Skip to main content Accessibility help
×
Home

Antagonistic activity of the fungus Pochonia chlamydosporia on mature and immature Toxocara canis eggs

  • A. S. MACIEL (a1), L. G. FREITAS (a1), L. D. FIGUEIREDO (a1), A. K. CAMPOS (a2) and I. N. K. MELLO (a3)...

Summary

In vitro tests were performed to evaluate the ability of 6 isolates of the nematophagous fungus Pochonia chlamydosporia to infect immature and mature Toxocara canis eggs on cellulose dialysis membrane. There was a direct relationship between the number of eggs colonized and the increase in the days of interaction, as well as between the number of eggs colonized and the increase in the concentration of chlamydospores (P<0·05). Immature eggs were more susceptible to infection than mature eggs. The isolate Pc-04 was the most efficient egg parasite until the 7th day, and showed no difference in capacity to infect mature and immature eggs in comparison to Pc-07 at 14 and 21 days of interaction, respectively. Isolate Pc-04 was the most infective on the two evolutionary phases of the eggs at most concentrations, but its ability to infect immature eggs did not differ from that presented by the isolates Pc-07 and Pc-10 at the inoculum level of 5000 chlamydospores. Colonization of infective larvae inside or outside the egg was observed in treatments with the isolates Pc-03, Pc-04, Pc-07 and Pc-10. The isolate Pc-04 of P. chlamydosporia has great biological capacity to destroy immature and mature T. canis eggs in laboratory conditions.

Copyright

Corresponding author

*Corresponding author: Laboratório de Controle Biológico de Nematóides, Bioagro, Universidade Federal de Viçosa, Minas Gerais, 36570-000, Brazil. Tel: +55 31 38992925. E-mail: ale_spalenza@yahoo.com.br

References

Hide All
Abrantes, I., Santos, S. A., Bourne, J., Ciancio, A., Lopez-Llorca, L., Kerry, B., Mota, M., Tzortzakakis, E. and Verdejo-Lucas, S. (2002). The use of Verticillium chlamydosporium as a biological control agent. In A Manual for Research on Verticillium chlamydosporium, a Potential Biological Control Agent for Root-Knot Nematodes (ed. Kerry, B. R. and Bourne, J. M.), pp. 112. IOBC/WPRS, Gent, Belgium.
Alcântara-Neves, N. M., Santos, A. B., Mendonça, L. R., Figueiredo, C. A. V. and Pontes-de-Carvalho, L. (2008). An improved method to obtain antigen-excreting Toxocara canis larvae. Experimental Parasitology 119, 349351.
Alonso, J. M., Stein, M., Chamorro, M. C. and Bojanich, M. V. (2001). Contamination of soils with eggs of Toxocara in a subtropical city in Argentina. Journal of Helminthology 75, 165168.
Aragane, K., Akao, N., Matsuyama, T., Sugita, M., Natsuaki, M. and Kitada, O. (1999). Fever, cough, and nodules on ankles. Lancet 354, 1872.
Araújo, J. V., Braga, F. R., Milani, J. A., Silva, A. S. and Tavela, A. O. (2008). In vitro evaluation of the effect of the nematophagous fungi Duddingtonia flagrans, Monacrosporium sinense and Pochonia chlamydosporia on Ascaris suum eggs. Parasitology Research 102, 787790.
Avcioglu, H. and Burgu, A. (2008). Seasonal prevalence of Toxocara ova in soil samples from public parks in Ankara, Turkey. Vector borne and Zoonotic Diseases 8, 345350.
Aycicek, H., Yarsan, E., Sarimehmetoglu, H. O., Tanyuksel, M., Girginkardesler, N. and Ozyurt, M. (2001). Efficacy of some disinfectants on embryonated eggs of Toxocara canis. Turkish Journal of Medical Sciences 31, 3539.
Basualdo, J. A., Ciarmela, M. L., Sarmiento, P. L. and Minvielle, M. C. (2000). Biological activity of Paecilomyces lilacinus genus against Toxocara canis eggs. Parasitology Research 86, 854859.
Blackwell, V., Ahmed, K., O'Docherty, C. and Hay, R. J. (2000). Cutaneous hyalohyphomycosis caused by Paecilomyces lilacinus in a renal transplant patient. British Journal of Dermatology 143, 873875.
Bouchet, F., Araújo, A., Harter, S., Chaves, S. M., Duarte, A. N., Monnier, J. L. and Ferreira, L. F. (2003). Toxocara canis (Werner, 1782) eggs in the Pleistocene site of Menez-Dregan, France (300,000–500,000 years before present). Memórias do Instituto Oswaldo Cruz 98, 137139.
Bowman, D. D., Mika-Grieve, M. and Grieve, R. B. (1987). Circulating excretory-secretory antigen levels and specific antibody responses in mice infected with Toxocara canis. The American Journal of Tropical Medicine and Hygiene 36, 7582.
Brunaská, M., Dubinsky, P. and Reiterova, K. (1995). Toxocara canis: ultrastructural aspects of larval moulting in the maturing eggs. International Journal for Parasitology 25, 683690.
Carey, J., D'Amico, R., Sutton, D. A. and Rinaldi, M. G. (2003). Paecilomyces lilacinus vaginitis in an immunocompetent patient. Emerging Infectious Diseases 9, 11551158.
Carvalho, R. O., Araújo, J. V., Braga, F. R., Araújo, J. M. and Alves, C. D. (2010). Ovicidal activity of Pochonia chlamydosporia and Paecilomyces lilacinus on Toxocara canis eggs. Veterinary Parasitology 169, 123127.
Chen, S. and Dickson, D. W. (2004). Biological control of nematodes by fungal antagonists. In Nematology, Advances and Perspectives, Nematode Management and Utilization (ed. Chen, Z., Chen, S. and Dickinson, D. W.), pp. 9791039. CABI Publishing, Cambridge, UK.
Coelho, L. M. P. S., Dini, C. Y., Milman, M. H. S. A. and Oliveira, S. M. (2001). Toxocara spp. eggs in public squares of Sorocaba, São Paulo State, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 43, 189191.
Daryani, A., Sharif, M., Amouei, A. and Gholami, S. (2009). Prevalence of Toxocara canis in stray dogs in Northern Iran. Pakistan Journal of Biological Sciences 12, 1031–1035.
Despommier, D. (2003). Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clinical Microbiology Reviews 16, 265272.
Dubinsky, P., Havasiova-Reiterowa, K., Petko, B., Hovorka, I. and Tomasovicova, O. (1995) Role of small mammals in the epidemiology of toxocariasis. Parasitology 110, 187193.
Fenoy, R., Del Hoyo, C. and Guillen-Llera, J. (1987). Estudio comparativo de la influencia de la luz en el embrionamento experimental de los huevos de Toxocara canis y Toxocara leonine. Revista Iberolatinoamericana de Parasitología 47, 173177.
Ferré, P. and Dorchies, P. (2000). Prevalence of Toxocara spp. eggs in sandpits of eight public parks in Toulouse (SW France). Revue de Médecine Vétérinaire 151, 501506.
Foley, J. E., Norris, C. R. and Jang, S. S. (2002). Paecilomycosis in dogs and horses and a review of the literature. Journal of Veterinary Internal Medicine 16, 238243.
Genchi, C. and Traldi, G. (1994). Infezioni zoonosiche da Toxocara canis: stato dell'arte. Journal of Medical Microbiology 9, 457461.
Giacometti, A., Cirioni, O., Fortuna, M., Osimani, P., Antonicelli, L., Del Prete, M. S., Riva, A., D'Errico, M. M., Petrelli, E. and Scalise, G. (2000). Environmental and serological evidence for the presence of toxocariasis in the urban area of Ancona, Italy. European Journal of Epidemiology 16, 10231026.
Glickman, L. (1993). The epidemiology of human toxocariasis. In Toxocara and Toxocariasis, Clinical, Epidemiological and Molecular Perspectives (ed. Lewis, J. and Maizels, R.), pp. 310. Institute of Biology and the British Society for Parasitology, London, UK.
Huang, X., Zhao, N. and Zhang, K. (2004). Extracellular enzymes serving as virulence factors in nematophagous fungi involved in infection of the host. Research in Microbiology 155, 811816.
Jansson, H. B. and Lopez-Llorca, L. V. (2004). Control of nematodes by fungi. In Fungal Biotechnology in Agriculture, Food, and Environmental Applications (ed. Arora, D. K.), pp. 205215. Marcel Dekker, New York, USA.
Jin, Z., Akao, N. and Ohta, N. (2008). Prolactin evokes lactational transmission of larvae in mice infected with Toxocara canis. Parasitology International 57, 495498.
Kerry, B. R. (2001). Exploitation of nematophagous fungal Verticillium chlamydosporium Goddard for the biological control of root-knot nematodes (Meloidogyne spp.). In Fungi as Biocontrol Agents: Progress, Problems and Potential (ed. Butt, T. M., Jackson, C. and Magan, N.), pp. 155167. CAB International, Wallingford, UK.
Kiewnick, S. and Sikora, R. A. (2006). Biological control of the root-knot nematode Meloidogyne incognita by Paecilomyces lilacinus strain 251. Biological Control 38, 179187.
Leij, F. A. A. M. and Kerry, B. R. (1991). The nematophagus fungus Verticillium chlamydosporium Goddard, as a potencial biological control agent for Meloidogyne arenaria (Neal) Chitwood. Revue de Nématologie 14, 157164.
Levine, N. D. (1968). Nematode Parasites of Domestic Animals and Man. Burgess, Minneapolis, Minnesota, USA.
Lloyd, S. (1998). Toxocarosis. In Zoonoses (ed. Palmer, S. R., Soulsby, E. J. L. and Simpson, D. I. H.), pp. 841854. Oxford Medical Publications, Oxford, UK.
Lopez-Llorca, L. V., Maciá-Vicente, J. G. and Jansson, H. B. (2008). Mode of action and interactions of nematophagous fungi. In Integrated Management and Biocontrol of Vegetable and Grain Crop Nematodes (ed. Ciancio, A. and Mukerji, K. G.), pp. 5176. Springer, Dordrecht, The Netherlands.
Lysek, H. and Krajci, D. (1987). Penetration of ovicidal fungus Verticillium chlamydosporium through the Ascaris lumbricoides egg-shells. Folia Parasitologica 34, 5760.
Lysek, H., Malinsky, J. and Janisch, R. (1985). Ultrastructure of eggs of Ascaris lumbricoides linnaeus, 1758 I. Egg-shells. Folia Parasitologica 32, 381384.
Lysek, H. and Sterba, J. (1991). Colonization of Ascaris lumbricoides eggs by the fungus Verticillium chlamydosporium Goddard. Folia Parasitologica 38, 255259.
Ming-Shun, W., Chien-Wei, L., Wen-Yun, D., Ting-Chang, K., Kua-Eyre, S., Yun-Ho, L., Chun-Chao, C. and Chia-Kwung, F. (2008). Enhanced expression of transforming growth factor-beta 1 in inflammatory cells, alpha-smooth muscle actin in stellate cells, and collagen accumulation in experimental granulomatous hepatitis caused by Toxocara canis in mice. Acta Tropica 105, 260268.
Mizgajska-Wiktor, H. and Uga, S. (2006). Exposure and environmental contamination. In Toxocara: the Enigmatic Parasite (ed. Holland, C. V. and Smith, H. V.), pp. 211227. CABI International, Wallingford, UK.
Monfort, E., Lopez-Llorca, L. V., Jansson, H. B. and Salinas, J. (2006). In vitro soil receptivity assays to egg-parasitic nematophagous fungi. Mycological Progress 5, 1823.
Morgan-Jones, G., White, J. F. and Rodrígues-Kábana, R. (1983). Phytonematode pathology: Ultrastructural studies. I. Parasitism of Meloidogyne arenaria eggs by Verticillium chlamydosporium. Nematropica 13, 245260.
Morimatsu, Y., Akao, N., Akiyoshi, H., Kawazu, T., Okabe, Y. and Aizawa, H. (2006). Case reports: a familial case of Visceral Larva Migrans after ingestion of raw chicken livers: appearance of specific antibody in bronchoalveolar lavage fluid of the patients. American Journal of Tropical Medicine and Hygiene 75, 303306.
Nordbring-Hertz, B. (1983). Dialysis membrane technique for studying microbial interaction. Applied and Environmental Microbiology 45, 290293.
Nordbring-Hertz, B., Jansson, H. B. and Tunlid, A. (2006). Nematophagous Fungi. Encyclopedia of Life Sciences. John Wiley & Sons, Chichester, UK.
O'Lorcain, P. (1994 a). Epidemiology of Toxocara spp. in stray dogs and cats in Dublin, Ireland. Journal of Helminthology 68, 331336.
O'Lorcain, P. (1994 b). Prevalence of Toxocara canis ova in public playgrounds in the Dublin area of Ireland. Journal of Helmintology 68, 237241.
Overgaauw, P. A. M. (1997 a). Aspects of Toxocara epidemicology: toxocariasis in dogs and cats. Critical Review in Microbiology 23, 233251.
Overgaauw, P. A. M. (1997 b). Aspects of Toxocara epidemiology: human toxocarosis. Critical Review in Microbiology 23, 215231.
Overgaauw, P. A. M. and Knapen, F. (2008). Toxocarosis, an important zoonosis. European Journal of Companion Animal Practice 18, 259266.
Parsons, J. C. (1987). Ascarid infections of cats and dogs. Veterinary Clinics of North America, Small Animal Practice 17, 13071339.
Pawloski, D. R., Brunker, J. D., Singh, K. and Sutton, D. A. (2010). Pulmonary Paecilomyces lilacinus infection in a cat. Journal of the American Animal Hospital Association 46, 197202.
Pecinali, N. R., Gomes, R. N., Amendoeira, F. C., Pereira Bastos, A. C. M., Martins, M. J. Q. A., Pegado, C. S., Pereira Bastos, O. M., Bozza, P. T. and Castro Faria Neto, H. C. (2005). Influence of murine Toxocara canis infection on plasma and bronchoalveolar lavage fluid eosinophil numbers and its correlation with cytokine levels. Veterinary Parasitology 134, 121130.
Pinelli, E., Brandes, S., Dormans, J., Fonville, M., Hamilton, C. M. and Van Der Giessen, J. (2007). Toxocara canis: Effect of inoculum size on pulmonary pathology and cytokine expression in BALB/c mice. Experimental Parasitology 115, 7682.
Ruiz de Ybáñez, M. R., Garijo, M. M. and Alonso, F. D. (2001). Prevalence and viability of eggs of Toxocara spp. And Toxascaris leonina in public parks in eastern Spain Journal of Helminthology 75, 169173.
Salem, G. and Schantz, P. (1992). Toxocaral visceral larva migrans after ingestion of raw lamb liver. Clinical Infectious Diseases 15, 743744.
Sayre, R. M. and Walter, D. E. (1991). Factors affecting the efficacy of natural enemies of nematodes. Annual Review of Phytopathology 29, 149166.
Segers, R., Butt, T. M., Keen, J. N., Kerry, B. R., Beckett, A. and Peberdy, J. F. (1996). The role of the proteinase VcP1 produced by the nematophagous fungus Verticillium chlamydosporium in the infection process of nematode eggs. Mycological Research 100, 421428.
Shimizu, T. (1993). Prevalence of Toxocara eggs in sandpits in Tokushima city and its outskirts. The Journal of Veterinary Medical Science 55, 807811.
Smith, D. and Onions, A. H. S. (1983). The Preservation and Maintenance of Living Fungi. Commonwealth Mycological Institute, Kew, UK.
Snow, K. R., Ball, S. J. and Bewick, J. A. (1987). Prevalence of Toxocara species eggs in the soil of five east London parks. Veterinary Record 120, 6667.
Statsoft (2004). Statistica for Windows. Computer Program Manual. Version 7.0. Statsoft. Tulsa. http://www.statsoft.com.
Sturchler, D., Weiss, N. and Gassner, M. (1990). Transmission of toxocariasis. Journal Infectious Diseases 162, 571.
Taylor, M. R. H. and Holland, C. V. (2001). Toxocariasis. In Principles and Practice of Clinical Parasitology (ed. Gillespie, S. H. and Pearson, R. D.), pp. 501519. John Wiley & Sons, New York, USA.
Tikhonov, V. E., Lopez-Llorca, L. V., Salinas, J. and Jansson, H. B. (2002). Purification and characterization of chitinases from the nematophagous fungi Verticillium chlamydosporium and V. suchlasporium. Fungal Genetics and Biology 35, 6768.
Watthanakulpanich, D., Smith, H. V., Hobbs, G., Whalley, A. J. and Billington, D. (2008). Application of Toxocara canis excretory-secretory antigens and IgG subclass antibodies (IgG1–4) in serodiagnostic assays of human toxocariasis. Acta Tropica 106, 9095.
Zare, R., Gams, W. and Evans, H. C. (2001). A revision of Verticillium section Prostrata. V. The genus Pochonia, with notes on Rotiferophthora. Nova Hedwigia 73, 5186.
Zhang, C., Wu, X. and Cai, X. (2009). Effect of chitinases produced by Pochonia chlamydosporia on egg-hatching of Meloidogyne incognita. Scientia Agricultura Sinica 42, 35093515.

Keywords

Antagonistic activity of the fungus Pochonia chlamydosporia on mature and immature Toxocara canis eggs

  • A. S. MACIEL (a1), L. G. FREITAS (a1), L. D. FIGUEIREDO (a1), A. K. CAMPOS (a2) and I. N. K. MELLO (a3)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed