Urine metabolites for the identification of Onchocerca volvulus infections in patients from Cameroon.


Journal

Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774

Informations de publication

Date de publication:
11 Aug 2021
Historique:
received: 07 05 2021
accepted: 24 07 2021
entrez: 12 8 2021
pubmed: 13 8 2021
medline: 20 11 2021
Statut: epublish

Résumé

The tropical disease onchocerciasis (river blindness), caused by Onchocerca volvulus filarial nematodes, is targeted for elimination by mass treatment with nematocidal and antimicrobial drugs. Diagnosis of O. volvulus infections is based on counts of skin-borne microfilariae, but additional diagnostic tools, e.g. worm- or host-derived small RNAs, proteins or metabolites, are required for high-throughput screening. N-acetyltyramine-O,β-glucuronide (NATOG) was suggested as a biomarker for onchocerciasis but its viability as diagnostic tool has been challenged. We performed a screening program of urine samples from individuals from Cameroon infected with O. volvulus, Loa loa, Mansonella perstans or a combination thereof. Urine metabolites were measured by liquid chromatography-mass spectrometry (LC-MS). Principle component analysis (PCA) revealed that onchocerciasis causes complex changes of the urine metabolome. The mean NATOG content was elevated in urine of O. volvulus-infected compared with non-infected individuals, but NATOG levels showed considerable variation. However, 13.8% of all O. volvulus-infected individuals had high NATOG levels never reached by individuals without filarial infections or only infected with L. loa or M. perstans. Therefore, the identification of individuals with high NATOG levels might be used to screen for the elimination of onchocerciasis after mass drug application. Additional metabolites, including a compound identified as cinnamoylglycine, had high PC1/PC2 loadings in the data set. Mean levels of cinnamoylglycine were increased in O. volvulus-infected individuals, and 17.2% of all O. volvulus individuals had elevated cinnamoylglycine levels not reached by the controls. On an individual level, NATOG alone had poor discriminative power distinguishing infected from non-infected individuals. However, 13.8% of all O. volvulus-infected individuals had NATOG levels never reached by individuals without filarial infections or infected with only L. loa or M. perstans. Discrimination of O. volvulus infections from controls or individuals suffering from multiple infections was improved by the measurement of additional metabolites, e.g. cinnamoylglycine. Thus, measuring a combination of urine metabolites may provide a way to assess onchocerciasis on the population level. This provides the possibility to design a strategy for large-scale onchocerciasis epidemiological screening programs based on urine rather than invasive techniques.

Sections du résumé

BACKGROUND BACKGROUND
The tropical disease onchocerciasis (river blindness), caused by Onchocerca volvulus filarial nematodes, is targeted for elimination by mass treatment with nematocidal and antimicrobial drugs. Diagnosis of O. volvulus infections is based on counts of skin-borne microfilariae, but additional diagnostic tools, e.g. worm- or host-derived small RNAs, proteins or metabolites, are required for high-throughput screening. N-acetyltyramine-O,β-glucuronide (NATOG) was suggested as a biomarker for onchocerciasis but its viability as diagnostic tool has been challenged.
METHODS METHODS
We performed a screening program of urine samples from individuals from Cameroon infected with O. volvulus, Loa loa, Mansonella perstans or a combination thereof. Urine metabolites were measured by liquid chromatography-mass spectrometry (LC-MS). Principle component analysis (PCA) revealed that onchocerciasis causes complex changes of the urine metabolome.
RESULTS RESULTS
The mean NATOG content was elevated in urine of O. volvulus-infected compared with non-infected individuals, but NATOG levels showed considerable variation. However, 13.8% of all O. volvulus-infected individuals had high NATOG levels never reached by individuals without filarial infections or only infected with L. loa or M. perstans. Therefore, the identification of individuals with high NATOG levels might be used to screen for the elimination of onchocerciasis after mass drug application. Additional metabolites, including a compound identified as cinnamoylglycine, had high PC1/PC2 loadings in the data set. Mean levels of cinnamoylglycine were increased in O. volvulus-infected individuals, and 17.2% of all O. volvulus individuals had elevated cinnamoylglycine levels not reached by the controls.
CONCLUSIONS CONCLUSIONS
On an individual level, NATOG alone had poor discriminative power distinguishing infected from non-infected individuals. However, 13.8% of all O. volvulus-infected individuals had NATOG levels never reached by individuals without filarial infections or infected with only L. loa or M. perstans. Discrimination of O. volvulus infections from controls or individuals suffering from multiple infections was improved by the measurement of additional metabolites, e.g. cinnamoylglycine. Thus, measuring a combination of urine metabolites may provide a way to assess onchocerciasis on the population level. This provides the possibility to design a strategy for large-scale onchocerciasis epidemiological screening programs based on urine rather than invasive techniques.

