Point-of-care test of blood Plasmodium RNA within a Pasteur pipette using a novel isothermal amplification without nucleic acid purification.


Journal

Infectious diseases of poverty
ISSN: 2049-9957
Titre abrégé: Infect Dis Poverty
Pays: England
ID NLM: 101606645

Informations de publication

Date de publication:
31 Oct 2024
Historique:
received: 13 05 2024
accepted: 16 10 2024
medline: 31 10 2024
pubmed: 31 10 2024
entrez: 31 10 2024
Statut: epublish

Résumé

Resource-limited regions face a greater burden of infectious diseases due to limited access to molecular tests, complicating timely diagnosis and management. Current molecular point-of-care tests (POCTs) either come with high costs or lack adequate sensitivity and specificity. To facilitate better prevention and control of infectious diseases in underserved areas, we seek to address the need for molecular POCTs that better align with the World Health Organization (WHO)'s ASSURED criteria-Affordable, Sensitive, Specific, User-friendly, Rapid and robust, Equipment-free, and Deliverable to end users. A novel molecular POCT, Pasteur Pipette-assisted isothermal probe amplification (pp-IPA), was developed for malaria detection. Without any microfluidics, this method captures Plasmodium 18S rRNA in a modified Pasteur pipette using tailed genus-specific probes. After washing, the bound tailed probes are ligated to form a template for subsequent novel isothermal probe amplification using a pair of generic primers, bypassing nucleic acid extraction and reverse transcription. The method was assessed using cultured Plasmodium and compared with real-time quantitative reverse transcription PCR (RT-qPCR) or reverse transcription loop-mediated isothermal amplification (RT-LAMP) in clinical blood samples. The entire assay is completed in 60-80 min with minimal hands-on time, using only a Pasteur pipette and a water bath. The pp-IPA's analytical sensitivity is 1.28 × 10 Designed to improve the accessibility of molecular detection in resource-limited settings, pp-IPA's simplicity, affordability, high sensitivity/specificity, and minimal equipment requirements make it a promising point-of-care pathogen identification tool in resource-constrained regions.

Sections du résumé

BACKGROUND BACKGROUND
Resource-limited regions face a greater burden of infectious diseases due to limited access to molecular tests, complicating timely diagnosis and management. Current molecular point-of-care tests (POCTs) either come with high costs or lack adequate sensitivity and specificity. To facilitate better prevention and control of infectious diseases in underserved areas, we seek to address the need for molecular POCTs that better align with the World Health Organization (WHO)'s ASSURED criteria-Affordable, Sensitive, Specific, User-friendly, Rapid and robust, Equipment-free, and Deliverable to end users.
METHODS METHODS
A novel molecular POCT, Pasteur Pipette-assisted isothermal probe amplification (pp-IPA), was developed for malaria detection. Without any microfluidics, this method captures Plasmodium 18S rRNA in a modified Pasteur pipette using tailed genus-specific probes. After washing, the bound tailed probes are ligated to form a template for subsequent novel isothermal probe amplification using a pair of generic primers, bypassing nucleic acid extraction and reverse transcription. The method was assessed using cultured Plasmodium and compared with real-time quantitative reverse transcription PCR (RT-qPCR) or reverse transcription loop-mediated isothermal amplification (RT-LAMP) in clinical blood samples.
RESULTS RESULTS
The entire assay is completed in 60-80 min with minimal hands-on time, using only a Pasteur pipette and a water bath. The pp-IPA's analytical sensitivity is 1.28 × 10
CONCLUSIONS CONCLUSIONS
Designed to improve the accessibility of molecular detection in resource-limited settings, pp-IPA's simplicity, affordability, high sensitivity/specificity, and minimal equipment requirements make it a promising point-of-care pathogen identification tool in resource-constrained regions.

Identifiants

pubmed: 39478546
doi: 10.1186/s40249-024-01255-8
pii: 10.1186/s40249-024-01255-8
doi:

Substances chimiques

RNA, Protozoan 0
RNA, Ribosomal, 18S 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

80

Subventions

Organisme : National Major Science and Technology Projects of China
ID : 2018ZX10101001

Informations de copyright

© 2024. The Author(s).

Références

Burden of Disease. https://ourworldindata.org/burden-of-disease . Access 12 October 2024.
Land KJ, Boeras DI, Chen XS, Ramsay AR, Peeling RW. REASSURED diagnostics to inform disease control strategies, strengthen health systems and improve patient outcomes. Nat Microbiol. 2019;4(1):46–54.
doi: 10.1038/s41564-018-0295-3 pubmed: 30546093
Gavina K, Franco LC, Khan H, Lavik JP, Relich RF. Molecular point-of-care devices for the diagnosis of infectious diseases in resource-limited settings–A review of the current landscape, technical challenges, and clinical impact. J Clin Virol. 2023;169: 105613.
doi: 10.1016/j.jcv.2023.105613 pubmed: 37866094
Wang X, Hong XZ, Li YW, Li Y, Wang J, Chen P, et al. Microfluidics-based strategies for molecular diagnostics of infectious diseases. Mil Med Res. 2022;9(1):1–27.
Kaso AW, Hailu A. Costs and cost-effectiveness of Gene Xpert compared to smear microscopy for the diagnosis of pulmonary tuberculosis using real-world data from Arsi zone, Ethiopia. PLoS ONE. 2021;16(10): e0259056.
doi: 10.1371/journal.pone.0259056 pubmed: 34695153
DiDiodato G, Allen A, Bradbury N, Brown J, Cruise K, Jedrzejko C, et al. The efficacy of the BioFire FilmArray gastrointestinal panel to reduce hospital costs associated with contact isolation: a pragmatic randomized controlled trial. Cureus. 2022;14(8): e27931.
pubmed: 36120274
Mabey D, Peeling RW, Ustianowski A, Perkins MD. Diagnostics for the developing world. Nat Rev Microbiol. 2004;2(3):231–40.
doi: 10.1038/nrmicro841 pubmed: 15083158
Martinez AW, Phillips ST, Whitesides GM, Carrilho E. Diagnostics for the developing world: microfluidic paper-based analytical devices. Anal Chem. 2010;82(1):3–10.
doi: 10.1021/ac9013989 pubmed: 20000334
Hou Y, Lv CC, Guo YL, Ma XH, Liu W, Jin Y, et al. Recent advances and applications in paper-based devices for point-of-care testing. J Anal Test. 2022;6(3):247–73.
doi: 10.1007/s41664-021-00204-w pubmed: 35039787
Moehling TJ, Choi G, Dugan LC, Salit M, Meagher RJ. LAMP diagnostics at the point-of-care: emerging trends and perspectives for the developer community. Expert Rev Mol Diagn. 2021;21(1):43–61.
doi: 10.1080/14737159.2021.1873769 pubmed: 33474990
Jirawannaporn S, Limothai U, Tachaboon S, Dinhuzen J, Kiatamornrak P, Chaisuriyong W, et al. Rapid and sensitive point-of-care detection of Leptospira by RPA-CRISPR/Cas12a targeting lipL32. PLoS Negl Trop Dis. 2022;16(1): e0010112.
doi: 10.1371/journal.pntd.0010112 pubmed: 34990457
Subsoontorn P, Lohitnavy M, Kongkaew C. The diagnostic accuracy of isothermal nucleic acid point-of-care tests for human coronaviruses: a systematic review and meta-analysis. Sci Rep. 2020;10(1):22349.
doi: 10.1038/s41598-020-79237-7 pubmed: 33339871
Atceken N, Munzer Alseed M, Dabbagh SR, Yetisen AK, Tasoglu S. Point-of-care diagnostic platforms for loop-mediated isothermal amplification. Adv Eng Mater. 2023;25(8):2201174.
doi: 10.1002/adem.202201174
Wong YP, Othman S, Lau YL, Radu S, Chee HY. Loop-mediated isothermal amplification (LAMP): a versatile technique for detection of micro-organisms. J Appl Microbiol. 2018;124(3):626–43.
doi: 10.1111/jam.13647 pubmed: 29165905
Iacobucci G. Covid-19: Rapid test missed over 50% of positive cases in Manchester pilot. BMJ. 2020;371: m4323.
doi: 10.1136/bmj.m4323 pubmed: 33158908
Kim SH, Lee SY, Kim U, Oh SW. Diverse methods of reducing and confirming false-positive results of loop-mediated isothermal amplification assays: a review. Anal Chim Acta. 2023:341693.
Xu G, Nolder D, Reboud J, Oguike MC, van Schalkwyk DA, Sutherland CJ, et al. Paper-origami-based multiplexed malaria diagnostics from whole blood. Angew Chem Int Ed Engl. 2016;128(49):15476–9.
doi: 10.1002/ange.201606060
Rodriguez NM, Wong WS, Liu L, Dewar R, Klapperich CM. A fully integrated paperfluidic molecular diagnostic chip for the extraction, amplification, and detection of nucleic acids from clinical samples. Lab Chip. 2016;16(4):753–63.
doi: 10.1039/C5LC01392E pubmed: 26785636 pmcid: 4747825
Khaliliazar S, Toldrà A, Chondrogiannis G, Hamedi MM. Electroanalytical paper-based nucleic acid amplification biosensors with integrated thread electrodes. Anal Chem. 2021;93(42):14187–95.
doi: 10.1021/acs.analchem.1c02900 pubmed: 34648274 pmcid: 8552215
Kang J, Li Y, Zhao Y, Wang Y, Ma C, Shi C. Nucleic acid extraction without electrical equipment via magnetic nanoparticles in Pasteur pipettes for pathogen detection. Anal Biochem. 2021;635: 114445.
doi: 10.1016/j.ab.2021.114445 pubmed: 34740597
Liu S, Wei M, Liu R, Kuang S, Shi C, Ma C. Lab in a Pasteur pipette: low-cost, rapid and visual detection of Bacillus cereu using denaturation bubble-mediated strand exchange amplification. Anal Chim Acta. 2019;1080:162–9.
doi: 10.1016/j.aca.2019.07.011 pubmed: 31409466
Cheng Z, Wang D, Tian X, Sun Y, Sun X, Xiao N, et al. Capture and ligation probe-PCR (CLIP-PCR) for molecular screening, with application to active malaria surveillance for elimination. Clin Chem. 2015;61(6):821–8.
doi: 10.1373/clinchem.2014.237115 pubmed: 25964304
Koepfli C, Nguitragool W, Hofmann NE, Robinson LJ, Ome-Kaius M, Sattabongkot J, et al. Sensitive and accurate quantification of human malaria parasites using droplet digital PCR (ddPCR). Sci Rep. 2016;6(1):39183.
doi: 10.1038/srep39183 pubmed: 27982132
Xu Z, Peng Y, Yang M, Li X, Wang J, Zou R, et al. Simultaneous detection of Zika, chikungunya, dengue, yellow fever, West Nile, and Japanese encephalitis viruses by a two-tube multiplex real-time RT-PCR assay. J Med Virol. 2022;94(6):2528–36.
doi: 10.1002/jmv.27658 pubmed: 35146775
Christensen P, Bozdech Z, Watthanaworawit W, Imwong M, Rénia L, Malleret B, et al. Reverse transcription PCR to detect low density malaria infections. Wellcome Open Res. 2021;6:39.
Mohon AN, Getie S, Jahan N, Alam MS, Pillai DR. Ultrasensitive loop mediated isothermal amplification (US-LAMP) to detect malaria for elimination. Malar J. 2019;18:1–10.
doi: 10.1186/s12936-019-2979-4
Linnes JC, Fan A, Rodriguez NM, Lemieux B, Kong H, Klapperich CM. Paper-based molecular diagnostic for Chlamydia trachomatis. RSC Adv. 2014;4(80):42245–51.
doi: 10.1039/C4RA07911F pubmed: 25309740
Ridley J. Pipetting and use of glassware. In: Dave G, editor. Essentials of clinical laboratory science. New York: Delmar; 2010. p. 185–205.
Eichhorn SJ, Sampson WW. Relationships between specific surface area and pore size in electrospun polymer fibre networks. J R Soc Interface. 2010;7(45):641–9.
doi: 10.1098/rsif.2009.0374 pubmed: 19812071
Xu G, Hu L, Zhong H, Wang H, Yusa S, Weiss TC, et al. Cross priming amplification: mechanism and optimization for isothermal DNA amplification. Sci Rep. 2012;2(1):246.
doi: 10.1038/srep00246 pubmed: 22355758
Shi C, Shang F, Zhou M, Zhang P, Wang Y, Ma C. Triggered isothermal PCR by denaturation bubble-mediated strand exchange amplification. Chem Commun (Camb). 2016;52(77):11551–4.
doi: 10.1039/C6CC05906F pubmed: 27602549
Zhang Y, Zhang L, Sun J, Liu Y, Ma X, Cui S, et al. Point-of-care multiplexed assays of nucleic acids using microcapillary-based loop-mediated isothermal amplification. Anal Chem. 2014;86(14):7057–62.
doi: 10.1021/ac5014332 pubmed: 24937125
Lalremruata A, Nguyen TT, McCall MBB, Mombo-Ngoma G, Agnandji ST, Adegnika AA, et al. Recombinase polymerase amplification and lateral flow assay for ultrasensitive detection of low-density Plasmodium falciparum infection from controlled human malaria infection studies and naturally acquired infections. J Clin Microbiol. 2020;58(5):10–1128.
doi: 10.1128/JCM.01879-19
Colbert AJ, Co K, Lima-Cooper G, Lee DH, Clayton KN, Wereley ST, et al. Towards the use of a smartphone imaging-based tool for point-of-care detection of asymptomatic low-density malaria parasitaemia. Malar J. 2021;20(1):1–13.
doi: 10.1186/s12936-021-03894-w
Vincent JP, Komaki-Yasuda K, Iwagami M, Kawai S, Kano S. Combination of PURE-DNA extraction and LAMP-DNA amplification methods for accurate malaria diagnosis on dried blood spots. Malar J. 2018;17(1):1–7.
doi: 10.1186/s12936-018-2527-7
Reboud J, Xu G, Garrett A, Adriko M, Yang Z, Tukahebwa EM, et al. Paper-based microfluidics for DNA diagnostics of malaria in low resource underserved rural communities. Proc Natl Acad Sci U S A. 2019;116(11):4834–42.
doi: 10.1073/pnas.1812296116 pubmed: 30782834
Choi G, Prince T, Miao J, Cui L, Guan W. Sample-to-answer palm-sized nucleic acid testing device towards low-cost malaria mass screening. Biosens Bioelectron. 2018;115:83–90.
doi: 10.1016/j.bios.2018.05.019 pubmed: 29803865
De Koninck A-S, Cnops L, Hofmans M, Jacobs J, Van den Bossche D, Philippé J. Diagnostic performance of the loop-mediated isothermal amplification (LAMP) based illumigene® malaria assay in a non-endemic region. Malar J. 2017;16:1–9.
doi: 10.1186/s12936-017-2065-8
Lin H, Zhao S, Liu Y, Shao L, Ye Y, Jiang N, et al. Rapid visual detection of Plasmodium using recombinase-aided amplification with lateral flow dipstick assay. Front Cell Infect Microbiol. 2022;12: 922146.
doi: 10.3389/fcimb.2022.922146 pubmed: 35811679
Lai MY, Lau YL. Detection of Plasmodium knowlesi using recombinase polymerase amplification (RPA) combined with SYBR Green I. Acta Trop. 2020;208: 105511.
doi: 10.1016/j.actatropica.2020.105511 pubmed: 32422380
Lee RA, Puig HD, Nguyen PQ, Angenent-Mari NM, Donghia NM, McGee JP, et al. Ultrasensitive CRISPR-based diagnostic for field-applicable detection of Plasmodium species in symptomatic and asymptomatic malaria. Proc Natl Acad Sci U S A. 2020;117(41):25722–31.
doi: 10.1073/pnas.2010196117 pubmed: 32958655

Auteurs

Lyu Xie (L)

Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences, School of Basic Medicine, Peking Union Medical College, No. 5, Dongdansantiao, Dongcheng District, Beijing, 10005, China.

Jiyu Xu (J)

Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences, School of Basic Medicine, Peking Union Medical College, No. 5, Dongdansantiao, Dongcheng District, Beijing, 10005, China.

Lihua Fan (L)

Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences, School of Basic Medicine, Peking Union Medical College, No. 5, Dongdansantiao, Dongcheng District, Beijing, 10005, China.

Xiaodong Sun (X)

Yunnan Institute of Parasitic Diseases & Yunnan Provincial Centre of Malaria Research, Pu'er, China.

Zhi Zheng (Z)

Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences, School of Basic Medicine, Peking Union Medical College, No. 5, Dongdansantiao, Dongcheng District, Beijing, 10005, China. zhizheng100@126.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH