Tumors after kidney transplantation: a population study

doi:10.21203/rs.3.rs-2185598/v1

Download PDF

Research Article

Tumors after kidney transplantation: a population study

https://doi.org/10.21203/rs.3.rs-2185598/v1

This work is licensed under a CC BY 4.0 License

Journal Publication

published 23 Jan, 2023

Read the published version in World Journal of Surgical Oncology →

You are reading this latest preprint version

One of the main causes of post-transplant-associated morbidity and mortality is cancer. The aim of the project was to study the neoplastic risk within the kidney transplant population and identify the determinants of this risk.

A cohort of 462 renal transplant patients from 2010 to 2020 was considered. The expected incidence rates of post-transplant cancer development in the referenced population, the standardized incidence ratios (SIR) taking the Italian population as a comparison, and the absolute risk and the attributable fraction were extrapolated from these cohort of patients.

Kidney transplant recipients had an overall cancer risk approximately three times that the one of the local population (SIR 2.8). A significantly increased number of cases were observed for Kaposi's sarcoma (KS) (SIR 195) and hematological cancers (SIR 6.8). In the first 3 years post-transplant, the risk to develop either KS or hematological cancers was four times higher than in the following years; in all cases of KS, the diagnosis was within 2 years from the transplant.

Post-transplant immunosuppression represents the cause of 99% of cases of KS and 85% of cases of lymphomas, while only 39% is represented by solid tumors.

Data related to the incidence, the percentages attributable to post-transplant immunosuppression and the time of onset of neoplasms, particularly for KS and hematological tumors, could help improving the management for the follow-up in these patients.

cancer risk

transplant

immunosuppression

population study

Kidney transplantation significantly increases life expectancy and life quality when compared to dialysis in end stage renal disease patients (ESRD) (1–3). However, the use of immunosuppressive drugs that are needed to prevent graft loss, is directly associated with an increased frequency of infections and cancers, which are one of the main causes of morbidity and mortality in transplanted patients (4). Nowadays post-transplant malignancy is the third most common cause of death in renal transplant recipients, with some malignancies occurring at much higher rates compared to the general population. Prolonged exposure to immunosuppressive drugs seems to adversely affect the antitumor immune surveillance capacity and enhance the carcinogenic effect of some risk factors, such as ultraviolet rays. Furthermore, some immunosuppressive drugs appear to promote carcinogenesis independently from the immunosuppressive mechanism (5, 6).

Taking advantage of the recently acquired knowledge in carcinogenesis, the quantification of cancer risks in transplanted recipients could add an important layer when programming the follow-up screenings in these patients. We need to take into consideration that the risk of developing a new cancer may vary depending on the type or location where the cancer will arise.

Moreover, there is an increased risk to develop a “common” type of cancer in a transplanted patient, because the current global impact is already high per se, than develop a more rare one (7).

Several studies have showed an inversely age-related risk of developing malignancies after transplantation, where younger recipients experience a much greater relative risk than older recipients (risk increased 15–30 times for children, but double for those transplanted over 65 years) (8, 9). In addition, the risk of developing a new post-transplant cancer is estimated about 40% for those patients who already have another tumor in their clinical history (7). Regarding the various types of cancer, the relative increase in incidence is most significant for Kaposi's sarcoma (KS), non-melanoma skin cancer, and lymphoma. In contrast, the risk of ovarian, prostate and multiple myeloma cancers would not seem to be increased (10).

Transplant patients are also vulnerable to viral infections or the reactivation of latent infections, which can be considered one of the reasons of tumorigenesis in these subjects. Among these viruses that can cause initiation of malignancies we can find; Epstein-Barr virus (EBV), Human herpesvirus 8 (HHV-8), Human Papillomavirus (HPV), Merkel Cell Polyomavirus, Hepatitis B virus (HBV), and Hepatitis C virus (HCV). There is a linear correlation between the speed at which some malignant tumors develop, even after transplantation, and the initiation of immunosuppression, that could be related with an uncontrolled viral replication. In support of this hypothesis, previous studies have demonstrated that, recipients whose transplanted kidney have been removed due to failure, or after reduction or cessation of immunosuppression, have lowered the risks of developing virus-induced cancers at levels observed in pre-transplant dialysis patients (11).

Post-transplant KS may arise from reactivation of latent HHV-8 infection in endemic areas, or acquisition of a new infection in non-endemic areas. An example of the first case was described by Luppi et al. in 2000, where the formation of a KS post-transplantation was due to an infected donated kidney which lead to a new acquisition of HHV-8 infection in the recipient (12). Barozzi et al. in 2006, reported an episode of KS in a transplanted patient deriving from the reactivation of a latent HHV-8 infection of a donated kidney (13).

EBV is also frequently associated in renal transplantation, being an ubiquitous viral pathogen, with a seroprevalence of more than 90% in adults. After primary infection, the virus persists within B lymphocytes for life with the majority of hosts demonstrating no evidence of active infection or replication. However, in kidney transplant recipients both acute infection and reactivation of latent infection may lead to pathology, with clinical syndromes associated with non-neoplastic viral replication on one end, and EBV-mediated neoplastic transformation, including post-transplantation lymphoproliferative disorder, on the other.

Not only does the risk of developing de novo cancer increases after kidney transplantation, but the prognosis for recipients diagnosed with post-transplantation cancer worsen compared to a non-transplanted patient.

Most of the tumors diagnosed in transplant recipients have more aggressive behaviour, as evidenced by the Israel Penn Registry, which has shown that mean survival for certain cancers, such as colon, lung, breast, prostate, and bladder cancer, is significantly lower in transplanted patients than in the general population (7).

The Australian and New Zealand Dialysis and Transplant Registry demonstrated that, transplanted women that underwent kidney transplantation and developed breast cancer have excess mortality of at least 40% compared to women with breast cancer in the general population (14–16). In a Dutch study, the median survival of kidney transplant recipients after cancer diagnosis was only 2.7 years, compared with an average survival of 8.3 years in cancer-free recipients (17).

Another consideration that should be attentioned is the phenomenon of “chimerism”, although is a concept that it is still debated. In fact, in addition to “de novo” tumors, although rare, tumors "donor transmitted" (DTT) and "donor derived" (DDT) are clearly described in scientific literature (18–21).

The transplant recipient is a chimera subject when two cellular populations exist. When a tumor develops shortly after transplantation, a transmission of malignancy from the donor should be considered, despite the accurate screening for the already ongoing neoplastic diseases before donation. An arbitrary 2-y cut-off time was stated to separate “donor-transmitted” from “donor derived” tumors, the latter arising from donor cells but not present at the time of transplant. However, 31% of donor-transmitted tumors arose after 24 months, emphasizing the need for continued surveillance beyond the conventional 2-y (22).

According to the data available, the risk of having a donor with undetected malignancy is 1.3% and the following risk of cancer transmission is 1% (18).

The “donor derived” tumors are extremely rare. In scientific literature there are few cases of DDT developed outside the graft with the genome of the donor who never experienced malignancy before. Between the tumors developed in the recipients through this modality we can find skin tumors, acute promyelocytic leukemia, Kaposi’s sarcoma, small cell carcinoma, hepatocellular carcinoma and pancreatic adenocarcinoma (18, 23–27).

Few cases of tumors developed on the graft but originated from cells of the recipient that cannot be considered the result of a metastasization process have been described. Among them we can find renal cell tumors developed on the renal graft several years after transplantation (28–32).

Studying chimerism of tumors in transplant recipients could be extremely useful and should be advised in order to identify chimeric cells within these neoplasms. This identification could lead to findings on (1) the mechanism of migration of these chimeric cells into the cancer, and particularly, what could be the triggering factor initiating this migration, and (2) identify the cells that start the chimeric process which lead to migration of chimeric cells into the tumor (33).

In conclusion, a transplanted patient who develops a donor-derived tumor might be a useful model to distinguish between tumor cells derived from the donor, and the ones of the recipient within the same organ where the tumor arose, that still show a normal phenotype. This might allow to potentially recapitulate the tumor phylogenesis.

By identifying the migrated cells from the dornor organ into the recipient body, if they will give rise to a tumor, these will be recognizable as donor-derived progenitor cells by the fact that they will still possess the donor genotype. This will allow us to potentially study, through our proposed model, the hierarchy of how a tumor develop into the recipient taking advantage of the genotypical differences between donor and recipient genotype.

This study analyzed patients' data transplanted at an Italian Transplant Center (ASST Sette Laghi, Varese, Italy) between January 1st, 2010 and December 24th, 2020.

A retrospective cohort of 462 renal transplant patients was considered.

Information were collected taking into consideration socio-demographic aspects (sex, date of birth), clinical history (including the presence of tumors before transplantation), and the diagnosis of tumors in the post-transplant period and current clinical conditions, from clinical records related to transplantation and post-transplant outpatient visits.

The neoplastic risk was calculated based on the reference to the first diagnoses of cancer. Cancer diagnoses were classified using the International Classification of Disease vers. 10 (ICD-10).

Statistical analysis data was performed using Microsoft Office – Excel® 2019, MedCalc® 19.5.3.

The cancer risk period (expressed in person-years, PY) was calculated from the 30th day following the date of transplant up to the date of cancer diagnosis, death, last follow-up, or the end date of the study (03.31.2021).

The reference population used to compare the incidence of tumors in transplanted patients was the population of the Province of Varese (Italy) of the same age and sex. The SIR, obtained by dividing the number of cases of cancers observed by the number of expected cases, was used. The number of expected cancers was obtained by multiplying the transplant recipients' PYs at cancer risk by the sex-specific and age-specific incidence rates found in the cancer registries of the International Agency for Cancer Research (IARC, vol XI) that referred to the population of the Province of Varese. For the SIR, exact 95% confidence intervals (95% CI) were calculated according to the Poisson distribution. Estimates of the SIR and relative confidence intervals were made for the total number of patients and by gender.

The expected rates of incidence in the reference population were also calculated and, based on these, the absolute risk (AR) (i.e., the excess incidence of cancer due to kidney transplantation) and the attributable fraction (AF) were derived. The risk factors associated with the onset of cancer were also evaluated (8).

The method used to calculate a confidence interval for the difference between two proportions is the Newcombe-Wilson method without continuity correction (1998). The confidence limits for the number needed to be treated are the inverse of the limits for the AR reduction. Confidence intervals for relative risk (RR) and odds ratios (OD) are calculated using the methods described by Armitage and Berry (Armitage P and Berry G (1994): Statistical Methods in Medical Research (3rd ed.). London: Blackwell, p 131). The RR reduction and its confidence limits are one minus the relative risk and its confidence limits.

A total of 462 kidney transplant recipients [313 male (67.7%), 149 females (32.3%)], mean age at the time of transplantation of 54 ± 11 years (range 19-76), with a follow-up time up to 2562.5 person-years for the total population (1714.3 for the male, 848.3 for the female) were included in this analysis.

Twenty-eight people (20 male, 8 females; 6% of the total) developed cancer (819.5 cases /100,000 PY). Table 2 shows the distribution of tumor types and the corresponding SIR. The most frequent types were non-melanoma skin cancers (7 cases), KS (5), hematological tumors (5), and urinary tract tumors (4).

Kidney transplant recipients showed an overall risk of cancer that was about three times (SIR 2.8; 95% CI 1.8-4.3) compared to the local population, with an overall risk for males of about double (SIR 2.3; 95% CI 1.3-4.0) and for females over triple (SIR 3.7; 95% CI 1.8-7.5). Significantly increased risks in both sexes were observed for KS (SIR 195), Lymphomas and Leukemias (SIR 6.8) (Table 1).

Overall, the incidence rate of tumors attributable to post-transplant immunosuppressive therapy was 819 cases/100,000 PY. In particular, the incidence rates for KS and Lymphomas were largely attributable to post-transplant immunosuppression, while the incidence attributable to post-transplant immunosuppression for solid tumors was just over one-third of the overall incidence (162 cases/100,000 PY out of a total of 429 cases/100,000 PY) (Figure 1).

Cancer risk increased significantly with age, while women showed a reduced risk, although not statistically significant, compared to men. Other significant associations concerned the period of tumor development after transplantation and the initiation of immunosuppressive therapy: in the first 3 years post-transplant, the risk was four times higher than in the subsequent years.

KS was diagnosed in 5 recipients at a median of 6.4 months (range 2-24) after transplant. Lesions were localized only to the skin of the extremities in 3 patients, to the skin and gastric mucosa in 1 patient, and to the inguinal lymph node in another patient. Four patients were positive at the HHV-8 serologic testing included in pre-transplant screening, while one recipient was not tested. HHV-8-DNA at KS diagnosis was detected positive in 3 recipients (Table 2).

Twenty-seven people (5.8% of the total) developed a benign neoplastic form or a precancerous lesion: of these 10 were skin lesions (3 lipomas, 2 dysplastic nevi, 2 hemangiomas, 1 neurofibroma, 1 poroma, 1 polyp fibroepithelial), 7 cellular atypia of the urinary tract with 1 bladder submucosal leiomyoma, 5 gastrointestinal lesions (4 colorectal adenomas, 1 gastric glandular polyp), 2 lung lesions (endobronchial metaplasia with dysplasia), 1 benign thyroid nodule, 1 leiomyoma ovarian, 1 condyloma acuminata.

The overall increase in cancer risk found in our study (2.8 times) is in line with the published data of SIR for cancers related to kidney transplantation, taken from national population-based studies (7, 34).

Our results also estimate a 6-fold increase in the risk of hematological cancers, slightly underestimated compared to studies from Australia, Canada, and the United States, where an increased risk of developing lymphomas was related particularly to post-transplant lymphoproliferative disorders (PTLD) (35).

In regards to the development of KS, we found an increased risk in our population in agreement with the literature data, which report the risk of KS in solid organ transplant recipients at least 200 to 500-fold greater than in the local population (36-38).

The onset of the KS was in all cases within two years after transplantation, as reported in previously published studies (38-40). In four of our recipients, pre-transplant seropositivity for HHV-8 suggests rapid reactivation of latent infection favored by immunosuppressive therapy, particularly with calcineurin inhibitors.

Although screening for HHV-8 has not been routinely included in the pre-transplant guidelines and currently available serological tests are not optimal for variable sensitivity and specificity, the identification of high-risk patients would allow for careful post-transplant follow-up (41, 42).

In our study, the cancer risks attributable to post-transplant immunosuppression are 99% for KS and 85% for Lymphomas, while the fraction of solid tumors represent a small part of the observed cases in post-transplanted patients (38%). This result is believed to be related to impaired immune control of the oncogenic viruses (i.e. HHV-8), which can be present in the recipient prior to transplant or transmitted at the time of transplant via the donor organ.

A similar situation can be seen in patients with a compromised immune system, i.e. HIV/AIDS patients, where there is an increased risk of contracting cancers, while whit post-transplanted patients, after immunosuppression withdrawal with the consequential return to dialysis regimen, we can observe a return to normal susceptibility to neoplastic risks.

This finding may represent a useful information for the post-transplant follow-up and the management of patient screening and monitoring. We need also to consider that the neoplastic risk is significantly increased in the first three years from the date of transplantation and, therefore, from the start of immunosuppressive therapy. An early diagnosis for example of KS, in which the mainstay of treatment is based on the minimization of the immunosuppression and treatment with an mTOR inhibitor, could be fundamental to treating cancer but also avoid graft rejection.

Another important aspect that needs to be taken into consideration is the study of pre-neoplastic lesions. Various pre-cancerous lesions were found in our analysis, but the recorded number could be underestimated. In immunosuppressed subjects, these lesions, such as pre-malignant polyps of the digestive cavity, tend to degenerate more rapidly into tumors than in the general population and must be diagnosed accurately during the follow-up before their malignant transformation (43).

It should be emphasized that, when comparing the neoplastic risk of the transplanted population with the one of the local population, the post-transplant path of the transplanted population should be taken into consideration.

In fact, transplant recipients are subjected to very close periodic visits by our center, considerably reducing the risk that severe complications such as tumors may not be adequately recorded, particularly in the first years of follow-up.

The present study has limitations. First of all, the relatively small sample size and the retrospectively collecting data do not permit a definitive conclusion about the neoplastic risk in the post-transplantation and do not allow to provide accurate estimates of the SIR for the low statistical power.

Due to the long period of years covered from this survey, the incidence rates from Italian cancer registries available at the time of the analysis were used.

Although this approach is frequently used, it should be noted that the intake of the rates are constant before and after the periods mentioned, and cannot be satisfied for all the cancers analyzed. Likewise, they could not take into consideration geographical differences in the incidence of tumors in the general Italian population due to poor coverage of extensive cancer registries areas.

In conclusion, the results of this study validate the concept that an association between immunosuppression and cancer might exist, especially for tumors linked to viral infections.

The data related to the incidence and percentages attributable to the post-transplant immunosuppression of neoplastic diseases, such as Lymphomas and KS, could improve the management of the recipients regarding the post-transplant follow-up, so that we can anticipate the tumor diagnosis, especially during the three years following the transplant. This might be extremely helpful because, as previously mentioned, tumors developed in transplant recipients are often more aggressive and develop at a much more advanced pace than in non-transplant patients.

standardized incidence ratios (SIR)
Kaposi's sarcoma (KS)
end stage renal disease patients (ESRD)
Epstein-Barr virus (EBV)
Human herpesvirus 8 (HHV-8)
Human Papillomavirus (HPV)
Hepatitis B virus (HBV)
Hepatitis C virus (HCV)
donor transmitted tumor (DTT)
donor derived tumor (DDT)
International Classification of Disease vers. 10 (ICD-10)
International Agency for Cancer Research (IARC)
confidence intervals (CI)
absolute risk (AR)
attributable fraction (AF)
relative risk (RR)
odds ratios (OD)
post-transplant lymphoproliferative disorders (PTLD)

Ethical Approval

The study belongs to a larger one for which was requested the approval of the local Ethical committee.

An informed consent was requested from the participants.

Competing interests

All authors declare no competing interests.

Authors' contributions

Dr Giuseppe Ietto: conceptualization and writing of the paper.

Dr. Mattia Gritti: data collection and writing of the paper.

Dr. Giuseppe Pettinato: revision and English editing of the manuscript.

Prof. Giulio Carcano: supervision.

Prof. Daniela Dalla Gasperina:, supervision.

Funding

No fundings were received for this study.

Availability of data and materials

All complete data are available if requested.

RA W, VB A, EL M, AO O, RE E, LY A, et al. Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant. The New England journal of medicine. 1999;341(23).
JF B, TM B, J T, TG G, RR A, MJ H, et al. Donor transmitted malignancies. Annals of transplantation. 2004;9(1).
Lafranca JA, Ijermans JNM, Betjes MGH, Dor FJMF. Body mass index and outcome in renal transplant recipients: A systematic review and meta-analysis. BMC Medicine. 2015;13(1).
RJ H, PR P, AI R, AW H, WJ VdW, WW P, et al. The changing causes of graft loss and death after kidney transplantation. Transplantation. 2002;73(12).
M G, C G, KW J, EK G. Pro- and anti-cancer effects of immunosuppressive agents used in organ transplantation. Transplantation. 2004;77(12).
P P, F P, E L, S F, R C, S C, et al. Epidemiologic study on the origin of cancer after kidney transplantation. Transplantation. 2004;77(3).
JR C, AC W, G W. Cancer in the transplant recipient. Cold Spring Harbor perspectives in medicine. 2013;3(7).
P P, G B, F C, L R, C C, C A, et al. [Kidney transplant and cancer risk: an epidemiological study in Northern and Central Italy]. Epidemiologia e prevenzione. 2008;32(4–5).
AC W, JC C, JM S, MP J, JR C. Identifying high risk groups and quantifying absolute risk of cancer after kidney transplantation: a cohort study of 15,183 recipients. American journal of transplantation: official journal of the American Society of Transplantation and the American Society of Transplant Surgeons. 2007;7(9).
J D, E P. Malignancies in renal transplantation: an unmet medical need. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association - European Renal Association. 2007;22 Suppl 1.
MT vL, AC W, MR M, JH S, SP M, J A, et al. Effect of reduced immunosuppression after kidney transplant failure on risk of cancer: population based retrospective cohort study. BMJ (Clinical research ed). 2010;340.
M L, P B, G S, R T, TF S, R M, et al. Molecular evidence of organ-related transmission of Kaposi sarcoma-associated herpesvirus or human herpesvirus-8 in transplant patients. Blood. 2000;96(9).
M L, P B, R B, D V, L P, F F, et al. Human herpesvirus 6 latency characterized by high viral load: chromosomal integration in many, but not all, cells. The Journal of infectious diseases. 2006;194(7).
CM V, SP M, MR M, MT vL, JH S, M L, et al. Cancer incidence before and after kidney transplantation. JAMA. 2006;296(23).
R N, AE G, NS M, GW M, AM K, CM V. De novo cancer-related death in Australian liver and cardiothoracic transplant recipients. American journal of transplantation: official journal of the American Society of Transplantation and the American Society of Transplant Surgeons. 2013;13(5).
J vdW, JI R, AC H, AJ H, W W. Patient survival after the diagnosis of cancer in renal transplant recipients: a nested case-control study. Transplantation. 2010;90(12).
Cancer Mortality in Kidney Transplantation - Kiberd – 2009 - American Journal of Transplantation - Wiley Online Library. 2022.
MJ G, DM S. Donor derived malignancy following transplantation: a review. Cell and tissue banking. 2007;8(4).
DC M, M R, VJ R. CADAVERIC RENAL HOMOTRANSPLANTATION WITH INADVERTENT TRANSPLANTATION OF CARCINOMA. JAMA. 1965;192.
RE W, EB H, CL H, JM C, JP M, JE M. Immunologic rejection of human cancer transplanted with a renal allograft. The New England journal of medicine. 1968;278(9).
B M, CF Z, DA K, E G. Transplanted carcinoma in an immunosuppressed patient. Transplantation. 1970;9(1).
Donor Cancer Transmission: Focusing on the Evidence: Transplantation. 2022.
I B, M P, JP R, J H, M B, MS W, et al. Donor-derived acute promyelocytic leukemia in a liver-transplant recipient. The New England journal of medicine. 1999;341(11).
C M, V S, J S, M Z. Transmission of malignancy with solid organ transplants. Transplantation. 2005;80(1 Suppl).
P F, HL T, H B-H, W K, MP M, J K, et al. Donor origin of de novo hepatocellular carcinoma in hepatic allografts. Transplantation. 2003;76(5).
P B, M L, F F, C M, M A, R S, et al. Post-transplant Kaposi sarcoma originates from the seeding of donor-derived progenitors. Nature medicine. 2003;9(5).
AM R, C J, M J, D E, M A. Adenocarcinoma arising in a transplanted pancreas. Transplantation. 2001;72(6).
R B, C S, M M, A Q, K B, E M, et al. Primary renal cell carcinoma in a transplanted kidney: genetic evidence of recipient origin. Transplantation. 2009;87(7).
Human De Novo Papillary Renal-Cell Carcinomas in a Kidney Graft: Evidence of Recipient Origin With Adenoma‐Carcinoma Sequence - Verine – 2013 - American Journal of Transplantation - Wiley Online Library. 2020.
Aractingi S, Kanitakis J, Euvrard S, Danff CL, Peguillet I, Khosrotehrani K, et al. Skin Carcinoma Arising From Donor Cells in a Kidney Transplant Recipient. 2005.
Verneuil L, Varna M, Ratajczak P, Leboeuf C, Plassa L-F, Elbouchtaoui M, et al. Human skin carcinoma arising from kidney transplant–derived tumor cells. 2013.
A J, H M, C L, JM C, E G, L L, et al. Donor-derived oral squamous cell carcinoma after allogeneic bone marrow transplantation. Blood. 2009;113(8).
Ietto G. The dynamics of CSCs and CTCs in a chimera subject: the solid organ transplant recipient who develops a neoplastic lesion. 2020.
RT B, AO O, RA W, RM M, WM B, SV M, et al. Immunosuppression and the risk of post-transplant malignancy among cadaveric first kidney transplant recipients. American journal of transplantation: official journal of the American Society of Transplantation and the American Society of Transplant Surgeons. 2004;4(1).
MP G, PJ K, M J, V P, A C, JC C, et al. Long-term cancer risk of immunosuppressive regimens after kidney transplantation. Journal of the American Society of Nephrology: JASN. 2010;21(5).
AE G, MT vL, MO F, CM V. Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet (London, England). 2007;370(9581).
C L, C L, C F. Kaposi sarcoma in transplantation. Transplantation reviews (Orlando, Fla). 2008;22(4).
SM M, EA E. Kaposi's sarcoma risk among transplant recipients in the United States (1993–2003). International journal of cancer. 2006;119(11).
Grossi P, Baidanti F, Corona A, Dalla Gasperina D, Laudini S, Vigano M, et al. Kaposi sarcoma following thoracic organ transplantation: Prevalence, correlation with human herpes virus 8 and new therapeutic options. Transplantation. 1999;67(7):S39-S.
EK C, MS L, CA C, KS P, EA E, RM P. Risk of Kaposi sarcoma after solid organ transplantation in the United States. International journal of cancer. 2018;143(11).
R PM, J H. Human herpesvirus 6, 7, and 8 in solid organ transplantation: Guidelines from the American Society of Transplantation Infectious Diseases Community of Practice. Clinical transplantation. 2019;33(9).
M M, E B, A M. Human herpesvirus 8 and Kaposi sarcoma: how should we screen and manage the transplant recipient? Current opinion in infectious diseases. 2021;34(6).
I P. Post-transplant malignancy: the role of immunosuppression. Drug safety. 2000;23(2).

Tables 1 to 2 are available in the Supplementary Files section

No competing interests reported.

Tables.docx

Download PDF

Journal Publication

published 23 Jan, 2023

Read the published version in World Journal of Surgical Oncology →

Editorial decision: Major revision
02 Jan, 2023
Reviews received at journal
31 Dec, 2022
Reviewers agreed at journal
23 Dec, 2022
Reviewers agreed at journal
21 Dec, 2022
Reviewers invited by journal
29 Oct, 2022
Editor assigned by journal
29 Oct, 2022
Submission checks completed at journal
24 Oct, 2022
First submitted to journal
20 Oct, 2022

You are reading this latest preprint version

Tumors after kidney transplantation: a population study

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Materials And Methods

Results

Discussion

Conclusion

Abbreviations

Declarations

References

Tables

Additional Declarations

Supplementary Files

Status:

Journal Publication

Version 1