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Food Additives & Contaminants: Part A
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Balancing the risks and the benefits of local fish consumption in Bermuda
É. Dewailly ab; P. Rouja c; R. Dallaire a; D. Pereg a; T. Tucker d; J. Ward c; J. P. Weber b; J. S. Maguire a; P. Julien a a Public Health Research Unit, Laval University Research Centre-CHUL-CHUQ, Québec, Canada b Institut National de Santé Publique du Québec, Québec, Canada c Department of Conservation Services, Government of Bermuda, Bermuda d Bermuda Underwater Exploration Institute, Bermuda
First Published on: 25 September 2008
To cite this Article Dewailly, É., Rouja, P., Dallaire, R., Pereg, D., Tucker, T., Ward, J., Weber, J. P., Maguire, J. S. and Julien, P.(2008)'Balancing the risks and the benefits of local fish consumption in Bermuda',Food Additives & Contaminants: Part A,
To link to this Article: DOI: 10.1080/02652030802175285
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Food Additives and Contaminants
2008, 1–11, iFirst
Balancing the risks and the benefits of local fish consumption in Bermuda
- b
- a
- a
- c
- b
- d
E. Dewaillyad , P. Rouja , R. Dallaire , D. Pereg , T. Tucker , J. Ward , J.P. Weber ,
*
J.S. Maguirea and P. Juliena
a
- ´
- Public Health Research Unit, Laval University Research Centre-CHUL-CHUQ, Quebec, Canada;
bDepartment of Conservation Services, Government of Bermuda, Bermuda; Bermuda Underwater Exploration Institute,
cd
- Bermuda; Institut National de Sante Publique du Quebec, Quebec, Canada
- ´
- ´
- ´
(Received 14 February 2008; final version received 1 May 2008)
Fish consumption today is widely recognized as highly beneficial since it constitutes a good source of several essential nutrients, such as selenium and polyunsaturated fatty acids (n-3 PUFA). However, fish can also contain contaminants such as mercury, which make the consumer, especially pregnant women, confused about the risk–benefit balance associated with fish consumption. This is particularly true for tropical fish species for which little information is available. We have previously reported that some Bermudian neonates had elevated mercury in their umbilical blood compared with international guidelines. The objective of this study was to give precise and balanced information on the content of mercury, selenium and PUFA in the most consumed fish species in Bermuda. In 2003 and 2006, a total of 307 fish were collected from 43 fish species and 351 samples were analysed (305 flesh samples, 44 liver samples, one roe and one fat sample) by inductively coupled plasma-mass spectrometry (ICP-MS) (metals) and high-resolution gas chromatography (HRGC) (fatty acids). Results show that mercury varies among species from 0.03 to 3.3 mg gÀ1 and that it is possible for at-risk groups such as pregnant women to make informed choices concerning fish consumption, e.g. maximizing fish species rich in nutrients and low in mercury.
Keywords: fish consumption; tropical; mercury; selenium; omega-3
Introduction
Despite the fact that n-3 fatty acids can be found in other foods, fish remains the best and richest source of these nutrients and hence is an important part of a healthy diet. Coastal populations have a generally high intake of long-chain PUFAs, the most important compounds being eicosapentanoic acid (EPA) and docosahexanoic acid (DHA). During pregnancy, fish consumption provides DHA to the mother and the foetus, which is critical in brain and retina development (Lauritzen et al. 2004; Hibbeln et al. 2007). In addition, fish and seafood are a very good natural source of selenium (Svensson et al. 1992; Leung et al. 2007). Concentrations of this element in foods depend on the local geological composition. It has been proposed that selenium may exert an antagonistic effect on mercury (Hg) toxicity (World Health Organization (WHO) 1990) and have a mediating effect on certain cancers, specifically prostate cancer.
