Persistent contaminants and herpesvirus OtHV1 are positively associated with cancer in wild California Sea Lions (Zalophus californianus)

Frances M. D. Gulland; Ailsa J. Hall; Gina M. Ylitalo; Kathleen M. Colegrove; Tenaya Norris; Pádraig J. Duignan; Barbie Halaska; Karina Acevedo Whitehouse; Linda J. Lowenstine; Alissa C. Deming; Teresa K. Rowles

doi:10.3389/fmars.2020.602565

Persistent contaminants and herpesvirus OtHV1 are positively associated with cancer in wild California Sea Lions (Zalophus californianus)

Frances M. D. Gulland, Ailsa J. Hall, Gina M. Ylitalo, Kathleen M. Colegrove, Tenaya Norris, Pádraig J. Duignan, Barbie Halaska, Karina Acevedo Whitehouse, Linda J. Lowenstine, Alissa C. Deming, Teresa K. Rowles

Research output: Contribution to journal › Article › peer-review

Abstract

The prevalence of cancer in wild California sea lions (Zalophus californianus) is one of the highest amongst mammals, with 18–23% of adult animals examined post-mortem over the past 40 years having urogenital carcinoma. To date, organochlorines, genotype and infection with Otarine herpesvirus-1 (OtHV-1) have been identified in separate studies using distinct animals as associated with this carcinoma. Multi-year studies using large sample sizes to investigate the relative importance of multiple factors on marine mammal health are rare due to logistical and ethical challenges. The objective of this study was to use a case control approach with samples from 394 animals collected over 20 years in a multifactorial analysis to explore the relative importance of distinct factors identified to date as associated with sea lion cancer in the likelihood of sea lion carcinoma. Stepwise regression indicated that the best model to explain carcinoma occurrence included herpesvirus status, contaminant exposure, and blubber depth, but not genotype at a single microsatellite locus, PV11. The odds of carcinoma was 43.57 times higher in sea lions infected with OtHV-1 (95% CI 14.61, 129.96, p <0.001), and 1.48 times higher for every unit increase in the log_e[contaminant concentrations], ng g^–1 (an approximate tripling of concentration), in their blubber (95% CI 1.11, 1.97, p <0.007), after controlling for the effect of blubber depth. These findings demonstrate the importance of contaminant exposure combined with OtHV1 infection, in the potential for cancer occurrence in wild sea lions.

Original language	English
Article number	602565
Number of pages	13
Journal	Frontiers in Marine Science
Volume	7
DOIs	https://doi.org/10.3389/fmars.2020.602565
Publication status	Published - 10 Dec 2020

Keywords

Cancer
Organochlorines
Sea lions
Herpesvirus
Microsatellite
Case control study

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.3389/fmars.2020.602565Licence: CC BY

Gullard_2020_front.marinesci_persistent-contaminants_CC
Copyright © 2020 Gulland, Hall, Ylitalo, Colegrove, Norris, Duignan, Halaska, Acevedo Whitehouse, Lowenstine, Deming and Rowles. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Final published version, 1.76 MBLicence: CC BY

NERC NC National Public Good 2018 - 2023: Sea Mammal Research Unit NC-NPG activities to fulfill NERC's statutory duties.
Sparling, C. E. (PI) & Hall, A. J. (CoI)
1/04/18 → 31/03/23
Project: Standard

Cancer in California Sea Lions (dataset)
Hall, A. J. (Creator), University of St Andrews, 10 Dec 2020
DOI: 10.17630/5e96ccde-3814-47ed-960b-6e8991da68df
Dataset

File
Cancer in California Sea Lions (additional dataset)
Hall, A. J. (Creator), University of St Andrews, 4 Jul 2022
DOI: 10.17630/bfee2acb-fa89-4361-9ee6-0bef629dbda2
Dataset

