Abstract
Background/Aims
Nodular gastritis (NG) is a well-known endoscopic finding observed in patients with a Helicobacter pylori infection, which may lead to invasive gastric cancer. Lymphofollicular gastritis consists of lymphoid follicles or lymphoid cell aggregates, and is common in children. The aim of this study was to identify patients with NG from those in whom gastric biopsied specimens showed lymphoid follicles and lymphoid cell aggregates.
Methods
Subjects, whose gastric biopsy specimens showed lymphoid follicles or lymphoid cell aggregates, were included in this study. The inclusion criterion was that they underwent a serum pepsinogen assay on the day of upper gastrointestinal endoscopy. NG was diagnosed if the endoscopy findings revealed regular-sized, multiple, colorless subepithelial nodules.
Results
Among 108 subjects who showed lymphoid follicles or lymphoid cell aggregates, 13 (12.0%) revealed NG on endoscopy, and all these subjects showed positive Giemsa staining. Patients diagnosed with NG were younger (p=0.012) and showed a female pre-dominance (p=0.001) compared to those without NG. The mean serum pepsinogen levels were higher (p=0.001) and lymphoid fol-licle-dominant subjects were more common (p<0.001) in the NG subjects than in those without NG. Logistic regression analysis revealed a younger age (p=0.041) and female gender (p=0.002) to be significant independent risk factors for NG.
Conclusions
NG should be distinguished from lymphofollicular gastritis because only 12% of patients showing gastric biopsy findings of lymphoid follicles and lymphoid cell aggregates demonstrated NG on endoscopy. NG is an endoscopic finding that is more common in women and in the younger population, irrespective of the biopsy findings and gastric secretory ability.
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Fig. 1.
Lymphoid follicle-dominant type. (A) On the upper gastrointestinal endoscopic findings, multiple 2 mm-sized, colorless subepithelial nodules were noticed. The findings were consistent with nodular gastritis of the small-granular type. (B) On the endoscopic findings, multiple 5 mm-sized, flat subepithelial nodules can be seen on the antrum. These findings are consistent with nodular gastritis of the large-nodular type. (C) On the gastric biopsied specimen of (A) taken from the proximal antrum, lymphoid follicles with prominent germinal centers were noticed with few lymphoplasma cell infiltration (H&E stain, ×40). The mucosa was expanded by prominent germinal centers reaching up to the superficial layer of the lamina propria. (D) On the gastric biopsied specimen of (B) from the proximal antrum, two lymphoid follicles were noticed with few lymphoid cell aggregates. The germinal centers were smaller and deeper than the first case (H&E stain, ×40).
![kjg-71-143f1.tif](/upload/SynapseXML/0028kjg/thumb/kjg-71-143f1.gif)
Fig. 2.
Lymphoid cell aggregate-dominant type. (A) The endoscopic findings of the antrum are consistent with nodular gastritis of the small-granular type. (B) The endoscopic findings are consistent with nodular gastritis of the large-nodular type. (C) On the biopsied specimen of (A), diffuse lymphoplasma cell infiltration can be observed as lymphoid cell aggregates (H&E stain, ×40). Infiltrated lymphoplasma cells on the superficial layer of the lamina propria are expanding the nodular mucosa. (D) On the biopsied specimen of (B) from the antrum, lymphoid cell aggregates can be seen on the deeper layer of lamina propria without a germinal center (H&E stain, ×40).
![kjg-71-143f2.tif](/upload/SynapseXML/0028kjg/thumb/kjg-71-143f2.gif)
Table 1.
Baseline Characteristics of the 108 Subjects Whose Gastric Biopsy Specimens Showed Lymphoid Follicles or Lymphoid Cell Aggregates
Table 2.
Serum Pepsinogen Assay, Endoscopy, and Gastric Biopsy Findings according to the Presence of Nodular Gastritis and Helicobacter pylori Infection
Variables | Nodular gastritis+ & Giemsa+ (n=13) | p-value (vs. 83 Giemsa+) | Nodular gastritis- & Giemsa+ (n=83) | p-value (vs. 12 Giemsa) | Nodular gastritis- & Giemsa (n=12) | p-value (vs. 13 nodular gastritis) | p-valuea |
---|---|---|---|---|---|---|---|
Pepsinogen I (ng/mL) | 74.3±28.9 | 0.379 | 68.4±21.2 | <0.001 | 43.4±16.6 | 0.004 | 0.001 |
Pepsinogen II (ng/mL) | 21.9±9.1 | 0.439 | 19.8±8.7 | <0.001 | 10.3±4.3 | 0.001 | 0.001 |
Pepsinogen I/II ratio | 3.5±0.8 | 0.393 | 3.9±1.5 | 0.045 | 4.9±2.3 | 0.049 | 0.062 |
Background gastric mucosa | <0.001 | 0.294 | <0.001 | <0.001 | |||
Normal finding | 0 (0) | 15 (18.1) | 0 (0) | ||||
Nodular gastritis | 13 (100.0) | 0 (0) | 0 (0) | ||||
Erosive gastritis | 0 (0) | 15 (18.1) | 4 (33.3) | ||||
Metaplastic gastritis | 0 (0) | 11 (13.3) | 1 (8.4) | ||||
Chronic atrophic gastritis | 0 (0) | 42 (50.5) | 7 (58.3) | ||||
Coexisting erosive esophagitis | 1 (7.7) | 0.652 | 6 (7.2) | 0.021 | 4 (33.3) | 0.160 | 0.034 |
Coexisting peptic ulcer disease | 0 (0) | 0.588 | 7 (8.4) | 0.590 | 0 (0) | − | 0.324 |
Dominant pathology | 0.340 | 0.001 | 0.001 | <0.001 | |||
Lymphoid follicles | 11 (84.6) | 58 (69.9) | 2 (16.7) | ||||
Lymphoid cell aggregations | 2 (15.4) | 25 (30.1) | 10 (83.3) |
Table 3.
Main Pathology Findings of 13 Nodular Gastritis Patients
Pathology finding | Endoscopy finding | Subject | PG I (ng/mL) | PG II (ng/mL) | PG I/II ratio | Other findings |
---|---|---|---|---|---|---|
Lymphoid follicle-dominant | Small-granular type | F/25 | 111.1 | 21.4 | 5.2 | − |
F/33a | 61.1 | 18.0 | 3.4 | Follow-up tests after 48 months | ||
F/53 | 35.7 | 11.8 | 3.0 | − | ||
F/41 | 75.3 | 18.0 | 4.2 | − | ||
F/47 | 57.7 | 18.5 | 3.1 | − | ||
Large-nodular type | M/36 | 67.0 | 20.2 | 3.3 | − | |
F/48a | 68.3 | 28.3 | 2.4 | Follow-up tests after 13 months | ||
F/53 | 70.1 | 27.4 | 2.6 | − | ||
F/55a | 70.4 | 20.6 | 3.4 | Follow-up tests after 49 months | ||
F/59 | 152.1 | 47.6 | 3.2 | DM | ||
F/60 | 69.6 | 19.5 | 3.6 | DM, HTN, erosive esophagitis | ||
Lymphoid cell | Small-granular type | F/37 | 51.8 | 11.7 | 4.4 | − |
aggregates-dominant | Large-nodular type | F/55 | 75.4 | 21.1 | 3.6 | − |
Table 4.
Pathology and Endoscopy Findings of 12 Subjects without a H. pylori Infection
Pathology finding | Endoscopy finding | Subject | PG I (ng/mL) | PG II (ng/mL) | PG I/ II ratio | Other findings |
---|---|---|---|---|---|---|
Lymphoid | Erosive gastritis | F/57 a | 66.1 | 10.6 | 6.2 | Follow-up tests after 58 months |
follicle-predominant | Chronic atrophic gastritis | M/39 | 50.9 | 11.0 | 4.6 | − |
Lymphoid cell | Erosive gastritis | F/47 | 38.1 | 8.2 | 4.7 | − |
aggregate-predominant | F/54 | 23.7 | 21.0 | 1.1 | NSAIDs | |
F/57 | 58.2 | 12.2 | 4.8 | Hormone replacement therapy | ||
Chronic atrophic gastritis | M/62 | 16.1 | 14.1 | 1.1 | NSAIDs | |
F/66 | 38.3 | 7.0 | 5.5 | − | ||
F/69 a | 35.4 | 5.3 | 6.6 | Follow-up tests after 24 months | ||
Chronic atrophic gastritis & | M/41 | 68.8 | 7.9 | 8.7 | − | |
erosive esophagitis | M/63 a | 43.1 | 11.8 | 3.9 | DM, HTN, H. pylori eradication | |
history, Follow-up tests after | ||||||
12 months | ||||||
M/68 | 27.7 | 7.2 | 3.8 | − | ||
Metaplastic gastritis & | M/56 | 53.9 | 7.0 | 7.7 | − | |
erosive esophagitis |
F, female; M, male; PG, pepsinogen; NSAID, nonsteroidal anti-inflammatory drug; DM, diabetes mellitus; HTN, hypertension; H. pylori, Helicobacter pylori.
a Three subjects were followed up using serum pepsinogen assay and upper gastrointestinal endoscopy. Neither nodular gastritis nor positive Giemsa staining was found at the follow-up tests. One subject (M/63) still showed lymphoid cell aggregates at the follow-up endoscopic biopsied specimen taken from the antrum.
Table 5.
Characteristics of the Subjects s according to the Pathology Findings
Table 6.
Independent Risk Factors for the Presence of Nodular Gastritis