First report of fibropapillomatosis (FP) and Chelonid alphaherpesvirus 5 (ChHV5) in a green sea turtle (Chelonia mydas) from the historically fibropapillomatosis-free Fernando de Noronha Archipelago, Northeastern Brazil

Authors

  • Marco Aurélio Gattamorta Universidade de São Paulo, Grupo de Pesquisa sobre Fibropapilomatose em Tartarugas Marinhas ; Instituto Federal de São Paulo https://orcid.org/0000-0001-9618-9466
  • Simone Almeida Gavilan Universidade Federal do Rio Grande do Norte, Departamento de Morfologia, Laboratório de Morfofisiologia de Vertebrados ; Universidade do Estado do Rio Grande do Norte, Projeto Cetáceos da Costa Branca https://orcid.org/0000-0003-1163-9822
  • Flavio José Lima da Silva Universidade do Estado do Rio Grande do Norte, Projeto Cetáceos da Costa Branca ; Universidade do Estado do Rio Grande do Norte, Programa de Pós-Graduação em Ciências Naturais, Projeto Golfinho Rotador https://orcid.org/0000-0002-6521-9367
  • Roberta Ramblas Zamana Universidade de São Paulo, Grupo de Pesquisa sobre Fibropapilomatose em Tartarugas Marinhas ; Universidade de São Paulo, Faculdade de Medicina Veterinária e Zootecnia, Departamento de Patologia, Laboratório de Patologia Comparada de Animais Selvagens https://orcid.org/0000-0002-4422-321X
  • Fabiola Eloisa Setim Universidade de São Paulo, Grupo de Pesquisa sobre Fibropapilomatose em Tartarugas Marinhas ; Fundação Projeto Tamar https://orcid.org/0000-0001-6532-694X
  • Silmara Rossi Universidade Federal do Rio Grande do Norte, Departamento de Morfologia, Laboratório de Morfofisiologia de Vertebrados https://orcid.org/0000-0003-0281-7236
  • Daniel Solon Dias de Farias Universidade Federal do Rio Grande do Norte, Departamento de Morfologia, Laboratório de Morfofisiologia de Vertebrados ; Universidade do Estado do Rio Grande do Norte, Projeto Cetáceos da Costa Branca https://orcid.org/0000-0002-5923-8625
  • Radan Elvis Matias de Oliveira Universidade Federal do Rio Grande do Norte, Departamento de Morfologia, Laboratório de Morfofisiologia de Vertebrados ; Universidade do Estado do Rio Grande do Norte, Projeto Cetáceos da Costa Branca https://orcid.org/0000-0002-0370-4447
  • Augusto Carlos da Boaviagem Freire Universidade do Estado do Rio Grande do Norte, Projeto Cetáceos da Costa Branca https://orcid.org/0000-0003-1705-2096
  • Armando José Barsante Santos Florida State University, Marine Turtle Research, Ecology and Conservation Group, Earth, Ocean and Atmospheric Science https://orcid.org/0000-0003-0696-329X
  • Paulo Hunold Lara Fundação Projeto Tamar https://orcid.org/0000-0001-8669-7272
  • Eliana Reiko Matushima Universidade de São Paulo, Grupo de Pesquisa sobre Fibropapilomatose em Tartarugas Marinhas ; Universidade de São Paulo, Faculdade de Medicina Veterinária e Zootecnia, Departamento de Patologia, Laboratório de Patologia Comparada de Animais Selvagens https://orcid.org/0000-0003-2526-7601

DOI:

https://doi.org/10.11606/issn.1678-4456.bjvras.2022.181776

Keywords:

Alphaherpesvirus, Fibropapilloma, Brazilian Atlantic coast, Fernando de Noronha Archipelago, Marine turtles, Tumors

