Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-29T13:23:11.822Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunomodulatory effect of various anti-parasitics: a review

Published online by Cambridge University Press:  07 December 2005

M. S. SAJID ,
Z. IQBAL ,
G. MUHAMMAD  and
M. U. IQBAL
M. S. SAJID
Affiliation:
Department of Veterinary Parasitology, Veterinary Clinical Medicine and Surgery, University of Agriculture, Faisalabad – 38040, Pakistan
Z. IQBAL
Affiliation:
Department of Veterinary Parasitology, Veterinary Clinical Medicine and Surgery, University of Agriculture, Faisalabad – 38040, Pakistan
G. MUHAMMAD
Affiliation:
Department of Veterinary Parasitology, Veterinary Clinical Medicine and Surgery, University of Agriculture, Faisalabad – 38040, Pakistan
M. U. IQBAL
Affiliation:
Department of Veterinary Parasitology, Veterinary Clinical Medicine and Surgery, University of Agriculture, Faisalabad – 38040, Pakistan
Get access Rights & Permissions [Opens in a new window]

Abstract

This paper reviews the immunomodulatory effects (immunosuppression or immunoactivation) of various anthelmintics including levamisole, fenvalerate, dieldrin, carbofuran, aminocarb, thiabendazole, fenbendazole, oxfendazole and ivermectin. The induced modulation of immune function may occur via direct and/or indirect mechanisms. The immunomodulatory effects of these anti-parasitics have been studied in a variety of bacterial (e.g. brucellosis, salmonellosis, paratuberculosis, mastitis), viral (e.g. infectious bovine rhinotracheitis, Herpes, foot and mouth disease), parasitic (e.g. onchocerciasis, coccidiosis, ascariasis, schistosomiasis) and neoplastic diseases. Some antiparasitics have also been used to boost immunity in a number of human diseases including leprosy, Hodgkin's disease, rheumatoid arthritis, and in adjuvanted therapy of colorectal cancer. The ability to stimulate the immune response of animals offers a new means of disease intervention. Future research on immunomodulatory effects of anti-parasitics, for humans and domestic farm animals, will provide additional methods of treating immunosuppressed subjects. The immunopotentiating or immunosuppressing activity of anti-parasitics will dictate whether co-administration of vaccines and anthelmintics or administration of vaccines during the window of immunoactivation is justified or not.

Keywords

immunomodulationantiparasiticslevamisolefenvaleratedieldrincarbofuranaminocarbthiabendazolefenbendazoleoxfendazoleivermectin
Type
Review Article
Information
Parasitology , Volume 132 , Issue 3 , March 2006 , pp. 301 - 313
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alex, P. C., Alikutty, K. M. and Mathew, S. ( 1995). Effect of levamisole administration on the incidence of bovine mastitis. Journal of Veterinary and Animal Science 26, 134–135.Google Scholar
Ali, D. N. and Chick, B. F. ( 1992). Effect of feed type on the pharmacokinetic disposition of oxfendazole in sheep. Research in Veterinary Science 52, 382–383.CrossRefGoogle Scholar
Ali, M. M. M., Mukhtar, M. M., Baraka, O. Z., Homeida, M. M. A., Kheir, M. M. and Mackenzie, C. D. ( 2002). Immunocompetence may be important in the effectiveness of Mectizan® (ivermectin) in the treatment of human onchocerciasis. Acta Tropica 84, 49–53.CrossRefGoogle Scholar
Babiuk, L. A. and Misra, V. ( 1981). Levamisole and bovine immunity: in vitro and in vivo effects on immune responses to herpes virus immunization. Canadian Journal of Microbiology 27, 1312–1319.CrossRefGoogle Scholar
Bernier, J., Fournier, M., Blais, Y., Lombardi, P. and Chevalier, G. ( 1988). Immunotoxicity of aminocarb. I. Comparative studies of sublethal exposure to aminocarb and dieldrin in mice. Pesticide Biochemistry and Physiology 30, 138–250.Google Scholar
Bernier, J., Hugo, P., Krzystyniak, K. and Fournier, M. ( 1987). Suppression of humoral immunity in inbred mice by dieldrin. Toxicological Letters 35, 231–240.CrossRefGoogle Scholar
