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Primary renal leiomyosarcoma in adult patients: a systematic review and individual patient data analysis
African Journal of Urology volume 30, Article number: 15 (2024)
Abstract
Purpose
The optimal management of primary renal leiomyosarcomas is unknown owing to its rarity and minimal available information about their primary, adjuvant treatment and clinical outcomes. This study systematically reviews treatment evidence and effects in terms of survival for leiomyosarcomas arising primarily from kidney, renal pelvis and renal vessels.
Method
PubMed and Embase databases were searched from inception to March 2023, with manual searches of reference lists. Two investigators independently reviewed the studies reporting management and survival outcomes of renal leiomyosarcomas.
Results
A total of 85 publications met inclusion criteria, reporting on 188 cases. The median age was 55.5 years, predominantly female [52.7%]. Pain was the most common presenting symptom [41.5%], and most tumors were high grade [45.8%]. Complete surgical resection with negative margins forms definitive treatment. The median disease-free survival and overall survival (OS) for all reviewed patients were 24 months [95%CI 4.1–43.9] and 42 months [95%CI 32.5–51.4], respectively. The OS of 1 year, 2 year, 3 year and 5 year was 78.8%, 64.4%, 53.8% and 38.9%, respectively. On univariate analysis, favorable factors for OS included tumor size ≤ 5 cm, low-grade histology, tumors of renal vascular origin and non-metastatic disease at presentation. Neoadjuvant or adjuvant treatment with either radiotherapy or chemotherapy has been shown to improve OS (NR vs. 36 months, p < 0.001), especially for high-grade tumors > 5 cm in size.
Conclusion
Radical nephrectomy with en bloc tumor resection with negative margins forms the mainstay of treatment for renal leiomyosarcomas. Adjuvant radiotherapy or chemotherapy appears to improve OS. To validate this treatment strategy, prospective multicentric efforts are required to acquire reliable data from randomized trials.
1 Introduction
Renal leiomyosarcomas are rare malignant tumors arising from smooth muscle found in inner layer of renal capsule, walls of stellate veins that drain superficial renal cortex, renal pelvis and renal blood vessels. Though they account for 50–60% of renal sarcomas, they constitute only < 1.5% of primary renal malignancies [1,2,3]. Being a rare entity, publications on renal leiomyosarcoma (LMS) are primarily either case reports or part of case series on renal sarcomas [4,5,6].
Owing to its rarity, there is little information available with limited understanding regarding their treatment, recurrence, metastasis and long-term survival outcomes. Hence, we proposed to perform systematic review and individual patient data analysis of all published cases to summarize existing evidence for primary and adjuvant treatment. A systematic review of case reports and series cannot establish the standard of care for managing renal LMS. However, it can identify significant associations and generate hypotheses for future studies. Our primary objective is to determine clinical and pathological characteristics, patterns of care and long-term survival outcomes of such patients.
2 Methods
2.1 Literature search and inclusion criteria
This systematic review with meta-analysis was constructed in accordance with Preferred Reporting Items for Systematic reviews and Meta-analysis (PRISMA) framework. Electronic databases such as PubMed and EMBASE were searched from inception to March 2023 to identify studies published in English language on renal LMS in adults > 18 years. The search strategy was carried out with the National Library of Medicine’s Medical Subject Heading (MeSH) terms like ‘leiomyosarcoma,’ ‘primary leiomyosarcoma,’ ‘kidney,’ ‘renal,’ ‘renal pelvis’ with different Boolean operators (and/or). A manual search of reference lists of included articles was also performed to make sure there was no additional case unidentified from the primary search. Only studies in English language were included. Cases were included only if patients had LMS arising primarily from kidney, renal pelvis and renal vessels and outcomes at last follow-up were mentioned. Recurrent LMS, LMS arising in renal transplants and inferior vena cava leiomyosarcomas were excluded. Also, non-human studies, review articles, systematic review or meta-analysis was excluded. Only case reports and case series were included which had individual patient details. The PICO (patient-intervention-comparison-outcome) questionnaire is attached in Table 1.
2.2 Study selection
Two investigators independently screened search results obtained through various databases for eligible publications by title and abstract screening after removing duplicates. Next, full text of eligible publications was reviewed for data synthesis and analysis. When a discrepancy was observed between the investigators, the said abstract was reviewed by both in collaboration.
2.3 Risk of bias
Based on the type of study included, risk of bias analysis was done. The Joanna Briggs Inventory (JBI) was used for the risk of bias analysis for case reports and National Institute of Health (NIH) quality assessment tool for case series [7, 8].
2.4 Data extraction and quality assessment
For each article, we extracted data on age, gender, clinical presentation, tumor size, grade, type of surgery, details of adjuvant treatment, if any, and outcomes in terms of patterns of relapse, disease status and survival, at the last follow-up.
2.5 Data analysis
The extracted data were tabulated in Statistical Package for Social Sciences (SPSS) version 23. Categorical variables were represented with percentages, median with interquartile range for continuous variables. Survival analysis was done using Kaplan–Meier method. Log-rank test was used to determine factors affecting survival, and p-value < 0.05 was considered significant. Univariate Cox regression analysis was used to determine the hazard ratios, and if they were significant, multivariate analyzed was done. Missing data were censored from the various sub-group analysis.
3 Results
Our search strategy yielded 1256 articles, of which 966 abstracts were screened after excluding duplicate articles. Based on exclusion criteria, 797 articles were excluded yielding 169 publications after add-ons from reference lists. Finally, 85 articles with 188 patient records were considered for quantitative analysis [Fig. 1, Table 2].
3.1 Patient demographics
Of 188 patients, 52.7% were females. The median age was 55.5 years, and 58% were symptomatic at presentation. The most common presenting symptom was pain (41.5%), followed by palpable mass (19.7%) and hematuria (13%). Primarily they originated from renal parenchyma, renal vessels (18.6%) and renal pelvis (7.4%)—over 50% patients presented with tumor size > 5 cm. Only 8.5% were metastatic at presentation (Table 3).
3.2 Treatment
The treatment characteristics are reported in Table 4. The primary modality of treatment was surgery (87.2%). Three-fourths underwent radical resection, only 3% underwent partial resection, while 1.6% underwent surgical debulking or biopsy. Only 23 patients received radiotherapy (9 palliative), and 28 received chemotherapy (15 palliative).
3.3 Patterns of relapse
Sixty-two (33%) had disease relapse after primary treatment. One-fourth (47) of the patients had distant relapse. Seven patients (3.7%) had both local and distant relapse, whereas three (1.6%) patients had only local relapse. Among distant relapses, lung metastasis was most common (16.5%), followed closely by liver (11.2%) and bones (6.4%).
3.4 Survival
After median follow-up of 19 months (interquartile range (IQR) 9–45 months), 70 (37%) were alive without any evidence of disease and 26 (13.8%) were alive with disease; 79 (42%) died of disease itself, while 13 (7%) died of other causes. The median disease-free survival (DFS) was 24 months [95% confidence interval (CI) 4.1–43.9 months]. The DFS rates at 1 year, 2 year, 3 year and 5 year were 65.3%, 49.4%, 43.6% and 33%, respectively. The median overall survival (OS) was 42 months [95% CI 32.5–51.4 months]. The survival rates at 1 year, 2 year, 3 year and 5 year were 78.8%, 64.4%, 53.8% and 38.9%, respectively. Kaplan–Meier curves for DFS and OS are shown in Fig. 2.
3.5 Factors affecting survival
Favorable prognosis with better OS (Fig. 3) was noted in female (54 vs. 31 months, p = 0.077) gender, patients having tumor size ≤ 5 cm (72 vs. 48 months, p = 0.056), renal vascular origin (72 vs. 36 months, p = 0.016), low-grade (138 vs. 48 vs. 19 months, p < 0.001) tumors and non-metastatic disease (45 vs. 12 months, p < 0.001). While univariate analysis demonstrated improved DFS with female gender (60 vs. 9 months, p = 0.007) and non-metastatic disease [36 vs. 3 months, p = 0.001], multivariate analysis showed significance for none (Table 5).
Patients who received multimodality treatment had significantly better survival than surgery alone (NR vs. 36 months, p < 0.001), while those without intervention had median survival of 2 months. The extent of surgery significantly impacted survival; those with partial or radical nephrectomy had better median OS (36 and 44 months) than those with debulking or biopsy only (3 months). Surgical margin status significantly impacted prognosis; positive margin status had 3-month survival, whereas median OS was not yet reached for those with negative margins (p < 0.001). Better survival was also noted in asymptomatic patients compared to those who were symptomatic at presentation (38 vs. 44 months, p = 0.898). However, on multivariate analysis, none significantly impacted survival.
Adding radiotherapy or chemotherapy in neo-adjuvant or adjuvant settings improved survival, especially in tumor > 5 cm and high-grade tumors. The 2-year survival in patients receiving surgery only was 89.3% (≤ 5 cm) and 58.4%(> 5 cm), while those receiving radiotherapy/chemotherapy was better, 100% (≤ 5 cm) and 100% (> 5 cm). Similar results were also observed with addition of chemoradiotherapy after surgery with regard to tumor grade: 88.9% (low grade with surgery only), 100% (low grade with radio-chemotherapy) vs 49.4% (high or intermediate grade with surgery only), 80% (high or intermediate grade with chemoradiotherapy).
4 Discussion
Soft tissue sarcomas (STS) account for < 1% of all cancers, with extremities being most common site. There are several histological types of STS, including LMS and liposarcoma. The genitourinary tract represents 2.1% of soft tissue sarcomas (STS), with renal being second most common location after para-testicular region. Primary renal LMS comprise 50–60% of all renal sarcomas and are extremely rare. They constitute 0.12% of all renal malignancies [1, 2, 9, 10]. Renal LMS originate from renal capsule, smooth muscles in renal pelvis or renal vessels. Preoperative diagnosis of these tumors is almost impossible because of non-specific clinical symptoms and radiological findings. Pathologically, differentiation from sarcomatoid renal cell carcinoma is essential as there is prognostic difference. Desmin positivity confirms diagnosis of LMS as sarcomatoid carcinomas may express smooth muscle actin (SMA) [11, 12].
The present analysis revealed that the median age at presentation for renal LMS was 55.5 years with predilection for female gender unlike other STS where there is male preponderance with male to female ratio of 1.4:1. The clinical presentation included abdominal pain (41.5%), abdominal mass, hematuria or combination, thus mimicking other renal tumors. Emergency presentations with spontaneous rupture have been reported in a few [13]. More than half of patients had tumor size > 5 cm at diagnosis, explaining that renal sarcomas expand and grow large due to lack of natural barriers. Further, in this study, we found that approximately one-third of patients relapse after primary treatment at median follow-up of 19 months, with distant recurrence accounting for nearly 50% relapses. The most common sites of metastases in order of decreasing frequency include lungs, liver and bones, exemplifying that renal LMS frequently spreads to distant areas via hematogenous route.
The present study demonstrated median survival of 42Â months for all reviewed renal LMS patients. The 3-year and 5-year survival was estimated to be 53.8% and 38.9%, respectively, similar to 5-year survival reported by Lee et al. in their study on urological STS [14]. They also reported 5-year survival rate of 73%, 44% and 82% for bladder, prostate and retroperitoneal sarcomas, respectively. Thus, renal sarcomas have poorer prognosis when compared to other urinary tract sarcomas. To our knowledge, this study is the first analysis reporting survival outcomes of renal LMS as distinct entity.
Primary LMS arising from renal vessels tend to have better prognosis than those from kidney or renal pelvis. Like other sarcomas, the most important prognostic factor was surgical resection status and metastatic disease at presentation [1, 14,15,16]. We found that patients with no surgical resection and those with positive margins after surgery had worse survival than those with negative margins. Metastatic disease at presentation carried poorer prognosis.
The most critical pathological prognostic feature influencing survival is tumor grade. Deyrup et al. showed that increasing grade of renal LMS and survival is inter-related [5]. High-grade tumors carried poorer survival compared to low and intermediate grade because of their high metastatic potential necessitating adjuvant treatment. Only 8% of patients with intermediate- or high-grade tumors received adjuvant or neoadjuvant treatment in this study. Neoadjuvant therapy was often employed for tumors with risk of positive margins on resection. The 2-year survival of intermediate and high grade improved by 38% with addition of chemotherapy and/or radiotherapy to surgery (49.4 vs. 80%).
Large tumor size also adversely affected outcomes. The 2-year survival for tumors > 5 cm also improved significantly with combination treatment compared to surgery alone. In a review by Miyajima et al., factors such as age, sex, tumor size, mitotic figures, necrosis and stage affected prognosis [17]. In our analysis, symptomatic patients performed worse as compared to asymptomatic patients. This may be because asymptomatic patients were incidentally diagnosed and hence treated at an early stage. On the other hand, symptomatic patients were most likely diagnosed at advanced stage and thereby had grave prognosis.
Further investigation could benefit from novel insights into its molecular pathogenesis, including genetic mutations or aberrant signaling pathways driving tumor initiation and progression. Exploring the tumor microenvironment's role could elucidate interactions between tumor cells and surrounding stromal components, potentially unveiling novel therapeutic targets or predictive biomarkers. Moreover, in-depth studies characterizing the radiological and histopathological features specific to renal leiomyosarcoma could aid accurate diagnosis and differentiation from other renal neoplasms. Collaborative efforts leveraging multi-omics approaches, such as genomics, transcriptomics and proteomics, could provide a comprehensive understanding of the disease's heterogeneity and inform personalized treatment strategies.
This is the most extensive study of renal LMS reporting on treatment, long-term survival outcomes and prognostic factors, from 188 cases of 85 publications since 1952. Drawing definitive conclusions from this review concerning this uncommon histology is a challenge as there is heterogeneity in data, and completeness of data could not be achieved due to missing information for certain variables in some case reports. However, this study would help to broaden the understanding of natural history of this rare disease.
5 Conclusion
Primary renal LMS is rare entity. Diagnosis is often delayed due to non-specific clinical features and radiological findings. The recommended treatment is radical nephrectomy with en bloc tumor resection with negative margin with adjuvant radiotherapy or chemotherapy specifically for large- and high-grade tumors. Neoadjuvant radiotherapy or chemotherapy may be helpful in unresectable tumors. We wish to highlight the scarcity of available data, which is obvious considering its rarity, not allowing appropriate randomized clinical trials. Hence, we believe that multinational efforts from several centers for sarcomas are required to acquire reliable data from randomized trials regarding best management and validate current treatment strategy.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
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TD helped in data acquisition, analysis and interpretation, manuscript drafting. KP contributed to conception, design, data interpretation, manuscript drafting. SG, RM, RK, CKD, SK and SKD were involved in manuscript drafting and revising. TE and PG helped in data acquisition and manuscript drafting. SGh performed conception, manuscript drafting and revising. All authors have approved the submitted version and agreed both to be personally accountable for the author's own contributions and to ensure that questions related to the accuracy or integrity of any part of the work, even ones in which the author was not personally involved, are appropriately investigated, resolved and the resolution documented in the literature.
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Periasamy, K., Dey, T., Goyal, S. et al. Primary renal leiomyosarcoma in adult patients: a systematic review and individual patient data analysis. Afr J Urol 30, 15 (2024). https://doi.org/10.1186/s12301-024-00418-1
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DOI: https://doi.org/10.1186/s12301-024-00418-1