Research

20 pages, 3504 KiB

Open AccessEditor’s ChoiceArticle

Fibropapillomatosis and Chelonid Alphaherpesvirus 5 Infection in Kemp’s Ridley Sea Turtles (Lepidochelys kempii)

by Annie Page-Karjian, Liam Whitmore, Brian A. Stacy, Justin R. Perrault, Jessica A. Farrell, Donna J. Shaver, J. Shelby Walker, Hilary R. Frandsen, Elina Rantonen, Craig A. Harms, Terry M. Norton, Charles Innis, Kelsey Yetsko and David J. Duffy

Animals 2021, 11(11), 3076; https://doi.org/10.3390/ani11113076 - 28 Oct 2021

Cited by 4 | Viewed by 4553

Abstract

Fibropapillomatosis (FP), a debilitating, infectious neoplastic disease, is rarely reported in endangered Kemp’s ridley sea turtles (Lepidochelys kempii). With this study, we describe FP and the associated chelonid alphaherpesvirus 5 (ChHV5) in Kemp’s ridley turtles encountered in the United States during [...] Read more.

Fibropapillomatosis (FP), a debilitating, infectious neoplastic disease, is rarely reported in endangered Kemp’s ridley sea turtles (Lepidochelys kempii). With this study, we describe FP and the associated chelonid alphaherpesvirus 5 (ChHV5) in Kemp’s ridley turtles encountered in the United States during 2006–2020. Analysis of 22 case reports of Kemp’s ridley turtles with FP revealed that while the disease was mild in most cases, 54.5% were adult turtles, a reproductively valuable age class whose survival is a priority for population recovery. Of 51 blood samples from tumor-free turtles and 12 tumor samples from turtles with FP, 7.8% and 91.7%, respectively, tested positive for ChHV5 DNA via quantitative polymerase chain reaction (qPCR). Viral genome shotgun sequencing and phylogenetic analysis of six tumor samples show that ChHV5 sequences in Kemp’s ridley turtles encountered in the Gulf of Mexico and northwestern Atlantic cluster with ChHV5 sequences identified in green (Chelonia mydas) and loggerhead (Caretta caretta) sea turtles from Hawaii, the southwestern Atlantic Ocean, and the Caribbean. Results suggest an interspecific, spatiotemporal spread of FP among Kemp’s ridley turtles in regions where the disease is enzootic. Although FP is currently uncommon in this species, it remains a health concern due to its uncertain pathogenesis and potential relationship with habitat degradation. Full article

(This article belongs to the Special Issue Oncogenic Viruses in Animals)

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22 pages, 3178 KiB

Open AccessEditor’s ChoiceArticle

Evolutionary Comparisons of Chelonid Alphaherpesvirus 5 (ChHV5) Genomes from Fibropapillomatosis-Afflicted Green (Chelonia mydas), Olive Ridley (Lepidochelys olivacea) and Kemp’s Ridley (Lepidochelys kempii) Sea Turtles

by Liam Whitmore, Kelsey Yetsko, Jessica A. Farrell, Annie Page-Karjian, Whitney Daniel, Donna J. Shaver, Hilary R. Frandsen, Jennifer Shelby Walker, Whitney Crowder, Caitlin Bovery, Devon Rollinson Ramia, Brooke Burkhalter, Elizabeth Ryan and David J. Duffy

Animals 2021, 11(9), 2489; https://doi.org/10.3390/ani11092489 - 25 Aug 2021

Cited by 7 | Viewed by 4000

Abstract

The spreading global sea turtle fibropapillomatosis (FP) epizootic is threatening some of Earth’s ancient reptiles, adding to the plethora of threats faced by these keystone species. Understanding this neoplastic disease and its likely aetiological pathogen, chelonid alphaherpesvirus 5 (ChHV5), is crucial to understand [...] Read more.

The spreading global sea turtle fibropapillomatosis (FP) epizootic is threatening some of Earth’s ancient reptiles, adding to the plethora of threats faced by these keystone species. Understanding this neoplastic disease and its likely aetiological pathogen, chelonid alphaherpesvirus 5 (ChHV5), is crucial to understand how the disease impacts sea turtle populations and species and the future trajectory of disease incidence. We generated 20 ChHV5 genomes, from three sea turtle species, to better understand the viral variant diversity and gene evolution of this oncogenic virus. We revealed previously underappreciated genetic diversity within this virus (with an average of 2035 single nucleotide polymorphisms (SNPs), 1.54% of the ChHV5 genome) and identified genes under the strongest evolutionary pressure. Furthermore, we investigated the phylogeny of ChHV5 at both genome and gene level, confirming the propensity of the virus to be interspecific, with related variants able to infect multiple sea turtle species. Finally, we revealed unexpected intra-host diversity, with up to 0.15% of the viral genome varying between ChHV5 genomes isolated from different tumours concurrently arising within the same individual. These findings offer important insights into ChHV5 biology and provide genomic resources for this oncogenic virus. Full article

(This article belongs to the Special Issue Oncogenic Viruses in Animals)

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12 pages, 582 KiB

Open AccessArticle

Chelonid Alphaherpesvirus 5 Prevalence and First Confirmed Case of Sea Turtle Fibropapillomatosis in Grenada, West Indies

by Amanda James, Annie Page-Karjian, Kate E. Charles, Jonnel Edwards, Christopher R. Gregory, Sonia Cheetham, Brian P. Buter and David P. Marancik

Animals 2021, 11(6), 1490; https://doi.org/10.3390/ani11061490 - 21 May 2021

Cited by 5 | Viewed by 3525

Abstract

Chelonid alphaherpesvirus 5 (ChHV5) is strongly associated with fibropapillomatosis, a neoplastic disease of sea turtles that can result in debilitation and mortality. The objectives of this study were to examine green (Chelonia mydas), hawksbill (Eretmochelys imbricata), and leatherback ( [...] Read more.

Chelonid alphaherpesvirus 5 (ChHV5) is strongly associated with fibropapillomatosis, a neoplastic disease of sea turtles that can result in debilitation and mortality. The objectives of this study were to examine green (Chelonia mydas), hawksbill (Eretmochelys imbricata), and leatherback (Dermochelys coriacea) sea turtles in Grenada, West Indies, for fibropapillomatosis and to utilize ChHV5-specific PCR, degenerate herpesvirus PCR, and serology to non-invasively evaluate the prevalence of ChHV5 infection and exposure. One-hundred and sixty-seven turtles examined from 2017 to 2019 demonstrated no external fibropapilloma-like lesions and no amplification of ChHV5 DNA from whole blood or skin biopsies. An ELISA performed on serum detected ChHV5-specific IgY in 18/52 (34.6%) of green turtles tested. In 2020, an adult, female green turtle presented for necropsy from the inshore waters of Grenada with severe emaciation and cutaneous fibropapillomas. Multiple tumors tested positive for ChHV5 by qPCR, providing the first confirmed case of ChHV5-associated fibropapillomatosis in Grenada. These results indicate that active ChHV5 infection is rare, although viral exposure in green sea turtles is relatively high. The impact of fibropapillomatosis in Grenada is suggested to be low at the present time and further studies comparing host genetics and immunologic factors, as well as examination into extrinsic factors that may influence disease, are warranted. Full article

(This article belongs to the Special Issue Oncogenic Viruses in Animals)

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20 pages, 1140 KiB

Open AccessArticle

Insights on Immune Function in Free-Ranging Green Sea Turtles (Chelonia mydas) with and without Fibropapillomatosis

by Justin R. Perrault, Milton Levin, Cody R. Mott, Caitlin M. Bovery, Michael J. Bresette, Ryan M. Chabot, Christopher R. Gregory, Jeffrey R. Guertin, Sarah E. Hirsch, Branson W. Ritchie, Steven T. Weege, Ryan C. Welsh, Blair E. Witherington and Annie Page-Karjian

Animals 2021, 11(3), 861; https://doi.org/10.3390/ani11030861 - 18 Mar 2021

Cited by 21 | Viewed by 4062

Abstract

Chelonid alphaherpesviruses 5 and 6 (ChHV5 and ChHV6) are viruses that affect wild sea turtle populations. ChHV5 is associated with the neoplastic disease fibropapillomatosis (FP), which affects green turtles (Chelonia mydas) in panzootic proportions. ChHV6 infection is associated with lung-eye-trachea disease [...] Read more.

Chelonid alphaherpesviruses 5 and 6 (ChHV5 and ChHV6) are viruses that affect wild sea turtle populations. ChHV5 is associated with the neoplastic disease fibropapillomatosis (FP), which affects green turtles (Chelonia mydas) in panzootic proportions. ChHV6 infection is associated with lung-eye-trachea disease (LETD), which has only been observed in maricultured sea turtles, although antibodies to ChHV6 have been detected in free-ranging turtles. To better understand herpesvirus prevalence and host immunity in various green turtle foraging aggregations in Florida, USA, our objectives were to compare measures of innate and adaptive immune function in relation to (1) FP tumor presence and severity, and (2) ChHV5 and ChHV6 infection status. Free-ranging, juvenile green turtles (N = 45) were captured and examined for external FP tumors in Florida’s Big Bend, Indian River Lagoon, and Lake Worth Lagoon. Blood samples were collected upon capture and analyzed for ChHV5 and ChHV6 DNA, antibodies to ChHV5 and ChHV6, in vitro lymphocyte proliferation using a T-cell mitogen (concanavalin A), and natural killer cell activity. Despite an overall high FP prevalence (56%), ChHV5 DNA was only observed in one individual, whereas 20% of turtles tested positive for antibodies to ChHV5. ChHV6 DNA was not observed in any animals and only one turtle tested positive for ChHV6 antibodies. T-cell proliferation was not significantly related to FP presence, tumor burden, or ChHV5 seroprevalence; however, lymphocyte proliferation in response to concanavalin A was decreased in turtles with severe FP (N = 3). Lastly, green turtles with FP (N = 9) had significantly lower natural killer cell activity compared to FP-free turtles (N = 5). These results increase our understanding of immune system effects related to FP and provide evidence that immunosuppression occurs after the onset of FP disease. Full article

(This article belongs to the Special Issue Oncogenic Viruses in Animals)

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18 pages, 846 KiB

Open AccessArticle

The Concurrent Detection of Chelonid Alphaherpesvirus 5 and Chelonia mydas Papillomavirus 1 in Tumoured and Non-Tumoured Green Turtles

by Narges Mashkour, Karina Jones, Wytamma Wirth, Graham Burgess and Ellen Ariel

Animals 2021, 11(3), 697; https://doi.org/10.3390/ani11030697 - 05 Mar 2021

Cited by 14 | Viewed by 2766

Abstract

Characterised by benign tumours, fibropapillomatosis (FP) is a debilitating disease that predominantly afflicts the endangered green turtle (Chelonia mydas). A growing body of histological and molecular evidence has associated FP tumours with Chelonid alphaherpesvirus 5 (ChHV5). However, a recent study which [...] Read more.

Characterised by benign tumours, fibropapillomatosis (FP) is a debilitating disease that predominantly afflicts the endangered green turtle (Chelonia mydas). A growing body of histological and molecular evidence has associated FP tumours with Chelonid alphaherpesvirus 5 (ChHV5). However, a recent study which detected both ChHV5 and Chelonia mydas papillomavirus 1 (CmPV1) DNA in FP tumour tissues has challenged this hypothesis. The present study aimed to establish a probe-based qPCR to assess the wider prevalence of CmPV1 and co-occurrence with ChHV5 in 275 marine turtles foraging in waters adjacent to the east coast of Queensland, Australia: three categories: Group A (FP tumours), Group B (non-tumoured skin from FP turtles) and Group C (non-tumoured skin from turtles without FP). Concurrent detection of ChHV5 and CmPV1 DNA is reported for all three categories, where Group A had the highest rate (43.5%). ChHV5 viral loads in Group A were significantly higher than loads seen in Group B and C. This was not the case for CmPV1 where the loads in Group B were highest, followed by Group A. However, the mean CmPV1 load for Group A samples was not significantly different to the mean load reported from Group B or C samples. Collectively, these results pivot the way we think about FP; as an infectious disease where two separate viruses may be at play. Full article