Abstract

Fibropapillomatosis (FP) is an infectious disease caused by Chelonid alphaherpesvirus 5 (ChHV5). Nevertheless, its clinical manifestations are considered multifactorial. Due to its relevance, FP is currently monitored in sea turtle populations in the United States, Australia, Caribbean, and Brazil. Between 2000 and 2020, the TAMAR Project/ TAMAR Project Foundation analyzed the prevalence of FP in nine states and oceanic islands along the Brazilian coast, including Fernando de Noronha Archipelago (FNA), a historically FP-free area. A total of 4,435 green sea turtles (Chelonia mydas) were monitored from 2010 to 2016. Additionally, in 2012 and 2014, 43 FP-free skin samples were analyzed for ChHV5 using a qualitative PCR for the UL30 polymerase (pol) sequence. In 2015, a bilateral ocular nodule characterized as an FP tumor was reported in one of the monitored individuals undergoing rehabilitation. Tissue samples were collected following surgical removal of the tumor. Characterization of a 454 bp UL30 polymerase gene revealed a ChHV5 sequence previously reported in other areas of the Atlantic Brazilian coast. In the years following this finding from January 2017 to March 2020, a total of 360 C. mydas were monitored in the same area and no FP tumors were detected. This is the first report of FP and the first detection of ChHV5 in FNA, a finding of great concern considering this site’s historical absence of FP occurrence. This study highlights the importance of monitoring this disease in historically FP-free areas of the Brazilian Atlantic coast.

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References

Ackermann M, Koriabine M, Hartmann-Fritsch F, de Jong PJ, Lewis TD, Schetle N, Work TM, Dagenais J, Balazs GH, Leong JA. The genome of chelonid herpesvirus 5 harbors atypical genes. PLoS One. 2012;7(10):e46623. http://dx.doi.org/10.1371/journal.pone.0046623. PMid:23056373.

Alfaro-Núñez A, Bertelsen MF, Bojesen AM, Rasmussen I, Zepeda-Mendoza L, Olsen MT, Gilbert MTP. Global distribution of Chelonia fibropapilloma-associated herpesvirus among clinically healthy sea turtles. BMC Evol Biol. 2014;14(1):206. http://dx.doi.org/10.1186/s12862-014-0206-z. PMid:25342462.

Alfaro-Núñez A, Gilbert MTP. Validation of a sensitive PCR assay for the detection of Chelonid fibropapillomaassociated herpesvirus in latent turtle infections. J Virol Methods. 2014;206:38-41. http://dx.doi.org/10.1016/j.jviromet.2014.05.019. PMid:24882497.

Baptistotte C. Fibropapillomatosis in sea turtles from South America – Brazil, Uruguay, and Argentina. In: Hargrove S, Work T, Brunson S, Foley AM, Balazs G, editors. Fibropapillomatosis: global status, trends, and population impacts. Proceedings of 2015 Summit on fibropapillomatosis: global status, trends, and population impacts; 2015 Jun 11- 14; Honolulu, HI. Washington: US Dep Commer; 2016. p. 22-5. (NOAA Tech Memo, NOAA-TM-NMFS-PIFSC-54). http://dx.doi.org/10.7289/V5/TM-PIFSC-54.

Chaves A, Aguirre AA, Blanco-Peña K, Moreira-Soto A, Monge O, Torres AM, Soto-Rivas JL, Lu Y, Chacón D, Fonseca L, Jiménez M, Gutiérrez-Espeleta G, Lierz M. Examining the role of transmission of Chelonid Alphaherpesvirus 5. EcoHealth. 2017;14(3):530-41. http://dx.doi.org/10.1007/s10393-017-1248-7. PMid:28512730.

Díaz-Delgado J, Gomes-Borges JC, Silveira AM, EinhardtVergara J, Groch KR, Cirqueira CS, Sansone M, Gattamorta MA, Matushima ER, Catão-Dias JL. Primary multicentric pulmonary low-grade fibromyxoid sarcoma and Chelonida Alphaherpesvirus 5 detection in a Leatherback sea turtle (Dermochelys coriacea). J Comp Pathol. 2019;68:1-7. http://dx.doi.org/10.1016/j.jcpa.2019.02.001.

Domiciano IG, Broadhurst MK, Domit C, Flaiban KKMC, Goldberg DW, Fritzen JTT, Bracarense APFRL. Chelonid alphaherpesvirus 5 DNA in fibropapillomatosis-affected Chelonia mydas. EcoHealth. 2019;16(2):248-59. http://dx.doi.org/10.1007/s10393-019-01412-8. PMid:31124021.

Foley AM, Schroeder BA, Redlow AE, Fick-Child KJ, Teas WG. Fibropapillomatosis in stranded green turtles (Chelonia mydas) from the eastern United States (1980–98): trends and associations with environmental factors. J Wildl Dis. 2005;41(1):29-41. http://dx.doi.org/10.7589/0090-3558-41.1.29. PMid:15827208.

Garla RC, Chapman DD, Shivji MS, Wetherbee, BM, Amorim AF. Habitat of juvenile Caribbean reef sharks Carcharhinus perezi, at two oceanic insular marine protected areas in the southwestern Atlantic Ocean: Fernando de Noronha Archipelago and Atol das Rocas, Brazil. Fisheries Research. 2006;81(2-3):236-241. http://dx.doi.org/10.1016/j.fishres.2006.07.003.

Greenblatt RJ, Work TM, Balazs GH, Sutton CA, Casey RN, Casey JW. The Ozobranchus leech is a candidate mechanical vector for the fibropapilloma associated turtle herpesvirus found latently infecting skin tumors on Hawaiian green turtles (Chelonia mydas). Virology. 2004;321(1):101-10. http://dx.doi.org/10.1016/j.virol.2003.12.026. PMid:15033569.

Herbst LH, Jacobson ER, Moretti R, Brown T, Sundberg JP, Klein PA. Experimental transmission of green turtle fibropapillomatosis using cell-free tumor extracts. Dis Aquat Organ. 1995;22:1-12. http://dx.doi.org/10.3354/dao022001.

Herbst LH. Fibropapillomatosis of marine turtles. Annu Rev Fish Dis. 1994;4:389-425. http://dx.doi.org/10.1016/0959-8030(94)90037-X.

Jones K, Burgess G, Budd AM, Huerlimann R, Mashkour N, Ariel E. Molecular evidence for horizontal transmission of chelonid alphaherpesvirus 5 at green turtle (Chelonia mydas) foraging grounds in Queensland, Australia. PLoS One. 2020;15(1):e0227268. http://dx.doi.org/10.1371/journal.pone.0227268. PMid:31917785.

Krafft AE, Russell KL, Hawksworth AW, McCall S, Irvine M, Daum LT, Connoly JL, Reid AH, Gaydos JC, Taubenberger JK. Evaluation of PCR testing of ethanol-fixed nasal swab specimens as an augmented surveillance strategy for influenza virus and adenovirus identification. J Clin Microbiol. 2005;43(4):1768-75. http://dx.doi.org/10.1128/JCM.43.4.1768-1775.2005. PMid:15814997.

Lackovich JK, Brown DR, Homer BL, Garber RL, Mader DR, Moretti RH, Patterson AD, Herbst LH, Oros J, Jacobson ER, Curry SS, Klein PA. Association of herpesvirus with fibropapillomatosis of the green turtle Chelonia mydas and the loggerhead turtle Caretta caretta in Florida. Dis Aquat Organ. 1999;37(2):89-97. http://dx.doi.org/10.3354/dao037089. PMid:10494499.

Landsberg JH, Balazs GH, Steidinger KA, Baden DG, Work TM, Russell DJ. 1999. The potential role of natural tumor promoters in marine turtle fibropapillomatosis. J Aquat Anim Health. 1990;11(3):199-210. http://dx.doi.org/10.1577/1548-8667(1999)0112.0.CO;2.

Marcovaldi MA, Marcovaldi GG. Marine turles of Brazil: the history and structure of Projeto TAMAR-IBAMA. Biol Conserv. 1999;91(1):35-41. http://dx.doi.org/10.1016/S0006-207(99)00043-9.

Monezi TA, Mehnert DU, Moura EMM, Muller NM, Garrafa P, Matushima ER, Werneck MR, Borella MI. Chelonid herpesvirus 5 in secretions and tumor tissues form green turtles (Chelonia mydas) from Southeastern Brazil: a tenyear study. Vet Microbiol. 2016;186:150-6. http://dx.doi.org/10.1016/j.vetmic.2016.02.020. PMid:27016769.

Patricio AR, Herbst LH, Duarte A, Vélez-Zuazo X, Santos Loureiro N, Pereira N, Tavares L, Toranzos GA. Global phylogeography and evolution of chelonid fibropapillomaassociated herpesvirus. J Gen Virol. 2012; 93:1035-45. https://doi.org/10.1099/vir.0.038950-0. PMID: 22258862.

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, Balazs GH, Casey JW. Quantitative analysis of herpesvirus sequences from normal tissue and fibropapillomas of marine turtles with Real-Time PCR. Virology. 2001;287(1):105-11. http://dx.doi.org/10.1006/viro.2001.1023. PMid:11504546.

Quackenbush SL, Work TM, Balazs GH, Casey RN, Rovnak J, Chaves A, DuToit L, Baines JD, Parrish CR, Bowser PR, Casey JW. Three closely related herpesviruses are associated with fibropapillomatosis in marine turtles. Virology. 1998;246(2):392-9. http://dx.doi.org/10.1006/viro.1998.9207. PMid:9657957.

Rodenbusch CR, Baptistotte C, Werneck MR, Pires TT, Melo MTD, Ataíde MW, Reis KDHL, Testa P, Alieve MM, Canal CW. Fibropapillomatosis in green turtles Chelonia mydas in Brazil: characteristics of tumors and virus. Dis Aquat Organ. 2014;111(3):207-17. http://dx.doi.org/10.3354/dao02782. PMid:25320033.

Rossi S, Sánchez-Sarmiento AM, Vanstreels RET, Santos RG, Prioste FES, Gattamorta MA. Challenges in Evaluating the Severity of Fibropapillomatosis: A Proposal for Objective Index and Score System for Green Sea Turtles (Chelonia mydas) in Brazil. PLoS ONE. 2016;11(12):e0167632. https://doi.org/10.1371/journal.pone.0167632. PMID: 27936118.

Rossi S, Zamana RR, Andrade-Santos PP, Bomfim AC, de Farias DS, Freite ACB, Oliveira RM, Gattamorta MA, Matushima ER, Pires JML, Sacristán C, Silva-Júnior ES, Silva FJL, Gavilan AS. Visceral neoplasms and Chelonid alphaherpesvirus 5 in green turtles with fibropapillomatosis. Arch Vet Sci. 2021;26(1):63-79. http://dx.doi.org/10.5380/avs.v26i1.76435.

Santos RG, Martins AS, Torezani E, Baptistotte C, Farias JN, Horta PA, Work TM, Balazs GH. Relationship between fibropapillomatosis and environmental quality: a case study with Chelonia mydas off Brazil. Dis Aquat Organ. 2010;89(1):87-95. http://dx.doi.org/10.3354/dao02178. PMid:20391916.

Silva CC, Klein RD, Barcarolli IF, Bianchini A. Metal contamination as a possible etiology of fibropapillomatosis in juvenile female green sea turtles Chelonia mydas form the southern Atlantic Ocean. Aquat Toxicol. 2016;170:42- 51. http://dx.doi.org/10.1016/j.aquatox.2015.11.007. PMid:26615366.

Smith GM, Coates CW. Fibro-epithelial growths of the skin in large marine turtles Chelonia mydas (Linnaeus). Zool NY. 1938;23(4):93-8. http://dx.doi.org/10.5962/p.203654.

Van Houtan KS, Hargrove SK, Balazs GH. Land use, macroalgae, and a tumor-forming disease in marine turtles. PLoS One. 2010;5(9):e12900. http://dx.doi.org/10.1371/journal.pone.0012900. PMid:20927370.

Work TM, Dagenais J, Balazs GH, Schettle N, Ackermann M. Dynamics of virus shedding and in situ confirmation of chelonid herpesvirus 5 in Hawaiian green turtles with fibropapillomatosis. Vet Pathol. 2015;52(6):1195-201. http://dx.doi.org/10.1177/0300985814560236. PMid:25445320.

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Published

2022-03-17

Issue

Vol. 59 (2022)

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CASE REPORT

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How to Cite

1.
Gattamorta MA, Gavilan SA, Silva FJL da, Zamana RR, Setim FE, Rossi S, et al. First report of fibropapillomatosis (FP) and Chelonid alphaherpesvirus 5 (ChHV5) in a green sea turtle (Chelonia mydas) from the historically fibropapillomatosis-free Fernando de Noronha Archipelago, Northeastern Brazil. Braz. J. Vet. Res. Anim. Sci. [Internet]. 2022 Mar. 17 [cited 2024 Dec. 27];59:e181776. Available from: https://revistas.usp.br/bjvras/article/view/181776