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Advances in the diagnosis of Ascaris suum infections in pigs and their possible applications in humans

Published online by Cambridge University Press:  24 April 2014

JOHNNY VLAMINCK ,
BRUNO LEVECKE ,
JOZEF VERCRUYSSE  and
PETER GELDHOF
JOHNNY VLAMINCK
Affiliation:
Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
BRUNO LEVECKE
Affiliation:
Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
JOZEF VERCRUYSSE
Affiliation:
Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
PETER GELDHOF*
Affiliation:
Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
*
*Corresponding author: Department of Virology, Parasitology and Immunology, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium. E-mail: peter.geldhof@ugent.be
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Summary

Ascariasis is one of the most common parasitic diseases in both humans and pigs. It has been shown to cause growth deficits in both species and to impair cognitive development in children. Notwithstanding its substantial impact on pig economy and public health, diagnosis of ascariasis has mostly relied on the detection of eggs in stool and further development of novel, more sensitive methods has been limited or non-existent. Here, we discuss the currently available techniques for the diagnosis of ascariasis in pigs, their caveats, and the implications of a new serological detection technique for the evaluation of both pig and human ascariasis.

Keywords

Ascaris suumAscaris lumbricoidesascariasisdiagnosisserologyELISA
Type
Special Issue Article
Information
Parasitology , Volume 141 , Issue 14: Symposia of the British Society for Parasitology Volume 52 Advances in diagnostics for parasitic diseases , December 2014 , pp. 1904 - 1911
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Copyright © Cambridge University Press 2014 

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References

REFERENCES

Abebe, W., Tsuji, N., Kasuga-Aoki, H., Miyoshi, T., Isobe, T., Arakawa, T., Matsumoto, Y. and Yoshihara, S. (2002). Species-specific proteins identified in Ascaris lumbricoides and Ascaris suum using two-dimensional electrophoresis. Parasitology Research 88, 868–871.Google Scholar
Adams, V. J., Markus, M. B., Kwitshana, Z. L., Dhansay, M. A., van der Merwe, L., Walzl, G. and Fincham, J. E. (2006). Recall of intestinal helminthiasis by HIV-infected South Africans and avoidance of possible misinterpretation of egg excretion in worm/HIV co-infection analyses. BMC Infectious Diseases 6, 88.Google Scholar
Andersen, S., Jorgensen, R. J., Nansen, P. and Nielsen, K. (1973). Experimental Ascaris suum infection in piglets. Inverse relationship between the numbers of inoculated eggs and the numbers of worms established in the intestine. Acta Pathologica et Microbiologica Scandinavica Section B – Microbiology and Immunology 81, 650–656.Google Scholar
Beloeil, P. A., Chauvin, C., Fablet, C., Jolly, J. P., Eveno, E., Madec, F. and Reperant, J. M. (2003). Helminth control practices and infections in growing pigs in France. Livestock Production Science 81, 99–104.Google Scholar
Bendall, R. P., Barlow, M., Betson, M., Stothard, J. R. and Nejsum, P. (2011). Zoonotic ascariasis, United Kingdom. Emerging Infectious Diseases 17, 1964–1966.CrossRefGoogle ScholarPubMed
Bergquist, R., Johansen, M. V. and Utzinger, J. (2009). Diagnostic dilemmas in helminthology: what tools to use and when? Trends in Parasitology 25, 151–156.Google Scholar
Bernardo, T. M., Dohoo, I. R. and Donald, A. (1990 a). Effect of ascariasis and respiratory diseases on growth rates in swine. Canadian Journal of Veterinary Research 54, 278–284.Google ScholarPubMed
Bernardo, T. M., Dohoo, I. R., Donald, A., Ogilvie, T. and Cawthorn, R. (1990 b). Ascariasis, respiratory diseases and production indices in selected Prince Edward Island swine herds. Canadian Journal of Veterinary Research 54, 267–273.Google Scholar
