Ciguatera Fish Poisoning: Past, Present, Future

Historical

Etiology /Ecology

Modern / Hawaiian Findings

Perspective for the FuturePerspective for the Future

• Bad News

• Good News

Poisoning: Past,

Acknowledgements

GEOHAB/BHAB Initiative of the International Oceanographic Commission, Scientific Committee on Oceanographic Research (SCOR/UNESCO)

This research was funded by National Science Foundation Grants OCE004-32479, OCE08-52301, and OCE11

Acknowledgements

GEOHAB/BHAB Initiative of the International Oceanographic Commission, Scientific Committee on Oceanographic Research

This research was funded by National Science Foundation Grants , and OCE11-29119

Ciguatera Fish Poisoning

• Occurs in tropical and subtropical regions

• Vector is exclusively reef fish

• Affects hundreds of thousands of people annually

• Underreported; misdiagnosed

Ciguatera Fish Poisoning

Occurs in tropical and subtropical regions

Vector is exclusively reef fish

Affects hundreds of thousands of people annually

Underreported; misdiagnosed

Urdaneta, 1580

Autumn 1525

Benthic Hazardous Algae

Oceans & Human Health Perspective

Gambierdiscus ecophysiology

Ciguatoxin(s)

CFP PrevalenceCFP Prevalence

CFP & Climate Change

Benthic Hazardous Algae

Oceans & Human Health Perspective

Ciguatera Sequence

Environmental conditions

Fish �

Gambierdiscus � Macroalgae � Herbivorous Fish

Fish �

Ciguatera Sequence

conditions ���� Gambierdiscus

Humans

Herbivorous Fish � Carnivorous Fish � Fishing Pressure

Humans

Gambierdiscus spp.

Why is Progress so Slow?

Detection

Diagnosis

Reporting

Societal Initiatives & CapabilitiesSocietal Initiatives & Capabilities

Why is Progress so Slow?

Ciguatoxin Molecule

Uncertainties in the CFP Cycle

• Increased proportions of toxic fish?

• Increased toxicity in the fish present?

• Increased fish harvesting and consumption by humans?

• Due to fish eating more toxic algal substrate?

• Due to different grazing patterns?

CFP INCIDENCE

INCREASED TOXICITY

IN HERBIVOROUS

FISH• Due to progressive toxin accumulation in older fish?

• Due to increased G. toxicus biomass?

• Due to increased specific toxicity of G. toxicus biomass present?

• Due to specific G. toxicus clone that produces CTX?

• Do certain conditions stimulate the growth of G. toxicus?

• Do certain conditions change the macroalgae where the G. toxicus grows?

• Do certain conditions stimulate the specific toxicity of G. toxicus?

FISH

INCREASED TOXIC

ALGAL SUBSTRATE

TRIGGERING

ENVIRONMENTAL

CONDITIONS

Uncertainties in the CFP Cycle

Increased proportions of toxic fish?

Increased toxicity in the fish present?

Increased fish harvesting and consumption by humans?

Due to fish eating more toxic algal substrate?

Due to different grazing patterns?

Due to progressive toxin accumulation in older fish?

Due to increased G. toxicus biomass?

Due to increased specific toxicity of G. toxicus biomass present?

Due to specific G. toxicus clone that produces CTX?

Do certain conditions stimulate the growth of G. toxicus?

Do certain conditions change the macroalgae where the G. toxicus grows?

Do certain conditions stimulate the specific toxicity of G. toxicus?

Reported Ciguatera IncidentsHawaii – 1963 to 2005

25

30

35

40

45

50

0

5

10

15

20

25

19631966196919721975197819811984

Reported Ciguatera Incidents

N = 676

19841987199019931996199920022005

Ciguatera Incidents By Island

Kauai, 152

Oahu, 286

Ciguatera Incidents By Island

Maui, 100

Molokai, 5

N = 676

Molokai, 5

Lanai, 2

Big Island, 131

Ciguatera Incidence By Island

Kauai, 342.3

Oahu, 35.6

Kauai, 342.3

�Per 1985 100,000 resident population

�Molokai and Lanai excluded

Ciguatera Incidence By Island

Maui, 129.7

N = 676

Oahu, 35.6

Big Island, 123.7

Fish Source for Ciguatera Incidents

Recreation, 558

Fish Source for Ciguatera Incidents

Market, 86

N = 676

Peddler, 16

Unknown, 6

Restaurant, 10

Catch Sites for Incident-Related FishMaui - 1963 to 2005

Related Fish

�57 incidents associated with associated with Maui catch sites

�53 with specific location

Catch Sites for Incident-Related FishOahu - 1963 to 2005

Related Fish

�127 incidents associated with associated with Oahu catch sites

�125 with specific location

Catch Sites for Incident-Related FishKauai - 1963 to 2005

Related Fish

�118 incidents associated with associated with Kauai catch sites

�113 with specific location

Catch Sites for Incident-Related FishBig Island - 1963 to 2005

Related Fish

�136 incidents associated with associated with Hawaii catch sites

�131 with specific location

Ciguatera IncidentsBy Type of Fish Consumed

Unknown

Oth

er

Mullet

Imported

Barracuda

Parrotfish

Goatfish

Surgeon Fish

Incidents involving consumption of >1 fish type were excluded

By Type of Fish Consumed

Snapper

Wrasse

MulletE

el

N = 635

Jack Fish

Grouper

Ciguatera Fish PoisoningTop 5 Offenders – Locally Caught Fish

1 21 2

Incident Jack Surgeon

Hospital Wrasse Jack

Locally Caught Fish

3 4 53 4 5

Grouper Snapper Wrasse

Snapper Grouper Surgeon

Jacks

Surgeon Fish

Grouper

Snappers

Wrasses

Interesting ResultsInteresting Results

Midway AtollMidway Atolln=57 39% hotn=57 39% hot

French Frigate ShoalsFrench Frigate Shoalsn=25 0% hotn=25 0% hotn=25 0% hotn=25 0% hot

Interesting ResultsInteresting Results

French Frigate ShoalsFrench Frigate Shoalsn=25 0% hotn=25 0% hot

http://www.noaanews.noaa.gov/stories2006/s2644.htm

n=25 0% hotn=25 0% hot

HawaiHawai!!iin=59 10% hot n=59 10% hot

UHM HOT FISHMHI

n = 112

CARNIVORES 15%

Summary of ResultsSummary of Results

N2a BioassayN2a Bioassay

CARNIVORES 15%

HERBIVORES 11%

ALL 13%

MHI n = 112

NWHIn = 182 TOTAL

15% 20% 18%

Summary of ResultsSummary of Results

N2a BioassayN2a Bioassay

15% 20% 18%

11% 17% 14%

13% 18% 16%

21.7

21.6

21.5

21.4

21.3

-158.2 -158.1 -158.0 -157.9 -157.8 -157.7 -157.6

1

5

20

100

510

100806040200

Percent Positive CTX21.0

20.9

20.8

20.7

20.6

Oahu

-158.2 -158.1 -158.0 -157.9 -157.8 -157.7 -157.6

20.2

20.0

19.8

19.6

19.4

19.2

19.0

-156.0 -155.6 -155.2 -154.8

1

5

20

100

510

100806040200

Percent Positive CTX

Hawaii

21.0

20.9

20.8

20.7

20.6

-156.6 -156.4 -156.2 -156.0 -155.8

1

5

20

100

510

100806040200

Percent Positive CTX

Maui

22.3

22.2

22.1

22.0

21.9

-159.8 -159.7 -159.6 -159.5 -159.4 -159.3 -159.2

1

5

20

100

510

100806040200

Percent Positive CTX

Kauai

Percent Ciguatoxic by Log

30

40

50

60

% C

igu

ato

xic

0

10

20

30

2.1 2.2 2.3 2.4 2.5 2.6 2.7

Log10Body Weight (g

% C

igu

ato

xic

Percent Ciguatoxic by Log10Body Weight (g)

2.8 2.9 3 3.1 3.2 3.3 3.4

Body Weight (g)

CTX Concentration vs Relative Position

log10

[CTX] (pg/mg) vs. RTP (‰)

2.0

RTP (‰)

4 6 8 10 12 14

log

10[C

TX

] (p

g/m

g)

-0.5

0.0

0.5

1.0

1.5

s Relative Trophic

[CTX] (pg/mg) vs. RTP (‰)

