Cited by 75Viral gastroenteritis research and epidemiologyBacteriophages and microbial interactionsAnimal Virus Infections Studies

Gut Virome Analysis of Cameroonians Reveals High Diversity of Enteric Viruses, Including Potential Interspecies Transmitted Viruses

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Yinda, Claude Kwe, Vanhulle, Emiel, Conceição-Neto, Nádia, Beller, Leen, Deboutte, Ward, Shi, Chenyan, Ghogomu, Stephen Mbigha, Maes, Piet +2 more·2019·mSphere

Abstract

Despite the availability of diagnostic tools for different enteric viral pathogens, a large fraction of human cases of gastroenteritis remains unexplained. This could be due to pathogens not tested for or novel divergent viruses of potential animal origin. Fecal virome analyses of Cameroonians showed a very diverse group of viruses, some of which are genetically related to those identified in animals. This is the first attempt to describe the gut virome of humans from Cameroon. Therefore, the data represent a baseline for future studies on enteric viral pathogens in this area and contribute to our knowledge of the world’s virome. The studies also highlight the fact that more viruses may be associated with diarrhea than the typical known ones. Hence, it provides meaningful epidemiological information on diarrhea-related viruses in this area.

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  • The picobirnavirus-related transcript found here is similar to picobirnaviruses described as potentially zoonotic in humans with gastroenteritis.

    “It is also similar to picobirnaviruses described as potentially zoonotic in humans with gastroenteritis (Yinda et al. 2019).”

    From Red fox viromes in urban and rural landscapes (2020) · cites this paper as Yinda et al. 2019

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  1. [3]Fong T-T, Lipp EK 2005 Enteric viruses of humans and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol Rev 69: 357– 371. doi: 10.1128/MMBR.69.2.357-371.2005. 15944460 PMC1197419 · DOI
  2. [4]Ayukekbong J, Kabayiza J-C, Lindh M, Nkuo-Akenji T, Tah F, Bergström T, Norder H 2013 Shift of Enterovirus species among children in Cameroon; identification of a new enterovirus, EV-A119. J Clin Virol 58: 227– 232. doi: 10.1016/j.jcv.2013.07.005. 23895932 · DOI
  3. [5]Santosham M, Chandran A, Fitzwater S, Fischer-Walker C, Baqui AH, Black R 2010 Progress and barriers for the control of diarrhoeal disease. Lancet 376: 63– 67. doi: 10.1016/S0140-6736(10)60356-X. 20609988 · DOI
  4. [6]Ayukekbong JA, Andersson ME, Vansarla G, Tah F, Nkuo-AkenjI T, Lindh M, Bergström T 2014 Monitoring of seasonality of norovirus and other enteric viruses in Cameroon by real-time PCR: an exploratory study. Epidemiol Infect 142: 1393– 1402. doi: 10.1017/S095026881300232X. 24047516 PMC9151225 · DOI
  5. [7]Ayukekbong J, Lindh M, Nenonen N, Tah F, Nkuo-Akenji T, Bergström T 2011 Enteric viruses in healthy children in Cameroon: viral load and genotyping of norovirus strains. J Med Virol 83: 2135– 2142. doi: 10.1002/jmv.22243. 22012721 · DOI
  6. [8]Ayukekbong JA 2013 PhD thesis. University of Gothenburg, Gothenburg, Sweden.
  7. [9]Li L, Victoria J, Kapoor A, Blinkova O, Wang C, Babrzadeh F, Mason CJ, Pandey P, Triki H, Bahri O, Oderinde BS, Baba MM, Bukbuk DN, Besser JM, Bartkus JM, Delwart EL 2009 A novel picornavirus associated with gastroenteritis. J Virol 83: 12002– 12006. doi: 10.1128/JVI.01241-09. 19759142 PMC2772710 · DOI
  8. [10]Phan TG, Sdiri-Loulizi K, Aouni M, Ambert-Balay K, Pothier P, Deng X, Delwart E 2014 New parvovirus in child with unexplained diarrhea, Tunisia. Emerg Infect Dis 20: 1911– 1913. doi: 10.3201/eid2011.140428. 25340816 PMC4214302 · DOI
  9. [11]Bosch A, Guix S, Sano D, Pintó RM 2008 New tools for the study and direct surveillance of viral pathogens in water. Curr Opin Biotechnol 19: 295– 301. doi: 10.1016/j.copbio.2008.04.006. 18508257 PMC7126527 · DOI
  10. [12]Fenton M, Simmons N 2015 Bats, a world of science and mystery. The University of Chicago Press, Chicago, IL.
  11. [13]Rupprecht CE, Smith JS, Fekadu M, Childs JE 1995 The ascension of wildlife rabies: a cause for public health concern or intervention? Emerg Infect Dis 1: 107– 114. doi: 10.3201/eid0104.950401. 8903179 PMC2626887 · DOI
  12. [14]Towner JS, Pourrut X, Albariño CG, Nkogue CN, Bird BH, Grard G, Ksiazek TG, Gonzalez J-P, Nichol ST, Leroy EM 2007 Marburg virus infection detected in a common African bat. PLoS One 2: e764. doi: 10.1371/journal.pone.0000764. 17712412 PMC1942080 · DOI
  13. [15]Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P, Delicat A, Paweska JT, Gonzalez J-P, Swanepoel R 2005 Fruit bats as reservoirs of Ebola virus. Nature 438: 575– 576. doi: 10.1038/438575a. 16319873 · DOI
  14. [16]Lau SKP, Woo PCY, Li KSM, Huang Y, Tsoi H-W, Wong BHL, Wong SSY, Leung S-Y, Chan K-H, Yuen K-Y 2005 Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A 102: 14040– 14045. doi: 10.1073/pnas.0506735102. 16169905 PMC1236580 · DOI
  15. [17]Memish ZA, Mishra N, Olival KJ, Fagbo SF, Kapoor V, Epstein JH, AlHakeem R, Durosinloun A, Al Asmari M, Islam A, Kapoor A, Briese T, Daszak P, Al Rabeeah AA, Lipkin WI 2013 Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis 19: 1819– 1823. doi: 10.3201/eid1911.131172. 24206838 PMC3837665 · DOI
  16. [18]Chua KB, Lek Koh C, Hooi PS, Wee KF, Khong JH, Chua BH, Chan YP, Lim ME, Lam SK 2002 Isolation of Nipah virus from Malaysian Island flying-foxes. Microbes Infect 4: 145– 151. 11880045
  17. [19]Wong S, Lau S, Woo P, Yuen K-YY 2007 Bats as a continuing source of emerging infections in humans. Rev Med Virol 17: 67– 91. doi: 10.1002/rmv.520. 17042030 PMC7169091 · DOI
  18. [20]Yinda CK, Rector A, Zeller M, Conceição-Neto N, Heylen E, Maes P, Stephen GM, Van Ranst M, Matthijnssens J, Ghogomu SM, Van Ranst M, Matthijnssens J 2016 A single bat species in Cameroon harbors multiple highly divergent papillomaviruses in stool identified by metagenomics analysis. Virol Rep 6: 74– 80. doi: 10.1016/j.virep.2016.08.001. PMC7103942 32289018 · DOI
  19. [21]Yinda CK, Zell R, Deboutte W, Zeller M, Conceição-Neto N, Heylen E, Maes P, Knowles NJ, Ghogomu SM, Van Ranst M, Matthijnssens J 2017 Highly diverse population of Picornaviridae and other members of the Picornavirales, in Cameroonian fruit bats. BMC Genomics 18: 249. doi: 10.1186/s12864-017-3632-7. 28335731 PMC5364608 · DOI
  20. [22]Yinda CK, Conceição-Neto N, Zeller M, Heylen E, Maes P, Ghogomu SM, Van Ranst M, Matthijnssens J 2017 Novel highly divergent sapoviruses detected by metagenomics analysis in straw-colored fruit bats in Cameroon. Emerg Microbes Infect 6: e38. doi: 10.1038/emi.2017.20. 28536431 PMC5520483 · DOI
  21. [23]Yinda CK, Ghogomu SM, Conceição-Neto N, Beller L, Deboutte W, Vanhulle E, Maes P, Van Ranst M, Matthijnssens J 2018 Cameroonian fruit bats harbor divergent viruses, including rotavirus H, bastroviruses, and picobirnaviruses using an alternative genetic code. Virus Evol 4: vey008. doi: 10.1093/ve/vey008. 29644096 PMC5888411 · DOI
  22. [24]Steyer A, Gutiérrez-Aguire I, Kolenc M, Koren S, Kutnjak D, Pokorn M, Poljšak-Prijatelj M, Racki N, Ravnikar M, Sagadin M, Fratnik Steyer A, Toplak N 2013 High similarity of novel orthoreovirus detected in a child hospitalized with acute gastroenteritis to mammalian orthoreoviruses found in bats in Europe. J Clin Microbiol 51: 3818– 3825. doi: 10.1128/JCM.01531-13. 24025904 PMC3889772 · DOI
  23. [25]Lelli D, Moreno A, Lavazza A, Bresaola M, Canelli E, Boniotti MB, Cordioli P 2013 Identification of mammalian orthoreovirus type 3 in Italian bats. Zoonoses Public Health 60: 84– 92. doi: 10.1111/zph.12001. 22931153 · DOI
  24. [26]Ciarlet M, Estes M 2002 Rotaviruses: basic biology, epidemiology and methodologies, p 2573– 2773. In Britton G (ed), Encyclopedia of environmental microbiology, John Wiley & Sons, New York, NY.
