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Correlation between pneumoperitoneum and surgical findings and morbidity and mortality in newborns with necrotising enterocolitis
Correlación entre el neumoperitoneo y los hallazgos quirúrgicos y morbimortalidad en recién nacidos con enterocolitis necrosante
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(a) Includes items 5–10, and combined items 1–2 and 3–4. (b) Includes items 12–14, 17, 21, 22. (c) Includes items 20, 25, 27–30, and combined items 24a–24b, 26a–26d and 26b–26c. Total<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>(a)<span class="elsevierStyleHsp" style=""></span>+<span class="elsevierStyleHsp" style=""></span>(b)<span class="elsevierStyleHsp" style=""></span>+<span class="elsevierStyleHsp" style=""></span>(c). The data for the items regarding “Delivery”, “6<span class="elsevierStyleHsp" style=""></span>h life” and “Delivery-6<span class="elsevierStyleHsp" style=""></span>h life” include the answers of all 89 hospitals. 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"apellidos" => "Villamil" "email" => array:1 [ 0 => "vanesa_villamil@yahoo.com.ar" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "María" "apellidos" => "Fernández-Ibieta" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 2 => array:3 [ "nombre" => "María Amparo" "apellidos" => "Gilabert Ubeda" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "María Josefa" "apellidos" => "Aranda García" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 4 => array:3 [ "nombre" => "Ramón" "apellidos" => "Ruiz Pruneda" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 5 => array:3 [ "nombre" => "Juana María" "apellidos" => "Sánchez Morote" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 6 => array:3 [ "nombre" => "José Ignacio" "apellidos" => "Ruiz Jiménez" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Servicio de Cirugía Pediátrica, Hospital Clínico Universitario Virgen de la Arrixaca, Murcia, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Servicio de Radiología, Hospital Clínico Universitario Virgen de la Arrixaca, Murcia, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Correlación entre el neumoperitoneo y los hallazgos quirúrgicos y morbimortalidad en recién nacidos con enterocolitis necrosante" ] ] "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" => 1099 "Ancho" => 1407 "Tamanyo" => 84381 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0075" class="elsevierStyleSimplePara elsevierViewall">Indications for surgery in newborns with necrotising enterocolitis. The absolute frequency is presented in parentheses. NEC, necrotising enterocolitis.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Necrotising enterocolitis (NEC), first described by Siebold in 1825,<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">1</span></a> is the most common gastrointestinal emergency occurring in neonatal intensive care units (NICUs),<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">2</span></a> with an estimated incidence of 0.3–3 cases per 1,000 live births.<a class="elsevierStyleCrossRefs" href="#bib0165"><span class="elsevierStyleSup">3,4</span></a> Its aetiology is not well understood, although it is hypothesised that it is related to decreased perfusion and ischaemia of the intestinal wall (particularly in immature intestines), leading to disruption of the intestinal barrier and enabling bacterial passage and activation of inflammatory mediators.<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">5</span></a> The main risk factors for the development of this disease are preterm birth, perinatal asphyxia, early enteral feeding in preterm newborns, congenital heart defects and umbilical catheterization, among others.<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">5</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Necrotising enterocolitis should not be confused with focal intestinal perforation, which is less frequent and affects up to 2% of extremely low birth weight infants.<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">3</span></a> Other differential features of focal intestinal perforation are: lack of systemic involvement, absence of intestinal pneumatosis, earlier onset, lower birth weight and extreme prematurity.<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">3</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Necrotising enterocolitis is classified according to the staging criteria proposed by Bell et al. as stage I (suspected), <span class="elsevierStyleSmallCaps">ii</span> (proven) or <span class="elsevierStyleSmallCaps">iii</span> (advanced),<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">6</span></a> a system that was later modified by Walsh and Kliegman in 1986.<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">7</span></a> In this modified scheme, stages are further subdivided into A or B depending on the radiographic findings: stage I<span class="elsevierStyleSmallCaps">A</span> or B (normal or intestinal dilation), stage IIA (ileus, pneumatosis intestinalis) or IIB (portal venous gas), stage IIIA (ascites) or IIIB (pneumoperitoneum).