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中华肺部疾病杂志(电子版)

中华肺部疾病杂志(电子版) ›› 2026, Vol. 19 ›› Issue (02) : 181 -188. doi: 10.3877/cma.j.issn.1674-6902.2026.02.001

论著

动态免疫特征预测晚期非小细胞肺癌免疫疗法治疗肺孢子菌感染风险的研究
乔伟1, 周前鑫2, 苏悦3, 马源4, 赵沙5,†()   
  1. 1201700　上海，上海大学医学院医大医院呼吸内科
    2200433　上海，同济大学附属上海市肺科医院胸外科
    3200433　上海，同济大学附属上海市肺科医院呼吸与危重症医学科
    4215400　太仓，上海交通大学医学院附属瑞金医院太仓分院呼吸与危重症医学科
    5200433　上海，同济大学附属上海市肺科医院肿瘤科
  • 收稿日期:2025-12-28 出版日期:2026-04-25
  • 通信作者: 赵沙
  • 基金资助:
    国家自然科学基金项目(82002418)

Dynamic immunogenicity analysis of Pneumocystis jirovecii infection prediction in patients with advanced non-small cell lung cancer after immunotherapy

Wei Qiao1, Qianxin Zhou2, Yue Su3, Yuan Ma4, Sha Zhao5,†()   

  1. 1Department of Respiratory Medicine, Shanghai University Medical College Hospital, Shanghai 201700, China
    2Department of Oncology, Shanghai Pulmonary Hospital Affiliated to Tongji University, Shanghai 200433, China
    3Department of cerebral surgery, Shanghai Pulmonary Hospital Affiliated to Tongji University, Shanghai 200433, China
    4Department of Respiratory and Critical Care Medicine, Shanghai Jiao Tong University School of Medicine Affiliated Ruijin Hospital Taicang Branch, Taicang Jiangsu 215400, China
    5Department of Oncology, Shanghai Pulmonary Hospital Affiliated to Tongji University, Shanghai 200433, China
  • Received:2025-12-28 Published:2026-04-25
  • Corresponding author: Sha Zhao
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引用本文：

乔伟, 周前鑫, 苏悦, 马源, 赵沙. 动态免疫特征预测晚期非小细胞肺癌免疫疗法治疗肺孢子菌感染风险的研究[J/OL]. 中华肺部疾病杂志(电子版), 2026, 19(02): 181-188.

Wei Qiao, Qianxin Zhou, Yue Su, Yuan Ma, Sha Zhao. Dynamic immunogenicity analysis of Pneumocystis jirovecii infection prediction in patients with advanced non-small cell lung cancer after immunotherapy[J/OL]. Chinese Journal of Lung Diseases(Electronic Edition), 2026, 19(02): 181-188.

目的

探讨晚期非小细胞肺癌(non-small cell lung cancer, NSCLC)患者接受免疫检查点抑制剂(immune checkpoint inhibitors, ICIs)治疗耶氏肺孢子菌(Pneumocystis jirovecii, PJ)感染风险、危险因素及与淋巴细胞亚群和外周炎性细胞因子的动态变化关系。

方法

回顾性纳入2019年1月至2024年12月我院收治的肺PJ感染接受ICIs治疗晚期NSCLC患者34例为观察组，同期无肺PJ感染患者47例为对照组。采用质谱细胞术(cytometry by time-of-flight, CyTOF)分析外周血单核细胞(peripheral blood mononuclear cells, PBMC)，CD4＋和CD8＋ T细胞亚群及耗竭标志物T细胞免疫球蛋白和黏蛋白结构域-3(T cell immunoglobulin and mucin domain-3, TIM-3＋)、淋巴细胞激活基因3(lymphocyte activation gene 3, LAG-3＋)、程序性死亡受体1(programmed death receptor 1, PD-1＋)表达。采用流式细胞术检测治疗前基线(T0)和治疗一个疗程后(T1)外周血T淋巴细胞亚群，通过酶联免疫吸附法检测血清细胞因子。

结果

与对照组相比，观察组白细胞计数[(6.50±2.10)×109/L比(5.21±1.14)×109/L，t＝3.249，P＝0.002]、中性粒细胞/淋巴细胞比值(neutrophil-to-lymphocyte ratio, NLR)[(5.17±2.58)比(3.53±2.07)，t＝3.210，P＝0.002]高，淋巴细胞计数[(1.28±0.56)×109/L比(1.55±0.67)×109/L，t＝－1.915，P＝0.049]、CD4＋ T细胞计数[(420.54±102.65)×106/L比(552.76±120.23)×106/L，t＝－5.170，P<0.001]及CD4＋/CD8＋ T细胞比值[(1.10±0.18)比(1.38±0.25)，t＝－5.910，P<0.001]低。多变量分析显示免疫联合化疗方案(OR＝1.910，P＝0.011)、PD-L1表达阴性(OR＝2.333，P＝0.033)、NLR(OR＝2.010，P＝0.020)、CD4＋/CD8＋ T细胞比值≤1.0(OR＝2.578，P＝0.036)与肺PJ感染风险相关。CyTOF分析显示，对照组中耗竭性CD8＋ T细胞及总CD8＋ T细胞相对丰度高于观察组(Z-score差异1.5~2.0)，伴CD366(TIM-3)、CD223(LAG-3)、CD279(PD-1)表达升高(log2FC>1.0，P<0.1)。流式细胞术显示，观察组T1时PD-1＋ CD8＋ T细胞计数[(298.50±48.25)/μl比(418.29±67.43)/μl，t＝－2.621，P＝0.013]较T0时增加，对照组T1时LAG-3＋ CD4＋ T细胞计数[(685.50±104.83)/μl比(229.35±34.26)/μl，t＝2.825，P＝0.007]和PD-1＋CD8＋ T细胞计数[(383.21±41.65)/μl比(108.21±37.43)/μl，t＝2.083，P＝0.043]较T0时下降。细胞因子水平显示，T1时血清白细胞介素-2[(45.23±15.01) pg/ml比(135.12±20.21) pg/ml，t＝－2.698，P＝0.045]、肿瘤坏死因子α[(60.56±9.18) pg/ml比(186.25±53.47) pg/ml，t＝－3.240，P＝0.021]和干扰素-γ[(50.56±10.34) pg/ml比(201.23±20.56) pg/ml，t＝－3.274，P＝0.019]水平较T0时呈上升趋势，对照组细胞因子水平变化倍数(T1/T0)高于观察组，白细胞介素-6水平呈下降趋势，变化倍数小。中位随访7.79个月，观察组患者中位生存时间短于对照组(7.23个月比14.12个月，P＝0.047)。

结论

耗竭T细胞数量减少和TNF-α增加可能是ICIs降低肺PJ感染易感性的潜在机制。耗竭T细胞对预测晚期NSCLC患者肺PJ感染风险具有临床意义。

关键词: 非小细胞肺癌, 免疫检查点抑制剂, 耶氏肺孢子菌感染, 淋巴细胞亚群, 质谱细胞术
Objective

To investigate the risk, risk factors, and dynamic changes in lymphocyte subsets and peripheral inflammatory cytokines of Pneumocystis jirovecii(PJ) infection in patients with advanced non-small cell lung cancer (NSCLC) receiving immune checkpoint inhibitors (ICIs) therapy.

Methods

This retrospective study included 34 patients with advanced NSCLC diagnosed with pulmonary PJ infection and treated with ICIs at our hospital between January 2019 and December 2024. Patients without pulmonary PJ infection during the same period served as the control group 47 patients. Peripheral blood mononuclear cells (PBMCs) were analyzed by cytometry by time-of-flight(CyTOF), including CD4+ and CD8+ T cell subsets and the expression of exhaustion markers T cell immunoglobulin and mucin domain-3 (TIM-3+ ), lymphocyte activation gene 3 (LAG-3+ ), and programmed death receptor 1 (PD-1+ ). Flow cytometry was used to detect peripheral blood T lymphocyte subsets at baseline (T0) and after one cycle of treatment (T1) in all subjects, and a series of serum cytokines were detected by enzyme-linked immunosorbent assay (ELISA).

Results

Compared with the control group, the observation group exhibited significantly higher white blood cell counts [(6.50±2.10) × 109/L vs. (5.21±1.14) ×109/L; t=3.249, P=0.002] and neutrophil-to-lymphocyte ratios (NLR) [(5.17±2.58) vs. (3.53±2.07); t=3.210, P=0.002]. Conversely, the observation group showed significantly lower lymphocyte counts [(1.28±0.56) ×109/L vs. (1.55±0.67)×109/L; t=-1.915, P=0.049], CD4+ T-cell counts [(420.54±102.65)×106/L vs. (552.76±120.23)×106/L; t=-5.170, P<0.001], and CD4+ /CD8+ T-cell ratios [(1.10±0.18) vs. (1.38±0.25); t=-5.910, P<0.001]. Multivariate analysis demonstrated that immunotherapy combined with chemotherapy (OR=1.910, P=0.011), negative PD-L1 expression (OR=2.333, P=0.033), NLR(OR=2.010, P=0.020), and a CD4+ /CD8+ T-cell ratio ≤1.0 (OR=2.578, P=0.036) were independent factors associated with an increased risk of pulmonary PJ infection. CyTOF analysis revealed that the relative abundances of exhausted CD8+ T cells and total CD8+ T cells in the control group were significantly higher than those in the observation group (Z-score difference of approximately 1.5~2.0), accompanied by the upregulated expression of CD366 (TIM-3), CD223 (LAG-3), and CD279 (PD-1) (Log2FC>1.0, P<0.1). Flow cytometry analysis demonstrated that PD-1+ CD8+ T-cell counts in the observation group significantly increased at T1 compared with T0 [(298.50±48.25)/μl vs. (418.29±67.43)/μl; t=-2.621, P=0.013]. Conversely, in the control group, significant decreases from T0 to T1 were observed in both LAG-3+ CD4+ T-cell counts [(685.50±104.83)/μl vs. (229.35±34.26)/μl; t=2.825, P=0.007] and PD-1+ CD8+ T-cell counts [(383.21±41.65)/μl vs. (108.21±37.43)/μl; t=2.083, P=0.043]. Analysis of cytokine levels revealed significant upward trends at T1 compared with T0 for serum interleukin-2 (IL-2) [(45.23±15.01) pg/ml vs. (135.12±20.21)pg/ml; t=-2.698, P=0.045], tumor necrosis factor-α(TNF-α) [(60.56±9.18) pg/ml vs. (186.25±53.47) pg/ml; t=-3.240, P=0.021], and interferon-γ(IFN-γ) [(50.56±10.34) pg/ml vs. (201.23±20.56) pg/ml; t=-3.274, P=0.019]. The fold changes (T1/T0) of these cytokines in the control group were significantly higher than those in the observation group. In contrast, interleukin-6 (IL-6) levels exhibited a downward trend, with a significantly smaller fold change observed in the control group compared with the observation group. With a median follow-up of 7.79 months, the median survival time of the observation group was significantly shorter than that of the control group (7.23 months vs. 14.12 months; P=0.047).

Conclusion

Reducing the number of exhausted T cells and increasing TNF-α may be potential mechanisms by which ICIs decreases susceptibility to pulmonary PJ infection. Exhausted T cells have potential predictive value for the risk of pulmonary PJ infection in patients with advanced NSCLC.

Key words: Non-small cell lung cancer, Immune checkpoint inhibitors, Pneumocystis jirovecii infection, Lymphocyte subsets, Mass cytometry
图1 肺孢子菌感染患者CT扫描结果。图A、B为ICIs治疗期间双肺呈弥漫性磨玻璃影，以双肺上叶为主，肺实质可见部分小片状网格状影，支气管和血管影略受影响，部分区域可见"毛刺样"纹理，未见明显大块实变，病灶呈弥漫性分布，符合典型肺孢子菌感染表现，实质破坏较轻；图C、D为ICIs治疗后双肺见广泛磨玻璃影，部分呈小结节或斑片状分布，支气管周围有轻度树枝状纹理增粗，右上肺较左肺受累，影像呈散在分布，间质增厚明显。气管及主支气管未见明显阻塞，肺纹理增粗，活动性感染特征明显
表1 两组NSCLC患者临床资料结果比较
临床资料 观察组(n＝34) 对照组(n＝47) t/χ2值 P值
病理亚型[n(%)]     5.793 0.055
腺癌 22(64.71) 41(87.23)    
鳞状细胞癌 8(23.53) 4(8.51)    
其他 4(11.76) 2(4.26)    
既往放射治疗史[n(%)] 21(61.76) 25(53.19) 0.591 0.442
脑转移[n(%)] 2(5.88) 5(10.64) 0.123 0.725
肝转移[n(%)] 9(26.47) 4(8.51) 4.723 0.030
骨转移[n(%)] 11(32.35) 16(34.04) 0.025 0.874
ECOG体能状态评分[n(%)]     4.426 0.035
0~1分 16(47.06) 33(70.21)    
2分 18(52.94) 14(29.79)    
治疗线数[n(%)]     2.041 0.360
一线治疗 16(47.06) 20(42.55)    
二线治疗 9(26.47) 8(17.02)    
≥三线治疗 9(26.47) 19(40.43)    
治疗方案[n(%)]     4.653 0.031
单药免疫治疗 15(44.12) 32(68.09)    
免疫联合化疗 19(55.88) 15(31.91)    
PD-1/PD-L1抑制剂种类[n(%)]        
帕博利珠单抗 10(29.41) 14(29.79) 0.001 0.971
卡瑞利珠单抗 7(20.59) 8(17.02) 0.166 0.683
替雷利珠单抗 5(14.71) 8(17.02) 0.078 0.779
PD-L1表达[n(%)]     11.135 0.025
阴性 20(58.82) 11(23.40)    
1%~10% 1(2.94) 4(8.51)    
11%~20% 1(2.94) 1(2.13)    
>20% 5(14.71) 15(31.91)    
未知 7(20.59) 16(34.04)    
实验室检查(±s)        
WBC(×109/L) 6.50±2.10 5.21±1.14 3.249 0.002
N(×109/L) 4.07±1.73 4.21±1.85 0.346 0.730
淋巴细胞计数(×109/L) 1.28±0.56 1.55±0.67 1.915 0.049
NLR 5.17±2.58 3.53±2.07 －3.210 0.002
CD4＋ T细胞计数(×106/L) 420.54±102.65 552.76±120.23 5.170 0.000
CD8＋ T细胞计数(×106/L) 381.34±90.02 402.34±113.21 0.880 0.380
CD4＋/CD8＋T细胞比值 1.10±0.18 1.38±0.25 5.910 0.000
表2 晚期NSCLC患者ICIs治疗肺部PJ感染Logistic分析
影响因素 β S.E Z值 P值 OR(95%CI)
吸烟史 0.718 0.382 1.880 0.060 2.050(0.970~4.335)
慢性阻塞性肺疾病 0.602 0.357 1.686 0.092 1.826(0.907~3.676)
支气管扩张 0.504 0.329 1.532 0.126 1.655(0.89~3.155)
肝转移 0.752 0.398 1.889 0.059 2.121(0.972~4.628)
ECOG表现状态2分 0.621 0.349 1.779 0.075 1.861(0.939~3.688)
免疫联合化疗方案 0.647 0.253 2.557 0.011 1.910(1.163~3.136)
PD-L1表达阴性 0.847 0.398 2.128 0.033 2.333(1.069~5.089)
白细胞计数≥10.0×109/L 0.798 0.418 1.909 0.056 2.221(0.979~5.039)
淋巴细胞计数≤0.8×109/L 0.699 0.376 1.859 0.063 2.012(0.963~4.204)
NLR 0.698 0.299 2.334 0.020 2.010(1.118~3.611)
CD4＋/CD8＋比值≤1.0 0.947 0.452 2.095 0.036 2.578(1.063~6.252)
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