Features of peripheral blood B-cell subset phenotype are associated with clinical outcome of widespread purulent peritonitis

Cover Page

Cite item


The aim of the study was to investigate the phenotypic features of peripheral blood B-lymphocytes in patients with widespread purulent peritonitis (WPP) during postoperative treatment depending on the disease outcome. 52 patients with acute surgical diseases and injuries of the abdominal organs complicated by WPP were examined. Blood sampling was performed before surgery (preoperative period), as well as on day 7, 14 and 21 of the postoperative period. All patients with WPP were divided into two groups depending on the disease outcome during postoperative period: patients with favorable outcome (n = 34), patients with unfavorable outcome (n = 18). 68 healthy subjects were included into control group. Immunophenotyping of blood B-lymphocytes was assessed by flow cytometry and direct immunofluorescence of whole peripheral blood stained with monoclonal antibodies. It was found that patients with WPP in preoperative period contained lowered B1-cell subset compared to control group that was paralleled with low absolute B-lymphocyte count. Moreover, a higher number of activated (based on upregulated CD23 expression) peripheral blood B1-lymphocytes was observed in the patients with unfavorable than in patients with favorable WPP outcome. In addition, dynamics of changes in frequency of B-lymphocytes during postoperative period (day 7—21) varied profoundly depending on the disease outcome. In particular, patients with favorable WPP outcome during postoperative period were found to contain decreased percentage of the most B-cell subsets (including activated cells) examined, whereas patients with unfavorable disease outcome had virtually unaltered B-cell composition in the postoperative period. Moreover, count of total B-cells, naive B-cells and B2-cells negative or positive for CD23 expression was higher in patients with unfavorable outcome than in patients with favorable WPP outcome throughout entire postoperative period. Percentage of some other B-cell subsets in patients with unfavorable than with favorable outcome was also higher only at certain stages of postoperative treatment. It is assumed that such features in peripheral blood B-cell subset composition were closely linked to the disease outcome so that patients with unfavorable WPP outcome turned out to have disturbed B-cell maturation and migration in developing immune response that might be due to lowered total sensitivity of host body to postoperative antibiotic therapy.

About the authors

V. D. Belenjuk

Research Institute of Medical Problems of the North, Federal Research Center KSC SB RAS

Email: dyh.88@mail.ru

Junior Researcher, Laboratory of Molecular-Cell Physiology and Pathology, Research Institute of Medical Problems of the North, Federal Research Center KSC SB RAS.


Russian Federation

A. A. Savchenko

Research Institute of Medical Problems of the North, Federal Research Center KSC SB RAS; Siberian Federal University

Email: aasavchenko@yandex.ru

PhD, MD (Medicine), Professor, Head of the Laboratory of Molecular-Cell Physiology and Pathology, Research Institute of Medical Problems of the North, Federal Research Center KSC SB RAS; Professor of the Medical Biological Department, Siberian Federal University.


Russian Federation

A. G. Borisov

Research Institute of Medical Problems of the North, Federal Research Center KSC SB RAS

Email: 2410454@mail.ru

PhD (Medicine), Leading Researcher, Laboratory of Molecular-Cell Physiology and Pathology, Research Institute of Medical Problems of the North, Federal Research Center KSC SB RAS.


Russian Federation

I. V. Kudryavtsev

Research Institute of Experimental Medicine

Author for correspondence.
Email: igorek1981@yandex.ru

Igor V. Kudryavtsev - PhD (Biology), Senior Researcher, Department of Immunology, Scientific Research Institute of Experimental Medicine.

197376, St. Petersburg, Akademika Pavlova str., 12.

