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Chemosphere 164 (2016) 462e468

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Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere

Assessment of sh consumption and mercury exposure among


pregnant women in Jamaica and Trinidad & Tobago
Phylicia Ricketts a, *, Niladri Basu b, Horace Fletcher c, Mitko Voutchkov a, Bharat Bassaw d
a
Faculty of Science & Technology, The University of the West Indies, Mona, Kingston 7, Jamaica
b
Faculty of Agricultural and Environmental Sciences, McGill University, Montreal, Quebec, Canada
c
Faculty of Medical Sciences, The University of the West Indies, Mona, Kingston 7, Jamaica
d
Faculty of Medical Sciences, The University of the West Indies, St. Augustine, Trinidad and Tobago

h i g h l i g h t s

 The preference of maternal sh intake is dependent on the country's captured sh production.


 Pregnant women in the Caribbean are susceptible to mercury exposure from sh intake.
 Consumers of large ocean pelagic sh have higher placental mercury concentrations.
 Consumers of small pelagic and reef nsh have lower placental mercury concentrations.

a r t i c l e i n f o a b s t r a c t

Article history: Background: Fish is an essential and traditional element in the diet of most Caribbean people. However it
Received 10 May 2016 also contains methylmercury which can have severe effects on fetal neurodevelopment. The objective of
Received in revised form this study was to assess the sh intake of a selected group of pregnant women from Jamaica and Trinidad
8 August 2016
& Tobago and evaluate prenatal mercury exposure, using the placenta as a biomarker.
Accepted 10 August 2016
Available online 7 September 2016
Method: Food frequency questionnaires and placental samples were obtained from participating par-
turients at the time of delivery at the University Hospital of the West Indies in Kingston, Jamaica
Handling Editor: Keith Maruya (N 100, from November 2012 to March 2013) and the Mt Hope Women's hospital in St Joseph, Trinidad
& Tobago (N 30, in June 2015). The participants were asked to identify the species of sh and the
Keywords: frequency of consumption. Placental samples were analysed for mercury using cold vapour atomic
Mercury absorption.
Exposure assessment Results: The sh consumption preferences for pregnant women, varies based on the marine sh catch
Biomarkers production of each country. The main sh species that contributed to the highest estimated methyl-
Placenta
mercury exposure in Jamaica and Trinidad & Tobago were cod and shark, respectively. There was a weak
Fish consumption
association between maternal sh intake and placental mercury concentrations. The mean placental
Caribbean
mercury concentrations in Jamaica and Trinidad & Tobago were 0.74 0.5 mg/kg and 1.46 0.6 mg/kg,
wet weight respectively.
Conclusion: The results from this study showed an inuence of Caribbean sh intake preferences on
mercury exposure and thus a recommendation for continuous bio-monitoring for public health purposes.
2016 Elsevier Ltd. All rights reserved.

1. Introduction of livelihood in the Caribbean community (CARICOM). The overall


consumption of sh per person in Caribbean countries is about
Fish is a traditional and essential element in the diet of most 31 kg/yr (Masters, 2012). This is well above the global average per
Caribbean people. The shing industry is also an important source person of 16.4 kg/yr in 2006 (Secretariat, 2016). The sh con-
sumption per person in some Caribbean countries, could be as high
as 69 kg/yr and 66 kg/yr in Antigua & Barbuda and Anguilla,
respectively (Masters, 2012). Fish is critical for a healthy diet. It
* Corresponding author. Present address: Department of Physics, The University
of the West Indies, Mona, Kingston 7, Jamaica. contains omega 3 fatty acids and vitamins D and B12, which are
E-mail address: phylicia.ricketts@mymona.uwi.edu (P. Ricketts). important for brain development and reducing the risk of heart

http://dx.doi.org/10.1016/j.chemosphere.2016.08.054
0045-6535/ 2016 Elsevier Ltd. All rights reserved.
P. Ricketts et al. / Chemosphere 164 (2016) 462e468 463