On the other hand, fish may also contain varying amount of contaminants such as Hg, most of which occurs in the form of methylmercury (MeHg) (over 90%). This phenomenon occurs because fish feed on aquatic organisms that contain MeHg originating from biomethylation of inorganic Hg by microorganisms.
Fish is one of the last remaining ‘wild foods’ in the diets of Bermuda residents and represents not only a rich source of several unique dietary nutrients, but also forms an important part of Bermuda’s cultural identity as an island nation. Highlighting the benefits and minimizing the risks from seafood consumption is an important part of maintaining this resource’s important nutritional and economic contribution to Bermuda’s residents.
Fish consumption today is widely recognized as highly beneficial since it constitutes a good source of several essential nutrients, such as selenium and polyunsaturated fatty acids (n-3 PUFA). Several health organizations recommend eating fish twice a week for the general population (Kris-Etherton et al. 2002; Harris 2004). In fact, fish consumption is recognized as beneficial for brain development (Uauy et al. 2001) in the foetus and newborn and has been demonstrated to be protective against cardiovascular diseases (He et al. 2004; Wang et al. 2006), mental disorders (Logan 2003; Sinclair et al. 2007), and various inflammatory conditions such as bowel disease, asthma, and arthritis (Ruxton et al. 2004).
*Corresponding author. Email: [email protected]
ISSN 0265–203X print/ISSN 1464–5122 online ß 2008 Taylor & Francis DOI: 10.1080/02652030802175285 http://www.informaworld.com
´E. Dewailly et al.
2Hg has always been present in all the world’s oceans as a result of river run off, undersea volcanoes, air deposition, etc. and has always built up in fish at the top of the food chain. However, in the last century the industrialization of many countries has resulted in a net increase in the load of Hg in the environment, which consequently is manifest in the world’s fish and in those people who consume them. This is not a local Bermuda problem but a global one. Coastal people living in some of the world’s most remote places are in fact finding that their fish are as contaminated as fish in industrialized coastal areas.
Hg measured was in the form of MeHg, pointing toward seafood as the main source of Hg exposure during pregnancy in Bermuda. In contrast, persistent organic pollutants (POPs) such as polychlorinated biphenyls (PCBs) and chlorinated pesticides along with lead were also measured in cord blood, but concentrations were very low (Dewailly and Pereg 2004). For that reason, only Hg was considered of public health concern.
Fish consumption was also measured and the association of Hg levels with fish consumption was tested using Pearson’s correlation coefficient. Fish consumption was estimated by the number of meals per month that each patient declared eating on a regular basis. Species that were most often consumed include wahoo, snapper, tuna and salmon; the consumption of other species seemed anecdotal. While wahoo and snapper are clearly of local origin, tuna is most often imported. The consumption of local fish was analysed separately from that of total fish consumption. Local fish consumption was estimated by pooling the number of meals/month of wahoo and snapper that each woman declared eating. Separate analyses were also conducted on each fish specie separately (salmon, wahoo, snapper, tuna), despite the low statistical power of some of these analyses.
A significant association was seen between Hg concentrations and the consumption of local fish (Spearman’s r ¼ 0.584, p 5 0.001, n ¼ 40), mainly wahoo (r ¼ 0.502, p ¼ 0.001, n ¼ 40) and snapper (r ¼ 0.499, p ¼ 0.001, n ¼ 40). The consumption of other fish species was not related to Hg content of cord blood.
The globalization of contaminants and the strong media attention regarding the presence of these contaminants in fish in all the world’s oceans has made some consumers wary of fish consumption. This has been counterbalanced by Western scientific discoveries of the last 20 years highlighting the unique health benefits to be gained from the consumption of fish. The informed consumer is today extremely sensitive in their consumption choice.
Given the fact that wild fish consumption is an important part of the lifestyle of many Bermuda residents and because this habit presents not only health benefits, but also risks for pregnant women and their unborn children, Atlantis researchers and the Ministry of the Environment and the Ministry of Health undertook the task of substantiating the Hg, selenium and fatty acid profiles of fish in Bermuda. Such an assessment is necessary in order to provide a baseline for guidelines regarding the number of meals and the type of fish to be preferentially consumed in order to maintain the benefits associated with a fishbased diet while avoiding excessive exposure to MeHg, particularly during pregnancy.
