Journal of Surgical Oncology 43:101-105 (1990)
Occurrence of Intestinal Metaplasia of the Stomach in Thai Patients With Gastritis, Benign Ulcer, and Gastric Cancer PAISAL PONGCHAIRERKS, MD, PANAS CHALERMSANYAKORN, MD, AND MONGKOL TANJAPATKUL, MD From the Departments of Surgery (P.P., M.T.1 and Pathology (P.C.), Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
Pathological sections of gastrectomized specimens of 74 patients with benign gastric ulcer and 79 with gastric cancer were reviewed. Intestinal metaplasia was found in 26 specimens with benign ulcer (35.1%) and in 43 with cancer (54.4%), a difference that is statistically significant. Further analysis of age groups showed that rate of occurrence of metaplasia in cancer patients older than 60 years was 70.3%, which was significantly higher than that of their younger counterparts (40.5%) and of patients with benign ulcer of either age group. A survey was also conducted by taking biopsies of mucosa of antrum and body of the stomach of 250 patients who underwent gastroscopic examinations. Acute and chronic gastritis was found in 22 and 156 patients, respectively. Intestinal metaplasia was found to be associated with acute gastritis in 2 (9.1%) and with chronic gastritis in 25 (16%) patients. In conclusion, intestinal metaplasia was associated with gastric cancer in patients who were older than 60 years in a significantly higher proportion than it was with benign gastric ulcer and gastritis among Thai patients. ~
KEY WORDS: pathology, gastrectomized specimens, endoscopic biopsy, gastric mucosa
INTRODUCTION Although the incidence of gastric cancer has been decreasing over the last 30 years in many parts of the world, it is still a common malignant disease with rather poor prognosis, except when treatment can be given in its early stage [ 11. If persons with higher-risk factors for developing this type of cancer can be identified and closely followed up, the possibility of diagnosing gastric cancer at its early phase will be increased. A close correlation between gastric cancer and intestinal metaplasia has been suggested [2]. Foci of carcinoma of the human stomach have been found to be surrounded by areas of intestinal metaplasia [3]. Epidemiologic studies also showed higher incidences of intestinal metaplasia in high-risk groups of the population [4-61. Moreover, intestinal metaplasia could be induced in rats by chemical carcinogens that induced gastric cancer at the same location in the stomach [7]. In fact, the proliferation of 0 1990 Wiley-Liss, Inc.
mucosal cells of the metaplastic glands has been found by [3H]thymidine autoradiography to start from the lower portion of glands rather than from the neck area as in normal gastric glands [S], indicating an altered proliferative behavior. Biochemical compositions and properties of their cytoplasm were also shown to be quite different from normal mucosal cells by lectin histochemical study [9]. These findings pointed toward alterations in almost every aspect of cells, not jusl in morphology alone. Therefore, intestinal metaplasia is thought possibly to be the beginning of neoplastic change of the gastric mucosa. Accepted for publication September 19, 1989. Address reprint requests to Dr. Paisa1 Pongchairerks, Department of Surgery, Ramathibodi Hospital, Rama VI Road, Bangkok 10400, Thailand. This work has been supported in part by the Ramathibodi Foundation Research Fund 1986.
102
Pongchairerks et al.
Fig. I. (Top figure) Intestinal metaplasia. Gastric mucosa showing mixture of normal gastric glands and glands with intestinal metaplasia with numerous goblet cells. The lamina propria is infiltrated with chronic inflammatory cells. H & E. X 100.
Fig. 2. (bottom figure) Intestinal metaplasia. Higher power showing gastric glands with goblet cells and well-defined brush-border of the epithelial cells. H & E, X400.
In Thailand, despite the fact that the stomach is one of the ten leading cancer sites, the importance of intestinal metaplasia in pathological sections of the stomach is usually overlooked since symptoms are usually not attributed to it. Therefore, not even a crude figure as to its incidence in the population as a whole, in patients with gastric cancer or in any other gastric conditions, is available in Thailand. It is the intention of this study to find
some figures of the association between these microscopic changes and various common pathologic findings of the stomach in Thai patients.
