Celiac Disease at Several Hospitals in Jakarta, Indonesia
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1 CASE REPORT Celiac Disease at Several Hospitals in Jakarta, Indonesia Marcellus Simadibrata Department of Internal Medicine, Faculty of Medicine, University of Indonesia - dr. Cipto Mangunkusumo Hospital. Jl. Diponegoro no. 7, Jakarta Pusat 040, Indonesia. Correspondence mail to: cgono@indosat.net.id ABSTRACT In Indonesia, no study has reported celiac disease. The present study is conducted to obtain characteristics, clinical data, endoscopic and histopathological features of patients with celiac disease. The study was conducted in patients with chronic diarrhea at several hospitals in Jakarta between 995 and 009. Patients were considered as having positive celiac disease and were included in the study if they had complaint of chronic diarrhea, villous atrophy at descending duodenum/jejunum as categorized in Marsh criteria and positive serology on serum anti-gliadin antibody. As the histopathological control, there were 7 normal mucosa biopsies of duodenum and jejunum in patients with dyspepsia who had normal endoscopic appearance. Of 89 chronic diarrhea cases, there were 5 (0.6%) cases of celiac disease with subject characteristics as follows: men (pts), age years (pts), Chinese (pts), wellfinancial status (5pts), good hygiene and sanitation (5pts), loose-, non-steatorea and unbleeding stools (5pts) and 6 months diarrhea duration (pts). Celiac disease was found more frequently in subjects with malnutrition (pts), anemia (pts) and hypoalbuminemia (pts). Most of histopathological examination demonstrated total villous atrophy of the small intestines (pts). Measurement of small intestinal villous mucosa revealing the mean value of villous mucosa in patients with celiac disease was μ; while in normal/control subjects, the mean value was μ. The height of crypt, villi width and intervillous space were different from control. Lymphocytes in the mucosa and intraepithelium were higher than control. Celiac disease is found in 0.6% cases of chronic diarrhea. The characteristics of subjects mostly include men, Chinese ethnicity, age years, good-financial status, good hygiene and sanitation, 6-month diarrhea, malnutrition, anemia and hypoalbuminemia. In celiac disease, mucosa villous atrophy and other changes of intestinal mucosa can be found. Key words: celiac disease, villous atrophy, characteristics, physical examination, histopathology. INTRODUCTION Celiac disease is a disease of the small intestine that is caused by hypersensitivity to gluten. -4 Gluten is found in food or cookies containing wheat, barley, rye, and oat. 5 It is usually known as celiac sprue or gluten-sensitive enteropathy due to villous atrophy and damages on the small intestines. It is frequently found in Western countries such as Ireland, Netherland, England and North America.,6-9 The prevalence of such disease is very rare in Asia; however, it is increasing annually since Asian people are more easily and frequently exposed to gluten. 0 Many factors take account in the pathogenesis of celiac disease, such as genetic factor, immune reaction, etc. Symptoms of celiac disease are greasy chronic diarrhea (steatorrhea) with or without vomiting, sometimes include abdominal pain after eating food that contains gluten, weight loss, nutrient deficiency particularly anemia, malaise, abdominal discomfort, bloating and growth failure in childhood, etc. Complications that may occur in adults include nutrient deficiency, malnutrition, osteopenia/ osteoporosis, lymphoma malignant, etc.,9,, Specific characteristic of such disease is the presence of villous atrophy of the small intestines, especially jejunum. 9 Diagnosis is made based on villous atrophy seen on biopsy of the small intestine, positive serology results of antiendomysial antibody (AEA) or antigliadin antibody (AGA) or tissue transglutaminase antibody (ttg-ab) found in patient s serum. -7 Recently, Asian people, including Indonesians eat a lot of food containing gluten e.g. bread, noodles, cookies. Little has been reported about celiac disease in Asia. In Indonesia, no study on celiac disease has been reported although relatively a lot of chronic diarrhea cases are found.
