Porcine circovirus type 2 and porcine circovirus-associated disease

Journal of Veterinary Internal Medicine

Volumn 23, Issue 6, 2009, Pages 1151-1163

  Gillespie, J ^a   Opriessnig, T ^a   Meng, X J ^a   Pelzer, K ^a   Buechner Maxwell, V ^a  

^a VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

Author keywords

Epidemiology; Immunohistochemistry; Infectious diseases; Microbiology; Respiratory tract; Viral virulence mechanisms; Virology general

Indexed keywords

VIRUS VACCINE;

ANIMAL; ANIMAL DISEASE; CIRCOVIRIDAE INFECTION; CIRCOVIRUS; CLASSIFICATION; EPIDEMIC; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; REVIEW; SWINE DISEASE; VIROLOGY;

ANIMALS; CIRCOVIRIDAE INFECTIONS; CIRCOVIRUS; DISEASE OUTBREAKS; SWINE DISEASES; VIRAL VACCINES;

ARTERIVIRUS; CIRCOVIRIDAE; CIRCOVIRUS; DNA VIRUSES; MYCOPLASMA; PORCINE CIRCOVIRUS; PORCINE CIRCOVIRUS 2; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE;

EID: 70350378485     PISSN: 08916640     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1939-1676.2009.0389.x     Document Type: Review

References (166)

1. British Pig Executive (BPEX). Pig Yearbook 2006. Kenilworth, Warwickshire, UK: Agriculture and Horticulture Develop-ment Board; 2006:47-50.
2. Carman S, McEwen B, DeLay J, et al. Porcine Circovirus type-2 associated disease continued in fall of 2005. Guelph Univ Anim Health Lab Newslett 2006;10:6-7.
3. Fenaux M, Halbur PG, Gill M, et al. Genetic characterization of type 2 porcine circovirus (PCV-2) from pigs with postweaning multisystemic wasting syndrome in different geographic regions of North America and development of a differential PCR-restriction fragment length polymorphism assay to detect and differentiate between infections with PCV-1 and PCV-2. J Clin Microbiol 2000;38: 2494-2503.
4. Olvera A, Cortey M, Segales J. Molecular evolution of porcine circovirus type 2 genomes: Phylogeny and clonality. Virol-ogy 2007;357:175-185.
5. Tischer I, Gelderblom H, Vettermann W, et al. A very small porcine virus with circular single-stranded DNA. Nature 1982;295: 64-66.
6. Allan GM, McNeilly F, Cassidy JP, et al. Pathogenesis of porcine circovirus; experimental infections of colostrum deprived piglets and examination of pig foetal material. Vet Microbiol 1995;44:49-64.
7. Allan GM, Ellis JA. Porcine circoviruses: A review. J Vet Diagn Invest 2000;12:3-14.
8. Tischer I, Mields W, Wolff D, et al. Studies on epidemiology and pathogenicity of porcine circovirus. Arch Virol 1986;91:271-276.
9. Allan GM, McNeilly F, Kennedy S, et al. Isolation of porcine circovirus-like viruses from pigs with a wasting disease in the USA and Europe. J Vet Diagn Invest 1998;10:3-10.
10. Ellis J, Clark E, Haines D, et al. Porcine circovirus-2 and concurrent infections in the field. Vet Microbiol 2004;98:159-163.
11. Harding J, Clark E. Recognizing and diagnosing postweaning multisystemic wasting syndrome (PMWS). J Swine Health Prod 1997;5:201-203.
12. Meehan BM, McNeilly F, Todd D, et al. Characterization of novel circovirus DNAs associated with wasting syndromes in pigs. J Gen Virol 1998;79(Part 9):2171-2179.
13. Segales J, Allan GM, Domingo M. Porcine circovirus diseases. Anim Health Res Rev 2005;6:119-142.
14. Allan G, McNeilly F, Meehan B. Isolation and characteriza-tion of circoviruses from pigs with wasting syndrome in Spain, Denmark, and Northern Ireland. Vet Microbiol 1999;66:115-123.
15. Grierson SS, King DP, Sandvik T, et al. Detection and genetic typing of type 2 porcine circoviruses in archived pig tissues from the UK. Arch Virol 2004;149:1171-1183.
16. Sanchez R, Nauwynch G, Pensaert M. Proceedings of the International Conference of ssDNA Viruses, Plants, Birds, Pigs, and Primates, St Malo, France, 2001, p. 122.
17. Walker IW, Konoby CA, Jewhurst VA, et al. Development and application of a competitive enzyme-linked immunosorbent as-say for the detection of serum antibodies to porcine circovirus type 2. J Vet Diagn Invest 2000;12:400-405.
18. Magar R, Muller P, Larochelle R. Retrospective serological survey of antibodies to porcine circovirus type 1 and type 2. Can J Vet Res 2000;64:184-186.
19. Rodriguez-Arrioja GM, Segales J, Rosell C, et al. Retro-spective study on porcine circovirus type 2 infection in pigs from 1985 to 1997 in Spain. J Vet Med B Infect Dis Vet Public Health 2003;50:99-101.
20. Opriessnig T, Yu S, Thacker EL, et al. Derivation of porcine circovirus type 2-negative pigs from positive breeding herds. J Swine Health Prod 2004;12:186-191.
21. USDA. Part II: Reference of Swine Health and Health Management in the United States. Fort Collins, CO: USDA:APHIS, VS, CEAH, National Animal Health Monitoring System; 2000, #N3550202. Available at: http://nahms.aphis.usda.gov/swine/swine2000/Swine2kHi2.pdf. Accessed November 4, 2008.
22. USDA. Swine 2006, Part II: Reference of Swine Health and Health Management Practices in the United States. Fort Collins, CO: USDA:APHIS, VS, CEAH; 2006, #N4791207. Available at: http://nahms.aphis.usda.gov/swine/swine2006/Swine2006_highlightsPt 2.pdf. Accessed November 4, 2008.
23. Opriessnig T, Meng XJ, Halbur PG. Porcine circovirus type 2 associated disease: Update on current terminology, clinical man-ifestations, pathogenesis, diagnosis, and intervention strategies. J Vet Diagn Invest 2007;19:591-615.
24. Todd D, Bendinelli M, Biagini P. Circoviridae. In: Fauquet MA, Mayo J, Maniloff U, Desselberger LA, eds. Ball Virus Taxonomy, Eighth Report of the International Committee on Taxonomy of Viruses. London: Elsevier Academic Press; 2005:327-334.
25. Gelderblom H, Kling S, Lurz R, et al. Morphological characterization of chicken anaemia agent (CAA). Arch Virol 1989;109: 115-120.
26. Niagro FD, Forsthoefel AN, Lawther RP, et al. Beak and feather disease virus and porcine circovirus genomes: Intermediates between the geminiviruses and plant circoviruses. Arch Virol 1998; 143:1723-1744.
27. Biagini P, Gallian P, Attoui H, et al. Genetic analysis of full-length genomes and subgenomic sequences of TT virus-like mini vi-rus human isolates. J Gen Virol 2001;82:379-383.
28. Miyata H, Tsunoda H, Kazi A, et al. Identification of a novel GC-rich 113-nucleotide region to complete the circular, single-stranded DNA genome of TT virus, the first human circovirus. J Virol 1999;73:3582-3586.
29. Nishizawa T, Okamoto H, Konishi K, et al. A novel DNA virus (TTV) associated with elevated transaminase levels in post-transfusion hepatitis of unknown etiology. Biochem Biophys Res Commun 1997;241:92-97.
30. Takahashi K, Iwasa Y, Hijikata M, et al. Identification of a new human DNA virus (TTV-like mini virus, TLMV) intermediately related to TT virus and chicken anemia virus. Arch Virol 2000;145:979-993.
31. Meehan BM, Creelan JL, McNulty MS, et al. Sequence of porcine circovirus DNA: Affinities with plant circoviruses. J Gen Virol 1997;78(Part 1):221-227.
32. Gibbs M, Weiller G. Evidence that a plant virus switched hosts to infect a vertebrate and then recombined with a vertebrate-infecting virus. Proc Natl Acad Sci USA 1999;96:8022-8027.
33. Cheung AK, Lager KM, Kohutyuk OI, et al. Detection of two porcine circovirus type 2 genotypic groups in United States swine herds. Arch Virol 2007;152:1035-1044.
34. Gagnon C, Tremblay D, Tijssen P, et al. PCV2 strain variation: What does it mean? Proc Am Assoc Swine Pract 38:535-540.
35. Cheung AK. Transcriptional analysis of porcine circovirus type 2. Virology 2003;305:168-180.
36. Cheung AK. The essential and nonessential transcription units for viral protein synthesis and DNA replication of porcine circovirus type 2. Virology 2003;313:452-459.
37. Lekcharoensuk P, Morozov I, Paul PS, et al. Epitope map-ping of the major capsid protein of type 2 porcine circovirus (PCV2) by using chimeric PCV1 and PCV2. J Virol 2004;78:8135-8145.
38. Mankertz A, Mankertz J, Wolf K, et al. Identification of a protein essential for replication of porcine circovirus. J Gen Virol 1998;79(Part 2):381-384.
39. Morozov I, Sirinarumitr T, Sorden SD, et al. Detection of a novel strain of porcine circovirus in pigs with postweaning multi-systemic wasting syndrome. J Clin Microbiol 1998;36:2535-2541.
40. Cheung AK. Identification of the essential and non-essential transcription units for protein synthesis, DNA replication and in-fectious virus production of porcine circovirus type 1. Arch Virol 2004;149:975-988.
41. Mankertz A, Hillenbrand B. Replication of porcine circovi-rus type 1 requires two proteins encoded by the viral rep gene. Virology 2001;279:429-438.
42. Liu J, Chen I, Kwang J. Characterization of a previously unidentified viral protein in porcine circovirus type 2-infected cells and its role in virus-induced apoptosis. J Virol 2005;79:8262-8274.
43. Larochelle R, Magar R, D'Allaire S. Genetic characteriza-tion and phylogenetic analysis of porcine circovirus type 2 (PCV2) strains from cases presenting various clinical conditions. Virus Res 2002;90:101-112.
44. Darwich L, Segales J, Mateu E. Pathogenesis of postweaning multisystemic wasting syndrome caused by porcine circovirus 2: An immune riddle. Arch Virol 2004;149:857-874.
45. Misinzo G, Delputte PL, Meerts P, et al. Porcine circovirus 2 uses heparan sulfate and chondroitin sulfate B glycosaminoglycans as receptors for its attachment to host cells. J Virol 2006;80:3487-3494.
46. Chianini F, Majo N, Segales J, et al. Immunohistological study of the immune system cells in paraffin-embedded tissues of conventional pigs. Vet Immunol Immunopathol 2001;82:245-255.
47. Sorden SD. Update on porcine circovirus and postweaning multisystemic wasting syndrome (PMWS). Swine Health Prod 2000; 8:133-136.
48. Vincent IE, Carrasco CP, Herrmann B, et al. Dendritic cells harbor infectious porcine circovirus type 2 in the absence of appar-ent cell modulation or replication of the virus. J Virol 2003;77: 13288-13300.
49. Tischer I, Peters D, Rasch R, et al. Replication of porcine circovirus: Induction by glucosamine and cell cycle dependence. Arch Virol 1987;96:39-57.
50. Mankertz A, Caliskan R, Hattermann K, et al. Molecular biology of porcine circovirus: Analyses of gene expression and viral replication. Vet Microbiol 2004;98:81-88.
51. Tischer I, Buhk HJ. Viral DNA from cells infected with porcine circovirus. Zentralbl Bakteriol Mikrobiol Hyg [A] 1988; 270:280-287.
52. Meerts P, Misinzo G, McNeilly F, et al. Replication kinetics of different porcine circovirus 2 strains in PK-15 cells, fetal card-iomyocytes and macrophages. Arch Virol 2005;150:427-441.
53. Magar R, Larochelle R, Thibault S, et al. Experimental transmission of porcine circovirus type 2 (PCV2) in weaned pigs: A sequential study. J Comp Pathol 2000;123:258-269.
54. Bolin SR, Stoffregen WC, Nayar GP, et al. Postweaning multisystemic wasting syndrome induced after experimental inocu-lation of cesarean-derived, colostrum-deprived piglets with type 2 porcine circovirus. J Vet Diagn Invest 2001;13:185-194.
55. Segales J, Calsamiglia M, Olvera A, et al. Quantification of porcine circovirus type 2 (PCV2) DNA in serum and tonsillar, na-sal, tracheo-bronchial, urinary and faecal swabs of pigs with and without postweaning multisystemic wasting syndrome (PMWS). Vet Microbiol 2005;111:223-229.
56. Maldonado J, Segales J, Martinez-Puig D, et al. Identifica-tion of viral pathogens in aborted fetuses and stillborn piglets from cases of swine reproductive failure in Spain. Vet J 2005;169:454-456.
57. Park JS, Kim J, Ha Y, et al. Birth abnormalities in pregnant sows infected intranasally with porcine circovirus 2. J Comp Pathol 2005;132:139-144.
58. Pensaert MB, Sanchez RE Jr, Ladekjaer-Mikkelsen AS, et al. Viremia and effect of fetal infection with porcine viruses with special reference to porcine circovirus 2 infection. Vet Microbiol 2004;98:175-183.
59. Stevenson GW, Kiupel M, Mittal SK, et al. Tissue distribu-tion and genetic typing of porcine circoviruses in pigs with naturally occurring congenital tremors. J Vet Diagn Invest 2001;13:57-62.
60. Shibata I, Okuda Y, Kitajima K, et al. Shedding of porcine circovirus into colostrum of sows. J Vet Med B Infect Dis Vet Public Health 2006;53:278-280.
61. Opriessnig T, Patterson AR, Meng XJ, et al. Porcine circovirus type 2 in muscle and bone marrow is infectious and transmissible to naive pigs by oral consumption. Vet Microbiol 2009;133:54-64.
62. McIntosh KA, Harding JC, Parker S, et al. Nested polymerase chain reaction detection and duration of porcine circovirus type 2 in semen with sperm morphological analysis from naturally infected boars. J Vet Diagn Invest 2006;18:380-384.
63. Kim J, Han DU, Choi C, et al. Differentiation of porcine circovirus (PCV)-1 and PCV-2 in boar semen using a multiplex nested polymerase chain reaction. J Virol Methods 2001;98:25-31.
64. Larochelle R, Bielanski A, Muller P, et al. PCR detection and evidence of shedding of porcine circovirus type 2 in boar semen. J Clin Microbiol 2000;38:4629-4632.
65. Kim J, Han DU, Choi C, et al. Simultaneous detection and differentiation between porcine circovirus and porcine parvovirus in boar semen by multiplex seminested polymerase chain reaction. J Vet Med Sci 2003;65:741-744.
66. Madson DM, Ramamoorthy S, Kuster C, et al. Characterization of shedding patterns of porcine circovirus types 2a and 2b in experimentally inoculated mature boars. J Vet Diagn Invest 2008;20:725-734.
67. Madson DM, Ramamoorthy S, Kuster C, et al. Infectivity of porcine circovirus type 2 DNA in semen from experimentally-infected boars. Vet Res 2009;40: article 10.
68. Allan GM, Kennedy S, McNeilly F, et al. Experimental reproduction of severe wasting disease by coinfection of pigs with porcine circovirus and porcine parvovirus. J Comp Pathol 1999;121: 1-11.
69. Balasch M, Segales J, Rosell C, et al. Experimental inoculation of conventional pigs with tissue homogenates from pigs with postweaning multisystemic wasting syndrome. J Comp Pathol 1999;121:139-148.
70. Harms PA, Sorden SD, Halbur PG, et al. Experimental re-production of severe disease in CD/CD pigs concurrently infected with type 2 porcine circovirus and porcine reproductive and respi-ratory syndrome virus. Vet Pathol 2001;38:528-539.
71. Rosell C, Segales J, Plana-Duran J, et al. Pathological, immunohistochemical, and insitu hybridization studies of natural cases of postweaning multisystemic wasting syndrome (PMWS) in pigs. J Comp Pathol 1999;120:59-78.
72. Yu S, Vincent AL, Opriessnig T, et al. In vitro studies on the use of quantitative real-time RT-PCR assay to detect PCV2 replication in peripheral blood mononuclear cells. Presented at the 18th Congress of the International Pig Veterinary Society, Hamburg, Germany, 2004.
73. Choi C, Chae C. Insitu hybridization for the detection of porcine circovirus in pigs with postweaning multisystemic wasting syndrome. J Comp Pathol 1999;121:265-270.
74. Yu S, Opriessnig T, Kitikoon P, et al. Porcine circovirus type 2 (PCV2) distribution and replication in tissues and immune cells in early infected pigs. Vet Immunol Immunopathol 2007;115:261-272.
75. Krakowka S, Ellis JA, Meehan B, et al. Viral wasting syndrome of swine: Experimental reproduction of postweaning multisystemic wasting syndrome in gnotobiotic swine by coinfec-tion with porcine circovirus 2 and porcine parvovirus. Vet Pathol 2000;37:254-263.
76. Pogranichnyy RM, Yoon KJ, Harms PA, et al. Characterization of immune response of young pigs to porcine circovirus type 2 infection. Viral Immunol 2000;13:143-153.
77. Rovira A, Balasch M, Segales J, et al. Experimental inoculation of conventional pigs with porcine reproductive and respiratory syndrome virus and porcine circovirus 2. J Virol 2002;76: 3232-3239.
78. McKeown NE, Opriessnig T, Thomas P, et al. Effects of porcine circovirus type 2 (PCV2) maternal antibodies on experimental infection of piglets with PCV2. Clin Diagn Lab Immunol 2005;12:1347-1351.
79. Ostanello F, Caprioli A, Di Francesco A, et al. Experimental infection of 3-week-old conventional colostrum-fed pigs with porcine circovirus type 2 and porcine parvovirus. Vet Microbiol 2005;108:179-186.
80. Allan G, McNeilly F, McNair I. Passive transfer of maternal antibodies to PCV2 protects against development of post-weaning multisystemic wasting syndrome (PMWS): Experimental infections and a field study. Pig J 2002;50:59-67.
81. McIntosh KA, Harding JC, Ellis JA, et al. Detection of Porcine circovirus type 2 viremia and seroconversion in naturally infected pigs in a farrow-to-finish barn. Can J Vet Res 2006;70: 58-61.
82. Larochelle R, Magar R, D'Allaire S. Comparative serologic and virologic study of commercial swine herds with and without postweaning multisystemic wasting syndrome. Can J Vet Res 2003; 67:114-120.
83. Rodriguez-Arrioja GM, Segales J, Calsamiglia M, et al. Dynamics of porcine circovirus type 2 infection in a herd of pigs with postweaning multisystemic wasting syndrome. Am J Vet Res 2002; 63:354-357.
84. Sibila M, Calsamiglia M, Segales J, et al. Use of a polymer-ase chain reaction assay and an ELISA to monitor porcine circovirus type 2 infection in pigs from farms with and without postweaning multisystemic wasting syndrome. Am J Vet Res 2004; 65:88-92.
85. Krakowka S, Ellis JA, McNeilly F, et al. Activation of the immune system is the pivotal event in the production of wasting disease in pigs infected with porcine circovirus-2 (PCV-2). Vet Pa-thol 2001;38:31-42.
86. Meerts P, Misinzo G, Lefebvre D, et al. Correlation between the presence of neutralizing antibodies against porcine circovirus 2 (PCV2) and protection against replication of the virus and development of PCV2-associated disease. BMC Vet Res 2006;2: article 6.
87. Darwich L, Pie S, Rovira A, et al. Cytokine mRNA expression profiles in lymphoid tissues of pigs naturally affected by postweaning multisystemic wasting syndrome. J Gen Virol 2003;84: 2117-2125.
88. Vincent IE, Balmelli C, Meehan B, et al. Silencing of natural interferon producing cell activation by porcine circovirus type 2 DNA. Immunology 2007;120:47-56.
89. Tischer I, Bode L, Apodaca J, et al. Presence of antibodies reacting with porcine circovirus in sera of humans, mice, and cattle. Arch Virol 1995;140:1427-1439.
90. Calsamiglia M, Sibila M, Segales J, et al. Detection of porcine circovirus type 2 in different routes of excretion: Possible transmission routes and correlation with presence of postweaning multisystemic syndrome characteristic lesions. Proceedings of the 17th International Pig Veterinary Society Congress, Ames, IA, 2002,1, p. 28.
91. Liu Q, Wang L, Willison P, et al. Quantitative, competitive PCR analysis of porcine circovirus DNA in serum from pigs with postweaning multisystemic wasting syndrome (PMWS). J Clin Microbiol 2000;38:3474-3477.
92. Sibila M, Calsamiglia M, Seagales J, et al. Detection of porcine circovirus type 2 genome in nasal swabs and serum samples from naturally infected pigs using polymerase chain reaction. Presented at the International Conference on ssDNA Viruses of Plants, Birds, Pigs, and Primates, St Malo, France, European Society of Veterinary Virology, 2001.
93. Rose N, Larour, Le Diguerher G. Serological profile of porcine circovirus type 2 (PCV2) in PMWS affected and non-affected farms. Presented at the International Conference on ssDNA Viruses of Plants, Birds, Pigs, and Primates, St Malo, France, 2001.
94. Grierson SS, King DP, Wellenberg GJ, et al. Genome sequence analysis of 10 Dutch porcine circovirus type 2 (PCV-2) isolates from a PMWS case-control study. Res Vet Sci 2004;77:265-268.
95. Allan G, McNeilly F, Meehan B, et al. Reproduction of postweaning multisystemic wasting syndrome in pigs experimen-tally inoculated with a Swedish porcine circovirus 2 isolate. J Vet Diagn Invest 2003;15:553-560.
96. Hasslung F, Wallgren P, Ladekjaer-Hansen AS, et al. Experimental reproduction of postweaning multisystemic wasting syndrome (PMWS) in pigs in Sweden and Denmark with a Swedish isolate of porcine circovirus type 2. Vet Microbiol 2005; 106:49-60.
97. Fenaux M, Opriessnig T, Halbur PG, et al. Two amino acid mutations in the capsid protein of type 2 porcine circovirus (PCV2) enhanced PCV2 replication in vitro and attenuated the virus in vivo. J Virol 2004;78:13440-13446.
98. DeLay J, McEwen B, Carman S, et al. Porcine circovirus type 2-associated disease is increasing. AHL Newsletter, 2005, 9, p. 22.
99. Lopez-Soria S, Segales J, Nofrarias M, et al. Genetic influence on the expression of PCV disease. Vet Rec 2004;155:504.
100. Opriessnig T, Fenaux M, Thomas P, et al. Evidence of breed-dependent differences in susceptibility to porcine circovirus type-2-associated disease and lesions. Vet Pathol 2006;43:281-293.
101. Meerts P, Van Gucht S, Cox E, et al. Correlation between type of adaptive immune response against porcine circovirus type 2 and level of virus replication. Viral Immunol 2005;18:333-341.
102. Pogranichniy RM, Yoon KJ, Harms PA, et al. Case-control study on the association of porcine circovirus type 2 and other swine viral pathogens with postweaning multisystemic wasting syndrome. J Vet Diagn Invest 2002;14:449-456.
103. Allan GM, McNeilly F, Meehan BM, et al. A sequential study of experimental infection of pigs with porcine circovirus and porcine parvovirus: Immunostaining of cryostat sections and virus isolation. J Vet Med B Infect Dis Vet Public Health 2000;47:81-94.
104. Kennedy S, Moffett D, McNeilly F, et al. Reproduction of lesions of postweaning multisystemic wasting syndrome by infection of conventional pigs with porcine circovirus type 2 alone or in com-bination with porcine parvovirus. J Comp Pathol 2000;122:9-24.
105. Opriessnig T, Fenaux M, Yu S, et al. Effect of porcine parvovirus vaccination on the development of PMWS in segregated early weaned pigs coinfected with type 2 porcine circovirus and porcine parvovirus. Vet Microbiol 2004;98:209-220.
106. Opriessnig T, Thacker EL, Yu S, et al. Experimental reproduction of postweaning multisystemic wasting syndrome in pigs by dual infection with Mycoplasma hyopneumoniae and porcine circo-virus type 2. Vet Pathol 2004;41:624-640.
107. Ellis JA, Allan G, Krakowka S. Effect of coinfection with genogroup 1 porcine torque teno virus on porcine circovirus type 2-associated postweaning multisystemic wasting syndrome in gnot-obiotic pigs. Am J Vet Res 2008;69:1608-1614.
108. McKeown NE, Fenaux M, Halbur PG, et al. Molecular characterization of porcine TT virus, an orphan virus, in pigs from six different countries. Vet Microbiol 2004;104:113-117.
109. Pallares FJ, Halbur PG, Opriessnig T, et al. Porcine circovirus type 2 (PCV-2) coinfections in US field cases of postweaning multisystemic wasting syndrome (PMWS). J Vet Diagn Invest 2002; 14:515-519.
110. Allan G, Mcneilly F, McNair I. Neonatal vaccination for Mycoplasma hyopneumoniae and post-weaning multisystemic wasting syndrome: A field trial. Pig J 2001;48:34-41.
111. Kyriakis SC, Saoulidis K, Lekkas S, et al. The effects of immuno-modulation on the clinical and pathological expression of postweaning multisystemic wasting syndrome. J Comp Pathol 2002; 126:38-46.
112. Opriessnig T, Yu S, Gallup JM, et al. Effect of vaccination with selective bacterins on conventional pigs infected with type 2 porcine circovirus. Vet Pathol 2003;40:521-529.
113. Hoogland MJ, Opriessnig T, Halbur PG. Effects of adjuv-ants on porcine circovirus type 2-associated lesions. J Swine Health Prod 2006;14:133-139.
114. Krakowka S, Ellis JA, McNeilly F, et al. Immunologic fea-tures of porcine circovirus type 2 infection. Viral Immunol 2002;15: 567-582.
115. Kawashima K, Tsunemitsu H, Horino R, et al. Effects of dexamethasone on the pathogenesis of porcine circovirus type 2 in-fection in piglets. J Comp Pathol 2003;129:294-302.
116. Fenaux M, Opriessnig T, Halbur PG, et al. A chimeric porcine circovirus (PCV) with the immunogenic capsid gene of the pathogenic PCV type 2 (PCV2) cloned into the genomic backbone of the nonpathogenic PCV1 induces protective immunity against PCV2 infection in pigs. J Virol 2004;78:6297-6303.
117. Fenaux M, Opriessnig T, Halbur PG, et al. Immunogenicity and pathogenicity of chimeric infectious DNA clones of pathogenic porcine circovirus type 2 (PCV2) and nonpathogenic PCV1 in wean-ling pigs. J Virol 2003;77:11232-11243.
118. Allan G, Krakowka S, Ellis J. PCV2: Ticking time bomb? Pig Prog 2002;18:14-15.
119. American Association of Swine Veterinarians (AASV). Porcine circovirus associated disease (PCVAD) case definition, 2006. Available at: http://www.aasp.org/aasv/position-PCVAD.htm. Accessed November 4, 2008.
120. Schulze C, Neumann G, Grutze I, et al. Case report: Porcine circovirus type 2 infection in an European wild boar (Sus scrofa) in the state of Brandenburg, Germany. Dtsch Tierarztl Wochenschr 2003;110:426-428.
121. Segales J, Domingo M. Postweaning multisystemic wasting syndrome (PMWS) in pigs. A review. Vet Q 2002;24:109-124.
122. Clark E., Postweaning multisystemic wasting syndrome. Proceedings of American Association of Swine Practitioners Que-bec City, Canada, 1997, 499-501.
123. Horlen KP, Dritz SS, Nietfeld JC, et al. A field evaluation of mortality rate and growth performance in pigs vaccinated against porcine circovirus type 2. J Am Vet Med Assoc 2008;232: 906-912.
124. Opriessnig T, Janke BH, Halbur PG. Cardiovascular lesions in pigs naturally or experimentally infected with porcine circovirus type 2. J Comp Pathol 2006;134:105-110.
125. Opriessnig T, McKeown NE, Harmon KL, et al. Porcine circovirus type 2 infection decreases the efficacy of a modified live porcine reproductive and respiratory syndrome virus vaccine. Clin Vaccine Immunol 2006;13:923-929.
126. Kim J, Chae C. Necrotising lymphadenitis associated with porcine circovirus type 2 in pigs. Vet Rec 2005;156:177-178.
127. Jensen T, Vigre H, Svensmark B, et al. Distinction between porcine circovirus type 2 enteritis and porcine proliferative enter-opathy caused by Lawsonia intracellularis. J Comp Pathol 2006;135: 176-182.
128. Harms PA, Halbur PG, Sorden SD. Three cases of porcine respiratory disease complex associated with porcine circovirus type 2 infection. J Swine Health Prod 2002;10:27-30.
129. Kim J, Chung HK, Chae C. Association of porcine circovi-rus 2 with porcine respiratory disease complex. Vet J 2003;166:251-256.
130. West KH, Bystrom JM, Wojnarowicz C, et al. Myocarditis and abortion associated with intrauterine infection of sows with porcine circovirus 2. J Vet Diagn Invest 1999;11:530-532.
131. Mikami O, Nakajima H, Kawashima K, et al. Nonsuppu-rative myocarditis caused by porcine circovirus type 2 in a weak-born piglet. J Vet Med Sci 2005;67:735-738.
132. Sanchez RE Jr, Nauwynck HJ, McNeilly F, et al. Porcine circovirus 2 infection in swine foetuses inoculated at different stages of gestation. Vet Microbiol 2001;83:169-176.
133. Johnson CS, Joo HS, Direksin K, et al. Experimental in utero inoculation of late-term swine fetuses with porcine circovirus type 2. J Vet Diagn Invest 2002;14:507-512.
134. Smith WJ, Thomson JR, Done S. Dermatitis/nephropathy syndrome of pigs. Vet Rec 1993;132:47.
135. Rosell C, Segales J, Ramos-Vara JA, et al. Identification of porcine circovirus in tissues of pigs with porcine dermatitis and ne-phropathy syndrome. Vet Rec 2000;146:40-43.
136. Choi C, Chae C. Colocalization of porcine reproductive and respiratory syndrome virus and porcine circovirus 2 in porcine dermatitis and nephrology syndrome by double-labeling technique. Vet Pathol 2001;38:436-441.
137. Thibault S, Drolet R, Germain MC, et al. Cutaneous and systemic necrotizing vasculitis in swine. Vet Pathol 1998;35:108-116.
138. Lainson FA, Aitchison KD, Donachie W, et al. Typing of Pasteurella multocida isolated from pigs with and without porcine dermatitis and nephropathy syndrome. J Clin Microbiol 2002;40: 588-593.
139. Thomson JR, Higgins RJ, Smith WJ, et al. Porcine dermatitis and nephropathy syndrome. Clinical and pathological features of cases in the United Kingdom (1993-1998). J Vet Med A Physiol Pathol Clin Med 2002;49:430-437.
140. Krakowka S, Hartunian C, Hamberg A, et al. Evaluation of induction of porcine dermatitis and nephropathy syndrome in gnotobiotic pigs with negative results for porcine circovirus type 2. Am J Vet Res 2008;69:1615-1622.
141. Choi J, Stevenson GW, Kiupel M, et al. Sequence analysis of old and new strains of porcine circovirus associated with congen-ital tremors in pigs and their comparison with strains involved with postweaning multisystemic wasting syndrome. Can J Vet Res 2002;66:217-224.
142. Correa AM, Zlotowski P, de Barcellos DE, et al. Brain lesions in pigs affected with postweaning multisystemic wasting syndrome. J Vet Diagn Invest 2007;19:109-112.
143. Seeliger FA, Brugmann ML, Kruger L, et al. Porcine circovirus type 2-associated cerebellar vasculitis in postweaning multisystemic wasting syndrome (PMWS)-affected pigs. Vet Pathol 2007;44:621-634.
144. Ellis J, Hassard L, Clark E, et al. Isolation of circovirus from lesions of pigs with postweaning multisystemic wasting syndrome. Can Vet J 1998;39:44-51.
145. Blanchard P, Mahe D, Cariolet R, et al. An ORF2 protein-based ELISA for porcine circovirus type 2 antibodies in post-weaning multisystemic wasting syndrome. Vet Microbiol 2003;94:183-194.
146. Liu C, Ihara T, Nunoya T, et al. Development of an ELISA based on the baculovirus-expressed capsid protein of porcine circo-virus type 2 as antigen. J Vet Med Sci 2004;66:237-242.
147. Nawagitgul P, Harms PA, Morozov I, et al. Modified indi-rect porcine circovirus (PCV) type 2-based and recombinant capsid protein (ORF2)-based enzyme-linked immunosorbent assays for detection of antibodies to PCV. Clin Diagn Lab Immunol 2002; 9:33-40.
148. Hamel AL, Lin LL, Sachvie C, et al. PCR detection and characterization of type-2 porcine circovirus. Can J Vet Res 2000; 64:44-52.
149. Shibata I, Okuda Y, Yazawa S, et al. PCR detection of porcine circovirus type 2 DNA in whole blood, serum, oropharyn-geal swab, nasal swab, and feces from experimentally infected pigs and field cases. J Vet Med Sci 2003;65:405-408.
150. Segales J. Proc Am Assoc Swine Veterinarians: PCV2/ PMWS Seminar 2006;12:1-7.
151. Rose N, Blanchard P, Cariolet R, et al. Vaccination of porcine circovirus type 2 (PCV2)-infected sows against porcine par-vovirus (PPV) and Erysipelas: Effect on post-weaning multisystemic wasting syndrome (PMWS) and on PCV2 genome load in the off-spring. J Comp Pathol 2007;136:133-144.
152. Opriessnig T, Thacker E, Halbur P. Chlortetracycline is effective in reducing lesions in pigs infected with Mycoplasma hyopneumoniae and porcine circovirus type 2. Proc. 19th Int. Pig Vet. Soc. Congr. 2006;2:203.
153. Royer R, Nawagitgul P, Halbur PG, et al. Susceptibility of porcine circovirus type 2 to commercial and laboratory disinfectants. J Swine Health Prod 2001;9:281-284.
154. Ramamoorthy S, Meng XJ. Porcine circovirus: A miniscule yet mammoth paradox. Anim Health Res Rev 2008;9:1-20.
155. Rose N, Larour G, Le Diguerher G, et al. Risk factors for porcine post-weaning multisystemic wasting syndrome (PMWS) in 149 French farrow-to-finish herds. Prev Vet Med 2003;61:209-225.
156. Lopez-Soria S, Segales J, Rose N, et al. An exploratory study on risk factors for postweaning multisystemic wasting syn-drome (PMWS) in Spain. Prev Vet Med 2005;69:97-107.
157. Dewey CE, Johnston WT, Gould L, et al. Postweaning mortality in Manitoba swine. Can J Vet Res 2006;70:161-167.
158. Halbur PG. Update on PRRSV in grow-finish. Proc. Swine Dis. Conf. Swine Pract. 2000;8:113-123.
159. Halbur PG. PMWS: Improved models and recent findings of clinical significance. Proc. Swine Dis. Conf. Swine Pract. 2001;9: 162-166.
160. Charreyre C, Beseme S, Brun A, et al. Vaccination strategies for the control of circoviral diseases in pigs. Proc Intern Conf Anim. Circoviruses Assoc. Dis. 2005;26-30.
161. Desrosier R, Clark E, Tremblay D. Pulmonary results with Ingelvacs Circo FLEXa to protect multiple ages of Quebec pigs against PCVAD. Proc Am Assoc Swine Pract. 2007;38:143-145.
162. Von Richthofen I, Woolfenden N, Lischewski A, et al. Field efficacy of a PCV2 vaccine in three week old piglets in the United Kingdom. Fifth Symposium on Emerging and Re-Emerging Pig Diseases Krakow, Poland, 2007, p. 122.
163. Grau AF, Jorgensen J, Thacker B, et al. Field performance of a conditionally licensed vaccine: The US experience. Proc Am Assoc Swine Vet.: PCV2/PMWS Sem. 2007;38:159-161.
164. Fenaux M, Halbur PG, Haqshenas G, et al. Cloned genomic DNA of type 2 porcine circovirus is infectious when injected directly into the liver and lymph nodes of pigs: Characterization of clinical disease, virus distribution, and pathologic lesions. J Virol 2002;76:541-551.
165. Opriessnig T, Patterson AR, Elsener J, et al. Influence of maternal antibodies on efficacy of porcine circovirus type 2 (PCV2) vaccination to protect pigs from experimental infection with PCV2. Clin Vaccine Immunol 2008;15:397-401.
166. Gillespie J, Juhan NM, DiCristina J, et al. A genetically engineered chimeric vaccine against porcine circovirus type 2 (PCV2) is genetically stable in vitro and in vivo. Vaccine 2008;26: 4231-4236.