Risk-benefit analysis of fish consumption: Fatty acid and mercury composition of farmed southern bluefin tuna, Thunnus maccoyii

Food Chemistry 131 (2012) 977–984

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Risk-benefit analysis of fish consumption: Fatty acid and mercury composition of farmed southern bluefin tuna, Thunnus maccoyii S. Balshaw a,b,c,⇑, J.W. Edwards a,c, B.J. Daughtry c,1, K.E. Ross c,2 a

Department of Environmental Health, School of Environment, Flinders University, P.O. Box 2100 Adelaide, South Australia 5001, Australia South Australian Research and Development Institute, Food Innovation and Safety, 33 Flemington Street Glenside, South Australia 5065, Australia c Aquafin Cooperative Research Centre, 2 Hamra Avenue, West Beach, South Australia 5204, Australia b

a r t i c l e

i n f o

Article history: Received 24 January 2010 Received in revised form 12 August 2011 Accepted 22 September 2011 Available online 29 September 2011 Keywords: Southern bluefin tuna Docosahexanoic acid Eicosapentaenoic acid Aquaculture Mercury Consumer safety

a b s t r a c t The docosahexanoic acid (DHA) and eicosapentaenoic acid (EPA) contents and total mercury concentration were measured in whole tissue composites of all edible tissues of wild caught and farmed southern bluefin tuna (Thunnus maccoyii, SBT) and each of the marketed tissue cuts (akami, chu-toro and o-toro) of these fish. Rapid lipid accumulation during culture resulted in a net reduction in mercury concentration of SBT composite tissues and an increase in the concentration of the dietary essential fatty acids. Moreover, the increased affinity of lipid for certain tissue cuts (o-toro) over that of others (e.g. akami), resulted in cross carcass variation in the mercury concentration of fish muscular tissue. Results highlight the potential for farming to be used as a tool to improve the flesh quality of fish species which could otherwise provide limited dietary essential fatty acids to consumers and potentially contain elevated contaminant levels. Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction Fatty acids (saturates, monounsaturates and polyunsaturates), along with proteins and carbohydrates, make up the three principle macronutrient groups needed for normal cellular structure and function (Fernandes & Venkatraman, 1993). The biological function of fatty acids is determined by their chemical structure, and good health is dependent on a balance between the proportions of different dietary fatty acids consumed (Fernandes & Venkatraman, 1993). Whilst all fatty acids provide a rich source of energy, health benefits of fat consumption are primarily associated with the dietary essential polyunsaturated fatty acids (PUFA), omega-6 linolenic acid (LA) and omega-3 a-linolenic acid (ALA). Following consumption, LA and ALA are converted into their physiologically active metabolites via a common enzymatic (d-6-desaturase) route (Ruxton, Reed, Simpson, & Millington, 2004). LA, which is available from most vegetable oils, including sunflower, corn, soybean and safflower oil, is converted into arachidonic acid (AA) and typically ⇑ Corresponding author at: Department of Environmental Health, School of Environment, Flinders University, P.O. Box 2100 Adelaide, South Australia 5001, Australia. Tel.: + 61 8 82262253; fax: + 61 8 82260330. E-mail address: sita.balshaw@flinders.edu.au (S. Balshaw). 1 Current address: Food Standards Australia New Zealand, 55 Blackall Street, Barton Australian Capital Territory 2600, Australia. 2 Current address: Department of Applied Science, Bachelor Institute of Indigenous Tertiary Education, Darwin Annex, Parap Northern Territory 0804, Australia. 0308-8146/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodchem.2011.09.091

comprises up to 5–7% of total dietary energy intake for western populations (Institute of Medicine, National Academy of Sciences (IOM/NAS), 2002). ALA, which is available from flaxseed, canola and soybean oil, is converted to docosahexanoic acid (DHA) and eicosapentaenoic acid (EPA) and typically comprises only 0.4% of total dietary energy intake (IOM/NAS, 2002). Additionally, DHA and EPA are directly bioavailable, almost exclusively from seafood (Howe, Meyer, Record, & Bagurst, 2006). Due to the competitive nature of LA and ALA metabolism into long chain physiologically active PUFA, the proportion of ALA that is effectively converted into its metabolic derivatives, DHA and EPA, is modest and controversial (Kris-Etherton, Harris, & Appel, 2002). Consequently, fish (and fish oil) consumption is the primary and potentially exclusive dietary source of DHA and EPA to modern human populations and, as such, is regarded as playing a crucial role in a healthy well balanced diet. Fish oils and associated DHA and EPA are largely recognised as being beneficial for brain and retinal development (Cohen, Bellinger, Connor, & Shaymitz, 2005; Innis, 2008) and protective against cardiovascular diseases (Kris-Etherton et al., 2002), various inflammatory conditions, such as bowl diseases, asthma and arthritis (Ruxton et al., 2004), and mental disorders (Ruxton et al., 2004). In order to maintain good health and prevent disease, the American Heart Association (see, www.americanheart.org), the UK Food Standards Agency (see, www.food.gov.uk) and the Australian Heart Foundation (see, www.heartfoundation.org.au) recommend consumption of a minimum of two servings of fish per

