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Id Subject Object Predicate Lexical cue
T1 0-78 Sentence denotes Detection of Invasive Pulmonary Aspergillosis in COVID-19 with Nondirected BAL
T2 80-94 Sentence denotes To the Editor:
T3 95-339 Sentence denotes Invasive pulmonary aspergillosis (IPA) can complicate influenza pneumonia in critically ill patients owing to viral destruction of bronchial mucosa, facilitating invasion of Aspergillus species, and compromised host defenses to Aspergillus (1).
T4 340-546 Sentence denotes Given the association between IPA and increased mortality in influenza, rapid diagnostic investigations and early (preemptive) treatment of IPA are recommended in critically ill patients with influenza (2).
T5 547-646 Sentence denotes In ICU patients with coronavirus disease (COVID-19), the same principles may apply as in influenza.
T6 647-801 Sentence denotes A high incidence of IPA in patients with COVID-19 admitted to the ICU has been reported in small cohorts of patients, some of which appeared online (3–7).
T7 802-1089 Sentence denotes However, in these studies, a bronchoscopy with BAL was not consistently applied, which may hamper estimation of the IPA incidence in COVID-19, as a BAL to obtain material for culture and for galactomannan (GM) measurement is generally recommended for IPA diagnosis in the critically ill.
T8 1090-1226 Sentence denotes However, owing to risk of aerosolization, only a restricted role for bronchoscopy with BAL is recommended in patients with COVID-19 (8).
T9 1227-1369 Sentence denotes We have applied a diagnostic approach by performing a nondirected BAL via a closed-circuit suction catheter, which we describe in this letter.
T10 1370-1685 Sentence denotes Using this nondirected BAL technique as a standard approach, we aimed to determine the proportion of patients with IPA in a cohort of patients with COVID-19 (PCR confirmed) requiring mechanical ventilation who were consecutively admitted to the ICU of our teaching hospital during a 3-week time frame in April 2020.
T11 1686-1815 Sentence denotes The institutional review board of the Amsterdam University Medical Center considered the study as not requiring informed consent.
T12 1816-2035 Sentence denotes The clinical AspICU algorithm can be used to distinguish IPA from colonization in critically ill patients (9), but as viral infection is not a classified host risk factor in this definition, the host factor was omitted.
T13 2036-2360 Sentence denotes The IPA definition used in this paper is based on nondirected BAL GM testing with a cutoff of 1 optical density index, for which sensitivity and specificity are 86% and 95%, respectively, combined with worsening clinical symptoms (i.e., increase in C-reactive protein, worsening PaO2/FiO2 ratio, persistent or rising fever).
T14 2361-2638 Sentence denotes Nondirected BAL was performed at a median of 2 days (range, 0–8 d) after ICU admission, in nonparalyzed patients, by advancing a 12-F suction catheter with a length of 54 cm via a closed circuit until bronchial wedging (Halyard Turbo-cleaning closed suction system for adults).
T15 2639-2748 Sentence denotes Then, 2 × 20 ml of sterile NaCl 0.9% was given via the closed circuit and retrieved via the suction catheter.
T16 2749-2875 Sentence denotes Samples were sent for GM (by ELISA, Platelia Aspergillus Ag from BIO-RAD) and culture only if it yielded nontransparent fluid.
T17 2876-3023 Sentence denotes All patients received a 5-day course of hydroxychloroquine and lopinavir/ritonavir, either of which was stopped upon the emergence of side effects.
T18 3024-3182 Sentence denotes Differences between IPA and non-IPA were tested with Student’s t test or Mann-Whitney U or chi-square test/Fisher’s exact test depending on data distribution.
T19 3183-3238 Sentence denotes P value <0.05 was considered statistically significant.
T20 3239-3411 Sentence denotes Of 53 included patients, 2 patients died within 24 hours after admission and 9 patients were transferred to another hospital for logistical reasons shortly after admission.
T21 3412-3503 Sentence denotes The remaining 42 patients underwent a nondirected BAL (patient characteristics in Table 1).
T22 3504-3644 Sentence denotes A classical IPA risk factor was present in only one patient, who received immunosuppressive medication in the context of a renal transplant.
T23 3645-3737 Sentence denotes None of the other patients received corticosteroid treatment before or during ICU admission.
T24 3738-3919 Sentence denotes Patients with IPA more often had chronic obstructive pulmonary disease or asthma compared with those without IPA (P < 0.05), which may suggest a role for impaired ciliary clearance.
T25 3920-3928 Sentence denotes Table 1.
T26 3930-3966 Sentence denotes Characteristics of Included Patients
T27 3967-4022 Sentence denotes   IPA (n = 9) Non-IPA (n = 33) All Patients (N = 42)
T28 4023-4080 Sentence denotes Age, yr, mean (range) 68 (39–76) 60 (25–79) 62 (25–79)
T29 4081-4129 Sentence denotes Sex, M, n (%) 5 (55.6%) 28 (84.8%) 33 (78.6%)
T30 4130-4176 Sentence denotes BMI, kg/m2 30 [26–34] 27 [27–29] 29 [28–30]
T31 4177-4236 Sentence denotes APACHE IV pred mort 19% [12–25]* 21% [17–26] 21% [17–25]
T32 4237-4297 Sentence denotes Lowest PF ratio 94 [74–114] 102 [91–114] 100 [91.2–110.2]
T33 4298-4378 Sentence denotes Galactomannan in BAL, ODI 3.33 [2.67–4.00]* 0.21 [0.17–0.27] 0.67 [0.39–0.95]
T34 4379-4424 Sentence denotes COPD, n (%) 4 (44.4%)* 4 (12.1%) 8 (19.0%)
T35 4425-4468 Sentence denotes DM, n (%) 1 (11.1%) 9 (27.3%) 10 (23.8%)
T36 4469-4526 Sentence denotes Chronic corticosteroid use, n (%) 1 (11.1%) 0 1 (2.4%)
T37 4527-4550 Sentence denotes Neutropenia, n 0 0 0
T38 4551-4583 Sentence denotes Stem cell transplant, n 0 0 0
T39 4584-4652 Sentence denotes Immunodeficiency (acquired/inherited), n (%) 1 (11.1%) 0 1 (2.4%)
T40 4653-4716 Sentence denotes Arterial hypertension, n (%) 3 (33.3%) 10 (30.3%) 13 (30.9%)
T41 4717-4764 Sentence denotes ICU LOS, d 37 [26–47]* 19 [15–23] 23 [18–27]
T42 4765-4818 Sentence denotes ICU mortality, n (%) 2 (22.2%) 5 (15.1%) 7 (16.6%)
T43 4819-5143 Sentence denotes Definition of abbreviations: APACHE IV = Acute Physiology and Chronic Health Evaluation IV; BMI = body mass index; COPD = chronic obstructive pulmonary disease; DM = diabetes mellitus; IPA = invasive pulmonary aspergillosis; LOS = length of stay; ODI = optical density index; PF = PaO2/FiO2; pred mort = predicted mortality.
T44 5144-5221 Sentence denotes Data are expressed as mean [95% confidence interval] unless stated otherwise.
T45 5222-5234 Sentence denotes * P < 0.05.
T46 5235-5431 Sentence denotes Based on clinical symptoms and a positive GM testing on nondirected BAL fluid, the proportion of putative IPA in the tested cohort was 21.4%, with a 95% confidence interval of 9.0–33.8% (Table 2).
T47 5432-5697 Sentence denotes Fungal cultures of the nondirected BAL yielded positive results in seven (77.8%) patients with IPA and only one (3%) patient without IPA, who, because of lack of clinical deterioration and lack of increased BAL GM levels, was ruled to be colonized with Aspergillus.
T48 5698-5828 Sentence denotes At 30-day follow-up after inclusion cessation, ICU mortality in the IPA group was 22.2% and 15.1% in the non-IPA group (P = 0.61).
T49 5829-5903 Sentence denotes Autopsies were not performed because of a perceived risk of contamination.
T50 5904-6005 Sentence denotes Mean ICU length of stay was 37 days for patients with IPA versus 19 for those without IPA (P < 0.05).
T51 6006-6014 Sentence denotes Table 2.
T52 6016-6080 Sentence denotes Diagnostic Variables of Patients with COVID-19 with Putative IPA
T53 6081-6092 Sentence denotes Patient No.
