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Id Subject Object Predicate Lexical cue
T1 0-77 Sentence denotes Delayed diagnosis of COVID-19 in a 34-year-old man with atypical presentation
T2 79-730 Sentence denotes The pandemic of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) challenges clinicians with a variety of presentations of COVID-19.1, 2, 3 Infection with SARS-CoV-2 is confirmed by real-time RT-PCR, typically done on nasopharyngeal (NP) swabs or, less commonly, samples from the lower respiratory tract, including bronchoalveolar lavage (BAL).4 Some data suggest that RT-PCR might be more sensitive with BAL than with NP swabs.5 Here, we present a man who developed rapidly progressive pulmonary disease and, following two negative NP tests, was diagnosed with COVID-19 on the basis of bronchoscopic biopsy and BAL after 9 days of illness.
T3 731-980 Sentence denotes 14 days before admission to Mount Sinai Hospital (New York, NY, USA), a 34-year-old man developed fever, cough, and dyspnoea due to influenza A, confirmed by an NP swab 2 days later at a walk-in urgent care facility of the Mount Sinai Health System.
T4 981-1004 Sentence denotes No radiograph was done.
T5 1005-1148 Sentence denotes The patient was previously healthy with no past hospitalisations, and works as an anaesthesiologist in a large medical centre in New York City.
T6 1149-1388 Sentence denotes His only medication was emtricitabine and tenofovir alafenamide for HIV pre-exposure prophylaxis, which he had been taking once a day for 5 months (and prior to that, tenofovir disoproxil fumarate and emtricitabine once a day for 3 years).
T7 1389-1489 Sentence denotes He was treated for influenza with oseltamivir for 5 days; symptoms resolved after 5 days of illness.
T8 1490-1607 Sentence denotes He felt fully recovered from influenza, and returned to work in the hospital 11 days after his symptoms had resolved.
T9 1608-1745 Sentence denotes On the afternoon of his first day back at work, the patient had rapid onset of fever, chills, rigors, dry cough, and shortness of breath.
T10 1746-1993 Sentence denotes On arrival at the emergency department of Mount Sinai Hospital, on the same afternoon as symptom onset (hospital day 1), his temperature was 39·4°C, blood pressure 142/80 mm Hg, heart rate 130 beats per min, and respiratory rate20 breaths per min.
T11 1994-2050 Sentence denotes Oxygen saturation ranged from 89% to 99% at ambient air.
T12 2051-2138 Sentence denotes On examination, he appeared acutely ill and in mild distress with normal breath sounds.
T13 2139-2311 Sentence denotes Plasmalyte (2 L), vancomycin (1 g once every 12 h), and ceftriaxone (2 g once a day) were administered intravenously; all medications are detailed in the appendix (pp 1–2).
T14 2312-2444 Sentence denotes The patient's white blood cell count was 13 900 cells per μL (reference range 4500–11 000), with a lymphocyte count of 9·2% (15–50).
T15 2445-2528 Sentence denotes Chest radiograph revealed an ill-defined nodule in the right mid-lung (figure 1A ).
T16 2529-2570 Sentence denotes The patient was admitted to the hospital.
T17 2571-2673 Sentence denotes On hospital day 1, a respiratory viral panel test of an NP swab was negative, including for influenza.
T18 2674-2786 Sentence denotes On day 2, RT-PCR (Roche Cobas 6800 System, Roche, Basel, Switzerland) of an NP swab was negative for SARS-CoV-2.
T19 2787-2999 Sentence denotes This assay targets open-reading frame 1, a region that is unique to SARS-CoV-2, and has a sensitivity of 1–5 copies per μL.6 An HIV test was negative, and intravenous azithromycin (500 mg once a day) was started.
T20 3000-3078 Sentence denotes The remainder of the laboratory tests are summarised in the appendix (pp 1–2).
T21 3079-3144 Sentence denotes Figure 1 Imaging with chest radiograph, chest CT, and radial EBUS
T22 3145-3326 Sentence denotes (A) Admission chest radiograph (hospital day 1) with right mid-lung nodule (arrow). (B) First chest CT (day 2) with right lower lobe rounded opacity with possible halo sign (arrow).
T23 3327-3766 Sentence denotes A second chest CT (day 6) showed new right upper lobe nodular opacities (C; arrows), a new large ground glass opacity in the right lower lobe (D; arrow); and enlargement of the right lower lobe rounded opacity with possible reverse halo sign (E; green arrow) and a new left lower lobe rounded opacity (E; blue arrow). (F) Radial EBUS image of right lower lobe rounded opacity (arrow) used to target the transbronchial lung biopsy on day 9.
T24 3767-3797 Sentence denotes EBUS=endobronchial ultrasound.
T25 3798-3937 Sentence denotes On hospital day 2, CT of the chest found a rounded opacity in the right lower lobe (figure 1B); the remainder of the lungs appeared normal.
T26 3938-4069 Sentence denotes On day 4, the patient's peak temperature was 37·8°C, and his cough and dyspnoea had improved; intravenous azithromycin was stopped.
T27 4070-4169 Sentence denotes On day 5, fever to a peak of 38·9°C occurred, and the patient developed rigors and severe coughing.
T28 4170-4321 Sentence denotes Intravenous azithromycin (500 mg once a day) was restarted and oral clindamycin (300 mg once every 6 h) was administered, without clinical improvement.
T29 4322-4465 Sentence denotes A repeat chest CT on day 6 showed enlargement of the right lower lobe opacity, which had become surrounded by a large new ground glass opacity.
T30 4466-4595 Sentence denotes A new rounded opacity was present in the left lower lobe, and a new multilobulated opacity in the right upper lobe (figure 1C–E).
T31 4596-4665 Sentence denotes The CT report suggested atypical pneumonia of fungal or viral origin.
T32 4666-4733 Sentence denotes A repeat RT-PCR of an NP swab for SARS-CoV-2 was negative on day 7.
T33 4734-4834 Sentence denotes Severe cough, malaise, rigors, and fever continued, and oxygen saturation was 92–94% at ambient air.
T34 4835-4989 Sentence denotes Antibiotics were stopped on day 8, and prednisone 40 mg was given orally on the mornings of day 8 and day 9 for presumed cryptogenic organising pneumonia.
T35 4990-5297 Sentence denotes Consulting radiologists noted CT evidence of a halo sign and reverse halo sign (figure 1B and 1E),7 suggestive of invasive fungal infection and not characteristic of previously reported CT findings for COVID-19.1, 8 On day 8, a serum galactomannan assay was ordered and pulmonary consultation was requested.
T36 5298-5383 Sentence denotes The pulmonary consultant recommended bronchoscopy with transbronchial biopsy and BAL.
T37 5384-5532 Sentence denotes Given the epidemic of COVID-19 in New York City at the time, the pulmonary team still considered COVID-19 a possible cause of the pulmonary disease.
T38 5533-5676 Sentence denotes On hospital day 9, bronchoscopy was done with appropriate personal and environmental protection precautions for COVID-19, including intubation.
T39 5677-5740 Sentence denotes The airways appeared normal without inflammation or secretions.
T40 5741-5914 Sentence denotes The original right lower lobe opacity was targeted for biopsy, and radial endobronchial ultrasound was used to select the airways leading directly to the lesion (figure 1F).
T41 5915-6027 Sentence denotes Transbronchial lung biopsy and BAL were done in the right lower lobe lateral segment through the target airways.
T42 6028-6204 Sentence denotes Appropriate specimens were sent for histopathological and cytological examinations and for routine bacterial, fungal, and mycobacterial cultures, and a BAL galactomannan assay.
T43 6205-6352 Sentence denotes Validated testing of BAL for SARS-CoV-2 was unavailable, and thus a swab used for NP specimens was swirled in the BAL specimen and sent for RT-PCR.
T44 6353-6568 Sentence denotes On day 9, pathology reported alveolar tissue with patchy chronic inflammation, type 2 pneumocyte hyperplasia, and areas of organising intra-alveolar fibrin and fibroblastic tissue, consistent with acute lung injury.
T45 6569-6775 Sentence denotes No hyaline membranes, viral cytopathic changes, giant cells, granulomas, or malignancy were present, and no microorganisms were identified on acid-fast or Grocott's methenamine silver staining (figure 2A ).
T46 6776-7008 Sentence denotes Cytological examination of the BAL found marked reactive changes in pneumocytes, with lymphocytes, histiocytes, and occasional fibroblastic balls lined by pneumocytes, with negative Grocott's methenamine silver staining (figure 2B).
T47 7009-7107 Sentence denotes RT-PCR for SARS-CoV-2 of the BAL specimen was positive; BAL and serum galactomannan were negative.
T48 7108-7157 Sentence denotes No additional antibiotic or prednisone was given.
T49 7158-7248 Sentence denotes On day 10, the patient declined treatment with hydroxychloroquine and was discharged home.
T50 7249-7397 Sentence denotes Via follow-up phone calls, the patient reported that his cough and myalgias slowly resolved, and he had no fever higher than 37·8°C after discharge.
T51 7398-7440 Sentence denotes No chest imaging was done after discharge.
T52 7441-7501 Sentence denotes Figure 2 Pathology of transbronchial biopsy and BAL cytology
T53 7502-7625 Sentence denotes (A) Transbronchial biopsy showing prominent pneumocyte hyperplasia with areas of organising fibrin and fibroblastic tissue.
T54 7626-7884 Sentence denotes The alveolar septa showed some mild chronic inflammatory cell infiltrates (haematoxylin-eosin stain, original magnification × 200). (B) BAL cytology specimen showing a fibroblastic ball lined by pneumocytes (Papanicolaou stain, original magnification × 400).
T55 7885-7912 Sentence denotes BAL=bronchoalveolar lavage.
T56 7913-8097 Sentence denotes This patient experienced an unusual, confusing clinical course during a 10-day hospitalisation, which concluded with a diagnosis of COVID-19, confirmed only with bronchoscopic samples.
T57 8098-8405 Sentence denotes An atypical presentation of SARS-CoV-2 can explain the entire clinical course during this hospitalisation, beginning with a possible mild cytokine storm and pulmonary infiltrate on hospital day 1, with initial clinical improvement followed by rapid progression within 4 days to multifocal pulmonary disease.
T58 8406-8602 Sentence denotes Development of a cytokine storm has been reported in patients with COVID-19, but its occurrence within a few hours after onset of symptoms seems unusual,9 as does the initial clinical improvement.
T59 8603-8835 Sentence denotes The patient's clinical course might have been affected by other factors, including the influenza infection itself or its treatment 11 days earlier, chronic antiretroviral therapy, and early initiation of treatment with azithromycin.
T60 8836-8977 Sentence denotes If SARS-CoV-2 was the sole cause of this presentation, starting on the day of admission, then the two negative NP tests were false negatives.
T61 8978-9187 Sentence denotes In a study by Wang and colleagues,5 BAL was positive in 14 (93%) of 15 positive cases, whereas nasal swabs were positive in 5 (63%) of 8 positive cases, and pharyngeal swabs in 126 (32%) of 398 positive cases.
T62 9188-9391 Sentence denotes The pathology from transbronchial lung biopsy, which was targeted specifically at the right lower lobe rounded opacity present on the initial chest CT, showed a pattern consistent with acute lung injury.
T63 9392-9722 Sentence denotes The few peer-reviewed publications reporting pulmonary pathology in COVID-19 to date have all described acute lung injury or diffuse alveolar damage.10, 11, 12, 13, 14, 15, 16 One report of BAL in a patient with COVID-19 described a large number of aggregates of plasma cells;17 this was not seen in the specimen from our patient.
T64 9723-9944 Sentence denotes Both the finding of acute lung injury in the area of lung affected at the onset of symptoms, and the positive RT-PCR test for SARS-CoV-2 in the BAL, support the diagnosis of COVID-19 to explain the entire hospital course.
T65 9945-10189 Sentence denotes Alternatively, a different infection might have caused the early sepsis presentation, with clinical improvement up to day 4 related to appropriate treatment with antibiotics, after which COVID-19 manifested on day 5, causing clinical worsening.
T66 10190-10547 Sentence denotes However, no infection other than SARS-CoV-2 was identified by culture, pathology, or respiratory viral panel, procalcitonin concentration was normal in the first 48 h (appendix p 1), serum and BAL galactomannan were negative, and the pathological finding of acute lung injury in the lesion was already present on day 2, which argue against this explanation.
T67 10548-10811 Sentence denotes A third possible explanation is that cryptogenic organising pneumonia or similar inflammatory illness spontaneously worsened and improved over the hospitalisation, and the positive RT-PCR represents a hospital-acquired infection incidental to the hospital course.
T68 10812-11015 Sentence denotes However, the sepsis-like presentation and the pathology and cytology findings showing an acute lung injury pattern with organising fibrin do not support the diagnosis of cryptogenic organising pneumonia.
T69 11016-11307 Sentence denotes This case represents a presentation of COVID-19 with atypical features, including sudden onset with a mild cytokine storm profile, apparent early response to antibiotics followed by rapid clinical worsening, and two negative RT-PCR tests of NP swabs, which delayed the diagnosis of COVID-19.
T70 11308-11459 Sentence denotes However, for a disease that was unknown only 5 months ago, it might also be too early for clinicians to be certain of which manifestations are typical.
T71 11460-11610 Sentence denotes In most patients requiring hospitalisation, COVID-19 is diagnosed by positive RT-PCR,1 and bronchoscopy is rarely required to establish the diagnosis.
T72 11611-12058 Sentence denotes As noted by the American Association of Bronchology and Interventional Pulmonology, “bronchoscopy should have an extremely limited role in diagnosis of COVID-19 and only be considered in intubated patients if upper respiratory samples are negative and other diagnosis is considered that would significantly change clinical management.”18 We agree with this statement, and feel that the presentation in our patient necessitated use of bronchoscopy.
T73 12060-12082 Sentence denotes Supplementary Material
T74 12083-12105 Sentence denotes Supplementary appendix
T75 12107-12119 Sentence denotes Contributors
T76 12120-12176 Sentence denotes TJH conceived the Case Report and wrote the first draft.
T77 12177-12273 Sentence denotes TJH and KMR collected pathology, cytology, and viral specimens, and designed the appendix table.
T78 12274-12313 Sentence denotes KMR and JM collected and collated data.
T79 12314-12391 Sentence denotes TJH and CE contributed radiology images, and CE interpreted radiology images.
T80 12392-12444 Sentence denotes AHS interpreted and photographed cytology specimens.
T81 12445-12495 Sentence denotes MBB reviewed and photographed pathology specimens.
T82 12496-12585 Sentence denotes All authors participated in the construction and editing of the manuscript and revisions.
T83 12586-12648 Sentence denotes Written consent for publication was obtained from the patient.
T84 12650-12674 Sentence denotes Declaration of interests
T85 12675-12709 Sentence denotes We declare no competing interests.