attacks (Washington State Department of Health, 2016). However, Trinidad & Tobago (N 30). In both sites participants were
there has been heightened concern about the presence of toxic recruited via convenience sampling. The sample collection was
methylmercury in sh (American Heart Association, 2015). Fish carried out during November 2012eApril 2013 and June 2015,
consumption was shown to be a major contributor to daily meth- respectively. Informed consent was obtained from each participant.
ylmercury intake for coastal populations (Cheng et al., 2013). The female population of child bearing age (18e44 years) for Ja-
Mercury exposure is of global concern in pregnant women maica and Trinidad & Tobago were approximately 591,567 and
because of placental transfer to the fetus (Karagas et al., 2012). The 264,424 respectively (Statistical Institute of Jamaica, 2014; Central
usual biomarkers for determining prenatal exposure to mercury are Statistical Ofce, 2015). Each tertiary teaching hospital institution
maternal hair, maternal blood and cord blood (Sakamoto et al., is situated in the capital cities for both countries. There was no
2007). While these have some value, there are noteworthy limita- known occupational exposure to mercury among the participants.
tions. For example, mercury concentrations in maternal blood and Both countries have different sh consumption preferences due to
hair may vary over different periods of pregnancy, and the rela- their sheries sector mechanism.
tionship between mercury in cord blood and maternal blood can
uctuate (Basu et al., 2014). Some of these limitations may be
2.2. Fish intake
overcome by studying the placenta, which integrates fetal exposure
for almost 36 weeks. In addition, the placenta is considered a non-
Food frequency questionnaires were administered to partici-
invasive, real time monitoring specimen that can reveal both
pating parturients at the time of delivery. The frequency of sh
maternal and fetal exposure to elements (Iyengar and Rapp, 2001).
consumption and the approximate amount of sh intake, using a
Therefore the mercury concentrations in placenta could be a suit-
Food Frequency Questionnaires (FFQ) similar to ones used previ-
able biomarker, though few studies have examined maternal sh
ously (Bjornberg et al., 2005; Goodrich et al., 2016). In the current
consumption and placental mercury concentrations (Ask et al.,
study, the participants were asked questions on 12 sh and 4
2002; Bjornberg et al., 2005; Hsu et al., 2007).
canned sh known to be commonly consumed in both countries.
Research on mercury exposure in the Caribbean is increasing. In
They were also given an option to suggest other types of sh not
a previous Caribbean study, the most common sh species
included in the list. Participants completed surveys detailing their
consumed in Barbados was ying sh, marlin and tuna. It was
sh consumption patterns within the last 3 months. The intake
found that hair mercury concentrations for Barbadians signicantly
options included never, once/month, 2e3 times per month, once/
increased when participants consumed high risk sh (such as tuna
week, 2e3 times per week, 4 or more times per week. Participants
and marlin) (Drescher et al., 2014). Another study found that
also reported consumption frequency, portion size and species.
mercury concentrations in the blood of pregnant women in the
Caribbean were two times higher when compared to Canada and
the US. This was primarily due to the frequency and sh species 2.3. Methylmercury intake
preference of Caribbean people. The study also showed that blood
mercury concentrations vary across each island (Forde et al., 2014). The mean mercury concentrations in sh were obtained from a
The purpose of the study was twofold: A) to characterize the sh compilation of the literature in Table 1. The mercury concentration
consumption patterns of a selected group of pregnant women from in some Jamaican sh was obtained from a preliminary seafood
Kingston in Jamaica and St. Joseph in Trinidad & Tobago, and B) to assessment (Fletcher et al., 2005). The mercury concentration of the
increase understanding of prenatal mercury exposure by charac- remaining varieties of sh was obtained from a large database
terizing mercury levels in the placenta. The outcomes of this study maintained by the U.S. Food and Drug Administration (Karimi et al.,
are expected to increase understanding of sh consumption in the 2012). The estimated methylmercury ingested dose was calculated
Caribbean region along with associated concerns of mercury based on daily sh intake, the mercury concentration in each
exposure, and together such research is needed for the purposes of species and body weight. The mean body weight for participants
public health but also to help countries meet obligations associated was 77 kg.
with the UN Minamata Convention on Mercury Pollution (Gustin The basic equation to estimate methylmercury intake per body
weight (mg/kg/d) is (World Health Organization, 2008):

   
g mg
Amount of fish ingested d
* Hg concentration in the ingested fish g

Body weight kg

et al., 2016). 2.4. Mercury analysis

Approximately a quarter of the at part of the placenta from the


2. Materials and methods
region of the umbilical cord was severed with a surgical blade. It
was then placed in a sealed plastic bag and stored in a freezer
2.1. Participants
at 18  C. The samples were dried in the drying oven (Memmert,
Schwabach, Germany) at 60  C. The oven was set to maintain a
Ethical approval was granted from the ethics committee of the
constant temperature for approximately 96 h. The sample was
Faculty of Medical Sciences at The University of the West Indies
removed from the oven and weighed intermittently every 30 min
Mona and St. Augustine campuses. Placental samples were
until a constant dry weigh was obtained. Mercury levels were
collected and dietary surveys administered to participants at the
measured following United States Environmental Protection
University Hospital of the West Indies in Kingston, Jamaica
Agency (US EPA) method 245.6 using the 400 A mercury analyzer.
(N 100) and the Mt. Hope Women's hospital in St. Joseph,
464 P. Ricketts et al. / Chemosphere 164 (2016) 462e468

Table 1
Mercury concentrations (mg/g) in selected sh species and reported maternal sh consumption patterns by study participants from Kingston, Jamaica and St. Joseph in Trinidad,
as determined through self-reported surveys at the time of pregnancy.

Common name Scientic name Hg concentration/mg/g Fish consumption pattern (median)

Kingston St. Joseph

Shark Carcharhinus 1.77 none 1/mth


Kingsh Scomberomorus cavalla 0.64b none 2e3/mth
Carite Scomberomorus 0.39 none 1/mth
White grunt Haemulon plumieri 0.38 1/mth none
Tuna-Bluen (canned) Thunnus thynnus 0.29 2e3/mth 1/week
Yellowtail snapper e 0.19 2e3/mth none
Sea Trout Cynoscion regalis 0.17b 2e3/mth 2e3/mth
Tuna-Albacore (fresh) T Alalunga 0.17 none 1/mth
Cod Gadus morhua 0.10 2e3/mth 2e3/mth
Other 0.10 1/mth 1/mth
Shad Alosa aestivalis 0.09 1/mth none
Croaker Micropogonias furnieri 0.07 none 1/week
Redtail snapper Lutjanus campechanus 0.05b 2e3/mth 1/week
Tilapia Oreochromis niloticus 0.05 2e3/mth none
Mackerel-jack (canned) Trachurus murphyi 0.05 2e3/mth 2e3/mth
Salmon-Pink (canned) Oncorhynchus gorbuscha 0.04 2e3/mth 1/mth
Herring-Atlantic Clupea harengus 0.03 1/mth none
Sardines (canned) Sardina pilchardus 0.02 1/week 2e3/week

Source: (Karimi et al., 2012), b(Fletcher et al., 2005).

About 0.3 g of dried placental tissue sample was placed in a three months of pregnancy. Cod was the most popular sh species
biochemical oxygen demand (BOD) bottle with 8 ml of concen- consumed among participants from Kingston (n 57%), while
trated sulfuric acid and 2 ml of concentrated nitric acid. The BOD shark was the most popular consumed sh species among par-
bottle was placed in a water bath maintained at 80  C until the ticipants from St. Joseph (n 37%) (Fig. 1). The most common sh
tissue completely dissolved (approximately 30 min). The sample consumed by participants sampled from each site were cod, red-
was cooled and 15 ml of potassium permanganate and 8 ml of tail snapper, sardines (canned), mackerel (canned) and tuna
potassium persulfate solutions were added and returned to the (canned). The least consumed sh consumed by participants
water bath and digested for an additional 90 min at 30  C. The sampled from each site was salmon (canned). The following sh
digested sample was diluted with 55 ml of reagent water and 6 ml species were classied as other by a few participants: sea bass
of sodium chloride-hydroxylamine sulfate solution was added to (Atractoscion nobilis), doctor sh (Acanthurus chirurgus), mullet
reduce the excess permanganate. Then 5 ml of stannous chloride (Mugil cephalus), Croaker- Atlantic (Micropogonias undulates) and
solution was added. A batch of 12 samples was measured daily over grouper (Myctoperca tigris). The frequency of consumption also
a 6 weeks period. Each sample was measured once, with blanks differed. In participants from Kingston, the most popular sh was
repeated twice and certied reference material measured after consumed 2e3 times per month (Table 1), while in St. Joseph the
every batch. The certied reference material used was IAEA 407 most popular sh was consumed once per month (Table 1). The
(Fish homogenate). An instrument calibration curve was estab- total daily sh intake per person (g/day) was higher in participants
lished by plotting standard concentrations against instrument from Kingston (38.5 g/day) than in St. Joseph (20.9 g/day)
reading absorbance. A regression statistics, R2 0.998 was calcu- (Table 2).
lated. The level of detection (LOD) for mercury in placenta was
0.5 mg/kg. The average recovery of the reference material was found
to be 77e80%. 3.2. Methylmercury ingested dose

2.5. Statistical analysis There were weak associations between maternal sh intake
and placental mercury concentrations for the study participants in
All data analysis was performed using Windows SPSS version 19. Kingston and St. Joseph. There was also a weak association be-
The data was not normally distributed. Descriptive statistics were tween meHg ingested dose and placental mercury concentrations
examined for each variable. Estimated sh consumption was for Kingston and St. Joseph. The average methylmercury ingested
normalized to daily intake. Initial assessment of residual and dose was calculated as 0.07 mg/kg/d, body weight and 0.15 mg/kg/d,
normal probability plots were used to identify outliers. The outliers body weight for participants in Kingston and St. Joseph,
were removed from the subsequent analyses. Linear regression respectively.
analysis (multiple R) was used to determine the relationship be- Since methylmercury exposure is primarily from sh intake, we
tween maternal daily sh intakes and placental mercury concen- used Groth's methodology (Groth, 2010) to rank the total methyl-
trations. There were about 48% of sample concentrations that were mercury exposure based on sh preferences in each location. The
found to be below the method detection limit (MDL), these were sum of methylmercury ingested dose by each participant was used
classied as non-detects. The Kaplan-Meier approach was used to to determine the sh species that contributed to the overall
confront these non-detects. methylmercury exposure in the population. The main sh species
that contributed to overall methylmercury exposure in participants
3. Results from Kingston (Table 3) was cod (25%). While the main sh species
that contributed to overall methylmercury exposure in participants
3.1. Questionnaire data from St. Joseph (Table 3) was shark (51%). Salmon (canned) and
Sardines (canned) contributed to the least methylmercury expo-
All the participants reported to have eaten sh within the last sure in the participants' diet.
P. Ricketts et al. / Chemosphere 164 (2016) 462e468 465

Fig. 1. Most popular sh consumed by study participants from Kingston, Jamaica and St. Joseph in Trinidad, as determined through self-reported surveys at the time of pregnancy.

Table 2
Mean placental mercury concentrations, ingested dose and sh intake for participants in Kingston and St. Joseph.