The amount of MeHg in fish usually correlates with several factors including the weight and age of the fish, its trophic level and the species.
Numerous studies have reported that MeHg present in predator fishes represents a potential health threat for the developing foetus. As this seafood borne contaminant affects the development of the cerebral architecture by perturbing neural cell division and migration, the developing nervous system is recognized as the main target (Castoldi et al. 2001; Counter and Buchanan 2004). Several prospective cohort studies have reported effects of prenatal exposure to MeHg on different domains of cognition (attention, memory, visuo-spatial performances and language) and gross and fine motor development, some of which persist well beyond the first years of life (Grandjean et al. 1997; Steuerwald et al. 2000; Debes et al. 2006). In contrast, a large epidemiological study from the Seychelles Islands did not find any effects on infant neurodevelopment from chronic MeHg in utero exposure (Myers et al. 2003; Davidson et al. 2006). Several explanations have been proposed to explain this discrepancy such as chronic versus episodic exposure, age at neurobehavioral assessment, differential confounders adjustment, etc. (National Research Council 2000).
In 2003, as part of the Atlantis Mission, we
- a
- conducted
- study titled ‘Prenatal Exposure of
the Bermudian Population to Environmental Contaminants’ that aimed to provide baseline data on prenatal exposure to a number of environmental contaminants, including Hg. The Atlantis Mobile Laboratory was created as a novel, unique infrastructure to meet emerging environmental and health challenges in remote settings. It is a completely autonomous facility specifically designed for fieldbased environmental and health assessments. It comprises six modules built in standard size containers. Three modules are laboratories and three are dedicated to support the facility.
Mean Hg concentration measured in umbilical cord blood from 42 healthy newborns was higher than
- expected, with a mean concentration of 8.3 mg lÀ1
- ,
ranging from 1 to 32.1 mg lÀ1 (Dewailly and Pereg 2004). Furthermore, it was estimated that 85% of total
Food Additives and Contaminants
3
Materials and methods
within acceptable limits for both CRMs. The laboratory participates successfully in several external quality assessment schemes for heavy metals, including selenium and Hg, in biological fluids and tissues.
Sampling
Fish samples were collected in fall 2003 and summer 2006 from species generally caught at the top of the food chain (e.g., predatory reef fish, pelagic fish) and those that people might commonly consume. Fish were mostly caught by fishermen and given to the researchers, who sampled them onboard the boat or at the laboratory. Some samples of local fresh fish were sampled at restaurants or bought at the store. A total of 307 fish were collected from 43 fish species and 351 samples were analysed (305 flesh samples, 44 liver samples, one roe and one fat sample). Fish samples were packaged in plastic bags and stored at À20ꢀC until laboratory analyses.
The total fatty acid composition of fish fillets was measured at Quebec Lipid Research Centre (CHUQ) after total lipid extraction using a chloroform/methanol mixture (2 : 1 v/v) spiked with phosphatidylcholine C:15 used as internal standard according to a modified Folch method (Shaikh and Downar 1981). Fatty acids were then methylated (Lepage and Roy 1986) and fatty acid profiles obtained by capillary gas–liquid chromatography using a HP5890 gas chromatograph (Hewlett Packard, Toronto, Canada) equipped with a HP-88 capillary column (100 m  0.25 mm i.d. Â0.20 mm film thickness) coupled with a flame ionization detector. Helium was used as carrier gas (split ratio ¼ 1 : 80). Fatty acids were identified according to their retention time, using a standard mixture of 43 methylated fatty acids (Supelco Inc., Bellefonte, PA, USA). Results were expressed as per cent of total fatty acids. The detection limit was 0.1% and the intra-assay coefficient of variation ranged from 0.87% for total omega-3 fatty acids to 6.8% for DHA. This standard method is currently used at the Quebec Lipid Research Centre. Data are presented as percent of total n-3 PUFA or as total n-3 PUFA concentrations (mg) per g of fresh flesh. Analyses of PUFA content were replicated for 16 fishes of different species in order to assess the potential variability between samples.
