Chemotherapy for urothelial carcinoma in renal transplantation patients: Initial results from a single center

  • Authors:
    • Yichen Zhu
    • Jing Xiao
    • Yuwen Guo
    • Jun Lin
    • Lei Zhang
    • Ye Tian
  • View Affiliations

  • Published online on: July 30, 2015     https://doi.org/10.3892/mco.2015.615
  • Pages: 1387-1391
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Abstract

The aim of this study was to assess the safety and efficacy of gemcitabine plus cisplatin/carboplatin (GC/GCa) chemotherapy in renal transplantation (RT) patients with urothelial carcinoma (UC). We reviewed the records of 12 RT patients with metastatic or locally advanced UC who received chemotherapy at our institution since January, 2013. All the patients received intravenous gemcitabine (800 mg/m2) on days 1, 8 and 15, plus cisplatin (70 mg/m2) or carboplatin (area under the curve = 5) on day 2, every 28 days. A total of 10 patients completed all the cycles, while 1 patient discontinued treatment due to disease progression and 1 patient discontinued due to non‑medical reasons. In total, 12 patients received a median of four cycles of chemotherapy. The overall response rate was 50% (4/8 cases) in patients with measurable lesions. At the time of the study, 5 patients had succumbed to the disease (overall survival, 9.2 months), while 7 patients remained alive (follow‑up time, 13.3 months). The most common toxicities were myelosuppression and gastrointestinal effects. Therefore, the GC/GCa regimen was found to be effective and tolerable in RT patients with UC. However, further studies involving more patients and control groups are required to confirm our results.

Introduction

The short-term survival of renal transplantation (RT) patients has increased significantly over the last few years, as a result of the development of immunosuppressive drugs, modification of immunosuppressive regimens and improved techniques in organ handling (1). The long-term survival of RT patients, however, has not improved significantly (1). The increased incidence of cancer due to the longer life span and chronic exposure to immunosuppressive drugs may play an important role in the lack of long-term improvement (2,3). A recent large-scale study involving 175,732 solid organ transplant recipients (58.4% kidney, 21.6% liver, 10.0% heart and 4.0% lung) demonstrated that the overall cancer risk, with 10,656 cases and an incidence of 1,375 per 100,000 person-years, has increased significantly compared to that in the non-transplant population (4). Furthermore, it was suggested that malignancy was surpassing cardiovascular disease as the leading cause of long-term post-transplantation mortality (5).

China has experienced a similar trend. Indeed, according to our published data, urothelial carcinoma (UC) is the predominant malignancy among Chinese RT patients (69). This is quite different from Western countries, in which non-melanoma skin cancer and post-transplantation lymphoproliferative disorder (PTLD) are the most common malignancies (10,11). Although surgical intervention is recommended, due to the rapid progression, post-transplantation UC is generally intractable and is associated with a poor prognosis (5,10).

Recently, cisplatin/carboplatin-based chemotherapy has been considered to be an effective treatment for locally advanced and metastatic UC (12). However, to the best of our knowledge, no study has yet investigated platinum-based chemotherapy in RT patients with UC. Renal toxicity and the potential risk of infection are likely the factors of greatest concern for physicians, thus preventing them from performing chemotherapy on RT patients. In our center, chemotherapy has been performed in RT patients with UC over several years. The purpose of this retrospective study was to initially assess the feasibility of gemcitabine plus cisplatin/carboplatin (GC/GCa) chemotherapy in post-RT UC patients.

Patients and methods

Patients and evaluation

Between January, 2013 and September, 2014, 12 RT patients who suffered from UC were included in the study. All the patients were histologically diagnosed with muscle-invasive or advanced UC. The patient medical records were retrospectively reviewed for data on demographics, previous transplantation history, radiological, pathological and surgical information and chemotherapy history. During all the cycles of chemotherapy, the complete blood count (CBC), urine routine test and biochemistry evaluation, including aspartate aminotransferase (AST), alanine aminotransferase (ALT), albumin and serum creatinine concentration (SCrC) were evaluated weekly. Glomerular filtration rate (GFR), computerized tomography (CT) scans of the chest, abdomen and pelvis, and radionuclide bone scans were evaluated every two cycles. Toxicity was graded according to the Common Terminology Criteria for Adverse Events scale, version 4.0 (13). The response category was determined using the Response Evaluation Criteria in Solid Tumors 1.1 (14).

Chemotherapeutic regimen

The eligibility criteria for chemotherapy were as follows: i) age ≥18 years; ii) Eastern Cooperative Oncology Group (ECOG) performance score ≤3; iii) adequate hematological and hepatic function (white blood cell count ≥ 3.5×109/l, absolute neutrophil count ≥1.5×109/l, platelet count ≥100×109/l, albumin level within normal limits, ALT and AST ≤2-fold the upper normal limit (for liver metastatic cases, ≤5-fold the upper normal limit); iv) normal renal function (GFR ≥30 ml/min/1.73 m2, absence of proteinuria and SCrC ≤ upper normal limit). Hospitalization was required for treatment on the day the chemotherapeutic drugs were administered. The patients received gemcitabine [800 mg/m2 as a 30-min intravenous (i.v.) infusion] on days 1, 8 and 15 separately, and cisplatin (70 mg/m2 as a 2-h i.v. infusion) on day 2 every 4 weeks (GC regimen). For cases with impaired renal function, cisplatin was replaced by carboplatin (area under the curve = 5; GCa regimen). Hematopoietic growth factor supportive therapy was required in cases with severe (≥ grade 2) marrow suppression. If the patients did not meet the eligibility criteria at the beginning of a cycle, the cycle was delayed until recovery. Treatment was discontinued in patients exhibiting disease progression or in cases of unacceptable toxicity.

Statistical method

The response rate, overall survival (OS) and progression-free survival (PFS) were measured at the time point of present study. OS was estimated by the Kaplan-Meier method, with the time measured from the first day of treatment.

Results

Patient characteristics

The characteristics of the 12 patients with UC are summarized in Table I. The reason for offering chemotherapy was detected metastatic lesions (M+) during the postoperative follow-up (n=6), postoperative histological diagnosis confirming positive lymph nodes (n=3) and only muscle-invasive disease (≥T2, n=3). All the cases had a history of exposure to aristolochic acid. The primary UC site included the upper tract and bladder in 11 cases and the upper tract alone in 1 case. In all the cases, SCrC was normal and only 1 patient was ineligible for cisplatin treatment due to a GFR of <60 min/ml, in which case cisplatin was replaced by carboplatin.

Table I.

Baseline patient characteristics.

Table I.

Baseline patient characteristics.

CharacteristicsNo. (%)
Age, years (mean ± SD)55.17±8.79
Time of transplantation, years (mean ± SD)11.0±2.33
Immunosuppressive regimen
  FK506+MMF+P5 (41.7)
  Rapamycin+MMF+P1 (8.3)
  CsA+MMF+P6 (50.0)
ECOG performance status
  010 (83.3)
  12 (16.7)
  ≥20 (0.0)
Histology
  Pure transitional cell carcinoma11 (91.7)
  Urothelial and SCC1 (8.3)
Primary UC sites
  UTUC alone1 (8.3)
  UTUC+BC11 (91.7)
Previous treatment
  RNU only2 (16.7)
  RNU+TUR-Bt7 (58.3)
  RNU+RC3 (25.0)
TNM stage at presentation
  T2-4N0M03 (25.0)
  TxN+M03 (25.0)
  TxNxM+6 (50.0)
Metastatic sites
  Bone3
  Lung2
  Liver1
  Lymph nodes6
  Peritoneum2
  Pelvic cavity1
Cisplatin eligibility
  Yes11 (91.7)
  No1 (8.3)
Biological parameters (base line)
  GFR (ml/min/1.73m2)62.56±6.53
  WBC count (×109/l)5.57±1.33
  PLT count (×109/l)238.33±66.31

[i] SD, STANDARD DEVIATION; SCC, SQUAMOUS CELL CARCINOMA; MMF, mycophenolate mofetil; P, prednisone; CsA, cyclosporin A; ECOG, Eastern Cooperative Oncology Group; UC, urotheliAL carcinoma; UTUC, upper tract UC; BC, bladder CANCER; RNU, radical nephroureterectomy; TUR-Bt, transurethral resection of bladder tumor; RC, radical cystectomy; GFR, glomerular filtration rate; WBC, white blood cell; PLT, platelet.

Treatment

All the patients received at least one cycle of GC chemotherapy, with a median number of four cycles (range, 1–8 cycles). One patient discontinued treatment due to disease progression and 1 patient discontinued due to non-medical reasons. The remaining 10 patients completed the therapy. The treatment delays and dose reductions are shown in Table II.

Table II.

Cycle delay and dose reduction.

Table II.

Cycle delay and dose reduction.

Cycles

Characteristics1 (n=12)2 (n=12)3 (n=10)4(n=10)
Number of cycles delayed0134
Reason for cycle delay
  Myelosuppression0022
  Renal toxicity0111
  Other00 1
Number of dose reductions0122
Reason for dose reduction
  Myelosuppression0011
  Renal toxicity0111
Toxicity

Overall, the GC regimen was well tolerated. Myelosuppression was the most common toxicity (10/12) and was also the main reason for cycle delay and dose reduction. A total of 5 patients with grade 2–3 granulocytopenia received granulocyte colony-stimulating factor (G-CSF) treatment. Nausea and vomiting (7/12) were the most common non-hematological toxicities, but they were mild (grade 1–2). Renal toxicity, which was the greatest concern for both physicians and RT patients, was mild. Renal injury (grade 1) and proteinuria (grade 1) were detected in only 2 cases, and both patients recovered quickly without further treatment. The treatment-related adverse events are summarized in Table III.

Table III.

Treatment-related toxicities.

Table III.

Treatment-related toxicities.

Cycles

Toxicities1(n=12)2(n=11)3(n=10)4(n=10)
Granulocytopenia
  Grade 12344
  Grade 21132
  Grade 30213
  Grade 40000
  Grade 50000
Thrombocytopenia
  Grade 12311
  Grade 20112
  Grade 30022
  Grade 40000
  Grade 50000
Anemia
  Grade 11233
  Grade 20112
  Grade 30000
  Grade 40000
  Grade 50000
Renal injury
  Grade 10111
  Grade 20000
  Grade 30000
  Grade 40000
  Grade 50000
Proteinuria
  Grade 11000
  Grade 20000
  Grade 30000
Diarrhea or constipation
  Grade 11213
  Grade 20000
  Grade 30000
  Grade 40000
  Grade 50000
Nausea or vomiting
  Grade 12345
  Grade 21132
  Grade 30000
  Grade 40000
  Grade 50000
Response and survival

Of the 8 patients with measurable lesions, 1 achieved complete response (CR) and 3 achieved partial response (PR) (overall response rate, 50%). Pain relief was achieved in 1 case. A total of 2 patients had stable disease (SD). Only 1 patient exhibited progressive disease (PD) during chemotherapy. At the time of this study, 5 patients had succumbed to the disease [mean OS, 9.2 months; 95% confidence interval (CI): 6.5–12.0 months). Of the 7 surviving patients at the 13.3-month follow-up, 3 exhibited PD. For all the cases with PD, the mean PFS was 7.8 months (95% CI: 4.0–11.5 months). The follow-up information is summarized in Table IV.

Table IV.

Follow-up.

Table IV.

Follow-up.

PatientsStatusTreatment cyclesMeasurable lesionsResponsePFS (months)Follow-up time (months)
1D1+SD410
2D1+PD16
3D4+SD39
4D6+SDa47
5D8-SD914
6A and P4+CR1521
7A and P5+PR1217
8A and P4-SD1418
9A and NP4+PR44
10A and NP4+PR77
11A and NP4-SD1414
12A and NP6-SD1212

a Pain relief. PFS, progression-free survival; D, DECEASED; A, alive; P, progression; NP, no progression; SD, stable disease; PD, progressive disease; CR, complete response; PR, partial response.

Discussion

In Asian countries, upper tract UC (UTUC) is more frequently observed compared with bladder involvement in RT patients with UC (69,11). Moreover, the incidence of multifocal lesions is considerably higher in RT recipients compared with that in the general population (61.9 vs. 23.7%, respectively) (11). Aggressive biological behavior, multifocality and an immunosuppressive status render UC particularly difficult to treat in RT patients.

Surgical treatment is the first choice for UC and prophylactic bilateral nephroureterectomy is recommended when UTUC is suspected. Our previous study demonstrated that, even without any imaging abnormalities, UC morbidity in the contralateral upper tract was significantly higher (15). Furthermore, mammalian target of rapamycin (mTOR) inhibitor-based and calcineurin inhibitor (CNI)-free regimens are recommended, given that several studies demonstrated that the risk of developing de novo malignancies was significantly higher in a group of patients receiving CNI-based immunosuppression compared with a group receiving mTOR inhibitors (16). mTOR inhibitors are considered to exert anti-angiogenic effects, which may inhibit tumor growth (17). However, the prognosis of UC in RT patients remains poor.

Unfortunately, no optimal treatment is currently available, particularly for UC patients. The efficacy of platinum-based chemotherapy has been generally demonstrated in UC patients. Neoadjuvant and adjuvant chemotherapy have been shown to improve OS in muscle-invasive bladder cancer patients (12,18). Furthermore, a recently published systemic review demonstrated that OS and disease-free survival may be prolonged by cisplatin-based neoadjuvant and adjuvant chemotherapy in UTUC patients (19). However, to the best of our knowledge, no report of the effectiveness of chemotherapy in post-RT UC patients has been published, which may be attributed to the fact that oncologists are concerned in regard to the potential renal toxicity from chemotherapy due to their unfamiliarity with kidney transplantations.

The present study demonstrated the feasibility of GC chemotherapy in RT patients. In cases with measurable lesions (advanced UC), the overall response rate was 50% and the mean PFS was 7.8 months, which is similar to other published trials (20). Furthermore, the GC/GCa regimen was well tolerated in RT patients, particularly in terms of renal toxicity. With strict surveillance of renal function, we did not detect severe renal injuries, either short- or long-term. In previous trials, the major toxicities of GC/GCa chemotherapy were myelosuppression and gastrointestinal effects (e.g., vomiting and nausea), which was also the case in our study. In the literature, grade 3–4 neutropenia and thrombocytopenia were observed in ≥60% of the patients (21,22). Considering that immunosuppressive drugs also induce myelosuppression, we used hematopoietic growth factors to prevent severe myelosuppression in our post-RT UC patients; this may explain the fact that our toxicity data compare favorably with those of previous GC trials.

Cisplatin was replaced by carboplatin in patients with impaired renal function. Several trials have reported acceptable efficacy and toxicity for the GCa regimen in UC patients (2123). In post-RT UC patients, renal function tended to be normal, as adequate immunosuppression was associated with a lower rate of chronic rejection, but a higher incidence of malignancy. In our study, only 1 patient was ineligible for cisplatin treatment and the GCa regimen was administered uneventfully in this case. Additional cases are required to confirm the efficacy and toxicity of the GCa regimen in RT patients with UC.

There were several limitations to this study. First, the small cohort of patients and short-term follow-up limited the possibility to assess the effect of chemotherapy on the OS. Further studies, involving more patients and a control group are required. Second, the present study included advanced UC as well as muscle-invasive UC cases, due to the small cohort of patients; therefore, the evaluation of the response rate was not rigorous. Third, a retrospective study is always associated with inherent bias.

In conclusion, GC/GCa chemotherapy was found to be feasible and well-tolerated in RT patients with UC. The main toxicities were myelosuppression and gastrointestinal effects, whereas renal toxicity was mild. However, larger-scale and long-term studies are required to validate our results.

Acknowledgements

This study was supported by the Capital Health Research and Development of Special Fund (grant no. 2011-2002-05).

Abbreviations:

GC/GCa

gemcitabine plus cisplatin/carboplatin

RT

renal transplantation

UC

urothelial carcinoma

AUC

area under the curve

PTLD

post-transplantation lymphoproliferative disorder

CBC

complete blood count

ALT

alanine aminotransferase

SCrC

serum creatinine concentration

GFR

glomerular filtration rate

CT

computerized tomography

CTCAE

Common Terminology Criteria for Adverse Events

RECIST

Response Evaluation Criteria in Solid Tumors

OS

overall survival

PFS

progression-free survival

ECOG

Eastern Cooperative Oncology Group

G-CSF

granulocyte colony-stimulating factor

CR

complete response

PR

partial response

SD

stable disease

PD

progressive disease

UTUC

upper tract urothelial carcinoma

mTOR

mammalian target of rapamycin

CNI

calcineurin inhibitor

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Spandidos Publications style
Zhu Y, Xiao J, Guo Y, Lin J, Zhang L and Tian Y: Chemotherapy for urothelial carcinoma in renal transplantation patients: Initial results from a single center. Mol Clin Oncol 3: 1387-1391, 2015
APA
Zhu, Y., Xiao, J., Guo, Y., Lin, J., Zhang, L., & Tian, Y. (2015). Chemotherapy for urothelial carcinoma in renal transplantation patients: Initial results from a single center. Molecular and Clinical Oncology, 3, 1387-1391. https://doi.org/10.3892/mco.2015.615
MLA
Zhu, Y., Xiao, J., Guo, Y., Lin, J., Zhang, L., Tian, Y."Chemotherapy for urothelial carcinoma in renal transplantation patients: Initial results from a single center". Molecular and Clinical Oncology 3.6 (2015): 1387-1391.
Chicago
Zhu, Y., Xiao, J., Guo, Y., Lin, J., Zhang, L., Tian, Y."Chemotherapy for urothelial carcinoma in renal transplantation patients: Initial results from a single center". Molecular and Clinical Oncology 3, no. 6 (2015): 1387-1391. https://doi.org/10.3892/mco.2015.615