Original article
Applicability of the COPD-LUCSS-DLCO score for patients with chronic obstructive pulmonary disease: Analysis in standard clinical practice conditions
Aplicabilidad del score COPD-LUCSS-DLCO en pacientes con enfermedad pulmonar obstructiva crónica: análisis en condiciones de práctica clínica habitual
J.M. Figueira Gonçalvesa,
, L.I. Pérez Mendezb,c, N. Gurbania, I. García-Talaveraa, J.L. Pérez Pinillad
Corresponding author
a Servicio de Neumología y Cirugía Torácica, Hospital Universitario Nuestra Señora de la Candelaria (HUNSC), Santa Cruz de Tenerife, Spain
b Departamento de Epidemiología Clínica y Bioestadística, Unidad de Investigación, Hospital Universitario Nuestra Señora de la Candelaria (HUNSC) y Gerencia de Atención Primaria AP, Santa Cruz de Tenerife, Spain
c CIBER de Enfermedades Respiratorias, Instituto de Salud Carlos III, Madrid, Spain
d Servicio de Medicina Física y Rehabilitación, Hospital Universitario Nuestra Señora de la Candelaria (HUNSC), Santa Cruz de Tenerife, Spain
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"apellidos" => "Pérez Pinilla" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">d</span>" "identificador" => "aff0020" ] ] ] ] "afiliaciones" => array:4 [ 0 => array:3 [ "entidad" => "Servicio de Neumología y Cirugía Torácica, Hospital Universitario Nuestra Señora de la Candelaria (HUNSC), Santa Cruz de Tenerife, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Departamento de Epidemiología Clínica y Bioestadística, Unidad de Investigación, Hospital Universitario Nuestra Señora de la Candelaria (HUNSC) y Gerencia de Atención Primaria AP, Santa Cruz de Tenerife, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "CIBER de Enfermedades Respiratorias, Instituto de Salud Carlos III, Madrid, Spain" "etiqueta" => "c" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "Servicio de Medicina Física y Rehabilitación, Hospital Universitario Nuestra Señora de la Candelaria (HUNSC), Santa Cruz de Tenerife, Spain" "etiqueta" => "d" "identificador" => "aff0020" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Aplicabilidad del <span class="elsevierStyleItalic">score</span> COPD-LUCSS-DLCO en pacientes con enfermedad pulmonar obstructiva crónica: análisis en condiciones de práctica clínica habitual" ] ] "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" => 1169 "Ancho" => 1468 "Tamanyo" => 63021 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Incidence curves for lung cancer according to the COPD-LUCSS-DLCO score.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Background</span><p id="par0005" class="elsevierStylePara elsevierViewall">It is well known that cigarette smoke is the main causal agent of lung cancer. At present, lung cancer is a silent disease in which the considerable majority of patients (more than 80%) are diagnosed in advanced stages, with a life expectancy at 5 years below 20%.<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">1</span></a> After various screening studies with chest radiography whose results were not favorable,<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">2</span></a> the Early Lung Cancer Action Program (ELCAP) study group<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">3</span></a> and, subsequently, the National Lung Screening Trial (NLST)<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">4</span></a> showed how screening with low-dose computed tomography (LDCT) in high-risk individuals is effective in detecting early stages of the disease, given that it achieved a reduction in mortality of approximately 20%. As a result, the United States Preventive Services Task Force and numerous scientific societies recommended lung cancer screening with LDCT in the United States<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">5</span></a>; however, its implementation in Europe is still debated.</p><p id="par0010" class="elsevierStylePara elsevierViewall">Factors have been identified that can act synergistically with cigarette smoke thereby increasing its effect. Chronic obstructive pulmonary disease (COPD) increases the risk of developing lung cancer by 3- to 5-fold over “healthy” smokers,<a class="elsevierStyleCrossRefs" href="#bib0180"><span class="elsevierStyleSup">6–11</span></a> with the degree of bronchial obstruction, emphysema and chronic bronchitis as independent risk factors for the onset of lung cancer.<a class="elsevierStyleCrossRefs" href="#bib0180"><span class="elsevierStyleSup">6–16</span></a> Risk prediction scales that integrate clinical (age, body mass index [BMI], packs-year index [PYI], family history of lung cancer or COPD), radiological (presence of emphysema in the computed tomography [CT]) and functional variables (reduction in the diffusing capacity of the lungs for carbon monoxide [DLCO]) have shown their usefulness in selecting candidates for lung cancer screening using LDCT.<a class="elsevierStyleCrossRefs" href="#bib0235"><span class="elsevierStyleSup">17–21</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Torres et al.<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">21</span></a> validated the COPD-LUCSS-DLCO scale as a useful tool for identifying patients with COPD at a high risk of dying of lung cancer, who would benefit to a greater extent from a screening program. To date, however, studies have not been conducted on the scale's clinical applicability in patients with COPD in outpatient follow-up.</p><p id="par0020" class="elsevierStylePara elsevierViewall">The aim of our study was to estimate the COPD-LUCSS-DLCO for patients with COPD treated in pulmonology consultations and to determine the incidence of lung cancer in each of the subgroups, in order to develop future strategies for protocolized follow-up that help with the early detection of this cancer in such patients.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Material and methods</span><p id="par0025" class="elsevierStylePara elsevierViewall">An observational, retrospective study was conducted on a cohort of patients diagnosed with COPD in pulmonology follow-up consultations between January 1, 2011 and March 1, 2017 at the University Hospital Nuestra Señora de Candelaria (HUNSC), which has a reference population of 452,000 inhabitants and 22 health areas.</p><p id="par0030" class="elsevierStylePara elsevierViewall">The inclusion criteria were an age greater than 40 years, active smoker or ex-smoker with a PYI ≥10 and a forced expiratory volume in 1 second (FEV<span class="elsevierStyleInf">1</span>) to forced vital capacity (FVC) ratio <70% after administering salbutamol. The exclusion criteria were the presence of chronic respiratory disease caused by something other than COPD, a cancer diagnosis prior to inclusion and the presence of chronic airflow obstruction without exposure to tobacco smoke or a PYI <10.</p><p id="par0035" class="elsevierStylePara elsevierViewall">After study approval by the HUNSC Ethics Committee, we collected the following data from each patient's computerized medical history: (a) COPD diagnosis date; (b) date of respiratory function tests at the time of study inclusion; (c) results of the respiratory function tests regarding FEV<span class="elsevierStyleInf">1</span> (the patients were categorized according to the severity level recorded in the 2009 Global Initiative for Chronic Obstructive Lung Disease [GOLD] guidelines<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">22</span></a>: mild [stage 1] FEV<span class="elsevierStyleInf">1</span> ≥80%; moderate [stage 2] FEV<span class="elsevierStyleInf">1</span> ≥50% and <80%; severe [stage 3] FEV<span class="elsevierStyleInf">1</span> ≥30% and <50%; and very severe [stage 4]) FEV<span class="elsevierStyleInf">1</span> <30%), FVC, FEV<span class="elsevierStyleInf">1</span>/FVC and DLCO using only the respiration test; d) BMI (weight in kg/[height in m]<span class="elsevierStyleSup">2</span>); e) PYI at the time of inclusion; and f) date of cancer diagnosis (any location and lung cancer) up to the end of the follow-up (March 1, 2017). The other covariates recorded were age, sex and age-adjusted Charlson comorbidity index.</p><p id="par0040" class="elsevierStylePara elsevierViewall">Each of the patients had their COPD-LUCSS-DLCO<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">21</span></a> calculated at the time of study inclusion. The scores for each component (BMI <25, PYI >60, age >60 years and DLCO <60%) and the definition of “Low Risk” and “High Risk” are listed in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>.</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Statistical analysis</span><p id="par0045" class="elsevierStylePara elsevierViewall">We performed an initial descriptive analysis using the mean<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>standard deviation (SD) or median and interquartile range (P25–P75) for the numerical variables and percentages (%) for the qualitative variables, with a point estimate and interval of 95% (95% CI) for the prevalence of high risk for lung cancer. To determine the incidence rate of lung cancer, we used the person-time to cancer diagnosis event index or the time to the completion of the follow-up period as the denominator. The Kaplan–Meier survival analysis was employed to compare the incidence of lung cancer between the patients in the low and high-risk categories according to the COPD-LUCSS-DLCO criterion indicated in the Material and Methods section. Statistical significance was determined by the log rank test. We employed a Cox proportional hazards regression to assess the increase in risk adjusted for other variables. All hypothesis tests were bilateral, for a significance level of 5%. The analysis was performed using the statistical program SPSS/PC (version 24.0 for Windows; SPSS, Inc., Chicago, IL) and EPIDAT (version 3.0, Department of Health, Government of Galicia and the Pan American Health Organization).</p></span></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Results</span><p id="par0050" class="elsevierStylePara elsevierViewall">The study included 159 patients with COPD. <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a> lists their characteristics, which include a mean age of 66<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>9 years, a 27% rate of active smokers and a mostly male (82%) proportion. Taking into account the 2009 GOLD classification, 9% of the patients were categorized as GOLD 1, 36% as GOLD 2, 44% as GOLD 3 and 11% as GOLD 4. Sixty-two percent of the patients had a high-risk COPD-LUCSS-DLCO (95% CI 54–69). The median follow-up time was 31 months (range, 15–37).</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">During the study, 12 of the 22 new cases of diagnosed cancer corresponded to lung cancer (9 in high-risk patients and 3 in low-risk patients), the latter of which had an estimated overall rate of 30 cases per 1000 patients with COPD-year (95% CI 16–53). When classifying the patients as high-risk and low-risk, we observed an incidence rate of 44 cases per 1000 patients with COPD-year (95% CI 18–76) and 17 cases per 1000 patients with COPD-year (95% CI 4–50), respectively, showing a high-risk/low-risk ratio of 2.3 (95% CI 0.58–13.3; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>.3155). Seventy-five percent of the lung cancer cases were diagnosed in the first 31 months after inclusion.</p><p id="par0060" class="elsevierStylePara elsevierViewall">Our series’ survival curves showed a higher incidence of lung cancer among the patients categorized as high-risk (<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>.132) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). In the Cox regression analysis, we obtained a crude HR for the high-risk patients versus the low-risk patients of 3.0 (95% CI 0.65–13.9; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>.159). After adjusting the HR, using as covariate the Charlson comorbidity index calculated at the time of inclusion, we obtained an adjusted HR of 4.9 (95% CI 1.02–23.0; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>.046).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Discussion</span><p id="par0065" class="elsevierStylePara elsevierViewall">The following conclusions were extracted from our study: (1) The COPD-LUCSS-DLCO can be a useful tool for detecting patients at a greater risk of lung cancer; (2) the incidence of lung cancer in the high-risk patients was twice that of the low-risk patients, although this increase was not statistically significant; and (3) 62% of the patients with COPD presented a high-risk score.</p><p id="par0070" class="elsevierStylePara elsevierViewall">The association between lung cancer and COPD has been clearly established. Various cohort studies, including lung cancer detection trials, have shown that patients with COPD have 2–4 times the risk of developing lung cancer than those who do not have COPD.<a class="elsevierStyleCrossRefs" href="#bib0180"><span class="elsevierStyleSup">6–11</span></a> The degree of bronchial obstruction, the presence of emphysema in the CT and chronic bronchitis are independent risk factors for the onset of lung cancer.<a class="elsevierStyleCrossRefs" href="#bib0180"><span class="elsevierStyleSup">6–16</span></a></p><p id="par0075" class="elsevierStylePara elsevierViewall">Torres et al.<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">20</span></a> validated a scoring system for lung cancer screening to identify high-risk patients with COPD in 2 screening cohorts in Spain (P-IELCAP) and the United States (PLuSS). The scale included age, BMI, PYI and the visual presence of emphysema in the LDCT. However, to facilitate the scale's clinical implementation and avoid the application of an LDCT, a new scoring system (known as COPD-LUCSS-DLCO) has been proposed, which replaces the radiological emphysema with DLCO. The high-risk patients showed a 2.4-fold increase in lung cancer mortality compared with the low-risk group (95% CI 2.0–2.7).<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">21</span></a></p><p id="par0080" class="elsevierStylePara elsevierViewall">A notable result of our study was that 62% of the patients were in the high-risk range. If we compare our series with similar studies in Spanish populations,<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">21</span></a> there were no significant differences in terms of mean age, FEV<span class="elsevierStyleInf">1</span>, BMI and PYI. However, more than half of our patients had an DLCO ≤60% despite the fact that the percentage of patients with COPD with a PYI >60 was lower (20% vs. 42%). Although a lower prevalence of COPD has been reported in the Canary Islands compared with the national mean, despite the high percentage of smokers,<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">23</span></a> we cannot rule out a greater susceptibility in our population with COPD to developing a greater degree of emphysema. COPD is a complex and multifactorial disease in which the association between genetic polymorphisms and the phenotype is probably nonlinear and in which the final phenotype depends on the genetics, the environment and the setting in which this genotype develops.<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">24</span></a></p><p id="par0085" class="elsevierStylePara elsevierViewall">Consistent with the severity obtained in the score, those high-risk patients with COPD demonstrated a higher incidence of lung cancer over the follow-up than the low-risk patients. Although this finding was not statistically significant, the magnitude of the signal achieved despite the low number of cancer diagnoses indicates the usefulness of the COPD-LUCSS-DLCO for detecting individuals in an outpatient population with a high probability of experiencing lung cancer, which allows us to manage lung cancer screening more efficiently. A study published by Torres et al.<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">25</span></a> conducted on 2 populations selected for follow-up (a control population who were monitored according to the GOLD guidelines and another who underwent lung cancer screening with annual LDCT) determined that the number of patients with COPD required for screening with the intent to save a life from lung cancer was only 34 patients, a significantly low number considering that the number needed for screening with the intent to save a life in the NLST study<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">4</span></a> was 271. In keeping with the above, the COPD-LUCCS-DLCO could help define what population would require a closer follow-up.</p><p id="par0090" class="elsevierStylePara elsevierViewall">However, once we have identified the presence of a “non-negligible” percentage of patients with COPD labeled as high risk, the issue is how follow-up should be conducted. Faced with the lack of favorable results in the lung cancer screening using chest radiography and given the ability of CT to detect smaller nodules than with conventional radiography,<a class="elsevierStyleCrossRefs" href="#bib0280"><span class="elsevierStyleSup">26,27</span></a> published data from the Early Lung Cancer Action Program group study<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">3</span></a> and subsequently from the NLST<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">4</span></a> showed that lung cancer screening using LDCT in individuals labeled as high risk helps diagnose most tumors in early phases of the disease, thereby achieving a reduction in lung cancer-specific mortality of approximately 16–20%. However, these results are currently the subject of debate in Europe, especially regarding overdiagnosis, radiation and associated risks, as well as its cost-effectiveness and organizational complexity.<a class="elsevierStyleCrossRefs" href="#bib0290"><span class="elsevierStyleSup">28,29</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">Despite the aforementioned discrepancies, LDCT currently appears to be the imaging technique of choice for lung cancer screening. However, doubts arise as to periodicity of its implementation and its duration in the follow-up. In our sample, 9% of the patients with COPD identified as high risk developed lung cancer in the first 31 months. However, we do not know the outcomes of high-risk patients who were not diagnosed during the follow-up period. Based on the NLST, the American Association for Thoracic Surgery<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">30</span></a> recommended performing LDCT annually in patients with a history of tobacco use and a PYI ≥30, starting at 55 years of age and ending at 79 years of age. It is likely that patients with COPD determined as high risk using the COPD-LUCSS-DLCO will benefit from this option, while for those at low risk the implementation of the LDCT could be more spaced out, enabling better management of the cases. Nevertheless, further studies are needed to verify this hypothesis.</p><p id="par0100" class="elsevierStylePara elsevierViewall">Our study had a several limitations. Firstly, the study population belonged to a single hospital, and the sample size was limited. Obviously, a larger sample could have shown differences undetected in the current analysis. Secondly, it is possible than an information bias occurred due to obtaining the variables from the patients’ medical history, although the current standardization of diagnostic criteria minimizes this possibility. Thirdly, not having performed an LDCT at the start of the study could have led to a lack of early detection of lung carcinoma in patient enrollment, with evidence of its clinical presence in the first 31 months of follow-up. Nevertheless, our study's objective was to use this score in an actual management situation in a pulmonology consultation, where unfortunately, not all patients undergo CT. The strength of our study lies in that it is the first to evaluate the COPD-LUCSS-DLCO in patients with COPD in a typical situation of standard clinical practice.</p><p id="par0105" class="elsevierStylePara elsevierViewall">In conclusion, the COPD-LUCSS-DLCO is an independent predictor of the risk of lung cancer. Its use in standard clinical practice could help detect patients at a greater risk of lung cancer, although this first needs to be confirmed in studies with larger sample sizes.</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Conflicts of interest</span><p id="par0110" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:11 [ 0 => array:3 [ "identificador" => "xres1087456" "titulo" => "Abstract" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Material and methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Conclusions" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1031453" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1087457" "titulo" => "Resumen" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Material y métodos" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Conclusiones" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1031452" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Background" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Material and methods" "secciones" => array:1 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Statistical analysis" ] ] ] 6 => array:2 [ "identificador" => "sec0020" "titulo" => "Results" ] 7 => array:2 [ "identificador" => "sec0025" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0030" "titulo" => "Conflicts of interest" ] 9 => array:2 [ "identificador" => "xack369195" "titulo" => "Acknowledgement" ] 10 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2018-01-25" "fechaAceptado" => "2018-04-18" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1031453" "palabras" => array:4 [ 0 => "Chronic obstructive pulmonary disease" 1 => "Lung" 2 => "Cancer" 3 => "Screening" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1031452" "palabras" => array:4 [ 0 => "Enfermedad pulmonar obstructiva crónica" 1 => "Pulmón" 2 => "Cáncer" 3 => "<span class="elsevierStyleItalic">Screening</span>" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:3 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Introduction</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The COPD-LUCSS-DLCO score had been validated as a predictive tool capable of identifying patients with chronic obstructive pulmonary disease (COPD) and a high mortality risk associated with lung cancer (LC); however, studies have not been conducted yet on its use in standard clinical practice. The aim of this study was to estimate the COPD-LUCSS-DLCO scores for patients with COPD treated in Pulmonology consultations and to determine the incidence of LC in each of the subgroups.</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Material and methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">A retrospective observational study was conducted with a cohort of 159 patients with COPD in Pulmonology outpatient follow-up consultations. We calculated the COPD-LUCSS-DLCO score (0–8) for each patient, with low risk considered at 0–3 points and high risk at ≥3.5 points. We calculated the incidence rate of LC in each of the subgroups.</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Sixty-two percent of the patients had a high-risk score. We estimated an overall LC rate of 30 per 1000 patients with COPD-year (95% CI: 16–53), 44 per 1000 patients with COPD-year (95% CI: 18–76) among those categorized as high risk and 17 per 1000 patients with COPD-year among those categorized as low risk (95% CI: 4–50).</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusions</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">The use of the COPD-LUCSS-DLCO score in standard clinical practice could help detect patients with a greater risk of developing LC, which could help to better manage cases in an LC screening program.</p></span>" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Material and methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Conclusions" ] ] ] "es" => array:3 [ "titulo" => "Resumen" "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducción</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">El <span class="elsevierStyleItalic">score</span> COPD-LUCSS-DLCO ha sido validado como una herramienta predictiva capaz de identificar pacientes con enfermedad pulmonar obstructiva crónica (EPOC) y alto riesgo de fallecer por cáncer de pulmón (CP). No obstante, hasta la fecha no se han realizado estudios acerca de su uso en la práctica clínica habitual. El objetivo del estudio fue estimar las puntuaciones del <span class="elsevierStyleItalic">score</span> COPD-LUCSS-DLCO en pacientes con EPOC atendidos en consultas de Neumología, así como determinar la incidencia de CP en cada uno de los subgrupos.</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Material y métodos</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Estudio observacional retrospectivo de una cohorte de 159 pacientes con EPOC en seguimiento en consultas ambulatorias de Neumología. Se calculó la puntuación del <span class="elsevierStyleItalic">score</span> COPD-LUCSS-DLCO (puntuación de 0-8) a cada uno de los sujetos, considerando bajo riesgo (BR) entre 0-3 puntos y alto riesgo (AR) ≥ 3,5 puntos. Se estimó la incidencia del CP en cada uno de los subgrupos.</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">El 62% presentaban un <span class="elsevierStyleItalic">score</span> de AR. Se estimó una tasa global de CP de 30 por 1.000 pacientes con EPOC-año (IC 95%:16-53), de 44 por 1.000 pacientes con EPOC-año (IC 95%: 18-76) entre los catalogados de AR y de 17 por 1.000 pacientes con EPOC-año (IC 95%: 4-50).</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusiones</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">El uso del <span class="elsevierStyleItalic">score</span> COPD-LUCSS-DLCO en la práctica clínica habitual podría permitir detectar pacientes con un mayor riesgo de desarrollar CP, lo cual ayudaría a una mejor gestión de casos en un programa de <span class="elsevierStyleItalic">screening</span> de CP.</p></span>" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Material y métodos" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Conclusiones" ] ] ] ] "NotaPie" => array:2 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as: Figueira Gonçalves JM, Pérez Mendez LI, Gurbani N, García-Talavera I, Pérez Pinilla JL. Aplicabilidad del <span class="elsevierStyleItalic">score</span> COPD-LUCSS-DLCO en pacientes con enfermedad pulmonar obstructiva crónica: análisis en condiciones de práctica clínica habitual. Rev Clin Esp. 2018;218:336–341.</p>" ] 1 => array:2 [ "etiqueta" => "☆☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0010">This study was awarded the prize for best presentation at the XXXII Regional Congress of the Canary Islands Association of Pulmonology and Thoracic Surgery (Neumocan).</p>" ] ] "multimedia" => array:3 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1169 "Ancho" => 1468 "Tamanyo" => 63021 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Incidence curves for lung cancer according to the COPD-LUCSS-DLCO score.</p>" ] ] 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" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">Abbreviations</span>: BMI, body mass index; DLCO, diffusing capacity of the lungs for carbon monoxide; PYI, packs-year index.</p><p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">Source: Based on De Torres et al.<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">21</span></a></p>" "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="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">COPD-LUCSS-DLCO \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Assigned score \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="table-entry " colspan="2" align="left" valign="top"><span class="elsevierStyleItalic">Components</span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>BMI <25 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.5 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>PYI >60 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Age, years >60 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.5 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>DLCO <60% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Total</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="2" align="left" valign="top"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="2" align="left" valign="top"><span class="elsevierStyleItalic">Categories</span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Low risk \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0–3 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>High risk \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.5–8 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1858247.png" ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Components of the COPD-LUCSS-DLCO score.</p>" ] ] 2 => array:8 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at2" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "<p id="spar0070" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">Abbreviations</span>: BMI, body mass index; COPD, chronic obstructive pulmonary disease; DLCO, diffusing capacity of the lungs for carbon monoxide; FEV<span class="elsevierStyleInf">1</span>, forced expiratory volume in one second; FVC, forced vital capacity; GOLD, Global Initiative for Chronic Obstructive Lung Disease; IQR, interquartile range; PYI, pack-year index; SD, standard deviation.</p>" "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="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Variable \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Global <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>159 \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Age, years (mean</span><span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">SD)</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">66<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>9 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Age >60 years, %</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">73 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Sex, % of males</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">82 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">BMI (mean</span><span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">SD)</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">27.6<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>5.4 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="2" align="left" valign="top"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="2" align="left" valign="top"><span class="elsevierStyleItalic">Degrees according to BMI, %</span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>BMI <25 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">31 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>BMI 25–29 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">32 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>BMI ≥30 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">37 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Active smokers, %</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">27 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">PYI (mean</span><span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">SD)</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">51<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>26 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">PYI >60, %</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">19 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Age-adjusted Charlson index (mean</span><span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">SD)</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">5<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>2 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">FEV</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">1</span></span><span class="elsevierStyleItalic">, % (mean</span><span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">SD)</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">50<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>19 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">FVC, % (mean</span><span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">SD)</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">82<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>20 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">DLCO, % (mean</span><span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">SD)</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">56<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>20 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">DLCO <60, %</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">58 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">GOLD 2009 I/II/III/IV</span> degrees, <span class="elsevierStyleItalic">%</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9/36/44/11 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Patients with high-risk score, %</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">62 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Median follow-up time, months (IQR)</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">31 (15–37) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Number of lung cancer diagnoses in all patients/in high-risk patients/in low-risk patients</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">12/9/3 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Overall incidence of lung cancer</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">30 per 1000 patients with COPD-year \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="2" align="left" valign="top"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="2" align="left" valign="top"><span class="elsevierStyleItalic">Lung cancer incidence</span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>COPD-LUCSS-DLCO low risk score \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">17 per 1000 patients with COPD-year \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>COPD-LUCSS-DLCO high risk score \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">44 per 1000 patients with COPD-year \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1858246.png" ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">Characteristics of the population with chronic obstructive pulmonary disease.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:30 [ 0 => array:3 [ "identificador" => "bib0155" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "One hundred years of lung cancer" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "S.G. 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