nature.com

Kidney function after nonmyeloablative hematopoietic cell transplant for sickle cell disease

Abstract

Hematopoietic cell transplantation (HCT) is potentially curative for patients with sickle cell disease (SCD). Both SCD and HCT cause kidney damage. This study analyzed data from 160 patients who received nonmyelablative HCT for SCD. Renal function was assessed at baseline and annually for 3years. The rate of new-onset eGFR <60 ml/min/1.73m2 was low (2.8%). Rapid kidney function decline in the first year post-HCT was noted in 7.5% of patients but was not associated with subsequently worse renal function. The eGFR decreased post-HCT (1 year: –7.19 p < 0.0001, 2 year: –11.32 *p* < 0.0001, 3 year: -12.37 ml/min/1.73m2 p < 0.0001). Mean eGFR remained within normal limits throughout the follow-up period (1 year:119, 2 year:115, 3 year:113 ml/min/1.73m2). Hyperfiltration rates decreased with a corresponding increase in patients with normal eGFR post-HCT. Therefore, the decline in eGFR after HCT may represent preservation of renal function. The prevalence of kidney damage increased transiently but, by 3 years post-HCT, was not significantly changed from baseline. Most cases of kidney damage were due to albuminuria. AKI, noted early post-HCT in 39% of patients, was most commonly stage 1 and was associated with decreased survival (p = 0.03). Larger studies with longer follow-up are required to explore the effects of HCT on renal function in patients with SCD.

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

Access options

Access through your institution

Change institution

Buy or subscribe

Subscribe to this journal

Receive 12 print issues and online access

$259.00 per year

only $21.58 per issue

Learn more

Buy this article

Purchase on SpringerLink

Instant access to full article PDF

Buy now

Prices may be subject to local taxes which are calculated during checkout

Additional access options:

Log in

Learn about institutional subscriptions

Read our FAQs

Contact customer support

Fig. 1: Schematic of patients included in baseline and 1, 2, and 3-year post-HCT analyses.

Fig. 2: Slope of eGFR decline post-transplant.

Fig. 3: Trend of eGFR post-HCT shown by mean values with 95% confidence intervals.

Fig. 4

Fig. 5: The proportion of patients at each time point with kidney damage defined by UACR ≥ 30 mg/dL and/or eGFR <60 mL/min/1.73 m2.

Fig. 6: A lower baseline eGFR is seen in patients who developed AKI and remains lower throughout the follow-up period.

Fig. 7: Kaplan Meier curve demonstrating differences in survival up to 10 years after HCT between patients with and without AKI.

Data availability

The datasets analysed in this study are available from the corresponding author on reasonable request.

References

Ataga KI, Saraf SL, Derebail VK. The nephropathy of sickle cell trait and sickle cell disease. Nat Rev Nephrol. 2022;18:361–77.

PubMedPubMed CentralGoogle Scholar

Saraf SL, Zhang X, Kanias T, Lash JP, Molokie RE, Oza B, et al. Haemoglobinuria is associated with chronic kidney disease and its progression in patients with sickle cell anaemia. Br J Haematol. 2014;164:729–39.

CASPubMedGoogle Scholar

Yeruva SL, Paul Y, Oneal P, Nouraie M. Renal failure in sickle cell disease: prevalence, predictors of disease, mortality and effect on length of hospital stay. Hemoglobin. 2016;40:295–9.

CASPubMedPubMed CentralGoogle Scholar

Olaniran KO, Allegretti AS, Zhao SH, Nigwekar SU, Kalim S. Acute kidney injury among black patients with sickle cell trait and sickle cell disease. Clin J Am Soc Nephrol. 2021;16:348–55.

CASPubMedPubMed CentralGoogle Scholar

Powars D, Chan L, Hiti A, Ramicone E, Johnson C. Outcome of sickle cell anemia: a 4-decade observational study of 1056 patients. Hemoglobin. 2005;84:363–76.

Google Scholar

Sharpe C, Thein S. Sickle cell nephropathy - a practical approach. Br J Haematol. 2011;155:287–97.

CASPubMedGoogle Scholar

Airy M, Eknoyan G. The kidney in sickle hemoglobinopathies. Clin Nephrol. 2017;87:55–68.

PubMedGoogle Scholar

Elmariah H, Garrett M, De Castro L, Jonassaint J, Ataga K, Eckman J, et al. Factors associated with survival in a contemporary adult sickle cell disease cohort. Am J Hematol. 2014;89:530–5.

CASPubMedPubMed CentralGoogle Scholar

Powars D, Elliott-Mills D, Chan L, Niland J, Hiti A, Opas L, et al. Chronic renal failure in sickle cell disease: risk factors, clinical course, and mortality. Ann Intern Med. 1991;115:614–20.

CASPubMedGoogle Scholar

Zahr RS, Ataga KI, Lebensburger JD, Winer JC. Kidney failure outcomes in children and young adults with sickle cell disease in the United States Renal Data System. Pediatr Nephrol. 2024;39:619–23.

PubMedGoogle Scholar

Saddadi F, Hakemi M, Najafi I, Moghadam K, Ghavamzadeh A, Jahani M, et al. Chronic kidney disease after hematopoietic cell transplantation: frequency, risk factors, and outcomes. Transpl Proc. 2009;41:2895–7.

CASGoogle Scholar

Ellis MJ, Parikh CR, Inrig JK, Kanbay M, Patel UD. Chronic kidney disease after hematopoietic cell transplantation: a systematic review. Am J Transpl. 2008;8:2378–90.

CASGoogle Scholar

Touzot M, Elie C, van Massenhove J, Maillard N, Buzyn A, Fakhouri F. Long-term renal function after allogenic haematopoietic stem cell transplantation in adult patients: a single-centre study. Nephrol Dialysis Transpl. 2010;25:624–7.

Google Scholar

Naesens M, Kuypers DR, Sarwal M. Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol. 2009;4:481–508.

CASPubMedGoogle Scholar

Hingorani S, Pao E, Stevenson P, Schoch G, Laskin BL, Gooley T, et al. Changes in glomerular filtration rate and impact on long-term survival among adults after hematopoietic cell transplantation: a prospective cohort study. Clin J Am Soc Nephrol. 2018;13:866–73.

PubMedPubMed CentralGoogle Scholar

Hingorani SR, Seidel K, Lindner A, Aneja T, Schoch G, McDonald G. Albuminuria in hematopoietic cell transplantation patients: prevalence, clinical associations, and impact on survival. Biol Blood Marrow Transpl. 2008;14:1365–72.

Google Scholar

Kersting S, Verdonck L. Successful outcome after nonmyeloablative allogeneic hematopoietic stem cell transplantation in patients with renal dysfunction. Biol Blood Marrow Transpl. 2008;14:1312–6.

Google Scholar

Zager RA, O’Quigley J, Zager BK, Alpers CE, Shulman HM, Gamelin LM, et al. Acute renal failure following bone marrow transplantation: a retrospective study of 272 patients. Am J Kidney Dis. 1989;13:210–6.

CASPubMedGoogle Scholar

Kanduri SR, Cheungpasitporn W, Thongprayoon C, Bathini T, Kovvuru K, Garla V, et al. Incidence and mortality of acute kidney injury in patients undergoing hematopoietic stem cell transplantation: a systematic review and meta-analysis. QJM. 2020;113:621–32.

CASPubMedPubMed CentralGoogle Scholar

Pedersen SJV, Monagel DA, Mammen C, Lewis VA, Guilcher GMT, Bruce AA. Stable renal function in children and adolescents with sickle cell disease after nonmyeloablative hematopoietic stem cell transplantation. Pediatr Blood Cancer. 2020;67:e28568.

CASPubMedGoogle Scholar

Krishnamurti L, Kharbanda S, Biernacki MA, Zhang W, Baker KS, Wagner JE, et al. Stable long-term donor engraftment following reduced-intensity hematopoietic cell transplantation for sickle cell disease. Biol Blood Marrow Transpl. 2008;14:1270–8.

Google Scholar

Matthes-Martin S, Lawitschka A, Fritsch G, Lion T, Grimm B, Breuer S, et al. Stem cell transplantation after reduced-intensity conditioning for sickle cell disease. Eur J Haematol. 2013;90:308–12.

PubMedGoogle Scholar

Dallas MH, Triplett B, Shook DR, Hartford C, Srinivasan A, Laver J, et al. Long-term outcome and evaluation of organ function in pediatric patients undergoing haploidentical and matched related hematopoietic cell transplantation for sickle cell disease. Biol Blood Marrow Transpl. 2013;19:820–30.

Google Scholar

Delgado C, Baweja M, Crews DC, Eneanya ND, Gadegbeku CA, Inker LA, et al. A unifying approach for GFR estimation: recommendations of the NKF-ASN task force on reassessing the inclusion of race in diagnosing kidney disease. Am J Kidney Dis. 2022;79:268–88.e1.

PubMedGoogle Scholar

Selistre L, Rabilloud M, Cochat P, de Souza V, Iwaz J, Lemoine S, et al. Comparison of the Schwartz and CKD-EPI equations for estimating glomerular filtration rate in children, adolescents, and adults: a retrospective cross-sectional study. PLoS Med. 2016;13:e1001979.

PubMedPubMed CentralGoogle Scholar

Levey AS, Inker LA, Matsushita K, Greene T, Willis K, Lewis E, et al. GFR decline as an end point for clinical trials in CKD: a scientific workshop sponsored by the National Kidney Foundation and the US Food and Drug Administration. Am J Kidney Dis. 2014;64:821–35.

PubMedGoogle Scholar

Stevens PE, Levin A. Evaluation and management of chronic kidney disease: synopsis of the kidney disease: improving global outcomes 2012 clinical practice guideline. Ann Intern Med. 2012;158:825–30.

Google Scholar

Ephraim R. Chronic kidney disease is common in sickle cell disease: a cross-sectional study in the Tema Metropolis, Ghana. BMC Nephrol. 2015;16:75.

PubMedPubMed CentralGoogle Scholar

KDIGO Clinical Practice Guideline for Acute Kidney Injury. Kidney International Supplements [Internet]. 2012; 2. Available from: https://kdigo.org/guidelines/acute-kidney-injury/.

Derebail V, Ciccone E, Zhou Q, Kilgore R, Cai J, Ataga K. Progressive Decline in Estimated GFR in Patients with Sickle Cell Disease: An Observational Cohort Study. Am J Kidney Dis. 2019;74:47–55.

PubMedPubMed CentralGoogle Scholar

Dovern E, Aydin M, DeBaun MR, Alizade K, Biemond BJ, Nur E. Effect of allogeneic hematopoietic stem cell transplantation on sickle cell disease-related organ complications: a systematic review and meta-analysis. Am J Hematol. 2024;99:1129–41.

CASPubMedGoogle Scholar

Lebensburger JD, Derebail VK. Sickle cell disease and the kidney. Filters Gone Awry Hematol Oncol Clin North Am 2022;36:1239–54.

PubMedGoogle Scholar

Hoste E, Clermont G, Kersten A, Venkataraman R, Angus D, De Bacquer D, et al. RIFLE criteria for acute kidney injury are associated with hospital mortality in critically Ill patients: a cohort analysis. Crit Care. 2006;10:R73.

PubMedPubMed CentralGoogle Scholar

Uchino S, Bellomo R, Goldsmith D, Bates S, Ronco C. An assessment of the RIFLE criteria for acute renal failure in hospitalized patients. Crit Care Med. 2006;34:1913–7.

PubMedGoogle Scholar

Renaghan AD, Jaimes EA, Malyszko J, Perazella MA, Sprangers B, Rosner MH. Acute kidney injury and CKD associated with hematopoietic stem cell transplantation. Clin J Am Soc Nephrol. 2020;15:289–97.

CASPubMedGoogle Scholar

Fitzhugh CD, Volanakis EJ, Idassi O, Duberman JA, DeBaun MR, Friedman DL. Long-term health effects of curative therapies on heart, lungs, and kidneys for individuals with sickle cell disease compared to those with hematologic malignancies. J Clin Med. 2022;11:3118.

CASPubMedPubMed CentralGoogle Scholar

Asnani M, Reid M. Cystatin C: a useful marker of glomerulopathy in sickle cell disease? Blood Cells Mol Dis. 2015;54:65–70.

CASPubMedGoogle Scholar

Yee M, Lane P, Archer D, Joiner C, Eckman J, Guasch A. Estimation of glomeruloar filtration rate using serum cystatin C and creatinine in adults with sickle cell anemia. Am J Hematol. 2017;92:E598–E9.

CASPubMedGoogle Scholar

Alvarez O, Zilleruelo G, Wright D, Montane B, Lopez-Mitnik G. Serum cystatin C levels in children with sickle cell disease. Pediatr Nephrol. 2006;21:533–7.

PubMedGoogle Scholar

Barreto M, Limerick E, Jeffries N, Varga J, Gharib A, Clark M, et al. Creatinine-based estimating equations for GFR outperform cystatin C-based equations in adults with sickle cell disease. Foundation for Sickle Cell Research; Fort Lauderdale, FL (2023).

Download references

Acknowledgements

Drs. Delbert Wigfall and Annabelle Chua of Duke Medical Center for contributing pediatric nephrology expertise.

Funding

This research was funded by the Cooperative Assessment of Late Effects for SCD Curative Therapies (COALESCE, 1U01HL156620-01, National Heart, Lung, and Blood Institute (NHLBI)) and was supported by the intramural research program of the NHLBI, National Institutes of Health.

Author information

Author notes

These authors contributed equally: Santosh L. Saraf, Courtney D. Fitzhugh.

Authors and Affiliations

National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD, USA

Emily Limerick, Matthew M. Hsieh, Mauricio Barretto, Neal Jeffries, Ritika Menon & Courtney D. Fitzhugh

Department of Medicine, Department of Nephrology, Wake Forest University School of Medicine, Winston-Salem, NC, USA

Clarissa Diamantidis

Division of Biostatistics, Duke University School of Medicine, Durham, NC, USA

Yuliya Lokhnygina

Division of Hematology & Oncology, Department of Medicine, Comprehensive Sickle Cell Center, University of Illinois at Chicago, Chicago, IL, USA

Santosh L. Saraf

Authors

Emily Limerick

View author publications

You can also search for this author inPubMedGoogle Scholar

2. Matthew M. Hsieh

View author publications

You can also search for this author inPubMedGoogle Scholar

3. Mauricio Barretto

View author publications

You can also search for this author inPubMedGoogle Scholar

4. Neal Jeffries

View author publications

You can also search for this author inPubMedGoogle Scholar

5. Clarissa Diamantidis

View author publications

You can also search for this author inPubMedGoogle Scholar

6. Yuliya Lokhnygina

View author publications

You can also search for this author inPubMedGoogle Scholar

7. Ritika Menon

View author publications

You can also search for this author inPubMedGoogle Scholar

8. Santosh L. Saraf

View author publications

You can also search for this author inPubMedGoogle Scholar

9. Courtney D. Fitzhugh

View author publications

You can also search for this author inPubMedGoogle Scholar

Contributions

EL, CD, YL, SS, and CF conceived and designed the analyses; EL, MH, and SS collected data; MB and RM contributed data; EL and NJ performed the analyses, EL and CF drafted the manuscript. All authors reviewed and approved the final manuscript.

Corresponding authors

Correspondence to Santosh L. Saraf or Courtney D. Fitzhugh.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics approval and consent to participate

All methods were performed in accordance with the relevant guidelines and regulations. Approval has been obtained from the National Institutes of Health and University of Illinois Chicago institutional review boards. Informed consent was obtained from all participants.

Additional information

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

Supplementary information

Supplemental Materials

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Limerick, E., Hsieh, M.M., Barretto, M. et al. Kidney function after nonmyeloablative hematopoietic cell transplant for sickle cell disease. Bone Marrow Transplant (2025). https://doi.org/10.1038/s41409-025-02550-0

Download citation

Received:21 July 2024

Revised:17 January 2025

Accepted:11 March 2025

Published:22 March 2025

DOI:https://doi.org/10.1038/s41409-025-02550-0

Share this article

Anyone you share the following link with will be able to read this content:

Get shareable link

Sorry, a shareable link is not currently available for this article.

Copy to clipboard

Provided by the Springer Nature SharedIt content-sharing initiative

Read full news in source page