Nutritional Composition of Cultured Sturgeon (Acipenserspp.)

JOURNAL OF FOOD COMPOSITION AND ANALYSIS ARTICLE NO.

9, 171–190 (1996)

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Nutritional Composition of Cultured Sturgeon (Acipenser spp.)1 A. BADIANI,*,2 P. ANFOSSI,† L. FIORENTINI,‡ P. P. GATTA,* M. MANFREDINI,* N. NANNI,* S. STIPA,* AND B. TOLOMELLI§ *Istituto di Approvvigionamenti Annonari, University of Bologna, Bologna, Italy; †Istituto di Farmacologia, Farmacocinetica e Tossicologia, University of Bologna, Bologna, Italy; ‡Istituto di Scienze degli Alimenti e della Nutrizione, University of Piacenza, Piacenza, Italy; and §Dipartimento di Biochimica ‘‘Giovanni Moruzzi,’’ University of Bologna, Bologna, Italy Received August 29, 1995, and in revised form January 11, 1996 Proximate composition and cholesterol content, fatty acid and amino acid profiles, selected mineral (Na, K, Mg, Ca, P, Fe, Zn) and vitamin (niacin, pantothenic acid, pyridoxine, vitamin B12) content, total and soluble collagen content, and purine bases (adenine, guanine, xanthine, hypoxanthine) were determined in cultured sturgeon. White sturgeon (Acipenser transmontanus), Italian sturgeon (Acipenser naccarii) and Siberian sturgeon (Acipenser baeri) were individually analyzed. The results were reported as a whole, since no commercial distinction is made between the three species. Mean content (per 100 g wet weight) of protein, lipid, ash, and cholesterol was 19.23 g, 7.63 g, 1.09 g, and 66 mg, respectively. Saturated, monounsaturated, and polyunsaturated (PUFA) fatty acid contents were 1.76, 3.12, and 1.46 g/100 g wet weight, respectively; n 0 3 PUFAs reached 1.18 g/100 g, whereas n 0 6 PUFAs were 0.28 g/100 g. The n 0 3/n 0 6 ratio was 4.23. Compared to human requirements, sturgeon protein was especially rich in histidine and isoleucine (0.82 and 0.92 g/100 g wet weight, respectively) but rather poor in tryptophan (0.14 g). The Mg concentration was fairly good (46.8 mg/100 g), providing more than 15% RDA. Vitamin B12 (1.27 mg/100 g), niacin (5.62 mg/100 g), and pyridoxine (0.44 mg/100 g) were able to meet 127, 31, and 22% RDA, respectively. Total collagen was 1.22 g/100 g wet weight, 68% of which was soluble. Xanthine was never detected. Adenine, guanine, and hypoxanthine mean levels were 15.47, 9.94, and 92.71 mg/100 g wet weight, respectively. q 1996 Academic Press, Inc.

INTRODUCTION

Seafood consumption patterns in Italy have changed dramatically over the last decade. Per capita consumption of both finfish and shellfish has increased from 12 kg (26.4 pounds) in 1985 to the unprecedented level of 22 kg (48.5 pounds) in 1993 (CIPE, 1994). Concern relating to health and nutrition has been cited as one of the primary reasons why consumers are attracted to seafoods. The potential health benefits offered by the long-term consumption of omega-3 highly unsaturated fatty acids found in marine lipids have been extensively studied, as recently reviewed by Pigott and Tucker (1990) and Nettleton (1995). Fish also has a relatively high content of high biological value proteins which are easily digested. Moreover, the amount of water-soluble vitamins in seafood muscle tissue compared to other food groups and the greater range of minerals fish contain are an undeniable asset when pursuing a healthier diet (Brown, 1

Reference to trade names, proprietary products, or specific equipment does not imply endorsement. To whom reprint requests should be addressed at Istituto di Approvvigionamenti Annonari, Facolta` di Medicina Veterinaria, Via Tolara di Sopra, 50, 40064 Ozzano Emilia (BO), Italy. Fax: Italy/51/792842. 2

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1986; Kinsella, 1988; Pigott and Tucker, 1990; Holland et al., 1993). Nor are these benefits confined to marine finfish or shellfish alone; freshwater fish has desirable nutritive value as well, although in general with a somewhat less favorable fatty acid ˚ gren et al., 1987; Hearn et al., 1987a; Henderson and Tocher, 1987; A ˚ gren profile (A et al., 1988; Vlieg and Body, 1988; Vlieg et al., 1988; Pigott and Tucker, 1990; Wang et al., 1990; Steiner-Asiedu et al., 1991a,b; Vlieg et al., 1991; Sinclair et al., 1992; Tidwell et al., 1993; Hyvo¨nen and Koivistoinen, 1994). In the fatty acid profile, estuarine or brackish water fish lie somewhere between marine and freshwater fish (Nair and Gopakumar, 1978; Henderson and Tocher, 1987). Anadromous species (salmon, sturgeon, and trout are among them) seem to deserve special interest as they are a valuable source of n 0 3 highly unsaturated fatty acids in human nutrition (Stansby, 1976; Ackman, 1989). The potential interest of these species increases even more if they are reared in captivity, and hence are likely to have a higher fat content, as long as substantial amounts of fish oil and/or fish scrap ˚ gren et al., 1987; Ackman are provided as part of their diet (Suzuki et al., 1986; A and McLeod, 1988; Pigott and Tucker, 1990; Polvi and Ackman, 1992). The significant progress and development of aquaculture in Italy, both as intensive rearing system in land-locked bodies of water, and as intensive or extensive farming of euryhaline species, is another explanation which accounts for the ever increasing national consumption of finfish and shellfish. Salmonid production, totalling 40,000 metric tons in 1992, constitutes the overwhelming bulk of the finfish farmed in Italy (ANON, 1993). Special attention has been paid to sturgeon rearing as well, such that Italy currently dominates the European market (EU) as the most important producer (Bronzi et al., 1994). Once much sought-after for caviar production, sturgeon has rapidly become appreciated for the quality of its flesh, though, to the best of our knowledge, scanty information exists about its nutritional aspects. The objective of this research was to determine the nutritional composition of sturgeon flesh. Given that Italian fish markets do not differentiate sturgeon on the grounds of species, it was deemed appropriate to examine together the three main species reared in Italy (Bronzi et al., 1994): white sturgeon (Acipenser transmontanus), Italian sturgeon (Acipenser naccarii), and Siberian sturgeon (Acipenser baeri). MATERIALS AND METHODS

Sampling Procedure Raceway-reared sturgeon (10 A. transmontanus, 10 A. naccarii, 10 A. baeri) were obtained from an intensive commercial fish farm based in Northern Italy over a period of 3 months, from April to June 1993. Samples were selected from fish weighing 3.35–5.70 kg, the dominant size in the market place. Age of the fish ranged from 42 to 54 months. Environmental conditions and feeding regimen were guaranteed as uniform among the three outdoor raceways (one for each species) throughout the rearing period; until sampled, the fish were fed a commercial pelleted diet for sturgeon, containing fish meals and fish oil. Freshly caught sturgeon were received on ice as whole, noneviscerated fish. After beheading and gutting, three cross-sectional slices were cut from each fish according to the AOAC method No. 937.07 (AOAC, 1990), modified in that much thicker slices (6 cm each) were taken to counteract any possible nonuniform distribution of carcass fat. Skin, bony scutes, subepithelial fat layers, dark muscle, and cartilage were removed from each thick steak, to obtain white flesh only, which was intended as the edible

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portion. This was finely diced (about 0.13 cm3), thoroughly mixed, and homogenized in three 5-s bursts with a Moulinette S food processor (Moulinex S.p.A., Milano, Italy) set at 10,000 rpm. The homogeneous sample mass prepared from each fish was divided into three parts, which were stored under different conditions depending on the analyses to be performed: one was retained to immediately determine moisture, protein, ash, lipid, fatty acid composition, cholesterol, and macro- and microminerals (phosphorus excepted). A second part of the homogenized sample was frozen at 0207C for subsequent analyses: phosphorus and vitamins. The third aliquot was lyophilyzed and defatted to determine amino acid composition, total and soluble collagen, and purine content. Each of the 30 sturgeon was individually analyzed for proximate composition, cholesterol content, and fatty acid content. Nine fish, evenly distributed among the three species, were randomly selected from the total group for the remaining analytical determinations, which were performed individually, as for the foregoing. Proximate Composition, Cholesterol Content, and Energy Value Samples were analyzed for moisture, total ash, and nitrogen using AOAC (1990) methods No. 950.46B, 920.153, and 981.10, respectively. Total protein was calculated from Kjeldahl nitrogen using a 6.25 conversion factor. Oil was extracted from 10 g of each homogenized sample following the method of Folch et al. (1957), as modified by Michaelsen et al. (1991), using chloroform/methanol (2:1, v/v) for extraction. Total lipids were measured gravimetrically on an aliquot of this extract. A second aliquot of the fat extract was transferred to a screw cap test tube, stored in a refrigerator (/47C) and used within 24 h for fatty acid analysis. Cholesterol content was determined by direct saponification (Adams et al., 1986), without derivatization, in accordance with Engeseth and Gray (1989). A known amount of 5-a-cholestane (Sigma Chemical Company Ltd, St. Louis, MO, U.S.A.) was added during extraction as an internal standard. Analysis of the cholesterol was performed on a Carlo Erba Fractovap 2350 gas chromatograph (Carlo Erba Instruments, Milano, Italy) designed to accomodate a 1.83 m 1 4 mm i.d. glass column packed with 3% OV-17 on Gas Chrom Q (100–120 mesh) (Alltech Associated, Inc., Deerfield, IL, U.S.A.). Nitrogen served as the carrier gas at a flow rate of 20 ml/min. Temperatures of the injector, oven, and detector were 300, 262, and 3007C, respectively. The injected volume was 4 ml and the run time was 40 min. The output signal from the detector was amplified at an electrometer sensitivity of 101. A DP 700 computing integrator (Carlo Erba Instruments) was used to calculate retention times and peak areas. Cholesterol was identified by comparing retention time to that of an authenticated standard (Sigma Chemical Company Ltd). Energy values were derived by multiplying the amounts of protein and fat by the factors 4 and 9 (kcal value) and 17 and 37 (kJ value), respectively (EEC, 1990). Fatty Acid Composition Lipid extracted from each sample was used for fatty acid determination. The lipid sample (50–60 mg, accurately weighed) was dissolved in toluene (1 ml). Free fatty acids were obtained and esterified using methanolic sulfuric acid (1%), according to the procedure described by Christie (1989). The recovered fatty acid methyl esters (FAME) were added with 10 mg methyltricosanoate (C23:0) as an internal standard and analyzed on a fused silica capillary column

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(Omegawax 320, 30 m 1 0.32 mm i.d., 0.25-mm coating thickness; Supelco, Inc., Bellefonte, PA, U.S.A.) in a Fisons Instruments HRGC 8560 Series Mega 2 gas chromatograph (Fisons Instruments, Milano, Italy) equipped with a flame ionization detector (FID) and operated with a split ratio of 100:1. High-purity helium served as the carrier gas at a flow rate of 105 kPa. High-purity hydrogen (50 kPa) and chromatographic air (100 kPa) were supplied to the FID. The injector and detector temperatures were 250 and 2607C, respectively. The column oven was programmed from 1807C (2-min hold) to 2007C at 57C/min; 10 min hold at 2007C was followed by a linear 107C/min increase to 2107C (10 min hold). The injected sample was 1 ml and the run time was 27 min. The output signal from the detector was amplified at an electrometer sensitivity of 101. Retention times and peak areas were automatically computed by a DP 700 computing integrator (Carlo Erba Instruments). Methyl esters were identified and quantified by comparing the retention time and peak area of the unknowns with those of known FAME standard mixtures (Supelco, Inc.; Alltech Associated). All fatty acid values were reported by two methods: (a) milligrams fatty acid per 100 g edible portion; (b) percentage of individual FAME based on total FAME present in injected sample. Besides some nutritional attributes based on the fatty acid composition (Pigott and Tucker, 1990), two indices were computed, which take the different atherogenic and/or thrombogenic potential of some fatty acids into account (Ulbricht and Southgate, 1991). Amino Acid Composition Three separate hydrolyses were performed in order to determine the amino acid composition of sturgeon flesh. Samples were hydrolyzed for 23 h at 1107C with 6 N HCl to obtain hydrolysates suitable for analysis of all amino acids except cystine / cysteine, methionine and tryptophan (Spackman et al., 1958). Samples oxidized with performic acid were hydrolyzed for 18 h at 1107C with 6 N HCl to obtain hydrolysates suitable for the determination of cystine / cysteine as cysteic acid and of methionine as methionine sulphone, by the method of Moore (1963). Tryptophan was determined by an alkaline hydrolysis method, using Ba(OH)2 at 1107C for 22 h (Eggum, 1968). The various amino acids from each hydrolysate were determined using a Carlo Erba 3A30 Amino-analyzer (Carlo Erba Instruments), equipped with an automatic sampler, and compared with standard amino acids (Sigma Chemical Company Ltd.; Serva Feinbiochimica GmbH, Heidelberg, Germany) analyzed under identical conditions. Amino acid content was expressed both as grams per 100 g edible portion and as grams per 16 g total nitrogen (i.e., grams per 100 g protein). A chemical score was computed for each essential amino acid based on whole egg protein amino acid composition as reported by Sheffner (1967). The lowest value was retained as the chemical score of sturgeon protein. The digestibility calculated–protein efficiency ratio was estimated from the essential amino acid composition of the samples using the equations provided by Satterlee et al. (1982). Finally, the lysine/arginine ratio was calculated, because, as suggested by Kritchevsky et al. (1982), it could be directly related to the specific protein atherogenicity. Mineral Content Ashed samples were dissolved in 3 N HCl and diluted to an appropriate concentration for mineral analysis according to the AOAC method No. 968.08 (AOAC, 1990).

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Four macroelements (Na, K, Mg, and Ca) and two microelements (Fe and Zn) were determined using a Pye Unicam SP9 atomic absorption spectrophotometer (Unicam Ltd., Cambridge, UK) equipped with hollow cathode lamps specific for each element and an air–acetylene flame. The instrument settings and other experimental conditions were in accordance with the manufacturer’s specifications. The wavelenghts (nm) used for each mineral were: Na, 589.0; K, 766.5; Mg, 285.2; Ca, 422.7; Fe, 248.3; Zn, 213.9. Concentrations were determined from calibration curves obtained with standard solutions of NaCl, KCl, MgCl2 r6H2O, CaCl2r6H2O, FeCl3r6H2O, and ZnCl2 (Carlo Erba Instruments). Samples diluted for calcium analysis contained 0.5% (w/v) lanthanum to overcome potential anionic interferences. Phosphorus was assayed colorimetrically on wet digested samples according to the AOAC procedure No. 972.22 (AOAC, 1990), using a Perkin–Elmer Lambda 1 UV/ VIS spectrometer (Perkin–Elmer Italia S.p.A., Monza, Italy). A calibration curve obtained with standard solutions of KH2PO4 (Merck, Darmstadt, Germany) was used to assess phosphorus concentration. Vitamin Content In planning the present research, a choice was made to determine only those watersoluble vitamins most likely to be present in ‘‘significant’’ quantities, where significant means ‘‘able to provide at least 15% of the Recommended Daily Amount (RDA) set by the European Union Council’’ (EEC, 1990). These vitamins, selected on the grounds of the data reported by Souci et al. (1989) for numerous species of finfish, were niacin, pantothenic acid, pyridoxine, and vitamin B12 . An attempt was made, however, to determine thiamin and riboflavin as well on three fish (one for each species) randomly selected out of the subsample (n Å 9) used for the assessment of vitamin content. Niacin, pantothenic acid, pyridoxine, vitamin B12 , and riboflavin were determined by microbiological assay techniques. In niacin assay, Lactobacillus plantarum (ATCC 8014) was the test microorganism (Eitenmiller and De Souza, 1985). The vitamin extraction was performed in 0.1 N HCl at 20 pounds pressure for 30 min. Pantothenic acid was determined according to the method reported by Wyse et al. (1985); the vitamin content was expressed as calcium pantothenate. Pyridoxine was assayed using Saccharomyces uvarum (ATCC 8040) as the test microorganism. In this case samples were extracted in 0.055 N HCl at 20 pounds pressure for 5 h (Toepfer and Polansky, 1970). Vitamin B12 was determined using Lactobacillus leichmanii (ATCC 7830) as the test microorganism. Samples were extracted in a solution containing 1.2 g citric acid, 1.3 g Na2HPO4 , and 1 g Na2S2O5 in 100 ml water by autoclaving at 20 pounds pressure for 30 min (Method No. 952.20; AOAC, 1990). Thiamin was assayed by the thiochrome procedure (Ellefson, 1985). Riboflavin was determined using Lactobacillus casei (ATCC 7469) as the test microorganism (Shah, 1985). Calibration curves were obtained using U.S.P. reference standards (The United States Pharmacopea, Inc., Rockville, MD, U.S.A.). Total and Soluble Collagen Content Three 1-g samples of freeze-dried powdered muscle for each fish were heated for 70 min at 777C in a Ringer’s solution and separated into supernatant and residue

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fractions following the procedure of Hill (1966). Each fraction was individually hydrolyzed in 6 N HCl for 22 h at 1107C. The hydroxyproline content both in the supernatant and in the residue was determined as outlined by Woessner (1961). Hydroxyproline content in the foregoing fractions was converted, respectively, to soluble and insoluble collagen using 15 as a conversion factor, a value derived by the work of Sato et al. (1989). Percentage soluble collagen was calculated by dividing the total solubilized collagen (supernatant) by the sum of total insoluble collagen (residue) and total solubilized collagen, times 100. Total collagen was expressed as g/100 g edible portion, soluble collagen as a percentage of total collagen. Purine Content The individual nitrogen bases (adenine, guanine, xanthine, hypoxanthine), instead of total purine content, were determined, because they produce different uricogenic effects in humans, the most active reportedly being adenine and hypoxanthine (Sarwar and Brule´, 1991; Brule´ et al., 1992). Samples were hydrolyzed, following the procedure described by Brule´ et al. (1988), for the quantitative liberation of the purine bases from nucleic acids. The bases were separated by isocratic elution using a reverse-phase column in a Beckman HPLC System (Beckman, San Ramon, CA, U.S.A.). The HPLC system was composed of a HPLC pump Model 126, an autosampler Model 507 fitted with a 50 ml loop (Beckman), a Supelcosil LC18DB analytical column (5 ml, 250 1 4.6 mm i.d.; Supelco, Inc.) with a Supelguard LC18DB guard column (5 ml, 20 1 4.6 mm i.d.; Supelco), a UV detector Model 166 set at 254 nm (Beckman). The HPLC mobile phase was a 0.025 M potassium phosphate buffer mixed with acetonitrile, at a flow rate of 1.0 ml/min. The best separation of the bases was attained by adjusting the pH of the buffer and the ratio (v/v) buffer:acetonitrile as follows: (a) pH 3.6, ratio Å 99:1 for guanine and hypoxanthine; (b) pH 4.0, ratio Å 99:1 for xanthine; (c) pH 5.5, ratio Å 97:3 for adenine. The amount of the injected sample was 20 ml. Standard solutions of known concentration of individual purine bases (Sigma Chemical Company Ltd.) were carried through the entire procedure to permit calculation of the percentage recoveries. Mean recovery rates were 108, 90, 89, and 100% for adenine, guanine, xanthine, and hypoxanthine, respectively. These percentages were then used to correct assay values for procedural losses. Chromatoghaphic data were stored on a PS2/50 IBM personal computer (IBM Inc., Porthsmouth, UK) and elaborated by the Beckman System Gold program (release 4.0). Summary statistics (mean and standard error of the mean) were computed for each variable. RESULTS AND DISCUSSION

Proximate Composition, Cholesterol Content, and Energy Value Table 1 reports the proximate composition, cholesterol content, and energy value of a 100-g edible portion of sturgeon. On the arbitrary scale proposed by Stansby (1976), sturgeon rated as a medium oil–high protein fish. The protein contribution to total energy value (usually abbreviated to Pcal%) was slightly less than 53%. As part of a mixed diet, 100 g sturgeon flesh would provide

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TABLE 1 PROXIMATE COMPOSITION, CHOLESTEROL CONTENT, AND ENERGY VALUE a OF EDIBLE PORTION OF CULTURED STURGEON (per 100 g)

a b

Means calculated from the data for 30 fish individually analyzed in duplicate. Calculated according to EEC (1990).

more than 38% of the protein required to meet the US Recommended Daily Amounts (RDA) for adults of both sexes (Bodwell and Anderson, 1986). As mentioned earlier, sturgeon is a medium fat fish (fat content ranging from 5 to 15%). In fact, 23.3% of the fish assayed were below this range, while only 3.33% were above, thus showing a certain amount of variability that obviously affected the moisture content (moisture and lipid provided about 80% edible portion, as is usual in fish) and energy value as well. Lipids gave a noticeable contribution to the calorie count of 100 g of sturgeon flesh, which actually reached the mean value of 47% (from 22.8 to 66.2%) of the total. A more balanced view of this nutritional aspect might be gained by considering that, with 7.63% fat content, a 100-g serving of sturgeon would provide 11.3% of the daily fat intake of 67 g, currently recommended for an adult on a normal 2000 kcal diet with no more than 30% energy from fat. While it is unlikely that sturgeon would be the first choice for a consumer aiming at reducing fat intake, nevertheless significant consumption of n03 highly unsaturated fatty acids requires that fish with a medium to high fat content must be selected. As expected, ash content was well within the range covered by most marine and freshwater fish (Souci et al., 1989), which was in any case indicative of a careful preparation of the samples. Cholesterol content was fairly modest (66 mg/100 g flesh, as an average). Even referring to the strict level suggested by Kinsella (1988), that is 100 mg of maximum daily intake/1000 kcal, a 100-g serving of sturgeon would cover just a third of the allowable amount in a normal 2000-kcal diet. Little information is available regarding the proximate composition of sturgeon flesh; what little there is quite often is derived from a small number of fish, in some cases as low as one (Sidwell et al., 1974; Moro, 1989; Price et al., 1989; Souci et al., 1989; Bianchi Paleari and Grimaldi, 1994). Few additional data were found for sturgeon fat content only (Hepburn et al., 1986; Ackman and McLeod, 1988; Naruse et al., 1989; Renon et al., 1991), and a single source was available for cholesterol content (Naruse et al., 1989).

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In general, a good level of agreement was found among the present results and literature figures for protein and ash content. A wide difference was found in the mean fat content (and consequently moisture and energy value), which ranged from a minimum of 0.96% (Moro, 1989) to the maximum of 7.63% here reported, thus again bringing to light the fat content variability in fish and its possible causes, emphasized by Stansby (1986) and recently reviewed by Pigott and Tucker (1990). Only Ackman and McLeod (1988) and Price et al. (1989) reported figures close to the present one, 7.20 and 7.40% respectively, the former as the mean value of two specimens, the latter as a peak value in a group of 10- to 13-month-old sturgeon. The single available value for cholesterol, published by Naruse et al. (1989), was almost 3.5 times higher than that reported in Table 1. Fatty Acid Composition The fatty acid profile of cultured sturgeon flesh is listed in Tables 2a and 2b. The class of monounsaturated fatty acids (MUFAs) clearly dominated, followed by saturated fatty acids (SFAs), closely followed by polyunsaturated fatty acids (PUFAs). In decreasing order, the main fatty acids were oleic (C18:1), palmitic (C16:0), docosahexaenoic (C22:6 n 0 3, DHA), palmitoleic (C16:1), and eicosapentaenoic (C20:5 n 0 3, EPA). Considering the isomers n 0 9 and n 0 7 together, C18:1 totalled 62.4% of MUFAs; in the same fatty acid class, C16:1 accounted for 16.4% of the total. SFAs were dominated by C16:0, with 77.2% of the total. DHA and EPA (usually referred to as n 0 3 highly unsaturated fatty acids) were the most important PUFAs, with 41.2 and 24.8%, respectively. These two accounted for 82% of the n 0 3 PUFAs; in this group a-linolenic acid (C18:3 n 0 3) reached a relatively modest level (3.9%). Linoleic acid (C18:2 n 0 6), which was about 14% of total PUFAs, was clearly dominant within the ‘‘n 0 6 group’’ (73.2%), of which 16.8% was provided by arachidonic acid (C20:4 n 0 6). Any information on the fatty acid make-up of sturgeon flesh which could be sensibly used as the basis for comparison is rather meager, expressed either gravimetrically (Hepburn et al., 1986; Ackman and McLeod, 1988), or as percentage total FAME (Naruse et al., 1989; Renon et al., 1991; Bianchi Paleari and Grimaldi, 1994). Ackman and McLeod (1988) found a much higher quantity of EPA (1400 mg/100 g) and slightly lower DHA (570 mg/100 g) in Atlantic sturgeon with 7.20% fat, while the amounts for these fatty acids reported by Hepburn et al. (1986) were 1000 and 500 mg/100 g, respectively, again in Atlantic sturgeon (6% fat). In both cases EPA far outnumbered DHA within the context of a general preponderance of PUFAs over other fatty acid classes. On the other hand, Renon et al. (1991), Bianchi Paleari and Grimaldi (1994), and Naruse et al. (1989) found MUFAs to predominate over SFAs and PUFAs. For all three studies, in accordance with our findings, C18:1 was the major fatty acid (from 26.4 to 34.3%) followed by C16:0 (from 13.9 to 19.8%). As regards linoleic acid, arachidonic acid, a-linolenie acid, EPA, and DHA, our findings were closer to those of Renon et al. (1991): 1.74, 1.10, 0.62, 4.41, and 8.43%, respectively, than to those of Bianchi Paleari and Grimaldi (1994): 4.40, 2.40, 5.40, 7.00, and 2.10% respectively. The same was true for n 0 3/n 0 6, which was 3.62 for Renon et al. (1991) and 2.76 for Bianchi Paleari and Grimaldi (1994). It should be noted that the latter set of data derived from a small group of cultured white sturgeon, whereas nothing is known about the origin of the fish analyzed by

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NUTRITIONAL COMPOSITION OF CULTURED STURGEON TABLE 2a FATTY ACID PROFILE

EDIBLE PORTION OF CULTURED STURGEON (% TOTAL FAME)a,b

OF

a

Means calculated from the data for 30 fish individually analyzed in duplicate. FAME, fatty acid methyl esters; LA, linoleic acid; ALA, a-linolenic acid; AA, arachidonic acid; EPA, eicosapentaenoic acid; DHA, docosahexaenoic acid; SFA, saturated fatty acid; MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty acid. b

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BADIANI ET AL. TABLE 2b FATTY ACID PROFILE

OF

EDIBLE PORTION

OF

CULTURED STURGEON (mg/100 g)a,b

a

Means calculated from the data for 30 fish individually analyzed in duplicate. LA, linoleic acid; ALA, a-linolenic acid; AA, arachidonic acid; EPA, eicosapentaenoic acid; DHA, docosahexaenoic acid; SFA, saturated fatty acid; MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty acid. b

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Renon et al. (1991) and Naruse et al. (1989). On the other hand, Ackman and McLeod (1988) derived their data from wild sturgeon, which was probably true for those reported by Hepburn et al. (1986) as well. On the whole, the observations made by van Vliet and Katan (1990) on wild and cultured fish (about the former having more n 0 3 highly unsaturated fatty acids than the latter) were confirmed. Many of the findings of this research regarding the fatty acid composition of sturgeon flesh were in agreement with those of Henderson and Tocher (1987) in freshwater fish. However, a number of differences do emerge, such as the rather high value for docosenoic acid (C22:1), very likely of dietary origin (Ackman et al., 1980), the low quantity of trienes (in particular a-linolenie acid) and tetraenes (especially arachidonic acid), the high value of the n 0 3/n 0 6 ratio when compared to the range given as characteristic of freshwater fish (0.5–3.8). The high level of DHA compared to EPA, a finding invariably observed by Polvi and Ackman (1992) in several groups of cultured Atlantic salmon fed widely different diets, is also worthy of note. In fact a number of authors (Kinsella, 1986; Ackman and McLeod, 1988; Armstrong et al., 1991; Sinclair and O’Dea, 1993) maintain that, once ingested, DHA has effects that are different, and perhaps even more beneficial, than those of EPA. Overall such differences would seem to emphasize the nutritional value of sturgeon flesh (Pigott and Tucker, 1990; Nettleton, 1995). A comparison between the values listed in Table 2a and those published on the fatty acid make-up of freshwater fish (Vlieg and Body, 1988; Wang et al., 1990; Sinclair et al., 1992; Yusuf et al., 1993) generally confirms this impression. In almost all cases sturgeon oil stands out for the particularly high n 0 3/n 0 6 ratio, which results from the low quantity of n 0 6 PUFAs present. It is this ratio that closely links sturgeon to mackerel among the numerous species, mainly of marine origin, studied by Hearn et al. (1987a). The positive nutritional characteristics hitherto shown for lipids extracted from sturgeon flesh are clearly a result of the diet, which was rich in products of marine origin (Henderson and Tocher, 1987; Pigott and Tucker, 1990). It is therefore possible, as suggested by Ackman and McLeod (1988), to exploit an estuarine fish, such as sturgeon, to tailor a product that combines a medium fat content with a good level of n 0 3 highly unsaturated fatty acids, so as to provide a noticeable EPA / DHA intake per single serving. According to a number of sources (Ackman, 1988; Pigott and Tucker, 1990; Bourre et al., 1992), the optimum intake of EPA / DHA would be about 300–400 mg/day. This would mean eating 100 g of fish, such as the sturgeon considered here (Table 2b), two or three times a week, provided that the fish is cooked in such a way so as to maintain its fatty acid profile substantially unaltered, e.g. by dry baking, grilling, or microwave cooking without added fat (Hearn et al., 1987b; Vlieg et al., 1988; Ackman, 1989; Pigott and Tucker, 1990; Sinclair et al., 1992).

c Index of atherogenicity Å (aS * / bS 9 / cS -)/(dP / eM / fM*), where S* Å C12:0, S9 Å C14:0, and S- Å C16:0; P Å sum of n 0 6 and n 0 3 PUFAs; M Å C18:1 and M * Å sum of other MUFAs. Empirical constants a, c, d, e, and f have been provisionally set at unity, whereas b has been set at 4 (Ulbricht and Southgate, 1991). d Index of thrombogenicity Å mSIV/[nM / oM* / p(n 0 6) / q(n 0 3) / (n 0 3)/(n 0 6)], where SIV Å sum of C14:0, C16: 0 and C18:0; (n 0 6) Å n 0 6 PUFAs; (n 0 3) Å n 0 3 PUFAs; M Å C18:1 and M* Å sum of other MUFAs. Empirical constant m has been set at unity; n, o and p have been assigned the value 0.5; q has been assigned the value 3. Fatty acid content was expressed as g/100 g (Ulbricht and Southgate, 1991).

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a b

OF

EDIBLE PORTION

OF

CULTURED STURGEONa

Means calculated from the data for nine fish individually analyzed in duplicate. Digestibility calculated-protein efficiency ratio (Satterlee et al., 1982).

Amino Acid Composition The amino acid profile of cultured sturgeon flesh is listed in Table 3, where 11 amino acids have been classified as essential as recently recommended by FAO/WHO (1990). By use of whole egg protein as the reference (Sheffner, 1967), the lowest chemical score was assigned to tryptophan, followed by methionine / cystine. Considering the rather high coefficient of variation obtained for tryptophan in the present investigation, the chemical score of the sturgeon protein, as shown in Table 3, was derived from the sulfur amino acid content (methionine / cystine). With whole egg protein again as the reference, the digestibility calculated–protein efficiency ratio, which is highly correlated with the in vivo protein efficiency ratio (Satterlee et al., 1982), was found to be very good, at 83.75% that of egg. A more comprehensive view can be gained by comparing the amino acid profile of sturgeon flesh to the requirement pattern recently proposed by FAO/WHO (1990)

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TABLE 4 SELECTED MINERAL CONTENT OF EDIBLE PORTION a OF CULTURED STURGEON (mg/100 g)

a

Means calculated from the data for nine fish individually analyzed in duplicate.

for humans above 1 year of age. The amino acid levels of a 100-g serving of sturgeon fully satisfy requirements, especially as regards histidine and isoleucine, with the single exception of tryptophan. The only other source of data available for the amino acid composition of sturgeon flesh (Moro, 1989) presents findings very similar to those presently found, with the single exception, once again, of tryptophan, which was higher (1.12 g/16 g total nitrogen). An analysis of the amino acid composition of several marine and freshwater fish, as derived from Souci et al. (1989), leads to similar conclusions. Sturgeon protein fared rather well for the ratio between essential and nonessential amino acids, whereas several species had higher ratios between essential amino acids and total nitrogen. Overall, however, it should be remembered that no substantial differences for amino acid composition are to be found, either between marine and freshwater fish (Brown, 1986) or between wild and cultured fish (Pigott and Tucker, 1990). As for the lysine/arginine ratio, the sturgeon figure (1.51) was within the range of values (1.44 to 1.77) obtained using the amino acid profiles of several marine and freshwater fish (Souci et al., 1989). It was slightly higher than the lysine/arginine value calculated by Kritchevsky et al. (1982) for fish protein (1.44), but lower than those found by the same authors for casein (1.89) and whole milk protein (2.44). Mineral Content Table 4 reports the macro- and microelement content of sturgeon flesh. Literature is lacking in reference data for this fish, therefore it will be necessary to make some comparison with range values given for finfish of several species. Moreover, for magnesium, calcium, phosphorus, iron, and zinc the values obtained for sturgeon flesh will be compared with the RDA suggested by the European Union Council (EEC, 1990). In calculating RDA percentages, a 100% availability of the element is assumed, in order to provide some measure of the contribution of each element to the diet. Sturgeon flesh is characterized by a low content of sodium, within the range reported

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BADIANI ET AL. TABLE 5 SELECTED VITAMIN CONTENT OF EDIBLE PORTION a OF CULTURED STURGEON (per 100 g)

a Means calculated from the data for nine fish individually analyzed in duplicate.

by Kinsella (1988) for fresh fish fillets and below that reported by Pigott and Tucker (1990). The range covered by the present data falls within that derived from Souci et al. (1989) for freshwater fish, which generally have a lower sodium content than marine fish (Vlieg et al., 1991). Sturgeon flesh could therefore be selected for inclusion in low-sodium diets. As is true for most fish, sturgeon flesh is a good source of potassium, within the ranges published by Pigott and Tucker (1990), as well as by Souci et al. (1989) and Holland et al. (1993) for freshwater fish. Sturgeon seems to be a good source of magnesium; its mean content is fairly high compared with published data both for marine and freshwater fish (Souci et al., 1989; Holland et al., 1993). A serving of sturgeon would provide slightly more than 15% of the European RDA (300 mg), which has been set as the significant mineral amount for nutrition labeling of processed food. Calcium levels are generally low in finfish, as long as bones are carefully removed, and sturgeon is no exception. The data generated from the present research fall at the lower end of the spectrum derived from Souci et al. (1989) both for freshwater and marine finfish, as well as within the broad range proposed by Kinsella (1988). A 100g serving of sturgeon would provide only 2.3% of the RDA (800 mg/day). Conversely, as is usual for most fish, sturgeon is rich in phosphorus, meeting about 30% of RDA (800 mg/day) with a single serving. Sturgeon is not especially rich in iron, as is the case for most fish, unless their edible portion contains a fairly high amount of dark muscle (Souci et al., 1989; Holland et al., 1993). Its contribution to the RDA (14 mg/day) is therefore rather low (around 3.8%). By comparison with published data for a wide range of fish species (Souci et al., 1989; Holland et al., 1993), zinc content is slightly more worth mentioning, as 100 g sturgeon flesh provides 5.6% of the RDA (15 mg/day). Vitamin Content Table 5 shows the water-soluble vitamin content of sturgeon flesh. The vitamins to be determined were selected as mentioned above. To the best of our knowledge, literature is lacking in reference values for vitamin content of sturgeon flesh. Some comparisons will therefore be made with data relating

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TABLE 6 HYDROXYPROLINE, COLLAGEN, AND PURINE CONTENT OF EDIBLE PORTION a OF CULTURED STURGEON (per 100 g, Unless Otherwise Noted)

a

Means calculated from the data for nine fish individually analyzed in duplicate. Hydroxyproline/collagen conversion factor Å 15 (derived from Sato et al., 1989). c Below level of quantitation (detection limit, 0.5 ng). b

to different species of finfish, as reported by Souci et al. (1989) and Holland et al. (1993). Niacin content was fairly high, to the point that a 100-g serving of sturgeon should be able to provide 31% of the RDA suggested by the European Union Council (EEC, 1990), which is 18 mg/day. Pantothenic acid, although present in quite a good amount compared with figures from Souci et al. (1989) and Holland et al. (1993), reached only 13% of the RDA (6 mg/day). Pyridoxine content compared favorably with published data, covering about 22% of the RDA (2 mg/day). Vitamin B12 content was fairly low, by comparison with literature values; nevertheless its content exceeded by far the European RDA, which is 1 mg/day. Thiamin content, determined individually on three fish, was 0.161 mg/100 g edible portion, which is a fairly good content as it falls in the higher part of the spectrum covered by the data from Souci et al. (1989) and Holland et al. (1993). As expected, though, a 100-g serving of fish gives a modest contribution (11%) to the RDA (1.4 mg/day). From the present research, sturgeon flesh was found to be a poor source of riboflavin. Its content, determined on three fish, was 0.04 mg/100 g edible portion, an unaccountably low level especially when compared with the figures reported by Holland et al. (1993) for fatty fish. Clearly, for both thiamin and riboflavin more data should be determined before drawing any conclusions about their content in sturgeon flesh. Total and Soluble Collagen Content Both hydroxyproline and collagen content are given in Table 6. No published data are available for sturgeon. A few considerations will therefore be made using literature values provided for other species. Mean hydroxyproline content fell within the upper third of the range (22–98 mg/ 100 g) reported by Sikorski et al. (1984) for numerous fish species. Furthermore, it

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was very similar to that found in carp by Kimura et al. (1988) as regards Type I collagen, which is the type predominating in fish in general and in sturgeon specifically (Sato et al., 1989). However, more numerous and interesting comparisons may be made if total collagen, expressed here as g/100 g edible portion, is considered. The sturgeon analyzed in this survey showed a considerably high total collagen content, which was between that of carp and eel, when compared with data reported by Sato et al. (1986a). The percentage of soluble collagen in sturgeon flesh was, however, noticeably higher. Of even greater interest is the comparison, again, with the data obtained by Sato et al. (1986b) for a large number of fish species, which were also scored for the tenderness of their raw and cooked flesh. Sturgeon collagen content, was close to the values found in the species with high collagen content, which proved tough when eaten raw, but much more tender after cooking (Sato et al., 1986b; Hatae et al., 1986). Manfredini (personal communication, 1994) confirmed this last observation for sturgeon flesh as well. According to Yamaguchi et al. (1976), the mechanical properties of connective tissue are governed by intermolecular bonds, both heat- and acid-labile, which cooking eliminates. Dunajski (1979) and Sikorski et al. (1984) have shown how thermal denaturation of collagen in cooked fish does away with the problem of toughness linked to connective tissue. Interest in the connective component of fish is in any case justified: (a) from a nutritional standpoint, in that a high collagen content could somewhat impair protein digestibility and utilization (Steiner-Asiedu et al., 1991b); (b) from a technological standpoint, since thermal changes in collagen play an important role during some processing techniques, such as hot smoking (Sikorski et al., 1984), which is commonly used for sturgeon. Purine Content The adenine, guanine, xanthine, and hypoxanthine content found in raw sturgeon flesh is reported in Table 6. Literature seems to be completely devoid of data about purine content in sturgeon flesh. Brule´ et al. (1988, 1989, 1992) and Souci et al. (1989) are among the few sources of information on purine content in fish. In most cases, as consistently found in the present research, xanthine was below level of quantitation. Guanine content in sturgeon proved to be almost always below values reported in literature. As for the uricogenic purine bases, adenine was within the range reported by Souci et al. (1989) for several fish species (4–21 mg/100 g edible portion) and by Brule´ et al. (1989, 1992) for haddock (11.1–22.9 mg), the latter being a rather wide range. The same is true for hypoxanthine, in haddock ranged from 72.1 to 124.3 (Brule´ et al., 1989, 1992). The lowest and highest values given for this base by Souci et al. (1989), encompassing several species, are 51 and 178 mg/100 g edible portion, respectively. Sturgeon flesh tends to appear in the medium–low area of these two ranges. CONCLUSIONS

On the basis of the present results, the most important features of cultured sturgeon were a high protein content of fairly good biological value, a medium fat and cholesterol content, fairly high levels of magnesium, niacin, pyridoxine, and vitamin B12 , a high proportion of soluble collagen, and moderate amounts of uricogenic purine bases.

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The fatty acid composition proved to be rather high in the n 0 3 PUFA content and n 0 3/n 0 6 ratio. Cultured fish with a medium fat content, like sturgeon, could probably be the most natural way to steadily provide health-conscious consumers with an appreciable amount of n 0 3 PUFAs, once fish fat has been conveniently tailored through suitable feeding choices. ACKNOWLEDGMENTS Financial support for this work was provided by the Italian Ministry of University and Scientific and Technological Research (MURST, ‘‘40%’’ Funds, Financial Year 1992). The valuable cooperation of Drs. Carlo Dalla Rosa and Paolo Bronzati is gratefully acknowledged.

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