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Parasites in Patients with Malabsorption Syndrome: A Clinical Study in Children and Adults

Abstract

Background: Intestinal parasites not only cause diarrheal diseases but also significant 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 modified 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 significantly 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 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 sero-negative. Conclusion: Celiac disease is the most common cause of malabsorption syndrome in both adults and children. These people harbor significantly 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.

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References

  1. Makharia G (2006) Where are Indian adult celiacs? Trop Gastroenterol 27:1–3

    PubMed  Google Scholar 

  2. Ramakrishna BS (1996) Malabsorption syndrome in India. Indian J Gastroenterol 15:135–141

    PubMed  CAS  Google Scholar 

  3. Farthing MJH (2002) Tropical malabsorption and tropical diarrhea. In: Feldman M, Friedman LS, Sleisenger MH (eds) Sleisenger, Fordtran’s gastrointestinal and liver disease, 7 th edn. Saunders, Philadelphia, pp 1842–1846

    Google Scholar 

  4. Brandborg LL, Goldberg SB, Breidenbach WC (1970) Human coccidiosis—a possible cause of malabsorption. N Engl J Med 283:1306–1313

    PubMed  CAS  Article  Google Scholar 

  5. de Onis M, de Onis M, Onyango AW, Borghi E, Garza C, Yang H (2006) WHO Multicentre Growth Reference Study Group. Comparison of the World Health Organization (WHO) Child Growth Standards and the National Center for Health Statistics/WHO international growth reference: implications for child health programmes. Public Health Nutr 9:942–947

    PubMed  Article  Google Scholar 

  6. Ehrenpreis ED, Salvino M, Craig RM (2001) Improving the serum d-xylose test for the identification of patients with small intestinal malabsorption. J Clin Gastroenterol 33:36–40

    PubMed  Article  CAS  Google Scholar 

  7. Van de Kamer JH, Huinink HTB, Weyers HA (1949) Rapid method for the determination of fat in feces. J Biol Chem 177:347–355

    Google Scholar 

  8. Simko V (1981) Fecal fat microscopy. Am J Gastroenterol 75:204–208

    PubMed  CAS  Google Scholar 

  9. Basic laboratory methods in medical parasitology (1991) WHO, Geneva:9–33

  10. Garcia LS, Bruckner DA, Brewer TC, Shimizu RY (1983) Techniques for the recovery and identification of cryptosporidium oocysts from stool specimens. J Clin Microbiol 18:185–190

    PubMed  CAS  Google Scholar 

  11. Weber R, Bryan RT, Owen RL, Wilcox CM, Gorelkin L, Visvesvara GS (1992) Improved light-microscopical detection of microsporidia spores in stool and duodenal aspirates. The Enteric Opportunistic Infections Working Group. N Engl J Med 326:161–166

    PubMed  CAS  Article  Google Scholar 

  12. Marsh MN, Crowe PT (1995) Morphology of the mucosal lesion in gluten sensitivity. Baillieres Clin Gastroenterol 9:273–293

    PubMed  Article  CAS  Google Scholar 

  13. Volta U, Molinaro N, Fusconi M, Cassani F, Bianchi FB (1991) IgA antiendomysial antibody test: a step forward in celiac disease screening. Dig Dis Sci 36:752–756

    PubMed  Article  CAS  Google Scholar 

  14. Unsworth DJ (1996) ACP Broadsheet No 149: September 1996. Serological diagnosis of gluten sensitive enteropathy. J Clin Pathol 49:704–711

    PubMed  Article  CAS  Google Scholar 

  15. Bhatnagar S, Gupta SD, Mathur M, Phillips AD, Kumar R, Knutton S, Unsworth DJ, Lock RJ, Natchu UC, Mukhopadhyaya S, Saini S, Bhan MK (2005) Celiac disease with mild to moderate histologic changes is a common cause of chronic diarrhea in Indian children. J Pediatr Gastroenterol Nutr 41:204–209

    PubMed  Article  Google Scholar 

  16. Report of Working Group of European Society of Paediatric Gastroenterology, Nutrition (1990) Revised criteria for diagnosis of celiac disease. Arch Dis Child 65:909–911

    Article  Google Scholar 

  17. Cook GC (1997) ‘Tropical sprue’: some early investigators favored an infective cause, but was a Coccidian protozoan involved? Gut 40:428–429

    PubMed  CAS  Google Scholar 

  18. Ortega YR, Adam D (1997) Giardia: overview and update. Clin Infect Dis 25:545–550

    PubMed  Article  CAS  Google Scholar 

  19. Sheehy TW, Meroney WH, Cox RS Jr, Soler JE (1962) Hookworm disease and malabsorption. Gastroenterology 42:148–156

    PubMed  CAS  Google Scholar 

  20. Pitchumoni CS, Floch MH (1969) Hookworm disease, malabsorption, and malnutrition. Am J Clin Nutr 22:813–816

    PubMed  CAS  Google Scholar 

  21. Mirdha BR, Samantray JC (2002) Hymenolepis nana: a common cause of paediatric diarrhea in urban slum dwellers. J Trop Pediatr 48:331–334

    PubMed  Article  Google Scholar 

  22. Kotler DP, Francisco A, Clayton F, Scholes JV, Orenstein JM (1990) Small intestinal injury and parasitic diseases in AIDS. Ann Intern Med 113:444–449

    PubMed  CAS  Google Scholar 

  23. Keating J, Bjarnason I, Somasundaram S, Macpherson A, Francis N, Price AB, Sharpstone D, Smithson J, Menzies IS, Gazzard BG (1995) Intestinal absorptive capacity, intestinal permeability and jejunal histology in HIV and their relation to diarrhea. Gut 37:623–629

    PubMed  Article  CAS  Google Scholar 

  24. Bhattacharya MK, Teka T, Faruque AS, Fuchs GJ (1997) Cryptosporidium infection in children in urban Bangladesh. J Trop Pediatr 43:282–286

    PubMed  Article  CAS  Google Scholar 

  25. Rahman M, Shahid NS, Rahman H, Sack DA, Rahman N, Hossain S (1990) Cryptosporidiosis: a cause of diarrhea in Bangladesh. Am J Trop Med Hyg 42:127–130

    PubMed  CAS  Google Scholar 

  26. Nagamani K, Rajkumari A, Gyaneshwari (2001) Cryptosporidiosis in a tertiary care hospital in Andhra Pradesh. Ind J Med Microbiol 19:215–216

    CAS  Google Scholar 

  27. Jaggi N, Rajeshwari S, Mittal SK, Mathur MD, Baveja UK (1994) Assessment of the immune and nutritional status of the host in childhood diarrhea due to Cryptosporidium. J Commun. Dis 26:181–185

    PubMed  CAS  Google Scholar 

  28. Connor BA, Shlim DR, Scholes JV, Rayburn JL, Reidy J, Rajah R (1993) Pathologic changes in the small bowel in nine patients with diarrhea associated with a coccidia-like body. Ann Intern Med 119:377–382

    PubMed  CAS  Google Scholar 

  29. Sasaki M, Tanaka A, Nishimura T, Tsujikawa T, Andoh A, Ishijuka I, Koyama S, Fujiyama Y, Kushima R (2004) A case of malabsorption syndrome caused by isosporiasis in an immunocompetent patient. J Gastroenterol 39:88–89

    PubMed  Article  Google Scholar 

  30. Mirdha BR, Kabra SK, Samantaray JC (2002) Isosporiasis in children. Indian Pediatr 39:941–944

    PubMed  Google Scholar 

  31. Garg PK, Perry S, Dorn M, Hardcastle L, Parsonnet J (2005) Risk of intestinal helminth and protozoan infection in a refugee population. Am J Trop Med Hyg 73:386–391

    PubMed  Google Scholar 

  32. Peters CS, Ronald S, William MJ, Andrea LC, Frank EK (1986) Prevalence of enteric parasites in homosexual patients attending an outpatient clinic. J Clin Microbiol 24:684–685

    PubMed  CAS  Google Scholar 

  33. Bentwich Z, Kalinkovich A, Weisman Z, Borkow G, Beyers N, Beyers AD (1999) Can eradication of helminthic infections change the face of AIDS and tuberculosis? Immunol Today 20:485–487

    PubMed  Article  CAS  Google Scholar 

  34. Elias D, Wolday D, Akuffo H, Petros B, Bronner U, Britton S (2001) Effect of deworming on human T cell responses to mycobacterial antigens in helminth-exposed individuals before and after Bacille Calmette-Guerin (BCG) vaccination. Clin Exp Immunol 123:219–225

    PubMed  Article  CAS  Google Scholar 

  35. Kullberg MC, Pearce EJ, Hieny SE, Sher A, Berzofsky JA (1992) Infection with Schistosoma mansoni alters Th1/Th2 cytokine responses to a non-parasite antigen. J Immunol 148:3264–3270

    PubMed  CAS  Google Scholar 

  36. Cooper PJ, Chico M, Sandoval C, Espinel I, Guevara A, Levine MM, Griffin GE, Nutman TB (2001) Human infection with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with the live oral cholera vaccine CVD 103-HgR. Infect Immun 69:1574–1580

    PubMed  Article  CAS  Google Scholar 

  37. Riemer K, Chin DP, Schecter GF, Reingold AL (1998) Tuberculosis among immigrants and refugees. Arch Intern Med 158:753–760

    Article  Google Scholar 

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Correspondence to B. R. Mirdha.

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Behera, B., Mirdha, B.R., Makharia, G.K. et al. Parasites in Patients with Malabsorption Syndrome: A Clinical Study in Children and Adults. Dig Dis Sci 53, 672–679 (2008). https://doi.org/10.1007/s10620-007-9927-9

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  • DOI: https://doi.org/10.1007/s10620-007-9927-9

Keywords

  • Chronic diarrhea
  • Celiac disease
  • Small intestine
  • Parasites
  • Coccidia
  • Microsporidia
  • Giardia lamblia
  • Helminthes
  • Pathogenic parasites
  • Non-pathogenic parasites