Key Points

Question Is dialysis facility ownership associated with access to kidney transplantation?

Findings In this retrospective cohort study that included 1 585 947 patients with end-stage kidney disease treated at 6512 US dialysis facilities from 2000-2016, patients receiving dialysis at for-profit facilities vs nonprofit facilities had significantly lower 5-year cumulative incidence rates for placement on the deceased donor kidney transplantation waiting list (−2.6%), receipt of a living donor kidney transplant (−0.9%), and receipt of a deceased donor kidney transplant (−1.4%).

Meaning Receiving dialysis at for-profit facilities in the United States was associated with lower kidney transplantation rates.

Abstract

Importance For-profit (vs nonprofit) dialysis facilities have historically had lower kidney transplantation rates, but it is unknown if the pattern holds for living donor and deceased donor kidney transplantation, varies by facility ownership, or has persisted over time in a nationally representative population.

Objective To determine the association between dialysis facility ownership and placement on the deceased donor kidney transplantation waiting list, receipt of a living donor kidney transplant, or receipt of a deceased donor kidney transplant.

Design, Setting, and Participants Retrospective cohort study that included 1 585 947 patients treated at 6512 US dialysis facilities. Adult patients with incident end-stage kidney disease from the US Renal Data System (2000-2016) were linked with facility ownership (Dialysis Facility Compare) and characteristics (Dialysis Facility Report).

Exposures The primary exposure was dialysis facility ownership, which was categorized as nonprofit small chains, nonprofit independent facilities, for-profit large chains (>1000 facilities), for-profit small chains (<1000 facilities), and for-profit independent facilities.

Main Outcomes and Measures Access to kidney transplantation was defined as time from initiation of dialysis to placement on the deceased donor kidney transplantation waiting list, receipt of a living donor kidney transplant, or receipt of a deceased donor kidney transplant. Cumulative incidence differences and multivariable Cox models assessed the association between dialysis facility ownership and each outcome.

Results Among 1 585 947 patients, the median age was 65 years (interquartile range, 54-75 years), with 55.8% male, and 28.4% non-Hispanic black patients. Eighty-eight percent of patients received care at a for-profit dialysis facility. A total of 115 650 patients (7.3%) received care at 435 nonprofit small chain facilities; 66 539 (4.2%) at 325 nonprofit independent facilities; 527 458 (33.3%) at 2239 facilities of large for-profit chain 1; 525 997 (33.2%) at 2082 facilities of large for-profit chain 2; 245 633 (15.5%) at 997 for-profit small chain facilities; and 104 670 (6.6%) at 434 for-profit independent facilities. During the study period, 230 202 patients (14.5%) were placed on the deceased donor waiting list, 39 767 (2.5%) received a living donor kidney transplant, and 88 431 (5.6%) received a deceased donor kidney transplant. For-profit facilities had lower 5-year cumulative incidence differences for each outcome vs nonprofit facilities (deceased donor waiting list: −2.6% [95% CI, −2.8% to −2.4%]; receipt of a living donor kidney transplant: −0.9% [95% CI, −1.0% to −0.8%]; and receipt of a deceased donor kidney transplant: −1.4% [95% CI, −1.5% to −1.3%]). Adjusted Cox analyses showed lower relative rates for each outcome among patients treated at all for-profit vs all nonprofit dialysis facilities: deceased donor waiting list (hazard ratio [HR], 0.87 [95% CI, 0.86 to 0.88]); receipt of a living donor kidney transplant (HR, 0.82 [95% CI, 0.80 to 0.84]); and receipt of a deceased donor kidney transplant (HR, 0.83 [95% CI, 0.81 to 0.84]).

Conclusions and Relevance Among US patients with end-stage kidney disease, receiving dialysis at for-profit facilities compared with nonprofit facilities was associated with a lower likelihood of accessing kidney transplantation. Given the possibility of residual confounding, the clinical and policy implications of the results are uncertain.