MATERIALS AND METHODS The study consisted of 2 parts: a retrospective review and a cross-sectional survey conducted in the Departments of Surgery and Pathology, Ramathibodi Hospital,
Gastric Intestinal Metaplasia in Thailand TABLE 1. Age and Sex Distribution of Patients With Gastric Cancer and Benign Ulcer Studied by Gastrectomized Specimens Age in years (%) Disease
Total cases
Cancer
79
Ulcer
74
60 37 (46.8) 32 (43.2)
Sex (%)
M 45 (57.0) 49 (66.2)
TABLE 111. Microscopic Findings of Biopsied Specimens Taken Via the Gastroscope in 246 Patients and Their Age and Sex Distribution Age in years (%)
F 34 (43.0) 25 (33.8)
103
Sex (%)
Total
60
M
F
Normal mucosa
68
51 (75.0)
Chronic gastritis
156
17 (25.0) 41 (26.3) 5 (22.7)
30 (44.1) 98 (62.8) 13 (59. I )
38 (55.9) 58 (37.2) 9 (40.9)
Finding
115
153
Acute gastritis
(73.7) 17 (77.3)
22 246
TABLE 11. Occurrence of Intestinal Metaplasia in Gastrectomized Specimens With Gastric Cancer and Benign Ulcer Disease
Total cases
Intestinal metaplasia
Percent
Cancer Ulcer
79 74
43 26
54.4" 35. I *
" P < .02 (chi-square test)
TABLE IV. Occurrence of Intestinal Metaplasia Associated With Chronic and Acute Gastritis in Biopsied Specimens Finding Chronic gastritis Acute .gastritis
Total cases
Intestinal metaplasia
Per cent
156 22
25 2
16.0" 9.1"
" P > . I (Fisher's exact test).
Bangkok, Thailand. In the retrospective study, pathological sections of gastrectomized specimens of 79 gastric cancer and 74 benign gastric ulcer patients from 1984 to 1986 were reviewed, and the association with intestinal metaplasia in the gastric mucosa was noted in each case. In the cross-sectional survey, biopsies of gastric mucosa were taken from the antrum and body of 250 patients who were examined by gastroscopy for various reasons, mostly epigastralgia and gastrointestinal bleeding. Biopsies were taken from the areas that did not show any ulcer. The patients with gross and microscopic cancer were excluded. The specimens were fixed with formalin, and paraffin sections were made and stained with hematoxylin-eosin. Intestinal metaplasia was defined by the appearance of goblet cells with or without Paneth's cells in the gastric mucosa (Figs. 1,2).
RESULTS Retrospective Study Table I shows the age group and sex distribution of patients with gastric cancer and benign ulcer whose pathological sections were reviewed. Patients who were younger and older than 60 years of age were about the same in number. The association of intestinal metaplasia with gastric cancer and benign ulcer is shown in Table TI. Intestinal metaplasia was found in 54.4% of gastric cancer specimens and in 35.1% of benign gastric ulcers. This difference was statistically significant. Cancer patients who were 60 years or older had a much more frequent association of intestinal metaplasia (70.3%) as compared to their younger counterparts
whose occurrence of intestinal metaplasia was only 40.5% (Table V). Notably, the percentages of cases with intestinal metaplasia were quite similar in patients with cancer who were younger than 60 years and those who had benign ulcers in young as well as old age groups.
Cross-Sectional Survey Four of the 250 cases in whom biopsies of the antral and body mucosa were taken had carcinoma in their stomach and were excluded. The microscopic findings of the remaining cases are shown in Table 111. Intestinal metaplasia could be found in both acute and chronic gastritis. As shown in Table IV, the difference was not statistically significant although the number of cases with acute gastritis was very small. Patients older and younger than 60 years of age with chronic gastritis did not have a significantly different occurrence of metaplastic changes (Table V). DISCUSSION It is well known that the incidence of gastric adenocarcinoma varies greatly in different countries, and even in different groups of the population in the same country. Correa and his colleagues [6]did an endoscopic survey in a group of people who were found to have a high risk and another group with low risk of developing gastric cancer in the city of Narino in Colombia and found the prevalence of intestinal metaplasia in the stomach to be 22% and 10.756, respectively. Our similar survey showed the occurrence of this condition in 27 of 246 patients (10.9%) examined endoscopically , which is
104
Pongchairerks et al. TABLE V. Occurrences of Intestinal Metaplasia in Patients With Gastric Cancer, Benign Ulcer, and Chronic Gastritis According to Ape Groups Diseases Retrospectiveb Cancer
Total cases Intestinal metaplasia
P -values*
Ulcer
60 vears
42 17 (40.5)“
37 26 (70.3) .I
60 vears 41
1I 5
15
10
(13.0)
(24.3)
> .05
“The No. in parentheses indicate percentage of the total cases in each age groups. ’Method of study. *P-values of differences between patients younger and older than 60 years of age who had the same disease (chi-square test)
very close to the low-risk group in Narino. In Japan, where gastric cancer is most prevalent, an autopsy study showed intestinal metaplasia in 41.5% of grossly normal looking stomachs [ 101. Several groups of investigators have reported a high prevalence of intestinal metaplasia in the stomach of patients with gastric adenocarcinoma compared to benign gastric conditions [4,1 I , 121. Segura and Montero [ 1 11 in Spain found the prevalence of intestinal metaplasia to be 80.7% in benign ulcers and 97.1 % in cancer. The figure from Japan also showed a very high prevalence [ 101. Our result agrees more favourably with those reported from rather low-risk areas of gastric cancer. Filipe and his colleagues [ 121 surveyed three centers in London, Reims, and Paris and found the prevalence to be 65% in gastric cancer, 36% in benign gastric ulcer, and 22% in gastritis. Our figures are 54.4%, 35.1%, and 16%, respectively . The results of this study showed that intestinal metaplasia is found more frequently in gastric cancer than in benign gastric ulcer and gastritis. Patients with benign ulcers in any age group and patients with gastric cancer in the younger age group had similar rates of association with intestinal metaplasia in their stomach. Patients with gastric cancer who were older than 60 years of age had a significantly higher rate of metaplasia. This observation, including the figures of the percentage of occurrence in each gastric condition and age groups (Tables 111, IV), is quite similar to what Imai et al. reported in 1971 for American patients with gastric cancer, ulcer, and gastritis in Minnesota but is different from the Japanese whose prevalence of metaplasia in older age groups was found to be significantly higher in any of the three gastric conditions than their younger counterparts 141. The observation cited in this study is important, since it implies that finding intestinal metaplasia in the stomach of patients older than 60 years of age should arouse a suspicion of cancer and thus indicate a more careful
scrutiny and follow-up endoscopic examination with biopsy. This type of patient should not be just “reassured” when a cancer is not found in the initial workup and allowed to be lost to follow-up or to wait until obvious symptoms occur. Repetition of gastroscopy should be recommended if their symptoms continue no matter how mild they are. If a benign ulcer or even gastritis is present with intestinal metaplasia in a biopsy, it should definitely be repeated after a certain period of treatment. Any abnormal finding should be recorded and biopsied. In any event, it should be kept in mind that this type of patient may have some risk factors for developing gastric cancer, and proper attention should be paid to them.
ACKNOWLEDGMENTS The authors would like to thank Dr. Prasert Trairatvorakul, Dr. Sopon Jirasiritham, Dr. Chakkrapan Urnorases, and Dr. Suriya Chakkapark for inclusion of many of their patients in this study. They also wish to thank to Mrs. Suteera Uyathumrangsit who gave good support as an endoscopic assistant during the whole period of the study. Lastly, they appreciate all the valuable advice Prof. Sira Bunyarattavej has given in the revision of the manuscript. REFERENCES 1. Yamada E, Nakazato M, Koike A , Suzuki K, Kato K, Kito T: Surgical results for early gastric cancer. Int Surg 597-14, 1974.
2. Morson BC: Carcinoma arising from areas of intestinal metaplasia in gastric mucosa. Br J Cancer 9:377-385, 1955. 3. Nakamura K, Sugano H, Takagi K: Carcinoma of the stomach in incipient phase: Its histogenesis and histological appearances. Gann 59:251-258, 1968. 4. Imai T, Kubo T, Watanabe H: Chronic gastritis in Japanese with reference to high incidence of gastric carcinoma. JNCI 47: 179195, 1971. 5 . Con-ea P, Cuello C, Duque E: Carcinoma and intestinal metaplasia of the stomach in Colombian migrants. JNCI 44:297-306, 1970. 6. C o m a P, Cuello C, Duque E, Burbano LC, Garcia FT, Bolanos
Gastric Intestinal Metaplasia in Thailand 0, Brown C , Haenszel W: Gastric cancer in Colombia. 111. Natural history of precursor lesions. JNCl 57: 1027-1035, 1976. 7. Matsukura N, Kawachi T, Sasajima K, Sano T, Sugimura T, Hirota T: Induction of intestinal metaplasia in the stomach of rats by N-Methyl-N'-Nitro-N-Nitrosoguanidine. JNCI 61: 141-143, 1978. 8. Hashimoto M , Tokunaga A, Nishi K , Wada M, Masumori K , Kumagae Y , Numajiri H, Matsukura N , Oshiyasu M, Tanaka N, Shirota A, Asano G: ['HI Thymidine autoradiographic and alkaline phosphatase histochemical studies of intestinal metaplasia of the human stomach. Histochem J 15:953-959, 1983. 9. Pongchairerks P, Matsukura N, Tokunaga A, Tanaka N, Onda M, Miki M, Asano G, Hirota T: Lectin histochemical studies on
105
gastric intestinal metaplasia with Ulex europaeus agglutinin-I, Dolochos biflorus and Peanut agglutinins in comparison with gastric and small and large intestinal mucosa. Acta Histochem Cytochem. 20:147-161, 1987. 10. lmai T, Maruyama H: Time trend in the prevalence of intestinal metaplasia in Japan. Cancer 52353-361, 1983. 11. Segura DI, Montero C: Histochemical characterization of different types of intestinal metaplasia in gastric mucosa. Cancer 52: 498-503, 1983. 12. Filipe MI, Bogomoletz W, Dawson P, Fabiani B, Potet F: Intestinal metaplasia subtypes in the assessment of gastric cancer risk. A multicenter prospective study. Gut 24:A974, 1983.
Occurrence of Intestinal Metaplasia of the Stomach in Thai Patients With Gastritis, Benign Ulcer, and Gastric Cancer PAISAL PONGCHAIRERKS, MD, PANAS CHALERMSANYAKORN, MD, AND MONGKOL TANJAPATKUL, MD From the Departments of Surgery (P.P., M.T.1 and Pathology (P.C.), Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
Pathological sections of gastrectomized specimens of 74 patients with benign gastric ulcer and 79 with gastric cancer were reviewed. Intestinal metaplasia was found in 26 specimens with benign ulcer (35.1%) and in 43 with cancer (54.4%), a difference that is statistically significant. Further analysis of age groups showed that rate of occurrence of metaplasia in cancer patients older than 60 years was 70.3%, which was significantly higher than that of their younger counterparts (40.5%) and of patients with benign ulcer of either age group. A survey was also conducted by taking biopsies of mucosa of antrum and body of the stomach of 250 patients who underwent gastroscopic examinations. Acute and chronic gastritis was found in 22 and 156 patients, respectively. Intestinal metaplasia was found to be associated with acute gastritis in 2 (9.1%) and with chronic gastritis in 25 (16%) patients. In conclusion, intestinal metaplasia was associated with gastric cancer in patients who were older than 60 years in a significantly higher proportion than it was with benign gastric ulcer and gastritis among Thai patients. ~
KEY WORDS: pathology, gastrectomized specimens, endoscopic biopsy, gastric mucosa
INTRODUCTION Although the incidence of gastric cancer has been decreasing over the last 30 years in many parts of the world, it is still a common malignant disease with rather poor prognosis, except when treatment can be given in its early stage [ 11. If persons with higher-risk factors for developing this type of cancer can be identified and closely followed up, the possibility of diagnosing gastric cancer at its early phase will be increased. A close correlation between gastric cancer and intestinal metaplasia has been suggested [2]. Foci of carcinoma of the human stomach have been found to be surrounded by areas of intestinal metaplasia [3]. Epidemiologic studies also showed higher incidences of intestinal metaplasia in high-risk groups of the population [4-61. Moreover, intestinal metaplasia could be induced in rats by chemical carcinogens that induced gastric cancer at the same location in the stomach [7]. In fact, the proliferation of 0 1990 Wiley-Liss, Inc.
mucosal cells of the metaplastic glands has been found by [3H]thymidine autoradiography to start from the lower portion of glands rather than from the neck area as in normal gastric glands [S], indicating an altered proliferative behavior. Biochemical compositions and properties of their cytoplasm were also shown to be quite different from normal mucosal cells by lectin histochemical study [9]. These findings pointed toward alterations in almost every aspect of cells, not jusl in morphology alone. Therefore, intestinal metaplasia is thought possibly to be the beginning of neoplastic change of the gastric mucosa. Accepted for publication September 19, 1989. Address reprint requests to Dr. Paisa1 Pongchairerks, Department of Surgery, Ramathibodi Hospital, Rama VI Road, Bangkok 10400, Thailand. This work has been supported in part by the Ramathibodi Foundation Research Fund 1986.
102
Pongchairerks et al.
Fig. I. (Top figure) Intestinal metaplasia. Gastric mucosa showing mixture of normal gastric glands and glands with intestinal metaplasia with numerous goblet cells. The lamina propria is infiltrated with chronic inflammatory cells. H & E. X 100.
Fig. 2. (bottom figure) Intestinal metaplasia. Higher power showing gastric glands with goblet cells and well-defined brush-border of the epithelial cells. H & E, X400.
In Thailand, despite the fact that the stomach is one of the ten leading cancer sites, the importance of intestinal metaplasia in pathological sections of the stomach is usually overlooked since symptoms are usually not attributed to it. Therefore, not even a crude figure as to its incidence in the population as a whole, in patients with gastric cancer or in any other gastric conditions, is available in Thailand. It is the intention of this study to find
some figures of the association between these microscopic changes and various common pathologic findings of the stomach in Thai patients.
MATERIALS AND METHODS The study consisted of 2 parts: a retrospective review and a cross-sectional survey conducted in the Departments of Surgery and Pathology, Ramathibodi Hospital,
Gastric Intestinal Metaplasia in Thailand TABLE 1. Age and Sex Distribution of Patients With Gastric Cancer and Benign Ulcer Studied by Gastrectomized Specimens Age in years (%) Disease
Total cases
Cancer
79
Ulcer
74
60 37 (46.8) 32 (43.2)
Sex (%)
M 45 (57.0) 49 (66.2)
TABLE 111. Microscopic Findings of Biopsied Specimens Taken Via the Gastroscope in 246 Patients and Their Age and Sex Distribution Age in years (%)
F 34 (43.0) 25 (33.8)
103
Sex (%)
Total
60
M
F
Normal mucosa
68
51 (75.0)
Chronic gastritis
156
17 (25.0) 41 (26.3) 5 (22.7)
30 (44.1) 98 (62.8) 13 (59. I )
38 (55.9) 58 (37.2) 9 (40.9)
Finding
115
153
Acute gastritis
(73.7) 17 (77.3)
22 246
TABLE 11. Occurrence of Intestinal Metaplasia in Gastrectomized Specimens With Gastric Cancer and Benign Ulcer Disease
Total cases
Intestinal metaplasia
Percent
Cancer Ulcer
79 74
43 26
54.4" 35. I *
" P < .02 (chi-square test)
TABLE IV. Occurrence of Intestinal Metaplasia Associated With Chronic and Acute Gastritis in Biopsied Specimens Finding Chronic gastritis Acute .gastritis
Total cases
Intestinal metaplasia
Per cent
156 22
25 2
16.0" 9.1"
" P > . I (Fisher's exact test).
Bangkok, Thailand. In the retrospective study, pathological sections of gastrectomized specimens of 79 gastric cancer and 74 benign gastric ulcer patients from 1984 to 1986 were reviewed, and the association with intestinal metaplasia in the gastric mucosa was noted in each case. In the cross-sectional survey, biopsies of gastric mucosa were taken from the antrum and body of 250 patients who were examined by gastroscopy for various reasons, mostly epigastralgia and gastrointestinal bleeding. Biopsies were taken from the areas that did not show any ulcer. The patients with gross and microscopic cancer were excluded. The specimens were fixed with formalin, and paraffin sections were made and stained with hematoxylin-eosin. Intestinal metaplasia was defined by the appearance of goblet cells with or without Paneth's cells in the gastric mucosa (Figs. 1,2).
RESULTS Retrospective Study Table I shows the age group and sex distribution of patients with gastric cancer and benign ulcer whose pathological sections were reviewed. Patients who were younger and older than 60 years of age were about the same in number. The association of intestinal metaplasia with gastric cancer and benign ulcer is shown in Table TI. Intestinal metaplasia was found in 54.4% of gastric cancer specimens and in 35.1% of benign gastric ulcers. This difference was statistically significant. Cancer patients who were 60 years or older had a much more frequent association of intestinal metaplasia (70.3%) as compared to their younger counterparts
whose occurrence of intestinal metaplasia was only 40.5% (Table V). Notably, the percentages of cases with intestinal metaplasia were quite similar in patients with cancer who were younger than 60 years and those who had benign ulcers in young as well as old age groups.
Cross-Sectional Survey Four of the 250 cases in whom biopsies of the antral and body mucosa were taken had carcinoma in their stomach and were excluded. The microscopic findings of the remaining cases are shown in Table 111. Intestinal metaplasia could be found in both acute and chronic gastritis. As shown in Table IV, the difference was not statistically significant although the number of cases with acute gastritis was very small. Patients older and younger than 60 years of age with chronic gastritis did not have a significantly different occurrence of metaplastic changes (Table V). DISCUSSION It is well known that the incidence of gastric adenocarcinoma varies greatly in different countries, and even in different groups of the population in the same country. Correa and his colleagues [6]did an endoscopic survey in a group of people who were found to have a high risk and another group with low risk of developing gastric cancer in the city of Narino in Colombia and found the prevalence of intestinal metaplasia in the stomach to be 22% and 10.756, respectively. Our similar survey showed the occurrence of this condition in 27 of 246 patients (10.9%) examined endoscopically , which is
104
Pongchairerks et al. TABLE V. Occurrences of Intestinal Metaplasia in Patients With Gastric Cancer, Benign Ulcer, and Chronic Gastritis According to Ape Groups Diseases Retrospectiveb Cancer
Total cases Intestinal metaplasia
P -values*
Ulcer
60 vears
42 17 (40.5)“
37 26 (70.3) .I
60 vears 41
1I 5
15
10
(13.0)
(24.3)
> .05
“The No. in parentheses indicate percentage of the total cases in each age groups. ’Method of study. *P-values of differences between patients younger and older than 60 years of age who had the same disease (chi-square test)
very close to the low-risk group in Narino. In Japan, where gastric cancer is most prevalent, an autopsy study showed intestinal metaplasia in 41.5% of grossly normal looking stomachs [ 101. Several groups of investigators have reported a high prevalence of intestinal metaplasia in the stomach of patients with gastric adenocarcinoma compared to benign gastric conditions [4,1 I , 121. Segura and Montero [ 1 11 in Spain found the prevalence of intestinal metaplasia to be 80.7% in benign ulcers and 97.1 % in cancer. The figure from Japan also showed a very high prevalence [ 101. Our result agrees more favourably with those reported from rather low-risk areas of gastric cancer. Filipe and his colleagues [ 121 surveyed three centers in London, Reims, and Paris and found the prevalence to be 65% in gastric cancer, 36% in benign gastric ulcer, and 22% in gastritis. Our figures are 54.4%, 35.1%, and 16%, respectively . The results of this study showed that intestinal metaplasia is found more frequently in gastric cancer than in benign gastric ulcer and gastritis. Patients with benign ulcers in any age group and patients with gastric cancer in the younger age group had similar rates of association with intestinal metaplasia in their stomach. Patients with gastric cancer who were older than 60 years of age had a significantly higher rate of metaplasia. This observation, including the figures of the percentage of occurrence in each gastric condition and age groups (Tables 111, IV), is quite similar to what Imai et al. reported in 1971 for American patients with gastric cancer, ulcer, and gastritis in Minnesota but is different from the Japanese whose prevalence of metaplasia in older age groups was found to be significantly higher in any of the three gastric conditions than their younger counterparts 141. The observation cited in this study is important, since it implies that finding intestinal metaplasia in the stomach of patients older than 60 years of age should arouse a suspicion of cancer and thus indicate a more careful
scrutiny and follow-up endoscopic examination with biopsy. This type of patient should not be just “reassured” when a cancer is not found in the initial workup and allowed to be lost to follow-up or to wait until obvious symptoms occur. Repetition of gastroscopy should be recommended if their symptoms continue no matter how mild they are. If a benign ulcer or even gastritis is present with intestinal metaplasia in a biopsy, it should definitely be repeated after a certain period of treatment. Any abnormal finding should be recorded and biopsied. In any event, it should be kept in mind that this type of patient may have some risk factors for developing gastric cancer, and proper attention should be paid to them.
ACKNOWLEDGMENTS The authors would like to thank Dr. Prasert Trairatvorakul, Dr. Sopon Jirasiritham, Dr. Chakkrapan Urnorases, and Dr. Suriya Chakkapark for inclusion of many of their patients in this study. They also wish to thank to Mrs. Suteera Uyathumrangsit who gave good support as an endoscopic assistant during the whole period of the study. Lastly, they appreciate all the valuable advice Prof. Sira Bunyarattavej has given in the revision of the manuscript. REFERENCES 1. Yamada E, Nakazato M, Koike A , Suzuki K, Kato K, Kito T: Surgical results for early gastric cancer. Int Surg 597-14, 1974.
2. Morson BC: Carcinoma arising from areas of intestinal metaplasia in gastric mucosa. Br J Cancer 9:377-385, 1955. 3. Nakamura K, Sugano H, Takagi K: Carcinoma of the stomach in incipient phase: Its histogenesis and histological appearances. Gann 59:251-258, 1968. 4. Imai T, Kubo T, Watanabe H: Chronic gastritis in Japanese with reference to high incidence of gastric carcinoma. JNCI 47: 179195, 1971. 5 . Con-ea P, Cuello C, Duque E: Carcinoma and intestinal metaplasia of the stomach in Colombian migrants. JNCI 44:297-306, 1970. 6. C o m a P, Cuello C, Duque E, Burbano LC, Garcia FT, Bolanos
Gastric Intestinal Metaplasia in Thailand 0, Brown C , Haenszel W: Gastric cancer in Colombia. 111. Natural history of precursor lesions. JNCl 57: 1027-1035, 1976. 7. Matsukura N, Kawachi T, Sasajima K, Sano T, Sugimura T, Hirota T: Induction of intestinal metaplasia in the stomach of rats by N-Methyl-N'-Nitro-N-Nitrosoguanidine. JNCI 61: 141-143, 1978. 8. Hashimoto M , Tokunaga A, Nishi K , Wada M, Masumori K , Kumagae Y , Numajiri H, Matsukura N , Oshiyasu M, Tanaka N, Shirota A, Asano G: ['HI Thymidine autoradiographic and alkaline phosphatase histochemical studies of intestinal metaplasia of the human stomach. Histochem J 15:953-959, 1983. 9. Pongchairerks P, Matsukura N, Tokunaga A, Tanaka N, Onda M, Miki M, Asano G, Hirota T: Lectin histochemical studies on
105
gastric intestinal metaplasia with Ulex europaeus agglutinin-I, Dolochos biflorus and Peanut agglutinins in comparison with gastric and small and large intestinal mucosa. Acta Histochem Cytochem. 20:147-161, 1987. 10. lmai T, Maruyama H: Time trend in the prevalence of intestinal metaplasia in Japan. Cancer 52353-361, 1983. 11. Segura DI, Montero C: Histochemical characterization of different types of intestinal metaplasia in gastric mucosa. Cancer 52: 498-503, 1983. 12. Filipe MI, Bogomoletz W, Dawson P, Fabiani B, Potet F: Intestinal metaplasia subtypes in the assessment of gastric cancer risk. A multicenter prospective study. Gut 24:A974, 1983.
