Association between Allergic Bronchopulmonary Aspergillosis and Tuberculosis: A Systematic Review of 397 cases in literature

doi:10.21203/rs.3.rs-2728729/v1

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Association between Allergic Bronchopulmonary Aspergillosis and Tuberculosis: A Systematic Review of 397 cases in literature

https://doi.org/10.21203/rs.3.rs-2728729/v1

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Introduction: Although allergic bronchopulmonary aspergillosis (ABPA) is classically described in asthma and cystic fibrosis, tuberculosis (TB) with post-tubercular cavitary lung disease has recently been considered a probable predisposing factor for development of ABPA. While association of chronic pulmonary aspergillosis in patients with structural lung disease post TB has been well elucidated, the association with ABPA has not been reviewed systematically and the literature is quite scarce.

Methods:

We systematically screened the available literature from PubMed, Embase, SCOPUS and Web of Science databases for studies reporting association between ABPA and TB from 2010 to present using appropriate search terms, including the development of ABPA and Aspergillus sensitization in patients with previous or concomitant TB or post-tubercular structural lung disease (PTLD).

Results: A total of 624 studies were identified from the initial search from the databases. After removal of duplicates (n = 213 results), 411 articles were chosen for review of abstracts. Out of these, 358 were removed after initial screening and eight were removed during final screening due to absence of adequate data on association of ABPA and TB. A total of 45 articles were included in the final systematic review of which, 21 were original articles and 24 were case reports. Four patterns of associations were described in a total of 397 patients: ABPA misdiagnosed as TB (51%), ABPA in patients with previous TB (22%), co-existent ABPA and TB (4%) and Aspergillus sensitization in patients with prior or active TB (23%). There was significant heterogeneity in terms of the criteria used for diagnosis of ABPA as well as in the diagnosis of pulmonary TB. The radiological patterns, treatment and outcomes were mostly reported for the overall population screened and not individually for patients who showed some form of ABPA-TB association. Central bronchiectasis (28%), mucoid-impaction/high-attenuation mucus/’glove and finger’ shadows (28%) and cavitary lesions (37%) were the most common radiographic abnormalities out of those whose individual radiological data could be extracted. Around 67% of the patients for whom treatment given were reported received steroids and/or antifungals. Adequate treatment response was reported for all the patients for whom it was reported.

Conclusion: ABPA may be associated with TB in numerous ways. Misdiagnosis of ABPA as TB is the most common pattern followed by the patterns of Aspergillus sensitization /ABPA developing in patients with history of TB. The least common pattern was the that of concomitant TB and ABPA. On account of lack of uniformity in diagnosing ABPA and TB – future well designed studies are required to confirm these associations.

Allergic bronchopulmonary aspergillosis

ABPA

aspergillus sensitization

post TB sequelae

post tubercular structural lung disease

The clinical spectrum of diseases due to Aspergillus varies depending on the host immune condition from invasive forms including angio-invasive and tissue-invasive pulmonary aspergillosis to allergic forms including allergic bronchopulmonary aspergillosis. [1][2] ABPA is characterized by a hypersensitivity reaction to the fungi Aspergillus fumigatus colonizing the airways, mainly in patients with asthma and cystic fibrosis.[3] Airway inflammation, along with bronchial obstruction and mucoid impaction in ABPA patients, can lead to permanent damage in the form of fibrosis, bronchiectasis etc. [4]

ABPA as a clinical entity was first described in 1952 in three patients presenting with recurrent wheezing, eosinophilia and pulmonary infiltrates. [5] The lack of specific clinical signs and symptoms and the lack of a reliable diagnostic test has historically resulted in significant underestimation of the disease burden. Over time, as the understanding of the pathophysiology and clinical characteristics of the disease improved, there was a recognition of the role of Aspergillus precipitins and serum immunoglobulin E in the diagnosis of ABPA. [6] [7] It was not until 1977 that diagnostic criteria were first proposed for the diagnosis of ABPA, when Rosenberg and Patterson described a set of seven primary and three secondary criteria for the diagnosis of ABPA.[8] Subsequently, modifications to the original criteria based on addition of A fumigatus-specific IgE and IgG and criteria for patients with cystic fibrosis as an underlying risk factor were proposed. [4][9] Most recently, the International Society for Human and Animal Mycology (ISHAM) proposed a new set of criteria clearly delineating predisposing factors and a set of obligatory as well as minor criteria for standardizing the diagnosis of ABPA uniformly. [10]

