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World J Gastroenterol. Feb 7, 2020; 26(5): 466-477
Published online Feb 7, 2020. doi: 10.3748/wjg.v26.i5.466
Endoscopic Kyoto classification of Helicobacter pylori infection and gastric cancer risk diagnosis
Osamu Toyoshima, Toshihiro Nishizawa, Department of Gastroenterology, Toyoshima Endoscopy Clinic, Tokyo 157-0066, Japan
Osamu Toyoshima, Kazuhiko Koike, Department of Gastroenterology, Graduate School of Medicine, The University of Tokyo, Tokyo 113-8655, Japan
Toshihiro Nishizawa, Department of Gastroenterology and Hepatology, International University of Health and Welfare, Mita Hospital, Tokyo 108-8329, Japan
ORCID number: Osamu Toyoshima (0000-0002-6953-6079); Toshihiro Nishizawa (0000-0003-4876-3384); Kazuhiko Koike (0000-0002-9739-9243).
Author contributions: Toyoshima O reviewed the literature and wrote the article; Nishizawa T revised and edited the article; Koike K revised and approved the final article.
Conflict-of-interest statement: Authors declare no conflict of interests for this article.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Corresponding author: Osamu Toyoshima, MD, Director, Doctor, Department of Gastroenterology, Toyoshima Endoscopy Clinic, 6-17-5 Seijo, Setagaya-ku, Tokyo 157-0066, Japan. t@ichou.com
Received: December 30, 2019
Peer-review started: December 30, 2019
First decision: January 11, 2020
Revised: January 15, 2020
Accepted: January 19, 2020
Article in press: January 19, 2020
Published online: February 7, 2020
Processing time: 38 Days and 23.8 Hours

Abstract

Recent advances in endoscopic technology allow detailed observation of the gastric mucosa. Today, endoscopy is used in the diagnosis of gastritis to determine the presence/absence of Helicobacter pylori (H. pylori) infection and evaluate gastric cancer risk. In 2013, the Japan Gastroenterological Endoscopy Society advocated the Kyoto classification, a new grading system for endoscopic gastritis. The Kyoto classification organized endoscopic findings related to H. pylori infection. The Kyoto classification score is the sum of scores for five endoscopic findings (atrophy, intestinal metaplasia, enlarged folds, nodularity, and diffuse redness with or without regular arrangement of collecting venules) and ranges from 0 to 8. Atrophy, intestinal metaplasia, enlarged folds, and nodularity contribute to gastric cancer risk. Diffuse redness and regular arrangement of collecting venules are related to H. pylori infection status. In subjects without a history of H. pylori eradication, the infection rates in those with Kyoto scores of 0, 1, and ≥ 2 were 1.5%, 45%, and 82%, respectively. A Kyoto classification score of 0 indicates no H. pylori infection. A Kyoto classification score of 2 or more indicates H. pylori infection. Kyoto classification scores of patients with and without gastric cancer were 4.8 and 3.8, respectively. A Kyoto classification score of 4 or more might indicate gastric cancer risk.

Key Words: Gastric cancer; Helicobacter pylori; Endoscopy; Kyoto classification; Atrophy; Intestinal metaplasia; Enlarged fold; Nodularity; Diffuse redness; Regular arrangement of collecting venules

Core tip: The Kyoto classification organizes endoscopic findings based on Helicobacter pylori (H. pylori) infection. The score of the Kyoto classification is the sum of scores of five endoscopic findings (atrophy, intestinal metaplasia, enlarged folds, nodularity, and diffuse redness with or without regular arrangement of collecting venules) and ranges from 0 to 8. A high score is believed to reflect a higher risk of current H. pylori infection and gastric cancer. A Kyoto classification score of 0 indicates no H. pylori infection. A Kyoto classification score of ≥ 2 indicates current H. pylori infection. A Kyoto classification score of ≥ 4 might indicate gastric cancer risk.
INTRODUCTION

Gastric cancer is the third most common cancer in the world and is the cancer with the third greatest number of mortalities. If gastric cancer is detected at an early stage, it can be cured via endoscopic submucosal dissection[1,2]. Although periodic endoscopic examination is important for detecting early gastric cancer, efficient surveillance requires identification of high-risk populations[3-7]. The genetic risks of gastric cancer have been reported to include hereditary cancer syndrome, single nucleotide polymorphisms, and family history[8-12]. Environmental risks include Helicobacter pylori infection, smoking, excessive salt consumption, and lack of vegetable. Among them, the association between H. pylori infection and the development of gastric cancer is well established, and H. pylori virulence factors (cagA, vacA, iceA, and dupA) are known[13-16]. The International Agency for Research on Cancer categorized H. pylori infection as a type I carcinogen and it is considered the primary cause of gastric cancer. On the other hand, H. pylori eradication reduces gastric cancer risk[17-20]. Therefore, the accurate assessment of H. pylori infection status is important. Nowadays, endoscopic examination is required to diagnose H. pylori infection status. In 2013, the Japan Gastroenterological Endoscopy Society advocated the Kyoto classification, a new grading system for endoscopic gastritis. In this review, we focus on up-to-date reports regarding the Kyoto classification to help improve endoscopic practice.

DEFINITION OF KYOTO CLASSIFICATION OF GASTRITIS

Thanks to advances in endoscopic technology, it is now possible to observe the gastric mucosa in minute detail. Today, endoscopy is used in the diagnosis of gastritis to determine the presence/absence of H. pylori infection and evaluate the risks of gastric cancer. The Kyoto classification of endoscopic findings was advocated when the 85th Congress of the Japan Gastroenterological Endoscopy Society was held in Kyoto in 2013. The purpose of the Kyoto classification was to evaluate the gastric mucosa, as this presents a potential risk of developing gastric cancer[21,22]. In this classification, 19 endoscopic findings related to gastritis, including atrophy, intestinal metaplasia, enlarged folds (tortuous folds), nodularity, diffuse redness, regular arrangement of collecting venules (RAC), map-like redness, foveolar-hyperplastic polyp, xanthoma, mucosal swelling, patchy redness, depressed erosion, sticky mucus, hematin, red streak, spotty redness, multiple white and flat elevated lesions, fundic gland polyp, and raised erosion, are characterized. Among them, atrophy, intestinal metaplasia, enlarged folds, and nodularity, which may be related to gastric cancer risk, and diffuse redness with or without RAC, which is related to H. pylori infection status, are accounted for in the Kyoto classification score (Table 1)[22].

Table 1 Kyoto classification score.
Kyoto classificationScore
Atrophy
  None, C10
  C2 and C31
  O1-O32
Intestinal metaplasia
  None0
  Antrum1
  Corpus and antrum2
Enlarged folds
  Absence0
  Presence1
Nodularity
  Absence0
  Presence1
Diffuse redness
  None0
  Mild (with RAC)1
  Severe2
Kyoto score0-8
RAC: Regular arrangement of collecting venules.
Endoscopic atrophy (Kimura-Takemoto classification)

Atrophy includes “pathological” atrophy and “endoscopic” atrophy. Atrophy is pathologically defined as a loss of glandular tissue[23]. The Kyoto classification adopted Kimura-Takemoto classification of endoscopic atrophy[24]. Kimura et al[24] defined a visible capillary network, low niveau, and yellowish pale in color as atrophic features, while diffuse redness with high mucosal height as characteristics of non-atrophy. We show endoscopic images and a schematic diagram in Figure 1. “Endoscopic” atrophy has been reported to correlate well with “pathological” atrophy[25-29]. In the Kyoto classification score, non-atrophy (C0) and C1 were scored as Atrophy score 0, C2 and C3 as Atrophy score 1, and O1 to O3 as Atrophy score 2.

Figure 1
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Figure 1 Kimura-Takemoto classification of endoscopic atrophy. Atrophic borders are indicated by a dotted line. A: C1 (Atrophy is limited to the antrum); B: C2 (Atrophy is limited to the minor area of the lesser curvature of the body); C: C3 (Atrophy exists in the major area of the lesser curvature of the body but does not extend beyond the cardia); D: O1 (Atrophy extends to the fundus over the cardia. Atrophic border of the body lies between the lesser curvature and anterior wall); E: O2 (Atrophic border of the body lies on the anterior wall); F: O3 (Atrophy is widespread with the border between the anterior wall and greater curvature).
Endoscopic intestinal metaplasia

