Comparison of Oral Contrast-Enhanced Transabdominal Ultrasound Imaging with Contrast-Enhanced Computed Tomography in preoperative tumor staging of gastric cancer

doi:10.21203/rs.3.rs-1525652/v1

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Comparison of Oral Contrast-Enhanced Transabdominal Ultrasound Imaging with Contrast-Enhanced Computed Tomography in preoperative tumor staging of gastric cancer

https://doi.org/10.21203/rs.3.rs-1525652/v1

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Purpose: To compare the diagnostic accuracy of oral contrast-enhanced transabdominal ultrasound (OCTU) with contrast-enhanced computed tomography (CT) for the preoperative tumor staging of gastric cancer, using postoperative pathology as the standard.

Methods: This prospective study included 108 cases of gastric cancer with simultaneous OCTU and enhanced CT preoperative tumor staging diagnoses. Results were compared with postoperative pathology based on the 8th edition of the American Joint Committee on Cancer (AJCC) tumor-node-metastasis (TNM) staging guidelines for gastric cancer. The accuracy of each tumor stage was obtained by comparing OCTU and enhanced CT diagnoses with postoperative pathology. The McNemar test was used to compare the overall accuracy of the two methods.

Results: There was no statistical significance in the accuracy of OCTU (72.2%) and enhanced CT (75.9%; P = 0.644) for overall preoperative tumor staging diagnosis. For stages T1 to T4, the accuracy rates of OCTU were 84.2%, 81.8%, 69.4%, and 65.5%, respectively, and that for enhanced CT were 52.6%, 72.7%, 87.8%, and 72.4%, respectively.

Conclusions: OCTU is comparable to enhanced CT in the preoperative overall T-stage diagnosis of gastric cancer.

Oral Contrast-Enhanced Transabdominal Ultrasound

Contrast-Enhanced Computed Tomography

Gastric Cancer

Neoplasm Staging

Gastric cancer is a malignant tumor originating from the epithelium of the gastric mucosa. It has the fifth-highest incidence rate among cancers and is the third leading cause of cancer deaths(1). Early gastric cancer often has no obvious symptoms, and most cases reach an advanced stage when symptoms appear(2). Gastric cancer staging is an important indicator that affects the survival and prognosis of patients(3). Surgical resection is the main treatment for gastric cancer, and preoperative staging can help select an individualized plan that is most beneficial to the patient. Treatments include endoscopic stripping, surgical operation, adjuvant chemotherapy, and multimodal treatment plan. Endoscopic and surgical options for early gastric cancer can especially increase the 5-year recurrence-free rate of patients(1, 4, 5). Preoperative identification of tumor staging for advanced gastric cancer can effectively determine the best intervention time for radical resection, so as to prevent patients from undergoing surgical operations for maintenance, with low survival benefits, and having to face the risk of surgical complications and perioperative chemotherapy(4–6).

Currently, enhanced computed tomography (CT) is the preferred tumor-staging modality for gastric cancer(1). Conventional ultrasound is limited for the diagnosis of gastric cancer due to gas interference and other factors. Recently, oral contrast-enhanced transabdominal ultrasound (OCTU) has been used to visualize the gastric wall and is increasingly standardized for the diagnosis and staging of gastric cancer(7–9). Here, the preoperative T stage of gastric cancer was compared between OCTU and simultaneous enhanced CT, with the aim to evaluate the application value of OCTU, as well as to provide a more comprehensive imaging evaluation for preoperative T staging of gastric cancer.

Patient cohort

From September 2020 to November 2021, 197 patients who were initially diagnosed with gastric cancer by gastroscopy biopsy and who then underwent OCTU examination at our hospital were prospectively and continuously recruited. The inclusion criteria were as follows: (1) no obstruction, active bleeding, or other clinical fasting conditions; (2) first diagnosis of gastric cancer; and (3) not receiving adjuvant therapy such as radiotherapy and chemotherapy. The exclusion criteria were: (1) no gastrectomy in 2 weeks; (2) enhanced CT data missing; (3) the quality of any imaging was poor and the tumor stage could not be diagnosed; and (4) the diagnosis of either of the two imaging modalities of the lesion was unclear. The detailed process of inclusion and exclusion is represented in Fig. 1.

Both OCTU and enhanced CT were used for preoperative T staging diagnosis of the lesions.

OCTU examination

All patients were examined using a GE LOGIQ E9 device (GE Healthcare, Wauwatosa, WI, USA) with an abdominal convex array probe (3.0 ~ 5.0 MHz) and a line array probe (5.0 ~ 12.0 MHz). Before the examination, patients fasted for > 8 h and did not drink water for more than 2 h.

