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First confirmed case of fibropapilloma in a leatherback turtle (Dermochelys coriacea)

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Patricia Huerta at consultor
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A. Alonso Aguirre at Colorado State University
A. Alonso Aguirre
Terry Spraker at Colorado State University
Terry Spraker
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i
NOAA TECHNICAL MEMORANDUM NMFS-SEFSC-477
PROCEEDINGS
OF THE
TWENTIETH ANNUAL SYMPOSIUM ON
SEA TURTLE
BIOLOGY AND CONSERVATION
29 February through 4 March 2000
Orlando, Florida, U.S.A.
Compilers:
Andrea Mosier
Allen Foley
Beth Brost
U.S. DEPARTMENT OF COMMERCE
Donald L. Evans, Secretary
NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION
Conrad C. Lautenbacker, Jr., Administrator
NATIONAL MARINE FISHERIES SERVICE
William T. Hogarth, Assistant Administrator for Fisheries
Technical Memoranda are used for documentation and timely communication of preliminary results,
interim reports, or special-purpose information, and have not received complete formal review, edito-
rial control or detailed editing.
193
Poster Presentations: Diseases, Veterinary Medicine, and Captive Care
Six Years of Observations on the Maintenance in Captivity of Sea Turtles
MARTHA HARFUSH AND ELPIDIO MARCELINO LÓPEZ REYES
Inst. Nal Pesca, Centro Mexicano de la Tortuga, Domicilio Conocido, Mazunte Tonameca, Correo Postal: Apartado Postal
16, Puerto Angel, Oaxaca Mexico 70902 (cmtharfu@angel.umar.mx)
Marine turtles have lived at the Centro Mexicano de la
Tortuga since the end of 1993. This has given us new
challenges to provide the optimum habitat conditions to
them. Day by day we learned more about hatchlings,
juveniles and adults of different species. In a way that was
not previously possible we have had the opportunity to
understand more about their food, water and environment
and to learn more about aspects of their biology such as
etiology. We have recently implemented a system of
tagging using chaquira (plastic colored balls) and tattoo.
The old system using steel tags was not liked by the turtles
who would bite them and often eat them.
We have also adapted the lodgings of some species
such as leatherback hatchlings. This species is very difficult
to maintain in captivity; its strength often causing
lacerations from the lodgings that sometimes resulted in
death. In addition, we have had the opportunity to study the
Table 1. Results in adaptation of sea turtles in captivity.
Species Name Common name Range of adaptation
to captivity
Lepidoche ly s olivacea olive ridley golfina Regular
Lepidoche ly s kempii Kemp 's ridley lora Good
Caretta caretta gigas Pacific loggerhead jabalina Good
Caretta ca retta caretta loggerhe ad cahuama Very goo d
Eretmoch elys imbricata hawksbi ll carey del golfo Very go od
E. imbricata bissa Pacific hawksbill carey Pacíí fico Very go od
Cheloni a mydas green turtle blanca o ver de Excellent
Chelonia agassizii black tur tle prieta Excellent
Dermochelys coriacea Leatherback laúúd o siete fi los Unknown
D. coria cea schlegelii Pacific leat her back laud del P acíífico No good
Natator depressus flatback kikila Australiana Not reported
feeding habits of several turtle species, carnivorous and
herbivores, as the Kemp’s and olive ridley and the black
turtle. Particularly their young stage. As a result we have
been able to formulate nutritious diets to suit their needs.