File

Cite this

Gulland, F. M. D., Hall, A. J., Ylitalo, G. M., Colegrove, K. M., Norris, T., Duignan, P. J., Halaska, B., Acevedo Whitehouse, K., Lowenstine, L. J., Deming, A. C., & Rowles, T. K. (2020). Persistent contaminants and herpesvirus OtHV1 are positively associated with cancer in wild California Sea Lions (Zalophus californianus). Frontiers in Marine Science, 7, Article 602565. https://doi.org/10.3389/fmars.2020.602565

@article{979fe3d74418438a99177a818609dbb3,

title = "Persistent contaminants and herpesvirus OtHV1 are positively associated with cancer in wild California Sea Lions (Zalophus californianus)",

abstract = "The prevalence of cancer in wild California sea lions (Zalophus californianus) is one of the highest amongst mammals, with 18–23% of adult animals examined post-mortem over the past 40 years having urogenital carcinoma. To date, organochlorines, genotype and infection with Otarine herpesvirus-1 (OtHV-1) have been identified in separate studies using distinct animals as associated with this carcinoma. Multi-year studies using large sample sizes to investigate the relative importance of multiple factors on marine mammal health are rare due to logistical and ethical challenges. The objective of this study was to use a case control approach with samples from 394 animals collected over 20 years in a multifactorial analysis to explore the relative importance of distinct factors identified to date as associated with sea lion cancer in the likelihood of sea lion carcinoma. Stepwise regression indicated that the best model to explain carcinoma occurrence included herpesvirus status, contaminant exposure, and blubber depth, but not genotype at a single microsatellite locus, PV11. The odds of carcinoma was 43.57 times higher in sea lions infected with OtHV-1 (95% CI 14.61, 129.96, p <0.001), and 1.48 times higher for every unit increase in the loge[contaminant concentrations], ng g–1 (an approximate tripling of concentration), in their blubber (95% CI 1.11, 1.97, p <0.007), after controlling for the effect of blubber depth. These findings demonstrate the importance of contaminant exposure combined with OtHV1 infection, in the potential for cancer occurrence in wild sea lions.",

keywords = "Cancer, Organochlorines, Sea lions, Herpesvirus, Microsatellite, Case control study",

author = "Gulland, {Frances M. D.} and Hall, {Ailsa J.} and Ylitalo, {Gina M.} and Colegrove, {Kathleen M.} and Tenaya Norris and Duignan, {P{\'a}draig J.} and Barbie Halaska and {Acevedo Whitehouse}, Karina and Lowenstine, {Linda J.} and Deming, {Alissa C.} and Rowles, {Teresa K.}",

note = "This work was funded by the Geoffrey Hughes Fellowship, the National Institutes of Health (Fogarty International Center) and National Science Foundation joint program for the Ecology of Infectious Disease, the National Marine Fisheries Service Marine Mammal Heath and Stranding Program, and the Natural Environment Research Council grant number NE/R015007/. ",

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doi = "10.3389/fmars.2020.602565",

language = "English",

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journal = "Frontiers in Marine Science",

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Gulland, FMD, Hall, AJ, Ylitalo, GM, Colegrove, KM, Norris, T, Duignan, PJ, Halaska, B, Acevedo Whitehouse, K, Lowenstine, LJ, Deming, AC & Rowles, TK 2020, 'Persistent contaminants and herpesvirus OtHV1 are positively associated with cancer in wild California Sea Lions (Zalophus californianus)', Frontiers in Marine Science, vol. 7, 602565. https://doi.org/10.3389/fmars.2020.602565

TY - JOUR

T1 - Persistent contaminants and herpesvirus OtHV1 are positively associated with cancer in wild California Sea Lions (Zalophus californianus)

AU - Gulland, Frances M. D.

AU - Hall, Ailsa J.

AU - Ylitalo, Gina M.

AU - Colegrove, Kathleen M.

AU - Norris, Tenaya

AU - Duignan, Pádraig J.

AU - Halaska, Barbie

AU - Acevedo Whitehouse, Karina

AU - Lowenstine, Linda J.

AU - Deming, Alissa C.

AU - Rowles, Teresa K.

N1 - This work was funded by the Geoffrey Hughes Fellowship, the National Institutes of Health (Fogarty International Center) and National Science Foundation joint program for the Ecology of Infectious Disease, the National Marine Fisheries Service Marine Mammal Heath and Stranding Program, and the Natural Environment Research Council grant number NE/R015007/.

PY - 2020/12/10

Y1 - 2020/12/10

N2 - The prevalence of cancer in wild California sea lions (Zalophus californianus) is one of the highest amongst mammals, with 18–23% of adult animals examined post-mortem over the past 40 years having urogenital carcinoma. To date, organochlorines, genotype and infection with Otarine herpesvirus-1 (OtHV-1) have been identified in separate studies using distinct animals as associated with this carcinoma. Multi-year studies using large sample sizes to investigate the relative importance of multiple factors on marine mammal health are rare due to logistical and ethical challenges. The objective of this study was to use a case control approach with samples from 394 animals collected over 20 years in a multifactorial analysis to explore the relative importance of distinct factors identified to date as associated with sea lion cancer in the likelihood of sea lion carcinoma. Stepwise regression indicated that the best model to explain carcinoma occurrence included herpesvirus status, contaminant exposure, and blubber depth, but not genotype at a single microsatellite locus, PV11. The odds of carcinoma was 43.57 times higher in sea lions infected with OtHV-1 (95% CI 14.61, 129.96, p <0.001), and 1.48 times higher for every unit increase in the loge[contaminant concentrations], ng g–1 (an approximate tripling of concentration), in their blubber (95% CI 1.11, 1.97, p <0.007), after controlling for the effect of blubber depth. These findings demonstrate the importance of contaminant exposure combined with OtHV1 infection, in the potential for cancer occurrence in wild sea lions.

AB - The prevalence of cancer in wild California sea lions (Zalophus californianus) is one of the highest amongst mammals, with 18–23% of adult animals examined post-mortem over the past 40 years having urogenital carcinoma. To date, organochlorines, genotype and infection with Otarine herpesvirus-1 (OtHV-1) have been identified in separate studies using distinct animals as associated with this carcinoma. Multi-year studies using large sample sizes to investigate the relative importance of multiple factors on marine mammal health are rare due to logistical and ethical challenges. The objective of this study was to use a case control approach with samples from 394 animals collected over 20 years in a multifactorial analysis to explore the relative importance of distinct factors identified to date as associated with sea lion cancer in the likelihood of sea lion carcinoma. Stepwise regression indicated that the best model to explain carcinoma occurrence included herpesvirus status, contaminant exposure, and blubber depth, but not genotype at a single microsatellite locus, PV11. The odds of carcinoma was 43.57 times higher in sea lions infected with OtHV-1 (95% CI 14.61, 129.96, p <0.001), and 1.48 times higher for every unit increase in the loge[contaminant concentrations], ng g–1 (an approximate tripling of concentration), in their blubber (95% CI 1.11, 1.97, p <0.007), after controlling for the effect of blubber depth. These findings demonstrate the importance of contaminant exposure combined with OtHV1 infection, in the potential for cancer occurrence in wild sea lions.

KW - Cancer

KW - Organochlorines

KW - Sea lions

KW - Herpesvirus

KW - Microsatellite

KW - Case control study

U2 - 10.3389/fmars.2020.602565

DO - 10.3389/fmars.2020.602565

M3 - Article

SN - 2296-7745

VL - 7

JO - Frontiers in Marine Science

JF - Frontiers in Marine Science

M1 - 602565

ER -

Persistent contaminants and herpesvirus OtHV1 are positively associated with cancer in wild California Sea Lions (Zalophus californianus)

Abstract

Keywords

UN SDGs

Access to Document

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Projects

NERC NC National Public Good 2018 - 2023: Sea Mammal Research Unit NC-NPG activities to fulfill NERC's statutory duties.

Datasets

Cancer in California Sea Lions (dataset)

Cancer in California Sea Lions (additional dataset)

Cite this