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Abstract

Background:

Human cystic echinococcosis frequently involves the lungs, and colonization of a residual cavity with Aspergillus spores can lead to chronic pulmonary aspergillosis (CPA).

Objectives:

We pooled and characterized cases of CPA co-existing with pulmonary cystic echinococcosis (PCE) through a systematic review of globally published data.

Design:

Systematic review.

Data sources and methods:

Primary literature was identified through searches of various electronic databases, including CINAHL, Ovid MEDLINE, MEDLINE (PubMed), EMBASE, Google Scholar, the Cochrane Database of Systematic Reviews, and African Journal Online. The search encompassed articles from inception to February 2024, using medical subject heading search terms “chronic pulmonary aspergillosis” OR “Aspergillus” OR “aspergilloma” OR “aspergillosis” AND “hydatid disease” OR “hydatidosis” OR “echinococcosis” OR “Echinococcus.” Two reviewers independently assessed titles, abstracts, and full texts for eligibility using the Rayyan web-based software. The eligible studies comprised original observational research, single case reports, and case series that reported on CPA in patients with PCE based on established criteria (microbiological and/or radiological diagnosis of PCE) without language or geographic restrictions. Cochrane Risk of Bias Tools (ROB2 and ROBINS-I) were used to assess study quality and risk of bias, and the quality of the evidence was rated using the Grading of Recommendations, Assessment, Development, and Evaluations tool. The extracted data were summarized using descriptive statistics.

Results:

A total of 148 studies were initially identified from a literature search, and after the screening, 52 articles were selected for full-text review. We included 41 studies published from 1996 to 2023 that met the eligibility criteria and involved 3035 participants. The studies comprised case reports (75.6%, n = 31), case series (12.2%, n = 5), retrospective cohort studies (7.3%, n = 3), and one (2.4%) each of prospective cohort and cross-sectional study, respectively. More than two-thirds were conducted in India (36.6%, n = 15), followed by Turkey (14.6%, n = 6) and Iran (12.2%, n = 5). Among the 72 CPA cases, 50% were male, and 38.9% were female, with a median age of 38 years. Common comorbidities included pulmonary tuberculosis (n = 5) and diabetes mellitus (n = 3). The most frequent symptoms were cough (n = 32), hemoptysis (n = 21), and fever (n = 16). Radiological examinations were conducted in 74.4% of hydatid disease cases, while histological examinations were performed in 82.1% of aspergillosis cases. Cavitary lesions were noted in 21.4% of radiological findings. Treatment involved both surgical and medical management for 43.1% of patients, with antifungals (50%) and anthelminthic drugs (50%) commonly used. Surgical treatments included cystectomy (57.9%) and lobectomy (55.3%). All patients with reported outcomes were cured.

Conclusion:

CPA complicates PCE and has both similar clinical and radiological features. Diagnostic approaches primarily include radiology and histology, while treatment often involves a combination of surgical and medical management, with antifungals and anthelminthic drugs commonly used. Despite the complexity of CPA, patients generally achieve favorable outcomes with appropriate treatment. Further research is needed to optimize diagnostic and therapeutic strategies for this condition.

Trial registration:

PROSPERO (CRD42024510441).

Plain language summary

When lung infections overlap: how a parasitic disease can lead to fungal lung infection

This study looks at how two lung diseases, cystic echinococcosis and chronic pulmonary aspergillosis (CPA), can happen together. Cystic echinococcosis is caused by a parasite and can lead to cysts in the lungs. Sometimes, these cysts can become infected with a type of fungus called Aspergillus, leading to CPA. This infection can cause symptoms like coughing, coughing up blood, and fever, and can make it harder for people to breathe. To understand how often this happens and what treatments work best, we reviewed 41 studies from around the world that included 3,035 patients. Most of the studies came from India, Turkey, and Iran. In total, 72 people with cystic echinococcosis also had CPA. These patients were mostly middle-aged, and half of them were men. Many also had other lung diseases like tuberculosis. Doctors used imaging scans and tissue samples to diagnose both conditions. Treatment often involved a combination of surgery and medicine. The most common surgeries were to remove cysts or parts of the lung, while medications included antifungal drugs and treatments to kill the parasite. The good news is that all patients who received proper treatment recovered. This research shows that while CPA can complicate lung disease caused by parasites, it can be effectively managed if diagnosed early and treated properly. More research is needed to improve ways to find and treat these overlapping lung infections.

Keywords

chronic pulmonary aspergillosis echinococcosis echinococcus hydatid disease hydatidurias

Introduction

Echinococcosis is a rare parasitic zoonosis caused by the larval stages of taeniid cestodes within the genus Echinococcus. Echinococcosis is a neglected tropical disease that occurs in two main forms, cystic echinococcosis (also known as hydatiduria) and alveolar echinococcosis, caused by the tapeworms Echinococcus granulosus and E. multilocularis, respectively.^1–3 The World Health Organization (WHO) estimates that more than 1 million people are affected with echinococcosis at any one time, with human cystic echinococcosis (HCE) being the most common form globally.⁴ The incidence rates for HCE can reach more than 50 per 100,000 person-years, and prevalence levels as high as 5%–10% may occur in parts of Argentina, Peru, East Africa, Central Asia, and China.⁴ A recent analysis of its global burden suggests that the number of HCE cases had increased from 134,980 in 1990 to 207,368 in 2019.⁵

