CT Findings in Patients with Esophageal Carcinoma and Its Correlation with Esophagographic Findings

Aim of the Study: Aim of this study is to evaluate the patients of biopsy proven esophageal carcinoma with Contrast CT studies (CECT thorax, abdomen or neck), correlate and compare the CT findings with esophagographic findings in each case and with biopsy findings wherever possible. Materials and Methods: Fifty (50) biopsy proven cases of esophageal carcinoma were taken into study in Radiology Department of Govt. Medical College, Patiala, Punjab after informed consents. All the patients underwent esophagography with barium sulphate as the contrast material and contrast enhanced CT scan of neck and/or thorax and/or abdomen. In all cases, esophagographic study preceded the CT scan. The time gap between the two studies was kept to the minimum to make the studies comparable. Results: The CT findings were found to have significant correlation with the esophagographic findings (p value > 0.05 in each finding) in regard to luminal narrowing, proximal dilatation and hold up of contrast, eccentricity of growth, site involved, length of growth, involvement of pyriform sinuses/valeculla and involvement of GE junction. Conclusions: CT study primarily helps to rule out unresectable or distant metastatic disease. Barium studies cannot provide any information regarding local invasion into mediastinal structures, regional or non-regional lymphadenopathy or metastases to distant organs which are significant for determining the treatment modality. CT has an advantage over esophagography for these information.