<a class="elsevierStyleCrossRefs" href="#bib0175"><span class="elsevierStyleSup">5,6</span></a> Another classification scheme was published in the <span class="elsevierStyleItalic">Vermont Oxford Network Manual of Operations</span> that described the clinical and radiographic findings required to establish the diagnosis of NEC.<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">8</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">There is widespread agreement that surgical intervention is necessary in patients with NEC that have developed intestinal gangrene, whose presence is evident if it leads to perforation and pneumoperitoneum, which is not always the case.<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">9</span></a> Free air in the abdominal cavity is the only radiographic feature universally accepted as an indication for surgical intervention in NEC.<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">10</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">The aim of this study was to analyse the cases of NEC treated with surgery to establish the reasons that led to performance of surgery, to determine whether pneumoperitoneum had been present in all patients with bowel perforation, and to assess patient outcomes based on whether pneumoperitoneum had or had not been present before surgery.</p><p id="par0030" class="elsevierStylePara elsevierViewall">To this end, we compared the radiographic findings (whether pneumoperitoneum was present or absent) with the surgical findings and the outcomes in a group of patients with NEC that underwent surgical intervention.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Sample and methods</span><p id="par0035" class="elsevierStylePara elsevierViewall">We conducted a retrospective study in a cohort of newborns with NEC that underwent surgery between January 2006 and December 2015. We divided these patients into 2 groups for comparison based on the preoperative presence or absence of pneumoperitoneum (P+/P–). We compared both groups based on the surgical findings, which included the length of resected bowel and the presence or absence of NEC <span class="elsevierStyleItalic">totalis</span> (involvement of 3 or more bowel segments). We also compared other variables related to morbidity and mortality: duration of symptoms from onset to the day of surgery, days of intubation, days of total parenteral nutrition, days from surgery at initiation of enteral feeding, length of stay in days, and mortality.</p><p id="par0040" class="elsevierStylePara elsevierViewall">In addition, we assessed interrater reliability, using the kappa statistic to compare the interpretation of the preoperatory findings made a posteriori by an expert paediatric radiologist masked to the symptoms to the preoperatory assessment made jointly by the neonatologist and the on-call paediatric surgeon. A <span class="elsevierStyleItalic">kappa</span> value of 0 signifies a total absence of interrater agreement, while a value of 1 signifies perfect agreement.<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">4</span></a> We assessed the level of agreement applying the criteria proposed by Landis and Koch: <span class="elsevierStyleItalic">k</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.20 (very poor), 0.21<span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">k</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.40 (poor), 0.41<span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">k</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.60 (fair), 0.61<span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">k</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.80 (good), and 0.81<span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">k</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>1.00 (excellent).<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">11</span></a></p><p id="par0045" class="elsevierStylePara elsevierViewall">To compare qualitative variables, we used the chi square test or the Fisher exact test as appropriate. We compared quantitative variables by means of the nonparametric Mann–Whitney <span class="elsevierStyleItalic">U</span> test. We assessed survival using the Kaplan–Meier method.</p><p id="par0050" class="elsevierStylePara elsevierViewall">We set the alpha level to define statistical significance at 0.05. The statistical analysis was performed with the software SPSS version 23.0.</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Results</span><p id="par0055" class="elsevierStylePara elsevierViewall">In the 10 years under study, 53 patients with NEC underwent surgical intervention. They had been born at a median of 28<span class="elsevierStyleHsp" style=""></span>+<span class="elsevierStyleHsp" style=""></span>6 weeks’ gestation (range, 23–41 weeks) with a mean birth weight of 1229<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>581<span class="elsevierStyleHsp" style=""></span>g (range, 590–3087<span class="elsevierStyleHsp" style=""></span>g), with 94.3% being born with a low birth weight (50 newborns with weight <2500<span class="elsevierStyleHsp" style=""></span>g), 73.6% with a very low birth weight (39 newborns with weight <1500<span class="elsevierStyleHsp" style=""></span>g) and 50.9% with an extremely low birth weight (27 newborns with weight <1000<span class="elsevierStyleHsp" style=""></span>g). We estimated an incidence of surgical NEC of 7 newborns per 10,000 live births.</p><p id="par0060" class="elsevierStylePara elsevierViewall">In this cohort, 51% of patients were female (<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>27) and 94.3% had been born preterm (born before 37 weeks’ gestation, <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>50), with 77.4% born very or extremely preterm (born before 32 weeks’ gestation, <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>41).</p><p id="par0065" class="elsevierStylePara elsevierViewall">The mean age at the time of surgery was 19<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>14 days (range, 2–63 days), and the mean weight was 1474<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>669<span class="elsevierStyleHsp" style=""></span>g (range, 650–3750<span class="elsevierStyleHsp" style=""></span>g).</p><p id="par0070" class="elsevierStylePara elsevierViewall">The sensitivity of abdominal radiography for the diagnosis of pneumoperitoneum is 54.5%, while the specificity is 92.3%. In 36% of patients (<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>19), surgery was performed due to the presence of pneumoperitoneum, while in the remaining patients (<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>34) it was performed for other reasons (clinical deterioration, metabolic derangement or intestinal obstruction) (Fig 1).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0075" class="elsevierStylePara elsevierViewall">When we analysed the two groups defined by the presence or absence of pneumoperitoneum (P+/P–), we found a shorter duration of symptoms from onset to surgery in the P+ group, with a mean of 2<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>1.7 days (range, 1–3 days) compared to 7<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>8 days in the P– group (range, 3–10 days), and also a shorter length of stay, which was of 79<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>28 days in the P+ group (60–98) compared to 127<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>43 days in the P– group (103–150) (excluding deceased patients), differences that were statistically significant (<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.008 and <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.003, respectively) (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). The differences remained significant when we adjusted the analysis for weight: in the group with birth weights of more than 1000<span class="elsevierStyleHsp" style=""></span>g (+1000<span class="elsevierStyleHsp" style=""></span>g), the mean length of stay was 58<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>10 days in P+ newborns (range, 48–69) compared to 89<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>15 days in the P– group (range, 71–107) (<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.005) (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). We also found differences in the group with birth weight of less than 1000<span class="elsevierStyleHsp" style=""></span>g, although they were not statistically significant: mean of 107<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>20 days (range, 78–135) in the P+ group vs. 146<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>43 days (range, 116–175) in the P– group (<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.064).</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0080" class="elsevierStylePara elsevierViewall">When we analysed mortality, we did not find statistically significant differences between the two groups. The overall mortality was 41.5%, corresponding to 10 newborns in the P+ group (45%) and 12 of the P– group (55%). We also found no statistically significant differences in any of the other variables under study (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>).</p><p id="par0085" class="elsevierStylePara elsevierViewall">The <span class="elsevierStyleItalic">kappa</span> statistic was 0.7, which corresponds to a good correlation based on the criteria proposed by Landis and Koch.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Discussion</span><p id="par0090" class="elsevierStylePara elsevierViewall">Necrotising enterocolitis is one of the main causes of morbidity and mortality in newborns.<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">12</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">Most cases of NEC occur in preterm newborns. The mean gestational age at birth in our cohort was 28<span class="elsevierStyleHsp" style=""></span>+<span class="elsevierStyleHsp" style=""></span>6 weeks (range, 23–41), which was consistent with previous studies.<a class="elsevierStyleCrossRefs" href="#bib0215"><span class="elsevierStyleSup">13,14</span></a></p><p id="par0100" class="elsevierStylePara elsevierViewall">The mean birth weight in our cohort was 1229<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>581<span class="elsevierStyleHsp" style=""></span>g, with a range of 590–3087<span class="elsevierStyleHsp" style=""></span>g, which was similar to the findings reported in the literature,<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">15</span></a> although there seems to be a declining trend in the mean birth weight of patients with surgical NEC, as suggested by other authors.<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">9</span></a></p><p id="par0105" class="elsevierStylePara elsevierViewall">The mean age at the time of surgery in our study was 19 days (range, 2–63), which was similar to the one reported in a study conducted in 2002<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">16</span></a> and another study we found in the reviewed literature.<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">13</span></a></p><p id="par0110" class="elsevierStylePara elsevierViewall">When medical treatment fails (including antibiotherapy, discontinuation of enteral feeding and supportive care),<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">17</span></a> the decision to perform surgery is based on radiographic findings and clinical manifestations suggestive of metabolic derangement.<a class="elsevierStyleCrossRefs" href="#bib0160"><span class="elsevierStyleSup">2,8</span></a></p><p id="par0115" class="elsevierStylePara elsevierViewall">In patients with suspected NEC, a radiological evaluation can confirm the staging as proven or advanced.<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">18</span></a> Extraluminal air (free air) is a sign of advanced NEC<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">8</span></a> and the sole radiologic finding that is universally accepted as an indication for surgical intervention,<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">19</span></a> as it is direct evidence of perforation. Some authors consider metabolic derangement a sufficient indication for surgery and have established a series of laboratory criteria and thresholds to determine the appropriateness of intervention, even in the absence of pneumoperitoneum.<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">3</span></a> We ought to highlight the importance of obtaining the two radiographic images (antero-posterior view and horizontal beam view with the patient in the supine position) within 48<span class="elsevierStyleHsp" style=""></span>h from onset, as most perforations develop in that time interval,<a class="elsevierStyleCrossRefs" href="#bib0200"><span class="elsevierStyleSup">10,12</span></a> something that we corroborated in our results, as we found that a mean of 2 days elapsed from the onset of symptoms to evidence of pneumoperitoneum, with a range of 1–3 days.</p><p id="par0120" class="elsevierStylePara elsevierViewall">Pneumoperitoneum is not always present and is found in 50–75% of patients with intestinal perforation due to NEC,<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">20</span></a> with other authors reporting its presence in as few as 12–50% of these patients.<a class="elsevierStyleCrossRefs" href="#bib0240"><span class="elsevierStyleSup">18,21</span></a> Thus, the sensitivity of this radiographic finding is much lower than expected. In our study, its sensitivity was 54.5%. There are several possible explanations for the absence of pneumoperitoneum in cases of intestinal perforation: (1) perforation of the jejunum or ileus, which may not contain air; (2) early closure of perforation; (3) retroperitoneal perforation; (4) small amount of gas due to effective suction through a nasogastric tube; (5) lack of an optimal radiographic view showing the pneumoperitoneum, and (6) perforation occurring after obtaining the radiograph and before surgery.<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">1</span></a></p><p id="par0125" class="elsevierStylePara elsevierViewall">This radiographic feature is not always easy to identify, and there are several radiographic signs that help detect its presence: Rigler's sign (gas on both sides of the intestinal wall), the falciform ligament sign (gas outlining the falciform ligament), the football sign (gas outlining the peritoneal cavity), the inverted-V sign (gas outlining the medial umbilical folds) and right-upper-quadrant gas sign (localised gas in this quadrant, in the subhepatic space).<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">22</span></a></p><p id="par0130" class="elsevierStylePara elsevierViewall">Some critically ill infants require mechanical ventilation, which may cause pneumothorax or pneumomediastinum and therefore pneumoperitoneum. In these patients, it is important to perform a correct differential diagnosis of gastrointestinal perforation and medical pneumoperitoneum to avoid unnecessary surgical procedures.<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">23</span></a> We found one such patient in this study. As we mentioned before, pneumoperitoneum was the indication for surgery in 39% of cases, a proportion that was similar to those reported in other studies.<a class="elsevierStyleCrossRefs" href="#bib0270"><span class="elsevierStyleSup">24,25</span></a></p><p id="par0135" class="elsevierStylePara elsevierViewall">In the past, there was widespread agreement that the prognosis of patients with NEC worsened once intestinal perforation occurred,<a class="elsevierStyleCrossRefs" href="#bib0155"><span class="elsevierStyleSup">1,10,26</span></a> although the published evidence is not completely concordant on this aspect.<a class="elsevierStyleCrossRefs" href="#bib0270"><span class="elsevierStyleSup">24,27</span></a> As Grosfeld et al. already stated in 1991, early diagnosis, advances in neonatal intensive care and prompt surgical intervention when indicated have improved survival in patients with NEC.<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">28</span></a></p><p id="par0140" class="elsevierStylePara elsevierViewall">In our study, we found that even adjusting for weight, radiographic evidence of pneumoperitoneum was not in and of itself associated to poorer outcomes, but rather the opposite. This was probably due to the association of pneumoperitoneum with a shorter duration of symptoms before surgery compared to patients without pneumoperitoneum. In many cases, the decision to perform surgery in preterm infants with manifestations suggestive of NEC is delayed for days while the patient receives more aggressive medical treatment, precisely because there are no radiographic findings that clearly “invite” the surgeon to intervene.</p><p id="par0145" class="elsevierStylePara elsevierViewall">Considering the low sensitivity of abdominal radiography found in our study, relying on the detection of free abdominal air as the sole definitive indication for surgery should by now be considered obsolete or risky. Other authors also recommend against waiting for stage IIIB NEC to operate, given that it may not always be detected radiographically, as long as the patient develops metabolic derangement or infection despite adequate medical treatment.</p><p id="par0150" class="elsevierStylePara elsevierViewall">In our study, 10 patients in the pneumoperitoneum group (45%) and 12 in the group without pneumoperitoneum (55%) died. The overall mortality was 41.5%, a proportion that was similar to those reported in other case series, which range between 55% and 83%.<a class="elsevierStyleCrossRefs" href="#bib0175"><span class="elsevierStyleSup">5,13</span></a></p><p id="par0155" class="elsevierStylePara elsevierViewall">The kappa statistic found in this study revealed a very good interrater reliability (0.7). Nevertheless, to decrease both false-negative and false-positive interpretation, it is recommended that an experienced radiologist always review the radiographs of patients with suspected NEC.<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">29</span></a></p><p id="par0160" class="elsevierStylePara elsevierViewall">The authors of a study conducted in 2002 estimated the sensitivity and specificity of pneumoperitoneum at 52% and 92%, respectively,<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">30</span></a> which are practically the same as the estimates obtained in our study.</p><p id="par0165" class="elsevierStylePara elsevierViewall">The limitations of this study include its retrospective design and the small sample size, and a prospective study would be necessary to collect more reliable information regarding patient outcomes that would allow drawing firmer conclusions.</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Conclusion</span><p id="par0170" class="elsevierStylePara elsevierViewall">Given that there is no specific clinical, radiologic or laboratory finding to establish the need for surgery and that (as occurred in 39% of the patients in our study) perforation may be present in the absence of pneumoperitoneum, the decision to operate must be based on the collection of clinical and radiologic features of the patient.</p><p id="par0175" class="elsevierStylePara elsevierViewall">We have not found other articles comparing the outcomes of patients that underwent surgery for NEC based on the presence or absence of pneumoperitoneum, so we believe that our study contributes relevant information to our understanding of the outcomes of NEC.</p><p id="par0180" class="elsevierStylePara elsevierViewall">The presence of pneumoperitoneum in cases of NEC is not associated with a less favourable outcome.</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Conflicts of interest</span><p id="par0185" class="elsevierStylePara elsevierViewall">The authors have no conflicts of interest to declare.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:11 [ 0 => array:3 [ "identificador" => "xres1089587" "titulo" => "Abstract" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Objective" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Methods" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Results" ] 4 => array:2 [ "identificador" => "abst0025" "titulo" => "Conclusions" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1033003" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1089588" "titulo" => "Resumen" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0030" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0035" "titulo" => "Objetivo" ] 2 => array:2 [ "identificador" => "abst0040" "titulo" => "Método" ] 3 => array:2 [ "identificador" => "abst0045" "titulo" => "Resultados" ] 4 => array:2 [ "identificador" => "abst0050" "titulo" => "Conclusiones" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1033002" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Sample and methods" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Results" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0025" "titulo" => "Conclusion" ] 9 => array:2 [ "identificador" => "sec0030" "titulo" => "Conflicts of interest" ] 10 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2017-07-11" "fechaAceptado" => "2017-11-13" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1033003" "palabras" => array:4 [ 0 => "Necrotising enterocolitis" 1 => "Pneumoperitoneum" 2 => "Intestinal perforation" 3 => "Mortality" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1033002" "palabras" => array:4 [ 0 => "Enterocolitis necrosante" 1 => "Neumoperitoneo" 2 => "Perforación intestinal" 3 => "Mortalidad" ] ] ] ] "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">Surgical intervention in necrotising enterocolitis (NEC) is correct when there is intestinal gangrene. This is evident when gangrene produces perforation and pneumoperitoneum, with this being the only universally accepted radiological indication for the surgical intervention of NEC.</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Objective</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">To perform an analysis on patients with surgically managed NEC, including determining how the decision to intervene is reached, the outcomes, and if patients with perforation had a pneumoperitoneum.</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Methods</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Retrospective review of neonates with surgical NEC over a period of 10<span class="elsevierStyleHsp" style=""></span>years (2006–2015). An analysis was made of pre-surgical X-ray findings, which were compared with surgical ones, in addition to the morbidity and mortality, depending on the presence (N+) or absence (N−) of pneumoperitoneum. An evaluation was also made of the interobserver concordance with a paediatric radiologist blinded to the clinical reason using the <span class="elsevierStyleItalic">kappa</span> agreement index.</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Results</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">A total of 53 neonates were included in the study. Surgical treatment was indicated after observing pneumoperitoneum in 36%. In the remaining neonates, the surgical decision was made after noting a clinical and metabolic deterioration with classical X-ray findings. Intestinal perforation was observed in 39% of the N− neonates.</p><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">There were no statistical differences between either group on analysing the excised intestinal length, days of intubation, starting of enteral nutrition, and the mortality rate. Comparisons in terms of duration of symptoms and total hospital stay were statistically significant (7 vs. 2 days, <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.008; 127 vs. 79 days, <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.003, respectively), with both being more favourable in the N+ group. These differences remained when the groups were adjusted by birthweight.</p></span> <span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Conclusions</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Surgical indication has to be done on an ensemble of clinical and radiological evidence, as 39% of the neonates in the N− groups were perforated.</p><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">In our study, the presence of a pneumoperitoneum did not correlate with a worse prognosis.</p></span>" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Objective" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Methods" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Results" ] 4 => array:2 [ "identificador" => "abst0025" "titulo" => "Conclusions" ] ] ] "es" => array:3 [ "titulo" => "Resumen" "resumen" => "<span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Introducción</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">La intervención quirúrgica en las enterocolitis necrosantes (EN) es precisa cuando existe gangrena intestinal, hecho evidente cuando produce perforación y neumoperitoneo, siendo este la única indicación radiológica aceptada universalmente para la intervención quirúrgica.</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Objetivo</span><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Analizar a los pacientes intervenidos de EN, saber por qué se les intervino, cómo evolucionan y si los pacientes perforados presentan neumoperitoneo.</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Método</span><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Estudio retrospectivo de una cohorte de recién nacidos con EN intervenidos durante un periodo de 10 años (2006-2015). Se analizan los hallazgos radiológicos preoperatorios y se correlacionan con los quirúrgicos y con la morbimortalidad, dependiendo de la presencia de neumoperitoneo (N+) o no (N–). Se evaluó la concordancia interobservador con radiólogo pediátrico enmascarado a la clínica mediante el índice de acuerdo <span class="elsevierStyleItalic">kappa</span>.</p></span> <span id="abst0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Resultados</span><p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Se analizó a 53 pacientes. El 36% se intervino tras la visualización de neumoperitoneo; en el resto, la indicación fue deterioro clínico y metabólico, junto con hallazgos radiológicos asociados. En el 39% del grupo N– se objetivó perforación.</p><p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">No se encontraron diferencias significativas en ambos grupos con respecto a longitud intestinal resecada, días de intubación, día de inicio de nutrición enteral y mortalidad. La comparación entre duración de síntomas y estancia hospitalaria total en ambos grupos (N–/N+) fue significativa (7 vs. 2 días, p = 0,008; 127 vs. 79 días, p<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0,003 respectivamente), siendo más favorable en el grupo N+. Estas diferencias se mantuvieron al ajustar por peso.</p></span> <span id="abst0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Conclusiones</span><p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">La indicación quirúrgica ha de basarse en un conjunto de datos clínicos y radiológicos, ya que el 39% de los pacientes sin neumoperitoneo presentaron perforación.</p><p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">En nuestro estudio la presencia de neumoperitoneo no se correlaciona con peor pronóstico.</p></span>" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0030" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0035" "titulo" => "Objetivo" ] 2 => array:2 [ "identificador" => "abst0040" "titulo" => "Método" ] 3 => array:2 [ "identificador" => "abst0045" "titulo" => "Resultados" ] 4 => array:2 [ "identificador" => "abst0050" "titulo" => "Conclusiones" ] ] ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as: Villamil V, Fernández-Ibieta M, Gilabert Ubeda MA, Aranda García MJ, Ruiz Pruneda R, Sánchez Morote JM, et al. Correlación entre el neumoperitoneo y los hallazgos quirúrgicos y morbimortalidad en recién nacidos con enterocolitis necrosante. An Pediatr (Barc). 2018;89:205–210.</p>" ] ] "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1099 "Ancho" => 1407 "Tamanyo" => 84381 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0075" class="elsevierStyleSimplePara elsevierViewall">Indications for surgery in newborns with necrotising enterocolitis. The absolute frequency is presented in parentheses. NEC, necrotising enterocolitis.</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="spar0085" class="elsevierStyleSimplePara elsevierViewall">Data expressed as means and <span class="elsevierStyleItalic">p</span> values.</p><p id="spar0090" class="elsevierStyleSimplePara elsevierViewall">EF, enteral feeding.</p><p id="spar0095" class="elsevierStyleSimplePara elsevierViewall">Statistically significant results are presented in boldface.</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">Variables \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><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><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">p</span> \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">Duration of symptoms in days (mean</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">±</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="char" valign="top">2<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>1.7 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top"><span class="elsevierStyleBold">0.008</span> \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">Days of intubation (mean</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">±</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="char" valign="top">7<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>11 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.59 \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">Days post-surgery at initiation of EF (mean</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">±</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="char" valign="top">6<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">11<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>13 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.24 \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">Length of stay in days (mean</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">±</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="char" valign="top">79<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>28 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">127<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>43 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top"><span class="elsevierStyleBold">0.003</span> \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>Length of stay in ≥1000<span class="elsevierStyleHsp" style=""></span>g \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">58<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>10 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">89<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>15 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top"><span class="elsevierStyleBold">0.005</span> \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>Length of stay in ¿1000<span class="elsevierStyleHsp" style=""></span>g \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">107<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>20 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">146<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>43 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.064 \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">Resected length of bowel in cm (mean</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">±</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="char" valign="top">13<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>9 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">20<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>11 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.21 \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">Mortality (n – %)</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">10 (45%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">12 (55%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.85 \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>Mortality in ≥1000<span class="elsevierStyleHsp" style=""></span>g \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7 (54%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">6 (46%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.6 \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>Mortality in ¿1000<span class="elsevierStyleHsp" style=""></span>g \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4 (40%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">6 (60%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.53 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1862782.png" ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0080" class="elsevierStyleSimplePara elsevierViewall">Statistical analysis of quantitative data in the two groups compared in the study.</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" => "Indications for operation in acute necrotizing enterocolitis of the neonate" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "A.M. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 7 | 11 | 18 |
| 2024 October | 62 | 23 | 85 |
| 2024 September | 63 | 28 | 91 |
| 2024 August | 96 | 43 | 139 |
| 2024 July | 91 | 31 | 122 |
| 2024 June | 79 | 30 | 109 |
| 2024 May | 64 | 31 | 95 |
| 2024 April | 47 | 31 | 78 |
| 2024 March | 55 | 21 | 76 |
| 2024 February | 51 | 21 | 72 |
| 2024 January | 82 | 23 | 105 |
| 2023 December | 125 | 24 | 149 |
| 2023 November | 82 | 12 | 94 |
| 2023 October | 62 | 26 | 88 |
| 2023 September | 52 | 20 | 72 |
| 2023 August | 49 | 17 | 66 |
| 2023 July | 55 | 24 | 79 |
| 2023 June | 52 | 23 | 75 |
| 2023 May | 79 | 20 | 99 |
| 2023 April | 62 | 18 | 80 |
| 2023 March | 89 | 24 | 113 |
| 2023 February | 75 | 19 | 94 |
| 2023 January | 58 | 21 | 79 |
| 2022 December | 82 | 25 | 107 |
| 2022 November | 77 | 22 | 99 |
| 2022 October | 76 | 42 | 118 |
| 2022 September | 54 | 22 | 76 |
| 2022 August | 67 | 48 | 115 |
| 2022 July | 55 | 34 | 89 |
| 2022 June | 44 | 40 | 84 |
| 2022 May | 66 | 45 | 111 |
| 2022 April | 49 | 41 | 90 |
| 2022 March | 97 | 50 | 147 |
| 2022 February | 57 | 24 | 81 |
| 2022 January | 104 | 36 | 140 |
| 2021 December | 58 | 45 | 103 |
| 2021 November | 58 | 34 | 92 |
| 2021 October | 115 | 81 | 196 |
| 2021 September | 63 | 44 | 107 |
| 2021 August | 44 | 49 | 93 |
| 2021 July | 61 | 35 | 96 |
| 2021 June | 52 | 31 | 83 |
| 2021 May | 60 | 37 | 97 |
| 2021 April | 220 | 89 | 309 |
| 2021 March | 86 | 45 | 131 |
| 2021 February | 60 | 20 | 80 |
| 2021 January | 67 | 20 | 87 |
| 2020 December | 65 | 19 | 84 |
| 2020 November | 68 | 22 | 90 |
| 2020 October | 128 | 15 | 143 |
| 2020 September | 159 | 31 | 190 |
| 2020 August | 107 | 13 | 120 |
| 2020 July | 90 | 25 | 115 |
| 2020 June | 97 | 11 | 108 |
| 2020 May | 86 | 21 | 107 |
| 2020 April | 70 | 35 | 105 |
| 2020 March | 75 | 15 | 90 |
| 2020 February | 74 | 17 | 91 |
| 2020 January | 63 | 17 | 80 |
| 2019 December | 108 | 15 | 123 |
| 2019 November | 58 | 14 | 72 |
| 2019 October | 49 | 13 | 62 |
| 2019 September | 50 | 15 | 65 |
| 2019 August | 114 | 25 | 139 |
| 2019 July | 50 | 32 | 82 |
| 2019 June | 32 | 11 | 43 |
| 2019 May | 97 | 24 | 121 |
| 2019 April | 85 | 24 | 109 |
| 2019 March | 55 | 13 | 68 |
| 2019 February | 55 | 16 | 71 |
| 2019 January | 48 | 17 | 65 |
| 2018 December | 43 | 30 | 73 |
| 2018 November | 64 | 27 | 91 |
| 2018 October | 164 | 33 | 197 |
| 2018 September | 45 | 17 | 62 |
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