1. Introduction
The extensive consumption of tuna, Thunnus sp., worldwide is easily explained by its nutritional benefits such as the high content in protein, low in fat and calories and relevant contribution in omega-3 fatty acids. However, apart from this and together with the sustainability of the most commonly consumed tuna species such as skipjack (Katsuwonus pelamis, SKJ) or yellowfin (Thunnus albacares, YF), the high consumption rate of tuna has been clearly intensified by the versatility that the canning industry has offered, providing a long shelf-life product for the unopened canned tuna, preserved with the nutritional properties at room temperature.
The worldwide canning tuna industry generates, therefore, huge volumes of waste from the processing, which involves deheading, gutting, filleting, cooking, etc., originating different discarded parts such as heads, viscera, central skeleton, dorsal fins, caudal fins and scales to be considered as by-products. In terms of numbers, from around 3 billion tons of global tuna fishing each year [1], the by-products suppose around 50–70% of the total raw material processed. Traditionally, all these by-products have been processed for the obtention of tuna black oil and tuna fishmeal, commonly mixed between them and with other species, reducing the potential for their use in high valuable applications. The main disadvantage of this process is the low economical and functional value of these products in the market, along with the high pollution generated by fish meal plants [2].
Exploring new avenues for these huge volumes of tuna derived by-products supposes a promising opportunity to not only increase their value but also mitigate economic losses and environmental impact [1]. Valuable biomolecules such us phospholipids, peptides, microelements, hydrolysates, etc. [3,4,5] can be isolated from these by-products though several isolation processes to produce functional compounds of high value for nutraceuticals, pharma or cosmetic applications [6,7]. Calcium phosphates are the dominant solid mineral phase in vertebrate bones. Bones provide support, protection and mobility, constituting a significant portion of fish (approximately 10–15% of their total biomass) particularly from head and vertebrae [8,9,10]. For these reasons, within all the possibilities, the by-products obtained from the mineral fraction (central skeleton, heads, fish bones, etc.) are some of the most promising as valuable sources of bio-derived calcium phosphates (CaP), representing the 10–15% of the total by-products generated during canned tuna processing [11].
This mineral fraction has been previously isolated in the literature [12,13], containing calcium phosphate (CaP) with high amounts of available calcium and phosphorous to cover the requirements for human and animal body growth, nutrient digestion and skeletal development [14]. Additionally, this bioceramic contains other trace minerals such as Na, Mg, Zn and/or K, known as essential metallic cofactors for enzymes related to human bone formation, providing a higher resemblance with the hydroxyapatite (HA, Ca10(PO4)6(OH)2) that constitutes the mineral part of human bones, with clear benefits in the regeneration of human bone tissue [15]. Moreover, in vivo studies by Suntornsaratoon et al. [16] showed that tuna bone is a great source of calcium to increase bone mineral density in both lactating rats and their offspring. This composition makes, therefore, the tuna-derived HA of great interest for its application in the biomedical field, as a high added value product.
Moreover, the ability of hydroxyapatite (HA, Ca10(PO4)6(OH)2) to incorporate different elements in their structure, such as F, Cl, Sr, Na, As and Pb, can be also of interest for biotechnological applications. Taking advantage of this property, Fijot et al. [17] developed customized purification filters, employing 3D printing technologies, composed of a polymer combined with fish-derived HA, to be used for the removal of heavy metals from an aqueous medium, in particular of cadmium (Cd) and lead (Pb). These authors proved the adsorption capability of the produced filters and provided the maximum adsorption level found for each element. It is known that the adsorption capability of hydroxyapatite is driven by a combination of ion exchange, dissolution precipitation on HA and surface complexation [17] and was also recently proposed by Wang et al. [18] for the geothermal water defluoridation; by Ying et al. [19] as a novel adsorbent for the denitrogenation of fuel; and by Cui et al. [20] for the removal of toxic metals in industrial soils, alleviating the toxicity to crops (soybean, maize).
The conversion of mineral fraction wastes into organic biofertilizers could be another cost-efficient application given that only a partial calcination is required to contribute with an eco-friendly and sustainable approach to overcome environmental issues as well as adverse agricultural problems derived from the use of chemical fertilizers [21]. The application of calcium phosphates, as hydroxyapatite (HA) or similar, in agricultural formulations has shown, recently, an increasing interest due to its biodegradability, compatibility and excellent performance as a plant nutrient and biostimulant, being fundamental for instance in crop fertilization [21,22,23].
Finally, another application of calcium phosphates in general, and of HA in particular, is related to its capability to withstand high temperatures. In relation to this, a recent work [24] investigates the application of HA in wood-based materials, such as medium density fiberboard (MDF), as a fire-retardant additive. Following the same approach, Sane et al. [25] proposed the use of HA for thermal energy storage purposes such as in concentrated solar power (CSP) plants or in units of heat recovery from industrial waste heat sources.
Nowadays, the calcium phosphates used are mostly from synthetic production, as they can be obtained by precipitation, microwave irradiation, ultrasound irradiation, sol-gel crystallization, electrodeposition, hydrothermal treatment and spray pyrolysis [26]. These processes are based on a chemical reaction between calcium and phosphate ions and suppose complicated methodologies with time consuming and costs. The fishing processed by-products, such as the ones from tuna, are affluent, can be collected at once and easily obtained by a controlled calcination [27,28].
Therefore, the aim of the present study was to evaluate in-depth the potential of the different by-products obtained from the canning tuna industry as calcium phosphate sources for high-added applications in the context of circular bioeconomy. By-products were generated in the industrial line from tuna canning activities for two of the most exploited species, yellowfin (Thunnus albacares) and skipjack (Katsuwonus pelamis), and subjected to different extraction methods (enzymatic hydrolysis/chemical extraction) followed by calcination of the isolated bone-fractions. The content in organic matter, nitrogen, total protein, lipids and amino acids of the clean bones is presented together with the main chemical bonds (FT-Raman), structure (X-ray diffraction) and elemental composition (X-ray fluorescence) of the calcium phosphates. The yield of clean bones recovery was obtained for each wasted part of the fish body (heads, branchial arc, viscera, central skeleton, caudal fin, dorsal fin, scales) together with the type of calcium phosphate relatively quantified; these aspects are essential to evaluate the potential of this mineral fraction as a source of CaP for high-added applications in terms of scaling up to an industrial process.
2. Results and Discussion
2.1. Recovery Yields and Proximal Composition
The yields obtained for the recovery of mineral by-products, using the two different extraction procedures, are shown in Table 1, expressed as percentage of wet skeletons (Ys, % (w/w) or g/100 g of waste substrate) and as percentage of dry skeletons treated at 80 °C/24 h (Yds, % w/w). As it is clearly observed, the highest recovery yield of wet skeletons was quantified for the by-products treated using the chemical treatment, with yield values >58%, being particularly high for dorsal (dF, 85.7 ± 4.8%) and caudal fin (cF, 89.7 ± 5.4%) of yellowfin tuna (YF). It is well known that by nature the original by-products from fins are less rich in muscular remains and mostly composed of rigid bone structures, which fits with the yield results obtained. On the opposite side, as expected, viscera showed the lowest wet skeleton percentages (Ys), extracted by enzymatic proteolysis, with values of (SKJ) 7.4 ± 4.3% and (YF) 5.3 ± 2.6%, respectively. This mineral fraction found can only proceed from other marine organisms present at viscera due to their digestion by tunas during their feeding in the marine environment before the capture. The results of dry skeletons (Yds) also shown in Table 1 indicated the same behaviors as exposed for wet skeletons.
