Trace Metals And Micronutrients In Bone Tissues Of The Red .
View metadata, citation and similar papers at core.ac.ukbrought to you byCOREprovided by PubMed CentralActa Theriol (2012) 57:233–244DOI 10.1007/s13364-012-0073-1ORIGINAL PAPERTrace metals and micronutrients in bone tissues of the red foxVulpes vulpes (L., 1758)Natalia Lanocha & Elzbieta Kalisinska &Danuta I. Kosik-Bogacka & Halina Budis &Kinga Noga-DerenReceived: 26 October 2011 / Accepted: 25 January 2012 / Published online: 10 February 2012# The Author(s) 2012. This article is published with open access at Springerlink.comAbstract In this study we determined the levels of traceelements (zinc, copper, lead, cadmium and mercury) in threelayers of bones of the hip joint (cartilage, compact bone andspongy bone) of 30 red foxes (Vulpes vulpes) from northwestern Poland. Concentrations of Cu, Zn, Pb and Cd weredetermined by atomic absorption spectrophotometry (ICPAES) in inductively coupled argon plasma using a PerkinElmer Optima 2000 DV. Determination of Hg concentrationwas performed by atomic absorption spectroscopy. In cartilage, compact bone and spongy bone samples from the redfox, median concentrations of the metals studied could bearranged in the following descending series: Zn Cu Pb Cd Hg, the values ranging from 142 to 0.002 mg/kg dw.There was a significant difference in Cu concentrations,among all the materials analyzed, with much more Cu foundin spongy bone than in compact bone. Significant differences were also noted in the case of Hg concentrations incartilage with compact bone and the spongy bone, andbetween concentrations of this metal in compact bone andspongy bone. In males, the concentration of Hg in spongybone was greater than in females. Younger foxes had ahigher concentration of this metal in cartilage than adults.The strongest synergistic relationships were observed inCommunicated by: Danuta I. Kosik-BogackaN. Lanocha : E. Kalisinska : D. I. Kosik-Bogacka (*) : H. BudisDepartment of Biology and Medical Parasitology,Pomeranian Medical University of Szczecin,Powstancow Wielkopolskich 72,70-111 Szczecin, Polande-mail: kodan@pum.edu.plK. Noga-DerenDepartment of Preclinical Conservative Dentistry and PreclinicalEndodontics, Pomeranian Medical University of Szczecin,Powstancow Wielkopolskich 72,70-111 Szczecin, Polandspongy bone between the Zn and Cu, Zn and Cd, as wellas between Cu and Cd. Statistically significant antagonisticrelationships were detected between zinc and lead in compact bone. In addition to monitoring studies conducted onthe abiotic environment, an urgent need exists for long-termmonitoring of concentrations of heavy metals with longterm effects on living organisms. An important addition isprovided by biomonitoring studies on domesticated andfree-living mammals, including Canidae.Keywords Red fox . Bioindicator . Bone tissue . TraceelementsIntroductionRepresentatives of Canidae, namely the red fox Vulpes vulpes(Linnaeus, 1758), the domesticated dog Canis lupus familiaris(Linnaeus, 1758), the wild raccoon dog Nyctereutes procyonoides (Gray 1834), and the wolf Canis lupus (Linnaeus,1758), are all common objects of ecotoxicological studies(Kalisinska et al. 2009; 2011; Millan et al. 2008; Shore et al.2001).The fox belongs to a group of hunted mammals commonly found in Eurasia and North America. It is a predatorpreferring food of animal origin including rodents, birds andsmall invertebrates (beetles, grubs, earthworms) (Kidawaand Kowalczyk 2011). The species occupies a high positionin the food pyramid and accumulates ingested substances. Italso exhibits a measurable response to environmental contaminants, including heavy metals (Kalisinska et al. 2009;2011; Lopez-Alonso et al. 2007).Many reports mention the neuro-, nephro- or hepatotoxiceffects of exposure to trace elements, but publications on theaccumulation of trace elements (including zinc, copper, lead,
234cadmium and mercury) in cartilage and bone elements ofhuman and animal joints are much less numerous (BrodziakDopierala et al. 2007; Jankovska et al. 2010; Kalisinska et al.2007; Kwapulinski et al. 1995; Piskorova et al. 2003).We examined bone tissues of the red fox in a risk assessment of exposure to trace elements, as they are subject to slowtransfer of some metals in the body. Due to its characteristicsand long renewal time, this tissue may reflect levels of chronicexposure and could be the basis of indirect environmentalassessment (Brodziak-Dopierala et al. 2007; 2009; Zaichickand Zaichick 2009; 2010; Zaichick et al. 2011).Zinc (Zn) and copper (Cu)Zinc and copper are involved in the formation and metabolism of bone tissue (Honda et al. 1997; Nielsen and Milne2004; Senczuk 2006; Yamaguchi 1998).Zinc is essential for the correct ossification and mineralization of bones, especially in the basal part of the femur. Itis a cofactor for the enzyme affecting the synthesis ofvarious ossein components and plays a role in the regulationof bone resorption (Machalinski et al. 1996; NRC 1980;Puzanowska-Tarasiewicz et al. 2009; Smrcka 2005). Bothtoo high and too low concentrations of Zn contribute to thegradual reduction of bone mass and reduce the concentration of calcium ions in bones and blood serum (Charles et al.2001).Copper in mammals is involved in the process of thehardening of collagen, hair keratinization and also normalizesthe deposition of calcium and phosphorus in bones. Cooperinhibits bone resorption, which may occur due to a reductionin prostaglandin synthesis (Senczuk 2006). Copper deficiencyleads to reduced bone mass, resulting in a decrease in itsmechanical strength and subsequent fractures.Studies on Cu and Zn supplementation in humans andanimals indicate that a deficiency of these micronutrientsleads to osteoporosis-like changes (Nielsen and Milne2004).Lead (Pb), cadmium (Cd) and mercury (Hg)The presence of Pb, Cd and Hg have been detected in alltissues of mammals, and even minimum concentrationshave been observed to cause metabolic disturbances, thusreducing physical efficiency, weakening immune and enzymatic processes, and leading to many diseases and sometimesdeath.Lead toxicity is manifested in anemia, impaired nervoussystem and kidney function and changes in bones such asdecreased bone mass (osteopenia) and delayed healing offractures (Gerhardsson et al. 2005; Kjellstrom 1992; Wiechulaet al. 2008). Accumulation of Pb in bone, in contrast to solidorgans, increases with age (Jurkiewicz et al. 2004).Acta Theriol (2012) 57:233–244Cadmium has mainly nephro- and hepatotoxic properties.The osteotoxic action of Cd was described in Japan as earlyas 1960 in 90% of older women (after menopause and manypregnancies) living in areas contaminated with Pb and Znores. The disease was called "Itai-Itai" (ouch-ouch disease).First, it was observed in the Japanese population of the JinzuRiver overflow area, consuming mainly rice grown in fieldsfertilized with silt derived from local plants (Starek 2007;Zhu et al. 2004). The concentration of Cd in that soil was8 mg/kg dw, and in rice up to 2.7 mg/kg. The patients hadosteomalacia resistant to vitamin D, accompanied by severepain around the sacrum, the lower limbs and ribs, spontaneous fractures, as well as proteinuria, glycosuria and decreased sodium reabsorption (Bernard 2008; Horiguchi et al.2010; Jarup and Akesson 2009; Umemura and Wako 2006).Mercury is a potent neurotoxin, primarily disrupting thefunction of the central and peripheral nervous system(Scheuhammer et al. 2008). However, individual studieshave drawn attention to the deposition of this metal inskeletal elements (Yoo et al. 2002; Zaichick and Zaichick2010; Zaichick et al. 2011).The determination of toxic element concentrations inliving organisms is one of the basic methods of indirectassessment of environmental pollution. Ecotoxicologicalstudies in Poland and the rest of the world are usuallycarried out on the liver and kidneys of warm-blooded vertebrates. However, there has been an increasing number ofbiomonitoring studies on bones. Apart from environmentalstudies, a large need exists for the monitoring of concentrations of heavy metals in humans, which can be supplemented with biomonitoring of both domesticated animals(such as the pig, sheep, cattle, horse and dog) and wildanimals (e.g., fox, boar, roe deer and deer) (Kalisinska etal. 2009; Lanocha et al. 2009; Lazarus et al. 2008; Liu2003).The aim of this study was to determine the concentrationsof five elements: two micronutrients (Zn and Cu) and threetoxic trace metals (Pb, Cd and Hg) in three types of biological materials derived from the bones of the red fox V.vulpes, and to determine intraspecific differences betweenthe concentrations of trace elements in cartilage, spongybone and compact bone.Materials and methodsStudy areaThe material was collected in north-western Poland, in theWest Pomeranian province including its capital, Szczecin.Most of the province's area is agricultural (38%) and forested (35%), and several percent of the area is covered by water(numerous lakes, rivers, the Odra estuary with Dabie Lake,
Acta Theriol (2012) 57:233–244and Szczecin Lagoon) (http://www.stat.gov.pl/cps/rde/xbcr/szczec/ASSETS przegl 2.pdf).MaterialThe material was collected in 2008–2009. Altogether itconsisted of 30 foxes from six districts of the West Pomeranian province (municipalities of Szczecin, Choszczno,Stargard, Gryfice, Kamien Pomorski and Mysliborz —three, eight, seven, one, two, and two specimens, respectively, and seven remaining foxes from the Provincial Veterinary Inspectorate in Szczecin). In Poland, the fox isincluded in the list of animals for hunting (Journal of Law2005, no 45, pos. 433), and according to the Minister ofEnvironment, it may be hunted from 1st July to 31st March(Journal of Law 2005, no 48, pos. 459).The acquisition of biological material from the foxes wasapproved by the Local Ethics Committee for Research onAnimals in Szczecin (Poland).235spongy bone with directly adjacent compact bone. Bonetissue was dried to constant weight at 55 C and 105 C indrying oven with natural convection, ED 53 (Binder GmbH,Germany). This procedure was used to determine the watercontent (gravimetric method). Dried samples were ground inan agate mortar (Sigma-Aldrich, Poland).Determination of zinc, copper, cadmium and leadThe samples were divided into doses, weighing from0.5 to 1.0 g. Bone tissue was mineralized by wetdigestion using a Velp Scientifica mineralizer (Italy)(Kalisinska et al. 2007).Concentrations of Zn, Cu, Pb and Cd were determined byatomic absorption spectrophotometry (ICP-AES) in inductively coupled argon plasma, using a Perkin-Elmer Optima2000 DV. The device’s limits of detection for Zn, Cu, Pb, Cdwere 0.2, 0.4, 1 and 0.1 μg/L, respectively.Determination of mercuryFox age determinationFox age categories were based on the examination of onesingle-root lower canine, with preserved anatomical crown,from 30 foxes. The teeth were placed immediately afterextraction in distilled water, and then dried. In order toobtain pantomographic images, all the teeth were glued oncardboard sheets. Radiographs were performed on a CranexCeph's Soredex digital pantomogram from a distance of120 cm (60 kV, 10 mA s). Measurements of linear parameters were performed using digital radiography DIGORA2.1 software (Soredex-Orion, Helsinki, Finland).They included the total width of the tooth (TW) andwidth of the pulp chamber (WC). According to the workof Knowlton and Whittemore (2001), the width of the canine pulp chamber was measured at a standard distance of15 mm from the root apex. Canine width index (CWI) wascalculated as the ratio of the width of the pulp chamber tothe overall width of the lower canine, which allowed thedivision of subjects into two age categories (adultus [ad];immaturus [im]). It was assumed that immature foxes werein the range of CWI from 0.20 to 0.50, and adults from 0.05to 0.20 (Cavallini and Santini 1995). Among the specimenscollected for analysis, some teeth had a very large pulpchamber and others very narrow. Following CWI values itwas determined that the examined group included 18 im and12 ad foxes, respectively (Table 1).Preparation of material for analysis of bone tissuesThe head, neck and part of the femoral shaft were collectedfrom the foxes using a glass tool. Chemical analysis wasperformed on three materials: cartilage, compact bone andTotal mercury (THg) concentrations were determined insamples dried at 55 C, using atomic absorption spectroscopy. The assays were run in an AMA 254 mercury analyzer(Altach Ltd, Czech Republic). For the analysis, we collectedfrom 100 to 300 mg of the sample and then placed it in anickel nacelle in which it was automatically weighed anddried. The sample was thermally decomposed in a stream ofoxygen to obtain the gaseous form, and its degradationproducts were transferred to an amalgamator for the selective off take of Hg. After determination of the parameters ofmeasurement, Hg vapor was released from the amalgamatorby brief heating. The amount of released Hg was measuredby atomic absorption (silicon UV diode detector in theAMA 254 analyzer) at a wavelength of 254 nm, in thearrangement of two measuring cells. The limit of detectionfor this method is 0.01 ng/100 mg of Hg in the sample. Foreach sample, two or three repetitions were performed, andthe statistical analysis used the average of the data,expressed in mg/kg dry mass (dw).Validation of analytical proceedingsThe reliability of the analytical procedure was controlled bythe determination of elements in two reference materialswith known concentrations: NIST SRM 1486 Bone Meal,and IAEA-407 Trace Elements and Methylmercury in Fish(National Institute of Standards and Technology [NIST] andthe International Atomic Energy Agency [IAEA]). Concentrations of metals in the reference materials provided by themanufacturers and our own determinations are shown inTable 2.
236Table 1 Sizes of mandibularcanine teeth from immature (im)and adult (ad) foxesActa Theriol (2012) 57:233–244Age category and number of specimens (n)ParameterWCTWCWIim (n018)AM SD1.49 0.584.95 0.910.29 0.60ad (n012)WC width of the pulp chamber,TW total width, CWI caninewidth index, AM arithmeticmean, Med median, SD standarddeviation, CV coefficient of variation in %Total (n030)Statistical analysisThe analysis used Statistica 9.0. StatSoft software. In orderto determine compliance with the expected normal distribution of results, we used a Kolmogorov–Smirnov test withLillefors correction (p 0.05). In order to compare the impact of various environmental factors on the concentrationof metals in the bone material marrow test, we used aKruskall–Wallis test, and in the case of significant differences,a Mann–Whitney U-test (p 0.05).In addition, we determined the Spearman rank correlationcoefficients between trace elements in different parts of thehip joint (cartilage, compact bone, spongy bone, cartilagewith compact bone).ResultsBasic data on the concentrations of metals in the fox bonematerial is presented in Table 3. Because two samples (compact bone and spongy bone) derived from two individualsexceeded Cu concentration found in the other samples manytimes, we also conducted statistical analysis of Cu withouttaking these samples into account. The concentration of Cuin these samples was 20.35 mg/kg dw in spongy bone and37.5 mg/kg dw in compact bone. In other samples, theTable 2 Concentrations of selected elements in the certifiedreference materials in mg/kg dryweightRV reference value, OD owndeterminationaEstimated valueMetalZnCu147.0 16.00.80aPbCdHg1.335 0.0140.003a–39.318.535.40.65 0.330.505.64 0.705.630.11 0.050.09Range51.112.447.9CVAM SD0.20–1.271.15 0.654.50–7.275.23 0.890.03–0.190.22 17.00.03–0.6057.4concentration of this metal did not exceed 2.5 mg/kg dw. Bothspecimens came from urban areas and had fed mostly fromtrash cans, which may be the reason for such high Cu levels.The distribution of empirical data on the concentrations ofPb, Cd and Hg in the cartilage, compact bone and spongybone, and Zn in the fox compact bone, diverged from theexpected normal distribution, and was examined using a Kolmogorov–Smirnov test (p 0.05) with Lillefors correction(p 0.05). For the concentration of Cu, the distribution of allresults was not consistent with the expected normal distribution, but after removal of the two aforementioned exceptionalsamples, the distribution of the remaining results was consistent with the expected normal distribution (Table 3).Among the micronutrients, Zn had the highest concentration in samples obtained from the examined fox bones, withthe median values ranging from about 100 to 140 mg/kg dw,depending on the type of material. However, the differencesbetween Zn concentrations were not significant (Table 3).The average concentration of Cu in different types ofsamples ranged from about 0.40 to 0.90 mg/kg dw, andthe Kolmogorov–Smirnov test revealed the existence of astatistically significant difference (p 0.05). The highestconcentration of Cu was observed in cartilage (0.88 mg/kg),and it was clearly higher compared to compact bone, cartilage,compact bone and spongy bone by 28%, 10% and 115%,respectively.Bone Meal SRM NIST 1486RVCVAM SDMedOD/RV (%)OD (n07)132.4 4.10.74 0.011.190 0.3060.0020 0.0002–90.092.589.166.7–Fish Tissue IAEA-407OD/RV (%)RVOD (n08)67.165.8 3.898.13.12 0.280.11 0.030.176 0.0100.237 0.00295.191.793.1106.83.280.120.1890.222
Acta Theriol (2012) 57:233–244237Table 3 Concentrations of trace elements (in mg/kg dry weight) in four types of bone material coming from fox in the vicinity of SzczecinMetalParameterCartilageCompact boneCartilage with adjacentcompact boneSpongy boneSignificanceK–WZnAM SDMed134.3 55.6141.8125.1 56.3105.9129.7 55.0130.4111.04 48.74116.31NSrangeCV19.6–219.841.419.6–296.2AM SDMed1.80 2.700.8846.2–296.245.0n0302.01 6.720.7211.21–219.5143.9n0301.17 3.640.43n0290.50 0.350.41CuaPbCdHg42.9n0290.77 0.460.69n0301.89 5.070.82n0291.29 ��34.490.10–9.660.07–20.360.07–1.18CVAM SDMedrange149.61.738 2.3250.7880.165–11.017336.60.978 1.1530.4470.150–4.35459.7267.41.36 1.860.4690.150–11.017154.4312.31.49 1.830.6100.069–6.14769.6CV133.8117.9136.9123.0AM SDMedrange0.137 0.0550.1630.028–0.1980.108 0.0730.1250.002–0.2260.123 0.0600.1500.002–0.2260.142 0.070.1690.034–0.260CVAM SDMed40.00.0060 0.00520.004467.70.0054 0.00470.003753.60.0057 0.00490.003849.20.0029 22687.20.0011–0.022686.70.0013–0.010577.2p 0.05NSNSp 0.05AM arithmetic mean, SD standard deviation, Med median, CV coefficient of variation (in %); K–W Kruskall–Wallis test, p level of significance, NSdifference non-significantaAnalysis for all specimens (n030), after removing samples with exceptionally high Cu concentrationIn the group of highly toxic metals, Pb had the greatestlevels, with the median value ranging from about 0.45 mg/kg(compact bone) to about 0.80 mg/kg dw (in cartilage), but withno statistically confirmed differences between the types ofsamples analyzed (Table 3). The maximum Pb concentrationin cartilage exceeded 10 mg/kg, and in half of the samples wasgreater than 1 mg/kg dw. In other types of samples maximumPb concentrations were not greater than 4.40 and6.15 mg/kg in the compact bone and spongy bone, respectively(Table 3).Mean Cd concentration in the analyzed materials rangedfrom 0.125 mg/kg (compact bone) to about 0.170 mg/kg(spongy bone), and the differences between them werestatistically significant. The highest Cd concentration wasfound in the spongy bone (0.169 mg/kg dw) and was highercompared to levels in cartilage, compact bone and cartilagewith adjacent compact bone by 4%, 35% and 13%,respectively.The average Hg concentration in the various types ofsamples ranged from about 0.002 (in the spongy bone) tomore than 0.004 mg/kg dw (in cartilage) and the Mann–Whitney U-test revealed statistically significant differences(p 0.05). Significant differences were found between theconcentration of this metal in the cartilage with the adjacentcompact bone and in spongy bone. Such differences alsoexisted between the Hg concentration in the compact boneand spongy bone, with about 50% higher concentration ofthis metal in the compact bone underlying the cartilage(Tables 3 and 4). Maximum Hg concentration in the compact bone reached 0.0226 mg/kg, and in 17% of the samplesit was greater than 0.0100 mg/kg dw.In fox cartilage, compact bone and spongy bone, concentrations of the examined metals can be arranged in thefollowing order: Zn Cu Pb Cd Hg.Comparative analysis, which included sex, showed thatbetween males and females, in principle, there were nostatistically proven differences in the concentrations of metals determined in the corresponding bone material. Mercuryin the spongy bone is an exception, as its concentration infemales was 0.0017 mg/kg dw and was over 70% lowercompared to males, where it was on average 0.0029 mg/kgdw (U-test063.0, p 0.05).In addition, a comparison of metal concentrations in thecorresponding bone material was carried out between foxesrepresenting two age categories — immature foxes (im) andthe adults (ad) (Table 5). Only in the case of Hg in cartilagewas there a confirmed statistical difference (U-test063.0,p 0.05); the average Hg concentration in young foxes was
238Acta Theriol (2012) 57:233–244Table 4 Significance of differences between metal concentrations indifferent fox bone materialsMetal Parameter C vs. CB C vs. SB CB vs. SB C CB vs. SBZnUn030 pNSNSNSNSCuUn029 p297.00.04217.00.001293.00.03510.00.001PbUn030 pNSNSNSNSCdUn030 pNSNS300.00,03NSHgUn030 pNS210.00.001243.00.002451.00.002C cartilage, CB compact bone, C CB cartilage with compact bone,SB spongy bone, U Mann–Whitney U-test, p level of significanceabout 100% higher than in adults (0.0054 and 0.0027 mg/kgdw, respectively). In addition, the cartilage Pb concentrationin the ad group was about 118% higher than in the im group(0.516 and 1.124 mg/kg dw), but this difference was notstatistically confirmed (p00.98).Taking into account data from all subjects (n030), weexamined the relationship between concentrations of metalspresent in the same kind of bone material, and between thevarious groups. Table 6 presents the Spearman rank correlation coefficients (rs) and significance, and the relationshipsconcerning metals present in the same types of fox bone.The strongest synergistic relationships (rs 0.70) were observed in spongy bone between the Zn and Cu and Zn andCd, as well as between Cu and Cd. A similar although aslightly weaker relationship (rs in the range 0.50–0.70) wasfound in other types of bone between the Zn and Cd, and theweakest (rs 0.40) between concentrations of Cu and Hg incartilage and cartilage with adjacent compact bone. Antagonistic statistically significant relationships were detectedbetween Zn and PB, while the absolute value of rs did notexceed 0.50 (Table 6).The results of statistical analysis of the relationship between the concentrations of micronutrients (Zn and Cu) andhighly toxic metals (Pb, Cd, Hg) occurring in various foxbone materials revealed a number of significant correlations(Tables 7 and 8).In the case of micronutrients, these correlations werepurely synergistic, and strongest (rs 0.60) between Zn incartilage and in the compact bone and samples of cartilagewith adjacent compact bone, as well as between Zn incompact bone and cartilage with compact bone. Moreover,Zn concentration in the spongy bone was correlated with Znconcentration (rs 0.70). In the case of Cu, strong correlations (rs 0.60) were observed between its concentration incartilage and cartilage with adjacent compact bone, and Cuconcentration in compact bone and cartilage with adjacentcompact bone (Table 7). We found a few less expressedstatistically significant correlations (rs 0.50) between theconcentration of Cu in the cartilage and compact bone, andspongy bone and cartilage with adjacent compact bone.In the group of toxic metals, we found both positive andnegative relationships between the metals present in varioustypes of bone samples (Table 8). Lead, with the greatestaffinity to bone among the studied metals, showed verystrong relationships between levels determined in all typesof samples. The rs values were very large (from about 0.87to 0.97) and highly statistically significant (p 0.0001). Regression equations were calculated for the strongestrelationships.Also in the case of Cd, high values of the Spearmancorrelation coefficient were recorded, especially betweenthe concentration of this metal in the cartilage with adjacentcompact bone and its concentrations in cartilage, compactbone and spongy bone (rs showed a rising trend, from 0.73to 0.83). For the relationship between Cd concentration inthe cartilage with adjacent compact bone and concentrationof this metal in the spongy bone a regression equation wascalculated. Also, the concentration of Hg in cartilage withcompact bone strongly correlated with the cartilage, compact bone and spongy bone, albeit with a downward rs trendin this sequence (from about 0.86 to 0.70). Between different metals (Table 8) we reported only two statistically significant associations (p 0.05): antagonist between theconcentration of Pb in spongy bone and Cd in compact bone(rs 0 0.401), and synergistic between Pb in compact boneand Hg in spongy bone (rs 00.388).DiscussionStudies on heavy metals in the environment include, amongother things, measuring concentrations in tissues and organsof animals living in land and water ecosystems. In mammals, including the red and arctic fox, toxic elements aredetermined mostly in the liver and kidneys which performdetoxification functions.Warm blooded vertebrates are the subject of multifacetedstudies, mainly in Central Europe and especially in Poland,the Czech Republic and Slovakia (Jankovska et al. 2010;Kalisińska et al. 2011; Piskorova et al. 2003), and lessfrequently in the United States and Canada (Dehn et al.2006; Hoekstra et al. 2003), i.e., in areas or decades exposedto large amounts of anthropogenic toxic substances.In Table 9, for comparison, we summarized data fromscientific literature concerning the concentrations of twomicronutrients (Zn and Cu) and three toxic metals (Pb, Cdand Hg) determined in different types of bones of long-livedmammals.
Acta Theriol (2012) 57:233–244239Table 5 Comparison of metal concentrations in analagous materials between immature and adult foxesImmature, n018CartilageAM SD136.6 52.81.90 1.341.876 2.7550.147 0.1290.0069 223CV38.770.0n017146.837.476.5AM SD108.8 71.020.85 0.511.016 1.2730.118 0.0770.0061 6CV65.360.6125.365.088.7AM SD118.4 47.4n0170.99 1.041.39 1.8530.149 0.0710.0031 .22647.60.0013–0.009170.5AM SDMedrange130.8 61.70143.619.6–205.40.123 3.4390.820.104–9.451.530 1.5641.1240.165–4.8270.123 0.0540.1440.031–0.1840.0045 pact boneSpongy boneAdult, n012CartilageAM SD108.4 48.8148.8n0110.67 0.370.922 0.3720.093 0.0680.0043 104CV45.055.7108.373.076.2AM SDMed100.0 50.6105.0n0110.45 0.330.351.654 1.8830.9270.132 0.070.1310.0028 91.1CartilageUpNSNSNS0.98NS63.00.05Compact boneUpUpNSNSNSNSNSNSNSNSNSNSCompact boneSpongy boneImmature vs. adultSpongy boneU Mann–Whitney U-test, NS statistically non-significant differenceIn literature, there is little data on the concentrations reflecting chronic, sublethal and lethal intoxication with lead, cadmium and mercury in mammal bones. The lowest leadconcentration in human bones is observed in newborns. Inchildren aged 11 months it is 1.5 mg/kg body weight, but thisconcentration usually increases even dozens of times over thelifespan, and the total concentration of this element in thebody of a 60- to 70-year-old male can exceed 200 mg/kg bodyweight (Ma 1996). The transition from a non-toxic to pathological state changes gradually, hence it is difficult to establisha clear line between non-toxic and toxic concentrations insolid elements (Kabata-Pendias and Pendias 1999). Concentrations of the three toxic elements in skeletal elements reflectchronic exposure, yet there is no proof whether the mobilization of elements accumulated in bones may occur so rapidlythat it may cause the symptoms of contamination.Zinc and copperIn available publications, we found little data on concentrations of Zn and Cu in the cartilage and bone of Canidae.In our earlier work (Lanocha et al. 2010) on dogs from
240Table 6 Spearman rank coefficient of variation of metal concentrations in the examined bonematerials of the fox (n030)Acta Theriol (2012) 57:233–244Metal correlationsCartilageCompact boneCartilage with compact boneSpongy boneZinc with:CuNSNS0.275*0.721***Cd0.536**0.688***0.695 SNSPbCdNSNSNSNSNSNSNS0.713***Copper with:NS statistically non-significantLevel of significance: *p 0.05;**p 0.01; ***p 0.001HgNS0.390*0.275*NSLead with:CdNSNSNSNSHgNSNSNSNSCadmium with:HgNSNSNSNSnorth-western Poland, Zn concentrations in cartilage andspongy bone were similar and amounted to 80 mg/kg,and the concentration of Cu was significantly higher incartilage than in spongy bone (2.3 and 1.8 mg/kg dw,respectively). Budis et al. (2009) examined the limb bonesof foxes from north-western Poland and observed that theconcentration of Cu in the compact bone was three timesgreater than in spongy bone ( 2.8 compared to 0.9 mg/kg),but the difference between
There was a significant difference in Cu concentrations, among all the materials analyzed, with much more Cu found in spongy bone than in compact bone. Significant differ-ences were also noted in the case of Hg concentrations in cartilage with compact bone and the spongy bone, and between concentrations of this metal in compact bone and spongy .
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