Intestinal metaplasia typically appears grayish-white and slightly elevated plaques surrounded by mixed patchy pink and pale areas of mucosa, forming an irregular uneven surface (Figure 2A). A villous appearance, whitish mucosa, and rough mucosal surface are useful indicators for endoscopic diagnosis of intestinal metaplasia[30]. Image-enhanced endoscopy, including narrow-band imaging (NBI), blue laser imaging, and linked color imaging, has improved the visibility of endoscopic findings and accuracy of endoscopic diagnosis of intestinal metaplasia[31-39]. A white opaque substance on the surface epithelium and light blue crest on the mucosal epithelial rim visualized using magnified NBI are associated with intestinal metaplasia[40-42].

Figure 2
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Figure 2 Endoscopic findings of Kyoto classification. A: Intestinal metaplasia; B: Map-like redness; C: Enlarged folds; D: Nodularity; E: Diffuse redness; F: Regular arrangement of collecting venules in weakly magnified image.

In the Kyoto classification score, the absence of intestinal metaplasia was scored as Intestinal metaplasia score 0, the presence of intestinal metaplasia within the antrum as Intestinal metaplasia score 1, and intestinal metaplasia extending into the corpus as Intestinal metaplasia score 2. The Intestinal metaplasia score is diagnosed by using white light imaging. Intestinal metaplasia diagnosis based on image-enhanced endoscopy using NBI, blue laser imaging, linked color imaging, and chromo-endoscopy is not included in the Kyoto score.

Map-like redness (synonymous with mottled patchy erythema) is defined as multiple flat or slightly depressed erythematous lesions that have various shapes, sizes, and red densities (Figure 2B)[6,43]. When using biopsy specimens of map-like redness, intestinal metaplasia is frequently observed (87.3%)[43]. The mechanism of the appearance of map-like redness is thought to be strengthening of the contrast between non-atrophic mucosa and atrophic mucosa after diffuse redness has disappeared following successful eradication[21]. Map-like redness is not always found following eradication. However, when it is observed, there is virtually no doubt that it is indicative of post-eradication gastric mucosa[22].

Enlarged folds

An enlarged fold is defined as a fold with a width of 5 mm or more that is not flattened or is only partially flattened by insufflation of the stomach (Figure 2C). Rugal hyperplasia is a synonym for enlarged folds.

In the Kyoto classification score, the absence and presence of enlarged folds was scored as Enlarged folds score 0 and 1, respectively.

Nodularity

Nodular gastritis is characterized by a miliary pattern resembling “goose flesh” mainly located in the antrum (Figure 2D). Nodularity can be more clearly seen following the use of indigo carmine spray. Lymphoid follicles and/or intense inflammatory cell infiltration are observed in biopsy specimens of nodularity[44]. Nodular gastritis displays a female predominance and improves gradually with age. A high serum H. pylori antibody titer is correlated to nodularity[45-49].

In the Kyoto classification score, the absence and presence of nodularity was scored as Nodularity score 0 and 1, respectively.

Diffuse redness

Diffuse redness refers to uniform redness with continuous expansion observed in non-atrophic mucosa mainly in the corpus (Figure 2E) and is typical of endoscopic superficial gastritis[22,24]. Congestion and dilation of the subepithelial capillary network in the gastric mucosa with inflammatory change of the mucosal surface color to red[50]. Since the assessment of the severity of diffuse redness is affected by the setting of the endoscope and monitor, objective assessment may be difficult.

On the other hand, RAC is a condition in which the collecting venules are arranged in the corpus. From a distance, it appears like numerous dots. From up close, it has the appearance of a regular pattern of starfish-like shapes (Figure 2F).

In the Kyoto classification score, the absence of diffuse redness was scored as Diffuse redness score 0, mild diffuse redness or diffuse redness with RAC as Diffuse redness score 1, and severe diffuse redness or diffuse redness without RAC as Diffuse redness score 2.

Kyoto classification score

The Kyoto classification score for gastritis is based on the sum of scores of the five endoscopic findings and ranges from 0 to 8 (Table 1). A high score is believed to reflect increased risk of H. pylori infection and gastric cancer. In a study that evaluated the usefulness and convenience of the Kyoto classification, a mini-lecture improved the accuracy of endoscopic diagnosis[51].