Kingston St. Joseph

Mean SD Range Mean SD Range

Maternal Age (yrs) 29 6 19e48 26 5 17e42


Total sh intake per person/day (g) 38.5 43.4 2.0e151.0 20.9 21.8 3e42.5
MeHg ingested dose (mg/kg/day, bw) 0.07 0.09 0.001e0.64 0.15 0.22 0.01e0.94
Placental mercury concentration (mg/kg) ww 0.74 0.4 0.3e1.5 1.46 0.6 0.3e2.5

Table 3 given in Table 2. The mean placental mercury concentrations in


Evaluation of sh species and their fractional contribution to the overall methyl-
participants from St. Joseph (1.46 0.6 mg/kg) were found to be
mercury exposure to the sample population in Kingston and St. Joseph.
higher than in participants in Kingston (0.74 0.4 mg/kg). Fig. 2aeb
Common name Kingston St. Joseph showed that placental mercury concentrations in both groups were
Shark 0% 51% not evenly distributed. In the Kingston group placental mercury
Kingsh 0% 17% concentrations were skewed to the left, which may be due to the
Carite 0% 12% 48% of non-detects recorded (i.e. their concentrations were below
White grunt 9% 1%
Tuna-Bluen (canned) 18% 2%
0.5 mg/kg). All the placental mercury concentrations in St. Joseph
Yellowtail snapper 12% 0% group were above the method detection limit and fairly distributed
Sea Trout 2% 1% about the mean value. The 5% of participants in St. Joseph with the
Tuna-Albacore (fresh) 0% 3% highest placental mercury concentrations reported to eat shark,
Cod 25% 4%
cod, tuna, Carite, croaker at least once per month. The 5% of
Other 7% 3%
Shad 5% 0% participants from Kingston group, with the highest placental mer-
Croaker 0% 3% cury concentrations reported to eat cod and snapper at least once
Redtail snapper 6% 1% per month.
Tilapia 1% 0%
Mackerel-jack (canned) 9% 1%
Salmon-Pink (canned) 1% 0% 4. Discussion
Herring-Atlantic 1% 0%
Sardines (canned) 5% 0% 4.1. Caribbean sheries

The range for sh consumption per person is from 3 to 69 kg/yr.


3.3. Placental mercury biomarker data The average sh consumption per person in Jamaica was 16 kg/yr
and for Trinidad & Tobago it was 15 kg/yr (Masters, 2012). The sh
The mercury concentrations in placenta for both countries are consumption per person from the Kingston group may be calculated
466 P. Ricketts et al. / Chemosphere 164 (2016) 462e468

Fig. 2. a. Distribution of total mercury concentration (mg/kg) wet weight in placenta collected from participants in Kingston, Jamaica. b. Distribution of total mercury concentration
(mg/kg) wet weight in placenta collected from participants in St. Joseph, Trinidad.

as 14 kg/yr while in St. Joseph group, it would be calculated as consumption from participants in Kingston was 2e3 times per
7.6 kg/yr. The selected participants in St. Joseph group may not be an month and in St. Joseph it was found to be once per month. A
accurate representative of the population. The questionnaire data similar target group in Puerto Rico reported average maternal sh
showed that the study participants from Kingston (Jamaica) mainly consumption of 1e2 times per month (Ortiz-Roque and Lopez-
consumed reef nsh while those from St. Joseph (Trinidad & Rivera, 2004). The sh consumption of women of child bearing
Tobago) consumed large ocean pelagic sh. Studies have shown that age in Martin County, Florida was also found to be 1e2 times per
a sh's length inuences its mercury concentration (Jewett et al., month (Nair et al., 2014). This indicates that the frequency of
2003; Gewurtz et al., 2011). Therefore exposure assessment of the maternal sh consumption is different in each country.
two groups was necessary. The sheries report in 2009, showed Although the total maternal sh intake per day for participants
where the large pelagic capture sh production in Trinidad & in St. Joseph was lower than those in Kingston, the estimated
Tobago was 5643 metric tonnes and none was captured in Jamaica. methylmercury ingested dose was calculated to be higher. This may
Meanwhile, the shallow reef nsh capture productions were be due to the type of sh consumed. Monte Carlos simulations done
12,500 and 52 metric tonnes, respectively for Jamaica and Trinidad by Chien et al. showed that mercury concentrations in sh can
& Tobago (Masters, 2012). This is an indication that sh available for contribute up to 72% of daily mercury exposure dose (Chien et al.,
consumption was primarily based on the country's yearly sh 2007). Based on mercury exposure assessment of both groups in
capture production. The Captured sheries sector is divided into this study, it was found that the participants who eat shark calcu-
marine, estuarine and riverine sheries (Kong, 2004). Countries lated the highest methylmercury ingested dose (~0.17 mg/kg/d,
such as Trinidad & Tobago have few river, streams or lakes, suitable body weight). Hence, there is a recommendation to develop sh
for freshwater sheries system. Therefore the types of sh available consumption advisories for populations that have continuous
for consumption are mainly from ocean and sea (i.e. marine envi- abundance of various sh species. Risk communications should also
ronment). Meanwhile, sh available for consumption in countries be improve so that pregnant women can choose to eat sh that
such as Jamaica, are both from inland freshwater systems and ma- have low mercury concentration (Groth, 2010).
rine environment (Masters, 2012). It is projected to be an increase in Pregnant women are advised to reduce consumption of
marine sh production in the Caribbean, therefore the health carnivorous or predatory sh due to health risk of mercury expo-
benets and risk for sh consumption should be a concern for the sure (Shao et al., 2011). The authors of a case study in Trinidad &
Region (Forde et al., 2014). There are many studies assessing dietary Tobago showed that consumers of sh only diets, consisting mainly
sh intake and mercury exposure (Mahaffey et al., 2009; Wolkin of shark and tuna, recorded elevated blood mercury levels up to
et al., 2012; Cheng et al., 2013). This dietary assessment method- 26.3 mg/L. Those authors also recommended the need to monitor
ology can be extended to other Caribbean Regional Fisheries sh consumption and mercury levels in Trinidad & Tobago due to
Mechanism member countries by adjusting the type of sh avail- the high availability of shark and tuna (Pinto Pereira and
able for consumption in each country. There is a concern for other Teelucksingh, 2009).
Caribbean countries that consume sh more frequently and/or sh
containing high levels of mercury. 4.3. Placental mercury concentration

4.2. Methylmercury exposure In this present study, the mean placental total mercury con-
centration was higher for the participants in St. Joseph
Results from survey responses showed that the median total sh (1.46 0.6 mg/kg) than those in Kingston (0.74 0.5 mg/kg). There
P. Ricketts et al. / Chemosphere 164 (2016) 462e468 467

are limited published results of placental mercury concentrations recognized this by adopting the UN Minamata Convention on
in the Caribbean. However, these concentrations were still lower Mercury Pollution which ultimately aims to protect human and
than those reported in Taiwan (19 1.8 mg/kg) and Sweden ecosystem health from mercury (UNEP, 2013; Gustin et al., 2016).
(median 1.8 mg/kg). Previous studies have also shown where the
placental mercury concentrations increases with an increase in Acknowledgements
maternal sh consumption (Ask et al., 2002; Hsu et al., 2007). The
present study showed that there was a weak association between This research project was funded by a Research and Publication
placental mercury concentrations and maternal sh intake. How- award granted by the Ofce of Graduate Studies and Research at the
ever, the study in Hawaii that showed signicant difference in University of the West Indies, Mona.
placental mercury concentrations between those participants who Collaboration with McGill University was made possible by
did not eat sh verses those who ate sh, also concluded that there funding from the Government of Canada, under the Canada- CAR-
was no close correlation with sh intake and placental mercury ICOM leadership scholarship programme. Mercury analyses were
levels (Gilman et al., 2015). funded by a National Sciences and Engineering Research Council
(NSERC) Canada Discovery Grant and Canada Research Chair (CRC)
4.4. Limitations to Niladri Basu.
Ethical approval was granted by the Ethics Committee of the
While the current study increases knowledge in a number of Faculty of Medical Sciences at the University of the West Indies,
areas and provides some initial data for which future studies can be Mona and St. Augustine campuses.
designed, there are some limitations worth mentioning. The sam-
ple size was not representative of the general pregnant women
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