Comparative Study on the Performance of Three Detection Methods for the Quantification of Pacific Ciguatoxins in French Polynesian Strains of Gambierdiscus polynesiensis
Abstract
:1. Introduction
2. Results and Discussion
2.1. Binding Affinity of CTX3C and Gambierdiscus polynesiensis Extracts Using the fRBA
2.1.1. Solvent Effect, Incubation Parameters, and Matrix Effects
2.1.2. Efficiency of the fRBA When Applied to CTX3C and Gambierdiscus polynesiensis Samples
2.2. Cytotoxic Activity of CTX3C and Gambierdiscus polynesiensis on N2a cells Using the CBA-N2a
2.3. Detection and Quantification of CTX3C and Gambierdiscus polynesiensis Using LC-MS/MS
2.4. Comparison of the Performance of the Three Detection Methods
2.5. Practical Considerations for Algal-Based Ciguatera Risk Monitoring Programs
3. Materials and Methods
3.1. Gambierdiscus Isolates
3.2. Reagents and Chemicals
3.3. In Vitro Cultures
3.4. Cells Harvest and Toxin Extraction
3.5. Fluorescent Receptor Binding Assay (fRBA)
3.5.1. Reagents
3.5.2. The fRBA Reaction
3.5.3. Solvent Effect
3.5.4. Incubation Parameters
3.5.5. Matrix Effects
3.5.6. Repeatability of fRBA
3.6. Neuroblastoma Cell-Based Assay (CBA-N2a)
3.7. Liquid Chromatography Tandem Mass Spectrometry (LC-MS/MS)
3.8. Statistical Analyses
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Toxin and Matrix | Parameters 1 | fRBA | rRBA | |||
---|---|---|---|---|---|---|
References | This Study | [136] | [87,88,126] | [91] | [84] | |
CTX3C | LOD = EC80 (ng mL−1) | 1.10 ± 0.08 | ND 2 | 0.90 ± 0.19 3 | ND | ND |
LOQ = EC50 (ng mL−1) | 2.10 ± 0.16 | 0.66 ± 0.16 | 1.92 ± 0.38 3 | 0.62 ± 0.13 | 0.62 ± 0.16 | |
EC20 (ng mL−1) | 4.06 ± 0.59 | ND | 4.17 ± 1.12 3 | ND | ND | |
Gambierdiscus | MCE (cell mL−1) | 16,000 | ND | 7500 | ND | ND |
LOD (fg CTX3C eq cell−1) | 68.53 ± 5.25 | ND | 250 | ND | 15.5 | |
LOQ (fg CTX3C eq cell−1) | 131.32 ± 9.94 | ND | ND | ND | <310–330 |
Strain Name 1 | ID# | EC50 2 (cell mL−1) | Coefficient of Variation (CV %) 3 | CTX Content 2 (pg CTX3C eq cell−1) | Coefficient of Variation (CV %) 3 |
---|---|---|---|---|---|
RG92 | RG92-a | 1188 ± 563 | 51 | 2.04 ± 1.40 | 69 |
RG92-b | 1926 ± 237 | 12 | 1.10 ± 0.15 | 14 | |
RG92-c | 1314 ± 101 | 8 | 1.64 ± 0.17 | 10 | |
RIK7 | RIK7-a | 482 ± 41 | 9 | 4.36 ± 0.14 | 3 |
RIK7-b | 467 ± 64 | 14 | 4.54 ± 0.48 | 11 | |
RIK7-c | 747 ± 36 | 5 | 2.88 ± 0.23 | 8 | |
RIK7-d | 1006 ± 57 | 6 | 2.14 ± 0.13 | 6 | |
RIK7-e | 448 ± 26 | 6 | 4.70 ± 0.18 | 4 | |
RIK7-f | 1143 ± 89 | 8 | 1.89 ± 0.31 | 16 | |
RIK7-g | 387 ± 14 | 4 | 5.56 ± 0.64 | 11 | |
RIK7-h | 405 ± 20 | 5 | 5.19 ± 0.21 | 4 | |
RIK7-i | 794 ± 85 | 11 | 2.74 ± 0.50 | 18 | |
RIK7-j | 368 ± 24 | 6 | 5.87 ± 0.76 | 13 | |
RIK7-k | 561 ± 47 | 8 | 3.76 ± 0.53 | 14 | |
RIK7-l | 415 ± 51 | 12 | 5.07 ± 0.49 | 10 | |
RAI1 | RAI1-a | 439 ± 43 | 10 | 4.90 ± 0.10 | 2 |
RAI1-b | 439 ± 33 | 8 | 4.92 ± 0.66 | 13 | |
RAI1-c | 377 ± 28 | 7 | 5.73 ± 0.73 | 13 | |
RAI1-d | 442 ± 30 | 7 | 4.88 ± 0.50 | 10 | |
RAI1-e | 376 ± 30 | 8 | 5.60 ± 0.35 | 6 | |
RAI1-f | 466 ± 230 | 49 | 5.53 ± 2.12 | 38 | |
RAI1-g | 579 ± 33 | 6 | 3.63 ± 0.45 | 12 | |
RAI1-h | 360 ± 14 | 4 | 5.87 ± 0.73 | 13 | |
NHA4 | NHA4-a | 267 ± 12 | 5 | 8.05 ± 0.40 | 5 |
NHA4-b | 255 ± 16 | 6 | 8.27 ± 0.68 | 8 | |
NHA4-c | 270 ± 15 | 6 | 7.97 ± 0.76 | 10 | |
NHA4-d | 272 ± 19 | 7 | 7.72 ± 0.17 | 2 | |
NHA4-e | 279 ± 15 | 5 | 7.53 ± 0.35 | 5 | |
NHA4-f | 279 ± 8 | 3 | 7.70 ± 0.46 | 6 | |
NHA4-g | 263 ± 11 | 4 | 8.01 ± 0.65 | 8 |
OV Treatment | CTX3C 1 | Gambierdiscus Matrix 1 | ||||
---|---|---|---|---|---|---|
O/V (µM) | LOD = EC80 (pg mL−1) | LOQ = EC50 (pg mL−1) | MCE (cell mL−1) | LOD (fg CTX3C eq cell−1) | LOQ (fg CTX3C eq cell−1) | References |
76.2/7.62 | ND 2 | ND | ND | 0.17 | 0.34 | [22] |
80/8 | ND | 3.10 ± 0.76 | ND | 0.17 | ND | [19,140] |
(80/8–90/9) | ND | 1.91 ± 0.22 | ND | ND | ND | [89] |
90/9 | 0.63 ± 0.05 | 1.50 ± 0.23 | 1904 | 0.33 ± 0.03 | 0.79 ± 0.12 | This study |
100/10 | ND | ND | ND | ND | 8.7 × 10−4–4.7 × 10−2 | [93] 3 |
ND | ND | ND | ND | 6.74–7.27 × 10−7 | [92] 3 | |
0.2 | ND | ND | ND | ND | [94] | |
ND | 1.44 ± 0.70 | ND | 0.17 | ND | [96] | |
ND | 1.73 ± 0.41 | ND | ND | ND | [115] | |
ND | 1.84 ± 0.31 | ND | ND | N−D | [109] | |
ND | 3.52 ± 0.27 | ND | ND | ND | [139] | |
250/25 | ND | 1.66 ± 0.16 | ND | ND | ND | [136] |
ND | 1.66 ± 0.16 | ND | ND | ND | [95] | |
500/50 | ND | 0.91 ± 0.13 | ND | ND | ND | [138] |
ND | 1.30 ± 0.06 | ND | ND | ND | [91] | |
ND | 0.57 ± 0.11 | ND | ND | ND | [137] |
Strain Name 1 | ID# | EC50 2 (cell mL−1) | Coefficient of Variation (CV %) 3 | CTX Content 2 (pg CTX3C eq cell−1) | Coefficient of Variation (CV %) 3 |
---|---|---|---|---|---|
RG92 | RG92-a | 2.28 ± 0.54 | 24% | 0.68 ± 0.09 | 14 |
RG92-b | 2.08 ± 0.46 | 23% | 0.68 ± 0.03 | 4 | |
RG92-c | 2.15 ± 0.50 | 22% | 0.75 ± 0.10 | 14 | |
RIK7 | RIK7-a | 0.73 ± 0.18 | 25% | 2.03 ± 0.12 | 6 |
RIK7-b | 0.67 ± 0.10 | 15% | 2.19 ± 0.30 | 14 | |
RIK7-c | 0.76 ± 0.09 | 12% | 2.03 ± 0.35 | 17 | |
RIK7-d | 1.45 ± 0.39 | 27% | 1.10 ± 0.35 | 22 | |
RIK7-e | 0.59 ± 0.13 | 23% | 2.53 ± 0.54 | 21 | |
RIK7-f | 0.72 ± 0.09 | 12% | 2.14 ± 0.17 | 8 | |
RIK7-g | 0.66 ± 0.13 | 20% | 2.34 ± 0.32 | 14 | |
RIK7-h | 0.45 ± 0.14 | 30% | 3.39 ± 0.91 | 27 | |
RIK7-i | 1.96 ± 0.31 | 16% | 0.79 ± 0.08 | 10 | |
RIK7-j | 0.46 ± 0.08 | 17% | 3.33 ± 0.43 | 13 | |
RIK7-k | 0.64 ± 0.16 | 25% | 2.32 ± 0.36 | 16 | |
RIK7-l | 0.45 ± 0.13 | 29% | 3.31 ± 0.33 | 10 | |
RAI1 | RAI1-a | 0.65 ± 0.17 | 26% | 2.44 ± 0.48 | 20 |
RAI1-b | 0.60 ± 0.11 | 18% | 2.57 ± 0.31 | 12 | |
RAI1-c | 0.65 ± 0.10 | 15% | 2.38 ± 0.41 | 22 | |
RAI1-d | 0.43 ± 0.07 | 16% | 3.55 ± 0.16 | 5 | |
RAI1-e | 0.50 ± 0.14 | 28% | 3.00 ± 0.24 | 8 | |
RAI1-f | 0.55 ± 0.09 | 17% | 2.70 ± 0.35 | 13 | |
RAI1-g | 0.64 ± 0.13 | 20% | 2.31 ± 0.16 | 7 | |
RAI1-h | 0.31 ± 0.04 | 14% | 4.72 ± 0.31 | 7 | |
NHA4 | NHA4-a | 0.31 ± 0.06 | 19% | 5.04 ± 0.63 | 13 |
NHA4-b | 0.21 ± 0.06 | 27% | 6.93 ± 0.66 | 10 | |
NHA4-c | 0.28 ± 0.06 | 20% | 5.75 ± 0.92 | 16 | |
NHA4-d | 0.36 ± 0.14 | 38% | 4.21 ± 0.73 | 17 | |
NHA4-e | 0.33 ± 0.05 | 16% | 4.45 ± 0.86 | 19 | |
NHA4-f | 0.40 ± 0.06 | 16% | 3.90 ± 0.49 | 13 | |
NHA4-g | 0.15 ± 0.04 | 29% | 9.72 ± 1.64 | 17 |
CTX3C 1 | Gambierdiscus1 | References | |||
---|---|---|---|---|---|
LOD (ng mL−1) | LOQ (ng mL−1) | MCE (cell mL−1) | LOD (fg CTX3C eq cell−1) | LOQ (fg CTX3C eq cell−1) | |
2 | 6 | 100,000 | 20 | 60 | This study |
5 | 10 | ND 2 | ND | ND | [23] |
2 | 6 | ND | ND | ND | [109] |
ND | 40 | ND | ND | [20–80] | [22] |
1 | ND | ND | ND | ND | [8,106] |
60 | ND | ND | ND | ND | [19] |
1–2 | ND | ND | ND | ND | [104] |
ND | ND | ND | 0.005 | ND | [76] |
Strain Name 1 | ID# | CTX3B 2 | CTX3C | CTX4A | CTX4B | M-Seco-CTX3C | 2OH-CTX3C | 3OH-CTX3C | CTX3C Isomers 4 | Total CTX Content 2 (pg CTX3C eq cell−1) | Coefficient of Variation (CV %) 5 | ||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
1 (6.90) | 2 (7.25) | 3 (7.70) | 4 (9.80) | 5 (10.10) | |||||||||||
RG92 | RG92-a | 0.35 ± 0.01 | 0.23 ± 0.02 | 0.07 ± 0.02 | 0.09 ± 0.02 | <LOD 3 | 0.09 ± 0.00 | <LOD | 0.06 ± 0.03 | 0.05 ± 0.03 | 0.06 ± 0.00 | 0.06 ± 0.04 | 0.07 ± 0.01 | 1.03 ± 0.10 | 10% |
RG92-b | 0.41 ± 0.04 | 0.42 ± 0.11 | 0.05 ± 0.01 | 0.07 ± 0.01 | <LOD | <LOD | <LOD | <LOQ 3 | <LOQ | 0.05 ± 0.03 | <LOD | 0.06 ± 0.04 | 1.01 ± 0.14 | 14% | |
RG92-c | 0.43 ± 0.01 | 0.47 ± 0.02 | 0.04 ± 0.04 | 0.10 ± 0.02 | <LOD | <LOD | <LOD | 0.05 ± 0.03 | 0.05 ± 0.03 | 0.06 ± 0.00 | <LOD | 0.07 ± 0.01 | 1.24 ± 0.06 | 5% | |
RIK7 | RIK7-a | 1.33 ± 0.17 | 0.96 ± 0.13 | 0.05 ± 0.01 | 0.07 ± 0.01 | <LOD | 0.11 ± 0.01 | <LOD | 0.05 ± 0.03 | 0.06 ± 0.03 | 0.07 ± 0.04 | 0.07 ± 0.04 | 0.09 ± 0.00 | 2.76 ± 0.31 | 11% |
RIK7-b | 1.51 ± 0.02 | 1.12 ± 0.11 | 0.06 ± 0.01 | 0.09 ± 0.03 | <LOD | 0.11 ± 0.01 | <LOD | 0.06 ± 0.03 | 0.07 ± 0.05 | 0.07 ± 0.02 | 0.08 ± 0.00 | 0.08 ± 0.01 | 3.18 ± 0.18 | 6% | |
RIK7-c | 0.98 ± 0.07 | 0.80 ± 0.04 | 0.10 ± 0.09 | 0.24 ± 0.07 | <LOD | <LOD | <LOD | 0.05 ± 0.03 | 0.06 ± 0.03 | 0.06 ± 0.00 | <LOD | 0.06 ± 0.04 | 2.27 ± 0.20 | 9% | |
RIK7-d | 0.98 ± 0.06 | 0.56 ± 0.01 | 0.05 ± 0.04 | 0.09 ± 0.02 | <LOD | <LOD | <LOD | <LOQ | 0.06 ± 0.00 | 0.05 ± 0.03 | <LOD | 0.07 ± 0.04 | 1.81 ± 0.16 | 9% | |
RIK7-e | 2.81 ± 0.21 | 1.42 ± 0.22 | 0.15 ± 0.03 | 0.23 ± 0.07 | <LOD | <LOD | 0.05 ± 0.03 | 0.06 ± 0.03 | 0.08 ± 0.01 | 0.07 ± 0.01 | 0.07 ± 0.04 | 0.07 ± 0.04 | 4.90 ± 0.48 | 10% | |
RIK7-f | 1.37 ± 0.06 | 0.98 ± 0.06 | 0.15 ± 0.08 | 0.26 ± 0.07 | <LOD | 0.05 ± 0.00 | <LOD | 0.06 ± 0.03 | 0.07 ± 0.01 | 0.08 ± 0.01 | 0.06 ± 0.04 | 0.08 ± 0.05 | 3.08 ± 0.07 | 2% | |
RIK7-g | 1.75 ± 0.03 | 1.31 ± 0.08 | 0.20 ± 0.12 | 0.43 ± 0.15 | <LOD | 0.06 ± 0.00 | <LOD | 0.06 ± 0.03 | 0.09 ± 0.01 | 0.10 ± 0.01 | 0.06 ± 0.01 | 0.07 ± 0.01 | 4.11 ± 0.16 | 4% | |
RIK7-h | 3.16 ± 0.25 | 1.58 ± 0.17 | 0.13 ± 0.03 | 0.18 ± 0.06 | <LOD | <LOD | <LOD | <LOQ | 0.07 ± 0.02 | 0.07 ± 0.02 | 0.06 ± 0.03 | 0.07 ± 0.04 | 5.25 ± 0.49 | 9% | |
RIK7-i | 0.92 ± 0.03 | 0.57 ± 0.03 | 0.06 ± 0.06 | 0.15 ± 0.04 | <LOD | <LOD | <LOD | 0.05 ± 0.03 | 0.05 ± 0.03 | 0.06 ± 0.01 | <LOD | 0.06 ± 0.04 | 1.87 ± 0.10 | 6% | |
RIK7-j | 3.07 ± 0.08 | 1.71 ± 0.21 | 0.10 ± 0.04 | 0.17 ± 0.04 | <LOD | <LOD | 0.06 ± 0.04 | 0.06 ± 0.03 | 0.11 ± 0.00 | 0.13 ± 0.01 | 0.07 ± 0.04 | 0.07 ± 0.04 | 5.41 ± 0.24 | 4% | |
RIK7-k | 1.96 ± 0.08 | 1.23 ± 0.17 | 0.19 ± 0.04 | 0.30 ± 0.09 | <LOD | 0.06 ± 0.03 | <LOD | <LOQ | 0.05 ± 0.03 | 0.07 ± 0.04 | 0.06 ± 0.03 | 0.06 ± 0.04 | 3.82 ± 0.35 | 9% | |
RIK7-l | 3.26 ± 0.10 | 1.65 ± 0.09 | 0.14 ± 0.03 | 0.22 ± 0.06 | 0.05 ± 0.03 | <LOD | <LOD | 0.06 ± 0.03 | 0.08 ± 0.01 | 0.10 ± 0.01 | 0.05 ± 0.03 | 0.06 ± 0.04 | 5.56 ± 0.12 | 2% | |
RAI1 | RAI1-a | 1.81 ± 0.02 | 1.29 ± 0.04 | 0.09 ± 0.03 | 0.17 ± 0.05 | <LOD | 0.06 ± 0.00 | <LOD | 0.06 ± 0.01 | 0.10 ± 0.02 | 0.10 ± 0.02 | 0.07 ± 0.01 | 0.08 ± 0.01 | 3.84 ± 0.01 | 0% |
RAI1-b | 1.43 ± 0.04 | 1.10 ± 0.07 | 0.12 ± 0.05 | 0.19 ± 0.05 | <LOD | 0.10 ± 0.00 | <LOD | 0.05 ± 0.03 | 0.08 ± 0.01 | 0.13 ± 0.01 | 0.07 ± 0.01 | 0.07 ± 0.01 | 3.33 ± 0.05 | 2% | |
RAI1-c | 1.46 ± 0.08 | 1.32 ± 0.01 | 0.20 ± 0.14 | 0.42 ± 0.13 | <LOD | 0.09 ± 0.00 | <LOD | 0.06 ± 0.03 | 0.10 ± 0.01 | 0.11 ± 0.01 | 0.07 ± 0.01 | 0.07 ± 0.00 | 3.87 ± 0.28 | 7% | |
RAI1-d | 2.73 ± 0.03 | 1.75 ± 0.17 | 0.12 ± 0.05 | 0.27 ± 0.08 | <LOD | <LOD | <LOD | 0.05 ± 0.03 | 0.07 ± 0.01 | 0.08 ± 0.01 | 0.06 ± 0.03 | 0.06 ± 0.04 | 5.12 ± 0.16 | 3% | |
RAI1-e | 2.91 ± 0.18 | 2.12 ± 0.35 | 0.10 ± 0.02 | 0.17 ± 0.05 | <LOD | <LOD | <LOD | 0.05 ± 0.03 | 0.10 ± 0.02 | 0.12 ± 0.01 | <LOQ | 0.08 ± 0.05 | 5.60 ± 0.52 | 9% | |
RAI1-f | 1.40 ± 0.02 | 0.92 ± 0.06 | 0.08 ± 0.02 | 0.09 ± 0.03 | <LOD | <LOD | <LOD | <LOQ | 0.06 ± 0.03 | 0.05 ± 0.03 | 0.05 ± 0.03 | 0.07 ± 0.04 | 2.60 ± 0.14 | 6% | |
RAI1-g | 1.76 ± 0.08 | 1.22 ± 0.11 | 0.15 ± 0.04 | 0.23 ± 0.07 | <LOD | 0.05 ± 0.03 | <LOQ | 0.06 ± 0.03 | 0.06 ± 0.01 | 0.09 ± 0.01 | 0.05 ± 0.03 | 0.06 ± 0.04 | 3.61 ± 0.27 | 7% | |
RAI1-h | 3.28 ± 0.15 | 1.91 ± 0.15 | 0.15 ± 0.03 | 0.22 ± 0.06 | <LOD | <LOD | <LOD | 0.06 ± 0.03 | 0.10 ± 0.02 | 0.11 ± 0.00 | 0.06 ± 0.01 | 0.08 ± 0.05 | 5.91 ± 0.32 | 5% | |
NHA4 | NHA4-a | 3.74 ± 0.14 | 2.37 ± 0.10 | 0.07 ± 0.01 | 0.11 ± 0.02 | 0.10 ± 0.01 | <LOD | <LOD | 0.06 ± 0.03 | 0.14 ± 0.01 | 0.16 ± 0.01 | 0.07 ± 0.01 | 0.07 ± 0.01 | 6.84 ± 0.21 | 3% |
NHA4-b | 4.12 ± 0.19 | 2.44 ± 0.33 | 0.08 ± 0.01 | 0.12 ± 0.04 | 0.07 ± 0.01 | <LOQ | 0.07 ± 0.00 | <LOQ | 0.08 ± 0.03 | 0.10 ± 0.01 | 0.05 ± 0.03 | 0.07 ± 0.04 | 7.14 ± 0.51 | 7% | |
NHA4-c | 4.31 ± 0.14 | 2.14 ± 0.16 | 0.08 ± 0.01 | 0.10 ± 0.02 | 0.09 ± 0.01 | <LOD | 0.06 ± 0.00 | 0.06 ± 0.01 | 0.14 ± 0.02 | 0.14 ± 0.01 | 0.06 ± 0.01 | 0.07 ± 0.01 | 7.25 ± 0.10 | 1% | |
NHA4-d | 3.27 ± 0.10 | 2.53 ± 0.17 | 0.10 ± 0.02 | 0.18 ± 0.05 | 0.11 ± 0.01 | 0.11 ± 0.01 | <LOD | <LOQ | 0.13 ± 0.07 | 0.17 ± 0.02 | 0.07 ± 0.02 | 0.08 ± 0.05 | 6.68 ± 0.19 | 3% | |
NHA4-e | 4.32 ± 0.19 | 2.72 ± 0.50 | 0.08 ± 0.01 | 0.11 ± 0.03 | 0.11 ± 0.00 | 0.05 ± 0.03 | <LOD | <LOQ | 0.12 ± 0.01 | 0.17 ± 0.03 | 0.06 ± 0.00 | 0.07 ± 0.01 | 7.76 ± 0.70 | 9% | |
NHA4-f | 3.66 ± 0.11 | 2.17 ± 0.07 | 0.09 ± 0.02 | 0.12 ± 0.03 | 0.09 ± 0.01 | 0.05 ± 0.00 | 0.06 ± 0.03 | 0.06 ± 0.04 | 0.16 ± 0.02 | 0.21 ± 0.01 | 0.06 ± 0.01 | 0.07 ± 0.01 | 6.74 ± 0.10 | 1% | |
NHA4-g | 4.87 ± 0.18 | 2.67 ± 0.25 | 0.09 ± 0.03 | 0.12 ± 0.04 | 0.09 ± 0.01 | <LOD | 0.05 ± 0.03 | <LOQ | 0.14 ± 0.02 | 0.18 ± 0.02 | 0.06 ± 0.03 | 0.07 ± 0.04 | 8.25 ± 0.45 | 6% |
Method | Min | Max | Median | Mean | Standard Deviation of Mean |
---|---|---|---|---|---|
fRBA | 1.10 | 8.27 | 5.002 | 4.996 | 2.11 |
CBA-N2a | 0.68 | 9.72 | 2.553 | 3.103 | 1.94 |
LC-MS/MS | 1.01 | 8.25 | 3.990 | 4.395 | 2.10 |
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Darius, H.T.; Revel, T.; Viallon, J.; Sibat, M.; Cruchet, P.; Longo, S.; Hardison, D.R.; Holland, W.C.; Tester, P.A.; Litaker, R.W.; et al. Comparative Study on the Performance of Three Detection Methods for the Quantification of Pacific Ciguatoxins in French Polynesian Strains of Gambierdiscus polynesiensis. Mar. Drugs 2022, 20, 348. https://doi.org/10.3390/md20060348
Darius HT, Revel T, Viallon J, Sibat M, Cruchet P, Longo S, Hardison DR, Holland WC, Tester PA, Litaker RW, et al. Comparative Study on the Performance of Three Detection Methods for the Quantification of Pacific Ciguatoxins in French Polynesian Strains of Gambierdiscus polynesiensis. Marine Drugs. 2022; 20(6):348. https://doi.org/10.3390/md20060348
Chicago/Turabian StyleDarius, Hélène Taiana, Taina Revel, Jérôme Viallon, Manoëlla Sibat, Philippe Cruchet, Sébastien Longo, Donnie Ransom Hardison, William C. Holland, Patricia A. Tester, R. Wayne Litaker, and et al. 2022. "Comparative Study on the Performance of Three Detection Methods for the Quantification of Pacific Ciguatoxins in French Polynesian Strains of Gambierdiscus polynesiensis" Marine Drugs 20, no. 6: 348. https://doi.org/10.3390/md20060348
APA StyleDarius, H. T., Revel, T., Viallon, J., Sibat, M., Cruchet, P., Longo, S., Hardison, D. R., Holland, W. C., Tester, P. A., Litaker, R. W., McCall, J. R., Hess, P., & Chinain, M. (2022). Comparative Study on the Performance of Three Detection Methods for the Quantification of Pacific Ciguatoxins in French Polynesian Strains of Gambierdiscus polynesiensis. Marine Drugs, 20(6), 348. https://doi.org/10.3390/md20060348