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First genetic characterisation of Giardia in human isolates from Jordan

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Abstract

Little is known about the epidemiology of Giardia in Jordan and to date, no genotyping studies have been conducted on Giardia isolates from Jordanians. In the present study, a total of 49 microscopy-positive faecal samples from Jordanian patients suffering from giardiasis were analysed at two loci: the triose phosphate isomerase (tpi) gene and the glutamate dehydrogenase (gdh) gene. At the tpi locus, a total of 28 samples amplified and assemblage A was identified in 46.4 % (13/28) samples, while assemblage B was identified in 50 % (14/28) samples and a mixed assemblage A and B was identified in one sample (3.6 %) (Table 1). At the gdh locus 48 isolates amplified and of these assemblages A was identified in 43.7 % (21/48) of isolates and assemblage B in 56.3 % (27/48) of isolates. No mixed infections were detected at the gdh locus. Subtyping at the gdh locus identified sub-assemblage AII in 43.7 % (21/48) of isolates and sub-assemblages BIII and BIV in 25 % (12/48) and 31.2 % (15/48) of isolates, respectively, with more genetic diversity in AII isolates than BIII or BIV isolates. Novel sub-types within each sub-assemblage were identified suggesting unique endemicity and anthroponotic transmission of Giardia in Jordanian patients suffering from giardiasis. Further studies are required to better understand the epidemiology and transmission of Giardia in Jordan.

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References

  • Abdel-Dayem M, Al Zou’bi R, Hani RB, Amr ZS (2014) Microbiological and parasitological investigation among food handlers in hotels in the Dead Sea area, Jordan. J Microbiol Immunol Infect 47(5):377–380

    Article  PubMed  Google Scholar 

  • Al-Mohammed HI (2011) Genotypes of Giardia intestinalis clinical isolates of gastrointestinal symptomatic and asymptomatic Saudi children. Parasitol Res 108:1375–1381

    Article  PubMed  Google Scholar 

  • Alyousefi NA, Mahdy MA, Xiao L, Mahmud R, Lim YA (2013) Molecular characterization of Giardia duodenalis in Yemen. Exp Parasitol 134(2):141–147

    Article  CAS  PubMed  Google Scholar 

  • Amer SE (2013) Genotypic and phylogenetic characterization of Giardia intestinalis from human and dairy cattle in Kafr El Sheikh Governorate, Egypt. J Egypt Soc Parasitol 43(1):133–146

    Article  PubMed  Google Scholar 

  • Baldursson S, Karanis P (2011) Waterborne transmission of protozoan parasites: review of worldwide outbreaks—an update 2004–2010. Water Res 45:6603–6614

    Article  CAS  PubMed  Google Scholar 

  • Cacciò SM, Beck R, Lalle M, Marinculic A, Pozio E (2008) Multilocus genotyping of Giardia duodenalis reveals striking differences between assemblages A and B. Int J Parasitol 38(13):1523–1531

    Article  PubMed  Google Scholar 

  • Çiçek C, Şakru N (2015) Genotyping of Giardia intestinalis isolates in the Thrace Region, Turkey. Mikrobiyol Bul 49(4):576–585

    Article  PubMed  Google Scholar 

  • El Basha NR, Zaki MM, Hassanin OM, Rehan MK, Omran D (2016) Giardia assemblages a and b in diarrheic patients: a comparative study in Egyptian children and adults. J Parasitol 102(1):69–74

    Article  PubMed  Google Scholar 

  • Elbakri A, Samie A, Bessong P, Potgieter N, Odeh RA (2014) Detection and molecular characterisation of Giardia lamblia genotypes in Sharjah, United Arab Emirates. Trans R Soc Trop Med Hyg 108(8):466–473

