Abstract
Giardia intestinalis is a common diarrheagenic parasite infecting children globally. It has been classified into eight morphologically identical but genetically distinct genotypes. Human infection is mainly associated with A and B assemblages with variable geographical distribution. The present work aimed to study the epidemiology of assemblages A and B in children inhabiting different areas in Lower Egypt. Stool samples were collected from 315 children and examined microscopically for parasitic infections. Giardia positive samples were genotyped using tpi assemblage specific primers. The prevalence of Giardia was 18.1% among the examined children. Mixed assemblages A and B was more common (47.4%) than single assemblage B (36.8%) or A (15.8%). The distribution of different genotypes was significantly associated with the residence area, animal contact, and handwashing habits. A non-significant association was observed between Giardia assemblages and the clinical manifestations. Assemblage B is the predominant genotype among Egyptian children. The distribution of different Giardia assemblages is strongly associated with the studied area and the habits of its people.
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References
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 43:133–146
Bartelt LA, Sartor RB (2015) Advances in understanding Giardia: determinants and mechanisms of chronic sequelae. F1000prime Rep 7:62. https://doi.org/10.12703/p7-62
Bertrand I, Albertini L, Schwartzbrod J (2005) Comparison of two target genes for detection and genotyping of Giardia lamblia in human feces by PCR and PCR-restriction fragment length polymorphism. J Clin Microbiol 43:5940–5944. https://doi.org/10.1128/jcm.43.12.5940-5944.2005
Caccio SM, Ryan U (2008) Molecular epidemiology of giardiasis. Mol Biochem Parasitol 160:75–80. https://doi.org/10.1016/j.molbiopara.2008.04.006
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 38:1523–1531. https://doi.org/10.1016/j.ijpara.2008.04.008
Cociancic P, Rinaldi L, Zonta ML, Navone GT (2018) Formalin-ethyl acetate concentration, FLOTAC Pellet and anal swab techniques for the diagnosis of intestinal parasites. Parasitol Res 117:3567–3573. https://doi.org/10.1007/s00436-018-6054-9
Einarsson E, Ma’ayeh S, Svard SG (2016) An up-date on Giardia and giardiasis. Curr Opin Microbiol 34:47–52. https://doi.org/10.1016/j.mib.2016.07.019
El-Badry A, Mohammed AF, Abdul Gawad A (2017) Predominance of Giardia intestinalis assemblage B in diarrhoeic children in Sharkia, Egypt. PUJ 10:39–41
El-Tantawy N, Taman A (2014) The epidemiology of Giardia intestinalis assemblages A and B among Egyptian children with diarrhea: a PCR-RFLP-based approach. PUJ 7:104–109. https://doi.org/10.4103/1687-7942.149557
Fantinatti M, Bello AR, Fernandes O, Da-Cruz AM (2016) Identification of Giardia lamblia assemblage E in humans points to a new anthropozoonotic cycle. J Infect Dis 214:1256–1259. https://doi.org/10.1093/infdis/jiw361
Feng Y, Xiao L (2011) Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev 24:110–140. https://doi.org/10.1128/cmr.00033-10
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. https://doi.org/10.1007/s00436-008-1113-2
Garcia LS, Arrowood M, Kokoskin E, Paltridge GP, Pillai DR, Procop GW et al (2017) Laboratory diagnosis of parasites from the gastrointestinal tract. Clin Microbiol Rev 31:e00025-00017. https://doi.org/10.1128/CMR.00025-17
Ghieth MA, El-Badry AA, Abu-Sarea EY, Abdel Gawad SS, Elsharkawy MM (2016) Genotypic analysis of Giardia duodenalis in children at Egypt. Comp Clin Path 25:1241–1246. https://doi.org/10.1007/s00580-016-2337-7
Hamed AF, Yousef F, Omran EK, Moustafa A (2013) Common parasitic infestation among rural population in Sohag Governorate, Egypt. J Am Sci 9:596–601
Hammouda N, Sadaka H, El-Gebaly W, El-Nassery S (1996) Opportunistic intestinal protozoa in chronic diarrhoeic immunosuppressed patients. J Egypt Soc Parasitol 26:143–153
Helmy MM, 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. https://doi.org/10.1645/ge-1670.1
Hollm-Delgado MG, Gilman RH, Bern C, Cabrera L, Sterling CR, Black RE, Checkley W (2008) Lack of an adverse effect of Giardia intestinalis infection on the health of Peruvian children. Am J Epidemiol 168:647–655. https://doi.org/10.1093/aje/kwn177
Homan WL, Mank TG (2001) Human giardiasis: genotype linked differences in clinical symptomatology. Int J Parasitol 31:822–826
Huey CS, Mahdy MA, Al-Mekhlafi HM, Nasr NA, Lim YA, Mahmud R, Surin J (2013) Multilocus genotyping of Giardia duodenalis in Malaysia. Infect Genet Evol 17:269–276. https://doi.org/10.1016/j.meegid.2013.04.013
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 115:1537–1545. https://doi.org/10.1007/s00436-015-4888-y
Hussein EM, Ismail OA, Mokhtar AB, Mohamed SE, Saad RM (2017) Nested PCR targeting intergenic spacer (IGS) in genotyping of Giardia duodenalis isolated from symptomatic and asymptomatic infected Egyptian school children. Parasitol Res 116:763–771. https://doi.org/10.1007/s00436-016-5347-0
Mahdy AK, Surin J, Mohd-Adnan A, Wan KL, Lim YA (2009) Molecular characterization of Giardia duodenalis isolated from Semai Pahang Orang Asli (Peninsular Malaysia aborigines). Parasitology 136:1237–1241. https://doi.org/10.1017/s0031182009990527
Naguib D, El-Gohary AH, Roellig D, Mohamed AA, Arafat N, Wang Y, Feng Y, Xiao L (2018) Molecular characterization of Cryptosporidium spp. and Giardia duodenalis in children in Egypt. Parasit Vectors 11:403. https://doi.org/10.1186/s13071-018-2981-7
Puebla LJ, Nunez FA, Fernandez YA, Fraga J, Rivero LR, Millan IA, Valdes LA, Silva IM (2014) Correlation of Giardia duodenalis assemblages with clinical and epidemiological data in Cuban children. Infect Genet Evol 23:7–12. https://doi.org/10.1016/j.meegid.2014.01.007
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. https://doi.org/10.1016/j.meegid.2004.02.001
Risk H, El-Shazly AM, Soliman M, Mohamad AA, El-Sharkawy EM, Morsy AT (2004) Genotyping of human giardiasis in relation to anti-Giardia secretory IgA and mucosal histopathology. J Egypt Soc Parasitol 34:471–481
Robertson LJ, Hanevik K, Escobedo AA, Morch K, Langeland N (2010) Giardiasis—why do the symptoms sometimes never stop? Trends Parasitol 26:75–82. https://doi.org/10.1016/j.pt.2009.11.010
Ryan U, Hijjawi N, Feng Y, Xiao L (2019) Giardia: an under-reported foodborne parasite. Int J Parasitol 49:1–11. https://doi.org/10.1016/j.ijpara.2018.07.003
Sadek G, El-Settawy M, Nasr S (2013) Genotypic characterization of Giardia duodenalis in children in Menoufiya and Sharkiya governorates Egypt. Life Sci J 10:4006–4015
Sahagun J, Clavel A, Goni P, Seral C, Llorente MT, Castillo FJ, Capilla S, Arias A, Gomez-Lus R (2008) Correlation between the presence of symptoms and the Giardia duodenalis genotype. Eur J Clin Microbiol Infect Dis 27:81–83. https://doi.org/10.1007/s10096-007-0404-3
Sprong H, Caccio SM, van der Giessen JW (2009) Identification of zoonotic genotypes of Giardia duodenalis. PLoS Negl Trop Dis 3:e558. https://doi.org/10.1371/journal.pntd.0000558
Sulaiman I, Fayer R, Bern C, Gilman RH, Trout JM, Schantz PM (2003) Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis. Emerg Infect Dis 9:1444. https://doi.org/10.3201/eid0911.030084
Taha SA, Abd Al Aal Z, Saleh NS, El-Badry AA (2018) Giardia intestinalis assemblages among Egyptian symptomatic children: prevalence and seasonal distribution in Cairo, Egypt. J Egypt Soc Parasitol 48:661–668
Thompson RC (2000) Giardiasis as a re-emerging infectious disease and its zoonotic potential. Int J Parasitol 30:1259–1267
Tungtrongchitr A, Sookrung N, Indrawattana N, Kwangsi S, Ongrotchanakun J, Chaicumpa W (2010) Giardia intestinalis in Thailand: identification of genotypes. J Health Popul Nutr 28:42–52
Wielinga CM, Thompson RC (2007) Comparative evaluation of Giardia duodenalis sequence data. Parasitology 134:1795–1821. https://doi.org/10.1017/s0031182007003071
Yu F, Amer S, Qi M, Wang R, Wang Y, Zhang S, Jian F, Ning C, El Batae H, Zhang L (2019) Multilocus genotyping of Giardia duodenalis isolated from patients in Egypt. Acta Trop 196:66–71. https://doi.org/10.1016/j.actatropica.2019.05.012
Acknowledgements
The authors would like to thank the screened children and their parents for giving consent to participate in the study. They also thank colleagues at the Parasitology Department, Medical Research Institute, Alexandria University, Egypt for their excellent technical assistance.
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The study was approved by the Research Ethics Committee of the Medical Research Institute (MRI), Alexandria University (IORG 0008812). All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments.
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Elhadad, H., Abdo, S., Tolba, M. et al. Detection of Giardia intestinalis assemblages A and B among children from three villages in the West Delta region, Egypt using assemblage specific primers. J Parasit Dis 45, 655–663 (2021). https://doi.org/10.1007/s12639-020-01338-x
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DOI: https://doi.org/10.1007/s12639-020-01338-x