Introduction

Quiz Ref IDKidney transplantation is the preferred treatment for most of the 700 000 adults with end-stage kidney disease (ESKD) in the United States as of 2016.1-3 However, only 14% of patients with incident ESKD are placed on the deceased donor kidney transplantation waiting list or receive transplants within 1 year of ESKD diagnosis.2 The Centers for Medicare & Medicaid Services (CMS) requires dialysis facilities to provide transplant education and help interested patients pursue kidney transplantation.4 The CMS amended the final rule for the End-Stage Renal Disease Prospective Payment System in 2018 by proposing a new dialysis facility quality metric to the End-Stage Renal Disease Quality Incentive Program to monitor the percentage of prevalent patients with ESKD on the waiting list for transplantation.5 In a July 2019 presidential executive order, the CMS also proposed the End-Stage Renal Disease Treatment Choices Model to improve access to kidney transplantation as part of the administration’s Advancing American Kidney Health initiative.6

Evidence suggests for-profit dialysis facilities have a lower standardized transplantation ratio,7 and their patients are less likely to be waitlisted compared with nonprofit facilities.8,9 Physicians at for-profit dialysis facilities are less likely to have detailed discussions with patients about transplantation or involve families in the discussion.10 This could lead to limited access to living donor kidney transplantation at for-profit dialysis facilities. Encouragement to pursue living donor kidney transplantation is highly advisable due to the limited supply of organs; no published study has assessed this relationship.

Quiz Ref IDIt has been suggested that for-profit dialysis facilities strive to reduce operating costs by limiting the provision of low-margin services11-13 (such as extended transplant discussions with patients and their families) in the interest of increasing returns to investors,14 and may impede their patients’ access to transplantation. This study aimed to determine the association between dialysis facility ownership and placement on the deceased donor kidney transplantation waiting list, receipt of a living donor kidney transplant, or receipt of a deceased donor kidney transplant. Changes over time in these associations also were examined.

Methods

Data Sources

A waiver of informed consent was granted for this retrospective, deidentified study (Emory University institutional review board decision No. 63645). All patients with incident ESKD from the publicly available US Renal Data System2 (USRDS) database (January 1, 2000-December 31, 2016) were merged with dialysis facility–level data from the Dialysis Facility Compare (2016) and the Dialysis Facility Report (2013-2016) CMS data sets. The USRDS collects information on US patients with ESKD at the start of long-term dialysis or receipt of a kidney transplant from the CMS-2728 form; it is prelinked with the United Network for Organ Sharing data on kidney transplantation waiting list and transplant events.

Dialysis Facility Compare reports the dialysis facility’s profit status and corporate ownership. The Dialysis Facility Report captures information on facility-level patient characteristics (mean age, percentage of males, race), mortality, treatment patterns, and transplantation rates. Patient observations from the USRDS and dialysis facility–level information from the Dialysis Facility Compare and the Dialysis Facility Report were linked using the facility’s CMS certification number. To obtain information on rurality, patient zip codes were linked to 2013 Rural Urban Continuum Codes from the US Department of Agriculture. Addresses from the Dialysis Facility Report were geocoded and used to calculate the distance from each facility to its nearest transplant center, in miles.

Study Population

All incident patients undergoing dialysis registered with the USRDS between January 1, 2000, and December 31, 2016, were considered for inclusion. Patients were excluded if they were younger than 18 years or older than 100 years, had a previous transplant or received multiple organ transplants, resided outside the 50 US states at the time of dialysis start, had unknown race/ethnicity or sex, or were placed on the waiting list or received a transplant prior to starting dialysis. Facilities with records in both the Dialysis Facility Compare and Dialysis Facility Report data sets were eligible for merging with the USRDS patient-level data (Figure 1).

Study Variables

The primary exposure was dialysis facility profit status and chain ownership obtained from the Dialysis Facility Compare data set. Facility profit status was defined as for-profit or nonprofit. Nonprofit facilities were defined as either small chain facilities or independent facilities based on Dialysis Facility Compare’s use of the term chain organization. Within the for-profit facility ownership categories, chain ownership was collapsed for each chain reported in Dialysis Facility Compare. For-profit chains with more than 1000 facilities were categorized as large chains; DaVita and Fresenius Medical Care (referred to as large chain 1 and large chain 2, respectively) were the only 2 chains with more than 1000 facilities and were categorized separately. For-profit chains with less than 1000 dialysis facilities were categorized collectively as small chains. The remaining facilities were classified as for-profit independent facilities. Patients were assigned to the dialysis facility from which they were receiving treatment when the outcome of interest occurred (ie, placement on the deceased donor kidney transplantation waiting list, receipt of a living donor kidney transplant, receipt of a deceased donor kidney transplant, death, or study end), and contributed all their person-time from dialysis start to event of interest to this facility.

