Michael Gurevich, Rina Zilkha-Falb, Jia Sherman, Maxime Usdin, Catarina Raposo, Licinio Craveiro, Polina Sonis, David Magalashvili, Shay Menascu, Mark Dolev, Anat Achiron
{"title":"基于机器学习的原发性进行性多发性硬化症疾病进展预测。","authors":"Michael Gurevich, Rina Zilkha-Falb, Jia Sherman, Maxime Usdin, Catarina Raposo, Licinio Craveiro, Polina Sonis, David Magalashvili, Shay Menascu, Mark Dolev, Anat Achiron","doi":"10.1093/braincomms/fcae427","DOIUrl":null,"url":null,"abstract":"<p><p>Primary progressive multiple sclerosis (PPMS) affects 10-15% of multiple sclerosis patients and presents significant variability in the rate of disability progression. Identifying key biological features and patients at higher risk for fast progression is crucial to develop and optimize treatment strategies. Peripheral blood cell transcriptome has the potential to provide valuable information to predict patients' outcomes. In this study, we utilized a machine learning framework applied to the baseline blood transcriptional profiles and brain MRI radiological enumerations to develop prognostic models. These models aim to identify PPMS patients likely to experience significant disease progression and who could benefit from early treatment intervention. RNA-sequence analysis was performed on total RNA extracted from peripheral blood mononuclear cells of PPMS patients in the placebo arm of the ORATORIO clinical trial (NCT01412333), using Illumina NovaSeq S2. Cross-validation algorithms from Partek Genome Suite (www.partek.com) were applied to predict disability progression and brain volume loss over 120 weeks. For disability progression prediction, we analysed blood RNA samples from 135 PPMS patients (61 females and 74 males) with a mean ± standard error age of 44.0 ± 0.7 years, disease duration of 5.9 ± 0.32 years and a median baseline Expanded Disability Status Scale (EDSS) score of 4.3 (range 3.5-6.5). Over the 120-week study, 39.3% (53/135) of patients reached the disability progression end-point, with an average EDSS score increase of 1.3 ± 0.16. For brain volume loss prediction, blood RNA samples from 94 PPMS patients (41 females and 53 males), mean ± standard error age of 43.7 ± 0.7 years and a median baseline EDSS of 4.0 (range 3.0-6.5) were used. Sixty-seven per cent (63/94) experienced significant brain volume loss. For the prediction of disability progression, we developed a two-level procedure. In the first level, a 10-gene predictor achieved a classification accuracy of 70.9 ± 4.5% in identifying patients reaching the disability end-point within 120 weeks. In the second level, a four-gene classifier distinguished between fast and slow disability progression with a 506-day cut-off, achieving 74.1 ± 5.2% accuracy. For brain volume loss prediction, a 12-gene classifier reached an accuracy of 70.2 ± 6.7%, which improved to 74.1 ± 5.2% when combined with baseline brain MRI measurements. In conclusion, our study demonstrates that blood transcriptome data, alone or combined with baseline brain MRI metrics, can effectively predict disability progression and brain volume loss in PPMS patients.</p>","PeriodicalId":93915,"journal":{"name":"Brain communications","volume":"7 1","pages":"fcae427"},"PeriodicalIF":4.1000,"publicationDate":"2025-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11707605/pdf/","citationCount":"0","resultStr":"{\"title\":\"Machine learning-based prediction of disease progression in primary progressive multiple sclerosis.\",\"authors\":\"Michael Gurevich, Rina Zilkha-Falb, Jia Sherman, Maxime Usdin, Catarina Raposo, Licinio Craveiro, Polina Sonis, David Magalashvili, Shay Menascu, Mark Dolev, Anat Achiron\",\"doi\":\"10.1093/braincomms/fcae427\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Primary progressive multiple sclerosis (PPMS) affects 10-15% of multiple sclerosis patients and presents significant variability in the rate of disability progression. Identifying key biological features and patients at higher risk for fast progression is crucial to develop and optimize treatment strategies. Peripheral blood cell transcriptome has the potential to provide valuable information to predict patients' outcomes. In this study, we utilized a machine learning framework applied to the baseline blood transcriptional profiles and brain MRI radiological enumerations to develop prognostic models. These models aim to identify PPMS patients likely to experience significant disease progression and who could benefit from early treatment intervention. RNA-sequence analysis was performed on total RNA extracted from peripheral blood mononuclear cells of PPMS patients in the placebo arm of the ORATORIO clinical trial (NCT01412333), using Illumina NovaSeq S2. Cross-validation algorithms from Partek Genome Suite (www.partek.com) were applied to predict disability progression and brain volume loss over 120 weeks. For disability progression prediction, we analysed blood RNA samples from 135 PPMS patients (61 females and 74 males) with a mean ± standard error age of 44.0 ± 0.7 years, disease duration of 5.9 ± 0.32 years and a median baseline Expanded Disability Status Scale (EDSS) score of 4.3 (range 3.5-6.5). Over the 120-week study, 39.3% (53/135) of patients reached the disability progression end-point, with an average EDSS score increase of 1.3 ± 0.16. For brain volume loss prediction, blood RNA samples from 94 PPMS patients (41 females and 