investigating the bioavailability in vitro of arsenic species from edible seaweed. Anal Bioanal Chem 402, 3359–3369 (2012). https://doi.org/10.1007/s00216-011-5483-4

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  • DOI: https://doi.org/10.1007/s00216-011-5483-4

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