Primary HCE typically involves a solitary cyst; however, multiple cysts or multiple organ involvement have also been reported, with the liver being the most common site for echinococcal cysts in pastoral strains (>65%), followed by the lungs (25%).^6,7 Patients with pulmonary cystic echinococcosis (PCE) remain asymptomatic for years until the hydatid cysts grow to a significant size, triggering symptoms such as chronic cough, chest pain, shortness of breath, and eventually hemoptysis, which often results from rupture of large intraparenchymal or pleural cysts.^4,7

Overall mortality in HCE ranges from 2% to 5% with adequate treatment.^2,8 However, in patients with PCE, superinfections or co-infections are common and contribute significantly to overall mortality.⁹ Co-existent infections occur in up to about 30% of patients initially presenting with PCE, with a mortality rate of about 6%.⁹ Saprophytic colonization of cystic or residual cavitary lesions with Aspergillus spores following PCE or surgical interventions is a rare complication.^10–16 This results in chronic pulmonary aspergillosis (CPA)—a progressive parenchymal disease that often occurs in patients with existing structural lung diseases, such as pulmonary tuberculosis.¹⁷ From recent estimates, the annual incidence of CPA is about 1.8 million cases, with 340,000 (18.5%) deaths.¹⁸

A large retrospective cohort study from Turkey of 100 patients with PCE found CPA in 2% of cases.¹⁰ Similarly, in a systematic review of 1247 cases of CPA from Africa, 19 (1.5%) had CPA as a complication of PCE.¹⁹ Thus, PCE is an underappreciated underlying disease that leads to the development of CPA, warranting a detailed review. Moreover, PCE and CPA have overlapping symptoms; therefore, underdiagnosis is common. In this systematic review, we aimed to pool and characterize cases of CPA complicating PCE by systematically reviewing globally published data to address these gaps, with the overarching goal of reducing morbidity from this seemingly neglected disease.

Methods and materials

Study design

We conducted a systematic review of literature following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.²⁰ The PRISMA checklist is provided as Supplemental File 1.

Inclusion criteria

Patient/Population (P)

Individuals with CPA and pulmonary echinococcosis.

Exposure (E)

Aspergillus and cystic lung lesions.

Outcome (O)

Clinical outcomes, including treatment types, vital statistics, and clinical manifestations.

Study design (S)

Case reports, case series, cross-sectional studies, cohort and retrospective studies, randomized clinical trials.

Data sources

Electronic databases searched included Medline (through PubMed), Scopus, Embase, Google Scholar, Web of Science, and African Journal Online (AJOL).

Search strategy

A qualified medical librarian (BM) conducted a detailed database search using the keywords and medical subject headings (MeSH) “chronic pulmonary aspergillosis” OR “Aspergillus” OR “aspergilloma” OR “aspergillosis” AND “hydatid disease” OR “hydatidosis” OR “echinococcosis” OR “Echinococcus”. No language restriction or year of publication was applied.

Inclusion criteria

We included single case reports, case series, and cohort studies, including cases of CPA in patients with microbiologically or radiologically confirmed PCE of all ages and sexes across the world. There were no language restrictions. CPA was defined as a spectrum of pulmonary disorders caused by Aspergillus species, characterized by one or more pulmonary cavities, with or without a fungal ball, associated with chronic respiratory symptoms lasting 3 months or more (e.g., cough, hemoptysis, fatigue, or weight loss), and confirmed by radiological findings and/or serological evidence of Aspergillus infection. PCE was defined as a parasitic infection of the lungs caused by the larval stage of Echinococcus species, presenting radiologically as one or more pulmonary cysts, which may be asymptomatic or associated with respiratory symptoms such as cough, chest pain, hemoptysis, or dyspnea, and confirmed by imaging and/or serological tests for echinococcal antibodies. Studies were eligible for inclusion if they explicitly reported diagnostic criteria or case definitions meeting these operational definitions.

Exclusion criteria

We excluded review articles and extrapulmonary cases.

Selection process

Two sets of independent reviewers (RO and PB, and AA and FB) conducted the initial screening of titles and abstracts, focusing on studies related to CPA and pulmonary echinococcosis co-infection. Full-text assessment was performed for selected articles. Discrepancies in inclusion/exclusion decisions were resolved through discussion or consultation with a third reviewer (FB or AA). Non-English abstracts were translated using Google Translate or DeepL.

Data extraction

A standardized data extraction form was developed by FB and AA and pilot-tested by PB and RO. Extracted data encompassed study characteristics, country, sample size, modes of diagnosis of CPA and echinococcosis, clinical manifestation, treatment for both diseases, including medical and surgical, and clinical outcomes. Data extraction was independently conducted by five reviewers (RO, PB, AA, BEE, and FB), and any discrepancies were discussed with and resolved by agreement of at least three authors.

Data analysis

We conducted a narrative synthesis using Microsoft Excel, summarizing key information on CPA diagnosis, echinococcosis diagnosis, clinical manifestation, treatment, and treatment outcomes using frequencies and percentages. No meta-analysis or subgroup analyses were conducted.

Ethical considerations

As the review involves the analysis of publicly available, previously published studies, ethical approval is not applicable.

Results

Study characteristics

A total of 148 studies were found in the initial literature search, and an additional four via citation searching. After removing three duplicates and screening the title and abstract, 97 studies were excluded, leaving 51 articles for full-text screening. Ten were excluded because they were reviews or editorials without primary case data (n = 4), reported duplicate patient populations (n = 1), or lacked sufficient clinical detail to confirm CPA complicating PCE (n = 5). Eventually, 41 studies conducted between 1996 and 2023 involving 3035 participants were included (Figure 1). The studies comprised case reports (75.6%, n = 31), case series (12.2%, n = 5), retrospective cohort studies (7.3%, n = 3), and one (2.4%) each of prospective cohort and cross-sectional study, respectively. More than two-thirds were conducted in India (36.6%, n = 15), followed by Turkey (14.6%, n = 6) and Iran (12.2%, n = 5), Figure 2.

Figure 1.

A PRISMA flow diagram showing the selection of articles for the systematic review.

Figure 2.

World map showing cases of co-infections with hydatid cysts and aspergillosis.

Characteristics of the patients

There were 74 cases of CPA as a complication of PCE reported in the included studies ( Table 1 ). Sex was specified in 38 studies, involving 66 participants, of whom more than half were male (56.1%, n = 37). The median age was 37.0 years (range: 3.5–62; interquartile range: 27.5–51.0 years). Pulmonary tuberculosis (n = 5, 6.8%), diabetes mellitus (n = 3, 4.1%), acute leukemia (n = 2, 2.7%), hyperthyroidism (n = 1, 1.4%), and asthma (n = 1, 1.4%) were reported comorbidities. In four patients whose risk factors were noted, contact with domestic animals (n = 3) was the most frequent, followed by smoking in one individual.

Table 1.

Characteristics of included studies and the study participants.

Study ID	Year	Study design	Study period	Population	Sample size	Country	Number of Cases	Age	M	F	DM	PTB	Acute leukemia	Asthma	Hyperthyroidism	Risk factors
Agrawal²¹	2024	Case report	2023	—	1	India	1	23	1	0	0	0	0	0	0	—
Adhikari¹¹	2023	Case report	2023	—	1	Nepal	1	30	0	1	0	0	0	0	0	—
Shahriarirad²²	2023	Cross-sectional study	2004 to 2018	Patients with echinococcosis.	501	Iran	4	30; 36; 55; 58	2	2	0	0	0	0	0	—
Ayadi¹³	2023	Case series	2004–2022	—	8	Tunisia	8	41.57	5	3	0	0	0	0	0	—
Verma²³	2022	Case report	2022	—	1	India	1	53	0	1	0	1	0	0	0	—
Çay²⁴	2022	Case report	2022	—	1	Turkey	1	3.5	0	1	0	0	1	0	0	—
Sharma²⁵	2021	Case report	2021	—	1	India	1	20	1	0	0	1	0	0	0	—
Aboksari²⁶	2020	Case report	2020	—	1	Iran	1	10	1	0	0	0	0	0	0	—
Zareshahrabadi²⁷	2020	Case report	2020	—	1	Iran	1	42	1	0	0	0	0	0	0	Contact with domestic animals.
Goyal²⁸	2019	Case report	2017	—	1	India	1	45	1	0	0	0	0	0	0	—
Collado-Aliaga⁹	2019	Cohort study	2019 (1998 to 2017)	Patients with cystic echinococcosis	594	Spain	3				0	0	0	0	0	—
Castillo-Minaya²⁹	2018	Case report	2018	—	1	Peru	1	33	0	1	0	0	0	0	0	—
Aala³⁰	2017	Case report	2017	—	1	Iran	1	34	0	1	0	0	0	0	1	—
Emiralioglu³¹	2017	Case report	2017	—	1	Turkey	1	14	0	1	0	0	0	0	0	—
Chopra³²	2017	Case report	2010	—	1	India	1	43	1	0	0	0	0	0	0	—
Nayak³³	2016	Case report	2015	—	1	India	1	36	0	1	0	0	0	0	0	—
Mishra¹⁶	2015	Case report	2012	—	1	India	1	43	1	0	0	0	0	0	0	—
Yazgan³⁴	2015	Case report	2015	—	1	Turkey	1	24	0	1	0	0	0	0	0	—
Agarwal³⁵	2013	Case report	2013	—	1	India	1	45	0	1	0	0	0	0	0	—
Agrawal³⁶	2013	Case report	2013	—	1	India	1	52	1	0	0	0	0	0	0	—
Pandey³⁷	2013	Case report	2013	—	1	India	1	60	0	1	0	0	0	0	0	Shepherd community.
Tiwari³⁸	2013	Case report	2013	—	1	India	1	44	1	0	0	0	0	0	0	—
El Hammoumi³⁹	2013	Case series	2012		3	Morocco	3	35; 56; 52	3	0	0	1	0	0	0	—
Fifer⁴⁰	2012	Case report	2012	—	1	United Kingdom	1	21	0	1	0	0	0	0	0	—
Mahmood¹²	2011	Case report	2011	—	1	USA	1	27	1	0	0	0	0	0	0	Farm worker.
Gürel⁴¹	2011	Case report	2011	—	1	Turkey	1	36	1	0	0	0	0	1	0	—
Grigoriyan⁴²	2010	Case report	2010	—	1	USA	1	62	0	1	0	0	0	0	0	—
M’saad⁴³	2010	Case series	2009	—	2	Tunisia	2	52; 56	1	1	0	0	0	0	0	Smoking (1)
Vaideeswar⁴⁴	2010	Case series	2009	—	2	India	2	36, 25	2	0	0	0	0	0	0	—
García⁴⁵	2010	Retrospective observational study	1996–2007	Patients with echinococcosis.	503	Spain	3				0	0	0	0	0	—
Nasrollah⁴⁶	2009	Case report	2009	—	1	-Iran	1	28	1	0	0	0	0	0	0	—
Nabi⁴⁷	2009	Case report	2009	—	1	Pakistan	1	50	1	0	1	1	0	0	0	—
Deshmukh⁴⁸	2009	Retrospective observational study	2002 to 2008	Patients undergoing flexible bronchoscopy.	1204	India	14		7	7	0	0	0	0	0	—
Manzoor⁴⁹	2008	Case report	2007	—	1	Pakistan	1	40	1	0	0	0	0	0	0	—
Vasquez⁵⁰	2008	Case series	2007	—	2	USA	2	42;41	1	1	1	1	0	0	0	—
Koçer¹⁰	2008	Retrospective observational study	1999 to 2004	Hematoxylin–eosin-stained sections with a diagnosis of hydatid cysts.	100	Turkey	2				0	0	0	0	0	—
Aydemir^15,51	2006	Case report	2006	—	1	Turkey	1	32	0	1	0	0	0	0	0	—
Gupta¹⁵	2006	Case report	2006	—	1	India	1	53	1	0	1	0	0	0	0	—
Bal⁵²	2008	Case report	2008	1	India	1	52	0	1	—	—	—	—	—	—	—
Pan⁵³	2013	Case report	2012	1	China	1	15	1	0	—	—	—	—	—	—	—

