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Target-shaped combined halo and reversed-halo sign, an atypical chest CT finding in COVID-19

      Highlights

      • Bilateral peripheral ground glass opacities, with or without consolidation are the chest CT findings in COVID-19.
      • Halo and reversed-halo signs are associated with lung fungal infections. They can also be atypical presentations of COVID-19
      • Target shaped lung lesions are unusual imaging findings that can be seen in COVID-19 without any other underlying disease

      Abstract

      Typical chest CT findings in COVID-19 have been described as bilateral peripheral ground glass opacities, with or without consolidation. Halo sign and reversed halo sign have been reported as atypical imaging findings in this disease. However, to the best of our knowledge, combined presence of these signs has never been reported before. Herein, we present a COVID-19 patient with numerous atypical target-shaped, combined halo and reversed halo pulmonary lesions, in the absence of any other underlying disease.

      Keywords

      1. Introduction

      The first clinical case of coronavirus disease 2019 (COVID-19) was reported in Wuhan city, China. To date (May 14, 2020), 4,248,389 patients have been infected, with 292,046 deaths reported worldwide [
      • World Health Organization
      Coronavirus disease (COVID-19) situation report.
      ].
      Clinical symptoms of COVID-19 are non-specific and include fever, cough, myalgia, or fatigue. Less common symptoms are diarrhea, nausea, headache, sputum production, and hemoptysis. Approximately, half of the patients experience dyspnea during disease progression [
      • Huang C.
      • Wang Y.
      • Li X.
      • Ren L.
      • Zhao J.
      • Hu Y.
      • et al.
      Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.
      ]. The predominant chest CT findings in COVID-19 have been described as bilateral and peripheral ground glass opacities, with or without consolidation. Lymphadenopathy, pleural effusion, and lung cavitation were less common imaging features [
      • Chung M.
      • Bernheim A.
      • Mei X.
      • Zhang N.
      • Huang M.
      • Zeng X.
      • et al.
      CT imaging features of 2019 novel coronavirus (2019-nCoV).
      ]. Previous studies have reported the halo and reversed halo signs as less frequent findings in patients with COVID-19 [
      • Chung M.
      • Bernheim A.
      • Mei X.
      • Zhang N.
      • Huang M.
      • Zeng X.
      • et al.
      CT imaging features of 2019 novel coronavirus (2019-nCoV).
      ,
      • Song F.
      • Shi N.
      • Shan F.
      • Zhang Z.
      • Shen J.
      • Lu H.
      • et al.
      Emerging 2019 novel coronavirus (2019-nCoV) pneumonia.
      ,
      • Salehi S.
      • Abedi A.
      • Balakrishnan S.
      • Gholamrezanezhad A.
      Coronavirus disease 2019 (COVID-19): a systematic review of imaging findings in 919 patients.
      ,
      • Farideh Gharekhanloo S.H.H.
      • Keramat Fariba
      • Esna-Ashari Farzaneh
      • Mamani Mojgan
      • Majzoubi Mohammad Mahdi
      • Eini Peyman
      • et al.
      Radiological manifestations from 101 patients with 2019 Novel Coronavirus Disease (COVID-19) in Hamadan, West of Iran: typical and atypical findings.
      ,
      • Wang J.
      • Xu Z.
      • Wang J.
      • Feng R.
      • An Y.
      • Ao W.
      • et al.
      CT characteristics of patients infected with 2019 novel coronavirus: association with clinical type.
      ]. The halo sign describes a nodule or mass surrounded by ground glass opacity. The reversed halo (Atoll) sign is defined as a crescent or complete ring of consolidation, surrounding a focal area of ground glass opacity [
      • Georgiadou S.P.
      • Sipsas N.V.
      • Marom E.M.
      • Kontoyiannis D.P.
      The diagnostic value of halo and reversed halo signs for invasive mold infections in compromised hosts.
      ].
      In this case report, we present unusual chest CT findings in a confirmed COVID-19 patient, who has recovered well after experiencing respiratory distress symptoms.

      2. Case presentation

      The patient was a 49-year-old, apparently healthy and non-smoker man, without any underlying disease. He was a taxi driver and in frequent contact with passengers. On March 13, he first presented with fever, dyspnea, and nausea. After four days, respiratory symptoms progressed, and he was admitted to the hospital with tachypnea and low peripheral oxygen saturation (temperature: 38.3 °C, heart rate: 96/min, respiratory rate: 26/min, SpO2 = 85%).
      He was immediately given respiratory support with supplemental oxygen (8 L/min O2 using face mask), with clinical suspicion of COVID-19. Primary laboratory workups demonstrated a significant increase in CPK and LDH and positive CRP (Table 1). The diagnosis of COVID −19 was confirmed using nasopharyngeal sample RT-PCR, which was positive for SARS-CoV2. Blood culture tests yielded negative results after 24, 48, 72 h.
      Table 1Laboratory results at the time of admission
      ResultReference range
      WBC, C/μL71004000–10,000
      Neutrophils, %63.4%49.0–74.0
      Lymphocytes, %33.1%26.0–46.0
      RBC, ×106C/μL5.024.4–6.2
      Hemoglobin, g/dL15.113.2–16.5
      Hematocrit, %45.341.5–53.0
      Platelets, ×103C/μL290130–450
      Na, mEq/L137.0135–145
      K, mEq/L4.03.5–5.5
      Urea, mg/dL38.315–50
      Creatinine, mg/dL1.020.7–1.4
      LDH, U/L572 ↑<480
      CPK, U/L527 ↑<196
      ESR 1 h, mm/h57 ↑0–15
      CRP, mg/L9 ↑<6
      PT, s13.513.5–18
      PTT, s2724–34
      Blood culture, 24, 48, 72 hNegative
      WBC: white blood cell, RBC: red blood cell, Na: sodium, K: potassium, LDH; lactate dehydrogenase, CPK: creatine phosphokinase, ESR: erythrocyte sedimentation rate, CRP: C-reactive protein, PT: Prothrombin time, PTT: partial thromboplastin time.
      Baseline chest CT was obtained on the first day of admission, showing diffuse non-rounded multifocal consolidations and air-bronchograms in both lungs, with confluent appearance in both lower lobes. There were several target-shaped reversed halo configurations with central round dense consolidation, which were described as combined halo and reversed halo signs (maximum size of 33 × 24 mm) coexisting on the same study (Fig. 1, Supplement video file). A small amount of pleural effusion was noted in the right hemithorax. No lymphadenopathy, pericardial effusion, collapse, or cavitary changes were found.
      The patient was started on multidrug treatment with hydroxychloroquine (400 mg/OD), oseltamivir (75 mg/BD), ribavirin (400 mg/BD), levofloxacin (500 mg/OD), and naproxen (500 mg/BD). He responded well to treatment. His fever resolved within 48 h and his respiratory symptoms subsided in 5 days of hospitalization. He did not require endotracheal intubation or ICU admission. The patient was discharged after one week with stable vital signs, and his SpO2 was 95%.
      Fig. 1
      Fig. 1Baseline chest CT displaying multilobar peripheral consolidations with mixed configuration of ‘reversed halo’ and ‘halo’ signs. This appearance was embedded in areas of consolidation. The described patterns were seen in the anterior and apicoposterior segments of the left upper lobe with a maximum size of 33 × 24 mm (arrowhead) (A). Another well visualized peripheral halo consolidation and central round nodule was seen in the posterior segment of the right lower lobe (28 × 18 mm) (B). Two additional areas of peripheral complete halo and central nodular opacity were seen in the lateral segment of the right lower lobe and lateral segment of the left lower lobe, measuring 29 × 21 mm and 25 × 15 mm, respectively (C).
      Four weeks after disease onset, a follow-up CT scan (Fig. 2) showed complete clearance of consolidations. Diffuse round pure ground glass opacities were seen in both lungs without intra- or inter-lobular septal thickening. Scar formation, cavitation, atelectasis, or lymphadenopathy were absent.
      Fig. 2
      Fig. 2Follow-up CT-scan, after 4 weeks of disease onset, showing diffuse multifocal patchy pure ground-glass opacities in both lungs, without consolidation. Significant clearance of lung fields in left upper lobe (A), right lower lobe (B), and bilateral lower lobes (C) is evident compared to the baseline. The patient denied any symptoms on the follow-up exam.

      3. Discussion

      In this study, we reported a COVID-19 patient with an unusual chest CT finding of combined halo and reverse halo signs coexisting on the same study, who recovered rapidly after multidrug treatment.
      Alveolar edema and hemorrhage may create the halo sign, while the reversed-halo sign may be formed by the organization and resolution of alveolar exudates [
      • Fan L.
      • Li D.
      • Xue H.
      • Zhang L.
      • Liu Z.
      • Zhang B.
      • et al.
      Progress and prospect on imaging diagnosis of COVID-19.
      ]. Although these findings are not specific, they are highly suggestive for early stages of opportunistic invasive fungal infections (e.g. aspergillosis, mucormycosis) in immunocompromised patients. They might be seen in immunocompetent individuals in other conditions such as non-fungal endemic infections, cryptogenic organizing pneumonia, vasculitis, and neoplastic and inflammatory diseases [
      • Georgiadou S.P.
      • Sipsas N.V.
      • Marom E.M.
      • Kontoyiannis D.P.
      The diagnostic value of halo and reversed halo signs for invasive mold infections in compromised hosts.
      ]. The Reversed Halo sign in invasive fungal infections appears as one or more large lesions; while in endemic infections (e.g. tuberculosis), lesions have a bilateral and asymmetric appearance with ground glass opacities, centrilobular nodules, or consolidations [
      • Maturu V.N.
      • Agarwal R.
      Reversed halo sign: a systematic review.
      ]. The multilobular, peripheral target-shaped findings in our COVID-19 patient were unlikely due to fungal co-infection, given lack of history of immunodeficiency, short disease course, and the resolution of consolidations without any antifungal treatment.
      Bernheim et al. reported that the frequency of uncommon chest CT findings, including the reversed halo sign, increases in the later stages of COVID-19 progression [
      • Bernheim A.
      • Mei X.
      • Huang M.
      • Yang Y.
      • Fayad Z.A.
      • Zhang N.
      • et al.
      Chest CT findings in coronavirus disease-19 (COVID-19): relationship to duration of infection.
      ]. There are no adequate data to explain the pathophysiology of the combined lesions in our patient. The coexistence of both halo and reversed halo signs could be an atypical presentation in COVID-19. To the best of our knowledge, this imaging feature has never been described before.
      This case report provides information for future secondary articles and systematic reviews. We advocate reporting unusual presentations of COVID-19 patients. Future studies on this data should be warranted better understand the pathophysiology and different characteristics of this newly emerged disease.
      The following is the supplementary data related to this article.

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