Eosinophil activity in Schistosoma mansoni infections in vivo and in vitro in relation to plasma cytokine profile pre- and posttreatment with praziquantel

Clinical and Vaccine Immunology

Volumn 13, Issue 5, 2006, Pages 584-593

  Reimert, Claus M ^a   Fitzsimmons, Colin M ^b   Joseph, Sarah ^b   Mwatha, Joseph K ^c   Jones, Frances M ^b   Kimani, Gachuhi ^c   Hoffmann, Karl F ^b   Booth, Mark ^b   Kabatereine, Narcis B ^d   Dunne, David W ^b   Vennervald, Birgitte J ^a  

^a DANISH BILHARZIASIS LABORATORY   (Denmark)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^d MINISTRY OF HEALTH   (Uganda)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; EOSINOPHIL CATIONIC PROTEIN; EOSINOPHIL PROTEIN X; EOTAXIN; INTERLEUKIN 10; INTERLEUKIN 5; INTERLEUKIN 6; PARASITE ANTIGEN; PRAZIQUANTEL; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANAPHYLAXIS; ARTICLE; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE SEVERITY; EOSINOPENIA; EOSINOPHIL COUNT; EOSINOPHILIA; FISHERMAN; FOLLOW UP; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; UGANDA;

ADOLESCENT; ADULT; ANIMALS; ANTIGENS, HELMINTH; CELLS, CULTURED; CYTOKINES; EOSINOPHIL CATIONIC PROTEIN; EOSINOPHIL-DERIVED NEUROTOXIN; EOSINOPHILS; HUMANS; IMMUNOLOGIC FACTORS; MALE; PRAZIQUANTEL; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI;

EID: 33646681006     PISSN: 15566811     EISSN: None     Source Type: Journal    
DOI: 10.1128/CVI.13.5.584-593.2006     Document Type: Article

References (72)

1. Ackerman, S. J., G. M. Kephart, F. H. Francis, K. Awadzi, G. J. Geich, and E. A. Ottesen. 1990. Eosinophil degranulation. An immunologic determinant in the pathogenesis of the Mazzotti reaction in human onchocerciasis. J. Immunol. 144:3961-3969.
2. Akdis, C. A., T. Blesken, M. Akdis, B. Wuthrich, and K. Blaser. 1998. Role of interleukin 10 in specific immunotherapy. J. Clin. Investig. 102:98-106.
3. Asadullah, K., W. Sterry, and H. D. Volk. 2003. Interleukin-10 therapy-review of a new approach. Pharmacol. Rev. 55:241-269.
4. Berhe, N., S. G. Gundersen, F. Abebe, H. Birrie, G. Medhin, and T. Gemetchu. 1999. Praziquantel side effects and efficacy related to Schistosoma mansoni egg loads and morbidity in primary school children in north-east Ethiopia. Acta Trop. 72:53-63.
5. Booij-Noord, H., K. de Vries, H. J. Sluiter, and N. G. M. Orie. 1972. Late bronchial obstructive reaction to experimental inhalation of house dust extract. Clin. Allergy 2:43-61.
6. Borish, L., A. Aarons, J. Rumbyrt, P. Cvietusa, J. Negri, and S. Wenzel. 1996. Interleukin-10 regulation in normal subjects and patients with asthma. J. Allergy Clin. Immunol. 97:1288-1296.
7. Butterworth, A. E., R. Sturrock, V. Houba, A. A. F. Mahmoud, A. Sher, and P. H. Rees. 1975. Eosinophils as mediators of antibody-dependent damage to schistosomula. Nature 256:272-279.
8. Butterworth, A. E., and K. J. I. Thorne. 1993. Eosinophils and parasitic diseases, p. 119-150. In H. Smith and R. M. Cook (ed.), Immunopharmacology of eosinophils. Academic Press, London, United Kingdom.
9. Butterworth, A. E., M. A. Vadas, D. L. Wassom, A. Dessein, M. Hogan, B. Sherry, G. J. Gleich, and J. R. David. 1979. Interactions between human eosinophils and schistosomula of Schistosoma mansoni. II. The mechanism of irreversible eosinophil adherence. J. Exp. Med. 150:1456-1471.
10. Carlson, M., L. Håkanson, M. Kämpe, G. Stålenheim, C. Peterson, and P. Venge. 1992. Degranulation of eosinophils from pollen-atopic patients with asthma is increased during pollen season. J. Allergy Clin. Immunol. 89:131-139.
11. Carlson, M., G. Oberg, C. Peterson, and P. Venge. 1994. Releaseability of human hypereosinophilic eosinophils is related to the density of the cells. Br. J. Haematol. 86:41-47.
12. Cioli, D., and L. Pica-Mattoccia. 2003. Praziquantel. Parasitol. Res. 90(Suppl. 1):3-9.
13. Clegg, J. A., S. R. Smithers, and R. J. Terry. 1971. Acquisition of human antigens by Schistosoma mansoni during cultivation in vitro. Nature 232:653-654.
14. Conrad, M. E. 1971. Hematologic manifestations of parasitic infections. Semin. Hematol. 8:267-303.
15. Cookson, W. O., C. F. Craddock, M. K. Benson, and S. R. Durham. 1989. Falls in peripheral eosinophil counts parallel the late asthmatic response. Am. Rev. Respir. Dis. 139:458-462.
16. Cooper, P. J., K. Awadzi, E. A. Ottesen, D. Remick, and T. B. Nutman. 1999. Eosinophil sequestration and activation are associated with the onset and severity of systemic adverse reactions following the treatment of onchocerciasis with ivermectin. J. Infect. Dis. 179:738-742.
17. Cooper, P. J., L. A. Beck, I. Espinel, N. M. Deyampert, A. Hartnell, P. J. Jos, W. Rardes, R. H. Guderian, and T. B. Nutman. 2000. Eotaxin and RANTES expression by dermal endothelium is associated with eosinophil infiltration after ivermectin treatment of onchocerciasis. Clin. Immunol. 95:51-61.
18. Cooper, P. J., R. H. Guderian, D. Prakash, D. G. Remick, I. Espinel, T. B. Nutman, D. W. Taylor, and G. E. Griffin. 1996. RANTES in onchocerciasis: changes with ivermectin treatment. Clin. Exp. Immunol. 106:462-467.
19. Cooper, P. J., L. B. Schwartz, A. M. Irani, K. Awadzi, R. H. Guderian, and T. B. Nutman. 2002. Association of transient dermal mastocytosis and development of adverse reactions after treatment of onchocerciasis with ivermectin. J. Infect. Dis. 186:1307-1313.
20. Dahl, R., P. Venge, and I. Olsson. 1978. Variations of blood eosinophils and eosinophil cationic protein in serum in patients with bronchial asthma. Studies during inhalation challenge test. Allergy 33:211-215.
21. David, J. R., M. A. Vadas, A. E. Butterworth, P. A. de Brito, E. M. Carvalho, R. A. David, J. C. Bina, and Z. A. Andrade. 1980. Enhanced helminthotoxic capacity of eosinophils from patients with eosinophilia. N. Engl. J. Med. 303:1147-1152.
22. Dunne, D. W., A. E. Butterworth, A. J. C. Fulford, H. C. Kariuki, J. G. Langley, J. H. Ouma, A. Capron, R. J. Pierce, and R. F. Sturrock. 1992. Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. Eur. J. Immunol. 22:1483-1494.
23. Durham, S. R., and A. B. Kay. 1985. Eosinophils, bronchial hyperreactivity and late-phase asthmatic reactions. Clin. Allergy 15:411-418.
24. Fitzsimmons, C. M., S. Joseph, F. M. Jones, C. M. Reimert, K. F. Hoffmann, F. Kazibwe, G. Kimani, J. K. Mwatha, J. H. Ouma, E. M. Tukahebwa, H. C. Kariuki, B. J. Vennervald, N. B. Kabatereine, and D. W. Dunne. 2004. Schistosomiasis chemotherapy in Ugandan fishermen: treatment can cause a rapid increase in plasma interleukin-5 levels but decreased levels of eosinophilia and worm-specific immunoglobulin E. Infect. Immun. 72:4023-4030.
25. Goldring, O. L., J. A. Clegg, S. R. Smithers, and R. J. Terry. 1976. Acquisition of human blood group antigens by Schistosoma mansoni. Clin. Exp. Immunol. 26:181-187.
26. Gopinath, R., L. E. Hanna, V. Kumaraswami, V. Perumal, V. Kavitha, V. Vijayasekaran, and T. B. Nutman. 2000. Perturbations in eosinophil homeostasis following treatment of lymphatic filariasis. Infect. Immun. 68:93-99.
27. Hagan, J. B., K. R. Bartemes, H. Kita, E. A. Ottesen, K. Awadzi, T. B. Nutman, and G. J. Gleich. 1996. Elevations in granulocyte-macrophage colony-stimulating factor and interleukin-5 levels precede post-treatment eosinophilia in onchocerciasis. J. Infect. Dis. 173:1277-1280.
28. Hagan, P., U. J. Blumenthal, M. Chaudri, B. M. Greenwood, R. J. Hayes, J. Hodgson, C. Kelly, M. Knight, A. J. G. Simpson, S. R. Smithers, and H. A. Wilkins. 1987. Resistance to reinfection with Schistosoma haematobium in Gambian children: analysis of their immune responses. Trans. R. Soc. Trop. Med. Hyg. 81:938-946.
29. Hagan, P., U. J. Blumenthal, D. Dunn, A. J. Simpson, and H. A. Wilkins. 1991. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349:243-245.
30. Hagan, P., H. A. Wilkins, U. J. Blumenthal, R. J. Hayes, and B. M. Greenwood. 1985. Eosinophilia and resistance to Schistosoma haematobium in man. Parasite Immunol. 7:625-632.
31. Joseph, S., F. M. Jones, G. Kimani, J. K. Mwatha, T. Kamau, F. Kazibwe, J. Kemijumbi, N. B. Kabatereine, M. Booth, H. C. Kariuki, J. H. Ouma, B. J. Vennervald, and D. W. Dunne. 2004. Cytokine production in whole blood cultures from a fishing community in an area of high endemicity for Schistosoma mansoni in Uganda: the differential effect of parasite worm and egg antigens. Infect. Immun. 72:728-734.
32. Kabatereine, N. B., B. J. Vennervald, J. H. Ouma, J. Kemijumbi, A. E. Butterworth, D. W. Dunne, and A. J. Fulford. 1999. Adult resistance to schistosomiasis mansoni: age-dependence of reinfection remains constant in communities with diverse exposure patterns. Parasitology 118:101-105.
33. Karanja, D. M., A. W. Hightower, D. G. Colley, P. N. Mwinzi, K. Galil, J. Andove, and W. E. Secor. 2002. Resistance to reinfection with Schistosoma mansoni in occupationally exposed adults and effect of HIV-1 co-infection on susceptibility to schistosomiasis: a longitudinal study. Lancet 360:592-596.
34. Katz, N. A., A. Chaves, and J. Pellegrino. 1972. A simple device for quantitative stool thick smear technique in schistosomiasis mansoni. Rev. Inst. Med. Trop. São Paulo 14:397-400.
35. Khalife, J., M. Capron, J. Y. Cesbron, P.-C. Tai, H. L. Taelman, and A. Capron. 1986. Role of specific IgE antibodies in peroxidase (EPO) release from human eosinophils. J. Immunol. 137:1659-1664.
36. Kimani, G., C. N. Chunge, A. E. Butterworth, T. Kamau, J. Bwayo, G. Gachihi, B. Mungai, and M. Mugambi. 1991. Eosinophilia and eosinophil helminthotoxicity in patients treated for Schistosoma mansoni infections. Trans. R. Soc. Trop. Med. Hyg. 85:489-492.
37. Kimani, G., C. N. Chunge, G. Gachihi, T. Kamau, B. Mungai, and G. M. Mkoji. 1992. Immune responses after treatment for Schistosoma mansoni infections. Scand. J. Immunol. Suppl. 11:29-33.
38. King, C. H. 2001. Epidemiology of schistosomiasis: determinants of transmission of infection, p. 115-132. In A. A. F. Mahmoud (ed.), Schistosomiasis. Imperial College Press, London, United Kingdom.
39. Krouwels, F. H., L. C. Kerstens, H. W. van der Maarel, H. J. Degenhart, and H. J. Neijens. 1995. Density of eosinophils reflects activity of disease in allergic asthmatic children. Clin. Exp. Allergy 25:1171-1178.
40. Krug, N., U. Napp, I. Enander, E. Eklund, C. H. Rieger, and U. Schauer. 1999. Intracellular expression and serum levels of eosinophil peroxidase (EPO) and eosinophil cationic protein in asthmatic children. Clin. Exp. Allergy 29:1507-1515.
41. Limaye, A. P., J. S. Abrams, J. E. Silver, K. Awadzi, H. F. Francis, E. A. Ottesen, and T. B. Nutman. 1991. Interleukin-5 and the posttreatment eosinophilia in patients with onchocerciasis. J. Clin. Investig. 88:1418-1421.
42. Limaye, A. P., E. A. Ottesen, V. Kumaraswami, J. S. Abrams, J. Regunathan, V. Vijayasekaran, K. Jayaraman, and T. B. Nutman. 1993. Kinetics of serum and cellular interleukin-5 in posttreatment eosinophilia of patients with lymphatic filariasis. J. Infect. Dis. 7:1396-1400.
43. McLaren, D. J., C. G. Peterson, and P. Venge. 1984. Schistosoma mansoni: further studies of the interaction between schistosomula and granulocyte-derived cationic proteins in vitro. Parasitology 88:491-503.
44. Meeusen, E. N. T., and A. Balic. 2000. Do eosinophils have a role in the killing of helminth parasites? Parasitol. Today 16:95-101.
45. Mehlhorn, H., B. Becker, P. Andrews, H. Thomas, and J. K. Frenkel. 1981. In vivo and in vitro experiments on the effect of praziquantel on Schistosoma mansoni. A light and electron microscopy study. Arzneimittelforschung 31:544-554.
46. Mutapi, F., P. D. Ndhlovu, P. Hagan, J. T. Spicer, T. Mduluza, C. M. Turner, S. K. Chandiwana, and M. E. Woolhouse. 1998. Chemotherapy accelerates the development of acquired immune responses to Schistosoma haematobium infection. J. Infect. Dis. 178:289-293.
47. Nakajima, H., G. J. Gleich, and H. Kita. 1996. Constitutive production of IL-4 and IL-10 and stimulated production of IL-8 by normal peripheral blood eosinophils. J. Immunol. 156:4859-4866.
48. Ottesen, E. A., and P. F. Weller. 1979. Eosinophilia following treatment of patients with schistosomiasis mansoni and Bancroft's filariasis. J. Infect. Dis. 139:343-347.
49. Owhashi, M., Y. Horii, and A. Ishii. 1983. Eosinophil chemotactic factor in schistosome eggs: a comparative study of eosinophil chemotactic factors in the eggs of Schistosoma japonicum and S. mansoni in vitro. Am. J. Trop. Med. Hyg. 32:359-366.
50. Pearlman, E., L. Toe, B. A. Boatin, A. A. Gilles, A. W. Higgins, and T. R. Unnasch. 1999. Eotaxin expression in Onchocerca volvulus-induced dermatitis after topical application of diethylcarbamazine. J. Infect. Dis. 180:1394-1397.
51. Petersen, B., R. Dahl, B. B. Larsen, and P. Venge. 1993. The effect of salmeterol on the early- and late-phase reaction to bronchial allergen and postchallange variation in bronchial reactivity, blood eosinophils, serum eosinophil cationic protein, and serum eosinophil protein X. Allergy 48:377-382.
52. Peterson, C. G., R. C. Garcia, M. Carlson, and P. Venge. 1987. Eosinophil cationic protein (ECP), eosinophil protein-X (EPX) and eosinophil peroxidase (EPO): granule distribution degranulation and characterization of released proteins, p. 1-19. In C. G. Peterson (ed.), Eosinophil granule proteins. Biochemical and functional studies. Uppsala University, Uppsala, Sweden.
53. Prin, L., M. Capron, A. B. Tonnel, O. Bletry, and A. Capron. 1983. Heterogeneity of human peripheral blood eosinophils: variability in cell density and cytotoxic ability in relation to the level and the origin of hypereosinophilia. Int. Arch. Allergy Appl. Immunol. 72:336-346.
54. Reimert, C. M., U. Minuva, A. Kharazmi, and K. Bendtzen. 1991. Eosinophil protein X/eosinophil derived neurotoxin (EPX/EDN). Detection by enzyme-linked immunosorbent assay and purification from normal human urine. J. Immunol. Methods 141:97-104.
55. Reimert, C. M., L. K. Poulsen, C. Bindslev-Jensen, A. Kharazmi, and K. Bendtzen. 1993. Measurement of eosinophil cationic protein (ECP) and eosinophil protein X/eosinophil derived neurotoxin (EPX/EDN). Time and temperature dependent spontaneous release in vitro demands standardized sample processing. J. Immunol. Methods 166:183-190.
56. Reimert, C. M., P. Venge, A. Kharazmi, and K. Bendtzen. 1991. Detection of eosinophil cationic protein (ECP) by an enzyme-linked immunosorbent assay. J. Immunol. Methods 138:285-290.
57. Reimert, C. M., P. S. Skov, and L. K. Poulsen. 1998. A microtiter assay for activation of eosinophils. Simultaneous monitoring of eosinophil adhesion and degranulation. Allergy 53:129-138.
58. Royer, B., S. Varadjalou, P. Saas, J. J. Guillosson, J. P. Kantelip, and M. Arock. 2001. Inhibition of IgE-induced activation of human mast cells by IL-10. Clin. Exp. Allergy 31:694-704.
59. Sher, A., B. F. Hall, and M. A. Vadas. 1978. Acquisition of murine major histocompatibility complex gene products by schistosomula of Schistosoma mansoni. J. Exp. Med. 148:46-57.
60. Spry, C. F. J. 1988. Eosinophils: a comprehensive review, and a guide to the scientific literature. Oxford University Press, Oxford, United Kingdom.
61. Supali, T., I. S. Ismid, P. Rückert, and P. Fischer. 2002. Treatment of Brugia timori and Wucherena bancrofti infections in Indonesia using DEC or a combination of DEC and albendazole: adverse reactions and short-term effects on microfilariae. Trop. Med. Int. Health 7:894-901.
62. Sur, S., D. G. Glitz, H. Kita, S. M. Kujawa, E. A. Peterson, D. A. Weiler, G. M. Kephart, J. M. Wagner, T. J. George, G. J. Gleich, and K. M. Leiferman. 1998. Localization of eosinophil-derived neurotoxin and eosinophil cationic protein in neutrophilic leukocytes. J. Leukoc. Biol. 63:715-722.
63. Tarleton, R. L., and W. M. Kemp. 1981. Demonstration of IgG-Fc and C3 receptors on adult Schistosoma mansoni. J. Immunol. 126:379-384.
64. Vadas, M., J. David, A. E. Butterworth, V. Houba, L. David, and N. Pisani. 1979. Comparison of the ability of eosinophils and neutrophils, and of eosinophils from patients with S. mansoni infection and normal individuals, to mediate in vitro damage to schistosomula of S. mansoni. Adv. Exp. Med. Biol. 114:677-682.
65. Vadas, M. A., J. R. David, A. E. Butterworth, V. Houba, R. F. Sturrock, L. David, R. Herson, T. A. Siongok, and R. Kimani. 1980. Functional studies on purified eosinophils and neutrophils from patients with Schistosoma mansoni infections. Clin. Exp. Immunol. 39:683-694.
66. Vadas, M. A., J. R. David, A. E. Butterworth, N. T. Pisani, and T. A. Siongok. 1979. A new method for the purification of human eosinophils and neutrophils, and a comparison of the ability of these cells to damage schistosomula of Schistosoma mansoni. J. Immunol. 122:1228-1236.
67. Van Dam, G. J., F. F. Stelma, B. Gryssels, S. T. Falcao Ferreira, I. Talla, M. Niang, J. P. Rotmans, and A. M. Deelder. 1996. Antibody response patterns against Schistosoma mansoni in a recently exposed community in Senegal. J. Infect. Dis. 173:1232-1241.
68. Venge, P., and R. Dahl. 1989. Are blood eosinophil number and activity important for the development of the late asthmatic reaction after allergen challenge? Eur. Respir. J. Suppl. 6:430s-434s.
69. Warren, K. S. 1973. Regulation of the prevalence and intensity of schistosomiasis in man: immunology or ecology? J. Infect. Dis. 127:595-609.
70. Webster, M., P. G. Fallon, A. J. Fulford, A. E. Butterworth, J. H. Ouma, G. Kimani, and D. W. Dunne. 1997. Effect of praziquantel and oxamniquine treatment on human isotype responses to Schistosoma mansoni: elevated IgE to adult worm. Parasite Immunol. 19:333-335.
71. Webster, M., A. J. C. Fulford, G. Braun, J. H. Ouma, H. C. Kariuki, J. C. Havercroft, K. Gachuhi, R. F. Sturrock, A. E. Butterworth, and D. W. Dunne. 1996. Human immunoglobulin E responses to a recombinant 22.6-kilodalton antigen from Schistosoma mansoni adult worms are associated with low intensities of reinfection after treatment. Infect. Immun. 64:4042-4046.
72. Woolhouse, M. E. J., and P. Hagan. 1999. Seeking the ghost of the worms past. Nat. Med. 5:1225-1227.