Antigen-Based Diagnosis of Human Giardiasis: A Systematic Review and Meta-Analysis
Abstract
Background: We aimed to present a systematic review and meta-analysis of studies that used antigen-based assays for the diagnosis of human giardiasis.
Methods: All the related published literature cited within PubMed, ISI web of science, Google Scholar, Embase, and Scopus, were searched up to December 2021. The search terms, both as MeSH terms and text words, were “Giardia”, “Giardia lamblia”, “Giardia intestinalis", "giardiasis", combined with "diagnosis", "antigen detection", serodiagnosis, or serological diagnosis. The required data was extracted from the papers. Pooled estimates of sensitivity and specificity were obtained and forest plots and summary receiver operating characteristics (SROC) plots were used to calculate sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV).
Results: The search of databases found 1683 papers, of which 46 articles fulfilled our eligibility criteria. The sensitivity of antigen-based methods for the diagnosis of human giardiasis ranged from 45% (95% CI: 31-59%) to 100% (95% CI: 100-100%) and the pooled estimate of sensitivity was 92% (95% CI: 90-93%). The pooled estimated specificity was 97% (95% CI: 96-98%), ranged from 81% (95% CI: 68-89%) to 100% (95% CI: 98-100%). The summary estimate of PPV and NPV were 92 % (95% CI: 90-93%) and 97% (95% CI: 96-98%) respectively. Comparing the performance of the antigen detection assays by region revealed a significant difference in the assay's performances in different regions of the world.
Conclusion: The antigen-based detection methods have acceptable and satisfactory performance in the diagnosis of human giardiasis. The task ahead is to identify more specific target antigens and design simpler, cheaper, and more sensitive methods for the diagnosis of this common worldwide-distributed parasitic infection.
1. Einarsson E, Ma’ayeh S, Svärd SG. An up-date on Giardia and giardiasis. Curr Opin Microbiol. 2016; 34:47-52.
2. Rogawski ET, Bartelt LA, Platts-Mills JA, S, et al. Determinants and impact of Giardia infection in the first 2 years of life in the MAL-ED birth cohort. J Pediatric Infect Dis Soc. 2017; 6(2):153-60.
3. Feng Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 2011; 24(1):110-40.
4. Bashir M, Farid A, Rabia I, et al. Serological versus antigen detection methods for Giardia duodenalis diagnosis. J Egypt Soc Parasitol. 2014; 44(3):709-18.
5. den Hartog J, Rosenbaum L, Wood Z, Burt D, Petri WA Jr. Diagnosis of multiple enteric protozoan infections by enzyme-linked immunosorbent assay in the Guatemalan highlands. Am J Trop Med Hyg. 2013; 88(1):167-71.
6. Sadaka H, Gaafar M, Mady R, Hezema N. Evaluation of ImmunoCard STAT test and ELISA versus light microscopy in diagnosis of giardiasis and cryptosporidiosis. Parasitol Res. 2015; 114(8):2853-63.
7. Singhal S, Mittal V, Khare V, Singh YI. Comparative analysis of enzyme-linked immunosorbent assay and direct microscopy for the diagnosis of Giardia intestinalis in fecal samples. Indian J Pathol Microbiol. 2015; 58(1):69-71.
8. Hiatt RA, Markell EK, Ng E. How many stool examinations are necessary to detect pathogenic intestinal protozoa? Am J Trop Med Hyg. 1995; 53(1):36-9.
9. Rosoff JD, Sanders CA, Sonnad SS, et al. Stool diagnosis of giardiasis using a commercially available enzyme immunoassay to detect Giardia-specific antigen 65 (GSA 65). J Clin Microbiol. 1989; 27(9):1997-2002.
10. Heyworth MF. Diagnostic testing for Giardia infections. Trans R Soc Trop Med Hyg. 2014; 108(3):123-5.
11. Vidal AMB, Catapani WR. Enzyme-linked immunosorbent assay (ELISA) imm-unoassaying versus microscopy: advantages and drawbacks for diagnosing giardiasis. Sao Paulo Med J. 2005; 123(6):282-5.
12. Christy NC, Hencke JD, Escueta-De Cadiz A, et al. Multisite performance evaluation of an enzyme-linked immunosorbent assay for detection of Giardia, Cryptosporidium, and Entamoeba histolytica antigens in human stool. J Clin Microbiol. 2012; 50(5):1762-3.
13. Silva RK, Pacheco FT, Martins AS,et al. Performance of microscopy and ELISA for diagnosing Giardia duodenalis infection in different pediatric groups. Parasitol Int. 2016;65(6 Pt A):635-640.
14. Uyar Y, Taylan Ozkan A. [Antigen detection methods in diagnosis of amebiasis, giardiasis and cryptosporidiosis]. Turkiye Parazitol Derg. 2009; 33(2):140-50.
15. Hooshyar H, Rostamkhani P, Arbabi M, Delavari M. Giardia lamblia infection: review of current diagnostic strategies. Gastroenterol Hepatol Bed Bench. 2019; 12(1):3-12.
16. Faubert G. Immune response to Giardia duodenalis. Clin Microbiol Rev. 2000;13(1):35-54.
17. Pacheco FTF, de Carvalho SS, Santos SA, et al. Specific IgG and IgA Antibody Reactivities in Sera of Children by Enzyme-Linked Immunoassay and Comparison With Giardia duodenalis Diagnosis in Feces. Ann Lab Med. 2020; 40(5):382-9.
18. Yılmaz A, Uslu H. Examination of Giardia intestinalis with Direct Microscopy and Direct Fluorescent Antibody in Patients with Diarrhea. Turkiye Parazitol Derg. 2020; 44(4):187-90.
19. Green E, Miles M, Warhurst D. Immunodiagnostic detection of Giardia antigen in faeces by a rapid visual enzyme-linked immunosorbent assay. Lancet. 1985; 2(8457):691-3.
20. Janoff E, Craft J, Pickering L, et al. Diagnosis of Giardia lamblia infections by detection of parasite-specific antigens. J Clin Microbiol. 1989; 27(3):431-5.
21. Knisley CV, Engelkirk PG, Pickering LK, et al. Rapid detection of Giardia antigen in stool with the use of enzyme immunoassays. Am J Clin Pathol. 1989; 91(6):704-8.
22. Schieven B, Hussain Z. Evaluation of an enzyme-immunoassay test kit for diagnosing infections with Giardia lamblia. Serodiag Immunother Infec Dis. 1990; 4:109-13.
23. Vidal M, Gilman R, Ungar B, et al. Detection of Giardia lamblia antigen in children living in a Peruvian periurban shantytown (Pueblo Joven). J Clin Microbiol. 1991; 29(3):636-7.
24. Goldin A, Apt Baruch W, Aguilera X, et al. A capture ELISA detects Giardia lamblia antigens in formalin-treated faecal samples. Trans R Soc Trop Med Hyg. 1992; 86:164-5
25. G arcia LS, Shimizu RY. Evaluation of nine immunoassay kits (enzyme immunoassay and direct fluorescence) for detection of Giardia lamblia and Cryptosporidium parvum in human fecal specimens. J Clin Microbiol. 1997; 35(6):1526-9.
26. Behr MA, Kokoskin E, Gyorkos TW, Cédilotte L, Faubert GM, MacLean JD. Laboratory diagnosis for Giardia lamblia infection: a comparison of microscopy, coprodiagnosis and serology. Can J Infect Dis. 1997; 8(1):33-8.
27. Aldeen WE, Carroll K, Robison A, Morrison M, Hale D. Comparison of nine commercially available enzyme-linked immunosorbent assays for detection of Giardia lamblia in fecal specimens. J Clin Microbiol. 1998; 36(5):1338-40.
28. Rocha MO, Guimarães TM, Toledo VT, et al. Detection of a Giardia lamblia coproantigen by using a commercially available imm-unoenzymatic assay, in Belo Horizonte, Brazil. Rev Inst Med Trop Sao Paulo. 1999; 41(3):151-4.
29. Chan R, Chen J, York MK, et al. Evaluation of a combination rapid immunoassay for detection of Giardia and Cryptosporidium antigens. J Clin Microbiol. 2000; 38(1):393-4.
30. Maraha B, Buiting A. Evaluation of four enzyme immunoassays for the detection of Giardia lamblia antigen in stool specimens. Eur J Clin Microbiol Infect Dis. 2000; 19(6):485-7.
31. Hanson KL, Cartwright CP. Use of an enzyme immunoassay does not eliminate the need to analyze multiple stool specimens for sensitive detection of Giardia lamblia. J Clin Microbiol. 2001; 39(2):474-7.
32. Schunk M, Jelinek T, Wetzel K, Nothdurft HD. Detection of Giardia lamblia and Entamoeba histolytica in stool samples by two enzyme immunoassays. Eur J Clin Microbiol Infect Dis. 2001; 20(6):389-91.
33. Duque-Beltrán S, Nicholls-Orejuela RS, Arévalo-Jamaica A, Guerrero-Lozano R, Montenegro S, James MA. Detection of Giardia duodenalis antigen in human fecal eluates by enzyme-linked immunosorbent assay using polyclonal antibodies. Mem Inst Oswaldo Cruz. 2002; 97(8):1165-8.
34. Garcia LS, Shimizu RY, Novak S, Carroll M, Chan F. Commercial assay for detection of Giardia lamblia and Cryptosporidium parvum antigens in human fecal specimens by rapid solid-phase qualitative immunochromatog-raphy. J Clin Microbiol. 2003; 41(1):209-12.
35. Johnston SP, Ballard MM, Beach MJ, Causer L, Wilkins PP. Evaluation of three commercial assays for detection of Giardia and Cryptosporidium organisms in fecal specimens. J Clin Microbiol. 2003; 41(2):623-6.
36. Garcia LS, Garcia JP. Detection of Giardia lamblia antigens in human fecal specimens by a solid-phase qualitative immunochromato-graphic assay. J Clin Microbiol. 2006; 44(12):4587-8.
37. Weitzel T, Dittrich S, Möhl I, Adusu E, Jelinek T. Evaluation of seven commercial antigen detection tests for Giardia and Cryptosporidium in stool samples. Clin Microbiol Infect. 2006; 12(7):656-9.
38. Schuurman T, Lankamp P, van Belkum A, Kooistra-Smid M, Van Zwet A. Comparison of microscopy, real-time PCR and a rapid immunoassay for the detection of Giardia lamblia in human stool specimens. Clin Microbiol Infect. 2007; 13(12):1186-91.
39. Youn S, Kabir M, Haque R, Petri Jr WA. Evaluation of a screening test for detection of Giardia and Cryptosporidium parasites. J Clin Microbiol. 2009; 47(2):451-2.
40. Chakarova B. Comparative evaluation of the diagnostic methods for detection of Giardia intestinalis in human fecal samples. Trakia J Sci. 2010; 8:174-79.
41. Al Saeed A, Issa S. Detection of Giardia lamblia antigen in stool specimens using enzyme-linked immunosorbent assay. East Mediterr Health J. 2010; 16(4):362-364.
42. Swierczewski B, Odundo E, Ndonye J, Kirera R, Odhiambo C, Oaks E. Comparison of the triage micro parasite panel and microscopy for the detection of Entamoeba histolytica/Entamoeba dispar, Giardia lamblia, and Cryptosporidium parvum in stool samples collected in Kenya. J Trop Med. 2012; 2012:564721.
43. Nguyen T, Kherouf H, Blanc-Pattin V, et al. Evaluation of an immunochromatographic assay: Giardia-Strip®(Coris BioConcept) for detection of Giardia intestinalis in human fecal specimens. Eur J Clin Microbiol Infect Dis. 2012; 31(4):623-5.
44. Goni P, Martin B, Villacampa M, et al. Evaluation of an immunochromatographic dip strip test for simultaneous detection of Cryptosporidium spp, Giardia duodenalis, and Entamoeba histolytica antigens in human faecal samples. Eur J Clin Microbiol Infect Dis. 2012; 31(8):2077-82.
45. Yagci S, Takmaz S, Eksi F, Balci I, Özen D. Diski Örneklerinde Giardia intestinalis' in Arastirilmasinda Direkt Mikroskopi, ELISA ve Direkt Floresan Antikor Yöntemlerinin Karsilastirilmasi/Comparison of Direct Microscopy, ELISA and Direct Fluorescent Antibody Methods for Detection of Giardia intestinalis in Human Fecal Specimens. Türkiye Klinikleri Tip Bilimleri Dergisi. 2013; 33:1308.
46. Elsafi SH, Al-Maqati TN, Hussein MI, Adam AA, Hassan MMA, Al Zahrani EM. Comparison of microscopy, rapid immunoassay, and molecular techniques for the detection of Giardia lamblia and Cryptosporidium parvum. Parasitol Res. 2013; 112(4):1641-6.
47. Jelinek T, Neifer S. Detection of Giardia lamblia stool samples: a comparison of two enzyme-linked immunosorbent assays. F1000Research. 2013; 2:39.
48. Kamel D, Farid A, Ali E, Rabia I, Hendawy M, Amir E. Diagnostic potential of target Giardia lamblia specific antigen for detection of human giardiasis using coproantigen sandwich ELISA. World J Med Sci. 2013; 9:113-22.
49. Alexander CL, Niebel M, Jones B. The rapid detection of Cryptosporidium and Giardia species in clinical stools using the Quik Chek immunoassay. Parasitol Int. 2013; 62(6):552-3.
50. Hawash Y. Evaluation of an immunoassay-based algorithm for screening and identification of Giardia and Cryptosporidium antigens in human faecal specimens from Saudi Arabia. J Parasitol Res. 2014; 2014:213745.
51. Moharm IM, El Enain G, Bahaa El Deen W, Mahgoub A, Hendawy M, Aly I. Evaluation of nano-gold beads based-ELISA for detection of Giardia lamblia antigen in stool samples of infected patients. Middle East J Sci Res. 2014; 21:2264-73.
52. Jahan N, Khatoon R, Ahmad S. A comparison of microscopy and enzyme linked immunosorbent assay for diagnosis of Giardia lamblia in human faecal specimens. J Clin Diagn Res. 2014; 8(11):DC04-06..
53. Van den Bossche D, Cnops L, Verschueren J, Van Esbroeck M. Comparison of four rapid diagnostic tests, ELISA, microscopy and PCR for the detection of Giardia lamblia , Cryptosporidium spp. and Entamoeba histolytica in feces. J Microbiol Methods. 2015; 110:78-84.
54. Selim MAE-W, Taha AAE-R, Abd El-Aal NF, Farag TI, Yousef AM. Detection of Giardia intestinalis coproantigens in diarrheic samples by immunochromatographic and ELISA techniques. J Egypt Soc Parasitol. 2015; 45(2):273-83.
55. Ghoshal U, Shukla R, Pant P, Ghoshal UC. Frequency, diagnostic performance of coproantigen detection and genotyping of the Giardia among patients referred to a multi-level teaching hospital in northern India. Pathog Glob Health. 2016; 110(7-8):316-20.
56. Bouyou-Akotet M, Owono-Medang M, Moussavou-Boussougou M, et al. Low sensitivity of the ImmunocardSTAT® Crypto/Giardia Rapid Assay test for the detection of Giardia and Cryptosporidium in fecal samples from children living in Libreville, Central Africa. J Parasit Dis. 2016; 40(4):1179-83.
57. Aly NS, Bayoumi I, Selem R, Kardoush M, Rashed G, Moharam A. A Novel Nano Magnetic Beads Dot ELISA Immunoassay and Its Application on the Detection of Giardia lamblia Coproantigen. Iran J Parasitol. 2018; 13(4):532-40.
58. Goudal A, Laude A, Valot S, et al. Rapid diagnostic tests relying on antigen detection from stool as an efficient point of care testing strategy for giardiasis and cryptosporidiosis? evaluation of a new immunochromatographic duplex assay. Diagn Microbiol Infect Dis. 2019; 93(1):33-6.
59. Mohram AF, Elawamy WE, Nageeb MM, Ali HS, Kishik SM. combined Mini-parasep Sf and nanogold immunoassay Show potential in Stool Antigen immunodetection for Giardiasis Diagnosis. Sci Rep. 2020; 10(1):2.
60. AboSheishaa GA. Efficacy of triage parasite panel in diagnosis of Entamoeba histolytica, Giardia lamblia , and Cryptosporidium parvum antigens in symptomatic children stool specimens. Egypt Vet Med Soc Parasitol J. 2021; 17:84-91.
61. Elmallawany MAI, Mousa A Mousa Attia, Samar S Ahmed, et al . Feasibility of a rapid lateral flow test for simultaneous detection of Giardia lamblia and Cryptosporidium parvum in duodenal aspirates of patients suffering from chronic liver diseases and eligible for upper endoscopy. J Egypt Soc Parasitol. 2021; 51:305-12.
62. El-Nahas HA, Salem DA, El-Henawy AA, El-Nimr HI, Abdel-Ghaffar HA, El-Meadawy AM. Giardia diagnostic methods in human fecal samples: a comparative study. Cytometry B Clin Cytom. 2013; 84(1):44-9.
63. Sarkari B, Khabisi SA. Immunodiagnosis of Human Fascioliasis: An Update of Concepts and Performances of the Serological Assays. J Clin Diagn Res. 2017; 11(6):OE05-OE10.
64. McHardy IH, Wu M, Shimizu-Cohen R, Couturier MR, Humphries RM. Detection of intestinal protozoa in the clinical laboratory. J Clin Microbiol. 2014;52(3):712-20.
65. Paulos S, Saugar JM, de Lucio A, Fuentes I, Mateo M, Carmena D. Comparative performance evaluation of four commercial multiplex real-time PCR assays for the detection of the diarrhoea-causing protozoa Cryptosporidium hominis/parvum, Giardia duodenalis and Entamoeba histolytica. PLoS One. 2019;14(4):e0215068.
66. Asghari A, Motazedian MH, Asgari Q, et al. Occurrence, genetic characterization, and zoonotic importance of Giardia duodenalis in various species of rodents (Mus musculus, Rattus norvegicus, and Rattus rattus). Comp Immunol Microbiol Infect Dis. 2022; 85:101812.
67. Sarkari B, Ashrafmansori A, Hatam GR, Motazedian MH, Asgari Q, Mohammadpour I. Genotyping of Giardia lamblia isolates from human in southern Iran. Trop Biomed. 2012; 29(3):366-71.
68. Sarkari B, Hosseini G, Motazedian MH, Fararouei M, Moshfe A. Prevalence and risk factors of intestinal protozoan infections: a population-based study in rural areas of Boyer-Ahmad district, Southwestern Iran. BMC Infect Dis. 2016; 16(1):703.
69. Seifollahi Z, Sarkari B, Motazedian MH, Asgari Q, Ranjbar MJ, Abdolahi Khabisi S. Protozoan Parasites of Rodents and Their Zoonotic Significance in Boyer-Ahmad District, Southwestern Iran. Vet Med Int. 2016; 2016:3263868.
70. Shafiei Z, Esfandiari F, Sarkari B, Rezaei Z, Fatahi MR, Hosseini Asl SMK. Parasitic infections in irritable bowel syndrome patients: evidence to propose a possible link, based on a case-control study in the south of Iran. BMC Res Notes. 2020; 13(1):264.
71. Fantinatti M, Gonçalves-Pinto M, Lopes-Oliveira LAP, Da-Cruz AM. Epidemiology of Giardia duodenalis assemblages in Brazil: there is still a long way to go. Mem Inst Oswaldo Cruz. 2021; 115:e200431.
72. Hijjawi N, Zahedi A, Al-Falah M, Ryan U. A review of the molecular epidemiology of Cryptosporidium spp. and Giardia duodenalis in the Middle East and North Africa (MENA) region. Infect Genet Evol. 2022; 98:105212.
2. Rogawski ET, Bartelt LA, Platts-Mills JA, S, et al. Determinants and impact of Giardia infection in the first 2 years of life in the MAL-ED birth cohort. J Pediatric Infect Dis Soc. 2017; 6(2):153-60.
3. Feng Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 2011; 24(1):110-40.
4. Bashir M, Farid A, Rabia I, et al. Serological versus antigen detection methods for Giardia duodenalis diagnosis. J Egypt Soc Parasitol. 2014; 44(3):709-18.
5. den Hartog J, Rosenbaum L, Wood Z, Burt D, Petri WA Jr. Diagnosis of multiple enteric protozoan infections by enzyme-linked immunosorbent assay in the Guatemalan highlands. Am J Trop Med Hyg. 2013; 88(1):167-71.
6. Sadaka H, Gaafar M, Mady R, Hezema N. Evaluation of ImmunoCard STAT test and ELISA versus light microscopy in diagnosis of giardiasis and cryptosporidiosis. Parasitol Res. 2015; 114(8):2853-63.
7. Singhal S, Mittal V, Khare V, Singh YI. Comparative analysis of enzyme-linked immunosorbent assay and direct microscopy for the diagnosis of Giardia intestinalis in fecal samples. Indian J Pathol Microbiol. 2015; 58(1):69-71.
8. Hiatt RA, Markell EK, Ng E. How many stool examinations are necessary to detect pathogenic intestinal protozoa? Am J Trop Med Hyg. 1995; 53(1):36-9.
9. Rosoff JD, Sanders CA, Sonnad SS, et al. Stool diagnosis of giardiasis using a commercially available enzyme immunoassay to detect Giardia-specific antigen 65 (GSA 65). J Clin Microbiol. 1989; 27(9):1997-2002.
10. Heyworth MF. Diagnostic testing for Giardia infections. Trans R Soc Trop Med Hyg. 2014; 108(3):123-5.
11. Vidal AMB, Catapani WR. Enzyme-linked immunosorbent assay (ELISA) imm-unoassaying versus microscopy: advantages and drawbacks for diagnosing giardiasis. Sao Paulo Med J. 2005; 123(6):282-5.
12. Christy NC, Hencke JD, Escueta-De Cadiz A, et al. Multisite performance evaluation of an enzyme-linked immunosorbent assay for detection of Giardia, Cryptosporidium, and Entamoeba histolytica antigens in human stool. J Clin Microbiol. 2012; 50(5):1762-3.
13. Silva RK, Pacheco FT, Martins AS,et al. Performance of microscopy and ELISA for diagnosing Giardia duodenalis infection in different pediatric groups. Parasitol Int. 2016;65(6 Pt A):635-640.
14. Uyar Y, Taylan Ozkan A. [Antigen detection methods in diagnosis of amebiasis, giardiasis and cryptosporidiosis]. Turkiye Parazitol Derg. 2009; 33(2):140-50.
15. Hooshyar H, Rostamkhani P, Arbabi M, Delavari M. Giardia lamblia infection: review of current diagnostic strategies. Gastroenterol Hepatol Bed Bench. 2019; 12(1):3-12.
16. Faubert G. Immune response to Giardia duodenalis. Clin Microbiol Rev. 2000;13(1):35-54.
17. Pacheco FTF, de Carvalho SS, Santos SA, et al. Specific IgG and IgA Antibody Reactivities in Sera of Children by Enzyme-Linked Immunoassay and Comparison With Giardia duodenalis Diagnosis in Feces. Ann Lab Med. 2020; 40(5):382-9.
18. Yılmaz A, Uslu H. Examination of Giardia intestinalis with Direct Microscopy and Direct Fluorescent Antibody in Patients with Diarrhea. Turkiye Parazitol Derg. 2020; 44(4):187-90.
19. Green E, Miles M, Warhurst D. Immunodiagnostic detection of Giardia antigen in faeces by a rapid visual enzyme-linked immunosorbent assay. Lancet. 1985; 2(8457):691-3.
20. Janoff E, Craft J, Pickering L, et al. Diagnosis of Giardia lamblia infections by detection of parasite-specific antigens. J Clin Microbiol. 1989; 27(3):431-5.
