Table of Contents

Lessons from registries

J NEPHROL 2003; 16: 40-48

Body mass index and enrollment on the renal transplant waiting list in the United States

Kevin C. Abbott¹, Christopher W. Glanton¹, Lawrence Y. Agodoa² - ¹Nephrology Service, Walter Reed Army Medical Center, Washington, DC, and Uniformed Services University of the Health Sciences, Bethesda, MD    ²NIDDK, NIH, Bethesda, MD - USA

ABSTRACT: Background: Previous studies of body mass index (BMI) and enrollment on the renal transplant waiting list have not analyzed a national population of chronic dialysis patients.
Methods: 161,265 patients in the United States Renal Data System (USRDS) initiated on end-stage renal disease (ESRD) therapy between 1 April 1995 and 30 June 1997 who had data sufficient to calculate BMI were analyzed in an historical cohort study. Cox Regression analysis was used to model the association of BMI and rates of listing for renal transplantation, censored for death and receipt of renal transplant, and adjusted for demographics, comorbidities in the Medical Evidence Form (2728) and in comparison with patient survival.
Results: In univariate analysis, only patients with BMI <21.3 kg/m² had a statistically significant lower rate of listing compared to patients with BMI 24.5-28.6 kg/m² (6.1 vs. 7.5/100 person years). In Cox Regression analysis, patients with BMI <21.3 kg/m² had a 18% lower adjusted rate of listing and a 38% lower rate of survival, and patients with BMI >=24.5-28.7 had an 11% higher adjusted rate of listing and no significant difference in adjusted survival compared with patients with BMI>=28.7 kg/m². Caucasian females were disproportionately affected by high BMI.
Conclusions: Among ESRD patients, lower BMI was independently associated with reduced adjusted rates of listing. High BMI affected rates of listing disproportionately in caucasian females.

Key words: Body mass index, Obesity, Renal transplantation, Waiting list, Female, Caucasian, African American, Diabetes, Age

Introduction

Obesity, commonly defined as body mass index (BMI) >=30 kg/m², is widely considered a relative contraindication to listing for renal transplantation (1-3). Previous analyses of a sample of the USRDS population showed that obese candidates are less likely to receive transplants than non-obese candidates (4). The finding that renal transplant recipients at either extremes of BMI have increased risk of graft loss and mortality (5) might be taken as support for current policy. However, obesity has also been shown to be associated with improved survival among patients on maintenance dialysis, compared to patients who are non-obese (6- 8). Previous analyses of BMI and rates of listing for transplant have not adjusted for baseline comorbid conditions or the effect of BMI on relative patient survival. Kutner and Zhang (6) have found that the relationship between BMI and survival in this population may be more complicated than previously appreciated: among end-stage renal disease (ESRD) patients, higher levels of BMI (obesity) were associated with improved survival in all subgroups of gender and race except for caucasian females, and have since been confirmed. (9)
Given this disparity, it is possible that BMI may not be applied uniformly in selecting renal transplant candidates, or that BMI is associated with different rates of mortality or complications in different subgroups. Females (10, 11) and African Americans (12, 13) had lower adjusted rates of listing for renal transplantation adjusted for BMI in a random sample of the USRDS population. However, due to sample size limitations, potential interactions between race, gender and BMI were not fully explored in these previous studies. This is relevant since females have higher BMI than males and African Americans have higher BMI than other races, particularly caucasians (14). Identifying variation in the association of BMI with enrollment on the renal transplant waiting list, if present, may allow targeted research to facilitate more equitable access to renal transplantation.
Therefore, to better characterize the association of BMI with enrollment on the renal transplant waiting list, we analyzed data from the 1999 USRDS database in an historical cohort study. Our null hypothesis was that BMI had no significant relationship with listing for renal transplantation in the U.S. ESRD population, and had no significant interactions with demographic subgroups.

Methods

We analyzed a national registry (the 1999 USRDS) in an historical cohort study of the association of BMI with listing for renal transplantation at presentation to ESRD from 1 April 1995 to 30 June 1997. The variables included in the USRDS standard analysis files (SAF's), as well as data collection methods and validation studies, are listed at the USRDS website (www.usrds.org), under 'Researcher's Guide to the USRDS Database', Section E, 'Contents of all the SAF's', and published in the USRDS. Hospitalization and mortality data may be incomplete during the first 90 days after dialysis initiation for patients younger than 65.
The files SAF.PATIENTS were used as the primary data set, including cause of renal disease (PDIS) and cause and date of patient death. SAF.MEDEVID was used for additional information coded in the CMMS (formerly HCFA) medical evidence form (2728) starting with a sample of ESRD patients prior to April 1995 and universal afterward, and has been validated for use in research (15). SAF.RXHIST was used to obtain follow-up dates. The file SAF.TXWAIT contains the date in which the patients of the above cohort were first placed on the transplant waiting list. Files were merged using unique patient identifiers. In contrast to previous studies, we did not exclude patients who may have received living donor transplants, due to recent increases in living related donation (16) and our desire to make the study as representative as possible. Neither did we exclude children, since the large size of the study population enabled adequate adjustment for age, and children have been included in recent studies of enrollment on the renal transplant waiting list (11). Details on anthropometric measurements or nutritional parameters other than serum albumin were unavailable. The USRDS researcher's agreement specifically prohibits patient contact or chart review, or analysis of center specific data.
All analyses were performed using SPSS 9.0 ^TM (SPSS, Inc., Chicago, IL). Files were merged and converted to SPSS files using DBMS/Copy (Conceptual Software, Houston, TX). Statistical significance was defined as p<0.01. Univariate analysis was performed with Chi-square testing for categorical variables and Student's t-test for continuous variables. Variables with p<0.10 in univariate analysis for a relationship with elevated BMI were entered into multivariable analysis as covariates. Continuous variables were examined for outliers, and values >=3 SD from the mean were removed from analysis with the exception of height and weight, since children were also included in the study. Outliers were removed from BMI after calculation, as above.
Stepwise Cox regression analysis compared the rate of wait-listing for all ESRD patients with valid BMI. Analysis was based on quartiles of BMI, also controlling for race, age, gender, year of first dialysis session, cause of end-stage renal disease (diabetes or glomerulonephritis), and additional variables from the medical evidence form, including diabetes and hypertension as comorbidities, distinct from causes of ESRD, as the independent variables. ESRD network (geographical regions of the United States used to administer ESRD care and research, http://www.esrdnetworks.org/) was also used as a variable for adjustment. We reported only the p values for this variable in our analysis. Because the effect of body size has previously been shown to be independent of dialysis adequacy (17), and because indices of dialysis adequacy were not available for the entire population of dialysis patients, dialysis adequacy was not assessed in this study. Violation of the proportional hazards assumption for each covariate was tested in Kaplan-Meier analysis.
Survival time for time to transplant listing was calculated as the time from the date of the first dialysis session until the date of first listing for transplant. Patients were censored at death, receipt of renal transplantation or latest available follow-up date. We censored patients upon receipt of renal transplantation because of the different association of BMI with mortality after transplantation vs. before (5). We did not remove patients from the category of listing for transplant if they were removed from the waiting list at a later time, or after renal transplantation, in intent to treat fashion. To test the assumption that ESRD patients in particular quartiles of BMI had higher mortality before listing for renal transplantation, and therefore did not survive to be listed for renal transplantation, Cox regression analysis of patient mortality of ESRD patients and patients on the renal transplant waiting list was performed with the same covariates above, with end points of patient death or most recent date of follow-up.
Because of the large number of missing/questionable serum albumin levels, analyses were run both assigning missing values the average value (this applied primarily to serum albumin), and by running analysis strictly limited to patients with complete information for every variable.
Since BMI may have different associations in children, patients age ¾15 years were also analyzed separately. Analysis was also performed excluding recipients of living donor kidney transplants.

Results

Of 171,218 patients who initiated ESRD therapy in the USRDS database from 1 April 1995 to 30 June 1997, 161,625 patients (94%) had sufficient information from the medical evidence form (2728) to calculate BMI, of whom 23,237 had dates of placement on the renal transplant waiting list, of whom 4087 had dates of listing prior to 1 April 1995, leaving 19,150 patients listed for transplant during the study period. The most recent follow-up date was 31 July 1998. The most recent date of listing was 6/30/98. Patients with missing data for either height or weight were younger (59.6±16.9 vs. 61.0±16.4 years, p<0.01 by student's t-test), less likely to be diabetic (39% vs. 43%, p<0.01 by Chi Square), and more likely to be African American (30% vs. 29%, P<0.01 by Chi Square) than those with complete height and weight. There were no significant differences in gender or year of first ESRD treatment. Table I shows descriptive statistics of the study population, which were comparable to previous USRDS reports. BMI was distributed normally in the study population, with outliers both above and below 3 SD from the mean. The variables with the largest numbers of missing values were HIV status and serum albumin, followed by hematocrit (after outliers were excluded). Table I also shows demographic factors and comorbidity percentages as distributed by quartile of BMI.
Unadjusted rates of listing for renal transplantation are shown in Table II. As shown, patients in the lowest quartile of BMI had the lowest rate of listing for renal transplantation. The mean BMI of patients placed on the renal transplant waiting list was higher than for those not listed (25.87±5.81 vs. 25.40±6.17 kg/m², p<0.01 by student's t-test). Of patients listed for renal transplantation, 22.5% had BMI >=30 kg/m² vs. 19.7% of those not listed (p<0.001 by Chi Square). Of patients with BMI >=30 kg/m², 13% were enrolled on the waiting list during the study, compared with 11.8% for the entire study population (p<0.01 by Chi Square). However, patients with BMI >=30 kg/m² were younger (58.1±13.8 vs. 61.8±16.8 years, p<0.001 by student's t-test) and more likely African American (36.1% vs. 27.6%), female (57.3% vs. 44.1%) and diabetic (57.1% vs. 39.7%) compared to non-obese ESRD patients (p<0.01 by Chi Square for all comparisons), consistent with the known demographics of obesity in the general population (14).
Among patients who eventually received renal transplants during the study period, 7178 (93.3%) of cadaveric kidney recipients were listed upon receipt of transplantation, while 3061 (42.8%) of living donor kidney recipients were listed upon receipt of transplantation.
Table III shows results of Cox Regression analysis of factors associated with time to listing for renal transplantation for the entire study population. BMI had a significant association with the rate of listing for renal transplantation in both univariate and multivariate analysis. Consistent with previous studies, females and African Americans had lower rates of listing for renal transplantation, which persisted even after adjustment for comorbidity and ESRD network. Patients with comorbid conditions were less likely to be listed. The only term that demonstrated qualitative confounding was diabetes, which had a negative association in univariate analysis but a positive association in multivariate analysis. Figure 1 shows the relationship between rate of listing for renal transplantation and the adjusted rates of survival by quartile of BMI, in which the adjusted rate of listing and the adjusted rate of survival were lowest in patients in the lowest quartile of BMI. Patients in the third quartile of BMI had a significantly higher adjusted rate of listing, with no significant difference in survival compared to patients in the highest quartile of BMI. Because more than 50% of recipients of living donor renal transplants were not enrolled on the renal transplant waiting list, analysis was also performed excluding recipients of living donor renal transplants (N=5355). However, results were similar to those of Table III and Figures 1-3.
There were significant interactions between quartiles of BMI and several other terms (bottom of Tab. III, "Interaction Terms"), the most pronounced of which was with gender. The only significant higher order interaction was between BMI, race and gender, which is depicted in Figures 2 and 3. The primary impact was on Caucasian females. Among Caucasian males (Fig. 2), the relationship between BMI and the rate of listing was similar to that of African American males (not shown), although the distinction of higher quartiles from the lowest quartile of BMI was greater in caucasian males. Among African American females (also not shown), the sequence of BMI quartiles 3 and 4 was switched, but patients in the lowest quartile of BMI still had the lowest rates of listing. Among caucasian females (Fig. 3), the pattern was most distinct and narrowly distributed. This was the only category in which patients in the lowest and highest quartiles of BMI had the lowest rates of listing for transplantation, virtually indistinguishable from each other. The pattern of time to listing for males and females was not different even for analysis restricted to the cohort of patients who survived until the end of the study. A Cox regression analysis of patient mortality showed a similar relationship between BMI and patient mortality in this subgroup. Results limited to patients with complete information in every variable were similar (not shown except for the N of the sample, Tab. III).
Age 15 or younger as a categorical variable was not significantly associated with mortality or listing, independent of quartiles of age. Results were substantially different when limited to analysis of patients aged 15 years or younger (N=1130), however. In this analysis, patients in the lowest quartile of BMI had the highest rate of listing, followed in order by the second, third and fourth quartiles of BMI, although BMI itself was not statistically significant. Subgroup analysis limited to caucasian males and caucasian females, respectively, showed that caucasian males in the first and second quartiles of BMI had the highest rate of listing, while caucasian females in the fourth and third quartiles of BMI had the highest rate of listing, although no results were statistically significant.
According to quartiles of age, the greatest separation for the time to listing for transplant by quartiles of BMI occurred in the highest three quartiles of age, and was narrowest in the lowest quartile of age (not shown). This is in contrast to the relationship for race between time to transplant listing found by Garg et al (13), in which the greatest disparity in listing for transplant between blacks and whites occurred in the younger age group.

Fig. 1 - Plot of adjusted rate of listing for renal transplantation, censored for death or receipt of renal transplantation (adjusted rate of listing for renal transplantation, left column) in cox regression at mean of all covariates listed in methods section, and inverse of adjusted hazard ratio for mortality (AHR, right column) in cox regression (the inverse given for comparability with rates of listing, corresponds to the adjusted hazard for "survival"), U.S. ESRD patients 1 April 1995-30 June 1997 with valid height and weight, Total N=161,625 (missing values for serum albumin and hematocrit assigned to average values as in methods section). *= p<0.05 by cox regression for adjusted rate of listing for renal transplantation vs. highest quartile of BMI. **=p<0.05 by cox regression for adjusted survival vs. highest quartile of BMI. As shown, patients in the first quartile of BMI had significantly lower adjusted rates of listing for renal transplantation while patients in the third quartile had significantly higher adjusted rates of listing for renal transplantation compared to patients in the highest quartile of BMI. Patients in the first two quartiles of BMI had significantly lower adjusted rates of survival compared with patients in the highest quartile of BMI.

Fig. 2 - Caucasian males with ESRD, 1 April 1995-30 June 1997, with valid BMI, cox regression plot of time to listing for renal transplantation by BMI, at the mean of all covariates listed in the methods section. N=57,017.
Patients in the lowest quartile of BMI had significantly longer times to listing for renal transplantation compared with both the second, third and fourth quartiles.

Fig. 3 - Caucasian females with ESRD, 1 April 1995-30 June 1997, with valid BMI, cox regression plot of time to listing for renal transplantation by BMI, at the mean of all covariates listed in the methods section. N=44,856. In contrast to Caucasian males or African Americans of either gender, patients in the lowest and highest quartiles of BMI had significantly longer times to listing for renal transplantation compared with both the second and third quartiles.

TABLE I - FACTORS ASSESSED IN ESRD PATIENTS, 1 APRIL 1995-30 JUNE 1997 WITH VALID HEIGHT AND WEIGHT

Data presented as % (N) or Mean±SD, unless otherwise specified, BMI=body mass index in kg/m²,
*=for continuous variables, this also included the percent missing after outliers (defined as >=2 SD above or below the mean) were excluded. For height and weight, no values were excluded due to the inclusion of children, and only outliers for BMI were excluded.
^ACondition at or in the ten years prior to presentation to ESRD.

TABLE II - UNADJUSTED RATES OF LISTING FOR RENAL TRANSPLANTATION AND SURVIVAL

  TABLE III - COX REGRESSION ANALYSIS OF FACTORS ASSOCIATED WITH RELATIVE RATE OF LISTING (RLT) FOR
RENAL TRANSPLANTATION, U.S. ESRD PATIENTS WITH VALID HEIGHT AND WEIGHT
1 APRIL 1995-30 JUNE 1997

Only variables significant in multivariate analysis (by Cox Regression, covariates as in methods section) shown except for BMI,
Hazard ratios for quartiles are given per higher quartile, BMI=Body mass index, kg/m², RLT=adjusted rate of listing for renal transplantation, 95% CI=95% confidence interval, NG = not given due to space limitations.

Discussion

The present study's finding that patients with the lowest quartiles of BMI were the least likely to be listed for renal transplantation is consistent with the relationship between BMI and mortality in patients with ESRD, most likely linked to poor nutrition and overall medical status (6, 7). Patients in the highest quartile of BMI had no statistically significant difference in rates of listing for renal transplantation or relative survival. A recent report documented that 52% of transplant programs screen patients perceived to be at high risk due to obesity, usually defined as >=30 kg/m² of body mass index (18). Our unadjusted analysis failed to show a substantially lower rate of listing for transplantation for patients with BMI >=30 kg/m², but the adjusted analysis showed that patients in the highest quartile of BMI had significantly lower rates of listing for transplant despite similar survival to patients in the third quartile of BMI (Tab. II). This illustrates the importance of correcting for other factors, since obese ESRD patients are often younger, more likely African American, female, and have fewer comorbidities than non-obese patients. The question of whether obese patients would benefit further from higher rates of listing for transplantation was not the subject of the present analysis. However, preliminary analysis has shown that renal transplantation is associated with a survival advantage in obese (>= 30 kg/m²) patients on the renal transplant waiting list (26).
Subgroup analysis disclosed an uneven impact of BMI on transplant listing. Caucasian females in the highest quartile of BMI had the lowest rate of transplant listing, in contrast to other gender/race categories. This is very similar to the relationship between BMI and mortality in Caucasian female dialysis patients depicted by Kutner and Zhang (6). The reason why caucasian females with ESRD who have high BMI are at disproportionately increased risk of mortality is not clear, but seems to be primarily due to increased risk of infectious death, (9, and Glanton et al, in press, Ann Epidemiol) as suggested in previous reports by this institution (19-21). The persistence of this association even in analysis limited to patients who survived until the end of the study suggests this association may not be entirely related to decreased survival. Rather, this may be associated with lower rates of permanent access placement in women with ESRD, independent of BMI (22, 23) and may also relate to the finding that sepsis due to vascular access infection is significantly more common in women than men with ESRD (21). These results persisted even after exclusion of recipients of living donor transplants.
Our study was limited by the lack of complete data in many of the fields, particularly for height and weight to calculate BMI. Nevertheless, the study still captured almost 95% of all US ESRD patients during that period. The study was also limited by the inability to determine how patient weights changed after the initiation of dialysis, and therefore could not determine how many patients who were obese at presentation to dialysis were still obese at a later time, or those who became obese later. The independent association of the lowest quartile of BMI with lower rates of listing for renal transplant may indicate that the current version of the medical evidence form is insensitive to malnutrition (15). BMI has recognized limitations as an indicator of obesity and nutritional status, particularly in the elderly (24) and in females (25), but has nevertheless been widely used in medical literature. We could not determine if high mortality in certain subgroups led to lower rates of listing or whether lower rates of listing led to lower rates of transplantation, which may have resulted in higher rates of mortality. However, analysis limited to patients who survived until the end of the study still showed the same associations between BMI and listing for transplantation, implicating an association independent of survival. Our analysis only considered rates of first episodes of listing for renal transplantation, similar to the intent to treat approach of previous investigators (10), and thus did not assess multiple listing.
In conclusion, ESRD patients with low BMI have lower adjusted rates of listing for transplantation, even when censored for death. Rates of listing for renal transplantation appear congruent with patient survival. An exception was seen for Caucasian females, in whom those with the highest BMI had the lowest adjusted rate of listing for transplantation. These associations should be investigated in future studies.

The opinions are solely those of the authors and do not represent an endorsement by the Department of Defense or the National Institutes of Health. This is a U.S. Government work. There are no restrictions on its use.

Address for correspondence: Kevin C. Abbott, M.D. - 7 Rudis Way Gaithersburg, MD 20878, USA kevin.abbott@na.amedd.army.mil

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Received: March 08, 2002 Revised: September 05, 2002 Accepted: November 19, 2002

Copyright (c) 2003 Italian Society of Nephrology

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