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NDT Advance Access originally published online on January 25, 2007
Nephrology Dialysis Transplantation 2007 22(5):1369-1376; doi:10.1093/ndt/gfl795
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© The Author [2007]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Post-allogeneic haematopoietic stem cell transplantation membranous nephropathy: clinical presentation, outcome and pathogenic aspects

Benjamin Terrier1, Yahsou Delmas2, Aurélie Hummel1, Claire Presne3, Francois Glowacki4, Bertrand Knebelmann1, Christian Combe2, Philippe Lesavre1, Natacha Maillard5, Laure-Hélène Noël6, Natahlie Patey-Mariaud de Serre6, Sylvie Nusbaum7, Isabelle Radford7, Agnès Buzyn5 and Fadi Fakhouri1

1Service de Néphrologie Adultes, Hôpital Necker-Enfants Malades, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, 2Département de Néphrologie, CHU Pellegrin, Bordeaux, 3Service de Néphrologie, CHU, Amiens, 4Service de Néphrologie, CHR Albert Calmette, Lille, 5Service d’Hématologie Adultes, Hôpital Necker-Enfants Malades, AP-HP, Paris, 6Service d’Anatomie Pathologique, Hôpital Necker-Enfants Malades, AP-HP, Paris and 7Service de Cytogénétique, Hôpital Necker-Enfants Malades, AP-HP, Paris, France

Correspondence and offprint requests to: Dr Fadi Fakhouri, Service de Néphrologie Adultes, Hôpital Necker-Enfants Malades, AP-HP, 149-161 rue de Sèvres, 75015 Paris, France. Email: fakhouri{at}necker.fr



   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 Acknowledgements
 References
 
Background. Post-allogeneic haematopoietic stem cell transplantation (HSCT) membranous nephropathy (MN), a rare complication of HSCT, remains an ill-defined entity. We describe the clinical and biological characteristics and outcome of five patients with post-HSCT MN, review the previously reported cases and discuss the pathogenic aspects of this nephropathy.

Methods. Cases were identified by using a questionnaire sent to nephrologists and pathologists in French university and general hospitals. Medical records and kidney biopsy specimens were reviewed and relevant data were collected. Moreover, the IgG subclasses in glomerular deposits and the presence of chimeric renal cells were studied.

Results. Five patients were identified. All had a history of chronic graft-vs-host disease (cGVHD) and all had active manifestations of cGVHD at MN diagnosis. Mean time between HSCT and diagnosis of MN was 24.4 months. Renal insufficiency was present in four patients. Renal biopsy examination showed typical features of MN in all patients. IgG1 and IgG4 were the predominant IgG subclasses in the glomerular deposits. No chimeric glomerular cell was detected. Initial treatment for MN consisted in corticosteroids and immunosuppressors (ciclosporin, mycophenolate mofetil, rituximab, chlorambucil) in all patients. Complete remission of nephrotic syndrome (NS) occurred in two patients, partial remission in one patient, while treatment was inefficacious in one (data not available for one patient). Most interestingly, the evolution of NS paralleled the evolution of cGVHD in all patients.

Conclusion. Our data suggest an association between cGVHD and post-HSCT MN. Treatment, mainly steroids and ciclosporin, should be aimed at the control of acute manifestations of cGVHD.

Keywords: membranous nephropathy; haematopoietic stem cell transplantation; graft-vs-host disease; ciclosporin



   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 Acknowledgements
 References
 
Allogeneic haematopoietic stem cell transplantation (HSCT) is an effective treatment of haematological disorders; it is however burdened by high morbidity and mortality rates, mainly related to graft-vs-host disease (GVHD) and infections. Renal complications of HSCT include drug toxicity (high dose chemotherapy, ciclosporin, antimicrobial agents) and total body irradiation toxicity (radiation nephritis), infections, thrombotic microangiopathy and nephrotic syndrome.

Nephrotic syndrome (NS) following HSCT is a rare complication, since only few cases are reported to date in the English literature. NS is mainly related to membranous nephropathy [1–18] and less frequently to minimal change disease, focal segmental glomerulonephritis, diffuse proliferative glomerulonephritis or IgA nephropathy.

Membranous nephropathy (MN) is the most common cause of adult-onset NS. The majority of cases of MN are idiopathic; however, up to one-third of the cases are related to systemic immunological disorders, solid tumours and haemopathies, infections, medications and more rarely HSCT. However, characteristics of patients with MN following HSCT, their outcome and the response of the NS to therapy, as well as pathogenic aspects of this nephropathy, remain largely ill defined.

Herein, we describe the clinical and biological characteristics and outcome of five adult patients with MN following allogeneic HSCT, review the previously reported cases and discuss the pathogenic mechanisms, especially the relationship between MN and chronic GVHD (cGVHD).



   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 Acknowledgements
 References
 
Patients selection
Patients with post-HSCT MN were identified through an inquiry in nephrology and haematology departments in 20 university and general hospitals in France. Inclusion criteria included the following: (i) patients aged 18 years who had undergone HSCT; (ii) MN documented by a renal biopsy and (iii) exclusion of common causes of secondary MN.

Patients’ medical records and kidney biopsy specimens were reviewed. NS was defined by proteinuria ≥3 g/day and serum albumin ≤3 g/dl. Renal insufficiency was defined as an estimated (Cockcroft–Gault formula) creatinine clearance ≤60 ml/min. Complete remission (CR) of NS was defined as a proteinuria ≤0.5 g/day with normal serum albumin (≥3.5 g/dl) and stable renal function. Partial remission (PR) was defined by a decrease in proteinuria <2.5 g/day or ≥50% decrease compared with baseline and serum albumin ≥3 g/dl with stable renal function.

Kidney biopsy analysis by light microscopy and immunofluorescence study of the IgG subclass in glomerular deposits
Kidney biopsy specimens were prepared for light microscopy and immunofluorescence (IF) microscopy using standard techniques. By light microscopy, the stage of MN and the tubulointerstitial lesions were evaluated using Masson's trichrome, Jone's and periodic acid-Schiff (PAS) staining. By IF study, the fluorescent-conjugated anti-human IgG, IgA, IgM, C1q, C3, fibrinogen and albumin antibodies were studied. Moreover, the IgG subclasses were evaluated by indirect IF with monoclonal antibodies directed to IgG1, IgG2, IgG3 and IgG4 in five patients (Division of Immunity and Infection, The Medical School East Wing, University of Birmingham, anti-IgG). All biopsies were reviewed by the same expert pathologist (L.-H.N.).

Fluorescent in situ hybridization (FISH) analysis of Y-chromosome in glomerular cells
Paraformaldehyde-fixed, paraffin-embedded kidney sections from two female patients in whom allogeneic HSCT had been performed with a male donor were labelled with a Y-chromosome paint probe. Paraffin-embedded sections were deparaffinized, hydrated to ethanol, serially dehydrated and reacted with Y-chromosome and X-chromosome paint probes. The Y-chromosome probe was detected with fluorescein isothiocyanate (FITC) (Play113.5), and the X-chromosome probe with rhodamin (PDMX1).



   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 Acknowledgements
 References
 
Clinical and biological characteristics of the patients (Tables 1 and 2)
Five patients were identified (three women and two men). The clinical characteristics of the patients at the time of MN diagnosis are summarized in Table 1. All patients had normal pre-transplant renal function, without proteinuria. All underwent allogeneic HSCT, with a sibling donor in three cases. Patients underwent non-myeloablative HSCT except patient 2. All had a prophylactic treatment of GVHD with ciclosporin (CSA) (Neoral®) associated with methotrexate (n = 4) or mycophenolate mofetil (MMF) (n = 1). Despite prophylaxis, four patients had acute GVHD (aGVHD) and all developed cGVHD. Initial treatment of cGVHD consisted in corticosteroids (CS) in all patients, associated with CSA (n = 3), azathioprine (AZA) (n = 2), tacrolimus (n = 1) and MMF (n = 1). Mean time between HSCT and diagnosis of MN was 24.4 months (range: 14–37 months). At the time of MN diagnosis, all patients had active manifestations of cGVHD, mainly mucosal and skin involvement, and none was currently taking CSA. NS was present in all cases [mean proteinuria 10.4 g/day (range: 7.9–16.2) and mean albuminaemia 1.6 g/dl (range: 0.7–2.2)]. Biological data at diagnosis are summarized in Table 2.


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  		Table 1. Characteristics of patients with post-allogeneic haematopoietic stem cell transplantation membranous nephropathy

 

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  		Table 2. Treatment and outcome of patients with membranous nephropathy after haematopoietic stem cell transplantation

 
Kidney biopsy data (Table 3)
Kidney biopsy features are summarized in Table 3. All cases disclosed features of MN by light microscopy and IF study. No cellular proliferation was noted. The intensity of tubulointerstitial lesions as well as vascular lesions (arteriolar hyaline thickening) was variable (Figure 1A).


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  		Table 3. Renal biopsy examination by light microscopy, standard immunofluorescence microscopy and immunofluorescence analysis of the IgG subclass deposits

 

Figure 1
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  		Fig. 1. Patient 1. Kidney biopsy. (A) Light microscopy, PAS staining: normal aspects of glomeruli. Presence of atrophic tubules (*). (B) Immunofluorescence study using a specific anti-IgG1 antibody. Presence of marked granular sub-epithelial deposits.

 
Analysis of the IgG subclasses deposited in the glomeruli showed that IgG1 was the predominant glomerular IgG subclass (Figure 1B), present in all analysed patients, associated with IgG4 deposits and less frequently IgG3.

Membranous nephropathy treatment (Table 2)
MN treatments are summarized in Table 2. At diagnosis of MN, four patients were still treated for cGVHD, using AZA (n = 2), CS (n = 2) and MMF (n = 1). Initial treatment for MN consisted in CS in all patients (including oral prednisone in four out of five and pulse of methylprednisolone and subsequently oral prednisone in one), associated in all cases with immunosuppressant agents (IS). Initial IS included CSA (Neoral®) (n = 2), chlorambucil (n = 1) (Ponticelli protocol), AZA (n = 1) and MMF (n = 1). Rituximab and CSA were used in one case when the initial therapy with CS and MMF proved inefficacious (patient 3). The use of angiotensin-converting enzyme inhibitors was instituted in four out of five patients, angiotensin receptor antagonists in one and anti-coagulant therapy in four out of five.

Clinical and biological outcome (Table 2)
Data regarding outcome were available for four patients (Table 2). The remaining patient (patient 2) died of septic shock 3 months after the initiation of therapy, having achieved a PR.

Mean duration of follow-up was 19.8 months (range: 8–36 months). Mean proteinuria after treatment was 2.6 g/day (range: 0–5.5) and mean albuminaemia 3.3 g/dl (range: 1.6–4.6). Renal function improved in two patients, remained stable in one case and worsened in another case. CR of NS was obtained in two patients (patient 1 and 4), and PR in 1 patient (patient 5). One patient (patient 3) developed progressive renal insufficiency with persistent severe NS.

Patient 1 experienced a clinical relapse after CS and CSA discontinuation, but CR was obtained after the re-initiation of the same treatment. Patient 3 received successive IS (MMF, rituximab, CSA) because of deterioration of renal function and persistence of NS, with no efficacy.

In all patients, evolution of NS paralleled the evolution of cGVHD. In two patients with CR of NS under therapy, manifestations of GVHD disappeared; in one patient with PR of NS, moderate mucosal manifestations of cGVHD persisted; the patient with persistent NS and worsening renal function experienced severe and multiorgan involvement of cGVHD.

Treatment-related complications occurred in three patients: death in the setting of a septic shock in patient 2, corticosteroid-induced diabetes and septicaemia in patient 3, and pulmonary embolism and psychiatric disorders in patient 5.

Chimeric cells in kidney biopsies (Figure 2)
In patients 2 and 4, no XY chimeric cells were detected within the glomeruli and the tubules. Only XX female cells were noted in the glomeruli. Chimeric cells were present in the periphery of glomeruli and renal tubules, within the renal interstitium (Figure 2).


Figure 2
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  		Fig. 2. Patient 2. Kidney biopsy. FISH analysis of Y-chromosome. Absence of XY chimeric cells in the glomerule (upper panel) and the tubule (lower panel). The limits of the glomerule and the tubule are outlined by the dashed line.

 


   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
Acknowledgements
 References
 
Post-allogeneic HSCT MN remains an ill-defined entity. It is probably a rare complication of HSCT with only 24 cases reported so far (Table 4) [1–18], while the estimated number of allogeneic HSCT worldwide is around 15 000 per year. We report five cases of post-HSCT MN that illustrate the uncertainties regarding its pathogenesis and the variability of its response to treatment.


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  		Table 4. Characteristics and outcome of patients with post-haematopoietic stem cell transplantation membranous nephropathy previously reported in the literature

 
The most striking observation is the association of post-HSCT MN with acute manifestations of cGVHD. Ninety-three percent of patients with post-HSCT MN had a history of cGVHD, and nephropathy was coincidental with acute manifestations of cGVHD in 83% of cases (Table 5). Moreover, in our study, evolution of cGVHD was clearly correlated with the evolution of MN.


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  		Table 5. Main characteristics of the 24 previously reported cases and of the five cases presented herein

 
GVHD, the most frequent complication of allogeneic HSCT, results from an immune conflict between donor lymphocytes and recipient tissues. The aGVHD develops in 50–60% of recipients of sibling-matched allografts [19], and cGVHD, occurring after the first 100 days following HSCT, concerns 30–60% of patients [20]. The cGVHD results from the selective activation of donor CD4+/Th2 cells alloreactive to MHC or non-MHC-recipient antigens; CD4+ cells act as helpers for host B cells, leading to B-cell activation and auto-antibody production [21] such as anti-nuclear, anti-glomerular basement membrane and anti-renal tubular epithelial cell antibodies [22]. In some instances, cGVHD mimicks or is associated to various autoimmune diseases such as systemic sclerosis, Sjögren's syndrome, primary biliary cirrhosis, myasthenia gravis, polymyositis, etc [23]. Post-HSCT MN, which is characterized by immune-complex (IC) deposits, may represent another consequence of this graft-vs-host conflict [22]. Interestingly, in murine models of cGVHD, atypical MN is the main renal manifestation [22]. Renal damage due to pre-HSCT conditioning regimen, including total body irradiation, may unmask hidden autoantigens or modify them leading to the selective activation of alloreactive donor CD4+ cells, the production of IC and ultimately MN. However, no target antigens of the MN have been clearly identified to date, even though several molecules are potential candidates: neutral endopeptidase—the target antigen in human antenatal MN [24], nephrin [25], podocin [26], etc.

On the other hand, one cannot exclude that post-HSCT MN, in parallel with de novo MN occurring after renal transplantation, may result from a host-vs-graft reaction.

Donor-specific chimeric mesangial cells [27], tubular cells [28] and endothelial cells [29] have been previously detected in renal biopsies performed in patients who had undergone HSCT. Similarly, the haematopoietic origin of podocytes has been also suggested [30]. Thus, we sought to determine whether the presence of donor-specific chimeric podocytes may trigger a host-vs-graft reaction leading to MN. However, we failed to detect any intraglomerular chimeric cells in kidney biopsy specimens of two patients. Thus, our data do not support an alloimmunization basis for the post-HSCT MN.

In our patients, post-HSCT MN pathological features were quite similar to those of idiopathic MN. IgG1 and IgG4 were the predominant IgG subclasses in the glomerular deposits, a pattern similar to the one reported in idiopathic MN [31]. In contrast, all IgG subclasses are present in lupus-associated MN [31] and IgG1 and IgG2 predominate in malignancy-associated MN [32].

However, post-HSCT MN biopsies were remarkable for the presence of radiation nephritis features (i.e. mesangiolysis, intraglomerular thrombi) noted in two patients who had undergone total body irradiation. Moreover, tubulointersitial lesions, characteristic of ciclosporin toxicity, were present in the five cases. These lesions were the most severe in the two patients who had received total body irradiation and CSA.

CS and CSA, and to a lesser extent Rituximab, are the most used treatments in post-HSCT MN patients. On one hand, CS and CSA are the mainstay of acute manifestations of cGVHD treatment [20] usually present at the time of MN diagnosis. On the other hand, CS, associated with alkylating agents, and CSA have also proved efficacious in the treatment of idiopathic MN [33]. Recent data suggest a pathogenic role of CD20-positive cells in MN possibly as antigen presenting cell [34]. In clinical studies, rituximab has been used as a steroid-sparing agent both in idiopathic MN [35] and in cGVHD [16,36].

Response of post-HSCT MN to treatment with CS and IS is variable, however, with about three out of four of patients reaching partial or complete NS remission. The control of acute manifestations of cGVHD seems a prerequisite to the remission of NS. In accordance, NS recurrence during tapering or following CSA withdrawal was associated in one-third of the cases to the relapse of acute manifestations of cGVHD. Resuming CSA usually leads to the remission of both NS and aGVHD. Regarding rituximab, data are too limited to draw any definitive conclusion even though preliminary data may suggest that rituximab may prove helpful in the management of severe GVHD, and thus post-HSCT MN. Thus, we believe that CS and CSA should remain the first-line treatment of post-HSCT MN. However, there is no definite proof supporting our recommendation. Moreover, long-term CSA nephrotoxicity may become a critical issue in these patients, even though short-term renal tolerance of CSA was rather good in our patients. Thus, alternative therapeutic options are urgently needed. In the meantime, clinicians should use the lowest dose of CSA that induces a remission of GVHD and NS. Repeated renal biopsies may also be indicated in order to monitor renal toxicity due to CSA.

Post-HSCT MN treatment is burdened by a high morbidity and mortality. In our series, treatment-related severe complications occurred in three out of five patients and led to the death of one patient. Furthermore, our data are in accordance with the findings of a recent study [17].

In conclusion, experimental data and clinical observations suggest an association between cGVHD and post-HSCT MN. Treatment of post-HSCT MN, mainly CS and CSA, should be aimed at the control of GVHD which seems a prerequisite to the remission of NS.



   Acknowledgements
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Acknowledgements
References
 
The authors thank Pr Marie-Christine Copin (Lille), Dr Carole Cordonnier (Amiens) and Dr Colette Deminière (Bordeaux) for their collaboration.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Acknowledgements
 References
 

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Received for publication: 29. 6.06
Accepted in revised form: 6.12.06


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