4/27/2012
CIGUATERA FISH POISONING:
at the intersection of human, animal, and
environmental health
Elizabeth Radke, MPH
University of Florida
Seminar in Contemporary Public Health Issues
March 19, 2012
bethradke@epi.ufl.edu
One Health Newsletter
• Quarterly newsletter distributed by the Florida Department
of Health and partners
• Designed to enhance the integration of animal, human,
and environmental health by demonstrating One Health in
practice
• To subscribe, email: OneHealth@doh.state.fl.us
Questions to Answer
• What is ciguatera fish poisoning?
• How does ciguatera fit into the One Health concept?
• How do environmental changes affect ciguatera incidence
and human health?
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Overview of CFP
• Foodborne illness acquired by eating reef fish containing
naturally occurring ciguatoxins produced by
Gambierdiscus dinoflagellates
Geographic Distribution
University of Maryland School of Medicine
Commonly toxic fish
• Barracuda
• Amberjack
• Red snapper
• Grouper
• Hine
• Moray eels
• Parrot fish
• King mackerel
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Public Health Significance
• Most commonly reported marine foodborne illness
• Estimated 50-500 thousand people affected each year
worldwide
• Substantial economic loss from lower fish exports, liability
concerns, missed work and medical cost
Gastrointestinal Symptoms
• Vomiting
• Diarrhea
• Abdominal pain
• Nausea
• Onset within 6-24 hours of eating
toxic fish
• Usually resolve spontaneously
within 1-4 days
Neurologic Symptoms
• Paresthesias in the extremities and oral
region
• Generalized pruritis
• Myalgia/Arthralgia
• Fatigue
• Reversal of hot/cold temperature
perception
• Neuropsychiatric (anxiety, depression,
memory loss)
• Onset within first few days of illness
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Other Symptoms
• Cardiac symptoms
• Hypotension
• Bradycardia
Illness Severity
• Varies dependent on locale and toxins present
• In Pacific: severe, more neuro, less GI
• In Caribbean: more GI, less neuro
• May vary base on other factors:
• Size and part of fish ingested
• Individual susceptibility
• Rarely fatal, but death may occur in severe cases due to
dehydration, cardiovascular shock during acute illness, or
respiratory failure
Chronicity
• Most cases will resolve on their own in days to weeks
• Some patients experience chronic symptoms that last
months or years
• Peripheral neurologic symptoms
• Neuropsychiatric symptoms
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4/27/2012
Recurrence
• Individuals who previously suffered from CFP seem to be
sensitized and more susceptible to future episodes
• Some patients experience recurrence of neurologic
symptoms after consuming alcohol, non-toxic fish, and
other foods such as nuts
Diagnosis
• No reliable biomarkers can confirm CFP in humans
• Diagnosis is based on:
• Characteristic symptoms
• History of having eaten reef fish
• Exclusion of other diagnoses that could account for
symptoms
• Ideal to confirm ciguatoxin in the consumed fish using
available laboratory methods
Treatment
• Primarily supportive and symptomatic
• Mannitol
• IV fluids
• Atropine for bradycardia
• Amitriptyline for paresthesias, pruritis, and headaches
• Fluoxetine for chronic fatigue
• Gabapentin for pain
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4/27/2012
Prevention
• Difficult because ciguatoxin is odorless and tasteless and
toxic fish cannot be identified by appearance or behavior
• Avoid high risk fish like large predatory reef fish
• Avoid eating viscera of reef fish
• Eating small portions of different fish may be safer than
eating larger portions of any individual fish
What environmental and other factors
i fl
influence
ciguatera
i
t
iincidence?
id
?
Changes in Ciguatera Incidence
• In the South Pacific, reported cases rose from 1 per 1000
in 1973-1983 to 2 per 1000 in 1998 to 2008
Lewis 1993 Mar Fish Rev.; Skinner 2011 PLoS NTD
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Changes in Ciguatera Incidence
• In the same studies, some areas experienced declines
• French Polynesia
• 5 per 1000 in 1973-1983
• 4 per 1000 in 1992-2001
• 3 per 1000 in 1998-2008
• 2 per 1000 in 2000-2008
• Changes in incidence could be due to changes in diet,
toxin variability, environmental changes, or other factors
Why has incidence increased in
some areas and decreased in
others?
th ?
