Pericarditis is a common human disease defined by inflammation of the pericardium. Currently, 40% to 85% of pericarditis cases have no identified etiology. Most of these cases are thought to be caused by an infection of undetected, unsuspected or unknown viruses. In this work, we used a culture- and sequence-independent approach to investigate the viral DNA communities present in human pericardial fluids. Seven viral metagenomes were generated from the pericardial fluid of patients affected by pericarditis of unknown etiology and one metagenome was generated from the pericardial fluid of a sudden infant death case. As a positive control we generated one metagenome from the pericardial fluid of a patient affected by pericarditis caused by herpesvirus type 3. Furthermore, we used as negative controls a total of 6 pericardial fluids from 6 different individuals affected by pericarditis of non-infectious origin: 5 of them were sequenced as a unique pool and the remaining one was sequenced separately. The results showed a significant presence of torque teno viruses especially in one patient, while herpesviruses and papillomaviruses were present in the positive control. Co-infections by different genotypes of the same viral type (torque teno viruses) or different viruses (herpesviruses and papillomaviruses) were observed. Sequences related to bacteriophages infecting Staphylococcus, Enterobacteria, Streptococcus, Burkholderia and Pseudomonas were also detected in three patients. This study detected torque teno viruses and papillomaviruses, for the first time, in human pericardial fluids.
References
[1]
Imazio M, Spodick DH, Brucato A, Trinchero R, Markel G, et al.. (2010) Diagnostic issues in the clinical management of pericarditis. International Journal of Clinical Practice 64: : 1384–1392. Available: http://doi.wiley.com/10.1111/j.1742-1241？.2009.02178.x. Accessed 2012 May 31.
[2]
Troughton RW, Asher CR, Klein AL (2004) Pericarditis. Lancet 363: 717–727 Available: http://www.ncbi.nlm.nih.gov/pubmed/15001？332.
[3]
Levy P-Y, Habib G, Collart F, Lepidi H, Raoult D (2006) Etiological diagnosis of pericardial effusion. Future microbiology 1: : 229–239. Available: http://www.ncbi.nlm.nih.gov/pubmed/17661？668. Accessed 2012 May 31.
[4]
Knowlton KU, Savoia MC, Oxman MN (2000): Myocarditis and pericarditis. In: Mandell, Bennett D. Principles and Practice of Infectious Diseases. Philadelphia: Churchill-Livingstone. pp. 925–941.
[5]
Levy P-Y, Corey R, Berger P, Habib G, Bonnet J-L, et al.. (2003) Etiologic diagnosis of 204 pericardial effusions. Medicine 82: : 385–391. Available: http://www.ncbi.nlm.nih.gov/pubmed/14663？288. Accessed 2012 May 31.
[6]
Palacios G, Druce J, Du L, Tran T, Birch C, et al.. (2008) A New Arenavirus in a Cluster of Fatal Transplant-Associated Diseases. New England Journal of Medicine 358: : 991–998. Available: http://www.nejm.org/doi/abs/10.1056/NEJM？oa073785. Accessed 2011 Sep 13.
[7]
Allander T (2005) From The Cover: Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proceedings of the National Academy of Sciences 102: : 12891–12896. Available: http://www.pnas.org/cgi/doi/10.1073/pnas？.0504666102. Accessed 2011 Sep 21.
[8]
Greninger AL, Runckel C, Chiu CY, Haggerty T, Parsonnet J, et al.. (2009) The complete genome of klassevirus - a novel picornavirus in pediatric stool. Virology Journal 6: : 82. Available: http://www.virologyj.com/content/6/1/82. Accessed 2012 Apr 30.
[9]
Feng H, Shuda M, Chang Y, Moore PS (2008) Clonal Integration of a Polyomavirus in Human Merkel Cell Carcinoma. Science 319: : 1096–1100. Available: http://www.sciencemag.org/cgi/doi/10.112？6/science.1152586. Accessed 2012 Apr 27.
[10]
Lysholm F, Wetterbom A, Lindau C, Darban H, Bjerkner A, et al.. (2012) Characterization of the Viral Microbiome in Patients with Severe Lower Respiratory Tract Infections, Using Metagenomic Sequencing. PLoS ONE 7: : e30875. Available: http://dx.plos.org/10.1371/journal.pone.？0030875. Accessed 2012 April 27.
