Skip to main content Accessibility help

Genetic influence on the kinetics and associated pathology of the early stage (intestinal-hepatic) migration of Ascaris suum in mice

  • C. DOLD (a1), J. P. CASSIDY (a2), P. STAFFORD (a1), J. M. BEHNKE (a3) and C. V. HOLLAND (a1)...


The generative mechanism(s) of aggregation and predisposition to Ascaris lumbricoides and A. suum infections in their host population are currently unknown and difficult to elucidate in humans and pigs for ethical/logistical reasons. A recently developed, optimized murine model based on 2 inbred strains, putatively susceptible (C57BL/6j) and resistant (CBA/Ca) to infection, was exploited to elucidate further the basis of the contrasting parasite burdens, most evident at the pulmonary stage. We explored the kinetics of early infection, focusing on the composite lobes of the liver and lung, over the first 8 days in an effort to achieve a more detailed understanding of the larval dispersal over time and the point at which worm burdens diverge. Larval recoveries showed a heterogenous distribution among the lobes of the lungs, being higher in the right lung of both strains, and in the susceptible strain larvae accumulating preferentially in 2 (caudal and middle) of the 4 lobes. Total larval burdens in these 2 lobes were largely responsible for the higher worm burdens in the susceptible strain. While total lung larval recoveries significantly differed between mouse strains, a difference in liver larval burdens was not observed. However, an earlier intense inflammatory response coupled with more rapid tissue repair in the hepatic lobes was observed in CBA/Ca mice, in contrast to C57BL/6j mice, and it is possible that these processes are responsible for restricting onward pulmonary larval migration in the resistant genotype.


Corresponding author

*Corresponding author: Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland. Tel: +353 (0)1 8962194. Fax: +353 (0)1 6778094. E-mail:


Hide All
Anderson, R. C. and May, R. M. (1985). Helminth infection of humans: mathematical models, population dynamics and control. Advances in Parasitology 24, 1101.
Arean, V. M. and Crandall, C. A. (1962). The effect of immunization on the fate of injected stage Ascaris lumbricoides larvae in the rabbit. American Journal of Tropical Medicine and Hygiene 11, 369379.
Bindseil, E. (1981). Pathogenesis of liver lesions in mice following a primary infection with Ascaris suum. Veterinary Pathology 18, 804812.
Boes, J., Medley, G. F., Eriksen, L., Roepstorff, A. and Nansen, P. (1998). Distribution of Ascaris suum in experimentally and naturally infected pigs and comparison with Ascaris lumbricoides infections in humans. Parasitology 117, 589596.
Copeman, D. B. and Gaafar, S. M. (1972). Sequential development of hepatic lesions of ascaridosis in colostrums-deprived pigs. Australian Veterinary Journal 48, 263268.
Croll, N. A. and Ghadirian, E. (1981). Wormy persons: Contributions to the nature and patterns of overdispersion with Ascaris lumbricoides, Ancylostoma duodenale, Necator americanus and Trichuris trichiura. Tropical and Geographical Medicine 33, 241248.
Crompton, D. W. T. (2001). Ascaris and ascariasis. Advances in Parasitology 48, 285375.
Douvres, F. W. and Tromba, F. G. (1971). Comparative development of Ascaris suum in rabbits, guinea pigs, mice and swine in eleven days. Proceedings of the Helminthological Society of Washington 38, 246252.
Eriksen, L., Andersen, S., Nielsen, K., Pedersen, A. and Nielsen, J. (1980). Experimental Ascaris suum infection in pigs. Serological response, eosinophilia in peripheral blood, occurrence of white spots in the liver and worm recovery from the intestine. Nordic Veterinary Medicine 32, 233242.
Eriksen, L., Nansen, P., Roepstorff, A., Lind, P. and Nilsson, O. (1992). Response to repeated inoculations with Ascaris suum eggs in pigs during the fattening period. I. Studies on worm population kinetics. Parasitology Research 78, 241246.
Fagerholm, H. P., Nansen, P., Roepstorff, A., Frandsen, F. and Eriksen, L. (2000). Differentiation of cuticular structures during the growth of the third-stage larva of Ascaris suum (Nematoda, Ascaridoidea) after emerging from the egg. Journal of Parasitology 86, 421427.
Fallis, M. A. (1948). Ascaris lumbricoides infection in guinea pigs with special reference to eosinophilia and resistance. Canadian Journal of Research, Series D Zoological Sciences 26, 307327.
Geenen, P. L., Bresciani, J., Boes, J., Pedersen, A., Eriksen, L., Fagerholm, H. P. and Nansen, P. (1999). The morphogenesis of Ascaris suum to the infective third-stage larvae within the egg. Journal of Parasitology 85, 616622.
Guerrero, J. and Silverman, P. H. (1969). Ascaris suum: immune reactions in mice. I. Larval metabolic and somatic antigens. Experimental Parasitology 26, 272281.
Haswell-Elkins, M. R., Elkins, D. B. and Anderson, R. M. (1987). Evidence for predisposition in humans to infection with Ascaris, hookworm, Enterobius and Trichuris in a South Indian fishing community. Parasitology 95, 323337.
Holland, C. V. (2009). Predisposition to ascariasis: patterns, mechanisms and implications. Parasitology (in the Press).
Holland, C. V. and Boes, J. (2002). Distributions and predisposition: people and pigs. In The Geohelminths: Ascaris, Trichuris and Hookworm (ed. Holland, C. V. and Kennedy, M. W.), pp. 124. Kluwer Academic Publishers, Boston/Dordrecht/London.
Holland, C. V., Asaolu, S. O., Crompton, D. W. T., Stoddard, R. C., Mc Donald, R. and Tormiro, S. E. A. (1989). The epidemiology of Ascaris lumbricoides and other soil-transmitted helminths in primary school children from Ile-Ife, Nigeria. Parasitology 99, 275285.
Holland, C. V., Crompton, D. W. T., Asaolu, S. O., Crichton, W. B., Torimiro, S. E. A. and Walters, D. E. (1992). A possible genetic factor influencing protection from infection with Ascaris lumbricoides in Nigerian children. Journal of Parasitology 78, 915916.
Inderbitzin, D., Studer, P., Sidler, D., Beldi, G., Djonov, Y., Keogh, A. and Candinas, D. (2006). Regenerative capacity of individual liver lobes in the microsurgical mouse model. Microsurgery 26, 465469.
Jenkins, D. C. (1968). Observations of early migration of larvae of Ascaris suum Goeze, 1782 in white mice. Parasitology 58, 431440.
Johnstone, C., Leventhal, R. and Soulsby, E. J. L. (1978). The spin method for recovering tissue larvae and its use in evaluating C57BL/6 mice as a model for the study of resistance to infection with Ascaris suum. The Journal of Parasitology 64, 10151020.
Jungersen, G., Fagerholm, H. P., Nansen, P. and Eriksen, L. (1999). Development of patent Ascaris suum infections in pigs following intravenous administration of larvae hatched in vitro. Parasitology 119, 503508.
Kennedy, M. W. and Qureshi, F. (1986). Stage-specific secreted antigens of the parasitic larval stages of the nematode Ascaris. Immunology 58, 515522.
Keittivuti, B. (1974). Sites of penetration of Ascaris suum larvae in experimentally infected mice and swine. Ph.D. thesis. Purdue University, Lafayette, Indiana, USA.
Kerr, K. B. (1938). The cellular response in acquired resistance in guinea pigs to an infection with pig Ascaris. American Journal of Hygiene 27, 2851.
Keymer, A. E. and Pagel, M. (1990). Predisposition to helminth infection. In Hookworm Disease: Current Status and New Directions (ed. Schad, G. A. and Warren, K. S.), pp. 177209. Taylor and Francis, London and Philadelphia.
Khoury, P. B., Stromberg, B. E. and Soulsby, E. J. L. (1977) Immune mechanisms to Ascaris suum in inbred guinea-pigs. I. Passive transfer of immunity by cells or serum. Immunology 32, 405411.
Lewis, R., Behnke, J. M., Stafford, P. and Holland, C. V. (2006). The development of a mouse model to explore resistance and susceptibility to early Ascaris suum infection. Parasitology 132, 289300.
Lewis, R., Behnke, J. M., Cassidy, J., Stafford, P., Murray, N. and Holland, C. V. (2007). The migration of Ascaris suum larvae, and the associated pulmonary inflammatory response in susceptible C57BL/6j and resistant CBA/Ca mice. Parasitology 134, 13011314.
Maronpot, R. R., Boorman, G. A. and Gaul, B. W. (1999) Pathology of the Mouse: Reference and Atlas. Cache River Press, Vienna, Illinois, USA.
McCraw, B. M. and Greenway, J. A. (1970). Ascaris suum infection in calves III. Pathology. Canadian Journal of Comparative Medicine 34, 247255.
McSharry, C., Xia, Y., Holland, C. V. and Kennedy, M. W. (1999). Natural immunity to Ascaris lumbricoides associated with immunoglobulin E antibody to ABA-1 allergen and inflammation indicators in children. Infection and Immunity 67, 16.
Mitchell, G. F., Hogarth-Scott, R. S., Edwards, R. D., Lewers, H. M., Cousins, G. and Moore, T. (1976). Studies on immune response to parasite antigens in mice 1. Ascaris suum larva numbers and antiphosphorylcholine responses to infected mice of various strains and hypothymic nu/nu mice. International Archives of Allergy and Applied Immunity 52, 6473.
Murrell, K. D., Eriksen, L., Nansen, P., Slotved, H. C. and Rasmussen, T. (1997). Ascaris suum: a revision of its early migratory path and implications for human ascariasis. Journal of Parasitology 83, 255260.
Nejsum, P., Roepstorff, A., Jørgensen, C., Fredholm, M., Görring, H. H. H., Anderson, T. J. C. and Thamsborg, S. M. (2009). High heritability for Ascaris and Trichuris infection levels in pigs. Heredity 102, 357364.
O'Lorcain, P. and Holland, C. V. (2000). The public health importance of Ascaris lumbricoides. Parasitology 121, S51S71.
Peréz, J., Garcia, P. M., Mozos, E., Bautista, M. J. and Carrasco, L. (2001). Immunohistochemical characterization of hepatic lesions associated with migrating larvae of Ascaris suum in pigs. Journal of Comparative Pathology 124, 200206.
Roepstorff, A., Eriksen, L., Slotved, H. C. and Nansen, P. (1997). Experimental Ascaris suum infection in the pig: worm population kinetics following single inoculations with three doses of infective eggs. Parasitology 115, 443452.
Ronéus, O. (1966). Studies on aetiology and pathogenesis of white spots in the liver of pigs. Dr Thesis, Acta Veterinaria Scandinavica 7, 1112.
Schwartz, B. and Alicata, J. E. (1932). Ascaris larvae as a cause of liver and lung lesions in swine. Journal of Parasitology 19, 1724.
Slotved, H. C., Eriksen, L., Murrell, K. D. and Nansen, P. (1998). Early Ascaris suum migration in mice as a model for pigs. The Journal of Parasitology 84, 1618.
Song, J. S., Kim, J. J., Min, D. Y. and Lee, K. T. (1985). Studies on the comparative migration patterns of Ascaris suum larvae between primary and re-infected mice. Kisaengchunghak Chapchi 23, 247252.
Soulsby, E. J. L. (1957). Immunization against Ascaris lumbricoides in the guinea pig. Nature, London 179, 783784.
Sprent, J. F. A. and Chen, H. H. (1949). Immunological studies in mice infected with the larvae of Ascaris lumbricoides. I. Criteria of immunity and immunizing effect of isolated worm tissues. Journal of Infectious Diseases 84, 111124.
Stromberg, B. E. (1979). The isolation and partial characterisation of a protective antigen from developing larvae of Ascaris suum. International Journal for Parasitology 9, 307311.
Taffs, L. F. (1968). Immunological studies on experimental infection of pigs with Ascaris suum Goeze, 1782. VI. The histopathology of the liver and lung. Journal of Helminthology 42, 157172.
Williams-Blangero, S., Vandeberg, J. L., Subedi, J., Jha, B., Correa-Oliveira, R. and Blangero, J. (2008). Localization of multiple quantitative trait loci influencing susceptibility to infection with Ascaris lumbricoides. The Journal of Infectious Diseases 197, 6671.



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