Advertisement

Parasitology Research

, Volume 117, Issue 11, pp 3507–3517 | Cite as

MaxEnt modeling of soil-transmitted helminth infection distributions in Thailand

  • J. Chaiyos
  • K. Suwannatrai
  • K. Thinkhamrop
  • K. Pratumchart
  • C. Sereewong
  • S. Tesana
  • S. Kaewkes
  • B. Sripa
  • T. Wongsaroj
  • A. T. Suwannatrai
Original Paper

Abstract

Infections due to soil-transmitted helminths (STHs), i.e. Ascaris lumbricoides, Trichuris trichiura, hookworms, and Strongyloides stercoralis, are widely distributed in tropical and subtropical areas in which approximately 1.5 billion people are infected. A clear understanding of the epidemiology and distribution of diseases is an important aid for control and prevention. The aim of our study was to identify the effects of environmental and climatic factors on distribution patterns of STHs and to develop a risk map for STH infections under current environmental and climate regimes in Thailand. Geographical information systems (GIS), remote sensing, and Maximum Entropy (MaxEnt) algorithm software were used to determine the significant factors and to create predictive risk maps for STH infections in Thailand. The disease data from Thailand covered the years from 1969 to 2014, while environmental and climatic data were compiled from the Worldclim database, MODIS satellite imagery, Soilgrids and ISCGM. The models predicted that STHs occur mainly in southern Thailand. Mean annual precipitation was the factor most affecting the current distribution of A. lumbricoides, T. trichiura, and S. stercoralis. Land cover class was the main predictor for distribution of S. stercoralis and important for hookworms. Altitude was the dominant factor affecting the distribution of hookworms, and mean temperature of the wettest quarter was significantly associated with A. lumbricoides distribution. A predicted distribution map of STHs to identify environmental risk factors in Thailand is presented. This work provides a model for use in STH monitoring and health planning not only in Thailand but also in other countries with similar disease conditions.

Keywords

Soil-transmitted helminths Geographic information system Remote sensing Ecological niche modeling Thailand 

Notes

Acknowledgments

We would like to acknowledge Prof. David Blair for editing the MS via Publication Clinic KKU, Thailand.

Funding

This research was supported by Thailand Research Fund (grant number TRG5790198) and Khon Kaen University New Researcher Development Grant.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

References

  1. Anamnart W, Pattanawongsa A, Intapan PM, Morakote N, Janwan P, Maleewong W (2013) Detrimental effect of water submersion of stools on development of Strongyloides stercoralis. PLoS One 8(12):e82339.  https://doi.org/10.1371/journal.pone.0082339 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Appleton CC, Gouws E (1996) The distribution of common intestinal nematodes along an altitudinal transect in KwaZulu-Natal, South Africa. Ann Trop Med Parasitol 90(2):181–188CrossRefGoogle Scholar
  3. Appleton CC, Maurihungirire M, Gouws E (1999) The distribution of helminth infections along the coastal plain of Kwazulu-Natal Province, South Africa. Ann Trop Med Parasitol 93(8):859–868CrossRefGoogle Scholar
  4. Beer RJ (1976) The relationship between Trichuris trichiura (Linnaeus 1758) of man and Trichuris suis (Schrank 1788) of the pig. Res Vet Sci 20:47–54PubMedGoogle Scholar
  5. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367(9521):1521–1532.  https://doi.org/10.1016/S0140-6736(06)68653-4 CrossRefPubMedGoogle Scholar
  6. Brooker S, Michael E (2000) The potential of geographical information systems and remote sensing in the epidemiology and control of human helminth infections. Adv Parasitol 47:245–288CrossRefGoogle Scholar
  7. Brooker S, Singhasivanon P, Waikagul J, Supavej S, Kojima S, Takeuchi T, Luong TV, Looareesuwan S (2003) Mapping soil-transmitted helminths in Southeast Asia and implications for parasite control. Southeast Asian J Trop Med Public Health 34(1):24–36PubMedGoogle Scholar
  8. Brown HW (1927) Studies on the rate of development and viability of the eggs of Ascaris lumbricoides and Trichuris trichiura under field conditions. J Parasitol 14(1):1–15CrossRefGoogle Scholar
  9. Chammartin F, Scholte RG, Guimaraes LH, Tanner M, Utzinger J, Vounatsou P (2013a) Soil-transmitted helminth infection in South America: a systematic review and geostatistical meta-analysis. Lancet Infect Dis 13(6):507–518.  https://doi.org/10.1016/S1473-3099(13)70071-9 CrossRefPubMedGoogle Scholar
  10. Chammartin F, Scholte RG, Malone JB, Bavia ME, Nieto P, Utzinger J, Vounatsou P (2013b) Modelling the geographical distribution of soil-transmitted helminth infections in Bolivia. Parasit Vectors 6:152.  https://doi.org/10.1186/1756-3305-6-152 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chandler AC (1929) Hookworm disease: its distribution, biology, epidemiology, pathology, diagnosis, treatment and control, 1st edn. The Macmillan Company, New YorkGoogle Scholar
  12. Clements AC, Lwambo NJ, Blair L, Nyandindi U, Kaatano G, Kinung'hi S, Webster JP, Fenwick A, Brooker S (2006) Bayesian spatial analysis and disease mapping: tools to enhance planning and implementation of a schistosomiasis control programme in Tanzania. Tropical Med Int Health 11(4):490–503.  https://doi.org/10.1111/j.1365-3156.2006.01594.x CrossRefGoogle Scholar
  13. Collender PA, Kirby AE, Addiss DG, Freeman MC, Remais JV (2015) Methods for quantification of soil-transmitted helminths in environmental media: current techniques and recent advances. Trends Parasitol 31(12):625–639.  https://doi.org/10.1016/j.pt.2015.08.007 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Croker C, Reporter R, Redelings M, Mascola L (2010) Strongyloidiasis-related deaths in the United States, 1991–2006. Am J Trop Med Hyg 83(2):422–426.  https://doi.org/10.4269/ajtmh.2010.09-0750 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Elith J, Graham CH, Anderson RP, Dudík M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz C, Nakamura M, Nakazawa Y, Overton JM, Peterson AT, Phillips SJ, Richardson KS, Scachetti-Pereira R, Schapire RE, Soberón J, Williams S, Wisz MS, Zimmermann NE (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151CrossRefGoogle Scholar
  16. Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8:993–1009CrossRefGoogle Scholar
  17. Gunawardena GS, Karunaweera ND, Ismail MM (2004) Wet-days: are they better indicators of Ascaris infection levels? J Helminthol 78:305–310CrossRefGoogle Scholar
  18. 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(9):e1341.  https://doi.org/10.1371/journal.pntd.0001341 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hay SI (2000) An overview of remote sensing and geodesy for epidemiology and public health application. Adv Parasitol 47:1–35CrossRefGoogle Scholar
  20. Hernandez PA, Graham CH, Master LL, Albert DL (2006) The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography 29(5):773–785CrossRefGoogle Scholar
