{"id":52071,"date":"2023-09-30T11:14:26","date_gmt":"2023-09-30T11:14:26","guid":{"rendered":"https:\/\/biomedpharmajournal.org\/?p=52071"},"modified":"2023-10-07T09:12:41","modified_gmt":"2023-10-07T09:12:41","slug":"effect-of-boric-acid-on-oxidative-damage-in-immunocompetent-organs-under-conditions-of-potassium-bichromate-and-gamma-radiation-exposure","status":"publish","type":"post","link":"https:\/\/biomedpharmajournal.org\/staging\/vol16no3\/effect-of-boric-acid-on-oxidative-damage-in-immunocompetent-organs-under-conditions-of-potassium-bichromate-and-gamma-radiation-exposure\/","title":{"rendered":"Effect of Boric Acid on Oxidative Damage in Immunocompetent Organs Under Conditions of Potassium Bichromate and Gamma Radiation Exposure"},"content":{"rendered":"\n

Introduction<\/strong><\/p>\n\n\n\n

Lymphoid cells are very susceptible to radiosensitization1-3<\/sup>. The immunodeficiency syndrome appears as damage to lymphopoiesis 4-7<\/sup> and impaired migration of lymphocytes, loss of their ability to recirculate to a node or other lymphoid unit 8,9<\/sup>. This is demonstrated by inhibition of cellular factors, depression of the humoral bundle and functional deficiency of the phagocytic component of immunity 10<\/sup>, caused by a complicated set of structural and metabolic disorders. Consequently, prevention, correction and treatment of disorders developing in the body, including in the immune system, remain important.<\/p>\n\n\n\n

Hexavalent chromium (CrVI) has a number of negative effects on human health: hepato-, nephro-, immunotoxicity, carcinogenicity, gonado- and embryotoxicity 11-13<\/sup>.<\/p>\n\n\n\n

Chromium can enter the human body through the skin, mucous membranes, lungs, as well as together with food and water (gastrointestinal tract), but some of its compounds are assimilated easier and faster (this is due to their solubility and valence of the metal in them). Thus, Cr (VI) is assimilated by the body better and faster than Cr (III), which is due to its high solubility at physiological pH values 14<\/sup>.<\/p>\n\n\n\n

In particular, we consider in\ndetail the ways of this trace element’s entry into the blood. The entry of the\nmetal into the blood is associated with transfer proteins located in the\nepithelium of the small intestine and carrying out active (energy-consuming)\ntransport of the element. If chromium particles enter the body through the\nlungs, then when exhaling with a stream of air they get into the oral cavity,\nfrom there into the gastrointestinal tract, and the process occurs as described\nabove.<\/p>\n\n\n\n

Once in the blood, a part of Cr (VI) binds to erythrocytes, as well as leukocytes and platelets and is reduced to Cr (III), which in turn forms a strong complex with hemoglobin (located on the surface of blood cells) and thus moves around the body. The remaining (unbound) portion of hexavalent chromium is excreted from the body through the kidneys 15<\/sup>.<\/p>\n\n\n\n

Cr (III) upon entering the\nblood binds to the protein transferrin (which is found in the free state in the\nblood plasma). If Cr (III) enters the body in large quantities, it can bind to\nthe protein albumin, globulin and amino acids in the blood plasma. Thus, the\ntransportation of this element in the blood is carried out. It is important to\nknow that the protein transferrin transports iron in the blood, and the trace\nelement chromium competes with it for binding sites.<\/p>\n\n\n\n

Moving through the body in a\nbound state, chromium accumulates in organs such as the lungs, liver, pancreas,\nand bone marrow. Chromium has a high affinity for these tissues.<\/p>\n\n\n\n

When CrVI enters a cell, it is reduced to metastable pentavalent chromium (Cr(V)) and then to trivalent chromium (Cr(III)), which is accompanied by the generation of reactive oxygen species (ROS) and causes damage to cellular structures, including immunocompetent organs 16<\/sup>. At the same time, oxidative stress plays the main role in the realization of the damaging effect arising from chromium intoxication. As a result of which, there is a depletion of the immune system with a transition to immunodeficiency 47-21<\/sup>.<\/p>\n\n\n\n

In this regard, the search for protective agents is\nnecessary to counteract oxidative damage and increase the capacity of the\ndefense response by activating the immune system.<\/p>\n\n\n\n

Boron (B) plays an important role in human and animal bodies 22-25<\/sup>. Boron has an effect on mineral metabolism, vitamin D absorption, enzyme and hormone production, and it also affects biochemical parameters and ROS26-29<\/sup>. Boron has hepatoprotective and antigenotoxic effects [30], antioxidative activity, inhibiting ROS31-34<\/sup>.<\/p>\n\n\n\n