21. Knisley CV, Engelkirk PG, Pickering LK, et al. Rapid detection of Giardia antigen in stool with the use of enzyme immunoassays. Am J Clin Pathol. 1989; 91(6):704-8.
22. Schieven B, Hussain Z. Evaluation of an enzyme-immunoassay test kit for diagnosing infections with Giardia lamblia. Serodiag Immunother Infec Dis. 1990; 4:109-13.
23. Vidal M, Gilman R, Ungar B, et al. Detection of Giardia lamblia antigen in children living in a Peruvian periurban shantytown (Pueblo Joven). J Clin Microbiol. 1991; 29(3):636-7.
24. Goldin A, Apt Baruch W, Aguilera X, et al. A capture ELISA detects Giardia lamblia antigens in formalin-treated faecal samples. Trans R Soc Trop Med Hyg. 1992; 86:164-5
25. G arcia LS, Shimizu RY. Evaluation of nine immunoassay kits (enzyme immunoassay and direct fluorescence) for detection of Giardia lamblia and Cryptosporidium parvum in human fecal specimens. J Clin Microbiol. 1997; 35(6):1526-9.
26. Behr MA, Kokoskin E, Gyorkos TW, Cédilotte L, Faubert GM, MacLean JD. Laboratory diagnosis for Giardia lamblia infection: a comparison of microscopy, coprodiagnosis and serology. Can J Infect Dis. 1997; 8(1):33-8.
27. Aldeen WE, Carroll K, Robison A, Morrison M, Hale D. Comparison of nine commercially available enzyme-linked immunosorbent assays for detection of Giardia lamblia in fecal specimens. J Clin Microbiol. 1998; 36(5):1338-40.
28. Rocha MO, Guimarães TM, Toledo VT, et al. Detection of a Giardia lamblia coproantigen by using a commercially available imm-unoenzymatic assay, in Belo Horizonte, Brazil. Rev Inst Med Trop Sao Paulo. 1999; 41(3):151-4.
29. Chan R, Chen J, York MK, et al. Evaluation of a combination rapid immunoassay for detection of Giardia and Cryptosporidium antigens. J Clin Microbiol. 2000; 38(1):393-4.
30. Maraha B, Buiting A. Evaluation of four enzyme immunoassays for the detection of Giardia lamblia antigen in stool specimens. Eur J Clin Microbiol Infect Dis. 2000; 19(6):485-7.
31. Hanson KL, Cartwright CP. Use of an enzyme immunoassay does not eliminate the need to analyze multiple stool specimens for sensitive detection of Giardia lamblia. J Clin Microbiol. 2001; 39(2):474-7.
32. Schunk M, Jelinek T, Wetzel K, Nothdurft HD. Detection of Giardia lamblia and Entamoeba histolytica in stool samples by two enzyme immunoassays. Eur J Clin Microbiol Infect Dis. 2001; 20(6):389-91.
33. Duque-Beltrán S, Nicholls-Orejuela RS, Arévalo-Jamaica A, Guerrero-Lozano R, Montenegro S, James MA. Detection of Giardia duodenalis antigen in human fecal eluates by enzyme-linked immunosorbent assay using polyclonal antibodies. Mem Inst Oswaldo Cruz. 2002; 97(8):1165-8.
34. Garcia LS, Shimizu RY, Novak S, Carroll M, Chan F. Commercial assay for detection of Giardia lamblia and Cryptosporidium parvum antigens in human fecal specimens by rapid solid-phase qualitative immunochromatog-raphy. J Clin Microbiol. 2003; 41(1):209-12.
35. Johnston SP, Ballard MM, Beach MJ, Causer L, Wilkins PP. Evaluation of three commercial assays for detection of Giardia and Cryptosporidium organisms in fecal specimens. J Clin Microbiol. 2003; 41(2):623-6.
36. Garcia LS, Garcia JP. Detection of Giardia lamblia antigens in human fecal specimens by a solid-phase qualitative immunochromato-graphic assay. J Clin Microbiol. 2006; 44(12):4587-8.
37. Weitzel T, Dittrich S, Möhl I, Adusu E, Jelinek T. Evaluation of seven commercial antigen detection tests for Giardia and Cryptosporidium in stool samples. Clin Microbiol Infect. 2006; 12(7):656-9.
38. Schuurman T, Lankamp P, van Belkum A, Kooistra-Smid M, Van Zwet A. Comparison of microscopy, real-time PCR and a rapid immunoassay for the detection of Giardia lamblia in human stool specimens. Clin Microbiol Infect. 2007; 13(12):1186-91.
39. Youn S, Kabir M, Haque R, Petri Jr WA. Evaluation of a screening test for detection of Giardia and Cryptosporidium parasites. J Clin Microbiol. 2009; 47(2):451-2.
40. Chakarova B. Comparative evaluation of the diagnostic methods for detection of Giardia intestinalis in human fecal samples. Trakia J Sci. 2010; 8:174-79.
41. Al Saeed A, Issa S. Detection of Giardia lamblia antigen in stool specimens using enzyme-linked immunosorbent assay. East Mediterr Health J. 2010; 16(4):362-364.
42. Swierczewski B, Odundo E, Ndonye J, Kirera R, Odhiambo C, Oaks E. Comparison of the triage micro parasite panel and microscopy for the detection of Entamoeba histolytica/Entamoeba dispar, Giardia lamblia, and Cryptosporidium parvum in stool samples collected in Kenya. J Trop Med. 2012; 2012:564721.
43. Nguyen T, Kherouf H, Blanc-Pattin V, et al. Evaluation of an immunochromatographic assay: Giardia-Strip®(Coris BioConcept) for detection of Giardia intestinalis in human fecal specimens. Eur J Clin Microbiol Infect Dis. 2012; 31(4):623-5.
44. Goni P, Martin B, Villacampa M, et al. Evaluation of an immunochromatographic dip strip test for simultaneous detection of Cryptosporidium spp, Giardia duodenalis, and Entamoeba histolytica antigens in human faecal samples. Eur J Clin Microbiol Infect Dis. 2012; 31(8):2077-82.
45. Yagci S, Takmaz S, Eksi F, Balci I, Özen D. Diski Örneklerinde Giardia intestinalis' in Arastirilmasinda Direkt Mikroskopi, ELISA ve Direkt Floresan Antikor Yöntemlerinin Karsilastirilmasi/Comparison of Direct Microscopy, ELISA and Direct Fluorescent Antibody Methods for Detection of Giardia intestinalis in Human Fecal Specimens. Türkiye Klinikleri Tip Bilimleri Dergisi. 2013; 33:1308.
46. Elsafi SH, Al-Maqati TN, Hussein MI, Adam AA, Hassan MMA, Al Zahrani EM. Comparison of microscopy, rapid immunoassay, and molecular techniques for the detection of Giardia lamblia and Cryptosporidium parvum. Parasitol Res. 2013; 112(4):1641-6.
47. Jelinek T, Neifer S. Detection of Giardia lamblia stool samples: a comparison of two enzyme-linked immunosorbent assays. F1000Research. 2013; 2:39.
48. Kamel D, Farid A, Ali E, Rabia I, Hendawy M, Amir E. Diagnostic potential of target Giardia lamblia specific antigen for detection of human giardiasis using coproantigen sandwich ELISA. World J Med Sci. 2013; 9:113-22.
49. Alexander CL, Niebel M, Jones B. The rapid detection of Cryptosporidium and Giardia species in clinical stools using the Quik Chek immunoassay. Parasitol Int. 2013; 62(6):552-3.
50. Hawash Y. Evaluation of an immunoassay-based algorithm for screening and identification of Giardia and Cryptosporidium antigens in human faecal specimens from Saudi Arabia. J Parasitol Res. 2014; 2014:213745.
51. Moharm IM, El Enain G, Bahaa El Deen W, Mahgoub A, Hendawy M, Aly I. Evaluation of nano-gold beads based-ELISA for detection of Giardia lamblia antigen in stool samples of infected patients. Middle East J Sci Res. 2014; 21:2264-73.
52. Jahan N, Khatoon R, Ahmad S. A comparison of microscopy and enzyme linked immunosorbent assay for diagnosis of Giardia lamblia in human faecal specimens. J Clin Diagn Res. 2014; 8(11):DC04-06..
53. Van den Bossche D, Cnops L, Verschueren J, Van Esbroeck M. Comparison of four rapid diagnostic tests, ELISA, microscopy and PCR for the detection of Giardia lamblia , Cryptosporidium spp. and Entamoeba histolytica in feces. J Microbiol Methods. 2015; 110:78-84.
54. Selim MAE-W, Taha AAE-R, Abd El-Aal NF, Farag TI, Yousef AM. Detection of Giardia intestinalis coproantigens in diarrheic samples by immunochromatographic and ELISA techniques. J Egypt Soc Parasitol. 2015; 45(2):273-83.
55. Ghoshal U, Shukla R, Pant P, Ghoshal UC. Frequency, diagnostic performance of coproantigen detection and genotyping of the Giardia among patients referred to a multi-level teaching hospital in northern India. Pathog Glob Health. 2016; 110(7-8):316-20.
56. Bouyou-Akotet M, Owono-Medang M, Moussavou-Boussougou M, et al. Low sensitivity of the ImmunocardSTAT® Crypto/Giardia Rapid Assay test for the detection of Giardia and Cryptosporidium in fecal samples from children living in Libreville, Central Africa. J Parasit Dis. 2016; 40(4):1179-83.
57. Aly NS, Bayoumi I, Selem R, Kardoush M, Rashed G, Moharam A. A Novel Nano Magnetic Beads Dot ELISA Immunoassay and Its Application on the Detection of Giardia lamblia Coproantigen. Iran J Parasitol. 2018; 13(4):532-40.
58. Goudal A, Laude A, Valot S, et al. Rapid diagnostic tests relying on antigen detection from stool as an efficient point of care testing strategy for giardiasis and cryptosporidiosis? evaluation of a new immunochromatographic duplex assay. Diagn Microbiol Infect Dis. 2019; 93(1):33-6.
59. Mohram AF, Elawamy WE, Nageeb MM, Ali HS, Kishik SM. combined Mini-parasep Sf and nanogold immunoassay Show potential in Stool Antigen immunodetection for Giardiasis Diagnosis. Sci Rep. 2020; 10(1):2.
60. AboSheishaa GA. Efficacy of triage parasite panel in diagnosis of Entamoeba histolytica, Giardia lamblia , and Cryptosporidium parvum antigens in symptomatic children stool specimens. Egypt Vet Med Soc Parasitol J. 2021; 17:84-91.
61. Elmallawany MAI, Mousa A Mousa Attia, Samar S Ahmed, et al . Feasibility of a rapid lateral flow test for simultaneous detection of Giardia lamblia and Cryptosporidium parvum in duodenal aspirates of patients suffering from chronic liver diseases and eligible for upper endoscopy. J Egypt Soc Parasitol. 2021; 51:305-12.
62. El-Nahas HA, Salem DA, El-Henawy AA, El-Nimr HI, Abdel-Ghaffar HA, El-Meadawy AM. Giardia diagnostic methods in human fecal samples: a comparative study. Cytometry B Clin Cytom. 2013; 84(1):44-9.
63. Sarkari B, Khabisi SA. Immunodiagnosis of Human Fascioliasis: An Update of Concepts and Performances of the Serological Assays. J Clin Diagn Res. 2017; 11(6):OE05-OE10.
64. McHardy IH, Wu M, Shimizu-Cohen R, Couturier MR, Humphries RM. Detection of intestinal protozoa in the clinical laboratory. J Clin Microbiol. 2014;52(3):712-20.
65. Paulos S, Saugar JM, de Lucio A, Fuentes I, Mateo M, Carmena D. Comparative performance evaluation of four commercial multiplex real-time PCR assays for the detection of the diarrhoea-causing protozoa Cryptosporidium hominis/parvum, Giardia duodenalis and Entamoeba histolytica. PLoS One. 2019;14(4):e0215068.
66. Asghari A, Motazedian MH, Asgari Q, et al. Occurrence, genetic characterization, and zoonotic importance of Giardia duodenalis in various species of rodents (Mus musculus, Rattus norvegicus, and Rattus rattus). Comp Immunol Microbiol Infect Dis. 2022; 85:101812.
67. Sarkari B, Ashrafmansori A, Hatam GR, Motazedian MH, Asgari Q, Mohammadpour I. Genotyping of Giardia lamblia isolates from human in southern Iran. Trop Biomed. 2012; 29(3):366-71.
68. Sarkari B, Hosseini G, Motazedian MH, Fararouei M, Moshfe A. Prevalence and risk factors of intestinal protozoan infections: a population-based study in rural areas of Boyer-Ahmad district, Southwestern Iran. BMC Infect Dis. 2016; 16(1):703.
69. Seifollahi Z, Sarkari B, Motazedian MH, Asgari Q, Ranjbar MJ, Abdolahi Khabisi S. Protozoan Parasites of Rodents and Their Zoonotic Significance in Boyer-Ahmad District, Southwestern Iran. Vet Med Int. 2016; 2016:3263868.
70. Shafiei Z, Esfandiari F, Sarkari B, Rezaei Z, Fatahi MR, Hosseini Asl SMK. Parasitic infections in irritable bowel syndrome patients: evidence to propose a possible link, based on a case-control study in the south of Iran. BMC Res Notes. 2020; 13(1):264.
71. Fantinatti M, Gonçalves-Pinto M, Lopes-Oliveira LAP, Da-Cruz AM. Epidemiology of Giardia duodenalis assemblages in Brazil: there is still a long way to go. Mem Inst Oswaldo Cruz. 2021; 115:e200431.
72. Hijjawi N, Zahedi A, Al-Falah M, Ryan U. A review of the molecular epidemiology of Cryptosporidium spp. and Giardia duodenalis in the Middle East and North Africa (MENA) region. Infect Genet Evol. 2022; 98:105212.
| Files | ||
| Issue | Vol 18 No 2 (2023) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v18i2.13180 | |
| Keywords | ||
| Giardiasis Diagnosis Antigen-based Meta-analysis | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Pouryousef A, Fararooei M, Sarkari B. Antigen-Based Diagnosis of Human Giardiasis: A Systematic Review and Meta-Analysis. Iran J Parasitol. 2023;18(2):140-154.
