bims-tumhet Biomed News
on Tumor Heterogeneity
Issue of 2024‒03‒03
eighteen papers selected by
Sergio Marchini, Humanitas Research



  1. JCO Precis Oncol. 2024 Feb;8 e2300483
      PURPOSE: To meet the urgent need for accessible homologous recombination-deficient (HRD) test options, we validated a laboratory-developed test (LDT) and a functional RAD51 assay to assess patients with ovarian cancer and predict the clinical benefit of poly(ADP-ribose) polymerase inhibitor therapy.METHODS: Optimization of the LDT cutoff and validation on the basis of samples from 91 patients enrolled in the ENGOT-ov24/NSGO-AVANOVA1&2 trial (ClinicalTrials.gov identifier: NCT02354131), previously subjected to commercial CDx HRD testing (CDx). RAD51 foci analysis was performed and tumors with ≥five foci/nucleus were classified as RAD51-positive (homologous recombination-proficient).
    RESULTS: The optimal LDT cutoff is 54. Comparing CDx genome instability score and LDT HRD scores show a Spearman's correlation of rho = 0.764 (P < .0001). Cross-tabulation analysis shows that the sensitivity of the LDT HRD score is 86% and of the LDT HRD status is 91.8% (Fisher's exact test P < .001). Survival analysis on progression-free survival (PFS) of LDT-assessed patients show a Cox regression P < .05. RAD51 assays show a correlation between low RAD51 foci detection (<20% RAD51+ cells) and significantly prolonged PFS (P < .001).
    CONCLUSION: The robust concordance between the open standard LDT and the CDx, especially the correlation with PFS, warrants future validation and implementation of the open standard LDT for HRD testing in diagnostic settings.
    DOI:  https://doi.org/10.1200/PO.23.00483
  2. Cancer Immunol Res. 2024 Feb 26.
      Chromosomal instability is a hallmark of human cancer that is associated with aggressive disease characteristics. Chromosome mis-segregations help fuel natural selection, but they risk provoking a cGAS-STING immune response through the accumulation of cytosolic DNA. The mechanisms of how tumors benefit from chromosomal instability while mitigating associated risks, such as enhanced immune surveillance, are poorly understood. Here, we identify cGAS-STING-dependent upregulation of the nuclease TREX1 as an adaptive, negative feedback mechanism that promotes immune evasion through digestion of cytosolic DNA. TREX1 loss diminishes tumor growth, prolongs survival of host animals, increases tumor immune infiltration, and potentiates response to immune checkpoint blockade selectively in tumors capable of mounting a type I interferon response downstream of STING. Together, these data demonstrate that TREX1 induction shields chromosomally unstable tumors from immune surveillance by dampening type I interferon production and suggest that TREX1 inhibitors might be used to selectively target tumors that have retained the inherent ability to mount an interferon response downstream of STING.
    DOI:  https://doi.org/10.1158/2326-6066.CIR-23-1093
  3. Clin Epigenetics. 2024 Feb 27. 16(1): 34
      BACKGROUND: Cell-free DNA (cfDNA) contains a large amount of molecular information that can be used for multi-cancer early detection (MCED), including changes in epigenetic status of cfDNA, such as cfDNA fragmentation profile. The fragmentation of cfDNA is non-random and may be related to cfDNA methylation. This study provides clinical evidence for the feasibility of inferring cfDNA methylation levels based on cfDNA fragmentation patterns. We performed whole-genome bisulfite sequencing and whole-genome sequencing (WGS) on both healthy individuals and cancer patients. Using the information of whole-genome methylation levels, we investigated cytosine-phosphate-guanine (CpG) cleavage profile and validated the method of predicting the methylation level of individual CpG sites using WGS data.RESULTS: We conducted CpG cleavage profile biomarker analysis on data from both healthy individuals and cancer patients. We obtained unique or shared potential biomarkers for each group and built models accordingly. The modeling results proved the feasibility to predict the methylation status of single CpG sites in cfDNA using cleavage profile model from WGS data.
    CONCLUSION: By combining cfDNA cleavage profile of CpG sites with machine learning algorithms, we have identified specific CpG cleavage profile as biomarkers to predict the methylation status of individual CpG sites. Therefore, methylation profile, a widely used epigenetic biomarker, can be obtained from a single WGS assay for MCED.
    Keywords:  Methylation status; Multi-cancer early detection; WGBS; WGS; cfDNA fragmentation profile
    DOI:  https://doi.org/10.1186/s13148-024-01646-6
  4. bioRxiv. 2024 Feb 14. pii: 2024.02.12.579956. [Epub ahead of print]
      Immune system control is a major hurdle that cancer evolution must circumvent. The relative timing and evolutionary dynamics of subclones that have escaped immune control remain incompletely characterized, and how immune-mediated selection shapes the epigenome has received little attention. Here, we infer the genome- and epigenome-driven evolutionary dynamics of tumour-immune coevolution within primary colorectal cancers (CRCs). We utilise our existing CRC multi-region multi-omic dataset that we supplement with high-resolution spatially-resolved neoantigen sequencing data and highly multiplexed imaging of the tumour microenvironment (TME). Analysis of somatic chromatin accessibility alterations (SCAAs) reveals frequent somatic loss of accessibility at antigen presenting genes, and that SCAAs contribute to silencing of neoantigens. We observe that strong immune escape and exclusion occur at the outset of CRC formation, and that within tumours, including at the microscopic level of individual tumour glands, additional immune escape alterations have negligible consequences for the immunophenotype of cancer cells. Further minor immuno-editing occurs during local invasion and is associated with TME reorganisation, but that evolutionary bottleneck is relatively weak. Collectively, we show that immune evasion in CRC follows a "Big Bang" evolutionary pattern, whereby genetic, epigenetic and TME-driven immune evasion acquired by the time of transformation defines subsequent cancer-immune evolution.
    DOI:  https://doi.org/10.1101/2024.02.12.579956
  5. JAMA Netw Open. 2024 Feb 05. 7(2): e240407
      IMPORTANCE: Platinum-based chemotherapy is the backbone of standard-of-care treatment for patients with advanced-stage, high-grade serous carcinoma (HGSC), the most common form of ovarian cancer; however, one-third of patients have or acquire chemoresistance toward platinum-based therapies.OBJECTIVE: To demonstrate the utility of tumor-stroma proportion (TSP) as a predictive biomarker of chemoresistance of HGSC, progression-free survival (PFS), and overall survival (OS).
    DESIGN, SETTING, AND PARTICIPANTS: This prognostic study leveraged tumors from patients with HGSC in The Cancer Genome Atlas (TCGA) cohort (1993-2013) and an independent cohort of resected clinical specimens from patients with HGSC (2004-2014) available in diagnostic and tissue microarray formats from the University of Tübingen in Germany. Data analysis was conducted from January 2021 to January 2024.
    EXPOSURE: Diagnosis of HGSC.
    MAIN OUTCOMES AND MEASURES: Principal outcome measures were the ability of TSP to predict platinum chemoresistance, PFS, and OS. Using hematoxylin and eosin-stained slides from the Tübingen cohort (used for routine diagnostic assessment from surgical specimens) as well as tissue microarrays, representative sections of tumors for scoring of TSP were identified using previously evaluated cutoffs of 50% stroma or greater (high TSP) and less than 50% stroma (low TSP). Digitized slides from the TCGA Cohort were analyzed and scored in a similar fashion. Kaplan-Meier time-to-event functions were fit to estimate PFS and OS.
    RESULTS: The study included 103 patients (mean [SD] age, 61.6 [11.1] years) from the TCGA cohort and 192 patients (mean [SD] age at diagnosis, 63.7 [11.1] years) from the Tübingen cohort. In the TCGA cohort, there was no significant association of TSP levels with chemoresistance, PFS, or OS. However, in the Tübingen cohort, high TSP was associated with significantly shorter PFS (HR, 1.586; 95% CI, 1.093-2.302; P = .02) and OS (hazard ratio [HR], 1.867; 1.249-2.789; P = .002). Patients with chemoresistant tumors were twice as likely to have high TSP as compared to patients with chemosensitive tumors (HR, 2.861; 95% CI, 1.256-6.515; P = .01). In tissue microarrays from 185 patients from the Tübingen cohort, high TSP was again associated with significantly shorter PFS (HR, 1.675; 95% CI, 1.012-2.772 P = .04) and OS (HR, 2.491; 95% CI, 1.585-3.912; P < .001).
    CONCLUSIONS AND RELEVANCE: In this prognostic study, TSP was a consistent and reproducible marker of clinical outcome measures of HGSC, including PFS, OS, and platinum chemoresistance. Accurate and cost-effective predictive biomarkers of platinum chemotherapy resistance are needed to identify patients most likely to benefit from standard treatments, and TSP can easily be implemented and integrated into prospective clinical trial design and adapted to identify patients who are least likely to benefit long-term from conventional platinum-based cytotoxic chemotherapy treatment at the time of initial diagnosis.
    DOI:  https://doi.org/10.1001/jamanetworkopen.2024.0407
  6. J Natl Cancer Inst. 2024 Feb 28. pii: djae050. [Epub ahead of print]
      There is growing interest in multicancer detection (MCD) tests, which identify molecular signals in the blood indicating a potential preclinical cancer. A key stage in evaluating MCD tests is a prediagnostic performance study, in which investigators store specimens from asymptomatic persons and later test stored specimens from cancer cases and a random sample of controls to determine predictive performance. Performance metrics include cancer-specific true and false positive rates and a cancer-specific positive predictive value, with the latter compared to a decision-analytic threshold. The sample size tradeoff method, which trades imprecise targeting of the true positive rate for precise targeting of a zero false positive rate can substantially reduce sample size while increasing the lower bound of positive predictive value. For a 1-year follow-up, with ovarian cancer as the rarest cancer considered, the sample size tradeoff method yields a sample size of 163,000 compared with a sample size of 720,000 based on standard calculations. These design and analysis recommendations should be considered in planning a specimen repository and in the prediagnostic evaluation of MCD tests.
    DOI:  https://doi.org/10.1093/jnci/djae050
  7. Sci Rep. 2024 Feb 29. 14(1): 4973
      In China, circulating tumor DNA analysis is widely used and numerous assays are available. Systematic evaluation to help users make informed selections is needed. Nine circulating tumor DNA assays, including one benchmark assay, were evaluated using 23 contrived reference samples. There were two sample types (cell-free DNA and plasma samples), three circulating tumor DNA inputs (low, < 20 ng; medium, 20-50 ng; high, > 50 ng), two variant allele frequency ranges (low, 0.1-0.5%; intermediate, 0.5-2.5%), and four variant types (single nucleotide, insertion/deletion, structural, and copy number). Sensitivity, specificity, reproducibility, and all processes from cell-free DNA extraction to bioinformatics analysis were assessed. The test assays were generally comparable or superior to the benchmark assay, demonstrating high analytical sensitivity. Variations in circulating tumor DNA extraction and quantification efficiency, sensitivity, and reproducibility were observed, particularly at lower inputs. These findings will guide circulating tumor DNA assay choice for research and clinical studies, allowing consideration of multiple technical parameters.
    DOI:  https://doi.org/10.1038/s41598-024-54361-w
  8. Trends Cell Biol. 2024 Feb 28. pii: S0962-8924(24)00029-1. [Epub ahead of print]
      The Stimulator of Interferon Genes (STING) has a crucial role in mediating the immune response against cytosolic double-stranded DNA (dsDNA) and its activation is critically involved in various diseases. STING is synthesized, modified, and resides in the endoplasmic reticulum (ER), and its ER exit is intimately connected with its signaling. The ER, primarily known for its roles in protein folding, lipid synthesis, and calcium storage, has been identified as a pivotal platform for the regulation of a wide range of STING functions. In this review, we discuss the emerging factors that regulate STING in the ER and examine the interplay between STING signaling and ER pathways, highlighting the impacts of such regulations on immune responses and their potential implications in STING-related disorders.
    Keywords:  STING; cell biology; endoplasmic reticulum; innate immunity
    DOI:  https://doi.org/10.1016/j.tcb.2024.02.006
  9. Surg Oncol Clin N Am. 2024 Apr;pii: S1055-3207(23)00117-5. [Epub ahead of print]33(2): 217-230
      Over the past three decades, the landscape of clinically available molecular tests has evolved due to advancements in basic science cancer research and the subsequent utilization of this knowledge to develop DNA, RNA, and protein-based molecular assays for oncology that can be employed for routine clinical use in diagnostics laboratories. Molecular testing of tumors is revealing gaps in previous histopathologic classification systems and opportunities for new, personalized treatment paradigms. Awareness of validated molecular assay options and their general advantages and limitations is crucial for oncology care providers to ensure the optimal test(s) are selected for each patient's circumstances.
    Keywords:  Circulating tumor DNA (ctDNA); Immunohistochemistry (IHC); Liquid biopsy; Molecular diagnostics; Next-generation sequencing (NGS); Precision oncology; Targeted therapy; Tumor biomarkers
    DOI:  https://doi.org/10.1016/j.soc.2023.12.026
  10. Cancer. 2024 Feb 29.
      The DNA mismatch repair (MMR) pathway is critical for correcting DNA mismatches generated during DNA replication. MMR-deficiency (MMR-D) leads to microsatellite instability (MSI) associated with an increased mutation rate, driving cancer development. This is particularly relevant in endometrial cancer (EC) as 25%-30% of tumors are of MMR-D/MSI-high (MSI-H) phenotype. Comprehensive assessment using immunohistochemistry (IHC) and sequencing-based techniques are necessary to fully evaluate ECs given the importance of molecular subtyping in staging and prognosis. This also influences treatment selection as clinical trials have demonstrated survival benefits for immune checkpoint inhibitors (ICIs) alone and in combination with chemotherapy for MMR-D/MSI-H EC patients in various treatment settings. As a portion of MMR-D/MSI-H ECs are driven by Lynch syndrome, an inherited cancer predisposition syndrome that is also associated with colorectal cancer, this molecular subtype also prompts germline assessment that can affect at-risk family members. Additionally, heterogeneity in the tumor immune microenvironment and tumor mutation burden (TMB) have been described by MMR mechanism, meaning MLH1 promoter hypermethylation versus germline/somatic MMR gene mutation, and this may affect response to ICI therapies. Variations by ancestry in prevalence and mechanism of MMR-D/MSI-H tumors have also been reported and may influence health disparities given observed differences in tumors of Black compared to White patients which may affect ICI eligibility. These observations highlight the need for additional prospective studies to evaluate the nuances regarding MMR-D heterogeneity as well as markers of resistance to inform future trials of combination therapies to further improve outcomes for patients with EC.
    Keywords:  Lynch syndrome; MMR-D mechanism; checkpoint inhibitors; endometrial cancer; genetic testing; microsatellite instability; mismatch repair-deficiency
    DOI:  https://doi.org/10.1002/cncr.35267
  11. Case Rep Oncol. 2024 Jan-Dec;17(1):17(1): 317-328
      Introduction: Breast cancer exhibits vast genomic diversity, leading to varied clinical manifestations. Integrating molecular subtyping with in-depth genomic profiling is pivotal for informed treatment choices and prognostic insights. Whole-genome clinical analysis provides a holistic view of genome-wide variations, capturing structural changes and affirming tumor suppressor gene loss of heterozygosity.Case Presentation: Here we detail four unique breast cancer cases from Seoul St. Mary's Hospital, highlighting the actionable benefits and clinical value of whole-genome sequencing (WGS). As an all-in-one test, WGS demonstrates significant clinical utility in these cases, including: (1) detecting homologous recombination deficiency with underlying somatic causal variants (case 1), (2) distinguishing double primary cancer from metastasis (case 2), (3) uncovering microsatellite instability (case 3), and (4) identifying rare germline pathogenic variants in TP53 gene (case 4). Our observations underscore the enhanced clinical relevance of WGS-based testing beyond pinpointing a few driver mutations in conventional targeted panel sequencing platforms.
    Conclusion: With genomic advancements and decreasing sequencing costs, WGS stands out as a transformative tool in oncology, paving the way for personalized treatment plans rooted in individual genetic blueprints.
    Keywords:  Breast cancer; Comprehensive genomic profiling; Whole-genome sequencing
    DOI:  https://doi.org/10.1159/000536087
  12. Cureus. 2024 Jan;16(1): e53088
      This comprehensive review explores the potential of salpingectomy as a groundbreaking strategy for the prevention of ovarian cancer. The discussion encompasses the biological rationale behind salpingectomy, emphasizing its foundation in the tubal hypothesis, which posits the fallopian tubes as a possible origin site for certain ovarian cancers. Ongoing clinical trials and observational studies provide evolving evidence supporting the safety and efficacy of salpingectomy, particularly in high-risk populations. The procedure's ethical considerations, including its impact on fertility and equitable access, are thoroughly examined. Implications for clinical practice underscore the importance of informed decision-making, risk-benefit assessments, and the integration of emerging evidence into reproductive health discussions. Looking ahead, the future landscape of ovarian cancer prevention involves continued research, technological innovations, and collaborative efforts to ensure a holistic and evidence-based approach. The goal is to forge a future where ovarian cancer is not only treatable but also preventable, with salpingectomy potentially playing a pivotal role in this transformative journey.
    Keywords:  clinical trials; ethical considerations; ovarian cancer prevention; reproductive health; salpingectomy; tubal hypothesis
    DOI:  https://doi.org/10.7759/cureus.53088
  13. Elife. 2024 Feb 26. pii: RP89321. [Epub ahead of print]12
      Cell-free DNA (cfDNA) tests use small amounts of DNA in the bloodstream as biomarkers. While it is thought that cfDNA is largely released by dying cells, the proportion of dying cells' DNA that reaches the bloodstream is unknown. Here, we integrate estimates of cellular turnover rates to calculate the expected amount of cfDNA. By comparing this to the actual amount of cell type-specific cfDNA, we estimate the proportion of DNA reaching plasma as cfDNA. We demonstrate that <10% of the DNA from dying cells is detectable in plasma, and the ratios of measured to expected cfDNA levels vary a thousand-fold among cell types, often reaching well below 0.1%. The analysis suggests that local clearance, presumably via phagocytosis, takes up most of the dying cells' DNA. Insights into the underlying mechanism may help to understand the physiological significance of cfDNA and improve the sensitivity of liquid biopsies.
    Keywords:  cellular turnover; cfDNA; clearance mechanisms; computational biology; human; liquid biopsy; systems biology
    DOI:  https://doi.org/10.7554/eLife.89321
  14. Clin Epigenetics. 2024 Feb 27. 16(1): 33
      BACKGROUND: Whole-genome methylation sequencing of cfDNA is not cost-effective for tumor detection. Here, we introduce reduced representative methylome profiling (RRMP), which employs restriction enzyme for depletion of AT-rich sequence to achieve enrichment and deep sequencing of CG-rich sequences.METHODS: We first verified the ability of RRMP to enrich CG-rich sequences using tumor cell genomic DNA and analyzed differential methylation regions between tumor cells and normal whole blood cells. We then analyzed cfDNA from 29 breast cancer patients and 27 non-breast cancer individuals to detect breast cancer by building machine learning models.
    RESULTS: RRMP captured 81.9% CpG islands and 75.2% gene promoters when sequenced to 10 billion base pairs, with an enrichment efficiency being comparable to RRBS. RRMP allowed us to assess DNA methylation changes between tumor cells and whole blood cells. Applying our approach to cfDNA from 29 breast cancer patients and 27 non-breast cancer individuals, we developed machine learning models that could discriminate between breast cancer and non-breast cancer controls (AUC = 0.85), suggesting possibilities for truly non-invasive cancer detection.
    CONCLUSIONS: We developed a new method to achieve reduced representative methylome profiling of cell-free DNA for tumor detection.
    DOI:  https://doi.org/10.1186/s13148-024-01641-x
  15. Genome Med. 2024 Feb 26. 16(1): 36
      Cancer stem cell plasticity refers to the ability of tumour cells to dynamically switch between states-for example, from cancer stem cells to non-cancer stem cell states. Governed by regulatory processes, cells transition through a continuum, with this transition space often referred to as a cell state landscape. Plasticity in cancer cell states leads to divergent biological behaviours, with certain cell states, or state transitions, responsible for tumour progression and therapeutic response. The advent of single-cell assays means these features can now be measured for individual cancer cells and at scale. However, the high dimensionality of this data, complex relationships between genomic features, and a lack of precise knowledge of the genomic profiles defining cancer cell states have opened the door for artificial intelligence methods for depicting cancer cell state landscapes. The contribution of cell state plasticity to cancer phenotypes such as treatment resistance, metastasis, and dormancy has been masked by analysis of 'bulk' genomic data-constituted of the average signal from millions of cells. Single-cell technologies solve this problem by producing a high-dimensional cellular landscape of the tumour ecosystem, quantifying the genomic profiles of individual cells, and creating a more detailed model to investigate cancer plasticity (Genome Res 31:1719, 2021; Semin Cancer Biol 53: 48-58, 2018; Signal Transduct Target Ther 5:1-36, 2020). In conjunction, rapid development in artificial intelligence methods has led to numerous tools that can be employed to study cancer cell plasticity.
    DOI:  https://doi.org/10.1186/s13073-024-01309-4
  16. J Thorac Dis. 2024 Jan 30. 16(1): 423-429
      Background: Carcinoembryonic antigen (CEA) has been routinely used as a postoperative monitoring biomarker for non-small cell lung cancer (NSCLC). Emergingly, circulating tumor DNA (ctDNA)-molecular residual disease (MRD) detection is a well-established prognostic marker, with better positive predictive value (PPV) and negative predictive value (NPV). However, the actual clinical efficiency of CEA in MRD context remain unknown. Hence, we conducted this study for direct comparison of CEA and MRD.Methods: Two cohorts were analyzed in this study. To investigate the prognostic and predictive value of CEA, we retrospective enrolled NSCLC patient stage IA2-IIIA (8th tumor-node-metastasis staging system) with longitudinal CEA between 2018 and 2019. We also performed a paired comparison of CEA and MRD in our previous published cohort. Survival data were analyzed using the Kaplan-Meier method, and comparisons were performed using the log-rank test. Sensitivity, specificity, PPV and NPV were calculated using the R package "epiR". McNemar's test was used to analyze the paired data. Statistical differences were set at a P value <0.05.
    Results: In the retrospective cohort, the sensitivity of longitudinal CEA was only 0.49 [95% confidence interval (CI): 0.37-0.60]. Even for patients with progressively elevated CEA levels, 32% of them still remained disease-free, with PPV of 0.68 (0.49-0.83) and NPV of 0.81 (0.77-0.85). Furthermore, we then compared CEA and MRD values in a previously described MRD cohort. As expected, CEA levels could not stratify the risk of recurrence in detectable versus undetectable MRD populations.
    Conclusions: MRD is superior to CEA in postoperative monitoring. there is insufficient evidence to support its use as postoperative monitoring tumor marker.
    Keywords:  Carcinoembryonic antigen (CEA); molecular residual disease (MRD); non-small cell lung cancer (NSCLC)
    DOI:  https://doi.org/10.21037/jtd-23-507
  17. J Thorac Dis. 2024 Jan 30. 16(1): 671-687
      Background and Objective: Malignant pleural mesothelioma (MPM) is a very aggressive primary tumor of the pleura whose main risk factor is exposure to asbestos. However, only a minority of exposed people develops MPM and the incidence of MPM cases without an apparent association with asbestos exposure has been increasing in recent years, suggesting that genetic predisposing factors may play a crucial role. In addition, several studies reported familial cases of MPM, suggesting that heredity may be an important and underestimated feature in MPM development. Several candidate genes have been associated with a predisposition to MPM and most of them play a role in DNA repair mechanisms: overall, approximately 20% of MPM cases may be related to genetic predisposition. A particular category of patients with high susceptibility to MPM is represented by carriers of pathogenic variants in the BAP1 gene. Germline variants in BAP1 predispose to the development of MPM following an autosomal dominant pattern of inheritance in the familial cases. MPMs in these patients are significantly less aggressive, and patients require a multidisciplinary approach that involves genetic counseling, medical genetics, pathology, surgical, medical, and radiation oncology expertise. In the present narrative review, we presented a comprehensive overview of genetic susceptibility in the development of MPM.Methods: The narrative review is based on a selective literature carried out in PubMed in 2023. Inclusion criteria were original articles in English language, and clinical trials (randomized, prospective, or retrospective).
    Key Content and Findings: We summarized the somatic and germline variants and the differences in terms of clinicopathological features and prognosis between gene-related MPM (GR-MPM) and asbestos-related MPM (AR-MPM). We also discussed the indications for screening, genetic testing, and surveillance of patients with BAP1 germline variants.
    Conclusions: In this narrative review, we have emphasized that the BAP1 gene's harmful germline variations are inherited in an autosomal dominant manner in familial cases. MPMs in individuals with these variations are less severe, and their medical care necessitates a collaborative effort. Additionally, we have outlined the current therapeutic prospects for MPM, including the possibility of gene-specific therapy, which is currently promising but still requires clinical validation.
    Keywords:  BRCA1 associated protein 1 (BAP1); Malignant pleural mesothelioma (MPM); genetic counseling; genetic susceptibility; pleural tumors
    DOI:  https://doi.org/10.21037/jtd-23-611