A Systematic Literature Review for Evidence of Aphanizomenon flos-aquae Toxigenicity in Recreational Waters and Toxicity of Dietary Supplements: 2000–2017
Abstract
:1. Introduction
2. Results
2.1. Toxigenicity
2.1.1. Anatoxin-a
2.1.2. Cylindrospermopsin
2.1.3. Microcystins
2.1.4. Saxitoxin
2.2. Fresh Water
2.3. Dietary Supplements
3. Discussion
4. Conclusions
4.1. Recommendation to Post Educational Signs as a Precautionary Measure at First Sight of Visible Scum
4.2. Recommendation to Limit Harvesting of AFA to Months When Toxicity Is Lowest
4.3. Recommendation to Include AFA in Cell Counts during Visible Blooms
4.4. Recommendation to Reduce Health Advisory Guideline Value for Cyanotoxin Levels
4.5. Recommendations for Proper Species Identification Using 16S rRNA Methods When Toxicity Levels Are Higher than Advisory Levels
4.6. Recommendations for Laboratory-Based Research to Confirm the Ability of AFA to Produce Toxins under Differing Environmental Conditions
5. Materials and Methods
5.1. Search Strategy
5.2. Inclusion Criteria
5.3. Exclusion Criteria
5.4. Study Quality Assessment
Funding
Acknowledgments
Conflicts of Interest
References
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Lead Author (Year) | Location | Findings | Method of Detection | Conclusions |
---|---|---|---|---|
Roy-Lachapelle (2017) | Canada | Out of 18 products tested, 8 contained cyanotoxins at levels exceeding WHO’s TDI. Supplements containing AFA had MC concentrations between 0.8 and 8.2 μg/g. Low amounts of BMAA (neurotoxin) were also found. | Lemieux and Adda oxidation. Chemical derivatization, laser diode thermal desorption, and liquid chromatography. | Some dietary products could be harmful upon long-term consumption due to the presence of cyanotoxins. A critical need exists for better monitoring for all BGAS, and guidelines for maximum intake. |
Chernova (2017) | Russia | Aphanizomenon flos-aquae found to produce ANTX in Sestroretskij Razliv Lake | PCR and LC-MS/MS and Restriction Fragment Length Polymorphism (RFLP) analysis | Both dominant species Aphanizomenon flos-aquae and Dolichospermum planctonicum are ANTX producers. |
Cires (2016) | Global | Aphanizomenon spp. known toxin producer specifically: CYN (11–41% of total toxins, up to 58–63% under certain conditions), ANTX (7–47% of total toxins), and SXTs (7–35% of total toxins) | Literature Review. | Although Aphanizomenon spp. are known toxin producers, the toxigenicity of AFA is still uncertain. |
Mariani (2015) | Sardinia | AFA and Aphanocapsa spp. dominated total cyanobacteria. | ELISA, Mass spectrometer. | Species composition during periods of maximum MC concentration differed from typical in other Mediterranean sites. |
Sulcius (2015) | Lithuania/Russia | Concentrations of cyanotoxins in scum materials increased from ~30~300 fold compared to bloom samples. AFA comprised ~19% of total cyanobacteria biomass. The most common toxin-producing cyanobacteria from Curonian Lagoon belong to the genera of Aphanizomenon spp., Microcystis, and Planktothrix. | Microscopic, and chemical. Extraction of saxitoxins with 4 mM ammonium formate buffer and acetonitrile 2:3 ratio, Mass spectrometer, information dependent acquisition mode, and multiple reaction monitoring. | Larger concentrations of cyanotoxins were found in scum compared to blooms. |
Dadheech (2014) | Germany | Although AFA dominated total phytoplankton at >80% contribution to total biomass, AFA did not show amplification for the mcyE gene, or STX and ANTX production. | Molecular analysis:16S rRNA sequencing, BLAST identification. | Differences seen in dominant taxon of field sample from Dolichospermum circinale in 2011 to AFA in 2012, with reduction in total MC content seen from 27.32 μg/L to 4.25 μg/L. |
Gkelis (2014) | Greece | C. raciborskii and AFA are potential STX producers. A. gracile confirmed STX producer. MC: 3.9–108 μg/L, CYNs: 0.3–2.8 μg/L, and STXs: 0.4–1.2 μg/L Aphanizomenon spp. STX gene cluster may be biogeographically differentiated by county. | Microscopy, molecular, and immunologic methods: ELISA. | AFA was not found to be the dominant species in blooms, or a producer of toxins. Co-occurrence of more than one cyanotoxins in sites used for drinking water, agriculture, or recreation represent potential health risks. |
Heussner (2012) | Germany | All AFA products tested positive for MCs and the mcyE gene. The contamination levels of the MC-positive samples were ≤1 μg MC-LR equivalents per g dry weight. | Colorimetric protein phosphatase inhibition assay (cPPIA), Adda-ELISA, Cell Culture, Liquid chromatography tandem mass spectrometry (LC-MS/MS), DNA extraction and PCR. | Recommendation for prohibition of marketing and sale of AFA-based dietary supplements in order to prevent acute and chronic exposure to MCs. |
Mooney (2011) | Ireland | AFA, Gomaphosphaeria spp. and Microcystis aeruginosa were the most dominant cyanobacterial species associated with high MC concentration. AFA was dominant in 1/14 sites with lake area of 382 km2, and MC concentration of 1652 ng/μg Chla | Synoptic survey of 14 sites, used high performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). | Further studies are recommended to use molecular detection methods to determine whether AFA is a MC producer. It is unknown which species produced the toxins, only recorded dominant cyanobacteria and total toxin per area. |
Blahova (2009) | France | CYN was found at 3 localities with Aphanizomenon spp. sub-dominated water blooms. Concentrations determined by ELISA (0.4–4 μg/L) were systematically higher than concentrations determined by LC/MS (0.01–0.3 μg/L). | ELISA and LC/MS. | AFA is a potential producer of CYN. |
Brient (2009) | Czech Republic | AFA var klebahnii found to be a potential producer of CYN. Intracellular concentrations of CYN ranged between 1.55 and 1.95 μg/L. | LC-MS/MS. | AFA is a potential producer of CYN. |
Palus (2007) | Poland | AFA dominated blooms August–October. The concentration of MC in water did not exceed 1 μg/L, Cyanobacteria co-occurrence found with E. coli. | Protein phosphatase inhibition assay (PPIA), ELISA and HPLC. | Phytoplankton biomass and genotoxicity of CyanoHABs should be assessed to avoid public health issues. |
Fastner (2007) | Germany | Concentrations reached up to 73.2 μg CYN/g dry weight. Study confirmed AFA is a CYN-producing species frequently inhabiting water bodies in temperate climatic regions. | Microscopy, Mass-spectrometer. | Aphanizomenon spp. may be an important CYN toxin producer in Germany waters. A world hazard analysis and risk assessment is recommended to confirm by geographic regions. |
Saker (2007) | Australia and Canada | mcyA gene was detected in all 12 AFA dietary supplements, suggesting contamination by Microcystis spp. | Multiplex PCR. | Dietary supplements containing AFA are more at risk for contamination by Microcystis spp., and should be monitored. Laboratory and toxicological analysis of Upper Klamath Lake cyanobacteria would provide useful information to inform and protect human health. |
Preussel (2006) | Germany | Toxin CYN detected in the range of 2.3–6.6 mg/g of cellular dry weight. | LC-MS/MS analysis and detection of PCR products of gene fragments. | First report of CYN in AFA strains. |
Ferreira (2001) | Portugal | Presence of PSP toxins: GTX4, GTX1, GTX3, and Cs toxin present either in cells of AFA or in other toxic isolates. | High performance liquid chromatography (HPLC) using 2 isocratic elution systems. | AFA known STX producer, but A. circinalis is also found to be potential STX producer. More work is needed to understand the toxicological profiles of cyanobacteria. |
Liu (2006) | China | STXs produced by AFA bloom. Significant glutathione-S-transferase (GST) and lactate dehydrogenase (LDH) increases, together with decrease of the glutathione (GSH) level, were measured. | High performance liquid chromatography with post-column fluorescence derivatization (HPLC-FLD) and liquid chromatographic mass spectrometry technique (LC-MS). | The results indicate a potential role of STXs intoxicating and metabolizing in test animals. |
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Lyon-Colbert, A.; Su, S.; Cude, C. A Systematic Literature Review for Evidence of Aphanizomenon flos-aquae Toxigenicity in Recreational Waters and Toxicity of Dietary Supplements: 2000–2017. Toxins 2018, 10, 254. https://doi.org/10.3390/toxins10070254
Lyon-Colbert A, Su S, Cude C. A Systematic Literature Review for Evidence of Aphanizomenon flos-aquae Toxigenicity in Recreational Waters and Toxicity of Dietary Supplements: 2000–2017. Toxins. 2018; 10(7):254. https://doi.org/10.3390/toxins10070254
Chicago/Turabian StyleLyon-Colbert, Amber, Shelley Su, and Curtis Cude. 2018. "A Systematic Literature Review for Evidence of Aphanizomenon flos-aquae Toxigenicity in Recreational Waters and Toxicity of Dietary Supplements: 2000–2017" Toxins 10, no. 7: 254. https://doi.org/10.3390/toxins10070254
APA StyleLyon-Colbert, A., Su, S., & Cude, C. (2018). A Systematic Literature Review for Evidence of Aphanizomenon flos-aquae Toxigenicity in Recreational Waters and Toxicity of Dietary Supplements: 2000–2017. Toxins, 10(7), 254. https://doi.org/10.3390/toxins10070254