Widespread Infection with Homologues of Human Parvoviruses B19, PARV4, and Human Bocavirus of Chimpanzees and Gorillas in the Wild

Journal of Virology

Volumn 84, Issue 19, 2010, Pages 10289-10296

  Sharp, Colin P ^a   LeBreton, Matthew ^b   Kantola, Kalle ^c   Nana, Ahmadou ^b   Diffo, Joseph Le Doux ^b   Djoko, Cyrille F ^b   Tamoufe, Ubald ^b   Kiyang, John A ^d   Babila, Tafon G ^e   Ngole, Eitel Mpoudi ^f   Pybus, Oliver G ^g   Delwart, Eric ^h   Delaporte, Eric ⁱ   Peeters, Martine ⁱ   Soderlund Venermo, Maria ^c   Hedman, Klaus ^c,j   Wolfe, Nathan D ^b,k   Simmonds, Peter ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b Global Viral Forecasting Initiative   (United States)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^d Limbe Wildlife Centre   (Cameroon)

^e Ape Action Africa   (Cameroon)

^f Projet Prevention du Sida au Cameroun PRESICA   (Cameroon)

^g UNIVERSITY OF OXFORD   (United Kingdom)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^j UNIVERSITY OF HELSINKI   (Finland)

^k STANFORD UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS ANTIBODY; VIRUS ANTIGEN;

APE; ARTICLE; BOCAVIRUS; CHIMPANZEE; ENZYME LINKED IMMUNOSORBENT ASSAY; FECES ANALYSIS; GENETIC VARIABILITY; GORILLA; HUMAN; HUMAN PARVOVIRUS B19; MONKEY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARVOVIRUS; PARVOVIRUS INFECTION; PARVOVIRUS PARV4; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SCREENING; ANIMAL; APE DISEASES; CAMEROON; CERCOPITHECIDAE; CLASSIFICATION; GENETIC RECOMBINATION; GENETICS; HUMAN BOCAVIRUS; ISOLATION AND PURIFICATION; MOLECULAR EPIDEMIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MONKEY DISEASES; PAN TROGLODYTES; PARVOVIRIDAE; PARVOVIRIDAE INFECTIONS; SPECIES DIFFERENCE; VETERINARY; VIROLOGY; WILD ANIMAL;

ANIMALS; ANIMALS, WILD; APE DISEASES; CAMEROON; CERCOPITHECIDAE; EVOLUTION, MOLECULAR; GENETIC VARIATION; GORILLA GORILLA; HUMAN BOCAVIRUS; HUMANS; MOLECULAR EPIDEMIOLOGY; MOLECULAR SEQUENCE DATA; MONKEY DISEASES; PAN TROGLODYTES; PARVOVIRIDAE INFECTIONS; PARVOVIRUS; PARVOVIRUS B19, HUMAN; PHYLOGENY; RECOMBINATION, GENETIC; SEROEPIDEMIOLOGIC STUDIES; SPECIES SPECIFICITY;

BOCAVIRUS; CERCOPITHECIDAE; ERYTHROVIRUS; HUMAN BOCAVIRUS; PAN; PAPIO; PARVOVIRUS; PRIMATES;

EID: 77956834049     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01304-10     Document Type: Article

References (65)

1. Allander, T. 2008. Human bocavirus. J. Clin. Virol. 41:29-33.
2. Allander, T., T. Jartti, S. Gupta, H. G. Niesters, P. Lehtinen, R. Osterback, T. Vuorinen, M. Waris, A. Bjerkner, A. Tiveljung-Lindell, B. G. van den Hoogen, T. Hyypia, and O. Ruuskanen. 2007. Human bocavirus and acute wheezing in children. Clin. Infect. Dis. 44:904-910.
3. Allander, T., M. T. Tammi, M. Eriksson, A. Bjerkner, A. Tiveljung-Lindell, and B. Andersson. 2005. Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc. Natl. Acad. Sci. U. S. A. 102:12891-12896.
4. Arthur, J. L., G. D. Higgins, G. P. Davidson, R. C. Givney, and R. M. Ratcliff. 2009. A novel bocavirus associated with acute gastroenteritis in Australian children. PLoS Pathog. 5:e1000391.
5. Brown, K. E., S. M. Anderson, and N. S. Young. 1993. Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 262:114-117.
6. Brown, K. E., Z. Liu, G. Gallinella, S. Wong, I. P. Mills, and M. G. O'Sullivan. 2004. Simian parvovirus infection: a potential zoonosis. J. Infect. Dis. 190:1900-1907.
7. Candotti, D., N. Etiz, A. Parsyan, and J. P. Allain. 2004. Identification and characterization of persistent human erythrovirus infection in blood donor samples. J. Virol. 78:12169-12178.
8. Cecchini, S., A. Negrete, T. Virag, B. S. Graham, J. I. Cohen, and R. M. Kotin. 2009. Evidence of prior exposure to human bocavirus as determined by a retrospective serological study of 404 serum samples from adults in the United States. Clin. Vaccine Immunol. 16:597-604.
9. Chen, K. C., B. C. Shull, E. A. Moses, M. Lederman, E. R. Stout, and R. C. Bates. 1986. Complete nucleotide sequence and genome organization of bovine parvovirus. J. Virol. 60:1085-1097.
10. Chieochansin, T., A. Kapoor, E. Delwart, Y. Poovorawan, and P. Simmonds. 2009. Absence of detectable replication of human bocavirus species 2 in the respiratory tract. Emerg. Infect. Dis. 15:1503-1505.
11. Chow, B. D., Z. Ou, and F. P. Esper. 2010. Newly recognized bocaviruses (HBoV, HBoV2) in children and adults with gastrointestinal illness in the United States. J. Clin. Virol. 47:143-147.
12. Eis-Hubinger, A. M., U. Reber, T. Abdul-Nour, U. Glatzel, H. Lauschke, and U. Putz. 2001. Evidence for persistence of parvovirus B19 DNA in livers of adults. J. Med. Virol. 65:395-401.
13. Fryer, J. F., A. Kapoor, P. D. Minor, E. Delwart, and S. A. Baylis. 2006. Novel parvovirus and related variant in human plasma. Emerg. Infect. Dis. 12:151-154.
14. Fryer, J. F., S. B. Lucas, D. Padley, and S. A. Baylis. 2007. Parvoviruses PARV4/5 in hepatitis C virus-infected patient. Emerg. Infect. Dis. 13:175-176.
15. Gilbert, N. L., T. W. Gyorkos, C. Beliveau, E. Rahme, C. Muecke, and J. C. Soto. 2005. Seroprevalence of parvovirus B19 infection in daycare educators. Epidemiol. Infect. 133:299-304.
16. Green, S. W., I. Malkovska, M. G. O'Sullivan, and K. E. Brown. 2000. Rhesus and pig-tailed macaque parvoviruses: identification of two new members of the erythrovirus genus in monkeys. Virology 269:105-112.
17. Hedman, L., M. Soderlund-Venermo, T. Jartti, O. Ruuskanen, and K. Hedman. 2010. Dating of human bocavirus infection with protein-denaturing IgG-avidity assays-secondary immune activations are ubiquitous in immunocompetent adults. J. Clin. Virol. 48:44-48.
18. Heegaard, E. D., and K. E. Brown. 2002. Human parvovirus B19. Clin. Microbiol. Rev. 15:485-505.
19. Hindiyeh, M. Y., N. Keller, M. Mandelboim, D. Ram, J. Rubinov, L. Regev, V. Levy, S. Orzitzer, H. Shaharabani, R. Azar, E. Mendelson, and Z. Grossman. 2008. High rate of human bocavirus and adenovirus coinfection in hospitalized Israeli children. J. Clin. Microbiol. 46:334-337.
20. Hokynar, K., J. Brunstein, M. Soderlund-Venermo, O. Kiviluoto, E. K. Partio, Y. Konttinen, and K. Hedman. 2000. Integrity and full coding sequence of B19 virus DNA persisting in human synovial tissue. J. Gen. Virol. 81:1017-1025.
21. Hokynar, K., M. Soderlund-Venermo, M. Pesonen, A. Ranki, O. Kiviluoto, E. K. Partio, and K. Hedman. 2002. A new parvovirus genotype persistent in human skin. Virology 302:224-228.
22. Jones, M. S., A. Kapoor, V. V. Lukashov, P. Simmonds, F. Hecht, and E. Delwart. 2005. New DNA viruses identified in patients with acute viral infection syndrome. J. Virol. 79:8230-8236.
23. Kapoor, A., P. Simmonds, E. Slikas, L. Li, L. Bodhidatta, O. Sethabutr, H. Triki, O. Bahri, B. S. Oderinde, M. M. Baba, D. N. Bukbuk, J. Besser, J. Bartkus, and E. Delwart. 2010. Human bocaviruses are highly diverse, dispersed, recombination prone, and prevalent in enteric infections. J. Infect. Dis. 201:1633-1643.
24. Kapoor, A., E. Slikas, P. Simmonds, T. Chieochansin, A. Naeem, S. Shaukat, M. M. Alam, S. Sharif, M. Angez, S. Zaidi, and E. Delwart. 2009. A newly identified bocavirus species in human stool. J. Infect. Dis. 199:196-200.
25. Keele, B. F., F. Van Heuverswyn, Y. Li, E. Bailes, J. Takehisa, M. L. Santiago, F. Bibollet-Ruche, Y. Chen, L. V. Wain, F. Liegeois, S. Loul, E. M. Ngole, Y. Bienvenue, E. Delaporte, J. F. Brookfield, P. M. Sharp, G. M. Shaw, M. Peeters, and B. H. Hahn. 2006. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313:523-526.
26. Kerr, J. R., J. P. Cartron, M. D. Curran, J. E. Moore, J. R. Elliott, and R. A. Mollan. 1995. A study of the role of parvovirus B19 in rheumatoid arthritis. Br. J. Rheumatol. 34:809-813.
27. Kuethe, F., J. Lindner, K. Matschke, J. J. Wenzel, P. Norja, K. Ploetze, S. Schaal, V. Kamvissi, S. R. Bornstein, U. Schwanebeck, and S. Modrow. 2009. Prevalence of parvovirus B19 and human bocavirus DNA in the heart of patients with no evidence of dilated cardiomyopathy or myocarditis. Clin. Infect. Dis. 49:1660-1666.
28. Kuhl, U., M. Pauschinger, M. Noutsias, B. Seeberg, T. Bock, D. Lassner, W. Poller, R. Kandolf, and H. P. Schultheiss. 2005. High prevalence of viral genomes and multiple viral infections in the myocardium of adults with "idiopathic" left ventricular dysfunction. Circulation 111:887-893.
29. Kurtzman, G. J., B. J. Cohen, A. M. Field, R. Oseas, R. M. Blaese, and N. S. Young. 1989. Immune response to B19 parvovirus and an antibody defect in persistent viral infection. J. Clin. Invest. 84:1114-1123.
30. Lahtinen, A., P. Kivela, L. Hedman, A. Kumar, A. Kantele, M. Lappalainen, K. Liitsola, M. Ristola, E. Delwart, C. Sharp, P. Simmonds, M. Soderlund-Venermo, and K. Hedman. Human parvovirus PARV4 - comprehensive serodiagnostics and identification of primary infections. Emerg. Infect. Dis., in press.
31. Lau, S. K., P. C. Woo, H. Tse, C. T. Fu, W. K. Au, X. C. Chen, H. W. Tsoi, T. H. Tsang, J. S. Chan, D. N. Tsang, K. S. Li, C. W. Tse, T. K. Ng, O. T. Tsang, B. J. Zheng, S. Tam, K. H. Chan, B. Zhou, and K. Y. Yuen. 2008. Identification of novel porcine and bovine parvoviruses closely related to human parvovirus 4. J. Gen. Virol. 89:1840-1848.
32. Lindner, J., L. Karalar, S. Zehentmeier, A. Plentz, H. Pfister, W. Struff, M. Kertai, H. Segerer, and S. Modrow. 2008. Humoral immune response against human bocavirus VP2 virus-like particles. Viral Immunol. 21:443-449.
33. Longhi, E., G. Bestetti, V. Acquaviva, A. Foschi, R. Piolini, L. Meroni, C. Magni, S. Antinori, C. Parravicini, and M. Corbellino. 2007. Human parvovirus 4 in the bone marrow of Italian patients with AIDS. AIDS 21:1481-1483.
34. Lukashov, V. V., and J. Goudsmit. 2001. Evolutionary relationships among parvoviruses: virus-host coevolution among autonomous primate parvoviruses and links between adeno-associated and avian parvoviruses. J. Virol. 75:2729-2740.
35. Lurcharchaiwong, W., T. Chieochansin, S. Payungporn, A. Theamboonlers, and Y. Poovorawan. 2008. Parvovirus 4 (PARV4) in serum of intravenous drug users and blood donors. Infection 36:488-491.
36. Manning, A., V. Russell, K. L. G. H. Eastick, N. Hallam, K. E. Templeton, and P. Simmonds. 2006. Epidemiological profile and clinical associations of human bocavirus and other human parvoviruses. J. Infect. Dis. 194:1283-1290.
37. Manning, A., S. J. Willey, J. E. Bell, and P. Simmonds. 2007. Comparison of tissue distribution, persistence, and molecular epidemiology of parvovirus B19 and novel human parvoviruses PARV4 and human bocavirus. J. Infect. Dis. 195:1345-1552.
38. Martin, E. T., M. P. Fairchok, J. Kuypers, A. Magaret, D. M. Zerr, A. Wald, and J. A. Englund. 2010. Frequent and prolonged shedding of bocavirus in young children attending daycare. J. Infect. Dis. 201:1625-1632.
39. Mossong, J., N. Hens, V. Friederichs, I. Davidkin, M. Broman, B. Litwinska, J. Siennicka, A. Trzcinska, P. V. Damme, P. Beutels, A. Vyse, Z. Shkedy, M. Aerts, M. Massari, and G. Gabutti. 2008. Parvovirus B19 infection in five European countries: seroepidemiology, force of infection and maternal risk of infection. Epidemiol. Infect. 136:1059-1068.
40. Neel, C., L. Etienne, Y. Li, J. Takehisa, R. S. Rudicell, I. N. Bass, J. Moudindo, A. Mebenga, A. Esteban, F. Van Heuverswyn, F. Liegeois, P. J. Kranzusch, P. D. Walsh, C. M. Sanz, D. B. Morgan, J. B. Ndjango, J. C. Plantier, S. Locatelli, M. K. Gonder, F. H. Leendertz, C. Boesch, A. Todd, E. Delaporte, E. Mpoudi-Ngole, B. H. Hahn, and M. Peeters. 2010. Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas. J. Virol. 84:1464-1476.
41. Nguyen, Q. T., S. Wong, E. D. Heegaard, and K. E. Brown. 2002. Identification and characterization of a second novel human erythrovirus variant, A6. Virology 301:374-380.
42. Norja, P., A. M. Eis-Hubinger, M. Soderlund-Venermo, K. Hedman, and P. Simmonds. 2008. Rapid sequence change and geographical spread of human parvovirus B19; comparison of B19 evolution in acute and persistent infections. J. Virol. 82:6427-6433.
43. Norja, P., K. Hokynar, L. M. Aaltonen, R. Chen, A. Ranki, E. K. Partio, O. Kiviluoto, I. Davidkin, T. Leivo, A. M. Eis-Hubinger, B. Schneider, H. P. Fischer, R. Tolba, O. Vapalahti, A. Vaheri, M. Soderlund-Venermo, and K. Hedman. 2006. Bioportfolio: lifelong persistence of variant and prototypic erythrovirus DNA genomes in human tissue. Proc. Natl. Acad. Sci. U. S. A. 103:7450-7453.
44. O'Sullivan, M. G., D. C. Anderson, J. D. Fikes, F. T. Bain, C. S. Carlson, S. W. Green, N. S. Young, and K. E. Brown. 1994. Identification of a novel simian parvovirus in cynomolgus monkeys with severe anemia. A paradigm of human B19 parvovirus infection. J. Clin. Invest. 93:1571-1576.
45. Panning, M., R. Kobbe, S. Vollbach, J. F. Drexler, S. Adjei, O. Adjei, C. Drosten, J. May, and A. M. Eis-Hubinger. 2010. Novel human parvovirus 4 genotype 3 in infants, Ghana. Emerg. Infect. Dis. 16:1143-1146.
46. Parrish, C. R. 1999. Host range relationships and the evolution of canine parvovirus. Vet. Microbiol. 69:29-40.
47. Parsyan, A., C. Szmaragd, J. P. Allain, and D. Candotti. 2007. Identification and genetic diversity of two human parvovirus B19 genotype 3 subtypes. J. Gen. Virol. 88:428-431.
48. Rohrer, C., B. Gartner, A. Sauerbrei, S. Bohm, B. Hottentrager, U. Raab, W. Thierfelder, P. Wutzler, and S. Modrow. 2008. Seroprevalence of parvovirus B19 in the German population. Epidemiol. Infect. 136:1564-1575.
49. Sanabani, S., W. K. Neto, J. Pereira, and E. C. Sabino. 2006. Sequence variability of human erythroviruses present in bone marrow of Brazilian patients with various parvovirus B19-related hematological symptoms. J. Clin. Microbiol. 44:604-606.
50. Santos, N., T. C. Peret, C. D. Humphrey, M. C. Albuquerque, R. C. Silva, F. J. Benati, X. Lu, and D. D. Erdman. 2010. Human bocavirus species 2 and 3 in Brazil. J. Clin. Virol. 48:127-130.
51. Schildgen, O., A. Muller, T. Allander, I. M. Mackay, S. Volz, B. Kupfer, and A. Simon. 2008. Human bocavirus: passenger or pathogen in acute respiratory tract infections? Clin. Microbiol. Rev. 21:291-304.
52. Schneider, B., J. F. Fryer, U. Reber, H. P. Fischer, R. H. Tolba, S. A. Baylis, and A. M. Eis-Hubinger. 2008. Persistence of novel human parvovirus PARV4 in liver tissue of adults. J. Med. Virol. 80:345-351.
53. Servant, A., S. Laperche, F. Lallemand, V. Marinho, M. G. De Saint, J. F. Meritet, and A. Garbarg-Chenon. 2002. Genetic diversity within human erythroviruses: identification of three genotypes. J. Virol. 76:9124-9134. (Pubitemid 34919871)
54. Sharp, C. P., A. Lail, S. Donfield, R. Simmons, C. Leen, P. Klenerman, E. Delwart, E. D. Gomperts, and P. Simmonds. 2009. High frequencies of exposure to the novel human parvovirus, PARV4 in haemophiliacs and injecting drug users detected by a serological assay for PARV4 antibodies. J. Infect. Dis. 200:1119-1125.
55. Sharp, C. P., M. Vermeulen, Y. Nébie, C. F. Djoko, M. LeBreton, U. Tamoufe, A. W. Rimoin, P. K. Kayembe, J. K. Carr, A. Servant-Delmas, S. Laperche, A. Harrison, O. Pybus, E. Delwart, N. D. Wolfe, A. Saville, J. Lefrère, and P. Simmonds. Widespread exposure to PARV4 infection in sub-Saharan Africa identified by serological screening for IgG antibodies to viral capsid protein. Emerg. Infect. Dis., in press.
56. Simmonds, P., J. Douglas, G. Bestetti, E. Longhi, S. Antinori, C. Parravicini, and M. Corbellino. 2008. A third genotype of the human parvovirus PARV4 in sub-Saharan Africa. J. Gen. Virol. 89:2299-2302.
57. Simmonds, P., A. Manning, R. Kenneil, F. W. Carnie, and J. E. Bell. 2007. Parenteral transmission of the novel human parvovirus, PARV4. Emerg. Infect. Dis. 13:1386-1388.
58. Soderlund, M., C. S. Brown, W. J. Spaan, L. Hedman, and K. Hedman. 1995. Epitope type-specific IgG responses to capsid proteins VP1 and VP2 of human parvovirus B19. J. Infect. Dis. 172:1431-1436.
59. Soderlund, M., R. von Essen, J. Haapasaari, U. Kiistala, O. Kiviluoto, and K. Hedman. 1997. Persistence of parvovirus B19 DNA in synovial membranes of young patients with and without chronic arthropathy. Lancet 349: 1063-1065.
60. Soderlund-Venermo, M., A. Lahtinen, T. Jartti, L. Hedman, K. Kemppainen, P. Lehtinen, T. Allander, O. Ruuskanen, and K. Hedman. 2009. Clinical assessment and improved diagnosis of bocavirus-induced wheezing in children, Finland. Emerg. Infect. Dis. 15:1423-1430.
61. Song, J. R., Y. Jin, Z. P. Xie, H. C. Gao, N. G. Xiao, W. X. Chen, Z. Q. Xu, K. L. Yan, Y. Zhao, Y. D. Hou, and Z. J. Duan. 2010. Novel human bocavirus in children with acute respiratory tract infection. Emerg. Infect. Dis. 16:324-327.
62. Vyse, A. J., N. J. Andrews, L. M. Hesketh, and R. Pebody. 2007. The burden of parvovirus B19 infection in women of childbearing age in England and Wales. Epidemiol. Infect. 135:1354-1362.
63. Williams, J. V. 2010. Deja vu all over again: Koch's postulates and virology in the 21st century. J. Infect. Dis. 201:1611-1614.
64. Yoo, B. C., D. H. Lee, S. M. Park, J. W. Park, C. Y. Kim, H. S. Lee, J. S. Seo, K. J. Park, and W. S. Ryu. 1999. A novel parvovirus isolated from Manchurian chipmunks. Virology 253:250-258.
65. Zehender, G., C. De Maddalena, M. Canuti, A. Zappa, A. Amendola, A. Lai, M. Galli, and E. Tanzi. 2010. Rapid molecular evolution of human bocavirus revealed by Bayesian coalescent inference. Infect. Genet. Evol. 10:215-220.