Advertisement

Essential and toxic elements in commercial microalgal food supplements

  • Piotr Rzymski
  • Joanna Budzulak
  • Przemysław Niedzielski
  • Piotr Klimaszyk
  • Jędrzej Proch
  • Lidia Kozak
  • Barbara Poniedziałek
Open Access
Article

Abstract

Arthrospira spp. (known commercially as Spirulina) and Chlorella spp., valued for their evidence-based nutritional and bioactive properties, are cultivated for the purpose of production of food supplements for worldwide distribution. However, the quality and safety of the final product depends on culturing and manufacturing conditions. The present study investigated the content of toxic elements (As species, Al, Cd, Hg, Ni, Pt, Pb, Cr (VI), rare earth elements) and minerals (Ca, Co, Cr, Cu, Fe, K, Na, Mg, Mn, P, Zn) in Chlorella (n = 10) and Spirulina (n = 13) food supplements registered in the European Union. Considering the most common recommended daily dosage 3.0, supplementation with any of the studied product would contribute significantly to mineral intake, with the exception of Fe which was found at high but acceptable levels in both Spirulina and Chlorella formulas. The majority of products revealed agreement between factual mineral content and that declared on the label, the only exception being Cu content in Chlorella products found to be significantly higher (> 130%). All studied supplements were found to have Cd, Hg, and Ni levels much below safety limits, although selected ones were characterized by increased content of Al, Pb, and inorganic As. No hexavalent Cr was detected in the studied products. The study highlights that microalgal supplements can be safe for consumers if appropriate measures are taken to ensure consumer safety, although it underlines the continuous need to monitor these products in order to fully eliminate those of low quality.

Keywords

Microalgal supplements Spirulina Chlorella Mineral content Contamination Metals Food safety Food quality 

Introduction

The market of food supplements is on the rise, with increasing numbers of individuals interested in using these formulas for various purposes in Europe, the USA, and Asia. There is particular interest in targeting those products that are based on ingredients of natural origin (Kennedy 2005; Hirayama et al. 2008; Bailey et al. 2013). Within this group, supplements that are based on microalgal biomass are not only gaining economic attention, but at the same time, their bioactive properties are being extensively explored using complementary research models: in vitro and in in vivo experiments, and randomized, placebo-controlled clinical trials involving different groups of patients (Panahi et al. 2016; de la Jara et al. 2018). These products use biomass of cyanobacteria belonging to the genera of Arthrospira (known commercially as Spirulina), Nostoc, and the former “Aphanizomenon,” and green algae representing the genera Haematococcus, Dunaliella, and Chlorella (Pulz and Gross 2004). The greatest market success has been achieved by Spirulina and Chlorella formulas, with the main cultivation plants located in the USA and Asia, particularly in China, the current leader in global microalgal biomass production (García et al. 2017).

Spirulina- and Chlorella-based products are known to be a rich source of proteins, fatty acids, pigments, minerals (e.g., calcium, magnesium, phosphorus, zinc, copper, and iron), digestive and restriction enzymes, and selected vitamins such as bioavailable forms of B12, C, and E (Buono et al. 2014; Wells et al. 2016). As evidenced using clinical trials, both supplements reveal promising bioactive properties encompassing immunomodulatory, antihypertensive, antilipidemic, and hypoglycemic effects (Nielsen et al. 2010; Kim et al. 2016; Juszkiewicz et al. 2018). This not only advocates the role of these products as functional foods but also supports their potential therapeutic use. For example, supplementation with Spirulina has been shown to decrease the viral load and increase CD4 cells in HIV-infected patients, modulate lipid metabolism, control appetite and promote weight loss in obese subjects (Zeinalian et al. 2017), and increase ability to resist mental and physical fatigue in men (Johnson et al. 2016), while Chlorella supplementation reveals a protective antioxidant effect in smokers (Panahi et al. 2013), may be efficiently used in adjunctive therapy for depressive disorders (Panahi et al. 2015), and to improve glycemic status in patients with non-alcoholic fatty liver disease (Ebrahimi-Mameghani et al. 2017).

There are no doubts that a biomedical exploration of the properties of Spirulina and Chlorella imparts a reliability to these products and helps to strengthen their market. It is, however, of high importance to ensure the safety of the final commercial product. Arthrospira spp. and Chlorella spp. are not known to produce any toxic compounds and their safety is well established (Buono et al. 2014; Wells et al. 2016; García et al. 2017). Nevertheless, one should note that cultivation of microalgae for scientific purposes may vary from that conducted on a large, commercial scale. Over recent years, the quality of selected microalgal supplements available in trade has been put in doubt due to the detection of cyanotoxins, e.g., neurotoxic anatoxin-a and β-methylamino-l-alanine, hepatotoxic microcystins resulting from alterations to culture purity and the co-occurrence of toxigenic species such as Microcystis aeruginosa (Vichi et al. 2012; Manali et al. 2017; Roy-Lachapelle et al. 2017). There have also been reports of increased levels of aluminium, lead, and inorganic arsenic, possibly as a consequence of the unsuitable location of cultivation ponds and the use of chemical methods to harvest biomass (Papazi et al. 2010; Hedegaard et al. 2013; Rzymski et al. 2015). However, some individuals, particularly those suffering from autoimmune disorders, can be specifically susceptible to microalgal supplements (Lee and Werth 2004), and it is likely that the occurrence of adverse effects such as diarrhea, nausea, abdominal pain, and skin rash reported after consumption of these products (Rzymski et al. 2015; Rzymski and Jaśkiewicz 2017) may have origins in their altered and imperfect quality. Therefore, it is imperative that the content of (potentially) toxic elements in these formulas be investigated, yet updated information in this regard is limited (Al-Dhabi 2013; Hedegaard et al. 2013; Rzymski et al. 2015).

Recent studies have shown that various food supplements such as multi-ingredient formulas can reveal high discrepancies between the factual nutritional value and that which is declared on the product label (Brandon et al. 2014; Niedzielski et al. 2016; Poniedziałek et al. 2018). Large-scale cultivation of microalgae for food production that most often employs raceway pond systems is prone to various environmental conditions, mitigation of which may be challenging. The nutritional value of produced biomass can be influenced by the presence and availability of certain compounds in cultivation medium. It is therefore of interest to examine whether the content of minerals declared on the labels of commercial microalgal supplements matches their factual levels within the accepted margin.

The aim of the present study was to assess the content of toxic metals (Al, Cd, Hg, Ni, Pb), hexavalent chromium, arsenic species, rare earth elements (REEs), and essential macro- and trace elements (Ca, Co, Cr, Cu, K, Mg, Mn, Mo, Na, Se, Fe, Zn) in Spirulina and Chlorella food supplements originating from different world regions and registered for distribution in the European Union. The determined levels of minerals were compared to those declared on the product labels.

Materials and methods

Food supplements

A total of 13 Spirulina-based and 10 Chlorella-based food supplements were randomly purchased from online stores. The inclusion criteria were official registration as a food supplement, country of origin declared on the label, powder or tablet form. The general characteristics of the studied products are given in Table 1. The following number of Spirulina and Chlorella products declared the content of the studied minerals on the label: Ca, 9 and 10; Cu, 9 and 8; K, 9 and 10; Mg, 10 each; Mn, 11 and 9; Fe, 11 and 10; Se, 3 and 1; Na, P, and Zn, 1 each 1; Cr and Mo, 1 and 0; Co, none.
Table 1

General characteristics of the studied group of microalgal food supplements (S, Spirulina; Ch, Chlorella)

Supplement

Declared species

Country of origin

Form

Daily dose recommendations

[g]

S-1

Spirulina sp.

China

Powder

4.0

S-2

Spirulina sp.

China

Powder

4.0

S-3

Spirulina sp.

China

Powder

1.5

S-4

Spirulina platensis

China

Powder

Not given

S-5

Spirulina sp.