(This article belongs to the Special Issue Oncogenic Viruses in Animals)

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16 pages, 2168 KiB

Open AccessArticle

Unlocking the Role of a Genital Herpesvirus, Otarine Herpesvirus 1, in California Sea Lion Cervical Cancer

by Alissa C. Deming, James F. X. Wellehan, Kathleen M. Colegrove, Ailsa Hall, Jennifer Luff, Linda Lowenstine, Pádraig Duignan, Galaxia Cortés-Hinojosa and Frances M. D. Gulland

Animals 2021, 11(2), 491; https://doi.org/10.3390/ani11020491 - 13 Feb 2021

Cited by 9 | Viewed by 4970

Abstract

Urogenital carcinoma in California sea lions (Zalophus californianus) is the most common cancer of marine mammals. Primary tumors occur in the cervix, vagina, penis, or prepuce and aggressively metastasize resulting in death. This cancer has been strongly associated with a sexually [...] Read more.

Urogenital carcinoma in California sea lions (Zalophus californianus) is the most common cancer of marine mammals. Primary tumors occur in the cervix, vagina, penis, or prepuce and aggressively metastasize resulting in death. This cancer has been strongly associated with a sexually transmitted herpesvirus, otarine herpesvirus 1 (OtHV1), but the virus has been detected in genital tracts of sea lions without cancer and a causative link has not been established. To determine if OtHV1 has a role in causing urogenital carcinoma we sequenced the viral genome, quantified viral load from cervical tissue from sea lions with (n = 95) and without (n = 163) urogenital carcinoma, and measured viral mRNA expression using in situ mRNA hybridization (Basescope^®) to quantify and identify the location of OtHV1 mRNA expression. Of the 95 sea lions diagnosed with urogenital carcinoma, 100% were qPCR positive for OtHV1, and 36% of the sea lions with a normal cervix were positive for the virus. The non-cancer OtHV1 positive cases had significantly lower viral loads in their cervix compared to the cervices from sea lions with urogenital carcinoma. The OtHV1 genome had several genes similar to the known oncogenes, and RNA in situ hybridization demonstrated high OtHV1 mRNA expression within the carcinoma lesions but not in normal cervical epithelium. The high viral loads, high mRNA expression of OtHV1 in the cervical tumors, and the presence of suspected OtHV1 oncogenes support the hypothesis that OtHV1 plays a significant role in the development of sea lion urogenital carcinoma. Full article

(This article belongs to the Special Issue Oncogenic Viruses in Animals)

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9 pages, 2117 KiB

Open AccessCommunication

Molecular Characterization of Chelonid Alphaherpesvirus 5 in a Black Turtle (Chelonia mydas) Fibropapilloma from Baja California Sur, Mexico

by Eduardo Reséndiz, Helena Fernández-Sanz, José Francisco Domínguez-Contreras, Amelly Hyldaí Ramos-Díaz, Agnese Mancini, Alan A. Zavala-Norzagaray and A. Alonso Aguirre

Animals 2021, 11(1), 105; https://doi.org/10.3390/ani11010105 - 07 Jan 2021

Cited by 4 | Viewed by 2710

Abstract

During routine monitoring in Ojo de Liebre Lagoon, Mexico, a juvenile black turtle (Chelonia mydas) was captured, physically examined, measured, weighed, sampled, and tagged. The turtle showed no clinical signs suggestive of disease. Eleven months later, this turtle was recaptured in [...] Read more.

