ORIGINAL PAPERS

 

Endoscopic ultrasound versus multidetector computed tomography in preoperative gastric cancer staging

Ultrasonografía endoscópica versus tomografía computarizada en la estadificación preoperatoria del cáncer gástrico

 

 

Marta Cimavilla-Román¹, Carlos de-la-Serna-Higuera¹, Andrea Loza-Vargas¹, César Benito-Fernández², Jesús Barrio-Andrés¹, Beatriz Madrigal-Rubiales³, Gabriel Fernández-Pérez⁴ and Manuel Pérez-Miranda¹

Departments of ¹Gastroenterology, ²General Surgery, ³Pathology and ⁴Radiology. Hospital. Universitario Río Hortega. Valladolid, Spain

Correspondence

 

 

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ABSTRACT

Introduction: Endoscopic ultrasonography (EUS) is the gold standard technique in loco-regional staging of gastric adenocarcinoma (GAC). Nevertheless, the introduction of multidetector-row computed tomography (MDCT) allows accurate studies to be performed.
Objective: To compare the diagnostic yield of EUS and MDCT in loco-regional preoperative staging of gastric adenocarcinoma.
Material and methods: This was a retrospective and comparative study of all surgical patients with GAC and preoperative staging by EUS and 64-row MDCT. The results for each case were compared with the histological data.
Results: Seventy seven surgical patients with GAC were identified and forty two had a complete preoperative staging and were finally included in the study. With regard to overall accuracy of T staging, EUS was superior to MDCT (62% vs 50%). In a subanalysis of early stages (T1-T2) and advanced stages (T3-T4), accuracy and sensitivity (S) were higher for EUS than for MDTC (83.3% vs 64.29% and 84.4% vs 59.5% respectively), although this did not reach statistical significance. The overall accuracy and sensitivity of EUS for N staging was lower than that for MDCT, although neither comparison reached statistical significance (57% vs 64% and 29% vs 55%).
Conclusions: EUS diagnostic yield is similar to new MDCT with regard to T and N preoperative staging of GAC. Nevertheless, both techniques should be considered as complementary until more extensive and randomized studies can confirm these results.

Key words: Gastric cancer. Staging. Endoscopic ultrasonography. Multidetector computed tomography.

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RESUMEN

Introducción: la ultrasonografía endoscópica (USE) es la técnica de elección para la estadificación loco-regional del adenocarcinoma gástrico (ACG). Sin embargo, la introducción de la tomografía computarizada multidetector (TCMD) permite obtener estudios de muy alta calidad diagnóstica.
Objetivo: nuestro objetivo fue comparar la rentabilidad diagnóstica de la USE frente a la TCMD en la estadificación loco-regional preoperatoria de los pacientes con ACG.
Material y métodos: se realizó un estudio retrospectivo y comparativo entre pacientes intervenidos de ACG con estadificación preoperatoria mediante USE y TCMD de 64 filas, comparando en cada caso los resultados con el informe anatomopatológico final.
Resultados: se analizaron 77 pacientes intervenidos de ACG, incluyéndose finalmente 42 que disponían de estadificación completa. Para la estadificación "T", la precisión diagnóstica (PD) global de USE fue superior a la de TCMD (62% vs. 50%). En un subanálisis entre estadios precoces (T1-2) y avanzados (T3-T4), la PD y sensibilidad (S) de la USE resultaron ser superiores a las de la TCMD (83,3% vs. 64,29% y 84,4% vs. 59,5% respectivamente), aunque sin alcanzarse niveles de significación estadística. Respecto al estadio N, la PD y S de la USE resultaron inferiores a las de la TCMD, aunque tampoco se alcanzaron diferencias estadísticamente significativas (57% vs. 64% y 29% vs. 55%).
Conclusiones: en nuestra experiencia, la rentabilidad diagnóstica de la ecoendoscopia es similar a la de los nuevos TCMD en la estadificación preoperatoria T y N en pacientes con ACG. Sin embargo, ambas técnicas deberían considerarse complementarias hasta que estudios más extensos y aleatorizados puedan confirmar estos resultados.

Palabras clave: Cáncer gástrico. Estadificación. Ecoendoscopia. Tomografía computarizada.

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Introduction

Gastric cancer is the fourth most frequent tumor worldwide and the second cause of cancer related death (1). Surgical treatment is considered to be the only curative option. However, new treatments have been recently proposed that improve survival and decrease morbidity and mortality. Endoscopic mucosal resection provides an alternative to surgery in early stages of the disease (T1a). In locally advanced tumors, neoadjuvant chemotherapy improves the chances of a subsequent complete tumor resection (1). An accurate preoperative staging is necessary in order provide an individualized treatment according to local and distant extension of the disease. Computed tomography (CT) is one of the diagnostic techniques used to determine tumor stage in gastric cancer and was traditionally used to evaluate the presence of distant metastasis. However, due to recent technological advances such as multidetector CT (MDCT), this also provides an accurate evaluation of loco-regional extension (2,3). In recent years, endoscopic ultrasonography (EUS) has been shown to be highly efficient in staging gastric adenocarcimona (GAC) due to its ability to differentiate the gastric wall layers and evaluate the perigastric anatomical structures (4-8). Many studies have demonstrated the value of EUS in loco-regional staging of gastric cancer. However, some professionals question its superiority over MDCT due to limited and heterogeneous studies (9-13). The aim of this study was to compare EUS and MDCT accuracy in local staging of gastric adenocarcinoma.

 

Material and methods

Study population

This was a retrospective and comparative study carried out from January 2012 to January 2016. All surgical patients that underwent a curative resection of GAC (total/partial gastrectomy and lymphadenectomy) with preoperative staging by MDCT and EUS were included in the study. All patients who had received neoadjuvant therapy and those with metastatic disease (M1) at diagnosis were excluded from the study. The MDCT and EUS staging results were compared with histological data of surgical specimens. Radiologists and endoscopists had access to previous imaging results in some cases.

Histological study

Histological staging was performed by an expert pathologist in gastrointestinal histology. TNM classification was used according to the 7^th edition (ed. 2010) of the American Joint Committee on Cancer (AJCC) (14). T1 stage was defined by the invasion of the lamina propria or submucosa, T2 tumors invade the muscularis propria, T3 tumors penetrate the subserosal connective tissue and T4 tumors invade the serosa or adjacent structures.

Endoscopic ultrasound study

The Olympus endoscopic ultrasound GF-UMQ 130 (Olympus, Hamburg) equipment was used with frequencies of 7.5 and 12 MHz. The exploration was carried out with the patient in the left lateral position and sedated using midazolam and propofol. Exploration was performed from the pylorus to the cardias after complete aspiration of the air contained in the gastric cavity; 200-300 ml of water were instilled and perpendicular images of the gastric wall were obtained in order to evaluate the normal mural gastric pattern distributed in five conventional layers. These included: 1^st hyperechoic layer, interface between the water and superficial mucosa; 2^nd hypoechoic layer, deep mucosa-muscularis mucosae; 3^rd hyperechoic layer, submucosa; 4^th hypoechoic layer, muscularis propria; and 5^th hyperechoic layer, adventitia. Ecoendoscopic staging was performed according to the 7^th edition AJCC criteria (14). T staging was performed as previously described. N staging was as follows: N0, absence of pathologic regional lymphatic nodes; N1, 1-2 pathologic lymph nodes; N2, 3-6 pathologic lymph nodes; and N3, seven or more pathologic lymph nodes. Malignant adenopathy was identified when at least two of the following ecoendoscopic criteria were identified: homogeneous hypoechoic pattern, oval-rounded shape, clearly limited border and size greater than 10 mm. When adenopathies were found in distant ganglion areas, endoscopic ultrasound guided fine needle aspiration (FNAB) was carried out in cases where a positive identification of malignant cells would result in a change in therapeutic management. The existence of micro-ascites or peritoneal thickening was evaluated and was considered as a sign of advanced disease and unresectability (M1).