RTP (‰)

14 16 18 20 22

CTX Potency, Threshold & Links

CTX Human Threshold Concentration 0.1

Upcoming EU & USFDA Limit � 0.01ppb

BHAB Conference: New Zealand, October 2014

Link to Hawaii Research & Information

www.fish4science.com

CTX Potency, Threshold & Links

CTX Human Threshold Concentration 0.1 – 4 ppb

0.01ppb

BHAB Conference: New Zealand, October 2014

Hawaii Research & Information

Brain0.6

Liver1.5

Figure 1.1 Distribution of average CTX

Concentration (ng/g) in ten samples of C. argus

Muscle Tissue0.2

Gonads1.4

= 26.4 ng [CTX]26.4 ng [CTX]

Replacing less than 5% of serving of muscle with an equivalent weight of internal

tissues yields a 24% increase in CTX load

= 34.6 ng [CTX]34.6 ng [CTX]

of serving of muscle with an equivalent weight of internal

24% increase in CTX load

Gambierdiscus Transport via Ships’ Ballast WaterTest Conditions: 4 T’s 22.C-29.0°C, Darkness

Findings

• Survival & Growth Rates: Controls = Tests• Survival & Growth Rates: Controls = Tests

• No Gambierdiscus in Ballast Waters

• No Cyst Development

Conclusions

• Ballast Water Will Allow Oceanic Translocation of

• Current U.S. Protocols Prevent this Occurrence

Transport via Ships’

C, Darkness

Survival & Growth Rates: Controls = TestsSurvival & Growth Rates: Controls = Tests

Ballast Water Will Allow Oceanic Translocation of Gambierdiscus

Occurrence

Neurotoxin Prevalence Turtle Tissues• TESTED

• Tissues: Muscle & Liver

• 72 Samples, 38 individuals, 3 species

FOUND• 12 Samples (32%): Positive for Na+-Channel Neurotoxin

• Feeding Behavior � Grazing on Near

• 2 species: Green (10/29) > Hawksbill (2/4) > Olive Ridley (0/5)

• Livers (10/28) > Muscles (8/38) > Both (6/32)

• First Demonstration of Na+-Channel Neurotoxicity (CTX) in Marine Turtles

Neurotoxin Prevalence in Marine

3 species

Channel Neurotoxin Presence

Grazing on Near-shore Macroalgae

2 species: Green (10/29) > Hawksbill (2/4) > Olive Ridley (0/5)

Both (6/32)

Channel Neurotoxicity (CTX) in Marine Turtles

Neurotoxin Prevalence in Stranded Marine Cetaceans

• TESTED• Tissues: Muscle, Liver, Brain, Testes

• 89 Samples, 34 individuals, 13 species

FOUND• 14 Samples (16%):Positive for Na-Neurotoxin Presence

• Feeding Behavior � Grazing on Near

• 6 species

• Livers (7) > Muscles (4) > Brain (3) > Tests (0)

• PosiMve AssociaMon ≠ Causal Factor

Prevalence in Stranded Marine

89 Samples, 34 individuals, 13 species

Neurotoxin Presence

Grazing on Near-shore Fishes

Livers (7) > Muscles (4) > Brain (3) > Tests (0)

Ciguatera: Societal Impacts

Reduction in primary food source

Increased health-related costs

Revenue Loss of reef-fish sales to extent markets

Loss of tourismLoss of tourism

Depopulation via migration

• Rongo et al. (2009): Polynesian voyages of discovery

Societal changes in eating habits

Societal changes in family/festival activities

Ciguatera: Societal Impacts

fish sales to extent markets

et al. (2009): Polynesian voyages of discovery

Societal changes in family/festival activities

Ciguatera: Perspective with Climate Changes

Greater Geographic Range of Incidence

Probability for Higher Biomass of Toxin Producers

Greater Toxicity Quota from

Coming Good News: Technological Response from Science

Ciguatera: Perspective with Climate Changes

Greater Geographic Range of Incidence

Probability for Higher Biomass of Toxin Producers

Greater Toxicity Quota from Gambierdiscus Biomass

Coming Good News: Technological Response from Science

Overview of Research DesignOverview of Research Design