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Recent advances in nucleic acid-based methods for detection of helminth infections and the perspective of biosensors for future development

Published online by Cambridge University Press:  16 December 2019

Hanif Ullah ,
Abdul Qadeer ,
Muhammad Rashid Open the ORCID record for Muhammad Rashid [Opens in a new window] ,
Muhammad Imran Rashid  and
Guofeng Cheng Open the ORCID record for Guofeng Cheng [Opens in a new window]
Hanif Ullah
Affiliation:
Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Animal Parasitology of Ministry of Agriculture and Rural Affairs, Shanghai, 200241, China
Abdul Qadeer
Affiliation:
Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Animal Parasitology of Ministry of Agriculture and Rural Affairs, Shanghai, 200241, China
Muhammad Rashid
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu730046, China
Muhammad Imran Rashid
Affiliation:
Department of Parasitology, University of Veterinary and Animal Sciences (UVAS), Lahore, Pakistan.
Guofeng Cheng*
Affiliation:
Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Animal Parasitology of Ministry of Agriculture and Rural Affairs, Shanghai, 200241, China
*
Author for correspondence: Guofeng Cheng, E-mail: [email protected]
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Abstract

Pathogenic helminth infections are responsible for severe health problems and economic losses worldwide. Timely and accurate diagnosis of helminth infections is critical for adopting suitable strategies for pathogen control. Here, we review recent advances in nucleic acid-based diagnostic methods, including polymerase chain reaction, quantitative qPCR, loop-mediated isothermal amplification and recombinase polymerase amplification, and discuss their advantages and disadvantages for diagnosing helminth infections. In addition, we highlight recent advances in biosensors for the detection of nucleic acid biomarkers that can potentially be used for the diagnosis of helminth infection.

Keywords

Biosensordiagnosishelminthsinfectionnucleic acids
Type
Review Article
Information
Parasitology , Volume 147 , Issue 4 , April 2020 , pp. 383 - 392
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Copyright
Copyright © Cambridge University Press 2019

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References

Abbasi, I, King, CH, Muchiri, EM and Hamburger, J (2010) Detection of Schistosoma mansoni and Schistosoma haematobium DNA by loop-mediated isothermal amplification: identification of infected snails from early prepatency. American Journal of Tropical Medicine and Hygiene 83, 427–432.CrossRefGoogle ScholarPubMed
Agarwal, M, Tomar, RS and Jyoti, A (2014) Detection of water-borne pathogenic bacteria: where molecular methods rule. International Journal of Multidisciplinary and Current Research 2, 351–358.Google Scholar
Ajibola, O, Gulumbe, B, Eze, A and Obishakin, E (2018) Tools for detection of schistosomiasis in resource limited settings. Medical Sciences 6, 39.CrossRefGoogle ScholarPubMed
Alhamoud, Y, Yang, D, Kenston, SSF, Liu, G, Liu, L, Zhou, H, Ahmed, F and Zhao, J (2019) Advances in biosensors for the detection of ochratoxin A: bio-receptors, nanomaterials, and their applications. Biosensors and Bioelectronics 141, 111418.CrossRefGoogle ScholarPubMed
Almeida, M, Bishop, H, Nascimento, FS, Mathison, B, Bradbury, RS and Silva, AD (2018) Multiplex TaqMan qPCR assay for specific identification of encapsulated Trichinella species prevalent in North America. Memorias do Instituto Oswaldo Cruz 113, e180305.CrossRefGoogle ScholarPubMed
Amoah, ID, Singh, G, Stenstrom, TA and Reddy, P (2017) Detection and quantification of soil-transmitted helminths in environmental samples: a review of current state-of-the-art and future perspectives. Acta Tropica 169, 187–201.CrossRefGoogle ScholarPubMed
Basuni, M, Muhi, J, Othman, N, Verweij, JJ, Ahmad, M, Miswan, N, Rahumatullah, A, Aziz, FA, Zainudin, NS and Noordin, R (2011) A pentaplex real-time polymerase chain reaction assay for detection of four species of soil-transmitted helminths. American Journal of Tropical Medicine and Hygiene 84, 338–343.CrossRefGoogle ScholarPubMed
Bonnefond, S, Cnops, L, Duvignaud, A, Bottieau, E, Pistone, T, Clerinx, J and Malvy, D (2019) Early complicated schistosomiasis in a returning traveller: key contribution of new molecular diagnostic methods. International Journal of Infectious Diseases 79, 72–74.CrossRefGoogle Scholar
