Skip to main content
SpringerLink
Log in

Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts

  • Review Article
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Experimental concurrent infection with two or more parasite species in mammalian host models may result in heterologous antagonistic and synergistic interactions ranging in magnitude from reduced/enhanced growth and fecundity to blockage/enhancement of establishment/expulsion. With some exceptions only, there is a reasonable correlation between the levels of interaction monitored by parasitological and by clinico-pathological parameters. Heterologous antagonistic interactions mediated by functional and specific immunological cross-reactivity occur between closely related parasite species exhibiting a marked immunobiological similarity. In contrast, antagonistic interactions between antigenetically more remote species of helminths, protozoan-induced resistance to helminth infection and helminth-induced suppression of concurrent protozoan infection generally appear mediated by immunologically non-specific factors like macrophage activation and inflammatory reactions. Synergistic heterologous interactions between helminths, helminth-induced enhancement of concurrent protozoan infection and interference with the development and maintenance of resistance to helminth infection in response to concurrent protozoan infection are generally thought to be mediated by non-specific parasite-induced immunosuppression. Concurrent experimental infection is very complex. There are problems and limitations in extrapolating from experimental studies on concurrent infection in laboratory animals to natural polyparasitism. This fact, coupled with the complex influence of ecological factors on the pattern and frequency of concurrent natural infection means that major consequences of natural concurrent parasite infection have not been definitively demonstrated. Appropriately planned and controlled field studies and further laboratory experiments on primate and domestic animal models are imperative for elucidation of the importance of heterologous interactions in concurrent parasite infection for the disease pattern in man and domestic stock. Experimental studies hitherto conducted on concurrent parasite infection pointing to natural heterologous interactions may be a valuable starting point for further studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abdel-Wahab MF, Powers KG, Mahmoud SS, Good WC (1974) Suppression of schistosome granuloma formation by malaria in mice. Am J Trop Med Hyg 23:915–918

    Google Scholar 

  • Aboul Atta NA, El-Sheikh HE (1981) Interaction between an early and late stages of Schistosoma mansoni and Trichinella spiralis infections in mice. J Egypt Soc Parasitol 11:321–330

    Google Scholar 

  • Aboul Atta NA, Michael AI, Farag HF (1982) The effect of Trichinella spiralis infection on Schistosoma mansoni liver granuloma. J Egypt Soc Parasitol 12:65–69

    Google Scholar 

  • Agrawal MC, Sahasrabudhe VK (1984) Factors affecting heterologous immune response in mice and rats against Schistosoma incognitum by immunisation with S. spindale. Indian Vet J 61:451–457

    Google Scholar 

  • Agrawal MC, Sahasrabudhe VK, Gehlot K (1979) Immunisation against Schistosoma incognitum in mice by administration of cercariae of Schistosoma indicum. Indian Vet J 56:682–685

    Google Scholar 

  • Agrawal MC, Sahasrabudhe VK, Shah HL (1983) Immunisation against Schistosoma incognitum in mice by administration of cercariae of Schistosoma spindale. Indian Vet J 60:321–322

    Google Scholar 

  • Alghali STO, Grencis RK (1986) Immunity to tapeworms: intraspecific cross-protective interactions between Hymenolepis citelli, H. diminuta and H. microstoma in mice. Parasitology 92:665–674

    Google Scholar 

  • Alghali STO, Hagan P, Robinson M (1985) Hymenolepis citelli (Cestoda) and Nematospiroides dubius (Nematoda): interspecific interaction in mice. Exp Parasitol 60:364–370

    Google Scholar 

  • Ali NMH, Behnke JM (1984) Non-specific immunosuppression by larval and adult Nematospiroides dubius. Parasitology 88:153–162

    Google Scholar 

  • Amin MA, Nelson GS (1969) Studies on heterologous immunity in schistosomiasis. 3. Further observations on heterologous immunity in mice. Bull WHO 41:225–232

    Google Scholar 

  • Amin MA, Nelson GS, Saoud FA (1968) Studies on heterologous immunity in schistosomiasis. 2. Heterologous schistosome immunity in rhesus monkeys. Bull WHO 38:19–27

    Google Scholar 

  • Aronstein WS, Lewis SA, Norden AP, Dalton JP, Strand M (1986) Molecular identity of a major antigen of Schistosoma mansoni which cross-reacts with Trichinella spiralis and Fasciola hepatica. Parasitology 92:133–151

    Google Scholar 

  • Ashley W (1962) The effect of a concurrent infection with Trypanosoma lewesi on the development and maintenance of acquired immunity to Nippostrongylus brasiliensis in rats. Proc Helminthol Soc Wash 29:59–62

    Google Scholar 

  • Au ACS, Ko RC (1979) Cross-resistance between Trichinella spiralis and Angiostrongylus cantonensis in laboratory rats. Z Parasitenkd 59:161–168

    Google Scholar 

  • Bailenger J, Guy M (1982) Interactions de deux parasitoses associées chez le rat: Plasmodium berghei et Strongyloides ratti. Ann Parasitol Hum Comp 57:513–526

    Google Scholar 

  • Behnke JM, Bland PW, Howard RJ, Wakelin D (1976) Expulsion of Trichinella spiralis: effect on concurrent helminth infections. Parasitology 73:xv

    Google Scholar 

  • Behnke JM, Bland PW, Wakelin D (1977) Effect of the expulsion phase of Trichinella spiralis on Hymenolepis diminuta infection in mice. Parasitology 75:79–88

    Google Scholar 

  • Behnke JM, Wakelin D, Wilson MM (1978) Trichinella spiralis: delayed rejection in mice concurrently infected with Nematospiroides dubius. Exp Parasitol 46:121–130

    Google Scholar 

  • Behnke JM, Ali NMH, Jenkins SN (1984) Survival to patency of low level infections with Trichuris muris in mice concurrently infected with Nematospiroides dubius. Ann Trop Med Parasitol 78:509–517

    Google Scholar 

  • Bindseil E (1970) Immunity to Ascaris suum. 4. The effect of different stimulations upon challenge with Ascaris suum in mice. Acta Pathol Microbiol Scand [B] 78:191–195

    Google Scholar 

  • Bindseil E, Andreassen J (1981) Effect of Ascaris suum on growth and expulsion of Hymenolepis diminuta in mice. Parasitology 83:489–496

    Google Scholar 

  • Blundell SK, Gemmell MA, Macnamara FN (1968) Immunological responses of the mammalian host against tapeworm infections. VI. Demonstration of humoral immunity in sheep induced by the activated embryos of Taenia hydatigena and T. ovis. Exp Parasitol 23:79–82

    Google Scholar 

  • Brindley PJ, Dobson C (1983) Specificity of passive serum prtection against Nippostrongylus brasiliensis and Nematospiroides dubius in mice. Aust J Exp Biol Med Sci 61:37–45

    Google Scholar 

  • Bristol JR, Pinon AJ, Mayberry LF (1983) Interspecific interactions between Nippostrongylus brasiliensis and Eimeria nieschulzi in the rat. J Parasitol 69:372–374

    Google Scholar 

  • Bruce RG, Wakelin D (1977) Immunological interactions between Trichinella spiralis and Trichuris muris in the intestine of the mouse. Parasitology 74:163–173

    Google Scholar 

  • Brumpt E (1933) Evolution de L'Hymenolepis nana var. frterna. Les deux cysticercoides. Leur importance biologique concernant l'origine du parasitisme et la signification des hÔtes intermédiaires. Arch Zool Exp Gen 75:235–246

    Google Scholar 

  • Bruna CD, Xenia B (1976) Nippostrongylus brasiliensis in mice: reduction of worm burden and prolonged infection induced by presence of Nematospiroides dubius. J Parasitol 62:490–491

    Google Scholar 

  • Buck AA, Anderson RI, MacRae AA, Fain A (1978a) Epidemiology of poly-parasitism. I. Occurrence, frequency and distribution of multiple infections in rural communities in Chad, Peru, Afghanistan and Zaire. Trop Med Parasitol 29:61–70

    Google Scholar 

  • Buck AA, Anderson RI, MacRae AA, Fain A (1978b) Epidemiology of poly-parasitism. II. Types of combinations, relative frequency and associations of multiple infections. Trop Med Parasitol 29:137–144

    Google Scholar 

  • Burden DJ, Hughes DL, Hammet NC, Collis KA (1978) Concurrent daily infection of calves with Fasciola hepatica and Ostertagia ostertagi. Res Vet Sci 25:302–306

    Google Scholar 

  • Campbell NJ, Kelly JD, Townsend RB, Dineen JK (1977) The stimulation of resistance in sheep to Fasciola hepatica by infection with Cysticercus tenuicollis. Int J Parasitol 7:347–351

    Google Scholar 

  • Campbell NJ, Dineen JK, Kelly JD (1979a) The effect of Taenia hydatigena infection on existing and concurrent infections of Fasciola hepatica in sheep. Res Vet Sci 26:391–393

    Google Scholar 

  • Campbell NJ, Kelly JD, Martin ICA (1979b) Stimulation of resistance to Taenia taeniaeformis in the rat by infection with Fasciola hepatica. Int J Parasitol 9:469–474

    Google Scholar 

  • Christensen NØ, Nansen P, Frandsen F, BjØrneboe A, Monrad J (1978) Schistosoma mansoni and Fasciola hepatica: crossresistance in mice. Exp Parasitol 46:113–120

    Google Scholar 

  • Christensen NØ, Monrad J, Nansen P, Frandsen F (1980) Schistosoma mansoni and Fasciola hepatica: cross-resistance in mice with single-sex schistosome infections. Exp Parasitol 49:116–121

    Google Scholar 

  • Christensen NØ, Nydal R, Frandsen F, Nansen P (1981a) Homologous immunotolerance and decreased resistance to Schistosoma mansoni in Echinostoma revolutum-infected mice. J Parasitol 67:164–166

    Google Scholar 

  • Christensen NØ, Nydal R, Frandsen F, Sirag SB, Nansen P (1981 b) Further studies on resistance to Fasciola hepatica and Echinostoma revolutum in mice infected with Schistosoma sp. Z Parasitenkd 65:293–298

    Google Scholar 

  • Christensen NØ, Fagbemi BO, Nansen P (1984) Trypanosoma brucei-induced blockage of expulsion of Echinostoma revolutum and of homologous E. revolutum resistance in mice. J Parasitol 70:558–561

    Google Scholar 

  • Christensen NØ, Knudsen J, Fagbemi B, Nansen P (1985) Impairment of primary expulsion of Echinostoma revolutum in mice concurrently infected with Schistosoma mansoni. J Helminthol 59:333–335

    Google Scholar 

  • Christie PR, Wakelin D, Wilson MM (1979) The effect of the expulsion phase of Trichinella spiralis on Hymenolepis diminuta infection in rats. Parasitology 78:323–330

    Google Scholar 

  • Chunge CN, Gachihi GS, Muigai R, Wasunna K, Rashid JR, Oster CN, Anabwani G (1985) Other parasitic diseases found in patients with visceral leishmaniasis. E Afr Med J 62:118–121

    Google Scholar 

  • Colwell DA, Wescott RB (1973) Prolongation of egg production of Nippostrongylus brasiliensis in mice concurrently infected with Nematospiroides dubius. J Parasitol 59:216

    Google Scholar 

  • Conchedda M, Ferretti G (1983) Vaccination of susceptible hosts with uninfective strains of the same parasite (Taenia taeniaeformis, Cestoda) provide protection against an infective strain. J Parasitol 69:1166–1167

    Google Scholar 

  • Copeland D, Grove DI (1979) Effects of Toxoplasma gondii (Gleadle strain) on the host-parasite relationship in trichinosis. Int J Parasitol 9:205–211

    Google Scholar 

  • Courtney CH, Forrester DJ (1973) Interspecific interactions between Hymenolepis microstoma (Cestoda) and Heligmosomoides polygyrus (Nematoda) in mice. J Parasitol 59:480–483

    Google Scholar 

  • Cox FEG (1975) Factors affecting infections of mammals with intraerythrocytic protozoa. Symp Soc Exp Biol 29:429–451

    Google Scholar 

  • Cox HW (1952) The effect of concurrent infection with the dog hookworm, Ancylostoma caninum, on the natural and acquired resistance of mice to Trichinella spiralis. J Elisha Mitchell Sci Soc 68:222–235

    Google Scholar 

  • Crandall CA, Crandall RB, Arean VM (1967) Increased resistance in mice to larval Ascaris suum infection induced by Nippostrongylus brasiliensis. J Parasitol 53:214–215

    Google Scholar 

  • Crandall RB, Crandall CA, Hunter III GW, Arean VM (1966) Studies on cross-resistance in schistosome and Ascaris suum infections of mice. Ann Trop Med Parasitol 60:70–77

    Google Scholar 

  • Dargie JD, Berry CI, Holmes PH, Reid JFS, Breeze R, Taylor MG, James ER, Nelson GS (1977) Immunization of sheep against a virulent strain of Schistosoma mattheei using a strain of S. mattheei attenuated by hamster passage. J Helminthol 51:347–357

    Google Scholar 

  • Dash KM (1981) Interaction between Oesophagostomum columbianum and Oesophagostomum venulosum in sheep. Int J Parasitol 11:201–207

    Google Scholar 

  • Davis LR, Herlich H, Bowman GW (1959a) Studies on experimental concurrent infections of dairy calves with coccidia and nematodes. I. Eimeria spp. and the small intestinal worm, Cooperia punctata. Am J Vet Res 20:281–286

    Google Scholar 

  • Davis LR, Herlich H, Bowman GW (1959b) Studies on experimental concurrent infections of dairy calves with coccidia and nematodes. II. Eimeria spp. and the medium stomach worm, Ostertagia ostertagi. Am J Vet Res 20:487–491

    Google Scholar 

  • Davis LR, Herlich H, Bowman GW (1960a) Studies on experimental concurrent infections of dairy calves with coccidia and nematodes. III. Eimeria spp. and the threadworm, Strongyloides papillosus. Am J Vet Res 21:181–187

    Google Scholar 

  • Davis LR, Herlich H, Bowman GW (1960b) Studies on experimental concurrent infections of dairy calves with coccidia and nematodes. IV. Eimeria spp. and the small hairworm, Trichostrongylus colubriformis. Am J Vet Res 21:188–194

    Google Scholar 

  • Dean DA (1983) A review. Schistosoma and related genera: acquired resistance in mice. Exp Parasitol 55:1–104

    Google Scholar 

  • Dineen JK, Gregg P, Windon RG, Donald AD, Kelly JD (1977) The role of immunologically specific and non-specific components of resistance in cross protection to intestinal nematodes. Int J Parasitol 7:211–215

    Google Scholar 

  • Dineen JK, Kelly JD, Campbell NJ (1978) Further observations on the nature and characteristics of cross protection against Fasciola hepatica produced in sheep by infection with Cysticercus tenuicollis. Int J Parasitol 8:173–176

    Google Scholar 

  • Dobson AP (1985) The population dynamics of competition between parasites. Parasitology 91:317–347

    Google Scholar 

  • Doy TG, Hughes DL, Harness E (1981) The heterologous protection of rats against a challenge with Fasciola hepatica by prior infection with the nematode Nippostrongylus brasiliensis. Parasite Immunol 3:171–180

    Google Scholar 

  • Durie PH (1962) Parasitic gastro-enteritis of cattle: seasonal fluctuations in populations of strongyle larvae on a calf pasture and their significance in infection of the grazing animal. Aust J Agric Res 13:767–777

    Google Scholar 

  • Duszynski DW, Russell D, Roy SA, Castro GA (1978) Suppressed rejection of Trichinella spiralis in immunized rats concurrently infected with Eimeria nieschulzi. J Parasitol 64:83–88

    Google Scholar 

  • El-Azazy OME, van veen Schillhorn TW (1985) The effect of pre-exposure to Fasciola hepatica or Schistosoma mansoni on challenge infection with Fasciola hepatica. Vet Parasitol 17:173–176

    Google Scholar 

  • El Raziky EH, Ahmed L, Maddison SE (1983) Prevalence of Entamoeba histolytica in patients with schistosomal colonic polyposis. Am J Trop Med Hyg 32:312–315

    Google Scholar 

  • Eriksen L (1981) Host-parasite relations in Ascaris suum infection in pigs and mice. Thesis, Royal Veterinary and Agricultural University, Copenhagen

    Google Scholar 

  • Eveland LK, Hsü SYL, Hsü HF (1969) Cross-immunity of Schistosoma japonicum, S. mansoni and S. bovis in rhesus monkeys. J Parasitol 55:279–288

    Google Scholar 

  • Ewing SA, Todd AC (1961a) Association among members of the genus Metastrongylus Molin, 1861 (Nematoda: Metastrongylidae). Am J Vet Res 22:1077–1080

    Google Scholar 

  • Ewing SA, Todd AC (1961b) Metastrongylosis in the field: species and sex ratios of the parasites, preferential location in respiratory apparatus of the host, and concomitant lesions. Am J Vet Res 22:606–609

    Google Scholar 

  • Fagbemi BO, Christensen NØ (1984) Delayed expulsion of Hymenolepis diminuta in Trypanosoma brucei infected mice. Z Parasitenkd 70:663–665

    Google Scholar 

  • Fagbemi BO, Christensen NØ, Nansen P (1985a) Suppression of Babesia microti infection in mice concurrently infected with Fasciola hepatica. Vet Parasitol 17:101–110

    Google Scholar 

  • Fagbemi BO, Christensen NØ, Nansen P (1985b) Suppression of Babesia microti infection in mice concurrently infected with Schistosoma mansoni. Acta Vet Scand 26:191–204

    Google Scholar 

  • Fenwick P (1980) The effect of Plasmodium berghei, Trypanosoma lewesi, Corynebacterium parvum, and Mycobacterium bovis (BCG) on the growth and survival of Hymenolepis diminuta in the rat. Parasitology 81:lix

    Google Scholar 

  • Ferretti G, Gabriele F, Palmas C, Wakelin D (1984) Interactions between Trichinella spiralis and Hymenolepis nana in the intestine of the mouse. Int J Parasitol 14:29–33

    Google Scholar 

  • Frandsen JC (1983) Effects of low-level infections by coccidia and roundworms on the nutritional status of rats fed an adequate diet. J Anim Sci 57:1487–1497

    Google Scholar 

  • Frandsen JC (1985) Effects of restrictions in dietary protein and vitamin A on the responses of rats to infections by Nippostrongylus brasiliensis (Nematoda) and N. brasiliensis plus Eimeria nieschulzi (Coccidia). Int J Parasitol 15:523–528

    Google Scholar 

  • Froyd G (1960) The incidence of liver flukes (Fasciola gigantica) and hydatid cysts (Echinococcus granulosus) in Kenya cattle. J Parasitol 46:659–662

    Google Scholar 

  • Gemmell MA (1964a) Species specificity of the immunogenic complexes of the tapeworm hexacanth embryo. Nature 204:705–707

    Google Scholar 

  • Gemmell MA (1964b) Immunological responses of the mammalian host against tapeworm infections: I. Species specificity of hexacanth embryos in protecting sheep against Taenia hydatigena. Immunology 7:489–499

    Google Scholar 

  • Gemmell MA (1965a) Immunological responses of the mammalian host against tapeworm infections: III. Species specificity of hexacanth embryos in protecting sheep against Taenia ovis. Immunology 8:281–290

    Google Scholar 

  • Gemmell MA (1965b) Immunological responses of the mammalian host against tapeworm infections: II. Species specificity of hexacanth embryos in protecting rabbits against Taenia pisiformis. Immunology 8:270–280

    Google Scholar 

  • Gemmell MA (1966) Immunological responses of the mammalian host against tapeworm infections: IV. Species specificity of hexacanth embryos in protecting sheep against Echinococcus granulosus. Immunology 11:325–335

    Google Scholar 

  • Gemmell MA (1967) Species specific and cross-protective functional antigens of the tapeworm embryo. Nature 213:500–501

    Google Scholar 

  • Gemmell MA (1969a) Hydatidosis and cysticercosis. I. Acquired resistance to the larval phase. Aust Vet J 45:521–524

    Google Scholar 

  • Gemmell MA (1969b) Immunological responses of the mammalian host against tapeworm infections: XI. Antigen sharing among Taenia pisiformis, T. hydatigena, and T. ovis. Exp Parasitol 26:67–72

    Google Scholar 

  • Gemmell MA (1970) Hydatidosis and cysticercosis. 3. Induced resistance to the larval phase. Aust Vet J 46:366–369

    Google Scholar 

  • Gemmell MA, Johnstone PD (1977) Experimental epidemiology of hydatidosis and cysticercosis. Adv Parasitol 15:311–369

    Google Scholar 

  • Golenser J, Spira DT, Shmuel Z (1976) Mutual influence of infection with Plasmodium berghei and Nippostrongylus brasiliensis in rats. Parasitology 73:XIII

    Google Scholar 

  • Goose J (1977) Studies on immunity to Fasciola hepatica in the rat. PhD thesis, Brunel University

  • Goulson HT (1958) Studies on the influence of a prior infection with Ancylostoma caninum on the establishment and maintenance of Trichinella spiralis in mice. J Elisha Mitchell Sci Soc 74:14–23

    Google Scholar 

  • Gretillat S (1981) nteractions parasitaires dans le polyparasitisme gastro-intestinal des animaux d'élevage en Afrique de l'Ouest. Conséquences et précautions à prendre lors d'une thérapeutique de masse. Rev Elev Med Vet Pays Trop 34:313–317

    Google Scholar 

  • Griffin L, Allonby EW, Preston JM (1981a) The interaction of Trypanosoma congolense and Haemonchus contortus infections in 2 breeds of goat: 1. Parasitology. J Comp Pathol 91:85–95

    Google Scholar 

  • Griffin L, Aucutt M, Allonby EW, Preston J, Castelino J (1981b) The interaction of Trypanosoma congolense and Haemonchus contortus infections in 2 breeds of goat: 2. Haematology. J Comp Pathol 91:97–103

    Google Scholar 

  • Hagan P, Wakelin D (1982) Nematospiroides dubius: effect of infection on lymphocyte responses to Trichinella spiralis in mice. Exp Parasitol 54:157–165

    Google Scholar 

  • Hague A, Camus D, Ogilvie BM, Capron M, Bazin H, Capron A (1981) Dipetalonema vitae infective larvae reach reproductive maturity in rats immunodepressed by prior exposure to Schistosoma mansoni or its products and in congenitally athymic rats. Clin Exp Immunol 43:1–9

    Google Scholar 

  • Hague A, Cuna W, Bonnel B, Capron A, Joseph M (1985) Platelet mediated killing of larvae from different filarial species in the presence of Dipetalonema vitae-stimulated IgE antibodies. Parasite Immunol 7:517–526

    Google Scholar 

  • Halawani AA, Farag HF, Awadalla HN (1977) Studies on experimental mixed infection of Schistosoma haematobium and Schistosoma mansoni in the albino mouse. Trop Med Parasitol 28:478–480

    Google Scholar 

  • Halvörsen O (1976) Negative interaction amongst parasites. In: Kennedy CR (ed) Ecological aspects of parasitology. North-Holland, Amsterdam 99–114

    Google Scholar 

  • Hammond JA (1973) Experimental chronic Fasciola gigantica infection in sheep. Trop Anim Health Prod 5:12–21

    Google Scholar 

  • Heath DD, Lawrence SB, Yong WK (1979) Cross-protection between the cysts of Echinococcus granulosus, Taenia hydatigena and T. ovis in lambs. Res Vet Sci 27:210–212

    Google Scholar 

  • Hendow HT, Storey DM, Kershaw WE (1976) Combined infections of Litomosoides carinii and Trypanosoma brucei in hooded rats. Parasitology 73:XIII

    Google Scholar 

  • Hendrix S, Kopia G, Lattime E (1975) Effects of concurrent infection with Nippostrongylus brasiliensis upon Hymenolepis diminuta in the rat small intestine. Proc Abst Am Soc Parasitol, 50th Meeting 241, p 101

  • Herlich H (1965) Immunity and cross immunity to Cooperia oncophora and Cooperia pectinata in calves and lambs. Am J Vet Res 26:1037–1041

    Google Scholar 

  • Heyneman D (1962) Studies on helminth immunity. II. Influence of Hymenolepis nana (Cestoda: Hymenolepididae) in dual infections with H. diminuta in white mice and rats. Exp Parasitol 12:7–18

    Google Scholar 

  • Hillyer GV (1976) Can we vaccinate against schistosomes? Fed Proc 35:2568–2571

    Google Scholar 

  • Hillyer GV (1981) Effect of Schistosoma mansoni infections on challenge infections with Fasciola hepatica in mice. J Parasitol 67:731–733

    Google Scholar 

  • Hillyer GV (1984) Immunity to schistosomes using heterologous trematode antigens — a review. Vet Parasitol 14:263–283

    Google Scholar 

  • Hillyer GV (1985) Induction of immunity in mice to Fasciola hepatica with a Fasciola/Schistosoma cross-reactive defined immunity antigen. Am J Trop Med Hyg 34:1127–1131

    Google Scholar 

  • Hillyer GV, Serrano AE (1983) The antigens of Paragonimus westermani, Schistosoma mansoni, and Fasciola hepatica adult worms. Evidence for the presence of cross-reactive antigens and for cross-protection to Schistosoma mansoni infection using antigens of Paragonimus westermani. Am J Trop Med Hyg 32:350–358

    Google Scholar 

  • Hitcho PJ, Thorson RE (1974) Nippostrongylus brasiliensis and Nematospiroides dubius: cross immunity studies using millipore diffusion chambers. Int J Parasitol 4:335–336

    Google Scholar 

  • Holland C (1984) Interactions between Moniliformis (Acanthocephala) and Nippostrongylus (Nematoda) in the small intestine of laboratory rats. Parasitology 88:303–315

    Google Scholar 

  • Holmes JC (1961) Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala): I. General effects and comparison with crowding. J Parasitol 47:209–216

    Google Scholar 

  • Holmes JC (1962a) Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala): II. Effects on growth. J Parasitol 48:87–96

    Google Scholar 

  • Holmes JC (1962b) Effects of concurrent nfections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala): III. Effects in hamsters. J Parasitol 48:97–100

    Google Scholar 

  • Holmes JC (1973) Site selection by parasitic helminths: interspecific interactions, site segregation, and their importance to the development of helminth communities. Can J Zool 51:333–347

    Google Scholar 

  • Hopkins CA (1980) Immunity and Hymenolepis diminuta. In: Arai HP (ed) Biology of the tapeworm Hymenolepis diminuta. Academic Press, New York London, 551–614

    Google Scholar 

  • Hopkins CA, Goodall RI, Zajac A (1977) The longevity of Hymenolepis microstoma in mice, and its immunological cross-reaction with Hymenolepis diminuta. Parasitology 74:175–183

    Google Scholar 

  • Howard RJ, Christie PR, Wakelin D, Wilson MM, Behnke JM (1978) The effect of concurrent infection with Trichinella spiralis on Hymenolepis microstoma in mice. Parasitology 77:273–279

    Google Scholar 

  • Hsü SYL, Hsü HF (1961) New approach to immunization against Schistosoma japonicum. Science 133:766

    Google Scholar 

  • Hsü SYL, Hsü HF (1963) Further studies on rhesus monkeys immunized against Schistosoma japonicum by administration of cercariae of the Formosan strain. Trop Med Parasitol 14:506–512

    Google Scholar 

  • Hsü SYL, Hsü HF (1968) A chimpanzee naturally infected with Schistosoma mansoni: its resistance against a challenge infection of S. japonicum. Trans R Soc Trop Med Hyg 62:901

    Google Scholar 

  • Hsü HF, Hsü SYL, Tsai CT (1964) Immunization against Schistosoma japonicum in rhesus monkeys by administration of cercariae of Schistosomatium douthitti. Trop Med Parasitol 15:435–440

    Google Scholar 

  • Hsü SYL, Hsü HF, Chu KY, Tsai CT, Eveland LK (1966) Immunization against Schistosoma haematobium in rhesus monkeys by administration of cercariae of Schistosoma bovis. Trop Med Parasitol 17:407–412

    Google Scholar 

  • Hsü HF, Hsü SYL, Eveland LK (1980) Schistosomiasis vaccination. Historical development, present status and future prospects. China Med J 93:297–312

    Google Scholar 

  • Hughes DL, Purnell RE, Brocklesby DW (1977) The effect of initial Fasciola hepatica infection on the pathogenicity of subsequent Babesia divergens infections in intact and splenectomised calves. Vet Rec 100:320–321

    Google Scholar 

  • Hughes DL, Harness E, Doy TG (1978) Failure to demonstrate resistance in goats, sheep and cattle to Fasciola hepatica after infection with Cysticercus tenuicollis. Res Vet Sci 25:356–359

    Google Scholar 

  • Hunter GW III, Ritchie LS, Lin S, Pan C, Tanabe H (1956) Immunological studies: I. Experiments with bird and human schistosomes in small mammals. Exp Parasitol 5:551–559

    Google Scholar 

  • Hunter GW III, Weinmann CJ, Hoffmann RG (1961) Studies on schistosomiasis. XVII. Non-reciprocal acquired resistance between Schistosoma mansoni and Schistosomatium douthitti in mice. Exp Parasitol 11:133–140

    Google Scholar 

  • Hunter GW III, Crandall RB, Arean VM (1963) Attempts to increase resistance to Schistosoma mansoni and Schistosomatium douthitti infection in mice by heterologous infections. J Parasitol 49 (suppl.):55

    Google Scholar 

  • Hunter GW III, Wallis MV, Crandall RB (1967) Studies on schistosomiasis. XXII. Cross resistance in Schistosoma mansoni and Nippostrongylus brasiliensis infections in albino mice. Exp Parasitol 21:9–15

    Google Scholar 

  • Hussein MF, Saeed AA, Nelson GS (1970) Studies on heterologous immunity in schistosomiasis: 4. Heterologous schistosome immunity in cattle. Bull WHO 42:745–749

    Google Scholar 

  • Jachowski LA, Bingham GA (1961) Influence of trichinosis on Schistosoma mansoni in mice. J Parasitol 47:719

    Google Scholar 

  • Jenkins DC (1975) The influence of Nematospiroides dubius on subsequent Nippostrongylus brasiliensis infections in mice. Parasitology 71:349–355

    Google Scholar 

  • Jenkins SN, Behnke JM (1977) Impairment of primary expulsion of Trichuris muris in mice concurrently infected with Nematospiroides dubius. Parasitology 75:71–78

    Google Scholar 

  • Joysey HS (1986) Suppression of Taenia crassiceps during concurrent infections with Mesocestoides corti in mice. Parasitology 92:199–207

    Google Scholar 

  • Jung RC, Beaver PC (1951) Clinical observations on Trichocephalus trichiurus (whipworm) infestation in children. Pediatrics 8:548–557

    Google Scholar 

  • Kates KC, Turner JH (1960) An experiment on the combined pathogenic effects of Haemonchus contortus and Nematodirus spathiger on lambs. Proc Helminthol Soc Wash 27:62–67

    Google Scholar 

  • Kazacos KR (1975) Increased resistance in the rat to Nippostrongylus brasiliensis following immunization against Trichinella spiralis. Vet Parasitol 1:165–174

    Google Scholar 

  • Kazacos KR (1976) Increased resistance in the rat to Strongyloides ratti following immunization against Trichinella spiralis. J Parasitol 62:493–494

    Google Scholar 

  • Kazacos KR, Thorson RE (1975) Cross-resistance between Nippostrongylus brasiliensis and Strongyloides ratti in rats. J Parasitol 61:525–529

    Google Scholar 

  • Keeling JED (1961) Experimental trichuriasis: I. Antagonism between Trichuris muris and Aspiculuris tetraptera in the albino mouse. J Parasitol 47:641–646

    Google Scholar 

  • Kennedy MW (1980) Immunologically mediated, non-specific interactions between the intestinal phases of Trichinella spiralis and Nippostrongylus brasiliensis in the mouse. Parasitology 80:61–72

    Google Scholar 

  • Klesius PH (1982) Immunopotentiation against internal parasites. Vet Parasitol 10:239–248

    Google Scholar 

  • Kloetzel K, Faleiros JJ, Mendes SR (1971) Concurrent infection of white mice with T. cruzi and S. mansoni. Trans R Soc Trop Med Hyg 65:530–531

    Google Scholar 

  • Kloetzel K, Faleiros JJ, Mendes SR, Stanley CT, Arias HS (1973) Concomitant infection of albino mice by Trypanosoma cruzi and Schistosoma mansoni. Parasitological parameters. Trans R Soc Trop Med Hyg 67:652–658

    Google Scholar 

  • Kloetzel K, Chieffi PP, Faleiros JJ, Merluzzi Filho TJ (1977) Mortality and other parameters of concomitant infections in albino mice: the Schistosoma-Toxoplasma model. Trop Geog Med 29:407–410

    Google Scholar 

  • Knight RA (1985) Attempts to stimulate resistance to Fasciola hepatica in calves with Schistosoma mansoni cercariae. Proc Helminthol Soc Wash 52:138–139

    Google Scholar 

  • Knight R, Chew LH (1974) The interaction between Entamoeba histolytica and Trichuris muris infections in mice. Am J Trop Med Hyg 23:590–594

    Google Scholar 

  • Knight R, Warren KS (1973) The interaction between Entamoeba histolytica and Schistosoma mansoni infections in mice. Trans R Soc Trop Med Hyg 67:644–651

    Google Scholar 

  • Kocan AA (1974) The influence of Nippostrongylus brasiliensis on the establishment of Angiostrongylus cantonensis in the laboratory rat. Proc Helminthol Soc Wash 41:237–241

    Google Scholar 

  • Kojima S, Yamamoto N, Kanazawa T, Ovary Z (1985a) Monoclonal IgE-dependent eosinophil cytotoxicity to haptenated schistosomula of Schistosoma japonicum: enhancement of the cytotoxicity and expression of Fc receptors for IgE by Nippostrongylus brasiliensis infection. J Immunol 134:2719–2722

    Google Scholar 

  • Kojima S, Yamamoto N, Kanazawa T, Shigematsu H, Ovary Z (1985 b) Enhancement of IgE-dependent eosinophil cytotoxicity to dinitrophenylated schistosomula by a nematode infection. Int Arch Allergy Appl Immunol 76:91–94

    Google Scholar 

  • Kusel JR, Phillips RS (1978) The interaction of malaria parasites and Schistosoma mansoni in mice. Trans R Soc Trop Med Hyg 72:642–643

    Google Scholar 

  • Lang BZ (1967) Fasciola hepatica and Hymenolepis microstoma in the laboratory mouse. J Parasitol 53:213–214

    Google Scholar 

  • Larsh JE, Campbell CH (1952) The effect on the natural resistance of mice to Hymenolepis nana var.fraterna of a simultaneous infection with Trichinella spiralis. J Parasitol 38 [Suppl]:20–21

    Google Scholar 

  • Larsh JE, Donaldson AW (1944) The effect of concurrent infection with Nippostrongylus on the development of Hymenolepis in mice. J Parasitol 30:18–20

    Google Scholar 

  • Larsh JE, Race GJ (1975) Allergic inflammation as a hypothesis for the expulsion of worms from tissues: a review. Exp Parasitol 37:251–266

    Google Scholar 

  • Lee TDG, Grencis RK, Wakelin D (1982) Specific cross-immunity between Trichinella spiralis and Trichuris muris: immunization with heterologous infections and antigens and transfer of immunity with heterologous immune mesenteric lymph node cells. Parasitology 84:381–389

    Google Scholar 

  • Lewinsohn R (1975) Anaemia in mice with concomitant Schistosoma mansoni and Plasmodium berghei yoelii infection. Trans R Soc Trop Med Hyg 69:51–56

    Google Scholar 

  • Liu GYH, Ivey MH (1961) Effect of several nematodes on an initial infection of Nematospiroides dubius in mice. J Parasitol 47:433–436

    Google Scholar 

  • Lloyd S (1979) Homologous and heterologous immunization against the metacestodes of Taenia saginata and Taenia taeniaeformis in cattle and mice. Z Parasitenkd 60:87–96

    Google Scholar 

  • Long E, Lwin M, Targett G, Doenhoff M (1981) Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse: VIII. Failure of concurrent infections with Plasmodium chabaudi to affect resistance to reinfection with S. mansoni. Ann Trop Med Parasitol 75:79–86

    Google Scholar 

  • Louch CD (1962) Increased resistance to Trichinella spiralis in the laboratory rat following infection with Nippostrongylus muris. J Parasitol 48:24–26

    Google Scholar 

  • Lucker JT, Vegors HH, Douvres FW (1964) Immunization against the cattle lungworm: oral vaccination with infective Dictyocaulus filaria larvae. Proc Helminthol Soc Wash 31:153–158

    Google Scholar 

  • Lwin M, Last C, Targett GAT, Doenhoff MJ (1982) Infection of mice concurrently with Schistosoma mansoni and rodent malarias: contrasting effects of patent S. mansoni infections on Plasmodium chabaudi, P. yoelii and P. berghei. Ann Trop Med Parasitol 76:265–273

    Google Scholar 

  • Machnicka B, Choromanski L (1979) The influence of immunosuppression generated by Trypanosoma cruzi on the development of Hymenolepis diminuta in CFW mice. Bull Acad Pol Sci [Ser Sci Biol] 27:739–748

    Google Scholar 

  • MacLean JM (1982) Radioisotopic techniques in the study of in vivo parasite metabolism. In: Proceedings symposium on nuclear techniques in the study of parasitic infections. International Atomic Energy Agency, Vienna, pp 483–495

    Google Scholar 

  • Magzoub M, Adam SEI (1977) Laboratory investigations on natural infection in zebu cattle with Fasciola gigantica and Schistosoma bovis. Zentralbl Veterinarmed [B] 24:53–62

    Google Scholar 

  • Mahmoud AAF, Warren KS, Strickland GT (1976) Acquired resistance to infection with Schistosoma mansoni induced by Toxoplasma gondii. Nature 263:56–57

    Google Scholar 

  • Mahmoud AAF, Strickland GT, Warren KS (1977) Toxoplasmosis and the host-parasite relationship in murine schistosomiasis mansoni. J Infect Dis 135:408–413

    Google Scholar 

  • Maizels RM, Partono F, Oemijati S, Denham DA, Ogilvie BM (1983) Cross-reactive surface antigens on three stages of Brugia malayi, B. pahangi and B. timori. Parasitology 87:249–263

    Google Scholar 

  • Maizels RM, Sutanto I, Gomez-Priego A, Lillywhite J, Denham DA (1985) Specificity of surface molecules of adult Brugia parasites: cross-reactivity with antibody from Wuchereria, Onchocerca and other human filarial infections. Trop Med Parasitol 36:233–237

    Google Scholar 

  • Maldonado-Moll JF (1977) Oograms of Schistosomatium douthitti in mice concomitantly infected with Fasciola hepatica. J Parasitol 63:946–947

    Google Scholar 

  • Malek EA (1981) Heterologous immunity against Schistosoma mansoni in mice by administration of Heterobilharzia americana. Z Parasitenkd 65:137–142

    Google Scholar 

  • Mansour NS, Soliman GN, El-Assal FM (1984) Studies on experimental mixed infections of Schistosoma mansoni and S. haematobium in hamsters. Z Parasitenkd 70:345–357

    Google Scholar 

  • Mapes CJ, Coop RL (1970) The interaction of infections of Haemonchus contortus and Nematodirus battus in lambs: I. The effect of massive infections of Haemonchus on subsequent infections of Nematodirus. J Comp Pathol 80:123–136

    Google Scholar 

  • Mapes CJ, Coop RL (1971) Effect of concurrent and terminated infections of Haemonchus contortus on the development and reproductive capacity of Nematodirus battus. J Comp Pathol 81:479–492

    Google Scholar 

  • Martínez-Fernández AR, Sanmartín-Durán ML, Santos MC (1981a) Interaction between Trichinella spp. (T. spiralis/T. pseudospiralis) and Oxyuroidea in the mouse intestine. In: Kim CW, Ruitenberg EJ, Teppema JS (eds) Trichinellosis. Proceedings of the 5th international conference on trichinellosis. Reedbooks, Chertsey, pp 153–157

    Google Scholar 

  • Martínez-Fernández AR, Sanmartín-Durán ML, Ortega MG, Garate T (1981b) Cross immunity levels among sibling species of Trichinella. In: Kim CW, Ruitenberg EJ, Teppema JS (eds) Trichinellosis. Proceedings of the 5th international conference on trichinellosis. Reedbooks, Chertsey, pp 129–133

    Google Scholar 

  • Massoud J, Nelson GS (1972) Studies on heterologous immunity in schistosomiasis. 6. Observations on cross-immunity to Ornithobilharzia turkestanicum, Schistosoma bovis, S. mansoni, and S. haematobium in mice, sheep, and cattle in Iran. Bull WHO 47:591–600

    Google Scholar 

  • Meerovitch E, Ackerman SJ (1974) Trypanosomiasis in rats with trichinosis. Trans R Soc Trop Med Hyg 68:417

    Google Scholar 

  • Meerovitch E, Ghadirian E (1980) Effect of Trichinella spiralis infection on the experimental amebic liver abscess in hamsters. Arch Invest Med (Mex) 11 (suppl.):185–188

    Google Scholar 

  • Meerovitch E, Pocock DME (1981) Trichinella spiralis as a modulator of tumour development. In: Kim CW, Ruitenberg EJ, Teppema JS (eds) Trichinellosis. Proceedings of the 5th international conference on trichinellosis. Reedbooks, Chertsey, pp 141–145

    Google Scholar 

  • Michael AI, Awadalla HN, Farag HF (1979) Granuloma size in the liver of mice with Schistosoma haematobium infection and Schistosoma mansoni challenge. Trop Med Parasitol 30:62–64

    Google Scholar 

  • Miller Jr HM (1932) Acquired immunity against a metazoan parasite by use of non-specific worm materials. Proc Soc Exp Biol Med 29:1125–1126

    Google Scholar 

  • Millott SM, Cox FEG (1985) Interactions between Trypanosoma brucei and Babesia spp. and Plasmodium spp. in mice. Parasitology 90:241–254

    Google Scholar 

  • Mitchell GBB, Armour J (1981) Stimulation of resistance to Fasciola hepatica infection in sheep by a regime involving the use of the immunomodulatory compound L tetramisole (levamisole). Res Vet Sci 30:343–348

    Google Scholar 

  • Monrad J, Christensen NØ, Nansen P, Frandsen F (1981) Resistance to Fasciola hepatica in sheep harbouring primary Schistosoma bovis infections. J Helminthol 55:261–271

    Google Scholar 

  • Moqbel R, Wakelin D (1979) Trichinella spiralis and Strongyloides ratti: immune interaction in adult rats. Exp Parasitol 47:65–72

    Google Scholar 

  • Morcock RE, Roberts LS (1976) Concurrent infections of Hymenolepis diminuta and Nippostrongylus brasiliensis: effects of host diets deficient in protein. Prog Abst Am Soc Parasitol, 51st Ann Meeting 109:49

    Google Scholar 

  • Muller GL (1968) The epizootiology of helminth infestation in sheep in the south-western districts of the Cape. Onderstepoort J Vet Res 35:159–194

    Google Scholar 

  • Murray J, Murray A, Murray M, Murray C (1978) The biological suppression of malaria: an ecological and nutritional interrelationship of a host and two parasites. Am J Clin Nutr 31:1363–1366

    Google Scholar 

  • Murray MJ, Murray AB, Murray MB, Murray CJ (1977) Parotid enlargement, forehead edema, and suppression of malaria as nutritional consequences of ascariasis. Am J Clin Nutr 30:2117–2121

    Google Scholar 

  • Murrell KD, Yogore MG, Lewert RM, Clutter WG, Vannier WE (1973) Immunization with a zoophilic strain of Schistosoma japonicum: a re-evaluation of the formosan strain of S. japonicum in rhesus monkeys. Am J Trop Med Hyg 22:723–733

    Google Scholar 

  • Mzembe SAT, Lloyd S, Soulsby EJL (1984) Macrophage mediated resistance to Babesia microti in Nematospiroides dubius-infected mice. Z Parasitenkd 70:753–761

    Google Scholar 

  • Nawa Y, Korenaga M (1983) Mast and goblet cell responses in the small intestine of rats concurrently infected with Nippostrongylus brasiliensis and Strongyloides ratti. J Parasitol 69:1168–1170

    Google Scholar 

  • Nawa Y, Mimori T, Korenaga M, Tada I (1982) Stage-specific cross-resistance between Nippostrongylus brasiliensis and Strongyloides ratti (Nematoda) in rats. J Parasitol 68:804–808

    Google Scholar 

  • Nelson GS (1974) Zooprophylaxis with special reference to schistosomiasis and filariasis. In: Soulsby EJL (ed) Parasitic zoonoses. Academic Press, New York, pp 273–285

    Google Scholar 

  • Nelson GS, Amin MA, Saoud MFA, Teesdale C (1968) Studies on heterologous immunity in schistosomiasis: 1. Heterologous schistosome immunity in mice. Bull WHO 38:9–17

    Google Scholar 

  • Ngwenya BZ (1982) Enhanced resistance to Plasmodium berghei in mice previously infected with Trichinella spiralis. Parasite Immunol 4:197–207

    Google Scholar 

  • Nichol CP, Sewell MMH (1984) Immunosuppression by larval cestodes of Babesia microti infections. Ann Trop Med Parasitol 78:228–233

    Google Scholar 

  • Novak M (1984) Cross-protection between the metacestodes of Mesocestoides corti and Taenia crassiceps in mice. Int J Parasitol 14:497–501

    Google Scholar 

  • Ogunrinade A, Adegoke GO (1982) Bovine fascioliasis in Nigeria — intercurrent parasitic and bacterial infections. Trop Anim Health Prod 14:121–125

    Google Scholar 

  • Olson LJ (1962) Organ distribution of Toxocara canis larvae in normal mice and in mice previously infected with Toxocara, Ascaris or Trichinella. Tex Rep Biol Med 20: 651–657

    Google Scholar 

  • Oothuman P, Denham DA, McGreevy PB, Nelson GS, Rogers R (1979) Successful vaccination of cats against Brugia pahangi with larvae attenuated by irradiation with 10 krad cobalt 60. Parasite Immunol 1:209–216

    Google Scholar 

  • Palmas C, Wakelin D, Cabaj W (1985) Immune responses to Trichinella pseudospiralis and Trichinella spiralis in mice. Int J Parasitol 15:321–325

    Google Scholar 

  • Parfitt JW, Sinclair IJ (1967) Cross resistance to Dictyocaulus viviparus produced by Dictyocaulus filaria infections in calves. Res Vet Sci 8:6–13

    Google Scholar 

  • Pedersen EM, Christensen NØ, Frandsen F (1982) Reduction in the severity of hepatosplenic schistosomiasis mansoni in mice by previous exposure to cercariae of the bird schistosome Trichobilharzia szidati. J Helminthol 56:1–3

    Google Scholar 

  • Phillips RS, Wakelin D (1976) Trichuris muris: effect of concurrent infections with rodent piroplasms on immune expulsion from mice. Exp Parasitol 39:95–100

    Google Scholar 

  • Phillips RS, Selby GR, Wakelin D (1974) The effect of Plasmodium berghei and Trypanosoma brucei infections on the immune expulsion of the nematode Trichuris muris from mice. Int J Parasitol 4:409–415

    Google Scholar 

  • Pitchford RJ (1976) Preliminary observations on the distribution, definitive hosts and possible relation with other schistosomes, of Schistosoma margrebowiei Le Roux, 1933 and Schistosoma leiperi Le Roux, 1955. J Helminthol 50:111–123

    Google Scholar 

  • Pitchford RJ (1977) Absence of schistosomes in potentially endemic areas in Africa. In: Gear JHS (ed) Medicine in a tropical environment. Balkema, Cape Town, pp 667–677

    Google Scholar 

  • Pitchford RJ, Wolstenholme B (1977) Further observations on the relationship and distribution of Schistosoma margrebowiei and S. leiperi in central southern Africa. J Helminthol 51:327–336

    Google Scholar 

  • Presidente PJA, Knapp SE, Nicol KD (1973) Pathogenicity of experimentally induced concurrent infections of Fasciola hepatica and Haemonchus contortus in sheep. Am J Vet Res 34:51–60

    Google Scholar 

  • Preston JM, Nelson GS, Saeed AA (1972) Studies on heterologous immunity in schistosomiasis. 5. Heterologous schistosome immunity in sheep. Bull WHO 47:587–590

    Google Scholar 

  • Rajasekariah GR, Rickard MD, Montague PE, Mitchell GF (1979) Attempts to immunise rats and mice against infection with Fasciola hepatica using antigens prepared from Taenia hydatigena. Z Parasitenkd 58:175–180

    Google Scholar 

  • Reid JFS, Armour J, Jennings FW, Kirkpatrick KS, Urquhart GM (1967) The fascioliasis/ostertagiasis complex in young cattle. A guide to diagnosis and therapy. Vet Rec 80:371–374

    Google Scholar 

  • Reinecke RK (1966) The value of uniform worm burdens in the larval anthelmintic test. JS Afr Vet Assoc 37:133–142

    Google Scholar 

  • Reinecke RK (1974) Studies on Haemonchus contortus. I. The influence of previous exposure to Trichostrongylus axei on infestation with H. contortus. Onderstepoort J Vet Res 41:213–216

    Google Scholar 

  • Reinecke RK, Snyman HM, Seaman H (1979) Studies on Haemonchus contortus. II. The effect of abomasal nematodes on subsequent challenge with H. contortus. Onderstepoort J Vet Res 46:199–205

    Google Scholar 

  • Rickard MD, Adolph AJ (1976) Vaccination of calves against Taenia saginata infection using a “parasite-free” vaccine. Vet Parasitol 1:389–392

    Google Scholar 

  • Rickard MD, Bell KJ (1971) Successful vaccination of lambs against infection with Taenia ovis using antigens produced during in vitro cultivation of the larval stages. Res Vet Sci 12:401–402

    Google Scholar 

  • Rickard MD, Coman BJ (1977) Studies on the fate of Taenia hydatigena and Taenia ovis larvae in rabbits, and cross-immunity with Taenia pisiformis larvae. Int J Parasitol 7:257–267

    Google Scholar 

  • Rickard MD, Parmeter SN, Gemmell MA (1975) The effect of development of Taenia hydatigena larvae in the peritoneal cavity of dogs on resistance to a challenge infection with Echinococcus granulosus. Int J Parasitol 5:281–283

    Google Scholar 

  • Rigby DW, Chobotar B (1966) The effects of Trypanosoma lewesi on the development of Hymenolepis diminuta in concurrently infected white rats. J Parasitol 52:389–394

    Google Scholar 

  • Roberts-Thomson IC, Grove DI, Stevens DP, Warren KS (1976) Suppression of giardiasis during the intestinal phase of trichinosis in the mouse. Gut 17:953–958

    Google Scholar 

  • Sadun EH, Yamaki A, Lin SS, Burke JC (1961) Studies on the host-parasite relationships to Schistosoma japonicum: VI. Acquired resistance in mice and monkeys infected with the formosan and Japanese strains. J Parasitol 47:891–897

    Google Scholar 

  • Schad GA (1966) Immunity, competition and natural regulation of helminth populations. Am Nat 100:359–364

    Google Scholar 

  • Schmidt LH, Esslinger JH (1981) Courses of infections with Plasmodium falciparum in owl monkeys displaying a microfilaremia. Am J Trop Med Hyg 30:5–11

    Google Scholar 

  • Sharp AD, Olson LJ (1962) Hypersensitivity responses in Toxocara-, Ascaris-, and Trichinella-infected guinea pigs to homologous and heterologous challenge. J Parasitol 48:362–367

    Google Scholar 

  • Shumard RF, Bolin DW, Eveleth DF (1957) Physiological and nutritional changes in lambs infected with the nematodes, Haemonchus contortus, Trichostrongylus colubriformis, and Nematodirus spathiger. Am J Vet Res 18:330–337

    Google Scholar 

  • Silver BB, Dick TA, Welch HE (1980) Concurrent infections of Hymenolepis diminuta and Trichinella spiralis in the rat intestine. J Parasitol 66:786–791

    Google Scholar 

  • Silverman PH, Poynter D, Podger KR (1962) Studies on larval antigens derived by cultivation of some parasitic nematodes in simple media: protection tests in laboratory animals. J Parasitol 48:562–571

    Google Scholar 

  • Simonsen PE, Andersen BJ (1986) Echinostoma revolutum in mice: dynamics of the antibody attack to the surface of an intestinal trematode. Int J Parasitol 16:475–482

    Google Scholar 

  • Sinclair IJ (1967) The effect of Dictyocaulus filaria on the resistance of guinea-pigs to Dictyocaulus viviparus. Res Vet Sci 8:14–19

    Google Scholar 

  • Sinski E (1972) Preliminary studies on cross-resistance in Nippostrongylus brasiliensis and Trichinella spiralis infection of rats. Acta Parasitol Pol 20:551–561

    Google Scholar 

  • Sirag SB, Christensen NØ, Frandsen F, Monrad J, Nansen P (1980) Homologous and heterologous resistance in Echinostoma revolutum infections in mice. Parasitology 80:479–486

    Google Scholar 

  • Sirag SB, Christensen NØ, Nansen P, Monrad J, Frandsen F (1981) Resistance to Fasciola hepatica in calves harbouring primary patent Schistosoma bovis infections. J Helminthol 55:63–70

    Google Scholar 

  • Smith MA, Clegg JA, Webbe G (1976) Cross-immunity to Schistosoma mansoni and S. haematobium in the hamster. Parasitology 73:53–64

    Google Scholar 

  • Stahl W (1966) Experimental aspiculuriasis: II. Effects of concurrent helminth infection. Exp Parasitol 18:116–123

    Google Scholar 

  • Stewart DF (1953) Studies on resistance of sheep to infestation with Haemonchus contortus and Trichostrongylus spp. and on the immunological reactions of sheep exposed to infestation: V. The nature of the “self-cure” phenomenon. Aust J Agric Res 4:100–117

    Google Scholar 

  • Stewart DF (1955) “Self-cure” in nematode infestations of sheep. Nature 176:1273–1274

    Google Scholar 

  • Stewart GL, Reddington JJ, Hamilton AM (1980) Eimeria nieschulzi and Trichinella spiralis: analysis of concurrent infection in the rat. Exp Parasitol 50:115–122

    Google Scholar 

  • Storey DM, Al-Mukhtar AS (1982) Vaccination of jirds, Meriones unguiculatus, against Litomosoides carinii and Brugia pahangi using irradiated larvae of L. carinii. Trop Med Parasitol 33:23–24

    Google Scholar 

  • Stromberg BE, Soulsby EJL (1977) Heterologous helminth induced resistance to Ascaris suum in guinea pigs. Vet Parasitol 3:169–175

    Google Scholar 

  • Sturrock RF, Butterworth AE, Houba V, Cottrell BJ, Kimani R, Joseph M, Capron A, Ramasamy R, Shah J (1985) Attempts to manipulate specific responses to induce resistance to Schistosoma mansoni in Kenyan baboons (Papio anubis). J Helminthol 59:175–186

    Google Scholar 

  • Taylor MG, Nelson GS, Smith M, Andrews BJ (1973) Studies on heterologous immunity in schistosomiasis: 7. Observations on the development of acquired homologous and heterologous immunity to Schistosoma mansoni in baboons. Bull WHO 49:57–65

    Google Scholar 

  • Taylor MG, James ER, Nelson GS, Bickle Q, Andrews BJ, Dobinson AR, Webbe G (1976) Immunisation of baboons against Schistosoma mansoni using irradiated S. mansoni cercariae and schistosomula and non-irradiated S. rodhaini cercariae. J Helminthol 50:215–221

    Google Scholar 

  • Taylor MG, James ER, Nelson GS, Bickle Q, Dunne DW, Dobinson AR, Dargie JD, Berry CI, Hussein MF (1977) Modification of the pathogenecity of Schistosoma mattheei for sheep by passage of the parasite in hamsters. J Helminthol 51:337–345

    Google Scholar 

  • Terry R, Hudson K (1982) Immunodepression in parasitic infections. Fortschr Zool 27:125–139

    Google Scholar 

  • Townson S, Nelson GS, Bianco AE (1985) Immunity to Onchocerca lienalis microfilariae in mice: II. Effects of sensitization with a range of heterologous species. J Helminthol 59:337–346

    Google Scholar 

  • Turner JH, Colglazier ML (1954) Control of pasture-acquired infections of Nematodirus spathiger and Haemonchus contortus in lambs with phenothiazine-salt mixture. Am J Vet Res 15:564–573

    Google Scholar 

  • Turner JH, Kates KC, Wilson GI (1962) The interaction of concurrent infections of the abomasal nematodes, Haemonchus contortus, Ostertagia circumcincta, and Trichostrongylus axei (Trichostrongylidae), in lambs. Proc Helminthol Soc Wash 29:210–216

    Google Scholar 

  • Urquhart GM, Murray M, Murray PK, Jennings FW, Bate E (1973) Immunosuppression in Trypanosoma brucei infections in rats and mice. Trans R Soc Trop Med Hyg 67:528–535

    Google Scholar 

  • Varela-Diaz VM, Gemmell MA, Williams JF (1972) Taenia hydatigena and T. ovis: antigen sharing: XII. Immunological responses of the mammalian host against tapeworm infections. Exp Parasitol 32:96–101

    Google Scholar 

  • Varma TK, Singh BP, Tewari HC (1983) Immunity to Schistosoma incognitum in mice by previous exposure to S. spindale. J Helminthol 57:37–38

    Google Scholar 

  • Vegors HH, Lucker JT, Douvres FW (1963) Sheep lungworm larvae as a vaccine against cattle lungworm. J Anim Sci 22:825

    Google Scholar 

  • Vinayak VK, Chopra AK (1978) The interaction between Entamoeba histolytica and Syphacia obvelata infection in mice. Ann Trop Med Parasitol 72:549–551

    Google Scholar 

  • Vyas S, Vardhani VV, Johri GN (1981) Analysis of cross-immune reactions. I. Effect of Hymenolepis nana infection in the expulsion of Ancylostoma caninum larvae in mice. Curr Sci 50:1059–1060

    Google Scholar 

  • Webbe G, James C, Nelson GS, Ismail MM, Shaw JR (1979) Cross resistance between Schistosoma haematobium and S. mansoni in the baboon. Trans R Soc Trop Med Hyg 73:42–54

    Google Scholar 

  • Wedrychowicz H, Maclean JM, Holmes PH (1983) The effect of Trypanosoma brucei infection on local and systemic antibody responses of rats to Nippostrongylus brasiliensis. Trop Med Parasitol 34:207–212

    Google Scholar 

  • Wedrychowicz H, Maclean JM, Holmes PH (1984) The influence of Trypanosoma brucei infection on local immunoglobulin responses of rats to Nippostrongylus brasiliensis. Int J Parasitol 14:453–458

    Google Scholar 

  • Weinmann CJ (1960) Studies on schistosomiasis: XV. Resistance to Schistosoma mansoni in mice immunized with Trichinella spiralis. J Parasitol 46 [Suppl]:37

    Google Scholar 

  • Weinmann CJ (1964) Host resistance to Hymenolepis nana. II. Specificity of resistance to reinfection in the direct cycle. Exp Parasitol 15:514–526

    Google Scholar 

  • Weinmann CJ (1966) Immunity mechanisms in cestode infections. In: Soulsby EJL (ed) Biology of parasites. Academic Press, New York, pp 301–320

    Google Scholar 

  • Wescott RB, Colwell DA (1980) Influence of numbers of Nematospiroides dubius upon delayed rejection of Nippostrongylus brasiliensis in mice. J Parasitol 66:858–859

    Google Scholar 

  • Wikerhauser T, Zukovic M, Dzakula N (1971) Taenia saginata and T. hydatigena: intramuscular vaccination of calves with oncospheres. Exp Parasitol 30:36–40

    Google Scholar 

  • Willett KC (1972) An observation on the unexpected frequency of some multiple infections. Bull WHO 47:747–749

    Google Scholar 

  • Wilson GI (1970) Immunity of sheep to Dictyocaulus filaria following vaccination with Dictyocaulus viviparus. Proc Helminthol Soc Wash 37:24–29

    Google Scholar 

  • Wright CA, Southgate VR, Howard GW (1979) Observations on the life cycle of Schistosoma margrebowiei and its possible interactions with S. leiperi in Zambia. J Nat Hist 13:499–506

    Google Scholar 

  • Yagi AI, Younis SA, Haroun EM, Gameel AA, Bushara HO, Taylor MG (1986) Studies on heterologous resistance between Schistosoma bovis and Fasciola gigantica in Sudanese cattle. J Helminthol 60:55–59

    Google Scholar 

  • Yoeli M (1956) Some aspects of concomitant infections of plasmodia and schistosomes: I. The effect of Schistosoma mansoni on the course of infection of Plasmodium berghei in the field vole (Microtus guentheri). Am J Trop Med Hyg 5:988–999

    Google Scholar 

  • Yusuf JN, Piekarski G, Pelster B (1980) Concurrent infections of Trichinella spiralis and Toxoplasma gondii in mice. Z Parasitenkd 62:231–240

    Google Scholar 

  • Yvore P, Esnault A, Besnard J (1980) Coccidiose expérimentale ovine: interactions entre helminthes et coccidies. Rev Med Vet (Toulouse) 131:237–245

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Danish Bilharziasis Laboratory, Jaegersborg Allé 1D, DK-2920, Charlottenlund, Denmark

    N. Ø. Christensen

  2. Institute of Veterinary Microbiology and Hygiene, Royal Veterinary and Agricultural University, Bülowsvej 13, DK-1870, Frederiksberg C, Denmark

    P. Nansen & J. Monrad

  3. Department of Veterinary Microbiology and Parasitology, University of Ibadan, Ibadan, Nigeria

    B. O. Fagbemi

Authors
  1. N. Ø. Christensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Nansen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B. O. Fagbemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Monrad
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Christensen, N.Ø., Nansen, P., Fagbemi, B.O. et al. Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts. Parasitol Res 73, 387–410 (1987). https://doi.org/10.1007/BF00538196

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00538196

Keywords

Search

Navigation