Physiological costs of infection: herpesvirus replication is linked to blood oxidative stress in equids.
Abstract: Viruses may have a dramatic impact on the health of their animal hosts. The patho-physiological mechanisms underlying viral infections in animals are, however, not well understood. It is increasingly recognized that oxidative stress may be a major physiological cost of viral infections. Here we compare three blood-based markers of oxidative status in herpes positive and negative individuals of the domestic horse (Equus ferus caballus) and of both captive and free-ranging Mongolian khulan (Equus hemionus hemionus) and plains zebra (Equus quagga). Herpes positive free-ranging animals had significantly more protein oxidative damage and lower glutathione peroxidase (antioxidant enzyme) than negative ones, providing correlative support for a link between oxidative stress and herpesvirus infection in free-living equids. Conversely, we found weak evidence for oxidative stress in herpes positive captive animals. Hence our work indicates that environment (captive versus free living) might affect the physiological response of equids to herpesvirus infection. The Mongolian khulan and the plains zebra are currently classified as near threatened by the International Union for Conservation of Nature. Thus, understanding health impacts of pathogens on these species is critical to maintaining viable captive and wild populations.
Publication Date: 2018-07-09 PubMed ID: 29985431PubMed Central: PMC6037783DOI: 10.1038/s41598-018-28688-0Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research investigates the link between herpesvirus infection and oxidative stress in the blood of domestic and wild horses as well as zebras. The results show a correlation between herpesvirus and increased oxidative stress levels in free-ranging animals but not necessarily in captive ones.
Research Background and Objectives
- The study explores the physiological impacts of viral infections in equids – such as domestic horses (Equus ferus caballus), Mongolian khulan (Equus hemionus hemionus), and plains zebra (Equus quagga) – focusing on the relationship between herpesvirus infection and blood oxidative stress.
- The goal of the paper is to improve understanding of viral infection mechanisms in animals, particularly how they may trigger oxidative stress – a physiological state that could have detrimental impacts on the well-being and fitness of the infected hosts.
Methods and Procedures
- Three blood-based oxidative stress markers were analyzed in both herpesvirus positive and negative equids.
- The study was conducted on both captive and free-ranging examples of the species in question.
Results and Findings
- According to the analysis, herpesvirus-infection resulted in significantly greater protein oxidative damage and reduced levels of glutathione peroxidase (an antioxidant enzyme) in free-ranging animals.
- This result establishes a correlation between increased oxidative stress and herpesvirus infection in wild equids.
- However, this evidence was not as conclusive in cases of animals kept in captivity. The study suggests the animal’s environment (captive versus free living) may influence the physiological response to herpesvirus infection.
Significance of the Study
- The physiological cost of the herpesvirus infection underlines the need for a comprehensive understanding of the health impacts of these viruses on fauna, particularly animals deemed near threatened according to the International Union for Conservation of Nature, such as the Mongolian khulan and the plains zebra.
- Such knowledge is paramount to the maintenance and survival of both captive and wild populations of these species.
Cite This Article
APA
Costantini D, Seeber PA, Soilemetzidou SE, Azab W, Bohner J, Buuveibaatar B, Czirják GÁ, East ML, Greunz EM, Kaczensky P, Lamglait B, Melzheimer J, Uiseb K, Ortega A, Osterrieder N, Sandgreen DM, Simon M, Walzer C, Greenwood AD.
(2018).
Physiological costs of infection: herpesvirus replication is linked to blood oxidative stress in equids.
Sci Rep, 8(1), 10347.
https://doi.org/10.1038/s41598-018-28688-0 Publication
Researcher Affiliations
- UMR 7221 CNRS/MNHN, Muséum National d'Histoire Naturelle, Sorbonne Universités, 7 rue Cuvier, 75005, Paris, France. david.costantini@mnhn.fr.
- Institute for Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, G12 8QQ, Glasgow, Scotland, UK. david.costantini@mnhn.fr.
- Department of Biology, University of Antwerp, Universiteitsplein 1, 2610, Antwerp, Belgium. david.costantini@mnhn.fr.
- Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Straße 17, 10315, Berlin, Germany.
- Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Straße 17, 10315, Berlin, Germany.
