Serological Comparison of Native Antigen ELISAs with Rapid ICT Test Kits for the Diagnosis of Human Alveolar and Cystic Echinococcosis in China
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethical Approval
2.2. Study Subjects
2.2.1. Individuals with a Clinical History of Echinococcosis
2.2.2. Community Survey of Children and Teenagers
2.3. Serological Tests
2.3.1. Native Antigen ELISAs
2.3.2. ADAMU-AE and CE Test Kits
2.4. Statistical Analysis
3. Results
3.1. Studied Subjects
3.1.1. Clinical Diagnosed Cases
3.1.2. Community Survey Individuals
3.2. Serological Outcomes
3.2.1. Results of Subjects with a Clinical History of Echinococcosis
3.2.2. Community Survey of Children and Teenagers
3.2.3. Consistency between Imaging Outcomes and the Two Serological Methods
3.2.4. The Sensitivity/Specificity and Level of Cross-Reactivity of the Two Serological Methods
3.2.5. Association between CE and AE Imaging Classification and the Two Serological Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Brunetti, E.; Kern, P.; Vuitton, D.A. Writing Panel for the WHO-IWGE Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop 2010, 114, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Fu, M.H.; Wang, X.; Han, S.; Guan, Y.Y.; Bergquist, R.; Wu, W.P. Advances in research on echinococcoses epidemiology in China. Acta Trop 2021, 219, 105921. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.; Cairang, Y.; Jiang, T.; Zhou, J.; Zhang, L.; Qi, B.; Ma, S.; Tang, L.; Xu, D.; Bu, L.; et al. Ultrasound identification of hepatic echinococcosis using a deep convolutional neural network model in China: A retrospective, large-scale, multicentre, diagnostic accuracy study. Lancet Digit. Health 2023, 5, e503–e514. [Google Scholar] [CrossRef] [PubMed]
- Kronenberg, P.A.; Reinehr, M.; Eichenberger, R.M.; Hasler, S.; Laurimae, T.; Weber, A.; Deibel, A.; Mullhaupt, B.; Gottstein, B.; Muller, N.; et al. Monoclonal antibody-based localization of major diagnostic antigens in metacestode tissue, excretory/secretory products, and extracellular vesicles of Echinococcus species. Front. Cell Infect. Microbiol. 2023, 13, 1162530. [Google Scholar] [CrossRef] [PubMed]
- Kronenberg, P.A.; Deibel, A.; Gottstein, B.; Grimm, F.; Mullhaupt, B.; Meyer Zu Schwabedissen, C.; Aitbaev, S.; Omorov, R.A.; Abdykerimov, K.K.; Minbaeva, G.; et al. Serological Assays for Alveolar and Cystic Echinococcosis-A Comparative Multi-Test Study in Switzerland and Kyrgyzstan. Pathogens 2022, 11, 518. [Google Scholar] [CrossRef] [PubMed]
- Knapp, J.; Sako, Y.; Grenouillet, F.; Bresson-Hadni, S.; Richou, C.; Gbaguidi-Haore, H.; Ito, A.; Millon, L. Comparison of the serological tests ICT and ELISA for the diagnosis of alveolar echinococcosis in France. Parasite 2014, 21, 34. [Google Scholar] [CrossRef]
- Tamarozzi, F.; Covini, I.; Mariconti, M.; Narra, R.; Tinelli, C.; De Silvestri, A.; Manzoni, F.; Casulli, A.; Ito, A.; Neumayr, A.; et al. Comparison of the Diagnostic Accuracy of Three Rapid Tests for the Serodiagnosis of Hepatic Cystic Echinococcosis in Humans. PLoS Negl. Trop Dis. 2016, 10, e0004444. [Google Scholar] [CrossRef]
- Retamozo, A.R.; Agüero, F.A.; Fuchs, A.G.; Maglioco, A.F. Serological Diagnosis in Hydatidosis: Searching Standardized Antigenic Support. Systematic Review and Meta-Analysis. Interam. J. Health Sci. 2021, 1, 89–108. Available online: https://ri.conicet.gov.ar/handle/11336/207809 (accessed on 17 October 2023).
- Ma, T.; Wang, Q.; Hao, M.; Xue, C.; Wang, X.; Han, S.; Wang, Q.; Zhao, J.; Ma, X.; Wu, X.; et al. Epidemiological characteristics and risk factors for cystic and alveolar echinococcosis in China: An analysis of a national population-based field survey. Parasit. Vectors 2023, 16, 181. [Google Scholar] [CrossRef]
- Wang, Q.; Zhao, S.; Jide, A.; Guo, Y.; Yang, J.; Naveed, A.; Gao, W. Co-Occurrence of Cystic and Alveolar Echinococcosis in the Liver: A Case Report. Iran. J. Parasitol. 2021, 16, 168–172. [Google Scholar] [CrossRef]
- Cadavid Restrepo, A.M.; Yang, Y.R.; McManus, D.P.; Gray, D.J.; Barnes, T.S.; Williams, G.M.; Soares Magalhaes, R.J.; Clements, A.C.A. Environmental risk factors and changing spatial patterns of human seropositivity for Echinococcus spp. in Xiji County, Ningxia Hui Autonomous Region, China. Parasit. Vectors 2018, 11, 159. [Google Scholar] [CrossRef]
- Sadjjadi, F.S.; Mohammadzadeh, T.; Jafari, S.H.; Sharifi, Y.; Deilami, H.N.; Hafezi, F.; Sadjjadi, S.M. 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, 1764–1772. [Google Scholar] [CrossRef]
- Tamarozzi, F.; Longoni, S.S.; Vola, A.; Degani, M.; Tais, S.; Rizzi, E.; Prato, M.; Scarso, S.; Silva, R.; Brunetti, E.; et al. Evaluation of Nine Commercial Serological Tests for the Diagnosis of Human Hepatic Cyst Echinococcosis and the Differential Diagnosis with Other Focal Liver Lesions: A Diagnostic Accuracy Study. Diagnostics 2021, 11, 167. [Google Scholar] [CrossRef]
- Sako, Y.; Fukuda, K.; Kobayashi, Y.; Ito, A. Development of an immunochromatographic test to detect antibodies against recombinant Em18 for diagnosis of alveolar echinococcosis. J. Clin. Microbiol. 2009, 47, 252–254. [Google Scholar] [CrossRef]
- Gessese, A.T. Review on Epidemiology and Public Health Significance of Hydatidosis. Vet. Med. Int. 2020, 2020, 8859116. [Google Scholar] [CrossRef]
- Di, X.; Li, S.; Ma, B.; Di, X.; Li, Y.; An, B.; Jiang, W. How climate, landscape, and economic changes increase the exposure of Echinococcus spp. BMC Public Health 2022, 22, 2315. [Google Scholar] [CrossRef]
- Simoncini, A.; Massolo, A. Multiscale ecological drivers of Echinococcus multilocularis spatial distribution in wild hosts: A systematic review. Food Waterborne Parasitol. 2024, 34, e00216. [Google Scholar] [CrossRef] [PubMed]
- Craig, P.S.; Hegglin, D.; Lightowlers, M.W.; Torgerson, P.R.; Wang, Q. Echinococcosis: Control and Prevention. Adv. Parasitol. 2017, 96, 55–158. [Google Scholar] [PubMed]
- Du, Q.; Wang, Y.; Guan, S.; Hu, C.; Li, M.; Zhou, L.; Zhang, M.; Chen, Y.; Mei, X.; Sun, J.; et al. The diagnostic nomogram of platelet-based score models for hepatic alveolar echinococcosis and atypical liver cancer. Sci. Rep. 2019, 9, 19403. [Google Scholar] [CrossRef] [PubMed]
- Peruzzu, A.; Mastrandrea, S.; Fancellu, A.; Bonelli, P.; Muehlethaler, K.; Masala, G.; Santucciu, C. Comparison and evaluation of analytic and diagnostic performances of four commercial kits for the detection of antibodies against Echinococcus granulosus and multilocularis in human sera. Comp. Immunol. Microbiol. Infect. Dis. 2022, 86, 101816. [Google Scholar] [CrossRef] [PubMed]
- Gottstein, B.; Lachenmayer, A.; Beldi, G.; Wang, J.; Merkle, B.; Vu, X.L.; Kurath, U.; Muller, N. Diagnostic and follow-up performance of serological tests for different forms/courses of alveolar echinococcosis. Food Waterborne Parasitol. 2019, 16, e00055. [Google Scholar] [CrossRef] [PubMed]
- Lightowlers, M.W.; Gasser, R.B.; Hemphill, A.; Romig, T.; Tamarozzi, F.; Deplazes, P.; Torgerson, P.R.; Garcia, H.H.; Kern, P. Advances in the treatment, diagnosis, control and scientific understanding of taeniid cestode parasite infections over the past 50 years. Int. J. Parasitol. 2021, 51, 1167–1192. [Google Scholar] [CrossRef] [PubMed]
- Schweiger, A.; Grimm, F.; Tanner, I.; Mullhaupt, B.; Bertogg, K.; Muller, N.; Deplazes, P. Serological diagnosis of echinococcosis: The diagnostic potential of native antigens. Infection 2012, 40, 139–152. [Google Scholar] [CrossRef] [PubMed]
- Tamarozzi, F.; Silva, R.; Fittipaldo, V.A.; Buonfrate, D.; Gottstein, B.; Siles-Lucas, M. Serology for the diagnosis of human hepatic cystic echinococcosis and its relation with cyst staging: A systematic review of the literature with meta-analysis. PLoS Negl. Trop. Dis. 2021, 15, e0009370. [Google Scholar] [CrossRef] [PubMed]
- Akira, I. Serodiagnosis of alveolar echinococcosis: Detection of antibody against EM18 in patients and rodents. Southeast Asian J. Trop. Med. Public Health 1997, 28 (Suppl. S1), 117–124. [Google Scholar]
US-Positive Patients | Number Tested | ELISA | ADAMU kit | ||||||
---|---|---|---|---|---|---|---|---|---|
Em | Eg | Em/Eg | No Ab | Em | Eg | Em/Eg | No Ab | ||
AE | 95 | 2 | 36 | 29 | 28 | 39 | 4 | 28 | 24 |
CE | 269 | 2 | 144 | 63 | 60 | 6 | 109 | 14 | 140 |
AE and CE | 6 | 0 | 4 | 1 | 1 | 0 | 1 | 2 | 3 |
Total | 370 | 4 | 184 | 93 | 89 | 45 | 114 | 44 | 167 |
ELISA | ADAMU Kit | |||
---|---|---|---|---|
US Classification | Po./All (%) | p-Value | Po./All(%) | p-Value |
CE types | ||||
CE1 a | 20/30 (67) | <0.01 a,b/a,d | 11/30 (37) | >0.05 (df = 3) |
CE2 b | 68/78 (87) | <0.01 b,c/b,d | 39/78 (50) | |
CE3 c | 14/23 (61) | >0.05 a,c | 13/23 (57) | |
CE4/CE5 d | 11/33 (33) | >0.05 c,d | 10/33 (30) | |
AE types | ||||
Infiltrating 1 | 10/29 (34) | >0.05 (df = 2) | 25/29 (86) | 1.0 1,2 |
Liquefied 2 | 4/15 (27) | 13/15 (87) | <0.05 2,3 | |
Calcified 3 | 14/45 (31) | 24/45 (53) | <0.01 1,3 |
US-Negative | Number Tested | ELISA | ADAMU Kit | ||||||
---|---|---|---|---|---|---|---|---|---|
Subjects | Em | Eg | Em/Eg | No Ab | Em | Eg | Em/Eg | No Ab | |
Group 1 | 251 | / | / | 251 | / | 1 | 0 | 0 | 250 |
Group 2 | 3672 | 29 | 448 | / | 3195 | N/A | N/A | N/A | N/A |
Total | 3923 | 29 | 448 | 251 | 3195 | 1 | 0 | 0 | 250 |
Category | AE | CE | ||||
---|---|---|---|---|---|---|
ELISA | ADAMU Kit | p-Value | ELISA | ADAMU Kit | p-Value | |
Sensitivity | 31/95 (33%) | 67/95 (71%) | <0.05 | 207/269 (77%) | 123/269 (46%) | <0.05 |
Specificity | 3643/3923 (93%) | 250/251 (99%) | <0.05 | 3224/3923 (82%) | 251/251 (100%) | <0.05 |
Cross-reactivity | 65/95 (68%) | 32/95 (34%) | <0.05 | 65/269 (24%) | 20/269 (7%) | <0.05 |
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Yang, S.-K.; Zhang, W.; Zhu, N.; McManus, D.P.; Gray, D.J.; Clements, A.C.A.; Cadavid Restrepo, A.M.; Williams, G.M.; Zhang, T.; Ma, G.-R.; et al. Serological Comparison of Native Antigen ELISAs with Rapid ICT Test Kits for the Diagnosis of Human Alveolar and Cystic Echinococcosis in China. Trop. Med. Infect. Dis. 2024, 9, 44. https://doi.org/10.3390/tropicalmed9020044
Yang S-K, Zhang W, Zhu N, McManus DP, Gray DJ, Clements ACA, Cadavid Restrepo AM, Williams GM, Zhang T, Ma G-R, et al. Serological Comparison of Native Antigen ELISAs with Rapid ICT Test Kits for the Diagnosis of Human Alveolar and Cystic Echinococcosis in China. Tropical Medicine and Infectious Disease. 2024; 9(2):44. https://doi.org/10.3390/tropicalmed9020044
Chicago/Turabian StyleYang, Shu-Kun, Wei Zhang, Na Zhu, Donald P. McManus, Darren J. Gray, Archie C. A. Clements, Angela M. Cadavid Restrepo, Gail M. Williams, Ting Zhang, Guo-Rong Ma, and et al. 2024. "Serological Comparison of Native Antigen ELISAs with Rapid ICT Test Kits for the Diagnosis of Human Alveolar and Cystic Echinococcosis in China" Tropical Medicine and Infectious Disease 9, no. 2: 44. https://doi.org/10.3390/tropicalmed9020044