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week with a special emphasis on oily species. These international recommendations on fish consumption are estimated to provide consumers with a combined intake of DHA and EPA of 0.45 g to 0.9 g daily (Ruxton et al., 2004). However, lipid levels (and levels of DHA and EPA) vary considerably between seafood species. Moreover, in addition to providing a rich source of beneficial PUFA, many fish species are prone to accumulating potentially toxic levels of environmental contaminants, such as polychlorinated biphenyls, dioxins and mercury (Domingo, Bocio, Falco, & Llobet, 2007). The toxic action of these contaminants has the potential to counteract the protective effects of fish oils and may increase the risk of disease (Mahaffey, 2004; Rissanen, Voutilainen, Nyyssonen, Lakka, & Salonen, 2000). Consequently, in order to effectively manage potential risks and benefits of seafood consumption, consumption of species that are high in fatty acids, but low in environmental contaminants, needs to be encouraged. Amongst those species that are recognised as being prone to accumulating elevated contaminant levels, tuna are one of the most frequently consumed and commercially available groups of fish worldwide (e.g. Food Standards Agency (FSA), 2002, Burger, Stern, & Gochfeld, 2005). The high tropic order of tunas, combined with a long life span, facilitates the gradual accumulation of toxic residues, and many wild caught tuna species have frequently been reported with mercury concentrations in excess of maximum international regulatory levels of 1 mg/kg fresh weight (Storelli, Giacominelli-Stuffler, & Marcotrigiano, 2002; Storelli & Marcotrigiano, 2001). Moreover, fatty acid profiles of tunas to date have levels of DHA and EPA that are significantly less than those of other fatty fish species, such as salmon, anchovy and mackerel (Domingo et al., 2007; Mahaffey, 2004; Mozaffarian & Rimm, 2006). However, recent research into the effects of farming on the southern bluefin tuna, Thunnus maccoyii (SBT), has indicated a reduction in mercury concentration of SBT during culture (Balshaw, Edwards, Ross, Ellis, Padula, & Daughtry, 2008). Farming of SBT is based on the transfer of wild caught fish into sea pontoons, where they are cultured under intensive fattening conditions for a period of several months before harvest. Reduced mercury concentration in farmed SBT appears to be the result of rapid lipid accumulation diluting mercury residues associated with fish tissues (Balshaw et al., 2008; Balshaw, Edwards, Ross, & Daughtry, 2008). Using the same cohort of SBT as previously described by Balshaw et al. (2008) and Balshaw, Edwards, Ross, and Daughtry (2008), we present the fatty acid profiles of wild caught and farmed SBT tissue composites and each of the marketed tissue cuts of these fish (akaim, chu-toto, and o-toro). The concentrations of EPA and DHA are compared with mercury concentration in SBT with a view to elucidating the effects of farming on the temporal and spatial distribution of mercury and beneficial fatty acids in SBT edible tissues. The current study builds on that of previous studies relating to mercury concentration of SBT tissues (Balshaw et al., 2008; Balshaw, Edwards, Ross, & Daughtry, 2008) by elucidating whether culture conditions have the two-fold benefit of rapidly decreasing toxic mercury concentration and increasing the concentration of beneficial fatty acids at harvest. Mercury and fatty acid levels in SBT are compared with dietary recommendations with a view to providing insight for farm managers, consumers and seafood advisory statements. Moreover, fatty acid profiles of SBT are compared with those reported for other tuna species and commonly consumed seafood species.

of the purse-seine capture of wild southern bluefin tuna (SBT) in the Great Australian Bight in March 2005. Over a period of weeks, SBT were towed to the coastal waters of Port Lincoln where they were transferred into two sea pontoons and fattened on a diet of local and imported baitfish species until harvest. The experiment lasted for 136 days from 8 April, 2005, until 22 August, 2005. In total, 35 SBT were harvested: five SBT at transfer into culture pontoons on 8 April, 2005 (day 0) and 5 SBT from each of two experimental pontoons at 52 days of culture on 30 May, 2005, 94 days of culture on 11 July, 2005, and 136 days of culture on 22 August, 2005. All fish were harvested in accordance with normal commercial operational procedures (see Hayward, Aiken, & Nowak, 2007) and were received eviscerated and bled, either frozen or fresh-chilled as for export-bound products. 2.2. Baitfish diets Throughout the culture period, SBT were fed a mixture of three baitfish species (Californian and Australian sardines, Sardinops sagax and Australian redbait, Emmelichthys nitidus) to apparent satiation, twice daily, 6 days a week (weather permitting) in accordance with commercial operational practice. Each pontoon was fed an individual baitfish diet as part of a collaborative, industry-driven research project. A sequential cross-over design was used in which the proportion that each baitfish species comprised, of diets, was changed after each experimental harvest. Results relating to the quantity of baitfish fed to SBT are not presented in the current study; however, the potential effects of differences in diet between the sea pontoons is accounted for as described in Sections 2.4. and 3.1. 2.3. Sample processing In the laboratory, the fork length and weight of specimens were recorded. The head and tail were removed, and the remainder of the carcass was split into left and right halves, each of which were separated into six sections labelled 1–6 (Fig. 1). Each half carcass was processed separately, either for compilation of a composite sample of all white muscular tissues on one side of a fish or for compilation of marketed tissue cut (akami, chu-toro and o-toro) samples. Carcasses were halved by slicing all flesh away from the spinal bone and major vertebral bones; any flesh that did not come away cleanly was later scraped off and placed with its corresponding section. The large portion of flesh that remained inside the dorsal head was removed and included as part of section 1. The skin, bones and dark meat were removed from each section and discarded. The remaining tissue was the white (edible) muscle portion of the fish. For compilation of composite samples, sections 1–6 were weighed and homogenised in a stainless steel Hobart™ food

2. Materials and methods 2.1. Experimental design SBT were obtained from commercially stocked and operated experimental farm pontoons. The operational procedure consisted

Fig. 1. Schematic diagram of SBT identifying each of the six cuts (1–6) used to produce the whole tissue composite and the tissue group composites.

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acid) with quantification by inductively coupled plasma mass spectroscopy (Perkin Elmer Elan 9000). Limit of reporting was 0.01 mg/kg fresh weight. Lipid determination was by gas chromatography mass resolution (Hewlett–Packard 6890 GC fitted with a flame ionisation detector), as described by Soltan and Gibson (2008). Total lipid content and fatty acid characterisation were reported as g/100 g fresh weight. 2.5. Data analysis

Fig. 2. Cross section of a farmed southern bluefin tuna indicating each of the tissue cuts (akami, chu-toto and o-toro).

Analysis of variance (ANOVA) and regression analysis were used to determine the effects of variables (culture time, dietary treatment, SBT age) on the fatty acid and mercury content of SBT. Temporal effects on the proportions of DHA and EPA of total lipids in SBT tissues were determined using regression analysis, following Arcsine square root transformation. Data were transformed to ensure that the proportional data complied with all assumptions of regression analysis. All statistical analyses were performed using the R statistical package, version 2.5.0 (R Development Core Team, 2006) with a significance value of P < 0.05. Total lipid content and fatty acid content of tissues are presented as g/100 g tissue fresh weight. Mercury concentration of tissues is presented as mg/kg tissue fresh weight. 3. Results

processor. Composite samples were composed of a proportionately prepared mixture of sub-samples taken from each of the six section homogenates. Weights of homogenate sub-samples used from each section were determined by calculation of each section’s percentage of total edible weight. Sub-samples were combined and again homogenised to ensure thorough mixing. Marketed tissue cut samples were collected from section 5 only and from just those SBT that were harvested from pontoon 2 after 136 days of culture (n = 5). Tissues in section 5 were divided into akami, chu-toro and o-toro tissue cuts, which are identifiable by location, muscle structure and colour (Fig. 2). Each tissue cut from within section 5 was weighed and homogenised. 2.4. Sample analysis All samples were stored in polythene bags at 80 °C and sent frozen to an accredited external laboratory for analysis (AgriQuality, New Zealand & Nutrition and Functional Food Science Laboratory, Adelaide University Australia). Mercury analysis was by means of wet digestion (Aristar nitric acid and Aristar hydrofluoric

3.1. Composite tissue samples All SBT harvested for the purpose of this study were determined to be 2 and 3 years of age, as is typical for Australian farmed SBT (for further details see Balshaw et al., 2008). ANOVA of age effects on the mercury concentration and fatty acid content of SBT composite tissues at harvest found no significant difference between the 2 and 3 year old SBT for either variable (p > 0.05). Moreover, dietary history of SBT (indicated by pontoon) was also found to have no significant effect on the mercury concentration or the fatty acid content of SBT at harvest (p > 0.05). Consequently, all composite tissue data were combined to produce a single data set combining SBT from across both age classes and dietary histories. The fatty acid profiles of SBT composite samples, at each harvest, are presented in Table 1. A temporal increase, which peaked after 94 days in culture, was observed in the composite tissue concentration of all fatty acid groups (harvest 3). Total lipid content increased from a mean of 0.969 g/100 g at transfer into culture pontoons up to 18.1 g/100 g after 94 days of culture. The combined

Table 1 Mean quantity of total lipid and selected fatty acids in SBT edible tissues during culture. All lipids are presented in g/100 g tissue fresh weight.

Total lipid content Total saturated fatty acids Total trans fatty acids Total mono saturated fatty acids Total omega-6 PUFA LA omega-6 linolenic acid (18:2n 6) AA arachidonic acid (20:4n 6) Total omega-3 PUFA ALA omega-3 a-linolenic acid (18:3n 3) EPA eicsapentaenoic acid (20:5n 3) DHA docosahexanoic acid (22:6n 3) EPA and DHA combined

Harvest 1, 0 days culture (n = 3)

Harvest 2, 52 days culture (n = 9)

Harvest 3, 94 days culture (n = 10)

Harvest 4, 136 days culture (n = 10)

0.969 0.393 0.007 0.248 0.044 0.016

11.5 3.79 0.024 3.38 0.420 0.182

18.1 5.66 0.028 5.18 0.622 0.265

16.6 5.25 0.027 4.79 0.585 0.255

0.020 0.276 0.006

0.115 3.88 0.113

0.169 6.584 0.153

0.157 5.85 0.149

0.073 0.170

1.32 1.89

2.73 2.68

2.28 2.52

0.243

3.21

5.40

4.80

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Fig. 3. Box plot of the percentages that EPA and DHA comprise of SBT composite tissues at each consecutive harvest. Note an outlier in harvest 4 has been identified with red. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

content of EPA and DHA increased from a mean concentration of 0.243 g/100 g at transfer into sea pontoons up to 5.40 g/100 g after 94 days of culture (Table 1). Although the total concentration of all fatty acids in composite tissues increased with time in culture, temporal fluctuations in the percentage (that each fatty acid group comprised of total lipids) was observed to vary with fatty acid group. A clear trend, which does not reach statistical significance, was observed, in which the proportion that EPA and DHA comprise of total lipids increased from that of wild-caught SBT (harvest 1) with each consecutive harvest (Fig. 3). However, there is a clear outlier in harvest 4 (Fig. 3). When this outlier was removed, significance was achieved for harvest 3 (p = 0.0047) and harvest 4 (p = 0.0011). This data point (composite tissue of SBT 33) is confirmed to be an outlier due to inconsistencies between the proportions that EPA and DHA comprise of total lipids in the composite tissue (16.8%) and that of each of the tissue groups (akami, 23.9%; chu-toro, 27.8%; and o-toro, 28.0%). Similarly to EPA and DHA, the proportion, that monounsaturated fatty acids and total omega-3 PUFA comprised of lipid, increased with culture time. However, the proportion that saturated fatty acids, trans fatty acids and omega-6 PUFA comprised of total lipid, decreased with time in culture. This variability resulted in apparent differences in the fatty acid composition between wild-caught and farmed SBT.

Fig. 4. The relationship between SBT composite tissue EPA and DHA concentration (g/100 g) and mercury concentration (mg/kg) at each consecutive harvest.

The mercury concentration of SBT composite tissue samples decreased during culture from a mean concentration at transfer into culture pontoons of 0.533 mg/kg to 0.331 mg/kg after 136 days of culture (harvest 3). Detailed analysis of the mercury content of SBT composite tissue samples has been presented by Balshaw et al. (2008). Minor differences in the lipid and mercury concentrations of SBT tissues, presented here and by Balshaw et al. (2008), are due to differences in sample size and analytical technique between the two studies. Regression analysis found a significant negative linear relationship between the combined content of EPA and DHA and that of mercury (R2 = 0.634, p < 0.0001). Culture of SBT resulted in a temporal increase in the EPA and DHA concentration of SBT tissues and an associated decrease in mercury concentration (Fig. 4).

3.2. Marketed tissue cuts SBT marketed tissue cut data were collected from a single pontoon (and dietary regime) after 136 days of culture (harvest 4) and treated as a single data set, regardless of SBT age. Total lipids and associated fatty acids shared an increased affinity for the o-toro tissues, followed by the chu-toro, over that of the akami (Table 2).

Table 2 Mean quantity of total lipid and selected fatty acids in SBT marketed tissue cuts, akaim, chu-toro and o-toro. All lipids are presented in g/100 g tissue fresh weight.

Total lipid content Total saturated fatty acids Total trans-fatty acids Total mono-saturated fatty acids Total omega-6 PUFA LA omega-6 linolenic acid (18:2n 6) AA arachidonic acid (20:4n 6) Total omega-3 PUFA ALA omega-3 a-linolenic acid (18:3n 3) EPA eicsapentaenoic acid (20:5n 3) DHA docosahexanoic acid (22:6n 3) EPA and DHA combined

Akami (n = 5)

Chu-toro (n = 5)

O-toro (n = 5)

4.17 1.44 0.009 1.22 0.140 0.058 0.043 1.34 0.029 0.535 0.579 1.11

21.1 6.43 0.035 6.12 0.752 0.322 0.203 7.74 0.195 3.07 3.29 6.35

32.2 9.77 0.048 9.46 1.12 0.486 0.305 11.7 0.309 4.50 5.08 9.58

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4. Discussion

Fig. 5. The relationship between EPA and DHA concentration (g/100 g) and mercury concentration (mg/kg) in each of the marketed tissue cuts of SBT (akami, chu-toro and o-toro).

After 136 days of culture, the mean total lipid content was 32.2 g/ 100 g in o-toro, 21.1 g/100 g in chu-toro and 4.17 g/100 g in akami tissues. The combined content of EPA and DHA was 9.58 g/100 g in o-toro, 6.35 g/100 g in chu-toro and 1.11 g/100 g in akami tissues (Table 1). The percentage that EPA and DHA comprised, of total lipids of SBT marketed tissues, increased with increased lipid content of the tissue. The chu-toro (p = 0.0098) and o-toro (p = 0.0139) tissues were both found to have a significantly higher percentage of EPA and DHA when compared with the akami tissue. The mean mercury concentrations of SBT marketed tissue cuts of akami, chu-toro and o-toro were 0.392 mg/kg, 0.317 mg/kg and 0.241 mg/kg, respectively. Regression analysis found a significant negative linear relationship between the combined content of EPA and DHA and that of mercury (R2 = 0.596, p < 0.001). Those tissues with an increased EPA and DHA content were observed to have a reduced mercury concentration (Fig. 5).

Seafood is widely recognised as a rich source of omega-3 PUFA and the only naturally occurring source of EPA and DHA in the human diet (Howe et al., 2006). However, amongst different fish species, there is considerable variation in the total lipid content of fish tissues and the proportions that different fatty acid groups comprise of total lipid (Soltan & Gibson, 2008). Results of this study indicate that, within SBT, the omega-3 PUFA, which are primarily comprised of EPA and DHA, represent one of the most abundant fatty acid groups present in SBT tissues. By comparison, the omega-6 PUFA comprise only a small fraction of total lipids. The high ratio of omega-3 to omega-6 fatty acids has important implications for consumer health as one of the primary benefits of fish consumption is the potential for redressing the dietary balance of AA to EPA and DHA, and ultimately the balance of these fatty acids in the functioning cells of tissues, such as platelets, neutrophils and cardiac tissues (Soltan & Gibson, 2008). The high ratio of omega-3 to omega-6 PUFA, observed in SBT, appears to be typical for tuna species. Bluefin tuna Thunnus thunnus, skipjack tuna Euthynnus pelamis and yellowfin tuna Thunnus albacares are reported with respective fresh fillet EPA and DHA contents of 23.9%, 25.3% and 22.9% of total lipids. By comparison, all other PUFA, including omega-6, comprise only 5.3%, 5.8% and 6.9% of total lipids in these species (United States Department of Agriculture (USDA), 2009). Moreover, SBT have previously been reported with respective omega-3 and omega-6 PUFA contents of 35.4% and 7.2% (Soltan & Gibson, 2008). However, the concentration of EPA and DHA in fish tissues is dependent on both the proportions that these PUFA comprise of total lipids and the total lipid content of fish tissues. Consequently, despite the large proportions of lipids which are present as EPA and DHA in tuna tissues, the typically low lipid content of many wild caught tunas, results in a minimal EPA and DHA concentration in fish fillets. By comparison, farmed tunas are typically observed to have elevated lipid levels and associated fatty acids, resulting from culture techniques specifically designed to increase fish condition, biomass and lipid content (Roy, Ando, Kawasaki, & Tsamasa, 2009; Balshaw et al., 2008; Nakamura, Ando, Seoka, Kawasaki, & Tsukamasa, 2007; AuguadoGimenez & Garcia-Garcia, 2005). Nakamura et al. (2007) report respective total lipid levels of 23% and 55.1% in the dorsal and ventral tissues of propagated Pacific bluefin tuna (PBT) and lipid levels of 2% and 16.2% in the same

Table 3 SBT dietary recommendations – number of fish meals required for population groups to obtain recommended weekly EPA and DHA intake, and the maximum number of fish meals allowable without exceeding tolerable weekly intake of mercury *. SBT meal

Infants

Women

Adults

CHD patientsc

HD patientsc

Number of serves required to meet EPA and DHA recommendationsa (Maximum number of servings permitted whilst maintaining total dietary mercury intake below tolerable weekly intake recommendations)b Wild composite Farmed composited Farmed akamid Farmed chu-torod Farmed o-torod

21 (1/2) 1 (1) 5 (1) 1 (1) 1 (1)

10 (1) 1 (2) 3 (1) 1 (2) 1 (3)

10 (2) 1 (4) 3 (4) 1 (5) 1 (6)

20 1 5 1 1

77 4 17 4 4

* Those SBT meals which represent a practical means of attaining recommended weekly EPA and DHA intake, whilst maintaining total dietary mercury intake below maximum tolerable levels are highlighted with bold numbering. a Serving sizes are based on Australian national serving sizes of 75 g for infants and 150 g for adults; the number of SBT meals required by consumer populations are rounded up to the nearest whole number of servings; EPA and DHA requirements are 0.5 g/day for infants and healthy adults, 1 g/day for coronary heart disease patients and up to 4 g/day for hyperglyceridemia patients. b The quantity (g) of each type of SBT meal that could be consumed without exceeding the tolerable weekly intake was calculated, assuming that the population consumes only this one type of fish. The contribution of non-seafood mercury exposure was taken into account in this calculation as described in FSANZ (2004). The quantity (g) of SBT meal types (wild, farmed, akami, chu-toro, o-toro) allowable were then rounded down to the nearest number of servings; serving sizes are based on Australian national serving sizes of 75 g for infants and 150 g for adults. c There are no recommendations available for the maximum allowable mercury intake of coronary heart disease (CHD) patients or hyperglyceridemia disorder (HD) patients. d Results are based on EPA, DHA and mercury concentration data of SBT harvested following 136 days of culture (harvest 4).

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and EPA comprise of total lipids. Those tissues with higher lipid contents were also observed to have an increased proportion of EPA and DHA. Consequently, the farming process appears to result in an increase in the nutritional value of SBT tissues. Moreover, as a negative linear relationship was observed between the concentration of EPA and DHA and the concentration of mercury in SBT tissues, farming of SBT appears to have the two-fold benefit of reducing the mercury concentration of SBT tissues and increasing the EPA and DHA concentration. Although variation is observed between individual SBT, results indicate that culture of SBT for 94 to 136 days will result in end-products with the highest level of integrity in terms of nutritional value and consumer safety (See Fig. 3). Maximum EPA and DHA levels reported for SBT in the current study were 5.40 g/ 100 g composite tissue after 94 days of culture and 9.58 g/100 g for o-toro tissues after 136 days of culture. As tis-

tissues of wild caught PBT. Moreover, fatty acid profiles of the lipids of wild-caught and farmed PBT were noted to be significantly different. Farmed PBT are observed to have a significantly increased proportion of monounsaturated fatty acids and a decreased proportion of PUFA (particularly DHA) when compared with their wild counterparts (Nakamura et al., 2007; Roy et al., 2009). Consequently, the nutritional value of wild PBT lipid is greater than that of farmed PBT. However, the higher lipid content in farmed PBT results in a greater concentration of omega-3 PUFA when compared with wild PBT. Interestingly, farmed PBT are reported to have a higher proportion of PUFA in akami tissues (lean tissues) when compared with the chu-toro and o-toro (Roy et al., 2009). In the current study, culture of SBT resulted in a rapid and significant increase in the total lipid content of tissues. In contrast to PBT, a significant increase was observed in the proportion that DHA

Table 4 Number of fish meals required for population groups to obtain recommended weekly EPA and DHA intake *. DHA & EPA (g/ 100 g)

PBT – farmed, ventral SBT – harvest 4, o-toro SBT – harvest 4, chutoro PBT – farmed, dorsal SBT – harvest 3, composite PBT – wild, ventral tissue Atlantic salmon Swordfish Hake Salmon, canned

Thunnus orientalis Thunnus maccoyii Thunnus maccoyii

14.3 9.58 6.35

1 1 1

1 1 1

1 1 1

2 2 3

Nakamura et al. (2007) Current paper Current paper

Thunnus orientalis Thunnus maccoyii

5.98 5.40

1 1

1 1

1 1

4 4

Nakamura et al. (2007) Current paper

Thunnus orientalis

4.89

2

1

1

4

Nakamura et al. (2007)

Salmo Salar Xiphias gladius

2.88 1.94 1.92 1.62

2 3 3 4

1 2 2 2

2 3 3 3

7 10 10 12

NBT Gemfish SBT – harvest 4, akami Mackerel, canned Mackerel European carp Tuna, canned, white Red mullet PBT – wild, dorsal Snook

Thunnus thunnus Rexen Solandri Thunnus maccoyii

1.17 1.12 1.11 0.851 0.840 0.770 0.711 0.710 0.604 0.584

5 5 5 6 6 7 8 8 9 9

2 3 3 3 3 4 4 4 4 5

4 5 5 6 6 7 7 7 8 9

16 17 17 22 23 25 27 27 31 32

Soltan and Gibson (2008) Soltan and Gibson (2008) Domingo et al. (2007) Shim, Dorworth, Lasrado, and Santerre (2004) USDA (2009) Soltan and Gibson (2008) Current paper Shim et al. (2004) Domingo et al. (2007) Soltan and Gibson (2008) Shim et al. (2004) Domingo et al. (2007) Nakamura et al. (2007) Soltan and Gibson (2008)

0.581 0.578 0.440 0.439 0.430 0.414 0.383 0.370 0.360 0.310 0.308 0.307 0.300 0.270 0.256 0.251 0.246 0.243

9 9 12 12 12 13 14 14 14 17 17 17 18 19 20 20 21 21

5 5 6 6 6 6 7 7 7 8 8 8 8 9 10 10 10 10

9 9 11 11 11 12 13 13 13 15 16 16 16 18 19 19 19 20

33 33 43 43 44 46 49 51 52 61 61 61 63 70 73 75 76 77

Soltan and Gibson (2008) Shim et al. (2004) Domingo et al. (2007) Soltan and Gibson (2008) Domingo et al. (2007) Soltan and Gibson (2008) Soltan and Gibson (2008) Domingo et al. (2007) Domingo et al. (2007) Soltan and Gibson (2008) Soltan and Gibson (2008) Soltan and Gibson (2008) Domingo et al. (2007) Domingo et al. (2007) USDA (2009) Soltan and Gibson (2008) Soltan and Gibson (2008) Current paper

0.232 0.218 0.210 0.190 0.180

22 23 24 27 28

10 10 12 13 13

21 22 23 25 26

81 86 89 99 104

Soltan and Gibson (2008) USDA (2009) Domingo et al. (2007) Domingo et al. (2007) Domingo et al. (2007)

Squid Tuna, canned, light Anchovy Australian salmon Sardine Tommy ruff Rainbow trout Sole Cuttlefish Deep sea cod Barramundi Red snapper Swordfish Mussel Skipjack tuna Skate Northern whiting SBT – harvest 1, composite SBT Yellowfin tuna Shrimp Tuna, unidentified Clam *

Thunnus orientalis Sphyraena novaehollandiae Sepioteuthis australis

Arripis trutta Arripis georgianus Oncorhynchus mykiss

Mora moro Lates Calcarifer Centroberyx gerrardi

Euthynnus pelamis Irolita waitii Sillago sihama Thunnus maccoyii Thunnus maccoyii Thunnus albacares

Healthy adults

HGb patients

Species name

Cyprinus carpio

Infants

CHDa patients

Common name

Source

Serving sizes are based on Australian national serving sizes of 75 g for infants and 150 g for adults; the numbers of fish meals required by consumer populations are rounded up to the nearest whole number of servings; EPA and DHA requirements are 0.5 g/day for infants and healthy adults, 1 g/day for coronary heart disease patients and up to 4 g/day for hyperglyceridemia patients. a Coronary heart disease (CHD) patients. b Hyperglyceridemia (HD) patients.

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sue cuts were not sampled at 94 days of culture, there is potential for further increases in the maximum achievable EPA and DHA content of SBT tissues under current industry practice. The practical significance of increased PUFA and decreased mercury levels in the tissues of farmed SBT can be evaluated by calculating the number of fish meals required to attain recommended daily intakes of EPA and DHA for consumer populations. Daily DHA and EPA dietary requirements vary according to the health status of consumers. Current international recommendations are that infants and healthy adults consume 0.5 g/day, patients with coronary heart disease (CHD) consume an average of 1 g/day and patients with hyperglyceridemia disorder (HD) consume up to 4 g/day in conjunction with mental consultation (Soltan & Gibson, 2008). Farmed SBT were determined to have a mean EPA and DHA content of 5.40 g/100 g after 94 days of culture (harvest 3) and 4.80 g/ 100 g after 136 days of culture (harvest 4). At these concentrations, EPA and DHA requirements of infants can be achieved solely through consumption of one 75 g SBT meal weekly; requirements of healthy adults and coronary heart disease patients can be achieved through consumption of one 150 g SBT meal weekly, and patients with hyperglyceridemia disorder can achieve the recommended intake through consumption of up to four 150 g SBT meals weekly. Moreover, if the chu-toro or o-toro tissues of farmed SBT are consumed, the number of fish meals required can be reduced further still (see Table 3). By comparison, attainment of recommended EPA and DHA intakes for consumer populations are largely unattainable through the consumption of wild-caught SBT alone. Respective weekly intakes of 21, 10, 20 and 77 wild-caught SBT meals would be required to achieve EPA and DHA requirements for infants, healthy adults, coronary heart disease patients and patients with hyperglyceridemia disorder (see Table 3). Moreover, the increased mercury concentration of wild-caught SBT would preclude any safe attempts to acquire recommended EPA and DHA intakes from wild-caught SBT alone. Current national (Food Standards Australia New Zealand (FSANZ), 2004) and international (Joint FAO/WHO Expert Committee on Food Additives (JEFCA), 2003) tolerable weekly intake levels set for mercury are 3.3 lg/kg body weight for the general population and 1.6 lg/kg body weight for women of child-bearing age. Mercury concentrations for composite tissue samples reported in the current study suggest that, under current Food Standards Australia New Zealand (FSANZ, 2004) recommendations, adults are able to consume up to four 150 g servings of farmed SBT, women of child-bearing age can consume two 150 g servings of farmed SBT and children are able to consume one weekly 75 g serving of farmed SBT whilst maintaining total mercury dietary intake levels below recommended levels (FSANZ, 2004). Consequently, results of this study identify farmed SBT as a rich source of PUFA which can provide consumer populations with recommended DHA and EPA requirements whilst maintaining total dietary mercury intake below maximum tolerable intake levels. Dietary recommendations are summarised in Table 3, in which the number of servings of SBT required to meet DHA and EPA recommended intake are presented, along with the maximum number of servings allowable without exceeding tolerable weekly intake of mercury. Results are presented for wild SBT and farmed SBT tissue composites and each of the marked tissues cuts. Comparison of the number of SBT meals required by consumer populations in order to attain daily DHA and EPA requirements from SBT and other commonly consumed seafoods is presented in Table 4. For the majority of fish species, consumption of two fish meals a week (as recommended by the Australian Heart Foundation and the American Heart Association) is unlikely to provide consumers with recommended EPA and DHA dietary intakes

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(Table 3). Comparison of SBT with that of other seafood species indicates that farmed SBT are likely to contain higher levels of EPA and DHA than are fishes such as salmon, anchovy and mackerel, which are typically advocated as the species likely to provide optimum levels of omega-3 PUFA whilst maintaining reduced levels of contaminants such as mercury (Mahaffey, 2008; Domingo et al., 2007). Results highlight the potential for farming to be used as a tool to ameliorate the flesh quality of fish species which could otherwise provide limited dietary essential fatty acids to consumers and potentially have elevated contaminant levels. 5. Conclusions Rapid lipid accumulation during culture resulted in a net reduction in mercury concentration of SBT composite tissues and an increase in the concentration of the dietary essential fatty acids. Moreover, the increased affinity of lipid for certain tissue cuts (otoro) over that of others (e.g. akami), resulted in cross carcass variation in the mercury concentration of fish muscular tissue. Results highlight the potential for farming to be used as a tool to improve the flesh quality of fish species which might otherwise provide limited dietary essential fatty acids to consumers and potentially have elevated contaminant levels. Acknowledgements This work formed part of a project of Aquafin CRC and received funds from the Australian Governments CRCs programme, the Fisheries R&D Corporation and other CRC participants. We thank Stephan Schilling, Terry Moir and DI Fishing for logistical support, Phil Bridgen and Agriquality New Zealand, for analytical services relating to mercury analysis, Robert Gibson, David Apps and the Nutrition and Functional Food Science Laboratory, Adelaide University, for analytical services relating to lipid characterisation, Tom Madigan, Samuel Phua, and Peter Babidge for technical support, and David Warland and David Ellis, for industry mentoring and liaising. References Augado-Gimenez, F., & Garcia-Garcia, B. (2005). Changes in some morthometric relationships in Atlantic bluefin tuna (Thunnus thynnus thynnus Linnaeus, 1758) as a result of fattening process. Aquaculture, 249, 303–309. Balshaw, S., Edwards, J. W., Ross, K. E., & Daughtry, B. J. (2008). Mercury distribution in the muscular tissue of farmed southern bluefin tuna (Thunnus maccoyii) is inversely related to the lipid content of tissues. Food Chemistry, 111, 616–621. Balshaw, S., Edwards, J. W., Ross, K. E., Ellis, D., Padula, D., & Daughtry, B. J. (2008). Empirical models to identify mechanisms driving reductions in tissue mercury concentration during culture of farmed southern bluefin tuna Thunnnus maccoyii. Marine Pollution Bulletin, 56(12), 2009–2017. Burger, J., Stern, A. H., & Gochfeld, M. (2005). Mercury in commercial fish: Optimising individual choices to reduce risk. Environmental Health Perspectives, 113, 1–6. Cohen, J. T., Bellinger, D. C., Connor, W. E., & Shaymitz, B. A. (2005). A quantitative analysis of prenatal intake of n 3 polyunsaturated fatty acids and cognitive development. American Journal of Preventative Medicine, 29, 366–378. Domingo, J. L., Bocio, A., Falco, G., & Llobet, J. M. (2007). Benefits and risks of fish consumption Part I. A quantitative analysis of the intake of omega-3 fatty acids and chemical contaminants. Toxicology, 230, 219–226. Fernandes, G., & Venkatraman, J. T. (1993). Role of omega-3 fatty acids in health and disease. Nutrition Research, 13(Suppl. 1), S19–S45. Food Standards Agency (FSA), (2002). Mercury in imported fish and shellfish and UK farmed fish and their products, Food Surveillance Information Sheet 40/03 2002. Accessed 05.06.08. Food Standards Australia and New Zealand (FSANZ), (2004). Mercury in Fish – Further Information. Available at: Accessed 29.07.07. Hayward, C. J., Aiken, H. M., & Nowak, B. F. (2007). Metazoan parasites on gills of southern bluefin tuna (Thunnus maccoyii) do not rapidly proliferate after transfer to sea cages. Aquaculture, 262, 10–16.

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