Gambierdiscus and seawater temperature
• Growth rates of
Gambierdiscus tend to
be highest from 29-30°C
(84.2-86°F)
• With seawater
temperatures (SWT)
rising, could suggest that
ciguatera incidence will
increase and the range
will expand
Tester 2010 Toxicon
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Ciguatera and SWT in South Pacific
• Hales, et al. used public
health data on ciguatera for
22 Pacific islands from 1973
to 1994
• On islands that experience
warming during El Nino
events, there was an
increase in ciguatera cases
Ciguatera and SWT in South Pacific
• Chateau-Degat et al. found a
significant association
between SWT and
Gambierdiscus abundance
with 13 and 17 month lag
• Increase in Gambierdiscus
abundance followed by
increase in ciguatera cases,
with a 3 month lag
Chateau-Degat 2005 Harmful Algae
Ciguatera and SWT in South Pacific
• Llewellyn found that high ciguatera incidence was most
likely in areas with seawater temperature above 28-29°C
82.4-84.2°F)
• Suggested might also be an upper temperature threshold
above which ciguatera incidence would be limited
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4/27/2012
Ciguatera and SWT in South Pacific
Llewellyn 2010 Toxicon
Ciguatera and SWT in the Caribbean
Tester 2010 Toxicon
Ciguatera and SWT in the Caribbean
• The number of days with sea
surface temperatures higher than
29°C has nearly doubled from 42
to 81, in the last three decades in
the southern Gulf of Mexico
• Rising temperatures may sustain
maximum growth of
Gambierdiscus species
Tester 2010 Toxicon
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Mechanisms for link with SWT
• Increased growth rate of Gambierdiscus
• Increased toxin production by Gambierdiscus
• Coral bleaching
• Storms
Coral reef health and ciguatera
• Reef disturbances are reported to be
temporally associated with ciguatera
outbreaks
• Natural disturbances
• Storms (hurricanes, cyclones)
• Man-made disturbances
• Dredging channels
• Ships anchoring
• Nuclear test explosions
• Other human impact
Coral reef health and ciguatera
• When coral reefs are disturbed, Gambierdiscus has the
opportunity to re-colonize the newly bare sections of reef
• Bare substrate hypothesis
• Petroleum platforms have acted as substrate
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4/27/2012
Other environmental influences
• Salinity
• Light
• Waves
• Nutrient levels
Fish health and ciguatera
• Possible lethal effects of ciguatoxin with high doses
• Otherwise, fish seem to be unaffected
• Changes in fish population can influence ciguatera
• Fewer large
large, older individuals
Ciguatera and One Health
Environmental
Health
(temperature,
coral reef health,
ecosystem)
Animal Health
(fish)
Human Health
(ciguatera
illness)
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4/27/2012
Expectations for St. Thomas, USVI
• Since seawater temperatures are increasing and coral
reef health is decreasing, we would expect ciguatera
incidence to increase
• Currently performing a large, multi-institute study to better
understand and predict ciguatera in St. Thomas
Project CaribCATCH
Incidence–St. Thomas
• Telephone surveys in 2010 and 2011
• Random digit dialing
• Asked about demographics, recent fish consumption,
history of ciguatera episodes, ciguatera awareness
• 807 participants
• 23% had ever had ciguatera
• 30% visited the emergency room for most recent episode
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Incidence–St. Thomas
• Emergency room visits obtained from medical record
review and past research
• 1971-79, 1995-2011
Ciguatera incidence estimates among adults
in St. Thomas (per 1000 population)
Data source
1980
2011
Emergency room visits*
18
6
Current survey vs. Morris et al. 1982
(age adjusted to nearest Census)
14
12
Current survey vs. Morris et al. 1982
(age adjusted to 1980 survey)
14
8
Current survey vs. McMillan et al. 1980
22% of
11% of
households households
*Averaged over 3 years, calculated by dividing the incidence of ER visits by the proportion of
survey participants who visited the ER for their most recent ciguatera illness. Assumes 50% of ill
individuals visited ER in 1971-71 and 30% visited ER in 2010-11 based on respective surveys.
Ciguatera and SWT in St. Thomas
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4/27/2012
Correlation between annual average SST and incidence
of ciguatera ER visits with a one year lag, 1971-2011*
Ciguatera inciden
nce per 1000
8
7
R² = 0.4939
6
5
4
3
2
1
0
26.8
27.3
27.8
28.3
Sea surface temperature (°C)
*Data from 1971-1979, 1995-1999, 2002-2005, 2007-2011
Ciguatera incide
ence per 1000
Correlation between SST and ciguatera ER visits with
two year lag, 2002-2011
2
1.8
R² = 0.4114
1.6
1.4
1.2
1
0.8
0.6
0.4
0.2
0
27.4
27.6
27.8
28
28.2
Sea surface temperature (°C)
Environmental Monitoring
• Four monitoring sites surveyed by the USVI Territorial
Coral Reef Monitoring program
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4/27/2012
Sampling
• Environmental parameters (seawater temperature,
salinity, precipitation, wind speed)
• Coral species composition/health
• Macroalgal cover/composition
• Nutrients
• Gambierdiscus abundance and species diversity
• Toxicity of dinoflagellate field samples and fish
Gambierdiscus isolated via micropipetting to
establish clonal cultures for genetic analyses
(LSU rRNA gene sequencing), toxin profiling,
and physiological studies
Microscopic and
molecular analyses
• Algal Sampling: Dictyota spp.
Gambierdiscus spp.
Gambierdiscus spp. growth vs. temperature (in progress)
Grow
wth (division day-1)
0.6
0.6
G. caribaeus
0.4
0.4
0.2
0.2
0
G. belizeanus
0
10
15
20
25
0.6 G
G. cf.
cf carolinianus
30
35
40
10
0.6
0.4
0.4
0.2
0.2
0
10
15
20
25
30
35
15
20
25
30
35
40
25
30
35
40
G sp.
G.
sp ribotype 1
0
10
40
Temperature (°C)
15
20
• Maximum growth at 27 -30°C, isolates well-adapted to temperature conditions in the USVI
• Temperatures above 30 °C strongly inhibit growth of all species; may pose an upper and
limiting threshold to the effects of rising seawater temperature.
15
4/27/2012
Gambierdiscus spp. abundance, Benner Bay
500
450
30
Max temp: 30.1 (Aug 10)
Min temp: 25.9 (Mar 11)
29
400
Cells g-1 Dictyota
C
28
300
250
27
200
26
150
100
SW temperature (°°C)
350
25
50
0
24
2008
2009
2010
2011
SW temp
Gambierdiscus spp. abundance positively correlated with SW temperature, ave precipitation,
NH4+; negatively correlated with ave wind velocity (Spearman’s rank correlation, p<0.05)
Gambierdiscus spp. abundance, Seahorse
30
Max temp: 29.7 (Aug 10)
Min temp: 25.8 (Mar 11)
500
29
400
28
300
27
200
26
100
25
0
24
2008
2009
2010
2011
SW temperature ((°C)
Ce
ells g-1 Dictyota
600
SW temp
Gambierdisus spp. abundance positively correlated with SW temperature
Gambierdiscus spp. abundance, Black Point
450
30
Max temp: 29.9 (Aug 10)
Min temp: 25.8 (Feb 08)
400
29
350
Cells g-1 Dictyota
28
250
27
200
150
26
SW temperature
e (°C)
300
100
25
50
0
24
2007
2008
2009
2010
2011
SW temp
Gambierdisus spp. abundance positively correlated with SW temperature, ave precipitation;
negatively correlated with PO43- and ave wind velocity (Spearman’s rank correlation, p<0.05)
16
4/27/2012
Gambierdiscus spp. abundance, Flat Cay
Max temp: 29.7 (Aug 10)
Min temp: 25.8 (Mar 11)
30
250
29
200
28
150
27
100
26
50
25
0
24
2007
2008
2009
2010
2011
SW temperature
e (°C)
Ce
ells g-1 Dictyota
300
SW temp
Gambierdisus spp. abundance positively correlated with SW temperature (Spearman’s rank correlation, p<0.05)
Coral reef health in the St. Thomas
40
dead coral
35
live coral
30
25
20
15
10
5
0
2003 2004 2005 2006 2007 2008 2009 2010 2011
St. Thomas Summary
• Incidence has not increased as expected based on
temperature and coral reef health
• More complicated picture
• What are some possible explanations for this?
• Upper temperature threshold
• Changes in behavior
• Fish consumption
• Fewer high risk individuals (low SES, born in Caribbean)
• Ciguatera avoidance
• Change in fish population
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4/27/2012
Other Research Activities in St. Thomas
• Epidemiology
• Individual level risk factors
• Clinical research
• Enrolling patients from ER and community with follow
up at 3 and 12 month
• Toxin studies
• Optimizing detection of toxin in fish
• Identifying methods for diagnosing disease in patients
Acknowledgements
Project CaribCATCH
UVI:
Tyler Smith
UMB:
Lynn Grattan
Sparkle Roberts
UF:
J. Glenn Morris
FDA GCSL:
Alison Robertson
Robert Dickey
WHOI:
Don Anderson
Mindy Richlin
Funding
18