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Influence of Splenomegaly and Splenectomy on the Immune Cell Profile of Patients with Common Variable Immunodeficiency Disease

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Abstract

Purpose

About 25% of patients with common variable immunodeficiency disease (CVID) have splenomegaly, necessitating sometimes splenectomy whom consequences on the immunological profile of CVID patients have never been studied. We analyzed 11 CVID patients’ comprehensive blood immune cell phenotypes pre- and post-splenectomy.

Methods

Flow cytometry analyses of immune cell populations.

Results

Among 89 CVID cohort patients, 41 with splenomegaly, splenomegaly was strongly associated with granulomatous disease, autoimmune disorders, lymphoid hyperplasia, and/or portal hypertension. CVID patients with splenomegaly have significant peripheral lymphopenia (p = 0.001), and significantly fewer peripheral class-switched memory B cells (smBs) (p = 0.001), CD4+ T lymphocytes (p = 0.001), NK (p = 0.0001) and dendritic cells (p ≤ 0.01), and significantly more circulating CD4+ and CD8+ (p = 0.00001) T cell subset activation (p = 0.00005), than CVID patients without splenomegaly. Examination of splenectomy impact on circulating lymphocyte subset distributions demonstrated the drastically enhanced total circulating lymphocyte count post-splenectomy, predominantly B lymphocytes and CD8+ T cells. However, splenectomy did not change B cell distribution, with smBs remaining persistently low, in contrast to complete inversion of the circulating T cell composition, with reversal of the CD4+/CD8+ ratio suggesting that amplification of the CD8+ T cell compartment is a CVID characteristic in patients with splenomegaly. Our results highlight this CD8+ amplification in CVID–splenomegaly patients that might be explained by a homing effect to the spleen and/or possible chronic virus replication, which in turn could induce T cell expansions.

Conclusion

Splenectomizing CVID patients with splenomegaly restores the absolute circulating lymphocyte count, suggesting that the decreased T cell count in the presence of splenomegaly cannot be used as an exclusive criterion for combined immunodeficiency.

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Funding

This study was carried out with the Internal Medicine Department’s own funds.

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Authors and Affiliations

  1. Department of Internal Medicine and Infectious Diseases, University of Bordeaux, Haut-Lévêque Hospital, 5, Avenue Magellan, 33604, Pessac, France

    Jean-François Viallard

  2. Pathology Department, University of Bordeaux, Haut-Lévêque Hospital, 33604, Pessac, France

    Marie Parrens

  3. CNRS, CIRID, UMR 5164, 33076, Bordeaux, France

    Patrick Blanco & Jean-François Moreau

  4. Clinical Immunology Department, Saint-Louis Hospital, Paris–Diderot University, 75475, Paris, France

    Eric Oksenhendler & Claire Fieschi

Authors
  1. Jean-François Viallard
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  2. Marie Parrens
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  3. Patrick Blanco
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  4. Jean-François Moreau
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  5. Eric Oksenhendler
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  6. Claire Fieschi
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Contributions

J.-F. V., E. O. and C. F. enrolled CVID patients in the cohort and collected clinical data. P. B. and J.-F. M. ran the flow cytometry analyses. M. P. conducted the histological analyses and tissue immunohistochemical labeling. J.-F. V. computed the statistical analyses of the data. J.-F. V., J.-F. M., and C. F. wrote the paper. All authors approved the final version for submission.

Corresponding author

Correspondence to Jean-François Viallard.

Ethics declarations

Ethics Approval and Consent to Participate

CVID patients were enrolled in the ALTADIH Cohort which was approved by the Bordeaux University Institutional Review Board on December 20, 2006 (no. 2.04.2007). Each CVID patient gave informed written consent before participating in the study.

Consent for Publication

The patient consent form contains permission to publish data without an identifier.

Conflict of Interest

The authors declare no competing interests.

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Viallard, JF., Parrens, M., Blanco, P. et al. Influence of Splenomegaly and Splenectomy on the Immune Cell Profile of Patients with Common Variable Immunodeficiency Disease. J Clin Immunol 44, 46 (2024). https://doi.org/10.1007/s10875-023-01648-8

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  • DOI: https://doi.org/10.1007/s10875-023-01648-8

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