Abstract
The aim of this study was to evaluate the nutritional composition and technological properties of meat from turkeys produced under organic conditions and compare them with those of turkeys produced under conventional conditions. Twenty carcasses of female B.U.T. Premium turkeys (Aviagen Turkeys) were obtained directly from the abattoir ten h after slaughter time of animals. Ten carcasses originated from female turkeys reared under conventional intensive husbandry conditions for meat-type turkeys (on average, 5611.8 ± 196.2 g of carcass weight) and the other ten carcasses corresponded to female turkeys raised under certified organic free-range conditions (PavosBio, Ávila, Spain) (on average, 5528.5 ± 354.4 g of carcass weight). Breast, thigh and wing meat samples were analyzed from each turkey: Chemical composition, fatty acid profile, free amino acids, mineral and vitamins content, color, and texture. Meat from female turkeys reared under organic conditions presented higher fat content in breast (1.90 vs. 1.01%, P = 0.032), thigh (3.79 vs. 2.68%, P = 0.022) and wing (12.0 vs. 8.91%, P = 0.012) than meat of female turkeys reared under intensive conventional conditions. The proportion of saturated fatty acids was higher in the meat of intensively reared female turkeys than in those reared under organic conditions (42.8 vs. 38.1%, P = 0.017 in breast; 38.8 vs. 33.6%, P = 0.0053 in thigh and 40.2 vs. 33.9%, P < 0.001 in wing). On the contrary, the proportion of monounsaturated fatty acids was higher in meat of organic turkeys (41.4 vs. 35.6%, P = 0.012 in breast; 42.3 vs. 35.6%, P < 0.001 in thigh and 46.9 vs. 39.3%, P = 0.011 in wing). Concentration of riboflavin and pyridoxine was higher by 21.1% (P = 0.010) and by 154% (P = 0.006), respectively, in meat from organically raised female turkeys than in that of female turkeys reared under intensive conditions. The organic turkey meat analyzed contained a higher proportion B2 and B6, lipids and monounsaturated fatty acids, and a lower content of omega-3 polyunsaturated fatty acids.
Key words: Turkey, meat quality, organic food, conventional food
INTRODUCTION
During the past decades, there has been a noteworthy increase in the global consumption of poultry meat (Yalcin et al., 2019). This rise is attributed to growing consumer demand for poultry products, particularly turkey meat, valued for its high protein concentration, low fat content, and role as a mineral source, including sodium, potassium, and iron. Additionally, it boasts appealing sensory attributes such as texture, color, and flavor (Castro et al., 2000; Food and Agriculture Organization (FAO), 2013; Marcon et al., 2018; Petracci et al. 2019; Freire et al., 2021). Indeed, a primary challenge confronting the poultry meat industry is the delivery of products that are tender, succulent, and characterized by appealing color and flavor (Marcon et al., 2018). As a result, turkey meat has risen to the second most popular choice among various poultry meats globally (Zampiga et al., 2020; Freire et al., 2021; Baéza et al., 2022; Kálmán and Szőllősi, 2022). Alongside the demand for turkey meat, consumers have elevated expectations regarding product quality. Speaking about meat quality typically involves considering a blend of organoleptic and biological indicators, which collectively determine its practical suitability in meeting human nutritional needs. The key attributes evaluated to ascertain the quality of turkey meat encompass its nutritional composition, color, and texture, all of which can be influenced by the rearing conditions of these birds (Yalcin et al., 2019; Vigar et al., 2020). The increase in demand for turkey meat has led to a diversification of consumer preferences, with greater attention paid to nutritional quality and sustainable production practices (Vigar et al., 2020; Kálmán and Szőllősi, 2022). In this context, turkey production, a popular source of poultry protein, has undergone significant evolution in terms of breeding methods, feeding, and living conditions (Vukasovič, 2014; Vigar et al., 2020). Fundamental differences between intensive and organic turkey production span from feeding and breeding practices to environmental conditions. These disparities raise significant questions and controversies regarding the nutritional quality of the resulting meat from each production system, including its protein, fat, vitamin, and mineral content (Castellini et al., 2002; Fanatico et al., 2005a; Werner et al., 2008; Cömert et al., 2016; Średnicka-Tober et al., 2016a; Hiscock et al., 2022), all crucial for human health and consumer preferences. However, there remains a significant gap in the scientific literature regarding the comparison of turkey meat quality between intensive and organic production systems, with no comprehensive studies addressing this issue to date. In this context, there arises a need to investigate and compare the nutritional composition of intensively and organically produced turkeys, aiming to provide robust scientific information on nutritional differences between the 2 production types.
At the core of this study lies the emerging concept of "locally sourced products," resonating with the growing consumer awareness of sustainability and preference for local products. Geographical proximity to the production site has become a critical criterion in food selection, and understanding how this choice relates to the nutritional composition of turkey meat is essential for addressing changing consumer expectations and needs.
In the European Union, organic livestock farming is overseen by EU Regulation 889/2008. This regulation includes provisions to ensure higher standards of animal welfare, such as providing more space and access to outdoor environments. Moreover, it requires that poultry must either be raised to a certain minimum age or be from breeds that grow slowly to prevent the use of intensive farming practices.
The aim of this study was to evaluate the nutritional composition, and technological properties of turkeys produced under organic conditions and compare them with those of turkeys produced under conventional conditions.
It is expected that the results of this research will contribute to improving understanding of the nutritional and environmental implications of different turkey production practices and provide a solid foundation for informed decision-making for both consumers and the poultry industry.
MATERIALS AND METHODS
Samples
To carry out this study, twenty carcasses of female B.U.T. Premium turkeys (Aviagen Turkeys) were obtained directly from the abattoir ten h after slaughter time of animals. Carcasses were subsequently stored at -20°C for 2 to 3 wk until cut up and analyzed. Ten carcasses originated from female turkeys reared under conventional intensive husbandry conditions for meat-type turkeys (on average, 5611.8 ± 196.2 g of carcass weight; liveweights from 7305 to 7838 g) and the other ten carcasses corresponded to female turkeys raised under certified organic free-range conditions (PavosBio, Ávila, Spain) (on average, 5528.5 ± 354.4 g of carcass weight; liveweights from 7001 to 7961 g). The nutrient composition of the finishing diet consumed by the turkeys was, respectively, 18.7 and 17.3% crude protein, 6.18 and 4.00% fat, 3.17 and 4.20% crude fiber, 5.16 and 6.70% ash, 1.12 and 1.30% lysine, 0.54 and 0.35% methionine, and 3124 and 3063 kcal/kg of metabolizable energy for intensively reared and organic turkeys. Therefore, the ratio metabolizable energy: crude protein amounted, respectively, to 16.7 and 17.7 kcal/g. Finally, the age of birds at slaughter was 95 and 110 d for intensively reared and organic turkeys, respectively.
All turkeys were processed from July 2023 to September 2023. After defrosting and carcass sectioning, breast, thigh and wing samples were stored at 4°C until the analyses were completed. The percentages of each meat sample in relation to carcass weight ranged from 16 to 18% in breast, 7 to 9% in thigh and 4 to 6% in wing. All visible skin and connective tissue were removed from breast and thigh samples.
Meat Composition
Chemical composition of breast, thigh and wing samples was determined in triplicate according to the AOAC methods (AOAC International, 2023). The moisture content (Method 950.46) was estimated by drying in an air oven at 100 to 105 °С until a constant weight was achieved. The fat content was measured by Soxhlet method (Method 960.39) with 10 g of sample and 85 mL of petroleum ether as extraction solvent during 4 h of extraction. The crude protein content (Method 955.04) was analyzed by titrimetric method using a Kjeldahl distillation (Büchi Distillation Unit K-355, BUCHI Ibérica S.L.U., Barcelona, Spain) after digestion of 2 g of sample with sulfuric acid and selenium as catalyst (N x 6.25).
The pH value was measured in triplicate for samples of breast, thigh and wing meat. A pH meter equipped with a probe for inside sample measurements was used (pH Sensor InLab Solids Go-ISM Mettler-Toledo, Barcelona, Spain). The calibrated probe was inserted for about 30 sec until the reading stabilized.
Fatty Acid Profile
The fatty acids profile of breast, thigh and wing fat samples (previously obtained by Soxhlet analysis) were quantitatively determined by triplicate using the COI method (International Olive Council, 2017) with some modifications. According to this method, the fatty acid methyl esters (FAME) were firstly prepared (50 mg of sample + 2 mL of heptane + 0.25 mL of the methanolic potassium hydroxide solution) and then analyzed by gas chromatography using a gas chromatograph (Agilent 8860 GC System, Agilent Technologies, Santa Clara, CA) equipped with a flame ionization detector (FID). A SP-2340 (Sigma Aldrich, St. Louis, MO) capillary column (60m x 0.32mmID, df 0.20μm) and helium as a carrier gas were used. The injector temperature was 250°C, the detector temperature was 250°C and the oven temperature was as follow: 165°C (8 min) to 210°C at 2°C/min. The content of a detected FAME, as a percentage by mass, was determined by the area of the corresponding peak relative to the sum of the areas of all the peaks.
Free Amino Acid Analysis
Free amino acids profile of breast, thigh and wing meat samples were quantitatively determined by UFLC coupled with a fluorescence detector (Shimadzu, Kyoto, Japan) followed the method described by Antoine et al. (Antoine et al., 1999). Mobile phase A was 80:19:1 of 0.05 M sodium phosphate buffer (pH 5.5), methanol, and tetrahydrofuran. Mobile phase B was composed of 80:20 of methanol and 0.05 M sodium phosphate buffer (pH 5.5). The flow rate was 1.5 mL/min with a gradient of 0 to 15% B in 7 min, 15 to 50% B in 12 min, and 50 to 100% B in 25 min, and injection volume was 50 µL. The column used was a SUPELCOSIL LC-18 4.6 mm x 150 mm, 5µm. Previously, 2.5 g of sample was derivatized with methanol and ortho-phthalaldehyde (OPA) (Antoine et al., 1999). To adjust retention times and identify peaks, commercial standards were inserted. The standards allow integration of the area of each peak which is directly proportional to the amino acid concentration.
Minerals Composition
The content of Fe, K, Mg, P, Se and Zn in breast, thigh and wing meat samples were determined by inductively coupled plasma optical emission spectrometer (ICP-OES Avio 220 Max, PerkinElmer, Waltham, MA) after digestion of the samples in a DKL 12 Automatic Digestion Unit (VELP Scientifica, Usmate Velate MB, Italy) followed a method based on Macedo et al. (2022). For this purpose, 0.2 g of dried meat was weighed in digestion vessels, and 3.0 mL of purified HNO3 + 3.0 mL of H2O + 2.0 mL of 30% wt H2O2 solution were added. After digestion, the samples were diluted up to 25 mL for Mg, K and P, 0,5 mL of the previous dilution was further diluted to 25 mL due to exceeding the detection limit of the equipment. Analytical blanks were prepared similarly, without the addition of samples into the digestion vessels. Argon and synthetic air were used for instrument gas supply and nitrogen as auxiliary gas.
Quantitative Determination of Vitamins
The content of vitamin B3 (Niacin), B6 (Pyridoxin), B2 (Riboflavin) and B12 (Cyano-cobalamin) in breast meat samples were analyzed by using a microbiological method. A microtiter plate test VitaFast (ifp Institut für Produktqualität GmbH, Berlin, Germany) was used for each vitamin. Each vitamin was extracted from 1 g of sample. The assay medium and the diluted extract were pipetted into the wells coated with a specific microorganism. The growth of it is dependent on the supply of the vitamin. The microorganism growth in relation to the extracted vitamin was measured as turbidity and compared to a standard curve. The measurement was done using a microtiter plate reader at 630 nm.
Color
Trichromatic coordinates (L*, a*, b*) of breast, thigh and wing meat samples were obtained by using a CR-5 colorimeter (Konica Minolta, Osaka, Japan). For measurements, a D65, 10° illuminant with a 30 mm port size was chosen. The average of 3 random readings at different locations, avoiding fat and visible connective tissue, was used to measure lightness (L*), redness (a*), and yellowness (b*). Calibration was per-formed using a white standard and light trap before testing.
Texture Analysis
Thawed raw breast sample was cut into 2 cm x 2 cm cubes for hardness and shear force analysis. Both assessments were done by triplicate using a TA-XT Plus Texture Analyzer (TA-XT Plus with Exponent Connect version 8.0.0.11 software, Stable Micro System, Godalming, Surrey, UK). For shear force analysis, v-shaped cutting probe was used, and for hardness analysis, 2 compression tests were performed in TPA mode under a cylindrical probe with a diameter of 50 mm (Part Code P/50). The test speed was 2 mm/s before the test, 1 mm/s during the test, and 10 mm/s after the test. The compression degree was 50%, and the compression holding time was 5 s.
Statistical Analysis
Data of variables were subjected to a 1-way analysis of variance (ANOVA) with turkey husbandry conditions as the main source of variation by using the general linear model procedure (Version 9.4, SAS Institute Inc., Cary, NC). Main treatment effect was declared significant at P < 0.05.
The following parameters were measured in breast, thigh and wing: pH, moisture, crude protein, fat, fatty acid profile, amino acid concentration, mineral concentration and color. Vitamin content and texture parameters were only determined in breast. In each case, measurements were done on 3 replicates and then, these 3 determinations were averaged. The turkey carcass represented the experimental unit for all the traits assessed.
RESULTS
Chemical Composition of Organic vs. Conventional Turkey Meat
The chemical composition of the analyzed turkey meat is shown in Table 1. Meat from female turkeys reared under organic conditions presented higher fat content in breast (88.1% higher, P = 0.032), thigh (41.4% higher, P = 0.022) and wing (34.7% higher, P = 0.012) than meat of female turkeys reared under intensive conventional conditions. No significant differences due to type of farming were detected for moisture content (on average, 74.6% in breast, 75.8% in thigh and 67.0% in wing), crude protein content (on average, 16.2% in breast, 14.1% in thigh and 15.3% in wing) or pH value (on average, 5.91 in breast, 6.07 in thigh and 6.09 in wing) in turkey meat.
Table 1.
Meat chemical composition of female B.U.T.
| Turkey husbandry conditions |
||||
|---|---|---|---|---|
| Conventional | Organic | SEM1 | P-value | |
| Breast | ||||
| pH | 5.95 | 5.87 | 0.035 | 0.15 |
| Moisture (%) | 73.8 | 75.5 | 0.696 | 0.12 |
| Crude protein (%) | 16.5 | 16.0 | 0.559 | 0.63 |
| Fat (%) | 1.01 | 1.90 | 0.241 | 0.032 |
| Thigh | ||||
| pH | 6.03 | 6.11 | 0.081 | 0.50 |
| Moisture (%) | 75.9 | 75.8 | 0.568 | 0.92 |
| Crude protein (%) | 14.1 | 14.1 | 0.546 | 0.99 |
| Fat (%) | 2.68 | 3.79 | 0.278 | 0.022 |
| Wing with skin | ||||
| pH | 6.09 | 6.09 | 0.022 | 0.93 |
| Moisture (%) | 67.7 | 66.4 | 0.519 | 0.10 |
| Crude protein (%) | 15.2 | 15.4 | 0.777 | 0.83 |
| Fat (%) | 8.91 | 12.0 | 0.689 | 0.012 |
Abbreviation: SEM, standard error of the mean.
n = 10 females per husbandry type (3 samples collected in each case per turkey).
Premium turkeys reared under conventional or organic conditions.
Lipid Profile of Organic vs. Conventional Turkey Meat
The fatty acid profile in turkeys’ meat is reported in Table 2 (breast), Table 3 (thigh) and Table 4 (wing). In breast, thigh and wing, the proportion of saturated fatty acids was higher in the meat of intensively reared female turkeys than in those reared under organic conditions (12.3% higher, P = 0.017 in breast; 15.5% higher, P = 0.0053 in thigh and 18.6% higher, P < 0.001 in wing). This was partly due to the higher content in palmitic acid in the meat of intensively reared turkeys (29.3 vs. 26.5%, P = 0.0030 in breast; 28.8 vs. 25.8%, P = 0.0042 in thigh and 32.2 vs. 26.1%, P < 0.001 in wing). On the contrary, the proportion of monounsaturated fatty acids was higher in meat of organic turkeys (16.3% higher, P = 0.012 in breast; 18.8% higher, P < 0.001 in thigh and 19.3% higher, P = 0.011 in wing). As regards the proportion of polyunsaturated fatty acids in meat, no significant differences were observed (on average, 21.0% in breast, 24.8% in thigh and 19.8% in wing). However, the proportion of ω-3 fatty acids was higher (37.5% higher, P = 0.028 in thigh and 41.1% higher, P = 0.012 in wing) and the ratio ω-6/ω-3 was lower (22.6% lower, P = 0.036 in thigh and 25.4% lower, P = 0.0035 in wing) in intensively reared turkeys than in organic ones, mainly due to the higher proportion of linolenic acid in the meat of intensively reared turkeys (1.84 vs. 1.32%, P = 0.019 in thigh and 1.51 vs. 1.07%, P = 0.012 in wing).
Table 2.
Fatty acid composition (% of total fatty acids) of breast meat from female B.U.T.
| Turkey husbandry conditions |
SEM1 | P-value | ||
|---|---|---|---|---|
| Conventional | Organic | |||
| C4:0 | 4.50 | 4.27 | 0.708 | 0.83 |
| C14:0 | 0.375 | 0.404 | 0.021 | 0.39 |
| C14:1 | 0.0 | 0.071 | 0.028 | 0.11 |
| C15:0 | 0.0 | 0.026 | 0.010 | 0.13 |
| C16:0 | 29.3 | 26.5 | 0.427 | 0.0030 |
| C16:1 | 4.28 | 8.15 | 0.363 | < 0.001 |
| C17:0 | 0.0 | 0.010 | 0.006 | 0.32 |
| C17:1 | 0.0 | 0.022 | 0.012 | 0.27 |
| C18:0 | 8.57 | 6.82 | 0.263 | 0.012 |
| C18:1 | 30.6 | 33.0 | 0.826 | 0.10 |
| C18:2 | 20.4 | 18.9 | 0.552 | 0.11 |
| C18:3 | 0.965 | 0.951 | 0.106 | 0.93 |
| C20:0 | 0.015 | 0.016 | 0.015 | 0.96 |
| C20:1 | 0.0 | 0.065 | 0.049 | 0.41 |
| C20:3 | 0.493 | 0.573 | 0.157 | 0.74 |
| C20:4 | 0.0 | 0.005 | 0.004 | 0.41 |
| C20:5 | 0.001 | 0.0 | 0.0006 | 0.29 |
| C22:1 | 0.042 | 0.037 | 0.037 | 0.93 |
| C22:4 | 0.266 | 0.047 | 0.160 | 0.39 |
| C22:6 | 0.0 | 0.002 | 0.002 | 0.41 |
| C24:1 | 0.193 | 0.131 | 0.036 | 0.29 |
| Saturated fatty acids | 42.8 | 38.1 | 0.922 | 0.017 |
| Monounsaturated fatty acids | 35.6 | 41.4 | 1.12 | 0.012 |
| Polyunsaturated fatty acids | 21.6 | 20.5 | 0.647 | 0.27 |
| ω-6 fatty acids | 21.1 | 19.5 | 0.639 | 0.27 |
| ω-3 fatty acids | 0.967 | 0.953 | 0.106 | 0.93 |
| Ratio ω-6/ω-3 | 22.1 | 20.6 | 1.79 | 0.61 |
Abbreviation: SEM, standard error of the mean.
n = 10 females per husbandry type (3 samples collected in each case per turkey).
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Table 3.
Fatty acid composition (% of total fatty acids) of thigh meat from female B.U.T.
| Turkey husbandry conditions |
||||
|---|---|---|---|---|
| Conventional | Organic | SEM1 | P-value | |
| C4:0 | 1.88 | 1.70 | 0.504 | 0.77 |
| C14:0 | 0.680 | 0.569 | 0.030 | 0.030 |
| C14:1 | 0.056 | 0.084 | 0.024 | 0.42 |
| C15:0 | 0.046 | 0.051 | 0.012 | 0.75 |
| C16:0 | 28.8 | 25.8 | 0.495 | 0.0042 |
| C16:1 | 5.86 | 8.66 | 0.488 | 0.0036 |
| C17:0 | 0.016 | 0.027 | 0.0066 | 0.28 |
| C17:1 | 0.0 | 0.025 | 0.0074 | 0.046 |
| C18:0 | 7.26 | 7.33 | 0.282 | 0.87 |
| C18:1 | 29.3 | 31.0 | 0.688 | 0.13 |
| C18:2 | 21.2 | 21.1 | 0.510 | 0.86 |
| C18:3 | 1.84 | 1.32 | 0.113 | 0.019 |
| C20:0 | 0.013 | 0.036 | 0.012 | 0.21 |
| C20:1 | 0.119 | 0.143 | 0.065 | 0.49 |
| C20:3 | 1.75 | 1.14 | 0.369 | 0.28 |
| C20:4 | 0.056 | 0.060 | 0.018 | 0.86 |
| C20:5 | 0.003 | 0.009 | 0.0061 | 0.49 |
| C22:1 | 0.116 | 0.095 | 0.033 | 0.62 |
| C22:4 | 0.583 | 0.603 | 0.237 | 0.94 |
| C22:6 | 0.026 | 0.026 | 0.015 | 0.99 |
| C24:1 | 0.396 | 0.222 | 0.067 | 0.10 |
| Saturated fatty acids | 38.8 | 33.6 | 0.929 | 0.0053 |
| Monounsaturated fatty acids | 35.6 | 42.3 | 0.694 | < 0.001 |
| Polyunsaturated fatty acids | 25.6 | 24.1 | 0.835 | 0.29 |
| ω-6 fatty acids | 23.8 | 22.9 | 0.638 | 0.20 |
| ω-3 fatty acids | 1.87 | 1.36 | 0.121 | 0.028 |
| Ratio ω-6/ω-3 | 13.0 | 16.8 | 1.19 | 0.036 |
Abbreviation: SEM, standard error of the mean.
n = 10 females per husbandry type (3 samples collected in each case per turkey).
Premium turkeys reared under conventional or organic conditions.
Table 4.
Fatty acid composition (% of total fatty acids) of wing meat plus skin from female B.U.T.
| Turkey husbandry conditions |
||||
|---|---|---|---|---|
| Conventional | Organic | SEM1 | P-value | |
| C4:0 | 1.56 | 1.59 | 0.128 | 0.89 |
| C14:0 | 0.788 | 0.558 | 0.017 | <0.001 |
| C14:1 | 0.176 | 0.157 | 0.021 | 0.56 |
| C15:0 | 0.082 | 0.116 | 0.028 | 0.40 |
| C16:0 | 32.2 | 26.1 | 0.686 | <0.001 |
| C16:1 | 8.01 | 10.2 | 0.567 | 0.027 |
| C17:0 | 0.063 | 0.024 | 0.019 | 0.22 |
| C17:1 | 0.044 | 0.053 | 0.012 | 0.65 |
| C18:0 | 5.50 | 5.46 | 0.289 | 0.79 |
| C18:1 | 31.1 | 36.3 | 1.40 | 0.031 |
| C18:2 | 18.4 | 17.8 | 1.13 | 0.60 |
| C18:3 | 1.51 | 1.07 | 0.097 | 0.012 |
| C20:0 | 0.036 | 0.048 | 0.010 | 0.46 |
| C20:1 | 0.140 | 0.197 | 0.027 | 0.38 |
| C20:3 | 0.168 | 0.113 | 0.034 | 0.31 |
| C20:4 | 0.025 | 0.034 | 0.0093 | 0.53 |
| C22:1 | 0.036 | 0.050 | 0.017 | 0.63 |
| C22:4 | 0.091 | 0.061 | 0.037 | 0.68 |
| C24:1 | 0.071 | 0.069 | 0.037 | 0.96 |
| Saturated fatty acids | 40.2 | 33.9 | 0.783 | <0.001 |
| Monounsaturated fatty acids | 39.3 | 46.9 | 1.64 | 0.011 |
| Polyunsaturated fatty acids | 20.5 | 19.2 | 1.24 | 0.38 |
| ω-6 fatty acids | 18.9 | 18.0 | 1.16 | 0.49 |
| ω-3 fatty acids | 1.51 | 1.07 | 0.097 | 0.012 |
| Ratio ω-6/ω-3 | 12.6 | 16.9 | 0.796 | 0.0035 |
Abbreviation: SEM, standard error of the mean.
n = 10 females per husbandry type (3 samples collected in each case per turkey).
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Free Amino Acid Composition of Organic vs. Conventional Turkey Meat
Tables 5, 6 and 7 report the free amino acid composition in breast, thigh and wing, respectively. No significant differences were found between intensive and organic husbandry conditions for the meat content in any of the amino acids studied.
Table 5.
Free amino acid content (mg/100 g) of breast meat from female B.U.T.
| Turkey husbandry conditions |
||||
|---|---|---|---|---|
| Conventional | Organic | SEM1 | P-value | |
| Aspartate | 0.300 | 0.272 | 0.040 | 0.64 |
| Glutamate | 0.870 | 0.747 | 0.103 | 0.42 |
| Serine | 0.420 | 0.392 | 0.082 | 0.81 |
| Histidine | 3.25 | 1.96 | 0.761 | 0.26 |
| Glycine | 0.594 | 0.706 | 0.118 | 0.52 |
| Thymine | 0.701 | 0.591 | 0.105 | 0.48 |
| Alanine | 0.617 | 0.508 | 0.094 | 0.44 |
| Arginine | 1.59 | 1.72 | 0.158 | 0.58 |
| Tyrosine | 1.63 | 1.25 | 0.141 | 0.12 |
| Cysteine | 1.21 | 1.43 | 0.569 | 0.82 |
| Valine | 0.331 | 0.273 | 0.032 | 0.23 |
| Methionine | 0.434 | 0.338 | 0.037 | 0.10 |
| Phenylalanine | 0.346 | 0.277 | 0.036 | 0.21 |
| Isoleucine | 0.256 | 0.211 | 0.019 | 0.13 |
| Leucine | 0.472 | 0.349 | 0.043 | 0.079 |
| Lysine | 0.702 | 0.578 | 0.065 | 0.21 |
| Proline | 1.43 | 0.926 | 0.541 | 0.53 |
Abbreviation: SEM, standard error of the mean.
n = 10 females per husbandry type (3 samples collected in each case per turkey).
Premium turkeys reared under conventional or organic conditions.
Table 6.
Free amino acid content (mg/100 g) of thigh meat from female B.U.T.
| Turkey husbandry conditions |
||||
|---|---|---|---|---|
| Conventional | Organic | SEM1 | P-value | |
| Aspartate | 0.418 | 0.351 | 0.054 | 0.40 |
| Glutamate | 1.16 | 1.13 | 0.112 | 0.87 |
| Serine | 1.48 | 1.32 | 0.171 | 0.53 |
| Histidine | 1.45 | 1.81 | 0.355 | 0.50 |
| Glycine | 0.421 | 0.579 | 0.158 | 0.50 |
| Thymine | 1.02 | 1.05 | 0.173 | 0.90 |
| Alanine | 0.597 | 0.539 | 0.063 | 0.54 |
| Arginine | 15.5 | 14.9 | 0.981 | 0.70 |
| Tyrosine | 2.43 | 2.34 | 0.233 | 0.81 |
| Cysteine | 1.96 | 1.31 | 0.465 | 0.35 |
| Valine | 0.380 | 0.375 | 0.057 | 0.96 |
| Methionine | 0.436 | 0.422 | 0.058 | 0.87 |
| Phenylalanine | 0.273 | 0.269 | 0.028 | 0.92 |
| Isoleucine | 0.242 | 0.234 | 0.031 | 0.86 |
| Leucine | 0.414 | 0.395 | 0.050 | 0.80 |
| Lysine | 0.656 | 0.637 | 0.089 | 0.88 |
| Proline | 1.68 | 1.30 | 0.709 | 0.76 |
Abbreviation: SEM, standard error of the mean.
n = 10 females per husbandry type (3 samples collected in each case per turkey).
Premium turkeys reared under conventional or organic conditions.
Table 7.
Free amino acid content (mg/100 g) of wing meat plus skin from female B.U.T.
| Turkey husbandry conditions |
||||
|---|---|---|---|---|
| Conventional | Organic | SEM1 | P-value | |
| Aspartate | 0.344 | 0.338 | 0.047 | 0.93 |
| Glutamate | 1.01 | 0.989 | 0.099 | 0.86 |
| Serine | 0.982 | 0.952 | 0.105 | 0.85 |
| Histidine | 1.75 | 1.84 | 0.241 | 0.79 |
| Glycine | 0.453 | 0.604 | 0.127 | 0.42 |
| Thymine | 0.672 | 0.642 | 0.080 | 0.80 |
| Alanine | 0.566 | 0.517 | 0.059 | 0.62 |
| Arginine | 3.16 | 3.52 | 0.464 | 0.60 |
| Tyrosine | 1.73 | 1.46 | 0.206 | 0.38 |
| Cysteine | 0.926 | 0.991 | 0.276 | 0.89 |
| Valine | 0.348 | 0.334 | 0.034 | 0.78 |
| Methionine | 0.473 | 0.456 | 0.040 | 0.78 |
| Phenylalanine | 0.310 | 0.284 | 0.020 | 0.38 |
| Isoleucine | 0.265 | 0.252 | 0.024 | 0.72 |
| Leucine | 0.464 | 0.436 | 0.038 | 0.61 |
| Lysine | 0.682 | 0.680 | 0.066 | 0.98 |
| Proline | 1.24 | 1.11 | 0.672 | 0.90 |
Abbreviation: SEM, standard error of the mean.
n = 10 females per husbandry type (3 samples collected in each case per turkey).
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Minerals and Vitamins Composition of Organic vs. Conventional Turkey Meat
Results on mineral concentration in turkey meat are provided in Table 8. Nor in breast, thigh or wing, did the concentration of iron, zinc, selenium, potassium, magnesium and phosphorus differ significantly between the 2 types of rearing conditions of turkeys.
Table 8.
Mineral content (mg/100 g) of meat from female B.U.T.
| Turkey husbandry conditions |
||||
|---|---|---|---|---|
| Conventional | Organic | SEM1 | P-value | |
| Breast | ||||
| Iron | 11.8 | 13.2 | 5.93 | 0.89 |
| Zinc | 38.6 | 48.1 | 8.30 | 0.61 |
| Selenium | 35.8 | 43.3 | 6.98 | 0.47 |
| Potassium | 13,048 | 14285 | 2,244 | 0.74 |
| Magnesium | 1,245 | 1280 | 137 | 0.86 |
| Phosphorus | 8,861 | 9245 | 1,105 | 0.81 |
| Thigh | ||||
| Iron | 29.3 | 31.1 | 8.14 | 0.88 |
| Zinc | 115 | 144 | 16.1 | 0.27 |
| Selenium | 35.5 | 38.1 | 2.65 | 0.50 |
| Potassium | 13,442 | 10,465 | 2,892 | 0.51 |
| Magnesium | 1,152 | 1,121 | 163 | 0.89 |
| Phosphorus | 8,685 | 8,417 | 1,177 | 0.88 |
| Wing with skin | ||||
| Iron | 20.2 | 25.7 | 5.56 | 0.50 |
| Zinc | 76.2 | 89.3 | 18.1 | 0.66 |
| Selenium | 32.4 | 36.5 | 2.16 | 0.22 |
| Potassium | 9,366 | 9510 | 1,768 | 0.96 |
| Magnesium | 818 | 880 | 115 | 0.71 |
| Phosphorus | 6,355 | 6,615 | 815 | 0.83 |
Abbreviation: SEM, standard error of the mean.
n = 10 females per husbandry type (3 samples collected in each case per turkey).
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The vitamin content in breast meat is shown in Table 9. Concentration of riboflavin and pyridoxine was higher by 21.1% (P = 0.010) and by 154% (P = 0.006), respectively, in meat from organically vs. raised female turkeys than in that of female turkeys reared under intensive conditions. No significant differences were detected for breast content in niacin or cyanocobalamin.
Table 9.
Vitamin content (mg/100 g) of breast meat from female B.U.T.
| Turkey husbandry conditions |
||||
|---|---|---|---|---|
| Conventional | Organic | SEM1 | P-value | |
| Riboflavin (mg/100 g) | 14.7 | 17.8 | 0.633 | 0.010 |
| Niacin (mg/100 g) | 10.4 | 8.34 | 0.832 | 0.14 |
| Pyridoxine (mg/100 g) | 0.558 | 1.42 | 0.163 | 0.006 |
| Cyanocobalamin (μg/100 g) | 1.67 | 1.43 | 0.467 | 0.74 |
Abbreviation: SEM, standard error of the mean.
n = 10 females per husbandry type (3 samples collected in each case per turkey).
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Color and Texture of Organic vs. Conventional Turkey Meat
Concerning meat color (Table 10), no significant differences were observed in both types of meat. Based on the CIELAB color space, average values for lightness (L*), redness tendency (a*) and yellowness (b*) were 55.7, 48.1 and 61.8, 9.30, 13.1 and 9.19, and 18.5, 18.7 and 17.8 in breast, thigh and wing, respectively.
Table 10.
Meat color in female B.U.T.
| Turkey husbandry conditions |
||||
|---|---|---|---|---|
| Conventional | Organic | SEM1 | P-value | |
| Breast | ||||
| Lightness, L* | 54.1 | 57.4 | 1.87 | 0.24 |
| Redness, a* | 9.32 | 9.29 | 0.666 | 0.98 |
| Yellowness, b* | 18.4 | 18.7 | 0.600 | 0.74 |
| Thigh | ||||
| Lightness, L* | 47.5 | 48.8 | 2.26 | 0.70 |
| Redness, a* | 13.1 | 13.1 | 0.863 | 1.00 |
| Yellowness, b* | 18.5 | 19.0 | 1.33 | 0.81 |
| Wing with skin | ||||
| Lightness, L* | 60.9 | 62.7 | 1.30 | 0.35 |
| Redness, a* | 9.83 | 8.56 | 0.633 | 0.20 |
| Yellowness, b* | 18.3 | 17.3 | 0.482 | 0.20 |
Abbreviation: SEM, standard error of the mean.
n = 10 females per husbandry type (3 samples collected in each case per turkey).
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Results on breast texture parameters are shown in Table 11. Neither hardness (on average, 0.087 N) nor shear force (on average, 58.5 N) differed significantly between the 2 types of turkey husbandry.
Table 11.
Texture parameters in breast meat from female B.U.T.
| Turkey husbandry conditions |
||||
|---|---|---|---|---|
| Conventional | Organic | SEM1 | P-value | |
| Hardness (N) | 0.088 | 0.087 | 0.0016 | 0.80 |
| Shear force (N) | 57.6 | 59.5 | 4.78 | 0.79 |
Abbreviation: SEM, standard error of the mean.
n = 10 females per husbandry type (3 samples collected in each case per turkey).
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DISCUSSION
In the present study, it was hypothesized that there are differences in the nutritional composition and technological properties between turkey meat raised under organic conditions and conventional turkey meat, which determine the quality of the different cuts analyzed (breast, thigh and wing).
No significant differences were observed between the 2 groups in terms of the main quality traits measured in this study. This observation could be explained by the fact that the guans of both groups were genetically the same, together with the fact that the weight at the time of slaughter was similar in the 2 groups, since, although the age of slaughter of organic guans (110 d) was higher than that of intensive guans (95 d), the former take longer to reach the same weight as intensive guans, because they exercise more due to the possibility of access to the outdoors.
Many factors determine the quality of poultry products, including functional properties and nutrient content, which can be affected by genotype, age, sex, and production system, as well as others, including environmental conditions up to the time of slaughter, diet, and stocking density, or their interactions (Owens et al., 2000; Castellini et al., 2002; Karacay et al., 2008). Sarica et al. (2011) evaluated the factors affecting the meat quality of 3 turkey genotypes raised with or without outdoor access (breast and thigh), which were provided with the same start, growth and end feed. It was observed that the housing system did not affect the pH, capacity to retain water and color in any of the parts analyzed, although there was a significant genotype x age interaction for the pH and redness values (a*) of the breast meat and for the pH value of the thigh meat. In addition, the genotype x sex interaction for the value of thigh meat moisture was also significant. No significant interactions were found between genotype and housing system, but there were significant interactions between the latter and other factors such as age and sex, which may indicate that the impact of outdoor access on quality parameters could vary depending on genotype, age and sex.
The significant differences observed were in relation to lipid content, fatty acid composition, and vitamin B2 and B6 content.
Organic turkey meat had a higher fat content than conventional turkey meat. These results may be surprising, as organic turkeys have access to an outdoor space and can therefore get more exercise than conventional turkeys. A possible hypothesis that would explain these facts is a higher energy/protein ratio of the finishing diet in organic turkeys (metabolizable energy ratio:crude protein = 16.7 kcal/g intensively farmed Turkeys vs. 17.7 kcal/g organically farmed turkeys) or a lack of methionine (0.54% intensively farmed turkeys vs. 0.35% organically farmed turkeys) that induced increased energy deposition in the muscles. On the other hand, in poultry, higher lipid synthesis correlates with higher synthesis of monounsaturated fatty acids, particularly palmitoleic acid (C16:1), the content of which was significantly higher in organic turkey meat than in conventional turkey.
On the other hand, although the organically produced turkeys had access to the outdoors, since the study was carried out in summer, exposure to high temperatures may also have influenced the results. Temperature fluctuations can lead to changes in carcass quality. Thus, heat can increase abdominal fat, while when temperatures are cold, less fat is deposited (Fanático et al. 2005b).
Omega-3 polyunsaturated fatty acids (n-3 PUFAs), such as docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA) were expected to be higher in the meat of turkeys that were raised in organic conditions, since with this type of breeding turkeys can obtain α-linolenic acid (ALA), which is a precursor to n-3 PUFAs, as reported in other studies conducted on poultry meat (Sosnówska-Czajka et al., 2017; Gálvez et al., 2020; Molee et al., 2022). However, the organic turkey meat tested in our study did not meet these forecasts. These contradictory results that we have obtained in the profiles of fatty acids have already been reported in other studies (Küçükyilmaz et al., 2012).
The results of Husak et al. (2008) agree with those of our study regarding monounsaturated fatty acids, but not regarding total saturated, total polyunsaturated, n-3 and n-6 fatty acids. The difference in fatty acid content is probably due to the intake of fatty acids in the diet, since the scientific literature reflects a clear relationship between the fat in the bird's diet and the fat deposited in the carcass (Gálvez et al., 2020). In the case of chickens, some authors conclude that the main reason that can explain the difference between organic and conventional farming may be the former's access to grass and other organic matter in the air (Castellini et al., 2002). This could also have been the reason for the differences observed in our study, since both types of birds received feed that mainly contained corn meal and soybean meal, although the feed used in the organic turkeys came from organic farming. On the other hand, the energy and protein content of the diet of organic turkeys was lower than that of conventional turkeys (18.7 and 17.3 g of protein, respectively; 3124 and 3036 kcal/kg of metabolizable energy, respectively); In addition, the methionine content of the diet of organic turkeys was also lower. These aspects have been able to induce a stimulation of lipid synthesis and deposition in peripheral tissues (muscle and adipose tissue), as the organic diet was not supplemented with chemical lysine and methionine.
If we analyze the published studies on the lipid profile of other types of organic vs. conventional meat, the results of a meta-analysis carried out by Średnicka-Tober et al. (2016a), whose main objective was to compare the nutrient content of different types of meat (beef, lamb, goat, pork, rabbit and chicken), organic and conventional, suggest that some organic meats (beef, lamb and pork) have higher concentrations of total polyunsaturated fatty acids and n-3 PUFAs. Results for these fatty acids varied between individual studies and studies conducted in different countries or regions. It is important to note that the heterogeneity shown by this metanalysis was high, probably due to differences between animal species and meat types. In the turkey meat analyzed in our study, the results differ from those obtained in the afore mentioned metanalysis, since in terms of the proportion of polyunsaturated fatty acids, no significant differences were found between both types, while the content of n-3 PUFAs, varied not only depending on the type of breeding, but also depending on the cut analyzed. In a study published by Ribas-Agustí et al. (2019), researchers compared the nutritional composition of organic and conventional beef sold at retail. The results shown agree with those obtained in our study for turkey meat in terms of palmitic acid, which was detected in a higher percentage in conventional meat than in organic meat, and total polyunsaturated fatty acids, for which no significant differences were found in either of the 2 studies. However, the percentage of monounsaturated fatty acids observed in the study by Ribas-Agustí et al. (2019) was lower in organic beef, while in our study a higher percentage for these fatty acids was found in all the parts analyzed in the organic turkeys. Finally, regarding n-3 PUFAs, Ribas-Agustí et al. (2019) reported a higher percentage of α-linolenic acid in organic beef, while in our study the percentage of this fatty acid was significantly higher in thigh and wing of conventional turkeys. Bjorklund et al. (2014) conducted a study comparing meat (loin) from organic and conventional dairy steers, randomly assigning male calves to 1 of 3 replicate groups: conventional, organic (grass + concentrate), or organic grass-fed only. The authors observed that grass-fed steers had lower monounsaturated fat content than organic and conventional steers (21.9%, 42.1% and 40.4%, respectively). In the organic turkey meat analyzed in our study, which was raised on pasture and ate feed intended for meat turkeys produced organically, percentages of monounsaturated fat like those obtained in the afore mentioned study were obtained, especially in the thigh (41.4% in breast; 42.3% in thigh and 46.9 % in wing). The same occurs with the ω-6/ω-3 ratio (12.9% in organic meat from dairy steers vs. 13.0% in thigh and 12.6 in wing of organic turkey meat).
Regarding protein content and moisture content, in our study, slightly higher protein percentages were observed in the breast and wing of organic turkeys compared to conventional ones, but these differences were not significant, while the moisture content was similar for both types of rearing. Husak et al. (2008) found significantly higher percentages of protein and lower percentages of moisture in these cuts of meat from organic broilers and those raised in the wild compared to conventional ones. The protein content of poultry meat is mainly influenced by the age of slaughter (Baéza et al., 2000; Baéza et al., 2012; Baéza et al., 2022). In our study there were no differences, in terms of age and weight, between animals from both types of breeding, organic vs. conventional. On the other hand, proteins and amino acids are closely related to the genetics of the animals (Zampiga et al., 2020). Therefore, we speculated that there were no significant differences in these parameters, since the turkeys studied from both types of production were from the same genetic line.
On the other hand, the analysis of the amino acid composition showed no differences between the 2 production systems. These results are consistent with those described by Ribarski et al. (2016) in wild turkey breast and Gálvez et al. (2020), in chicken meat. Likewise, Zhao et al. (2011) found no differences in amino acid content between 2 broiler breeds.
Regarding the vitamin content of organic vs. conventional turkey meat, in our study vitamins B3 (Niacin), B6, (Pyridoxin), B2 (Riboflavin) and B12 (Cyanocobalamin) were analyzed, observing a statistically higher content of B2 and B6 in organic turkey meat. These results could be due to an additional intake of vitamins contained in the pastures. The inclusion of fresh forage in their diet, due to the outdoor access of organic turkeys, provides them with an extra source of B vitamins and carotenes (Mancinelli et al., 2021).
The mineral composition of meat is another important aspect to consider. The results of our study did not show significant differences between the 2 types of aging for the minerals analyzed (Fe, Zn, K and Mg). Gálvez et al. (2020), analyzed Ca, Fe, K, Mg, Na, P and Zn in industrial vs. free-range vs. organic chicken meat. Our study showed similar results for Zn and K, but not for Mg and Fe. The study by Galvez et al. (2020) reported higher values of Na in the breast of conventional chickens than the other 2 groups; the Mg content was higher in the group of industrial chickens than in free-range and organic chickens in both thigh and breast; finally, the Fe content was significantly higher in the thigh of organic chickens than in that of industrial chickens, while free-range chickens showed intermediate values. If we analyze the results obtained for minerals in other types of meat, Zhao et al. (2016) studied the mineral composition of pork from organic farms vs. conventional farms. The results of this last study showed that there were no significant differences for Na, K, Mg, Ca, Ni, Fe, Zn and Sr. These results coincide with those obtained in our research on Fe, Zn, K and Mg.
In our study, no significant differences were found between the 2 groups in terms of lightness (L*), redness (a*) and yellowness (b*). These results do not match those reported in other studies (Govindarajan, 1973; Husak et al.,2008; Gornowizc et al., 2017; Gálvez et al., 2020). In these studies, darker color values were associated with higher pH values, a fact that in our study was only observed in the thigh (P > 0.05). It has been speculated that the age of the birds could also affect redness values. Older birds tend to have higher myoglobin concentrations compared to younger ones (Castellini et al., 2002). The ages of the turkeys analyzed in our study were similar, which would explain the subtle differences in color.
Meat texture is mainly affected by age, genotype, breeding system, slaughter conditions and postmortem carcass processing techniques, while diet has little significant effect (Baéza et al., 2022). In our study we did not find significant effects of the breeding system on hardness or cutting force, probably because the determining factors mentioned above did not vary in the 2 types of meat analyzed. Shear force was higher in organic turkeys, although the differences were not significant, as mentioned previously. This difference could be due to greater access to fresh air, which allows them more exercise and greater muscle activity. The texture of the meat will also depend on the postmortem evolution of the pH and the rigor mortis phase. When the pH is higher than 5.7, the meat is classified as "dark, firm and dry" (Baéza, et al., 2022). All the turkey meat analyzed in our study had a pH higher than this value, with no significant differences between the 2 types of breeding.
These results could reflect that the differences observed between both types of meat are due to the organic farming conditions, since the sex and genetic line of the meats analyzed for the 2 types of rearing were the same female B.U.T. Premium turkeys (Aviagen Turkeys). However, the heterogeneity of agricultural practices, both organic and conventional, represents an important limit when extrapolating the results of research carried out in this sense, in different contexts and countries. This conclusion has been reached in various studies. Thus, in 2 meta-analyses (Średnicka-Tober et al., 2016a; Średnicka-Tober et al., 2016b), in which the nutritional properties of organic vs. conventional meat and dairy were compared, the authors concluded that greater grazing/forage consumption were the main reasons for the differences observed in the composition of these foods. However, the opposite is true in some organic systems where organic dairy or lamb are produced without grazing, because cold weather conditions or parasitism do not allow it (Kusche et al., 2015; Średnicka-Tober et al., 2016a).
Therefore, the organic turkey meat evaluated in our study presented as advantages over intensive turkey meat, in terms of its possible positive impact on the health of consumers, a lower content of saturated fatty acids and a higher content of monounsaturated fatty acids. The scientific literature shows that diets rich in monounsaturated fatty acids and polyunsaturated fatty acids, and low in saturated fatty acids and trans fatty acids, were associated with a reduction in cardiovascular events (Yamagishi et al., 2010; Estruch et al., 2018). However, it should be noted that the organic meat analyzed had a higher total lipid content and a lower n-3 PUFA content.
Based on the results shown in the published scientific literature (Baker et al., 2002; Dangour et al., 2009; Palupi et al., 2012), one may be tempted to conclude that the consumption of organic foods results in a higher dietary intake of nutritionally desirable compounds. However, current research on the role of organic food consumption in human health is still scarce when compared to other topics researched in nutritional epidemiology. There are important aspects to be determined concerning the differences between the composition of organically produced and conventionally produced foods. Thus, more data should be provided on the differences between meat products from different livestock species and the differences between individual crops. On the other hand, there is little published information on a wide range of nutrients that may be nutritionally relevant, such as water-soluble vitamins and some minerals in meat and milk. Finally, it is important to note the need for more long-term intervention studies with sufficient sample sizes to identify this possible relationship between food consumption and health. In this sense, the assessment of compliance is a challenge for the scientific community since, in the absence of specific biomarkers of exposure, the consumption of organic foods must be based on self-reported data with the greatest risk of bias that this entails. In addition, some of the existing studies show that consumers who buy organic products are more active, follow dietary patterns, and generally healthier lifestyles (Kesse-Guyot et al., 2013; Eisinger-Watzl et al., 2014; Bradbury et al., 2014; Torjusen et al., 2014), so these residual confounders need to be considered.
CONCLUSIONS
The organic turkey meat analyzed in our study contained a higher proportion riboflavin (B2) and pyridoxine (B6). In addition, it also contained a higher content of lipids and monounsaturated fatty acids, and a lower content of omega-3 polyunsaturated fatty acids.
It is important to carefully examine the fat content of organically produced poultry products, as low-fat meat may be suitable for a health-driven market, while meat with higher fat content may be appreciated by a gourmet market.
DISCLOSURES
The authors declare no conflict of interest.
ACKNOWLEDGMENTS
This work has been developed within the framework of the research project “Design of a digital platform for the promotion of healthy and local agri-food products from the Province of Ávila (AGRO4TEC)” with code PT2022_001, financed with funds from the Centre for Knowledge Transfer, Innovation and Entrepreneurship within the framework of the Territorial Development Program for Ávila and its Environment promoted by the Institute of Business Competitiveness of Castilla y León, the Government of Castilla y León, the Provincial Council of Ávila and the City Council of Avila. The partners of the project are the Catholic University of Ávila through the research groups "Integral Approach to Health” (AISA) and “Digital Economy & Knowledge and Information Society” (DEKIS), Association of the Agri-Food Industry of Ávila (AvilaAgro) and the company Turkeys Bio.
We sincerely thank the company AN Avícola Mélida S.L. for providing the carcasses of the conventionally produced turkeys.
Author contributions: AGS, CGB, CR and RP made substantial contributions to the conception and design of the manuscript. All authors contributed substantially to the acquisition of data or analysis and interpretation of data, revised the manuscript critically for important intellectual content, and approved the final version to be published. CG and PJ have carried out the laboratory analyses and created the database.
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