[11]
McMullan LK, Frace M, Sammons SA, Shoemaker T, Balinandi S, et al.. (2012) Using next generation sequencing to identify yellow fever virus in Uganda. Virology 422: : 1–5. Available: http://www.ncbi.nlm.nih.gov/pubmed/21962？764. Accessed 2012 Apr 30.
[12]
Sullivan PF, Allander T, Lysholm F, Goh S, Persson B, et al.. (2011) An unbiased metagenomic search for infectious agents using monozygotic twins discordant for chronic fatigue. BMC Microbiology 11: : 2. Available: http://www.biomedcentral.com/1471-2180/1？1/2. Accessed 2011 Sep 13.
[13]
Nakamura S, Yang C-S, Sakon N, Ueda M, Tougan T, et al.. (2009) Direct Metagenomic Detection of Viral Pathogens in Nasal and Fecal Specimens Using an Unbiased High-Throughput Sequencing Approach. PLoS ONE 4: : e4219. Available: http://dx.plos.org/10.1371/journal.pone.？0004219. Accessed 2011 Sep 13.
[14]
Thurber R V, Haynes M, Breitbart M, Wegley L, Rohwer F (2009) Laboratory procedures to generate viral metagenomes. Nature protocols 4: : 470–483. Available: http://www.ncbi.nlm.nih.gov/pubmed/19300？441. Accessed 2013 May 24.
[15]
Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics (Oxford, England) 22: : 1658–1659. Available: http://www.ncbi.nlm.nih.gov/pubmed/16731？699. Accessed 2012 May 9.
[16]
Sun S, Chen J, Li W, Altintas I, Lin A, et al.. (2010) Community cyberinfrastructure for Advanced Microbial Ecology Research and Analysis: the CAMERA resource. Nucleic Acids Research 39: : D546–D551. Available: http://www.nar.oxfordjournals.org/cgi/do？i/10.1093/nar/gkq1102. Accessed 2011 Sep 22.
[17]
Roux S, Faubladier M, Mahul A, Paulhe N, Bernard A, et al. (2011) Metavir: a web server dedicated to virome analysis. Bioinformatics 27: 3074–3075 Available: http://bioinformatics.oxfordjournals.org？/content/27/21/3074.abstract.
[18]
Angly FE, Willner D, Prieto-Davó A, Edwards RA, Schmieder R, et al.. (2009) The GAAS Metagenomic Tool and Its Estimations of Viral and Microbial Average Genome Size in Four Major Biomes. PLoS Computational Biology 5: : e1000593. Available: http://dx.plos.org/10.1371/journal.pcbi.？1000593. Accessed 2011 Sep 13.
[19]
Peng YH, Nishizawa T, Takahashi M, Ishikawa T, Yoshikawa A, et al.. (2002) Analysis of the entire genomes of thirteen TT virus variants classifiable into the fourth and fifth genetic groups, isolated from viremic infants. Archives of virology 147: : 21–41. Available: http://www.ncbi.nlm.nih.gov/pubmed/11855？633. Accessed 2012 May 7.
[20]
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods in molecular biology (Clifton, NJ) 132: : 365–386. Available: http://www.ncbi.nlm.nih.gov/pubmed/10547？847. Accessed 2012 May 7.
[21]
Pant？cek R, Doskar J, R？zicková V, Kaspárek P, Orácová E, et al.. (2004) Identification of bacteriophage types and their carriage in Staphylococcus aureus. Archives of virology 149: : 1689–1703. Available: http://www.ncbi.nlm.nih.gov/pubmed/15593？413. Accessed 2012 May 9.
[22]
Balding C, Bromley SA, Pickup RW, Saunders JR (2005) Diversity of phage integrases in Enterobacteriaceae: development of markers for environmental analysis of temperate phages. Environmental microbiology 7: : 1558–1567. Available: http://www.ncbi.nlm.nih.gov/pubmed/16156？729. Accessed 2012 May 7.
[23]
Dwivedi B, Schmieder R, Goldsmith DB, Edwards RA, Breitbart M (2012) PhiSiGns: an online tool to identify signature genes in phages and design PCR primers for examining phage diversity. BMC bioinformatics 13: : 37. Available: http://www.ncbi.nlm.nih.gov/pubmed/22385？976. Accessed 2012 May 7.
[24]
Favre M, Obalek S, Jablonska S, Orth G (1989) Human papillomavirus (HPV) type 50, a type associated with epidermodysplasia verruciformis (EV) and only weakly related to other EV-specific HPVs. Journal of Virology 63: 4910.
[25]
Li J, Cai H, Xu Z, Wang Q, Hang D, et al.. (2012) Nine complete genome sequences of cutaneous human papillomavirus genotypes isolated from healthy skin of individuals living in rural He Nan province, China. Journal of virology 86: : 11936. Available: http://www.pubmedcentral.nih.gov/article？render.fcgi?artid=3486313&tool=pmcentrez？&rendertype=abstract Accessed 2013 May 20.
[26]
Delius H HB (1994) Primer-directed sequencing of human papillomavirus types. Curr Top Microbiol Immunol 186: 13–31. doi: 10.1007/978-3-642-78487-3_2
[27]
Delius H, Saegling B, Bergmann K, Shamanin V, De Villiers EM (1998) The genomes of three of four novel HPV types, defined by differences of their L1 genes, show high conservation of the E7 gene and the URR. Virology 240: 359–365 Available: http://www.ncbi.nlm.nih.gov/pubmed/94547？09.
[28]
Hallett RL, Clewley JP, Bobet F, McKiernan PJ, Teo CG (2000) Characterization of a highly divergent TT virus genome. The Journal of general virology 81: 2273–2279 Available: http://www.pubmedcentral.nih.gov/article？render.fcgi?artid=2777865&tool=pmcentrez？&rendertype=abstract.
[29]
Heller F, Zachoval R, Koelzer A, Nitschko H, Froesner GG (2001) Isolate KAV: a new genotype of the TT-virus family. Biochemical and biophysical research communications 289: : 937–941. Available: http://www.ncbi.nlm.nih.gov/pubmed/11741？280. Accessed 2013 Apr 9.
[30]
Kao K-L, Yeh S-J, Chen C-C (2010) Myopericarditis associated with varicella zoster virus infection. Pediatric cardiology 31: : 703–706. Available: http://www.ncbi.nlm.nih.gov/pubmed/20087？580. Accessed 2013 May 6.
[31]
Seddon DJ (1986) Pericarditis with pericardial effusion complicating chickenpox. Postgraduate medical journal 62: 1133–1134 Available: http://www.pubmedcentral.nih.gov/article？render.fcgi?artid=2418950&tool=pmcentrez？&rendertype=abstract.
[32]
Willner D, Furlan M, Haynes M, Schmieder R, Angly FE, et al.. (2009) Metagenomic Analysis of Respiratory Tract DNA Viral Communities in Cystic Fibrosis and Non-Cystic Fibrosis Individuals. PLoS ONE 4: : e7370. Available: http://dx.plos.org/10.1371/journal.pone.？0007370. Accessed 2011 Sep 13.
[33]
Nishizawa T, Okamoto H, Konishi K, Yoshizawa H, Miyakawa Y, et al. (1997) A novel {DNA} virus ({TTV)} associated with elevated transaminase levels in posttransfusion hepatitis of unknown etiology. Biochem Biophys Res Commun 241: 92–97 doi:10.1006/bbrc.1997.7765.
[34]
Hsieh SY, Wu YH, Ho YP, Tsao KC, Yeh CT, et al. (1999) High prevalence of {TT} virus infection in healthy children and adults and in patients with liver disease in Taiwan. J Clin Microbiol 37: 1829–1831.
[35]
Vasilyev E V, Trofimov DY, Tonevitsky AG, Ilinsky V V, Korostin DO, et al.. (2009) Torque Teno Virus ({TTV)} distribution in healthy Russian population. 6: : 134. Available: http://www.virologyj.com/content/6/1/134. Accessed 2013 Jan 16.
[36]
Abe K, Inami T, Asano K, Miyoshi C, Masaki N, et al. (1999) {TT} virus infection is widespread in the general populations from different geographic regions. J Clin Microbiol 37: 2703–2705.
[37]
Zhong S, Yeo W, Tang M, Liu C, Lin X, et al. (2002) Frequent detection of the replicative form of {TT} virus {DNA} in peripheral blood mononuclear cells and bone marrow cells in cancer patients. J Med Virol 66: 428–434. doi: 10.1002/jmv.2163
[38]
Biagini P, Gallian P, Attoui H, Cantaloube JF, De Micco P, et al. (1999) Determination and phylogenetic analysis of partial sequences from TT virus isolates. The Journal of general virology 80 (Pt 2): 419–424 Available: http://www.ncbi.nlm.nih.gov/pubmed/10073？702.
[39]
Ball JK, Curran R, Berridge S, Grabowska AM, Jameson CL, et al. (1999) TT virus sequence heterogeneity in vivo: evidence for co-infection with multiple genetic types. The Journal of general virology 80 (Pt 7): 1759–1768 Available: http://www.ncbi.nlm.nih.gov/pubmed/10423？145.
[40]
Irving WL, Ball JK, Berridge S, Curran R, Grabowska AM, et al. (1999) TT virus infection in patients with hepatitis C: frequency, persistence, and sequence heterogeneity. The Journal of infectious diseases 180: 27–34 Available: http://www.ncbi.nlm.nih.gov/pubmed/10353？857.
[41]
Khudyakov YE, Cong ME, Nichols B, Reed D, Dou XG, et al. (2000) Sequence heterogeneity of {TT} virus and closely related viruses. J Virol 74: 2990–3000. doi: 10.1128/jvi.74.7.2990-3000.2000
[42]
D'Herelle F (1922) The bacteriophage: its r？le in immunity. Baltimore [Md.]: Williams & Wilkins. Available: http://www.worldcat.org/title/bacterioph？age-its-role-in-immunity/oclc/14789160. Accessed 2013 May 20.
[43]
Pride DT, Salzman J, Haynes M, Rohwer F, Davis-Long C, et al.. (2011) Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. The ISME Journal 6: : 915–926. Available: http://www.nature.com/doifinder/10.1038/？ismej.2011.169. Accessed 2012 May 3.
[44]
Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, et al.. (2010) Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466: : 334–338. Available: http://www.nature.com/doifinder/10.1038/？nature09199. Accessed 2011 Sep 26.
[45]
Willner D, Furlan M, Schmieder R, Grasis JA, Pride DT, et al.. (2010) Colloquium Paper: Metagenomic detection of phage-encoded platelet-binding factors in the human oral cavity. Proceedings of the National Academy of Sciences 108: : 4547–4553. Available: http://www.pnas.org/cgi/doi/10.1073/pnas？.1000089107. Accessed 2011 Sep 13.
[46]
Gaidelyte A, Vaara M, Bamford DH (2007) Bacteria, phages and septicemia. PLoS ONE 2: e1145.59. doi: 10.1371/journal.pone.0001145
[47]
Levy P-Y, Fournier PE, Fenollar F, Raoult D (2013) Systematic PCR detection in culture negative osteoarticular infections. Am J Med. 126 (12): : 1143.e25ons. Am 3.
[48]
Fournier PE, Thuny F, Richet H, Lepidi H, Casalta J-P, et al. (2010) Comprehensive diagnostic strategy for blood culture-negative endocarditis: a prospective study of 819 new cases. Clin Infect Dis 51: 131–140 Available: http://www.ncbi.nlm.nih.gov/pubmed/20540？619.
[49]
Wommack KE, Ravel J, Hill RT, Colwell RR (1999) Hybridization Analysis of Chesapeake Bay Virioplankton. Appl Envir Microbiol 65: : 241–250. Available: http://aem.asm.org/content/65/1/241.abst？ract?ijkey=73b1a36cd0bbaba1ea8a78472e1f5？7e09bf640a1&keytype2=tf_ipsecsha. Accessed 2013 May 20.
[50]
Bergh O, B？rsheim KY, Bratbak G, Heldal M (1989) High abundance of viruses found in aquatic environments. Nature 340: : 467–468. Available: http://www.ncbi.nlm.nih.gov/pubmed/27555？08. Accessed 2013 May 20.
