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Review

The Incidence of Marine Toxins and the Associated Seafood Poisoning Episodes in the African Countries of the Indian Ocean and the Red Sea

by
Isidro José Tamele
1,2,3,
Marisa Silva
1,4 and
Vitor Vasconcelos
1,4,*
1
CIIMAR/CIMAR—Interdisciplinary Center of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto, Avenida General Norton de Matos, 4450-238 Matosinhos, Portugal
2
Institute of Biomedical Science Abel Salazar, University of Porto, R. Jorge de Viterbo Ferreira 228, 4050-313 Porto, Portugal
3
Department of Chemistry, Faculty of Sciences, Eduardo Mondlane University, Av. Julius Nyerere, n 3453, Campus Principal, Maputo 257, Mozambique
4
Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, 4619-007 Porto, Portugal
*
Author to whom correspondence should be addressed.
Toxins 2019, 11(1), 58; https://doi.org/10.3390/toxins11010058
Submission received: 27 November 2018 / Revised: 10 January 2019 / Accepted: 10 January 2019 / Published: 21 January 2019
(This article belongs to the Special Issue Toxins:10th Anniversary)
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Abstract

:
The occurrence of Harmful Algal Blooms (HABs) and bacteria can be one of the great threats to public health due to their ability to produce marine toxins (MTs). The most reported MTs include paralytic shellfish toxins (PSTs), amnesic shellfish toxins (ASTs), diarrheic shellfish toxins (DSTs), cyclic imines (CIs), ciguatoxins (CTXs), azaspiracids (AZTs), palytoxin (PlTXs), tetrodotoxins (TTXs) and their analogs, some of them leading to fatal outcomes. MTs have been reported in several marine organisms causing human poisoning incidents since these organisms constitute the food basis of coastal human populations. In African countries of the Indian Ocean and the Red Sea, to date, only South Africa has a specific monitoring program for MTs and some other countries count only with respect to centers of seafood poisoning control. Therefore, the aim of this review is to evaluate the occurrence of MTs and associated poisoning episodes as a contribution to public health and monitoring programs as an MT risk assessment tool for this geographic region.
Keywords:
Indian Ocean; marine toxins; harmful algal bloom
Key Contribution: The scarcity of MT data along African countries of the Indian Ocean and the Red Sea suggests the need for further studies and the creation of specific monitoring programs of MTs, particularly for dinoflagellates and diatoms since these constitute the phytoplankton that produces fatal MTs.

1. Introduction

The occurrence of Harmful Algal Blooms (HABs) in marine ecosystems can be one of the great threats to public health due to their capacity to produce marine toxins (MTs) as secondary metabolites [1,2,3,4,5,6,7,8,9,10,11,12,13,14]. MTs can be accumulated by distinct marine organisms such as fish, mollusks and crustaceans [15,16,17,18,19,20,21,22,23,24] which are the basic diet of coastal human populations. Suspected or confirmed episodes of human poisoning caused by MTs have been reported worldwide in the last century [20,21,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48]. The occurrence of episodes of human poisoning occurs via ingestion of contaminated marine food due to the lack of monitoring programs in some countries or violations of national health authorities’ regulations imposing the closure of harvesting areas and seafoodcommercialization [18,20,26,35,39,45,47,49]. Despite the ideal environmental conditions for theformation of blooms in this geographical area, there are insufficient data related to their occurrence and toxin production [50]. This review analyses the occurrence of MTs and their producers along the African Indian and the Red Sea coasts (from Egypt to South Africa) and associated human poisoning episodes. The existence of monitoring programs of MTs will be also highlighted and finally, some suggestions for the control and prevention of marine toxins in this area will be presented.

2. Marine Toxins and Their Producers

Chemically, toxins can be grouped according to their polarity, lipophilic and hydrophilic. Concerning MT monitoring, analysis and quantification methods in seafood are described in Table 1, including bioassays, immunoassays, and analytical chemistry methods. The bioassay methods (Mouse Bioassay (MBA), Rat Bioassay (RBA)) are no longer in use due to ethical reasons according to Directive 86/609/EEC [51] and procedural variation [52] (e.g., use of different extraction solvents and consequently shortcomings). Chemical methods, mainly liquid chromatography coupled to mass spectrometry, are considered as the most promising since they are fully validated and standardized to replace bioassays in many organizations worldwide. Further information related to each toxin group such as syndromes, producers, common vectors, symptoms, detections methods in seafood, limit of detection (LOD) and quantification (LOQ) and permitted limit used in some parts of the world is also described in Table 1.

2.1. Lipophilic Toxins

Lipophilic toxins are lipid soluble toxins and this group comprises okadaic acid (OA), ciguatoxins (CTX), cyclic imines (CIs) [spirolides (SPXs), gymnodimines (GYMs), pinnatoxins (PnTXs) and pteriatoxins (PtTXs)], brevetoxins (PbTxs), pectenotoxins (PTXs), yessotoxins (YTXs) and azaspiracids [AZAs], Table 1.

2.1.1. Okadaic Acid and Analogs

Okadaic acid (OA)and their analogs, dinophysistoxins-1, -2 and -3 (DTXs) (Figure 1), are polyethers produced by dinoflagellates: Prorocentrum spp. [8], Dinophysis spp. [2,6,9,10,15,53,54] and Phalacroma rotundatum [55] (Table 1).These polyethers are frost-resistant and heat-stable and consequently, their toxicity is not affected by the cooking procedures in water (they are stable at <150 °C) [56]. The OA group is responsible for the diarrheic shellfish poisoning syndrome (DSP), with OA being the main representative of DSP toxins. Okadaic acid (OA)and its analogs act as inhibitors of the serine/threonine phosphoprotein phosphatases 1,22B,4,5 types [57,58].

2.1.2. Ciguatoxins

Ciguatoxins (CTXs) (Figure 2A) are a group of toxins produced by tropical and subtropical dinoflagellates species: Gambierdiscus toxicus and Fukuyoa spp. [59,60] (Table 1) mainly found in the Pacific, Caribbean and the Indian Ocean regions [P-CTX, C-CTX and I-CTX, respectively]. CTXs are lipid-soluble polyethers with 13-14 rings fused by ether linkages into a rigid ladder-like structure [60]. To date, the structures of20 P-CTXs, 10 C-CTXSand 4 I-CTXs analogs have been fully identified and the most reported include P-CTX-1, P-CTX-2, P-CTX-3, P-CTX-3C [61,62,63,64,65,66,67], gambiertoxin [GbTXs, namely, P-CTX-4A and P-CTX-4B] [68], C-CTX-1, C-CTX-2 [67,69], I-CTX-1, I-CTX-2, I-CTX-3 and I-CTX-4 [70,71] mostly in predatory fish and gastropods [20,21,23,66,69,72,73,74]. The major analog of each group of CTXsis P-CTX-1. C-CTX-1, C-CTX-2, I-CTX1, and I-CTX-2. The chemical structure of the last two (I-CTXs) have the same molecular weight and similar structures as C-CTX-1 [62,67,70,71]. CTXs are odorless and tasteless heat-stable molecules and are not affected when subjected to water cooking, freezing and acid or basic conditions, though they suffer structural alterations by oxidation [60]. CTXs and Maitotoxin (MTX) (Figure 2B) (produced by Gambierdiscus spp. [68]) were the first group of toxins reported to be responsible for ciguatera shellfish poisoning (CFP) [23]. The mechanism of action of CTX and analogs is to elevate calcium ion concentration and activate non-selective cation channels in cells causing neurologic effects in humans [75].

2.1.3. Cyclic Imines

Cyclic imines (CI) (Figure 3) are toxins produced by dinoflagellates: SPXs: Alexandrium spp. [1,76], GYMs: Gymnodium spp. [77], PnTXs: Vulcanodinium rugosum [78] and PtTXs: biotransformation from PnTXs via metabolic and hydrolytic transformation in shellfish [1,5,77,78,79] (Table 1). CIs are a heterogenous group composed ofspirolides (SPXs), gymnodimines (GYMs), pinnatoxins (PnTXs) and pteriatoxins (PtTXs) and more than 24 structural analogs have been described to date [80].
Regarding chemical properties, these toxins are a group of macrocyclic compounds that have in common an imine functional group and spiro-linked ether moieties in their structure [80]. They are colorless amorphous solid macrocyclic compounds with imine and spiro-linked ether moieties [80], considerably soluble in organic solvents such as methanol, acetone, chloroform and ethyl acetate [5,80]. CIs are neurotoxins and actby inhibiting the nicotinic and muscarinic acetylcholine receptors (mAChR and nAChR, respectively) in the nervous system and at the neuromuscular junction [81]. CI bioactivity seems to depend on the imine functional group since the hydrolysis of spirolides A–D produce spirolide E and F with a keto-amine structure that is fully inactive [81]. To date, there are no regulations for CIs and no common symptoms can be recognized [82].

2.1.4. Brevetoxins

Brevetoxins (PbTxs) (Figure 4) are cyclic polyethers produced by dinoflagellates: Karenia spp. [4,16,87] (Table 1). There are two known types of BTXs, named type A and type B (also called type 1(PbTx-1) and type 2 (PbTx-2), respectively). The difference between two types of PbTxs consists in a few transfused rings that are ten for PbTx-1 and eleven for PbTx-2. The main analogs include PbTx-3, PbTx-6, PbTx-9, PbTx-B1, PbTx-B2, S-desoxy-PbTx-B2, PbTx-B3, PbTx-B4, and PbTx-B5 [44,88,89,90,91,92,93,94]. PbTxs are lipid-soluble cyclic polyether consisting of 10 to 11 transfused rings [95], stable and resistant to heat and steam autoclaving [96]. PbTxs cause neurotoxic shellfish poisoning (NSP) and actby binding with high affinity to receptor site 5 of the voltage-gated sodium channels (NaV) in cell membranes, and lactone is important for the toxin activity [97]. PbTxs are regulated in USA [98], New Zealand, and Australia [99,100] (Table 1).

2.1.5. Pectenotoxin Group

Pectenotoxins (PTXs) (Figure 5) are lipophilic polyethers produced by several dinoflagellate species [101] (Table 1). They contain spiroketal, bicyclic ketal, cyclic hemiketals, and oxolanes in their structure. To date, more than 15 PTX analogs have been documented and many are derived through biotransformation of PTX2 in marine organism metabolism such as bivalve mollusks [102]. The most reported analogs include PTX1, epi-PTX1, PTX2, PTX2 seco acid (PTX2 SA), 7-epi-PTX2 seco acid (7-epi-PTX2 SA), PTX3, PTX4, PTX6, epi-PTX6, PTX7, PTX11 (34S-hydroxy-PTX2) [6,101,103,104,105]. PTXs are heat-stable and unstable under alkaline conditions [103]. PTX and analogs alter actin-based structures [103,106] causing cell death and apoptosis [107]. PTXs co-occur with the OA—group and contribute to DSP in humans [108].

2.1.6. Yessotoxins

Yessotoxins (YTXs) (Figure 6) are produced by dinoflagellates species: Protoceratium reticulatum [4,109], Lingulodinium polyhedral [4] and Gonyaulax polyhedra [4] (Table 1). They are a heat-stable polyether, with eleven transfused ether rings, an unsaturated side chain, and two sulfate esters [110]. To date, more than 90 YTX analogues have been isolated [102] and only YTX, 45-hydroxyYTX, carboxylic, 1a-homoYTX, 45,46,47-trinorYTX, ketoYTX, 40-epi-ketoYTX, 41a-homoYTX, 9Me-41a-homoYTX, 44,55-dihydroxyYTX, 45-hydroxy-1a-homoYTX, carboxy-1a-homoYTX [111] have been fully identified [111]. The mechanism of action of YTX and their analogs is not fully understood; however, they are involved in phosphodiesterase activation [112] and modulation of calcium migration at several levels [113], alteration of protein disposal [114], cell change shape [115], apoptosis and cell death [116]. To date, there are no reports of human illness associated with YTXs [111].

2.1.7. Azaspiracids

Azaspiracids (AZAs) (Figure 7) are toxins produced by dinoflagellates: Azadinium spinosum [117] and Protoperidinum crassipes [118] (Table 1). They are colorless, odorless and amorphous solids of toxins containing a heterocyclic amine, a unique tri-spiro-assembly and an aliphatic carboxylic acid in their structures [117,119,120,121,122,123,124]. Around 21 compounds of AZAs are well known and documented [117,119,120,121,122,123,124] of which AZA, AZA2, AZA3, AZA4, and AZA5 are the most prevalent ones based on occurrence and toxicity in humans. AZAs are responsible for the AZP syndrome (Table 1) and their mechanism of action is the inhibition of hERG voltage-gated potassium channels [125].

2.2. Hydrophilic Toxins

Hydrophilic Toxins are polar soluble compounds and they include domoic acid (DA) and analogs, Paralytic Shellfish Toxins (PSTs), tetrodotoxins (TTXs) and palytoxins (PlTXs).

2.2.1. Domoic Acid and Analogs

Domoic acid (DA) (Figure 8) and analogs are polar cyclic amino acid toxins of diatom origin Pseudo-nitzschia spp. [126] and red algae: Chondria armata [127] (Table 1). They present three carboxylic acid groups and the most reported DA analogs include epi-domoic acid (epi-DA), domoic acid C5′-diastereomer and isodomoic acids A, B, C, D, E, F, G and H [iso-DA A-H] [128,129]. DA is the representative molecule of the DA-group that is responsible for amnesic shellfish poisoning (ASP) syndrome [130]. The characteristic symptomology of ASP is detailed in Table 1.

2.2.2. Paralytic Shellfish Toxins.

Paralytic shellfish toxins (PSTs) (Figure 9) are water-soluble tetrahydropurine toxins produced mainly by dinoflagellates Alexandrium spp. [2,3,7], Gymnodinium catenatum [3], Pyrodinium bahamense [3] and by cyanobacteria Trichodesmium erythraeum [131] except M (Figure 9) toxins that are Mytilus spp. metabolism products [132]. This group is composed of several analogs and they are prone to various conversions depending on pH (Figure 9), being divided into several groups: carbamoyl (saxitoxin (STX), neosaxitoxin (NeoSTX) and gonyautoxins (GTX1-4)) decarbamoyl [dc-](dcSTX, dcNeoSTX, dcGTX1-4), Nsulfo-carbamoyl [GTX5-6, C1-4], hydroxylated saxitoxins [M1-4] [133,134,135] and benzoyl toxins (GC1-3) [135]. Their heat stability is pH dependent (except for Nsulfo-carbamoyl components) [136]. STX and analogs act by binding to Nav and consequently blocking ion conductance in nerves and muscles fibers leading to paralysis [137]. Symptoms resulting from PSTs poisoning are described in Table 1.

2.2.3. Tetrodotoxins

Tetrodotoxins (TTXs) (Figure 10) are toxins produced by bacteria in marine environments: Serratia marcescens, Vibrio spp. [83], Aeromonas sp. [138], Microbacterium arabinogalactanolyticum [139], Pseudomonas sp. [140], Shewanella putrefaciens [141], Alteromonas sp. [142], Pseudoalteromonas ssp. [143], and Nocardiopsis dassonvillei [144] (Table 1). They are colorless, crystalline-weak basic compounds with one positively charged guanidinium group and a pyrimidine ring [145,146]. TTXpoisoning has been recognized since ancient Egyptian times [42]. To date, TTX is considered an extremely potent emergent toxin in the Atlantic Ocean [83] and acts by binding to Nav on the surface of nerve cell membranes blocking the cellular communication and causing death by cardio-respiratory paralysis [147]. Several poisoning incidents have reported in Asia [Japan is the most affected country] [148], the Mediterranean Sea and the Indian Ocean [35]. TTX is usually concentrated in the ovaries, liver, intestines, and skin ofits principal vector [puffer fish] [42]. To date, the structures of 26 analogs of TTX have been fully elucidated but their relative toxicity and occurrence are not yet fully known [145,146] except for 12compounds, namely, TTX, 11-oxoTTX, 11-deoxyTTX, 11-norTTX-6[R]-ol, 11-norTTX-6[S]-ol, 4-epiTTX, 4,9-anhydroTTX, 5,6,11-trideoxyTTX. [131], 4-CysTTX, 5-deoxyTTX, 5,11-dideoxyTTX, and 6,11-dideoxyTTX [149,150,151,152].

2.2.4. Palytoxin

Palytoxin (PlTX) and its derivatives (Figure 11) are toxins produced by marine zoanthids Palythoa spp., dinoflagellates: Ostreopsis ovata. [153,154,155] and possibly by cyanobacteria: Trichodesmium sp. [156] (Table 1). These polyhydroxylated toxins have both lipophilic and hydrophilic properties [157] with a partial unsaturated aliphatic backbone containing cyclic ethers, 64 chiral centers, 40–42 hydroxyl and 2 amide groups [157]. Among PlTX analogs, known are: isobaric PlTX, ostreocin-D, ovatoxin [a to f], mascarenotoxins, ostreotoxin-1 and 2, homopalytoxin, bishomopalytoxin, neopalytoxin, deopalytoxin and 42-hydroxypalytoxin and their molecular weights range from 2659 to 2680 DA [158,159,160]. PlTX and analogs act on Na+, K+ -ATPase pumps molecules in the cell membrane [161] and the loss of intracellular contents into the blood plasma and consequent injury causing rhabdomyolysis, among other signs, are the most reported as signs of PlTX poisoning [161].

2.3. Marine Cyanotoxins

Most marine toxins reported are produced mainly by microalgae (composed basically by dinoflagellates, diatoms, and marine bacteria), while cyanobacteria are reported as toxin producers in fresh, brackish waters and terrestrial habitats. Recently, cyanotoxins typical from freshwater have been identified in the marine environment [162]. Thus, this section will be focused on the description of the most reported marine cyanotoxins involved in seafood poisoning, their producers and mode of action (Table 1).
One of the most relevant groups of marine cyanotoxins is themicrocystin group (MCs) [163] (Figure 12). MCs are produced by cyanobacteria of genus Pseudoanabaena, Phormidium, Spirilia [164], Leptolyngbya, Oscillatoria, Geitlerinema [165], Trichodesmium [166] and Synechococcus [167] and their occurrence have been reported in many parts of the world, namely: the central Atlantic coast of Portugal [168], Canary Islands Archipelago [166], Brazilian coast [169], Amvrakikos Gulf (Greece) [167] and Indian Ocean [170]. To date, MCs is regulated in freshwater habitats but should be extended to the marine environments since there are reports of these hepatotoxins in marine environments [162].
Other reported marine cyanotoxins [in parenthesis is indicated their producers] (Figure 13) are aplysiatoxin (AT) [171] (Figure 13a), debromoaplysiatoxin (DAT) [171] (Figure 13) (algae Gracilaria coronopifolia [172] and cyanobacteria Lyngbya majuscule [171]), kalkitoxin (KTX) (cyanobacteria Lyngbyamajuscula [173]) (Figure 13b), lyngbyatoxins (LA, LB and LC) (cyanobacteria Lyngbya majuscule [174]) [Figure 13c], cylindrospermopsins (CYNs) (cyanobacteria Cylindrospermopsis raciborskii [175]) (Figure 13d), jamaicamides (JCDs) (Cyanobacteria Lyngbya majuscule [176]) (Figure 13e), anatoxins (ANTX) (cyanobacteria Hydrocoleum lyngbyaceum [177]) [178] (Figure 13f) andantillatoxins (ATX) (cyanobacteria Lyngbya majuscule [179]) (Figure 13g). The mechanism of action anddetection methods are presented in Table 1.
Recent studies indicate Homoanatoxin-a (HANTX, a derivative of anatoxin-a) produced by the cyanobacteria Hydrocoleum sp. and Trichodesmium sp. which co-occur with G. toxicus, may be the causative toxin of CFP [43] (rather than CTXs). This evidence suggests further studies to clarify marine cyanotoxins responsible for CFP and their mechanism of action [178]. The reports of seafood poisoning involving marine cyanotoxins are very scarce and consequently, there is no specific symptomology that can be related to marine cyanotoxin human poisoning.

3. Incidence of Harmful Algal Blooms MarineToxins and Consequent Poisoning Incidents along African Indian and the Red Sea Coasts

The main geographical focus of this review is the African Indian and the Red Sea coasts, including surrounding islands (Figure 14). The marine environment of this area is understudied due to a lack of monitoring infrastructure. There is a high rate of poverty in local communities, and the local population is vulnerable to natural disasters [including HABs, tropical storms]. The exponential increase in population accompanied by industrialization and climate change contributes to eutrophication in coastal areas [295,296]. This study area is characterized as subtropical to tropical climate with a water temperature above 20 °C [297]. Eutrophication and the transportation of cysts [through maritime traffic] are considered the main factors contributing to large phytoplankton blooms, including those comprised of HAB species and/or pathogenic bacteria [295,296]. Countries with monitoring programs of marine environments related to control of seafood poisoning are listed in Table 2. A few of these programs have noted the presence of MTs (Figure 14) and HAB species [dinoflagellates, cyanobacteria, diatoms], some of which [HAB species] were detected/confirmed by microscopic techniques and some confirmed by partial 16 S rRNA genes analysis [12,13,298,299,300,301,302,303,304,305,306,307,308,309,310,311,312,313,314,315,316,317,318,319,320,321,322,323].

3.1. South Africa

The occurrence of species of phytoplankton including MTs-producing HABs has been reported in coastal waters of South Africa through scientific reports and environmental monitoring programmes since 2011 [324]. Reported producer species include cyanobacteria (Microcystisaeruginosa, Oscillatoria sp., Trichodesmium sp.), dinoflagellates (Dinophysisacuminata, D. rotundata, Alexandrium catenella, A. minutum, Gymnodinium sp., Prorocentrum sp., Gambierdiscustoxicus, Ostreopsis siamensis, O. ovata, P. lima, P. concavum), diatoms (Pseudo-nitzschia multiseries) [19,305,309,315,331,332,333] and bacteria (Vibrio parahaemolyticus) [298]. Seafood poisoning cases were also reported in South Africa caused by PSTs, DSPs, PlTXs and GYM [19,216,309,334] (Table 3) after the consumption of mussels (Donax serra, Perna perna and Chloromytilus meridionalis) (Table 4) [37]. To minimize seafood poisoning by MTs, South Africa has implemented, through the Department of Agriculture, a program for MT monitoring in molluscan shellfish on all coasts (South African Molluscan Shellfish Monitoring and Control Programme) [324] (Table 2). This program was created based on the regulations of the European Commission (EC) Regulation, namely: Commission Regulation (EC) No 2074/2005, No 853/2004 and No 15/2011 where limit values are described for MTs and analytical techniques are advised to monitor shellfish [324].
Due to the absence of legislation regarding CTXs, currently, there is an absence of monitoring programs regarding this group in South Africa.Since the Indian Ocean is considered an endemic site of CTXs, this is a matter of major importance.

3.2. Mozambique

Studies related to HAB occurrence in Mozambique are very scarce and the few published works indicate the occurrence of dinoflagellates of the genus Alexandrium [313] and species of cyanobacteria (Phormidium ambiguum, Lyngbya majuscula, and Lyngbya cf. putealis) [307]. To date, due to the absence of a Monitoring Program and trained health staff to recognize specific symptoms of seafood poisoning in humans, there are no records of published data of MT occurrence or reports of seafood poisoning cases in this country.

