Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-17T17:22:49.224Z Has data issue: false hasContentIssue false
  • English
  • Français

Assessing the zoonotic potential of Ascaris suum and Trichuris suis: looking to the future from an analysis of the past

Published online by Cambridge University Press:  19 March 2012

P. Nejsum ,
M. Betson ,
R.P. Bendall ,
S.M. Thamsborg  and
J.R. Stothard
P. Nejsum*
Affiliation:
Danish Centre for Experimental Parasitology, Department of Veterinary Disease Biology, Faculty of Life Sciences, University of Copenhagen, Copenhagen, Denmark Genetics and Bioinformatics, Department of Basic Animal and Veterinary Sciences, Faculty of Life Sciences, Copenhagen University
M. Betson
Affiliation:
Disease Control Strategy Group, Liverpool School of Tropical Medicine, Liverpool, UK
R.P. Bendall
Affiliation:
Royal Cornwall Hospital, Clinical Microbiology, Truro, UK
S.M. Thamsborg
Affiliation:
Danish Centre for Experimental Parasitology, Department of Veterinary Disease Biology, Faculty of Life Sciences, University of Copenhagen, Copenhagen, Denmark
J.R. Stothard
Affiliation:
Disease Control Strategy Group, Liverpool School of Tropical Medicine, Liverpool, UK
*
*Fax: +45 35282774 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The two geohelminths, Ascaris lumbricoides and Trichuris trichiura, infect more than a billion people worldwide but are only reported sporadically in the developed part of the world. In contrast, the closely related species A. suum and T. suis in pigs have a truly global distribution, with infected pigs found in most production systems. In areas where pigs and humans live in close proximity or where pig manure is used as fertilizer on vegetables for human consumption, there is a potential risk of cross-infections. We therefore review this relationship between Ascaris and Trichuris in the human and pig host, with special focus on recent evidence concerning the zoonotic potential of these parasites, and identify some open questions for future research.

Type
Research Papers
Information
Journal of Helminthology , Volume 86 , Issue 2 , June 2012 , pp. 148 - 155
Copyright
Copyright © Cambridge University Press 2012

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

Abebe, W., Tsuji, N., Kasuga-Aoki, H., Miyoshi, T., Isobe, T., Arakawa, T., Matsumoto, Y. & Yoshihara, S. (2002a) Lung-stage protein profile and antigenic relationship between Ascaris lumbricoides and Ascaris suum. Journal for Parasitology 88, 826–828.Google Scholar
Abebe, W., Tsuji, N., Kasuga-Aoki, H., Miyoshi, T., Isobe, T., Arakawa, T., Matsumoto, Y. & Yoshihara, S. (2002b) Species-specific proteins identified in Ascaris lumbricoides and Ascaris suum using two-dimensional electrophoresis. Parasitology Research 88, 868–871.CrossRefGoogle ScholarPubMed
Anderson, T.J.C. (1995) Ascaris infections in humans from North America: molecular evidence for cross-infection. Parasitology 110, 215–219.CrossRefGoogle ScholarPubMed
Anderson, T.J.C. (2001) The dangers of using single locus markers in parasite epidemiology: Ascaris as a case study. Trends in Parasitology 17, 183–188.CrossRefGoogle ScholarPubMed
Anderson, T.J.C. & Jaenike, J. (1997) Host specificity, evolutionary relationships and macrogeographic differentiation among Ascaris populations from humans and pigs. Parasitology 115, 325–342.CrossRefGoogle ScholarPubMed
Anderson, T.J.C., Romero-Abal, M.E. & Jaenike, J. (1993) Genetic structure and epidemiology of Ascaris populations: patterns of host affiliation in Guatemala. Parasitology 107, 319–334.CrossRefGoogle ScholarPubMed
Ansel, M. & Thibaut, M. (1973) Value of the specific distinction between Ascaris lumbricoides Linne 1758 and Ascaris suum Goeze 1782. International Journal for Parasitology 3, 317–319.Google Scholar
Areekul, P., Putaporntip, C., Pattanawong, U., Sitthicharoenchai, P. & Jongwutiwes, S. (2010) Trichuris vulpis and T. trichiura infections among schoolchildren of a rural community in northwestern Thailand: the possible role of dogs in disease transmission. Asian Biomedicine 4, 49–60.Google Scholar
Arizono, N., Yoshimura, Y., Tohzaka, N., Yamada, M., Tegoshi, T., Onishi, K. & Uchikawa, R. (2010) Ascariasis in Japan: is pig-derived Ascaris infecting humans? Japanese Journal of Infectious Diseases 63, 447–448.CrossRefGoogle ScholarPubMed
Beer, R.J.S. (1973) Studies on the biology of the life-cycle of Trichuris suis Schrank, 1788. Parasitology 67, 253–262.CrossRefGoogle ScholarPubMed
Beer, R.J.S. (1976) Relationship between Trichuris trichiura (Linnaeus 1758) of man and Trichuris suis (Schrank 1788) of pig. Research in Veterinary Science 20, 47–54.CrossRefGoogle ScholarPubMed
Bendall, R.P., Barlow, M., Betson, M., Stothard, J.R. & Nejsum, P. (2011) Zoonotic ascariasis. United Kingdom. Emerging Infectious Diseases 17, 1964–1966.CrossRefGoogle ScholarPubMed
Bethony, J., Brooker, S., Albonico, M., Geiger, S.M., Loukas, A., Diemert, D. & Hotez, P.J. (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367, 1521–1532.Google Scholar
Betson, M., Halstead, F.D., Nejsum, P., Imison, E., Khamis, I.S., Sousa-Figueiredo, J.C., Rollinson, D. & Stothard, J.R. (2011) A molecular epidemiological investigation of Ascaris on Unguja, Zanzibar using isoenyzme analysis, DNA barcoding and microsatellite DNA profiling. Transactions of the Royal Society of Tropical Medicine and Hygiene 105, 370–379.CrossRefGoogle ScholarPubMed
Boes, J., Willingham, A.L., Fuhui, S., Hu, X.G., Eriksen, L., Nansen, P. & Stewart, T.B. (2000) Prevalence and distribution of pig helminths in the Dongting Lake Region (Hunan Province) of the People's Republic of China. Journal of Helminthology 74, 45–52.CrossRefGoogle ScholarPubMed
Brooker, S. (2010) Estimating the global distribution and disease burden of intestinal nematode infections: Adding up the numbers - a review. International Journal for Parasitology 40, 1137–1144.CrossRefGoogle ScholarPubMed
Bundy, D.A.P. & Cooper, E.S. (1989) Trichuris and Trichuriasis in humans. Advances in Parasitology 28, 107–173.CrossRefGoogle ScholarPubMed
Burden, D.J., Hammet, N.C. & Brookes, P.A. (1987) Field observations on the longevity of Trichuris suis ova. Veterinary Record 121, 43.CrossRefGoogle ScholarPubMed
Carstensen, L., Vaarst, M. & Roepstorff, A. (2002) Helminth infections in Danish organic swine herds. Veterinary Parasitology 106, 253–264.Google Scholar
Chan, M.S. (1997) The global burden of intestinal nematode infections – fifty years on. Parasitology Today 13, 438–443.Google Scholar
Clark, E.G., Vondewitz, A. & Acompanado, G. (1989) Spurious Ascaris suum Infection in lambs. Canadian Veterinary Journal 30, 903.Google ScholarPubMed
Crewe, W. & Smith, D.H. (1971) Human infection with pig Ascaris (A. suum). Annals of Tropical Medicine and Parasitology 65, 85.CrossRefGoogle ScholarPubMed
Criscione, C.D., Anderson, J.D., Sudimack, D., Peng, W., Jha, B., Williams-Blangero, S. & Anderson, T.J.C. (2007) Disentangling hybridization and host colonization in parasitic roundworms of humans and pigs. Proceedings of the Royal Society Biological Sciences 274, 2669–2677.CrossRefGoogle ScholarPubMed
Crompton, D.W. (2001) Ascaris and ascariasis. Advances in Parasitology 48, 285–375.Google Scholar
Cutillas, C., Callejon, R., de Rojas, M., Tewes, B., Ubeda, J.M., Ariza, C. & Guevara, D.C. (2009) Trichuris suis and Trichuris trichiura are different nematode species. Acta Tropica 111, 299–307.Google Scholar
De Silva, N.R., Chan, M.S. & Bundy, D.A.P. (1997) Morbidity and mortality due to ascariasis: re-estimation and sensitivity analysis of global numbers at risk. Tropical Medicine & International Health 2, 519–528.Google Scholar
De Silva, N.R., Brooker, S., Hotez, P.J., Montresor, A., Engels, D. & Savioli, L. (2003) Soil-transmitted helminth infections: updating the global picture. Trends in Parasitology 19, 547–551.Google Scholar
Dold, C. & Holland, C.V. (2011) Ascaris and ascariasis. Microbes Infections 13, 632–637.Google Scholar
Eijck, I.A.J.M. & Borgsteede, F.H.M. (2005) A survey of gastrointestinal pig parasites on free-range, organic and conventional pig farms in The Netherlands. Veterinary Research Communications 29, 407–414.Google Scholar
Fisher, M. (2003) Toxocara cati: an underestimated zoonotic agent. Trends in Parasitology 19, 167–170.CrossRefGoogle ScholarPubMed
Galvin, T.J. (1968) Development of human and pig Ascaris in the pig and rabbit. Journal for Parasitology 54, 1085–1091.CrossRefGoogle Scholar
Hall, A., Hewitt, G., Tuffrey, V. & de Silva, N. (2008) A review and meta-analysis of the impact of intestinal worms on child growth and nutrition. Maternal and Child Nutrition 4 (Suppl. 1), 118–236.CrossRefGoogle ScholarPubMed
Hawley, J.H. & Peanasky, R.J. (1992) Ascaris suum: are trypsin inhibitors involved in species specificity of Ascarid nematodes? Experimental Parasitology 75, 112–118.CrossRefGoogle ScholarPubMed
Hill, C.H. (1957) The survival of swine whipworm eggs in hog lots. Journal of Parasitology 43, 104.CrossRefGoogle Scholar
Holland, C. & Boes, J. (2002) Distribution and predisposition: people and pigs. pp. 1–24 in Holland, C.V. & Kennedy, M.W. (Eds) The geohelminths: Ascaris, Trichuris and hookworm. World class parasite, vol. 2. Boston, Kluwer Academic Publishers.CrossRefGoogle Scholar
Hotez, P.J., Brindley, P.J., Bethony, J.M., King, C.H., Pearce, E.J. & Jacobson, J. (2008) Helminth infections: the great neglected tropical diseases. Journal of Clinical Investigation 118, 1311–1321.Google Scholar
Inatomi, Y., Murakami, T., Tokunaga, M., Ishiwata, K., Nawa, Y. & Uchino, M. (1999) Encephalopathy caused by visceral larva migrans due to Ascaris suum. Journal of the Neurological Sciences 164, 195–199.Google Scholar
Jaskoski, B.J. (1961) An apparent swine Ascaris infection of man. Journal of the American Veterinary Association 138, 504–505.Google ScholarPubMed
Jex, A.R., Liu, S., Li, B., Young, N.D., Hall, R.S., Li, Y., Yang, L., Zeng, N., Xu, X., Xiong, Z., Chen, F., Wu, X., Zhang, G., Fang, X., Kang, Y., Anderson, G.A., Harris, T.W., Campbell, B.E., Vlaminck, J., Wang, T., Cantacessi, C., Schwarz, E.M., Ranganathan, S., Geldhof, P., Nejsum, P., Sternberg, P.W., Yang, H., Wang, J., Wang, J. & Gasser, R.B. (2011) Ascaris suum draft genome. Nature 479, 529–533.Google Scholar
