Skip to main content
SpringerLink
Log in

Effect of Soil Temperature on Canine Soil-Transmitted Nematodes in Kandy District with the First Record of Hookworm, Ancylostoma tubaeforme from Sri Lanka

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Purpose

Soil-transmitted nematodes (STNs) are widespread in tropical and subtropical regions, particularly where the communities are socio-economically challenged. We investigated the effect of soil temperature on the prevalence and intensity of STN infection in free-roaming dogs.

Methods

Fresh faecal samples collected from free-roaming dogs in Digana and Pussellawa town areas in the Kandy District, Sri Lanka, were microscopically analysed for canine STNs. Soil temperature was measured at each sampling site. Highly prevalent canine hookworm Ancylostoma, was further studied using PCR and sequencing, followed by phylogenetic analysis.

Results

The soil temperature ranged between 28 and 31 °C (mean = 29.79 °C) and 18–21 °C (mean = 19.52 °C) in Digana and Pussellawa, respectively, showing a significant difference in the two sites (Students t-test t = 1.68, p < 0.0001). Of the total 44 dogs sampled, 41 (93.2%) were positive for STNs. During microscopic analysis, five nematodes: Ancylostoma spp., Capillaria sp., Strongyloides sp., Toxocara canis, and Trichuris sp., were identified. Ancylostoma species (93.2%) were the most prevalent, followed by Strongyloides sp. (22.7%) and Toxocara canis (15.9%). Infection prevalence of Strongyloides sp. was higher in Digana (40.9%) compared to that in Pussellawa (4.5%; Chi-square test, χ2 = 8.28, p = 0.004) and also the infection intensity from Digana (EPG = 8.02 ± 20.2) compared to that from Pussellawa (0.45 ± 2.1; Mann Whitney U test, p = 0.006). Amplicons (ITS1-5.8S-ITS2) of the expected size for A. caninum, and A. tubaeforme were produced. An A. caninum sequence reported here (OQ101719) illustrated the highest similarity of 99.2% to one of the local sequences (MZ707153) upon pairwise comparison.

Conclusion

Digana, with a higher soil temperature than Pussellawa, had a significantly higher prevalence and infection intensity, particularly Strongyloides sp. This study also signifies the first molecular identification of hookworm species A. tubaeforme in Sri Lanka.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

The datasets generated during and/or analysed during the current study are available on the Open Science Framework site (link: https://osf.io/tpd9g).

References

  1. CDC (2022) Soil-Transmitted Helminths. CDC. https://www.cdc.gov/parasites/sth/index.html. Accessed 21 Aug 2023

  2. WHO (2023) Soil-Transmitted Helminth Infections. WHO. https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections. Accessed 29 Aug 2023

  3. Knopp S, Steinmann P, Keiser J, Utzinger J (2012) Nematode infections. Infect Dis Clin 26:341–358. https://doi.org/10.1016/j.idc.2012.02.006

    Article  Google Scholar 

  4. Pullan RL, Brooker SJ (2012) The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasit Vectors 5:1–14. https://doi.org/10.1186/1756-3305-5-81

    Article  Google Scholar 

  5. Brooker S, Bethony J, Hotez PJ (2004) Human hookworm infection in the 21st century. Adv Parasitol 58:197–288. https://doi.org/10.1016/S0065-308X(04)58004-1

    Article  PubMed  PubMed Central  Google Scholar 

  6. Jones KR (2021) Trichuris spp. in animals, with specific reference to neo-tropical rodents. Vet Sci 8:2–15. https://doi.org/10.3390/vetsci8020015

    Article  CAS  Google Scholar 

  7. Siyadatpanah A, Pagheh AS, Daryani A, Sarvi S, Hosseini SA, Norouzi R et al (2020) Parasitic helminth infections of dogs, wolves, foxes, and golden jackals in Mazandaran Province, North of Iran. Vet World 13:2643–2648. https://doi.org/10.14202/vetworld.2020.2643-2648

    Article  PubMed  PubMed Central  Google Scholar 

  8. Mekonnen Z, Getachew M, Bogers J, Vercruysse J, Levecke B (2019) Assessment of seasonality in soil-transmitted helminth infections across 14 schools in Jimma Town, Ethiopia. Pan Afr Med J 32:6. https://doi.org/10.11604/pamj.2019.32.6.16085

    Article  PubMed  PubMed Central  Google Scholar 

  9. Jenkins EJ, Schurer JM, Gesy KM (2011) Old problems on a new playing field: Helminth zoonoses transmitted among dogs, wildlife, and people in a changing northern climate. Vet Parasitol 182:54–69. https://doi.org/10.1016/j.vetpar.2011.07.015

    Article  PubMed  Google Scholar 

  10. Mas-Coma S, Valero MA, Bargues MD (2008) Effects of climate change on animal and zoonotic helminthiases. OIE Rev Sci Tech 27:443–57. https://doi.org/10.20506/RST.27.2.1822

    Article  CAS  Google Scholar 

  11. Paquet-Durand I, Hernández J, Dolz G, Zuñiga JJR, Schnieder T, Epe C (2007) Prevalence of Toxocara spp., Toxascaris leonina and ancylostomidae in public parks and beaches in different climate zones of Costa Rica. Acta Trop 104:30–37. https://doi.org/10.1016/j.actatropica.2007.06.011

    Article  PubMed  Google Scholar 

  12. Panigrahi PN, Gupta AR, Behera SK, Panda BSK, Patra RC, Mohanty BN et al (2014) Evaluation of gastrointestinal helminths in canine population of Bhubaneswar, Odisha, India: a public health appraisal. Vet World 7:295–8. https://doi.org/10.14202/vetworld.2014.295-298

    Article  Google Scholar 

  13. Drake J, Carey T (2019) Seasonality and changing prevalence of common canine gastrointestinal nematodes in the USA. Parasit Vectors 12:1–7. https://doi.org/10.1186/s13071-019-3701-7

    Article  Google Scholar 

  14. Amarasekera M, Gunawardena NK, de Silva NR, Douglass JA, O’Hehir RE, Weerasinghe A (2012) Impact of helminth infection on childhood allergic diseases in an area in transition from high to low infection burden. Asia Pac Allergy 2:122–128. https://doi.org/10.5415/apallergy.2012.2.2.122

    Article  PubMed  PubMed Central  Google Scholar 

  15. Jenkins TP, Rathnayaka Y, Perera PK, Peachey LE, Nolan MJ, Krause L et al (2017) Infections by human gastrointestinal helminths are associated with changes in faecal microbiota diversity and composition. PLoS One 12:e0184719. https://doi.org/10.1371/journal.pone.0184719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Perera PK, Rajapakse RPVJ, Rajakaruna RS (2013) Gastrointestinal parasites of dogs in Hantana area in the Kandy District. J Natl Sci Found Sri Lanka 41:81–91. https://doi.org/10.4038/jnsfsr.v41i2.5703

    Article  Google Scholar 

  17. De Silva TK, Rajakaruna RS, Mohotti KM, Rajapakse RPVJ, Perera PK (2022) First molecular identification of Ancylostoma species in dogs in a rural tea estate community in Sri Lanka and the detection of other zoonotic gastro-intestinal parasites. Acta Parasitol 67:1086–1096. https://doi.org/10.1007/s11686-022-00531-7

    Article  CAS  PubMed  Google Scholar 

  18. Bandaranayaka KO, Rajapakse RPVJ, Rajakaruna RS (2019) Potentially zoonotic gastrointestinal parasites of dogs in Lunugala Tea estate community in Central Sri Lanka. Ceylon J Sci 48:43–50. https://doi.org/10.4038/cjs.v48i1.7587

    Article  Google Scholar 

  19. Gunawardena K, Kumarendran B, Ebenezer R, Gunasingha MS, Pathmeswaran A, de Silva N (2011) Soil-transmitted helminth infections among plantation sector schoolchildren in Sri Lanka: prevalence after ten years of preventive chemotherapy. PLoS Negl Trop Dis 5:e1341. https://doi.org/10.1371/journal.pntd.0001341

    Article  PubMed  PubMed Central  Google Scholar 

  20. Taylor MA, Coop RL, Wall RL (2016) Veterinary Parasitology. Blackwell, London

  21. Fu Y, Huang Y, Abuzeid AMI, Hang J, Yan X, Wang M et al (2019) Prevalence and potential zoonotic risk of hookworms from stray dogs and cats in Guangdong. China Vet Parasitol Reg Stud Reports 17:100316. https://doi.org/10.1016/j.vprsr.2019.100316

    Article  PubMed  Google Scholar 

  22. Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA, McWilliam H et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404

    Article  CAS  PubMed  Google Scholar 

  23. Swofford DL (1993) PAUP: phylogenetic analysis using parsimony Version 3.1. CIPRES cyberinfrastructure for phylogenetic research. https://www.phylo.org/tools/obsolete/Paup_Doc_31.pdf. Accessed 7 Aug 2023

  24. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Sepalage CS, Perera PK, Rajakaruna RS (2020) Helminthiasis in dogs of University of Peradeniya premises: a potential public health problem. Ceylon J Sci 49:29–36. https://doi.org/10.4038/cjs.v49i1.7703

    Article  Google Scholar 

  26. Gilles HM (1985) Selective primary health care: strategies for control of disease in the developing world. XVII. Hookworm infection and anemia. Rev Infect Dis 7:111–118. https://doi.org/10.1093/clinids/7.1.111

    Article  CAS  PubMed  Google Scholar 

  27. Okulewicz A (2017) The impact of global climate change on the spread of parasitic nematodes. Ann Parasitol 63:15–20. https://doi.org/10.17420/ap6301.79

    Article  PubMed  Google Scholar 

  28. Blum AJ, Hotez PJ (2018) Global “worming”: climate change and its projected general impact on human helminth infections. PLoS Negl Trop Dis 12:e0006370. https://doi.org/10.1371/journal.pntd.0006370

    Article  PubMed  PubMed Central  Google Scholar 

  29. Page W, Judd JA, Bradbury RS (2018) The unique life cycle of Strongyloides stercoralis and implications for public health action. Trop Med Infect Dis 3:53. https://doi.org/10.3390/tropicalmed3020053

    Article  PubMed  PubMed Central  Google Scholar 

  30. Preisser W (2019) Latitudinal gradients of parasite richness: a review and new insights from helminths of cricetid rodents. Ecography 42:1315–1330. https://doi.org/10.1111/ecog.04254

    Article  Google Scholar 

  31. Dobzhansky T (1950) Evolution in the tropics. Am Sci 38:209–221

    Google Scholar 

  32. Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227. https://doi.org/10.1038/35012228

    Article  CAS  PubMed  Google Scholar 

  33. Willig MR, Kaufman DM, Stevens RD (2003) Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annu Rev Ecol Evol Syst 34:273–309. https://doi.org/10.1146/annurev.ecolsys.34.012103.144032

    Article  Google Scholar 

  34. Amarasena PGDS, Mohotti KM, De Costa DM (2016) Effects of changing rainfall and soil temperature on population density of Pratylenchus loosi in tea lands at different elevations. Trop Agric Res 27:265–276. https://doi.org/10.4038/tar.v27i3.8205

    Article  Google Scholar 

  35. Traversa D, Frangipane Di Regalbono A, Di Cesare A, La Torre F, Drake J, Pietrobelli M (2014) Environmental contamination by canine geohelminths. Parasit Vectors 7:67. https://doi.org/10.1186/1756-3305-7-67

    Article  PubMed  PubMed Central  Google Scholar 

  36. Traversa D (2012) Pet roundworms and hookworms: a continuing need for global worming. Parasit Vectors 5:1–19. https://doi.org/10.1186/1756-3305-5-91

    Article  Google Scholar 

  37. Dissanaike AS, Ihalamulla RL, De SD, Pathirana S, Weerakoon U, Amaratunga MS et al (2000) On a dead female hookworm, probably Ancylostoma tubaeforme, from the vitreous of a patient in Sri Lanka. Ceylon J Med Sci 43:25–30. https://doi.org/10.4038/cjms.v43i2.4871

    Article  Google Scholar 

  38. Mahdy MAK, Lim YAL, Ngui R, Fatimah MS, Choy SH, Yap NJ et al (2012) Prevalence and zoonotic potential of canine hookworms in Malaysia. Parasit Vectors 5:1–7. https://doi.org/10.1186/1756-3305-5-88

    Article  Google Scholar 

  39. Inpankaew T, Schär F, Dalsgaard A, Khieu V, Chimnoi W, Chhoun C et al (2014) High prevalence of Ancylostoma ceylanicum hookworm infections in humans, Cambodia, 2012. Emerg Infect Dis 20:976–982. https://doi.org/10.3201/eid2006.131770

    Article  PubMed  PubMed Central  Google Scholar 

  40. Traub RJ (2013) Ancylostoma ceylanicum, a re-emerging but neglected parasitic zoonosis. Int J Parasitol 43:1009–1015. https://doi.org/10.1016/j.ijpara.2013.07.006

    Article  PubMed  Google Scholar 

  41. Shi XL, Fu YQ, Abdullahi AY, Wang MW, Yang F, Yu XG et al (2018) The mitochondrial genome of Ancylostoma tubaeforme from cats in China. J Helminthol 92:22–33. https://doi.org/10.1017/S0022149X17000116

    Article  CAS  PubMed  Google Scholar 

  42. Lucio-Forster A, Liotta JL, Yaros JP, Briggs KR, Mohammed HO, Bowman DD (2012) Morphological differentiation of eggs of Ancylostoma caninum, Ancylostoma tubaeforme, and Ancylostoma braziliense from dogs and cats in the United States. J Parasitol 98:1041–1044. https://doi.org/10.1645/GE-2928.1

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the technical staff of the Department of Zoology and the Department of Veterinary Pathobiology of University of Peradeniya for providing immense support in laboratory work. This work was supported by the University of Peradeniya Research Grants (Grant No: URG/2022/64/S).

Funding

This work was funded by the University of Peradeniya Research Grants (Grant no: URG/2022/64/S) Piyumali K. Perera.

Author information

Authors and Affiliations

  1. Department of Zoology, Faculty of Science, University of Peradeniya, Peradeniya, Sri Lanka

    Sakunika Amarasingha, Rupika S. Rajakaruna & Piyumali K. Perera

  2. Department of Veterinary Pathobiology, Faculty of Veterinary Medicine and Animal Science, University of Peradeniya, Peradeniya, Sri Lanka

    N. M. T. Anupama & R. P. V. J. Rajapakse

Authors
  1. Sakunika Amarasingha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. M. T. Anupama
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rupika S. Rajakaruna
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. P. V. J. Rajapakse
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Piyumali K. Perera
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by [Sakunika Amarasingha] and [Piyumali K. Perera]. The first draft of the manuscript was written by [Sakunika Amarasingha] and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Piyumali K. Perera.

Ethics declarations

Conflict of interest

All authors declare no conflict of interest.

Ethical Approval

Ethical clearance for the study was obtained from the Ethical Clearance Committee of Postgraduate Institute of Science, University of Peradeniya, Sri Lanka (Reference no: CEC_PGIS_2022_04).

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amarasingha, S., Anupama, N.M.T., Rajakaruna, R.S. et al. Effect of Soil Temperature on Canine Soil-Transmitted Nematodes in Kandy District with the First Record of Hookworm, Ancylostoma tubaeforme from Sri Lanka. Acta Parasit. (2024). https://doi.org/10.1007/s11686-024-00829-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11686-024-00829-8

Keywords

Search

Navigation