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Journal of Food Protection, Vol. 71, No. 12, 2008, Pages 2572–2577 Copyright ᮊ, International Association for Food Protection

Research Note Assessment of Safety, Nutritional, and Spoilage Characteristics of Different Lagoon Grey Mullets (Liza ramada, Liza aurata, and Liza saliens)

SYLVAIN SADO KAMDEM,1 PAMELA VERNOCCHI,1* MIRKO MAFFEI,2 NICOLETTA BELLETTI,1 FAUSTO GARDINI,1 M. ELISABETTA GUERZONI,1 AND ROSALBA LANCIOTTI1 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/71/12/2572/2364831/0362-028x-71_12_2572.pdf by guest on 25 September 2021

1Dipartimento di Scienze degli Alimenti, Universita` degli Studi di Bologna, Piazza Goidanich 60, 47023 Cesena, Italy; and 2Cooperativa M.A.R.E., Via Enrico Toti 2, 47841 Cattolica – Rimini, Italy

MS 08-127: Received 10 March 2008/Accepted 6 July 2008

ABSTRACT

Different lagoon grey mullets such as Liza ramada (thinlip ), Liza aurata (golden grey mullet), and Liza saliens (leaping grey mullet) were analyzed for their nutritional, microbiological, and safety parameters. The microbiological values never exceeded the lower limits stipulated by the Italian Higher Institute of Health. The pathogenic species frequently associated with seafood (Salmonella, Listeria monocytogenes, Vibrio cholerae, Vibrio parahaemolyticus, and Aeromonas hydrophila) were never detected. The absence of coliforms and of Escherichia coli was noted in all fish species after 4 days of storage in ice. Heavy metals such as cadmium and mercury were always below the detection limits (0.01 mg/kg). All three fish species had low levels of total biogenic amines (80 to 100 mg/kg), and the presence of histamine was sporadic. All Liza species, particularly L. ramada and L. saliens, are a good source of ⍀3 long-chain polyunsaturated fatty acids.

Consumption of fish has increased during recent years mented for some fish species. A change in temperature from as consumers have become more aware of the nutritional 26 to 14ЊC caused an increase in the total fatty acids in value of fish and the safety issues associated with other cephalus (grey mullet) after 4 weeks of acclimati- foods, such as chicken and beef. Fresh fish from the Med- zation, whereas low salinity caused an increase in the per- iterranean Sea, lagoons, and aquaculture facilities constitute centage of some polyunsaturated fatty acids such as 22:5 a high percentage of the fish consumed (5). Among the (⍀3), 22:6 (⍀3), and 20:4 (⍀6) (13, 20, 25). lipid most popular fish, some such as Salmo salar (salmon), Di- nutritional quality depends of the ratio of ⍀6 polyunsatu- centrarchus labrax (sea bass), and Sparus aurata (sea rated fatty acid (PUFA) to ⍀3 PUFA and the ration of bream) have been studied extensively regarding their PUFAs to saturated fatty acids (SFAs), which are highly growth, nutritional, compositional, and storage character- correlated with coronary heart diseases (28). istics (7, 15). Few studies have been conducted on other The benefits from fish consumption are sometimes species such as Liza ramada (thinlip mullet), Liza aurata veiled by the risk of chemical intoxication by heavy metals (golden grey mullet), and Liza saliens (leaping grey mullet). such as cadmium, mercury, and lead (13). Consequently the These three species in the family Mugilidae are found in concentration of heavy metals in the water, sediment, and both tropical and temperate seas close to shore and in es- finally the fish muscle tissue is of great importance for the tuaries, lagoons, and sometimes even rivers. Mullets can be safety of seafood. characterized by differences in compositional and micro- Bacterial contaminants can affect both the product biological features related to the habitat of origin due to safety and shelf life of fishery products (22). Some patho- their wide range of feeding and water temperature and sa- genic bacteria such as vibrios, Aeromonas hydrophila, and linity adaptations (6). Listeria monocytogenes are naturally present in the aquatic Assessment of the chemical, safety, and compositional environment, and Staphylococcus aureus, Salmonella, Shi- characteristics of fish and the water in which they live is gella, and Escherichia coli O157:H7 are generally associ- becoming a key tool in food chain safety and commercial- ated with fish processing. Bacterial groups such as Pseu- ization. The increased demand for seafood may lead to in- domonas spp., sulfur-producing bacteria, and Enterobacte- creased problems associated with both the environment and riaceae affect product spoilage (14). The lipolytic activity public health. The influence of the environment on growth of Pseudomonas species is one cause of the rancid odor of rate, composition, and safety characteristics is well docu- stored fish and especially frozen fish under abusive thermal conditions (14). Sulfur-producing bacteria are mostly re- * Author for correspondence. Tel: ϩ390547636145; Fax: sponsible for the production of volatile compounds related ϩ390547338103; E-mail: [email protected]. to the putrefaction of seafood (14), whereas Enterobacte- J. Food Prot., Vol. 71, No. 12 SAFETY AND QUALITY ASSESSMENT OF LAGOON GREY MULLETS 2573

riaceae, Pseudomonas spp., and Shewanella putrefaciens Chemical-physical analysis. Moisture, protein, lipid, and also accumulate biogenic amines. Several authors have pro- ash content were analyzed according to an AOAC method (3), posed biogenic amine concentration as an index of fish and TVNB was analyzed according to another AOAC method (4). freshness (23, 29). Histamine, cadaverine, and putrescine Extraction of lipids and esterification of free fatty acids were performed as described by Kinsella et al. (21). The gas chromato- together may be considered as major quality indicators for graphic profiles of free fatty acids and their identification and fish products. Assessment of the total volatile nitrogen base quantification were determined according to the procedures re- (TVNB) was recommended by the European Community ported by Vernocchi et al. (30). The relative quantities of free fatty for monitoring the freshness of fish stored in ice or frozen acids were expressed as weight percentage of the total fatty acids (1). The nonprotein nitrogenous fraction can be used by in each sample. The index of atherogenicity (IA; serum lipid ac- some microorganisms, and the production of nitrogenous cumulation) and index of thrombogenicity (IT; clotting activity of volatile compounds such as ammonia and trimethylamine platelets and their aggregation into thrombus) indices were cal- is easily detected (14). Several factors affect the TVNB culated according to the method of Ulbricht and Southgate (28) concentrations, e.g., the fish species, the type of stress ex- using the following formulas Downloaded from http://meridian.allenpress.com/jfp/article-pdf/71/12/2572/2364831/0362-028x-71_12_2572.pdf by guest on 25 September 2021 perienced by the fish during capture, and the type of muscle aSЈϩbSЉϩcSٞ IA ϭ (17, 18). dP ϩ eM ϩ fMЈ The main aim of this work was to study the spoilage Ј Љ ٞ ␻ where S is C12:0, S is C14:0, S is C16:0, P is the sum of 6 pattern and determine some safety indices (presence of ␻ Ј PUFA and 3 PUFA, M is oleic acid (C18:1), M is the sum of pathogenic microbial species and heavy metal and biogenic other monounsaturated fatty acids, and a through f are empirical amine concentrations) and nutritional indices (percentage constants based on the atherogenicity of the different groups: b composition and fatty acid profile) for L. ramada, L. au- has been set to 4 and a, c, d, e, and f have been provisionally set rata, and L. saliens during storage. to 1. mS iv MATERIALS AND METHODS IT ϭ nM ϩ oMЈϩp(␻6) ϩ q(␻3) ϩ (␻3/␻6) Microbiological analysis. L. ramada, L. aurata, and L. sal- iv ␻ ␻ iens individuals were caught in the Comacchio Lagoon, a wide where S is the sum of C14:0, C16:0, and C18:0, 6is 6 PUFA, ␻ ␻ estuarine area located near the mouth of the Po River in the Adri- 3is 3 PUFA, and m, n, o, p, and q are unknown constants atic Sea in northeastern Italy. The fishes caught were 23 to 25 cm with up to the following known assigned values: m has been set long and weighed 100 to 120 g. The fishes (about 20 kg) were to 1; n, o, and p have the value 0.5 because monounsaturated fatty ␻ ␻ immediately refrigerated under ice and transported to the labora- acids and 6 PUFA are less antiatherogenic than is 3 PUFA; tory for analyses. and q has the value 3. Three subsamples of each species (about 1 kg of fish, cor- The detection and quantification of metals was performed (4). responding to nine fishes) were used for the microbiological anal- according to the AOAC method The elemental concentrations in the solution were measured with a Spectra A20 flame atomic yses, which were carried out after 1, 2, 3, and 4 days of storage. absorption spectrophotometer (Varian Inc., Palo Alto, Calif.). The fishes were scrubbed free of dirt, sliced, and homogenized in stomacher (BagMixer, Interscience, St. Nom, France). Determination of biogenic amines. Ten grams of the ho- Total coliforms (TC) were enumerated after plating on violet mogenized sample was extracted three times with 15 ml of 5% red bile agar (Oxoid, Basingstoke, UK) plates that were incubated trichloroacetic acid (Carlo Erba Reagenti, Milan, Italy), and the at 37ЊC for 36 h, and E. coli populations were determined on the three supernatant fractions were combined and made up to 50 ml same medium with 4-methyl-umbelliferyl-glucuronide (MUG) with 5% trichloroacetic acid. Amine derivatization was performed added on plates that were incubated at 37ЊC for 24 h. The E. coli according to the method of Eerola et al. (9). The analyses were colonies on this medium were fluorescent. For evaluation of Sal- performed using an Intelligent PU-2089 high-pressure liquid chro- monella in 25 g of fish homogenate, the method of the Interna- matography quaternary pump and an Intelligent UV-VIS multi- tional Organization for Standardization (19) was followed. Qual- wavelength detector UV 2070 Plus (Jasco Corporation, Tokyo, itative analyses for Vibrio spp. and A. hydrophila were conducted Japan) and a manual injector equipped with a 20-␮l loop (Rheo- with 25 g of fish homogenate using the method of Colakoglu et dyne, Rohnert Park, Calif.) according to the conditions described al. (8). Listeria spp. were isolated according to the method of by Gardini et al (12). Vernocchi et al. (30), and the isolates were assigned to species Fish samples were analyzed in triplicate, and data are ex- using to the API Listeria method (bioMe´rieux, Marcy l’Etoile, pressed as means. The amount of each amine is expressed as mil- France). Pseudomonas spp. were counted on plates of Pseudo- ligrams of amine per kilogram of sample based on reference to a monas agar base with CFC (cetrimide, fucidin, and cephaloridine) calibration curve. supplement (Oxoid) that were incubated for 48 h at 30ЊC. Entero- Statistical analysis. The data reported are the means of three cocci were grown on Slanetz and Bartley medium (Oxoid) plates repetitions. The standard deviations (SD) are reported in the ta- that were incubated for 24 h at 44ЊC. The determination of sulfur- bles. The statistical treatment was performed using Microsoft Of- producing bacteria was carried out using iron sulfite agar (Oxoid) fice Excel 2003 (Microsoft, Redmond, Wash.). for72hat25ЊC. On this medium, the colonies S. putrefaciens were black and those of Photobacterium phosphoreum were RESULTS white. These plates were incubating at 25ЊC for 3 days for S. putrefaciens and at 10ЊC for 14 days for P. phosphoreum. Total Microbial analysis. The counts of total aerobic bac- aerobic bacteria were counted on plate count agar (Oxoid) plates teria, TC, E. coli, enterococci, Pseudomonas spp., and sul- that were incubated for 72 h at 25ЊC. All samples for all analysis fur-producing bacteria during fish storage are listed in Table were diluted with phosphate-buffered peptone water. 1. The microbial population in L. saliens samples was dom- 2574 SADO KAMDEM ET AL. J. Food Prot., Vol. 71, No. 12

TABLE 1. Total aerobic bacteria, TC, E. coli, enterococci, Pseudomonas spp., and sulfur-producing bacteria (Shewanella, Photobac- terium) during storage in ice of Liza aurata, L. ramada, and L. saliens Bacterial populations (log CFU/g)a Storage time Total aerobic Total Sulfur-producing Species (days) bacteria coliforms E. coli Enterococci Pseudomonas spp. bacteria

Liza aurata 1 3.78 Ϯ 0.45 ND ND ND 2.48 Ϯ 0.38 ND 2 2.90 Ϯ 0.32 ND ND ND 3.56 Ϯ 0.37 ND 3 4.15 Ϯ 0.49 ND ND 2.12 Ϯ 0.29 2.48 Ϯ 0.28 ND 4 2.71 Ϯ 0.30 ND ND ND 3.62 Ϯ 0.46 ND L. ramada 1 2.78 Ϯ 0.38 ND ND ND 3.20 Ϯ 0.37 ND 2 3.41 Ϯ 0.43 ND ND ND 2.48 Ϯ 0.35 ND 3 2.78 Ϯ 0.38 ND ND 2.48 Ϯ 0.35 2.84 Ϯ 0.36 ND Downloaded from http://meridian.allenpress.com/jfp/article-pdf/71/12/2572/2364831/0362-028x-71_12_2572.pdf by guest on 25 September 2021 4 2.75 Ϯ 0.30 ND ND ND 3.62 Ϯ 0.47 ND L. saliens 1 3.58 Ϯ 0.44 ND ND ND ND 3.99 Ϯ 0.46 2 3.65 Ϯ 0.37 1.09 Ϯ 0.09 ND ND ND 4.81 Ϯ 0.54 3 4.11 Ϯ 0.48 ND ND ND ND 4.21 Ϯ 0.49 a Values are the mean Ϯ standard deviation for three replicate experiments. ND, not detected (below the detection limit). inated by sulfur-producing bacteria. At the end of the stor- tected never exceeded 12.6 mg/100 g. No marked differ- age period, the samples of this fish species had low total ences in relation to fish species and storage time were ob- aerobic bacteria counts and no detectable TC or E. coli served during the period of analysis. (below the limit of detection of 1 log CFU/g). The micro- Concentrations of biogenic amines after 4 days of stor- bial counts of L. ramada and L. aurata indicated that the age at 4ЊC for the three fish species are reported in Table dominant spoilage organism was Pseudomonas spp., but the 3. Under these experimental conditions, six biogenic counts for sulfur-producing bacteria on iron agar were be- amines were detected: 2-phenylethylamine, putrescine, ca- low the limits of detection, which in our experiment was 2 daverine, histamine, tyramine, and spermidine. The two ar- log CFU/g. No relevant differences in the counts of total omatic amines (tyramine and 2-phenylethylamine) were the aerobic bacteria for the three fish species were recorded. In most abundant; concentrations of tyramine were 23 to 41 all the samples, enterococci were found only randomly and mg/kg. However, the three species had low levels of total never exceeded 2.5 log CFU/g. biogenic amines (81 to 103 mg/kg) and low levels of his- Regarding the safety of the products, Salmonella, L. tamine. monocytogenes, Vibrio cholerae, Vibrio parahaemolyticus, and A. hydrophila were not detected in any of the samples Fish composition and fatty acids. The percentage analyzed. composition in these three fish species after 1 day of storage in ice is reported in Table 4. No relevant differences among Heavy metals, TVNB, and biogenic amines. The the species were found when compared with the mean per- concentrations of heavy metals such as cadmium, mercury, centage composition of M. cephalus, which was published and lead detected after 1 day of storage in ice were always by the Italian National Institute of Nutrition (26). The flat- below the limits imposed by the European Commission (2). head mullets studied in this work were characterized by Cadmium and mercury were always below the detection 3.64 to 3.73% fat and 18.45 to 20.09% protein, lower than limits (0.01 mg/kg), and lead was detected in all three spe- those percentages (6.8 and 15.8 %, respectively) previously cies at a mean concentration of 0.2 mg/kg. reported for flathead mullets. The concentrations of TVNB in these fish species dur- The percentage fatty acid composition of the three fish ing storage are reported in Table 2. The TVNB values de- species is shown in Table 5. The fatty acid profiles were quite similar for SFAs, which accounted for 24.23, 22.49, TABLE 2. Total volatile nitrogen base (TVNB) measured during and 22.24% of the total lipids of L. aurata, L. ramada, and the storage of Liza aurata, L. ramada, and L. saliens in ice L. saliens, respectively. The main SFA recorded, indepen- dent of the fish species, was C , followed by C , Storage TVNB (mg/100 g of sample)a 16:0 14:0 time C15:0, and C18:0. However, the fatty acid profiles of the fish (days) L. aurata L. ramada L. saliens species studied were dominated by monounsaturated fatty acids, particularly by C16:1n7 and C18:1n9. L. aurata was 1 12.54 Ϯ 0.81 12.55 Ϯ 1.07 12.52 Ϯ 1.21 characterized by markedly higher concentrations of C Ϯ Ϯ 14:1 2 12.54 0.75 ND 12.54 1.11 and C and lower concentrations of PUFA ⍀3 and par- Ϯ 15:1 3 11.17 0.96 ND ND ticularly C ⍀3 compared with the other species. Conse- 4 11.16 Ϯ 1.05 12.53 Ϯ 1.09 12.56 Ϯ 1.11 20:5 quently, L. ramada and L. saliens had a three times lower a Values are the mean Ϯ standard deviation for three replicate ratio of ⍀6to⍀3 when compared with L. aurata. The two experiments. ND, not detected (below the detection limit). other nutritional indices investigated, the IA (potential for J. Food Prot., Vol. 71, No. 12 SAFETY AND QUALITY ASSESSMENT OF LAGOON GREY MULLETS 2575

TABLE 3. Biogenic amine concentration on fresh weight of Liza aurata, Liza ramada, and Liza saliens after 4 days of storage in ice Amine concn (mg/kg)a

Species 2-PHE PU CA HI TY SD Total

Liza aurata 20.41 Ϯ 1.36 26.17 Ϯ 3.9 ND ND 27.36 Ϯ 0.14 28.30 Ϯ 0.12 102.24 Ϯ 4.46 L. ramada 19.51 Ϯ 3.29 3.57 Ϯ 5.05 8.80 Ϯ 1.52 3.32 Ϯ 4.7 23.85 Ϯ 5.4 22.16 Ϯ 2.61 81.21 Ϯ 1.58 L. saliens 16.50 Ϯ 0.82 4.96 Ϯ 0.29 2.94 Ϯ 4.15 3.16 Ϯ 4.46 41.12 Ϯ 7.03 34.79 Ϯ 2.81 103.47 Ϯ 3.07 a Values are the mean Ϯ standard deviation for three replicate experiments. 2-PHE, 2-phenylalanine; PU, putrescine; CA, cadaverine; HI, histamine; TY, tyramine; SD, spermidine; ND, not detected (below the detection limit). increasing serum lipids) and IT (potential for inducing nificantly to the development of fruity and rancid off-fla- thrombus formation), also were calculated. The IA for L. vors (14, 16). P. phosphoreum produced amounts of tri- Downloaded from http://meridian.allenpress.com/jfp/article-pdf/71/12/2572/2364831/0362-028x-71_12_2572.pdf by guest on 25 September 2021 aurata was significantly higher than that for the other two methylamine 10 to 100 times higher than those produced species, which had nearly the same value. The IT was about by S. putrefaciens but lower amounts of sulfur compounds two times higher in L. aurata than it was in L. ramada and (14, 16). L. saliens, which did not have significantly different IT val- The low biogenic amine concentrations found in L. au- ues. rata, L. ramada and L. saliens after 4 days of ice storage are compatible with their low contamination levels. How- DISCUSSION ever, biogenic amine production became evident when the L. aurata, L. ramada, and L. saliens maintained their bacterial load (total viable bacteria count) was higher than high quality during the storage period evaluated. The mi- 5 log CFU/g (25). In addition to the effect on the freshness crobiological data indicated that the limits imposed by the indices, some biogenic amines, particularly histamine and Italian Higher Institute of Nutrition (26) were never ex- tyrosine, can have toxic effects (27). However, histamine ceeded. Lower total aerobic bacteria counts and the absence was not detected in L. aurata and was found only sporad- of TC and E. coli characterized all three fish species after ically in L. ramada and L. saliens at levels not exceeding 4 days of storage in ice. Pathogenic species frequently as- 3.5 mg/kg, below the limit (100 mg/kg) indicated by the sociated with seafood and considered the major source of European Union for scombroid fishes. seafood-associated illness, such as Salmonella, L. mono- The analyses of heavy metals revealed that the Liza cytogenes, V. cholerae, V. parahaemolyticus, and A. hydro- species studied could be considered safe. Of particular in- phila (17) were never detected. However, the microbiolog- terest was the low level of mercury compared with those ical analyses provided information on the spoilage bacteria reported by the European Food Safety Authority (10) and on three fish species for which few reports are available. Gochfeld and Burger (13). The fatty acid analysis revealed The spoilage population of L. saliens was dominated by that the Liza species analyzed can be a good source of long- ⍀ H2S-producing bacteria (mainly S. putrefaciens and P. chain PUFAs, particularly the 3 variety. L. ramada and phosphoreum), whereas Pseudomonas spp. prevailed in L. L. saliens had three times higher concentrations of long- ramada and L. aurata. In previous studies, Pseudomonas chain ⍀3 PUFA than did L. aurata (11). Although the ratio spp. and H2S-producing bacteria were the specific spoilage of PUFA/SFA is commonly used to evaluate the fat quality, bacteria in fish from temperate and tropical waters (14) and all the SFAs are assumed to have negative effects on health. in fresh Mediterranean fish stored aerobically under refrig- However, ⍀6 PUFAs, whose parent member is linoleic eration or in ice. The low populations attained at the end acid, are beneficial in protecting against atheroma even of storage by the main microbial spoilage groups accounted when these PUFAs are only moderately increased in the for the low concentrations of TVNB detected in all fish diet, because high amounts of these PUFAs can lead to samples. The TVNB never exceeded a mean value of 12.56 high-density lipoprotein depression and low-density lipo- mg/100 g, far below the TVNB limit for human consump- protein lowering. In the three species studied, linoleic acid tion of 25 mg TVNB/100 g for other fishery products (1). was present at about 2.23 to 2.56% of the total fatty acid, Pseudomonas spp. can produce aldehydes, ketones, esters, indicating no particular difference regarding this fatty acid ⍀ ␣ H2S, and high-molecular-weight sulfur compounds from among the Liza species. Regarding the 3 fatty acids, -l- amino acid catabolism. These compounds contribute sig- inoleic acid is mainly found in plant tissues, and in mam-

TABLE 4. Water, protein, lipid, ash, and carbohydrate composition of Liza aurata, L. ramada, and L. saliens after 1 day of storage in ice Species Water (%) Proteins (%) Lipids (%) Ash (%) Carbohydrates (%)

Liza aurata 74.45 Ϯ 3.09a 20.09 Ϯ 2.51 3.64 Ϯ 0.96 1.42 Ϯ 0.03 0.40 Ϯ 0.07 L. ramada 74.35 Ϯ 3.32 19.81 Ϯ 2.75 3.66 Ϯ 0.61 1.58 Ϯ 0.24 0.60 Ϯ 0.08 L. saliens 76.04 Ϯ 3.66 18.45 Ϯ 2.11 3.73 Ϯ 0.12 1.28 Ϯ 0.94 0.5 Ϯ 0.08 a Values are the mean Ϯ standard deviation for three replicate experiments. 2576 SADO KAMDEM ET AL. J. Food Prot., Vol. 71, No. 12

TABLE 5. Fatty acid composition of Liza aurata, L. ramada, and L. saliens after 1 day of storage in ice Fatty acid concn (mg fatty acid methyl ester/100 mg fish oil)b

L. aurata L. ramada L. saliens Fatty acidsa Total fat (g/100 g fish, %): 6.40 Ϯ 0.56 4.66 Ϯ 0.39 4.15 Ϯ 0.34

Ϯ Ϯ Ϯ C14:0 6.15 0.57 4.99 0.44 4.39 0.41 Ϯ Ϯ Ϯ C15:0 3.49 0.33 2.67 0.23 2.45 0.22 Ϯ Ϯ Ϯ C16:0 13.56 1.11 13.39 1.21 13.27 1.24 Ϯ Ϯ Ϯ C17:0 0.11 0.02 0.38 0.02 0.61 0.05 Ϯ Ϯ Ϯ C18:0 0.92 0.08 1.06 0.09 1.52 0.16 Ϯ Ϯ Ϯ C22:0 0.06 0.01 0.10 0.01 0.09 0.01 Ϯ Ϯ C23:0 ND 0.23 0.02 0.21 0.02

⌺ SFA 24.23 Ϯ 2.11 22.49 Ϯ 2.16 22.24 Ϯ 2.40 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/71/12/2572/2364831/0362-028x-71_12_2572.pdf by guest on 25 September 2021 Ϯ Ϯ Ϯ C14:1 7.70 0.69 0.43 0.03 0.26 0.03 Ϯ Ϯ Ϯ C15:1 5.71 0.44 2.34 0.22 2.81 0.24 Ϯ Ϯ Ϯ C16:1n7 25.38 2.13 23.66 2.29 19.48 1.95 Ϯ Ϯ Ϯ C17:1 0.79 0.06 1.82 0.16 2.05 0.18 Ϯ Ϯ Ϯ C18:1n9 15.24 1.13 16.16 1.45 14.55 1.32 Ϯ Ϯ Ϯ C18:1n7 4.77 0.38 6.45 0.56 5.96 0.54 Ϯ Ϯ Ϯ C20:1n9 0.11 0.02 0.25 0.03 0.11 0.01 Ϯ Ϯ Ϯ C22:1n9 0.05 0.01 0.25 0.02 0.18 0.01 Ϯ Ϯ Ϯ C22:1n7 0.24 0.22 0.46 0.03 0.35 0.04 Ϯ Ϯ Ϯ C23:1 0.06 0.01 0.13 0.01 0.19 0.02 ⌺ MUFA 60.05 Ϯ 5.80 51.93 Ϯ 4.99 45.93 Ϯ 4.37 Ϯ Ϯ Ϯ C16:2n7 3.74 0.27 3.18 0.28 3.02 0.28 Ϯ Ϯ Ϯ C16:2n6 1.80 0.12 0.93 0.09 0.83 0.07 Ϯ Ϯ Ϯ C18:2n6 2.56 0.30 2.38 0.17 2.23 0.19 Ϯ Ϯ Ϯ C18:3n6 0.11 0.02 0.53 0.03 0.11 0.01 Ϯ Ϯ Ϯ C20:3n6 1.12 0.09 1.15 0.09 1.99 0.21 Ϯ Ϯ Ϯ C20:4n6 1.78 0.19 2.00 0.13 4.33 0.39 Ϯ Ϯ Ϯ C22:5n6 0.12 0.04 0.15 0.01 0.17 0.02 ⌺ PUFAd ⍀6 7.36 Ϯ 0.69 7.00 Ϯ 0.67 9.49 Ϯ 0.09 Ϯ Ϯ Ϯ C18:3n3 0.78 0.06 0.52 0.05 0.76 0.06 Ϯ Ϯ Ϯ C18:4n3 0.73 0.06 0.37 0.03 0.12 0.01 Ϯ Ϯ Ϯ C20:5n3 1.32 0.11 11.93 1.67 15.01 1.58 Ϯ Ϯ Ϯ C22:5n3 1.28 0.09 1.68 0.13 2.35 0.25 Ϯ Ϯ Ϯ C22:6n3 0.26 0.03 0.42 0.03 0.52 0.04 ⌺ PUFAn3 4.37 Ϯ 0.38 14.92 Ϯ 1.23 18.77 Ϯ 1.95 ⌺ PUFA 15.48 Ϯ 1.34 25.10 Ϯ 2.44 31.28 Ϯ 2.99 ⌺ PUFA/⌺ SFA 0.64 Ϯ 0.03 1.12 Ϯ 0.10 1.41 Ϯ 0.16 ⌺⍀6/⌺⍀3 1.68 Ϯ 0.14 0.47 Ϯ 0.03 0.51 Ϯ 0.04 IAc 0.51 Ϯ 0.04 0.43 Ϯ 0.04 0.40 Ϯ 0.03 ITd 0.43 Ϯ 0.02 0.25 Ϯ 0.02 0.22 Ϯ 0.03 a SFA, saturated fatty acids; MUFA, monounsaturated fatty acids; PUFA, polyunsaturated fatty acids. b Values are the mean Ϯ standard deviation for three replicate experiments. ND, not detected (below the detection limit). c IA, index of atherogenicity. d IT, index of thrombogenicity. mals these fatty acids are converted into longer PUFAs, the obtained on L. ramada, L. aurata, and L. saliens may en- most important of which are eicosapentaenoic acid (EPA) courage consumers to try these widespread but undercon- and docosahexaenoic acid (DHA), which are very effective sumed fish species, which score high on qualitative indices. at inhibiting platelet aggregation. L. ramada and L. saliens This information may help regulators to redefine recom- were very rich in EPA (more than 10 times higher) and mendations for fish consumption strictly dependent on con- DHA (2 times higher) with respect to L. aurata. Among sumer choice and nutrient and safety characteristics. the fish studied, L. aurata had the lowest nutritive quality REFERENCES regarding fat associated with the prevention of cardiovas- cular diseases. 1. Anonymous. 1995. Commission regulation (EC) no. 95/149/EC of 8 March 1995 fixing the total volatile basic nitrogen (TVB-N) limit Because the variability among fish species composi- values for certain categories of fishery products and specifying the tion, hazardous chemical substance contamination, and mi- analysis methods to be used. Off. J. Eur. Communities 97(29.04.95): crobiological quality is well documented, the information 84. J. Food Prot., Vol. 71, No. 12 SAFETY AND QUALITY ASSESSMENT OF LAGOON GREY MULLETS 2577

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