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Echinococcus granulosus sensu stricto, Echinococcus ortleppi; and E. intermedius (G7) are present in Bolivia

Published online by Cambridge University Press:  01 April 2020

V. Ali ,
E. Martinez ,
P. Duran ,
M. A. Seláez ,
M. Barragan ,
P. Nogales ,
A. Peña y Lillo ,
M. Castañares ,
Y. Claros  and
P. Deplazes
...Show all authors
V. Ali
Affiliation:
Instituto de Investigación en Salud y Desarrollo (IINSAD), cátedra de Parasitología, Facultad de Medicina, Universidad Mayor de San Andrés (UMSA), La Paz, Bolivia
E. Martinez
Affiliation:
Instituto de Investigación en Salud y Desarrollo (IINSAD), cátedra de Parasitología, Facultad de Medicina, Universidad Mayor de San Andrés (UMSA), La Paz, Bolivia
P. Duran
Affiliation:
Instituto de Investigación en Salud y Desarrollo (IINSAD), cátedra de Parasitología, Facultad de Medicina, Universidad Mayor de San Andrés (UMSA), La Paz, Bolivia
M. A. Seláez
Affiliation:
Centro Municipal de Faeno, Gobierno Autónomo Municipal de La Paz, La Paz, Bolivia
M. Barragan
Affiliation:
Centro Municipal de Faeno, Gobierno Autónomo Municipal de La Paz, La Paz, Bolivia
P. Nogales
Affiliation:
Frente Acción por la Salud, La Paz, Bolivia
A. Peña y Lillo
Affiliation:
Emeritus Professor of Surgery, Facultad de Medicina, Universidad Mayor de San Andrés (UMSA), La Paz, Bolivia
M. Castañares
Affiliation:
Instituto de Gastroenterología Boliviano Japonés (IGBJ), La Paz, Bolivia
Y. Claros
Affiliation:
Facultad de Medicina, Universidad Mayor de San Andrés (UMSA), La Paz, Bolivia
P. Deplazes
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Zürich, Zurich, Switzerland
C. A. Alvarez Rojas*
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Zürich, Zurich, Switzerland
*
Author for correspondence: C. A. Alvarez Rojas, E-mail: cristan.alvarezrojas@uzh.ch
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Abstract

Cystic echinococcosis (CE) is a zoonotic disease caused by a complex of species known as Echinococcus granulosus sensu lato. CE is endemic in Argentina, Chile, Peru, Uruguay and the South part of Brazil. In contrast, little is known regarding the presence of CE in Bolivia. In this study, 35 cysts isolated from livestock (mostly from the Department of La Paz) and 3 from humans (La Paz, Oruro and Potosi) were genetically characterized analysing the sequence of the cox1 gene (1609 bp). In total, 30 cysts (from La Paz, Cochabamba and Beni) were characterized as E. granulosus sensu stricto (3 fertile and 4 non-fertile cysts from sheep, 8 fertile and 12 non-fertile cysts from cattle and 3 fertile cysts from humans). A detailed analysis of the cox1 haplotypes of E. granulosus s.s. is included. Echinococcus ortleppi (G5) was found in 5 fertile cysts from cattle (from La Paz and Cochabamba). Echinococcus intermedius (G7) was identified in 3 fertile cysts from pigs (from Santa Cruz). Additionally, E. granulosus s.s. was detected in 4 dog faecal samples, while E. ortleppi was present in other two dog faecal samples. The implications of these preliminary results in the future implementation of control measures are discussed.

Keywords

Boliviacystic echinococcosisEchinococcus granulosusmolecular epidemiologyhaplotypesgenotypes
Type
Research Article
Information
Parasitology , Volume 147 , Issue 9 , August 2020 , pp. 949 - 956
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Copyright © The Author(s) 2020. Published by Cambridge University Press

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References

Addy, F, Wassermann, M, Banda, F, Mbaya, H, Aschenborn, J, Aschenborn, O, Koskei, P, Umhang, G, De La Rue, M, Elmahdi, IE, Mackenstedt, U, Kern, P and Romig, T (2017) Genetic polymorphism and population structure of Echinococcus ortleppi. Parasitology 144, 450–458.CrossRefGoogle ScholarPubMed
Alvarez Rojas, CA, Gauci, CG and Lightowlers, MW (2013) Antigenic differences between the EG95-related proteins from Echinococcus granulosus G1 and G6 genotypes: implications for vaccination. Parasite Immunology 35, 99–102.CrossRefGoogle ScholarPubMed
Alvarez Rojas, CA, Romig, T and Lightowlers, MW (2014) Echinococcus granulosus Sensu Lato genotypes infecting humans – review of current knowledge. International Journal for Parasitology 44, 9–18.CrossRefGoogle ScholarPubMed
Alvarez Rojas, CA, Ebi, D, Gauci, CG, Scheerlinck, JP, Wassermann, M, Jenkins, DJ, Lightowlers, MW and Romig, T (2016) Microdiversity of Echinococcus granulosus Sensu Stricto in Australia. Parasitology 143, 1026–1033.CrossRefGoogle ScholarPubMed
Alvarez Rojas, CA, Ebi, D, Paredes, R, Acosta-Jamett, G, Urriola, N, Roa, JC, Manterola, C, Cortes, S, Romig, T, Scheerlinck, J-P and Lightowlers, MW (2017) High intraspecific variability of Echinococcus granulosus Sensu Stricto in Chile. Parasitology International 66, 112–115.CrossRefGoogle ScholarPubMed
Armua-Fernandez, MT, Castro, OF, Crampet, A, Bartzabal, Á, Hofmann-Lehmann, R, Grimm, F and Deplazes, P (2014) First case of peritoneal cystic echinococcosis in a domestic cat caused by Echinococcus granulosus Sensu Stricto (genotype 1) associated to feline immunodeficiency virus infection. Parasitology International 63, 300–302.10.1016/j.parint.2013.11.005CrossRefGoogle Scholar
Badaraco, JL, Ayala, FJ, Bart, JM, Gottstein, B and Haag, KL (2008) Using mitochondrial and nuclear markers to evaluate the degree of genetic cohesion among Echinococcus Populations. Experimental Parasitology 119, 453–459.CrossRefGoogle ScholarPubMed
Balbinotti, H, Santos, GB, Badaraco, J, Arend, AC, Graichen, DÂS, Haag, KL and Zaha, A (2012) Echinococcus Ortleppi (G5) and Echinococcus granulosus Sensu Stricto (G1) loads in cattle from Southern Brazil. Veterinary Parasitology 188, 255–260.CrossRefGoogle ScholarPubMed
Beteta Ortiz, M (1999) Llegada del vacuno español a Suramérica. Vol. 2019 (ed. EspaÑa, R. A. d. C. V. d.).Google Scholar
Bowles, J, Blair, D and McManus, DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.CrossRefGoogle ScholarPubMed
Cabrera, R (2007) Equinococosis quística en el Perú: necesidades de prevención y control de una enfermedad postergada. Bol Epidemiol (Lima) 16, 669.Google Scholar
Callisaya (2018) Registro de Granjas Porcinas. (ed. Tierra, M. d. D. R. y.).Google Scholar
Cardona, GA and Carmena, D (2013) A review of the global prevalence, molecular epidemiology and economics of cystic echinococcosis in production animals. Veterinary Parasitology 192, 10–32.CrossRefGoogle ScholarPubMed