During the examination, patients were instructed to take a 400 ml echo-type visualization aid oral contrast agent (commercially available Tianxia brand, 50 g/pack, a mixture consisting of coix seed, yam, tangerine peel, and rice. It is an echo-type gastrointestinal aid, which can form an acoustic window. The high-viscosity factor in the auxiliary agent is in full contact with the gastrointestinal mucosal layer, and the specific gravity effect is used to improve gastric ultrasound imaging. East Asia Institute of Gastrointestinal Ultrasound, Huzhou, China).

The convex array probe was used to scan the cardia, gastric fundus, gastric body, gastric angle, and gastric antrum, and the corresponding slices were stored in sequence. A linear array probe was used to observe the layers of the stomach wall at the lesion. The lesion location, shape, size, echo, blood flow, etc. of the lesion was observed and the images were stored.

Enhanced CT examination

All enhanced CT scans were performed using a 64-slice multi-detector scanner (Discovery CT750 HD, GE Healthcare, Milwaukee, WI, USA). Patients fasted for at least 6 h and were expected to ingest approximately 1500 mL of water to achieve adequate distension of the gastrointestinal tract within 1 h prior to the scan. The iodine-based contrast agent (Optiray, 350 mg I/mL, Mallinckrodt, Canada) was administered at a rate of 3–4 mL/s using an automatic power injector (Stellant; Medrad, Indianola, PA, USA) according to the weight-based algorithm (1 mL/kg), and then flushed with a 20 mL saline solution.

The enhanced CT scan parameters included 120-kV tube voltage, automatic tube current (range from 80 to 260 mA), 512 × 512 matrix, and an appropriate field of view to fit the patient. Images were acquired with a slice thickness of 5 mm for primary review and then reconstructed to 3 mm-thick images for multi-plane assessment. Dual-phase images were obtained at 20–30 s (arterial phase) and 55–60 s (intestinal phase) after the injection of an intravenous contrast agent via the antecubital vein. The inspection interval between all enhanced CT and OCTU did not exceed 1 week.

Pathology, OCTU, and enhanced CT staging standards (Table 1).

Image analysis

OCTU image diagnosis and tumor staging were performed by two sonographers with at least 5 years of experience in abdominal ultrasound, while enhanced CT diagnosis and tumor staging were performed by two radiologists with more than 10 years of experience in abdominal CT.

All diagnosing physicians perform tumor staging of patients before surgery under independent conditions using a single imaging modality. When the diagnosis is divergent, the differences were resolved after discussion.

Pathology

All cases underwent gastrectomy, and postoperative histopathological data were complete.

Statistical analysis

The patient’s age and body mass index (BMI) were expressed as mean ± standard deviation. The accuracy, sensitivity, and specificity of OCTU and enhanced preoperative CT staging were calculated based on the postoperative pathology. The McNemar test was used to compare the accuracy of the preoperative staging of the two methods, and a P < 0.05 indicated statistical significance.

There were 126 cases with complete pathological staging data, complete OCTU, and enhanced CT images with acceptable image quality. The overall, early, and advanced detection rates of the 126 cases of gastric cancer were 93.6%, 77.8%, and 100% by OCTU; and 86.5%, 55.6%, and 98.9% by CT, respectively. The detailed detection rates of the two imaging modalities in each period are shown in Table 2. Among the 126 cases, 8 were unclear on ultrasound, 17 were unclear on CT, and 7 were unclear on both. Finally, 108 patients with comparable stages were included.

A total of 108 patients (79 men and 29 women; mean age, 61.7 ± 11.2years; age range, 27–87 years; mean BMI, 22.4 ± 3.2kg/m²; BMI range, 15.3–33.1 kg/m²) were enrolled in this prospective comparative study. The main locations of intraoperative combined gastroscopy lesions were 15 cases at the cardia, 9 cases at the gastric fundus, 33 cases at the gastric body, 14 cases at the gastric angle, and 37 cases at the gastric antrum.

The pathological features were adenocarcinoma in 103 cases and other types in five cases. Nineteen cases were of early gastric cancer with tumor invasion depth limited to the submucosa and 89 cases were of advanced gastric cancer (Table 3).

OCTU [72.2% (78/108)] and enhanced CT [75.9% (82/108), P = 0.644] were comparable in accuracy for the overall T staging diagnosis of gastric cancer. The accuracy of OCTU in the T1 stage of gastric cancer was better than that of enhanced CT (P = 0.031), additionally, the accuracy of OCTU in the T2 stage was also slightly better than that of enhanced CT; however, the differences were not statistically significant (P > 0.999). Furthermore, the accuracy of enhanced CT in the T3 stage of gastric cancer was better than that of OCTU (P = 0.049), and the accuracy of CT in the T4 stage was also better than that of OCTU, but there were no statistically significant differences (P = 0.804). Comparison of diagnostic accuracy of OCTU and enhanced CT in each tumor Stage is shown in Table 4.

In early gastric cancer, OCTU classified two cases of T1 stage as T2 stage, one case of T1 stage as T3 stage. Enhanced CT classified seven cases of T1 stage as T2 stage and two cases of T1 stage as T3 stage. Among them, both OCTU and enhanced CT classified one case of T1 stage as T3 stage. The pathology of this case indicated that the cancer was confined to the submucosa, while the accompanying ulcer reached the subserosal layer. Among advanced gastric cancers, OCTU judged ten cases of tumor invasion depth too deeply, 17 cases too shallowly, and the corresponding number of cases with enhanced CT was six and 11, respectively (Table 5). The images of the OCTU and enhanced CT T1–T4 stages are shown in Figs. 2–5.

Research has shown that drinking water can effectively diagnose the depth of gastric cancer invasion after filling the gastric cavity(10, 11). In our study, the echogenic visualization aid of the grain mixture was used to fill the gastric cavity, achieving full contact with the gastric mucosa, staying in the gastric cavity for an extended time, and providing sufficient observation time to achieve clear visualization of the gastric wall. OCTU can evaluate the depth of tumor invasion by examining the disorder and the interruption to the gastric wall(7, 9, 12). In this study, the accuracy of OCTU's overall T staging rate was 72.2%, and the accuracy rates of T1 to T4 stages were 84.2%, 81.8%, 69.4%, and 65.5%, respectively. In a similar study, Liu et al. showed that the accuracy of OCTU in the overall staging of gastric cancer was 77.3%(13). In addition, studies by He et al. and Wang et al. showed that OCTU combined with venography (double contrast-enhanced ultrasound) can effectively supplement endoscopic ultrasound (EUS) and enhance the accuracy of preoperative gastric cancer T staging by CT(8, 9). EUS is the main method used for T staging in early gastric cancer. Large sample studies reported an accuracy rate of approximately 67.4%(14). Enhanced CT is currently the preferred imaging method for preoperative staging of gastric cancer. The overall accuracy of T staging is 73%-91%(15–21). The range of accuracy is first related to the sample size of each T stage included in the study and technological progress. The latest research shows that under the condition of the gastric window of enhanced CT, the T1 and T2 stages of gastric cancer can be diagnosed more accurately(22).

In this study, OCTU inaccurately determined the T stages of 30 gastric cancer cases. These included nine cases of T3 which were overstaged as T4 and seven cases of T4 which were understaged as T3. The difference between T3 and T4a in pathological staging is that in T3 the tumor has only invaded the subserosal connective tissue and not the visceral peritoneum. The resolution of ultrasound imaging depends on the difference in tissue echo between the interfaces. The five-layer structure of the normal gastric wall shows three high echo light bands and two low echo light bands in OCTU. From inside to outside, are high (superficial mucosa), low (muscular mucosa), high (submucosa), low (muscular propria), high (serosa and extraserosa adipose tissue) strip echo. Subserosal connective tissue and visceral peritoneal echo are hyperechoic, especially when combined with micro-invasion of cancer foci, it is difficult to judge by ultrasound whether the visceral peritoneum has been invaded. While enhanced CT can be more sensitive in judging the invasion of the serous membrane, diaphragm, omentum, abdominal wall, and other tissues(23, 24).

In addition to the above 16 cases with inaccurate staging, we also had 10 cases that were inaccurately staged. Of these, the cancer foci of seven cases were located in the greater curvature of the gastric body. The possible reasons for inaccurate staging could be that the depth exceeds the best observation distance range of the line array high-frequency probe, and the reduced resolution makes it difficult to distinguish the middle structure of the stomach wall. Both OCTU and enhanced CT in early gastric cancer identified one case of T1 as T3. The pathology of this case suggested that the cancer foci were limited to the submucosa, and the accompanying ulcer reached the subserosal layer. Ulcerative cancer tissue and normal gastric tissue penetrated by ulcers interfere with OCTU and enhanced CT to judge the depth of tumor invasion. So, both OCTU and contrast-enhanced CT may stage too deep, and the depth of ulcer penetration is misjudged as the depth of tumor invasion. Two cases of T1 were overstaged as T2, they were gastric antrum poorly differentiated carcinoma, which indicates that the inaccurate stage may be related to tumor differentiation, stronger gastric motility at the gastric antrum, and more gastric wall folds. One case of T2 was overstaged as T3 by OCTU, and postoperative pathology showed that both nerves and vessels were invaded. It was analyzed that the deep staging of this case may be related to the existence of tumor microinfiltration.

In this study, seven cases of T1 were overstaged as T2 by enhanced CT (six cases of poor differentiation and one case of moderate-low differentiation), compared with differentiated gastric cancer, undifferentiated gastric cancer lacks blood vessels and manifests as diffuse infiltration, and the use of angiographic contrast agents has an impact on the accuracy of CT staging(25, 26). Studies have pointed out that histological differences and perivascular infiltration have a certain influence on the accuracy of enhanced CT staging, and undifferentiated and inflammatory gastric cancer tends to be overstaged(27). In addition, enhanced CT is excellent in imaging the blood supply of tumors, but tomographic imaging has a partial volume effect, which may lead to overstaging, and insufficient gastric wall opening will also affect the accuracy of staging.

Currently, preoperative T staging comparison between OCTU and enhanced CT focuses on advanced gastric cancer. In our study, all tumor stages of gastric cancer were included for a more comprehensive comparison. There was no significant significance (P = 0.644) in the overall staging accuracy between OCTU [72.2% (78/108)] and enhanced CT [75.9% (82/108) ].

The accuracy of OCTU staging was higher than those of enhanced CT for T1 and lower for T3 stage (P<0.05). While the accuracy of OCTU staging was higher than those of enhanced CT for T2, and lower for T4 stage (P>0.05)

OCTU is better than enhanced CT in determining the depth of tumor invasion in the submucosa and lamina propria. This may be because ultrasound has a high resolution for soft tissues and can observe the detailed local conditions of small lesions in multiple directions. Early gastric cancer often has small lesions and no obvious enhancement of the mucosa, especially when there is edema, which will affect the 50% judgment index of the total thickness of the gastric wall on enhanced CT(28). Spatial resolution in enhanced CT is not affected by tumor location. Tumor blood supply imaging outlines the depth of invasion and is better than OCTU in identifying occult invasions such as the peritoneum and diaphragm(23).

In this study, firstly, the sample size of T2 stage accounted for a small proportion, and it is necessary to increase the sample size of T2 stage by expanding the sample size to improve the reliability and the diagnostic accuracy of OCTU staging. Secondly, patients with preoperative CT staging of T4b often lose the opportunity for radical surgery and received adjuvant chemotherapy first. Such patients could not obtain accurate pathological staging results and were not included in this study, which resulted in inclusion bias for the study population.

Among the preoperative staging methods for gastric cancer, EUS is invasive, and enhanced CT has the disadvantages of ionizing radiation, contrast agent allergy, and relatively high cost. The advantages of OCTU, such as low cost, no radiation, and convenience, provide clinicians and patients with more options.

In summary, enhanced CT is better than OCTU in evaluating T3 and T4 stages; that is, it is more accurate in judging tumor invasion of the visceral peritoneum and surrounding organs. Its excellent spatial resolution can visually display a wide range of lesions, which is an irreplaceable preoperative staging imaging method for gastric cancer. OCTU was more effective for T1 and T2 staging. It can assist enhanced CT for accurate preoperative T staging of gastric cancer, especially in patients with enhanced CT contraindications, such as patients with low renal excretion and allergy to contrast agents.

American Joint Committee On Cancer (AJCC), Tumor-Node-Metastasis (TNM), Oral Contrast-Enhanced Transabdominal Ultrasound (OCTU), Contrast-Enhanced Computed Tomography (CT), Body Mass Index (BMI), Endoscopic Ultrasound (EUS)

Acknowledgements

We wish to thank the timely as well as free help given by Gastrointestinal Surgery and Radiology Department of our hospital in analyzing the large number of samples.

Funding

No funds, grants, or other support was received.

Ethics approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the Bioethics Committee of Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology (TJ-IRB20210974), and the research has received informed consent from all participants.

Data Statement

The data that support the findings of this study are available on request from the corresponding author.The data are not publicly available due to privacy or ethical restrictions.

Consent to Publish

The study was approved by the Bioethics Committee of Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology (TJ-IRB20210974), and the research has received informed consent from all participants.

Competing interest

All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript.

Author Contributions

guarantor of integrity of the entire study: KaiYan Li, LingLing Wu
study concepts and design: KaiYan Li, LingLing Wu
literature research: LingLing Wu, JunYi Xin
clinical studies: KaiYan Li, JingJing Wang,QunQun Feng, XiaoLi Xu
experimental studies / data analysis: LingLing Wu
statistical analysis: LingLing Wu
manuscript preparation: LingLing Wu
manuscript editing: KaiYan Li, LingLing Wu, JunYi Xin, JingJing Wang,QunQun Feng, XiaoLi Xu

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Table 1

Staging standards for pathology (AJCC 8^th edition), OCTU, and enhanced CT

Tumor invasion depth (T stage)		Pathology	OCTU	Enhanced CT
T1	T1a	Tumor invades lamina propria, or muscularis mucosa	The dark area of the second layer (mucosal layer) is thickened	Continuous and complete low-enhancement bands can be seen between the inner layer of high-enhancement cancer and the outer layer of slightly higher-enhanced muscle layer
T1	T1b	Tumor invades submucosa	The thickened dark zone extends from the second layer (mucosal layer) to the third layer (submucosa) but has not reached the fourth layer (muscularis propria)
T2	T2	Tumor invades muscularis propria	The thickened dark area reaches, but has not penetrated, the fourth layer, and the outer layer retains a smooth echo boundary	Interruption and disappearance of the low-strength band in the middle layer, and the remnant part of the outer layer is slightly higher to strengthen the muscular layer
T3	T3	Tumor penetrates subserosal connective tissue without invasion of visceral peritoneum or adjacent structures	The structure of each layer disappeared completely, but the hyperechoic zone (serosa layer) remained on the outermost side	High-enhancing cancer invades the entire layer of the stomach wall, with a smooth serous surface or a few short thin cords
T4	T4a	Tumor invades serosa (visceral peritoneum)	The structure of each layer disappears, and the hyperechoic zone of the serosa layer disappears at the same time, or the "burr sign" or "crab foot sign" that clearly shows the strong echo line breakthrough of the serosal layer can be seen	Irregular or nodular morphology of serosal surface, dense burr or band-like infiltration of the surrounding fat gap
T4	T4b	Tumor invades adjacent structures	Full-thickness involvement, and the echo boundary with neighboring organ structures (spleen, pancreas, liver, etc.) disappeared	Disappearance of the fat gap with adjacent structures, finger-like insertion or direct infiltration is the exact sign of invasion

Table 2 Gastric cancer detection rate by OCTU and enhanced CT (n=126)

Postoperative pT staging Detection rate (%)	OCTU	enhanced CT	P-value
T1	77.8（28/36）	55.6（20/36）	0.021
T2	100（12/12）	91.7（11/12）	1.000
T3	100（49/49）	100（49/49）	1.000
T4	100（29/29）	100（29/29）	1.000

Table 3 Characteristics of 108 cases of gastric cancer

characteristics	Number of cases (n)
The main anatomical parts of the lesion (intraoperative combined gastroscopy)
Cardia	15
Fundus of stomach	9
Gastric body	33
Gastric horn	14
Gastric antrum	37
Extent of gastric resection
Proximal stomach	12
Distal stomach	53
Whole stomach	43
Macroscopic appearance
Paris type
0-Ⅰ	1
0-Ⅱb	6
0-Ⅱc	1
0-Ⅲ	11
Borrmann type
Ⅰ	16
Ⅱ	57
Ⅲ	6
Ⅳ	10
Pathology
Adenocarcinoma	103
Medullary carcinoma with lymphoid stroma	1
Neuroendocrine carcinoma	1
Small cell carcinom	1
Poorly cohesive	1
Undifferentiated carcinoma	1
Pathological differentiation
Well	3
Between well and moderate	4
moderate	17
Between moderate and poor	29
poor	54
Undifferentiated	1
Pathologic stage
T1a	6
T1b	13
T2	11
T3	49
T4a	26
T4b	3

Table 4 Comparison of diagnostic accuracy of OCTU and enhanced CT in each Tumor Stage

postoperative pathology (cases）	Accuracy of OCTU ( %)	Accuracy of enhanced CT ( %)	P-value
19	84.2	52.6	0.031
11	81.8	72.7	1.000
49	69.4	87.8	0.049
29	65.5	72.4	0.804

Table 5 Preoperative staging of OCTU and Enhanced CT stage Compared With Postoperative pathological stage for Each Tumor Stage

Imaging tumor stage	Postoperative pathology
Imaging tumor stage	T1（n=19）	T2（n=11）	T3（n=49）	T4（n=29）
OCTU
T1	16	1	1	1
T2	2	9	5	2
T3	1	1	34	7
T4	0	0	9	19
Enhanced CT
T1	10	1	0	2
T2	7	8	2	1
T3	2	2	43	5
T4	0	0	4	21

No competing interests reported.

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Comparison of Oral Contrast-Enhanced Transabdominal Ultrasound Imaging with Contrast-Enhanced Computed Tomography in preoperative tumor staging of gastric cancer

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