Journal of Pathology and Translational Medicine

Original Articles

Gastric Lymphoid Follicles in Helicobacter Pylori Infection: Frequency, Distribution and Relationship to Inflammation in 331 Gastric Biopsy Material.: Kyoung Mee Kim, Anhi Lee, Sang In Shim, Hyun Suk Chae; Korean J Pathol. 1995;29(4):442-449.

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Abstract PDF: Helicobacter pylori(H. pylori) infection is considered the most important cause of chronic active gastritis and peptic ulcer. To determine the prevalence, distribution and it's relationship to degree of inflammation, gastric biopsy specimens were obtained from 331 nonulcer dyspepsia(NUD) patients consisting of 52 H. pylori negative normal volunteers and 279 H. pylori infected patients. Lymphoid follicles, degree of acute and chronic inflammation(Grade 0 to 3), and degree of H. pylori(Grade 0 to 4) were observed. The prevalence of H. pylori in NUD was 84.29%. The lymphoid follicles were found in 138 patients(41.7%) and only 5 patients(l.5%) without H. pylori showed lymphoid follicles. There was strong a relationship between lymphoid follicles and degree of acute and chronic inflammation and intensity of H. pylori infection(P<0.001). Acute and chronic inflammation were more serious in the antrum than body in H. pylori infected patients. There was no relationship between lymphoid follicles and the site in the stomach of H. pylori infection(P<0.078), but the body portion had an increased frequency of lymphoid follicles compared to the in antrum. Our results indicate that the prevalence of H. pylori infection in Korea is higher than in Western people and the degree of acute and chronic inflammation are strongly correlated with the presence of lymphoid follicles. The lymphoid follicles are believed to be absent from the normal stomach and their presence is strongly associated with H. pylori infection. The fact there is an that increased frequency of lymphoid follicles in H. pylori infected patients, and that they are more prevalent in the body of the antrum, support the concept that H. pylori may be a precursor in the development of primary gastric lymphoma.

Helicobacter pylori Infection and Histopathological Features of Gastric Mucosa.: Gyung Hyuck Ko, Cheol Keun Park, Chun Sik Choi, Heung Bae Park, Jeong Hee Lee, Hye Jung Lee, Hyun Ju Kim, Kwang Ho Rhee; Korean J Pathol. 1996;30(3):199-209.

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Abstract PDF: A microscopic examination of 1,000 cases of gastroscopic biopsy specimens revealed that the prevalence and severity of chronic gastritis, neutrophilic infiltration, and Helicobacter pylori infection increased with advancing age until the age reached about 40, but they decreased thereafter in accordance with the increasing prevalence of intestinal metaplasia. The prevalence and severity of Helicobacter pylori infection, chronic gastritis, and neutrophilic infiltration were proportionately related to each other and to gastric peptic ulcer, but inversely related with intestinal metaplasia and gastric carcinoma. The results suggested that chronic gastritis and gastric peptic ulcer may be associated with Helicobacter pylori infection and that if these lesions persist, intestinal metaplasia may develop with decreased severity of chronic gastritis and Helicobacter pylori infection but, instead, increase of the risk of gastric carcinoma. And it is thought that the cause of the high incidence of gastric carcinoma in Korea may be related to the fact that chronic gastritis and Helicobacter pylori infection develop earlier in life and therefore the prevalence of intestinal metaplasia is higher in Korea than in other countries.

Histopathologic Analysis of Helicobacter Pylori Associated Gastritis.: Ho Jung Lee, Eun Sil Yu, In Chul Lee; Korean J Pathol. 1996;30(9):764-774.

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Abstract PDF: Gastric mucosa shows continuous changes in surface epithelium as well as inflammatory reaction by various substances from the outside and their metabolic products. Gastric mucosal lesions are proven to be associated with bacterial infection by the discovery of Heliobacter pylori(H. pylori) and many studies about histopathologic changes of gastric mucosa associated H. pylori infection has been advanced. It is known that H. pylori associated gastritis displays surface foveolar epithelial changes, such as cytoplasmic vacuolation, mucin loss, juxtaluminal cytoplasm erosion, epithelial denudation, and mucosal irregularity. There have been many studies that H. pylori infection is associated with intestinal metaplasia, gastric dysplasia, and carcinoma. Also chronic H. pylori infection with its induction of gastric lymphoid follicle has been implicated as a precursor of gastric lymphoma of the unique B-cell type that arises from mucosa-associated lymphoid tissue(MALT). However, these gastric mucosal changes are also observed in gastritis with other causes. In this study, we aimed to define specific histopathiologic findings associated with H. pylori infection. A total of 463 gastric biopsy specimens were reviewed. They were Helicobacter-associated gastritis and were divided as many (MH), a few (AH), and no (NH), according to the number of H. pylori. 210 (MH), 131 (AH), and 122 (NH) biopsy specimens were included. Lymphocytes, plasma cells in lamina propria, eosinophils and neutrophils in surface epithelium and crypt as well as lamina propria were graded from 0 to 3. Surface epithelial changes including cytoplasmic vacuolation, mucin loss, juxtaluminal erosion, epithelial denudation and mucosal irregrarity were observed in 200 of 210 cases(95%) in MH group, 34 of 131 cases(26%) in AH group, and 6 of 122 cases(5%) in NH group. This result indicates there is significant difference in surface epithelial changes according to the number of H. pylori(p<0.001). Severity of eosinophil, neutrophil, lymphocyte, and plasma cell infiltration is increased in proportion to the number of H. pylori. Especially, neutrophilic infiltration is not identified in 95 of 122 cases(78%) in NH group, whereas MH group shows severe infitration (grade 3) in 127 of 210 cases(61%), and no (grade 0) in 11 of 210 cases(5%). This data well explains that the severity of neutrophil infiltration is associated with, the degree of H. pylori infection in chronic active gastritis, with statistical significance. The prevalence of lymphoid follicle formation was 17 of 120 cases(14%) in NH group, 24 of 131 cases(18%) in AH group, and 52 of 210 cases(25%) in MH group. This shows that lymphoid follicle formation correlates with the number of H. pylori, but without statistical significance. The prevalence of intestinal metaplasia in NH, AH, and MH was 43 of 122 cases(35%), 46 of 131 cases(35%), and 69 of 210 cases(33%), showing no association between intestinal metaplasia and H. pylori. In summary, H. pylori associated gastritis dispays characteristic histopathological changes in gastric mucosa, in which surface epithelial changes and various inflammatory infiltrates are increased in proportion to the number of H. pylori. Especially vacuolization of surface foveolar epithelium, cryptitis, and crypt abscess are specific findings of H. pylori associated gastritis.

Prevalence of Lymphoid Follicles in Helicobacter Pylori Associated Peptic Ulcer and Non-ulcer Dyspepsia in Human Stomach.: Tae Jung Jang, Jung Ran Kim; Korean J Pathol. 1996;30(12):1083-1090.

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Abstract PDF: To determine the prevalence of lymphoid follicles in Helicobacter pylori(H. pylori) positive and negative gastritis and its relationship to age, biopsy site, gastritis activity, degree of gastritis, number of H. pylori and gastritis score in H. pylori associated gastritis, we examined the gastric tissue of patients with 121 nonulcer dyspepsia and 99 peptic ulcers. The gastritis score was obtained by adding together the figures for gastritis degree, gastritis activity and number of H. pylori. H. pylori was detected in 75.2% of nonulcer dyspepsia, 84.5% of gastric ulcers and 90.3% of duodenal ulcers. Lymphoid follicles were found in 63.3% of H. pylori associated gastritis and 4.7% of H. pylori negative gastritis, and there was a strong relationship between the prevalence of lymphoid follicles and H. pylori infection(P<0.01). Lymphoid follicles were found in 100% of H. pylori associated gastritis, showing severe chronic inflammatory cell infiltration, and strong relationship between the prevalene of lymphoid follicles and the degree of gastritis (P<0.01). There was no significant difference among lymphoid follicles, age, biopsy site, clinical diagnosis, gastritis activity and number of H. pylori. Lymphoid follicles were found in 58.3% of gastritis score 4, 67.6% of gastritis score 7 and 100% of gastritis score 9, and there was significant correlation between the prevalence of lymphoid follicles and a gastritis score(P<0.01, R=0.85). In summary, gastric lymphoid follicle is significantly associated with H. pylori infection and its presence in H. pylori associated gastritis is related to chronic inflammatory cell infiltration.

Correlation between Helicobacter pylori Infection and Lymphoid Follicle Formation in Gastrectomy Specimens.: Won Ae Lee, Hye Sung Hahn, Woo Ho Kim, Yong Il Kim; Korean J Pathol. 1998;32(3):162-168.

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Abstract PDF: Histopathologic studies for Helicobacter pylori (H. pylori)-associated chronic gastritis have been mostly undertaken with endoscopic biopsy specimens, often leading to an inappropriate evaluation of the gastric mucosal alterations. The purpose of this paper was designed to investigate the actual prevalence of lymphoid follicle formation by H. pylori infection using the resected stomachs. A total of 16 fresh gastrectomy specimens bearing gastric carcinoma were examined under the quick and gentle procedure, with which H. pylori was detected in 12 cases (75%) and lymphoid follicles in 14 cases (87.5%), while the detection rate of H. pylori remained 56.3% in the control group which comprised the same 16 resected stomachs and were examined by routine tissue preparation procedure without any special care. There was a significant correlation between the presence of H. pylori and lymphoid follicle formation (p=0.05), but no correlation was found between the grades of H. pylori and lymphoid follicles. The topographical distribution of H. pylori or lymphoid follicles in antrum and body gave no statistical difference. Similarly, there was no correlation between H. pylori infection and intestinal metaplasia, activity of chronic gastritis or histologic types of accompanying adenocarcinoma. We conclude that studies of the gastric mucosal change by H. pylori infection using the gastrectomy specimens provide a useful information for analysis of lymphoid follicle formation which is a consistent morphological characteristic of H. pylori infection.

Histopathologic Analysis of Helicobacter pylori-associated Chronic Gastritis between cagA-positive and cagA-negative Strains.: Hun Kyung Lee, Gyeong Hoon Kang, Hwoon Yong Jung, On Ja Kim; Korean J Pathol. 1998;32(7):504-510.

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Abstract: Infection with Helicobacter pylori (H. pylori) leads to gastritis, but the majority of infected persons are asymptomatic, and it has been recently described that the ability of H. pylori to cause more severe disease is related to the presence of the cytotoxin-associated gene A (cagA). We investigated the prevalence of cagA-bearing strains in a group of H. pylori-positive gastritis, and compared the morphologic differences between cagA-positive and cagA-negative cases on H&E stained slides. Polymerase chain reaction (PCR) assays for detection of H. pylori and cagA of 62 gastric biopsy specimens were performed. All the slides were analyzed by the updated Sydney system. Forty eight (77.4%) were PCR positive for H. pylori and thirty four (54.8%) were positive for cagA. There were no significant differences in numbers of H. pylori, degree of infiltration of mononuclear cells and degree of atrophy between cagA-positive and cagA-negative groups. The rates of neutrophilic infiltration and intestinal metaplasia were significantly higher in cagA-positive group than in cagA-negative group. In conclusion, the detection of H. pylori by PCR method is more sensitive than that of microscopic examination and H. pylori strains possessing cagA are associated with an enhanced induction of severe gastritis.

Detection Rate of Helicobacter Pylori in Gastric Adenocarcinoma and Effect of Helicobacter Pylori Infection on Proliferative Activity of Gastric Epithelium.: Young Lyun Oh, Geung Hwan Ahn; Korean J Pathol. 1999;33(8):581-588.

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Abstract PDF: Helicobacter pylori infection has been shown to be associated with gastric carcinoma. However, despite the frequent detection of seropositivity for H. pylori and histologic detection in biopsy specimen, histologic detection rate of H. pylori in surgical specimens has been low. In this study, we investigated the prevalence of H. pylori infection in gastrectomy specimens bearing gastric adenocarcinoma and compared it with both endoscopic biopsy and serologic results. H. pylori infection was identified by Giemsa stain in the mucosa stripped from the tumor, body, and antrum in 61 gastrectomy specimens. We evaluated the effect of H. pylori infection on gastric mucosal cell proliferation by using monoclonal antibody for Ki-67. H. pylori detection rate using Giemsa stain was higher in gastrectomy specimens (67.3%) compared to that (48.1%) of biopsy specimens (p=0.006). The detection rate was higher in body than that of antrum or tumor site in the same patients (p=0.001). The H. pylori seropositivity was 60.5% and relatively nonspecific. The mean value of Ki-67 labeling index in the H. pylori-positive group was higher than that in the H. pylori-negative group (p<0.05). The increase in gastric epithelial cell proliferation was not influenced by the location of the tumor or the site of the specimen. The results suggest that the actual prevalence of H. pylori infection in patients with gastric carcinoma is considerably higher than that evaluated on endoscopic biopsy specimens. In addition, the increased cell proliferation in the H. pylori-positive group suggests some evidence that H. pylori may be involved in gastric carcinogenesis.

Topographic Difference of Inflammatory Reactions in Gastric Mucosa in Various Helicobacter pylori-Associated Diseases.: Suk Jin Choi, Tae Jung Jang; Korean J Pathol. 2000;34(1):29-33.

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Abstract PDF: Gastric biopsy specimens from 140 patients (66 chronic gastritis, 33 gastric ulcers, 26 duodenal ulcers, 15 gastric cancers) were examined to investigate the topographic difference of inflammation, glandular atrophy, intestinal metaplasia, and Helicobacter pylori (H. pylori) colonization by the updated Sydney system. Density of H. pylori of the antrum was significantly higher in duodenal ulcers than in chronic gastritis, gastric ulcers, and gastric cancers. Inflammation of duodenal ulcers was predominantly antral and glandular atrophy and intestinal metaplasia of duodenal ulcer were significantly less than those of gastric ulcers and gastric cancers. Chronic inflammation of gastric ulcers and gastric cancers was higher in antrum than in corpus. Increasing atrophy of the antrum was associated with decreasing density of H. pylori of antrum itself, but increasing colonization of the corpus. This study reveals the inflammatory reactions of gastric mucosa differ in chronic gastritis, gastric ulcers, gastric cancers, and duodenal ulcers and suggests that antral atrophy fosters the colonization of oxyntic mucosa by H. pylori.

Detection of Helicobacter pylori in the Gastric Mucous Layer in Pediatric Patients.: You Kyung Kim, Jong Sil Lee, Hwal Woong Kim, Jeong Hee Lee, Hee Shang Youn, Gyung Hyuck Ko; Korean J Pathol. 2002;36(5):292-295.

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Abstract PDF: BACKGROUND
Helicobacter pylori is present mainly in the gastric mucous layer. However, the mucous layer, along with the bacteria, is lost during conventional tissue processing in which formalin is used for fixation. The purpose of this study is to ascertain - if the mucous layer is preserved by using Carnoy solution as a fixative - whether the detection rate of H. pylori is increased in pediatric patients.
METHODS
Five pieces of gastric mucosal tissue were obtained from the gastric antrum and the body of one hundred pediatric patients. One of the specimens was fixed with formalin. Another specimen was fixed with Carnoy solution. The tissue sections were stained with hematoxylin-eosin and immunohistochemically stained for H. pylori. For reference, a rapid urease test was performed on the remaining three specimens.
RESULTS
In the formalin-fixed tissue, the detection rate of H. pylori was 13% in the gastric antrum and 12% in the body (overall 16%). In the Carnoy solution-fixed tissue, the mucous layer was preserved and the detection rate of H. pylori was 23% in the antrum and 27% in the body (overall 28%). The positive rate of the rapid urease test was 26% in the antrum and 28% in the body (overall 29%).
CONCLUSIONS
When the number of H. pylori is small in the gastric mucosa, the bacteria may not be detected by conventional histologic methods. In that case, the detection rate of H. pylori may be increased by using Carnoy solution, rather than formalin, as a tissue fixative.

Relationships between Types of Proximal Gastric Mucosa and Clinicopathological Features.: Jong Sil Lee, Hwal Woong Kim, Jeong Hee Lee, Hee Shang Youn, Woon Tae Jung, Gyung Hyuck Ko; Korean J Pathol. 2003;37(1):15-18.

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Abstract PDF: BACKGROUND
It has been believed that there is a pure mucus-secreting cardiac mucosa (CM), about 2 cm in length, below the gastroesophageal junction. However, recent reports suggest that CM might not be located at the most proximal portion of the stomach. The purpose of this study is to investigate the relationships between the types of proximal gastric mucosa and patients' age, sex, their condition regarding the Helicobacter pylori infection, and severity of chronic gastritis.
METHODS
Two pieces of mucosal tissue from the most proximal portion of the stomach and the antrum of 44 pediatric and 85 adult patients were examined using a light microscope. A rapid urease test was performed on the other antral specimen from each patient.
RESULTS
In 46 (90.2%) out of 51 patients with aged 30 or under, only the pure acid-secreting oxyntic mucosa (OM) was present at the most proximal portion of the stomach. The cardiac or mixed oxyntocardiac mucosa (OCM) increased in prevalence with age. The CM or OCM was found more frequently in patients with H. pylori infection or severe gastritis than in those without H. pylori infection or those with mild gastritis. However, there were no statistically significant differences within the same age groups.
CONCLUSIONS
Although the OCM is sometimes present at the most proximal portion of the stomach, the CM is absent or rare in individuals under the age of 30. The OCM or CM increases in prevalence with age. There are no direct relationships between the type of proximal gastric mucosa and a patient's gender, his/her condition regarding the H. pylori infection, and severity of chronic gastritis.

Clinicopathologic Analysis of Lymphocytic Gastritis.: Jeong Eun Hwang, Young Ok Hong, Dong Eun Song, Se Jin Jang, Eunsil Yu; Korean J Pathol. 2007;41(5):289-295.

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Abstract PDF: BACKGROUND
Lymphocytic gastritis (LG) is defined as an infiltration of more than 25 intraepithelial lymphocytes (IELs) per 100 surface epithelial cells, and the histological differential diagnosis of LG and residual mucosa associated lymphoid tissue (MALT) lymphoma can be difficult. Helicobacter pylori (H. pylori) is regarded as one of the possible causes of LG, but its clinicopathologic features of LG have not been clarified in Korea, which has a much higher prevalence of H. pylori infection than Western countries. We analyzed the clinicopathologic findings of LG in Korean patients and compared the cytologic findings of IELs of LG with those of MALT lymphoma.
METHODS
Sixty six cases of LG and 59 cases of MALT lymphoma were selected and clinicopathologic features were analyzed.
RESULTS
Eighteen cases (27.3%) of LG were found to be associated with H. pylori infection. The IELs in LG were found to diffusely and regularly infiltrate in the epithelium, but MALT lymphoma showed patchy IELs. IELs in LG and MALT lymphoma were CD 8+T lymphocytes and CD20+B lymphocytes, respectively. The mean nuclear size of IELs in LG was 4.37 micrometer, which was significantly smaller than those in MALT lymphoma (5.19 micrometer).
CONCLUSION
LG, a rare variant of chronic gastritis is partly associated with H. pylori infection and more complex unknown causative factors. In addition to the immunophenotyping, the nuclear sizes of IELs can be helpful in the differential diagnosis of LG and residual MALT lymphoma.

Relationship of Gastric Metaplasia of the Duodenum with Age, Duodenal Ulcer and Helicobacter pylori Infection.: Dae Hyun Song, Dong Chul Kim, Jong Sil Lee, Jeong Hee Lee, Hyun Jin Kim, Hee Shang Youn, Gyung Hyuck Ko; Korean J Pathol. 2007;41(4):217-223.

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Abstract PDF: BACKGROUND
Gastric metaplasia of the duodenum is thought to be associated with the pathogenesis of duodenal ulcer. We investigated the pathological features of gastric metaplasia and their relation to age, gender, duodenal ulcer and H. pylori infection.
METHODS
We reviewed the duodenal endoscopic findings of 535 patients (age range: 0 to 87) and the microscopic slides of the duodenal biopsy specimens.
RESULTS
Gastric metaplasia was first noted at the age of 4 and the prevalence increased thereafter until the patients' mean age reached about 30. The prevalence of gastric metaplasia was 53.7% after 30 years of age. As the metaplasia became severer, it became more polypoid in appearance and it more often contained parietal cells. Gastric metaplasia was more frequently observed or severe in duodenal ulcer patients, in males and in the first portion of the duodenum than in patients without duodenal ulcer, in females and in the second portion, respectively. There was a lack of correlation between gastric metaplasia and H. pylori infection.
CONCLUSIONS
The prevalence and/or severity of gastric metaplasia of the duodenum increases with age, and it is thought that most duodenal ulcers develop in the areas of gastric metaplasia.

Pathological Findings of Crohn's Disease in the Stomach .: Changyoung Yoo, Bo In Lee, Kyu Yong Choi, Lee So Maeng, Anhi Lee, Chang Suk Kang, Ghee Young Kwon, Kyoung Mee Kim, Cheol Keun Park; Korean J Pathol. 2006;40(4):269-273.

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Abstract PDF: BACKGROUND
The incidence of Crohn's disease in the upper digestive tract, and especially in the stomach, is recently increasing. Focal inflammatory reaction without Helicobacter pylori (H. pylori) infection is thought to be the characteristic pathologic findings suggesting Crohn's disease in the stomach. Yet gastric involvement of Crohn's disease has not been studied in Korea. We studied the endoscopic and pathologic findings of patients with Crohn's disease in the stomach by taking biopsies.
METHODS
Thirty patients with Crohn's disease who underwent gastroduodenoscopy followed by biopsies were included in the study. The pathology of the gastric biopsy specimens and the presence of H. pylori were evaluated.
RESULTS
Among 30 cases, 22 cases (73.3%) were H. pylori negative and 8 cases (26.7%) were H. pylori positive. For the H. pylori negative cases, all but one cases showed pit abscess and focal lymphocytic collections in the antrum. Granulomas were found in 6 cases (20%) and they were exclusively located in the antrum.
CONCLUSIONS
In the stomach, pit abscess and focal lymphocytic collections that are not associated with H. pylori infection are the characteristic pathologic findings found in Crohn's disease.

Histopathologic Features of Gastric Mucosa Colonized by Helicobacter pylori.: Tae Jung Jang, Dong Haeng Lee, Sang Kun Sim; Korean J Pathol. 1994;28(4):368-375.

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Abstract PDF: TO evaluate the histopathologic features of gastric mucosa by Helicobacter pylori (HP), we reviewed 70 endoscopically biopsied chronic gastritis and peptic ulcer. The results are as fonows. l. HP was detected in 923% (48/52) of active gastritis, 8l8% (9/l l) of peptic ulcer and l43% (1/7) of chronic gastritis. The prevalence of HP infection was significantly higher in active gastritis and peptic ulcer than chronic gastritis (P<0005). 2. The infiltration of intraepithelial neutrophil of the 58 HP-positive cases was significantly more than of the l2 HP-negative cases (P<0005). 3. The infiltration of neutrophil and chronic inflammatory cells in the lamina propria of the 58 HP positive cases were significantly more than of 12 HP-negative cases (P<0.005, P<0.01) 4. The gastric epithelium of 58 HP positive case showed characteristic degenerative change, such as epithelial pits (93.l%), irregular surface (84.4%), individua1 cell drop-out (46.5%) and microerosion (27.6%). The similiar changes were not seen in l2 HP-negative cases. In summary, HP is significantly correlated with inflammatory reaction of the gastric mucosa. It is also significantly correlated with the epithelial degenerative changes that is considered to the precursor of peptic ulcer.

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