Variations in Risk of Cancer and Death From Cancer According to Kidney Allograft Function, Graft Loss, and Return to Dialysis : Transplantation

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Original Clinical Science—General

Variations in Risk of Cancer and Death From Cancer According to Kidney Allograft Function, Graft Loss, and Return to Dialysis

Au, Eric H.K. PhD1,2,3; Chapman, Jeremy R. PhD2; Teixeira-Pinto, Armando PhD1,3; Craig, Jonathan C. PhD4; Wong, Germaine PhD1,2,3

Author Information
Transplantation ():10.1097/TP.0000000000004493, January 23, 2023. | DOI: 10.1097/TP.0000000000004493
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Abstract

INTRODUCTION

Cancer is one of the most common causes of death in patients after kidney transplantation.1 Previous studies have shown a 2- to 3-fold increased risk of cancer and cancer-related mortality in patients after kidney transplantation compared with the age- and sex-matched general population.2-4 This increased cancer risk in kidney transplant recipients has been attributed to the direct effects of immunosuppressive medications, the proliferation of oncogenic viruses, and the effects of reduced kidney function.5,6

Although the increased risk of cancer after kidney transplantation is well described and characterized from observational and registry data, few studies have explored the risk of cancer in patients after kidney graft loss and how the risk changes as patients transition from having a functioning kidney transplant to graft loss and return to dialysis and to subsequent kidney transplants.7,8 Also, prior studies have not investigated the changes in the risk of cancer death during times with allograft function and after graft loss.

An understanding of the risk of cancer and cancer-related death, as patients progress through different modalities of kidney replacement therapy, may help guide preventative and treatment decisions, such as cancer screening and the management of immunosuppression after allograft loss and return to dialysis. This study aims to evaluate the risk of cancer incidence and cancer mortality along the patient journey—from dialysis to kidney transplantation, to graft loss and return to dialysis, and subsequent transplantation—and compare this risk with the age- and sex-matched general population.

MATERIALS AND METHODS

Study Population and Data Collection

All Australian patients aged 20 y or above who commenced kidney replacement therapy between 1982 and 2014 were included in the Australia and New Zealand Dialysis and Transplant (ANZDATA) Registry. The ANZDATA Registry collects data on all patients on dialysis and kidney transplant recipients as reported regularly by renal units across Australia and New Zealand. Data collected include age, sex, ethnicity, cause of kidney failure, year of starting kidney replacement therapy, and treatment modality (hemodialysis, peritoneal dialysis, kidney transplantation). Immunosuppression medication use is collected in the ANZDATA Registry for patients with a functioning kidney transplant but not collected for patients on dialysis or after graft loss. Events collected include changes in dialysis modality, transplantation date/s, date/s of graft loss, and death.

For this analysis, patient follow-up time was divided into separate periods based on the modality of kidney replacement therapy: dialysis (without previous kidney transplant), first functioning kidney transplant, dialysis after first graft loss (ie, after loss of the first kidney transplant), second functioning kidney transplant, and dialysis after second graft loss (ie, after loss of the second kidney transplant). Thus, individual patients can contribute follow-up time to several treatment periods as they transition between different modalities of kidney replacement therapy, for example, as the patient moves from dialysis to first transplantation, to graft loss (and subsequent treatment). To minimize carry-over effects from a previous modality of kidney replacement therapy, patients with cancer diagnosed before or within 90 d of a change in treatment modality (transplantation or graft loss) were excluded from the subsequent period. Patients were censored at the time of receiving a third kidney transplant or loss to follow-up.

Ascertainment of Cancer Outcome

All incident cancers and cancer-related deaths are reported to the ANZDATA Registry regularly by renal units, including cancer type, location, date of diagnosis, and treatment. The first diagnosis of non-melanoma skin cancer is also recorded. Previous studies have demonstrated the accuracy and completeness of cancer and mortality reporting to the ANZDATA Registry, with a high concordance rate found when compared with mandatory reporting to cancer and death registries.9,10 For comparison with the Australian general population, cancer incidence and mortality data for the age- and sex-matched Australian general population was obtained from the Australian Institute of Health and Welfare.11

Statistical Analysis

Crude cancer incidence and mortality rates for patients during each treatment period (ie, dialysis, functioning transplant, and after graft loss) were calculated. Cumulative cancer incidence and cancer mortality were calculated using the Aalen-Johansen method, which takes into account competing events. Death and changes in treatment modality were considered competing events for cancer incidence. Death from other causes were considered competing events for cancer mortality. Standardized incidence ratios (SIRs) and standardized mortality ratios (SMRs) for cancer (excluding non-melanoma skin cancer) were calculated using indirect standardization by age group (20–34, 35–49, 50–64, and over 65 y old), sex, and year of death (1982–2014 in 5-y periods). All analyses were performed in SAS version 9.4 (SAS Institute) and R version 3.6.0 (R Foundation).

Ethics Statement

This study was exempt from institutional review board approval. ANZDATA Registry uses an opt-out consent process for data collection. All patients are provided information on the registry and provided the opportunity to opt-out of the registry.

RESULTS

Between 1982 and 2014, we identified 44 765 patients who commenced dialysis (without previous transplantation), 13 443 patients who received a first kidney transplant (including 1202 pre-emptive kidney transplants), 2951 patients who returned to dialysis after the loss of their first kidney transplant (first graft loss), 1010 patients who received a second kidney transplant, and 279 patients who returned to dialysis after loss of their second kidney transplant (second graft loss) (Figure 1). There was a total of 274 660 person-years of follow-up, comprising 149 302 person-years for patients on dialysis, 106 723 person-years for patients with a first transplant, 10 268 person-years for patients on dialysis after first graft loss, 7212 person-years for patients with a second transplant, and 1155 person-years for patients on dialysis after second graft loss. The median duration (and interquartile range [IQR]) of follow-up was 2.4 (IQR 1.1–4.7) y for dialysis, 6.5 (IQR 2.6–11.9) y for first transplant, 2.3 (IQR 0.8–4.9) y for dialysis after first graft loss, 5.6 (IQR 2.2–10.5) y for second transplant, and 2.9 (IQR 1.1–6.2) y for dialysis after second graft loss.

F1
FIGURE 1.:
Flow diagram of study cohort.

Baseline Characteristics of the Study Cohort

The baseline characteristics for patients at the start of each treatment period are shown in Table 1. The majority of patients in each treatment period were male, with a median age of 59.0 (IQR 47.0–70.0) y for dialysis, 47.5 (IQR 37.0–56.6) y for first transplant, 49.0 (IQR 39.3–58.4) y for dialysis after first graft loss, 45.4 (IQR 37.4–54.3) y for second transplant, and 45.6 (IQR 38.5–54.6) y for dialysis after second graft loss. Over 75% of patients were European Australians across all treatment periods, with <10% of patients of Indigenous Australian ethnic background. The most common causes of kidney failure were glomerulonephritis and diabetes for patients across all treatment periods.

TABLE 1. - Baseline characteristics for patients in each treatment period
Dialysis, n (%) First transplant, n (%) First graft loss, n (%) Second transplant, n (%) Second graft loss, n (%)
Total 44 765 (100.0) 13 443 (100.0) 2951 (100.0) 1010 (100.0) 279 (100.0)
Sex
 Male 26 321 (58.8) 8249 (61.4) 1790 (60.7) 632 (62.6) 173 (62.0)
 Female 18 444 (41.2) 5194 (38.6) 1161 (39.3) 378 (37.4) 106 (38.0)
Age
 20-34 4164 (9.3) 2820 (21.0) 488 (16.5) 179 (17.7) 41 (14.7)
 35-49 8934 (20.0) 4814 (35.8) 1076 (36.5) 459 (45.5) 135 (49.4)
 50-64 13 657 (30.5) 4769 (35.5) 1029 (34.9) 322 (31.9) 87 (31.2)
 65 or over 18 010 (40.2) 1040 (7.7) 358 (12.1) 50 (5.0) 16 (5.7)
 Mean ± SD 57.7 ± 15.5 46.7 ± 12.5 48.7 ± 12.7 45.9 ± 10.8 46.7 ± 10.9
Ethnicity
 European Australians 34 943 (78.1) 11 367 (84.6) 2484 (84.2) 904 (89.5) 251 (90.0)
 Indigenous 4016 (9.0) 480 (3.6) 171 (5.8) 28 (2.8) 12 (4.3)
 Other 5806 (13.0) 1596 (11.9) 296 (10.0) 78 (7.7) 16 (5.7)
Cause of kidney failure
 Glomerulonephritis 11 460 (25.6) 3572 (26.6) 811 (27.5) 291 (28.8) 88 (31.5)
 Vascular 5425 (12.1) 1633 (12.2) 357 (12.1) 121 (12.0) 37 (13.3)
 Polycystic kidney disease 2964 (6.6) 874 (6.5) 184 (6.2) 54 (5.4) 12 (4.3)
 Reflux 1734 (3.9) 499 (3.7) 108 (3.7) 39 (3.9) 9 (3.2)
 Diabetes 13 311 (29.7) 3845 (28.6) 843 (28.6) 299 (29.6) 87 (31.2)
 Other 9871 (22.1) 3020 (22.5) 648 (22.0) 206 (20.4) 47 (16.5)
Comorbidities
 Chronic lung disease 6335 (15.4) 571 (4.6) 96 (3.8) 19 (2.0) 5 (2.1)
 Coronary artery disease 16 221 (39.3) 1297 (10.6) 239 (9.6) 33 (3.6) 11 (4.7)
 Peripheral vascular disease 10 539 (25.6) 756 (6.1) 144 (5.7) 22 (2.4) 7 (2.9)
 Cerebrovascular disease 5996 (14.6) 398 (3.2) 79 (3.1) 16 (1.7) 1 (0.4)
 Diabetes 16 874 (40.4) 2216 (17.6) 445 (17.0) 67 (7.0) 22 (8.6)
Smoker (current or former) 21 312 (47.6) 5098 (37.9) 1077 (36.5) 342 (33.9) 97 (34.8)

Cancer Incidence

A total of 2335 (5.2%) patients on dialysis (without previous transplant), 1669 (12.4%) patients with a first kidney transplant, 122 (4.1%) patients who were on dialysis after first graft loss, 110 (10.9%) patients with a second kidney transplant, and 19 (6.8%) patients who were on dialysis after second graft loss were diagnosed with cancer. The median time to cancer diagnosis from the start of each treatment period was 2.4 (IQR 1.1–4.4) y for patients on dialysis, 6.7 (IQR 3.0–11.3) y for patients with a first transplant, 2.9 (IQR 1.3–5.6) y for patients on dialysis after first graft loss, 5.6 (IQR 2.6–11.8) y for patients with a second transplant, and 3.9 (IQR 1.7–9.6) y for patients on dialysis after second graft loss.

The crude cancer incidence rate (per 100 000 person-years) was 1564 for patients on dialysis (without previous transplant), coincidentally also 1564 for patients with a first transplant, 1188 for patients on dialysis after first graft loss, 1525 for patients with a second transplant, and 1645 for patients on dialysis after second graft loss, compared with 626 for the general population. The 5-y cumulative incidence of cancer was 4.5% (95% confidence interval [CI], 4.2%-4.7%) for patients on dialysis, 4.8% (95% CI, 4.4%-5.2%) for patients with a first transplant, 3.3% (95% CI, 2.6%-4.0%) for patients on dialysis after first graft loss, 5.2% (95% CI, 3.8%-5.8%) for patients with a second transplant, and 4.3% (95% CI, 2.2%-7.3%) for patients on dialysis after second graft loss, as shown in Figure 2A.

F2
FIGURE 2.:
Cumulative (A) and standardized (B) cancer incidence and cumulative (C) and standardized (D) cancer mortality by treatment period.

Compared to the general population, the SIR for cancer was 1.15 (95% CI, 1.11-1.20) for patients on dialysis (without previous transplant), 2.03 (95% CI, 1.94-2.13) for patients with a first transplant, 1.55 (95% CI, 1.29-1.85) for patients on dialysis after first graft loss, 2.18 (95% CI, 1.79-2.63) for patients with a second transplant, and 2.59 (95% CI, 1.56-4.04) for patients on dialysis after second graft loss, as shown in Figure 2B.

Cancer Mortality

There were a total of 1135 (2.5%) cancer-related deaths in patients on dialysis, 735 (5.5%) in patients with a first transplant, 40 (1.4%) in patients on dialysis after first graft loss, 50 (5.0%) in patients with a second transplant, and 9 (3.2%) in patients on dialysis after second graft loss. The median time from the start of each treatment period to cancer death was 3.3 (IQR 1.8–5.7) y for patients on dialysis, 8.5 (IQR 5.0–12.5) y for patients with a first transplant, 3.9 (IQR 1.9–6.6) y for patients on dialysis after first graft loss, 8.7 (IQR 4.7–13.4) y for patients with a second transplant, and 4.7 (IQR 3.7–9.7) y for patients on dialysis after second graft loss.

The crude cancer mortality rate (per 100 000 person-years) was 760 for patients on dialysis (without previous transplant), 689 for patients with a first transplant, 390 for patients on dialysis after first graft loss, 693 for patients with a second transplant, and 779 for patients on dialysis after second graft loss, compared with 258 for the general population. The 5-y cumulative mortality from cancer was 2.1% (95% CI, 1.9%-2.2%) for patients on dialysis, 1.6% (95% CI, 1.4%-1.9%) for patients with a first transplant, 1.1% (95% CI, 0.8%-1.6%) for patients on dialysis after first graft loss, 1.5% (95% CI, 0.9%-2.6%) for patients with a second transplant, and 2.1% (95% CI, 0.8%-4.6%) for patients on dialysis after second graft loss, as shown in Figure 2C.

Compared to the general population, the SMR for cancer-related deaths was 1.29 (95% CI, 1.21-1.36) for patients on dialysis (without previous transplant), 2.50 (95% CI, 2.33-2.69) for patients with a first transplant, 1.40 (95% CI, 1.00-1.90) for patients on dialysis after first graft loss, 3.00 (95% CI, 2.23-3.96) for patients with a second transplant, and 3.82 (95% CI, 1.75-7.25) for patients on dialysis after second graft loss, as shown in Figure 2D.

DISCUSSION

In this registry-based cohort study of dialysis and transplant patients comprising 274 660 total person-years of follow-up, the overall risk of cancer and cancer mortality doubled during periods with a functioning first or second kidney transplant, compared to the age- and sex-matched general population. After the loss of the first kidney transplant and return to dialysis, there was a reduction in the relative cancer incidence and mortality risk compared with recipients with a functioning first kidney transplant, but these estimates remained higher than that of the general population. In contrast, the overall cancer incidence and cancer death risk ratio remained elevated after the loss of the second allograft, with an excess risk of at least 2.5 and 3.5 times for cancer incidence and cancer-related death compared with the general population.

The heightened risk of cancer in recipients after kidney transplantation is well supported by evidence from observational and registry analyses.2-4 However, relatively few studies have examined the risk of cancer and cancer mortality in patients after kidney transplant allograft loss.7,8 In an analysis of transplant registry and linked cancer data from the United States, cancer incidence was found to change in an alternating, “seesaw” pattern between periods with a functioning kidney transplant and periods of graft loss, particularly for cancers associated with infection or immunosuppression.8 Similarly in an earlier analysis of 8173 Australian kidney transplant recipients from the ANZDATA Registry, the incidence rates of cancers associated with immunosuppression and infection, such as Kaposi’s sarcoma, non-Hodgkin lymphoma, and melanoma were found to be elevated in patients with a kidney transplant, but the incidence of these cancers decreased after allograft loss and return to dialysis.7 These studies also found that the incidence of cancers associated with reduced kidney function and kidney failure, such as thyroid cancer, kidney cancer, and urinary tract cancer, remained elevated in both patients with a functioning kidney transplant and those after graft loss.7,8 In this current analysis, we reported the changing overall cancer mortality risk over periods of graft function and dysfunction and found a “seesaw” pattern similar to that seen previously for cancer incidence, with a higher observed mortality risk seen as patients transitioned from dialysis (or graft loss) to first or second kidney transplantation, and a relatively lower cancer incidence and mortality risk is seen as patients transitioned from first kidney transplant to first graft loss. A reduction in cancer risk for patients on dialysis after second graft loss was not observed in the current study, suggesting ongoing increased cancer burden despite reduction and withdrawal of immunosuppression.

There are several possible reasons that may have contributed to the observed changes in cancer incidence and mortality risk as patients progress from dialysis to kidney transplantation, to graft loss, and further kidney transplants. Variations in the observed cancer risk may reflect the changes in immunosuppression doses as patients transition between a functioning kidney transplant to graft loss. A gradual reduction in immunosuppression doses may occur as transplant recipients transition from having a functioning graft to graft loss and return to dialysis. Therefore, the association between changes in graft function and cancer risk may be confounded by changes in the level of immunosuppression. Chronic immunosuppression use is associated with an increase in virus-associated cancers such as cervical cancer (human papillomavirus) and post-transplant lymphoproliferative disorder (Epstein Barr virus); and several immune-related cancers such as melanoma.3,4,6 In Australia, immunosuppressive therapies are often reduced or withdrawn over time after kidney graft loss, with patients generally remaining on only low-dose prednisolone in the longer term.12,13 This reduction in immunosuppression after graft loss may correlate with the lower cancer risk seen in those who experienced their first graft loss (SIR and SMR of 1.4–1.5) compared with patients with a functioning first or second transplant (SIR and SMR > 2). Although the cancer incidence and mortality ratios for patients after second graft loss were less precise, as there were only few patients with cancer after second graft loss in our cohort, the overall cancer risk remained elevated in our cohort after return to dialysis with second graft loss. This observed elevated cancer risk in patients on dialysis after second graft loss may be the result of the cumulative effects of immunosuppression use over time and the deleterious effects of chronic immunosuppression from the 2 previous kidney transplants.

In addition to changes in immunosuppression, patients who experienced graft loss and return to dialysis may be burdened with one or more co-existing comorbid conditions such as cardiovascular disease. These competing events may also affect their overall survival and thus the observed incidence of cancer. Prior studies have reported an up to 3-fold relative increase in overall mortality risk in patients after graft loss compared to those with a functioning kidney transplant.14-17 A study of 78 564 patients from the United States Renal Data System found a 7-fold and 4-fold increased risk of cardiovascular and infection-related death in patients after graft loss compared to patients with a functioning kidney transplant.15 This observed increased risk of death after graft loss, in particular cardiovascular mortality, may be due to the accelerated atherosclerosis and progression of cardiovascular disease from loss of kidney function.18 The reduced survival after transplant graft loss is observed in the current study with shorter median follow-up duration in patients after first and second graft loss (2.3 y and 2.9 y, respectively) compared to patients with a functioning first or second kidney transplant (6.5 y and 5.6 y, respectively). The increased risk of other competing causes of death including cardiovascular death after graft loss may explain the lower observed rates of cancer incidence and cancer death for patients on dialysis after first graft loss.

Furthermore, there is likely to be selection and survival bias in patients as they transition between each treatment period. Patients on dialysis (without previous transplant) in this study were older on average compared to patients who have received a kidney transplant (or a kidney transplant with subsequent graft loss). This likely contributed to the relatively high unadjusted cancer incidence and mortality in dialysis patients (without previous transplants) compared to patients who have received a kidney transplant; after standardization by age and sex, the SIR and SMR for dialysis patients without previous transplants were then lower than that of patients who received a first kidney transplant. Additionally, the rigorous selection process before kidney transplantation suggests that these patients in later treatment periods were likely to have different characteristics from those in earlier treatment periods. For example, patients who received a kidney transplant were younger and have less comorbidities compared with those who were deemed ineligible to receive a kidney transplant. These differences in patient characteristics, apart from age and sex, were not accounted for in the analysis using SIR and SMR and may have contributed to differences in observed cancer risk across different treatment periods. There is also likely to be survival bias in the estimates for patients in later treatment periods. These patients have survived through earlier treatment periods and have avoided cancer complications during these earlier treatment periods. Thus, the estimates of cancer risk for these later treatment periods in our study may be an underestimate of patients’ true cancer risk.

This study has several strengths and potential limitations. There was comprehensive data on a population-based cohort of dialysis and transplant patients using a binational dialysis and transplant registry, including robust data on periods of transplant function and graft loss, and over 30 y of follow-up and cancer and mortality outcome data. However, although we compared the cancer incidence and mortality risk with the general population using indirect standardization for age and sex, we were unable to further explore other important factors that may have contributed to the increased cancer risk and death in this population, such as smoking status. We were not able to directly assess the effect of changes in immunosuppression from transplantation and graft loss on cancer risk, as granular details of immunosuppression such as dosing and drug levels were not collected by the ANZDATA Registry for patients on dialysis and patients after graft loss. There was insufficient power with a limited number of cancers, particularly in patients with second transplants and after second graft loss to allow analysis of the variations in cancer incidence for specific cancer types. Further studies exploring the factors associated with cancer after kidney transplant graft loss may improve our understanding of the specific mechanisms of increased cancer risk and cancer mortality in this population, particularly in patients who experience kidney graft loss after a second kidney transplant.

In summary, this study identifies kidney transplantation carries a life-long increased risk of cancer, irrespective of the fate of the graft and despite stopping immunosuppression. Strategies to reduce that risk should thus be implemented before the first transplant and importantly be continued after graft loss, including pretransplant and posttransplant screening for cancer and reducing potential carcinogenic exposures including smoking and the use of effective vaccines against viruses that cause cancer in high-risk transplant individuals (such as vaccines against human papillomavirus for cervical cancer). Improving the uptake of cancer screening, which has been found to be low in transplant recipients,19,20 is another strategy to reduce the burden of cancer. This may be achieved by improving patients’ knowledge and access to screening and a shared decision-making process to support patients in cancer screening. Finding the right time to reduce or stop immunosuppressants in transplant recipients with a failing or failed allograft, and to start transition to dialysis or a second transplant is also a challenge. Many of these decisions require detailed considerations of the competing concerns of preservation of residual kidney function and the risk of complications and toxicity such as infections and cancers associated with long-term immunosuppressant use. This study identifies the need to further research the optimal use of immunosuppressants in kidney transplantation, particularly after loss of graft function, to minimize the adverse impacts of immunosuppression on long-term cancer risk post-transplant and after graft loss.

ACKNOWLEDGMENTS

The authors would like to acknowledge the contributions of all renal units throughout Australia and New Zealand, whose contributions to Australia and New Zealand Dialysis and Transplant Registry make this work possible.

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