Advertisement
American Journal of Kidney Diseases

Association of Citizenship Status With Kidney Transplantation in Medicaid Patients

Published:November 08, 2017DOI:https://doi.org/10.1053/j.ajkd.2017.08.014

      Background

      Although individuals classified as nonresident aliens, including undocumented immigrants, are entitled to receive emergency dialysis in the United States regardless of their ability to pay, most states do not provide them with subsidized care for maintenance dialysis or kidney transplantation. We explored whether nonresident aliens have similar outcomes to US citizens after receiving kidney transplants covered by Medicaid, a joint federal and state health insurance program.

      Study Design

      Retrospective observational cohort study.

      Setting & Participants

      All adult Medicaid patients in the US Renal Data System who received their first kidney transplant from 1990 to 2011.

      Predictor

      Citizenship status, categorized as US citizen, nonresident alien, or permanent resident.

      Outcome

      All-cause transplant loss.

      Measurements

      HRs and 95% CIs estimated by applying Cox proportional hazards frailty models with transplantation center as a random effect.

      Results

      Of 10,495 patients, 8,660 (82%) were US citizens, 1,489 (14%) were permanent residents, and 346 (3%) were nonresident aliens, whom we assumed were undocumented immigrants. Nonresident aliens were younger, healthier, receiving dialysis longer, and more likely to have had a living donor. 71% underwent transplantation in California, and 61% underwent transplantation after 2005. Nonresident aliens had a lower unadjusted risk for transplant loss compared with US citizens (HR, 0.48; 95% CI, 0.35-0.65). Results were attenuated but still significant when adjusted for demographics, comorbid conditions, dialysis, and transplant-related factors (HR, 0.67; 95% CI, 0.46-0.94).

      Limitations

      Citizenship status was self-reported, possible residual confounding.

      Conclusions

      Our study suggests that the select group of insured nonresident aliens who undergo transplantation with Medicaid do just as well as US citizens with Medicaid. Policymakers should consider expanding coverage for kidney transplantation in nonresident aliens, including undocumented immigrants, given the associated high-quality outcomes in these patients.

      Index Words

      Editorial, p. 157
      An estimated 6,000 undocumented immigrants in the United States have end-stage kidney disease, based on 2014 data.
      • Rodriguez R.A.
      Dialysis for undocumented immigrants in the United States.
      • Passel J.C.
      • Cohn D.
      Overall number of U.S. unauthorized immigrants holds steady since 2009.
      • Campbell G.A.
      • Sanoff S.
      • Rosner M.H.
      Care of the undocumented immigrant in the United States with ESRD.
      Although the United States provides life-sustaining maintenance dialysis for virtually all its citizens with end-stage kidney disease, care for undocumented immigrants is fragmented.
      • Rodriguez R.A.
      Dialysis for undocumented immigrants in the United States.
      Although some states extend the benefit of scheduled maintenance dialysis to undocumented immigrants, most states dialyze them only when their condition is acutely life-threatening, a situation under which federal funding may be used to cover costs.
      • Rodriguez R.A.
      Dialysis for undocumented immigrants in the United States.
      Access to kidney transplantation for this population is even more limited because there is no federal mandate to subsidize kidney transplantation for noncitizens.
      • Linden E.A.
      • Cano J.
      • Coritsidis G.N.
      Kidney transplantation in undocumented immigrants with ESRD: a policy whose time has come?.
      This is despite the fact that transplantation is a more cost-effective form of renal replacement therapy and provides better outcomes for patients with end-stage kidney disease.
      • Wolfe R.A.
      • Ashby V.B.
      • Milford E.L.
      • et al.
      Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant.
      • Schweitzer E.J.
      • Wiland A.
      • Evans D.
      • et al.
      The shrinking renal replacement therapy “break-even” point.
      • Purnell T.S.
      • Luo X.
      • Kucirka L.M.
      • et al.
      Reduced racial disparity in kidney transplant outcomes in the United States from 1990 to 2012.
      Although some states provide funding for kidney transplantation for this population, most undocumented immigrants must rely on either charitable donations or private insurance to cover the costs of this procedure, making it unfeasible for the vast majority of these patients.
      • Grubbs V.
      Undocumented immigrants and kidney transplant: costs and controversy.
      Little is known about the outcomes of undocumented immigrant recipients of kidney transplants. Critics have voiced concerns that undocumented immigrants would not do well because they are subject to deportation, which could disrupt the social and financial stability necessary for proper posttransplantation health care.
      • Bramstedt K.A.
      Supporting organ transplantation in non-resident aliens within limits.
      We hypothesized that undocumented immigrants would have similar outcomes to US citizens following kidney transplantation if they were equally insured. To test this, we analyzed a cohort of patients with Medicaid, a joint federal and state health insurance program for low-income patients, who received their first kidney transplant from 1990 through 2011. We compared the outcomes of presumed undocumented immigrants with those of US citizens.

      Methods

      Data Source and Study Population

      From the US Renal Data System (USRDS), a national database of virtually all patients with end-stage kidney disease, we identified all adult (aged ≥18 years) patients with end-stage kidney disease who received their first kidney transplant from January 1, 1990, through December 31, 2011 (Fig S1). We excluded patients who underwent transplantation after 2011 because the categories for recording citizenship status were changed in 2012 to a combination of US citizen/non–US citizen and US resident/non–US resident, such that undocumented immigrants would be indistinguishable from permanent residents (because both would be listed as non–US citizen/US resident).
      • Glazier A.K.
      • Danovitch G.M.
      • Delmonico F.L.
      Organ transplantation for nonresidents of the United States: a policy for transparency.
      By restricting the cohort to patients whose primary payer was Medicaid, we also minimized the inclusion of patients who traveled to the United States for the purpose of transplantation because it would be unlikely that such “transplant tourists” would qualify for Medicaid.

      Exposure and Outcomes

      The primary exposure of interest was recipient citizenship status, which was self-reported on the Transplant Candidate Registration form (US citizen vs resident alien vs nonresident alien). The 3-category exposure was used for all analyses. We considered resident aliens to be permanent residents or individuals who are allowed to live and work in the United States indefinitely. We assumed nonresident aliens to be undocumented immigrants.
      To assess the validity of the citizenship variable from the Transplant Candidate Registration form, we reviewed medical records of all patients covered by Medicaid who had received a kidney transplant from 2009 to 2011 at a single center to find their United Network for Organ Sharing (UNOS) registration number. For logistical reasons, we were unable to access records at other transplantation centers. Whereas US citizens and permanent residents are registered in UNOS using their social security numbers, nonresident aliens are given UNOS registration numbers beginning with 9FN. We also reviewed social work evaluations to determine whether patients had traveled to the United States for the purpose of receiving a transplant.
      For survival analyses, our primary outcome was all-cause transplant failure. We analyzed nonfatal transplant failure and all-cause mortality individually as secondary outcomes. We treated death as a competing event for nonfatal transplant failure. All outcomes we ascertained from the USRDS transplantation file.

      Patient Characteristics

      We obtained demographics, dialysis characteristics, comorbid conditions, transplant characteristics, and donor characteristics from the USRDS transplantation files. These data are derived from Organ Procurement and Transplantation Network candidates, recipients, donors, and histocompatibility files.

      Statistical Analysis

      We tabulated transplant recipient characteristics by citizenship status using frequency and percentage and mean ± standard deviation or median with interquartile range and compared the groups using analysis of variance or Kruskal-Wallis test for continuous variables and χ2 or Fisher exact test for categorical variables, as appropriate.
      We used Cox proportional hazards frailty models with transplantation center as a random effect to estimate the hazard ratio (HR) for all-cause transplant failure and all-cause mortality in nonresident aliens versus US citizens. In the presence of the competing event of death, we used cause-specific hazards frailty models with transplantation center as a random effect to estimate the cause-specific HRs for nonfatal transplant failure by treating the competing event as censoring. We defined the index date as the date of transplantation. Patients were censored after 5 years of follow-up or on end of study (January 1, 2012), whichever was earlier. All HRs were accompanied by their corresponding 95% confidence interval (CI).
      We created the following models: (1) unadjusted analysis (citizenship status only), (2) adjusted for demographics (age at transplantation, sex, and race/ethnicity), (3) model 2 plus dialysis factors (years on dialysis therapy pretransplantation and cause of kidney failure), (4) model 3 plus transplant factors (HLA antigen 0 mismatch [vs any mismatch], living [vs deceased] donor, and transplantation before 2000 [vs 2000 or after]), and (5) model 4 plus comorbid condition count (number of comorbid conditions a patient has).
      We assessed effect modification by living (vs deceased) donor, age (<50 or ≥50 years), and race/ethnicity separately by including an interaction term between the variable of interest and citizenship in the full model. Age was treated as a binary variable in the effect modification analyses to ease interpretation.

      Sensitivity Analyses

      We conducted 2 sensitivity analyses. In the first, given the potential for misclassification of nonresident aliens as permanent residents and vice versa, we conducted analyses combining these 2 groups and comparing them against US citizens. Because we cannot capture outcomes of nonresident aliens who leave the United States and do not return, this may bias results toward a beneficial association with nonresident alien status. Thus, we conducted a second set of sensitivity analyses restricting the outcomes to 1- and 3-year survival because the shorter the follow-up, the less likely patients will have left the country.
      All analyses were performed using R, version 3.3.0 (R Foundation for Statistical Computing). The Institutional Review Board of the Los Angeles Biomedical Institute at Harbor-UCLA Medical Center approved the study and waived the requirement for written consent owing to the deidentified nature of the data.

      Results

      Patient Characteristics

      Of 278,779 adult patients who received their first kidney transplant from 1990 to 2011, Medicaid was the primary payer for 10,495 (Fig S1). Of these patients, 8,660 (82.4%) were US citizens, 1,489 (14.2%) were permanent residents, and 346 (3.3%) were nonresident aliens (Table 1). Nonresident aliens were younger and more likely to be male and Hispanic than both US citizens and permanent residents. They generally had better functional status and were less likely to have comorbid conditions despite having spent more time receiving maintenance dialysis before transplantation. The panel-reactive antibody profiles of nonresident aliens did not differ significantly from those of US citizens, and they were more likely to have blood type O and to have received a 0 HLA antigen–mismatched kidney. There was a longer time for nonresident aliens to get waitlisted and undergo transplantation, with a higher proportion undergoing transplantation in more recent years. Two hundred ten (61%) nonresident aliens underwent transplantation after 2005, whereas only 3,704 (36%) permanent resident and US citizen recipients underwent transplantation after 2005. Nonresident aliens were also more likely to have had living donors (40% vs 32% of US citizens and 27% of permanent residents). Like their recipients, donors of nonresident aliens tended to be younger, Hispanic, and permanent residents or nonresident aliens themselves. Nonresident aliens received transplants in 20 states, with 71% undergoing transplantation in California, the state with the highest percentage of Medicaid-funded transplantations that went to nonresident aliens (Fig 1; Table S1).
      Table 1Baseline Characteristics of Adult Patients on Medicaid Who Received Kidney Transplants From 1990 to 2011
      US Citizens (n = 8,660)Permanent Residents (n = 1,489)Nonresident Aliens (n = 346)P
      Demographics
       Age, y42.0 [31.0-53.0]46.0 [34.0-57.0]34.5 [27.0-49.0]<0.001
       Male sex4,364 (50.4%)835 (56.1%)219 (63.3%)<0.001
       Race/ethnicity<0.001
      Hispanic1,766 (20.4%)890 (59.8%)265 (76.6%)
      Non-Hispanic black2,899 (33.5%)122 (8.2%)34 (9.8%)
      Non-Hispanic white or other3,995 (46.1%)477 (32.0%)47 (13.6%)
      Dialysis characteristics
       Dialysis modality
      Missing for 196 US citizens, 20 permanent residents, and fewer than 10 nonresident aliens.
      <0.001
      No dialysis1,802 (20.8%)127 (8.5%)
      Per federal research regulations, any cell counts less than 10 must not be reported.
      Hemodialysis5,796 (66.9%)1,195 (80.3%)289 (83.5%)
      Peritoneal dialysis866 (10.0%)147 (9.9%)44 (12.7%)
       Primary cause of ESRD<0.001
      Other5,107 (59.0%)904 (60.7%)214 (61.8%)
      Diabetes2,027 (23.4%)276 (18.5%)41 (11.8%)
      Unknown1,526 (17.6%)309 (20.8%)91 (26.3%)
       Dialysis vintage < 1 y before transplantation
      Missing for 426 US citizens, 69 permanent residents, and 11 nonresident aliens.
      4,842 (55.9%)568 (38.1%)120 (34.7%)<0.001
      Comorbid conditions
       Peripheral vascular disease
      Missing for 1,007 US citizens, 140 permanent residents, and 19 nonresident aliens.
      277 (3.2%)47 (3.2%)
      Per federal research regulations, any cell counts less than 10 must not be reported.
      >0.05
      We have masked the specific P values to prevent the n<10 cells from being calculated.
       Cerebrovascular disease
      Missing for 1,218 US citizens, 175 permanent residents, and 36 nonresident aliens.
      224 (2.6%)27 (1.8%)
      Per federal research regulations, any cell counts less than 10 must not be reported.
      <0.05
      We have masked the specific P values to prevent the n<10 cells from being calculated.
       Lung disease (COPD)
      Missing for 897 US citizens, 125 permanent residents, and 17 nonresident aliens.
      98 (1.1%)11 (0.7%)
      Per federal research regulations, any cell counts less than 10 must not be reported.
      <0.05
      We have masked the specific P values to prevent the n<10 cells from being calculated.
       Cancer
      Missing for 956 US citizens, 126 permanent residents, and 16 nonresident aliens.
      147 (1.7%)14 (0.9%)
      Per federal research regulations, any cell counts less than 10 must not be reported.
      <0.05
      We have masked the specific P values to prevent the n<10 cells from being calculated.
       Diabetes
      Missing for 641 US citizens, 100 permanent residents, and 13 nonresident aliens.
      3,135 (36.5%)439 (29.5%)59 (17.1%)<0.001
       Functional status<0.001
      NYHA I or II6,812 (78.7%)1,228 (82.5%)310 (89.6%)
      NYHA III804 (9.3%)91 (6.1%)13 (3.8%)
      NYHA IV191 (2.2%)68 (4.6%)
      Per federal research regulations, any cell counts less than 10 must not be reported.
      Unknown853 (9.8%)102 (6.9%)18 (5.2%)
       Comorbid condition count0.7 ± 0.50.8 ± 0.50.9 ± 0.4
      Transplant characteristics
       <1 y from dialysis to waitlist
      Missing for 1,089 US citizens, 136 permanent residents, and 34 nonresident aliens.
      4,555 (52.6%)581 (39.0%)109 (31.5%)<0.001
       Transplant date before 20002,589 (29.9%)346 (23.2%)38 (11.0%)<0.001
       Deceased donor5,900 (68.1%)1,094 (73.5%)206 (59.5%)<0.001
       >80% PRA
      Missing for 772 US citizens, 52 permanent residents, and 16 nonresident aliens.
      216 (2.5%)53 (3.6%)
      Per federal research regulations, any cell counts less than 10 must not be reported.
      >0.05
      We have masked the specific P values to prevent the n<10 cells from being calculated.
       0-mismatch HLA
      Missing for 250 US citizens, 55 permanent residents, and 16 nonresident aliens.
      875 (10.1%)174 (11.7%)58 (16.8%)<0.001
       BMI, kg/m2
      Missing for 1,629 US citizens, 247 permanent residents, and 53 nonresident aliens.
      26.2 ± 5.225.1 ± 4.724.2 ± 4.4<0.001
       Multiple organ recipient537 (6.2%)48 (3.2%)
      Per federal research regulations, any cell counts less than 10 must not be reported.
      <0.001
       ABO blood group<0.001
      A3,119 (36.0%)486 (32.6%)98 (28.3%)
      AB440 (5.1%)76 (5.1%)22 (6.4%)
      B1,206 (13.9%)212 (14.2%)34 (9.8%)
      O3,895 (45.0%)715 (48.0%)192 (55.5%)
       Cold ischemia time >14 h
      Missing for 1,405 US citizens, 205 permanent residents, and 61 nonresident aliens.
      3,487 (40.3%)643 (43.2%)122 (35.3%)0.075
      Donor characteristics
       Donor age, y
      Missing for 15 US citizens, 0 permanent residents, and 0 nonresident aliens.
      36.6 ± 15.437.0 ± 15.634.5 ± 15.70.02
       Male donor
      Missing for 15 US citizens, 0 permanent residents, and 0 nonresident aliens.
      4,732 (54.6%)838 (56.3%)197 (56.9%)0.4
       Donor race
      Missing for 17 US citizens, less than 10 permanent residents, and 0 nonresident aliens.
      <0.001
      White6,106 (70.5%)849 (57.0%)165 (47.7%)
      Black1,509 (17.4%)137 (9.2%)25 (7.2%)
      Other1,028 (11.9%)502 (33.7%)156 (45.1%)
       Hispanic donor1,766 (20.4%)890 (59.8%)265 (76.6%)<0.001
       Donor citizenship<0.001
      US citizen8,181 (94.5%)1,164 (78.2%)226 (65.3%)
      Resident alien215 (2.5%)200 (13.4%)51 (14.7%)
      Nonresident alien126 (1.5%)87 (5.8%)62 (17.9%)
       Donor serum creatinine, mg/dL
      Missing for 760 US citizens, 107 permanent residents, and 11 nonresident aliens.
      1.1 ± 1.11.1 ± 1.01.0 ± 0.80.7
      Note: Values for categorical variables are given as number (percentage); values for continuous variables, as mean ± standard deviation or median [first quartile-third quartile].
      Abbreviations: BMI, body mass index; COPD, chronic obstructive pulmonary disease; ESRD, end-stage renal disease; NYHA, New York Health Association; PRA, panel-reactive antibody.
      a Missing for 196 US citizens, 20 permanent residents, and fewer than 10 nonresident aliens.
      b Per federal research regulations, any cell counts less than 10 must not be reported.
      c Missing for 426 US citizens, 69 permanent residents, and 11 nonresident aliens.
      d Missing for 1,007 US citizens, 140 permanent residents, and 19 nonresident aliens.
      e We have masked the specific P values to prevent the n < 10 cells from being calculated.
      f Missing for 1,218 US citizens, 175 permanent residents, and 36 nonresident aliens.
      g Missing for 897 US citizens, 125 permanent residents, and 17 nonresident aliens.
      h Missing for 956 US citizens, 126 permanent residents, and 16 nonresident aliens.
      i Missing for 641 US citizens, 100 permanent residents, and 13 nonresident aliens.
      j Missing for 1,089 US citizens, 136 permanent residents, and 34 nonresident aliens.
      k Missing for 772 US citizens, 52 permanent residents, and 16 nonresident aliens.
      l Missing for 250 US citizens, 55 permanent residents, and 16 nonresident aliens.
      m Missing for 1,629 US citizens, 247 permanent residents, and 53 nonresident aliens.
      n Missing for 1,405 US citizens, 205 permanent residents, and 61 nonresident aliens.
      o Missing for 15 US citizens, 0 permanent residents, and 0 nonresident aliens.
      p Missing for 15 US citizens, 0 permanent residents, and 0 nonresident aliens.
      q Missing for 17 US citizens, less than 10 permanent residents, and 0 nonresident aliens.
      r Missing for 760 US citizens, 107 permanent residents, and 11 nonresident aliens.
      Figure thumbnail gr1
      Figure 1Percent of adult Medicaid patients who received kidney transplants from 1990 through 2011 who were nonresident aliens, by state. CA (244), MA (18), and NY (26) performed transplantation on the most nonresident aliens with Medicaid. The following states performed transplantation on 1 to 9 undocumented patients with Medicaid: DC, FL, GA, HI, IL, MI, MN, MO, NC, NJ, OR, PA, SD, TN, TX, VA, WA. Per federal research regulations, any counts less than 10 must not be reported.

      Association of Citizenship With Outcomes

      We identified 2,741 transplant losses over 37,000 person-years of follow-up, for a rate of 7.3 all-cause transplant losses per 100 person-years (Table 2). Nonresident aliens had a >45% lower unadjusted risk for all-cause transplant loss, death-censored transplant loss, and death compared with US citizens (Table 3; Figs 2, S2, and S3). Results were attenuated when further adjusted for demographics (model 2), dialysis factors (model 3), transplant factors (model 4), and comorbid condition count (model 5), with no significant difference in mortality in model 4 or in death-censored transplant loss or death in the fully adjusted model 5. Type of donor (living vs deceased), age (<50 vs ≥50 years), and race/ethnicity did not modify any of the associations.
      Table 2Number of Events, Follow-up Time, and Incidence and Unadjusted Survival Rates for All Study Outcomes
      All Patients (N = 10,495)US Citizen (n = 8,660)Permanent Residents (n = 1,489)Nonresident Aliens (n = 346)
      All-cause transplant failure
       No. of events2,7412,44525442
       Survival rate at 5 y70%68%79%84%
       Mean follow-up, y3.56 ± 1.783.57 ± 1.783.54 ± 1.753.31 ± 1.80
       Total follow-up, person-y37,36530,9365,2821,147
       Incident rate, per 100 person-y7.37.94.83.7
      Death-censored transplant failure
       No. of events1,8241,62416832
       Survival rate at 5 y80%79%86%88%
       Mean follow-up, y3.95 ± 1.584.00 ± 1.573.79 ± 1.633.52 ± 1.73
       Total follow-up, person-y41,46534,6025,6451,218
       Incident rate, per 100 person-y4.44.73.02.6
      Death from any cause
       No. of events1,3891,24312818
       Survival rate at 5 y85%84%89%93%
       Mean follow-up, y3.56 ± 1.783.57 ± 1.783.55 ± 1.753.31 ± 1.80
       Total follow-up, person-y37,36530,9365,2821,147
       Incident rate, per 100 person-y3.74.02.41.7
      Note: Patients were only followed up for up to 5 years.
      Table 3Hazard Ratios for Adverse Transplantation Outcomes for Nonresident Aliens Versus US Citizens Estimated From a Frailty Model Clustered by Transplantation Center
      ModelHR (95% CI)
      Citizenship was a 3-level variable. See table d of Item S1 for HRs for permanent residents versus US citizens. Type II P values of the Wald test (ie, null hypothesis of no difference across all 3 groups) were <0.001 for all outcomes.
      All-Cause Transplant LossDeath-Censored Transplant Loss
      HRs for death-censored transplant loss are cause-specific.
      Death
      1: unadjusted0.48 (0.35-0.65)0.55 (0.39-0.79)0.42 (0.26-0.67)
      2: adjusted for demographics
      Age, sex, and race/ethnicity (Hispanic, non-Hispanic black, non-Hispanic white, or other).
      0.56 (0.41-0.76)0.59 (0.41-0.85)0.58 (0.36-0.93)
      3: model 2 + dialysis factors
      Time on dialysis therapy (<1 or ≥1 year) and cause of kidney failure (diabetes, other, or unknown).
      0.58 (0.42-0.78)0.60 (0.41-0.86)0.58 (0.36-0.93)
      4: model 3 + transplant factors
      Zero HLA antigen mismatch, living/deceased donor, and transplantation before 2000.
      0.63 (0.45-0.85)0.65 (0.45-0.94)0.65 (0.40-1.06)
      5: model 4 + comorbid condition count
      Count included peripheral vascular disease, cerebrovascular disease, lung disease, cancer, and diabetes.
      0.67 (0.48-0.94)0.68 (0.46-1.01)0.68 (0.41-1.15)
      Note: Patients were followed up to 5 years.
      Abbreviations: CI, confidence interval; HR, hazard ratio.
      a Citizenship was a 3-level variable. See table d of Item S1 for HRs for permanent residents versus US citizens. Type II P values of the Wald test (ie, null hypothesis of no difference across all 3 groups) were <0.001 for all outcomes.
      b HRs for death-censored transplant loss are cause-specific.
      c Age, sex, and race/ethnicity (Hispanic, non-Hispanic black, non-Hispanic white, or other).
      d Time on dialysis therapy (<1 or ≥1 year) and cause of kidney failure (diabetes, other, or unknown).
      e Zero HLA antigen mismatch, living/deceased donor, and transplantation before 2000.
      f Count included peripheral vascular disease, cerebrovascular disease, lung disease, cancer, and diabetes.
      Figure thumbnail gr2
      Figure 2Kaplan-Meier curve for unadjusted overall transplant survival in adult Medicaid patients who received kidney transplants from 1990 through 2011, by citizenship status.
      We performed sensitivity analyses in which we: (1) addressed misclassification of immigrants by combining nonresident aliens and permanent residents into one group and compared them against US citizens and (2) restricted follow-up times to 1 and 3 years to minimize differential loss to follow-up between groups. All results were materially unchanged from that of the primary analysis (tables a-c of Item S1). Citizenship was treated as a 3-level variable in all analyses except for the first sensitivity analysis. Outcomes of permanent residents versus US citizens are reported in tables d to f of Item S1.

      Validity of Exposure Variable

      To assess the validity of the citizenship variable from the Transplant Candidate Registration form, we reviewed medical records of all 29 patients covered by Medicaid who had received a kidney transplant from 2009 to 2011 at a single center. Of 20 patients categorized as nonresident aliens on the form, 19 (95%) were confirmed to be nonresident aliens via chart review. Conversely, all 19 patients who were found to be nonresident aliens via chart review were correctly categorized as such on the form. Sensitivity of the nonresident alien variable was 95%, and specificity was 90%. None of the patients at this center had traveled to the United States for the purpose of receiving a transplant.

      Discussion

      Our study examined kidney transplantation outcomes in adult nonresident aliens in the United States and found that very few Medicaid patients who received their first kidney transplant between 1990 and 2011 were nonresident aliens. Our analyses suggest that they have comparable outcomes to US citizens when similarly insured. These results were robust in models that adjusted for various demographic, dialysis, and transplant-related factors, as well as sensitivity analyses that varied the length of follow-up and that combined permanent resident outcomes with those of nonresident aliens.
      The nonresident aliens in this study likely represent a select subgroup of patients. We assumed they were undocumented immigrants, who have a high employment rate and tend to be younger and healthier than US citizens.
      • Rodriguez R.A.
      Dialysis for undocumented immigrants in the United States.
      Their younger age may explain the lower prevalence of diabetic nephropathy compared with US citizens. The predominantly Hispanic immigrants may also have a higher rate of Mesoamerican nephropathy that partly accounts for the high percentage of unknown cause of end-stage kidney disease in the group. Given the barriers to transplantation for noncitizens, these nonresident aliens who receive transplants are likely to be healthier, have stronger family and financial support, and be better able to navigate the health care system. Such selection bias could explain why the nonresident aliens had lower rates of all-cause transplant loss than US citizens. Although not all undocumented immigrants may be suitable transplant candidates, our study suggests that with proper screening, citizenship status itself is not predictive of poor outcomes.
      Our findings that nonresident aliens have favorable transplant outcomes are in line with a recent single-center study of 289 pediatric kidney transplant recipients in California, 48 (17%) of whom were undocumented immigrants.
      • McEnhill M.E.
      • Brennan J.L.
      • Winnicki E.
      • et al.
      Effect of immigration status on outcomes in pediatric kidney transplant recipients.
      In contrast to our study, citizenship status was ascertained by chart review. Patients were categorized as either undocumented immigrants or US citizens, with permanent residents considered as citizens. After adjustment for patient age, donor age, donor type, and HLA antigen mismatch, the authors found that undocumented immigrant children had a lower risk for transplant loss at 5 years as compared with permanent residents and US citizens (HR, 0.38; 95% CI, 0.15-0.96). More than 20% of undocumented recipients who reached 21 years or older subsequently lost their transplants, primarily because they could not afford their immunosuppressive medications when they aged out of the state-funded program that covers these medications for pediatric patients. The insurance status of these patients was not reported, so it is not clear if these patients were covered by Medicaid or other insurance at the time of their transition out of the pediatric program.
      Both our study and the pediatric study highlight the limited access that nonresident aliens, including undocumented immigrants, have to kidney transplantation. Most adult US citizens have their dialysis and kidney transplantation costs covered by Medicare, a federal health insurance program.
      • Rettig R.A.
      Special treatment–the story of Medicare's ESRD entitlement.
      However, the Omnibus Reconciliation Act of 1986 restricts federal Medicaid funds from being spent on undocumented immigrants unless it is for a life-threatening or emergency situation.

      Omnibus Budget Reconciliation Act of 1986. Section 9406, Public Law 99-509.

      Thus, the estimated 6,000 undocumented immigrants in the United States with end-stage kidney disease are entitled to emergency dialysis regardless of their ability to pay, but maintenance dialysis is available only in certain areas depending on state and local legislation and policy interpretation.
      • Rodriguez R.A.
      Dialysis for undocumented immigrants in the United States.
      • Campbell G.A.
      • Sanoff S.
      • Rosner M.H.
      Care of the undocumented immigrant in the United States with ESRD.
      • Straube B.M.
      Reform of the US healthcare system: care of undocumented individuals with ESRD.
      For instance, California, home to the most undocumented immigrants in the United States (2.35 million), uses state funds to provide maintenance dialysis for these patients.

      Hou NV, Vangala C, Raghavan R. Undocumented with end stage renal disease: characteristics and outcomes associated with delayed initiation. Kidney Week. Chicago, IL: American Society of Nephrology; November 15-20, 2016.

      By contrast, Texas, which has the second largest number of undocumented immigrants (1.65 million), often only dialyzes these patients if they present with imminent life-threatening symptoms, a practice that leads to increased costs, higher mortality rates, and poor quality of life stemming from the physical and psychosocial distress of receiving emergent-only dialysis.

      Hou NV, Vangala C, Raghavan R. Undocumented with end stage renal disease: characteristics and outcomes associated with delayed initiation. Kidney Week. Chicago, IL: American Society of Nephrology; November 15-20, 2016.

      • Raghavan R.
      When access to chronic dialysis is limited: one center's approach to emergent hemodialysis.
      • Raghavan R.
      • Nuila R.
      Survivors–dialysis, immigration, and U.S. law.
      • Sheikh-Hamad D.
      • Paiuk E.
      • Wright A.J.
      • Kleinmann C.
      • Khosla U.
      • Shandera W.X.
      Care for immigrants with end-stage renal disease in Houston: a comparison of two practices.
      • Hogan A.N.
      • Fox W.R.
      • Roppolo L.P.
      • Suter R.E.
      Emergent dialysis and its impact on quality of life in undocumented patients with end-stage renal disease.
      • Cervantes L.
      • Fischer S.
      • Berlinger N.
      • et al.
      The illness experience of undocumented immigrants with end-stage renal disease.
      Kidney transplantation is not considered an emergency treatment for end-stage kidney disease. Thus, unlike dialysis, under no condition would it be federally subsidized for undocumented immigrants, although it leads to lower morbidity and mortality rates and better quality of life for patients at a lower cost.
      • Wolfe R.A.
      • Ashby V.B.
      • Milford E.L.
      • et al.
      Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant.
      • Schweitzer E.J.
      • Wiland A.
      • Evans D.
      • et al.
      The shrinking renal replacement therapy “break-even” point.
      Transplantation centers often deny uninsured patients kidney transplantation out of concern that they might not be able to pay for their transplant-sustaining immunosuppressant medications.
      • Herring A.A.
      • Woolhandler S.
      • Himmelstein D.U.
      Insurance status of U.S. organ donors and transplant recipients: the uninsured give, but rarely receive.
      • Gill J.S.
      • Tonelli M.
      Penny wise, pound foolish? Coverage limits on immunosuppression after kidney transplantation.
      • Evans R.W.
      • Applegate W.H.
      • Briscoe D.M.
      • et al.
      Cost-related immunosuppressive medication nonadherence among kidney transplant recipients.
      In the era of the Affordable Care Act, undocumented immigrants remain one of the few groups of patients ineligible for either Medicaid or insurance through the Health Insurance Marketplaces.
      • Sommers B.D.
      Stuck between health and immigration reform–care for undocumented immigrants.
      Immigrants with valid visas are eligible to participate in the exchange. Undocumented immigrants can be insured through off-the-exchange commercial health insurance plans subsidized by charitable organizations, although it is unclear whether this option is sustainable.
      • Raghavan R.
      New opportunities for funding dialysis-dependent undocumented individuals.
      As a result, many undocumented immigrants have turned to state programs for insurance coverage for transplantation. This is likely the reason that the vast majority of the undocumented immigrants in our study underwent transplantation in California. About 1,350 of 61,000 (2%) patients receiving dialysis in that state are undocumented immigrants.
      • Hurley L.
      • Kempe A.
      • Crane L.A.
      • et al.
      Care of undocumented individuals with ESRD: a national survey of US nephrologists.
      Although emergency Medi-Cal (the California version of Medicaid) does not cover transplantations, anecdotally, patients have been getting transplants by securing full-scope Medi-Cal as immigrants permanently residing in the United States under color of law (PRUCOL).
      • Kuruvilla R.
      • Raghavan R.
      Health care for undocumented immigrants in Texas: past, present, and future.
      PRUCOL patients are individuals living in the United States with the knowledge of the US Citizenship and Immigration Services (USCIS) but who the USCIS does not plan to deport. Undocumented immigrants not yet receiving dialysis do not qualify for the program. This is likely the reason that none of the nonresident aliens in our study received preemptive transplants. Regarding pediatric patients, in 2016, California state law expanded Medi-Cal coverage to low-income children regardless of immigration status.
      • Fabi R.
      • Saloner B.
      Covering undocumented immigrants—state innovation in California.
      In 2011, the state legislature also passed a bill mandating that Medi-Cal would continue to provide antirejection medications for up to 2 years posttransplantation if the patient has no other insurance coverage, even if patients later become ineligible for Medi-Cal (eg, if they are no longer considered low income).

      Assembly Bill (AB) 2352, Perez. Chapter 676. Vol Statutes of 20102011:Welfare and Institutions Code.

      Many safety-net and county hospital programs will also provide these medications if patients cannot afford them, making long-term transplant survival feasible even for low-income patients. These state-sponsored initiatives do not violate federal policies because they use only state and not federal funds. Notably, increasing access to kidney transplantation has not resulted in an influx of undocumented immigrants to California; after peaking at 2.8 million in 2007, the number of undocumented immigrants has slowly decreased to 2.35 million.

      Hou NV, Vangala C, Raghavan R. Undocumented with end stage renal disease: characteristics and outcomes associated with delayed initiation. Kidney Week. Chicago, IL: American Society of Nephrology; November 15-20, 2016.

      Illinois is another state that subsidizes transplantation for undocumented immigrants. In 2014, it passed the Comprehensive Medicaid Legislation, which allows undocumented immigrants already enrolled in the state-funded dialysis program to receive state public aid funds to cover kidney transplantation.
      • Ansell D.
      • Pallok K.
      • Guzman M.D.
      • Flores M.
      • Oberholzer J.
      Illinois law opens door to kidney transplants for undocumented immigrants.
      The financial savings were a driving factor in approving the bill. Even with the cost of surgery, transplantation is more cost-effective than dialysis after less than 2 years. Based on an 8-year life expectancy, the projected savings would be $321,000 per patient.
      • Linden E.A.
      • Cano J.
      • Coritsidis G.N.
      Kidney transplantation in undocumented immigrants with ESRD: a policy whose time has come?.
      The savings would be even more dramatic in states that provide only emergent (rather than maintenance) dialysis, where costs are estimated to reach $285,000 a year per patient.
      • Sheikh-Hamad D.
      • Paiuk E.
      • Wright A.J.
      • Kleinmann C.
      • Khosla U.
      • Shandera W.X.
      Care for immigrants with end-stage renal disease in Houston: a comparison of two practices.
      In states without coverage for kidney transplantation, undocumented immigrants are often denied a better and more cost-effective end-stage kidney disease treatment option. Some have argued that such unequal access is inevitable given the relative scarcity of deceased donors in the United States. However, this argument fails to consider that undocumented immigrants disproportionately contribute to the pool of potential deceased donors for the United States.
      • Goldberg A.M.
      • Simmerling M.
      • Frader J.E.
      Why nondocumented residents should have access to kidney transplantation: arguments for lifting the federal ban on reimbursement.
      In the 22 years of our study, 990 deceased donors were nonresident aliens, more than 4 times the number of nonresident aliens receiving Medicaid who received a deceased donor transplant.
      • Collins A.J.
      • Foley R.N.
      • Chavers B.
      • et al.
      US Renal Data System 2013 annual data report.
      Also, 40% of nonresident aliens in our study had living donors and did not take away any organs from potential US citizen recipients. Similarly, a survey of undocumented immigrants receiving dialysis in New York found that 60% had potential living donors.
      • Linden E.A.
      • Cano J.
      • Coritsidis G.N.
      Kidney transplantation in undocumented immigrants with ESRD: a policy whose time has come?.
      Expanding coverage for kidney transplantation for these patients with living donors would improve their outcomes without negatively affecting the chances of US citizens undergoing transplantation. Even if half the undocumented immigrants with end-stage kidney disease in the United States were to be waitlisted for a deceased donor transplant, it would increase the waitlist by only 3%.
      There would also be a societal benefit to having these patients receive transplants. They tend to be younger, healthier, and thus more likely to contribute to the US workforce if they undergo transplantation.
      • Linden E.A.
      • Cano J.
      • Coritsidis G.N.
      Kidney transplantation in undocumented immigrants with ESRD: a policy whose time has come?.
      As noted earlier, there would be health care savings associated with having nonresident alien patients receiving maintenance dialysis treatments undergo transplantation.
      Our study has several limitations. The primary one is that citizenship status was self-reported as nonresident alien, resident alien, and US citizen. Thus, it is difficult to discern whether nonresident aliens were undocumented immigrants, foreign nationals with a legal visa, or foreign nationals traveling to the United States for transplantation (though it is unlikely that the last group would have qualified for Medicaid). Similarly, undocumented immigrants may have been misclassified as resident aliens. Chart review from a single center found the citizenship variable to be highly sensitive and specific, but it is unclear how generalizable these measures are to other centers. Another limitation is that we cannot capture outcomes of nonresident aliens who leave the United States and do not return. This would bias results toward a beneficial association with nonresident alien status. Given the low number of outcomes in the nonresident alien group, we also could not adjust for many potential confounders, including the specific cause of kidney failure, body mass index, specific comorbid conditions (instead of a comorbid condition count), and donor characteristics. We also could not adjust for unobserved confounders such as immunosuppressive regimen and employment status. Our results may not be generalizable to wealthier patients who do not qualify for Medicaid or to residents outside of California, the home state of >70% of the nonresident aliens. We were also unable to assess patient-reported outcomes such as quality of life. As with all observational studies, we cannot prove causation. However, the limitations must be balanced against the strengths of the study, which include a large national cohort and results that were consistent across various sensitivity analyses.
      In conclusion, we found that only a small percentage of patients with Medicaid who received transplants in the United States were nonresident aliens. The transplantations occurred mostly in California and have increased in recent years, and our study suggests that these nonresident aliens do no worse than US citizens after transplantation. Policymakers should consider expanding coverage for kidney transplantation in nonresident aliens, including undocumented immigrants, because it is associated with high-quality outcomes.

      Acknowledgements

      We thank Arleen Brown and Steven Wallace for critically reviewing earlier versions of the manuscript. The manuscript was reviewed and approved for publication by an officer of the National Institute of Diabetes and Digestive and Kidney Diseases.
      Disclaimer: Data reported herein were supplied by the USRDS. 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.
      Prior Presentation: Aspects of this study were presented in abstract form at the Society of General Internal Medicine Annual Meeting, April 19 to 22, 2017, Washington, DC.
      Peer Review: Received March 9, 2017. Evaluated by 3 external peer reviewers, with editorial input from a Statistics/Methods Editor, an Associate Editor, and the Editor-in-Chief. Accepted in revised form August 7, 2017.

      Supplementary Material

      References

        • Rodriguez R.A.
        Dialysis for undocumented immigrants in the United States.
        Adv Chronic Kidney Dis. 2015; 22: 60-65
        • Passel J.C.
        • Cohn D.
        Overall number of U.S. unauthorized immigrants holds steady since 2009.
        in: Numbers, Facts and Trends Shaping the World. Pew Research Center, 2016
        • Campbell G.A.
        • Sanoff S.
        • Rosner M.H.
        Care of the undocumented immigrant in the United States with ESRD.
        Am J Kidney Dis. 2010; 55: 181-191
        • Linden E.A.
        • Cano J.
        • Coritsidis G.N.
        Kidney transplantation in undocumented immigrants with ESRD: a policy whose time has come?.
        Am J Kidney Dis. 2012; 60: 354-359
        • Wolfe R.A.
        • Ashby V.B.
        • Milford E.L.
        • 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: 1725-1730
        • Schweitzer E.J.
        • Wiland A.
        • Evans D.
        • et al.
        The shrinking renal replacement therapy “break-even” point.
        Transplantation. 1998; 66: 1702-1708
        • Purnell T.S.
        • Luo X.
        • Kucirka L.M.
        • et al.
        Reduced racial disparity in kidney transplant outcomes in the United States from 1990 to 2012.
        J Am Soc Nephrol. 2016; 27: 2511-2518
        • Grubbs V.
        Undocumented immigrants and kidney transplant: costs and controversy.
        Health Affairs. 2014; 33: 332-335
        • Bramstedt K.A.
        Supporting organ transplantation in non-resident aliens within limits.
        Ethics Med. 2006; 22: 75-81
        • Glazier A.K.
        • Danovitch G.M.
        • Delmonico F.L.
        Organ transplantation for nonresidents of the United States: a policy for transparency.
        Am J Transplant. 2014; 14: 1740-1743
        • McEnhill M.E.
        • Brennan J.L.
        • Winnicki E.
        • et al.
        Effect of immigration status on outcomes in pediatric kidney transplant recipients.
        Am J Transplant. 2016; 16: 1827-1833
        • Rettig R.A.
        Special treatment–the story of Medicare's ESRD entitlement.
        N Engl J Med. 2011; 364: 596-598
      1. Omnibus Budget Reconciliation Act of 1986. Section 9406, Public Law 99-509.

        • Straube B.M.
        Reform of the US healthcare system: care of undocumented individuals with ESRD.
        Am J Kidney Dis. 2009; 53: 921-924
      2. Hou NV, Vangala C, Raghavan R. Undocumented with end stage renal disease: characteristics and outcomes associated with delayed initiation. Kidney Week. Chicago, IL: American Society of Nephrology; November 15-20, 2016.

        • Raghavan R.
        When access to chronic dialysis is limited: one center's approach to emergent hemodialysis.
        Semin Dial. 2012; 25: 267-271
        • Raghavan R.
        • Nuila R.
        Survivors–dialysis, immigration, and U.S. law.
        N Engl J Med. 2011; 364: 2183-2185
        • Sheikh-Hamad D.
        • Paiuk E.
        • Wright A.J.
        • Kleinmann C.
        • Khosla U.
        • Shandera W.X.
        Care for immigrants with end-stage renal disease in Houston: a comparison of two practices.
        Texas Med. 2007; 103 (53): 54-58
        • Hogan A.N.
        • Fox W.R.
        • Roppolo L.P.
        • Suter R.E.
        Emergent dialysis and its impact on quality of life in undocumented patients with end-stage renal disease.
        Ethn Dis. 2017; 27: 39-44
        • Cervantes L.
        • Fischer S.
        • Berlinger N.
        • et al.
        The illness experience of undocumented immigrants with end-stage renal disease.
        JAMA Intern Med. 2017; 177: 529-535
        • Herring A.A.
        • Woolhandler S.
        • Himmelstein D.U.
        Insurance status of U.S. organ donors and transplant recipients: the uninsured give, but rarely receive.
        Int J Health Serv. 2008; 38: 641-652
        • Gill J.S.
        • Tonelli M.
        Penny wise, pound foolish? Coverage limits on immunosuppression after kidney transplantation.
        N Engl J Med. 2012; 366: 586-589
        • Evans R.W.
        • Applegate W.H.
        • Briscoe D.M.
        • et al.
        Cost-related immunosuppressive medication nonadherence among kidney transplant recipients.
        Clin J Am Soc Nephrol. 2010; 5: 2323-2328
        • Sommers B.D.
        Stuck between health and immigration reform–care for undocumented immigrants.
        N Engl J Med. 2013; 369: 593-595
        • Raghavan R.
        New opportunities for funding dialysis-dependent undocumented individuals.
        Clin J Am Soc Nephrol. 2017; 12: 370-375
        • Hurley L.
        • Kempe A.
        • Crane L.A.
        • et al.
        Care of undocumented individuals with ESRD: a national survey of US nephrologists.
        Am J Kidney Dis. 2009; 53: 940-949
        • Kuruvilla R.
        • Raghavan R.
        Health care for undocumented immigrants in Texas: past, present, and future.
        Texas Med. 2014; 110: e1
        • Fabi R.
        • Saloner B.
        Covering undocumented immigrants—state innovation in California.
        N Engl J Med. 2016; 375: 1913-1915
      3. Assembly Bill (AB) 2352, Perez. Chapter 676. Vol Statutes of 20102011:Welfare and Institutions Code.

        • Ansell D.
        • Pallok K.
        • Guzman M.D.
        • Flores M.
        • Oberholzer J.
        Illinois law opens door to kidney transplants for undocumented immigrants.
        Health Affairs. 2015; 34: 781-787
        • Goldberg A.M.
        • Simmerling M.
        • Frader J.E.
        Why nondocumented residents should have access to kidney transplantation: arguments for lifting the federal ban on reimbursement.
        Transplantation. 2007; 83: 17-20
        • Collins A.J.
        • Foley R.N.
        • Chavers B.
        • et al.
        US Renal Data System 2013 annual data report.
        Am J Kidney Dis. 2014; 63: e1-e420

      Linked Article

      • The United States Needs a National Policy on Dialysis for Undocumented Immigrants With ESRD
        American Journal of Kidney DiseasesVol. 71Issue 2
        • Preview
          An estimated 6,500 undocumented immigrants with end-stage renal disease (ESRD) reside in the United States.1 The availability of standard outpatient (thrice-weekly) hemodialysis for undocumented immigrants with ESRD varies throughout the country. Although many states offer emergency-only hemodialysis (dialysis only after an emergency department evaluation), others offer standard hemodialysis.2 This considerable variation by state is due to the lack of a national policy. Undocumented immigrants with ESRD are eligible for neither the 1972 Medicare ESRD entitlement program nor full-scope Medicaid coverage.
        • Full-Text
        • PDF