Dietary exposure to trace elements (B, Ba, Li, Ni, Sr, and V) and toxic metals (Al, Cd, and Pb) from the consumption of commercial preparations of Spirulina platensis

  1. González-Weller, Dailos
  2. Rubio, Carmen
  3. Paz, Soraya
  4. Hardisson, Arturo
  5. Dominik-Jakubiec, Marcel
  6. Gutiérrez, Ángel J.
  1. 1 Universidad de La Laguna
    info

    Universidad de La Laguna

    San Cristobal de La Laguna, España

    ROR https://ror.org/01r9z8p25

Revue:
Environmental Science and Pollution Research

ISSN: 0944-1344 1614-7499

Année de publication: 2021

Type: Article

DOI: 10.1007/S11356-020-12260-3 GOOGLE SCHOLAR

D'autres publications dans: Environmental Science and Pollution Research

Résumé

Spirulina is a multicellular cyanobacterium that is consumed as a dietary supplement. The content of trace elements (B, Ba, Li, Ni, Sr, V) and toxic metals (Al, Cd, Pb) was determined in 24 spirulina samples marketed in two different formulations (tablets and powder) by ICP-OES (inductively coupled plasma optical emission spectrometry). The highest element concentration was found in the powder presentation, except for Li. The powder presentation element levels (mg/kg dry weight) were Al (28.1), Sr (10.3), B (1.73), Li (1.47), Ba (1.25), Ni (0.63), Pb (88.1 μg/kg dw), Cd (37.2 μg/kg dw), and V (22.9 μg/kg dw). Considering an adult with a body weight of 68.48 kg and the posology guidelines (14 tablespoons per week), the consumption of powdered spirulina contributes greatly to the Al intake by 2.04% of its TWI (tolerable weekly intake) set at 1 mg/kg body weight/week, followed by Cd with 1.05% of its TWI set at 2.5 μg/kg bw/week. Pb intake represents 1.05% of the BMDL (benchmark dose) level associated with nephrotoxicity and 0.44% of the BMDL associated with cardiovascular effects. This assessment suggests that spirulina consumption does not pose risks to the consumer as far as exposure to toxic metals (Al, Cd, Pb) is concerned. However, the presence of trace elements and toxic metals in spirulina preparations should be monitored to ensure its quality and safety.

Références bibliographiques

  • AECOSAN (Agencia Española de Consumo, Seguridad Alimentaria y Nutrición) (2006a) Dictamen del Comité Científico de la AESA sobre una cuestión presentada por la Comunidad Autónoma de Castilla-La Mancha relativa a la evaluación del riesgo en relación con el empleo del cloruro de litio como marcador en vinos con destino a la destilación. Rev Commit Cient 4: 55-59.
  • AECOSAN (Agencia Española de Consumo, Seguridad Alimentaria y Nutrición) (2006b) Spanish model diet for the determination of consumer exposure to chemicals. Ministry of Health, Social Services and Equality. Madrid, Spain.
  • Ali SK, Saleh AM (2012) Spirulina – an overview. Int J Pharm Pharm Sci 4(3):9–15
  • Boffito C (2000) Barium. Kirk-Othmer. Encyclopedia of. Chem Technol:1–12
  • Calvino-Casilda V, Perozo-Rondón E, Ferrera-Escudero S, Ávila-Rey M, López-Peinado AJ, Aranda M (2005) Enseñanza de las Ciencias: El indiscutible descubridor del Vanadio, el español Andrés Manuel del Río. Rev 100cias@ UNED 8: 140-143.
  • Camacho-Cristóbal JJ, Rexach J, González-Fontes A (2008) Boron in plants: deficiency and toxicity. J Integr Plant Biol 50(10). https://doi.org/10.1111/j.1744-7909.2008.00742.x
  • Castro-García SZ, Chamorro-Cevallos G, Quevedo-Corona L, McCarty MF, Bobadilla-Lugo RA (2018) Beneficial effects of phycobiliproteins from Spirulina maxima in a preeclampsia model. Life Sci 211:17–24
  • Chen Y, Chang G, Kuo S, Huang S, Lo Y et al (2016) Well-tolerated Spirulina extract inhibits influenza virus replication and reduces virus- induced mortality. Sci Rep 6(1)
  • Crespo E (2001) El boro, elemento nutricional esencial en la funcionalidad ósea. Rev Esp Cir Osteoart 36(206):88–95
  • Das KK, Das SN, Dhundasi SA (2008) Nickel, its adverse health effects & oxidative stress. Indian J Med Res 128:412–425
  • Desideri D, Cantaluppi C, Ceccotto F, Meli MA, Roselli C, Feduzi L (2016) Essential and toxic elements in seaweeds for human consumption. J Toxicol Environ Health PA 79(3):112–122. https://doi.org/10.1080/15287394.2015.1113598
  • Dolara P (2014) Occurrence, exposure, effects, recommended intake and possible dietary use of selected trace compounds (aluminium, bismuth, cobalt, gold, lithium, nickel, silver). Int J Food Sci Nutr 65(8):911–924
  • Domínguez-Ortega L, Medina-Ortiz O, Cabrera García-Armenter S (2006) Intoxicación con litio. Anal Med Int 23(9):441–445
  • EC (European Commission) (2006). Regulation
  • (CE) No 1881/2006 of the Commission of December 19, 2006 establishing the maximum content of certain contaminants in food products. Off J Euro Union L364/5.
  • EFSA (European Food Safety Authority) (2010) Scientific opinion on lead in food. EFSA J 8(4):1570
  • EFSA (European Food Safety Authority) (2011a) Statement on the evaluation on a new study related to thee bioavailability of aluminium in food. EFSA J 9(5):2157
  • EFSA (European Food Safety Authority) (2011b) Panel on Contaminants in the Food Chain (CONTAM). Statement on tolerable weekly intake for cadmium. EFSA J 9(2):1975
  • EFSA (European Food Safety Authority) (2013) Technical report: dietary exposure to aluminium-containing food additives. In: Supporting Publications EN-411
  • EFSA (European Food Safety Authority) (2015) Scientific opinion on the risks to public health related to the presence of nickel in food and drinking water. EFSA J 13(2):4002–4204
  • El-Din SMM (2017) Effect of copper and lead on growth and some metabolic activities of cyanobacterium Spirulina platensis (Nordstedt). Egypt J Bot 57(3):445–456
  • El-Din NGS, Mohamedein LI, El-Moselhy KM (2014) Seaweeds as bioindicators of heavy metals off a hot spot area on the Egyptian Mediterranean Coast during 2008-2010. Environ Monit Assess 186:5865–5881
  • El-Sheekh M, El-Sabagh S, Elsoud GA, Elbeltagy A (2020) Efficacy of immobilized biomass of the seaweeds Ulva lactuca and Ulva fasciata for cadmium biosorption. Iranian J Sci Tech Trans A Sci 44:37–49
  • EU (European Union) (2014) COMMISSION REGULATION, No 488/2014 of 12 May 2014 amending Regulation
  • (EC) No 1881/2006 as regards maximum levels of cadmium in foodstuffs. Off J Eur Union L138(/75)
  • Golding LA, Angel BM, Batley GE, Apte SC, Krassoi R, Doyle CJ (2015) Derivation of a water quality guideline for aluminium in marine waters. Environ Toxicol Chem 34(1):141–151
  • Habib M, Parvin M, Hungtinton T, Hasan M (2008) A review on the culture, production and use of Spirulina as food for humans and feeds for domestic animals and fish. Food and Agriculture Organization of the United Nations. Rome, Italy
  • Hardisson A, Revert C, González-Weller D, Gutiérrez A, Paz S, Rubio C (2017) Aluminium exposure through the diet. HSOA Food Sci Nutr 3(2):1–11
  • Huang H, Liao D, Pu R, Cui Y (2018) Quantifying the effects of spirulina supplementation on plasma lipid and glucose concentrations, body weight, and blood pressure. Diab Metab Synd Obes 11:729–742
  • IARC (International Agency for Research on Cancer) (2020) Agents classified by the IARC monographs. Volumes 1–125.
  • IOM (Institute of Medicine) (2001) Food and Nutrition Board of the Institute of Medicine of the National Academies. Dietary reference intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. In: National Academy Press. USA, Washington
  • IUPAC (International Union of Pure and Applied Chemistry) (1995) Nomenclature in evaluation of analytical methods including detection and quantification capabilities. Pure Appl Chem 67:1699–1723
  • Kalafati M, Jamurtas A, Nikolaidis M, Paschalis V, Theodorous A, Sakellariou G et al (2010) Ergogenic and antioxidant effects of spirulina supplementation in humans. Med Sci Sports Exerc 42(1):142–151
  • Khan N, Ryu KY, Choi JY, Nho EY, Habte G, Choi H, Kim MH, Park KS, Kim KS (2015) Determination of toxic heavy metals and speciation of arsenic in seaweeds from South Korea. Food Chem 169:464–470
  • Li G, Schoneker D, Ulman KL, Sturm JJ, Thackery LM, Kauffman JF (2015) Elemental impurities in pharmaceutical excipients. J Pharm Sci 104(12):4197–4206
  • Lupatini AL, Colla LM, Canan C, Colla E (2017) Potential application of microalga Spirulina platensis as a protein source. J Sci Food Agric 97:724–732
  • Nasirian F, Dadkhah M, Moradi-kor N, Obeidavi Z (2018) Effects of Spirulina platensis microalgae on antioxidant and anti-imflamatory factors in diabetic rats. Diab Metab Synd Obes 11:375–380
  • Nielsen SP (2004) The biological role of strontium. Bone 35:583–588
  • Ortiz-Villota MT, Romero-Morales MA, Meza-Rodríguez LD (2018) La biorremediación con microalgas (Spirulina máxima, Spirulina platensis y Chlorella vulgaris) como alternativa para tratar la eutrofización de la laguna de Ubaque, Colombia. Rev Invest Des Innov 9(1):163–176. https://doi.org/10.19053/20278306.v9.n1.2018.8153
  • Paz S, Rubio C, Frías I, Luis-González G, Gutiérrez AJ, González-Weller D, Hardisson A (2019a) Human exposure assessment to macro- and trace elements in the most consumed edible seaweeds in Europe. Environ Sci Pollut Res 26:36478–36485
  • Paz S, Rubio C, Frías I, Gutiérrez AJ, González-Weller D, Martín V, Revert C, Hardisson A (2019b) Toxic metals (Al, Cd, Pb and Hg) in the most consumed edible seaweeds in Europe. Chemosphere 218:879–884
  • Ramírez-Moreno L, Olvera-Ramírez R (2006) Uso tradicional y actual de Spirulina sp. (Arthrospira sp.). Interciencia 31(9):657–663
  • Razali NM, Wah YB (2011) Power comparisons of Shapiro-Wilk, Kolmogorov-Smirnov, Lilliefors and Anderson-Darling tests. J Stat Model Anal 2:21–33
  • Rubio C, Napoleone G, Luis-González G, Gutiérrez AJ, González-Weller D, Hardisson A, Revert C (2017) Metals in edible seaweed. Chemosphere 173:572–579
  • Sayadi MH, Rashki O, Shahri E (2019) Application of modified Spirulina platensis and Chlorella vulgaris powder on the adsorption of heavy metals from aqueous solution. J Environ Chem Engin 7:103169
  • SCHER (Scientific Committee on Health and Environmental Risk) (2012) Assessment of the tolerable daily intake of barium. European Commission. 10.2772/49651
  • Selmi C, Leung P, Fischer L, German B, Yang C, Kenny T et al (2011) The effects of Spirulina on anemia and immune function in senior citizens. Cell Mol Inmunol 8(3):248–254
  • Serfor-Armah Y, Nyarko BJB, Osae EK, Carboo D, Arnim-Sampong S, Seku F (2001) Rhodophyta seaweed species as bioindicators for monitoring toxic element pollutants in the marine ecosystem of Ghana. Water Air Soil Pollut 127:243–253
  • Singh NK, Raghubanshi AS, Upadhyay AK, Rai UN (2016) Arsenic and other heavy metal accumulation in plants and algae growing naturally in contaminated area of West Bengal, India. Ecotox Environ Safe 130:224–233
  • Sjögren B, Iregren A, Elinder CG, Yokel RA (2007) Chapter 17: Aluminum. In: Nordberg GF, Fowler BA, Nordberg M, Friberg L (eds) Handbook on the Toxicology of Metals, 3rd edn. Academic Press, Netherlands
  • Smith JL, Summers G, Wong R (2010) Nutrient and heavy metal content of edible seaweeds in New Zealand. New Zea J Crop Horticul Sci 38(1):19–28
  • Soni RA, Sudhakar K, Rana RS (2017) Spirulina – From growth to nutritional product: A review. Trends Food Sci Technol 69:157–171
  • WHO (World Health Organization) (2010) Strontium and strontium compound. Concise International Chemical Assessment Document 77: 1-63.
  • Wu Q, Liu L, Miron A, Klímová B, Wan D, Kuc K (2016) The antioxidant, immunomodulatory, and anti-inflammatory activities of Spirulina: an overview. Arch Toxicol 90:1817–1840. https://doi.org/10.1007/s00204-016-1744-5
  • Yamanappa W, Sudeep P, Sabu MK, Rajan J (2018) Non-local means image denoising using Shapiro-Wilk Similarity measure. IEEE Access 1(6):66914–66922