Octopus Lipid and Vitamin E Composition - American Chemical Society

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Octopus Lipid and Vitamin E Composition: Interspecies, Interorigin, and Nutritional Variability Á lvaro Torrinha,† Rebeca Cruz,‡ Filipa Gomes,† Eulália Mendes,‡ Susana Casal,*,‡ and Simone Morais*,† †

REQUIMTE, Instituto Superior de Engenharia do Porto, Instituto Politécnico do Porto, Rua Dr. António Bernardino de Almeida, 431, 4200-072 Porto, Portugal ‡ REQUIMTE, Laboratório de Bromatologia e Hidrologia, Faculdade de Farmácia, Universidade do Porto, Rua de Jorge Viterbo Ferreira, 228, 4050-313 Porto, Portugal S Supporting Information *

ABSTRACT: Octopus vulgaris, Octopus maya, and Eledone cirrhosa from distinct marine environments [Northeast Atlantic (NEA), Northwest Atlantic (NWA), Eastern Central Atlantic, Western Central Atlantic (WCA), Pacific Ocean, and Mediterranean Sea] were characterized regarding their lipid and vitamin E composition. These species are those commercially more relevant worldwide. Significant interspecies and interorigin differences were observed. Unsaturated fatty acids account for more than 65% of total fatty acids, mostly ω-3 PUFA due to docosahexaenoic (18.4−29.3%) and eicosapentanoic acid (11.4− 23.9%) contributions. The highest ω-3 PUFA amounts and ω-3/ω-6 ratios were quantified in the heaviest specimens, O. vulgaris from NWA, with high market price, and simultaneously in the lowest graded samples, E. cirrhosa from NEA, of reduced dimensions. Although having the highest cholesterol contents, E. cirrhosa from NEA and O. maya from WCA have also higher protective fatty acid indexes. Chemometric discrimination allowed clustering the selected species and several origins based on lipid and vitamin E profiles. KEYWORDS: octopus, fatty acids, cholesterol, vitamin E, nutritional assessment, chemometric discrimination

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INTRODUCTION

nutritional parameters such as total fat, fatty acids, cholesterol, and fat soluble vitamins are nowadays taken into account in order to maintain a good nutritional balance, since they are positively or negatively associated with health problems. To the best of our knowledge, O. vulgaris from MS5−9 and NEA10−13 have been analyzed for their fatty acids, but there is a lack of information on this subject concerning other geographical provenance, as well as regarding the other most relevant species, E. cirrhosa14 and O. maya.15 Also, data are very limited regarding the levels of cholesterol and vitamin E in these species and their different origins, being inexistent for O. maya. Furthermore, several studies16−18 reported that cephalopods are highly sensitive to the environmental changes during all stages of the cephalopod’s life, being able to respond to these changes actively (for example, migrating to areas with more propitious environmental conditions for feeding or spawning) or passively (using optimum environmental conditions to reach certain life stages at different growth rates between different generations).17 Thus, the aim of the present work was to characterize the total fat, fatty acids, cholesterol, and vitamin E concentrations in the arms of the three aforementioned species of octopus from distinct marine environments [NEA, Northwest Atlantic Ocean (NWA), Eastern Central Atlantic Ocean (ECA), Western Central Atlantic Ocean (WCA), PO, and MS]. The selected species are representative of the current octopus

Cephalopods are part of the traditional diet of Japan, Korea, Argentina, Taiwan, and China, and of coastal communities of southern Europe, such as Spain, Portugal, Morocco, Mauritania, Greece, and Italy. Unfortunately, octopus catches have been declining through time mainly due to stock overexploitation in some areas.1 Still, cephalopods comprise, in general, a major food resource for human consumption with catches of 3.77 million tonnes in 2010 and representing always high values in terms of auction transaction of the wholesale market registered for marine species.1,2 In terms of world trade and landing, Octopus vulgaris (common octopus), Eledone cirrhosa (curled octopus), and Octopus maya (Mexican four-eyed octopus) represent the most important octopus species available to consumers being those selected for this study. The two former species are the most abundant species from their taxonomical genus.3 Based on FAO information, the world geographical distribution of the three species is presented in Figure 1. As it can be seen, O. vulgaris have a wide distribution, being found in the Atlantic, Indian, and Pacific Oceans (PO) as well as in the Mediterranean Sea (MS). The endemic species O. maya is specifically found in the Yucatan peninsula, in the Gulf of Mexico. On the other hand, E. cirrhosa is distributed in the Northeast Atlantic Ocean (NEA) and in the MS.3 Seafood is known to be very important in human nutrition regarding the prevention of health disorders due to the presence of polyunsaturated fatty acids in their lipid composition [including the essential linoleic (C18:2) and alpha-linolenic (C18:3) acids, as well as docosahexaenoic (DHA; C22:6ω-3) and eicosapentanoic acids (EPA; C20:5ω3)]4 and octopus species are no exception. Thus, some © 2014 American Chemical Society

Received: Revised: Accepted: Published: 8508

May 28, 2014 July 30, 2014 August 3, 2014 August 4, 2014 dx.doi.org/10.1021/jf502502b | J. Agric. Food Chem. 2014, 62, 8508−8517

Journal of Agricultural and Food Chemistry

Article

Figure 1. Geographical distribution of (a) O. vulgaris, (b) O. maya, and (c) E. cirrhosa according to FAO (1984). and reconstituted in n-hexane. The remaining extract was hydrolyzed with KOH (0.5 mol/L in methanol) at 100 °C (10 min) and further methylated with BF3 (30 min at 100 °C) to convert the acyl-snglycerols and free fatty acids in the samples to volatile methyl esters (FAMEs). The lipids were extracted with n-hexane, and the solution was used initially for cholesterol quantification by HPLC, and thereafter for fatty acids analysis by GC-FID. HPLC Conditions for Vitamin E and Cholesterol Analysis. The liquid chromatograph consisted of a Jasco integrated system (Japan) equipped with an LC-NetII/ADC data unit, a refrigerated autosampler (AS-2057 Plus), a PU-980 Intelligent Pump, and a multiwavelength DAD (MD-910, recorded at 210 nm), connected in series to a FD (FP-2020 Plus; λexc = 290 nm and λem = 330 nm; gain 10). The chromatographic separation was achieved on a Supelcosil LC-SI column (75 × 3.0 mm, 3 μm; Supelco, Bellefonte, PA) operating at constant room temperature (23 °C). A mixture of nhexane and 1,4-dioxane (97.5:2.5, v/v) was used as eluent at a flow rate of 0.8 mL/min. Data were analyzed with the ChromNAV Control CenterJASCO Chromatography Data Station (Japan). The compounds were identified by chromatographic comparisons with authentic standards, by coelution, and by their UV spectra. Vitamin E was evaluated by the internal standard method based on the fluorescence data. Cholesterol was quantified at 210 nm, with calibration based on external standard solutions. Gas Chromatographic Conditions for Fatty Acids Analysis. Gas chromatography was performed on a Chrompack CP 9001 chromatograph (Chrompack, Middelburg, The Netherlands) equipped with a split−splitless injector, a flame-ionization detector, and a Chrompack CP-9050 autosampler. The temperatures of the injector and detector were 250 and 270 °C, respectively. Separation was achieved on a 50 m × 0.25 mm i.d. CP-Sil 88 column (0.19 μm film; Chrompack-Varian), using a temperature program from 140 to 220 °C. Helium was used as the carrier gas at an internal pressure of 120 kPa. Fatty acid identification (from C14:0 to C22:6ω-3) was accomplished by comparing the relative retention times of FAMEs of commercially available fatty acids methyl esters (Supelco 37-FAME mix, Supelco, USA). Total fatty acids content was estimated on the basis of the total fatty acid methyl ester area counts in comparison with the undecanoic methyl ester by converting the FAMEs to their respective fatty acid equivalents using the appropriate conversion factors. Individual fatty acids were initially quantified on a g/100 g fatty acids basis and then converted to mg/100 g wet weight (ww) using the fatty acid internal standard (C11:0) and moisture content. Saturated fatty acids (SFA) include 12:0, 14:0, 15:0, 16:0, 17:0, 18:0, 20:0, and 22:0; monounsatured fatty acids (MUFA) include 16:1 isomers (ω-7 plus ω-9), 18:1 (ω-7 and ω-9), 20:1ω-9, 22:1ω-9, and 24:1ω-9; while polyunsaturated fatty acids (PUFA) include several omega-6 (18:2ω-6, 20:2ω-6, 20:3ω-6, 20:4ω-6, and 22:4ω-6) and omega-3 (18:3ω-3, 20:5ω-3, 22:2ω-6, 22:5ω-3, and 22:6ω-3) fatty acids. Nutritional Assessment. The most relevant nutritional lipid quality indexes such as total ω-3/ω-6 ratio, PUFA/SFA, DHA + EPA sum, atherogenicity index (AI), thrombogenicity index (TI), and hypocholesterolemic:hypercholesterolemic ratio (HH) were estimated.24 AI, TI, and HH indexes were calculated using eqs 1, 2, and 3, respectively:

generally consumed worldwide, being those commercially available in Portugal. The interspecies and interorigin composition variability and the associated benefit−risk balance of consumption of these species were evaluated. Also, the suitability of using fatty acids, cholesterol, and vitamin E concentrations as chemical descriptors to differentiate the octopus species and oceanic provenance was assessed.

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MATERIAL AND METHODS

Reagents. For cholesterol, vitamin E, fatty acids, and total fat analysis, propan-2-ol, cyclohexane, and HPLC grade n-hexane were purchased from Merck (Darmstadt, Germany), while 1,4-dioxane was from Sigma-Aldrich (Steinheim, Germany). Methanol and potassium hydroxide were acquired from Panreac (Spain). Boron trifluoride in methanol (14%), butylated hydroxytoluene (BHT), and ascorbic acid were obtained from Sigma-Aldrich. The internal standard for fatty acids quantification, triundecanoin, was also from Sigma-Aldrich (Steinheim, Germany), while the internal standard for vitamin E quantification, tocol, was obtained from Matreya (USA). Alfatocopherol and cholesterol standards were from Sigma-Aldrich (Steinheim, Germany), and the fatty acids methyl esters (FAMEs) standard was from Supelco (Bellefonte, PA). All other chemicals were of analytical grade from diverse suppliers. Sample Collection. Octopus (n = 69) from the different geographical origins available to Portuguese consumers was purchased frozen randomly from the markets in the NW region of Portugal during spring 2012. The species collected were O. vulgaris from NWA (n = 8), NEA (n = 8), ECA (n = 8), WCA (n = 8), PO (n = 8), and MS (n = 5); O. maya from ECA (n = 8) and WCA (n = 8); and E. cirrhosa from NEA (n = 8). The origin was established based on the label information, as well as the date of capture (from 11 October to 9 December 2011). Sample collection, biometric characterization, and preparation were performed in accordance with the EPA Guide No. 823-B-00-07, DL No. 187/2005,19 and CE Regulation No. 333/ 2007.20 Specimens were carefully identified and manually eviscerated. Only the edible tissues were preserved. Homogenization was performed mechanically with a blender until a smooth paste was obtained. For each sample, three independent subsamples were defined. Samples were preserved at −18 °C, and subportions were freeze-dried (Telstar Cryodos-80, Terrassa, Barcelona) for fatty acid, cholesterol, and vitamin E quantification. Moisture was evaluated using 10 g of sample according to the Portuguese Standard NP 2282-1991 and the official AOAC method.21 Fatty Acids, Cholesterol, and Vitamin E Analysis. For total fat content, approximately 1 g (accurately weighed) of the homogenized sample was extracted with 30.0 mL of acetone:ether petroleum (1:2, v/v) by microwave-assisted extraction, according to Ramalhosa et al.22 Extraction and analysis of fatty acids, cholesterol, and vitamin E were performed according to a validated study, conducted by Cruz and co-workers.23 Briefly, an accurate freeze-dried sample portion (300 mg) was extracted with a ternary mixture of propan-2-ol, cyclohexane, and 0.9% (m/v) KCl, in the presence of the internal standards (tocol and triundecanoate), plus antioxidants (ascorbic acid and BHT). Onethird of the organic extract was directly used for vitamin E analysis by HPLC, after being taken to dryness under a gentle nitrogen stream 8509

dx.doi.org/10.1021/jf502502b | J. Agric. Food Chem. 2014, 62, 8508−8517


Article

Figure 2. Biometric parameters (□, mean; rectangles, mean ± standard deviation; bars above and below rectangles, range) of the characterized octopus species (n = 69). Each letter (a−i) corresponds to a species and inherent origin (a, O. vulgaris from Northeast Atlantic Ocean (NEA); b, O. vulgaris from Northwest Atlantic Ocean (NWA); c, O. vulgaris from Eastern Central Atlantic Ocean (ECA); d, O. vulgaris from Western Central Atlantic Ocean (WCA); e, O. vulgaris from Pacific Ocean (PO); f, O. vulgaris from Mediterranean Sea (MS); g, O. maya from ECA; h, O. maya from WCA; i, E. cirrhosa from NEA). The same letters in a box plot indicate that the given means are not statistically different (p > 0.05). AI =

C12:0 + 4 × C14:0 + C16:0 ∑ MUFA + ∑ ω‐3 + ∑ ω‐6

(1)

TI =

C14:0 + C16:0 + C18:0 0.5∑ MUFA + 0.5∑ ω‐6 + 3∑ ω‐3

(2)

highly heterogeneous in length and weight, particularly O. vulgaris from the MS, which hindered the identification of biometric differences between the several tested species and geographical origins. Still, this high variability is in accordance with other documented results and may be related to biological factors.7,10,12,13,25,26 Fatty Acids Composition. In opposition to the biometric data, the fatty acids composition (as relative percentage of total fatty acids) was highly homogeneous in terms of fatty acids classes among the samples analyzed. PUFA is the more abundant class, followed by SFA and MUFA. Total PUFA ranged from 51.9% (O. maya from ECA) to 59.0% (O. vulgaris from NWA), followed by SFA from 25.6% (E. cirrhosa from NEA) to 31.1% (O. maya from ECA) and MUFA from 11.6% (O. vulgaris from WCA and MS) to 14.1% (O. vulgaris from NEA). Unsaturated fatty acids (PUFA + MUFA) account for more than 65% of total fatty acids. The majority of the published studies in octopus composition concern O. vulgaris caught in MS. The attained results for this species are in accordance with Estefanell et al.,5,6 Ozogul et al.,7 and Passi et al.8 while much higher SFA contents were reported by Karakoltsidis et al.9 (41%). In particular, some authors have determined the fatty acid profiles of O. vulgaris captured in NEA. The reported values are similar to ours with only slight variations: SFA 31.9−34.6%, MUFA 9.2−11.6%, PUFA 55.7%;10 SFA 27.3−33.2%, MUFA 9.6−10.4%, PUFA 54.8−59.2%;12 SFA 34.2−40.8%, MUFA 4.5−7.9%, PUFA 47.6−56.4%;11 SFA 25.9%, MUFA 15.5%, PUFA 58.6%.13 The results reached for O. vulgaris from PO and E. cirrhosa are also

HH = (C18:1ω‐9 + C18:2ω‐6 + C20:4ω‐6 + C18:3ω‐3 + C20:5ω‐3 + C22:5ω‐3 + C22:6ω‐3)/(C14:0 + C16:0)

(3) Statistical Analysis. Statistical analysis was performed using the SPSS (IBM SPSS Statistics 20) and Statistica software (v. 7, StatSoft Inc., USA). Data were expressed as mean ± standard deviation and range and were grouped according to species and origins. Mean values were compared through the nonparametric Mann−Whitney U test, since normal distribution was not observed by Shapiro−Wilk’s test. Statistical significance was defined as p ≤ 0.05. Principal components analysis (PCA) was applied, after variable standardization to mean zero and unit variance to assess which variables may be used as chemical descriptors among the three species or origins.

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RESULTS AND DISCUSSION Biometric Data. The collected biometric data is presented in Figure 2. Generally, E. cirrhosa may be clearly distinguished from the other species due to its statistically significantly reduced dimensions, which explain its lower market price. On average, the heavier specimens were from O. vulgaris from NWA (1443 ± 336 g) while the biggest (14.0 ± 3.7 cm for mantle, 56.3 ± 17.9 cm for tentacle, and 70.3 ± 21.0 cm for total length) were from MS O. vulgaris species. Generally, the commercialized individuals of each species and origin were 8510



Article

from WCA exhibits the highest levels (1.6−3.9 times higher) of ω-6 PUFA mainly due to the contributions of ARA and C22:4ω-6 and supported by the higher lipids content. MUFA content ranged from 23.0 mg/100 g ww (O. vulgaris from MS and O. maya from ECA) to 126 mg/100 g ww (for E. cirrhosa from NEA). Oleic acid (C18:1; here reported as the sum of ω-7 and ω-9 isomers) was the most abundant within the monounsaturated class representing 31% (O. vulgaris from PO) to 46% (O. vulgaris from NWA) of the total MUFA mean amounts. Considering all species and origins, the strongest significant differences in C18:1 concentrations were detected between E. cirrhosa and the others (p < 0.01), as well as among O. vulgaris NWA and all the species apart from O. maya from WCA. Within the studied O. vulgaris sources, individuals from the NWA location presented the major statistical differences. SFA values varied from 51 mg/100 g ww (O. maya from ECA) to 219 mg/100 g ww (E. cirrhosa from NEA). Statistical differences were found between E. cirrhosa and the other species (p < 0.01), as well as among O. maya WCA and all the remaining ones (p < 0.01). Palmitic acid (C16:0) followed by stearic acid (C18:0) were the compounds that contributed most for the total SFA mean. C16:0 corresponded to 13.9% (O. maya WCA) to 17.7% (O. vulgaris NWA) while C18:0 represented 5.4% (E. cirrhosa NEA) to 10.4% (O. maya ECA). The same statistical differences as those for the SFA class were found between species for C16:0 and C18:0. Among all the factors influencing cephalopod fatty acid composition, diet is the most important and what affects most.30 Several reports about cultured octopus have shown that fatty acid profile is significantly affected by the prey composition.28,31−33 The availability of certain preys and the feeding habits of the species are connected, to some extent, with the geographical region. Octopus lipid composition is also largely influenced by water temperature (which depends on location and season), such that in colder water they store more fat.15,34 Other influencing factors are oogenesis, spermatogenesis, and starvation of females during brooding.7,9,11,12 Vitamin E. The high prevalence of unsaturated fatty acids requires effective measures to protect them from oxidation. In nature, vitamin E levels are usually allied with high concentrations of unsaturated fatty acids.35,36 The oxidation of a methyl group in PUFA gives formation to a free radical by a hydrogen atom removal becoming reactive and goes under chain reaction. Vitamin E that is incorporated in biological membranes acts as chain-breaking antioxidant. The phenol group of vitamin E compounds donates a hydrogen atom to the peroxyl radical, forming a tocopherol radical and a lipid hydroperoxide. The tocopherol radical can then link to another peroxyl radical forming inactive molecular products.35 Vitamin E embraces several lipophilic tocochromanols with antioxidant properties, but in the octopus samples analyzed only α-tocopherol was detected and quantified. As expected, higher amounts of vitamin E were quantified in the samples with higher PUFA amounts (Figure 3 and Table 1). Detectable concentrations of vitamin E varied from 0.29 (for O. vulgaris from WCA) to 2.5 mg/100 g ww (for O. vulgaris from NWA). The results varied about a factor of 10 showing high intervariability between species and origins. The mean vitamin E content of O. vulgaris from NWA (1.60 ± 0.5 mg/100 g ww), E. cirrhosa from NEA (1.25 ± 0.46 mg/100 g ww), and O. vulgaris from PO (1.00 ± 0.45 mg/100 g ww) may be clearly distinguished from the other species by their highest contents. No statistical differences were verified between the mean of E.

in agreement with those scarce previously published (Turner et al.27 for O. vulgaris from PO; Rosa et al.14 for E. cirrhosa). To the best of our knowledge, no information exists in the literature about fatty acids composition of O. vulgaris from NWA, ECA, and WCA, as well as wild O. maya. Studies concerning reared octopus were not used for comparison purposes since marine specimens created in captivity show differences from the wild ones because feeding habits are different.28 In recent years, chemical and nutritional compositions of cephalopods have been extensively studied for aquaculture and industrial production purposes. Benthic species like O. vulgaris and O. maya are examples with high potential for aquaculture due to the worldwide high consumption demand and to their physiological, behavioral, and environmental characteristics.28 Regarding the fatty acids composition on an edible basis (mg/100 g ww) only the ones with more quantitative/ nutritional importance are detailed in Table 1. There were wide variation and significant differences (p < 0.05) among the fatty acid profiles of the different species and origins in terms of total and individual compounds. Overall, E. cirrhosa stands out for its statistically significantly greater concentrations of the three main classes of fatty acids (SFA, MUFA, and PUFA) followed by O. maya from WCA. The MUFA and PUFA levels of O. maya from WCA were only similar to those from O. vulgaris from NWA. Within the different oceanic regions of O. vulgaris, the maximum total fatty acids mean (including the higher average value per fatty acid class) was observed in specimens from NWA. In contrast, the poorest species in fatty acids content was the most expensive and consumed worldwide species, O. vulgaris from MS. Still, its PUFA and SFA levels were similar to those from the same species from NEA and ECA, as well as to those of O. maya from ECA. Concerning total PUFA averages, more than 56% (O. maya from WCA) up to 89% (O. vulgaris from NWA) are ω-3 fatty acids, ranging respectively from 83 ± 27 to 341 ± 60 mg/100 g on a fresh basis. Marine organisms living in cold waters have usually a higher percentage of ω-3 fatty acids composition,29 which is consistent with this benthic species. The compounds that contributed most for total PUFA proportions in the fatty acids were, by descending order, docosahexaenoic acid (DHA; C22:6ω-3) with 18.4% for O. maya from ECA (47 ± 18 mg/ 100 g ww) to 29.3% for E. cirrhosa from NEA (195 ± 31 mg/ 100 g ww), followed by eicosapentanoic acid (EPA; C20:5ω-3) ranging 11.4% for O. maya WCA (31 ± 11 mg/100 g ww) to 23.9% (94 ± 11 mg/100 g ww) for O. vulgaris NWA, and arachidonic acid (ARA; C20:4ω-6) with 4.6% for O. vulgaris NWA (19 ± 2 mg/100 g ww) to 19.4% for O. maya WCA (86 ± 10 mg/100 g ww). This pattern of variation is slightly different for O. vulgaris from WCA and PO, as well as for O. maya from ECA due to the higher contribution of ARA than EPA. In absolute amounts, as consumed, the lowest DHA (27 mg/100 g ww) and EPA (15 mg/100 g ww) contents were detected in O. maya from ECA while the highest were determined in E. cirrhosa from NEA, with 252 and 171 mg/100 g ww, respectively. Interestingly, the same O. maya but from WCA was the third group with higher DHA amounts (82 ± 11 mg/100 g), just after O.vulgaris from NWA. DHA and EPA are important in marine species since they are components in membrane cells where they maintain structural functions and their extremely low freezing temperatures are consistent with the demands of a life in cold seas. Taking a deeper look into the ω-6 PUFA concentrations, it can be also observed that O. maya 8511


8512

ω-3/ω-6

PUFAd

C22:6ω-3 (DHA) ω-3 PUFA

C20:5ω-3 (EPA) C22:5ω-3

C20:3ω-3

C18:3ω-3

ω-6 PUFA

C22:4ω-6

C20:4ω-6 C22:2ω-6

C20:2ω-6

C18:2ω-6

MUFAc

C18:1 C20:1ω-9

C16:1

SFAb

115 ± 50 a (60− 190) 145 ± 44 a (101− 217) 4.9 ± 2.8 a (1.4− 8.4)

4.5 ± 1.4 a (3.2− 6.9) 63 ± 23 a (38−99)

0.6 ± 0.1 ab (0.5− 0.8) 3.0 ± 0.5 b (2.5− 4.1) 94 ± 11 b (80− 112) 6.5 ± 1.1 b (4.6− 8.1) 102 ± 12 b (87− 125) 206 ± 24 b (181− 249) 232 ± 25 b (206− 276) 9.2 ± 1.2 b (7.1− 10.8)

C20:0

0.7 ± 0.2 a (0.5− 1.3) 1.3 ± 1.0 a (0.3− 2.8) 46 ± 25 a (18−82)

0.3 ± 0.1 ab (0.1− 0.4) 109 ± 10 b (96− 122) 6.2 ± 1.0 ab (5.1− 8.2) 23 ± 4 b (17−30) 10.1 ± 1.3 b (8.4− 11.6) 50 ± 8 b (38−60)

0.4 ± 0.3 a (0.1− 1.1) 79 ± 19 a (56− 109) 6.0 ± 1.0 a (4.4− 7.5) 15 ± 4 a (10−21) 6.6 ± 3.2 a (3.0− 11.4) 38 ± 8 a (30−53)

C18:0

C16:0

3.5 ± 1.5 b (1.3− 6.0) 0.5 ± 0.8 b (0.1− 2.9) 19 ± 2 ab (16−23) 0.5 ± 0.3 b (0.2− 1.2) 1.4 ± 0.3 b (1.0− 2.0) 23 ± 3 ab (20−30)

28 ± 2 b (24−32)

20 ± 4 a (14−24)

total fatty acids C14:0

2.2 ± 0.8 a (1.2− 3.4) 1.3 ± 0.5 a (0.7− 2.1) 21 ± 8 a (13−34) 0.9 ± 0.2 a (0.7− 1.4) 2.2 ± 1.3 a (1.1− 4.5) 28 ± 10 a (18−45)

81.5 ± 1.0 b (80.7− 82.8) 394 ± 40 b (346− 457) 3.9 ± 1.5 ab (2.0− 6.3) 69 ± 8 b (60−79)

88.7 ± 3.6 a (84.5−92.4) 271 ± 73 a (194− 389) 3.1 ± 1.3 a (1.3− 4.7) 44 ± 15 a (28−65)

moisture

NWA (n = 8)

NEA (n = 8)

0.6−0.2 abc (0.4− 1.7 ± 0.7 d (1.0− 1.0) 3.6) 1.0 ± 0.4 ac (0.5− 0.6 ± 0.2 ad (0.4− 1.6) 1.0) 49 ± 14 ac (30−65) 41 ± 8 acd (28− 51) 5.2 ± 1.1 c (4.2− 5.8 ± 0.6 bd (5.0− 7.1) 6.7) 62 ± 14 ac (44−78) 64 ± 8 acd (55− 79) 119 ± 28 ac (87− 113 ± 14 acd (96− 148) 137) 143 ± 32 ac (104− 184 ± 12 d (161− 178) 202) 5.3 ± 1.1 ac (3.8− 1.7 ± 0.5 d (1.1− 6.7) 2.3)

0.4 ± 0.2 abcd (0.2−0.9) 103 ± 9 bd (85− 114) 8.3 ± 1.2 c (5.8− 8.6 ± 1.6 cd (6.2− 10.3) 11.7) 11 ± 3 c (7−15) 17 ± 4 ad (13−24) 6.3 ± 2.1 ac (3.9− 6.7 ± 0.9 acd (6.0− 9.4) 9.4) 34 ± 6 ac (26−43) 39 ± 5 acd (33− 48) 1.4 ± 0.5 c (0.7− 1.9 ± 0.5 acd (1.4− 2.1) 2.8) 1.1 ± 0.4 ac (0.8− 1.8 ± 0.2 d (1.4− 1.8) 2.2) 17 ± 4 abc (10−22) 56 ± 11 d (41−72) 0.6 ± 0.2 bc (0.2− 0.9 ± 0.2 ad (0.7− 0.9) 1.2) 1.8 ± 0.4 ac (1.2− 7.3 ± 2.5 d (4.7− 2.4) 11.6) 23 ± 5 abc (14−29) 69 ± 15 d (50−92)

0.3 ± 0.2 bc (0.1− 0.7) 73 ± 13 ac (58−87)

18 ± 3 ac (14−22)

85.9 ± 0.6 ad (85.6−86.7) 337 ± 24 ad (289− 364) 3.5 ± 0.3 abcd (3.1−4.0) 48 ± 5 acd (38− 57) 33 ± 2 d (28−36)

WCA (n = 8)

O. vulgaris 91.7 ± 4.1 ac (88.4− 97.4) 257 ± 50 ac (196− 311) 3.1 ± 1.2 abc (2.0− 5.0) 42 ± 9 ac (32−53)

ECA (n = 8)

113 ± 13 acde (100− 134) 174 ± 19 acde (142− 202) 2.2 ± 0.9 de (1.2− 3.6)

7.0 ± 3.1 bcde (4.4− 12.3) 65 ± 8 acde (42−74)

0.9 ± 0.4 ace (0.2− 1.4) 0.6 ± 0.1 ade (0.4− 0.7) 39 ± 11 ade (26−57)

1.9 ± 0.9 acde (0.8− 3.0) 2.5 ± 1.0 de (1.2− 3.9) 45 ± 16 e (28−69) 1.0 ± 0.5 ade (0.2− 1.7) 5.7 ± 2.1 de (3.0− 8.7) 59 ± 21 de (34−90)

0.8 ± 1.1 ade (0.2− 4.1) 90 ± 21 ade (59− 117) 8.1 ± 1.7 cde (5.9− 11.6) 14 ± 3 ade (11−17) 8.1 ± 4.5 abcde (3.9− 15.0) 45 ± 5 abe (32−52)

89.2 ± 0.6 ace (88.5− 89.9) 319 ± 42 ade (254− 375) 3.4 ± 0.5 abcde (2.9− 4.2) 46 ± 11 acde (29− 58) 28 ± 9 bde (16−39)

PO (n = 8)

ECA (n = 8)

WCA (n = 8)

144 ± 27 ah (100− 175) 257 ± 35 bh (204− 316) 1.3 ± 0.2 gh (1.0− 1.5)

1.7 ± 0.6 dh (1.1− 2.7) 0.8 ± 0.2 acfh (0.6− 1.2) 50 ± 14 acfh (27− 65) 9.9 ± 3.0 h (6.9− 15.0) 82 ± 11 ah (64−96)

2.8 ± 0.4 abh (2.2− 3.7) 2.6 ± 0.4 eh (2.0− 3.1) 86 ± 10 h (75−108) 1.0 ± 0.2 adefgh (0.7−1.5) 12.9 ± 2.1 h (9.9− 17.2) 110 ± 12 h (98−138)

0.1 ± 0.1 h (n.d. 0.3) 129 ± 15 h (110− 148) 9.9 ± 2.5 cdeh (6.1− 13.3) 25 ± 4 bh (20−31) 9.1 ± 1.5 abeh (6.3− 11.5) 55 ± 8 bh (43−73)

44 ± 4 h (38−52)

86.1 ± 1.7 adh (84.0−88.0) 450 ± 53 h (386− 531) 3.3 ± 0.8 abcdefh (2.4−5.2) 62 ± 8 h (51−74)

O. maya 92.2 ± 2.0 acfg (90.5−94.9) 263 ± 102 acfg (181−448) 2.1 ± 0.6 ag (1.4− 3.0) 40 ± 18 acefg (23− 71) 17 ± 2 acf (14−22) 26 ± 12 aeg (17− 49) 0.9 ± 0.5 ef (0.2−1.7) 1.2 ± 1.3 abcdefg (0.2−4.1) 69 ± 6 acf (57−76) 82 ± 36 acefg (51− 147) 7.0 ± 1.2 abef (5.1− 4.4 ± 1.6 g (2.5− 9.2) 7.1) 11 ± 1 cf (9−13) 14 ± 5 acefg (9−24) 5.6 ± 1.4 acdef (4.1− 4.5 ± 1.0 aeg (3.3− 7.2) 5.8) 28 ± 3 f (23−31) 35 ± 10 acdg (23− 54) 1.8 ± 0.6 acdef (0.9− 2.1 ± 1.4 acdefg 2.5) (0.9−4.6) 1.2 ± 0.2 acf (0.9− 2.0 ± 2.1 acg (0.6− 1.5) 5.7) 21 ± 6 abcf (16−33) 39 ± 24 eg (18−81) 0.9 ± 0.2 adef (0.7− 0.9 ± 0.6 acdefg 1.2) (0.4−2.0) 2.3 ± 0.8 acf (1.7− 4.9 ± 4.0 efg (1.6− 3.6) 11.7) 27 ± 7 abf (22−41) 51 ± 35 eg (23− 111) 0.6 ± 0.3 abcf (0.1− 1.0 ± 0.5 aeg (0.5− 1.0) 1.9) 1.4 ± 0.8 acdf (0.3− 0.4 ± 0.2 deg (0.2− 2.3) 0.7) 44 ± 12 acdef (31− 31 ± 11 adeg (15− 60) 46) 3.9 ± 0.6 af (3.2−4.9) 4.3 ± 2.4 afg (2.2− 8.6) 59 ± 13 acdef (43− 47 ± 18 aefg (27− 77) 76) 109 ± 26 acdef (80− 83 ± 27 afg (45− 140) 117) 138 ± 23 acf (105− 137 ± 55 acfg (92− 166) 233) 4.3 ± 1.6 af (2.2−5.9) 2.2 ± 1.3 deg (1.0− 3.8)

91.0 ± 2.8 acef (88.5−94.3) 241 ± 32 acf (190− 277) 2.8 ± 0.5 abcf (2.3− 3.6) 39 ± 5 acef (32−46)

MS (n = 5)

12.7 ± 4.0 i (9.3− 20.4) 195 ± 31 i (150− 252) 341 ± 60 i (257− 448) 403 ± 74 i (298− 536) 5.9 ± 0.7 ai (4.6− 6.7)

127 ± 24 i (94−171)

1.5 ± 0.5 dhi (0.9− 2.2) 4.6 ± 1.4 i (2.6−6.5)

4.3 ± 1.2 egi (2.7− 6.8) 59 ± 14 egi (39−83)

3.6 ± 1.2 bi (2.4− 5.8) 2.2 ± 0.9 dei (1.3− 4.0) 40 ± 10 egi (28−56) 3.8 ± 1.0 i (2.5−5.6)

2.9 ± 3.5 fgi (0.2− 12.5) 176 ± 25 i (138− 219) 10.0 ± 1.4 hi (7.8− 12.8) 34 ± 9 i (25−49) 18.0 ± 2.6 i (14.8− 22.9) 89 ± 20 i (68−126)

36 ± 5 di (28−46)

84.1 ± 1.6 abdhi (82.0−85.9) 686 ± 119 i (518− 901) 4.7 ± 0.7 bi (3.8− 5.7) 108 ± 15 i (87−130)

NEA (n = 8)

E. cirrhosa

Table 1. Moisture (%) and Total and Fatty Acids Composition (Mean ± Standard Deviation and Range; mg/100 g wet weight) in the Arms of Octopus from Different Originsa

Journal of Agricultural and Food Chemistry Article


Each letter (a−i) corresponds to a species and inherent origin (a, O. vulgaris from Northeast Atlantic Ocean (NEA); b, O. vulgaris from Northwest Atlantic Ocean (NWA); c, O. vulgaris from Eastern Central Atlantic Ocean (ECA); d, O. vulgaris from Western Central Atlantic Ocean (WCA); e, O. vulgaris from Pacific Ocean (PO); f, O. vulgaris from Mediterranean Sea (MS); g, O. maya from ECA; h, O. maya from WCA; i, E. cirrhosa from NEA). The same letters in a row indicate that the given means are not statistically different (p > 0.05). bSFA = saturated fatty acids. cMUFA = monounsaturated f ́ TI = thrombogenic index. gHH = hypocholesterolaemic/hypercholesterolaemic ratio. fatty acids. dPUFA = polyunsaturated fatty acids. eAI = atherogenic index.

Article

Figure 3. Vitamin E concentrations (□, mean; rectangles, mean ± standard deviation; bars above and below rectangles, range; mg/100 g wet weight) in the edible tissues of the characterized octopus species. Each letter (a−i) corresponds to a species and inherent origin (a, O. vulgaris from Northeast Atlantic Ocean (NEA); b, O. vulgaris from Northwest Atlantic Ocean (NWA); c, O. vulgaris from Eastern Central Atlantic Ocean (ECA); d, O. vulgaris from Western Central Atlantic Ocean (WCA); e, O. vulgaris from Pacific Ocean (PO); f, O. vulgaris from Mediterranean Sea (MS); g, O. maya from ECA; h, O. maya from WCA; i, E. cirrhosa from NEA). The same letters in a box plot indicate that the given means are not statistically different (p > 0.05).

cirrhosa and those of O. vulgaris from NWA and from PO. In contrast, O. maya ECA was the octopus with the lowest vitamin E content, being simultaneously among the ones with lower PUFA content. Statistical differences were found between O. maya ECA and all the other species (p = 0.01). Data concerning vitamin E levels in octopus species are quite scarce and were not found for O. vulgaris from NWA, ECA, WCA, and PO, as well as for O. maya and E. cirrhosa. The attained concentrations for O. vulgaris from MS and NEA are in agreement with those previously reported by Passi et al.8 (0.74 mg/100 g ww for O. vulgaris from MS), Nunes et al.37 (0.73 mg/100 g ww for O. vulgaris from NEA), and Dias et al.38 (0.78 mg/100 g ww for O. vulgaris consumed in Portugal with no indication of the geographical provenance). Villanueva and coworkers36 characterized the vitamin E contents in the early life stages of O. vulgaris laboratory hatchlings and wild juveniles (9.2−14.2 g ww) from MS. They reported a much higher value (9.1 mg/100 g ww) possibly because vitamin E content seems to be higher in the early stages of cephalopods compared to adult stages and due to the fact that vitamin E was analyzed in whole octopus instead of in edible parts. It is known that digestive gland and gonads have higher contents of lipids than muscle parts.10,14 Cholesterol. Cephalopod consumption is usually associated with elevated cholesterol ingestion. Cholesterol plays an important role in cephalopods, with structural functions in cell membranes, and acts as a precursor of steroid hormones.14 In opposition, and humans having the inherent ability to synthesize cholesterol, dietary cholesterol has been positively associated with low density lipoprotein (LDL) cholesterol and deleterious health outcomes. Therefore, in order to support adequately the data obtained from the nutritional point of view, the intra- and interspecific variability of the cholesterol concentrations in octopus edible tissues was also analyzed (Figure 4). Cholesterol mean content ranged from 85 ± 14

a

HHg

TIf

AIe

E. cirrhosa

1.6 ± 0.1 adeghi (1.5−1.6) 0.26 ± 0.03 degi (0.23−0.29) 0.14 ± 0.01 i (0.12− 0.15) 3.7 ± 0.4 bdefghi (3.2−4.2) 1.7 ± 0.4 adegh (1.5− 2.4) 0.24 ± 0.03 eh (0.20−0.28) 0.22 ± 0.03 degh (0.19−0.28) 4.0 ± 0.6 deh (3.1− 4.8) 1.6 ± 0.6 acdefg (1.0−2.4) 0.28 ± 0.02 deg (0.24−0.29) 0.23 ± 0.06 deg (0.17−0.29) 3.4 ± 0.4 abcefg (3.1−4.0) 1.4 ± 0.1 acdef (1.2− 1.6) 0.30 ± 0.02 abcf (0.27−0.33) 0.17 ± 0.03 abcef (0.14−0.20) 3.4 ± 0.3 abcef (3.1− 3.8) 1.8 ± 0.6 ade (1.2− 2.7) 0.27 ± 0.05 abde (0.20−0.37) 0.20 ± 0.05 ade (0.12−0.27) 3.7 ± 0.8 abcde (2.4− 5.1) 1.1 ± 0.1 b (1.0− 1.2) 0.30 ± 0.03 ab (0.26−0.37) 0.15 ± 0.01 b (0.14−0.18) 3.4 ± 0.2 ab (2.9− 3.7) DHA/EPA

1.6 ± 0.4 a (1.2− 2.2) 0.30 ± 0.03 a (0.24−0.35) 0.18 ± 0.03 a (0.15−0.25) 3.3 ± 0.2 a (3.1− 3.7)

1.3 ± 0.2 ac (1.1− 1.7) 0.31 ± 0.03 abc (0.27−0.35) 0.16 ± 0.01 ac (0.15−0.17) 3.3 ± 0.2 abc (3.1− 3.7)

1.6 ± 0.3 ad (1.4− 2.1) 0.28 ± 0.02 d (0.25−0.30) 0.22 ± 0.02 d (0.19−0.24) 3.7 ± 0.2 d (3.4− 4.0)

MS (n = 5) PO (n = 8) WCA (n = 8) NWA (n = 8) NEA (n = 8)

Table 1. continued

ECA (n = 8)

O. vulgaris

ECA (n = 8)

O. maya

WCA (n = 8)

NEA (n = 8)


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other factors, besides dietary, such as the demand during oogenesis and spermatogenesis, may affect the cholesterol content in cephalopods. Nutritional Assessment. Although no specific data concerning octopus per capita consumption were found, cephalopod species are highly appreciated, particularly in Mediterranean and Asian countries. According to FAO,1 in 2010 the average cephalopod intake varied widely worldwide, being 3.4 kg per capita per year in Portugal and reaching 6.5 kg per capita per year in Korea, of which octopuses represent an important part. Nowadays, there is clear evidence that the type of fat is more important in diminishing metabolic and cardiovascular disease risk than the total quantity of fat in the diet.4 In addition, marine lipids are generally regarded as healthy, due to their high amounts of long chain PUFA, particularly EPA and DHA. Thus, to assess the potential health outcomes from the consumption of the characterized octopus species, the most important nutritional quality indexes were analyzed. Regarding the fatty acid composition, all the selected species had a favorable ω-3/ω-6 ratio, from 1.7 ± 0.5 to 9.2 ± 1.2 for O. vulgaris from WCA and NWA, respectively, 1.3 ± 0.2 to 2.2 ± 1.3 for O. maya from WCA and ECA, respectively; and 5.9 ± 0.7 for E. cirrhosa from NEA, confirming the importance of these species for ingestion of ω-3 PUFAs. The geographical provenance of O. vulgaris showed a marked influence on this ratio. A portion of 78 g (E. cirrhosa from NEA) to 321 g (O. maya from ECA) provides 250 mg of DHA + EPA, the daily recommended intake.42 DHA and EPA are described as hypotriacylglycerolemic, antiarrhythmic, antiatherogenic, antithrombotic, and anti-inflammatory, being considered as protective agents against coronary heart diseases.43 Also, the attained PUFA/SFA ratios are significantly higher (1.7 for O. maya from ECA to 2.2 for E. cirrhosa from NEA) than the recommended minimum of 0.45.44 The atherogenic and thrombogenic indexes, AI and TI, estimated on the basis of the fatty acid composition, are indicative of potential cardiovascular disease risk factors and therefore must be kept low. The fatty acid influence on cholesterol synthesis is also frequently estimated by the hypocholesterolemic/hypercholesterolemic (HH) index (Table 1). The AI attained mean (0.24 ± 0.03 (O. maya from WCA) to 0.31 ± 0.03 (O. vulgaris from ECA)) and TI from 0.14 ± 0.01 (E. cirrhosa from NEA) to 0.23 ± 0.06 (O. maya from ECA) can be considered favorable for the consumption of all species due to the cardioprotective effect of their MUFA and PUFA concentrations. Concerning the obtained HH index (3.3 ± 0.2 for O. vulgaris from ECA and NEA to 4.0 ± 0.6 for O. maya from WCA) high values are desired from a nutritional standpoint24 since it estimates effects of specific fatty acids on cholesterol metabolism. E. cirrhosa from NEA and O. maya from WCA presented simultaneously the highest cholesterol amounts and the more protective HH indexes. Therefore, despite the elevated cholesterol amount in some species and origins, the octopus HH is protective from the nutritional point of view, balancing the potential health effects derived from cholesterol ingestion. These results constitute an added value for food consumption choices since these species are marketed at lower prices when compared with O. vulgaris. Still, to exceed the guideline target of less than 300 mg/day established by the American Heart Association,45 a portion of 20 to 25% of the whole collected specimens should be consumed corresponding to the entire individual for E. cirrhosa.

Figure 4. Cholesterol concentrations (□, mean; rectangles, mean ± standard deviation; bars above and below rectangles, range; mg/100 g wet weight) in the edible tissues of the characterized octopus species. Each letter (a−i) corresponds to a species and inherent origin (a, O. vulgaris from Northeast Atlantic Ocean (NEA); b, O. vulgaris from Northwest Atlantic Ocean (NWA); c, O. vulgaris from Eastern Central Atlantic Ocean (ECA); d, O. vulgaris from Western Central Atlantic Ocean (WCA); e, O. vulgaris from Pacific Ocean (PO); f, O. vulgaris from Mediterranean Sea (MS); g, O. maya from ECA; h, O. maya from WCA; i, E. cirrhosa from NEA). The same letters in a box plot indicate that the given means are not statistically different (p > 0.05).

mg/100 g ww for O. vulgaris from MS to 180 ± 11 mg/100 g ww for E. cirrhosa (Figure 4). This variability is highly interesting from the nutritional point of view indicating that one cannot classify all species and origins on the same basis regarding this parameter. Edible tissues of O. vulgaris from WCA (141 ± 11 mg/100 g ww) and from PO (162 ± 30 mg/ 100 g ww), O. maya from WCA (166 ± 17 mg/100 g ww), and E. cirrhosa from NEA exhibited significantly higher mean levels of cholesterol than the other species. Although some authors have concluded that cholesterol is not correlated with fat content (Oehlenschläger, 2006),38 as confirmed in the present study, these species have all superior SFA and ω-6 PUFA amounts. In humans, some studies indicate that SFA as C16:0 and myristic acid (C14:0) raise blood cholesterol by decreasing LDL receptors that are responsible for cholesterol regulation.4 O. maya from WCA and E. cirrhosa from NEA only exhibited similarity with O. vulgaris from PO (p = 0.76 and p = 0.16, respectively). The highest intravariability was observed for O. maya from ECA (65−164 mg/100 g ww), but the mean content (99 ± 39 mg/100 g ww) was not statistically different from those of O. vulgaris from NEA (109 ± 19 mg/100 g ww), from NWA (94 ± 4 mg/100 g ww), from ECA (87 ± 15 mg/ 100 g ww), and from MS (85 ± 14 mg/100 g ww). There is limited information about cholesterol levels in octopus species. Data was found for only E. cirrhosa14,25and O. vulgaris from NEA37,39 and from MS,9,26,40,41 ranging from 64 mg/100 g ww37 to 158 mg/100 g ww;40. Morillo-Velarde et al.41 reported lower values in the muscle of O. vulgaris caught in the MS (31.6−62.2 mg/100 g ww) which may be explained by the fact that the individuals were analyzed after artificial feeding or absence of it (induced starvation of 4 days). Octopus natural preys are bivalves and crustaceans like shrimp, crab, and lobster,3 all containing elevated cholesterol amounts. However, the food habits of octopuses are not completely known especially in the paralarva stage. According to Rosa et al.,10 8514



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for C18:1 (PC1 loading = 0.956), C16:0 (PC1 loading = 0.953), C22:6ω-3 (PC1 loading = 0.933), C22:5ω-3 (PC1 loading = 0.895), and C20:5ω-3 (PC1 loading = 0.843) than O. vulgaris samples. The second component factor (PC2), which justifies 29.9% of the total variance observed, was able to separate at least O. maya from E. cirrhosa, which may be explain by the higher C22:4ω-6 (PC2 loading = 0.937) and C20:4ω-6 (PC2 loading = 0.910) content of the former. PCA was also tested to infer the oceanic origin of octopus species. Four main clusters corresponding to NEA, WCA, NWA, and PO/ECA/ MS can be distinguished based on both components. NEA samples are characterized by lower C22:4ω-6 and C20:4ω-6 amounts than WCA samples. On the other hand, both of these oceans showed higher C18:1, C16:0, C22:6ω-3, C22:5ω-3, and C20:5ω-3 contents than all the remaining ones. The observed results match the statistical differences observed in the fatty acids composition. Despite the difficulty of defining a biochemical profile representative of a specific species and oceanic area based on a limited number of individuals, the attained differentiation may be useful for authenticity control. It can be particularly relevant for mislabeling detection since O. vulgaris is usually highly rated on the market when compared with O. maya and E. cirrhosa. Prato and Biandolino52 and Torrinha et al.46 also applied successfully chemometric discrimination to cluster several marine organisms based on the most important fatty acids.

The potential negative effects of dietary cholesterol are relatively small compared to those of SFA.4 The SFA levels in octopus species are considerably lower than those of meat products (about 40%). Both SFA and cholesterol are unavoidable in omnivorous diets, and attempts to reduce intake completely would require significant changes to dietary patterns and introduce undesirable effects, such as inadequate intakes of micronutrients and protein.4 The reached AI, TI, and HH compare favorably in terms of nutritional evaluation with those determined for other cephalopods, such as squids46 and common cuttlefish,47 as well as for other worldwide consumed marine species (hake, silver and black scabbardfish, ray, angler, blackbelly rosefish, and megrim).48,49 Although existing at low concentrations in the studied species, vitamin E protects unsaturated fatty acids from peroxidation, preventing the formation of free radicals and subsequent health disorders.35,50 The ingestion of a portion of 100 g of octopus will contribute to 2.0 (O. maya from ECA) to 10.7% (O. vulgaris from NWA) of the recommended dietary allowance (RDA) established for adult males and females (15 mg/day) by the Food and Nutrition Board of Institute of Medicine.51 Principal Components Analysis. PCA was applied as a pattern recognition technique to identify chemical descriptors for the selected species (Figure 5) or origins (Figure 1S,

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ASSOCIATED CONTENT

S Supporting Information *

Figure depicting principal components analysis of the octopus oceanic origins. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: sucasal@ff.up.pt. Phone: +351-2220428638. Fax: +351-226093390. *E-mail: [email protected]. Phone: +351-228340500. Fax: +351228321159. Funding

This work received financial support from the European Union (FEDER funds through COMPETE) and National Funds (FCT, Fundaçaõ para a Ciência e Tecnologia) through Projects PTDC/AGR-AAM/102316/2008 and Pest-C/EQB/LA0006/ 2013. The work also received financial support from the European Union (FEDER funds) under the framework of QREN through Project NORTE-07-0124-FEDER-000069.

Figure 5. Principal components analysis of the characterized octopus species (○, O. vulgaris; ●, O. maya; and △, E. cirrhosa) based on concentrations of selected individual fatty acids (C18:1, C16:0, C22:6ω-3, C22:5ω-3, C20:5ω-3, C22:4ω-6, and C20:4ω-6).

Notes

The authors declare no competing financial interest.

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Supporting Information). PCA allowed explaining 93.8% of total data variance by using two principal components based on seven individual fatty acids (C18:1, C16:0, C22:6ω-3, C22:5ω3, C20:5ω-3, C22:4ω-6, and C20:4ω-6). In Figure 5, three distinct octopus groups are represented corresponding to O. vulgaris, O. maya, and E. cirrhosa clusters. The first principal component factor (PC1), which comprises 63.9% of the total variance, is able to separate the three groups, being O. maya and E. cirrhosa, in general, located in the positive region, while O. vulgaris is positioned in the negative region. Still, some O. maya samples revealed greater similarities to those of O. vulgaris. All these may be justified by the fact that O. maya and E. cirrhosa samples, in general, reported higher figures

ACKNOWLEDGMENTS To all financing sources the authors are greatly indebted. ABBREVIATIONS USED AI, atherogenic index; ARA, arachidonic acid; CDA, canonical discriminant analysis; DHA, docosahexaenoic acid; ECA, East Center Atlantic; EPA, eicosapentanoic acid; HH, hypocholesterolemic/hypercholesterolemic; MCS, mean canonical score; MS, Mediterranean sea; MUFA, monounsaturated fatty acids; NEA, Northeast Atlantic; NWA, Northwest Atlantic; PO, Pacific Ocean; PUFA, polyunsaturated fatty acids; RDA, 8515



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Zuur, A. F. A review of cephalopod−environment interactions in European Seas. Hydrobiologia 2008, 612, 49−70. (18) Pecl, G. T.; Jackson, G. D. The potential impacts of climate change on inshore squid: biology, ecology and fisheries. Rev. Fish Biol. Fish. 2008, 18, 373−385. (19) United States Environmental Protection Agency (USEPA). Guidance for Assessing Chemical Contaminant Data for Use in Fish Advisories, Vol. 1, Fish Sampling and Analysis; EPA 823-B-00-007, 3rd ed.; Office of Science and Technology: Washington, DC, 2000. (20) European Commission. Regulation (EC) No 333/2007 of 28 March 2007 laying down the methods of sampling and analysis for the official control of the levels of lead, cadmium, mercury, inorganic tin, 3-MCPD and benzo(a)pyrene in foodstuffs. Off. J. Eur. Union 2007, L 88/29. (21) AOAC. Official Methods of Analysis of AOAC International, 18th ed.; AOAC International: Arlington, VA, 2007. (22) Ramalhosa, M. J.; Paíga, P.; Morais, S.; Alves, M. R.; DelerueMatos, C.; Oliveira, M. B. P. P. Lipid content of frozen fish: comparison of different extraction methods and variability during freezing storage. Food Chem. 2012, 131, 328−336. (23) Cruz, R.; Casal, S.; Mendes, E.; Costa, A.; Santos, C.; Morais, S. Validation of a single-extraction procedure for sequential analysis of vitamin E, cholesterol, fatty acids, and total fat in seafood. Food Anal. Methods 2013, 6, 1196−1204. (24) Guimarães, R. C. A.; Macedo, M. L. R.; Munhoz, C. L.; Filiu, W.; Viana, L. H.; Nozaki, V. T.; Hiane, P. A. Sesame and flaxseed oil: nutritional quality and effects on serum lipids and glucose in rats. Food Sci. Technol. (Campinas) 2013, 33, 209−217. (25) Rosa, R.; Pereira, J.; Nunes, M. L. Biochemical composition of cephalopods with different life strategies with special reference to a giant squid Architeuthis sp. Mar. Biol. 2005, 146, 739−751. (26) Valverde, J.; Hernández, M.; García-Garrido, S.; Rodríguez, C.; Estefanell, J.; Gairín, J.; Rodríguez, C.; Tomás, A.; García, B. Lipid classes from marine species and meals intended for cephalopod feeding. Aquacult. Int. 2012, 20, 71−89. (27) Turner, N.; Hulbert, A.; Else, P. Sodium pump molecular activity and membrane lipid composition in two disparate ectotherms, and comparison with endotherms. J. Comp. Physiol., B 2005, 175, 77− 85. (28) Prato, E.; Portacci, G.; Biandolino, F. Effect of diet on growth performance, feed efficiency and nutritional composition of Octopus vulgaris. Aquaculture 2010, 309, 203−211. (29) Ç elik, M.; Diler, A.; Kücu̧ ̈kgülmez, A. 2005. A comparison of the proximate compositions and fatty acid profiles of zander (Sander lucioperca) from two different regions and climatic conditions. Food Chem. 2005, 92, 637−641. (30) Kaya, Y.; Erdem, M. E. Seasonal comparison of wild and farmed brown trout (Salmo trutta forma fario L., 1758): crude lipid, gonadosomatic index and fatty acids. Int. J. Food Sci. Nutr. 2009, 60, 413−423. (31) Biandolino, F.; Portacci, G.; Prato, E. Influence of natural diet on growth and biochemical composition of Octopus vulgaris Cuvier, 1797. Aquacult. Int. 2010, 18, 1163−1175. (32) Miliou, H.; Fintikaki, M.; Tzitzinakis, M.; Kountouris, T.; Verriopoulos, G. Fatty acid composition of the common octopus, Octopus vulgaris, in relation to rearing temperature and body weight. Aquaculture 2006, 256, 311−322. (33) Navarro, J.; Villanueva, R. Lipid and fatty acid composition of early stages of cephalopods: an approach to their lipid requirements. Aquaculture 2000, 183, 161−177. (34) Harris, K.; Fleming, J.; Kris-Etherton, P. Challenges in estimating omega-3 fatty acid content of seafood from US nutrient databases: A salmon case study. J. Food Compos. Anal. 2011, 24, 1168− 1173. (35) Kulawik, P.; Ö zogul, F.; Glew, R.; Ö zogul, Y. Significance of antioxidants for seafood safety and human health. J. Agric. Food Chem. 2013, 61, 475−491. (36) Villanueva, R.; Escudero, J.; Deulofeu, R.; Bozzano, A.; Casoliva, C. Vitamin A and E content in early stages of cephalopods and their

recommended dietary allowance; SFA, saturated fatty acids; TI, thrombogenic index; WCA, West Center Atlantic

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REFERENCES

(1) FAO. 1961−2010 Fish and fishery products: world apparent consumption statistics based on food balance sheets; FAO Yearbook, Fishery and Aquaculture Statistics; Food and Agriculture Organization of the United Nations: Rome, 2013. (2) Lourenço, D.; Silva, L. J. G.; Lino, C. M.; Morais, S.; Pena, A. SPE-LC-FD Determination of polycyclic aromatic hydrocarbon monohydroxy derivatives in cephalopods. J. Agric. Food Chem. 2014, 62, 2685−2691. (3) FAO. FAO Species CatalogueVol. 3 Cephalopods of the World; FAO Fisheries Synopsis N. 125, Volume 3, 1984. (4) US Department of Agriculture and US Department of Health and Human Services. Report of the Dietary Guidelines Advisory Committee (DGAC) on the dietary guidelines for Americans, Part D. Section 3: Fatty Acids and cholesterol; Washington, DC, 2010; pp 210−258. Available at: http://www.cnpp.usda.gov/DGAs2010-DGACReport.htm. Accessed on September 20th 2013. (5) Estefanell, J.; Socorro, J.; Tuya, F.; Izquierdo, M.; Roo, J. Growth, protein retention and biochemical composition in Octopus vulgaris fed on different diets based on crustaceans and aquaculture by-products. Aquaculture 2011, 322−323, 91−98. (6) Estefanell, J.; Roo, J.; Guirao, R.; Afonso, J.; Fernández-Palacios, H.; Izquierdo, M.; Socorro, J. Efficient utilization of dietary lipids in Octopus vulgaris (Cuvier 1797) fed fresh and agglutinated moist diets based on aquaculture by-products and low price trash species. Aquacult. Res. 2013, 44, 93−105. (7) Ozogul, Y.; Duysak, O.; Ozogul, F.; Ö zkütük, A.; Türeli, C. Seasonal effects in the nutritional quality of the body structural tissue of cephalopods. Food Chem. 2008, 108, 847−852. (8) Passi, S.; Ctaudell, S.; Di Marco, P.; De Simone, F.; Rastrelli, L. Fatty Acid Composition and Antioxidant Levels in Muscle Tissue of Different Mediterranean Marine Species of Fish and Shellfish. J. Agric. Food Chem. 2002, 50, 7314−7322. (9) Karakoltsidis, P.; Zotos, A.; Constantinides, S. Composition of the commercially important Mediterranean finfish, Crustaceans and molluscs. J. Food Compos. Anal. 1995, 8, 258−273. (10) Rosa, R.; Costa, P.; Nunes, M. Effect of sexual maturation on the tissue biochemical composition of Octopus vulgaris and O. def ilippi (Mollusca: Cephalopoda). Mar. Biol. 2004, 145, 563−574. (11) Rosa, R.; Nunes, L.; Reis, C. Seasonal changes in the biochemical composition of Octopus vulgaris Cuvier, 1797, from three areas of the Portuguese coast. Bull. Mar. Sci. 2002, 71, 739−751. (12) Sieiro, M.; Aubourg, S.; Rocha, F. Seasonal study of the lipid composition in different tissues of the common octopus (Octopus vulgaris). Eur. J. Lipid Sci. Technol. 2006, 108, 479−487. (13) Vaz-Pires, P.; Barbosa, A. Sensory, microbiological, physical and nutritional properties of iced whole common octopus (Octopus vulgaris). Lebensm.-Wiss. Technol. 2004, 37, 105−114. (14) Rosa, R.; Costa, P.; Pereira, J.; Nunes, M. Biochemical dynamics of spermatogenesis and oogenesis in Eledone cirrhosa and Eledone moschata (Cephalopoda: Octopoda). Comp. Biochem. Physiol., Part B 2004, 139, 299−310. (15) Noyola, J.; Mascaró, M.; Caamal-Monsreal, C.; Noreña-Barroso, E.; Díaz, F.; Re, D.; Sánchez, A.; Rosas, C. Effect of temperature on energetic balance and fatty acid composition of early juveniles of Octopus maya. J. Exp. Mar. Biol. Ecol. 2013, 445, 156−165. (16) Morais, S.; Gomes, F.; Ramalhosa, M. J.; Delerue-Matos, C.; Oliveira, M. B. P. P. Occurrence of Polycyclic Aromatic Hydrocarbons in Cephalopods. In Handbook of Polycyclic Aromatic Hydrocarbons: Chemistry, Occurrence and Health Issues; Bandeira, G. C., Meneses, H. E., Eds.; Nova Science Publishers, Inc.: New York, 2013; pp 197−216. (17) Pierce, G. J.; Valavanis, V. D.; Guerra, A.; Jereb, P.; Orsi-Relini, L.; Bellido, J. M.; Katara, I.; Piatkowski, U.; Pereira, J.; Balguerias, E.; Sobrino, I.; Lefkaditou, E.; Wang, J.; Santurtun, M.; Boyle, P. R.; Hastie, L. C.; Macleod, C. D.; Smith, J. M.; Viana, M.; González, A. F.; 8516



Article

dietary effects in Octopus vulgaris paralarvae. Aquaculture 2009, 286, 277−282. (37) Nunes, M.; Bandarra, N.; Oliveira, L.; Batista, I.; Calhau, M. Composition and nutritional value of fishery products consumed in Portugal. In Seafood research from fish to dish: quality, safety and processing of wild and farmed fish; Luten, J. B., Jacobsen, C., Bekaert, K., Saebo, A., Oehlenschläger, J., Eds.; Wageningen Academic Publishers: Netherlands, 2006; pp 477−487. (38) Dias, G.; Sánchez, V.; Bártolo, H.; Oliveira, L. Vitamin content of fish and fish products consumed in Portugal. Electron. J. Environ., Agric. Food Chem. 2003, 2, 510−513. (39) Oehlenschläger, J. Cholesterol content in food, data from the last decade: a review. In Seafood research from fish to dish: quality, safety and processing of wild and farmed fish; Luten, J. B., Jacobsen, C., Bekaert, K., Saebo, A., Oehlenschläger, J., Eds.; Wageningen Academic Publishers: The Netherlands, 2006; pp 41−57. (40) García-Garrido, S.; Hachero-Cruzado, I.; Garrido, D.; Rosas, C.; Domingues, P. Lipid composition of the mantle and digestive gland of Octopus vulgaris juveniles (Cuvier, 1797) exposed to prolonged starvation. Aquacult. Int. 2010, 18, 1223−1241. (41) Morillo-Velarde, P. S.; Valverde, J. C.; Llinares, R. M. S.; García, B. G. Changes in lipid composition of different tissues of common octopus (Octopus vulgaris) during short-term starvation. Aquacult. Res. 2013, 44, 1177−1189. (42) EFSA. EFSA panel on dietetic products, nutrition, and allergies (NDA); Scientific opinion on dietary reference values for fats, including saturated fatty acids, polyunsaturated fatty acids, monounsaturated fatty acids, trans fatty acids, and cholesterol. EFSA J. 2010, 8, 1461. (43) Wijendran, V.; Hayes, K. C. Dietary n-6 and n-3 fatty acid balance and cardiovascular health. Annu. Rev. Nutr. 2004, 24, 597−615. (44) Department of Health. Nutritional aspects of cardiovascular disease: report on Health and social subjects; HMSO: London, 1994. (45) Lichtenstein, A. H.; Appel, L. J.; Brands, M.; Carnethon, M.; Daniels, S.; Franch, H. A.; Franklin, B.; Kris-Etherton, P. M.; Harris, W. S.; Howard, B.; Karanja, N.; Lefevre, M.; Rudel, L.; Sacks, F.; Horn, L. V.; Winston, M.; Wylie-Rosett, J. Diet and lifestyle recommendations revision 2006. A scientific statement from the American Heart Association nutrition committee. Circulation 2006, 114, 82−96. (46) Torrinha, A.; Gomes, F.; Oliveira, M.; Cruz, R.; Mendes, E.; Delerue-Matos, C.; Casal, S.; Morais, S. Commercial squids: Characterization, assessment of potential health benefits/risks and discrimination based on mineral, lipid and vitamin E concentrations. Food Chem. Toxicol. 2014, 67, 44−56. (47) Ayas, D.; Ozogul, Y.; Ozogul, I.; Uçar, Y. The effects of season and sex on fat, fatty acids and protein contents of Sepia officinalis in the northeastern Mediterranean Sea. Int. J. Food Sci. Nutr. 2012, 63, 440−445. (48) Afonso, C.; Lourenço, H. M.; Cardoso, C.; Bandarra, N. M.; Carvalho, M. L.; Castro, M.; Nunes, M. L. From fish chemical characterization to the benefit-risk assessement − Part A. Food Chem. 2013, 137, 99−107. (49) Afonso, C.; Cardoso, C.; Lourenço, H. M.; Anacleto, P.; Bandarra, N. M.; Carvalho, M. L.; Castro, M.; Nunes, M. L. Evaluation of hazards and benefits associated with the consumption of six fish species from the Portuguese coast. J. Food Compos. Anal. 2013, 32, 59−67. (50) Maestre, R.; Pazos, M.; Medina, I. Role of the raw composition of pelagic fish muscle on the development of lipid oxidation and rancidity during storage. J. Agric. Food Chem. 2011, 59, 6284−6291. (51) FNIC. Dietary Reference Intakes (DRIs): Recommended Dietary Allowances and Adequate Intakes, Vitamins; Food and Nutrition Board; Institute of Medicine, National Academy of Sciences: Washington, DC, 2010. (52) Prato, E.; Biandolino, F. Total lipid content and fatty acid composition of commercially important fish species from the Mediterranean, Mar Grande Sea. Food Chem. 2012, 131, 1233−1239.

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Octopus Lipid and Vitamin E Composition - American Chemical Society

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