As indicated in the Materials and Methods section, the extraction by the enzymatic method was used for heads (He), branchial arches (bA), central skeletons (cS) and viscera (V) as it is the most appropriate one to obtain protein hydrolysates with functional peptides. The chemical extraction was used for caudal and dorsal fins together with scales to produce gelatin and/or collagen hydrolysates. The methods used per each by-product are, therefore, the ones used in the industrial production lines [5,29]. This way, the corresponding released mineral fractions of both extraction methods were collected and evaluated at the present work and will be in consonance with the ones at production lines, which will facilitate the valorization of these mineral parts. Given that experiments comparing treatments for the same by-product have not been the focus of these work, it is not clear that the chemical treatment is more efficient than the enzymatic one, as each by-product was subjected just to the extraction method already optimized at the production line, and therefore, the differences in yield found between both methodologies are not clearly influenced by the extraction method. Moreover, in this aspect, SKJ tuna wastes showed in general terms lower dispersion in yields (error as confidence intervals) than in YF tuna, due to an industrial process more automatized for the obtention of the different cut fractions.
The proximal composition determined from the two tuna species in all these recovered by-products from the production line methods is presented in Table 2. Differences in the composition calculated on a wet basis between tuna species can be clearly observed, being the differences for most of the by-products evaluated statistically significant for moisture, ash and organic matter (p < 0.05). However, no clear patterns were observed. In fact, in some by-products the content of OM or ash was higher in SKJ than in YF, for example OM in heads (He): (SKJ) 24.6 ± 1.3% vs. (YF) 21.0 ± 0.5%; meanwhile this outcome was contrary to others being higher in YF than in SKJ, as in bA (SKJ: 21.1 ± 2.3% against YF: 26.6 ± 2.1%). This remarkable variability may be due to actual differences in the composition of tuna species together with differences in the amount of OM attached to the clean bones in each species. Moreover, in some substrates, the hydrolysis processing and the analytical determinations could also contribute to the variability between the batches of each sample. When comparing the differences in the composition calculated on a wet basis between the by-products, high percentages in ash, directly related to the amount in mineral fraction, were found for heads and dorsal fins of both species, with values of He-SKJ: 40.6 ± 0.5, He-YF: 34.7 ± 0.5, dF-SKJ: 56.9 ± 1.3 and dF-YF: 35.0 ± 4.3.
Attending to the dry basis data (samples dried at 107 °C for 16 h), the percentage of ashes achieved values ranging 52–66% in the majority of the substrates, with a remarkable level of lipids (>17%) in Sc. These values agree with those showed in the isolation of collagen from bone of deep-sea redfish [30]. These authors attempted the use of EDTA and hexane during 24 h to remove fat, which may hinder its potential application on an industrial scale. The protein was ranged in the interval of 30–53%, as it was also obtained in other fish bone wastes [31]. Based on this chemical composition, tuna skeletons could be a valuable ingredient to include in plant growth formulations [21]. In that work, bones of Sardinella aurita calcinated at 300 °C, 600 °C and 900 °C, and with a similar content of organic matter, revealed interesting capacity of coleoptile and seed biostimulant as well as P-fertilizer.
The amount of collagen present in each substrate—based on the sum of glycine, proline and hydroxyproline—revealed important differences between the skeleton origins (Table 3): heads, dorsal fin and caudal fin of both species showed percentages around 40% with more than 18% of Pro + OHPro. Quite similar content was found in bA-YF, but not in SKJ (p < 0.05). In cF-YF the sum of proline and hydroxyproline reached a level of 20%. Other authors have obtained similar compositional values after the extraction of collagen derivate from bones of deep-sea redfish [30], rainbow trout [32], hake [33] and mackerel [34]. This type of behavior was also observed in the recovery of gelatins from skins of turbot, seabream and seabass [35,36]. As expected, higher values of collagen amino acids cause a significant decrease (p < 0.05) in the proportion of total essential amino acids (TEAA), since Gly, Pro and OHPro are not essential ones for human, aquaculture and bacteria nutrition [37,38,39]. In this context, bA-YF and cS-YF achieved the highest levels of TEAA (36% and 38%, respectively). Protein hydrolysates obtained by enzyme proteolysis of by-products (head and skins) from various fish species (blue whiting, mackerel, gurnard and megrim) also yielded percentages in that similar interval of essential amino acids [40,41].
2.2. Physicochemical Characterization
The physicochemical characterization determined from the two tuna species in all by-products was also evaluated. Figure 1 shows the XRD patterns of the bioceramics obtained from the dorsal fin, viscera and head of SKJ (K. pelamis) in the range of 30° to 35°, where the most relevant peaks are diffracted. The XRD patterns reveal the presence of crystalline structures. Going into detail, in the case of the diffraction pattern obtained from the dorsal fin (Figure 1A) the RIR semi-quantitative evaluation establishes an apatite phase, particularly hydroxyapatite, with typical reflections located at 31.8°, 32.2°, 32.9° and 34.1°, corresponding to the (1, 2, 1), (1, 1, 2), (3, 0, 0) and (2, 0, 2) diffraction planes [42,43]. In the case of the bioceramics extracted from the viscera of the same fish (Figure 1B) the reflections located at 31.2°, 32.7° and 34.6°, respectively, correspond to the (0, 2, 10), (1, 2, 8) and (2, 2, 0) diffraction planes assigned to a non-apatite phase, particularly whitlockite/β-tricalcium phosphate [42,44]. Finally, the bioceramic extracted from the head (Figure 1C) presented a diffraction pattern with reflections associated to both phases (apatite and non-apatite), confirming a biphasic calcium phosphate bioceramic.
The same bioceramics were analyzed using Raman, and the resulting spectral fingerprint region (250–1200 cm−1), where the relevant inorganic molecular vibrations are present, are shown at Figure 2 for dorsal fin (Figure 2(A.1,A.2)), viscera (Figure 2(B.1,B.2)) and head (Figure 2(C.1,C.2)). Moreover, the deconvolution of the corresponding main Raman band in the 930–990 cm−1 region is also included for each one. According to previous studies [42,45,46] the Raman spectra exhibit the main vibration modes associated with PO43− groups: a band in the range 400 cm−1 to 485 cm−1 attributed to symmetric bending (ν2), a peak at 570 cm−1 to 620 cm−1 assigned to asymmetric bending (ν4) and an intense band at 930 cm−1 to 990 cm−1 due to the symmetric stretching (ν1). The three low resolution peaks centered at 1030 cm−1, 1048 cm−1 and 1078 cm−1 are also characteristic of the asymmetric stretching (ν3) of PO43− groups. Although the Raman spectra of these three bioceramics are similar, some differences can be observed, particularly in the range between 900 cm−1 and 1000 cm−1. As already explained, this region is dominated by a wide band representing the symmetric stretching vibration (ν1) of PO43− groups. In the case of the spectrum obtained for dF-SKJ dorsal fin (Figure 2(A.1)), the band is fairly symmetrical compared to He-SKJ (Figure 2(C.1)), while V-SKJ (Figure 2(B.1)) presents a well-defined doublet. Taking into account the XRD results (Figure 1) and the literature data [42,47,48,49], this band can be associated with both the symmetric stretching mode of PO43− groups in apatite (hydroxyapatite) and with non-apatite crystalline structures (whitlockite or β-TCP).
