Respiratory Manifestations in Primary Immunodeficiencies: Findings From a Pediatric and Adult Cohort

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(b) Age distribution at diagnosis according to different IEI. (c) Diagnostic delay. (d) Distribution of respiratory infections among the three groups. (e) Upper respiratory tract infections within Group 1. (f) Lower respiratory tract infections within Group 1. (g) Prevalence of rhinosinusitis in Group 2. (h) Distribution of respiratory infections within Group 3. *P-value≤.05, ** P-value≤.01, *** P-value≤.0001." ] ] ] "textoCompleto" => "Primary immunodeficiencies (PIDs) are a heterogeneous group of more than 400 inherited immune system disorders, with overall prevalence 1/1000–1/5000.<a class="elsevierStyleCrossRef" href="#bib0050">1</a> At any age, recurrent-to-persistent respiratory infections are often the first presenting sign of PIDs.<a class="elsevierStyleCrossRef" href="#bib0055">2</a> Poor defense from opportunistic or non-opportunistic pathogens, as well as non-infectious complications may significantly impact morbidity and mortality of the conditions, even when early detected.<a class="elsevierStyleCrossRef" href="#bib0060">3</a>In PIDs, type, outcome and severity of the underlying defect might influence type and severity of patients’ respiratory phenotypes, but only few studies documented this.<a class="elsevierStyleCrossRef" href="#bib0065">4</a>In this report, we compared the respiratory manifestations and the chest imaging findings from a cohort of pediatric and adult patients from a tertiary level hospital, a major referral for PID, located in Campania region, in Southern Italy. In order to describe the respiratory phenotypes in different PID groups and to investigate their prevalence, we conducted a retrospective study over a three-year period, from mid-2018 to mid-2020 and created a database of 269 patients with PID including 182 children (mean age, 9±4 years; 67% of the total) and 87 adults (mean age, 20±6.5 years; 33% of the total). According to the underlying diagnosis, patients were allocated to three groups: cellular immunity defects [Group 1, n=48, 17.9% of the total, including Ataxia–Teleangiectasia (A–T), partial DiGeorge syndrome (pDGS), or Severe Combined Immune-deficiencies (SCID) before treatment]; humoral immunity defects [Group 2, n=203, 75.5% of the total, including Common Variable Immune-deficiency (CVID), X-linked Agammaglobulinemia (XLA), or selective IgA Deficiency (sIgAD)]; innate immunity defects [Group 3, n=18, 6.6% of the total, including Chronic Granulomatous Disease (CGD), STAT1 gain of function, hyper IgE Syndrome, MYD88 Deficiency, or congenital neutropenia]. We analyzed variables including gender, type of PID, age at diagnosis, age at onset of respiratory symptoms, diagnostic delay (the time elapsed between the onset of respiratory symptoms and the diagnosis of PID), history of upper (i.e. rhinosinusitis and/or otitis) or lower (i.e. bronchitis and/or pneumonia) airway infections, chest imaging phenotypes (at X-ray or Computed Tomography or Magnetic Resonance Imaging).<a class="elsevierStyleCrossRef" href="#bib0070">5</a> In our study population, Groups 1 and 3 included only children, while Group 2 was composed of both pediatric and adult patients with humoral immunity defects.Comparisons between groups were performed applying t-test for numerical variables and chi-test for categorical variables.The age at onset of respiratory symptoms was significantly higher in Group 2 than Groups 1 and 3 (P<.001; <a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>A). In more than half of the cases, a diagnosis of cellular immunity defect was established, in nearly 90%, of cases in the first decade (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>B). A wide variability of age at diagnosis was found in cases with humoral immunity defects, while patients with defects of innate immunity were diagnosed always before adolescence. The diagnostic delay was lower in patients with cellular immunity defects than in other groups (P<.01; <a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>C). Rhinosinusitis was more common in Group 2, with a significant difference when compared to Groups 1 and 3 (P<.05), and otitis was more frequent in Group 1. No significant difference in the prevalence of lower airway infections was found among all groups (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>D).<elsevierMultimedia ident="fig0005"></elsevierMultimedia>In order to investigate whether a different localization of airway infections in each disease group was associated with a specific immunological defect, we compared the prevalence within subgroups. In Group 1, upper airway infections were more frequent in A-T patients, while lower airway infections were more prevalent among SCID patients (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>E–F). Within the pediatric patients from Group 2, we compared the prevalence among XLA, CVID and sIgAD, and found that rhinosinusitis was more prevalent in the CVID subgroup (P<.05) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>G). Within Group 3, patients with CGD or other innate immunity disorders showed higher prevalence of pneumonia in the CGD subgroup (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>H).Of 269 patients, 197 (72.3%) underwent chest imaging examinations at the time of database creation. Four major categories of radiological changes were analyzed: consolidation, bronchiectasis, interstitial lung disease and Granulomatous and Lymphocytic Interstitial Lung Disease (GLILD).<a class="elsevierStyleCrossRef" href="#bib0075">6</a>Consolidation was more common among patients with cellular and innate immunity defects than in those with humoral immunity defects (P<.05). Prevalence of bronchiectasis was significantly higher in patients with humoral immunity defects compared to cellular immunity defects (P<.05). As the only group including both pediatric and adult patients is Group 2, we compared the general characteristics, clinical manifestations and chest imaging findings between the two age subgroups (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). As expected, adults with humoral immunity defects had a straightforward delay in the diagnosis of PID (6.1 versus 1.3 years in the pediatric population; P<.00001), while children showed a fairly higher rate of otitis than adults (55% versus 6.8%, respectively; P<.00001). Finally, no noteworthy difference was found in the prevalence of radiological findings between the two age subgroups, except for GLILD that was found in 28 CVID patients of which 93% were adults (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>).<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>Overall, our report reveals, as expected, that in cases with the most severe PID, such as cellular or innate immunity defects, respiratory symptoms start early.<a class="elsevierStyleCrossRef" href="#bib0080">7</a> This resulted in a prompt immunological diagnosis. Patients with humoral immunity defects usually present with mild upper respiratory tract infections which might be, indeed, overlooked, thus delaying the referral to the immunology center. The association with other non-immunological features may also reduce the diagnostic delay in selected cases (A-T or DGS). Moreover, the finding that rhinosinusitis is the most prevalent respiratory manifestation in CVID (Group 2) or A-T patients (Group 1) might be explained by the long-lasting T-cell defect in both disorders, rather than by the severity of T-cell impairment or the selective humoral immunity defects. While we did not find any significant difference in lower respiratory tract infections distribution among all groups, rhinosinusitis associated with GLILD appeared a distinctive feature of the respiratory phenotype of CVID. Early recurrent sinopulmonary infections are extremely common in CVID, and a high proportion of cases may develop chronic lung disease with bronchiectasis.<a class="elsevierStyleCrossRef" href="#bib0060">3</a> A host of other systemic manifestations, including autoimmune disorders and lymphoproliferation may also occur which significantly worsen patients’ morbidity and mortality. Prognosis of CVID is largely affected by GLILD, a lymphoproliferative disorder characterized by progressive lung damage including airway disease and the need for continuous chest treatment.<a class="elsevierStyleCrossRefs" href="#bib0085">8,9</a>Although the hallmarks of respiratory manifestations in the different groups of PID are already known, our report, through a stratified sampling method on a single-center cohort including both pediatric and adult patients, highlights that rhinosinusitis and GLILD are almost exclusively found in CVID, suggesting that the contextual presence of a cell-mediated defect of long duration in association with the humoral defect is necessary for its development. Hopefully, the precocious identification of the lung disease may help improve the final outcome of the disease and more importantly may significantly impact the quality of life of patients with PID.FundingThis research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.Conflicts of InterestThe authors declare to have no conflict of interest directly or indirectly related to the manuscript contents." "textoCompletoSecciones" => array:1 [ "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0005" "titulo" => "Funding" ] 1 => array:2 [ "identificador" => "sec0010" "titulo" => "Conflicts of Interest" ] 2 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "NotaPie" => array:1 [ 0 => array:3 [ "etiqueta" => "◊" "nota" => "Both share correspondence co-authorship." "identificador" => "fn1" ] ] "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 3016 "Ancho" => 2925 "Tamanyo" => 469645 ] ] "descripcion" => array:1 [ "en" => "(a) Age of onset of respiratory symptoms. (b) Age distribution at diagnosis according to different IEI. (c) Diagnostic delay. (d) Distribution of respiratory infections among the three groups. (e) Upper respiratory tract infections within Group 1. (f) Lower respiratory tract infections within Group 1. (g) Prevalence of rhinosinusitis in Group 2. (h) Distribution of respiratory infections within Group 3. *P-value≤.05, ** P-value≤.01, *** P-value≤.0001." ] ] 1 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "Abbreviations: GLILD, granulomatous lymphocytic interstitial lung disease." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Whole Group \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Children \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Adults \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">P \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " colspan="5" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">General characteristics</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Patients, N \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">203 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">116 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">87 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">N.A. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Gender, % males \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">52 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">79 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">44 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">.017 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Mean age at last clinical follow-up, years \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">30 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">16 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">44 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><.00001 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Diagnostic delay, years \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">9.6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1.3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">6.1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><.00001 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " colspan="5" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"></td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " colspan="5" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Clinical manifestations</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Rhinosinusitis, % \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">62 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">63 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">60 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">.78 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Otitis, % \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">34 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">55 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">6.8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><.00001 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Bronchitis, % \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">48 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">60.9 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">.24 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Pneumonia, % \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">56 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">43 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">57 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">.059 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " colspan="5" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"></td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " colspan="5" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Chest imaging findings</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Patients who underwent imaging, N \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">145 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">93 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">52 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">.002 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Collapse/consolidation, % \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">33 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">30 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">38 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">.41 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Bronchiectasis, % \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">24 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">22 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">28 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">.52 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Interstitial lung disease, % \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">9 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8.6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">9 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">.92 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">GLILD, % \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><.00001 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab2738037.png" ] ] ] ] "descripcion" => array:1 [ "en" => "General Characteristics, Clinical Manifestations and Chest Imaging Findings of Group 2 Including Pediatric and Adult Patients With Humoral Immunity Defects; the Comparison Between the Two Age Groups, Calculated Using Either t-test or chi-test, Are Shown on the Right Column." ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:9 [ 0 => array:3 [ "identificador" => "bib0050" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Human inborn errors of immunity: 2019 update on the classification from the international union of immunological societies expert committee" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "S.G. Tangye" 1 => "W. Al-Herz" 2 => "A. Bousfiha" 3 => "T. Chatila" 4 => "C. Cunningham-Rundles" 5 => "A. Etzioni" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1007/s10875-019-00737-x" "Revista" => array:6 [ "tituloSerie" => "J Clin Immunol" "fecha" => "2020" "volumen" => "40" "paginaInicial" => "24" "paginaFinal" => "64" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/31953710" "web" => "Medline" ] ] ] ] ] ] ] ] 1 => array:3 [ "identificador" => "bib0055" "etiqueta" => "2" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Respiratory disease in common variable immunodeficiency and other primary immunodeficiency disorders" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "F.A. Hampson" 1 => "A. Chandra" 2 => "N.J. Screaton" 3 => "A. Condliffe" 4 => "D.S. Kumararatne" 5 => "A.R. 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Scientific Letter

Respiratory Manifestations in Primary Immunodeficiencies: Findings From a Pediatric and Adult Cohort

Manifestaciones respiratorias en las inmunodeficiencias primarias: hallazgo de una cohorte pediátrica y adulta

Roberta Romanoa, Melissa Borrellia, Emilia Cirilloa, Giuliana Giardinoa, Giuseppe Spadarob, Ludovica Crescenzib, Ilaria Mormileb, Laura Vendittoa, Claudio Pignataa,◊,

Corresponding author

pignata@unina.it

Corresponding authors.

, Francesca Santamariaa,◊,

Corresponding author

santamar@unina.it

Corresponding authors.

a Department of Translational Medical Sciences – Section of Pediatrics, University of Naples Federico II, Naples, Italy

b Department of Translational Medical Sciences – Center for Basic and Clinical Immunology Research, University of Naples Federico II, Naples, Italy

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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">&#40;a&#41; Age of onset of respiratory symptoms&#46; &#40;b&#41; Age distribution at diagnosis according to different IEI&#46; &#40;c&#41; Diagnostic delay&#46; &#40;d&#41; Distribution of respiratory infections among the three groups&#46; &#40;e&#41; Upper respiratory tract infections within Group 1&#46; &#40;f&#41; Lower respiratory tract infections within Group 1&#46; &#40;g&#41; Prevalence of rhinosinusitis in Group 2&#46; &#40;h&#41; Distribution of respiratory infections within Group 3&#46; &#42;<span class="elsevierStyleItalic">P</span>-value<span class="elsevierStyleHsp" style=""></span>&#8804;<span class="elsevierStyleHsp" style=""></span>&#46;05&#44; &#42;&#42; <span class="elsevierStyleItalic">P</span>-value<span class="elsevierStyleHsp" style=""></span>&#8804;<span class="elsevierStyleHsp" style=""></span>&#46;01&#44; &#42;&#42;&#42; <span class="elsevierStyleItalic">P</span>-value<span class="elsevierStyleHsp" style=""></span>&#8804;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Primary immunodeficiencies &#40;PIDs&#41; are a heterogeneous group of more than 400 inherited immune system disorders&#44; with overall prevalence 1&#47;1000&#8211;1&#47;5000&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">1</span></a> At any age&#44; recurrent-to-persistent respiratory infections are often the first presenting sign of PIDs&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">2</span></a> Poor defense from opportunistic or non-opportunistic pathogens&#44; as well as non-infectious complications may significantly impact morbidity and mortality of the conditions&#44; even when early detected&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">3</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">In PIDs&#44; type&#44; outcome and severity of the underlying defect might influence type and severity of patients&#8217; respiratory phenotypes&#44; but only few studies documented this&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">4</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">In this report&#44; we compared the respiratory manifestations and the chest imaging findings from a cohort of pediatric and adult patients from a tertiary level hospital&#44; a major referral for PID&#44; located in Campania region&#44; in Southern Italy&#46; In order to describe the respiratory phenotypes in different PID groups and to investigate their prevalence&#44; we conducted a retrospective study over a three-year period&#44; from mid-2018 to mid-2020 and created a database of 269 patients with PID including 182 children &#40;mean age&#44; 9<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>4 years&#59; 67&#37; of the total&#41; and 87 adults &#40;mean age&#44; 20<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>6&#46;5 years&#59; 33&#37; of the total&#41;&#46; According to the underlying diagnosis&#44; patients were allocated to three groups&#58; cellular immunity defects &#91;Group 1&#44; <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>48&#44; 17&#46;9&#37; of the total&#44; including Ataxia&#8211;Teleangiectasia &#40;A&#8211;T&#41;&#44; partial DiGeorge syndrome &#40;pDGS&#41;&#44; or Severe Combined Immune-deficiencies &#40;SCID&#41; before treatment&#93;&#59; humoral immunity defects &#91;Group 2&#44; <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>203&#44; 75&#46;5&#37; of the total&#44; including Common Variable Immune-deficiency &#40;CVID&#41;&#44; X-linked Agammaglobulinemia &#40;XLA&#41;&#44; or selective IgA Deficiency &#40;sIgAD&#41;&#93;&#59; innate immunity defects &#91;Group 3&#44; <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>18&#44; 6&#46;6&#37; of the total&#44; including Chronic Granulomatous Disease &#40;CGD&#41;&#44; <span class="elsevierStyleItalic">STAT1</span> gain of function&#44; hyper IgE Syndrome&#44; <span class="elsevierStyleItalic">MYD88</span> Deficiency&#44; or congenital neutropenia&#93;&#46; We analyzed variables including gender&#44; type of PID&#44; age at diagnosis&#44; age at onset of respiratory symptoms&#44; diagnostic delay &#40;the time elapsed between the onset of respiratory symptoms and the diagnosis of PID&#41;&#44; history of upper &#40;i&#46;e&#46; rhinosinusitis and&#47;or otitis&#41; or lower &#40;i&#46;e&#46; bronchitis and&#47;or pneumonia&#41; airway infections&#44; chest imaging phenotypes &#40;at X-ray or Computed Tomography or Magnetic Resonance Imaging&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">5</span></a> In our study population&#44; Groups 1 and 3 included only children&#44; while Group 2 was composed of both pediatric and adult patients with humoral immunity defects&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">Comparisons between groups were performed applying t-test for numerical variables and chi-test for categorical variables&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">The age at onset of respiratory symptoms was significantly higher in Group 2 than Groups 1 and 3 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;001&#59; <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>A&#41;&#46; In more than half of the cases&#44; a diagnosis of cellular immunity defect was established&#44; in nearly 90&#37;&#44; of cases in the first decade &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>B&#41;&#46; A wide variability of age at diagnosis was found in cases with humoral immunity defects&#44; while patients with defects of innate immunity were diagnosed always before adolescence&#46; The diagnostic delay was lower in patients with cellular immunity defects than in other groups &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;01&#59; <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>C&#41;&#46; Rhinosinusitis was more common in Group 2&#44; with a significant difference when compared to Groups 1 and 3 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;05&#41;&#44; and otitis was more frequent in Group 1&#46; No significant difference in the prevalence of lower airway infections was found among all groups &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>D&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0030" class="elsevierStylePara elsevierViewall">In order to investigate whether a different localization of airway infections in each disease group was associated with a specific immunological defect&#44; we compared the prevalence within subgroups&#46; In Group 1&#44; upper airway infections were more frequent in A-T patients&#44; while lower airway infections were more prevalent among SCID patients &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>E&#8211;F&#41;&#46; Within the pediatric patients from Group 2&#44; we compared the prevalence among XLA&#44; CVID and sIgAD&#44; and found that rhinosinusitis was more prevalent in the CVID subgroup &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;05&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>G&#41;&#46; Within Group 3&#44; patients with CGD or other innate immunity disorders showed higher prevalence of pneumonia in the CGD subgroup &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>H&#41;&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">Of 269 patients&#44; 197 &#40;72&#46;3&#37;&#41; underwent chest imaging examinations at the time of database creation&#46; Four major categories of radiological changes were analyzed&#58; consolidation&#44; bronchiectasis&#44; interstitial lung disease and Granulomatous and Lymphocytic Interstitial Lung Disease &#40;GLILD&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">6</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall">Consolidation was more common among patients with cellular and innate immunity defects than in those with humoral immunity defects &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;05&#41;&#46; Prevalence of bronchiectasis was significantly higher in patients with humoral immunity defects compared to cellular immunity defects &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;05&#41;&#46; As the only group including both pediatric and adult patients is Group 2&#44; we compared the general characteristics&#44; clinical manifestations and chest imaging findings between the two age subgroups &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; As expected&#44; adults with humoral immunity defects had a straightforward delay in the diagnosis of PID &#40;6&#46;1 <span class="elsevierStyleItalic">versus</span> 1&#46;3 years in the pediatric population&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;00001&#41;&#44; while children showed a fairly higher rate of otitis than adults &#40;55&#37; <span class="elsevierStyleItalic">versus</span> 6&#46;8&#37;&#44; respectively&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;00001&#41;&#46; Finally&#44; no noteworthy difference was found in the prevalence of radiological findings between the two age subgroups&#44; except for GLILD that was found in 28 CVID patients of which 93&#37; were adults &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0045" class="elsevierStylePara elsevierViewall">Overall&#44; our report reveals&#44; as expected&#44; that in cases with the most severe PID&#44; such as cellular or innate immunity defects&#44; respiratory symptoms start early&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">7</span></a> This resulted in a prompt immunological diagnosis&#46; Patients with humoral immunity defects usually present with mild upper respiratory tract infections which might be&#44; indeed&#44; overlooked&#44; thus delaying the referral to the immunology center&#46; The association with other non-immunological features may also reduce the diagnostic delay in selected cases &#40;A-T or DGS&#41;&#46; Moreover&#44; the finding that rhinosinusitis is the most prevalent respiratory manifestation in CVID &#40;Group 2&#41; or A-T patients &#40;Group 1&#41; might be explained by the long-lasting T-cell defect in both disorders&#44; rather than by the severity of T-cell impairment or the selective humoral immunity defects&#46; While we did not find any significant difference in lower respiratory tract infections distribution among all groups&#44; rhinosinusitis associated with GLILD appeared a distinctive feature of the respiratory phenotype of CVID&#46; Early recurrent sinopulmonary infections are extremely common in CVID&#44; and a high proportion of cases may develop chronic lung disease with bronchiectasis&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">3</span></a> A host of other systemic manifestations&#44; including autoimmune disorders and lymphoproliferation may also occur which significantly worsen patients&#8217; morbidity and mortality&#46; Prognosis of CVID is largely affected by GLILD&#44; a lymphoproliferative disorder characterized by progressive lung damage including airway disease and the need for continuous chest treatment&#46;<a class="elsevierStyleCrossRefs" href="#bib0085"><span class="elsevierStyleSup">8&#44;9</span></a></p><p id="par0050" class="elsevierStylePara elsevierViewall">Although the hallmarks of respiratory manifestations in the different groups of PID are already known&#44; our report&#44; through a stratified sampling method on a single-center cohort including both pediatric and adult patients&#44; highlights that rhinosinusitis and GLILD are almost exclusively found in CVID&#44; suggesting that the contextual presence of a cell-mediated defect of long duration in association with the humoral defect is necessary for its development&#46; Hopefully&#44; the precocious identification of the lung disease may help improve the final outcome of the disease and more importantly may significantly impact the quality of life of patients with PID&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Funding</span><p id="par0055" class="elsevierStylePara elsevierViewall">This research did not receive any specific grant from funding agencies in the public&#44; commercial&#44; or not-for-profit sectors&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Conflicts of Interest</span><p id="par0060" class="elsevierStylePara elsevierViewall">The authors declare to have no conflict of interest directly or indirectly related to the manuscript contents&#46;</p></span></span>"
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          "leyenda" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">Abbreviations</span>&#58; GLILD&#44; granulomatous lymphocytic interstitial lung disease&#46;</p>"
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Mean age at last clinical follow-up&#44; years&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">30&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">16&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">44&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#60;&#46;00001&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Diagnostic delay&#44; years&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">9&#46;6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&#46;3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6&#46;1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#60;&#46;00001&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="5" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="5" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Clinical manifestations</span></td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Rhinosinusitis&#44; &#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">62&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">63&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">60&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;78&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Otitis&#44; &#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">34&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">55&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6&#46;8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#60;&#46;00001&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Bronchitis&#44; &#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">50&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">48&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">60&#46;9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;24&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Pneumonia&#44; &#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">56&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">43&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">57&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;059&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="5" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="5" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Chest imaging findings</span></td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Patients who underwent imaging&#44; <span class="elsevierStyleItalic">N</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">145&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">93&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">52&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;002&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Collapse&#47;consolidation&#44; &#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">33&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">30&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">38&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;41&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Bronchiectasis&#44; &#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">24&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">22&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">28&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;52&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Interstitial lung disease&#44; &#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">8&#46;6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;92&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>GLILD&#44; &#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">19&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">50&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#60;&#46;00001&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">General Characteristics&#44; Clinical Manifestations and Chest Imaging Findings of Group 2 Including Pediatric and Adult Patients With Humoral Immunity Defects&#59; the Comparison Between the Two Age Groups&#44; Calculated Using Either t-test or chi-test&#44; Are Shown on the Right Column&#46;</p>"
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0015"
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                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Human inborn errors of immunity&#58; 2019 update on the classification from the international union of immunological societies expert committee"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:6 [
                            0 => "S&#46;G&#46; Tangye"
                            1 => "W&#46; Al-Herz"
                            2 => "A&#46; Bousfiha"
                            3 => "T&#46; Chatila"
                            4 => "C&#46; Cunningham-Rundles"
                            5 => "A&#46; Etzioni"
                          ]
                        ]
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                    ]
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                    0 => array:2 [
                      "doi" => "10.1007/s10875-019-00737-x"
                      "Revista" => array:6 [
                        "tituloSerie" => "J Clin Immunol"
                        "fecha" => "2020"
                        "volumen" => "40"
                        "paginaInicial" => "24"
                        "paginaFinal" => "64"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/31953710"
                            "web" => "Medline"
                          ]
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                      ]
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              "identificador" => "bib0055"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Respiratory disease in common variable immunodeficiency and other primary immunodeficiency disorders"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:6 [
                            0 => "F&#46;A&#46; Hampson"
                            1 => "A&#46; Chandra"
                            2 => "N&#46;J&#46; Screaton"
                            3 => "A&#46; Condliffe"
                            4 => "D&#46;S&#46; Kumararatne"
                            5 => "A&#46;R&#46; Exley"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:6 [
                        "tituloSerie" => "Clin Radiol"
                        "fecha" => "2012"
                        "volumen" => "67"
                        "paginaInicial" => "587"
                        "paginaFinal" => "595"
                        "itemHostRev" => array:3 [
                          "pii" => "S0967586813004335"
                          "estado" => "S300"
                          "issn" => "09675868"
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              "identificador" => "bib0060"
              "etiqueta" => "3"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "The lung in primary immunodeficiencies&#58; new concepts in infection and inflammation"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:4 [
                            0 => "U&#46; Baumann"
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Article information

ISSN: 03002896
Original language: English

DOI:10.1016/j.arbres.2021.01.019

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Year/Month	Html	Pdf	Total

2024 November	8	5	13
2024 October	50	28	78
2024 September	64	11	75
2024 August	73	39	112
2024 July	47	26	73
2024 June	60	17	77
2024 May	89	29	118
2024 April	45	25	70
2024 March	77	23	100
2024 February	51	25	76
2024 January	54	28	82
2023 December	70	24	94
2023 November	74	39	113
2023 October	59	36	95
2023 September	55	31	86
2023 August	56	25	81
2023 July	63	32	95
2023 June	43	8	51
2023 May	63	21	84
2023 April	52	43	95
2023 March	89	38	127
2023 February	77	21	98
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2022 December	81	40	121
2022 November	108	48	156
2022 October	74	28	102
2022 September	64	30	94
2022 August	57	47	104
2022 July	47	44	91
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2022 April	63	37	100
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2022 January	2	2	4
2021 December	3	0	3
2021 November	24	10	34
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