Frailty is a clinical syndrome of decreased physiologic reserve, characterized by multisystem dysregulation with a deep biological basis of vulnerability that becomes evident when individuals are confronted with a stressor.1 In the United States, 15% of community-dwelling older adults are frail,2 based on the phenotype developed by Fried and colleagues.3 Although initially identified and characterized in community-dwelling older adults, frailty is now thought to be an important risk factor for adverse outcomes among individuals of all ages with end-stage kidney disease (ESKD).4 Among patients undergoing hemodialysis, frailty is associated with falls,5 hospitalizations,6-8 poor cognitive function,9 decreased health-related quality of life,10 and mortality.6,8 Additionally, among kidney transplant (KT) candidates, frailty is associated with lower likelihood of listing,11 higher waitlist mortality,12 and lower KT rates.11 Among KT recipients, frailty is associated with delayed graft function,13 postoperative delirium,14 longer length of stay,15 early hospital readmission,16 immunosuppression intolerance,17 lower health-related quality of life,18 impaired functioning,19 poor cognitive function,20 and higher mortality.21 Although research from up to 7078 KT candidates and 893 KT recipients supports the importance of frailty as a prognosticator in KT candidates and recipients, it is unclear how these findings are impacting clinical perceptions of frailty and clinical practices regarding the assessment of frailty.
In a Delphi study (n = 41 clinicians caring for older ESKD patients), a consensus building study, of clinicians treating patients with ESKD, 98% of respondents reported that frailty is an important construct among ESKD patients.22 Yet, this study demonstrated that clinicians are unable to identify which patients with ESKD meet the criteria for frailty, and patients themselves cannot recognize if they are frail.23 Although frailty is widely recognized as a construct of vulnerability, clinicians and patients may not agree on how to measure frailty because there are over 67 assessment tools available.24 Given the potential utility of frailty evaluation as a prognosticator among KT candidates, it is important to understand the global perceptions and practices regarding frailty at transplant programs in the United States.
Therefore, the American Society of Transplantation (AST) Kidney/Pancreas Community of Practice (KPCOP) convened a workgroup to better understand the landscape of frailty evaluation in KT candidates and recipients through a survey of US KT programs. The goals of this study were to characterize the national perceptions of frailty and to describe how frailty was currently being used in clinical practice at US adult KT programs.
MATERIALS AND METHODS
Survey Source Population
Adult transplant programs were identified using data from the Scientific Registry of Transplant Recipients (SRTR) external release. The SRTR data system includes data on all donors, waitlisted candidates, and transplant recipients in the United States submitted by members of the Organ Procurement and Transplantation Network (OPTN). The Health Resources and Services Administration, United States Department of Health and Human Services provides oversight to the activities of the OPTN and SRTR contractors. We included all transplant programs that performed adult KT in the United States in 2017. These national registry datasets were also used to determine program characteristics including total adult KT volume, median wait time, 1-year mortality and graft loss, mean age of adult recipients, percentage of recipients who were older (aged >65 y) at the time of KT, percentage of recipients who were female, percentage of recipients who were Hispanic, percentage of recipients who were African American, percentage of recipients who received deceased donor KT, and percentage of recipients who had less than a high school education.
Surveys about perceptions and practices related to frailty in KT were distributed via email to the members of the AST KPCOP and to the US transplant programs between November 2017 and April 2018. Adult transplant programs were identified in SRTR, and a list of transplant program medical directors was collated by the workgroup and AST Consensus Conference Organizers. All surveys were conducted using Qualtrics Survey Software. Representatives from programs without a respondent were sent a minimum of 1 and a maximum of 4 emails about the survey. One response per program was recorded, and the first complete response was considered for this analysis; no significant discordance was noted when multiple responses were returned from the same program.
The survey instrument was developed using an iterative process, based on a thorough review of the literature surrounding frailty in KT and discussions with the AST KPCOP Frailty workgroup and the members of the AST Frailty in Solid Organ Transplantation Consensus Conference. The final survey was approved by the AST KPCOP Educational Committee and the AST Board and consisted of 2 screening questions, 2 questions about the respondent, and included 10 core questions applicable to all solid organ transplant programs, and 16 questions developed specifically for KT programs. All questions were multiple choice or open text (Table S1, SDC, https://links.lww.com/TP/B746). The survey was reviewed and acknowledged to be exempt by the Johns Hopkins School of Medicine Institutional Review Board (September 2017); this research is in adherence with the Declaration of Helsinki and the Declaration of Istanbul.
First, we used individual, recipient-level data from 2017 to estimate program characteristics (mean age of adult recipients, percentage of recipients who were older at the time of KT, percentage of recipients who were female, percentage of recipients who were Hispanic, percentage of recipients who were African American, percentage of recipients who received deceased donor KT, and percentage of recipients who had less than a high school education) for each program. We then compared the distribution of these program characteristics and assessed whether they responded to the survey using weighted means and SDs; the weights were based on program volume in 2017.
The frequency of responses for all survey questions was calculated. Additionally, we quantified the associations between program characteristics and whether the program assessed frailty at evaluation and at admission for KT using modified Poisson regression to directly estimate the prevalence ratios (PRs) (as opposed to logistic regression to estimate the odds ratio); all program characteristics were included in a single model. For surveys with partial responses, each question was treated as a complete case analysis. For all analyses, a P < 0.05 was considered significant. All analyses were performed using Stata 14.0 (College Station, TX).
Participating Program Characteristics
Of the 202 adult KT programs in the United States, 133 responded (66%) to this national survey. Respondents were most commonly transplant nephrologists (61%) or transplant surgeons (28%). In 2017, the programs that responded to the survey listed 79% of the total KT candidates and performed 77% of the total adult KTs in the United States. The transplant programs that responded to the survey had a higher mean volume in 2017 (110.2 versus 62.6; P < 0.001) but were similar otherwise (Table 1).
Perceptions of Frailty in KT
Among the 133 responding adult KT programs, 99% agreed that frailty is potentially a useful concept in evaluating KT candidacy because frailty was viewed as a risk factor for adverse outcomes both before (98%) and after (98%) KT (Table 2). Functional limitations (eg, walking speed, grip strength, and sarcopenia) were the most important feature of frailty, with 65% of programs ranking this as the most important facet; functional limitations were followed by morbidity (16% of programs ranked most important) and cognitive ability (14% of programs ranked most important) (Figure 1). When asked about the essential components of frailty, the need for activities of daily living (ADL) assistance was reported by 95% of programs (Figure 1); the next most commonly reported components included sit to stand test (89%), unintentional weight loss (82%), and low physical activity (82%). The least commonly reported components were mood (30%) and laboratory markers (39%).
While 96% of programs agreed that the results of a frailty assessment should be used in decisions regarding candidate selection for KT, only 61% of programs reported that frailty assessments should be used in decisions for the timing of KT (Table 2). There was support for a distinction between irreversible and reversible frailty (84%) and a distinction between biological aging and frailty (93%); only 61% of programs considered biological age when assessing frailty in KT candidates and recipients. As such, 92% of programs reported that there is a need to develop a frailty score in the setting of KT.
Practices Related to Frailty in KT
In practice, 31% of programs never, 44% sometimes, and 25% always measured frailty during KT evaluation (Figure 2). No program characteristics were associated with measuring frailty at the time of KT evaluation (Table 3). Fewer programs measured frailty at the time of admission for KT (never: 72%; sometimes: 19%; and always: 9%). Of those programs that measured frailty at evaluation, 34% also measured frailty at admission for KT. KT programs with longer wait times were less likely to perform frailty assessments at KT evaluation (Table 3); for example, compared to centers with a wait time between 1 month and 9.6 months, those with a wait time of >1 year and 8 months were 22% less likely to measure frailty at KT evaluation. KT programs that had a higher percentage of male recipients (PR for a 10% increase: 1.54, 95% confidence interval [CI], 1.05-2.24; P = 0.03) and older recipients (PR for a 10% increase: 1.91, 95% CI, 1.10-3.32; P = 0.02) were more likely to perform frailty assessments than not perform frailty assessments at the time of admission for KT (Table 3). Of those who did not measure frailty, 97% were interested in measuring frailty in KT candidates and recipients. Frailty assessments were most often performed by a nurse (16%) or doctor (32%) during evaluation. Finally, transplant centers that measured frailty at KT had 1-year patient mortality (mean: 2.1% [SD = 1.6] versus 2.7% [SD = 1.9]) and 1-year graft loss (mean: 0.5% [SD = 0.6] versus 0.7% [SD = 1.0]) that were less than those center who did not measure frailty at admission for KT.
Programs reported using a variety of tools to measure frailty in KT (Figure 3); 18 out of 20 tools were used by >1 program, and 10% of programs reported a tool outside of the 20 frailty tools that were listed. The most commonly used tool to assess frailty in practice was a timed walk test, which was reported by 19% of programs. The next most commonly reported tools were measuring body mass index (15%), assessing functional status (12%), testing stair climbing (11%), conducting a timed-up-and-go test (11%), and counting the number of hospitalizations (10%). Sarcopenia, Montreal Cognitive Assessment, and the Fried frailty phenotype were assessed by 8% of programs. Body mass index as a tool to quantify wasting was used to measure frailty at 15% of centers. No programs reported using the Winograd Screening Instrument or the Rockwood Clinical Frailty Scale. Most programs (67%) reported assessing frailty using >1 tool.
The application for frailty assessments varied. Twenty-three percent of programs performed these assessments only for older patients (which was most commonly defined as age 65 and older) and 38% for all candidates. In addition, 89% of program reported comorbidities other than age were considered when deciding who should undergo frailty measurement; the most common of these comorbidities was history of a stroke and 7% of centers considered a patients’ obesity status when considering whether to measure frailty for that patient. Among programs that measured frailty, 91% indicated that information on frailty is presented at selection committee.
When a patient was identified as being frail, frailty was an absolute contraindication to listing at 75% of centers and to deceased donor transplantation at 33% of centers. Additionally, programs reported that when a patient was identified as being frail, the program was more likely to determine the amount of social/home support before listing (89%), prescribe prehabilitation (97%), and tailor immunosuppression (92%). No program reported using a candidate’s frailty status in isolation to decide whether to proceed with a living donor transplant or to accept a high kidney donor profile index organ offer.
In this national survey of KT programs, representing 79% of all KT candidates and 77% of all KTs performed in the United States, we found that 99% of programs agreed that frailty is a useful concept in evaluating candidacy for KT. The majority of these programs (95%) identified the inability to perform ADLs as the most essential component of frailty. However, we found that US KT programs use a variety of tools to measure frailty, and that no single tool was used by >20% of programs. The most commonly reported tool was a timed walk test, and 67% of programs used >1 tool. Frailty was more likely to be measured at KT evaluation than at admission for KT, and programs that had a higher percentage of male and older KT recipients were more likely to measure frailty at the time of KT. Over half of programs reported that they would be less likely to list a KT candidate who is frail, and the programs favored the use of interventions such as prehabilitation for frail candidates. Our survey results, representing majority of the US Transplant programs, highlight the heterogeneity in practice patterns for frailty measurements and the importance of standardizing tools and practices to improve the care of frail KT candidates.
The results from this survey extend the previous findings on the importance of frailty from a single-center Delphi study of clinicians who care for older patients with ESKD,22 showing that 99% of transplant programs consider frailty as a useful concept in evaluating candidacy for KT. The Delphi study found that there was consensus about the need for an ESKD-specific measure of frailty. In the current survey, we found that 92% of programs reported the need to develop a frailty score in the setting of KT. Furthermore, we found that 96% of programs felt that the results of a frailty assessment should be used to influence decisions regarding candidate selection for KT.
We have extended the findings of an international survey of geriatricians that suggested that there is a wide range of tools to measure frailty in clinical practice25 and in research;24 our survey findings confirmed that KT programs use many different tools and often >1 to assess frailty. Similar to geriatric practices,25 walk speed, as measured by a timed walk test, was the most commonly used tool to measure frailty. Many tools that were used by transplant programs are included in the hypothesized cycle of frailty by Fried and colleagues (gait speed, disability, and sarcopenia) or tools to measure geriatric syndromes that are associated with frailty (the Short Physical Performance Battery [SPPB] as a measure of lower extremity impairment, Montreal Cognitive Assessment as a measure of cognitive function, and self-reported functional status as a measure of dependence).3 However, it is important to consider that from a geriatrics and gerontology standpoint, comorbidity, cognitive impairment, physical function, and frailty are all separate geriatric syndromes.9,19,26-29 However, previous research in KT recipients suggests that different tools to assess vulnerability will identify different recipients as being frail,19 with prevalence rates among KT recipients ranging from 3% for cognitive impairment measured by the Modified Mini Mental Status Exam30 to 53% for the SPPB.19,31
As transplant centers consider the potential trade-offs of incorporating frailty measures into their practices, it is important to note that not all frailty assessments have been studied in the context of KT, and not all measures of vulnerability are necessarily associated with adverse outcomes among KT candidates or recipients. For example, the timed-up-and-go test is not associated with waitlist outcomes or post-KT hospitalizations among KT candidates.32 A previous study of KT recipients suggests that among the 5 components of the Fried frailty phenotype, poor grip strength, exhaustion, and slowed walking speed was the combination of components that was most strongly associated with post-KT mortality.29 Finally, previous studies have identified specific subgroups of patients in whom frailty is most strongly associated with adverse outcomes,33-35 suggesting that targeted screening for frailty may be warranted. For example, a study of 2086 KT candidates on the waitlist at Johns Hopkins or University of Michigan found that frailty was more strongly associated with waitlist mortality among candidates with a low comorbidity burden; this suggests that among high-risk patients, knowing a candidate’s frailty status provides less information about their mortality risk, than among those who are lower risk, such as those without a high comorbidity burden.33
Although centers agree that frailty is important, there are several potential barriers to more widespread adoption of frailty assessments by transplant programs. One very substantial barrier is that there are multitude of ways to identify vulnerable patients, as evidenced by the numerous frailty assessments that were reported in our survey study. Centers are already beginning to adopt specific measures for waitlist management;36 for example, Mayo Clinic has reported that as part of routine practice, all high-risk KT candidates undergo both physical frailty phenotype and SPPB at their center.37 Furthermore, new research suggests that the timing of frailty measurement matters with respect to post-KT risk stratification because frailty is dynamic while awaiting KT.38 To address the current lack in consistency in transplant center practices, future studies should establish and validate a single ESKD-specific tool to measure frailty in both KT candidates and recipients,39 build off the prior research on possible interventions to reverse frailty,40,41 and clarify whether all KT candidates and recipients, regardless of age, should have frailty assessed.41,42 Given that much of the evidence on the association between frailty and KT candidate and recipient outcomes has been derived from just a few centers (ie, 7078 KT candidates and 893 KT recipients from the University of Michigan, Johns Hopkins, and Methodist [KT candidates only]), future studies should include a broader spectrum of transplant centers across the United States and identify the ideal components of frailty metric for KT candidates as suggested by the recent AST-sponsored consensus conference on frailty in solid organ transplantation. Finally, an additional next step may be to initiate an implementation science study to promote the systematic expansion of measuring frailty among KT candidates and recipients pre and postrehabilitative programs to improve physiological processes and physical function.43-46
This survey has limitations. We were unable to obtain surveys from all US KT programs. The response rate, or percentage of all adult KT programs that responded to the survey, was 66%. However, most national surveys of transplant programs have response rates <60%,47-49 and our results reflect perceptions and practices of programs that impact 77% of all KT recipients and 79% of all KT candidates in the United States. Furthermore, we did not obtain information about perceptions and practices regarding frailty from dialysis units or during waitlist clinic evaluations. There are a number of strengths of this study, including a wide range of questions on the perceptions and practices regarding frailty, the geographic diversity of the participating programs, and the high percentage of US KT recipients that are reflected by the results of this survey.
In conclusion, this national survey of KT programs suggests that frailty is widely recognized as an important and clinically useful tool for evaluation of candidates. However, there was no consistent tool used to measure frailty and assess candidacy for KT across US transplant programs. Our data suggest an inconsistency of programs assessing KT candidates; thus, concerns arise that ambiguity regarding the most appropriate choice of frailty tools to be used in KT evaluations may adversely impact access to KT, particularly for older KT candidates.50 There is a need for education of transplant providers surrounding the number of tools to measure frailty. It is important for the field of transplantation to identify an existing tool or develop a novel tool to measure frailty51 that is valid, reliable, and easy to implement in clinical practice to determine whether a frail candidate will benefit from KT.
This article is a work product of the AST KPCOP and has been endorsed by the AST. We thank the study participants for their contributions to this study. The data reported here have been supplied by the Hennepin Healthcare Research Institute as the contractor for the SRTR. The interpretation and reporting of these data are the responsibility of the authors and in no way should be seen as an official policy of or interpretation by the SRTR, OPTN/UNOS, or the US Government. The authors are the members of the Frailty Consensus workgroup formed by the AST KPCOP; K.L.L. is the American Society of Nephrology Quality Committee representative to the workgroup.
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