Bernardo, T. M., Dohoo, I. R. and Ogilvie, T. (1990 c). A critical assessment of abattoir surveillance as a screening test for swine ascariasis. Canadian Journal of Veterinary Research 54, 274–277.Google Scholar
Bethony, J., Brooker, S., Albonico, M., Geiger, S. M., Loukas, A., Diemert, D. and Hotez, P. J. (2006). Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367, 1521–1532.CrossRefGoogle ScholarPubMed
Betson, M., Halstead, F. D., Nejsum, P., Imison, E., Khamis, I. S., Sousa-Figueiredo, J. C., Rollinson, D. and 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.Google Scholar
Betson, M., Nejsum, P., Llewellyn-Hughes, J., Griffin, C., Atuhaire, A., Arinaitwe, M., Adriko, M., Ruggiana, A., Turyakira, G., Kabatereine, N. B. and Stothard, J. R. (2012). Genetic diversity of Ascaris in southwestern Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 106, 75–83.CrossRefGoogle ScholarPubMed
Betson, M., Nejsum, P. and Stothard, J. R. (2013). From the twig tips to the deeper branches: new insights into evolutionary history and phylogeography of Ascaris. In Ascaris, the Neglected Parasite (ed. Holland, C.), pp. 265–286. Elsevier, Amsterdam, the Netherlands.Google Scholar
Boes, J., Nansen, P. and Stephenson, L. S. (1997). False-positive Ascaris suum egg counts in pigs. International Journal for Parasitology 27, 833–838.Google Scholar
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, 589–596.CrossRefGoogle ScholarPubMed
Bogh, H. O., Eriksen, L., Lawson, L. G. and Lind, P. (1994). Evaluation of an enzyme-linked-immunosorbent-assay and a histamine-release test system for the detection of pigs naturally infected with Ascaris suum. Preventive Veterinary Medicine 21, 201–214.Google Scholar
Booth, M., Vounatsou, P., N'Goran, E. K., Tanner, M. and Utzinger, J. (2003). The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma mansoni and hookworm co-infections in rural Cote d'Ivoire. Parasitology 127, 525–531.Google Scholar
Charlier, J., Van der Voort, M., Hogeveen, H. and Vercruysse, J. (2012). ParaCalc®: a novel tool to evaluate the economic importance of worm infections on the dairy farm. Veterinary Parasitology 184, 204–211.Google Scholar
Charlier, J., Vercruysse, J., Morgan, E., Van Dijk, J. and Williams, D. J. (2014). Recent advances in the diagnosis, impact on production and prediction of Fasciola hepatica in cattle. Parasitology 141, 326–335.Google Scholar
Cringoli, G., Rinaldi, L., Maurelli, M. P. and Utzinger, J. (2010). FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nature Protocols 5, 503–515.Google Scholar
Dangolla, A., Bjorn, H., Willeberg, P., Roepstorff, A. and Nansen, P. (1996). A questionnaire investigation on factors of importance for the development of anthelmintic resistance of nematodes in sow herds in Denmark. Veterinary Parasitology 63, 257–271.Google Scholar
Engels, D., Sinzinkayo, E. and Gryseels, B. (1996). Day-to-day egg count fluctuation in Schistosoma mansoni infection and its operational implications. American Journal for Tropical Medicine and Hygiene 54, 319–324.Google Scholar
Engels, D., Sinzinkayo, E., De Vlas, S. J. and Gryseels, B. (1997). Intraspecimen fecal egg count variation in Schistosoma mansoni infection. American Journal for Tropical Medicine and Hygiene 57, 571–577.Google Scholar
Eriksen, L. (1982). Experimentally induced resistance to Ascaris suum in pigs. Nordisk Veterinaer Medicin 34, 177–187.Google Scholar
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. Nordisk Veterinaer Medicin 32, 233–242.Google ScholarPubMed
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, 241–246.Google Scholar
Fincham, J. E., Markus, M. B., van der Merwe, L., Adams, V. J., van Stuijvenberg, M. E. and Dhansay, M. A. (2007). Ascaris, co-infection and allergy: the importance of analysis based on immunological variables rather than egg excretion. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 680–682.Google Scholar
Flesja, K. I. and Ulvesaeter, H. O. (1980). Pathological lesions in swine at slaughter. III. Inter-relationship between pathological lesions, and between pathological lesions and 1) carcass quality and 2) carcass weight. Acta Veterinaria Scandinavica Supplement, 1–22.Google Scholar
Frontera, E., Serrano, F., Reina, D., Alcaide, M., Sanchez-Lopez, J. and Navarrete, I. (2003). Serological responses to Ascaris suum adult worm antigens in Iberian finisher pigs. Journal of Helminthology 77, 167–172.Google Scholar
Glinz, D., Silue, K. D., Knopp, S., Lohourignon, L. K., Yao, K. P., Steinmann, P., Rinaldi, L., Cringoli, G., N'Goran, E. K. and Utzinger, J. (2010). Comparing diagnostic accuracy of Kato-Katz, Koga agar plate, ether-concentration, and FLOTAC for Schistosoma mansoni and soil-transmitted helminths. PLoS Neglected Tropical Diseases 4, e754.CrossRefGoogle ScholarPubMed
Hale, O. M., Stewart, T. B. and Marti, O. G. (1985). Influence of an experimental infection of Ascaris suum on performance of pigs. Journal of Animal Science 60, 220–225.Google Scholar
Hall, A. and Holland, C. (2000). Geographical variation in Ascaris lumbricoides fecundity and its implications for helminth control. Parasitology Today 16, 540–544.Google Scholar
Helwigh, A. B. and Nansen, P. (1999). Establishment of Ascaris suum in the pig: development of immunity following a single primary infection. Acta Veterinaria Scandinavica 40, 121–132.Google Scholar
Jeandron, A., Abdyldaieva, G., Usubalieva, J., Ensink, J. H., Cox, J., Matthys, B., Rinaldi, L., Cringoli, G. and Utzinger, J. (2010). Accuracy of the Kato-Katz, adhesive tape and FLOTAC techniques for helminth diagnosis among children in Kyrgyzstan. Acta Tropica 116, 185–192.Google Scholar
Jourquin, J. (2007). Strategic de-worming to boost performance. International Pig Topics 22, 7–9.Google Scholar
Jungersen, G., Eriksen, L., Nansen, P. and Fagerholm, H. P. (1997). Sex-manipulated Ascaris suum infections in pigs: implications for reproduction. Parasitology 115, 439–442.Google Scholar
Kanora, A. (2009). Effect on productivity of treating fattening pigs every 5 weeks with flubendazole in feed. Vlaams Diergeneeskundig Tijdschrift 78, 170–175.Google Scholar
Katz, N., Chaves, A. and Pellegrino, J. (1972). A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Revista do Instituto de Medicina Tropical de Sao Paulo 14, 397–400.Google Scholar
Kipper, M., Andretta, I., Monteiro, S. G., Lovatto, P. A. and Lehnen, C. R. (2011). Meta-analysis of the effects of endoparasites on pig performance. Veterinary Parasitology 181, 316–320.Google Scholar
Knecht, D., Jankowska, A. and Zalesny, G. (2012). The impact of gastrointestinal parasites infection on slaughter efficiency in pigs. Veterinary Parasitology 184, 291–297.Google Scholar
Knopp, S., Mgeni, A. F., Khamis, I. S., Steinmann, P., Stothard, J. R., Rollinson, D., Marti, H. and Utzinger, J. (2008). Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Neglected Tropical Diseases 2, e331.Google Scholar
Knopp, S., Glinz, D., Rinaldi, L., Mohammed, K. A., N'Goran, E. K., Stothard, J. R., Marti, H., Cringoli, G., Rollinson, D. and Utzinger, J. (2009). FLOTAC: a promising technique for detecting helminth eggs in human faeces. Transactions of the Royal Society for Tropical Medicine and Hygiene 103, 1190–1194.CrossRefGoogle ScholarPubMed
Kotze, A. C. and Kopp, S. R. (2008). The potential impact of density dependent fecundity on the use of the faecal egg count reduction test for detecting drug resistance in human hookworms. PLoS Neglected Tropical Diseases 2, e297.Google Scholar
Krauth, S. J., Coulibaly, J. T., Knopp, S., Traore, M., N'Goran, E. K. and Utzinger, J. (2012). An in-depth analysis of a piece of shit: distribution of Schistosoma mansoni and hookworm eggs in human stool. PLoS Neglected Tropical Diseases 6, e1969.CrossRefGoogle ScholarPubMed