DM, diabetes mellitus; F, Female; M, Male; PTB, pulmonary tuberculosis.

Clinical presentation

Cough (n = 34; 45.9%) with hemoptysis (n = 23; 31.1%), fever (n = 17; 23.0%), and chest pain (n = 14; 18.9%) were the most frequent symptoms. The duration of symptoms at diagnosis ranged from 2 weeks to 3 years. The most frequently reported clinical sign was decreased breath sounds, reported in nine studies (Table 2).

Table 2.

Clinical presentation.

Study ID	Year	Cough	Hemoptysis	Chest pain	Fever	Weight loss	Dyspnea	Night sweats	Bronchorrhea	Duration of symptoms	Significant clinical findings
Agrawal²¹	2024	0	0	0	0	0	0	0	0	2 months
Adhikari¹¹	2023	1	1	1	0	0	0	0	0	3 years	Decreased breath sounds.
Shahriarirad²²	2023	4	2	0	2	0	1	0	1
Ayadi¹³	2023	0	0	0	0	0	0	0	0
Verma²³	2022	1	1	0	1	0	0	1	0
Çay²⁴	2022	0	0	0	0	0	0	0	0
Sharma²⁵	2021	1	1	0	0	0	0	0	0
Aboksari²⁶	2020	1	0	0	1	0	0	0	0	3 months	Mild leucocytosis.
Zareshahrabadi²⁷	2020	0	0	0	0	0	0	0	0
Goyal²⁸	2019	1	1	0	1	0	0	0	0	2 weeks
Collado-Aliaga⁹	2019	0	0	0	0	0	0	0	0
Castillo-Minaya²⁹	2018	0	0	1	1	0	0	0	0		Decreased breath sounds, cloudy chest tube discharge.
Aala³⁰	2017	1	0	1	0	0	0	0	0		Relatively normal.
Emiralioglu³¹	2017	1	1	0	0	0	0	0	0		Decreased breath sounds, elevated C-reactive protein (CRP) and erythrocyte sedimentation rate (ESR).
Chopra³²	2017	1	1	1	1	1	0	0	0	4 months
Nayak³³	2016	1	1	0	0	0	0	0	0	3 months
Mishra¹⁶	2015	1	1	1	1	1	0	0	0
Yazgan³⁴	2015	1	0	0	0	0	0	0	0	1 month
Agarwal³⁵	2013	1	1	0	1	0	0	0	0		Decreased breath sounds, chest movements, and dull percussion notes.
Agrawal³⁶	2013	1	0	0	0	1	0	0	0	4 months	Decreased breath sounds.
Pandey³⁷	2013	1	0	1	0	0	0	0	0	6 months	Hydropneumothorax.
Tiwari³⁸	2013	1	1	1	0	0	0	0	0
El Hammoumi³⁹	2013	1	1	0	0	0	0	0	0
Fifer⁴⁰	2012	1	0	1	1	0	0	0	0
Mahmood¹²	2011	1	0	1	1	0	0	0	0	3 months	Mild clubbing, bronchial breath sounds, and impaired percussion note.
Gürel⁴¹	2011	1	1	0	0	0	0	0	0	1 year	Mild anemia.
Grigoriyan⁴²	2010	1	1	0	1	0	0	0	0
M’saad⁴³	2010	1	1	1	0	1	0	1	0	2 years	Pallor and decreased breath sounds.
Vaideeswar⁴⁴	2010	1	1	1	0	0	0	0	0
García⁴⁵	2010	0	0	0	0	0	0	0	0
Nasrollah⁴⁶	2009	0	0	0	0	0	1	0	0
Nabi⁴⁷	2009	0	0	0	1	0	0	1	0		Bronchial breath sounds with coarse crepitations.
Deshmukh⁴⁸	2009	1	1	1	0	0	0	0	0
Manzoor⁴⁹	2008	1	0	0	1	0	0	0	0	3 months	Mild anemia.
Vasquez⁵⁰	2008	1	1	0	0	0	0	0	0
Koçer¹⁰	2008	1	1	1	1	0	0	0	0
Aydemir^15,51	2006	1	0	0	0	0	0	0	0		Decreased breath sounds.
Gupta¹⁵	2006	1	1	0	1	0	0	0	0	3 months
Bal⁵²	2008	1	1	1	0	0	1	0	0	5 days
Pan⁵³	2013	1	1	0	1	0	0	0	0	1 month

