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Published in: EcoHealth 2/2019

01-06-2019 | Original Contribution

Chelonid Alphaherpesvirus 5 DNA in Fibropapillomatosis-Affected Chelonia mydas

Authors: Isabela G. Domiciano, Matt K. Broadhurst, Camila Domit, Karina K. M. C. Flaiban, Daphne W. Goldberg, Juliana T. T. Fritzen, Ana Paula F. R. L. Bracarense

Published in: EcoHealth | Issue 2/2019

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Abstract

Fibropapillomatosis is a panzootic and chronic disease among Chelonia mydas—usually associated with anthropogenic impacts. This study contributes towards understanding fibropapillomatosis implications for C. mydas populations as a reflector of environmental quality, via prevalence and histological, molecular and blood analyses at a World Heritage site in southern Brazil. Sixty-three juvenile C. mydas (31.3–54.5 cm curved carapace length–CCL) were sampled during two years. Eighteen specimens (~ 29%) had tumours (which were biopsied), while 45 had none. Degenerative changes in the epidermis and Chelonid alphaherpesvirus 5 DNA detection with three variants support a herpesvirus infection. Phylogenetic analysis indicated that variants A and B were similar to a herpesvirus lineage from the Atlantic group, but variant C was similar to a herpesvirus from the eastern Pacific lineage and represents the first published case for marine turtles off Brazil. Significantly lower levels of seven blood parameters, but greater numbers of eosinophils, were observed in tumour-afflicted animals. These observations were attributed to metabolism efficiencies and/or differences in diet associated with temporal-recruitment bias and disease development, and greater non-specific immune stimulation. While most animals had adequate body condition independent of disease, longer-term studies are required to elucidate any protracted population effects.
Literature
go back to reference Aguirre AA, Lutz PL (2004) Marine turtles as sentinels of ecosystem health: is fibropapillomatosis an indicator?. EcoHealth 1: 275–283 Aguirre AA, Lutz PL (2004) Marine turtles as sentinels of ecosystem health: is fibropapillomatosis an indicator?. EcoHealth 1: 275–283
go back to reference Aguirre AA, Balazs GH (2000) Blood biochemistry values of green turtles, Chelonia mydas, with and without fibropapillomatosis. Comparative Haematology International 10: 132–137CrossRef Aguirre AA, Balazs GH (2000) Blood biochemistry values of green turtles, Chelonia mydas, with and without fibropapillomatosis. Comparative Haematology International 10: 132–137CrossRef
go back to reference Aguirre AA, Balazs GH, Spraker TR, Gross TS (1995) Adrenal and hematological responses to stress in juvenile green turtles (Chelonia mydas) with and without fibropapillomatosis. Physiological Zoology 68: 831–854CrossRef Aguirre AA, Balazs GH, Spraker TR, Gross TS (1995) Adrenal and hematological responses to stress in juvenile green turtles (Chelonia mydas) with and without fibropapillomatosis. Physiological Zoology 68: 831–854CrossRef
go back to reference Bolten AB, Bjorndal KA (1992) Blood profiles for a wild population of green turtles (Chelonia mydas) in the southern Bahamas: size-specific and sex-specific relationships. Journal of Wildlife Disease 28: 407–413CrossRef Bolten AB, Bjorndal KA (1992) Blood profiles for a wild population of green turtles (Chelonia mydas) in the southern Bahamas: size-specific and sex-specific relationships. Journal of Wildlife Disease 28: 407–413CrossRef
go back to reference Bourjea J, Lapègue S, Gagnevin L, Broderick D, Mortimer JA, Ciccione S, Roos D, Taquet C, Grizel H (2007) Phylogeography of the green turtle, Chelonia mydas, in the Southwest Indian Ocean. Molecular Ecology 16: 175–186CrossRefPubMed Bourjea J, Lapègue S, Gagnevin L, Broderick D, Mortimer JA, Ciccione S, Roos D, Taquet C, Grizel H (2007) Phylogeography of the green turtle, Chelonia mydas, in the Southwest Indian Ocean. Molecular Ecology 16: 175–186CrossRefPubMed
go back to reference Campbell TW (2014) Clinical pathology. In: Current therapy in reptile medicine and surgery, Mader DR, Divers SJ (editors), Missouri: Elsevier, 70–92CrossRef Campbell TW (2014) Clinical pathology. In: Current therapy in reptile medicine and surgery, Mader DR, Divers SJ (editors), Missouri: Elsevier, 70–92CrossRef
go back to reference Carretero R, Sektioglu IM, Garbi, N, Salgado OC, Beckhove P (2015) Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8(+) T cells. Nature Immunology 16: 609–617CrossRefPubMed Carretero R, Sektioglu IM, Garbi, N, Salgado OC, Beckhove P (2015) Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8(+) T cells. Nature Immunology 16: 609–617CrossRefPubMed
go back to reference Coelho VF, Domit C, Broadhurst MK, Nishizawa H, Prosdocimi L, Almeida FS (2018) Intra-specific variation in skull morphology of juvenile Chelonia mydas in the southwestern Atlantic Ocean. Marine Biology 165:174CrossRef Coelho VF, Domit C, Broadhurst MK, Nishizawa H, Prosdocimi L, Almeida FS (2018) Intra-specific variation in skull morphology of juvenile Chelonia mydas in the southwestern Atlantic Ocean. Marine Biology 165:174CrossRef
go back to reference Chaloupka M, Work TM, Balazs GH, Murakawa SKK, Morris M (2008) Cause-specific temporal and spatial trends in green sea turtle strandings in the Hawaiian archipelago (1982–2004). Marine Biology 154: 887–898CrossRef Chaloupka M, Work TM, Balazs GH, Murakawa SKK, Morris M (2008) Cause-specific temporal and spatial trends in green sea turtle strandings in the Hawaiian archipelago (1982–2004). Marine Biology 154: 887–898CrossRef
go back to reference Diniz GS, Barbarino E, Lourenço SO (2012) On the chemical profile of marine organisms from the coastal subtropical environments: gross composition and nitrogen-to-protein conversion factors. In: Marcelli, M (ed) Oceanography. Intech, Rijeka, pp 297–320 Diniz GS, Barbarino E, Lourenço SO (2012) On the chemical profile of marine organisms from the coastal subtropical environments: gross composition and nitrogen-to-protein conversion factors. In: Marcelli, M (ed) Oceanography. Intech, Rijeka, pp 297–320
go back to reference Domiciano IG, Domit C, Bracarense APFRL (2017) The Green turtle Chelonia mydas as a marine and coastal environmental sentinels: anthropogenic activities and diseases. Semina 38: 3417–3434 Domiciano IG, Domit C, Bracarense APFRL (2017) The Green turtle Chelonia mydas as a marine and coastal environmental sentinels: anthropogenic activities and diseases. Semina 38: 3417–3434
go back to reference Domiciano IG, Domit C, Broadhurst MK, Koch MS, Bracarense APFRL (2016) Assessing disease and mortality among small cetaceans stranded at a World Heritage Site in southern Brazil. PloS ONE 11: e0149295.1– e0149295.17CrossRef Domiciano IG, Domit C, Broadhurst MK, Koch MS, Bracarense APFRL (2016) Assessing disease and mortality among small cetaceans stranded at a World Heritage Site in southern Brazil. PloS ONE 11: e0149295.1– e0149295.17CrossRef
go back to reference Doweiko JP, Nompleggi DJ (1991) The role of albumin in human physiology and pathophysiology, Part III: albumin and disease state. Journal of Parenteral and Enteral Nutrition 15: 476–483CrossRefPubMed Doweiko JP, Nompleggi DJ (1991) The role of albumin in human physiology and pathophysiology, Part III: albumin and disease state. Journal of Parenteral and Enteral Nutrition 15: 476–483CrossRefPubMed
go back to reference Felsenstein, J. (1985) Confidence Limits on Phylogenies: An Approach Using the Bootstrap. Evolution, 39: 783-791CrossRefPubMed Felsenstein, J. (1985) Confidence Limits on Phylogenies: An Approach Using the Bootstrap. Evolution, 39: 783-791CrossRefPubMed
go back to reference Flint M, Morton JM, Limpus CJ, Patterson-Kane JC, Murray PJ, Mills PC (2009) Development and application of biochemical and haematological reference intervals to identify unhealthy green sea turtles (Chelonia mydas). The Veterinary Journal 185: 299–304CrossRefPubMed Flint M, Morton JM, Limpus CJ, Patterson-Kane JC, Murray PJ, Mills PC (2009) Development and application of biochemical and haematological reference intervals to identify unhealthy green sea turtles (Chelonia mydas). The Veterinary Journal 185: 299–304CrossRefPubMed
go back to reference Foley AM, Schroeder BA, Redlow AE, Fick-Child K, Teas WG (2005) Fibropapillomatosis in stranded green turtles (Chelonia mydas) from the eastern United States (1980–98): trends and association with environmental factors. Journal of Wildlife Disease 41: 29–41CrossRef Foley AM, Schroeder BA, Redlow AE, Fick-Child K, Teas WG (2005) Fibropapillomatosis in stranded green turtles (Chelonia mydas) from the eastern United States (1980–98): trends and association with environmental factors. Journal of Wildlife Disease 41: 29–41CrossRef
go back to reference Gama LR, Domit C, Broadhurst MK, Fuentes MPB, Millar RB (2016) Green turtle Chelonia mydas foraging ecology at 25°S in the western Atlantic: evidence to support a feeding model driving by intrinsic and extrinsic variability. Marine Ecology Progress Series 542: 209–219CrossRef Gama LR, Domit C, Broadhurst MK, Fuentes MPB, Millar RB (2016) Green turtle Chelonia mydas foraging ecology at 25°S in the western Atlantic: evidence to support a feeding model driving by intrinsic and extrinsic variability. Marine Ecology Progress Series 542: 209–219CrossRef
go back to reference Goldwasser P, Feldman J (1997) Association of serum albumin and mortality risk. Journal of Clinical Epidemiology 50: 693–703CrossRefPubMed Goldwasser P, Feldman J (1997) Association of serum albumin and mortality risk. Journal of Clinical Epidemiology 50: 693–703CrossRefPubMed
go back to reference Greenblatt RJ, Work TM, Dutton P, Sutton C, Spraker TR, Casey RN, Diez CE, Parker, D, St. Leger J, Balazs GH, Casey JW (2005) Geographic variation in marine turtle fibropapillomatosis. Journal of Zoo and Wildlife Medicine 36: 527–530CrossRefPubMed Greenblatt RJ, Work TM, Dutton P, Sutton C, Spraker TR, Casey RN, Diez CE, Parker, D, St. Leger J, Balazs GH, Casey JW (2005) Geographic variation in marine turtle fibropapillomatosis. Journal of Zoo and Wildlife Medicine 36: 527–530CrossRefPubMed
go back to reference Hamann M, Schäuble CS, Simon T, Evans S (2006) Demographic and health parameters of green sea turtle Chelonia mydas foraging in the Gulf of Carpentaria, Australia. Endangered Species Research 2: 81–88.CrossRef Hamann M, Schäuble CS, Simon T, Evans S (2006) Demographic and health parameters of green sea turtle Chelonia mydas foraging in the Gulf of Carpentaria, Australia. Endangered Species Research 2: 81–88.CrossRef
go back to reference Hasbún CR, Lawrence AJ, Naldo J, Samour JH, Al-Ghais SM (1998) Normal blood chemistry of free-living green sea turtles, Chelonia mydas, from the United Arab Emirates. Comparative Haematology International 8: 174–177CrossRef Hasbún CR, Lawrence AJ, Naldo J, Samour JH, Al-Ghais SM (1998) Normal blood chemistry of free-living green sea turtles, Chelonia mydas, from the United Arab Emirates. Comparative Haematology International 8: 174–177CrossRef
go back to reference Herbst L, Ene A, Su M, Desalle R, Lenz J (2004) Tumor outbreaks in marine turtles are not due to recent herpesvirus mutation. Current Biology 14: 697–699CrossRef Herbst L, Ene A, Su M, Desalle R, Lenz J (2004) Tumor outbreaks in marine turtles are not due to recent herpesvirus mutation. Current Biology 14: 697–699CrossRef
go back to reference Herbst LH, Jacobson ER (2003) Practical approaches for studying sea turtle health and disease. In: The Biology of Sea Turtles, Volume II, Lutz PL, Musick JA, Wyneken J (editors), Florida: CRC press, 385–410 Herbst LH, Jacobson ER (2003) Practical approaches for studying sea turtle health and disease. In: The Biology of Sea Turtles, Volume II, Lutz PL, Musick JA, Wyneken J (editors), Florida: CRC press, 385–410
go back to reference Herbst LH, Jacobson ER, Klein PA, Balazs GH, Moretti R, Brown T, Sundberg JP (1999) Comparative pathology and pathogenesis of spontaneous and experimentally induced fibropapillomas of green turtles (Chelonia mydas). Veterinary Pathology 36: 551–564CrossRefPubMed Herbst LH, Jacobson ER, Klein PA, Balazs GH, Moretti R, Brown T, Sundberg JP (1999) Comparative pathology and pathogenesis of spontaneous and experimentally induced fibropapillomas of green turtles (Chelonia mydas). Veterinary Pathology 36: 551–564CrossRefPubMed
go back to reference Jones K, Ariel E, Burgess G, Read M (2016) A review of fibropapillomatosis in green turtles (Chelonia mydas). Veterinary Journal 212: 48–57CrossRefPubMed Jones K, Ariel E, Burgess G, Read M (2016) A review of fibropapillomatosis in green turtles (Chelonia mydas). Veterinary Journal 212: 48–57CrossRefPubMed
go back to reference Kage-Karjian A, Norton TM, Krimer P, Groner M, Nelson SE, Gottdenker NL (2014) Factors influencing survivorship of rehabilitating green sea turtles (Chelonia mydas) with fibropapillomatosis. Journal of Zoo and Wildlife Medicine 45: 507–519CrossRef Kage-Karjian A, Norton TM, Krimer P, Groner M, Nelson SE, Gottdenker NL (2014) Factors influencing survivorship of rehabilitating green sea turtles (Chelonia mydas) with fibropapillomatosis. Journal of Zoo and Wildlife Medicine 45: 507–519CrossRef
go back to reference Keller JM, Balazs GH, Nielsen F, Rice M, Work TM, Jensen BA (2014) Investigating the potential role of persistent organic pollutants in Hawaiian green sea turtle fibropapillomatosis. Environmental Science & Technology 48: 7807–7816CrossRef Keller JM, Balazs GH, Nielsen F, Rice M, Work TM, Jensen BA (2014) Investigating the potential role of persistent organic pollutants in Hawaiian green sea turtle fibropapillomatosis. Environmental Science & Technology 48: 7807–7816CrossRef
go back to reference Kumar S, Stecher G, Tamura K (2016) MEGA 7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870–1874CrossRefPubMedPubMedCentral Kumar S, Stecher G, Tamura K (2016) MEGA 7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870–1874CrossRefPubMedPubMedCentral
go back to reference Labrada-Martagón V, Mendéz-Rodríguez LC, Gardner SC, Cruz-Escalona VH, Zenteno-Savín T (2010) Health indices of the green turtle (Chelonia mydas) along the Pacific coast of Baja California Sur, Mexico. II. Body condition index. Chelonian Conservation Biology 9: 173–183CrossRef Labrada-Martagón V, Mendéz-Rodríguez LC, Gardner SC, Cruz-Escalona VH, Zenteno-Savín T (2010) Health indices of the green turtle (Chelonia mydas) along the Pacific coast of Baja California Sur, Mexico. II. Body condition index. Chelonian Conservation Biology 9: 173–183CrossRef
go back to reference Lewbart GA, Hirschfeld M, Denkinger J, Vasco K, Guevara N, García J, Muñoz J, Lohmann KJ (2014) Blood gases, biochemistry, and hematology of Galapagos green turtle (Chlonia mydas). PloS ONE 9: e96487CrossRefPubMedPubMedCentral Lewbart GA, Hirschfeld M, Denkinger J, Vasco K, Guevara N, García J, Muñoz J, Lohmann KJ (2014) Blood gases, biochemistry, and hematology of Galapagos green turtle (Chlonia mydas). PloS ONE 9: e96487CrossRefPubMedPubMedCentral
go back to reference March DT, Vinette-Herrin K, Peters A, Ariel E, Blyde D, Hayward D, Christidis L, Kelaher BP (2018) Hematological and biochemical characteristics of stranded green sea turtles. Journal of Veterinary Diagnostic Investigation 30: 423–429CrossRefPubMedPubMedCentral March DT, Vinette-Herrin K, Peters A, Ariel E, Blyde D, Hayward D, Christidis L, Kelaher BP (2018) Hematological and biochemical characteristics of stranded green sea turtles. Journal of Veterinary Diagnostic Investigation 30: 423–429CrossRefPubMedPubMedCentral
go back to reference Masat RJ, Dessauer HC (1968). Plasma albumin in reptiles. Comparative Biochemistry and Physiology 25: 119–122CrossRefPubMed Masat RJ, Dessauer HC (1968). Plasma albumin in reptiles. Comparative Biochemistry and Physiology 25: 119–122CrossRefPubMed
go back to reference Monezi TA, Mehnert DU, Moura EMM, Muller NMG, Garrafa P, Matushima ER, Werneck MR, Borella MI (2016). Chelonid herpesvirus 5 in secretions and tumor tissues from Green turtles (Chelonia mydas) from Southeastern Brazil: a ten-year study. Veterinary Microbiology 186: 150–156CrossRefPubMed Monezi TA, Mehnert DU, Moura EMM, Muller NMG, Garrafa P, Matushima ER, Werneck MR, Borella MI (2016). Chelonid herpesvirus 5 in secretions and tumor tissues from Green turtles (Chelonia mydas) from Southeastern Brazil: a ten-year study. Veterinary Microbiology 186: 150–156CrossRefPubMed
go back to reference Morrison CL, Iwanowicz L, Work TM, Fahsbender E, Breitbart M, Adams C, Iwanowicz D, Sanders L, Ackermann M, Cornman RS (2018) Genomic evolution, recombination, and inter-strain diversity of chelonid alphaherpesvirus 5 from Florida and Hawaii green sea turtles with fibropapillomatosis. PeerJ 6: e4386. Doi: 10.7717/peerj.4386CrossRefPubMedPubMedCentral Morrison CL, Iwanowicz L, Work TM, Fahsbender E, Breitbart M, Adams C, Iwanowicz D, Sanders L, Ackermann M, Cornman RS (2018) Genomic evolution, recombination, and inter-strain diversity of chelonid alphaherpesvirus 5 from Florida and Hawaii green sea turtles with fibropapillomatosis. PeerJ 6: e4386. Doi: 10.7717/peerj.4386CrossRefPubMedPubMedCentral
go back to reference Naro-Maciel E, Le M, FitzSimmons N, Amato G (2008) Evolutionary relationships of marine turtles: A molecular phylogeny based on nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution 49: 659–662CrossRefPubMed Naro-Maciel E, Le M, FitzSimmons N, Amato G (2008) Evolutionary relationships of marine turtles: A molecular phylogeny based on nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution 49: 659–662CrossRefPubMed
go back to reference Page-Karjian A, Rivera S, Torres F, Diez C, Moore D, van Dam R, Brown C (2015) Baseline blood values for healthy free-ranging green sea turtles (Chelonia mydas) in Puerto Rico. Comparative Clinical Pathology 24: 567–573CrossRef Page-Karjian A, Rivera S, Torres F, Diez C, Moore D, van Dam R, Brown C (2015) Baseline blood values for healthy free-ranging green sea turtles (Chelonia mydas) in Puerto Rico. Comparative Clinical Pathology 24: 567–573CrossRef
go back to reference Patrício AR, Herbst LH, Duarte A, Vélez-Zuazo X, Loureiro NS, Pereira N, Tavares L, Toranzos GA (2012) Global phylogeography and evolution of chelonid fibropapilloma-associated herpesvirus. Journal of General Virology 93: 1035–1045CrossRefPubMed Patrício AR, Herbst LH, Duarte A, Vélez-Zuazo X, Loureiro NS, Pereira N, Tavares L, Toranzos GA (2012) Global phylogeography and evolution of chelonid fibropapilloma-associated herpesvirus. Journal of General Virology 93: 1035–1045CrossRefPubMed
go back to reference Proietti MC, Reisser JW, Kinas PG (2007) Avaliação preliminar da ocorrência de fibropapilomatose em tartarugas-verde (Chelonia mydas) incidentes na Reserva Biológica Marinha do Arvoredo. In Proceedings of the 12nd Congresso Latino-Americano de Ciências do Mar (COLACMAR)’, (AOCEANO: Florianópolis), pp 1–3 Proietti MC, Reisser JW, Kinas PG (2007) Avaliação preliminar da ocorrência de fibropapilomatose em tartarugas-verde (Chelonia mydas) incidentes na Reserva Biológica Marinha do Arvoredo. In Proceedings of the 12nd Congresso Latino-Americano de Ciências do Mar (COLACMAR)’, (AOCEANO: Florianópolis), pp 1–3
go back to reference Quackenbush SL, Casey RN, Murcek RJ, Paul TA, Work TM, Limpus CJ, Chaves A, duToit L, Perez JV, Aguirre AA, Spraker TR, Horrocks JA, Vermeer LA, Balasz GH, Casey JW (2001) Quantitative analysis of herpesvirus sequences from normal tissue and fibropapillomas of marine turtles with real-time PCR. Virology 287: 105–111CrossRefPubMed Quackenbush SL, Casey RN, Murcek RJ, Paul TA, Work TM, Limpus CJ, Chaves A, duToit L, Perez JV, Aguirre AA, Spraker TR, Horrocks JA, Vermeer LA, Balasz GH, Casey JW (2001) Quantitative analysis of herpesvirus sequences from normal tissue and fibropapillomas of marine turtles with real-time PCR. Virology 287: 105–111CrossRefPubMed
go back to reference Ramirez AC (2017) Investigation into Chelonid Alphaherpesvirus 5 infection and fibropapillomatosis in the Pacific green turtle (Chelonia mydas agassizii) and the olive Ridley turtle (Lepidochelys olivacea) in the Pacific of Costa Rica and Nicaragua. Dissertation at Faculties of Veterinary Medicine and Medicine of the Justus Liebig University Giessen. Ramirez AC (2017) Investigation into Chelonid Alphaherpesvirus 5 infection and fibropapillomatosis in the Pacific green turtle (Chelonia mydas agassizii) and the olive Ridley turtle (Lepidochelys olivacea) in the Pacific of Costa Rica and Nicaragua. Dissertation at Faculties of Veterinary Medicine and Medicine of the Justus Liebig University Giessen.
go back to reference Rodenbusch CR, Baptistotte C, Werneck MR, Pires TT, Melo MTD, Ataíde MW, Reis KDHL, Testa P, Alieve MM, Canal CW (2014) Fibropapillomatosis in green turtles Chelonia mydas in Brazil: characteristics of tumors and virus. Diseases of Aquatic Organisms 11: 207–217CrossRef Rodenbusch CR, Baptistotte C, Werneck MR, Pires TT, Melo MTD, Ataíde MW, Reis KDHL, Testa P, Alieve MM, Canal CW (2014) Fibropapillomatosis in green turtles Chelonia mydas in Brazil: characteristics of tumors and virus. Diseases of Aquatic Organisms 11: 207–217CrossRef
go back to reference Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425PubMed Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425PubMed
go back to reference Santos MRD, Martins AS, Baptistotte C, Work TM (2015) Health condition of juvenile green turtles in southeastern Brazil. Diseases of Aquatic Organisms 115: 193–201CrossRef Santos MRD, Martins AS, Baptistotte C, Work TM (2015) Health condition of juvenile green turtles in southeastern Brazil. Diseases of Aquatic Organisms 115: 193–201CrossRef
go back to reference Santos RG, Martins AS, Torezani E, Baptistotte C, Farias JN, Horta PA, Work TM, Balazs GH (2010) Relationship between fibropapillomatosis and environmental quality: a case study with Chelonia mydas off Brazil. Diseases of Aquatic Organisms 89: 87–95CrossRefPubMed Santos RG, Martins AS, Torezani E, Baptistotte C, Farias JN, Horta PA, Work TM, Balazs GH (2010) Relationship between fibropapillomatosis and environmental quality: a case study with Chelonia mydas off Brazil. Diseases of Aquatic Organisms 89: 87–95CrossRefPubMed
go back to reference Spotila JR (2004) Sea turtles: a complete guide to their biology, behavior, and conservation. 1st ed. Baltimore: The Johns Hopkins University Press and Oakwood Arts Spotila JR (2004) Sea turtles: a complete guide to their biology, behavior, and conservation. 1st ed. Baltimore: The Johns Hopkins University Press and Oakwood Arts
go back to reference Stacy NI, Allemann AR, Sayler KA (2011) Diagnostic hematology of reptiles. Clinics in Laboratory Medicine 31: 87–108CrossRefPubMed Stacy NI, Allemann AR, Sayler KA (2011) Diagnostic hematology of reptiles. Clinics in Laboratory Medicine 31: 87–108CrossRefPubMed
go back to reference Swimmer JY (2000) Biochemical responses to fibropapillomatosis and captivity in the green turtle. Journal of Wildlife Disease 36: 102–110CrossRef Swimmer JY (2000) Biochemical responses to fibropapillomatosis and captivity in the green turtle. Journal of Wildlife Disease 36: 102–110CrossRef
go back to reference Tagliolatto AB, Guimarães SM, Lobo-Hajdu G, Monteiro-Neto C (2016) Characterization of fibropapillomatosis in green turtles Chelonia mydas (Cheloniidae) captured in a foraging area in southeastern Brazil. Diseases of Aquatic Organisms 121: 233–240CrossRefPubMed Tagliolatto AB, Guimarães SM, Lobo-Hajdu G, Monteiro-Neto C (2016) Characterization of fibropapillomatosis in green turtles Chelonia mydas (Cheloniidae) captured in a foraging area in southeastern Brazil. Diseases of Aquatic Organisms 121: 233–240CrossRefPubMed
go back to reference Tonyushkina K, Nichols JA (2009) Glucose meters: a review of technical challenges to obtaining accurate results. Journal of Diabetes Science and Technology 3: 971–980CrossRefPubMedPubMedCentral Tonyushkina K, Nichols JA (2009) Glucose meters: a review of technical challenges to obtaining accurate results. Journal of Diabetes Science and Technology 3: 971–980CrossRefPubMedPubMedCentral
go back to reference Torezani E, Baptistotte C, Mendes SL, Barata PCR (2010) Juvenile green turtles (Chelonia mydas) in the effluent discharge channel of a steel plant, Espírito Santo, Brasil, 2000-2006. Journal of the Marine Biological Association of United Kingdom 90: 233–246CrossRef Torezani E, Baptistotte C, Mendes SL, Barata PCR (2010) Juvenile green turtles (Chelonia mydas) in the effluent discharge channel of a steel plant, Espírito Santo, Brasil, 2000-2006. Journal of the Marine Biological Association of United Kingdom 90: 233–246CrossRef
go back to reference Whiting SD, Guinea ML, Limpus CL, Fomiatti K (2007) Blood chemistry reference values for two ecologically distinct populations of foraging green turtles, eastern Indian Ocean. Comparative Clinical Pathology 16: 109–118CrossRef Whiting SD, Guinea ML, Limpus CL, Fomiatti K (2007) Blood chemistry reference values for two ecologically distinct populations of foraging green turtles, eastern Indian Ocean. Comparative Clinical Pathology 16: 109–118CrossRef
go back to reference Whyte MP, Walkenhorst DA, Fedde KN, Henthorn PS, Hill C (1996) Hypophosphatasia: levels of bone alkaline phosphatase immunoreactivity in serum reflect disease severity. The Journal of Clinical Endocrinology & Metabolism 81: 2142–2148 Whyte MP, Walkenhorst DA, Fedde KN, Henthorn PS, Hill C (1996) Hypophosphatasia: levels of bone alkaline phosphatase immunoreactivity in serum reflect disease severity. The Journal of Clinical Endocrinology & Metabolism 81: 2142–2148
go back to reference Work TM, Balazs GH (1999) Relating tumor score to hematology in green turtles with fibropapillomatosis in Hawaii. Journal of Wildlife Diseases 35:804–807CrossRefPubMed Work TM, Balazs GH (1999) Relating tumor score to hematology in green turtles with fibropapillomatosis in Hawaii. Journal of Wildlife Diseases 35:804–807CrossRefPubMed
go back to reference Work TM, Balazs GH, Rameyer RA, Morris RA (2004) Retrospective pathology survey of green turtles Chelonia mydas with fibropapillomatosis in the Hawaiian islands, 1993-2003. Diseases of Aquatic Organisms 62: 163–176CrossRefPubMed Work TM, Balazs GH, Rameyer RA, Morris RA (2004) Retrospective pathology survey of green turtles Chelonia mydas with fibropapillomatosis in the Hawaiian islands, 1993-2003. Diseases of Aquatic Organisms 62: 163–176CrossRefPubMed
go back to reference Work TM, Dagenais J, Balazs GH, Schettle N, Ackermann M (2015) Dynamics of virus shedding and in situ confirmation of Chelonid herpesvirus 5 in Hawaiian green turtles with fibropapillomatosis. Veterinary Pathology 52: 1195–1201CrossRefPubMed Work TM, Dagenais J, Balazs GH, Schettle N, Ackermann M (2015) Dynamics of virus shedding and in situ confirmation of Chelonid herpesvirus 5 in Hawaiian green turtles with fibropapillomatosis. Veterinary Pathology 52: 1195–1201CrossRefPubMed
go back to reference Zwarg T, Rossi S, Sanches TC, Cesar MO, Werneck MR, Matushima ER (2014) Hematological and histopathological evaluation of wildlife green turtles (Chelonia mydas) with and without fibropapilloma from the north coast of São Paulo state, Brazil. Pesquisa Veterinária Brasileira 34: 682–688CrossRef Zwarg T, Rossi S, Sanches TC, Cesar MO, Werneck MR, Matushima ER (2014) Hematological and histopathological evaluation of wildlife green turtles (Chelonia mydas) with and without fibropapilloma from the north coast of São Paulo state, Brazil. Pesquisa Veterinária Brasileira 34: 682–688CrossRef
Metadata
Title
Chelonid Alphaherpesvirus 5 DNA in Fibropapillomatosis-Affected Chelonia mydas
Authors
Isabela G. Domiciano
Matt K. Broadhurst
Camila Domit
Karina K. M. C. Flaiban
Daphne W. Goldberg
Juliana T. T. Fritzen
Ana Paula F. R. L. Bracarense
Publication date
01-06-2019
Publisher
Springer US
Published in
EcoHealth / Issue 2/2019
Print ISSN: 1612-9202
Electronic ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-019-01412-8

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