Casas, N, Otero, SC, Céspedes, G, Sosa, S and Santillán, G (2013) Detección de coproantígenos para el diagnóstico de echinococosis canina en la zona fronteriza de La Quiaca-Villazón. Revista Argentina de Microbiología 45, 154–159.CrossRefGoogle Scholar
Clement, M, Posada, D and Crandall, KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.CrossRefGoogle ScholarPubMed
Corrêa, F, Stoore, C, Horlacher, P, Jiménez, M, Hidalgo, C, Alvarez Rojas, CA, Figueiredo Barros, G, Bunselmeyer Ferreira, H, Hernández, M, Cabrera, G and Paredes, R (2018) First description of Echinococcus Ortleppi and cystic echinococcosis infection status in Chile. PLOS ONE 13, e0197620.CrossRefGoogle ScholarPubMed
Craig, PS, Hegglin, D, Lightowlers, MW, Torgerson, PR and Wang, Q (2017) Chapter two – Echinococcosis: control and prevention. In Thompson, RCA, Deplazes, P and Lymbery, AJ (eds), Advances in Parasitology, vol. 96. London: Academic Press, pp. 55–158.Google Scholar
Cucher, MA, Macchiaroli, N, Baldi, G, Camicia, F, Prada, L, Maldonado, L, Avila, HG, Fox, A, Gutiérrez, A, Negro, P, López, R, Jensen, O, Rosenzvit, M and Kamenetzky, L (2016) Cystic echinococcosis in South America: systematic review of species and genotypes of Echinococcus granulosus Sensu Lato in humans and natural domestic hosts. Tropical Medicine & International Health 21, 166–175.CrossRefGoogle ScholarPubMed
de la Rue, ML, Takano, K, Brochado, JF, Costa, CV, Soares, AG, Yamano, K, Yagi, K, Katoh, Y and Takahashi, K (2011) Infection of humans and animals with Echinococcus granulosus (G1 and G3 strains) and E. ortleppi In Southern Brazil. Veterinary Parasitology 177, 97–103.CrossRefGoogle Scholar
Deplazes, P, Rinaldi, L, Alvarez Rojas, CA, Torgerson, PR, Harandi, MF, Romig, T, Antolova, D, Schurer, JM, Lahmar, S, Cringoli, G, Magambo, J, Thompson, RCA and Jenkins, EJ (2017) Chapter six – global distribution of alveolar and cystic Echinococcosis. In Thompson, RCA, Deplazes, P and Lymbery, AJ (eds), Advances in Parasitology, vol. 95. London: Academic Press, pp. 315–493.Google Scholar
Eckert, J and Deplazes, P (2004) Biological, epidemiological, and clinical aspects of Echinococcosis, a zoonosis of increasing concern. Clinical Microbiology Reviews 17, 107–135.CrossRefGoogle ScholarPubMed
Escobari de Querejazu, L (1985) Producción y comercio en el espacio sur andino en el siglo XVII: Cuzco-Potosí, 1650–1700, Embajada de España en Bolivia.Google Scholar
Espinoza, S, Salas, AM, Vargas, A, Freire, V, Diaz, E, Sánchez, G and Venegas, J (2014) Detection of the G3 genotype of Echinococcus granulosus from hydatid cysts of Chilean cattle using COX1and ND1mitochondrial markers. Parasitology Research 113, 139–147.CrossRefGoogle Scholar
Guarnera, EA, Parra, A, Kamenetzky, L, García, G and Gutiérrez, A (2004) Cystic echinococcosis in Argentina: evolution of metacestode and clinical expression in various Echinococcus granulosus strains. Acta Tropica 92, 153–159.CrossRefGoogle ScholarPubMed
Hidalgo, C, Stoore, C, Pereira, I, Paredes, R and Alvarez Rojas, CA (2019) Multiple haplotypes of Echinococcus granulosus Sensu Stricto in single naturally infected intermediate hosts. Parasitology Research 119, 763–770.CrossRefGoogle ScholarPubMed
Hüttner, M, Nakao, M, Wassermann, T, Siefert, L, Boomker, JDF, Dinkel, A, Sako, Y, Mackenstedt, U, Romig, T and Ito, A (2008) Genetic characterization and phylogenetic position of Echinococcus Felidis Ortlepp, 1937 (Cestoda: Taeniidae) from the African lion. International Journal for Parasitology 38, 861–868.CrossRefGoogle Scholar
Jarovsky, D, Brito, CRDS, Monteiro, DU, Azevedo, MID, Botton, SDA, Mimica, MJ, Arnoni, MV, Sáfadi, MAP, Berezin, EN, Salgado Filho, H, Almeida, FJ and Rue, MLDL (2020) Imported hepatopulmonary echinococcosis: first report of Echinococcus granulosus Sensu Stricto (G1) in Bolivia. Revista da Sociedade Brasileira de Medicina Tropical 53, 1–4.CrossRefGoogle Scholar
Kamenetzky, L, Canova, SG, Guarnera, EA and Rosenzvit, MC (2000) Echinococcus granulosus: DNA extraction from germinal layers allows strain determination in fertile and nonfertile hydatid cysts. Experimental Parasitology 95, 122–127.CrossRefGoogle ScholarPubMed
Kamenetzky, L, Gutierrez, AM, Canova, SG, Haag, KL, Guarnera, EA, Parra, A, García, GE and Rosenzvit, MC (2002) Several strains of Echinococcus granulosus Infect livestock and humans in Argentina. Infection, Genetics and Evolution 2, 129–136.CrossRefGoogle ScholarPubMed
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P and Drummond, A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 1647–1649.CrossRefGoogle ScholarPubMed
Konyaev, SV, Yanagida, T, Nakao, M, Ingovatova, GM, Shoykhet, YN, Bondarev, AY, Odnokurtsev, VA, Loskutova, KS, Lukmanova, GI, Dokuchaev, NE, Spiridonov, S, Alshinecky, MV, Sivkova, TN, Andreyanov, ON, Abramov, SA, Krivopalov, AV, Karpenko, SV, Lopatina, NV, Dupal, TA, Sako, Y and Ito, A (2013) Genetic diversity of Echinococcus Spp. in Russia. Parasitology 140, 1637–1647.CrossRefGoogle ScholarPubMed
Laurimäe, T, Kinkar, L, Andresiuk, V, Haag, KL, Ponce-Gordo, F, Acosta-Jamett, G, Garate, T, Gonzàlez, LM and Saarma, U (2016) Genetic diversity and phylogeography of highly zoonotic Echinococcus granulosus genotype G1 in the Americas (Argentina, Brazil, Chile and Mexico) based on 8279bp of mtDNA. Genetics and Evolution 45, 290–296CrossRefGoogle ScholarPubMed
Laurimäe, T, Kinkar, L, Romig, T, Omer, RA, Casulli, A, Umhang, G, Gasser, RB, Jabbar, A, Sharbatkhori, M, Mirhendi, H, Ponce-Gordo, F, Lazzarini, LE, Soriano, SV, Varcasia, A, Rostami Nejad, M, Andresiuk, V, Maravilla, P, González, LM, Dybicz, M, Gawor, J, Šarkūnas, M, Šnábel, V, Kuzmina, T and Saarma, U (2018) The benefits of analysing complete mitochondrial genomes: deep insights into the phylogeny and population structure of Echinococcus granulosus Sensu Lato genotypes G6 and G7. Infection. Genetics and Evolution 64, 85–94.CrossRefGoogle Scholar
Leigh, JW and Bryant, D (2015) Popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.CrossRefGoogle Scholar
Lymbery, AJ, Jenkins, EJ, Schurer, JM and Thompson, RCA (2015) Echinococcus canadensis, E. borealis, and E. intermedius. What's in a name? Trends in Parasitology 31, 23–29.CrossRefGoogle Scholar
Manterola, C, Benavente, F, Melo, A, Vial, M and Roa, JC (2008) Description of Echinococcus granulosus genotypes in human hydatidosis in a region of southern Chile. Parasitology International 57, 342–346.CrossRefGoogle Scholar
Mathis, A, Deplazes, P and Eckert, J (1996) An improved test system for PCR-based specific detection of Echinococcus multilocularis eggs. Journal of Helminthology 70, 219–222.CrossRefGoogle ScholarPubMed
MDR&T (2014) Producción pecuaria de porcinos. (ed. tierras, M. d. d. r. y.).Google Scholar
MDR&T (2017) Producción pecuaria de bovinos. (ed. Tierra, M. d. D. R. y.).Google Scholar
Monteiro, DU, Botton, SA, Tonin, AA, Azevedo, MI, Graichen, DAS, Noal, CB and de la Rue, ML (2014) Echinococcus canadensis (G7) and Echinococcus granulosus Sensu Stricto (G1) in swine of southern Brazil. Veterinary Parasitology 202, 335–338.CrossRefGoogle ScholarPubMed
Moro, P and Schantz, PM (2006) Cystic echinococcosis in the Americas. Parasitology International 55, S181–S186.CrossRefGoogle ScholarPubMed
Moro, PL, Nakao, M, Ito, A, Schantz, PM, Cavero, C and Cabrera, L (2009) Molecular identification of Echinococcus Isolates from Peru. Parasitology International 58, 184–186.CrossRefGoogle ScholarPubMed
Nakao, M, McManus, DP, Schantz, PM, Craig, PS and Ito, A (2006) A molecular phylogeny of the genus Echinococcus Inferred from complete mitochondrial genomes. Parasitology 134, 713–722.CrossRefGoogle ScholarPubMed
Nakao, M, Lavikainen, A and Hoberg, E (2015) Is Echinococcus intermedius a valid species? Trends in Parasitology 31, 342–343.CrossRefGoogle ScholarPubMed
Pavletic, CF, Larrieu, E, Guarnera, EA, Casas, N, Irabedra, P, Ferreira, C, Sayes, J, Gavidia, CM, Caldas, E, Lise, MLZ, Maxwell, M, Arezo, M, Navarro, AM, Vigilato, MAN, Cosivi, O, Espinal, M and Del Rio Vilas, VJ (2017) Cystic echinococcosis in South America: a call for action. Revista Panamericana de Salud Publica 41, 1–8.Google ScholarPubMed
Plata, W (2005) Pampa Belen comunarios, maestros y residentes defienden su tierra. La Paz: Fundación TIERRA.Google Scholar
Primo, A (1992) El ganado bovino ibérico en las Américas: 500 años después. Archivos de zootecnia, ISSN 0004–0592 41, 41.Google Scholar
Primo, AT (2004) América : conquista e colonizac¸ão : a fantástica história dos conquistadores ibéricos e seus animais na era dos descobrimentos, Movimento, Porto Alegre.Google Scholar
Ramos-Sarmiento, D and Chiluisa-Utreras, V (2020) First molecular identification of hydatid tapeworm Echinococcus granulosus Sensu Lato G6/G7 in Ecuador. Journal of Helminthology 94, e100.CrossRefGoogle Scholar
Romig, T, Ebi, D and Wassermann, M (2015) Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Veterinary Parasitology 213, 76–84.CrossRefGoogle ScholarPubMed
Romig, T, Deplazes, P, Jenkins, D, Giraudoux, P, Massolo, A, Craig, PS, Wassermann, M, Takahashi, K and de la Rue, M (2017) Chapter five – ecology and life cycle patterns of echinococcus Species. In Thompson, RCA, Deplazes, P and Lymbery, AJ (eds), Advances in Parasitology, vol. 95. London: Academic Press, pp. 213–314.Google Scholar
Rosenzvit, MC, Zhang, LH, Kamenetzky, L, Canova, SG, Guarnera, EA and McManus, DP (1999) Genetic variation and epidemiology of Echinococcus granulosus in Argentina. Parasitology 118, 523–530.CrossRefGoogle ScholarPubMed
Salud, MD (2019) Boletin integrado de vigilancia. Vol. 477.Google Scholar
Sánchez, E, Cáceres, O, Náquira, C, Garcia, D, Patiño, G, Silvia, H, Volotão, AC and Fernandes, O (2010) Molecular characterization of Echinococcus granulosus From Peru by sequencing of the mitochondrial cytochrome C oxidase subunit 1 gene. Memórias do Instituto Oswaldo Cruz 105, 806–810.CrossRefGoogle ScholarPubMed
