Evaluation of an Antibody Detecting Point of Care Test for Diagnosis of Taenia solium Cysticercosis in a Zambian Rural Community: A Prospective Diagnostic Accuracy Study
Abstract
:1. Introduction
2. Methods
2.1. Study Setting, Design and Participant Recruitment
2.2. Sampling and Sample Processing
2.3. Diagnostic Methods
2.3.1. Index Test—The TS POC CC Test Strip
2.3.2. Reference Tests
2.4. Data Analysis
2.5. Trial Registration
3. Results
3.1. Flow and Demographic Characteristics of Participants
3.2. Reference Test Results
3.3. Estimates of Diagnostic Accuracy
3.4. Agreement between Tests
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Coral-Almeida, M.; Gabriël, S.; Abatih, E.N.; Praet, N.; Benitez, W.; Dorny, P. Taenia Solium Human Cysticercosis: A Systematic Review of Sero-Epidemiological Data from Endemic Zones around the World. PLoS Negl. Trop. Dis. 2015, 9, e0003919. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Afonso, S.M.; Vaz, Y.; Neves, L.; Pondja, A.; Dias, G.; Willingham, A.L.; Vilhena, M.; Duarte, P.C.; Jost, C.C.; Noormahomed, E.V. Human and Porcine Taenia Solium Infections in Mozambique: Identifying Research Priorities. Anim. Health Res. Rev. 2011, 12, 123–129. [Google Scholar] [CrossRef] [PubMed]
- Gabriël, S.; Mwape, K.E.; Hobbs, E.C.; Devleesschauwer, B.; Van Damme, I.; Zulu, G.; Mwelwa, C.; Mubanga, C.; Masuku, M.; Mambwe, M.; et al. Potential Elimination of Active Taenia Solium Transmission in Africa. N. Engl. J. Med. 2020, 383, 396–397. [Google Scholar] [CrossRef] [PubMed]
- Garcia, H.H.; Gonzalez, A.E.; Rodriguez, S.; Gonzalvez, G.; Llanos-Zavalaga, F.; Tsang, V.C.; Gilman, R.H.; Grupo de Trabajo en Cisticercosis en Peru. Epidemiology and Control of Cysticercosis in Peru. Rev. Peru Med. Exp. Salud Publica 2010, 27, 592–597. [Google Scholar] [CrossRef]
- Medina, M.T.; Aguilar-Estrada, R.L.; Alvarez, A.; Durõn, R.M.; Martínez, L.; Dubõn, S.; Estrada, A.L.; Zúniga, C.; Cartagena, D.; Thompson, A.; et al. Reduction in Rate of Epilepsy from Neurocysticercosis by Community Interventions: The Salamá, Honduras Study. Epilepsia 2011, 52, 1177–1185. [Google Scholar] [CrossRef]
- Sarti, E.; Schantz, P.M.; Avila, G.; Ambrosio, J.; Medina-Santillán, R.; Flisser, A. Mass Treatment against Human Taeniasis for the Control of Cysticercosis: A Population-Based Intervention Study. Trans. R. Soc. Trop. Med. Hyg. 2000, 94, 85–89. [Google Scholar] [CrossRef]
- Rodriguez, S.; Wilkins, P.; Dorny, P. Immunological and Molecular Diagnosis of Cysticercosis. Pathog. Glob. Health 2012, 106, 286–298. [Google Scholar] [CrossRef] [Green Version]
- Tsang, V.C.; Brand, J.A.; Boyer, A.E. An Enzyme-Linked Immunoelectrotransfer Blot Assay and Glycoprotein Antigens for Diagnosing Human Cysticercosis (Taenia solium). J. Infect. Dis. 1989, 159, 50–59. [Google Scholar] [CrossRef]
- Praet, N.; Rodriguez-Hidalgo, R.; Speybroeck, N.; Ahounou, S.; Benitez-Ortiz, W.; Berkvens, D.; Van Hul, A.; Barrionuevo-Samaniego, M.; Saegerman, C.; Dorny, P.; et al. Infection with versus Exposure to Taenia Solium: What Do Serological Test Results Tell Us? Am. J. Trop. Med. Hyg. 2010, 83, 413–415. [Google Scholar] [CrossRef] [Green Version]
- Garcia, H.H.; O’Neal, S.E.; Noh, J.; Handali, S.; Gilman, R.H.; Gonzalez, A.E.; Tsang, V.C.W.; Rodriguez, S.; Martinez, M.; Gonzales, I.; et al. Laboratory Diagnosis of Neurocysticercosis (Taenia solium). J. Clin. Microbiol. 2018, 56, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Hancock, K.; Pattabhi, S.; Whitfield, F.W.; Yushak, M.L.; Lane, W.S.; Garcia, H.H.; Gonzalez, A.E.; Gilman, R.H.; Tsang, V.C. Characterization and Cloning of T24, a Taenia Solium Antigen Diagnostic for Cysticercosis. Mol. Biochem. Parasitol. 2006, 147, 109–117. [Google Scholar] [CrossRef]
- Dermauw, V.; Carabin, H.; Cissé, A.; Millogo, A.; Tarnagda, Z.; Ganaba, R.; Noh, J.; Handali, S.; Breen, K.; Richter, V.; et al. Evaluating the Recombinant T24H Enzyme-Linked Immunoelectrotransfer Blot Assay for the Diagnosis of Neurocysticercosis in a Panel of Samples from a Large Community-Based Randomized Control Trial in 60 Villages in Burkina Faso. Am. J. Trop. Med. Hyg. 2018, 98, 565–569. [Google Scholar] [CrossRef] [Green Version]
- Dorny, P.; Phiri, I.K.; Vercruysse, J.; Gabriel, S.; Willingham, A.L., 3rd; Brandt, J.; Victor, B.; Speybroeck, N.; Berkvens, D. A Bayesian Approach for Estimating Values for Prevalence and Diagnostic Test Characteristics of Porcine Cysticercosis. Int. J. Parasitol. 2004, 34, 569–576. [Google Scholar] [CrossRef]
- Fleury, A.; Hernandez, M.; Avila, M.; Cardenas, G.; Bobes, R.J.; Huerta, M.; Fragoso, G.; Uribe-Campero, L.; Harrison, L.J.; Parkhouse, R.M.; et al. Detection of HP10 Antigen in Serum for Diagnosis and Follow-up of Subarachnoidal and Intraventricular Human Neurocysticercosis. J. Neurol. Neurosurg. Psychiatry 2007, 78, 970–974. [Google Scholar] [CrossRef] [Green Version]
- Del Brutto, O.H.H.; Nash, T.E.E.; White, A.C.C.; Rajshekhar, V.; Wilkins, P.P.P.; Singh, G.; Vasquez, C.M.M.; Salgado, P.; Gilman, R.H.H.; Garcia, H.H.H.; et al. Revised Diagnostic Criteria for Neurocysticercosis. J. Neurol. Sci. 2017, 372, 202–210. [Google Scholar] [CrossRef] [Green Version]
- World Health Organization. Taenia Solium Taeniasis/Cysticercosis Diagnostic Tools; WHO: Geneva, Switzerland, 2015. [Google Scholar]
