Advertisement

Applied Microbiology and Biotechnology

, Volume 103, Issue 19, pp 8115–8125 | Cite as

Rapid assessment of viral water quality using a novel recombinase polymerase amplification test for human adenovirus

  • Emily K. Rames
  • Joanne MacdonaldEmail author
Applied genetics and molecular biotechnology

Abstract

Sensitive and rapid methods for determining viral contamination of water are critical, since illness can be caused by low numbers of viruses and bacterial indicators do not adequately predict viral loads. We developed novel rapid assays for detecting the viral water quality indicator human adenovirus (HAdV). A simple 15-min recombinase polymerase amplification step followed by a 5-min lateral flow detection is used. Species-specific assays were developed to discriminate HAdV A, B, C and F, and combined into a multiplex test (Ad-FAC). Species-specific assays enabled detection of 10–50 copies of the HAdV plasmid. Sample testing using methods optimised for wastewater analysis indicated the Ad-FAC assay showed 100% sensitivity and 100% specificity when compared with HAdV qPCR, with a detection limit as low as 50 gene copies. This is the first study to demonstrate the use of RPA for detecting enteric viruses in water samples, to assess virological water quality. The ability to rapidly detect enteric virus contamination of water could assist in more effective management of water safety and better protection of public health.

Keywords

Recombinase polymerase amplification Lateral flow immunoassay Water quality Adenovirus Inhibition Isothermal amplification 

Notes

Acknowledgements

The authors thank Maxim Scheludchenko and Anna Padovan for collection of wastewater samples and PEG precipitations. We also thank Professor Richard Burns for critical review of the manuscript, and we are grateful to Helen Stratton, Anne Roiko and Charles Lemckert for advice and encouragement.

Funding

This study was funded by a University of the Sunshine Coast (USC, Australia) Faculty Seed Grant. Author1 received a scholarship provided by USC and Griffith University as part of a PONDS Project funded by the Queensland Government DSITIA Science Fund project, through the Smart Water Research Centre (Griffith University, Australia).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2019_10077_MOESM1_ESM.pdf (1 mb)
ESM 1 (PDF 1041 kb)

References

  1. Abbaszadegan M, Huber M, Gerba CP, Pepper IL (1993) Detection of enteroviruses in groundwater with the polymerase chain reaction. Appl Environ Microbiol 59(5):1318–1324Google Scholar
  2. Boyle DS, Lehman DA, Lillis L, Peterson D, Singhal M, Armes N, Parker M, Piepenburg O, Overbaugh J (2013) Rapid detection of HIV-1 proviral DNA for early infant diagnosis using recombinase polymerase amplification. MBio 4(2):e00135–e00113CrossRefGoogle Scholar
  3. Bridge JW, Oliver DM, Chadwick D, Godfray HCJ, Heathwaite AL, Kay D, Maheswaran R, McGonigle DF, Nichols G, Pickup R (2010) Engaging with the water sector for public health benefits: waterborne pathogens and diseases in developed countries. Bull World Health Organ 88(11):873–875CrossRefGoogle Scholar
  4. Castle PE, Eaton B, Reid J, Getman D, Dockter J (2015) Comparison of human papillomavirus detection by Aptima HPV and cobas HPV tests in a population of women referred for colposcopy following detection of atypical squamous cells of undetermined significance by Pap cytology. J Clin Microbiol 53(4):1277–1281CrossRefGoogle Scholar
  5. Cordray MS, Richards-Kortum RR (2015) A paper and plastic device for the combined isothermal amplification and lateral flow detection of Plasmodium DNA. Malar J 14(1):1CrossRefGoogle Scholar
  6. Crannell ZA, Rohrman B, Richards-Kortum R (2015) Development of a quantitative recombinase polymerase amplification assay with an internal positive control. J Vis Exp 97:e52620–e52620Google Scholar
  7. Euler M, Wang Y, Heidenreich D, Patel P, Strohmeier O, Hakenberg S, Niedrig M, Hufert FT, Weidmann M (2013) Development of a panel of recombinase polymerase amplification assays for detection of biothreat agents. J Clin Microbiol 51(4):1110–1117CrossRefGoogle Scholar
  8. Fongaro G, Do Nascimento MA, Rigotto C, Ritterbusch G, da Silva ADA, Esteves PA, Barardi CR (2013) Evaluation and molecular characterization of human adenovirus in drinking water supplies: viral integrity and viability assays. Virol J 10(1):166CrossRefGoogle Scholar
  9. Franz G, Feuerstein U (1997) Chemical stability of some model polysaccharides. In: Macromolecular Symposia, vol 120. Wiley Online Library, pp 169–181Google Scholar
  10. Gibson K, Schwab K, Spencer S, Borchardt M (2012) Measuring and mitigating inhibition during quantitative real time PCR analysis of viral nucleic acid extracts from large-volume environmental water samples. Water Res 46(13):4281–4291CrossRefGoogle Scholar
  11. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  12. Heim A, Ebnet C, Harste G, Pring-Åkerblom P (2003) Rapid and quantitative detection of human adenovirus DNA by real-time PCR. J Med Virol 70(2):228–239CrossRefGoogle Scholar
  13. Hewitt J, Greening GE, Leonard M, Lewis GD (2013) Evaluation of human adenovirus and human polyomavirus as indicators of human sewage contamination in the aquatic environment. Water Res 47(17):6750–6761CrossRefGoogle Scholar
  14. Hybridetect (2014) Hybridetect instruction manual, Milenia Biotec GmbH. pp 1–8. Available from https://www.milenia-biotec.de/en/research/hybridetect/. Accessed 18 Aug 2019 
  15. James A, Macdonald J (2015) Recombinase polymerase amplification: emergence as a critical molecular technology for rapid, low-resource diagnostics. Expert Rev Mol Diagn 15(11):1475–1489CrossRefGoogle Scholar
  16. Katayama H, Haramoto E, Oguma K, Yamashita H, Tajima A, Nakajima H, Ohgaki S (2008) One-year monthly quantitative survey of noroviruses, enteroviruses, and adenoviruses in wastewater collected from six plants in Japan. Water Res 42(6):1441–1448CrossRefGoogle Scholar
  17. Kersting S, Rausch V, Bier FF, von Nickisch-Rosenegk M (2014a) Rapid detection of Plasmodium falciparum with isothermal recombinase polymerase amplification and lateral flow analysis. Malar J 13(1):99CrossRefGoogle Scholar
  18. Kersting S, Rausch V, Bier FF, von Nickisch-Rosenegk M (2014b) Multiplex isothermal solid-phase recombinase polymerase amplification for the specific and fast DNA-based detection of three bacterial pathogens. Microchim Acta 181(13-14):1715–1723CrossRefGoogle Scholar
  19. Kim T-H, Park J, Kim C-J, Cho Y-K (2014) Fully integrated lab-on-a-disc for nucleic acid analysis of food-borne pathogens. Anal Chem 86(8):3841–3848CrossRefGoogle Scholar
  20. Kolokassidou C, Pashalidis I, Costa C, Efstathiou A, Buckau G (2007) Thermal stability of solid and aqueous solutions of humic acid. Thermochim Acta 454(2):78–83CrossRefGoogle Scholar
  21. Krõlov K, Frolova J, Tudoran O, Suhorutsenko J, Lehto T, Sibul H, Mäger I, Laanpere M, Tulp I, Langel Ü (2014) Sensitive and rapid detection of Chlamydia trachomatis by recombinase polymerase amplification directly from urine samples. J Mol Diagn 16(1):127–135CrossRefGoogle Scholar
  22. Kunze A, Dilcher M, Abd El Wahed A, Hufert F, Niessner R, Seidel M (2015) On-chip isothermal nucleic acid amplification on flow-based chemiluminescence microarray analysis platform for the detection of viruses and bacteria. Anal Chem 88(1):898–905CrossRefGoogle Scholar
  23. Li J, Macdonald J (2015) Advances in isothermal amplification: novel strategies inspired by biological processes. Biosens Bioelectron 64:196–211CrossRefGoogle Scholar
  24. Li J, Macdonald J (2016) Multiplexed lateral flow biosensors: technological advances for radically improving point-of-care diagnoses. Biosens Bioelectron 83:177–192CrossRefGoogle Scholar
  25. Mara D, Hamilton A, Sleigh A, Karavarsamis N (2010) Discussion paper: options for updating the 2006 WHO guidelines. WHO-FAO-IDRC-IWMGoogle Scholar
  26. Nordgren J, Matussek A, Mattsson A, Svensson L, Lindgren P-E (2009) Prevalence of norovirus and factors influencing virus concentrations during one year in a full-scale wastewater treatment plant. Water Res 43(4):1117–1125CrossRefGoogle Scholar
  27. Ogorzaly L, Walczak C, Galloux M, Etienne S, Gassilloud B, Cauchie H-M (2015) Human adenovirus diversity in water samples using a next-generation amplicon sequencing approach. Food Environ Virol 7(2):112–121CrossRefGoogle Scholar
  28. Okoh AI, Sibanda T, Gusha SS (2010) Inadequately treated wastewater as a source of human enteric viruses in the environment. Int J Environ Res Public Health 7(6):2620–2637CrossRefGoogle Scholar
  29. Pepe MS (2003) The Statistical Evaluation Of Medical Tests For Classification And Prediction. Oxford University Press, CaryGoogle Scholar
  30. Piepenburg O, Williams CH, Stemple DL, Armes NA (2006) DNA detection using recombination proteins. PLoS Biol 4(7):e204CrossRefGoogle Scholar
  31. Piepenburg O, Williams CH, Armes NA (2016) Methods for multiplexing recombinase polymerase amplification. US Patent 20,160,097,090Google Scholar
  32. Rames E, Roiko A, Stratton H, Macdonald J (2016) Technical aspects of using human adenovirus as a viral water quality indicator. Water Res 96:308–326CrossRefGoogle Scholar
  33. Rames E, Roiko A, Stratton H, Macdonald J (2017) DNA heat treatment for improving qPCR analysis of human adenovirus in wastewater. Food Environ Virol 9(3):354–357CrossRefGoogle Scholar
  34. Redwan N, Al-Fassi F, Ali M (2008) Health aspects of virological water quality: an overview review. J Appl Sci Res 4(10):1205–1215Google Scholar
  35. Rees WA, Yager TD, Korte J, Von Hippel PH (1993) Betaine can eliminate the base pair composition dependence of DNA melting. Biochemistry 32(1):137–144CrossRefGoogle Scholar
  36. Rodriguez NM, Wong WS, Liu L, Dewar R, Klapperich CM (2016) A fully integrated paperfluidic molecular diagnostic chip for the extraction, amplification, and detection of nucleic acids from clinical samples. Lab Chip 16(4):753–763CrossRefGoogle Scholar
  37. Rohrman B, Richards-Kortum R (2015) Inhibition of recombinase polymerase amplification by background DNA: a lateral flow-based method for enriching target DNA. Anal Chem 87(3):1963–1967CrossRefGoogle Scholar
  38. Rosario K, Nilsson C, Lim YW, Ruan Y, Breitbart M (2009) Metagenomic analysis of viruses in reclaimed water. Environ Microbiol 11(11):2806–2820CrossRefGoogle Scholar
  39. Rowe L, Sprigg G (2014) Applications of emerging technologies in the drinking water sector. In: Bridle H (ed) Waterborne pathogens: detection methods and applications. Elsevier Science, London, pp 351–379CrossRefGoogle Scholar
  40. Sedmak G, Bina D, MacDonald J (2003) Assessment of an enterovirus sewage surveillance system by comparison of clinical isolates with sewage isolates from Milwaukee, Wisconsin, collected August 1994 to December 2002. Appl Environ Microbiol 69(12):7181–7187CrossRefGoogle Scholar
  41. Sheludchenko M, Padovan A, Katouli M, Stratton H (2016) Removal of fecal indicators, pathogenic bacteria, adenovirus, Cryptosporidium and Giardia oocysts in waste stabilization ponds in northern and eastern Australia. Int J Environ Res Public Health 13(1):96CrossRefGoogle Scholar
  42. Shieh Y-S, Wait D, Tai L, Sobsey MD (1995) Methods to remove inhibitors in sewage and other fecal wastes for enterovirus detection by the polymerase chain reaction. J Virol Methods 54(1):51–66CrossRefGoogle Scholar
  43. Stock C, Hielscher T (2013) DTComPair: comparison of binary diagnostic tests in a paired study design R package version 1. https://rdrr.io/cran/DTComPair/. Accessed 18 Aug 2019
  44. Symonds EM, Breitbart M (2015) Affordable enteric virus detection techniques are needed to support changing paradigms in water quality management. CLEAN Soil Air Water 43(1):8–12Google Scholar
  45. TwistDx-Manual (2014) TwistAmp™ DNA amplification kits: combined instruction manual. TA01cmanual Revision E. Available at www.twistdx.co.uk. Accessed 21 July 2016
  46. VIC-Guidelines (2013) Guidelines for validating treatment processes for pathogen reduction: supporting class a recycled water schemes in Victoria. Department of Health, VictoriaGoogle Scholar
  47. WHO (2017) World Health Organization Drinking Water Parameter Cooperation ProjectGoogle Scholar
  48. Wold W, Ison M (2013) Adenoviruses. In: Knipe D, Howley P (eds) Fields Virology, 6th edn. Lippincott Williams & Wilkins, Philadelphia, pp 1732–1767Google Scholar
  49. Wong K, Fong T-T, Bibby K, Molina M (2012) Application of enteric viruses for fecal pollution source tracking in environmental waters. Environ Int 45:151–164CrossRefGoogle Scholar
  50. Zhou X-H, McClish DK, Obuchowski NA (2011) Statistical methods in diagnostic medicine. Wiley, HobokenCrossRefGoogle Scholar
  51. Zucker M, Markham N (1995) Quickfold http://unafold.rna.albany.edu/?q=DINAMelt/Quickfold. Accessed 18 Aug 2019

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Genecology Research Centre, School of Science and EngineeringUniversity of the Sunshine CoastSippy DownsAustralia

Personalised recommendations