Skip to main content
Log in

Molecular and epidemiological characterization of Giardia Intestinalis assemblages detected in Djelfa, Algeria

  • Original Article
  • Published:
Journal of Parasitic Diseases Aims and scope Submit manuscript

Abstract

Giardia intestinalis is a flagellated protozoan that lives and proliferates in the small intestine of the host causing giardiasis. The route of transmission is the fecal–oral route, either directly or indirectly. Limited genetic information on G. intestinalis is known in Algeria. This study aimed to estimate the prevalence of G. intestinalis assemblages in the city of Djelfa. A total of 355 fecal samples were collected from symptomatic and asymptomatic school children aged ranged between 6 and 11 years old. Genotyping was done to the Giardia positive samples (n = 30) targeting the beta-giardin gene by applying PCR/RFLP assay. Our data showed that most of the cases were asymptomatic (56.7%). Co-infection with other intestinal parasites was found in 16.6% of cases. We obtained 28/30 positive PCR products while two samples only showed false-negative results, and only 20 samples have shown strong PCR products suitable for RFLP analysis. Assemblage A (70%) was more prevalent than assemblage B (30%) and was more expressed by signs than assemblage B. Moreover, only assemblage A was associated with close contacts with domestic animals and birds. In conclusion, this study gave the first molecular data on G. intestinalis isolates in the city of Djelfa. Further expanded studies using more genes and covering other cities in Algeria are mostly needed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abdullah I, Tak H, Ahmad F, Gul N, Nabi S, Sofi TA (2016) Predominance of gastrointestinal protozoan parasites in children: a brief review. J Health Educ Res Dev 4:4. https://doi.org/10.4172/2380-5439.1000194

    Google Scholar 

  • Acosta AM, Chavez CB, Flores JT, Olotegui MP, Pinedo SR, Trigoso DR et al (2014) The MAL-ED Study: a multinational and multidisciplinary approach to understand the relationship between enteric pathogens, malnutrition, gut physiology, physical growth, cognitive development, and immune responses in infants and children up to 2 years of age in resource-Poor environments. Clin Infect Dis 59:193–206. https://doi.org/10.1093/cid/ciu653

    CAS  Google Scholar 

  • Al-Mohammed HI (2011) Genotypes of Giardia intestinalis clinical isolates of gastrointestinal symptomatic and asymptomatic Saudi children. Parasitol Res 108:1375–1381. https://doi.org/10.4297/najms.2011.3362

    PubMed  Google Scholar 

  • Al-Shehri H, LaCourse EJ, Klimach O, Kabatereine NB, Stothard JR (2018) Molecular characterization and taxon assemblage typing of giardiasis in primary school children living close to the shoreline of Lake Albert, Uganda. Parasite Epidemiol Control 3:e00074. https://doi.org/10.1016/j.parepi.2018.e00074

    Google Scholar 

  • Amar CF, Dear PH, Pedraza-Diaz S, Looker N, Linnane E, McLauchlin J (2002) Sensitive PCR-restriction fragment length polymorphism assay for detection and genotyping of Giardia duodenalis in human feces. J Clin Microbiol 40(2):446–452. https://doi.org/10.1128/JCM.40.2.446-452.2002

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anuar TS, Moktar N, Salleh FM, Al-Mekhlafi HM (2015) Human Giardiasis in Malaysia: correlation between the presence of clinical manifestation and Giardia intestinalis assemblage. Southeast Asian J Trop Med Public Health 46(5):835–843

    PubMed  Google Scholar 

  • Babaei Z, Oormazdi H, Akhlaghi L, Rezaie S, Razmjou E, Soltani- Arabshahi SK, Meamar AR, Hadighi R (2008) Molecular characterization of the Iranian isolates of Giardia lamblia: application of the glutamate dehydrogenase gene. Iran J Publ Health 37(2):75–82

    CAS  Google Scholar 

  • Benouis A, Bekkouche Z, Benmansour Z (2013) Epidemiological study of human intestinal parasitosis in the Hospital of Oran (Algeria). Int J Innov Appl Studies (IJIAS) 2(4):613–620

    Google Scholar 

  • 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(12):5940–5944. https://doi.org/10.1128/JCM.43.12.5940-5944.2005