T54 6094-6286 Sentence denotes Sex Age (yr) APACHE IV Pred Mort. (%) BMI (kg/m2) LOS at IPA Diagnosis (d) GM in BAL at Diagnosis (ODI) Fungal Culture Comorbidity Clinical Findings at Diagnosis Radiological Findings
T55 6287-6389 Sentence denotes 1 M 39 12.55 34.57 19 3.14 No growth Obese, asthma Persistent fever, increase in CRP CT: GGO
T56 6390-6537 Sentence denotes 2 F 76 25.73 39.34 4 >4.00 A. fumigatus Obese, AHT, asthma Persistent fever, increase in CRP, worsening PF ratio CT: GGO, consolidations
T57 6538-6680 Sentence denotes 3 F 73 14.73 29.78 3 >4.00 A. fumigatus Obese, AHT, COPD Persistent fever, increase in CRP X-ray: patchy, peripheral consolidations
T58 6681-6806 Sentence denotes 4 M 64 21.49 27.76 3 1.10 A. fumigatus Overweight Rising fever, increase in CRP, MOF CT: GGO, basal consolidations
T59 6807-6950 Sentence denotes 5 M 74 12.22 23.15 1 >4.00 A. fumigatus None Rising fever, increase in CRP, low PF ratio X-ray: conglomerate alveolar consolidations
T60 6951-7114 Sentence denotes 6 F 72 18.45 29.70 1 >4.00 A. fumigatus Obese, COPD Rising fever, increase in CRP, worsening PF ratio CT: extensive peripheral consolidations, emphysema
T61 7115-7245 Sentence denotes 7 M 76 30.67 27.78 1 >4.00 A. flavus Overweight, AHT Rising fever, increase CRP, MOF CT: GGO, peripheral consolidations
T62 7246-7380 Sentence denotes 8 M 64 12.80 31.46 6 2.60 No growth Obese Rising fever, increase in CRP, worsening PF ratio X-ray: increasing consolidations
T63 7381-7548 Sentence denotes 9 M 73 28.62 26.32 3 3.35 A. terreus Overweight, DM II renal transplant Rising fever, worsening PF ratio X-ray: increasing consolidations, mainly peripheral
T64 7549-8175 Sentence denotes Definition of abbreviations: A. flavus = Aspergillus flavus; A. fumigatus = Aspergillus fumigatus; A. terreus = Aspergillus terreus; AHT = arterial hypertension; APACHE = Acute Physiology and Chronic Health Evaluation; BMI = body mass index; COPD = chronic obstructive pulmonary disease; COVID-19 = coronavirus disease; CRP = C-reactive protein; CT = computed tomography; DM II = diabetes mellitus type 2; GGO = ground glass opacifications; GM = galactomannan; IPA = invasive pulmonary aspergillosis; LOS = length of stay; MOF = multiorgan failure; ODI = optical density index; PF = PaO2/FiO2; Pred Mort = predicted mortality.
T65 8176-8330 Sentence denotes A bronchoscopy with BAL is the preferred diagnostic approach because GM antigen detection and culture have a good sensitivity in influenza-associated IPA.
T66 8331-8596 Sentence denotes However, given the risk of aerosolization, The American Association for Bronchology and Interventional Pulmonology issued a statement providing a limited role for bronchoscopy in patients with COVID-19, advocating the use of a nonbronchoscopic alveolar lavage (10).
T67 8597-8722 Sentence denotes The technique we used in this study minimizes the risk for care providers while providing a diagnostic tool for our patients.
T68 8723-8796 Sentence denotes However, the nondirected BAL technique is not validated for GM detection.
T69 8797-9071 Sentence denotes As all patients had consolidations in all regions of the lung, the chances that a nondirected BAL may result in sampling of a lung region that was not affected by IPA may be low, although it is unclear to which extent consolidations are caused by the virus or by the fungus.
T70 9072-9205 Sentence denotes More importantly, we cannot rule out overdiagnosis, as a nondirected sample may not always reflect microbiology of the lower airways.
T71 9206-9284 Sentence denotes Therefore, instead of 0.5, a cutoff GM index of 1.0 was applied in this study.
T72 9285-9334 Sentence denotes Nevertheless, sampling error cannot be ruled out.
T73 9335-9438 Sentence denotes Of note, however, concordance between GM index >1.0 and positive Aspergillus cultures was high (77.8%).
T74 9439-9525 Sentence denotes Early detection and treatment of IPA improves outcome compared with delayed diagnosis.
T75 9526-9708 Sentence denotes Therefore, we opted to treat all nine patients who were deemed to have putative IPA with antifungal therapy (with an empirical regimen consisting of amphotericin B and voriconazole).
T76 9709-9831 Sentence denotes We noted a longer ICU length of stay for patients who developed IPA, although ICU mortality did not differ between groups.
T77 9832-9975 Sentence denotes However, whether COVID-19–associated IPA contributes to mortality, or whether IPA therapy improves outcome, cannot be dissected from our study.
T78 9976-10140 Sentence denotes We conclude that the incidence of putative IPA may be high in patients with COVID-19 and that chronic obstructive pulmonary disease may be a particular risk factor.
T79 10141-10270 Sentence denotes Implementation of surveillance of mechanically ventilated patients with COVID-19 using the nondirected BAL technique is feasible.
T80 10271-10532 Sentence denotes As COVID-19–associated IPA appears to resemble influenza-associated IPA in many ways, and ICU length of stay was longer in those with IPA versus those without, it is our opinion that active surveillance and treatment may be beneficial in patients with COVID-19.
T81 10534-10570 Sentence denotes This letter has a related editorial.
T82 10571-10608 Sentence denotes Originally Published in Press as DOI:
T83 10609-10652 Sentence denotes 10.1164/rccm.202005-2018LE on July 15, 2020
T84 10653-10738 Sentence denotes Author disclosures are available with the text of this letter at www.atsjournals.org.