Outside of asthma and cystic fibrosis, ABPA has also been described in other conditions like chronic granulomatous diseases, bronchiectasis, lung transplant patients etc. [11][12] The recent International Society for Human and Animal Mycology (ISHAM) has mentioned post-tubercular fibro-cavitary disease as a possible predisposing condition for development of ABPA. [10][13] However, the evidence for post-TB pulmonary condition has not been well-characterized in literature.

Pulmonary TB and the resultant post-tubercular lung disease (PTLD) are known predisposing factors for chronic pulmonary aspergillosis (CPA) especially in endemic countries. [14][15] However, occurrence of the allergic manifestation of ABPA has not been as well elucidated, and no prior systematic review was identified which explored the association between ABPA and TB. As in cystic fibrosis, where there is a combination of abnormal muco-ciliary clearance, epithelial damage to the airways, trapping of Aspergillus spores in the viscid secretions etc, the milieu in the airways in patients afflicted with PTLD may be conducive to development of allergic sensitization and possible ABPA, which may be more likely in the backdrop of a genetic predisposition. [16][17] In this systematic review, we appraised the literature for describing the relationship of ABPA with PTB with the overarching goal of identifying cases of ABPA developing in PTLD patients.

We did a systematic review of the existing literature on association of ABPA and TB limited to the time period after 2010 without language restriction. We included all types of studies including case reports which evaluated ABPA including allergic sensitization to Aspergillus precipitins/antigens in patients with either past history of tuberculosis or active tuberculosis. An overview of the methodology adopted in our systematic review (SR) is shown in Fig. 1.

A systematic review of literature in PubMed, Embase, SCOPUS and Web of Science databases was conducted using appropriate search strings. Studies published from 2010 to present were included. We used MESH terms “allergic aspergilloses” and “bronchopulmonary” AND “tuberculosis” in PubMed, which retrieved 43 results. Applying the search terms “tuberculosis” AND (“lung” OR “pulmonary”) AND “aspergillus” AND (“allergy” OR “allergic”) on EMBASE retrieved 227 results. SCOPUS search using search terms ( “allergic” OR “allergy” ) AND ( “bronchopulmonary” OR “lung” OR “pulmonary” ) AND “aspergillosis” AND “tuberculosis” ) retrieved 236 results while using (“aspergillus” or “aspergillosis” or “mycosis” or “bronchopulmonary aspergillosis” or “bronchopulmonary mycosis”) AND (“allergy or allergic”) AND (“tuberculosis) on Web of science yielded 118 results, constituting a total of 624 results. After removal of duplicates (n = 213 results), 411 articles were screened for inclusion. Out of these, 358 were removed during summary removal. Out of the remaining 53, eight were removed during final screening and 45 articles were included in this systematic review (Supplementary appendix 1). Of these, 24 were case reports and rest of the 21 were descriptive or observational studies including one meta-analysis which included 11 studies. The geographic distribution of studies included in this systematic review is shown in Fig. 2.

The studies included as part of this review included descriptive studies, observational studies, case reports and a meta-analysis (Fig. 3a). The cases identified were grouped into four categories namely those where ABPA was 1. previously misdiagnosed as TB, 2. ABPA in patients with previous history of TB with or without PTLD, 3. concomitant ABPA-TB and 4. allergic sensitization to Aspergillus in patients with tuberculosis (vide Fig. 3b). A brief summary of all the studies and case reports included in this systematic review is provided in Supplementary appendix 1.

