Skip to main content

Association of Bowman’s capsule rupture with prognosis in patients with lupus nephritis

Abstract

Background and objective

Lupus nephritis is one of the most severe manifestations of systemic lupus erythematosus. The clinical and prognostic significance of Bowman’s capsule rupture in patients with lupus nephritis is unknown.

Methods

One hundred eighty patients with lupus nephritis were enrolled in the study and the integrity of Bowman’s capsule was assessed. Both inflammatory and proliferative cells were detected by immunochemistry staining. The primary events of interest were end-stage renal disease and death.

Results

After retrospective analysis of the data, 52 (28.9%) patients were found to have Bowman’s capsule rupture, which was accompanied by high levels of serum creatinine, 24 h urine protein, and Activity/Chronicity Index. Bowman’s capsule rupture was correlated with the level of crescents, tubular atrophy, and interstitial fibrosis. The number of CD20+ cells was higher in the Bowman’s capsule rupture ( +) group compared with the Bowman’s capsule rupture (−) group, while no differences in other inflammatory cells were observed. In addition, the end stage renal disease-free survival in the Bowman’s capsule rupture ( +) group was lower than in the Bowman’s capsule rupture (−) group. Moreover, serum creatinine (HR 39.56, P < 0.001), Activity Index (HR 1.50, P < 0.05) as well as Bowman’s capsule rupture (HR 1.09, P < 0.05) predicted end-stage renal disease progression. Notably, for patients with existing crescents, Bowman’s capsule rupture increased the cumulative risk of end-stage renal disease.

Conclusions

Bowman’s capsule rupture is an important renal pathological lesion, which correlates with severe clinical manifestations, pathological changes, and poor prognosis in patients with lupus nephritis.

Graphical abstract

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Anders HJ, Saxena R, Zhao MH, Parodis I, Salmon JE, Mohan C (2020) Lupus nephritis. Nat Rev Dis Primers 6(1):7. https://doi.org/10.1038/s41572-019-0141-9

    Article  PubMed  Google Scholar 

  2. Parikh SV, Almaani S, Brodsky S, Rovin BH (2020) Update on lupus nephritis: core curriculum 2020. Am J Kidney Dis 76(2):265–281. https://doi.org/10.1053/j.ajkd.2019.10.017

    Article  PubMed  Google Scholar 

  3. Bajema IM, Wilhelmus S, Alpers CE et al (2018) Revision of the International Society of Nephrology/Renal Pathology Society classification for lupus nephritis: clarification of definitions, and modified National Institutes of Health activity and chronicity indices. Kidney Int 93(4):789–796. https://doi.org/10.1016/j.kint.2017.11.023

    Article  PubMed  Google Scholar 

  4. Yu F, Haas M, Glassock R, Zhao MH (2017) Redefining lupus nephritis: clinical implications of pathophysiologic subtypes. Nat Rev Nephrol 13(8):483–495. https://doi.org/10.1038/nrneph.2017.85

    Article  PubMed  Google Scholar 

  5. Morel-Maroger Striker L, Killen PD, Chi E, Striker GE (1984) The composition of glomerulosclerosis. I. Studies in focal sclerosis, crescentic glomerulonephritis, and membranoproliferative glomerulonephritis. Lab Invest 51(2):181–192

    CAS  PubMed  Google Scholar 

  6. Al-Hussain T, Asiri S, Amer S, Al Mana H, Akhtar M (2017) Patterns of glomerulonephritis with crescents: experience at a tertiary medical center in Saudi Arabia. Saudi J Kidney Dis Transpl 28(3):532–537. https://doi.org/10.4103/1319-2442.206448

    Article  PubMed  Google Scholar 

  7. Chen A, Lee K, Guan T, He JC, Schlondorff D (2020) Role of CD8+ T cells in crescentic glomerulonephritis. Nephrol Dial Transplant 35(4):564–572. https://doi.org/10.1093/ndt/gfz043

    CAS  Article  PubMed  Google Scholar 

  8. Hakroush S, Tampe B (2021) Correspondence on “Bowman’s capsule rupture on renal biopsy improves the outcome prediction of ANCA-associated glomerulonephritis classifications.” Ann Rheum Dis. https://doi.org/10.1136/annrheumdis-2021-219970

    Article  PubMed  Google Scholar 

  9. L’Imperio V, Vischini G, Ferraro M, Pagni F (2021) Response to: “Correspondence on ‘Bowman’s capsule rupture on renal biopsy improves the outcome prediction of ANCA-associated glomerulonephritis classifications’” by Hakroush and Tampe. Ann Rheum Dis. https://doi.org/10.1136/annrheumdis-2021-219988

    Article  PubMed  Google Scholar 

  10. L’Imperio V, Vischini G, Pagni F, Ferraro PM (2020) Bowman’s capsule rupture on renal biopsy improves the outcome prediction of ANCA-associated glomerulonephritis classifications. Ann Rheum Dis. https://doi.org/10.1136/annrheumdis-2020-217979

    Article  PubMed  Google Scholar 

  11. Sethi S, Haas M, Markowitz GS et al (2016) Mayo clinic/renal pathology society consensus report on pathologic classification, diagnosis, and reporting of GN. J Am Soc Nephrol 27(5):1278–1287. https://doi.org/10.1681/ASN.2015060612

    Article  PubMed  Google Scholar 

  12. Broder A, Mowrey WB, Khan HN et al (2018) Tubulointerstitial damage predicts end stage renal disease in lupus nephritis with preserved to moderately impaired renal function: a retrospective cohort study. Semin Arthritis Rheum 47(4):545–551. https://doi.org/10.1016/j.semarthrit.2017.07.007

    Article  PubMed  Google Scholar 

  13. Couzi L, Merville P, Deminiere C et al (2007) Predominance of CD8+ T lymphocytes among periglomerular infiltrating cells and link to the prognosis of class III and class IV lupus nephritis. Arthritis Rheum 56(7):2362–2370. https://doi.org/10.1002/art.22654

    CAS  Article  PubMed  Google Scholar 

  14. Geetha D, Jefferson JA (2020) ANCA-associated vasculitis: core curriculum 2020. Am J Kidney Dis 75(1):124–137. https://doi.org/10.1053/j.ajkd.2019.04.031

    CAS  Article  PubMed  Google Scholar 

  15. Obrisca B, Jurubita R, Andronesi A et al (2018) Histological predictors of renal outcome in lupus nephritis: the importance of tubulointerstitial lesions and scoring of glomerular lesions. Lupus 27(9):1455–1463. https://doi.org/10.1177/0961203318776109

    Article  PubMed  Google Scholar 

  16. Boucher A, Droz D, Adafer E, Noel LH (1987) Relationship between the integrity of Bowman’s capsule and the composition of cellular crescents in human crescentic glomerulonephritis. Lab Invest 56(5):526–533

    CAS  PubMed  Google Scholar 

  17. Goumenos D, Tsomi K, Iatrou C et al (1998) Myofibroblasts and the progression of crescentic glomerulonephritis. Nephrol Dial Transplant 13(7):1652–1661. https://doi.org/10.1093/ndt/13.7.1652

    CAS  Article  PubMed  Google Scholar 

  18. Lin W, Shen C, Zhong Y et al (2021) Glomerular immune deposition in MPO-ANCA associated glomerulonephritis is associated with poor renal survival. Front Immunol. https://doi.org/10.3389/fimmu.2021.625672

    Article  PubMed  PubMed Central  Google Scholar 

  19. Hakroush S, Tampe D, Korsten P, Ströbel P, Tampe B (2021) Bowman’s capsule rupture links glomerular damage to tubulointerstitial inflammation in ANCA-associated glomerulonephritis. Clin Exp Rheumatol 39(Suppl 129):27–31

    Article  Google Scholar 

  20. Rijnink EC, Teng YKO, Wilhelmus S et al (2017) Clinical and histopathologic characteristics associated with renal outcomes in lupus nephritis. Clin J Am Soc Nephrol 12(5):734–743. https://doi.org/10.2215/cjn.10601016

    Article  PubMed  PubMed Central  Google Scholar 

  21. Moroni G, Vercelloni PG, Quaglini S et al (2018) Changing patterns in clinical-histological presentation and renal outcome over the last five decades in a cohort of 499 patients with lupus nephritis. Ann Rheum Dis 77(9):1318–1325. https://doi.org/10.1136/annrheumdis-2017-212732

    CAS  Article  PubMed  Google Scholar 

  22. Faurschou M, Dreyer L, Kamper AL, Starklint H, Jacobsen S (2010) Long-term mortality and renal outcome in a cohort of 100 patients with lupus nephritis. Arthritis Care Res (Hoboken) 62(6):873–880. https://doi.org/10.1002/acr.20116

    Article  Google Scholar 

  23. Munguia-Realpozo P, Mendoza-Pinto C, Sierra Benito C et al (2019) Systemic lupus erythematosus and hypertension. Autoimmun Rev 18(10):102371. https://doi.org/10.1016/j.autrev.2019.102371

    Article  PubMed  Google Scholar 

  24. Lan HY, Nikolic-Paterson DJ, Atkins RC (1992) Involvement of activated periglomerular leukocytes in the rupture of Bowman’s capsule and glomerular crescent progression in experimental glomerulonephritis. Lab Invest 67(6):743–751

    CAS  PubMed  Google Scholar 

  25. Moroni G, Ponticelli C (2014) Rapidly progressive crescentic glomerulonephritis: early treatment is a must. Autoimmun Rev 13(7):723–729. https://doi.org/10.1016/j.autrev.2014.02.007

    Article  PubMed  Google Scholar 

  26. Hu SY, Jia XY, Li JN et al (2016) T cell infiltration is associated with kidney injury in patients with anti-glomerular basement membrane disease. Sci China Life Sci 59(12):1282–1289. https://doi.org/10.1007/s11427-016-5030-9

    CAS  Article  PubMed  Google Scholar 

  27. Chen A, Lee K, D’Agati VD et al (2018) Bowman’s capsule provides a protective niche for podocytes from cytotoxic CD8+ T cells. J Clin Invest 128(8):3413–3424. https://doi.org/10.1172/JCI97879

    Article  PubMed  PubMed Central  Google Scholar 

  28. Tsokos GC, Lo MS, Costa Reis P, Sullivan KE (2016) New insights into the immunopathogenesis of systemic lupus erythematosus. Nat Rev Rheumatol 12(12):716–730. https://doi.org/10.1038/nrrheum.2016.186

    CAS  Article  PubMed  Google Scholar 

  29. Murphy G, Isenberg DA (2019) New therapies for systemic lupus erythematosus—past imperfect, future tense. Nat Rev Rheumatol 15(7):403–412. https://doi.org/10.1038/s41584-019-0235-5

    Article  PubMed  Google Scholar 

  30. Fanouriakis A, Kostopoulou M, Cheema K et al (2020) 2019 Update of the Joint European League Against Rheumatism and European Renal Association-European Dialysis and Transplant Association (EULAR/ERA-EDTA) recommendations for the management of lupus nephritis. Ann Rheum Dis 79(6):713–723. https://doi.org/10.1136/annrheumdis-2020-216924

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are thankful to the physicians and nurses of the Second Xiangya Hospital, Central South University and patients who made it possible to conduct this study.

Funding

This work was supported by the Key Program of General Program of the National Natural Science Foundation of China (NSFC) (81730018).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. TD is the first author. LS obtained funding. TD, QZ, AC, CT, XZ, LS designed the study. LX, LH, HL, SD, SY, FY, JZ, XZ, MC, YiL, YuL and FL collected the data. TD, QZ, XZ cleaned and analyzed the data. TD drafted the manuscript. AC, SY and FL contributed to critical revision of the manuscript for important intellectual content and approved the final version of the manuscript. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Lin Sun.

Ethics declarations

Conflict of interest

All the authors declared no competing interests.

Ethical approval

The study complied with the Helsinki Declaration and was approved by the ethical review committee of The Second Xiangya Hospital, Central South University (Ethics approval number: 2021–072).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 337 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Duan, T., Zhu, X., Zhao, Q. et al. Association of Bowman’s capsule rupture with prognosis in patients with lupus nephritis. J Nephrol 35, 1193–1204 (2022). https://doi.org/10.1007/s40620-022-01316-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40620-022-01316-x

Keywords

  • Bowman’s capsule rupture
  • Lupus nephritis
  • Histopathology
  • CD20
  • Prognosis