Comparison of Native Hydatid Cyst Fluid (HCF), Lyophilized HCF, Antigen B (AgB) and Lyophilized AgB (LAgB) Originated from Echinococcus granulosus Sensu Stricto for Sero-Diagnosis of Active, Transitional and Inactive Human Liver Cystic Echinococcosis
-
Fatemeh Sadat Sadjjadi
,
Tahereh Mohammadzadeh
,
Seyed Hamed Jafari
,
Yosef Sharifi
,
Hamed Nikoupour Dailami
,
Fatemeh Hafezi
,
Seyed Mahmoud Sadjjadi
Abstract
Background: Cystic echinococcosis (CE) is an important zoonotic parasitic disease caused by the larval stage or metacestode of the tapeworm Echinococcus granulosus sensu lato. Due to treatment protocols for different liver cysts, diagnosis of cyst stages is very important. Different antigens have been used for CE diagnosis. However, each one is more sensitive and effective for the diagnosis of specific CE stages is not known well. We aimed to compare Native Hydatid Cyst Fluid (HCF), Lyophilized Hydatid Cyst Fluid (LHCF), antigen B (AgB) and Lyophilized antigen B (LAgB) originated from E. granulosus sensu stricto (G1-G3) genotype, for sero- diagnosis of active, transitional and inactive human liver CE using ELISA technique.
Methods: The HCF was collected aseptically from liver CE cysts of sheep slaughtered from 2018 to 2019 in Shiraz slaughterhouse, Southern, Iran. The cysts were characterized by PCR and sequencing for genotype specification. Four types of antigens were used: HCF, LHCF, AgB and LAgB originated from E. granulosus sensu stricto (G1-G3) genotype. Thirty-three serum samples from active, transitional, and inactive human cysts were collected. Overall, 48 samples from other parasitic diseases and 60 samples from healthy subjects as negative controls were checked using four antigens by ELISA method.
Results: The best diagnostic sensitivity with 96.97% was observed by anti-LHCF IgG ELISA test. The best specificity with 95.37% was observed in ELISA test using LAgB.
Conclusion: Simultaneous test of sera with anti-LHCF IgG ELISA and anti-LAgB IgG ELISA would be the best in the diagnosis of human liver cystic echinococcosis.
1. Thompson A, Deplazes P, Lymbery A (2017). Preface. Adv Parasitol, 95: xiii-xiv.
2. Rokni MB (2009). Echinococ-cosis/hydatidosis in Iran. Iran J Parasitol, 4 (2): 1–16.
3. Sadjjadi SM (2006). Present situation of echinococcosis in the Middle East and Arabic North Africa. Parasitol Int, 55: 197–202.
4. Sadjjadi SM, Ardehali S, Noman-Pour B, et al (2001). Diagnosis of cystic echinococ-cosis: ultrasound imaging or countercur-rent immunoelectrophoresis? East Medi-terr Health J, 7 (6): 907–11.
5. Brunetti E, Kern P, Vuitton DA (2010). Writing Panel for the WHO-IWGE. Ex-pert consensus for the diagnosis and treatment of cystic and alveolar echino-coccosis in humans. Acta Trop, 114 (1): 1–16.
6. Turgut AT, Akhan O, Bhatt S, et al (2008). Sonographic spectrum of hydatid dis-ease. Ultrasound Q, 24 (1): 17–29.
7. WHO Informal Working Group (2003). In-ternational classification of ultrasound images in cystic echinococcosis for ap-plication in clinical and field epidemio-logical settings. Acta Trop, 85 (2): 253–61.
8. Tamarozzi F, Akhan O, Cretu CM, et al (2019). Epidemiological factors associat-ed with human cystic echinococcosis: a semi-structured questionnaire from a large population-based ultrasound cross-sectional study in Eastern Europe and Turkey. Parasit Vectors, 12 (1): 371.
9. Brunetti E, Tamarozzi F, Macpherson C, et al (2018). Ultrasound and cystic echino-coccosis. Ultrasound Int Open, 4(3): E70–E78.
10. Rinaldi F, Brunetti E, Neumayr A, et al (2014). Cystic echinococcosis of the liv-er: A primer for hepatologists. World J Hepatol, 6 (5): 293–305.
11. Tamarozzi F, Nicoletti GJ, Neumayr A, et al (2014). Acceptance of standardized ul-trasound classification, use of albend-azole, and long-term follow-up in clini-cal management of cystic echinococ-cosis: a systematic review. Curr Opin Infect Dis, 27 (5): 425–31.
