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Diagnostic value of fibulin-3 for malignant pleural mesothelioma: A systematic review and meta-analysis

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Oncotarget. 2016; 7:84851-84859. https://doi.org/10.18632/oncotarget.12707

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Ran Ren, Pengpeng Yin, Yan Zhang, Jianyun Zhou, Yixing Zhou, Rufu Xu, Hai Lin _ and Chunji Huang

Abstract

Ran Ren1,*, Pengpeng Yin1,*, Yan Zhang1,*, Jianyun Zhou1, Yixing Zhou1, Rufu Xu1, Hai Lin2, Chunji Huang2

1Division of Scientific Research, Xinqiao Hospital, Third Military Medical University, Chongqing, 400037, China

2Department of Scientific Research, Third Military Medical University, Chongqing, 400038, China

*These authors have contributed equally to this work

Correspondence to:

Hai Lin, email: 36348599@qq.com

Chunji Huang, email: 13883197243@163.com

Keywords: Fibulin-3, malignant pleural mesothelioma, diagnostic value, meta-analysis, systematic review

Received: September 08, 2016     Accepted: October 01, 2016     Published: October 17, 2016

ABSTRACT

Background: Several studies have investigated the diagnostic value of fibulin-3 for malignant pleural mesothelioma (MPM), but the results were various. Therefore, we performed a systematic review and meta-analysis to evaluate the diagnostic value of fibulin-3 for MPM.

Results: Eight studies were included in this work. The overall sensitivity of blood fibulin-3 were 0.87 (95% CI, 0.58 – 0.97) and 0.89 (95% CI, 0.77 – 0.95), respectively. The overall sensitivity and specificity of PF fibulin-3 for MPM were 0.73 (95% CI, 0.54 – 0.86) and 0.80 (95% CI, 0.60 – 0.91), respectively. The area under curve of blood and pleural effusion (PF) Fibulin-3 were 0.94 (95% CI, 0.91 – 0.96) 0.83 (95% CI, 0.79 – 0.86), respectively.

Methods: PubMed and EMBASE databases were searched up to July 29, 2016 to verify studies investigating the diagnostic value of fibulin-3 for MPM. The quality of eligible studies was assessed using the revised Quality Assessment for Studies of Diagnostic Accuracy tool (QUADAS-2). The overall sensitivity and specificity were pooled using a bivariate model.

Conclusion: Fibuoin-3 is a useful diagnostic marker for MPM.


INTRODUCTION

Malignant pleural mesothelioma (MPM) is one of the most common cancers in asbestos-exposed individuals around the world [1, 2]. Timely and accurate diagnosis of MPM can improve the outcomes of patients [3]. Currently, the diagnosis of MPM mainly relies on pleural biopsy, which is invasive and the sample error is a problem [4, 5]. Therefore, developing non-invasive biomarkers for MPM diagnosis is of great value [6]. During past decades, many circulating biomarkers for MPM has been developed, such as soluble mesothelin-related peptides (SMRP) [7, 8] and osteopontin [9, 10]. However, the sensitivity and specificity of theses biomarkers are modest. Therefore, it is valuable to explore novel biomarkers that can improve the diagnostic value of the traditional biomarkers or replace them.

Fibulin-3 is a secreted glycoprotein that plays an important role in the regulation of cell migration and proliferation [11]. During past years, many studies have revealed that fibulin-3, either in blood or pleural effusion (PF), is a potential diagnostic biomarker for MPM [6]. However, the results from these studies were heterogeneous. Therefore, we performed a systematic review and meta-analysis to investigate the diagnostic value of fibulin-3 for MPM.

RESULTS

Summary of eligible studies

Eight studies were included in present systematic review and meta-analysis [1219]. A flowchart depicting study selection is shown in Figure 1. Summary of eligible studies is listed in Table 1. Eight studies investigated the diagnostic value of blood (three used serum [15, 17, 18] and five used plasma [1214, 16, 19]) fibulin-3 for MPM and five studies investigated the diagnostic value of PF fibulin-3. The study performed by Pass et.al. [12] contained two study cohorts and thus is regarded as two independent studies. The sample sizes ranged from 36 to 228. Components of control in eligible studies were various, including asbestos-exposed persons [12, 13, 18, 19], patients with pleural effusion [13, 16, 19] or metastatic pleural malignancy [15], healthy controls [17] or patients with extrapleural pneumonectomy [14]. One study did not report reference standard used for MPM diagnosis [12], and one study [13] used biopsy and follow-up to diagnose MPM. The remaining studies used biopsy to as reference standard. One study [14] was retrospective design and two [15, 19] did not report the type of design; and the remaining studies were prospective design.

Table 1: Summary of included studies

Author

Year

Country

N

Component of control

Reference

Specimen

Design

Blood

 

 

 

 

 

 

 

Pass [12], Detroit cohort

2012

USA

228

AEPs

NR

Plasma

Prospective

Pass [12], Toronto cohort

2012

USA

144

AEPs

NR

Plasma

Prospective

Creaney [13]

2014

Australia

202

PFs; AEPs

Biopsy and follow-up

Plasma

Prospective

Kirschner [14]

2015

Switzerland

130

Patients with extrapleural pneumonectomy or undergoing cardiac or aortic surgery for CAD or aortic disease, pleural plaques or pleuritis

Biopsy

Plasma

Retrospective

Agha [15]

2014

Egypt

36

Metastatic pleural malignancy

Biopsy

Serum

Unknown

Elgazzar [16]

2014

Egypt

60

Malignant PFs

Biopsy

Plasma

Prospective

Kaya [17]

2015

Turkey

83

Healthy controls

Biopsy

Serum

Prospective

Demir [18]

2016

Turkey

90

AEPs

Biopsy

Serum

Prospective

Napolitano [19]

2016

USA and UK

80

Benign PFs; AEPs

Biopsy

Plasma

Unknown

PF

 

 

 

 

 

 

 

Pass [12], Detroit cohort

2012

USA

167

Patients with PF

NR

PF

Prospective

Creaney [13]

2014

Australia

174

Patients with PF

Biopsy and follow-up

PF

Prospective

Kirschner [14]

2015

Australia

90

Patients with PF

Biopsy

PF

Retrospective

Agha [15]

2014

Egypt

36

Patients with PF

Biopsy

PF

Unknown

Elgazzar [16]

2014

Egypt

60

Patients with PF

Biopsy

PF

Prospective

N, sample size; PF, pleural effusion; CAD, coronary artery disease; AEP, asbestos-exposed person; NR, not reported.

Flow chart depicting the literature search and study selection process.

Figure 1: Flow chart depicting the literature search and study selection process.

Quality assessment of eligible studies

Quality assessment of eligible studies is listed in Table 2. The patient selection domain of all eligible studies was labeled as high because lacking of uniform including and excluding criteria, and the study cohort in each eligible studies was not enrolled consecutively. Index domain in all eligible studies, except one [13], was labeled as unknown because whether index test was performed in a blind manner was not reported. Reference standard domain in one study [12] was labeled as unknown because the diagnostic criteria for MPM was not reported. Flow and timing domain of four studies was labeled as high because of the differential verification bias [17, 18], partial verification bias [12] or disease progression bias [13].