    CAS  PubMed  PubMed Central  Google Scholar 

  • Caccio SM, Ryan U (2008) Molecular epidemiology of giardiasis. Mol Biochem Parasit 160:75–80

    CAS  Google Scholar 

  • Caccio SM, De Giacomo M, Pozio E (2002) Sequence analysis of the beta-giardin gene and development of a polymerase chain reaction-restriction fragment length polymorphism assay to genotype Giardia duodenalis cysts from human fecal samples. Int J Parasitol 32(8):1023–1030

    CAS  PubMed  Google Scholar 

  • Cardona GA, Carabin H, Goñi P, Arriola L, Robinson G, Fernández- Crespo JC, Clavel A, Chalmers RM, Carmena D (2011) Identification and molecular characterization of Cryptosporidium and Giardia in children and cattle populations from the province of Alava, North of Spain. Sci Total Environ 413:101–108. https://doi.org/10.1016/j.scitotenv.2011.09.076

    CAS  Google Scholar 

  • Cedillo-Rivera R, Darby JM, Enciso-Moreno JA, Ortega-Pierres G, Ey PL (2003) Genetic homogeneity of axenic isolates of Giardia intestinalis derived from acute and chronically infected individuals in Mexico. Parasitol Res 90(2):119–123

    PubMed  Google Scholar 

  • de Lucio A, Martínez-Ruiz R, Merino FJ, Bailo B, Aguilera M, Fuentes I, Carmena D (2015) Molecular genotyping of Giardia duodenalis isolates from symptomatic individuals attending two major public hospitals in Madrid, Spain. PLoS One 10:e0143981. https://doi.org/10.1371/journal.pone.0143981

    CAS  PubMed  PubMed Central  Google Scholar 

  • Feng Y, Xiao L (2011) Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev 24(1):110–140. https://doi.org/10.1128/CMR.00033-10

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gasparinho C, Ferreira FS, Mayer AC, Mirante MC, Nery SV, Santos-Reis A, Portugal-Calisto D, Brito M (2017) Molecular characterization of Giardia lamblia in children less than 5 years of age with diarrhoea attending the Bengo General Hospital, Angola. Trans R Soc Trop Med Hyg 111:497–503. https://doi.org/10.1093/trstmh/try004

    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 diarrhea in human patients in Belgium. Parasitol 136(10):1161–1168. https://doi.org/10.1017/S0031182009990436

    CAS  Google Scholar 

  • Hamaidi F, Chaouch A, Kais H, Zahraoui R, Benghrebia A, Hamaidi MS, Megatel S (2010) Etude des parasitoses digestives dans la région de Boufarik (Blida), Nord-Ouest d’Algérie. La science en liberté 4:13

    Google Scholar 

  • Hatam Nahavand K, Fallah E, Asgharzadeh M, Mırsamad N, Mahdavıpour B (2011) Glutamate dehydrogenase and triose-phosphate-isomerase coding genes for detection and genetic characterization of Giardia lamblia in human feces by PCR and PCRRFLP. Turk J Med Sci 41(2):283–289

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Hooshyar H, Ghafarinasab S, Arbabi M, Delavari M, Rasti S (2017) Genetic variation of Giardia lamblia isolates from food-handlers in Kashan, Central Iran. Iran J Parasitol 12(1):83–89

    PubMed  PubMed Central  Google Scholar 

  • Itagaki T, Kinoshita S, Aoki M, Itoh N, Saeki H, Sato N, Uetsuki J, Izumiyama S, Yagita K, Endo T (2005) Genotyping of Giardia intestinalis from domestic and wild animals in Japan using glutamate dehydrogenase gene sequencing. Vet Parasitol 133(4):283–287

    CAS  PubMed  Google Scholar 

  • Jerez-Puebla LE, Núñez FA, Martinez-Silva I, Rojas-Rivero L, Martinez-González M, Mendez-Sutil Y, Ayllon-Valdés L, Atencio-Millán I, Müller N (2015) Molecular characterization and risk factors of Giardia duodenalis among school children from La Habana, Cuba. J Parasitol Res 2015:378643. https://doi.org/10.1007/s12639-016-0816-z