Identifiants

pubmed: 34380554
doi: 10.1186/s13071-021-04893-1
pii: 10.1186/s13071-021-04893-1
pmc: PMC8359580
doi:

Substances chimiques

Biomarkers 0
Glucuronides 0
cinnamoylglycine 16534-24-0
Glycine TE7660XO1C

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

397

Subventions

Organisme : Bill and Melinda Gates Foundation
ID : OPP1083888
Organisme : Deutsches Zentrum für Infektionsforschung
ID : TI 03.907
Organisme : Deutsche Forschungsgemeinschaft
ID : TRR 261

Informations de copyright

© 2021. The Author(s).

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Auteurs

Vera Wewer (V)

Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Venusberg-Campus 1, 53127, Bonn, Germany.
Center of Excellence in Plant Sciences (CEPLAS), Mass Spectrometry Platform, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany.

Helga Peisker (H)

Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, Karlrobert-Kreiten-Str. 13, 53115, Bonn, Germany.

Katharina Gutbrod (K)

Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, Karlrobert-Kreiten-Str. 13, 53115, Bonn, Germany.

Mazen Al-Bahra (M)

Kekulé-Institute of Organic Chemistry and Biochemistry, University of Bonn, Gerhard-Domagk-Str. 1, 53121, Bonn, Germany.

Dirk Menche (D)

Kekulé-Institute of Organic Chemistry and Biochemistry, University of Bonn, Gerhard-Domagk-Str. 1, 53121, Bonn, Germany.

Ngongeh Glory Amambo (NG)

Research Foundation for Tropical Diseases and the Environment (REFOTDE), Buea, Cameroon.
Parasite and Vector Research Unit (PAVRU), Department of Microbiology and Parasitology, University of Buea, Buea, Cameroon.

Fanny F Fombad (FF)

Research Foundation for Tropical Diseases and the Environment (REFOTDE), Buea, Cameroon.
Parasite and Vector Research Unit (PAVRU), Department of Microbiology and Parasitology, University of Buea, Buea, Cameroon.

Abdel Jelil Njouendou (AJ)

Research Foundation for Tropical Diseases and the Environment (REFOTDE), Buea, Cameroon.
Parasite and Vector Research Unit (PAVRU), Department of Microbiology and Parasitology, University of Buea, Buea, Cameroon.

Kenneth Pfarr (K)

Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Venusberg-Campus 1, 53127, Bonn, Germany. kenneth.pfarr@ukbonn.de.
German Center for Infection Research (DZIF), Partner Site Bonn-Cologne, Bonn, Germany. kenneth.pfarr@ukbonn.de.

Samuel Wanji (S)

Research Foundation for Tropical Diseases and the Environment (REFOTDE), Buea, Cameroon.
Parasite and Vector Research Unit (PAVRU), Department of Microbiology and Parasitology, University of Buea, Buea, Cameroon.

Achim Hoerauf (A)

Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Venusberg-Campus 1, 53127, Bonn, Germany. achim.hoerauf@ukbonn.de.
German Center for Infection Research (DZIF), Partner Site Bonn-Cologne, Bonn, Germany. achim.hoerauf@ukbonn.de.

Peter Dörmann (P)

Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, Karlrobert-Kreiten-Str. 13, 53115, Bonn, Germany. doermann@uni-bonn.de.

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