Laboratory analyses
Fish fillets were analysed for their Hg, selenium and fatty acid concentrations, whereas livers were analysed for their Hg and selenium contents only. Determination of Hg concentrations was performed in the Atlantis mobile laboratory and at the reference laboratory of the Quebec Toxicology Center (INSPQ) by cold vapour atomic absorption mass spectrometry. Samples were digested in nitric acid in pressurized vials. Digests were analysed by cold vapour atomic absorption mass spectrometry in a Pharmacia mercury monitor, model 100. In this instrument, samples are vaporized through a cell that is crossed by a light beam and Hg concentration is calculated by comparing the absorbance at 254 nm with that obtained with a Hg standard curve. Results are expressed on a wet weight basis and the limit of detection using this method is 0.05 mg gÀ1 wet weight.
Selenium concentrations of local Bermuda fish were determined in flesh and liver samples at the INSPQ by inductively coupled plasma mass spectrometry (ICP-MS). Samples were diluted in ammonium hydroxide and elements were brought to their elementary form by passing through argon plasma before being identified by mass spectrometry. All samples were analysed on a Perkin Elmer Sciex Elan 6000 ICP- MS (DRC II for Hg) instrument. Detection limits for
Statistical analysis
For computational purposes, samples with undetected levels of Hg or selenium were attributed a value equal to half the detection limit, which was 0.025 and 0.005 mg gÀ1, respectively. Arithmetic means, standard deviations and range of Hg, selenium and fatty acid concentrations in flesh and/or liver were computed for species with more than one sample available. n-3 PUFA concentrations (mg) were reported for a portion of 220 g of fish. The 220 g mean portion comes from the US Environmental Protection Agency (USEPA) (2000) using a postal survey (with pictures of fish portion size) of 2600 adult consumers.
- selenium were 0.01 mg gÀ1
- .
For metals, sample analyses were done using methods developed and validated by the Quebec Toxicology Center (CTQ). The CTQ laboratory is accredited under ISO 17025 by the Standard Council of Canada (SCC). Appropriate analyses of method blanks, spiked samples and replicates were used to validate the data. To ensure accuracy, certified reference materials (CRMs) DORM-2 (Dogfish Muscle Certified Reference Material for Trace Metals) and DOLT-2 (Dogfish Liver Certified Reference Material for Trace Metals) from the Canadian National Research Council were analysed with each series of samples. Results were
Correlations between fish Hg content and fish weight were carried out. For these analyses data were available only for some of the samples and were therefore carried out by species. Correlation analyses were carried out using Pearson’s correlation coefficients.
Results
Mercury (Hg)
Table 1 shows the Hg concentrations found in all fish flesh samples analysed (wet weight). These mean Hg
´E. Dewailly et al.
4
Table 1. Mercury and selenium concentrations (mg gÀ1) in the flesh of local fish and crustacean species.
- Mercury
- Selenium
- Mean Æ SD
- Common name
- Scientific name
Seriola dumerili Sardinella anchovia Caranx ruber Paranthias furcifer Sphyraena barracuda Kyphosus sectatrix Coryphaena hipparus Euthynnus alletteratus Panulirus argus Mycteroperca bonaci Thunnus atlanticus Makaira nigricans Caranx fusus Haemulon sciurus Albula vulpes Seriola rivoliana Haemulon carbonarum Cephalopholis fulva Etelis oculatus Carcharhinus galapagensis Bothus sp. Cypselurus heterurus Anchoa choerostoma Epinephelus cruentatus Lutjanus griseus Mustelus antarcticus Pseudocaranx dentex Lachnolaimus maximus Cephalopholis fulva Caranx ruber Decapterus macarellus Elagatis bipinnulata Epinephelus guttatus Lutjanus sp. Hexanchus griseus Xiphias gladius Ruvettus nuvettus Thunnus sp. n
- Mean Æ SD
- Range
n
Range
Amberjack Anchovy Bar jack/green jack Barber (creole fish) Barracuda Bermuda chub Bermuda dolphinfish Bermuda mackerel Bermuda spiny lobster Black grouper Blackfin tuna Blue marlin Blue runner Blue-striped grunt Bone fish Bonita (alamaco jack) Caesar grunt Coney Deep water red snapper Dusky shark (Galapagos) Flounder sp. Flying fish Frys Grasby Gray snapper Gummy shark (dogfish) Gwelly
811
- 0.55 Æ 0.46
- 0.20–1.55
- 7
11
11
4
14
- 1.33 Æ 2.24
- 0.42–6.40
0.07 1.0
1.50 0.41
- 12 0.035 Æ 0.028 0.025–0.12
- 0.68 Æ 0.12
0.37 Æ 0.12 0.24 Æ 0.20
0.47–0.86 0.29–0.54 0.11–0.68
- 7
- 0.73 Æ 0.38 0.18–1.40
15 0.038 Æ 0.039 0.025–0.17
1
15
482
0.05
0.68 Æ 0.69 0.21 Æ 0.08 0.87 Æ 0.46 0.20 Æ 0.00 3.10 Æ 0.17 0.98 Æ 0.33 0.33 Æ 0.09
0.50
0.17–2.30 0.15–0.30 0.35–1.55 0.20–0.20 3.00–3.30 0.39–1.30 0.20–0.51
13
3
- 0.50 Æ 0.22
- 0.33–0.50
- 0.37–0.52
- 0.45 Æ 0.08
- 3
- 3
10 14
1
14
1
2.10 Æ 0.35 0.40 Æ 0.07 0.35 Æ 0.05
0.68
1.90–2.50 0.28–0.54 0.23–0.47
10 14
1
- 17 0.170 Æ 0.139 0.025–0.53
- 0.48 Æ 0.09
- 0.32–0.66
0.27–0.78 0.39–0.73
1
29
1
0.09
0.21 Æ 0.10
0.52
0.46
- 0.55 Æ 0.17
- 0.10–0.52
- 17
21621
13
1151
0.56 Æ 0.24
1621
13
11811
17
2
29
211158
0.06
0.035 Æ 0.016 0.025–0.057
0.42
0.31 Æ 0.04 0.54 Æ 0.09
0.62
0.26–0.38
- 0.47–0.60
- 0.12 Æ 0.01
- 0.05–0.19
0.16
0.28 Æ 0.17
1.4 0.37
- 0.09–0.68
- 0.33 Æ 0.05
- 0.25–0.42
0.21–0.42
0.47 0.58
- Hogfish
- 0.067 Æ 0.044 0.025–0.15
- 0.32 Æ 0.09
Hybrid coney-barber Longfin jack/bar jack Ocean robin Rainbow runner Red hind Red snapper Sixgill shark Swordfish Tapioca fish Tuna
0.12 0.48
0.54
- 0.28
- 1
13
2
0.23 Æ 0.09 0.16 Æ 0.06 0.26 Æ 0.08 0.10 Æ 0.01
0.92
0.07–0.35 0.11–0.20 0.14–0.41 0.09–0.10
- 0.69 Æ 0.19
- 0.41–0.95
- 0.43–0.43
- 0.43 Æ 0.00
- 2
- 0.46 Æ 0.00
- 0.46–0.46
3.31 0.15
- 0.35 Æ 0.21
- 0.21–0.70
- 1
77
16
21
0.63
Turbot Wahoo