Leles, D., Gardner, S. L., Reinhard, K., Iniguez, A. and Araujo, A. (2012). Are Ascaris lumbricoides and Ascaris suum a single species? Parasites and Vectors 5, 42.Google Scholar
Levecke, B., De Wilde, N., Vandenhoute, E. and Vercruysse, J. (2009). Field validity and feasibility of four techniques for the detection of Trichuris in simians: a model for monitoring drug efficacy in public health? PLoS Neglected Tropical Diseases 3, e366.Google Scholar
Lind, P., Eriksen, L., Nansen, P., Nilsson, O. and Roepstorff, A. (1993). Response to repeated inoculations with Ascaris suum eggs in pigs during the fattening period. II. Specific IgA, IgG, and IgM antibodies determined by enzyme-linked immunosorbent assay. Parasitology Research 79, 240–244.Google Scholar
Liu, G. H., Wu, C. Y., Song, H. Q., Wei, S. J., Xu, M. J., Lin, R. Q., Zhao, G. H., Huang, S. Y. and Zhu, X. Q. (2012). Comparative analyses of the complete mitochondrial genomes of Ascaris lumbricoides and Ascaris suum from humans and pigs. Gene 492, 110–116.Google Scholar
Lundenheim, N. and Holmgren, N. (2010). Prevalence of lesions found at slaughter among Swedish fattening pigs. In 21st IVPS Congress. Vancouver, Canada.Google Scholar
Maizels, R. M., Bundy, D. A., Selkirk, M. E., Smith, D. F. and Anderson, R. M. (1993). Immunological modulation and evasion by helminth parasites in human populations. Nature 365, 797–805.Google Scholar
Masure, D., Vlaminck, J., Wang, T., Chiers, K., Van den Broeck, W., Vercruysse, J. and Geldhof, P. (2013 a). A role for eosinophils in the intestinal immunity against infective Ascaris suum larvae. PLoS Neglected Tropical Diseases 7, e2138.Google Scholar
Masure, D., Wang, T., Vlaminck, J., Claerhoudt, S., Chiers, K., Van den Broeck, W., Saunders, J., Vercruysse, J. and Geldhof, P. (2013 b). The intestinal expulsion of the roundworm Ascaris suum is associated with eosinophils, intra-epithelial T cells and decreased intestinal transit time. PLoS Neglected Tropical Diseases 7, e2588.Google Scholar
McCarthy, J. S., Lustigman, S., Yang, G. J., Barakat, R. M., Garcia, H. H., Sripa, B., Willingham, A. L., Prichard, R. K. and Basanez, M. G. (2012). A research agenda for helminth diseases of humans: diagnostics for control and elimination programmes. PLoS Neglected Tropical Diseases 6, e1601.Google Scholar
Murray, C. J., Vos, T., Lozano, R., Naghavi, M., Flaxman, A. D., et al. (2012). Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380, 2197–2223.Google Scholar
Nakagawa, M., Yoshihara, S., Suda, H. and Ikeda, K. (1983). Pathological studies on white spots of the liver in fattening pigs. National Institute of Animal Health Quarterly 23, 138–149.Google Scholar
Nejsum, P., Parker, E. D. Jr., Frydenberg, J., Roepstorff, A., Boes, J., Haque, R., Astrup, I., Prag, J. and Skov Sorensen, U. B. (2005). Ascariasis is a zoonosis in Denmark. Journal of Clinical Microbiology 43, 1142–1148.Google Scholar
Nejsum, P., Roepstorff, A., Jorgensen, C. B., Fredholm, M., Goring, H. H., Anderson, T. J. and Thamsborg, S. M. (2009 a). High heritability for Ascaris and Trichuris infection levels in pigs. Heredity 102, 357–364.Google Scholar
Nejsum, P., Thamsborg, S. M., Petersen, H. H., Kringel, H., Fredholm, M. and Roepstorff, A. (2009 b). Population dynamics of Ascaris suum in trickle-infected pigs. Journal of Parasitology 95, 1048–1053.Google Scholar
Nejsum, P., Betson, M., Bendall, R. P., Thamsborg, S. M. and Stothard, J. R. (2012). Assessing the zoonotic potential of Ascaris suum and Trichuris suis: looking to the future from an analysis of the past. Journal of Helminthology 86, 148–155.Google Scholar
Neumann, E., Hall, W., Stevenson, M., Morris, R. and Ling Min Than, J. (2013). Descriptive and temporal analysis of post-mortem lesions recorded in slaughtered pigs in New Zealand from 2000 to 2010. New Zealand Veterinary Journal. [Epub ahead of print] doi: 10.1080/00480169.2013.853278.Google Scholar