Introduction
The prevalent histology of esophageal tumors is Squamous cell carcinoma in most parts of the world [1].More than 90% of esophageal cancers are either Squamous cell carcinoma (SCCs) or Adenocarcinoma [2].Other histological types like small cell carcinoma (oat cell carcinoma) are extremely rare.Non-regional lymph nodes metastases are designated as M1a disease because patients with M1a disease have a worse prognosis than those with N1 disease [3].In general, intra-thoracic and abdominal lymph nodes greater than 1 cm in diameter are considered to be enlarged, and supraclavicular lymph nodes with a short axis greater than 5 mm are considered to be pathologic [4] [5].
Regional Lymph Nodes in Esophageal Cancer [6] 1) Cervical esophagus Scalene, Internal jugular, Upper and lower cervical, Periesophageal, Supraclavicular 2) Intra-thoracic esophagus (upper, middle and lower) Upper periesophageal (above the azygos vein)-Subcarinal Lower periesophageal (below the azygos vein) 3) Gastro-esophageal junction Lower esophageal (below the azygos vein), Diaphragmatic, Pericardial, Left gastric, Celiac.Non-regional lymph nodes include cervical lymph nodes (for proximal esophageal tumors) and celiac axis lymph nodes (for distal esophageal tumors).Celiac lymph nodes are considered to be regional lymph nodes if the tumor involves gastro-esophageal junction.The sensitivity of spiral CT for the detection of masses 1 cm or larger is approximately 90% [7].
Barium studies are often used to evaluate these patients and double contrast barium studies have been found to be a sensitive technique for detection of carcinoma esophagus and esophagogastric junction with a positive predictive value of 42% [8].When an esophageal stricture is identified by esophagography, it may be classified as benign or malignant.Benign strictures typically have symmetric areas of narrowing with smooth contour and tapered proximal and distal margins.Malignant strictures typically cause asymmetric narrowing with abrupt, shelf like margins and irregular contours with a nodular or ulcerated mucosal surface [9].Esophageal tumors can be polypoidal, infiltrative, varicoid or ulcerative when seen by esophagography [10].Superficial spreading lesions tend to show a nodular mucosal pattern without a well-defined mass.Early esophageal cancers may have very subtle findings on barium studies and therefore endoscopic follow-up of any suspected abnormality should be performed [9] [10].In depressed lesions, the presence and size of mucosal surface granules were found to correlate with the depth of invasion, as did thickened folds and esophageal wall rigidity [11] [12].Gastric invasion is an unusual finding with Squamous cell carcinoma, which largely occur in the middle third of esophagus [13].Complications such as tracheo-esophageal fistula formation from a locally advanced disease can be seen on barium studies.Once a diagnosis of esophageal malignancy has been established, barium studies may be used to evaluate the morphology and size of tumors before and after treatment.Esophageal cancer can easily spread to adjacent structures in the neck or thorax, including the trachea, thyroid gland, larynx, bronchi, aorta, lung, pericardium, and diaphragm [14].Tracheo-bronchial invasion may result in tracheo-esophageal or broncho-esophageal fistulas [15].It may be difficult to determine whether two discrete lesions represent synchronous primary tumors or a single cancer with disseminated lymphatic metastases [13].The most common sites of metastases includes the liver, lungs, bones, adrenal glands, kidneys, and brain, in descending order of frequency of occurrence [16] [17].
Computed tomography (CT) is considered complimentary to endoscopy and barium studies and is used to stage and follow esophageal cancers.CT can be used to define the local extent of tumor by showing the extent of involvement of esophageal wall by tumor and tumor invasion of periesophageal fat.CT cannot reliably delineate the individual layers of the esophageal wall and therefore cannot distinguish between T1 and T2 lesions.Infiltration of the tumor into the periesophageal fat as seen on CT denotes a T3 tumor and does adversely affect prognosis, although en-bloc resection for cure may still be attempted [18].The reported accuracy of CT in diagnosing mediastinal invasion ranges from 59% to 82% [18].Tumor infiltration to involve adjacent mediastinal structures such as the aorta or tracheo-bronchial tree denotes a T4 lesion that is considered inoperable.Contiguous invasion of adjacent structures may be difficult to predict when tumor abuts other structures in the mediastinum.Specific findings of tracheo-bronchial invasion include demonstration of a tracheo-bronchial fistula or tumor extension within the airway lumen.If the esophageal tumor indents or displaces the adjacent airway, invasion is likely.Thickening of the wall of tracheo-bronchial tree also suggests invasion.Loss of fat planes between the tumor and the adjacent airway is not always a specific finding for tumor invasion and may be seen in normal individuals; however, if the loss of fat planes occurs only at the level of esophageal mass with preservation of fat planes cranially and caudally, invasion is likely.Virtual endoscopy has been attempted to determine its value in patients with esophageal cancer infiltrating the tracheo-bronchial tree and found to be accurate in identifying endoluminal tumors in those patients who were not amenable to endoscopy although it could not be used to replace endoscopy in all patients with tracheo-bronchial invasion [19].The overall circumference of contact between tumor and the aortic wall was shown to be a useful predictor with an interference arc greater than 90 degrees suggesting invasion [20].The loss of the triangular area of fat between the esophagus, aorta and spine has also been used to predict aortic invasion [21].The normal esophageal wall is usually less than 3 mm thick at CT when the esophagus is distended [22]; any wall thickness greater than 5 mm is considered abnormal [23].CT is unable to adequately help differentiate between T1, T2 and T3 disease, a distinction that is important when considering the use of neo-adjuvant chemotherapy and radiation therapy [24].Exclusion of T4 disease, as indicated by the preservation of fat planes between the esophageal cancer and the adjacent structures, is the most important role of CT in the determination of T status [25].
Displacement of the trachea or bronchus, or indentation of the posterior wall of the trachea or bronchus by the tumor, have also proved accurate in predicting tracheo-bronchial invasion [26].Pericardial invasion is suspected if pericardial thickening, pericardial effusion, or indentation of the heart with loss of the pericardial fat plane is seen.The reported sensitivity and specificity of CT for detecting mediastinal invasion in patients with esophageal cancer are 88% to 100% and 85% to 100% respectively [27].Although obliteration of fat planes is a reliable sign of tumor involvement of adjacent structures, it can also occur in cachectic patients or in patients who have undergone radiation therapy or surgery [27].

Material and Methods
The study was carried out in the Department of Radio-diagnosis, Rajindra Hospital, Patiala, Punjab (India) during December 2010 to June 2012.Fifty (50) biopsy proven patients of esophageal carcinoma were included in the study after informed consent.All the patients underwent esophagography with barium sulphate as the contrast material and contrast enhanced CT scan of neck and/or thorax and/or abdomen.In all the cases, esophagographic study preceded the CT scan.The time gap between the two studies was kept to the minimum to make the studies comparable.
Patients were scanned using Siemens 6 slice Somatom Emotion Machine.Soft copy images were studied and analyzed on the high resolution radiology monitor.Hard copy was available for the patient referral.The details of the procedure were explained to the patient.Serial CT slices were obtained at a distance of every 8mm.Axial images were taken of the body part (neck, thorax or abdomen) under study.Coronal and sagittal reconstructions were done whenever needed.Each study was done with straight gantry.Slice thickness of 8mm with 8mm collimation was used.Very uncooperative patients were studied after giving mild sedation to the patient.Documentation was done with a window width of 300 for non-enhanced (NE) CT and 350 for contrast enhanced CT (CECT).The window centre selected was 30 -50 for NECT and CECT.Bone windows for possible bony involvement i.e.W2300/C-250 and lung window for possible parenchymal or pleural involvement were obtained in all relevant cases (W = 1600, C = −600).
Non-ionic contrast (Ioversol) was used in our study.Contrast was injected intravenously by the peripheral intravenous route.Continuous monitoring of the vital parameters and allergic reactions (if any) was done during contrast injection.Oral contrast was given in all cases.
Single contrast esophagographic studies were done on 500 mA X-ray machine of Allangers.Barium sulphate solution was used as contrast material in these studies which was prepared by diluting the Barium sulphate powder with water in a ratio of 1:1 dilution.
Patients were advised to come in the morning time with overnight fasting in order to prevent aspiration during the procedure.The procedure was well explained to the patient before starting it.All the studies were done with the pa-
Regional lymphadenopathy was seen in 60% of the cases whereas non-regional lymphadenopathy was seen in 18% of the cases.Lymph nodes more than 1cm in size in short axis diameter were only considered to be significant.Most of the patients have esophageal wall thickness > 15 mm (78%), 22% of the patients have esophageal wall thickness between 5 -15 mm.Distant metastases to lung and bone were seen in 2 (4%) patients and 1 (2%) patient respectively.Distant metastases to liver were seen in 4 (8%) patients.
Figure 1 shows esophagographic findings and CT findings in a patient with liver and lung metastases.
Local invasion of the structures adjacent to the growth included Tracheo-bronchial (10%), Aortic (8%), Gastric (8%), Pericardium (2%) and Pyriform sinuses/Valeculla (2%) invasion.The esophageal wall thickening or mass was eccentrically located in 58% of the cases with atleast minimal luminal narrowing seen in all the 50 Cases (100%).Dilatation of the esophagus proximal to the obstructing growth was seen in 30 cases (60%).In 70% of the patients, periesophageal soft tissue or fat stranding was seen.The cranio-caudal length of the growth were as follows: ≤2 cm (6%), 2.1 -4 cm (38%), 4.1 -6 cm (42%), 6.1 -8 cm (10%), >8 cm (4%).The most common type of growth visualized was ulcerative (44%) followed by infiltrative (40%).Other less common types of growth seen were polypoidal (6%) and fungating types (10%).Except for 1 case, the strictures seen in rest of the 49 cases (98%) were of the irregular type (having irregular margins).Mucosal destruction/irregularity was the most common All the 3 cases of Adenocarcinoma were found in the lower esophagus, none of the Adenocarcinoma was seen in upper or middle esophagus.However, Squamous cell carcinoma was seen in all the parts of esophagus-upper (14%), middle (40%) and lower (40%).The CT findings were found to have significant correlation with the esophagographic findings (p value > 0.05 in each finding) in regard to luminal narrowing, proximal dilatation and hold up of contrast, eccentricity of growth, site involved, length of growth, involvement of pyriform sinuses/valeculla and involvement of GE junction.

Discussion
In this study, 29 patients (58%) were males and 21 patients (42%) were females, thus having a slight male predominance with a M:F ratio of 1.38:1.In a study by Mohebbi et al. [28] on 1693 patients with esophageal carcinoma in Iran, the sex ratio of M:F in esophageal carcinoma was 1.1:1.In a study by Sinha et al. [29], the M:F ratio in patients having carcinoma esophagus was compared between that in US (M:F ratio = 3.5:1) with that in India (M:F ratio = 1.49:1).In a study in Tamil Nadu of India by Cherian et al. [30], M:F ratio was found to be 2.16:1 in patients with esophageal carcinoma.In the study by Khan et al. [31] in valley of Kashmir, Northern India, the M:F ratio was 2.4:1.Thus, the present study correlates well with previous studies done.Most common age group of patients affected were between 55 -65 years of age (38%) followed by above 65 years of age (24%) and it was found to be rare in ≤35 yrs of age (6%).In a study by Chitra et al. [32], most common age group affected was 51 -60 yrs (38%) followed by 61 -70 (24%) and was found to be rare in age < 40 yrs (5%).In another study by Gatei et al. [33] on 40 patients of Kenyan population, the most common age group affected was 50 -60 yrs.In a study on 1077 patients by Huang et al. [34], 50% of the cases were seen in age 40 -60 yrs and 49% of the cases were seen in age > 60 yrs.In another study by Subhasinge et al. [35] on 48 patients, the median age of patients with esophageal carcinoma was 59.5 years.Thus, the present study correlates well with the previous studies done.
The most common histological type was Squamous cell carcinoma (94%) followed by Adenocarcinoma (6%).In a study by Cherian et al. [30] on 994 south Indian carcinoma esophagus patients, Squamous cell carcinoma and Adenocarcinoma were seen in 92% and 8% of the cases respectively.In another study by Gatei et al. [33], 94.5% were of the Squamous cell type.In a study by Wakhisi et al. [37] on 468 patients, Squamous cell carcinoma accounted for 90% of the cas- es.In another study by Nishimaki et al. [38] on 224 cases of carcinoma esopha-gus, 96.4% cases were of Squamous cell type.Thus, the present study correlates well with previous studies.
The lower 1/3 rd of the esophagus including the GE junction was the most common site (46%) followed by middle esophagus (40%).The upper 1/3 rd of esophagus was involved in 14% of cases.In a study by Wakhisi et al. [37]  esophagus.In another study by Subhasinge et al. [35] on 48 patients, 2.08%, 37.5%, 50% of the cases were seen in upper, middle and lower esophagus respectively and 10.42% of the cases were seen involving both the middle and lower esophagus.Thus, the present study correlates well with the previous studies done.
In the present study, regional lymphadenopathy was seen in 60% of the cases whereas non-regional lymphadenopathy was seen in 18% cases.Lymph nodes more than 1cm in size in short axis diameter were only considered to be significant.In a study by Nishimaki et al. [38] on 224 patients with esophageal carcinoma, 65.2% cases had regional lymph node involvement and 7.2% had non-regional lymph node metastases.In a study by Kim et al. [40], 13 out of 50 (26%) patients had non-regional lymph node metastases.In a study by Hsu et al.
[41] on 45 patients with esophageal carcinoma, regional lymph node involvement was seen in 46.7% cases and non-regional lymph node metastases was seen in 24.4% cases.Thus, the present study correlates well with the previous studies done.In the present study, most of the patients have esophageal wall thickness > 15 mm (78%), 22% of the patients have wall thickness between 5 -15 mm.In a study by Roedl et al. [42] on 36 patients with early malignant esophageal lesions, 52.8% cases had esophageal wall thickness between 15 -30 mm, 22.2% have thickness > 30 mm, and 25% have thickness < 15 mm.Thus, the present study correlates well with the previous study done.
The esophageal wall thickening or mass was eccentrically located in 58% of cases with at least minimal luminal narrowing seen in all the 50 Cases (100%).
In the present study, on CT scan, all the 3 cases of Adenocarcinoma were found in the lower esophagus, none of the Adenocarcinoma was seen in upper or middle esophagus.However, Squamous cell carcinoma was seen in all the parts of esophagus-upper (14%), middle (40%) and lower (40%).Among the Squamous cell carcinoma, local invasion or distant metastases was most commonly seen in poorly differentiated type (80%) followed by moderately differentiated type (28%).No local invasion/distant metastases was seen in well differentiated type.Local invasion or distant metastases were seen in 66.6% of the cases of Adenocarcinoma.The CT findings were found to have significant correlation with the esophagographic findings (p value >0.05 in each finding) with regard to luminal narrowing, proximal dilatation and hold up of contrast, eccentricity of growth, site involved, length of growth, involvement of pyriform sinuses/valeculla and involvement of GE junction.

Conclusions
CT plays a significant role in the evaluation of patients with esophageal carcinoma by providing important information to determine which patients with esophageal carcinoma may be suitable for surgical resection.CT study primarily helps to rule out unresectable or distant metastatic disease.
CT provided significant and valuable information regarding the esophageal wall thickness, site involved, eccentricity of the growth, the approximate length of the tumor, dilatation of the esophagus just proximal to the growth, esophageal luminal narrowing, peri-esophageal soft tissue or fat stranding, local invasion to Aorta, pericardium, tracheo-bronchial tree, pyriform sinuses/valeculla, and stomach.CT also provided detailed information about the significant lymphadenopathy pattern in patients with esophageal carcinoma including both the regional and the non-regional lymphadenopathy.The site of the primary tumours (upper, middle or lower third)were also considered in determining whether the significant lymph nodes were regional or non-regional.CT also guided in determining metastases to distant organs including Liver, Lungs, Bone, Adrenals, Kidneys, Spleen, Pancreas, Brain etc.
Esophagographic (Barium Swallow) findings strongly correlated with the CT findings including esophageal luminal narrowing, hold up of contrast and dilatation of the esophagus just proximal to the growth, eccentricity of the growth, site involved, length of the growth, involvement of GE junction and involvement of pyriform sinuses/valeculla.Other significant findings in esophagography included Shouldering sign, mucosal destruction/irregularity, gross type of growth (ulcerative, fungating, polypoidal, infiltrative), type of stricture (smooth or irregular).However, Barium studies cannot provide any information regarding local invasion into mediastinal structures, regional or non-regional lymphadenopathy or metastases to distant organs which are significant for determining the treatment modality.CT has an advantage over esophagography for these information.
All the cases of Adenocarcinoma were seen in lower 1/3 rd of esophagus.Squamous cell carcinoma was seen more commonly in middle and lower esophagus than upper esophagus.The degree of differentiation of Squamous cell carcinoma also showed significant correlation with the local invasion or distant metastases.These findings strongly suggest that there exists a significant correlation between CT findings and histopathology.
How to cite this paper: Agrawal, B. (2018) CT Findings in Patients with Esophageal Carcinoma and Its Correlation with Esophagographic Findings.Open Journal of Radiology, 8, 109-124.B. Agrawal DOI: 10.4236/ojrad.2018.82013110 Open Journal of Radiology tient in the standing position.Additional images were taken in supine and prone position whenever required and in patients who were too sick to undergo the procedure in standing position.All the patients who aspirated significant amount of contrast material and thus could not underwent further study were excluded from the study.Patients with slight or minimal aspiration of contrast who were able to undergo complete study were included in the study.Lateral and Antero-posterior views were taken as images including the whole length of esophagus up to the gastroesophageal junction.Additional oblique views were taken whenever required.

Figure 1 .
Figure 1.AP and lateral view esophagographic images showing concentric irregular abrupt luminal narrowing of mid esophagus with mucosal destruction giving Shouldering sign with hold up of contrast (HC) and dilatation of the proximal esophagus (PD).Axial and coronal CECT Thorax images showing concentric esophageal wall thickening, hold up of contrast (HC) and dilatation of proximal esophagus (PD) with maximum wall thickness of 23 mm, involving the middle thoracic esophagus with a periesophageal lymph node (PLN) measuring 21 mm in SAD.Metastases to lung and liver are also shown on Pulmonary window and axial CECT image of upper abdomen respectively.

Figure 2 .
Figure 2. AP and lateral view esophagographic images showing concentric irregular abrupt luminal narrowing of midthoracic esophagus with mucosal destruction giving Shouldering sign (S) with hold up of contrast (HC) and dilatation of the proximal esophagus (PD).Axial CECT Thorax images showing concentric esophageal wall thickening (arrow), with maximum wall thickness of 23 mm, involving the midthoracic esophagus with a periesophageal lymph node (PLN) measuring approx.13 mm in SAD.

Table 2 .
Correlation between CT findings and esophagographic findings was found significant (p value > 0.05) and Table3describes this correlation and significance in relation to each finding.

Table 1 .
Histopathological correlation with ct findings.

Table 3 .
Correlation of ct findings with esophagograhic findings.