DIAGNOSIS OF HELICOBACTER PYLORI INFECTION BY ENDOSCOPIC FINDINGS

There are several reports to investigate the relationship between endoscopic findings and H. pylori infection[52-56]. Table 2 shows the diagnostic values of the Kyoto classification for H. pylori infection[57-62]. Enlarged folds had a relatively good positive predictive value (56.2–86.0%). Although nodularity had a low sensitivity (6.4%–32.1%) for H. pylori infection, it had excellent specificity for a current infection (95.8%–98.8%). Diffuse redness had a good positive predictive value (65.6%–91.5%). RAC had a high sensitivity for non-infection (86.7%–100%).

Table 2 Diagnostic value of Kyoto classification for Helicobacter pylori infection.
Endoscopic findingsRef.YearNo. of subjectsSensitivitySpecificityPPVNPV
Diagnosis for current H. pylori infection
Enlarged foldsKato et al[59]201327558.579.576.962.2
Enlarged foldsMao et al[60]201625660.292.386.074.6
Enlarged foldsYoshii et al[61]201949823.196.656.287.0
NodularityLaine et al[57]19955232.195.890.054.8
NodularityKato et al[59]20132755.398.875.059.4
NodularityYoshii et al[61]20194986.498.341.784.9
Diffuse rednessKato et al[59]201327583.466.973.878.4
Diffuse rednessMao et al[60]201625657.595.891.574.7
Diffuse rednessYoshii et al[61]201949860.094.765.693.3
Diagnosis for negative H. pylori infection
RACYagi et al[58]200255791.197.995.096.2
RACKato et al[59]201327593.648.087.066.8
RACMao et al[60]201625686.790.287.589.6
RACGarcés-Durán et al[62]2019140100.049.047.3100.0
PPV: Positive predictive value; NPV: Negative predictive value; RAC: Regular arrangement of collecting venules; H. pylori: Helicobacter pylori.

Yoshii et al[61] reported that endoscopic atrophy has a specificity of 75.5% for the diagnosis of past H. pylori infection. Furthermore, intestinal metaplasia and map-like redness also have a higher specificity (92.6% and 98.0%, respectively) for the diagnosis of past H. pylori infection.

Diagnosis of H. pylori infection based on Kyoto classification score

Several studies investigated the relationship between the total Kyoto classification score and H. pylori infection. We reported an association between total Kyoto classification score and serum H. pylori antibody titer[48]. Kyoto scores were 0.1, 0.4, 1.9, and 2.3 for negative-low, negative-high, positive-low, and positive-high titers of H. pylori antibody, respectively. Kyoto scores increased in line with the H. pylori antibody titer. In subjects with a negative-high H. pylori antibody titer, the Kyoto classification had an excellent area under the receiver operating characteristics curve (0.886) for predicting H. pylori infection with a cutoff value of 2. A Kyoto score of ≥ 2 could predict H. pylori infection with an accuracy of 90%[63]. In 870 subjects with no history of H. pylori eradication therapy, H. pylori infection rates in those with Kyoto classification scores of 0, 1, and ≥ 2 were 1.5%, 45%, and 82%, respectively[64].

High Kyoto scores do not always correspond to an active H. pylori infection. False diagnosis can occur due to either a spontaneous negative conversion or an unintentional eradication. In cases of spontaneous negative conversion, the harsh environment of the intestinal metaplasia removes the H. pylori infection spontaneously. In cases of unintentional eradication, the H. pylori infection is eradicated after the treatment of other infectious diseases with antibiotics.

Essentially, a Kyoto classification score of ≥ 2 indicates H. pylori infection. On the other hand, a Kyoto classification score of 0 indicates no H. pylori infection.

GASTRIC CANCER RISK ASSESSED BASED ON ENDOSCOPIC FINDINGS OF KYOTO CLASSIFICATION

There are several reports of gastric cancer risk assessed based on endoscopic findings[65-69]. Three Japanese cohort studies revealed the association of endoscopic atrophy with gastric cancer incidence (Table 3). They showed that the gastric cancer incidence of mild, moderate, and severe atrophy is 0.04%–0.10%/year, 0.12%–0.34%/year, and 0.31%–1.60%/year, respectively[70-72]. Shichijo et al[71] reported that cancer incidence was extremely high, affecting 16.0% of patients with severe atrophy over 10-year periods. Gastric cancer risk increases according to the extent of the gastric atrophy.

