Department of Surgery, University of Maryland, Baltimore, MD 21201, USA.
Department of Cardiothoracic Surgery, University of Pittsburgh, Pittsburgh, PA 15213, USA.
Sci Transl Med. 2024 Aug 21;16(761):eadl4222. doi: 10.1126/scitranslmed.adl4222.
Respiratory failure occurs more frequently after thoracic surgery than abdominal surgery. Although the etiology for this complication is frequently attributed to underlying lung disease present in patients undergoing thoracic surgery, this notion is often unfounded because many patients with normal preoperative pulmonary function often require prolonged oxygen supplementation even after minimal resection of lung tissue. Using a murine model of pulmonary resection and peripheral blood samples from patients undergoing resection of the lung or abdominal organs, we demonstrated that lung surgery initiates a proinflammatory loop that results in damage to the remaining lung tissue, noncardiogenic pulmonary edema, hypoxia, and even death. Specifically, we demonstrated that resection of murine lung tissue increased concentrations of the homeostatic cytokine interleukin-7, which led to local and systemic activation of type 2 innate lymphoid cells. This process activated lung-resident eosinophils and facilitated stress-induced eosinophil maturation in the bone marrow in a granulocyte-macrophage colony-stimulating factor-dependent manner, resulting in systemic eosinophilia in both mice and humans. Up-regulation of inducible nitric oxide synthase in lung-resident eosinophils led to tissue nitrosylation, pulmonary edema, hypoxia, and, at times, death. Disrupting this activation cascade at any stage ameliorated deleterious outcomes and improved survival after lung resection in the mouse model. Our data suggest that repurposing US Food and Drug Administration-approved eosinophil-targeting strategies may potentially offer a therapeutic intervention to improve outcomes for patients who require lung resection for benign or malignant etiology.
与腹部手术相比,胸部手术后更常发生呼吸衰竭。尽管这种并发症的病因通常归因于接受胸部手术的患者存在基础肺部疾病,但这种观念往往没有依据,因为许多术前肺功能正常的患者即使在进行最小的肺组织切除术后也常常需要长时间的氧补充。通过对肺切除术的小鼠模型以及来自接受肺或腹部器官切除术的患者的外周血样本进行研究,我们证明肺手术会引发促炎循环,从而导致剩余肺组织受损、非心源性肺水肿、缺氧,甚至死亡。具体而言,我们证明了切除小鼠的肺组织会增加稳态细胞因子白细胞介素 7 的浓度,从而导致 2 型固有淋巴细胞在局部和全身被激活。这个过程以粒细胞-巨噬细胞集落刺激因子依赖性的方式激活肺驻留嗜酸性粒细胞,并促进骨髓中的应激诱导的嗜酸性粒细胞成熟,导致在小鼠和人类中出现全身嗜酸性粒细胞增多症。肺驻留嗜酸性粒细胞中诱导型一氧化氮合酶的上调导致组织亚硝基化、肺水肿、缺氧,有时还会导致死亡。在任何阶段阻断这种激活级联反应都可以改善小鼠模型中肺切除术后的不良结果并提高生存率。我们的数据表明,重新利用美国食品和药物管理局批准的靶向嗜酸性粒细胞的策略可能为需要因良性或恶性病因进行肺切除术的患者提供治疗干预,以改善其预后。