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Health benefits and functions of salt-fermented fish

Journal of Ethnic Foods volume 11, Article number: 34 (2024) Cite this article

Abstract

Salt-fermented fish, a typical food in many regions of the world, was classified into three types depending on the processing method. It was divided into a process of fermenting by adding fish and salt only, a method of filtering it to form a fish sauce, and a method of lactic acid fermenting by adding additional carbohydrates. The free amino acids produced in large quantities through fermentation make salt-fermented fish a valuable protein source in regions where rice is the staple food. Furthermore, they also have significant amounts of omega-3 fatty acids (EPA and DHA), making them nutritionally excellent and functional, with antioxidant, antihypertensive, and fibrinolytic activities that benefit cardiovascular health. Some lactic acid bacteria (LAB) isolated from fermented fish products have beneficial effects on humans, including bacteriocin and probiotic effects. Looking to the future, the potential benefits of reducing naturally occurring biogenic amines and adjusting the salt content for storage stability could further enhance the health and taste benefits of salt-fermented fish, providing hope and optimism for the future of food preservation and nutrition.

Introduction

Fermentation, an ancient method of food preservation, is a cost-effective means to extend the shelf life of highly perishable fish while enhancing flavor and nutritional quality [1]. Rooted in history since around 6000 BC, humans salted seafood using earthenware vessels, triggering natural fermentation by salt-tolerant bacteria and shaping salting and fermentation technology [2]. The historical significance of fermented fish, a practice transcending time and cultures, is evident in ancient Greece, where it became a vital Mediterranean trade commodity [3]. This rich cultural heritage adds a layer of appreciation to the nutritional and health benefits of salt-fermented fish.

Fish fermentation relies on endogenous autolytic enzymes, predominantly pepsin and trypsin, complemented by associated microflora, with the process influenced by the chosen fermentation method [1]. In the presence of salt, spoilage microorganisms cease activity, allowing the fish's autolytic enzymes to hydrolyze proteins, lipids, and carbohydrates, creating characteristic flavors [1]. When bacteria participate, organic acids like acetic and lactic acid form, resulting in easily digestible and nutritious fermented fish products [4, 5]. These products smoothly integrate into diets globally, serving as seasonings or supplementary ingredients across Asia, Africa, Europe, and Mediterranean regions [6].

Southeast Asia, a region with rice as a staple food, embraces salted fish as a traditional fermented food, meeting dietary needs for sodium and protein [3]. In Korea, a grain-culture area, health concerns arise due to high sodium intake from salt-fermented fish alongside kimchi, soybean paste, and soy sauce [7]. Extensive studies have explored the nutritional value of salt-fermented fish, such as antioxidants, antibacterial properties, antihypertensive effects, anti-thrombotic benefits, anti-obesity potential, immune enhancement, osteoporosis prevention, and skin whitening [1, 3, 6, 8, 9]. Salted fish containing γ-aminobutyric acid (GABA) and a thrombolytic enzyme from Bacillus bacteria is reported to aid in preventing cardiovascular diseases [1, 9, 10].

This review comprehensively explores fermented fish processing methods, regional distributions, the diverse health benefits of nutritional and functional characteristics, and biogenic amines related to food hygiene.

Fermentation types of salt-fermented fish around the world

Numerous traditional fermented fish products exist worldwide, including in Asia, Africa, and Europe. Although the primary method for all fermented fish products involves the use of high amounts of salt, differences exist in the choice of raw materials, fish-to-salt ratio, duration of fermentation, and addition of other raw materials during the fermentation process.

Fermented fish products can be divided into three groups depending on the fermentation type shown in Table 1. The final product appearance is (1) a product consisting of whole, small pieces of meat or viscous paste, such as rakfish (Norway), freseekh (Egypt), ngari (India), ngapi (Myanmar), bagoong (Philippines), pra-hoc (Cambodia), pla-ra (Thailand), belacan (Malaysia); (2) a fish sauce (used as liquid with more or less viscosity), such as nuoc-mam (Vietnam) or nam-pla (Thailand), bakasang (Indonesia), shottsuru (Japan), aek-jeot (Korea); or (3) fish lacto-fermented with a source of carbohydrates (cooked rice, vegetables, millet and malt as a starter), such as plaa-som (Thailand), phaak (Cambodia), narezushi (Japan), and sikhae (Korea).

Table 1 Salt-fermented fish products around the world
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Fermenting whole or large pieces of fish results in the fish retaining as much as possible of its original structure [6, 11]. Fermented fish pastes, where the fish is converted into paste-like products [12], and fish sauce, which is completely converted into a liquid form [13]. Based on processing methods, fermented fish can be divided into two classifications: fermentation using fish and salt only. Second, fermentation uses fish, salt, and carbohydrate, including cooked rice, millet, and flour [6]. In fermented fish products using fish and salt, for example, rackfish is a native fish dish of Norway made from salmonid freshwater fishes (trout or char) and 4–6% salt [6]. Feseekh of Egypt is mainly made of pebbly fish (Alestes baremose) and 20–30% salt [14]. Surströmming, having a unique smell, is a fermented fish product made from herring in Sweden [6]. Lanhouin is made from whole cassava fish (Pseudotolithus senegalensis), a traditional fermented salted fish condiment in West African countries [15]. Ngari is a fermented fish product of Manipur in North-East India and is usually eaten as a side dish with cooked rice [16]. Jeotgal, known as salt-fermented seafood in Korean cuisine, adds 5–30% (w/w) salt to raw materials such as shrimp, shellfish, and fish [9].

Even in Southeast Asia, many salt-fermented fish products that use the whole fish body or are in paste form are being introduced. For example, the ngapi-gaun of Myanmar is made by adding 30% salt to catfish and maturing it for about a month [1]. Bagoong is a fermented product made by adding 30% salt to fish such as sardines, mackerel, and anchovies and maturing them for 2–6 months [11]. Meanwhile, prahok is a salt-fermented fish paste that uses carp as a raw fish, and it is favored in Cambodian cuisine as a seasoning or condiment [11]. Fish paste made from freshwater fish, such as pla-ra, is also used in Thailand [1, 9]. Salt-fermented fish products such as terasi of Indonesia, kapi of Thailand, and belacan of Malaysia are made from shrimp as a paste [1, 11].

Fish sauce is traditionally produced by using whole fish with salt in a ratio of 1:1 to 3:1 and fermenting anywhere between 6 and 12 months or even longer [17]. The fermented liquid is rich in fish-soluble proteins, peptides, and amino acids characterized by umami tastes [18]. Different names in different countries are used to describe these sauces. In Vietnam, it is called nouc-mam; in Thailand, it is called nam-pla. The others, including budu of Malaysia and Indonesia, patis of the Philippines, bakasang of Indonesia [19], yu-lu of China [20], shottsuru of Japan, and aek-jeot of Korea have been popularly used throughout the Asian region. Colatura di alici is a traditional anchovy sauce produced in Campania, Italy [21]. Fish sauces generally contain all essential amino acids, vitamins, and minerals [6]. Nowadays, Southeast and East Asian countries are the leaders in their fish sauce production and have annually expanded into international markets [6].

Other fermented fish products using fish, salt, and carbohydrates, including cooked rice, millet, and malt, have been widely used in Asia, as shown in Table 1. For example, plaa-som of Thailand is a fermented fish for which whole fish or fish fillets are mixed with salt (8:1; fish: salt ratio, w/w), cooked rice, and minced garlic [6]. Sometimes, cooked rice and garlic are replaced with palm syrup and roasted rice [22]. Pekasam of Malaysia is a fermented fish product prepared by mixing freshwater fish with salt (below 10%) and ground, roasted, uncooked rice in 2–4 weeks of fermentation [23]. The fermented fish products, phaak of Cambodia, bulong-isuda of the Philippines, and mam chua of Vietnam, were produced using freshwater fishes or marine fish using similar methods in Southeast Asia [11]. Narezushi and fish-nukazuke are salt-fermented fish using carp, mackerel, and sardine with rice bran and cooked rice and are very popular in Japan [6, 24, 25]. Sikhae, made from various fish species such as flat-fish, Alaska pollack, and squid, is a representative fermented fish product on the East coast of Korea. Malt powder as an additive can enhance the enzymatic degradation of fish and acid and alcohol fermentation by adding carbohydrates such as cooked rice and millet [26, 27].

On the other hand, since salt added to fermented fish is known to increase the risk of hypertension and cardiovascular diseases [27], fish lacto-fermented with a carbohydrate source is considered suitable as a fermented fish product for modern society.

Nutritional values of salt-fermented fish

Free amino acids

Low molecular weight compounds such as soluble proteins, peptides, and amino acids are produced during proteolytic degradation by endogenous proteases in fish muscles or digestive tracts of fish, and various microorganisms exist in fish fermentation [17, 28]. Fish sauce, therefore, is considered an important source of dietary proteins and amino acids and has become a necessity in Southeast Asian households [29].

The compositions of free amino acids in salt-fermented fish products are summarized in Table 2. The total contents of free amino acids ranged from 6815 to 10,223 mg/100 in fish sauce products such as nam-pla (Thailand), nuoc mam (Vietnam), patis (Philippines), bakasang (Indonesia), budu (Malaysia), aek-jeot (Korea), and ishiru (Japan) [30, 31]. These fish sauces are fermented using red meat fish such as anchovies, sardines, and sand lances as raw materials, and the total content of free amino acids is thought to vary depending on the fish species and fermentation time. Meanwhile, the amino acid content was relatively low at 1443–5753 mg/100 g in fermented whole fish (or fish paste) such as jeotgal (Korea) [32] or adjuevan (Ivory Coast) [33] and fish products fermented with carbohydrates such as narezushi (Japan) [34] and sikhae (Korea) [35]. The content of essential amino acids ranged from 465 to 5010 mg/100 g. However, most fish sauces accounted for more than 50% of total amino acids, and the proportion was particularly high in patis (59.3%) and bakasang (57.0%). Salt-fermented fish, therefore, are considered to be responsible for the difference. In addition, branched-chain amino acid (BCAA) content, recently known as skeletal muscle synthesis amino acids and playing a very important role in protein metabolism [36], was also present in the range of 1154–1867 mg/100 g in fish sauces, accounting for 16–25% of all free amino acids. However, in sikhae made of Alaska pollack, it was very low at 213 mg/100 g, accounting for 14.8% of total free amino acids [35]. Unlike the red meat fish used in fish sauces, white meat fish species and the short fermentation time (within four weeks) are considered to be the effect.

Table 2 Free amino acid contents of salt-fermented fish products1,2
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Taurine, detected in considerable amounts in jeotgal, narezushi, and sikhae, has been well known to have several beneficial physiological actions, including antioxidant, detoxification, osmoregulation, cell membrane stabilization, and neuromodulation [37,38,39,40,41,42]. γ-Aminobutyrate (GABA), a major inhibitory neurotransmitter in the adult mammalian brain, is also present in fermented fish products [43]. Since plant-based foods are also deficient in lysine and methionine, consuming fermented fish containing these will fulfill the amino acid requirements of people with a cereal-based diet [1].

Each amino acid has its unique taste, and Fuke and Shimizu [44] have identified two amino acids, aspartic acid and glutamic acid, as having an umami taste, and five amino acids, threonine, serine, glycine, alanine, and lysine, as having a sweet taste. Additionally, six amino acids, valine, methionine, isoleucine, leucine, phenylalanine, and histidine have a bitter taste [45]. Using this method, the content of sweet taste in fish sauces was highest in the range of 1529–4140 mg/100 g, accounting for 24.6–41.2% of the total free amino acids. Next, the bitter taste ranged from 1737 to 3232 mg/100 g, accounting for 28.4 to 47.4% of the total free amino acids. Moreover, the umami flavor ranged from 982 to 2520 mg/100 g, accounting for 16–25.2% of the total free amino acids. However, the taste threshold of aspartic acid and glutamic acid, which have an umami taste, is 3 and 5, respectively, which is 4 to 100 times lower than that of other amino acids, so when converted to each taste value (concentration of each amino acid/threshold of each amino acid), the taste-active compounds in all fish sauces are naturally considered aspartic acid and glutamic acid [46]. Glutamic acid is found to increase umami perception and improve overall food preference and is known to have synergistic effects with 5’-nucleotides such as adenylate, inosinate, and guanylate [30].

Fatty acid compositions

The fatty acid contents of salt-fermented fish products are shown in Table 3. In the fatty acid composition of salt-fermented fish, excluding suan yu and shidal using freshwater fish as raw materials, the proportion of polyunsaturated fatty acids (PUFAs) was the highest, followed by saturated fatty acids (SFAs) and monounsaturated fatty acids (MUFA) [32, 34, 47,48,49,50,51]. On the other hand, the proportion of MUFAs was the lowest in suan yu and shidal [52, 53]. The ratios of C16:0 and C18:0 were naturally dominant in SFAs, and C16:1 and C18:1 were also dominant in MUFAs.

Table 3 Fatty acid contents of salt-fermented fish products
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Among PUFAs, the n-3 series, C22:6, and C20:5, were dominant, and C18:4 was also present in large amounts in fermented fish such as narezushi, tareeh, and mehiawh [34, 51]. The n-6 PUFAs were present in concentrations in the order of C18:2, C18:3, C22:4, and C20:4. These PUFAs are easily oxidized during storage to create off-flavors and odors. However, the added salt suppresses the deterioration of salt-fermented fish's quality and maintains the polyunsaturated fatty acids' content [54, 55].

The proportion of n-6 fatty acids accounted for 3.3–8.9% of salt-fermented fish processed in Asia, such as sardine sauce, bagoong, narezushi, and jeotgal, but n-3 fatty acids accounted for 27.9–34.3%, and 4.6–8.5 times higher than n-6 fatty acids [32, 34, 47,48,49,50]. However, in fermented fish such as tareeh and mehiawh processed in the Arabian Gulf, and suan yu and shidal, which are made from freshwater fish, n-6 fatty acids were 1.9–3.2 times and 1.2–1.4 times higher than n-3 fatty acids, respectively [51,52,53].

As a result of calculating the ratio (n-6/n-3) of n-6 fatty acids to n-3 fatty acids in salt-fermented fish, it varied from 0.1 to 3.16. In particular, fermented fish made from freshwater fish such as carp and puntius had the highest values ​​of 3.16 and 1.94, respectively, while fermented fish made from anchovies, shrimp, sandfish, and silver stripe round herring had very low values ​​ranging from 0.1 to 0.29. These low values showed that n-3 series fatty acids were dominant in fermented saltwater fish.

Before industrialization, the ratio of n-6/n-3 series fatty acids in human diets was approximately 1:1–2:1 due to sufficient consumption of vegetables and marine products rich in n-3 fatty acids. However, this ratio gradually increased to approximately 10:1–20:1 due to industrialization [56, 57]. Additionally, overnutrition and Western-style eating habits can further exacerbate this imbalance in the n-6/n-3 ratio. In particular, deficiency of n-3 long-chain PUFA (n-3 LCPUFA), such as eicosapentaenoic acid (EPA) or docosahexaenoic acid (DHA), easily leads to a pro-inflammatory state and increases hyperinsulinemia and insulin resistance [56]. These changes may ultimately lead to the development of nonalcoholic fatty liver disease (NAFLD) and steatosis (hepatocyte triacylglycerol accumulation and cirrhosis) [58].

On the other hand, the consumption of n-3 and n-6 ​​PUFAs is known to have various beneficial effects ranging from fetal development to cancer prevention [59]. Additionally, PUFAs not only have a preventive effect against arterial hypertension, asthma, and inflammatory diseases but also have a preventive effect against breast cancer and immune system disorders [60]. For example, n-3 fatty acids protect against several cardiovascular diseases, such as myocardial infarction, atherosclerosis, arrhythmia, hypertension, and human coronary artery disease [59, 61], lowering blood pressure by reducing platelet aggregation and adhesion to the blood [62]. DHA, an n-3 LCPUFA, plays an important role in developing the nervous system of fetuses and newborns [63]. Therefore, salt-fermented fish products are considered an excellent food material as a source of n-3 fatty acids and nutritional value.

Health benefits of salt-fermented fish

Antioxidant activity

As a consequence of fermentation, the breakdown of fish proteins by endogenous or microbial proteases may release amino acids and peptides with biological activities potentially used as nutraceuticals and functional ingredients for health promotion and disease risk reduction, depending on their structural, compositional, and sequential properties [8, 64].

In studies on the health benefits of salt-fermented fish, antioxidant activity was most frequently reported, followed by angiotensin-I-converting enzyme (ACE) inhibitory activity known as an antihypertensive effect [65,66,67,68]. The results are shown in Table 4.

Table 4 Antioxidant activity and ACE inhibitory activity of salt-fermented fish products
Full size table

The 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical-scavenging activity method was most commonly used to measure antioxidant activity. This method uses the principle that when DPPH reacts with a proton-donating substance such as an antioxidant, the radical is scavenged, and the absorbance is reduced [69].

The DPPH scavenging activity of salt-fermented fish products varied from 7.05 to 74.14 µmol TE/g sample, with budu II (fish sauce made from marine fish) [64] being the highest at 74.14, while koong-som (made from small shrimp) [65] and jaloo (made from krill) [65] were the lowest at 8.58 and 7.05, respectively. Kapi (made from shrimp) [64, 65] showed 49.49–53.67 µmol TE/g sample and 10.6% depending on the analysis method, regardless of type. Kung-chom (made from shrimp) [65] also had a 36.55–37.61 µmol TE/g sample.

When DPPH was analyzed by scavenging activity (%), all salt-fermented fish products except sikhae products showed activity above 50%. In particular, patis II (round scad sauce) [67] showed the highest scavenging activity at 83.5%, followed by ngari (salt-free fermented fish made from puntius) [68] at 71.31%, patis I (anchovy sauce) [67] at 69.2%, pekasam (made from freshwater fish) [70] at 68.81%, jeotgal (made from whangseoke) [71] at 63.83%, and bagoong (made from shrimp) [48] at 61.5% [48, 66,67,68, 70, 71]. In addition, sikhae III, made from sea squirt, showed a high scavenging activity of 67.5% [72], but sikhae I and II, made from flat-fish [26] and Alaska pollack [73], showed the lowest scavenging activity of 2.65 and 4.33%, respectively. Fish sauces such as patis [67] and budu [67], which had a long fermentation period, generally had higher antioxidant activity than fish pastes such as kapi [65] and jaloo [65] or salted fish fermented by adding carbohydrates such as pla-som [64], pla-ra [64], and koong-som [65].

The observed changes in antioxidant activities in fish sauces are influenced by the fermentative products, mainly peptides and amino acids, produced due to the prolonged fermentation process [67]. It contains high levels of glutamic acid, alanine, lysine, leucine, and aspartic acid, known for their antioxidative properties [13, 47, 67].

As a result of measuring the IC50 (half maximal inhibitory concentration) of DPPH of the salt-fermented fish extract, it was very active at 1.062 mg/ml in budu I [74] and 1.36 mg/ml in pekasam [70]. However, it was very low at 18.87 mg/ml in flat-fish sikhae [26] and 11.55 mg/ml in Alaska pollack sikhae [73], respectively, showing a similar tendency to the free amino acid content of salt-fermented fish (Table 2). Meanwhile, the DPPH scavenging activity (IC50) of the alcohol extract of squid sikhae was 1.66–2.68 ml/ml, which was higher than that of the water extract (6.09–12.19) and increased with the fermentation period [75]. In a study by Kwon et al. [76], the ingredients such as garlic and red pepper used for kimchi were reported to have antioxidative effects.

The ABTS radical-scavenging activity of salt-fermented fish such as budu II, kapi II and III, koong-chom, tai-pla, pla-ra, and pla-som generally showed a similar trend to the antioxidant results shown in DPPH [64, 65]. However, the scavenging activities of ABTS in kung-som I and II and jaloo, where the activities of DPPH were lower than that of other salt-fermented fish, were relatively very high [64, 65].

Ferric reducing antioxidant power (FRAP) was the highest in budu II at 60.86 μmol TE/g, and the rest of the salted fish generally varied in the range of 8.43–42.01 μmol TE/g [64, 65]. Faithong et al. [65] studied the correlations between antioxidative activities determined by different assays. They reported that the relationship between ABTS and DPPH radical-scavenging activities is correlated very well (r2 ≧0.9085) and between ABTS radical-scavenging activities and FRAP (r2 ≧0.943). FRAP also correlated with DPPH radical-scavenging activities (r2 ≧0.9635) in salt-fermented fish products.

Another method of measuring the antioxidant's capability was hydrogen peroxide scavenging activity, which was 6.88% in patis I (anchovy sauce) [67], 9.45% in patis II (round scad sauce) [70], 51.1% in bagoong (shrimp paste) [48], and 15.17% in the ethanol extract of sikhae IV (squid) [75], respectively.

Najafian and Babji [74] separated two novel peptides with strong antioxidant power using HPLC and ESI-TOF MS/MS in budu, Lue-Asp-Pro-Val-Phe-Ile-His (LDDPVFIH) and Val-Ala-Gly-Arg-Thr-Asp-Gly-Val-His (VAAGRTDAGVH). Among these peptides, hydrophobic amino acids (Ile and Leu), acidic (Asp), and basic (His) amino acids contribute to the high antioxidant power of budu.

In addition, two novel peptides, Ala-Ile-Pro-His-Tyr-Pro (AIPPHYP) and Ile-Ala-Glu-Val-Phe-Leu-Ile-Tre-Asp-Pro (IAEVFLITDPK) with an IC50 of 0.636 mg/ml of ABTS, were isolated and identified from pekasam in the same way [70].

Antihypertensive activity

In general, hypertension is associated with angiotensin-I-converting enzyme (ACE), and many peptides showing ACE inhibitory activity are produced through protein degradation during the aging process of salted fish [68, 77,78,79].

ACE inhibitory activities of extract of salt-fermented fish products varied in the range of 3.36–77.31%, shown in Table 4. Salt-fermented fish, such as pla-som and pla-ra, made with freshwater fish, salt, and carbohydrates, showed the highest activity at 77.31% and 76.66%, respectively [64]. Next, bakasang, made from skipjack tuna, is a typical fish sauce in Indonesia, at 68.8% [80], followed by tai-pla, made from fish viscera, at 68.17% [64]. In kung-chom I and II, made with shrimp, salt, and roasted rice, the activity was 53.82 and 52.40%, respectively [64], whereas in kapi II and III, shrimp paste using shrimp and salt only, the change in activity was very large at 3.36% and 42.25%, respectively [64]. Compared with the other products, douchi, a traditional Chinese fermented soybean, contained 56.8% to 76.3% ACE inhibitory activity [80].

Less ACE inhibitory was exhibited by ngari of India at 33.62% activity [71], and sikhae II and III made from Alaska pollack and sea squirt showed 29.38% and 24.8% activity, respectively [72, 73]. These different activities are considered to be due to the raw materials, ingredients, and processing employed according to local producers [64]. Phadke et al. [68] reported that higher ACE inhibition was observed significantly at higher protein concentrations by all the ngari samples fermented for different periods (P < 0.05), and ACE inhibitory activity increased with fermentation time.

On the other hand, in blue mussel [81] and oyster sauce [82], which are fish sauces using shellfish, IC50 values of ACE inhibitory activity appeared to be 1.01 mg/ml and 2.45 mg/ml, respectively, showing similar activity to IC50 1.70 ml/ml in Alaska pollack sikhae [73]. Je et al. [81, 82] also isolated and purified peptides showing competitive inhibition of ACE from blue mussel- and oyster-fermented sauces, and their IC50 values of ACE inhibition were 2.98 μM (blue mussel sauce, MW 6.5 kDa) and 0.147 mM (oyster sauce, MW 593 Da), and reported that they effectively reduced blood pressure in spontaneous hypertension rats (SHR) after oral administration. As a result of oral administration of narezushi water extract having ACE inhibitory activity (IC50 value 0.06 mg/mL), the systolic blood pressure of SHR was effectively reduced [83].

Many studies have reported the direct isolation of peptides with strong ACE-inhibiting ability from these fermented fish products. Okamoto et al. [84] isolated three peptides from the fermented salmon sauce, Gly-Trp, Ile-Trp, and Val-Trp. In a similar study, Ichimura et al. [85] isolated nine peptides having ACE inhibitory activity, such as Ala-Pro, Lys-Pro, Arg-Pro, Gly-Pro, Glu-Pro, Thr-Pro, Val-Pro, Gly-Ile, and Asp-Phe from anchovy sauce and also nine peptides from sardine sauce, and four peptides from bonito sauce, respectively. The reason why so many peptides containing proline with high ACE inhibitory activity are isolated from fish sauces is thought to be because of the unique structure of proline being an imine acid [85]. Peptide bonds containing proline residues, therefore, are resistant to hydrolysis by general peptidases. This may be the reason why these proline-containing dipeptides survived long-term fermentation [8, 85]. specially, three peptides, Arg–Pro, Lys–Pro, and Ala–Pro, from three sauces (anchovy, sardine, and bonito) showed the highest ACE inhibitory activity, with IC50s of 21, 22, and 29 μM, respectively. Ichimura et al. [85] reported that the oral administration of Lys–Pro reduced the blood pressure of SHRs [85], and fermented anchovy sauce itself also stimulated insulin secretion by cultured RINm5F insulinoma cells.

Although fermented fish products may not be directly used as a functional food because of their high concentration of sodium chloride, the sauce may be useful as a source of biologically active substances. Since the high salt content of salt-fermented fish, however, is known to be a causative agent of adult diseases such as high blood pressure, it is considered that epidemiological studies related to the intake of these salt-fermented fish should also be added.

Other biological activities

Fibrinolytic enzymes, known as thrombolytic agents, were found in various fermented foods. High fibrinolytic activity has been reported in traditional fermented fish of India, such as ngari and shedal [86] as well as in fermented shrimp, anchovy, and yellow corvine Korean jeotgal products [87]. Cha et al. [26] also reported that flat-fish and Alaska pollack sikhaes showed strong fibrinolytic enzyme activity comparable to that of kimchi, and that this was due to the effect of organic acids produced by lactic acid fermentation [88].

Some lactic acid bacteria (LAB), such as Lactobacillus sp. (L. plantarum, L. pentosus, L. sakei) isolated from fermented fish products, have demonstrated healthy effects [89, 90]. These LABs are known to produce bacteriocin, which inhibits pathogens [1]. When consumed in foods, the metabolites of this group of bacteria are known to have probiotic effects [1]. Therefore, these LAB strains can be used to design probiotic formulations or to produce new fermented seafood products [91].

Functional activities in the ethanol extract of squid sikhae, such as inhibitions on α-glucosidase, β-glucuronidase, and elastase, were found [75], while bile acid binding capacity (23.80 mM/g) [92] and XO inhibitory activity (IC50 value: 0.56 mg/ml) [73] were observed in Alaska pollack sikhae during fermentation. Additionally, fermented low-salt squid (Todarodes pacificus) jeotgal improved the learning and memory impairments in SD rats by inhibiting acetylcholinesterase activity in the brain [93]. In another study, the hydrophobic peptide fraction isolated from anchovy fish sauce has been shown to have a strong anti-proliferative effect against human lymphoma cells (U937) by inducing this apoptosis (IC50 value: 31 μg/mL) [8]. Coenzyme Q, known as an energy booster and immune-system enhancer, is also found in a large amount of 291.0 mg/g in jeotgal, Korean fermented fish [94]. However, the efficacy of these in vitro results is considered necessary for further future verification studies through animal and human tests.

On the other hand, a specific study on the daily intake of salt-fermented fish has yet to be introduced. Therefore, additional research on the functional promotion effect related to the consumption of salt-fermented fish is expected to contribute significantly to improving the processing suitability of fermented fish products.

Biogenic amines and their reduction in salt-fermented fish

Intake of low amounts of biogenic amines, produced by decarboxylation of amino acids in foods, does not harm human health [95, 96]. However, when their amount in food is too high, and detoxification ability is inhibited or disturbed, biogenic amines could cause problems such as rashes, migraines, high blood pressure, and low blood pressure after ingestion [8, 96].

A total of 11 types of biogenic amines were analyzed in salt-fermented fish (Table 5). Among them, five types, including tryptamine, putrescine, cadaverine, histamine, and tyramine, were detected as major amines in anchovy and sand lance sauce, and six types, including phenylethylamine, serotonin, spermidine, noradrenaline, dopamine, and spermine, were detected as minor amines (Table 5)[97]. In jeotgal I, made from shrimp, except for dopamine, the remaining amines were detected in small amounts, whereas in jeotgal II (squid), except for high amounts of cadaverine, the remaining amines were generally low in content [97]. This trend was similar to the rest of the salt-fermented fish, with high levels of cadaverine and tyramine detected in jeotgal III (viscera), cadaverine and spermine in jeotgal V (clam), and histamine and dopamine in jeotgal VI (yellow corvina) [97]. In narezushi (sandfish), the content of putrescine was highest at 370 mg/kg, followed by tyramine at 340 mg/kg, tryptamine at 70 mg/kg, and histamine was the least detected at 10 mg/kg [98]. Gowda et al. [17], however, reported that the predominant amines detected in fish sauces are six types: histamine, putrescine, cadaverine, tyramine, tryptamine, and phenylethylamine.

Table 5 Biogenic amine contents and their reduction effects in salt-fermented fish products1
Full size table

Meanwhile, the U.S. Food and Drug Administration (FDA) has recommended that the concentrations of histamine, tyramine, and total biogenic amines among fish and seafood products be less than 50 mg/kg, 100 mg/kg, and 1000 mg/kg, respectively, and less than 500 mg/kg in fish sauce [99, 100]. The European Union (EU) states that the acceptable histamine level should be less than 400 mg/kg for fish sauce [8]. In Canada, Finland, Switzerland, and South Africa, the total amount of biogenic amines allowed for fish and seafood products is 100 mg/kg [101].

Therefore, many studies have attempted to develop methods to reduce the content of biogenic amines in fermented fish. As shown in Table 5, all of the biogenic amines decreased after fermentation except for cadaverine in anchovy sauce produced by Aspergillus oryzae [66]. In addition, when acid-assisted fermentation was performed by adding tamarind pulp or dripped slipper fruit, the average values of putrescine, cadaverine, and histidine were not significant compared to naturally fermented Ikan pekasam, but there was a reducing effect in the range of 13.7–22.8%, respectively [23]. Moreover, the total biogenic content in layú II fermented by adding sucrose was 112.5 mg/kg, 21.7% lower than in the case of no addition (143.7 mg/kg) [102].

On the other hand, Mah and Hwang reported that biogenic amine concentration decreased by 16% in fermented anchovy jeotgal by inoculating with Staphylococcus xylosus 0538 compared to controls. In particular, the resolution was highest for histamine [103]. Supplementation of Moringa oleifera leaves (5–10%, w/w) was also reported as the effect of reducing histamine without sensory problems in the quality of fermented shrimp paste [104].

Additional research on reducing biogenic amines is thought to be needed in the future to improve the quality of these salt-fermented fish and stabilize food hygiene.

Conclusion

Salt-fermented fish is a traditional seafood that has been favored in many regions of the world for a long time. Fermented fish products can be divided into three groups depending on the fermentation type. The final product consists of fish (or crushed fish paste) and salt only, fish sauce (used as liquid) after filtrating, and fish lacto-fermented with a source of carbohydrates (cooked rice, vegetables, millet, and malt). These fermented fish are not only nutritionally superior in terms of free amino acid content that is produced through fermentation but also have excellent functionality such as antioxidant and ACE-inhibiting ability and also contain large amounts of omega-3 series substances (EPA and DHA) that were effective in preventing cardiovascular diseases. Some lactic acid bacteria (LAB) isolated from fermented fish products are known to have beneficial effects on humans, including bacteriocin and probiotic effects. However, the efficacy of these in vitro test results is considered necessary for further future verification studies through animal or human tests. Moreover, since the salt content added is high for storage, it is believed that processing methods that reduce sodium chloride and biogenic amines will satisfy the tastes of modern society.

Availability of data and materials

All data generated or analyzed during this study are included in this published article.

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  1. Department of Food and Nutrition, Changwon National University, Changwon, 51140, Korea

    Yong-Jun Cha & Daeung Yu

  2. Interdisciplinary Program in Senior Human-Ecology, Major in Food and Nutrition, Changwon National University, Changwon, 51140, Korea

    Daeung Yu

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Cha, YJ., Yu, D. Health benefits and functions of salt-fermented fish. J. Ethn. Food 11, 34 (2024). https://doi.org/10.1186/s42779-024-00251-5

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Keywords

Journal of Ethnic Foods

ISSN: 2352-619X

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