Introduction

The interaction of external ionizing radiation with tissues of the human body depends in part on the elemental composition of the tissues. The dose from internal sources of ionizing radiation depends on the radioactivity and metabolism of these sources in tissue, the characteristics of radiation emitted by them, and the elemental composition of the tissue. Bone is the most mineralized tissue in the human body. According to studies conducted with radionuclides (Moskalev 1985), many chemical elements including the alkaline earth elements [barium (Ba), beryllium (Be), calcium (Ca), magnesium (Mg), radium (Ra), strontium (Sr)], rare earth elements [scandium (Sc), yttrium (Y), lanthanum (La) and lanthanides, actinium (Ac) and actinides, including thorium (Th) and uranium (U)], lead (Pb), and some others are bone-seeking elements. Thus, data on the elemental composition of bone are very important for radioecology, radiation protection, medical radiology, radiobiology, and biophysics of the bone tissue.

In 1975, the International Commission on Radiological Protection (ICRP) published comprehensive elemental data in order to define ‘Reference Man’ as a typical individual in its Publication 23 (ICRP-23 1975). Current reference values of the ICRP for element mass fractions in bone and skeleton were issued in 2002 (ICRP-89 2002). Thus, the most comprehensive data are available from people living in both West Europe and North America, the latter regions being the main basis for the calculation of the ICRP reference values (ICRP-89 2002). For skeleton and bone (bone mineral), the report 89 of ICRP presents data on no more than 11 [hydrogen (H), carbon (C), nitrogen (N), oxygen (O), sodium (Na), Mg, phosphorus (P), sulfur (S), chlorine (Cl), Ca, and iron (Fe)] and nine (H, C, N, O, Na, Mg, P, S, and Ca) elemental mass fractions, respectively. As was pointed in (ICRP-89 2002), these values may not be representative for the populations of all countries.

State-of-the-art nuclear analytical methods and inductively coupled plasma (ICP) techniques allow detection of many trace and ultra-trace element mass fractions in bone. A number of investigations based on both nuclear and non-nuclear methods have contributed to the growth of data of elemental mass fractions in human bone as documented in numerous published papers. However, it is difficult to improve and to enrich current knowledge using accumulated data because, as follows from some reviews on the subject (Iyengar et al. 1978; Zwanziger 1989; Iyengar and Tandon 1999), there is a very widespread of results for almost all elements. Several sources of potential difficulties in dealing with bone samples were identified (Grynpas et al. 1987; Zaichick 1997, 2004a). The most important difficulties are associated with the issues of sample treatment. The majority of data published are based upon non-intact bones. In most cases, bone samples were ashed or were first treated with solvents in order to remove collagen, fat, and marrow before they were ashed. There is some evidence that certain elements of the bone mineral matrix are lost by this process and that the relationship between elemental mass fractions is also affected (Grynpas et al. 1987; Zaichick 1997, 2004a).

The first aim of the present study was to use the five most powerful instrumental analytical methods available [neutron activation analysis with high-resolution spectrometry of short-lived radionuclides (NAA-SLR), neutron activation analysis with high-resolution spectrometry of long-lived radionuclides (NAA-LLR), particle-induced gamma-ray emission (PIGE), inductively coupled plasma atomic emission spectrometry (ICP-AES), and inductively coupled plasma mass spectrometry (ICP-MS)] for a systematic investigation of elemental mass fractions in intact rib bone samples of residents from a non-industrial region in the Central European part of Russia. The second aim was to investigate any potential age and gender variations in elemental mass fractions. The third aim was to estimate the median of means and the uncertainty of results published on elemental mass fractions in human bones and rib bone separately, while the fourth aim was to calculate elemental mass fractions in the skeleton of the Russian Reference Man (males/females) and to compare the results with data for the ICRP-89 Reference Man and the Chinese Reference Man (Zhu et al. 2010).

Materials and methods

Samples of the human rib bone were obtained at postmortems from intact cadavers (38 females and 46 males, 15–55 years old, Caucasian, European living habits) within 24 h after death. Each death had resulted from automobile accidents, falls, shootings, stabbing, hanging, acute alcohol poisoning, or hypothermia. All the deceased were citizens of Obninsk, a small city in a non-industrial region 105 km southwest of Moscow. None of those who died a sudden death had suffered previously from any systematic or chronic disorders. All studies were approved by the Forensic Medicine Department of Obninsk City Hospital and the Ethical Committee of the Medical Radiological Research Center.

Sample preparation

The majority of samples were taken from the 3rd, 4th, 5th, or 6th rib on the right side. A tool made of titanium and plastic was used to clean soft tissues and blood from the samples. Then, the samples were weighed and the weights were recorded and used in the data analysis. Then, the samples were freeze-dried until a constant mass was obtained. A titanium scalpel was used to cut thin cross-sections of the rib (subsamples), each weighing about 50–100 mg. Four subsamples were made from each rib bone sample: one subsample for NAA-SLR, the second for NAA-LLR, the third for PIGE, and the last one for ICP-AES and ICP-MS. The subsamples for NAA-SLR were sealed separately in thin polyethylene films prewashed with acetone and rectified alcohol. The sealed samples were placed in labeled polyethylene ampoules. The subsamples for NAA-LLR were wrapped separately in a high-purity aluminum foil washed with rectified alcohol beforehand and placed in a nitric acid-washed quartz ampoule. The subsamples for PIGE were dried for an additional 92 h in an oven at 110 °C. The subsamples for ISP-AES and ISP-MS were decomposed in autoclaves. 1.5 mL of concentrated HNO3 (Nitric acid 65 %, max. 0.0000005 % Hg, GR, ISO, Merck) and 0.3 mL of H2O2 (pure for analysis) were added to rib bone samples, placed in one-chamber autoclaves (Ancon-AT2, Ltd., Russia), and then heated for 3 h at 160–200 °C. After autoclaving, they were cooled to room temperature and solutions from the decomposed samples were diluted with deionized water (up to 20 mL) and transferred to plastic measuring bottles. Simultaneously, the same procedure was performed in autoclaves without bone samples (only HNO3 + H2O2 + deionized water), and the resultant solutions were used as control samples.

Analytical procedures

The bone content of 69 elements was measured with the methods mentioned above (Table 1).

Table 1 Arithmetic means ± standard deviations or possible upper limits of the means of elemental mass fractions (mg/kg on a wet mass basis) in intact human rib bone obtained by means of five analytical methods
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Details of the analytical methods and procedures used here such as nuclear reactions, radionuclides, gamma-energies, wavelength, isotopes, spectrometers, spectrometer parameters, and operating conditions were presented in earlier publications (Zaichick et al. 2000, 2009, 2011a; Sastri et al. 2001; Zaichick and Zaichick 2009, 2010).

Standard and certified reference material analysis

For quality control, ten subsamples of the certified reference material CRM IAEA H-5 Animal Bone from the International Atomic Energy Agency (IAEA), nine subsamples of the standard reference material SRM NIST 1486 Bone Meal from the National Institute Standards and Technologies (NIST, USA), and three subsamples of certified reference materials CRM INCT-TL-1 Tea Leaves and CRM INCT-MPH-2 Mixed Polish Herbs from the Institute of Nuclear Chemistry and Technology (INCT, Warsaw, Poland) were analyzed simultaneously with the investigated rib samples. To check the accuracy of the analytical results for fluorine (F), four subsamples of the reference materials SRM NIST 1486 Bone Meal, SRM NIST-1632a Coa, and USGS ScO-l Cody Shale l from NIST were also analyzed. All samples of standard and certified reference materials were treated in the same way as the rib samples. Detailed results of this quality assurance program were presented in earlier publications (Zaichick et al. 2000, 2009, 2011a; Sastri et al. 2001; Zaichick and Zaichick 2009, 2010).

Computer programs and statistics

Using Microsoft Office Excel, a summary of statistical features (arithmetic mean, standard deviation, standard error of mean, minimum and maximum values, median, percentiles with 0.025 and 0.975 levels) or upper limits of the means and detection limits for elemental mass fraction of 69 elements were determined for intact human rib bone. For elements investigated by two or more methods, the mean of all results was used. Using individual values of water content in the investigated bone samples, all elemental mass fractions were calculated on a wet mass basis. The significance of any apparent difference in the results obtained for the female and male subcohorts as well as that in the results obtained for two age groups was evaluated by Student’s t test.

Results

Table 1 depicts the results obtained for 69 elemental mass fractions (arithmetic mean ± standard deviation, upper limit of the mean, detection limit) in intact human rib bone (both females and males taken together) measured by means of the five analytical methods described above.

Table 2 represents certain statistical features (arithmetic mean, standard deviation, standard error of mean, minimum and maximum values, median, percentiles at 0.025 and 0.975 levels) of 33 elements in rib bone of both males and females, taken together.

Table 2 Some statistical parameters of elemental mass fractions (mg/kg on a wet mass basis) in rib bone of both healthy females and males aged 15–55 years, taken together (n = 84)
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To estimate the effect of age on the results obtained, two age groups were examined separately: one comprised a younger group with ages ranging from 15 to 35 years while the other comprised older people with ages ranging from 36 to 55 years. The results for females and males, taken separately and together, are shown in Table 3.

Table 3 Effect of age on mean values (M ± SEM) of elemental mass fractions in intact human rib bone (mg/kg on a wet mass basis)
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The entire dataset for both females and males taken separately was also used to quantify any gender-related differences (see Table 4). However, significant differences were found to accrue from differences in age only, as judged by p values (see Table 3). This led us to provide the additional information in Table 4.

Table 4 Effect of gender on mean values (M ± SEM) of elemental mass fractions in intact human rib bone (mg/kg on a wet mass basis)
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Range of means (medians) and max/min ratio of elemental mass fractions in human bone (various bones) and human rib bone (given separately) according to data from the literature are shown in Tables 5, 6, respectively. In the literature, sometimes, elemental mass fractions in human rib bone were not expressed on a wet mass basis. In this case, for Table 6, we calculated these values using published data for water and ash contents in the rib bone (Zaichick et al. 2000; Tzaphlidou and Zaichick 2003).

Table 5 Range (minimum–maximum value) of means/medians of elemental mass fractions (mg/kg on a dry mass basis) and max/min ratio of the elemental mass fractions in various human bones according to the data from the literature
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Table 6 Median and minimum and maximum values of means/medians of elemental mass fractions (mg/kg on a wet mass basis) and max/min ratios of the elemental mass fractions in human rib bone according to the data from the literature
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Variations due to analytical uncertainty, analytical uncertainty and individual element variability combined, and due to differences between the results obtained in the present work and those of a previous publication with good quality control (Zhu et al. 2010) are given in Table 7, while in Table 8, median values of means (medians) of 79 elemental mass fractions calculated using published data are compared with results obtained here for the human rib bone.

Table 7 Comparison of the variations in the max/min ratios of the elemental mass fractions in bone arising from analytical uncertainty alone, from analytical and elemental variability combined, and between those of this work and those of Zhu et al. (2010)
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Table 8 Median of means/medians of 79 element mass fractions (mg/kg on a wet mass basis) in human bone (adult) from the literature in comparison with the present results
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Skeleton burdens of 79 elements were finally estimated for the Russian Reference Man/Woman using the results obtained in the present work and the accepted values of mass fractions for some bulk (C, H, N, O), trace (Ge, I, Si), and ultra-trace (In, Po, Ra) elements (Table 9). The results are compared with the published data (also shown in Table 9).

Table 9 Skeleton (sum of all skeleton tissues) burdens of 79 elements (g) in different Reference individuals
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Discussion

The use of five analytical methods allowed to estimate the mass fractions of 69 elements in human rib bones. Good agreement was found between the results obtained with NAA and ICP for major (Ca, P), minor (K, Mg, Na), and trace elements (Fe, Mn, Sr, Zn) indicating complete digestion of the rib bone samples (for ICP techniques) and correctness of all results obtained by the various methods (Table 1). The fact that the elemental mass fractions (mean ± SD) of the standard and certified reference materials obtained in the present work were in good agreement with the certified values and within the corresponding 95 % confidence intervals (Zaichick 1995; Zaichick et al. 2000, 2009; Sastri et al. 2001; Zaichick and Zaichick 2009, 2010; Zaichick et al. 2011a, b) suggests an acceptable accuracy of the measurements performed on intact rib bone samples.

Elemental mass fractions in rib bone of Russian adult men/women

The mass fractions for 33 chemical elements listed in Table 1 (Ba, Bi, Ca, Cd, Ce, Cl, Co, Cu, Dy, Er, F, Fe, Gd, K, La, Li, Mg, Mn, Mo, Na, Nd, P, Pb, Pr, Rb, S, Sm, Sr, Tb, Tl, U, Yb, and Zn) were measured in the total or in a major fraction of the investigated rib bone samples. This allowed calculation of the mean values and selected statistical features for these elements for both males and females, taken separately and together (Table 2).

The mass fractions of Ag, Al, B, Be, Br, Cr, Cs, Eu, Hg, Ho, Lu, Ni, Sb, Se, Te, Th, Ti, Tm, and Y (19 elements) were determined only in a few samples collected. The possible upper limit of the mean (≤M) for these elements (Table 1) was calculated as the average mass fraction for each element, using the value of the detection limit instead of the individual value when these latter were found below the detection limit:

$$ \le M = {{\left( {\sum\limits_{i}^{{n_{i} }} {C_{i} + DL \cdot n_{j} } } \right)} \mathord{\left/ {\vphantom {{\left( {\sum\limits_{i}^{{n_{i} }} {C_{i} + DL \cdot n_{j} } } \right)} n}} \right. \kern-0pt} n} $$

where C i is the individual value of chemical element mass fraction in the ith sample, n i is the number of samples with a measured mass fraction above the detection limit (DL), n j is the number of samples with a measured mass fraction below the DL, and n = n i  + n j is the number of investigated samples.

Generally, the mass fractions of 17 elements were lower than the corresponding detection limits (DL, mg/kg on wet mass basis): As(<0.006), Au(<0.0004), Ga(<0.1), Hf(<0.01), Ir(<0.00002), Nb(<0.006), Pa(<0.04), Pd(<0.006), Pt(<0.001), Re(<0.0003), Rh(<0.006), Sc(<0.0006), Sn(<0.1), Ta(<0.003), V(<0.02), W(<0.06), and Zr(<0.02) (Table 1).

Age-related changes in elemental mass fractions of rib bone

An age-related decrease in Ca, Mg, and P mass fractions was observed in separate cohorts of females and males (see Table 3). Note that the most pronounced and statistically significant age-related differences in Ca and Mg mass fractions were detected when the age groups of females and males were analyzed together. Information from other sources on the impact of age on Ca, Mg, and P mass fractions is contradictory. Tipton et al. (1968) reported that Americans of Caucasian origin lose some 20 % of Ca by the age of 55 years. The rib content of Mg also drops with age in American adults. For Germans, the Ca loss was reported to be much lower in comparison with Americans (Schneider and Anke 1971; Anke et al. 1978). However, for Japanese (Yoshinaga et al. 1989; Yoshinaga et al. 1995), no change in Ca and P content was observed for subjects up to the age of 90 years.

The mass fractions of Fe in the male rib bone increase significantly with age (Table 3). A positive Fe-age correlation in the rib bone was also observed by Yoshinaga et al. (1995). In contrast, age variations for the studied trace elements Cu, Sr, and Zn were found to be not significant. This is in agreement with the data by Sowden and Stitch (1957), Nusbaum et al. (1965), Anke et al. (1978), Tanaka et al. (1981), Patti et al. (1984), and Schuhmacher et al. (1992). Nevertheless, a positive Zn-age correlation in the rib bone was observed by Yoshinaga et al. (1995), and a negative Sr-age correlation was reported by Schneider and Anke (1971).

Comparison of mass fractions of rare earth elements (REEs) in the ribs of the two age groups revealed a statistically significant increase with age of Ce, Dy, Er, Gd, La, Nd, Pr, Sm, Tb, and Yb (Table 3). Thus, the present results indicate an age-dependent accumulation for those REEs, for which the determination of average mass fractions and other statistical features was possible. The observed age-dependent increase of the REE mass fractions is better fitted by an exponential relation than by a linear, polynomial, logarithmic, or power relation (Zaichick et al. 2011b). However, the regression parameters (R 2) obtained for most of the REEs are very low, and differences between the different relations are not significant. If this exponential increase of the mass fractions of REEs in the ribs of healthy people living in a non-industrial, ecologically safe region will be confirmed by additional studies, this could be interpreted as the result of a global increase of the concentrations of La and lanthanides in the environment.

Gender-related differences in elemental mass fractions of rib bone

It was pointed out by Schneider and Anke (1971), Schroeder et al. (1972), Anke et al. (1978), and Yoshinaga et al. (1989, 1995) that in women, the rib bone mass fractions of Ca, P, and Sr are higher than those for men. Our results also indicate this (Table 4). In fact, gender-related differences were detected for Ba, Ca, Fe, Mo, Na, P, Sr, and Zn mass fractions for all the age groups studied. Note, however, that statistically significant differences became apparent only for the entire age interval (15–55 years), for both females and males. Higher mass fractions of Ba, Mo, Na, and a lower mass fraction of Fe in the female rib as compared to the male rib have not been reported previously. Elevated levels of Ca, P, and lower level of Fe in the bone tissue of women compared with men can be attributed to physiological characteristics of the female body related to menstruation and reproduction. A high mass fraction of Ba, Na, and Sr in the bones of women is likely due to differences in diet preferences. Usually, Central European region of Russia females consume more vegetable foods than males, which is the main supplier of Ba and Sr in the human body, and more marinated and salted appetizers, which contain salt (NaCl). Note that salt is one of the main sources of Na in nutrition. Elevated levels of Mo may be attributed to a much more frequent use of costume jewelry by women, because stainless steel contains Mo both as an alloying ingredient and a cheap substitute for platinum. The lower Zn mass fraction in bones of male compared with female can be explained by the specific metabolism of this element associated with the physiology of the male reproductive system. A lower content of Zn in male ribs, as compared to female ribs, has not been reported previously.

No statistically significant gender-related differences were detected for all the REEs studied. But, according to the results shown in Table 4, it appears that REEs’ mass fractions (for Ce, Dy, Er, Gd, La, Nd, Pr, Tb, and Yb) for males are either equivalent to or higher than those of females, but never lower. Of course, the involved uncertainties are large, and differences between mass fractions for males and females may not be significant for each REE. However, when considering all the REEs, the present results suggest that REEs’ mass fractions may be higher in males’ rib bones than in females’ rib bones. This observation needs, however, to be confirmed by further measurements. No published data referring to any gender dependence of REEs’ mass fractions in human bone have been found.

Analytical uncertainty and individual variability of elemental mass fractions in bones

Levels of variation (maximum/minimum ratio of means/medians) reported in the literature arising from both analytical uncertainty and individual variability of elemental mass fractions in human bones are surprisingly wide (Table 5). To eliminate the effect of bone differences on the levels of these reported variations, a review of the published data on elemental mass fractions in human rib bones, published in the period from 1940 to 2010, was prepared (Table 6). The means and the corresponding upper limits obtained in the present work for Ag, Al, B, Ba, Be, Bi, Br, Ca, Ce, Cl, Co, Cr, Cs, Cu, Er, F, Fe, Hg, Ho, K, Mg, Mn, Mo, Na, Ni, P, Pb, Rb, S, Se, Sr, and Zn, as shown in Table 1 (last column), agree well with ranges of the mean values cited by other researchers for the human rib bone (including samples received from persons, who died from different diseases) (Table 6). The mean values for Cd, Gd, Dy, La, Li, Nd, Pr, Sm, Tb, Tl, U, and Yb (Table 1, last column) are somewhat lower than the minimum mean value of previously reported data (Table 6). The upper limit of means for Eu, Lu, Sb, Th, Ti, Tm, and Y (Table 1, last column) is nearly equal to two orders of magnitude and for Te (Table 1) is two orders of magnitude lower, than previously reported results (Table 6). The detection limits of ICP-MS show that the content of Re in intact rib bone of healthy men (Table 1, last column) is at least one order of magnitude lower than previously reported data (Table 6). No published data referring to Ir, Pa, Pd, and Rh mass fractions of human rib bone were found. Levels of variation (max/min ratio of means/medians) arising from both analytical uncertainty and individual variability of elemental mass fractions in human rib bone separately, according to the data published in the literature (Table 6), show some values lower than those for various human bones (Table 5); however, the differences are minor.

Thus, it seems reasonable to assume that the enormous level of variation observed arises mainly from the analytical uncertainty. This assumption may well be illustrated by the following historical example: In the late 1970s/early 1980s, the International Atomic Energy Agency (IAEA) was concerned about the poor reproducibility of chemical element analysis in biological samples. Therefore, it was decided to introduce several approaches of improving measurement quality, including the development of standard reference materials from natural biological substances. For this purpose, a large amount of certain biological materials (including animal bones) was dried, homogenized, and packaged in hermetically sealed containers. Samples of each biological material were sent to key analytical laboratories around the world for a quantitative analysis of chemical element mass fractions. The idea was that the average values of element mass fractions measured with acceptable reproducibility would provide appropriate reference values and could then be used as international standards for designated elements. The results were amazing. Analyses of the same element from the same biological sample received from various laboratories differed by many orders of magnitude (Zaichick 2006b). The ranges of variation (max/min ratios) of the element mass fractions obtained for the animal bone sample are presented in Table 7. The assumption expressed above is confirmed if one compares the IAEA results and the variations of data for the element mass fractions in human rib bones taken from the literature (Tables 5,6).

At the end of the twentieth century, a special system of measures of analytical quality control was developed to guarantee good reproducibility of results. This complex system includes regular intra-laboratory quality monitoring and inter-laboratory or external control, as well as the obligatory use of national or international standard materials for comparison. Comparison of the results obtained in the present work with those of Zhu et al. (2010), the most representative study on the subject with modern analytical quality control, shows that the level of variation (max/min ratios) arising from individual variability of element mass fraction in intact human rib bone is now much lower (Table 7): Although the comparison includes different populations (of various races and on different continents), the variations observed for means for all main bone elements (Ca, P, Mg, Na) are in a range of a few percent, and those for almost all of the trace elements do not exceed one order of magnitude.

Comparison with published data and accepted values of mass fractions

Data presented in Table 8 summarize current knowledge of elemental mass fractions in human bone including 79 elements, that is, the major portion of the 91 naturally occurring (not artificially synthesized) elements in the periodic table with only 12 elements, that is, noble gases and ultra-trace rare elements (Ru, Os, Pm, At, Fr, and Ac) being excluded. Table 8 demonstrates that the ICRP-89 Reference Man includes only nine reference values for bulk (C, H, N, O, S), major (Ca and P), and minor (Mg and Na) elements for human bone (ICRP-89 2002). In contrast, the studies by Iyengar et al. (1978) and by Iyengar and Tandon (1999) provide mass fractions for 48 and 69 elements, respectively. For rib bone of the Chinese Reference Man, mass fractions for 60 elements were recently determined by Zhu et al. (2010). In the present work, data published over a period of 70 years (1940–2010) were reviewed and mass fractions of 72 elements in rib bone were found (see Table 8). As follows from the data collected in Table 8, the values of many trace and ultra-trace element mass fractions obtained in the twentieth century differ greatly from those obtained in the last decade, which reflects the impact of improved analytical techniques and quality control. Therefore, the more recent findings may provide a more systematic and representative dataset than those published earlier, for either establishment of parameters relevant for an improved ICRP Reference Man or for further revision of the ICRP Reference Man.

The mass fraction of bulk elements C, H, N, and O in human rib bone published by Woodard and White (1982) was accepted for the bone tissue of the Russian Reference Man (Table 8, last column). According to our review, the median of means/medians of the Ge, I, and In mass fractions and the median values of Po and Ra mass fractions Iyengar and Tandon (1999) were also accepted for the Russian Reference Man. The value of the Ca mass fraction chosen in the present study (116,000 mg/kg on a wet mass basis) is equal to the median mass fraction obtained from 34 references. The data obtained in the present study for Mg and P were nearly equal to the medians calculated based on 18 and 22 references, respectively, and values of 1,450 and 57,800 mg/kg (on a wet mass basis) were accepted for the Russian Reference Man. For Na, the result of our review (about 3,300 mg/kg) and of our measurements (about 3,220 mg/kg) was quite similar and the mean value (3,260 mg/kg) was accepted for the Russian Reference Man. For all other elements, mass fractions obtained in the present study were accepted for the bone tissue of the Russian Reference Man (Table 8, last column).

It is shown in Table 8 that among 79 elements in the bone tissue, the Po mass fraction (8 × 10−12 mg/kg on a wet mass basis) is the lowest while that for O is the highest (442,000 mg/kg on a wet mass basis); thus, the range of elemental mass fractions in human rib bone covers 17 orders of magnitude from 10−1 to 10−18 kg/kg. The sum of accepted values of 79 element mass fractions in the bone tissue of the Russian Reference Man (0.9999995 kg/kg on a wet mass basis) is very close to 1 as it should be.

The mass fractions of N, Na, and O in the bone of the Russian Reference Man are close to, those of Ca, Mg, P, and S are 1.5–3.0 times lower, and those of C and H are 1.5–2.0 times higher than the corresponding mass fractions used for ICRP-89 Reference Man (2002).

Note that the mass fractions obtained in the present work differ somewhat from those used in the Russian State Standard (GOST18622-79 1981) for bone-tissue equivalent materials, for H, C, N, O, P, and Ca (in g/kg: H–40, C–156, N–44, O–443, P–105, and Ca–211).

Skeleton burdens of elements in the Russian Reference Man/Woman

The bone samples selected for the present study were taken from ribs, which are easy to sample at autopsy. In our previous studies, it was found, however, that there are some differences in elemental mass fractions of various bones (Zaichick 2004b, 2006a, 2007; Zaichick et al. 2000, 2009). A typical adult human skeleton consists of 206 bones. Thus, for the precise measuring of elemental mass fractions in the whole skeleton, it would be necessary to investigate 206 bones, which is practically not possible. However, for an approximate estimation of elemental ratios, there is an alternative option: The biggest differences in elemental composition are between compact (cortical) and trabecular (cancellous, spongy) bone (Zaichick 2006a). The densities of compact and trabecular fresh bone are typically of the order of 2.0 (1.8–2.3) g/cm3 and 1.1 (0.8–1.4) g/cm3, respectively. The rib bone samples contain both compact and trabecular bone and, therefore, the densities of the whole fresh adult skeleton (1.30 g/cm3—MCRP-89, 2002) and fresh rib bone (1.41 g/cm3—Woodard and White 1982) are quite similar. Thus, it was assumed here that the ribs’ elemental mass fractions are representative to those of the skeleton in general. For example, this was also assumed in the estimation of elemental burdens in the skeleton of Chinese Reference Man (Zhu et al. 2010).

Using data on the accepted mass fractions (bulk elements C, H, N, and O and trace elements Ge, I, In, Po, and Ra) and on the skeleton’s mass (ICRP-89 2002), total skeleton burdens of 79 elements in the bone tissue of the Russian Reference Man/Woman were calculated. For this purpose, the elemental mass fractions of Ba, Ca, Fe, Mo, Na, P, Sr, and Zn, that is, elements with statistically significant gender-related differences in mass fractions, for rib bone of males and females (see Table 4) were used (Table 9). For comparison, Table 9 also includes information on skeleton burdens of elements in the ICRP-89 Reference Man (2002), Iyengar’s reevaluation (1998), and the Chinese Reference Man (Zhu et al. 2010).

The comparison shows that—for almost all elements—the values obtained in the present study for the Russian Reference Man more or less agree with those for the Chinese Reference Man (Zhu et al. 2010), with the skeleton burdens of As, Bi, and Co being the only exceptions (Table 9): The skeleton burden of As and Co in the Russian Reference Man/Woman is one order of magnitude lower than in the Chinese Reference Man. This may be associated with different level of these elements in the environment. For example, it was shown in studies with biomonitors that atmospheric levels of As and Co are at least one order of magnitude lower in Central Russia than in China (Zhang et al. 2003; Ermakova et al. 2004). In contrast, in the Russian Reference Man/Woman, the skeleton burden of Bi is one order of magnitude higher than in the Chinese Reference Man.

Note that in the skeleton of the Russian Reference Woman/Man, the burden of C, Ca, Fe (for men), H, Mg, Na, O, and P is nearly equal to that of Fe (women) and S is two times lower, and that of N and Cl is 1.5–2.0 times higher than those in the ICRP-89 Reference Man (2002).

The data shown in Tables 8, 9 suggest that elemental mass fractions in bone and those in the skeleton of the ICRP Reference Man need revision.

Conclusions

The combination of various analytical methods allowed measurement of the contents of no less than 69 elements in human rib bone samples of healthy adults. Mean values (M ± SD) for the elemental mass fractions (mg/kg on a wet mass basis) of 33 elements could be measured: Ba (1.62 ± 0.98), Bi (0.0087 ± 0.0070), Ca (116,000 ± 30200), Cd (0.028 ± 0.025), Ce (0.018 ± 0.013), Cl (621 ± 274), Co (0.0016 ± 0.0014), Cu (0.62 ± 0.23), Dy (0.0013 ± 0.0010), Er (0.00068 ± 0.00062), F (978 ± 441), Fe (83 ± 50), Gd (0.00097 ± 0.00071), K (863 ± 244), La (0.012 ± 0.010), Li (0.0236 ± 0.0095), Mg (1,345 ± 333), Mn (0.165 ± 0.081), Mo (0.033 ± 0.026), Na (3,222 ± 738), Nd (0.0067 ± 0.0054), P (50,700 ± 12,600), Pb (1.42 ± 0.80), Pr (0.0021 ± 0.0021), Rb (0.94 ± 0.38), S (1,169 ± 237), Sm (0.00089 ± 0.00077), Sr (177 ± 101), Tb (0.00024 ± 0.00015), Tl (0.00031 ± 0.00015), U (0.00082 ± 0.00059), Yb (0.00046 ± 0.00029), and Zn (57 ± 13). For 19 elements, upper limits of mean elemental mass concentrations were calculated: Ag ≤ 0.0065, Al ≤ 4.7, B ≤ 0.42, Be ≤ 0.0020, Br ≤ 2.5, Cr ≤ 0.14, Cs ≤ 0.0049, Eu ≤ 0.00060, Hg ≤ 0.0096, Ho ≤ 0.00033, Lu ≤ 0.00015, Ni ≤ 0.64, Sb ≤ 0.0056, Se ≤ 0.11, Te ≤ 0.0029, Th ≤ 0.0019, Ti ≤ 1.7, Tm ≤ 0.000040, and Y ≤ 0.0029. Finally, elemental mass concentrations of 17 elements were lower than their detection limits: As < 0.006, Au < 0.0004, Ga < 0.1, Hf < 0.01, Ir < 0.00002, Nb < 0.006, Pa < 0.04, Pd < 0.006, Pt < 0.001, Re < 0.0003, Rh < 0.006, Sc < 0.0006, Sn < 0.1, Ta < 0.003, V < 0.02, W < 0.06, and Zr < 0.02.

It was shown that Ca, Mg, and P mass fractions decrease while mass fractions of rare earth elements in the human rib increase with age. Gender-related differences were detected for Ba, Ca, Fe, Mo, Na, P, Sr, and Zn.

Since all the deceased were citizens of a small city in a non-industrial region, and none of them had suffered previously from any acute or chronic disorders, the data of the present study on 69 elements in intact rib bone may be representative for residents of the Central European region of Russia.

Using published and measured data, the mass fractions for 79 elements for the rib bone have been derived. Based on accepted elemental mass fractions for bone and reference values for the skeleton mass of Reference Man, the elemental burdens in the total skeleton were estimated. These results may provide a representative basis for establishing related reference values of the Russian Reference Man/Woman and revising and extending current reference values of the International Commission on Radiological Protection (ICRP) Reference Man. The data obtained in the present study will also be very valuable for many other applications in radiation protection, radioecology, radiotherapy dosimetry, medical radiology, radiobiochemistry, radiobiophysics, and other scientific fields.