12. Junghanss T, da Silva AM, Horton J, et al (2008). Clinical management of cystic echinococcosis: state of the art, prob-lems, and perspectives. Am J Trop Med Hyg, 79 (3): 301–11.
13. Mihmanli M, Idiz UO, Kaya C, et al (2016). Current status of diagnosis and treat-ment of hepatic echinococcosis. World J Hepatol, 8 (28): 1169–1181.
14. Tamarozzi F, Silva R, Fittipaldo VA, et al (2021). Serology for the diagnosis of human hepatic cystic echinococcosis and its relation with cyst staging: A sys-tematic review of the literature with me-ta-analysis. PLoS Negl Trop Dis, 15 (4): e0009370.
15. González-Sapienza G, Lorenzo C, Nieto A (2000). Improved immunodiagnosis of cystic hydatid disease by using a synthet-ic peptide with higher diagnostic value than that of its parent protein, Echino-coccus granulosus antigen B. J Clin Mi-crobiol, 38 (11): 3979–83.
16. Piccoli L, Tamarozzi F, Cattaneo F, et al (2014). Long-term sonographic and sero-logical follow-up of inactive echinococ-cal cysts of the liver: hints for a “watch-and-wait” approach. PLoS Negl Trop Dis, 8 (8): e3057.
17. Sadjjadi SM, Abidi H, Sarkari B, et al (2007). Evaluation of enzyme linked immuno-sorbent assay, utilizing native antigen B for serodiagnosis of human hydatidosis. Iran J Immunol, 4 (3): 167–72.
18. Virginio VG, Hernández A, Rott MB, et al (2003). A set of recombinant antigens from Echinococcus granulosus with potential for use in the immunodiagnosis of hu-man cystic hydatid disease. Clin Exp Immunol, 132 (2): 309–15.
19. Carmena D, Benito A, Eraso E (2006). An-tigens for the immunodiagnosis of Echi-nococcus granulosus infection: An update. Acta Trop, 98 (1): 74–86.
20. Sadjjadi SF, Mohammadzadeh T, Hafezi F, et al (2022) Evaluation of the Ability of Antigen B Originated from Echinococcus granulosus Sensu Stricto and E. canadensis for the Diagnosis of Confirmed Human Cystic Echinococcosis Using ELISA. Iran J Parasitol, 17(3):358-65.
21. Pagnozzi D, Biosa G, Addis MF, et al (2014). An easy and efficient method for native and immunoreactive Echinococcus granulosus antigen 5 enrichment from hydatid cyst fluid. PLoS One, 9 (8): e104962.
22. Verastegui M, Moro P, Guevara A, et al (1992). Enzyme-linked immunoelectro-transfer blot test for diagnosis of human hydatid disease. J Clin Microbiol, 30 (6): 1557-61.
23. Oriol R, Williams JF, Pérez Esandi MV, et al (1971). Purification of lipoprotein an-tigens of Echinococcus granulosus from sheep hydatid fluid. Am J Trop Med Hyg, 20 (4): 569–74.
24. Bradford MM (1976). A rapid and sensitive method for the quantitation of mi-crogram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem, 72 (1-2): 248–54.
25. Sadjjadi FS, Ahmadi N, Rezaie-Tavirani M, et al (2021). Following up of Surgical Treated Human Liver Cystic Echino-coccosis: A Proteomics Approach. Iran J Parasitol. 16(1):11-22.
26. Haniloo A, Massoud J, Rokni MB (2005). Evaluation and comparison of antigen B-ELISA and antigen B-immunoblotting in immunodiagnosis of cystic hydatid disease. Pak J Med Sci, 21 (3): 352-356.
27. Khalilpour A, Sadjjadi SM, Kazemi-Moghadam Z, et al (2014). Lateral flow test using Echinococcus granulosus native an-tigen B and comparison of IgG and IgG4 dipsticks for detection of human cystic echinococcosis. Am J Trop Med Hyg, 91 (5): 994–999.
28. Zibaei M, Azargoon A, Ataie-Khorasgani M, et al (2013). The serological study of cystic echinococcosis and assessment of surgical cases during 5 years (2007-2011) in Khorram Abad, Iran. Niger J Clin Pract, 16 (2): 221-5.
29. Mamuti W, Sako Y, Nakao M, et al (2006). Recent advances in characterization of Echinococcus antigen B. Parasitol Int, 55 Suppl:S57-62.
30. Rokni MB, Lesan S, Massoud J, et al (2006). Comparative evaluation of Fast enzyme linked immunosorbent assay (FastELI-SA) and standard-ELISA for the diagno-sis of human hydatidosis. Iran J Public Health, 35 (2): 29-32.
31. Asghari M, Mohebali M, Kia EB, et al (2013). Seroepidemiology of Human Hydatidosis Using AgB-ELISA Test in Arak, Central Iran. Iran J Public Health, 42(9): 391-396.
32. Dabaghzadeh H, Bairami A, Kia EB, et al (2018). Seroprevalence of human cystic echinococcosis in Alborz Province, Central Iran in 2015. Iran J Public Health, 47: 561-566.
33. Darabi E, Motevaseli E, Khorramizadeh MR, et al (2019). Design and Construc-tion of a Fusion Peptide Containing B1, B2, B4, and EPC1 Epitopes for Diagno-sis of Human Cystic Echinococcosis. Iran J Public Health, 48 (9): 1671-1680.
34. Hafezi F, Mohammadzadeh T, Pazoki R, et al (2022). Sero-Epidemiological Study of Human Hydatidosis in Semnan and Sorkheh, Semnan Province, Iran. Iran J Public Health, 51 (6): 1411-1418.
35. Mohammadzadeh T, Sako Y, Sadjjadi SM, et al (2012). Comparison of the useful-ness of hydatid cyst fluid, native antigen B and recombinant antigen B8/1 for se-rological diagnosis of cystic echinococ-cosis. Trans R Soc Trop Med Hyg, 106 (6): 371–5.
36. Sbihi Y, Rmiqui A, Rodriguez-Cabezas MN, et al (2001). Comparative sensitivity of six serological tests and diagnostic value of ELISA using purified antigen in hyda-tidosis. J Clin Lab Anal, 15 (1): 14–8.
37. Nasrieh MA, Abdel-Hafez SK (2004). Echi-nococcus granulosus in Jordan: assess-ment of various antigenic preparations for use in the serodiagnosis of surgically confirmed cases using enzyme immuno assays and the indirect haemagglutina-tion test. Diagn Microbiol Infect Dis, 48 (2): 117–23.
38. Tawfeek GM, Elwakil HS, Awad NS, et al (2009). Genetic variability of antigen B among Echinococcus granulosus Egyp-tian isolates. Korean J Parasitol, 47 (3): 259–64.
39. Siles-Lucas M, Casulli A, Conraths FJ, et al (2017). Laboratory diagnosis of Echino-coccus spp. in human patients and in-fected animals. Adv Parasitol, 96: 159–257.
40. Manzano-Román R, Sánchez-Ovejero C, Hernández-González A, et al (2015). Se-rological diagnosis and follow-up of human cystic echinococcosis: A new hope for the future? Biomed Res Int, 2015:428205.
2. Rokni MB (2009). Echinococ-cosis/hydatidosis in Iran. Iran J Parasitol, 4 (2): 1–16.
3. Sadjjadi SM (2006). Present situation of echinococcosis in the Middle East and Arabic North Africa. Parasitol Int, 55: 197–202.
4. Sadjjadi SM, Ardehali S, Noman-Pour B, et al (2001). Diagnosis of cystic echinococ-cosis: ultrasound imaging or countercur-rent immunoelectrophoresis? East Medi-terr Health J, 7 (6): 907–11.
5. Brunetti E, Kern P, Vuitton DA (2010). Writing Panel for the WHO-IWGE. Ex-pert consensus for the diagnosis and treatment of cystic and alveolar echino-coccosis in humans. Acta Trop, 114 (1): 1–16.
6. Turgut AT, Akhan O, Bhatt S, et al (2008). Sonographic spectrum of hydatid dis-ease. Ultrasound Q, 24 (1): 17–29.
7. WHO Informal Working Group (2003). In-ternational classification of ultrasound images in cystic echinococcosis for ap-plication in clinical and field epidemio-logical settings. Acta Trop, 85 (2): 253–61.
8. Tamarozzi F, Akhan O, Cretu CM, et al (2019). Epidemiological factors associat-ed with human cystic echinococcosis: a semi-structured questionnaire from a large population-based ultrasound cross-sectional study in Eastern Europe and Turkey. Parasit Vectors, 12 (1): 371.
9. Brunetti E, Tamarozzi F, Macpherson C, et al (2018). Ultrasound and cystic echino-coccosis. Ultrasound Int Open, 4(3): E70–E78.
10. Rinaldi F, Brunetti E, Neumayr A, et al (2014). Cystic echinococcosis of the liv-er: A primer for hepatologists. World J Hepatol, 6 (5): 293–305.
11. Tamarozzi F, Nicoletti GJ, Neumayr A, et al (2014). Acceptance of standardized ul-trasound classification, use of albend-azole, and long-term follow-up in clini-cal management of cystic echinococ-cosis: a systematic review. Curr Opin Infect Dis, 27 (5): 425–31.
12. Junghanss T, da Silva AM, Horton J, et al (2008). Clinical management of cystic echinococcosis: state of the art, prob-lems, and perspectives. Am J Trop Med Hyg, 79 (3): 301–11.
13. Mihmanli M, Idiz UO, Kaya C, et al (2016). Current status of diagnosis and treat-ment of hepatic echinococcosis. World J Hepatol, 8 (28): 1169–1181.
14. Tamarozzi F, Silva R, Fittipaldo VA, et al (2021). Serology for the diagnosis of human hepatic cystic echinococcosis and its relation with cyst staging: A sys-tematic review of the literature with me-ta-analysis. PLoS Negl Trop Dis, 15 (4): e0009370.
15. González-Sapienza G, Lorenzo C, Nieto A (2000). Improved immunodiagnosis of cystic hydatid disease by using a synthet-ic peptide with higher diagnostic value than that of its parent protein, Echino-coccus granulosus antigen B. J Clin Mi-crobiol, 38 (11): 3979–83.
16. Piccoli L, Tamarozzi F, Cattaneo F, et al (2014). Long-term sonographic and sero-logical follow-up of inactive echinococ-cal cysts of the liver: hints for a “watch-and-wait” approach. PLoS Negl Trop Dis, 8 (8): e3057.
17. Sadjjadi SM, Abidi H, Sarkari B, et al (2007). Evaluation of enzyme linked immuno-sorbent assay, utilizing native antigen B for serodiagnosis of human hydatidosis. Iran J Immunol, 4 (3): 167–72.
18. Virginio VG, Hernández A, Rott MB, et al (2003). A set of recombinant antigens from Echinococcus granulosus with potential for use in the immunodiagnosis of hu-man cystic hydatid disease. Clin Exp Immunol, 132 (2): 309–15.
19. Carmena D, Benito A, Eraso E (2006). An-tigens for the immunodiagnosis of Echi-nococcus granulosus infection: An update. Acta Trop, 98 (1): 74–86.
20. Sadjjadi SF, Mohammadzadeh T, Hafezi F, et al (2022) Evaluation of the Ability of Antigen B Originated from Echinococcus granulosus Sensu Stricto and E. canadensis for the Diagnosis of Confirmed Human Cystic Echinococcosis Using ELISA. Iran J Parasitol, 17(3):358-65.
21. Pagnozzi D, Biosa G, Addis MF, et al (2014). An easy and efficient method for native and immunoreactive Echinococcus granulosus antigen 5 enrichment from hydatid cyst fluid. PLoS One, 9 (8): e104962.
22. Verastegui M, Moro P, Guevara A, et al (1992). Enzyme-linked immunoelectro-transfer blot test for diagnosis of human hydatid disease. J Clin Microbiol, 30 (6): 1557-61.
23. Oriol R, Williams JF, Pérez Esandi MV, et al (1971). Purification of lipoprotein an-tigens of Echinococcus granulosus from sheep hydatid fluid. Am J Trop Med Hyg, 20 (4): 569–74.
24. Bradford MM (1976). A rapid and sensitive method for the quantitation of mi-crogram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem, 72 (1-2): 248–54.
25. Sadjjadi FS, Ahmadi N, Rezaie-Tavirani M, et al (2021). Following up of Surgical Treated Human Liver Cystic Echino-coccosis: A Proteomics Approach. Iran J Parasitol. 16(1):11-22.
26. Haniloo A, Massoud J, Rokni MB (2005). Evaluation and comparison of antigen B-ELISA and antigen B-immunoblotting in immunodiagnosis of cystic hydatid disease. Pak J Med Sci, 21 (3): 352-356.
27. Khalilpour A, Sadjjadi SM, Kazemi-Moghadam Z, et al (2014). Lateral flow test using Echinococcus granulosus native an-tigen B and comparison of IgG and IgG4 dipsticks for detection of human cystic echinococcosis. Am J Trop Med Hyg, 91 (5): 994–999.
28. Zibaei M, Azargoon A, Ataie-Khorasgani M, et al (2013). The serological study of cystic echinococcosis and assessment of surgical cases during 5 years (2007-2011) in Khorram Abad, Iran. Niger J Clin Pract, 16 (2): 221-5.
29. Mamuti W, Sako Y, Nakao M, et al (2006). Recent advances in characterization of Echinococcus antigen B. Parasitol Int, 55 Suppl:S57-62.
30. Rokni MB, Lesan S, Massoud J, et al (2006). Comparative evaluation of Fast enzyme linked immunosorbent assay (FastELI-SA) and standard-ELISA for the diagno-sis of human hydatidosis. Iran J Public Health, 35 (2): 29-32.
31. Asghari M, Mohebali M, Kia EB, et al (2013). Seroepidemiology of Human Hydatidosis Using AgB-ELISA Test in Arak, Central Iran. Iran J Public Health, 42(9): 391-396.
32. Dabaghzadeh H, Bairami A, Kia EB, et al (2018). Seroprevalence of human cystic echinococcosis in Alborz Province, Central Iran in 2015. Iran J Public Health, 47: 561-566.
33. Darabi E, Motevaseli E, Khorramizadeh MR, et al (2019). Design and Construc-tion of a Fusion Peptide Containing B1, B2, B4, and EPC1 Epitopes for Diagno-sis of Human Cystic Echinococcosis. Iran J Public Health, 48 (9): 1671-1680.
34. Hafezi F, Mohammadzadeh T, Pazoki R, et al (2022). Sero-Epidemiological Study of Human Hydatidosis in Semnan and Sorkheh, Semnan Province, Iran. Iran J Public Health, 51 (6): 1411-1418.
35. Mohammadzadeh T, Sako Y, Sadjjadi SM, et al (2012). Comparison of the useful-ness of hydatid cyst fluid, native antigen B and recombinant antigen B8/1 for se-rological diagnosis of cystic echinococ-cosis. Trans R Soc Trop Med Hyg, 106 (6): 371–5.
36. Sbihi Y, Rmiqui A, Rodriguez-Cabezas MN, et al (2001). Comparative sensitivity of six serological tests and diagnostic value of ELISA using purified antigen in hyda-tidosis. J Clin Lab Anal, 15 (1): 14–8.
37. Nasrieh MA, Abdel-Hafez SK (2004). Echi-nococcus granulosus in Jordan: assess-ment of various antigenic preparations for use in the serodiagnosis of surgically confirmed cases using enzyme immuno assays and the indirect haemagglutina-tion test. Diagn Microbiol Infect Dis, 48 (2): 117–23.
38. Tawfeek GM, Elwakil HS, Awad NS, et al (2009). Genetic variability of antigen B among Echinococcus granulosus Egyp-tian isolates. Korean J Parasitol, 47 (3): 259–64.
39. Siles-Lucas M, Casulli A, Conraths FJ, et al (2017). Laboratory diagnosis of Echino-coccus spp. in human patients and in-fected animals. Adv Parasitol, 96: 159–257.
40. Manzano-Román R, Sánchez-Ovejero C, Hernández-González A, et al (2015). Se-rological diagnosis and follow-up of human cystic echinococcosis: A new hope for the future? Biomed Res Int, 2015:428205.
| Files | ||
| Issue | Vol 52 No 8 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v52i8.13416 | |
| Keywords | ||
| Cystic echinococcosis Ultrasonography Echinococcus granulosus Antigens Human | ||
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How to Cite
1.
Sadjjadi FS, Mohammadzadeh T, Jafari SH, Sharifi Y, Nikoupour Dailami H, Hafezi F, Sadjjadi SM. Comparison of Native Hydatid Cyst Fluid (HCF), Lyophilized HCF, Antigen B (AgB) and Lyophilized AgB (LAgB) Originated from Echinococcus granulosus Sensu Stricto for Sero-Diagnosis of Active, Transitional and Inactive Human Liver Cystic Echinococcosis. Iran J Public Health. 2023;52(8):1764-1772.
