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Minerals and trace elements in Icelandic dairy products and meat
Journal of Food Composition and Analysis 24 (2011) 980–986
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Original Article
Minerals and trace elements in Icelandic dairy products and meat Olafur Reykdal a,*, Sasan Rabieh a,1, Laufey Steingrimsdottir b, Helga Gunnlaugsdottir a a b
Matis ohf., Icelandic Food and Biotech R&D, Vinlandsleid 12, IS-113 Reykjavik, Iceland Unit for Nutrition Research, Landspitali Hospital and Faculty for Food Science and Nutrition, University of Iceland, Eiriksgata 29, IS-101 Reykjavik, Iceland
A R T I C L E I N F O
A B S T R A C T
Article history: Received 13 May 2010 Received in revised form 1 March 2011 Accepted 2 March 2011 Available online 8 March 2011
The aim of this study was to update the Icelandic Food Composition Database with respect to minerals (Ca, K, Mg, Na, and P) and trace elements (Cu, Fe, Hg, Se, and Zn) in frequently consumed agricultural products and to study the seasonal and geographical variation for these elements. Five food products typical for the Icelandic food basket were analysed: whole milk, fresh cheese (skyr), firm cheese (Gouda), lamb meat and minced beef together with skimmed milk, cream and whey. Concentrations of minerals and trace elements were determined by an inductively coupled plasma mass spectrometer (ICP-MS). Seasonal and geographical variation in whole milk was found only for selenium. Concentration of selenium in meat was variable and especially low for beef (1.4–9.6 mg/100 g fresh weight). Mercury was below the detection limit of 0.3 mg/100 g except for one sample of cheese. Skyr was rich in protein, calcium and phosphorus and retains almost all selenium in the skimmed milk used for its production. Skyr whey contains more calcium, magnesium, phosphorus and zinc than cheese whey. Skyr whey is a nutritious product, almost as rich in calcium, potassium and zinc as whole milk and could be used more by the Icelandic food industry. ß 2011 Elsevier Inc. All rights reserved.
Keywords: Minerals Trace elements Selenium Dairy products Skyr Lamb Beef Inductively coupled plasma mass spectrometry Food analysis Food composition
1. Introduction Milk, dairy products and meat are major sources of essential minerals and trace elements in western diets. Accurate values for the mineral content of these foods are thus of special importance as relatively small errors may affect results of dietary surveys and intake estimates to a great extent. Calcium, iron and selenium are of special concern since the intake of these elements might be limited and below reference intakes in certain groups (Steingrimsdottir et al., 2003) while high intake of sodium in relation to potassium, is a serious health concern in other groups of the population (Meneton et al., 2005). While variation in major mineral (Ca, K, Mg, Na, and P) content of foods is mainly determined by food processing and fortification, environmental conditions may greatly affect selenium and mercury in foods (Ekholm et al., 2007; Navarro-Alarcon and Cabrera-Vique, 2008; Levenson and Axelrad, 2006). Selenium is a component of several selenoproteins with essential biological functions and acts as a cofactor of the GPx family of enzymes which protect against oxidative stress. Selenium protects animals against
* Corresponding author. Tel.: +354 422 5098; fax: +354 422 5001. E-mail address: [email protected] (O. Reykdal). 1 Present address: Environmental Geochemistry, University of Bayreuth, Universitaetsstr. 30, 95447 Bayreuth, Germany. 0889-1575/$ – see front matter ß 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.jfca.2011.03.002
toxicity associated with high exposure of heavy metals like mercury (Navarro-Alarcon and Cabrera-Vique, 2008). Mercury is a toxic element and may cause neurological effects, especially in developing nervous systems of unborn or growing children (Debes et al., 2006). Selenium in plants is affected by the content and availability of the element in soil while selenium content of milk and meat is affected by the selenium content in feeds and its availability. Icelandic soil originates from volcanic matter in many areas and is rich in elements like iron and selenium. On the other hand, the soil is rather acidic and contains aluminium oxide that binds selenium. As a consequence low concentrations of selenium are generally found in hay used as feed for cows and sheep in Iceland and selenium deficiencies have been reported in Icelandic livestock (Johannesson et al., 2007). Processing and cooking of food can further diminish selenium concentration (Navarro-Alarcon and Cabrera-Vique, 2008). Icelandic lambs graze in the highlands until slaughtered in September or October. Compared with most other countries, Icelandic lambs are younger or of similar age (4–6 months) when slaughtered. Dairy cattle and cattle for meat production are fed on hay, barley and concentrates throughout the year but also graze on grass pasture during summer. Fish meal was an important part of the feed for cattle in the 20th century but the use of this meal has now decreased considerably. All Icelandic sheep are of the same original Icelandic breed, brought to the island in the ninth and
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tenth century. Similarly all dairy cattle are from the original Icelandic breed that has been isolated from inter-breeding with other cattle for more than 1100 years. However, the cattle for meat production are from the Icelandic breed that has been inter-bred with Galloway, Aberdeen-Angus or Limousine. Low intake of calcium and iron has been reported for certain groups in Iceland, especially young women (Steingrimsdottir et al., 2003) and poor iron status has been described for young Icelandic children prior to a successful public health intervention on a national level (Gunnarsson et al., 2004). While selenium intake seemed sufficient in Iceland in 2002, selenium intake can change rapidly in a population due to changing concentration in foods resulting from altered feeding practices, changes in fertilizers or food imports. It is therefore of great importance to monitor the levels of this trace element in the food supply. Milk, dairy products and meat have traditionally played a very important role in the daily food of most Icelanders. Lamb has been by far the most commonly consumed meat in Iceland and still it amounts to about half of all meat consumed in the country. Skyr is a type of fresh cheese that evolved in Iceland early on as a way of preserving milk and maximizing its food value. It is made from skimmed milk and live cultures, the product is left to coagulate and skyr whey is removed as a by-product. In the old days each farm made its own skyr. When dairy plants were established early in the 20th century skyr became one of the most important dairy products in Iceland. The traditional skyr was produced by filtration of coagulate on linen cloth. In modern dairies the process has been modified and made more efficient by including centrifugation and ultrafiltration (Hilmarsdottir and Arnadottir, 1989). Data on minerals and trace elements in food from Icelandic agriculture have been limited. Specifically information has been lacking on processing effects on elements in dairy products like skyr. Also, the feeding strategies of agriculture have changed during the last decade, making updating of food data crucial. The aim of this study was to update the Icelandic Food Composition Database with respect to minerals (Ca, K, Mg, Na, and P) and trace elements (Cu, Fe, Hg, Se, and Zn) in frequently consumed agricultural products and to study the seasonal and geographical variation for these elements. This work was carried out to make studies on the mineral and trace element intake of Icelanders possible. 2. Materials and methods 2.1. Samples Whole pasteurized and packaged (paperboard containers) milk was sampled in two dairies (MS Dairy Selfoss South-Iceland and MS Dairy Akureyri North-Iceland) during winter (January and March 2008) and summer (June and August 2008). Both dairies
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process milk from all dairy farmers in the region during two consecutive days. Sampling was carried out on Wednesdays and Thursdays in the last week of the indicated months. Five 1 L samples were collected over the entire milk processing period each day. A composite sample was made from 10 primary samples for each dairy and month. The two dairies process about 90% of the whole pasteurized and packaged milk in the country. The milk production is based on one cattle breed. Industrially produced skyr was sampled at the MS Dairy Selfoss in January, March and August 2008. Each time skyr was collected from three processing lots/days making one composite sample (6 kg, plastic containers). The skyr was made from skimmed milk that was pasteurized and subsequently cooled down and incubated with cultures. Whey was removed by ultrafiltration retaining valuable whey proteins in the skyr. Skyr whey, skimmed milk, cream and whole milk were also collected from the same three processing lots as the skyr and production quantities recorded to investigate distribution of nutrients between skyr and whey. Samples of skimmed milk, cream and whole milk were pasteurized and packaged (paperboard containers) products, 3 kg per composite samples of skimmed milk and whole milk and 1.5 kg per composite sample of cream. Traditionally produced skyr and skyr whey were sampled in March, June and August 2008 at the MS Dairy Akureyri. Each time a composite sample was made from three processing lots/days (1.5 kg skyr and 3 kg whey per composite sample, plastic containers). Traditional skyr was produced by the old method using incubation with rennet and old skyr and finally cloth filtration to separate the curd (skyr) and the skyr whey. The sampled foods are defined in Table 1. Gouda cheese, cheese whey and pasteurized cheese milk were sampled in January, March and August 2008 at the MS Dairy Akureyri, each time from two processing lots for one composite sample (3 kg cheese, 4 kg whey and milk). The cheese samples were collected twice: after pressing (two days old) and after ripening for about 3 months. The whey collected was the first whey used for cheese spread production. A cheese spread made by concentrating cheese whey by heating and evaporation and adding skimmed milk, cream and sugar, was sampled during winter and summer from three production lots each time. Lamb meat was sampled from four regions in slaughterhouses during the annual slaughter season September–October 2008. All sheep in the country originate from the same Icelandic breed. Each sample consisted of three legs of lamb from three carcasses from the same farm. Farms were selected randomly but lamb numbers were recorded and information regarding the farm was studied later. The lamb legs were defatted and deboned before homogenization. Beef was grade UNI minced meat from the whole carcass, except fillet, leg, topside and thick flank, sampled in March and October 2008. Each beef sample consisted of 5 subsamples (500 g each) collected during one day at a meat processing plant. Several
Table 1 Description of food samples. English name
Original name
Comments
LanguaL codea
Whole milk Cream Skimmed milk Skyr, industrial Skyr whey, industrial Skyr, traditional Skyr whey, traditional Cheese, Gouda Cheese whey Cheese spread from whey Lamb leg Beef, minced
Ny´mjo´lk Rjo´mi Undanrenna Skyr Skyrmysa Skyr, hefðbundið Skyrmysa, hefðbundin Ostur, Gouda Ostamysa Mysingur Lambalæri Nautgripahakk
Fat 4 g/100 g Fat 36 g/100 g Fat 0.8 g/100 g Semisolid yoghurt-like cheese. Fat 0.3 g/100 g Fat 0.3 g/100 g. Semisolid yoghurt-like cheese. Fat 0.3 g/100 g. Fat 0.3 g/100 g. Fat 26 g/100 g Fat 0.3 g/100 g. Fat 8 g/100 g. Defatted, fat about 6 g/100 g. Fat 6–16 g/100 g
A0780 A0782 A0780 A0786 A0783 A0786 A0783 A0785 A0783 A0786 A0794 A0794
a
LanguaL is a method for describing, capturing and retrieving data about food (LanguaL, 2010).
B1201 B1201 B1201 B1201 B1201 B1201 B1201 B1201 B1201 B1201 B1669 B1161
C0235 C0161 C0235 C0245 C0244 C0245 C0244 C0245 C0244 C0244 C0266 C0270
E0123 E0139 E0123 E0119 E0109 E0119 E0109 E0151 E0109 E0119 E0150 E0117
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carcasses were processed for each sample; the total number of carcasses was 58 for all 10 beef samples. Samples were collected from four processing plants representing about 70% of the minced beef produced in the country. Meat samples were kept frozen until they were homogenized. Dairy samples were refrigerated, transported to Matis the day after sampling and prepared immediately for analysis. 2.2. Sample preparation Meat samples were homogenized in a stainless steel rotating knife homogenizer (Tecator 1094; Foss, Hillerod, Denmark). Liquid dairy samples were mixed by pouring the contents of all 1 L packages four times between containers. Skyr samples were mixed in plastic bags. Cheese samples were cut into small cubes, mixed in plastic bags and homogenized in a homogenizer (Tecator 1094). All containers and equipments were made from either plastic or stainless steel. Containers and equipments were washed by a solution of 2% sodium EDTA (>95% purity; Sigma–Aldrich, Steinheim, Germany) and 2% sodium citrate (>98.5% purity, Sigma–Aldrich) to remove ions. Finally all surfaces were washed by Milli-Q water (18.2 MV cm quality; Millipore SAS, Molsheim, France) before contact with samples. 2.3. Analysis Total selenium and other elements (Ca, Cu, Fe, Hg, K, Mg, Na, P, and Zn) concentrations in the dairy and meat samples were determined by an inductively coupled plasma mass spectrometer (ICP-MS) (Agilent 7500ce; Agilent Technologies, Waldbronn, Germany) with an octopole based collision/reaction cell in the full quantitative mode. Helium and hydrogen gases were used as collision and reaction gases, respectively. Argon was used as sample introduction and plasma gas. All gases were 99.999% pure and were supplied by ISAGA (Reykjavik, Iceland). Prior to analysis for total element concentrations a complete destruction of the organic matrix of homogenized samples is required and during the mineralization process all organic element compounds were converted into inorganic elements. Therefore, the samples were microwave digested (MARS microwave oven; CEM, Matthews, USA) with HNO3 (Suprapure, Merck, Darmstadt, Germany) and H2O2 (TraceSelect Ultra; Sigma–Aldrich) at up to 220 8C for 15– 30 min in closed vessels. Digested samples were diluted appropriately with ultra-pure laboratory Milli-Q water (18.2 MV cm quality; Millipore SAS). The sample digests were kept frozen at 20 8C until ICP-MS analysis. Each sample was digested in triplicate and analyses were carried out once on each digest. The ICP-MS instrument was tuned daily by 1 mg L 1 tuning
Table 2 Operating conditions for measurements with inductively coupled plasma mass spectrometer. Masses
23 (Na)c, 24 (Mg)c, 31 (P)a, 39 (K)b, 43 (Ca)a, 56 (Fe)b, 63 (Cu)a, 66 (Zn)a, 78 (Se)b, 202 (Hg)c
Integration time Radio frequency (RF) power Skimmer cone Spray chamber temperature Plasma gas (Ar) Nebulizer gas (Ar) Make-up gas (Ar) Collision gas (He) Reaction gas (H2) Nebulizer Sample delivery Replicates
0.1 s 1500 W Ni 2 8C 15 L min 1 0.9 L min 1 0.16 L min 1 3.9 L min 1 3.5 L min 1 Micromist About 0.5 mL min 3
a b c
1
He mode. H2 mode. Nogas mode.
solution. ICP-MS operation conditions are reported in Table 2. The elements Cu, Fe, Hg, Se and Zn were analysed simultaneously. Digested samples were further diluted for macro-minerals (Ca, K, Mg, Na, and P) analysis. Monoelemental, high purity grade 1 g L 1 standard stock solutions of Ca, Cu, Fe, Hg, K, Mg, Na, P, Se and Zn were purchased from CPI International (Amsterdam, The Netherlands). In order to check the trueness of the analysis, certified reference materials skim milk powder (CRM 063R) and bovine muscle (CRM 184) from the Institute for Reference Materials and Measurements (IRMM, Geel, Belgium) were analysed. Good agreement was obtained between certified and analysed values for the elements measured (see Table 3 for details). Element recovery tests were carried out with beef, skimmed milk and skyr by adding standards. The average elemental recovery in these three matrixes ranged between 91 and 108%. Water content of all samples was calculated from the weight loss during drying at 103 2 8C for 4 h (ISO, 1999). Protein was determined by the Kjeldahl method (ISO, 2005). Samples were digested in sulphuric acid (>98.5% purity; Sigma–Aldrich) in the presence of technical grade CuSO4 catalyst (Foss Analytical AB, Ho¨ganas, Sweden). The solution was made alkaline by technical grade NaOH (JSC, Volgograd, Russia) and the released ammonia was distilled in a distillation unit (2400 Kjeltec Analyzer, Foss) into boric acid (>98.5% purity; Sigma–Aldrich) solution which was then titrated with H2SO4 to determine the nitrogen content. The determined nitrogen content was multiplied by 6.25 for meat and 6.38 for dairy products to report protein content. Each sample was digested in
Table 3 Certified and found values for certified reference materials (CRM) (mean standard deviation). Element
Unit
Ca P Mg K Na Se Zn Fe Cu Hg
g/kg g/kg g/kg g/kg g/kg mg/kg mg/kg mg/kg mg/kg mg/kg
Skim milk powder CRM 063Ra
Bovine muscle CRM 184a
Certified value
Found value n = 18
Certified value
Found value n = 9
13.49 0.10 11.10 0.13 1.263 0.024 17.68 0.19 4.37 0.031 (129) 49.0 0.6 2.32 0.23 0.602 0.019 NAc
13.74 0.35 10.88 0.53 1.241 0.093 16.55 1.65 4.16 0.23 132 7 48.7 1.5 2.29 0.10 0.574 0.014 <3
(0.15)b (8.3) (1.02) (16.6) (2.0) 183 12 166 3 79 2 2.36 0.06 2.6 0.6
0.14 0.02 8.79 0.45 1.03 0.37 16.89 1.65 2.02 0.03 181 4 167.3 0.9 78.2 1.2 2.31 0.02 <3
n = number of samples. a Institute for Reference Materials and Measurements (Geel, Belgium). b Values in brackets are not certified. c Not reported.
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Table 4 Water, protein and mineral values per 100 g fresh dairy products (mean standard deviation). Product
n
Water (g/100 g)
Protein N 6.38 (g/100 g)
Ca (mg/100 g)
P (mg/100 g)
Mg (mg/100 g)
K (mg/100 g)
Na (mg/100 g)
Whole milk summer Whole milk winter Whole milk for skyr Cream Skimmed milk Skyr, industrial Skyr whey, industrial Skyr traditional Skyr whey traditional Milk for cheese Cheese, Gouda, 2nd day Cheese, Gouda, ripe Cheese whey Cheese spread from whey
4 4 3 3 3 3 3 3 3 3 3 3 3 2
87.3 0.1 87.7 0.2 87.5 0.1 57.8 0.4 91.2 0.1 83.1 0.3 94.6 0.1 81.6 0.2 94.1 0.1 88.8 0.6 43.5 0.3 42.8 0.5 93.4 0.1 32.3
3.27 0.09 3.30 0.09 3.34 0.04 2.22 0.07 3.43 0.05 11.2 0.4 0.22 0.01 13.1 0.5 0.41 0.00 3.40 0.06 25.0 0.1 25.0 0.3 0.94 0.02 8.78
126 5 114 5 114 11 67.6 8.5 107 6 100 7 109 6 85.0 4.8 108 9 118 9 732 9 788 17 34.9 1.2 261
124 3 123 8 125 6 78 4 116 3 192 21 88 10 190 26 84 9 124 1 479 14 503 37 51 8 361
9.63 0.61 9.98 0.30 9.60 0.61 5.43 0.51 8.87 0.32 9.37 1.10 8.37 0.93 8.67 1.22 8.30 0.92 10.1 0.6 29.7 1.0 33.5 2.4 6.33 0.72 51.6
144 5 146 5 146 2 92 5 142 2 123 14 145 17 114 15 132 16 152 6 80 3 88 7 140 13 1040
40.1 1.6 38.8 2.5 39.9 2.8 25.6 2.5 38.8 2.4 32.0 1.8 39.8 3.3 27.9 3.3 35.7 3.0 40.0 2.0 419 97 618 36 39.5 1.7 315
n = number of samples.
duplicate for protein analysis. Phosphorus was determined by colorimetry as phosphate vanadomolybdate at 420 nm (AOAC, 1990) for comparison to the ICP-MS data. For measurements of water, protein and phosphorus duplicate analysis of each sample was carried out. Reference material was analysed for phosphorus (skim milk powder, CRM 063R, IRMM). Methods for water and protein were accredited for fish. Protein measurements were tested by participation in proficiency measurements which gave 64.89 g protein/100 g fish meal compared to the average of 64.49 g/100 g for the 18 participants. 2.4. Statistical analysis Statistical analysis was performed using the Number Cruncher Statistical System 2000 (NCSS) software (Kaysville, UT, USA). Analysis of variance was used to determine significance difference among areas, periods or production methods. 3. Results and discussion 3.1. Dairy products Data for water, protein, minerals and trace elements in dairy products are shown in Tables 4 and 5. The products are whole pasteurized milk, industrially produced skyr (semisolid yoghurtlike cheese) and Gouda cheese together with milk, skimmed milk and cream used in the production of industrial skyr and cheese. The by-products skyr whey and cheese whey are included together with cheese spread made from cheese whey. Traditional skyr and skyr whey are also included for comparison. The foods
are defined in Table 1 by names, descriptions and LanguaL codes. LanguaL is a method for describing, capturing and retrieving data about food (LanguaL, 2010) used increasingly in Europe and internationally. The dairy products are important sources of calcium, phosphorus and selenium. Mercury in dairy samples was below the detection limit of 0.3 mg/100 g except for one ripe cheese sample which contained 1.4 mg Hg/100 g. The European Union legislation on food has been adapted in Iceland and in the present legislation there are no maximum levels for Hg in the foods reported in this paper. The concentrations of iron, copper and zinc in the dairy products were low. Whole pasteurized summer milk and winter milk from two regions were compared. Significant geographical variation was only found for selenium (p < 0.05). Significant seasonal variation was found for selenium (p < 0.005) and moisture (p < 0.05). On dry weight basis significant difference was found only for selenium (p < 0.005). Higher selenium in the winter milk can be explained by more selenium supplemented feeds given to the cows during winter. Skyr is made from skimmed milk and is rich in protein but low in fat. Fat has been determined as 0.25 0.11 g/100 g (Matis, 2010). Skyr produced by two methods (industrial and traditional) was compared. Significant difference (p < 0.05) between methods was found for protein, water, calcium, iron and selenium. Traditional skyr contains more protein and selenium but less calcium than the industrial skyr. The difference between industrial and traditional skyr can be explained by different filtering methods and water content. The traditional skyr is filtered to a greater extent thus more protein and Se are retained within the product on
Table 5 Trace element values per 100 g fresh dairy products (mean standard deviation). Product
n
Se (mg/100 g)
Zn (mg/100 g)
Fe (mg/100 g)
Cu (mg/100 g)
Hg (mg/100 g)
Whole milk, summer Whole milk, winter Whole milk for skyr Cream Skimmed milk Skyr, industrial Skyr whey, industrial Skyr, traditional Skyr whey, traditional Milk for cheese Cheese, Gouda, 2nd day Cheese, Gouda, ripe Cheese whey Cheese spread from whey
4 4 3 3 3 3 3 3 3 3 3 3 3 2
2.15 0.13 2.63 0.15 2.17 0.31 2.53 0.38 1.83 0.21 6.43 1.10 <0.3 9.70 1.25 <0.3–0.3 2.57 0.23 19.0 2.7 21.6 2.6 0.63 0.06 6.80
0.433 0.050 0.389 0.016 0.419 0.024 0.246 0.011 0.474 0.056 0.521 0.061 0.374 0.033 0.448 0.019 0.399 0.031 0.380 0.002 3.62 0.127 3.61 0.292 0.013 0.009 0.262
0.027 0.004 0.020 0.001 0.023 0.004 0.050 0.002 0.020 0.001 0.045 0.005 0.016 0.002 0.065 0.004 0.008 0.002 0.024 0.004 0.133 0.008 0.139 0.023 0.014 0.003 0.102
0.0041 0.0005 0.0042 0.0006 0.0046 0.001 0.0043 0.0009 0.0060 0.0001 0.0157 0.0031 0.0010 0.0003 0.0158 0.0032 0.0009 0.0002 0.0036 0.0003 0.0261 0.0055 0.0266 0.0080 0.0016 0.0003 0.0122
<0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3–1.4 <0.3 <0.3
n = number of samples.
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Table 6 Water, protein and mineral values per 100 g fresh meat (mean standard deviation). Product
n
Water (g/100 g)
Lamb leg, South-Iceland Lamb leg, West-Iceland Lamb leg, Northwest-Iceland Lamb leg, Northeast-Iceland Lamb leg, all samples Beef, minced Beef, minced, fibre added Beef, minced, all samples
3 3 3 3 12 7 3 10
71.5 1.2 71.0 0.5 69.0 1.4 71.8 0.9 70.8 1.5 68.8 3.1 70.4 2.7 69.3 2.9
Protein N 6.25 (g/100 g)
Ca (mg/100 g)
P (mg/100 g)
Mg (mg/100 g)
K (mg/100 g)
Na (mg/100 g)
20.7 0.7 17.6 0.8 19.7 1.6
5.1 0.7 5.1 0.4 8.9 3.9 3.8 0.3 5.7 2.6 5.7 0.8 7.0 0.7 6.1 1.0
232 8 218 12 227 6 197 13 219 17 194 6 162 4 184 16
21.3 0.8 20.0 1.7 20.4 0.6 18.3 0.6 20.0 1.4 17.4 0.6 15.4 0.6 16.8 1.1
334 11 321 9 313 10 313 8 320 12 273 8 265 14 271 10
46.8 2.7 45.8 1.4 44.5 1.2 47.1 3.0 46.1 2.2 68.7 9.3 106 7 79.8 20
n = number of samples.
a weight basis than in the industrially produced skyr. The ultrafiltration used by the dairy industry retains more calcium than the traditional filtering of coagulate through fabric. Skyr whey is a nutritious product, almost as rich in calcium, zinc and potassium as whole milk. This product could be used more by the Icelandic food industry. Gouda cheese is very rich in calcium, phosphorus and selenium. The Gouda cheese retains zinc very well since zinc concentration of the whey is very low. The composition of ripe cheese and cheese samples after 2 days is similar except for the higher sodium content of the ripe cheese. The cheese whey is rich in minerals, especially potassium which is similar to whole milk. The K/Na ratio is 3.5 for the whey while it is 0.1 for the ripe cheese. Cheese whey spread is made by concentrating the cheese whey and adding skimmed milk, cream and sugar. The spread is therefore very rich in minerals and trace elements, containing 7–20 times more minerals and trace elements than the whey. The composition of the spread did not differ between one winter sample and one summer sample. Selenium content of Icelandic whole milk and cheese was higher than values reported from low selenium areas (Lindmark-Ma˚nsson et al., 2003; Barclay et al., 1995; NavarroAlarcon and Cabrera-Vique, 2008). Selenium is added to the feeds of milking cows in Iceland and this most likely explains the relatively high levels found. The concentrations of iron and copper in the dairy products were very low. Phosphorus in Icelandic whole milk is about 30% higher than reported earlier for Icelandic milk and Swedish milk (Lindmark-Ma˚nsson et al., 2003). This could be explained by the magnesium phosphate and calcium phosphate that are now added to the feeds for milking cows. The phosphorus content of these feeds is about 1%. Earlier determinations of phosphorus in milk have generally used colorimetric methods for the determination of phosphorus. Therefore the determination of phosphorus of four milk samples was repeated with the colorimetric method. Results were lower than when ICP-MS was used for the quantification of phosphorus and within the range reported earlier for Icelandic milk. Phosphorus determined by the colorimetric method in a reference material (Skim milk powder CRM 063R) was 93% of the certified value. The colorimetric
method thus might underestimate the phosphorus content in dairy products. During the processing of industrial skyr and Gouda cheese all products and by-products were sampled and production quantities recorded. The distribution of skimmed milk proteins, minerals and trace elements between skyr and whey was studied. The proteins of the skimmed milk are retained in skyr which contains about 11 g protein per 100 g, while whey contains only 0.22 g protein/100 g. The total amount of selenium in skimmed milk is almost exclusively captured in the skyr. Strong association of selenium with the casein fraction is well known (Rodriguez Rodriguez et al., 2002). During the skyr production pH drops to about 4.5 making minerals more soluble. Considerable parts of the amounts of some elements in the skimmed milk are found in the skyr whey (average of three determinations SD): calcium 72 1%, phosphorus 52 1%, magnesium 68 0.3%, potassium 74 0.1%, sodium 75 1% and zinc 63 3%. It can thus be concluded that industrial skyr whey is rich in minerals and zinc. The composition of cheese whey and skyr whey differs considerably. The skyr whey contains more calcium (p < 0.005), magnesium (p < 0.05), phosphorus (p < 0.05), and zinc (p < 0.005) than the cheese whey. This can be explained by the lower pH during skyr production (pH 4.5) than during the Gouda cheese production (pH 5.2). The concentration of potassium and sodium is similar in all samples of whey, whole milk and skimmed milk. These minerals are known to be essentially diffusible in whole milk whereas calcium (70%), phosphate (50%) and magnesium (40%) are partially bound to the casein micelles (Mekmane et al., 2009). 3.2. Meat Data for lamb and beef are present in Tables 6 and 7. Little variation is found in the composition of lamb between the four areas with the exception of selenium which shows a range of 2.9– 11.7 mg/100 g. On dry weight basis significant geographical differences (p < 0.05) are only found for selenium in lamb. There are also considerable differences for selenium within regions. Lamb meat is a rich source of protein, iron, phosphorus and zinc. Mercury was below detection limit (0.3 mg/100 g) for all samples.
Table 7 Trace element values per 100 g fresh meat (mean standard deviation). Product
n
Se (mg/100 g)
Zn (mg/100 g)
Fe (mg/100 g)
Cu (mg/100 g)
Hg (mg/100 g)
Lamb leg, South-Iceland Lamb leg, West-Iceland Lamb leg, Northwest-Iceland Lamb leg, Northeast-Iceland Lamb leg, all samples Beef, minced Beef, minced, fibre added Beef, minced, all samples
3 3 3 3 12 7 3 10
4.8 2.8 10.8 2.6 7.5 3.3 10.9 1.3 8.5 3.5 3.4 1.9 4.8 4.1 3.8 2.6
2.79 0.21 2.79 0.06 3.02 0.13 2.63 0.07 2.81 0.18 4.08 0.52 3.49 0.09 3.91 0.51
1.43 0.11 1.51 0.11 1.58 0.06 1.54 0.05 1.52 0.09 1.76 0.17 1.60 0.20 1.71 0.18
0.097 0.005 0.095 0.001 0.095 0.007 0.094 0.002 0.096 0.004 0.047 0.006 0.047 0.002 0.047 0.005
<0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3
n = number of samples.
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Table 8 Comparison of levels (mg/100 g fresh weight) of selenium in meat in some countries. Meat
Country
n
Beef minced Beef Beef Beef Beef steak Lamb leg Lamb Lamb Lamb Lamb chop
Iceland UK Ireland Denmark Australia Iceland UK Ireland Denmark Australia
10 4 14 48 6 12 4 16 9 2
Se (mg/100 g)
Source
Mean
Range
3.8 7.6 8.1 9.3 20 8.5 3.8 8.8 6.1 22
1.4–9.6 6.8–8.4 6.1–10.5 <4–14.8 17–21 2.9–13.8 2.9–4.7 7.1–10.9 <4–11.1 20–23
Present study Barclay et al. (1995) Murphy and Cashman (2001) Larsen et al. (2002) Tinggi et al. (1992) Present study Barclay et al. (1995) Murphy and Cashman (2001) Larsen et al. (2002) Tinggi et al. (1992)
n = number of samples.
This is consistent with very low mercury concentrations reported for Icelandic lamb organs (Reykdal and Thorlacius, 2001). The nutrient profile of minced beef differed between processing plants. Samples from one of the plants were minced beef with potato fibre added and contained significantly (p < 0.05) less protein and more sodium than minced beef from the other plants. Fibre plus carbohydrates estimated as difference (100 sum of water, protein, fat and ash values) were 2.1 0.4 g/100 g for minced beef with added fibre while it was 0.0 g/100 g for minced beef from other plants. Selenium in the minced beef samples was very variable (1.4–9.6 mg/100 g). Mercury for minced beef was below the detection limit (0.3 mg/100 g). Selenium concentration was generally considerably higher in Icelandic lamb than in beef (p < 0.005). For UK data (Barclay et al., 1995) the order was different, there beef had higher selenium concentrations than lamb. Table 8 compares selenium levels reported for beef and lamb in five countries. The table shows that selenium concentration for Icelandic beef is low compared to data from the other countries. Low selenium concentrations in Icelandic beef can most likely be explained by the low concentration of selenium in Icelandic hay (Johannesson et al., 2007) and limited use of selenium supplemented feeds. Lambs graze in the Icelandic highlands until slaughtered and depend on availability of the element from plants and soil. It has been reported that selenium concentration is higher in plants in the highlands than in hay from cultivated areas (Johannesson et al., 2007). This is the most likely explanation for the higher concentration of selenium in lamb meat than beef in Iceland. Selenium concentration in Icelandic lamb is comparable to levels found in some other countries (Table 8). 4. Conclusions Iceland is a low selenium area due to poor availability of selenium from soil. Nevertheless, agricultural food products show quite variable selenium levels. Selenium in milk is maintained by adding selenium to the feed. Beef, on the other hand, is very low in selenium reflecting limited selenium in the feed. Lamb is higher in selenium than beef (p < 0.005) but concentration of selenium in both beef and lamb is very variable. Mercury is below the detection limit except for one sample of cheese. Skyr is a nutritious product, rich in protein, calcium, phosphorus and selenium but very low in fat. It is noteworthy that skyr retains almost all the selenium in the skimmed milk used for its production. Skyr whey contains more calcium (p < 0.005), magnesium (p < 0.05), phosphorus (p < 0.05), and zinc (p < 0.005) than cheese whey and could be used more extensively for food production. Composition of lamb meat shows little variation except for selenium. Icelandic lambs graze their whole lifetime in the wild.
Consequently the variation in selenium concentration reflects natural geographical variety of plants and soils with respect to selenium. The composition of beef samples was variable and reflects the trend in the meat industry to add carbohydrates, fibre and water to the meat products. Due to the variability of selenium in the food supply, its concentration should be monitored in food and feed.
Acknowledgments This work was supported by the Icelandic Agricultural Productivity Fund, Matis ohf and the Agricultural University of Iceland. Olafur Unnarsson at the MS Dairy Selfoss, Kristin Halldorsdottir at MS Dairy Akureyri and Oli Thor Hilmarsson at Matis are greatly acknowledged for their work on sampling and valuable advice. References AOAC, 1990. Phosphorus (total) in meat. In: Helrich, K. (Ed.), Official Methods of Analysis of the Association of Official Analytical Chemists. 15th ed. Association of Official Analytical Chemists, Arlington, USA, Method No. 969.31. Barclay, M.N.I., MacPherson, A., Dixon, J., 1995. Selenium content of a range of UK foods. Journal of Food Composition and Analysis 8, 307–318. Debes, F., Budtz-Jørgensen, E., Weihe, P., White, R.F., Grandjean, P., 2006. Impact of prenatal methylmercury exposure on neurobehavioral function at age 14 years. Neurotoxicology and Teratology 28, 363–375. Ekholm, P., Reinivuo, H., Mattila, P., Pakkala, H., Koponen, J., Happonen, A., Hellstro¨m, J., Ovaskainen, M.-L., 2007. Changes in the mineral and trace element contents of cereals, fruits and vegetables in Finland. Journal of Food Composition and Analysis 20, 487–495. Gunnarsson, B.S, Thorsdottir, I., Palsson, G., 2004. Iron status in 2-year-old Icelandic children and associations with dietary intake and growth. European Journal of Clinical Nutrition 58, 901–906. Hilmarsdottir, E., Arnadottir, A.T., 1989. Nutritional effects of pickle fermentation of blood and liver sausages in skyr whey. In: Somogyi, J.C., Mu¨ller, H.R. (Eds.), Nutritional Impact of Food Processing, Bibliotheca Nutritio et Dieta, No. 43. Karger, Basel, Switzerland, pp. 47–58. ISO, 1999. Determination of moisture and other volatile matter content. In: ISO Standard 6496, The International Organization for Standardization, Geneva, Switzerland. ISO, 2005. Determination of nitrogen content and calculation of crude protein content. In: ISO Standard 5983, The International Organization for Standardization, Geneva, Switzerland. Johannesson, T., Eiriksson, T., Gudmundsdottir, K.B., Sigurdarson, S., Kristinsson, J., 2007. Overview. Seven trace elements in Icelandic forage. Their value in animal health and with special relation to scrapie. Icelandic Agricultural Sciences 20, 3–24. LanguaL International Framework for Food Description, LanguaL Food Description Thesaurus, 2010, Retrieved March 31, 2010 from the Langual Home Page: http://www.langual.org Larsen, E.H., Andersen, N.L., Møller, A., Petersen, A., Mortensen, G.K., Petersen, J., 2002. Monitoring the content and intake of trace elements from food in Denmark. Food Additives and Contaminants 19 (1), 33–46. Levenson, C.W., Axelrad, D.M., 2006. Too much of a good thing? Update on fish consumption and mercury exposure. Nutrition Reviews 64, 139–145. Lindmark-Ma˚nsson, H., Fonde´n, R., Pettersson, H.-E., 2003. Composition of Swedish dairy milk. International Dairy Journal 13, 409–425.
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Matis. The Icelandic Food Composition Database on Internet, 2010, Retrieved March 31, 2010, from the Matis Home Page: http://www.matis.is/isgem/en Mekmane, O., Graet, Y.L., Gaucheron, F., 2009. A model for predicting salt equilibria in milk and mineral-enriched milks. Food Chemistry 116, 233–239. Meneton, P., Jeunemaitre, X., De Wardener, H.E., McGregor, G.A., 2005. Links between dietary salt intake, renal salt handling, blood pressure, and cardiovascular diseases. Physiological Reviews 85, 679–715. Murphy, J., Cashman, K.D., 2001. Selenium content of a range of Irish foods. Food Chemistry 74, 493–498. Navarro-Alarcon, M., Cabrera-Vique, C., 2008. Selenium in food and the human body: a review. Science of the Total Environment 400, 115–141.
Reykdal, O., Thorlacius, A., 2001. Cadmium, mercury, iron, copper, manganese and zinc in livers and kidneys of Icelandic lambs. Food Additives and Contaminants 18 (11), 960–969. Rodriguez Rodriguez, E.M.R., Alaejos, M.S., Romero, C.D., 2002. Mineral content in goats’ milk. Journal of Food Quality 25, 343–358. Steingrimsdottir, L., Thorgeirsdottir, H., Olafsdottir, A.S., 2003 The diet of Icelanders, Dietary survey of the Icelandic Nutrition Council 2002, Main findings. Rannso´knir Manneldisra´ðs V. Ly´ðheilsusto¨ð. (In Icelandic with English summary). Tinggi, U., Reilly, C., Patterson, C.M., 1992. Determination of selenium in foodstuffs using spectrofluorimetry and hydride generation atomic absorption spectroscopy. Journal of Food Composition and Analysis 5, 269–280.
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Journal of Food Composition and Analysis journal homepage: www.elsevier.com/locate/jfca
Original Article
Minerals and trace elements in Icelandic dairy products and meat Olafur Reykdal a,*, Sasan Rabieh a,1, Laufey Steingrimsdottir b, Helga Gunnlaugsdottir a a b
Matis ohf., Icelandic Food and Biotech R&D, Vinlandsleid 12, IS-113 Reykjavik, Iceland Unit for Nutrition Research, Landspitali Hospital and Faculty for Food Science and Nutrition, University of Iceland, Eiriksgata 29, IS-101 Reykjavik, Iceland
A R T I C L E I N F O
A B S T R A C T
Article history: Received 13 May 2010 Received in revised form 1 March 2011 Accepted 2 March 2011 Available online 8 March 2011
The aim of this study was to update the Icelandic Food Composition Database with respect to minerals (Ca, K, Mg, Na, and P) and trace elements (Cu, Fe, Hg, Se, and Zn) in frequently consumed agricultural products and to study the seasonal and geographical variation for these elements. Five food products typical for the Icelandic food basket were analysed: whole milk, fresh cheese (skyr), firm cheese (Gouda), lamb meat and minced beef together with skimmed milk, cream and whey. Concentrations of minerals and trace elements were determined by an inductively coupled plasma mass spectrometer (ICP-MS). Seasonal and geographical variation in whole milk was found only for selenium. Concentration of selenium in meat was variable and especially low for beef (1.4–9.6 mg/100 g fresh weight). Mercury was below the detection limit of 0.3 mg/100 g except for one sample of cheese. Skyr was rich in protein, calcium and phosphorus and retains almost all selenium in the skimmed milk used for its production. Skyr whey contains more calcium, magnesium, phosphorus and zinc than cheese whey. Skyr whey is a nutritious product, almost as rich in calcium, potassium and zinc as whole milk and could be used more by the Icelandic food industry. ß 2011 Elsevier Inc. All rights reserved.
Keywords: Minerals Trace elements Selenium Dairy products Skyr Lamb Beef Inductively coupled plasma mass spectrometry Food analysis Food composition
1. Introduction Milk, dairy products and meat are major sources of essential minerals and trace elements in western diets. Accurate values for the mineral content of these foods are thus of special importance as relatively small errors may affect results of dietary surveys and intake estimates to a great extent. Calcium, iron and selenium are of special concern since the intake of these elements might be limited and below reference intakes in certain groups (Steingrimsdottir et al., 2003) while high intake of sodium in relation to potassium, is a serious health concern in other groups of the population (Meneton et al., 2005). While variation in major mineral (Ca, K, Mg, Na, and P) content of foods is mainly determined by food processing and fortification, environmental conditions may greatly affect selenium and mercury in foods (Ekholm et al., 2007; Navarro-Alarcon and Cabrera-Vique, 2008; Levenson and Axelrad, 2006). Selenium is a component of several selenoproteins with essential biological functions and acts as a cofactor of the GPx family of enzymes which protect against oxidative stress. Selenium protects animals against
* Corresponding author. Tel.: +354 422 5098; fax: +354 422 5001. E-mail address: [email protected] (O. Reykdal). 1 Present address: Environmental Geochemistry, University of Bayreuth, Universitaetsstr. 30, 95447 Bayreuth, Germany. 0889-1575/$ – see front matter ß 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.jfca.2011.03.002
toxicity associated with high exposure of heavy metals like mercury (Navarro-Alarcon and Cabrera-Vique, 2008). Mercury is a toxic element and may cause neurological effects, especially in developing nervous systems of unborn or growing children (Debes et al., 2006). Selenium in plants is affected by the content and availability of the element in soil while selenium content of milk and meat is affected by the selenium content in feeds and its availability. Icelandic soil originates from volcanic matter in many areas and is rich in elements like iron and selenium. On the other hand, the soil is rather acidic and contains aluminium oxide that binds selenium. As a consequence low concentrations of selenium are generally found in hay used as feed for cows and sheep in Iceland and selenium deficiencies have been reported in Icelandic livestock (Johannesson et al., 2007). Processing and cooking of food can further diminish selenium concentration (Navarro-Alarcon and Cabrera-Vique, 2008). Icelandic lambs graze in the highlands until slaughtered in September or October. Compared with most other countries, Icelandic lambs are younger or of similar age (4–6 months) when slaughtered. Dairy cattle and cattle for meat production are fed on hay, barley and concentrates throughout the year but also graze on grass pasture during summer. Fish meal was an important part of the feed for cattle in the 20th century but the use of this meal has now decreased considerably. All Icelandic sheep are of the same original Icelandic breed, brought to the island in the ninth and
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tenth century. Similarly all dairy cattle are from the original Icelandic breed that has been isolated from inter-breeding with other cattle for more than 1100 years. However, the cattle for meat production are from the Icelandic breed that has been inter-bred with Galloway, Aberdeen-Angus or Limousine. Low intake of calcium and iron has been reported for certain groups in Iceland, especially young women (Steingrimsdottir et al., 2003) and poor iron status has been described for young Icelandic children prior to a successful public health intervention on a national level (Gunnarsson et al., 2004). While selenium intake seemed sufficient in Iceland in 2002, selenium intake can change rapidly in a population due to changing concentration in foods resulting from altered feeding practices, changes in fertilizers or food imports. It is therefore of great importance to monitor the levels of this trace element in the food supply. Milk, dairy products and meat have traditionally played a very important role in the daily food of most Icelanders. Lamb has been by far the most commonly consumed meat in Iceland and still it amounts to about half of all meat consumed in the country. Skyr is a type of fresh cheese that evolved in Iceland early on as a way of preserving milk and maximizing its food value. It is made from skimmed milk and live cultures, the product is left to coagulate and skyr whey is removed as a by-product. In the old days each farm made its own skyr. When dairy plants were established early in the 20th century skyr became one of the most important dairy products in Iceland. The traditional skyr was produced by filtration of coagulate on linen cloth. In modern dairies the process has been modified and made more efficient by including centrifugation and ultrafiltration (Hilmarsdottir and Arnadottir, 1989). Data on minerals and trace elements in food from Icelandic agriculture have been limited. Specifically information has been lacking on processing effects on elements in dairy products like skyr. Also, the feeding strategies of agriculture have changed during the last decade, making updating of food data crucial. The aim of this study was to update the Icelandic Food Composition Database with respect to minerals (Ca, K, Mg, Na, and P) and trace elements (Cu, Fe, Hg, Se, and Zn) in frequently consumed agricultural products and to study the seasonal and geographical variation for these elements. This work was carried out to make studies on the mineral and trace element intake of Icelanders possible. 2. Materials and methods 2.1. Samples Whole pasteurized and packaged (paperboard containers) milk was sampled in two dairies (MS Dairy Selfoss South-Iceland and MS Dairy Akureyri North-Iceland) during winter (January and March 2008) and summer (June and August 2008). Both dairies
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process milk from all dairy farmers in the region during two consecutive days. Sampling was carried out on Wednesdays and Thursdays in the last week of the indicated months. Five 1 L samples were collected over the entire milk processing period each day. A composite sample was made from 10 primary samples for each dairy and month. The two dairies process about 90% of the whole pasteurized and packaged milk in the country. The milk production is based on one cattle breed. Industrially produced skyr was sampled at the MS Dairy Selfoss in January, March and August 2008. Each time skyr was collected from three processing lots/days making one composite sample (6 kg, plastic containers). The skyr was made from skimmed milk that was pasteurized and subsequently cooled down and incubated with cultures. Whey was removed by ultrafiltration retaining valuable whey proteins in the skyr. Skyr whey, skimmed milk, cream and whole milk were also collected from the same three processing lots as the skyr and production quantities recorded to investigate distribution of nutrients between skyr and whey. Samples of skimmed milk, cream and whole milk were pasteurized and packaged (paperboard containers) products, 3 kg per composite samples of skimmed milk and whole milk and 1.5 kg per composite sample of cream. Traditionally produced skyr and skyr whey were sampled in March, June and August 2008 at the MS Dairy Akureyri. Each time a composite sample was made from three processing lots/days (1.5 kg skyr and 3 kg whey per composite sample, plastic containers). Traditional skyr was produced by the old method using incubation with rennet and old skyr and finally cloth filtration to separate the curd (skyr) and the skyr whey. The sampled foods are defined in Table 1. Gouda cheese, cheese whey and pasteurized cheese milk were sampled in January, March and August 2008 at the MS Dairy Akureyri, each time from two processing lots for one composite sample (3 kg cheese, 4 kg whey and milk). The cheese samples were collected twice: after pressing (two days old) and after ripening for about 3 months. The whey collected was the first whey used for cheese spread production. A cheese spread made by concentrating cheese whey by heating and evaporation and adding skimmed milk, cream and sugar, was sampled during winter and summer from three production lots each time. Lamb meat was sampled from four regions in slaughterhouses during the annual slaughter season September–October 2008. All sheep in the country originate from the same Icelandic breed. Each sample consisted of three legs of lamb from three carcasses from the same farm. Farms were selected randomly but lamb numbers were recorded and information regarding the farm was studied later. The lamb legs were defatted and deboned before homogenization. Beef was grade UNI minced meat from the whole carcass, except fillet, leg, topside and thick flank, sampled in March and October 2008. Each beef sample consisted of 5 subsamples (500 g each) collected during one day at a meat processing plant. Several
Table 1 Description of food samples. English name
Original name
Comments
LanguaL codea
Whole milk Cream Skimmed milk Skyr, industrial Skyr whey, industrial Skyr, traditional Skyr whey, traditional Cheese, Gouda Cheese whey Cheese spread from whey Lamb leg Beef, minced
Ny´mjo´lk Rjo´mi Undanrenna Skyr Skyrmysa Skyr, hefðbundið Skyrmysa, hefðbundin Ostur, Gouda Ostamysa Mysingur Lambalæri Nautgripahakk
Fat 4 g/100 g Fat 36 g/100 g Fat 0.8 g/100 g Semisolid yoghurt-like cheese. Fat 0.3 g/100 g Fat 0.3 g/100 g. Semisolid yoghurt-like cheese. Fat 0.3 g/100 g. Fat 0.3 g/100 g. Fat 26 g/100 g Fat 0.3 g/100 g. Fat 8 g/100 g. Defatted, fat about 6 g/100 g. Fat 6–16 g/100 g
A0780 A0782 A0780 A0786 A0783 A0786 A0783 A0785 A0783 A0786 A0794 A0794
a
LanguaL is a method for describing, capturing and retrieving data about food (LanguaL, 2010).
B1201 B1201 B1201 B1201 B1201 B1201 B1201 B1201 B1201 B1201 B1669 B1161
C0235 C0161 C0235 C0245 C0244 C0245 C0244 C0245 C0244 C0244 C0266 C0270
E0123 E0139 E0123 E0119 E0109 E0119 E0109 E0151 E0109 E0119 E0150 E0117
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carcasses were processed for each sample; the total number of carcasses was 58 for all 10 beef samples. Samples were collected from four processing plants representing about 70% of the minced beef produced in the country. Meat samples were kept frozen until they were homogenized. Dairy samples were refrigerated, transported to Matis the day after sampling and prepared immediately for analysis. 2.2. Sample preparation Meat samples were homogenized in a stainless steel rotating knife homogenizer (Tecator 1094; Foss, Hillerod, Denmark). Liquid dairy samples were mixed by pouring the contents of all 1 L packages four times between containers. Skyr samples were mixed in plastic bags. Cheese samples were cut into small cubes, mixed in plastic bags and homogenized in a homogenizer (Tecator 1094). All containers and equipments were made from either plastic or stainless steel. Containers and equipments were washed by a solution of 2% sodium EDTA (>95% purity; Sigma–Aldrich, Steinheim, Germany) and 2% sodium citrate (>98.5% purity, Sigma–Aldrich) to remove ions. Finally all surfaces were washed by Milli-Q water (18.2 MV cm quality; Millipore SAS, Molsheim, France) before contact with samples. 2.3. Analysis Total selenium and other elements (Ca, Cu, Fe, Hg, K, Mg, Na, P, and Zn) concentrations in the dairy and meat samples were determined by an inductively coupled plasma mass spectrometer (ICP-MS) (Agilent 7500ce; Agilent Technologies, Waldbronn, Germany) with an octopole based collision/reaction cell in the full quantitative mode. Helium and hydrogen gases were used as collision and reaction gases, respectively. Argon was used as sample introduction and plasma gas. All gases were 99.999% pure and were supplied by ISAGA (Reykjavik, Iceland). Prior to analysis for total element concentrations a complete destruction of the organic matrix of homogenized samples is required and during the mineralization process all organic element compounds were converted into inorganic elements. Therefore, the samples were microwave digested (MARS microwave oven; CEM, Matthews, USA) with HNO3 (Suprapure, Merck, Darmstadt, Germany) and H2O2 (TraceSelect Ultra; Sigma–Aldrich) at up to 220 8C for 15– 30 min in closed vessels. Digested samples were diluted appropriately with ultra-pure laboratory Milli-Q water (18.2 MV cm quality; Millipore SAS). The sample digests were kept frozen at 20 8C until ICP-MS analysis. Each sample was digested in triplicate and analyses were carried out once on each digest. The ICP-MS instrument was tuned daily by 1 mg L 1 tuning
Table 2 Operating conditions for measurements with inductively coupled plasma mass spectrometer. Masses
23 (Na)c, 24 (Mg)c, 31 (P)a, 39 (K)b, 43 (Ca)a, 56 (Fe)b, 63 (Cu)a, 66 (Zn)a, 78 (Se)b, 202 (Hg)c
Integration time Radio frequency (RF) power Skimmer cone Spray chamber temperature Plasma gas (Ar) Nebulizer gas (Ar) Make-up gas (Ar) Collision gas (He) Reaction gas (H2) Nebulizer Sample delivery Replicates
0.1 s 1500 W Ni 2 8C 15 L min 1 0.9 L min 1 0.16 L min 1 3.9 L min 1 3.5 L min 1 Micromist About 0.5 mL min 3
a b c
1
He mode. H2 mode. Nogas mode.
solution. ICP-MS operation conditions are reported in Table 2. The elements Cu, Fe, Hg, Se and Zn were analysed simultaneously. Digested samples were further diluted for macro-minerals (Ca, K, Mg, Na, and P) analysis. Monoelemental, high purity grade 1 g L 1 standard stock solutions of Ca, Cu, Fe, Hg, K, Mg, Na, P, Se and Zn were purchased from CPI International (Amsterdam, The Netherlands). In order to check the trueness of the analysis, certified reference materials skim milk powder (CRM 063R) and bovine muscle (CRM 184) from the Institute for Reference Materials and Measurements (IRMM, Geel, Belgium) were analysed. Good agreement was obtained between certified and analysed values for the elements measured (see Table 3 for details). Element recovery tests were carried out with beef, skimmed milk and skyr by adding standards. The average elemental recovery in these three matrixes ranged between 91 and 108%. Water content of all samples was calculated from the weight loss during drying at 103 2 8C for 4 h (ISO, 1999). Protein was determined by the Kjeldahl method (ISO, 2005). Samples were digested in sulphuric acid (>98.5% purity; Sigma–Aldrich) in the presence of technical grade CuSO4 catalyst (Foss Analytical AB, Ho¨ganas, Sweden). The solution was made alkaline by technical grade NaOH (JSC, Volgograd, Russia) and the released ammonia was distilled in a distillation unit (2400 Kjeltec Analyzer, Foss) into boric acid (>98.5% purity; Sigma–Aldrich) solution which was then titrated with H2SO4 to determine the nitrogen content. The determined nitrogen content was multiplied by 6.25 for meat and 6.38 for dairy products to report protein content. Each sample was digested in
Table 3 Certified and found values for certified reference materials (CRM) (mean standard deviation). Element
Unit
Ca P Mg K Na Se Zn Fe Cu Hg
g/kg g/kg g/kg g/kg g/kg mg/kg mg/kg mg/kg mg/kg mg/kg
Skim milk powder CRM 063Ra
Bovine muscle CRM 184a
Certified value
Found value n = 18
Certified value
Found value n = 9
13.49 0.10 11.10 0.13 1.263 0.024 17.68 0.19 4.37 0.031 (129) 49.0 0.6 2.32 0.23 0.602 0.019 NAc
13.74 0.35 10.88 0.53 1.241 0.093 16.55 1.65 4.16 0.23 132 7 48.7 1.5 2.29 0.10 0.574 0.014 <3
(0.15)b (8.3) (1.02) (16.6) (2.0) 183 12 166 3 79 2 2.36 0.06 2.6 0.6
0.14 0.02 8.79 0.45 1.03 0.37 16.89 1.65 2.02 0.03 181 4 167.3 0.9 78.2 1.2 2.31 0.02 <3
n = number of samples. a Institute for Reference Materials and Measurements (Geel, Belgium). b Values in brackets are not certified. c Not reported.
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Table 4 Water, protein and mineral values per 100 g fresh dairy products (mean standard deviation). Product
n
Water (g/100 g)
Protein N 6.38 (g/100 g)
Ca (mg/100 g)
P (mg/100 g)
Mg (mg/100 g)
K (mg/100 g)
Na (mg/100 g)
Whole milk summer Whole milk winter Whole milk for skyr Cream Skimmed milk Skyr, industrial Skyr whey, industrial Skyr traditional Skyr whey traditional Milk for cheese Cheese, Gouda, 2nd day Cheese, Gouda, ripe Cheese whey Cheese spread from whey
4 4 3 3 3 3 3 3 3 3 3 3 3 2
87.3 0.1 87.7 0.2 87.5 0.1 57.8 0.4 91.2 0.1 83.1 0.3 94.6 0.1 81.6 0.2 94.1 0.1 88.8 0.6 43.5 0.3 42.8 0.5 93.4 0.1 32.3
3.27 0.09 3.30 0.09 3.34 0.04 2.22 0.07 3.43 0.05 11.2 0.4 0.22 0.01 13.1 0.5 0.41 0.00 3.40 0.06 25.0 0.1 25.0 0.3 0.94 0.02 8.78
126 5 114 5 114 11 67.6 8.5 107 6 100 7 109 6 85.0 4.8 108 9 118 9 732 9 788 17 34.9 1.2 261
124 3 123 8 125 6 78 4 116 3 192 21 88 10 190 26 84 9 124 1 479 14 503 37 51 8 361
9.63 0.61 9.98 0.30 9.60 0.61 5.43 0.51 8.87 0.32 9.37 1.10 8.37 0.93 8.67 1.22 8.30 0.92 10.1 0.6 29.7 1.0 33.5 2.4 6.33 0.72 51.6
144 5 146 5 146 2 92 5 142 2 123 14 145 17 114 15 132 16 152 6 80 3 88 7 140 13 1040
40.1 1.6 38.8 2.5 39.9 2.8 25.6 2.5 38.8 2.4 32.0 1.8 39.8 3.3 27.9 3.3 35.7 3.0 40.0 2.0 419 97 618 36 39.5 1.7 315
n = number of samples.
duplicate for protein analysis. Phosphorus was determined by colorimetry as phosphate vanadomolybdate at 420 nm (AOAC, 1990) for comparison to the ICP-MS data. For measurements of water, protein and phosphorus duplicate analysis of each sample was carried out. Reference material was analysed for phosphorus (skim milk powder, CRM 063R, IRMM). Methods for water and protein were accredited for fish. Protein measurements were tested by participation in proficiency measurements which gave 64.89 g protein/100 g fish meal compared to the average of 64.49 g/100 g for the 18 participants. 2.4. Statistical analysis Statistical analysis was performed using the Number Cruncher Statistical System 2000 (NCSS) software (Kaysville, UT, USA). Analysis of variance was used to determine significance difference among areas, periods or production methods. 3. Results and discussion 3.1. Dairy products Data for water, protein, minerals and trace elements in dairy products are shown in Tables 4 and 5. The products are whole pasteurized milk, industrially produced skyr (semisolid yoghurtlike cheese) and Gouda cheese together with milk, skimmed milk and cream used in the production of industrial skyr and cheese. The by-products skyr whey and cheese whey are included together with cheese spread made from cheese whey. Traditional skyr and skyr whey are also included for comparison. The foods
are defined in Table 1 by names, descriptions and LanguaL codes. LanguaL is a method for describing, capturing and retrieving data about food (LanguaL, 2010) used increasingly in Europe and internationally. The dairy products are important sources of calcium, phosphorus and selenium. Mercury in dairy samples was below the detection limit of 0.3 mg/100 g except for one ripe cheese sample which contained 1.4 mg Hg/100 g. The European Union legislation on food has been adapted in Iceland and in the present legislation there are no maximum levels for Hg in the foods reported in this paper. The concentrations of iron, copper and zinc in the dairy products were low. Whole pasteurized summer milk and winter milk from two regions were compared. Significant geographical variation was only found for selenium (p < 0.05). Significant seasonal variation was found for selenium (p < 0.005) and moisture (p < 0.05). On dry weight basis significant difference was found only for selenium (p < 0.005). Higher selenium in the winter milk can be explained by more selenium supplemented feeds given to the cows during winter. Skyr is made from skimmed milk and is rich in protein but low in fat. Fat has been determined as 0.25 0.11 g/100 g (Matis, 2010). Skyr produced by two methods (industrial and traditional) was compared. Significant difference (p < 0.05) between methods was found for protein, water, calcium, iron and selenium. Traditional skyr contains more protein and selenium but less calcium than the industrial skyr. The difference between industrial and traditional skyr can be explained by different filtering methods and water content. The traditional skyr is filtered to a greater extent thus more protein and Se are retained within the product on
Table 5 Trace element values per 100 g fresh dairy products (mean standard deviation). Product
n
Se (mg/100 g)
Zn (mg/100 g)
Fe (mg/100 g)
Cu (mg/100 g)
Hg (mg/100 g)
Whole milk, summer Whole milk, winter Whole milk for skyr Cream Skimmed milk Skyr, industrial Skyr whey, industrial Skyr, traditional Skyr whey, traditional Milk for cheese Cheese, Gouda, 2nd day Cheese, Gouda, ripe Cheese whey Cheese spread from whey
4 4 3 3 3 3 3 3 3 3 3 3 3 2
2.15 0.13 2.63 0.15 2.17 0.31 2.53 0.38 1.83 0.21 6.43 1.10 <0.3 9.70 1.25 <0.3–0.3 2.57 0.23 19.0 2.7 21.6 2.6 0.63 0.06 6.80
0.433 0.050 0.389 0.016 0.419 0.024 0.246 0.011 0.474 0.056 0.521 0.061 0.374 0.033 0.448 0.019 0.399 0.031 0.380 0.002 3.62 0.127 3.61 0.292 0.013 0.009 0.262
0.027 0.004 0.020 0.001 0.023 0.004 0.050 0.002 0.020 0.001 0.045 0.005 0.016 0.002 0.065 0.004 0.008 0.002 0.024 0.004 0.133 0.008 0.139 0.023 0.014 0.003 0.102
0.0041 0.0005 0.0042 0.0006 0.0046 0.001 0.0043 0.0009 0.0060 0.0001 0.0157 0.0031 0.0010 0.0003 0.0158 0.0032 0.0009 0.0002 0.0036 0.0003 0.0261 0.0055 0.0266 0.0080 0.0016 0.0003 0.0122
<0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3–1.4 <0.3 <0.3
n = number of samples.
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Table 6 Water, protein and mineral values per 100 g fresh meat (mean standard deviation). Product
n
Water (g/100 g)
Lamb leg, South-Iceland Lamb leg, West-Iceland Lamb leg, Northwest-Iceland Lamb leg, Northeast-Iceland Lamb leg, all samples Beef, minced Beef, minced, fibre added Beef, minced, all samples
3 3 3 3 12 7 3 10
71.5 1.2 71.0 0.5 69.0 1.4 71.8 0.9 70.8 1.5 68.8 3.1 70.4 2.7 69.3 2.9
Protein N 6.25 (g/100 g)
Ca (mg/100 g)
P (mg/100 g)
Mg (mg/100 g)
K (mg/100 g)
Na (mg/100 g)
20.7 0.7 17.6 0.8 19.7 1.6
5.1 0.7 5.1 0.4 8.9 3.9 3.8 0.3 5.7 2.6 5.7 0.8 7.0 0.7 6.1 1.0
232 8 218 12 227 6 197 13 219 17 194 6 162 4 184 16
21.3 0.8 20.0 1.7 20.4 0.6 18.3 0.6 20.0 1.4 17.4 0.6 15.4 0.6 16.8 1.1
334 11 321 9 313 10 313 8 320 12 273 8 265 14 271 10
46.8 2.7 45.8 1.4 44.5 1.2 47.1 3.0 46.1 2.2 68.7 9.3 106 7 79.8 20
n = number of samples.
a weight basis than in the industrially produced skyr. The ultrafiltration used by the dairy industry retains more calcium than the traditional filtering of coagulate through fabric. Skyr whey is a nutritious product, almost as rich in calcium, zinc and potassium as whole milk. This product could be used more by the Icelandic food industry. Gouda cheese is very rich in calcium, phosphorus and selenium. The Gouda cheese retains zinc very well since zinc concentration of the whey is very low. The composition of ripe cheese and cheese samples after 2 days is similar except for the higher sodium content of the ripe cheese. The cheese whey is rich in minerals, especially potassium which is similar to whole milk. The K/Na ratio is 3.5 for the whey while it is 0.1 for the ripe cheese. Cheese whey spread is made by concentrating the cheese whey and adding skimmed milk, cream and sugar. The spread is therefore very rich in minerals and trace elements, containing 7–20 times more minerals and trace elements than the whey. The composition of the spread did not differ between one winter sample and one summer sample. Selenium content of Icelandic whole milk and cheese was higher than values reported from low selenium areas (Lindmark-Ma˚nsson et al., 2003; Barclay et al., 1995; NavarroAlarcon and Cabrera-Vique, 2008). Selenium is added to the feeds of milking cows in Iceland and this most likely explains the relatively high levels found. The concentrations of iron and copper in the dairy products were very low. Phosphorus in Icelandic whole milk is about 30% higher than reported earlier for Icelandic milk and Swedish milk (Lindmark-Ma˚nsson et al., 2003). This could be explained by the magnesium phosphate and calcium phosphate that are now added to the feeds for milking cows. The phosphorus content of these feeds is about 1%. Earlier determinations of phosphorus in milk have generally used colorimetric methods for the determination of phosphorus. Therefore the determination of phosphorus of four milk samples was repeated with the colorimetric method. Results were lower than when ICP-MS was used for the quantification of phosphorus and within the range reported earlier for Icelandic milk. Phosphorus determined by the colorimetric method in a reference material (Skim milk powder CRM 063R) was 93% of the certified value. The colorimetric
method thus might underestimate the phosphorus content in dairy products. During the processing of industrial skyr and Gouda cheese all products and by-products were sampled and production quantities recorded. The distribution of skimmed milk proteins, minerals and trace elements between skyr and whey was studied. The proteins of the skimmed milk are retained in skyr which contains about 11 g protein per 100 g, while whey contains only 0.22 g protein/100 g. The total amount of selenium in skimmed milk is almost exclusively captured in the skyr. Strong association of selenium with the casein fraction is well known (Rodriguez Rodriguez et al., 2002). During the skyr production pH drops to about 4.5 making minerals more soluble. Considerable parts of the amounts of some elements in the skimmed milk are found in the skyr whey (average of three determinations SD): calcium 72 1%, phosphorus 52 1%, magnesium 68 0.3%, potassium 74 0.1%, sodium 75 1% and zinc 63 3%. It can thus be concluded that industrial skyr whey is rich in minerals and zinc. The composition of cheese whey and skyr whey differs considerably. The skyr whey contains more calcium (p < 0.005), magnesium (p < 0.05), phosphorus (p < 0.05), and zinc (p < 0.005) than the cheese whey. This can be explained by the lower pH during skyr production (pH 4.5) than during the Gouda cheese production (pH 5.2). The concentration of potassium and sodium is similar in all samples of whey, whole milk and skimmed milk. These minerals are known to be essentially diffusible in whole milk whereas calcium (70%), phosphate (50%) and magnesium (40%) are partially bound to the casein micelles (Mekmane et al., 2009). 3.2. Meat Data for lamb and beef are present in Tables 6 and 7. Little variation is found in the composition of lamb between the four areas with the exception of selenium which shows a range of 2.9– 11.7 mg/100 g. On dry weight basis significant geographical differences (p < 0.05) are only found for selenium in lamb. There are also considerable differences for selenium within regions. Lamb meat is a rich source of protein, iron, phosphorus and zinc. Mercury was below detection limit (0.3 mg/100 g) for all samples.
Table 7 Trace element values per 100 g fresh meat (mean standard deviation). Product
n
Se (mg/100 g)
Zn (mg/100 g)
Fe (mg/100 g)
Cu (mg/100 g)
Hg (mg/100 g)
Lamb leg, South-Iceland Lamb leg, West-Iceland Lamb leg, Northwest-Iceland Lamb leg, Northeast-Iceland Lamb leg, all samples Beef, minced Beef, minced, fibre added Beef, minced, all samples
3 3 3 3 12 7 3 10
4.8 2.8 10.8 2.6 7.5 3.3 10.9 1.3 8.5 3.5 3.4 1.9 4.8 4.1 3.8 2.6
2.79 0.21 2.79 0.06 3.02 0.13 2.63 0.07 2.81 0.18 4.08 0.52 3.49 0.09 3.91 0.51
1.43 0.11 1.51 0.11 1.58 0.06 1.54 0.05 1.52 0.09 1.76 0.17 1.60 0.20 1.71 0.18
0.097 0.005 0.095 0.001 0.095 0.007 0.094 0.002 0.096 0.004 0.047 0.006 0.047 0.002 0.047 0.005
<0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3 <0.3
n = number of samples.
O. Reykdal et al. / Journal of Food Composition and Analysis 24 (2011) 980–986
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Table 8 Comparison of levels (mg/100 g fresh weight) of selenium in meat in some countries. Meat
Country
n
Beef minced Beef Beef Beef Beef steak Lamb leg Lamb Lamb Lamb Lamb chop
Iceland UK Ireland Denmark Australia Iceland UK Ireland Denmark Australia
10 4 14 48 6 12 4 16 9 2
Se (mg/100 g)
Source
Mean
Range
3.8 7.6 8.1 9.3 20 8.5 3.8 8.8 6.1 22
1.4–9.6 6.8–8.4 6.1–10.5 <4–14.8 17–21 2.9–13.8 2.9–4.7 7.1–10.9 <4–11.1 20–23
Present study Barclay et al. (1995) Murphy and Cashman (2001) Larsen et al. (2002) Tinggi et al. (1992) Present study Barclay et al. (1995) Murphy and Cashman (2001) Larsen et al. (2002) Tinggi et al. (1992)
n = number of samples.
This is consistent with very low mercury concentrations reported for Icelandic lamb organs (Reykdal and Thorlacius, 2001). The nutrient profile of minced beef differed between processing plants. Samples from one of the plants were minced beef with potato fibre added and contained significantly (p < 0.05) less protein and more sodium than minced beef from the other plants. Fibre plus carbohydrates estimated as difference (100 sum of water, protein, fat and ash values) were 2.1 0.4 g/100 g for minced beef with added fibre while it was 0.0 g/100 g for minced beef from other plants. Selenium in the minced beef samples was very variable (1.4–9.6 mg/100 g). Mercury for minced beef was below the detection limit (0.3 mg/100 g). Selenium concentration was generally considerably higher in Icelandic lamb than in beef (p < 0.005). For UK data (Barclay et al., 1995) the order was different, there beef had higher selenium concentrations than lamb. Table 8 compares selenium levels reported for beef and lamb in five countries. The table shows that selenium concentration for Icelandic beef is low compared to data from the other countries. Low selenium concentrations in Icelandic beef can most likely be explained by the low concentration of selenium in Icelandic hay (Johannesson et al., 2007) and limited use of selenium supplemented feeds. Lambs graze in the Icelandic highlands until slaughtered and depend on availability of the element from plants and soil. It has been reported that selenium concentration is higher in plants in the highlands than in hay from cultivated areas (Johannesson et al., 2007). This is the most likely explanation for the higher concentration of selenium in lamb meat than beef in Iceland. Selenium concentration in Icelandic lamb is comparable to levels found in some other countries (Table 8). 4. Conclusions Iceland is a low selenium area due to poor availability of selenium from soil. Nevertheless, agricultural food products show quite variable selenium levels. Selenium in milk is maintained by adding selenium to the feed. Beef, on the other hand, is very low in selenium reflecting limited selenium in the feed. Lamb is higher in selenium than beef (p < 0.005) but concentration of selenium in both beef and lamb is very variable. Mercury is below the detection limit except for one sample of cheese. Skyr is a nutritious product, rich in protein, calcium, phosphorus and selenium but very low in fat. It is noteworthy that skyr retains almost all the selenium in the skimmed milk used for its production. Skyr whey contains more calcium (p < 0.005), magnesium (p < 0.05), phosphorus (p < 0.05), and zinc (p < 0.005) than cheese whey and could be used more extensively for food production. Composition of lamb meat shows little variation except for selenium. Icelandic lambs graze their whole lifetime in the wild.
Consequently the variation in selenium concentration reflects natural geographical variety of plants and soils with respect to selenium. The composition of beef samples was variable and reflects the trend in the meat industry to add carbohydrates, fibre and water to the meat products. Due to the variability of selenium in the food supply, its concentration should be monitored in food and feed.
Acknowledgments This work was supported by the Icelandic Agricultural Productivity Fund, Matis ohf and the Agricultural University of Iceland. Olafur Unnarsson at the MS Dairy Selfoss, Kristin Halldorsdottir at MS Dairy Akureyri and Oli Thor Hilmarsson at Matis are greatly acknowledged for their work on sampling and valuable advice. References AOAC, 1990. Phosphorus (total) in meat. In: Helrich, K. (Ed.), Official Methods of Analysis of the Association of Official Analytical Chemists. 15th ed. Association of Official Analytical Chemists, Arlington, USA, Method No. 969.31. Barclay, M.N.I., MacPherson, A., Dixon, J., 1995. Selenium content of a range of UK foods. Journal of Food Composition and Analysis 8, 307–318. Debes, F., Budtz-Jørgensen, E., Weihe, P., White, R.F., Grandjean, P., 2006. Impact of prenatal methylmercury exposure on neurobehavioral function at age 14 years. Neurotoxicology and Teratology 28, 363–375. Ekholm, P., Reinivuo, H., Mattila, P., Pakkala, H., Koponen, J., Happonen, A., Hellstro¨m, J., Ovaskainen, M.-L., 2007. Changes in the mineral and trace element contents of cereals, fruits and vegetables in Finland. Journal of Food Composition and Analysis 20, 487–495. Gunnarsson, B.S, Thorsdottir, I., Palsson, G., 2004. Iron status in 2-year-old Icelandic children and associations with dietary intake and growth. European Journal of Clinical Nutrition 58, 901–906. Hilmarsdottir, E., Arnadottir, A.T., 1989. Nutritional effects of pickle fermentation of blood and liver sausages in skyr whey. In: Somogyi, J.C., Mu¨ller, H.R. (Eds.), Nutritional Impact of Food Processing, Bibliotheca Nutritio et Dieta, No. 43. Karger, Basel, Switzerland, pp. 47–58. ISO, 1999. Determination of moisture and other volatile matter content. In: ISO Standard 6496, The International Organization for Standardization, Geneva, Switzerland. ISO, 2005. Determination of nitrogen content and calculation of crude protein content. In: ISO Standard 5983, The International Organization for Standardization, Geneva, Switzerland. Johannesson, T., Eiriksson, T., Gudmundsdottir, K.B., Sigurdarson, S., Kristinsson, J., 2007. Overview. Seven trace elements in Icelandic forage. Their value in animal health and with special relation to scrapie. Icelandic Agricultural Sciences 20, 3–24. LanguaL International Framework for Food Description, LanguaL Food Description Thesaurus, 2010, Retrieved March 31, 2010 from the Langual Home Page: http://www.langual.org Larsen, E.H., Andersen, N.L., Møller, A., Petersen, A., Mortensen, G.K., Petersen, J., 2002. Monitoring the content and intake of trace elements from food in Denmark. Food Additives and Contaminants 19 (1), 33–46. Levenson, C.W., Axelrad, D.M., 2006. Too much of a good thing? Update on fish consumption and mercury exposure. Nutrition Reviews 64, 139–145. Lindmark-Ma˚nsson, H., Fonde´n, R., Pettersson, H.-E., 2003. Composition of Swedish dairy milk. International Dairy Journal 13, 409–425.
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