First Confirmed Case of Fibropapilloma in a Leatherback Turtle (Dermochelys coriacea)
PATRICIA HUERTA1, HUMBERTO PINEDA1, ALONSO AGUIRRE2, TERRY SPRAKER3, LAURA S ARTI1, AND ANA BARRAGÁN1
1Instituto Nacional de la Pesca, SEMARNAP, Pitágoras 1320, Col. Sta. Cruz Atoyac, México D.F. 03310
(pedlla@rocketmail.com)
2Wildlife Preservation Trust, Post Office Box 326, Grafton, Massachusetts 01519, USA
3Colorado Veterinary Diagnostic Laboratory, Colorado State University, Fort Collins, Colorado, USA
Fibropapillomatosis has been described as a major
epizootic disease that affects several sea turtle species. So
far, it has been reported for populations of green turtles
(Chelonia mydas), olive ridleys (Lepidochelys olivacea),
hawksbills (Eretmochelys imbricata) and flatbacks
(Natator depressus), but cases of leatherbacks
(Dermochelys coriacea) with fibropapillomas were
unknown. On December 16, 1997, an adult female
leatherback nested on Mexiquillo Beach, in the Pacific
coast of Mexico. During the routine examination of the
condition of the female, a tumor was found, which was
removed and fixed. The sample was sent to NMFSC-
Honolulu Lab in Hawaii, for analysis. The diagnosis
confirmed that it was a fibropapilloma in regression. This is
the first documented observation of fibropapilloma in
leatherback turtles. Given the current situation of the
Eastern Pacific leatherback population, which is drastically
depleted, the presence of fibropapillomas is cause of
concern. Since the prevalence of fibropapillomas in the
population is unknown, it is recommended to carefully
examine the nesting females in order to evaluate the
frequency of the disease and its possible impact.
LITERATURE C ITED
Harshbarger, J. C. 1974. Activities report registry of tumors in lower
animals, 1965-1973. Smithsonian Institute Press. Washington
D.C.
Ippen, R. 1972. Ein beitrag zu den spontantumoren bei Reptilien.
XIV Internationalen Symposium uber die Erkrankungen die
Zootiere. Akademie der Wissenschafter der DDR, Berlin.
... In man, low-grade fibrosarcomas (LGFs) encompass three well-recognized subtypes (low-grade fibromyxoid sarcoma; hyalinizing spindle cell tumour with giant collagen rosettes; sclerosing epithelioid fibrosarcoma) (Antonescu and Baren, 2004). In the present case, features that supported a diagnosis of PLGFMS were low cellularity, differentiated neoplastic spindle-shaped cells, low mitotic index and whorling in collagenized stroma with transition to fibromyxoid and inflamed areas (Jakowski and Wakely, 2008). Some histological features of the present case were analogous to those seen in canine maxillary well-differentiated fibrosarcoma, a histologically low-grade, yet biologically high-grade, Sarcoma in a Leatherback Sea Turtle fibroblastic tumour (Hendrick, 2017). ...
... In the present case, despite some histological commonalities with IPF, features of invasion, replacement and remarkable remodelling supported a diagnosis of PLGFMS (Jakowski and Wakely, 2008). We demonstrated ChHV5 genetic material by PCR analysis, increasing the few reports for this host species (Huerta et al., 2002;. Despite the fact that several tumour subtypes in sea turtles have been linked to ChHV5 (Work et al., 2004), a potential pathological role, including oncogenetic implications (Herbst et al., 1995;Lackovich et al., 1999), for the virus remains unknown. ...
... We demonstrated ChHV5 genetic material by PCR analysis, increasing the few reports for this host species (Huerta et al., 2002;. Despite the fact that several tumour subtypes in sea turtles have been linked to ChHV5 (Work et al., 2004), a potential pathological role, including oncogenetic implications (Herbst et al., 1995;Lackovich et al., 1999), for the virus remains unknown. However, the spatialetemporal coincidence in the present case may suggest an association. ...
Primary Multicentric Pulmonary Low-grade Fibromyxoid Sarcoma and Chelonid Alphaherpesvirus 5 Detection in a Leatherback Sea Turtle (Dermochelys coriacea)
Article
  • Feb 2019
  • J COMP PATHOL
We describe the gross, microscopical, histochemical and immunohistochemical features of a sclerosing pneumopathic disease process resembling primary multicentric pulmonary low-grade fibromyxoid sarcoma in a juvenile female leatherback sea turtle (Dermochelys coriacea). The animal was fresh, presented in good body condition and stranded dead in Aracaju, Sergipe state, Brazil, in September, 2017. Grossly, the lungs were enlarged bilaterally and the parenchyma was replaced by large, coalescing, white, firm masses that extended into the bronchi and bronchioles and to the pleura. Microscopically, these masses consisted of paucicellular populations of well-differentiated, spindle-shaped fibroblasts with low pleomorphism and low mitotic count, but tissue invasion. Abundant collagen in compact areas merged with peripheral fibromyxoid foci and inflamed stroma. Antibodies specific for cytokeratins AE1/AE3 and smooth muscle actin (SMA) labelled pneumocytes lining the remaining distorted alveoli and the hypertrophied and hyperplastic bronchial muscles, respectively. Tumour cells were negative for SMA; neither neoplastic nor normal tissues cross-reacted with antibodies specific for vimentin or Ki67. Chelonid alphaherpesvirus 5 (ChHV5) polymerase chain reaction analysis from formalin-fixed, paraffin wax-embedded lung tissue sections amplified a 450 base pair fragment of DNA-polymerase (UL30 region) that had 100% homology to sequences previously detected in green sea turtles (Chelonia mydas) on the Brazilian coast. Enterocolitis was a concomitant condition that likely caused morbidity in this case. These findings contribute to the body of knowledge on sea turtle health and expand the known geographical range for ChHV5 in the southern hemisphere.
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... Desde 1980, la FP ha aumentado drásticamente en diferentes regiones del mundo alcanzando una prevalencia del 50 % al 92 % . En México, la FP se ha reportado en tortuga lora (Lepidochelys kempii) en Rancho Nuevo, Tamaulipas (Barragán y Sarti, 1994), en tortuga laúd (Dermochelys coriacea) en la costa de Michoacán (Huerta et al., 2002), en tortugas golfinas en la costa de Colima y Oaxaca (Gámez et al., 2009;Reséndiz et al., 2015) y en tortugas verdes en Yucatán, Sinaloa, Veracruz y Baja California Sur (Maldonado-Gasca y Zapata, 2007;Mejía-Radillo et al., 2019;Suárez-Domínguez et al., 2020;Reséndiz et al., 2016;. Los casos de FP en tortugas marinas en México han aumentado durante las últimas décadas, tanto en sitios de alimentación (juveniles y adultos) como en playas de anidación (hembras adultas), lo que implica un alto riesgo de infección para las diferentes poblaciones y especies de tortugas que convergen en las costas mexicanas. ...
Primer registro de lesiones epiteliales sugerentes de Fibropapilomatosis en tortugas Golfinas (Lepidochelys olivacea) anidadoras en Baja California Sur, México
Article
Full-text available
  • May 2024
In this study, epithelial proliferative lesions were macros- copically identified and characterized in olive ridley turtles (Lepidochelys olivacea) nesting at El Suspiro beach, Baja California Sur, Mexico, during the 2022 nesting season. From June to December, 123 day and night surveys were carried out. During this period, 419 nesting female olive ridleys were observed, of which 8 presented epithelial proliferative lesions suggestive of fibropapillomatosis. These 8 organisms measured an average of 66.43 ± 3.13 cm in curved carapace length and presented a total of 51 lesions suggestive of fi- bropapillomatosis, with score 1, 2 and 3. The prevalence of turtles with these lesions was 0.019 %, the lesion incidence rate was 0.069, and the acumulative incidence was 0.019. The presence of fibropapillomatosis-like lesions in nesting olive ridley turtles in the region, represents an additional risk factor that may contribute to the populations decline of this species. The information generated supports the importance of including health assessments in sea turtle monitoring in Mexico, helps to strengthen management plans and develop new conservation strategies for these organisms and their habitats.
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... FP was first described in green turtles (Chelonia mydas) from Key West, Florida (Smith & Coates 1938). It has been reported among all seven species of sea turtles (Hashberger 1991, Limpus et al. 1993, Barragan & Sarti 1994, Alonso-Aguirre et al. 1999, D'Amato & Moraes 2000, Huerta et al. 2002 inhabiting coastal and shallow waters. Thus, it has a circumtropical distribution (Alonso-Aguirre & Lutz 2004). ...
What do we know about sea turtle fibropapillomatosis studies in the American continent? A bibliographic review
Article
Full-text available
  • Jul 2022
Fibropapillomatosis (FP) is a debilitating neoplastic infectious disease that affects sea turtles globally. Researchers on the American continent have generated valuable information about FP that can serve as the current source of biological knowledge on the disease, but this information is scattered throughout many scientific journals, books, thesis, and conference proceedings. Through a systematic literature review, the present study intends to summarize the current state of knowledge available on the American continent and highlight the knowledge gaps regarding FP in sea turtles. We reviewed 192 studies published from 1938 to 2021 performed on the American continent. The maximum annual number of publications occurred in 2019 with 15 publications, and there is an increasing trend in studies published over the past 25 years. One hundred thirty studies were performed in North America, 43 in South America, 14 in the Caribbean region, and 5 in Central America. The USA, Brazil, and Mexico were the most productive countries for FP research. The main topics addressed were pathological findings, records/incidences of FP, and molecular characterization. The most studied species with FP is the green turtle (Chelonia mydas). Our results show a lack of geographical information about FP, particularly in the Central American region and the Pacific coast of South America. While there has been a significant increase in FP knowledge in the last two decades, most of the studies focused on pathological findings, while viral replication and transmission of this disease remains unknown, highlighting the need for studies that describe immune characteristics, stressful environmental conditions, or disorders in blood chemical values in organisms affected by FP.
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... In Mexico, while the presence of FP has widely been reported in the eastern Pacific (Huerta et al. 2002;Vivaldo et al. 2009), Gulf of Mexico (Barragan and Sarti 1994) and Caribbean (Maldonado-Gasca and Zapata-Rosales 2007), ChHV5 has, however, only been documented in the southern Pacific coast (Quackenbush et al. 2001). In the Baja California Peninsula, herpesvirus-like particles revealed by transmission electron microscopy from a FP tumor were visualized (Reséndiz et al. 2016) presenting the first preliminary evidence of ChHV5 in the area. ...
Genetic Analysis of Chelonid Herpesvirus 5 in Marine Turtles from Baja California Peninsula
Article
  • Jul 2020
The Chelonid herpesvirus 5 (ChHV5) is the primary etiological agent associated with fibropapillomatosis (FP), a neoplastic disease in marine turtles. In this study, we report for the first time ChHV5 in marine turtles and a leech from Baja California Peninsula. Eighty-seven black, olive or loggerhead turtle species, one FP tumor and five leeches were analyzed. The tumor sample from an olive, a skin sample from a black and a leech resulted positive of ChHV5 for conventional PCR. Two viral variants were identified and grouped within the Eastern Pacific phylogenetic group, suggesting a possible flow of the virus in this region.
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... mydas) from Key West, Florida (Smith and Coates 1938). Since then, FP-tumor lesions have been described in loggerhead (Harshbarger 1991;Mascarenhas and Iverson 2008;Page-Karjian et al. 2015;Rossi et al. 2015), Kemp's ridley (Lepidochelys kempii; Barragan and Sarti 1994), hawksbill (D' Amato and Moraes-Neto 2000), olive ridley (Aguirre et al. 1999), flatback (Natator depressus; Limpus et al. 1993), and leatherback (Huerta et al. 2002) turtles. FP is most frequently reported in sea turtles at coastal feeding grounds, areas often impacted by human activities (e.g., land use, high nitrogen concentration, and onshore sewage disposal in turtle feeding areas), leading to a eutrophication process through delivery and retention of nitrogen in coastal waters (Aguirre and Lutz 2004;Ene et al. 2005;Van Houtan et al. 2010). ...
Stranded Marine Turtles in Northeastern Brazil: Incidence and Spatial–Temporal Distribution of Fibropapillomatosis
Article
Full-text available
  • Oct 2019
Fibropapillomatosis is a threat to the survival of marine turtles, especially green turtles; therefore, studies on this neoplastic disease are considered a conservation priority. Our goal was to characterize the incidence and spatial–temporal distribution of fibropapillomatosis in the Potiguar Basin, Rio Grande do Norte and Ceará states, Brazil. This study was based on data obtained during daily observations by a beach monitoring program from 2012 to 2015. A total of 2688 marine turtles, comprising the 5 species that occur in the Brazilian coast, were observed; 604 of the 610 individuals that presented fibropapillomatosis tumors were green turtles ( Chelonia mydas). During the study period, we identified an increase in relative fibropapillomatosis frequency from 13.16% (2012) to 35.29% (2015), with a yearly peak in strandings between October and December. Fibropapillomatosis tumors were classified according to anatomical distribution, size, and the Southwest Atlantic Fibropapillomatosis Score (e.g., mild, moderate, and severe). The total number of tumors varied from 1 to 67; most were classified as size B and mild and were located mainly on the forelimbs and neck (49.63 and 25.95%, respectively). Our study shows the need to implement mitigation measures to promote sea turtle conservation in the Potiguar Basin, an important area for marine turtles in Brazil.
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... The neoplastic disease, fibropapillomatosis (FP) is present in sea turtles worldwide (Quackenbush et al., 1998;Lackovich et al., 1999), primarily affecting green sea turtles (Chelonia mydas; Smith & Coates, 1938) and to a lesser extent loggerhead (Caretta caretta; Harshbarger, 1991), olive ridley (Lepidochelys olivacea; Aguirre et al., 1999), Kemp's ridley (Lepidochelys kempii; Barragan & Sarti, 1994), hawksbill (Eretmochelys imbricate; D 'Amato & Moraes-Neto, 2000) and leatherback (Dermochelys coriacea; Huerta et al., 2002) sea turtles. FP manifests as external fibropapillomas or fibromas and internal fibromas, myxofibromas, or fibrosarcomas of low grade malignancy (Herbst, 1994) and when severe, can lead to immunosuppression (Work et al., 2001), secondary bacterial infections (Work et al., 2003), and death (Work et al., 2004). ...
Genomic evolution, recombination, and inter-strain diversity of chelonid alphaherpesvirus 5 from Florida and Hawaii green sea turtles with fibropapillomatosis
Article
Full-text available
  • Feb 2018
Chelonid alphaherpesvirus 5 (ChHV5) is a herpesvirus associated with fibropapillomatosis (FP) in sea turtles worldwide. Single-locus typing has previously shown differentiation between Atlantic and Pacific strains of this virus, with low variation within each geographic clade. However, a lack of multi-locus genomic sequence data hinders understanding of the rate and mechanisms of ChHV5 evolutionary divergence, as well as how these genomic changes may contribute to differences in disease manifestation. To assess genomic variation in ChHV5 among five Hawaii and three Florida green sea turtles, we used high-throughput short-read sequencing of long-range PCR products amplified from tumor tissue using primers designed from the single available ChHV5 reference genome from a Hawaii green sea turtle. This strategy recovered sequence data from both geographic regions for approximately 75% of the predicted ChHV5 coding sequences. The average nucleotide divergence between geographic populations was 1.5%; most of the substitutions were fixed differences between regions. Protein divergence was generally low (average 0.08%), and ranged between 0 and 5.3%. Several atypical genes originally identified and annotated in the reference genome were confirmed in ChHV5 genomes from both geographic locations. Unambiguous recombination events between geographic regions were identified, and clustering of private alleles suggests the prevalence of recombination in the evolutionary history of ChHV5. This study significantly increased the amount of sequence data available from ChHV5 strains, enabling informed selection of loci for future population genetic and natural history studies, and suggesting the (possibly latent) co-infection of individuals by well-differentiated geographic variants.
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... Fibropapillomatosis (FP) (Figure 14.73), tumorous growth, of marine turtles affects primarily the green turtle (Chelonia mydas), but has also been reported from other turtles such as loggerhead (Caretta caretta), olive ridley (Lepidochelys olivacea), hawksbill (Eretmochelys imbricata), leatherback (Dermochelys coriacea), and flatback (Natator depressus) (Huerta et al. 2002). Foley et al. (2005) examined data collected by the U.S. Sea Turtle Stranding and Salvage Network based on 4,328 dead or debilitated green turtles in the eastern half of the United States from Massachusetts to Texas from 1980 to 1998 and found that 22.6 % (682/3,016) of the turtles in the southern half of Florida had tumors. ...
Diseases and Mortalities of Fishes and Other Animals in The Gulf of Mexico
Chapter
Full-text available
  • Jun 2017
Most mortality results from natural causes including red tide which is primarily restricted to West Florida and cold-kills that have greater influence in the warmer regions of South Texas and South Florida, but also kill a significant amount of fish and other animals in the northern Gulf. With the exception of red tide and other harmful algal blooms, the health of the Gulf has not been systematically studied. Mexico has only recently started to evaluate the health of its coastlines. Mortalities of marine animals, particularly fishes, in the Gulf caused by natural and anthropogenic events seem to interact with infectious disease agents and noninfectious diseases, but the mortalities are often attributed to the disease agents alone. “Events” that cause mortalities include eutrophication; hypoxia; algal blooms; temperature, salinity, and weather extremes; and chemical and sediment pollution. “Diseases” include those caused by infectious agents, parasites, neoplasms, and developmental abnormalities. Interactions of the effects of diseases and stressful events are considered important but little investigated.
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Adaptive evolution of major histocompatibility complex class I immune genes and disease associations in coastal juvenile sea turtles
Article
Full-text available
  • Feb 2022
Characterizing polymorphism at the major histocompatibility complex (MHC) genes is key to understanding the vertebrate immune response to disease. Despite being globally afflicted by the infectious tumour disease fibropapillomatosis (FP), immunogenetic variation in sea turtles is minimally explored. We sequenced the α 1 peptide-binding region of MHC class I genes (162 bp) from 268 juvenile green ( Chelonia mydas ) and 88 loggerhead ( Caretta caretta ) sea turtles in Florida, USA. We recovered extensive variation (116 alleles) and trans-species polymorphism. Supertyping analysis uncovered three functional MHC supertypes corresponding to the three well-supported clades in the phylogeny. We found significant evidence of positive selection at seven amino acid sites in the class I exon. Random forest modelling and risk ratio analysis of Ch. mydas alleles uncovered one allele weakly associated with smooth FP tumour texture, which may be associated with disease outcome. Our study represents the first characterization of MHC class I diversity in Ch. mydas and the largest sample of sea turtles used to date in any study of adaptive genetic variation, revealing tremendous genetic variation and high adaptive potential to viral pathogen threats. The novel associations we identified between MHC diversity and FP outcomes in sea turtles further highlight the importance of evaluating genetic predictors of disease, including MHC and other functional markers.
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Fibropapillomatosis in immature Green Turtles (Chelonia mydas) from the Gulf of Venezuela
Article
Full-text available
  • Dec 2021
Fibropapillomatosis (FP) is affecting multiple marine turtle (MT) species worldwide. In Venezuela, the understanding about this neoplastic condition is still in early stage. Hence, this paper aims to assess the occurrence and frequency of FP in green turtles (GT) in the Gulf of Venezuela (GV). Herein, it was compiled and analyzed the reports in the database of the NGO ‘Grupo de Trabajo en Tortugas Marinas del Golfo de Venezuela’, which includes all records of stranded MT in the GV from 2000 to 2011. Between 2000 and 2006, in the GV only 2 cases of FP in MT had been reported (1.71 % of total records). Subsequently, between 2008 and 2011, encounters of FP were more frequent; resulting in a total of 7 immature GT (2.93 % of the records) documented showing large masses or skin tumors in various parts of the body. The most affected area of the MT’s body was neck and venous sinus (37.50 %), followed by the anterior flippers (18.75 %), plastron (18.75 %), posterior region (cloaca 18.75 %) and lastly, the eyes (6.25 %). All individuals presented two or more body areas with FP. Although a correlation between the presence of FP and environmental factors observed in the study area was not assessed, the turtles evaluated came from coastal waters with high levels of eutrophication, habitat degradation, and pollution. It is necessary to monitor the occurrence of this disease and the environmental factors that may negatively affect the survival of MT populations in the GV.
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Genotype data not consistent with clonal transmission of sea turtle fibropapillomatosis or goldfish schwannoma
Article
Full-text available
  • Sep 2021
Recent discoveries of transmissible cancers in multiple bivalve species suggest that direct transmission of cancer cells within species may be more common than previously thought, particularly in aquatic environments. Fibropapillomatosis occurs with high prevalence in green sea turtles (Chelonia mydas) and the geographic range of disease has increased since fibropapillomatosis was first reported in this species. Widespread incidence of schwannomas, benign tumours of Schwann cell origin, reported in aquarium-bred goldfish (Carassius auratus), suggest an infectious aetiology. We investigated the hypothesis that cancers in these species arise by clonal transmission of cancer cells. Through analysis of polymorphic microsatellite alleles, we demonstrate concordance of host and tumour genotypes in diseased animals. These results imply that the tumours examined arose from independent oncogenic transformation of host tissue and were not clonally transmitted. Further, failure to experimentally transmit goldfish schwannoma via water exposure or inoculation suggest that this disease is unlikely to have an infectious aetiology.
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