Collagenous gastritis associated with lymphocytic gastritis and celiac disease. (Case Reports).
(Arch Pathol Lab Med. 2001;125:1579-1584)
Collagenous gastritis is a rare entity of unknown etiology that, similar to its colonic counterpart, is characterized by subepithelial collagen fibrosis greater than 10 [micro]m in thickness associated with mixed inflammatory infiltrate of the lamina propria. The disorder was originally described by Colletti and Trainer (1) in a 15-year-old girl with refractory Helicobacter pylori-negative chronic gastritis in which these specific histologic features were first noted. Since then 7 more cases of collagenous gastritis have been reported, either in isolation (2) or in association with collagenous colitis, (3-5) collagenous duodenitis, (6) lymphocytic colitis, (7) and celiac disease. (8)
Lymphocytic gastritis, first described by Haot and colleagues (9) in 1988, is characterized histologically by intra-epithelial lymphocytosis with at least 25 lymphocytes/100 epithelial cells accompanied by chronic inflammation in the lamina propria. It is associated with various etiologies and disease states, such as celiac disease (38%); H pylori infection (29%); varioliform gastritis (4%); and Crohn's disease, human immunodeficiency virus infection, inflammatory polyps, lymphoma, and esophageal carcinoma (approximately 1.5% each). In roughly 20% of the cases, the etiology is unknown.
Celiac disease is a T-cell-mediated disorder triggered by gluten in susceptible subjects, affecting not only the small bowel but also the gastric and colonic mucosae. Various histopathologic features of gastric mucosa have been noted in gluten-sensitive patients, including mild to marked increase in the cellularity of the lamina propria with a predominance of chronic inflammatory cells, intra-epithelial lymphocytosis, and, recently, increased deposition of subepithelial collagen to a thickness of more than 10 [micro]m. (8)
We report an additional case of collagenous gastritis associated with lymphocytic gastritis and celiac disease in the absence of collagenous or lymphocytic colitis, and we review the previously published observations of subepithelial collagen deposition in gastric mucosa.
REPORT OF A CASE
A 42-year-old man presented with chronic iron deficiency anemia, intermittent diarrhea, rectal bleeding, postprandial flatulence, and periumbilical cramps relieved by bowel movements. He had not traveled, he took no medications, and there was no known environmental or occupational exposure; he had a family history positive for colon cancer. Physical examination was normal. Laboratory data showed mild iron deficiency anemia. Serology was positive for antigliadin, antiendomysial, and antitissue transglutaminase antibodies. Stool cultures and examination for ova and parasites were negative. The patient underwent upper gastrointestinal endoscopy, which showed a small hiatal hernia, a fundic polyp, and mild diffuse gastric erythema. In the duodenum a geographic pattern with scalloping and erythema was seen. Colonoscopy performed for rectal bleeding revealed 4 colonic polyps.
Biopsies were taken from stomach (fundus, body, and antrum), small intestine (distal duodenum and proximal jejunum), and colon (ascending, transverse, and sigmoid colon). The patient was placed on a gluten-free diet, which led to subsequent improvement of the symptoms. An esophagogastroduodenoscopy was performed after 3 months; it showed mild antritis and partially recovered distal duodenal mucosa. Biopsies were taken from the stomach (fundus, body, and antrum) and from the distal duodenum.