- Pai, N.P.; Vadnais, C.; Denkinger, C.; Engel, N.; Pai, M. Point-of-Care Testing for Infectious Diseases: Diversity, Complexity, and Barriers in Low- And Middle-Income Countries. PLoS Med. 2012, 9, e1001306. [Google Scholar] [CrossRef] [Green Version]
- Mubanga, C.; Mwape, K.E.; Phiri, I.K.; Trevisan, C.; Zulu, G.; Chabala, C.; van Damme, I.; Schmidt, V.; Dorny, P.; Gabriël, S. Progress on the Development of Rapid Diagnostic Tests for Foodborne Neglected Zoonotic Helminthiases: A Systematic Review. Acta Trop. 2019, 194, 135–147. [Google Scholar] [CrossRef]
- Levine, M.Z.; Calderon, J.C.; Wilkins, P.P.; Lane, W.S.; Asara, J.M.; Hancock, K.; Gonzalez, A.E.; Garcia, H.H.; Gilman, R.H.; Tsang, V.C.W.; et al. Characterization, Cloning, and Expression of Two Diagnostic Antigens for Taenia Solium Tapeworm Infection. J. Parasitol. 2004, 90, 631–638. [Google Scholar] [CrossRef]
- Van Damme, I.; Trevisan, C.; Mwape, K.E.; Schmidt, V.; Magnussen, P.; Zulu, G.; Mubanga, C.; Stelzle, D.; Bottieau, E.; Abatih, E.N.; et al. Trial Design for a Diagnostic Accuracy Study of a Point-of-Care Test for the Detection of Taenia Solium Taeniosis and (Neuro)Cysticercosis in Community Settings of Highly Endemic, Resource-Poor Areas in Zambia: Challenges and Rationale. Diagnostics 2021, 11, 1138. [Google Scholar] [CrossRef]
- Gabriël, S.; Mwape, K.E.; Phiri, I.K.; Devleesschauwer, B.; Dorny, P. Taenia Solium Control in Zambia: The Potholed Road to Success. Parasite Epidemiol. Control 2019, 4, e00082. [Google Scholar] [CrossRef]
- Mubanga, C.; Mwape, K.E.; Phiri, I.K.; Trevisan, C.; Kabululu, M.; Zulu, G.; Van Damme, I.; Schmidt, V.; Dorny, P.; Gabriël, S. Operational Characteristics of an Antibody Detecting Point of Care Test for Taenia Solium Infections in a Community and Hospital Setting. BMC Infect. Dis. 2021, 21, 607. [Google Scholar] [CrossRef]
- Noh, J.; Rodriguez, S.; Lee, Y.M.; Handali, S.; Gonzalez, A.E.; Gilman, R.H.; Tsang, V.C.; Garcia, H.H.; Wilkins, P.P. Recombinant Protein- and Synthetic Peptide-Based Immunoblot Test for Diagnosis of Neurocysticercosis. J. Clin. Microbiol. 2014, 52, 1429–1434. [Google Scholar] [CrossRef] [Green Version]
- Lesaffre, E.; Speybroeck, N.; Berkvens, D. Bayes and Diagnostic Testing. Vet. Parasitol. 2007, 148, 58–61. [Google Scholar] [CrossRef]
- Berkvens, D.; Speybroeck, N.; Praet, N.; Adel, A.; Lesaffre, E. Estimating Disease Prevalence in a Bayesian Framework Using Probabilistic Constraints. Epidemiology 2006, 17, 145–153. [Google Scholar] [CrossRef]
- Nakazawa, M. Fmsb: Functions for Medical Statistics Book with Some Demographic Data. R Package Version 0.5.1. 2014. Available online: http://CRAN.Rproject.Org/Package=fmsb (accessed on 21 February 2021).
- Feinstein, A.R.; Cicchetti, D.V. High Agreement but Low Kappa: I. the Problems of Two Paradoxes. J. Clin. Epidemiol. 1990, 43, 543–549. [Google Scholar] [CrossRef]
- Donadeu, M.; Fahrion, A.S.; Olliaro, P.L.; Abela-Ridder, B. Target Product Profiles for the Diagnosis of Taenia Solium Taeniasis, Neurocysticercosis and Porcine Cysticercosis. PLoS Negl. Trop. Dis. 2017, 11, e0005875. [Google Scholar] [CrossRef] [Green Version]
- Lightowlers, M.W.; Garcia, H.H.; Gauci, C.G.; Donadeu, M.; Abela-Ridder, B. Monitoring the Outcomes of Interventions against Taenia Solium: Options and Suggestions. Parasite Immunol. 2016, 38, 158–169. [Google Scholar] [CrossRef] [Green Version]
- Hernández-González, A.; Noh, J.; Perteguer, M.J.; Gárate, T.; Handali, S. Comparison of T24H-His, GST-T24H and GST-Ts8B2 Recombinant Antigens in Western Blot, ELISA and Multiplex Bead-Based Assay for Diagnosis of Neurocysticercosis. Parasites Vectors 2017, 10, 237. [Google Scholar] [CrossRef]
- Mwape, K.E.; Praet, N.; Benitez-Ortiz, W.; Muma, J.B.; Zulu, G.; Celi-Erazo, M.; Phiri, I.K.; Rodriguez-Hidalgo, R.; Dorny, P.; Gabriël, S. Field Evaluation of Urine Antigen Detection for Diagnosis of Taenia Solium Cysticercosis. Trans. R. Soc. Trop. Med. Hyg. 2011, 105, 574–578. [Google Scholar] [CrossRef]
- Gass, K. Time for a Diagnostic Sea-Change: Rethinking Neglected Tropical Disease Diagnostics to Achieve Elimination. PLoS Negl. Trop. Dis. 2020, 14, e0008933. [Google Scholar] [CrossRef]
- Mwape, K.E.; Phiri, I.K.; Praet, N.; Speybroeck, N.; Muma, J.B.; Dorny, P.; Gabriel, S. The Incidence of Human Cysticercosis in a Rural Community of Eastern Zambia. PLoS Negl. Trop. Dis. 2013, 7, e2142. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mukendi, D.; Kalo, J.-R.L.; Lutumba, P.; Barbé, B.; Jacobs, J.; Yansouni, C.; Gabriël, S.; Dorny, P.; Chappuis, F.; Boelaert, M.; et al. High Frequency of Taenia Solium Antigen Positivity in Patients Admitted for Neurological Disorders in the Rural Hospital of Mosango, Democratic Republic of Congo. BMC Infect. Dis. 2020, 21, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Umemneku Chikere, C.M.; Wilson, K.; Graziadio, S.; Vale, L.; Allen, A.J. Diagnostic Test Evaluation Methodology: A Systematic Review of Methods Employed to Evaluate Diagnostic Tests in the Absence of Gold Standard—An Update. PLoS ONE 2019, 14, e0223832. [Google Scholar] [CrossRef] [PubMed]
- Habib, I.; Sampers, I.; Uyttendaele, M.; De Zutter, L.; Berkvens, D. A Bayesian Modelling Framework to Estimate Campylobacter Prevalence and Culture Methods Sensitivity: Application to a Chicken Meat Survey in Belgium. J. Appl. Microbiol. 2008, 105, 2002–2008. [Google Scholar] [CrossRef]
- Jansen, F.; Dorny, P.; Gabriël, S.; Eichenberger, R.M.; Berkvens, D. Estimating Prevalence and Diagnostic Test Characteristics of Bovine Cysticercosis in Belgium in the Absence of a ‘Gold Standard’ Reference Test Using a Bayesian Approach. Vet. Parasitol. 2018, 254, 142–146. [Google Scholar] [CrossRef]
- Praet, N.; Verweij, J.J.; Mwape, K.E.; Phiri, I.K.; Muma, J.B.; Zulu, G.; van Lieshout, L.; Rodriguez-Hidalgo, R.; Benitez-Ortiz, W.; Dorny, P.; et al. Bayesian Modelling to Estimate the Test Characteristics of Coprology, Coproantigen ELISA and a Novel Real-Time PCR for the Diagnosis of Taeniasis. Trop. Med. Int. Health 2013, 18, 608–614. [Google Scholar] [CrossRef]
- Ng-Nguyen, D.; Stevenson, M.A.; Dorny, P.; Gabriël, S.; Van Vo, T.; Nguyen, V.-A.T.; Van Phan, T.; Hii, S.F.; Traub, R.J. Comparison of a New Multiplex Real-Time PCR with the Kato Katz Thick Smear and Copro-Antigen ELISA for the Detection and Differentiation of Taenia Spp. in Human Stools. PLoS Negl. Trop. Dis. 2017, 11, e0005743. [Google Scholar] [CrossRef] [Green Version]
- Speybroeck, N.; Praet, N.; Claes, F.; van Hong, N.; Torres, K.; Mao, S.; van den Eede, P.; Thinh, T.T.; Gamboa, D.; Sochantha, T.; et al. True versus Apparent Malaria Infection Prevalence: The Contribution of a Bayesian Approach. PLoS ONE 2011, 6, e16705. [Google Scholar] [CrossRef]
Characteristic | |
---|---|
Age (years) | |
Mean | 33 |
Range (min–max) | 10–95 |
Gender | |
Female (%) | 718 (57.3%) |
Male (%) | 536 (42.7%) |
TS POC CC | rT24H EITB | Serum Ag ELISA | n |
---|---|---|---|
1 | 1 | 1 | 8 |
1 | 1 | 0 | 3 |
1 | 0 | 1 | 1 |
1 | 0 | 0 | 2 |
1 | 1 | 1 | 5 |
1 | 1 | 0 | 11 |
1 | 0 | 1 | 15 |
1 | 0 | 0 | 93 |
0 | 1 | 1 | 1 |
0 | 1 | 0 | 8 |
0 | 0 | 1 | 13 |
0 | 0 | 0 | 95 |
Diagnostic Test | |||
---|---|---|---|
Measure of Accuracy | TS POC CC | rT24H EITB | Serum Ag ELISA |
Se (95% CI) | 35 (14–63) | 94 (91–98) | 36 (15–67) |
Sp (95% CI) | 87 (83–90) | 95 (91–98) | 87 (81–92) |
PPV (95% CI) | 16 (8–26) | 62 (40–86) | 17 (7–32) |
NPV (95% CI) | 94 (89–98) | 100 (99–100) | 94 (89–98) |
TS POC CC | rT24H EITB | |
---|---|---|
TS POC CC | NA | |
rT24H EITB | κ = 0.14 ppos = 0.24, pneg = 0.9 | NA |
Serum Ag ELISA | κ = 0.09 ppos = 0.21, pneg = 0.87 | κ = 0.09 ppos = 0.18, pneg = 0.9 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mubanga, C.; Van Damme, I.; Trevisan, C.; Schmidt, V.; Phiri, I.K.; Zulu, G.; Noh, J.; Handali, S.; Mambo, R.; Chembensofu, M.; et al. Evaluation of an Antibody Detecting Point of Care Test for Diagnosis of Taenia solium Cysticercosis in a Zambian Rural Community: A Prospective Diagnostic Accuracy Study. Diagnostics 2021, 11, 2121. https://doi.org/10.3390/diagnostics11112121
Mubanga C, Van Damme I, Trevisan C, Schmidt V, Phiri IK, Zulu G, Noh J, Handali S, Mambo R, Chembensofu M, et al. Evaluation of an Antibody Detecting Point of Care Test for Diagnosis of Taenia solium Cysticercosis in a Zambian Rural Community: A Prospective Diagnostic Accuracy Study. Diagnostics. 2021; 11(11):2121. https://doi.org/10.3390/diagnostics11112121
Chicago/Turabian StyleMubanga, Chishimba, Inge Van Damme, Chiara Trevisan, Veronika Schmidt, Isaac K. Phiri, Gideon Zulu, John Noh, Sukwan Handali, Richard Mambo, Mwelwa Chembensofu, and et al. 2021. "Evaluation of an Antibody Detecting Point of Care Test for Diagnosis of Taenia solium Cysticercosis in a Zambian Rural Community: A Prospective Diagnostic Accuracy Study" Diagnostics 11, no. 11: 2121. https://doi.org/10.3390/diagnostics11112121