Diagnostic evaluation

Regarding hydatid disease, chest imaging was the most common investigation performed in 31 studies (73.8%), followed by histology (64.3%, n = 27), serology (14.3%, n = 6), and microbiology (4.8%, n = 2). For aspergillosis, histology was most often performed (81.0%, n = 34), followed by radiology (28.6%, n = 12), microbiology (19.0%, n = 8), and serology (4.8%, n = 2; Figure 3).

Figure 3.

Bar charts showing the diagnostic methods used for echinococcosis and aspergillosis.

Microbiology and serology

In 17 studies reporting microbiological findings, sputum microscopy revealed Echinococcus granulosus in only one study,⁴⁰ while positive indirect hemagglutination was used to identify it in one study.⁵¹ For the majority (88.2%, n = 15), sputum microscopy and culture did not reveal any significant findings related to E. granulosus. Aspergillus spp. was also identified in sputum cultures in only seven studies.^{12,30,35,40,44,47,52} None of the studies reported positive acid-fast bacilli findings or Mycobacterium tuberculosis.

Serological findings were reported for eight cases in seven studies. One case showed an intermediate-strength purified protein derivative (PPD) skin test with 15 mm induration.¹² Hydatid serology, using a specific anti-Echinococcus IgG enzyme-linked immunosorbent assay, was positive in three studies.^12,40,52,53 Repeat Aspergillus serology in one of these cases was positive, with ImmunoCAP showing 195 mgA/L and a significantly raised serum IgE of 1503 kIU/L (reference range: 0–100).⁴⁰ Aspergillus-specific IgE was positive in a different case, with normal Aspergillus galactomannan levels.³¹ Positive serological tests for Aspergillus and indirect hemagglutination for E. granulosus were also reported in another patient.⁴³ Additionally, one case confirmed the presence of Aspergillus flavus species by molecular assay.³⁰ However, elevated Aspergillus IgE levels are not diagnostic for CPA.

Histology

Histological findings from 34 studies involving 59 participants revealed a range of characteristics associated with co-infection with Echinococcus and aspergillosis. In 21 studies (61.8%) of the 34 with histological findings, cyst walls were infiltrated by fungal hyphae.^{11,13,16,21,24,26,27,30,31,33–37,41–44,47,52} Other common observations included cavities^{16,32,37,39,40,44,50,51} containing aspergilloma^{16,29,32,37,42,50,51} and chronic organized pneumonia.^16,41,49,51 Polymorphs and histiocytes with fragments of Echinococcus and Aspergillus were sometimes found in smears.^15,41 Seven studies showed laminated membranes of hydatid cysts,^{11,13,21,35,37,40,43} with Echinococcus hooklets in four studies,^15,35,40,47 and septate fungal hyphae in nine studies,^{11,13,27,31,35,37,53} sometimes confirmed by periodic acid-Schiff^{11,13,27,31,35,37,53} and Grocott’s methenamine silver staining.³⁵ Chronic inflammatory changes in the surrounding lung parenchyma were frequently observed,^{28,32,42,47,53} and necrotic lung tissue was common.^31,38,40 The presence of mixed inflammatory cells,^{21,26,30,31,37} fibroblastic proliferation,^31,51 and vascular infiltration,³¹ in response to fungal invasion, was also a notable finding.

Radiological findings

Radiological findings from the 36 studies with available results showed that 14 out of 58 cases (24.1%) had cavitary lesions with air-fluid levels (n = 6, 10.3%). Chest X-rays revealed oval or round densities in 10 cases (17.9%), while thoracic CT scans detailed cavitating lesions, pneumonic infiltration, and residual cavities with collapsed membranes in 15 cases (26.8%). Air crescent signs suggestive of aspergilloma were noted in 8 cases (13.8%), and fine curvilinear membranes indicating hydatid cysts were present in 2 cases (3.4%).^35,49 Additional findings included thick-walled cavities near the hilum in 3 cases (5.2%),^28,30,47 cystic lesions in 9 cases (15.5%),^{11,27–30,34–36,52} and significant consolidation in 11 cases (19.0%).^{16,30,32,35,38,40,48} Complex cysts often ruptured and contained air or mass-like opacities,^25,26 and necrotic lesions showing intense enhancement were also reported.^31,41

Bronchoscopy

Bronchoscopy findings were present in seven studies involving 21 patients co-infected with hydatid cysts and aspergillosis.^{10,12,26,32,47,48,53} In one case, fresh blood and necrotic material were observed coming from the superior segment of the right lower lobe.⁴⁷ Inflammation and secretions were noted in the left lung during bronchoscopic examination, with no fistula found in another case.^12,32 One case reported no abnormalities.³² In another study, a separate tissue cut section exhibited a fibrous wall containing necrotic material and dichotomous branching septate fungal hyphae admixed with neutrophilic infiltration.²⁶ During bronchoscopy, hemorrhagic lesions were found in the upper right lobe, and Serratia was identified in one case.¹⁰ Findings in multiple cases included a white glistening membrane resembling tender coconut, pathognomonic for cystic hydatidosis (n = 9, 42.9%), and mucoid secretions (n = 3, 14.3%).⁴⁸

Management and clinical outcomes

Thirty-three patients (44.6%) received both surgical and medical management, while one patient received medical management only²⁵ and seven received surgical management only,^{13,16,27,35,43,46,49} Table 3. Of the 32 cases that received at least one form of medical management, 18 (52.9%) received anthelminthic drugs (albendazole), 16 (50.0%) received antifungals, and 7 (21.9%) received antibiotics. Only 7 (21.9%) patients received both antifungals and anthelminthic drugs. Itraconazole (n = 12) and voriconazole (n = 2) were the only antifungals used. Of the 40 cases (54.1%) who received surgical treatment, cystectomy (57.5%, n = 23), lobectomy (55.0%, n = 22), and capitonnage (27.5%, n = 11) were the most performed procedures (Figure 4). Abscess and hemorrhage were reported as postoperative complications in one patient each.

Table 3.

Management and clinical outcomes.

Study ID	Year	Medical management	Surgery	Specific medical management	Specific surgical management	Complications	Clinical outcomes
Agrawal²¹	2024	1	1	Oral albendazole 10 mg/kg/day for 3 months	Cystectomy		Cured
Adhikari¹¹	2023	1	1	Oral albendazole 10–15 mg/kg/day postoperative.	Cystectomy and capitonnage		Cured
Shahriarirad²²	2023	4	4	Albendazole, metronidazole, clindamycin, ceftriaxone, ciprofloxacin	Lobectomy, resection, mediastinal lymphadenectomy, segmentectomy		Cured
Ayadi¹³	2023	0	1		Resection		No outcome available
Verma²³	2022	0	0				No outcome available
Çay²⁴	2022	1	1	Albendazole 15 mg/kg/day for 41 months, voriconazole 8 mg/kg/dose bd for 16 months	Partial cystectomy		No outcome available
Sharma²⁵	2021	1	0	Oral itraconazole (200 mg bd) for 1 month; albendazole 10 mg/kg/day for 12 months.			No outcome available
Aboksari²⁶	2020	1	1	Albendazole 15 mg/kg/day for 4 weeks.	Capitonnage		Cured
Zareshahrabadi²⁷	2020	0	1		Lobectomy		No outcome available
Goyal²⁸	2019	1	1	Oral itraconazole 400 mg; albendazole 800 mg.	Lobectomy		No outcome available
Collado-Aliaga⁹	2019	1	1				No outcome available
Castillo-Minaya²⁹	2018	1	1	Albendazole 200 mg 12 hourly	Lobectomy		Cured
Aala³⁰	2017	1	1	Albendazole (10 mg/kg/day); oral itraconazole (200 mg/day) for 3 months)	Thoracotomy		Cured
Emiralioglu³¹	2017	1	1	IV voriconazole at 8 mg/kg/day and oral voriconazole on discharge.	Cystectomy		No outcome available
Chopra³²	2017	1	1	Anti-tuberculosis therapy (ATT) for 6 months.	Bronchial artery embolization; Lobectomy.		Cured
Nayak³³	2016	1	1	Antifungal and anti-helminthic agents	Lobectomy		No outcome available
Mishra¹⁶	2015	0	1		BAE and lobectomy		No outcome available
Yazgan³⁴	2015	1	1		Cystectomy and capitonnage		Cured
Agarwal³⁵	2013	0	1		Cystectomy		Cured
Agrawal³⁶	2013	1	1	Albendazole 10 mg/kg/day for 3 months.	Cystectomy		No outcome available
Pandey³⁷	2013	1	1	Itraconazole 100 mg/day for 3 months.	Cystectomy		Cured
Tiwari³⁸	2013	1	1	Albendazole 400 mg twice a day (BD).	BAE and lobectomy		Cured
El Hammoumi³⁹	2013	1	1	Itraconazole 100 mg/day for 3 months.	Cystectomy and capitonnage in 2, cystectomy in one.		Cured
Fifer⁴⁰	2012	1	1	Post-op oral itraconazole 200 mg bd.	Lobectomy and cystectomy.		No outcome available
Mahmood¹²	2011	1	1	Clindamycin 600 mg three times a day (TDS) for 10 days with no response.	Lobectomy		Cured
Gürel⁴¹	2011	1	1	Antifungals (not specified).	Cystectomy and capitonnage		No outcome available
Grigoriyan⁴²	2010	1	1		Open-lung biopsy		No outcome available
M’saad⁴³	2010	0	1		Lobectomy; wedge resection	Abscess (1) hemorrhage (1)	No outcome available
Vaideeswar⁴⁴	2010	2	2	Itraconazole.	Cystectomy and capitonnage (1); lobectomy (1)		No outcome available
García⁴⁵	2010	0	0				No outcome available
Nasrollah⁴⁶	2009	0	1		Capitonage		No outcome available
Nabi⁴⁷	2009	1	1	Albendazole; Itraconazole.	Wedge resection		Cured
Deshmukh⁴⁸	2009	1	1		Lobectomy (9); cystectomy (2); pneumonectomy (1).		Cured
Manzoor⁴⁹	2008	0	1		Wedge resection		No outcome available
Vasquez⁵⁰	2008	1	1	Itraconazole 100 mg/day.	Cystectomy±capitonnage (2); Pneumonectomy (1).		No outcome available
Koçer¹⁰	2008	1	1	Albendazole with no response.	Cystectomy and capitonnage (2)		No outcome available
Aydemir^15,51	2006	1	1	Albendazole 10 mg/kg; itraconazole (200 mg/day).	Cystectomy and wedge resection.		No outcome available
Gupta¹⁵	2006	0	0				No outcome available
Bal⁵²	2008	1	1	Albendazole therapy	Cystectomy	—	Cured
Pan⁵³	2013	1	1	Albendazole therapy	Lobectomy	—	No outcome available

BAE, bronchial artery embolization.

Figure 4.

Procedures performed in the management of chronic pulmonary aspergillosis complicating pulmonary cystic echinococcosis.

Discussion

This systematic review reports the co-existence of 74 cases of CPA as a complication of PCE. Although PCE is globally distributed, reports of cases with Aspergillus co-infection were confined to a limited number of countries, including India and Pakistan in Asia; Iran, Tunisia, and Morocco in the Middle East and North Africa; Spain and Turkey in Europe; and Peru in South America. The higher case burdens observed in these countries could be due to better case reporting, improved diagnostic capabilities, and the high endemicity of echinococcosis and TB. The review did not reveal any predilection for the female sex or immune compromise as sometimes asserted by some authors.¹¹ In most studies, aspergillosis was diagnosed incidentally by histology, suggesting that clinical suspicion was often low.

The patchy distribution of CPA and PCE co-infection is not surprising. Cystic echinococcosis is a neglected tropical disease that receives little funding for research and treatment relative to its burden of disease. It is, therefore, underdiagnosed. To illustrate, the disease is considered endemic in sub-Saharan Africa, but only scarce data, if any, exist for most countries.⁵⁴ The rarity of reports of CPA and PCE co-infection may, therefore, in part be attributed to the neglected status of hydatid disease.

PCE is typically asymptomatic in the early stages. As cysts become larger or more complex, symptoms may develop and vary depending on size, location, compression of nearby structures, and the condition of the cystic structures.¹¹ From our review, cough, fever, hemoptysis, and chest pain—symptoms that can occur in independent cases of both PCE and CPA—were the commonest presentations. Thus, the coexistence of Aspergillus in hydatid cysts is prone to being overlooked, and diagnosis can only be made by deliberate investigations, including imaging and serology.

The diagnosis of PCE is usually based on radiology.²⁷ On imaging, PCE is associated with a variety of signs, depending on whether the cysts are complicated or not. Intact cysts present as sharply defined round to oval homogenous opacities of variable size, typically 1–20 cm in diameter, on plain chest radiographs.⁵⁵ Partially evacuated cysts give the waterlily or Camelote sign in about 10%–15% of PCE cases. The signet ring sign, seen when a bleb of air dissects into the wall of the cyst, giving it the shape of a ring, is indicative of impending cyst rupture.⁵⁵ In contrast, ruptured cysts produce a host of signs, such as the air crescent or meniscus sign, inverse crescent sign, Cumbo sign (onion peel sign), rising sun sign, and air bubble sign.⁵⁵ The air bubble sign on a CT scan, which has high sensitivity and specificity, signifies a ruptured, infected hydatid cyst, differentiating it from abscesses or tumors.

For CPA, chest radiography is the initial screening imaging modality and can demonstrate cavities, bronchiectasis, soft tissue within the cavity, nodules, and volume loss/lung fibrosis.⁵⁶ High-resolution chest computed tomography is the imaging modality of choice for better delineation of cavities, cavity wall invasion, intracavitary soft tissue, pleural thickening, and lymphadenopathy.⁵⁶ In simple aspergillomas, chest radiograph shows an air-filled cavity with intracavitary soft tissue, usually located in the upper lobes. At the same time, high-resolution CT of the thorax typically depicts a well-defined soft-tissue mass within a lung cavity, with a characteristic Monod sign (air surrounding the aspergilloma in a pre-existing cavity).