3.3. Tanzania

Published studies indicate the occurrence of cyanobacteria, namely: Pseudanabaena sp., Spirulina labyrinthiformis, Spirulina sp., Leptolyngbya sp., Phormidium sp., Oscillatoria sp., Lyngbyaaestuarii, Lyngbya sp., Lyngbya majuscula, Nodularia sp., Synechococcus sp., Microcystis sp.; Dinoflagellates: Gambierdiscus toxicus, Procentrum sp. and diatoms: Pseudo-nitzschia sp., Pseudo-nitzschia pungens, P. seriata and P. cuspidate [335,336,337,338,339,340,341]. Data related to MTs and seafood poisoning episodes are very scarce in Tanzania. In 2003, the Tanzanian government created guidelines for investigation and control of foodborne diseases and the regulatory institution is the Tanzania Food and Drugs Authority (TFDA) (Table 2) [325]. The main objective of TFDA is to regulate matters related to food quality and safety for consumers through the dissemination of the information related to causative agents, latency period [duration], principal symptoms, typical vectors, and prevention of poisoning as measures of public health protection [325]. Among several foodborne disease sources, MTs such as CTXs, TTXs, DA, and PSTs are described by TFDA. The creation of alert and monitoring programs is an effective way to prevent poisoning episodes caused by MT-contaminated seafood.

3.4. Kenya

In order to reduce the cases of seafood poisoning caused by MTs, the Kenya Marine and Fisheries Research has carried out projects funded by governmental and non-governmental institutions for monitoring levels of HABs and their toxins (Table 2) in coastal waters and shellfish as well as the possible transfer in the trophic food web [326].Since October 2017, there is an ongoing project called: The occurrence and distribution of HABS in East and South Africa (BIOTOXINS Research Project] funded by National Commission for Science, Technology and Innovation (NACOSTI) at Mombasa Research Center [326]. This project will cover a period of 2 years, which is not enough for long-termmonitoring. In these coastal waters were reported to occur several species of diatoms: Nitzschia sp., N. closterium, N. longisigma, N. sigma, Pseudo-nitzschia sp. Guinardia sp., G. striata, G.delicatula, Skeletonema sp, Leptocylindrus sp., Rhizosolenia sp., Cerataulina sp., Coscinodiscus sp., Thalassiosira sp., Corethron sp., C. criopilum, C. cenofemus and Chaetoceros sp.; dinoflagellates: Alexandrium sp., Dinophysis sp., D. caudata, Gambierdiscus sp., G. toxicus, Gonyaulax sp., Gymnodinium sp., Gyrodinium sp., Ostreopsis sp., Peridinium sp., Prorocentrum sp., Ceratium sp., C. fusus, C. furca, Noctiluca sp., N. scintillans, Protoperidinium sp., Scrippsiella sp. and S. trochoidea [301,310]. Cyanobacteria were also reported: Lyngbya sp., Oscillatoria sp., Fischerella epiphytica, Anabaena sp., Nodularia spumigena, Umezakia natans, Aphanizomenon flos-aquae, Microcystis aeruginosa and Trichodesmium sp. [342].

3.5. Madagascar

Madagascar is the country with more records of published data regarding MT occurrence (Figure 14) and consequently, many reported cases of seafood poisoning [36,47,49,343]. The seafood poisoning cases in Madagascar have been registered since 1930 mainly after the consumption of fish of the family Sphyrnidae, Cacharinidae, Clupeidae (herrings, sardines), and marine turtles species (Eretmochelys imbricata and Chelonia mydas) [36,47,49,343]. The main marine poisoning causative agents reported are CTXs, TTXs, and PlTXs [18,344] (Table 4). To reduce the number of seafood poisoning events, the MadagascarMinistry of Health has created a Seafood Poisoning National Control Program (Table 2) based on the setting of an epidemiological surveillance network, prevention of the communities through educational programs and the development of research on marine eco-environment [327].

3.6. Indian Ocean French Islands

Mayotte, Europa, Banc du Geyser, Bassas da India, Glorioso, Juan de Nova, Reunion and Tromelin islands administratively make part in the French government but since they are in the Indian Ocean, were considered for the present study. In these islands, there are reports of the occurrence of HABs and cases of seafood poisoning linked to MTs. The reported HAB forming species include: dinoflagellates (Prorocentrum lima, P. convacum, Ostreopsis ovata, Gambierdiscus toxicus, Alexandrium spp.), cyanobacteria (Hydrocoleum sp., Lyngbya majuscula, Phormidium sp., Leptolyngbya sp. and Oscillatoria sp.) [70,300,317,319,345]. The recorded human intoxications were due to DSTs and TTXs [35,328] (Table 4). Centers of Disease for control and Preventing is the organization responsible for National Biomonitoring Program of toxins (PSTs) in these islands [35,328] (Table 2).

3.7. Mauritius

In Mauritius there are registered cases of seafood poisoning caused mainly by CTXs [346] after the consumption of reeffish (Lutjanus sebae) [70,71,71] (Table 4). The Ministry of Ocean Economy, Marine Resources, Fisheries and Shipping of Mauritius is the institute responsible for themonitoring of HABs (Table 2) [347,348], developing several activities and reporting the principal vectors species involved in seafood poisoning, namely: fish (Variola louti, Plectroponus maculatus, ceragidae, Vieille loutre, V. plate, V. cuisinier, Lutjanus gibbus, L. sebae, L. monostigmus, L. bohar, Anyperodon leucogramnicus, Harengula ovalis, Sphyraena barracuda, Synancela verrucose, Remora remora, Lactoria carnuta, Diodon hystrix), turtles (Eretmochelys imbricate), crabs (Carpillus maculatus), sea-urchins (Echinothrix sp.) and bivalves (Tridaena sp.) [348].
HAB producers recorded in Mauritius include several dinoflagellates species (Ostreopsis mascarenensis, Gambierdiscus toxicus Adachi & Fukuyo, Ostreopsis ovata Fukuyo, Ostreopsis siamensis, O. mascarenensis, Prorocentrum lima, P. concavum, P. hoffmanianum, Amphidinium sp., A. carterae, Coolia sp., Sinophysis sp., Gymnodinium sp., Gonyaulax sp., and Alexandrium sp.), diatoms (Pseudo-nitzschia sp.) and cyanobacteria (Phormidium sp., Oscillatoria sp. and Lyngbya sp., Phormidium sp., Oscillatoria sp. and Lyngbya sp.) [308].

3.8. The Archipelago of Comoros

Published data of the archipelago of Comoros indicate the occurrence of Gambierdiscus toxicus, G. yasumotoi, G. belizeanus, Prorocentrum arenarium, P. maculosum, P. belizeanum, P. lima, P. mexicanum, P. hoffmanianum, P. concavum, P. emarginatum, P. elegans, P. sp., Ostreopsis caribbeanus, O. mascarenensis, O. ovata O. heptagona, O. labens, O. siamensis, O. lenticularis, O. marinus, Cooliamonotis, C. tropicalis, Sinophysis microcephalus, S. canaliculate and Amphidiniopsis sp. [10,300]. Suspected seafood poisoning episodes linked to MTs were registered in the archipelago of Comoros after the consumption of turtle Eretmochelys imbricate with symptomatology similar to CFP [26], suggesting the presence of CTXs (Table 4).

3.9. Somalia and Seychelles

There are no published studies related to the occurrence of HABs and MTs in Somalia and Seychelles. While there are no published reports of HABs or MTs in Somalia and Seychelles waters, the proximity to other countries with such reports and currents in the area suggest that investigations are necessary to avoid potential seafood poisoning events [62].

