Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 
Print this page Email this page Users Online: 228

 
ORIGINAL ARTICLE
Ahead of print publication  

Histopathology of gastroesophageal lesions and its correlation with Helicobacter pylori and mucin histochemistry


 Department of Pathology, Government Medical College, Nagpur, Maharashtra, India

Date of Submission30-May-2020
Date of Decision28-Jun-2020
Date of Acceptance20-Jul-2020

Correspondence Address:
Anupama Praveen Gupta,
203, Shyam Dham, C. A. Road, Babulban, Nagpur - 440 008, Maharashtra
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/mjdrdypu.mjdrdypu_82_20

  Abstract 


Objective: Helicobacter pylori infection and subsequent gastric atrophy and intestinal metaplasia (IM) are postulated to increase incidence of gastroesophageal cancers. Hence, this study was carried out with objective to study histomorphology of gastroesophageal lesions and correlate with H. pylori and mucin histochemistry. Materials and Methods: This is an observational, prospective study on 120 gastroesophageal biopsies for identification of H. pylori and mucin histochemistry for type of metaplasia in addition to routine histopathology. Results: Of 120 gastroesophageal biopsies, 58 were esophageal and 62 gastric. Various esophageal lesions comprised of esophagitis, Barrett's esophagus, dysplasia, and esophageal malignancies. H. pylori were detected in 1, 4, and 1 cases of esophagitis, Barrett's esophagus, and adenosquamous carcinoma, respectively. IM was seen in 2 cases of Barrett's esophagus and one each of adenocarcinoma and adenosquamous carcinoma of esophagus. Gastric pathologies comprised of chronic gastritis, gastric ulcer, hyperplastic polyp, Peutz–Jeghers syndrome, adenocarcinoma, and gastrointestinal stromal tumor. A study for H. pylori and mucin histochemistry revealed statistically significant association between H. pylori and gastric adenocarcinoma, chronic gastritis but not with gastric ulcer. 76.31% and 21.73% cases of adenocarcinoma and gastric nonneoplastic lesions showed IM with statistically significant association with gastric adenocarcinoma particularly intestinal type. Conclusion: Since there is significant role of H. pylori and gastroesophageal malignancies histopathology and early detection of the bacilli can help in timely treatment and prevention of gastroesophageal malignancy.

Keywords: Gastroesophageal, Helicobacter pylori, intestinal metaplasia, mucin histochemistry



How to cite this URL:
Gupta AP, Suryawanshi UD, Kumbhalkar DT. Histopathology of gastroesophageal lesions and its correlation with Helicobacter pylori and mucin histochemistry. Med J DY Patil Vidyapeeth [Epub ahead of print] [cited 2021 Nov 30]. Available from: https://www.mjdrdypv.org/preprintarticle.asp?id=321284




  Introduction Top


Helicobacter pylori (H. pylori) infect more than half the global population, causing peptic ulcer diseases, and chronic gastritis; it is also strongly associated with gastric malignancies. It has been classified as a class I carcinogen.[1]

Atrophy and intestinal metaplasia (IM) of stomach are considered preneoplastic lesions which are associated with inflammatory processes, especially H. pylori infection. It has postulated that if gastritis persists atrophy and IM ensue sequentially over a period of decades.[2] Thus, pathologist are questioned whether H. pylori is present and whether cancer or a precancerous lesion like IM is present or not.[3] Studies have also documented presence of H. pylori in Barrett's esophagus and associated adenocarcinoma.[4] Hence, the present study was carried out to study histomorphology of gastroesophageal lesion and its correlation with H. pylori and mucin histochemistry.


  Materials and Methods Top


This is observational, prospective study on 120 adequate gastroesophageal biopsies (open and endoscopic) done at tertiary care hospital of central India over 2 years' period.

Institutional ethical clearance and informed consent was taken vide letter number COI/Patho/49312020 dated 30-06-2020. The study was aimed to look for histomorphology of gastroesophageal lesions and correlate its association with mucin histochemistry and H. pylori.

Patients with upper gastrointestinal symptoms underwent endoscopy and if having gastroesophageal lesions in the form of ulcer, polyp, growth, etc., were biopsied. Only properly oriented adequate biopsies having muscularis mucosa were included in the study. Two antral and one corpus biopsies were taken from stomach in gastritis and four quadrant biopsies were taken from other lesions in stomach and esophagus. The additional biopsy was taken if necessary and was totally at endoscopist's discretion. The biopsies were put on a wet filter paper with mucosal surface on the upper side to avoid curling of the biopsy. Using 10% formalin and routine paraffin embedding, four serial sections of five microns were prepared from each block and stained with routine hematoxylin and Eosin, giemsa for H. pylori, and alcian blue/PAS for mucin histochemistry.