- Institut für Virologie, Robert von Ostertag-Haus, Zentrum für Infektionsmedizin, Freie Universität Berlin, Robert-von-Ostertag-Str. 7-13, 14163, Berlin, Germany.
- Department of Reproduction Management, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Straße 17, 10315, Berlin, Germany.
- Wildlife Conservation Society, Mongolia Program, Ulaanbaatar, Mongolia.
- Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Straße 17, 10315, Berlin, Germany.
- Department of Ecological Dynamics, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Straße 17, 10315, Berlin, Germany.
- Center for Zoo and Wild Animal Health, Copenhagen Zoo, Roskildevej 38, 2000, Frederiksberg, Denmark.
- Parc Zoologique de Thoiry, Rue du Pavillon de Montreuil, 78770, Thoiry, France.
- Research Institute of Wildlife Ecology, University of Veterinary Medicine, Savoyenstrasse 1, A-1160, Vienna, Austria.
- Norwegian Institute for Nature Research - NINA, Sluppen, NO-7485, Trondheim, Norway.
- Faculty of Veterinary Medicine, Université de Montréal, 3200 Rue Sicotte, Saint-Hyacinthe, Québec, J2S 2N4, Canada.
- Réserve Africaine de Sigean, 19 Chemin Hameau du Lac, RD 6009, 11130, Sigean, France.
- Department of Evolutionary Ecology, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Straße 17, 10315, Berlin, Germany.
- Ministry of Environment and Tourism, Private Bag 13301, Windhoek, Namibia.
- Réserve Africaine de Sigean, 19 Chemin Hameau du Lac, RD 6009, 11130, Sigean, France.
- Institut für Virologie, Robert von Ostertag-Haus, Zentrum für Infektionsmedizin, Freie Universität Berlin, Robert-von-Ostertag-Str. 7-13, 14163, Berlin, Germany.
- Givskud Zoo, Løveparkvej 3, Givskud, 7323, Give, Denmark.
- Parc Zoologique de Thoiry, Rue du Pavillon de Montreuil, 78770, Thoiry, France.
- Research Institute of Wildlife Ecology, University of Veterinary Medicine, Savoyenstrasse 1, A-1160, Vienna, Austria.
- Wildlife Conservation Society, 2300 Southern Blvd., 10460, Bronx, New York, USA.
- Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Straße 17, 10315, Berlin, Germany.
- Department of Veterinary Medicine, Freie Universität Berlin, Oertzenweg 19, Berlin, 14163, Germany.
MeSH Terms
- Animals
- DNA, Viral / genetics
- DNA, Viral / metabolism
- Equidae
- Female
- Glutathione Peroxidase / metabolism
- Herpesviridae / genetics
- Herpesviridae / isolation & purification
- Herpesviridae / physiology
- Herpesviridae Infections / pathology
- Herpesviridae Infections / veterinary
- Herpesviridae Infections / virology
- Horses
- Least-Squares Analysis
- Male
- Oxidative Stress
- Protein Carbonylation
- Species Specificity
- Virus Replication
Grant Funding
- SAW-2015-IZW-1 440 / Leibniz-Gemeinschaft (Leibniz Association)
- SAW-2015-IZW-1 440 / Leibniz-Gemeinschaft (Leibniz Association)
Conflict of Interest Statement
The authors declare no competing interests.
References
This article includes 51 references
- Sheldon BC, Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology.. Trends Ecol Evol 1996 Aug;11(8):317-21.
- Daszak P, Cunningham AA, Hyatt AD. Emerging infectious diseases of wildlife--threats to biodiversity and human health.. Science 2000 Jan 21;287(5452):443-9.
- Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. Global trends in emerging infectious diseases.. Nature 2008 Feb 21;451(7181):990-3.
- Graham AL. Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology.. Funct. Ecol. 2011;25:5–17.
- Asghar M, Hasselquist D, Hansson B, Zehtindjiev P, Westerdahl H, Bensch S. Chronic infection. Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds.. Science 2015 Jan 23;347(6220):436-8.
- Marco I, Rosell R, Cabezón O, Mentaberre G, Casas E, Velarde R, Lavín S. Border disease virus among chamois, Spain.. Emerg Infect Dis 2009 Mar;15(3):448-51.
