中国肺癌患者真实世界免疫检查点抑制剂相关性肺炎的流行病学分析

doi:10.19401/j.cnki.1007-3639.2022.06.001

中国癌症杂志 ›› 2022, Vol. 32 ›› Issue (6): 469-477.doi: 10.19401/j.cnki.1007-3639.2022.06.001

中国肺癌患者真实世界免疫检查点抑制剂相关性肺炎的流行病学分析

吴建辉¹()(), 储香玲², 王李强¹^,³, 林心情¹, 谢晓鸿¹, 谢梦青², 赵静², 邓海怡¹, 杨伊霖¹, 邱桂焕¹, 周茂林¹, 孙霓¹, 李茹¹^,⁴, 陈萤¹, 邓佳茜¹, 曾晨¹, 潘柏林⁵, 秦茵茵¹, 刘明¹, 苏春霞²()(), 周承志¹()()

1.呼吸疾病国家重点实验室,国家呼吸系统疾病临床研究中心,广州医科大学附属第一医院,广州呼吸健康研究院,肿瘤内科一区,广东广州 510120
2.同济大学附属上海市肺科医院肿瘤科,上海 200433
3.河南大学生命科学学院,河南开封 475001
4.河南大学临床医学院,河南开封 475001
5.广州医科大学第一临床学院,广东广州 510182

收稿日期:2022-04-20 修回日期:2022-05-20 出版日期:2022-06-30 发布日期:2022-07-21
通信作者: 苏春霞,周承志 E-mail:496346580@qq.com;susu_mail@126.com;doctorzcz@163.com
作者简介:吴建辉（ORCID: 0000-0002-0216-9796）,硕士研究生在读。E-mail: 496346580@qq.com
周承志,医学博士,主任医师,教授,博士研究生导师。现任广州医科大学附属第一医院广州呼吸健康研究院,国家呼吸医学中心临床诊疗部部长,呼吸与危重症学科副主任,呼吸五区（肿瘤一区）主任,肿瘤中心主任助理。现兼任中华医学会呼吸分会肺癌学组副组长、中国医师协会呼吸分会肺癌工作组委员、中国呼吸肿瘤协作组秘书长兼青年委员会副主任委员、中国临床肿瘤学会青年专家委员会委员及患者教育专家委员会委员、广东省胸部肿瘤疾病学会肿瘤危重症专委会主任委员、广东省精准医学应用学会肺癌分会主任委员、广东省医学会呼吸病学分会肺癌学组副组长、广东省医学会肺部肿瘤学分会副主任委员、广东省医师协会肿瘤内科分会副主任委员、广东省临床医学会肺癌分会及真实世界研究分会副主任委员。在国际上率先提出“重症肺癌”的概念,并牵头发表第一版“重症肺癌国际共识”。提出了“癌肺同治”、“ PS评分具有可逆性和波动性”、“抗肿瘤药物升降级”等肺癌全程管理理念。

Epidemiological analysis of real-world immune checkpoint inhibitor-related pneumonitis in Chinese patients with lung cancer

WU Jianhui¹()(), CHU Xiangling², WANG Liqiang¹^,³, LIN Xinqing¹, XIE Xiaohong¹, XIE Mengqing², ZHAO Jing², DENG Haiyi¹, YANG Yilin¹, QIU Guihuan¹, ZHOU Maolin¹, SUN Ni¹, LI Ru¹^,⁴, CHEN Ying¹, DENG Jiaxi¹, ZENG Chen¹, PAN Bolin⁵, QIN Yinyin¹, LIU Ming¹, SU Chunxia²()(), ZHOU Chengzhi¹()()

1. State Key Laboratory of Respiratory Disease, National Clinical Research Centre for Respiratory Disease, Guangzhou Institute of Respiratory Health, First Affiliated Hospital, Guangzhou Medical University, Guangzhou 510120, Guangdong Province, China
2. Department of Medical Oncology, Shanghai Pulmonary Hospital, School of Medicine, Tongji University, Shanghai 200433, China
3. School of Life Sciences, Henan University, Kaifeng 475001, Henan Province, China
4. School of Clinical Medicine, Henan University, Kaifeng 475001, Henan Province, China
5. The First Clinical College of Guangzhou Medical University, Guangzhou 510182, Guangdong Province, China

Received:2022-04-20 Revised:2022-05-20 Published:2022-06-30 Online:2022-07-21
Contact: SU Chunxia, ZHOU Chengzhi E-mail:496346580@qq.com;susu_mail@126.com;doctorzcz@163.com

摘要/Abstract

摘要：

背景和目的：临床研究中免疫检查点抑制剂相关性肺炎（checkpoint inhibitor-related pneumonitis,CIP）在程序性死亡[蛋白]-1（programmed cell death-1,PD-1）和程序性死亡[蛋白]配体-1（programmed cell death-ligand-1,PD-L1）抑制剂引起的免疫相关不良反应（immune-related adverse event,irAE）致死原因中排第一位,而真实世界CIP的流行病学情况缺乏大宗人群研究报道。本研究旨在了解中国真实世界中肺癌免疫治疗的CIP发病率,并进一步总结其特征、治疗现状和转归。方法：回顾并收集2019年1月—2021年9月在广州医科大学附属第一医院和同济大学附属上海市肺科医院首诊肺癌且接受了免疫检查点抑制剂（immune checkpointinhibitor,ICI）治疗的患者基本临床信息,以及CIP患者肺炎的发生时间、等级、治疗方案和转归。总结CIP在研究队列以及各亚组CIP的发病率、发病特点、危险因素以及CIP患者接受免疫抑制治疗的临床现状以及转归。结果：共纳入 2 031 例免疫治疗患者,CIP发生率为7.2%（147/2 031）,重症率为2.6%（52/2 031）,致死率为0.4% （9/2 031）。其中CIP人群中重症率为35.4%（52/147）,死亡率为6.1%（9/147）。与非CIP患者相比,CIP多见于男性、老年（>65岁)、联合治疗、晚期二线免疫治疗的患者。在各亚组CIP发病率的对比中,男性、老年（>65岁)、鳞癌、联合治疗、抗PD-1单抗组、晚期一线及二线治疗的患者发病率更高。真实世界CIP的中位发病时间为免疫治疗后148 d,具有双高峰的特点,即免疫治疗后60~90 d及150~210 d是发病的双高峰时间段。CIP发病还具有一定的季节性,秋冬季高发。治疗的患者均使用了糖皮质激素作为一线治疗;本研究中CIP的免疫抑制治疗率为76.2%,治疗后97.9%轻症CIP患者能预后良好,81.2%重症患者能在治疗后有较好的预后,有17.3%重症患者因CIP死亡。结论：真实世界肺癌患者免疫治疗时总人群CIP发生率为7.2%,重症率为2.6%,致死率为0.4%;其中CIP人群重症率为35.4%,死亡率为6.1%。CIP中位发病时间有双高峰特点,且秋冬季高发;男性、老年、鳞癌、联合治疗、抗PD-1单抗组、晚期一线及二线治疗的患者CIP发病率较高。大部分CIP患者经过免疫抑制治疗后转归良好。

关键词: 肺癌, 免疫检查点抑制剂相关性肺炎, 免疫相关不良反应, 免疫检查点抑制剂, 流行病学, 真实世界研究

Abstract:

Background and purpose: In clinical studies, checkpoint inhibitor-related pneumonitis (CIP) ranks first among the causes of death in programmed cell death protein-1 (PD-1)/programmed death ligand-1 (PD-L1) inhibitor immune-related adverse events. Real-world CIP situations lack extensive population reports. This study aimed to understand the incidence of CIP in the real world of lung cancer in China, and to summarize its characteristics, treatment status and outcomes. Methods: This study retrospectively collected the essential clinical information of patients with an initral diagnosis of lung cancer who received treatment with immune checkpoint inhibitors (ICIs) at the First Affiliated Hospital of Guangzhou Medical University and Shanghai Pulmonary Hospital between January 2019 and September 2021. For patients with CIP, we also collected the time of its onset, grade, treatment regimen and outcome. The analyses of incidence, patient’s characteristics and the risk factors of CIP in overall and subgroup were carried out. Moreover, we analyzed the outcomes of patients treated with immunosuppressive therapy. Results: A total of 2 031 patients with immunotherapy were enrolled, with a CIP incidence rate of 7.2% (147/2 031), a severe CIP rate of 2.6% (52/2 031) and a mortality rate of 0.4% (9/2 031). The rate of severe grade in the population with CIP was 35.4%, and the mortality rate was 6.1% (9/147). Compared with non-CIP patients, more CIP patients were male, older (>65 years), with combination therapy, and on first- and second-line immunotherapy in advanced treatment. In subgroup analyses, the incidence of CIP was higher in men, the elderly (>65 years), squamous cancer, combination therapy, anti-PD-1 inhibitors, and first- and second-line therapy in advanced treatment. The median onset time of CIP in the real world was 148 days, with a double-peak characteristic, that was, 60-90 days and 150-210 days after immunotherapy were both the peak time periods for CIP onset. The incidence of CIP was also influenced by seasonality, with a high incidence in autumn and winter. All treated patients used corticosteroids as first-line treatment; the immunosuppressive treatment rate of CIP in this study was 76.2%. After treatment, 97.9% of mild CIP patients and 81.2% of severe CIP patients had a good prognosis, and 17.3% of severe CIP patients died due to CIP. Conclusion: In the real world, the incidence of CIP for lung cancer patients was 7.2%, incidence of severe CIP was 2.6%, and mortality rate was 0.4%; the incidence of severe disease in the population with CIP was 35.4%, and mortality rate was 6.1%. The median onset time of CIP was characterized by a double peak, and incidence of CIP was higher in autumn and winter. Men, the elderly, squamous cancer patients, patients on combination therapy, patients who used anti-PD-1 inhibitors, and patients with advanced treatment had higher incidence of CIP. Most patients with CIP had good outcomes after immunosuppressive therapy.

Key words: Lung cancer, Checkpoint inhibitor-related pneumonitis, Immune-related adverse event, Immune checkpoint inhibitor, Epidemiology, Real-world research

中图分类号:

R734.2

吴建辉, 储香玲, 王李强, 林心情, 谢晓鸿, 谢梦青, 赵静, 邓海怡, 杨伊霖, 邱桂焕, 周茂林, 孙霓, 李茹, 陈萤, 邓佳茜, 曾晨, 潘柏林, 秦茵茵, 刘明, 苏春霞, 周承志. 中国肺癌患者真实世界免疫检查点抑制剂相关性肺炎的流行病学分析[J]. 中国癌症杂志, 2022, 32(6): 469-477.

WU Jianhui, CHU Xiangling, WANG Liqiang, LIN Xinqing, XIE Xiaohong, XIE Mengqing, ZHAO Jing, DENG Haiyi, YANG Yilin, QIU Guihuan, ZHOU Maolin, SUN Ni, LI Ru, CHEN Ying, DENG Jiaxi, ZENG Chen, PAN Bolin, QIN Yinyin, LIU Ming, SU Chunxia, ZHOU Chengzhi. Epidemiological analysis of real-world immune checkpoint inhibitor-related pneumonitis in Chinese patients with lung cancer[J]. China Oncology, 2022, 32(6): 469-477.

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Characteristics	All n (%)	Non-CIP n (%)	CIP n (%)	CIP incidence/%	χ²	P value
All	2 031	1 884	147	7.2	-	-
Gender					5.498	0.019
Male	1 632 (80.4)	1 503 (79.8)	129 (87.8)	7.9
Female	399 (19.6)	381 (20.2)	18 (12.2)	4.5
Age/year					13.778	0.000
≤ 65	1 206 (59.4)	1 140 (60.5)	66 (44.9)	5.5
>65	825 (40.6)	744 (39.5)	81 (55.1)	9.8
Subtype					5.869	0.118
SQC	727 (35.8)	662 (35.1)	65 (44.2)	8.9
ADC	904 (44.5)	844 (44.8)	60 (40.8)	6.6
Other NSCLC	195 (9.6)	186 (9.9)	9 (6.1)	4.6
SCLC	205 (10.1)	192 (10.2)	13 (8.8)	6.3
Year of immunotherapy					0.913	0.633
2019	558 (27.5)	513 (27.2)	45 (30.6)	8.1
2020	899 (44.3)	835 (44.3)	64 (43.5)	7.1
2021	574 (28.3)	536 (28.5)	38 (25.9)	6.6
Immunotherapy					6.997	0.008
Monotherapy	389 (19.2)	373 (19.8)	16 (10.9)	4.1
Combination	1 642 (80.8)	1 511 (80.2)	131 (89.1)	8.0
Types of ICIs					0.132	0.716
Anti-PD-1	1 921 (94.6)	1 781 (94.5)	140 (95.2)	7.3
Anti-PD-L1	110 (5.4)	103 (5.5)	7 (4.8)	6.4
Treatment line					10.955	0.012
Neoadjuvant	105 (5.3)	103 (5.5)	2 (1.4)	1.9
Adjuvant	211 (10.2)	204 (10.8)	7 (4.8)	3.3
First-line	1 173 (57.8)	1 079 (57.3)	94 (63.9)	8.0
Second-line and above	542 (26.7)	498 (26.4)	44 (29.9)	8.1

Characteristics	CIP n (%)	Mild (grade 1-2) n (%)	Severe (grade 3-4) n (%)	Severe rate/%	χ²	Pvalue
All	147	95	52	35.4	-	-
Gender					1.552	0.213
Male	129 (87.8)	81 (85.3)	48 (92.3)	37.2
Female	18 (12.2)	14 (14.7)	4 (7.7)	22.2
Age/year					0.014	0.904
≤65	66 (44.9)	43 (45.3)	23 (44.2)	34.8
>65	81 (55.1)	52 (54.7)	29 (55.8)	35.8
Subtype					1.430	0.699
SQC	65 (44.2)	43 (45.3)	22 (42.3)	33.8
ADC	60 (40.8)	36 (37.9)	24 (46.2)	40.0
Other NSCLC	9 (6.1)	7 (7.4)	2 (3.8)	22.2
SCLC	13 (8.9)	9 (9.5)	4 (7.7)	30.8
Immunotherapy					1.680	0.195
Monotherapy	16 (10.9)	8 (8.4)	8 (15.4)	50.0
Combination	131 (89.1)	87 (91.6)	44 (84.6)	33.6
Types of ICIs					0.175	0.675
Anti-PD-1	140 (95.2)	91 (95.8)	49 (94.2)	35.0
Anti-PD-L1	7 (4.8)	4 (4.2)	3 (5.8)	42.9
Treatment line		0 (0.0)			5.053	0.168
Neoadjuvant	2 (1.4)	1 (1.1)	1 (1.9)	50.0
Adjuvant	7 (4.8)	5 (5.3)	2 (3.8)	28.6
First-line	94 (63.9)	55 (57.9)	39 (75.0)	41.5
Second-line and above	44 (29.9)	34 (35.8)	10 (19.2)	22.7

Characteristics	CIP n (%)	Mild (grade 1-2) n (%)	Severe (grade 3-5) n (%)	χ²	P value
Time from treatment to onset (IQR)/d	148 (63-242)	134 (61-242)	156 (92-257)	-	0.225
Immunosuppressive therapy				48.839	0.000
Corticosteroids	90 (61.2)	58 (61.1)	32 (61.5)
Corticosteroids plus immunosuppressant	22 (15.0)	2 (2.1)	20 (38.5)
None	35 (23.8)	35 (36.8)	0 (0.0)
Corticosteroid dose				46.244	0.000
Small dose	2 (1.4)	2 (2.1)	0 (0.0)
Medium dose	16 (10.9)	11 (11.6)	5 (9.6)
High dose	83 (56.5)	45 (47.4)	38 (73.1)
Over dose	11 (7.5)	2 (2.1)	9 (17.3)
None	35 (23.8)	35 (36.8)	0 (0.0)
Treatment outcome				30.626	0.000
Completely resolved	20 (13.6)	19 (20.0)	1 (1.9)
Improve	80 (54.4)	55 (57.9)	25 (48.1)
Stable	30 (20.4)	19 (20.0)	11 (21.2)
Worsened	8 (5.4)	2 (2.1)	6 (11.5)
Dead	9 (6.1)	0 (0.0)	9 (17.3)

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中国肺癌患者真实世界免疫检查点抑制剂相关性肺炎的流行病学分析

Epidemiological analysis of real-world immune checkpoint inhibitor-related pneumonitis in Chinese patients with lung cancer

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