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Year : 2018  |  Volume : 21  |  Issue : 3  |  Page : 146-152

Intestinal metaplasia and glandular atrophy in patients with chronic gastritis in Ilorin

1 Department of Histopathology, Federal Medical Centre, Owo, Ondo State, Nigeria
2 Department of Pathology, University of Ilorin/University of Ilorin Teaching Hospital, Ilorin, Nigeria

Date of Web Publication4-Oct-2018

Correspondence Address:
Dr. David Eyitayo Ibikunle
Department of Histopathology, Federal Medical Centre, Owo, Ondo State
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DOI: 10.4103/smj.smj_29_17

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Background: Intestinal metaplasia and glandular atrophy are pre malignant conditions occurring as a complication of prolonged, untreated or poorly treated chronic gastritis. This study aims at detecting the presence and severity of intestinal and glandular atrophy. Method: A retrospective study of 316 cases meeting the inclusion criteria with a male to female ratio of 1.1:1 were enlisted into the study spanning a 5-year period. Results: Intestinal metaplasia was reported in 64 (20.2%) cases with majority 36 (56.3%) graded as mild intestinal metaplasia. Complete intestinal metaplasia was seen in 44(68.8%) and incomplete in 20(31.2%). Glandular atrophy was reported in 137(43.3%) cases with majority 97(70.8%) graded as mild. Patients that are 41 years and above were responsible for more than 70% of all cases of intestinal metaplasia and glandular atrophy. The result in this study is comparable to similar studies by sister institutions. Conclusion: It is our recommendation therefore that all patients that are 40 years and above with unresolving dyspepsia be referred to the gastroenterologist for a proper evaluation to prevent these complications and ultimately reduce the occurrence of gastric malignancies.

Keywords: Dyspepsia, glandular atrophy, intestinal metaplasia

How to cite this article:
Ibikunle DE, Kazeem Ibrahim OO, Abiodun Afolayan EO. Intestinal metaplasia and glandular atrophy in patients with chronic gastritis in Ilorin. Sahel Med J 2018;21:146-52

How to cite this URL:
Ibikunle DE, Kazeem Ibrahim OO, Abiodun Afolayan EO. Intestinal metaplasia and glandular atrophy in patients with chronic gastritis in Ilorin. Sahel Med J [serial online] 2018 [cited 2020 May 27];21:146-52. Available from: http://www.smjonline.org/text.asp?2018/21/3/146/242743

  Introduction Top

Intestinal metaplasia which is defined as the replacement of normal gastric mucosa by metaplastic epithelial cells and glandular atrophy defined as decrease or loss of glandular tissue characterized by mucosa thinning, have both been described as premalignant gastric lesions in which case early detection can be used to determine the patients at a high risk of developing gastric cancer.[1],[2]

Majority of patients from which these premalignant conditions were detected at histology usually present late to the clinic on account of unresolved dyspepsia for which they had been using home remedies and over the counter medications. Since it has been documented severally that the early detection of these changes in gastric epithelium can prevent the development of gastric malignancy, we therefore set out to review the prevalence of these premalignant conditions in the gastric biopsies of patients seen in the University of Ilorin Teaching Hospital (UITH).

The rate of glandular atrophy varies widely among various studies reviewed. In an earlier study of 57 cases, herein, Ilorin Badmos et al. reported a total incidence of 31.6%, while Oluwasola and Ogunbiyi in Ibadan reported 16.7%, Zhang in Japan, 36.8%, Atisook in Thailand, 11.6%, and Asaka in Japan, 82.9%, in Helicobacter pylori-positive patients and 9.8% in H. pylori-negative patients.[3],[4],[5] In another study by Ohkuma et al. in Japan, an increase in the risk of atrophy is seen in patients who are 60 years above, especially in those infected by H. pylori.[6] Atisook et al. reported glandular atrophy in 11.6% of their patients which is low but in keeping with trends observed in Thailand.[7]

The total frequency of intestinal metaplasia reported varies from study to study. The least reported was 1.7% by Holcomb et al., 8.8% by Badmos et al., 9.4% by Oluwasola and Ogunbiyi, and 8.2% by Atisook et al.[4],[5],[7],[8] Higher values of 15.2% have been reported by Al Knawy et al. and 43.1% in H. pylori-positive patients by Asaka et al.[9],[10] In the study by Badmos et al. in Ilorin, intestinal metaplasia was graded as mild and moderate in 3.5% and 5.3%, respectively, and no marked case was reported. There were 3 cases of Type 1 and 2 cases of Type 2 intestinal metaplasia while all the 8 cases reported in Ibadan by oluwasola were mild grade and Type 1.[4],[5] In the study by Al-Knawy et al., no sex predilection was found, and Type 1 intestinal metaplasia was found in 59.3% while Type 2 and Type 3 are 26.3 and 14%, respectively.[10] Atisook et al. in a nationwide study involving 3776 patients in Thailand also reported that Type 1 intestinal metaplasia is most common.[7] Ozdil et al. in Turkey reported from the study of 2353 patients that the risk of intestinal metaplasia increases with age.[11]

  Materials and Methods Top

This is a 5-year (January 1, 2006–December 31, 2010) retrospective review of all gastric endoscopic biopsies taken from dyspeptic patients in UITH, Ilorin.

All records of gastric endoscopic biopsies were retrieved from the surgical pathologic register. Patients' biodata (such as sex and age) and other clinical information (such as presenting complaints, endoscopic findings, sites, and number of biopsies taken) were extracted from the request cards. Where necessary, patients' case folders were retrieved for additional information. All the corresponding hematoxylin and eosin (H and E)-stained sections of cases were reviewed.

Paraffin wax-embedded tissue blocks of cases with broken, damaged, or faded slides and those requiring histochemical stains were retrieved from the tissue block bank, and fresh sections were cut and stained for H and E to demonstrate most basic microscopic features such as chronic inflammation and inflammatory activity and modified Giemsa to demonstrate the presence and the severity of colonization by H. pylori. When intestinal metaplasia is present, alcian blue stain with periodic acid–Schiff (PAS) stain at pH 2.5 was used to confirm the presence, type, and severity of intestinal metaplasia.

Methods of analysis

All H and E-stained slides were reviewed according to the Sydney system and results presented in words and tables.[3]

Data obtained from this study were analyzed using simple statistical analysis. Photomicrographs of slides are presented where necessary.

Ethical consideration

Permission was obtained from the Ethical Review Committee of UITS, Ilorin, for this study.

Sample size

All cases who met the inclusion criteria within the period under review were studied.

Exclusion criteria

The followings were excluded from the cohort:

  1. All endoscopic gastric biopsies with incomplete data (such as age, sex, and endoscopic findings) from the request cards, case notes, and missing tissue blocks
  2. All endoscopic gastric biopsies that did not include the muscularis mucosae and regarded as inadequate sample
  3. Cases with gastric neoplasm.

  Results Top

A total of 10,225 surgical biopsy specimens were received in the Department of Pathology of UITH, Ilorin, during the 5-year under review. Out of these cases, 372 (3.64%) were gastric biopsies from patients with dyspeptic symptoms. Chronic gastritis was reported in 316 (84.9%) cases and was thus included in the study. The remaining 56 (15.1%) were excluded on account of gastric carcinoma in 26 (7%) cases, normal histology in 13 (3.5%) cases, inadequate sampling in 12 (3.2%) cases, and missing tissue blocks in 5 (1.3%) cases.

Sex and age distribution of patients

There were 170 (53.8%) males and 146 (46.2%) females giving a male-to-female ratio of 1.1:1. The youngest age recorded was 5 years, the oldest age recorded was 93 years, and the modal age range was 41–50 years (26.6%). Patients aged 41 years and above were responsible for 71.1% of the cases.

Topographic pattern of the biopsies

Majority of the biopsies, i.e. 221 (69.9%) were taken from both the corpus and pyloric antrum while 66 (20.9%) biopsies were taken solely from the pyloric antrum and 29 (9.2%) from the corpus alone. The pyloric antrum was biopsied in 287 (90.8%) cases.

Graded histologic variables in Sydney classification of chronic gastritis

The various graded histologic variables were scored and graded in each case using the Sydney system score scale [Appendix A][20],[21] with a guided visual score [Appendix B]. Chronic inflammation was the most common graded variable seen in all 316 (100%) cases, followed by inflammatory activity, 207 (65.5%), H. pylori colonization, 171 (54.1%), and glandular atrophy, 137 (43.4%), and the least common was intestinal metaplasia in 64 (20.2%) cases.

Glandular atrophy

In this study, glandular atrophy [Figure 1] was diagnosed in 137 (43.3%) patients composed of 86 (62.8%) males and 51 (37.2%) females. The peak incidence of glandular atrophy occurred in the age group of 51–60 years with 43 (31.4%) cases, patients aged 41 years and above accounting for 97.8% (134) cases. No case of glandular atrophy was seen in patients <30 years. In the grading of glandular atrophy, there were 97 (30.7%) cases of mild glandular atrophy, 32 (10.1%) cases of moderate glandular atrophy, and 8 (2.5%) cases of marked glandular atrophy [Table 1].
Figure 1: Gastric biopsy showing marked glandular atrophy in the pyloric antrum of a 65-year-old male characterized by marked reduction of glands and low glandstromal ratio. Only two glands (arrows) are visible in this field (H and E, ×100)

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Table 1: Grades of glandular atrophy within the age group

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Intestinal metaplasia

A total of 64 (20.2%) cases with intestinal metaplasia [Figure 2] and [Figure 3] were diagnosed in dyspeptic patients with 38 (59.4%) males and 26 (40.6%) females. Patients within the age group of 51–60 years represented the modal age group with 19 (29.7%) cases, patients who were 41 years and above had 90.6% of cases, and just one (1.6%) case was diagnosed in patients who were <39 years old. The metaplastic changes were graded as mild, moderate, and marked in 36 (11.4%), 21 (6.6%), and 7 (2.2%) cases, respectively [Table 2]. Out of the 64 cases with intestinal metaplasia, 44 (68.8%) were of the complete type while the remaining 20 (31.2%) were of the incomplete type.
Figure 2: Gastric biopsy showing marked intestinal metaplasia in a 50-year-old man characterized by colonic-type epithelial lining of the glands with goblet cells (arrows) (H and E, ×400)

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Figure 3: Gastric biopsy showing complete intestinal metaplasia in a 66-year-old woman characterized by a positive alcian blue/periodic acid–Schiff staining of the intestinal-type epithelium (arrows). Alcian blue/periodic acid–Schiff at pH 2.5, ×100

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Table 2: Grades of intestinal metaplasia within the age group

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  Discussion Top

The role of upper gastrointestinal (UGI) endoscopy and biopsy in the management of patients with dyspepsia cannot be overemphasized. In this study, gastric biopsies from dyspeptic patients were reviewed. The Sydney system of reporting chronic gastritis in dyspeptic patients which has made the classification and evaluation on histology objective, reproducible, and useful to the pathologist, the gastroenterologist, and more importantly the patient in their management was utilized.[3]

Total number of biopsies

A total of 372 (3.6%) out of 10,225 surgical biopsies, registered in the Department of Pathology, were endoscopic gastric biopsies from dyspeptic patients submitted for histological diagnosis over the study period. This frequency is higher than 0.6% reported in Ibadan by Oluwasola and Ogunbiyi.[5] Before 2006, the only form of gastric biopsies received in the Department of Pathology of UITH was obtained by laparotomy because there were no facilities and workforce for UGI endoscopy and biopsy and as such patients were referred to other centers.

Age and sex distribution of patients with dyspepsia

There is a slight male preponderance in this study. There were 191 (53.8%) males and 164 (46.2%) females giving a male-to-female ratio of 1.2:1. This ratio is similar to the 1.1:1 found the studies by Badmos et al. in Ilorin, Hameed et al. in Lagos and Al-Knawy et al. in Abha, Saudi Arabia.[4],[10],[12] Most other studies showed that there is no significant sex predilection in dyspepsia as highlighted in this study.

Patients in this study were between 5 and 93 years old with those in their fifth decade of life and above constituting 86.3% of all biopsies taken. This is in tandem with the studies by Badmos et al., 15–85 years with peak at the fifth decade, Guindy and Ghoraba, 25–63 years with peak at the fifth decade, and Khan, 2–60 years.[4],[13],[14] Although there is a wide range of age reported, the peak falls at about the generally acceptable age of 45 years for which an endoscopy and biopsy are recommended in the management of dyspepsia.

There are, however, newer indications from other studies that this age may be reviewed upward to 55 years, especially in the Western society; no absolute age cutoff is feasible, due to the presence of gastric cancer in those <55 years in this study.[15] The fact that patients younger than 45 years had endoscopy and biopsy in this study is not unconnected to the fact that diagnosis needs to be verified and treatment instituted on time in cases of unresolved dyspepsia as this may be associated with H. pylori infection which occurs in Nigerians as early as childhood or the presence of an early gastric cancer.[16],[17],[18]

Topographic distribution of the biopsies

In this study, 69.9% of biopsies were taken from the antrum and corpus, 9.2% from the corpus alone, and 20.9% from the pyloric antrum alone. A large majority, i.e. 287 (90.8%) had the pyloric antrum as a component of the biopsy. This finding is similar to the study by Badmos et al.[4] in which 79% of all biopsies were from the pyloric antrum. This result differs significantly from the study by Ohkuma et al.[6] where equal numbers (50%) of biopsies were taken from the corpus and antrum. The effects of chronic inflammation, intestinal metaplasia, and glandular atrophy are seen more in the pyloric antrum than in the oxyntic mucosa. It is expedient, therefore, to have biopsies from both the antral and oxyntic mucosa for complete and adequate evaluation of biopsies.[5] The number of corpus only biopsies in this study (9.3%) is, however, lower than the one in the study by Badmos et al. (21%).[4] The biopsy from the corpus becomes very useful in patients who have been commenced on anti-H pylori regimen as the organism becomes less apparent in the pyloric antrum compared to the corpus. Therefore, the percentage of antral biopsy in this study is highly significant in the evaluation of glandular atrophy and intestinal metaplasia.

Glandular atrophy

The rate of glandular atrophy in this study was 43.4%. This value is much higher than other values reported in studies by Badmos et al., 31.6%, Oluwasola and Ogunbiyi, 16.7%, Zhang et al., 36.8%, and Atisook, 11.6%. The only study with a higher frequency, 82.9%, of atrophy was the study by Asaka et al. in Japan where only H. pylori positive cases were studied. Mild atrophy was the most common grade, 29.5%, followed by moderate, 9.7%, and marked, 2.4%. This is similar to the grading by Badmos et al. where mild was 19.3%, moderate was 12.3%, and no single case of marked atrophy was reported.

The peak age of atrophy in this study was 51–60 years, and no single case of atrophy was seen before the age of 30 years. This peak takes a decade after the peak of infection with H. pylori which has been implicated as a major etiological factor in the pathogenesis of glandular atrophy.

Asaka et al. reported 9.4% atrophy in patients <20 years; however, this value increases to 70% in those who are 60 years and above. In the study by Ohkuma et al., patients who are 60 years and above and those who are positive for H. pylori have a significantly increased risk of developing glandular atrophy.[6],[9]

There is a statistically significant relationship between H. pylori colonization and glandular atrophy which has been alluded in previous studies; hence, glandular atrophy is not regarded as a function of aging as once opined but more of complications and sequela of H. pylori infection.[6],[9],[19]

Intestinal metaplasia

Intestinal metaplasia was not uncommon in this study with a rate of 20.2%. This frequency is higher than the 1.7% by Holcombe and Adeyemi, 8.2% by Atisook et al., 8.8% by Badmos et al., 9.4% by Oluwasola and Ogunbiyi, and 15.2% by Al Knawy.[4],[5],[7],[8],[10] The increase in the frequency reported in this study is as a result of histochemical stains (PAS, alcian blue) used which has increased the sensitivity with which intestinal metaplasia is identified. Mild grade was most common with 10.9%.

Mild grade, 9.4%, was also most common in the Oluwasola and Ogunbiyi's study; however, moderate grade was more than mild in the study by Badmos et al. The peak age of incidence of intestinal metaplasia is similar to that of glandular atrophy, 51–60 years. It is low (1.6%) in patients who are <30 years with majority (90.6%) occurring in patients older than 40 years similar to the study by Ozdil et al. in Turkey.[11] As stated earlier, the slight reduction in the age group of 70 years and above may be as a result of the effect of drug therapy and the ability of host immune status to wall off H. pylori.

Type 1 intestinal metaplasia was most common in this study with 68.8%, similar to 60% by Badmos et al. and 59% by Al Knawy as against the Type 2. However, in the study by Oluwasola and Ogunbiyi in Ibadan, 100% showed Type 1 intestinal metaplasia. The Type 1 intestinal metaplasia is not a risk factor in predisposition to gastric malignancy like Type 2, hence the need to subclassify.

Intestinal metaplasia is a common sequela of chronic gastritis of all causes which increases in prevalence with disease duration. Although areas that are affected by intestinal metaplasia are usually ignored when grading the degree of H. pylori, a statistically significant relationship [Table 2] was found to exist between these two parameters at varying degree. Intestinal metaplasia is almost constant sequelae of chronic infection with H. pylori. This is obvious from the fact that 61 (35.7%) of all H. pylori positive cases have intestinal metaplasia. This is comparable to a similar study by Al-Knawy in Saudi Arabia where intestinal metaplasia was found in 35.7% of cases with H. pylori.[10]

  Conclusion Top

Chronic gastritis presenting as dyspepsia is a common presentation in everyday clinical practice, and the association between H. pylori colonization of the gastric epithelium and gastric premalignant lesions such as glandular atrophy and intestinal metaplasia has also been established. Chronic gastritis and gastric malignancies are major underlining diseases in patients presenting with dyspepsia as seen in this study. Premalignant conditions are seen in 22% (intestinal metaplasia) and 40% (glandular atrophy) of patients, and they peak at about the fifth decade of life which is about a decade earlier than gastric malignancies which are more common in the sixth decade.

This study has demonstrated the great value of UGI endoscopy and biopsy in the diagnosis and evaluation of patients with chronic gastritis, especially in the prevention of gastric malignancies.


The authors would like to thank Late Mrs. Omole Adewumi for helping with the preparation of the H and E and special stain slides.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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Zhang C, Yamada N, Wu YL, Wen M, Matsuhisa T, Matsukura N, et al. Comparison of Helicobacter pylori infection and gastric mucosal histological features of gastric ulcer patients with chronic gastritis patients. World J Gastroenterol 2005;11:976-81.  Back to cited text no. 3
Badmos KB, Olokoba AB, Ibrahim OO, Abubakar-Akanbi SK. Histomorphology of Helicobacter pylori associated chronic gastritis in Ilorin. Afr J Med Med Sci 2010;39:37-40.  Back to cited text no. 4
Oluwasola AO, Ogunbiyi JO. Chronic gastritis and Helicobacter pylori infection in University College Hospital Ibadan, Nigeria – A study of 85 fibre optic gastric biopsies. Niger J Med 2004;13:372-8.  Back to cited text no. 5
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  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2]


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