Skip to main content
Top
Published in: Virology Journal 1/2013

Open Access 01-12-2013 | Research

Monitoring of adenovirus serotypes in environmental samples by combined PCR and melting point analyses

Authors: Nils Marten Hartmann, Melanie Dartscht, Regine Szewzyk, Hans-Christoph Selinka

Published in: Virology Journal | Issue 1/2013

Login to get access

Abstract

Background

Human adenoviruses are promising candidates for addressing health risks associated with enteric viruses in environmental waters. Relatively harmless but common, these DNA viruses persist within the population and are generally considered extremely stable, remaining infectious in water for long periods of time. Group-specific or single species detection of human adenoviruses in environmental samples is usually based on polymerase chain reaction assays. Simultaneous identification of specific species or serotypes needs additional processing. Here we present a simple molecular approach for the monitoring of serotypic diversity in the human adenovirus populations in contaminated water sites.

Methods

Diversity patterns of human adenoviruses in environmental samples, collected in an outdoor artificial stream and pond simulation system, were analyzed using a closed tube polymerase chain reaction method with subsequent melting point analysis.

Results

Human adenovirus serotype 41 was the most prominent adenovirus serotype detected in environmental water samples, but melting point analyses indicated the presence of additional adenovirus serotypes.

Conclusions

Based on investigations with spiked and environmental samples, a combination of qPCR and melting point analysis was shown to identify adenovirus serotypes in sewage contaminated water.
Appendix
Available only for authorised users
Literature
1.
go back to reference Longe EO, Ogundipe AO: Assessment of wastewater discharge impact from a sewage treatment plant on lagoon later, Lagos, Nigeria. Res J Appl Sci Eng Technol 2010,2(3):274-282. Longe EO, Ogundipe AO: Assessment of wastewater discharge impact from a sewage treatment plant on lagoon later, Lagos, Nigeria. Res J Appl Sci Eng Technol 2010,2(3):274-282.
2.
go back to reference Hrudey SE, Hrudey EJ: Published case studies of waterborne disease outbreaks – evidence of a recurrent threat. Water Environ Res 2007,79(3):233-245. 10.2175/106143006X95483PubMedCrossRef Hrudey SE, Hrudey EJ: Published case studies of waterborne disease outbreaks – evidence of a recurrent threat. Water Environ Res 2007,79(3):233-245. 10.2175/106143006X95483PubMedCrossRef
3.
go back to reference Coelho SM, Rijstenbil JW, Brown MT: Impacts of anthropogenic stresses on the early development stages of seaweeds. J Aquat Ecosyst Stress Recovery 2000,7(4):317-333. 10.1023/A:1009916129009CrossRef Coelho SM, Rijstenbil JW, Brown MT: Impacts of anthropogenic stresses on the early development stages of seaweeds. J Aquat Ecosyst Stress Recovery 2000,7(4):317-333. 10.1023/A:1009916129009CrossRef
4.
go back to reference Jobling S, Nolan M, Tyler CR, Brighty G, Sumpter JP: Widespread sexual disruption in wild fish. Environ Sci Technol 1998,32(17):2498-2506. 10.1021/es9710870CrossRef Jobling S, Nolan M, Tyler CR, Brighty G, Sumpter JP: Widespread sexual disruption in wild fish. Environ Sci Technol 1998,32(17):2498-2506. 10.1021/es9710870CrossRef
5.
go back to reference Calabrese A: How some pollutants affect embryos and larvae of american oyster and hard-shell clam. Mar Fish Rev 1972,34(11–12):66-77. Calabrese A: How some pollutants affect embryos and larvae of american oyster and hard-shell clam. Mar Fish Rev 1972,34(11–12):66-77.
6.
go back to reference Khan FA, Ansari AA: Eutrophication: An ecological vision. Bot Rev 2005,71(4):449-482. 10.1663/0006-8101(2005)071[0449:EAEV]2.0.CO;2CrossRef Khan FA, Ansari AA: Eutrophication: An ecological vision. Bot Rev 2005,71(4):449-482. 10.1663/0006-8101(2005)071[0449:EAEV]2.0.CO;2CrossRef
7.
go back to reference Smith SV: Responses of Kaneohe Bay, Hawaii, to relaxation of sewage stress. In Estuaries and Nutrients. Edited by: Neilson BJ, Cronin LE. Clifton, New Jersey: Humana Press Inc; 1981:391-410.CrossRef Smith SV: Responses of Kaneohe Bay, Hawaii, to relaxation of sewage stress. In Estuaries and Nutrients. Edited by: Neilson BJ, Cronin LE. Clifton, New Jersey: Humana Press Inc; 1981:391-410.CrossRef
8.
go back to reference Appelbee AJ, Thompson RCA, Measures LM, Olson ME: Giardia and Cryptosporidium in harp and hooded seals from the Gulf of St. Lawrence, Canada. Vet Parasit 2010,173(1–2):19-23.CrossRef Appelbee AJ, Thompson RCA, Measures LM, Olson ME: Giardia and Cryptosporidium in harp and hooded seals from the Gulf of St. Lawrence, Canada. Vet Parasit 2010,173(1–2):19-23.CrossRef
9.
go back to reference WHO: Health Based Monitoring of Recreational Waters: The Feasibility of a New Approach (the ‘Annapolis Protocol’). Geneva: World Health Organisation; 1999. WHO: Health Based Monitoring of Recreational Waters: The Feasibility of a New Approach (the ‘Annapolis Protocol’). Geneva: World Health Organisation; 1999.
10.
go back to reference Enriquez CE, Hurst CJ, Gerba CP: Survival of the enteric adenoviruses 40 and 41 in tap, sea, and waste water. Water Res 1995,29(11):2548-2553. 10.1016/0043-1354(95)00070-2CrossRef Enriquez CE, Hurst CJ, Gerba CP: Survival of the enteric adenoviruses 40 and 41 in tap, sea, and waste water. Water Res 1995,29(11):2548-2553. 10.1016/0043-1354(95)00070-2CrossRef
11.
go back to reference Medema GJ, Shaw S, Waite M, Snozzi M, Morreau A, Grabow W: Catchment characterisation and source water quality. In Assessing microbial safety of drinking water: Improving approaches and methods. Edited by: Dufour A, Snozzi M, Köster W, Bartram J, Ronchi E, Fewtrell L. London, UK: IWA Publishing, on behalf of the World Health Organization and the Organisation for Economic Co-operation and Development; 2003:111-158. Medema GJ, Shaw S, Waite M, Snozzi M, Morreau A, Grabow W: Catchment characterisation and source water quality. In Assessing microbial safety of drinking water: Improving approaches and methods. Edited by: Dufour A, Snozzi M, Köster W, Bartram J, Ronchi E, Fewtrell L. London, UK: IWA Publishing, on behalf of the World Health Organization and the Organisation for Economic Co-operation and Development; 2003:111-158.
12.
go back to reference Bosch A: Human enteric viruses in the water environment: a minireview. Internatl Microbiol 1998,1(3):191-196. Bosch A: Human enteric viruses in the water environment: a minireview. Internatl Microbiol 1998,1(3):191-196.
13.
