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Acute Tropical Pulmonary Eosinophilia. Characterization of the Lower Respiratory Tract Inflammation and Its Response to Therapy

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Acute Tropical Pulmonary Eosinophilia. Characterization of the Lower Respiratory Tract Inflammation and Its Response to Therapy Acute tropical pulmonary eosinophilia. Characterization of the lower respiratory tract inflammation and its response to therapy. P Pinkston, … , T Takemura, G Yenokida J Clin Invest. 1987;80(1):216-225. https://doi.org/10.1172/JCI113050. Research Article Although acute tropical pulmonary eosinophilia (TPE) is well recognized as a manifestation of filarial infection, the processes that mediate the abnormalities of the lung in TPE are unknown. To evaluate the hypothesis that the derangements of the lower respiratory tract in this disorder are mediated by inflammatory cells in the local milieu, we utilized bronchoalveolar lavage to evaluate affected individuals before and after therapy. Inflammatory cells recovered from the lower respiratory tract of individuals with acute, untreated TPE (n = 8) revealed a striking eosinophilic alveolitis, with marked elevations in both the proportion of eosinophils (TPE 54 +/- 5%; normal 2 +/- 5%; P less than 0.001) and the concentration of eosinophils in the recovered epithelial lining fluid (ELF) (TPE 63 +/- 20 X 10(3)/microliter; normal 0.3 +/- 0.1 X 10(3)/microliter; P less than 0.01). Importantly, when individuals (n = 5) with acute TPE were treated with diethylcarbamazine (DEC), there was a marked decrease of the lung eosinophils and concomitant increase in lung function. These observations are consistent with the concept that at least some of the abnormalities found in the lung in acute TPE are mediated by an eosinophil-dominated inflammatory process in the lower respiratory tract. Find the latest version: https://jci.me/113050/pdf Acute Tropical Pulmonary Eosinophilia Characterization of the Lower Respiratory Tract Inflammation and Its Response to Therapy Paula Pinkston, V. K. Vijayan, Thomas B. Nutman, William N. Rom, Kathleen M. O'Donnell, Mary J. Cornelius, V. Kumaraswaml, V. 1. Ferrans, T. Takemura, Gordon Yenokida, K. V. Thirivengadam, S. P. Tripathy, Eric A. Ottesen, and Ronald G. Crystal Pulmonary Branch and Pathology Branch, National Heart, Lung, and Blood Institute and Laboratory ofParasitic Diseases, National Institute ofAllergy and Infectious Diseases, National Institutes ofHealth, Bethesda, Maryland 20892; Tuberculosis Research Center, Indian Council ofMedical Research, Madras, India Abstract cough, dyspnea, nocturnal wheezing, and occasionally fever, an- orexia, and weight loss. Their chest x-rays have diffuse reticu- Although acute tropical pulmonary eosinophilia (TPE) is well lonodular infiltrates, and pulmonary function tests show pri- recognized as a manifestation of filarial infection, the processes marily restrictive defects with mild obstruction (1, 5, 6). Unlike that mediate the abnormalities of the lung in TPE are unknown. results obtained from normals and individuals with other man- To evaluate the hypothesis that the derangements of the lower ifestations of filarial infection, laboratory studies from individuals respiratory tract in this disorder are mediated by inflammatory with acute TPE demonstrate marked peripheral blood eosino- cells in the local milieu we utilized bronchoalveolar lavage to philia and high serum concentrations of IgE and filarial-specific evaluate affected individuals before and after therapy. Inflam- IgG and IgE antibodies (1-5). Although most individuals with inatory cells recovered from the lower respiratory tract of indi- acute TPE have a rapid clinical response to a standard course viduals with acute, untreated TPE (a = 8) revealed a striking of diethylcarbamazine (DEC), with reduced cough and dyspnea, eosinophilic alveolitis, with marked elevations in both the pro- in some individuals the pulmonary disease progresses to a chronic portion of eosinophils (TPE 54±5%; normal 2±5%; P < 0.001) form that results in interstitial fibrosis and permanent loss of and the concentration of eosinophils in the recovered epithelial lung function (6-9). lining fluid (ELF) (TPE 63±20 X 103/Al; normal 03±0.1 The current hypothesis concerning the pathogenesis of TPE X 103/jl; P < 0.01). Importantly, when individuals (a = 5) with suggests that it begins with a lung parenchymal inflammation acute TPE were treated with diethylcarbamazine (DEC), there in persons highly sensitized immunologically to filarial parasites. was a marked decrease of the lung eosinophils and concomitant This inflammation is initiated by microfilariae that have been increase in lung function. These observations are consistent with released from lymphatic dwelling adult worms into the circu- the concept that at least some of the abnormalities found in the lation and cleared in the pulmonary vasculature. According to lung in acute TPE are mediated by an eosinophil-dominated in- this concept, these trapped microfilariae degenerate and release flammatory process in the lower respiratory tract. their antigenic constituents that trigger local inflammatory and immune processes (9-11). Consistent with this concept, very Introduction limited morphologic data has revealed evidence of degenerating microfilariae and diffuse inflammation in the lung parenchyma Tropical pulmonary eosinophilia (TPE)' is an interstitial lung (6, 9, 10, 12, 13). disease that results from a heightened immunologic response to In this context, it is reasonable to hypothesize that the clinical the human filarial parasites, Wuchereria bancrofti and Brugia and physiologic pulmonary abnormalities characteristic of TPE malayi (1). TPE has been reported from filarial endemic regions are mediated, at least in part, by the accumulation of inflam- all over the world, but it is especially prevalent in India and matory cells in the lung parenchyma. As a first step in defining Southeast Asia (1, 2). For reasons that are not yet clear, indi- the inflammatory processes, we have utilized the technique of viduals with TPE respond to filarial infections with vigorous bronchoalveolar lavage to sample and analyze the inflammatory immune responses and severe clinical manifestations that con- cells from the lower respiratory tract of individuals with acute trast markedly with those of most individuals living in the filarial TPE and to correlate the status of this inflammation with the endemic region, who often have filarial infections but commonly changes in lung function observed following therapy with DEC. show highly suppressed immunologic responses and minimal clinical reactions (2-4). Individuals with acute TPE characteristically present with Methods Study population Address repnrnt requests to Dr. Crystal, Building 10, Room 6D03, NIH, All individuals in the study population were residents of the area sur- Bethesda, MD 20892. rounding Madras, India, a region endemic for bancroftian filariasis. Receivedfor publication 2 June 1986 and in revisedform 17 December Clinical evaluation ofeach individual included detailed history, physical 1986. examination, chest x-rays, pulmonary function tests (using P. K. Morgan pulmonary function test apparatus), and blood and stool examinations 1. Abbreviations used in this paper: DEC; diethylcarbamazine; ELF, ep- for the presence ofother parasites. To determine the immunologic status ithelial lining fluid; FEVI, forced expiratory volume in 1 s; TPE, tropical of the study population to filaria, each individual had total serum IgE pulmonary eosinophilia. measured by a standard radioimmunosorbant technique (14) (Pharmacia Fine Chemicals, Piscataway, NJ) and specific IgG filarial antibody de- The Journal of Clinical Investigation, Inc. termined by an enzyme immunoassay (15) using antigen prepared from Volume 80, July 1987, 216-225 Brugia malayi adult worms (14). 216 Pinkston et al. Individuals with acute TPE. The diagnosis of acute TPE was estab- lished in eight individuals based on the accepted criteria (1) of residence 00-o in the endemic area of southern India, recent onset of symptoms, chest 00 __ C. O E x-ray infiltrates, lung function abnormalities, peripheral eosinophilia, 'a-0 A (14 q- O OC.) high total serum IgE, and high serum titers of antifilarial IgG (Table I). c" 0O cO OCO o)I 0r 0 0 00 -E 14 0° 0O In addition, two individuals complained of fever and weight loss. °f CO N Q -9 _ 'or01 Normals. Seven normal nonsmokers from the Madras area were C.) evaluated as controls (Table I). None had respiratory symptoms or ab- OC._ normal physical findings, and all had normal chest x-rays and normal 0 00 pulmonary function tests. None had elevated peripheral blood eosinophil O0- Cu, g C.) counts, high serum concentrations of total IgE, or high concentrations oCO N° of filarial-specific IgG. sz Individuals with elephantiasis. Four individuals who had elephan- (U tiasis, a manifestation of filarial infection with no pulmonary involvement, > oOC N^ _ were also evaluated (Table I). Except for the chronic problem of ele- G +l +1 +1 +J phantiasis, all individuals were asymptomatic at the time of evaluation, with normal chest examinations, chest x-rays and pulmonary function 3 '-E 0.0'a O tests. Mean blood eosinophil counts were normal, but there were mildly 0 elevated serum IgE levels. Antifilarial IgG antibody titers were distinctly 00 00 CO ._ ~0Wo TPE - lower than those of the patients. 00 0000 Individuals with asthma. Since acute TPE and asthma are both char- v - _) acterized by cough, dyspnea, wheezing, and blood eosinophilia, four in- +1 +1 +1 +1 0 dividuals with asthma but no evidence of filarial infection were also Fe C- CT evaluated (Table I). The diagnosis of asthma was based on a history of l 00 _ LoX wheezing, exertional dyspnea, and clinical response to therapy with oral +1 +1 00I+1 +1 bronchodilators.
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