NTD Partner Website (2012). Uniting to Combat Neglected Tropical Diseases. Ending the Neglect and Reaching 2020 Goals. http://www.unitingtocombatntds.org.Google Scholar
Peng, W., Yuan, K., Hu, M. and Gasser, R. B. (2007). Recent insights into the epidemiology and genetics of Ascaris in China using molecular tools. Parasitology 134, 325–330.Google Scholar
Perez, 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, 200–206.Google Scholar
Polley, L. R. and Mostert, P. E. (1980). Ascaris suum in Saskatchewan pigs: an abattoir survey of prevalence and intensity of infection. Canadian Veterinary Journal 21, 307–309.Google Scholar
Prickett, J., Simer, R., Christopher-Hennings, J., Yoon, K. J., Evans, R. B. and Zimmerman, J. J. (2008). Detection of Porcine reproductive and respiratory syndrome virus infection in porcine oral fluid samples: a longitudinal study under experimental conditions. Journal of Veterinary Diagnostic Investigation 20, 156–163.Google Scholar
Pullan, R. L., Smith, J. L., Jasrasaria, R. and Brooker, S. J. (2014). Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasites and Vectors 7, 37.Google Scholar
Roepstorff, A. (1997). Helminth surveillance as a prerequisite for anthelmintic treatment in intensive sow herds. Veterinary Parasitology 73, 139–151.Google Scholar
Roepstorff, A. (1998). Natural Ascaris suum infections in swine diagnosed by coprological and serological (ELISA) methods. Parasitological Research 84, 537–543.Google Scholar
Roepstorff, A. and Murrell, K. D. (1997). Transmission dynamics of helminth parasites of pigs on continuous pasture: Ascaris suum and Trichuris suis. International Journal for Parasitology 27, 563–572.Google Scholar
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, 443–452.Google Scholar
Sanchez-Vazquez, M. J., Nielen, M., Gunn, G. J. and Lewis, F. I. (2012). National monitoring of Ascaris suum related liver pathologies in English abattoirs: a time-series analysis, 2005–2010. Veterinary Parasitology 184, 83–87.Google Scholar
Sinniah, B. (1982). Daily egg production of Ascaris lumbricoides: the distribution of eggs in the faeces and the variability of egg counts. Parasitology 84, 167–175.Google Scholar
Speich, B., Knopp, S., Mohammed, K. A., Khamis, I. S., Rinaldi, L., Cringoli, G., Rollinson, D. and Utzinger, J. (2010). Comparative cost assessment of the Kato-Katz and FLOTAC techniques for soil-transmitted helminth diagnosis in epidemiological surveys. Parasites and Vectors 3, 71.Google Scholar
Stewart, T. B. and Hale, O. M. (1988). Losses to internal parasites in swine production. Journal of Animal Science 66, 1548–1554.Google Scholar
Stewart, T. B., Bidner, T. D., Southern, L. L. and Simmons, L. A. (1984). Efficacy of fenbendazole against migrating Ascaris suum larvae in pigs. American Journal of Veterinary Research 45, 984–986.Google Scholar
Thamsborg, S. M., Nejsum, P. and Mejer, H. (2013). Impact of Ascaris suum in livestock. In Ascaris: the Neglected Parasite (ed. Holland, C.), pp. 363–382. Elsevier, Amsterdam, the Netherlands.Google Scholar
Theodoropoulos, G., Theodoropoulou, E. and Melissaropoulou, G. (2001). Worm control practices of pig farmers in Greece. Veterinary Parasitology 97, 285–293.Google Scholar
Theodoropoulos, G., Stevens, K. B., Hartsa, A., Theodoropoulou, H. and Pfeiffer, D. U. (2009). Farm-level factors associated with above-average production on pig farms in Evia, Greece. Preventive Veterinary Medicine 89, 163–166.Google Scholar
Urban, J. F. Jr. and Romanowski, R. D. (1985). Ascaris suum: protective immunity in pigs immunized with products from eggs and larvae. Experimental Parasitology 60, 245–254.Google Scholar
Urban, J. F. Jr., Alizadeh, H. and Romanowski, R. D. (1988). Ascaris suum: development of intestinal immunity to infective second-stage larvae in swine. Experimental Parasitology 66, 66–77.Google Scholar
Van Meirhaeghe, P. and Maes, L. (1996). Effect of strategic deworming with flubendazole on the incidence of Ascarid liver lesions in fattening pigs. In IVPS Congress, Bologna, Italy.Google Scholar
Vercruysse, J., Geurden, T. and Peelaers, I. (2006). Development and Bayesian evaluation of an ELISA to detect specific antibodies to Sarcoptes scabiei var suis in the meat juice of pigs. Veterinary Record 158, 506–508.CrossRefGoogle ScholarPubMed
Vlaminck, J., Martinez-Valladares, M., Dewilde, S., Moens, L., Tilleman, K., Deforce, D., Urban, J., Claerebout, E., Vercruysse, J. and Geldhof, P. (2011). Immunizing pigs with Ascaris suum haemoglobin increases the inflammatory response in the liver but fails to induce a protective immunity. Parasite Immunology 33, 250–254.Google Scholar
Vlaminck, J., Nejsum, P., Vangroenweghe, F., Thamsborg, S. M., Vercruysse, J. and Geldhof, P. (2012). Evaluation of a serodiagnostic test using Ascaris suum haemoglobin for the detection of roundworm infections in pig populations. Veterinary Parasitology 189, 267–273.Google Scholar
Wagner, B. and Polley, L. (1997 a). Anthelmintic use on Saskatchewan pig farms: results from a postal survey. Veterinary Parasitology 73, 299–307.Google Scholar
Wagner, B. and Polley, L. (1997 b). Ascaris suum prevalence and intensity: an abattoir survey of market hogs in Saskatchewan. Veterinary Parasitology 73, 309–313.Google Scholar
Walker, M., Hall, A., Anderson, R. M. and Basanez, M. G. (2009). Density-dependent effects on the weight of female Ascaris lumbricoides infections of humans and its impact on patterns of egg production. Parasites and Vectors 2, 11.Google Scholar
Weng, Y. B., Hu, Y. J., Li, Y., Li, B. S., Lin, R. Q., Xie, D. H., Gasser, R. B. and Zhu, X. Q. (2005). Survey of intestinal parasites in pigs from intensive farms in Guangdong Province, People's Republic of China. Veterinary Parasitology 127, 333–336.Google Scholar
World Health Organization (2006). Preventive Chemotherapy in Human Helminthiasis: Coordinated Use of Anthelminthic Drugs in Control Interventions: a Manual for Health Professionals and Program Managers. World Health Organization, Geneva, Switzerland.Google Scholar
World Health Organization (2011). Helminth Control in School-Age Children: a Guide for Managers of Control Programmes, 2nd Edn. World Health Organization, Geneva, Switzerland.Google Scholar
World Health Organization (2012 a). Soil-transmitted helminthiases: number of children treated in 2010. Weekly Epidemiological Record 87, 225–232.Google Scholar
World Health Organization (2012 b). Eliminating Soil-Transmitted Helminthiases as a Public Health Problem in Children. Progress Report 2001–2010 and Strategic Plan 2011–2020. World Health Organization, Geneva, Switzerland.Google Scholar
Wilhelm, E., Hilbert, F., Paulsen, P., Smulders, F. J. M. and Rossmanith, W. (2007). Salmonella diagnosis in pig production: methodological problems in monitoring the prevalence in pigs and pork. Journal of Food Protection 70, 1246–1248.Google Scholar
Wossene, A., Tsuji, N., Kasuga-Aoki, H., Miyoshi, T., Isobe, T., Arakawa, T., Matsumoto, Y. and Yoshihara, S. (2002). Lung-stage protein profile and antigenic relationship between Ascaris lumbricoides and Ascaris suum. Journal of Parasitology 88, 826–828.Google Scholar
Ye, X. P., Donnelly, C. A., Fu, Y. L. and Wu, Z. X. (1997). The non-randomness of the distribution of Trichuris trichiura and Ascaris lumbricoides eggs in faeces and the effect of stirring faecal specimens. Tropical Medicine and International Health 2, 261–264.Google Scholar
Yoshihara, S., Oya, T., Furuya, T. and Goto, N. (1993). Use of body fluid of adult female Ascaris suum as an antigen in the enzyme-linked immunosorbent assay (ELISA) for diagnosis of swine ascariosis. Journal of Helminthology 67, 279–286.Google Scholar