https://orcid.org/0000-0001-7982-5213
Abstract
Background
Pre-emptive kidney transplantation (PEKT), i.e., transplantation performed before initiation of maintenance dialysis, is considered an ideal renal replacement therapy because there is no exposure to long-term dialysis therapy. Therefore, we summarized advantages/disadvantages of PEKT to assist in deciding whether kidney transplantation should be performed pre-emptively.
Methods
This study was registered with PROSPERO, CRD42021269163. Observational studies comparing clinical outcomes between PEKT and non-PEKT were included; those involving only pediatric recipients or simultaneous multi-organ transplantations were excluded. The PubMed/MEDLINE, Cochrane Library, and Ichushi-Web databases were searched on 1 August 2021. Studies were pooled using the generic inverse-variance method with random effects model, and risk of bias was assessed using ROBINS-I.
Results
Seventy-six studies were included in the systematic review (sample size, 23–121,853; enrollment year, 1968–2019). PEKT patients had lower all-cause mortality (adjusted HR: 0.78 [95% CI 0.66–0.92]), and lower death-censored graft failure (0.81 [0.67–0.98]). Unadjusted RRs for the following outcomes were comparable between the two patient groups: cardiovascular disease, 0.90 (0.58–1.40); biopsy-proven acute rejection, 0.75 (0.55–1.03); cytomegalovirus infection, 1.04 (0.85–1.29); and urinary tract infection, 0.89 (0.61–1.29). Mean differences in post-transplant QOL score were comparable in both groups. The certainty of evidence for mortality and graft failure was moderate and that for other outcomes was very low following the GRADE classification.
Conclusions
The present meta-analysis shows the potential benefits of PEKT, especially regarding patient and graft survival, and therefore PEKT is recommended for adults with end-stage kidney disease.
Introduction
Chronic kidney disease (CKD) is usually an irreversible and progressive disease that can lead to end-stage kidney disease (ESKD), which is a significant risk factor for death and cardiovascular disease (CVD) [Citation1]. Most patients with ESKD require renal replacement therapy via hemodialysis, peritoneal dialysis, or kidney transplantation. Although the mortality rate has declined among dialysis patients in recent decades [Citation2,Citation3], it remains high compared with that of the general population [Citation4]. Kidney transplantation is preferable to dialysis because it is associated with superior survival, cardiovascular outcome, and quality of life (QOL) and has a lower cost than dialysis [Citation5–8].
Previous studies have indicated that longer waiting time on pre-transplant dialysis is a strong risk factor for death [Citation9,Citation10]. Therefore, pre-emptive kidney transplantation (PEKT), i.e., transplantation performed before initiation of maintenance dialysis, is considered the ideal and optimal treatment for most patients with ESKD because of no exposure to long-term dialysis therapy. Although PEKT is generally recommended when the glomerular filtration rate falls below 15 mL/min, the optimal timing for PEKT is still unclear [Citation11]. The Descartes Working Group and the European Renal Best Practice (ERBP), which are both official bodies of the ERA-EDTA (European Renal Association-European Dialysis and Transplant Association), recommend that PEKT is planned in order to avoid dialysis, based on the results of their systematic literature review in 2016 on PEKT limited to living donor transplantation [Citation11]. However, only 2.5% of patients with ESKD in the United States and 4% of patients with ESKD in European countries actually receive a pre-emptive transplant [Citation12,Citation13].
As living donor transplantations account for only 31.7% of all kidney transplantations [Citation14], both living and deceased donor transplantations need to be included in order to systematically evaluate the usefulness of PEKT. Furthermore, a large number of papers on PEKT have been published since the publication of the ERA-EDTA recommendation in 2016, and there is a strong need to collect together the findings of these recent studies and update the evidence concerning the clinical effects of PEKT. In addition, whether kidney transplantation should be performed pre-emptively is an important clinical question; however, no meta-analysis has been conducted to evaluate the clinical efficacy of PEKT.
We therefore conducted a systematic review of the literature on kidney transplantation from living and deceased donors and meta-analyses to summarize the advantages and disadvantages of PEKT over non-PEKT. We hope that understanding the prognostic characteristics of PEKT will help clinical physicians to decide whether kidney transplantation should be performed pre-emptively in their medical practice.
