Medires Publishers - Article

Abstract

Thyroid diseases rank second among endocrine disorders, and prevalence of the diseases is higher in the elderly as compared to the younger population. An excess or deficiency of trace element contents in thyroid play important role in goitro- and carcinogenesis of gland.   The correlations with age of the seven-trace element (TE) contents (Br, Cu, Fe, I, Rb, Sr, and Zn), I/Br, I/Cu, I/Fe, I/Rb, I/Sr, and I/Zn ratios, and inter relationships between TE contents and I/TE content ratios in normal thyroid of 73 males (mean age 37.3 years, range 2.0-80) was investigated by radionuclide-induced energy dispersive X-ray fluorescent analysis. Our data reveal that the I content and the I/Fe ratio increase in the normal thyroid of male during a lifespan. Therefore, a goitrogenic and tumorigenic effect of excessive I level in the thyroid of old males and of disturbance in intrathyroidal I/Fe relationships with increasing age may be assumed. Furthermore, it was found that the levels of Br, Cu, Rb, and Zn in the thyroid gland are interconnected and depend on the content of I in it. Because I plays a decisive role in the function of the thyroid gland, the data obtained allow us to conclude that, along with I, such TEs as Br, Cu, Rb, and Zn, if not directly, then indirectly, are involved in the process of thyroid hormone synthesis.

Introduction

According to the World Health Organization (WHO), thyroid diseases rank second among endocrine disorders after diabetes mellitus. More than 665 million people in the world have endemic goiter or suffer from other thyroid pathologies. At the same time, according to the same statistics, the increase in the number of thyroid diseases in the world is 5% per year [1]. It has been suggested that risk factors for the development of thyroid disorders may be numerous factors, including genetics, radiation, autoimmune diseases, as well as adverse environmental factors, such as an increase in the content of various chemicals in the environment [2].

Trace elements (TE) are among these various chemicals, because their levels in the environment have increased significantly over the past hundred years as a result of the industrial revolution and the tremendous technological changes that have taken place in metallurgy, chemical production, electronics, agriculture, food processing and storage, cosmetics, pharmaceuticals and medicine. In connection with these changes, the levels and ratio of TE entering the human body from the outside have been significantly disturbed, compared with the conditions in which human societies have lived for many millennia.

More than 50 years ago, we formulated the postulate about the somatic TE homeostasis, which is now generally recognized [3]. According to this postulate, under evolutionary environmental conditions, the mechanisms of homeostasis of organisms maintain the levels and ratios of TE in tissues and organs within certain limits. If the content of TE in the environment changes significantly, the mechanisms of somatic homeostasis may respond inadequately. Inadequate response of homeostasis mechanisms leads to changes in TE levels in tissues and organs, which, in turn, can affect their function and lead to the development of pathological conditions. The correctness of this conclusion was illustrated by us earlier on the example of the study of the role of TE in the normal and pathophysiology of the prostate [4-24]. It was shown, in particular, that a special role in the development of pathological transformations of the prostate is played by disturbances in the relationship between TE in the tissue and gland secretion. Moreover, it was found that changes in the relationship between TE can be used as highly informative markers of various prostate diseases, including malignant tumors [25-39]. These findings stimulated our investigations of TE relationships in thyroid tissue in normal and pathological conditions.

There are many studies regarding TE content in human thyroid, using chemical techniques and instrumental methods [40-47]. However, among the published data, no works on the relationship of TE in the normal human thyroid were found.

This work had three aims. The primary purpose of this study was to determine reliable values for the bromine (Br), coper (Cu), iron (Fe), iodine (I), rubidium (Rb), strontium (Sr), and zinc (Zn) mass fractions in the normal thyroid of subjects ranging from children to elderly males using radionuclide-induced energy-dispersive X-ray fluorescence analysis and calculate individual values of I/Br, I/Cu, I/Fe, I/Rb, I/Sr, and I/Zn. The second aim was to compare the Br, Cu, Fe, Rb, Sr, and Zn mass fractions in thyroid gland obtained in the study with published data. The final aim was to estimate the inter-correlations of TE contents and I/TE content ratios in normal thyroid of males and changes of these parameters with age.

All studies were approved by the Ethical Committees of the Medical Radiological Research Centre, Obninsk. All the procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments, or with comparable ethical standards.

Materials and Methods

Samples of the human thyroid were obtained from randomly selected autopsy specimens of 73 males (European-Caucasian) aged 2.0 to 80 years. All the deceased were citizens of Obninsk and had undergone routine autopsy at the Forensic Medicine Department of City Hospital, Obninsk. The available clinical data were reviewed for each subject. None of the subjects had a history of an intersex condition, endocrine disorder, or other chronic disease that could affect the normal development of the thyroid. None of the subjects were receiving medications or used any supplements known to affect thyroid TE contents. The typical causes of sudden death of most of these subjects included trauma or suicide and also acute illness (cardiac insufficiency, stroke, embolism of pulmonary artery, alcohol poisoning). All right lobes of thyroid glands were divided into two portions using a titanium scalpel [48]. One tissue portion was reviewed by an anatomical pathologist while the other was used for the TE content determination. A histological examination was used to control the age norm conformity as well as the unavailability of microadenomatosis and latent cancer.

After the samples intended for TE analysis were weighed, they were transferred to -20°C and stored until the day of transportation in the Medical Radiological Research Center, Obninsk, where all samples were freeze-dried and homogenized [49]. To determine the contents of the TE by comparison with a known standard, aliquots of commercial, chemically pure compounds were used [50]. Ten subsamples of the Certified Reference Material (CRM) IAEA H-4 (animal muscle) and IAEA HH-1 (human hair) were analyzed to estimate the precision and accuracy of results. The CRM IAEA H-4 and IAEA HH-1 subsamples were prepared in the same way as the samples of dry homogenized thyroid tissue. 

The TE contents in thyroid samples were determined using radionuclide-induced energy-dispersive X-ray fluorescence analysis (EDXRF) with 109Cd source for Br, Cu, Fe, Rb, Sr, and Zn and 241Am source for I. The mass fraction of TE was calculated by the relative way of comparing between intensities of corresponding Kα-lines induced by radiation from radionuclide sources in tissue samples and standards. Details of the sample preparation, the facility and method of analysis were presented in our previous publication [51-53].

All thyroid samples were prepared in duplicate, and mean values of TE contents were used in final calculation. Using Microsoft Office Excel, a summary of the statistics, including, arithmetic mean, standard deviation, standard error of mean, minimum and maximum values, median, percentiles with 0.025 and 0.975 levels were calculated for TE contents and I/TE content ratios.  Pearson's correlation coefficient was used in Microsoft Office Excel to calculate the relationship "age – TE mass fraction", as well as to identify relationships between different TE contents and between different TE content ratios.

Results

Table 1 depicts comparison of our data for seven TE in ten sub-samples of CRM IAEA H-4 (animal muscle) and IAEA HH-1 (human hair) with the corresponding certified values of TE contents in these materials.

Table 1. EDXRF data of Br, Cu, Fe, I, Rb, Sr, and Zn contents in certified reference material IAEA H-4 (animal muscle) and IAEA HH-1 (human hair) compared to certified values (mg/kg, dry mass basis)

M – arithmetical mean, SD – standard deviation, a – certified values, b – information values.

Table 2 represents certain statistical parameters (arithmetic mean, standard deviation, standard error of mean, minimal and maximal values, median, percentiles with 0.025 and 0.975 levels) of the Br, Cu, Fe, I, Rb, Sr, and Zn mass fractions, as well as I/Br, I/Cu, I/Fe, I/Rb, I/Sr, and I/Zn mass fraction ratios in normal thyroid of males.

Table 2. Some statistical parameters of Br, Cu, Fe, I, Rb, Sr, and Zn mass fraction (mg/kg, dry tissue) as well as I/Br, I/Cu, I/Fe, I/Rb, I/Sr, and I/Zn mass fraction ratios in normal thyroid of male (n=73). 

Mean – arithmetic mean, SD – standard deviation, SEM – standard error of mean, Min – minimum value, Max – maximum value, P 0.025 – percentile with 0.025 level, P 0.975 – percentile with 0.975 level.

The comparison of our results with published data for the Br, Cu, Fe, I, Rb, Sr, and Zn contents in the human thyroid is shown in Table 3.

Table 3. Median, minimum and maximum value of means Br, Cu, Fe, I, Rb, Sr, and Zn contents in normal human thyroid according to data from the literature in comparison with our results (mg/kg, dry tissue)

M –arithmetic mean, SD – standard deviation, (n)* – number of all references, (n)** – number of samples.

To estimate the effect of age on the TE contents and I/TE content ratios Pearson's correlation coefficient was used (Table 4). 

Table 4. Correlations between age (years) and trace element content (mg/kg, dry tissue), as well as between age and I/trace element mass fraction ratios in the normal thyroid of males (r – coefficient of correlation)

Statistically significant values: a p£0.05, b p£0.01.

The data of inter-correlation calculations (values of r – Pearson's coefficient of correlation) including all TE and I/TE ratios identified by us are presented in Tables 5 and 6, respectively.

Discussion

Good agreement of the Br, Cu, Fe, I, Rb, Sr, and Zn contents analyzed by EDXRF with the certified data of CRMs IAEA H-4 and IAEA HH-1 (Table 1) indicates an acceptable accuracy of the results obtained in the study for TE contents and I/TE content ratios in the normal male thyroid presented in Tables 2–6.

The content of TE was determined in all or most of the examined samples, which made it possible to calculate the main statistical parameters: the mean value of the mass fraction (M), standard deviation (SD), standard error of the mean (SEM), minimum (Min), maximum (Max), median (Med), and percentiles with levels of 0.025 (P 0.025) and 0.975 (P 0.975), of the Br, Cu, Fe, I, Rb, Sr, and Zn mass fractions, as well as I/Br, I/Cu, I/Fe, I/Rb, I/Sr, and I/Zn mass fraction ratios in normal thyroid of males (Table 2). The values ​​of M, SD, and SEM can be used to compare data for different groups of samples only under the condition of a normal distribution of the results of determining the content of TE in the samples under study. Statistically reliable identification of the law of distribution of results requires large sample sizes, usually several hundred samples, and therefore is rarely used in biomedical research. In the conducted study, we could not prove or disprove the “normality” of the distribution of the results obtained due to the insufficient number of samples studied. Therefore, in addition to the M, SD, and SEM values, such statistical characteristics as Med, range (Min-Max) and percentiles P 0.025 and P 0.975 were calculated, which are valid for any law of distribution of the results of TE content in thyroid tissue.

The obtained means for Br, Cu, Fe, Rb, Sr, and Zn mass fraction, as shown in Table 3, agree well with the medians of mean values cited by other researches for the human thyroid, including samples received from person

s who died from different non-thyroid diseases [40-47]. A number of values for TE mass fractions were not expressed on a dry mass basis by the authors of the cited references. However, we calculated these values using published data for water (75%) [54] and ash (4.16% on dry mass basis) [55] contents in thyroid of adults. No published data referring to I/Br, I/Cu, I/Fe, I/Rb, I/Sr, and I/Zn mass fraction ratios in human thyroid was found.

With age, the I content and the I/Fe ratio increase (Table 4). These characteristics can be used to estimate the "biological age" of the male thyroid gland.

A significant direct correlation between the Br and Cu, Br and Rb, Br and Sr, Br and Zn, Cu and Fe, Cu and Rb, Rb and Cu mass fractions as well as an inverse correlation between I and Fe mass fractions was seen in male thyroid (Table 5). Since no correlations were found between I and other TE, except for an inverse correlation between I and Fe, it would appear that the content of Br, Cu, Rb, Sr, and Zn in the thyroid gland is independent of I content. However, this is not quite so. If we bring the content of the studied TE to the content of I (I/TE ratio), then there are close relationships between I/Br, I/Cu, I/Fe, I/Rb, and I/Zn. (Table 6). From this it follows that, at least, the levels of Br, Cu, Fe, Rb, and Zn in the thyroid gland are interconnected and depend on the content of I in it.  Because I plays a decisive role in the function of the thyroid gland, the data obtained allow us to conclude that, along with I, such TE as Br, Cu, Fe, Rb, and Zn, if not directly, then indirectly, are involved in the process of thyroid hormone synthesis.

Table 5. Intercorrelations of the trace element mass fractions in the normal thyroid of male (r – coefficient of correlation)

Statistically significant values: a p£0.05, b p£0.01.

Table 6. Intercorrelations of the I/trace element mass fraction ratios in the normal thyroid of male (r – coefficient of correlation)

 Statistically significant values: a p£0.05, b p£0.01, c p£0.001.

Conclusion

The 109Cd and 241Am radionuclide-induced energy-dispersive X-ray fluorescence analysis is a useful analytical tool for the non-destructive determination of TE contents in the thyroid tissue samples. This method allows determine means for Br, Cu, Fe, I, Rb, Sr, and Zn(seven TE). 

Our data reveal that the I content and the I/Fe ratio increase in the normal thyroid of male during a lifespan. Therefore, a goitrogenic and tumorogenic effect of excessive I level in the thyroid of old males and of disturbance in intrathyroidal I/Fe relationships with increasing age may be assumed. Furthermore, it was found that the levels of Br, Cu, Rb, and Zn in the thyroid gland are interconnected and depend on the content of I in it. Because I plays a decisive role in the function of the thyroid gland, the data obtained allow us to conclude that, along with I, such TEs as Br, Cu, Rb, and Zn, if not directly, then indirectly, are involved in the process of thyroid hormone synthesis.

Acknowledgements

We are grateful to Dr. Yu. Choporov, Head of the Forensic Medicine Department of City Hospital, Obninsk, for supplying thyroid samples.

References

1. Wang H, Jiang Y, Song J, Liang H, Liu Y, Huang J, Tin P, Wu D, Zhang H, Liu P, Zhon D, Wei W, Lei L, Peng J, Zhang J. The risk of perchlorate and iodine on the incidence of thyroid tumors and nodular goiter: a case-control study in southeastern China. Environ Health. 2022; 21: 4. 2.
   View at Publisher | View at Google Scholar
2. Tang Z, Zhang J, Zhou Q, Xu S, Cai Z, Jiang G. Thyroid Cancer
   View at Publisher | View at Google Scholar
3. Zaichick V. Medical elementology as a new scientific discipline. J Radioanal Nucl Chem. 2006: 269: 303-309.
   View at Publisher | View at Google Scholar
4. Zaichick V. A systematic review of the mercury content of the normal human prostate gland. Archives of Urology 2020; 3(2): 35-45.
   View at Publisher | View at Google Scholar
5. Zaichick V. A systematic review of the cobalt content of the normal human prostate gland. J Clin Res Oncol. 2020; 3(1): 1-8. 6.
   View at Publisher | View at Google Scholar
6. Zaichick V. A systematic review of the phosphorus content of the normal human prostate gland. Applied Medical Research 2020; 7(2): 1-7.
   View at Publisher | View at Google Scholar
7. Zaichick V. A systematic review of the antimony content of the normal human prostate gland. Journal of Hematology and Oncology Research 2021; 4(1): 17-27.
   View at Publisher | View at Google Scholar
8. Zaichick V. A systematic review of the chromium content of the normal human prostate gland. Innovare Journal of Medical Sciences 2021; 9(1): 1-6.
   View at Publisher | View at Google Scholar
9. Zaichick V. A systematic review of the nickel content of the normal human prostate gland. Health Sciences 2020; 1(ID 234): 1-6.
   View at Publisher | View at Google Scholar
10. Zaichick V. A systematic review of the aluminum content of the normal human prostate gland. Advances in Hematology and Oncology Research 2021; 4(1): 69-75.
    View at Publisher | View at Google Scholar
11. Zaichick V. A systematic review of the lead content of the normal human prostate gland. J Cancer Oncol Res. 2021; 2(1): 1-8.
    View at Publisher | View at Google Scholar
12. Zaichick V. A systematic review of the arsenic content of the normal human prostate gland. International Journal of Medicine Sciences 2021; 3(1): 1-6.
    View at Publisher | View at Google Scholar
13. Zaichick V. A systematic review of the calcium content of the normal human prostate gland. Iberoamerican Journal of Medicine 2021; 3(1): 85-94
    View at Publisher | View at Google Scholar
14. Zaichick V. A systematic review of the tin content of the normal human prostate gland. Journal of Cellular & Molecular Oncology 2021; 3(1): 1-7.
    View at Publisher | View at Google Scholar
15. Zaichick V. Barium levels in the prostate of the normal human: a review. Universal Journal of Pharmaceutical Research 2021; 6(1): 52-60.
    View at Publisher | View at Google Scholar
16. Zaichick V. A systematic review of the zinc content of the hyperplastic human prostate gland. Biomedical Research on Trace Elements 2020; 31 (3): 98-116.
    View at Publisher | View at Google Scholar
17. Zaichick V. Beryllium content of the normal human prostate gland: A systematic review. Acta Scientific Medical Sciences 2021; 5(4): 78-85.
    View at Publisher | View at Google Scholar
18. Zaichick V. Boron level in the prostate of the normal human: A systematic review. J Nano Nano Sci Rese. 2021; 1(2): 1-9.
    View at Publisher | View at Google Scholar
19. Zaichick V. Bismuth level in the prostate of normal human: A systematic review. Int J Biopro Biotechnol Advance 2021; 7(1): 264-273.
    View at Publisher | View at Google Scholar
20. Zaichick V. A systematic review of the cadmium content of the normal human prostate gland. World Journal of Advanced Research and Reviews 2021; 10(01): 258-269.
    View at Publisher | View at Google Scholar
21. Zaichick V. A systematic review of the strontium content of the normal human prostate gland. Journal of Medical Research and Health Sciences (JMRHS) 2021; 4 (5): 1257-1269.
    View at Publisher | View at Google Scholar
22. Zaichick V. Thallium content of the normal human prostate gland - A systematic review. Archives of Clinical Case Reports 2021; 2(5): 223-229.
    View at Publisher | View at Google Scholar
23. Zaichick V. Vanadium content of the normal human prostate gland: A systematic review. Archives of Pharmacy Practice 2021; 12(3): 15-21.
    View at Publisher | View at Google Scholar
24. Zaichick V, A systematic review of the zinc content of the normal human prostate gland. Biol Trace Elem Res. 2021; 199(10): 3593-3607.
    View at Publisher | View at Google Scholar
25. Zaichick V, Zaichick S. Ratios of selected chemical element contents in prostatic tissue as markers of malignancy. Hematol Med Oncol. 2016; 1(2): 1-8.
    View at Publisher | View at Google Scholar
26. Zaichick V, Zaichick S. Ratios of Zn/trace element contents in prostate gland as carcinoma’s markers. Cancer Rep Rev. 2017; 1(1): 1-7.
    View at Publisher | View at Google Scholar
27. Zaichick V, Zaichick S. Ratios of Mg/trace element contents in prostate gland as carcinoma’s markers. SAJ Canc Sci. 2017; 2(1): 102.
    View at Publisher | View at Google Scholar
28. Zaichick V, Zaichick S. Ratios of calcium/trace elements as prostate cancer markers. J Oncol Res Ther. 2017; 2017(4): J116.
    View at Publisher | View at Google Scholar
29. Zaichick V, Zaichick S. Ratios of cobalt/trace element contents in prostate gland as carcinoma’s markers. The International Journal of Cancer Epidemiology and Research 2017; 1(1): 21-27.
    View at Publisher | View at Google Scholar
30. Zaichick V, Zaichick S. Ratios of cadmium/trace element contents in prostate gland as carcinoma’s markers. Canc Therapy & Oncol Int J. 2017; 4(1): 555626.
    View at Publisher | View at Google Scholar
31. Zaichick V, Zaichick S. Ratios of selenium/trace element contents in prostate gland as carcinoma’s markers. J Tumor Med Prev. 2017; 1(2): 555556.
    View at Publisher | View at Google Scholar
32. Zaichick V, Zaichick S. Ratios of rubidium/trace element contents in prostate gland as carcinoma’s markers. Can Res and Clin Oncology 2017; 1(1): 13-21.
    View at Publisher | View at Google Scholar
33. Zaichick V, Zaichick S. Ratio of zinc to bromine, iron, rubidium, and strontium concentration in the prostatic fluid of patients with benign prostatic hyperplasia. Acta Scientific Medical Sciences 2019; 3(6): 49-56.
    View at Publisher | View at Google Scholar
34. Zaichick V, Zaichick S. Ratio of zinc to bromine, iron, rubidium, and strontium concentration in expressed prostatic secretions as a source for biomarkers of prostatic cancer. American Journal of Research 2019; 5-6: 140-150.
    View at Publisher | View at Google Scholar
35. Zaichick V, Zaichick S. Some trace element contents and ratios in prostatic fluids as ancillary diagnostic tools in distinguishing between the benign prostatic hyperplasia and chronic prostatitis. Archives of Urology 2019; 2(1): 12-20.
    View at Publisher | View at Google Scholar
36. Zaichick V, Zaichick S. Some trace element contents and ratios in prostatic fluids as ancillary diagnostic tools in distinguishing between the chronic prostatitis and prostate cancer. Medical Research and Clinical Case Reports 2019; 3(1): 1-10.
    View at Publisher | View at Google Scholar
37. Zaichick V, Zaichick S. Using prostatic fluid levels of zinc to strontium concentration ratio in non-invasive and highly accurate screening for prostate cancer. Acta Scientific Cancer Biology 2020; 4(1): 12-21.
    View at Publisher | View at Google Scholar
38. Zaichick V, Zaichick S. Using prostatic fluid levels of zinc to iron concentration ratio in non-invasive and highly accurate screening for prostate cancer. SSRG International Journal of Medical Science 2019; 6(11): 24-31.
    View at Publisher | View at Google Scholar
39. Zaichick V. Using prostatic fluid levels of rubidium and zinc concentration multiplication in non-invasive and highly accurate screening for prostate cancer. J Cancer Prev Curr Res. 2019; 10(6): 151‒158.
    View at Publisher | View at Google Scholar
40. Zhu H, Wang N, Zhang Y, Wu Q, Chen R, Gao J, Chang P, Liu Q, Fan T, Li J, Wang J, Wang J. Element contents in organs and tissues of Chinese adult men. Health Phys. 2010; 98(1): 61-73.
    View at Publisher | View at Google Scholar
41. Salimi J, Moosavi K, Vatankhah S, Yaghoobi A. Investigation of heavy trace elements in neoplastic and non-neoplastic human thyroid tissue: A study by proton – induced X-ray emissions. Iran J Radiat Res. 2004; 1(4): 211-216.
    View at Publisher | View at Google Scholar
42. Ataulchanov IA. Age-related changes of manganese, cobalt, coper, zinc, and iron contents in the endocrine glands of females. Problemy Endocrinologii 1969; 15(2): 98-102.
    View at Publisher | View at Google Scholar
43. Reddy SB, Charles MJ, Kumar MR, Reddy BS, Anjaneyulu Ch, Raju GJN, Sundareswar B, Vijayan V. Trace elemental analysis of adenoma and carcinoma thyroid by PIXE method. Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms 2002; 196(3-4): 333-339.
    View at Publisher | View at Google Scholar
44. Neimark II, Timoschnikov VM. Development of carcinoma of the thyroid gland in person residing in the focus of goiter endemic. Problemy Endocrinilogii 1978; 24(3): 28-32.
    View at Publisher | View at Google Scholar
45. Zabala J, Carrion N, Murillo M, Quintana M, Chirinos J, Seijas N, Duarte L, Brätter P. Determination of normal human intrathyroidal iodine in Caracas population. J Trace Elem Med Bio. 2009; 23(1): 9-14.
    View at Publisher | View at Google Scholar
46. Boulyga SF, Zhuk IV, Lomonosova EM, Kanash N, Bazhanova NN. Determination of microelements in thyroids of the inhabitants of Belarus by neutron activation analysis using the k0-method. J Radioanal Nucl Chem. 1997; 222(1-2): 11-14.
    View at Publisher | View at Google Scholar
47. Tipton IH, Cook MJ. Trace elements in human tissue. Part II. Adult subjects from the United States. Health Phys. 1963; 9(2): 103-145.
    View at Publisher | View at Google Scholar
48. Zaichick V, Zaichick S. Instrumental effect on the contamination of biomedical samples in the course of sampling. The Journal of Analytical Chemistry 1996; 51(12): 1200-1205.
    View at Publisher | View at Google Scholar
49. Zaichick V, Zaichick S. A search for losses of chemical elements during freeze-drying of biological materials. J Radioanal Nucl Chem. 1997; 218(2): 249-253.
    View at Publisher | View at Google Scholar
50. Zaichick V. Applications of synthetic reference materials in the medical Radiological Research Centre. Fresenius J Anal Chem. 1995; 352: 219-223.
    View at Publisher | View at Google Scholar
51. Zaichick S, Zaichick V. Method and portable facility for energy-dispersive X-ray fluorescent analysis of zinc content in needle-biopsy specimens of prostate. X-Ray Spectrom. 2010; 39: 83-89.
    View at Publisher | View at Google Scholar
52. Zaichick S, Zaichick V. The Br, Fe, Rb, Sr, and Zn content and interrelation in intact and morphologic normal prostate tissue of adult men investigated by energy dispersive X-ray fluorescent analysis. X-Ray Spectrom. 2011; 40(6): 464-469.
    View at Publisher | View at Google Scholar
53. Zaichick V, Zaichick S. Energy-dispersive X-ray fluorescence of iodine in thyroid puncture biopsy specimens. J Trace Microprobe Tech. 1999; 17(2): 219-232.
    View at Publisher | View at Google Scholar
54. Katoh Y, Sato T, Yamamoto Y. Determination of multielement concentrations in normal human organs from the Japanese. Biol Trace Elem Res. 2002; 90(1-3): 57-70.
    View at Publisher | View at Google Scholar
55. Schroeder HA, Tipton IH, Nason AP. Trace metals in man: strontium and barium. J Chron Dis. 1972; 25(9): 491-517
    View at Publisher | View at Google Scholar