2 Marcellus Simadibrata Acta Med Indones-Indones J Intern Med Based on such problems, therefore, this case report was conducted to obtain characteristics, endoscopic and histopathological features of patients with celiac disease. CASE ILLUSTRATION Patients with chronic diarrhea who visited or were hospitalized in Cipto Mangunkusumo Hospital and some private hospitals in Jakarta between (5- years period of study) were enrolled in the study. Esophagogastroduodeno-jejunoscopy, ileocolonoscopy, biopsies on transverse duodenum/proximal jejunum and antigliadin antibody test. Gastroduodenoscope and colonoscope of Olympus or Pentax manufacturers were utilized. Eating and drinking habit, including eating wheat (bread, etc) was recorded. Antigliadin antibody test was performed at Laboratory of Amsterdam University or United States/Prodia. Histopathological examination was performed in the associate hospitals and the histopathological slides were re-evaluated at Cipto Mangunkusumo Hospital and Amsterdam University. The antigliadin antibody serum was considered positive (+) when the serum antigliadin level was found in a titer of 5 AE/ml or more. It was considered uncertain (+) when the level was 0-4 AE/ ml and considered negative (-) when the level was less than 0 AE/ml). All patients underwent stool evaluation to exclude infection of giardia lamblia etc. which may cause villous atrophy of the small intestines. Celiac disease was considered positive and patients were enrolled in the study if they had complaint of chronic diarrhea, experienced villous atrophy on descending duodenum/jejunum in keeping with Marsh Criteria along with positive serology result of serum anti-gliadin antibody. The Marsh histopathological criteria and classification of intestinal mucosa are: 8 Marsh stage 0: normal mucosa Marsh stage : increased number of intraepithelial lymphocytes, usually exceeding 0 per 00 enterocytes Marsh stage : proliferation of the crypts of Lieberkuhn Marsh stage : partial or complete villous atrophy Marsh stage 4: hypoplasia of the small bowel architecture. Chronic diarrhea was diagnosed if the passage of stool was more than 00g per day or if passage of soft and watery stool was more than times per day with or without blood or mucous in the stool and it lasted more than 5 days. 9 As histopathological control, there were 7 normal mucosa biopsies of duodenum and jejunum in patients with dyspepsia who had normal endoscopic appearance. Patients were excluded if they had Giardia lamblia on stool examination, positive histopathological results and tropical spure. Patients were also excluded if they were not cooperative or unwilling to have esophagogastroduodenojejunoscopy, ileocolonoscopy and biopsy. In 5-year period of time, there were 89 cases of chronic diarrhea. Of all cases, 5 patients (0.6%) were diagnosed as celiac disease that met the inclusion criteria. The dominant subject characteristics were as follows: men (pts), age years (pts), Chinese ethnicity (pts), well-financial status (5pts), history of eating bread and other food containing wheat (5 pts), good hygiene and sanitation, (5pts), loose, non-steatorea and unbleeding stools (5pts) and 6-month diarrhea duration (pts). (Table ) Table. Characteristics of the patients Characteristics Number of patients (pts) (Total=5) Sex: Male/Female / Ethnicity: - Chinese - Minang - Javanese Age group: years years years Financial status: Good 5 History of food intake containing wheat or gluten 5 Hygiene-sanitation status: Good 5 Type of diarrhea: Soft non-bloody non steatorrheic stool 5 Duration of diarrhea: - 6 months - 4 months By physical examination and laboratory result, malnutrition (pts), anemia (pts) and hypoalbuminemia (pts) were found. (Table ) Table. Physical examination and laboratory results Physical examination/ laboratory results Nutritional status: - Underweight Anemia: - Yes - No Hypoalbuminemia: - Yes - No Number of patients (pts) (Total = 5)
3 Vol 4 Number 4 October 00 Celiac Disease at Several Hospitals in Jakarta, Indonesia By endoscopy, it was apparent that most subjects had normal gaster ( pts), normal duodenum (-4 pts), normal jejunum (4 pts), and normal ileum terminal ( pts). (Table ) Table. Endoscopic findings of small intestines and colon Endoscopic Findings Gaster: - Mild hyperemia (gastritis) Duodenum: - Bulbus: - Hyperemia (gastritis) - Ulcer - Pars descendens; - Scalloping Jejunum: : - Scalloping: Terminal ileum: - Hyperemia - Follicle lymphoid hyperplasia Colon: - Polyp - Hyperemia & erosions (Colitis) Number of patients (Total =5) On the disease progression, the first case had complication of malignant intestinal/abdominal lymphoma and the patient finally died due to septic shock. Histopathological examination revealed that most subjects had total villous atrophy of the small intestine mucosa. By measuring villi of the intestinal mucosa with micro-meter, it was found that the height of mucosa villi in patients with celiac disease was μ. It is very different from the normal villous height of the mucosa in Indonesian people, i.e μ. Unfortunately, there were only a little number of cases and, therefore, it could not be analyzed statistically. The crypt depth of the mucosa in patients with celiac sprue was μ, which was different from the normal depth in Indonesian people of μ. The villous width and intervillous space of such patients were smaller than normal. In patients with celiac disease, there were a lot of mucosal and intraepithelial lymphocytes infiltrations compared to normal control. (Table 4) DISCUSSION The present study demonstrated prevalence of celiac disease to be 0.6% similar to data of other 4 4 Table 4. Histopathological results of transverse duodenum/ jejunum mucosa Histopathological examination Villous atrophy: - Total atrophy - Focal Partial atrophy Measuring villous mucosa: - Villous height - Crypt depth - Villous width - Intervillous space Inflammatory cells: Lymphocytes: ++ Intraepithelial lymphocytes: ++ Plasma cells: - 0 Eosinophils: Patients (total n=5) Number Means ( ): Frequency (%) 5/5(00) 5/5(00) 5/5(00) /5(60) /5(40) Control (total n=7) 0 0 Means ( ) Frequency (%) 7/7(00) 0/7 0/7 /7(.7) 6/7(97.) 0/7(54.) 6/7(4.) /7(.7) countries.,6,7 However, the data were obtained from hospitals and may not represent population in the community. The hospital data of University Maryland, USA 0 reported that the prevalence of celiac disease in patients who have the risk due to family factor was of patients (4.55%). In addition, the prevalence of celiac disease in patients without any risk was of patients (0.75%). Moreover, the prevalence of celiac disease in Denmark population is : 00, about : 050 in Sweden, : 600 in Scotland, and :00 in Ireland. 7 It is estimated that the prevalence of celiac disease in Europe, Australia and North America is about 0.5- %., Compared to the study reports in China, Indonesia has different study results. Jiang LL et al. reported that the incidence of celiac disease was 6.5% of chronic diarrhea patients that had been studied. Bhatnagar S et al 4 also found relatively a lot of cases, i.e. approximately 59 children in India and 4% of them had severe enteropathy. Indonesians heavily consume food containing wheat or gluten including noodles, bread, cookies, etc. It is logical to think that if there is hypersensitivity to wheat or gluten in other countries, then there might be similar cases in Indonesia. The low frequency in Indonesia may be due to low knowledge level and experience of the physicians on celiac disease as well as inadequate diagnostic facilities for such a disease, the need of duodenojejunoscopy and histopathological examination that is quite expensive, in addition to the need on
4 Marcellus Simadibrata Acta Med Indones-Indones J Intern Med serologic test (IgA-) endomysial and antigliadin antibodies, which is not available in Indonesia and only can be performed abroad such as in Netherland/United States. Subject characteristics vary in literature. In the present study, most subjects were male, which is different from literature data suggesting most subjects were female. 7 Most subjects were at the age of years; while other literature demonstrates the mean age of 4 years. 7 On physical examination, there were patients with anemia and hypoalbuminemia, which is consistent with the data of literature reporting similar complications. 7,5 Serologic test on anti-gliadin antibody was performed in Amsterdam and United States through the Prodia laboratory with a relatively high cost since the test still cannot be performed in Indonesia. If the antigliadin or other serologic antibody tests can be maintained at low cost with simple procedures in Indonesia, then such laboratory tests will be utilized as a screening test for celiac disease in Indonesia. Recently, some studies in Asian countries begin to demonstrate an increased number of celiac disease as Asian people are more often consuming wheat that contains gluten.,4 Incidence of celiac disease in Indonesia may possibly increase since there are more people consuming food that contains gluten. In the present study, endoscopy revealed more subjects with normal appearance of the small intestine since it is difficult to differentiate villous atrophy and the normal by endoscopy. Therefore, duodenum and jejunum biopsies in all chronic diarrhea cases are necessary, especially in patients who consume food containing wheat/gluten. One patient with celiac sprue eventually died due to abdominal/intestinal malignant lymphoma which is in keeping with the literature data reporting that there are large numbers of malignant lymphoma complication in celiac disease cases. 0, Histopathologic examination on celiac cases revealed total and focal partial villous atrophy of the intestinal mucosa, which is consistent with literature reports.,6,7 Compared to normal control, intestinal mucosa of patients with celiac disease is apparently different. The villous height is considerably shorter than normal, which is consistent with literature data. Crypt depth is much deeper than normal and it is also consistent with literature. Villous width and intervillous space are smaller than the normal control, which vary compared to the literature. The present study found increased infiltration of mucosal and intraepithelial lymphocytes cell in keeping with literature data.,8 Other infiltration cells were not significantly different compared to the normal control. CONCLUSION Celiac disease may be found in Indonesian people with 0.6% prevalence in patients with chronic diarrhea. The most characteristics found for celiac disease include men, Chinese ethnicity, age years, good-financial status, good hygiene and sanitation, 6- month duration of diarrhea, malnutrition, anemia and hypoalbuminemia. Celiac disease causes villous atrophy of the intestinal mucosa with extremely different villous height, crypt depth, villous width and intervillous space compared to normal. In patients with celiac disease, there are increased mucosal and intraepithelial lymphocytes compared to normal subjects. ACKNOWLEDGEMENT I would like to thank to dr. Vera Yuwono SpPA(K), Prof. Dr. FJW Ten Kate PhD, Prof. Dr. GNJ Tytgat PhD, Prof. Dr. Daldiyono PhD and Prof. Dr. Laurentius Lesmana PhD, Dr. Murdani Abdullah PhD, nurses at endoscopy facilities of Cipto Mangunkusumo Hospital, Abdi waluyo and Pluit Hospital and Prodia laboratory for their help, contribution and suggestion for me. REFERENCES. Kelly CP, Feighery CF, Gallagher RB, Weir DG. Diagnosis and treatment of Gluten-sensitive enteropathy. Adv Intern Med. 990;5: Wikipedia. Coeliac disease. Available from url: en.wikipedia.org/wiki/coeliac_disease. downloaded May 00.. Meschino JP. Celiac disease: A commonly underdiagnosed condition of the small bowel. Available from url: article.php?id=5406. downloaded May Da Silva NMM, Gonzales-Garcia MB, Nouws HP, Delerue- Matos C, Santos-Silva A, Costa-Garcia A. Celiac disease diagnosis and gluten-free food analytical control. Anal Bioanal Chem 00. Available from url: pubmed/ downloaded 4 May Press TV. Mouth ulcers predict celiac disease. Available from url: downloaded May Fine KD, Meyer RL, Lee EL. The prevalence and causes of chronic diarrhea in patients with celiac sprue treated with a gluten-free diet. Gastroenterol. 997;:
5 Vol 4 Number 4 October 00 Celiac Disease at Several Hospitals in Jakarta, Indonesia 7. Dickey W. Serology and endoscopy in coeliac disease: applications and limitations. Academisch Proefschrift. December 000. Universiteit van Amsterdam. 8. Freeman H. Celiac disease: A review. BCMJ. 00;4: O Farrely C. Is villous atrophy always and only the result of gluten sensitive disease of the intestine. Eur J Gastroenterol Hepatol. 000;: Mathus-Vliegen EMH. Coeliac disease and lymphoma: current status.neth J Med. 996; 49: -0.. Johnston SD & Watson RGP. Small bowel lymphoma in unrecognized coeliac disease: a cause for concern? Eur J Gastroenterol Hepatol. 000;: Makishima H, Ito T, Kodama R, Asano N, Nakazawa H, Hirabayashi K, et al. Intestinal diffuse large B-cell lymphoma associated with celiac disease: a Japanese case. Int J Hematol. 006;8:6-5.. Farrell RJ, Kelly CP. Celiac sprue. N Engl J Med. 00;46: Sollid LM, Khosla C. Future therapeutic options for celiac disease. Nat Clin Pract Gastroenterol Hepatol. 005;: Van der Windt DA, Jellema P, Mulder CJ, Kneepkens CM, van der Horst HE. Diagnostic testing for celiac disease among patients with abdominal symptoms: a systematic review. JAMA. 00;0: Caristo E, Tognato E, Di Dio G, Rapa A, Fonio P. Increasing prevalence of celiac children with negative serum antigliadin antibodies. Minerva Pediatr. 00;6: Makovicky P. What can we do to promote the recognition of celiac disease: a report on diagnostic strategies. Bratisl Lek Listy. 00;:6-5, 8. Marsh M. Gluten, major histocompatibility complex, and the small intestine. A molecular and immunobiologic approach to the spectrum of gluten sensitivity ( celiac sprue ). Gastroenterol. 99;0: Simadibrata M, Tytgat GN, Yuwono V, Daldiyono, Lesmana L, Syam AF, et al. Microorganisms and parasites in chronic infective diarrhea. Acta Med Indones. 004;6; University of Maryland. Celiac disease is more prevalent in US than previously thought. Available from url: downloaded 4 May 00.. Cataldo F, Montalto G. Celiac disease in the developing countries: a new and challenging public health problem. World J Gastroenterol. 007;:5 9.. Harrison MS, Wehbi M, Obideen K. Celiac disease: More common than you think. Available from url: enotes.tripod.com/celiac007.pdf. Downloaded May 00.. Jiang LL, Zhang BL, Liu YS. Is adult celiac disease really uncommon in Chinese? J Zhejiang Univ Sci B. 009;0: Bhatnagar S, Gupta SD, Mathur M, Phillips AD, Kumar R, Knutton S, et al. Celiac disease with mild to moderate histologic changes is a common cause of chronic diarrhea in Indian children. J Pediatr Gastroenterol Nutr. 005;4: Hatting M, Galm O, Meyer M, trautwein C, Tischendorf JJ. Anemia and severe thrombocytopenia in celiac disease. Med Klin (Munich). 00;05:
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