Table 3 Gastric cancer incidence according to endoscopic atrophy.
Ref.PopulationNo. of subjectsNo. of cancersDuration, yrGastric cancer incidence, %/yr
MildModerateSevere
Take et al[70], 2011Post eradication with peptic ulcer1674285.60.040.280.62
Shichijo et al[71], 2016Post eradication573216.20.0710.3411.601
Kaji et al[72], 2019Medical examination12941633.70.100.160.31
Post eradication2571203.70.060.120.42
1Incidence was calculated by dividing the incidence per 10 years by 10.

Table 4 shows the odds ratio of gastric cancer depending on the presence or absence of the endoscopic findings of the Kyoto classification[49,73-75]. Gastric atrophy (open-type) was associated with gastric cancer with an odds ratio of 7.2–14.2[76,77].

Table 4 Odds ratios of endoscopic findings for gastric cancer.
Endoscopic findingsRef.PopulationNo. of subjectsOdds ratio
AtrophyMasuyama et al[76], 2015Without eradication2777714.21
AtrophySekikawa et al[77], 2016Screening18237.21
Intestinal metaplasiaSugimoto et al[74], 2017Endoscopic gastritis12005.0
Enlarged foldsNishibayashi et al[73], 2003H. pylori positive2765.0
NodularityNishikawa et al[49], 2018H. pylori positive67413.9
RACMajima et al[75], 2019Post eradication1940.4
1Odds ratio for open-type atrophy calculated with closed-type atrophy as a reference. RAC: Regular arrangement of collecting venules; H. pylori: Helicobacter pylori.

Sugimoto et al[74] have reported that endoscopic intestinal metaplasia was associated with early gastric cancer with an odds ratio of 5.0. Intestinal metaplasia is reported to be associated with intestinal-type cancer[78].

A cross-sectional study reported an odds ratio of 5.0 for enlarged folds of 5 mm or more for gastric cancer patient with H. pylori-infected controls as a reference[73]. It also indicated an upward shift in the distribution of gastric fold widths in H. pylori-positive patients with gastric cancer to an odds ratio of 35.5 in those with a fold width of 7 mm. Inflammation-induced DNA methylation of various genes is involved in the development of gastric cancer in gastritis with enlarged folds[50,73,79-85]. Enlarged folds are reported to be associated with diffuse-type gastric cancer[73,86].

Nishikawa et al[49] reported an odds ratio of 13.9 for gastric cancer in H. pylori-positive patients with nodularity. In a study involving H. pylori-positive patients under the age of 29, nodularity provided an odds ratio of 64.2 for gastric cancer. Nodularity is reported to be associated with diffuse-type cancer[49,87].

RAC was reported to be negatively associated with gastric cancer (odds ratio: 0.4)[75].

Gastric cancer risk assessed using the Kyoto classification score

Sugimoto et al[74] presented the relationship between total Kyoto classification score and gastric cancer risk. In their cross-sectional study, the total Kyoto classifications scores of patients with and without gastric cancer were 4.8 and 3.8, respectively. This study suggests that a Kyoto classification score of ≥ 4 might indicate gastric cancer risk.

CONCLUSION

The Kyoto classification organized endoscopic findings related to H. pylori infection. A Kyoto classification score ≥ 2 indicates H. pylori infection. An H. pylori test is essential for such cases with no history of H. pylori eradication.

A Kyoto classification score ≥ 4 might indicate gastric cancer risk. Such cases need careful follow-up. However, research related to the Kyoto score is still scarce and further study is needed.

Footnotes

Manuscript source: Invited manuscript

Corresponding Author's Membership in Professional Societies: Japan Gastroenterological Endoscopy Society, No. 36450775; The Japanese Society of Gastroenterology, No. 037068; The Japanese Society of Internal Medicine, No. 24993; European Society of Gastrointestinal Endoscopy, No. 11413; American Society for Gastrointestinal Endoscopy, No. 154418; Japan Surgical Society, No. 0416990; The Japanese Society for Helicobacter Research, No. 773815.

Specialty type: Gastroenterology and Hepatology

Country of origin: Japan

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