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The roundworm Strongyloides stercoralis in children, dogs, and soil inside and outside a segregated settlement in Eastern Slovakia: frequent but hardly detectable parasite

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Abstract

A comparative study was carried out to evaluate the Strongyloides stercoralis infections in children and dogs inside and outside the segregated settlement in Medzev, Eastern Slovakia, and a survey of the soil within the settlement was included. Applying the Koga agar plate (KAP) culture method and microscopy examination of stool samples collected from 60 Roma and 21 nonRoma children, no larvae of S. stercoralis were detected but eggs of three nematodes (Ascaris lumbricoides, Trichuris trichiura, and Enterobius vermicularis) and cysts of two protozoan endoparasites (Giardia duodenalis and Cryptosporidium spp.) were often found. However, immunoenzymatic assay (ELISA) for the evidence of IgG antibodies against S. stercoralis showed 33.3% seroprevalence in Roma children and 23.8% prevalence in children from the majority population, attending the same school. Eosinophilia was regularly present in children with exclusive infection of S. stercoralis (eight cases) as well as in individuals suffering from mixed infections of S. stercoralis and some of the above listed parasites (16 cases); high eosinophil counts sometimes, but not always, occurred in parasitized children lacking S. stercoralis antibodies. A comparison of S. stercoralis in dogs from the settlement (40 dogs) and from a distant dog shelter (20 dogs) did not reveal remarkable differences: the direct microscopy of faecal samples revealed rhabditiform larvae in 13.3% of the dogs from the settlement (4/30) and in 10.0% of the dogs from the shelter (2/20). Out of blood samples collected from the second dog group, 55% of the dogs contained antibodies against S. stercoralis. In the soil collected from 14 various locations within the settlement, S. stercoralis larvae were observed in two samples (14.3%); however, 13 samples (92.9%) were positive for human or dog endoparasites of the genera Ancylostoma, Ascaris, Toxocara, Toxascaris, Trichuris, and Hymenolepis.

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References

  • Acha PN, Szyfres B (2003) Zoonoses and communicable disease common to man and animal. Volume III. Parasitoses. Scientific and Technical Publication No. 580. Washington, pp 395

  • Agrawal V, Agrawal T, Ghoshal UC (2009) Intestinal strongyloidiasis: a diagnosis frequently missed in the tropics. Trans R Soc Trop Med Hyg 103:242–246. doi:10.1016/j.trstmh.2008.08.009

    Article  PubMed  Google Scholar 

  • Ashton FT, Bhopale VM, Holt D, Smith G, Schad GA (1998) Developmental switching in the parasitic nematode Strongyloides stercoralis is controlled by the ASF and ASI amphidial neurons. J Parasitol 84:691–695

    Article  CAS  PubMed  Google Scholar 

  • Basile A, Simzar S, Bentow J, Antelo F, Shitabata P et al (2010) Disseminated Strongyloides stercoralis: hyperinfection during medical immunosuppression. J Am Acad Dermatol 63:896–902. doi:10.1016/j.jaad.2009.09.037

    Article  PubMed  Google Scholar 

  • 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. doi:10.1016/S0140-6736(06)68653-4

    Article  PubMed  Google Scholar 

  • Brooker S, Clements ACA, Bundy DAP (2006) Global epidemiology, ecology and control of soil-transmitted helminth infections. Adv Parasitol 62:221–261. doi:10.1016/S0065-308X(05)62007-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Concha R, Harrington W Jr, Rogers AI (2005) Intestinal strongyloidiasis: recognition, management, and determinants of outcome. J Clin Gastroenterol 39:203–211. doi:10.1097/01.mcg.0000152779.68900.33

    Article  PubMed  Google Scholar 

  • Dillard KJ, Saari SAM, Anttila M (2007) Strongyloides stercoralis infection in a Finnish kennel. Acta Vet Scand 49:37. doi:10.1186/1751-0147-49-37

    Article  PubMed  PubMed Central  Google Scholar 

  • Dziuban M (1928) Contribution to the problem of the intestinal parasites in Subcarpathian Ruthenia. Čas lék čes 67(42):1432–1434

    Google Scholar 

  • Dziuban M (1962) Some observations and findings regarding strongyloidosis in Slovakia. Čs epidemiol 11(2):139–144

    CAS  Google Scholar 

  • Garcia LS (2016) Intestinal nematodes. In: Garcia LS (ed) Diagnostic medical parasitology 6th edn. ASM Press, Washington DC, pp 299–335

  • Garcia LS, Bruckner DA (1997) Collection, preservation, and shipment of fecal specimens. In: Garcia LS, Bruckner DA (ed) Diagnostic medical parasitology, 3rd edn. ASM Press, Washington DC, pp 593–607

  • Genta RM (1989) Global prevalence of strongyloidosis: critical review with epidemiologic insights into the prevention of disseminated disease. Rev Infect Dis 11:755–767

    Article  CAS  PubMed  Google Scholar 

  • Giboda M, Maloveská M (1982) Strongyloidosis in Eastern Slovakia. Bratisl lek listy 77(2):197–201

    CAS  PubMed  Google Scholar 

  • Goncalves AL, Machado GA, Goncalves-Pires MR, Ferreira-Júnior A, Silva DA, Costa-Cruz JM (2007) Evaluation of strongyloidosis in kennel dogs and keepers by parasitological and serological assays. Vet Parasitol 147(1–2):132–139. doi:10.1016/j.vetpar.2007.03.016

    Article  CAS  PubMed  Google Scholar 

  • Grzybek A, Spausta G, Ciarkowska J, Twrdowska-Saucha K (1998) Infection with gastrointestinal parasites in patients treated at the Clinic of internal diseases and diabetology of the Silesian medical academy, Zabrze. Ann Parasitol 44(4):705–713

    Google Scholar 

  • Jíra J (1998) Medical helminthology. Helminths Parasitic Diseases. 1st edn. Galén, Praha, pp 491

  • Kazacos KR (1983) Improved method for recovering ascarid and other helminth eggs from soil associated with epizootics and during survey studies. Am J Vet Res 44(5):896–900

    CAS  PubMed  Google Scholar 

  • Keiser P, Nutman T (2004) Strongyloides stercoralis in the immunocompromised population. Clin Microbiol Rev 17:208–217. doi:10.1128/CMR.17.1.208-217.2004

    Article  PubMed  PubMed Central  Google Scholar 

  • Khieu V, Schär F, Marti H, Sayasone S, Duong S, Muth S, Odermatt P (2013) Diagnosis, treatment and risk factors of Strongyloides stercoralis in schoolchildren in Cambodia. PLoS Negl Trop Dis 7(2):e2035. doi:10.1371/journal.pntd.0002035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koga K, Kasuya S, Khamboonruang C, Sukhavat K, Ieda M, Takatsuka N, Kita K, Ohtomo H (1991) A modified agar plate method for detection of Strongyloides stercoralis. AmJTrop Med Hyg 54(4):518–521

    Google Scholar 

  • Koňáková G, Virgala J, Straka Š, Kožárová M, Škračíková J (1986) Strongyloidosis within the framework of mixed parasitoses in a 16-month-old child. Čs Pediat 41(12):728–729

    Google Scholar 

  • Loufty MR, Wilson M, Keystone JS, Kain KC (2002) Serology and eosinophil count in the diagnosis and management of strongyloidiasis in a non-endemic area. AmJTrop Med Hyg 66(6):749–752

    Google Scholar 

  • Magnaval JF, Mansuy JM, Villeneuve L, Cassaing S (2000) A retrospective study of autochthonous strongyloidiasis in Région Midi-Pyrénées (Southwestern France). Eur J Epid 16(2):179–182

    Article  CAS  Google Scholar 

  • Marcos LA, Terashima A, Dupont HL, Gotuzzo E (2008) Strongyloides hyperinfection syndrome: an emerging global infectious disease. Trans R Soc Trop Med Hyg 102(4):314–318. doi:10.1016/j.trstmh.2008.01.020

    Article  PubMed  Google Scholar 

  • Mejia R, Nutman TB (2012) Screening, prevention, and treatment for hyperinfection syndrome and disseminated infections caused by Strongyloides stercoralis. Curr Opin Infect Dis 25(4):458–463. doi:10.1097/QCO.0b013e3283551dbd

    Article  PubMed  PubMed Central  Google Scholar 

  • Mirdha B (2009) Human strongyloidiasis: often brushed under the carpet. Trop Gastroenterol 30(1):1–4

    Article  CAS  PubMed  Google Scholar 

  • Nolan TJ (2001) Canine strongyloidiasis. In: Bowman DD (ed): Companion and Exotic Animal Parasitology, International veterinary information Service, Ithaca, New York, USA

  • Nolan TJ, Brenes M, Ashton FT, Zhu X, Forbes WM, Boston R, Schad GA (2004) The amphidial neuron pair ALD controls the temperature-sensitive choice of alternative developmental pathways in the parasitic nematode, Strongyloides stercoralis. Parasitology 129:753–759 https://doi.org/10.1017/S0031182004006092

    Article  CAS  PubMed  Google Scholar 

  • Olsen A, van Lieshout I, Marti H, Polderman T, Polman K, Steinmann P, Stothard R et al (2009) Strongyloidiasis—the most neglected of the neglected tropical diseases? Trans R Soc Trop Med Hyg 103(10):967–972. doi:10.1016/j.trstmh.2009.02.013

    Article  PubMed  Google Scholar 

  • Papazahariadou M, Founta A, Papadopoulos E, Chliounakis S, Antoniadou-Sotiriadou K, Theodorides Y (2007) Gastrointestinal parasites of shepherd and hunting dogs in the Serres Prefecture, Northern Greece. Vet Parasitol 148:170–173. doi:10.1016/j.vetpar.2007.05.013

    Article  CAS  PubMed  Google Scholar 

  • Riggio F, Mannella R, Ariti G, Perrucci S (2013) Intestinal and lung parasites in owned dogs and cats from central Italy. Vet Parasitol 193(1–3):78–84. doi:10.1016/j.vetpar.2012.11.026

    Article  PubMed  Google Scholar 

  • Rudohradská P, Halánová M, Ravaszová P, Goldová M, Valenčáková A, Halán M et al (2012) Prevalence of intestinal parasites in children from minority group with low hygienic standards in Slovakia. Helminthologia 49:63–66. doi:10.2478/s11687-012-0013-2

    Article  Google Scholar 

  • Sánchez PR, Guzman AP, Guillen SM, Adell RI, Estruch AM, Gonzalo IN, Olmos CR (2001) Endemic strongyloidiasis on the Spanish Mediterranean coast. Q J Med 94(7):357–363. doi:10.1093/qjmed/94.7.357

    Article  Google Scholar 

  • Sánchez PR, Guzman AP, Guillen SM, Adell RI, Generoso SS, Estébanez CT (2003) High prevalence of Strongyloides stercoralis among farm workers on the Mediterranean coast of Spain: analysis of the predictive factors of infection in developed countries. AmJTrop Med Hyg 69(3):336–340

    Google Scholar 

  • Schad GA, Smith G, Megyeri Z, Bhopale VM, Niamatali S, Maze R (1993) Strongyloides stercoralis an initial autoinfective burst amplifies primary infection. AmJTrop Med Hyg 48:716–725

    CAS  Google Scholar 

  • Siddiqui AA, Berk SL (2001) Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis 33:1040–1047. doi:10.1086/322707

    Article  CAS  PubMed  Google Scholar 

  • Steinmann P, Zhou X-N, Du Z-W, Jiang J-Y, Wang L-B et al (2007) Occurrence of Strongyloides stercoralis in Yunnan province, China, and comparison of diagnostic methods. PLoS Negl Trop Dis 1(1):e75. doi:10.1371/journal.pntd.0000075

    Article  PubMed  PubMed Central  Google Scholar 

  • Taylor MJ, Garrard TA, O’Donahoo FJ, Ross KE (2014) Human strongyloidiasis: identifying knowledge gaps, with emphasis on environmental control. Research and Reports in Tropical Medicine 5:55–63. doi:10.2147/RRTM.S63138

    Article  Google Scholar 

  • ten Hove R, van Esbroeck M, Vervoort T, van den Ende J, van Lieshout L, Verweij J (2009) Molecular diagnostics of intestinal parasites in returning travellers. Eur J Clin Microbiol Infect Dis 28:1045–1053. doi:10.1007/s10096-009-0745-1

    Article  PubMed  PubMed Central  Google Scholar 

  • Weese JS, Peregrine AS, Anderson MEC, Fulford MB (2011) Parasitic diseases. In: Weese JS and Fulford MB (ed) Companion Animal Zoonoses, 1st edn. Ames, Iowa, USA, pp 3–107

  • Weller PF, Nutman TB (2012) Intestinal nematode infections. In: Longo DL, Fauci AS, Kasper DL, Hauser SL, Jameson JL, Loscalzo J (eds) Harrison’s principles of internal medicine, vol 1, 18th edn. McGraw Hill Medical, New York, pp 1739–1744

  • Wurtz R, Mirot M, Fronda G, Peters C, Kocka F (1994) Short report: gastric infection by Strongyloides stercoralis. AmJTrop Med Hyg 51:339–340

    CAS  Google Scholar 

  • Zukiewicz M, Kaczmarski M, Topczewska M, Sidor K, Tomaszewska BM (2011) Epidemiologial and clinical picture of parasitic infection in the group of children and adolescent from north-east region of Poland. Ann Parasitol 57(3):179–187

    Google Scholar 

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Acknowledgments

This study was funded by the projects of the Scientific Grant Agency of the Ministry of Education of the SR and the Slovak Academy of Sciences, VEGA 1/0455/15.

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Correspondence to G. Štrkolcová.

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Štrkolcová, G., Goldová, M., Bocková, E. et al. The roundworm Strongyloides stercoralis in children, dogs, and soil inside and outside a segregated settlement in Eastern Slovakia: frequent but hardly detectable parasite. Parasitol Res 116, 891–900 (2017). https://doi.org/10.1007/s00436-016-5362-1

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