Biopsy specimens from stomach (initial biopsies: 3 fundus, 1 body, 1 antrum; follow-up biopsies: 6 fundus and body, 1 antrum), distal duodenum/proximal jejunum (n = 6), and colon (n = 5) were fixed in 10% formalin and embedded in paraffin. Five-micrometer sections were stained with hematoxylin-eosin. The gastric and small intestine biopsies were also stained with modified Giemsa, Masson trichrome, and Congo red stains. The thickness of subepithelial collagen fibrosis in the gastric biopsies stained with Masson trichrome was measured with an ocular micrometer. The intra-epithelial lymphocytes were assessed in hematoxylin-eosin-stained sections at x 40 magnification by counting both lymphocytes and epithelial cell nuclei in an uninterrupted length of surface and foveolar epithelium. Five hundred epithelial cell nuclei were counted, and the results were expressed as lymphocytes per 100 epithelial cells. Counts were performed on the most involved areas of the biopsies from gastric fundus, body, and antrum. Lymphocytic gastritis was diagnosed when 25 or more intra-epithelial lymphocytes/100 epithelial cell nuclei were present in the surface and foveolar epithelium. The intra-epithelial lymphocytes were identified by the following characteristics: small size, hyperchromatic nuclei, and clear perinuclear cytoplasm. They showed positive immunostain with antibody to CD3 (Dako Corporation, Carpinteria, Calif) using a avidin-biotin detection system. The degree of acute and chronic inflammation of the lamina propria, as well as the extent of atrophy and intestinal metaplasia, were determined by using the visual analogue scales of updated Sydney system for grading chronic gastritis.
Initial Biopsies.--The biopsies of the gastric fundus and body showed diffuse moderate to marked lymphoplasmacytic infiltrate, rare intra-epithelial neutrophils, and mild glandular atrophy. The epithelial surface was focally eroded and showed focal simplification with cuboidal cells with amphophilic cytoplasm and increased nucleus-cytoplasm ratio consistent with reepithelialization. The surface and foveolar epithelium of the biopsies originating from the fundus showed increased numbers of intra-epithelial lymphocytes and cuboidal epithelial cells with degenerative changes (Figure 1). The number of intra-epithelial lymphocytes ranged from 17 to 44 per 100 epithelial cell nuclei (mean of 29/100) in 5 adjacent areas. The surface and foveolar epithelium of the gastric body did not show the typical features of lymphocytic gastritis; however, the intra-epithelial lymphocytes were slightly increased in number (13.6/100 epithelial cell nuclei) compared with normal gastric mucosa (<5 intra-epithelial lymphocytes/100 epithelial cells). (8) The antrum showed a degree of chronic inflammation similar to that of the fundus, no neutrophilic infiltrates, and mild atrophy. The antral surface and foveolar epithelium showed intra-epithelial lymphocytosis, ranging from 12 to 57 intra-epithelial lymphocytes/100 epithelial cell nuclei (mean 34.8). The intra-epithelial lymphocytes within oxyntic glands of the fundus and corpus were considerably less numerous than in the surface epithelium and averaged 5 and 4, respectively, per 100 epithelial cell nuclei.
[FIGURE 1 OMITTED]
In the subepithelial region of the fundic lamina propria, a thick hyalinized collagen band with entrapped capillaries, fibroblasts, and inflammatory cells was identified (Figure 2). The collagen deposition was discontinuous, involved 30% to 60% of the subepithelial regions of all 3 fragments (mean 50%), and ranged from 10 to 26 [micro]m (mean 20 [micro]m) in thickness. Focal degenerative changes were noted in the corresponding surface epithelium (Figure 3). The subepithelial collagen deposition in the gastric body was focal, encompassing 15% of the total length of the biopsy, and ranged from 10 to 14/[micro]m (mean 12 [micro]m) in thickness. No thickened subepithelial collagen band was noted in the antral biopsy. The presence of abnormal subepithelial collagen deposition was confirmed by Masson trichrome stain (Figure 4); staining for amyloid with Congo red was negative. Mild deep fibrosis of the lamina propria showing coarse collagen fibers was noted only in the gastric body biopsy. The histologic findings are summarized in Table 1.
[FIGURE 2-4 OMITTED]
Distal Duodenum and Proximal Jejunum Biopsies (n = 3).-- Severe villous atrophy and crypt hyperplasia accompanied by transmucosal moderate to severe lymphoplasmacytic infiltrates with rare neutrophils and increased numbers of intra-epithelial lymphocytes was identified (Figure 5) together with surface epithelial damage (cuboidal appearance and focal flattening of superficial cells). The villi-crypt ratio ranged from 0:3 to 1:3, and the mucosa measured 0.51 mm in thickness. Crypt hyperplasia and increase in mitotic activity of the crypt epithelium were present. No collagen plate thickening was identified. No ova or trophozoites of Giardia lamblia were present on hematoxylin-eosin-stained sections.
[FIGURE 5 OMITTED]
Colonic Biopsies (n = 5).--Four tubular adenomas (0.3 to 0.8 cm in size) with low-grade dysplasia were found in sigmoid, proximal transverse, and distal ascending colon. Multiple fragments of nonadenomatous colonic mucosa at 30, 70, and 80 cm showed normal numbers of intra-epithelial lymphocytes, normal subepithelial collagen plate, and no degenerative changes of the surface epithelium; these were considered to show normal-appearing large intestine mucosa.
Follow-up Biopsies.--Gastric Biopsies (n = 7).--The mucosa from the gastric fundus and body showed residual and predominantly superficial mild lymphoplasmacytic infiltrate. Neither atrophy nor intra-epithelial lymphocytosis was noted. The subepithelial collagen band was discontinuously present in only 1 of the 6 mucosal fragments, involving 30% of the biopsy length. It was uniform in thickness and measured 15 [micro]m.
The antrum showed chronic H pylori-negative gastritis with moderate transmucosal lymphoplasmacytic infiltrate and mild atrophy. The intra-epithelial lymphocytes were less numerous (range 13 to 28 intra-epithelial lymphocytes/100 epithelial cell nuclei, mean 21). In contrast with the first biopsy, in which no subepithelial collagen deposition was identified, the follow-up antral sample showed a discontinuous subepithelial collagen band with a uniform thickness of 19 [micro]m involving 50% of the mucosal length. This discrepancy may be explained by the patchy distribution of collagenous gastritis.
Distal Duodenal Biopsies (n = 3).--The mucosal surface showed partial height recovery of the villi, with a villous-crypt ratio of 1:1 to 2:1 and a thickness of 0.85 mm. Residual mild to moderate chronic inflammation was present in the lamina propria accompanied by rare clusters of intra-epithelial lymphocytes and mild reactive epithelial changes.
Collagenous gastritis is a rare clinicopathologic entity of unknown etiology and pathogenesis. Similar to its more common counterparts in colon (collagenous colitis) and small intestine (collagenous sprue), it is characterized by increased discontinuous collagen deposition in the subepithelial lamina propria with irregular edge and entrapment of capillaries, fibroblasts, and inflammatory cells. (1) Depending on the extent of the accompanying lymphoplasmacytic infiltrate in the lamina propria, the corresponding surface epithelium may show cuboidal cytoplasmic changes and reactive nuclear enlargement, subepithelial edema with or without epithelial detachment, and erosions. All 8 previously reported cases and the present case showed a variable degree of glandular atrophy. The clinical and pathologic features are summarized in Tables 2 and 3.
Collagenous gastritis has been described in pediatric and elderly patients (age range 9 to 75 years). Clinicopathologic correlation cannot be considered definitive, as so few cases are available for study. So far, however, there has been a difference between the cases of the younger patients and those of the adults, with the former presenting with upper gastrointestinal tract symptoms, whereas the adults presented with diarrhea. A corollary of this is that the endoscopic findings in the upper gastrointestinal tract were more impressive in the young patients (erosive gastritis and hemorrhages) than in the adults. Therapy in these patients did not have a consistent effect on the thickness of the collagen band, but improvement of the clinical picture was in general achieved with symptomatic treatment. In 3 of the 7 cases in which tissue was available from the large intestine, collagenous colitis or lymphocytic colitis was found.
One of the cases present in the literature (Vesoulis et al (8)) and the current report showed an association of celiac disease and collagenous gastritis. Both patients presented with diarrhea, chronic iron deficiency anemia, and a serologic picture of celiac disease supported by characteristic histologic abnormalities of duodenal mucosa. In contrast to the clinical course of the patient presented in the current report, the patient reported by Vesoulis et al (8) eventually developed a clinical, endoscopic, and histologic picture of chronic active ulcerative colitis, suggesting overlapping causes or a similar pathogenesis. The gastric biopsies in these 2 patients show features similar to the previous cases of collagenous gastritis, with a maximum collagen band thickness of 26 [micro]m in the current case and 45 [micro]m in the previous case. Unique to the cases of collagenous gastritis associated with celiac disease was the presence of lymphocytic gastritis, which is known to occur in 38% of cases of celiac disease and is thought to represent a local immune response to luminal antigens such as gliadin, rather than being part of the histologic features of collagenous gastritis. (8) Although in some of the previous cases a mild increase in intra-epithelial lymphocytes was reported, (2,5,7) the numbers were not high enough (7 to 20 intra-epithelial lymphocytes/100 epithelial cells) to render the diagnosis of lymphocytic gastritis, which requires at least 25 intra-epithelial lymphocytes/100 epithelial cells. (9)
Celiac intestinal antibodies and subclinical gluten sensitivity have been reported in association with collagenous colitis. (10) Collagenous colitis and collagenous gastritis also share other histologic features besides the defining bandlike linear deposition of extracellular matrix: they both show lack of extension of the linear matrix deposition forming the thickened collagen plate along the crypts, lymphocytic infiltrate of the overlying epithelium is present in both, and the surface epithelium in both sites may flatten or become cuboidal.
Three major pathogenic hypotheses have been proposed for increased deposition of subepithelial collagen in collagenous colitis: (1) chronic inflammation and autoimmunity, (2) abnormality of the pericryptal fibroblast sheath, and (3) leakage of plasma proteins and fibrinogen with subsequent replacement with collagen. It is conceivable that these theories could also be suggested for collagenous gastritis, given the histologic similarities and the frequent association between these 2 conditions. The coexistence of collagenous gastritis with lymphocytic gastritis and celiac disease, as well as the significant histologic improvement after 3 months of gluten-free diet in our case, appear to concur with the first theory. According to this theory, an initial insult caused by an infective agent, drugs, or gluten may damage mucosal surface, leading to an autoimmune response with ongoing inflammation in susceptible individuals. It is conceivable that various cytokines released by mononuclear inflammatory cells may activate the upward-migrating pericryptal myofibroblasts and thus induce increased subepithelial collagen deposition; however, this theory remains to be demonstrated.
Regardless of the causative agent, the distribution within different segments of gastrointestinal tract, and the various clinical associations, the presence of the prominent subepithelial deposition represents a unifying histologic feature of this rare entity, most likely indicative of a common pathogenetic mechanism. The significance of collagenous gastritis in the clinical course of celiac disease still remains to be determined by long-term follow-up studies.
Although collagenous gastritis is a rare entity, it is our belief that through wider recognition of its clinicopathologic features, more cases will be brought to light and provide additional information on its etiology and pathogenesis.
Table 1. Combined Histologic Features of Lymphocytic and Collagenous Gastritis * Inflammation ([dagger]) IEL Range (Mean) Site Acute Chronic Surface Glands Antrum 0 2 12-57 -- (34.8) Body 1 3 7-18 4 (13.6) Fundus 0 2 17-44 5 (29) Subepithelial Collagen Band Thickness in [micro]m Site % Mucosa Range (Mean) Antrum -- -- Body 15 10-14 (12) Fundus 50 10-26 (20) * IEL indicates intra-epithelial lymphocytes (number/100 epithelial cells); %, mucosal length occupied by the collagen band. ([dagger]) Grading of acute/chronic inflammation based on visual analogue scales (updated Sydney classification): 0 = no inflammation, 1 = mild, 2 = moderate, 3 = severe. Table 2. Clinical and Endoscopic Features of Reported Cases of Collagenous Gastritis * Age, y/ Upper GI Lower GI Case Reports Sex Symptoms Symptoms Collagenous 15/F Epigastric pain, No gastritis (1) recurrent he- matochezia Collagenous 9/F Retrosternal pain No gastritis (2) linked to se- vere anemia (Hb 1.7 mmol/L) Collagenous 75/F No Watery diarrhea gastroduodeni- tis and collag- enous colitis (3) Collagenous 20/M Epigastric pain, Diarrhea, stool gastritis and vomiting, fa- OB+ (6 y af- metachronous tigue, malaise ter first epi- (6 years) col- sode) lagenous coli- tis (4) Collagenous 57/F Anorexia, vomit- Watery diarrhea gastrobulbitis ing, postpran- and collage- dial fullness nous colitis (5) Collagenous 67/F No Watery diarrhea gastroduodeni- tis (6) Collagenous 35/F No Abdominal dis- gastritis and tention, fla- lymphocytic tulence, colitis (7) watery diarrhea Collagenous 57/M No Loose stools and gastritis, celi- bloody diar- ac disease, rhea and ulcerative colitis (8) Collagenous 42/M No Diarrhea, flatu- gastritis, lym- lence, abdom- phocytic gas- inal cramps, tritis, and ce- rectal bleed- liac disease ing (present case) Other Symptoms, Age, y/ Signs, or Case Reports Sex Lab Results Endoscopy Collagenous 15/F No Gastric hemor- gastritis (1) rhages; nor- mal duode- num and co- lon Collagenous 9/F No Diffuse gastric gastritis (2) erythema, ero- sions; normal duodenum and colon Collagenous 75/F Weight loss Normal upper gastroduodeni- and lower en- tis and collag- doscopy enous colitis (3) Collagenous 20/M Weight loss, Diffuse nodulari- gastritis and anemia, hook- ty of gastric metachronous worm ova in mucosa; nor- (6 years) col- stools mal duode- lagenous coli- num and rec- tis (4) tum Collagenous 57/F Weight loss; de- Gastric and bul- gastrobulbitis crease in se- bar mucosa and collage- rum albumin with patchy nous colitis (5) and total pro- erythema; tein normal colon- ic mucosa Collagenous 67/F No Normal upper gastroduodeni- and lower en- tis (6) doscopy Collagenous 35/F No Diffuse gastric gastritis and edema and lymphocytic submucosal colitis (7) nodules; nor- mal colon Collagenous 57/M Anemia, weight Duodenal vil- gastritis, celi- loss, serology lous abnor- ac disease, diagnostic of mality; erythe- and ulcerative celiac disease ma and ulcer- colitis (8) ation of entire colon; gastric findings not reported Collagenous 42/M Anemia, serolo- Diffuse gastric gastritis, lym- gy diagnostic erythema; du- phocytic gas- of celiac dis- odenal erythe- tritis, and ce- ease ma with geo- liac disease graphic pat- (present case) tern; normal colonic muco- sa with 4 pol- yps Age, y/ Previous Therapy and Case Reports Sex Drugs Follow-up Collagenous 15/F Antacids Antacids; not re- gastritis (1) sponsive Collagenous 9/F No Steroids, omep- gastritis (2) razole; asymptomatic; no endoscopic or histologic improvement Collagenous 75/F No Not reported gastroduodeni- tis and collag- enous colitis (3) Collagenous 20/M Not reported Antacids, anti- gastritis and helminthics; metachronous no symptom, (6 years) col- endoscopic, lagenous coli- or histologic tis (4) improvement Collagenous 57/F NSAIDs Steroids; symp- gastrobulbitis tomatic im- and collage- provement, nous colitis (5) but no de- crease in col- lagen Collagenous 67/F Estrogens and Loperamide; not gastroduodeni- diazepam for responsive tis (6) 10 days Collagenous 35/F No Sulfasalazine; gastritis and remission of lymphocytic diarrhea, no colitis (7) relief of the other symp- toms Collagenous 57/M Not reported Gluten-free diet, gastritis, celi- steroids, Asa- ac disease, col; clinical and ulcerative and serologic colitis (8) improvement Collagenous 42/M No Gluten-free diet; gastritis, lym- clinical and phocytic gas- histologic im- tritis, and ce- provement liac disease (present case) * GI indicates gastrointestinal; Hb, hemoglobin; NSAIDS, nonsteroidal anti-inflammatory drugs; and OB+, fecal occult blood positive. Table 3. Comparative Histopathologic Features of Collagenous Gastritis * Location of Gastric Collagen Band Case Reports (width in [micro]m) Collagenous gastritis (1) Gastric body (20- 30, up to 75), subepithelial Collagenous gastritis (2) Gastric body and antrum (mean 40, range 13-96), subepithelial Collagenous gastritis and Gastric body and metachronous (6 years) antrum (range collagenous colitis (4) 15-43), subepi-, thelial and at the level of foveolae Collagenous gastrobulbi- Gastric body and tis and collagenous co- antrum (20-40), litis (5) subepithelial, rarely at the floor of the foveolae Collagenous gastroduode- Gastric body and nitis (6) antrum (60), sub- epithelial Collagenous gastritis and Gastric body and lymphocytic colitis (7) antrum (20-30), subepithelial Collagenous gastritis, ce- Gastric antrum (13- liac disease, and ulcer- 45, mean 25), ative colitis (8) subepithelial Collagenous gastritis, Gastric fundus and lymphocytic gastritis, body (10-26, and celiac disease mean 20), subepi- (present case) thelial Other Gastric Case Reports Pathology Collagenous gastritis (1) Chronic active gas- tritis, focal atro- phy, erosions Collagenous gastritis (2) Chronic gastritis, 12 to 20 CD3/CD8+ IELs Collagenous gastritis and Diffuse chronic gas- metachronous (6 years) tritis, moderate to collagenous colitis (4) severe atrophy, no increase in IELs Collagenous gastrobulbi- Chronic active atro- tis and collagenous co- phic gastritis, fo- litis (5) cal intestinal metaplasia, sparse IELs Collagenous gastroduode- Focal atrophy nitis (6) Collagenous gastritis and Chronic active gas- lymphocytic colitis (7) tritis, 7 IELs Collagenous gastritis, ce- Chronic gastritis, in- liac disease, and ulcer- creased numbers ative colitis (8) of IELs (mean 61.5) Collagenous gastritis, Marked chronic gas- lymphocytic gastritis, tritis, atrophy, in- and celiac disease creased numbers (present case) of IELs (12-57, mean 34.8) Duodenal Case Reports Pathology Collagenous gastritis (1) Mild focal inflam- mation Collagenous gastritis (2) Normal Collagenous gastritis and Not reported metachronous (6 years) collagenous colitis (4) Collagenous gastrobulbi- Subepithelial colla- tis and collagenous co- gen band (20-30 litis (5) [micro]m), acute in- flammation and erosions Collagenous gastroduode- Villous atrophy of nitis (6) proximal duode- num Collagenous gastritis and Not studied lymphocytic colitis (7) Collagenous gastritis, ce- Near total villous at- liac disease, and ulcer- rophy, crypt hy- ative colitis (8) perplasia, marked chronic inflamma- tion Collagenous gastritis, Severe villous atro- lymphocytic gastritis, phy, crypt hyper- and celiac disease plasia, extensive (present case) lymphoplasmacyt- ic infiltrate Colonic/Rectal Case Reports Pathology Collagenous gastritis (1) Normal Collagenous gastritis (2) Nomal Collagenous gastritis and Subepithelial colla- metachronous (6 years) gen band (20-30 collagenous colitis (4) [micro]m) and mild chronic proctitis Collagenous gastrobulbi- Subepithelial colla- tis and collagenous co- gen band (>30 litis (5) [micro]m), mild lym- phoplasmacytic infiltrate Collagenous gastroduode- Not studied nitis (6) Collagenous gastritis and Mild lymphoplasma- lymphocytic colitis (7) cytic infiltrate, 30 IELs Collagenous gastritis, ce- Diffuse chronic ac- liac disease, and ulcer- tive ulcerative ative colitis (8) pancolitis Collagenous gastritis, 4 tubular adenomas lymphocytic gastritis, with mild dyspla- and celiac disease sia, normal nona- (present case) denomatous mu- cosa Follow-up Case Reports Biopsy (mo) Collagenous gastritis (1) 17 mo; no reduction in band thickness Collagenous gastritis (2) 26 mo; no reduction in band thickness Collagenous gastritis and 3 mo; increase in metachronous (6 years) gastric collagen collagenous colitis (4) band (23-225 [micro]m) Collagenous gastrobulbi- 18 mo; collagen tis and collagenous co- band present litis (5) Collagenous gastroduode- 12 mo; collagen nitis (6) band present Collagenous gastritis and No lymphocytic colitis (7) Collagenous gastritis, ce- No liac disease, and ulcer- ative colitis (8) Collagenous gastritis, 3 mo; less extensive lymphocytic gastritis, collagen band (19 and celiac disease [micro]m); partial re- (present case) covery of villi * IELs indicates intra-epithelial lymphocytes expressed as number/100 epithelial cells.
Note.--Subsequent to acceptance of this manuscript, an article by Lagorce-Pages et al(11) has been published. The authors report 6 new cases of this rare condition, none associated with celiac disease. The authors confirmed the suggestion that 2 subsets of patients (young with severe symptoms and adults with chronic watery diarrhea) may be identified in collagenous gastritis.
(1.) Colletti RB, Trainer TD. Collagenous gastritis. Gastroenterology. 1989;97: 1552-1555.
(2.) Cote JF, Hankard GF, Faure C, et al. Collagenous gastritis revealed by severe anemia in a child. Hum Pathol. 1998;29:883-886.
(3.) Stolte M, Ritter M, Borchard F, Koch-Scherrer G. Collageneous gastroduodenitis on collagenous colitis. Endoscopy. 1990;22:186-187.
(4.) Pulimood AB, Ramakrishna BS, Mathan MM. Collagenous gastritis and collagenous colitis: a report with sequential histological and ultrastructural findings. Gut. 1999;44:881-885.
(5.) Castellano VM, Munoz MT, Colina F, Nevado M, Casis B, Solis-Herruzo JA. Collagenous gastrobulbitis and collagenous colitis. Scand J Gastroenterol. 1999;6:632-638.
(6.) Borchard F, Niederau C. Kollagene gastroduodenitis. Dtsch Med Wochenschr. 1989;114:1345-.
(7.) Groisman GM, Meyers S, Harpaz N. Collagenous gastritis associated with lymphocytic colitis. J Clin Gastroenterol. 1996;22:134-137.
(8.) Vesoulis Z, Lozanski G, Ravichandran P, Esber E. Collagenous gastritis: a case report, morphologic evaluation and review. Mod Pathol. 2000;13:591-596.
(9.) Haot J, Hamichi L, Wallez L, Mainguet P. Lymphocytic gastritis: a newly described entity: a retrospective endoscopic and histologic study. Gut. 1988;29:1258-1264.
(10.) Moayyedi P, O'Mahony S, Jackson P, et al. Small intestine in lymphocytic and collagenous colitis. J Clin Pathol. 1997;50:527-529.
(11.) Lagorce-Pages C, Fabiani B, Bouvier R, Scoazec JY, Durand L, Flejou JF. Coliagenous gastritis. Am J Surg Pathol. 2001;25:1174-1179.
Accepted for publication June 8, 2001.
From the Departments of Pathology and Laboratory Medicine (Drs Stancu, De Petris, and Lev) and Gastroenterology (Dr Palumbo), Roger Williams Medical Center, Providence, RI, a Boston University affiliate.
Corresponding author: Giovanni De Petris, MD, Department of Pathology and Laboratory Medicine, Roger Williams Medical Center, 825 Chalkstone Ave, Providence, RI 02908.
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|Author:||Stancu, Mirela; De Petris, Giovanni; Palumbo, Theodore P.; Lev, Robert|
|Publication:||Archives of Pathology & Laboratory Medicine|
|Date:||Dec 1, 2001|
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