B administration increases the amount of antioxidants in the body (glutathione and its derivatives), thereby limiting oxidative damage to the cell 35<\/sup>. Boric acid displayed hepatoprotective, antioxidant, anti-inflammatory and immunomodulatory activities in animals 36,37<\/sup>. Boron supplementation is believed to have immunostimulatory effects, including on T-cell proliferation and increased levels of natural killer cells 38,39<\/sup>. A number of studies have shown that B reduced levels of inflammatory biomarkers and modulated cellular response in inflammatory processes 40-43<\/sup>, as well as playing a key role as a regulator of immune and inflammatory responses and hematopoiesis 44-47<\/sup>. According to a number of scientists 48-52<\/sup>, B compounds are found to have a protective effect by modulating oxidative stress indicators.<\/p>\n\n\n\n

The effect of B on immune system disorders, on the\nstate of lipid peroxidation and antioxidant system in immunocompetent organs\nunder the influence of Cr(VI) and gamma irradiation has not been studied.\nTherefore, it was the subject of the current experimental study.<\/p>\n\n\n\n

Materials and\nMethods<\/strong><\/p>\n\n\n\n

The experiment was conducted on 70 male Wistar rats\nweighing 170-190 g. The rats were kept in the vivarium under standard\nconditions. Lighting was natural, room temperature – in accordance with the\napproved standards. Nutrition – free availability of food and water.<\/p>\n\n\n\n

Animals were kept in standard conditions in the\nvivarium of the Scientific and Practical Center of the Non-Commercial Joint\nStock Company “West Kazakhstan Medical University named after Marat\nOspanov” (Aktobe, Republic of Kazakhstan) under natural illumination and\nmaximum normalized temperature and food regime with free access to food and\nwater. The experiment was conducted in accordance with the European Convention\nfor the Protection of Vertebrate Animals Used for Experimental and Other\nPurposes (Strasbourg, 1986). The experimental program was discussed and\napproved by the university ethics committee of October 20, 2022, protocol No. 8\n(local bioethics committee).<\/p>\n\n\n\n

The animals were randomly divided into 5 groups (14\nrats in each group) 10 days after they had been acclimatized. The first group\nwas the control group. Animals of the 3rd and 5th groups at the beginning of\nthe experiment received potassium bichromate with drinking water daily for 4\nweeks at a dose of 520 mg\/L. Animals of the 4th and 5th groups received boric\nacid in a dose of 400 mg\/l.<\/p>\n\n\n\n

Four weeks after the start of the experiment, all rats\nwere subjected to gamma irradiation at a sublethal dose (6 Gy, N = 0.54 Gy\/min;\nTeragam radiotherapy unit (manufactured by the Czech Republic, in 2008). The\ndistribution distance from the source to the skin was 70 cm.<\/p>\n\n\n\n

Immunological parameters. To study the cells of\nlymphoid organs of the immune system, suspensions were prepared from thymus,\nspleen and lymph nodes of the small intestine. The total number of lymphoid\ncells and organ mass were determined.<\/p>\n\n\n\n

Lipid peroxidation and antioxidant status. The content of malondialdehyde (MDA) in tissues of thymus, spleen and intestinal lymph nodes was determined spectrophotometrically according to the Draper method modified by Hadley 53<\/sup>. Superoxide dismutase (SOD) activity was estimated according to the method of Beauchamp and Fridovich 54<\/sup>. Catalase (CAT) activity was determined according to the method of Korolyuk 55<\/sup>. Glutathione peroxidase (GPO) activity was determined according to the method of Flohe and Gunzlcer 56<\/sup>.<\/p>\n\n\n\n

Statistical analysis. Statistical data processing was\nperformed using Statistica 10 (StatSoft, Inc., USA) program package.<\/p>\n\n\n\n

Results and\nDiscussions<\/strong><\/p>\n\n\n\n

The study of the effect of boric acid on the cellular\ncomposition of lymphoid organs showed the following. At sublethal dose of gamma-irradiation\n(Table 1) there is a decrease of thymus cells by 56%, lymph nodes by 22%, and\nat the same time the number of lymphoid cells in spleen increases by 44%.<\/p>\n\n\n\n

Under the combined effect of CrVI and gamma-radiation\nthere is a decrease in the number of lymphoid cells in all studied\nimmunocompetent organs. In thymus the complex of cell composition decreases by\n70%, in spleen – by 40%, in lymph nodes – by 42% in comparison with control\ndata.<\/p>\n\n\n\n

Under the influence of boric acid in the irradiated\norganism the number of lymphoid cells significantly increases in thymus by 47%,\nin lymph nodes – by 14% (p<0,05) compared to the data of animals exposed\nonly to irradiation. The number of cells in the spleen is at the level of the\ncontrol group data. Prophylactic administration of boric acid under combined\nexposure to CRVI and \u03b3-irradiation causes an increase in the composition of\nthymus cells by 75%, spleen by 87%, lymph nodes by 22% compared to the data of\npositive control animals (CRVI and \u03b3-irradiation).<\/p>\n\n\n\n

The effect of CrVI and \u03b3-irradiation on lipid\nperoxidation and antioxidant status in immunocompetent organs was evaluated, as\nwell as the protective effect of boric acid under these exposure conditions.<\/p>\n\n\n\n

Under the action of a sublethal dose of\ngamma-irradiation there was observed an increase of MDA in lymph nodes by 69%,\nin spleen and thymus tissues by 40 and 57%, respectively, compared to the\ncontrol. SOD activity was decreased in lymph nodes, spleen and thymus tissues\nby 35, 27 and 22%, respectively. The activity of catalase, respectively, by 39,\n47 and 53%, the activity of HPO – by 17, 37 and 20%, respectively (Table 2)\ncompared to the data of animals of the control group.<\/p>\n\n\n\n

Prophylactic administration of boric acid under\nconditions of isolated exposure to gamma-irradiation was accompanied by\nreduction of MDA content in lymph nodes by 26%, in spleen and thymus tissues –\nby 19 and 25%. Accordingly, the activity of SOD, GPO and CAT in lymph nodes\nincreased by 41, 31 and 43% respectively, in spleen tissues – by 19, 64 and\n200% respectively, in thymus tissues – by 21, 51 and 100% compared to the data\nof positive control (gamma-irradiation).<\/p>\n\n\n\n

The combined effect of CrVI and gamma-irradiation\nresulted in the increase of MDA level in lymph nodes, spleen and thymus tissues\nby 169 and 122, 157%, respectively.<\/p>\n\n\n\n

Antioxidant system enzymes – SOD activity in lymph\nnodes, in spleen and thymus tissues – by 46, 36 and 40% respectively, HPO\nactivity – by 27, 45 and 32% respectively, CAT – by 55, 64 and 62% compared to\ncontrol.<\/p>\n\n\n\n

Administration of group B compounds under conditions\nof combined exposure to Cr VI and gamma-irradiation led to a decrease in MDA\ncontent in lymph nodes by 37%, in spleen tissues – by 35%, in thymus tissues –\nby 28%. The activity of enzymes increased. SOD activity in spleen, thymus and\nlymph node tissues by 41, 33 and 50%, respectively; catalase activity by 125,\n100 and 50%, respectively; VI and ICR.<\/p>\n\n\n\n

Under the influence of CRVI and gamma irradiation, LPO\nand AOS disorders were more pronounced (p<0.05). SOD activity in spleen\ntissues (p>0.05), HPO activity in lymph nodes (p>0.05), in spleen and\nthymus tissues (p>0.05) were the exceptions (Table 2) compared to the data\nof gamma-irradiated animals.<\/p>\n\n\n\n

In response to extreme radiation exposure, various pathological processes develop, affecting the immune system, which is very sensitive to the action of ionizing radiation 57<\/sup> and heavy metals 58,59<\/sup>. Ionizing radiation and chromium cause destruction of lymphoid tissue60<\/sup>.<\/p>\n\n\n\n

Considering the diverse functions of B compounds as regulators of immune, inflammatory reactions and hematopoiesis 61<\/sup>, we hypothesized that the positive effect of boric acid may be useful for the prevention of immune system disorders. Especially in the case of oxidative damage of immunocompetent organs under the combined effect of CrVI and gamma radiation.<\/p>\n\n\n\n

Another mechanism of action of boric acid may be the\nantioxidant potential of boron compounds. Boron may counteract the inhibitory\neffect of oxidative stress on lymphocyte proliferation. In our previous studies\n[62-64], it was found that boric acid at a low dose (400 mg\/L), sodium\ntetraborate at a dose of 22.5 mg\/kg body weight when co-administered with\npotassium bichromate (700 mg\/L) exhibited antioxidant effects and reduced\ndamage to immunocompetent organs, providing an immunoprotective effect.<\/p>\n\n\n\n

Application of boric acid in a dose of 400 mg\/l daily for 28 days reduces the amount of MDA in lymph nodes, thymus and spleen tissues by 26, 25 and 19%, respectively, as well as by 37, 28 and 35% compared to the data of animals of the corresponding groups of positive control. The activity of antioxidant defense enzymes SOD, GPO and CAT in the studied immunocompetent organs, respectively, significantly (p<0.05) increased both at isolated and combined exposure compared to the data of positive control animals (irradiation, CRVI + irradiation). Under the same experimental conditions, boric acid causes an increase in cellularity of lymph nodes, in spleen and thymus tissues. Apparently, B compounds can promote lymphocyte multiplication by increasing the antioxidant potential of cells.<\/p>\n\n\n\n

Table 1: Effects of boric acid on the lymphoid organs (cellularity) under conditions of isolated and combined exposure to potassium bichromate and gamma radiation<\/strong>.<\/p>\n\n\n\n\n\n\n\n\n
\n

Cellularity<\/strong><\/p>\n

(*106<\/sup>\/gr)<\/strong><\/p>\n<\/td>\n

\n

Control<\/strong><\/p>\n<\/td>\n

\n

IRR<\/strong><\/p>\n<\/td>\n

\n

Cr+IRR<\/strong><\/p>\n<\/td>\n

\n

B+IRR<\/strong><\/p>\n<\/td>\n

\n

B+Cr+IRR<\/strong><\/p>\n<\/td>\n<\/tr>\n

\n

Thymus<\/p>\n<\/td>\n

\n

1650\u00b1157<\/p>\n<\/td>\n

\n

720\u00b175*<\/sup><\/p>\n<\/td>\n

\n

503\u00b187*<\/sup><\/p>\n<\/td>\n

\n

1056\u00b1133*<\/sup><\/p>\n<\/td>\n

\n

880\u00b190*<\/sup>0<\/sub><\/p>\n<\/td>\n<\/tr>\n

\n

Spleen<\/p>\n<\/td>\n

\n

363\u00b146<\/p>\n<\/td>\n

\n

521\u00b161*<\/sup><\/p>\n<\/td>\n

\n

213\u00b1330<\/sub><\/p>\n<\/td>\n

\n

330\u00b1480<\/sub><\/p>\n<\/td>\n

\n

403\u00b1540<\/sub><\/p>\n<\/td>\n<\/tr>\n

\n

Lymph nodes<\/p>\n<\/td>\n

\n

937\u00b1120<\/p>\n<\/td>\n

\n

727\u00b193*<\/sup><\/p>\n<\/td>\n

\n

543\u00b175*<\/sup><\/p>\n<\/td>\n

\n

831\u00b193*<\/sup><\/p>\n<\/td>\n

\n

660\u00b1770<\/sub><\/p>\n<\/td>\n<\/tr>\n<\/tbody>\n<\/table>\n

Note:  * – p<0.05; compared with the data of positive control groups among themselves – 0-p<0.05;<\/p>\n

IRR – gamma radiation; Cr+IRR \u2013 potassium bichromate + gamma radiation; B – is boric acid.<\/p>\n\n\n

Table 2: The effect of boric acid on the level of malondialdehyde and the activity of enzymes of the antioxidant system in immunocompetent organs with isolated and combined effects of bichromate and gamma irradiation<\/strong>.<\/p>\n\n\n\n\n\n\n\n\n\n\n\n\n\n\n\n\n\n
\n<\/td>\n\n

Object of study<\/strong><\/p>\n<\/td>\n

\n

Control<\/strong><\/p>\n<\/td>\n

\n

IRR<\/strong><\/p>\n<\/td>\n

\n

Cr+IRR<\/strong><\/p>\n<\/td>\n

\n

B+IRR<\/strong><\/p>\n<\/td>\n

\n

B+(Cr+IRR)<\/strong><\/p>\n<\/td>\n<\/tr>\n

\n

MDA, nmol\/ml<\/p>\n<\/td>\n

\n

Lymph nodes<\/p>\n<\/td>\n

\n

16\u00b11.8<\/p>\n<\/td>\n

\n

27\u00b12.5*<\/sup><\/p>\n<\/td>\n

\n

43\u00b14.3*<\/sup><\/p>\n<\/td>\n

\n

20\u00b11.8*<\/sup><\/p>\n<\/td>\n

\n

27\u00b12.4*<\/sup><\/p>\n<\/td>\n<\/tr>\n

\n

Spleen<\/p>\n<\/td>\n

\n

23\u00b13.0<\/p>\n<\/td>\n

\n

32.2\u00b15.1*<\/sup><\/p>\n<\/td>\n

\n

51.1\u00b18.40<\/sub><\/p>\n<\/td>\n

\n

26\u00b12.70<\/sub><\/p>\n<\/td>\n

\n

33\u00b15.3*<\/sup>0<\/sub><\/p>\n<\/td>\n<\/tr>\n

\n

Thymus<\/p>\n<\/td>\n

\n

21\u00b12.12<\/p>\n<\/td>\n

\n

36\u00b14.8*<\/sup><\/p>\n<\/td>\n

\n

54\u00b19.0*<\/sup><\/p>\n<\/td>\n

\n

27\u00b12.2*<\/sup>0<\/sub><\/p>\n<\/td>\n

\n

39\u00b15.4*<\/sup>0<\/sub><\/p>\n<\/td>\n<\/tr>\n

\n

SOD, unit\/ml<\/p>\n<\/td>\n

\n

Lymph nodes<\/p>\n<\/td>\n

\n

26\u00b13.3<\/p>\n<\/td>\n

\n

17\u00b11.8*<\/sup><\/p>\n<\/td>\n

\n

14\u00b11.3*<\/sup><\/p>\n<\/td>\n

\n

24\u00b12.10<\/sub><\/p>\n<\/td>\n

\n

21\u00b12.7*<\/sup>0<\/sub><\/p>\n<\/td>\n<\/tr>\n

\n

Spleen<\/p>\n<\/td>\n

\n

66\u00b19.0<\/p>\n<\/td>\n

\n

48\u00b15.4*<\/sub><\/p>\n<\/td>\n

\n

44\u00b15.2*<\/sub><\/p>\n<\/td>\n

\n

57\u00b19.0*<\/sup>0<\/sub><\/p>\n<\/td>\n

\n

62\u00b18.10<\/sub><\/p>\n<\/td>\n<\/tr>\n

\n

Thymus<\/p>\n<\/td>\n

\n

45\u00b15.0<\/p>\n<\/td>\n

\n

33\u00b13.0*<\/sub><\/p>\n<\/td>\n

\n

27\u00b12.5*<\/sup><\/p>\n<\/td>\n

\n

40\u00b13.90<\/sub><\/p>\n<\/td>\n

\n

36\u00b14.0*<\/sup><\/p>\n<\/td>\n<\/tr>\n

\n

GPO,  unit\/ml<\/p>\n<\/td>\n

\n

Lymph nodes<\/p>\n<\/td>\n

\n

247\u00b138<\/p>\n<\/td>\n

\n

206\u00b145*<\/sub><\/p>\n<\/td>\n

\n

180\u00b130*<\/sub><\/p>\n<\/td>\n

\n

270\u00b1430<\/sub><\/p>\n<\/td>\n

\n

23\u00b1400<\/sub><\/p>\n<\/td>\n<\/tr>\n

\n

Spleen<\/p>\n<\/td>\n

\n

275\u00b135<\/p>\n<\/td>\n

\n

172\u00b136*<\/sub><\/p>\n<\/td>\n

\n

151\u00b130*<\/sub><\/p>\n<\/td>\n

\n

282\u00b1500<\/sub><\/p>\n<\/td>\n

\n

186\u00b133*<\/sup>0<\/sub><\/p>\n<\/td>\n<\/tr>\n

\n

Thymus<\/p>\n<\/td>\n

\n

133\u00b126<\/p>\n<\/td>\n

\n

106\u00b121*<\/sub><\/p>\n<\/td>\n

\n

90\u00b118*<\/sub><\/p>\n<\/td>\n

\n

166\u00b1360<\/sup><\/p>\n<\/td>\n

\n

128\u00b1330<\/sub><\/p>\n<\/td>\n<\/tr>\n

\n

CAT, mol\/s<\/p>\n<\/td>\n

\n

Lymph nodes<\/p>\n<\/td>\n

\n

49\u00b18.1<\/p>\n<\/td>\n

\n

30\u00b16.6*<\/sub><\/p>\n<\/td>\n

\n

22\u00b14.0*<\/sup><\/p>\n<\/td>\n

\n

43\u00b17.20<\/sub><\/p>\n<\/td>\n

\n

33\u00b16.6*<\/sup>0<\/sub><\/p>\n<\/td>\n<\/tr>\n

\n

Spleen<\/p>\n<\/td>\n

\n

33\u00b13.9<\/p>\n<\/td>\n

\n

16\u00b13.6*<\/sup><\/p>\n<\/td>\n

\n

12\u00b130*<\/sup><\/p>\n<\/td>\n

\n

48\u00b19.9*<\/sup>0<\/sub><\/p>\n<\/td>\n

\n

27\u00b16.60<\/sub><\/p>\n<\/td>\n<\/tr>\n

\n

Thymus<\/p>\n<\/td>\n

\n

52\u00b18.4<\/p>\n<\/td>\n

\n

25\u00b15.2*<\/sup><\/p>\n<\/td>\n

\n

20\u00b13.6*<\/sup><\/p>\n<\/td>\n

\n

50\u00b17.00<\/sub><\/p>\n<\/td>\n

\n

40\u00b15.4*<\/sup>0<\/sub><\/p>\n<\/td>\n<\/tr>\n<\/tbody>\n<\/table>\n

Note: * \u2013 p<0.05; o – p < 0.05 compared with the data of the positive group; IRR – gamma irradiation; Cr+IRR \u2013 potassium bichromate + gamma irradiation<\/p>\n\n\n

Conclusion<\/strong> <\/p>\n\n\n\n

The combined and isolated effect of Cr and\ngamma-irradiation leads to activation of free-radical oxidation with a decrease\nin the activity of the antioxidant system in lymphoid organs. This contributes\nto changes in immunologic and biochemical indices, which leads to depletion of\ncells in the organs of immunogenesis and development of immunologic\nsuppression. Boric acid administration attenuates the development of oxidative\nstress, lipid peroxidation decreases, and the activity of antioxidant defense\nenzymes in immunocompetent cells increases. Boric acid modulates the entire\nimmune response, playing a key role in the regulation of immune and\ninflammatory reactions.<\/p>\n\n\n\n

Acknowledgments<\/strong><\/p>\n\n\n\n

We express our deep gratitude to the staff of the Medical University,\nthe staff of the laboratory and the vivarium.<\/p>\n\n\n\n

Conflict of\ninterest<\/strong><\/p>\n\n\n\n

There is no conflict of interest.<\/p>\n\n\n\n

Funding Source<\/strong> <\/p>\n\n\n\n

The experiment was carried out at the expense of the researchers’ own\nfunds.<\/p>\n\n\n\n

References <\/strong><\/p>\n\n\n\n

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  7. \u0413\u0443\u043b\u0438\u043a \u0415.\u0421., \u041a\u043e\u0441\u0442\u0435\u0448\u0430 \u041d.\u042f., \u0411\u043e\u0440\u0438\u043b\u043e \u0413.\u0410. \u0412\u043b\u0438\u044f\u043d\u0438\u0435 \u0445\u0438\u0442\u0430\u0431\u0438\u0441\u0430 \u0438 \u0435\u0433\u043e \u043a\u043e\u043c\u043f\u043e\u043d\u0435\u043d\u0442\u043e\u0432 \u043d\u0430 \u0441\u0442\u0440\u0443\u043a\u0442\u0443\u0440\u043d\u043e-\u0444\u0443\u043d\u043a\u0446\u0438\u043e\u043d\u0430\u043b\u044c\u043d\u043e\u0435 \u0441\u043e\u0441\u0442\u043e\u044f\u043d\u0438\u0435 \u0442\u043e\u043d\u043a\u043e\u0433\u043e \u043a\u0438\u0448\u0435\u0447\u043d\u0438\u043a\u0430 \u0438 \u043a\u0440\u043e\u0432\u0435\u0442\u0432\u043e\u0440\u0435\u043d\u0438\u044f \u043e\u0431\u043b\u0443\u0447\u0435\u043d\u043d\u044b\u0445 \u043a\u0440\u044b\u0441. \u0412\u0435\u0441\u0442\u043d\u0438\u043a \u0422\u043e\u043c\u0441\u043a\u043e\u0433\u043e \u0433\u043e\u0441\u0443\u0434\u0430\u0440\u0441\u0442\u0432\u0435\u043d\u043d\u043e\u0433\u043e \u0443\u043d\u0438\u0432\u0435\u0440\u0441\u0438\u0442\u0435\u0442\u0430. \u0411\u0438\u043e\u043b\u043e\u0433\u0438\u044f. 2012; 3 (19): 146-159 <\/li>
  8. Willams J.P., McBride W.H. After the bomb drops: A new look at radiation-induced multiple organ dysfunction syndrome. International Journal of Radiation Biology 2011; 87(8):851-868.
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  9. \u0410\u043b\u0435\u043a\u0435\u043d\u043e\u0432\u0430 \u0410.\u0410., \u041a\u0430\u0431\u0434\u043e\u043b\u043b\u0430\u0435\u0432\u0430 \u0421.\u0417., \u0416\u0430\u0440\u043c\u0430\u0445\u0430\u043d\u043e\u0432\u0430 \u0413.\u041c., \u0418\u043b\u044c\u0434\u0435\u0440\u0431\u0430\u0435\u0432\u0430 \u0413.\u041e. \u0418\u0437\u043c\u0435\u043d\u0435\u043d\u0438\u044f \u0432 \u0438\u043c\u043c\u0443\u043d\u043d\u043e\u0439 \u0438 \u0430\u043d\u0442\u0438\u043e\u043a\u0441\u0438\u0434\u0430\u043d\u0442\u043d\u043e\u0439 \u0441\u0438\u0441\u0442\u0435\u043c\u0435 \u043f\u0440\u0438 \u0434\u0435\u0439\u0441\u0442\u0432\u0438\u0438 \u0432\u044b\u0441\u043e\u043a\u043e\u0439 \u0434\u043e\u0437\u044b \u0433\u0430\u043c\u043c\u0430-\u0438\u0437\u043b\u0443\u0447\u0435\u043d\u0438\u044f \u0432 \u043e\u0442\u0434\u0430\u043b\u0435\u043d\u043d\u043e\u043c \u043f\u0435\u0440\u0438\u043e\u0434\u0435. \u0421\u0435\u0440\u0438\u044f \u043a\u043e\u043d\u0444\u0435\u0440\u0435\u043d\u0446\u0438\u0439 \u0417\u041a\u041c\u0423 \u0438\u043c\u0435\u043d\u0438 \u041c\u0430\u0440\u0430\u0442\u0430 \u041e\u0441\u043f\u0430\u043d\u043e\u0432\u0430, 2019; 8: 68-74<\/li>
  10. \u041c\u0430\u0434\u0438\u0435\u0432\u0430 \u041c.\u0420., \u0416\u0435\u0442\u043f\u0438\u0441\u0431\u0430\u0435\u0432 \u0411.\u0410., \u0423\u0437\u0431\u0435\u043a\u043e\u0432\u0430 \u0421.\u0415., \u0416\u0435\u0442\u043f\u0438\u0441\u0431\u0430\u0435\u0432\u0430 \u0425.\u0421., \u0421\u0430\u0439\u0434\u0430\u0445\u043c\u0435\u0442\u043e\u0432\u0430 \u0410.\u0421., \u0422\u043e\u043a\u0435\u0448\u0435\u0432\u0430 \u0413.\u041c., \u0420\u0430\u043a\u044b\u043c\u0436\u0430\u043d\u043e\u0432\u0430 \u0421.\u041e. \u041d\u0435\u0441\u043f\u0435\u0446\u0438\u0444\u0438\u0447\u0435\u0441\u043a\u0430\u044f \u0444\u0430\u0433\u043e\u0446\u0438\u0442\u0430\u0440\u043d\u0430\u044f \u0440\u0435\u0437\u0438\u0441\u0442\u0435\u043d\u0442\u043d\u043e\u0441\u0442\u044c \u0432 \u043e\u0442\u0434\u0430\u043b\u0435\u043d\u043d\u043e\u043c \u043f\u0435\u0440\u0438\u043e\u0434\u0435 \u043f\u043e\u0441\u043b\u0435 \u0432\u043e\u0437\u0434\u0435\u0439\u0441\u0442\u0432\u0438\u044f \u0440\u0430\u0437\u043b\u0438\u0447\u043d\u044b\u0445 \u0434\u043e\u0437 \u0433\u0430\u043c\u043c\u0430 \u0438\u0437\u043b\u0443\u0447\u0435\u043d\u0438\u044f. \u0410\u0441\u0442\u0430\u043d\u0430 \u043c\u0435\u0434\u0438\u0446\u0438\u043d\u0430\u043b\u044b\u043a \u0436\u0443\u0440\u043d\u0430\u043b\u044b, 2010; 2(60): 162-165 <\/li>
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  12. Ozasa K., Shimizu Y., Suyama A., Kasagi F., Soda M., Grant E.Y. et.al. Studies of the mortality of atomic bomb survivors. Reprot 14, 1950-2003. An overview of cancer and noncancer diseases. Radiat.Res.2012; 177: 229-43.
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  13. O’Brien T.J., Ceryak Sand S.R.Patierno. Complexities of chromium carcinogenesis: role of cellular response, repair and recovery mechanism. Mutat. Res. 2003; 533: 3-36.
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  14. \u041c\u0430\u043c\u044b\u0440\u0431\u0430\u0435\u0432 \u0410.\u0410. \u0422\u043e\u043a\u0441\u0438\u043a\u043e\u043b\u043e\u0433\u0438\u044f \u0445\u0440\u043e\u043c\u0430 \u0438 \u0435\u0433\u043e \u0441\u043e\u0435\u0434\u0438\u043d\u0435\u043d\u0438\u0439. \u0410\u043a\u0442\u043e\u0431\u0435, 2012: 284. <\/li>
  15. \u0416\u0435\u0442\u043f\u0438\u0441\u0431\u0430\u0435\u0432 \u0411.\u0410., \u041d\u0443\u0440\u043c\u0430\u0434\u0438\u0435\u0432\u0430 \u0413.\u0422., \u0410\u0440\u0493\u044b\u043d\u0431\u0435\u043a\u043e\u0432\u0430 \u0410.\u0421., \u0418\u0431\u0440\u0430\u0433\u0438\u043c\u043e\u0432\u0430 \u041b.\u0410. \u0424\u0438\u0442\u043e\u043a\u043e\u0440\u0440\u0435\u043a\u0446\u0438\u044f \u043e\u0431\u043c\u0435\u043d\u0430 \u043f\u0443\u0440\u0438\u043d\u043e\u0432\u044b\u0445 \u043d\u0443\u043a\u043b\u0435\u043e\u0442\u0438\u0434\u043e\u0432 \u0432 \u043f\u0435\u0447\u0435\u043d\u0438 \u0438 \u043d\u0430\u0434\u043f\u043e\u0447\u0435\u0447\u043d\u0438\u043a\u0430\u0445 \u043f\u0440\u0438 \u0441\u043e\u0447\u0435\u0442\u0430\u043d\u043d\u043e\u043c \u0434\u0435\u0439\u0441\u0442\u0432\u0438\u0438 \u0441\u0442\u0440\u0435\u0441\u0441\u043e\u0433\u0435\u043d\u043d\u044b\u0445 \u0444\u0430\u043a\u0442\u043e\u0440\u043e\u0432. \u0421\u0435\u0440\u0438\u0438 \u043a\u043e\u043d\u0444\u0435\u0440\u0435\u043d\u0446\u0438\u0439 \u0417\u041a\u041c\u0423 \u0438\u043c\u0435\u043d\u0438 \u041c\u0430\u0440\u0430\u0442\u0430 \u041e\u0441\u043f\u0430\u043d\u043e\u0432\u0430 2019; VIII: 47-52. <\/li>
  16. \u0418\u0437\u0442\u043b\u0435\u0443\u043e\u0432 \u041c.\u041a., \u0413\u043e\u043c\u0435\u043e\u0441\u0442\u0430\u0437 \u0438 \u0445\u0440\u043e\u043c\u043e\u0432\u0430\u044f \u043f\u0430\u0442\u043e\u043b\u043e\u0433\u0438\u044f. \u041c\u043e\u043d\u043e\u0433\u0440\u0430\u0444\u0438\u044f. – \u0410\u043a\u0442\u043e\u0431\u0435, 2003. – 213. <\/li>
  17. \u0421\u0443\u043b\u0435\u0439\u043c\u0435\u043d\u043e\u0432\u0430 \u0420.\u041a., \u0418\u0437\u0442\u043b\u0435\u0443\u043e\u0432 \u041c.\u041a., \u0421\u0443\u043d\u0434\u0435\u0442\u043e\u0432 \u0416.\u0421., \u0418\u0437\u0442\u043b\u0435\u0443\u043e\u0432 \u0415.\u041c. \u041a\u043e\u0440\u0440\u0435\u043a\u0446\u0438\u044f \u043c\u0430\u0441\u043b\u044f\u043d\u044b\u043c \u044d\u043a\u0441\u0442\u0440\u0430\u043a\u0442\u043e\u043c \u0438\u0437 \u043a\u043e\u0440\u043d\u0435\u0439 \u0441\u043e\u043b\u043e\u0434\u043a\u0438 \u043d\u0430\u0440\u0443\u0448\u0435\u043d\u0438\u0439 \u0438\u043c\u043c\u0443\u043d\u043d\u043e\u0433\u043e \u0441\u0442\u0430\u0442\u0443\u0441\u0430, \u0432\u044b\u0437\u044b\u0432\u0430\u0435\u043c\u044b\u0445 \u0441\u043e\u0435\u0434\u0438\u043d\u0435\u043d\u0438\u044f\u043c\u0438 \u0445\u0440\u043e\u043c\u0430. \u041c\u0435\u0436\u0434\u0443\u043d\u0430\u0440\u043e\u0434\u043d\u0430\u044f \u043d\u0430\u0443\u0447\u043d\u043e \u2013 \u043f\u0440\u0430\u043a\u0442\u0438\u0447\u0435\u0441\u043a\u0430\u044f \u043a\u043e\u043d\u0444\u0435\u0440\u0435\u043d\u0446\u0438\u044f \u00ab\u0410\u043a\u0442\u0443\u0430\u043b\u044c\u043d\u044b\u0435 \u0432\u043e\u043f\u0440\u043e\u0441\u044b \u043f\u0430\u0442\u043e\u0444\u0438\u0437\u0438\u043e\u043b\u043e\u0433\u0438\u0438 \u0438 \u043c\u0435\u0434\u0438\u0446\u0438\u043d\u044b\u00bb. \u0410\u043b\u043c\u0430\u0442\u044b, 2008; – 46-50. <\/li>
  18. \u0418\u0437\u0442\u043b\u0435\u0443\u043e\u0432 \u041c.\u041a., \u0418\u0437\u0442\u043b\u0435\u0443\u043e\u0432 \u0415.\u041c. \u0425\u0440\u043e\u043c \u043c\u0435\u043d \u0431\u043e\u0440 \u049b\u043e\u0441\u044b\u043b\u044b\u0441\u0442\u0430\u0440\u044b\u043d\u044c\u04a3 \u0431\u0456\u0440\u043b\u0435\u0441\u043a\u0435\u043d \u04d9\u0441\u0435\u0440\u0456\u043d\u0435\u043d \u0438\u043d\u0434\u0443\u043a\u0446\u0438\u044f\u043b\u0430\u043d\u0493\u0430\u043d \u0440\u0435\u043f\u0440\u043e\u0434\u0443\u043a\u0442\u0438\u0432\u0442\u0456\u043a \u0444\u0443\u043d\u043a\u0446\u0438\u044f \u0431\u04b1\u0437\u044b\u043b\u044b\u0441\u0442\u0430\u0440\u044b\u043d \u0431\u0430\u0493\u0430\u043b\u0430\u0443 \u0436\u04d9\u043d\u0435 \u043a\u043e\u0440\u0440\u0435\u043a\u0446\u0438\u044f\u043b\u0430\u0443. \u04d8\u0434\u0456\u0441\u0442\u0435\u043c\u0435\u043b\u0456\u043a \u043d\u04b1\u0441\u049b\u0430\u0443\u043b\u0430\u0440. \u0410\u049b\u0442\u04e9\u0431\u0435: \u00ab\u041c\u0430\u0440\u0430\u0442 \u041e\u0441\u043f\u0430\u043d\u043e\u0432 \u0430\u0442\u044b\u043d\u0434\u0430\u0493\u044b \u0411\u049a\u041c\u0423\u00bb \u041a\u043e\u0410\u049a, 2022; 345. <\/li>
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