Taiwan

Powder

3.0

S-6

Spirulina Pacifica

USA

Tablets

3.0

S-7

Arthrospira platensis

China

Powder

3.0

S-8

Spirulina platensis

China

Tablets

3.0

S-9

Spirulina sp.

China

Tablets

2.0–3.0

S-10

Spirulina maxima

China

Tablets

1.5

S-11

Spirulina sp.

China

Tablets

2.0

S-12

Spirulina sp.

China

Tablets

2.0

S-13

Spirulina sp.

India

Powder

5.0

Ch-1

Chlorella sp.

China

Tablets

3.0

Ch-2

Chlorella vulgaris

Taiwan

Tablets

3.0

Ch-3

Chlorella pyrenoidosa

Japan

Tablets

3.0

Ch-4

Chlorella sp.

India

Tablets

Not given

Ch-5

Chlorella sp.

China

Powder

2.0–3.0

Ch-6

Chlorella sp.

China

Powder

Not given

Ch-7

Chlorella pyrenoidosa

China

Powder

3.0

Ch-8

Chlorella vulgaris

China

Powder

3.0

Ch-9

Chlorella vulgaris

Portugal

Powder

0.6

Ch-10

Chlorella vulgaris

China

Tablets

3.0

Total element content analysis

The whole batch of each supplement was ground, thoroughly mixed, and weighed. Afterwards, 0.50 g of each formula was digested in 8 mL of suprapure HNO3 in closed Teflon vessels using the microwave sample digestion system Mars 6 (CEM, USA). The digestion procedure consisted of two steps: ramp to temperature 180 °C for 20 min and hold at 180 °C for 30 min. After digestion, the solution was diluted to a final volume of 15 mL with ultrapure water obtained in the Milli-Q system (Millipore, USA). Each supplement was prepared in triplicate.

The content of essential macroelements (Ca, Mg, K, Na, and P) and trace elements (Co, Cr, Cu, Mn, Mo, Se, Fe, and Zn), toxic metals (Al, Cd, Ni, Hg and Pb), light REEs (LREEs: Ce, Eu, Gd, La, Nd, Pr, Sc, Sm), and heavy REEs (HREEs: Dy, Er, Ho, Lu, Tb, Tm, Y, and Yb) was determined using the inductively coupled plasma optical emission spectrometer Agilent 5110 ICP-OES (Agilent, USA). ICP commercial analytical standards (Romil, England) were applied for the calibration. The following common instrumental parameters were used for determination of all elements: RF power 1.2 kW, plasma gas (argon) flow 12 L min−1, nebulizer gas (argon) flow 0.7 L min−1, axial plasma observation. The applied wavelengths (nm), limits of detection (mg kg−1), and levels of instrumental precision (%) for each determined element are summarized in Table S1. Traceability was checked using the standard reference materials: CRM S-1, CRM NCSDC (73349), CRM 2709, CRM 405, and CRM 667. The recovery (80–120%) was acceptable for all the elements determined.

Arsenic speciation analyses

To determine the inorganic and organic As content, 1.00 g of each supplement (homogenized by rubbing and sieving through a 0.02-mm sieve) was placed in a glass flask containing 10 mL 1 M phosphoric acid and several drops of Triton-100 and extracted in an ultrasonic bath (30 min at ambient temperature). Next, the solution was filtered using a paper filter (the filter was washed by 200 mL of water and 20 mL of phosphoric buffer). The pH of the solution was adjusted to 6–6.5 by the addition of 10 mol L−1 solution of NaOH, and finally, the solution was diluted to 20 mL with phosphate buffer. Each supplement was prepared in triplicate. The inorganic arsenic species, arsenite As (III) and arsenate As(V) in the acid extracts, were determined by HPLC–HG-ICP-OES immediately following the extraction procedure. The HPLC instrument was a liquid chromatograph (Shimadzu, Japan) with an anion-exchange column (Supelco, USA) LC-SAX1 (250 mm, 4.6 mm i.d.). The chromatographic run was isocratic at 3 mL min−1 of phosphate buffer (1 mmol L−1 Na2HPO4 and 10 mmol L−1 KH2PO4.2H2O) with an injection volume of 200 μL. PEEK (polyetheretherketone) tubing was inserted into a Tygon sleeve for transfer of the eluent from the LC column to the hydride generation unit. A spectrometer, model Agilent 5110 ICP-OES (Agilent, USA), with in-spray chamber generation of arsenic hydrides was used. For quantification, calibration curves based on the peak area for As (III) and As(V) were used. The final results were given as the mean concentration of As (III) and As(V); the remaining fraction (determined after ICP-OES analysis) was identified as organic As (Niedzielski et al. 2013).

Hexavalent chromium determination

To determine Cr (VI), the colorimetric method with 1,5-diphenylcarbazide was applied (Poniedziałek et al. 2018). For 2 mL of the sample extracted by 1 M phosphoric acid, several drops of 0.5% (m/m) solution of diphenylcarbazide in acetone were added. Each supplement was prepared in triplicate. The eventual presence of a red-colored complex of Cr (VI) was determined spectrophotometrically at 540 nm.

Statistical analyses and calculations

The results were analyzed using STATISTICA 10.0 software (StatSoft, USA). Because most of the data were not normally distributed (Shapiro-Wilk test, p < 0.05), the non-parametric Mann-Whitney U test was used for comparison in element content between Spirulina and Chlorella products. In all analyses, p < 0.05 was considered as statistically significant.

The content of Cd, Hg, and Pb was with maximum allowance levels set for FS by the European Commission, 1.0, 0.1, and 3.0 mg kg−1, respectively (Commission Regulation (EC) No 629/2008: amending Regulation (EC) No 1881/2006). The total content of REEs was confronted with a maximum allowance threshold of 7.0 mg kg−1 dry weight (equivalent to 0.7 mg kg−1 fresh weight) set by China, the only country yet to regulate REEs in foodstuffs (SAC 2012). The contents of Al and Ni were related to their Tolerable Weekly Intake (TWI) set by the European Food Safety Authority (EFSA) at 1.0 and 0.0195 mg kg-1body weight, respectively (EFSA 2008, 2015), assuming a daily consumption of 3.0 g of a supplement (the most common recommended dose, see Table 1) for a week by a 70-kg adult. Similarly, determined levels of essential elements were compared to Adequate Intake (AI) established by the EFSA (2017a). The following AI (per day) were assumed: Ca, 950 mg; P, 550 mg; Mg, 350 mg; Na, not set; K, 3500 mg; Cu, 1.6 mg; Cr, not set; Co, not set; Mn, 3.0 mg; Mo, 0.065 mg; Fe, 11 mg; Se, 0.07 mg; Zn, 11.7 mg. The determined content of Ca, Cu, K, Fe, Mg, and Mn was compared with that declared on the label. These minerals were selected because unlike Se, Na, P, Zn, Ce, Mo, and Co, these minerals were listed on the labels of the majority of the studied products. Seventy to 130% of declared value was considered as an acceptable margin (Niedzielski et al. 2016; Poniedziałek et al. 2018). In the case of As, the provisional Tolerable Weekly Intake (PTWI) established at a level of 15 μg kg−1 body weight (bw) of total As previously by the Joint FAO/WHO Expert Committee on Food Additives (JECFA 2012) has been disapproved by EFSA as inappropriate as adverse effects have been reported for exposures at lower levels of As. Instead, a benchmark dose lower confidence limit (BMDL01) was identified for cancers of the lung, skin, and bladder, as well as skin lesions, at a level of 0.3 μg kg−1 bw day−1 for an increased cancer risk at 1% (EFSA 2009), and the content of As in the studied supplements was related to this value, assuming a daily consumption of 3.0 g of a product by a 70-kg adult.

Results

Toxic elements

Aluminium

The mean ± SD (median) content of Al amounted to 2155.6 ± 1774.7 (1299.8) mg kg−1 in Spirulina supplements and did not differ significantly from that found in Chlorella preparations—1732.8 ± 1991.5 (1095.3) mg kg−1 (p > 0.05, Mann-Whitney U test). Three Spirulina and two Chlorella products whose weekly consumption at a daily dose of 3.0 g by a 70-kg adult would exceed TWI for Al were identified (Fig. 1).
Fig. 1

The content (mean ± SD) of Al (a), As species (b), and Ni (c) in Spirulina (left column; n = 13) and Chlorella (right column; n = 10) in food supplements. The red line represents Tolerable Weekly Intake (TWI) set by the EC considering a weekly consumption at a daily dose of 3.0 g by a 70-kg adult; the dashed red line represents Provisional Tolerable Weekly Intake (PTWI) set by the World Health Organization considering the same consumption as for TWI calculation. The dotted red line represents the Benchmark Dose Lower Confidence Limit (BMDL01) set for inorganic As at a consumption of 3.0 g of supplement by a 70-kg adult

Arsenic

The As content was below detection limits (0.1 mg kg−1) in six Spirulina (46.1%) and 5 Chlorella (50.0%) products. In other supplements, the following order of As species was found: As organic > As(V) > As (III), with sum of inorganic As ranging from 1.7–2.2 mg kg−1 in Spirulina and 2.3–2.7 mg kg−1 in Chlorella (Fig. 1). Considering the usual recommended daily dose of 3 g of supplement consumption, use of these products would lead to daily exposure to inorganic As at a level of 5.1–6.7 for Spirulina and 6.2–8.1 μg in the case of Chlorella. Such exposure would constitute respectively 24.3–31.9% and 29.5–38.6% of BMDL01 assuming consumption by a 70-kg adult.

Nickel

The Ni content in Spirulina and Chlorella supplements was comparable and amounted to a mean ± SD (median) of 1.52 ± 0.72 (1.33) and 1.38 ± 0.63 (1.29) mg kg−1, respectively. The highest content in the former group of products was 3.26 mg kg−1, and in the latter, 2.81 mg kg−1. Weekly supplementation with any studied supplement at a daily dose of 3.0 g by a 70-kg adult would not exceed 40% of the established TWI for Ni, and in most cases, it was lower than 20% of the TWI (Fig. 1).

Hexavalent chromium

The Cr (VI) content was below the limit of detection (0.01 mg kg−l) in all studied samples.

Cadmium

The Cd content in all tested products fell much below the maximum allowance level (1.0 mg kg−1) set by the European Commission (Fig. 2) and did not differ significantly between Spirulina- and Chlorella-based supplements (p > 0.05, Mann-Whitney U test) with mean ± SD (median) content amounting to 0.125 ± 0.055 (0.128) and 0.142 ± 0.071 (0.134) mg kg−1, respectively.
Fig. 2

Y-axis for b item in right column. It stated "Ni" but should state "Hg". The updated version, uploaded by me as an attachment, has this issue corrected."?>The content (mean ± SD) of Cd (a), Hg (b), and Pb (c) and Hg in Spirulina (left column; n = 13) and Chlorella (right column; n = 10) food supplements. The blue line represents maximum allowance limit for food supplements established by the European Commission. bdl, below detection limits

Mercury

Hg was detected in seven Spirulina (53.8%) and eight Chlorella (80.0%) food supplements at mean ± SD (median) levels of 0.027 ± 0.031 (0.022) and 0.41 ± 0.017 (0.042), respectively, not differing significantly from each other (p > 0.05, Mann-Whitney U test). Most of the tested products revealed Hg content much below the maximum allowance level set for food supplements by the European Commission (Fig. 2).

Lead

The mean ± SD (median) content of Pb in Spirulina and Chlorella supplements was 2.6 ± 1.9 (2.3) and 2.6 ± 1.3 (2.1) and did not differ significantly (p > 0.05, Mann-Whitney U test). Four Chlorella (40%) and five Spirulina (30.8%) products exceeded the maximum allowance level of Pb (3.0 mg kg−1) set by the European Commission, with one Chlorella supplement exceeding it over 2-fold (Fig. 2).

Rare earth elements

The total mean ± SD (median) content of REEs in Spirulina and Chlorella was 2.14 ± 1.89 (1.25) and 2.03 ± 11.28 (1.63) mg kg−1, respectively. A significantly higher content of LREEs was noted in both product groups (p < 0.05, Mann-Whitney U test) with a mean LREEs:HREEs ratio of 4:1. The maximum allowed REE content (7.0 mg kg−1 dw) was exceeded by only one Spirulina product (Table 2).
Table 2

Mean content (mg kg−1) of rare earth elements (REEs) in Spirulina (n = 13) and Chlorella (n = 10) supplements

 

Light REEs

Heavy REEs

 

Spirulina supplements (n = 13)

 

La

Ce

Eu

Gd

Nd

Pr

Sm

Sc

Dy

Er

Ho

Lu

Tb

Tm

Y

Yb

ΣREEs

 S1

0.254

0.013

0.004

0.111

0.153

0.514

n.d.

0.059

n.d.

0.005

n.d.

n.d.

n.d.

0.014

0.101

0.025

1.253

 S2

0.096

0.011

0.003

0.109

0.155

0.512

n.d.

0.049

n.d.

n.d.

0.004

n.d.

n.d.

0.027

0.112

0.029

1.107

 S3

0.335

0.058

0.014

0.177

0.338

0.428

0.007

0.109

0.034

0.036

0.019

n.d.

n.d.

0.007

0.362

0.056

1.980

 S4

0.094

0.015

0.003

0.080

0.147

0.363

n.d.

0.142

0.043

n.d.

0.012

n.d.

n.d.

n.d.

0.157

0.033

1.089

 S5

0.061

0.005

n.d.

0.092

0.104

0.380

n.d.

0.025

n.d.

n.d.

0.014

n.d.

n.d.

n.d.

0.026

0.012

0.719

 S6

0.190

0.100

0.036

0.279

0.246

0.742

n.d.

0.146

0.029

0.035

0.021

0.008

0.014

0.047

0.938

0.099

2.930

 S7

0.097

0.017

n.d.

0.086

0.166

0.437

n.d.

0.041

n.d.

n.d.

0.015

n.d.

n.d.

n.d.

0.051

0.013

0.923

 S8

0.201

0.035

n.d.

0.076

0.286

6.793

n.d.

0.051

n.d.

0.004

n.d.

n.d.

0.116

0.005

0.307

0.019

7.893

 S9

0.084

0.014

0.007

0.119

0.169

0.604

n.d.

0.053

n.d.

0.003

0.009

n.d.

n.d.

0.033

0.098

0.025

1.218

 S10

0.189

0.030

0.009

0.135

0.217

0.406

n.d.

0.058

n.d.

0.004

0.028

n.d.

0.011

n.d.

0.122

0.024

1.233

 S11

0.532

0.005

0.005

0.095

0.131

0.639

n.d.

0.065

0.028

n.d.

0.037

n.d.

0.006

0.007

0.026

0.005

1.581

 S12

0.367

0.068

0.014

0.219

0.404

0.550

n.d.

0.119

0.021

0.004

n.d.

n.d.

0.008

0.058

0.183

0.034

2.049

 S13

0.502

0.095

0.029

0.184

0.571

0.812

n.d.

0.172

0.087

0.033

n.d.

n.d.

0.007

0.030

0.537

0.053

3.112

 Mean (SD)

0.231 (0.159)

0.036 (0.034)

0.012 (0.011)

0.136 (0.062)

0.237 (0.133)

1.01 (1.74)

0.084 (0.047)

0.040 (0.024)

0.016 (0.016)

0.018 (0.010)

0.027 (0.044)

0.025 (0.019)

0.232 (0.258)

0.033 (0.025)

2.14 (1.895)

Chlorella supplements (n = 10)

 Ch1

0.743

1.174

0.026

0.312

0.817

0.836

n.d.

0.284

0.120

0.100

n.d.

0.052

0.087

0.072

0.736

0.116

5.475

 Ch2

0.085

0.024

0.004

0.147

0.266

0.471

n.d.

0.011

n.d.

0.011

n.d.

0.036

0.049

n.d.

0.045

0.018

1.167

 Ch3

0.150

0.121

0.018

0.238

0.240

0.514

n.d.

0.007

n.d.

n.d.

0.016

0.034

0.037

n.d.

0.036

0.028

1.439

 Ch 4

0.353

0.557

0.019

0.148

0.382

0.903

n.d.

0.154

0.022

0.022

n.d.

0.021

0.017

n.d.

0.112

0.022

2.732

 Ch 5

0.109

0.153

0.014

0.184

0.235

0.717

n.d.

0.036

n.d.

0.013

0.027

0.033

0.026

n.d.

0.066

0.028

1.641

 Ch 6

0.082

0.104

0.021

0.173

0.203

0.508

n.d.

0.019

n.d.

n.d.

0.022

0.028

0.027

n.d.

0.042

0.022

1.251

 Ch 7

0.090

0.134

0.021

0.171

0.224

0.831

n.d.

0.020

n.d.

0.010

0.007

0.028

0.019

n.d.

0.044

0.021

1.62

 Ch 8

0.084

0.110

0.017

0.138

0.232

0.960

n.d.

0.046

n.d.

0.005

n.d.

0.024

0.036

n.d.

0.071

0.021

1.744

 Ch 9

0.042

0.138

n.d.

0.083

0.219

1.108

n.d.

n.d.

n.d.

0.022

n.d.

0.050

0.035

n.d.

0.008

0.012

1.717

 Ch 10

0.160

0.237

0.007

0.072

0.261

0.448

n.d.

0.092

0.024

0.008

n.d.

0.033

0.021

n.d.

0.110

0.022

1.495

 Mean (SD)

0.190 (0.213)

0.275 (0.347)

0.016 (0.007)

0.167 (0.070)

0.308 (0.186)

0.730 (0.233)

0.074 (0.092)

0.055 (0.056)

0.024 (0.031)

0.018 (0.009)

0.034 (0.021)

0.035 (0.021)

0.127 (0.216)

0.031 (0.030)

2.028 (1.284)

n.d. not detected; SD standard deviation

Essential elements

Macroelements

The content of macroelements in Spirulina and Chlorella food supplements is summarized in Table 3. Their mean content decreased in the order K > Ca > P > Na > Mg for Spirulina products and K > P > Ca > Na > Mg for Chlorella supplements. A significantly higher content of Ca was observed for Spirulina products while Chlorella displayed a greater P level. In the case of most products, consumption of the most commonly recommended daily dose of 3.0 g would not lead to their significant intake (Table 3). Most of the studied supplements revealed an agreement between factual and declared content of Ca, K, and Mg (Fig. 3).
Table 3

The content of macroelements and trace elements in Spirulina (n = 13) and Chlorella (n = 10) food supplements. The reported p value is for Mann-Whitney U test. Percentage of Adequate Intake (%AI) established by the European Food Safety Authority was calculated assuming a daily consumption of 3.0 g dose of a supplement

  

Mean ± SD (median)

Min–max

p

%AI

Macroelements

 

[g kg−1]

 

Mean (min–max)

 Ca

Spirulina

12.5 ± 32.1 (3.3)

2.2–119.3

*

3.9 (0.7–37.6)

Chlorella

5.9 ± 2.6 (5.4)

2.9–12.3

1.9 (0.9–3.9)

 P

Spirulina

11.9 ± 14.1 (8.3)

6.6–58.7

***

6.5 (3.6–32.0)

Chlorella

12.4 ± 3.8 (11.8)

5.0–18.6

6.7 (2.7–10.1)

 Mg

Spirulina

3.4 ± 1.3 (2.9)

1.9–6.6

n.s.

2.9 (1.6–5.6)

Chlorella

3.5 ± 1.8 (3.3)

1.3–6.3

3.0 (1.1–5.4)

 Na

Spirulina

11.0 ± 6.6 (10.4)

4.2–28.1

*

Chlorella

5.0 ± 4.8 (3.3)

0.5–13.2

 K

Spirulina

15.7 ± 2.8 (16.0)

8.5–20.9

n.s.

1.3 (0.7–1.8)

Chlorella

14.5 ± 4.5 (12.4)

9.8–23.0

1.2 (0.8–2.0)

Trace elements

 

[mg kg−1]

 

Mean (min–max)

 Co

Spirulina

1.0 ± 2.5 (0.3)

0.08–9.4

n.s.

Chlorella

0.2 ± 0.09 (0.21)

0.07–0.39

 Cr

Spirulina

3.6 ± 6.3 (1.6)

0.6–24.4

n.s.

Chlorella

2.5 ± 1.3 (2.3)

1.1–4.8

 Cu

Spirulina

4.4 ± 4.5 (2.4)

0.9–15.1

**

0.8 (0.2–2.8)

Chlorella

10.1 ± 8.8 (6.3)

2.6–29.4

1.9 (0.5–5.5)

 Fe

Spirulina

994.7 ± 475.8 (873.6)

368.5–2286.6

n.s.

27.1 (10.0–62.3)

Chlorella

1045.9 ± 382.3 (1121.0)

438.4–1661.5

28.5 (11.9–45.3)

 Mn

Spirulina

45.8 ± 25.7 (36.3)

26.1–109.8

n.s.

4.6 (2.6–11.0)

Chlorella

53.8 ± 14.1 (51.1)

24.2–74.6

5.4 (2.4–7.5)

 Mo

Spirulina

0.3 ± 0.2 (0.2)

0.09–0.90

n.s.

1.4 (0.4–4.1)

Chlorella

0.8 ± 1.8 (0.2)

0.14–5.8

3.7 (0.6–26.8)

 Se

Spirulina

0.3 ± 0.5 (0.1)

0.0–1.6

n.s.

1.3 (0.0–7.0)

Chlorella

0.7 ± 0.3 (0.8)

0.4–1.1

3.0 (1.7–4.7)

 Zn

Spirulina

23.2 ± 13.3 (19.7)

9.6–61.4

n.s.

0.6 (0.2–1.6)

Chlorella

28.4 ± 16.9 (23.3)

11.2–73.5

0.7 (0.3–1.9)

n.s. not significant (p > 0.05)

*p < 0.05; ** p < 0.01; *** p < 0.001

Fig. 3

The content of Ca, Cu, K, Mg, Mn, and Fe determined in Spirulina (left) and Chlorella (right) food supplements presented as a percentage of the content declared on the label

Trace elements

The mean content of trace elements decreased in the following order: Fe > Mn > Zn > Cu > Cr > Co > Mo = Se in Spirulina supplements and Fe > Mn > Zn > Cu > Cr > Mo > Se > Co in Chlorella products. Their contents, which are summarized in Table 3, did not differ between Spirulina and Chlorella products, except for Cu levels being significantly higher in the latter. They were also mostly low when compared with AI values by assuming a daily consumption of a 3.0-g dose. The only exception was the level of Fe which in a similar scenario would be provided at over 25% of AI on average, with some Spirulina and Chlorella supplements providing even substantially more (Table 3). For the majority of Spirulina products, the factual and declared content of Cu, Mn, and Fe was found to correspond very closely. In the case of Chlorella supplements, larger discrepancies were noted, particularly with respect to Cu content, which was found to significantly exceed the value declared on the label (Fig. 3).

