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Steroid withdrawal or avoidance after kidney transplant.

Question: What is the evidence regarding steroid withdrawal or avoidance strategies and the effect on acute rejection and graft survival?

Corticosteroids have played a major role in immunosuppressive therapy since the early days of kidney transplantation (Hricik, Kupin, & First, 1994; Luan, Steffick, Gadegbeku, et al., 2009). Experiments in the 1950s, which focused on improving the survival of skin grafts in rabbits, led to the use of steroids in the treatment of rejection in recipients of kidney transplant. This ultimately contributed to the development of kidney transplantation as a successful and viable option for the treatment of kidney disease because steroids in combination with azathioprine formed the basis for maintenance immunosuppression (Jaber et al., 2007). However, while steroids have been found to have an important role in the treatment and prevention of acute rejection (Luan, Steffick, Gadegbeku et al., 2009), chronic steroid therapy is associated with significant adverse effects. These adverse effects include the promotion of hypertension, hyperlipidemia, diabetes, infection, osteoporosis, avascular necrosis, weight gain, cataracts, and mood changes, and may contribute to the development or worsening of cardiovascular disease (Jaber et al., 2007; Luan, Steffick, Gadegbeku et al., 2009; Nehus, Goebel, & Abraham, 2012; Oh, Kim, Kim, & Lee, 2012).

As early as 1972, studies aimed at reducing the toxic effects of steroids by decreasing the doses used for the prevention and treatment of acute rejection appeared in the literature (Augustine & Hricik, 2006; Hricik et al., 1994). The introduction of cyclosporine A (CyA) in the early 1980s brought increased interest in the prospect of steroid-free immunosuppression. CyA was found to be "steroid sparing," allowing for lower cumulative doses of steroids than had been possible with azathioprine (Hricik et al., 1994). Several studies, however, suggested that CyA, independent of steroids, contributed to the development of hypertension, diabetes, hyperlipidemia, and osteoporosis (Bennett & Porter, 1988; Hricik, Bartucci et al., 1991; Hricik et al., 1994; Hricik, Mayes, & Schulak, 1991; Hricik, O'Toole, Schulak, & Herson, 1993; Kasiske, Tortorice, Heim-Duthoy, Awni, & Rao, 1991; Movsowitz, Epstein, Fallon, Ismail, & Thomas, 1988; Yoshimura et al., 1988). Thus, there was concern that the benefit of decreasing exposure to steroids post-transplant could potentially be mitigated by the effects of CyA (Hricik et al., 1994).

Literature Review

Meta-Analyses

In 1993, a meta-analysis by Hricik and colleagues reviewed the findings of seven prospective, randomized trials published between 1984 and 1992. These studies examined patient and allograft survival, as well as the incidence of acute rejection, in patients receiving steroid-free, CyA-based maintenance immunosuppression with or without azathioprine (Hricik et al., 1993). Six studies examined either the complete avoidance of steroids or the withdrawal of steroids within three months following transplant. Findings suggested that steroid avoidance, or withdrawal, was associated with an increased risk of acute rejection with no effect on graft or patient survival. However, only one study examined graft and patient survival beyond two years; therefore, the authors concluded that more research was needed with longer patient follow up to assess the effect of steroid withdrawal or avoidance on chronic rejection, as well as to more fully assess the risk of acute rejection in cases of late steroid withdrawal (Hricik et al., 1993).

In a later meta-analysis, however, Kasiske, Chakkera, Louis, and Ma (2000) reviewed 10 steroid withdrawal studies published between 1987 and 1999, four of which extended patient follow up to four or five years. Their findings mirrored those of Hricik et al. (1993), suggesting that steroid withdrawal was associated with an increased risk of acute rejection. They also found a 40% increase in the relative risk of graft failure following steroid withdrawal, which only became evident when follow up was extended to five years (Kasiske et al., 2000).

As a result of these early findings, which seemed to clearly demonstrate an increased risk of acute rejection and possibly graft loss in the setting of steroid withdrawal or avoidance, interest in steroid-free immunosuppression was diminished (Luan, Steffick, & Ojo, 2009). Additionally, because only 47% of patients was found to be successfully maintained on steroid-free immunosuppression (Hricik et al., 1993), the long-term risk to graft survival was seen to offset any benefit that might be achieved from the withdrawal of steroids (Luan, Steffick, & Ojo, 2009).

The Effect of New Immunosuppressive Agents

In the late 1990s, new immunosuppressive agents were introduced, which revived the testing of steroid withdrawal regimens (Heilman et al., 2006; Luan, Steffick, Gadegbeku et al., 2009). Tacrolimus (TAC) and mycophenolate mofetil (MMF), as well as induction agents, such as thymoglobulin

and basiliximab, led to a decrease in acute rejection rates and seemed to present a more potent foundation on which to base steroid-free, or steroid withdrawal, immunosuppression (Heilman et al., 2006; Luan, Steffick, Gadegbeku et al, 2009; Luan, Steffick, & Ojo, 2009; Oh et al., 2012; Pascual, Quereda, Zamora, & Hernandez, 2004). As a result, Pascual et al. (2004) conducted another meta-analysis of steroid withdrawal trials published from 1999 to 2002. Their analysis, however, specifically focused on randomized controlled trials (RCTs) of steroid withdrawal in patients treated with either TAC or a modified, microemulsified form of CyA, along with MMF. This represented the most commonly used combination of immunosuppressive agents being used at the time, their goal being to separate these studies from the previous ones using CyA and azathioprine (Pascual et al., 2004). They reviewed four trials in patients receiving CyA and two in patients receiving TAC. Findings suggested an increased risk of acute rejection following steroid withdrawal, with no increased risk of early graft failure. Once again, however, the follow-up period was relatively short, one to two years in all but one study, the remaining study having a follow-up period of only three months. The authors again noted the need for steroid-withdrawal trials with longer follow-up periods to better assess the effect on long-term graft and patient survival (Pascual et al., 2004).

A Large Scale Review

In 2009, Pascual, Zamora, Galeano, Royuela, and Quereda undertook a larger scale systematic review of the steroid avoidance literature. In addition to RCTs, this review included a large number of observational, non-randomized studies because the authors believed valuable evidence might be found in these studies that might contribute important information when interpreted in light of the earlier systematic reviews (Pascual et al., 2009). Criteria for inclusion in this review included RCTs, or quasi-RCTs, in which one treatment group was randomized to either steroid avoidance or steroid withdrawal more than two weeks after transplant, and where intention-to-treat parameters for acute rejection and graft failure were clearly established. Observational studies were also included, provided that they included a system of retrospective cohort control. Study populations included adult and pediatric recipients of kidney transplants and patients with both first transplants and retransplants; however, recipients of multi-organ transplants were excluded. Specific interventions reviewed included steroid avoidance or withdrawal within 14 days of transplant versus maintenance steroids, steroid withdrawal more than 14 days after transplant versus maintenance steroids, and early (within 14 days of transplant) versus late (more than 14 days after transplant) withdrawal of steroids. Outcome measures included death, with or without graft function, graft loss, intention-to-treat (ITT) acute rejection, creatinine, and proteinuria, and also included blood pressure and number of antihypertensive medications prescribed, lipid values, new-onset diabetes, glycohemoglobin A1C values, infection, cataracts, bone density, weight gain, and malignancies (Pascual et al., 2009).

This review confirmed previous findings that despite an increased incidence of acute rejection, neither steroid avoidance nor steroid withdrawal approaches to immunosuppression following kidney transplant were associated with any increase in graft loss or patient death. Additionally, steroid withdrawal was associated with a decreased need for antihypertensive and lipid-lowering medications, a decrease in semm cholesterol, and a decreased incidence of cataracts and new onset diabetes requiring treatment. Steroid avoidance was associated with a decrease risk of cardiovascular events. In comparing steroid avoidance with steroid withdrawal, the only key difference identified was a decreased incidence of new onset diabetes requiring treatment in steroid avoidance groups.

The length of follow-up periods in the reviewed studies was once again identified as a limitation. The authors noted that, while more studies included extended patient follow up of three to five years, much of the long-term data was retrospective in nature and not part of a prospective study design. They concluded that steroid avoidance, or withdrawal within a few days of transplant, appeared to be safe options when coupled with antilymphocyte antibody induction therapy and maintenance immunosuppression consisting of either CyA or TAC and MMF or a similar agent, mycophenolic acid (MPA). Absent antibody induction, steroid withdrawal three to six months after transplant also seemed to be a safe strategy in patients being treated with CyA or TAC and MMF or MPA (Pascual et al., 2009). Pascual and colleagues (2009) cautioned they drew their conclusions "in the absence of strong, long-term data," and recommended long-term RCTs to clearly determine which steroid avoidance strategy is safest and most beneficial (p. 14).

Current Literature

A review of the literature from the past five years revealed an ongoing lack of studies with long-term follow up. Out of 16 studies dealing in some way with steroid withdrawal or avoidance following kidney transplant, only six included any follow up that was longer than three years. Only two studies extended follow up of some participants to 10 years, but one study specifically concerned the risk of graft loss from recurrent IgA nephropathy rather than general graft and/or patient survival (Aull et al., 2012; Cantarovich et al., 2010, 2013; Clayton, McDonald, & Chadban, 2011; Iwamoto et al., 2012; Kishikawa et al., 2010; Li et al., 2011; Luan, Steffick, & Ojo, 2011; Mai et al., 2013; Muthukumar et al, 2013; Nainani et al., 2012; Oh et al., 2012; Opelz & Dohler, 2013; Padiyar et al., 2010; Rizzari et al., 2012; Sureshkumar, Hussain, Thai, & Marcus, 2013; Suszynski et al., 2013; Thierry et al., 2012). However, studies continued to suggest that there is no decrease in graft or patient survival associated with steroid withdrawal protocols when used in conjunction with induction therapy and some combination of CyA/TAC and MMF (Aull et al., 2012; Cantarovich et al., 2010, 2013; Iwamoto et al., 2012; Mai et al., 2013; Oh et al., 2012; Rizzari et al., 2012; Sureshkumar et al., 2013; Suszynski et al., 2013; Thierry et al., 2012). While some studies continued to find an increased risk of acute rejection (Cantarovich et al., 2010; Iwamoto et al., 2012), others found no such increased risk, including one of the studies with 10-year follow up (Mai et al., 2013; Suszynski et al, 2013; Thierry et al., 2012). Rapid steroid withdrawal was associated with increased risk of acute rejection in African-American patients, a population generally held to be at increased immunologic risk, within the first 12 months after transplant. Biopsy-proven acute rejection episodes occurred in non-African-American patients in the first three months, while the incidence of acute rejection in African-American patients continued to increase throughout the first year (Padiyar et al., 2010).

One difficulty in the review and interpretation of steroid withdrawal/avoidance literature is related to the variability in practice and research protocols. Some "steroid-free" protocols are truly steroid-free, while others administer steroids for several days after transplant (early withdrawal), still others discontinue steroids several months after transplant (late withdrawal), and in some studies, the administered dose of steroid is not specified (Steiner, 2012). Variability also exists with regard to induction therapy agents and concomitant maintenance immunosuppression. All of these factors complicate the processes of meta-analysis and registry review (Steiner, 2012).

Evidence-Based Guidelines

The Kidney Disease: Improving Global Outcomes (KDIGO) workgroup was established in 2003 in recognition of the improved patient care that comes from the implementation of evidence-based clinical practice guidelines (Eckardt & Kasiske, 2009; Eknoyan et al., 2004). The stated mission of the KDIGO is to "improve the care and outcomes of kidney disease patients worldwide, through promoting coordination, collaboration, and integration of initiatives to develop and implement clinical practice guidelines" (Eknoyan et al., 2004, p. 1313, [paragraph] 3). Each guideline is graded according to the strength of the recommendation and the quality of the supporting evidence (Eckardt & Kasiske, 2009). The previous two clinical practice guidelines regarding the care of recipients of kidney transplants published by the American Society of Transplantation and a European best practices group had been primarily opinion-based. Therefore, the KDIGO workgroup saw a definite need for comprehensive, evidence-based guidelines that would improve the care of recipients of kidney transplants but also draw attention to areas where evidence was lacking (KDIGO Transplant Work Group, 2009).

In their clinical practice guidelines regarding immunosuppression, KDIGO recommended that steroids be discontinued within the first week following kidney transplant for patients that were considered to be at low immunologic risk for rejection, who had also received induction therapy. However, for patients remaining on steroids beyond the first week post-transplant, they recommended that steroids be continued indefinitely. Both guidelines, however, were given the lesser grade of "suggestion" rather than "recommendation," and while the strength of the evidence supporting the withdrawal of steroids during the first week was graded as "moderate," the evidence in support of the continuation of steroids was graded as "poor." They noted that the withdrawal or avoidance of steroids resulted in the trade-off of an increased rate of acute rejection, sensitive to treatment with steroids, with a decrease in steroid-related complications (KDIGO Transplant Work Group, 2009). Their recommendations for future research echo those made by the authors of review articles and meta-analyses: a large-scale RCT with long-term follow up "to determine if the benefits of steroid avoidance outweigh the harm" (KDIGO Transplant Work Group, 2009, p. S13, [paragraph] 6).

Support for the KDIGO guidelines on immunosuppression is not universal. Kidney transplant programs continue to have varied practices with regard to immunosuppression protocols in general, and the use of steroids in particular. Miller and Brennan (2014) specifically reference the 2009 KDIGO guidelines. They do not agree with the recommendation to discontinue steroids within the first week after transplant in low-risk patients who have received induction therapy. The reasons given for their disagreement with the KDIGO clinical practice guidelines include the lack of long-term follow up in the studies, which seem to show a benefit to steroid withdrawal, as well as the exclusion in these studies of patients considered to be at high immunologic risk for rejection. In their final recommendations, Miller and Brennan (2014) state their belief that the effects of long-term TAC or CyA use outweigh the long-term effects of low-dose steroids and note their use of low-dose steroids in their maintenance immunosuppression regimen.

Conclusion

After 40 years, the use or withdrawal of steroids following kidney transplantation remains a somewhat controversial issue. Some transplant centers use steroids as part of their routine maintenance immunosuppression protocol, and others routinely discontinue steroids. Differences also exist among centers that discontinue steroids; some withdraw steroids within the first week after transplant, and others discontinue them up to 12 months later (Miller & Brennan, 2014). The varied nature of transplant recipients and their specific risks for rejection and other complications would seem to point to the need for options or variation with regard to immunosuppressive regimens (Steiner & Awdishu, 2011). While the literature suggests that recipients of kidney transplants can be safely managed without the use of chronic steroids, the lack of large-scale, long-term RCTs makes it difficult to answer the question definitively. More research is necessary to once and for all define the risk of rejection and loss of graft function versus the benefits of an immunosuppressive regimen that does not include the use of long-term steroids.

Key Words: Kidney transplant, steroid withdrawal, steroid avoidance, immunosuppression.

References

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Linda S. Wright, DrNP, RN, CNN, CCTC, is Lead Kidney Transplant Coordinator, Thomas Jefferson University Hospital, Philadelphia, PA, and a member of ANNA's Keystone Chapter and the ANNA Research Committee. She may be contacted via email at linda.wright@jefferson.edu
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Title Annotation:Exploring the Evidence
Author:Wright, Linda S.
Publication:Nephrology Nursing Journal
Article Type:Report
Geographic Code:1USA
Date:Nov 1, 2014
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