Informed consent was obtained from all patients before the endoscopic examination. All procedures were carried out by one physician (CSH) with more than five year experience in the unit at the time of the study. Identical protocol and inclusion criteria were used. The endoscopy result was compared with that obtained from the MDCT exploration and the surgical sample and/or exploratory laparoscopy-laparotomy.

CT study

A 64-slice MDCT scanner (Siemens SOMATOM Definition, Siemens Medical Solutions, Forchheim, Germany) was used. A total of 500 ml of diluted oral contrast was administered and an automatic injector was used to deliver 80-100 ml of intravenous contrast (Ultravist 300; Bayer Schering Pharma, Berlin, Germany) at 2 ml/sec.

The chest and abdomen were scanned in a cranio-caudal direction with a delay time of 35 and 70 seconds, respectively. Imaging settings were as follows: tube voltage, 120 kVp; tube current, 180 mAs with automatic modulation; slice thickness, 1.25 (for a detector configuration of 64 x 0.6 mm); rotation time, 0.6 sec; and pitch, 1.2. A convolution kernel (B30) and a 512 x 512 pixel matrix were used for image reconstruction.

Axial images were reconstructed with a slice thickness of 3 mm and a reconstruction increment of 1.5 mm. Sagittal and coronal images were reconstructed with a slice thickness of 1.5 mm. Images were reviewed by two radiologists with over ten year experience in gastrointestinal CT scan interpretation using a picture archiving and communication system (PACS). The review was blinded with regard to location, size, surgical findings and histological results. TNM staging using MDCT was performed according to the 7^th edition of the AJCC manual as follows:

- T1 (mucosa/submucosa): the tumor exhibits mucosal layer enhancement and/or thickening as compared to the adjacent healthy mucosa, or low-attenuated layer disruption (less than 50% of thickness).

- T2 (muscularis propria): disruption may be seen in the low-attenuated layer (more than 50% of thickness) without involvement of the outer, high-attenuated layer.

- T3 (subserosa): discriminating between the gastric lesion and the outermost gastric layer is visually impossible except with the presence of a homogeneous, well-delineated border or if the perigastric adipose tissue has a slightly festooned appearance.

- T4 (serosa/adjacent structures): the outer layer border is irregular or nodular and/or perigastric fat density is increased, or there is obliteration of the adipose layer between the gastric lesion and adjacent organs, or directly infiltrated organs can be seen.

Statistical analysis

A normal distribution of quantitative variables was determined using the Kolmogorov-Smirnov test. Quantitative variables were described as mean ± standard deviation (SD) and qualitative variables were expressed as absolute and relative (percentage) frequencies according to their category.

A diagnostic test study was carried out using data from a contingency table of study test findings against the results of the reference test. The following parameters were estimated together with their 95% CIs: sensitivity (S), specificity (Sp), positive predictive value (PPV), negative predictive value (NPV), positive likelihood ratio (LR+) and negative likelihood ratio (LR-). Diagnostic precision (DP) was defined as the percentage of correctly identified patients among the total patients assessed using the study diagnostic tests. The comparison of two proportions test was used to compare percentages; p values less than 0.05 were considered as statistically significant. The degree of agreement between the study diagnostic tests and the gold standard was also assessed using the kappa statistic. All calculations were performed using the SPSS v. 15.0 software package (SPSS Inc. Chicago, IL, 1989-2006).

 

Results

During the study period, 77 patients diagnosed with gastric adenocarcinoma received surgical treatment with a curative intent. Pre-surgical staging with thoracoabdominal MDCT and echoendoscopy was available for 48 patients. Six patients were excluded who had received neoadjuvant therapy and then underwent a surgical procedure. The final statistical analysis included 42 patients with a reference diagnostic test and surgical specimen results. Mean study population age was 70.04 (SD 12.36) years; 26 patients were male (61.9%) and 16 were female (38.1%).

With regard to the globally assessed T stage, the diagnostic precision of EUS was superior to that of MDCT (62% vs 50%) (95% CI, 47-75% and 36-64%, respectively), although statistical significance was not reached (p = 0.38) (Table 1).

 

 

The diagnostic precision of EUS was superior to that of MDCT according to a comparative sub-analysis of early-stage patients (T1-T2) versus advanced-stage patients (T3-T4) (83.3% vs 64.29%) (95% CI, 70.87-95.79% and 48.60-79.97%, respectively). However, it did not reach statistical significance (p = 0.082). The kappa coefficient for the agreement between both techniques and the final histological result was also superior for EUS (0.76 vs 0.43). When the diagnostic accuracy of EUS was specifically assessed for early stages, this value was much higher for T1 (all five cases staged as such were confirmed with the surgical specimen) than for T2 (none of the eight cases were confirmed histologically). Thus, there was a clear tendency toward understaging as five of eight (62.5%) were histologically classified as T3-T4 (Table 1).

EUS sensitivity was also superior to that of MDCT (84.4% vs 59.5%) (95% CI: 70.23-98.52% and 40.80-77.95%, respectively), with a p value at the limit of statistical significance (p = 0.05). Specificity was identical in both groups: 80%, p = 1. EUS PPV vs MDCT PPV was 93.10% vs 90.48%, with an NPV of 61.54% vs 38.10% (Table 2).

 

 

Finally, T1 patients with tumor infiltration to the submucosa including the T1a sub stage (involvement restricted to the mucous membrane), which may be approached endoscopically with curative intent, were compared to patients with more advanced stages (T2-T4). No statistically significant differences were observed between EUS and MDCT with regard to diagnostic precision (92.9% vs 90.5%; p = 1.00) or sensitivity (100% vs 91.2%; p = 0.56). Endoscopic ultrasound sensitivity was inferior to that of MDCT (62.5% vs 87.5%) only in this case but did not reach statistical significance (p = 0.24). Finally, the PPV and NPV of EUS for the identification of advanced gastric adenocarcinoma was 70% and 96.9% (Table 2). No differences with regard to yield were found between both techniques according to histological type (only four cases were signet cell tumors), location or presence of ulceration. The latter was not consistently recorded in reports.

With regard to N stage (N0: no nodal involvement vs N+: N1-N3), diagnostic precision was lower with EUS as compared to MDCT for N0 and higher for N+, although it did not reach statistical significance in all cases (diagnostic precision for N0 was 8/11 patients [72.72%] and 9/31 [29.03%] for N+, p = 0.19 and p = 0.53) (Table 3). The sensitivity was 29% for EUS vs 55% for MDCT (p = 0.07). The specificity was slightly higher for EUS, although non-significant (73% vs 63%; p = 1) (Table 2).

 

 

Discussion

Locally advanced gastric tumors have a high rate of postoperative recurrence and a poor prognosis. Thus, identifying patients who may benefit from neoadjuvant therapy is important. During the past ten years, new adjuvant and neoadjuvant chemotherapy regimens have been introduced which improved the survival of patients with tumor infiltration into the muscularis propria (T2 or higher) or with high suspicion of lymph node infiltration (1,19-22). Previously, the standard of care for gastric cancer was almost exclusively based on surgical resection, which is dependent upon distant spread (M) rather than T and N staging (22). However, the current tailored therapy strategies require accurate and reproducible tumor staging procedures in order to define resectability and the need for adjuvant or neoadjuvant therapy.

EUS and CT represent the most commonly used diagnostic tests in order to evaluate gastric cancer extension, the former technique for loco-regional assessment and the latter to identify distant metastasis. Previous comparative studies of EUS versus CT for the loco-regional staging of gastric tumors were performed in the 1990s, and all of them found a greater diagnostic precision with echoendoscopy as compared to conventional CT with regard to T staging (16-18). During the last few years, the development of helical and multidetector scanners has greatly advanced CT technology, providing more accurate images of the gastric wall and adjacent structures. The recent meta-analysis by Seevaratnam et al. (15) showed an overall precision of 75% for T staging with CT, which rose to 80% when MDCT with four or more detectors was used. The precision was 66% for N staging. Thus, some authors challenge the superiority of EUS over MDCT in the loco-regional staging of locally advanced gastric adenocarcinoma (13). In the only study to date that compared EUS to 64-detector MDCT, almost identical results were obtained by both techniques with regard to T and N staging (overall diagnostic precision: T, 74.7% vs 76.9; N, 66% vs 62.8%) (9).

Furthermore, the impact of the changes made to the recent editions of the TNM classification remains unknown with regard to EUS and CT staging accuracy. There are significant changes in the latest (7^th) edition, on which this study is based, with respect to the previous 6^th edition (2002). T4 is now assigned to serosal involvement (previously it was T3) and lymph-node count for N stages was reduced (N1: 1-2 abnormal nodes, previously 1-6, and N2: 3-6 nodes, previously 7-15) (14). In addition, the "distance" criterion has been modified since the 5^th edition to "number of affected nodes", as noted by Polkowski et al. (22), which may alter EUS diagnostic yield due to the peculiarities of the technique.

The numerous studies performed during the last few decades on EUS yield for the study of gastric adenocarcinoma extension are very heterogeneous. Some describe a marked tendency for overstaging of locally advanced tumors, leading to an overuse of neoadjuvant therapy in over half of patients (23). Other studies (24,25) describe a tendency toward understaging with regard to T and N. These differences (even in the most recent systematic review of 66 publications for a total of 7,747 patients) are not clearly understood (26), but may be related to a number of factors such as varying methodology, the changes in the TNM classification, the type of ultrasound probe and practitioner experience. The yield of EUS is low when discriminating between superficial tumors (T1a vs T1b) and assessing N stage (N0 vs N+) (26). Similarly, diagnostic precision, sensitivity and specificity values are highly variable and range from 50% to 100% in all the case series reported and systematically reviewed until 2016 (5,26). A sustained tendency towards an increased sensitivity may be seen in the detection of advanced T stages (T3-4), with specificity remaining very high (above 90%) for T staging (15). Therefore, a comparison of EUS versus other imaging modalities (CT, magnetic resonance imaging [MRI]) is challenging due to the small number of studies and the heterogeneity of head-to-head studies reported to date (9,22,28-32).

In this series, we set out to compare the yield of EUS with a conventional probe (high-frequency miniprobes do not seem to increase diagnostic yield in advanced stages) versus a latest-generation MDCT using the most recent edition (7^th, 2010) of the AJCC TNM classification. A pathology study of the surgical specimen was used as the gold standard.

This study shows a higher overall diagnostic precision of EUS versus MDCT with regard to T staging, and this difference is more pronounced in a specific sub-analysis of advanced T stages (T3 and T4) as compared to earlier stages. In advanced cases, higher diagnostic precision and sensitivity values were obtained with EUS versus MDCT (DP: 84% vs 55%; S: 84% vs 59.5%), with identical specificity values for both tests (80%). While absolute values were always higher for EUS, no statistically significant differences were found between the groups. There was a tendency toward statistical significance (p = 0.05) for sensitivity but a value < 0.05 was never achieved; this is likely due to the small sample size. The consistency with histologic data was better for echoendoscopy than for MDCT, with a kappa value of 0.76 vs 0.43.

Eight of 42 cases (19.04%) who met early gastric cancer criteria (T1 and any N stage, according to the AJCC) and were candidates for endoscopic or surgical treatment with a curative intent were assessed in a sub-group analysis. The diagnostic yield was higher for MDCT than for EUS (CT sensitivity of 87.5% and EUS sensitivity of 62.5%) although, specificity and PPV were 100% for patients diagnosed with EUS. In general, EUS overstaged three patients with early gastric adenocarcinoma and appropriately identified all patients with advanced gastric adenocarcinoma.

These results suggest that EUS with a conventional 7.5-12 MHz probe provides very high sensitivity and overall diagnostic precision in the T staging of gastric adenocarcinoma. The overall diagnostic precision of EUS was 62% and 50% for CT, which is comparable to the latest generation MDCT. Most relevant is the diagnostic precision for advanced T stages (T3-T4), with a sensitivity of 84% with EUS and 59.5% for MDCT. Therefore, patients requiring neoadjuvant chemotherapy may be identified, which has a demonstrated significant increase in survival (15-21). The diagnostic precision results for EUS in T staging obtained in this study are similar to those reported by recent meta-analyses and other previous studies (Polkowski [22], 63%; Hwang [9], 61.7%). However, they are slightly lower than those reported in the Spanish study by Repiso et al. (70%) (4) and the study by Tsendsuren (68.3%) (32). Even though no statistically significant differences were found between both techniques, as demonstrated in a previous study comparing EUS and MDCT (9), this may be related in our case to a limited sample size. The impact that higher-frequency EUS probes, a prospective randomized design and an increased homogeneous sample size could have on these results is unclear. It should be noted that the differences in T staging results identified by previous studies do not seem attributable to the newer criteria established by the AJCC in the 7^th edition. This is due to the fact that the modifications included only refer to the discrimination between T3 and T4 in the setting of advanced gastric cancer (serosal involvement was considered T3 in the 6^th edition and T4 in the 7^th edition), and these stages were not specifically addressed in this study.

In patients with early-stage gastric cancer (T1), EUS sensitivity decreases significantly versus MDCT (62.5% vs 87.5%), albeit at the expense of a specificity of 100%. This low diagnostic yield of EUS for T1 is difficult to assess due to the reduced sample size in this subgroup. However, it is similar to that reported in the literature (6-9) and does not seem to be improved by the use of high-frequency miniprobes (5,6,15). In fact, ulceration, central depression and extension greater than 20 mm are factors associated with overstaging by EUS (6). In such cases, direct endoscopic resection/dissection is advised without prior EUS staging when endoscopic semiology suggests an early stage (30) as the diagnostic precision of miniprobes is almost identical to that of conventional endoscopy in some studies (79.5% vs 79%) (31). The results of this study in patients with early stage gastric adenocarcinoma may be influenced by the small number of T1 patients (19.04%) which is in contrast with reported series from Southeast Asian countries where gastric cancer screening is performed (65% of T1 cases in the South Korean study by Hwang et al.) (9).

With regard to N staging, our results corroborate those from previous comparative studies using conventional CT, where a higher diagnostic precision and sensitivity were seen for CT in N+ patients regardless of the imaging criteria used to classify a lymph node as pathological (22). The diagnostic precision and sensitivity results of MDCT were superior (CT vs EUS sensitivity, 55% vs 29%), although they never reached statistical significance despite the apparently reduced N requirement in the latest TNM classification (7^th edition).

Our study has limitations derived from its retrospective nature, reduced sample size (particularly for early stage patients) and the fact that physicians analyzing the images could be aware of the results of previous tests. Furthermore, the eventual surgical treatment was not strictly influenced in all patients by the staging results provided by both tests according to the recently issued SEOM guidelines (21). However, the study strengths included the ability to fully compare conventional EUS as implemented in most institutions, latest-generation CT and the laparotomy/surgical specimen as a gold standard in all patients. This is also the only recent staging study using the latest TNM classification (7^th edition, 2010) and discusses its potential impact on diagnostic yield.

To conclude, our results seem altogether to suggest that echoendoscopy still plays a major role in the loco-regional T staging of gastric cancer, with a high diagnostic yield which is comparable to that of the latest generation helical multidetector CT. In view of the technical limitations of EUS in the assessment of N stage, the irreplaceable status of CT for the study of distant spread (M) and the lack of prospective, controlled, larger studies, we consider both tests as complementary for the preoperative assessment of gastric cancer and the planning of individualized treatment. Further studies are needed for a clearer definition of the future role of endoscopic ultrasound versus newer MDCT scanners in this setting.

 

References

1. Ajani JA, Bentrem DJ, Besh S. Gastric cancer, version 2.2013 featured updates to the NCCN Guidelines. J Natl Compr Cancer Netw 2013;11(5):531-46.         [ Links ]

2. Yang DM, Kim HC, Jin W, et al. 64 Multidetector-row computed tomography for preoperative evaluation of gastric cancer: Histological correlation. J Comput Assist Tomogr 2007;31(1):98-103. DOI: 10.1097/01.rct.0000234072.16209.ab.         [ Links ]

3. Chao Y, Zhu ZG, Yan M, et al. Value of multidetector-row computed tomography in the preoperative T and N staging of gastric carcinoma: A large-scale Chinese study. J Surg Oncol 2009;100(3):205-14. DOI: 10.1002/jso.21316.         [ Links ]

4. Repiso A, Lombera MM, Romero M, et al. Utilidad de la ecoendoscopia en la estadificiación preoperatoria del cáncer gástrico: rentabilidad diagnóstica e impacto terapéutico. Rev Esp Enferm Dig 2010;102:413-20.         [ Links ]

5. Mocellin S, Marchet A, Nitti D. EUS for the staging of gastric cancer: A meta-analysis. Gastrointest Endosc 2011;73(6):1122-34. DOI: 10.1016/j.gie.2011.01.030.         [ Links ]

6. Pei Q, Wang L, Pan J, et al. EUS for staging depth of invasion in early gastric cancer: A meta-analysis. J Gastroenterol Hepatol 2015;30:1566-73. DOI: 10.1111/jgh.13014.         [ Links ]

7. Cardoso R, Coburn N, Seevaratnam R, et al. A systematic review and meta-analysis of the utility of EUS for preoperative staging for gastric cancer. Gastric Cancer 2012;15(Supl. 1):19-26. DOI: 10.1007/s10120-011-0115-4.         [ Links ]

8. Puli S-R, Batapati Krishna Reddy J, Bechtold ML, et al. How good is endoscopic ultrasound for TNM staging of gastric cancers. A meta-analysis and systematic review. World J Gastroenterol 2008;14(25):4011-9.         [ Links ]

9. Hwang SW, Lee DH, Lee SH, et al. Preoperative staging of gastric cancer by endoscopic ultrasonography and multidetector-row computed tomography. J Gastroenterol Hepatol 2010;25(3):512-8. DOI: 10.1111/j.1440-1746.2009.06106.x.         [ Links ]

10. Fairweather M, Jajoo K, Sainani N, et al. Accuracy of EUS and CT imaging in preoperative gastric cancer staging. J Surg Oncol 2015;111(8):1016-20. DOI: 10.1002/jso.23919.         [ Links ]

11. Feng X-Y, Wang W, Luo G-Y, et al. Comparison of endoscopic ultrasonography and multislice spiral computed tomography for the preoperative staging of gastric cancer - Results of a single institution study of 610 chinese patients. PLoS One 2013;8(11):e78846.         [ Links ]

12. Hye SA, Lee HJ, Yoo MW, et al. Diagnostic accuracy of T and N stages with endoscopy, stomach protocol CT, and endoscopic ultrasonography in early gastric cancer. J Surg Oncol 2009;99(1):20-7. DOI: 10.1002/jso.21170.         [ Links ]

13. Habermann CR, Weiss F, Riecken R, et al. Preoperative staging of gastric adenocarcinoma: Comparison of helical CT and endoscopic US. Radiology 2004;230(11):465-71. DOI: 10.1148/radiol.2302020828.         [ Links ]

14. Edge SB, Compton CC. The American Joint Committee on Cancer: The 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol 2010;17(6):1471-4. DOI: 10.1245/s10434-010-0985-4.         [ Links ]

15. Seevaratnam R, Cardoso R, McGregor C, et al. How useful is preoperative imaging for tumor, node, metastasis (TNM) staging of gastric cancer? A meta-analysis. Gastric Cancer 2012;15(Supl. 1):3-18 DOI: 10.1007/s10120-011-0069-6.         [ Links ]

16. Botet JF, Lightdale CJ, Zauber AG, et al. Preoperative staging of gastric cancer: comparison of endoscopic US and dynamic CT. Radiology 1991; 181: 426-32 DOI: 10.1148/radiology.181.2.1924784.         [ Links ]

17. Ziegler K, Sanft C, Zimmer T, et al. Comparison of computed tomography, endosonography and intraoperativa assessment in TN staging of gastric carcinoma. Gut 1993;34:604-10 DOI: 10.1136/gut.34.5.604.         [ Links ]

18. Greenberg J, Durkin M, Van Drumen M, et al. Computed tomography or endoscopic ultrasonography in preoperative staging of gastric and esophageal tumors. Surgery 1994;116:696-701.         [ Links ]

19. Paoletti X, Oba K, Burzykowski T, et al. Benefit of adjuvant chemotherapy for resectable gastric cancer: A meta-analysis. JAMA 2010:303:1729-37.         [ Links ]

20. Mezhir JJ, Tang LH, Coit DG. Neoadjuvant therapy of locally advanced gastric cancer. J Surg Oncol 2010;101:305-14. DOI: 10.1002/jso.21483.         [ Links ]

21. Martin-Richard M, Custodio A, García-Girón C, et al. Seom guidelines for the treatment of gastric cancer 2015. Clin Transl Oncol 2015;17:996-1004. DOI: 10.1007/s12094-015-1456-y.         [ Links ]

22. Polkowski M, Palucki J, Wronska E, et al. Endosonography versus helical computed tomography for locoregional staging of gastric cancer. Endoscopy 2004;36:617-23. DOI: 10.1055/s-2004-814522.         [ Links ]

23. Arocena MG, Barturen A, Bujanda L, et al. Resonancia magnética y ecoendoscopia para el estadiaje del cáncer gástrico. Rev Esp Enferm Dig 2006;98(8):582-90.         [ Links ]

24. Kwee RM, Kwee TC. Imaging in assessing lymph node status in gastric cancer. Gastric Cancer 2009;12:6-22. DOI: 10.1007/s10120-008-0492-5.         [ Links ]

25. Kwee RM, Kwee TC. Imaging in local staging of gastric cancer: A systematic review J Clin Oncol 2007;25:2107-16.         [ Links ]

26. Papanikolau IS, Triantafyllou M, Triantafyllou K, et al. EUS in the management of gastric cancer. Ann Gastroenterol 2011;24:9-15.         [ Links ]

27. Choi J, Kim SG, Im JP, et al. Comparison of endoscopic ultrasonography and conventional endoscopy for prediction of depth of tumor invasion in early gastric cancer. Endoscopy 2010;42:705-13. DOI: 10.1055/s-0030-1255617.         [ Links ]

28. Tsendsuren T, Jung SM, Mian XH. Usefulness of endoscopic ultrasonography in preoperative TNM of gastric cancer. World J Gastroenterol 2006;12(1):43-4.         [ Links ]

 

 

Correspondence:
Carlos de la Serna Higuera.
Department of Digestive Diseases.
Hospital Universitario Río Hortega.
C/ Dulzaina, 2. 47012 Valladolid, Spain
e-mail: csernah@hotmail.com

Received: 05-10-2016
Accepted: 07-07-2017