Disparities in Provision of Transplant Education by Profit Status of the Dialysis Center

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1 American Journal of Transplantation 2012; 12: Wiley Periodicals Inc. C Copyright 2012 The American Society of Transplantation and the American Society of Transplant Surgeons doi: /j x Disparities in Provision of Transplant Education by Profit Status of the Dialysis Center K. S. Balhara a,l.m.kucirka a,b.g.jaar b,c,d and D. L. Segev a,c, * a Department of Surgery, Johns Hopkins School of Medicine, MD b Department of Medicine, Division of Nephrology, Johns Hopkins School of Medicine, MD c Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, MD d Nephrology Center of Maryland *Corresponding author: Dorry Segev, dorry@jhmi.ed Kidney transplant education is associated with higher transplantation rates; however national policies regarding optimal timing and content of transplant education are lacking. We aimed to characterize nephrologists attitudes regarding kidney transplant education, and to compare practices between nephrologists at for-profit and nonprofit centers. We surveyed 906 nephrologist practicing in the United States. Most respondents (81%) felt the ideal time to spend on transplant education was >20 min, but only 43% reported actually doing so. Spending >20 min was associated with covering more topics, having one-on-one and repeated conversations, involving families in discussions and initiating discussions at CKD-stage 4. Providers at for-profit centers were significantly less likely to spend >20 min (RR = 0.89, 95%CI: ) or involve families (RR = 0.57, 95%CI: ); they reported that fewer of their patients received transplant counseling (RR = 0.58, 95%CI: ), initiated transplant discussions (RR = 0.58, 95%CI: ), or were eligible for transplantation (RR = 0.45, 95%CI: ). Of nephrologists who spent 20 min, those at for-profit centers more often cited lack of reimbursement as a reason (30.0% vs. 18.9%, p = 0.02). Disparities in quality of education at for-profit centers might partially explain previously documented disparities in access to transplantation for patients at these centers. National policies detailing the optimal timing and content of transplant education are needed to improve equity. Key words: Access to transplant, kidney, profit, transplant education Abbreviations: RR, relative rate; CI, confidence interval; ESRD, end-stage renal disease; KT, kidney transplantation. Received 16 November 2011, revised 21 May 2012 and accepted for publication 15 June 2012 Introduction For many patients with end-stage renal disease (ESRD), kidney transplant (KT) offers improved survival and quality of life compared to dialysis (1 5). However, many patients with excellent predicted postkt survival (based on demographic and clinical characteristics) are never listed for KT (6,7). The nephrologist is often the first to educate patients about KT and direct potentially eligible patients to a transplant center for evaluation (8,9). Recent national data indicate that 30.1% of patients were not informed about KT by their nephrologists at ESRD-onset, and the most common reason reported by nephrologists was that the patient was simply unassessed, meaning that their eligibility for transplant had not yet been evaluated; furthermore, unassessed patients had a 46% lower rate of access to KT compared to similar patients who were informed (10). There may be additional barriers to the provision of timely and comprehensive transplant education. Nephrologists must provide counsel for numerous other issues related to ESRD-onset, and given limited time may wisely choose to focus on more immediate concerns. Medicare reimburses nephrologists for up to six education sessions; however, these must be used to cover all aspects of ESRD management, and thus KT education may require time beyond these reimbursed sessions. Furthermore, many patients are not eligible for Medicare coverage until several months after ESRD-onset (11). These barriers to providing KT education might disproportionately affect for-profit dialysis centers. For-profit centers must generate a profit and pay taxes while providing equivalent care at the same reimbursement rates as nonprofit centers (12). A previous study showed that for-profit centers have lower staffing levels per dialysis treatment compared with nonprofit centers (13), adding further challenges to the timely provision of KT education. Patients at for-profit centers have less access to KT compared to their counterparts at nonprofit centers (14,15); we hypothesized that this difference might be partially explained by disparities in the quality of KT education. The goals of our study were to understand, on a national level, nephrologists attitudes and practices regarding KT education, and to compare attitudes and practices between nephrologists at for-profit and those at nonprofit dialysis centers. 3104

2 Education at For-Profit Dialysis Centers Methods Study design and response Between June 3 and October 18, 2010, we sent electronic surveys to addresses that we could find through the internet (through association websites, PubMed and other journal listings and other internet sources) that might belong to nephrologists. We ed the survey for the first time on June 3, 2010, with three subsequent reminder s, using Survey Monkey. Nephrologists currently in practice in the United States were eligible, of which the AMA reports 7740 currently actively involved in patient care (16). However, it is unclear how many of our addresses were no longer valid (181 were returned as invalid, but many mail servers do not provide this information to senders and instead just ignore the s) or belonged to nonnephrologists such as researchers, students, physicians in specialties other than nephrology and other clinical personnel (17 responded that they were ineligible, but 5092 never responded at all, so eligibility could not be determined). As such, many of those included in our initial mailing were likely ineligible, so our reported response rate of 15% represents a minimum and is likely higher. Survey development The survey was designed based on a combination of a review of the literature on ESRD and KT education and the expertise of nephrologists who practice in both for-profit and nonprofit settings. Ten nephrologists pilot tested an initial draft of the survey; their suggestions were incorporated into the final draft that was distributed nationally. Survey content Each provider was asked questions about their center and patient demographics, their attitudes toward reimbursement for KT education and the proportion of their patients they educated about KT. For the following topics regarding KT education, providers were asked to indicate (1) what they thought was ideal and (2) what they actually did in practice: time spent with each patient, education format (one-on-one, written literature/brochures, videos, patient panels, group sessions), providers responsible for informing patients about KT (nephrologist, primary care doctor, nurse or nurse practitioner, transplant center staff), and stage of chronic kidney disease (CKD) when education was provided. Providers also rated 13 KT topics on a 5-point scale regarding how often they discussed each topic during a KT education session. Time spent and depth and breadth of kidney transplant education We used a modified Poisson approach (briefly, a Poisson regression implemented through a generalized linear model with a robust error variance and a modified distribution to account for a binary outcome) as previously described (17) to examine whether spending >20 min on KT education was associated with greater depth and breadth of counseling. Measures of depth and breadth included (1) having one-on-one conversations with patients about KT, (2) discussing KT with patients more than once, (3) discussing KT with all patients versus selected patients, (4) involving family in KT education, (5) giving KT education at CKD stage 4, and (6) covering more topics. Factors associated with greater time spent on kidney transplant education Univariate and multivariate generalized linear models were built as described above and used to identify provider and center-level factors associated with spending >20 min on KT education. Factors analyzed were profit-status of nephrologists center, years in practice, area of nephrology, affiliation with university hospital offering KT and volume of practice; additionally, the proportion of the nephrologist s patients that were African American, over 65, insured through Medicare or Medicaid, perceived by the nephrologist to be eligible for KT, and initiated KT discussion were also analyzed. All factors either statistically significant in univariate analysis or hypothesized to be strongly associated with our outcome were included in the final multivariable model. Factors associated with greater depth and breadth of kidney transplant education Multivariate ordinal logistic regression models were built to examine center characteristics associated with each of the following outcomes: (1) frequency of family involvement in KT education, (2) proportion of patients