Blakley, B. R. and Rousseaux, C. G. ( 1991). Effect of ivermectin on the immune response in mice. American Journal of Veterinary Research 52, 593–595.Google Scholar
Blecha, F. ( 1988). Immunomodulation: a means of diseased prevention in stressed livestock. Journal of Animal Science 66, 2084–2090.CrossRefGoogle Scholar
Bordmann, G., Rudin, W. and Favre, N. ( 1998). Immunisation of mice with phosphatidylcholine drastically reduces the parasitaemia of subsequent Plasmodium chajandi chajandi bleed-stage infections. Immunology 94, 35–40.Google Scholar
Borgsteede, F. H. M., deLeeuw, W. A. and van de Burg, W. P. J. ( 1988). A comparison of efficacy of four different long acting boluses to prevent infections with Dictyocaulus viviparous in calves. Veterinary Quarterly 10, 177–186.Google Scholar
Brieger, W. R., Awedoba, A. K. C., Eneanya, I., Hagan, M., Obguagu, K. F., Okello, D. O., Ososanya, O. O., Ovuga, E. B., Noma, M., Kale, O. O., Burnham, G. M. and Remme, J. H. ( 1998). The effects of ivermectin on Onchocercal Skin Disease and severe itching: results of a multicenter trial. Tropical Medical Institute of Health 3, 951–961.CrossRefGoogle Scholar
Brunner, C. J. and Muscoplat, C. C. ( 1980). Immunomodulatory effect of levamisole. Journal of American Veterinary Medical Association 176, 1159–1162.Google Scholar
Cabaj, W., Stankiewicz, M., Jones, W. E. and Moore, L. G. ( 1994). Fenbendazole and its effect on the immune system of the sheep. New Zealand Veterinary Journal 42, 216–220.CrossRefGoogle Scholar
Campbell, W. C. ( 1990). Benzimidazoles: veterinary uses. Parasitology Today 6, 130–133.CrossRefGoogle Scholar
Chirigos, M. A. ( 1992). Immunomodulators: current and future development and application. Thymus-Research 19, 517–520.Google Scholar
Christin, M. S., Gendron, A. D., Brousseau, P., Menard, L., Macrogliese, D. J., Cyr, D., Ruby, S. and Fournier, M. ( 2003). Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environmental Toxicology and Chemistry 22, 1127–1133.CrossRefGoogle Scholar
Chukwu, C. C. ( 1985). Serological response of cattle following Brucella abortus strain 19 vaccination and simultaneous administration of levamisole. International Journal of Zoonoses 12, 196–202.Google Scholar
Cox, W. I. ( 1988). Examining the immunologic and haematopoietic properties of an immunostimulant. Veterinary Medicine 6, 424–428.Google Scholar
Day, K. P., Spark, R., Garner, P., Raiko, A., Wenger, J. D., Weiss, N., Mitchell, G. F., Alpers, M. P. and Kazura, J. W. ( 1991). Serological evaluation of the macrofilaricidal effects of diethylcarbamazine treatment in bancroftian filariasis. American Journal of Tropical Medicine and Hygiene 44, 528–535.CrossRefGoogle Scholar
Dea-Ayuela, M. A. and Bolas-Fernandez, F. ( 1999). Trichinella antigens: a review. Veterinary Research 30, 559–571.Google Scholar
Donskaya, E., Lundy, J., Simon, R. and Goldschneider, I. ( 1982). Thiabendazole (TBZ), an immunomodulator. I. Effects on lymph node and spleen. International Journal of Immunopharmacology 4, 487–496.Google Scholar
Downey, N. E. ( 1988). Effect of treatment of first season calves with an OPRB on their immunity to lungworm in the second season. Veterinary Record 123, 571–572.CrossRefGoogle Scholar
Dvoroznakova, E., Boroskova, Z., Dubinsky, P., Velebny, S., Tomasovicova, O. and Machicka, B. ( 1998). Changes in cellular immunity in mice treated for larval toxocariosis with fenbendazole. Helminthologia 35, 4, 189–195.Google Scholar
Espinasse, J. ( 1980). Immunostimulation par le levamisole en clinique veterinaire. Cah. Med. Vet. 49, 5–13.Google Scholar
Eysker, M. and Boersema, J. H. ( 1989). Delay in timing of the oxfendazole pulse release bolus in calves in the Netherlands. Veterinary Quarterly 11, 210–215.CrossRefGoogle Scholar
Eysker, M., Boersema, J. H. and Kooyman, F. N. J. ( 1990). Immunity of calves treated with an oxfendazole pulse release bolus to challenge with Dictyocaulus viviparus. Research in Veterinary Science 48, 301–305.Google Scholar
Fenichel, R. L. and Chirigos, M. A. ( 1984). Immune Modulation Agents and their Mechanisms. Marcell Dekker, Inc, New York.
Fernie, D. S., Ripley, P. H. and Walker, P. D. ( 1983). Swine dysentery protection against experimental challenge following single-dose parentral immunization with inactivated Treponema hyodysenteriae. Research in Veterinary Science 35, 217–221.Google Scholar
Flesh, J., Harel, W. and Nelken, D. ( 1982). Immunopotentiating effect of levamisole in the prevention of bovine mastitis, fetal death and endometritis. The Veterinary Record 111, 56–57.CrossRefGoogle Scholar
Flipo, D., Bernier, J., Girard, D., Krzystyniak, K. and Fournier, M. ( 1992). Combined effect of selected insecticide on humoral immune response in mice. International Journal of Immunopharmacology 14, 747–752.CrossRefGoogle Scholar
Fournier, M., Chevalier, G., Nadeau, D., Trottier, B. and Krzystyniak, K. ( 1988). Virus-pesticide interactions with murine cellular immunity after sublethal exposure to dieldrin and aminocarb. Journal of Toxicology and Environmental Health 25, 103–118.CrossRefGoogle Scholar
Giambrone, J. J. and Klesius, P. H. ( 1985). Effect of levamisole on the response of broilers to coccidiosis vaccination. Poultry Science 54, 1033.CrossRefGoogle Scholar
Gilleard, J. S., Duncan, J. L. and Tait, A. ( 1995). Dictyocaulus viviparus: surface antigens of the L3 cuticle and sheath. Experimental Parasitology 80, 441–453.CrossRefGoogle Scholar
Gottschall, D. W., Theodorides, V. J. and Wang, R. ( 1990). The metabolism of benzimidazole anthelmintics. Parasitology Today 6, 115–124.CrossRefGoogle Scholar
Gualzata, M. D., Rudin, W., Weiss, N. and Heusser, C. H. ( 1988). The cross-reactive immune response between infective larvae and adult worms of Acanthocheilonema (Dipetalonema) viteae is dominated by phosphorylcholine. Parasite Immunology 10, 481–491.CrossRefGoogle Scholar
Gualzata, M., Weiss, N. and Heusser, C. H. ( 1986). Dipetalonema viteae: phosphorylcholine and non-phosphorylcholine antigenic determinants in infective larvae and adult worms. Experimental Parasitology 61, 95–102.CrossRefGoogle Scholar
Guerrero, J. ( 1977). Immunological modulating influence of levamisole. Proceedings of the Heartworm Symposium Atlanta, Georgia, 18–20 March 1977. American Heartworm Society, Veterinary Medicine Publishing Co., Bonner Springs, Kansas, USA, 1978, pp. 104–108.
Gunter, L., Roger, D. D. and Rudolf, G. ( 2000). Phosphorylcholine substituents in nematodes: structures, occurrence and biological implications. Biological Chemistry 381, 839–847.Google Scholar
Gutman, G. A. and Mitchell, G. F. ( 1977). Ascaris suum: location of phosphorylcholine in lung larvae. Experimental Parasitology 43, 161–168.CrossRefGoogle Scholar
Gwilt, P., Tempero, M., Kremer, A., Connolly, M. and Ding, C. ( 2000). Pharmacokinetics of levamisole in cancer patients treated with 5-fluorouracil. Cancer Chemotherapy and Pharmacology 45, 247–251.CrossRefGoogle Scholar
Hadden, J. W. ( 1994). T–cell adjuvants. International Journal of Immunopharmacology 16, 703–710.CrossRefGoogle Scholar
Harnett, W. and Harnett, M. ( 1993). Inhibition of murine B cell proliferation and down-regulation of protein kinase C levels by a phosphorylcholine-containing filarial excretory-secretory product. Journal of Immunology 151, 4829–4837.Google Scholar
Harnett, W. and Harnett, M. M. ( 1999). Phosphorylcholine: friend or foe of the immune system? Immunology Today 20, 125–129.Google Scholar
Harnett, W. and Harnett, M. M. ( 2001). Modulation of the host immune system by phosphorylcholine-containing glycoproteins secreted by parasitic filarial nematodes. Biochimica et Biophysica Acta 1539, 7–15.CrossRefGoogle Scholar
Harnett, W. and Parkhouse, R. M. E. ( 1995). Nature and function of parasitic nematode surface and excretory-secretory antigens. In Perspectives in Nematode Physiology and Biochemistry ( ed. Sood, M. L. and Kapur, J.), pp. 207–242. Narendra Publishing House, Delhi.
Harnett, W., Worms, M. J., Kapil, A., Grainger, M. and Parkhouse, R. M. E. ( 1989). Origin, kinetics of circulation and fate in vivo of the major excretory-secretory product of Acanthocheilonema viteae. Parasitology 99, 229–239.CrossRefGoogle Scholar
Hassan, A. B., Atta, A. H., Soliman, R. T. and Afifi, N. A. ( 1989). Effect of levamisole hydrochloride on the immune response to Newcastle disease virus vaccine in chicken. Indian Veterinary Journal 66, 389–394.Google Scholar
Hersey, P., Ho, K. and Werkmeister, J. ( 1981). Inhibition of suppressor T cells in pokeweed mitogen-stimulated cultures of T and B cells by levamisole in vitro and in vivo. Clinical Experimental Immunology 46, 340–349.Google Scholar
Hewlett, E. L., Hamid, O. Y., Ruffier, J. and Mahmoud, A. A. ( 1981). In vivo supression of delayed hypersensitivity by thiabendazole and diethylcarbamazine. Immunopharmcology 3, 325–332.CrossRefGoogle Scholar
Holcombe, R. F., Li, A. and Stewart, R. M. ( 1998). Levamisole and interleukin-2 for advanced malignancy. Biotherapy 11, 255–258.CrossRefGoogle Scholar
Holcombe, R. F., Milovanovic, T., Stewart, R. M. and Brodhag, T. M. ( 2001). Investigation in the role of immunomodulation for colon cancer prevention: results of an in vivo dose escalation trial of levamisole with immunologic endpoints. Cancer Detection and Prevention 25, 183–191.Google Scholar
Hugo, P., Bernier, J., Krzystyniak, K., Potworowski, E. F. and Fournier, M. ( 1988 a). Abrogation of graft-versus-host reaction by dieldrin in mice. Toxicology Letters 41, 11–22.Google Scholar
Hugo, P., Bernier, J., Krzystyniak, K. and Fournier, M. ( 1988 b). Transient inhibition of mixed lymphocyte reactivity by dieldrin in mice. Toxicology Letters 41, 1–9.Google Scholar
Irwin, M. R., Holmberg, C. A., Knight, H. D. and Hjerpe, C. A. ( 1976). Effects of vaccination against infectious bovine rhinotracheitis and simultaneous administration of levamisole on primary humoral responses in calves. American Journal of Veterinary Research 37, 223–226.Google Scholar
Jacobs, D. E., Pitt, S. R., Foster, J. and Fox, M. T. ( 1987). Interaction between chemoprophylaxis and immunity to bovine parasitic gastroenteritis and bronchitis pilot studies using an oxfendazole pulse release bolus. Research in Veterinary Science 43, 273–275.Google Scholar
Jansen, P. A. J. ( 1976). The levamisole story. Progress in Biophysiology and Moleclular Biology 20, 347–383.CrossRefGoogle Scholar
Jolicoeur, P., Fournier, M. and Krzystyniak, K. ( 1988). Suppression of microbiocidal activity of peritoneal exudate by sublethal dieldrin exposure of outbred and inbred mice. Pesticide Biochemistry and Physiology 31, 203–212.CrossRefGoogle Scholar
Kaneene, J. M. B., Okino, F. C., Anderson, R. K., Muscoplat, C. C. and Johnson, D. W. ( 1981). Levamisole potentiation of antigen specific lymphocyte blastogenic response to Brucella abortus exposed but non-responsive cattle. Veterinary Immunology and Immunopathology 2, 75–85.CrossRefGoogle Scholar
Kayatas, M. ( 2002). Levamisole treatment enhances protective antibody response to hepatitis B vaccination in haemodialysis patients. Artificial Organs 26, 492–496.CrossRefGoogle Scholar
Kehrli, M. E. Jr and Roth, J. A. ( 1990). Chemically induced immunomodulation in domestic food animals. Advances in Veterinary Science and Compararative Medicine 35, 103–119.CrossRefGoogle Scholar
Kende, M. M., Gainer, J. and Chirigos, M. ( 1984). Chemical Regulation of Immunity in Veterinary Medicine. Alan R. Liss, Inc., New York.
Khurana, R. and Chauhan, R. S. ( 2000). Immunopathological effects of fenvalerate on cell mediated immune response in sheep. Journal of Immunology and Immunopathology 2, 56–59.Google Scholar
Khurana, R. and Chauhan, R. S. ( 2003). Effect of fenvalerate on humoral immunity in sheep. Journal of Immunology and Immunopathology 5, 44–46.Google Scholar
Khurana, R., Mahipal, S. K. and Chauhan, R. S. ( 1999). Effect of pesticide on delayed type hypersensitivity reaction in sheep. Indian Journal of Animal Science 69, 880–881.Google Scholar
Kimball, E. S, Clark, M. C., Scheinder, C. R. and Persico, F. J. ( 1991). Enhancement of in vitro lipopolysaccharide-stimulated interleukin-1 production by levamisole. Clinical Immunology and Immunopathology 58, 385–398.CrossRefGoogle Scholar
Krzystyniak, K., Flipo, D., Mansour, S. and Fournier, M. ( 1989). Suppression of avidin processing and presentation by mouse macrophages after sublethal exposure to dieldrin. Immunopharmacology 18, 157–166.CrossRefGoogle Scholar
Kumran, M. R. ( 1993). Recent clinical trials with levamisole. Annals of the New York Academy of Sciences 685, 269–277.Google Scholar
Lammie, P. J., Hightower, A. W., Richards, Fo Jr., Bryan, R. T., Spencer, H. C., McNeeley, D. F., McNeeley, M. B. and Eberhard, M. L. ( 1992). Alterations in filarial antigen specific immunologic reactivity following treatment with ivermectin and diethylcarbamazine. American Journal Tropical Medicine and Hygiene 46, 292–295.CrossRefGoogle Scholar
Lapteva, L. A. ( 1988). Study of the mitotic activity of the somatic cell populations in the bone marrow of rats under the influence of benzimidazole derivatives. Bulleten 'Vsesoyuznogo Instituta Gel'mintolgii im. K. I. Skryabina 49, 32–34.Google Scholar
Lejan, C. and Asso, J. ( 1981). Induction of immunity in calves. In Current Therapy in Theriogenology ( ed. Morrow, D. A.), pp. 224–226. W. B. Saunders Company, Philadelphia.
Lowe, R. J. ( 1980). Levamisole as an immunomodulant. Veterinary Record 106, 390.CrossRefGoogle Scholar
Lundy, J. and Lovett, E. J. 3rd. ( 1978). Immunomodulation with thiabendazole: a review of immunologic properties and efficacy in combined modality cancer therapy. Cancer Treatment Reports 62, 1955–1962.Google Scholar
Lundy, J., Lovett, E. J. 3rd., Conran, P. and Goldblatt, P. J. ( 1976). Thiabendazole: a potential adjuvant in cancer therapy. Surgery 80, 636–640.Google Scholar
Lundy, J., Lovett, E. J. 3rd., Wolinsky, S. M. and Conran, P. ( 1979). Immune impairment and metastatic tumor growth: the need for an immunorestorative drug as an adjuvant to surgery. Cancer 43, 945–951.3.0.CO;2-V>CrossRefGoogle Scholar
Luty, A. J., Downham, M. D., Whilworth, J. A., Morgan, D. and Taylor, D. W. ( 1992). Immunolgical studies on onchocerciasis in Sierra Leone. 2. Cell mediated immune response after repeated treatment with ivermectin. Tropical Medicine and Parasitology 43, 54–58.Google Scholar
Maiboroda, L. A. and Shevchenko, L. L. ( 1978). Dynamic of the immunobiological reaction in hamsters infected with Ascaris and treated with thiabendazole. I Vsesoyuznyi s” ezd parazitotsenologov (Poltava, Sentyabr' 1978 g). Tezisy dokladov. Chast' 3. “Naukova Dumka”, Kiev, USSR, pp. 88–90.
Marriner, S. E. and Bogan, J. A. ( 1981). Pharmacokinetics of oxfendazole in sheep. American Journal of Veterinary Research 42, 1143–1145.Google Scholar
Meroni, P. L. and Barcellini, W. ( 1985). In vitro and in vivo effects of a new immunomodulating agent (Biostim) on human lymphocytes. International Journal of Immunopharmacology 7, 47.CrossRefGoogle Scholar
Miller, T. W., Chaiet, L., Cole, D. J., Cole, L. J., Flor, J. E., Goegelman, R. T., Gullo, V. P., Joshua, H., Kemph, A. J., Krellwitz, W. R., Monaghan, R. L., Ormond, R. E., Wilson, R. E., Albers-Schonberg, G. and Putter, I. ( 1979). Avermectins, new family of potent anthelmintic agents: Isolation and chromatographic Properties. Antimicrobial Agents and Chemotherapy 15, 368–371.CrossRefGoogle Scholar
Mitchell, G. F. and Lewers, H. M. ( 1976). Studies on immune responses to parasite antigens in mice. IV. Inhibition of an anti-DNP antibody response with antigen, DNP-Ficoll containing phosphorylcholine. International Archives of Allergy and Applied Immunology 52, 235–240.Google Scholar
Moertel, C. G., Fleming, T. R. and MacDonald, J. S. ( 1990). Levamisole and Fluorouracil for adjuvant therapy of resected colon carcinoma. New England Journal of Medicine 322, 352–358.CrossRefGoogle Scholar
Moertel, C. G., Fleming, T. R. and MacDonald, J. S. ( 1995). Fluorouracil and levamisole as effective adjuvant therapy after resection of stage III colon carcinoma: a final report. Annals of Internal Medicine 122, 321–326.CrossRefGoogle Scholar
Mojzisova, J., Hromada, R., Paulik, S., Ondrasovic, M. and Bajova, V. ( 2004). Immune response and immunomodulatory effect of levamisole in immunosuppressed dogs vaccinated against Parvo virus. Bulletin of Veterinary Institute in Pulawy 48, 93–97.Google Scholar
Mondal, D., Sinha, R. P. and Tiwary, B. K. ( 1993). Levamisole-induced immunomodulation in Mycobacterium paratuberculosis infections. Indian Veterinary Journal 70, 207–209.Google Scholar
Movsesyan, S. O., Agadzhanyan, A. M., Balayan, K. S. and Galstyan, S. Kh. ( 1988). The effect of thiabendazole and Panacur on the immune status of sheep with gastrointestinal nematodes. Biologicheskii Zhurnal Armenii 41, 633–639.Google Scholar
Mulcahy, G. and Quinn, P. J. ( 1986). A review of immunomodulators and their applications in veterinary medicine. Journal of Veterinary Pharmacology and Therapeutics 9, 119.CrossRefGoogle Scholar
Naylor, P. H. and Hadden, J. W. ( 2003). T cell-targeted immune enhancement yields effective T cell adjuvants. International Immunopharmacology 3, 1205–1215.CrossRefGoogle Scholar
Nielsen, H. and Bonde, J. ( 1986). Immunostimulation of blood monocyte function by RU 41 740 (Biostim) in patients with chronic bronchitis. Journal of Immunopharmacology 8, 589–592.CrossRefGoogle Scholar
Panigraphy, B., Grumbles, L. C., Miller, D., Naq, S. A. and Hall, C. F. ( 1979). Antibiotic induced immunosuppression and levamisole induced immunopotentiation in turkeys. Avian Diseases 23, 401–408.CrossRefGoogle Scholar
Parish, S. J., McFarlane, R. G., Familton, A. S. and Abell, T. J. ( 1996). The effect of fenbendazole on the immune system of lambs. Proceedings of New Zealand Society of Animal Production 56, 80–83.Google Scholar
Pelleteir, M., Roberge, C. J., Gauthier, M., Vandal, K., Tessier, P. A. and Girard, D. ( 2001). Activation of human neutrophils in vitro and dieldrin-induced neutrophilic inflammation in vivo. Journal of Leukocyte Biology 70, 367–373.Google Scholar
Pelletier, M., Willoughby, D. A. and Giround, J. P. ( 1978). Modulating effect of levamisole on DNA synthesis in macrophages in vitro. Journal of the Reticuloendothelial Society 24, 333–338.Google Scholar
Pery, P., Luffau, G., Charley, J., Petit, A., Rouze, P. and Bernard, S. ( 1979). Phosphorylcholine antigens from Nippostrongylus brasiliensis I. Anti-phosphocholine antibodies in infected rats and localization of phosphocholine antigens. Annals of Immunology (Inst. Pasteur) 130C, 879–888.Google Scholar
Prakash, M. S., Rao, V. M. and Reddy, V. ( 1998). Effect of levamisole on immune status of malnourished children. Journal of Tropical Pediatrics 44, 165–166.CrossRefGoogle Scholar
Quinn, P. J. ( 1990). Mechanism of actions of some immunomodulators used in veterinary medicine. Advances in Veterinary Science and Comparative Medicine 35, 43–49.CrossRefGoogle Scholar
Rao, U. R., Chandrashekar, R. and Subrahmanyam, D. ( 1987). Effect of ivermectin on serum dependent cellular interactions to Dipetalonema viteae microfilariae. Tropical Medicine and Parasitology 38, 123–127.Google Scholar
Razzaq, A. ( 2000). Immunomodulatory effect of oxfendazole in commercial chicken layers. M.Sc. Thesis, Department of Veterinary Microbiology, Faculty of Veterinary Science, University of Agriculture, Faisalabad, Pakistan.
Rehman, A. S., Fatima, A. and Jagannath, M. S. ( 1989). Effect of selenium on primary and secondary immune response in calves challenged with infectious bovine rhinotracheitis virus. Journal of Nutrition 118, 229.Google Scholar
Reiss, C. S., Herrman, J. M. and Hopkins, R. E. ( 1987). Effect of anthelmintic treatment on the immune response of mice. Laboratory Animal Science 37, 773–775.Google Scholar
Renoux, G. ( 1986). The Ten Commandments for immunotherapeutic drugs at the example of sulfer-containing agents. Comparative Immunology Microbiology and Infectious Diseases 9, 121–129.CrossRefGoogle Scholar
Renoux, G. and Renoux, M. ( 1974). Modulation of immune reactivity by phenylimidazothiazole salts in mice immunized by sheep red blood cells. Journal of Immunology 113, 779–790.Google Scholar
Renoux, G. and Renoux, M. ( 1977). Brucellosis, immunosuppression and levamisole. Lancet, 372.CrossRefGoogle Scholar
Rojas, A. F., Mickiewica, E., Feierstein, J. N., Glait, H. and Olivari, A. J. ( 1976). Levamisole in advanced human breast cancer. Lancet 1, 211.CrossRefGoogle Scholar
Roth, J. A., Kaeberle, M. L. and Hubbard, R. D. ( 1984). Attempt to use thiabendazole to improve the immune response in dexamethasone – treated or stressed cattle. Immunopharmacology 8, 121–128.CrossRefGoogle Scholar
Saini, S. S., Sharma, J. K., Joshi, V. B. and Kwarta, M. S. ( 1991). Effect of levamisole on humoral response of cow-calves vaccinated with Brucella abortus strain 19 vaccine. Indian Journal of Animal Research 25, 69–72.Google Scholar
Sajid, M. S. ( 2004). Studies on the immunomodulatory effect of ivermectin in rabbits. M.Sc. Thesis, Department of Veterinary Parasitology, Faculty of Veterinary Science, University of Agriculture, Faisalabad, Pakistan.
Sangster, N. C., Rickard, J. M., Hennessy, D. R., Steel, J. W. and Collins, G. H. ( 1991). Disposition of oxfendazole in goats and efficacy compared with sheep. Research in Veterinary Science 51, 258–263.CrossRefGoogle Scholar
Sanders, M. A., Bruce, A., Stephen, B., Nancy, I., Kerkvliet, N. I. and Kaminski, N. E. ( 1991). Symposium on indirect mechanisms of immune modulation. Fundamental and Applied Toxicology 17, 641–650.CrossRefGoogle Scholar
Savanur, N. H., Honnegowda., Krishnappa, G., Shastri, K. N. V. and Narayana, K. K. ( 1996). Effect of ivermectin on lymphocyte status in rabbits. Indian Veterinary Journal 73, 501–503.Google Scholar
Savanur, N. H., Honnegowda., Shastri, K. N. V., Krishnappa, G. and Narayana, K. K. ( 1995). Effect of ivermectin on immune response in rabbits inoculated with Salmonella antigen. Indian Veterinary Journal 72, 221–223.Google Scholar
Sceto, C., Gillespie, K. M. and Mathieson, P. W. ( 2000). Levamisole induces interleukin-18 and shifts type 1/type 2 cytokine balance. Immunology 100, 217–224.Google Scholar
Schiller, J. H., Lindstrom, M., Witt, P. L., Hank, J. A., Mahvi, D., Wagner, R. J., Sondel, P. and Borden, E. C. ( 1991). Immunological effects of levamisole in vitro. Journal of Immunotherapy 10, 297–306.CrossRefGoogle Scholar
Schimied, L. M. and Rosenbusch, C. ( 1973). Effects del levamisole sobre el indice de sueroprotection en privacunation antiaftosa. Revue de Medicina Veterinaria 54, 467–471.Google Scholar
Singh, B. P., Singhal, L. K. and Chauhan, R. S. ( 2001). Fenvelerate-induced cell mediated immunological alterations in chicken. Journal of Immunnology and Immunopathology 3, 59–62.Google Scholar
Singh, G., Singh, S. P., Sharma, L. D. and Ahmad, A. H. ( 2003). Fenvalerate-induced immunosuppression in buffaloe calves. Journal of Immunology and Immunopathology 5, 70–72.Google Scholar
Singh, K. K. and Jha, G. J. ( 1996). Effect of chronic fenvalerate (synthetic pyrethroid) intoxication on the immune response of goats to Brucella abortus strain 19 vaccine. Journal of Comparative Pathology 115, 299–303.CrossRefGoogle Scholar
Sloan, T., Docg, D. and Joyce, P. ( 1991). Identification of phosphorylcholine containing antigens of Fasciola hepatica – successful tolerisation against this epitope in experimental animals. Parasite Immunology 13, 447–455.CrossRefGoogle Scholar
Soboslay, P. T., Luder, C. G., Hoffmann, W. H., Michaelis, I., Helling, G., Heuschkel, C., Dreweck, C. M., Blanke, C. H., Pritze, S., Banla, M. and Schulz-Key, H. ( 1994). Ivermectin-facilitated immunity in onchocerciasis; activation of parasite-specific Th 1-type responses with subclinical Onchocerca volvulus infection. Clinical and Experimental Immunology 96, 238.Google Scholar
