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Advances in the Formation and Control Methods of Undesirable Flavors in Fish

College of Food Engineering and Nutritional Science, Shaanxi Normal University, Xi’an 710119, China
The Engineering Research Center for High-Valued Utilization of Fruit Resources in Western China, Ministry of Education, Shaanxi Normal University, Xi’an 710119, China
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Foods 2022, 11(16), 2504;
Received: 19 July 2022 / Revised: 11 August 2022 / Accepted: 16 August 2022 / Published: 19 August 2022
(This article belongs to the Special Issue Food Perception: Taste, Smell and Flavour)


Undesirable flavor formation in fish is a dynamic biological process, decreasing the overall flavor quality of fish products and impeding the sale of fresh fish. This review extensively summarizes chemical compounds contributing to undesirable flavors and their sources or formation. Specifically, hexanal, heptanal, nonanal, 1−octen−3−ol, 1−penten−3−ol, (E,E)−2,4−heptadienal, (E,E)−2,4−decadienal, trimethylamine, dimethyl sulfide, 2−methyl−butanol, etc., are characteristic compounds causing off−odors. These volatile compounds are mainly generated via enzymatic reactions, lipid autoxidation, environmentally derived reactions, and microbial actions. A brief description of progress in existing deodorization methods for controlling undesirable flavors in fish, e.g., proper fermenting, defatting, appropriate use of food additives, and packaging, is also presented. Lastly, we propose a developmental method regarding the multifunctional natural active substances made available during fish processing or packaging, which hold great potential in controlling undesirable flavors in fish due to their safety and efficiency in deodorization.

1. Introduction

Flavor is one of the most important palatable characteristics of food, significantly affecting food quality and consumer acceptance. Fish have long been considered an excellent source of high−quality protein. However, some unpleasant odors in fish caused by bacterial growth, the environment, processing methods, and storage conditions have still not been fundamentally resolved, which restricts fish processing in foodstuff. Therefore, promoting the quality of flavor and utilizing fish resources effectively have become one of the hottest research topics in fish processing.
Fish in general are classified into two main types, namely, fresh− and saltwater fish. The undesirable flavors of freshwater fish, such as earthy/muddy, fishy, and grassy, come from multiple sources [1]. Among these, the earthy odor is primarily caused by the metabolites of the inhabitant microorganism flora, i.e., mainly cyanobacteria (e.g., Anabaena, Lyngbya, Microcystis, and Skeletonema) [2] and actinomycetes (e.g., Streptomyces) [3]. Saltwater fish often have less intense undesirable odors than freshwater fish [4], and normally, saltwater fish tend to release “sea breeze−like” odors [5]. The differences in undesirable flavor profiles between freshwater and saltwater fish are the result of different volatile odor compositions; specifically, freshwater fish have more aldehydes, contributing to stronger fishy and grassy aromas, and have a stronger earthy odor, caused by geosmin (GSM), when compared to saltwater fish [5,6].
Cultured fish for human consumption contain richer lipids within their muscle tissue than fish living in the wild [7]. Experimental results showed that the relative concentration of lipid−derived volatile compounds was significantly higher (p < 0.05) in aquacultured fish samples as compared to wild samples [8], from which it may be concluded that oily fish often have more volatile oxides than lean fish. Sensory differences were also measured in a comparison of wild and cultured fish; assessors described wild gilthead sea bream as having ‘‘a more pleasant taste’’ and ‘‘a firmer texture’’, while the cultured group was thought of as having ‘‘poor taste’’, indicating the superiority of the wild fish [9,10].
Consumers demand commercial fish products with no unpleasant aroma or taste. An improved understanding of the compositions and formation of undesirable flavors helps to develop the flavor quality of fish products. We thus review the unpleasant components and their various sources, including enzymatic reactions, lipid autoxidation, environmentally derived reactions, and microbial actions. Meanwhile, most deodorization methods are summarized and evaluated in this review, and the use of natural deodorization methods can be highly effective while remaining environmentally friendly.

2. Volatile Compounds Contributing to Undesirable Flavors in Fish

Strong undesirable flavors are the most significant problem encountered in aquaculture, causing the dissatisfaction of consumers and a reduction in the market value of the product. Shi et al. reported that the primary volatile compounds in fish are alcohols and carbonyl compounds (the total relative contents are above 90%) [11]. Among these compounds, 2−−/3−methylbutanal, hexanal, heptanal, octanal, nonanal, (E,E)−2,4−heptadienal, (E,Z)−2,6−nonadienal, (E,E)−2,4−decadienal, (Z)−4−heptenal, (E)−2−octenal, (E)−2−nonenal, 1−penten−3−ol, 1−octen−3−ol, acetic acid, butanoic acid, (E,E)−3,5−octadien−2−one, (Z)−1,5−octadien−3−one, etc., play an important role in the characteristic flavor of fish, and most of them have been identified in many types of fish [5,8,12]. On the one hand, the same volatile compound can give off several flavors and odors: for example, 1−octen−3−ol not only has mushroom−like and strong plant−like flavors but also has a metallic−like flavor; 2,4−decadienal gives off orange, fresh, fatty, or green aromas [13]. On the other hand, a certain flavor is composed of a complex mixture of volatiles; for example, the fishy or rancid odor of fish products primarily consists of hexanal, (E,E)−2,4−decadienal, (E,E)−2,4−heptadienal, heptanal, etc. [14]. In general, a few relatively low molecular weight aldehydes mixed together are responsible for the pungent fishy smell of fish [8,11].
Previous research has shown that in a recirculating aquaculture system (RAS), earthy/musty odors originating from geosmin (GSM) and 2−methylisoborneol (MIB) are the most perceivable undesirable flavors in cultured freshwater fish [6,15]. It has also been reported that MIB contributes to the musty odor, while GSM is responsible for the earthy odor [16,17]. Moreover, GSM and/or MIB co−existing with aldehydes and alcohols such as hexanal and 1−octen−3−ol notably intensify the musty off−flavor in catfish fillet [18]. β−Cyclocitral, a characteristic undesirable flavor compound in fish providing tobacco/smoky/moldy smells [19], also contributes to off−flavors to fish in ponds [20]. Existing findings suggest that fish directly absorb these chemical compounds from ambient water and rapidly store them within their fatty tissue [21].
Characteristic sulfur and nitrogen derivatives are also regarded as volatile off−odor compounds, both of which are usually related to the deterioration of seafood. Due to low threshold values, the compounds can influence the overall aroma even in very low proportions [22]. Dimethyl sulfide (DMS) is considered the typical spoilage marker of sulfur−containing compounds and has been detected at low concentrations in some freshwater fish species [23]. Similarly, trimethylamine (TMA) is also regarded as a fish microbial spoilage marker and is used as a potential indicator of fish freshness. TMA comes from the reduction of trimethylamine−oxide (TMAO) [24], which occurs in saltwater fish and plays a significant role in keeping pH and osmoregulation stable, and the formation of TMA is accompanied by ammonia−like and fish−house−like odors [25]. It has been suggested that TMA in combination with DMS significantly contributes to saltwater fish odors, producing a fishy and seafood flavor that is much stronger than that of TMA alone [4].
Freshly harvested saltwater fish often have pleasant seaweedy, sweet, and faint green aromas. However, neutral to acid odors develop during storage, culminating in an overall pungent odor of fish and resulting in lower sensory grades (Figure 1) [26]. Triqui et al. [26,27] assumed that the concomitant elevation of concentrations of (Z)−4−heptenal, (Z)−1,5−octadien−3−one, and methional correlated with the development of an overall fishy odor in sardine during ice storage. Likewise, a study revealed that after storage of the raw material, the OAVs (odor activity value: a ratio of concentration to odor threshold) of (Z,Z)−3,6−nonadienal and (Z)−3−hexenal were significantly enhanced, which are responsible for the fatty and fishy off−flavors of boiled trout [28]. Moreover, it is noteworthy that both cultured and wild fish showed complex volatile profiles throughout the entire storage period; for example, rancid, putrid, sulfurous, and ammonia−like odors in fish are attributed to volatile odor compounds such as TMA, dimethyl disulfide, dimethyl trisulfide, piperidine, 1−penten−3−ol, 3−methyl−1−butanol, methanethiol, and acetic acid [24].

3. The Formation of Post−Harvest Undesirable Flavors in Fish

3.1. Lipid Oxidation

Many compounds causing undesirable flavors may originate from the process of lipid oxidation. Lipid oxidation is a major cause of poor quality and is also responsible for causing the development of fishy odors in fish, as well as undesirable textural changes through the interaction of protein and lipid oxidation products [29,30]. Phospholipids containing polyunsaturated fatty acids within the cell membrane are closely related to lipid oxidation in fish since they have a high degree of unsaturation and large surface area that are susceptible to oxidation [31]. Previous analyses have shown that the incidence rate of oxidation depends not only on the amount of lipids in the sample but also on the oxidative conditions, the enzymatic activity of the lipoxygenases, and the abundance of the antioxidant compounds present [32]. Enzymic involvement is necessary for the generation of lipid−derived volatiles in fresh fish; however, research indicates that lipid peroxidation in nonliving fish tissue is initiated nonenzymatically, primarily by heme−protein autoxidation [33,34]. In fact, lipid oxidation in the fish muscle is induced by several catalysts, including hemoglobin, iron, and lipoxygenases; furthermore, lipoxygenases result in severe fishy odors, while hemoglobin can be affiliated with a strong oxidized oil odor [35,36].
Oxidative enzymatic reactions and the autoxidation of lipids contribute to fresh fish with green, plant−like, metallic, and fishy aromas to a significant degree [37]. The main volatiles derived from lipids are reported in Table 1. Notably, biochemical reactions of polyunsaturated fatty acids (PUFAs) with lipoxygenases and hydroperoxide lyases produce unsaturated carbonyls and alcohols, such as 5−, 6−, 8−, 9−, and 11−carbon alcohols and carbonyls (e.g., eicosapentaenoic acid, shown in Figure 2) [12,13]. Meanwhile, autoxidation of PUFAs produces other types of unsaturated carbonyls, such as 6−, 7−, 8−, and 10−carbon carbonyls. In addition, enzymatic and nonenzymatic oxidation can occur simultaneously during cooking [38], and the most polyunsaturated of all of these acyl groups shows the highest tendency to undergo autoxidation. Previously, the fish muscle was covered by fish skin and was less susceptible to oxidation; therefore, the muscle released a minimal fishy flavor compared to the fish’s skin when perceived by smell [39]. Furthermore, the rate of lipid oxidation of the yellowtail dark muscle was faster than that of the ordinary muscle. The total lipid hydroperoxide content and thiobarbituric acid−reactive substances (TBARS) of the dark muscle were significantly higher than those of the ordinary muscle after 2 days of ice storage [40]. In addition to the characteristics of the fish itself, some physical factors also affect the degree of oxidation. For example, heme proteins, which are well−known prooxidants, can be further activated during the pH−shift process [34]. The intensity of heat treatment plays an important role in the extent of oxidation in cooked meat, with higher temperatures generally making hidden volatiles identifiable and accelerating retro−aldol condensation. As a result, more (Z)−4−heptenal and acetaldehyde are formed from (E,Z)−2,6−nonadienal, and (Z)−2−pentenal and acetaldehyde have the potential to be formed from (E,Z)−2,4−heptadienal [41].

3.2. Microbial Metabolites

Fish is a high−protein product that is susceptible to the proteolytic activity of microorganisms. Some related studies have reported that the microbial spoilage of harvested fish accounted for the loss of approximately 10% of fish catches worldwide [47,48]. Furthermore, spoilage from microorganisms produces metabolites responsible for various unpleasant undesirable flavors, leading to the eventual sensory rejection of fish products. The organisms causing the highest spoilage potential in specific products or storage conditions are named specific spoilage organisms (SSOs). Shewanella putrefaciens and Pseudomonas spp. are generally recognized as the specific spoilage bacteria of fresh fish, regardless of the origin of the fish [49]. Pseudomonas, Shewanella, Lactobacillus, and Carnobacterium species, identified by 16S rRNA gene sequencing analysis, were proved to be SSOs of gilt−head sea bream at various temperatures and atmospheric conditions [50]. Meanwhile, Carnobacterium, Serratia, Shewanella, and Yersinia were shown to be the dominate species in horse mackerel fillets at the time of sensory rejection [51]. Additionally, Photobacterium phosphoreum and Psychrobacter are the most common SSOs reported in fish products [52,53,54].
In general, different growth substrates can affect the growth rates of microorganisms, such as different fish species or the fish flesh in different process conditions. For example, psychrotolerant Gram−negative bacteria (e.g., Pseudomonas spp. and Shewanella spp.) are reported to grow in chilled fish, whereas fermentative bacteria (e.g., Vibrionaceae) prefer to multiply in unpreserved fish [55]. In addition, different water temperatures, seasonal variation, geographical location, surrounding gaseous composition, and processing might also have complex effects on the initial microbiota [56]. Specific spoilage microflorae dominating in fresh fish meat during storage under different gas atmospheres are shown in Table 2, which potentially determine the composition of the primary microflora [57]. Meanwhile, SSO populations were found to be significantly higher in retail−derived catfish in comparison to lab−filleted catfish tissue [58], and some chemical indicators of spoilage, such as the TMA value, in ungutted sea bass increased slowly, while the TMA values of gutted samples were much higher [59], suggesting that mishandling during processing is a major reason for rapid fish tissue spoilage.
Volatile compounds are associated with the metabolic activities of particular microbial groups. Pseudomonas spp. produce large amounts of volatile alcohols, ketones, esters, and sulfides (except H2S), whose typical descriptions are fruity, rotten, and sulfhydryl flavors in iced fish [49]. Shewanella spp. release intense undesirable odors as well, producing H2S and biogenic amines, as well as reducing TMAO to TMA, and even show proteolytic activity at low temperatures [60,61]. Moreover, Aeromonas spp., psychrotolerant Enterobacteriaceae, Photobacterium phosphoreum, and Vibrionaceae were all able to utilize TMAO in order to form TMA, resulting in off−odors [22,55]. Serratia fonticola and Serratia liquefaciens, Aeromonas, Acinetobacter, and some Pseudomonas spp. are known to produce histamine [62]. It is because microorganisms can utilize different precursor compounds that volatile metabolites are subsequently generated. As shown in Table 3, ethanol, organic acids, and esters are produced primarily from glucose. Leucine and isoleucine metabolism of fish meat led to increased 2−methyl−1−butanol, 3−methyl−1−butanol, 2−methylbutanal, and 3−methylbutanal; sulfur−containing volatiles are mainly generated by microbial−mediated enzymatic degradation of cysteine, methionine, and derivatives (e.g., DMS shown in Figure 3).

3.3. Living Environment

Due to increased consumption demand, aquaculture requires high stocking densities and feed supplies to satisfy productivity, which, however, lead to unfavorable eutrophication. Simultaneously, high fish stocking densities (>10,000/ha) and feeding rates (>70 kg/ha/d) fuel the rapid growth of algae, particularly cyanobacteria, which are known to produce undesirable flavors [72,73]. In addition, the relationship between the temperature and photoperiod associated with climate warming may affect phytoplankton growth [74]; in particular, the cyanobacteria growth rate and their ability to produce toxins are positively correlated with temperature elevation [75,76]. Rising temperature can result in cyanobacterial bloom enhancement, which poses a threat to water quality [77]. Fish are very susceptible to consuming food as well as industrial pollutants and natural off−odor compounds existing in their living environment [33]. These undesirable flavors from the environment render fish unmarketable unless purified by large quantities of clean water, causing a heavy economic burden on the aquaculture industry.
Moreover, it was shown that the concentrations of MIB, GSM, and β−cyclocitral are high in pond water, yielding undesirable fish flavors [18]. Furthermore, studies showed that MIB, GSM, β−cyclocitral, and dimethyl trisulfide are volatile compounds that frequently exist during cyanobacterial bloom episodes and were successfully detected in all predominant odor compositions from fish tissue, sediment, and algal cell samples [78,79,80,81]. Typically, cyanobacteria, certain fungi, and various actinomycetes produce these flavor metabolites and excrete them into the environment: Streptomyces can produce MIB and GSM, and nannocystis has been shown to produce MIB [82,83] (the biosynthesis of MIB and GSM is shown in Figure 4); Microcystis promotes β−cyclocitral synthesis [84]; microalgae, seaweed, and plankton are rich in a large quantity of dimethyl−β−propiothetin (DMPT, a precursor of DMS) [4]; and cyanobacteria and fish feed are the primary sources of odor−active terpenes [20,85,86]. Fish then take up these metabolites across their gill membranes, leading to the accumulation of these compounds within tissues that are rich in lipids. Besides the sources mentioned above, drinking water treatment plants and industrial waste treatment facilities are also key factors in producing undesirable flavors. For example, naphthalene compounds such as 2,6−dimethylnaphthalene and 2−methylnaphthalene, the degradation products of factory waste via microorganisms, can accumulate in fish as environmental pollutants [87]. Accidental spills of petroleum hydrocarbons also cause pollution in the same way [83].

4. Odor Control Techniques

Increased fish supplies are required to meet increased human consumption demands, while undesirable flavor contamination substantially delays harvest, thereby causing economic losses for fish farmers [83]. Effectively controlling the odor of fish products is critically important.

4.1. Environmental Renovation

Both GSM and MIB, derived from the culture environment, are the primary earthy and musty compounds associated with fish. The current method is to move the fish to a large body of clean water and stop feeding in order to purge the undesirable flavor compounds from the fish’s tissue [88]. However, this approach may take days or weeks to obtain the lowest residual levels of geosmin and MIB in the fish flesh, depending on various factors, such as the intensity of the undesirable flavor, the water temperature, and the fat content of the fish flesh [15,89,90]. In addition, fasting will greatly reduce the quality of fish [91]. In addition to temporary cultivation with clean water, strategies such as hindering the growth of bacteria and algae that produce odors and the adsorption or removal of undesirable flavor substances in aquaculture water are usually adopted.
The results obtained in previous studies demonstrate that aerobic, organic−rich conditions are beneficial to the growth of bacteria [88], and certain nutritional factors can stimulate GSM production by actinomycetes [15]. As a result, the biofloc technology (BFT) production system was launched to maintain the water’s turbulence through continuous aeration, make bacteria lose their cell buoyancy regulation ability, and metabolize excreted feed nitrogen, thus decreasing cyanobacteria and actinomycetes and significantly weakening the intensity of undesirable “earthy” and “musty” flavors [92].
In order to solve the undesirable flavor problem of cyanobacteria, accumulating experimental evidence has proven that ultrasound technologies have also shown significant potential in the management of cyanobacteria and possess the advantages of energy conservation, safety, and cleanness [93,94,95]. One of the damage mechanisms owing to ultrasonic irradiation is the increased presence of free radicals that destroy cellular constituents and functions by inducing lipid peroxidation, damaging cellular membranes, and inhibiting photosynthesis [96]. The relative content of malondialdehyde (MDA), used as a quantitative indicator of lipid peroxidation, was significantly increased after ultrasonic irradiation in most species of cyanobacteria [97]. In addition to algae removal, ultrasonically induced cavitation has been demonstrated to directly reduce off−flavor compounds GSM and MIB from RAS water, and high−frequency ultrasound (850 kHz) was more effective compared to low−frequency ultrasound (20 kHz) [98].
Due to the hydrophobic structures of GSM and MIB, adsorbents such as activated carbon and zeolite are often used to adsorb and remove odorous substances in water, which have noticeable effects [99]. However, natural organic substances in ponds are also adsorbed, thus greatly reducing the adsorption capacity of activated carbon [100]. Ozone (O3) is a kind of oxidant used in water treatment because of its high oxidation potential. Under specific conditions, O3 catalyzes the decomposition of hydroxyl radicals to form highly oxidizing hydroxyl radicals and then oxidizes GSM and MIB [101]. However, Atasi et al. reported that conventional ozonation degradation of GSM and MIB has a strong dependence on the dose of ozone: when the dose reaches 8 mg/L, the removal rate is still less than 30%, and a high dose of ozone may cause toxic side effects on aquaculture [102,103]. There are other oxidation treatments for GSM and MIB, including ultraviolet (UV) radiation and advanced oxidation processes using different catalysts, and the combination of different treatments, such as UV−TiO2 photocatalysis [104] and the combined use of O3 and UV [105], can greatly improve the degradation rate.
A biological control method involves the introduction of specific microorganisms into the aquaculture environment to reduce the odor substances in water and fish through microbial metabolism. Compared with physical and chemical methods, this method is more environmentally friendly. To date, Bacillus spp. [106], Stenotro−phomonas spp. [107], Pseudomonas spp. [108], Enterobacter spp. [109], Micrococcus spp. [110], Flavobacterium spp. [111], and Brevibacterium spp. [110] have been found to be able to use GSM and MIB for normal metabolism. Although MIB and GSM can be removed by microbial degradation, the degradation rate is quite slow [108,110]. Biodegradation combined with photocatalysis has been proved to have the potential to repair natural water contaminated by odorous substances [112,113]. Fu et al. [114] developed a tightly coupled photocatalytic and biodegradation system to remove GSM and MIB, which significantly improved the removal efficiency of MIB and GSM.

4.2. Processing Treatment

4.2.1. Freezing

Decreasing the storage temperature is a common and natural preservation method used to increase the stability of fish and commercial fish products. Rahman et al. found that with an increase in storage temperature, the rate of lipid oxidation in dried grouper increases significantly [115]. It has been shown that −35 °C is the optimal temperature for maintaining high−quality fish for long−term storage [116]. Ultra−low−temperature storage (<−40 °C) can inhibit biochemical reactions, but the use of ultra−low−temperature storage has a negative impact on the structure of fish due to ice crystal generation and increases the possibility of fish tissue rupture and costs. Storage at −35 °C with oxygen barrier material packaging is sufficient to stabilize proteins, inhibit the formation of TMAO in fish tissue, and maintain good texture characteristics of lean fish. In addition, on the basis of a suitable temperature, increasing the freezing speed and reducing the size of ice can effectively reduce damage by ice crystals [117]. Furthermore, increasing the freezing rate also reduces the destructive effect of ice crystals, which effectively diminishes the size of the ice. The results showed that carp (Cyprinus carpio) samples treated with ultrasound−assisted immersion freezing (UIF) at 180W ultrasonic power reduced the freezing time compared to the control groups with no ultrasound treatment. Meanwhile, UIF was shown to retard the growth of TBARS and total volatile basic nitrogen values (TVB−N) when compared to air freezing (AF) and immersion freezing (IF) during storage [118].

4.2.2. Salting and Drying

Salting and drying have been applied to suppress the growth of Gram−negative bacteria and inhibit enzyme−related chemical reactions in meat products by reducing water activity [119]. In traditional manufacturing, fish fillets, fish pieces, or whole fish are exposed to a fluidized bed full of salt particles in hot and dried air, controlling the time and temperature of drying and salting. Drying produces a unique flavor of products, catering to the demands of consumers. There are also several different drying methods, such as natural sun, hot air, vacuum solar, electric heat, and microwave drying. Studies have indicated that sensory indices and the chemical composition of salted fish are not associated with different drying methods. However, the microwave drying efficiency outperforms that of other drying methods in terms of microbial bacteria [120,121].

4.2.3. High−Pressure Processing

High−pressure processing (HPP) can change cell morphology and damage major components, such as bacterial cell membranes and walls, as well as several organelles, reducing microbial loads within meat and seafood products. Meat products receive uniform treatment under high pressure and maintain high sensory quality due to its low impact on flavor [122]. It has been shown that HPP increases the hardness and springiness of frozen hake. Moreover, cooked hake is also influenced by HPP and obtains the best quality at 300 MPa during 6 months of frozen storage [123]. Meanwhile, HPP inactivates the endogenous cathepsin that easily causes the deterioration of chilled fillets; for instance, bluefish cathepsin C nearly lost its activity after treatment at 300 MPa for 30 min, providing better fish quality [124].

4.2.4. Boiling

Boiling can suppress lipid deterioration in fish in several ways, such as denaturing lipoxygenases, forming water−soluble antioxidants, and destroying heme compounds. As a result of heat treatment, the quantity of aldehydes in fish has been shown to drop to nearly undetectable levels due to carbonyl−amino reactions [125]. Meanwhile, Kim et al. indicated that the fish gelatin of dried anchovies was hydrolyzed after boiling, forming an invisible edible film that protected against oxidative rancidity [126]. Boiling could slow the lipid hydrolysis process of dried sardines but adversely led to the loss of PUFAs, ultimately damaging sensory characteristics during storage [127].

4.2.5. Fermenting

Bacteria as a starter have significant potential in improving the flavor of fish products. T. halophilus is used in the fermentation of fish sauce, which significantly improves the amino acid composition of the product and reduces the concentrations of undesirable flavor compounds, such as dimethyl disulfide and biogenic amines [128]. Similarly, in Thailand, Staphylococcus xylosus is used to produce fish sauce in order to change the flavor notes. As a result, the sensory evaluation indicated that the fishy, fecal, rancid, and sweaty notes of fish sauce inoculated with the bacterium were weaker than those of the fish sauce without treatment [129]. In addition, irradiation−assisted salting and fermentation can significantly improve sensory flavor characteristics, especially by reducing the typical fishy smell and improving color and microbial safety [130].

4.2.6. Defatting

Removing the fat from fish is a direct method used to inhibit unpleasant odors caused by lipid oxidation. Enzymes, organic solvents, and alkaline treatment can be used to achieve the effect of degreasing. For example, lipoxygenase extracted from marine macroalga reduced the undesirable odors of fish oil by site−specific cleavage of hydroperoxides, producing more desirable alcohols, aldehydes, and ketones, thus releasing fresh fish and fruit flavors [131]. The gelatins from seabass skin use citric acid and isopropanol alcohol to remove lipids, inhibiting the abundance of volatile compounds, thereby lowering fishy odors, the peroxide value, and TBARS [132]. The protein isolate separated by acid or alkaline solubilization and isoelectric precipitation from Nile tilapia and broad−head catfish had lower GSM and MIB concentrations as well as a negligible muddy odor [133,134]. In this regard, using a polar antioxidant can effectively prevent oxidation in protein isolates regardless of pH treatment [34].

4.2.7. Masking

Seasonings can be used as masking agents that are directly added to food during the cooking process to cover up unpleasant odors. Catfish fillets blended with lemon pepper and soaked in a food container satisfied the majority of evaluation panelists. Due to the presence of masking agents, the muddy/earthy odorant MIB was perceived less or even not at all [135]. Washed minced fish were treated with piper guineense and salt to make kamaboko. The addition of piper guineense increased the kamaboko score for taste and overall acceptability, as well as significantly reduced the microbial flora of kamaboko [136]. In India, Japan, China, and Southeast Asia, ginger is very suitable for fish dishes, bringing sensations of pungency and hotness to mask undesirable flavors. In addition to ginger, cumin, coriander, basil, mint, and celery are often used in Asian cuisine recipes [137].

4.3. Application of Additives

4.3.1. Synthetic Additives

Legal food additives with specified contents are indispensable in the industrial production of fish products. A food additive, which can be synthetic or natural, is normally not consumed as a food itself but is intentionally added to food to improve aroma, taste, texture, or shelf−life [138]. As undesirable flavors are primarily caused by oxidation, it is beneficial to add antioxidants to food systems in order to reduce oxidation. Antioxidants, such as propyl gallate (PG), butylated hydroxytoluene (BHT), butylated hydroxyanisole (BHA), tert−butylhydroxyquinone (TBHQ), vitamin E (tocopherol), vitamin C (ascorbic acid), phosphates, and citrate, have been used individually or in combination to suppress the oxidation process [139]. The addition of antimicrobial agents is also vital in inhibiting the development of microorganisms, thereby improving the appearance and flavor of fish products. Lactic, sorbic, and benzoic acids and their salts can be extracted directly or obtained synthetically and are effective organic compounds widely used as antimicrobial agents to prolong the sensory quality [140]. Nitrite is an ordinary synthetic antimicrobial compound that is used to control bacteria and fungi during meat preservation, such as Flavobacterium, Micrococcus, and Pseudomonas; however, its dosage is strictly controlled to prevent harm to the human body at high dosages [141]. Meanwhile, in industrial production, seasonings, antioxidants, and antibacterial agents (or preservatives) can be added to the product formulation according to regulations (e.g., in the United States, the additive must be GRAS−listed (Generally Recognized as Safe) according to the American Food and Drug Administration (USFDA, 2009). In Canada, it must fall under GMP (Good Manufacturing Practice) in accordance with the Canadian Food and Drug Act (HC, 2006). In China, it must comply with “National Food Safety Standards for Food Additives” (GB 2760−2014)). These active solutions can be used to spray and penetrate the raw fish product in order to control the odor [140].

4.3.2. Natural Additives

Great attention has been paid to natural additives because synthetic additives have been implicated as potentially toxic and carcinogenic hazards in past decades. With the overall improvement of living standards, natural materials with antioxidant activity became more popular for consumers. Immersion or coating is the conventional treatment for applying natural antioxidants to fish or other seafood. Clove water extract is applied to oven−dried omena fish (Rastrineobola argentea) by immersion, significantly reducing the concentrations of TBARS and peroxide values of omena fish [142]. Moreover, caffeic acid is an active antioxidant that prevents lipid oxidation in the minced white muscle of horse mackerel during frozen storage [143]. Furthermore, grape polyphenols can inhibit lipid oxidation in frozen minced fish muscle, protecting the endogenous antioxidant system of fatty fish [144,145]. Similarly, tea polyphenols effectively inhibit TMAO breakdown and the oxidation of lipids and therefore maintain the quality of dried−seasoned squid [146]. Tan and Shahidi demonstrated that phytosterol displayed an excellent antioxidant effect as well [147]. In general, active substances function as antioxidants through several action mechanisms, such as chelating prooxidative metal ions [148], scavenging free radicals, suppressing oxidative enzymes and reactive oxygen species, or interacting with bio−membranes [149].
Moreover, besides lipid oxidation, phenolic compounds can play a significant role in preventing microbial spoilage; for instance, catechin has been shown to have great antimicrobial activity against bacteria that produce H2S in fish and fish products [150]. Tannic acid was also reported to retard the growth of psychrophilic bacteria and inhibit the increase in the total viable count in striped catfish slices during refrigerated storage [151]. Citrus essential oil was shown to inhibit the growth of pathogenic and fungi flora in sea bass fillet [152]. Oregano (0.8%) [153], thyme (1%), and laurel essential oils (1%) [154] were also shown to improve the quality of fish. Interestingly, many studies have reported that essential oils contain phenolic compounds, such as eugenol, thymol, or carvacrol [155]. These phenolic compounds can lyse the cell walls of microorganisms, disrupt membrane proteins, further damage various enzymatic systems, and inactivate genetic material in order to strengthen their antimicrobial properties [156]. Recent research has also indicated that phenolic compounds can be chemically reactive with various food constituents, such as proteins, or directly react with volatile odor compounds to modify the product’s flavor [157,158]. Furthermore, bacteriocins, namely, small bacterial peptides, showed strong antimicrobial activity. Nisin has also been used to control the quality of snakehead fish fillets during cold storage [159].
Natural products, especially antioxidants and antimicrobial agents of natural origin, should be widely studied as safe alternatives to synthetic additives. Moreover, different plants and microbes should be screened qualitatively and quantitatively for the presence of potent active compounds and their potential uses in fish and fish products.

4.4. Packaging

4.4.1. Vacuum Packaging (VP)

With the decreasing usage of synthetic additives, the packaging, used as the last barrier, becomes more and more important before the distribution and storage of fish products. Preventing fishery products from coming into contact with oxygen is a precautionary measure against oxidative deterioration. Vacuum packaging (VP) and modified atmosphere packaging (MAP) of meat and meat products have gained importance in improving shelf−life and avoiding the development of rancidity [160]. In VP, there are no air gaps between the product and the packaging. Moreover, VP is used for packaging frozen fish or preserved fish products in order to prevent the formation of undesirable flavors from oxidation. However, due to the enhancement of trimethylamine formation under anaerobic conditions, VP is not recommended to apply to marine fish products [161].

4.4.2. Modified Atmosphere Packaging (MAP)

Carbon dioxide (CO2), nitrogen (N2), and oxygen (O2) are the principal gases in MAP, with each having different purposes and functions. Typically, CO2 is used to inhibit bacteria and mold, N2 is used to prevent lipid oxidation and package collapse, and O2 is used to prevent the growth of anaerobes [162]. In many fishery products, MAP with high CO2 has been proven to be more effective than VP in inhibiting the growth of spoilage microorganisms. CO2 can penetrate bacterial cytomembranes and influence cytoplasmic enzyme activity. Meanwhile, it is critical to control the storage temperature for MAP. Higher temperatures result in the reduction of dissolved CO2 within the product, leading to higher microbial and enzymatic activity and consequently damaging the quality of the product [163]. In addition, recent studies have indicated that super−chilling prior to MAP is a valuable measure that has a significant impact on bacterial inhibition. MAP super−chilled fillets were shown to have a longer shelf−life and lower bacterial counts compared to other chilled fillets [164].

4.4.3. Active Packaging (AP)

Active packaging (AP) techniques are concerned with substances that absorb oxygen, ethylene, moisture, CO2, and flavors/odors and those that release CO2, antimicrobial agents, antioxidants, and flavors [165]. In general, packaging materials need proper water and gas barrier capabilities as well as excellent sealing properties. In practical applications, polyethylene (PE) and polypropylene (PP) have excellent water barrier properties [166]. Ethylene vinyl alcohol (EVOH) exhibits excellent gas barrier properties [167]. These are synthetic polymers widely used in food packaging, but they cannot undergo physical, chemical, or biological degradation and have thus caused numerous severe environmental and health−related problems [168,169]. Therefore, there is an increasing interest in the development of environmentally friendly biodegradable polymers (i.e., biopolymers) for packaging materials. Biopolymers based on polysaccharides, proteins, and lipids from numerous plant and animal sources can be formed into either edible films or coatings and have suitable application properties [170,171]. Chitosan is one of the most popular polysaccharide biopolymers that can form a semipermeable film with intrinsic antimicrobial activity [172]. Blending active components in packaging material can also improve the barrier characteristics. For example, chitosan blended with various antimicrobial agents, such as tea tree essential oils and cinnamon oil, was made into an improved antimicrobial film to enhance the odor, texture, and color of trout fillets [173,174]. For wrapping dried anchovy, chitosan film containing acetic or propionic acid was shown to have a superior effect on oxidative stability compared to polyester–polyethylene laminate during five months of storage [175]. A growing trend of packaging is to integrate water absorbers, oxygen scavengers, and antimicrobial agents into the packaging material rather than apply them as individual sachets [176,177].

5. Conclusions

In recent years, in the pursuit of health, fish have been favored by consumers because they are rich in high−quality proteins and PUFAs. However, undesirable flavors limit consumers’ purchase and consumption. The undesirable flavors of fish are mainly due to the water quality in the aquaculture environment and deterioration reactions (enzymatic reactions, lipid autoxidation, and microbial actions). The synergistic effect of carbonyl compounds, alcohols, GSM, MIB, TMA, and other substances gives fish a worse flavor. In order to develop high−value fish products, odor removal from fish during production, processing, transportation, and consumption has been widely studied. Traditional methods, such as basic aquaculture management, salting, freezing, masking, and heat treatment, have been widely used in fish production and processing, but many of them require further improvement. More deodorization technologies for fish have been deeply explored, such as functional microbial degradation, ultrasonic irradiation, the addition of natural antioxidant and antimicrobial agents, and fresh−keeping packaging. Among them, due to the synergistic effect, the combined use of two or more deodorization strategies usually shows more effective results. At present, existing deodorization technologies and methods are diverse, but they have certain limitations and limited scopes of application. To sum up, it is necessary to establish a comprehensive, applicable, and efficient deodorization scheme that can satisfy consumers’ demand for better sensory quality of fish and fish products.

Author Contributions

T.W. and M.W.: Writing—Original Draft Preparation, Formal Analysis, Investigation, Methodology, and Writing—Review and Editing; P.W. and H.T.: Conceptualization, Supervision and Funding Acquisition; P.Z.: Writing—Review and Editing, Validation, Conceptualization, and Funding Acquisition. All authors have read and agreed to the published version of the manuscript.


This research was conducted with support from the Special Support Plan of Shaanxi Province (TZ0432), the Science and Technology Innovation Team of Shaanxi Province (2022TD-14), the Key Research and Development Program of Shaanxi Province (2022NY-144), and the Fundamental Research Funds for the Central Universities (GK202002004).

Conflicts of Interest

The authors declare no conflict of interest.


  1. Zhou, X.X.; Chong, Y.Q.; Ding, Y.T.; Gu, S.Q.; Liu, L. Determination of the effects of different washing processes on aroma characteristics in silver carp mince by MMSE-GC-MS, e-nose and sensory evaluation. Food Chem. 2016, 207, 205–213. [Google Scholar] [CrossRef] [PubMed]
  2. Smith, J.L.; Boyer, G.L.; Zimba, P.V. A review of cyanobacterial odorous and bioactive metabolites: Impacts and management alternatives in aquaculture. Aquaculture 2008, 280, 5–20. [Google Scholar] [CrossRef]
  3. Auffret, M.; Pilote, A.; Proulx, E.; Proulx, D.; Villemur, R. Establishment of a real-time pcr method for quantification of geosmin-producing Streptomyces spp. in recirculating aquaculture systems. Water Res. 2011, 45, 6753–6762. [Google Scholar] [CrossRef] [PubMed]
  4. Kawai, T.; Sakaguchi, M. Fish flavor. Crit. Rev. Food Sci. Nutr. 1996, 36, 257–298. [Google Scholar] [CrossRef] [PubMed]
  5. An, Y.; Qian, Y.L.; Alcazar Magana, A.; Xiong, S.; Qian, M.C. Comparative characterization of aroma compounds in silver carp (Hypophthalmichthys molitrix), pacific whiting (Merluccius productus), and alaska pollock (Theragra chalcogramma) surimi by aroma extract dilution analysis, odor activity value, and aroma recombination studies. J. Agric. Food Chem. 2020, 68, 10403–10413. [Google Scholar]
  6. Howgate, P. Tainting of farmed fish by geosmin and 2-methyliso-borneol: A review of sensory aspects and of ptake/depuration. Aquaculture 2004, 234, 155–181. [Google Scholar] [CrossRef]
  7. Alasalvar, C.; Taylor, K.D.A.; Zubcov, E.; Shahidi, F.; Alexis, M. Differentiation of cultured and wild sea bass (Dicentrarchus labrax): Total lipid content, fatty acid and trace mineral composition. Food Chem. 2002, 79, 145–150. [Google Scholar] [CrossRef]
  8. Frank, D.; Poole, S.; Kirchhoff, S.; Forde, C. Investigation of sensory and volatile characteristics of farmed and wild barramundi (Lates calcarifer) using gas chromatography-olfactometry mass spectrometry and descriptive sensory analysis. J. Agric. Food Chem. 2009, 57, 10302–10312. [Google Scholar] [CrossRef]
  9. Grigorakis, K.; Taylor, K.D.A.; Alexis, M.N. Organoleptic and volatile aroma compounds comparison of wild and cultured gilthead sea bream (Sparus aurata): Sensory differences and possible chemical basis. Aquaculture 2003, 225, 109–119. [Google Scholar] [CrossRef]
  10. Grigorakis, K. Compositional and organoleptic quality of farmed and wild gilthead sea bream (Sparus aurata) and sea bass (Dicentrarchus labrax) and factors affecting it: A review. Aquaculture 2007, 272, 55–75. [Google Scholar] [CrossRef]
  11. Shi, W.Z.; Ying, M.M.; Wang, X.C. Effect of seasons on volatile compounds in grass carp meat. Adv. Mater. Res. 2012, 554–556, 1565–1571. [Google Scholar] [CrossRef]
  12. Li, J.-L.; Tu, Z.-C.; Zhang, L.; Lin, D.-R.; Sha, X.-M.; Zeng, K.; Wang, H.; Pang, J.-J.; Tang, P.-P. Characterization of volatile compounds in grass carp (Ctenopharyngodon idellus) soup cooked using a traditional Chinese method by GC-MS. J. Food Process. Preserv. 2017, 41, e12995. [Google Scholar] [CrossRef]
  13. Josephson, D.B.; Lindsay, R.C. Enzymic generation of volatile aroma compounds from fresh fish. In Biogeneration of Aromas; American Chemical Society: Washington, DC, USA, 1986; pp. 201–219. [Google Scholar]
  14. Suffet, I.H.; Djanette, K.; Auguste, B. The drinking water taste and odor wheel for the millennium: Beyond geosmin and 2-methylisoborneol. Water Sci. Technol. 1999, 40, 1–13. [Google Scholar] [CrossRef]
  15. Lindholm-Lehto, P.C.; Vielma, J. Controlling of geosmin and 2-methylisoborneol induced off-flavours in recirculating aquaculture system farmed fish-A review. Aquac. Res. 2019, 50, 9–28. [Google Scholar] [CrossRef]
  16. Tucker, C.S.; Schrader, K.K. Off-flavors in pond-grown ictalurid catfish: Causes and management options. J. World Aquac. Soc. 2020, 51, 7–92. [Google Scholar] [CrossRef]
  17. Petersen, M.A.; Hyldig, G.; Strobel, B.W.; Henriksen, N.H.; Jørgensen, N.O.G. Chemical and sensory quantification of geosmin and 2-methylisoborneol in rainbow trout (Oncorhynchus mykiss) from recirculated aquacultures in relation to concentrations in basin water. J. Agric. Food Chem. 2011, 59, 12561–12568. [Google Scholar] [CrossRef]
  18. Liu, S.; Liao, T.; Mccrummen, S.T.; Hanson, T.R.; Wang, Y. Exploration of volatile compounds causing off-flavor in farm-raised channel catfish (Ictalurus punctatus) fillet. Aquac. Int. 2017, 25, 413–422. [Google Scholar] [CrossRef]
  19. Lee, J.; Rai, P.K.; Jeon, Y.J.; Kim, K.-H.; Kwon, E.E. The role of algae and cyanobacteria in the production and release of odorants in water. Environ. Pollut. 2017, 227, 252–262. [Google Scholar] [CrossRef]
  20. Podduturi, R.; Petersen, M.A.; Mahmud, S.; Rahman, M.M.; Jørgensen, N.O.G. Potential contribution of fish feed and phytoplankton to the content of volatile terpenes in cultured pangasius (Pangasianodon hypophthalmus) and tilapia (Oreochromis niloticus). J. Agric. Food Chem. 2017, 65, 3730–3736. [Google Scholar] [CrossRef]
  21. Mccrummen, S.T.; Wang, Y.; Hanson, T.R.; Bott, L.; Liu, S. Culture environment and the odorous volatile compounds present in pond-raised channel catfish (Ictalurus punctatus). Aquac. Int. 2018, 26, 685–694. [Google Scholar] [CrossRef]
  22. Guen, S.L.; Prost, C.; Demaimay, M. Characterization of odorant compounds of mussels (Mytilus edulis) according to their origin using gas chromatography-olfactometry and gas chromatography-mass spectrometry. J. Chromatogr. A 2000, 896, 361–371. [Google Scholar] [CrossRef]
  23. Varlet, V.; Fernandez, X. Review. Sulfur-containing volatile compounds in seafood: Occurrence, odorant properties and mechanisms of formation. Food Sci. Technol. Int. 2010, 16, 463–503. [Google Scholar] [CrossRef] [PubMed]
  24. Alasalvar, C.; Taylor, K.D.A.; Shahidi, F. Comparison of volatiles of cultured and wild sea bream (Sparus aurata) during storage in ice by dynamic headspace analysis/gas chromatography-mass spectrometry. J. Agric. Food Chem. 2005, 53, 2616–2622. [Google Scholar] [CrossRef] [PubMed]
  25. Hebard, C. Occurrence and significance of trimethylamine oxide and its derivatives in fish and shellfish. In Chemistry and Biochemistry of Marine Food Products; AVI: Westport, CT, USA, 1982; pp. 149–304. [Google Scholar]
  26. Triqui, R.; Bouchriti, N. Freshness assessments of moroccan sardine (Sardina pilchardus): Comparison of overall sensory changes to instrumentally determined volatiles. J. Agric. Food Chem. 2003, 51, 7540–7546. [Google Scholar] [CrossRef]
  27. Triqui, R. Sensory and flavor profiles as a means of assessing freshness of hake (Merluccius merluccius) during ice storage. Eur. Food Res. Technol. 2005, 222, 41–47. [Google Scholar] [CrossRef]
  28. Milo, C.; Grosch, W. Changes in the odorants of boiled trout (Salmo fario) as affected by the storage of the raw material. J. Agric. Food Chem. 1993, 41, 2366–2371. [Google Scholar] [CrossRef]
  29. Sae-Leaw, T.; Benjakul, S.; Gokoglu, N.; Nalinanon, S. Changes in lipids and fishy odour development in skin from nile tilapia (Oreochromis niloticus) stored in ice. Food Chem. 2013, 141, 2466–2472. [Google Scholar] [PubMed]
  30. Reineccius, G.A. Symposium on meat flavor off-flavors in meat and fish—A review. J. Food Sci. 1979, 44, 12–24. [Google Scholar] [CrossRef]
  31. Cui, L.; Decker, E.A. Phospholipids in foods: Prooxidants or antioxidants? J. Agric. Food Chem. 2016, 96, 18–31. [Google Scholar] [CrossRef]
  32. Vidal, N.P.; Manzanos, M.J.; Goicoechea, E.; Guillén, M.D. Farmed and wild sea bass (Dicentrarchus labrax) volatile metabolites: A comparative study by SPME-GC/MS. J. Sci. Food Agric. 2016, 96, 1181–1193. [Google Scholar]
  33. Josephson, D.B.; Lindsay, R.C.; Stuiber, D.A. Identification of compounds characterizing the aroma of fresh whitefish (Coregonus clupeaformis). J. Agric. Food Chem. 1983, 31, 326–330. [Google Scholar] [CrossRef]
  34. Raghavan, S.; Hultin, H.O. Effect of various antioxidants on the oxidative stability of acid and alkali solubilized muscle protein isolates. J. Food Biochem. 2010, 33, 163–175. [Google Scholar] [CrossRef]
  35. Jónsdóttir, R.; Bragadóttir, M.; Olafsdottir, G. The role of volatile compounds in odor development during hemoglobin-mediated oxidation of cod muscle membrane lipids. J. Aquat. Food Prod. Technol. 2007, 16, 67–86. [Google Scholar] [CrossRef]
  36. Fu, X.; Xu, S.; Wang, Z. Kinetics of lipid oxidation and off-odor formation in silver carp mince: The effect of lipoxygenase and hemoglobin. Food Res. Int. 2009, 42, 85–90. [Google Scholar] [CrossRef]
  37. Morita, K.; Kubota, K.; Aishima, T. Comparison of aroma characteristics of 16 fish species by sensory evaluation and gas chromatographic analysis. J. Sci. Food Agric. 2003, 83, 289–297. [Google Scholar] [CrossRef]
  38. Nomikos, T.; Karantonis, H.C.; Skarvelis, C.; Demopoulos, C.A.; Zabetakis, I. Antiatherogenic properties of lipid fractions of raw and fried fish. Food Chem. 2006, 96, 29–35. [Google Scholar] [CrossRef]
  39. Mansur, M.; Bhadra, A.; Takamura, H.; Matoba, T. Volatile flavor compounds of some sea fish and prawn species. Fish. Sci. 2003, 69, 864–866. [Google Scholar] [CrossRef]
  40. Sohn, J.-H.; Taki, Y.; Ushio, H.; Kohata, T.; Shioya, I.; Ohshima, T. Lipid oxidations in ordinary and dark muscles of fish: Influences on rancid off-odor development and color darkening of yellowtail flesh during ice storage. J. Food Sci. 2005, 70, s490–s496. [Google Scholar] [CrossRef]
  41. Hsieh, R.J.; Kinsella, J.E. Lipoxygenase generation of specific volatile flavor carbonyl compounds in fish tissues. J. Agric. Food Chem. 1989, 37, 279–286. [Google Scholar] [CrossRef]
  42. Prost, C.; Hallier, A.; Cardinal, M.; Serot, T.; Courcoux, P. Effect of storage time on raw sardine (Sardina pilchardus) flavor and aroma quality. J. Food Sci. 2004, 69, S198–S204. [Google Scholar] [CrossRef]
  43. Hsieh, R.J.; Kinsella, J.E. Oxidation of polyunsaturated fatty acids: Mechanisms, products, and inhibition with emphasis on fish. Adv. Food Nutr. Res. 1989, 33, 233–341. [Google Scholar] [PubMed]
  44. Xu, Y.; Liu, Y.; Jiang, C.; Zhang, C.; Li, X.; Zhu, D.; Li, J. Determination of volatile compounds in turbot (Psetta maxima) during refrigerated storage by headspace solid-phase microextraction and gas chromatography-mass spectrometry. J. Sci. Food Agric. 2014, 94, 2464–2471. [Google Scholar] [CrossRef] [PubMed]
  45. Patton, S.; Barnes, I.J.; Evans, L.E. n-Deca-2,4-dienal, its origin from linoleate and flavor significance in fats. J. Am. Oil Chem. Soc. 1959, 40, 280–283. [Google Scholar] [CrossRef]
  46. Swoboda, P.A.T.; Peers, K.E. Volatile odorous compounds responsible for metallic, fishy taint formed in butterfat by selective oxidation. J. Sci. Food Agric. 1977, 28, 1010–1018. [Google Scholar] [CrossRef]
  47. Fraser, O.P.; Sumar, S. Compositional changes and spoilage in fish (Part II)—Microbiological induced deterioration. Nutr. Food Sci. 1998, 98, 325–329. [Google Scholar] [CrossRef]
  48. Tesfay, S.; Teferi, M. Assessment of fish post-harvest losses in Tekeze dam and Lake Hashenge fishery associations: Northern Ethiopia. Agric. Food Secur. 2017, 6, 219. [Google Scholar] [CrossRef]
  49. Gram, L.; Huss, H.H. Microbiological spoilage of fish and fish products. Int. J. food Microbiol. 1996, 33, 121–137. [Google Scholar] [CrossRef]
  50. Parlapani, F.F.; Kormas, K.A.; Boziaris, I.S. Microbiological changes, shelf life and identification of initial and spoilage microbiota of sea bream fillets stored under various conditions using 16S rRNA gene analysis. J. Sci. Food Agric. 2015, 95, 2386–2394. [Google Scholar] [CrossRef]
  51. Alfaro, B.; Hernández, I.; Marc, Y.L.; Pin, C. Modelling the effect of the temperature and carbon dioxide on the growth of spoilage bacteria in packed fish products. Food Control 2013, 29, 429–437. [Google Scholar] [CrossRef]
  52. Broekaert, K.; Heyndrickx, M.; Herman, L.; Devlieghere, F.; Vlaemynck, G. Seafood quality analysis: Molecular identification of dominant microbiota after ice storage on several general growth media. Food Microbiol. 2011, 28, 1162–1169. [Google Scholar] [CrossRef]
  53. Dalgaard, P. Qualitative and quantitative characterization of spoilage bacteria from packed fish. Int. J. Food Microbiol. 1995, 26, 319–333. [Google Scholar] [CrossRef]
  54. Gonzalez, C.J. Psychrobacters and related bacteria in freshwater fish. J. Food Prot. 2000, 63, 315–321. [Google Scholar] [CrossRef] [PubMed]
  55. Gram, L.; Dalgaard, P. Fish spoilage bacteria—Problems and solutions. Curr. Opin. Biotechnol. 2002, 13, 262–266. [Google Scholar] [CrossRef]
  56. Parlapani, F.F.; Boziaris, I.S. Monitoring of spoilage and determination of microbial communities based on 16S rRNA gene sequence analysis of whole sea bream stored at various temperatures. LWT-Food Sci. Technol. 2016, 66, 553–559. [Google Scholar] [CrossRef]
  57. Nychas, G.-J.E.; Marshall, D.L.; Sofos, J.N. Meat, poultry, and seafood. In Food Microbiology: Fundamentals and Frontiers; ASM Press: Washington, DC, USA, 2007. [Google Scholar]
  58. Hickey, M.E.; Accumanno, G.M.; Mcintosh, D.M.; Blank, G.S.; Lee, J.L. Comparison of extracellular DNase- and protease-producing spoilage bacteria isolated from Delaware pond-sourced and retail channel catfish (Ictalurus punctatus). J. Sci. Food Agric. 2015, 95, 1024–1030. [Google Scholar] [CrossRef] [PubMed]
  59. Papadopoulos, V.; Chouliara, I.; Badeka, A.; Savvaidis, I.N.; Kontominas, M.G. Effect of gutting on microbiological, chemical, and sensory properties of aquacultured sea bass (Dicentrarchus labrax) stored in ice. Food Microbiol. 2003, 20, 411–420. [Google Scholar] [CrossRef]
  60. Gram, L.; Trolle, G.; Huss, H.H. Detection of specific spoilage bacteria from fish stored at low (0 °C) and high (20 °C) temperatures. Int. J. Food Microbiol. 1987, 4, 65–72. [Google Scholar] [CrossRef]
  61. Serio, A.; Fusella, G.C.; Lòpez, C.C.; Sacchetti, G.; Paparella, A. A survey on bacteria isolated as hydrogen sulfide-producers from marine fish. Food Control 2014, 39, 111–118. [Google Scholar] [CrossRef]
  62. Chen, H.-C.; Kung, H.-F.; Chen, W.-C.; Lin, W.-F.; Hwang, D.-F.; Lee, Y.-C.; Tsai, Y.-H. Determination of histamine and histamine-forming bacteria in tuna dumpling implicated in a food-borne poisoning. Food Chem. 2008, 106, 612–618. [Google Scholar] [CrossRef]
  63. Parlapani, F.F.; Mallouchos, A.; Haroutounian, S.A.; Boziaris, I.S. Volatile organic compounds of microbial and non-microbial origin produced on model fish substrate un-inoculated and inoculated with gilt-head sea bream spoilage bacteria. LWT-Food Sci. Technol. 2017, 78, 54–62. [Google Scholar] [CrossRef]
  64. Broekaert, K.; Noseda, B.; Heyndrickx, M.; Vlaemynck, G.; Devlieghere, F. Volatile compounds associated with Psychrobacter spp. and Pseudoalteromonas spp., the dominant microbiota of brown shrimp (Crangon crangon) during aerobic storage. Int. J. Food Microbiol. 2013, 166, 487–493. [Google Scholar] [CrossRef] [PubMed]
  65. Casaburi, A.; Piombino, P.; Nychas, G.-J.; Villani, F.; Ercolini, D. Bacterial populations and the volatilome associated to meat spoilage. Food Microbiol. 2015, 45, 83–102. [Google Scholar] [CrossRef] [PubMed]
  66. Nychas, G.J.E.; Drosinos, E.; Board, R.G. The microbiology of meat and poultry. In Chemical Changes in Stored Meat; Blackie Academic and Professional: London, UK, 1998; pp. 288–326. [Google Scholar]
  67. Ferrocino, I.; Storia, A.L.; Torrieri, E.; Musso, S.S.; Mauriello, G.; Villani, F.; Ercolini, D. Antimicrobial packaging to retard the growth of spoilage bacteria and to reduce the release of volatile metabolites in meat stored under vacuum at 1 °C. J. Food Prot. 2013, 76, 52–58. [Google Scholar] [CrossRef]
  68. Duflos, G.; Coin, V.M.; Cornu, M.; Antinelli, J.-F.; Malle, P. Determination of volatile compounds to characterize fish spoilage using headspace/mass spectrometry and solid-phase microextraction/gas chromatography/mass spectrometry. J. Sci. Food Agric. 2006, 86, 600–611. [Google Scholar] [CrossRef]
  69. Joffraud, J.J.; Leroi, F.; Roy, C.; Berdaguéb, J.L. Characterisation of volatile compounds produced by bacteria isolated from the spoilage flora of cold-smoked salmon. Int. J. Food Microbiol. 2001, 66, 175–184. [Google Scholar] [CrossRef]
  70. Ercolini, D.; Casaburi, A.; Nasi, A.; Ferrocino, I.; Monaco, R.D.; Ferranti, P.; Mauriello, G.; Villani, F. Different molecular types of Pseudomonas fragi have the same overall behaviour as meat spoilers. Int. J. Food Microbiol. 2010, 142, 120–131. [Google Scholar] [CrossRef] [PubMed]
  71. Karpas, Z.; Tilman, B.; Gdalevsky, R.; Lorber, A. Determination of volatile biogenic amines in muscle food products by ion mobility spectrometry. Anal. Chim. Acta 2002, 463, 155–163. [Google Scholar] [CrossRef]
  72. Zimba, P.V.; Tucker, C.S.; Mischke, C.C.; Grimm, C.C. Short-term effect of diuron on catfish pond ecology. N. Am. J. Aquac. 2002, 64, 16–23. [Google Scholar] [CrossRef]
  73. Zimba, P.V.; Boue, S.; Chatham, M.A.; Nonneman, D. Variants of microcystin in south-eastern USA channel catfish (Ictalurus punctatus Rafinesque) production ponds. SIL Proc. 1922–2010 2002, 28, 1163–1166. [Google Scholar] [CrossRef]
  74. Nicklisch, A.; Shatwell, T.; Köhler, J. Analysis and modelling of the interactive effects of temperature and light on phytoplankton growth and relevance for the spring bloom. J. Plankton Res. 2008, 30, 75–91. [Google Scholar] [CrossRef]
  75. McQueen, D.J.; Leam, D.R.S. Influence of water temperature and nitrogen to phosphorus ration the dominance of blue-green algae in lake St. George, Ontario. Can. J. Fish. Aquat. Sci. 1987, 44, 598–604. [Google Scholar] [CrossRef]
  76. Lehman, P.W.; Marr, K.; Boyer, G.L.; Acuna, S.; Teh, S.J. Long-term trends and causal factors associated with microcystis abundance and toxicity in San Francisco Estuary and implications for climate change impacts. Hydrobiologia 2013, 718, 141–158. [Google Scholar] [CrossRef]
  77. Paerl, H.W.; Huisman, J. Blooms like it hot. Science 2008, 320, 57–58. [Google Scholar] [CrossRef]
  78. Ginzburg, B.; Chalifa, I.; Zohary, T.; Hadas, O.; Dor, I.; Lev, O. Identification of oligosulphide odorous compounds and their source in the Lake of Galilee. Water Res. 1998, 32, 1789–1800. [Google Scholar] [CrossRef]
  79. Zorn, H.; Langhoff, S.; Sheibner, M.; Berger, R.G. Cleavage of β,β-carotene to flavor compounds by fungi. Appl. Microbiol. Biotechnol. 2003, 62, 331–336. [Google Scholar] [CrossRef]
  80. Yang, M.; Yu, J.W.; Li, Z.L.; Guo, Z.H.; Burch, M.; Lin, T.F. Taihu Lake not to blame for Wuxi’s woes. Science 2008, 319, 158. [Google Scholar] [CrossRef]
  81. Chen, J.; Xie, P.; Ma, Z.; Niu, Y.; Tao, M.; Deng, X.; Wang, Q. A systematic study on spatial and seasonal patterns of eight taste and odor compounds with relation to various biotic and abiotic parameters in Gonghu Bay of Lake Taihu, China. Sci. Total Environ. 2010, 409, 314–325. [Google Scholar] [CrossRef] [PubMed]
  82. Dickschat, J.S.; Nawrath, T.; Thiel, V.; Kunze, B.; Muller, R.; Schulz, S. Biosynthesis of the off-flavor 2-methylisoborneol by the myxobacterium Nannocystis exedens. Angew. Chem. Int. Ed. 2007, 46, 8287–8290. [Google Scholar] [CrossRef]
  83. Tucker, C.S. Off-flavor problems in aquaculture. Rev. Fish. Sci. 2000, 8, 45–88. [Google Scholar] [CrossRef]
  84. Zimba, P.V.; Grimm, C.C. A synoptic survey of musty/muddy odor metabolites and microcystin toxin occurrence and concentration in southeastern USA channel catfish (Ictalurus punctatus Ralfinesque) production ponds. Aquaculture 2003, 218, 81–87. [Google Scholar] [CrossRef]
  85. Gutierrez, R.; Whangchai, N.; Sompong, U.; Prarom, W.; Sugiura, N. Off-flavour in nile tilapia (Oreochromis niloticus) cultured in an integrated pond-cage culture system. Maejo Int. J. Sci. Technol. 2013, 7, 1–13. [Google Scholar]
  86. Houle, S.; Schrader, K.K.; François, N.R.L.; Comeau, Y.; Kharoune, M.; Summerfelt, S.T.; Savoie, A.; Vandenberg, G.W. Geosmin causes off-flavour in arctic charr in recirculating aquaculture systems. Aquac. Res. 2011, 42, 360–365. [Google Scholar] [CrossRef]
  87. Chung, H.Y.; Yung, I.K.S.; Ma, W.C.J.; Kim, J.S. Analysis of volatile components in frozen and dried scallops (Patinopecten yessoensis) by gas chromatography/mass spectrometry. Food Res. Int. 2002, 35, 43–53. [Google Scholar] [CrossRef]
  88. Guttman, L.; Rijn, J.V. Identification of conditions underlying production of geosmin and 2-methylisoborneol in a recirculating system. Aquaculture 2008, 279, 85–91. [Google Scholar] [CrossRef]
  89. Burr, G.S.; Wolters, W.R.; Schrader, K.K.; Summerfelt, S.T. Impact of depuration of earthy-musty off-flavors on fillet quality of atlantic salmon, salmo salar, cultured in a recirculating aquaculture system. Aquac. Eng. 2012, 50, 28–36. [Google Scholar] [CrossRef]
  90. Drake, S.L.; Drake, M.A.; Sanderson, R.; Daniels, H.V.; Yates, M.D. The effect of purging time on the sensory properties of aquacultured southern flounder (Paralichthys lethostigma). J. Sens. Stud. 2010, 25, 246–259. [Google Scholar] [CrossRef]
  91. Palmeri, G.; Turchini, G.M.; Marriott, P.J.; Morrison, P.; Silva, S. Biometric, nutritional and sensory characteristic modifications in farmed Murray cod (Maccullochella peelii peelii) during the purging process. Aquaculture 2009, 287, 354–360. [Google Scholar] [CrossRef]
  92. Green, B.W.; Schrader, K.K. Effect of stocking large channel catfish in a biofloc technology production system on production and incidence of common microbial off-flavor compounds. J. Aquac. Res. Dev. 2015, 6, 314. [Google Scholar]
  93. Lee, T.J.; Nakano, K.; Matsumara, M. Ultrasonic irradiation for blue-green algae bloom control. Environ. Technol. Lett. 2001, 22, 383–390. [Google Scholar] [CrossRef]
  94. Ahn, C.Y.; Park, M.H.; Joung, S.H.; Kim, H.S.; Jang, K.Y.; Oh, H.M. Growth inhibition of cyanobacteria by ultrasonic radiation: Laboratory and enclosure studies. Environ. Sci. Technol. 2003, 37, 3031–3037. [Google Scholar] [CrossRef]
  95. Tang, J.W.; Wu, Q.Y.; Hao, H.W.; Chen, Y.F.; Wu, M.S. Growth inhibition of the cyanobacterium Spirulina (Arthrospira) platensis by 1.7 MHz ultrasonic irradiation. J. Appl. Phycol. 2003, 15, 37–43. [Google Scholar] [CrossRef]
  96. Halliwell, B.; Gutteridge, J.M.C. Free radicals in biology and medicine. J. Free Radic. Biol. Med. 1999, 1, 331–332. [Google Scholar] [CrossRef]
  97. Tang, J.W.; Wu, Q.Y.; Hao, H.W.; Chen, Y.F.; Wu, M.S. Effect of 1.7 MHz ultrasound on a gas-vacuolate cyanobacterium and a gas-vacuole negative cyanobacterium. Colloids Surf. B 2004, 36, 115–121. [Google Scholar] [CrossRef] [PubMed]
  98. Nam-Koong, H.; Schroeder, J.P.; Petrick, G.; Schulz, C. Removal of the off-flavor compounds geosmin and 2-methylisoborneol from recirculating aquaculture system water by ultrasonically induced cavitation. Aquac. Eng. 2016, 70, 73–80. [Google Scholar] [CrossRef]
  99. Cook, D.; Newcombe, G.; Sztajnbok, P. The application of powdered activated carbon for mib and geosmin removal: Predicting pac doses in four raw waters. Water Res. 2001, 35, 1325–1333. [Google Scholar] [CrossRef]
  100. Newcombe, G.; Morrison, J.; Hepplewhite, C.; Knappe, D.R.U. Simultaneous adsorption of MIB and NOM onto activated carbon: II. Competitive effects. Carbon 2002, 40, 2147–2156. [Google Scholar] [CrossRef]
  101. Yao, W.K.; Qu, Q.Y.; Gunten, U.V.; Chen, C.; Yu, G.; Wang, Y.J. Comparison of methylisoborneol and geosmin abatement in surface water by conventional ozonation and an electro-peroxone process. Water Res. 2017, 108, 373–382. [Google Scholar] [CrossRef]
  102. Atasi, K.Z.; Chen, T.; Huddieston, J.I.; Young, C.C.; Suffet, I.H. Factor screening for ozonating the taste- and odor-causing compounds in source water at Detroit, USA. Water Sci. Technol. 1999, 40, 115–122. [Google Scholar] [CrossRef]
  103. Collivignarelli, C.; Sorlini, S. AOPs with ozone and UV radiation in drinking water: Contaminants removal and effects on disinfection byproducts formation. Water Sci. Technol. 2004, 49, 51–56. [Google Scholar] [CrossRef]
  104. Rodriguez-Gonzalez, L.; Pettit, S.L.; Zhao, W.; Michaels, J.T.; Kuhn, J.N.; Alcantar, N.A.; Ergas, S.J. Oxidation of off flavor compounds in recirculating aquaculture systems using UV-TiO2 photocatalysis. Aquaculture 2019, 502, 32–39. [Google Scholar] [CrossRef]
  105. Berlt, M.M.G.; Schneider, R.D.C.D.S.; Machado, Ê.L.; Kist, L.T. Comparative assessment of the degradation of 2-methylisoborneol and geosmin in freshwater using advanced oxidation processes. Environ. Technol. 2021, 42, 3832–3839. [Google Scholar] [CrossRef] [PubMed]
  106. Narayan, L.V.; III, W.J.N. Biological control: Isolation and bacterial oxidation of the taste- and-odor compound geosmin. J. Am. Water Work. Assoc. 1974, 66, 532–536. [Google Scholar] [CrossRef]
  107. Zhou, B.H.; Yuan, R.F.; Shi, C.H.; Yu, L.Y.; Gu, J.N.; Zhang, C.L. Biodegradation of geosmin in drinking water by novel bacteria isolated from biologically active carbon. J. Environ. Sci. 2011, 23, 816–823. [Google Scholar] [CrossRef]
  108. Izaguirre, G.; Wolfe, R.L.; Means, E.G. Degradation of 2-methylisoborneol by aquatic bacteria. Appl. Environ. Microbiol. 1988, 54, 2424–2431. [Google Scholar] [CrossRef]
  109. Elhadi, S.L.N.; Huck, P.M.; Slawson, R.M. Factors affecting the removal of geosmin and MIB in drinking water biofilters. J. Am. Water Work. Assoc. 2006, 98, 108–119. [Google Scholar] [CrossRef]
  110. Yuan, R.; Zhou, B.; Shi, C.; Yu, L.; Zhang, C.; Gu, J. Biodegradation of 2-methylisoborneol by bacteria enriched from biological activated carbon. Front. Environ. Sci. Eng. 2012, 6, 701–710. [Google Scholar] [CrossRef]
  111. Clercin, N.A.; Druschel, G.K.; Gray, M. Occurrences of 2-methylisoborneol and geosmin-degrading bacteria in a eutrophic reservoir and the role of cell-bound versus dissolved fractions. J. Environ. Manag. 2021, 297, 113304. [Google Scholar] [CrossRef] [PubMed]
  112. Li, G.; Park, S.; Kang, D.W.; Krajmalnik-Brown, R.; Rittmann, B.E. 2,4,5-Trichlorophenol degradation using a novel TiO2-coated biofilm carrier: Roles of adsorption, photocatalysis, and biodegradation. Environ. Sci. Technol. 2011, 45, 8359–8367. [Google Scholar] [CrossRef]
  113. Li, G.; Park, S.; Rittmann, B. Degradation of reactive dyes in a photocatalytic circulating-bed biofilm reactor. Biotechnol. Bioeng. 2012, 109, 884–893. [Google Scholar] [CrossRef]
  114. Fu, S.Y.; Zhao, X.Y.; Zhou, Z.; Li, M.Y.; Zhu, L. Effective removal of odor substances using intimately coupled photocatalysis and biodegradation system prepared with the silane coupling agent (SCA)-enhanced TiO2 coating method. Water Res. 2021, 188, 116569. [Google Scholar] [CrossRef]
  115. Rahman, M.S.; Al-Belushi, R.M.; Guizani, N.; Al-Saidi, G.S.; Soussi, B. Fat oxidation in freeze-dried grouper during storage at different temperatures and moisture contents. Food Chem. 2009, 114, 1257–1264. [Google Scholar] [CrossRef]
  116. Tolstorebrov, I.; Eikevik, T.M.; Bantle, M. Effect of low and ultra-low temperature applications during freezing and frozen storage on quality parameters for fish. Int. J. Refrig. 2016, 63, 37–47. [Google Scholar] [CrossRef]
  117. Indergård, E.; Tolstorebrov, I.; Larsen, H.; Eikevik, T.M. The influence of long-term storage, temperature and type of packaging materials on the quality characteristics of frozen farmed Atlantic salmon (Salmo salar). Int. J. Refrig. 2014, 41, 27–36. [Google Scholar] [CrossRef]
  118. Sun, Q.; Sun, F.; Xia, X.; Xu, H.; Kong, B. The comparison of ultrasound-assisted immersion freezing, air freezing and immersion freezing on the muscle quality and physicochemical properties of common carp (Cyprinus carpio) during freezing storage-sciencedirect. Ultrason. Sonochem. 2019, 51, 281–291. [Google Scholar] [CrossRef]
  119. Qiu, X.; Chen, S.; Lin, H. Oxidative stability of dried seafood products during processing and storage: A review. J. Aquat. Food Prod. Technol. 2019, 28, 329–340. [Google Scholar] [CrossRef]
  120. Wu, T.; Mao, L. Influences of hot air drying and microwave drying on nutritional and odorous properties of grass carp (Ctenopharyngodon idellus) fillets. Food Chem. 2008, 110, 647–653. [Google Scholar] [CrossRef]
  121. Al-Rubai, H.H.; Hassan, K.H.A.; Eskandder, M.Z. Drying and salting fish using different methods and their effect on the sensory, chemical and microbial indices. Multidiscip. Rev. 2020, 3, e2020003. [Google Scholar] [CrossRef]
  122. Simonin, H.; Duranton, F.; Lamballerie, M.D. New insights into the high-pressure processing of meat and meat products. Compr. Rev. Food Sci. Food Saf. 2012, 11, 285–306. [Google Scholar] [CrossRef]
  123. Pita-Calvo, C.; Guerra-Rodríguez, E.; Saraiva, J.A.; Aubourg, S.P.; Vázquez, M. Effect of high-pressure processing pretreatment on the physical properties and colour assessment of frozen european hake (Merluccius merluccius) during long term storage. Food Res. Int. 2018, 112, 233–240. [Google Scholar] [CrossRef]
  124. Campus, M. High pressure processing of meat, meat products and seafood. Food Eng. Rev. 2010, 2, 256–273. [Google Scholar] [CrossRef]
  125. Salum, P.; Guclu, G.; Selli, S. Comparative evaluation of key aroma-active compounds in raw and cooked red mullet (Mullus barbatus) by aroma extract dilution analysis. J. Agric. Food Chem. 2017, 65, 8402–8408. [Google Scholar] [CrossRef]
  126. Kim, H.J.; Son, K.T.; Lee, S.G.; Park, S.Y.; Heu, M.S.; Kim, J.S. Suppression of lipid deterioration in boiled-dried anchovy by coating with fish gelatin hydrolysates. J. Food Biochem. 2017, 41, e12331. [Google Scholar] [CrossRef]
  127. Cyprian, O.O.; Nguyen, M.V.; Sveinsdottir, K.; Tomasson, T.; Arason, S. Influence of blanching treatment and drying methods on the drying characteristics and quality changes of dried sardine (Sardinella gibbosa) during storage. Dry. Technol. 2016, 35, 478–489. [Google Scholar] [CrossRef]
  128. Udomsil, N.; Rodtong, S.; Choi, Y.J.; Hua, Y.; Yongsawatdigul, J. Use of Tetragenococcus halophilus as a starter culture for flavor improvement in fish sauce fermentation. J. Agric. Food Chem. 2011, 59, 8401–8408. [Google Scholar] [CrossRef] [PubMed]
  129. Fukami, K.; Funatsu, Y.; Kawasaki, K.; Watabe, S. Improvement of fish-sauce odor by treatment with bacteria isolated from the fish-sauce mush (Moromi) made from frigate mackerel. J. Food Sci. 2004, 69, 45–49. [Google Scholar] [CrossRef]
  130. Kim, J.H.; Ahn, H.J.; Yook, H.S.; Kim, K.S.; Rhee, M.S.; Ryu, G.H.; Byun, M.W. Color, flavor, and sensory characteristics of gamma-irradiated salted and fermented anchovy sauce. Radiat. Phys. Chem. 2004, 69, 179–187. [Google Scholar] [CrossRef]
  131. Hu, S.P.; Pan, B.S. Modification of fish oil aroma using a macroalgal lipoxygenase. J. Am. Oil Chem. Soc. 2000, 77, 343–348. [Google Scholar] [CrossRef]
  132. Sae-leaw, T.; Benjakul, S.; O’Brien, N.M. Effects of defatting and tannic acid incorporation during extraction on properties and fishy odour of gelatin from seabass skin. LWT-Food Sci. Technol. 2016, 65, 661–667. [Google Scholar] [CrossRef]
  133. Yarnpakdee, S.; Benjakul, S.; Penjamras, P.; Kristinsson, H.G. Chemical compositions and muddy flavour/odour of protein hydrolysate from nile tilapia and broadhead catfish mince and protein isolate. Food Chem. 2014, 142, 210–216. [Google Scholar] [CrossRef]
  134. Abdollahi, M.; Undeland, I. Structural, functional, and sensorial properties of protein isolate produced from salmon, cod, and herring by-products. Food Bioprocess Technol. 2018, 11, 1733–1749. [Google Scholar] [CrossRef]
  135. Bett, K.L.; Ingram, D.A.; Grimm, C.C.; Vinyard, B.T.; Boyette, K.D.C.; Dionigi, C.P. Alteration of the sensory perception of the muddy/earthy odorant 2-methylisoborneol in channel catfish Ictalurus punctatus fillet tissues by addition of seasonings. J. Sens. Stud. 2000, 15, 459–472. [Google Scholar] [CrossRef]
  136. Negbenebor, C.A.; Godiya, A.A.; Igene, J.O. Evaluation of Clarias anguillaris treated with spice (Piper guineense) for washed mince and kamaboko-type product. J. Food Compos. Anal. 1999, 12, 315–322. [Google Scholar] [CrossRef]
  137. Nair, K.P.P. Ginger as a spice and flavorant. In The Agronomy and Economy of Turmeric and Ginger; Elsevier: Amsterdam, The Netherlands, 2013; pp. 497–510. [Google Scholar]
  138. Pressman, P.; Clemens, R.; Hayes, W.; Reddy, C. Food additive safety: A review of toxicologic and regulatory issues. Toxicol. Res. Appl. 2017, 1, 1–22. [Google Scholar] [CrossRef]
  139. Ladikos, D.; Lougovois, V. Lipid oxidation in muscle foods: A review. Food Chem. 1990, 35, 295–314. [Google Scholar] [CrossRef]
  140. Lucera, A.; Costa, C.; Conte, A.; Nobile, M.A.D. Food applications of natural antimicrobial compounds. Front. Microbiol. 2012, 3, 287. [Google Scholar] [CrossRef]
  141. Dave, D.; Ghaly, A.E. Meat spoilage mechanisms and preservation techniques: A critical review. Am. J. Agric. Biol. Sci. 2011, 6, 486–510. [Google Scholar]
  142. Slavin, M.; Dong, M.; Gewa, C. Effect of clove extract pretreatment and drying conditions on lipid oxidation and sensory discrimination of dried omena (Rastrineobola argentea) fish. Int. J. Food Sci. Technol. 2016, 51, 2376–2385. [Google Scholar] [CrossRef]
  143. Medina, I.; González, M.J.; Iglesias, J.; Hedges, N.D. Effect of hydroxycinnamic acids on lipid oxidation and protein changes as well as water holding capacity in frozen minced horse mackerel white muscle. Food Chem. 2009, 114, 881–888. [Google Scholar] [CrossRef]
  144. Pazos, M.; Gallardo, J.M.; Torres, J.L.; Medina, I. Activity of grape polyphenols as inhibitors of the oxidation of fish lipids and frozen fish muscle. Food Chem. 2005, 92, 547–557. [Google Scholar] [CrossRef]
  145. Pazos, M.; González, M.J.; Gallardo, J.M.; Torres, J.L.; Medina, I. Preservation of the endogenous antioxidant system of fish muscle by grape polyphenols during frozen storage. Eur. Food Res. Technol. 2005, 220, 514–519. [Google Scholar] [CrossRef]
  146. Dong, L.; Zhu, J.; Li, X.; Li, J. Effect of tea polyphenols on the physical and chemical characteristics of dried-seasoned squid (Dosidicus gigas) during storage. Food Control 2013, 31, 586–592. [Google Scholar] [CrossRef]
  147. Tan, Z.; Shahidi, F. Chemoenzymatic synthesis of phytosteryl ferulates and evaluation of their antioxidant activity. J. Agric. Food Chem. 2011, 59, 12375–12383. [Google Scholar] [CrossRef] [PubMed]
  148. Galati, G.; Lin, A.; Sultan, A.M.; O’Brien, P.J. Cellular and in vivo hepatotoxicity caused by green tea phenolic acids and catechins. Free Radic. Biol. Med. 2006, 40, 570–580. [Google Scholar] [CrossRef]
  149. Maqsood, S.; Benjakul, S.; Shahidi, F. Emerging role of phenolic compounds as natural food additives in fish and fish products. Crit. Rev. Food Sci. Nutr. 2013, 53, 162–179. [Google Scholar] [CrossRef] [PubMed]
  150. Nirmal, N.P.; Benjakul, S. Melanosis and quality changes of pacific white shrimp (Litopenaeus vannamei) treated with catechin during iced storage. J. Agric. Food Chem. 2009, 57, 3578–3586. [Google Scholar] [CrossRef] [PubMed]
  151. Maqsood, S.; Benjakul, S. Synergistic effect of tannic acid and modified atmospheric packaging on the prevention of lipid oxidation and quality losses of refrigerated striped catfish slices. Food Chem. 2010, 121, 29–38. [Google Scholar] [CrossRef]
  152. Boulares, M.; Moussa, O.B.; Mankai, M.; Sadok, S.; Hassouna, M. Effects of lactic acid bacteria and citrus essential oil on the quality of vacuum-packed sea bass (Dicentrarchus labrax) fillets during refrigerated storage. J. Aquat. Food Prod. Technol. 2018, 27, 698–711. [Google Scholar] [CrossRef]
  153. Goulas, A.E.; Kontominas, M.G. Combined effect of light salting, modified atmosphere packaging and oregano essential oil on the shelf-life of sea bream (Sparus aurata): Biochemical and sensory attributes. Food Chem. 2007, 100, 287–296. [Google Scholar] [CrossRef]
  154. Erkan, N.; Tosun, Ş.Y.; Ulusoy, Ş.; Üretener, G. The use of thyme and laurel essential oil treatments to extend the shelf life of bluefish (Pomatomus saltatrix) during storage in ice. J. Verbr. Lebensm. 2011, 6, 39–48. [Google Scholar] [CrossRef]
  155. Jayasena, D.D.; Jo, C. Essential oils as potential antimicrobial agents in meat and meat products: A review. Trends Food Sci. Technol. 2013, 34, 96–108. [Google Scholar] [CrossRef]
  156. Burt, S. Essential oils: Their antibacterial properties and potential applications in foods-a review. Int. J. Food Microbiol. 2004, 94, 223–253. [Google Scholar] [CrossRef] [PubMed]
  157. Guo, A.; Xiong, Y.L. Myoprotein-phytophenol interaction: Implications for muscle food structure-forming properties. Compr Rev Food Sci Food Saf. 2021, 20, 2801–2824. [Google Scholar] [CrossRef] [PubMed]
  158. Jeong, S.; Lee, H.G.; Cho, C.H.; Yoo, S.R. Deodorization films based on polyphenol compound-rich natural deodorants and polycaprolactone for removing volatile sulfur compounds from kimchi. J. Food Sci. 2021, 86, 1004–1013. [Google Scholar] [CrossRef] [PubMed]
  159. Lu, F.; Ding, Y.; Ye, X.; Liu, D. Cinnamon and nisin in alginate-calcium coating maintain quality of fresh northern snakehead fish fillets. LWT-Food Sci. Technol. 2010, 43, 1331–1335. [Google Scholar] [CrossRef]
  160. Flick, G.J.; Hong, G.-P.; Knobl, G.M. Lipid oxidation of seafood during storage. In Lipid Oxidation in Food; ACS: Washington, DC, USA, 1992; pp. 183–207. [Google Scholar]
  161. Noseda, B.; Vermeulen, A.; Ragaert, P.; Devlieghere, F. Packaging of fish and fishery products. In Seafood Processing: Technology, Quality and Safety; Wiley: Chichester, UK, 2013; pp. 237–261. [Google Scholar]
  162. Narasimha Rao, D.; Sachindra, N.M. Modified atmosphere and vacuum packaging of meat and poultry products. Food Rev. Int. 2002, 18, 263–293. [Google Scholar] [CrossRef]
  163. Sivertsvik, M.; Jeksrud, W.K.; Rosnes, J.T. A review of modified atmosphere packaging of fish and fishery products—Significance of microbial growth, activities and safety. Int. J. Food Sci. Technol. 2002, 37, 107–127. [Google Scholar] [CrossRef]
  164. Hansen, A.Å.; Mørkøre, T.; Rudi, K.; Langsrud, Ø.; Eie, T. The combined effect of superchilling and modified atmosphere packaging using CO2 emitter on quality during chilled storage of pre-rigor salmon fillets (Salmo salar). J. Sci. Food Agric. 2009, 89, 1625–1633. [Google Scholar] [CrossRef]
  165. Vermeiren, L.; Devlieghere, F.; Beest, M.V.; Beest, M.V.; Kruijf, N.D.; Debevere, J. Developments in the active packaging of foods. Trends Food Sci. Technol. 2004, 10, 77–86. [Google Scholar] [CrossRef]
  166. Tyagi, P.; Salem, K.S.; Hubbe, M.A.; Pal, L. Advances in barrier coatings and film technologies for achieving sustainable packaging of food products—A review. Trends Food Sci. Technol. 2021, 115, 461–485. [Google Scholar] [CrossRef]
  167. Maes, C.; Luyten, W.; Herremans, G.; Peeters, R.; Carleer, R.; Buntinx, M. Recent Updates on the Barrier Properties of Ethylene Vinyl Alcohol Copolymer (EVOH): A Review. Polym. Rev. 2018, 58, 209–246. [Google Scholar] [CrossRef]
  168. Shaikh, S.; Yaqoob, M.; Aggarwal, P. An overview of biodegradable packaging in food industry. Curr. Res. Food Sci. 2021, 4, 503–520. [Google Scholar] [CrossRef] [PubMed]
  169. Jafarzadeh, S.; Salehabadi, A.; Nafchi, A.M.; Oladzadabbasabadi, N.; Jafari, S.M. Cheese packaging by edible coatings and biodegradable nanocomposites; improvement in shelf life, physicochemical and sensory properties. Trends Food Sci. Technol. 2021, 116, 218–231. [Google Scholar] [CrossRef]
  170. Mohamed, S.A.A.; El-Sakhawy, M.; El-Sakhawy, M.A.-M. Polysaccharides, protein and lipid -based natural edible films in food packaging: A review. Carbohydr. Polym. 2020, 238, 116178. [Google Scholar] [CrossRef] [PubMed]
  171. Debeaufort, F.; Quezada-Gallo, J.A.; Voilley, A. Edible films and coatings: Tomorrow’s packagings: A review. Crit. Rev. Food Sci. Nutr. 1998, 38, 299–313. [Google Scholar] [CrossRef]
  172. Shahidi, F.; Arachchi, J.K.V.; Jeon, Y.J. Food applications of chitin and chitosans. Trends Food Sci. Technol. 1999, 10, 37–51. [Google Scholar] [CrossRef]
  173. van den Broek, L.A.M.; Knoop, R.J.I.; Kappen, F.H.J.; Boeriu, C.G. Chitosan films and blends for packaging material. Carbohydr. Polym. 2015, 116, 237–242. [Google Scholar] [CrossRef]
  174. Ojagh, S.M.; Rezaei, M.; Razavi, S.H.; Hosseini, S.M.H. Effect of chitosan coatings enriched with cinnamon oil on the quality of refrigerated rainbow trout. Food Chem. 2010, 120, 193–198. [Google Scholar] [CrossRef]
  175. Vimaladevi, S.; Panda, S.K.; Xavier, K.A.M.; Bindu, J. Packaging performance of organic acid incorporated chitosan films on dried anchovy (Stolephorus indicus). Carbohydr. Polym. 2015, 127, 189–194. [Google Scholar] [CrossRef]
  176. Restuccia, D.; Spizzirri, U.G.; Parisi, O.I.; Cirillo, G.; Curcio, M.; Iemma, F.; Puoci, F.; Vinci, G.; Picci, N. New EU regulation aspects and global market of active and intelligent packaging for food industry applications. Food Control 2010, 21, 1425–1435. [Google Scholar] [CrossRef]
  177. Malhotra, B.; Keshwani, A.; Kharkwal, H. Antimicrobial food packaging: Potential and pitfalls. Front. Microbiol. 2015, 6, 611. [Google Scholar] [CrossRef]
Figure 1. Freshness assessment of iced−stored sardine with emphasis on odor development according to EU grading and QIM (the EU grade is the European Union grade; the QIM score is the Quality Index Method score). The EU freshness grading distinguishes four categories of fish, from E (very fresh state), A, and B to C (not admitted). The QIM uses many weighted parameters (e.g., appearance, eyes, cover, and gills) with a scoring system from 0 to 4 demerit points for each parameter; it gives a total score of zero to very fresh fish and returns an increasingly larger result as fish deteriorates [26].
Figure 1. Freshness assessment of iced−stored sardine with emphasis on odor development according to EU grading and QIM (the EU grade is the European Union grade; the QIM score is the Quality Index Method score). The EU freshness grading distinguishes four categories of fish, from E (very fresh state), A, and B to C (not admitted). The QIM uses many weighted parameters (e.g., appearance, eyes, cover, and gills) with a scoring system from 0 to 4 demerit points for each parameter; it gives a total score of zero to very fresh fish and returns an increasingly larger result as fish deteriorates [26].
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Figure 2. Proposed mechanism for biochemical reactions of eicosapentaenoic acid.
Figure 2. Proposed mechanism for biochemical reactions of eicosapentaenoic acid.
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Figure 3. Enzymatic degradation of cysteine and methionine, generating DMS.
Figure 3. Enzymatic degradation of cysteine and methionine, generating DMS.
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Figure 4. (a) Biosynthesis of MIB via methylation of geranyldiphosphate (GPP) and cyclization of (E) −−2−−geranyldiphosphate; (b) biosynthesis of GSM via 1,2−−hydride shift, loss of hydroxypropyl moiety, and capture of water.
Figure 4. (a) Biosynthesis of MIB via methylation of geranyldiphosphate (GPP) and cyclization of (E) −−2−−geranyldiphosphate; (b) biosynthesis of GSM via 1,2−−hydride shift, loss of hydroxypropyl moiety, and capture of water.
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Table 1. The main volatiles derived from lipids contributing to off−flavors.
Table 1. The main volatiles derived from lipids contributing to off−flavors.
No.Off−FlavorsOriginOxidation CausesRefs.
11−Penten−3−olEicosapentaenoic acid15−Lipoxygenase[13]
2(E)−2−PentenalLinolenic acid, docosahexaenoic acid
/n−3 polyunsaturated fatty acids
3HexanalLinoleic acid
/n−6 Polyunsaturated fatty acids
4(E)−3−Hexen−1−olEicosapentaenoic acid15−Lipoxygenase[13]
5(E)−2−HexenalLinolenic acid
/n−3 polyunsaturated fatty acids
6Heptanaln−6 Polyunsaturated fatty acidsAutoxidation[42,43,44]
71−Octen−3−olArachidonic acid, linoleic acid
/n−6 polyunsaturated fatty acids
8(Z)−1,5−Octadien−3−oneEicosapentaenoic acid
/n−3 polyunsaturated fatty acids
9Nonanaln−9 Polyunsaturated fatty acids12−Lipoxygenase[42,43]
10(E)−2−NonenalLinoleic acid, arachidonic acid12−Lipoxygenase[43]
11(E,Z)−2,6−NonadienalEicosapentaenoic acid
/n−3 polyunsaturated fatty acids
122,4−Heptadienal (two isomers)Linolenic acid
/n−3 polyunsaturated fatty acids
132,4−Decadienal (two isomers)Linoleic acidAutoxidation[45]
14Short− and branched−chain fatty acids (e.g., butanoic, 2−/3−methylbutanoic, hexanoic, and octanoic acids)Fatty acidsAutoxidation[46]
Table 2. Specific spoilage microflora dominating in fresh fish meat during cold storage under different gas atmospheres.
Table 2. Specific spoilage microflora dominating in fresh fish meat during cold storage under different gas atmospheres.
Gas CompositionMicroflora
AirS. putrefaciens, Pseudomonas spp.
>50% CO2 with O2B. thermosphacta, S. putrefaciens
50% CO2P. phosphoreum, Lactic acid bacteria
50% CO2 with O2P. phosphoreum, Lactic acid bacteria, B. thermosphacta
100% CO2Lactic acid bacteria
Vacuum packagedPseudomonas spp.
From Reference [57].
Table 3. VOCs that common bacteria (e.g., Pseudomonas spp. and Shewanella spp.) produce in fish during aerobic storage and their precursors and attributes.
Table 3. VOCs that common bacteria (e.g., Pseudomonas spp. and Shewanella spp.) produce in fish during aerobic storage and their precursors and attributes.
CompoundsPseudomonasShewanellaLactic Acid Bacteria (LAB)Precursor(s)Flavor DescriptorsRefs.
2−Methyl−1−butanolYY/IsoleucineMalt, wine, onion[63,64]
3−Methyl−1−butanolYYYLeucineWhiskey, malty, burnt[63,64]
EthanolYYYGlucoseAlcoholic, ethereal, medical[63,65]
2−Methylbutanal//YIsoleucineCocoa, coffee, fruit[63,66]
3−Methylbutanal//YLeucineSweet, malty, sour[63,66]
Benzene acetaldehyde//YPhenylalanineSweet, honey sweet[67]
3−Hydroxy−2−butanone//YGlucoseButter, creamy, dairy, milk, fatty[63,68]
2−HeptanoneYY/Fatty acidFruity, spicy[63,69]
Ethyl acetateNAD/YMultiple originsEthereal, fruit, sweet[68]
Ethyl octanoateY/NADMultiple originsfruit, fat[63,70]
3−Methylbutyl acetate//YMultiple originsFruit, sweet, banana, ripe[63,69]
Organic acids
Acetic acid/YYGlucosePungent sour[55,63,69]
Sulfur compounds
Hydrogen sulfide/YYCystine, cysteine, methionineRotten eggs[23,69]
MethanethiolYY/Methionine, cysteineSulfur, gasoline, garlic[23,49,64]
Dimethyl sulfideYY/Methanethiol, methionine, cysteineCabbage, sulfur, gasoline[23,49]
Dimethyl disulfideYY/Methionine, cysteineOnion, cabbage, putrid[23,63,64]
Dimethyl trisulfideYY/Methionine, methanethiol, cysteineSulfur, fish, cabbage[23,69]
Nitrogen compounds
AmmoniaNADNADNADAmino acids
(e.g., arginine, histidine, tyrosine)
Trimethylamine/Y/Trimethylamine oxideFishy, oily, rancid, sweaty[49,68,71]
NAD, no available data; Y, can produce; /, cannot produce. Flavor descriptors according to: Flavornet (, accessed on 13 June 2022); The Good Scents Company (, accessed on 13 June 2022); The kinds of volatile compounds are in a bold.
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Wu, T.; Wang, M.; Wang, P.; Tian, H.; Zhan, P. Advances in the Formation and Control Methods of Undesirable Flavors in Fish. Foods 2022, 11, 2504.

AMA Style

Wu T, Wang M, Wang P, Tian H, Zhan P. Advances in the Formation and Control Methods of Undesirable Flavors in Fish. Foods. 2022; 11(16):2504.

Chicago/Turabian Style

Wu, Tianle, Meiqian Wang, Peng Wang, Honglei Tian, and Ping Zhan. 2022. "Advances in the Formation and Control Methods of Undesirable Flavors in Fish" Foods 11, no. 16: 2504.

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