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Molecular analysis of human- and pig-derived Ascaris in Honduras

Published online by Cambridge University Press:  05 March 2018

A. Palma ,
B. Ortiz ,
L. Mendoza ,
G. Matamoros ,
J.A. Gabrie ,
A.L. Sánchez  and
G. Fontecha
A. Palma
Affiliation:
Escuela de Microbiologı́a, Universidad Nacional Autónoma de Honduras (UNAH), Ciudad Universitaria, J1 Edificio, 4to piso, UNAH, Tegucigalpa, Honduras
B. Ortiz
Affiliation:
Escuela de Microbiologı́a, Universidad Nacional Autónoma de Honduras (UNAH), Ciudad Universitaria, J1 Edificio, 4to piso, UNAH, Tegucigalpa, Honduras
L. Mendoza
Affiliation:
Escuela de Microbiologı́a, Universidad Nacional Autónoma de Honduras (UNAH), Ciudad Universitaria, J1 Edificio, 4to piso, UNAH, Tegucigalpa, Honduras
G. Matamoros
Affiliation:
Maestrı́a en Enfermedades Infecciosas y Zoonóticas, Escuela de Microbiologı́a, Universidad Nacional Autónoma de Honduras (UNAH), Ciudad Universitaria, J1 Edificio, 4to piso, UNAH, Tegucigalpa, Honduras
J.A. Gabrie
Affiliation:
Department of Community Health Sciences, Brock University, 500 Glenridge Ave., St. Catharines, Ontario, CanadaL2S 3A1
A.L. Sánchez
Affiliation:
Department of Community Health Sciences, Brock University, 500 Glenridge Ave., St. Catharines, Ontario, CanadaL2S 3A1
G. Fontecha*
Affiliation:
Instituto de Investigación en Microbiologı́a, Escuela de Microbiologı́a, Universidad Nacional Autónoma de Honduras (UNAH), Ciudad Universitaria, J1 Edificio, 4to piso, UNAH, Tegucigalpa, Honduras
*
Author for correspondence: G. Fontecha, E-mail: [email protected]
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Abstract

Ascaris sp. is a soil-transmitted helminth (STH) significantly affecting the health of human and swine populations. Health inequities and poverty, with resulting deficiencies in water, sanitation and hygiene, are directly associated with Ascaris lumbricoides prevalence in humans. Resource constraints also lead to small-scale livestock production under unsanitary conditions. Free-ranging pigs, for instance, are exposed to a number of infectious agents, among which Ascaris suum is one of the most common. Under these conditions, close proximity between people and pigs can result in cross-contamination; that is, pigs harbouring human Ascaris and vice versa. Moreover, the potential interbreeding between these two Ascaris species has been demonstrated. The present study analysed Ascaris worms obtained from children and pigs in Honduras. Adult worms were collected from stool samples of children after pharmacological treatment, and from pigs’ intestines after slaughter for commercial purposes at a local abattoir. A nuclear ribosomal internal transcribed spacer (ITS) region was amplified by polymerase chain reaction (PCR) and digested with a restriction enzyme in order to separate putative human- and pig-derived Ascaris isolates. PCR products were also sequenced, and cladograms were constructed. All parasites isolated from children showed the typical human-derived genotype of Ascaris, whereas 91% of parasites from pigs showed the expected pig-derived genotype. Cross-infections between hosts were not demonstrated in this study. Nine per cent of pig-derived worms showed a restriction band pattern highly suggestive of a hybrid human–pig Ascaris genotype. These results contribute to the understanding of ascariasis epidemiology and its zoonotic potential in a highly endemic region.

Type
Research Paper
Information
Journal of Helminthology , Volume 93 , Issue 2 , March 2019 , pp. 154 - 158
Copyright
Copyright © Cambridge University Press 2018 

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References

Anderson, TJ (1995) Ascaris infections in humans from North America: molecular evidence for cross-infection. Parasitology 110, 215–219.Google Scholar
Anderson, TJ and Jaenike, J (1997) Host specificity, evolutionary relationships and macrogeographic differentiation among Ascaris populations from humans and pigs. Parasitology 115, 325–342.Google Scholar
Anderson, TJ, Romero-Abal, ME and Jaenike, J (1993) Genetic structure and epidemiology of Ascaris populations: patterns of host affiliation in Guatemala. Parasitology 107, 319–334.Google Scholar
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 Jornal of Infectious Diseases 63, 447–448.Google Scholar
Bendall, RP, Barlow, M, Betson, M, Stothard, JR and Nejsum, P (2011) Zoonotic ascariasis, United Kingdom. Emerging Infectious Diseases 17, 1964–1966.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. Journal of Infectious Diseases 210, 932–941.Google Scholar
Brooker, S, Clements, AC and Bundy, DA (2006) Global epidemiology, ecology and control of soil-transmitted helminth infections. Advances in Parasitology 62, 221–261.Google Scholar
Carlsgart, J, Roepstorff, A and Nejsum, P (2009) Multiplex PCR on single unembryonated Ascaris (roundworm) eggs. Parasitology Research 104, 939–943.Google Scholar
Crewe, W and Smith, DH (1971) Human infection with pig Ascaris. (A. suum). Annals of Tropical Medicine and Parasitology 65, 85.Google Scholar
Criscione, CD, Anderson, JD, Raby, K, et al. (2007a) Microsatellite markers for the human nematode parasite Ascaris lumbricoides: development and assessment of utility. Journal of Parasitology 93, 704–708.Google Scholar
Criscione, CD, Anderson, JD, Sudimack, D, Peng, W, Jha, B, Williams-Blangero, S and Anderson, TJ (2007b) Disentangling hybridization and host colonization in parasitic roundworms of humans and pigs. Proceedings. Biological Sciences 274, 2669–2677.Google Scholar
Dutto, M and Petrosillo, N (2013) Hybrid Ascaris suum/lumbricoides (Ascarididae) infestation in a pig farmer: a rare case of zoonotic ascariasis. Central European Journal of Public Health 21, 224–226.Google Scholar
Hotez, PJ, Bottazzi, ME, Franco-Paredes, C, Ault, SK and Periago, MR (2008) The neglected tropical diseases of Latin America and the Caribbean: a review of disease burden and distribution and a roadmap for control and elimination. PLoS Neglected Tropical Diseases 2, e300.Google Scholar
INE (Instituto Nacional de Estadística de Honduras) (2016) Hogares en condición de pobreza. Secondary Hogares en condición de pobreza. Available at http://www.ine.gob.hn/images/Productos%20ine/Boletines/Boletin%202017/BOLETIN%20CIFRAS%20DE%20PAIS%202010%20-%202016.pdf (accessed 4 December 2017).Google Scholar
Iniguez, AM, Leles, D, Jaeger, LH, Carvalho-Costa, FA, Araujo, A; Amazonas Research Group (2012) Genetic characterisation and molecular epidemiology of Ascaris spp. from humans and pigs in Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 106, 604–612.Google Scholar
Jungersen, G, Eriksen, L, Nielsen, CG, Roepstorff, A and Nansen, P (1996) Experimental transfer of Ascaris suum from donor pigs to helminth naive pigs. Journal of Parasitology 82, 752–756.Google Scholar
Leles, D, Araujo, A, Vicente, AC and Iniguez, AM (2010) ITS1 intra-individual variability of Ascaris isolates from Brazil. Parasitology International 59, 93–96.Google Scholar
Leles, D, Gardner, SL, Reinhard, K, Iniguez, A and Araujo, A (2012) Are Ascaris lumbricoides and Ascaris suum a single species? Parasites & Vectors 5, 42.Google Scholar
Macko, JK and Dubinsky, P (1997) Taxonomic deliberations on human and pigs ascarids. Helminthologia 34, 167–171.Google Scholar
Mejia Torres, RE, Franco Garcia, DN, Fontecha Sandoval, GA, Hernandez Santana, A, Singh, P, Mancero Bucheli, ST, Saboya, M and Paz, MY (2014) Prevalence and intensity of soil-transmitted helminthiasis, prevalence of malaria and nutritional status of school going children in Honduras. PLoS Neglected Tropical Diseases 8, e3248.Google Scholar
Miller, LA, Colby, K, Manning, SE, et al. (2015) Ascariasis in humans and pigs on small-scale farms, Maine, USA, 2010–2013. Emerging Infectious Diseases 21, 332–334.Google Scholar
Nadler, SA and Hudspeth, DS (2000) Phylogeny of the Ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: hypotheses of structural and sequence evolution. Journal of Parasitology 86, 380–393.Google Scholar
Nejsum, P, Parker, ED Jr, Frydenberg, J, Roepstorff, A, Boes, J, Haque, R, Astrup, I, Prag, J and Skov Sorensen, UB (2005) Ascariasis is a zoonosis in Denmark. Journal of Clinical Microbiology 43, 1142–1148.Google Scholar
Nejsum, P, Betson, M, Bendall, RP, Thamsborg, SM and Stothard, JR (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
Nejsum, P, Hawash, MB, Betson, M, Stothard, JR, Gasser, RB and Andersen, LO (2017) Ascaris phylogeny based on multiple whole mtDNA genomes. Infection, Genetics and Evolution 48, 4–9.Google Scholar
Peng, W and Criscione, CD (2012) Ascariasis in people and pigs: new inferences from DNA analysis of worm populations. Infections, Genetics and Evolution 12, 227–235.Google Scholar
Peng, W, Yuan, K, Zhou, X, Hu, M, Abs El-Osta, YG and Gasser, RB (2003) Molecular epidemiological investigation of Ascaris genotypes in China based on single-strand conformation polymorphism analysis of ribosomal DNA. Electrophoresis 24, 2308–2315.Google Scholar
Peng, W, Yuan, K, Hu, M, Zhou, X and Gasser, RB (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
Peng, W, Yuan, K, Hu, M and Gasser, RB (2007) Recent insights into the epidemiology and genetics of Ascaris in China using molecular tools. Parasitology 134, 325–330.Google Scholar
Sanchez, AL, Gabrie, JA, Usuanlele, MT, Rueda, MM, Canales, M and Gyorkos, TW (2013) Soil-transmitted helminth infections and nutritional status in school-age children from rural communities in Honduras. PLoS Neglected Tropical Diseases 7, e2378.Google Scholar
Sanchez, AL, Gabrie, JA, Rueda, MM, Mejia, RE, Bottazzi, ME and Canales, M (2014) A scoping review and prevalence analysis of soil-transmitted helminth infections in Honduras. PLoS Neglected Tropical Diseases 8, e2653.Google Scholar
Sanchez, AL, Gabrie, JA, Canales, M, Rueda, MM, Fontecha, GA, Mason, P, Bearmen, G and Steven, MP (2016) Soil-transmitted helminths, poverty, and malnutrition in Honduran children living in remote rural communities. Human Parasitic Diseases 8, 27–35.Google Scholar
Sarti, E, Schantz, PM, Plancarte, A, Wilson, M, Gutierrez, IO, Lopez, AS, Roberts, J and Flisser, A (1992) Prevalence and risk factors for Taenia solium taeniasis and cysticercosis in humans and pigs in a village in Morelos, Mexico. American Journal of Tropical Medicine and Hygiene 46, 677–685.Google Scholar
Shao, CC, Xu, MJ, Alasaad, S, Song, HQ, Peng, L, Tao, JP and Zhu, XQ (2014) Comparative analysis of microRNA profiles between adult Ascaris lumbricoides and Ascaris suum. BMC Veterinary Research 10, 99.Google Scholar
Soe, MJ, Kapel, CM and Nejsum, P (2016) Ascaris from humans and pigs appear to be reproductively isolated species. PLoS Neglected Tropical Diseases 10, e0004855.Google Scholar
Sparks, AM, Betson, M, Oviedo, G, Sandoval, C, Cooper, PJ and Stothard, JR (2015) Characterization of Ascaris from Ecuador and Zanzibar. Journal of Helminthology 89, 512–515.Google Scholar
Takata, I (1951) Experimental infection of man with Ascaris of man and the pig. The Kitasato Archives of Experimental Medicine 23, 151–159 (English transl., 49–59).Google Scholar
Umar, AS and Nura, A (2008) Training needs and risk assessment among farmers and animal handlers on zoonoses in Sokoto metropolis. The Nigerian Postgraduate Medical Journal 15, 168–174.Google 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.Google 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.Google Scholar