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Strongyloides stercoralis larvae found for the first time in tap water using a novel culture method

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Abstract

Strongyloides stercoralis (S. stercoralis) is a soil-borne helminth but its prevalence in water samples is underestimated. The aim of the present study is to propose non-nutrient agar (NNA) as a novel culture method in the diagnosis of Strongyloides and to detect the prevalence rate of S. stercoralis larvae in tap water samples in Beni-Suef Governorate, Egypt. Eighty tap water samples were collected from Beni-Suef Governorate and each sample was filtered in three steps using three filters: one filter for microscopic examination of wet mount, while the remaining two filters were cultured on both NNA and nutrient agar plate (APC). S. stercoralis larvae, adults, and eggs were detected in two (2.5%) and four (5%) out of 80 samples after examination of wet mount preparation and cultures on both NNA and APC, respectively. NNA succeeded to maintain Strongyloides alive for up to 1 month. Our study is the first to detect Strongyloides larvae in tap water in Egypt and the first to use NNA as a novel culture media for Strongyloides.

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References

  • Anamnart W, Intapan PM, Maleewong WA (2013) Modified formalin-ether concentration technique for diagnosis of human strongyloidiasis. Korean J Parasitol 51:743–745

    Article  PubMed  PubMed Central  Google Scholar 

  • Antonios SN, Tolba OA, Othman AA, Saad MA (2010) A preliminary study on the prevalence of parasitic infections in immunocompromised children. J Egypt Soc Parasitol 40:617–630

    PubMed  Google Scholar 

  • Arakaki TM, Iwanaga F, Kinjo A, Saito R, Asato T (1990) Efficacy of agar plate culture in detection of Strongyloides stercoralis infection. J Parasitol 76:425–428

    Article  CAS  PubMed  Google Scholar 

  • Azira NMS, Zeehaida M (2010) Strongyloides stercoralis hyperinfection in a diabetic patient: case report. Trop Biomed 27:115–119

    CAS  PubMed  Google Scholar 

  • Badawy AA, Gneidy MR, Ghoniemy AE (2012) Acute diarrhea among military recruits. J Egypt Soc Parasitol 42:309–320

    Article  PubMed  Google Scholar 

  • Bisoffi Z, Buonfrate D, Montresor A, Requena-Méndez A, Muñoz J, Krolewiecki A, Gotuzzo E, Mena MA, Chiodini PL, Anselmi M, Moreira J, Albonico M (2013) Strongyloides stercoralis: a plea for action. PLoS Negl Trop Dis 7:e2214

    Article  PubMed  PubMed Central  Google Scholar 

  • Bogitsh BJ, Carter CE, Oeltmann TN (2012) Intestinal nematodes in human parasitology 4th edn, chapter 16; 291–327,Waltham: Elsevier Academic Press

    Chapter  Google Scholar 

  • Bradbury RS (2013) Free-living amoebae recovered from human stool samples in Strongyloides agar culture. J Clin Microbiol 52(2):699–700

    Article  PubMed  Google Scholar 

  • Duvignaud A, Pistone T, Malvy D (2016) Strongyloidiasis in a young French woman raises concern about possible ongoing autochthonous transmission in Spain. Int J Infect Dis 42:43–44

    Article  PubMed  Google Scholar 

  • El-Beshbishi SN, Abdel-Magied AA, El-Nahas HA, Azab MS, ElShazly AM, Morsy AT, Gamal-Edin MK, El Kadi MA (2005) Geoparasites in rural Dakahlia Governorate, a preliminary based study for development of the community-based intervention programs. J Egypt Soc Parasitol 35:1051–1070

    PubMed  Google Scholar 

  • Etewa SE, Abdel-Rahman SA, Abd El-Aal NF, Fathy GM, El-Shafey MA, Ewis AM (2016) Geohelminths distribution as affected by soil properties, physicochemical factors and climate in Sharkyia governorate Egypt. J Parasit Dis 40:496–504

    Article  PubMed  Google Scholar 

  • Farghly AM, Mohamed SMA, Abdel-Rahman SA, Mohammed FE, El-Bahaie ES, El-Shafey MA (2016) The relation between the prevalence of soil transmitted parasites in the soil and among school children in Zagazig district, Sharkyia Governorate, Egypt. J Parasit Dis 40:1021–1029

    Article  PubMed  Google Scholar 

  • Garcia LS (2001) Diagnostic medical parasitology, 4th edn. ASM Press, Washington, DC

    Google Scholar 

  • Geneidy MR, El-Hamshary NK (2012) A fatal case of strongyloidiasis stercoralis superinfection in an immunocompromized patient. J Egypt Soc Parasitol 42:691–696

    Article  PubMed  Google Scholar 

  • Greaves D, Coggle S, Pollard C, Aliyu S, Moore E (2013) Strongyloides stercoralis infection. BMJ 347:f4610

    Article  PubMed  Google Scholar 

  • Hammersmith KM (2006) Diagnosis and management of Acanthamoeba keratitis. Curr Opin Opthalmol 17:327–331

    Article  Google Scholar 

  • Intapan PM, Maleewong W, Wongsaroj T, Singthong S, Morakote N (2005) Comparison of the quantitative formalin ethyl acetate concentration technique and agar plate culture for diagnosis of human strongyloidiasis. J Clin Microbial 43:1932–1933

    Article  CAS  Google Scholar 

  • Kamizoulis G (2008) Setting health based targets for water reuse (in agriculture). Desalination 218:154–163

    Article  CAS  Google Scholar 

  • Koga K, Kasuya S, Khamboonruang C, Sukhavat K, Nakamura Y, Tani S, Ieda M, Tomita K, Tomita S, Hattan N, Mori M, Makino S (1990) An evaluation of the agar plate method for the detection of Strongyloides stercoralis in northern Thailand. J Trop Med Hyg 93:183–188

    CAS  PubMed  Google Scholar 

  • Koga K, Kasuya S, Khamboonruang C, Sukhavat K, Ieda M, Takatsuka N et al (1991) A modified agar plate method for detection of Strongyloides stercoralis. Am J Trop Med Hyg 45:518–521

    Article  CAS  PubMed  Google Scholar 

  • Krolewiecki AJ, Lammie P, Jacobson J, Gabrielli AF, Levecke B, Socias E, Arias LM, Sosa N, Abraham D, Cimino R, Echazu A, Crudo F, Vercruysse J, Albonico M (2013) A public health response against Strongyloides stercoralis: time to look at soil-transmitted helminthiasis in full. PLoS Negl Trop Dis 7:e2165

    Article  PubMed  PubMed Central  Google Scholar 

  • Mandarino-Pereira A, de Souza FS, Lopes CW, Pereira MJ (2010) Prevalence of parasites in soil and dog feces according to diagnostic tests. Vet Parasitol 170:176–181

    Article  PubMed  Google Scholar 

  • Mara D, Sleigh A (2010) Estimation of Ascaris infection risks in children under 15 from the consumption of wastewater irrigated carrots. J Water Health 8:35–38

    Article  PubMed  Google Scholar 

  • Meamar AR, Rezaian M, Mohraz M, Hadighi R, Kia EB (2007) Strongyloides stercoralis hyper-infection syndrome in HIV+/AIDS patients in Iran. Parasitol Res 101:663–665

    Article  CAS  PubMed  Google Scholar 

  • Noor Azian MY, Sakhone L, Lokman Hakim S, Yusri MY, Nurulsyamzawaty Y, Zuhaizam AH, MohdRodi I, Maslawaty MN (2008) Detection of helminths infections in dogs and soil contamination in rural and urban areas. Southeast Asian J Trop Med Public Health 39:205–212

    Google Scholar 

  • Nunes CM, Sinhorini IL, Ogassawara S (1994) Influence of soil texture in the recovery of Toxocara canis eggs by a flotation method. Vet Parasitol 53:269–274

    Article  CAS  PubMed  Google Scholar 

  • Oge H, Oge S (2000) Quantitative comparison of various methods for detecting eggs of Toxocara canis in samples of sand. Vet Parasitol 92:75–79

    Article  CAS  PubMed  Google Scholar 

  • Olivera Rivero MJ, Alemán MR, López C, Moncada L, Harker PR (2014) Detection of Strongyloides stercoralis in Tierralta, Colombia using four parasitological methods. Rev Cubana Med Trop 66:202–209

    Google Scholar 

  • Olsen A, van Lieshout L, Marti H, Polderman T, Polman K, Steinmann P, Stothard R, Thybo S, Verweij JJ, Magnussen P (2009) Strongyloidiasis - the most neglected of the neglected tropical diseases? Trans R Soc Trop Med Hyg 103:967–972

    Article  PubMed  Google Scholar 

  • Requena-Méndez A, Chiodini P, Bisoffi Z, Buonfrate D, Gotuzzo E, Munoz J (2013) The laboratory diagnosis and follow up of strongyloidiasis: a systematic review. PLoS Negl Trop Dis 7:e2002

    Article  PubMed  PubMed Central  Google Scholar 

  • Richter J, Müller-Stöver I, Strothmeyer H, Göbels K, Schmitt M, Häussinger D (2006) Arthritis associated with Strongyloides stercoralis infection in a HLA B-27-positive African. Parasitol Res 99:706–707

    Article  PubMed  Google Scholar 

  • Román-Sánchez P, Pastor-Guzmán A, Moreno-Guillén S, Igual-Adell R, Suñer-Generoso S, Tornero-Estébanez C (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. Am J Trop Med Hyg 69:336–340

    Article  PubMed  Google Scholar 

  • Schuster FL (2002) Cultivation of pathogenic and opportunistic free-living amebas. Clin Microbiol Rev 15:342–354

    Article  PubMed  PubMed Central  Google Scholar 

  • El Shazly AM, Soliman M, Nemr HI, El Moafyo N, Abel Gawad AG, El Bendary M (2003) Nematodes and water pollution in eastern part of Nile Delta. J Egypt Soc Parasitol 33:631–636

    PubMed  Google Scholar 

  • el-Shazly AM, el-Nahas HA, Soliman M, Sultan DM, Abedl Tawab AH, Morsy TA (2006) The reflection of control programs of parasitic diseases upon gastrointestinal helminthiasis in Dakahlia Governorate, Egypt. J Egypt Soc Parasitol 36:467–480

    PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Steinmann P, Zhou XN, Du ZW, Jiang JY, Wang LB, Wang XZ et al (2007) Occurrence of Strongyloides stercoralis in Yunnan Province, China, and comparison of diagnostic methods. PLoS Negl Trop Dis 1:e75

    Article  PubMed  PubMed Central  Google Scholar 

  • Sukhavat K, Morakote N, Chaiwong P, Piangjai S (1994) Comparative efficacy of four methods for the detection of Strongyloides stercoralis in human stool specimens. Ann Trop Med Parasitol 88:95–96

    Article  CAS  PubMed  Google Scholar 

  • Tzanetou K, Geros I, Kalogeropoulou E, Karathanasis A, Tsoufakis G, Zeroyiannis P, Malamou-Lada E (2003) Is Strongyloides stercoralis endemic in Greece? Arch Hellen Med 20:60–66

    Google Scholar 

  • Umar AA, Bassey SE (2010) Incidence of Strongyloides stercoralis infection in Ungogo, Nassarawa, Dala and Fagge local government areas of Kano state, Nigeria. Bayero J Pure Appl Sci 3:76–80

    Google Scholar 

  • Wang L, Xu L, Luo S, Xie H, Chen W, Wu Z, Sun X (2017) Diagnosis of Strongyloides stercoralis by morphological characteristics combine with molecular biological methods. Parasitol Res 116:1159–1163

    Article  PubMed  Google Scholar 

  • Zaghlool DA, Hassan AA, Moustafa AM, Shahin WA (2016) A case of fatal gastrointestinal haemorrhage due to hyperinfection with Strongyloides stercoralis. J Parasit Dis 40:1347–1350

    Article  PubMed  Google Scholar 

  • Zeehaida M, Zairi NZ, Rahmah N, Maimunah A, Madihah B (2011) Strongyloides stercoralis in common vegetables and herbs in Kota Bharu, Kelantan, Malaysia. Trop Biomed 28:188–193

    CAS  PubMed  Google Scholar 

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Correspondence to Wegdan M. Abd El Wahab.

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The authors declare that they have no competing interests.

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This study was ethically approved from the Committee of Research, Publications, and Ethics of the Faculty of Medicine, Beni-Suef University.

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Handling Editor: Julia Walochnik

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El-Badry, A.A., Hamdy, D.A. & Abd El Wahab, W.M. Strongyloides stercoralis larvae found for the first time in tap water using a novel culture method. Parasitol Res 117, 3775–3780 (2018). https://doi.org/10.1007/s00436-018-6078-1

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  • DOI: https://doi.org/10.1007/s00436-018-6078-1

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