53 males), mean ± standard error age of 43.7 ± 0.7 years and a median baseline EDSS of 4.0 (range 3.0-6.5) were used. Sixty-seven per cent (63/94) experienced significant brain volume loss. For the prediction of disability progression, we developed a two-level procedure. In the first level, a 10-gene predictor achieved a classification accuracy of 70.9 ± 4.5% in identifying patients reaching the disability end-point within 120 weeks. In the second level, a four-gene classifier distinguished between fast and slow disability progression with a 506-day cut-off, achieving 74.1 ± 5.2% accuracy. For brain volume loss prediction, a 12-gene classifier reached an accuracy of 70.2 ± 6.7%, which improved to 74.1 ± 5.2% when combined with baseline brain MRI measurements. In conclusion, our study demonstrates that blood transcriptome data, alone or combined with baseline brain MRI metrics, can effectively predict disability progression and brain volume loss in PPMS patients.</p>\",\"PeriodicalId\":93915,\"journal\":{\"name\":\"Brain communications\",\"volume\":\"7 1\",\"pages\":\"fcae427\"},\"PeriodicalIF\":4.1000,\"publicationDate\":\"2025-01-08\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11707605/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Brain communications\",\"FirstCategoryId\":\"1085\",\"ListUrlMain\":\"https://doi.org/10.1093/braincomms/fcae427\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2025/1/1 0:00:00\",\"PubModel\":\"eCollection\",\"JCR\":\"Q1\",\"JCRName\":\"CLINICAL NEUROLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Brain communications","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/braincomms/fcae427","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/1/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
引用次数: 0
摘要
原发性进行性多发性硬化症(PPMS)影响10-15%的多发性硬化症患者,在残疾进展率方面表现出显著的可变性。确定关键的生物学特征和高风险的快速进展患者对于制定和优化治疗策略至关重要。外周血细胞转录组有可能为预测患者预后提供有价值的信息。在这项研究中,我们利用机器学习框架应用于基线血液转录谱和脑MRI放射计数来开发预后模型。这些模型旨在确定可能经历重大疾病进展的PPMS患者,以及谁可以从早期治疗干预中受益。使用Illumina NovaSeq S2对ORATORIO临床试验(NCT01412333)安慰剂组PPMS患者外周血单个核细胞中提取的总RNA进行RNA序列分析。来自Partek Genome Suite (www.partek.com)的交叉验证算法用于预测120周内的残疾进展和脑容量损失。为了预测残疾进展,我们分析了135名PPMS患者(61名女性和74名男性)的血液RNA样本,平均±标准误差年龄为44.0±0.7岁,疾病持续时间为5.9±0.32年,中位基线扩展残疾状态量表(EDSS)评分为4.3(范围为3.5-6.5)。在120周的研究中,39.3%(53/135)的患者达到残疾进展终点,平均EDSS评分增加1.3±0.16。为了预测脑容量损失,使用94名PPMS患者(41名女性,53名男性)的血液RNA样本,平均±标准误差年龄为43.7±0.7岁,基线EDSS中位数为4.0(范围为3.0-6.5)。67%(63/94)经历了显著的脑容量损失。为了预测残疾进展,我们制定了一个两级程序。在第一级,10个基因预测器在识别120周内达到残疾终点的患者时达到了70.9±4.5%的分类准确率。在第二级,四基因分类器区分快速和缓慢的残疾进展,截断时间为506天,准确率为74.1±5.2%。对于脑容量损失预测,12个基因分类器的准确率为70.2±6.7%,与基线脑MRI测量相结合时提高到74.1±5.2%。总之,我们的研究表明,血液转录组数据,单独或结合基线脑MRI指标,可以有效地预测PPMS患者的残疾进展和脑容量损失。
Machine learning-based prediction of disease progression in primary progressive multiple sclerosis.
Primary progressive multiple sclerosis (PPMS) affects 10-15% of multiple sclerosis patients and presents significant variability in the rate of disability progression. Identifying key biological features and patients at higher risk for fast progression is crucial to develop and optimize treatment strategies. Peripheral blood cell transcriptome has the potential to provide valuable information to predict patients' outcomes. In this study, we utilized a machine learning framework applied to the baseline blood transcriptional profiles and brain MRI radiological enumerations to develop prognostic models. These models aim to identify PPMS patients likely to experience significant disease progression and who could benefit from early treatment intervention. RNA-sequence analysis was performed on total RNA extracted from peripheral blood mononuclear cells of PPMS patients in the placebo arm of the ORATORIO clinical trial (NCT01412333), using Illumina NovaSeq S2. Cross-validation algorithms from Partek Genome Suite (www.partek.com) were applied to predict disability progression and brain volume loss over 120 weeks. For disability progression prediction, we analysed blood RNA samples from 135 PPMS patients (61 females and 74 males) with a mean ± standard error age of 44.0 ± 0.7 years, disease duration of 5.9 ± 0.32 years and a median baseline Expanded Disability Status Scale (EDSS) score of 4.3 (range 3.5-6.5). Over the 120-week study, 39.3% (53/135) of patients reached the disability progression end-point, with an average EDSS score increase of 1.3 ± 0.16. For brain volume loss prediction, blood RNA samples from 94 PPMS patients (41 females and 53 males), mean ± standard error age of 43.7 ± 0.7 years and a median baseline EDSS of 4.0 (range 3.0-6.5) were used. Sixty-seven per cent (63/94) experienced significant brain volume loss. For the prediction of disability progression, we developed a two-level procedure. In the first level, a 10-gene predictor achieved a classification accuracy of 70.9 ± 4.5% in identifying patients reaching the disability end-point within 120 weeks. In the second level, a four-gene classifier distinguished between fast and slow disability progression with a 506-day cut-off, achieving 74.1 ± 5.2% accuracy. For brain volume loss prediction, a 12-gene classifier reached an accuracy of 70.2 ± 6.7%, which improved to 74.1 ± 5.2% when combined with baseline brain MRI measurements. In conclusion, our study demonstrates that blood transcriptome data, alone or combined with baseline brain MRI metrics, can effectively predict disability progression and brain volume loss in PPMS patients.