Expanding Utilization of Organs from Donors with Small Renal Masses

Kidney Transplantation (KT) is an optimal treatment for patients with End-Stage Renal Disease (ESRD), but a huge imbalance between the large number of listed patients and the shortage of organ supply exists all through the way. To narrow the gap, Expanded Criteria Donor (ECD) kidneys has gradually stepped onto the stage in recent years. The experience of using kidneys with Small Renal Masses (SRMs) in transplantation been reported in a number of studies represents a potential avenue to expand the donor pool. Besides, some other reported cases about the transplants of other organs from donors with SRMs provides a new possibility of multiorgan transplantation. This article briefly presents the status of renal and other organ transplantation from donors with SRMs and provides some opinions on the potential utilization of remaining organs from this group of donors.

The number of patients diagnosed with End-Stage Renal Disease (ESRD) has been increasing with time [1]. Over the last five decades, medical and surgical advances have made kidney transplantation the best therapy for this patient population, which ensures better quality of life, long-term patient survival and more economic benefits in comparison with dialysis treatment [2-5]. Nevertheless, only a minority of patients with ESRD ultimately received a transplant for the fact that organ demand far outstrips its supply [6]. Multiple strategies have been implemented to liberalize donor and organ selection criteria without compromising recipient outcomes. Such efforts include living kidney donation, Donation after Cardiac Death (DCD) and Expanded Criteria Donor (ECD) kidney [7-9]. Despite such efforts, high organ discard rate – 20% of deceased donor kidneys – contributes significantly to organ underutilization [10,11]. One important factor is the discovery of renal masses during organ procurement or living donor work-up. About 270,000 cases of kidney cancer were found worldwide every year and the incidence of kidney cancer reaches 1.55% to 1.76% in large-scale autopsy [12,13]. It is traditionally believed that organs with tumors should be banned from transplantation which may cause disgarding a number of potential donor kidney. In fact, it is reported that the occurrence rate of incidental small renal carcinoma during renal procurement reached 0.9% [14], while few cases were reported using those kidneys for transplantation.

On the other hand, multiple cases have been reported describing the transplantation of tumorectomized or contralateral kidneys and other organs from donors with SRMs (Table 1). Of inspiration, during the post-transplant follow-up, the recurrence and transmission was rarely observed. These reports merit our further study on the optimal and safe use of this kind of organs, given the urgent need for transplantation services. In this article, based on existent experience of renal and other organ transplantation from donors with SRMs, we discussed the potential utility of organs from SRMs donors as well as related immunosuppression therapy and implement procedures.

Kidney transplantation from donor with SRMs

Renal Cell Carcinoma (RCC) constitutes 3% of all malignancies in the general population and goes higher in patients over 60. According to the American Urological Association and European Association of Urology, the standard surgical procedure for SRMs (<4cm T1a) is Partial Nephrectomy (PN), as it has similar oncological outcomes to radical nephrectomy but can better preserve kidney function [15-19]. The RCC recurrence rate could be as low as nearly 1.47% after PN [20,21]. Besides, reasonable active surveillance strategy is helpful to control the recurrence of RCC, which could detect metastasis timely and, as reported, reduce the risk for donor-transmitted cancer to 0.05% [22-24]. Currently, owing to low risk of recurrence and progression as well as proper function preservation, kidneys with SRMs excised are gradually considered as sources for transplantation. A number of patients being implanted kidneys from this source achieved good results [25-30]. Not limited to tumor-affected kidneys, contralateral kidneys are being accepted as eligible grafts in many transplantation centers as well [28,36]. Guidelines released by the European Committee recommend choosing kidneys with T1a renal masses as a donor choice [31]. The widely accepted RCC stage of candidate donors is not over T1a while pathological type is predominantly the clear-cell subtype, followed by chromophobe type, lipoma, and oncocytoma [31-34]. Fuhrman nuclear grading is necessary to evaluate tumors after being recovered by Organ Procurement Organization (OPO). Relevant registration and reporting system should be established to disclose every potential SRMs donor to public. Nevertheless, to date, no clear consensus has been reached in terms of oncological outcomes, surgical safety, or functional results of KTs after SRM excision [35]. Further research is to be conducted to stratify the analysis.

Multiorgan transplantation from donor with SRMs

As tumor-affected organ transplantation has gradually matured, it is considered safe to use tumorectomized kidneys as well as contralateral kidneys and even other available organs from donors with SRMs. Although discussions regarding the risk of RCC metastasis in contralateral renal and other organs are various, the risk is relatively low based on available literature. The Organización Nacional de Trasplantes (ONT) Registry did not detect any tumour transmission among 59 recipients transplanted with grafts from 47 donors registered with RCC. Carver mentioned that none of the two patients receiving the liver and contralateral kidney from one donor with RCC were found tumor transmission after 4 years of follow-up [36]. Serralta reported four liver recipients who received livers from donors with renal cell carcinoma were not observed tumor recurrence or metastasis during 49.75 months of follow-up [37]. The MALORY Initiative reported 6-year transplant experience involving 35 RCC donors, in which no tumor transmission was observed after transplantation (28 livers, 18 healthy kidneys, 13 hearts and 13 lungs) during 2-year follow-up [38]. In the era when organ demand far outstrips supply, it makes sense to promote the utilization of every available organ from deceased donor with SRMs, though the use of remaining organs from a cancer donor may be questioned for lack of sufficient evidence that definitely exclude the cancer risk.

Patients who are waiting to receive heart transplantation commonly complicate with renal dysfunction and may develop irreversible kidney failure that needs dialysis or renal transplantation. From this perspective, adults with congenital heart disease are facing higher risk for the unique physiological conditions imposed by the disease [39]. For this patient group, receiving a kidney and a heart simultaneously may be a better choice to improve their clinical outcomes [40]. Liver transplantation is an optimal treatment for End-Stage Liver Disease (ESLD). However, hepatic decompensation would lead to Hepatorenal Syndrome (HRS) or Acute Kidney Injury (AKI), while chronic liver disease could develop diabetes, a risk factor for Chronic Kidney Disease (CKD) that may even result in End-Stage Kidney Disease (ESRD) [41]. In this setting, simultaneous liver-kidney transplantation (SLKT) seems to be a better choice [42]. In addition, patients with primary hyperoxaluria or polycystic kidney-liver disease are considered more appropriate to receive SLKT [43,44]. Moreover, as the main cause of chronic renal failure, diabetes leads to more ESRD as its prevalence increases worldwide. For type I diabetes mellitus, renal replacement options include dialysis, Deceased Donor Kidney Transplant (DDKT), Living Donor Kidney Transplant (LDKT), or Simultaneous Pancreas-Kidney Transplant (SPKT). Research has proven that SPKT is associated with better kidney allograft and patient survival compared to dialysis or DDKT [45,46]. And as reported, SPKT is associated with superior pancreas survival compared to that by living donor kidney transplant (PALK) when mortality rates remained close [46]. Therefore, for patients with multiorgan failure that keep showing up on Multiorgan Transplant (MOT) lists, to receive simultaneous heart/kidney, liver/kidney, pancreas/kidney and so on may be an optimal alternative choice to get better outcomes. Certainly, this calls for more available multi-organ donors.

One of our previous studies reported a case in which a patient with ESRD and dilated cardiomyopathy received heart-kidney transplantation from a donor with SRM. No recurrence or transmission was observed after 32 months post-transplant follow-up with organ function remained proper [47].

Because of the low risk of tumor progression and metastasis mentioned above, if we can implement active surveillance, the utility of remaining organs from donors with SRMs would be a promising way to further expand the donor pool for MOT. Of course, the feasibility and relevant ethical problems are awaiting further study.

Immunosuppression regime

Another concern that cannot be ignored is the SOT recipients might be susceptible for donor-transmitted cancer due to immunosuppressive state [48]. However, it is reported that post-transplant immunosuppression may not alter the natural history of localized RCC [20]. A systematic review shows that variable post-transplant immunosuppression presents no difference in oncological outcomes [35]. Despite the potential higher risk of relapse related to immunosuppression in theory, risk of renal tumor recurrence when transplanting a SRM-excised kidney seems to be very low. Neither the use of tumor-excised kidney, nor the immunosuppression substantially increased the recurrence of RCC after renal transplantation [26,28,49,50]. The routine regimen for immunosuppressive therapy after transplantation commonly consists of a Calcineurin Inhibitor (CNI), an anti-proliferative agent, and a steroid. In our study, no recurrence or metastasis was observed after single-or multi-organ transplant. The immunosuppressive protocals are as follows respectively: tacrolimus and mizoribine for a renal transplant recipient (the SRM-excised kidney, reducing the intensity of immunosuppressive as appropriate); tacrolimus, mycophenolate mofetil and prednisone for the heart-kidney transplant recipient (the contralateral kidney); tacrolimus and rapamycin for the liver recipient (primary liver cancer) [47]. It represented our attempt to adjust immunosuppressive therapy for recipients of MOT from donor with SRMs. Everolimus is currently approved for treatment of metastatic RCC [51]. The mizoribine has the effect of reducing tumor cell adhesion and inducing it differentiation [52,53]. The relative mild immunosuppression of mizoribine could improve the immunity to some extent which may also help with anti-neoplastic. In addition, we consider that when the recipient has a tumor (such as liver cancer), it is more appropriate to switch to or use in combination with mTOR inhibitor shortly after operation in spite of its possible influence on wound healing. The effect of immunosuppression on patients receiving organs from donors with SRMs necessitates further research to provide sufficient evidence, and more work need to be done to set better immunosuppressive protocols under this tough situation.

Management of incidental RCC

Most of current studies are dealing with existent kidney masses, while few handles incidental tumors. However, quite a few cases (especially with masses smaller than 2cm in diameter) are discovered during or after organ procurement, calling for a relatively standard procedure to address the situation. Compared to preoperative donor evaluation, it is more important to evaluate organs for neoplastic diseases during and after procurement. Cases of tumor transmission from RCC donors do exist when the tumor was not detected and the risk of transmission not assessed before transplantation. Penn reported 17 recipients who received kidneys with undetected malignant renal tumors during organ acquisition. Seven of these recipients died of metastatic disease after an average of 12 months [54]. It is reported that an incidental renal tumors were not discovered as perirenal fat was not removed for careful examination during kidney acquisition, while the contralateral kidney and the heart had been transplanted to the recipients renal recipient underwent nephrectomy 4 months after transplantation due to tumor infiltration, and heart transplant recipient died of metastatic RCC 7 months after transplantation [55].

The pathological type of these tumors that transmitted after transplantation are mostly undifferentiated ones, suggesting that the risk of tumor transmission may rarely be related to primitive, small, well-differentiated, less invasive RCC. Nevertheless, the risk of undetection due to careless kidney examination without removal of perirenal fat during organ procurement cannot be ignored. Moreover, in our practice, there are cases where kidneys with SRM, perirenal bronchogenic cyst, perirenal vascular leiomyoma and accessory pancreatic tissue similar to colon tumor were detected, so detailed abdominal exploration and accurate preoperative pathological examination are extremely important and indispensable. Besides, a standard protocol to deal with incidental tumors needs to be developed.

Other tips

There is no doubt that it is feasible to implement organ transplantation from donors with SRMs, yet some points still need our attention. Tumor excision should be performed during bench surgery and masses analyzed immediately through frozen section to evaluate histological characteristics and confirm negative in the cut edge. Every recipient should be fully informed of the risk of tumor transmission and provide clear consent before the implantation of kidneys/organs. It is necessary to determine the immunosuppression therapy based on patients' characteristics, including age, sex, as well as the size and pathological types of kidney masses.

Overall, kidneys from donors with SRMs can be considered to utilize due to the low recurrence rates after transplantation. Concerning the potential impact of immunosurppresion on the cancer, individualized regimens should be determined according to the type of transplantation from the RCC donors. Despite studies on multiorgan utilization from tumor affected-donors are still scarce and further research is needed, the utilization of remaining organs is feasible and promising in expanding the donor pool with the strategy of tumor recurrence surveillance and follow-up. As to incidental tumors, careful intraoperative exploration and timely pathological examination are critical. Structured and protocolized procedures as well as long-term follow-up strategies for recurrence surveillance should be established in transplant centers when using organs derived from donors with SRMs in the future.

This work is supported by Shanghai Changhai Hospital. The manuscript has been reviewed and approved by all authors and is neither in submission nor under consideration for publication by any other journal. All authors have read the author-ship agreement and policy on disclosure of potential conflicts of interest of Translational Research and have no disclosures to declare.

Ethical approval

This study was approved by our institutional review board.

Statement of human and animal rights

This article does not contain any studies with human or animal subjects.

Statement of informed consent

Not applicable.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

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