Functional Properties of Fish and Fish Products: A Review

Abstract

This article presents a review on the functional constituents of fish and fish products originating from different basins. In recent years, increasing attention has been focused on the significance of polyunsaturated fatty acids in human nutrition. Polyunsaturated fatty acids are classed according to the position of the first double bond in omega-3 polyunsaturated fatty acids and omega-6 polyunsaturated fatty acids. The omega-3 family includes the fatty acids eicosapentaenoic acid and docosahexaenoic acid. The acids eicosapentaenoic acid and docosahexaenoic acid are focused on in this article because of their importance in reducing the risks of cardiovascular disorders. In addition, the article highlights other functional components (essential amino acids, vitamin D₃, selenium) whose levels in fish are higher than in other foodstuffs. The presented data show, that in addition to nutritive effects, fish and fish products contribute to a decreased incidence of diseases. Fish and fish products also contribute to the improvement of certain bodily functions.

Keywords:

• Fish
• Fatty acids
• Selenium
• Vitamin D
• Lysine
• EPA
• DHA

INTRODUCTION

The interest in nutrition as a way to promote health is continually growing in contemporary society. Improper diet is believed to increase susceptibility to civilization-related diseases. According to Finn Holm FoodGroup Denmark,[1] the impact of the improper diet on civilization-related diseases exceeds 30% for cardiovascular symptoms, 35% for cancers, 70% for constipation, 50% for obesity, 25% for type 2 diabetes, and 30% for dental caries. Food studies conducted in Japan, the USA, and in the developed countries of western Europe have proved that many foods have nutritional value as well as health-promoting qualities. Foods with both of these qualities are known as “functional foods.”[2]

A document issued in 1999 by Foods for Special Health Uses—FOSHU[3] adopted the following definition of functional food: “Food will be deemed functional if apart from its nutritive effect, it explicitly demonstrates a beneficial impact on improving the health and general well-being and/or if such food demonstrates reduced susceptibility to diseases.” The features of functional foods must be similar to those of traditional food. Such food must prove its beneficial impact on the human body when consumed in average portions in the ordinary diet. Functional foods must not be administered in the form of pills, capsules, or drops and should integrate into the components of a regular diet. Many scientists believe that functional foods might play particular roles in certain periods of human life. For example, the consumption of some types of food can lead to reduced risk of osteoporosis during menopause in women, or they can reduce the risk of heart disease developing in middle-aged men.[2,4,5]

The following are some examples of food groups classified into functional food categories:[6] (i) products supplemented with omega-3 fatty acids, including eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA); (ii) products supplemented with dietary cellulose; (iii) products supplemented with vitamins (water- or fat-soluble); (iv) products supplemented with mineral constituents (macro- and micro-element groups); (v) products with pro-biotic supplements (e.g., lactic fermentation bacteria); (vi) products with pre-biotic supplements (that stimulate the development of certain bacteria inside the alimentary tract, such as oligosaccharides and polysaccharides).

Furthermore, well-assimilated proteins that are rich in essential amino acids, such as lysine, methionine, or cysteine, are valuable food components because of their nutritive qualities.[7] Fish and fish products are very important for the diet and can be classified as food with functional properties. Fish are a vital food because of their nutritive values and the beneficial impact they have on human health. Fish and fish products contain proteins that are rich in essential amino acids: lysine, methionine, cysteine, threonine, and tryptophan,[8] and micro- and macro-elements: calcium, phosphorus, fluorine, and iodine. In addition, fish contain fats that are valuable sources of energy, and fat-soluble vitamins. The most important contribution from fish are their polyunsaturated fatty acids, particularly those from the omega-3 family. These acids display a number of qualities connected with the improvement of human bodily functions and the reduction in susceptibility to cardiovascular diseases and cancer.[9,10]

Table 1 contains data concerning the EPA and DHA content of a wide variety of fish species, namely, sardine, tuna, anchovy, mackerel, swordfish, hake, salmon, red mullet, sole, herring, sturgeon, sprat, halibut, cod, flounder, haddock, perch, plaice, trout, tilapia, golden bass, pollock, weakfish, croaker, pampano, manhaden, and fish from the Vistula Lagoon. Canned, smoked, salted, and marinated fish products are included in Table 1. This study focuses on the most popular fish species that enjoy the greatest share of the EU market. According to the FAO,[11] the highest fish landings were for salmon, herring, anchovy, tuna, mackerel, pilchard, rainbow trout, and carp. However, the current survey also includes some species caught in local fishing areas. Examples of these species are: Brazilian Manhaden, Alaskan Pollock, and fish from the Vistula Lagoon in Poland. The data collected were used to calculate the amount of fish/fish product that provides 1 g of EPA + DHA. A review of the health benefits of fish consumption and data concerning the EPA + DHA content in a wide variety of fish species show the functional qualities of fish. This can help to promote fish consumption, which is necessary and beneficial to society.

Table 1 Contents of EPA and DHA in fish (wet weight) and daily amounts of fish consumption ensuring supply of 1 g of EPA + DHA

Fish/Fish product	Content of EPA [g/100 g] or [g/3.5 oz]	Content of DHA [g/100 g] or [g/3.5 oz]	Content of EPA + DHA [g/100 g] or [g/3.5 oz]	Amount* necessary for daily supply of 1 g of EPA + DHA [g]	References
Fish
Sardine/Catalonia, Spain/	0.18	0.25	0.43	232.6	101
Sardine	—	—	0.98–1.70	58.8–102.0	21
Sardine	—	—	1.0	100.0	96
Sardine, Brazilian**	0.32	1.07	1.39	71.9	111
Sardine, Mediterranean**	0.86	1.83	2.69	37.2	112
Tuna/Catalonia, Spain/	0.05	0.14	0.19	526.3	101
Tuna, Bluefin	0.4	1.2	1.6	62.5	104
Tuna, Bluefin	0.3	0.9	1.2	83.3	24
Tuna, Albacore	0.3	1.0	1.3	76.9	105
Tuna, Albacore	—	—	0.86	116.3	96
Tuna	0.1	0.4	0.5	200.0	105
Tuna	—	—	0.24–1.28	78.1–416.7	21
Anchovy/Catalonia, Spain/	0.19	0.25	0.44	227.3	101
Anchovy	—	—	2.05	48.8	96
Anchovy, European	0.5	0.9	1.4	71.4	104
Anchovy, Mediterranean**	0.22	0.60	0.82	122.0	112
Mackerel/Catalonia, Spain/	0.45	0.39	0.84	119.0	101
Mackerel, Atlantic	0.9	1.6	2.5	40.0	104
Mackerel, Atlantic	—	—	1.2	83.3	96
Mackerel, King	1.0	1.2	2.2	45.5	104, 105
Mackerel, King	—	—	0.4	250.0	96
Mackerel, Chub	0.9	1.0	1.9	52.6	104
Mackerel	0.9	1.4	2.3	43.5	24
Swordfish	0.1	0.1	0.2	500.0	105
Swordfish	0.1	0.5	0.6	166.7	24
Swordfish	—	—	0.82	122.0	96
Swordfish/Catalonia, Spain/	0.06	0.24	0.30	333.3	101
Hake/Catalonia, Spain/	0.16	0.32	0.48	208.3	101
Hake, Atlantic**	0.06–0.17	0.30–0.45	0.36–0.62	161.3–277.8	108
Salmon/Catalonia, Spain/	1.54	1.10	2.64	37.9	101
Salmon, Atlantic	0.32	1.12	1.44	69.4	107
Salmon, Atlantic	—	—	0.9–1.56	64.1–111.1	21
Salmon, Coho	0.43	0.66	1.09	91.7	107
Salmon	0.3	1.1	1.4	71.4	24
Salmon	—	—	1.0	100.0	96
Salmon, Chnook	1.0	0.9	1.9	52.6	24
Salmon, Baltic	0.54	1.90	2.44	41.0	115
Red mullet/Catalonia, Spain/	0.44	0.27	0.71	140.8	101
Sole/Catalonia, Spain/	0.16	0.21	0.37	270.3	101
Sole, European	Trace	0.1	0.1	1000.0	104
Sole	—	—	0.42	238.1	21
Sole	0.72	0.46	1.18	84.7	109
Sole, Turkey**	0.02	0.08	0.1	1000	110
Herring, Pacyfic	1.0	0.7	1.7	58.8	21, 104, 105
Herring, Atlantic	0.7	0,9	1.6	62.5	21, 104
Herring, Atlantic	—	—	2.0	50.0	96
Herring	0.56	1.23	1.79	55.9	109
Herring, Vistula Lagoon	0.19	0.47	0.66	151.5	114
Herring, South Baltic	0.25	0.82	1.07	93.5	119
Sturgeon, Atlantic	1.0	0.5	1.5	66.7	104
Sprat	0.5	0.8	1.3	76.9	104
Sprat, South Baltic	0.88	2.05	2.93	34.1	115
Halibut, Greenland	0.5	0.4	0.9	111.1	21, 104
Halibut, Pacific	0.1	0.3	0.4	250.0	21, 105
Halibut	—	—	0.47	212.8	96
Cod, Atlanic	0.1	0.2	0.3	333.3	105
Cod, Atlanic	—	—	0.16	625.0	96
Cod, Pacyfic	—	—	0.13	769.2	21
Cod (Gadus morhua marsi-albi)	0.3	0.76	1.06	94.3	109
Cod	Trace	0.1	0.1	1000	24
Flounder	0.1	0.1	0.2	500.0	105
Haddock	0.1	0.1	0.2	500.0	21, 105
Perch, Ocean	0.1	0.1	0.2	500.0	105
Place, European	0.1	0.1	0.2	500.0	105
Snapper, Red	Trace	0.2	0.2	500.0	106
Trout	—	—	0.93	107.5	96
Trout, rainbow	—	—	0.84	54.3	21
Trout, rainbow	0.17	0.42	0.59	169.5	107
Trout, sea, Norway	0.38	1.03	1.41	70.9	109
Trout, sea, Siberia	0.28	1.18	1.46	68.5	109
Tilapia, Brazilian**	0.1	—	0.1	1000	111
Picarel, Mediterranean**	0.27	0.55	0.82	121.9	112
Bass Golden, Gulf of Mexico	—	—	0.9	111.1	96
Bass Golden, Atlantic	—	—	0.9	111.1	96
Bass, Vistula Lagoon	0.03	0.15	0.18	555.6	114
Pollock, Alascan	—	—	0.47	212.8	96
Menhaden, Brazilian	1.24	1.55	2.79	35.8	113
Weakfish, king	0.03	0.08	0.11	909.0	113
Croaker, white	0.07	0.11	0.18	555.6	113
Pampano, Brazilian	0.14	0.52	0.66	151.5	113
Burbot, Vistula Lagoon	0.03	0.11	0.14	714.3	114
Bream, Vistula Lagoon	0.16	0.19	0.35	285.7	114
Roach, Vistula Lagoon	0.05	0.16	0.21	476.2	114
Pikeperch, Vistula Lagoon	0.02	0.11	0.13	769.2	114
Eel, Vistula Lagoon	0.71	1.45	2.16	46.3	114
Fish products
Canned sprat in tomato sauce	0.19	0.24	0.43	232.5	88
Canned sprat in oil	0.62	1.04	1.66	60.2	88
Canned herring in tomato sauce	0.29	0.41	0.70	142.9	88
Canned herring fillets in oil	0.79	1.10	1.89	52.9	88
Canned tuna in oil	0.04	0.21	0.25	400.0	88
Canned tuna in oil	0.01	0.14	0.15	666.7	116
Canned tuna in oil	Trace	0.2	0.2	500.0	24
Canned tuna in water	0.09	0.16	0.25	400.0	116
Canned tuna in water	0.2	0.6	0.8	125.0	24
Canned mackerel in tomato sauce	0.30	0.60	0.90	111.1	88
Canned mackerel fillets in oil	0.65	1.15	1.80	55.6	88
Canned sardine in oil	0.85	0.98	1.83	54.6	88
Canned sardine in oil	1.2	1.24	2.44	41.0	116
Canned salmon	0.9	0.8	1.7	58.8	24
Smoked mackerel	1.11	1.83	2.94	34.0	31
Smoked mackerel	1.0	1.7	2.7	37.0	116
Smoked sprat	0.97	1.45	2.42	42.0	31
Smoked herring	0.32	0.39	0.71	142.0	31
Smoked herring	1.03	0.45	1.48	67.6	116
Smoked Baltic salmon	0.55	1.39	1.94	52.0	31
Smoked Norwegian salmon	0.88	1.13	2.01	50.0	31
Salted herring fillets	0.63	0.72	1.35	74.0	31
Salted herring fillets	0.96	0.89	1.85	54.1	116
Marinated herring fillets	0.72	0.73	1.45	68.0	31
Marinated herring	0.7	1.11	1.81	55.3	116
Fish burger	−	−	0.55	181.8	96
Anchovy oil	14.3–23.3	4.6–12.5	18.9–35.8	2.8–5.3	103
*Calculated by the author.
**Calculated according to Exler et al. (1975).[102]
Recommended Total Daily Intake of EPA + DHA (Kris-Etherton et al., 2002):[21]
0.3–0.5 g: Recommended daily intake in the prevention of cardiac diseases.
1 g: Recommended daily dose in patients with cardiac disease history.
2–4 g: Recommended in patients who require reduced triglyceride levels (controlled by the physician).