3.10. Mediterranean and Red Sea (Djibouti, Eritrea, Sudan, Egypt)

Several research works related to MTs are carried out in the Red Sea but are very limited on the African coast. Saudi Arabia is the country with the most published studies related to the occurrence of HABs along the Red Sea [13,308,311,316,321,322,352,353]. The Dinoflagellates (Alexandrium sp., Dinophysis sp., Prorocentrum sp., Pyrodinium sp., Gymnodinium sp.), cyanobacteria (Lyngbya sp., Oscillatoria sp., Trichodesmium sp.) and diatoms (Pseudonitzschia spp.) are the most reported marine producer species [13,308,311,316,321,322,352,353]. The bacteria Vibrio paraehemolyticus, producer of TTX, was detected in shrimp (Penaeus latisulcatus) in the Suez Gulf [299]. MTs reported in the Red Sea, mainly the Egyptian coast, described in Table 3 and Table 4, include CTXs, TTXs, PSTs detected in puffer fish such as Pleuranacanthus sceleratus and Lagocephalus sceleratus [13,316,349,350,351,352,353]. Cases of seafood poisoning caused by CTXs and TTXs were reported, and according to the Poison Control Center, affiliated with Ain Shams University (Cairo, Egypt), CTXs are the third most responsible agents that induce food poisoning in Egypt [354]. Puffer fish poisoning has been recorded since ancient Egyptian times [42]. In Egypt, there is monitoring ofHABs in aquatic ecosystems since 1994 when Egypt became a member of the Convention on Biological Diversity although the Nature Conservation Sector, Egyptian Environment Affairs Agency and the Ministry of State for Environmental Affairs (Table 2) are focal points [330]. There are no reports of HABs and MT occurrence in coastal areas of Djibouti, Eritrea, and Sudan.

4. Final Considerations and Recomendations

African Indian Ocean and the Red Sea coasts have a subtropical and tropical climate, considered optimal for the development and transportation of several HAB-forming species, and consequently, the production of MTs. Paradoxically, studiesrelated to the occurrence and incidence of HABs and MTs are very limited, from South Africa to Egypt. From a few data available in this zone, most describe only the genus and not the full species, making it very difficult to evaluate the occurrence of the toxic species. The most reported HAB phytoplanktons in this region are cyanobacteria, followed by dinoflagellates, and diatoms as potential MT producers. Relative to MTs, the most reported and involved in seafood poisoning episodes include CTXs, PSTs, and TTXs. The scarcity of the data related to MTs suggests the need for further studies and the creation of specific monitoring programs of HABs, particularly for dinoflagellates and diatoms since these constitute the phytoplankton that produces more fatal MTs, though in recent years several genera of bacteria have been described as producers of a potent group of marine toxins, TTXs, which have already been detected on the African coasts of the Indian Ocean and Red Sea. The main MTs that must be monitored in shellfish are presented in Table 5. Analytical techniques such as LC-MS/MS are advised and recommended as determination and quantification methods due to their higher reproducibility, specificity, sensitivity and capacity to discriminate analogs of given toxins in the sample. The permitted limit of a toxin in shellfish can be adopted from other countries as an example to follow such as the EU region, USA, Japan, Australia, and New Zealand.
For the success of the MT monitoring programs, the integration and intercollaboration of environmental, public health and researches institutions and universities of the all African Countries of the Indian Ocean and the Red Sea is crucial.

Author Contributions

Conceptualization, V.V. and M.S.; Writing-Original Draft Preparation, I.J.T.; Writing-Review & Editing, I.J.T, M.S. and V.V.; Supervision, V.V. and M.S.

Funding

This research was supported by the project Alertox-Net [EAPA-317-2016] of the Interreg Atlantic Area Program funded by the European Regional Development Fund and by the Portuguese Foundation of Science and Technology [FCT] project UID/Multi/04423/2013.

Acknowledgments

We acknowledge the project EMERTOX [grant 734748], funded by H2020-MSCA-RISE 2016.

Conflicts of Interest

The authors declare no conflict of interest.

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Toxins 11 00058 g001 550
Figure 1. Chemical structure of OA and main derivatives [DTX1, DTX2, and DTX3].
Figure 1. Chemical structure of OA and main derivatives [DTX1, DTX2, and DTX3].
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Figure 2. Chemical structure of major CTXs analogs from Pacific (P-CTXs) (a) and Caribbean (C-CTXs) (b) regions. The major CTXs from Indian region (I-CTXs) have a similar structure with C-CTX-1. (c) Chemical structure of maitotoxin (MTX).
Figure 2. Chemical structure of major CTXs analogs from Pacific (P-CTXs) (a) and Caribbean (C-CTXs) (b) regions. The major CTXs from Indian region (I-CTXs) have a similar structure with C-CTX-1. (c) Chemical structure of maitotoxin (MTX).
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Figure 3. Chemical structures of CI (SPXs (a), GYMs (b), PnTXs (c), and PtTXs (c),) and Silva et al. [79,83,84,85,86].
Figure 3. Chemical structures of CI (SPXs (a), GYMs (b), PnTXs (c), and PtTXs (c),) and Silva et al. [79,83,84,85,86].
Toxins 11 00058 g003aToxins 11 00058 g003b
Toxins 11 00058 g004a 550Toxins 11 00058 g004b 550
Figure 4. Chemical structures of the main group of PbTxs (PbTxs-A and PbTxs-B). The capital letter A in first ring indicates type A and type B (also called type 1and type 2, respectively [4]). These rings contain lactone group that is most important for the toxin activity.
Figure 4. Chemical structures of the main group of PbTxs (PbTxs-A and PbTxs-B). The capital letter A in first ring indicates type A and type B (also called type 1and type 2, respectively [4]). These rings contain lactone group that is most important for the toxin activity.
Toxins 11 00058 g004aToxins 11 00058 g004b
Toxins 11 00058 g005 550
Figure 5. Chemical structures of main pectenotoxins.
Figure 5. Chemical structures of main pectenotoxins.
Toxins 11 00058 g005
Toxins 11 00058 g006 550
Figure 6. Chemical structures of YTXs n corresponds to the number of methyl groups in the molecule.
Figure 6. Chemical structures of YTXs n corresponds to the number of methyl groups in the molecule.
Toxins 11 00058 g006
Toxins 11 00058 g007 550
Figure 7. Chemical structure of AZAs.
Figure 7. Chemical structure of AZAs.
Toxins 11 00058 g007
Toxins 11 00058 g008 550
Figure 8. Chemical structure of DA and analogs.
Figure 8. Chemical structure of DA and analogs.
Toxins 11 00058 g008
Toxins 11 00058 g009 550
Figure 9. Chemical structures of STX group.
Figure 9. Chemical structures of STX group.
Toxins 11 00058 g009
Toxins 11 00058 g010 550
Figure 10. Chemical structure of TTX and their main analogues.
Figure 10. Chemical structure of TTX and their main analogues.
Toxins 11 00058 g010
Toxins 11 00058 g011 550
Figure 11. Chemical Structure of PlTXs [PTX and Ostreocin-D].
Figure 11. Chemical Structure of PlTXs [PTX and Ostreocin-D].
Toxins 11 00058 g011
Toxins 11 00058 g012 550
Figure 12. Chemical structure of MC.
Figure 12. Chemical structure of MC.
Toxins 11 00058 g012
Toxins 11 00058 g013a 550Toxins 11 00058 g013b 550
Figure 13. Chemical structures of Aplysiatoxin (AT) and Debromoaplysiatoxin (DAT) (a); kalkitoxins (KTX) (b); lyngbyatoxins A, B and C (LA, LB and LC) (c); cylindrospermopsins (CYN) (d); jamaicadimes (JCD) (e); anatoxin-a (ANTX) and homoanatoxin-a (HANTX) (f) and antillatoxins (ATX) (g).
Figure 13. Chemical structures of Aplysiatoxin (AT) and Debromoaplysiatoxin (DAT) (a); kalkitoxins (KTX) (b); lyngbyatoxins A, B and C (LA, LB and LC) (c); cylindrospermopsins (CYN) (d); jamaicadimes (JCD) (e); anatoxin-a (ANTX) and homoanatoxin-a (HANTX) (f) and antillatoxins (ATX) (g).
Toxins 11 00058 g013aToxins 11 00058 g013b
Toxins 11 00058 g014 550
Figure 14. Map of the incidence of marine toxins (MT) along African countries of the Indian Ocean and the Red Sea, from EgypttoSouth Africa and nearby islands. Red circles [ Toxins 11 00058 i001]—confirmed or suspected seafood poisoning episodes caused by MT; green circles [ Toxins 11 00058 i002]—MT or Harmful Algal Blooms monitoring programmes or Centers of seafood poisonings; Toxins 11 00058 i003—Saxitoxins group; Toxins 11 00058 i004—Okadaic Acid group; Toxins 11 00058 i005—Ciguatoxin group; Toxins 11 00058 i006—Palytoxin group; Toxins 11 00058 i007—Domoic Acid group and Toxins 11 00058 i008—Tetrodotoxin group.
Figure 14. Map of the incidence of marine toxins (MT) along African countries of the Indian Ocean and the Red Sea, from EgypttoSouth Africa and nearby islands. Red circles [ Toxins 11 00058 i001]—confirmed or suspected seafood poisoning episodes caused by MT; green circles [ Toxins 11 00058 i002]—MT or Harmful Algal Blooms monitoring programmes or Centers of seafood poisonings; Toxins 11 00058 i003—Saxitoxins group; Toxins 11 00058 i004—Okadaic Acid group; Toxins 11 00058 i005—Ciguatoxin group; Toxins 11 00058 i006—Palytoxin group; Toxins 11 00058 i007—Domoic Acid group and Toxins 11 00058 i008—Tetrodotoxin group.
Toxins 11 00058 g014
Table
Table 1. Marine toxins and their symptoms, producers, permitted limit, detection methods, limit of detection/limit of quantification [LOD/LOQ] and toxicity equivalency factors [TEF] according to the European Food Safety Authority [EFSA].
Table 1. Marine toxins and their symptoms, producers, permitted limit, detection methods, limit of detection/limit of quantification [LOD/LOQ] and toxicity equivalency factors [TEF] according to the European Food Safety Authority [EFSA].
Toxin (Syndrome)SymptomsDetectionPermitted LimitToxin (TEF)Producer
MethodsLOD, μgKg−1LOQ, μgKg−1
OA and analogs (DSP)diarrhea, nausea, vomiting, abdominal pain and tumor formation in the digestive system [50]BA [180,181]160 0.16mg OA equivalents/Kg shellfish meat in EU region [182]OA[1.0]Dinoflagellates: Prorocentrum spp. [8], Dinophysis spp. [2,6,9,10,15,53,54] and Phalacroma rotundatum [55]
DTX1[1.0]
EIA [183,184,185,186]10–26 3–41
DTX2 [0.6]
LC-MS [183], -UVD [187]15–301–50
DTX3 [1.0; 1; 0.6]
CTXs and analogs (CFP)vomiting, diarrhea, nausea,
tingling, itching, hypotension, bradycardia. In extreme cases, death through respiratory failure in 30 min and 48 h after fish consumption [50]		BA [188,189]0.16–0.560 P-CTX [190] 0.01 μg P-CTX-1 equivalents/kg of fish in USA [191]P-CTX-1[1.0]Dinoflagellates: Gambierdiscus toxicus, Ostreopsis siamensis and Prorocentrum lima [59]
CTA [192,193,194]~106 - 0.039 C-CTX P-CTX-2[0.3]
2,3-dihydroxy P-CTX-3C[1.0]
EIA [72,189,195,196,197,198,199]-0.032 P-CTX
LC-MS/MS
[67,70,71,74,200], -UVD [62,201,202]		 C-CTX-1[0.1]
CIsnon-specific symptoms such as gastric distress and tachycardia in humans [82]BA5.6–77 PnTXE Not regulated 13-desmethyl SPX C[1.0]Dinoflagellates: SPXs: Alexandrium spp. [1,76], GYMs: Gymnodium spp. [77], PnTXs: Vulcanodinium rugosum [78] and PtTXs: biotransformation from PnTXs via metabolic and hydrolytic transformation in shellfish [1,5,77,78,79]
FPA [203]80–85 13-SPXC
LC-MS/MS [79,204], - UVD [205]0.8–20 13-SPXC/GYMA
PbTxs and analogs (NSP)nausea, vomiting, diarrhea, paresthesia, cramps, bronchoconstriction, paralysis, seizures in 30 min to 3 h [87]BA [206] 800 μg BTX-2 equivalents/kg shellfish in USA [98], New Zealand, and Australia [99,100]BTX-2, BTX-3, BTX2-B2 and S-deoxy-BTX-B2 [same TEF]Dinoflagellate: Karenia spp. [4,16,87]
CTA [192]250 BTX-1
RB [108]30BTX-3
EIA [207,208]1 BTXs and 25 BTXs
LC – MS/MS [209]0.2 – 2 BTXs
PTX and analogsNo specific symptomsMBA- 160 µg OA equivalents./kg shellfish meat in EU region [210]PTX [1,2,3,4,6 and 11][1.0]Dinoflagellate: Dinophysis acuta [101]
EIA [207]-
PTX [7,8,9 and 2SA] and 7-epiPTX2 SA [<<10]
LC – MS/MS [211,212]1
YTX and analogsNo specific symptomsBA 3.75 mg YTX equivalents/Kg shellfish meat in EU region [124]YTX[1.0]Dinoflagellate: Protoceratium reticuatum [4,109], Lingulodinium polyedrum [4] and Gonyaulax polyhedral [4]
EIA [213] 1a-homoYTX[1.0]
45-hydroxyYTX[1.0]
LC-MS/MS [111]0.017
45-hydroxy-1a-homoYTX[0.5]
AZA and analogs (AZP)nausea, vomiting, diarrhea and decreased reaction to stomach cramps, deep pain, dizziness, hallucinations, confusion, short-term memory loss, seizure [214]BA [181]0.05 0.16 mg AZA1equivalents/Kg shellfish in EU region [210]AZA1[1.0]Dinoflagellates: Azadinium spinosum [117] and Protoperidinum crassipes [118]
AZA2[1.8]
LC-MS/MS
AZA3[1.4]
AZA4[0.4]
AZA5[0.2]
STX and analogs (PSP)Numbness in the face and neck; headache,
dizziness, nausea, vomiting, diarrhea, muscular paralysis; pronounced respiratory difficulty;
death through respiratory paralysis [215]		BA [216,217] 0.8 mg STX equivalent/Kg shellfish in EU region [210]STX[1.0]Dinoflagellates: Alexandrium spp. [2,3,7], Gymnodinium catenatum [3], Pyrodinium bahamense [3] and cyanobacteria Trichodesmium erythraeum [131]
NSTX[1.0]
SBA [218] GTX1[1.0]
GTX2[0.4]
GTX3[0.6]
CTA [192,219] GTX4[0.7]
GTX5[0.1]
Antibodies Assay [220,221,222,223,224] GTX[0.1]
C2[0.1]
Eletrophoresis [225] C4[0.1]
de-STX[1.0]
LC-MS/MS [226,227,228,229]23–42 STX de-GTX3[0.2]
de-NSTX2[0.2]
de-GTX3[0.4]
11-hydroxy-STX[0.3]
DA and analogs (ASP)nausea, vomiting, diarrhea or abdominal cramps] within 24 h of consuming DA contaminated shellfish and/or neurological symptoms or signs [confusion, loss of memory or other serious signs such as seizure or coma] occurring within 48 h BA [230]40 20 mg DA equivalents/Kg shellfish in EU region [210] Diatoms: Pseudo-nitzschia spp. [126] and red algae: Chondria armata [127].
(a) ASP- EIA [184,231]0.003 0.01
SPR [232]20
RB [233,234,235]20
Capillary electrophoresis [236,237,238]0.15 -1
LC -MS/MS [211,239,240], UVD [241,242]0.015
TLC [243]10
TTX and analogsVomiting, strong headache, muscle weakness, respiratory failure, hypotension and even death in hours [244]BA [144,245,246,247]1.1 [247] 2 mg TTX equivalents/Kg shellfish in Japan [248]S/R 11-norTTX-[6]-ol[0.19/0.17]Bacteria: Serratia marcescens, Vibrio spp. [83], V. Aeromonas sp. [138], Microbacterium, arabinogalactanolyticum [139], Pseudomonas sp. [140], Shewanella putrefaciens [141], Alteromonas sp. [142], Pseudoalteromonas sp. [143], and Nocardiopsis dassonvillei [144]
RB [249]2–4.10−3TTX
4-epiTTX[0.16]
EIA [245,246,247,250,251,252,253,254,255,256]0.002/mL [255], 0. 0001/mL [253]
TLC [139,257]2 [257] 4,9-anhydroTTX[0.02]
GC-MS [28,258,259]500 1000 [258]
5,6,11-deoxyTTX[0.01]
LC-MS/MS [260,261,262,263,264] – FLD [265]0. 00009?-24.5 [260,261,262,263,264]40 [265] – 100 [265]
PlTXVasoconstriction, hemorrhage, myalgia, ataxia, muscle weakness, ventricular fibrillation, ischemia and death [266,267] and rhabdomyolysis [268]BA Not regulated toxin but proposed value is 0.25mg PlTX equivalent/Kg shellfish in EU region [269]PlTX[1.0]Zoanthids: Palythoa spp. anddinoflagellates: Ostreopsis ovata. [153,154,155] and possibly cyanobacteria: Trichodesmium sp. [156]
Hemolysis assay [270]1.6
CTA [107]50
streocin-D[0.4–1.0]
EIA [254]1/mL
LC-MS/MS [204,271]–FLD and–UVD [272]2,5.10−5–0, 50.10−5
MCliver hemorrhage within a few hours of an acute dose and death [273]LC-MS [167,274,275,276] and EIA [277] Tolerable daily intake: 0.04 μg/kg of MC body weight/day [278] Cyanobacteriaof genus: Pseudoanabaena, Phormidium, Spirilia [164], Leptolyngbya, Oscillatoria, Geitlerinema [165], Trichodesmium [166] and Synechococcus [167]
ANTX and HANTXHypersalivation, diarrhea, shaking and nasal mucus discharge [279], respiratory arrest and death [280]RB and GC/MS [281,282] Cyanobacteria: Hydrocoleum lyngbyaceum [177]
AT and DATContact dermal: dermatitis initiating with erythema
and burning sensations, appearing a few hours after exposure,
gave way to blister formation and deep desquamation,
lasting up to several days
[283,284] and consumption of contaminated seafood; burningsensation in the mouth and throat, vomiting and diarrhea [285]		LC-MS/MS [286] Algae Gracilaria coronopifolia [172] and cyanobacteria Lyngbya majuscula [171]
LA, LB, and LC Cyanobacteria Lyngbya majuscule [174]
ATX and analogsNo specific symptomsLC [287] Cyanobacteria: Lyngbya majuscula [179]
JCD and analogsNo specific symptomsLC, TLC and [288] Cyanobacteria: Lyngbya majuscula [176]
KTX and analogsNo specific symptomsLC [173] Cyanobacteria: Lyngbya majuscula [173]
CYN and analogsGastroenteritis [289]LC-MS/MS [290],–PDAD [291]1 [292]–200 [293] Cyanobacteria: Cylindrospermopsis raciborskii [175]
EIA [294]
Toxins: DA—domoic acid, DTX, CTX -ciuatoxin, AZA—azaspiracid, CI—cyclic imines, PTX—pectenotoxin, YTX—yessotoxin, STX—saxitoxin, OA—okadaic acid, BTX—revetoxin, PlTX—palytoxin, TTX -tetrodotoxin, MC—microcystin, ANTX—anatoxin, HANTX—homoanatoxin, LA, LB and LC—lyngbyatoxins A, B and C respectively. ATX—antillatoxin, KTX—kalkitoxin, CYN—cylindrospermopsins AT—aplysiatoxin, DAT—debromoaplysiatoxin, JCD—jamaicamides, Syndrome: PSP—Paralyc Poisoning, DSP—Diarrheic Shellfish Poisoning, ASP—Amnesic Shellfish Poisoning, AZP—Azaspiracid Shellfish Poisoning, CFP—CiguateraShellfish Poisoning, NSP—Neurologic Shellfish Poisoning, Detection methods: CTA—Cytotoxicity assay, EIA—Enzyme-ImmunoAssay, SPR—Surface Plasmon Resonance, RB—Receptor-based, GC—Gas Chromatography, BA—Bioassay; UVD—Ultra Violet Detection; LC—Liquid Chromatography and MS—Mass Spectroscopy, FPA—Fluorescence Polarization Assay, TLC—Thin Layer Chromatography, SBA—Saxitoxin Binding Assay, PDAD—photo diode array detection.
Table
Table 2. MT monitoring scenario of the African countries of the Indian Ocean and the Red Sea.
Table 2. MT monitoring scenario of the African countries of the Indian Ocean and the Red Sea.
CountryMonitored MTPermitted Limit, mgKg−1 ShellfishDetectionLaboratories for Toxin AnalysisReference
South AfricaPST0.8 STX Research centers and Universities[324]
OA, DTX1-2, PTX1-20.16 mg OALC-MS/MS
YTX, 45 OH YTX, homo YTX, and 45 OH homo YTX8 mg YTXLC-MS/MS
AST20 mg DA
AZA1-30.16 mg OALC-MS/MS
MozambiqueN.D.N.D.N.D.N.D.N.D.
TanzaniaCTX, TTX, ASTN.D.Symptomology and vectorsN.D.[325]
KenyaMT producers [HAB]N.D.N.D.Mombasa Research Center[326]
MadagascarN.D.N.D.Educational programmesResearches centers and Universities[327]
French IslandsN.D.N.D.N.D.Researches centers[35,328]
MauritiusN.D.N.D.N.D. [324]
ComorosN.D.N.D.N.D.N.D.
Somalia and SeychellesN.D.N.D.N.D.N.D.
EygptN.D.N.D.N.D.Poison Control Center, Ain Shams University [329,330]
DjiboutiN.D.N.D.N.D.N.D.
EritreaN.D.N.D.N.D.N.D.
SudanN.D.N.D.N.D.N.D.
N.D.—No Data.
Table
Table 3. Geographic occurrence MT per country, MT producer, and MT vector along African countries of the Indian ocean and red sea coasts. TX - toxin.
Table 3. Geographic occurrence MT per country, MT producer, and MT vector along African countries of the Indian ocean and red sea coasts. TX - toxin.
ToxinDateLocationToxin ProducerDetermination MethodToxin VectorTX Concentration, (mg TX Equivalents per Kg Shellfish Meat)Cell/Extract ToxicityReference
PSTs1999South AfricaAlexandrium catenellaAOAC mouse bioassayHaliotis midae0. 01609 STX [22]
1998–2002South Africa: Yzerfontein, Alexandrium catenellaHPLC-FLD--4.8 pg STX eq cell−1[334]
Alexandrium tamiyavanichi0.14 pg STX eq cell−1
2003–2004South Africa: Cape Town Alexandrium minutumLC-FD and HILIC-MS/MS--0.65 pg GTX cell−1[309]
2012–2014Central
Red Sea		Pyrodinium bahamense, Ceratium sp., Alexandrium sp. and Protoperidinium spp.ELISA -->> 0.4 ng mL1 [349]
