Regional features of essential elements in children's hair with cardiomyopathy

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Ахмедова, Д., Ахмедова, Н., Рузматова, Д., Данилова, Е., & Хушниддинова, С. (2023). Regional features of essential elements in children’s hair with cardiomyopathy . in Library, 20(3), 1813–1824. извлечено от https://inlibrary.uz/index.php/archive/article/view/24537
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Аннотация

Abstract. The study aimed to study the content of toxic and essential microelements in the hair of children with cardiomyopathy living in areas with different climatic and geographical conditions. 96 hair samples of children with cardiomyopathy living in different environmental conditions were examined. The research results showed that the problem of microelements is typical not only for the Aral Sea region but also for other regions: deficit and/or deficiency of 2 or more vital microelements is found in 96% of children with CMP. The frequency of trace elements in children in all regions was high in Ca, Cr, Co, Cu, He and Zn.
Children living in the Aral Sea region were characterized by excessive levels of manganese, bromine, and iodine; children living in relatively advantaged regions were characterized by reliably high levels of potassium, chlorine, and iodine.

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REGIONAL FEATURES OF ESSENTIAL

ELEMENTS IN CHILDREN'S HAIR WITH

CARDIOMYOPATHY

Akhmedova D.I.

1

,

2

, Akhmedova N.R.

1,2

, Ruzmatova D.M.

1

, Danilova E.A.

3

, Khusniddinova

S.Kh.

3

1

-Republican Specialized Scientific and Practical Medical Center for Pediatrics of the Ministry

of Health of the Republic of Uzbekistan, Uzbekistan

2

-Tashkent Pediatric Medical Institute, Uzbekistan

3

- Institute of Nuclear Physics of Academy of Sciences of RUz, Uzbekistan

Abstract. The study aimed to study the content of toxic and essential microelements in

the hair of children with cardiomyopathy living in areas with different climatic and
geographical conditions. 96 hair samples of children with cardiomyopathy living in different
environmental conditions were examined. The research results showed that the problem of
microelements is typical not only for the Aral Sea region but also for other regions: deficit
and/or deficiency of 2 or more vital microelements is found in 96% of children with CMP. The
frequency of trace elements in children in all regions was high in Ca, Cr, Co, Cu, He and Zn.
Children living in the Aral Sea region were characterized by excessive levels of manganese,
bromine, and iodine; children living in relatively advantaged regions were characterized by
reliably high levels of potassium, chlorine, and iodine.

Keywords: children, cardiomyopathy, macro- and microelements, hair, Aral Sea

region.

Introduction

. At present, it has been established that success in protecting and promoting

children's health depends largely on the environment. An "optimal environmental health level
characterizes each region with significant environmental differences" and the presence of
specific features of adaptation reactions of organs and systems in a specific environmental
situation [10, 17, 19, 21, 23, 24]. Children, being in the process of growth and development,
functional instability of the div's regulatory systems, are the most sensitive to changes in
environmental conditions, so the health of the children's population can serve as a reliable
indicator of the region's ecological well-being [1, 6, 10, 14].

The important role of microelements (ME) in the vital functions of the human div is

beyond doubt. A significant number of studies are devoted to studying the influence of trace
elements on metabolism [6, 7, 8, 18]. The attention of a wide range of researchers is focused on
studying the content of macro- and microelements (ME) in human biosubstrates under various
pathological conditions living in various environmental conditions. The microelement status of
the population, especially children as the most sensitive part of the population, is one of the
objective ecological and hygienic indicators of the territory's well-being [4, 5, 12, 22]. Among
the conditions that contribute to the formation of inferior health of children, a special role is
assigned to environmental disadvantage against the background of deteriorating social and living


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conditions, primarily malnutrition with insufficient protein and vitamin and mineral components
[11, 12].

Deviations in the content of macro-and micronutrients caused by food, environmental,

and climato-geographical factors of particular relevance contribute to the early formation of
functional and structural cardiovascular disorders in children. The study of the role of elemental
status changes in the formation of cardiovascular pathology is particularly relevant. Several
studies have shown an essential role of macro- and microelements imbalance in the pathogenesis
of heart and vascular diseases in residents of biogeochemical provinces [9, 15, 16, 17, 26]. In
connection with the above, it is necessary to consider the diverse role of several chemical
elements in complex mechanisms of cardiovascular pathology formation.

Recently, the study of hair to detect the state of metabolism of trace elements in the div

and toxic effects of heavy metals is of increasing interest. Hair is a "mineral image" which is
proportional to the composition of trace elements in the whole div [3, 11, 18].

The importance of complex research on the balance of micro- and macro elements is

determined by the high biological activity and physiological significance of many of them,
complex relationships between them in physiological and especially pathological conditions.

The study aim

s to study the content of toxic and essential microelements in the hair of

children with cardiomyopathy living in areas with different climatic and geographical conditions.

Materials and methods

. Regions with different climatic and geographical conditions

and different ecological situation were selected for the study. Microelement composition of hair
was studied in 96 children with cardiomyopathies, hospitalized cardioreumatological
departments of the Republican Specialized Scientific-Practical Medical Center of Pediatrics and
Republican Children's Multidisciplinary Medical Center of the Republic of Karakalpakstan.
Depending on the region where children with cardiomyopathy live, the children were divided
into 2 groups:

Group 1 - 54 children (56.2%) living in relatively favorable regions (children from all

regions except Karakalpakstan Republic and Khorezm region);

2 group - 42 children (43.8%) living in an environmentally unfavorable Aral Sea region

(Republic of Karakalpakstan and Khorezm region).

Fig.1. Distribution of children by region of residence

56.2

43.8

0

10

20

30

40

50

60

Group 1

Group 2


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Evaluation of the content of chemical elements in the human div is the main issue in

studying the impact on his health of deficiency, excess or redistribution of macro and trace
elements.

The use of physico-chemical methods of research provides an opportunity to obtain data

in the most unexpected areas of medical biology. Nowadays, in the world, different practice
methods of quantitative determination of chemical elements in human hair are used.

The most used methods are atomic absorption spectroscopy, plasma mass spectrometry

and neutron activation analysis. These methods allow for the simultaneous determination of
several microelements in one sample of biosubstrate (blood, hair, nails, urine), which is very
important for studying the mutual influence of these elements. Each of these methods has its
advantages and disadvantages [21].

The Instrumental Neutron Activation Method (INAM) is also a multi-element method

that allows the determination of a significant number of elements in various biosubstrates with
too high sensitivity. An important advantage of the method is the simple sample preparation
without sample decomposition, no correction for blank experience, low sample flow, high
selectivity and exceptionally high throughput. The detection limits of the individual elements are
up to 1 ng/g.

The study of hair samples for the content of macro - and trace elements were conducted

in the Laboratory of Ecology and Biotechnology of the Institute of Nuclear Physics, Academy of
Sciences of the Republic of Uzbekistan by instrumental neutron activation analysis (INAM).

Hair for analysis was cut with scissors from 3-5 places at the occipital part of the head.

Hair length from root to distal part was 2-4 cm. Hair samples were thoroughly washed in
acetone, dried, weighed and packed in marked polyethylene bags. The prepared samples were
subjected to neutron-activation analysis. The technique of analysis is described in detail in paper
21.

Deviations of individual and group element profiles of children's hair from the norm were

noted based on accepted reference values of chemical elements contained in the hair. Statistical
processing was carried out using generally accepted methods using the universal application
package Microsoft Excel 2007 and Statistica 6.0.

Results and discussion.

Determination of chemical elements in hair serves as an

objective indicator of the state of the organism as a whole. Hair has some advantages in
comparison with other biosubstrates: a non-invasive prostate fence of the material, the possibility
of stable storage at room temperature for an unlimited time, a higher concentration of trace
elements in comparison with other bioobjects (blood, urine). Based on this, hair as a sufficiently
informative substrate to confirm the diagnosis of microelementosis is widely used by many
researchers [1, 11, 13].

In this connection, we determined the level of macro- and microelements in hair. The

results of the studies presented in Table 1 show that the content of some potentially toxic and
essential elements (Hg, Au, Ag, U, Sb, La, Na, Sc) in the hair is within the reference
(biologically permissible) values.


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Table 1: The element content of children with cardiomyopathy, µg/g

Element

Group 1

Group 2

Р

References values

Sc

0,0039±0,00031

0,0047±0,00028

<0,01

0,06-0,015

Ag

0,075±0,013

0,15±0,083

<0,01

0,1-0,25

Sb

0,059±0,0081

0,028±0,0026

<0,01

<0,2

La

0,015±0,0014

0,018±0,0025

>0,05

0,02-0,04

Au

0,014±0,0017

0,011±0,0029

>0,05

0,025-0,075

Hg

0,046±0,0064

0,061±0,0054

<0,01

0,1-0,3

U

0,13±0,024

0,27±0,037

<0,01

0,1-0,3

Note: * - validity of differences between children's scores relative to reference values; P - the
validity of differences between the scores of compared groups.

In other cases, various changes in the content of trace elements were noted, which are

presented in the following tables 2 and 3.

The following table 2. presents average values of macro- and micronutrients, the content

of which had similar changes in both group 1 and group 2 patients.

These changes were characterized by lower contents of Ca, Cr, Co, Cu, and Ge compared

to reference values, with higher values of Cl, Br, and I among children in both groups. More
pronounced changes were common among children in group 1: their Cl was 2.2 times greater
than allowed values, while children in group 2 were 1.5 times greater than allowed values
(p<0.001); and, bromine was nearly 2 times greater than allowed values, while children in group
2 were 1.2 times greater than allowed values; iodine was also 10 times greater than the reference
values of children in group 1 and 2 times greater than allowed values in comparison group 1
(p<0.001).

Table 2: The element content of children with cardiomyopathy, µg/g

Element

Group 1

Group 2

Р

References values

Na

870±115

890±130

>0,05

400-900

Cl

5100,0±610,0*

3400,0±420,0*

<0,001

1200-2300

Ca

660,0±71,0*

930,0±135,0*

<0,001

1000-1500

Cr

0,24±0,024*

0,22±0,016*

>0,05

0,35-1,0

Co

0,031±0,0035*

0,030±0,0038*

>0,05

0,05-0,1

Cu

6,1±0,61*

6,9±0,41*

>0,05

10-15

Se

0,43±0,024

0,45±0,015

>0,05

0,35-1,0

Br

6,7±1,5*

4,1±1,3*

<0,001

1,0-3,5

I

10,0±4,3*

2,1±1,4*

<0,001

0,5-1,0

Note: * - validity of differences between children's scores relative to reference values; P - the
validity of differences between the scores of compared groups.

Children in Group 1 had low Fe and Zn levels relative to both reference values and

children in Group 2 (p<0.001). However, Aral Sea region children, in contrast to children in the


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comparison group, had significantly higher levels of manganese (-1.2±0.30 µg/g versus
0.64±0.061 µg/g, respectively).

Besides, children in Group 1 were characterized by excessive potassium and rubidium

content (p<0.001), while children in the Aral Sea region were within reference values. And the
level of potassium exceeded the permissible values (800-1500 µg/g) 1.3 times (2000.0±350.0
µg/g, p<0.001), and rubidium 1.6 times (1.6±0.30 µg/g, p<0.01).

Table 3: The element content of children with cardiomyopathy, µg/g

Element

Group 1

Group 2

Р

References values

Mn

0,64±0,061

1,2±0,30*

<0,01

0,4-1,0

Fe

19,0±0,75*

24,0±1,0

<0,001

20-30

Zn

127,0±8,3*

153,0±8,1

<0,01

150-200

K

2000,0±350,0*

1200,0±200,0

<0,001

800-1500

Rb

1,6±0,30*

0,74±0,012

<0,001

0,5-1,0

Note: * - validity of differences between children's scores relative to reference values; P -

the validity of differences between the scores of compared groups.

Rubidium has a physiological effect on muscle contractility and acid-base balance similar

to potassium. The mechanisms of toxicity of elevated concentrations of rubidium are also similar
to those of excess potassium toxicity [14].

Figures 2 and 3 show the frequency of microelementosis in sick children, depending on

the region of residence.

Fig. 2. Microelement frequency in sick children living in a relatively favorable region.

As the research results showed, the problem of trace elements is typical not only for the

Aral Sea region but also for other regions. The conducted studies of microelements in hair
showed that 96% of children with IUC had a deficit or insufficient content of 2 or more vital
microelements relative to reference values.

14

19

12

22

36

36

-7

-10

-24

-76

-20

-20

-85

-98

-36

-10

-27

-2.5

-37

-100

-80

-60

-40

-20

0

20

40

60

Na

Cl

Ca

Cr

Mn

Fe

Co

Cu

Zn

K

Se

Br

I

norm

flaw

surplus


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Fig. 3. Microelement frequency in children with CMP living in the Aral Sea region

A detailed analysis of children's macro- and micronutrient levels revealed that almost all

of the study subjects, regardless of their region of residence, had a deficit or insufficient copper
content in their hair (Figure 4).

Fig.4. Number of children (%) with copper deficiency/insufficiency by region of residence

As revealed in Figure 5.5, children with a copper deficiency were 2.5 times more likely to

be in Group 1 (46.3% vs 18.6%, p<0.001), while its deficiency prevailed in Group 2 (86% vs
53.7%, p<0.001). Its average values were 6.1±0.6 µg/g in the 1st group and -6.9±0.41 µg/g in the
2nd group, which is reliably below the reference values. At a low level of Cu in the organism,
the risk of cardiovascular pathology increases significantly [13].

Ceruloplasmine enzyme containing Cu plays an important role in the mechanisms of

antioxidant protection in myocardial ischemia; its content varies depending on the degree of

30

10

7

21

12

16

16

-7

-32

-7

-88

-9

-5

-84

-93

-35

-35

-23

-23

-56

-100

-80

-60

-40

-20

0

20

40

Na

Cl

Ca

Cr

Mn

Fe

Co

Cu

Zn

K

Se

Br

I

норма

flaw

surplus

0

20

40

60

80

100

Deficiency

Flaw

18.6

86

46.3

53.7

Group 2

Group 1


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coronary heart muscle damage. In case of Cu deficiency, the activity of lysiloxylase decreases,
resulting in the normal formation of collagen and elastin, which in turn leads to pathological
changes in the connective tissue structures of the heart and blood vessels [2, 9].

The vast majority of children living in the Aral Sea region had iodine deficiency (60.5%),

while the number of children in group 1 was 1.4 times less and accounted for 43.9% (p<0.01).
Overweight was found in 34.1% of group 1 children and 6.97% of children living in the Aral Sea
region. Average iodine levels in children in the 1st group were significantly higher than
comparison and reference values (p<0.01). However, the lack, as well as an excess of chemical
elements, depresses protective mechanisms [2, 8].

Chromium deficiency was found among children in both the 2nd group and comparison

group in almost equal amounts (30.2 and 29.3% respectively, p>0.05). However, its deficiency
prevailed among children in the Aral Sea region (53.5% vs 43.9%, p<0.001).

The literature provides examples of hypocalcaemia and cardiomyopathy among children

with rickets [15]. In our research, calcium deficiency prevailed in most children, regardless of
their region of residence. However, there were 7.4 times more children with calcium deficiency
in Group 1 (Figure 5). There was a more pronounced decrease in children in Group 1, compared
to Group 2 (660.0±71.0 µg/g vs 930.0±135.0 µg/g, p<0.001).

Fig.5. Percentage of children with calcium deficiency/insufficiency by region of residence.

According to the literature, in DCMP there is an increase in serum content of copper, the

severity of which is inversely proportional to the size of the FM and heart index of such patients,
as well as a decrease in zinc levels in comparison with healthy and sick other cardiovascular
diseases, in particular coronary heart disease. However, the significance of these changes in the
origin of the disease remains a subject of research so far [13].

It is known that the entry of calcium into cardiomyocytes occurs with the direct

participation of such chemical elements as aluminum, copper, iron, lithium, manganese,
molybdenum, lead, strontium, vanadium and zinc, and deviation from the norm of any of them in

0

10

20

30

40

50

60

70

Deficiency

Flaw

2.3

65.1

17.1

65.9

Group 2

Group 1


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the div may cause the formation of diastolic dysfunction of the left ventricle [13], coronary
circulation disorders and ventricular fibrillation. According to W. Nordhoy et al., calcium
deficiency may be one of the causes of PQ interval shortening and QT elongation [27].

In case of deficiency of Co, heart rhythm disorders, asthenic syndrome develop, and its

excessive intake into the div may lead to "cobalt" cardiopathy [2, 8].

In both Group 1 and 2, the insufficient content of cobalt was found in almost the same

number of children (80.5% and 81.4%, p>0.05) and its average values were 0.031±0.0035 µg/g
and 0.030±0.0038 µg/g, which is significantly lower than the acceptable values (p<0.01) (Table
2).

Potassium content was insufficient in 37.2% of children, and 30.7% of patients living in

the Aral Sea region had a deficit. This indicator was 24.4% and 12.2% in Group 1, respectively.
However, it was almost 3 times more prevalent among children in the 1st group, compared to
children in the 2nd group (34.1% versus 11.6%, p<0.001). Its average values were 2000.0±350.0
µg/yr, which is reliably above the upper bound (800-1500 µg/yr) (Figure 6).

Fig.6. Percentage of children with potassium deficiency/insufficiency and overproduction,

depending upon the region of residence.

Selenium (Se) is a cardioprotector protecting the myocardium from cardiotoxic

substances, xenobiotics, viruses. It helps to normalize lipid metabolism and prevent the
development of atherosclerosis. Se deficiency is a risk factor for the development of CHD, which
is associated with the higher morbidity of this pathology in selendeficiency areas [15, 16].
Cardioprotective effect of Se on the reduction of frequency of reperfusion arrhythmias has been
shown. Cardioprotective and angioprotective effect of Se is significantly related to the
antioxidant role of this ME. Selenium-containing proteins are an essential component of the
antioxidant protection system. An important role of selenoprotein P in maintaining normal
function of the endothelium of vessel walls damaged by one of the products of oxidative stress
peroxynitrite has been shown [15, 16].

37.2

30.7

11.6

24.4

12.2

34.1

0

5

10

15

20

25

30

35

40

Flaw

Deficiency

Surplus

Group 2

Group 1


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Some studies have shown a connection between selenium deficiency and the

development of cardiomyopathy and other cardiovascular diseases (myocardial infarcts, coronary
heart disease) [13, 15, 16].

Studies found that selenium deficiency was found in only 2 (4.9%) of Group 1 patients,

but was reported in nearly 1/3 of Group 2 children (32.6% vs. 21.95%; p<0.001). Average
selenium was below the reference values in both groups: 0.29±0.024 µg/y in Group 1 children
and 0.31±0.015 µg/y in Group 2 children (p>0.05).

Zinc deficiency was found in 34.9% of children in group 2 and 43.9% of children in

group 1. In other patients, the average zinc content was comparable to the norm (150-200 µg/g)
(Figure 7). Because of the large number of children with zinc deficiency in Group 1, its mean
value was 127.0±8.3 µg/g, which is significantly lower than the norm and comparison group
values (153.0±8.1 µg/g) (Table 3).

Zn deficiency is associated with the development of such pathological conditions as

congestive heart failure, rheumatic heart disease. Zn and Cu deficiency limits the activity of
antioxidant metalloenzymes, promotes the formation of endothelial dysfunction and vascular
permeability disorder [2].

Fig.7. Percentage of children with zinc deficiency, by region

Bromine was excessive among children in the 1st group (39% vs 13.9%), and it was

deficient among children in the 2nd group (18.6% vs 2.4%). Group 1 children (6.7±1.5 µg/y)
were 1.9 times more likely to have bromine, while Group 2 children (4.1±1.3 µg/y) were 1.2
times more likely to have bromine (1.0-3.5 µg/y).

Iodine content in group 1 was 10±4.3 µg/g, which was 10 times higher than the reference

values (0.5-1.0 µg/g). In children in Group 2, its value was 2 times higher than the reference
values of 2.1±1.4 µg/g.

0

10

20

30

40

50

Flaw

34.9

43.9

Group 2

Group 1


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Insufficient or excessive content of other elements (iron, manganese) was insignificant in

children. Most children's scores were similar to reference values regardless of their region of
residence. Analysis of the macronutrient and trace element indices in the hair suggests that most
children have a physiological level in their bodies. Concentrations of the elements were either at
or below acceptable limits.

But it should be noted that manganese plays a significant role in myocardial energy

supply [11]. Studies have shown that myocardial infarction is selectively activated by MPPSOD
[11]. High cardioprotective activity of Mn synthetic preparations in myocardial ischemia has
been noted [2].

When studying the micronutrient status of each child with cardiomyopathy regardless of

the region of residence, it can be assumed that in addition to the main disease, 16% of children
have disorders of the nervous system, 15% have disorders of the immune system, and 12% have
disorders of the urinary tract.

Thus, the data obtained indicate a significant role of deficiency, excess and imbalance of

some macro- and microelements in the development of cardiomyopathy in children.

Conclusions

.

1.

Microelements are typical not only for the Aral Sea region but also for other regions:

deficit and/or deficiency of 2 or more vital microelements are found in 96% of children with
IUC.

2.

The frequency of trace elements in children in all regions was high in Ca, Cr, Co, Cu, He

and Zn. Children living in the Aral Sea region were characterized by excessive levels of
manganese, bromine, and iodine (p<0.01); children living in relatively favorable regions were
characterized by reliably high levels of potassium, chlorine, and iodine (p<0.01).

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background image

European Journal of Molecular & Clinical Medicine

ISSN 2515-8260 Volume 7, Issue 2, 2020

1824

1824

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Namazbayeva Z.I. Microelement and cytological status of children in urban areas: scientific publication / Z. I. Namazbayeva, L. T. Bazeluk [et al.] // Labor medicine and industrial ecology. - Moscow, 2011. - №6. - pp.22-25.

Some Mechanisms of Selenium Participation in Pathology Development / V. Vapirov, M. E. Shubina, N. V. Vapirova et al. (in Russian) // Eco-analytical control of natural objects in Karelia: Collection of articles. - Petrozavodsk: PetrSU, 2002. —pp. 47—56.

Rozyhodzhaeva G.A. Study of microelement composition of hair in patients with carotid atherosclerosis: a scientific publication / G.A. Rozyhodzhaeva, S.K. Khudoynazarov [et al.] // Therapeutic bulletin of Uzbekistan. - Tashkent, 2012. - №2-3. - pp.90-91.

Rybkin V. S., Bogdanov N.A., Chuikov Yu. A. Heavy metals as a factor of possible ecologically caused diseases in Astrakhan region // Hygiene and sanitation. - 2014. - Т. 93, № 2. - pp. 27–31.

Sviridov, C. V. What are the "silent" microelements about: a scientific publication / S. V. Sviridov, S. V. Fedorov [et al.] // Vestnik Intensive Care. - М., 2012. - №2. - pp.11-17.

Svyatova N.V., Sitdikova A.A., Misbakhov A.A., Romanyuk O.N., Golovina E.A. Interrelation of microelement status of children living in a megapolis and motor transport as a source of influence of striking factors of the dangerous situations initiated by human economic activity // Fundamental studies. - – 2015. - – № 2-21. - pp.4665- 4670.

Senatorova A.S., Boychenko A.D., Buzhinskaya N. A.S., Boychenko A.D., Buzhinskaya N.R., etc. / Secondary cardiomyopathy in children; pod. ed. A.S. Senatorova. - J.: A new word, 2011. – p. 344.

Rock A. V. Chemical elements in human physiology and ecology (in Russian) / A. V. Skalny. - Moscow: ONIKS 21 Century Publishing House: World, 2004. – p. 216.

Suleymanova D. N. Neutron-activating analysis of the hair of children with anemia in the study of microelements imbalance / D. N. Suleymanova, S. M. Mukhamedov, D. F. Mamatkulova, M. U. Narmetova et al. // Actual problems of hematology and transfusiology: a collection of scientific articles // Proc. of Conf. (October 27-28, 2011, Tashkent). - Tashkent, 2011. - pp. 63-64.

Tupikov V. A., Naumova N. L., Rebezov M. B. Elemental composition of hair as a reflection of the ecological situation // Bulletin of South Ural State University. - 2012. - № 21 (280). - pp. 119–122.

Turbine E.S. The influence of air pollution by suspended solids on the health of children in Birobidzhan // Izvestia Samara Scientific Center of the Russian Academy of Sciences. -2010. - Т. 12, № 1(7). - pp.1710-1714.

Turbine E.S. The influence of air pollution on the morbidity of respiratory diseases of preschool children in Birobidzhan: Author's thesis. ... doctor of medical sciences. Birobidzhan, 2012. P.138.

Inman M, Daneman D, Curtis J, Sochett E, Clarke A, Dunger DB, Deanfield J, Mahmud FH. Social Determinants of Health Are Associated with Modifiable Risk Factors for Cardiovascular Disease and Vascular Function in Pediatric Type 1 Diabetes. J Pediatr. 2016 Oct; 177: 167-172. doi: 10.1016/j.jpeds.2016.06.049.

Nordhoy W., Anthonsen H.W., Bruvold M. et al. Manganeseionsas intracellular contrastagents: proton relaxation and calcium interactionsinr at myocardium // NMR Biomed. - — 2003. - Vol. 16 (2). - pp. 82-95.

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