Discussion

Considering the biological activities of Spirulina and Chlorella food supplements, now evidenced also on a clinical level, it is expected that the market for these products will continue to develop. Thus, it is imperative to ensure that the quality of the final product is high and safe for consumers through, e.g., implementation of a food safety management system according to ISO 22000, efficient enforcement of various food regulations, systematic monitoring of contaminant levels, and credibility of information declared on the product label (Fernández-Segovia et al. 2014; Poniedziałek et al. 2018). The present study is a comprehensive assessment of Spirulina and Chlorella food supplements registered for trade in the EU as regards levels of essential and (potentially) toxic elements.

A variable content of toxic elements was found in the investigated products. This particularly concerned Al whose levels notably differed between various products, reaching over 6000 mg kg−1 in selected ones. It has been previously reported that some microalgal food supplements can contain a high content of this element, most likely as a result of the use of aluminium chloride as a flocculant to harvest biomass (Papazi et al. 2010; Rzymski et al. 2015). Although inexpensive and efficient, such a method may contaminate the final product with Al at unsafe levels, exceeding maximum dietary tolerance thresholds (Rzymski et al. 2015). Despite the poor bioavailability of Al ingested orally, and that once absorbed most of its load is excreted readily with urine (Taylor et al. 1998), exposure to this element has greatly increased over the decades and is now estimated to reach annually as much as 11 kg per capita (Exley 2013). Therefore, an effort must be made to reduce its content in food, and setting a (still not established) maximum threshold level of Al in different foodstuffs (including food supplements) would be a beneficial step forward in this regard. Moreover, one should note that some individuals, particularly those with renal failure diseases, may be more prone to the toxic effects of Al due to its increased retention and consequently, bioaccumulation (Yokel and McNamara 2001). There are number of alternative methods, such as physical or biological flocculation, whose efficiency is reliable enough to be applied to the harvest of microalgal biomass (Salim et al. 2011; Vandamme et al. 2013; Choy et al. 2018), and because they do not lead to biomass contamination, their use is highly advised in the production of Spirulina and Chlorella food supplements.

Previous studies have already reported that some food supplements containing biomass (e.g., plant material) may reveal increased levels of toxic elements such as Cd or Pb. This is most probably due to contamination of the ambient environment from which the biomass was originally derived, and the bioaccumulation process. Some microalgae are also known for their tolerance and uptake of toxic metals so the chemical quality of the culture medium is likely to have a profound effect on the presence of contaminants in the produced supplement. Importantly, the present study found that Cd and Hg content in studied Spirulina and Chlorella formulas was much below the maximum allowance limits set for food supplements by the EFSA. However, the Pb levels in selected products, exceeding the allowance threshold of 3.0 mg kg−1, are rising concerns. Microalgae sequester Pb preferentially over other toxic metals, and additionally, Pb is more environmentally abundant than Cd or Hg—contamination with this element of microalgal biomass is therefore more plausible (Rzymski et al. 2014). The increased contents of this metal have previously been reported in Spirulina and Chlorella supplements implicated in cases of human intoxication; extracts of which revealed a cytotoxicity in vitro (although the causative agent was not unambiguously elucidated) (Rzymski et al. 2015). An effort is required to eliminate microalgal biomass contaminated significantly with Pb to decrease exposure and ensure consumer safety. One should, however, note that selected multi-ingredient food supplements that contain a mixture of vitamins and minerals have been reported to contain even greater Pb content (Poniedziałek et al. 2018). The potential monitoring enforcement should therefore encompass not only microalgal-based formulations but all food supplements.

Previous studies have shown that some food supplements may be contaminated with the hexavalent form of Cr (Martone et al. 2013) which is recognized as a human carcinogen (Sun et al. 2015). Thus, it remains important to screen microalgal products to exclude such contamination and, as shown in the present study, none of the Spirulina and Chlorella products contained detectable levels of the Cr (VI) form. The As speciation analyses revealed, in turn, that content of this metalloid (if detectable) was mostly constituted of an organic form that reveals low or even no toxicity for humans (Hughes 2002). This is in line with previous observations (Hsu et al. 2001; Hedegaard et al. 2013; Rzymski et al. 2015). However, one should note that selected Spirulina and Chlorella products had detectable levels of inorganic As species, particularly the As(V) form. According to the EFSA (2014), the mean daily exposure to inorganic As in Europe varies from 0.24 to 0.38 μg kg−1 bw per day for adults, equivalent to 16.8–26.6 μg of As per day for a 70-kg adult. This considered, use of a usual 3.0 g dose of supplements with detected inorganic As would contribute significantly to its exposure, although one should note that in any case, the BMDL01 value would be exceeded. There are currently no maximum limits for As in food supplements set in European Union—this study would suggest that the establishment of such limits would lead to the prevention of low-quality products from contaminating the market.

To the best of our knowledge, the present study is the first to analyze the level of REEs in microalgal food supplements. They represent an emerging group of pollutants whose emissions have risen over recent decades due to certain human activities (Pagano et al. 2015) resulting in increased human exposure via different routes (Poniedziałek et al. 2017). The outcomes of these exposures are yet to be fully explored, although selected REEs reveal cytotoxicity and have been potentially linked to anti-testicular effects, male sterility, hypertension in females, reduced IQ, and neurological alterations in children (Zhu et al. 1996; Marzec-Wróblewska et al. 2015; Wang et al. 2017; Gwenzi et al. 2018). Diet may constitute an important route of human exposure to REEs, and various foodstuffs such as mushrooms or vegetables already have been reported to exceed the maximum 0.7 mg kg−1 fresh weight (7.0 mg kg−1 dry weight) threshold limit, set so far only in China (SAC 2012; Li et al. 2013; Rzymski et al. 2017; Siwulski et al. 2017; Zhuang et al. 2017). Interestingly, some REEs, namely Ce, Gd, La, and Sc, have been reported to increase the growth of some microalgae and their content of lutein, violaxanthin, β-carotene, and chlorophylls (Goecke et al. 2017). Microalgae from the Arthrospira and Chlorella genera were also experimentally shown to bioconcentrate some REEs such as Ce or Nd (Sadovsky et al. 2016; Kücüker et al. 2017). In the present study, all studied microalgal food supplements, except for one product based on Spirulina (exceeding maximum allowance limit) and one based on Chlorella (reaching 78% of the limit), were characterized by a relatively low content of REEs. The highest share was represented by light REEs (with Pr reaching the highest mean content in Spirulina and Chlorella products) which are known to accumulate to a greater extent in the human body (Wei et al. 2013; Hao et al. 2015). All in all, the findings of the present study indicate that microalgal food supplements, with certain exceptions, do not represent a significant dietary source of REEs.

While Spirulina and Chlorella food products are known to contain a high content of proteins, polyunsaturated fatty acids, and various pigments, the nutritional value of their mineral content, both macro- and trace elements, is relatively low, particularly if one considers the most commonly recommended dose of 3.0 g daily. In this regard, they cannot compete with a number of other commonly eaten food products such as vegetables or fruits. On the other hand, the Tolerable Upper Intake Level (UL) and Safety Upper Level (SUL)/Guidance Level (GL) as set respectively by the EFSA (2017b) and the Expert Group on Vitamins and Minerals (2003) were not exceeded for any essential element considered by this study. This is an important finding as food supplements should only serve as an accessory source of nutrients in a balanced diet and not as their substitution. An excessive intake of minerals can lead to various adverse effects including neurotoxic responses (Mn), cardiotoxicity (Co), gastrointestinal symptoms (Cu, Fe, K, Mg), altered immune function (Zn), or unwanted cardiovascular events (Ca) (Verkaik-Kloosterman et al. 2012). One should note, however, that the studied Spirulina and Chlorella food supplements served as a rich source of Fe. On average, daily supplementation with the most commonly recommended dose of 3.0 g would constitute 25% of AI with some Spirulina and Chlorella products reaching over 60 and 40% of AI, respectively. As found in previous studies, bioavailability of Fe from Spirulina biomass (in which it is mostly present as ferrihydrite) is lower than that of ferrous sulfate, often used in mineral food supplements, but higher than that in whole wheat (Kapoor and Mehta 1992; Perfiliev et al. 2018). However, in the case of Fe-fortified Spirulina, mineral bioavailability can be even higher than that from meat products (Puyfoulhoux et al. 2001). Considering the Fe content in microalgal food supplement and the fact that they can contain bioavailable forms of vitamin B12 (Nakano et al. 2010; De et al. 2011; Merchant et al. 2015), these products are potentially of high interest to individuals on vegetarian diets which are becoming increasingly popular in different populations (Dinu et al. 2017). It would be therefore interesting to conduct a clinical trial investigating whether Spirulina supplementation may have a beneficial effect on Fe burden. Although one recent study has shown that such intervention unexpectedly decreased the concentration of serum Fe (Suliburska et al. 2016), one should note that this parameter alone, without assessing a number of other biochemical markers (e.g., transferrin, ferritin, hemoglobin, hepcidin, etc.), is not sufficient to evaluate Fe status in humans (Rzymski and Ganz 2018).

The nutritional value of the food supplement declared on the container label is an important factor in assisting the consumers’ decision-making processes when purchasing a product. A worrisome finding of some recent investigations is that actual declared levels of ingredients in various food supplements does not agree with their actual content, with the majority of investigated products being far from meeting the acceptable margin (Brandon et al. 2014; Niedzielski et al. 2016; Verkaik-Kloosterman et al. 2017; Poniedziałek et al. 2018). Contrary to this, most of the studied products revealed good agreement in this respect. This particularly concerned the content of Ca, K, Mg, Mn, and Fe in Spirulina supplements. Some discrepancies were found for some Chlorella products with most of those studied having a significantly higher content of Cu than that declared on the label. Although the origins of such an increased content of Cu levels can only be hypothesized, one should note that Cu compounds can be used in Chlorella cultures as selective inhibitors of some grazing rotifers which can occur in open pond cultivation systems and cause a significant economic loss (Pradeep et al. 2015; Day et al. 2017); such an application may significantly alter Cu content in the final food product.

Conclusion

In summary, the study screened the content of minerals and toxic elements in selected Spirulina and Chlorella food supplements registered on the European market and originating from Asia, North America, and Europe. Considering the most commonly recommended daily dose of 3 g, the use of such products would rather not contribute significantly to mineral intake, except for Fe whose levels were found to be high in both Spirulina and Chlorella formulas. An important finding is that most of the studied products revealed a good agreement between declared and factual content of elements. The microalgal food supplements appear not to contribute significantly to dietary intake of REEs. Even though some of the products screened by this study revealed increased levels of toxic metals such as Al or Pb, this should by no means be a reason to disregard the very promising bioactive properties of Arthrospira or Chlorella. It is rather an indication that the quality control of such products should be strengthened so that only those microalgal food supplements which ensure consumer safety can reach the market.

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10811_2018_1681_MOESM1_ESM.doc (46 kb)
ESM 1 (DOC 45 kb)

References

  1. Al-Dhabi NA (2013) Heavy metal analysis in commercial Spirulina products for human consumption. Saudi J Biol Sci 20:383–388CrossRefPubMedGoogle Scholar
  2. Bailey RL, Gahche JJ, Miller PE, Thomas PR, Dwyer JT (2013) Why US adults use food supplements. JAMA Intern Med 173:355–361CrossRefGoogle Scholar
  3. Brandon EF, Bakker MI, Kramer E, Bouwmeester H, Zuidema T, Alewijn M (2014) Bioaccessibility of vitamin A, vitamin C and folic acid from dietary supplements, fortified food and infant formula. Int J Food Sci Nutr 65:426–435CrossRefGoogle Scholar
  4. Buono S, Langellotti AL, Martello A, Rinna F, Fogliano V (2014) Functional ingredients from microalgae. Food Funct 58:1669–1685CrossRefGoogle Scholar
  5. Choy SY, Prasad KMN, Wu TY, Raghunandan ME, Phang S-M, Juan JC, Ramanan RN (2018) Separation of Chlorella biomass from culture medium by flocculation with rice starch. Algal Res 30:162–172CrossRefGoogle Scholar
  6. Commission Regulation (EC) No 629/2008 of 2 July 2008 amending Regulation (EC) No 1881/2006 setting maximum levels for certain contaminants in foodstuffsGoogle Scholar
  7. Day JG, Gong Y, Hu Q (2017) Microzooplanktonic grazers–a potentially devastating threat to the commercial success of microalgal mass culture. Algal Res 27:356–365CrossRefGoogle Scholar
  8. de la Jara A, Ruano-Rodriguez C, Polifrone M, Assunçao P, Brito-Casillas Y, Wägner AM, Serra-Majem L (2018) Impact of dietary Arthrospira (Spirulina) biomass consumption on human health: main health targets and systematic review. J Appl Phycol 30:2403–2423CrossRefGoogle Scholar
  9. De M, Halder A, Chakraborty T, Das U, Paul S, De A, Banerjee J, Chatterjee T, De S (2011) Incidence of anemia and effect of nutritional supplementation on women in rural and tribal populations of eastern and northeastern India. Hematology 16:190–192CrossRefGoogle Scholar
  10. Dinu M, Abbate R, Gensini GF, Casini A, Sofi F (2017) Vegetarian, vegan diets and multiple health outcomes: a systematic review with meta-analysis of observational studies. Crit Rev Food Sci Nutr 57:3640–3649CrossRefGoogle Scholar
  11. Ebrahimi-Mameghani M, Sadeghi Z, Abbasalizad Farhangi M, Vaghef-Mehrabany E, Aliashrafi S (2017) Glucose homeostasis, insulin resistance and inflammatory biomarkers in patients with non-alcoholic fatty liver disease: beneficial effects of supplementation with microalgae Chlorella vulgaris: a double-blind placebo-controlled randomized clinical trial. Clin Nutr 36:1001–1006CrossRefGoogle Scholar
  12. EFSA (2008) Safety of aluminium from dietary intake - Scientific opinion of the Panel on Food Additives, Flavourings, Processing Aids and Food Contact Materials (AFC). EFSA J 754:1–34Google Scholar
  13. EFSA (2009) Scientific opinion on arsenic in food. EFSA Panel on Contaminants in the Food Chain (CONTAM). EFSA J 7:1351CrossRefGoogle Scholar
  14. EFSA (2014) Dietary exposure to inorganic arsenic in the European population. EFSA J 12:3597Google Scholar
  15. EFSA (2015) Scientific opinion on the risks to public health related to the presence of nickel in food and drinking water. EFSA J 13:4002Google Scholar
  16. EFSA (2017a) Dietary reference values for nutrients. Summary report. EFSA supporting publication.  https://doi.org/10.2903/sp.efsa.2017.e15121
  17. EFSA (2017b) Overview on Tolerable Upper Intake Levels as derived by the Scientific Committee on Food (SCF) and the EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA) https://www.efsa.europa.eu/sites/default/files/assets/UL_Summary_tables.pdf. Accessed 21 October 2018
  18. Exley C (2013) Human exposure to aluminium. Environ Sci Process Impacts 15:1807–1816CrossRefGoogle Scholar
  19. Fernández-Segovia I, Pérez-Llácer A, Peidro B, Fuentes A (2014) Implementation of a food safety management system according to ISO 22000 in the food supplement industry: a case study. Food Control 43:28–34CrossRefGoogle Scholar
  20. García JL, de Vicente M, Galán B (2017) Microalgae, old sustainable food and fashion nutraceuticals. Microb Biotechnol 10:1017–1024CrossRefPubMedGoogle Scholar
  21. Goecke F, Vítová M, Lukavský J, Nedbalová L, Řezanka T, Zachleder V (2017) Effects of rare earth elements on growth rate, lipids, fatty acids and pigments in microalgae. Phycol Res 65:226–234CrossRefGoogle Scholar
  22. Gwenzi W, Mangori L, Danha C, Chaukura N, Dunjana N, Sanganyado E (2018) Sources, behaviour, and environmental and human health risks of high-technology rare earth elements as emerging contaminants. Sci Total Environ 636:299–313CrossRefGoogle Scholar
  23. Hao Z, Li Y, Li H, Wei B, Liao X, Liang T, Yu J (2015) Levels of rare earth elements, heavy metals and uranium in a population living in Baiyun Obo, Inner Mongolia, China: a pilot study. Chemosphere 128:161–170CrossRefGoogle Scholar
  24. Hedegaard R, Rokkjær I, Sloth JJ (2013) Total and inorganic arsenic in dietary supplements based on herbs, other botanicals and algae—a possible contributor to inorganic arsenic exposure. Anal Bioanal Chem 405:4429–4435CrossRefGoogle Scholar
  25. Hirayama F, Lee AH, Binns CW, Watanabe F, Ogawa T (2008) Food supplementation by older adults in Japan. Asia Pac J Clin Nutr 17:280–284Google Scholar
  26. Hsu Y-M, Hwang J-M, Yeh T-R (2001) Inorganic elements determination for algae/Spirulina food marketed in Taiwan. J Food Drug Anal 9:178–182Google Scholar
  27. Hughes MF (2002) Arsenic toxicity and potential mechanisms of action. Toxicol Lett 133:1–16CrossRefGoogle Scholar
  28. JECFA (2012) Safety evaluation of certain food additives/prepared by the seventy fourth meeting of the Joint FAO/WHO Expert Committee on Food Additives (JECFA) WHO Food Additives Series, vol 65Google Scholar
  29. Johnson M, Hassinger L, Davis J, Devor ST, DiSilvestro RA (2016) A randomized, double blind, placebo controlled study of Spirulina supplementation on indices of mental and physical fatigue in men. Int J Food Sci Nutr 67:203–206CrossRefGoogle Scholar
  30. Juszkiewicz A, Basta P, Petriczko E, Machaliński B, Trzeciak J, Łuczkowska K, Skarpańska-Stejnborn A (2018) An attempt to induce an immunomodulatory effect in rowers with Spirulina extract. J Int Soc Sports Nutr 15:9CrossRefPubMedGoogle Scholar
  31. Kapoor R, Mehta U (1992) Iron bioavailability from Spirulina platensis, whole egg and whole wheat. Indian J Exp Biol 30:904–907PubMedGoogle Scholar
  32. Kennedy J (2005) Herb and supplement use in the US adult population. Clin Ther 27:1847–1858CrossRefPubMedGoogle Scholar
  33. Kim S, Kim J, Lim Y, Kim YJ, Kim JY, Kwon O (2016) A dietary cholesterol challenge study to assess Chlorella supplementation in maintaining healthy lipid levels in adults: a double-blinded, randomized, placebo-controlled study. Nutr J 15:54CrossRefPubMedGoogle Scholar
  34. Kücüker MA, Wieczorek N, Kuchta K, Copty NK (2017) Biosorption of neodymium on Chlorella vulgaris in aqueous solution obtained from hard disk drive magnets. PLoS One 12:e0175255CrossRefPubMedGoogle Scholar
  35. Lee AN, Werth VP (2004) Activation of autoimmunity following use of immunostimulatory herbal supplements. Arch Dermatol 140:723–727CrossRefGoogle Scholar
  36. Li X, Chen Z, Chen Z, Zhang Y (2013) A human health risk assessment of rare earth elements in soil and vegetables from a mining area in Fujian Province, Southeast China. Chemosphere 93:1240–1246CrossRefGoogle Scholar
  37. Manali KM, Arunraj R, Kumar T, Ramya M (2017) Detection of microcystin producing cyanobacteria in Spirulina dietary supplements using multiplex HRM quantitative PCR. J Appl Phycol 29:1279–1286CrossRefGoogle Scholar
  38. Martone N, Rahman GM, Pamuku M, Kingston HM (2013) Determination of chromium species in food supplements using speciated isotope dilution mass spectrometry with mass balance. J Agric Food Chem 61:9966–9976CrossRefGoogle Scholar
  39. Marzec-Wróblewska U, Kamiński P, Łakota P, Ludwikowski G, Szymański M, Wasilow K, Stuczyński T, Buciński A, Jerzak L (2015) Determination of rare earth elements in human sperm and association with semen quality. Arch Environ Contam Toxicol 69:191–201CrossRefPubMedGoogle Scholar
  40. Merchant RE, Phillips TW, Udani J (2015) Nutritional supplementation with Chlorella pyrenoidosa lowers serum methylmalonic acid in vegans and vegetarians with a suspected vitamin B12 deficiency. J Med Food 18:1357–1362CrossRefGoogle Scholar
  41. Nakano S, Takekoshi H, Nakano M (2010) Chlorella pyrenoidosa supplementation reduces the risk of anemia, proteinuria and edema in pregnant women. Plant Foods Hum Nutr 65:25–30CrossRefGoogle Scholar
  42. Niedzielski P, Mleczek M, Magdziak Z, Siwulski M, Kozak L (2013) Selected arsenic species: As (III), As(V) and dimethylarsenic acid (DMAA) in Xerocomus badius fruiting bodies. Food Chem 141:3571–3577CrossRefGoogle Scholar