The primary outcome was access to kidney transplantation, which was defined as placement on the deceased donor kidney transplantation waiting list, receipt of a living donor kidney transplant, or receipt of a deceased donor kidney transplant, each analyzed separately. If a patient was waitlisted and received a living or deceased donor kidney transplant, they contributed an event to each model. Patients were censored for either death or the end of the study (December 31, 2016), or the transplant date. The time to an event was calculated from the dialysis start date to the event date or censor date.

Clinical and demographic characteristics of patients were obtained from the USRDS data and collected from the CMS-2728 form by a dialysis facility staff member at dialysis start. Known risk factors for delayed transplantation were considered, including age at the start of dialysis, sex, race/ethnicity (both were classified by dialysis facility staff in fixed categories: sex as either male or female; race/ethnicity as either non-Hispanic white, non-Hispanic black, Hispanic white, or other defined as either Asian, Middle Eastern, Native American, Pacific Islander, or multiracial), rural/urban status, health insurance, primary cause of ESKD, dialysis modality (in-center hemodialysis, peritoneal dialysis, and home hemodialysis), and the presence of comorbidities such as body mass index greater than 35 (calculated as weight in kilograms divided by height in meters squared), cardiovascular disease, diabetes, and hypertension.

Due to the select all that apply format of the comorbidity section on the CMS-2728 form,5 comorbidities were coded as “yes” if a response was recorded or “no” if a response was missing. The primary cause of ESKD was categorized as diabetes, hypertension, glomerulonephritis, or other disease. Cardiovascular disease was defined as the presence of any of the following cardiac or pulmonary conditions: congestive heart failure, atherosclerotic heart disease, pulmonary vascular disease, cerebrovascular disease, chronic obstructive pulmonary disease, or other cardiac disease.

Dialysis facility–level characteristics were obtained from either the Dialysis Facility Compare or Dialysis Facility Report data sets. Patient-level variables from the USRDS were aggregated to define the facility-level number of patients and the percentage of patients reported by the facility that were not informed of kidney transplantation due to medical reasons. The Dialysis Facility Report provided the facility-level number of social workers, the ratio of patients to social workers, the ratio of patients to staff, the standardized mortality ratio, and the ESRD Network geographic areas.

The hospitalization rate per 100 person-years was obtained from the Dialysis Facility Compare data set. Transplant-center affiliation was defined through the United Network for Organ Sharing transplant center ID; and the hospital affiliation of a facility was defined by its CMS certification number. The addresses from the Dialysis Facility Compare data set were geocoded and used to calculate the distance from each facility to its nearest transplant center in miles.

Statistical Analysis

A descriptive analysis was performed for the overall population and comparisons between facility ownership were determined using either the χ2 test (for categorical variables), the Kruskal-Wallis test (for nonparametric continuous variables presented as median interquartile range [IQR]), or the t test (for parametric continuous variables presented as mean [SD]). Cumulative incidence differences and 95% CIs were calculated using the Aalen-Johansen estimator at follow-up years 3, 5, and 10 and accounted for the competing risk of death.15 The number needed to treat for each outcome was calculated using the inverse of the 5-year cumulative incidence difference.

To examine whether the cumulative incidence difference between facilities was constant by calendar year, we stratified the cohort into 2-year increments. Follow-up time was truncated for each period on December 31 of each 2-year period, and the unadjusted 2-year incidence rates (per 100 person-years) for placement on the deceased donor kidney transplantation waiting list, receipt of a living donor kidney transplant, and receipt of a deceased donor kidney transplant were calculated by dividing the count of events for incident patients by the number of incident patients in the dialysis facility ownership group for each interval. The incident rate differences (per 100 person-years) were calculated as the 2-year incidence difference between all nonprofit and all for-profit facilities.

Bivariable Cox proportional hazard models were used to determine the crude association between covariates and access to transplantation. Cox models were used to determine the crude and adjusted association between dialysis facility ownership and each outcome. Multiple imputation using the fully conditional specification implemented by the chained equations (MICE) algorithm were performed for missing covariate data. For continuous and categorical variables, Ridge Bayesian linear regression, allowing for posterior sampling and random forest, respectively, was conducted.16

We used robust sandwich covariance matrix estimates to account for intracluster dependence17 of patients within dialysis facilities. The adjusted Cox proportional hazard models in this study were developed using a 4-step process: (1) bivariable association between dialysis facility ownership and outcomes of interest, (2) adjustment for patient demographics (age, sex, and race/ethnicity), (3) adjustment for clinical characteristics, and (4) additional adjustment for socioeconomic variables. We tested the proportional hazards assumption by examining the significance of the Schoenfeld residuals with ranked follow-up time, and all proportionality assumptions were met.

Several sensitivity analyses were conducted to ensure the robustness of the results. Supplemental descriptive statistics and multivariable Cox models were generated for this population and were stratified by whether a patient switched dialysis facilities during the study follow-up. Dialysis facility switching was classified by comparing the patients’ first vs last dialysis facility. Sensitivity analyses examined cumulative incidence differences. Cox models were used to assess a cohort of “ideal kidney transplant candidates” that excluded patients (1) aged 66 years or older; (2) diagnosed with peripheral vascular disease, coronary heart failure, or cerebrovascular disease; or (3) not assessed for transplantation due to medical reasons (reported by dialysis facility staff on the CMS-2728 form). The Cox models assessed effect modification of geographic area and the association between facility affiliation with either a transplant center or hospital and each outcome.

Data management and statistical analysis were conducted using SAS version 9.4 (SAS Institute Inc) and Python version 3.6.8 (Python Software Foundation). Two-sided P values were used for all analyses and P < .05 was considered statistically significant.

Results

There were 1 865 462 incident patients with ESKD registered with the USRDS between January 1, 2000, and December 31, 2016. Patients were excluded if (1) younger than 18 years (n = 15 559) or older than 100 years (n = 67), (2) had a prior kidney transplant or index multiple organ transplants (n = 4772), (3) were living outside the United States (n = 27 934), (4) had unknown race/ethnicity (n = 1546) or sex (n = 222), (5) were preemptively waitlisted or received a transplant prior to initiating dialysis (n = 91 722), (6) had duplicate observations that did not occur at the last treatment facility (n = 550), and (7) did not match to a dialysis facility within the Dialysis Facility Compare or Dialysis Facility Report data sets (n = 137 093), leaving a final cohort of 1 585 947 unique patients included in the primary analysis (Figure 1). The median age was 65 years (IQR, 54-75 years), with 55.8% male, and 28.4% non-Hispanic black patients. Multiple imputation was used in the Cox models to account for the following missing data: health insurance coverage: 121 115 patients (7.6%); type of dialysis: 7944 (0.5%); distance from assigned dialysis facility to nearest transplant center: 341 693 (21.5%); and metropolitan rural-urban classification: 127 712 (8.1%).

The 1 585 947 included patients had a median follow-up time to placement on waiting list or censor date of 1.8 years (IQR, 0.7-4.0 years) and a median follow-up time to transplant or censor date of 2.3 years (IQR, 0.8-4.6 years). The majority of patients with ESKD received care at for-profit large chains with more than 1000 facilities (for-profit large chain 1: n = 527 458 [33.3%] at 2239 facilities; for-profit large chain 2: n = 525 997 [33.2%] at 2082 facilities; P < .001; Table 1). Nonprofit dialysis facilities had a slightly lower percentage of non-Hispanic black patients compared with for-profit facilities (26.4% vs 28.7%, respectively; P < .001), and there was a higher percentage of patients in the South treated at for-profit facilities compared with nonprofit facilities (42.7% vs 26.4%; P < .001) (Table 1 and eFigure in the Supplement).

Patient comorbidities were mostly similar across dialysis facility ownership categories. Treatment location for approximately 84.5% of patients diagnosed with hypertension ranged from 83.1% at nonprofit independent facilities to 85.6% at for-profit small chain facilities (P < .001). However, for patients diagnosed with diabetes, treatment location ranged from 44.0% at nonprofit independent facilities to 49.7% at for-profit independent facilities (P < .001). A higher percentage of patients treated at nonprofit independent facilities (8.6%), nonprofit small chain facilities (7.0%), and for-profit independent facilities (7.0%) were reported by facility staff as not being informed of kidney transplant options because of medical reasons compared with patients treated at facilities of for-profit large chain 1 (4.1%), facilities of for-profit large chain 2 (4.9%), and for-profit small chain facilities (4.8%) (P < .001). All nonprofit facilities had a median hospitalization rate of 178.1 (IQR, 148.3-209.9) per 100 person-years compared with the higher rate of 189.8 (IQR, 151.5-224.9) per 100 person-years for all for-profit facilities.

Primary Analysis

A total of 230 202 patients (14.5%) with incident ESKD were placed on the deceased donor kidney transplantation waiting list, 39 767 (2.5%) received a living donor kidney transplant, and 88 431 (5.6%) received a deceased donor kidney transplant. The percentage of patients placed on the deceased donor kidney transplantation waiting list during the study period was 16.8% for those treated at nonprofit small chain facilities, 17.2% for those treated at nonprofit independent dialysis facilities, 14.7% for those treated at facilities of for-profit large chain 1, 14.0% for those treated at facilities of for-profit large chain 2, 14.2% for those treated at for-profit small chain facilities, and 12.9% for those treated at for-profit independent facilities (Table 2). There was a lower percentage of patients treated at all for-profit facilities vs all nonprofit facilities who received a living donor kidney transplant (2.4% vs 3.3%, respectively) or a deceased donor kidney transplant (5.4% vs 7.0%).

In bivariable Cox proportional hazard models, patients younger than 60 years had an increased probability of being placed on the deceased donor kidney transplantation waiting list, receiving a living donor kidney transplant, or receiving a deceased donor kidney transplant. Compared with patients with ESKD caused by diabetes, those with ESKD attributed to glomerulonephritis were more likely to be placed on the deceased donor kidney transplantation waiting list (hazard ratio [HR], 1.20 [95% CI, 1.19-1.22]), to receive a living donor kidney transplant (HR, 2.26 [95% CI, 2.19-2.32]), or to receive a deceased donor kidney transplant (HR, 1.13 [95% CI, 1.11-1.15]) (Table 2).

The crude and adjusted time to event associations between dialysis facility ownership and placement on the deceased donor kidney transplantation waiting list, receipt of a living donor kidney transplant, and receipt of a deceased donor kidney transplant appear in Table 3. Nonprofit small chain dialysis facilities were used as the reference group. Patients receiving dialysis at all for-profit facilities vs all nonprofit facilities had lower 5-year cumulative incidence of placement on the deceased donor kidney transplantation waiting list (cumulative incidence difference, −2.6% [95% CI, −2.8% to −2.4%]), receipt of a living donor kidney transplant (−0.9% [95% CI, −1.0% to −0.8%]), and receipt of a deceased donor kidney transplant (−1.4% [95% CI, −1.5% to −1.3%]).

Compared with patients treated at nonprofit small chain dialysis facilities, patients were less likely to be placed on the deceased donor kidney transplantation waiting list at nonprofit independent facilities (HR, 0.93 [95% CI, 0.91-0.96]), facilities of for-profit large chain 1 (HR, 0.84 [95% CI, 0.82-0.85]), at facilities of for-profit large chain 2 (HR, 0.86 [95% CI, 0.85-0.88]), for-profit small chain dialysis facilities (HR, 0.85 [95% CI, 0.83-0.86]), and for-profit independent chain facilities (HR, 0.79 [95% CI, 0.77-0.80]) (Table 3). Patients treated at all for-profit facilities were less likely to receive a living donor kidney transplant compared with patients treated at all nonprofit facilities (HR, 0.82 [95% CI, 0.80-0.84]).

Patients treated at nonprofit independent facilities (HR, 0.89 [95% CI, 0.86-0.93]), facilities of for-profit large chain 1 (HR, 0.78 [95% CI, 0.76-0.80]), facilities of for-profit large chain 2 (HR, 0.82 [95% CI, 0.80-0.84]), for-profit small chain dialysis facilities (HR, 0.80 [95% CI, 0.78-0.83]), and for-profit independent chain facilities (HR, 0.73 [95% CI, 0.71-0.76) were less likely to receive a deceased donor kidney transplant compared with their counterparts in nonprofit small chain dialysis facilities. Based on 5-year cumulative incidence differences between for-profit and nonprofit facilities, the number needed to treat for placement on the deceased donor kidney transplantation waiting list is 38.5 (95% CI, 35.7-41.7); for receipt of a living donor kidney transplant, 111.1 (95% CI, 100.0-125.0); and for receipt of a deceased donor kidney transplant, 71.4 (95% CI, 66.7-83.3).

Two-year event incidence rates during the study period showed a general decrease during the last 17 years across dialysis facility ownership categories in patient placement on the deceased donor kidney transplantation waiting list (Figure 2A), receipt of a living donor kidney transplant (Figure 2B), and receipt of a deceased donor kidney transplant (Figure 2C). From 2001-2016, for-profit dialysis facilities had a lower 2-year incidence rate per 100 person-years for each event compared with other dialysis facility ownership categories. The for-profit vs nonprofit facility rate differences ranged from −1.83 to −2.89 per 100 person-years for placement on the deceased donor kidney transplantation waiting list; −0.27 to −0.88 per 100 person-years for receipt of a living donor kidney transplant; and −0.14 to −0.43 per 100 person-years for receipt of a deceased donor kidney transplant (Figure 2).

Overall, 77.0% of patients did not switch dialysis facilities during the study period, 19.7% switched facilities within the same profit status, 1.1% switched from for-profit facilities to nonprofit facilities, and 2.2% switched from nonprofit facilities to for-profit facilities (eTable 1 in the Supplement). Among the patients who switched facilities, the median time from first to last facility was 1.2 years (IQR, 0.3-3.2 years).

Sensitivity Analyses

The sensitivity analysis for the association between switching dialysis facilities and the outcomes of interest, stratified by the last dialysis facility where the patients received treatment appears in eTable 2 in the Supplement. Patients who switched from a nonprofit facility to a for-profit facility were less likely to be placed on the deceased donor kidney transplantation waiting list or receive a living or deceased donor kidney transplant compared with patients who started and continued treatment at for-profit facilities. For example, patients who switched from a nonprofit facility to a for-profit large chain 2 facility had a lower hazard of being placed on the deceased donor kidney transplantation waiting list (HR, 0.73 [95% CI, 0.70-0.77]) than patients who started and continued dialysis at the same for-profit large chain 2 facility.

The sensitivity analysis among the ideal kidney transplant candidate cohort reported similar relative risks to the primary analysis (eTable 3 in the Supplement). The 5-year cumulative incidence differences between all nonprofit facilities and all for-profit facilities were higher in the ideal cohort analysis for placement on the deceased donor kidney transplantation waiting list (−4.7% [95% CI, −5.1% to −4.3%]), receipt of a living donor kidney transplant (−2.2% [95% CI, −2.4% to −2.0%]), and receipt of a deceased donor kidney transplant (−2.9% [95% CI, −3.2% to −2.6%]). The sensitivity analyses found consistent results of lower rates for each outcome among nonprofit facilities vs for-profit facilities regardless of geographic area (eTable 4 in the Supplement). A reclassification based on either transplant center–affiliated dialysis facilities (eTable 5 in the Supplement) or hospital-affiliated dialysis facilities (eTable 6 in the Supplement) by profit status showed similar associations between nonprofit facilities and placement on the deceased donor kidney transplantation waiting list, receipt of a living donor kidney transplant, and receipt of a deceased donor kidney transplant.

Discussion

Quiz Ref IDAmong US patients with incident ESKD, nonprofit dialysis facilities had a higher percentage of patients who were placed on the deceased donor kidney transplantation waiting list, who received a living donor kidney transplant, and who received a deceased donor kidney transplant compared with the other dialysis facility ownership categories. However, the differences between nonprofit and other dialysis facility ownership categories for all outcomes were small.