To clarify the structural differences between these bioceramics, the deconvolution of this main Raman band in the region 930–990 cm−1 was carried out (Figure 2(A.2–C.2)). Thus, in the case of the dF-SKJ spectrum (Figure 2(A.2)), it can be clearly observed as the band is composed of one vibrational band, located at 962 cm−1, attributed to hydroxyapatite crystal [42,47,48]. The Raman spectrum of V-SKJ (Figure 2(B.2)) shows a broad band made up of two independent vibrations located at 960 cm−1 and 975 cm−1 attributed to whitlockite or β-TCP structures [42,48,49]. Finally, the deconvolution of the He-SKJ Raman spectrum (Figure 2(C.2)) shows a main peak centered at 962 cm−1 and two secondary peaks located at 949 cm−1 and 975 cm−1, which are values close to those reported for HA and whitlockite/β-TCP mixtures [42]. This result agrees with the XRD analysis (Figure 1) of a biphasic calcium phosphate bioceramic (apatite and non-apatite phases).
Following the same methodology as for SKJ, the bioceramics obtained from different discards of Thunnus albacares (YF) were also analyzed. The XRD diffraction pattern obtained together with the deconvoluted main Raman band are both presented in Figure 3 for the branchial arch. The same discard obtained from SKJ is also presented. The results indicated that the bA-YF waste corresponds to a hydroxyapatite, while the same section obtained from SKJ indicates a biphasic bioceramic: hydroxyapatite and whitlockite. A similar result was observed for the bioceramics obtained from the scales, presented in Figure 4.
The elemental composition for these calcium phosphates was also evaluated by XRF and presented in Table 4 as certified wt.% per element. All samples are presented as major elements Ca and P. The presence of other elements such as Mg, Sr, Zn, Ag, Mn and Fe was also detected, however in much smaller proportions and not accurately quantified (uncertified values).
A summary of the calcium phosphate structure obtained according to the corresponding XRD pattern for the branchial arch, caudal fin, dorsal fin, central skeleton, head and viscera discards evaluated from both species is presented in Table 5. It can be observed as, depending on the origin of the discard and the species, the calcium phosphate presents different crystalline structure: monophasic (apatite or non-apatite) structure or biphasic (mixture of both). Thus, the calcium phosphate obtained from caudal fin, dorsal fin and central skeleton discard yellowfin and skipjack tuna of both species corresponds with an apatite structure, particularly hydroxyapatite. In the case of viscera tuna discard, it is a non-apatite structure, whitlockite/β-TCP. The head wastes of YT and SKJ originated a biphasic calcium phosphate. In the case of the branchial arch and scales discard, the calcium phosphate structures vary by species, being in both discards’ hydroxyapatite for YF but biphasic for SKJ.
3. Materials and Methods
3.1. Tuna Skeleton Substrates and Processing
The substrates from yellowfin tuna (Thunnus albacares, YF) and skipjack tuna (Katsuwonus pelamis, SKJ) were produced in the canning processing of tuna from Jealsa Foods S.A.U. (Boiro, Spain). They were obtained by mechanical cutting in the industrial line and classified and characterized separately: head (He), branchial arc (bA), viscera (V), central skeleton (cS), caudal fin (cF), dorsal fin (dF) and scales (Sc). Two different extraction methods were used to obtain a rich mineral by-product together with functional biocompounds depending on their specific prevalence in each part of the tuna. The preconditioning step for all the by-products was the mechanical cut of the raw material to obtain pieces of a maximum of 5 cm × 5 cm.
On one hand, an enzymatic hydrolysis was performed in a glass jacketed reactor of 5 L capacity employing the following experimental conditions: (solid:water) ratio of 1:1, 0.1% (v:w) of Novozym 37071 (Nordisk, Bagsvaerd, Denmark), controlled temperature at 60 °C, 2 h of hydrolysis without pH control and continuous agitation at 250 rpm. This method was used for He, bA, cS and V from both species (SKJ and YF) to obtain protein hydrolysates with functional peptides [5]. The released mineral fractions were studied in this work.
On the other hand, a chemical extraction was performed using a (solid:water) ratio 1:2.5, adding 0.02 M H2SO4, for 1 h of hydrolysis at 15 °C with soft agitation (10 rpm), followed by a thermal extraction with water (solid:water) ratio 1:2.5, for 2.5 h at 50 °C with soft agitation (10 rpm). This protocol was used for cF, dF and Sc from SKJ and YF to produce gelatin and/or collagen hydrolysates. The mineral remains generated were explored in the present work. For both procedures, a minimum of three replicates were conducted for each part of the tuna body.
Finally, each mineral substrate was calcined at 950 °C, in a laboratory furnace, for 16 h at a heating rate of 5 °C/min. After the calcination temperature was achieved, calcium phosphates remained inside the furnace isothermally for a period of 16 h and cooled down at a cooling rate of 5 °C/min before being recovered from the furnace.
3.2. Chemical Analysis
The proximal composition of the different skeletons was determined by means of (1) water, ash and organic matter content using gravimetry [50]; (2) total nitrogen concentration performing spectrophotometric measurement after Kjeldhal digestion and subsequent ammonium reaction in alkaline medium [50]; (3) total protein was calculated as total nitrogen × 6.25 and transformed to percentage versus dry weight; (4) total lipids using Soxhlet extraction and gravimetric quantification [51] and (5) the amino acid profiles by ninhydrin reaction, using an amino acid analyzer (Biochrom 30 series, Biochrom Ltd., Cambridge, UK), according to the method of [52].
3.3. Physicochemical Characterization
The crystalline structure of the corresponding calcium phosphates obtained was evaluated by X-ray diffraction (XRD) in a X’Pert Pro Panalytical diffractometer (Malvern Panalytical, Malvern, UK) with monochromated Cu-Kα radiation (λ = 1.5406 Å) and with a 2θ range of 4–100° (CACTI, UVigo, Vigo, Spain). Moreover, to identify the main molecular vibrations and corresponding functional groups, Raman spectroscopy (Raman) was carried out using a B&W Tek i-Raman-785S instrument (Metrohm, Herisau, Switzerland) equipped with a BAC 100 Probe (785 nm) and a maximum incident laser radiation of 340 mW. Measurements were performed in the 200–3200 cm−1 range of Raman shift with a global resolution of 4 cm−1. The Raman spectra obtained were corrected by a parabolic baseline and deconvoluted in the band area 930–1000 cm−1 using the MagicPlot Pro 3.0.1 software. Finally, elemental analysis of the calcium phosphates was performed by X-ray fluorescence (XRF Olympus Vanta C, CINTECX, UVigo, Vigo, Spain) using a certified reference material Geochem.
4. Conclusions
The feasibility of obtaining various calcium phosphates from the by-products of the tuna canning industry has been demonstrated, with calcium and phosphorus identified as the predominant chemical elements in all mineral fractions. The proximal composition of tuna skeletons showed significant variations among different substrates and species, highlighting the notably total lipid content in the scales (exceeding 17%) and the presence of glycine, proline and hydroxyproline in He, dF and cF, indicating a substantial collagen presence. Furthermore, the balanced composition of ash and organic matter in fish skeletons could be very attractive for applications in the fertilizer industry. The different crystalline structures obtained from Ca/P, primarily consisting of hydroxyapatite or in a biphasic combination with whitlockite/β-TCP, can also offer other interesting high added-value solutions, such as in biotechnological applications for purification filters, fire-retardant additives or even in the biomedical field, where synthetic HA is one of the most commonly used materials in bone tissue regeneration. Moreover, biphasic materials, such as those obtained from the heads of both species, have recently gained interest for their enhanced performance in biomedical applications compared to single-phase formulations. By achieving a balance composition, where the soluble component (β-TCP) provides favorable degradation and bioactivity, while the stable component (HA) ensures structural integrity and excellent mechanical characteristics, faster bone regeneration be promoted [53].
In conclusion, the differences found could impact the utilization of these by-products in industrial applications, highlighting the importance of selecting the appropriate part of the skeleton and species based on the application’s objectives. This paper presents a range of calcium phosphates from different parts and species that can serve various purposes, emphasizing their potential versatility in various applications and promoting a more sustainable approach. All of this within the context of the circular bioeconomy, as summarized in the graphical abstract (image attributions from [54,55,56,57]).
Conceptualization, P.S.-M., S.D., M.L.-Á. and J.A.V.; methodology, P.S.-M., S.D., M.L.-Á. and J.A.V.; validation, P.S.-M., S.D., M.L.-Á. and J.A.V.; formal analysis, P.S.-M., S.D., M.L.-Á. and J.A.V.; investigation, P.S.-M., S.D., M.L.-Á. and J.A.V.; resources, P.S.-M., S.D., M.L.-Á., P.G., J.S., S.P.-D. and J.A.V.; writing—original draft preparation, M.L.-Á., P.G., J.S., S.P.-D. and J.A.V.; writing—review and editing, M.L.-Á., P.G., J.S., S.P.-D. and J.A.V.; visualization, M.L.-Á., P.G., J.S., S.P.-D. and J.A.V.; supervision, P.G., J.S. and J.A.V.; project administration, P.G., J.S. and J.A.V.; funding acquisition, P.G., J.S. and J.A.V. All authors have read and agreed to the published version of the manuscript.
Data is contained within the article.
The technical staff from CACTI (UVigo) is gratefully acknowledged.
Authors Paula Souto Montero and Salvador Durán are employees of the Company Jealsa Foods S.A.U. as participants of the LIFE-REFISH Project in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The remaining authors have no conflicts of interest to declare.
Footnotes
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.
Enlarge this image.Figure 1. XRD patterns in the range from 30° to 35° of calcium phosphate extracted from Katsuwonus pelamis (SKJ) dorsal fin (A), viscera (B) and head (C).
Enlarge this image.Figure 2. Raman spectra of calcium phosphate extracted from Katsuwonus pelamis (SKJ) dorsal fin, viscera and head. (A.1–C.1) The deconvolution of the corresponding main Raman band in the 930–990 cm−1 region is also included (A.2–C.2).
Enlarge this image.Figure 3. XRD patterns (left) in the range from 30° to 35° and deconvolution of the main Raman band in the 930–990 cm−1 region (right) of calcium phosphate extracted from Thunnus albacares (YF) and Katsuwonus pelamis (SKJ) branchial arch. The sign * corresponds to the apatite phase, while the sign + indicates non-apatite phase.
Enlarge this image.Figure 4. XRD patterns (left) in the range from 30° to 35° and deconvolution of the main Raman band in the 930–990 cm−1 region (right) of calcium phosphate extracted from Thunnus albacares (YF) and Katsuwonus pelamis (SKJ) scale. The sign * corresponds to the apatite phase, while the sign + indicates non-apatite phase.
Yields of skeleton material released after enzyme or chemical hydrolysis from wastes of two tuna species (skipjack tuna, SKJ, and yellowfin tuna, YF). He: head. cS: central skeleton. V: viscera. bA: branchial arches. dF: dorsal fin. cF: caudal fin. Sc: scale. Ys: percentage of wet skeletons. Yds: percentage of dry skeleton treated at 80 °C/24 h. Data are in % (w/w) or g/100 g of waste substrate. Error are the confidence intervals for n = 3–12 (independent batches) and α = 0.05. Different superscript letters in each row mean statistically significant differences between all samples (p < 0.05). Different superscript numbers in each row mean significant differences between samples from each species (p < 0.05).
| Substrate | Procedure | Ys (%) | Yds (%) |
|---|---|---|---|
| He-SKJ | enzymatic | 30.8 ± 4.0 ab,1 | 13.6 ± 1.8 a,1 |
| He-YF | 23.4 ± 8.0 bc,1 | 10.5 ± 1.4 a,1 | |
| cS-SKJ | enzymatic | 37.5 ± 5.6 a,1 | 22.9 ± 2.1 b,1 |
| cS-YF | 9.9 ± 9.9 c,2 | 5.8 ± 2.3 c,2 | |
| V-SKJ | enzymatic | 7.4 ± 4.3 c,1 | 3.4 ± 0.7 d,1 |
| V-YF | 5.3 ± 2.6 c,2 | 2.5 ± 1.2 d,2 | |
| bA-SKJ | enzymatic | 51.2 ± 1.0 d,1 | 35.2 ± 3.9 ef,1 |
| bA-YF | 23.0 ± 0.9 c,2 | 15.4 ± 2.2 a,2 | |
| dF-SKJ | chemical | 63.0 ± 2.8 e,1 | 45.0 ± 4.2 f,1 |
| dF-YF | 85.7 ± 4.8 f,2 | 59.1 ± 5.1 g,2 | |
| cF-SKJ | chemical | 74.2 ± 6.4 g,1 | 32.8 ± 3.9 e,1 |
| cF-YF | 89.7 ± 5.4 f,2 | 41.2 ± 3.6 f,2 | |
| Sc-SKJ | chemical | 58.3 ± 2.5 e,1 | 32.8 ± 3.9 e,1 |
| Sc-YF | 60.2 ± 3.3 e,1 | 35.8 ± 2.1 e,1 |
Proximal composition of different skeletons, calculated on wet and dry basis, from two tuna species (skipjack tuna, SKJ, and yellowfin tuna, YF). He: head. cS: central skeleton. V: viscera. bA: branchial arches. dF: dorsal fin. cF: caudal fin. Sc: scales. Mo: moisture. Ash: ash. OM: organic matter. Lip: total lipids. Prt: total protein. All data are in % (w/w) or g/100 g of skeleton. Different superscript letters in each row mean significant differences between each tuna species (p < 0.05).
| Wet Basis | Dry Basis | |||||
|---|---|---|---|---|---|---|
| Tuna Skeleton | Mo (%) | Ash (%) | OM (%) | Ash (%) | Lip (%) | Pr-tN (%) |
| He-SKJ | 34.9 ± 1.6 a | 40.6 ± 0.5 a | 24.6 ± 1.3 a | 61.3 ± 1.6 a | 1.8 ± 0.3 a | 36.9 ± 0.9 a |
| He-YF | 44.3 ± 0.3 b | 34.7 ± 0.5 b | 21.0 ± 0.5 b | 60.8 ± 1.1 a | 2.2 ± 1.9 b | 37.1 ± 1.8 a |
| cS-SKJ | 58.6 ± 1.9 a | 23.4 ± 1.0 a | 17.9 ± 0.3 a | 58.3 ± 0.7 a | 5.9 ± 1.0 a | 35.9 ± 1.2 a |
| cS-YF | 54.1 ± 0.9 b | 27.5 ± 1.3 b | 18.4 ± 0.5 a | 60.5 ± 0.4 b | 4.4 ± 2.8 a | 35.1 ± 1.0 a |
| V-SKJ | 67.7 ± 1.4 a | 21.5 ± 0.4 a | 10.8 ± 1.0 a | 65.8 ± 1.8 a | 3.2 ± 0.8 a | 31.1 ± 1.2 a |
| V-YF | 37.5 ± 5.1 b | 35.8 ± 5.8 b | 26.8 ± 0.7 b | 53.8 ± 2.6 b | 4.1 ± 0.6 a | 42.1 ± 2.1 b |
| bA-SKJ | 62.3 ± 1.8 a | 16.6 ± 0.5 a | 21.1 ± 2.3 a | 40.2 ± 1.0 a | 9.8 ± 1.2 a | 50.0 ± 1.4 a |
| bA-YF | 39.4 ± 4.7 b | 34.0 ± 3.2 b | 26.6 ± 2.1 b | 52.5 ± 1.6 b | 8.7 ± 0.2 a | 38.8 ± 0.9 b |
| dF-SKJ | 14.2 ± 0.6 a | 56.9 ± 1.3 a | 28.9 ± 0.9 a | 63.8 ± 3.1 a | 5.5 ± 0.1 a | 30.8 ± 1.4 a |
| dF-YF | 38.7 ± 5.7 b | 35.0 ± 4.3 b | 26.3 ± 1.0 b | 54.5 ± 1.7 b | 7.2 ± 0.2 b | 38.3 ± 1.9 b |
| cF-SKJ | 46.5 ± 2.3 a | 23.7 ± 0.9 a | 29.8 ± 0.6 a | 48.9 ± 2.4 a | 5.9 ± 0.3 a | 45.2 ± 3.4 a |
| cF-YF | 52.2 ± 1.1 b | 18.9 ± 1.0 b | 28.9 ± 0.1 b | 40.5 ± 1.1 b | 6.5 ± 0.2 b | 53.0 ± 2.9 b |
| Sc-SKJ | 53.1 ± 2.9 a | 14.6 ± 2.3 a | 32.3 ± 0.6 a | 33.0 ± 1.6 a | 25.1 ± 3.2 a | 42.0 ± 1.6 a |
| Sc-YF | 50.0 ± 1.6 a | 16.1 ± 0.8 a | 33.9 ± 1.1 a | 34.2 ± 0.7 a | 16.9 ± 2.2 b | 48.1 ± 1.2 b |
Ratio of total essential amino acids (TEAA)/total amino acids (TAA), and percentage of glycine (Gly), proline (Pro) and hydroxyproline (OHPro) from total amino acids for each dry fish skeleton. Different superscript letters in each row mean statistically significant differences between samples from each species (p < 0.05). Different superscript numbers in each row mean significant differences between species for each sample (p < 0.05).
| Species | Sample | TEAA/TAA (%) | Gly (%) | Pro (%) | OHPro (%) |
|---|---|---|---|---|---|
| SKJ | He | 27.9 ± 0.7 a,c,1 | 21.0 ± 0.6 a,b,1 | 10.1 ± 0.2 a,1 | 8.5 ± 0.3 a,1 |
| cS | 37.7 ± 3.1 b,1 | 13.2 ± 2.5 b,1 | 7.6 ± 0.4 b,1 | 4.8 ± 1.4 b,1 | |
| V | 29.8 ± 1.4 a,1 | 19.7 ± 0.1 a,1 | 8.8 ± 0.5 c,1 | 7.5 ± 0.4 c,1 | |
| dF | 27.3 ± 0.5 c,1 | 20.9 ± 0.5 c,1 | 10.4 ± 0.3 a,1 | 9.3 ± 0.6 a,1 | |
| cF | 27.9 ± 0.4 c,1 | 20.2 ± 0.9 a,c,1 | 10.3 ± 0.4 a,1 | 8.6 ± 0.2 a,1 | |
| Sc | 30.0 ± 0.6 d,1 | 19.5 ± 0.7 a,c,1 | 10.2 ± 0.7 a,1 | 7.7 ± 0.6 c,1 | |
| bA | 36.0 ± 0.7 b,1 | 13.7 ± 0.6 b,1 | 7.8 ± 0.2 b,1 | 5.4 ± 0.1 b,1 | |
| YF | He | 28.1 ± 0.5 a,1 | 21.0 ± 0.6 a,1 | 9.9 ± 0.2 a,1 | 8.4 ± 0.5 a,c,1 |
| cS | 30.8 ± 1.0 b,2 | 17.8 ± 0.6 b,2 | 9.0 ± 0.2 b,2 | 7.7 ± 0.2 a,2 | |
| V | 32.7 ± 0.2 c,2 | 16.7 ± 0.1 c,2 | 8.5 ± 0.4 b,2 | 6.4 ± 0.4 b,2 | |
| dF | 28.9 ± 0.3 a,1 | 19.8 ± 0.2 d,2 | 10.3 ± 0.3 a,1 | 8.6 ± 0.3 c,1 | |
| cF | 27.8 ± 0.8 a,1 | 20.8 ± 0.5 a,1 | 11.1 ± 0.4 c,1 | 9.1 ± 0.5 c,1 | |
| Sc | 31.0 ± 0.6 b,1 | 17.8 ± 0.7 b,2 | 9.7 ± 0.3 a,1 | 7.6 ± 0.3 a,1 | |
| bA | 29.3 ± 0.4 a,2 | 20.0 ± 0.6 a,d,2 | 10.2 ± 0.3 a,2 | 8.2 ± 0.5 a,c,2 |
Calcium phosphates elemental composition by X-ray fluorescence.
| Calcium Phosphates | Ca | P | Others |
|---|---|---|---|
| He-SKJ | 35.3 | 13.1 | Sr, Zn, Ag, Mn, Fe, Co, Cu, Mo, Th, Pb |
| He-YF | 33.8 | 12.7 | Sr, Zn, Ag, Fe, Th |
| bA-YF | 34.1 | 12.3 | Sr, Zn, Ag, Mn, Fe, Co, Mo, Th |
| bA-SKJ | 33.7 | 12.4 | Sr, Zn, Ag, Mn, Fe, Cu, Mo, Th, Sb |
| cF-YF | 33.0 | 10.4 | Cl, Sr, Zn, Ag, Fe, Cu, Mo, Th, Ni |
| cF-SKJ | 32.9 | 12.1 | Sr, Zn, Ag, Fe, Mo, Th |
| dF-YF | 34.6 | 12.1 | Cl, Sr, Zn, Ag, Fe, Co, Cu, Mo, Th, Ti |
| dF-SKJ | 34.4 | 12.2 | Sr, Zn, Ag, Fe, Co, Mo, Th, |
| Sc-SKJ | 34.7 | 12.0 | Sr, Zn, Ag, Fe, Cu, Mo, Ti, Se |
| Sc-YF | 33.1 | 11.9 | Sr, Zn, Ag, Fe, Mo, Th |
| cS-SKJ | 34.9 | 12.0 | Sr, Zn, Ag, Fe, Th |
| cS-YF | 36.0 | 12.6 | Sr, Zn, Ag, Fe, Cu, Mo, Th |
| V-SKJ | 30.3 | 14.5 | Mg (3.1 wt.%) |
| V-YF | 30.5 | 13.5 | Sr, Zn, Ag, Fe, Cu, Mo, Th, Cd, Rb |
Type of calcium phosphate presented in the different skeletons of tuna.
| Calcium Phosphate Structure | Tuna Skeleton |
|---|---|
| Hydroxyapatite | bA-YF |
| cF-YF | |
| cF-SKJ | |
| dF-YF | |
| dF-SKJ | |
| cS-SKJ | |
| cS-YF | |
| Sc-YF | |
| Whitlockite/β-TCP | V-SKJ |
| V-YF | |
| Hydroxyapatite and Whitlockite/β-TCP | Sc-SKJ |
| bA-SKJ | |
| He-SKJ | |
| He-YF |
References
1. FAO. The State of World Fisheries and Aquaculture 2020. Sustainability in Action; FAO: Rome, Italy, 2020; [DOI: https://dx.doi.org/10.4060/ca9229en]
2. Coppola, D.; Lauritano, C.; Esposito, F.P.; Riccio, G.; Rizzo, C.; de Pascale, D. Fish Waste: From Problem to Valuable Resource. Mar. Drugs; 2021; 19, 116. [DOI: https://dx.doi.org/10.3390/md19020116] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33669858]
3. Gamarro, E.G.; Orawattanamateekul, W.; Sentina, J.; Gopal, T.K.S. By-Products of Tuna Processing. GLOBEFISH Research Programme; FAO: Rome, Italy, 2013; Volume 112.
4. Unnikrishnan, P.; Kizhakkethil, B.P.; George, J.C.; Aliyamveetil Abubacker, Z.; Ninan, G.; Chandragiri Nagarajarao, R. Antioxidant Peptides from Dark Meat of Yellowfin Tuna (Thunnus albacares): Process Optimization and Characterization. Waste Biomass Valorization; 2021; 12, pp. 1845-1860. [DOI: https://dx.doi.org/10.1007/s12649-020-01129-8]
5. Vázquez, J.A.; Pedreira, A.; Durán, S.; Cabanelas, D.; Souto-Montero, P.; Martínez, P.; Mulet, M.; Pérez-Martín, R.I.; Valcarcel, J. Biorefinery for Tuna Head Wastes: Production of Protein Hydrolysates, High-Quality Oils, Minerals and Bacterial Peptones. J. Clean. Prod.; 2022; 357, 131909. [DOI: https://dx.doi.org/10.1016/j.jclepro.2022.131909]
6. Ideia, P.; Pinto, J.; Ferreira, R.; Figueiredo, L.; Spínola, V.; Castilho, P.C. Fish Processing Industry Residues: A Review of Valuable Products Extraction and Characterization Methods. Waste Biomass Valorization; 2020; 11, pp. 3223-3246. [DOI: https://dx.doi.org/10.1007/s12649-019-00739-1]
7. Yang, X.R.; Zhao, Y.Q.; Qiu, Y.T.; Chi, C.F.; Wang, B. Preparation and Characterization of Gelatin and Antioxidant Peptides from Gelatin Hydrolysate of Skipjack Tuna (Katsuwonus pelamis) Bone Stimulated by in Vitro Gastrointestinal Digestion. Mar. Drugs; 2019; 17, 78. [DOI: https://dx.doi.org/10.3390/md17020078] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/30678362]
8. Toppe, J.; Albrektsen, S.; Hope, B.; Aksnes, A. Chemical Composition, Mineral Content and Amino Acid and Lipid Profiles in Bones from Various Fish Species. Comp. Biochem. Physiol. B Biochem. Mol. Biol.; 2007; 146, pp. 395-401. [DOI: https://dx.doi.org/10.1016/j.cbpb.2006.11.020]
9. Glimcher, M.J. Bone: Nature of the Calcium Phosphate Crystals and Cellular, Structural, and Physical Chemical Mechanisms in Their Formation. Rev. Miner. Geochem.; 2006; 64, pp. 223-282. [DOI: https://dx.doi.org/10.2138/rmg.2006.64.8]
10. Gnanasekaran, R.; Yuvaraj, D.; Muthu, C.M.M.; Ashwin, R.; Kaarthikeyan, K.; Kumar, V.V.; Ramalingam, R.J.; Al-Lohedan, H.; Reddy, K. Extraction and Characterization of Biocompatible Hydroxyapatite (Hap) from Red Big Eye Fish Bone: Potential for Biomedical Applications and Reducing Biowastes. Sustain. Chem. Environ.; 2024; 7, 100142. [DOI: https://dx.doi.org/10.1016/j.scenv.2024.100142]
11. Shavandi, A.; Hou, Y.; Carne, A.; McConnell, M.; Bekhit, A.E. din A. Marine Waste Utilization as a Source of Functional and Health Compounds. Adv. Food Nutr. Res.; 2019; 87, pp. 187-254. [DOI: https://dx.doi.org/10.1016/bs.afnr.2018.08.001]
12. Abrams, S.A. Calcium Absorption in Infants and Small Children: Methods of Determination and Recent Findings. Nutrients; 2010; 2, pp. 474-480. [DOI: https://dx.doi.org/10.3390/nu2040474]
13. Cormick, G.; Belizán, J.M. Calcium Intake and Health. Nutrients; 2019; 11, 1606. [DOI: https://dx.doi.org/10.3390/nu11071606] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31311164]
14. Albrektsen, S.; Østbye, T.K.; Pedersen, M.; Ytteborg, E.; Ruyter, B.; Ytrestøyl, T. Dietary Impacts of Sulphuric Acid Extracted Fish Bone Compounds on Astaxanthin Utilization and Muscle Quality in Atlantic Salmon (Salmo salar). Aquaculture; 2018; 495, pp. 255-266. [DOI: https://dx.doi.org/10.1016/j.aquaculture.2018.05.047]
15. Dorozhkin, S.V. Bioceramics of Calcium Orthophosphates. Biomaterials; 2010; 31, pp. 1465-1485. [DOI: https://dx.doi.org/10.1016/j.biomaterials.2009.11.050]
16. Suntornsaratoon, P.; Charoenphandhu, N.; Krishnamra, N. Fortified Tuna Bone Powder Supplementation Increases Bone Mineral Density of Lactating Rats and Their Offspring. J. Sci. Food Agric.; 2018; 98, pp. 2027-2034. [DOI: https://dx.doi.org/10.1002/jsfa.8688]
17. Fijoł, N.; Abdelhamid, H.N.; Pillai, B.; Hall, S.A.; Thomas, N.; Mathew, A.P. 3D-Printed Monolithic Biofilters Based on a Polylactic Acid (PLA)-Hydroxyapatite (HAp) Composite for Heavy Metal Removal from an Aqueous Medium. RSC Adv.; 2021; 11, pp. 32408-32418. [DOI: https://dx.doi.org/10.1039/D1RA05202K]
18. Wang, F.; Chen, Y.; Dong, Y.; Zhang, H.; Yun, R.; Liu, Z. Removal of Fluoride from Geothermal Water by Waste-Synthesized Al(OH)3-HAP@ZMS Composite Adsorbent: Sorption Capability and Mechanism. Water Air Soil Pollut.; 2023; 234, 411. [DOI: https://dx.doi.org/10.1007/s11270-023-06448-9]
19. Yin, P.; Chen, Y.; Wang, Y.; Chi, Y.; Li, B.; Xu, M.; Song, H.; Chen, C. Hydroxyl Modified Nano Calcium Phosphate, a Novel Adsorbent for Denitrogenation of Fuel: Synthesis, Characterization and Adsorptive Performance for Quinoline. J. Environ. Chem. Eng.; 2023; 11, 110374. [DOI: https://dx.doi.org/10.1016/j.jece.2023.110374]
20. Cui, X.; Cao, X.; Xue, W.; Xu, L.; Cui, Z.; Zhao, R.; Ni, S.Q. Integrative Effects of Microbial Inoculation and Amendments on Improved Crop Safety in Industrial Soils Co-Contaminated with Organic and Inorganic Pollutants. Sci. Total Environ.; 2023; 873, 162202. [DOI: https://dx.doi.org/10.1016/j.scitotenv.2023.162202] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/36775162]
21. Carella, F.; Seck, M.; Esposti, L.D.; Diadiou, H.; Maienza, A.; Baronti, S.; Vignaroli, P.; Vaccari, F.P.; Iafisco, M.; Adamiano, A. Thermal Conversion of Fish Bones into Fertilizers and Biostimulants for Plant Growth-A Low Tech Valorization Process for the Development of Circular Economy in Least Developed Countries. J. Environ. Chem. Eng.; 2021; 9, 104815. [DOI: https://dx.doi.org/10.1016/j.jece.2020.104815]
22. Radziemska, M.; Vaverková, M.D.; Adamcová, D.; Brtnický, M.; Mazur, Z. Valorization of Fish Waste Compost as a Fertilizer for Agricultural Use. Waste Biomass Valorization; 2019; 10, pp. 2537-2545. [DOI: https://dx.doi.org/10.1007/s12649-018-0288-8]
23. Ar, Y. The Disappearing Nutrient. Nature; 2009; 461, pp. 716-718.
24. Ozyhar, T.; Tschannen, C.; Thoemen, H.; Zoppe, J.O. Evaluating the Use of Calcium Hydrogen Phosphate Dihydrate as a Mineral-Based Fire Retardant for Application in Melamine-Urea-Formaldehyde (MUF)-Bonded Wood-Based Composite Materials. Fire Mater.; 2022; 46, pp. 595-604. [DOI: https://dx.doi.org/10.1002/fam.3009]
25. Sane, A.R.; Pham Minh, D.; Semlal, N.; Boulif, R.; Toussaint, C.; Germeau, A.; Nzihou, A. Clay/Phosphate-Based Ceramic Materials for Thermal Energy Storage—Part I: Effect of Synthetic Phosphate Content on Microstructure, Thermo-Physical and Thermo-Mechanical Properties. Open Ceram.; 2023; 14, 100346. [DOI: https://dx.doi.org/10.1016/j.oceram.2023.100346]
26. Nam, P.V.; Hoa, N.; Van,; Trung, T.S. Properties of Hydroxyapatites Prepared from Different Fish Bones: A Comparative Study. Ceram. Int.; 2019; 45, pp. 20141-20147. [DOI: https://dx.doi.org/10.1016/j.ceramint.2019.06.280]
27. Boutinguiza, M.; Pou, J.; Comesaña, R.; Lusquiños, F.; De Carlos, A.; León, B. Biological Hydroxyapatite Obtained from Fish Bones. Mater. Sci. Eng. C; 2012; 32, pp. 478-486. [DOI: https://dx.doi.org/10.1016/j.msec.2011.11.021]
28. Venkatesan, J.; Qian, Z.J.; Ryu, B.; Thomas, N.V.; Kim, S.K. A Comparative Study of Thermal Calcination and an Alkaline Hydrolysis Method in the Isolation of Hydroxyapatite from Thunnus obesus Bone. Biomed. Mater.; 2011; 6, 035003. [DOI: https://dx.doi.org/10.1088/1748-6041/6/3/035003]
29. Sousa, S.C.; Vázquez, J.A.; Pérez-Martín, R.I.; Carvalho, A.P.; Gomes, A.M. Valorization of By-Products from Commercial Fish Species: Extraction and Chemical Properties of Skin Gelatins. Molecules; 2017; 22, 1545. [DOI: https://dx.doi.org/10.3390/molecules22091545]
30. Wang, L.; An, X.; Yang, F.; Xin, Z.; Zhao, L.; Hu, Q. Isolation and Characterisation of Collagens from the Skin, Scale and Bone of Deep-Sea Redfish (Sebastes mentella). Food Chem.; 2008; 108, pp. 616-623. [DOI: https://dx.doi.org/10.1016/j.foodchem.2007.11.017] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26059140]
31. Szpak, P. Fish Bone Chemistry and Ultrastructure: Implications for Taphonomy and Stable Isotope Analysis. J. Archaeol. Sci.; 2011; 38, pp. 3358-3372. [DOI: https://dx.doi.org/10.1016/j.jas.2011.07.022]
32. Tabarestani, S.; Maghsoudlou, Y.; Motamedzadegan, A.; Mahoonak, S.; Rostamzad, H. Study on Some Properties of Acid-Soluble Collagens Isolated from Fish Skin and Bones of Rainbow Trout (Onchorhynchus mykiss). Int. Food Res. J.; 2012; 19, pp. 251-257.
33. Blanco, M.; Sotelo, C.G.; Pérez-Martín, R.I. New Strategy to Cope with Common Fishery Policy Landing Obligation: Collagen Extraction from Skins and Bones of Undersized Hake (Merluccius merluccius). Polymers; 2019; 11, 1485. [DOI: https://dx.doi.org/10.3390/polym11091485] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31514432]
34. Li, Z.R.; Wang, B.; Chi, C.F.; Zhang, Q.H.; Gong, Y.D.; Tang, J.J.; Luo, H.Y.; Ding, G.F. Isolation and Characterization of Acid Soluble Collagens and Pepsin Soluble Collagens from the Skin and Bone of Spanish Mackerel (Scomberomorous niphonius). Food Hydrocoll.; 2013; 31, pp. 103-113. [DOI: https://dx.doi.org/10.1016/j.foodhyd.2012.10.001]
35. Valcarcel, J.; Fraguas, J.; Hermida-Merino, C.; Hermida-Merino, D.; Piñeiro, M.M.; Vázquez, J.A. Production and Physicochemical Characterization of Gelatin and Collagen Hydrolysates from Turbot Skin Waste Generated by Aquaculture Activities. Mar. Drugs; 2021; 19, 491. [DOI: https://dx.doi.org/10.3390/md19090491] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/34564153]
36. Valcarcel, J.; Hermida-Merino, C.; Piñeiro, M.M.; Hermida-Merino, D.; Vázquez, J.A. Extraction and Characterization of Gelatin from Skin By-Products of Seabream, Seabass and Rainbow Trout Reared in Aquaculture. Int. J. Mol. Sci.; 2021; 22, 12104. [DOI: https://dx.doi.org/10.3390/ijms222212104]
37. Ruhdal, J.P.; Hammer, K. Minimal Requirements for Exponential Growth of Lactococcus lactis. Appl. Environ. Microbiol.; 1993; 59, pp. 4363-4366.
38. Hou, Y.; Yin, Y.; Wu, G. Dietary Essentiality of “Nutritionally Non-Essential Amino Acids” for Animals and Humans. Exp. Biol. Med.; 2015; 240, pp. 997-1007. [DOI: https://dx.doi.org/10.1177/1535370215587913] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26041391]
39. Hou, Y.; Wu, G. Nutritionally Essential Amino Acids. Adv. Nutr.; 2018; 9, pp. 849-851. [DOI: https://dx.doi.org/10.1093/advances/nmy054]
40. Vázquez, J.A.; Fernández-Compás, A.; Blanco, M.; Rodríguez-Amado, I.; Moreno, H.; Borderías, J.; Pérez-Martín, R.I. Development of Bioprocesses for the Integral Valorisation of Fish Discards. Biochem. Eng. J.; 2019; 144, pp. 198-208. [DOI: https://dx.doi.org/10.1016/j.bej.2019.02.004]
41. Vázquez, J.A.; Meduíña, A.; Durán, A.I.; Nogueira, M.; Fernández-Compás, A.; Pérez-Martín, R.I.; Rodríguez-Amado, I. Production of Valuable Compounds and Bioactive Metabolites from By-Products of Fish Discards Using Chemical Processing, Enzymatic Hydrolysis, and Bacterial Fermentation. Mar. Drugs; 2019; 17, 139. [DOI: https://dx.doi.org/10.3390/md17030139]
42. Aguiar, H.; Chiussi, S.; López-Álvarez, M.; González, P.; Serra, J. Structural Characterization of Bioceramics and Mineralized Tissues Based on Raman and XRD Techniques. Ceram. Int.; 2018; 44, pp. 495-504. [DOI: https://dx.doi.org/10.1016/j.ceramint.2017.09.203]
43. Hughes, J.M.; Cameron, M.; Crowley, K.D. Structural Variations in Natural F, OH, and Cl Apatites. Am. Mineral.; 1989; 74, pp. 870-876.
44. Hughes, J.M.; Jolliff, B.L.; Rakovan, J. The Crystal Chemistry of Whitlockite and Merrillite and the Dehydrogenation of Whitlockite to Merrillite. Am. Mineral.; 2008; 93, pp. 1300-1305. [DOI: https://dx.doi.org/10.2138/am.2008.2683]
45. Posset, U.; Löcklin, E.; Thull, R.; Kiefer, W. Vibrational Spectroscopic Study of Tetracalcium Phosphate in Pure Polycrystalline Form and as a Constituent of a Self-Setting Bone Cement. J. Biomed. Mater. Res.; 1998; 40, pp. 640-645. [DOI: https://dx.doi.org/10.1002/(SICI)1097-4636(19980615)40:4<640::AID-JBM16>3.0.CO;2-J]
46. Penel, G.; Delfosse, C.; Descamps, M.; Leroy, G. Composition of Bone and Apatitic Biomaterials as Revealed by Intravital Raman Microspectroscopy. Bone; 2005; 36, pp. 893-901. [DOI: https://dx.doi.org/10.1016/j.bone.2005.02.012] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15814305]
47. Corno, M.; Busco, C.; Civalleri, B.; Ugliengo, P. Periodic Ab Initio Study of Structural and Vibrational Features of Hexagonal Hydroxyapatite Ca10(PO4)6(OH)2. Phys. Chem. Chem. Phys.; 2006; 8, pp. 2464-2472. [DOI: https://dx.doi.org/10.1039/b602419j]
48. De Aza, P.N.; Guitiá, F.; Santos, C.; De Aza, S.; Cuscó, R.; Artú, L. Vibrational Properties of Calcium Phosphate Compounds. 2. Comparison between Hydroxyapatite and-Tricalcium Phosphate. Chem. Mater.; 1997; 9, pp. 916-922. [DOI: https://dx.doi.org/10.1021/cm9604266]
49. Kim, D.H.; Hwang, K.H.; Lee, J.D.; Park, H.C.; Yoon, S.Y. Long and Short Range Order Structural Analysis of In-Situ Formed Biphasic Calcium Phosphates. Biomater. Res.; 2015; 19, 14. [DOI: https://dx.doi.org/10.1186/s40824-015-0036-0]
50. AOAC. (Association of Official Analytical Chemistry). Methods of Analysis; 15th ed. AOAC: Washington, DC, USA, 1997.
51. Bligh, E.G.; Dyer, W.J. A Rapid Method of Total Lipid Extraction and Purification. Can. J. Biochem. Physiol.; 1959; 37, pp. 911-917. [DOI: https://dx.doi.org/10.1139/y59-099]
52. Moore, S.; Spackman, D.H.; Stein, W.H. Chromatography of Amino Acids on Sulfonated Polystyrene Resins an Improved System. Anal. Chem.; 1958; 30, pp. 1185-1190. [DOI: https://dx.doi.org/10.1021/ac60139a005]
53. Duta, L.; Dorcioman, G.; Grumezescu, V. A Review on Biphasic Calcium Phosphate Materials Derived from Fish Discards. Nanomaterials; 2021; 11, 2856. [DOI: https://dx.doi.org/10.3390/nano11112856]
54. Icono de Iconic Panda, from Freepik. Desechos Alimentarios. Available online: https://www.freepik.es/icono/desechos-alimentarios_14191536 (accessed on 3 October 2023).
55. Icono de Eucalyp from Freepik. Icono Matraz. Available online: https://www.freepik.es/icono/matraz_2637054#fromView=search&page=1&position=48&uuid=23fa991c-896b-414a-9cd6-3ef833682cd1 (accessed on 3 October 2023).
56. Icono de Eucalyp, from Frepik. Icono Lata Conserva Pescado. Available online: https://www.freepik.es/icono/pder_884662 (accessed on 3 October 2023).
57. Icono de Iconic Panda, from Freepik. Icono Estrategia. Available online: https://www.freepik.es/icono/estrategia_11296676 (accessed on 3 October 2023).
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Details
; Souto-Montero, Paula 2
; Durán, Salvador 3 ; Pérez-Davila, Sara 4 ; Vázquez, José Antonio 4
; González, Pío 1
; Serra, Julia 1 1 CINTECX, Universidade de Vigo, Grupo Novos Materiais, 36310 Vigo, Spain;
2 Departamento de I + D + i, Jealsa Foods S.A.U., Corporación Jealsa, Vimieiro, 20 Bajo, 15930 Boiro, Galicia, Spain;
3 Departamento de I + D + i, Jealsa Foods S.A.U., Corporación Jealsa, Vimieiro, 20 Bajo, 15930 Boiro, Galicia, Spain;
4 Grupo de Reciclado y Valorización de Materiales Residuales (REVAL), Instituto de Investigaciones Marinas (IIM-CSIC), C/Eduardo Cabello 6, 36208 Vigo, Spain;