Table 2: Quality assessment of eligible studies

Study

Risk of bias

Applicability concerns

Patient selection

Index test

Reference standard

Flow and timing

Patient selection

Index test

Reference standard

Serum

 

 

 

 

 

 

 

Pass [12], Detroit cohort

High

Unknown

Unknown

High

Low

Low

Unknown

Pass [12], Toronto cohort

High

Unknown

Unknown

High

Low

Low

Unknown

Creaney [13]

High

Low

Low

High

Low

Low

Low

Kirschner [14]

High

Unknown

Low

Low

High

Low

Low

Agha [15]

High

Unknown

Low

Low

Low

Low

Low

Elgazzar [16]

High

Unknown

Low

Low

Low

Low

Low

Kaya [17]

High

Unknown

Low

High

High

Low

Low

Demir [18]

High

Unknown

Low

High

Low

Low

Low

Napolitano [19]

High

Unknown

Low

Low

Low

Low

Low

PF

 

 

 

 

 

 

 

Pass [12]

High

High

Unknown

High

Low

Low

Unknown

Creaney [13]

High

Low

Low

High

Low

Low

Low

Kirschner [14]

High

Unknown

Low

Low

Low

Low

Low

Agha [15]

High

Unknown

Low

Low

Low

Low

Low

Elgazzar [16]

High

Unknown

Low

Low

Low

Low

Low

Diagnostic value of fibulin-3 for MPM

Table 3 lists the diagnostic value of fibulin-3 in each eligible studies. All studies used ELISA to determine fibulin-3.

Table 3: Diagnostic value of fibulin-3 in eligible publications

Author

Test method

MPM/Control

Cut-offs

TP

FN

FP

TN

Blood

 

 

 

 

 

 

 

Pass [12], Detroit cohort

ELISA

92/136

52.8 ng/ml

66

26

0

136

Pass [12], Toronto cohort

ELISA

48/96

28.96 ng/ml

35

13

11

85

Creaney [13]

ELISA

82/120

29 ng/ml

39

43

35

85

Kirschner [14]

ELISA

84/56

29 ng/ml

11

73

4

52

Agha [15]

ELISA

25/11

66.5 ng/ml

22

3

2

9

Elgazzar [16]

ELISA

30/30

54.3 ng/ml

30

0

1

29

Kaya [17]

ELISA

43/40

30.1 ng/ml

42

1

5

35

Demir [18]

ELISA

42/48

51.41 ng/ml

37

5

16

32

Napolitano [19]

ELISA

22/58

29 ng/ml

22

0

15

43

PF

 

 

 

 

 

 

 

Pass [12]

ELISA

74/93

346.01 ng/ml

62

12

11

82

Creaney [13]

ELISA

103/71

346 ng/ml

61

42

34

37

Kirschner [14]

ELISA

30/60

346 ng/ml

14

22

22

38

Agha [15]

ELISA

25/11

150 ng/ml

18

7

2

9

Elgazzar [16]

ELISA

30/30

520 ng/ml

27

3

1

29

PF, pleural effusion; ELISA, enzyme-linked immunosorbent assay; TP, true positive; TN, true negative; FP, false positive; FN, false negative.

Figure 2 is a forest plot for blood fibulin-3. The overall sensitivity and specificity of blood fibulin-3 for MPM were 0.87 (95% CI, 0.58 – 0.97) and 0.89 (95% CI, 0.77 – 0.95), respectively. Significant heterogeneity was observed for both sensitivity and specificity, with I2 of 96 and 93 respectively. Table 4 lists the results of subgroup analysis. Type of data collection (prospective or others), matrix used for fibulin-3 measurement (serum or plasma) and the components of controls (asbestos-exposed individual only or others), were not the sources of heterogeneity.

Table 4: Diagnostic accuracy of blood fibulin-3 for MPM

 

Cohorts

Sensitivity (95% CI)

Specificity (95% CI)

Blood

 

 

 

 All

9

0.87 (0.58 – 0.97)

0.89 (0.77 – 0.95)

Specimen

 

 

 

 Serum

3

0.94 (0.80 – 1.00)

0.80 (0.58 – 1.00)

 Plasma

6

0.79 (0.52 – 1.00)

0.92 (0.84 – 1.00)

Design

 

 

 

 Prospective

6

0.88 (0.70 – 1.00)

0.91 (0.81 – 1.00)

 Retrospective or unknown

3

0.81 (0.42 – 1.00)

0.86 (0.67 – 1.00)

Control

 

 

 

 AEP only

3

0.79 (0.40 – 1.00)

0.93 (0.83 – 1.00)

 Others

6

0.90 (0.72 – 1.00)

0.87 (0.74 – 0.99)

AEP, asbestos-exposed person; CI, confidence interval.

Forest plots estimating the sensitivity and specificity of blood fibulin-3 for MPM.

Figure 2: Forest plots estimating the sensitivity and specificity of blood fibulin-3 for MPM. Each point represents the sensitivity and specificity of each eligible studs and error bars are 95% CIs.

The overall sensitivity and specificity of PF fibulin-3 for MPM were 0.73 (95% CI, 0.54 – 0.86) and 0.80 (95% CI, 0.60 – 0.91), respectively. The I2 for sensitivity and specificity were 91 and 92 respectively, indicating that great heterogeneity was exist among eligible studies.

The AUCs for sROC of blood and PF fibulin-3 were 0.94 (95% CI, 0.91 – 0.96) and 0.83 (95% CI, 0.79 – 0.86), respectively (Figure 3). The diagnostic odds ratios (DORs) for blood and PF fibulin-3 were 53 (95% CI, 10 – 289) and 11 (95% CI, 2 – 59), respectively.

Summary receiver operating characteristic curves for overall diagnostic accuracy of blood fibulin-3.

Figure 3: Summary receiver operating characteristic curves for overall diagnostic accuracy of blood fibulin-3.

Publication bias

Figure 4 shows a funnel plot for the eligible studies. Obvious symmetry was observed, indicating publication bias is insignificant (P= 0.70).

A Funnel plot assessing publication bias.

Figure 4: A Funnel plot assessing publication bias.

DISCUSSION

To the best of our knowledge, this is the first meta-analysis investigating the diagnostic value of blood and PF fubulin-3 for MPM. The major findings of present study are as follows. First, both blood and PF fibulin-3 were useful diagnostic markers for MPM. Second, the available studies have some design weakness and further well-designed studies are needed to rigorously evaluate the diagnostic value of fibulin-3. Third, there was no publication bias among all available studies, indicating that the results of present work are reliable.

To present, many diagnostic biomarkers for MPM has been developed. Among these biomarkers, SMRP and osteopontin are the most promising ones [12, 20]. Evidence from meta-analysis revealed that the diagnostic sensitivity and specificity for SMRP were 0.61 and 0.87, respectively [7]. For osteopontin, a meta-analysis also revealed that its sensitivity and specificity were 0.65 and 0.81, respectively [10]. Our study revealed that the diagnostic specificity of blood fibulin-3 was 0.89, which was comparable to those of SMRP and osteopontin. However, the sensitivity of blood fibulin-3 was 0.87, which was obviously higher than those of SMRP and osteopontin. Therefore, blood fibulin-3 represents a promising diagnostic marker for MPM, and it may have a potential to replace SMRP or osteopontin in MPM diagnosis. Further studies designed in a head-to-head comparison manner are needed to clarify whether the diagnostic value of fibulin-3 is superior to those of SMRP and osteopontin.

AUC of sROC is an index determining overall diagnostic value of a test [21, 22]. Our study revealed that the AUCs for blood and PF fibuin-3 were 0.94 and 0.83, respectively, indicating that both PF and blood fibulin-3 are useful for MPM diagnosis. Besides, previous meta-analysis also show that the AUCs for SMRP and osteopontin were 0.81 and 0.83, respectively, also supporting our hypothesis that the diagnostic value of fibulin-3 is superior to those of SMRP and osteopontin.

The sources of PF fibulin-3 are largely unknown. Three studies have investigated the correlation between circulating and PF fibulin-3 [12, 13, 15], and two failed to observe a positive correlation between circulating and PF fibulin-3 [12, 13]. These results indicate that PF fibulin-3 is not derived from circulating fibulin-3, and measuring fibulin-3 in PF may yield additional diagnostic value. However, in a study performed by Agha et al. [15], there was a good relationship between serum and PF fibulin-3. Reasons for inconsistent finding across these three studies are unknown. Further studies are needed to elucidate the basis of the discrepancy.

An exploration of the sources for heterogeneity, rather than pooling the results of all eligible studies, is an important goal of meta-analysis. Because great heterogeneity was observed across all eligible studies investigating diagnostic value of blood fibulin-3 for MPM, we performed a subgroup analysis to explore the sources of heterogeneity. We found that some of the design characteristics, including type of data collection, matrix used for fibulin-3 measurement and the components of controls, were not the sources of heterogeneity. Future studies with more eligible studies are needed to explore the sources of heterogeneity.

To facilitate more well-designed future studies on this topic, some of the methodological weakness of the available studies should be noted. The major design weakness of available studies was two-gate design [23], which can result participant selection bias. The subjects in all studies were not enrolled according to a pre-designed inclusion and exclusion criteria. That means, the subjects enrolled in these studies may not be representative of the target population in whom MPM is suspected. Therefore, the conclusions of available studies should be interpreted with caution.

Taken together, present study indicated that fibulin-3 was a useful diagnostic marker for MPM. Due to the small number of eligible studies, and all of the eligible studies have higher risk for subject selection, further well-designed studies are needed to rigorously evaluate the diagnostic value of fibulin-3 for MPM.

MATERIALS AND METHODS

Database and literature retrieve

This systematic review and meta-analysis was performed in accordance with preferred reporting items for systematic reviews and meta-analyses (PRISMA) guideline [24]. Two investigator independently searched PubMed and EMBASE for potential eligible studies. The last search date is July 29, 2016. The searched algorithm used for searching PubMed was “(Fibulin-3 OR EFEMP1 protein, human[nm] OR “Fibulin 3”) AND mesothelioma”. Similar search strategy was used for searching EMBASE. A manual search was also performed by reviewing references listed at the end of retrieved publications.

Inclusion and exclusion criteria

Inclusion criteria of this systematic review and meta-analysis were: (1) studies investigating the diagnostic value of fibulin-3, either in blood or PF, for MPM; (2) A 2 by 2 table can be constructed using sensitivity, specificity and sample size reported, or using data presented in the scatter plot. Conference abstracts and animal studies were excluded. Studies with sample size less than 10 were excluded because studies with small sample sizes can yield bias.

The study selection process was performed by two independent investigators. In the first round, the titles and abstracts of retrieved publications were screened and the irrelevant studies were excluded. In the second round, a full text reviewing was performed to select eligible studies for the remaining studies. Disagreements were resolved by consensus or full text review.

Data extraction and quality assessment

Two investigators independently extracted data from eligible studies. Following data were extracted: sample size, publication year, sources of participants, components of control, reference standard used for MPM diagnosis, type of design (prospective or retrospective) and fibulin-3 measurement methods. For each eligible studies, a 2 by 2 table, which consisted of true positive (TP), false negative (FN), false positive (FP) and true negative (TN), was constructed.

The revised Quality Assessment for Studies of Diagnostic Accuracy tool (QUADAS-2) [25] was used to assess the quality of eligible studies. Any disagreement in quality assessment was resolved by consensus. The corresponding authors of the eligible studies were not contacted for unknown information regarding study design.

Statistical analysis

The overall sensitivity and specificity of fibulin-3 for MPM diagnosis were pooled using a bivariate model [26]. The summary receiver operating characteristic (sROC) curve was constructed to depict the overall diagnostic value of fibulin-3 [27]. The funnel plots and the Deeks’s test were used to test publication bias [28]. All analyses were performed in STATA 13.0 (Stata Corp LP, College Station, TX) and the midas command was used for all statistical analyses.

CONFLICTS OF INTEREST

The authors declare no conflicts of interest.

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