Renal Transplantation in the ANCA-Associated Vasculitides
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1 American Journal of Transplantation 2007; 7: Blackwell Munksgaard Minireview C 2007 The Authors Journal compilation C 2007 The American Society of Transplantation and the American Society of Transplant Surgeons doi: /j x Renal Transplantation in the ANCA-Associated Vasculitides D. Geetha a, and P. Seo b a Division of Nephrology and b Division of Rheumatology, Department of Medicine, Johns Hopkins University, Baltimore, MD Corresponding author: Duvuru Geetha, gduvura@jhmi.edu Despite advances in the diagnosis and treatment of the antineutrophil cytoplasmic autoantibodies (ANCA)- associated vasculitides, renal morbidity is common. End-stage renal disease occurs in up to 20% of patients with these diagnoses, which include Wegener s granulomatosis and microscopic polyangiitis. As the mortality of patients with ANCA-associated vasculitis continues to improve, our ability to address the consequences of renal failure in this patient population becomes paramount. Renal transplantation is an important therapeutic option for these patients. Graft and patient survival rates among patients with ANCA-associated vasculitis are comparable to those observed in nondiabetic patients. This review summarizes our current knowledge of indications and contraindications for renal transplantation in these patients, the recurrence of vasculitis after transplantation and the impact of posttransplant immunosuppression on the clinical course of these patients. Key words: ANCA, immunosuppression, kidney, recurrence, transplant, vasculitis Received 29 March 2007, revised 08 August 2007 and accepted for publication 09 August 2007 The small vessel vasculitides are comprised of a heterogenous group of uncommon disorders that are prone to cycles of remission and relapse. An important subset of these diseases is strongly associated with the presence of antineutrophil cytoplasmic autoantibodies (ANCA). These vasculitides include Wegener s granulomatosis (WG) and microscopic polyangiitis (MPA). The prevalence of the ANCA-associated vasculitides (AAV) has increased in recent years, an observation that is in part due to increased recognition of these complex diseases (1). Although the incidence of the AAV is only 20 cases per million per year, they are the most common cause of rapidly progressive glomerulonephritis (2). Despite advances in the diagnosis and treatment of the AAV, 20 40% of patients with pauciimmune renal vasculitis develop end-stage renal disease (ESRD) and have to be treated with renal replacement therapy (3). In one series of 123 patients with glomerulonephritis from either WG or MPA (followed for a median of 55 months), the 10-year renal survival was only 72% (4). ANCA and AAV Pathogenesis In 1985, van der Woude et al. reported finding ANCA in 25 of 27 serum samples from patients with active WG (5). Since that time, ANCA testing has become a standard part of the assessment of patients suspected of having a necrotizing vasculitis, and has greatly facilitated the diagnosis of incipient cases of WG and MPA. Whether ANCA actually cause AAV, however, has been less clear. Hypothetically, neutrophils can be primed by a variety of nonspecific stimuli; this process causes neutrophils to express antigens that bind ANCA (6). In vitro, it has been demonstrated that this interaction leads to neutrophil activation. In theory, these activated neutrophils could adhere to endothelial cells and degranulate, causing vascular necrosis. This theory has recently been bolstered by the development of animal models that demonstrate that, in the correct milieu, antimyeloperoxidase ANCA can cause glomerulonephritis as well as other organ manifestations associated with systemic vasculitis (7). This theory, however, fails to account for a minority of patients who clinically have AAV, but lack the eponymous antibody (6). Furthermore, it has been difficult to demonstrate a consistent correlation between the ANCA titer and vasculitis activity, which further calls into question the centrality of ANCA in the pathogenesis of these diseases. Outcome of AAV Patients on Dialysis Information about the long-term outcomes of AAV patients on dialysis is crucial to assess the value of renal transplantation for these patients. However, the literature on AAV relapse rate and patient survival after ESRD is scant. This may be due in part to a systematic failure to diagnose AAV among patients who present with ESRD. In 1993, Weidemann et al. detected ANCA in 97 (7.6%) of 1277 German chronic hemodialysis patients. Clinical evidence of vasculitis was found in 30 of these 97 patients. Four had a known diagnosis of WG and 3 had a clinical diagnosis of MPA. Although extra-renal manifestations of vasculitis were confirmed retrospectively, the diagnosis of AAV was initially missed in 23 of these patients (8). Of the 23 patients, 2657
2 Geetha and Seo 6 were diagnosed with WG, 12 were diagnosed with MPA and 5 were diagnosed with renal-limited vasculitis. There is mounting evidence that the diagnosis of AAV does not adversely affect mortality among patients with ESRD due to AAV. A systematic survey of over 1700 patients with rare systemic vascular diseases as a cause of ESRD was reported by Nissenson et al., who analyzed data from 28 of the 32 American ESRD Networks from 1983 to 1985 (9). The report concluded that the survival of patients with AAV was equal to that of a control nondiabetic population; the 33-month survival of patients with WG, for example, was 58%. A second study reported a 1-year actuarial patient survival of 82% and a 5-year actuarial patient survival of 59% for 59 AAV patients on chronic dialysis (3); this compares favorably with survival data from other dialysis registries, regardless of the cause of ESRD. In this study, AAV patients treated with either hemodialysis or peritoneal dialysis had an overall mortality that was comparable to that experienced by a nonimmunosuppressed population. Haubitz et al. (10) reported that the 2- and 5-year patient survival rate in 35 patients with WG and ESRD on chronic dialysis was comparable to the 2- and 5-year survival rates for patients with WG and renal involvement who were not dialysis dependent; these survival rates were also comparable to the survival rates for patients with ESRD from other causes. It has been speculated that chronic renal failure and dialysis decrease disease activity in AAV, similar to what has been observed among patients with lupus nephritis (11). Unfortunately, recurrence of vasculitis in patients on dialysis is not uncommon, and can affect any organ system (10,12). Moreover, vasculitis flares can mimic some of the complications of hemodialysis (e.g. pulmonary hemorrhage in a patient on hemodialysis could be mistaken for pulmonary edema; similarly gastrointestinal vasculitis could mimic peritonitis in a patient receiving peritoneal dialysis); this can lead to delayed diagnosis and potentially fatal delays in treatment (3). Different relapse rates for AAV have been described in the literature, ranging from 0.09 to 0.3 episodes per patient per year (3,10,12,13). These relapse rates are similar to those observed before ESRD develops; the discrepancy between studies may be due to the different treatment strategies employed by each group. Neither the form of vasculitis (i.e. WG vs. MPA) nor the type of hemodialysis membrane (i.e. cellulosic vs. noncellulosic) impacts the frequency of relapse among AAV patients on chronic dialysis (10). Interestingly, however, patients experience a 70 80% reduction in relapse rates after renal transplant (3); this may be due to the use of chronic immunosuppression after transplant. Renal Transplantation in AAV Patients Renal transplantation has been recognized as an option for renal replacement therapy since 1972, when Lyons and Lindsey reported a successful outcome for a renal allograft in a 29-year-old man with WG (14). Renal transplantation has been shown to improve the quality and quantity of life among patients with ESRD, regardless of the cause of renal failure (15,16). In one large retrospective analysis of 59 AAV patients with ESRD from a single center, transplanted patients had better survival than those who remained on dialysis (although they were also younger, which makes this observation difficult to interpret) (3). In a large cohort of 378 transplanted WG patients, the 10-year patient survival was significantly better than the 10-year patient survival of transplanted patients with polycystic kidney disease (80% vs. 70.9%, p < 0.05) and was slightly reduced when compared with transplanted patients with IgA nephropathy after renal transplant (84.5%, p = 0.005) (17). The mean 10-year graft survival for the patients with WG was 65.4% (17), which compares favorably to graft survival observed in other nonsystemic inflammatory conditions (3,17,18,19). Unfortunately, renal transplant for patients with AAV may not be without risk; a recent analysis of 43 patients with pauci-immune small vessel vasculitis (n = 33) and anti-glomerular basement membrane (anti-gbm) disease (n = 10) noted a significant increase in malignancy (mainly skin cancer) after renal transplantation (18). Recurrence of AAV After Transplantation The initial hope was that the standard transplantation protocols for rejection prophylaxis might be sufficient to prevent vasculitis relapse. That hope vanished when Steinman et al. reported recurrence of WG 4 years after transplantation despite continued immunosuppression with prednisone and azathioprine (20). Subsequently, several case series have reported relapse rates among patients with AAV after transplant that range from 0.02 to 0.1 relapses per patient per year (Table 1). A pooled analysis by Nachman et al. of both reported and unreported cases showed an overall recurrence rate of 17%, with an average time from transplant to relapse of 31 months (21). These relapses may vary significantly with respect to severity and organ involvement. Cases of catastrophic onset of anuric renal failure due to acute arteritis and ureteral stenosis, and obstructive uropathy due to granulomatous vasculitis at the ureterovesicle junction have been reported (22,23). In general, however, disease recurrence in the renal allograft will manifest as a pauci-immune necrotizing glomerulonephritis (Figure 1) (24). Nevertheless, not all vasculitis flares after transplant will affect the kidney. Table 1: Relapse rate after transplant Study Subjects Relapse per patient per year Schmitt, Haubitz, Allen, Elmedhem, American Journal of Transplantation 2007; 7:
3 Renal Transplantation in the ANCA-Associated Vasculitides patients with positive ANCA (10,13,26 29). C-ANCA was detectable in 8 of 12 WG patients at the time of transplantation in the study by Schmidt et al. (12), and in 7 of 8 patients in a case series by Rostaing et al. (30). Only one of the patients in the latter group relapsed; four others remained ANCA positive during follow-up but remained in remission. In a pooled analysis of recurrent AAV after renal transplant in 33 patients, there was no significant difference in the relapse rate between those with or without detectable ANCA titers at the time of transplantation. There was also no difference in the rate of relapse after transplantation based on ANCA pattern or antigen specificity (21). Figure 1: Crescentic glomerulonephritis in a patient with WG (Courtesy of Basim Mohammed, M.D.). In the pooled analysis of recurrent AAV after renal transplant by Nachman et al., 60% of patients had recurrent glomerulonephritis (either alone or in addition to other organ involvement) whereas 40% had signs of recurrent extra-renal vasculitis only. The mean time from transplant to relapse in this study was 31 months; however, disease flare can occur as early as 5 days or as late as 13 years after transplantation (22,25). Factors that could affect the rate of relapse include (1) time on dialysis prior to transplant, (2) ANCA status at the time of transplant and (3) the choice of posttransplant immunosuppression. Each of these issues raises important questions that are often faced by clinicians during the evaluation of a patient with AAV for renal transplant. 1. Do patients benefit from delaying renal transplant? A retrospective analysis of nine patients with AAV who underwent renal transplant noted that the two patients who had relapsed had received hemodialysis for a mean of 10 months prior to renal transplantation, as opposed to a mean of 54 months among the patients who did not relapse (p = 0.22). In contrast, a comprehensive pooled analysis of 127 patients with AAV demonstrated no statistically significant difference in the distribution of time on dialysis between patients who relapsed and those who remained in remission (21). Therefore, once clinical remission is achieved, a further delay in transplantation does not seem to improve the outcome. 2. Does a positive ANCA preclude renal transplant? In contrast to anti-gbm disease (in which persisting anti- GBM antibodies are associated with a higher recurrence rate), evidence is accumulating that the presence of positive ANCA should not preclude transplantation in patients who are clinically in remission. Several groups have reported successful transplantation in both WG and MPA Although the presence of ANCA at the time of transplantation does not appear to increase the risk of relapse, it is common practice to monitor ANCA titers after transplant in an attempt to identify patients who may be at greater risk of disease flare. The value of serial ANCA measurements, however, has been difficult to demonstrate across studies. For example, Tervaert et al. report that an increase in PR3- ANCA is a strong predictor of relapse within 1 year (relative risk 18.6; 95% confidence interval (CI): ) (31). In contrast, Finkielman et al. recently reported that increases in PR3-ANCA levels did not predict relapse among patients with WG (hazard ratio 1.0, 95% CI: ) (32). The disagreement among studies is likely due to differences in study designs and the absence of a universally accepted method of testing for ANCA (33,34). Until ANCA testing is standardized, it is difficult to recommend serial ANCA measurements as a method of risk stratification. 3. How does the choice of background immunosuppression affect disease outcomes? Although monoclonal anti-t-cell antibodies have been employed for the treatment of refractory WG, there are no data on how administration of antibodies against IL-2R, CD-20 or T cells for rejection prophylaxis affect relapse rate in AAV. Nevertheless, many immunosuppressive drugs used for renal transplant are also used to treat AAV. It is therefore reasonable to wonder whether the choice of maintenance immunosuppression might influence long-term outcomes in the underlying vasculitis. Clarke et al. suggested that cyclosporine-based immunosuppression was associated with a lower relapse rate than azathioprine-based regimens (35), but this has not been confirmed in recent reports. The pooled analysis by Nachman et al. of 127 transplanted AAV patients demonstrated a recurrence rate of 20% among the cyclosporine-treated patients, which was not significantly different from the relapse rate observed in the group as a whole. Mycophenolate mofetil has been used to induce and maintain remission of vasculitis in AAV patients in a nontransplant setting. Stassen et al. used mycophenolate mofetil for induction in 32 patients with WG who were intolerant American Journal of Transplantation 2007; 7:
4 Geetha and Seo of cyclophosphamide, and were able to induce remission in all but 1 patient (36). Nowack et al. successfully used mycophenolate mofetil and low-dose prednisone for remission maintenance in 11 patients with AAV. In this 15 month study, only one patient relapsed (14 months after treatment was initiated) (37). This contrasts with the series by Langford et al. in which 6 out of 14 patients treated with mycophenolate mofetil relapsed (38). Unfortunately, the use of mycophenolate mofetil as part of the transplant protocol does not guarantee long-term remission. New data from the Collaborative Transplant Study on 378 WG patients who received kidney transplants showed that treatment with mycophenolate mofetil after transplant was associated with a significantly higher relapse rate than treatment with azathioprine (39). In a single center cohort of AAV patients undergoing kidney transplant, Gera et al. reported only three non-renal relapses among 35 patients, the majority of whom received maintenance immunosuppression with mycophenolate mofetil, tacrolimus and glucocorticoids. It is important to note, however, that 28 of these patients also received induction therapy with ATG, which may have played some role in the low relapse rate observed (40). Regardless, it is clear that the transplanted kidney is not immune to relapse: in one cohort of 19 patients with AAV who were followed for a mean of 45 months after renal transplant, 7 patients experienced a relapse that involved the kidneys, yielding a renal relapse rate of per patient per year (41). It is sobering to note that over half of these events occurred during the first 3 months following transplant. These data suggest that even modern immunosuppression regimens used in renal transplant do not provide absolute protection from relapse. Treatment of AAV After Transplantation When first described, generalized WG was a uniformly fatal diagnosis. The Fauci Wolff protocol which introduced the use of cyclophosphamide for the treatment of AAV was a watershed, transforming a formerly terminal illness into a chronic disease. Oral cyclophosphamide continues to form the cornerstone of therapy for glomerulonephritis and other severe manifestations of the AAV. This holds true after renal transplantation as well: the pooled analysis of recurrent AAV by Nachman et al. and other series demonstrate a generally good response to cyclophosphamide for the treatment of relapses (13,19,22,30,42,43). Despite its success at remission induction, cyclophosphamide-induced remission comes at a heavy price: in the NIH experience, 44% of patients with WG develop treatment-related morbidity, including hemorrhagic cystitis, bladder cancer and myelodysplasia. In addition, over half of women (57%) with AAV treated with cyclophosphamide became infertile (44). The modern approach to the treatment of the AAV employs a cytotoxic agent (such as cyclophosphamide) for a period of 6 months to achieve remission, after which remission is maintained by using a less toxic antimetabolite drug, such as methotrexate or azathioprine. Mycophenolate mofetil or leflunomide may also be appropriate for remission maintenance (45). Although this treatment strategy greatly reduces overall exposure to cyclophosphamide, the need for alternative, less toxic treatment strategies is clear. Biologic therapies, which selectively target components of the immune system, have revolutionized the treatment of autoimmune disease. Unfortunately, TNF inhibitors (such as etanercept, infliximab and adalimumab) have not proven to be broadly effective for the treatment of patients with AAV (46). On the other hand, B-cell directed therapies hold great promise for the treatment of these diseases. Rituximab is a monoclonal anti-cd20 antibody that depletes B lymphocytes through a variety of mechanisms. Several case series have indicated that rituximab may be effective for the treatment of severe manifestations of AAV, even for patients who are refractory to cyclophosphamide therapy (47,48). Although rituximab-induced remission is not permanent (49), early evidence indicates that additional cycles of rituximab are both safe and welltolerated (50). Because this treatment strategy is new, the risks associated with rituximab may not yet be fully evident (51). It is therefore difficult to recommend rituximab over standard treatment strategies at this time. Nevertheless, this drug and other biologic agents may dramatically change our approach to these diseases in the near future. Conclusions Renal transplantation is an important option for patients with AAV who develop ERSD. Despite this, the long-term outcomes of patients with AAV after renal transplant are not well described. Given the small number of AAV patients undergoing renal transplantation in any single center, questions regarding transplantation in the setting of active disease, the choice of optimal anti-rejection regimen and the safety and efficacy of immunosuppression in this patient population can only be answered by prospectively collecting data in a multicenter registry of patients with AAV undergoing renal transplantation. Until such data are available, we believe that it is reasonable to draw the following conclusions from the available literature: Patient and graft survival rates are comparable to those observed among patients with ESRD from other causes. Currently available data do not support the need for a waiting period after remission is achieved prior to transplant; neither length of time on dialysis nor ANCA status correlate reliably with posttransplant outcomes American Journal of Transplantation 2007; 7:
5 Renal Transplantation in the ANCA-Associated Vasculitides Both renal and extra-renal relapse occur in patients with AAV after transplant, regardless of the background immunosuppression regimen chosen. Recurrence of glomerulonephritis after transplant can be treated effectively with cyclophosphamide, but other regimens using rituximab or other biologic agents may soon supplant cytotoxic drug-based therapies. Acknowledgment Dr. Seo is a Lowe Family Scholar in the Johns Hopkins University Center for Innovative Medicine. References 1. Watts RA, Carruthers DM, Scott DG. Epidemiology of systemic vasculitis: Changing Incidence or Definiton? Semin Arthritis Rheum 1995; 25: Jayne DR, Marshall PD, Jones SJ, Lockwood CM. Autoantiboides to GBM and neutrophils cytoplasm in rapidly progressive glomerulonephritis. Kidney Int 1990; 37: Allen A, Pusey C, Gaskin C. Outcome of renal replacement therapy in antineutrophil cytoplasmic antibody associated systemic vasculitis. 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