SELECTED CONSTITUENTS AND FUNCTIONAL ROLES OF FISH AND FISH PRODUCTS

Polyunsaturated Fatty Acids

The essential difference between fish fats and other animal or vegetable fats is the high level of polyunsaturated fatty acids (PUFAs) in fish. PUFAs are classed according to the position of the first double bond in omega-3 PUFAs and omega-6 PUFAs. Among the fatty acids in fish are docosahexaenoic acid (C22:6, n-3, DHA) and eicosapentaenoic acid (C20:5, n-3, EPA). EPA and DHA are omega-3 family acids. In fact, fish fats are the basic source of these acids in the human diet, although nuts and some vegetable oils contain considerable amounts of another omega-3 family acid: α-linolenic acid (C18:3, n-3, ALA). PUFAs also include omega-6 family acids. According to many scientists,[12–15] the prophylactic activity of fatty acids is determined not only by the PUFA's level, but in addition it is a function of the omega-3 to omega-6 acids ratio. This ratio should be 0.2, based on an average daily consumption of roughly 8 g of essential unsaturated fatty acids (EUFA). Because of the consumption of significant amounts of vegetable oils and animal fats, the omega-3 to omega-6 proportion is considerably lowered to about 0.04 in the average diet of people from the Americas and western Europe.[16] Given that omega-3 and omega-6 acids compete in metabolic transformations in the human body, health benefits will improve if the intake of omega-6 acids is reduced and the consumption of omega-3 acids is increased. Current results indicate that there are two strategies for reducing the risk of coronary heart disease (CHD). The first is to replace saturated fatty acids and fatty trans-acids with cis-mono- and polyunsaturated acids, and the second is to increase omega-3 fatty acids intake from vegetable and fish sources or, alternatively, to use nutraceultical supplements. When combined, these two strategies can lead to achieving great cardiac benefits through a fatty acid dietary regime.[17,18]

According to the European Food Safety Authority (EFSA),[19] the ratio of omega-3 to omega-6 acids fluctuates from 1.3 (carp) to 21.2 (herring) in eight fish species (rainbow trout, salmon, tuna, herring, mackerel, pilchard, anchovy, carp) that are consumed in the largest quantities in EU countries. Hence, increasing fish consumption in the diet might contribute significantly to increased omega-3 acids intake and to the optimization of EPA and DHA utilization for the improvement of different body functions.

Specific interest in omega-3 acids has been increasing since researchers observed that the Inuit people from Greenland hardly suffered from cardiovascular diseases (CVD). The Inuit diet contains mainly fat fish and sea animals with, among other qualities, high levels of EPA and DHA.[20] Without a doubt, the data obtained in epidemiological and experimental studies support the beneficial activity of omega-3 acids in the prevention of CVDs. In 2002, the American Heart Association (AHA) issued a declaration approving the use of omega-3 acids for both the primary and secondary prevention of CVDs.[21]

EPA and DHA belong to the group of essential dietary constituents. Since the human body is not itself capable of synthesizing these compounds in amounts necessary to ensure good health, they have to be supplied to humans and animals by the food they ingest.^[21] The intake of food-origin omega-3 and omega-6 acids varies among populations.[22] The most wide-ranging database concerning alimentation in America (NHNES III) states that the medians of EPA + DHA and ALA intakes are 0 and 1 g/day, respectively—US Department of Health.[23] The proportion of omega-6 to omega-3 acids intake is estimated at 20–25:1 in the contemporary, western diet. Palaeolithic people consumed foods rich in omega-3 acids, at an estimated proportion of omega-6 to omega-3 of 1:1.[16] Such a dramatic nutritional shift results from the relative decrease in fish consumption. In addition, today, the share of omega-3 acids in meat and fish is lower compared to the past. The use of commercial fodder containing high levels of omega-6 acids and low levels of omega-3 acids is the underlying reason for the present low level of omega-3 acids in meat and farmed fish. Even cultivated vegetables are poorer in omega-3 acids than are plants that grow in the natural environment.[24]

Fish and fish products contain fats whose proportions of omega-6 to omega-3 acids are much below the recommended values of about 5.[12–14] From a nutritional point of view, this is favorable and very desirable, as it improves the proportions of the omega-3 to omega-6 acids in the total human daily diet. Proportions of these acids in other food products highly exceed the recommended levels. For example, in animal fats omega-6 to omega-3 ratio is 10 to 20 at a very low level of EUFAs, whereas in vegetable oils it is from 15 up to as high as 200.

Many surveys done in large population groups have demonstrated the favorable activity of omega-3 acid-rich fish fats. Positive effects accompanying the recommended intake of EPA and DHA acids in the form of fish food were observed. These acids help to reduce triglyceride levels, the risk of sudden lethal cardiac death, heart attacks, abnormal cardiac rhythms, and cardiovascular diseases as well as suppressing the evidence of atheromatous plaques, slightly reducing blood pressure, and supporting immunity to inflammatory conditions. Furthermore, they stimulate favorably the functions of the nervous system, brain, and memory. Similar effects have been reported in the case of α-linolenic acid; however, the scientific evidence is incomplete. Hence, apart from their unquestionable nutritional value, fish, in particular fatty fish, comply with all the requirements of functional foods—FOSHU,[3] since they reduce the incidence of some diseases and strengthen certain bodily functions. It is important to note that high doses of EPA and DHA might have the detrimental impact of reducing blood coagulation capacity and increasing the risk of possible hemorrhage. Presented below are the main benefits, as supported by scientific evidence that result from the consumption of fatty fish.

