Pathophysiology of the Gastrointestinal Phase

  • Gilbert A. Castro
  • Graham R. Bullick


Physiological alterations associated with the gastrointestinal (GI) phase of trichinosis are considered using a format based on several physiological and pathological principles. Since physiology involves a study of structure-function relationships, and abnormal biochemistry and physiology generally accompany abnormal morphology, both structural and functional tissue changes are considered. Qualitative and quantitative aspects of pathogenesis of infection with Trichinella spiralis are conditioned by prior contact with the parasite. Because of this, some attention is given to the onset and expression of structural-functional changes as they occur in primary as compared with secondary infection. Although it is quite evident that the degree of pathological damage in trichinosis is influenced in part by the intensity of infection, pathophy- siological changes are considered primarily with regard to their presence in the host, not with regard to the size of the infective inoculum.


Lamina Propria Primary Infection Secondary Infection Pancreatic Secretion Intestinal Transit 
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  1. Barker, I.K., 1973, Scanning electron microscopy of the duodenal mucosa of lambs infected with Trichostrongylus colubriformis, Parasitology 67: 307–314.PubMedCrossRefGoogle Scholar
  2. Binder, H.J., (ed.), 1979, Mechanisms of Intestinal Secretion, Kroc Foundation Series, Vol. 12, Alan R. Liss, New York.Google Scholar
  3. Bowen, J.C., Paddack, G.L., Bush, J.C., Wilson, R.J., and Johnson, L.R., 1978, Comparison of gastric responses to small intestinal resection and bypass in rats, Surgery 83: 402–405.PubMedGoogle Scholar
  4. Bullick, G., Frizzell, R., and Castro, G.A., 1981, Change in epithelial transport with rapid immune rejection of Trichinella spiralis, Program and abstracts, 56th Annual Meeting of the American Society of Parasitologists, Abstract No. 13.Google Scholar
  5. Campbell, C.H., 1955, The antigenic role of the excretions and secretions of Trichinella spiralis in the production of immunity in mice, J. Parasitol. 41: 483–491.PubMedCrossRefGoogle Scholar
  6. Castro, G.A., 1976, Spatial and temporal integration of host responses to intestinal stages of Trichinella spiralis: Retro-and prospective views, in: Biochemistry of Parasites and Host-Parasite Relationships (H. Van den Bossche, ed.), North-Holland, New York, pp. 343–358.Google Scholar
  7. Castro, G.A., and Fairbairn, D., 1969, Carbohydrates and lipids of T. spiralis larvae and their utilization in vitro, J. Parasitol. 55: 51–58.PubMedCrossRefGoogle Scholar
  8. Castro, G.A., and Gentner, H., 1972, Disaccharidase deficiency associated with the intestinal phase of trichinosis in guinea pigs, Proc. Soc. Exp. Biol. Med. 140: 342–345.PubMedGoogle Scholar
  9. Castro, G.A., and Olson, L.J., 1967, Relationship between body weight and food and water intake in Trichinella spiralis-infected guinea pigs, J. Parasitol. 53: 589–594.PubMedCrossRefGoogle Scholar
  10. Castro, G.A., Olson, L.J., and Baker, R.D., 1967, Glucose malabsorption and intestinal histopathology in Trichinella spiralis-infected guinea pigs, J. Parasitol. 53: 595–612.PubMedCrossRefGoogle Scholar
  11. Castro, G.A., Ferguson, J.D., and Gorden, C.W., 1973, Amine excretion in excysted larvae and adults of Tnchinella spiralis, Comp. Biochem. Physiol. 45A: 819–828.CrossRefGoogle Scholar
  12. Castro, G.A., Roy, S.A., and Stockstill, R., 1974, Trichinella spiralis: Peroxidase activity in isolated cells from the rat small intestine, Exp. Parasitol. 36: 307–315.PubMedCrossRefGoogle Scholar
  13. Castro, G.A., Badial-Aceves, F., Smith, J.W., Dudrick, S.J., and Weisbrodt, N.W., 1976a, Altered small bowel propulsion associated with enteric parasitism, Gastroenterology 71: 620–625.PubMedGoogle Scholar
  14. Castro, G.A., Copeland, E.M., Dudrick, S.J., and Johnson, L.R., 1976b, Serum and antral gastrin levels in rats infected with intestinal parasites, Am. J. Trop. Med. Hyg. 25: 848–853.PubMedGoogle Scholar
  15. Castro, G.A., Post, C.A., and Roy, S.A., 1977, Intestinal motility during the enteric phase of trichinellosis in immunized rats, J. Parasitol. 63: 713–719.PubMedCrossRefGoogle Scholar
  16. Castro, G.A., Hessel, J J., and Whalen, G., 1979a, Altered intestinal fluid movement in response to Trichinella spiralis in immunized rats, Parasite Immunol. 1: 259–266.PubMedCrossRefGoogle Scholar
  17. Castro G.A., Copeland, E.M., Dudrick, S.J., and Ramaswamy, K., 1979b, Enterai and parenteral feeding to evaluate malabsorption in intestinal parasitism, Am. J. Trop. Med. Hyg. 28: 500–507.PubMedGoogle Scholar
  18. Catty, D., 1969, The immunology of nematode infections: Trichinosis in guinea pigs as a model, in: Monograph in Allergy, Vol. 5 (P. Kalles, M. Hasek, T.M. Inderbitzen, P.A. Miescher, and B.H. Waksman, eds.), S. Karger, New York, p. 134.Google Scholar
  19. Charniga, L., Stewart, G.L., Kramar, G.W., and Stanfield, J.S., 1981, The effects of host sex on enteric response to infection with Trichinella spiralis, J. Parasitol. 67: 917–922.PubMedCrossRefGoogle Scholar
  20. Coulson, E.J., 1953, The Schultz-Dale technique, J. Allergy 24: 458–473.PubMedCrossRefGoogle Scholar
  21. Crandall, R.B., 1965, Chemotactic response of polymorphonuclear leukocytes to Trichinella spiralis and Ascaris suum extracts, J. Parasitol. 51: 397–404.PubMedCrossRefGoogle Scholar
  22. Crane, R.K., 1975, The physiology of the intestinal absorption of sugars, in: Physiological Effects of Food Carbohydrates, American Chemical Symposium Series No. 15 (A. Jeanes and J. Hodge, eds.), American Chemical Society, Washington, D.C., pp. 1–37.Google Scholar
  23. Cutz, E., Chan, W., Track, N.S., Goth, A., and Said, S.I., 1978, Release of vasoactive intestinal polypeptide in mast cells by histamine liberators, Nature (London) 275: 661–662.CrossRefGoogle Scholar
  24. Dembinski, A.B., Johnson, L.R., and Castro, G.A., 1979a, Influence of parasitism on secretin-inhibited gastric secretion, Am. J. Trop. Med. Hyg. 28: 854–859.PubMedGoogle Scholar
  25. Dembinski, A.B., Johnson, L.R., and Castro, G.A., 1979b, Influence of enteric parasitism on hormone-regulated pancreatic secretion in dogs, Am. J. Physiol. 237: R232–R238.PubMedGoogle Scholar
  26. Dowling, R.H., and Riecker, E.O., 1973, Intestinal Adaptation, Proceedings of the International Conference on the Anatomy, Physiology and Biochemistry of Intestinal Adaptation, Titisee, Germany (May 1973), Schattauer, New York, p. 271.Google Scholar
  27. Ewert, A., and Olson, L.J., 1961, The use of a mouse LD5O to evaluate the immunogenicity of Trichinella spiralis metabolic antigens, Tex. Rep. Biol. Med. 19: 580–584.PubMedGoogle Scholar
  28. Ferguson, A., and Jarrett, E.E., 1975, Hypersensitivity reactions in the small intestine. I. Thymus dependence of experimental partial villous atrophy, Gut 16: 114–117.PubMedCrossRefGoogle Scholar
  29. Ferguson, A., and MacDonald, T.T., 1979, Effects of local delayed hypersensitivity on the small intestine, in: Symposium on Immunology of the Gut, Ciba Foundation Symposium, 46, New Series, Elsevier/North-Holland, New York, pp. 305–327.Google Scholar
  30. Field, M., 1980, Regulation of small intestinal ion transport by cyclic nucleotides and calcium, in: Secretory Diarrhea (M. Field, J.S. Fordtran, and S. Schultz, eds.), American Physiological Society, Bethesda, Maryland, pp. 21–30.Google Scholar
  31. Field, M., Fordtran, J.S., and Schultz, S. (eds.), 1980, Secretory Diarrhea, American Physiological Society, Bethesda, Maryland.Google Scholar
  32. Furth, R.J. van, Hirsh, J.G., and Fedorko, M.E., 1970, Morphology and peroxidase cytochemistry of mouse promonocytes, monocytes, and macrophages, J. Exp. Med. 132: 794–812.PubMedCrossRefGoogle Scholar
  33. Gould, S.E., 1970a, Clinical manifestations, A. Symptomatology, in: Trichinosis in Man and Animals (S.E. Gould, ed.), Charles C. Thomas, Springfield, Illinois, pp. 269–306.Google Scholar
  34. Gould, S.E., 1970b, Anatomic pathology, in: Trichinosis in Man and Animals (S.E. Gould, ed.), Charles C. Thomas, Springfield, Illinois, pp. 147–189.Google Scholar
  35. Graham, R.C., Jr., and Karnovsky, M.J., 1966, The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: Ultrastructural cytochemistry by a new technique, J. Histochem. Cytochem. 14: 291–302.PubMedCrossRefGoogle Scholar
  36. Gustowska, L., Ruitenberg, E.J., and Elgersma, A., 1980, Cellular reactions in tongue and gut in murine trichinellosis and their thymus dependence, Parasite Immunol. 2: 133–154.CrossRefGoogle Scholar
  37. Haskins, W.T., and Weinstein, P.P., 1957a, The amine excretory products of Ascaris lumbricoides and Trichinella spiralis larvae, J. Parasitol. 43: 28–32.PubMedCrossRefGoogle Scholar
  38. Haskins, W.T., and Weinstein, P.P., 1957b, Nitrogenous excretory products of Trichinella spiralis larvae, J. Parasitol. 43: 19–24.PubMedCrossRefGoogle Scholar
  39. Hessel, J.J., Ramaswamy, K., and Castro, G.A., 1982, Rapid change in enterocyte absorptive capacity in immune hosts after challenge with Trichinella spiralis, J. Parasitol. 68: 202–207.PubMedCrossRefGoogle Scholar
  40. Ivey, M.H., 1965, Immediate hypersensitivity and serological responses in guinea pigs infected with Toxocara canis or Trichinella spiralis, Am. J. Trop. Med. Hyg. 14: 1044–1051.PubMedGoogle Scholar
  41. Jensen, L.J., and Castro, G.A., 1981, Trichinella spiralis: Generation in vitro of factors chemotactic for rat cells in the presence of rat serum, Exp. Parasitol. 52: 53–61.PubMedCrossRefGoogle Scholar
  42. Johnson, L.R., and Grossman, M.I., 1968, Secretin, the enterogasterone released by acid in the duodenum, Am. J. Physiol. 215: 885–888.PubMedGoogle Scholar
  43. Johnson, L.R., and Grossman, M.I., 1969, Characteristics of inhibition of gastric secretion by secretin, Am. J. Physiol. 217: 1401–1404.PubMedGoogle Scholar
  44. Kimberg, D.V., Field, M., Johnson, J., Henderson, A., and Gershow, E., 1971, Stimulation of intestinal adenylate cyclase by cholera enterotoxin and prostaglandins, J. Clin. Invest. 50: 1218–1230.PubMedCrossRefGoogle Scholar
  45. Kozek, W.J., and Crandall, R.B., 1974, Intestinal and serum immunoglobulins and antibodies in mice infected with Trichinella, in: Trichinellosis, Proceedings of the 3rd International Conference on Trichinellosis (C.W. Kim, ed.), Intext, New York, pp. 157–164.Google Scholar
  46. Kramar, M., Stewart, G.L., and Charniga, L., 1981. Comparative study of Trichinella spiralis (Owen, 1835) and Tnchinella pseudospiralis (Garkavi, 1972), J. Parasitol. 67: 911–916.PubMedCrossRefGoogle Scholar
  47. Larsh, J.E., Jr., 1947, The relationship in mice of intestinal emptying time and natural resistance to Hymenolepis, J. Parasitol. 33: 79–84.PubMedCrossRefGoogle Scholar
  48. Larsh, J.E., Jr., 1963, Experimental trichinosis, Adv. Parasitol. 1: 213–286.PubMedCrossRefGoogle Scholar
  49. Larsh, J.E., Jr., and Hendricks, J.R., 1949, The probable explanation for the difference in the localization of adult Tnchinella spiralis from rats, J. Parasitol. 35: 101–106.PubMedCrossRefGoogle Scholar
  50. Larsh, J.E., Jr., and Race, G.J., 1954, A histopathological study of the anterior small intestine of immunized and non-immunized mice infected with Trichinella spiralis, J. Infect. Dis. 38: 262–272.CrossRefGoogle Scholar
  51. Larsh, J.E., Jr., Ottolenghi, A., and Weatherly, N.F., 1974, Trichinella spiralis: Phospholipase in challenged mice and rats, Exp. Parasitol. 36: 299–306.PubMedCrossRefGoogle Scholar
  52. Lee, G.B., and Ogilvie, B.M., 1980, The mucus layer in nematode infections, in: The Mucosal Immune System in Health and Disease, Proc. 81st Ross Conf. on Pediatric Res. Ross Laboratories, Columbus, Ohio, pp. 175–182.Google Scholar
  53. Leid, R.W., and Williams, J.F., 1979, Helminth parasites and the host inflammatory system, Chem. Zool. 11: 229–266.Google Scholar
  54. Leonard, A.B., and Beahm, E.H., 1941, Studies on the distribution of Trichinella larvae in the albino rat, Trans. Kans. Acad. Sci. 44: 419–433.Google Scholar
  55. Lichtenberger, L.M., and Graziani, L.A., 1981, Possible importance of dietary ammonia (NH3) in the postprandial release of gastrin (G), Gastroenterology 30(Pt. 2): 1212.Google Scholar
  56. Lichtenberger, L.M., Lechago, J., and Johnson, L.R., 1975, Depression of antral and serum gastrin concentration by food deprivation in the rat, Gastroenterology 68: 1473–1479.PubMedGoogle Scholar
  57. Lin, T.-M., and Olson, L.J., 1970, Pathophysiology of reinfection with Trichinella spiralis in guinea pigs during the intestinal phase, J. Parasitol. 56: 529–539.PubMedCrossRefGoogle Scholar
  58. Manson-Smith, D.F., 1979, Villous atrophy and expulsion of intestinal Trichinella spiralis are mediated by T cells, Cell Immunol. 47: 285–292.PubMedCrossRefGoogle Scholar
  59. McCoy, O.R., 1940, Rapid loss of trichinella larvae fed to immune rats and its bearing of the mechanism of immunity, Am. J. Hyg. 32: 105–116.Google Scholar
  60. Miller, H.R.P., and Nawa, T., 1979, Nippostrongylus brasiliensis: Intestinal goblet cell response in adoptively immunized rats, Exp. Parasitol. 47: 81–90.PubMedCrossRefGoogle Scholar
  61. Mills, C.K., and Kent, N.H., 1965, Excretions and secretions of Trichinella spiralis and their role in immunity, Exp. Parasitol. 16: 300–310.PubMedCrossRefGoogle Scholar
  62. Olson, L.J., and Richardson, J.A., 1968, Intestinal malabsorption of D-glucose in mice infected with Trichinella spiralis, J. Parasitol. 54: 441–451.CrossRefGoogle Scholar
  63. Olson, L.J., and Schultz, C.W., 1963, Nematode induced hypersensitivity reactions in guinea pigs: Onset of eosinophilia and positive Schultz-Dale reactions following graded infections with Toxocara canis, Ann. N.Y. Acad. Sci. 113: 440–445.PubMedCrossRefGoogle Scholar
  64. Palmer, J.M., Weisbrodt, N.W., and Castro, G.A., 1981, Small intestinal myoelectric activity during intestinal trichinellosis in the rat, Program and abstracts, 56th Annual Meeting of the American Society of Parasitologists, Abstract No. 154.Google Scholar
  65. Pambuccian, G., and Cironeanu, F.I., 1961, Observations on experimental trichinellosis in white rats, Rum. Med. Rev. 6(2): 8–13.Google Scholar
  66. Polak, J.M., Pearse, A.G.E., Garaud, J.C., and Bloom, S.R., 1974, Cellular localization of a vasoactive intestinal peptide in the mammalian and avian gastrointestinal tract, Gut 15: 720–724.PubMedCrossRefGoogle Scholar
  67. Race, G.J., Larsh, J.E., Jr., Martin, J.H., and Weatherly, N.F., 1974, Light and electron microscopy of the intestinal tissue of mice parasitized by Trichinella spiralis, in: Trichinellosis, Proceedings the 3rd International Conference on Trichinellosis (C.W. Kim, ed.), Intext, New York, pp. 75–100.Google Scholar
  68. Rogers, W.P., 1942, The metabolism of trichinosed rats during the intermediate phase of the disease, J. Helminthol. 20: 139–158.CrossRefGoogle Scholar
  69. Ruitenberg, E.J., and Elgersma, A., 1976, Absence of intestinal mast cell response in congenitally athymic mice during Trichinella spiralis infection, Nature (London) 264: 258–260.CrossRefGoogle Scholar
  70. Ruitenberg, E.J., and Elgersma, A., 1979, A response of intestinal globule leucocytes in the mouse during a Trichinella spiralis infection and its dependence on intestinal mast cells, Br. J. Exp. Pathol. 60: 246–251.PubMedGoogle Scholar
  71. Ruitenberg, E.J., Elgersma, A., Kruizinga, W., and Leenstra, F., 1977a, Trichinella spiralis infection in congenitally athymic (nude) mice; Parasitological, serological and haematological studies with observations on intestinal pathology, Immunology 33: 581–587.PubMedGoogle Scholar
  72. Ruitenberg, E.J., Elgersma, A., Kruizinga, W., and Leenstra, F., 1977b, Thymus dependence and independence of intestinal pathology in a Trichinella spiralis infection: A study in congenitally athymic (nude) mice, Br.J. Exp. Pathol. 58: 311–314.PubMedGoogle Scholar
  73. Ruitenberg, E.J., Elgersma, A., and Kruizinga, W., 1979, Intestinal mast cells and globule leukocytes: Role of the thymus on their presence and proliferation during a Trichinella spiralis infection in the rat, Int. Arch. Allergy Appl. Immunol. 60: 302–309.PubMedCrossRefGoogle Scholar
  74. Ruitenberg, E.J., Perrudet-Badoux, A., Boussac-Aron, Y., and Elgersma, A., 1980, Trichinella spiralis infection in animals genetically selected for high and low antibody production: Studies on intestinal pathology, Int. Arch. Allergy Appl. Immunol. 62: 104–110.PubMedCrossRefGoogle Scholar
  75. Russell, D.A., and Castro, G.A., 1979, Physiological characterization of a biphasic immune response to Trichinella spiralis in the rat, J. Infect. Dis. 139: 304–312.PubMedCrossRefGoogle Scholar
  76. Schanbacher, L.M., Nations, J.K., Weisbrodt, N.W., and Castro, G.A., 1978, Intestinal myoelectric activity in parasitized dogs, Am. J. Physiol. 234: R188–R195.PubMedGoogle Scholar
  77. Schultz, S.G., and Zelusky, R., 1964, Ion transport in isolated rabbit ileum. I. Short-circuit current and Na fluxes, J. Gen. Physiol. 47: 567–584.PubMedCrossRefGoogle Scholar
  78. Schwartz, C.J., Kimberg, D.V., Sheerin, H.E., Field, M., and Said, S.I., 1974, Vasoactive intestinal peptide stimulation of adenylate cyclase and active electrolyte secretion in intestinal mucosa, J. Clin. Invest. 54: 536–544.PubMedCrossRefGoogle Scholar
  79. Sheehy, T.W., Meroney, W.H., Cox. R.S., Jr., and Sola, J.E., 1962, Hookworm disease and malabsorption, Gastroenterology 42: 148–156.PubMedGoogle Scholar
  80. Smith, J.W., and Castro, G.A., 1978, Relation of peroxidase activity in gut mucosa to inflammation, Am. J. Physiol. 234: R72–R79.PubMedGoogle Scholar
  81. Snook, J.T., 1973, Protein digestion in nutritional metabolic considerations, in: World Review of Nutrition and Dietetics, Vol. 18 (G.H. Bourne, ed.), S. Karger, New York, pp. 121–176.Google Scholar
  82. Sprinz, H., 1962, Morphological response of intestinal mucosa to enteric bacteria and its implication in sprue and Asiatic cholera, Fed. Proc. Fed. Am. Soc. Exp. Biol. 21: 57–64.Google Scholar
  83. Symons, L.E.A., and Fairbairn, D., 1962, Pathology, absorption, transport and activity of digestive enzymes in rat jejunum parasitized by the nematode Nippostrongylus brasi-liensis, Fed. Proc. 21: 913–918.PubMedGoogle Scholar
  84. Takeuchi, A., Sprinz, H., Labrec, E.H., and Formal, S.B., 1965, Experimental bacillary dysentery, Am. J. Pathol. 47: 1011–1044.PubMedGoogle Scholar
  85. Tanner, C.E., and Gregory, J., 1961, Immunochemical study of the antigens of Trichinella spiralis. I. Identification and enumeration of antigens, Can. J. Microbiol. 7: 473–481.PubMedCrossRefGoogle Scholar
  86. Ussing, H.H., and Zerahn, K., 1951, Active transport of sodium as the source of electric current in the short circuited isolated frog skin, Acta Physiol. Scand. 23: 110–127.PubMedCrossRefGoogle Scholar
  87. Vagne, M., and Grossman, M.I., 1968, Cholecystokinetic potency of gastrointestinal hormones and related peptides, Am. J. Physiol. 215: 881–884.PubMedGoogle Scholar
  88. Von Brand, T., Weinstein, P.P., Mehlman, B., and Weinbach, E.C., 1952, Observations on the metabolism of bacteria-free larvae of Trichinella spiralis, Exp. Parasitol. 1: 245–255.CrossRefGoogle Scholar
  89. Warren, K.S., Karp, R., and Pelly, R.P., 1976, The eosinophil stimulation promoter in murine and human Trichinella spiralis infection, J. Infect. Dis. 134: 277–280.PubMedCrossRefGoogle Scholar
  90. Weisbrodt, N.W., Badial-Aceves, F., Dudrick, S.J., Burks, T., and Castro, G.A., 1977, Tolerance to the effect of morphine on intestinal transit, Proc. Soc. Exp. Biol. Med. 154: 587–590.PubMedGoogle Scholar
  91. Wine, A.C., Stone, M.K., and Mahmond, A.A.F., 1977, Eosinophil chemotaxis by products of antigen-stimulated spleen cells, Clin. Res. 25: 351A.Google Scholar

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© Plenum Press, New York 1983

Authors and Affiliations

  • Gilbert A. Castro
    • 1
  • Graham R. Bullick
    • 1
  1. 1.Department of Physiology and Cell BiologyUniversity of Texas Medical School at HoustonHoustonUSA

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