Analysis of the factors affecting small airway dysfunction and evaluation of cardiopulmonary function in the patients with chronic duration of asthma_Chinese Journal of Respiratory and Critical Care Medicine

Authors：

HUANG Nanxin ¹ , LIU Lijun ¹ , ZHAO Shaoqian ¹ ,  LIU Lanying ^1,2 ,  WANG Hesheng ¹

1. Department of Acupuncture and Rehabilitation, The Affiliated Hospital of Nanjing University of Chinese Medicine, Jiangsu Provincial Hospital of Traditional Chinese Medicine, Nanjing, Jiangsu 210029, P. R. China;
2. Nanjing University of Chinese Medicine Combined with Key Laboratory of Ministry of Education, Nanjing, JIangsu 210023, P. R. China;

Corresponding author：

LIU Lanying, Email: bluelany@163.com; WANG Hesheng, Email: wanghesheng2010@126.com

Keywords：

Asthma; small airway dysfunction; influencing factors; cardiopulmonary exercise test; cardiopulmonary function

DOI：

10.7507/1671-6205.202410033

Video：

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Objective To observe the clinical characteristics of asthma patients with chronic duration stage combined with small airway dysfunction (SAD), and analyze the influencing factors of SAD and the cardiopulmonary function of such patients under exercise. Methods The patients with chronic duration of asthma admitted to Nanjing Affiliated Hospital of Traditional Chinese Medicine from July 2022 to April 2024 were divided into a SAD group and a non-SAD group according to the lung function results. Clinical data and relevant data of cardiopulmonary exercise test (CPET) were collected, the clinical data and cardiopulmonary function between the two groups were compared. The influencing factors of SAD were explored by multivariate logistic regression analysis. Results A total of 102 patients with chronic asthma duration, 59 (57.8%) in the SAD group and 43 (42.2%) in the non-SAD group were included. In the SAD group, age, body masss index, asthma duration were greater than those in the non-SAD group, and SAD score was lower than that in the non-SAD group; the proportion of patients with acute onset of asthma, history of smoking, allergic rhinitis, and asthma control test score were higher than those in the non-SAD group, the exhaled nitric oxide level of SAD group was higher than that in the non-SAD group, and the conventional lung function level was lower than that in the non-SAD group (P<0.05). CPET showed that the VE/VCO₂ slope and CO₂ equivalent in the SAD group were higher than those in the non-SAD group, and the peak kg oxygen uptake, peak heart rate, and respiratory reserve were lower than those in the non-SAD group, showing a statistically significant difference (P<0.05). Multivariate logistic analysis showed that age, increase of carbon dioxide equivalent at peak exercise, acute onset of asthma and allergic rhinitis were independent risk factors for SAD, and the increase of peak expiratory flow rate was the protective factor (P<0.05). Conclusions SAD in chronic persistent asthma is affected by various factors such as age, acute asthma attacks and history of allergic rhinitis. CPET indicates that patients with asthma who also have SAD have their cardiopulmonary function and aerobic capacity impaired to some extent.

1.	Thomas D, McDonald VM, Pavord ID, et al. Asthma remission: what is it and how can it be achieved? Eur Respir J, 2022, 60(5): 2102583.
2.	Lipworth B, Manoharan A, Anderson W. Unlocking the quiet zone: the small airway asthma phenotype. Lancet Respir Med, 2014, 2(6): 497-506.
3.	孙天生, 宋慧慧, 唐昊. 小气道功能在支气管哮喘中的研究进展. 临床肺科杂志, 2024, 29(5): 754-758.
4.	Abdo M, Trinkmann F, Kirsten AM, et al. Small airway dysfunction links asthma severity with physical activity and symptom control. J Allergy Clin Immunol Pract, 2021, 9(9): 3359-3368. e1.
5.	Katsoulis KK, Kostikas K, Kontakiotis T. Techniques for assessing small airways function: possible applications in asthma and COPD. Respir Med, 2016, 119: e2-e9.
6.	中国呼吸医师协会肺功能与临床呼吸生理工作委员会, 中华医学会呼吸病学分会呼吸治疗学组. 肺功能检查报告规范——肺量计检查、支气管舒张试验、支气管激发试验. 中华医学杂志, 2019, 99(22): 1681-1691.
7.	中华医学会心血管病学分会, 中国康复医学会心肺预防与康复专业委员会, 中华心血管病杂志编辑委员会, 等. 心肺运动试验临床规范应用中国专家共识. 中华心血管病杂志, 2022, 50(10): 973-986.
8.	张也, 孙兴国, 郝璐, 等. Max试验验证个体化症状限制性心肺运动试验为最大极限运动临床研究. 中国全科医学, 2019, 22(20): 2441-2447+2454.
9.	Stickland MK, Neder JA, Guenette JA, et al. Using cardiopulmonary exercise testing to understand dyspnea and exercise intolerance in respiratory disease. Chest, 2022, 161(6): 1505-1516.
10.	刘丽君, 黄楠馨, 罗家麒, 等. 未良好控制哮喘慢性持续期患者运动通气功能评价. 中国呼吸与危重监护杂志, 2024, 23(5): 305-311.
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12.	Juniper EF, Guyatt GH, Epstein RS, et al. Evaluation of impairment of health related quality of life in asthma: development of a questionnaire for use in clinical trials. Torax, 1992, 47(2): 76-83.
13.	Zhang YF, Zhang HH, Su X, et al. Analysis of influencing factors and a predictive model of small airway dysfunction in adults. BMC Pulm Med, 2023, 23(1): 141.
14.	任梦怡, 李瑾, 张明, 等. 心肺运动试验在食管癌患者术后并发症预测中的应用. 中国胸心血管外科临床杂志, 2024, 31(8): 1148-1155.
15.	Xiao D, Chen Z, Wu S, et al. Prevalence and risk factors of small airway dysfunction, and association with smoking, in China: findings from a national cross-sectional study. Lancet Respir Med, 2020, 8(11): 1081-1093.
16.	宋骏, 徐汉文, 杨慧珍. 哮喘患者小气道功能障碍的影响因素及预测模型分析. 中国现代医生, 2023, 61(14): 58-62.
17.	Dixon AE, Poynter ME, Garrow OJ, et al. Peripheral airway dysfunction in obesity and obese asthma. Chest, 2023, 163(4): 753-762.
18.	冯欣然, 王雪峰. 中医药治疗儿童支气管哮喘的概述. 辽宁中医杂志, 2025, 52(2): 204-207.
19.	Papi A, Brightling C, Pedersen SE, et al. Asthma. Lancet, 2018, 391(10122): 783-800.
20.	Singh D, Long G, Cançado JED, et al. Small airway disease in chronic obstructive pulmonary disease: insights and implications for the clinician. Curr Opin Pulm Med, 2020, 26(2): 162-168.
21.	Galiniak S, Rachel M. Comparison of fractional exhaled nitric oxide in asthmatics with and without allergic rhinitis. Biomarkers, 2021, 26(2): 174-183.
22.	申倩, 祝楠波, 余灿清, 等. 中国成年人吸烟与心血管疾病发病风险的关联及其性别差异分析. 中华流行病学杂志, 2018, 39(1): 8-15.
23.	中华医学会儿科学分会呼吸学组肺功能协作组《中华实用儿科临床杂志》编辑委员会. 儿童肺功能系列指南(二): 肺容积和通气功能. 中华实用儿科临床杂志, 2016, 31(10): 744-750.
24.	中华医学会呼吸病学分会肺功能专业组. 肺功能检查指南(第二部分)——肺量计检查. 中华结核和呼吸杂志, 2014, 37(7): 481-486.
25.	陈丽洁, 樊军, 刘德松, 等. 肺功能检测在儿童哮喘长期管理中的应用探讨. 中国妇幼保健, 2013, 28(32): 5314-5315.
26.	Dweik RA, Boggs PB, Erzurum SC, et al. An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications. Am J Respir Crit Care Med, 2011, 184(5): 602-615.
27.	李东旭, 柳丽, 景晓, 等. 支气管哮喘患者血清miR-181a、S1PR1 mRNA表达水平与急性发作期发生的相关性. 国际检验医学杂志, 2024, 45(14): 1687-1691,1698.
28.	陈文丽, 韩梅, 于超伟, 等. 肺泡一氧化氮测定在哮喘患者中的临床意义. 重庆医学, 2021, 50(14): 2442-2445.
29.	吴常伟, 刘锦铭, 杨文兰, 等. 摄氧效率与慢性阻塞性肺疾病稳定期患者运动耐力的相关性. 中华结核和呼吸杂志, 2013, 36(9): 661-666.
30.	Torchio R, Mazzucco A, Guglielmo M, et al. Minute ventilation to carbon dioxide output (V'E/V'CO₂ slope) is the strongest death predictor before larger lung resections. Monaldi Arch Chest Dis, 2017, 87(3): 817.
31.	李文婷, 袁平, 吴常伟, 等. 右心房压力联合二氧化碳通气当量斜率预测慢性血栓栓塞性肺动脉高压患者预后的价值研究. 中国循环杂志, 2020, 35(7): 670-676.
32.	贺晓玉, 李稚, 邓京捷. Verification phase作为判定最大摄氧量新方法的研究进展. 中国运动医学杂志, 2019, 38(12): 1087-1093.
33.	朱子聪, 金凌, 王子璇, 等. 皮肌炎患者肌力评估及康复治疗研究现状. 中国皮肤性病学杂志, 2022, 36(12): 1350-1355.
34.	Cocchiarella L, Anderson G. American Medical Association: guides to the evaluation of permanent impairment. 5th ed. Chicago: American Medical Association, 2000. 107.
35.	Guazzi M, Arena R, Halle M, et al. 2016 focused update: clinical recommendations for cardiopulmonary exercise testing data assessment in specific patient populations. Circulation, 2016, 133(24): e694-e711.
36.	陈瑜, 曹芳. 居家腹膜透析患者体力活动水平现状及护理对策. 中国卫生标准管理, 2024, 15(3): 164-168.
37.	黄君, 罗健. 哮喘及疑诊哮喘患儿运动激发试验中肺功能及目标心率到达与维持时间分析. 中国临床新医学, 2021, 14(5): 492-496.
38.	蒋琦, 常益益, 李洋. 心肺运动试验在老年慢性阻塞性肺疾病中应用. 中国老年学杂志, 2023, 43(20): 4949-4952.
39.	郝永发, 陈琛, 马晓虎, 等. 心肺运动试验对慢性阻塞性肺疾病患者气流受限严重程度的预测价值. 宁夏医学杂志, 2023, 45(11): 988-991,960.
40.	Cottini M, Lombardi C, Berti A, et al. Small-airway dysfunction in paediatric asthma. Curr Opin Allergy Clin Immunol, 2021, 21(2): 128-134.
41.	Pigakis KM, Stavrou VT, Kontopodi AK, et al. Impact of isolated exercise-induced small airway dysfunction on exercise performance in professional male cyclists. Sports (Basel), 2024, 12(4): 112.

1. Thomas D, McDonald VM, Pavord ID, et al. Asthma remission: what is it and how can it be achieved? Eur Respir J, 2022, 60(5): 2102583.
2. Lipworth B, Manoharan A, Anderson W. Unlocking the quiet zone: the small airway asthma phenotype. Lancet Respir Med, 2014, 2(6): 497-506.
3. 孙天生, 宋慧慧, 唐昊. 小气道功能在支气管哮喘中的研究进展. 临床肺科杂志, 2024, 29(5): 754-758.
4. Abdo M, Trinkmann F, Kirsten AM, et al. Small airway dysfunction links asthma severity with physical activity and symptom control. J Allergy Clin Immunol Pract, 2021, 9(9): 3359-3368. e1.
5. Katsoulis KK, Kostikas K, Kontakiotis T. Techniques for assessing small airways function: possible applications in asthma and COPD. Respir Med, 2016, 119: e2-e9.
6. 中国呼吸医师协会肺功能与临床呼吸生理工作委员会, 中华医学会呼吸病学分会呼吸治疗学组. 肺功能检查报告规范——肺量计检查、支气管舒张试验、支气管激发试验. 中华医学杂志, 2019, 99(22): 1681-1691.
7. 中华医学会心血管病学分会, 中国康复医学会心肺预防与康复专业委员会, 中华心血管病杂志编辑委员会, 等. 心肺运动试验临床规范应用中国专家共识. 中华心血管病杂志, 2022, 50(10): 973-986.
8. 张也, 孙兴国, 郝璐, 等. Max试验验证个体化症状限制性心肺运动试验为最大极限运动临床研究. 中国全科医学, 2019, 22(20): 2441-2447+2454.
9. Stickland MK, Neder JA, Guenette JA, et al. Using cardiopulmonary exercise testing to understand dyspnea and exercise intolerance in respiratory disease. Chest, 2022, 161(6): 1505-1516.
10. 刘丽君, 黄楠馨, 罗家麒, 等. 未良好控制哮喘慢性持续期患者运动通气功能评价. 中国呼吸与危重监护杂志, 2024, 23(5): 305-311.
11. 中华医学会呼吸病学分会哮喘学组. 支气管哮喘防治指南(2020年版). 中华结核和呼吸杂志, 2020, 43(12): 1023-1048.
12. Juniper EF, Guyatt GH, Epstein RS, et al. Evaluation of impairment of health related quality of life in asthma: development of a questionnaire for use in clinical trials. Torax, 1992, 47(2): 76-83.
13. Zhang YF, Zhang HH, Su X, et al. Analysis of influencing factors and a predictive model of small airway dysfunction in adults. BMC Pulm Med, 2023, 23(1): 141.
14. 任梦怡, 李瑾, 张明, 等. 心肺运动试验在食管癌患者术后并发症预测中的应用. 中国胸心血管外科临床杂志, 2024, 31(8): 1148-1155.
15. Xiao D, Chen Z, Wu S, et al. Prevalence and risk factors of small airway dysfunction, and association with smoking, in China: findings from a national cross-sectional study. Lancet Respir Med, 2020, 8(11): 1081-1093.
16. 宋骏, 徐汉文, 杨慧珍. 哮喘患者小气道功能障碍的影响因素及预测模型分析. 中国现代医生, 2023, 61(14): 58-62.
17. Dixon AE, Poynter ME, Garrow OJ, et al. Peripheral airway dysfunction in obesity and obese asthma. Chest, 2023, 163(4): 753-762.
18. 冯欣然, 王雪峰. 中医药治疗儿童支气管哮喘的概述. 辽宁中医杂志, 2025, 52(2): 204-207.
19. Papi A, Brightling C, Pedersen SE, et al. Asthma. Lancet, 2018, 391(10122): 783-800.
20. Singh D, Long G, Cançado JED, et al. Small airway disease in chronic obstructive pulmonary disease: insights and implications for the clinician. Curr Opin Pulm Med, 2020, 26(2): 162-168.
21. Galiniak S, Rachel M. Comparison of fractional exhaled nitric oxide in asthmatics with and without allergic rhinitis. Biomarkers, 2021, 26(2): 174-183.
22. 申倩, 祝楠波, 余灿清, 等. 中国成年人吸烟与心血管疾病发病风险的关联及其性别差异分析. 中华流行病学杂志, 2018, 39(1): 8-15.
23. 中华医学会儿科学分会呼吸学组肺功能协作组《中华实用儿科临床杂志》编辑委员会. 儿童肺功能系列指南(二): 肺容积和通气功能. 中华实用儿科临床杂志, 2016, 31(10): 744-750.
24. 中华医学会呼吸病学分会肺功能专业组. 肺功能检查指南(第二部分)——肺量计检查. 中华结核和呼吸杂志, 2014, 37(7): 481-486.
25. 陈丽洁, 樊军, 刘德松, 等. 肺功能检测在儿童哮喘长期管理中的应用探讨. 中国妇幼保健, 2013, 28(32): 5314-5315.
26. Dweik RA, Boggs PB, Erzurum SC, et al. An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications. Am J Respir Crit Care Med, 2011, 184(5): 602-615.
27. 李东旭, 柳丽, 景晓, 等. 支气管哮喘患者血清miR-181a、S1PR1 mRNA表达水平与急性发作期发生的相关性. 国际检验医学杂志, 2024, 45(14): 1687-1691,1698.
28. 陈文丽, 韩梅, 于超伟, 等. 肺泡一氧化氮测定在哮喘患者中的临床意义. 重庆医学, 2021, 50(14): 2442-2445.
29. 吴常伟, 刘锦铭, 杨文兰, 等. 摄氧效率与慢性阻塞性肺疾病稳定期患者运动耐力的相关性. 中华结核和呼吸杂志, 2013, 36(9): 661-666.
30. Torchio R, Mazzucco A, Guglielmo M, et al. Minute ventilation to carbon dioxide output (V'E/V'CO₂ slope) is the strongest death predictor before larger lung resections. Monaldi Arch Chest Dis, 2017, 87(3): 817.
31. 李文婷, 袁平, 吴常伟, 等. 右心房压力联合二氧化碳通气当量斜率预测慢性血栓栓塞性肺动脉高压患者预后的价值研究. 中国循环杂志, 2020, 35(7): 670-676.
32. 贺晓玉, 李稚, 邓京捷. Verification phase作为判定最大摄氧量新方法的研究进展. 中国运动医学杂志, 2019, 38(12): 1087-1093.
33. 朱子聪, 金凌, 王子璇, 等. 皮肌炎患者肌力评估及康复治疗研究现状. 中国皮肤性病学杂志, 2022, 36(12): 1350-1355.
34. Cocchiarella L, Anderson G. American Medical Association: guides to the evaluation of permanent impairment. 5th ed. Chicago: American Medical Association, 2000. 107.
35. Guazzi M, Arena R, Halle M, et al. 2016 focused update: clinical recommendations for cardiopulmonary exercise testing data assessment in specific patient populations. Circulation, 2016, 133(24): e694-e711.
36. 陈瑜, 曹芳. 居家腹膜透析患者体力活动水平现状及护理对策. 中国卫生标准管理, 2024, 15(3): 164-168.
37. 黄君, 罗健. 哮喘及疑诊哮喘患儿运动激发试验中肺功能及目标心率到达与维持时间分析. 中国临床新医学, 2021, 14(5): 492-496.
38. 蒋琦, 常益益, 李洋. 心肺运动试验在老年慢性阻塞性肺疾病中应用. 中国老年学杂志, 2023, 43(20): 4949-4952.
39. 郝永发, 陈琛, 马晓虎, 等. 心肺运动试验对慢性阻塞性肺疾病患者气流受限严重程度的预测价值. 宁夏医学杂志, 2023, 45(11): 988-991,960.
40. Cottini M, Lombardi C, Berti A, et al. Small-airway dysfunction in paediatric asthma. Curr Opin Allergy Clin Immunol, 2021, 21(2): 128-134.
41. Pigakis KM, Stavrou VT, Kontopodi AK, et al. Impact of isolated exercise-induced small airway dysfunction on exercise performance in professional male cyclists. Sports (Basel), 2024, 12(4): 112.

Chinese Journal of Respiratory and Critical Care Medicine

Latest ArticlesAnalysis of the factors affecting small airway dysfunction and evaluation of cardiopulmonary function in the patients with chronic duration of asthma

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