- Marescot L. Social status mediates the fitness costs of infection with canine distemper virus in Serengeti spotted hyenas.. Funct. Ecol. in press (2018).
- Virgin HW, Wherry EJ, Ahmed R. Redefining chronic viral infection.. Cell 2009 Jul 10;138(1):30-50.
- Kaleta EF. Herpesviruses of birds--a review.. Avian Pathol 1990 Apr;19(2):193-211.
- Woźniakowski G, Samorek-Salamonowicz E. Animal herpesviruses and their zoonotic potential for cross-species infection.. Ann Agric Environ Med 2015;22(2):191-4.
- Nucci C, Palamara AT, Ciriolo MR, Nencioni L, Savini P, D'Agostini C, Rotilio G, Cerulli L, Garaci E. Imbalance in corneal redox state during herpes simplex virus 1-induced keratitis in rabbits. Effectiveness of exogenous glutathione supply.. Exp Eye Res 2000 Feb;70(2):215-20.
- Valyi-Nagy T, Olson SJ, Valyi-Nagy K, Montine TJ, Dermody TS. Herpes simplex virus type 1 latency in the murine nervous system is associated with oxidative damage to neurons.. Virology 2000 Dec 20;278(2):309-21.
- Palamara AT, Brandi G, Rossi L, Millo E, Benatti U, Nencioni L, Iuvara A, Garaci E, Magnani M. New synthetic glutathione derivatives with increased antiviral activities.. Antivir Chem Chemother 2004 Mar;15(2):83-91.
- Kavouras JH, Prandovszky E, Valyi-Nagy K, Kovacs SK, Tiwari V, Kovacs M, Shukla D, Valyi-Nagy T. Herpes simplex virus type 1 infection induces oxidative stress and the release of bioactive lipid peroxidation by-products in mouse P19N neural cell cultures.. J Neurovirol 2007 Oct;13(5):416-25.
- Sebastiano M, Chastel O, de Thoisy B, Eens M, Costantini D. Oxidative stress favours herpes virus infection in vertebrates: a meta-analysis.. Curr Zool 2016 Aug;62(4):325-332.
- Mathew SS, Bryant PW, Burch AD. Accumulation of oxidized proteins in Herpesvirus infected cells.. Free Radic Biol Med 2010 Aug 1;49(3):383-91.
- Halliwell BH, Gutteridge JMC. Free radicals in biology and medicine.. Oxford University Press (2015).
- Lassoued S, Ben Ameur R, Ayadi W, Gargouri B, Ben Mansour R, Attia H. Epstein-Barr virus induces an oxidative stress during the early stages of infection in B lymphocytes, epithelial, and lymphoblastoid cell lines.. Mol Cell Biochem 2008 Jun;313(1-2):179-86.
- Gargouri B, Van Pelt J, El Feki Ael F, Attia H, Lassoued S. Induction of Epstein-Barr virus (EBV) lytic cycle in vitro causes oxidative stress in lymphoblastoid B cell lines.. Mol Cell Biochem 2009 Apr;324(1-2):55-63.
- Sebastiano M, Eens M, Abd Elgawad H, Thoisy B, Lacoste V, Pineau K, Asard H, Chastel O, Costantini D. Oxidative stress biomarkers are associated with visible clinical signs of a disease in frigatebird nestlings.. Sci Rep 2017 May 9;7(1):1599.
- Sorci G, Faivre B. Inflammation and oxidative stress in vertebrate host-parasite systems.. Philos Trans R Soc Lond B Biol Sci 2009 Jan 12;364(1513):71-83.
- Costantini D. Oxidative stress and hormesis in evolutionary ecology and physiology: a marriage between mechanistic and evolutionary approaches.. Springer-Verlag, Berlin Heidelberg, pp. 348 (2014).
- Reed SM, Toribio RE. Equine herpesvirus 1 and 4.. Vet Clin North Am Equine Pract 2004 Dec;20(3):631-42.
- Blunden AS, Smith KC, Whitwell KE, Dunn KA. Systemic infection by equid herpesvirus-1 in a Grevy's zebra stallion (Equus grevyi) with particular reference to genital pathology.. J Comp Pathol 1998 Nov;119(4):485-93.
- van Maanen C. Equine herpesvirus 1 and 4 infections: an update.. Vet Q 2002 Jun;24(2):58-78.
- Borchers K, Wiik H, Frölich K, Ludwig H, East ML. Antibodies against equine herpesviruses and equine arteritis virus in Burchell's zebras (Equus burchelli ) from the Serengeti ecosystem.. J Wildl Dis 2005 Jan;41(1):80-6.
- Abdelgawad A, Hermes R, Damiani A, Lamglait B, Czirják GÁ, East M, Aschenborn O, Wenker C, Kasem S, Osterrieder N, Greenwood AD. Comprehensive Serology Based on a Peptide ELISA to Assess the Prevalence of Closely Related Equine Herpesviruses in Zoo and Wild Animals.. PLoS One 2015;10(9):e0138370.
- Dunowska M, Wilks CR, Studdert MJ, Meers J. Equine respiratory viruses in foals in New Zealand.. N Z Vet J 2002 Aug;50(4):140-7.
- Ataseven VS, Bilge-Dagalp S, Oguzoglu TC, Karapinar Z, Güzel M, Tan MT. Detection and sequence analysis of equine gammaherpesviruses from horses with respiratory tract disease in Turkey.. Transbound Emerg Dis 2010 Aug 1;57(4):271-6.
- Williams KJ, Maes R, Del Piero F, Lim A, Wise A, Bolin DC, Caswell J, Jackson C, Robinson NE, Derksen F, Scott MA, Uhal BD, Li X, Youssef SA, Bolin SR. Equine multinodular pulmonary fibrosis: a newly recognized herpesvirus-associated fibrotic lung disease.. Vet Pathol 2007 Nov;44(6):849-62.
- Cohen J. Power analysis for the behavioural sciences.. Erlbaum, Hillsdale (1988).
- Møller A, Jennions MD. How much variance can be explained by ecologists and evolutionary biologists?. Oecologia 2002 Aug;132(4):492-500.
- Dalle-Donne I, Giustarini D, Colombo R, Rossi R, Milzani A. Protein carbonylation in human diseases.. Trends Mol Med 2003 Apr;9(4):169-76.
- Dalle-Donne I, Aldini G, Carini M, Colombo R, Rossi R, Milzani A. Protein carbonylation, cellular dysfunction, and disease progression.. J Cell Mol Med 2006 Apr-Jun;10(2):389-406.
- Camini FC, da Silva Caetano CC, Almeida LT, de Brito Magalhães CL. Implications of oxidative stress on viral pathogenesis.. Arch Virol 2017 Apr;162(4):907-917.
- Durgut R, Ataseven VS, Sağkan-Öztürk A, Oztürk OH. Evaluation of total oxidative stress and total antioxidant status in cows with natural bovine herpesvirus-1 infection.. J Anim Sci 2013 Jul;91(7):3408-12.
- Costantini D, Møller AP. Does immune response cause oxidative stress in birds? A meta-analysis.. Comp Biochem Physiol A Mol Integr Physiol 2009 Jul;153(3):339-44.
- Costantini D. Meta-analysis reveals that reproductive strategies are associated with sexual differences in oxidative balance across vertebrates.. Curr Zool 2018 Feb;64(1):1-11.
- Walzer C. Nondomestic equids.. In: West, G (Ed.): Zoo Animal and Wildlife Immobilization andAnesthesia. 2. Ed. Ames, Iowa, Wiley Blackwell, pp. 719–728 (2014).
- Fukushi H, Tomita T, Taniguchi A, Ochiai Y, Kirisawa R, Matsumura T, Yanai T, Masegi T, Yamaguchi T, Hirai K. Gazelle herpesvirus 1: a new neurotropic herpesvirus immunologically related to equine herpesvirus 1.. Virology 1997 Jan 6;227(1):34-44.
- Borchers K, Lieckfeldt D, Ludwig A, Fukushi H, Allen G, Fyumagwa R, Hoare R. Detection of Equid herpesvirus 9 DNA in the trigeminal ganglia of a Burchell's zebra from the Serengeti ecosystem.. J Vet Med Sci 2008 Dec;70(12):1377-81.
- Azab W, Kato K, Arii J, Tsujimura K, Yamane D, Tohya Y, Matsumura T, Akashi H. Cloning of the genome of equine herpesvirus 4 strain TH20p as an infectious bacterial artificial chromosome.. Arch Virol 2009;154(5):833-42.
- Turan N, Yildirim F, Altan E, Sennazli G, Gurel A, Diallo I, Yilmaz H. Molecular and pathological investigations of EHV-1 and EHV-4 infections in horses in Turkey.. Res Vet Sci 2012 Dec;93(3):1504-7.
- Hussey SB, Clark R, Lunn KF, Breathnach C, Soboll G, Whalley JM, Lunn DP. Detection and quantification of equine herpesvirus-1 viremia and nasal shedding by real-time polymerase chain reaction.. J Vet Diagn Invest 2006 Jul;18(4):335-42.
- Abdelgawad A, Azab W, Damiani AM, Baumgartner K, Will H, Osterrieder N, Greenwood AD. Zebra-borne equine herpesvirus type 1 (EHV-1) infection in non-African captive mammals.. Vet Microbiol 2014 Feb 21;169(1-2):102-6.
- Kleiboeker SB, Schommer SK, Johnson PJ, Ehlers B, Turnquist SE, Boucher M, Kreeger JM. Association of two newly recognized herpesviruses with interstitial pneumonia in donkeys (Equus asinus).. J Vet Diagn Invest 2002 Jul;14(4):273-80.
- Seeber PA, Soilemetzidou SE, East ML, Walzer C, Greenwood AD. Equine behavioral enrichment toys as tools for non-invasive recovery of viral and host DNA.. Zoo Biol 2017 Sep;36(5):341-344.
- Vitikainen EIK. Evidence of oxidative shielding of offspring in a wild mammal.. Front. Ecol. Evol. 2016;4:58.
- Costantini D, Wachter B, Melzheimer J, Czirják GÁ. Socioecological and environmental predictors of physiological stress markers in a threatened feline species.. Conserv. Physiol. 2017;5:cox069.
- Del Re AC. Compute.es: compute effect sizes.. R package version 0.2–2, http://cran.r-project.org/web/packages/compute.es (2013).
- R Core Team. A language and environment for statistical computing.. R Foundation for Statistical Computing Vienna, Austria. https://www.R-project.org/ (2013).
Citations
This article has been cited 8 times.- Kosaruk W, Brown JL, Towiboon P, Punyapornwithaya V, Pringproa K, Thitaram C. Measures of Oxidative Status Markers in Relation to Age, Sex, and Season in Sick and Healthy Captive Asian Elephants in Thailand. Animals (Basel) 2023 May 5;13(9).
- Costantini D. A meta-analysis of impacts of immune response and infection on oxidative status in vertebrates. Conserv Physiol 2022;10(1):coac018.
- Stasiak K, Dunowska M, Rola J. Kinetics of the Equid Herpesvirus 2 and 5 Infections among Mares and Foals from Three Polish National Studs. Viruses 2022 Mar 29;14(4).
- Tsai MS, François S, Newman C, Macdonald DW, Buesching CD. Patterns of Genital Tract Mustelid Gammaherpesvirus 1 (Musghv-1) Reactivation Are Linked to Stressors in European Badgers (Meles Meles). Biomolecules 2021 May 11;11(5).
- Goertz CEC, Reichmuth C, Thometz NM, Ziel H, Boveng P. Comparative Health Assessments of Alaskan Ice Seals. Front Vet Sci 2019;6:4.
- Seeber PA, Dayaram A, Sicks F, Osterrieder N, Franz M, Greenwood AD. Noninvasive Detection of Equid Herpesviruses in Fecal Samples. Appl Environ Microbiol 2019 Feb 1;85(3).
- Ji Y, Zhao X, Liu W. Detection of equine herpesvirus antibodies in large-scale donkey farms in Liaocheng area. Vet Med Sci 2024 Sep;10(5):e70016.
- Chen L, Li S, Li W, Yu Y, Sun Q, Chen W, Zhou H, Wang C, Li L, Xu M, Khan MZ, Li Y, Wang T. Rutin prevents EqHV-8 induced infection and oxidative stress via Nrf2/HO-1 signaling pathway. Front Cell Infect Microbiol 2024;14:1386462.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists