LETTERS

C. cayetanensis and these closely re- Mountain in Shaanxi Province, northwest Serologic surveys indicate that lated species in monkeys; what ad- China. PLoS ONE. 2013;8:e58216. http:// infect marine mam- dx.doi.org/10.1371/journal.pone.0058216 ditional monkey host species, espe- 7. da Silva AJ, Bornay-Llinares FJ, Moura mals worldwide (5); however, only 1 cially on Bioko Island, may harbor I, Slemenda SB, Tuttle JL, Pieniazek fatal case in a bottlenose (Tur- Cyclospora spp.; and what other as yet NJ. Fast and reliable extraction of proto- siops truncatus) has been confirmed unrecognized species of Cyclospora zoan parasite DNA from fecal specimens. in the Southern Hemisphere (in the Mol Diagn. 1999;4:57–64. http://dx.doi. may be infecting primates. org/10.1016/S1084-8592(99)80050-2 southwestern Pacific Ocean) (6). Posi- 8. da Silva AJ, Cacciò S, Williams C, tive DMV-specific antibody titers in Mark L. Eberhard, Won KY, Nace EK, Whittier C, et al. 3 Fraser’s (Lagenodelphis Jacob R. Owens, Molecular and morphologic charac- hosei) stranded off and Argen- Henry S. Bishop, terization of a Cryptosporidium geno- type identified in lemurs. Vet Parasitol. tina in 1999 indicate the exposure of Marcos E. de Almeida, 2003;111:297–307. http://dx.doi.org/10.1016/ South Atlantic cetaceans to morbil- Alex J. da Silva, Gail Hearn, S0304-4017 (02)00384-9 livirus (7). We report a case of lethal and Shaya Honarvar 9. Jones PJ. Biodiversity in the Gulf of infection in a Guiana Guinea: an overview. Biodiversity and Author affiliations: Centers for Disease Conservation. 1994;3:772–84. http:// dolphin (Sotalia guianensis), a coastal Control and Prevention, Atlanta, Georgia, dx.doi.org/10.1007/BF00129657 marine and estuarine species that oc- USA (M.L. Eberhard, H.S. Bishop, M.E. de 10. Xing J, Wang H, Han K, Ray DA, curs off the Atlantic Coast of South Almeida, A.J. da Silva); and Drexel Univer- Huang CH, Chemnick LG, et al. A and . mobile element based phylogeny of sity, Philadelphia, Pennsylvania, USA (J.R. Old World monkeys. Mol Phylogenet A female Guiana dolphin calf Owens, G. Hearn, S. Honarvar) Evol. 2005;37:872–80. http://dx.doi. (108 cm in total body length) (8) was org/10.1016/j.ympev.2005.04.015 DOI: http://dx.doi.org/10.3201/eid2003.131368 found stranded dead in Guriri (18°44′S; 39°44′W), São Mateus, Espírito Santo Address for correspondence: Mark L. Eberhard, References State, Brazil, on November 30, 2010; Centers for Disease Control and Prevention, the dead calf was severely emaciated. 1. Herwaldt BL. Cyclospora cayetanensis: 1600 Clifton Rd NE, Mailstop D65, Atlanta, GA Postmortem examination of the a review, focusing on the outbreaks 30333, USA; email: [email protected] showed multifocal ulcers in the oral if cyclosporiasis in the 1990s. Clin Infect Dis. 2000;31:1040–57. http:// mucosa and genital slit, diffusely dark dx.doi.org/10.1086/314051 red and edematous lungs, and con- 2. Herwaldt BL. The ongoing saga of gested and edematous brain. Samples U.S. outbreaks of cyclosporiasis associ- of selected tissues were collected, fixed ated with imported fresh produce: what Cyclospora cayetanensis has taught us in buffered formalin, and processed and what we have yet to learn. In: Institute according to routine histopathologic of Medicine, editors. Addressing food- Novel Cetacean methods. By microscopy, the most borne threats to health: policies, practices, noteworthy lesions included marked and global coordination. Washington Morbillivirus in (DC): National Academies Press. 2006. p. lymphoplasmacytic and neutrophil- 85–115, 131–140. Guiana Dolphin, ic meningoencephalitis, optic nerve 3. Centers for Disease Control and Brazil perineuritis, and hypophysitis. Lungs Prevention. Notes from the field: outbreaks showed moderate acute diffuse lym-  of cyclosporiasis United States, June– To the Editor: Since 1987, mor- August 2013. MMWR Morb Mortal Wkly phoplasmacytic and neutrophilic inter- Rep. 2013;62:862–86. billivirus (family Paramyxoviridae, stitial pneumonia; severe multicentric 4. Eberhard ML, daSilva AJ, Lilley BG, genus Morbillivirus) outbreaks among lymphoid depletion and multifocal nec- Pieniazek NJ. Morphologic and molecular pinnipeds and cetaceans in the North- rotizing hepatitis were also observed. characterization of new Cyclospora spe- ern Hemisphere have caused high cies from Ethiopian monkeys: C. cercopi- Immunohistochemical analysis theci sp.n., C. colobi sp.n., and C. papio- rates of death (1,2). Two morbillivirus was performed by using CDV-NP MAb nis sp.n. Emerg Infect Dis. 1999;5:651–8. species are known to affect aquatic an- (VMRD, Inc., Pullman, WA, USA), a http://dx.doi.org/10.3201/eid0505.990505 imals: Phocine distemper (PDV) monoclonal antibody against the nu- 5. Eberhard ML, Njenga MN, daSilva AJ, and Cetacean morbillivirus (CeMV). Owino D, Nace EK, Won KY, et al. cleoprotein antigen of canine distemper A survey for Cyclospora spp. in Kenyan PDV has been isolated from pinni- virus that cross-reacts with cetacean primates with some notes on its biology. peds, and 3 strains of CeMV ( morbilliviruses (9). Known positive J Parasitol. 2001;87:1394–7. morbillivirus [PMV], dolphin morbil- and negative control tissues and test 6. Zhao GH, Cong MM, Bian QQ, Chen WY, livirus [DMV], and pilot mor- Wang RJ, Qi M, et al. Molecular character- sections with omitted first-layer an- ization of Cyclospora-like organisms from billivirus [PWMV]) have been iso- tibody were included. Viral antigen golden snub-nosed monkeys in Qinling lated from dolphins and (3,4). was detected in neurons in the brain,

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 20, No. 3, March 2014 511 LETTERS bronchiolar epithelium and macro- strains PMV, DMV, and PWMV (Fig- are a major risk to previously unex- phages in the lungs, bile duct epithe- ure). The sample shared 79.8% nt and posed nonimmune populations of lium in the liver, and macrophages and 58.4% aa identity with PMV, 78.7% nt aquatic (1,2). A high num- lymphocytes in lymph nodes. and 56.6% aa identity with DMV, and ber of morbillivirus-related deaths We extracted RNA from frozen 78.7% nt and 57.1% aa identity with have not yet been reported among lung samples by using TRIzol Re- PWMV. Within the Morbillivirus spp., aquatic mammals in the waters off agent (Life Technologies Corporation, PDV shared the lowest sequence iden- Brazil, but our findings shows that Carlsbad, CA, USA) according to the tity (51.1% nt and 26.8% aa). Guiana dolphin calves are suscep- manufacturer’s instructions and am- In summary, sequence analysis tible to infection. Subclinical mor- plified a 374-bp conserved fragment of the morbillivirus from the dead billivirus infection with immune of the phosphoprotein (P) gene by re- Guiana dolphin suggests that the suppression has been reported in verse transcription PCR. The follow- virus is a novel strain of the CeMV bottlenose dolphins in Florida (10). ing Morbillivirus spp.–specific primers species; this conclusion is sup- It is unknown whether subclinical in- were used for PCR: 5′-ATGTTTAT- ported by phylogenic analysis and fection occurs in this host population GATCACAGCGGT-3′ (forward) and geographic distribution of the virus or whether the virus has undergone 5′-ATTGGGTTGCACCACTTGTC-3′ and by its distinct host. Emaciation, species-adaptive changes, as pro- (reverse) (3). MEGA5 (http://mega marked lymphoid depletion, inter- posed for PWMV (4). The sequence software.net/) was used to construct stitial pneumonia, and meningoen- data from our study suggest that the a neighbor-joining phylogenic tree cephalitis are common findings in virus from the Guiana dolphin calf based on the sequenced amplicon morbillivirus-infected (1,2). is the fourth member of the CeMV from this study (GenBank accession Together with antigenic and genom- group and is closer to the root of the no. KF711855) and 12 other GenBank ic evidence, our findings indicate CeMV clade than to that of DMV, sequences that represent the 6 morbil- that morbillivirus infection is extant PMV, or PWMV. Further studies are livirus species already described in in Guiana dolphins in the waters required to determine the epidemiol- the literature. The analysis placed the off Brazil. ogy of morbillivirus infection in this Guiana dolphin strain at the CeMV Morbillivirus outbreaks have and other cetacean species and to as- clade, but segregated it from the al- caused a high number of deaths sess the risk for epizootic outbreaks ready described dolphin morbillivirus among pinnipeds and cetaceans and among South Atlantic cetaceans.

Figure. Phylogenetic tree of a 374-bp conserved region from the phosphoprotein gene of a cetacean morbillivirus isolated from a Guiana dolphin (in boldface; GenBank accession no. KF711855) and 12 other previously described morbilliviruses. Sendai virus was added as an outgroup member. Sequences were aligned and a neighbor-joining tree with 1,000 bootstrap replications was generated by using MEGA5 (http://megasoftware.net/). For comparison, recognized of the Morbillivirus spp. (Measles virus [MV], Rinderpest virus [RPV], Peste-des-petits ruminants virus [PPRV], Canine distemper virus [CDV], and Phocine distemper virus [PDV]) were included, as were the 3 Cetacean morbillivirus (CeMV) strains: porpoise morbillivirus (PMV), dolphin morbillivirus (DMV), and morbillivirus (PWMV). Sequence names are followed by species of cetacean, year of stranding (when available), and the abbreviation for the geographic area. Me, Mediterranean Coast; Pa, Pacific Ocean; At, Atlantic Ocean; No, North Sea. The sequence for PMV strain phocoena, is from Barrett et al. (3). The scale bar indicates nucleotide substitutions per site.

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Acknowledgments References Address for correspondence: Kátia R. Groch, We thank Ariosvaldo Pinto dos Santos Laboratório de Patologia Comparada de 1. Di Guardo G, Marruchella G, Agrimi U, and volunteers for the valuable help during Animais Selvagens, FMVZ, Universidade Kennedy S. Morbillivirus infections the fieldwork; Projeto TAMAR and Parque in aquatic mammals: a brief overview. de São Paulo, Av. Orlando Marques de Paiva Estadual de Itaúnas for reporting stranded J Vet Med A Physiol Pathol Clin Med. 87, São Paulo, SP, 05508-270, Brazil; email: marine mammals and providing logistical 2005;52:88–93. http://dx.doi.org/10.1111/ [email protected] j.1439-0442.2005.00693.x support in many stranding events; Jane 2. Kennedy S. Morbillivirus infections Megid, Adriana Cortez, Susan D. Allen- in aquatic mammals. J Comp Pathol. dorf, Cíntia Maria Favero, and laboratory 1998;119:201–25. http://dx.doi.org/10.1016/ staffs from participating institutions for S0021-9975(98)80045-5 3. Barrett T, Visser IK, Mamaev L, Goatley L, assistance during analysis; and the journal Van Bressem MF, Osterhaus AD. editor and 2 anonymous reviewers for their Dolphin and porpoise morbilliviruses are constructive comments. genetically distinct from phocine distemper virus. Virology. 1993;193:1010–2. http:// Fundação de Amparo à Pesquisa do dx.doi.org/10.1006/viro.1993.1217 Estado de São Paulo provided grants (pro- 4. Taubenberger JK, Tsai MM, Atkin TJ, cesses 2010/50094-3, 2011/08357-0 and Fanning TG, Krafft AE, Moeller RB, et al. Molecular genetic evidence of 2012/00021-5), which are greatly appreci- a novel morbillivirus in a long-finned ated. Veracel Celulose provided financial pilot whale (Globicephalus melas). Emerg support to the Rescue Program. Projeto Infect Dis. 2000;6:42–5. http://dx.doi. Baleia Jubarte is sponsored by Petroleo org/10.3201/eid0601.000107 5. Van Bressem M-F, Raga JA, Guardo GD, Brasileiro (Petrobras). J.L.C.-D. is a re- Jepson PD, Duignan PJ, Siebert U, et al. cipient of a professorship by the Conselho Emerging infectious diseases in ceta- Outbreak of a Nacional de Desenvolvimento Científico e ceans worldwide and the possible role Tecnológico–CNPq (301517/2006-1). of environmental stressors. Dis Aquat Organ. 2009;86:143–57. http://dx.doi. New Strain of This study was conducted by K.R.G. org/10.3354/dao02101 as partial fulfillment of the requirements 6. Stone BM, Blyde DJ, Saliki JT, Flu at a Fair Blas-Machado U, Bingham J, Hyatt A, for a doctoral degree at the Departamen- et al. Fatal cetacean morbillivirus infec- to de Patologia, Faculdade de Medicina tion in an Australian offshore bottlenose Dr. Karen Wong, an EIS Veterinária e Zootecnia, Universidade de dolphin (Tursiops truncatus). Aust Vet J. officer with the Centers São Paulo. 2011;89:452–7. http://dx.doi.org/10.1111/ j.1751-0813.2011.00849.x for Disease Control and 7. Van Bressen MF, Van Waerebeek K, Prevention, discusses her Kátia R. Groch, Jepson PD, Raga JA, Duignan PJ, Nielsen O, et al. An insight into the epidemiology of Adriana C. Colosio, dolphin morbillivirus worldwide. Vet Mi- study about flu outbreaks Milton C. C. Marcondes, crobiol. 2001;81:287–304. http://dx.doi. at agricultural fairs. Daniele Zucca, org/10.1016/S0378-1135(01)00368-6 Josué Díaz-Delgado, 8. Di Beneditto APM, Ramos RMA. Biology of the marine dolphin Claudia Niemeyer, ( fluviatilis) in south-eastern Juliana Marigo, Brazil. Journal of the Marine Biologi- Paulo E. Brandão, cal Association of the United King- Antonio Fernández, dom. 2004;84:1245–50. http://dx.doi. org/10.1017/S0025315404010744h and José Luiz Catão-Dias 9. Saliki JT, Cooper EJ, Gustavson JP. Author affiliations: University of São Paulo, Emerging morbillivirus infections of São Paulo, Brazil (K.R. Groch, C. Niemey- marine mammals: development of er, J. Marigo, P.E. Brandão, J.L. Catão- two diagnostic approaches. Ann N Y Acad Sci. 2002;969:51–9. http://dx.doi. Dias); Instituto Baleia Jubarte, Caravelas, org/10.1111/j.1749-6632.2002.tb04350.x Brazil (K.R. Groch, A.C. Colosio, M.C.C. 10. Bossart GD, Romano TA, Peden- Marcondes); and University of Las Palmas Adams MM, Schaefer A, McCulloch de Gran Canaria, Las Palmas de Gran Ca- S, Goldstein JD, et al. Clinicoimmuno- pathologic findings in Atlantic bottlenose naria, Canary Islands, Spain (D. Zucca, J. dolphins Tursiops truncatus with positive http://www2c.cdc. Díaz-Delgado, A. Fernández) cetacean morbillivirus antibody titers. gov/podcasts/player. Dis Aquat Organ. 2011;97:103–12. http:// DOI: http://dx.doi.org/10.3201/eid2003.131557 dx.doi.org/10.3354/dao02410 asp?f=8627464

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