Alterations in T cell immunity over 6–12 months post-COVID-19 infection in convalescent individuals: a screening study

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Abstract

Acute COVID-19 is a viral infection caused by a severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) that results in dramatically decreased peripheral blood CD3+ T cell count apparently due to alterations of thymic T cell maturation, that can persist long term afterwards. Therefore, we analyzed the levels of peripheral blood TRECs (T-cell receptor excision circles), and investigated the main alterations in peripheral blood T cell subsets in COVID-19 convalescents. We performed molecular quantification of TRECs with “TREC/KREC-AMP PS” kit and flow cytometric analysis of peripheral blood lymphocytes from three groups of patients. The first group contained 109 samples from COVID-19 convalescents (6–12 month post-acute COVID-19) with normal levels of TRECs (TRECn); the second was formed from COVID-19 convalescents (6–12 month post-acute COVID-19) with decreased levels of TRECs (TREClow, n = 29), and healthy control group (HC, n = 18). We noticed no significant differences between all three groups in CD3+ T cell relative and absolute numbers. However, CD4+ T cell frequencies were decreased in TREClow and TRECn groups compared to HC (40.8% (31.6; 50.1) and 46.4% (40.0; 53.0) vs 53.5% (47.36; 56.9), p < 0.001 and р = 0.004, respectively). Furthermore, Th cell levels were decreased in TREClow patients vs HC and TRECn groups (701 cell/1 µL (478; 807) vs 1005 cell/1 µL (700; 1419), р = 0.020, and 876 cell/ 1 µL (661; 1046), р = 0.008, respectively). Finally, both groups of COVID-19 convalescents had increased frequencies of circulating CD8+ T cells — 29.4% (20.7; 39.7) in TREClow group, 26.5% (21.1; 32.7) in TRECn group vs 21.3% (17.1; 26.0) in healthy controls (p = 0.024 and р = 0.026, respectively). In TRECn group, CD8+ T cell count was elevated vs control range (508 cell/1 µL (372; 622) vs 356 cell/1 µL (247; 531), р = 0.044). Thus, COVID-19 convalescents (6–12 month post-acute COVID-19) showed an imbalance in CD4+ and CD8+ T cell level even at 6–12 months post-acute SARS-CoV-2 infection, and the observed changes in peripheral blood T cells could be closely related to the alterations in thymic T cell maturation and differentiation. Such a long-term decline in TREC levels in the circulation may have a profound impact on immune system functions and requires immunocorrection therapy.

About the authors

A. V. Zurochka

Institute of Immunology and Physiology, Ural Branch of the Russian Academy of Sciences; Federal Research Institute of Viral Infections “Virom”

Email: igorek1981@yandex.ru

DSc (Medicine), Professor, Honored Scientist of the Russian Federation, Leading Researcher, Laboratory of Immunopathophysiology; Leading Researcher, Laboratory of Transmissible Viral Diseases

Russian Federation, Yekaterinburg; Ekaterinburg

M. А. Dobrynina

Institute of Immunology and Physiology, Ural Branch of the Russian Academy of Sciences; Federal Research Institute of Viral Infections “Virom”; State Research Center of the Russian Federation — Federal Medical Biophysical Center named after A.I. Burnazyan of the Federal Medical and Biological Agency of the Russian Federation

Email: igorek1981@yandex.ru

PhD (Medicine), Associate Professor, Researcher, Laboratory of Immunopathophysiology; Senior Researcher, Laboratory of Transmissible Viral Diseases; Associate Professor, Department of Internal Medicine, Medical and Biological University of Innovation and Continuing Education

Russian Federation, Yekaterinburg; Yekaterinburg; Moscow

E. A. Safronova

State Research Center of the Russian Federation — Federal Medical Biophysical Center named after A.I. Burnazyan of the Federal Medical and Biological Agency of the Russian Federation; South Ural State Medical University

Email: igorek1981@yandex.ru

PhD (Medicine), Associate Professor, Associate Professor of the Department of Polyclinic Therapy and Clinical Pharmacology; Lecturer at the Department of Therapy

Russian Federation, Moscow; Chelyabinsk

V. A. Zurochka

Institute of Immunology and Physiology, Ural Branch of the Russian Academy of Sciences; Federal Research Institute of Viral Infections “Virom”

Email: igorek1981@yandex.ru

DSc (Medicine), Senior Researcher; Senior Researcher, Biotechnology Laboratory, Russian-Chinese Center

Russian Federation, Yekaterinburg; Ekaterinburg

A. A. Zuikova

Federal Research Institute of Viral Infections “Virom”

Email: igorek1981@yandex.ru

Intern of the Laboratory of Transmissible Viral Diseases

Russian Federation, Ekaterinburg

G. P. Sarapultsev

354 Military Clinical Hospital of the Russian Ministry of Defense

Email: igorek1981@yandex.ru

Head of Endoscopy Department

Russian Federation, Ekaterinburg

O. I. Zabkov

Federal Research Institute of Viral Infections “Virom”

Email: igorek1981@yandex.ru

Researcher, Laboratory of Transmissible Viral Diseases

Russian Federation, Ekaterinburg

A. A. Mosunov

Federal Research Institute of Viral Infections “Virom”; Chelyabinsk State University

Email: igorek1981@yandex.ru

Student; Intern of the Laboratory of Transmissible Viral Diseases

Russian Federation, Ekaterinburg; Chelyabinsk

M. D. Verkhovskaya

Federal Research Institute of Viral Infections “Virom”; Chelyabinsk State University

Email: igorek1981@yandex.ru

Student; Intern of the Laboratory of Transmissible Viral Diseases

Russian Federation, Ekaterinburg; Chelyabinsk

V. V. Ducardt

Federal Research Institute of Viral Infections “Virom”

Email: igorek1981@yandex.ru

Senior Researcher, Laboratory of Transmissible Viral Diseases

Russian Federation, Ekaterinburg

L. O. Fomina

Federal Research Institute of Viral Infections “Virom”

Email: igorek1981@yandex.ru

Researcher, Laboratory of Transmissible Viral Diseases

Russian Federation, Ekaterinburg

E. G. Kostolomova

Tyumen State Medical University

Email: igorek1981@yandex.ru

PhD (Biology), Associate Professor, Department of Microbiology

Russian Federation, Tyumen

Yu. V. Ostankova

St. Petersburg Pasteur Institute

Email: igorek1981@yandex.ru

PhD (Biology), Head of the Laboratory of immunology and Virology HIV Infection, Senior Researcher of the Laboratory of Molecular Immunology

Russian Federation, St. Petersburg

Igor V. Kudryavtsev

Institute of Experimental Medicine

Author for correspondence.
Email: igorek1981@yandex.ru

PhD (Biology), Head of the Cell Immunology Laboratory, Department of Immunology

Russian Federation, St. Petersburg

A. A. Totolian

St. Petersburg Pasteur Institute

Email: igorek1981@yandex.ru

RAS Full Member, DSc (Medicine), Professor, Head of the Laboratory of Molecular Immunology, Director

Russian Federation, St. Petersburg

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2. Figure 1. Peripheral blood T cell frequencies in COVID-19 convalescents with varying TRECs levels. Note. The obtained data are presented as percent of cells within total lymphocyte subset (%, left), as well as absolute numbers (the number of cells in 1 μL of whole peripheral blood, right). Each dot represents individual subjects, and horizontal bars depict the group medians and quartile ranges [Med (Q25; Q75)]. The statistical analysis was performed with the Mann–Whitney U test. Here and on the Fig. 2 and 3: white circles denote healthy control group (HC, n = 18); black circles — convalescent COVID-19 individuals with normal levels of TRECs (TRECn, n = 109); black squares — convalescent COVID-19 individuals with low levels of TRECs (TREClow, n = 29).

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3. Figure 2. CD4+ T cells frequencies in peripheral blood samples from COVID-19 convalescents with different levels of TRECs. Note. The obtained data are presented as percent of cells within total lymphocyte subset (%, left), as well as absolute numbers (the number of cells in 1 μL of whole peripheral blood, right). Each dot represents individual subjects, and horizontal bars depict the group medians and quartile ranges [Med (Q25; Q75)]. The statistical analysis was performed with the Mann–Whitney U test.

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4. Figure 3. CD8+ T cells frequencies in peripheral blood samples from COVID-19 convalescents with different levels of TRECs. Note. The obtained data are presented as percent of cells within total lymphocyte subset (%, left), as well as absolute numbers (the number of cells in 1 μL of whole peripheral blood, right). Each dot represents individual subjects, and horizontal bars depict the group medians and quartile ranges [Med (Q25; Q75)]. The statistical analysis was performed with the Mann–Whitney U test.

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5. Figure 4. Significant correlations between flow cytometric data based on monoclonal antibodies, manufactured by “Alkor Bio” (Russia) and “Beckman Coulter Inc.” (USA). Note. Correlation analysis was performed using Spearman’s correlation coefficient.

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Copyright (c) 2024 Zurochka A.V., Dobrynina M.А., Safronova E.A., Zurochka V.A., Zuikova A.A., Sarapultsev G.P., Zabkov O.I., Mosunov A.A., Verkhovskaya M.D., Ducardt V.V., Fomina L.O., Kostolomova E.G., Ostankova Y.V., Kudryavtsev I.V., Totolian A.A.

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