Clin Endosc.  2021 Jul;54(4):464-476. 10.5946/ce.2021.186.

Current Status of Image-Enhanced Endoscopy for Early Identification of Esophageal Neoplasms

• Kim SH
• Hong SJ

• KMID: 2518848
• DOI: http://doi.org/10.5946/ce.2021.186

Abstract

Advanced esophageal cancer is known to have a poor prognosis. The early detection of esophageal neoplasms, including esophageal dysplasia and early esophageal cancer, is highly important for the accurate treatment of the disease. However, esophageal dysplasia and early esophageal cancer are usually subtle and can be easily missed. In addition to the early detection, proper pretreatment evaluation of the depth of invasion of esophageal cancer is very important for curative treatment. The progression of non-invasive diagnosis via image-enhanced endoscopy techniques has been shown to aid the early detection and estimate the depth of invasion of early esophageal cancer and, as a result, may provide additional opportunities for curative treatment. Here, we review the advancement of image-enhanced endoscopy-related technologies and their role in the early identification of esophageal neoplasms.

Keyword

Diagnostic imaging; Early detection of cancer; Esophageal neoplasms; Narrow-band imaging

Figure

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  Fig. 1. Pink-color sign. (A, B) The pink-color discoloration within the Lugol-voiding area was observed 2–3 min after staining (arrow).

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  Fig. 2. (A) White light image endoscopy (WLE) shows flat reddish mucosal lesions; however, it is difficult to define the margin of the abnormal mucosa. (B) The tumor margin is more distinct from the background mucosa under narrow-band imaging (NBI) without magnification (white dotted line). This lesion is diagnosed as highgrade intraepithelial neoplasia after endoscopic submucosa dissection. (C) WLE shows a flat reddish mucosal lesion, and it is more delineated than (A); however, it is difficult to define the distal margin. (D) NBI showed the distal margin more definitely than WLE (white arrows). This lesion is diagnosed as squamous cell carcinoma after biopsy. (E) Intrapapillary capillary loop (IPCL) shows red dots under WLE with magnification. (F) IPCL shows brown dots under NBI with magnification (ME-NBI) and the morphological features are more clearly observed under ME-NBI. The caliber of IPCL is prominently increased and the loop-like formation is reserved (IPCL type IV).

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  Fig. 3. Various morphologic features of intrapapillary capillary loop (IPCL) in squamous cell neoplasms under narrow-band imaging with magnification. (A) In normal mucosa: thin and regular patterns of IPCL can be observed. (B) The caliber and the density of IPCL is slightly increased and the length of IPCL is also elongated. This lesion was histologically diagnosed as low-grade intraepithelial dysplasia of the esophagus. (C-1) The caliber of the IPCL is prominently increased, and the loop-like formation is reserved. (C-2) The density is prominently increased compared to the background mucosa, and it appears as a brownish island (formation of area). This lesion was histologically diagnosed as a high-grade intraepithelial dysplasia of the esophagus. (D) The caliber of the IPCL is increased irregularly and the arrangement is irregular. This lesion was histologically diagnosed as esophageal high-grade intraepithelial dysplasia with focal squamous cell carcinoma of focally invaded the muscularis mucosae. (E) Tortuous, irregular IPCL was observed, and the arrangement was irregular. The loop-like formation was destroyed. This lesion was histologically diagnosed as esophageal squamous cell carcinoma with focal invasion of the submucosa at a depth of 200 μm. (F) Highly dilated multiple layered, irregularly branched, and reticular vessels were observed. This indicates a massively invasive submucosal carcinoma.

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  Fig. 4. Intrapapillary capillary loop patterns undergo stepwise morphologic changes of “dilation”, “tortuosity”, “change in caliber” and “various shapes” with the progression of esophageal squamous cell neoplasm.

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  Fig. 5. Classification systems for esophageal squamous cell neoplasm with magnifying narrow-band imaging. (A) Inoue classification [45-47]. Type I IPCL pattern is observed in the normal esophageal mucosa. The elongation and dilation of capillaries are observed in the Type II IPCL. This pattern may indicate esophagitis or reactive changes. Type III IPCL pattern is observed in the “borderline lesions between benign and malignant tumors. Increased vessel caliber and elongation of the IPCL toward the epithelial surface are two important factors in Type IV IPCL pattern. This pattern is observed in a borderline lesion to definite carcinoma. Type V IPCL pattern is divided into four subtypes. Type V1 pattern corresponds to carcinoma in situ (M1) with four characteristic morphological changes: dilation, tortuosity, irregular caliber, and non-uniformity between each IPCL. Type V2 pattern corresponds to the invasion of the lamina propria mucosae (M2) and adds to the features of Type V1 with an elongation of the vessel in the vertical plane. In Type V3, the abnormal vessel spreads in a horizontal plane or extends toward the deeper mucosal layer while losing its loop arrangement. It corresponds to cancer invasion reaching the muscularis mucosa or even to the submucosa. In Type VN pattern, the vessel diameter is approximately three times that of Type V3. This corresponds to a massively invasive submucosal carcinoma. Since there is an extremely low risk of lymph node (LN) metastasis, superficial esophageal squamous cell carcinoma limited to the epithelium or the lamina propria mucosae is absolutely indicated for endoscopic treatment. Endoscopic treatment is indicated for a tumor invading the muscularis mucosa or the submucosa to a depth of 200 μm or less from the muscularis mucosae because the rate of LN metastasis is 10%–15%. Tumors invading the submucosa to a depth of more than 200 μm should be treated with surgery or definitive chemoradiotherapy because the rate of LN metastasis is 30%–50%. (B) Arima classification [48]. (a) Schematic drawing of microvascular patterns of superficial esophageal lesions. Type 1. Thin, linear capillaries in the subepithelial papilla are observed. This is similar to the normal mucosa. Type 2. Distended and dilated vessels with variations are observed. The structure of capillaries in the subepithelial papilla is preserved and shows a relatively regular arrangement. It is usually observed in inflammatory lesions. Type 3. Irregular arrangement of destructed vessels in the subepithelial papilla, spiral vessels with an irregular caliber, and crushed vessels are observed. It can be observed in m1 or m2 cancers. Type 4. Irregularly multilayered, irregularly branched, and reticular vessels are observed. Multilayered type 4 vessels appear in tumors with deep m2 invasion. (b) Schematic drawing of subtypes of type 4 vessels. (C) JES classification for narrow-band imaging with magnifying endoscopy [51]. EP, epithelium; HGIN, high-grade intraepithelial neoplasia; IPCL, intrapapillary capillary loop; JES, Japan Esophageal Society; LGIN, low-grade intraepithelial neoplasia; LPM lamina propria mucosae; MM, muscularis mucosae; SCC, squamous cell carinoma; SM, submucosa.

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  Fig. 6. Blue laser image (BLI) and linked color image (LCI) of esophageal squamous cell carcinoma. (A) A flat reddish lesion was observed under white-light endoscopy. (B) The lesion was observed to be of purple color with LCI. (C) The lesion was observed with brown color with BLI. (D) Intrapapillary capillary loops were observed under BLI with magnification and it is similar with narrow-band image with magnification.

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