DSTs2000Europa Island Mozambic channel, France]Prorocentrum arenariumFR3T3 fibroblast --IC50 = 0,1 µg OA ml−1 and 50 µg extract ml−1[11]
PPIA
HPLC-FD
HPLC-MS22 ng OA/mg of extract
2001Lagoons of La Reunion Mayotte and Mauritius IslandsProrocentrum
lima		PPIA- -IC50 1.3–25 mg/mL onon fibroblast;6261.3 ± 156.5 − 128.3±17.2 ng eq OA/mg crudeextract[328]
2002–2018South Africa:Abalgold--Haliotis asinina--[324]
2008South Africa: Saldanha Bay and
Lambert’s Bay 		Dinophysis acuminataLC-MS/MSCrassostrea gigas0.267 OA
Choromytilus meridionalis0.012 OA
CTXs2001Mauritius: Nazareth, Saya de Malha and Soudan-HPLC-MS/RLB, Mongoose feeding test, and MBALutjanus sebae and
Lutjanus
Lab		Qualitative analysis-[71]
2002North of the Republic
of Mauritius, Banks fishery 		-HPLC-MS/RLBLutjanus sebae -[70]
2012–2013Central Red SeaGambierdiscus belizeanus and
Ostreopsis spp.		Mouse neuroblastoma cell-based assay--6,50–1,14.10 −5 pg P-CTX−1 eq. cell−1[350]
2013Madagascar: district of Fenoarivo Atsinanana Gambierdiscus spp.CBA Carcharhinus leucas0.083
P-CTX-1		-[20]
MBA 0. 09272 P-CTX-1
LC-ESI-HRMS0. 01628 P-CTX-1
MBA752 MU/g
PlTXs1994Madagascar:
Antalaha District		Ostreopsis siamensisMBAHerklotsichthys quadrimaculatus0. 00045 PTXs/fish [head and esophagus] [18]
Hemolysis assays0. 00002 PTXs/fish [head and esophagus]
Cytotoxicity tests0. 00000005/fish [head and esophagus]
MS
1996Mauritius: Rodrigues IslandOstreopsis mascarenensisHPLC-diode array detector, Nanoelectrospray ionization quadrupole time-of-flight and HPLC-ESI-MS/MS analysis -- [14,160]
Hemolysis assays 8.00 ± 0.01 ng PTX mL−1
Cytotoxicity AssayIC50 = 10 μM against human H460 lung cancer cells
2008South Africa: Saldanha Bay and
Lambert’s Bay 		Dinophysis acuminataLC-MS/MSCrassostrea gigas0.267 OA
Choromytilus meridionalis0.012 OA
DA cultures 2012South Africa: Algoa BayPseudo-nitzschia multiseriesELISA--0.076 pg DA cell−1–0.098 pg DA cell–1[12]
LC/MS–MS0.086 pg DA cell–1–0.086 pg DA cell–1
TTXs 1990–1991Egypt: Suez City, in the northwestern
part of the Red Sea		 TLC, electrophoresis, UV, GC–MS Pleuranacanthus
sceleratus		 [316]
752 MU/g
MBA
1998Madagascar: Nosy Be Island --MBA 16 MU/g [41]
2002–2003Egypt: Gulf of Suez MBALagocephalus sceleratus3950
MU/g		 [351]
2013Reunion Island MBA and LC-MS/MSLagocephalus sceleratus17 TTX-[35]
Table
Table 4. Seafood poisoning episodes caused by MTs, observed effects/Symptoms, fish or shellfish consumed and victim number affected along African countries of the Indian Ocean and Red sea coasts. TX - Toxin
Table 4. Seafood poisoning episodes caused by MTs, observed effects/Symptoms, fish or shellfish consumed and victim number affected along African countries of the Indian Ocean and Red sea coasts. TX - Toxin
LocalDateSeafoodObserved Effects/SymptomsTXDetection MethodTX Concentration, (mg TX Equivalents/Kg Shellfish Meat)Victim NumberReference
Comoros islands:
Ndrondroni 		24 December 2012Eretmochelys imbricata
(turtle)		Itching, Asthenia, Vomiting, Abdominal pain, Rash Myalgia
Shortness of breath, Nausea
Itching of the mouth/throat, Fever, Diarrhea Vertigo, Paresthesia, Dysphagia
Mouth burn Sore throat, Erectile dysfunction		---49 suspected cases and 8 probable cases, age range [0–40 years], 1 death[26]
North-eastern coast of MadagascarDecember 1994TurtleNausea, vomiting, dysphagia, acute stomatitis---60 persons with poisoning attack rate were 48% with a lethality of 7.7%[47],
Madagascar: district of Fenoarivo AtsinananaNovember 2013Carcharhinus leucas (shark)Paresthesia of the extremities, dysesthesia, and reversing sensitivity of hot and cold accompanied by a headache, dizziness, and arthralgia between 2 and 12h after ingestion CTXsMBA0.083
P-CTX-1 		124 people, 9% deaths[20]
CBA0. 09272 P-CTX-1
Madagascar: Antalaha DistrictJanuary 1994Herklotsichthys quadrimaculatus (Fish)Malaise, uncontrollable vomiting, diarrhea, tinglings of extremities,
delirium and death		PlTXsMBA0. 00045 PTXs/fish [head and esophagus]Death of one adult[18]
Hemolysis assays0. 00002 PTXs/fish (head and esophagus)
Cytotoxicity tests0. 00000005/fish (head and esophagus)
Mass spectroscopy-
Madagascar: Nosy Be IslandJuly 1998--TTXsMBA16 MU/g (no data to covert to mg/Kg)4 people, one death[41]
Madagascar: Manakara district November 1993Carcharhinus amboinensis [shark] Deep coma and death,
body rigidity due to loss of cerebral function,
myosis, mydriasis,
convulsions, Respiratory distress due to acute pulmonary edema, cardiovascular collapse, bradycardia, gengivorrhagia
Dehydration, paresthesia on fingertips and toes, dizziness,
pruritus, narcosis, faintness, hyperthermia, ataxia asthenia, dehydration, cephalalgia, diarrhea, epigastralgia, laryngeal distress		CTXsCiguatera poisoning Symptomology-500 people, 20% deaths[21]
South Africa: Cape TownMay 1978Choromytilus meridionlis [Mussel]Paraesthesia of en
fingers/hands, Circumoral paresthesia, paranesthesia of toes/feet, Vertigo, Floating sensation, Ataxia, Weakness of upper, Weakness of lower limbs and Dysarthria
A headache		PSTsMBA72.83 STX17 people, no deaths[39]
South Africa: Natal coastDecember 1957Mytilus
meridionalis [Mussel]		peculiar
lightness of the body, with a tingling around mouth, finger, and toes; no moving; feeble inarticulate noise;		PSTsMBA0.04 STX5 people and one cat[40]
South Africa: Table and False Bays1888Donax serra [Mussel]-----[37]
South Africa: Cape TownApril 1948Donax serra [Mussel] and Chloromytilus
meridionalis [Mussel]		----One death
South Africa: Natal coastDecember 1957Perna perna [Mussel]----5 people, one death
South Africa: Cape Town aMay 1958Chloromytilus meridionalis [Mussel]-- -One death
Reunion IslandSeptember 10th, 2013Lagocephalus sceleratus [fish]peri-oral paresthesia, weakness of both lower limbs, paresthesia all over the body, headache, dyspnea,
nausea and vomiting, blurring of vision, and vertigo		TTXMBALiver: 17 TTX
Flesh: 5 TTX 		10 people[35]
Table
Table 5. Recommended marine toxins to be monitored and suggestion of permitted limit to be used.
Table 5. Recommended marine toxins to be monitored and suggestion of permitted limit to be used.
ToxinSyndromePermitted Limit, mgKg−1To be adopted from
STXPSP0.8 STXeqEU region
CTXCFP0.00001 P-CTX-1eqUSA
YTX-3.75 YTXeqEU region
PTX-0.16 OAeqEU region
TTX-2 TTeqJapan
DAASP20 DAeqEU region
OADSP0.16 OAeqEU region
AZAAZP0.16 AZAeqEU region
PlTX-0.25 PlTXeq *EU region
PbTxNSP0.8 TX-2 eqUSA, New Zealand, and Australia
* This toxin is not monitored and 0.25 PlTXeq was proposed in the first meeting (Cesenatico, Italy, 24–25 October 2005) of the working group on Toxicology of the national reference laboratories [NRLs] for Marine Biotoxins.

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Tamele, I.J.; Silva, M.; Vasconcelos, V. The Incidence of Marine Toxins and the Associated Seafood Poisoning Episodes in the African Countries of the Indian Ocean and the Red Sea. Toxins 2019, 11, 58. https://doi.org/10.3390/toxins11010058

AMA Style

Tamele IJ, Silva M, Vasconcelos V. The Incidence of Marine Toxins and the Associated Seafood Poisoning Episodes in the African Countries of the Indian Ocean and the Red Sea. Toxins. 2019; 11(1):58. https://doi.org/10.3390/toxins11010058

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Tamele, Isidro José, Marisa Silva, and Vitor Vasconcelos. 2019. "The Incidence of Marine Toxins and the Associated Seafood Poisoning Episodes in the African Countries of the Indian Ocean and the Red Sea" Toxins 11, no. 1: 58. https://doi.org/10.3390/toxins11010058

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