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Journal Pre-Proof Journal Pre-proof Presenting Clinico-radiologic Features, Causes, and Clinical Course of Exogenous Lipoid Pneumonia in Adults Bilal F. Samhouri, MD, Yasmeen K. Tandon, MD, Thomas E. Hartman, MD, Yohei Harada, MD, Hiroshi Sekiguchi, MD, Eunhee S. Yi, MD, Jay H. Ryu, MD PII: S0012-3692(21)00433-5 DOI: https://doi.org/10.1016/j.chest.2021.02.037 Reference: CHEST 4063 To appear in: CHEST Received Date: 20 December 2020 Revised Date: 14 February 2021 Accepted Date: 16 February 2021 Please cite this article as: Samhouri BF, Tandon YK, Hartman TE, Harada Y, Sekiguchi H, Yi ES, Ryu JH, Presenting Clinico-radiologic Features, Causes, and Clinical Course of Exogenous Lipoid Pneumonia in Adults, CHEST (2021), doi: https://doi.org/10.1016/j.chest.2021.02.037. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Copyright © 2021 Published by Elsevier Inc under license from the American College of Chest Physicians. 1 Word count: abstract –283, text – 3,108 2 Title: Presenting Clinico-radiologic Features, Causes, and Clinical Course of Exogenous Lipoid 3 Pneumonia in Adults 4 Short title: Exogenous Lipoid Pneumonia 5 Author list: 6 Bilal F. Samhouri MD 1, Yasmeen K. Tandon MD 2, Thomas E. Hartman MD 2, Yohei Harada MD 1, 7 Hiroshi Sekiguchi MD 1, Eunhee S. Yi MD 3, Jay H. Ryu MD 1 8 Author affiliations: 9 1Division of Pulmonary and Critical Care Medicine, Mayo Clinic, Rochester, Minnesota 10 2Department of Radiology, Mayo Clinic, Rochester, Minnesota 11 3Division of Anatomic Pathology, Mayo Clinic, Rochester, Minnesota 12 13 Corresponding author: Dr. Jay H Ryu, Division of Pulmonary and Critical Care Medicine, Gonda 18 14 South, Mayo Clinic, 200Journal First St. SW, Rochester, MNPre-proof 55905. E-mail address: [email protected]. 15 Conflict of interest: The authors have none to disclose. 16 Funding: None 17 18 1 19 Abbreviation List: 20 BAL: Bronchoalveolar lavage 21 COPD: Chronic obstructive pulmonary disease 22 ELP: Exogenous lipoid pneumonia 23 FEV1: Forced expiratory volume in 1 st second 24 GERD: Gastroesophageal reflux disease 25 GI: Gastrointestinal 26 IQR: Interquartile range 27 LP: Lipoid pneumonia 28 LTOT: Long-term oxygen therapy 29 OR: Odds ratio 30 PET: Positron emission tomography 31 PFT: Pulmonary functionJournal test Pre-proof 32 SMA: Superior mesenteric artery 33 SUV: Standardized uptake values 34 2 35 Abstract 36 Background: 37 Exogenous lipoid pneumonia (ELP) develops when lipid-containing substances enter the airways through 38 aspiration or inhalation, and incite an inflammatory response. The diagnosis of ELP is often difficult as 39 findings may be nonspecific. ELP’s clinical course has not been well-characterized. 40 Research Question: 41 What are the presenting clinico-radiologic features of ELP, its causative agents, and clinical course? 42 Study Design and Methods: 43 We searched the Mayo Clinic electronic medical records for patients diagnosed with ELP between 1998 44 and 2020. Inclusion diagnostic criteria were: 1) lipoid pneumonia on histopathology, 2) lipid-laden 45 macrophages in bronchoalveolar lavage fluid, or 3) fatty-attenuation of parenchymal opacities on chest 46 CT. Additionally, all patients were required to have a clinician diagnosis of lipoid pneumonia in the 47 absence of conditions known to cause endogenous lipoid pneumonia. 48 Results: 49 Thirty-four patients wereJournal identified. Mean age was 71Pre-proof years, with no gender predominance; one-half were 50 asymptomatic. The diagnosis was confirmed by lung biopsy (including 3 lobectomies for suspected 51 malignancy) in 71%, CT in 24%, and bronchoalveolar lavage in 5% of patients. Most patients manifested 52 bilateral parenchymal opacities that commonly involved the lower lobes; fatty-attenuation was 53 identifiable in only 41% of patients. A causative substance was identified in 79% of cases, in most cases 54 after the diagnosis was established. Over a median follow-up of 1.2-years, only 20% of patients with 55 chronic respiratory symptoms improved, while 50% worsened. Over a median follow-up interval of 1 3 56 year, CT abnormalities improved/resolved in 33%, and progressed in 39%. Patients who deteriorated were 57 older, with a higher prevalence of gastrointestinal disorders than those who remained stable or improved. 58 Interpretation: 59 ELP is often asymptomatic and may not manifest fatty-attenuation on chest CT. Clinical and radiologic 60 abnormalities persist or worsen in the majority of affected patients, even when the causative agent is 61 discontinued. 62 Journal Pre-proof 4 63 Manuscript 64 Lipoid pneumonia (LP) refers to the presence of lipoid material or lipid-laden macrophages within the 65 alveoli and can be endogenous or exogenous, depending on the source of lipids. LP of exogenous origin 66 was first described in 1925 by Laughlen1, and was later termed “exogenous lipoid pneumonia” (ELP). 67 ELP develops when lipid-containing substances of mineral, animal or vegetable origin reach the lower 68 respiratory tract, most commonly through aspiration of nasally applied or ingested material or, less 69 commonly, through inhalation.2 Subsequently, these substances are ingested by alveolar macrophages 70 which initiate a foreign-body like inflammatory reaction, and granulomatous inflammation may ensue.3,4 71 In endogenous lipoid pneumonia, the source of lipids is local cellular breakdown, typically occurring in 72 the setting of airway obstruction, which leads to intracytoplasmic accumulation of fine vacuoles in the 73 alveolar macrophages, as opposed to intra- or extra-cellular accumulation of larger, irregular-sized 74 vacuoles in the setting of ELP. 2,3 75 ELP was initially reported among users of nose drops, and subsequent reports have implicated numerous 76 other substances in the pathogenesis of ELP. Mineral oil (also called liquid paraffin), an over-the-counter 77 preparation often used to treat constipation, remains the most common etiological agent of ELP.5 ELP can 78 be acute or chronic; acute ELP occurs when a large quantity of lipid-containing material is aspirated into 79 the airways (e.g., “fire-eater’sJournal pneumonia”), 6Pre-proof whereas chronic ELP occurs with repeated 80 aspiration/inhalation of small quantities of an oily substance. 81 Chronic ELP can affect individuals of any age, with predilection to involve the extremes of age (i.e., 82 infants and the elderly).5,7 Although ELP is uncommon, its prevalence is higher in specific at-risk 83 populations; a study published in 1951 described ELP in 15% of 389 chronically-ill patients.8 Evidence of 84 lipoid pneumonia was found in 1-2.5% of subjects included in past autopsy series.9 Features inherent to 85 ELP make the ascertainment of its prevalence and incidence difficult: 1) affected individuals may never 86 come to clinical attention due to lack of symptoms, and 2) when ELP manifests clinically, it may be 5 87 erroneously diagnosed as another respiratory illness, e.g., community-acquired pneumonia, owing to 88 similar nonspecific manifestations, and clinicians’ unfamiliarity with ELP. Many cases of ELP are 89 unsuspected prior to lung biopsy, and some are diagnosed at autopsy. 2,10 90 When the diagnosis of ELP is established, management consists of supportive care and discontinuation of 91 the implicated exposure, when one is identifiable. However, the clinical and radiologic evolution of ELP 92 remains unclear. In this retrospective study, we sought to clarify the presenting clinical and radiologic 93 features, causative agents, and subsequent course of ELP. 94 Study Design and Methods: 95 We searched the pathology, radiology and autopsy reports in Mayo Clinic’s electronic medical records for 96 the diagnosis “lipoid pneumonia”. We included adult patients (≥18 years old) who fulfilled at least one of 97 the following criteria: 1) lipoid pneumonia on lung biopsy (Figure 1), 2) lipid-laden macrophages on 98 cytological examination of bronchoalveolar lavage (BAL) fluid, and/or 3) chest CT scan depicting one or 99 more parenchymal lesion(s) with fatty-attenuation in a patient with an ingestion known to cause ELP 100 (Figure 2). Two additional requirements needed to be met for inclusion: 1) ELP was considered the most 101 likely diagnosis by the treating clinician and other potential explanations for the pulmonary process were 102 adequately excluded, and 2) conditions known to cause endogenous lipoid pneumonia (obstructive airway Journal Pre-proof2,3 103 lesions, lipid storage disorders, and pulmonary alveolar proteinosis) were absent. Similar criteria for 104 ELP have been employed in prior reports.3,5,10 105 Thirty-seven electronic charts of patients seen at the three Mayo Clinic sites (Minnesota, Arizona and 106 Florida) were identified. Three patients did not meet our inclusion criteria and were excluded; one patient 107 was a child, and two others had other more likely explanations for their clinical and radiologic findings: 108 pulmonary vasculitis, and cryptogenic organizing pneumonia, respectively. 6 109 All patient charts were manually reviewed; demographic, clinical, laboratory, radiologic and pulmonary 110 function data were extracted. Severity of respiratory impairment was classified based on forced expiratory 111 volume in 1 st second (FEV1). The chest CT scan closest to the date of diagnosis was selected as the 112 “initial” study, and the most recent chest CT scan was selected as the “follow-up” study. 113 Chest CT scans were reviewed by two board-certified thoracic radiologists, both of whom were blinded to 114 the underlying diagnosis.
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