Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
BMC Pregnancy and Childbirth
Published in: BMC Pregnancy and Childbirth 1/2016

Open Access 01-12-2016 | Research article

Characterization of B cells in healthy pregnant women from late pregnancy to post-partum: a prospective observational study

Authors: Jorge Lima, Catarina Martins, Maria J. Leandro, Glória Nunes, Maria-José Sousa, Jorge C. Branco, Luís-Miguel Borrego

Published in: BMC Pregnancy and Childbirth | Issue 1/2016

Login to get access

Abstract

Background

B cells play a role in pregnancy due to their humoral and regulatory activities. To our knowledge, different maturational stages (from transitional to memory) of circulating B cell subsets have not yet been characterized (cell quantification and phenotype identification) in healthy pregnant women. Thus, the objective of our study was to characterize these subsets (as well as regulatory B cells) from late pregnancy to post-partum and to compare them with the circulating B cells of non-pregnant women.

Methods

In all of the enrolled women, flow cytometry was used to characterize the circulating B cell subsets according to the expression of IgD and CD38 (Bm1-Bm5 classification system). Regulatory B cells were characterized based on the expression of surface antigens (CD24, CD27, and CD38) and the production of IL-10 after lipopolysaccharide stimulation.

Results

Compared to the absolute counts of B cells in the non-pregnant women (n = 35), those in the pregnant women (n = 43) were significantly lower (p < 0.05) during the 3rd trimester of pregnancy and on delivery day (immediately after delivery). The percentages of these cells on delivery day and at post-partum were significantly lower than those in the non-pregnant women.
In general, the absolute counts and percentages of the majority of the B cell subsets were significantly lower in the 3rd trimester of pregnancy and on delivery day than in the non-pregnant women. However, these counts and percentages did not differ significantly between the post-partum and the non-pregnant women.
The most notable exceptions to the above were the percentages of naïve B cells (which were significantly higher in the 3rd trimester and on delivery day than in the non-pregnant women) and of CD24hiCD38hi regulatory B cells (which were significantly higher in the post-partum than in the non-pregnant women).

Conclusion

According to our study, the peripheral B cell compartment undergoes quantitative changes during normal late pregnancy and post-partum. Such findings may allow us to better understand immunomodulation during human pregnancy and provide evidence that could aid in the development of new strategies to diagnose and treat pregnancy-associated disturbances. Our findings could also be useful for studies of the mechanisms of maternal responses to vaccination and infection.
Appendix
Available only for authorised users
Literature
1.
Nahmias AJ, Schollin J, Abramowsky C. Evolutionary-developmental perspectives on immune system interactions among the pregnant woman, placenta, and fetus, and responses to sexually transmitted infectious agents. Ann N Y Acad Sci. 2011;1230:25–47.CrossRefPubMed
2.
Perricone C, de Carolis C, Perricone R. Pregnancy and autoimmunity: a common problem. Best Pract Res Clin Rheumatol. 2012;26(1):47–60.CrossRefPubMed
3.
Yasumizu T. Influenza complicating pregnancy. Nihon Rinsho. 2006;64(10):1930–3.PubMed
4.
Birkeland SA, Kristoffersen K. Lymphocyte transformation with mitogens and antigens during normal human pregnancy: a longitudinal study. Scand J Immunol. 1980;11(3):321–5.CrossRefPubMed
5.
Muzzio D, Zenclussen AC, Jensen F. The role of B cells in pregnancy: the good and the bad. Am J Reprod Immunol. 2013;69(4):408–12.CrossRefPubMed
6.
Bemark M, Holmqvist J, Abrahamsson J, Mellgren K. Translational mini-review series on B cell subsets in disease. Reconstitution after haematopoietic stem cell transplantation - revelation of B cell developmental pathways and lineage phenotypes. Clin Exp Immunol. 2012;167(1):15–25.CrossRefPubMedPubMedCentral
7.
Marie-Cardine A, Divay F, Dutot I, Green A, Perdrix A, Boyer O, et al. Transitional B cells in humans: characterization and insight from B lymphocyte reconstitution after hematopoietic stem cell transplantation. Clin Immunol. 2008;127(1):14–25.CrossRefPubMed
8.
Bohnhorst JO, Bjorgan MB, Thoen JE, Natvig JB, Thompson KM. Bm1-Bm5 classification of peripheral blood B cells reveals circulating germinal center founder cells in healthy individuals and disturbance in the B cell subpopulations in patients with primary Sjogren’s syndrome. J Immunol. 2001;167(7):3610–8.CrossRefPubMed
9.
10.
Sims GP, Ettinger R, Shirota Y, Yarboro CH, Illei GG, Lipsky PE. Identification and characterization of circulating human transitional B cells. Blood. 2005;105(11):4390–8.CrossRefPubMedPubMedCentral
11.
Guzman Moreno R. B-cell depletion in autoimmune diseases. Advances in autoimmunity. Autoimmun Rev. 2009;8(7):585–90.CrossRefPubMed
12.
Blair PA, Norena LY, Flores-Borja F, Rawlings DJ, Isenberg DA, Ehrenstein MR, et al. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity. 2010;32(1):129–40.CrossRefPubMed
13.
Iwata Y, Matsushita T, Horikawa M, Dilillo DJ, Yanaba K, Venturi GM, et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood. 2011;117(2):530–41.CrossRefPubMedPubMedCentral
14.
Rolle L, Memarzadeh Tehran M, Morell-Garcia A, Raeva Y, Schumacher A, Hartig R, et al. Cutting edge: IL-10-producing regulatory B cells in early human pregnancy. Am J Reprod Immunol. 2013;70(6):448–53.CrossRefPubMed
15.
Ruocco MG, Chaouat G, Florez L, Bensussan A, Klatzmann D. Regulatory T-cells in pregnancy: historical perspective, state of the art, and burning questions. Front Immunol. 2014;5:389.CrossRefPubMedPubMedCentral
16.
Rosser EC, Mauri C. Regulatory B cells: origin, phenotype, and function. Immunity. 2015;42(4):607–12.CrossRefPubMed
17.
Bhat NM, Mithal A, Bieber MM, Herzenberg LA, Teng NN. Human CD5+ B lymphocytes (B-1 cells) decrease in peripheral blood during pregnancy. J Reprod Immunol. 1995;28(1):53–60.CrossRefPubMed
18.
Christiansen JS, Andersen AR, Osther K, Peitersen B, Bach-Mortensen N, Lebech PE. The relationship between pregnancy, HCS and B lymphocytes. Acta Pathol Microbiol Immunol Scand [C]. 1976;84C(4):313–8.
19.
Delgado I, Neubert R, Dudenhausen JW. Changes in white blood cells during parturition in mothers and newborn. Gynecol Obstet Invest. 1994;38(4):227–35.CrossRefPubMed
20.
Iwatani Y, Amino N, Tachi J, Kimura M, Ura I, Mori M, et al. Changes of lymphocyte subsets in normal pregnant and postpartum women: postpartum increase in NK/K (Leu 7) cells. Am J Reprod Immunol Microbiol. 1988;18(2):52–5.CrossRefPubMed
21.
Kraus TA, Engel SM, Sperling RS, Kellerman L, Lo Y, Wallenstein S, et al. Characterizing the pregnancy immune phenotype: results of the viral immunity and pregnancy (VIP) study. J Clin Immunol. 2012;32(2):300–11.CrossRefPubMed
22.
Kuhnert M, Strohmeier R, Stegmuller M, Halberstadt E. Changes in lymphocyte subsets during normal pregnancy. Eur J Obstet Gynecol Reprod Biol. 1998;76(2):147–51.CrossRefPubMed
23.
Mahmoud F, Abul H, Omu A, Al-Rayes S, Haines D, Whaley K. Pregnancy-associated changes in peripheral blood lymphocyte subpopulations in normal Kuwaiti women. Gynecol Obstet Investig. 2001;52(4):232–6.CrossRef
24.
Matthiesen L, Berg G, Ernerudh J, Hakansson L. Lymphocyte subsets and mitogen stimulation of blood lymphocytes in normal pregnancy. Am J Reprod Immunol. 1996;35(2):70–9.CrossRefPubMed
25.
Moore MP, Carter NP, Redman CW. Lymphocyte subsets defined by monoclonal antibodies in human pregnancy. Am J Reprod Immunol. 1983;3(4):161–4.CrossRefPubMed
26.
Valdimarsson H, Mulholland C, Fridriksdottir V, Coleman DV. A longitudinal study of leucocyte blood counts and lymphocyte responses in pregnancy: a marked early increase of monocyte-lymphocyte ratio. Clin Exp Immunol. 1983;53(2):437–43.PubMedPubMedCentral
27.
Watanabe M, Iwatani Y, Kaneda T, Hidaka Y, Mitsuda N, Morimoto Y, et al. Changes in T, B, and NK lymphocyte subsets during and after normal pregnancy. Am J Reprod Immunol. 1997;37(5):368–77.CrossRefPubMed
28.
Auerbach L, Hafner T, Huber JC, Panzer S. Influence of low-dose oral contraception on peripheral blood lymphocyte subsets at particular phases of the hormonal cycle. Fertil Steril. 2002;78(1):83–9.CrossRefPubMed
29.
Shinoda R, Watanabe M, Nakamura Y, Maruoka H, Kimura Y, Iwatani Y. Physiological changes of Fas expression in peripheral lymphocyte subsets during the menstrual cycle. J Reprod Immunol. 2003;60(2):159–68.CrossRefPubMed
30.
Yanaba K, Bouaziz JD, Haas KM, Poe JC, Fujimoto M, Tedder TF. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity. 2008;28(5):639–50.CrossRefPubMed
31.
Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Statist. 2001;29(4):1165–88.CrossRef
32.
Medina KL, Smithson G, Kincade PW. Suppression of B lymphopoiesis during normal pregnancy. J Exp Med. 1993;178(5):1507–15.CrossRefPubMed
33.
Muzzio DO, Soldati R, Ehrhardt J, Utpatel K, Evert M, Zenclussen AC, et al. B cell development undergoes profound modifications and adaptations during pregnancy in mice. Biol Reprod. 2014
34.
Gomez-Lopez N, Tanaka S, Zaeem Z, Metz GA, Olson DM. Maternal circulating leukocytes display early chemotactic responsiveness during late gestation. BMC Pregnancy Childbirth. 2013;13 Suppl 1:S8.CrossRefPubMed
35.
Tessier DR, Raha S, Holloway AC, Yockell-Lelievre J, Tayade C, Gruslin A. Characterization of immune cells and cytokine localization in the rat utero-placental unit mid- to late gestation. J Reprod Immunol. 2015;110:89–101.CrossRefPubMed
36.
Hussein MR, Abd-Elwahed AR, Abodeif ES, Abdulwahed SR. Decidual immune cell infiltrate in hydatidiform mole. Cancer Invest. 2009;27(1):60–6.CrossRefPubMed
37.
Zhang L, Chang K-K, Li M-Q, Li D-J, Yao X-Y. Mouse endometrial stromal cells and progesterone inhibit the activation and regulate the differentiation and antibody secretion of mouse B cells. Int J Clin Exp Pathol. 2014;7(1):123–33.PubMed
38.
Christiaens I, Zaragoza DB, Guilbert L, Robertson SA, Mitchell BF, Olson DM. Inflammatory processes in preterm and term parturition. J Reprod Immunol. 2008;79(1):50–7.CrossRefPubMed
39.
van der Vlugt LE, Mlejnek E, Ozir-Fazalalikhan A, Janssen Bonas M, Dijksman TR, Labuda LA, et al. CD24(hi)CD27(+) B cells from patients with allergic asthma have impaired regulatory activity in response to lipopolysaccharide. Clin Exp Allergy. 2014;44(4):517–28.CrossRefPubMed
40.
Quan C, ZhangBao J, Lu J, Zhao C, Cai T, Wang B, et al. The immune balance between memory and regulatory B cells in NMO and the changes of the balance after methylprednisolone or rituximab therapy. J Neuroimmunol. 2015;282:45–53.CrossRefPubMed
41.
Morbach H, Eichhorn EM, Liese JG, Girschick HJ. Reference values for B cell subpopulations from infancy to adulthood. Clin Exp Immunol. 2010;162(2):271–9.CrossRefPubMedPubMedCentral
Metadata
Title
Characterization of B cells in healthy pregnant women from late pregnancy to post-partum: a prospective observational study
Authors
Jorge Lima
Catarina Martins
Maria J. Leandro
Glória Nunes
Maria-José Sousa
Jorge C. Branco
Luís-Miguel Borrego
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Pregnancy and Childbirth / Issue 1/2016
Electronic ISSN: 1471-2393
DOI
https://doi.org/10.1186/s12884-016-0927-7

Other articles of this Issue 1/2016

BMC Pregnancy and Childbirth 1/2016 Go to the issue

Case report

Vertebral artery dissection in hypertensive disorders of pregnancy: a case series and literature review

Research article

The obstetric care subsidy policy in Burkina Faso: what are the effects after five years of implementation? Findings of a complex evaluation

Research article

Perineal injuries and birth positions among 2992 women with a low risk pregnancy who opted for a homebirth

Research article

Associations between maternal lipid profile and pregnancy complications and perinatal outcomes: a population-based study from China

Research article

Survival of neonates and predictors of their mortality in Tigray region, Northern Ethiopia: prospective cohort study

Research article

Maternal near miss and mortality due to postpartum infection: a cross-sectional analysis from Rwanda