go back to reference Leclerc H, Schwartzbrod L, Dei-Cas E: Microbial agents associated with waterborne diseases. In Microbial waterborne pathogens. Edited by: Cloete TE, Rose J, Nel LH, Ford T. London, UK: IWA Publishing London; 2004:1-54. Leclerc H, Schwartzbrod L, Dei-Cas E: Microbial agents associated with waterborne diseases. In Microbial waterborne pathogens. Edited by: Cloete TE, Rose J, Nel LH, Ford T. London, UK: IWA Publishing London; 2004:1-54.
14.
go back to reference Ashbolt NJ, Grabow WOK, Snozzi M: Indicators of microbial water quality. In Water quality: Guidelines, standards and health. Edited by: Fewtrell L, Barthram J. London, UK: IWA Publishing; 2001:289-316. Ashbolt NJ, Grabow WOK, Snozzi M: Indicators of microbial water quality. In Water quality: Guidelines, standards and health. Edited by: Fewtrell L, Barthram J. London, UK: IWA Publishing; 2001:289-316.
15.
go back to reference Figueras MJ, Borrego JJ: New perspectives in monitoring drinking water microbial quality. Int J Environ Res Public Health 2010,7(12):4179-4202. 10.3390/ijerph7124179PubMedPubMedCentralCrossRef Figueras MJ, Borrego JJ: New perspectives in monitoring drinking water microbial quality. Int J Environ Res Public Health 2010,7(12):4179-4202. 10.3390/ijerph7124179PubMedPubMedCentralCrossRef
16.
go back to reference US EPA: Drinking water contaminant list 3 – Final. Fed Reg 2009,74(194):51850-51862. US EPA: Drinking water contaminant list 3 – Final. Fed Reg 2009,74(194):51850-51862.
17.
go back to reference WHO: Guidelines for Drinking-water Quality. Volume 1. 3rd edition. Geneva: World Health Organization; 2008. WHO: Guidelines for Drinking-water Quality. Volume 1. 3rd edition. Geneva: World Health Organization; 2008.
18.
go back to reference Fong T-T, Lipp EK: Enteric viruses of humans and animals in aquatic environments: Health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol Rev 2005,69(2):357-371. 10.1128/MMBR.69.2.357-371.2005PubMedPubMedCentralCrossRef Fong T-T, Lipp EK: Enteric viruses of humans and animals in aquatic environments: Health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol Rev 2005,69(2):357-371. 10.1128/MMBR.69.2.357-371.2005PubMedPubMedCentralCrossRef
19.
go back to reference Beuret C: Simultaneous detection of enteric viruses by multiplex real-time RT-PCR. J Virol Meth 2004,11(1):1-8.CrossRef Beuret C: Simultaneous detection of enteric viruses by multiplex real-time RT-PCR. J Virol Meth 2004,11(1):1-8.CrossRef
20.
go back to reference Aslan A, Xagoraraki I, Simmons FJ, Rose JB, Dorevitch S: Occurrence of adenovirus and other enteric viruses in limited-contact freshwater recreational areas and bathing waters. J Appl Microbiol 2011,111(5):1250-1261. 10.1111/j.1365-2672.2011.05130.xPubMedCrossRef Aslan A, Xagoraraki I, Simmons FJ, Rose JB, Dorevitch S: Occurrence of adenovirus and other enteric viruses in limited-contact freshwater recreational areas and bathing waters. J Appl Microbiol 2011,111(5):1250-1261. 10.1111/j.1365-2672.2011.05130.xPubMedCrossRef
21.
go back to reference Siqueira-Silva J, Perez Yeda F, Favier A-L, Mezin P, Silva ML, Médici Barrella K, Mehnert DU, Fender P, Hársi CM: Infection kinetics of human adenovirus serotype 41 in HEK 293 cells. Mem Inst Oswaldo Cruz 2009,104(5):736-744. 10.1590/S0074-02762009000500013PubMedCrossRef Siqueira-Silva J, Perez Yeda F, Favier A-L, Mezin P, Silva ML, Médici Barrella K, Mehnert DU, Fender P, Hársi CM: Infection kinetics of human adenovirus serotype 41 in HEK 293 cells. Mem Inst Oswaldo Cruz 2009,104(5):736-744. 10.1590/S0074-02762009000500013PubMedCrossRef
22.
go back to reference Jiang SC, Han J, He J-W, Chu W: Evaluation of four cell lines for assay of infectious adenoviruses in water samples. J Water Health 2009,7(4):650-656. 10.2166/wh.2009.088PubMedCrossRef Jiang SC, Han J, He J-W, Chu W: Evaluation of four cell lines for assay of infectious adenoviruses in water samples. J Water Health 2009,7(4):650-656. 10.2166/wh.2009.088PubMedCrossRef
23.
go back to reference Xu W, McDonough MC, Erdman DD: Species-specific identification of human adenoviruses by a multiplex PCR assay. J Clin Microbiol 2000,38(11):4114-4120.PubMedPubMedCentral Xu W, McDonough MC, Erdman DD: Species-specific identification of human adenoviruses by a multiplex PCR assay. J Clin Microbiol 2000,38(11):4114-4120.PubMedPubMedCentral
24.
go back to reference Balkin HB, Margolin AB: Detection of poliovirus by ICC/qPCR in concentrated water samples has a greater sensitivity and is less costly using BGM cells in suspension as compared to monolaysers. Virology J 2010, 7: 282-285. 10.1186/1743-422X-7-282CrossRef Balkin HB, Margolin AB: Detection of poliovirus by ICC/qPCR in concentrated water samples has a greater sensitivity and is less costly using BGM cells in suspension as compared to monolaysers. Virology J 2010, 7: 282-285. 10.1186/1743-422X-7-282CrossRef
25.
go back to reference Murugesan G, Hsi ED: Development of a clinical assay for JAK2 V617F genotyping in chronic myeloproliferative disorders. Pathol Res 2006, 1-4. Murugesan G, Hsi ED: Development of a clinical assay for JAK2 V617F genotyping in chronic myeloproliferative disorders. Pathol Res 2006, 1-4.
26.
go back to reference Reed GH, Wittwer CT: Sensitivity and specificity of single-nucleotide polymorphism scanning by high-resolution melting analysis. Clin Chem 2004,50(10):1748-1754. 10.1373/clinchem.2003.029751PubMedCrossRef Reed GH, Wittwer CT: Sensitivity and specificity of single-nucleotide polymorphism scanning by high-resolution melting analysis. Clin Chem 2004,50(10):1748-1754. 10.1373/clinchem.2003.029751PubMedCrossRef
27.
go back to reference Hernroth BE, Conden-Hansson A, Rehnstam-Holm A, Girones R, Allard AK: Environmental factors influencing human viral pathogens and their potential indicator organisms in the blue mussel, Mytilu eduli : the first Scandinavian report. Appl Environ Microbiol 2002,68(9):4523-4533. 10.1128/AEM.68.9.4523-4533.2002PubMedPubMedCentralCrossRef Hernroth BE, Conden-Hansson A, Rehnstam-Holm A, Girones R, Allard AK: Environmental factors influencing human viral pathogens and their potential indicator organisms in the blue mussel, Mytilu eduli : the first Scandinavian report. Appl Environ Microbiol 2002,68(9):4523-4533. 10.1128/AEM.68.9.4523-4533.2002PubMedPubMedCentralCrossRef
29.
go back to reference Allard A, Albinsson B, Wadell G: Rapid typing of human adenoviruses by a general PCR combined with restriction endonuclease analysis. J Clin Microbiol 2001,39(2):498-505. 10.1128/JCM.39.2.498-505.2001PubMedPubMedCentralCrossRef Allard A, Albinsson B, Wadell G: Rapid typing of human adenoviruses by a general PCR combined with restriction endonuclease analysis. J Clin Microbiol 2001,39(2):498-505. 10.1128/JCM.39.2.498-505.2001PubMedPubMedCentralCrossRef
30.
go back to reference Scipioni A, Mauroy A, Ziant D, Saegerman C, Thiry E: A SYBR green RT-PCR assay in single tube to detect human and bovine noroviruses and control for inhibition. J Virol Meth 2008,5(94):1-8. Scipioni A, Mauroy A, Ziant D, Saegerman C, Thiry E: A SYBR green RT-PCR assay in single tube to detect human and bovine noroviruses and control for inhibition. J Virol Meth 2008,5(94):1-8.
31.
go back to reference Lin J-H, Tseng C-P, Chen Y-J, Lin C-Y, Chang S-S, Wu H-S, Cheng J-C: Rapid differentiation of influenza A virus subtypes and genetic screening for virus variants by high-resolution melting analysis. J Clin Microbiol 2008,46(3):1090-1097. 10.1128/JCM.02015-07PubMedPubMedCentralCrossRef Lin J-H, Tseng C-P, Chen Y-J, Lin C-Y, Chang S-S, Wu H-S, Cheng J-C: Rapid differentiation of influenza A virus subtypes and genetic screening for virus variants by high-resolution melting analysis. J Clin Microbiol 2008,46(3):1090-1097. 10.1128/JCM.02015-07PubMedPubMedCentralCrossRef
32.
go back to reference Steer PA, Kirkpatrick NC, O’Rourke D, Noormohammadi AH: Classification of fowl adenovirus serotypes using high resolution melting curve analysis of the hexon gene region. J Clin Microbiol 2009,47(2):311-321. 10.1128/JCM.01567-08PubMedPubMedCentralCrossRef Steer PA, Kirkpatrick NC, O’Rourke D, Noormohammadi AH: Classification of fowl adenovirus serotypes using high resolution melting curve analysis of the hexon gene region. J Clin Microbiol 2009,47(2):311-321. 10.1128/JCM.01567-08PubMedPubMedCentralCrossRef
33.
go back to reference D’haene B, Hellemans J: The importance of quality control during qPCR data analysis. Int Drug Discov 2010, 18-24. D’haene B, Hellemans J: The importance of quality control during qPCR data analysis. Int Drug Discov 2010, 18-24.
34.
go back to reference McInerney JO, Mullarkey M, Wernecke ME, Powell R: Bacteria and Archaea: Molecular techniques reveal astonishing diversity. Biodiversity 2002,3(2):3-10. 10.1080/14888386.2002.9712571CrossRef McInerney JO, Mullarkey M, Wernecke ME, Powell R: Bacteria and Archaea: Molecular techniques reveal astonishing diversity. Biodiversity 2002,3(2):3-10. 10.1080/14888386.2002.9712571CrossRef
35.
go back to reference Breitbart M, Thompson LR, Suttle CA, Sullivan MB: Exploring the vast diversity of marine viruses. Oceanography 2007,20(2):135-139. 10.5670/oceanog.2007.58CrossRef Breitbart M, Thompson LR, Suttle CA, Sullivan MB: Exploring the vast diversity of marine viruses. Oceanography 2007,20(2):135-139. 10.5670/oceanog.2007.58CrossRef
36.
go back to reference Cantalupo PG, Calgua B, Zhao G, Hundesa A, Wier AD, Katz JP, Grabe M, Hendrix RW, Girones R, Wang D, Pipas JM: Raw sewage harbors diverse viral populations. mBio 2011,2(5):e00180-11.PubMedPubMedCentralCrossRef Cantalupo PG, Calgua B, Zhao G, Hundesa A, Wier AD, Katz JP, Grabe M, Hendrix RW, Girones R, Wang D, Pipas JM: Raw sewage harbors diverse viral populations. mBio 2011,2(5):e00180-11.PubMedPubMedCentralCrossRef
37.
go back to reference Maluquer de Motes C, Hundesa A, Almeida FC, Bofill-Mas S, Girones R: Isolation of a novel monkey adenovirus reveals a new phylogenetic clade in the evolutionary history of simian adenoviruses. Virology J 2011, 8: 125-132. 10.1186/1743-422X-8-125CrossRef Maluquer de Motes C, Hundesa A, Almeida FC, Bofill-Mas S, Girones R: Isolation of a novel monkey adenovirus reveals a new phylogenetic clade in the evolutionary history of simian adenoviruses. Virology J 2011, 8: 125-132. 10.1186/1743-422X-8-125CrossRef
38.
go back to reference Phan TG, Shimizu H, Nishimura S, Okitsu S, Maneekarn N, Ushijima H: Human adenovirus type 1 related to feline adenovirus: evidence of interspecies transmission. Clin Lab 2006,52(9–10):515-518.PubMed Phan TG, Shimizu H, Nishimura S, Okitsu S, Maneekarn N, Ushijima H: Human adenovirus type 1 related to feline adenovirus: evidence of interspecies transmission. Clin Lab 2006,52(9–10):515-518.PubMed
39.
go back to reference Chen EC, Yagi S, Kelly KR, Mendoza SP, Maninger N, Rosenthal A, Spinner A, Bales KL, Schnurr DP, Lerche NW, Chiu CY: Cross-species transmission of a novel adenovirus associated with a fulminant pneumonia outbreak in a New World Monkey colony. PLOS Pathog 2011,7(7):e1002155. 10.1371/journal.ppat.1002155PubMedPubMedCentralCrossRef Chen EC, Yagi S, Kelly KR, Mendoza SP, Maninger N, Rosenthal A, Spinner A, Bales KL, Schnurr DP, Lerche NW, Chiu CY: Cross-species transmission of a novel adenovirus associated with a fulminant pneumonia outbreak in a New World Monkey colony. PLOS Pathog 2011,7(7):e1002155. 10.1371/journal.ppat.1002155PubMedPubMedCentralCrossRef
40.
go back to reference Wevers D, Metzger S, Babweteera F, Bieberbach M, Boesch C, Cameron K, Couacy-Hymann E, Cranfield M, Gray M, Harris LA, Head J, Jeffery K, Knauf S, Lankester F, Leendertz SAJ, Lonsdorf E, Mugisha L, Nitsche A, Reed P, Robbins M, Travis DA, Zommers Z, Leendertz FH, Ehlers B: Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions. J Virol 2001,85(20):10774-10784.CrossRef Wevers D, Metzger S, Babweteera F, Bieberbach M, Boesch C, Cameron K, Couacy-Hymann E, Cranfield M, Gray M, Harris LA, Head J, Jeffery K, Knauf S, Lankester F, Leendertz SAJ, Lonsdorf E, Mugisha L, Nitsche A, Reed P, Robbins M, Travis DA, Zommers Z, Leendertz FH, Ehlers B: Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions. J Virol 2001,85(20):10774-10784.CrossRef
41.
go back to reference Wyn-Jones AP, Carducci A, Cook N, D´Agostino MD, Divizia M, Fleischer J, Gantzer C, Gawler A, Girones R, Höller C, de Roda Husman AM, Kay D, Kozyra I, López-Pila J, Muscillo M, São José Nascimento M, Papageorgiou G, Rutjes S, Sellwood J, Szewzyk R, Wyer M: Surveillance of adenoviruses and noroviruses in European recreational waters. Water Res 2011,45(3):1025-1038. 10.1016/j.watres.2010.10.015PubMedCrossRef Wyn-Jones AP, Carducci A, Cook N, D´Agostino MD, Divizia M, Fleischer J, Gantzer C, Gawler A, Girones R, Höller C, de Roda Husman AM, Kay D, Kozyra I, López-Pila J, Muscillo M, São José Nascimento M, Papageorgiou G, Rutjes S, Sellwood J, Szewzyk R, Wyer M: Surveillance of adenoviruses and noroviruses in European recreational waters. Water Res 2011,45(3):1025-1038. 10.1016/j.watres.2010.10.015PubMedCrossRef
Metadata
Title
Monitoring of adenovirus serotypes in environmental samples by combined PCR and melting point analyses
Authors
Nils Marten Hartmann
Melanie Dartscht
Regine Szewzyk
Hans-Christoph Selinka
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2013
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-10-190

Other articles of this Issue 1/2013

Virology Journal 1/2013 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine