Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-23T22:32:27.374Z Has data issue: false hasContentIssue false
  • English
  • Français

Ascaris lumbricoides and Ascaris suum vary in their larval burden in a mouse model

Published online by Cambridge University Press:  26 February 2020

G. Deslyper Open the ORCID record for G. Deslyper [Opens in a new window] ,
O.A. Sowemimo ,
J. Beresford  and
C.V. Holland
G. Deslyper*
Affiliation:
Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin, Ireland
O.A. Sowemimo
Affiliation:
Department of Zoology, Obafemi Awolowo University, Ile-Ife, Osun State, Nigeria
J. Beresford
Affiliation:
Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin, Ireland
C.V. Holland
Affiliation:
Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin, Ireland
*
Author for correspondence: G. Deslyper, E-mail: deslypeg@tcd.ie
Get access Rights & Permissions [Opens in a new window]

Abstract

Ascariasis is a neglected tropical disease, caused by Ascaris lumbricoides, affecting 800 million people worldwide. Studies focused on the early stage of parasite infection, occurring in the gut, liver and lungs, require the use of a mouse model. In these models, the porcine ascarid, Ascaris suum, is often used. The results obtained from these studies are then used to draw conclusions about A. lumbricoides infections in humans. In the present study, we sought to compare larval migration of A. suum and A. lumbricoides in mouse models. We used a previously developed mouse model of ascariasis, which consists of two mouse strains, where one mouse strain – C57BL/6J – is a model for relative susceptibility and the other – CBA/Ca – for relative resistance. Mice of both strains were infected with either A. suum or A. lumbricoides. The larval burden was assessed in two key organs, the liver and lungs, starting at 6 h post infection (p.i.) and ending on day 8 p.i. Additionally, we measured the larval size of each species (μm) at days 6, 7 and 8 p.i. in the lungs. We found that larval burden in the liver is significantly higher for A. lumbricoides than for A. suum. However, the inverse is true in the lungs. Additionally, our results showed a reduced larval size for A. lumbricoides compared to A. suum.

Keywords

Ascaris lumbricoidesAscaris suumliverlungsmigrationmouse model
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e128
Copyright
Copyright © The Author(s) 2020. Published by 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

Anderson, TJ (1995) Ascaris infections in humans from North America: molecular evidence for cross-infection. Parasitology 110(Pt 2), 215–219.CrossRefGoogle ScholarPubMed
Anderson, TJ, Romero-Abal, ME and Jaenike, J (1993) Genetic structure and epidemiology of Ascaris populations: patterns of host affiliation in Guatemala. Parasitology 107(Pt 3), 319–334.CrossRefGoogle ScholarPubMed
Ansel, M and Thibaut, M (1973) Value of the specific distinction between Ascaris lumbricoides Linnè 1758 and Ascaris suum Goeze 1782. International Journal for Parasitology 3, 317–319.CrossRefGoogle ScholarPubMed
Arizono, N, Yoshimura, Y, Tohzaka, N, Yamada, M, Tegoshi, T, Onishi, K and Uchikawa, R (2010) Ascariasis in Japan: is pig-derived Ascaris infecting humans? Japanese Journal of Infectious Diseases 63, 447–448.Google ScholarPubMed
Betson, M, Nejsum, P and Stothard, JR (2013) From the twig tips to the deeper branches: new insights into evolutionary history and phylogeography of Ascaris. pp. 265–285 In Holland, C (Ed.) Ascaris: the neglected parasite. Amsterdam, Elsevier.Google Scholar
Betson, M, Nejsum, P, Bendall, RP, Deb, RM and Stothard, JR (2014) Molecular epidemiology of ascariasis: a global perspective on the transmission dynamics of Ascaris in people and pigs. The Journal of Infectious Diseases 210, 932–941.CrossRefGoogle ScholarPubMed
Bhowmick, DK (1964) Beiträge zu dem Problem der Wanderwege der Askaridenlarven (Ascaris lumbricoides Linné 1758 und Toxocara canis Werner 1782) im experimentellen und natürlichen Wirt. Zeitschrift für Parasitenkunde 24, 121–168.CrossRefGoogle Scholar
Boes, J, Eriksen, L and Nansen, P (1998a) Embryonation and infectivity of Ascaris suum eggs isolated from worms expelled by pigs treated with albendazole, pyrantel pamoate, ivermectin or piperazine dihydrochloride. Veterinary Parasitology 75, 181–190.CrossRefGoogle Scholar
Boes, J, Medley, GF, Eriksen, L, Roepstorff, A and Nansen, P (1998b) Distribution of Ascaris suum in experimentally and naturally infected pigs and comparison with Ascaris lumbricoides infections in humans. Parasitology 117(Pt 6), 589–596.CrossRefGoogle Scholar
Boes, J, Kanora, A, Havn, KT, Christiansen, S, Vestergaard-Nielsen, K, Jacobs, J and Alban, L (2010) Effect of Ascaris suum infection on performance of fattening pigs. Veterinary Parasitology 172, 269–276.CrossRefGoogle ScholarPubMed
Buske, M and Engelbrecht, H (1968) Über die Larva migrans visceralis von Ascaris lumbricoides im Experimentalwirt (Maus). Zeitschrift für Parasitenkunde 30, 337–346.CrossRefGoogle Scholar
Cho, MJ (1967) Experimental studies on the efficacy of thiabendazole against the migratory stages of Ascarids in mouse. Kisaengchunghak Chapchi 5, 35–50.Google Scholar
Criscione, CD, Anderson, JD, Sudimack, D, Peng, W, Jha, B, Williams-Blangero, S and Anderson, TJ (2007) Disentangling hybridization and host colonization in parasitic roundworms of humans and pigs. Proceedings of the Royal Society B: Biological Sciences 274, 2669–2677.CrossRefGoogle ScholarPubMed
Crofton, HD (1971) A quantitative approach to parasitism. Parasitology 63, 343–364.CrossRefGoogle Scholar
Croll, NA and Ghadirian, E (1981) Wormy persons: contributions to the nature and patterns of overdispersion with Ascaris lumbricoides, Ancylosotma duodenale, Necator americanus and Trichuris trichiura. Tropical and Geographical Medicine 33, 241–248.Google ScholarPubMed
Deslyper, G and Holland, CV (2017) Overview on ascariasis in humans in South Asia. pp. 83–120In Singh, SK (Ed.) Neglected tropical diseases-South Asia. Cham, Springer.CrossRefGoogle Scholar
Deslyper, G, Colgan, TJ, Cooper, AJ, Holland, CV and Carolan, JC (2016) A proteomic investigation of hepatic resistance to Ascaris in a murine model. PLOS Neglected Tropical Diseases 10, e0004837.CrossRefGoogle Scholar
Deslyper, G, Doherty, DG, Carolan, JC and Holland, CV (2019a) The role of the liver in the migration of parasites of global significance. Parasit Vectors 12, 531.CrossRefGoogle Scholar
Deslyper, G, Holland, CV, Colgan, TJ and Carolan, JC (2019b) The liver proteome in a mouse model for Ascaris suum resistance and susceptibility: evidence for an altered innate immune response. Parasit Vectors 12, 402.CrossRefGoogle Scholar
Dold, C and Holland, CV (2011) Ascaris and ascariasis. Microbes and Infection 13, 632–637.CrossRefGoogle ScholarPubMed
Dold, C, Cassidy, JP, Stafford, P, Behnke, JM and Holland, CV (2010) Genetic influence on the kinetics and associated pathology of the early stage (intestinal-hepatic) migration of Ascaris suum in mice. Parasitology 137, 173–185.CrossRefGoogle ScholarPubMed
Douvres, FW and Tromba, FG (1971) Comparative development of Ascaris suum in rabbits, guinea pigs, mice and swine in 11 days. Proceedings of the Helminthological Society 38, 236–242.Google Scholar
Gazzinelli-Guimarães, PH, Gazzinelli-Guimarães, AC, Silva, FN, et al. (2013) Parasitological and immunological aspects of early Ascaris spp. infection in mice. International Journal for Parasitology 43, 697–706.CrossRefGoogle ScholarPubMed
Geenen, PL, Bresciani, J, Boes, J, Pedersen, A, Eriksen, L, Fagerholm, HP and Nansen, P (1999) The morphogenesis of Ascaris suum to the infective third-stage larvae within the egg. Journal of Parasitology 85, 616–622.CrossRefGoogle Scholar
Holland, CV (2009) Predisposition to ascariasis: patterns, mechanisms and implications. Parasitology 136, 1537–1547.CrossRefGoogle ScholarPubMed
Holland, CV, Asaolu, SO, Crompton, DW, Stoddart, RC, Macdonald, R and Torimiro, SE (1989) The epidemiology of Ascaris lumbricoides and other soil-transmitted helminths in primary school children from Ile-Ife, Nigeria. Parasitology 99(Pt 2), 275–285.CrossRefGoogle ScholarPubMed
Holland, CV, Behnke, JM and Dold, C (2013) Larval Ascariasis: impact, significance, and model organisms. pp. 107–125In Holland, C (Ed.) Ascaris: the neglected parasite. Amsterdam, Elsevier.CrossRefGoogle Scholar
Johnstone, C, Leventhal, R and Soulsby, EJ (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. Journal of Parasitology 64, 1015–1020.CrossRefGoogle Scholar
Jourdan, PM, Lamberton, PHL, Fenwick, A and Addiss, DG (2018) Soil-transmitted helminth infections. Lancet 391, 252–265.CrossRefGoogle ScholarPubMed
Kumar, V and Singh, KS (1968) In vivo behaviour of Ascaris lumbricoides eggs and the emerging juveniles. Indian Journal of Medical Research 56, 1304–1308.Google ScholarPubMed
Lewis, R, Behnke, JM, Stafford, P and Holland, CV (2006) The development of a mouse model to explore resistance and susceptibility to early Ascaris suum infection. Parasitology 132, 289–300.CrossRefGoogle ScholarPubMed
Lewis, R, Behnke, JM, Cassidy, JP, Stafford, P, Murray, N and Holland, CV (2007) The migration of Ascaris suum larvae, and the associated pulmonary inflammatory response in susceptible C57BL/6j and resistant CBA/Ca mice. Parasitology 134, 1301–1314.CrossRefGoogle ScholarPubMed
Liu, GH, Wu, CY, Song, HQ, Wei, SJ, Xu, MJ, Lin, RQ, Zhao, GH, Huang, SY and Zhu, XQ (2012) Comparative analyses of the complete mitochondrial genomes of Ascaris lumbricoides and Ascaris suum from humans and pigs. Gene 492, 110–116.CrossRefGoogle ScholarPubMed
Loeffler, W (1932) Zur Differentialdiagnose der Lungen-infiltrierungen. II Ueber fluchtige Succedanininfiltrate (mit Eosinophilie). Beiträge zur Klinik der Tuberkulose 79, 368–382.Google Scholar
Loeffler, W (1956) Transient lung infiltrations with blood eosinophilia. International Archives of Allergy and Immunology 8, 54–59.CrossRefGoogle Scholar
Massara, CL, Costa, HM and Carvalho, OoS (1990) Contribuição para o estudo do Ascaris lumbricoides em laboratório. Revista da Sociedade Brasileira de Medicina Tropical 23, 43–47.CrossRefGoogle Scholar
Massara, CL, Costa, HM, De Souza, DW, Souza, MS and Carvalho, OoS (1991) Viability of Ascaris lumbricoides eggs eliminated after anti-helminthic therapy. Memórias do Instituto Oswaldo Cruz 86, 233–237.CrossRefGoogle ScholarPubMed
Maung, M (1973) Ascaris lumbricoides Linné, 1758 and Ascaris suum Goeze, 1782: morphological differences between specimens obtained from man and pig. Southeast Asian Journal of Tropical Medicine and Public Health 4, 41–45.Google ScholarPubMed
Maung, M (1978) The occurrence of the second moult of Ascaris lumbricoides and Ascaris suum. International Journal for Parasitology 8, 371–378.CrossRefGoogle ScholarPubMed
Murrell, KD, Eriksen, L, Nansen, P, Slotved, HC and Rasmussen, T (1997) Ascaris suum: a revision of its early migratory path and implications for human ascariasis. Journal of Parasitology 83, 255–260.CrossRefGoogle ScholarPubMed
Nejsum, P, Parker, ED, Frydenberg, J, Roepstorff, A, Boes, J, Haque, R, Astrup, I, Prag, J and Skov Sørensen, UB (2005) Ascariasis is a zoonosis in Denmark. Journal of Clinical Microbiology 43, 1142–1148.CrossRefGoogle ScholarPubMed
Nejsum, P, Roepstorff, A, Anderson, TJ, Jørgensen, C, Fredholm, M and Thamsborg, SM (2009) The dynamics of genetically marked Ascaris suum infections in pigs. Parasitology 136, 193–201.CrossRefGoogle ScholarPubMed
Nogueira, DS, Gazzinelli-Guimarães, PH, Barbosa, FS, et al. (2016) Multiple exposures to Ascaris suum induce tissue injury and mixed Th2/Th17 immune response in mice. PLoS Neglected Tropical Diseases 10, e0004382.CrossRefGoogle ScholarPubMed
O'Lorcain, P and Holland, CV (2000) The public health importance of Ascaris lumbricoides. Parasitology 121 ,S51–S71.CrossRefGoogle ScholarPubMed
Peng, W, Yuan, K, Peng, G, Qiu, L, Dai, Z, Yuan, F, Hu, Y and Hu, N (2012) Ascaris: development of selected genotypes in mice. Experimental Parasitology 131, 69–74.CrossRefGoogle ScholarPubMed
Pullan, RL, Smith, JL, Jasrasaria, R and Brooker, SJ (2014) Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors 7, 37.CrossRefGoogle ScholarPubMed
R Core Team (2018) R: a language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing.Google Scholar
Ribeiro, JD and Fisher, GB (2002) Eosinophilic lung diseases. Paediatric Respiratory Reviews 3, 278–284.CrossRefGoogle ScholarPubMed
Roepstorff, A, Eriksen, L, Slotved, HC 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(Pt 4), 443–452.CrossRefGoogle ScholarPubMed
Shaw, DJ and Dobson, P (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111–S133.CrossRefGoogle ScholarPubMed
Song, JS, Kim, JJ, Min, DY and Lee, KT (1985) Studies on the comparative migration patterns of Ascaris suum larvae between primary and re-infected mice. Kisaengchunghak Chapchi 23, 247–252.Google ScholarPubMed
Sprent, JF (1952a) Anatomical distinction between human and pig strains of Ascaris. Nature 170, 627–628.CrossRefGoogle Scholar
Sprent, JFA (1952b) On the migratory behavior of the larvae of various Ascaris species in white mice. I. Distribution of larvae in tissues. The Journal of Infectious Diseases 90, 165–176.CrossRefGoogle Scholar
Stewart, FH (1917) On the development of Ascaris lumbricoides Lin. and Ascaris suilla Duj. in the rat and mouse. Parasitology 9, 213–227.CrossRefGoogle Scholar
Stewart, FH (1918) On the development of Ascaris lumbricoides and A. mystax in the mouse. Parasitology 10, 189–196.CrossRefGoogle Scholar
Stewart, TB, Southern, LL, Gibson, RB and Simmons, LA (1985) Immunization of pigs against Ascaris suum by sequential experimental infections terminated with fenbendazole during larval migration. Veterinary Parasitology 17, 319–326.CrossRefGoogle ScholarPubMed
Venables, W and Ripley, B (2002) Modern applied statistics. 4th edn. New York, Springer.CrossRefGoogle Scholar
Wright, JE, Werkman, M, Dunn, JC and Anderson, RM (2018) Current epidemiological evidence for predisposition to high or low intensity human helminth infection: a systematic review. Parasites & Vectors 11, 65.CrossRefGoogle ScholarPubMed
Zeileis, A, Kleiber, C and Jackman, S (2008) Regression models for count data in R. Journal of Statistical Software 27, 1–25.CrossRefGoogle Scholar
Zhou, C, Li, M, Yuan, K, Deng, S and Peng, W (2012) Pig Ascaris: an important source of human ascariasis in China. Infection, Genetics and Evolution 12, 1172–1177.CrossRefGoogle Scholar
Zhu, X, Chilton, NB, Jacobs, DE, Boes, J and Gasser, RB (1999) Characterisation of Ascaris from human and pig hosts by nuclear ribosomal DNA sequences. International Journal for Parasitology 29, 469–478.CrossRefGoogle ScholarPubMed
Supplementary material: File

Deslyper et al. supplementary material

Tables S1-S2

Download Deslyper et al. supplementary material(File)
File 13 KB