Poorer Survival in Stage IB Lung Cancer Patients After Pneumonectomy

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Novoa, José Luis Aranda, Marcelo F. Jiménez, Gonzalo Varela" "autores" => array:6 [ 0 => array:4 [ "nombre" => "María" "apellidos" => "Rodríguez" "email" => array:1 [ 0 => "mery.rodriguez.perez@gmail.com" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] 1 => array:2 [ "nombre" => "María Teresa" "apellidos" => "Gómez Hernández" ] 2 => array:2 [ "nombre" => "Nuria M." "apellidos" => "Novoa" ] 3 => array:2 [ "nombre" => "José Luis" "apellidos" => "Aranda" ] 4 => array:2 [ "nombre" => "Marcelo F." "apellidos" => "Jiménez" ] 5 => array:2 [ "nombre" => "Gonzalo" "apellidos" => "Varela" ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Servicio de Cirugía Torácica, Hospital Universitario de Salamanca, Salamanca, Spain" "identificador" => "aff0005" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "La neumonectomía ofrece menor supervivencia a los pacientes con carcinoma de pulmón en estadio patológico IB" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1179 "Ancho" => 1581 "Tamanyo" => 69044 ] ] "descripcion" => array:1 [ "en" => "Age- and FEV1%-adjusted survival of patients undergoing lobectomy or pneumonectomy (Log-rank P=.0357)." ] ] ] "textoCompleto" => "IntroductionAccording to the 7th edition of the TNM classification of lung cancer, stage IB includes tumors 3–5cm in diameter, with bronchial involvement 2cm or more distal to the carina, partial pulmonary atelectasis or invasion of the visceral pleura.<a class="elsevierStyleCrossRef" href="#bib0075">1</a> The surgical approach, therefore, in many tumors classified at this stage will vary, depending on the operating field and the skill of the attending surgeon. In an earlier publication,<a class="elsevierStyleCrossRef" href="#bib0080">2</a> we reported that 30-day mortality is a poor indicator of pneumonectomy risk, since death due to reasons other than cancer is much greater 6 months after the intervention than at 30 days. The hypothesis of this study is that, when all-cause mortality is taken into account, pneumonectomy in stage IB patients is associated with poorer survival.MethodStudy PopulationA retrospective review was performed of patients undergoing pulmonary lobectomy or pneumonectomy for pathological stage IB (pIB) lung cancer in our hospital between January 2000 and December 2011. Information was retrieved from a prospective, computerized double entry database. To ensure maximum homogeneity, patients who had received induction chemotherapy were excluded, even if their definitive staging was pT1-2aN0M0, since in most cases indication for induction chemotherapy was based on a clinical classification of N2. Stage pIB patients who received adjuvant chemotherapy were included in the study, irrespective of the indication for chemotherapy.Patient Screening CriteriaBefore surgery, all patients underwent the same tests: physical examination, complete blood count and serum biochemistry, electrocardiogram, chest X-ray, computed tomography (CT) of the chest and abdomen, and bronchoscopy. PET-CT was performed in all patients included since 2007. Invasive mediastinal staging (by mediastinoscopy or endobronchial ultrasound since 2009) was performed if mediastinal lymphadenopathies >1cm were seen on CT and if the mediastinal PET-CT was positive. All patients performed lung function tests; from 2009 onwards DLCO was routinely included.<a class="elsevierStyleCrossRef" href="#bib0085">3</a> Cardiac risk was evaluated according to criteria previously published by our group.<a class="elsevierStyleCrossRef" href="#bib0090">4</a> Patients with any neurological signs or symptoms on clinical examination underwent head CT, although this was not routinely ordered. Patients were classified for this study according to the TNM classification, 7th edition.<a class="elsevierStyleCrossRef" href="#bib0075">1</a> Age was not a contraindication for patients with an indication for pneumonectomy who met screening criteria after individual discussion of the case by a multidisciplinary committee.Perioperative Treatment and Follow-upThe surgical approach in all cases was muscle-sparing posterior thoracotomy, or either video-assisted or non-video-assisted axillary thoracotomy. The same group of anesthetists and thoracic surgeons were responsible for all anesthetic and surgical procedures, respectively. Systematic mediastinal lymphadenectomy was performed in all cases, based on current clinical guidelines.<a class="elsevierStyleCrossRef" href="#bib0095">5</a> Antibiotic prophylaxis consisted of a single dose of 1500mg cefuroxime that could be repeated after 6h if surgery was prolonged. Patients were extubated before they left the operating room, and after a few hours in the reanimation unit were transferred to the thoracic surgery ward. Bupivacaine and fentanyl were administered as postoperative analgesia via a thoracic epidural catheter for the first 3 days. After catheter withdrawal, analgesia consisted of oral non-steroidal anti-inflammatories and paracetamol.A single face-to-face visit was performed 1 month after surgery, and all other follow-up contact was made in the form of telephone calls to the patient or family members. If contact with the patient was lost, the date of death was retrieved from hospital records or treating physicians in the corresponding hospital.Variables AnalyzedIndependent variables included were type of resection (pneumonectomy or other), patient age, preoperative FEV1%, and Charlson index.<a class="elsevierStyleCrossRef" href="#bib0100">6</a> The latter was not recorded prospectively; instead, it was calculated retrospectively from variables recorded in the database that provided all the necessary variables. DLCO was only recorded routinely after 2009,<a class="elsevierStyleCrossRef" href="#bib0085">3</a> so it was not included in the analysis. The dependent variable was all-cause death, excluding postoperative death (death within the first 30 days or any time before hospital discharge after the procedure).Data AnalysisA Cox's regression model with bootstrap resampling with 100 replicates was used to examine associations between independent variables and survival. Age- and FEV1%-adjusted survival functions were constructed for patients undergoing pneumonectomy or lobectomy, and a log-rank test was performed to estimate the P-value of the differences between both functions. Data were analyzed using Stata/IC 13 software (StataCorp, Texas, USA).ResultsA total of 407 patients (373 lobectomies and 34 pneumonectomies) were included in the study. Four patients died during surgery (0.98%; 1 pneumonectomy and 3 lobectomies).At the time of starting this study, 212 patients had died; 195 (47.9%) remained alive. Causes of death were as follows: lung cancer, 112 cases; other cancer, 10; lung problems, 14; heart problems, 11; stroke, 6; other diseases, 12. In 47 cases (11.5%), cause of death was unknown.Continuous variables are described in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>. Patients undergoing pneumonectomy were slightly younger than the lobectomized patients.<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>Cox's regression analysis (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>) shows that age, FEV1%, and undergoing pneumonectomy are associated with poorer survival. Age-adjusted survival function and FEV1% are shown in <a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>. P-Value in the log-rank test was .0357.<elsevierMultimedia ident="tbl0010"></elsevierMultimedia><elsevierMultimedia ident="fig0005"></elsevierMultimedia>DiscussionPerioperative mortality risk (death within 30 days of surgery) in pneumonectomy is still as high as 7%, almost 3-fold the risk of lobectomy.<a class="elsevierStyleCrossRef" href="#bib0105">7</a> As we reported in a previous study,<a class="elsevierStyleCrossRef" href="#bib0080">2</a> mortality of patients undergoing pneumonectomy even increases over time, and can reach 25% within 6 months of surgery in patients undergoing right pneumonectomy. This increase in mortality in our series was not associated with underlying cancer or bronchopleural fistula, but rather with a greater incidence of cardiorespiratory complications in pneumonectomized patients.Despite these data, pneumonectomy is sometimes necessary in patients with stage IB non-small cell lung cancer (NSCLC), either because the surgeon lacks the technical skill to carry out parenchymal-sparing techniques, or because of the anatomical site of the tumor.In the first situation, the number of pneumonectomies carried out in a surgical unit decreases as surgeons acquire expertise in bronchoplastic and angioplastic techniques.<a class="elsevierStyleCrossRef" href="#bib0110">8</a> With regard to anatomical site, if proximal infiltration of the hilar structures or general extension across the lung fissure is observed, parenchymal-sparing techniques may be impossible. Even if lung fissure extension is not generalized and visceral pleural invasion is limited to a single point, several authors maintain that prognosis can be poorer in these patients.<a class="elsevierStyleCrossRefs" href="#bib0115">9–12</a> Some suggest that patients with T1 or T2 tumors with visceral pleural involvement crossing the interlobar fissure be classified as T3, or at least stage IIB (which comes down to the same), since survival is reduced by 10%–15% compared to patients with disease confined to a single lobe.<a class="elsevierStyleCrossRef" href="#bib0130">12</a> The high number of patients undergoing pneumonectomy in the series published by Okada et al.<a class="elsevierStyleCrossRef" href="#bib0120">10</a> and Demir et al.<a class="elsevierStyleCrossRef" href="#bib0125">11</a> make their results difficult to interpret, since the intervention in itself may act as a confounding factor when determining survival. Nevertheless, the study by Joshi et al.,<a class="elsevierStyleCrossRef" href="#bib0130">12</a> that includes only patients undergoing lobectomy plus wedge resection or bilobectomy, also reports poorer survival, typical of that between stages I and II, in patients with stage I NSCLC with interlobar extension. Taken together, the results of these studies suggest that both factors–fissure extension and pneumonectomy–play a fundamental role in the survival of these patients.Unfortunately, fissure or hilar extension as a reason for indicating pneumonectomy was not included among our study variables; neither were the surgeon's technical reasons for performing lobectomy or pneumonectomy, nor the side in which pneumonectomy was performed. The influence of adjuvant treatments on survival was not analyzed. With regard to surgical risk factors, DLCO was only recorded in our series after 2009,<a class="elsevierStyleCrossRef" href="#bib0085">3</a> so it could not be included as an independent variable in the regression model. Moreover, in 2002, an intensive postoperative respiratory physiotherapy protocol was introduced, leading to a significant reduction of respiratory complications.<a class="elsevierStyleCrossRef" href="#bib0135">13</a> We did not adjust for this factor, which may have affected the study results.Another limitation of this study is that the dependent variable is all-cause death; no differences were made between non-surgical causes, causes related with long-term complications derived from surgery and cancer-related causes. In our previous study,<a class="elsevierStyleCrossRef" href="#bib0080">2</a> we found that oncological causes and bronchopleural fistula did not increase long-term mortality, while cardiorespiratory complications did. However, as we did not have the exact causes of the death of all of our patients in this series, these factors cannot be analyzed. Neither do we have data on the disease-free interval of patients with death due to tumor progression, and the information at our disposal was mostly obtained from telephone interviews. While, in our experience,<a class="elsevierStyleCrossRef" href="#bib0140">14</a> this method is comparable to face-to-face patient interviews, it is impossible to guarantee the veracity of the information gathered.To conclude, these data confirm that in pathological stage IB NSCLC patients, not only older age and lower FEV1% are associated with poorer survival after lung resection surgery, but prognosis is also compromised by pneumonectomy. Although it continues to be an effective intervention in the treatment of NSCLC in selected cases, care must be taken when indicating this procedure, taking account the individual surgical risk of each patient and the other treatment options available.Conflict of InterestThe authors state that they have no conflict of interest." "textoCompletoSecciones" => array:1 [ "secciones" => array:10 [ 0 => array:3 [ "identificador" => "xres484711" "titulo" => "Abstract" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Objective" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Conclusions" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec506943" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres484710" "titulo" => "Resumen" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Objetivo" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Método" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Conclusiones" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec506942" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Method" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Study Population" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Patient Screening Criteria" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Perioperative Treatment and Follow-up" ] 3 => array:2 [ "identificador" => "sec0030" "titulo" => "Variables Analyzed" ] 4 => array:2 [ "identificador" => "sec0035" "titulo" => "Data Analysis" ] ] ] 6 => array:2 [ "identificador" => "sec0040" "titulo" => "Results" ] 7 => array:2 [ "identificador" => "sec0045" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0050" "titulo" => "Conflict of Interest" ] 9 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2014-07-03" "fechaAceptado" => "2014-09-19" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec506943" "palabras" => array:5 [ 0 => "Pneumonectomy" 1 => "Lobectomy" 2 => "Lung neoplasms" 3 => "Early stage" 4 => "Survival" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec506942" "palabras" => array:5 [ 0 => "Neumonectomía" 1 => "Lobectomía" 2 => "Cáncer de pulmón" 3 => "Estadio precoz" 4 => "Supervivencia" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:3 [ "titulo" => "Abstract" "resumen" => "ObjectivePneumonectomy may be needed in exceptional cases in patients with early stage NSCLC, especially in stage IB. The aim of this study was to evaluate whether overall survival in stage IB (T2aN0M0) NSCLC patients is worse after pneumonectomy. MethodsRetrospective study of a series of pathological IB (pIB) patients who underwent either lobectomy or pneumonectomy between 2000 and 2011. The dependent variable was all-cause death. Operative mortality was excluded. The relationship between the age, FEV1%, Charlson index and performance of pneumonectomy variables and the dependent variable were analyzed using a Cox regression. Overall survival for both groups of patients was then plotted in Kaplan–Meier graphs and compared using the log-rank test. ResultsA total of 407 cases were analyzed (373 lobectomies and 34 pneumonectomies). According to Cox regression, age, FEV1% and pneumonectomy were associated with poorer survival (P<.05). Age-adjusted survival and FEV1% showed diminished survival in patients who underwent pneumonectomy (log-rank, P=.0357). ConclusionsIn stage pIB NSCLC patients, pneumonectomy is associated with poorer survival compared to lobectomy." "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Objective" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Conclusions" ] ] ] "es" => array:3 [ "titulo" => "Resumen" "resumen" => "ObjetivoLa neumonectomía puede ser necesaria de forma excepcional en pacientes con cáncer de pulmón no microcítico (CPNM) en estadios precoces, algo más frecuentemente en el estadio IB. En este estudio se pretende evaluar si la neumonectomía se asocia con peor supervivencia global en pacientes con CPNM en estadios patológico IB (T2aN0M0). MétodoEstudio retrospectivo sobre una población de pacientes con carcinoma de pulmón pIB sometidos a lobectomía pulmonar o neumonectomía entre 2000 y 2011. La variable dependiente es la muerte del paciente por cualquier causa, excluida la mortalidad operatoria. Mediante regresión de Cox se analizó la relación de las variables: edad del paciente, FEV1%, índice de Charlson y neumonectomía sobre la variable dependiente. Se elaboró un gráfico de Kaplan Meier en el que se representó la supervivencia de los pacientes con lobectomía o neumonectomía y se compararon las 2 funciones mediante la prueba log-rank. ResultadosSe han analizado 407casos (373 lobectomías y 34 neumonectomías). En la regresión de Cox, la edad, el FEV1% y la neumonectomía se asociaron con una peor supervivencia (p<0,05). La función de supervivencia ajustada para edad y FEV1% demuestra menor supervivencia en los casos intervenidos mediante neumonectomía (log-rank p=0,0357). ConclusionesEn los pacientes con estadio patológico IB la neumonectomía se asocia a una menor supervivencia comparada con la lobectomía." "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Objetivo" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Método" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Conclusiones" ] ] ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "Please cite this article as: Rodríguez M, Gómez Hernández MT, Novoa NM, Aranda JL, Jiménez MF, Varela G. La neumonectomía ofrece menor supervivencia a los pacientes con carcinoma de pulmón en estadio patológico IB. Arch Bronconeumol. 2015;51:223–226." ] ] "multimedia" => array:3 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1179 "Ancho" => 1581 "Tamanyo" => 69044 ] ] "descripcion" => array:1 [ "en" => "Age- and FEV1%-adjusted survival of patients undergoing lobectomy or pneumonectomy (Log-rank P=.0357)." ] ] 1 => array:7 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:3 [ "leyenda" => "SD: standard deviation." "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="" valign="top" scope="col" style="border-bottom: 2px solid black"> \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">Lobectomy (n=373) \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">Pneumonectomy (n=34) \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">P \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 " align="left" valign="top">Age (mean, SD) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">66.4 (9.4) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">62.4 (9.9) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">.0213<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="left" valign="top">FEV1% (mean, SD) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">72.6 (17.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">74.4 (17.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">.3366<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="left" valign="top">Charlson index (median, range) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.8 (2–5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.5 (2–5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">.4856<a class="elsevierStyleCrossRef" href="#tblfn0010">b</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab767380.png" ] ] ] "notaPie" => array:2 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "a" "nota" => "Student t-test." ] 1 => array:3 [ "identificador" => "tblfn0010" "etiqueta" => "b" "nota" => "Wilcoxon test." ] ] ] "descripcion" => array:1 [ "en" => "Description of Patient Continuous Variables." ] ] 2 => array:7 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:2 [ "leyenda" => "Wald Chi-squared: 31.15.Prob>Chi-squared: 0.0000." "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">Hazard ratio \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">95% CI</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">P \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 " align="left" valign="top">Pneumonectomy \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.7298 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.0795 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.7716 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">.023 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="left" valign="top">Age \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.0299 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.0156 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.0445 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">.000 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="left" valign="top">FEV1% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.9884 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.9801 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.9969 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">.008 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab767379.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Cox's Regression Model." ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:14 [ 0 => array:3 [ "identificador" => "bib0075" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:1 [ "host" => array:1 [ 0 => array:1 [ "LibroEditado" => array:3 [ "titulo" => "TNM classification of malignant tumours" "edicion" => "7th ed." 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Original Article

Poorer Survival in Stage IB Lung Cancer Patients After Pneumonectomy

La neumonectomía ofrece menor supervivencia a los pacientes con carcinoma de pulmón en estadio patológico IB

María Rodríguez

Corresponding author

mery.rodriguez.perez@gmail.com

Corresponding author.

, María Teresa Gómez Hernández, Nuria M. Novoa, José Luis Aranda, Marcelo F. Jiménez, Gonzalo Varela

Servicio de Cirugía Torácica, Hospital Universitario de Salamanca, Salamanca, Spain

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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">According to the 7th edition of the TNM classification of lung cancer&#44; stage IB includes tumors 3&#8211;5<span class="elsevierStyleHsp" style=""></span>cm in diameter&#44; with bronchial involvement 2<span class="elsevierStyleHsp" style=""></span>cm or more distal to the carina&#44; partial pulmonary atelectasis or invasion of the visceral pleura&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">1</span></a> The surgical approach&#44; therefore&#44; in many tumors classified at this stage will vary&#44; depending on the operating field and the skill of the attending surgeon&#46; In an earlier publication&#44;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">2</span></a> we reported that 30-day mortality is a poor indicator of pneumonectomy risk&#44; since death due to reasons other than cancer is much greater 6 months after the intervention than at 30 days&#46; The hypothesis of this study is that&#44; when all-cause mortality is taken into account&#44; pneumonectomy in stage IB patients is associated with poorer survival&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Method</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Study Population</span><p id="par0010" class="elsevierStylePara elsevierViewall">A retrospective review was performed of patients undergoing pulmonary lobectomy or pneumonectomy for pathological stage IB &#40;pIB&#41; lung cancer in our hospital between January 2000 and December 2011&#46; Information was retrieved from a prospective&#44; computerized double entry database&#46; To ensure maximum homogeneity&#44; patients who had received induction chemotherapy were excluded&#44; even if their definitive staging was pT1-2aN0M0&#44; since in most cases indication for induction chemotherapy was based on a clinical classification of N2&#46; Stage pIB patients who received adjuvant chemotherapy were included in the study&#44; irrespective of the indication for chemotherapy&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Patient Screening Criteria</span><p id="par0015" class="elsevierStylePara elsevierViewall">Before surgery&#44; all patients underwent the same tests&#58; physical examination&#44; complete blood count and serum biochemistry&#44; electrocardiogram&#44; chest X-ray&#44; computed tomography &#40;CT&#41; of the chest and abdomen&#44; and bronchoscopy&#46; PET-CT was performed in all patients included since 2007&#46; Invasive mediastinal staging &#40;by mediastinoscopy or endobronchial ultrasound since 2009&#41; was performed if mediastinal lymphadenopathies &#62;1<span class="elsevierStyleHsp" style=""></span>cm were seen on CT and if the mediastinal PET-CT was positive&#46; All patients performed lung function tests&#59; from 2009 onwards DLCO was routinely included&#46;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">3</span></a> Cardiac risk was evaluated according to criteria previously published by our group&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">4</span></a> Patients with any neurological signs or symptoms on clinical examination underwent head CT&#44; although this was not routinely ordered&#46; Patients were classified for this study according to the TNM classification&#44; 7th edition&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">1</span></a> Age was not a contraindication for patients with an indication for pneumonectomy who met screening criteria after individual discussion of the case by a multidisciplinary committee&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Perioperative Treatment and Follow-up</span><p id="par0020" class="elsevierStylePara elsevierViewall">The surgical approach in all cases was muscle-sparing posterior thoracotomy&#44; or either video-assisted or non-video-assisted axillary thoracotomy&#46; The same group of anesthetists and thoracic surgeons were responsible for all anesthetic and surgical procedures&#44; respectively&#46; Systematic mediastinal lymphadenectomy was performed in all cases&#44; based on current clinical guidelines&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">5</span></a> Antibiotic prophylaxis consisted of a single dose of 1500<span class="elsevierStyleHsp" style=""></span>mg cefuroxime that could be repeated after 6<span class="elsevierStyleHsp" style=""></span>h if surgery was prolonged&#46; Patients were extubated before they left the operating room&#44; and after a few hours in the reanimation unit were transferred to the thoracic surgery ward&#46; Bupivacaine and fentanyl were administered as postoperative analgesia via a thoracic epidural catheter for the first 3 days&#46; After catheter withdrawal&#44; analgesia consisted of oral non-steroidal anti-inflammatories and paracetamol&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">A single face-to-face visit was performed 1 month after surgery&#44; and all other follow-up contact was made in the form of telephone calls to the patient or family members&#46; If contact with the patient was lost&#44; the date of death was retrieved from hospital records or treating physicians in the corresponding hospital&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Variables Analyzed</span><p id="par0030" class="elsevierStylePara elsevierViewall">Independent variables included were type of resection &#40;pneumonectomy or other&#41;&#44; patient age&#44; preoperative FEV1&#37;&#44; and Charlson index&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">6</span></a> The latter was not recorded prospectively&#59; instead&#44; it was calculated retrospectively from variables recorded in the database that provided all the necessary variables&#46; DLCO was only recorded routinely after 2009&#44;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">3</span></a> so it was not included in the analysis&#46; The dependent variable was all-cause death&#44; excluding postoperative death &#40;death within the first 30 days or any time before hospital discharge after the procedure&#41;&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Data Analysis</span><p id="par0035" class="elsevierStylePara elsevierViewall">A Cox&#39;s regression model with bootstrap resampling with 100 replicates was used to examine associations between independent variables and survival&#46; Age- and FEV1&#37;-adjusted survival functions were constructed for patients undergoing pneumonectomy or lobectomy&#44; and a log-rank test was performed to estimate the <span class="elsevierStyleItalic">P</span>-value of the differences between both functions&#46; Data were analyzed using Stata&#47;IC 13 software &#40;StataCorp&#44; Texas&#44; USA&#41;&#46;</p></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Results</span><p id="par0040" class="elsevierStylePara elsevierViewall">A total of 407 patients &#40;373 lobectomies and 34 pneumonectomies&#41; were included in the study&#46; Four patients died during surgery &#40;0&#46;98&#37;&#59; 1 pneumonectomy and 3 lobectomies&#41;&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">At the time of starting this study&#44; 212 patients had died&#59; 195 &#40;47&#46;9&#37;&#41; remained alive&#46; Causes of death were as follows&#58; lung cancer&#44; 112 cases&#59; other cancer&#44; 10&#59; lung problems&#44; 14&#59; heart problems&#44; 11&#59; stroke&#44; 6&#59; other diseases&#44; 12&#46; In 47 cases &#40;11&#46;5&#37;&#41;&#44; cause of death was unknown&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">Continuous variables are described in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#46; Patients undergoing pneumonectomy were slightly younger than the lobectomized patients&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">Cox&#39;s regression analysis &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41; shows that age&#44; FEV1&#37;&#44; and undergoing pneumonectomy are associated with poorer survival&#46; Age-adjusted survival function and FEV1&#37; are shown in <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#46; <span class="elsevierStyleItalic">P</span>-Value in the log-rank test was &#46;0357&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Discussion</span><p id="par0060" class="elsevierStylePara elsevierViewall">Perioperative mortality risk &#40;death within 30 days of surgery&#41; in pneumonectomy is still as high as 7&#37;&#44; almost 3-fold the risk of lobectomy&#46;<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">7</span></a> As we reported in a previous study&#44;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">2</span></a> mortality of patients undergoing pneumonectomy even increases over time&#44; and can reach 25&#37; within 6 months of surgery in patients undergoing right pneumonectomy&#46; This increase in mortality in our series was not associated with underlying cancer or bronchopleural fistula&#44; but rather with a greater incidence of cardiorespiratory complications in pneumonectomized patients&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Despite these data&#44; pneumonectomy is sometimes necessary in patients with stage IB non-small cell lung cancer &#40;NSCLC&#41;&#44; either because the surgeon lacks the technical skill to carry out parenchymal-sparing techniques&#44; or because of the anatomical site of the tumor&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">In the first situation&#44; the number of pneumonectomies carried out in a surgical unit decreases as surgeons acquire expertise in bronchoplastic and angioplastic techniques&#46;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">8</span></a> With regard to anatomical site&#44; if proximal infiltration of the hilar structures or general extension across the lung fissure is observed&#44; parenchymal-sparing techniques may be impossible&#46; Even if lung fissure extension is not generalized and visceral pleural invasion is limited to a single point&#44; several authors maintain that prognosis can be poorer in these patients&#46;<a class="elsevierStyleCrossRefs" href="#bib0115"><span class="elsevierStyleSup">9&#8211;12</span></a> Some suggest that patients with T1 or T2 tumors with visceral pleural involvement crossing the interlobar fissure be classified as T3&#44; or at least stage IIB &#40;which comes down to the same&#41;&#44; since survival is reduced by 10&#37;&#8211;15&#37; compared to patients with disease confined to a single lobe&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">12</span></a> The high number of patients undergoing pneumonectomy in the series published by Okada et al&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">10</span></a> and Demir et al&#46;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">11</span></a> make their results difficult to interpret&#44; since the intervention in itself may act as a confounding factor when determining survival&#46; Nevertheless&#44; the study by Joshi et al&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">12</span></a> that includes only patients undergoing lobectomy plus wedge resection or bilobectomy&#44; also reports poorer survival&#44; typical of that between stages I and II&#44; in patients with stage I NSCLC with interlobar extension&#46; Taken together&#44; the results of these studies suggest that both factors&#8211;fissure extension and pneumonectomy&#8211;play a fundamental role in the survival of these patients&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Unfortunately&#44; fissure or hilar extension as a reason for indicating pneumonectomy was not included among our study variables&#59; neither were the surgeon&#39;s technical reasons for performing lobectomy or pneumonectomy&#44; nor the side in which pneumonectomy was performed&#46; The influence of adjuvant treatments on survival was not analyzed&#46; With regard to surgical risk factors&#44; DLCO was only recorded in our series after 2009&#44;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">3</span></a> so it could not be included as an independent variable in the regression model&#46; Moreover&#44; in 2002&#44; an intensive postoperative respiratory physiotherapy protocol was introduced&#44; leading to a significant reduction of respiratory complications&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">13</span></a> We did not adjust for this factor&#44; which may have affected the study results&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Another limitation of this study is that the dependent variable is all-cause death&#59; no differences were made between non-surgical causes&#44; causes related with long-term complications derived from surgery and cancer-related causes&#46; In our previous study&#44;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">2</span></a> we found that oncological causes and bronchopleural fistula did not increase long-term mortality&#44; while cardiorespiratory complications did&#46; However&#44; as we did not have the exact causes of the death of all of our patients in this series&#44; these factors cannot be analyzed&#46; Neither do we have data on the disease-free interval of patients with death due to tumor progression&#44; and the information at our disposal was mostly obtained from telephone interviews&#46; While&#44; in our experience&#44;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">14</span></a> this method is comparable to face-to-face patient interviews&#44; it is impossible to guarantee the veracity of the information gathered&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">To conclude&#44; these data confirm that in pathological stage IB NSCLC patients&#44; not only older age and lower FEV1&#37; are associated with poorer survival after lung resection surgery&#44; but prognosis is also compromised by pneumonectomy&#46; Although it continues to be an effective intervention in the treatment of NSCLC in selected cases&#44; care must be taken when indicating this procedure&#44; taking account the individual surgical risk of each patient and the other treatment options available&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Conflict of Interest</span><p id="par0090" class="elsevierStylePara elsevierViewall">The authors state that they have no conflict of interest&#46;</p></span></span>"
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    "fechaRecibido" => "2014-07-03"
    "fechaAceptado" => "2014-09-19"
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            0 => "Pneumonectomy"
            1 => "Lobectomy"
            2 => "Lung neoplasms"
            3 => "Early stage"
            4 => "Survival"
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            0 => "Neumonectom&#237;a"
            1 => "Lobectom&#237;a"
            2 => "C&#225;ncer de pulm&#243;n"
            3 => "Estadio precoz"
            4 => "Supervivencia"
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    "resumen" => array:2 [
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Objective</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Pneumonectomy may be needed in exceptional cases in patients with early stage NSCLC&#44; especially in stage IB&#46; The aim of this study was to evaluate whether overall survival in stage IB &#40;T2aN0M0&#41; NSCLC patients is worse after pneumonectomy&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Retrospective study of a series of pathological IB &#40;pIB&#41; patients who underwent either lobectomy or pneumonectomy between 2000 and 2011&#46; The dependent variable was all-cause death&#46; Operative mortality was excluded&#46; The relationship between the age&#44; FEV1&#37;&#44; Charlson index and performance of pneumonectomy variables and the dependent variable were analyzed using a Cox regression&#46; Overall survival for both groups of patients was then plotted in Kaplan&#8211;Meier graphs and compared using the log-rank test&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">A total of 407 cases were analyzed &#40;373 lobectomies and 34 pneumonectomies&#41;&#46; According to Cox regression&#44; age&#44; FEV1&#37; and pneumonectomy were associated with poorer survival &#40;<span class="elsevierStyleItalic">P</span>&#60;&#46;05&#41;&#46; Age-adjusted survival and FEV1&#37; showed diminished survival in patients who underwent pneumonectomy &#40;log-rank&#44; <span class="elsevierStyleItalic">P</span>&#61;&#46;0357&#41;&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusions</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">In stage pIB NSCLC patients&#44; pneumonectomy is associated with poorer survival compared to lobectomy&#46;</p></span>"
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            "titulo" => "Objective"
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            "titulo" => "Methods"
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        "titulo" => "Resumen"
        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Objetivo</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">La neumonectom&#237;a puede ser necesaria de forma excepcional en pacientes con c&#225;ncer de pulm&#243;n no microc&#237;tico &#40;CPNM&#41; en estadios precoces&#44; algo m&#225;s frecuentemente en el estadio IB&#46; En este estudio se pretende evaluar si la neumonectom&#237;a se asocia con peor supervivencia global en pacientes con CPNM en estadios patol&#243;gico IB &#40;T2aN0M0&#41;&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">M&#233;todo</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Estudio retrospectivo sobre una poblaci&#243;n de pacientes con carcinoma de pulm&#243;n pIB sometidos a lobectom&#237;a pulmonar o neumonectom&#237;a entre 2000 y 2011&#46; La variable dependiente es la muerte del paciente por cualquier causa&#44; excluida la mortalidad operatoria&#46; Mediante regresi&#243;n de Cox se analiz&#243; la relaci&#243;n de las variables&#58; edad del paciente&#44; FEV1&#37;&#44; &#237;ndice de Charlson y neumonectom&#237;a sobre la variable dependiente&#46; Se elabor&#243; un gr&#225;fico de Kaplan Meier en el que se represent&#243; la supervivencia de los pacientes con lobectom&#237;a o neumonectom&#237;a y se compararon las 2 funciones mediante la prueba <span class="elsevierStyleItalic">log-rank</span>&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Se han analizado 407casos &#40;373 lobectom&#237;as y 34 neumonectom&#237;as&#41;&#46; En la regresi&#243;n de Cox&#44; la edad&#44; el FEV1&#37; y la neumonectom&#237;a se asociaron con una peor supervivencia &#40;p<span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#44;05&#41;&#46; La funci&#243;n de supervivencia ajustada para edad y FEV1&#37; demuestra menor supervivencia en los casos intervenidos mediante neumonectom&#237;a &#40;<span class="elsevierStyleItalic">log-rank</span> p<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;0357&#41;&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusiones</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">En los pacientes con estadio patol&#243;gico IB la neumonectom&#237;a se asocia a una menor supervivencia comparada con la lobectom&#237;a&#46;</p></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0015">Please cite this article as&#58; Rodr&#237;guez M&#44; G&#243;mez Hern&#225;ndez MT&#44; Novoa NM&#44; Aranda JL&#44; Jim&#233;nez MF&#44; Varela G&#46; La neumonectom&#237;a ofrece menor supervivencia a los pacientes con carcinoma de pulm&#243;n en estadio patol&#243;gico IB&#46; Arch Bronconeumol&#46; 2015&#59;51&#58;223&#8211;226&#46;</p>"
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          "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Age- and FEV1&#37;-adjusted survival of patients undergoing lobectomy or pneumonectomy &#40;<span class="elsevierStyleItalic">Log-rank P</span>&#61;&#46;0357&#41;&#46;</p>"
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          "leyenda" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">SD&#58; standard deviation&#46;</p>"
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                  <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="" valign="top" scope="col" style="border-bottom: 2px solid black">&nbsp;\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">Lobectomy &#40;n&#61;373&#41;&nbsp;\t\t\t\t\t\t\n
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Article information

ISSN: 15792129
Original language: English

DOI:10.1016/j.arbr.2015.03.006

The statistics are updated each day

Year/Month	Html	Pdf	Total

2024 November	2	1	3
2024 October	51	19	70
2024 September	42	17	59
2024 August	74	34	108
2024 July	55	20	75
2024 June	49	24	73
2024 May	65	35	100
2024 April	37	23	60
2024 March	44	16	60
2024 February	31	21	52
2023 March	10	7	17
2023 February	34	16	50
2023 January	28	30	58
2022 December	66	35	101
2022 November	58	35	93
2022 October	47	28	75
2022 September	30	28	58
2022 August	34	36	70
2022 July	38	33	71
2022 June	41	30	71
2022 May	38	25	63
2022 April	36	28	64
2022 March	41	34	75
2022 February	64	36	100
2022 January	37	20	57
2021 December	41	41	82
2021 November	51	42	93
2021 October	75	38	113
2021 September	60	38	98
2021 August	54	38	92
2021 July	40	31	71
2021 June	57	34	91
2021 May	51	21	72
2021 April	110	31	141
2021 March	73	28	101
2021 February	44	20	64
2021 January	35	17	52
2020 December	46	24	70
2020 November	49	24	73
2020 October	34	10	44
2020 September	42	12	54
2020 August	63	12	75
2020 July	104	19	123
2020 June	36	9	45
2020 May	46	23	69
2020 April	37	14	51
2020 March	48	15	63
2020 February	42	21	63
2020 January	43	18	61
2019 December	44	22	66
2019 November	40	20	60
2019 October	43	17	60
2019 September	39	13	52
2019 August	33	20	53
2019 July	40	19	59
2019 June	26	20	46
2019 May	26	22	48
2019 April	42	35	77
2019 March	30	20	50
2019 February	42	26	68
2019 January	46	19	65
2018 December	35	20	55
2018 November	113	24	137
2018 October	149	29	178
2018 September	72	11	83
2018 May	61	0	61
2018 April	53	4	57
2018 March	142	9	151
2018 February	51	13	64
2018 January	187	7	194
2017 December	161	9	170
2017 November	22	9	31
2017 October	25	17	42
2017 September	18	9	27
2017 August	15	12	27
2017 July	19	11	30
2017 June	55	11	66
2017 May	28	6	34
2017 April	22	7	29
2017 March	17	5	22
2017 February	19	4	23
2017 January	11	5	16
2016 December	26	6	32
2016 November	29	7	36
2016 October	34	8	42
2016 September	38	17	55
2016 August	34	4	38
2016 July	20	7	27
2016 April	2	0	2
2016 March	4	0	4
2015 December	3	0	3
2015 October	39	2	41
2015 September	37	5	42
2015 August	51	20	71
2015 July	2	1	3
2015 June	0	1	1
2015 April	3	1	4

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