Skip to main content

Advertisement

Log in

Genetic characterization of human hydatid cysts shows coinfection by Echinococcus canadensis G7 and Echinococcus granulosus sensu stricto G1 in Argentina

  • Short Communication
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Human cystic echinococcosis caused by the larval stage of Echinococcus granulosus sensu lato (s.l.) is a highly endemic disease in the province of Neuquén, Patagonia, Argentina. Human infections with E. granulosus sensu stricto (s.s.) G1 and Echinococcus canadensis G6 were reported in Neuquén in previous studies, whereas four genotypes were identified in livestock: G1, G3, G6, and G7. The aim of this study was to identify the genotypes of E. granulosus s.l. isolates from humans of Neuquén province, Patagonia, Argentina, through the 2005–2014 period. Twenty six hydatid cysts were obtained from 21 patients. The most frequent locations were the liver and lungs. Single cysts were observed in 81.0% of patients, and combined infection of liver and lungs was detected in 9.5% of cases. Partial sequencing of mitochondrial cytochrome c oxidase subunit 1 (cox1) and NADH dehydrogenase subunit 1 (nad1) genes identified the presence of E. granulosus s.s. G1 (n = 11; 42.3%) including three different partial sequences; E. canadensis G6 (n = 14; 53.8%) and E. canadensis G7 (n = 1; 3.9%). Coinfection with G1 and G7 genotypes was detected in one patient who harbored three liver cysts. Most of the liver cysts corresponded to G1 and G6 genotypes. This study presents the first report in the Americas of a human infection with E. canadensis G7 and the second worldwide report of a coinfection with two different species and genotypes of E. granulosus s.l in humans. The molecular diversity of this parasite should be considered to redesign or improve the control program strategies in endemic regions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

References

  • Alvarez Rojas CA, Romig T, Lightowlers MW (2014) Echinococcus granulosus sensu lato genotypes infecting humans—review of current knowledge. Int J Parasitol 44:9–18

    Article  PubMed  Google Scholar 

  • Avila HG, Santos GB, Cucher MA, Macchiaroli N, Pérez MG, Baldi G, Jensen O, Pérez V, López R, Negro P, Scialfa E, Zaha A, Ferreira HB, Rosenzvit M, Kamenetzky L (2017) Implementation of new tools in molecular epidemiology studies of Echinococcus granulosus sensu lato in South America. Parasitol Int 66:250–257

    Article  CAS  PubMed  Google Scholar 

  • Beato S, Parreira R, Roque C, Gonçalves M, Silva L, Maurelli MP, Cringoli G, Grácio MA (2013) Echinococcus granulosus in Portugal: the first report of the G7 genotype in cattle. Vet Parasitol 198:235–239

    Article  PubMed  Google Scholar 

  • Bowles J, McManus DP (1993) NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. Int J Parasitol 23:969–972

    Article  CAS  PubMed  Google Scholar 

  • Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54:165–174

    Article  CAS  PubMed  Google Scholar 

  • Budke CM, Deplazes P, Torgerson PR (2006) Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis 12:296–303

    Article  PubMed  PubMed Central  Google Scholar 

  • Cucher MA, Macchiaroli N, Baldi G, Camicia F, Prada L, Maldonado L, Avila HG, Fox G, Gutiérrez A, Negro P, López R, Jensen O, Rosenzvit M, Kamenetzky L (2016) Cystic echnococcosis in South America: systematic review of species and genotypes of Echinococcus granulosus sensu lato in humans and natural domestic hosts. Tropical Med Int Health 21:166–175

    Article  Google Scholar 

  • Djuricic SM, Grebeldinger S, Kafka DI, Djan I, Vukadin M, Vasiljevic ZM (2010) Cystic echinococcosis in children—the seventeen-year experience of two large medical centers in Serbia. Parasitol Int 59:257–261

    Article  PubMed  Google Scholar 

  • Dopchiz MC, Elissondo MC, Rossin MA, Denegri G (2007) Hydatidosis cases in one of Mar del Plata hospitals, Buenos Aires, Argentina. Rev Soc Bras Med Trop 40:635–639

    Article  PubMed  Google Scholar 

  • Dybicz M, Gierczak A, Dąbrowska J, Rdzanek Ł, Michałowicz B (2013) Molecular diagnosis of cystic echinococcosis in humans from central Poland. Parasitol Int 62:364–367

    Article  CAS  PubMed  Google Scholar 

  • Eckert J, Schantz PM, Gasser RB, Torgerson PR, Bessonov AS, Movessian SO, Thakur A, Grim F, Nikogossian MA (2001) Geographic distribution and prevalence. In: Eckert J, Gemmell MA, Meslin FX, Pawlowski Z (eds) WHO/OIE manual on echinococcosis in humans and animals. WHO/OIE, Paris, pp 100–142

    Google Scholar 

  • Guarnera EA, Parra A, Kamenetzky L, García G, Gutiérrez A (2004) Cystic echinococcosis in Argentina: evolution of metacestode and clinical expression in various Echinococcus granulosus strains. Acta Trop 92:153–159

    Article  PubMed  Google Scholar 

  • Hüttner M, Nakao M, Wassermann T, Siefert L, Boomker JD, Dinkel A, Sako Y, Mackenstedt U, Romig T, Ito A (2008) Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. Int J Parasitol 38:861–868

    Article  PubMed  Google Scholar 

  • Kamenetzky L, Gutierrez AM, Canova SG, Haag KL, Guarnera EA, Parra A, Rosenzvit MC (2002) Several strains of Echinococcus granulosus infect livestock and humans in Argentina. Infect Genet Evol 2:129–136

    Article  PubMed  Google Scholar 

  • 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, Ito A (2013) Genetic diversity of Echinococcus spp. in Russia. Parasitology 140:1637–1647

    Article  PubMed  Google Scholar 

  • Kurul IC, Topcu S, Altinok T, Yazucu U, Tastepe I, Kaya S, Cetin G (2002) One-stage operation for hydatid disease of lung and liver: principles of treatment. J Thorac Cardiovasc Surg 124:1212–1215

    Article  PubMed  Google Scholar 

  • Larrieu EJ, Frider B (2001) Human cystic echinococcosis: contributions to the natural history of the disease. Am J Trop Med Parasitol 95:679–687

    Article  CAS  Google Scholar 

  • Laurimäe T, Kinkar L, Andresiuk V, Haag KL, Ponce-Gordo F, Acosta-Jamett G, Garate T, Gonzàlez LM, 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. Infect Genet Evol 45:290–296

    Article  PubMed  Google Scholar 

  • Lavikainen A, Lehtinen MJ, Meri T, Hirvelä-Koski V, Meri S (2003) Molecular genetic characterization of the Fennoscandian cervid strain, a new genotypic group (G10) of Echinococcus granulosus. Parasitology 127:207–215

    Article  CAS  PubMed  Google Scholar 

  • Monteiro DU, Botton SA, Tonin AA, Azevedo MI, Graichen DA, Noal CB, de la Rue ML (2014) Echinococcus canadensis (G7) and Echinococcus granulosus sensu stricto (G1) in swine of southern Brazil. Vet Parasitol 202:335–338

    Article  CAS  PubMed  Google Scholar 

  • Moro P, Schantz PM (2009) Echinococcosis: a review. Int J Infect Dis 13:125–133

    Article  CAS  PubMed  Google Scholar 

  • Nakao M, Lavikainen A, Yanagida T, Ito A (2013) Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae). Int J Parasitol 43:1017–1029

    Article  CAS  PubMed  Google Scholar 

  • National System of Health Surveillance (2017) http://www.msal.gob.ar/index.php/home/boletin-integrado-de-vigilancia. Accessed 15 April 2017

  • Oudni-M’rad M, M’rad S, Ksia A, Lamiri R, Mekki M, Nouri A, Mezhoud H, Babba H (2016) First molecular evidence of the simultaneous human infection with two species of Echinococcus granulosus sensu lato: Echinococcus granulosus sensu stricto and Echinococcus canadensis. Parasitol Res 115:1065–1069

    Article  PubMed  Google Scholar 

  • Pierangeli NB, Soriano SV, Roccia I, Giménez J, Lazzarini LE, Grenóvero MS, Menestrina C, Basualdo JA (2007) Heterogeneous distribution of human cystic echinococcosis after a long-term control program in Neuquén, Patagonia Argentina. Parasitol Int 56:149–155

    Article  PubMed  Google Scholar 

  • Provintial Direction of Statistic and Census (2017) Neuquén Province http://www.estadisticaneuquen.gob.ar/index.php?sec=aplicacion_neuquen_numeros. Accessed 15 April 2017

  • Romig T, Ebi D, Wassermann M (2015) Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Vet Parasitol 213:76–84

    Article  CAS  PubMed  Google Scholar 

  • Sadjjadi SM, Mikaeili F, Karamian M, Maraghi S, Sadjjadi S, Shariat-Torbaghan S, Kia EB (2013) Evidence that the Echinococcus granulosus G6 genotype has an affinity for the brain in humans. Int J Parasitol 43:875–877

    Article  CAS  PubMed  Google Scholar 

  • Schneider R, Gollackner B, Schindl M, Tucek G, Auer H (2010) Echinococcus canadensis G7 (pig strain): an underestimated cause of cystic echinococcosis in Austria. Am J Trop Med Hyg 82:871–874

    Article  PubMed  PubMed Central  Google Scholar 

  • Soriano SV, Pierangeli NB, Pianciola LA, Mazzeo M, Lazzarini LE, Saiz MS, Kossman AV, Bergagna HFJ, Chartier K, Basualdo JA (2010) Molecular characterization of Echinococcus isolates indicates goats as reservoir for Echinococcus canadensis G6 genotype in Neuquén, Patagonia Argentina. Parasitol Int 59:626–628

    Article  CAS  PubMed  Google Scholar 

  • Soriano SV, Pierangeli NB, Pianciola LA, Mazzeo M, Lazzarini LE, Debiaggi MF, Bergagna HF, Basualdo JA (2015) The optimum cut-off value to differentiate Echinococcus granulosus sensu stricto from other species of E. granulosus sensu lato using larval rostellar hook morphometry. J Helminthol 89:1–8

    Article  CAS  PubMed  Google Scholar 

  • Soriano SV, Debiaggi MF, Pierangeli NB, Pianciola LA, Bergagna HF, Lazzarini LE, Mazzeo M, Basualdo JA (2016) First study about the development of adult Echinococcus canadensis G6 genotype of goat origin in experimentally infected dogs. Vet Parasitol 228:6–12

    Article  PubMed  Google Scholar 

  • Thompson RCA, McManus DP (2001) Aetiology: parasites and life-cycles. In: Eckert J, Gemmell A, Meslin FX, Pawlowski Z (eds) WHO/OIE manual on echinococcosis in humans and animals. WHO/OIE, Paris, pp 1–16

    Google Scholar 

  • Umhang G, Richomme C, Boucher JM, Hormaz V, Boué F (2013) Prevalence survey and first molecular characterization of Echinococcus granulosus in France. Parasitol Res 112:1809–1812

    Article  CAS  PubMed  Google Scholar 

  • Umhang G, Chihai O, Boué F (2014) Molecular characterization of Echinococcus granulosus in a hyperendemic European focus, the Republic of Moldova. Parasitol Res 113:4371–4376

    Article  PubMed  Google Scholar 

  • Zait H, Kouidri M, Grenouillet FE, Umhang G, Millon L, Hamrioui B, Grenouillet F (2016) Molecular characterization of Echinococcus granulosus sensu stricto and Echinococcus canadensis in humans and livestock from Algeria. Parasitol Res 115:2423–2431

    Article  PubMed  Google Scholar 

  • Zhang T, Yang D, Zeng Z, Zhao W, Liu A, Piao D, Jiang T, Cao J, Shen Y, Liu H, Zhang W (2014) Genetic characterization of human-derived hydatid cysts of Echinococcus granulosus sensu lato in Heilongjiang Province and the first report of G7 genotype of E. canadensis in humans in China. PLoS One 9:1–7 e109059

    Google Scholar 

Download references

Acknowledgements

The authors are grateful with the surgery department of public and private hospitals of Neuquén province.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to María Florencia Debiaggi.

Ethics declarations

Funding

This study was funded by grant 04/N018 from the Secretaría de Ciencia y Técnica de la Universidad Nacional del Comahue.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This research study was approved by the Science and Technology Secretary of the National University of Comahue according to Permission No. 0991/05 Record No. 02327/05 dated on September 27, 2005. All adult subjects and parents/tutors of the children gave their written informed consent for surgery. The information of patients has been anonymised so that they cannot be identified.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Debiaggi, M.F., Soriano, S.V., Pierangeli, N.B. et al. Genetic characterization of human hydatid cysts shows coinfection by Echinococcus canadensis G7 and Echinococcus granulosus sensu stricto G1 in Argentina. Parasitol Res 116, 2599–2604 (2017). https://doi.org/10.1007/s00436-017-5555-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-017-5555-2

Keywords

Navigation