Sánchez, E, Cáceres, O, Náquira, C, Miranda, E, Samudio, F and Fernandes, O (2012) Echinococcus granulosus genotypes circulating in alpacas (Lama pacos) and pigs (Sus scrofa) from an endemic region in Peru. Memórias do Instituto Oswaldo Cruz 107, 275–278.CrossRefGoogle ScholarPubMed
Santivañez, SJ, Gutierrez, AM, Rosenzvit, MC, Muzulin, PM, Rodriguez, ML, Vasquez, JC, Rodriguez, S, Gonzalez, AE, Gilman, RH and Garcia, HH and Cysticercosis Working Group in P (2008) Human hydatid disease in Peru is basically restricted to Echinococcus granulosus genotype G1. The American Journal of Tropical Medicine and Hygiene 79, 89–92.CrossRefGoogle ScholarPubMed
Šarkūnas, M, Vienažindienė, Ž, Alvarez Rojas, CA, Radziulis, K and Deplazes, P (2019) Praziquantel treatment of dogs for four consecutive years decreased the transmission of Echinococcus intermedius G7 to pigs in villages in Lithuania. Food and Waterborne Parasitology 15, e00043.CrossRefGoogle ScholarPubMed
Schantz, PM (1972) Hidatidosis: magnituzd del problema y perspectivas de control. Boletin de La Oficina Sanitaria Panamerica 73, 187–197.Google Scholar
Schneider, R, Gollackner, B, Schindl, M, Tucek, G and Auer, H (2010) Echinococcus canadensis G7 (pig strain): an underestimated cause of cystic echinococcosis in Austria. American Journal of Tropical Medicine and Hygiene 82, 871–874.CrossRefGoogle ScholarPubMed
Soriano, SV, Pierangeli, NB, Pianciola, L, Mazzeo, M, Lazzarini, LE, Saiz, MS, Kossman, AV, Bergagna, HFJ, Chartier, K and Basualdo, JA (2010) Molecular characterization of Echinococcus Isolates indicates goats as reservoir for Echinococcus canadensis G6 genotype in Neuquén, Patagonia Argentina. Parasitology International 59, 626–628.CrossRefGoogle ScholarPubMed
Štefanić, S, Shaikenov, BS, Deplazes, P, Dinkel, A, Torgerson, PR and Mathis, A (2004) Polymerase chain reaction for detection of patent infections of Echinococcus granulosus (“sheep strain”) in naturally infected dogs. Parasitology Research 92, 347–351.CrossRefGoogle Scholar
Thompson, RCA (2017). Chapter two – biology and systematics of Echinococcus. In Thompson, RCA, Deplazes, P and Lymbery, AJ (eds), Advances in Parasitology, vol. 95. London: Academic Press, pp. 65–109.Google Scholar
Thompson, RCA, Kumaratilake, LM and Eckert, J (1984) Observations on Echinococcus granulosus of cattle origin in Switzerland. International Journal for Parasitology 14, 283–291.CrossRefGoogle ScholarPubMed
Trachsel, D, Deplazes, P and Mathis, A (2007) Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134, 911–920.CrossRefGoogle ScholarPubMed
Villalobos Cortés, A, Martinez, A and and Delgado, JV (2009) Historia de los bovinos en Panama y su relacion con las poblaciones bovinas de Iberoamerica. Archivos de Zootecnia 58, 121.CrossRefGoogle Scholar
Villena, E (2011) Proyecto de Fortalecimiento de la Cooperación Técnica entre Uruguay y Bolivia para mejorar el control de la Hidatidosis en Bolivia. Tupiza: WHO/PAHO.Google Scholar
Yanagida, T, Mohammadzadeh, T, Kamhawi, S, Nakao, M, Sadjjadi, SM, Hijjawi, N, Abdel-Hafez, SK, Sako, Y, Okamoto, M and Ito, A (2012) Genetic polymorphisms of Echinococcus granulosus Sensu Stricto in the Middle East. Parasitology International 61, 599–603.CrossRefGoogle ScholarPubMed
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