Materials and methods
This systematic review and meta-analysis was performed according to the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) statement and the Meta-analysis of Observational Studies in Epidemiology (MOOSE) reporting guideline [Citation15,Citation16]. The protocol for the review was registered and published on International Prospective Register of Systematic Reviews (PROSPERO) (ID: CRD42021269163).
Eligibility criteria
Studies were eligible for inclusion if they had examined the important clinical outcomes described in the ‘Data collection process’ section in both PEKT and non-PEKT patients. PEKT was defined as kidney transplantation performed before initiation of maintenance dialysis, while non-PEKT was defined as kidney transplantation after initiation of maintenance dialysis. All adults with ESKD eligible for kidney transplantation, regardless of the type of donor (living or deceased) were included in the present study. Studies involving only pediatric recipients (age <18 years) and those involving only simultaneous multi-organ transplantations were excluded. Non-English and non-Japanese articles were included for languages where an appropriate translator was available. Although we would like to aim to include randomized controlled trials (RCTs), it is almost impossible for ethical reasons to conduct RCTs comparing the outcome after PEKT vs. non PEKT. Therefore, we included only observational studies.
Information sources and search strategy
A systematic electronic search was performed in PubMed/MEDLINE, The Cochrane Library, and Ichushi-Web, which is an online database of articles published in Japanese-language medical journals, on 1 August 2021. In addition, we hand-searched the reference list of a relevant systematic review [Citation11] for additional studies and confirmed that all studies were included in the results list of the initial database search. The detailed search strategies are included in Supplemental Table 1. Two authors (T.A. and N.K.) independently searched the database following the advice of experienced searchers, and any studies considered potentially relevant by at least one reviewer was recovered for further review.
Table 1. Overview of studies included in the systematic review.
Selection process
As a primary screening, titles and abstracts were independently screened by two authors (T.A. and N.K.). In the secondary screening that followed, the full text of each potentially relevant study was independently assessed by two authors (T.A. and N.K.) for inclusion in the present systematic review. Unpublished data and reports from conference abstracts were excluded from the systematic review. Disagreements between reviewers were resolved by a consensus-based discussion.
Data collection process
Data from included studies were extracted by two authors (T.A. and N.K.). We contacted study authors via e-mail for additional information where necessary. The detailed list of relevant items collected during data extraction is available in Online Resource 1. The primary outcome was patient survival. Secondary outcomes were as follows: graft survival, cardiovascular events, biopsy-proven acute rejection, health-related QOL, and infections. Detailed information on the definition of outcomes is found in Online Resource 2.
Study risk of bias assessment
We assessed the risk of bias in included studies using ROBINS-I which assesses risk of bias in seven domains: confounding, selection of participants in to the study, classification of interventions, deviations from intended interventions, missing data, measurement of outcomes, and selection of the reported result [Citation17]. Confounding domains and co-interventions are listed in Online Resource 3. Risk of bias assessment was performed independently by two authors (T.A. and N.K.). Disagreements between individual judgments were resolved through consensus-based discussion.
Effect measures and synthesis methods
Studies reporting adjusted hazard ratio (HR) for mortality and graft loss, the number of cases of each outcome (CVD, acute rejection, and infectious diseases), and the respective mean of each QOL score was integrated into the meta-analyses. Data were combined using the generic inverse-variance method in RevMan 5.4 (Reviewer Manager 5.4, Cochrane, Oxford, UK). Dichotomous outcomes are summarized using pooled HRs with corresponding 95% CI or RRs with 95% CIs. Mean differences with 95% CIs were used as the summary effect measures of continuous outcomes. We visually checked each effect estimate and 95% CI for both individual studies and meta-analysis in a forest plot. If CIs for the results of individual studies had poor overlap, the heterogeneity of intervention effects was evaluated using the I2 statistic. I2>50.0% was considered to represent significant heterogeneity. To assess heterogeneity, I2 was compared between subgroups as described in Online Resource 4. We used a random effects model that incorporated the potential heterogeneity among included studies to synthesize data. Publication bias for each outcome was assessed through visual inspection of the symmetry of the funnel plots. Sensitivity analyses were also performed to evaluate the influence of individual studies on each outcome using a leave-one-out method.
Certainty assessment
The certainty of evidence was evaluated according to the Grading of Recommendations Assessment, Development and Evaluation (GRADE) criteria, with each outcome being estimated as having a high, moderate, low, or very low level of evidence using the online software, GRADEpro GDT [Citation18–20].
Results
Characteristics of included studies
After removing duplicated studies, 3074 articles were identified in the initial search. Following screening, 97 articles were fully assessed for eligibility. Of these, 76 observational studies fulfilled the inclusion criteria and were included in the present study (). The reviewers agreed on study inclusion for 91.7% of articles (κ = 0.81). The main characteristics of the studies are summarized in and Supplemental Tables 2–9. Study sample sizes ranged from 23 to 121,853 (median 550), and the enrollment year of study participants ranged from 1968 to 2019.
Figure 1. Flow diagram of study inclusion.
Patient survival
Sixty-two studies compared mortality between PEKT patients and non-PEKT patients (sample sizes 44–121,853; median 719.5). Fourteen studies reported the adjusted HR of all-cause mortality, and 10 studies for which detailed information was available were included in the meta-analysis, with a combined sample size of 125,089 individuals (PEKT, 34,846 participants vs. non-PEKT, 90,243 patients).
The overall adjusted HR for all-cause mortality was 0.78 (95% confidence interval [CI], 0.66–0.92; I2=85%; moderate certainty evidence), indicating that PEKT likely reduced the likelihood of all-cause mortality relative to non-PEKT, with a large heterogeneity (). Post hoc subgroup analyses suggested that there was a statistically significant subgroup effect among the dialysis duration subgroup (p=.02) (Supplemental Table 10). On the other hand, in the subgroup analysis by donor type, the HRs for all-cause mortality were lower for PEKT, regardless of donor type (Supplemental Fig. 1). In post hoc sensitivity analysis, the leave-one-out analysis showed that no single study had a significant impact on overall estimations (Supplemental Table 11).
Figure 2. Forest plot of patient mortality.
Three studies that examined death with functioning graft (DWFG) were included in another meta-analysis, with a combined sample size of 68,912 individuals (PEKT, 32,496 participants vs. non-PEKT, 36,416 patients). The overall adjusted HR for DWFG was 0.74 (95% CI, 0.61–0.89; I2=82%), indicating that PEKT also likely resulted in a reduction in the likelihood of DWFG relative to non-PEKT (Supplemental Fig. 2).
Graft survival
Sixty-six studies compared the graft survival in PEKT patients with that in non-PEKT patients (sample sizes 44–121,853; median 773). Fourteen studies examined the adjusted HRs for death-censored graft failure (DCGF). Nine studies for which detailed information was available were included in the meta-analysis, with a combined sample size of 142,674 individuals (PEKT, 60,623 participants vs. non-PEKT, 82,051 participants). The overall adjusted HR for DCGF was 0.81 (95% CI, 0.67–0.98; I2=93%; moderate certainty evidence) (). The test for subgroup differences suggested that there was a statistically significant subgroup effect among the publication year subgroups (p<.001) (Supplemental Table 10). In post hoc leave-one-out analysis, we found that no single study had a significant impact on the overall estimations (Supplemental Table 11).
Figure 3. Forest plot of death-censored graft failure.
Cardiovascular diseases
In unadjusted analyses, six studies compared the cardiovascular event in PEKT patients with that in non-PEKT patients (sample sizes 44–786; median 155.5). All six studies were included in the meta-analysis, with a combined sample size of 1649 individuals (PEKT, 606 participants vs. non PEKT, 1043 participants). The overall risk ratio (RR) for CVD was 0.90 (95% CI, 0.58–1.40; I2=0%; very low certainty evidence) (Supplemental Fig. 3). PEKT may have no effect on CVDs, but the evidence is very uncertain.
Acute rejection
In unadjusted analyses, 39 studies compared acute rejection associated with PEKT with that associated with non-PEKT (sample sizes 23–90,160; median 334). Of these, 19 studies specified that acute rejection was defined as biopsy-proven. Nine studies were included in the meta-analysis, with a combined sample size of 3293 individuals (PEKT, 497 participants vs. non-PEKT, 2796 participants). The overall RR for biopsy-proven acute rejection was 0.75 (95% CI, 0.55–1.03; I2=36%; very low certainty evidence) (Supplemental Fig. 4). PEKT may have little effect on acute rejection, but the evidence is very uncertain.
Quality of life
In unadjusted analyses, five studies compared the QOL score in PEKT patients with that in non-PEKT patients (sample sizes 32–1849; median 99). Of these, four studies compared QOL score using the SF-36 (MOS 36-Item Short-Form Health Survey) between PEKT and non-PEKT patients. One study used the AIS (Acceptance of Illness Scale), SWLS (Satisfaction With Life Scale), and STAI (State-Trait Anxiety Inventory) as QOL scores instead [Citation15]. Of the four studies that compared SF-36 scores between PEKT and non-PEKT patients, three studies for which detailed data were available were integrated into the meta-analysis, with a combined sample size of 505 individuals (PEKT, 240 participants vs. non-PEKT, 265). The overall mean differences for each of the eight scaled scores of SF-36 did not differ between PEKT and non-PEKT participants (very low certainty evidence) (Supplemental Fig. 5). For outcomes other than BP (bodily pain) score, there was no evidence of heterogeneity across studies. When the study of Mitsui et al. [Citation21]. was omitted from the post hoc analysis, the heterogeneity completely disappeared (I2 reduced from 67% to 0%). Therefore, PEKT may have no effect on post-transplant QOL scores, but the evidence is very uncertain.
Infectious diseases
In unadjusted analyses, 10 studies compared the incidence of cytomegalovirus (CMV) infection in PEKT patients with that in non-PEKT patients (sample sizes 23–452; median 84). Nine studies were included in the meta-analysis, with a combined sample size of 1114 individuals (PEKT, 322 participants vs. non-PEKT, 892 participants). The overall RR for CMV infection was 1.04 (95% CI, 0.85–1.29; I2=0%; very low certainty evidence) (Supplemental Fig. 6). Five studies compared the incidence of urinary tract infection in PEKT patients with that in non-PEKT patients (sample sizes 44–452; median 82). Of these, one study showed that the incidence of urinary tract infections in PEKT patients was significantly lower than that in non-PEKT patients (PEKT 20.3% vs. non-PEKT 44.4%, p=.02), but the detailed data that is required for integration into the meta-analysis was not available [Citation17]. The remaining four studies for which detailed data were available were integrated into the meta-analysis, with a combined sample size of 650 individuals (PEKT, 144 participants vs. non-PEKT, 506 participants). The overall RR for urinary tract infection was 0.89 (95% CI, 0.61–1.29; I2=0%; very low certainty evidence) (Supplemental Fig. 7). Taken together, PEKT may have no effect on CMV infection and urinary tract infection, but the evidence is very uncertain.
Risk of bias and certainty of evidence
All eligible studies used a cohort design. Risk of bias was assessed in all 76 studies (192 outcomes) and the result is presented in Supplemental Table 12 and Supplemental Figs. 8–13. Funnel plots indicated no substantial publication biases for primary and secondary outcomes (Supplemental Figs. 14–19). A summary of findings in the present study is shown in .
Table 2. Summary of findings.
Discussion
This is the first meta-analysis that compared post-transplant outcomes between PEKT and non-PEKT patients and revealed that PEKT was likely associated with a reduced risk of mortality and graft loss relative to non-PEKT. The reduced mortality risk was probably consistent for different donor sources. However, the incidence of CVD, acute rejection, and infectious disease and post-transplant QOL scores did not significantly differ between PEKT and non-PEKT patients. Taken together, these results suggest that PEKT is the preferred therapeutic approach for adult patients with ESKD, especially in terms of low mortality and graft loss.
Our subgroup analysis of mortality in a living donor transplantation was consistent with ERA-EDTA recommendation for living donor transplantation [Citation11]. In addition, our meta-analysis of deceased donor transplants similarly showed that patient survival was better in PEKT patients than in non-PEKT patients. Therefore, PEKT is the preferred choice for transplantation from both living and deceased donors.
We also conducted post hoc subgroup analyses separated by the duration of dialysis in order to examine the impact of the duration of dialysis before kidney transplantation on post-transplant mortality. The adjusted HR for mortality in PEKT patients vs. short dialysis patients (on dialysis <1.5 years) tended to be lower (0.94, 95% CI, 0.88–1.01). A previous retrospective study that followed transplanted patients for a median of 8.2 years, which was included in the present subgroup meta-analysis, clearly showed, a stepwise dose-dependent increase in mortality with increasing dialysis duration [Citation10]. In contrast, a US dataset clearly indicated that there was no difference in patient mortality between PEKT and non-PEKT patients when the comparison was limited to short-term dialysis patients with a pre-transplant dialysis period of <1 year [Citation22]. Therefore, although we found that the adjusted HR for mortality in PEKT patients vs. short dialysis period patients tended to be lower, the correlation of dialysis duration before transplantation, especially of short-term dialysis, with survival is controversial; therefore, it is difficult to conclude that pre-transplant dialysis duration strongly affects mortality.
The detailed mechanism that leads to a lower mortality in PEKT patients than in non-PEKT patients has not been fully elucidated. Vascular calcification, chronic inflammation, arterial stiffening, and increased risk of infections, which are common in dialysis patients [Citation23–27], may contribute to the higher mortality rate in non-PEKT patients. In fact, the inverse association between eGFR and specific causes of death, including CVD and infection, was reported in a previous study [Citation28]. However, the incidence of CVD itself was not less in PEKT patients in the present study (RR, 0.90; 95% CI, 0.58–1.40; I2=0%; very low certainty evidence), indicating that PEKT may not be superior to non-PEKT in terms of CVD prevention. However, it should be noted that the incidence rate of CVD in studies included our meta-analyses was lower than that in a previous large database study [Citation29]. In addition, infectious disease is also an important factor that contributes to mortality in kidney transplant recipients. The present study found that there were no significant differences in the risk of developing CMV infection or urinary tract infection between PEKT and non-PEKT patients, although viral infection and urinary tract infection only cause a small number of deaths in kidney transplant patients [Citation30]. Furthermore, previous studies have shown that there is no significant difference in the proportion of deaths caused by infectious diseases between PEKT and non-PEKT patients [Citation10,Citation31]. Therefore, because there is no clear evidence that PEKT reduces CVD or infections, the present study did not elucidate the reasons that could explain the lower mortality with PEKT.
In terms of graft survival, PEKT also showed a benefit over non-PEKT. A French database study clearly indicated the gradual increase in HR for graft failure with pre-transplant dialysis duration [Citation32]. However, another cohort study indicated the advantage of PEKT on graft survival but did not find the significant association between rate of graft loss and pre-transplant dialysis duration [Citation10]. No plausible reason for this discrepancy has yet been found, but a national cohort study in the United States demonstrated that pre-listing ESKD time had a stronger impact on graft loss than waiting time on the deceased donor transplant list, and that pre-listing ESKD time was associated with comorbid conditions, socioeconomic status, and access to healthcare [Citation33], indicating the possibility that these factors, not pre-transplant dialysis time, may directly affect graft loss. Developing acute rejection can be considered another factor that strongly affects graft survival [Citation34]. The initiation of dialysis treatment is known to improve T-cell activation in ESKD patients [Citation35], although it is not known whether this causes acute rejection. Therefore, pre-transplant dialysis may increase the risk of acute rejection. In the present study, the overall RR for biopsy-proven acute rejection tended to be lower (RR, 0.75; 95% CI, 0.55–1.03; I2=36%; very low certainty evidence). Less rejection may partly be the reason for the lower HR for graft failure in PEKT patients, but because the result regarding acute rejection had very low certainty evidence, we cannot conclude a causal relationship between graft failure and rejection in the present study.
For patients on dialysis, receiving a kidney transplant can lead to independence from dialysis and improve their QOL [Citation36]. The QOL scores before transplantation in PEKT patients was better than that of dialysis patients [Citation19] because they have not experienced dialysis therapy. However, PEKT can also improve QOL and mental satisfaction after transplantation, albeit slowly [Citation21]. As the pre-transplant QOL scores themselves are different between PEKT and non-PEKT patients, it is difficult to directly compare the improvement in QOL scores before and after transplant between both groups. Therefore, we simply compared their QOL scores after transplantation, and found no significant difference between them.
The strengths of this systematic review include a comprehensive review of qualitative and quantitative study evidence, risk of bias assessment using ROBINS-I (Risk of Bias In Non-randomized Studies – of Interventions), and grading the certainty of evidence following the GRADE approach. However, these strengths should be balanced against the high heterogeneity across studies in the primary outcome. Post hoc subgroup analyses did not explain the heterogeneity in patient mortality across studies. However, among the dialysis duration subgroups, the test for subgroup differences suggested that there was a statistically significant subgroup effect, possibly and partially due to the small number of studies. Therefore, we judged that there was serious inconsistency in the primary outcome between studies.
Some limitations should be noted in the present meta-analyses. First, the time difference in ESKD period between PEKT and non-PEKT patients (i.e., lead time) may have affected the clinical advantage of PEKT. A previous registry study suggested that accounting for lead time moved estimates toward a survival disadvantage for PEKT, although this was in comparison to those transplanted within 6 months of commencing dialysis [Citation37]. However, it is difficult to accurately assess lead-time bias when the duration of dialysis is so short, as the prognostic difference by lead-time is unlikely to be clear. Although the issue of lead-time bias was not resolved in the present meta-analysis, future clinical studies should be designed to eliminate lead-time bias in order to assess the ‘true’ clinical efficacy of PEKT. If an RCT could be conducted in ESKD patients randomly assigning PEKT vs. non-PEKT as an intervention, it would be possible to assess the ‘true’ clinical efficacy of PEKT, completely removing the influence of lead time, but it is ethically difficult to implement. Alternatively, it may be possible to reduce the influence of lead time by conducting a retrospective study that observes the prognosis of ESKD patients in the PEKT and non-PEKT groups from the pre-transplant time point of matching eGFR in both groups. Second, because we integrated unadjusted RRs for CVD, acute rejection, and infections and unadjusted mean differences for each QOL score in PEKT patients vs. non-PEKT patients in our meta-analyses, baseline confounding was not fully eliminated; therefore, bias due to confounding may have affected the results (Supplemental Table 11). Third, no study evaluated CVD, acute rejection, or infectious diseases as a primary outcome; all have been evaluated as secondary outcomes or components thereof. Fourth, there are some variations in the definitions of CVD and infectious diseases among studies. Although we extracted myocardial infarction, stroke, CMV infection, and urinary tract infection as outcomes, their diagnostic methods were not described or defined in detail in each study; therefore, our meta-analyses may not have been able to assess identical outcomes.
To our knowledge, this is the first meta-analysis that examines the post-transplant outcome of PEKT and non-PEKT. The present meta-analysis shows the potential benefits of PEKT, especially regarding patient and graft survival. Nevertheless, the risk of rejection and infection in PEKT patients was comparable to that in non-PEKT patients, indicating that PEKT may not lead to any disadvantage. On the basis of these findings, we recommend that transplantation is performed pre-emptively.
Supplemental Material
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Download PDF (315.9 KB)Acknowledgements
We thank Dr. Sayaka Shimizu at Department of Community Medicine, Graduate School of Medicine, Kyoto University for help in conducting the statistical analysis. This systematic review was performed for the Evidence-based Clinical Practice Guideline for CKD 2023 on behalf of the Scientific Committee, Japanese Society of Nephrology, and therefore, we also thank the committee for their support in searching database and collecting papers. We also thank John Holmes, MSc, from Edanz (https://jp.edanz.com/ac) for editing a draft of this manuscript.
Disclosure statement
The authors report there are no competing interests to declare.
Data availability statement
The data used to support the findings of this study are included in the main text or supplementary materials. Any remaining information are available from the corresponding author upon reasonable request.
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