Overall, the most common pattern for the 397 patients included in the final analysis was ABPA misdiagnosed as TB (51%) followed by allergic sensitization to Aspergillus in patients with past or current tuberculosis (23%) and ABPA in previous tuberculosis (22%). Concomitant ABPA and TB was reported in 4% of cases (Fig. 3b). A detailed analysis of radiological features of patients with one of the patterns ABPA-tuberculosis alone was difficult, since most of the studies which evaluated the association have reported radiological features for the overall population screened. Of a total of 43 patients in groups 2,3,4 for whom radiological characteristics were reported, 12 (28%) had central bronchiectasis, mucoid-impaction/high-attenuation mucus/glove and finger shadows were seen in 12 (28%), consolidation/mass/nodule was seen in seven (16%), fungal ball in seven (16%) and cavitary lesions in 16 (37%). Of the specific subset of patients who developed ABPA after previous tuberculosis or with concomitant tuberculosis, treatment response was reported only for 12, ~ 67% of whom received steroids and antifungals. All 12 (100%) showed adequate clinical response with either steroids alone or with antifungals. As with radiological features, both treatment options and response rates were mostly reported only for the overall population included in the studies and the criteria for response used were variable.

ABPA misdiagnosed as tuberculosis

A total of 20 original articles (which dealt with the different manifestations of ABPA, including eight original studies, a meta-analysis which included 11 studies (18) and 11 case reports) reported the prevalence of ABPA in patients misdiagnosed previously as TB. The overall compiled data from these studies is shown in Table 1. As shown, out of a total of 625 patients with ABPA reported in these studies, 203 (32.5%) were previously misdiagnosed and treated as TB. While the criteria used for diagnosis of ABPA varied across the different studies, most of the cases of TB were presumptively treated likely on clinic-radiological basis and a definitive diagnostic criteria for diagnosis of TB is not mentioned for most of the included studies. Of the 19 studies and 11 case reports which studied this association, seven studies used ISHAM criteria for diagnosis of ABPA, Greenberger and Rosenberg-Patterson criteria were used in five and four studies respectively and three studies used either a clinical diagnosis of ABPA or did not report the exact criteria used for diagnosis. Only three case reports specified the criteria used for diagnosis of ABPA (two used Rosenberg Patterson while one used ISHAM criteria). None of these studies mentioned the criteria used for diagnosis of tuberculosis, which in most cases were likely to be clinic-radiological.

Table 1

ABPA misdiagnosed as tuberculosis
Total number of original articles = 9* (19 studies)
Case reports = 11
Total number of patients with ABPA = 625
Number misdiagnosed as tuberculosis (%) = 203/625 ( 32.5%)
	Observational studies (614 patients)	Case reports (11 patients)
1. Criteria for ABPA diagnosis used in included studies	(n = 19 studies **)	(n = 11 case reports)
ISHAM:	7	1
Rosenberg-Patterson:	4	2
Greenberger	5	0
NA/Clinical/Others:	3	8
2. Criteria for TB diagnosis in included studies	(n = 19 studies **)	(n = 11 case reports)
Clinico-radiological	0	4
AFB positive	0	0
NAAT	0	1
NA	19	6
*1 was a meta-analysis which included 11 studies
** Includes the studies reported in the meta-analysis

ABPA in patients with previous tuberculosis

A total of six original articles and ten case reports reporting ABPA in patients with previous TB were retrieved. Out of the total of 175 patients with ABPA, 88 (50.3%) had previous history of TB as shown in Table 2. 36.1% of patients with previous TB subsequently developed ABPA. Out of the 16 articles, a single article used the ISHAM criteria, two articles each used Greenberger and Rosenberg Patterson criteria for the diagnosis of ABPA and eleven articles (two studies and nine case reports) did not report the exact criteria used for diagnosis of ABPA. Only two articles (both case reports) reported the exact criteria used for diagnosis of tuberculosis in these patients as shown in Table 2. Radiological findings were reported individually for 25 patients with previous TB who developed ABPA, out of which ten (40%) had central bronchiectasis, while cavitary lesions were present in 16 (64%), mucoid-impaction/HAM/Glove and finger shadows in nine (36%), consolidation/mass/nodule in five (20%), and fungal ball in six (24%). Six out of the total ten patients for whom treatment was reported had received steroids, while seven received antifungals. Clinical outcomes were good for all these patients as shown in Table 2.

Table 2

ABPA diagnosed in patients with previous tuberculosis
Total number of observational studies = 6
Case reports = 10
Total number of patients with ABPA = 175
Total number of patients with previous TB = 244
Patients with ABPA and previous tuberculosis = 88
Previous tuberculosis in patients with ABPA (%) = 50.3% (88/175) ABPA in patients with previous tuberculosis = 36.1% (88/244)
1. Criteria for ABPA diagnosis	Observational studies (n = 6 studies)	Case reports (n = 10 case reports)
ISHAM:	1	0
Rosenberg-Patterson:	1	1
Greenberger	2	0
NA/Clinical :	2	9
2. Criteria for TB diagnosis	Observational studies (n = 6 studies)	Case reports (n = 10 case reports)
Clinico-radiological	0	1
AFB positive	0	1
NAAT	0	0
NA	6	8
3. Radiological features	Observational studies (n = 15 patients)	Case reports (n = 10 patients)
Central bronchiectasis	4	6
Cavitatory lesion	11	5
Mucoid-impaction/HAM/Glove and finger shadows	3	6
Fungal ball	6	-
Fleeting opacities/Patchy infiltrates		1
Consolidation/Mass/Nodule	0	5
4. Treatment		N = 10 patients
	Treatment specific to ABPA-Previous TB subgroup not reported	Systemic steroids + Antifungal = 5 Only antifungal = 2 Only steroid = 1 Omalizumab = 1 Thoracotomy = 1
5. Response		N = 10 patients
	Outcomes specific to ABPA-Previous TB subgroup not reported	All showed clinical improvement

Co-existent ABPA-TB

A total of six articles (three studies and three case reports) were retrieved which described co-existence of ABPA and active tuberculosis. Out of a total of 40 ABPA patients who were screened, 15 had concomitant ABPA and active tuberculosis as shown in Table 3. Of the six articles, ABPA was diagnosed using Greenberger, Rosenberg-Patterson and ISHAM criteria in one each while three either did not report the criteria used for diagnosis or used a clinical criteria for diagnosis of ABPA; tuberculosis was diagnosed microbiologically in three articles (all case reports) while the criteria was not mentioned in three articles. The radiographic features were only reported for three patients while treatment options used and outcomes were only reported for two patients as shown in Table 3.

Table 3

Co-Existent ABPA-TB
Total number of observational studies = 3
Case reports = 3
Total number of patients with ABPA = 40
Number with co-existent tuberculosis (%) = 15/40 (37.5%)
	Observational studies (n = 3 studies)	Case reports (n = 3 case reports)
1. Criteria for ABPA diagnosis
ISHAM:	0	1
Rosenberg-Patterson:	1	0
Greenberger	1	0
NA/Clinical :	1	2
2. Criteria for TB diagnosis	Observational studies (n = 3 studies)	Case reports (n = 3 case reports)
Clinico-radiological	0	0
AFB positive	0	2
NAAT	0	1
NA	3	0
3. Radiological features	Observational studies (n = 37 patients)	Case reports (n = 3 patients)
Central bronchiectasis	Not reported	1
Mucoid-impaction/HAM/Glove and finger shadows	Not reported	1
Pleuropulmonary fibrosis	Not reported	0
Fleeting opacities/Patchy infiltrates	Not reported	0
Consolidation/Mass/Nodule	Not reported	2
Miliary pattern with centrilobular nodules	Not reported	0
4. Treatment	Observational studies (n = 37 patients)	Case reports (n = 3 patients)*
4. Treatment	Not reported	ATT + Steroids + Antifungal = 1 ATT + Steroids = 1 Not reported = 1
5. Response	Observational studies (n = 37 patients)	Case reports (n = 3 patients)*
5. Response	Not reported	Both showed clinical improvement
*Reported only for two patients

Aspergillus sensitization in tuberculosis patients (concurrent or post-tubercular lung disease)

A total of four articles (including one which also reported the incidence of ABPA in patients with previous tuberculosis) evaluated the prevalence of Aspergillus sensitization in patients with either concurrent tuberculosis or post-tubercular structural lung disease. Of the 265 patients with past history of tuberculosis with or without structural lung disease, reported from three studies, 82 (31%) showed evidence of Aspergillus sensitization. The criteria used for defining Aspergillus sensitization are shown in Table 4. Only one study out of the three that assessed Aspergillus sensitization in patients with previous tuberculosis clearly reported the criteria used for diagnosis of tuberculosis, which was either microbiological or clinic-radiological with response to antitubercular therapy. Of the 16 patients with previous tuberculosis who developed Aspergillus sensitization for whom radiological features were described, central bronchiectasis, mucoid-impaction/HAM/Glove and finger shadows and fungal ball were each reported in one patient.

Table 4

*Aspergillus* sensitization in tuberculosis
Total number of observational studies = 4
Case reports = 0
Total number of patients with previous tuberculosis = 265
Aspergillus sensitization = 82/265 (31%)
Total number of patients with active tuberculosis = 101
Aspergillus sensitization = 9 (10%)*
1. Criteria for Aspergillus sensitization	Studies on patients with previous Tuberculosis (n = 3 studies)	Studies on patients with concurrent TB (n = 1 study)
Type I reaction to A. fumigatus antigen or an A. fumigatus-specific serum IgE level .0.35 kUA/l	1	-
A fumigatus-specific IgE > 0.35 kUA/L and IgG > 27 mgA/L	1	-
A fumigatus-specific IgE > 0.35 kUA/L	-	1
NA/Clinical :	1	0
2. Criteria for TB diagnosis	Studies on patients with previous Tuberculosis (n = 3 studies)	Studies on patients with concurrent TB (n = 1 study)
Microbiological/ Clinico-radiological with ATT response	1	-
Microbiological/ Clinico-radiogical	-	1 (93%/7%)
NA	2	0
3. Radiological features	Previous Tuberculosis (n = 16)**	Concurrent TB (n = 9 patients)
Central bronchiectasis	1	Not reported
Cavitatory lesion	-	Not reported
Mucoid-impaction/HAM/Glove and finger shadows	1	Not reported
Fungal ball	1	Not reported
Fleeting opacities/Patchy infiltrates	-	Not reported
Consolidation/Mass/Nodule	-	Not reported
Centrilobular nodules	-	Not reported
*9/93 (Only 93 had Aspergillus specific IgE evaluated)
** Reported only for 16 with Aspergillus sensitization

A single study reported the prevalence of Aspergillus sensitization in HIV-infected patients with active pulmonary tuberculosis diagnosed either microbiologically (93%) or clinico-radiologically (7%). This study showed a prevalence of 10% for Aspergillus sensitization, defined as Aspergillus fumigatus specific IgE > 0.35 kUA/L at the end of treatment duration of 24 months. The radiological features specific to the subgroup of patients with Aspergillus sensitization were not reported as shown in Table 4.

This systematic review, for the first time, evaluated the occurrence of ABPA in the background of PTLD. A total of 397 cases were identified in 24 case reports and 21 original articles. Three patterns of occurrence of ABPA were observed in the background of the PTB namely – co-existence of ABPA and TB, misdiagnosis of ABPA as TB ,and ABPA developing in patients having prior history of pulmonary TB, constituting a total of 306 patients. Out of this, ABPA misdiagnosed as TB was the most common, constituting 203 (51%) cases, followed by ABPA in patients with previous tuberculosis in 88 (22%); ABPA-TB co-existence was seen in 15 cases (4%) and Aspergillus sensitization in patients with prior or current tuberculosis constituted 23% of the association between ABPA/Aspergillus sensitization and tuberculosis. There were 82 cases (31.3%) of Aspergillus sensitization in 265 patients with either previous history of TB or those with PTLD while out of 101 patients with active tuberculosis, nine (10% of those assessed) showed evidence of Aspergillus sensitization.

Most of the cases diagnosed as tuberculosis were not microbiologically proven but were clinically-diagnosed tuberculosis. As per WHO data, 83% of total TB cases diagnosed globally in 2021 were attributed to pulmonary TB, of which 63% were bacteriologically confirmed, with considerable difference in the rate of confirmation in different parts of the world.[19] The general trend was of better rates of bacteriological confirmation in the high-income countries as compared to the low-income countries. [19] It has been known that a proportion of these cases, having other conditions, may be misdiagnosed as a case of pulmonary TB. [20] It seems plausible, that in a proportion of reported cases of ABPA after PTB, as seen in this review, may represent misdiagnosis of other conditions as PTB. However, some of these cases, had stigmata of previous infections with a compatible history of disease, imaging and clinician-reported response to anti-tubercular therapy. This further suggests that a subset of these cases may represent true cases of ABPA developing after pulmonary TB. As reported by a previous study from a TB-endemic setting, 32% of cases may have Aspergillus sensitization after history of pulmonary TB with suggestive fibro cavitary changes.[21] However, the significance of the sensitization could not be commented upon in the study, pending more evidence. The conglomeration of similar cases in other studies, as shown in this SR, further lays credence to the development of ABPA in PTLD patients.