    PubMed  PubMed Central  Google Scholar 

  • Kasaei R, Carmena D, Jelowdar A, Beiromvand M (2018) Molecular genotyping of Giardia duodenalis in children from Behbahan, southwestern Iran. Parasitol Res 117(5):1425–1431. https://doi.org/10.1007/s00436-018-5826-6

    PubMed  Google Scholar 

  • Kashinahanji M, Haghighi A, Bahrami F, Fallah M, Saidijam M, Matini M, Maghsood AH (2019) Giardia lamblia assemblages A and B isolated from symptomatic and asymptomatic persons in Hamadan, West of Iran. J Parasit Dis 43(4):616–623. https://doi.org/10.1007/s12639-019-01139-x

    PubMed  Google Scholar 

  • Laishram S, Kang G, Ajjampur SS (2012) Giardiasis: a review on assemblage distribution and epidemiology in India. Indian J Gastroenterol 31(1):3–12. https://doi.org/10.1007/s12664-012-0161-9

    PubMed  Google Scholar 

  • Lalle M, Jimenez-Cardosa E, Cacciò SM, Pozio E (2005) Genotyping of Giardia duodenalis from humans and dogs from Mexico using a β-giardin nested polymerase chain reaction assay. J Parasitol 91(1):203–205

    CAS  PubMed  Google Scholar 

  • Lalle M, Bruschi F, Castagna B, Campa M, Pozio E, Cacciò SM (2009) High genetic polymorphism among Giardia duodenalis isolates from Sahrawi children. Trans R Soc Trop Med Hyg 103:834–838. https://doi.org/10.1016/j.trstmh.2009.04.017

    CAS  PubMed  Google Scholar 

  • Lane S, Lloyd D (2002) Current trends in research into the waterborne parasite Giardia. Crit Rev Microbiol 28(2):123–147

    PubMed  Google Scholar 

  • Lebbad M, Petersson I, Karlsson L, Botero-Kleiven S, Andersson JO, Svenungsson B, Svard SG (2011) Multilocus genotyping of human Giardia isolates suggests limited zoonotic transmission and association between assemblage B and flatulence in children. PLoS Negl Trop Dis 5(8):e1262. https://doi.org/10.1371/journal.pntd.0001262

    PubMed  PubMed Central  Google Scholar 

  • Muhsen K, Cohen D, Levine MM (2014) Can Giardia lamblia infection lower the risk of acute diarrhea among preschool children? J Trop Pediatr 60(2):99–103. https://doi.org/10.1093/tropej/fmt085

    PubMed  Google Scholar 

  • Nasiri Goorabi L, Pirestani M, Sadraei J (2017) Genotyping of Giardia duodenalis by β-giardin gene in asymptomatic patients. J Mazandaran Univ Med Sci 27:27–34

    Google Scholar 

  • Pestehchian N, Rasekh H, Babaei Z, Yousefi HA, Eskandarian AA, Kazemi M, Akbari M (2012) Identification of genotypes of Giardia duodenalis human isolates in Isfahan, Iran, using polymerase chain reaction—restriction fragment length polymorphism. Adv Biomed Res 1:84. https://doi.org/10.4103/2277-9175.105166

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qader AM, Bakir TY (2011) Molecular identification of Giardia duodenalis parasite isolates from human by polymerase chain reaction–restriction fragment length polymorphism technique (PCR-RFLP) in Baghdad province. Diyala J Pure Sci 7(4):54–66

    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 

  • Ramírez JD, Heredia RD, Hernández C, León CM, Moncada LI, Reyes P, Pinilla AE, Lopez MC (2015) Molecular diagnosis and genotype analysis of Giardia duodenalis in asymptomatic children from a rural area in Central Colombia. Infect Genet Evol 32:208–213. https://doi.org/10.1016/j.meegid.2015.03.015

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Robertson LJ, Hanevik K, Escobedo AA, Mørch K, Langeland N (2010) Giardiasis—why do the symptoms sometimes never stop? Trends Parasitol 26(2):75–82. https://doi.org/10.1016/j.pt.2009.11.010

    PubMed  Google Scholar 

  • Roointan ES, Rafiei A, Samarbafzadeh AR, Shayesteh AA, Shamsizadeh A, Pourmahdi Borujeni M (2013) Genotype analysis of Giardia lamblia isolated from children in Ahvaz, South west of Iran. Jundishapur J Microbiol 6(3):279–283

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Saksirisampant W, Boontanom P, Mungthin M, Tan-ariya P, Lamchuan D, Siripattanapipong S, Leelayoova S (2012) Prevalence of giardiasis and genotypic of Giardia duodenalis in hilltribe children, northern Thailand. Trop Biomed 29(3):331–338

    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 

  • Savioli L, Smith H, Thompson A (2006) Giardia and Cryptosporidium join the neglected diseases initiative. Trends Parasitol 22(5):203–208. https://doi.org/10.1016/j.pt.2006.02.015

    CAS  PubMed  Google Scholar 

  • Sirize JY, Vitoux C, Holvort L, Carrie E (2008) Main pathologies of children returning from holiday in their country of origin. J Pediatr Pueric 21:67–77

    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. https://doi.org/10.1016/j.actatropica.2015.10.008

    CAS  PubMed  Google Scholar 

  • Skhal D, Aboualchamat G, Al Mariri A, Al Nahhas S (2017) Prevalence of Giardia duodenalis assemblages and sub-assemblages in symptomatic patients from Damascus city and its suburbs. Infect Gen Evol 47:155–160. https://doi.org/10.1016/j.meegid.2016.11.030

    Google Scholar 

  • Soliman RH, Fuentes I, Rubio JM (2011) Identification of a novel Assemblage B sub-genotype and a zoonotic Assemblage C in human isolates of Giardia intestinalis in Egypt. Parasitol Int 60:507–511. https://doi.org/10.1016/j.parint.2011.09.006

    CAS  PubMed  Google Scholar 

  • Sprong H, Caccio SM, van der Giessen JWB, On behalf of the ZOOPNET Network and Partners (2009) Identification of zoonotic genotypes of Giardia duodenalis. PLoS Negl Trop Dis 3(12):e558. https://doi.org/10.1371/journal.pntd.0000558

    CAS  PubMed  PubMed Central  Google Scholar 

  • Squire SA, Ryan U (2017) Cryptosporidium and Giardia in Africa: current and future challenges. Parasit Vectors 10:195. https://doi.org/10.1186/s13071-017-2111-y

    PubMed  PubMed Central  Google Scholar 

  • Veenemans J, Mank T, Ottenhof M, Baidjoe A, Mbugi EV, Demir AY, Wielders JP, Savelkoul HF, Verhoef H (2011) Protection against diarrhea associated with Giardia intestinalis Is lost with multi-nutrient supplementation: a study in Tanzanian children. PLoS Negl Trop Dis 5(6):e1158. https://doi.org/10.1371/journal.pntd.0001158

    PubMed  PubMed Central  Google Scholar 

  • Wielinga C, Thompson RC, Monis P, Ryan U (2015) Identification of polymorphic genes for use in assemblage B genotyping assays through comparative genomics of multiple assemblage B Giardia duodenalis isolates. Mol Biochem Parasitol 201:1–4. https://doi.org/10.1016/j.molbiopara.2015.05.002

    CAS  PubMed  Google Scholar 

  • Yong TS, Park SJ, Hwang UW, Yang HW, Lee KW, Min DY, Min DY, Rim HJ, Wang Y, Zheng F (2000) Genotyping of Giardia lamblia isolates from humans in China and Korea using ribosomal DNA sequences. J Parasitol 86:887–891. https://doi.org/10.1645/0022-3395(2000)086%5b0887:goglif%5d2.0.co;2

    CAS  PubMed  Google Scholar 

Download references

Acknowledgement

The authors thank all the patients’ families who participated in this study. This research was conducted with co assistance from both Damascus University, Syria and Zîane Achour University, Algeria.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Samar Al Nahhas.

Ethics declarations

Conflict of interest

We declare that no conflicts of interest concerning the work reported in this paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rebih, N., Boutaiba, S., Aboualchamat, G. et al. Molecular and epidemiological characterization of Giardia Intestinalis assemblages detected in Djelfa, Algeria. J Parasit Dis 44, 281–288 (2020). https://doi.org/10.1007/s12639-020-01206-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12639-020-01206-8

Keywords

Navigation