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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

Dinh Ng-Nguyen, Mark A Stevenson, Pierre Dorny UGent, Sarah Gabriël UGent, Tinh Van Vo, Van-Anh Thi Nguyen, Trong Van Phan, Sze Fui Hii and Rebecca J Traub (2017) PLOS NEGLECTED TROPICAL DISEASES. 11(7).
abstract
Background : Taenia solium, the cause of neurocysticercosis (NCC), has significant socioeconomic impacts on communities in developing countries. This disease, along with taeniasis is estimated to infect 2.5 to 5 million people globally. Control of T. solium NCC necessitates accurate diagnosis and treatment of T. solium taeniasis carriers. In areas where all three species of Taenia tapeworms (T. solium, Taenia saginata and Taenia asiatica) occur sympatrically, conventional microscope-and copro-antigen based diagnostic methods are unable to distinguish between these three Taenia species. Molecular diagnostic tools have been developed to overcome this limitation; however, conventional PCR-based techniques remain unsuitable for large-scale deployment in community-based surveys. Moreover, a real-time PCR (qPCR) for the discrimination of all three species of Taenia in human stool does not exist. This study describes the development and validation of a new triplex Taq-Man probe-based qPCR for the detection and discrimination of all three Taenia human tapeworms in human stools collected from communities in the Central Highlands of Vietnam. The diagnostic characteristics of the test are compared with conventional Kato Katz (KK) thick smear and copro-antigen ELISA (cAgELISA) method utilizing fecal samples from a community based cross-sectional study. Using this new multiplex real-time PCR we provide an estimate of the true prevalence of taeniasis in the source population for the community based cross-sectional study. Methodology/Principal findings : Primers and TaqMan probes for the specific amplification of T. solium, T. saginata and T. asiatica were designed and successfully optimized to target the internal transcribed spacer I (ITS-1) gene of T. solium and the cytochrome oxidase subunit I (COX-1) gene of T. saginata and T. asiatica. The newly designed triplex qPCR (T3qPCR) was compared to KK and cAgELISA for the detection of Taenia eggs in stool samples collected from 342 individuals in Dak Lak province, Central Highlands of Vietnam. The overall apparent prevalence of taeniasis in Dak Lak province was 6.72% (95% confidence interval (CI) [3.94-9.50]) in which T. solium accounted for 1.17% (95% CI [0.37-3.17]), according to the T3qPCR. There was sympatric presence of T. solium, T. saginata and T. asiatica. The T3qPCR proved superior to KK and cAgELISA for the detection and differentiation of Taenia species in human feces. Diagnostic sensitivities of 0.94 (95% credible interval (CrI) [0.88-0.98]), 0.82 (95% CrI [0.58-0.95]) and 0.52 (95% CrI [0.07-0.94]), and diagnostic specificities of 0.98 (95% CrI [0.94-1.00]), 0.91 (95% CrI [0.85-0.96]) and 0.99 (95% CrI [0.96-1.00]) were estimated for the diagnosis of taeniasis for the T3qPCR, cAgELISA and KK thick smear in this study, respectively. Conclusions : T3qPCR is not only superior to the KK thick smear and cAgELISA in terms of diagnostic sensitivity and specificity, but it also has the advantage of discriminating between species of Taenia eggs in stools. Application of this newly developed T3qPCR has identified the existence of all three human Taenia tapeworms in Dak Lak province and proves for the first time, the existence of T. asiatica in the Central Highlands and the south of Vietnam.
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author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
LINKED-IMMUNOSORBENT-ASSAY, SOLIUM TAENIASIS, COPROANTIGEN ELISA, DIAGNOSIS, CYSTICERCOSIS, ASIATICA, NEUROCYSTICERCOSIS, PATHOGENESIS, FIELD
journal title
PLOS NEGLECTED TROPICAL DISEASES
Plos Neglect. Trop. Dis.
volume
11
issue
7
article number
e0005743
pages
18 pages
Web of Science type
Article
Web of Science id
000408057300050
ISSN
1935-2735
DOI
10.1371/journal.pntd.0005743
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
8529854
handle
http://hdl.handle.net/1854/LU-8529854
date created
2017-08-30 07:42:35
date last changed
2017-10-05 08:25:29
@article{8529854,
  abstract     = {Background : Taenia solium, the cause of neurocysticercosis (NCC), has significant socioeconomic impacts on communities in developing countries. This disease, along with taeniasis is estimated to infect 2.5 to 5 million people globally. Control of T. solium NCC necessitates accurate diagnosis and treatment of T. solium taeniasis carriers. In areas where all three species of Taenia tapeworms (T. solium, Taenia saginata and Taenia asiatica) occur sympatrically, conventional microscope-and copro-antigen based diagnostic methods are unable to distinguish between these three Taenia species. Molecular diagnostic tools have been developed to overcome this limitation; however, conventional PCR-based techniques remain unsuitable for large-scale deployment in community-based surveys. Moreover, a real-time PCR (qPCR) for the discrimination of all three species of Taenia in human stool does not exist. This study describes the development and validation of a new triplex Taq-Man probe-based qPCR for the detection and discrimination of all three Taenia human tapeworms in human stools collected from communities in the Central Highlands of Vietnam. The diagnostic characteristics of the test are compared with conventional Kato Katz (KK) thick smear and copro-antigen ELISA (cAgELISA) method utilizing fecal samples from a community based cross-sectional study. Using this new multiplex real-time PCR we provide an estimate of the true prevalence of taeniasis in the source population for the community based cross-sectional study. 
Methodology/Principal findings : Primers and TaqMan probes for the specific amplification of T. solium, T. saginata and T. asiatica were designed and successfully optimized to target the internal transcribed spacer I (ITS-1) gene of T. solium and the cytochrome oxidase subunit I (COX-1) gene of T. saginata and T. asiatica. The newly designed triplex qPCR (T3qPCR) was compared to KK and cAgELISA for the detection of Taenia eggs in stool samples collected from 342 individuals in Dak Lak province, Central Highlands of Vietnam. The overall apparent prevalence of taeniasis in Dak Lak province was 6.72\% (95\% confidence interval (CI) [3.94-9.50]) in which T. solium accounted for 1.17\% (95\% CI [0.37-3.17]), according to the T3qPCR. There was sympatric presence of T. solium, T. saginata and T. asiatica. The T3qPCR proved superior to KK and cAgELISA for the detection and differentiation of Taenia species in human feces. Diagnostic sensitivities of 0.94 (95\% credible interval (CrI) [0.88-0.98]), 0.82 (95\% CrI [0.58-0.95]) and 0.52 (95\% CrI [0.07-0.94]), and diagnostic specificities of 0.98 (95\% CrI [0.94-1.00]), 0.91 (95\% CrI [0.85-0.96]) and 0.99 (95\% CrI [0.96-1.00]) were estimated for the diagnosis of taeniasis for the T3qPCR, cAgELISA and KK thick smear in this study, respectively. 
Conclusions : T3qPCR is not only superior to the KK thick smear and cAgELISA in terms of diagnostic sensitivity and specificity, but it also has the advantage of discriminating between species of Taenia eggs in stools. Application of this newly developed T3qPCR has identified the existence of all three human Taenia tapeworms in Dak Lak province and proves for the first time, the existence of T. asiatica in the Central Highlands and the south of Vietnam.},
  articleno    = {e0005743},
  author       = {Ng-Nguyen, Dinh and Stevenson, Mark A and Dorny, Pierre and Gabri{\"e}l, Sarah and Vo, Tinh Van and Nguyen, Van-Anh Thi and Phan, Trong Van and Hii, Sze Fui and Traub, Rebecca J},
  issn         = {1935-2735},
  journal      = {PLOS NEGLECTED TROPICAL DISEASES},
  keyword      = {LINKED-IMMUNOSORBENT-ASSAY,SOLIUM TAENIASIS,COPROANTIGEN ELISA,DIAGNOSIS,CYSTICERCOSIS,ASIATICA,NEUROCYSTICERCOSIS,PATHOGENESIS,FIELD},
  language     = {eng},
  number       = {7},
  pages        = {18},
  title        = {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},
  url          = {http://dx.doi.org/10.1371/journal.pntd.0005743},
  volume       = {11},
  year         = {2017},
}

Chicago
Ng-Nguyen, Dinh, Mark A Stevenson, Pierre Dorny, Sarah Gabriël, Tinh Van Vo, Van-Anh Thi Nguyen, Trong Van Phan, Sze Fui Hii, and Rebecca J Traub. 2017. “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 Neglected Tropical Diseases 11 (7).
APA
Ng-Nguyen, D., Stevenson, M. A., Dorny, P., Gabriël, S., Vo, T. V., Nguyen, V.-A. T., Phan, T. V., et al. (2017). 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 NEGLECTED TROPICAL DISEASES, 11(7).
Vancouver
1.
Ng-Nguyen D, Stevenson MA, Dorny P, Gabriël S, Vo TV, Nguyen V-AT, et al. 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 NEGLECTED TROPICAL DISEASES. 2017;11(7).
MLA
Ng-Nguyen, Dinh, Mark A Stevenson, Pierre Dorny, et al. “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 NEGLECTED TROPICAL DISEASES 11.7 (2017): n. pag. Print.