Phone: +7 (812) 234-29-29

Russian Federation


  1. Гасанов М.Дж. Формирование алгоритмов для определения степени тяжести эндотоксикоза при перитонитах // Хирургия. Журнал им. Н.И. Пирогова. 2015. № 1. С. 54—57.
  2. Кудрявцев И.В., Субботовская А.И. Опыт измерения параметров иммунного статуса с использованием шестицветного цитофлуоримерического анализа // Медицинская иммунология. 2015. Т. 17, № 1. С. 19—26.
  3. Савченко А.А., Борисов А.Г., Здзитовецкий Д.Э., Кудрявцев И.В. Состояние клеточного и гуморального иммунитета в зависимости от исхода распространенного гнойного перитонита // Инфекция и иммунитет. 2015. Т. 5, № 1. С. 63—70.
  4. Савченко А.А., Гвоздев И.И., Борисов А.Г., Черданцев Д.В., Первова О.В., Кудрявцев И.В., Мошев А.В. Особенности фагоцитарной активности и состояния респираторного взрыва нейтрофилов крови у больных распространенным гнойным перитонитом в динамике послеоперационного периода // Инфекция и иммунитет. 2017. Т. 7, № 1. С. 51—60.
  5. Савченко А.А., Здзитовецкий А.Г., Борисов А.Г., Лузан Н.А. Хемилюминесцентная и энзиматическая активность нейтрофильных гранулоцитов у больных распространенным гнойным перитонитом в зависимости от исхода заболевания // Вестник Российской академии медицинских наук. 2014. № 4—5. С. 23—28.
  6. Чулкова С.В., Шолохова Е.Н., Грищенко Н.В., Рябчиков Д.А., Гривцова Л.Ю., Базин И.С., Тупицын Н.Н. Ключевая роль популяций В1-лимфоцитов в иммунном ответе у больных раком желудка // Российский биотерапевтический журнал. 2018. Т. 17, № 4. С. 64-70.
  7. Bisht N., Khatri V., Chauhan N., Kalyanasundaram R. Cystatin from filarial parasites suppress the clinical symptoms and pathology of experimentally induced colitis in mice by inducing T-regulatory cells, B1-cells, and alternatively activated macrophages. Biomedicines, 2019, 7 (4): 85. doi: 10.3390/biomedicines7040085
  8. Brook A.C., Jenkins R.H., Clayton A., Kift-Morgan A., Raby A.C., Shephard A.P., Mariotti B., Cuff S.M., Bazzoni F., Bowen T., Fraser D.J., Eberl M. Neutrophil-derived miR-223 as local biomarker of bacterial peritonitis. Sci. Rep., 2019, vol. 9, no. 1: 10136. doi: 10.1038/s41598-019-46585-y
  9. Chen L., Ishigami T., Nakashima-Sasaki R., Kino T., D o i H. , Minegishi S., Umemura S. Commensal microbe-specific activation of B2 cell subsets contributes to atherosclerosis development independently of lipid metabolism. EBioMedicine, 2016, vol. 13, pp. 237-247. doi: 10.1016/j.ebiom.2016.10.030
  10. De Souza Costa M., Teles R.H.G., Dutra Y.M., Neto J.C.R.M., de Brito T.V., de Sousa Nunes Queiroz F.F., do Vale D.B.N., de Souza L.K.M., Silva I.S., Dos Reis Barbosa A.L., Medeiros J.R., Parizotto N.A., de Carvalho Filgueiras M. Photobiomodulation reduces neutrophil migration and oxidative stress in mice with carrageenan-induced peritonitis. Lasers Med. Sci., 2018, vol. 33, no. 9, pp. 1983-1990. doi: 10.1007/s10103-018-2569-7
  11. Ding W., Wang K., Liu B., Fan X., Wang S., Cao J., Wu X., Li J. Open Abdomen improves survival in patients with peritonitis secondary to acute superior mesenteric artery occlusion. J. Clin. Gastroenterol., 2017, vol. 51, no. 9, pp. e77-e82. doi: 10.1097/MCG.0000000000000799
  12. Elfessi Z., Liu E., Dukarevich Y., Caniff K., Marquez K., Shabbir Z. Sepsis induced bacterial peritonitis caused by Granulicatella adiacens. Am. J. Emerg. Med., 2019, vol. 37, no. 12: 2263.e1-2263.e3. doi: 10.1016/j.ajem.2019.158428
  13. Jegouzo S.A.F., Feinberg H., Morrison A.G., Holder A., May A., Huang Z., Jiang L., Lasanajak Y., Smith D.F., Werling D., Drickamer K., Weis W.I., Taylor M.E. CD23 is a glycan-binding receptor in some mammalian species. J. Biol. Chem., vol. 294, no. 41, pp. 14845-14859. doi: 10.1074/jbc.RA119.010572
  14. Maciuliene A., Maleckas A., Krisciukaitis A., Maciulis V., Vencius J., Macas A. predictors of 30-day in-hospital mortality in patients undergoing urgent abdominal surgery due to acute peritonitis complicated with sepsis. Med. Sci. Monit., 2019, vol. 25, pp. 6331-6340. doi: 10.12659/MSM.915435
  15. Mai M., Stengel S., Al-Herwi E., Peter J., Schmidt C., Rubio I., Stallmach A., Bruns T. Genetic variants of TRAF6 modulate peritoneal immunity and the risk of spontaneous bacterial peritonitis in cirrhosis: a combined prospective-retrospective study. Sci. Rep., 2017, vol. 7: 4914. doi: 10.1038/s41598-017-04895-z
  16. Morris G., Puri B.K., Olive L., Carvalho A.F., Berk M., Maes M. Emerging role of innate B1 cells in the pathophysiology of autoimmune and neuroimmune diseases: Association with inflammation, oxidative and nitrosative stress and autoimmune responses. Pharmacol. Res., 2019, vol. 148: 104408. doi: 10.1016/j.phrs.2019.104408
  17. Mustaffa-Kamal F., Liu H., Pedersen N.C., Sparger E.E. Characterization of antiviral T cell responses during primary and secondary challenge of laboratory cats with feline infectious peritonitis virus (FIPV). BMC Vet. Res., 2019, vol. 15: 165. doi: 10.1186/s12917-019-1909-6
  18. Nieto J.C., Sanchez E., Romero C., Roman E., Poca M., Guarner C., Juarez C., Soriano G., Vidal S. Impaired innate immune response of leukocytes from ascitic fluid of patients with spontaneous bacterial peritonitis. J. Leukoc. Biol., 2015, vol. 98, no. 5, pp. 819-825. doi: 10.1189/jlb.3AB0315-106R
  19. Obi Y., Streja E., Mehrotra R., Rivara M.B., Rhee C.M., Soohoo M., Gillen D.L., Lau W.L., Kovesdy C.P., Kalantar-Zadeh K. Impact of obesity on modality longevity, residual kidney function, peritonitis, and survival among incident peritoneal dialysis patients. Am. J. Kidney Dis., 2018, vol. 71, no. 6, pp. 802-813. doi: 10.1053/j.ajkd.2017.09.010
  20. Rauch P.J., Chudnovskiy A., Robbins C.S., Weber G.F., Etzrodt M., Hilgendorf I., Tiglao E., Figueiredo J.L., Iwamoto Y., Theurl I., Gorbatov R., Waring M.T., Chicoine A.T., Mouded M., Pittet M.J., Nahrendorf M., Weissleder R., Swirski F.K. Innate response activator B cells protect against microbial sepsis. Science, vol. 335, no. 6068, pp. 597-601. doi: 10.1126/science.1215173
  21. Sjaastad F.V., Condotta S.A., Kotov J.A., Pape K.A., Dail C., Danahy D.B., Kucaba T.A., Tygrett L.T., Murphy K.A., Cabrera-Perez J., Waldschmidt T.J., Badovinac V.P., Griffith T.S. Polymicrobial sepsis chronic immunoparalysis is defined by diminished ag-specific t cell-dependent b cell responses. Front. Immunol., 2018, vol. 9: 2532. doi: 10.3389/fimmu.2018.02532
  22. Soares R.R., Antinarelli L.M.R., Abramo C., Macedo G.C., Coimbra E.S., Scopel K.K.G. What do we know about the role of regulatory B cells (Breg) during the course of infection of two major parasitic diseases, malaria and leishmaniasis? Pathog. Glob. Health, 2017, vol. 111, no. 3, pp. 107-115. doi: 10.1080/20477724.2017.1308902
  23. Soriano F.G., Barbeiro H.V., Barbeiro D.F. Inflammatory response: role of B1 cells. Shock, 2013, vol. 39, no. 1, pp. 5-9. doi: 10.1097/SHK.0b013e31828fad82
  24. Sutherland D.R., Ortiz F., Quest G., Illingworth A., Benko M., Nayyar R., Marinov I. High-sensitivity 5-, 6-, and 7-color PNH WBC assays for both Canto II and Navios platforms. Cytometry B. Clin. Cytom., 2018, vol. 94, no. 1, pp. 1-15. doi: 10.1002/cyto.b.21626
  25. Tomasdottir V., Thorleifsdottir S., Vikingsson A., Hardardottir I., Freysdottir J. Dietary omega-3 fatty acids enhance the B1 but not the B2 cell immune response in mice with antigen-induced peritonitis. J. Nutr. Biochem., 2014, vol. 25, no. 2, pp. 111-117. doi: 10.1016/j.jnutbio.2013.09.010
  26. Wu E.K., Henkes Z.I., McGowan B., Bell R.D., Velez M.J., Livingstone A.M., Ritchlin C.T., Schwarz E.M., Rahimi H. TNF-induced interstitial lung disease in a murine arthritis model: accumulation of activated monocytes, conventional dendritic cells, and CD21(+)/CD23(—) B cell follicles is prevented with anti-TNF therapy. J. Immunol., 2019, vol. 203, no. 11, pp. 2837-2849. doi: 10.4049/jimmunol.1900473
  27. Yesillik S., Agrawal S., Gollapudi S.V., Gupta S. Phenotypic analysis of CD4+ Treg, CD8+ Treg, and breg cells in adult common variable immunodeficiency patients. Int. Arch. Allergy. Immunol., 2019, vol. 180, no. 2, pp. 150-158. doi: 10.1159/000501457
  28. Yong L., Tang Y., Ren C., Liu M., Shen J., Hou X. B1 cells protect against Schistosoma japonicum-induced liver inflammation and fibrosis by controlling monocyte infiltration. PLoS Negl. Trop. Dis., 2019, 13 (6): e0007474. doi: 10.1371/journal.pntd.0007474
  29. Yu W., Yao D., Yu S., Wang X., Li X., Wang M., Liu S., Feng Z., Chen X., Li W., Wang L., Liu W., Ma J., Yu L., Tong C., Song B., Cui Y. Protective humoral and CD4(+) T cellular immune responses of Staphylococcus aureus vaccine MntC in a murine peritonitis model. Sci. Rep., 2018, 8: 3580. doi: 10.1038/s41598-018-22044-y

Supplementary files

There are no supplementary files to display.

Copyright (c) 2020 Belenjuk V.D., Savchenko A.A., Borisov A.G., Kudryavtsev I.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies