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Article

Evaluation of Lipid Damage, Microbial Spoilage and Sensory Acceptance of Chilled Pouting (Trisopterus luscus), an Underutilized Lean Fish Species

by
Julio Maroto
1,
Marcos Trigo
2,
José M. Miranda
3,
Santiago P. Aubourg
2,* and
Jorge Barros-Velázquez
3
1
Área Tecnología de los Productos Pesqueros, Centro Tecnológico del Mar CETMAR, C/Eduardo Cabello s/n, Bouzas, E-36208 Vigo, Spain
2
Department of Food Technology, Marine Research Institute (CSIC), E-36208 Vigo, Spain
3
Department of Analytical Chemistry, Nutrition and Food Science, School of Veterinary Sciences, University of Santiago de Compostela, E-27002 Lugo, Spain
*
Author to whom correspondence should be addressed.
Appl. Sci. 2024, 14(16), 6905; https://doi.org/10.3390/app14166905
Submission received: 11 July 2024 / Revised: 1 August 2024 / Accepted: 2 August 2024 / Published: 7 August 2024
(This article belongs to the Special Issue Antioxidant Compounds in Food Processing)
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Abstract

:
The present study focused on the use of pouting (Trisopterus luscus), an underutilized gadoid fish species, as a fresh product of potential commercial interest. Accordingly, non-degutted pouting specimens (145–195 g and 15–22 cm) were stored under chilling conditions (0 °C) for microbial, chemical and sensory analyses to evaluate their commercial quality and shelf life. A progressive quality loss (p < 0.05) was detected for this lean species (5.58 g lipids·kg−1 muscle) as the storage time increased, as determined through microbial (aerobes, psychrotrophs and Enterobacteriaceae counts), lipid hydrolysis (free fatty acid value), lipid oxidation (conjugated diene and triene, thiobarbituric acid reactive substance, and fluorescence values) and sensory acceptance assessment. A detailed comparison to related lean fish species revealed that the pouting exhibited a fast quality breakdown under refrigeration conditions. Thus, after 9 d of chilled storage, the psychrotroph counts exceeded the acceptable limits (8.54 log CFU·g−1), and the fish specimens were found to be rejectable, with the sensory panel, external odor and eye appearance being the limiting factors. In contrast, the pouting specimens exhibited high quality after 3 d of storage, with the quality being still acceptable after 6 d. According to the current search for novel, underutilized species, pouting is proposed as a promising source.

1. Introduction

Fish and seafood in general are sources of energy and proteins with high biological value, also contributing to the intake of essential nutrients such as proteins, trace elements and lipophilic vitamins (namely A and D) [1,2]. Seafood is also a key source of ω3 long-chain polyunsaturated fatty acids with well-established health benefits, and it is a component of dietary patterns associated with good health [3,4].
Fish species give rise to commercial food of great economic relevance in most countries [5]. Nevertheless, availability of traditional species is currently undergoing relevant decreases resulting from a wide variety of drastic changes [6,7,8]. Therefore, the fish industry is currently searching for unconventional sources in order to employ them as initial substrates [9,10,11].
One such species is pouting (Trisopterus luscus), a gadoid fish which is naturally from an extensive area comprising the Shetland Islands, Morocco and the western Mediterranean Sea, showing a preference for shallow coastal waters with depths in the range of 30–100 m [12,13,14]. For many decades, pouting has been ignored as a commercial fish, being either discarded at sea or processed into fishmeal [15], surimi [16] or fish fingers and ready-to-eat meals [17]. Published research has addressed investigation of the composition and nutritional values of pouting [18,19] as well as the presence of valuable constituents such as ascorbic and dehydroascorbic acids [20], peptones [21], essential elements [17] and citric acid [22]. However, there is a lack of previous studies regarding the processing of this species. The available reports focused on sensory and physicochemical changes during refrigerated (2 °C) storage [23], physical, chemical and sensory changes during frozen (−20 °C) storage [19] and lipid oxidation and hydrolysis development in heated (30 °C) minced muscle [24].
Among the different preservation treatments, chilling storage has been most commonly employed for fish commercialization, with the fish either fresh or further processed as food product [25,26]. However, remarkable quality changes related to the different deteriorative pathways (i.e., microbial breakdown, endogenous enzyme activity and lipid oxidation events) have been mentioned to be present as the storage period progresses [27,28,29]. Accordingly, the present study was focused on the investigation of quality preservation of pouting fish, currently an underutilized marine food source, during chilled storage with the aim to explore its marketability. An evaluation of both microbial activity and lipid damage events during chilled storage was carried out. In addition, the effects of both damage mechanisms on sensory acceptance were also evaluated, with the aim of presenting this fish species as a potential novel commercial seafood product.

2. Materials and Methods

2.1. Raw Fish, Chilled Storage and Sampling Procedure

Fresh pouting (T. luscus) (48 specimens) were caught along the Galician Atlantic coast (northwestern Spain) in June 2021. Until arrival at the laboratory (10 h), the fish specimens (lengths and weights within the 15–22 cm and 145–195 g ranges, respectively) were maintained in ice.
As a first step, 12 fish specimens were taken, divided into three different batches (four specimens in each batch) and analyzed independently (n = 3). Such specimens were considered the initial fish. The remaining fish (36 non-gutted specimens) were distributed into three batches (12 specimens in each batch) which were immediately placed in ice at a fish:ice ratio of 1:1 (w/w). The specimens were placed inside a 4 °C refrigerated room. Boxes allowing the drainage of melted ice were employed. The ice was renewed periodically so that a 1:1 ice:fish ratio was maintained throughout the storage period. The analysis of the fish samples was carried out on days 3, 6 and 9. At each time, four specimens from each batch were subjected to sensory, microbial and chemical analyses, being analyzed independently (n = 3). At each sampling time and for each batch, two specimens were employed for the sensory analysis. In the case of microbial and chemical determinations, one specimen was employed for each.
The chemical reagents and solvents used corresponded to the reagent degree and were acquired from Merck (Darmstadt, Germany); otherwise, the source is expressed.

2.2. Determination of Microbial Count Evolution

Microbial count assessment was carried out in 10 g samples. Fish samples were obtained from the muscle and were mixed with 90 mL of 0.1% peptone water. Homogenization of the mixtures was carried out in sterilized stomacher bags (AES, Combourg, France), in agreement with previous research [11,30]. Dilution of all kinds of extracts was carried out by using 0.1% peptone water.
The aerobic mesophiles were analyzed in plate count agar (PCA) (Oxoid Ltd., London, UK) after a 48 h period of incubation at 30 °C. The psychrotrophs were determined in PCA after a 7 day period of incubation at 7 °C. The analysis of Enterobacteriaceae was carried out in Violet Red Bile Agar (VRBA) after a 24 h period of incubation at 37 °C. In all cases, microbial determinations were performed in triplicate.

2.3. Determination of Trimethylamine (TMA) Value

Assessment of the TMA-nitrogen (TMA-N) value was achieved by using the picrate spectrophotometric procedure (410 nm; Beckman Coulter DU 640 spectrophotometer, Beckman Coulter Inc., Brea, CA, USA), in agreement with the method of Tozawa et al. [31]. The pouting’s white muscle was extracted with 5% trichloroacetic acid (10 g·25 mL−1). The TMA values are expressed as mg TMA-N·kg−1 fish muscle.

2.4. Lipid Damage Assessment

The lipid fraction was extracted from the pouting white muscle (approximately 5 g) in agreement with the procedure of Bligh and Dyer [32]. A chloroform/methanol (1/1, v/v) mixture was employed. The lipid fraction was quantified in agreement with the procedure of Herbes and Allen [33]. The lipid value was calculated in terms of g·kg−1 pouting muscle.
Formation of conjugated dienes (CDs) was assessed spectrophotometrically at 233 nm [34] for the lipid fraction. The results were calculated by employing the formula CD = A × V·w−1, where A, V and w indicate the absorbance reading, the volume (mL) of the aliquot employed and the weight (mg) of the aliquot employed, respectively.
Conjugated triene (CT) formation was measured at 268 nm [34] for the lipid extract. The results were calculated by applying the formula CT = A × V·w−1, where A, V and w indicate the absorbance reading, the volume (mL) of the aliquot employed and the weight (mg) of the aliquot employed, respectively.
The peroxide value (PV) was assessed spectrophotometrically (520 nm) for the lipid fraction. In this method, ferric thiocyanate was employed for peroxide reduction [35]. The results are expressed as meq. active oxygen·kg−1 lipids.
Determination of the thiobarbituric acid index (TBA-i) was carried out according to the method of Vyncke [36]. Spectrophotometrical determination at 532 nm was carried out for assessing the thiobarbituric acid reactive substance (TBARS) value. A standard curve prepared with 1,1,3,3-tetraethoxy-propane employed, with the results being expressed as mg malondialdehyde·kg−1 muscle.
The content of free fatty acids (FFAs) was determined with the lipid fraction of the pouting muscle, in agreement with the method of Lowry and Tinsley [37]. In this analytical method, a cupric acetate-pyridine complex is produced and subsequently determined by spectrophotometric (715 nm) analysis. The results are expressed as g FFAs·kg−1 lipids.

2.5. Interaction Compound Formation

Interaction compounds resulting from the reaction of oxidized lipids and protein-type compounds were assessed using fluorescence spectroscopy (Fluorimeter LS 45; Perkin Elmer España; Tres Cantos, Madrid, Spain) according to previous research [38]. The relative fluorescence (RF) was calculated by employing the equation RF = F/Fst, where F is the fluorescence measured at each excitation/emission wavelength pair and Fst is the fluorescence intensity of a quinine sulfate solution (1 µg·mL−1 in 0.05 M H2SO4) for the corresponding wavelength pair. The formation of fluorescent compounds was determined as the fluorescence ratio (FR) between the two RF values (i.e., FR = RF393/463nm/RF327/415nm), and it was determined in the aqueous phase resulting from the lipid extraction [32].

2.6. Evaluation of Sensory Acceptance

The sensory value of fish was evaluated by a taste panel consisting of five experienced testers, in agreement with the guidelines presented in Table 1 regarding fresh fish [39]. The samples were handled in a preparation room and analyzed in a well-ventilated room provided with good lighting. The following categories were ranked: highest (E), good (A), fair (B) and objectional (C) qualities. Sensory evaluation of the fish included different descriptors (skin, eyes, gills and external odor). Previous to the present study, the panelists were specifically trained with fresh pouting; two dozen fresh pouting were employed at each of the seven training sessions carried out. At each sampling time of the present study, the fish samples were presented to the panelists in a “blind” manner provided by a three-digit number and scored individually. The samples tested were shared by the panel members.

2.7. Statistical Analysis

The microbiological and chemical data were subjected to the ANOVA method in order to analyze any differences resulting from the storage period. The least-squares difference (LSD) method was used for carrying out the means comparison. PASW Statistics 6.0 software for Windows (SPSS Inc., Chicago, IL, USA) was used. In all cases, a significant confidence interval at the 95% level (p < 0.05) was taken into account.
Correlation analyses between the chilling time and quality indices and among the different microbial and chemical parameters were determined by employing the Pearson test. Linear fittings are indicated; otherwise, the kind of fitting (logarithmic or quadratic) is mentioned.

3. Results and Discussion

3.1. Determination of the Microbial Count Evolution

A progressive increase (p < 0.05) in the total aerobe counts (r = 0.94, quadratic fitting) was detected in the fish muscle as the storage time progressed (Table 2). However, even at the end of the storage period (9 d), the aerobe counts did not reach values above 6 log CFU units, and therefore, they did not pass over the 7 log CFU value considered the acceptable limit [40].
In contrast, the psychrotroph counts exhibited important increases which led to concentrations above 7 log CFU units at the end of the storage time (Table 2). However, the psychrotroph counts on day 6 did not reach 6 log CFU units, and as in the case of the aerobes, this may be regarded as a satisfactory result. As in the case of the aerobe mesophiles, the psychrotrophic bacteria steadily increased (p < 0.05) during refrigerated storage (r = 0.92, quadratic fitting).
Similar to the results observed for the other microbial parameters evaluated, a substantial (p < 0.05) increase in the Enterobacteriaceae counts was observed after 3 and 6 days of storage (Table 2). Interestingly, and although an average increase was also determined at the end of the storage time (day 9), this increase was not found significant. Notably, the Enterobacteriaceae counts showed a good relationship with the storage time (r = 0.94). Interestingly, the presence of Enterobacteriaceae in the pouting muscle did not reach unsatisfactory levels (4 log CFU units) [40] even after 9 days of refrigerated storage.
To the best of our knowledge, no previous studies have evaluated the metrics of the microbial breakdown of pouting muscle during chilled storage. Thus, the present study set a mathematical correlation for the microbial growth of three relevant microbial parameters as the refrigeration time progressed and revealed that the two main indicators of spoilage (aerobes) and hygiene (Enterobacteriaceae) did not reach unsatisfactory concentrations in the pouting muscle even after 6 days of refrigerated storage. Thus, it has been reported that, while alive, the immune system of marine species in general prevents bacterial growth [41]. However, the immune system collapses post-mortem, and consequently, bacteria are able to invade the fish flesh during chilled storage [42].
In general, lower microbial growth than that in the present case has been described for related lean fish species. Thus, the aerobe counts attained values of 6.7, 6.1 and 6.6 log CFU units in chilled turbot (Psetta maxima) [30], hake (Merluccius merluccius) [43] and ray (Raja clavata) [44] after 19, 12 and 10 d of chilled storage in ice, respectively. Regarding psychrotroph development, values of 6.2 and 6.3 log CFU units were determined in chilled sea bream (Sparus aurata) and farmed sea bass (Dicentrarchus labrax), respectively, after 12 d of storage in ice [45]. Notably, psychrotroph concentrations of about 5 log CFU units were determined in both species after an 8 day storage period. Regarding underutilized low-fat species such as chilled Bombay duck (Harpodon nehereus) [46] and lobster krill (Munida sp.) [11], aerobic counts of 6.4 and 6.8 log CFU units after a 10 day storage period were determined, respectively.

3.2. Assessment of the TMA-N Value

The TMA-N content has been reported to be a valid index for quality loss assessment during the refrigerated storage of fish species on the basis of the strong relationship between its value and the freshness loss [26,47]. Volatile amine compounds such as TMA have been shown to originate partially as a result of endogenous enzyme activity but mostly as a result of microbial growth [48,49].
In the present study, a marked increase (p < 0.05) in the TMA-N value in the fish muscle was detected as the chilling time increased (r = 0.94, quadratic fitting) (Figure 1). In agreement with the above-mentioned data on microbial count evolution, this increase can be explained on the basis of the microbial activity development during refrigerated storage. Thus, good correlation values were detected for the TMA-N value with the above-mentioned microbial counts (mesophiles, r = 0.93; psychrotrophs, r = 0.95; Enterobacteriaceae, r = 0.90).
Previous research has already shown remarkable TMA formation during the refrigerated storage of pouting. Thus, Gallardo and Montemayor [50] observed exponential TMA-N formation during storage at 2 °C. In this study, the 1.0 mg TMA-N·100 g−1 value at day 9 rose after 15 days up to a 31.4 mg TMA-N·100 g−1 value. Similarly, marked TMA-N formation was reported by González-Tesouro et al. [23] during 2 °C refrigerated storage. Thus, values in the range of 11.0–15.7 mg·100 g−1 were detected in the pouting muscle after 7–8 d of storage.
TMA-N formation has also been detected in related lean fish species during chilled storage. Thus, no relevant TMA-N formation was detected in hake (M. merluccius) muscle during chilling storage for up to 12 d. Then, a sharp increase up to 11.5 g·100 g−1 muscle was observed on day 19 [43]. Likewise, iced wild turbot (Scophthalmus maximus) attained a 38.9 mg TMA-N·100 g−1 muscle value after 19 days of storage [51], while a 19.6 value was detected after 8 days of storage. In the case of farmed turbot (Psetta maxima), Rodríguez et al. [30] reported low TMA-N formation (4.5 mg·kg−1 muscle) after 19 d of chilled storage. Low TMA-N formation (0.9 and 2.2 mg TMA-N·100 g−1 muscle) were also described by Cakli et al. [45] in chilled sea bream (S. aurata) and sea bass (D. labrax), respectively, after 12 d of storage. Relatively low TMA-N values were also detected in the dorsal and ventral zones of Atlantic pomfret (Brama brama) [52] after 15 d of storage, and thus TMA-N values of 1.0 and 2.1 mg·100 g−1 muscle were assessed, respectively.

3.3. Determination of the Lipid Content and Lipid Hydrolysis Events

The pouting muscle showed a low lipid content (5.58 ± 0.39 g·kg−1 muscle), which corresponds to a lean fish species [53]. This lipid content agrees with a previous seasonal study which indicated a 0.54–1.08 g·100 g−1 muscle range for the entire ground muscle (white and dark muscles altogether) of the current fish species [18]. Recently, a low lipid content (i.e., 1.0 ± 0.1 g·100 g−1 muscle) was also reported for pouting by Blanco et al. [19].
Lipid hydrolysis events in pouting muscle were investigated by assessing the FFA content (Figure 2). The initial FFA value was 13.4 ± 1.0 g·kg−1 lipids. Afterward, remarkable increases in the FFA content (p < 0.05) with the chilling time were observed (r = 0.94, quadratic fitting). Notably, the FFA fraction represented approximately 17% of the total lipid fraction at the end of the study, with this value being over 10 times higher than the initial value.
It has been signaled that FFA formation during chilled storage would occur as a result of endogenous enzyme and microbial activities [25,27]. Before attaining the end of the microbial lag phase, FFAs are reported to be mainly produced by effect of endogenous enzyme activity (namely lipases and phospholipases) [48,49]. Then, the impact of microbial activity should increase as a result of processes related to bacterial catabolism [26,27]. In agreement with this important role of microbial activity in FFA formation, good correlation values between the FFA values and both the aerobic mesophile and psychrotroph counts (r = 0.94 in both cases) were detected in the present study.
Although the release of FFAs themselves does not imply any remarkable loss of nutritional quality, FFA accumulation has been linked to an enhancement of lipid oxidation [54,55] and textural deterioration due to interactions with proteins [47,56]. Additionally, FFAs have been reported to undergo a faster oxidation rate than higher molecular weight lipid classes such as triacylglycerols and phospholipids. This differential behavior has been explained on the basis of offering a lower steric hindrance to the initial development of the oxidation mechanism [24,57].
To the best of our knowledge, no previous studies have addressed the FFA evolution of pouting muscle during refrigerated storage. Regarding other lean fish species, FFA formation has been shown to occur to a lesser extent in general compared with the present species. Thus, low FFA values were detected in the dorsal and ventral zones of Atlantic pomfret (Brama brama) [52]. After 15 days of storage, FFA contents of 3.2 and 4.6 g·100 g−1 lipids were observed, respectively. Hake (M. merluccius) muscle attained a 2.5 g·100 g−1 lipids range after a 19 day storage period [58]. Low FFA formation (approximately 13 g·kg−1 lipids) was also detected in farmed turbot (Psetta maxima) muscle after a 19 day period [59]. However, wild turbot (Scophthalmus maximus) led to notably higher FFA formation (20.6 g·100 g−1 lipids) after a 19 day storage period [51]. Regarding underutilized low-fat species, chilled lobster krill (Munida sp.) exhibited an FFA value of 28.1 g·kg−1 lipids (10 days of storage) [11].

3.4. Assessment of Lipid Oxidation Development

The development of lipid oxidation in pouting muscle was determined at different stages of this damage mechanism. Thus, the formation of CD and CT compounds indicated progressive formation (p < 0.05) of these kinds of molecules during chilling storage (Table 3). The CD content depicted a fair correlation value with the chilling time (r = 0.88, quadratic fitting), while better correlation was detected for the CT value (r = 0.93, quadratic fitting). Compared with the lipid hydrolysis evolution (i.e., the FFA value), a fair correlation value for the CD content (r = 0.90) and a better one for the CT level (r = 0.94) were observed.
Regarding peroxide formation (Table 3), the levels found for this kind of oxidation compound were roughly in the 1.2–2.2 meq. active oxygen·kg−1 lipid range throughout the whole study. This range can be considered especially low if we compare it to the values found for other fish species stored under similar processing conditions [26,60,61]. Due to the effect of the storage time, a small increase (p < 0.05) was achieved on day 3, but no differences (p > 0.05) were subsequently detected for the 3–9 day storage times in this study.
The determination of the secondary lipid oxidation compounds (i.e., TBARSs) indicated progressive formation (p < 0.05) as the chilling time increased (r = 0.94) (Table 3). Thus, an increase (p < 0.05) was detected after 3 and 6 d of storage, but no effect (p > 0.05) was detected at the end of the study. Fair correlation values (r = 0.87) for the TBA index with the CD and CT values were determined.
The investigation of the FR indicated relevant formation (p < 0.05) of interaction compounds after 6 and 9 d of chilling storage (Figure 3). Thus, good correlation with the chilling time was achieved (r = 0.91, quadratic fitting). Good correlation values were also detected with other lipid quality indices, such as the FFA (r = 0.94) and CT (r = 0.91) values.
The lipid oxidation mechanism has been described as a complex process in which different types of molecules are produced, with most of them being unstable [61,62]. Such molecules are likely to degrade, leading to low molecular weight compound formation or reaction with other compounds included in the fish muscle. Thus, the determination of each kind of compound cannot always afford a valuable method for assessment of the quality degradation in fish. A relevant increase in the CD, CT and TBARS values was observed in the present study. The high reactivity or the electrophilic character of lipid oxidation compounds in general led them to break down or react with food constituents possessing nucleophilic groups (i.e., –NH2 and –SH functions) [63,64,65,66]. As a result, a remarkable increase in the presence of fluorescent compounds (tertiary lipid oxidation compounds) was observed [67,68]. It is concluded that lipid-related indices (CD, CT, TBA and FR values) are valuable tools for assessing the lipid damage development of the current species under chilling conditions. Contrary to this, the PV did not afford an accurate measurement of the oxidation degree as being an indication of the initiation of lipid oxidation [26,61].
To the best of our knowledge, no previous information is available regarding the lipid oxidation development of pouting during refrigerated storage. However, lipid oxidation development in pouting muscle has been described when subjected to other technological treatments. Thus, an important fluorescent compound formation was detected in a heated muscle system (25 d at 30 °C) [24]. However, no increase in the TBA value was detected by Blanco et al. [19] in frozen pouting muscle after 6 months of storage at −20 °C.
Previous reports accounted for the assessment of lipid oxidation development in lean fish species during chilled storage. According to these reports, low peroxide formation was detected in chilled hake (M. merluccius) (3.7 meq.·kg−1 lipids after 8 d) [58] and turbot (P. maxima) (2.9 meq.·kg−1 lipids after 9 d) [59]. However, relevant peroxide formation was observed in Atlantic pomfret (B. brama) (12.1–15.3 meq. active oxygen·kg−1 lipids) after a 9 day storage period [52]. A marked increase in peroxide formation was detected in an underutilized species, Bombay duck (H. nehereus), (ca. 25 meq. active oxygen·kg−1 lipids), after 13 d of storage [46].
In agreement with the present study, TBARS formation has been detected in chilled lean fish. Thus, relatively low TBARS formation was detected in Atlantic pomfret (B. brama) (0.2–0.3 mg malondialdehyde·kg−1 muscle range value after a 15 day storage period) [52] and wild turbot (S. maximus) (0.5 mg malondialdehyde·kg−1 muscle value after a 19 day storage period) [51]. On the contrary, greater formation was observed in sea bream (S. aurata) and farmed sea bass (D. labrax) after an 18 day storage period in ice (1.4 and 1.0 mg malondialdehyde·kg−1 muscle values, respectively) [45]. Regarding underutilized lean species, lobster krill (Munida sp.) exhibited a 0.13 mg malondialdehyde·kg−1 muscle value after a 10 day storage period [11].
Finally, progressive formation of fluorescent compounds was detected in related lean species during the storage time. These results refer to Atlantic pomfret (B. brama) [52], European hake (M. merluccius) [58] and lobster krill (Munida sp.) [11].

3.5. Evaluation of Sensory Acceptance

Sensory evaluation was carried out on whole pieces of pouting fish (Table 4). According to the above-mentioned microbial and chemical determinations, the high quality of the initial fish (E score in all analyzed descriptors) was observed, and this decreased progressively as the chilling time increased. However, the fish specimens were still acceptable on day 6. On the contrary, the fish were found to be of objectional quality on day 9. According to the evaluation carried out by the panelists, eye appearance (concave and milky aspect) and external odor (i.e., putrid odor development) were found to be the limiting descriptors.
Previous research accounted for the decrease in sensory acceptance of pouting fish specimens during storage under refrigeration conditions. Thus, González-Tesouro et al. [23] showed that refrigerated (2 °C) pouting was unacceptable after 6–7 days of storage. Notably, the first sign of deterioration was the development of a slightly off odor after 3–4 days of storage. An average decrease in the general aspect, texture and taste scores was observed after a 6 month storage period at −20 °C [19].
A progressive sensory quality decrease has also been detected in related lean fish species during chilled storage. In general, a longer shelf life has been found for relatively larger species, while relatively small-sized species have shown shorter shelf lives. Thus, chilled wild turbot (S. maximus) was found to be acceptable at day 15 [51], while farmed turbot (P. maxima) was still acceptable after a 19 day storage period [30]. European hake (M. merluccius) [58] and ray (R. clavata) [44] showed relatively short shelf lives (5 and 3 days, respectively) during chilled storage. Regarding underutilized lean species, Bombay duck (H. nehereus) [46] and lobster krill (Munida sp.) [11] showed shelf lives of 10 and 6 d, respectively, during refrigerated storage.

4. Conclusions

This study addressed the use of pouting (T. luscus), a currently discarded and underutilized gadoid fish species, as a potential commercial fresh product. A progressive quality loss (p < 0.05) as the storage time increased was detected, according to the results of microbial activity (aerobes, psychrotrophs and Enterobacteriaceae counts), lipid hydrolysis (FFA), oxidation (CD, CT and FR values) and sensory evaluation. On the contrary, peroxide formation did not show itself to be relevant throughout the storage time. A comparison with related lean fish species indicated fast development of damage mechanisms in pouting. The two main microbial indicators of spoilage (aerobes) and hygiene (Enterobacteriaceae) were not unsatisfactory after a 6 day storage period. However, on day 9, the psychrotroph counts and sensory evaluation were not considered acceptable. In the latter case, external odor and eye appearance were determined to be the limiting factors.
In agreement with current global interests, in the search for underutilized food sources of promising commercial relevance, this research opens the way to a novel and beneficial consideration of pouting as a valuable fresh product. Studying the employment of preserving technologies (i.e., the addition of natural antimicrobials and antioxidants or previous physical treatments) is recommended in order to enlarge the shelf life time and quality of this labile species as a commercial fresh product.

Author Contributions

Conceptualization, J.M., S.P.A. and J.B.-V.; methodology, M.T. and J.M.M.; data curation, M.T. and J.M.M.; writing—original draft preparation, S.P.A.; writing—review and editing, J.M., S.P.A. and J.B.-V. All authors have read and agreed to the published version of the manuscript.

Funding

This research was carried out under a research contract funded by the Fundación Pública Gallega Centro Tecnológico del Mar. Fundación CETMAR.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data used to support the findings of this study can be made available by the corresponding author upon request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Applsci 14 06905 g001
Figure 1. Evolution of trimethylamine (TMA; mg TMA-N·kg−1 muscle) value in pouting muscle subjected to chilling storage. Average values of three independent determinations (n = 3), with standard deviations denoted by bars. Different letters (a, b and c) denote differences (p < 0.05) with chilling time.
Figure 1. Evolution of trimethylamine (TMA; mg TMA-N·kg−1 muscle) value in pouting muscle subjected to chilling storage. Average values of three independent determinations (n = 3), with standard deviations denoted by bars. Different letters (a, b and c) denote differences (p < 0.05) with chilling time.
Applsci 14 06905 g001
Applsci 14 06905 g002
Figure 2. Formation of free fatty acids (FFAs; g·kg−1 lipids) in pouting muscle subjected to chilling storage. Average values of three independent determinations (n = 3), where standard deviations are denoted by bars. Different letters (a, b, c and d) denote differences (p < 0.05) in chilling time.
Figure 2. Formation of free fatty acids (FFAs; g·kg−1 lipids) in pouting muscle subjected to chilling storage. Average values of three independent determinations (n = 3), where standard deviations are denoted by bars. Different letters (a, b, c and d) denote differences (p < 0.05) in chilling time.
Applsci 14 06905 g002
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Figure 3. Fluorescent compound formation (fluorescence ratio (FR)) in pouting muscle subjected to chilling storage. Average values of three independent determinations (n = 3), with standard deviations indicated by bars. Different letters (a, b and c) denote differences (p < 0.05) in chilling time.
Figure 3. Fluorescent compound formation (fluorescence ratio (FR)) in pouting muscle subjected to chilling storage. Average values of three independent determinations (n = 3), with standard deviations indicated by bars. Different letters (a, b and c) denote differences (p < 0.05) in chilling time.
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Table 1. Scale used for freshness degree evaluation of pouting fish.
Table 1. Scale used for freshness degree evaluation of pouting fish.
DescriptorHighest Quality
(E)		Good Quality
(A)		Fair Quality
(B)		Objectional Quality
(C)
SkinHighly intense pigmentation;
transparent mucus		Milky mucus; insignificant pigmentation lossesSlightly grayish mucus; pigmentation without shineWidely opaque mucus; important pigmentation losses
EyesConvex; transparent cornea;
bright and black pupil		Convex and slightly sunken; slightly opalescent cornea; black and cloudy pupilFlat; opalescent cornea;
opaque pupil		Concave and milky cornea; internal organs blurred
GillsBright red; without odor; lamina perfectly separatedRose-colored; without odor; lamina adhered in groupsSlightly pale; incipient fishy odor; lamina adhered in groupsGray-yellowish color; intense ammonia odor; lamina totally adhered
External odorSharp seaweed and shellfish smellWeak seaweed and shellfish smellIncipiently putrid and rancidPutrid and rancid
Table 2. Determination of microbial activity (log CFU·g−1 muscle) * in pouting muscle subjected to chilling storage **.
Table 2. Determination of microbial activity (log CFU·g−1 muscle) * in pouting muscle subjected to chilling storage **.
Microbial ParametersChilling Time (Days)
0369
Total aerobes3.90 ± 0.35 a3.94 ± 0.42 a4.36 ± 0.32 a5.52 ± 0.07 b
Psychrotrophs4.38 ± 0.03 a5.55 ± 0.65 b5.89 ± 0.13 b8.54 ± 0.36 c
Enterobacteriaceae1.23 ± 0.40 a2.09 ± 0.16 b2.49 ± 0.20 c3.10 ± 0.95 c
* Average values ± standard deviations of three independent determinations (n = 3). ** In each row, different letters (a, b and c) indicate differences (p < 0.05) with chilling time.
Table 3. Assessment of lipid oxidation events * in pouting muscle subjected to chilling storage **.
Table 3. Assessment of lipid oxidation events * in pouting muscle subjected to chilling storage **.
Lipid Oxidation IndexChilling Time (Days)
0369
Conjugated dienes (absorbance·mL sample·mg−1 sample)0.46 ± 0.04 a0.56 ± 0.02 b0.55 ± 0.02 b0.70 ± 0.07 c
Conjugated trienes
(absorbance·mL sample·mg−1 sample)		0.053 ± 0.010 a0.068 ± 0.007 ab0.076 ± 0.006 b0.116 ± 0.048 c
Peroxide value
(meq. active oxygen·kg−1 lipids)		1.29 ± 0.17 a2.18 ± 0.24 b2.00 ± 0.19 b2.17 ± 0.11 b
Thiobarbituric acid index (mg malondialdehyde·kg−1 muscle)0.09 ± 0.02 a0.43 ± 0.10 b0.68 ± 0.04 c0.88 ± 0.29 c
* Average values ± standard deviations of three independent determinations (n = 3). ** In each row, different letters (a, b and c) denote differences (p < 0.05) in chilling time.
Table 4. Sensory acceptance of pouting muscle subjected to chilling storage *.
Table 4. Sensory acceptance of pouting muscle subjected to chilling storage *.
Sensory DescriptorChilling Time (Days)
0369
SkinEAAB
EyesEABC
GillsEABB
External odorEBBC
* Freshness categories are E (excellent), A (good), B (fair) and C (objectional), as expressed in Table 1.
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Maroto, J.; Trigo, M.; Miranda, J.M.; Aubourg, S.P.; Barros-Velázquez, J. Evaluation of Lipid Damage, Microbial Spoilage and Sensory Acceptance of Chilled Pouting (Trisopterus luscus), an Underutilized Lean Fish Species. Appl. Sci. 2024, 14, 6905. https://doi.org/10.3390/app14166905

AMA Style

Maroto J, Trigo M, Miranda JM, Aubourg SP, Barros-Velázquez J. Evaluation of Lipid Damage, Microbial Spoilage and Sensory Acceptance of Chilled Pouting (Trisopterus luscus), an Underutilized Lean Fish Species. Applied Sciences. 2024; 14(16):6905. https://doi.org/10.3390/app14166905

Chicago/Turabian Style

Maroto, Julio, Marcos Trigo, José M. Miranda, Santiago P. Aubourg, and Jorge Barros-Velázquez. 2024. "Evaluation of Lipid Damage, Microbial Spoilage and Sensory Acceptance of Chilled Pouting (Trisopterus luscus), an Underutilized Lean Fish Species" Applied Sciences 14, no. 16: 6905. https://doi.org/10.3390/app14166905

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