  43. Niedzielski P, Rudnicka M, Wachelka M, Kozak L, Rzany M, Wozniak M, Kaskow Z (2016) Selenium species in selenium fortified food supplements. Food Chem 190:454–459CrossRefGoogle Scholar
  44. Nielsen CH, Balachandran P, Christensen O, Pugh ND, Tamta H, Sufka KJ, Wu X, Walsted A, Schjørring-Thyssen M, Enevold C, Pasco DS (2010) Enhancement of natural killer cell activity in healthy subjects by Immulina®, a Spirulina extract enriched for Braun-type lipoproteins. Planta Med 76:1802–1808CrossRefGoogle Scholar
  45. Pagano G, Aliberti F, Guida M, Oral R, Siciliano A, Trifuoggi M, Tommasi F (2015) Rare earth elements in human and animal health: state of art and research priorities. Environ Res 142:215–220CrossRefGoogle Scholar
  46. Panahi Y, Mostafazadeh B, Abrishami A, Saadat A, Beiraghdar F, Tavana S, Pishgoo B, Parvin S, Sahebkar A (2013) Investigation of the effects of Chlorella vulgaris supplementation on the modulation of oxidative stress in apparently healthy smokers. Clin Lab 59:579–587Google Scholar
  47. Panahi Y, Badeli R, Karami GR, Badeli Z, Sahebkar A (2015) A randomized controlled trial of 6-week Chlorella vulgaris supplementation in patients with major depressive disorder. Complement Ther Med 23:598–602CrossRefGoogle Scholar
  48. Panahi Y, Darvishi B, Jowzi N, Beiraghdar F, Sahebkar A (2016) Chlorella vulgaris: a multifunctional dietary supplement with diverse medicinal properties. Curr Pharm Des 22:164–173CrossRefGoogle Scholar
  49. Papazi A, Makridis P, Divanach P (2010) Harvesting Chlorella minutissima using cell coagulants. J Appl Phycol 22:349–355CrossRefGoogle Scholar
  50. Perfiliev YD, Tambiev AK, Konnychev MA, Skalny AV, Lobakova ES, Kirpichnikov MP (2018) Mössbauer spectroscopic study of transformations of iron species by the cyanobacterium Arthrospira platensis (formerly Spirulina platensis). J Trace Elem Med Biol 48:105–110CrossRefGoogle Scholar
  51. Poniedziałek B, Rzymski P, Pięt M, Niedzielski P, Mleczek M, Wilczak M, Rzymski P (2017) Rare-earth elements in human colostrum milk. Environ Sci Pollut Res 24:26148–26154CrossRefGoogle Scholar
  52. Poniedziałek B, Niedzielski P, Kozak L, Rzymski P, Wachelka M, Rzymska I, Karczewski J, Rzymski P (2018) Monitoring of essential and toxic elements in multi-ingredient food supplements produced in European Union. Journal of Consumer Protection and Food Safety 13(1):41–48Google Scholar
  53. Pradeep V, Van Ginkel SW, Park S, Igou T, Yi C, Fu H, Johnston R, Snell T, Chen Y (2015) Use of copper to selectively inhibit Brachionus calyciflorus (predator) growth in Chlorella kessleri (prey) mass cultures for algae biodiesel production. Int J Mol Sci 16:20674–20684CrossRefPubMedGoogle Scholar
  54. Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–648CrossRefGoogle Scholar
  55. Puyfoulhoux G, Rouanet JM, Besançon P, Baroux B, Baccou JC, Caporiccio B (2001) Iron availability from iron-fortified Spirulina by an in vitro digestion/Caco-2 cell culture model. J Agric Food Chem 49:1625–1629CrossRefGoogle Scholar
  56. Roy-Lachapelle A, Solliec M, Bouchard MF, Sauvé S (2017) Detection of cyanotoxins in algae dietary supplements. Toxins 9Google Scholar
  57. Rzymski P, Ganz T (2018) Comment on “Serum Hepcidin and Soluble Transferrin Receptor in the Assessment of Iron Metabolism in Children on a Vegetarian Diet”. Biol Trace Elem Res 185:252–254CrossRefPubMedGoogle Scholar
  58. Rzymski P, Jaśkiewicz M (2017) Microalgal food supplements from the perspective of Polish consumers: patterns of use, adverse events, and beneficial effects. J Appl Phycol 29:1841–1850CrossRefPubMedGoogle Scholar
  59. Rzymski P, Niedzielski P, Poniedziałek B, Karczewski J (2014) Biosorption of toxic metals using freely suspended Microcystis aeruginosa biomass. Centr Eur J Chem 12:1232–1238CrossRefGoogle Scholar
  60. Rzymski P, Niedzielski P, Kaczmarek N, Jurczak T, Klimaszyk P (2015) The multidisciplinary approach to safety and toxicity assessment of microalgae-based food supplements following clinical cases of poisoning. Harmful Algae 46:34–42CrossRefGoogle Scholar
  61. Rzymski P, Mleczek M, Siwulski M, Jasińska A, Budka A, Niedzielski P, Kalac P, Gąsecka M, Budzyńska S (2017) Multielemental analysis of fruit bodies of three cultivated commercial Agaricus species. J Food Compos Anal 59:170–178CrossRefGoogle Scholar
  62. SAC 2012 Standardization Administration of the People’s Republic of China. Maximum levels of contaminants in foods; GB 2762–2012 J Verbrauch Lebensm. http://www.cirs-group.com/uploads/soft/140901/GB_2762-2012_Food_Safety_National_Standard_for_Maximum_levels_of_contaminants_in_foods.pdf. Accessed 21 October 2018
  63. Sadovsky D, Brenner A, Astrachan B, Asaf B, Gonen R (2016) Biosorption potential of cerium ions using Spirulina biomass. J Rare Earths 34:644–652CrossRefGoogle Scholar
  64. Salim S, Bosma R, Vermuë MH, Wijffels RH (2011) Harvesting of microalgae by bio-flocculation. J Appl Phycol 23:849–855CrossRefGoogle Scholar
  65. Siwulski M, Mleczek M, Rzymski P, Budka A, Jasińska A, Niedzielski P, Kalac P, Gąsecka M, Budzyńska S, Mikołajczak P (2017) Screening the multi-element content of Pleurotus mushroom species using inductively coupled plasma optical emission spectrometer (ICP-OES). Food Anal Methods 10:487–496CrossRefGoogle Scholar
  66. Suliburska J, Szulińska M, Tinkov AA, Bogdański P (2016) Effect of Spirulina maxima supplementation on calcium, magnesium, iron, and zinc status in obese patients with treated hypertension. Biol Trace Elem Res 173:1–6CrossRefPubMedGoogle Scholar
  67. Sun H, Brocato J, Costa M (2015) Oral chromium exposure and toxicity. Curr Environ Health Rep 2:295–303CrossRefPubMedGoogle Scholar
  68. Taylor GA, Moore PB, Ferrier IN, Tyrer SP, Edwardson JA (1998) Gastrointestinal absorption of aluminium and citrate in man. J Inorg Biochem 69:165–169CrossRefGoogle Scholar
  69. The Expert Group on Vitamins and Minerals (2003) Safe upper levels for vitamins and minerals. Food Standards Agency Publications, LondonGoogle Scholar
  70. Vandamme D, Foubert I, Muylaert K (2013) Flocculation as a low-cost method for harvesting microalgae for bulk biomass production. Trends Biotechnol 31:233–239CrossRefGoogle Scholar
  71. Verkaik-Kloosterman J, McCann MT, Hoekstra J, Verhagen H (2012) Vitamins and minerals: issues associated with too low and too high population intakes. Food Nutr Res 56:5728CrossRefGoogle Scholar
  72. Verkaik-Kloosterman J, Seves SM, Ocké MC (2017) Vitamin D concentrations in fortified foods and dietary supplements intended for infants: implications for vitamin D intake. Food Chem 221:629–635CrossRefGoogle Scholar
  73. Vichi S, Lavorini P, Funari E, Scardala S, Testai E (2012) Contamination by Microcystis and microcystins of blue-green algae food supplements (BGAS) on the Italian market and possible risk for the exposed population. Food Chem Toxicol 50:4493–4499CrossRefGoogle Scholar
  74. Wang B, Yan L, Huo W, Lu Q, Cheng Z, Zhang J, Li Z (2017) Rare earth elements and hypertension risk among housewives: a pilot study in Shanxi Province, China. Environ Pollut 220:837–842CrossRefGoogle Scholar
  75. Wei B, Li Y, Li H, Yu J, Ye B, Liang T (2013) Rare earth elements in human hair from a mining area of China. Ecotoxicol Environ Saf 96:118–123CrossRefGoogle Scholar
  76. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2016) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29:949–982CrossRefPubMedGoogle Scholar
  77. Yokel RA, McNamara PJ (2001) Aluminium toxicokinetics: an updated minireview. Pharmacol Toxicol 88:159–167CrossRefPubMedGoogle Scholar
  78. Zeinalian R, Farhangi MA, Shariat A, Saghafi-Asl M (2017) The effects of Spirulina platensis on anthropometric indices, appetite, lipid profile and serum vascular endothelial growth factor (VEGF) in obese individuals: a randomized double blinded placebo controlled trial. BMC Complement Altern Med 17:225CrossRefPubMedGoogle Scholar
  79. Zhu WF, Xu SQ, Zhang H, Shao PP, Wu DS, Yang WJ (1996) Investigation of children intelligence quotient in REE mining area: bio-efffect study of REE mining area of South Jiangxi. Chin Sci Bull 41:914–916Google Scholar
  80. Zhuang M, Zhao J, Li S, Liu D, Wang K, Xiao P, Yu L, Jiang Y, Song J, Zhou J, Wang L, Chu Z (2017) Concentrations and health risk assessment of rare earth elements in vegetables from mining area in Shandong, China. Chemosphere 168:578–582CrossRefGoogle Scholar

Copyright information

© The Author(s) 2018
corrected publication December/2018

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Department of Environmental MedicinePoznan University of Medical SciencesPoznańPoland
  2. 2.Department of Analytical ChemistryAdam Mickiewicz UniversityPoznańPoland
  3. 3.Department of Water ProtectionAdam Mickiewicz UniversityPoznańPoland

Personalised recommendations