Chronic Pulmonary Aspergillosis as a Considerable Complication in Post-Tuberculosis Lung Disease

Abstract

Post-tuberculosis lung disease (PTLD) has only recently been put in the spotlight as a medical entity. Recent data suggest that up to 50% of tuberculosis (TB) patients are left with PTLD-related impairment after completion of TB treatment. The presence of residual cavities in the lung is the largest risk factor for the development of chronic pulmonary aspergillosis (CPA) globally. Diagnosis of CPA is based on four criteria including a typical radiological pattern, evidence of Aspergillus species, exclusion of alternative diagnosis, and a chronic course of disease. In this manuscript, we provide a narrative review on CPA as a serious complication for patients with PTLD.

Keywords

post-tuberculosis disease - post-tuberculosis lung disease - chronic pulmonary aspergillosis - fungal infection - Aspergillus

Publication History

Article published online:
09 January 2024

• References

• 1 [Anonymous] Global tuberculosis report 2020. In: WHO; 2020
• 2 Allwood BW, Byrne A, Meghji J, Rachow A, van der Zalm MM, Schoch OD. Post-tuberculosis lung disease: clinical review of an under-recognised global challenge. Respiration 2021; 100 (08) 751-763
• 3 Denning DW, Cadranel J, Beigelman-Aubry C. et al; European Society for Clinical Microbiology and Infectious Diseases and European Respiratory Society. Chronic pulmonary aspergillosis: rationale and clinical guidelines for diagnosis and management. Eur Respir J 2016; 47 (01) 45-68
• 4 Denning DW, Pleuvry A, Cole DC. Global burden of chronic pulmonary aspergillosis complicating sarcoidosis. Eur Respir J 2013; 41 (03) 621-626
• 5 Laursen CB, Davidsen JR, Van Acker L. et al. CPAnet registry-an international chronic pulmonary aspergillosis registry. J Fungi (Basel) 2020; 6 (03) 6
• 6 Baluku JB, Nuwagira E, Bongomin F, Denning DW. Pulmonary TB and chronic pulmonary aspergillosis: clinical differences and similarities. Int J Tuberc Lung Dis 2021; 25 (07) 537-546
• 7 Cohen A, Mathiasen VD, Schön T, Wejse C. The global prevalence of latent tuberculosis: a systematic review and meta-analysis. Eur Respir J 2019; 54 (03) 54
• 8 Tiemersma EW, van der Werf MJ, Borgdorff MW, Williams BG, Nagelkerke NJ. Natural history of tuberculosis: duration and fatality of untreated pulmonary tuberculosis in HIV negative patients: a systematic review. PLoS One 2011; 6 (04) e17601
• 9 Dodd PJ, Yuen CM, Jayasooriya SM, van der Zalm MM, Seddon JA. Quantifying the global number of tuberculosis survivors: a modelling study. Lancet Infect Dis 2021; 21 (07) 984-992
• 10 Maier C, Chesov D, Schaub D. et al. Long-term treatment outcomes in patients with multidrug-resistant tuberculosis. Clin Microbiol Infect 2023; 29 (06) 751-757
• 11 Otto-Knapp R, Häcker B, Krieger D. et al. Long-term multidrug- and rifampicin-resistant tuberculosis treatment outcome by new WHO definitions in Germany. Eur Respir J 2022; 60 (05) 60
• 12 Linh NN, Viney K, Gegia M. et al. World Health Organization treatment outcome definitions for tuberculosis: 2021 update. Eur Respir J 2021; 58 (02) 58
• 13 Romanowski K, Baumann B, Basham CA, Ahmad Khan F, Fox GJ, Johnston JC. Long-term all-cause mortality in people treated for tuberculosis: a systematic review and meta-analysis. Lancet Infect Dis 2019; 19 (10) 1129-1137
• 14 Menzies NA, Quaife M, Allwood BW. et al. Lifetime burden of disease due to incident tuberculosis: a global reappraisal including post-tuberculosis sequelae. Lancet Glob Health 2021; 9 (12) e1679-e1687