In the diagnosis of hydatid disease, serological testing typically serves a supportive role. In addition to the assay format, the sensitivity of serological assays depends on the location, number, integrity, and viability of the cyst.⁵⁵ The seropositivity rate is higher in hepatic cysts than in pulmonary cysts.⁵⁵ In PCE, intact pulmonary cysts often give a falsely negative serological test, while ruptured cysts increase the likelihood of seropositivity. This is because the sequestration of antigens within intact cysts minimizes their ability to stimulate antibody production by the host’s immune system. On the other hand, serological tests for CPA have become a mainstay of diagnosis, as elevated Aspergillus-specific IgG antibodies are found in over 90% of patients with CPA.⁵⁷ However, our review indicates that serology for aspergillosis was rarely performed, possibly due to its non-availability or a low index of suspicion. Microbiological cultures of respiratory specimens can also be used for diagnosis, but they are less sensitive. The recovery rate of Aspergillus spp. is significantly higher for high-volume cultures than for conventional cultures.⁵⁸

PCE requires a combined surgical and medical therapy, with a PAIR (puncture, aspiration, injection, and re-aspiration) approach; medical therapy, typically with albendazole or mebendazole, is the standard of care.⁵⁹ Cystic echinococcosis generally has a good prognosis, with cure rates as high as 100% and very low recurrence rates.^59,60 On the other hand, medical therapy is the mainstay of managing CPA. Oral itraconazole or voriconazole for 6–12 months or lifelong is the mainstay of therapy for most symptomatic patients and is associated with a significant improvement in quality of life.^61,62 Mortality in treated cases of CPA is about 20% at 1 year and about 50% at 5 years.^63–65 In CPA, surgical treatment is indicated for patients with Aspergillus nodules and for those with simple aspergilloma with good lung function test results.⁶⁶ Surgery is curative; however, a few patients relapse.^67,68 In Africa, the surgical management of patients had a mortality rate of less than 10%.⁶⁹ Video-assisted thoracoscopic surgery is an emerging surgical option associated with lower post-operative complications, recurrence, and post-procedural sepsis.⁷⁰

This review provides a comprehensive analysis of CPA as a complication of PCE and a new insight into the expanding risk factor for CPA. CPA diagnosis is becoming more feasible in low-income countries with the introduction of the Aspergillus IgG–IgM lateral flow assay.⁷¹ Demonstration of a possible occurrence of CPA-PCE -PTB is a significant proportion in this review and warrants further investigations into the need for enhanced clinical suspicion for CPA in PCE, PTB, or co-infected individuals. An important limitation of this systematic review is that we included case reports and case series, given their underreporting in the literature. This limits the statistical inferences we can make, and the descriptions are prone to selection bias.

Limitations and future directions

This systematic review has several limitations that should be acknowledged. First, most included studies were case reports and small case series, which are inherently subject to publication and reporting bias, as unusual or severe presentations are more likely to be published than typical cases. Second, there was marked heterogeneity in the diagnostic approaches used across studies, with limited application of standardized criteria for both chronic pulmonary aspergillosis and PCE. This variation limits the comparability of cases and may have led to under- or over-diagnosis in some reports. Third, important clinical details, such as comorbidities, treatment regimens, and outcomes, were inconsistently reported, further limiting the ability to draw robust conclusions. Finally, the geographic clustering of studies in a few endemic regions suggests that the true global burden of CPA complicating PCE remains underestimated, and findings from this review may not be generalizable to all settings.

Future studies should address these gaps through prospective cohort studies conducted in endemic regions, which would provide more reliable estimates of CPA incidence, clinical outcomes, and risk factors complicating PCE. The development and validation of standardized diagnostic scoring systems could also enhance comparability across studies and improve early recognition of this co-infection. In addition, integrating advanced molecular and omics-based approaches for pathogen identification holds promise for clarifying host–pathogen interactions and uncovering novel diagnostic and therapeutic targets.

Conclusion

PCE can predispose both immunocompromised and immunocompetent individuals to the development of CPA. Diagnostic approaches primarily include radiology and histology, while treatment often involves a combination of surgical and medical management, with antifungals and anthelminthic drugs being commonly used. Despite the complexity of CPA, patients generally achieve favorable outcomes with appropriate treatment. Although rare, greater awareness and understanding of this co-infection will improve diagnosis and management, ultimately enhancing patient care in areas endemic for echinococcosis. Proactive steps should be taken to detect Aspergillus co-infection using computed tomography scans and serological testing. Where these are negative, follow-up of persons managed for PCE may be warranted to detect the development of CPA promptly. Further research is needed to optimize diagnostic and therapeutic strategies for this condition.

Supplemental Material

sj-docx-1-tai-10.1177_20499361251404362 – Supplemental material for Chronic pulmonary aspergillosis complicating pulmonary cystic echinococcosis: a global systematic review

Supplemental material, sj-docx-1-tai-10.1177_20499361251404362 for Chronic pulmonary aspergillosis complicating pulmonary cystic echinococcosis: a global systematic review by Felix Bongomin, Aayush Adhikari, Ronald Olum, Pratik Baral, Iriagbonse Iyabo Osaigbovo, Winnie Kibone, Bassey E. Ekeng, Linda Atulinda, Bethan Morgan, Shailendra Katwal, Norman van Rhijn and David W. Denning in Therapeutic Advances in Infectious Disease

Footnotes

Acknowledgements

Felix Bongomin is supported by the Carigest MA Conny Maeva Charitable Foundation as part of the “Chronic Pulmonary Aspergillosis: Optimization of Therapy, Immunogenetic Screening, and Diagnosis in Uganda [CPA_OPTIONS_Uganda]” as a PhD studentship at the University of Manchester, United Kingdom. CARIGEST SA did not play any role in the design, implementation, and analysis of the study.

Declarations

ORCID iDs

Felix Bongomin

Ronald Olum

Iriagbonse Iyabo Osaigbovo

Winnie Kibone

Bassey E. Ekeng

Supplemental material

Supplemental material for this article is available online.

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