Soboslay, P. T., Dreweck, C. M., Hoffmann, W. H., Luder, C. G., Heuschkel, C., Gorgen, H., Banla, M. and Schulz-Key, H. ( 1992). Ivermectin-facilitated immunity to onchocerciasis. Reversal of lymphocytopenia, cellular anergy and deficienct cytokine production after single treatment. Clinical and Experimental Immunology 89, 407–413.Google Scholar
Stankiewicz, M., Cabaj, W., Jonas, W. E., Moore, L. G., Millar, K. and Ng Chie, W. ( 1995). Influence of ivermectin on cellular and humoral immune responses of lambs. Veterinary Immunology and Immunopathology 44, 347–358.CrossRefGoogle Scholar
Stankiewicz, M., Cabaj, W., Jonas, W. E., Moore, L. G. and Ng Chie, W. ( 1994). Oxfendazole treatment of non-parasitized lambs and its effect on the immune system. Veterinary Research Communications 18, 7–18.CrossRefGoogle Scholar
Stevenson, H. C., Green, I., Hamilton, J. M., Calabro, B. A. and Parkinson, D. R. ( 1991). Levamisole: known effects on immune system, clinical results, and future applications to the treatment of cancer. Journal of Clinical Oncology 9, 2052–2066.CrossRefGoogle Scholar
Symoens, J. and Rosenthal, M. ( 1977). Levamisole in the modulation of the immune response: the current experimental and clinical state: a Review. Journal of the Reticuloendothelial Society 21, 175–221.Google Scholar
Symoens, J., Cree, J. D. and Van Bever, W. ( 1979). Levamisole. In Pharmacological and Biochemical Properties of Drug Substances, Vol. 2. ( ed. Goldberg, N. E.), pp. 407–464. Washington Academy of Pharmacologists Association, Washington, DC.
Tall, B. G., Van Tinteren, H. and Zoetmulder, F. A. ( 2001). Adjuvants 5-FU plus levamisole in colonic or rectal cancer: improved survival in stage II and III. British Jouranl of Cancer 85, 1437–1443.Google Scholar
Theinpont, D., Vanparijs, O. F. J., Raeymaekers, A. H. M., Vanderberk, J., Demoen, P. J. A., Allewijn, F. T. N., Marsboom, R. P. H., Niemegeers, C. J. E., Schellekens, K. H. L. and Janseen, P. A. J. ( 1966). Teteramisole (R8299), a new, potent broad spectrum anthelmintic. Nature, London 209, 1084.Google Scholar
Uhlir, J. and Volf, P. ( 1992). Ivermectin: its effect on the immune system of rabbits and rats infested with ectoparasites. Veterinary Immunology and Immunopathology 34, 325–336.CrossRefGoogle Scholar
Van Der Maaten, M. J., Schmerr, M. J. F., Miller, J. M. and Sacks, J. M. ( 1983). Levamisole does not effect the virological and serological responses of bovine leukemia virus-infected cattle and sheep. Canadian Journal of Comparative Medicine 47, 474–479.Google Scholar
Vercruysse, J., Dorny, P., Berghen, P. and Frankena, K. ( 1987). Use of an oxfendazole pulse release bolus in the control of parasitic gastroenteritis and parasitic bronchitis in first season grazing calves. Veterinary Record 121, 297–300.CrossRefGoogle Scholar
Wade, M. G., Foster, W. G., Younglai, E. V., McMahon, A., Leingartner, K., Yagminas, A., Blakey, D., Fournier, M., Desaulniers, D. and Hughes, C. L. ( 2002). Effects of subchronic exposure to a complex mixture of persistent contaminants in male rats: systemic, immune and reproductive effects. Toxicological Sciences 69, 286–287.CrossRefGoogle Scholar
Webster, L. T. ( 1985). Drugs used in the chemotherapy of helminthiasis. In The Pharmacological Basis of Therapeutics, 7th Edn ( ed. Gilman, A. G., Goodman, L. S., Rall, T. W. and Murad, F.), pp. 1007–1028. MacMillan, New York.
Wenger, J. D., Forsyth, K. P. and Kazura, J. W. ( 1988). Identification of phosphorylcholine epitope-containing antigens in Brugia malayi and relation of serum epitope levels to infection status of jirds with brugian filariasis. American Journal of Tropical Medicine and Hygiene 38, 133–141.CrossRefGoogle Scholar
Wigginton, J. M. ( 1995). Reversal of ferritin-mediated immunosuppression by levamisole: a rationale for its application to management of the acquired immune deficiency syndrome (AIDS). Medical Hypotheses 44, 85–88.CrossRefGoogle Scholar
Zheng, H. J., Tao, Z. H., Cheng, W. F., Wang, S. H., Cheng, S. H., Ye, Y. M., Luo, L. F., Chen, X. R., Gan, G. B. and Piessens, W. F. ( 1991). Efficacy of ivermectin for the control of microfilaremia recurring after treatment with diethylcarbamazine. II. Immunological changes following treatment. American Journal of Tropical Medicine and Hygiene 45, 175–181.Google Scholar