During routine monitoring in Ojo de Liebre Lagoon, Mexico, a juvenile black turtle (Chelonia mydas) was captured, physically examined, measured, weighed, sampled, and tagged. The turtle showed no clinical signs suggestive of disease. Eleven months later, this turtle was recaptured in the same area, during which one lesion suggestive of fibropapilloma on the neck was identified and sampled for histopathology and molecular analysis. Histopathology revealed hyperkeratosis, epidermal hyperplasia, acanthosis, papillary differentiation and ballooning degeneration of epidermal cells, increased fibroblasts in the dermis, and angiogenesis, among other things. Hematological values were similar to those reported for clinically healthy black turtles and did not show notable changes between the first capture and the recapture; likewise, clinicopathological evaluation did not show structural or functional damage in the turtle’s systems. The chelonid alphaherpesvirus 5 (ChHV5) UL30 gene was amplified and sequenced for phylogeny; Bayesian reconstruction showed a high alignment with the genus Scutavirus of the Eastern Pacific group. This is one of the first reports of ChHV5 in a cutaneous fibropapilloma of a black turtle in the Baja California peninsula. Full article

(This article belongs to the Special Issue Oncogenic Viruses in Animals)

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13 pages, 286 KiB

Open AccessFeature PaperArticle

Molecular Assessment of Chelonid Alphaherpesvirus 5 Infection in Tumor-Free Green (Chelonia mydas) and Loggerhead (Caretta caretta) Sea Turtles in North Carolina, USA, 2015–2019

by Annie Page-Karjian, Maria E. Serrano, Jeffrey Cartzendafner, Ashley Morgan, Branson W. Ritchie, Christopher R. Gregory, Joanne Braun McNeill, Justin R. Perrault, Emily F. Christiansen and Craig A. Harms

Animals 2020, 10(11), 1964; https://doi.org/10.3390/ani10111964 - 25 Oct 2020

Cited by 10 | Viewed by 2231

Abstract

Fibropapillomatosis is associated with chelonid alphaherpesvirus 5 (ChHV5) and tumor formation in sea turtles. We collected blood samples from 113 green (Chelonia mydas) and 112 loggerhead (Caretta caretta) turtles without fibropapillomatosis, including 46 free-ranging turtles (20 green turtles, 26 [...] Read more.

Fibropapillomatosis is associated with chelonid alphaherpesvirus 5 (ChHV5) and tumor formation in sea turtles. We collected blood samples from 113 green (Chelonia mydas) and 112 loggerhead (Caretta caretta) turtles without fibropapillomatosis, including 46 free-ranging turtles (20 green turtles, 26 loggerheads), captured in Core Sound, North Carolina, and 179 turtles (93 green turtles, 86 loggerheads) in rehabilitative care in North Carolina. Blood samples were analyzed for ChHV5 DNA using quantitative polymerase chain reaction (qPCR), and for antibodies to ChHV5 peptides using an enzyme-linked immunosorbent assay (ELISA). None of the samples from foraging turtles tested positive for ChHV5 by qPCR; ELISA was not used for foraging turtles. Samples from 18/179 (10.1%) rehabilitating turtles tested positive for ChHV5 using qPCR, and 32/56 (57.1%) rehabilitating turtles tested positive for antibodies to ChHV5 using ELISA. Five turtles that tested positive by qPCR or ELISA at admission converted to being undetectable during rehabilitation, and five that initially tested negative converted to being positive. Both sea turtle species were significantly more likely to test positive for ChHV5 using ELISA than with qPCR (p < 0.001). There was no difference in the proportions of green turtles versus loggerheads that tested positive for ChHV5 using qPCR, but loggerheads were significantly more likely than green turtles to test positive for ChHV5 using ELISA. This finding suggests that loggerheads infected with ChHV5 at some point in their life may be more able than green turtles to mount an effective immune response against recrudescent infection, pointing to species-specific genetic differences in the two species’ immune response to ChHV5 infection. This is the first study to analyze antibodies to ChHV5 in loggerhead turtles and represents the most complete dataset on ChHV5 DNA detection in sea turtles encountered in the more northern latitudes of their western Atlantic habitat. Full article

(This article belongs to the Special Issue Oncogenic Viruses in Animals)

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