Skip to main content
Bulletin of the World Health Organization logoLink to Bulletin of the World Health Organization
. 1976;54(5):485–494.

Subclinical intestinal malabsorption in developing countries

S J Baker
PMCID: PMC2366489  PMID: 800354

Abstract

Asymptomatic small intestinal disease characterized by abnormalities of structure and function has been reported from many developing countries. Abnormalities of structure include changes in villus architecture and in appearance under both the light and the electron microscope. Changes in function include abnormalities in the absorption of xylose, fat, vitamin B12, amino acids, and dipeptides and excessive faecal losses of nitrogen and energy. The etiology of the condition is unknown but appears to be closely related to exposure to the environment. The nutritional consequences of this condition have not been fully explored but for people living on marginally sufficient dietary intakes they may be extremely important.

Full text

PDF
485

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ABRAMS G. D., BAUER H., SPRINZ H. Influence of the normal flora on mucosal morphology and cellular renewal in the ileum. A comparison of germ-free and conventional mice. Lab Invest. 1963 Mar;12:355–364. [PubMed] [Google Scholar]
  2. Ament M. E., Shimoda S. S., Saunders D. R., Rubin C. E. Pathogenesis of steatorrhea in three cases of small intestinal stasis syndrome. Gastroenterology. 1972 Nov;63(5):728–747. [PubMed] [Google Scholar]
  3. BANWELL J. G., HUTT M. S., TUNNICLIFFE R. OBSERVATIONS ON JEJUNAL BIOPSY IN UGANDAN AFRICANS. East Afr Med J. 1964 Feb;41:46–54. [PubMed] [Google Scholar]
  4. Baker S. J. Geographical variations in the morphology of the small intestinal mucosa in apparently healthy individuals. Pathol Microbiol (Basel) 1973;39(3):222–237. doi: 10.1159/000162651. [DOI] [PubMed] [Google Scholar]
  5. Baker S. J., Jacob R., Mathan V. I. An evaluation of the 5 g D-xylose absorption test, with fractional urine collections, in subjects living in Southern India. Indian J Med Res. 1971 Dec;59(12):1869–1877. [PubMed] [Google Scholar]
  6. Baker S. J., Mathan V. I. Tropical enteropathy and tropical sprue. Am J Clin Nutr. 1972 Oct;25(10):1047–1055. doi: 10.1093/ajcn/25.10.1047. [DOI] [PubMed] [Google Scholar]
  7. Banwell J. G., Hutt M. R., Leonard P. J., Blackman V., Connor D. W., Marsden P. D., Campbell J. Exocrine pancreatic disease and the malabsorption syndrome in tropical Africa. Gut. 1967 Aug;8(4):388–401. doi: 10.1136/gut.8.4.388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bhat P., Shantakumari S., Rajan D., Mathan V. I., Kapadia C. R., Swarnabai C., Baker S. J. Bacterial flora of the gastrointestinal tract in southern Indian control subjects and patients with tropical sprue. Gastroenterology. 1972 Jan;62(1):11–21. [PubMed] [Google Scholar]
  9. Bornside G. H., Cohn I., Jr The normal microbial flora: comparative bacterial flora of animals and man. Am J Dig Dis. 1965 Oct;10(10):844–852. doi: 10.1007/BF02236093. [DOI] [PubMed] [Google Scholar]
  10. Brunser O., Eidelman S., Klipstein F. A. Intestinal morphology of rural Haitians. A comparison between overt tropical sprue and asymptomatic subjects. Gastroenterology. 1970 May;58(5):655–668. [PubMed] [Google Scholar]
  11. Brunser O., Reid A., Mönckeberg F., Maccioni A., Contreras I. Jejunal biopsies in infant malnutrition: with special reference to mitotic index. Pediatrics. 1966 Oct;38(4):605–612. [PubMed] [Google Scholar]
  12. Burman D. The jejunal mucosa in kwashiorkor. Arch Dis Child. 1965 Oct;40(213):526–531. doi: 10.1136/adc.40.213.526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Burman N. N., Sehgal A. K., Chakravarti R. N., Sodhi J. S., Chhuttani P. N. Morphological and absorption studies of small intestine in hookworm infestation (ankylostomiasis). Indian J Med Res. 1970 Mar;58(3):317–325. [PubMed] [Google Scholar]
  14. CREGAN J., HAYWARD N. J. The bacterial content of the healthy human small intestine. Br Med J. 1953 Jun 20;1(4824):1356–1359. doi: 10.1136/bmj.1.4824.1356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Chacko C. J., Mathan V. I., Baker S. J. Changes in the mucosal pattern of isolated loops of jejunum in albino rats. A dissection microscope study. Br J Exp Pathol. 1968 Feb;49(1):40–43. [PMC free article] [PubMed] [Google Scholar]
  16. Chacko C. J., Paulson K. A., Mathan V. I., Baker S. J. The villus architecture of the small intestine in the tropics: a necropsy study. J Pathol. 1969 Jun;98(2):146–151. doi: 10.1002/path.1710980209. [DOI] [PubMed] [Google Scholar]
  17. Cook G. C. Impairment of D-xylose absorption in Zambaian patients with systemic bacterial infections. Am J Clin Nutr. 1972 May;25(5):490–493. doi: 10.1093/ajcn/25.5.490. [DOI] [PubMed] [Google Scholar]
  18. Cook G. C., Kajubi S. K., Lee F. D. Jejunal morphology of the African in Uganda. J Pathol. 1969 Jul;98(3):157–169. doi: 10.1002/path.1710980302. [DOI] [PubMed] [Google Scholar]
  19. Cowan B., Satija V. K., Malvea B. P. Steatorrhoea in the Punjab: the results of a village survey. J Trop Med Hyg. 1971 Jun;74(6):137–140. [PubMed] [Google Scholar]
  20. DEO M. G., RAMALINGASWAMI V. REACTION OF THE SMALL INTESTINE TO INDUCED PROTEIN MALNUTRITION IN RHESUS MONKEYS. A STUDY OF CELL POPULATION KINETICS IN THE JEJUNUM. Gastroenterology. 1965 Aug;49:150–157. [PubMed] [Google Scholar]
  21. Donaldson R. M., Jr Studies on the pathogenesis of steatorrhea in the blind loop syndrome. J Clin Invest. 1965 Nov;44(11):1815–1825. doi: 10.1172/JCI105289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Drasar B. S., Shiner M., McLeod G. M. Studies on the intestinal flora. I. The bacterial flora of the gastrointestinal tract in healthy and achlorhydric persons. Gastroenterology. 1969 Jan;56(1):71–79. [PubMed] [Google Scholar]
  23. Einstein L. P., Mackay D. M., Rosenberg I. H. Pediatric xylose malabsorption in East Pakistan: correlation with age, growth retardation, and weanling diarrhea. Am J Clin Nutr. 1972 Nov;25(11):1230–1233. doi: 10.1093/ajcn/25.11.1230. [DOI] [PubMed] [Google Scholar]
  24. England N. W., O'Brien W. Appearances of the jejunal mucosa in acute tropical sprue in Singapore. Gut. 1966 Apr;7(2):128–139. doi: 10.1136/gut.7.2.128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Falaiye J. M. Present status of subclinical intestinal malabsorption in the tropics. Br Med J. 1971 Nov 20;4(5785):454–458. doi: 10.1136/bmj.4.5785.454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Falaiye J. M. Survey of d-xylose absorption and nutritional deficiencies in Nigeria. West Afr Med J Niger Pract. 1969 Jun;18(3):71–74. [PubMed] [Google Scholar]
  27. Foroozan P., Trier J. S. Mucosa of the small intestine in pernicious anemia. N Engl J Med. 1967 Sep 14;277(11):553–559. doi: 10.1056/NEJM196709142771101. [DOI] [PubMed] [Google Scholar]
  28. Gerson C. D., Kent T. H., Saha J. R., Siddiqi N., Lindenbaum J. Recovery of small-intestinal structure and function after residence in the tropics. II. Studies in Indians and Pakistanis living in New York City. Ann Intern Med. 1971 Jul;75(1):41–48. doi: 10.7326/0003-4819-75-1-41. [DOI] [PubMed] [Google Scholar]
  29. Gorbach S. L., Banwell J. G., Jacobs B., Chatterjee B. D., Mitra R., Mazumder D. N., Sen N. N. Tropical sprue and malnutrition in West Bengal. I. Intestinal microflora and absorption. Am J Clin Nutr. 1970 Dec;23(12):1545–1558. doi: 10.1093/ajcn/23.12.1545. [DOI] [PubMed] [Google Scholar]
  30. Gorbach S. L., Nahas L., Lerner P. I., Weinstein L. Studies of intestinal microflora. I. Effects of diet, age, and periodic sampling on numbers of fecal microorganisms in man. Gastroenterology. 1967 Dec;53(6):845–855. [PubMed] [Google Scholar]
  31. Halsted C. H., Sheir S., Sourial N., Patwardhan V. N. Small intestinal structure and absorption in Egypt. Influence of parasitism and pellagra. Am J Clin Nutr. 1969 Jun;22(6):744–754. doi: 10.1093/ajcn/22.6.744. [DOI] [PubMed] [Google Scholar]
  32. Harper G. P. Xylose malabsorption and growth retardation in East Pakistani children. Am J Clin Nutr. 1972 Nov;25(11):1227–1229. doi: 10.1093/ajcn/25.11.1227. [DOI] [PubMed] [Google Scholar]
  33. Hellier M. D., Radhakrishnan A. N., Ganapathy V., Gammon A., Baker S. J. Intestinal absorption in normal Indian and English people. Br Med J. 1976 Jan 24;1(6003):186–188. doi: 10.1136/bmj.1.6003.186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hermos J. A., Adams W. H., Liu Y. K., Sullivan L. W., Trier J. S. Mucosa of the small intestine in folate-deficient alcoholics. Ann Intern Med. 1972 Jun;76(6):957–965. doi: 10.7326/0003-4819-76-6-957. [DOI] [PubMed] [Google Scholar]
  35. Jensen H., Jarnum S., Hart Hansen J. P. Gastrointestinal protein loss and intestinal function in the nephrotic syndrome. Nephron. 1966;3(4):209–220. doi: 10.1159/000179536. [DOI] [PubMed] [Google Scholar]
  36. Kapadia C. R., Radhakrishnan A. N., Mathan V. I., Baker S. J. A study of the ratios of bile salt conjugates of glycine to taurine in the jejunum and ileum in patients with tropical sprue. Scand J Gastroenterol. 1971;6(4):357–361. doi: 10.3109/00365527109181133. [DOI] [PubMed] [Google Scholar]
  37. Keusch G. T., Plaut A. G., Troncale F. J. The interpretation and significance of the xylose tolerance test in the tropics. J Lab Clin Med. 1970 Apr;75(4):558–565. [PubMed] [Google Scholar]
  38. Keusch G. T. Subclinical malabsorption in Thailand. I. Intestinal absorption in Thai children. Am J Clin Nutr. 1972 Oct;25(10):1062–1066. doi: 10.1093/ajcn/25.10.1062. [DOI] [PubMed] [Google Scholar]
  39. Klipstein F. A., Beauchamp I., Corcino J. J., Maldonado M., Tomasini J. T., Maldonado N., Rubio C., Schenk E. A. Nutritional status and intestinal function among rural populations of the West Indies. II. Barrio Nuevo, Puerto Rico. Gastroenterology. 1972 Nov;63(5):758–767. [PubMed] [Google Scholar]
  40. Klipstein F. A. Recent advances in tropical malabsorption. Scand J Gastroenterol Suppl. 1970;6:93=114–93=114. [PubMed] [Google Scholar]
  41. Klipstein F. A., Samloff I. M., Schenk E. A. Tropical sprue in Haiti. Ann Intern Med. 1966 Mar;64(3):575–594. doi: 10.7326/0003-4819-64-3-575. [DOI] [PubMed] [Google Scholar]
  42. Klipstein F. A. Tropical sprue--an iceberg disease? Ann Intern Med. 1967 Mar;66(3):622–623. doi: 10.7326/0003-4819-66-3-622. [DOI] [PubMed] [Google Scholar]
  43. LAYRISSE M., BLUMENFELD N., CARBONELL L., DESENNE J., ROCHE M. INTESTINAL ABSORPTION TESTS AND BIOPSY OF THE JEJUNUM IN SUBJECTS WITH HEAVY HOOKWORM INFECTION. Am J Trop Med Hyg. 1964 Mar;13:297–305. doi: 10.4269/ajtmh.1964.13.297. [DOI] [PubMed] [Google Scholar]
  44. LINDENBAUM J. MALABSORPTION DURING AND AFTER RECOVERY FROM ACUTE INTESTINAL INFECTION. Br Med J. 1965 Aug 7;2(5457):326–329. doi: 10.1136/bmj.2.5457.326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Lindenbaum J., Alam A. K., Kent T. H. Subclinical small-intestinal disease in East Pakistan. Br Med J. 1966 Dec 31;2(5530):1616–1619. doi: 10.1136/bmj.2.5530.1616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Lindenbaum J., Gerson C. D., Kent T. H. Recovery of small-intestinal structure and function after residence in the tropics. I. Studies in Peace Corps volunteers. Ann Intern Med. 1971 Feb;74(2):218–222. doi: 10.7326/0003-4819-74-2-218. [DOI] [PubMed] [Google Scholar]
  47. Lindenbaum J., Harmon J. W., Gerson C. D. Subclinical malabsorption in developing countries. Am J Clin Nutr. 1972 Oct;25(10):1056–1061. doi: 10.1093/ajcn/25.10.1056. [DOI] [PubMed] [Google Scholar]
  48. Lindenbaum J., Kent T. H., Sprinz H. Malabsorption and jejunitis in American Peace Corps volunteers in Pakistan. Ann Intern Med. 1966 Dec;65(6):1201–1209. doi: 10.7326/0003-4819-65-6-1201. [DOI] [PubMed] [Google Scholar]
  49. Lindenbaum J., Pezzimenti J. F., Shea N. Small-intestinal function in vitamin B 12 deficiency. Ann Intern Med. 1974 Mar;80(3):326–331. doi: 10.7326/0003-4819-80-3-326. [DOI] [PubMed] [Google Scholar]
  50. Lindenbaum J. Small intestine dysfunction in Pakistanis and Americans resident in Pakistan. Am J Clin Nutr. 1968 Sep;21(9):1023–1029. doi: 10.1093/ajcn/21.9.1023. [DOI] [PubMed] [Google Scholar]
  51. Mata L. J., Urrutia J. J., Albertazzi C., Pellecer O., Arellano E. Influence of recurrent infections on nutrition and growth of children in Guatemala. Am J Clin Nutr. 1972 Nov;25(11):1267–1275. doi: 10.1093/ajcn/25.11.1267. [DOI] [PubMed] [Google Scholar]
  52. Mathan M., Mathan V. I., Baker S. J. An electron-microscopic study of jejunal mucosal morphology in control subjects and in patients with tropical sprue in southern India. Gastroenterology. 1975 Jan;68(1):17–32. [PubMed] [Google Scholar]
  53. Mathan M., Mathan V. I., Swaminathan S. P., Yesudoss S. Pleomorphic virus-like particles in human faeces. Lancet. 1975 May 10;1(7915):1068–1069. doi: 10.1016/S0140-6736(75)91832-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Mathan V. I., Swarnabai S., Baker S. J. Intestinal absorption of radioactive vitamin B 12: a comparison of plasma, faecal and urinary tests. Indian J Med Res. 1973 May;61(5):714–723. [PubMed] [Google Scholar]
  55. Mayoral L. G., Tripathy K., Bolaños O., Lotero H., Duque E., García F. T., Ghitis J. Intestinal, functional, and morphologic abnormalities in severly protein-malnourished adults. Am J Clin Nutr. 1972 Oct;25(10):1084–1091. doi: 10.1093/ajcn/25.10.1084. [DOI] [PubMed] [Google Scholar]
  56. Mayoral L. G., Tripathy K., García F. T., Klahr S., Bolaños O., Ghitis J. Malabsorption in the tropics: a second look. I. The role of protein malnutrition. Am J Clin Nutr. 1967 Aug;20(8):866–883. doi: 10.1093/ajcn/20.8.866. [DOI] [PubMed] [Google Scholar]
  57. Metz G., Jenkins D. J., Peters T. J., Newman A., Blendis L. M. Breath hydrogen as a diagnostic method for hypolactasia. Lancet. 1975 May 24;1(7917):1155–1157. doi: 10.1016/s0140-6736(75)93135-9. [DOI] [PubMed] [Google Scholar]
  58. NAIMAN J. L., OSKI F. A., DIAMOND L. K., VAWTER G. F., SHWACHMAN H. THE GASTROINTESTINAL EFFECTS OF IRON-DEFICIENCY ANEMIA. Pediatrics. 1964 Jan;33:83–99. [PubMed] [Google Scholar]
  59. Nasr K., Haghighi P., Abadi P., Lahimgarzadeh A., Hedayati H., Halstead J. A., Reinhold J. D. Idiopathic enteropathy: an evaluation in rural Iran with an appraisal of nutrient loss. Am J Clin Nutr. 1976 Feb;29(2):169–176. doi: 10.1093/ajcn/29.2.169. [DOI] [PubMed] [Google Scholar]
  60. RAWSON A., ROSENTHAL F. D. The mucosa of the stomach and small intestine in iron deficiency. Lancet. 1960 Apr 2;1(7127):730–731. doi: 10.1016/s0140-6736(60)90617-6. [DOI] [PubMed] [Google Scholar]
  61. Robins S. J., Garcia-Palmieri M., Rubio C. Low serum cholesterol levels and subclinical malabsorption. Ann Intern Med. 1967 Mar;66(3):556–567. doi: 10.7326/0003-4819-66-3-556. [DOI] [PubMed] [Google Scholar]
  62. Russell P. K., Aziz M. A., Ahmad N., Kent T. H., Gangarosa E. J. Enteritis and gastritis in young asymptomatic Pakistani men. Am J Dig Dis. 1966 Apr;11(4):296–306. doi: 10.1007/BF02233978. [DOI] [PubMed] [Google Scholar]
  63. SHEEHY T. W., MERONEY W. H., COX R. S., Jr, SOLER J. E. Hookworm disease and malabsorption. Gastroenterology. 1962 Feb;42:148–156. [PubMed] [Google Scholar]
  64. SPRINZ H., SRIBHIBHADH R., GANGAROSA E. J., BENYAJATI C., KUNDEL D., HALSTEAD S. Biopsy of small bowel of Thai people. With special reference to recovery from Asiatic cholera and to an intestinal malabsorption syndrome. Am J Clin Pathol. 1962 Jul;38:43–51. doi: 10.1093/ajcp/38.1.43. [DOI] [PubMed] [Google Scholar]
  65. Sammons H. G., Morgan D. B., Frazer A. C., Montgomery R. D., Philip W. M., Phillips M. J. Modification in the xylose absorption test as an index of intestinal function. Gut. 1967 Aug;8(4):348–353. doi: 10.1136/gut.8.4.348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Schneider R. E., Viteri F. E. Luminal events of lipid absorption in protein-calorie malnourished children; relationship with nutritional recovery and diarrhea. I. Capacity of the duodenal content to achieve micellar solubilization of lipids. Am J Clin Nutr. 1974 Aug;27(8):777–787. doi: 10.1093/ajcn/27.8.777. [DOI] [PubMed] [Google Scholar]
  67. Schneider R. E., Viteri F. E. Morphological aspects of the duodenojejunal mucosa in protein--calorie malnourished children and during recovery. Am J Clin Nutr. 1972 Oct;25(10):1092–1102. doi: 10.1093/ajcn/25.10.1092. [DOI] [PubMed] [Google Scholar]
  68. Sheehy T. W., Legters L. J., Wallace D. K. Tropical jejunitis in Americans serving in Vietnam. Am J Clin Nutr. 1968 Sep;21(9):1013–1022. doi: 10.1093/ajcn/21.9.1013. [DOI] [PubMed] [Google Scholar]
  69. Stanfield J. P., Hutt M. S., Tunnicliffe R. Intestinal biopsy in kwashiorkor. Lancet. 1965 Sep 11;2(7411):519–523. doi: 10.1016/s0140-6736(65)91474-1. [DOI] [PubMed] [Google Scholar]
  70. Stemmermann G. N. Strongyloidiasis in migrants. Pathological and clinical considerations. Gastroenterology. 1967 Jul;53(1):59–70. [PubMed] [Google Scholar]
  71. Tandon B. N., Das B. C., Saraya A. K., Deo M. G. Functional and structural studies of small bowel in ankylostomiasis. Br Med J. 1966 Mar 19;1(5489):714–716. doi: 10.1136/bmj.1.5489.714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Tandon B. N., Magotra M. L., Saraya A. K., Ramalingaswami V. Small intestine in protein malnutrition. Am J Clin Nutr. 1968 Aug;21(8):813–819. doi: 10.1093/ajcn/21.8.813. [DOI] [PubMed] [Google Scholar]
  73. Tripathy K., Duque E., Bolaños O., Lotero H., Mayoral L. G. Malabsorption syndrome in ascariasis. Am J Clin Nutr. 1972 Nov;25(11):1276–1281. doi: 10.1093/ajcn/25.11.1276. [DOI] [PubMed] [Google Scholar]
  74. Troncale F. J., Keusch G. T., Miller L. H., Olsson R. A., Buchanan R. D. Normal absorption in Thai subjects with non-specific jejunal abnormalities. Br Med J. 1967 Dec 9;4(5579):578–580. doi: 10.1136/bmj.4.5579.578. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Bulletin of the World Health Organization are provided here courtesy of World Health Organization

RESOURCES