    Article  CAS  PubMed  Google Scholar 

  • Fahmy HM, El-Serougi AO, El Deeb HK, Hussein HM, Abou-Seri HM, Klotz C, Aebischer T, El Sayed Khalifa Mohamed K (2015) Giardia duodenalis assemblages in Egyptian children with diarrhea. Eur J Clin Microbiol Infect Dis 34(8):1573–1581

    Article  CAS  PubMed  Google Scholar 

  • Feng Y, Xiao L (2011) Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev 24(1):110–40

  • Foronda P, Bargues MD, Abreu-Acosta N, Periago MV, Valero MA, Valladares B, Mas-Coma S (2008) Identification of genotypes of Giardia intestinalis of human isolates in Egypt. Parasitol Res 103:1177–1181

    Article  CAS  PubMed  Google Scholar 

  • Geurden T, Geldhof P, Levecke B, Martens C, Berkvens D, Casaert S, Vercruysse J, Claerebout E (2008) Mixed Giardia duodenalis assemblage A and E infections in calves. Int J Parasitol 38(2):259–264

    Article  CAS  PubMed  Google Scholar 

  • Geurden T, Levecke B, Cacció SM, Visser A, De Groote G, Casaert S, Vercruysse J, Claerebout E (2009) Multilocus genotyping of Cryptosporidium and Giardia in non-outbreak related cases of diarrhoea in human patients in Belgium. Parasitology 136(10):1161–1168

    Article  CAS  PubMed  Google Scholar 

  • Hazrati Tappeh K, Manafi G, Asgharzadeh M, Manafi F (2014) Incidence of Giardia lamblia Subspecies by PCR-RFLP in stool specimens of hospitalized children at Urmia Mutahhari Hospital, West Azerbaijan Province, Iran. Iran J Parasitol 9(4):541–547

    PubMed  PubMed Central  Google Scholar 

  • Hellard ME, Sinclair MI, Hogg GG, Fairley CK (2000) Prevalence of enteric pathogens among community based asymptomatic individuals. J Gastroenterol Hepatol 15:290–293

    Article  CAS  PubMed  Google Scholar 

  • Helmy MMF, Abdel-Fattah HS, Rashed L (2009) Real-time PCR/RFLP assay to detect Giardia intestinalis genotypes in human isolates with diarrhea in Egypt. J Parasitol 95:1000–1004

    Article  CAS  PubMed  Google Scholar 

  • Helmy YA, Klotz C, Wilking H, Krücken J, Nöckler K, Von Samson-Himmelstjerna G, Zessin KH, Aebischer T (2014) Epidemiology of Giardia duodenalis infection in ruminant livestock and children in the Ismailia province of Egypt: insights by genetic characterization. Parasit Vectors 7(1):321

    Article  PubMed  PubMed Central  Google Scholar 

  • Hijjawi N, Ng J, Yang R, Atoum MF, Ryan U (2010) Identification of rare and novel Cryptosporidium GP60 subtypes in human isolates from Jordan. Exp Parasitol 125(2):161–164

    Article  CAS  PubMed  Google Scholar 

  • Hussein AI, Yamaguchi T, Nakamoto K, Iseki M, Tokoro M (2009) Multiple-subgenotype infections of Giardia intestinalis detected in Palestinian clinical cases using a subcloning approach. Parasitol Int 58(3):258–262

    Article  PubMed  Google Scholar 

  • Hussein EM, Zaki WM, Ahmed SA, Almatary AM, Nemr NI, Hussein AM (2016) Predominance of Giardia lamblia assemblage A among iron deficiency anaemic pre-school Egyptian children. Parasitol Res

  • Karanis P, Kourenti C, Smith H (2007) Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt. J Water Health 5(1):1–38

    Article  PubMed  Google Scholar 

  • Kohli A, Bushen OY, Pinkerton RC, Houpt E, Newman RD, Sears CL, Lima AA, Guerrant RL (2008) Giardia duodenalis assemblage, clinical presentation and markers of intestinal inflammation in Brazilian children. Trans R Soc Trop Med Hyg 102(7):718–725

    Article  PubMed  PubMed Central  Google Scholar 

  • Miyamoto Y, Eckmann L (2015) Drug development against the major diarrhea-causing parasites of the small intestine, Cryptosporidium and Giardia. Front Microbiol 6:1208

    Article  PubMed  PubMed Central  Google Scholar 

  • Monis PT, Mayrhofer G, Andrews RH, Homan WL, Limper L, Ey PL (1996) Molecular genetic analysis of Giardia intestinalis isolates at the glutamate dehydrogenase locus. Parasitology 112(Pt 1):1–12

    Article  CAS  PubMed  Google Scholar 

  • Monis PT, Andrews RH, Mayrhofer G, Ey PL (2003) Genetic diversity within the morphological species Giardia intestinalis and its relationship to host origin. Infect Genet Evol 3:29–38

    Article  CAS  PubMed  Google Scholar 

  • Mowatt MR, Weinbach EC, Howard TC, Nash TE (1994) Complementation of an Escherichia coli glycolysis mutant by Giardia lamblia triosephosphate isomerase. Exp Parasitol 78(1):85–92

    Article  CAS  PubMed  Google Scholar 

  • Nimri LF (1993) Evidence of an epidemic of Blastocystis hominis infections in preschool children in northern Jordan. J Clin Microbiol 31(10):2706–2708

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nimri LF (1994) Prevalence of giardiasis among primary school children. Child Care Health Dev 20(4):231–237

    Article  CAS  PubMed  Google Scholar 

  • Nimri LF (2003) Cyclospora cayetanensis and other intestinal parasites associated with diarrhea in a rural area of Jordan. Int Microbiol 6(2):131–135

    Article  PubMed  Google Scholar 

  • Nimri LF, Meqdam M (2004) Enteropathogens associated with cases of gastroenteritis in a rural population in Jordan. Clin Microbiol Infect 10(7):634–639

    Article  CAS  PubMed  Google Scholar 

  • Painter JE, Gargano JW, Collier SA, Yoder JS, Centers for Disease Control and Prevention (2015) Giardiasis surveillance—United States, 2011–2012. MMWR Surveill Summ 64(Suppl 3):15–25

    Google Scholar 

  • Pestechian N, Rasekh H, Rostami-Nejad M, Yousofi HA, Hosseini-Safa A (2014) Molecular identification of Giardia lamblia; is there any correlation between diarrhea and genotyping in Iranian population? Gastroenterol Hepatol Bed Bench 7(3):168–172

    PubMed  PubMed Central  Google Scholar 

  • Rafiei A, Roointan ES, Samarbafzadeh AR, Shayesteh AA, Shamsizadeh A, Pourmahdi Borujeni M (2013) Investigation of possible correlation between Giardia duodenalis genotypes and clinical symptoms in Southwest of Iran. Iran J Parasitol 8(3):389–395

    PubMed  PubMed Central  Google Scholar 

  • Rayani M, Zasmy Unyah N, Hatam G (2014) Molecular Identification of Giardia duodenalis isolates from Fars Province, Iran. Iran J Parasitol 9(1):70–78

    CAS  PubMed  PubMed Central  Google Scholar 

  • Read CM, Monis PT, Thompson RC (2004) Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infect Genet Evol 4:125–130

    Article  CAS  PubMed  Google Scholar 

  • Rendtorff RC (1954) The experimental transmission of human intestinal protozoan parasites. II. Giardia lamblia cysts given in capsules. Am J Hyg 59:209–220

    CAS  PubMed  Google Scholar 

  • Robertson LJ, Forberg T, Hermansen L, Hamnes IS, Gjerde B (2007) Giardia duodenalis cysts isolated from wild moose and reindeer in Norway: genetic characterization by PCR-RFLP and sequence analysis at two genes. J Wildl Dis 43:576–585

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Hernandez J, Canut-Blasco A, Martin-Sanchez AM (1996) Seasonal prevalences of Cryptosporidium and Giardia infections in children attending day care centres in Salamanca (Spain) studied for a period of 15 months. Eur J Epidemiol 12:291–295

    Article  CAS  PubMed  Google Scholar 

  • Ryan U, Cacciò SM (2013) Zoonotic potential of Giardia. Int J Parasitol 43(12–13):943–956

    Article  CAS  PubMed  Google Scholar 

  • Sarkari B, Ashrafmansori A, Hatam GR, Motazedian MH, Asgari Q, Mohammadpour I (2012) Genotyping of Giardia lamblia isolates from human in southern Iran. Trop Biomed 29(3):366–371

    CAS  PubMed  Google Scholar 

  • Skhal D, Aboualchamat G, Al Nahhas S (2016) Giardia duodenalis in Damascus, Syria: Identification of Giardia genotypes in a sample of human fecal isolates using polymerase chain reaction and restriction fragment length polymorphism analyzing method. Acta Trop 154:1–5

    Article  CAS  PubMed  Google Scholar 

  • Soliman RH, Fuentes I, Rubio JM (2011) Identification of a novel assemblage B subgenotype and a zoonotic assemblage C in human isolates of Giardia intestinalis in Egypt. Parasitol Int 60:507–511

    Article  CAS  PubMed  Google Scholar 

  • Sprong H, Cacciò SM, van der Giessen JW, ZOOPNET network and partners (2009) Identification of zoonotic genotypes of Giardia duodenalis. PLoS Negl Trop Dis 3(12):e558

    Article  PubMed  PubMed Central  Google Scholar 

  • Sulaiman IM, Fayer R, Bern C, Gilman RH, Trout JM, Schantz PM, Das P, Lal AA, Xiao L (2003) Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis. Emerg Infect Dis 9:1444–1452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamer GS, Kasap M, Er DK (2015) Genotyping and phylogenetic analysis of Giardia duodenalis isolates from Turkish children. Med Sci Monit 21:526–532

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Giessen JW, de Vries A, Roos M, Wielinga P, Kortbeek LM, Mank TG (2006) Genotyping of Giardia in Dutch patients and animals: a phylogenetic analysis of human and animal isolates. Int J Parasitol 36(7):849–858

    Article  PubMed  Google Scholar 

  • Xiao L, Fayer R (2008) Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int J Parasitol 38:1239–1255

    Article  CAS  PubMed  Google Scholar 

  • Yang R, Murphy C, Song Y, Ng-Hublin J, Estcourt A, Hijjawi N, Chalmers R, Hadfield S, Bath A, Gordon C, Ryan U (2013) Specific and quantitative detection and identification of Cryptosporidium hominis and C. parvum in clinical and environmental samples. Exp Parasitol 135:142–147

    Article  CAS  PubMed  Google Scholar 

  • Yee J, Dennis PP (1992) Isolation and characterization of a NADP-dependent glutamate dehydrogenase gene from the primitive eucaryote Giardia lamblia. J Biol Chem 267:7539–7544

    CAS  PubMed  Google Scholar 

  • Youssef M, Shurman A, Bougnoux M, Rawashdeh M, Bretagne S, Strockbine N (2000) Bacterial, viral and parasitic enteric pathogens associated with acute diarrhea in hospitalized children from northern Jordan. FEMS Immunol Med Microbiol 28:257–263

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Una Ryan.

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Human samples were collected under human ethics permit number 1401254/32.

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The authors declare that they have no competing interests. The authors certify that they have no affiliation with or financial involvement in any organisation or entity with a direct financial interest in the subject matter or materials discussed in the manuscript.

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Hijjawi, N., Yang, R., Mukbel, R. et al. First genetic characterisation of Giardia in human isolates from Jordan. Parasitol Res 115, 3723–3729 (2016). https://doi.org/10.1007/s00436-016-5132-0

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