  25. [27]Estes MK, Cohen J 1989 Rotavirus gene structure and function. Microbiol Rev 53: 410– 449. 2556635 PMC372748
  26. [28]Knowles NJ, Hovi T, Hyypiä T, King AMQ, Lindberg M, Pallansch MA, Palmenberg AC, Simmonds P, Skern T, Stanway G, Yamashita T, Zell R 2012 Picornaviridae, p 855– 880. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (ed), Virus taxonomy: classification and nomenclature of viruses. Ninth report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego, CA.
  27. [29]Tracy S, Chapman NM, Drescher KM, Kono K, Tapprich W 2006 Evolution of virulence in picornaviruses, p 193– 209. In Domingo E (ed), Quasispecies: concept and implications for virology. Springer, Berlin, Germany. 16568900
  28. [30]Wang X, Ren J, Gao Q, Hu Z, Sun Y, Li X, Rowlands DJ, Yin W, Wang J, Stuart DI, Rao Z, Fry EE 2015 Hepatitis A virus and the origins of picornaviruses. Nature 517: 85– 88. doi: 10.1038/nature13806. 25327248 PMC4773894 · DOI
  29. [31]Sadeuh-Mba SA, Bessaud M, Massenet D, Joffret M-L, Endegue M-C, Njouom R, Reynes J-M, Rousset D, Delpeyroux F 2013 High frequency and diversity of species C enteroviruses in Cameroon and neighboring countries. J Clin Microbiol 51: 759– 770. doi: 10.1128/JCM.02119-12. 23254123 PMC3592076 · DOI · Paper page
  30. [32]Kroneman A, Vennema H, Deforche K, Avoort HVD, Peñaranda S, Oberste MS, Vinjé J, Koopmans M 2011 An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol 51: 121– 125. doi: 10.1016/j.jcv.2011.03.006. 21514213 · DOI
  31. [33]Tolf C, Gullberg M, Johansson ES, Tesh RB, Andersson B, Lindberg AM 2009 Molecular characterization of a novel Ljungan virus (Parechovirus; Picornaviridae) reveals a fourth genotype and indicates ancestral recombination. J Gen Virol 90: 843– 853. doi: 10.1099/vir.0.007948-0. 19264646 PMC2889435 · DOI
  32. [34]Sun G, Wang Y, Tao G, Shen Q, Cao W, Chang X, Zhang W, Shao C, Yi M, Shao S, Yang Y 2012 Complete genome sequence of a novel type of human parechovirus strain reveals natural recombination events. J Virol 86: 8892– 8893. doi: 10.1128/JVI.01241-12. 22843855 PMC3421728 · DOI
  33. [35]Figueroa JP, Ashley D, King D, Hull B 1989 An outbreak of acute flaccid paralysis in Jamaica associated with echovirus type 22. J Med Virol 29: 315– 319. 2621458
  34. [36]Koskiniemi M, Paetau R, Linnavuori K 1989 Severe encephalitis associated with disseminated echovirus 22 infection. Scand J Infect Dis 21: 463– 466. 2587949
  35. [37]Oberste MS, Maher K, Kilpatrick DR, Pallansch MA 1999 Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 73: 1941– 1948. 9971773 PMC104435
  36. [38]Chuchaona W, Khamrin P, Yodmeeklin A, Saikruang W, Kongsricharoern T, Ukarapol N, Okitsu S, Hayakawa S, Ushijima H, Maneekarn N 2015 Detection and characterization of a novel human parechovirus genotype in Thailand. Infect Genet Evol 31: 300– 304. doi: 10.1016/j.meegid.2015.02.003. 25681699 · DOI
  37. [39]Holtz LR, Finkbeiner SR, Kirkwood CD, Wang D 2008 Identification of a novel picornavirus related to cosaviruses in a child with acute diarrhea. Virol J 5: 159. doi: 10.1186/1743-422X-5-159. 19102772 PMC2615758 · DOI
  38. [40]Naeem A, Hosomi T, Nishimura Y, Alam MM, Oka T, Zaidi SSZ, Shimizu H 2014 Genetic diversity of circulating Saffold viruses in Pakistan and Afghanistan. J Gen Virol 95: 1945– 1957. doi: 10.1099/vir.0.066498-0. 24899154 · DOI
  39. [41]Chiu CY, Greninger AL, Kanada K, Kwok T, Fischer KF, Runckel C, Louie JK, Glaser CA, Yagi S, Schnurr DP, Haggerty TD, Parsonnet J, Ganem D, DeRisi JL 2008 Identification of cardioviruses related to Theiler’s murine encephalomyelitis virus in human infections. Proc Natl Acad Sci U S A 105: 14124– 14129. doi: 10.1073/pnas.0805968105. 18768820 PMC2528868 · DOI
  40. [42]Ren L, Gonzalez R, Xiao Y, Xu X, Chen L, Vernet G, Paranhos-Baccalà G, Jin Q, Wang J 2009 Saffold cardiovirus in children with acute gastroenteritis, Beijing, China. Emerg Infect Dis 15: 1509– 1511. doi: 10.3201/eid1509.081531. 19788828 PMC2819865 · DOI
  41. [43]Cristina J, Costa-Mattioli M 2007 Genetic variability and molecular evolution of hepatitis A virus. Virus Res 127: 151– 157. doi: 10.1016/j.virusres.2007.01.005. 17328982 · DOI
  42. [44]Franco E, Meleleo C, Serino L, Sorbara D, Zaratti L 2012 Hepatitis A: epidemiology and prevention in developing countries. World J Hepatol 4: 68– 73. doi: 10.4254/wjh.v4.i3.68. 22489258 PMC3321492 · DOI
  43. [45]Tjon GMS, Wijkmans CJ, Coutinho RA, Koek AG, van den Hoek JAR, Leenders ACAP, Schneeberger PM, Bruisten SM 2005 Molecular epidemiology of hepatitis A in Noord-Brabant, The Netherlands. J Clin Virol 32: 128– 136. doi: 10.1016/j.jcv.2004.03.008. 15653415 · DOI
  44. [47]Xi JN, Graham DY, Wang KN, Estes MK 1990 Norwalk virus genome cloning and characterization. Science 250: 1580– 1583. 2177224
  45. [48]McFadden N, Bailey D, Carrara G, Benson A, Chaudhry Y, Shortland A, Heeney J, Yarovinsky F, Simmonds P, Macdonald A, Goodfellow I 2011 Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLoS Pathog 7: e1002413. doi: 10.1371/journal.ppat.1002413. 22174679 PMC3234229 · DOI
  46. [49]Zheng D-P, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS 2006 Norovirus classification and proposed strain nomenclature. Virology 346: 312– 323. doi: 10.1016/j.virol.2005.11.015. 16343580 · DOI
  47. [50]Oka T, Lu Z, Phan T, Delwart EL, Saif LJ, Wang Q 2016 Genetic characterization and classification of human and animal sapoviruses. PLoS One 11: e0156373. doi: 10.1371/journal.pone.0156373. 27228126 PMC4881899 · DOI
  48. [51]Olarte-Castillo XA, Hofer H, Goller KV, Martella V, Moehlman PD, East ML 2016 Divergent sapovirus strains and infection prevalence in wild carnivores in the Serengeti ecosystem: a long-term study. PLoS One 11: e0163548. doi: 10.1371/journal.pone.0163548. 27661997 PMC5035092 · DOI
  49. [54]Ng TFF, Zhang W, Sachsenröder J, Kondov NO, da Costa AC, Vega E, Holtz LR, Wu G, Wang D, Stine CO, Antonio M, Mulvaney US, Muench MO, Deng X, Ambert-Balay K, Pothier P, Vinjé J, Delwart E 2015 A diverse group of small circular ssDNA viral genomes in human and non-human primate stools. Virus Evol 1: vev017. doi: 10.1093/ve/vev017. 27774288 PMC5014484 · DOI
  50. [55]Phan TG, da Costa AC, del Valle Mendoza J, Bucardo-Rivera F, Nordgren J, O’Ryan M, Deng X, Delwart E 2016 The fecal virome of South and Central American children with diarrhea includes small circular DNA viral genomes of unknown origin. Arch Virol 161: 959– 966. doi: 10.1007/s00705-016-2756-4. 26780893 PMC4814309 · DOI
  51. [56]Smits SL, Schapendonk CME, van Beek J, Vennema H, Schürch AC, Schipper D, Bodewes R, Haagmans BL, Osterhaus ADME, Koopmans MP 2014 New viruses in idiopathic human diarrhea cases, the Netherlands. Emerg Infect Dis 20: 1218– 1222. doi: 10.3201/eid2007.140190. 24964003 PMC4073879 · DOI
  52. [57]Cheung AK, Ng TF, Lager KM, Alt DP, Delwart EL, Pogranichniy RM 2014 Unique circovirus-like genome detected in pig feces. Genome Announc 2: e00251-14. doi: 10.1128/genomeA.00251-14. 24723710 PMC3983299 · DOI
  53. [58]Woo PCY, Lau SKP, Teng JLL, Tsang AKL, Joseph M, Wong EYM, Tang Y, Sivakumar S, Bai R, Wernery R, Wernery U, Yuen K-Y 2014 Metagenomic analysis of viromes of dromedary camel fecal samples reveals large number and high diversity of circoviruses and picobirnaviruses. Virology 471–473: 117– 125. doi: 10.1016/j.virol.2014.09.020. PMC7112128 25461537 · DOI
  54. [59]Kraberger S, Argüello-Astorga GR, Greenfield LG, Galilee C, Law D, Martin DP, Varsani A 2015 Characterisation of a diverse range of circular replication-associated protein encoding DNA viruses recovered from a sewage treatment oxidation pond. Infect Genet Evol 31: 73– 86. doi: 10.1016/j.meegid.2015.01.001. 25583447 · DOI
  55. [60]Roux S, Enault F, Hurwitz BL, Sullivan MB 2015 VirSorter: mining viral signal from microbial genomic data. PeerJ 3: e985. doi: 10.7717/peerj.985. 26038737 PMC4451026 · DOI
  56. [61]Buchfink B, Xie C, Huson DH 2015 Fast and sensitive protein alignment using DIAMOND. Nat Methods 12: 59– 60. doi: 10.1038/nmeth.3176. 25402007 · DOI · Paper page
  57. [62]Bolduc B, Jang HB, Doulcier G, You Z-Q, Roux S, Sullivan MB 2017 vConTACT: an iVirus tool to classify double-stranded DNA viruses that infect Archaea and Bacteria. PeerJ 5: e3243. doi: 10.7717/peerj.3243. 28480138 PMC5419219 · DOI
  58. [63]Yinda CK, Zeller M, Conceicaõ-Neto N, Maes P, Deboutte W, Beller L, Heylen E, Ghogomu SM, Van Ranst M, Matthijnssens J 2016 Novel highly divergent reassortant bat rotaviruses in Cameroon, without evidence of zoonosis. Sci Rep 6: 34209. doi: 10.1038/srep34209. 27666390 PMC5035928 · DOI
  59. [64]Clokie MRJ, Millard AD, Letarov AV, Heaphy S 2011 Phages in nature. Bacteriophage 1: 31– 45. doi: 10.4161/bact.1.1.14942. 21687533 PMC3109452 · DOI
  60. [65]Ayukekbong JA, Fobisong C, Lindh M, Nkuo-Akenji T, Bergström T, Norder H 2014 Molecular analysis of enterovirus in Cameroon by partial 5′UTR-VP4 gene sequencing reveals a high genetic diversity and frequency of infections. J Med Virol 86: 2092– 2101. doi: 10.1002/jmv.23926. 24634190 · DOI
  61. [66]Sadeuh-Mba SA, Bessaud M, Joffret M-L, Endegue Zanga M-C, Balanant J, Mpoudi Ngole E, Njouom R, Reynes J-M, Delpeyroux F, Rousset D 2014 Characterization of enteroviruses from non-human primates in Cameroon revealed virus types widespread in humans along with candidate new types and species. PLoS Negl Trop Dis 8: e3052. doi: 10.1371/journal.pntd.0003052. 25079078 PMC4117447 · DOI
  62. [67]Cascio A, Bosco M, Vizzi E, Giammanco A, Ferraro D, Arista S 1996 Identification of picobirnavirus from faeces of Italian children suffering from acute diarrhea. Eur J Epidemiol 12: 545– 547. 8905320 PMC7088005
  63. [68]Pereira H, Linhares A, Candeias JA, Glass R 1993 National laboratory surveillance of viral agents of gastroenteritis in Brazil. Pan Am J Public Heal 27: 224– 233. 8220517
  64. [69]Lim ES, Wang D, Holtz LR 2016 The bacterial microbiome and virome milestones of infant development. Trends Microbiol 24: 801– 810. doi: 10.1016/j.tim.2016.06.001. 27353648 · DOI
  65. [70]Lim ES, Zhou Y, Zhao G, Bauer IK, Droit L, Ndao IM, Warner BB, Tarr PI, Wang D, Holtz LR 2015 Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat Med 21: 1228– 1234. doi: 10.1038/nm.3950. 26366711 PMC4710368 · DOI
  66. [71]Hong Y, Dover SL, Cole TE, Brasier CM, Buck KW 1999 Multiple mitochondrial viruses in an isolate of the Dutch elm disease fungus Ophiostoma novo-ulmi. Virology 258: 118– 127. doi: 10.1006/viro.1999.9691. 10329574 · DOI
  67. [72]Krishnamurthy SR, Wang D 2018 Extensive conservation of prokaryotic ribosomal binding sites in known and novel picobirnaviruses. Virology 516: 108– 114. doi: 10.1016/j.virol.2018.01.006. 29346073 · DOI · Paper page
  68. [73]Dyall SD, Brown MT, Johnson PJ 2004 Ancient invasions: from endosymbionts to organelles. Science 304: 253– 257. doi: 10.1126/science.1094884. 15073369 · DOI
  69. [75]Katz JM, Plowden J, Renshaw-Hoelscher M, Lu X, Tumpey TM, Sambhara S 2004 Immunity to influenza. Immunol Res 29: 113– 124. doi: 10.1385/IR:29:1-3:113. 15181275 · DOI
  70. [76]Brodin P, Davis MM 2017 Human immune system variation. Nat Rev Immunol 17: 21– 29. doi: 10.1038/nri.2016.125. 27916977 PMC5328245 · DOI · Paper page
  71. [78]Béland K, Dore-Nguyen M, Gagné M-J, Patey N, Brassard J, Alvarez F, Halac U 2014 Torque Teno virus in children who underwent orthotopic liver transplantation: new insights about a common pathogen. J Infect Dis 209: 247– 254. doi: 10.1093/infdis/jit423. 23922368 · DOI
  72. [79]Maggi F, Pifferi M, Fornai C, Andreoli E, Tempestini E, Vatteroni M, Presciuttini S, Marchi S, Pietrobelli A, Boner A, Pistello M, Bendinelli M 2003 TT virus in the nasal secretions of children with acute respiratory diseases: relations to viremia and disease severity. J Virol 77: 2418– 2425. 12551979 PMC141071
  73. [80]Chung J-Y, Han TH, Koo JW, Kim SW, Seo JK, Hwang ES 2007 Small anellovirus infections in Korean children. Emerg Infect Dis 13: 791– 793. doi: 10.3201/eid1305.061149. 18044047 PMC2738455 · DOI
  74. [81]Miyamoto M, Takahashi H, Sakata I, Adachi Y 2000 Hepatitis-associated aplastic anemia and transfusion-transmitted virus infection. Intern Med 39: 1068– 1070. 11197792
  75. [82]Spandole S, Cimponeriu D, Berca LM, Mihăescu G 2015 Human anelloviruses: an update of molecular, epidemiological and clinical aspects. Arch Virol 160: 893– 908. doi: 10.1007/s00705-015-2363-9. 25680568 · DOI
  76. [84]Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI 2010 Viruses in the fecal microbiota of monozygotic twins and their mothers. Nature 466: 334– 338. doi: 10.1038/nature09199. 20631792 PMC2919852 · DOI
  77. [85]Rohwer F 2003 Global phage diversity. Cell 113: 141. 12705861
  78. [86]Conceicao-Neto N, Zeller M, Lefrere H, De Bruyn P, Beller L, Deboutte W, Yinda CK, Lavigne R, Maes P, Van Ranst M, Heylen E, Matthijnssens J 2015 Modular approach to customise sample preparation procedures for viral metagenomics: a reproducible protocol for virome analysis. Sci Rep 5: 16532. doi: 10.1038/srep16532. 26559140 PMC4642273 · DOI
  79. [87]Bolger AM, Lohse M, Usadel B 2014 Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114– 2120. doi: 10.1093/bioinformatics/btu170. 24695404 PMC4103590 · DOI · Paper page
  80. [88]Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA 2012 SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19: 455– 477. doi: 10.1089/cmb.2012.0021. 22506599 PMC3342519 · DOI
  81. [89]Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH 2015 CDD: NCBI’s conserved domain database. Nucleic Acids Res 43: D222– D226. doi: 10.1093/nar/gku1221. 25414356 PMC4383992 · DOI
  82. [90]Kumar S, Stecher G, Tamura K 2016 MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 1870– 1874. doi: 10.1093/molbev/msw054. 27004904 PMC8210823 · DOI
  83. [91]Katoh K, Misawa K, Kuma K, Miyata T 2002 MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059– 3066. 12136088 PMC135756
  84. [92]Keane TM, Creevey CJ, Pentony MM, Naughton TJ, McInerney JO 2006 Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6: 29. doi: 10.1186/1471-2148-6-29. 16563161 PMC1435933 · DOI
  85. [93]Stamatakis A 2014 RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312– 1313. doi: 10.1093/bioinformatics/btu033. 24451623 PMC3998144 · DOI · Paper page
  86. [95]Langmead B, Salzberg SL 2012 Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357– 359. doi: 10.1038/nmeth.1923. 22388286 PMC3322381 · DOI · Paper page
  87. [98]Grissa I, Vergnaud G, Pourcel C 2007 The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8: 172. doi: 10.1186/1471-2105-8-172. 17521438 PMC1892036 · DOI
  88. [99]Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ 2010 Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119. doi: 10.1186/1471-2105-11-119. 20211023 PMC2848648 · DOI
  89. [100]Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, Christmas R, Avila-Campilo I, Creech M, Gross B, Hanspers K, Isserlin R, Kelley R, Killcoyne S, Lotia S, Maere S, Morris J, Ono K, Pavlovic V, Pico AR, Vailaya A, Wang P-L, Adler A, Conklin BR, Hood L, Kuiper M, Sander C, Schmulevich I, Schwikowski B, Warner GJ, Ideker T, Bader GD 2007 Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2: 2366– 2382. doi: 10.1038/nprot.2007.324. 17947979 PMC3685583 · DOI · Paper page

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Sorted by citations

Authors
Yinda, C. K., Vanhulle, E., Conceição-Neto, N., Beller, L., Deboutte, W., Shi, C., Ghogomu, S. M., Maes, P., Van Ranst, M., & Matthijnssens, J.
Affiliations
  • Rega Institute for Medical Research (BE)
  • Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Viral Metagenomics, KU Leuven-University of Leuven, Leuven, Belgium
  • University of Buea (CM)
  • Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory for Clinical and Epidemiological Virology, KU Leuven-University of Leuven, Leuven, Belgium
Corresponding author
Matthijnssens, Jelle
Venue
mSphere
Published
2019-02-27
Volume
4
Issue
1
ISSN
2379-5042 (ISSN-L)
OpenAlex
W2911301213
Cited by
75
References
6
Citations by year
2026: 6 · 2025: 5 · 2024: 10 · 2023: 6 · 2022: 10 · 2021: 18 · 2020: 17 · 2019: 3
FWCI
9.20
Type
journal article
Language
en
Open access
Locations
  • mSphere (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Lirias (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
KU Leuven (EJX-C9928-StG/15/020BF)
Topics
  • Health Sciences › Medicine › Infectious Diseases › Viral gastroenteritis research and epidemiology
  • Physical Sciences › Environmental Science › Ecology › Bacteriophages and microbial interactions
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
Keywords
gut virome, enteric viruses, interspecies transmission, viral diversity, diarrhea, Cameroon, viral epidemiology
MeSH terms
Adolescent, Adult, Aged, Aged, 80 and over, Animals, Cameroon, Child, Child, Preschool, Diarrhea, Feces, Female, Humans, Infant, Infant, Newborn, Male, Middle Aged, Phylogeny, Virus Diseases, Viruses, Zoonoses, Prevalence, Disease Transmission, Infectious, Young Adult, Metagenomics

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