For geimsa staining after deparaffinization and rehydration through graded alcohols to water, rinse in buffered distilled water (pH 6.8) and stain the slide with giemsa stain for 1 min. Then, dilute with buffer solution and keep for 8–10 min. Wash with tap water, dry, clear with xylene and mount. Bacilli stain deep blue.

For AB-PAS method, after deparaffinizing and rehydration through graded ethanol to deionized water. Stain in the alcian blue solution for 30 min. Rinse in running tap water for 5 min and then briefly in deionized water. Then, proceed with routine PAS stain. Then, dehydrate, clear, and mount. Glycogen, neutral mucins, various glycoprotein stain magenta, acid mucins (sulfomucin and sialomucins) stains blue, proteoglycans and hyaluronic acid stains blue. Cells or tissue that contains both neutral mucins and acid mucins may stain various shades of blue-purple to purple.

Data were compiled, tabulated, and analyzed using Pearson's Chi-square test using appropriate software. P < 0.001 was considered statistically significant.


  Results Top


Of 120 adequate gastroesophageal biopsies, 110 were endoscopic biopsies and 10 were open biopsies (both surgical specimens and surgical biopsies in inoperable case). Of which 58 were from esophageal and 62 were from gastric lesions. M: F ratio was 2:1. Maximum cases (34; 28.33%) were in the age group of 61–70 years.

Of 58 esophageal lesions, maximum cases (51) were of esophageal malignancy followed by Barrett's esophagus (4), esophagitis (2), and dysplasia (1) [Table 1]. Of two esophagitis, H. Pylori were detected in one of them but no IM was seen. All 4 cases of Barrett's esophagus were male in the age group of 40–60 years with long standing history of gastroesophageal reflux disease (GERD). Of 4 Barrett's esophagus, one was suspected as esophageal carcinoma on endoscopy. H. Pylori were detected in all four cases. Mucin histochemistry revealed acidic mucin (IM) and neutral mucin (gastric metaplasia) in 2 cases (50%) of Barrett's esophagus [Figure 1]. Two showed mild dysplasia but malignancy was not detected in any of them. Among esophageal malignancies, 48 cases (94.12%) of squamous cell carcinoma (SCC) predominated, others were one each (1.96%) of adenocarcinoma, adenosquamous carcinoma, and small cell carcinoma. Of 48 cases of SCC, 1 (2.08%) was of basaloid SCC. M:F ratio was 2:1. Endoscopy revealed exophytic growth, ulcerative growth, and ulcero-infiltrative growth in 74.5% (38/51), 17.65% (9/51), and 7.85% (4/51) cases, respectively. H. pylori and IM was not seen in SCC and small cell carcinoma whereas H. pylori were detected in one case of adenosquamous carcinoma. IM was present in cases of adenocarcinoma and adenosquamous carcinoma [Figure 2].
Table 1: List of diagnosis of esophageal lesions

Click here to view
Figure 1: Barrett's esophagus: (a) H and E × 10 columnar metaplasia of squamous epithelium, (b) H and E × 40 Gastric type of columnar epithelium, Inset-alcian blue/PAS × 40 PAS positive gastric type glands, (c) alcian blue/PAS × 40 intestinal metaplasia showing alcian blue positive goblet cells, (d) giemsa × 100 curved Helicobacter pylori organisms

Click here to view
Figure 2: Esophageal carcinoma: (a) H and E × 40 SCC showing pearl, (b) H and E × 40 Basaloid squamous cell carcinoma showing peripheral palisading and squamous areas, (c) H and E × 40 Adenocarcinoma showing malignant glands, (d) H and E × 10 Adenosquamous carcinoma showing malignant adeno and squamous component, Inset-alcian blue/PAS × 40 showing alcian blue positive cells

Click here to view


Of 62 gastric biopsies, 38, 11, 10 were of adenocarcinoma, chronic gastritis, gastric ulcer, respectively, and 1 each of hyperplastic polyp, Peutz–Jeghers syndrome, gastrointestinal stromal tumor (GIST) [Table 2]. Of 38 gastric adenocarcinomas, 78.94% and 21.06% were of intestinal and diffuse type using Lauren's classification.[5] M: F ratio was equal in diffuse type, whereas male preponderance was noted in intestinal type. We used Updated Sydney classification for the assessment of chronic gastritis.[6] H. pylori was present in 10; 90.91%, chronic inflammation in 11; 100%, activity in 9; 81.82%, atrophy in 9; 81.82% and IM in 3; 27.27% cases. The ratio of antrum predominant gastritis and pangastritis (antrum + body) was 9:2.
Table 2: List of diagnosis in gastric lesions

Click here to view


H. pylori were found in 90.91%, 63.16%, 40% cases of chronic gastritis, gastric adenocarcinoma, gastric ulcer, respectively. There was statistically significant association between H. pylori and gastric adenocarcinoma (χ2 = 16.81, P < 0.001) but no significant association with gastric ulcer cases (P = 1.00). H. pylori were found in 10; 90.91% cases of chronic gastritis un-associated with gastric adenocarcinoma or ulcer. In addition, chronic gastritis was seen in adjacent mucosa of gastric adenocarcinoma in 18 cases and in 4 cases of gastric ulcer. Thus, of total 33 cases of chronic gastritis H. pylori was seen in 24 cases. There was significant association between H. pylori and chronic gastritis (χ2 = 25.49, P < 0.001) [Table 3].
Table 3: Statistically significant association of Helicobacter pylori with chronic gastritis

Click here to view


IM was seen in 76.31%, 21.73% cases of adenocarcinoma and gastric nonneoplastic lesions, respectively. Nonneoplastic gastric lesions with IM had 27.27% and 20% cases of chronic gastritis and gastric ulcer. Gastric adenocarcinoma had statistically significant association (χ2 = 16.11, P < 0.001) with IM particularly with intestinal type of adenocarcinoma (93.33%). IM was seen in 55.26% (21/38) H. pylori positive gastric lesions with no significant association between IM and H. pylori infection (χ2 = 0.01, P = 0.93). There was one classical case of Menetrier's disease associated with intestinal type of gastric adenocarcinoma which showed H. pylori and IM.


  Discussion Top


Various studies have emphasized on importance of H. pylori from the time it was first cultured in vitro and was associated with gastritis and peptic ulcers.[7] It has shown its association with diseases such as dyspepsia, peptic ulcer disease, adenocarcinoma, and gastric mucosa-associated lymphoid tissue lymphoma.[8] Barry J. Marshall recommends that for diagnosis and management of H. pylori most sensitive test should be used which at present is nothing but histology.[9] Histology can establish diagnosis of associated gastritis and other disease conditions such as malignancies important for further management. In addition, pathologists are often enquired on preneoplastic changes like IM as proportion of gastric cancers develops in epithelium showing IM. Tumors showing tubular differentiation with goblet cells secreting acid mucins and an expanding pattern of growth (intestinal type) are considered to arise in IM while those showing little glandular differentiation and an infiltrating pattern of growth (diffuse type) arise in normal gastric mucosa.[10] Hence, taking histology as gold standard, the present study was carried out on gastro esophageal biopsies to look for the association of H. pylori and mucin histochemistry with various gastroesophageal lesions.

Of total 120 gastroesophageal biopsies, 58 were from esophageal lesions and 62 were from gastric lesions. Maximum cases (34; 28.33%) were in the age group of 61–70 years where majority (97; 80.8%) fell in the age group of 41–70 years.

Of 58 esophageal biopsies, malignancy predominated with 51 cases, the remaining were Barrett's esophagus 4, esophagitis 2, and dysplasia 1 case. Of two reflux esophagitis, H. Pylori was found in one but IM was not seen. H. pylori prevalence in GERD has been reported in range of 20%–75%. Such wide range of prevalence could be due to difference in selection of patients, insufficient numbers of patients, and heterogeneous selection of control population.[11]

All 4 Barrett's esophagus cases had long standing history of GERD. Out of 4 one was suspected as esophageal carcinoma on endoscopy. H. Pylori were detected in all 4 and mucin histochemistry revealed acidic mucin (IM) and neutral mucin (gastric metaplasia) in 2 (50%) each, of which 2 cases also showed mild dysplasia but malignancy was not detected. Newton M evaluated H. pylori in reflux esophagitis and Barrett's esophagus and found positivity in 25%.[12] Lord RV in a study on Barrett's oesophagus or Barrett's adenocarcinoma found H. pylori in 8/160 (5%) patients.[13] Randall found acidic mucin in 70% of cases.[14] Chandrasoma found IM and gastric type of metaplasia in 73% and 27% cases, respectively.[15]

Among esophageal malignancy SCC predominated with 94.11% (48/51) and 1.96% (1/51) cases were of adenocarcinoma, adenosquamous carcinoma, and small cell carcinoma each. Of 48 cases of SCC, 1 (2.08%) was of basaloid SCC. SCC predominated in other studies also.[16],[17] Rare variants such as basaloid (squamous cell) carcinoma and small cell carcinoma have been also reported.[18],[19] H. pylori and IM was not detected in SCC and small cell carcinoma but H. pylori were found in one case of adeno SCC and IM was present in one case each of adenocarcinoma and adenosquamous carcinoma in our study. Rokkas et al. reported no statistically significant relationship with SCC and H. pylori.[20] Wu DC found 22.1% cases and 43.3% controls positive for H. pylori.[21] They also reported that subjects with positive H. pylori had a significantly reduced risk of developing SCC than those without but additional studies are needed for confirmation.