Another aspect of the problem described is the possible overlap between ABPA and CPA, which may be common in patients with PTLD. [14] As described by a previous study, PTLD patients might exhibit features and satisfy criteria for both ABPA and CPA. This might be due to the different nature of inflammatory response (allergic i.e Th2 vs invasive i.e Th1) mounted by the host (immunocompetent vs mildly immunocompromised).[22] This possible relationship between CPA and ABPA, however, needs to be expounded further in large prospective studies.

The limitations of the present systematic review were inability to conclude on the reliability of diagnosis of TB in the absence of microbiological evidence in majority of cases especially for the group with past history of tuberculosis, wide heterogeneity in the diagnostic criteria used for ABPA (which might have led to variable accuracy of diagnosis) and inability to conduct a meta- analysis due to heterogeneity of type of studies (inclusion of case reports and series; wide variation in the methodologies; clinic-radiographic features reported, treatment modalities used and patient outcomes described).

However, the present systematic review nevertheless represents the first attempt to systematically deduce the relationship of ABPA with TB, as reported in the present literature. This review highlights several aspects of the association between TB and ABPA which needs to be rigorously examined: 1) What proportion of TB patients develop Aspergillus sensitization? 2) How many of those with sensitization develop ABPA? 3. Are there particular risk factors amongst PTLD (e.g fibrocavitary diseases) which have higher risk of developing ABPA 4. How to segregate and quantify the damages caused by PTLD and ABPA (e.g bronchiectasis due to PTLD vs ABPA) 5. Does the treatment strategy vary in these subset of patients? Future studies should systematically examine the relationship between ABPA and TB as well the questions posed above in well-designed studies.

The present systematic review demonstrates the potential relationship between PTB and ABPA, while highlighting the absence of well-designed studies evaluating the accurate relationship between the two diseases. Apart from misdiagnosis of cases of ABPA as pulmonary TB and their co-occurrence, it is likely that ABPA can develop in patients with PTLD, likely reflecting a predisposing role of PTLD in the development of ABPA. This is of particular importance especially for TB-endemic areas with high burden of both active tuberculosis and post-tubercular structural lung disease, which might serve as a primer for development of ABPA. Further, the lack of awareness and systematic screening for ABPA in these settings potentially leads to significant underestimation of the disease burden thereby impacting both treatment and long -term outcomes including pulmonary function, quality of life and mortality. There is thus a dire need of studies exploring this potential relationship in the future.

Compliance with ethical standards

Funding:

The authors declare that no funds, grants or other support were received for this systematic review and preparation of the manuscript.

Competing interests:

AA and AR have no relevant financial or non-financial interests to disclose.

MH reports grants and research funding from Astellas, Gilead, MSD, Pfizer, Euroimmun, F2G, Pulmocide, IMMY, Mundipharma and Scynexis.

Author contributions:

AR conceptualised the idea and design of this systematic review. AA and AR screened the databases for relevant literature, extracted articles relevant to the systematic review and screened the results for articles fulfilling requirements of the review. All included articles were screened by all three authors for relevant data extraction, compilation and analysis. All three authors were involved in the preparation of manuscript and give final approval for the manuscript being submitted.

Patient consent:

As this was a review of available published literature, this manuscript does not include factors requiring patient consent. In addition, as no patients were directly or indirectly involved in this review, no ethical clearance was deemed necessary.

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Association between Allergic Bronchopulmonary Aspergillosis and Tuberculosis: A Systematic Review of 397 cases in literature

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Abstract

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Introduction

Methods

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ABPA misdiagnosed as tuberculosis

ABPA in patients with previous tuberculosis

Co-existent ABPA-TB

Discussion

Conclusion

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References

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