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. 2021 Apr 22;32(6):882–888. doi: 10.1093/icvts/ivab012

Recurrence rates of surgically resected solitary fibrous tumours of the pleura: a systematic review and meta-analysis

Wan-Li Liu 1,2, Wei Wu 3, Qiong-Chuan Hong 1,2, Kun Lv 1,✉
PMCID: PMC8923378  PMID: 33885754

Abstract

 

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OBJECTIVES

Recurrence rates of solitary fibrous tumours of the pleura (SFTP) after surgical resection vary widely in the published literature. Our objective was to systematically review the existing literature to determine an accurate estimate of SFTP recurrence rates after surgical resection and to determine risk factors associated with recurrence.

METHODS

PubMed, EMBASE and the Cochrane library were systematically searched for randomized controlled trials and observational studies (prospective or retrospective) through 20 June 2020 that reported the recurrence rates after surgical resection. The outcome of interest was recurrence.

RESULTS

Of the 23 included studies comparing 1262 patients, the overall recurrence of SFTP in patients who underwent surgical resection was 9% [95% confidence interval (CI) 7–12%; I2 = 52%]. In addition, pooled benign and malignant recurrence rates were 3% (95% CI 2–5%; I2 = 8%) and 22% (95% CI 15–32%; I2 = 52%), respectively. A benign SFTP was associated with a significantly lower recurrence rate than a malignant SFTP [odds ratio (OR) 0.11; 95% CI 0.06–0.20; I2 = 0%]. There was no significant difference in the recurrence rates between lesions originating from parietal versus visceral pleura (OR 1.30; 95% CI 0.28–6.02; I2 = 59%). Female sex was associated with increased recurrence (OR 5.29; 95% CI 1.66–16.92; I2 = 0%).

CONCLUSIONS

Collectively, this systematic review demonstrated a 9% SFTP post-resection recurrence rate. Furthermore, the recurrence rates for benign and malignant SFTP were 3% and 22%, respectively. Histological malignancy and female sex were associated with higher risk.

Keywords: Solitary fibrous tumour of the pleura, Recurrence, Meta-analysis

INTRODUCTION

Solitary fibrous tumours of the pleura (SFTPs) are relatively rare mesenchymal neoplasms that originate from pluripotent stem cells under the pleural mesothelium and present with a broad spectrum of biological behaviours [1]. In 1931, Klemperer et al. [2, 3] first described SFTP. The tumour can be malignant or benign with an estimated incidence of 2.8 cases per 100 000 registrations. Approximately 90% of SFTPs are benign, whereas 10% are malignant. Malignant SFTPs were mainly diagnosed according to criteria proposed by England et al. [4].

No standard practice guidelines have been developed to guide therapeutic decisions for these patients. Complete surgical resection of the lesion is considered the best treatment and the best predictor of survival for all benign and malignant SFTP [5, 6]. However, surveillance after resection of SFTP remains undefined. Caution is warranted because the post-resection recurrence rates were higher during the intermediate follow-up period in patients with benign or malignant SFTP [7]. Unfortunately, no study including a large number of patients who had complete surgical resection reported the overall recurrence of SFTP. Therefore, we performed a systematic review and meta-analysis to review the existing literature to determine an accurate estimate of overall recurrence rates of SFTP and recurrence rates of benign and malignant SFTP, respectively, after surgical resection and to determine the risk factors associated with recurrence.

METHODS

Our systematic review and meta-analysis were performed in accordance with Preferred Reporting Items for Systematic Review and Meta-analysis (PRISMA). The protocol for this review was prospectively registered with PROSPERO (CRD42020193089).

Inclusion and exclusion criteria

The inclusion criteria were as follows: (i) randomized controlled trials (RCTs), nonrandomized trials and observational studies of more than 10 participants; (ii) participants with a solitary fibrous tumour of the pleura who had a complete resection, the pathological diagnosis (benign or malignant) of which was confirmed; and (iii) participants with a malignant SFTP diagnosed according to the England criteria. We excluded studies that were case reports with fewer than 10 participants; if the patients received chemotherapy or radiotherapy alone; and if no outcomes and no prognoses were reported.

Search strategy

We systematically searched 3 databases (PubMed, EMBASE and Cochrane library) for RCTs and observational studies (prospective or retrospective) through 20 June 2020. We searched Medical Subject Headings and Embase Subject Headings for ‘solitary fibrous tumour, pleural’ and ‘recurrence’ or ‘prognosis’ in the Embase, PubMed and Cochrane Library databases. To maximize the search for relevant studies, the search did not apply language restrictions. The detailed literature search strategy is presented in the Supplementary Material, Files.

Data extraction and quality assessment

Two independent researchers (W.-L.L. and K.L.) used a standard data extraction form to obtain the following data from each included trial: first author, year of publication, study type, number of incurrences and included patients, characteristics of participants and follow-up years. Disagreements were resolved by consensus.

The risk of bias and the methodological quality of all included studies were assessed by 2 independent researchers (W.-L.L. and W.W.) based on Cochrane risk-of-bias criteria [8] for RCTs and the Agency for Healthcare Research and Quality [9] for observational studies. Disagreements were resolved through discussion and by consulting a third researcher (K.L.). The Cochrane risk-of-bias tool involved 7 items, and each quality item was graded as low risk, high risk or unclear risk. The items included (i) random sequence generation; (ii) allocation concealment; (iii) blinding of participants and personnel; (iv) blinding of assessment; (v) incomplete outcome data; (vi) selective reporting; and (vii) other sources of bias. The Agency for Healthcare Research and Quality tool involved an 11-item checklist. An item would be scored ‘0’ if it was answered with a ‘no’ or ‘unclear’; if it was answered ‘yes’, then the item would be scored ‘1’.

Statistical analyses

The primary measure was overall recurrence rate for patients with SFTP who had surgical resection. The recurrence rates for benign and malignant SFTP were respectively pooled for all studies that reported these outcomes. We used odd ratios and their associated 95% confidence interval (CI) to estimate the risk factors of recurrence: male versus female, benign versus malignant histology, diameter ≥10 cm versus diameter <10 cm and originating from parietal versus visceral pleura. We assessed heterogeneity using the I2 statistics. We pooled the recurrence data using fixed effects models when significant heterogeneity was not present (I2 < 50%); we used random effects models to pool outcomes if significant heterogeneity was present (I2 > 50%). A continuity correction was applied if any study had either zero or all events [10]. Sensitivity analysis was performed by excluding low-quality studies. The presence of publication bias was assessed qualitatively by visual estimates of the funnel plot and quantitatively by using Egger’s test [11].

All statistical analyses were performed using meta package in R (version 4.0.2; R Project for Statistical Computing, Institute for Statistics and Mathematics, Vienna, Austria). All tests were 2-tailed, and a P-value less than 0.05 was considered statistically significant.

RESULTS

Eligible studies and study characteristics

We initially identified 788 records through database searching. Titles and abstracts of 750 records were screened for inclusion. After removing 717 studies, we read the full texts of 33 studies and included 23 eligible studies [5, 12–31] in the final meta-analysis (Fig. 1). The 23 studies were retrospective that involved a total of 1262 patients. Table 1 reports the baseline characteristics of the included studies. Supplementary Material, Files show the assessment of the risk of bias for all included studies.

Figure 1:

Figure 1:

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Flow diagram of literature search and screening process. E-SFT: extrapleural solitary fibrous tumour; PM: pleural mesothelioma.

Table 1:

Baseline characteristics of included studies

Study Year Type of study Included years Number of patients Age Male Benign Follow-up year(s)
Bellini 2019 Retrospective 1972–2018 107 59.72 (18.69–79.95) 76 79 7 (0–42)
Bini 2009 Retrospective 1984–2007 18 56 (33–77) 7 NR NR
Cardillo 2009 Retrospective 1990–2008 110 56.4 (17–79) 63 95 1–18.5a
Diebold 2017 Retrospective 2000–2015 78 61 ± 11 32 NR 3 (0.08–18)
England 1989 Retrospective NR 155 NR NR 98 4.8 (0.08–26.4)
Enon 2012 Retrospective 1985–2009 25 41.1 (25–64) 14 25 2.8 (0.8–11.8)
Fattahi 2016 Retrospective 2001–2014 13 50.46 (26–76) 6 NR 10b
Franzen 2014 Retrospective 1992–2012 42 62 (56–71) 20 24 NR
Guo 2011 Retrospective 2004–2008 39 44.6 ± 14.5 27 NR 3.4 (2.5–7.4)
Harrison-Phipps 2009 Retrospective 1972–2002 84 57 (34–83) 39 73 12 (2–32)
Lahon 2012 Retrospective 1980–2010 156 58 (13–87) 72 90 NR
Liu 2010 Retrospective 2000–2008 21 52.5 (33–76) 9 18 3.6 (0.3–8)
Liu 2007 Retrospective 1979–2004 15 57 (25–76) 8 11 4.8 (0.6–16)
Lococo 2015 Retrospective NR 43 NR 43 0 NR
Lu 2008 Retrospective 2002–2007 13 47 (27–72) 4 6 1.3 (0.3–3)
Magdeleinat 2002 Retrospective 1981–2000 60 55 (30–87) 25 38 7.3 (0.3–21.1)
Mezzetti 2002 Retrospective 1986–2000 15 55b 4 NR 1–15a
Perna 2008 Retrospective 1995–2006 15 51.5 (29–82) 3 9 6.6b
Schirosi 2008 Retrospective NR 88 59.5 (33–88) 43 NR 7.1c
Takahama 2003 Retrospective 1992–2002 13 49.8 (37–72) 7 NR 4.1 (0.5–10)
Tan 2018 Retrospective 2003–2015 82 58 (29–79) 37 70 4.7c
Tapias 2012 Retrospective 1977–2010 59 57 ± 14 32 NR 12.9 (0.08–32.8)
Yanik 2019 Retrospective 2006–2016 16 60.5 (30–87) 9 14 4.2 (0.2–9.5)
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Data are presented as median (range) or mean ± standard deviation, unless otherwise indicated.

a

Range.

b

Mean.

c

Median.

NR: not reported.

Overall recurrence rates

All 23 studies reported the outcomes and prognoses of patients with SFTP who underwent surgical resection. The pooled overall recurrence rate was 9% (95% CI 7–12%; I2 = 52%) (Fig. 2). The moderate heterogeneity likely reflects the wide variety of patient populations and methods presented in the included articles. A sensitivity analysis was conducted to investigate the stability of the result by omitting 1 study at a time. The meta-analysis results for overall recurrence were robust in sensitivity analyses (Supplementary Material, Files). Finally, based on the funnel plot analysis, asymmetry was found for the meta-analysis results (Fig. 3); in addition, the Egger test (P = 0.03) detected significant small study effects.

Figure 2:

Figure 2:

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Estimate of recurrence of solitary fibrous tumour of the pleura after surgical resection.

Figure 3:

Figure 3:

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Funnel plot of recurrence rate to detect publication bias. Maximum-likelihood estimator for tau2.

Benign and malignant recurrence rates

Ten studies reported the histopathological features of the patients whose SFTP recurred [4, 5, 13, 19, 21, 23, 25, 27, 30, 31]. A total of 577 patients with benign SFTP were involved, and the pooled recurrence rate was 3% (95% CI 2–5%; I2 = 8%) (Fig. 4A). Furthermore, a total of 296 participants with malignant SFTP were included; they had a pooled relapse rate of 22% (95% CI 15–32%; I2 = 52%) (Fig. 4B).

Figure 4:

Figure 4:

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Estimate of recurrence of benign and malignant solitary fibrous tumours of the pleura (SFTP). (A) Recurrence rate of benign SFTP and (B) recurrence rate of malignant SFTP.

Factors associated with recurrence

In general, we examined the association between the histopathological features and SFTP recurrence that were extracted from 10 observational studies [4, 5, 13, 19, 21, 23, 25, 27, 30, 31]. The recurrence rates were lower in the benign group than in the malignant group [odds ratio (OR) 0.11, 95% CI 0.06–0.20; I2 = 0%] (Fig. 5A). As shown in Fig. 5B, 4 articles reported the origin of lesions of relapse cases. There was no significant difference in the recurrence rates of tumours originating from the parietal versus visceral pleura (OR 1.30, 95% CI 0.28–6.02; I2 = 59%) (Fig. 5B) [5, 19, 23, 25]. Only 2 studies included the gender of the patients whose tumours recurred [5, 23]. The recurrence rates were higher in female patients than in male patients (OR 5.29, 95% CI 1.66–16.92; I2 = 0%) (Fig. 5C).

Figure 5:

Figure 5:

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Meta-analysis results of odds ratios for solitary fibrous tumours of the pleura. (A) Benign features versus malignant features from 10 studies; (B) origin from parietal pleura versus visceral pleura from 4 studies; (C) women versus men from 2 studies.

Meta-regression

We performed a meta-regression to find potential sources of heterogeneity between the studies. Unfortunately, it did not demonstrate any significant association between recurrence rates and publication year, study sample size or follow-up year (Table 2). There was considerable unexplained residual heterogeneity even after adjusting for the different study characteristics.

Table 2:

Univariate meta-regression of study characteristics

Studies, n P-value for difference Residual (%)
Publication year
 Before 2010 11 0.76 50
 After 2010 12
Study sample size
 <20 8 0.94 52.7
 >20 15
Follow-up (years) 0.8 44
 <5 13
 >5 9
 NR 4
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NR: not reported.

DISCUSSION

This study is the first to systematically review the existing literature on rates of recurrence in patients with SFTP who had complete resection of the tumour. A meta-analysis of data from 23 eligible studies, totalling over 1262 participants, showed that 3% of patients experience SFTP recurrence after surgical resection. Additionally, the recurrence rates of benign and malignant SFTP were 3% and 22%, respectively.

Complete resection with tumour-free margins has long been considered an undisputable principle of oncological surgery. This principle also applies to SFTP: En bloc resection with tumour-free margins represents the best predictor of good prognosis and the mainstay of treatment for SFTP [31, 32]. However, an important but as yet unresolved question is how to predict the recurrence of SFTP in the postoperative period. Results of this meta-analysis showed that histological malignancy was a risk for recurrence. The criteria used for the diagnosis of malignant SFTP were proposed by England et al. [4] as follows: (i) mitotic count greater than 4 mitoses per 10 high-power fields; (ii) increased cellularity (sarcoma-like appearance); (iii) nuclear pleomorphism; and (iv) presence of tumour necrosis. The presence of these pathological characteristics may explain the higher risk of recurrence seen in patients with a malignant histopathological diagnosis [5].

Furthermore, the biological behaviour did not always correlate with atypical histological features. For that reason, combining histopathological and macroscopic tumour characteristics, de Perrot et al. [33], Tapias et al. [22] and Diebold et al. [14] proposed de Perrot staging, the Tapias score and the Diebold score, respectively. Tapias et al. provided evidence that lesions that originated from parietal pleura had an increased risk of recurrence. However, our meta-analysis showed that the difference of recurrence between tumours originating from parietal and visceral pleura was not statistically significant. More large studies are necessary to determine the association between the mode of origin of the tumour and recurrence. In addition, the available literature reported that the risk factors associated with recurrence included sessile morphology, a tumour >10 cm and a high proliferation rate evident with MIB-1 labelling [14, 22]. Unfortunately, we were not able to evaluate these factors because the related data could not be extracted. The goal of recognizing risk factors associated with recurrence is to identify, at the time of the initial resection, patients with the highest risk of recurrence who may benefit from closer and longer postoperative follow-up.

No authors reported an association between gender and recurrence, and no epidemiological study reported a gender difference in the prevalence of SFTP. In our meta-analysis, the pooled results showed that female sex was a risk factor for recurrence, although our analysis included only 2 studies. However, our meta-analysis provided encouraging initial evidence that female sex was associated with a higher risk of recurrence. Gender differences should be taken into account when a recurrence score or staging system for SFTP is proposed in the future. Due to the rarity of this disease and its unknown aetiology and pathogenesis, it is difficult to determine the risk factors associated with recurrence after surgery. Accordingly, more studies are needed to determine risk factors for recurrence. We expect that identifying risk factors could improve the management of SFTP.

Strengths and limitations

This is the first systematic review of SFTP recurrence rates after complete resection. It provides the most reliable estimate of overall, benign and malignant recurrence to date, based on comprehensive evaluation of existing articles. Having an accurate estimate for recurrence will enable medical practitioners to provide better counselling for patients with SFTP who had complete resection. Further analysis identified risk factors associated with higher recurrence rates, including histological malignancy and female sex. These findings will facilitate communication with patients and could provide evidence for further studies.

This study has several limitations. First, the increasing recognition of these disease processes is controversial, so we may have missed some articles in order to meet the accuracy of the data analyses. Second, there was moderate heterogeneity among the included studies, even though a random effects meta-analysis model was used. This heterogeneity may have reduced the precision of the final estimated recurrence rate. Unfortunately, unexplained residual heterogeneity was found after meta-regression analysis. Third, the estimation of risk factors was not completely assessed in all included articles. Fourth, because all of the studies were retrospective, there was a high risk of reporting and ascertainment bias, and asymmetry was found for the meta-analysis results. Lastly, no RCTs were included in our meta-analysis. Retrospective observational studies have the natural limitation of selection bias and unmeasured confounders. As a result, in the future, RCTs with a sufficient number of samples should be conducted to estimate the recurrence rates.

CONCLUSIONS

To our knowledge, this is the first meta-analysis and systematic review to study SFTP recurrence. We found that 9% of patients with SFTP who underwent an operation will develop a recurrence. Furthermore, the post-resection recurrence rates for patients with benign and malignant SFTP are 3% and 22%, respectively. Two factors were associated with a higher risk of recurrence: malignant histopathological features and female sex. We did not find an association between the origin of the tumour and recurrence rates. The data were insufficient to consider development of a risk stratification system.

SUPPLEMENTARY MATERIAL

Supplementary material is available at ICVTS online.

Conflict of interest: none declared.

Supplementary Material

ivab012_Supplementary_Data
Click here for additional data file. (2.9MB, zip)

ABBREVIATIONS

CI

Confidence interval

OR

Odds ratio

RCT

Randomized controlled trial

SFTP

Solitary fibrous tumours of the pleura

Author contributions

Wan-Li Liu: Conceptualization; Data curation; Formal analysis; Methodology; Validation; Visualization; Writing—original draft; Writing—review & editing. Wei Wu: Conceptualization; Formal analysis; Methodology; Validation; Writing—original draft; Writing—review & editing. Qiong-Chuan Hong: Conceptualization; Supervision; Writing—original draft; Writing—review & editing. Kun Lv: Conceptualization; Methodology; Supervision; Validation; Visualization; Writing—original draft; Writing—review & editing.

Reviewer information

Interactive CardioVascular and Thoracic Surgery thanks Stefano Margaritora and the other, anonymous reviewer(s) for their contribution to the peer review process of this article.

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Associated Data

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Supplementary Materials

ivab012_Supplementary_Data
Click here for additional data file. (2.9MB, zip)

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