Nutrient composition of fish and seafood products

Fish and other seafood products, namely molluscs, crustaceans and echinoderms, consumed directly or processed provide a huge variety of products of interest for nutritional benefits in human. The detailed composition of finfish, crustacean, mollusc and echinoderm species can be found in a selected number of international databases (United States Department of Agriculture National Nutrient Database for Standard Reference Nutrient Data Laboratory (NDL)/Food and Nutrition Information Center (FNIC) Food Composition Database, http://ndb.nal.usda.gov; SELFNutritionData, http://nutritiondata.self.com; International Network of Food Data Systems Standards and Guidelines, http://www.fao.org/infoods/infoods/standards-guidelines/en/as well as in some national databases, e.g. Base española de datos de composición de alimentos, http://www.bedca.net/

Depending on the species, fish has a water content ranging 60–80 % weight and the marine invertebrates 53–96 %. The N fraction is composed of proteins (12–20 %) and of non-protein N compounds (1–2 %). Seafood proteins have a high digestibility and biological value because muscles mainly constitute sarcoplasmic (myoalbumin, globulins and enzymes) and myofibrillar proteins (actin, myosin and tropomyosin) with a very low content of connective proteins (collagen ranging 3–10 %, compared with 17 % of mammals). All essential amino acids are present in fish protein in adequate amounts compared with milk, eggs and meat. Free amino acids, namely histidine and taurine, some peptides, such as anserine and carnosine, as well as other non-protein compounds, such as free nucleotides and creatine, are also present in comparatively high amounts⁽Reference Oehlenschläger^3, Reference Ros, Martinez-Graciá, Santaella-Pascual and Gil¹⁹⁾.

Lipids are important nutrients for fish. Depending on its lipid content, fish is classified into lean fish ( < 2·5 % fat, mainly Gadidae and Pleuronectidae, e.g. cod, haddock, saithe and sole), medium fatty fish (2·5–6 % fat, mainly Merlucciidae and Phycidae, e.g. hake, sea bass and ocean perch) and fatty fish (>6–25 % fat, mainly Cupleidae, Engraulidae, Scombridae and Salmonidae, e.g. anchovy, herring, sardine, mackerel, tunas, bonitos and salmon). The quantitative and qualitative lipid contents vary according to the species, age, sex, period of the year, etc. n-3 LC-PUFA are key compounds abundant in sea fish, ranging from about 0·2 % weight in lean fish to about 3 % weight in fat fish. Crustaceans, shellfish and cephalopods are lean species with lipid content ranging 0·9–2·2 %⁽Reference Oehlenschläger^3, Reference Ros, Martinez-Graciá, Santaella-Pascual and Gil¹⁹⁾.

Fish have on average 35 mg cholesterol/100 g and contribute little to the dietary cholesterol intake. However, most of crustaceans, e.g. shrimps and prawns, show high contents of cholesterol (about 100–150 mg/100 g). Even higher levels are found in cephalopods (>200 mg/100 g) and the richest content is found in fish eggs and derived by-products such as caviar (about 500 mg/100 g)⁽Reference Oehlenschläger^3, Reference Ros, Martinez-Graciá, Santaella-Pascual and Gil¹⁹⁾.

The carbohydrate content of fish and other seafood products is usually lower than 0·5 %⁽Reference Ros, Martinez-Graciá, Santaella-Pascual and Gil¹⁹⁾.

The amount of vitamins and minerals is species-specific and varies according to the diet and season of the year. Fish is considered a good source of Ca (about 10–100 mg/100 g), Mg (10–170 mg/100 g) and P (200–300 mg/100 g), as well as F (300–400 μg/100 g), I (10–300 μg/100 g), Se (35–45 μg/100 g), Fe (0·3–2·8 mg/100 g), Zn (0·3–1·3 mg/100 g) and Cu (0·1–0·2 mg/100 g). However, fish is a poor source of Na (20–140 mg/100 g) but rich in K (200–400 mg/100 g). Seafood products are one of the few natural sources of I and Se⁽Reference Oehlenschläger^3, Reference Ros, Martinez-Graciá, Santaella-Pascual and Gil¹⁹⁾. The highest Se levels are usually present in tuna, swordfish and scad⁽Reference Olmedo, Hernández and Pla¹⁶⁾. Mussels, scad and sardines are the fresh species with the highest Zn levels. Molluscs and crustaceans are the major contributors of Cu and Fe; their remarkable concentration of Cu could be accounted for the presence of haemocyanin, a Cu-containing respiratory protein found in the blood of those species⁽Reference Olmedo, Hernández and Pla^16, Reference Sirot, Dumas and Leblanc²⁰⁾.

Fish is rich in vitamins, namely thiamin (vitamin B₁) (40–210 μg/100 g), riboflavin (vitamin B₂) (50–360 μg/100 g), niacin (vitamin B₃) (2–10 mg/100 g), pyridoxine (200–980 μg/100 g) and specially cobalamin (vitamin B₁₂) (1–9 μg/100 g). Clupeidae and Engraulidae exhibit the highest content of vitamin B₁₂. Liposoluble vitamins, mainly vitamins A and D, are mostly accumulated in the liver, although some species also exhibit a high content in the muscle mass. It is well known that high content of vitamins A and D is present in the liver of codfish species. Vitamin A in fish fillet ranges 3–180 mcg (micrograms)/100 g. The vitamin D content of fish may vary enormously and it is not well correlated with the fat content, values range 3–20 μg/100 g⁽Reference Oehlenschläger^3, Reference Ros, Martinez-Graciá, Santaella-Pascual and Gil^19, Reference Lund²¹⁾.

Health outcomes related to fish and other seafood consumption

The epidemiological evidence to support the consumption of seafood is mainly derived from cohort studies. However, it is difficult to identify which nutrient is important due to the presence of other covariants in the diet⁽Reference Lund²¹⁾.

Moderate-to-high intake of fish has been associated with a decrease in the prevalence of chronic diseases associated with obesity, namely CVD, diabetes and some cancers⁽Reference Oehlenschläger^3, Reference Lund²¹⁾. Although n-3 LC-PUFA, derived mainly from fatty fish, have been the most important focus of research related to benefits of fish consumption and because of their relevant benefits will be considered separately in the present report, protein, some non-protein N compounds, namely taurine and choline, some minerals, particularly Se, and vitamins B₁₂ and D have been reported to be associated in protection against CHD. Seafood consumption is associated with reduced markers of inflammation⁽Reference Zampelas, Panagiotakos and Pitsavos²²⁾, which can explain, at least in part, its effect of protection against CVD and diabetes. It is also associated to reduced blood pressure and less vascular damage⁽Reference Panagiotakos, Zeimbekis and Boutziouka²³⁾. Meta-analyses of cohort studies also suggest a strong protective effect of stroke⁽Reference Bouzan, Cohen and Connor^24, Reference He, Song and Daviglus²⁵⁾. This effect cannot be exclusively attributed to EPA and DHA, but also to other seafood components. Thus, taurine in experimental animals have positive effects on the cardiovascular system and diabetes. In addition, it has been associated with a number of health effects such as better fat digestion and visual acuity improvement in infants⁽Reference Manna, Das and Sil²⁶⁾. Vitamin B₁₂ can also be important in relation to both CVD and stroke through reduction of plasma homocysteine⁽Reference Ryan-Harshman and Aldoori²⁷⁾. Mineral elements are among the most important nutrients provided by fish because they participate in many biological processes. In fact, seafood consumption may contribute to the reduction in the prevalence of mineral inadequacies and as a consequence seafood consumption could be promoted⁽Reference Sirot, Dumas and Leblanc²⁰⁾. Zn is a cofactor to more than 300 enzymes involved in important functions such as RNA and DNA metabolism and plays a major role in the stabilisation of the structure of a large number of proteins, including signalling enzymes at all levels of cellular signal transduction⁽Reference Chasapis, Loutsidou and Spiliopoulou²⁸⁾. Through its ability to change oxidation state, Cu is a well-established essential element that is required as a catalytic cofactor in numerous critical enzyme reactions⁽Reference Stern²⁹⁾. Se is a critical component of numerous selenoproteins in humans, some of which are important antioxidant systems (e.g. glutathione peroxidase) that actively protect against damage from free radicals and reactive oxygen species, which in turn could protect against cancer or CVD⁽Reference Flores-Mateo, Navas-Acien and Pastor-Barriuso^30, Reference Greenwald, Anderson and Nelson³¹⁾. Fish intervention studies, e.g. SEAFOOD Plus and AQUAMAX, funded by the European Union, have focused on biomarkers of effect. Indeed, the intake of 300–450 g/week of both cod and salmon improves the Se status and contributes to the reduction of inflammatory and cardiovascular biomarkers and lead to some benefit in weight control and blood pressure⁽Reference Parra, Bandarra and Kiely³²⁾. Similarly, in pregnant women, the weekly intake of two portions of salmon is associated to a better status of Se in mothers and their newborns, as well as to a higher activity of glutathione peroxidase⁽Reference García-Rodríguez, Mesa and Olza³³⁾. Several studies also showed that Se may protect against the toxic effects of Hg, particularly organic methylmercury⁽Reference Bates, Prentice and Birch^34, Reference Park and Mozaffarian³⁵⁾. Accordingly, the Hg:Se ratio could be a useful tool to better assess the risk associated with fish intake, especially in predatory species such as tuna⁽Reference Olmedo, Hernández and Pla^16, Reference Burger and Gochfeld³⁶⁾.

Large cohort studies show that fish intake is not associated with either increase or decreases in the risk of cancer overall. However, there is significant evidence of protection for colorectal cancer⁽Reference Geelen, Schouten and Kamphuis³⁷⁾ and some evidence in relation to prostate cancer⁽Reference Linseisen, Rohrmann and Bueno-de-Mesquita³⁸⁾. Not only n-3 LC-PUFA but also vitamin D and Se can have a role in this protective effect⁽Reference Lund²¹⁾.

Health benefits of fish consumption related to n-3 long-chain PUFA

n-3 LC-PUFA are conditionally essential nutrients for adequate growth, development and function in humans. The effects of DHA and EPA are mediated by modulation of membrane biophysical properties but also by effects on cell growth, differentiation and functional maturation, and by modulating gene expression during development and at all subsequent stages of human life⁽Reference Gil, Serra-Majem and Calder^2, Reference Corella and Ordovás³⁹⁾. Additionally, fish consumption and hence n-3 LC-PUFA has been associated with a reduced risk for a number of chronic diseases (Table 1).

Table 1 Levels of evidence of effects of fish and n-3 long-chain (LC) PUFA consumption on disease prevention

BC, breast cancer; CHD, coronary heart disease; CRC, colorectal cancer; PC, prostate cancer.

Health risks of fish consumption

Marine toxins and infectious agents including parasites (nematodes, cestodes and trematodes) and bacteria have been found in seafood products. For example, bivalve molluscs feed by filtering large volumes of seawater. During this process, they can accumulate and concentrate pathogenic micro-organisms. The illnesses caused by these agents range from gastrointestinal diseases to severe poisonings (paralytic, amnesic, neurotoxic and diarrhoeic syndromes). Allergens have also been found in seafood products and are usually associated with allergy processes in sensitive subjects.

However, the most concerning problem from a public health point of view is the exposure to low doses of chemical pollutant mixtures (heavy metals and organic compounds such as organochlorine pesticides, polycyclic aromatic hydrocarbons, PCB, dioxins and dibenzofurans) among populations in non-occupational settings, especially women of reproductive age, pregnant or nursing women; breast-fed infants; and young children living in industrial areas. They are exposed by inhaling pollutants from industrial emissions and also by eating and drinking polluted food (including seafood) and water⁽Reference Rodríguez-Barranco, Lacasaña and Aguilar-Garduño^52, Reference Hernández, Gil, Tsatsakis and Gupta⁵³⁾. Food Safety and Nutrition Agencies have raised public concern as it claimed that some pollutants (e.g. methylmercury) in certain fish species make them unsuitable for consumption by children and pregnant women, so that it is important to provide information in order to achieve a better risk assessment from seafood consumption. For example, European regulations limit the amount and type of certain contaminants that can appear in foodstuffs⁽⁵⁴⁾.

More than 1000 chemical substances are known to have neurotoxic effects in experimental animals. Of these, Pb, methylmercury and As are three relevant substances that have been shown to cause neurodevelopmental disorders in humans and subclinical brain dysfunction⁽Reference Rodríguez-Barranco, Lacasaña and Aguilar-Garduño⁵²⁾. A number of epidemiological studies on neurobehavioral development in children have been conducted in populations consuming seafood products⁽Reference Grandjean, Weihe and White^55–Reference Davidson, Strain and Myers⁵⁷⁾ and there is convincing evidence of adverse neurological/neurodevelopmental outcomes in infants and young children associated with methylmercury exposure during fetal development due to maternal fish consumption during pregnancy^(6, Reference Axelrad, Bellinger and Ryan⁵⁸⁾. Other important conclusions from FAO and WHO Expert Committee were as follows: (1) the absence of probable or convincing evidence of risk of CHD associated with methylmercury; (2) when comparing the benefits of n-3 LC-PUFA with the risks of methylmercury among women of childbearing age, maternal fish consumption lowers the risk of suboptimal neurodevelopment in their offspring compared with the offspring of women not eating fish in most circumstances evaluated.

Also several epidemiological studies provide limited evidence of an association between methylmercury body burden, primarily from fish consumption and CVD⁽Reference Hallgren, Hallmans and Jansson^59, Reference Yoshizawa, Rimm and Morris⁶⁰⁾.

More recently, our research team⁽Reference Olmedo, Pla and Hernández¹⁷⁾ has published the levels of Hg, Cd, Pb, Sn and As in fresh, canned and frozen fish and shellfish products from a total of 485 samples of the forty-three most frequently consumed species in Andalusia (Southern Spain). High Hg concentrations were found in some predatory species (blue shark, cat shark, swordfish and tuna), although they were below the regulatory maximum levels (Table 2 and Fig. 1). In the case of Cd, bivalve molluscs such as canned clams and mussels presented higher concentrations than fish, but almost none of the samples analysed exceeded the maximum levels regulated. Pb concentrations were almost negligible with the exception of frozen common sole, which showed median levels above the legal limit. Sn levels in canned products were far below the maximum regulatory limit, indicating that no significant Sn was transferred from the can. As concentrations were higher in crustaceans such as fresh and frozen shrimps. Storelli et al. ⁽Reference Storelli, Normanno and Barone⁶¹⁾ found similar Hg levels in fresh tuna (0·530 mg/kg ww) and swordfish (0·800 mg/kg ww). However, in our samples analysed, Cd concentrations were rather low, which is in contrast to Storelli et al. ⁽Reference Storelli, Normanno and Barone⁶¹⁾ who found remarkable Cd levels in cuttlefish and swordfish (0·85 and 0·25 mg/kg ww, respectively) caught in Italy. The risk assessment performed indicated that fish and shellfish products were safe for the average consumer, although a potential risk cannot be dismissed for regular or excessive consumers of particular fish species, such as tuna, swordfish, blue shark and cat shark (for Hg) and common sole (for Pb).

Table 2 Estimated amounts of toxic elements ingested by fish in Andalusia, Spain and their respective provisional tolerable weekly intake percentages

PTWI, provisional tolerable weekly intake.

Fig. 1 Comparison between metal levels ((a) mercury, (b) lead, (c) cadmium and (d) tin) found in fish and shellfish Spanish samples analysed and the legal categories for each metal according to the European Commission (Regulation EC no. 1881/2006 amended by EC no. 629/2008 and EC no. 420/2011). * Includes muscle meat fish excluding 3.3.2 category. † Muscle meat of fish for category 3.3.2. ‡ Muscle meat of fish (all categories). ■, Number of samples and percentage under limit of detection. □, Number of samples and percentage over the maximum legal limit.

We have also published⁽Reference Olmedo, Hernández and Pla¹⁶⁾ the levels of four essential elements (Cu, Mn, Se and Zn) in fish and shellfish products mentioned earlier, including the risk and nutritional assessment and Hg:Se ratios as well as Se health benefit value. Concerning Se, probably the most important of them, two fresh predatory fish species (tuna and swordfish) presented the most remarkable concentrations of this element. All the species analysed showed beneficial Hg:Se ratios and Se health benefit values, except for the shark species (blue shark and cat shark) and gilt-head bream because of their high Hg levels and low Se content, respectively. Nevertheless, the biomagnification usually observed in hazardous metals such as Hg would not occur for the essential elements measured in predatory species. The contribution of seafood products to the recommended daily allowances and adequate intakes of these mineral elements ranges from 2·5 % (Mn) to 25·4 % (Se). The species more advisable according to Se health benefit values were sardine and anchovy.

Moreover, PCDD and PCDF, PCB including dioxin-like PCB and non-dioxin-like PCB, organochlorine pesticides, and polybrominated diphenyl ethers are lipophillic organic compounds whose origin comes from many different sources. PCDD/PCDF and PCB are ubiquitous and persistent environmental pollutants with a well-known potential toxicity⁽Reference Domingo and Bocio^62, Reference Yu, Guo and Zeng⁶³⁾. Dioxin and PCB levels in fish are usually low and potential carcinogenic and other effects are outweighed by potential benefits of fish intake and should have little impact on choices or consumption of seafood⁽Reference Mozaffarian and Rimm¹⁴⁾. Although dioxins can cause a variety of adverse health effects, including cancer, effects on the immune system, reproductive system, nervous system and endocrine system, it has been concluded that at levels of maternal exposure to dioxins (from fish and other dietary sources) that do not exceed the provisional tolerable monthly intake of 70 pg/kg body weight established by Joint FAO/WHO Expert Committee on Food Additives (JECFA) (for PCDD, PCDF and coplanar PCB), neurodevelopmental risk for the fetus is negligible. At levels of maternal exposure to dioxins (from fish and other dietary sources) that exceed the provisional tolerable monthly intake, neurodevelopmental risk for the fetus may no longer be negligible. Finally, they observed that there was insufficient evidence for adverse health effects (e.g. endocrine disruption, immunological and neurodevelopmental effects, and cancer) associated with exposure to dioxins from fish consumption⁽⁶⁾. Only a specific fish preparation (Cantonese salted fermented fish) has been identified as being convincingly associated with nasopharyngeal cancer⁽⁶⁴⁾. For example, in France, PCB and dioxins were far below the regulatory thresholds in oysters ( < 0·6 pg/g), mussels ( < 0·6 pg/g) and king scallops ( < 0·4 pg/g), despite of species that filter large volumes of water to extract their food and thus could be excellent bioaccumulators of marine environmental pollutants⁽Reference Guéguen, Amiard and Arnich⁶⁵⁾. However, it is always necessary to consider the exception of certain products from specific regions located around known heavy-point source. Generally, European consumers have higher exposure levels of PCDD/PCDF and dioxin-like-PCB, while American and Asians have relatively higher exposure levels of organochlorine pesticides and PCB. By contrast, all global populations are found to have lower exposure levels of polybrominated diphenyl ethers, which may be attributed to its relatively shorter history of use compared with PCB and organochlorine pesticides⁽Reference Yu, Guo and Zeng⁶³⁾.

Total dietary intake of PCDD/PCDF for the general population of Tarragona County was estimated to be 27·81 pg WHO-toxic equivalents/d established by the WHO in 1998, value notably lower than that found in the 2002 study (63·80 pg WHO-toxic equivalents/d). Fish and seafood were the most important contributors (28 %) to this intake, although it seems quite evident that in recent years the dietary intake of PCDD/PCDF has considerably diminished as a direct consequence of the reduction in the atmospheric emissions of these environmental pollutants⁽Reference Martí-Cid, Bocio and Domingo⁶⁶⁾.

Guéguen et al. ⁽Reference Guéguen, Amiard and Arnich⁶⁵⁾ have also published the benzo(a)pyrene concentration in shellfish (marketed mussels and farmed shellfish) but does not exceed the regulatory European threshold. Martorell et al. ⁽Reference Martorell, Perelló and Martí-Cid¹⁵⁾ have shown an important decreasing trend in the dietary exposure to polycyclic aromatic hydrocarbons (PAH) for the population living in Catalonia and they found that fish and seafood products contributed with 3·6 % to the total PAH food intake in contrast to meat and meat products (49·2 %).

Several international projects have been developed to approach risk–benefit assessment from fish consumption. Among them, Benefit–Risk Analysis of Foods⁽Reference Hoekstra, Hart and Boobis⁶⁷⁾, Benefit–Risk Assessment for Food and Quality of Life-Integrated Benefit and Risk Analysis should be highlighted⁽⁶⁾. Other specific tools have been performed for risk–benefit assessment such as European Food Safety Agency (EFSA) guidelines⁽⁶⁸⁾, disability-adjusted life-year⁽Reference Hoekstra, Verkaik-Kloosterman and Rompelberg⁶⁹⁾, quality-adjusted life-year⁽Reference Ponce, Bartell and Wong⁷⁰⁾, fish risk–benefit assessment by the Institute of Medicine in the USA and quantitative risk–benefit assessment of fish consumption by the USFDA⁽⁷¹⁾. In general, the aim has been to establish diagrams for exposure and dose–response modelling and to compare/estimate following a matrix combining the positive effects or benefits from fish intake (e.g. from n-3 LC-PUFA) and negative effects or risks (e.g. from environmental pollutant) on the common health end points (e.g. child intelligence quotient or mortality), depending on the number of servings per week. Thereby, these matrices allow estimating changes in these end points resulting from the child's mother having consumed fish with different contaminants and essential elements including EPA and DHA contents at different servings per week.

Finally, Table 3 summarises the main health outcomes associated with seafood product consumption including the benefits and risks⁽Reference Oehlenschläger^3, Reference Lund^21–Reference Ryan-Harshman and Aldoori²⁷⁾.

Table 3 Health benefits v. risks derived from regular fish consumption*

OCP, organochlorine pesticides; PAH, polycyclic aromatic hydrocarbons; PCB, polychlorinated biphenyls.

* Based on Oehlenschläger⁽Reference Oehlenschläger³⁾, Lund⁽Reference Lund²¹⁾, Zampelas et al. ⁽Reference Zampelas, Panagiotakos and Pitsavos²²⁾, Panagiotakos et al. ⁽Reference Panagiotakos, Zeimbekis and Boutziouka²³⁾, Bouzan et al. ⁽Reference Bouzan, Cohen and Connor²⁴⁾, He et al. ⁽Reference He, Song and Daviglus²⁵⁾, Manna et al. ⁽Reference Manna, Das and Sil²⁶⁾, Ryan-Harshman & Aldoori⁽Reference Ryan-Harshman and Aldoori²⁷⁾.