Cetacean morbillivirus: Current knowledge and future directions

Viruses

Volumn 6, Issue 12, 2014, Pages 5145-5181

  Van Bressem, Marie Françoise ^a   Duignan, Pádraig J ^b   Banyard, Ashley ^c   Barbieri, Michelle ^d   Colegrove, Kathleen M ^e   de Guise, Sylvain ^f   di Guardo, Giovanni ^g   Dobson, Andrew ^h   Domingo, Mariano ⁱ   Fauquier, Deborah ^j   Fernandez, Antonio ^k   Goldstein, Tracey ^l   Grenfell, Bryan ^h,m   Groch, Kátia R ^n,o   Gulland, Frances ^d,p   Jensen, Brenda A ^q   Jepson, Paul D ^r   Hall, Ailsa ^s   Kuiken, Thijs ^t   Mazzariol, Sandro ^u   Morris, Sinead E ^h   Nielsen, Ole ^v   Raga, Juan A ^w   Rowles, Teresa K ^j   Saliki, Jeremy ^x   Sierra, Eva ^k   Stephens, Nahiid ^y   Stone, Brett ^z   Tomo, Ikuko ^aa   Wang, Jianning ^ab   Waltzek, Thomas ^ac   Wellehan, James F X ^ac   more..

^a Cetacean Conservation Medicine Group (CMED)   (Peru)

^b UNIVERSITY OF CALGARY   (Canada)

^c VETERINARY LABORATORIES AGENCY   (United Kingdom)

^d The Marine Mammal Centre   (United States)

^e UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^f UNIVERSITY OF CONNECTICUT   (United States)

^g UNIVERSITY OF TERAMO   (Italy)

^h PRINCETON UNIVERSITY   (United States)

ⁱ UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^j NATIONAL MARINE FISHERIES SERVICE   (United States)

^k UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

^l UNIVERSITY OF CALIFORNIA   (United States)

^m NATIONAL INSTITUTES OF HEALTH   (United States)

ⁿ UNIVERSITY OF SÃO PAULO   (Brazil)

^o INSTITUTO BALEIA JUBARTE   (Brazil)

^p Marine Mammal Commission   (United States)

^q HAWAII PACIFIC UNIVERSITY   (United States)

^r INSTITUTE OF ZOOLOGY   (United Kingdom)

^s UNIVERSITY OF ST ANDREWS   (United Kingdom)

^t ERASMUS MEDICAL CENTER   (Netherlands)

^u UNIVERSITY OF PADOVA   (Italy)

^v FISHERIES AND OCEANS CANADA   (Canada)

^w UNIVERSITY OF VALENCIA   (Spain)

^x University of eorgia   (United States)

^y MURDOCH UNIVERSITY   (Australia)

^z QML Vetnostics   (Australia)

^aa SOUTH AUSTRALIAN MUSEUM   (Australia)

^ab CSIRO   (Australia)

^ac University of Florida College of Veterinary Medicine   (United States)

more..

Author keywords

Cetacean morbillivirus; Diagnosis; Endemic infections; Epidemics; Mass stranding; Pathogenesis; Phylogeny; SLAM

Indexed keywords

CD147 ANTIGEN; CD150 ANTIGEN; CD4 ANTIGEN; GLYCOPROTEIN; GLYCOPROTEIN H; GROWTH FACTOR; HEMAGGLUTININ; LYMPHOCYTE ANTIGEN; NECTIN 4; RNA POLYMERASE; UNCLASSIFIED DRUG; VIRUS RECEPTOR; VIRUS RNA;

BRONCHOPNEUMONIA; CETACEAN MORBILLIVIRUS; DOLPHIN; ENCEPHALITIS; ENZYME LINKED IMMUNOSORBENT ASSAY; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOCYTE DEPLETION; MEASLES VIRUS; MORBILLIVIRUS INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PILOT WHALE; PORPOISE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SERODIAGNOSIS; SOTALIA GUIANENSIS; STENELLA; TURSIOPS ADUNCUS; TURSIOPS TRUNCATUS; VIRUS STRAIN; VIRUS TRANSMISSION; ANIMAL; CETACEA; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; MORBILLIVIRUS; PHYSIOLOGY; TRANSMISSION; VETERINARY; VIROLOGY;

CETACEA; CETACEAN MORBILLIVIRUS; DELPHINIDAE; MAMMALIA; MORBILLIVIRUS; SOTALIA GUIANENSIS; TURSIOPS; TURSIOPS ADUNCUS;

ANIMALS; CETACEA; MORBILLIVIRUS; MORBILLIVIRUS INFECTIONS; PHYLOGENY;

EID: 84919820072     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v6125145     Document Type: Review

References (148)

1. McCullough, S.J.; McNeilly, F.; Allan, G.M.; Kennedy, S.; Smyth, J.A.; Cosby, S.L.; McQuaid, S.; Rima, B.K. Isolation and characterisation of a porpoise morbillivirus. Arch. Virol.1991, 118, 247-252.
2. Domingo, M.; Ferrer, L.; Pumarola, M.; Marco, A.; Plana, J.; Kennedy, S.; McAliskey, M.; Rima, B.K. Morbillivirus in dolphins. Nature1990,348, 21.
3. Van Bressem, M.-F.; Visser, I.K.G.; van de Bildt, M.W.; Teppema, J.S.; Raga, J.A.; Osterhaus, A.D.M.E. Morbillivirus infection in Mediterranean striped dolphins (Stenella coeruleoalba). Vet Rec. 1991, 129,471-472.
4. Taubenberger, J.K.; Tsai, M.M.; Atkin, T.J.; Fanning, T.G.; Krafft, A.E.; Moeller, R.B.; Kodsi, S.E.; Mense, M.G.; Lipscomb, T.P. Molecular genetic evidence of a novel morbillivirus in a long-finned pilot whale (Globicephalamelas). Emerg. Infect. Dis. 2000, 6, 42-45.
5. West, K.L.; Sanchez, S.; Rotstein, D.; Robertson, K.M.; Dennison, S.; Levine, G.; Davis, N.; Schofield, D.; Potter, C.W.; Jensen, B. A Longman’s beaked whale (Indopacetus pacificus) strands in Maui, Hawaii, with first case of morbillivirus in the central Pacific. Mar. Mamm. Sci.2013, 29, 767-776.
6. Groch, K.R.; Colosio, A.C.; Marcondes, M.C.; Zucca, D.; Díaz-Delgado, J.; Niemeyer, C.; Marigo, J., Brandão, P.E., Fernández, A.; Luiz Catão-Dias, J. Novel cetacean morbillivirus in Guiana dolphin, Brazil. Emerg. Infect. Dis. 2014, 20, 511-513.
7. Stephens N.; Duignan, P.J.; Wang, J.; Bingham, J.; Finn, H.; Bejder, L.; Patterson, A.P.; Holyoake, C. Cetacean morbillivirus in coastal Indo-Pacific bottlenose dolphins, Western Australia. Emerg. Infect. Dis. 2014, 20, 666-670.
8. Barrett, T. Morbillivirus infections, with special emphasis on morbilliviruses of carnivores. Vet. Microbiol.1999, 69, 3-13.
9. Ohishi, K.; Suzuki, R.; Maruyama, T. Host-Virus Specificity of the Morbillivirus Receptor, SLAM, in Marine Mammals: Risk Assessment of infection based on three-dimensional models. InNew Approaches to the Study of Marine Mammals; Romero, A., Keith, E.O., Eds.; InTech: Rijeka, Croatia, 2012; pp. 183-204.
10. Hall, A.J. Morbilliviruses in marine mammals. Trends Microbiol. 1995, 3, 4-9.
11. Woo, P.C.; Lau, S.K.; Wong, B.H.; Fan, R.Y.; Wong, A.Y.; Zhang, A.J.; Wu, Y.; Choi, G.K.; Li, K.S.; Hui, J., et al.Feline morbillivirus, a previously undescribed paramyxovirus associated with tubulointerstitial nephritis in domestic cats. Proc. Natl. Acad. Sci. USA 2012, 109, 5435-5440.
12. Delpeut, S.; Noyce, R.S.; Richardson, C.D. The tumor-associated marker, PVRL4 (nectin-4), is the epithelial receptor for morbilliviruses. Viruses2014, 6, 2268-2286.
13. Shimizu, Y.; Ohishi, K.; Suzuki, R.; Tajima, Y.; Yamada, T.; Kakizoe, Y.; Bando, T.; Fujise, Y.; Taru, H.; Murayama, T., et al. Amino acid sequence variations of signaling lymphocyte activation molecule and mortality caused by morbillivirus infection in cetaceans. Microbiol. Immunol.2013, 57, 624-632.
14. Barrett, T.; Blixenkrone-Møller, M.; diGuardo, G.; Domingo, M.; Duignan, P.; Hall, A.; Mamaev, L.; Osterhaus, A.D.M.E. Morbilliviruses in aquatic mammals: Report on round table discussion. Vet. Microbiol. 1995, 44, 261-265.
15. Osterhaus, A.D.M.E.; de Swart, R.L.; Vos, H.W.; Ross, P.S.; Kenter, M.J.H.; Barrett, T. Morbillivirus infections of aquatic mammals: Newly identified members of the genus. Vet. Microb. 1995, 44, 219-227.
16. Barrett, T.; Visser, I.K.G.; Mamaev, L.; Goatley, L.; van Bressem, M.-F.; Osterhaus, A.D.M.E. Dolphin and porpoise morbilliviruses are genetically distinct from phocine distemper virus. Virology 1993, 193, 1010-1012.
17. Blixenkrone-Möller, M.; Bolt, G.; Gottschalk, E.; Kenter, M. Comparative analysis of the gene encoding the nucleocapsid protein of dolphin morbillivirus reveals its distant evolutionary relationship to measles virus and ruminant morbilliviruses. J. Gen. Virol. 1994, 75, 2829-2834.
18. Bolt, G.; Blixenkrone-Möller, M.; Gottschalk, E.; Wishaupt, R.G.A.; Welsh, M.J.; Earle, P.J.A.; Rima, B.K. Nucleotide and deduced amino acid sequences of the matrix (M) and fusion (F) protein genes of cetacean morbilliviruses isolated isolated from a porpoise and a dolphin. Virus Res. 1994,34, 291-304.
19. Rima, B.K.; Collin, A.M.; Earle, J.A. Completion of the sequence of a cetacean morbillivirus and comparative analysis of the complete genome sequences of four morbilliviruses. Virus Genes. 2005, 30, 113-119.
20. Banyard, A.C.; Grant, R.J.; Romero, C.H.; Barrett, T. Sequence of the nucleocapsid gene and genome and antigenome promoters for an isolate of porpoise morbillivirus. Virus Res. 2008, 132, 213-219.
21. Van Bressem, M.-F.; Visser, I.K.G.; de Swart, R.L.; Örvell, C.; Stanzani, L.; Androukaki, E.; Siakavara, K.; Osterhaus, A.D.M.E. Dolphin morbillivirus in different parts of the Mediterranean Sea. Arch. Virol. 1993, 129, 235-242.
22. Visser, I.K.G.; van Bressem, M.-F.; de Swart, R.L.; van de Bildt, M.W.G.; Vos, H.W.; van der Heijden, R.W.J.; Saliki, J.T.; Örvell, C.; Kitching, P.; Kuiken, T., et al. Characterization of morbilliviruses isolated from dolphins and porpoises in Europe. J. Gen. Virol. 1993, 74, 631-641.
23. Duignan, P.J.; House, C.; Geraci, J.R.; Early, G.; Copland, H.G.; Walsh, M.T.; Bossart, G.D.; Cray, C.; Sadove, S.; St Aubin, D.J., et al. Morbillivirus infection in two species of pilot whales (Globicephala sp.) from the western Atlantic. Mar. Mamm. Sci.1995, 11, 150-162.
24. Duignan, P.J.; House, C.; Geraci, J.R.; Duffy, N.; Rima, B.K.; Walsh, M.T.; Early, G.; St Aubin, D.J.; Sadove, S.; Koopman, H., et al. Morbillivirus infection in cetaceans of the western Atlantic. Vet. Microbiol.1995, 44, 241-249.
25. Duignan, P.J.; House, C.; Ode11, D.K.; Wells, R.S.; Hansen, W.; Walsh, M.T.; St Aubin, D.J.; Rima, B.K.; Geraci J.R. Morbillivirus in bottlenose dolphins: Evidence for recurrent epizootics in the western Atlantic and Gulf of Mexico. Mar. Mamm. Sci. 1996, 12, 499-515.
26. Rowles, T.R.; Schwacke, L.S.; Wells, R.S.; Saliki, J.T.; Hansen, L.; Hohn, A.; Townsend, F.; Sayre, R.A.; Hall, A.J. Evidence of susceptibility to morbillivirus infection in cetaceans from the United States. Mar. Mamm. Sci. 2011, 27,1-19.
27. Banyard, A.C.; Tiwari, A.; Barrett, T. Morbillivirus infection in pilot whales: Strict protein requirement drives genetic conservation. Arch. Virol.2011,156, 1853-1839.
28. Van de Bildt, M.W.; Kuiken, T.; Osterhaus, A.D.M.E. Cetacean morbilliviruses are phylogeneticallydivergent. Arch. Virol.2005, 150, 577-583
29. Muhlebach, M.D.; Mateo, M.; Sinn, P.L.; Prufer, S.; Uhlig, K.M.; Leonard, V.H.; Navaratnarajah, C.K.; Frenzke, M.; Wong, X.X.; Sawatsky, B., et al. Adherens junction protein nectin-4 is the epithelial receptor for measles virus. Nature 2011, 480, 530-533.
30. Noyce, R.S.; Bondre, D.G.; Ha, M.N.; Lin, L.T.; Sisson, G.; Tsao, M.S.; Richardson, C.D. Tumor cell marker PVRL4 (nectin 4) is an epithelial cell receptor for measles virus. PLoS Pathog. 2011, 7, e1002240.
31. Watanabe, A.; Yoneda, M.; Ikeda, F.; Terao-Muto, Y.; Sato, H.; Kai, C. CD147/EMMPRIN acts as a functional entry receptor for measles virus on epithelial cells. J. Virol.2010, 84, 4183-4193
32. Baron, M.D. Wildtype rinderpest virus uses SLAM (CD150) as its receptor. J. Gen. Virol.2005,86, 1753-1787.
33. Adombi, C.M.; Lelenta, M.; Lamien, C.E.; Shamaki, D.; Koffi, Y.M.; Traoré, A.; Silber, R.; Couacy-Hymann, E.; Bodjo, S.C.; Djaman, J.A., et al. Monkey CV1 cell line expressing the sheep-goat SLAM protein: A highly sensitive cell line for the isolation of peste des petits ruminants virus from pathological specimens. J. Virol. Methods 2011,173, 306-313.
34. Ono, N.; Tatsuo, H.; Tanaka, K.; Minagawa, H.; Yanagi, Y. V domain of human SLAM (CDw150) is essential for its function as a measles virus receptor. J. Virol. 2001, 75, 1594-1600.
35. Bieringer, M.; Han, J.W.; Kendl, S.; Khosravi, M.; Plattet, P.; Schneider-Schaulies, J. Experimental adaptation of wild-type canine distemper virus (CDV) to the human entry receptor CD150. PLoS One2013, 8, e57488.
36. Kemper, M.C.; Woolford, L.; Tomo, I.; Dickason, C.; Bastianello, S.; Gibbs, S.; Kelly, D.; Wang, J.; Bingham, J. Abnormally high dolphin mortalities linked to Morbillivirus in South Australia. In Proceedings of the 20 Biennial Conference on the Biology of Marine Mammals, Dunedin, New Zealand, 9-13 December2013.
37. Van Bressem, M.-F.; Raga, J.-A.; di Guardo, G.; Jepson, P.D.; Duignan, P.J.; Siebert, U.; Barrett, T.; Santos, M.C.; Moreno, I.B.; Siciliano, S., et al. Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors.Dis. Aquat. Org.2009, 86, 143-157.
38. Kennedy, S.; Smyth, J.A.; Cush, P.F.; McCullough, S.J.; Allan, G.M.; McQuaid, S. Viral distemper now found in porpoises. Nature 1988, 336, 21.
39. Kennedy, S.; Smyth, J.A.; Cush, P.F.; McAliskey, M.; McCullough, S.J.; Rima, B.K. Histopathologic and immunocytochemical studies of distemper in harbor porpoises.Vet. Pathol. 1991, 28, 1-7.
40. Grant, R.J.; Banyard, A.C.; Barrett, T.; Saliki, J.T.; Romero, C.H. Real-time RT-PCR assays for the rapid and differential detection of dolphin and porpoise morbilliviruses. J. Virol. Methods.2009, 156, 117-123.
41. Soto, S.; Alba, A.; Ganges, L.; Vidal, E.; Raga, J.A.; Alegre, F.; González, B.; Medina, P.; Zorrilla, I.; Martínez, J. Post-epizootic chronic dolphin morbillivirus infection in Mediterranean striped dolphins Stenella coeruleoalba. Dis. Aquat. Organ. 2011, 96, 187-194.
42. Lipscomb, T.P.; Schulman, F.Y.; Moffett, D.; Kennedy, S. Morbilliviral disease in Atlantic bottlenose dolphins (Tursiops truncatus) from the 1987-1988 epizootic.J. Wildl. Dis. 1994, 30, 567-557
43. Di Guardo, G.; Agrimi, U.; Morelli, L.; Cardeti, G.; Terracciano, G.; Kennedy, S. Post mortem investigations on cetaceans found stranded on the coasts of Italy between 1990 and 1993. Vet. Rec.1995, 136, 439-442.
44. Domingo, M.; Visa, J.; Pumarola, M.; Marco, A.; Ferrer, L.; Rabanal, R.; Kennedy, S.Pathologic and immunocytochemical studies of morbillivirus infection in striped dolphins (Stenella coeruleoalba).Vet. Pathol. 1992, 29, 1-10.
45. Duignan, P.J.; Geraci, J.R.; Raga, J.A.; Calzada, N. Pathology of morbillivirus infection in striped dolphins (Stenella coeruleoalba) from Valencia and Murcia, Spain. Can. J. Vet. Res.1992, 56, 242-248.
46. Van Bressem, M.-F.; Jepson, P.; Barrett, T. Further insight on the epidemiology of cetacean morbillivirus in the northeastern Atlantic. Mar. Mamm. Sci.1998, 14, 605-613.
47. Van Bressem, M-F.; van Waerebeek, K.; Fleming, M.; Barrett, T. Serological evidence of morbillivirus infection in small cetaceans from the Southeast Pacific. Vet. Microb.1998,59, 89-98.
48. Van Bressem, M-F.; van Waerebeek, K.; Jepson, P.D.; Raga, J.A.; Duignan, P.J.; Nielsen, O.; di Beneditto, A.P.; Siciliano, S.; Ramos, R.; Kant, W., et al. An insight into the epidemiology of dolphin morbillivirus worldwide. Vet. Microb. 2001, 81, 287-304.
49. Bossart, G.D.; Reif, J.S.; Schaefer, A.M.; Goldstein, J.; Fair, P.A.; Saliki, J.T. Morbillivirus infection in free-ranging Atlantic bottlenose dolphins (Tursiops truncatus) from the Southeastern United States: Seroepidemiologic and pathologic evidence of subclinical infection. Vet. Microbiol.2010, 143, 160-166.
50. Bossart, G.D.; Romano, T.A.; Peden-Adams, M.M.; Schaefer, A.; McCulloch, S.; Goldstein, J.D.; Rice, C.D.; Saliki, J.T.; Fair, P.A.; Reif, J.S. Clinicoimmunopathologic findings in atlantic bottlenose dolphins Tursiops truncatuswith positive cetacean morbillivirus antibody titers. Dis. Aquat. Organ.2011,97, 103-112.
51. Di Guardo, G.; di Francesco, C.E.; Eleni, C.; Cocumelli, C.; Scholl, F.; Casalone, C.; Peletto, S.; Mignone, W.; Tittarelli, C.; di Nocera, F., et al. Morbillivirus infection in cetaceans stranded along the Italian coastline: Pathological, immunohistochemical and biomolecular findings. Res. Vet. Sci. 2013, 94, 132-137.
52. Raga, J.A.; Banyard, A.; Domingo, M.; Corteyn, M.; Van Bressem, M-F.; Fernández, M.; Aznar, F.J.; Barrett, T. Dolphin morbillivirus epizootic resurgence, Mediterranean Sea. Emerg. Infect. Dis. 2008,14, 471-473.
53. Stone, B.M.; Blyde, D.J.; Saliki, J.T.; Blas-Machado, U.; Bingham, J.; Hyatt, A.; Wang, J.; Payne, J.; Crameri, S. Fatal cetacean morbillivirus infection in an Australian offshore bottlenose dolphin (Tursiopstruncatus). Aust. Vet. J. 2011,89, 452-457.
54. Sierra, E.; Zucca, D.; Arbelo, M.; García-Álvarez, N.; Andrada, M.; Déniz, S.; Fernández, A. Fatal systemic morbillivirus infection in bottlenose dolphin, Canary Islands, Spain. Emerg. Infect. Dis.2014, 20, 269-271.
55. Yang, W.C.; Pang, V.F.; Jeng, C.R.; Chou, L.S.; Chueh, L.L. Morbilliviral infection in a pygmy sperm whale (Kogia breviceps) from Taiwanese waters. Vet. Microbiol. 2006,116, 69-76
56. NOAA. 2013-2014 Bottlenose Dolphin Unusual Mortality Event in the Mid-Atlantic. 2014. Available online: http://www.nmfs.noaa.gov/pr/health/mmume/midatldolphins2013.html (accessedon 28 August 2014).
57. Nielsen, O.; Smith, G.; Weingartl, H.; Lair, S.; Measures, L. Use of a SLAM transfected Vero cell line to isolate and characterize marine mammal morbilliviruses using an experimental ferret model. J. Wildl. Dis.2008,44, 600-611.
58. Orvell, C.; Blixenkrone-Möller, M.; Svansson, V.; Have, P. Immunological relationships between phocid and canine distemper virus studied with monoclonal antibodies. J. Gen. Virol. 1990, 71, 2085-2092.
59. Saliki, J.T.; Lehenbauer, T.W. Monoclonal antibody-based competitive enzyme-linked immunosorbentassay for detection of morbillivirus antibody in marine mammal sera. J. Clin. Microbiol.2001,39, 1877-1881.
60. Reidarson, T.H.; McBain, J.; House, C.; King, D.P.; Stott, J.L.; Krafft, A., Taubenberger, J.K.; Heyning, J.; Lipscomb, T.P. Morbillivirus infection in stranded common dolphins from the Pacific Ocean. J. Wildl. Dis. 1998,34, 771-776.
61. Lindmark, R.; Thorén-Tolling, K.; Sjöquist, J. Binding of immunoglobulins to protein A and immunoglobulin levels in mammalian sera. J. Immunol. Methods. 1983,62, 1-13.
62. Grant, R.J.; Kelley, K.L.; Maruniak, J.E.; Garcia-Maruniak, A.; Barrett, T.; Manire, C.A.; Romero, C.H. Expression from baculovirus and serological reactivity of the nucleocapsid protein of dolphin morbillivirus. Vet. Microbiol. 2010, 143, 384-388.
63. Nielsen, O.; Stewart, R.E.; Measures, L.; Duignan, P.; House, C. A morbillivirus antibody survey of Atlantic walrus, narwhal and beluga in Canada. J. Wildl. Dis. 2000,36, 508-517.
64. Duignan, P.J.; Nielsen, O.; House, C.; Kovacs, K.M.; Duffy, N.; Early, G.; Sadove, S.; St Aubin, D.J.; Rima, B.K.; Geraci, J.R. Epizootiology of morbillivirus infection in harp, hooded, and ringed seals from the Canadian Arctic and western Atlantic. J. Wildl. Dis.1997, 33, 7-19.
65. Krafft, A.; Lichy, J.H.; Lipscomb, T.P.; Klaunberg, B.A.; Kennedy, S.; Taubenberger, J.K. Postmortem diagnosis of morbillivirus infection in bottlenose dolphins (Tursiops truncatus) in the Atlantic and Gulf of Mexico epizootics by polymerase chain reaction-based assay. J. Wildl. Dis.1995, 31, 410-415.
66. Rubio-Guerri, C.; Melero, M.; Rivera-Arroyo, B.; Bellière, E.N.; Crespo, J.L.; García-Párraga, D.; Esperón, F.; Sánchez-Vizcaíno, J.M. Simultaneous diagnosis of Cetacean morbillivirus infection in dolphins stranded in the Spanish Mediterranean sea in 2011 using a novel Universal Probe Library (UPL) RT-PCR assay. Vet. Microbiol. 2013,165, 109-114.
67. Rubio-Guerri, C.; Melero, M.; Esperón, F.; Bellière, E.N.; Arbelo, M.; Crespo, J.L.; Sierra, E.; García-Párraga, D.; Sánchez-Vizcaíno, J.M. Unusual striped dolphin mass mortality episode related to cetacean morbillivirus in the Spanish Mediterranean sea. BMC Vet. Res. 2013, 9, e106.
68. Ludlow, M.; McQuaid, S.; Milner, D.; de Swart, R.L.; Duprex, W.P. Pathological consequences of systemic measles virus infection. J. Pathol.2015, 235, 253-265
69. De Swart, R.L.; Ludlow, M.; de Witte, L.; Yanagi, Y.; van Amerongen, G.; McQuaid, S.; Yuksel, S.; Geijtenbeek, T.B.; Duprex, W.P.; Osterhaus, A.D. Predominant infection of CD150+ lymphocytes and dendritic cells during measles virus infection of macaques. PLoS Pathog. 2007, 3, e178.
70. Appel, M.P.G. Pathogenesis of canine distemper. Am. J. Vet. Res. 1969, 30, 1167-1182.
71. Lemon, K.; de Vries, R.D.; Mesman, A.W.; McQuaid, S.; van Amerongen, G.; Yuksel, S.; Ludlow, M.; Rennick, L.J.; Kuiken, T.; Rima, B.K., et al. Early target cells of measles virus after aerosol infection of non-human primates. PLoS Pathog. 2011, 7, e1001263.
72. Schulman, F.Y.; Lipscomb, T.P.; Moffett, D.; Krafft, A.E.; Lichy, J.H.; Tsai, M.M.; Taubenberger, J.K.; Kennedy, S. Histologic, immunohistochemical, and polymerase chain reaction studies of bottlenose dolphins from the 1987-1988 United States Atlantic coast epizootic. Vet. Pathol.1997, 34, 288-295.
73. Fernández, A.; Esperón, F.; Herraéz, P.; Espinosa de los Monteros, A.; Clavel, C.; Bernabé, A.; Sanchez-Vizcaino, M.; Verborgh, P.; DeStephanis, R.; Toledano, F., et al. Morbillivirus and pilot whale deaths, Mediterranean Sea. Emerg.Infect. Dis.2008, 14, 792-794.
74. Mazzariol, S.; Marcer, F.; Mignone, W.; Serracca, L.; Goria, M.; Marsili, L.; di Guardo, G.; Casalone, C. Dolphin Morbillivirus and Toxoplasma gondiicoinfection in a Mediterranean fin whale (Balaenoptera physalus). BMC Vet. Res. 2012, 8, e20.
75. Stone, B.M.; Blyde, D.J.; Saliki, J.T.; Morton, J.M. Morbillivirus infection in live stranded, injured, trapped, and captive cetaceans in southeastern Queensland and northern New South Wales, Australia. J. Wildl. Dis. 2012,48, 47-55.
76. Soto, S.; Gonzalez, B.; Willoughby, K.; Maley, M.; Olivera, A.; Kennedy, S.; Marco, A.; Domingo, M. Systemic herpesvirus and morbillivirus co-infection in a striped dolphin (Stenella coeruleoalba). J. Comp. Pathol. 2012, 146, 269-273.
77. Taubenberger, J.K.; Tsai, M.; Krafft, A.E.; Lichy, J.H.; Reid, A.H.; Schulman, F.Y.; Lipscomb, T.P. Two morbilliviruses implicated in bottlenose dolphin epizootics. Emerg. Infect. Dis. 1996, 2, 213-216.
78. Lin, W.H.; Kouyos, R.D.; Adams, R.J.; Grenfell, B.T.; Griffin, D.E. Prolonged persistence of measles virus RNA is characteristic of primary infection dynamics. Proc. Natl. Acad. Sci. USA 2012,109, 14989-14994.
79. Domingo, M.; Vilafranca, M.; Visa, J.; Prats, N.; Trudgett, A.; Visser, I. Evidence for chronic morbillivirus infection in the Mediterranean striped dolphin (Stenella coeruleoalba). Vet. Microbiol. 1995, 44, 229-239.
80. Garg, R.K. Subacute sclerosing panencephalitis. J. Neurol.2008, 255, 1861-1871.
81. Gutierrez, J.; Issacson, R.S.; Koppel, B.S. Subacute sclerosing panencephalitis: An update. Dev. Med. Child Neurol. 2010,52, 901-917.
82. Headley, S.A.; Amude, A.M.; Alfieri, A.F.; Bracarense, A.P.; Alfieri, A.A.; Summers, B.A. Molecular detection of Caninedistemper virus and the immunohistochemical characterization of the neurologic lesions in naturally occurring old dog encephalitis. J. Vet. Diagn. Invest.2009, 21, 588-597
83. Vandevelde, M.; Kristensen, B.; Braund, K.G.; Greene, C.E.; Swango, L.J.; Hoerlein, B.F. Chronic canine distemper virus encephalitis in mature dogs. Vet. Pathol. 1980, 17, 17-28.
84. Griffin, D.E.; Lin, W.H.; Pan, C.H. Measles virus, immune control, and persistence. FEMS Microbiol. Rev. 2012, 36, 649-662.
85. Vandevelde, M.; Zurbriggen, A. The neurobiology of canine distemper virus infection. Vet. Microb.1995, 44, 271-280.
86. Axthelm, M.K.; Krakowka, S. Experimental old dog encephalitis (ODE) in a gnotobiotic dog. Vet. Pathol. 1998, 35, 527-534
87. Maxie, M.G.; Youssef, S. Nervous system. In Jubb, Kennedy, and Palmer’s Pathology of Domestic Animals; Maxie, M.G., Ed.; Saunders/Elsevier: Philadelphia, PA, USA, 2007; Volume 1, pp. 405-408.
88. Di Guardo, G. Morbillivirus-host interaction: Lessons from aquatic mammals. Front. Microbiol. 2012, 3, e431.
89. Gomez de Segura, A.; Crespo, E.A.; Pedraza, S.N.; Hammond, P.S.; Raga, J.A. Abundance of small cetaceans in the waters of the central Spanish Mediterranean. Mar. Biol.2006, 150, 149-160.
90. Schönberger, K.; Ludwig, M.S.; Wildner, M.; Weissbrich, B. Epidemiology of subacute sclerosing panencephalitis (SSPE) in Germany from 2003 to 2009: A risk estimation. PLoS One 2013, 8, e68909.
91. Uchida, K.; Muranaka, M.; Horii, Y.; Murakami, N.; Yamaguchi, R.; Tateyama, S. Non-purulent meningoencephalomyelitis of a Pacific striped dolphin (Lagenorhynchus obliquidens). The first evidence of morbillivirus infection in a dolphin at the Pacific Ocean around Japan. J. Vet. Med.Sci.1999, 61, 159-162.
92. Kennedy, S. Morbillivirus infections in aquatic mammals. J. Comp. Pathol.1998, 119, 201-225.
93. Ludlow, M.; de Vries, R.D.; Lemon, K.; McQuaid, S.; Millar, E.; van Amerongen, G.; Yüksel, S.; Verburgh, R.J.; Osterhaus, A.D.ME.; de Swart, R.L., et al. Infection of lymphoid tissues in the macaque upper respiratory tract contributes to the emergence of transmissible measles virus. J. Gen. Virol. 2013, 94, 1933-1944.
94. Appel, M.J.; Shek, W.R.; Summers, B.A. Lymphocyte-mediated immune cytotoxicity in dogs infected with virulent canine distemper virus.Infect. Immun.1982, 37, 592-600.
95. Griffin, D.E.; Ward, B.J.; Esolen, L.M. Pathogenesis of measles virus infection: An hypothesis for altered immune responses. J. Infect. Dis.1994, 170 (Suppl 1), S24-S31.
96. Heaney, J.; Barrett, T.; Cosby, S.L. Inhibition of in vitroleukocyte proliferation by morbilliviruses. J. Virol.2002, 76, 3579-3584.
97. Schlender, J.; Schnorr, J.J.; Spielhoffer, P.; Cathomen, T.; Cattaneo, R.; Billeter, M.A.; ter Meulen, V.; Schneider-Schaulies, S. Interaction of measles virus glycoproteins with the surface of uninfected peripheral blood lymphocytes induces immunosuppression in vitro. Proc. Natl. Acad. Sci. USA 1996, 93, 13194-13199.
98. Black, F. Epidemiology of Paramyxoviridae. In The Paramyxoviruses;Kingsburry, D.W., Ed.; Plenum Press: New York, NY, USA, 1991;pp. 509-536.
99. Van Bressem, M.-F.; van Waerebeek, K.; Raga, J.A. A review of virus infections of cetaceans and the potential impact of morbilliviruses, poxviruses and papillomaviruses on host population dynamics. Dis. Aquat. Organ. 1999, 38, 53-65.
100. Rijks, J.M.; Osterhaus, A.D.M.E.; Kuiken, T.; Frölich, K. Morbillivirus Infections. In Infectious Diseases of Wild Mammals and Birds in Europe; Gavier-Widén, D., Duff, J.P., Meredith, A., Eds.; Wiley-Blackwell: Oxford, UK, 2012.
101. Van Bressem, M.F.; Raga, J.A. Viruses of Cetaceans. In Studies in Viral Ecology;Hurst, C., Ed.; John Wiley & Sons: Hoboken, NJ, USA, 2011; pp. 309-332.
102. Birkun, A., Jr.; Kuiken, T.; Krivokhizhin, S.; Haines, D.M.; Osterhaus, A.D.M.E.; vandeBildt, M.W.; Joiris, C.R.; Siebert, U. Epizootic of morbilliviral disease in common dolphins (Delphinus delphis ponticus) from the Black sea. Vet. Rec. 1999, 144, 85-92.
103. Chiba, M.E.; Saito, M.; Suzuki, N.; Honda, Y.; Yaegashi, N. Measles infection in pregnancy. J. Infect. 2003, 47, 40-44.
104. Giusti, D.; Burette, J.; Nguyen, Y.; Lévêque, N.; Graesslin, O.; Andreoletti, L. Virological diagnosisand management of two cases of congenital measles. J. Med. Virol.2013,85, 2136-2138.
105. Di Guardo, G.; Cocumelli, C.; Scholl, F.; di Francesco, C.E.; Speranza, R.; Pennelli, M.; Eleni, C. Morbilliviral encephalitis in a striped dolphin Stenella coeruleoalbacalf from Italy. Dis. Aquat. Organ. 2011, 95, 247-251.
106. West, K.L.; Levine, G.; Jacob, J.; Jensen, B.; Sanchez, S.; Colegrove, K.; Rotstein, D. Coinfection and vertical transmission of Brucellaand Morbillivirusin a neonatal sperm whale (Physeter macrocephalus) in Hawaii, USA. J. Wildl. Dis. 2014, doi: 10.7589/2014-04-092.
107. Almberg, E.S.; Cross, P.C.; Smith, D.W. Persistence of canine distemper virus in the Greater Yellowstone ecosystem’s carnivore community. Ecol. Appl.2010, 7, 2058-2074.
108. Dobson, A.; Holdo, R.M.; Holt, R.D. Rinderpest. In Encyclopedia of Biological Invasions;Simberloff, D., Rejmánek, M., Eds.; University of California Press: Berkeley, CA, USA, 1991;pp. 597-604.
109. Griffin, D.E.; Bellini, W.J. Measles virus. In Fields Virology, 3rd ed.;Fields, B.N., Knipe, D.M., Howley, P.M., Chanock, R.M., Melnick, J.I., Monath, T.P., Roizman, B., Straus, S.E., Eds.; Lippincott-Raven Publishers: Philadelphia, PA, USA, 1996; pp. 1267-1312.
110. Wohlsein, P.; Puff, C.; Kreutzer, M.; Siebert, U.; Baumgärtner, W. Distemper in a dolphin. Emerg. Infect. Dis. 2007,13, 1959-1961.
111. Jauniaux, T.; Charlier, G.; Desmecht, M.; Haelters, J.; Jacques, T.; Losson, B.; van Gompel, J.; Tavernier, J.; Coignoul, F. Pathological findings in two fin whales (Balaenoptera physalus) with evidence of morbillivirus infection. J. Comp. Pathol. 2000,123,198-201.
112. Aguilar, A.; Raga, J.A. The striped dolphin epizootic in the Mediterranean Sea. Ambio1993, 22, 524-528.
113. Tsur, L.; Goffman, O.; Yakobsen, B.; Moffet, D.; Kennedy, S. Morbillivirus infection in a bottlenose dolphin (Tursiops truncatus) from the Mediterranean Sea. Eur. J. Vet. Pathol. 1997, 2, 83-85.
114. Hersh, S.L.; Odell, D.K.; Asper, E.D. Bottlenose dolphin mortality patterns in the Indian/Banana river system in Florida. In The Bottlenose Dolphin; Leatherwood, S.P., Reeves, R.R., Eds.; Academic Press: San Diego, CA, USA, 1990;pp. 155-164.
115. Update on the dolphin morbillivirus outbreak and the 2013-2014 U.S.Mid-Atlantic bottlenose dolphin (Tursiops truncatus) unusual mortality event.Available online: https://events.iwc.int/index.php/scientific/SC65B/paper/viewFile/759/757/SC-65b-E03.pdf (accessed on 15 August 2014).
116. Tomo, I.; Bastianello, S.; Woolford, L.; Kemper, C.; Dickson, C., Kelly D.; Wang, J.; Bingham, J. Pathology of dolphins during an unusual mortality event in South Australia, 2013. In Proceedings of the 20 Biennial Conference on the Biology of Marine Mammals, Dunedin, New Zealand, 9-13 December 2013.
117. Kennedy, S.; Kuiken, T.; Ross, H.M.; McAliskey, M.; Moffett, D.; McNiven, M.; Carole, M. Morbillivirus infection in two common porpoises (Phocoena phocoena) from the coasts of England and Scotland. Vet. Rec.1992, 31, 286-290.
118. Jepson, P.D.; Baker, J.R.; Kuiken, T.; Simpson, V.R.; Kennedy, S.; Bennett, P.M. Pulmonary pathology of harbour porpoises (Phocoena phocoena) stranded in England and Wales between 1990 and 1996. Vet. Rec.2000, 46, 721-728.
119. Siebert, U.; Wünschmann, A.; Weiss, R.; Frank, H.; Benke, H.; Frese, K. Post-mortem findings in harbour porpoises (Phocoena phocoena) from the German North and Baltic Seas. J. Comp. Pathol. 2001,124, 102-114.
120. Jauniaux, T.; Petitjean, D.; Brenez, C.; Borrens, M.; Brosens, L.; Haelters, J.; Tavernier, T.; Coignoul, F. Post-mortem findings and causes of death of harbour porpoises (Phocoena phocoena) stranded from 1990 to 2000 along the coastlines of Belgium and Northern France. J. Comp. Pathol.2002, 126, 243-253.
121. Hammond, P.S.; Berggren, P.; Benke, H.; Borchers, D.L.; Collet, A.; Heide-Jorgensen, M.P.; Heimlich, S.; Hiby, A.R.; Leopold, M.F.; Øien, N. Abundance of harbour porpoise and other cetaceans in the North Sea and adjacent waters. J. Appl. Ecol. 2002, 39, 361-376.
122. Forcada, J.; Aguilar, A.; Hammond, P.S.; Pastor, X.; Aguilar, R. Distribution and numbers of striped dolphins in the western Mediterranean sea after the 1990 epizootic outbreak. Mar. Mamm. Sci.1994, 10, 137-150.
123. Garibaldi, F.; Mignone, W.; Caroggio, P.; Ballardini, M.; Podestà, M.; Bozzetta, E.; Casalone, C.; Marsilio, F.; di Francesco, C.E.; Proietto, U., et al. Serological evidence of Morbillivirus infection in striped dolphins (Stenella coeruleoalba) found stranded on the Ligurian Sea coast of Italy. In Proceedings of the 22th European Cetacean Society Conference, Egmond aan Zee, The Netherlands, 10-12 March2008; pp. 192-193.
124. Wierucka, K.; Verborgh, P.; Meade, R.; Colmant, L.; Gauffier, P.; Esteban, R.; de Stephanis, R.; Cañadas, A. Effects of a morbillivirus epizootic on long-finned pilot whales Globicephala melasin Spanish Mediterranean waters. Mar. Ecol.Prog. Ser.2014, 502, 1-10.
125. Gomez De Segura, A.; Hammond, P.S.; Cañadas, A.; Raga, J.A. Comparing cetacean abundance estimates derived from spatial models and design-based line transect methods. Mar. Ecol. Prog. Ser 2007, 329,289-299.
126. Soto, S. Morbillivirus Infection in Mediterranean Striped Dolphins (Stenella coeruleoalba) during the 2007 Epidemic and the Post-Epidemic Years. Ph.D. Thesis, Universidad Autonoma de Barcelona, Barcelona, Spain, September 2014.
127. Aguilar, A.; Borrell, A. Abnormally high polychlorinated biphenyl levels in striped dolphins (Stenella coeruleoalba) affected by the 1990-1992 Mediterranean epizootic. Sci. Total Environ.1994, 154, 237-247
128. Aznar, F.J.; Perdiguero, D.; Pérez del Olmo, A.; Repullés, A.; Agustí, C.; Raga, J.A. Changes in epizoic crustacean infestations during cetacean die-offs: The mass mortality of Mediterranean striped dolphins Stenella coeruleoalba revisited. Dis. Aquat. Org.2005, 67, 239-247
129. Fossi, M.C.; Casini, S.; Marsili, L. Potential toxicological hazard due to endocrine-disrupting chemicals on Mediterranean top predators: State of art, gender differences and methodological tools. Environ. Res. 2007, 104, 174-182.
130. Valsecchi, E.; Amos, W.; Raga, J.A.; Podestà, M.; Sherwin, W. The effects of inbreeding on mortality during a morbillivirus outbreak in the Mediterranean striped dolphin (Stenella coeruleoalba). Anim. Cons. 2004, 7, 139-146.
131. Casalone, C.; Mazzariol, S.; Pautasso, A.; di Guardo, G.; di Nocera, F.; Lucifora, G.; Ligios, C.; Franco, A.; Fichi, G.; Cocumelli, C., et al. Cetacean strandings in Italy: An unusual mortality event along the Tyrrhenian Sea coast in 2013. Dis. Aquat. Org.2014, 109, 81-86.
132. Nortobartolo di Sciara, G.; Birkun, G. Conserving Whales, Porpoises and Dolphins in the Mediterranean and Black Seas: An ACCOBAMS Status Report; ACOBAMS: Monaco, Principality of Monaco, 2010;p. 212.
133. McLellan, W.; Friedlaender, A.; Mead, J.; Potter, C.; Pabst, D.A. Analysing 25 years of bottlenose dolphin (Tursiops truncatus) strandings along the Atlantic coast of the USA: Do historic records support the coastal migratory stock hypothesis. J. Cet. Res. Manag.2002, 4, 297-304.
134. Rosel, P.E.; Hansen, L.; Hohn, A.A. Restricted dispersal in a continuously distributed marine species: Common bottlenose dolphins Tursiops truncatusin coastal waters of the western North Atlantic. Mol. Ecol. 2009, 18, 5030-5045.
135. Lipscomb, T.P.; Kennedy, S.; Moffett, D.; Krafft, A.; Klaunberg, B.A.; Lichy, J.H.; Regan G.T.; Worthy, G.A.; Taubenberger, J.K. Morbilliviral epizootic in bottlenose dolphins of the Gulf of Mexico. J. Vet. Diagn. Invest. 1996, 8, 283-290.
136. Worthy, A.J. Patterns of Bottlenose Dolphin, Tursiops truncatus, Strandings in Texas. In Characteristics and Causes of Texas Marine Strandings;Zimmennan, R., Ed.; NOAA TechnicalReportNMFS 143; U.S. DepartmentCommerce: Galveston,TX, USA, 1998; p. 85.
137. Cantor, M.; Wedekin, L.L.; Daura-Jorge, F.G.; Rossi-Santos, M.R.; Simoes-Lopes, P. Assessing population parameters and trends of Guiana dolphins (Sotalia guianensis): An eight-year mark-recapture study. Mar. Mamm. Sci. 2012, 28, 63-83.
138. Rossi-Santos, M.; Wedekin, L.L.; Sousa-Lima, R.S. Distribution and habitat use of small cetaceans off Abrolhos Bank, eastern Brazil. LAJAM2006,5, 23-28.
139. Martins, C.C.A.; Morete, M.E.; Engel, M.H.; Freitas, A.C., Secchi, E.R.; Kinas, P.G. Aspects of habitat use patterns of humpback whales in the Abrolhos Bank, Brazil, breeding ground. Mem. Qld. Mus.2001,47, 563-570.
140. Wedekin, L.L.; Freitas, A.; Engel, M.H.; Sazima, I. Rough-toothed dolphins (Steno bredanensis) catch diskfishes while interacting with humpback whales (Megaptera novaeangliae) off Abrolhos Bank breeding ground, southwest Atlantic. Aquat. Mamm.2004,30, 327-329.
141. Groch, K.R.; Carvalho, V.L.; Meirelles, A.C.O.; Gonzales-Viera, O.; Kolesnikovas, C.K.M.; Groch, K.R.; Zucca, D.; Fernández, A.; Catão-Dias, J.L. Morbillivirus in live stranded cetaceans from Brazilian coast: Immunohistochemical evidence. In Proceedings of the 20th Biennial Conference onthe Biology of Marine Mammals, Dunedin, New Zealand, 9-13 December 2013; pp. 85-86
142. Bodewes, R.; Morick, D.; van de Bildt, M.W.G.; Osinga, N.; Rubio Garcia, A.; Sanchez Contreras, G.J.; Smits, S.L.; Reperant, L.A.P.; Kuiken, T.; Osterhaus, A.D.M.E. 2014 Prevalence of phocine distemper virus specific antibodies: Bracing for the next seal epizootic in north-western Europe. Emerg. Microbes. Infect.2013, 2, e3.
143. Prachayangprecha, S.; Schapendonk, C.M.; Koopmans, M.P.; Osterhaus, A.D.M.E.; Schürch, A.C.; Pas, S.D.; van der Eijk, A.A.; Poovorawan, Y.; Haagmans, B.L.; Smits, S.L. Exploring the potential of next-generation sequencing in detection of respiratory viruses. J. Clin. Microbiol. 2014,52, 3722-3730.
144. Muniraju, M.; Munir, M.; Parthiban, A.R.; Banyard, A.C.; Bao, J.; Wang, Z.; Ayebazibwe, C.; Ayelet, G.; El Harrak, M.; Mahapatra, M., et al. Molecular evolution of peste des petits ruminants virus. Emerg. Infect. Dis. 2014, 20,2023-2033.
145. Drexler, J.F.; Corman, V.M.; Müller, M.A.; Maganga, G.D.; Vallo, P.; Binger, T.; Gloza-Rausch, F.; Cottontail, V.M.; Rasche, A.; Yordanov, S., et al. Bats host major mammalian paramyxoviruses. Nat. Commun.2012,3, e796.
146. Mazzariol, S.; Peletto, S.; Mondin, A.; Centelleghe, C.; di Guardo, G.; di Francesco, C.E.; Casalone, C.; Acutis, P.L. Dolphin morbillivirus infection in a captive harbor seal (Phoca vitulina). J. Clin. Microbiol. 2013, 51, 708-711.
147. Van de Bildt, M.W.; Martina, B.E.; Sidi, B.A.; Osterhaus, A.D.M.E. Morbillivirus infection in a bottlenose dolphin and a Mediterranean monk seal from the Atlantic coast of West Africa. Vet. Rec.2001, 148, 210-211.
148. Grenfell, B.T.; Lonergan, M.E.; Harwood, J. Quantitative investigations of the epidemiology of phocine distemper virus (PDV) in European common seal populations. Sci. Total Environ. 1992, 115, 15-29.