Letter to the Editor
Follicular bronchiolitis, a frequently misdiagnosed condition
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Serras, J.A. Oliveira, L. Pereira, C. Barreto" "autores" => array:4 [ 0 => array:2 [ "nombre" => "I." "apellidos" => "Serras" ] 1 => array:2 [ "nombre" => "J.A." "apellidos" => "Oliveira" ] 2 => array:2 [ "nombre" => "L." "apellidos" => "Pereira" ] 3 => array:2 [ "nombre" => "C." "apellidos" => "Barreto" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S2531043719300169?idApp=UINPBA00004E" "url" => "/25310437/0000002500000001/v1_201902260629/S2531043719300169/v1_201902260629/en/main.assets" ] "en" => array:15 [ "idiomaDefecto" => true "cabecera" => "<span class="elsevierStyleTextfn">Letter to the Editor</span>" "titulo" => "Follicular bronchiolitis, a frequently misdiagnosed condition" "tieneTextoCompleto" => true "saludo" => "Dear Editor," "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "62" "paginaFinal" => "64" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "A.C. Duarte, A. Cordeiro, J. Soares, P. Gonçalves" "autores" => array:4 [ 0 => array:4 [ "nombre" => "A.C." "apellidos" => "Duarte" "email" => array:1 [ 0 => "catarinaduarte89@gmail.com" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "A." "apellidos" => "Cordeiro" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 2 => array:3 [ "nombre" => "J." "apellidos" => "Soares" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "P." "apellidos" => "Gonçalves" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Rheumatology Department, Hospital Garcia de Orta, Almada, Portugal" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Pneumology Department, Hospital Garcia de Orta, Almada, Portugal" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 975 "Ancho" => 1505 "Tamanyo" => 219417 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Chest computed tomography at diagnosis (A, B) and 8 months after treatment with steroids and clarithromycin (C, D). Peribronchovascular micronodules and dilated and thick-walled bronchioles with a fluffy tree-in-bud similar to “cotton-in-bud” present at diagnosis (A, B), resolved after treatment with steroids in association with 4 months of clarithromycin (C, D).</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Rheumatoid arthritis (RA) is associated with several extra-articular manifestations, including lung disease. Pulmonary manifestations can result from parenchyma, airways, pleura or vasculature involvement and are a major contributor to morbimortality.<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">1</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Follicular bronchiolitis (FB) is a small airways disease reported in RA patients, which results from hyperplasia of bronchus-associated lymphoid tissue.</p><p id="par0015" class="elsevierStylePara elsevierViewall">We report the case of a 49-years-old Caucasian female, who presented with an erosive polyarthritis of hands and wrists at the age of 25, with positive anti-citrullinated protein antibodies and negative rheumatoid factor. A diagnosis of RA was assumed, without extra-articular involvement. She had previously received hydroxychloroquine (stopped for retinopathy), infliximab and adalimumab (both stopped due to adverse reaction) and etanercept (stopped for inefficacy) and was currently under prednisolone (PDN) 5<span class="elsevierStyleHsp" style=""></span>mg/day and methotrexate (MTX) 20<span class="elsevierStyleHsp" style=""></span>mg/week, after one cycle of rituximab.</p><p id="par0020" class="elsevierStylePara elsevierViewall">She remained in clinical remission until 4 years ago, when she noticed persistent dry cough, with periods of fever and sputum, and a rise in inflammatory markers. Sequential chest X-rays had migratory pulmonary infiltrates and computed tomography (CT) showed peribronchovascular micronodules, dilated and thick-walled bronchioles with a fluffy tree-in-bud (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>A, B). The patient was recurrently diagnosed with presumed chest infections and treated with multiple cycles of antibiotics; MTX was suspended and PDN raised to 10<span class="elsevierStyleHsp" style=""></span>mg/day.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">Due to symptoms’ persistence, with concomitant anorexia and loss of 10<span class="elsevierStyleHsp" style=""></span>kg in 2 months, she was admitted into hospital for further evaluation. She denied smoking habits or occupational/environmental exposures. On examination she had a body mass index of 21<span class="elsevierStyleHsp" style=""></span>kg/m<span class="elsevierStyleSup">2</span>, pulmonary auscultation with subtle crackles in both lung bases, without arthritis, lymphadenopathies or organomegaly. Pulmonary function tests (PFTs), including carbon monoxide diffusing capacity (DLCO), were normal, without hypoxemia. Complementary exams showed negative viral serology (human immunodeficiency virus and hepatitis B/C), negative serology for acute infection by <span class="elsevierStyleItalic">Mycoplasma pneumoniae</span>, normal serum proteinogram, normal immunoglobulins levels and negative antinuclear antibodies. Abdominal/pelvic CT scan and endoscopy were normal. She was submitted to bronchoscopy with unspecific inflammatory changes; bronchoalveolar lavage had normal cellularity, without identification of any microorganisms, including <span class="elsevierStyleItalic">Mycobacterium tuberculosis</span>. Transbronchial biopsy had nonspecific lymphocytic infiltrate, forming small aggregates, without vasculitis, granulomas or neoplastic tissue. The patient was then submitted to surgical lung biopsy that demonstrated lymphoid follicles with peribronchiolar germinal centers and associated bronchiole constriction (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>), making the diagnosis of FB. The patient started PDN (0.75<span class="elsevierStyleHsp" style=""></span>mg/kg/day), with clinical and radiological improvement, but one month later she developed steroid-associated neuropsychiatric symptoms and PDN was tapered. However, fever and sputum recurred, without evidence of infection. BF relapse was assumed and the addition of a second drug was discussed between rheumatologists and pulmonologists. Due to the absence of articular activity and considering the previous adverse events experienced by the patient with immunosuppressive drugs and the fear of these drugs to worsen lung disease, clarithromycin (500<span class="elsevierStyleHsp" style=""></span>mg/day) was added for 4 months, with progressive symptomatic improvement and PDN tapering. Four months later complete resolution of chest CT alterations was noted (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>C, D) and PDN was stopped. The patient remains currently under no treatment for 10 months, without evidence of BF recurrence and no need for further immunosuppression.</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0030" class="elsevierStylePara elsevierViewall">FB was first described in 1979 by Epler et al.,<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">2</span></a> after noticing extensive proliferation of lymphoid follicles in the bronchiolar walls of 2 patients with RA and eosinophilic fasciitis treated with <span class="elsevierStyleSmallCaps">d</span>-penicillamine.</p><p id="par0035" class="elsevierStylePara elsevierViewall">In 1985 Yousem et al.<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">3</span></a> identified three clinicopathological groups of FB. The first two included FB secondary to connective tissue disease (CTD) and congenital/acquired immunodeficiency, respectively, and the third was considered a “primary/idiopathic” subtype.</p><p id="par0040" class="elsevierStylePara elsevierViewall">Patients may present with persistent cough (occasionally productive), breathlessness on exertion, fever, weight loss and recurrent chest infections/sinusitis.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">4</span></a></p><p id="par0045" class="elsevierStylePara elsevierViewall">Chest X-ray can be normal, but lung hyperinflation due to air trapping, small nodules, reticular, or reticulonodular infiltrates also occur.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">4</span></a> CT findings include centrilobular and peribronchial micronodules associated with patchy ground-glass opacities.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">4</span></a> Some patients also present a tree-in-bud pattern with a “cotton-in-bud” appearance.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">4</span></a></p><p id="par0050" class="elsevierStylePara elsevierViewall">PFTs can show a normal, restrictive or obstructive pattern,<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">4,5</span></a> sometimes with reduced DLCO.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">5</span></a> The diagnosis is histological, consisting of hyperplasic lymphoid follicles with reactive germinal centers along small airways.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">5</span></a></p><p id="par0055" class="elsevierStylePara elsevierViewall">Treatment of FB usually includes steroids, mostly prednisolone 1<span class="elsevierStyleHsp" style=""></span>mg/kg/day.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">5</span></a> Relapse when tapering steroids can occur and the addition of a steroid-sparing drug is necessary. In secondary FB, treatment is usually aimed to manage the underlying disease. The first cases of RA-related FB successfully treated with macrolides were reported in 1996<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">6</span></a> and later corroborated in a case report.<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">7</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall">FB is generally associated with a good prognosis, without any related deaths reported. However, younger patients with an underlying immunodeficiency tend to have more severe disease.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">4</span></a></p><p id="par0065" class="elsevierStylePara elsevierViewall">In conclusion, lung involvement should be considered as a differential diagnosis in patients with CTD presenting with respiratory symptoms. FB is commonly misdiagnosed as recurrent chest infections and can be extremely challenging for the clinician. Macrolides have anti-inflammatory/immunomodulatory properties and their potential role in FB was reinforced in this work.</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Conflicts of interest</span><p id="par0070" class="elsevierStylePara elsevierViewall">The authors have no conflicts of interest to declare.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0005" "titulo" => "Conflicts of interest" ] 1 => array:2 [ "identificador" => "xack394424" "titulo" => "Acknowledgements" ] 2 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 975 "Ancho" => 1505 "Tamanyo" => 219417 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Chest computed tomography at diagnosis (A, B) and 8 months after treatment with steroids and clarithromycin (C, D). Peribronchovascular micronodules and dilated and thick-walled bronchioles with a fluffy tree-in-bud similar to “cotton-in-bud” present at diagnosis (A, B), resolved after treatment with steroids in association with 4 months of clarithromycin (C, D).</p>" ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 681 "Ancho" => 905 "Tamanyo" => 192776 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Hematoxylin and eosin-stained slide (40×) of patient's lung tissue, demonstrating hyperplastic lymphoid follicles with peribronchiolar germinal centers and bronchiole narrowing.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:7 [ 0 => array:3 [ "identificador" => "bib0040" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Rheumatoid arthritis-associated lung disease" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:4 [ 0 => "M. Shaw" 1 => "B.F. Collins" 2 => "L.A. Ho" 3 => "G. Raghu" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1183/09059180.00008014" "Revista" => array:6 [ "tituloSerie" => "Eur Respir Rev" "fecha" => "2015" "volumen" => "24" "paginaInicial" => "1" "paginaFinal" => "16" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/25726549" "web" => "Medline" ] ] ] ] ] ] ] ] 1 => array:3 [ "identificador" => "bib0045" "etiqueta" => "2" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Bronchiolitis and bronchitis in connective tissue disease. A possible relationship to the use of penicillamine" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:6 [ 0 => "G.R. Epler" 1 => "G.L. Snider" 2 => "E.A. Gaensler" 3 => "E.S. Cathcart" 4 => "M.X. FitzGerald" 5 => "C.B. 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Carrington" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "Hum Pathol" "fecha" => "1985" "volumen" => "16" "paginaInicial" => "700" "paginaFinal" => "706" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/4007845" "web" => "Medline" ] ] ] ] ] ] ] ] 3 => array:3 [ "identificador" => "bib0055" "etiqueta" => "4" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Follicular bronchiolitis: a literature review" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:4 [ 0 => "B. Tashtoush" 1 => "N.C. Okafor" 2 => "J.F. Ramirez" 3 => "L. 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Iwata" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1164/ajrccm.154.5.8912776" "Revista" => array:6 [ "tituloSerie" => "Am J Respir Crit Care Med" "fecha" => "1996" "volumen" => "154" "paginaInicial" => "1531" "paginaFinal" => "1536" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/8912776" "web" => "Medline" ] ] ] ] ] ] ] ] 6 => array:3 [ "identificador" => "bib0070" "etiqueta" => "7" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Successful teatment of follicular bronchiolitis with macrolide" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "M.R. Aerni" 1 => "R. Vassallo" 2 => "J.H. Ryu" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:4 [ "tituloSerie" => "Chest" "fecha" => "2005" "volumen" => "128" "paginaInicial" => "428S" ] ] ] ] ] ] ] ] ] ] "agradecimientos" => array:1 [ 0 => array:4 [ "identificador" => "xack394424" "titulo" => "Acknowledgements" "texto" => "<p id="par0075" class="elsevierStylePara elsevierViewall">Mónica Cardoso, Department of Anatomic Pathology, Hospital Santa Maria, Centro Hospitalar Lisboa Norte.</p>" "vista" => "all" ] ] ] "idiomaDefecto" => "en" "url" => "/25310437/0000002500000001/v1_201902260629/S2531043719300170/v1_201902260629/en/main.assets" "Apartado" => array:4 [ "identificador" => "72880" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Letters to the Editor" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/25310437/0000002500000001/v1_201902260629/S2531043719300170/v1_201902260629/en/main.pdf?idApp=UINPBA00004E&text.app=https://journalpulmonology.org/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S2531043719300170?idApp=UINPBA00004E" ]
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| 2020 February | 133 | 27 | 160 |
| 2020 January | 129 | 38 | 167 |
| 2019 December | 148 | 33 | 181 |
| 2019 November | 150 | 35 | 185 |
| 2019 October | 171 | 24 | 195 |
| 2019 September | 208 | 32 | 240 |
| 2019 August | 181 | 36 | 217 |
| 2019 July | 112 | 30 | 142 |
| 2019 June | 136 | 34 | 170 |
| 2019 May | 103 | 36 | 139 |
| 2019 April | 109 | 59 | 168 |
| 2019 March | 161 | 84 | 245 |
| 2019 February | 46 | 23 | 69 |
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