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Parasites in Patients with Malabsorption


Dig Dis Sci (2008) 53:672–679 DOI 10.1007/s10620-007-9927-9

ORIGINAL PAPER

Parasites in Patients with Malabsorption Syndrome: A Clinical Study in Children and Adults
Bijayini Behera ? B. R. Mirdha ? Govind K. Makharia ? Shinjini Bhatnagar ? Siddhartha Dattagupta ? J. C. Samantaray

Received: 12 January 2007 / Accepted: 9 July 2007 / Published online: 31 August 2007 ? Springer Science+Business Media, LLC 2007

Abstract Background: Intestinal parasites not only cause diarrheal diseases but also signi?cant malabsorption. Literature on the role of parasites, such as intestinal coccidia and microsporidia in malabsorption syndrome is limited. Methods: Three consecutive stool samples from 50 adult and 50 children patients with malabsorption syndrome and an equal number of healthy controls without diarrhea were examined for intestinal coccidia, microsporidia and other intestinal parasites by wet mount, Kinyoun’s modi?ed acid-fast staining and chromotrope 2R staining. Results: Celiac disease was the commonest cause of malabsorption syndrome in both adults (52%) and children (74%). Forty (80%) and 41 (82%) adults and children, respectively, with malabsorption syndrome were infected with parasites. These results were signi?cantly higher in comparison to those from the healthy adults and children controls (22% and 16%), respectively (P < 0.001). Of them, 48% and 46% of the adults and children, respectively, with malabsorption had pathogenic parasitic infections. The pathogenic parasites detected in
B. Behera ? B. R. Mirdha (&) ? J. C. Samantaray Department of Microbiology, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India e-mail: mirdhabr@hotmail.com G. K. Makharia Department of Gastroenterology and Human nutrition, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India S. Bhatnagar Department of Pediatrics, Centre for Diarrheal Diseases and Nutrition Research, All India Institute of Medical Sciences, New Delhi 110029, India S. Dattagupta Department of Pathology, All India Institute of Medical Sciences, New Delhi 110029, India

adults were Giardia lamblia 12 (24%), E. histolytica / dispar 5 (10%), Ancylostoma duodenale 4 (8%), H. nana 2 (4%) and Cyclospora cayetanensis 1 (2%). The pathogenic parasites detected in children with malabsorption syndrome were Giardia lamblia 8 (16%), Cryptosporidium 7 (14%), E. histolytica / dispar 3 (6%), Ancylostoma duodenale 3 (6%), Isospora belli 1 (2%), and H. nana 1 (2%). None of the stool samples from healthy controls were positive for Cryptosporidium spp., Cyclospora and Isospora belli. All the patients infected with intestinal coccidia were HIV seronegative. Conclusion: Celiac disease is the most common cause of malabsorption syndrome in both adults and children. These people harbor signi?cantly more pathogenic parasites and are more frequently colonized with harmless commensals as compared to healthy controls. Intestinal coccidia are associated with malabsorption syndrome, particularly in malnourished children. Keywords Chronic diarrhea ? Celiac disease ? Small intestine ? Parasites ? Coccidia ? Microsporidia ? Giardia lamblia ? Helminthes ? Pathogenic parasites ? Non-pathogenic parasites

Introduction The causes of malabsorption syndrome differ according to geographical location (developing and developed countries) and different age groups of patients [1]. While tropical sprue, intestinal parasitosis, celiac disease and immunode?ciency states are important causes of malabsorption syndrome in developing countries; celiac disease and Crohn’s disease are the most important causes of malabsorption syndrome in industrialized countries [2]. Intestinal parasites are not only important causes of acute

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diarrheal illnesses, but they also cause chronic diarrhea and malabsorption 3]. Giardiasis, strongyloidosis and capillariasis are de?nitive causes of malabsorption of many nutrients [3]. The concept of human coccidia and microsporidia as a cause of malabsorption syndrome has come into limelight during the past 20 years [4]. Although there are studies on the parasitic causes of malabsorption, most of them, however, have concentrated on giardiasis. There is a lack of comprehensive study on the role of parasites both pathogenic and non-pathogenic in patients with malabsorption syndrome. Therefore, in a prospective study, we evaluated both children and adults patients with malabsorption syndrome for presence of both pathogenic and non-pathogenic parasites. Patients and methods This cross-sectional prospective study was conducted at All India Institute of Medical sciences, New Delhi from July 2004 to June 2006. Both children and adult patients with malabsorption syndrome were included in this study. Inclusion criteria Adults Fifty adult patients ful?lling the following two criteria for the diagnosis of malabsorption syndrome were included: (1) chronic diarrhea of more than three weeks duration and (2) presence of malabsorption as evidenced by one or more of the following (a) abnormal D-xylose test—excretion of less than 1 g of D-xylose in the urine over 5 h after ingestion of 5 g of D-xylose (b) clinical features suggestive of nutritional de?ciencies (iron, folate, cyanocobalamin, vitamin D and vitamin K), and/or (c) presence of anemia and hypoalbuminaemia. Children Fifty children ful?lling the following two criteria for a diagnosis of malabsorption syndrome were included in the study (1) abnormal D-xylose test- excretion of less than 1 g of D-xylose excretion in the urine over 5 h after ingestion of 5 g of D-xylose; (2) presence of malabsorption as evidenced by one or more of the following: (a) chronic diarrhea of more than 6 weeks duration, (b) weight and/or height less than two standard deviation for the age according to National Centre for Health Statistics criteria [5], (c) clinical features suggestive of nutritional de?ciencies, and (d) presence of anemia, hypoalbuminaemia, and/ or abnormal lipid pro?le.

Tests for absorptive functions Urinary excretion of D-xylose was measured after an oral dose of 5 g. In patients with borderline 5 h urinary excretion values, 1 h serum D-xylose levels were estimated after repeating the test. Urinary excretion below 1 g/5 g/5 h of D-xylose or 1 h serum level D-xylose of less than 20 mg/dl was considered abnormal [6]. Fecal fat was estimated by either Van de Kamer quantitative method [7] or by Sudan III staining [8] fecal fat content >7 g/day in adults and >4.5 g/day in children or more than 12 droplets/high-power ?eld of microscope (Sudan III staining) were taken as abnormal [7, 8].

Determination of etiology of malabsorption syndrome Depending upon the clinical setting, patients were individualized for appropriate investigations to determine the etiology of malabsorption.

Stool examination Three consecutive stool samples from all the patients with malabsorption syndrome were collected and examined. The stool samples were concentrated by formol-ether concentration technique, according to standard methods [9]. Direct microscopic examination of fecal specimens was performed in fresh physiologic saline and Lugol’s iodine. Stool samples were also stained by modi?ed Kinyoun’s acid-fast staining for coccidian oocysts and chromotrope 2R staining for microsporidia using standard methods [10, 11]. We initially screened the entire microscopic ?eld using a 10· objective (100· magni?cation), and then using a 40· objective (400· magni?cation) in case of any ambiguity. Finally we examined 10 microscopic ?elds at each corner and 10 microscopic ?eld in the center (total 50 microscopic ?elds) under the 40· objective before reporting a specimen as no parasites found. Every stool sample was examined by two experienced microbiologists. Micrometry was done in case of ambiguity to con?rm the size of different coccidian oocysts (Fig. 1, 2, 3, 4). Quality control: Known positive slides for Cryptosporidium, Cyclospora, Isospora and microsporidia were stained with each batch of staining and compared with stool preparations of both patients and healthy controls.

Upper gastrointestinal endoscopic examination and mucosal histology All patients underwent upper gastrointestinal endoscopic examination and multiple mucosal biopsies were obtained

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Fig. 1 Microphotograph showing Cryptosporidium oocysts appearing as bright pinkish stained organisms against green back ground stained by Kinyoun’s modi?ed acid–fast staining. (Magni?cation 1000·)

Fig. 3 Microphotograph showing Isospora oocysts, stained red against green background. Elongated ellipsoidal in shape, (magni?cation 1000·)

Fig. 2 Microphotograph showing Cyclospora cayetanensis oocysts appear as round and have a wrinkled appearance, stained by Kinyoun’s modi?ed acid–fast staining. (Magni?cation 1000·)

Fig. 4 Microphotograph showing Giardia trophozoites appearing as sickle shaped organism attached to the surface or free within the mucus layer in a duodenal biopsy specimens (H&E staining·20)

from the third part of the duodenum or proximal jejunum. Duodenal biopsy specimens were paraf?n-processed, formalin-?xed, serially sectioned and stained by hematoxylin and eosin (H&E) staining. The presence of parasitic elements (trophozoites of Giardia, coccidian oocysts and spores of microsporidia) were carefully looked for. Modi?ed Marsh classi?cation was used for grading of the mucosal changes: Grade 0, normal histology; Grade 1, mild increase in intraepithelial lymphocytes (IEL), crypt-villous (CV) ratio 1:1; Grade 2, moderate villous atrophy with CV ratio more than 1; Grade 3, ?at mucosa with no recognizable villi [12].

Serological tests for celiac disease Serum IgA-anti-endomysial (AEA) antibody test was done using monkey esophagus as a substrate for celiac disease [13]. (Indirect immuno?uorescence assay; binding site, Birmingham, England). Anti-gliadin antibodies were tested using a solid phase enzyme linked immunoadsorbent assay with commercially available crude gliadin [14] (Sigma, St. Louis, MO). Serum IgA levels and anti-gliadin IgG were performed only in subjects who had moderate or severe mucosal changes and were negative for serum IgAAEA. Serum immunoglobulin levels (IgA, IgG, and IgM)

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were obtained in patients whose clinical pro?les were consistent with celiac disease but had negative serological tests for celiac disease. Other tests, including hemogram, blood chemistry, and coagulation parameters, were done on all the patients. Antibodies to HIV-1 and HIV-2 were done when indicated clinically. The diagnosis of celiac disease in them was made on the basis of the modi?ed European Society of Pediatric Gastroenterology Hepatology and Nutrition (ESPAGHAN) criteria [15, 16]. Controls Age and gender matched 50 healthy adults and 50 healthy children having no gastrointestinal manifestations were recruited and two consecutive stool samples were collected and examined as per protocol described above. An informed consent was taken from patients and this study was cleared by the Ethics Committee of All India Institute of Medical Sciences, New Delhi. Statistical analysis Descriptive statistics, such as mean, median, range, were used to describe baseline demographic and clinical pro?le of all the patients. An unpaired t-test was used to assess the mean signi?cant difference of various quantitative parameters between patients and controls. For skewed data (non-normal), the corresponding non-parametric test, i.e., Mann-Whitney U-test was applied. Further, one way analysis of variance (ANOVA) with post hoc analysis was used to assess the mean signi?cant difference between patients of various parasitic and nonparasitic causes of malabsorption syndrome. For skewed data (non-normal), the corresponding non-parametric test, i.e., Kruskal-Wallis test was applied for the same. Chi-square test was used in order to examine the association of various qualitative variables with the outcome. A P-value of <0.05 was considered to be statistically signi?cant. All the statistical analysis was done by using statistical software SPSS 11.5. Results The mean age of adult patients with malabsorption syndrome were 30.1 ± 10.1 years (males 28). Children with malabsorption syndrome had a mean age of 87.44 ± 47.4 months (males 35). The demographic, clinical and biochemical pro?le of 50 adults and pediatric patients with various causes of malabsorption syndrome is shown in Tables 1 and 2, respectively.

Etiology of malabsorption in adults Celiac disease (26/50, 52%) was the commonest cause of malabsorption syndrome in adults. Other causes of malabsorption in adults included giardiasis in 12 (24%), tropical sprue in 6 (12%), intestinal lymphangiectasia in 3 (6%), common variable immunode?ciency syndrome in 3 (6%), hypothyroidism in 2 (4%) and immuno-proliferative small intestinal disease (IPSID) in 1 (2%). Four (8%) patients had a combination of celiac disease and giardiasis. C. cayetanensis was present in a 36-year-old immunocompetent lady with malabsorption syndrome and none in healthy controls. She had had chronic diarrhea, abdominal pain and bloating for the past 6 weeks. She was HIV sero-negative and had not traveled outside Delhi. However, none of the intracellular life-cycle stages of C. cayetanensis could be identi?ed in the duodenal biopsy specimen. Although the mean duration of diarrhea in patients with giardiasis was shorter (6.6 ± 7.5 months) in comparison to patients with non-parasitic causes of malabsorption, the difference did not reach to a level of statistical signi?cance. Patients with celiac disease had lower hemoglobin in comparison to other causes of malabsorption. There was no signi?cant difference in the urinary D-xylose excretion and serum albumin level among various causes of malabsorption in adults (P > 0.05; Table 1).

Etiology of malabsorption in children The mean duration of the disease was 43.1 ± 41.7 months. Seventy-four percent (37 children) had celiac disease as a cause of malabsorption syndrome. Of them 3 (6%) patients had superimposed infection with Giardia lamblia infection. Sixteen patients (32%) had evidence of parasitic infection [giardiasis 8 (16%), Cryptosporidiosis 7 (14%) and Isosporiosis 1 (2%)] (Table 2). All the patients with Cryptosporidiosis and Isosporiosis were HIV negative. There was a signi?cant difference in the mean age of children with different causes of malabsorption. Children positive for Cryptosporidium spp. were younger as compared to children with celiac disease (P = 0.010). Children positive for Cryptosporidium spp. also had a signi?cantly shorter duration of diarrhea in comparison to those with celiac disease (P = 0.003). Mean serum albumin level in children with Cryptosporidium spp. was signi?cantly lower than in children with giardiasis and celiac disease, (P = 0.001) (Table 2). There was no signi?cant difference in blood hemoglobin in patients with celiac disease and parasitosis.

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Table 1 Demographic, clinical and biochemical parameters in adults patients with different causes of malabsorption Parameter Total (n = 50) 29.8 ± 10.2 28:22 16.1 ± 15.9 10.7 ± 1.7 4.1 ± 0.7 0.59 ± 0.17 Celiac disease (n = 22) 29.5 ± 9.6 15:7 22.8 ± 19.5 9.6 ± 1.2 4.4 ± 0.6 0.55 ± 0.16 Giardiasis (n = 8) 29.6 ± 11.3 5:3 6.6 ± 7.5 12.9 ± 1.1 4.1 ± 0.3 0.56 ± 0.19 Giardiasis + Celiac disease (n = 4) 24 ± 4.7 2:2 22.5 ± 10.2 11.2 ± 1.1 4.5 ± 0.4 0.45 ± 0.09 Cyclosporiasis (n = 1) 36 – 1 10.8 4.2 0.58 Other causes (n = 15)* 31 ± 11.9 6:9 13.2 ± 11.3 10.8 ± 1.5 3.7 ± 0.5 0.65 ± 0.15 P-value

Age (years) Sex(M:F) Duration of diarrhea (months) Hb (g/dl) Serum albumin (g/dl) Urine D-xylose Values shown as mean ± SD

0.509 0.774 0.110 0.001 0.183 0.451

*Tropical sprue, 6; intestinal lymphangiectasia, 3; common variable immunode?ciency, 3; hypothyroidism, 2; immunoproliferative small intestinal disease, 1

Parasites in patients with malabsorption In 40 (80%) and 41 (82%) adult and children patients with malabsorption, stool examination revealed some form of parasites (pathogenic or non-pathogenic) in comparison to 11 (22%) and 8 (16%) healthy adult and children controls, respectively (P < 0.001). In adults, of 40 patients having parasites in stool, 24 (60%) were pathogenic and 40% were non-pathogenic. In the corresponding healthy control group, 5 (45%) of 11 had pathogenic parasites in their stool. Of 41 children with malabsorption syndrome having parasitic infection, 23 (56%) and 18 (44%) had pathogenic and non-pathogenic parasites, respectively. Among eight healthy children having parasitic infection, four each had pathogenic and non-pathogenic parasitic infection. (Table 3). The total numbers of intestinal parasites (both pathogenic and non-pathogenic) were signi?cantly more in both adult and children patients with malabsorption syndrome as compared to adults and children healthy controls (P < 0.001; Table 3). Both adults and children patients with celiac disease were more frequently harboring pathogenic parasites (Giardia lamblia, Hymenolepis nana, Hookworm) and were colonized with harmless commensals. (Entamoeba dispar, Entamoeba coli, Endolimax nana, Iodamoeba butschlii).

Prevalence of coccidia in patients with malabsorption syndrome was signi?cantly higher in the pediatrics age group in comparison to that in the adults (16% vs. 2%). Among the coccidia, Cryptosporidium spp. was the most common. Isospora belli and Cyclospora cayetanensis was detected in one patient each. Frequency of Cryptosporidium infection was signi?cantly higher in children with malabsorption syndrome as compared to adults (P = 0.01).

Histological changes Among patients with giardiasis, the intestinal villi were either normal or had mild crypt-villous abnormalities. None of the patients with giardiasis had moderate to severe villous abnormality. Trophozoites of Giardia lamblia was found in 62.5% and 60% of adults and children with giardiasis, respectively in the duodenal biopsies.

Discussion Our study shows that celiac disease is the most important cause of malabsorption both in adults and children. Gastrointestinal parasites also contribute to a signi?cant

Table 2 Demographic, clinical and biochemical parameters in children with different causes of malabsorption Parameter Total (n = 50) 89.96 ± 46.6 28:22 43.19 ± 41.7 8.7 ± 2.7 3.9 ± 0.87 0.53 ± 0.28 Celiac disease (n = 34) 91.59 ± 44.4 20:14 51.79 ± 43.0 8.4 ± 2.6 4.0 ± 0.81 0.59 ± 0.30 Giardiasis (n = 5) 85.2 ± 51.8 4:1 45.2 ± 26.0 9.8 ± 3.6 4.4 ± 0.68 0.43 ± 0.20 Giardiasis + Celiac disease (n = 3) 45.67 ± 35.07 1:2 42 ± 46.8 8.5 ± 2.1 3.8 ± 0.78 0.25 ± 0.04 Cryptosporidiosis (n = 7) 58.57 ± 73.4 6:1 0.46 ± 0.14 9.1 ± 3.5 2.8 ± 0.47 0.47 ± 0.25 Isosporiasis (n = 1) 36 F 1 9.2 4.0 0.62 P-value

Age (months) Sex (M:F) Duration of diarrhea (months) Hemoglobin (g/dl) S albumin (g/dl) Urine D-xylose

0.030 0.312 0.001 0.862 0.005 0.107

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Dig Dis Sci (2008) 53:672–679 Table 3 Intestinal parasitic pro?le in cases and controls Organisms Adults Cases (n = 50) Pathogenic protozoa Cryptosporidium spp. Isospora belli Cyclospora cayetanensis Microsporidia Giardia* E. histolytica/E. dispar Pathogenic Helminths Hymenolepis nana Hookworm Non-pathogenic parasites Entamoeba coli Endolimax nana Iodamoeba butschlii Total 6 (12%) 3 (6%) 5 (10%) 40 (80%) 3 (6%) 0 3 (6%) 11 (22%) <0.001 5 (10%) 3 (6%) 7 (14%) 41 (82%) 1 (2%) 0 3 (6%) 8 (16%) 0 0 1 (2%) 0 12 (24%) 5 (10%) 2 (4%) 4 (8%) 0 0 0 0 4 (8%) 1 (2%) 0 0 0.05 0.20 0.49 0.11 0.98 7 (14%) 1 (2%) 0 0 8 (16%) 3 (6%) 1 (2%) 3 (6%) 0 0 0 0 3 (6%) 1 (2%) 0 0 Control (n = 50) p value Children Cases (n = 50) Control (n = 50)

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p value

0.01 0.98

0.20 0.61 0.98 0.24

<0.001

*Among 12 adult cases positive for Giardia lamblia, three had both cyst and trophozoites where as among the eight pediatrics patients; only one patient had trophozoites in stool

proportion of patients with malabsorption syndrome. Eighty percent of adults and 82% of children patients with malabsorption syndrome harbored parasites (both pathogenic and non-pathogenic), whereas only 22% and 16% of healthy adult and children controls harbored parasites in their gastrointestinal tract. Tropical sprue had been the commonest cause of malabsorption in India; however, the incidence of tropical sprue is gradually on decline, most likely due to increasing use of antibiotics and improvement in water sanitation. In the present study, only six (12%) adults and none of the children with malabsorption syndrome had tropical sprue. Some of the reports also suggest coccidian parasites, such as etiological agents for tropical sprue [17]. In our study, however, we did not ?nd coccidian parasites in any of the patients with tropical sprue. Malabsorption in cases of giardiasis has been well documented and may be responsible for the substantial weight loss that occurs in those with Giardia lamblia infection [18]. Even when the infection is asymptomatic, malabsorption of fats, carbohydrates, sugars and vitamins may occur [18]. In our study, Giardia lamblia infection was detected in 24% of adults and 16% of children with malabsorption syndrome. In few patients with malabsorption syndrome, there may be super-infection by Giardia lamblia, in addition to another cause of malabsorption syndrome as seen in our patients. There is considerable controversy as to whether hookworm infection can result in malabsorption [19, 20]. In the

present study, hookworm infestation was detected in 8% of the adults and 6% of children. They were seen in association with celiac disease and hypothyroidism; hence, their independent contribution to malabsorption syndrome in these patients could not be ascertained. In our study, Hymenolepis nana was detected in 4% of adults and 2% of children with malabsorption syndrome. They were seen in association with other causes of malabsorption syndrome. An earlier study carried out at our institution showed Hymenolepis nana as a cause of diarrhea in children residing in urban slums [21]: however, there is no study elucidating its role in patients with malabsorption syndrome. It is possible that their presence in the stool was a incidental chance ?nding. We could not ascertain if they had played a role either in producing some symptoms of their own or they aggravated the symptoms of underlying disease. Small-bowel dysfunction, including malabsorption of vitamin B12, D-xylose, and fat, has been found in patients with AIDS and infection caused by Cryptosporidium spp., Cyclospora cayetanensis, microsporidia and Isospora [22]. Histopathological studies have documented a broad range of structural abnormalities in all four of these infections, including villous shortening or ?attening, crypt hyperplasia, and increased numbers of leukocytes in the lamina propria and epithelium [22]. Studies also provide evidence that patients with AIDS can have these mucosal abnormalities as well as abnormal D-xylose tests in the absence of infection by coccidian parasites [23]. Hence, the role of these groups of pathogens in causing these abnormalities remains to be

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evaluated with much larger population. In our study, Cryptosporidium oocysts were present in seven (14%) children with malabsorption syndrome and none of the adults with malabsorption and healthy controls. All these children were HIV sero-negative. Cryptosporidium spp. was more frequently detected in children less than 2 years of age (71%). According to a report by Bhattacharya et al. [24] isolation of Cryptosporidium spp. was highest among children between 6 months and 12 months (38.2%) of age. Older children had a lower rate of infection, indicating increased susceptibility of infants to Cryptosporidium. Study by Rahman et al. [25] and by Nagamani et al. [26] also reported similar ?ndings. All the children with Cryptosporidium were malnourished. In a study from India, Jaggi et al. [27] has also shown malnutrition to be the strongest risk factor for pediatric cryptosporidiosis. In our study, we found only one immunocompetent patient (36-year-old female) with malabsorption syndrome having infection with C. cayetanensis. However, none of the intracellular life-cycle stages of C. cayetanensis could be identi?ed in the duodenal biopsy specimen. Connor and colleagues [28] reported malabsorption syndrome in nine immunocompetent persons with cyclosporiasis. To the best of our knowledge, this the ?rst report of C. cayetanensis from our country in an immunocompetent adult with no travel history. Isosporiasis generally occur in immunocompromised hosts, in our study a 13-year-old immunocompetent individual with malabsorption syndrome was infected with Isospora belli. Duodenal biopsy could not be performed due to lack of consent. The child was HIV sero-negative. Isospora belli was the sole infecting pathogen in this case. He was treated successfully with co-trimoxazole. Sasaki et al. [29] earlier reported Isospora belli in a patient with malabsorption syndrome. In a previous study from our department, Isospora belli in ?ve HIV seronegative children were reported [30]. Microsporidia were not detected in any of the cases and control by chromotrope 2R staining. Signi?cantly more patients, both adults and children, with malabsorption syndrome were observed to harbor and excrete both pathogenic and non-pathogenic parasites (both protozoa and helminthes) in comparison to healthy controls. There is no previous report on this issue in the English literature. Our observation raises a basic question, do patients with malabsorption syndrome are predisposed to multiple parasitic infections? It is possible that we might have overestimated the frequency of these parasites in cases compared to controls, as we examined three consecutive stool samples in cases where we could have examined two– three stool samples from each healthy control. In a recent study from Santa Clara County, California, of a refugee clinic with 533 refugees, stool parasites were identi?ed from 14% of refugees, including 9% found to

have one or more protozoa and 6% found to have at least one helminth [31]. Protozoa were more frequent in refugees <18 years of age (OR: 2.2 [1.2–4.2]), whereas helminthes were more common in refugees from South Central Asia (OR: 8.0 [2.3–27.7]) and Africa (OR: 5.9 [1.6–21.6]), when compared with refugees from Eastern Europe and the Middle East. Similar increased prevalence of these commensal parasites has been found in homosexuals with AIDS and refugees [31]. Several studies support high rates of infection with non-pathogenic ameba in the homosexual population with acquired immunode?ciency syndrome [32]. The authors hypothesized that parasites acted as a cofactor to facilitate HIV infection and/ or its progression to AIDS by depressing cell-mediated immunity. The importance of recognizing parasitic infection in patients with malabsorption syndrome extends beyond the clinical diseases they speci?cally elicit. Although most infections are asymptomatic, an increasing amount of data indicate that harboring helminthes may alter the course of other, more life-threatening and communicable infectious diseases, such as tuberculosis and HIV [33]. Besides upregulating Th2 responses, many helminthes also downregulate Th1 responses, affecting the ability of the host’s immune system to respond to other pathogens or vaccines [34–35]. A. lumbricoides and Onchocerca volvulus, parasites commonly found in immigrant populations, have been found to impair immune response to both acute (Vibrio) and chronic (Mycobacteria) infection [36]. High rates of latent TB infection have been noted in a number of refugee screening studies [37]. With reactivation of latent TB often occurring within the ?rst few years of immigration, it is conceivable that untreated helminthes infections contribute to this important public health problem. It is possible that presence of non-pathogenic helminthes in patients with malabsorption syndrome may be changing the course of underlying cause of malabsorption by means of altering the host immune response. In conclusion, celiac disease was the commonest cause of sporadic malabsorption syndrome in both adults and children. Cryptosporidium spp. was common in malnourished children, but rare in adults. More than 80% of both children and adult patients with malabsorption syndrome were infected with either pathogenic or non-pathogenic parasites, which was signi?cantly more than the rate for healthy individuals.

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