Bora, U, Sett, A and Singh, D (2013) Nucleic acid based biosensors for clinical applications. Biosensors Journal 1, 104.Google Scholar
Bouguelia, S, Roupioz, Y, Slimani, S, Mondani, L, Casabona, MG, Durmort, C, Vernet, T, Calemczuk, R and Livache, T (2013) On-chip microbial culture for the specific detection of very low levels of bacteria. Lab on a Chip 13, 4024–4032.CrossRefGoogle ScholarPubMed
Cai, P, Weerakoon, KG, Mu, Y, Olveda, RM, Ross, AG, Olveda, DU and McManus, DP (2019) Comparison of Kato–Katz, antibody-based ELISA and droplet digital PCR diagnosis of schistosomiasis japonica: lessons learnt from a setting of low infection intensity. PLoS Neglected Tropical Diseases 13, e0007228.CrossRefGoogle ScholarPubMed
Cai, X-Q, Yu, H-Q, Li, R, Yue, Q-Y, Liu, G-H, Bai, J-S, Deng, Y, Qiu, D-Y and Zhu, X-Q (2014) Rapid detection and differentiation of Clonorchis sinensis and Opisthorchis viverrini using real-time PCR and high resolution melting analysis. The Scientific World Journal 2014, 893981.CrossRefGoogle ScholarPubMed
Chaya, D and Parija, SC (2014) Performance of polymerase chain reaction for the diagnosis of cystic echinococcosis using serum, urine, and cyst fluid samples. Tropical Parasitology 4, 43.Google Scholar
Chen, M, Ai, L, Zhang, R, Xia, J, Wang, K, Chen, S, Zhang, Y, Xu, M, Li, X and Zhu, X (2011) Sensitive and rapid detection of Paragonimus westermani infection in humans and animals by loop-mediated isothermal amplification (LAMP). Parasitology Research 108, 1193–1198.CrossRefGoogle Scholar
Cheng, G (2015) Circulating miRNAs: roles in cancer diagnosis, prognosis and therapy. Advanced Drug Delivery Reviews 81, 75–93.CrossRefGoogle Scholar
Cheng, CW, Chen, CK, Chen, YS and Chen, LY (2008) Determination of Schistosoma japonicum circulating antigens in dilution serum by piezoelectric immunosensor and S/N enhancement. Biosensors & Bioelectronics 24, 136–140.CrossRefGoogle ScholarPubMed
Cheng, G, Luo, R, Hu, C, Cao, J and Jin, Y (2013) Deep sequencing-based identification of pathogen-specific microRNAs in the plasma of rabbits infected with Schistosoma japonicum. Parasitology 140, 1751–1761.CrossRefGoogle ScholarPubMed
Clark, LC Jr and Lyons, C (1962) Electrode systems for continuous monitoring in cardiovascular surgery. Annals of the New York Academy of Sciences 102, 29–45.CrossRefGoogle ScholarPubMed
Chung, J, Kang, JS, Jurng, JS, Jung, JH and Kim, BC (2015) Fast and continuous microorganism detection using aptamer-conjugated fluorescent nanoparticles on an optofluidic platform. Biosensors & Bioelectronics 67, 303–308.CrossRefGoogle Scholar
Corrado, M, James Lacourse, E, Lisa, R and Stothard, JR (2016) Focusing nucleic acid-based molecular diagnostics and xenomonitoring approaches for human helminthiases amenable to preventive chemotherapy. Parasitology Open 2, 1–17.Google Scholar
Daher, RK, Stewart, G, Boissinot, M and Bergeron, MG (2016) Recombinase polymerase amplification for diagnostic applications. Clinical Chemistry 62, 947–958.CrossRefGoogle ScholarPubMed
Deng, M-H, Zhong, L-Y, Kamolnetr, O, Limpanont, Y and Lv, Z-Y (2019) Detection of helminths by loop-mediated isothermal amplification assay: a review of updated technology and future outlook. Infectious Diseases of Poverty 8, 20.CrossRefGoogle ScholarPubMed
Diguta, CF, Rousseaux, S, Weidmann, S, Bretin, N, Vincent, B, Guilloux-Benatier, M and Alexandre, H (2010) Development of a qPCR assay for specific quantification of Botrytis cinerea on grapes. FEMS Microbiology Letters 313, 81–87.CrossRefGoogle ScholarPubMed
Elmahalawy, ST, Halvarsson, P, Skarin, M and Hoglund, J (2018) Droplet digital polymerase chain reaction (ddPCR) as a novel method for absolute quantification of major gastrointestinal nematodes in sheep. Veterinary Parasitology 261, 1–8.CrossRefGoogle Scholar
Enk, MJ, e Silva, GO and Rodrigues, NB (2012) Diagnostic accuracy and applicability of a PCR system for the detection of Schistosoma mansoni DNA in human urine samples from an endemic area. PLoS ONE 7, e38947.CrossRefGoogle ScholarPubMed
Euler, M, Wang, Y, Nentwich, O, Piepenburg, O, Hufert, FT and Weidmann, M (2012) Recombinase polymerase amplification assay for rapid detection of rift valley fever virus. Journal of clinical virology 54, 308–312.CrossRefGoogle ScholarPubMed
Feng, K, Li, W, Guo, Z, Duo, H, Fu, Y, Shen, X, Tie, C, C, XIAO, Y, LUO and G, QI (2017) Development of LAMP assays for the molecular detection of taeniid infection in canine in Tibetan rural area. Journal of Veterinary Medical Science 79, 1986–1993.CrossRefGoogle ScholarPubMed
Fernández-Soto, P, Arahuetes, JG, Hernández, AS, Abán, JL, Santiago, BV and Muro, A (2014) A loop-mediated isothermal amplification (LAMP) assay for early detection of Schistosoma mansoni in stool samples: a diagnostic approach in a murine model. PLoS Neglected Tropical Diseases 8, e3126.CrossRefGoogle ScholarPubMed
Fink, DL, Kamgno, J and Nutman, TB (2011) Rapid molecular assays for specific detection and quantitation of Loa loa microfilaremia. PLoS Neglected Tropical Diseases 5, e1299.CrossRefGoogle ScholarPubMed
Fischer, P, Supali, T, Wibowo, H, Bonow, I and Williams, SA (2000) Detection of DNA of nocturnally periodic Brugia malayi in night and day blood samples by a polymerase chain reaction-ELISA-based method using an internal control DNA. American Journal of Tropical Medicine and Hygiene 62, 291–296.CrossRefGoogle ScholarPubMed
Flores, MD, Gonzalez, LM, Hurtado, C, Motta, YM, Domínguez-Hidalgo, C, Merino, FJ, Perteguer, MJ and Gárate, T (2018) HDP2: a ribosomal DNA (NTS-ETS) sequence as a target for species-specific molecular diagnosis of intestinal taeniasis in humans. Parasites & Vectors 11, 117.CrossRefGoogle ScholarPubMed
Fracchiolla, NS, Artuso, S and Cortelezzi, A (2013) Biosensors in clinical practice: focus on oncohematology. Sensors 13, 6423–6447.CrossRefGoogle ScholarPubMed
Fung, MS, Xiao, N, Wang, S and Carlton, EJ (2012) Field evaluation of a PCR test for Schistosoma japonicum egg detection in low-prevalence regions of China. American Journal of Tropical Medicine and Hygiene 87, 1053–1058.CrossRefGoogle ScholarPubMed
Gandasegui, J, Fernández-Soto, P, Carranza-Rodríguez, C, Pérez-Arellano, JL, Vicente, B, López-Abán, J and Muro, A (2015) The rapid-heat LAMPellet method: a potential diagnostic method for human urogenital schistosomiasis. PLoS Neglected Tropical Diseases 9, e0003963.CrossRefGoogle ScholarPubMed
Gobert, GN, Chai, M, Duke, M and McManus, DP (2005) Copro-PCR based detection of Schistosoma Eggs using mitochondrial DNA markers. Molecular and Cellular Probes 19, 250–254.CrossRefGoogle ScholarPubMed
Gordon, CA, Acosta, LP, Gray, DJ, Olveda, RM, Jarilla, B, Gobert, GN, Ross, AG and McManus, DP (2012) High prevalence of Schistosoma japonicum infection in Carabao from Samar province, the Philippines: implications for transmission and control. PLoS Neglected Tropical Diseases 6, e1778.CrossRefGoogle ScholarPubMed
Gordon, CA, McManus, DP, Acosta, LP, Olveda, RM, Williams, GM, Ross, AG, Gray, DJ and Gobert, GN (2015) Multiplex real-time PCR monitoring of intestinal helminths in humans reveals widespread polyparasitism in Northern Samar, the Philippines. International Journal for Parasitology 45, 477–483.CrossRefGoogle ScholarPubMed
Gutierrez-Aguirre, I, Racki, N, Dreo, T and Ravnikar, M (2015) Droplet digital PCR for absolute quantification of pathogens. Methods in Molecular Biology 1302, 331–347.CrossRefGoogle ScholarPubMed
Hajia, M, Rahbar, M, Farzami, MR, Dolatyar, A, Imani, M, Saburian, R and Farzanehkhah, M (2014) Efficacy of multiplex PCR procedure for Iranian Streptococcus pneumoniae isolates. Caspian Journal of Internal Medicine 5, 109.Google ScholarPubMed
Hawkins, SFC and Guest, PC (2017) Multiplex analyses using real-time quantitative PCR. In Guest P (ed.), Multiplex Biomarker Techniques. Methods in Molecular Biology. New York: Humana Press, pp. 125–133.CrossRefGoogle Scholar
He, P, Gordon, CA, Williams, GM, Li, Y, Wang, Y, Hu, J, Gray, DJ, Ross, AG, Harn, D and McManus, DP (2018) Real-time PCR diagnosis of Schistosoma japonicum in low transmission areas of China. Infectious Diseases of Poverty 7, 8.CrossRefGoogle ScholarPubMed
Hernández, M, Gonzalez, L, Fleury, A, Saenz, B, Parkhouse, R, Harrison, L, Garate, T and Sciutto, E (2008) Neurocysticercosis: detection of Taenia solium DNA in human cerebrospinal fluid using a semi-nested PCR based on HDP2. Annals of Tropical Medicine & Parasitology 102, 317–323.CrossRefGoogle ScholarPubMed
Hinz, R, Schwarz, NG, Hahn, A and Frickmann, H (2017) Serological approaches for the diagnosis of schistosomiasis – a review. Molecular and Cellular Probes 31, 2–21.CrossRefGoogle Scholar
Hong, C-Y, Chen, X, Liu, T, Li, J, Yang, H-H, Chen, J-H and Chen, G-N (2013) Ultrasensitive electrochemical detection of cancer-associated circulating microRNA in serum samples based on DNA concatamers. Biosensors and Bioelectronics 50, 132–136.CrossRefGoogle ScholarPubMed
Hoy, AM, Lundie, RJ, Ivens, A, Quintana, JF, Nausch, N, Forster, T, Jones, F, Kabatereine, NB, Dunne, DW and Mutapi, F (2014) Parasite-derived microRNAs in host serum as novel biomarkers of helminth infection. PLoS Neglected Tropical Diseases 8, e2701.CrossRefGoogle ScholarPubMed
Hsieh, K, Mage, PL, Csordas, AT, Eisenstein, M and Soh, HT (2014) Simultaneous elimination of carryover contamination and detection of DNA with uracil-DNA-glycosylase-supplemented loop-mediated isothermal amplification (UDG-LAMP). Chemical Communications 50, 3747–3749.CrossRefGoogle Scholar
Hussein, HM, El-Tonsy, MM, Tawfik, RA and Ahmed, SA-E-G (2012) Experimental study for early diagnosis of prepatent schistosomiasis mansoni by detection of free circulating DNA in serum. Parasitology Research 111, 475–478.CrossRefGoogle ScholarPubMed
Ibironke, OA, Phillips, AE, Garba, A, Lamine, SM and Shiff, C (2011) Diagnosis of Schistosoma haematobium by detection of specific DNA fragments from filtered urine samples. American Journal of Tropical Medicine and Hygiene 84, 998–1001.CrossRefGoogle ScholarPubMed
Ittarat, W, Chomean, S, Sanchomphu, C, Wangmaung, N, Promptmas, C and NgrenngarmLert, W (2013) Biosensor as a molecular malaria differential diagnosis. Clinica Chimica Acta 419, 47–51.CrossRefGoogle ScholarPubMed
Janissen, R, Sahoo, PK, Santos, CA, da Silva, AM, von Zuben, AA, Souto, DE, Costa, AD, Celedon, P, Zanchin, NI and Almeida, DB (2017) Inp nanowire biosensor with tailored biofunctionalization: ultrasensitive and highly selective disease biomarker detection. Nano Letters 17, 5938–5949.CrossRefGoogle ScholarPubMed
Jeon, H-K and Eom, KS (2013) Molecular approaches to Taenia asiatica. The Korean Journal of Parasitology 51, 1.CrossRefGoogle ScholarPubMed
Jeon, H-K, Yong, T-S, Sohn, W-M, Chai, J-Y, Hong, S-J, Han, E-T, Jeong, H-G, Chhakda, T, Sinuon, M and Socheat, D (2011) Molecular identification of Taenia Tapeworms by Cox1 gene in Koh Kong, Cambodia. The Korean Journal of Parasitology 49, 195.CrossRefGoogle Scholar
Jongthawin, J, Intapan, PM, Lulitanond, V, Sanpool, O, Thanchomnang, T, Sadaow, L and Maleewong, W (2016) Detection and quantification of Wuchereria bancrofti and Brugia malayi DNA in blood samples and mosquitoes using duplex droplet digital polymerase chain reaction. Parasitology Research 115, 2967–2972.CrossRefGoogle ScholarPubMed
Kagai, J, Mpoke, S, Muli, F, Hamburger, J and Kenya, E (2008) Molecular technique utilising sputum for detecting Wuchereria bancrofti infections in Malindi, Kenya. East African Medical Journal 85, 118–122.Google ScholarPubMed
Kaliappan, SP, George, S, Francis, MR, Kattula, D, Sarkar, R, Minz, S, Mohan, VR, George, K, Roy, S and Ajjampur, SSR (2013) Prevalence and clustering of soil-transmitted helminth infections in a tribal area in southern India. Tropical Medicine & International Health 18, 1452–1462.CrossRefGoogle Scholar
Kato-Hayashi, N, Kirinoki, M, Iwamura, Y, Kanazawa, T, Kitikoon, V, Matsuda, H and Chigusa, Y (2010) Identification and differentiation of human schistosomes by polymerase chain reaction. Experimental Parasitology 124, 325–329.CrossRefGoogle ScholarPubMed
Kato-Hayashi, N, Leonardo, LR, Arevalo, NL, Tagum, MNB, Apin, J, Agsolid, LM, Chua, JC, Villacorte, EA, Kirinoki, M and Kikuchi, M (2015) Detection of active schistosome infection by cell-free circulating DNA of Schistosoma japonicum in highly endemic areas in Sorsogon Province, the Philippines. Acta Tropica 141, 178–183.CrossRefGoogle ScholarPubMed
Khoshakhlagh, P, Spotin, A, Mahami-Oskouei, M, Shahbazi, A and Ozlati, M (2017) Loop-mediated isothermal amplification as a reliable assay for Toxocara canis infection in pet dogs. Parasitology Research 116, 2591–2597.CrossRefGoogle ScholarPubMed
Lier, T, Simonsen, GS, Wang, T, Lu, D, Haukland, HH, Vennervald, BJ, Hegstad, J and Johansen, MV (2009) Real-time polymerase chain reaction for detection of low-intensity Schistosoma japonicum infections in China. American Journal of Tropical Medicine and Hygiene 81, 428–432.CrossRefGoogle ScholarPubMed
Liu, J, Gratz, J, Amour, C, Kibiki, G, Becker, S, Janaki, L, Verweij, JJ, Taniuchi, M, Sobuz, SU and Haque, R (2013) A laboratory-developed TaqMan array card for simultaneous detection of 19 enteropathogens. Journal of Clinical Microbiology 51, 472–480.CrossRefGoogle ScholarPubMed
Lodh, N, Mikita, K, Bosompem, KM, Anyan, WK, Quartey, JK, Otchere, J and Shiff, CJ (2017) Point of care diagnosis of multiple schistosome parasites: species-specific DNA detection in urine by loop-mediated isothermal amplification (LAMP). Acta Tropica 173, 125–129.CrossRefGoogle Scholar
Lodh, N, Naples, JM, Bosompem, KM, Quartey, J and Shiff, CJ (2014) Detection of parasite-specific DNA in urine sediment obtained by filtration differentiates between single and mixed infections of Schistosoma mansoni and S. haematobium from endemic areas in Ghana. PLoS ONE 9, e91144.CrossRefGoogle ScholarPubMed
Luz, JG, Souto, DE, Machado-Assis, GF, de Lana, M, Luz, RC, Martins-Filho, OA, Damos, FS and Martins, HR (2016) Applicability of a novel immunoassay based on surface plasmon resonance for the diagnosis of Chagas disease. Clinica Chimica Acta 454, 39–45.CrossRefGoogle Scholar
Mejia, R, Vicuña, Y, Broncano, N, Sandoval, C, Vaca, M, Chico, M, Cooper, PJ and Nutman, TB (2013) A novel, multi-parallel, real-time polymerase chain reaction approach for eight gastrointestinal parasites provides improved diagnostic capabilities to resource-limited at-risk populations. American Journal of Tropical Medicine and Hygiene 88, 1041–1047.CrossRefGoogle ScholarPubMed
Meningher, T, Lerman, G, Regev-Rudzki, N, Gold, D, Ben-Dov, IZ, Sidi, Y, Avni, D and Schwartz, E (2017) Schistosomal MicroRNAs isolated from extracellular vesicles in sera of infected patients: a new tool for diagnosis and follow-up of human schistosomiasis. Journal of Infectious Diseases 215, 378–386.Google ScholarPubMed
Meurs, L, Brienen, E, Mbow, M, Ochola, EA, Mboup, S, Karanja, DM, Secor, WE, Polman, K and van Lieshout, L (2015) Is PCR the next reference standard for the diagnosis of Schistosoma in stool? A comparison with microscopy in Senegal and Kenya. PLoS Neglected Tropical Disease 9, e0003959.CrossRefGoogle Scholar
Michelet, L, Fleury, A, Sciutto, E, Kendjo, E, Fragoso, G, Paris, L and Bouteille, B (2011) Human neurocysticercosis: comparison of different diagnostic tests using cerebrospinal fluid. Journal of Clinical Microbiology 49, 195–200.CrossRefGoogle ScholarPubMed
Minetti, C, Lacourse, EJ, Reimer, L and Stothard, JR (2016) Focusing nucleic acid-based molecular diagnostics and xenomonitoring approaches for human helminthiases amenable to preventive chemotherapy. Parasitology Open 2, e16.CrossRefGoogle Scholar
Mohan, S, Srivastava, P, Maheshwari, S, Sundar, S and Prakash, R (2011) Nano-structured nickel oxide based DNA biosensor for detection of visceral leishmaniasis (kala-azar). The Analyst 136, 2845–2851.CrossRefGoogle Scholar
Moradi, M, Sattarahmady, N, Rahi, A, Hatam, GR, Sorkhabadi, SMR and Heli, H (2016) A label-free, PCR-free and signal-on electrochemical DNA biosensor for Leishmania major based on gold nanoleaves. Talanta 161, 48–53.CrossRefGoogle ScholarPubMed
Morales-Hojas, R, Post, RJ, Shelley, AJ, Maia-Herzog, M, Coscarón, S and Cheke, RA (2001) Characterisation of nuclear ribosomal DNA sequences from Onchocerca volvulus and Mansonella ozzardi (Nematoda: Filarioidea) and development of a PCR-based method for their detection in skin biopsies. International Journal for Parasitology 31, 169–177.CrossRefGoogle ScholarPubMed
Mori, Y and Notomi, T (2020) Loop-mediated isothermal amplification (LAMP): Expansion of its practical application as a tool to achieve universal health coverage. Journal of Infection and Chemotherapy 26, 13–17.CrossRefGoogle ScholarPubMed
Mugambi, RM, Agola, EL, Mwangi, IN, Kinyua, J, Shiraho, EA and Mkoji, GM (2015) Development and evaluation of a loop mediated isothermal amplification (LAMP) technique for the detection of hookworm (Necator americanus) infection in fecal samples. Parasites & Vectors 8, 574.CrossRefGoogle ScholarPubMed
Ngui, R, Lim, YA and Chua, KH (2012) Rapid detection and identification of human hookworm infections through high resolution melting (HRM) analysis. PLoS ONE 7, e41996.CrossRefGoogle ScholarPubMed
Nie, J, Zhang, Y, Wang, H, Wang, S and Shen, G (2012) Superhydrophobic surface-based magnetic electrochemical immunoassay for detection of Schistosoma japonicum antibodies. Biosensors & Bioelectronics 33, 23–28.CrossRefGoogle ScholarPubMed
O'Connell, EM and Nutman, TB (2016a) Molecular diagnostics for soil-transmitted helminths. American Journal of Tropical Medicine and Hygiene, 95, 508–513.CrossRefGoogle Scholar
O'Connell, EM and Nutman, TB (2016b) Molecular diagnostics for soil-transmitted helminths. American Journal of Tropical Medicine and Hygiene, 95, 508–513.CrossRefGoogle Scholar
Pak, BJ, Vasquez-Camargo, F, Kalinichenko, E, Chiodini, PL, Nutman, TB, Tanowitz, HB, McAuliffe, I, Wilkins, P, Smith, PT, Ward, BJ, Libman, MD and Ndao, M (2014) Development of a rapid serological assay for the diagnosis of strongyloidiasis using a novel diffraction-based biosensor technology PLoS Neglected Tropical Diseases 8, e3002.CrossRefGoogle Scholar
Papaiakovou, M, Gasser, RB and Littlewood, DTJ (2019) Quantitative PCR-based diagnosis of soil-transmitted helminth infections: faecal or fickle? Trends in Parasitology 35, 491–500.CrossRefGoogle ScholarPubMed
Phuphisut, O, Yoonuan, T, Sanguankiat, S, Chaisiri, K, Maipanich, W, Pubampen, S, Komalamisra, C and Adisakwattana, P (2014) Triplex polymerase chain reaction assay for detection of major soil-transmitted helminths, Ascaris lumbricoides, Trichuris trichiura, Necator americanus, in fecal samples. Southeast Asian Journal of Tropical Medicine and Public Health 45, 267.Google ScholarPubMed
Piepenburg, O, Williams, CH, Stemple, DL and Armes, NA (2006) DNA Detection using recombination proteins. PLoS biology 4, e204.CrossRefGoogle ScholarPubMed
Plichart, C and Lemoine, A (2013) Monitoring and evaluation of lymphatic filariasis interventions: an improved PCR-based pool screening method for high throughput Wuchereria bancrofti detection using dried blood spots. Parasites & Vectors 6, 110.CrossRefGoogle ScholarPubMed
Poole, CB, Tanner, NA, Zhang, Y, Evans, TC Jr and Carlow, CK (2012) Diagnosis of Brugian filariasis by loop-mediated isothermal amplification. PLoS Neglected Tropical Diseases 6, e1948.CrossRefGoogle ScholarPubMed
Poulton, K and Webster, B (2018) Development of a lateral flow recombinase polymerase assay for the diagnosis of Schistosoma mansoni infections. Analytical Biochemistry 546, 65–71.CrossRefGoogle Scholar
Prado, IC, Mendes, VG, Souza, ALA, Dutra, RF and De-Simone, SG (2018) Electrochemical immunosensor for differential diagnostic of Wuchereria bancrofti using a synthetic peptide. Biosensors & Bioelectronics 113, 9–15.CrossRefGoogle ScholarPubMed
Prince-Guerra, JL, Cama, VA, Wilson, N, Thiele, EA, Likwela, J, Ndakala, N, wa Muzinga, JM, Ayebazibwe, N, Ndjakani, YD and Pitchouna, NA (2018) Comparison of PCR methods for Onchocerca volvulus detection in skin snip biopsies from the Tshopo province, Democratic Republic of the Congo. American Journal of Tropical Medicine and Hygiene, 98, 1427–1434.CrossRefGoogle ScholarPubMed
Rahman, SM, Song, HB, Jin, Y, Oh, J-K, Lim, MK, Hong, S-T and Choi, M-H (2017) Application of a loop-mediated isothermal amplification (LAMP) assay targeting cox1 gene for the detection of Clonorchis sinensis in human fecal samples. PLoS Neglected Tropical Diseases 11, e0005995.CrossRefGoogle ScholarPubMed
Rashwan, N, Diawara, A, Scott, ME and Prichard, RK (2017) Isothermal diagnostic assays for the detection of soil-transmitted helminths based on the SmartAmp2 method. Parasites & Vectors 10, 496.CrossRefGoogle ScholarPubMed
Rathinasamy, V, Hosking, C, Tran, L, Kelley, J, Williamson, G, Swan, J, Elliott, T, Rawlin, G, Beddoe, T and Spithill, TW (2018) Development of a multiplex quantitative PCR assay for detection and quantification of DNA from Fasciola hepatica and the intermediate snail host, Austropeplea tomentosa, in water samples. Veterinary Parasitology 259, 17–24.CrossRefGoogle ScholarPubMed
Rosser, A, Rollinson, D, Forrest, M and Webster, B (2015) Isothermal recombinase polymerase amplification (RPA) of Schistosoma haematobium DNA and oligochromatographic lateral flow detection. Parasites & Vectors 8, 446.CrossRefGoogle ScholarPubMed
Sandoval, N, Siles-Lucas, M, Perez-Arellano, JL, Carranza, C, Puente, S, Lopez-Aban, J and Muro, A (2006) A new PCR-based approach for the specific amplification of DNA from different Schistosoma species applicable to human urine samples. Parasitology 133, 581–587.CrossRefGoogle ScholarPubMed
Santos, GS, Andrade, CA, Bruscky, IS, Wanderley, LB, Melo, FL and Oliveira, MD (2017) Impedimetric nanostructured genosensor for detection of schistosomiasis in cerebrospinal fluid and serum samples. Journal of Pharmaceutical and Biomedical Analysis 137, 163–169.CrossRefGoogle ScholarPubMed
Santos, GS, Caldas, RGSC, Melo, FL, Bruscky, IS, Silva, MAL, Wanderley, LB, Andrade, CAS and Oliveira, MDL (2019) Label-free nanostructured biosensor for Schistosoma mansoni detection in complex biological fluids. Talanta 204, 395–401.CrossRefGoogle ScholarPubMed
Sarhan, RM, Kamel, HH, Saad, GA and Ahmed, OA (2015) Evaluation of three extraction methods for molecular detection of Schistosoma mansoni infection in human urine and serum samples. Journal of Parasitic Diseases 39, 499–507.CrossRefGoogle ScholarPubMed
Sengupta, ME, Hellstrom, M, Kariuki, HC, Olsen, A, Thomsen, PF, Mejer, H, Willerslev, E, Mwanje, MT, Madsen, H, Kristensen, TK, Stensgaard, AS and Vennervald, BJ (2019) Environmental DNA for improved detection and environmental surveillance of schistosomiasis. Proceedings of the National Academy of Sciences of the USA 116, 8931–8940.CrossRefGoogle ScholarPubMed
Shahin, K, Gustavo Ramirez-Paredes, J, Harold, G, Lopez-Jimena, B, Adams, A and Weidmann, M (2018) Development of a recombinase polymerase amplification assay for rapid detection of Francisella noatunensis subsp. orientalis. PLoS ONE 13, e0192979.CrossRefGoogle ScholarPubMed
Sin, ML, Mach, KE, Wong, PK and Liao, JC (2014) Advances and challenges in biosensor-based diagnosis of infectious diseases. Expert Review of Molecular Diagnostics 14, 225–244.CrossRefGoogle ScholarPubMed
Taniuchi, M, Verweij, JJ, Noor, Z, Sobuz, SU, Lieshout, L, Petri, WA Jr, Haque, R and Houpt, ER (2011) High throughput multiplex PCR and probe-based detection with Luminex beads for seven intestinal parasites. American Journal of Tropical Medicine and Hygiene 84, 332–337.CrossRefGoogle ScholarPubMed
ten Hove, RJ, Verweij, JJ, Vereecken, K, Polman, K, Dieye, L and van Lieshout, L (2008) Multiplex real-time PCR for the detection and quantification of Schistosoma mansoni and S. haematobium infection in stool samples collected in northern Senegal. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 179–185.CrossRefGoogle ScholarPubMed
Toé, L, Boatin, BA, Adjami, A, Back, C, Merriweather, A and Unnasch, TR (1998) Detection of Onchocerca volvulus infection by O-150 polymerase chain reaction analysis of skin scratches. Journal of Infectious Diseases 178, 282–285.CrossRefGoogle ScholarPubMed
Tomita, N, Mori, Y, Kanda, H and Notomi, T (2008) Loop-mediated isothermal amplification (LAMP) of gene sequences and simple visual detection of products. Nature Protocols 3, 877.CrossRefGoogle Scholar
Tong, QB, Chen, R, Zhang, Y, Yang, GJ, Kumagai, T, Furushima-Shimogawara, R, Lou, D, Yang, K, Wen, LY, Lu, SH, Ohta, N and Zhou, XN (2015) A new surveillance and response tool: risk map of infected Oncomelania hupensis detected by loop-mediated isothermal amplification (LAMP) from pooled samples. Acta Tropica 141, 170–177.CrossRefGoogle ScholarPubMed
Touron, A, Berthe, T, Pawlak, B and Petit, F (2005) Detection of Salmonella in environmental water and sediment by a nested-multiplex polymerase chain reaction assay. Research in Microbiology 156, 541–553.CrossRefGoogle ScholarPubMed
Traub, RJ, Macaranas, J, Mungthin, M, Leelayoova, S, Cribb, T, Murrell, KD and Thompson, RA (2009) A new PCR-based approach indicates the range of Clonorchis sinensis now extends to Central Thailand. PLoS Neglected Tropical Diseases 3, e367.CrossRefGoogle ScholarPubMed
Verbarg, J., Plath, W. D., Shriver-Lake, L. C., Howell, P. B. Jr, Erickson, J. S., Golden, J. P. and Ligler, F. S. (2013). Catch and release: integrated system for multiplexed detection of bacteria. Analytical Chemistry, 85, 4944–4950.CrossRefGoogle ScholarPubMed
Verweij, JJ, Brienen, EA, Ziem, J, Yelifari, L, Polderman, AM and Van Lieshout, L (2007) Simultaneous detection and quantification of Ancylostoma Duodenale, Necator americanus, and Oesophagostomum bifurcum in fecal samples using multiplex real-time PCR. American Journal of Tropical Medicine and Hygiene 77, 685–690.CrossRefGoogle ScholarPubMed
Verweij, JJ, Polderman, AM, Wimmenhove, MC and Gasser, RB (2000) PCR assay for the specific amplification of Oesophagostomum bifurcum DNA from human faeces. International Journal for Parasitology 30, 137–142.CrossRefGoogle ScholarPubMed
Verweij, JJ and Stensvold, CR (2014) Molecular testing for clinical diagnosis and epidemiological investigations of intestinal parasitic infections. Clinical Microbiology Reviews 27, 371–418.CrossRefGoogle ScholarPubMed
Vică, ML, Matei, HV and Siserman, CV (2016). The Advantages of Using Multiplex PCR for the Simultaneous Detection of Six Sexually Transmitted Diseases. In Polymerase Chain Reaction for Biomedical Applications InTech.CrossRefGoogle Scholar
Warren, K, Bundy, D and Anderson, R (2001) Helminth infection. Dalam: jamison DT, mosley WH, measham AR, penyunting: disease control priorities in developing countries. In Jamison, DT, M., W., Measham, AR, Bobadilla, JL (eds), Disease Control Priorities in Developing Countries, vol. 1993. New York: Oxford University Press for World Bank, pp. 131–160.Google Scholar
Watts, MR, James, G, Sultana, Y, Ginn, AN, Outhred, AC, Kong, F, Verweij, JJ, Iredell, JR, Chen, SC and Lee, R (2014) A loop-mediated isothermal amplification (LAMP) assay for Strongyloides stercoralis in stool that uses a visual detection method with SYTO-82 fluorescent dye. American Journal of Tropical Medicine and Hygiene 90, 306–311.CrossRefGoogle ScholarPubMed
Weerakoon, KG and McManus, DP (2016) Cell-free DNA as a diagnostic tool for human parasitic infections. Trends in parasitology 32, 378–391.CrossRefGoogle ScholarPubMed
Weerakoon, KG, Gordon, CA, Cai, P, Gobert, GN, Duke, M, Williams, GM and McManus, DP (2017a) A novel duplex ddPCR assay for the diagnosis of schistosomiasis japonica: proof of concept in an experimental mouse model. Parasitology 144, 1005–1015.CrossRefGoogle Scholar
Weerakoon, KG, Gordon, CA, Williams, GM, Cai, P, Gobert, GN, Olveda, RM, Ross, AG, Olveda, DU and McManus, DP (2017b) Droplet digital PCR diagnosis of human schistosomiasis: parasite cell-free DNA detection in diverse clinical samples. Journal of Infectious Diseases 216, 1611–1622.CrossRefGoogle Scholar
WHO (2019a) World Health Organisation. Soil-transmitted helminth infections fact sheet. Avaibale at https://www.who.int/en/news-room/fact-sheets/detail/soil-transmitted-helminth-infections.Google Scholar
WHO (2019b) World Health Organization. Schistosomiasis fact-sheets. Available at http://www.who.int/news-room/fact-sheets/detail/schistosomiasis.Google Scholar
Wicht, B, Yanagida, T, Scholz, T, Ito, A, Jiménez, JA and Brabec, J (2010) Multiplex PCR for differential identification of broad tapeworms (Cestoda: Diphyllobothrium) infecting humans. Journal of clinical microbiology 48, 3111–3116.CrossRefGoogle ScholarPubMed
Wong, SSY, Poon, RWS, To, KKW, Chan, JFW, Lu, G, Xing, F, Cheng, VCC and Yuen, KY (2019) Improving the specific diagnosis of trematode, cestode and nematode infections by a multiplex single-tube real-time PCR assay. Journal of Clinical Pathology 72, 487–492.CrossRefGoogle ScholarPubMed
Wongkamchai, S, Nochote, H, Foongladda, S, Dekumyoy, P, Thammapalo, S, Boitano, JJ and Choochote, W (2014) A high resolution melting real time PCR for mapping of filaria infection in domestic cats living in brugian filariasis-endemic areas. Veterinary Parasitology 201, 120–127.CrossRefGoogle Scholar
Xia, C-M, Rong, R, Lu, Z-X, Shi, C-J, Xu, J, Zhang, H-Q, Gong, W and Luo, W (2009) Schistosoma japonicum: a PCR assay for the early detection and evaluation of treatment in a rabbit model. Experimental parasitology 121, 175–179.CrossRefGoogle ScholarPubMed
Ximenes, C, Brandao, E, Oliveira, P, Rocha, A, Rego, T, Medeiros, R, Aguiar-Santos, A, Ferraz, J, Reis, C, Araujo, P, Carvalho, L and Melo, FL (2014) Detection of Wuchereria bancrofti DNA in paired serum and urine samples using polymerase chain reaction-based systems. Memorias do Instituto Oswaldo Cruz 109, 978–983.CrossRefGoogle ScholarPubMed
Xing, W, Yu, X, Feng, J, Sun, K, Fu, W, Wang, Y, Zou, M, Xia, W, Luo, Z, He, H, Li, Y and Xu, D (2017) Field evaluation of a recombinase polymerase amplification assay for the diagnosis of Schistosoma japonicum infection in Hunan province of China. BMC Infectious Diseases 17, 164.CrossRefGoogle Scholar
Xu, J, Duan, ZL, Guan, ZX, Wang, YY, Lin, C, Zhang, TT, Zhang, HQ, Qian, X and Xia, CM (2017) Early detection of circulating DNA of Schistosoma japonicum in sentinel mice models. Experimental parasitology 176, 82–88.CrossRefGoogle ScholarPubMed
Xu, J, Guan, ZX, Zhao, B, Wang, YY, Cao, Y, Zhang, HQ, Zhu, XQ, He, YK and Xia, CM (2015) DNA detection of Schistosoma japonicum: diagnostic validity of a LAMP assay for low-intensity infection and effects of chemotherapy in humans. PLoS Neglected Tropical Diseases 9, e0003668.CrossRefGoogle ScholarPubMed
Xu, J, Rong, R, Zhang, H, Shi, C, Zhu, X and Xia, C (2010) Sensitive and rapid detection of Schistosoma japonicum DNA by loop-mediated isothermal amplification (LAMP). International Journal for Parasitology 40, 327–331.CrossRefGoogle Scholar
Zhong, M, McCarthy, J, Bierwert, L, Lizotte-Waniewski, M, Chanteau, S, Nutman, TB, Ottesen, EA and Williams, SA (1996) A polymerase chain reaction assay for detection of the parasite Wuchereria bancrofti in human blood samples. American Journal of Tropical Medicine and Hygiene 54, 357–363.CrossRefGoogle ScholarPubMed