Kelley, G.W. & Smith, L.J. (1956) The daily egg production of Ascaris suum and the inability of low levels of aureomycin to affect egg production and embryonation. Journal of Parasitology 42, 587.Google Scholar
Kennedy, M.W., Qureshi, F., Haswell-Elkins, M. & Elkins, D.B. (1987) Homology and heterology between the secreted antigens of the parasitic larval stages of Ascaris lumbricoides and Ascaris suum. Clinical and Experimental Immunology 67, 20–30.Google ScholarPubMed
Knight, R.A. (1984) Morphological differences in Trichuris ovis associated with different host species. Journal of Parasitology 70, 842–843.CrossRefGoogle ScholarPubMed
Kradin, R.L., Badizadegan, K., Auluck, P., Korzenik, J. & Lauwers, G.Y. (2006) Iatrogenic Trichuris suis infection in a patient with Crohn disease. Archives of Pathology and Laboratory Medicine 130, 718–720.CrossRefGoogle Scholar
Krasnonos, L. (1978) Prolonged survival of Ascaris lumbricoides L.,1758 ova in the soil in Samarkand. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 47, 103–105(in Russian).Google Scholar
Kringel, H. & Roepstorff, A. (2006) Trichuris suis population dynamics following a primary experimental infection. Veterinary Parasitology 139, 132–139.CrossRefGoogle ScholarPubMed
Lee, A.C., Schantz, P.M., Kazacos, K.R., Montgomery, S.P. & Bowman, D.D. (2010) Epidemiologic and zoonotic aspects of ascarid infections in dogs and cats. Trends in Parasitology 26, 155–161.CrossRefGoogle ScholarPubMed
Liu, G.H., Wu, C.Y., Song, H.Q., Wei, S.J., Xu, M.J., Lin, R.Q., Zhao, G.H., Huang, S.Y. & Zhu, X.Q. (2012a) Comparative analyses of the complete mitochondrial genomes of Ascaris lumbricoides and Ascaris suum from humans and pigs. Gene 15, 110–116.CrossRefGoogle Scholar
Liu, G.H., Gasser, R.B., Su, A., Nejsum, P., Wei, S.J., Peng, L., Lin, R.Q., Li, M.W. & Zhu, X.Q. (2012b) Clear genetic distinctiveness between human- and pig-derived Trichuris based on analyses of mitochondrial datasets. PLoS Neglected Tropical Diseases 6, e1539.CrossRefGoogle ScholarPubMed
Lord, W.D. & Bullock, W.L. (1982) Swine Ascaris in humans. New England Journal of Medicine 306, 1113.Google Scholar
Loreille, O. & Bouchet, F. (2003) Evolution of ascariasis in humans and pigs: a multi-disciplinary approach. Memorias do Instituto Oswaldo Cruz 98, 39–46.CrossRefGoogle ScholarPubMed
Maguire, J. (2005) Intestinal roundworms. pp. 3260–3267in Mandell, G.L., Bennett, J.E. & Dolin, R. (Eds) Principles and practice of infectious diseases. 6th edn. Philadelphia, Elsevier.Google Scholar
Maung, M. (1973) Ascaris lumbricoides Linne, 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
Mayr, E. (1963) Animal species and evolution. Cambridge, Belknap Press.Google Scholar
McCraw, B.M. & Lautenslager, J.P. (1971) Pneumonia in calves associated with migrating Ascaris suum larvae. Canadian Veterinary Journal 12, 87–90.Google ScholarPubMed
Muller, G. (1953) Untersuchungen über die Lebensdauer von Askarideneiern in Gartenerde. Zentrallblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene 159, 377–379 (in German).Google Scholar
Nadler, S.A. (1987) Biochemical and immunological systematics of some ascaridoid nematodes: genetic divergence between congeners. Journal for Parasitology 73, 811–816.CrossRefGoogle ScholarPubMed
Nansen, P. & Roepstorff, A. (1999) Parasitic helminths of the pig: factors influencing transmission and infection levels. International Journal for Parasitology 29, 877–891.CrossRefGoogle ScholarPubMed
Nejsum, P., Parker, E.D., Frydenberg, J., Roepstorff, A., Boes, J., Haque, R., Astrup, I., Prag, J. & Sørensen, U.B.S. (2005) Ascariasis is a zoonosis in Denmark. Journal of Clinical Microbiology 43, 1142–1148.CrossRefGoogle ScholarPubMed
Nejsum, P., Thamsborg, S.M., Petersen, H.H., Kringel, H., Fredholm, M. & Roepstorff, A. (2009) Population dynamics of Ascaris suum in trickle-infected pigs. Journal of Parasitology 95, 1048–1053.CrossRefGoogle ScholarPubMed
Nejsum, P., Bertelsen, M.F., Betson, M., Stothard, J.R. & Murrell, K.D. (2010) Molecular evidence for sustained transmission of zoonotic Ascaris suum among zoo chimpanzees (Pan troglodytes). Veterinary Parasitolology 171, 273–276.Google Scholar
Nissen, S., Poulsen, I.H., Nejsum, P., Olsen, A., Roepstorff, A., Rubaire-Akiiki, C. & Thamsborg, S.M. (2011) Prevalence of gastrointestinal nematodes in growing pigs in Kabale District in Uganda. Tropical Animal Health and Production 43, 567–572.CrossRefGoogle ScholarPubMed
Nissen, S., Al-Jubury, A., Hansen, T.V.A., Olsen, A., Christensen, H., Thamsborg, S.M. & Nejsum, P. (2012) Genetic analysis of Trichuris recovered from human and pigs in a sympatric setting in Uganda. Veterinary Parasitology accepted.Google Scholar
Olsen, A., Namwanje, H., Nejsum, P., Roepstorff, A. & Thamsborg, S.M. (2009) Albendazole and mebendazole have low efficacy against Trichuris trichiura in school-age children in Kabale District, Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 443–446.CrossRefGoogle ScholarPubMed
Olsen, L.S., Kelley, G.W. & Sen, H.G. (1958) Longevity and egg-production of Ascaris suum. Transactions of the American Microscopy Society 77, 380–383.CrossRefGoogle Scholar
Ooi, H.K., Tenora, F., Itoh, K. & Kamiya, M. (1993) Comparative study of Trichuris trichiura from non-human primates and from man, and their difference with T. suis. Journal of Veterinary Medical Science 55, 363–366.Google Scholar
Pedersen, K., Monrad, J., Henriksen, S.A., Bindseil, B., Nielsen, J.S., Jensen, E. & Knold, P. (1992) Infektion med svinets spolorm (Ascaris suum) hos lam. Dansk Veterinærtidsskrift 75, 170–174.Google Scholar
Pedersen, S. & Saeed, I. (2000) Experimental infection of pigs with three dose levels of Trichuris suis. Parasite 7, 275–281.CrossRefGoogle ScholarPubMed
Peng, W., Anderson, T.J., Zhou, X. & Kennedy, M.W. (1998) Genetic variation in sympatric Ascaris populations from humans and pigs in China. Parasitology 117, 355–361.CrossRefGoogle ScholarPubMed
Peng, W.D., Yuan, K., Zhou, X.M., Hu, M., El Osta, Y.G.A. & Gasser, R.B. (2003) Molecular epidemiological investigation of Ascaris genotypes in China based on single-strand conformation polymorphism analysis of ribosomal DNA. Electrophoresis 24, 2308–2315.CrossRefGoogle Scholar
Peng, W.D., Yuan, K., Hu, M., Zhou, X.M. & Gasser, R.B. (2005) Mutation scanning-coupled analysis of haplotypic variability in mitochondrial DNA regions reveals low gene flow between human and porcine Ascaris in endemic regions of China. Electrophoresis 26, 4317–4326.Google Scholar
Phillipson, R.F. & Race, J.W. (1967) Human infection with porcine Ascaris. British Medical Journal 3, 865.Google Scholar
Pinelli, E., Willers, S.M., Hoek, D., Smit, H.A., Kortbeek, L.M., Hoekstra, M., de Jongste, J., van Knapen, F., Postma, D., Kerkhof, M., Aalberse, R., van der Giessen, J.W. & Brunekreef, B. (2009) Prevalence of antibodies against Ascaris suum and its association with allergic manifestations in 4-year-old children in The Netherlands: the PIAMA birth cohort study. European Journal of Clinical Microbiology and Infectious Diseases 28, 1327–1334.CrossRefGoogle ScholarPubMed
Pinelli, E., Herremans, T., Harms, M.G., Hoek, D. & Kortbeek, L.M. (2011) Toxocara and Ascaris seropositivity among patients suspected of visceral and ocular larva migrans in the Netherlands: trends from 1998 to 2009. European Journal of Clinical Microbiology and Infectious Diseases 30, 873–879.CrossRefGoogle ScholarPubMed
Räisänen, S., Ruuskanen, L. & Nyman, S. (1985) Epidemic ascariasis – evidence of transmission by imported vegetables. Scandinavian Journal of Primary Health Care 3, 189–191.CrossRefGoogle ScholarPubMed
Roepstorff, A. & Jorsal, S.E. (1989) Prevalence of helminth infections in swine in Denmark. Veterinary Parasitology 33, 231–239.CrossRefGoogle ScholarPubMed
Roepstorff, A., Eriksen, L., Slotved, H.C. & Nansen, P. (1997) Experimental Ascaris suum infection in the pig: worm population kinetics following single inoculations with three doses of infective eggs. Parasitology 115, 443–452.CrossRefGoogle ScholarPubMed
Roepstorff, A., Nilsson, O., Oksanen, A., Gjerde, B., Richter, S.H., Ortenberg, E., Christensson, D., Martinsson, K.B., Bartlett, P.C., Nansen, P., Eriksen, L., Helle, O., Nikander, S. & Larsen, K. (1998) Intestinal parasites in swine in the Nordic countries: prevalence and geographical distribution. Veterinary Parasitology 76, 305–319.CrossRefGoogle ScholarPubMed
Roepstorff, A., Mejer, H., Nejsum, P. & Thamsborg, S.M. (2011) Helminth parasites in pigs: new challenges in pig production and current research highlights. Veterinary Parasitology 180, 72–81.CrossRefGoogle ScholarPubMed
Roneus, O. & Christensson, D. (1977) Mature Ascaris suum in naturally infected calves. Veterinary Parasitology 3, 371–375.CrossRefGoogle Scholar
Sauvageau, R. & Frechette, J.L. (1980) Hepatic ascariasis in a lamb. Canadian Veterinary Journal 21, 66(in French).Google ScholarPubMed
Soulsby, E.J.L. (1982) Helminths, arthropods and protozoa of domesticated animals. 7th edn. London, Baillière Tindall.Google Scholar
Spakulova, M. (1994) Discriminant-analysis as a method for the numerical evaluation of taxonomic characters in male trichurid nematodes. Systematic Parasitology 29, 113–119.Google Scholar
Sprent, J.F.A. (1952) Anatomical distinction between human and pig strains of Ascaris. Nature 170, 627–628.Google Scholar
Summers, R.W., Elliott, D.E., Urban, J.F. Jr, Thompson, R.A. & Weinstock, J.V. (2005) Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128, 825–832.Google Scholar
Takata, I. (1951) Experimental infection of man with Ascaris of man and the pig. Kitasato Archives of Experimental Medicine 23, 49–59.Google ScholarPubMed
Tilney, L.G., Connelly, P.S., Guild, G.M., Vranich, K.A. & Artis, D. (2005) Adaptation of a nematode parasite to living within the mammalian epithelium. Journal of Experimental Zoology. Part A, Comparative Experimental Biology 303, 927–945.CrossRefGoogle ScholarPubMed
Traversa, D. (2011) Are we paying too much attention to cardio-pulmonary nematodes and neglecting old-fashioned worms like Trichuris vulpis? Parasites and Vectors 4, 32.CrossRefGoogle ScholarPubMed
Van Knapen, F., Buijs, J., Kortbeek, L.M. & Ljungstrom, I. (1992) Larva migrans syndrome: Toxocara, Ascaris, or both? Lancet 340, 550–551.CrossRefGoogle ScholarPubMed
Zhou, C., Li, M., Yuan, K., Hu, N. & Peng, W. (2011) Phylogeography of Ascaris lumbricoides and A. suum from China. Parasitology Research 109, 329–338.CrossRefGoogle Scholar