Of 62 gastric biopsies 38, 11, 10 were of adenocarcinoma, chronic gastritis and gastric ulcer respectively and 1 each of hyperplastic polyp, Peutz–Jeghers syndrome, GIST. Among adenocarcinoma 1 interesting case was associated with Menetrier's disease. Only one case of chronic gastritis was associated with long standing history of NSAID.

Using updated Sydney classification in chronic gastritis H. pylori, chronic inflammation, activity, atrophy, and IM was noted in 10; 90.91%, 11; 100%, 9; 81.82%, 9; 81.82%, and 3; 27.27% cases, respectively where majority had antrum predominant gastritis. It is well established fact that H pylori are main cause of chronic gastritis. We found H. pylori in 90.91% (10/11) cases of chronic gastritis un-associated with gastric adenocarcinoma or ulcer [Figure 3]. In addition, chronic gastritis was seen in adjacent mucosa of gastric adenocarcinoma in 18 cases and in 4 cases of gastric ulcer. Of total 33 cases of chronic gastritis H. pylori were seen in 24 cases. There was statistically significant association between H. pylori and chronic gastritis (χ2 = 25.49 P < 0.001). Initial studies by Warren and Marshall have also identified H. pylori in large proportion of cases of chronic gastritis and peptic ulcer.[7] Other studies have also reported high association of this bacilli and histological changes in antral biopsies and peptic ulcer disease.[22],[23]
Figure 3: Chronic active atrophic gastritis: (a) H and E × 4 Gastric antrum showing severe atrophy, (b) H and E × 10 Showing inflammatory infiltrate, activity and moderate atrophy, (c) Alcian blue/PAS × 40-Showing alcian blue positive goblet cells, (d) Giemsa × 100-Showing small curved Helicobacter pylori organisms

Click here to view


The prevalence of H. pylori infection in India is reported as 22%, 56% and 87% in 0–4, 5–9 and 10–19 years of age group, respectively, with no statistical difference between sexes. Annual incidence is 0.3%–0.7% in developed countries and 6%–14% in developing nations. Re-infection rate after treatment is higher in under five-age group of children.[24] Prasad S detected H. pylori in the gastric mucosa of 25/30; 83.3% normal volunteers and high prevalence rates in the disease groups which included 92.6%, 81.3%, and 71.4% positive cases in duodenal ulcer, gastric ulcer, and nonulcer dyspepsia, respectively.[25] They found H. pylori colonization was associated with histological abnormalities such as chronic atrophic gastritis and superficial gastritis.[25] Seery et al. reported that Indian and white patients had the same rate of H. pylori infection.[26] They found that there was no excess of H. pylori-related pathology in Southall immigrant Indians and suggested that the high rates of duodenal ulceration, gastritis, and H. pylori in India are environmentally related rather than racially determined.[26]

Activity was noticed in 9 (81.82%) cases of chronic gastritis and of them 8 showed H. pylori. The association of H. pylori and activity is a known fact proved by various studies who also found that bacilli increases toward ulcerative areas and often seen in proximity of polymorphs.[23],[27] Nine (81.82%) cases of chronic gastritis showed atrophy. Mild, moderate, and severe atrophy was noticed in 5, 2, and 2 cases, respectively. H. pylori were detected in all cases of gastric mucosal atrophy. In all 3 (27.27%) cases, IM was evident in antrum and they showed H. pylori and mild atrophy. The attachment of H. pylori to epithelium having incomplete type of IM has been documented, which was further confirmed by immunohistochemical study by researchers.[28]

Of 10 gastric ulcers, 1, 2, and 7 were of acute gastric ulcer, chronic peptic ulcer, and perforation peritonitis, respectively. History of smoking, alcoholism, and chronic use of NSAIDs was seen in cases who presented with perforation peritonitis. H. pylori and IM was seen in 4; 40% and 2; 20% cases, respectively of gastric ulcer. There was no statistically significant association between H. pylori and gastric ulcer (P = 1.00). Jain et al. found significantly greater number of smokers and alcoholics in duodenal ulcer group as compared to the controls and reported similar relation with NSAIDs.[29] A meta-analysis clarified that H. pylori and NSAIDs are important factors for peptic ulcer.[30] We also found yeast as well as mycelium of Candida in 30% (3/10) cases of gastric ulcer having perforation peritonitis. Katzenstein and Maksem found fungal organism in 1/3 of 72 gastric ulcers and mentioned that they had high postoperative mortality.[31]

Of 2 cases of gastric polyps one was of 17-year-old male with hyperplastic polyp and other was 13 years/F with Peutz–Jeghers syndrome, with positive family history and presence of oral melanosis. She presented with multiple polyps in body and fundic region of stomach and jejunum. H. pylori and IM were not found in any of them.

Of 39 gastric neoplasms, 38 were of adenocarcinoma and one of the gastrointestinal tumors (GIST). M: F ratio was 26:12. Majority (29/38; 76.31%) of cases were above 50 years of age. On endoscopy predominant pattern of growth was exophytic (25/38; 65.79%), followed by ulcerative (9/38; 23.68%), ulceroinfiltrative (3/38; 7.89%).

Antrum was the most common site of malignancy (26/38; 68.42%); followed by antrum + body (7/38; 18.42%), cardia (2/38; 5.26%), body (2/38; 5.26%), and cardia + body (1/38; 2.63%), respectively.

We had 30/38; 78.94% and 8/38; 21.06% cases of intestinal and diffuse type respectively with equal M: F occurrence in diffuse type but male preponderance (73.33%) was noted in intestinal type, similar to study by Lauren and Parsonnet.[5],[32] We found H. pylori in (24/38; 63.16%) cases of adenocarcinoma [Figure 4]. Of which 19 and 5 were of intestinal and diffuse type respectively with statistically significant association of H. pylori with gastric adenocarcinoma. However, there was no significant difference between associations of H pylori infection with the type of adenocarcinoma. Significant association of H. pylori with gastric carcinoma has been reported by many authors.[32],[33],[34],[35]
Figure 4: Gastric adenocarcinoma: (a) Endoscopy showing exophytic growth, (b) H and E × 40 - Diffuse adenocarcinoma showing signet ring cells with intra cellular mucin, Inset showing gastric type mucin, (c) H and E × 10 - Intestinal type of gastric adenocarcinoma, Inset-giemsa × 100 showing Helicobacter pylori, (d) alcian blue/PAS × 40 Intestinal type adenocarcinoma showing acidic mucin

Click here to view


Mucin study revealed intestinal type of mucin (acidic) in 76.32% (29/38) cases of gastric carcinoma. Of which 28 and 1 were of intestinal and diffuse type, respectively, with statistically significant association between IM and gastric adenocarcinoma (P < 0.001) particularly for intestinal type. Similar high association is also reported by other authors' too.[33],[36]

One interesting case of 55 years/M where adenocarcinoma was associated with Menetrier's disease which classically presented with hyperplastic rugae involving fundus and body and sparing antrum. He had a history of edema of feet and face, loss of weight and appetite, nausea, and vomiting since 3 years. Serum protein was 4 g%. H. pylori and IM was detected in this case [Figure 5] and [Figure 6]. Vandenborre et al. reported a case of hypertrophic gastropathy associated with gastric adenocarcinoma.[37] Bayerdörffer et al. also described case of Menetrier's disease associated with protein loss from the stomach where antibacterial treatment led to eradication of H pylori and the return to normal rugae and the mucosal histology suggesting that these patients can be healed if treated early by the eradication of H. pylori.[38]
Figure 5: Menetrier's disease: (a) specimen showing hypertrophic rugae resembling cerebral convolutions, (b) H and E × 10 Microphotogragh showing foveolar hyperplasia, (c) H and E × 40 Adenocarcinoma in Menetrier's disease, (d) Alcian blue/PAS × 40 showing a positive goblet cells

Click here to view
Figure 6: MGG stain × 100 showing plenty of curved deep blue Helicobacter pylori bacilli in Menetrier's disease

Click here to view


We also studied adjacent mucosa in 18/38 cases of gastric adenocarcinoma. All had evidence of chronic gastritis. We found atrophy, activity, H. pylori and IM in 10; 55.55%, 17; 94.44%, 12; 66.67%, and 14; 77.78% cases, respectively. Out of 10 cases of chronic atrophy (8/10; 80%) had intestinal type of adenocarcinoma and (2/10; 20%) had diffuse type of adenocarcinoma. Thus, chronic atrophic gastritis was closely associated with intestinal type of adenocarcinoma similar to other authors.[5],[39] Byung Mu Lee studied total of 175 paired gastric specimens (175 tumors and 175 tissues adjacent to tumor) and found H. pylori in 78.9% (138/175) cases and H. pylori in 42.9% among tumor specimens, while in 72.6% among tissues adjacent to the tumor.[34]

While comparing IM in gastric adenocarcinoma and nonneoplatic condition of stomach, it was found that IM was evident in76.31% (29/38) cases of gastric adenocarcinoma, and in 21.73% (5/23) cases of nonneoplastic gastric lesions indicating strong correlation between IM and gastric adenocarcinoma. Other authors have also reported similar findings.[33],[40]

We also studied the association of H. pylori with IM and found that out of 120 gastroesophageal lesions, IM was seen in 38, of which maximum cases were of (29/38) gastric adenocarcinoma, followed by 5 of gastritis and gastric ulcer inclusive, 2 of Barrett's esophagus, and one each of adenocarcinoma and adenosquamous carcinoma of esophagus. H. pylori were present in (44/120; 36.67%) cases of gastroesophageal lesions. IM was present in (24/44; 54.54%) H. pylori positive cases, of which majority were of (61.29%, 38/62) gastric lesions. Of 38 H. pylori positive gastric lesions, IM was seen in 55.26% (21/38) cases with no significant association between IM and H. pylori infection (P = 0.93). Similar results were noted by Evrensel et al.[41]

Eidt S noted that the prevalence of IM varied in the groups and stated that hypothetically H. pylori promote mucosal regeneration which can lead to IM.[42] Schneller et al. found increased incidence of IM in Cag A + samples than with Cag A-samples (52.2% vs. 15.4%, respectively).[43] Their findings indicate that the virulent H. pylori strain is associated with a high incidence of IM and that these patients may be at greater risk for developing gastric cancer than the general population.

Authors have highlighted association of H. pylori with acute and chronic inflammation and that its presence was strongly associated with foveolar hyperplasia and lymphoid follicles.[44] Long-term follow-up and test and treat strategy in patients with H. pylori, especially in early stage before the development of pre neoplastic changes will prove to be cost-effective in preventing development of gastric cancers.[45]


  Conclusion Top


Hence, ours is a comprehensive study on histopathology of gastroesophageal lesions, a gold standard and its association with H. pylori and mucin histochemistry. The study revealed statistically significant association of H. pylori and IM with gastric adenocarcinoma.

Future recommendation: More such studies would lead to early detection and eradication of H. pylori and prevention of its dreadful complications. Additional study of adjacent mucosa can throw light on associated mucosal changes in malignant lesions.

Acknowledgment

We would like to thank Dr. Rasika Gadkari, Professor AIIMS, Nagpur and technical staff of Pathology, Government Medical College, Nagpur, India.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Anonymous. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans, Lyon, 7-14 June 1994. In IARC Monogr. Eval. Carcinog. Risks Hum 1994;61:1-241.  Back to cited text no. 1
    
2.
Guarner J, Herrera-Goepfert R, Mohar A, Sanchez L, Halperin D, Ley C, et al. Gastric atrophy and extent of intestinal metaplasia in a cohort of Helicobacter pylori-infected patients. Hum Pathol 2001;32:31-5.  Back to cited text no. 2
    
3.
El-Zimaity HM, Graham DY. Evaluation of gastric mucosal biopsy site and number for identification of helicobacter pylori or intestinal metaplasia: Role of the sydney system. Hum Pathol 1999;30:72-7.  Back to cited text no. 3
    
4.
Quddus MR, Henley JD, Sulaiman RA, Palumbo TC, Gnepp DR. Helicobacter pylori infection and adenocarcinoma arising in Barrett's esophagus. Hum Pathol 1997;28:1007-9.  Back to cited text no. 4
    
5.
Lauren P. The two histological main types of gastric carcinoma: Diffuse and so-called intestinal-type carcinoma. An attempt at a histo-clinical classification. Acta Pathol Microbiol Scand 1965;64:31-49.  Back to cited text no. 5
    
6.
Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol 1996;20:1161-81.  Back to cited text no. 6
    
7.
Warren JR, Marshall B. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 1983;1:1273-5.  Back to cited text no. 7
    
8.
El-Zimaity H, Serra S, Szentgyorgyi E, Vajpeyi R, Samani A. Gastric biopsies: the gap between evidence-based medicine and daily practice in the management of gastric Helicobacter pylori infection. Can J Gastroenterol 2013;27:e25-30.  Back to cited text no. 8
    
9.
Malik GM, Mubarik M, Kadla SA. Helicobacter pylori infection in endoscopic biopsy specimens of gastric antrum: Laboratory diagnosis and comparative efficacy of three diagnostic tests. Diagn Ther Endosc 1999;6:25-9.  Back to cited text no. 9
    
10.
Jass JR, Filipe MI. The mucin profiles of normal gastric mucosa, intestinal metaplasia and its variants and gastric carcinoma. Histochem J 1981;13:931-9.  Back to cited text no. 10
    
11.
Pieramico O, Zanetti MV. Relationship between intestinal metaplasia of the gastro-oesphageal junction and Helicobacter pylori infection and gastro-oseophageal reflux disease: a prospective study. Digest Liver Dis 2000;32:567-72.  Back to cited text no. 11
    
12.
Newton M, Bryan R, Burnham WR, Kamm MA. Evaluation of Helicobacter pylori in reflux oesophagitis and Barrett's oesophagus. Gut 1997;40:9-13.  Back to cited text no. 12
    
13.
Lord RV, Frommer DJ, Inder S, Tran D, Ward RL. Prevalence of Helicobacter pylori infection in 160 patients with Barrett's oesophagus or Barrett's adenocarcinoma. Aust N Z J Surg 2000;70:26-33.  Back to cited text no. 13
    
14.
Lee RG. Mucins in Barrett's esophagus: a histochemical study. Am J Clin Pathol 1984;81:500-3.  Back to cited text no. 14
    
15.
Chandrasoma PT, Der R, Dalton P, Kobayashi G, Ma Y, Peters J, et al. Distribution and significance of epithelial types in columnar-lined esophagus. Am J Surg Pathol 2001;25:1188-93.  Back to cited text no. 15
    
16.
Cherian JV, Sivaraman R, Muthusamy AK, Jayanthi V. Carcinoma of the esophagus in Tamil Nadu (South India): 16-year trends from a tertiary center. J Gastrointestin Liver Dis 2007;16:245-9.  Back to cited text no. 16
    
17.
Abdullah M, Karim AA, Goh KL. Late presentation of esophageal cancer: observations in a multiracial South-East Asian population. J Dig Dis 2010;11:28-33.  Back to cited text no. 17
    
18.
Li TJ, Zhang YX, Wen J, Cowan DF, Hart J, Xiao SY. Basaloid squamous cell carcinoma of the esophagus with or without adenoid cystic features. Arch Pathol Lab Med 2004;128:1124-30.  Back to cited text no. 18
    
19.
Hosokawa A, Shimada Y, Matsumura Y, Yamada Y, Muro K, Hamaguchi T, et al. Small cell carcinoma of the esophagus. Analysis of 14 cases and literature review. Hepatogastroenterology 2005;52:1738-41.  Back to cited text no. 19
    
20.
Rokkas T, Pistiolas D, Sechopoulos P, Robotis I, Margantinis G. Relationship between Helicobacter pylori infection and esophageal neoplasia: a meta-analysis. Clin Gastroenterol Hepatol 2007;5:1413-7, 1417.e1-2.  Back to cited text no. 20
    
21.
Wu DC, Wu IC, Lee JM, Hsu HK, Kao EL, Chou SH, et al. Helicobacter pylori infection: a protective factor for esophageal squamous cell carcinoma in a Taiwanese population. Am J Gastroenterol 2005;100:588-93.  Back to cited text no. 21
    
22.
Romshoo GJ, Malik GM, Bhat MY, Rather AR, Basu JA, Qureshi KA. Helicobacter pylori associated antral gastritis in peptic ulcer disease patients and normal healthy population of kashmir, India. Diagn Ther Endosc 1998;4:135-9.  Back to cited text no. 22
    
23.
Johnston BJ, Reed PI, Ali MH. Campylobacter like organisms in duodenal and antral endoscopic biopsies: relationship to inflammation. Gut 1986;27:1132-7.  Back to cited text no. 23
    
24.
Das JC, Paul N. Epidemiology and pathophysiology of Helicobacter pylori infection in children. Indian J Pediatr 2007;74:287-90.  Back to cited text no. 24
    
25.
Prasad S, Mathan M, Chandy G, Rajan DP, Venkateswaran S, Ramakrishna BS, et al. Prevalence of Helicobacter pylori in southern Indian controls and patients with gastroduodenal disease. J Gastroenterol Hepatol 1994;9:501-6.  Back to cited text no. 25
    
26.
Seery JP, Henshaw DJ, Sandhu PJ, Mather HM, Ahmad F, McNeil I. Helicobacter pylori infection and upper gastrointestinal pathology in a British immigrant Indian community. Eur J Gastroenterol Hepatol 1997;9:191-4.  Back to cited text no. 26
    
27.
Wyatt JI, Dixon MF. Campylobacter-associated chronic gastritis. Pathol Annu 1990;25 Pt 1:75-98.  Back to cited text no. 27
    
28.
Ota H, Katsuyama T, Nakajima S, El-Zimaity H, Kim JG, Graham DY, et al. Intestinal metaplasia with adherent Helicobacter pylori: A hybrid epithelium with both gastric and intestinal features. Hum Pathol 1998;29:846-50.  Back to cited text no. 28
    
29.
Jain A, Buddhiraja S, Khurana B, Singhal R, Nair D, Arora P, et al. Risk factors for duodenal ulcer in north India. Trop Gastroenterol 1999;20:36-9.  Back to cited text no. 29
    
30.
Huang JQ, Sridhar S, Hunt RH. Role of Helicobacter pylori infection and non-steroidal anti-inflammatory drugs in peptic-ulcer disease: A meta-analysis. Lancet 2002;359:14-22.  Back to cited text no. 30
    
31.
Katzenstein AL, Maksem J. Candidal infection of gastric ulcers. Histology, incidence, and clinical significance. Am J Clin Pathol 1979;71:137-41.  Back to cited text no. 31
    
32.
Parsonnet J, Gary DF, Vandersteen DP. Helicobacter pylori infection and the risk of gastric carcinoma. New Eng J med 1991;325:1127-31.  Back to cited text no. 32
    
33.
Matsukuma A, Mori M, Enjoji M. Sulphomucin-secreting intestinal metaplasia in the human gastric mucosa. An association with intestinal-type gastric carcinoma. Cancer 1990;66:689-94.  Back to cited text no. 33
    
34.
Lee BM, Jang JJ, Kim JS, You YC, Chun SA, Kim HS, et al. Association of Helicobacter pylori infection with gastric adenocarcinoma. Jpn J Cancer Res 1998;89:597-603.  Back to cited text no. 34
    
35.
Rugge M, Busatto G, Cassaro M, Shiao YH, Russo V, Leandro G, et al. Patients younger than 40 years with gastric carcinoma: Helicobacter pylori genotype and associated gastritis phenotype. Cancer 1999;85:2506-11.  Back to cited text no. 35
    
36.
Tatsuta M, Lishi H, Okuda S, Taniguchi H, Yokota Y. The association of Helicobacter pylori with differentiated-type early gastric cancer. Cancer 1993;72:1841-5.  Back to cited text no. 36
    
37.
Vandenborre KM, Ghillebert GL, Rutgeerts LJ, Geboes KR, Rutgeerts PJ, Verbanck JJ, et al. Hypertrophic lymphocytic gastritis with a gastric carcinoma. Eur J Gastroenterol Hepatol 1998;10:797-801.  Back to cited text no. 37
    
38.
Bayerdörffer E, Ritter MM, Hatz R, Brooks W, Ruckdeschel G, Stolte M. Healing of protein losing hypertrophic gastropathy by eradication of Helicobacter pylori--is Helicobacter pylori a pathogenic factor in Ménétrier's disease? Gut 1994;35:701-4.  Back to cited text no. 38
    
39.
Sipponen P, Kekki M, Siurala M. Age-related trends of gastritis and intestinal metaplasia in gastric carcinoma patients and in controls representing the population at large. Br J Cancer 1984;49:521-30.  Back to cited text no. 39
    
40.
Arora MM, Talwar OP. Intestinal Metaplasia, sulphomucins and endoscopic gastric mucosal biopsies; A histochemical study. Med J Armed Forces India 1991; 47:78-84.  Back to cited text no. 40
    
41.
Evrensel T, Manavoğlu O, Ozyardimci C, Gülten M, Nak SG, Yerci O. Helicobacter pylori and intestinal metaplasia. J Environ Pathol Toxicol Oncol 1996;15:215-9.  Back to cited text no. 41
    
42.
Eidt S, Stolte M. Prevalence of lymphoid follicles and aggregates in Helicobacter pylori gastritis in antral and body mucosa. J Clin Pathol 1993;46:832-5.  Back to cited text no. 42
    
43.
Schneller J, Gupta R, Mustafa J, Villanueva R, Straus EW, Raffaniello RD. Helicobacter pylori infection is associated with a high incidence of intestinal metaplasia in the gastric mucosa of patients at inner-city hospitals in New York. Dig Dis Sci 2006;51:1801-9.  Back to cited text no. 43
    
44.
Trindade LM, Menezes LB, de Souza Neta AM, Leite Rolemberg PC, Souza LD, Barreto ID, et al. Prevalence of Helicobacter pylori infection in samples of gastric biopsies. Gastroenterology Res 2017;10:33-41.  Back to cited text no. 44
    
45.
Venerito M, Vasapolli R, Rokkas T, Malfertheiner P. Helicobacter pylori and Gastrointestinal Malignancies. Helicobacter 2015;20 Suppl 1:36-9.  Back to cited text no. 45
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

 
Top
 
 
  Search
 
     Search Pubmed for
 
    -  Gupta AP
    -  Suryawanshi UD
    -  Kumbhalkar DT
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
   Abstract
  Introduction
   Materials and Me...
  Results
  Discussion
  Conclusion
   References
   Article Figures
   Article Tables

 Article Access Statistics
    Viewed257    
    PDF Downloaded3    

Recommend this journal