Features of immunological reactivity in Sami women

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BACKGROUND: The Sami are a small group of indigenous people of the Russian Federation. The Sami have one of the lowest birth rates among all the peoples of the North of Russia. They often have more health problems than residents of other nationalities in the Murmansk region, due to a high incidence of acute respiratory infections. Extreme climatic and geographical conditions of the Arctic have a negative impact on immunological reactivity.

AIM: To identify the features of immunological reactivity in Sami women.

MATERIALS AND METHODS: Forty-nine practically healthy Sami women aged from 21 to 44 years living in the Lovozero Village in the Murmansk region were examined. A control group consisting of 50 practically healthy Russian women of the Arkhangelsk region of the same age range was used. The hemogram, phagocytic activity of neutrophils of peripheral venous blood, and the content of lymphocytes with CD3, CD4, CD8, and CD10 phenotypes were studied by indirect immunoperoxidase reaction (Sorbent, Moscow) and flow cytometry (Beckman Coulter Immunotech, France). Additionally, concentrations of IgM, IgG, IgA, sCD54, and sCD62L (Bender MedSystems, Austria) were determined by enzyme immunoassay, circulating immune complexes (CIC) were determined by the precipitation method. The total amount of microflora, cytogram, phagocytic activity of neutrophils, the sorption capacity of epithelial cells, the content of sIgA and CIC IgG were studied in the separated mucous membranes of the pharynx, intestines, and urine. For comparison between groups, the independent samples t-test or the nonparametric Mann–Whitney U-test was used depending on the distribution.

RESULTS: In Sami women, the frequency of deficiency of phagocytic activity of blood neutrophils and mucosal secretions was higher than in the control group. Increased reactions of cell-mediated and antibody-dependent cytotoxicity of lymphocytes were recorded. The frequency of elevated concentrations of CIC was higher in the Sami women than in the control group. A remarkable feature of the Sami immune reactivity was high concentrations of IgA and IgM against a background of low IgG content.

CONCLUSION: In Sami women, the percentage of actively phagocytic neutrophil granulocytes of peripheral venous blood and mucous membranes was lower than in the control. A distinctive feature of the immunoglobulin profile of the blood serum of Sami women was the low IgG content against the background of increased concentrations of CIC, including immunoglobulins of this class. Sami women had higher levels of leukocyte migration into mucosa-associated mucosal tissue, which was correlated with a decrease in the sorption capacity of epitheliocytes, phagocytic activity of neutrophils, and concentrations of secretory immunoglobulins.

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Introduction. One of the most important issues in the field of biology is to identify the features of interaction and the ratio of local and systemic immune responses. There is no clear information about the state of the local immune defense of the respiratory, urinary and digestive systems. There are isolated data on the role of local immune defense defects in the formation of systemic immune reactions [1, 2]. High incidence, its chronic course, predisposition to the spread of inflammation occur against the background of a decrease in the protection of local immunity [3, 4]. Deficiency of IgA content is the most common defect of immune protection in residents living in the North [5]. The significance and reasons for the involvement of hyperergic reactions in compensating for IgA insufficiency are not entirely clear [6, 7]. Cases of the development of a systemic inflammatory response syndrome, which is often associated with a deficiency of immune responses in the area of distress, pose a big problem. [8, 9, 10, 11].
The purpose of our study was to identify the correlation between the state of local and immune reactions in Sami women living in the village of Lovozero, Murmansk region. The village of Lovozero (68°00'22" s.w. 35°00'57" v.d.) of the Lovozersky district of the Murmansk region of the Russian Federation is located beyond the Arctic Circle in the central part of the Kola Peninsula. The territory belongs to an extremely uncomfortable zone with an intense impact of harsh natural and climatic conditions on people and the strain of adaptation systems [12, 13, 14].
Methods. 49 practically healthy Sami women aged 21 to 44 years living in the Murmansk region in Lovozero village were examined. The comparison group consisted of 50 practically healthy women of the Arkhangelsk region of the same age range.
All studies were conducted with the consent of volunteers and in accordance with the requirements of the document "Helsinki Declaration of the World Medical Association. Ethical principles of conducting medical research with the participation of a person as a subject" (1964, as amended and supplemented in 2013), as well as approved and approved by the Commission on Biomedical Ethics at the IFPA of the FITSKIA Ural Branch of the Russian Academy of Sciences (Protocol No. 5 of 11.02.2022).
The complex of immunological examination included the study of hemogram, phagocytic activity of neutrophil leukocytes of peripheral blood. The number and ratio of hemogram cells were calculated in blood smears stained by the Romanovsky–Gimze method. The phagocytic activity of neutrophil granulocytes was determined using the "Reacomplex" test kit (Russia). The phenotypes of lymphocytes (CD3+, CD4+, CD8+, CD10+, CD95+) were studied by indirect immunoperoxidase reaction using monoclonal antibodies ("Sorbent", G. Moscow) and flow cytometry using the Epics XL apparatus of Beckman Coulter (USA) reagents "Immunotech a Beckman Coulter Company" (France). The content of immunoglobulins (IgM, IgG, IgA) in blood serum was studied by enzyme immunoassay; reactions were evaluated using a Multiskan MS photometer (Labsystems, Finland). The concentration of circulating immune complexes (CEC) was determined by the standard precipitation method using 3.5; 4.0; 7.5% PEG-6000 in blood serum. The reaction was evaluated on an automatic enzyme immunoassay analyzer "Evolis" of the company "Bio-RAD" (Germany).
Cytogram, phagocytic activity of neutrophil granulocytes, the sorption capacity of epithelial cells, the content of secretory IgA (sIgA) and CEC IgG were studied in the separated mucous membranes of the pharynx, gastrointestinal tract and urine. The composition and content of bacteria, the cytogram was determined using a direct research microscope Nicon Eclipse Ni-U (Japan) and standard bacteriological methods.
Statistical processing of the obtained data was carried out using the application software package "Statistica 21.0" (StatSoft, USA). The results are presented as the arithmetic mean and the error of the mean (M±m). Independent sampling t-test or nonparametric Mann-Whitney U-test were used for comparison between groups. The Pearson correlation coefficient was calculated for the two-dimensional normal distribution data. The Spearman correlation coefficient was calculated for two-dimensional data of abnormal distribution. The critical significance level (p) in the work was assumed to be 0.05.
Results. It was found that the total leukocyte count in the peripheral venous blood of Sami women was higher (5.59±0.21 and 4.64±0.19 x 109 cells/l in the comparison group; p=0.028) due to neutrophil granulocytes (3.01±0.12 and 2.43±0.11 x 109 cells/l; p=0.017) mainly with 2 and 3 segments of cores (respectively 1.12±0.07 and 0.83±0.05x109 cl/l; p=0.006 and 1.28±0.07 and 0.94±0.06X109 cl/l; p=0.007). Absolute neutropenia (<2x109 cells/l) was detected in 18.52 and 34% of women, respectively. The phagocytic activity of neutrophils and the intensity of phagocytosis are lower on average in Sami women (51.42±1.21 and 60.10±1.60 %; p=0.015) and (3.92±0.14 and 4.88±0.35 pcs.; p=0.036), respectively, which is confirmed by a higher frequency of registration of active phagocyte deficiency by 1.5 times (30.77 vs. 20%). At the same time, absolute neutropenia (<2x109 kl/l) was detected almost 2 times less frequently, which means that the low content of circulating neutrophils mainly concerns secreting granulocytes. It can be assumed that the secretory activity of granulocytes, despite the decrease in their phagocytic function, does not noticeably suffer. An indirect confirmation of this assumption is the absence of differences in the average content of circulating eosinophils and monocytes, the first reaction of which is mainly secretory activity. In women of both groups, the contents of these cells were statistically insignificant (0.12±0.01 and 0.14±0.01X109 cl/L) and (0.35±0.03 and 0.34±0.02X109 cl/L); elevated concentrations of these cells were observed more often in the Murmansk region (7.41 and 11.11% vs. 4 and 8%).
In Lovozero women, the average absolute content of lymphocytes is slightly higher (2.11±0.08 and 1.74±0.09 x 109 cells/l; p=0.032) due to mature T cells with CD3 receptor (1.25±0.10 and 0.91±0.03 x 109 cells/l; p<0.001), cytotoxic CD8 lymphocytes (1.00±0.11 and 0.35±0,02X109 cl/l; p<0.001), T-helper cells (0.95±0.09 and 0.32±0,02X109 cl/l) and cells capable of CD10 proliferation (1.02±0.16 and 0.29±0,02X109 cl/l; p<0.001). Elevated levels of lymphocytes with CD8, CD4 and CD10 receptors were found at 75.51; 51.02, respectively; 71.43% of cases, which indicates the activation of cell-mediated cytotoxicity and lymphoproliferation.
The average IgA content in the peripheral venous blood of all Sami women is within the limits of physiological standards (on average 2.46 ± 0.23 in the control 1.42± 0.13 g / l; p < 0.001); 36% of women in the Arkhangelsk region revealed their deficiency. The Sami have a disproportion of high levels of circulating IgM in the blood (2.30±0.11 vs. 1.02±0.06 g/l; p<0.001; elevated concentrations of 61.22%) and relatively low levels of IgG (5.32±0.36 vs. 11.89±0.96 g/l; p<0.001; deficiency of 73.47%).
Elevated concentrations of circulating immune complexes containing IgA, M, G were detected in the blood of the examined women of S. Lovozero. In 14.29% of the Sami above the physiological limit of the concentration of CIC IgA with an average content of 2.02 ± 0.38 g / l. The average CIC IgM content was 3.22±0.53 g/l, elevated levels of which were recorded in 32.65% of cases. And almost all women (97.96%) had high concentrations of CEC IgG on average 10.93±0.73 g/l. On the contrary, in women of the Arkhangelsk region, the levels of the average CEC IgA and IgM are lower and are within physiological boundaries (1.25±0.18 and 2.04±0.21 g/l, respectively; p<0.001). Concentrations of CIC IgG were (3.39±0.27 g/l), elevated levels were detected in 34% of the examined. So, the Sami have higher concentrations of IgA, IgM and IgG CEC and their increased concentrations are more often recorded.
Table 1 presents the features of the content of immunocompetent cells and indicators of local immunity in the separated mucous membranes of the intestine, urinary system and pharynx in the examined Murmansk and Arkhangelsk regions.
Statistically significant differences were found with respect to cytograms of the mucous membranes of the pharynx and urination organs: in Sami, the relative content of cells is significantly higher. The concentration of IgG CIC in urine is also higher against the background of low sorption activity of epithelial cells (Table 1). In our opinion, these data determine the risk of adverse effects of climatic conditions on the tissues of these systems.
So, the Sami have a higher frequency of phagocytic mucosal protection deficiency and sIgA deficiency, as well as the sorption capacity of the epithelium against a background of higher concentrations of CIC (Table 2). The decrease in the sorption capacity of the epithelium and phagocytic protection occurs against the background of increased migration of neutrophils, macrophages and lymphocytes (57,14–100%). So, a decrease in the levels of sorption activity of epithelial cells and phagocytic protection, as mechanisms of local immune reactions, is compensated by an increase in the migration ability of leukocytes providing cytolytic protection. The increased level of leukocyte migration into the mucous membranes indicates the activation of hemodynamic reactions and the secretion of adhesion molecules. This is confirmed by data on more significant concentrations of bacteria of representatives of the normal microflora of the mucous membranes (Fig.1).

Discussion of the results. The immune status of Sami women is characterized by the usual activation of cell-mediated mechanisms of cytotoxicity, phagocyte activity deficiency and accumulation of CEC, but these features are more pronounced in them. The Sami have a high frequency of registration of deficiency of phagocytic protection of neutrophil granulocytes both in the blood and on the mucous membranes. It is known that neutrophil granulocytes are sources of almost all known primary and secondary mediators of inflammatory reactions and cytokines, not only phagocytize, but also are antigen-reactive cells, perform antibody-dependent cytolysis of affected, transformed and old cells [15, 16, 17, 18, 19, 20, 21]. It is believed that a large population of neutrophils (about 70%) performs mainly phagocytic functions, a smaller one is secretory. A decrease in the level of active phagocytes during activation of the secretory function of neutrophils is confirmed by a sufficiently large number of convincing facts [22, 23, 24, 25, 26, 27, 28, 29]. IL-17 of neutrophils stimulates neutrophil infiltration, activating their migration ability primarily [30].
Activation of cell-mediated cytotoxicity with increasing concentrations of circulating cytotoxic T-lymphocytes means activation of mechanisms of destruction of cells, carriers of antigenic information (transformed, tumor, functionally obsolete cells labeled for apoptosis). Such mechanisms can be lysis by natural killers and cytotoxic lymphocytes, antibody-dependent lysis by neutrophils and macrophages [31, 32, 33, 34].
The second feature of the Sami immune reactivity is the preservation of a relatively high degree of antibody activity of immunoglobulins of classes A and M. It is known that IDMS are 1000 times more effective at binding cells that carry antigenic structures or microorganisms on their surface in cytolysis and bacteriolysis tests [35, 36, 37, 38]. This is the main feature of preventive immune reactions in practically healthy Sami women. A relatively high level of sIgA antibody formation by the musico-associated lymphoid tissue provides activation of systemic reactions [39]. It is known that antibodies of this class reduce the adhesion of bacteria and viruses on the surface of epithelial cells [4].
Higher concentrations of CIC are explained not only by a high level of antibody formation, but also by a deficiency of phagocytic activity. It is known that elevated levels of CIC content are caused by an increase in the rate of their formation over the rate of elimination with a deficiency of phagocytic activity or due to insufficient activity of the complement system. It is known that the formation of immune complexes is a physiological reaction in which, in addition to specific antigen-antibody binding, there is also a non-specific interaction between Fc structures. Fc receptors are present in almost all cells, they bind aggregated Ig or immune complexes. The initiating action of the complexes includes activation of plasma components and Hageman factor. The consequences of reactions involving complexes are adhesion of complexes on neutrophils, macrophages, erythrocytes, platelets, and other cells; effects of chemotaxis for mobile phagocytes, lymphocytes, and cell lysis. When activated in this way, agglomeration of cells occurs with the formation of clusters and rosettes [40]. Previously, data were obtained that the aggregation activity of erythrocytes, platelets and leukocytes of peripheral venous blood in Arctic residents is 1.5-2.5 times higher than that of people living in more favorable climatic conditions [41].
The formation of local immune reactions is greatly influenced by the level of sorption activity of epithelial cells. The protective role of the sorption capacity of epitheliocytes is determined by the possibility of fixation of microorganisms, their exocytic damage and clearance together with cells through the secret [42, 43]. A direct relationship has been established between the sorption capacity of the mucosal epithelium and the content of not only sIgA, but also serum immunoglobulins of this class [44]. A decrease in the sorption capacity of the mucosal epithelium can occur with a decrease in the levels of IgA, IgM, IgG, as well as the activity of the complement system, lysozyme and contribute to the weakening of humoral protection on the mucous membranes [45, 46, 47].
Conclusion. Thus, Sami women have higher levels of phagocytic defense deficiency, which inhibits CIC clearance. A decrease in the frequency of neutropenia registration does not compensate for the deficiency of phagocytic protection, but increases the secretory activity of neutrophils.
The secretory activity of leukocytes is associated with their higher migration capacity into the mucous membranes, which does not compensate for the low activity of local phagocytes, the sorption capacity of epithelial cells and sIgA.
A feature of the Sami immune reactivity is higher concentrations of IgA and IgM against a background of low IgG content. The preservation of antibody formation at the initiation stage, and not at the phase of its prolongation, can be explained by the extreme level of antigen influence. There is information in the literature about "antigenic stress" characteristic of residents of extremely uncomfortable climatic zones [6, 7].
The migration activity of leukocytes into the mucous membranes, including phagocytes, is noticeably higher in the Sami. The migration activity of leukocytes is initiated by preventive reactions in places of distress and begins with reactions of hemodynamic changes. Perhaps, therefore, the concentration of granulocytes and lymphocytes in the Sami blood is higher due to cells with cytolytic activity.



About the authors

Anna V. Samodova

N. Laverov Federal Center for Integrated Arctic Research

Author for correspondence.
Email: annapoletaeva2008@yandex.ru
ORCID iD: 0000-0001-9835-8083
SPIN-code: 6469-0408
Scopus Author ID: 5534446910
ResearcherId: Q-5144-2017

Cand. Sci. (Med.), leader research associate

Russian Federation, 249 Lomonosova avenue, 163000, Arhangel'sk

Liliya K. Dobrodeeva

N. Laverov Federal Center for Integrated Arctic Research

Email: dobrodeevalk@mail.ru
ORCID iD: 0000-0003-3211-7716
SPIN-code: 4518-6925
Scopus Author ID: 6603579532
ResearcherId: J-3753-2018

Dr. Sci. (Med.), professor, chief research associate

Russian Federation, Arkhangelsk

Svetlana N. Balashova

N. Laverov Federal Center for Integrated Arctic Research

Email: ifpa-svetlana@mail.ru
ORCID iD: 0000-0003-4828-6485
SPIN-code: 3475-3251
Scopus Author ID: 57191543951
ResearcherId: Q-4942-2017

Cand. Sci. (Med.), senior research associate

Russian Federation, Arkhangelsk

Ksenia O. Pashinskaya

N. Laverov Federal Center for Integrated Arctic Research

Email: nefksu@mail.ru
ORCID iD: 0000-0001-6774-4598
SPIN-code: 2201-0289
Scopus Author ID: 57261870200
ResearcherId: AAM-3348-2020

junior research associate

Russian Federation, Arkhangelsk


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