Survival Benefit in Older Patients Transplanted With Viremic Hepatitis C Positive Kidneys When Compared With High KDPI Kidneys : Transplantation

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Original Clinical Science—General

Survival Benefit in Older Patients Transplanted With Viremic Hepatitis C Positive Kidneys When Compared With High KDPI Kidneys

Sibulesky, Lena MD1,2; Leca, Nicolae MD2,3; Limaye, Ajit P. MD2,4; Ramasamy, Bakthavatsalam MBBS1; Perkins, James D. MD1,2

Author Information
doi: 10.1097/TP.0000000000004179
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Abstract

INTRODUCTION

Kidney transplantation is the preferred therapy for patients with end-stage renal disease. When compared with alternative therapies, it is associated with superior survival and improved quality of life. Although the number of donors have increased over the years, there continues to be a wide gap between the number of candidates on the waiting list and the number of organs available for transplantation. Because of the increased demand and ongoing critical reevaluation, kidneys that were previously considered too risky to transplant, including kidneys from donors with risk criteria for blood-borne viruses, high Kidney Donor Profile Index (KDPI) >85% kidneys, are now successfully utilized with increasing frequency.1-3

Deceased donor kidney allografts are allocated based on the category of estimated posttransplant survival (EPTS) score of recipients. The lowest EPTS score (≤20%) patients are prioritized to receive deceased donor kidneys with the lowest risk of transplant failure. The higher KDPI kidneys >85%, although not specifically allocated to a recipient category, are more likely to be allocated to candidates with higher EPTS score. Bae et al4 demonstrated that for candidates with middle or high EPTS scores survival benefit decreased with higher KDPI kidney transplants when compared with lower KDPI kidney transplants but still led to improved survival when compared with remaining on the waiting list.

Introduction of highly effective direct-acting antiviral (DAA) therapy has allowed consideration of transplantation of organs that were previously discarded.5 Studies using DAAs in hepatitis C (Hep C)–positive chronic kidney disease patients heightened interest in exploring the possibility of transplanting hepatitis C virus (HCV)–infected kidneys in both positive and naive recipients. Despite this, the transplant community is cautious when considering these kidneys for transplantation because of isolated reports of fulminant cholestatic hepatitis, potential increased risk of acute cellular rejection and injury resembling membranoproliferative glomerulonephritis because of modulation of immune response, and the logistical issues with obtaining the DAA medications.6-8

It has been demonstrated repeatedly that the quality and outcomes of kidneys recovered from HCV-positive donors are comparable to the quality and outcomes of the kidneys from the donors who are HCV negative when the Kidney Donor Risk Index of these HCV-positive kidneys is modified by assuming the HCV status to be negative in the scoring formula.9,10 Kidneys from donors who are viremic or antibody positive for HCV are usually recovered from donors who are significantly younger, more likely to be White, and less likely to have hypertension and diabetes. Nonetheless, Chang et al11 demonstrated that despite the decrease in kidney discard in recent years, kidneys from viremic compared with aviremic seronegative donors still had 48% higher odds of discard in 2019.

In this study, we aimed to define specific kidney transplant candidates for whom Hep C–viremic or antibody-positive kidneys would lead to a significant survival benefit. We hypothesized that the patients with higher EPTS score would have better survival and thus have more benefit with Hep C–positive kidneys compared with receiving high KDPI >85% kidney allografts.

MATERIALS AND METHODS

Using Organ Procurement and Transplantation Network (OPTN) data, we conducted a retrospective analysis of all adult (≥18 y old) recipients undergoing kidney transplant from May 10, 2013, to June 30, 2021. Exclusion criteria included patients receiving multiorgan transplants and living kidney transplants. The endpoint of our analysis was 1-, 3-, and 5-y patient and graft survival.

Recipients of kidney transplant were stratified according to their EPTS score and deceased donor types. They were divided into 3 groups: (1) EPTS 0%–20% who have received KDPI >85% kidneys, Hep C antibody-positive (Ab+) nucleic acid testing–positive (NAT)+ kidneys, Hep C Ab+NAT– kidneys; (2) EPTS 21%–60% who have received KDPI >85% kidneys, Hep C Ab+NAT+ kidneys, Hep C Ab+NAT– kidneys; and (3) EPTS 61%–100% who have received KDPI >85% kidneys, Hep C Ab+NAT+ kidneys, Hep C Ab+NAT– kidneys.

Recorded baseline data included recipient characteristics such as age, gender, race (Asian, Black, Hispanic, Other, or White), body mass index, diagnosis of end-stage kidney disease, including hypertension, diabetes, and other, time on dialysis, waiting time on the list, ABO blood type, peak panel reactive antibody (0%–9%, 10%–79%, 80%–100%), and Hep C seropositive status.

Donor characteristics recorded included age, gender, race (Asian, Black, Hispanic, Other, or White), height, weight, terminal creatinine level, diabetes, hypertension, donation after circulatory death or donation after brain death, Hep C seropositivity (HCV) and NAT status, and KDPI.

The data for this analysis is OPTN data released August 1, 2021. The United Network for Organ Sharing as the contractor for the OPTN supplied this data. The interpretation and reporting of these data are the responsibility of the authors and in no way should be seen as an official policy of or interpretation by the OPTN or the US Government. The University of Washington Human Subjects Division deems the OPTN database is de-identified and publicly available and, thus, not human subjects’ data. Therefore, this study was exempt from human subject review.

Statistical Analysis

Continuous variables were given as median and interquartile ranges. Categorical variables were presented as count and percentages. Donor and recipient height and/or weight had <0.1% missing values and these were imputed with linear regression using gender, age and race. Student t test or Wilcoxon, as appropriate for the distribution, was used to compare the continuous variables and chi-square analysis for categorical variables. We used the Kaplan-Meier with Log-Rank analysis to calculate graft and patient survival. All results were considered significant with a P < 0.05. All analyses were conducted in JMP Pro Version 15 (SAS Institute Inc).

RESULTS

In total, there were over 86 000 kidney-alone, deceased donor transplants performed between May 10, 2013, and June 20, 2021. Of these, 24.2% of kidney transplants were performed in 0%–20% EPTS group, 34.6% in 21%–60% EPTS group, and 41% of the kidney transplants were performed in the EPTS group of 61%–100%. In the 61%–100% EPTS group, there were 6.7% of Hep C seropositive recipients compared with 1.7% in EPTS 0%–20% group and 4.9% in 20%–60% group. The wait time was statistically different with 1376 d (interquartile range [IQR], 762–2105 d) in the lowest EPTS group, 1693 d (IQR, 933–2529 d) in the middle EPTS group, and 1797 d (IQR, 1128–2534 d) in the EPTS 61%–100% group. The median KDPI was 15% (8%–34%) in the EPTS 0%–20%, 46% (29%–65%) in the EPTS 21%–60%, and 54% (34%–74%) in the EPTS 61%–100% (Table 1).

TABLE 1. - Recipient demographics
Variables EPTS groups P
0–20 (N = 20 873, 24.2%) 21–60 (N = 29 806, 34.6%) 61–100 (N = 35 538, 41.2%)
Age, y 36 (30–42) 53 (47–59) 64 (58–69) <0.001
Female gender 9072 (43.5%) 12 910 (43.4%) 12 426 (35.0%) <0.001
Race <0.001
 White 7101 (34.0%) 11 495 (38.6%) 12 893 (36.3%)
 AA 6730 (32.3%) 10 734 (36.0%) 12 163 (34.2%)
 Hispanic 4893 (23.4%) 4881 (16.4%) 6827 (19.2%)
 Asian 1570 (7.5%) 2039 (6.8%) 2757 (7.8%)
 Other 579 (2.8%) 657 (2.2%) 898 (2.5%)
Kidney disease <0.001
 Diabetes 187 (0.9%) 4779 (16.0%) 19 635 (55.3%)
 HTN 5185 (24.8%) 8859 (29.7%) 6133 (17.3%)
 Other 15 501 (74.3%) 16 168 (54.2%) 9770 (27.5%)
Dialysis, y 3.6 (1.9–5.7) 4.5 (2.3–6.9) 4.7 (2.7–6.8) <0.001
BMI, kg/m2 27.0 (23.0–31.9) 28.3 (24.7–32.6) 29.0 (25.5–32.9) <0.001
Waiting time, d 1376 (762–2105) 1693 (933–2529) 1797 (1128–2534) <0.001
ABO <0.001
 A 7368 (35.3%) 10 394 (34.9%) 12 489 (35.1%)
 B 2780 (13.3%) 4133 (13.9%) 5082 (14.3%)
 O 9614 (46.1%) 13 651 (45.8%) 16 239 (45.7%)
 AB 111 (5.3%) 1628 (5.5%) 1728 (4.9%)
PRA percent <0.001
 0–9 12 557 (60.2%) 17 544 (58.9%) 23 178 (65.2%)
 10–79 4239 (20.3%) 5828 (19.6%) 6982 (19.7%)
 80–100 4077 (19.5%) 6434 (21.6%) 5378 (15.1%)
Hep C serostatus positive 363 (1.7%) 1464 (4.9%) 2366 (6.7%) <0.001
All data are presented as median (interquartile range) or count (%).
AA, African American; BMI, body mass index; EPTS, estimated posttransplant survival score; Hep C, hepatitis C; HTN, hypertension; PRA, panel reactive antibody.

Kidneys from Hep C–viremic donors were used in 5.6% (n = 2001) of patients in EPTS >61% group compared with 5.1% of patients in 21–60 EPTS group and 1.9% of 0–20 EPTS group (P < 0.001). Of all transplants performed in the EPTS 61%–100% group 11.9% were KDPI >85% compared with 5.2% in the EPTS 21%–60%, and 0.5% in the EPTS 0%–20% (Table 2). Across all EPTS groups, Hep C kidneys, viremic and aviremic, were from younger donors, with fewer having history of diabetes and hypertension (Table 3). The KDPI of Hep C Ab+NAT+ kidneys was 51% (38%–63%), 53% (40%–68%), and 55% (39%–72%) in 0–20, 21–60, and 61–100 EPTS groups. The modified KDPI (Kidney Donor Risk Index–Hep C) was 26% (14%–38%), 28% (15%–43%), and 30% (15%–48%) in 0–20, 21–60, and 61–100 EPTS groups.

TABLE 2. - Donor demographics
Variables EPTS groups P
0–20 21–60 61–100
Age, y 27 (21–36) 42 (31–51) 46 (34–55) <0.001
Female gender 6501 (31.2%) 11 828 (39.7%) 14 684 (41.3%) <0.001
Race <0.001
 White 14 622 (70.0%) 20 252 (68.0%) 23 837 (67.1%)
 AA 1851 (8.9%) 4424 (14.8%) 5296 (14.9%)
 Hispanic 3541 (17.0%) 3910 (13.1%) 4780 (13.5%)
 Asian 410 (2.0%) 702 (2.4%) 1008 (2.8%)
 Other 449 (2.1%) 518 (1.7%) 617 (1.7%)
Height, cm 175 (166.4–180.3) 170.2 (163–178) 170.2 (163.0–178.0) <0.001
Weight, kg 80 (68.1–94.8) 81.5 (68.1–97.0) 81.5 (68.4–97.5) <0.001
DCD 4263 (20.4%) 7853 (26.4%) 9491 (26.7%) <0.001
Terminal serum Cr 0.9 (0.7–1.2) 1.0 (0.7–1.5) 1.0 (0.7–1.5) <0.001
Hep C status <0.001
 Negative 20 237 (96.9%) 27 299 (91.6%) 32 204 (90.6%)
 Ab+NAT– 247 (1.2%) 991 (3.3%) 1333 (3.8%)
 Ab+NAT+ 389 (1.9%) 1516 (5.1%) 2001 (5.6%)
Any type diabetes 576 (2.8%) 2434 (8.2%) 3681 (10.4%) <0.001
HTN 2343 (11.2%) 9173 (30.8%) 13 403 (37.7%) <0.001
KDPI 15%(8%–34%) 46%(29%–65%) 54%(34%–74%) <0.001
KDPI >85% 110 (0.5%) 1563 (5.2%) 4212 (11.9%) <0.001
All data are presented as median (interquartile range) or count (%).
AA, African American; Ab, antibody; Cr, creatinine; DCD, donation after circulatory death; EPTS, estimated posttransplant survival score; Hep C, hepatitis C; HTN, hypertension; KDPI, Kidney Donor Profile Index; NAT, nucleic acid testing.

TABLE 3. - Donor demographics of KDPI >85% kidneys and Hep C Ab+NAT+ and Ab+NAT– kidneys
EPTS groups 86–100 Ab+NAT– Ab+NAT+ P
EPTS group 0–20 N = 110 N = 239 N = 375
 Donor age 56 (52–61) 35 (29–41) 33 (28–39) <0.001
 HTN 87 (79.1%) 45 (18.8%) 47 (12.5%) <0.001
 DM 37 (33.6%) 10 (4.2%) 7 (1.9%) <0.001
 Terminal Cr 1.1 (0.8–1.6) 0.9 (0.7–1.2) 0.9 (0.7–1.6) 0.36
EPTS group 21–60 N = 1563 N = 865 N = 1437
 Donor age 60 (55–64) 36 (30–43) 34 (28–40) <0.001
 HTN 1245 (79.7%) 154 (17.8%) 166 (11.6%) <0.001
 DM 472 (30.2%) 40 (4.6%) 24 (1.7%) <0.001
 Terminal Cr 1.2 (0.8–1.7) 1.0 (0.7–1.4) 0.9 (0.7–1.4) 0.19
EPTS group 61–100 N = 4212 N = 1077 N = 1815
 Donor age 61 (57–66) 36 (31–45) 33 (29–40) <0.001
 HTN 3294 (78.2%) 221 (20.5%) 215 (11.9%) <0.001
 DM 1201 (28.5%) 40 (3.7%) 39 (2.2%) <0.001
 Terminal Cr 1.1 (0.8–1.6) 0.9 (0.7–1.3) 0.9 (0.7–1.3) 0.28
All data are presented as median (interquartile range) or count (%).
Ab, antibody; Cr, creatinine; DM, diabetes; EPTS, estimated posttransplant survival score; Hep C, hepatitis C; HTN, hypertension; KDPI, Kidney Donor Profile Index; NAT, nucleic acid testing.

In the EPTS 0%–20%, the patient and graft survivals using KDPI >85% and Hep C NAT+ kidneys are demonstrated in Tables 4 and 5 and Figure 1A and B.

TABLE 4. - Graft survival
EPTS groups 1 y 3 y 5 y P
EPTS group 0–20 <0.001
 KDPI 86–100 91.8 (61) 76.2 (22) 64.5 (12)
 Ab+NAT– 99.0 (133) 94.0 (26) 83.2 (6)
 Ab+NAT+ 97.4 (168) 90.5 (36) 85.7 (9)
EPTS group 21–60 <0.001
 KDPI 86–100 92.3 (949) 80.8 (340) 69.6 (65)
 Ab+NAT– 96.6 (466) 86.0 (128) 76.6 (22)
 Ab+NAT+ 95.9 (790) 88.4 (252) 75.2 (43)
EPTS group 61–100 <0.001
 KDPI 86–100 87.5 (2364) 71.5 (855) 52.2 (135)
 Ab+NAT– 94.1 (555) 81.9 (162) 68.2 (17)
 Ab+NAT+ 91.8 (1017) 81.9 (341) 66.3 (59)
All data are presented as percent survival (numbers at risk).
Ab, antibody; EPTS, estimated posttransplant survival score; KDPI, Kidney Donor Profile Index; NAT, nucleic acid testing.

TABLE 5. - Patient survival
EPTS groups 1 y 3 y 5 y P
EPTS group 0–20 Unstable
 86–100 99 (62) 97.2 (22) 97.2 (6)
 Ab+NAT– 99.5 (133) 98.6 (26) 87.3 (1)
 Ab+NAT+ 99.6 (169) 93.1 (36) 88.2 (9)
EPTS group 21–60 0.08
 86–100 96.5 (968) 87.6 (348) 80.1 (70)
 Ab+NAT– 98.3 (470) 92.0 (129) 82.4 (23)
 Ab+NAT+ 97.1 (794) 91.9 (253) 82.4 (46)
EPTS group 61–100 <0.001
 86–100 91.7 (2424) 77.6 (893) 55.9 (142)
 Ab+NAT– 95.2 (559) 84.7 (165) 70.2 (18)
 Ab+NAT+ 94.0 (1034) 83.8 (347) 67.4 (59)
All data are presented as percent survival (numbers at risk).
Ab, antibody; EPTS, estimated posttransplant survival score; NAT, nucleic acid testing.

F1
FIGURE 1.:
Kidney graft survival and Patient survival by EPTS groups. A, Graft survival in the EPTS 0%–20% by KDPI. B, Patient survival in the EPTS 0%–20% by KDPI. Ab, antibody; EPTS, estimated posttransplant survival score; KDPI, Kidney Donor Profile Index; NAT, nucleic acid testing.

In the EPTS 21%–60%, 1-y graft survival was 91.8% with KDPI>85% kidneys, 99.0% with Hep C Ab+NAT– kidneys, and 97.4% with Hep C Ab+NAT+ kidneys. At 5 y, in this group of patients graft survival was 69.5% in high KDPI>85% kidneys, 76.6% with Hep C Ab+NAT– kidneys, and 75.2% in Hep C Ab+NAT+ (Table 4; Figure 2A).

F2
FIGURE 2.:
Kidney graft survival and Patient survival by EPTS groups. A, Graft survival in the EPTS 21%–60% by KDPI. B, Patient survival in the EPTS 21%–60% by KDPI. Ab, antibody; EPTS, estimated posttransplant survival score; KDPI, Kidney Donor Profile Index; NAT, nucleic acid testing.

The patient survival in the EPTS 21%–60% was 96.5% at 1 y with KDPI >85% kidneys, compared with 98.3% with Hep C Ab+NAT– kidneys and 97.1% with Hep C Ab+NAT + kidneys. At 5 y, the survival was again similar across all types of kidney transplants (Table 5; Figure 2B).

When looking at the EPTS group 61%–100%, 1-y graft survival was 87.5% with KDPI >85% kidneys compared with 91.8% with Hep C Ab+NAT+, and 94.1% with Hep C Ab+NAT– kidneys (P < 0.001). A 3-y graft survival was 71.5% in KDPI >85%, compared with 81.9% in Hep C NAT + and NAT– kidneys, whereas the graft survival at 5 y was 68.2% in Hep C Ab+NAT+, compared with 66.3% with Hep C Ab+ NAT+ kidneys and significantly lower at 52.2% in KDPI >85% (P < 0.001) (Table 4; Figure 3A). The patient survival was 91.7% with high KDPI >85% kidneys, 95.2% with Hep C Ab+NAT–, and 94.0% with Hep C Ab+NAT+ kidneys. At 3 y, the patient survival was significantly longer with Hep C kidneys, 84.7% with Ab+NAT– kidneys, 83.8% Ab+NAT+ kidneys, and only 77.6% with KDPI >85% kidneys (P < 0.001). The same trend continued at 5 y (Table 5; Figure 3B).

F3
FIGURE 3.:
Kidney graft survival and Patient survival by EPTS groups. A, Graft survival in the EPTS 61%–100% by KDPI. B, Patient survival in the EPTS 61%–100% by KDPI. Ab, antibody; EPTS, estimated posttransplant survival score; KDPI, Kidney Donor Profile Index; NAT, nucleic acid testing.

For waitlist candidates, the acceptance rates for Hep C NAT-positive donor kidneys in the 1%–20%, 21%–60%, and 61%–100% EPTS groups were 1.4%, 2.8%, and 3.1% in 2013 and increased to 17.5%, 21.1%, and 24.1%, respectively, in 2021 (Figure 4).

F4
FIGURE 4.:
Acceptance rate of HCV NAT-positive kidneys by EPTS. EPTS, estimated posttransplant survival score; HCV, hepatitis C virus; NAT, nucleic acid testing.

DISCUSSION

In this study of a large nationwide registry of transplant recipients, we demonstrated that the patient survival of the transplant patients with EPTS >61% was substantially longer with Hep C–viremic and –aviremic/Ab+ kidneys when compared with high KDPI >85% kidneys.

Although older registry studies in the United States have consistently demonstrated worse patient and graft survival with the use of HCV-seropositive kidneys more recent trials have demonstrated excellent outcomes.12,13 DAAs have changed the landscape of HCV care, including transplantation with Hep C–positive donor organs. The safety and feasibility was demonstrated in the Transplanting Hepatitis C Kidneys into Negative Kidney Transplant Recipients trial and the Exploring Renal Transplants Using Hepatitis-C Infected Donors for HCV-Negative Recipients-1 trial. In Transplanting Hepatitis C Kidneys into Negative Kidney Transplant Recipients trial Goldberg et al12 reported that all non–HCV-infected patients who received kidneys from HCV-viremic donors with genotype 1 infection and who received HCV treatment achieved sustained virologic response (SVR) 12 and had an excellent graft function and patient survival 1 y posttransplantation with a similar glomerular filtration rate at 6 and 12 mo when compared with matched recipients of HCV-negative kidneys. In 2018, Durand et al13 also showed that with prophylactic treatment using DAA therapy in the Exploring Renal Transplants Using Hepatitis C Infected Donors for HCV-negative Recipients trial, all 10 Hep C–naive patients who received HCV-positive kidneys achieved SVR12 and had an excellent graft and patient survival. Both trials were done in a research setting. Since then, there have been multiple small studies in the literature that demonstrated the “real-world” safety of these transplants and excellent outcomes.14,15 Jandovitz et al15 showed that HCV NAT-negative recipients can be safely and successfully transplanted with HCV NAT-positive donor kidneys outside of a research protocol. They reported on 25 HCV NAT-positive donor kidney transplants with all patients achieving initial SVR12 with 1 patient requiring retreatment to achieve SVR12. In this study, the death censored graft survival was 96% at 1 y. They also noted that in their study, the recipients of HCV NAT-positive organs compared with HCV NAT-negative organs received younger donors (mean 35 ± 8.9 versus 45.1 ± 15.7 y; P < 0.01). Because of the younger age and fewer donor comorbidities, the quality of these organs tend to be better with better graft survival when stratified by KDPI of these organs.

Even though the excellent outcomes are reported with HCV kidney transplantation, few concerns have been raised. Kapila et al16 presented an experience with 2 cases of fibrosing cholestatic hepatitis posttransplantation in HCV-negative recipients who underwent kidney transplantation from viremic donors. Both subsequently responded to DAA therapy. Immune complex injury to the allograft resembling membranoproliferative glomerulonephritis and possible increased risk of rejection have been described as adverse posttransplant events with viremic organs.7 Also, the cost of DAA therapy and potential logistical challenges obtaining DAA medications are factors that should be carefully taken in consideration.

Despite mounting evidence of excellent outcomes with HCV-viremic kidney transplantation, there are still concerns from providers and the candidates when it comes to acceptance of these organs. Couri et al17 demonstrated that some providers continued to believe that a HCV-positive organ reduced the odds of a successful transplant at 1-y posttransplant. Less than half of providers believed in offering HCV-positive kidney transplantation for routine care rather than for research. This can also be seen in the listing practices for Hep C–positive kidney donors. Analysis of OPTN database demonstrated that while the number of kidney transplant candidates listed for Hep C NAT-positive kidneys increased between 2013 and 2021, it remains low. Only 25% of patients in the EPTS group, 61%–100% were listed for viremic Hep C–positive kidneys.

Our findings show that in the kidney transplant candidates with EPTS 61%–100%, the patient survival significantly improved from 55.9% to 67.4% at 5 y if they were to receive Hep C–viremic organs when compared with high KDPI >85% kidneys. Although KDPI >85% kidneys offer increased survival to this group over remaining on the waiting list, transplantation with Hep C–positive kidneys improves the survival even further.

Our analysis has limitations, including the inherent limitations of a large national dataset, including miscoding and the interpretation of prior actions to predict future events. We also chose to mostly study EPTS and KDPI, realizing that there are other important factors that influence patient and graft survival. Additionally, the Hep C NAT+ status of the recipients is lacking in the national database making it difficult to study the current allocation of the viremic Hep C NAT+ organs and the patient and graft survival post–kidney transplantation in this set of patients.

In conclusion, our results provide evidence that there is a survival benefit when the kidneys from Hep C donors both viremic and aviremic are being utilized. These findings could be used when the candidates are being counseled on the types of kidneys they could consider for transplantation that could potentially improve their outcomes. We believe the consideration should be given to both viremic and aviremic Hep C–positive kidneys in the era of DAA therapy in candidates with EPTS score above 60%. Although progress is being made, we encourage continued reevaluation of listing practices for Hep C NAT-positive kidney allografts.

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