  21. Khieu V, Schar F, Forrer A, Hattendorf J, Marti H, Duong S, Vounatsou P, Muth S, Odermatt P (2014) High prevalence and spatial distribution of Strongyloides stercoralis in rural Cambodia. PLoS Negl Trop Dis 8(6):e2854.  https://doi.org/10.1371/journal.pntd.0002854 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Lai D, Bartholomew PH (1996) Soil-transmitted helminthiases in China: a spatial statistical analysis. Southeast Asian J. Trop. Med. Public Health 27(4):754–759PubMedGoogle Scholar
  23. Mabaso ML, Appleton CC, Hughes JC, Gouws E (2003) The effect of soil type and climate on hookworm (Necator americanus) distribution in KwaZulu-Natal, South Africa. Tropical Med Int Health 8(8):722–727CrossRefGoogle Scholar
  24. Malavade SS (2015) Assessment of soil transmitted helminth infection (STHI) in school children, risk factors, interactions and environmental control in El Salvador. University of South Florida, TampaGoogle Scholar
  25. Nithikathkul C, Trevanich A, Wongsaroj T, Wongsawad C, Reungsang P (2017) Health informatics model for helminthiasis in Thailand. J Helminthol 91(5):528–533.  https://doi.org/10.1017/S0022149X16000614 CrossRefPubMedGoogle Scholar
  26. Phillips SJ, Dudík M (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31(2):161–175CrossRefGoogle Scholar
  27. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259CrossRefGoogle Scholar
  28. Raso G, Vounatsou P, Gosoniu L, Tanner M, N'Goran EK, Utzinger J (2006) Risk factors and spatial patterns of hookworm infection among schoolchildren in a rural area of western Cote d’Ivoire. Int J Parasitol 36(2):201–210.  https://doi.org/10.1016/j.ijpara.2005.09.003 CrossRefPubMedGoogle Scholar
  29. Schule SA, Clowes P, Kroidl I, Kowuor DO, Nsojo A, Mangu C, Riess H, Geldmacher C, Laubender RP, Mhina S, Maboko L, Loscher T, Hoelscher M, Saathoff E (2014) Ascaris lumbricoides infection and its relation to environmental factors in the Mbeya region of Tanzania, a cross-sectional, population-based study. PLoS One 9(3):e92032.  https://doi.org/10.1371/journal.pone.0092032 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Seamster AP (1950) Developmental studies concenring the eggs of Ascaris lumbricoides var. suum. Am Midl Nat 43:450–468CrossRefGoogle Scholar
  31. Segarra-Newnham M (2007) Manifestations, diagnosis, and treatment of Strongyloides stercoralis infection. Ann Pharmacother 41(12):1992–2001.  https://doi.org/10.1345/aph.1K302 CrossRefPubMedGoogle Scholar
  32. Spindler LA (1929) The relation of moisture to the distribution of human trichuris and ascaris. Am J Epidemiol 10(2):476–496CrossRefGoogle Scholar
  33. Stephenson LS, Latham MC, Ottesen EA (2000) Malnutrition and parasitic helminth infections. Parasitology 121(Suppl):S23–S38CrossRefGoogle Scholar
  34. Stoltzfus RJ, Dreyfuss ML, Chwaya HM, Albonico M (1997) Hookworm control as a strategy to prevent iron deficiency. Nutr Rev 55(6):223–232CrossRefGoogle Scholar
  35. Suwannatrai A, Pratumchart K, Suwannatrai K, Thinkhamrop K, Chaiyos J, Kim CS, Suwanweerakamtorn R, Boonmars T, Wongsaroj T, Sripa B (2017) Modeling impacts of climate change on the potential distribution of the carcinogenic liver fluke, Opisthorchis viverrini, in Thailand. Parasitol Res 116(1):243–250.  https://doi.org/10.1007/s00436-016-5285-x CrossRefPubMedGoogle Scholar
  36. Weaver HJ, Hawdon JM, Hoberg EP (2010) Soil-transmitted helminthiases: implications of climate change and human behavior. Trends Parasitol 26(12):574–581.  https://doi.org/10.1016/j.pt.2010.06.009 CrossRefPubMedGoogle Scholar
  37. Wongsaroj T, Nithikathkulb C, Rojkitikulc W, Nakaia W, Royalb L, Rammasutc P (2014) National survey of helminthiasis in Thailand. Asian Biomed 8(6):779–783CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • J. Chaiyos
    • 1
  • K. Suwannatrai
    • 2
  • K. Thinkhamrop
    • 3
  • K. Pratumchart
    • 1
  • C. Sereewong
    • 1
  • S. Tesana
    • 1
  • S. Kaewkes
    • 1
  • B. Sripa
    • 4
    • 5
  • T. Wongsaroj
    • 6
  • A. T. Suwannatrai
    • 1
  1. 1.Department of Parasitology, Faculty of MedicineKhon Kaen UniversityKhon KaenThailand
  2. 2.Department of Biology, Faculty of Science and TechnologySakon Nakhon Rajabhat UniversitySakon NakhonThailand
  3. 3.Data Management and Statistical Analysis Center, Faculty of Public HealthKhon Kaen UniversityKhon KaenThailand
  4. 4.WHO Collaborating Centre for Research and Control of Opisthorchiasis, Tropical Disease Research LaboratoryKhon KaenThailand
  5. 5.Department of Pathology, Faculty of MedicineKhon Kaen UniversityKhon KaenThailand
  6. 6.Department of Disease Control, Bureau of General Communicable DiseasesMinistry of Public HealthNonthaburiThailand

Personalised recommendations