Reduction in Triglyceride (TG) Blood Levels

There is convincing scientific proof from research conducted on human patients that the omega-3 acids (specifically EPA and DHA) contained in fish fat reduce triglyceride blood levels considerably.[16,25] This depends on the dose, which should not be lower than 2 g of omega-3 acids per day; higher doses will yield better results. For instance, 4 g per day can reduce the triglyceride levels by 25 to 40%. The results of EPA and DHA effects in the treatment of hypertriglyceridemia are similar in patients with or without a history of diabetes and in nephric dialysis patients. Researchers were anxious about the presumed impact of omega-3 acids, which were supposed to increase the low-density lipoprotein-related cholesterol (LDL-C) levels and the potential of lipid oxidation. Today, such concerns seem baseless since there is sufficient evidence of the protective action of omega-3 fatty acids on the heart.[26,27] Studies have demonstrated that omega-3 fatty acids may incite a slight increase (by about 1–3%) in high-density lipoprotein-related cholesterol (HDL-C). Yet, in most patients examined the impact of omega-3 acids on HDL-C levels did not seem to play an important role in the reduction of cardiovascular hazards.[28] Other surveys described by Jakobsen[29] showed that the administration of omega-3 acids in doses ranging from 0.8 to 5.4 g per day resulted in a reduction in TG levels by 27 mg/dl, an increase in HDL-C levels by 1.6 mg/dl, and an increase in LDL-C levels by 6 mg/dl. It should be underscored, however, that the positive effects of omega-3 fatty acids, including EPA and DHA, result not as much from the modified lipid profile as from the change in the composition of the cell membranes (enrichment of cell membrane phospholipids in EPA and DHA).[30] Such cell membrane changes clearly explain the counteracting role of omega-3 fatty acids, including EPA and DHA, in the case of arrhythmia, hypotension, deposition of atheromatous plaques, and inflammatory conditions. Omega-3 fatty acids, including EPA and DHA, also have a positive impact on endothelium functions and on the activity of the autonomous system.[29]

In its report from 2003, the American Heart Association (AHA) recommended that a daily administration of 2–4 grams of EPA + DHA (e.g., 68 to 136 g of smoked mackerel or 100 to 200 g of smoked Norwegian salmon a day)[31] could reduce triglyceride levels by 20–40%.[32] However, taking into account the increased risk of hemorrhage attributable to omega-3 acids administration, especially at doses exceeding 3 g per day, a doctor should be consulted prior to commencement of treatment.

Secondary Cardiovascular Disease Prevention

A number of randomized clinical trials have surveyed the function of omega-3 fatty acids in the secondary prevention of cardiovascular diseases. In the Diet and Reinfarction Trial (DART), 2,033 male patients with a history of cardiac infarction were randomly selected to increased their dietary intake of fish (200–400 g of fatty fish per week, which corresponds to 500–800 mg/day of omega-3 fatty acids). The survey showed a 29% reduction in all the causes of death.[33] The best benefits were observed in the prevention of lethal myocardial infarction.[34] Italian researchers who conducted surveys on a test group of 11,323 men who had suffered a heart attack less than three months before the study, obtained similar results. The study applied EPA + DHA acid supplementation at doses of 850 mg/day; the general death rate dropped by 21%. The rate of sudden death resulting from cardiac infarction was lower by 45% compared with the control group—GISSI—Prevenzione Investigators.[35]

The beneficial effects of administrating omega-3 PUFAs in the prevention of atrial fibrillation (AF) were demonstrated in patients who had coronary artery bypass graft surgery. Supplementation of 850 to 882 mg omega-3 PUFAs for five days prior to surgery and in the post-surgery period, resulted in a decreased number of AF episodes (by 54.4%) as well as a shortened hospitalization period.[36] In its 2003 recommendations, the AHA suggests that patients with cardiac diseases should take about 1 gram of EPA and DHA every day. This can be achieved by consuming fatty fish, such as 34 g of smoked mackerel daily.[31]

Primary Cardiovascular Disease Prevention

A number of epidemiological and survey data concerning primary prevention (in patients without histories of cardiac infarction) indicate that there is a considerable reduction in the cardiovascular death rate in people who eat fish on a regular basis. A scientific survey conducted by Stone[37] demonstrated that men who ate even small amounts of fish every week displayed a reduced mortality rate connected with coronary heart disease (CHD) as compared with men who did not eat fish at all. Decreased general mortality rates, CHD-induced mortality, and CHD incidence was observed in the following studies: (i) the Chicago Western Electric Study conducted on a test group of 1,822 male patients;[38] (ii) the Nurses' Health Study conducted on a test group of 84,688 female patients. The results indicated that consumption of fatty fish containing considerable levels of EPA and DHA; 1 to 3 times a month, once a week, 2–4 times a week, and more than 5 times a week decreased the CHD-induced mortality risk by 21, 29, 31, and 34%, respectively, compared with women who ate fish less than once a month;[39–41] (ii) the EUROASPIRE study on a group of 415 patients (285 men, 130 women) also indicated that consuming fish rich in ALA, EPA, and DHA results in lowered overall mortality and lowered CHD-induced mortality in comparison with patients whose diets are poor in fish.[16]

Rice[42] reported that the consumption of two fish meals a week would decrease cardiovascular mortality rate, roughly by 30–40%. Furthermore, studies conducted in the USA on a group of more than 20,500 female patients demonstrated that consumption of more than one fish meal a week was correlated with a decrease in the cardiac infarction-induced mortality rate by 52% compared to women who did not eat fish at all.[20] The surveys of US Physicians' Health conducted on a test group of 20,551 male patients demonstrated a reduction in the general mortality rate and in the incidence of sudden cardiac deaths. In the studies, no reduction in deaths other than sudden deaths in the course of CHD and no cardiac infarction deaths were observed.[43]

There are epidemiological surveys that do not confirm the positive effects of EPA and DHA on primary cardiovascular disease prevention.[44] The evidence suggesting the benefits of regular consumption of fatty fish, however, is convincing. Prior to any final conclusions about such benefits, well-designed randomized studies that classify people into applicable cardiac disease susceptibility categories, are required.[45] In 2003, the AHA suggested that all adults should eat fish at least twice a week.[46] Specifically recommended are fatty fish species such as mackerel, brown trout, herring, sardine, tuna, and salmon. The recommended preventive dose of EPA + DHA for the reduction of cardiovascular disease risk is 500 mg/day.

High Blood Pressure Reduction

Most surveys in human patients did not confirm a substantial reduction in blood pressure as a consequence of omega-3 acids intake.[47] The decrease is usually 2–5 mm Hg, but there can be more of a decrease when higher blood pressures are taken into account. Better results might be achieved with increased doses of omega-3 acid,[47] and DHA might be more effective than EPA.[48] However, suitable clinical effects might require an intake of more than 3 g of omega-3 acids per day. Since such high doses might increase the risk of hemorrhage, a physician should be consulted about the proper dosage.[21]

Inhibition of Blood Coagulation

One of the ways omega-3 fatty acids have a protective impact on the cardiovascular system is to inhibit blood coagulation. The production of coagulation-stimulating A₂ thromboxane eicosanoide is inhibited by EPA in the process of cyclooxygenase bonding, which is competitive to arachidonic acid bonding. Furthermore, omega-3 acids inhibit the adhesion and aggregation of thrombocytes as well as the production of B₂ thromboxane, which is another coagulation-stimulating cytokine.[49]

Decreased Risk of Cancer Incidence

A survey conducted in Sweden on more than 60,000 women aged 40–76 demonstrated that the incidence of kidney cancer in women who ingested fatty fish (rich in EPA and DHA) at least once a week, would decrease by 74% within 10 years as compared to that of women who did not eat fish at all.[50] The survey conducted by Norat et al.[51] demonstrated that the incidence of rectal (colorectal) carcinoma in patients who consume fish was considerably lower than that in patients who ate no fish but only red meat. English et al.[52] obtained similar results in their study.

Rheumatic Arthritis

Many randomized tests demonstrated decreased morning arthralgia with the regular intake of fish oil supplements. To date, studies of the effects of fish oils on rheumatic arthritis have lasted for periods no longer than 3 months.[53] The benefits noted are comparable to those of anti-inflammatory drugs, such as ibuprofen or aspirin. The confirmation of any positive benefits in patients with rheumatic arthritis from the ingestion of fish oils will require longer studies; no three-month experimental study can yield unambiguous results.

Prevention Subsequent to Organ Transplantations

The studies made focused on the examination of many patients who were administered fish oil supplements after heart or kidney transplantations. An improvement in renal functions occurred in a majority of these cases[54] along with decreased hypertension, compared with patients who were not supplied with the fish oil supplements. Although there are other studies that did not demonstrate any renal improvement,[55] most scientific evidence supports the beneficial effects of fish oils for renal functions. No changes in transplant rejection or assimilation have been observed.

Arteriosclerosis and Atheromatosis

Certain studies indicated that the regular intake of fish or fish oil supplements can reduce the risk of atheromatous plaque deposits on the internal walls of coronary arteries,[56] and yet there are other studies that do not confirm this.[57] Nonetheless, evidence of the counter-atheromatosis properties of fish oil supplementation prevails. More studies are needed before any key conclusions are drawn in this area.

Improvement of Some Bodily Functions

Many studies indicate that the benefits of n-3 PUFAs for health and general well being result not only from the reduced risk of cardiovascular disease and reduced risk of cancer incidence,[58,59] but also from the improvement of some other bodily functions that are essential for women during pregnancy or lactation, and in small children. The improvement of bodily functions is reflected in the optimal development of the nervous system. Low consumption of EPA and DHA (the main dietary sources are fish and fish products) during pregnancy leads to low levels of these acids in newborns. Deficiencies in these acids, specifically of DHA, leads to a number of nervous system disorders, and can also result in irreversible and adverse changes in brain cells.[60–64]

The improvement of bodily functions can be seen in the reduction of inflammatory symptoms as well as the prevention of abnormal mental and psychological development and prevention of visual acuity disorders. There is well-documented evidence of the positive impact of omega-3 acids on a reduction in the risk of atopic dermatitis, rheumatic arthritis, and ulcerative inflammation of the colon as well as attenuation of symptoms of such diseases. Insufficient consumption of fish and the related poor intake of DHA leads to the substitution of omega-3 with omega-6 acids in the phospholipids. This phenomenon produces unfavorable modifications in the proportion of omega-6/omega-3 acids, which in turn produces impairment of visual function in newborns.[20,61,65–67] It was demonstrated that increased DHA food levels attenuated unfavorable symptoms significantly.[66]Jorgensen et al.[68] demonstrated a correlation between food consumption and better visual acuity in children. Further studies proved that children whose mothers had consumed four fish meals a week during pregnancy demonstrated higher brain development rates at 18 months of age compared with children of women who had not eaten fish at all.[41,68] The analysis of studies on the significance of fish and the applicable significance of omega-3 family fatty acids suggested that lower consumption of these could lead to the occurrence of many disorders in children. These disorders include impulsive behaviors, hyperactivity, learning disabilities, speaking disorders, motor activity disorders, ADHD (Attention Deficit Hyperactivity Disorder), lack of normal brain development, and the subsequent decline in IQ.[42,64,66,69,70] A study conducted among boys aged 6 to 12 demonstrated that low blood levels of EPA and DHA were linked with problems, such as aggression, trouble falling asleep, and bad moods. Increased consumption of fish and fish products that included omega-3 acids decreased the incidence of these symptoms. Most important, an increase in omega-3 acids in the diet reduced to a minimum the hostile attitude of the children in their surroundings. Studies conducted in Japan demonstrated that 1.5 to 1.8 g DHA per day reduced frustration and anger in children considerably.[63]

Impact on the Attenuation of Allergic Symptoms, Asthma, and Eczema

Studies conducted by Sausenthaler et al.[71] demonstrated that children whose mothers had consumed large amounts of fish during pregnancy had considerably lower occurrences of eczema in the first years of life. Kull et al.[72] conducted similar studies in 4,089 newborns in Stockholm. The results indicated that children whose diet was supplemented with fish in the first year of life demonstrated reduced incidences of asthma, eczema, allergies, and allergic rhinitis compared with children who did not receive fish in their diet. Reduced risk depends on the amounts of fish and fish product consumption. Stronger correlations were observed in children who consumed fish and fish products more than twice a month compared with children who consumed such foods on a less frequent basis.[72]

Salam et al.[73] noted that the degree of fish and fish product consumption decreased the incidence of asthma in children. The authors of the study clearly confirmed that the consumption of fatty fish at least once a month was inversely proportional to asthma incidence in children. On the other hand, the authors found that a higher risk of this disease occurred in children who consumed fish sticks. This is because fish sticks are manufactured with low-fat fish containing minute amounts of omega-3 acids. Moreover, the manufacturing process requires the addition of vegetable oil that contains substantial amounts of omega-6 acids. This addition increases the omega-6 to omega-3 acids proportion unfavorably. Additionally, industrial deep fats used for frying contain fatty trans-acid isomers that are detrimental to health.[73]

Essential Amino Acids

Fish and fish products are valuable sources of easily digestible proteins (having more than 95% digestibility),[7] which are in the group of the most important and crucial food constituents. Amino acids are fundamental components of proteins. Nine amino acids are classified as essential. Human beings and other mammals are not capable of synthesizing these amino acids, which means that the amino acids have to be ingested with foods.[74]

The amino acid composition of the standard protein was modified in 1991 by a committee of experts at the FAO/WHO[75] who took into consideration the latest research in this field. The composition appears to be the optimum measure of protein quality in the nutrition for all groups of the population. In order to define protein quality, the term “limiting amino acid,” must be defined first. It is an essential amino acid that occurs in certain food proteins in the smallest amounts, compared with standard protein. This amino acid limits the optimal utilization of other food amino acids in the process of systemic protein synthesis.[76] Examples of limiting amino acids are lysine, methionine, and cysteine. These amino acids (expressed in milligrams of amino acid per gram of protein nitrogen) are present in fish and fish products, generally in larger amounts than in the FAO[75] standard protein. Fish and fish products are particularly good sources of lysine.

Given that proteins contained in cereals are poor in lysine, cereals should be supplemented with fish products whose protein contains excessive amounts of this amino acid in comparison with standard proteins.[7] This permits better utilization of food proteins by the body. The role of lysine in the human body can be defined as follows:[77,78] (i) it is essential for protein build-up, mainly in muscles and bones; (ii) it absorbs calcium and improves mental concentration; (iii) it relieves the symptoms of common colds and influenza; (iv) it is necessary for the production of hormones, antibodies, and enzymes; (v) deficiency of it causes fatigue and irritation, anemia, and hair loss.

Vitamin D₃

Fish, fish liver, and fish-liver oil are the most significant sources of vitamin D₃ (cholecalciferol).[79,80] Vitamin D₃ is necessary for regular calcium and phosphate management by humans and animals and its deficiency is the underlying cause of rachitis in children. An insufficient supply of cholecalciferol causes the body to excrete phosphates in inadequate amounts. This phenomenon leads to hypocalcaemia because phosphates are responsible for blood calcium binding.[81,82] Consequently, increased bone resorption and osteoporosis are observed.[81–83] Susceptibility to bone fractures increases in connection with bone structure deterioration resulting from deficient vitamin D₃, which is particularly apparent in elderly people. A sufficient vitamin D₃ supply is also indispensable for teenagers when they experience periods of intense development and bone mass accumulation.[84]

Studies conducted over the past 20 years have demonstrated that vitamin D₃ deficiency can increase the risk of some cancers, such as that of the colon, prostate, breast, or esophagus,[81,85] as well as of some auto-immunological diseases, such as multiple sclerosis, chronic rheumatic arthritis, or insulin-dependent diabetes type I.^[85] Vitamin D₃ is a unique food component that plays many health-friendly roles. It is the only vitamin produced by the cutis cells under the impact of solar radiation.[86] This is why a dietary supply of vitamin D₃ is extremely important for people who live in areas with very limited access to UV radiation.[83,85] Relying on solar radiation as the only source of vitamin D₃, however, can lead to variable cholecalciferol levels in the body, which is detrimental to the health.[86] Hence, including fish and fish products rich in vitamin D₃ in the diet can provide considerable health improvement specifically in areas where solar insolation is poor.

Mineral Constituents

Mineral constituents are defined as groups of compounds that are classified as essential, and these elements must be supplied in suitable amounts and proportions with ingested foods. Fish and fish products are very good sources of some macro- and micro-elements, which both play important roles in the human body. From a functional point of view, the most important mineral constituents found in fish and fish products in considerable amounts are calcium and phosphorus (macro-elements) and iodine, fluorine, and selenium (micro-elements).[31,87,88]

Their functions can be described as follows:[89] (i) calcium: (a) takes part in the process of the osseous system and tooth tissue construction; (b) in combination with phosphorus it increases bone resistance; (c) takes part in the processes of blood coagulation; and (d) conducts nervous system pulses; (ii) phosphorus: (a) takes part in the process of cell regeneration; (b) improves the condition of gums and teeth; (c) takes part in growth processes; and (d) regulates blood pH; (iii) selenium: (a) fosters normal function in enzymatic systems; (b) protects red blood cells and cellular membranes from the impact of free radicals; (c) prevents undesirable oxidation processes; (d) deficiencies might be a reason for cancer;[90] (iv) fluorine: (a) helps keep teeth in good condition; (b) fosters normal function of the skeletal system; (v) iodine: (a) fosters normal function of the thyroid gland; (b) supports normal physical and mental development in the period of pubescence; (c) supports normal development of reproductive functions.

Functionally Essential Components in Fish and Fish Products

Given the considerable amounts of components listed in point 2 above, fish and fish products can be classified as functional food according to the 1999 FOSHU definition,[3] since apart from their nutritional qualities they make positive contributions to improving health and overall well being. A survey of the EPA and DHA content in various fish species and fish products is presented in Table 1, while that of selenium, lysine, and vitamin D₃ is in Table 2. Apart from the above, Table 1 shows the quantity of fish and fish products that contain the amounts of EPA and DHA recommended in cardiovascular disease prevention. The tables also contain the recommended doses of nutritive components necessary to ensure proper body functioning.

Table 2 Contents of selenium, vitamin D₃, and lysine in selected fish species and fish products

Fish/Fish product	Selenium [μg/100 g]	References	Vitamin D3 [μg/100 g]	References	Lysine [mg/100 g]	References
Fish
Anchovy	68.0	96	—	—	—	—
Cod, Atlantic	38.0	96	—	—	—	—
Cod, Balic Sea	—	—	6.9	117	1772	116
Cod	—	—	2.0	118	—	—
Cod	—	—	7.0	79	—	—
Golden bass, Gulf of Mexico	52.0	96	—	—	—	—
Golden bass, Atlantic	52.0	96	—	—	—	—
Fish burger	17.0	96	—	—	—	—
Halibut	47.0	96	—	—	1443	116
Herring, Atlantic	47.0	96	15.4	79
Herring, Baltic	—	—	17.1	117	1297	116
Mackarel, Atlantic	52.0	96	—	—	1491	116
Mackarel, King	47.0	96	—	—	—	—
Pollok, Alaska	43.0	96	—	—	1320	116
Salmon	46.0	96	24.5/12.4	79, 118	1742	116
Sardines	53.0	96	—	—	2063	116
Trout	15.0	96	9.3	118	1528	116
Tuna, Skipjack	80.0	96	7.2	79	—	—
Tuna, Albacore	66.0	96	4.1	118	2107	116
Bream, Baltic Sea	—	—	13.8	117	—	—
Perch, Baltic Sea	—	—	2.3	117	1908	116
Pike, Baltic Sea	—	—	4.7	117	1471	116
Pike, Lake Saimaa	—	—	4.1	117	—	—
Pikeperch, Baltic Sea			24.5	117	1528	116
Trout, rainbow	—	—	7.6	117	—	—
Vendace, Lake Saimaa	—	—	24.5	117	—	—
Whitefish, Baltic Sea	—	—	12.2	117	—	—
Whitefish, Lake Saimaa	—	—	44.4	117	—	—
Bluefish	—	—	10.4	118	—	—
Swordfish	—	—	11.1	118	—	—
Eel			25.6	79	1045	116
Sole	—	—	—	—	1605	116
Fish products
Smoked salmon	17.9	31	11.0	31	1333/1920	7, 116
Smoked mackarel	22.2	31	3.1	31	1655/1570	7, 116
Smoked herring	21.8	31	15.8	31	1734/1680	7, 116
Smoked eel	—	—	—	—	1708	116
Smoked sprat	20.0	31	11.9	31	1640	7
Smoked trout	12.9	31	5.9	31	2040	7
Salted herring	12.6	31	2.4	31	1545/1140	7, 116
Marinated herring	16.3	31	0.9	31	1986/1370	7, 116
Canned sprat in oil	14.7	88	10.4	88	1360	7
Canned herring in tomato sauce	12.8	88	0.8	88	1091/990	7, 116
Canned tuna in oil	29.0	88	0.9	88	2626/1666	7, 116
Canned mackerel in oil	14.9	88	3.0	88	1552	7
Canned sardine in oil	25.5	88	2.9	88	1963/1700	7, 116
Recommended Total Daily Intake (TDI):
Selenium: 65 μg/day in adults (Śmigielska, H.; Lewandowicz, G.; Gawędzki, J. Biopierwiastki w żywności. Przemysł spożywczy 2005, 7, 28–32).
Vitamin D3: 5 μg/day in adults; 10 μg/day in children (FAO/WHO. Handbook of nutritional requirements. FAO/WHO: Rome, 1988).
Lysine: 9.4 mg/kg body weight; 660 mg/70 kg body weight (according to Gawędzki, J. ed. Białka w żywności i żywieniu. Poznań 1997).

Among the fish species listed in Table 1, the highest EPA and DHA levels occur in Baltic sprats, Mediterranean sardines, Atlantic mackerel, Baltic salmon, and Atlantic herring. Just two meals of 150 g of Baltic salmon a week provide the quantity of EPA and DHA that is recommended for the prevention of cardiovascular diseases. The levels of EPA and DHA acids in fish products are dependent on the fish species used in the manufacturing process, thus, sprat, mackerel, and salmon products, which contain the highest quantities of these acids, can be recommended.

Fish and fish products are rich in essential amino acids, including primarily lysine. In order to meet the recommended daily lysine intake, a consumer who weighs 70 kg should eat between 25 g and 65 g of fish or fish products that are listed in Table 2. Of the fish species listed in Table 2, whitefish, eel, vendace, salmon, and pike-perch have relatively high contents of vitamin D₃. For instance, the adult recommended daily dose of this vitamin is met by consuming between 20 and 40 g of salmon per day. Furthermore, fish is a good source of selenium, and the adult daily requirement for this micro-element can be met by consuming 100 g of tuna or anchovy (Table 2). Similar selenium levels are reported for sardines, Atlantic mackerel, and Golden bass.

Contaminants in Fish

Although the current survey is devoted to the health benefits resulting from fish consumption, it is well known that fish, especially fatty fish, can contribute significantly to dietary exposure to contaminants. Some of these contaminants are methylmercury (MeHg), persistent organochlorine compounds, brominated flame retardants, and organotin compounds. The most important of these are MeHg, polychlorinated dibenzo-p-dioxins, dibenzofurans (PCDD/Fs), and dioxin-like polychlorinated biphenyls (DL-PCBs). Therefore, there is concern that high level consumers of certain fish might exceed the provisional tolerable weekly intake (PTWI) even without taking into account other sources of dietary exposure. Such excessive exposure, if repeated frequently, is undesirable and can pose health risks. On the other hand, eating meat instead of fish will not necessarily decrease exposure to dioxin-like compounds.

The current article focuses on fish that are widely available in the EU, and those that will likely be consumed most frequently. Of these, the highest levels of MeHg are found in tuna and other top predatory fish that are mostly caught in the wild. According to the EFSA, the fish with the highest levels of PCDD/Fs and Dl-PCBs are Baltic salmon and Baltic herring. Frequent consumers of wild Baltic salmon are more likely to exceed the PTWI for PCDD/F and DL-PCBs than other consumers of fatty fish.[19] However, spatial variation in contaminants in fish from the Baltic Sea has been observed.[91,92]

Investigations conducted in Poland[31,88] indicated that fish products available on the Polish market contained low levels of MeHg. The highest levels of PCDD/Fs and dl-PCBs were observed in smoked Baltic salmon and smoked sprat.^[31] These products should be avoided by pregnant or nursing women and young children. Research on PCDD/Fs and dl-PCBs in fish caught in the southern part of the Baltic Sea (Polish Catch Area) indicated that the highest levels of contaminants, which exceeded the permissible limits established by the EU, were detected in salmon samples. Some sprat samples also exhibited elevated levels of these contaminants.[92] Other fish, such as herring and other fish products from the Polish market, were not hazardous for consumers, and their nutritional composition should encourage increased consumption.

Sidhu[93] estimated the potential health risks related to carcinogenic contaminants (e.g., PCDD/Fs, dl-PCB, etc.) in fish using the U.S. EPA-approved cancer risk assessment guidelines. The potential health risk estimates were evaluated by comparing them with the acceptable excess risk level range of 10⁻⁶–10⁻⁴. Risk estimates in humans for carcinogenic environmental contaminants in contaminated fish at the State of Michigan, USA, Trigger Levels (e.g.,10 ppt for PCDD/Fs), ranged from an excess risk level of 3 × 10⁻⁶–9 × 10⁻⁴. These risk estimates met the acceptable excess risk level criteria. Therefore, the consumption of fish in accordance with the State of Michigan, USA Fish Advisory Guidelines is safe and should be encouraged. The top 11 most popular fish species (e.g., sardines, mackerel, Atlantic and Pacific herring, lake trout, Chinook, Atlantic, and Sockeye salmon, European anchovy, sablefish, and bluefish) provide an adequate amount of omega-3 PUFAs (2.7–7.5 g/meal) and met the nutritional recommendations of the American Heart Association.

Based on a review of various reports, Santeree[94,95] demonstrated that the regular consumption of 227 g of salmon per week for 70 years could increase the risk of cancer deaths by 6,000 (in the entire American population of 300 million), due to the presence of methyl-mercury and organic chlorine compounds. For the purpose of comparison, and in light of the fact that the same diet supplies the recommended dose of 1 g per day of EPA and DHA, the risk of sudden death resulting from coronary heart disease is reduced by 20–40%, and according to the American Heart Association (AHA) in 2003, this applies to 50,000 to 100,000 Americans. Similar conclusions were drawn by Mozaffarian and Rimm,[96] who stated that the consumption of fish (1–2 rations per week) rich in EPA and DHA can reduce the risk of death from cardiac disease by 36%, and can reduce the general mortality rate by 17%. These authors concluded that the benefits of fish consumption considerably exceed the possible risks connected with the presence of dioxins and poly-chlorinated biphenyls. The same applies to nursing women provided they consume selected fish species.

Scientific data indicate that the consumption of fish oil containing omega-3 PUFAs reduces the risk of coronary heart disease, decreases mild hypertension, and prevents certain cardiac arrhythmias and sudden death. However, two conflicting views regarding the importance of fish oil consumption are presented in the international literature. The main themes of the discussion are the benefits for consumers and the risk posed by contamination. Although there is wide-ranging acceptance within the scientific community of the principles for determining guidelines for basic health, the interpretation of results of such evaluations can differ significantly depending on the approaches of particular nations. Moreover, at present there is no agreed methodology for a quantitative comparison of human health risk and benefits stemming from fish oil consumption. The EFSA Panel recommends developing just such a consistent and approved methodology.[19]

CONCLUSION

The comparison of data presented by various authors in Tables 1 and 2 indicates that there is considerable variety in the proportions of functional components among fish and fish products. The composition depends on fish species, catch season and location, gonad maturation stage, and fish age and sex. A similar relationship applies to fish fat content, which fluctuates more than protein levels in various fish species and in individual fish from the same species. Depending on the fat content in muscular tissue, fish can be classified as “fatty” (oily, blue) or “low-fat” (white) fish. According to the Danish Fish Assessment,[97] oily fish contain more than 8% fat whereas white fish contain less than 2% fat. Oily fish accumulate fat in their muscular tissue whereas white fish, such as cod accumulate fat mainly in their livers. Furthermore, fat is not uniformly distributed in muscular tissue. In general, fat contents in fillets decreases from the head down to the tail and from the abdomen up to the dorsal muscle. The highest amount of fat is just under the skin in fish, and in the red muscles.[98] Similarly, the fatty acid profiles in fish are determined by different factors, such as fish food composition and water temperature.[19] In many fish species, the percentage of mono-unsaturated acids (MUFA), of PUFAs, and specifically of long-chain PUFAs (LC-PUFAs) increases with lower water temperature, to maintain membrane fluidity. For this reason, consumption of the same amounts of various fish species or catches from various periods can yield various levels of EPA + DHA intake. According to EFSA,^[19] 100 g of rainbow trout contains an average of 621 mg of EPA + DHA compared with as many as 2,723 mg of these acids in the same 100 g of fat herring. Hence, in order to supply the proper dose of EPA + DHA and to ensure their functional role in the body, a mixed diet from a combination of various fish species is recommend during the week. The discussion of functional components of fish in diets usually focuses on omega-3 fatty acids that comprise a significant share of the fish fat. Less attention is paid to other functional components, such as the whole and easily digestible proteins that are rich in essential amino acids, the fat-soluble vitamins (especially vitamin D₃), as well as the micro-elements and macro-elements, including calcium, magnesium, iodine, and selenium. All these components have a considerable impact on health and bodily functions. As they are found in fish in considerably larger amounts than in many other popular food products, fish can constitute an important source of these components in a mixed diet. “Functional food supplemented with EPA and DHA (eggs, dairy products, salad dressings, cereals) may also supply reasonable doses of such acids without the need to consume products originating from the sea,” commented Mozaffarian and Rimm.^[96] They continue, however, that “compared with food additives (supplements), fish may also present potential benefits connected with the supply of proteins, vitamin D₃, and selenium.” Most authors, especially dietitians, note that the benefits resulting from fish consumption exceed the potential risks.[96,99] Other authors do not agree. Based on comprehensive bibliographical studies, Stern[100] demonstrated that the beneficial effects of fish-origin PUFAs intake in reducing cardiovascular disease incidence might be diminished because of the increased risk connected with the excessive presence of MeHg in fish. Furthermore, Domingo et al.,[101] although far from doubting the importance of fish consumption for decreasing the incidence of cardiovascular disease, indicated that persistent organic compounds, MeHg, and other contaminants are a considerable health problem connected with fish consumption. To summarize, in order to ensure public health, consumers should adopt the suggestion by Stern^[100] and select reasonably from among the fish and fish products available on the market so as to increase maximum benefits (high contents of omega-3 acids, including EPA and DHA) and decrease risks (low levels of contaminants).

DECLARATION OF INTEREST

The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the article.

ACKNOWLEDGMENT

The authors have no financial interest in any commercial undertaking of the fish industry. This project was financed by the Polish Ministry of Science and Higher Education as a research project from funds for scientific studies in the 2008–2011 period.