To our knowledge, no studies have examined the relationship between dialysis facility profit status and both a living donor or a deceased donor kidney transplantation, and only 2 studies have examined the relationship between facility profit status and placement on the deceased donor kidney transplantation waiting list, reporting that patients were less likely to be waitlisted if initially treated at for-profit dialysis facilities vs nonprofit facilities.8,9 This study extends the work of Zhang et al8 by using hierarchical survival analysis to examine how dialysis facility ownership is associated with living donor and deceased donor kidney transplant and placement on the deceased donor kidney transplantation waiting list in a large national cohort of patients with ESKD from 2000 to 2016.

A strength of this analysis vs prior research was a novel approach of assigning dialysis facilities to patients. Nearly 23.0% of patients switched dialysis facilities during follow-up; however, only 3.3% of patients switched dialysis facilities by profit status. Recognizing this fact, the typically short follow-up these patients have with their initial dialysis facilities (median, 1.1 years), and the intensity of clinical follow-up leading up to placement on the deceased donor kidney transplantation waiting list or receipt of a kidney transplant (median, 2.3 years to transplantation), indicate that the last facility where a patient was treated may be more representative of the preparatory transplant care he or she receives.

Patients undergoing home dialysis also were included in this study (9.4% of cohort). Patients who receive home dialysis are more likely to undergo transplantation,18,19 but previous studies have excluded these patients.8,9

Quiz Ref IDThe sensitivity analysis that stratified patients by dialysis facility switch status showed that patients switching from nonprofit facilities to for-profit facilities were less likely to access transplantation vs patients who started and remained at the same nonprofit facility. The 2-year incidence rates for receipt of a living donor and a deceased donor kidney transplant decreased each year, and the incidence rate for placement on the deceased donor kidney transplantation waiting list increased from 2001-2014 and then decreased in 2015, congruent with declines observed in national reports.2,20 The decrease in placement on the deceased donor kidney transplantation waiting list since the new kidney allocation system took place in December 2014 is similar to the decline reported in the study by Zhang et al21 of 3.45 waitlisted events per month per 10 000 patients with ESKD. The profit-status disparity in the 2-year incidence rates for each outcome of interest persisted every year within this 17-year study cohort despite research identifying this problem nearly 2 decades ago.9

In 2014, the CMS began administering the In-Center Hemodialysis Consumer Assessment of Healthcare Providers and Systems (ICH CAHPS) survey to collect patient-reported satisfaction.22 The Dialysis Facility Compare website allows users to review patient satisfaction scores for local facilities and state- and national-level metrics under the “survey of patients experiences” tab. Based on the ICH CAHPS survey responses, only an estimated 67% of patients reported that their nephrologists “always communicated well and cared for them as a person.”23 These national data are similar to previous reports that more than 30% of incident patients with ESKD were uninformed of transplant options24 and nephrologists working at for-profit dialysis facilities were significantly less likely to spend longer than 20 minutes with their patients, counsel their patients about transplantation, or involve family members in the discussion.10

Quiz Ref IDClinician-level barriers, including clinician perception of the appropriateness of the possible transplantation,25-27 poor medical follow-up, time spent with patients,10 and format of transplant education,10 may lead to delays in access to transplantation, and could explain some of these findings, but are unmeasured in national data. Additional barriers, such as resource allocation of staffing to enable transplant education, could also play a role because prior research found that increased staff may improve access to kidney transplantation.7 Although this study reported more staff and social workers per patient at for-profit facilities vs nonprofit facilities, these findings did not explain the observed associations.

Limitations

This study has several limitations. First, given the availability of the data, it was not possible to determine the differences between profit status and chain affiliations regarding staffing resources,10,24,25,28,29 education policies,30-33 and transplant referral practices,34,35 all of which may be associated with increased access to kidney transplantation.

Second, although this analysis clustered dialysis facility ownership categories, we were unable to account for the nonrandom geographical location of for-profit and nonprofit chains, which may lead to unmeasured differences in patient characteristics across profit status categories.

Third, it is difficult to capture steps in the transplantation process that precede placement on the deceased donor kidney transplantation waiting list or receipt of a living donor or a deceased donor kidney transplant, such as transplant evaluation or referral for a transplant evaluation, and the effects may not be consistent by transplant step. A study by Patzer et al34 found that, among patients with ESKD in Georgia, the patients treated at for-profit facilities were more likely to be referred for a kidney transplant evaluation compared with patients treated at nonprofit facilities (odds ratio, 1.51 [95% CI, 1.20-1.91]), and there was no difference in placement on the deceased donor kidney transplantation waiting list among those referred within 1 year (odds ratio, 1.09 [95% CI, 0.83-1.44]). The sensitivity analyses found the association between profit vs nonprofit facilities and access to transplantation was consistent across all geographic areas; however, further research on transplant referral would permit analyses examining geographic differences in steps more closely aligned with dialysis facility behavior.36

Fourth, because of the wide variations in placement on the deceased donor kidney transplantation waiting list and in the practices of transplant centers across the United States,37,38 and the limitation of patient-level data collected at the start of dialysis, this study was unable to identify the patients truly eligible for transplantation. The sensitivity analysis of an ideal kidney transplantation cohort showed higher cumulative incidence differences and relative risks reporting the profit status disparity as presented in our primary analysis.

Fifth, the inclusion of dialysis facility staff–reported race/ethnicity could create a misclassification bias. However, Roach et al39 found high agreement between staff-reported race on the CMS-2728 form and patient-reported race in the Medicare enrollment database.

Sixth, the differences in the primary outcomes between for-profit and nonprofit facilities were small (0.9% to 2.6%). Given the observational nature of this study, residual confounding is of concern.

Conclusions

Among US patients with end-stage kidney disease, receiving dialysis at for-profit facilities compared with nonprofit facilities was associated with a lower likelihood of accessing kidney transplantation. Given the possibility of residual confounding, the clinical and policy implications of the results are uncertain.

Back to top Article Information

Corresponding Author: Rachel E. Patzer, PhD, MPH, Departments of Surgery and Medicine, Emory University School of Medicine, 101 Woodruff Cir, 5101 Woodruff Memorial Research Bldg, Atlanta, GA 30322 (rpatzer@emory.edu).

Accepted for Publication: August 6, 2019.

Retraction and Replacement: This article was retracted and replaced on April 21, 2020, to fix errors in the Key Points; Abstract; Results and Discussion sections; Figures 1 and 2; Tables 1, 2, and 3; and the eFigure and eTables 1 through 6 in Supplement 1 (see Supplement 2 for the retracted article with errors highlighted and Supplement 3 for the replacement article with corrections highlighted).

Author Contributions: Drs Gander and Patzer had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Gander, Ross, Browne, Pastan, Patzer.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Gander, Zhang, Ross, Browne, Wang, Patzer.

Critical revision of the manuscript for important intellectual content: Gander, Wilk, McPherson, Browne, Pastan, Walker, Patzer.

Statistical analysis: Gander, Zhang, Ross, Wilk, McPherson, Walker, Wang, Patzer.

Obtained funding: Gander, Patzer.

Administrative, technical, or material support: Gander, McPherson, Browne, Pastan, Walker, Patzer.

Supervision: Gander, Pastan, Patzer.

Other: Walker.

Conflict of Interest Disclosures: Dr Pastan reported receiving compensation and travel funds from ESRD Network 6 and receiving compensation from Retrophin Corporation. He is a shareholder of Old National Dialysis and a former minority owner of Fresenius College Park Dialysis; these companies were involved in litigation with Fresenius Medical Care, which has been resolved by binding arbitration. No other disclosures were reported.

Funding/Support: The study was supported in part by grant F32DK107191 from the National Institute of Diabetes and Digestive and Kidney Diseases, grants R01MD010290 and U01MD010611 from the National Institute on Minority Health and Health Disparities, and grants UL1TR002378 and TL1TR002382 from the National Center for Advancing Translational Sciences.

Role of the Funder/Sponsor: The funders/sponsors had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; or decision to submit the manuscript for publication.

Disclaimer: The data reported herein have been supplied by the US Renal Data System. The interpretation and reporting of these data are the responsibility of the authors and in no way should be seen as official policy or interpretation of the US government.

Additional Contributions: We thank Charles Wilson, senior news producer at Last Week Tonight With John Oliver, for opening this topic for discussion during interviews with Drs Gander and Patzer leading to the dialysis episode that aired on May 14, 2017.