First Molecular Characterization of Trichostrongylus colubriformis Infection in Rural Patients from Chile

Abstract

Purpose

The aim was to characterize the infection by Trichostrongylus spp. in patients from Chile using a combination of molecular detection techniques and phylogenetic analysis relating the findings to clinical and epidemiological reports of the patients

Methods

Strongylid eggs were detected in seven patients by coproparasitological techniques. From each sample a fragment of the ITS-2 ribosomal gene was amplified by PCR, sequenced and analyzed by the Neighbor-Joining method.

Results

All the sequences and phylogenetic clusters corresponded to T. colubriformis. Two samples presented a single nucleotide polymorphism showing two possible haplotypes. Six patients presented gastrointestinal symptoms. All of them lived on farms and used sheep manure as fertilizer.

Conclusion

T. colubriformis was the strongylid involved in the infections of these Chilean patients associated with the presence of livestock and agricultural practices that favor infection by this type of nematode.

This is a preview of subscription content, access via your institution.

Fig. 1

Source: Map data 2019, Google Earth)

Fig. 2
Fig. 3

References

  1. 1.

    Manfredi MT (2006) Biology of gastrointestinal nematodes of ruminants. Parassitologia 48:397–401

    CAS  PubMed  Google Scholar 

  2. 2.

    Zajac AM (2006) Gastrointestinal nematodes of small ruminants: life cycle, anthelmintics, and diagnosis. Vet Clin North Am Food Anim Pract 22:529–541

    Article  Google Scholar 

  3. 3.

    Ghadirian E, Arfaa A (1973) First report of human infection with Haemonchus contortus, Ostertagia ostertagi, and Marshallagia marshalli (Family Trichostrongylidae) in Iran. J Parasitol 59:1144–1145

    CAS  Article  Google Scholar 

  4. 4.

    Ashrafi K, Sharifdini M, Heidari Z, Rahmati B, Kia E (2020) Zoonotic transmission of Teladorsagia circumcincta and Trichostrongylus species in Guilan province, northern Iran: molecular and morphological characterizations. BMC Infect Dis 20:28

    CAS  Article  Google Scholar 

  5. 5.

    Lattès S, Ferté H, Delaunay P, Depaquit J, Vassallo M, Vittier M, Kokcha S, Coulibaly E, Marty P (2011) Trichostrongylus colubriformis nematode infections in humans, France. Emerg Infect Dis 17:1301–1302

    Article  Google Scholar 

  6. 6.

    Sato M, Yoonuan T, Sanguankiat S, Nuamtanong S, Pongvongsa T, Phimmayoi I, Phanhanan V, Boupha B, Moji K, Waikagul J (2011) Human Trichostrongylus colubriformis infection in a rural village in Laos. Am J Trop Med Hyg 84:52–54

    Article  Google Scholar 

  7. 7.

    Phosuk I, Intapan P, Sanpool O, Janwan P, Thanchomnang T, Sawanyawisuth K, Morakote N, Maleewong W (2013) Molecular evidence of Trichostrongylus colubriformis and Trichostrongylus axei infections in humans from Thailand and Lao PDR. Am J Trop Med Hyg 89:376–379

    Article  Google Scholar 

  8. 8.

    Souza R, Souza J, Menezes J, Alcântara L, Matos-Soares N, Teixeira M (2013) Human infection by Trichostrongylus spp. in residents of urban areas of Salvador city, Bahia. Brazil Biomédica 33:439–445

    PubMed  Google Scholar 

  9. 9.

    Watthanakulpanich D, Pongvongsa T, Sanguankiat S, Nuamtanong S, Maipanich W, Yoonuan T, Phuphisut O, Boupha B, Moji K, Sato M, Waikagul J (2013) Prevalence and clinical aspects of human Trichostrongylus colubriformis infection in Lao PDR. Acta Trop 126:37–42

    Article  Google Scholar 

  10. 10.

    Gholami S, Babamahmoodi F, Abedian R, Sharif M, Shahbazi A, Pagheh A, Fakhar M (2015) Trichostrongylus colubriformis: possible most common cause of human infection in Mazandaran Province, North of Iran. Iran J Parasitol 10:110–115

    PubMed  PubMed Central  Google Scholar 

  11. 11.

    Sharifdini M, Derakhshani S, Alizadeh S, Ghanbarzadeh L, Mirjalali H, Mobedi I, Saraei M (2017) Molecular identification and phylogenetic analysis of human Trichostrongylus species from an endemic area of Iran. Acta Trop 176:293–299

    Article  Google Scholar 

  12. 12.

    Barker I (1975) Intestinal pathology associated with Trichostrongylus colubriformis infection in sheep: histology. Parasitology 7:165–171

    Article  Google Scholar 

  13. 13.

    Gasser R, Chilton N, Hoste H, Stevenson L (1994) Species identification of trichostrongyle nematodes by PCR-RFLP. Int J Parasitol 24:291–293

    CAS  Article  Google Scholar 

  14. 14.

    Gasser R, Monti J (1997) Identification of parasitic nematodes by PCR-SSCP of ITS-2 rDNA. Mol Cell Probes 11:201–209

    CAS  Article  Google Scholar 

  15. 15.

    Mizania A, Gilld P, Daryania A, Sarvia S, Amoueia A, Katrimie A, Soleymanib E, Mirshafieef S, Gholami S, Hosseinia S, Gholami S, Rahimig M, Hashemi-Sotehh M, Sharif M (2017) A multiplex restriction enzyme-PCR for unequivocal identification and differentiation of Trichostrongylus species in human samples. Acta Trop 173:180–184

    Article  Google Scholar 

  16. 16.

    Torres P, Figueroa L, Navarrete N (1972) Trichostrongylosis en la provincia de Valdivia, Chile. Bol Chil Parasitol 27:52–55

    CAS  PubMed  Google Scholar 

  17. 17.

    Hidalgo A, Melo A, Romero F, Hidalgo V, Villanueva J, Fonseca-Salamanca F (2018) DNA extraction in Echinococcus granulosus and Taenia spp. eggs in dogs stool samples applying thermal shock. Exp Parasitol 186:10–16

    CAS  Article  Google Scholar 

  18. 18.

    Sambrook J, Fritsch E, Maniatis T (1989) Molecular Cloning. Book 3. Appendix B: Preparation of reagents and buffers used in molecular cloning. 2da ed. Cold Spring Harbor Laboratory.

  19. 19.

    Chilton N (2004) The use of nuclear ribosomal DNA markers for the identification of bursate nematodes (order Strongylida) and for the diagnosis of infections. Anim Health Res Rev 5:173–187

    CAS  Article  Google Scholar 

  20. 20.

    Ashrafi K, Tahbaz A, Sharifdini M, Mas-Coma S (2015) Familial Trichostrongylus infection misdiagnosed as acute fascioliasis. Emerg Infect Dis 21:1869–1870

    Article  Google Scholar 

  21. 21.

    Ghanbarzadeh L, Saraei M, Kia E, Amini F, Sharifdini M (2019) Clinical and haematological characteristics of human trichostrongyliasis. J Helminthol 93:149–153

    CAS  Article  Google Scholar 

  22. 22.

    Wall E, Bhatnagar N, Watson J, Doherty T (2011) An unusual case of hypereosinophilia and abdominal pain: an outbreak of Trichostrongylus imported from New Zealand. J Travel Med 18:59–60

    Article  Google Scholar 

  23. 23.

    Strauch D (1991) Survival of pathogenic micro-organisms and parasites in excreta, manure and sewage sludge. Sci Tech Rev 10:813–846

    CAS  Article  Google Scholar 

  24. 24.

    Bosco A, Rinaldi A, Maurelli M, Musella V, Coles G, Cringoli G (2014) The comparison of FLOTAC, FECPAK and McMaster techniques for nematode egg counts in cattle. Acta Parasitol 59:625–628

    Article  Google Scholar 

  25. 25.

    Charitha V, Rayulu V, Kondaiah P, Srilatha Ch (2013) Comparative evaluation of flotation techniques for the detection of soil borne parasites. J Parasit Dis 37:260–263

    Article  Google Scholar 

  26. 26.

    Savioli L, Albonico M (2004) Focus: Soil-transmitted helminthiasis. Nat Rev Microbiol 2:618–619

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Raúl Sánchez Gutiérrez (from Center of Translational Medicine Scientific and Technological Nucleus (CEMT-BIOREN), Universidad de La Frontera. Temuco, Chile) for the support granted to carry out this research

Funding

This study was supported by DIUFRO (Grant number: DI 160045) from Universidad de La Frontera, Temuco, Chile.

Author information

Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by AH, PG, AM, CO, CH and FFS. The first draft of the manuscript was written by AH and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Flery Fonseca-Salamanca.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

Approval was obtained from the ethics committee of the Universidad de La Frontera. The procedures used in this study adhere to the tenets of the Declaration of Helsinki.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hidalgo, A., Gacitúa, P., Melo, A. et al. First Molecular Characterization of Trichostrongylus colubriformis Infection in Rural Patients from Chile. Acta Parasit. 65, 790–795 (2020). https://doi.org/10.2478/s11686-020-00206-1

Download citation

Keywords

  • Trichostrongylus colubriformis
  • PCR
  • Strongylid
  • Livestock
  • Manure