• 15 Quaife M, Houben RMGJ, Allwood B. et al. Post-tuberculosis mortality and morbidity: valuing the hidden epidemic. Lancet Respir Med 2020; 8 (04) 332-333
• 16 Nightingale R, Carlin F, Meghji J. et al. Post-TB health and wellbeing. Int J Tuberc Lung Dis 2023; 27 (04) 248-283
• 17 Ahmad N, Javaid A, Syed Sulaiman SA. et al. Effects of multidrug resistant tuberculosis treatment on patients' health related quality of life: results from a follow up study. PLoS One 2016; 11 (07) e0159560
• 18 Daniels KJ, Irusen E, Pharaoh H, Hanekom S. Post-tuberculosis health-related quality of life, lung function and exercise capacity in a cured pulmonary tuberculosis population in the Breede Valley District, South Africa. S Afr J Physiother 2019; 75 (01) 1319
• 19 Muniyandi M, Rajeswari R, Balasubramanian R. et al. Evaluation of post-treatment health-related quality of life (HRQoL) among tuberculosis patients. Int J Tuberc Lung Dis 2007; 11 (08) 887-892
• 20 Rajeswari R, Muniyandi M, Balasubramanian R, Narayanan PR. Perceptions of tuberculosis patients about their physical, mental and social well-being: a field report from south India. Soc Sci Med 2005; 60 (08) 1845-1853
• 21 Meghji J, Gregorius S, Madan J. et al. The long term effect of pulmonary tuberculosis on income and employment in a low income, urban setting. Thorax 2021; 76 (04) 387-395
• 22 Igbokwe V, Ruby LC, Sultanli A, Bélard S. Post-tuberculosis sequelae in children and adolescents: a systematic review. Lancet Infect Dis 2023; 23 (04) e138-e150
• 23 Mpagama SG, Msaji KS, Kaswaga O. et al. The burden and determinants of post-TB lung disease. Int J Tuberc Lung Dis 2021; 25 (10) 846-853
• 24 Meghji J, Mortimer K, Agusti A. et al. Improving lung health in low-income and middle-income countries: from challenges to solutions. Lancet 2021; 397 (10277): 928-940
• 25 Allwood B, van der Zalm M, Makanda G, Mortimer K. Steering Committee of the First International Post-Tuberculosis Symposium. The long shadow post-tuberculosis. Lancet Infect Dis 2019; 19 (11) 1170-1171
• 26 Amaral AF, Coton S, Kato B. et al; BOLD Collaborative Research Group. Tuberculosis associates with both airflow obstruction and low lung function: BOLD results. Eur Respir J 2015; 46 (04) 1104-1112
• 27 Maleche-Obimbo E, Odhiambo MA, Njeri L. et al. Magnitude and factors associated with post-tuberculosis lung disease in low- and middle-income countries: a systematic review and meta-analysis. PLoS Glob Public Health 2022; 2 (12) e0000805
• 28 Visca D, Centis R, Munoz-Torrico M, Pontali E. Post-tuberculosis sequelae: the need to look beyond treatment outcome. Int J Tuberc Lung Dis 2020; 24 (08) 761-762
• 29 Rachow A, Ivanova O, Wallis R. et al. TB sequel: incidence, pathogenesis and risk factors of long-term medical and social sequelae of pulmonary TB - a study protocol. BMC Pulm Med 2019; 19 (01) 4
• 30 Ravimohan S, Kornfeld H, Weissman D, Bisson GP. Tuberculosis and lung damage: from epidemiology to pathophysiology. Eur Respir Rev 2018; 27 (147) 27
• 31 Byrne AL, Marais BJ, Mitnick CD, Lecca L, Marks GB. Tuberculosis and chronic respiratory disease: a systematic review. Int J Infect Dis 2015; 32: 138-146
• 32 Meghji J, Simpson H, Squire SB, Mortimer K. A systematic review of the prevalence and pattern of imaging defined post-TB lung disease. PLoS One 2016; 11 (08) e0161176
• 33 Panda A, Bhalla AS, Sharma R. et al. Correlation of chest computed tomography findings with dyspnea and lung functions in post-tubercular sequelae. Lung India 2016; 33 (06) 592-599
• 34 Malherbe ST, Shenai S, Ronacher K. et al; Catalysis TB–Biomarker Consortium. Persisting positron emission tomography lesion activity and Mycobacterium tuberculosis mRNA after tuberculosis cure. Nat Med 2016; 22 (10) 1094-1100
• 35 Allwood BW, Stolbrink M, Baines N. et al. Persistent chronic respiratory symptoms despite TB cure is poorly correlated with lung function. Int J Tuberc Lung Dis 2021; 25 (04) 262-270
• 36 Pasipanodya JG, Miller TL, Vecino M. et al. Pulmonary impairment after tuberculosis. Chest 2007; 131 (06) 1817-1824
• 37 Ivanova O, Hoffmann VS, Lange C, Hoelscher M, Rachow A. Post-tuberculosis lung impairment: systematic review and meta-analysis of spirometry data from 14 621 people. Eur Respir Rev 2023; 32 (168) 32
• 38 Gai X, Allwood B, Sun Y. Post-tuberculosis lung disease and chronic obstructive pulmonary disease. Chin Med J (Engl) 2023; 136 (16) 1923-1928
• 39 Meghji J, Lesosky M, Joekes E. et al. Patient outcomes associated with post-tuberculosis lung damage in Malawi: a prospective cohort study. Thorax 2020; 75 (03) 269-278
• 40 Nightingale R, Chinoko B, Lesosky M. et al. Respiratory symptoms and lung function in patients treated for pulmonary tuberculosis in Malawi: a prospective cohort study. Thorax 2022; 77 (11) 1131-1139
• 41 Christenson SA, Smith BM, Bafadhel M, Putcha N. Chronic obstructive pulmonary disease. Lancet 2022; 399 (10342): 2227-2242
• 42 Xing Z, Sun T, Janssens JP. et al. Airflow obstruction and small airway dysfunction following pulmonary tuberculosis: a cross-sectional survey. Thorax 2023; 78 (03) 274-280
• 43 Hnizdo E, Singh T, Churchyard G. Chronic pulmonary function impairment caused by initial and recurrent pulmonary tuberculosis following treatment. Thorax 2000; 55 (01) 32-38
• 44 de Vallière S, Barker RD. Residual lung damage after completion of treatment for multidrug-resistant tuberculosis. Int J Tuberc Lung Dis 2004; 8 (06) 767-771
• 45 Ralph AP, Kenangalem E, Waramori G. et al. High morbidity during treatment and residual pulmonary disability in pulmonary tuberculosis: under-recognised phenomena. PLoS One 2013; 8 (11) e80302
• 46 Byrne AL, Marais BJ, Mitnick CD. et al. Chronic airflow obstruction after successful treatment of multidrug-resistant tuberculosis. ERJ Open Res 2017; 3 (03) 3
• 47 Manji M, Shayo G, Mamuya S, Mpembeni R, Jusabani A, Mugusi F. Lung functions among patients with pulmonary tuberculosis in Dar es Salaam - a cross-sectional study. BMC Pulm Med 2016; 16 (01) 58
• 48 Devoid I, Sillah AK, Sutherland J. et al. The household economic burden of drug-susceptible TB diagnosis and treatment in The Gambia. Int J Tuberc Lung Dis 2022; 26 (12) 1162-1169
• 49 Günther G, Ithete S. Clinical care for patients with post-TB lung disease. Int J Tuberc Lung Dis 2021; 25 (03) 252-253
• 50 Cudahy PGT, Wilson D, Cohen T. Risk factors for recurrent tuberculosis after successful treatment in a high burden setting: a cohort study. BMC Infect Dis 2020; 20 (01) 789
• 51 Theron G, Venter R, Calligaro G. et al. Xpert MTB/RIF results in patients with previous tuberculosis: can we distinguish true from false positive results?. Clin Infect Dis 2016; 62 (08) 995-1001
• 52 Fayos M, Silva JT, López-Medrano F, Aguado JM. Non-tuberculous mycobacteria and Aspergillus lung co-infection: systematic review. J Clin Med 2022; 11 (19) 11
• 53 Takeda K, Imamura Y, Takazono T. et al. The risk factors for developing of chronic pulmonary aspergillosis in nontuberculous mycobacteria patients and clinical characteristics and outcomes in chronic pulmonary aspergillosis patients coinfected with nontuberculous mycobacteria. Med Mycol 2016; 54 (02) 120-127
• 54 Khan R, Malik NI, Razaque A. Imaging of pulmonary post-tuberculosis sequelae. Pak J Med Sci 2020; 36 (01) S75-S82
• 55 van Kampen SC, Wanner A, Edwards M. et al. International research and guidelines on post-tuberculosis chronic lung disorders: a systematic scoping review. BMJ Glob Health 2018; 3 (04) e000745
• 56 Bongomin F. Post-tuberculosis chronic pulmonary aspergillosis: an emerging public health concern. PLoS Pathog 2020; 16 (08) e1008742
• 57 Hsu D, Irfan M, Jabeen K. et al. Post tuberculosis treatment infectious complications. Int J Infect Dis 2020; 92S: S41-S45
• 58 Rajpurohit R, Wagh P, Heda M, Dubey G, Gujar PS. Prevalence of chronic pulmonary aspergillosis in fibrocavitary pulmonary tuberculosis patients. J Family Med Prim Care 2023; 12 (01) 106-110
• 59 Menon B, Nima G, Dogra V, Jha S. Evaluation of the radiological sequelae after treatment completion in new cases of pulmonary, pleural, and mediastinal tuberculosis. Lung India 2015; 32 (03) 241-245
• 60 Qi Q, Wang W, Li T, Zhang Y, Li Y. Aetiology and clinical characteristics of patients with bronchiectasis in a Chinese Han population: a prospective study. Respirology 2015; 20 (06) 917-924
• 61 Dhar R, Singh S, Talwar D. et al. Bronchiectasis in India: results from the European Multicentre Bronchiectasis Audit and Research Collaboration (EMBARC) and Respiratory Research Network of India Registry. Lancet Glob Health 2019; 7 (09) e1269-e1279
• 62 Anwar GA, McDonnell MJ, Worthy SA. et al. Phenotyping adults with non-cystic fibrosis bronchiectasis: a prospective observational cohort study. Respir Med 2013; 107 (07) 1001-1007
• 63 Pasteur MC, Helliwell SM, Houghton SJ. et al. An investigation into causative factors in patients with bronchiectasis. Am J Respir Crit Care Med 2000; 162 (4 Pt 1): 1277-1284
• 64 Denning DW, Riniotis K, Dobrashian R, Sambatakou H. Chronic cavitary and fibrosing pulmonary and pleural aspergillosis: case series, proposed nomenclature change, and review. Clin Infect Dis 2003; 37 (Suppl. 03) S265-S280
• 65 Lowes D, Al-Shair K, Newton PJ. et al. Predictors of mortality in chronic pulmonary aspergillosis. Eur Respir J 2017; 49 (02) 49
• 66 Agarwal R, Vishwanath G, Aggarwal AN, Garg M, Gupta D, Chakrabarti A. Itraconazole in chronic cavitary pulmonary aspergillosis: a randomised controlled trial and systematic review of literature. Mycoses 2013; 56 (05) 559-570
• 67 Smith NL, Denning DW. Underlying conditions in chronic pulmonary aspergillosis including simple aspergilloma. Eur Respir J 2011; 37 (04) 865-872
• 68 Singla R, Singhal R, Rathore R. et al. Risk factors for chronic pulmonary aspergillosis in post-TB patients. Int J Tuberc Lung Dis 2021; 25 (04) 324-326
• 69 Nguyen NTB, Le Ngoc H, Nguyen NV. et al. Chronic pulmonary aspergillosis situation among post tuberculosis patients in Vietnam: an observational study. J Fungi (Basel) 2021; 7 (07) 7
• 70 Kwizera R, Katende A, Bongomin F, Nakiyingi L, Kirenga BJ. Misdiagnosis of chronic pulmonary aspergillosis as pulmonary tuberculosis at a tertiary care center in Uganda: a case series. J Med Case Rep 2021; 15 (01) 140
• 71 Denning DW, Pleuvry A, Cole DC. Global burden of chronic pulmonary aspergillosis as a sequel to pulmonary tuberculosis. Bull World Health Organ 2011; 89 (12) 864-872
• 72 Agarwal R, Denning DW, Chakrabarti A. Estimation of the burden of chronic and allergic pulmonary aspergillosis in India. PLoS One 2014; 9 (12) e114745
• 73 Denning DW, Cole DC, Ray A. New estimation of the prevalence of chronic pulmonary aspergillosis (CPA) related to pulmonary TB - a revised burden for India. IJID Reg 2022; 6: 7-14
• 74 Kwizera R, Parkes-Ratanshi R, Page ID. et al. Elevated Aspergillus-specific antibody levels among HIV infected Ugandans with pulmonary tuberculosis. BMC Pulm Med 2017; 17 (01) 149
• 75 Oladele RO, Irurhe NK, Foden P. et al. Chronic pulmonary aspergillosis as a cause of smear-negative TB and/or TB treatment failure in Nigerians. Int J Tuberc Lung Dis 2017; 21 (09) 1056-1061
• 76 Hedayati MT, Azimi Y, Droudinia A. et al. Prevalence of chronic pulmonary aspergillosis in patients with tuberculosis from Iran. Eur J Clin Microbiol Infect Dis 2015; 34 (09) 1759-1765
• 77 Salzer HJ, Heyckendorf J, Kalsdorf B, Rolling T, Lange C. Characterization of patients with chronic pulmonary aspergillosis according to the new ESCMID/ERS/ECMM and IDSA guidelines. Mycoses 2017; 60 (02) 136-142
• 78 Salzer HJF, Wang JY. Chronic pulmonary aspergillosis as a sequel to pulmonary TB. Int J Tuberc Lung Dis 2021; 25 (07) 519-520
• 79 Ngah V, Maud P, Baines N. et al. Respiratory presentations to acute services at a tertiary hospital in South Africa. S Afr Med J 2021; 111 (11) 1104-1109
• 80 Lakoh S, Kamara JB, Orefuwa E. et al. Prevalence and predictors of Aspergillus seropositivity and chronic pulmonary aspergillosis in an urban tertiary hospital in Sierra Leone: a cross-sectional study. PLoS Negl Trop Dis 2023; 17 (07) e0011284
• 81 Rozaliyani A, Setianingrum F, Azahra S. et al. Performance of LDBio Aspergillus WB and ICT antibody detection in chronic pulmonary aspergillosis. J Fungi (Basel) 2021; 7 (04) 7
• 82 Mohamed A, Obanda BA, Njeri HK. et al. Serological evidence of chronic pulmonary aspergillosis in tuberculosis patients in Kenya. BMC Infect Dis 2022; 22 (01) 798
• 83 Setianingrum F, Rozaliyani A, Syam R. et al. Evaluation and comparison of automated and manual ELISA for diagnosis of chronic pulmonary aspergillosis (CPA) in Indonesia. Diagn Microbiol Infect Dis 2020; 98 (03) 115124
• 84 Rozaliyani A, Rosianawati H, Handayani D. et al. Chronic pulmonary aspergillosis in post tuberculosis patients in Indonesia and the role of LDBio Aspergillus ICT as part of the diagnosis scheme. J Fungi (Basel) 2020; 6 (04) 6
• 85 Maitre T, Cottenet J, Godet C. et al. Chronic pulmonary aspergillosis: prevalence, favouring pulmonary diseases and prognosis. Eur Respir J 2021; 58 (02) 58
• 86 Godet C, Alastruey-Izquierdo A, Flick H. et al; CPAnet. A CPAnet consensus statement on research priorities for chronic pulmonary aspergillosis: a neglected fungal infection that requires attention. J Antimicrob Chemother 2018; 73 (02) 280-286
• 87 Denning DW, Page ID, Chakaya J. et al. Case definition of chronic pulmonary aspergillosis in resource-constrained settings. Emerg Infect Dis 2018; 24 (08) 24
• 88 Hou X, Zhang H, Kou L, Lv W, Lu J, Li J. Clinical features and diagnosis of chronic pulmonary aspergillosis in Chinese patients. Medicine (Baltimore) 2017; 96 (42) e8315
• 89 Salzer HJF, Lange C, Hönigl M. [Aspergillus in airway material : ignore or treat?]. Internist (Berl) 2017; 58 (11) 1150-1162
• 90 Salzer HJF, Prattes J, Flick H. et al. Evaluation of galactomannan testing, the Aspergillus-specific lateral-flow device test and levels of cytokines in bronchoalveolar lavage fluid for diagnosis of chronic pulmonary aspergillosis. Front Microbiol 2018; 9: 2223
• 91 Page ID, Baxter C, Hennequin C. et al. Receiver operating characteristic curve analysis of four Aspergillus-specific IgG assays for the diagnosis of chronic pulmonary aspergillosis. Diagn Microbiol Infect Dis 2018; 91 (01) 47-51
• 92 Salzer HJF, Reimann M, Oertel C. et al; CPAnet. Aspergillus-specific IgG antibodies for diagnosing chronic pulmonary aspergillosis compared to the reference standard. Clin Microbiol Infect 2023 ;7:S1198-743X(23)00416-0
• 93 Sehgal IS, Choudhary H, Dhooria S. et al. Diagnostic cut-off of Aspergillus fumigatus-specific IgG in the diagnosis of chronic pulmonary aspergillosis. Mycoses 2018; 61 (10) 770-776
• 94 Polverino E, Goeminne PC, McDonnell MJ. et al. European Respiratory Society guidelines for the management of adult bronchiectasis. Eur Respir J 2017; 50 (03) 50
• 95 Salzer HJ, Cornely OA. Awareness of predictors of mortality may help improve outcome in chronic pulmonary aspergillosis. Eur Respir J 2017; 49 (02) 49
• 96 Koyama K, Ohshima N, Suzuki J. et al. Recurrence of chronic pulmonary aspergillosis after discontinuation of maintenance treatment by antifungal triazoles. J Infect Chemother 2014; 20 (06) 375-379
• 97 Rodriguez-Goncer I, Harris C, Kosmidis C, Muldoon EG, Newton PJ, Denning DW. Assessment of posaconazole salvage therapy in chronic pulmonary aspergillosis using predefined response criteria. Int J Antimicrob Agents 2018; 52 (02) 258-264
• 98 Sehgal IS, Dhooria S, Muthu V, Prasad KT, Agarwal R. An overview of the available treatments for chronic cavitary pulmonary aspergillosis. Expert Rev Respir Med 2020; 14 (07) 715-727
• 99 Sehgal IS, Dhooria S, Muthu V. et al. Efficacy of 12-months oral itraconazole versus 6-months oral itraconazole to prevent relapses of chronic pulmonary aspergillosis: an open-label, randomised controlled trial in India. Lancet Infect Dis 2022; 22 (07) 1052-1061
• 100 Van Braeckel E, Page I, Davidsen JR. et al; CPAnet. Treatment outcome definitions in chronic pulmonary aspergillosis: a CPAnet consensus statement. Eur Respir J 2022; 59 (06) 59
• 101 Alastruey-Izquierdo A, Cadranel J, Flick H. et al; on behalf of CPAnet. Treatment of chronic pulmonary aspergillosis: current standards and future perspectives. Respiration 2018; 96 (02) 159-170
• 102 Bongomin F, Harris C, Hayes G, Kosmidis C, Denning DW. Twelve-month clinical outcomes of 206 patients with chronic pulmonary aspergillosis. PLoS One 2018; 13 (04) e0193732
• 103 Shu CC, Wei YF, Chen KH. et al. inhaled corticosteroids increase risk of nontuberculous mycobacterial lung disease: a nested case-control study and meta-analysis. J Infect Dis 2022; 225 (04) 627-636
• 104 Muñoz-Torrico M, Rendon A, Centis R. et al. Is there a rationale for pulmonary rehabilitation following successful chemotherapy for tuberculosis?. J Bras Pneumol 2016; 42 (05) 374-385
• 105 Lin H, Lin Y, Xiao L, Chen Y, Zeng X, Chang C. How do smoking status and smoking cessation efforts affect TB recurrence after successful completion of anti-TB treatment? A multicenter, prospective cohort study with a 7-year follow-up in China. Nicotine Tob Res 2021; 23 (12) 1995-2002