considered eligible for KT, (3) proportion of patients reported to initiate discussion about KT, (4) proportion of patients given KT education, (5) number of topics covered in KT education and (6) frequency of giving KT education at CKD stage 4. Factors of interest were profit-status of nephrologists center, center volume, proportion of the nephrologist s patients that were African American, over 65 and insured through Medicare or Medicaid. All models were also adjusted for provider affiliation with a KT hospital, years in practice and involvement in transplant nephrology. Results Study population Of 906 survey respondents, 47 states were represented, with 30.9% female respondents (vs. 34.2% nationally), 58.7% Caucasian (vs. 57.6%), 24.3% Asian/Pacific Islander (vs. 26.7%), 3.4% African American/Black (vs. 5.6%), and 4.9% Hispanic (vs. 7.1%) (Table 1) (16). The majority (59.6%) of our respondents were over the age of 40 (age was assessed categorically in our study; mean age nationally is 46.4) (16). 31.7% of respondents were in practice 5 years or less while 23.7% had been in practice >25 years. The majority had hemodialysis or outpatient nephrology practices and 57.8% practiced exclusively at a for-profit center; however, 30.5% of respondents were involved in transplant nephrology and 14.8% identified as mostly research. Of respondents, 31% reported that >50% of their patients were African American, 80.6% that >50% of their patients had Medicare or Medicaid as primary payers and 40.4% that >50% of their patients were over age of 65. Duration of kidney transplant education A total of 81% of respondents reported that >20 min was an ideal amount of time to spend on transplant education, but only 43% reported actually spending >20 min (Figure 1A). At the individual level, 61.4% reported that the actual time they spent on KT education was less than what they considered to be the ideal amount of time, 36.9% reported actually spending what they considered ideal time, and 1.7% reported spending more time than what they considered ideal (Figure 1B). Format of kidney transplant education Nephrologists who spent >20 min on KT education were more likely to discuss a greater number of topics (RR 1.38, American Journal of Transplantation 2012; 12:

3 Balhara et al. Table 1: Demographic and practice characteristics of survey respondents All Nonprofit (42.2%) For-profit (57.8%) p-value Provider characteristics Age (years) > Female Race Caucasian Asian/Pacific Islander African American or Black Hispanic Other Years in practice 5orless > Area of nephrology Hemodialysis < Peritoneal dialysis Outpatient Nephrology Involved w/ transplant nephrology < Mostly research < Practice characteristics Affiliated with transplant hospital < Volume (mean) < Urban location < % of patients African American > % of patients with Medicare/Medicaid > % of patients over the age of 65 < > Percentages do not add up to 100% since respondents were allowed to choose more than one option. 95% CI , p < 0.001) (Table 2), more likely to have one-on-one conversations (RR 1.45, 95% CI , p < 0.001), more likely to discuss KT more than once (RR 1.33, 95% CI: , p < 0.001), more likely to have a conversation about KT with all their patients as opposed to only selected patients (RR 1.53, 95% CI , p = 0.001), more frequently involved the family in KT education (RR 1.53, 95% CI: , p < 0.001), and more frequently initiated KT education at CKD stage 4 (RR 1.16, 95% CI , p = 0.005). Characteristics of providers at for-profit and nonprofit centers Providers at for-profit centers were similar in age, gender, race and years in practice to those at nonprofit centers, but were more likely to practice in hemodialysis or 3106 American Journal of Transplantation 2012; 12:

4 Education at For-Profit Dialysis Centers Figure 1: Ideal and actual time spent on KT education, (A) among the entire cohort and (B) individual-level differences. Table 2: Association between spending >20 minutes on KT counseling and depth and breadth of education provided RR (95% CI) Factor For >20 min p-value Greater depth of counseling ( ) <0.001 Have one-on-one 1.45 ( ) <0.001 conversations Discuss KT repeatedly 1.33 ( ) <0.001 KT counseling for ALL patients 1.53 ( ) Frequency of involving family 1.53 ( ) <0.001 in KT counseling 2 Frequency of providing KT 1.16 ( ) counseling at CKD stage 4 3 RR = relative rate. Quartile of emphasis score. 2 Categorized as seldom/never, sometimes, very often, and always. 3 Categorized as none/very few patients, some, most and all patients. outpatient nephrology and less likely to be involved in transplant nephrology or associated with a university hospital performing transplants (Table 1). For-profit providers reported a higher volume of patients (mean vs. 68.6, p < 0.001), a lower percentage of patients with Medicare/Medicaid as the primary payer (p = 0.014), and a higher percentage of patients over the age of 65 (p < 0.001). Attitudes of providers at for-profit and nonprofit centers Providers at for-profit centers were less likely to report that >20 min was an ideal amount of time to spend on KT education (73.9% vs. 82.5%, p = 0.03, Table 3), less likely to believe that involving family and close friends is important (51.9% vs. 67.6%, p = 0.001) and more likely to cite lack of reimbursement as a reason for not spending an ideal amount of time on KT education (30.0% vs. 18.9%, p = 0.02). Providers at for-profit and nonprofit centers reported at similar rates that one-on-one conversations are the ideal format and that CKD stage 4 is the ideal time to first provide KT education. Factors associated with greater time spent on kidney transplant education In univariable analysis, providers at for-profit centers were 27% less likely to spend >20 min on KT education (95% CI American Journal of Transplantation 2012; 12:

5 Balhara et al. Table 3: Attitudes toward KT education, comparing nephrologists from nonprofit and for-profit centers Nonprofit For-profit p-value Attitudes toward KT education >20 min is the ideal time 82.5% 73.9% 0.03 to spend One-on-one conversations 68.5% 75.0% 0.1 are the ideal format Involving family and close 67.6% 51.9% friends is very important Theidealtimetofirst providektinfoisat diagnosis with CKD stage 4 not yet on dialysis 64.2% 71.7% 0.1 Reasons for not spending an ideal amount of time Not enough time available 89.5% 80.9% 0.02 Time not reimbursed by 18.9% 30.0% 0.02 insurance Lack of patient interest 8.5% 10.0% 0.6 Among those who did not spend what they considered to be an ideal amount of time on kidney transplant education , p = 0.006) (Table 4). Also, having >50% of patientsafrican American,>50% with Medicare or Medicaid insurance, or >50% of patients over age 65 was associated with spending less time on KT education. After adjusting for provider and center characteristics, the for-profit disparity was attenuated but not eliminated (arr 0.89, 95% CI , p = 0.03); being in practice longer (arr 1.06, 95% CI: , p < 0.001) and having involvement in transplant nephrology (arr 1.22, 95% CI: , p < 0.001) were also independently associated with spending >20 min on KT education. Factors associated with depth and breadth of kidney transplant education Even after adjusting for a number of important differences between providers at for-profit and nonprofit centers, those at for-profit centers involved family and close friends in the KT education process less frequently (arr 0.57, 95%CI , p = 0.008), considered a lower percentage of their patients eligible for KT (arr 0.45, 95% CI , p < 0.001), were less likely to report that their patients initiated discussions about KT (arr 0.58, 95% CI: , p = 0.01), and counseled a lower percentage of their patients about KT (arr 0.59, 95% CI: , p = 0.03) (Table 5). Providers from higher volume centers were less likely to involve family in KT counseling, considered a lower percentage of patients eligible for KT and were less likely to inform patients about KT when they were in CKD stage 4. Providers who reported that >50% of their patients were African American were less likely to involve family in KT counseling (arr 0.44, 95% CI: , p < 0.001). Discussion In this national study of 906 nephrologists, we found that the majority of providers spent less time on KT education than they believed to be ideal and that those who spent >20 min on KT education covered more topics, had more one on one conversations, were more likely to involve the patient s family and were more likely to initiate KT education early during CKD stage 4. Providers at for-profit centers were less likely to spend >20 min on KT education, involve the patient s family, educate patients about KT more than once, report that their patients initiated KT discussions, or consider their patients eligible for KT. Previous studies have shown that patients at for-profit centers have lower access to KT than their counterparts at nonprofit centers (14,15); it is possible that less comprehensive KT education is a mechanism for this disparity. Our findings are unlikely due to differences in the patient population, as previous studies have shown for-profit and nonprofit centers to be similar in that regard (14) and this lack of clinically relevant differences was consistent in the self-described patient populations of our respondents. Adjusting for patient volume, which was significantly higher at for-profit centers, as well as other center and provider characteristics, attenuated but did not eliminate the disparity in time spent on KT education. It is possible that differences in time spent on KT education are explained by selection at the level of the nephrologist, where those giving less comprehensive KT education are more likely to choose to work in a for-profit center. However, providers at for-profit centers were significantly more likely to cite lack of reimbursement as a reason for spending less than an ideal amount of time on KT education, suggesting providers at these centers might be differentially affected by financial pressures. Medicare currently reimburses providers for up to six education sessions; however, these must be used to counsel patients about myriad ESRD-related issues, of which KT is only one component (11). Younger patients are often not eligible for Medicare until several months after ESRD onset, which might result in a delay in KT education: for patients without Medicare coverage, KT education may not be reimbursed. Given that KT is a more cost-effective form of renal replacement than dialysis for many patients (18), the efficacy of financial incentives for KT education warrants further study. It is important to note that, while providers at for-profit centers were less likely to spend >20 min on KT education, the majority of providers from both types of centers reported spending less time than they personally believed to be ideal, and there was wide variation between providers in both ideal and actual time spent. This variation might result from a lack of national policies outlining the optimal timing, content and 3108 American Journal of Transplantation 2012; 12:

6 Table 4: Factors associated with spending >20 minutes on KT education (patient and provider characteristics) Education at For-Profit Dialysis Centers Univariate >20 min Multivariate >20 min RR (95% CI) p-value RR (95% CI) p-value Provider/practice characteristics For-profit practice 0.73 ( ) ( ) 0.03 Years in practice 1.14 ( ) < ( ) < Affiliated with transplant hospital 1.10 ( ) ( ) Transplant nephrologist 1.74 ( ) < ( ) < Volume of practice ( ) < ( ) 0.03 Patient population >50% African American 0.78 ( ) ( ) 0.05 >50% with Medicare/Medicaid 0.76 ( ) ( ) 0.1 >50% over age ( ) ( ) 0.05 % Considered Eligible for KT ( ) < ( ) 0.1 % Reported to initiate discussion ( ) ( ) 0.5 RR = relative. 1 Categorized as <25, 25 49, 50 99, , and 200 or more patients. 2 Categorized as 40% or less, 41 50%, 51 70% and > 70% of patients. 3 Categorized as 20% or less, 41 50%, and > 50% of patients. Table 5: Multivariate ordinal logistic regression models to identify factors associated with family involvement, increased perception patient eligibility and initiative and depth and breadth of KT education Factor Frequency of family involvement in KT counseling 1 % of patients considered eligible for KT 2 % of patients reported to initiate discussion about KT 3 % of patients given KT counseling 4 Frequency of giving KT counseling at CKD-IV 6 Greater depth of counseling 3 OR OR OR OR OR OR (95% CI) (95% CI) (95% CI) (95% CI) (95% CI) (95% CI) For-profit ( ) ( ) ( ) ( ) ( ) ( ) Volume of practice ( ) ( ) ( ) ( ) ( ) ( ) >50% African American ( ) ( ) ( ) ( ) ( ) ( ) >50% on Medicare/ Medicaid ( ) ( ) ( ) ( ) ( ) ( ) >50% over age ( ) ( ) ( ) ( ) ( ) ( ) Each column is a separate ordered logistic regression model with outcomes shown across the top row. All models were adjusted for the covariates in the first column and also for provider affiliation with university hospital offering KT, provider years in practice and practicing as transplant nephrologist. BOLD indicates the result was statistically significant, defined as p < Categorized as seldom/never, sometimes, very often and always. 2 Categorized as 40% or less, 41 50%, 51 70% and > 70% of patients. 3 Categorized as 20% or less, 41 50% and > 50% of patients. 4 50% or less, 51 70% and > 70% of patients. 5 Quartile of emphasis score. 6 Categorized as none/very few patients, some, most and all patients. frequency of KT education, as well as which patients should receive it. Our study is limited in that practices were self-reported and as such subject to recall and social desirability bias, although the latter is less likely in an anonymous electronic survey. Because we lacked data on transplant outcomes for the patients of the nephrologists we surveyed, we were unable to analyze causal associations between quality of transplant education and access to transplant, although we were able to analyze associations between time spent educating and various metrics of education quality. We cannot be certain that our results are generalizable to nephrologists nationally, as respondents may be different from nonrespondents; however, (1) the demographics of our respondents are similar to those reported by the American Medical Association (AMA) (16), and (2) even in the setting of selection or nonresponse bias, an interaction (effect modification) between characteristics associated with participation in the study and the for-profit/nonprofit effect American Journal of Transplantation 2012; 12:

7 Balhara et al. would have to exist for our primary inferences to become biased, which we believe to be unlikely. Finally, we captured for-profit and nonprofit as a binary indicator without further details about each center s financial structure, and as a result were unable to account for variation that might exist within these groups. Nephrologists at for-profit centers report providing less comprehensive transplant education to a lower percentage of their patients; this finding that might partially explain previously identified disparities in access to KT for patients at for-profit centers. Development of national policies to guide the provision of KT education might help facilitate equity and quality. Acknowledgments We would like to sincerely thank all 906 nephrologists who took the time to participate in this survey as well as those involved in the formative phase of study development. Disclosure The authors of this manuscript have no conflicts of interest to disclose as described by the American Journal of Transplantation. References 1. Cetingok M, Winsett RP, Hathaway DK. A comparative study of quality of life among the age groups of kidney transplant recipients. Prog Transplant 2004; 14: Wolfe RA, Ashby VB, Milford EL, et al. Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant. N Engl J Med 1999; 341: Landreneau K, Lee K, Landreneau MD. Quality of life in patients undergoing hemodialysis and renal transplantation a metaanalytic review. Nephrol Nurs J 2010; 37: Maglakelidze N, Pantsulaia T, Tchokhonelidze I, Managadze L, Chkhotua A. Assessment of health-related quality of life in renal transplant recipients and dialysis patients. Transplant Proc 2011; 43: Tomasz W, Piotr S. A trial of objective comparison of quality of life between chronic renal failure patients treated with hemodialysis and renal transplantation. Ann Transplant 2003; 8: Schold JD, Srinivas TR, Kayler LK, Meier-Kriesche HU. The overlapping risk profile between dialysis patients listed and not listed for renal transplantation. Am J Transplant 2008; 8: Grams ME, Kucirka LM, Hanrahan CF, Montgomery RA, Massie AB, Segev DL. Candidacy for kidney transplantation of older adults. J Am Geriat Soc 2012; 60: Epstein AM, Ayanian JZ, Keogh JH, et al. Racial disparities in access to renal transplantation clinically appropriate or due to underuse or overuse? N Engl J Med 2000; 343: , 2 p preceding Scandling JD. Kidney transplant candidate evaluation. Semin Dial 2005; 18: Kucirka LM, Grams ME, Balhara KS, Jaar BG, Segev DL. Am J Transplant 2012; 12: Health Care Financing Administration Medicare and Medicaid; provider agreements: Redesignation and rewrite of Medicare regulations; effective dates; effect of change in ownership. Final rule with comment period. Fed Regist 1980; 45(67 Pt 2): Nudelman PM, Andrews LM. The value added of not-for-profit health plans. N Engl J Med 1996; 334: Griffiths RI, Powe NR, Gaskin DJ, Anderson GF, de Lissovoy GV, Whleton PK. The production of dialysis by for-profit versus notfor-profit freestanding renal dialysis facilities. Health Services Research 1994; 29(4): Garg PP, Frick KD, Diener-West M, Powe NR. Effect of the ownership of dialysis facilities on patients survival and referral for transplantation. N Engl J Med 1999; 341: Garg PP, Powe NR. Profit-making in the treatment of chronic kidney disease: Truth and consequences. Semin Dial 2001; 14: Smart, DR. Physician Characteristics and Distribution in the US. Chicago, IL: American Medical Association; 2012: 18, 25, 31 32, Zou G. A modified poisson regression approach to prospective studies with binary data. Am J Epidemiol 2004; 159: Finkelstein FO, Story K, Firanek C, et al. Health-related quality of life and hemoglobin levels in chronic kidney disease patients. CJASN 2009; 4: American Journal of Transplantation 2012; 12: