- Department of Respiratory and Critical Care Medicine, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
Bronchiectasis is a heterogeneous disease characterized by abnormal expansion of the bronchi, manifested by cough, sputum, and recurring lung infections. As one of the common fungi of lung infection, aspergillus can not only appear as the outcome of the disease in bronchiectasis, but also as an inducement to participate in the disease progression, and ultimately complicate the course of bronchiectasis. This article describes the susceptibility factors and pathogenic mechanisms of aspergillus in bronchiectasis, and further introduces the diagnosis and treatment status of bronchiectasis combined with aspergillus infection, aiming to clarify the effect of aspergillus infection on bronchiectasis and provide new thinking directions for its clinical diagnosis and treatment.
Citation: LI Xiu, TONG Xiang, FAN Hong. Role of aspergillus infection in bronchiectasis and its diagnosis and treatment. West China Medical Journal, 2022, 37(1): 1-7. doi: 10.7507/1002-0179.202112064 Copy
1. | 支气管扩张症专家共识撰写协作组, 中华医学会呼吸病学分会感染学组. 中国成人支气管扩张症诊断与治疗专家共识. 中华结核和呼吸杂志, 2021, 44(4): 311-321. |
2. | Chalmers JD, Chang AB, Chotirmall SH, et al. Bronchiectasis. Nat Rev Dis Primers, 2018, 4(1): 45. |
3. | Chalmers JD, Aliberti S, Blasi F. Management of bronchiectasis in adults. Eur Respir J, 2015, 45(5): 1446-1462. |
4. | Boyton RJ, Altmann DM. Bronchiectasis: current concepts in pathogenesis, immunology, and microbiology. Annu Rev Pathol, 2016, 11: 523-554. |
5. | Chotirmall SH, Al-Alawi M, Mirkovic B, et al. Aspergillus-associated airway disease, inflammation, and the innate immune response. Biomed Res Int, 2013, 2013: 723129. |
6. | Yang B, Kim T, Ryu J, et al. Increased incidence and associated risk factors of aspergillosis in patients with bronchiectasis. J Pers Med, 2021, 11(5): 422. |
7. | Aliberti S, Lonni S, Dore S, et al. Clinical phenotypes in adult patients with bronchiectasis. Eur Respir J, 2016, 47(4): 1113-1122. |
8. | Gramegna A, Amati F, Terranova L, et al. Neutrophil elastase in bronchiectasis. Respir Res, 2017, 18(1): 211. |
9. | 焦丽君, 章菁仪, 王欣燕. 中性粒细胞弹性蛋白酶对支气管扩张症作用机制的研究进展. 现代医学, 2021, 49(6): 710-713. |
10. | Amitani R, Wilson R, Rutman A, et al. Effects of human neutrophil elastase and pseudomonas aeruginosa proteinases on human respiratory epithelium. Am J Respir Cell Mol Biol, 1991, 4(1): 26-32. |
11. | Kunst H, Wickremasinghe M, Wells A, et al. Nontuberculous mycobacterial disease and aspergillus-related lung disease in bronchiectasis. Eur Respir J, 2006, 28(2): 352-357. |
12. | De Soyza A, Aliberti S. Bronchiectasis and aspergillus: how are they linked?. Med Mycol, 2017, 55(1): 69-81. |
13. | Fröhlich-Nowoisky J, Pickersgill DA, Després VR, et al. High diversity of fungi in air particulate matter. Proc Natl Acad Sci U S A, 2009, 106(31): 12814-12819. |
14. | Lewington-Gower E, Chan L, Shah A. Review of current and future therapeutics in ABPA. Ther Adv Chronic Dis, 2021, 12: 20406223211047003. |
15. | Máiz L, Vendrell M, Olveira C, et al. Prevalence and factors associated with isolation of aspergillus and candida from sputum in patients with non-cystic fibrosis bronchiectasis. Respiration, 2015, 89(5): 396-403. |
16. | Moldoveanu B, Gearhart AM, Jalil BA, et al. Pulmonary aspergillosis: spectrum of disease. Am J Med Sci, 2021, 361(4): 411-419. |
17. | Robinson BW, Venaille TJ, Mendis AH, et al. Allergens as proteases: an Aspergillus fumigatus proteinase directly induces human epithelial cell detachment. J Allergy Clin Immunol, 1990, 86(5): 726-731. |
18. | Tomee JF, Wierenga AT, Hiemstra PS, et al. Proteases from Aspergillus fumigatus induce release of proinflammatory cytokines and cell detachment in airway epithelial cell lines. J Infect Dis, 1997, 176(1): 300-303. |
19. | Kogan TV, Jadoun J, Mittelman L, et al. Involvement of secreted Aspergillus fumigatus proteases in disruption of the actin fiber cytoskeleton and loss of focal adhesion sites in infected A549 lung pneumocytes. J Infect Dis, 2004, 189(11): 1965-1973. |
20. | Kauffman HF. Immunopathogenesis of allergic bronchopulmonary aspergillosis and airway remodeling. Front Biosci, 2003, 8: e190-e196. |
21. | Oguma T, Asano K, Tomomatsu K, et al. Induction of mucin and MUC5AC expression by the protease activity of Aspergillus fumigatus in airway epithelial cells. J Immunol, 2011, 187(2): 999-1005. |
22. | Yang Z, Jaeckisch SM, Mitchell CG. Enhanced binding of Aspergillus fumigatus spores to A549 epithelial cells and extracellular matrix proteins by a component from the spore surface and inhibition by rat lung lavage fluid. Thorax, 2000, 55(7): 579-584. |
23. | 廖军, 钟白玉, 郝飞. 烟曲霉及其渗出物影响肺泡巨噬细胞功能的实验研究. 西南国防医药, 2007(6): 695-697. |
24. | Amitani R, Taylor G, Elezis EN, et al. Purification and characterization of factors produced by Aspergillus fumigatus which affect human ciliated respiratory epithelium. Infect Immun, 1995, 63(9): 3266-3271. |
25. | Mircescu MM, Lipuma L, van Rooijen N, et al. Essential role for neutrophils but not alveolar macrophages at early time points following Aspergillus fumigatus infection. J Infect Dis, 2009, 200(4): 647-656. |
26. | Borger P, Koëter GH, Timmerman JA, et al. Proteases from Aspergillus fumigatus induce interleukin (IL)-6 and IL-8 production in airway epithelial cell lines by transcriptional mechanisms. J Infect Dis, 1999, 180(4): 1267-1274. |
27. | Gibson PG, Wark PA, Simpson JL, et al. Induced sputum IL-8 gene expression, neutrophil influx and MMP-9 in allergic bronchopulmonary aspergillosis. Eur Respir J, 2003, 21(4): 582-588. |
28. | Kauffman HF, Tomee JF, van de Riet MA, et al. Protease-dependent activation of epithelial cells by fungal allergens leads to morphologic changes and cytokine production. J Allergy Clin Immunol, 2000, 105(6 Pt 1): 1185-1193. |
29. | Wark PA, Saltos N, Simpson J, et al. Induced sputum eosinophils and neutrophils and bronchiectasis severity in allergic bronchopulmonary aspergillosis. Eur Respir J, 2000, 16(6): 1095-1101. |
30. | Sepper R, Konttinen YT, Sorsa T, et al. Gelatinolytic and type Ⅳ collagenolytic activity in bronchiectasis. Chest, 1994, 106(4): 1129-1133. |
31. | Kita H, Abu-Ghazaleh RI, Sur S, et al. Eosinophil major basic protein induces degranulation and IL-8 production by human eosinophils. J Immunol, 1995, 154(9): 4749-4758. |
32. | Ohno I, Ohtani H, Nitta Y, et al. Eosinophils as a source of matrix metalloproteinase-9 in asthmatic airway inflammation. Am J Respir Cell Mol Biol, 1997, 16(3): 212-219. |
33. | Sepper R, Konttinen YT, Ding Y, et al. Human neutrophil collagenase (MMP-8), identified in bronchiectasis BAL fluid, correlates with severity of disease. Chest, 1995, 107(6): 1641-1647. |
34. | Becker KL, Gresnigt MS, Smeekens SP, et al. Pattern recognition pathways leading to a Th2 cytokine bias in allergic bronchopulmonary aspergillosis patients. Clin Exp Allergy, 2015, 45(2): 423-437. |
35. | Chen JJ, He YS, Zhong XJ, et al. Ribonuclease T2 from Aspergillus fumigatus promotes T helper type 2 responses through M2 polarization of macrophages. Int J Mol Med, 2020, 46(2): 718-728. |
36. | Homma T, Kato A, Bhushan B, et al. Role of Aspergillus fumigatus in triggering protease-activated receptor-2 in airway epithelial cells and skewing the cells toward a T-helper 2 bias. Am J Respir Cell Mol Biol, 2016, 54(1): 60-70. |
37. | Chen K, Kolls JK. T cell-mediated host immune defenses in the lung. Annu Rev Immunol, 2013, 31: 605-633. |
38. | Zhu Z, Homer RJ, Wang Z, et al. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J Clin Invest, 1999, 103(6): 779-788. |
39. | Zheng T, Zhu Z, Wang Z, et al. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema. J Clin Invest, 2000, 106(9): 1081-1093. |
40. | Roilides E, Dimitriadou A, Kadiltsoglou I, et al. IL-10 exerts suppressive and enhancing effects on antifungal activity of mononuclear phagocytes against Aspergillus fumigatus. J Immunol, 1997, 158(1): 322-329. |
41. | Cenci E, Mencacci A, Del Sero G, et al. Interleukin-4 causes susceptibility to invasive pulmonary aspergillosis through suppression of protective type I responses. J Infect Dis, 1999, 180(6): 1957-1968. |
42. | Asadullah K, Sterry W, Volk HD. Interleukin-10 therapy-review of a new approach. Pharmacol Rev, 2003, 55(2): 241-269. |
43. | Kim Y, Lee HY, Gu KM, et al. Delayed diagnosis of allergic bronchopulmonary aspergillosis due to absence of asthmatic symptoms. Asia Pac Allergy, 2016, 6(3): 187-191. |
44. | Wang S, Zhang J, Zhang C, et al. Clinical characteristics of allergic bronchopulmonary aspergillosis in patients with and without bronchiectasis. J Asthma, 2021, 30: 1-7. |
45. | Mac Aogáin M, Tiew PY, Lim AYH, et al. Distinct “immunoallertypes” of disease and high frequencies of sensitization in non-cystic fibrosis bronchiectasis. Am J Respir Crit Care Med, 2019, 199(7): 842-853. |
46. | Vandewoude KH, Blot SI, Depuydt P, et al. Clinical relevance of aspergillus isolation from respiratory tract samples in critically ill patients. Crit Care, 2006, 10(1): R31. |
47. | 申旺, 叶丽燕, 杨文丽, 等. 血浆(1, 3)-β-D-葡聚糖在侵袭性真菌感染临床诊治中的应用评价. 中华医院感染学杂志, 2018, 28(9): 1288-1291. |
48. | 林贵兰, 马晓波, 房丽丽, 等. (1, 3)-β-D-葡聚糖连续监测在抗真菌药物治疗中的评价. 中华医院感染学杂志, 2016, 26(1): 37-39. |
49. | 黄猛, 黎国喜, 陈天全. 支气管肺泡灌洗液 1, 3-β-D 葡聚糖检测(G 试验)、半乳甘露聚糖检测(GM 试验)对早期诊断侵袭性肺部真菌感染的诊断价值. 临床肺科杂志, 2019, 24(6): 992-995. |
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52. | Zhang K, Yu C, Li Y, et al. Next-generation sequencing technology for detecting pulmonary fungal infection in bronchoalveolar lavage fluid of a patient with dermatomyositis: a case report and literature review. BMC Infect Dis, 2020, 20(1): 608. |
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- 1. 支气管扩张症专家共识撰写协作组, 中华医学会呼吸病学分会感染学组. 中国成人支气管扩张症诊断与治疗专家共识. 中华结核和呼吸杂志, 2021, 44(4): 311-321.
- 2. Chalmers JD, Chang AB, Chotirmall SH, et al. Bronchiectasis. Nat Rev Dis Primers, 2018, 4(1): 45.
- 3. Chalmers JD, Aliberti S, Blasi F. Management of bronchiectasis in adults. Eur Respir J, 2015, 45(5): 1446-1462.
- 4. Boyton RJ, Altmann DM. Bronchiectasis: current concepts in pathogenesis, immunology, and microbiology. Annu Rev Pathol, 2016, 11: 523-554.
- 5. Chotirmall SH, Al-Alawi M, Mirkovic B, et al. Aspergillus-associated airway disease, inflammation, and the innate immune response. Biomed Res Int, 2013, 2013: 723129.
- 6. Yang B, Kim T, Ryu J, et al. Increased incidence and associated risk factors of aspergillosis in patients with bronchiectasis. J Pers Med, 2021, 11(5): 422.
- 7. Aliberti S, Lonni S, Dore S, et al. Clinical phenotypes in adult patients with bronchiectasis. Eur Respir J, 2016, 47(4): 1113-1122.
- 8. Gramegna A, Amati F, Terranova L, et al. Neutrophil elastase in bronchiectasis. Respir Res, 2017, 18(1): 211.
- 9. 焦丽君, 章菁仪, 王欣燕. 中性粒细胞弹性蛋白酶对支气管扩张症作用机制的研究进展. 现代医学, 2021, 49(6): 710-713.
- 10. Amitani R, Wilson R, Rutman A, et al. Effects of human neutrophil elastase and pseudomonas aeruginosa proteinases on human respiratory epithelium. Am J Respir Cell Mol Biol, 1991, 4(1): 26-32.
- 11. Kunst H, Wickremasinghe M, Wells A, et al. Nontuberculous mycobacterial disease and aspergillus-related lung disease in bronchiectasis. Eur Respir J, 2006, 28(2): 352-357.
- 12. De Soyza A, Aliberti S. Bronchiectasis and aspergillus: how are they linked?. Med Mycol, 2017, 55(1): 69-81.
- 13. Fröhlich-Nowoisky J, Pickersgill DA, Després VR, et al. High diversity of fungi in air particulate matter. Proc Natl Acad Sci U S A, 2009, 106(31): 12814-12819.
- 14. Lewington-Gower E, Chan L, Shah A. Review of current and future therapeutics in ABPA. Ther Adv Chronic Dis, 2021, 12: 20406223211047003.
- 15. Máiz L, Vendrell M, Olveira C, et al. Prevalence and factors associated with isolation of aspergillus and candida from sputum in patients with non-cystic fibrosis bronchiectasis. Respiration, 2015, 89(5): 396-403.
- 16. Moldoveanu B, Gearhart AM, Jalil BA, et al. Pulmonary aspergillosis: spectrum of disease. Am J Med Sci, 2021, 361(4): 411-419.
- 17. Robinson BW, Venaille TJ, Mendis AH, et al. Allergens as proteases: an Aspergillus fumigatus proteinase directly induces human epithelial cell detachment. J Allergy Clin Immunol, 1990, 86(5): 726-731.
- 18. Tomee JF, Wierenga AT, Hiemstra PS, et al. Proteases from Aspergillus fumigatus induce release of proinflammatory cytokines and cell detachment in airway epithelial cell lines. J Infect Dis, 1997, 176(1): 300-303.
- 19. Kogan TV, Jadoun J, Mittelman L, et al. Involvement of secreted Aspergillus fumigatus proteases in disruption of the actin fiber cytoskeleton and loss of focal adhesion sites in infected A549 lung pneumocytes. J Infect Dis, 2004, 189(11): 1965-1973.
- 20. Kauffman HF. Immunopathogenesis of allergic bronchopulmonary aspergillosis and airway remodeling. Front Biosci, 2003, 8: e190-e196.
- 21. Oguma T, Asano K, Tomomatsu K, et al. Induction of mucin and MUC5AC expression by the protease activity of Aspergillus fumigatus in airway epithelial cells. J Immunol, 2011, 187(2): 999-1005.
- 22. Yang Z, Jaeckisch SM, Mitchell CG. Enhanced binding of Aspergillus fumigatus spores to A549 epithelial cells and extracellular matrix proteins by a component from the spore surface and inhibition by rat lung lavage fluid. Thorax, 2000, 55(7): 579-584.
- 23. 廖军, 钟白玉, 郝飞. 烟曲霉及其渗出物影响肺泡巨噬细胞功能的实验研究. 西南国防医药, 2007(6): 695-697.
- 24. Amitani R, Taylor G, Elezis EN, et al. Purification and characterization of factors produced by Aspergillus fumigatus which affect human ciliated respiratory epithelium. Infect Immun, 1995, 63(9): 3266-3271.
- 25. Mircescu MM, Lipuma L, van Rooijen N, et al. Essential role for neutrophils but not alveolar macrophages at early time points following Aspergillus fumigatus infection. J Infect Dis, 2009, 200(4): 647-656.
- 26. Borger P, Koëter GH, Timmerman JA, et al. Proteases from Aspergillus fumigatus induce interleukin (IL)-6 and IL-8 production in airway epithelial cell lines by transcriptional mechanisms. J Infect Dis, 1999, 180(4): 1267-1274.
- 27. Gibson PG, Wark PA, Simpson JL, et al. Induced sputum IL-8 gene expression, neutrophil influx and MMP-9 in allergic bronchopulmonary aspergillosis. Eur Respir J, 2003, 21(4): 582-588.
- 28. Kauffman HF, Tomee JF, van de Riet MA, et al. Protease-dependent activation of epithelial cells by fungal allergens leads to morphologic changes and cytokine production. J Allergy Clin Immunol, 2000, 105(6 Pt 1): 1185-1193.
- 29. Wark PA, Saltos N, Simpson J, et al. Induced sputum eosinophils and neutrophils and bronchiectasis severity in allergic bronchopulmonary aspergillosis. Eur Respir J, 2000, 16(6): 1095-1101.
- 30. Sepper R, Konttinen YT, Sorsa T, et al. Gelatinolytic and type Ⅳ collagenolytic activity in bronchiectasis. Chest, 1994, 106(4): 1129-1133.
- 31. Kita H, Abu-Ghazaleh RI, Sur S, et al. Eosinophil major basic protein induces degranulation and IL-8 production by human eosinophils. J Immunol, 1995, 154(9): 4749-4758.
- 32. Ohno I, Ohtani H, Nitta Y, et al. Eosinophils as a source of matrix metalloproteinase-9 in asthmatic airway inflammation. Am J Respir Cell Mol Biol, 1997, 16(3): 212-219.
- 33. Sepper R, Konttinen YT, Ding Y, et al. Human neutrophil collagenase (MMP-8), identified in bronchiectasis BAL fluid, correlates with severity of disease. Chest, 1995, 107(6): 1641-1647.
- 34. Becker KL, Gresnigt MS, Smeekens SP, et al. Pattern recognition pathways leading to a Th2 cytokine bias in allergic bronchopulmonary aspergillosis patients. Clin Exp Allergy, 2015, 45(2): 423-437.
- 35. Chen JJ, He YS, Zhong XJ, et al. Ribonuclease T2 from Aspergillus fumigatus promotes T helper type 2 responses through M2 polarization of macrophages. Int J Mol Med, 2020, 46(2): 718-728.
- 36. Homma T, Kato A, Bhushan B, et al. Role of Aspergillus fumigatus in triggering protease-activated receptor-2 in airway epithelial cells and skewing the cells toward a T-helper 2 bias. Am J Respir Cell Mol Biol, 2016, 54(1): 60-70.
- 37. Chen K, Kolls JK. T cell-mediated host immune defenses in the lung. Annu Rev Immunol, 2013, 31: 605-633.
- 38. Zhu Z, Homer RJ, Wang Z, et al. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J Clin Invest, 1999, 103(6): 779-788.
- 39. Zheng T, Zhu Z, Wang Z, et al. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema. J Clin Invest, 2000, 106(9): 1081-1093.
- 40. Roilides E, Dimitriadou A, Kadiltsoglou I, et al. IL-10 exerts suppressive and enhancing effects on antifungal activity of mononuclear phagocytes against Aspergillus fumigatus. J Immunol, 1997, 158(1): 322-329.
- 41. Cenci E, Mencacci A, Del Sero G, et al. Interleukin-4 causes susceptibility to invasive pulmonary aspergillosis through suppression of protective type I responses. J Infect Dis, 1999, 180(6): 1957-1968.
- 42. Asadullah K, Sterry W, Volk HD. Interleukin-10 therapy-review of a new approach. Pharmacol Rev, 2003, 55(2): 241-269.
- 43. Kim Y, Lee HY, Gu KM, et al. Delayed diagnosis of allergic bronchopulmonary aspergillosis due to absence of asthmatic symptoms. Asia Pac Allergy, 2016, 6(3): 187-191.
- 44. Wang S, Zhang J, Zhang C, et al. Clinical characteristics of allergic bronchopulmonary aspergillosis in patients with and without bronchiectasis. J Asthma, 2021, 30: 1-7.
- 45. Mac Aogáin M, Tiew PY, Lim AYH, et al. Distinct “immunoallertypes” of disease and high frequencies of sensitization in non-cystic fibrosis bronchiectasis. Am J Respir Crit Care Med, 2019, 199(7): 842-853.
- 46. Vandewoude KH, Blot SI, Depuydt P, et al. Clinical relevance of aspergillus isolation from respiratory tract samples in critically ill patients. Crit Care, 2006, 10(1): R31.
- 47. 申旺, 叶丽燕, 杨文丽, 等. 血浆(1, 3)-β-D-葡聚糖在侵袭性真菌感染临床诊治中的应用评价. 中华医院感染学杂志, 2018, 28(9): 1288-1291.
- 48. 林贵兰, 马晓波, 房丽丽, 等. (1, 3)-β-D-葡聚糖连续监测在抗真菌药物治疗中的评价. 中华医院感染学杂志, 2016, 26(1): 37-39.
- 49. 黄猛, 黎国喜, 陈天全. 支气管肺泡灌洗液 1, 3-β-D 葡聚糖检测(G 试验)、半乳甘露聚糖检测(GM 试验)对早期诊断侵袭性肺部真菌感染的诊断价值. 临床肺科杂志, 2019, 24(6): 992-995.
- 50. 中华医学会呼吸病学分会感染学组, 中华结核和呼吸杂志编辑委员会. 肺真菌病诊断和治疗专家共识. 中华结核和呼吸杂志, 2007, 30(11): 821-834.
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