Tierarztl Prax Ausg K Kleintiere Heimtiere 2021; 49(06): 462-467
DOI: 10.1055/a-1666-8378
Case Report

A testudinid herpesvirus 1 (TeHV1)-associated disease outbreak in a group of Horsfield’s tortoises (Testudo horsfieldii)

Ein mit Testudinid-Herpesvirus 1 (TeHV1) assoziierter Krankheitsausbruch bei Vierzehenschildkröten (Testudo horsfieldii)
Lisa Schüler
1   Laboklin GmbH & Co. KG, Bad Kissingen, Germany
,
Pierre Picquet
2   Clinique Vétérinaire des Estuaires, Saint James, France
,
Christoph Leineweber
1   Laboklin GmbH & Co. KG, Bad Kissingen, Germany
,
Janosch Dietz
1   Laboklin GmbH & Co. KG, Bad Kissingen, Germany
,
Elisabeth Müller
1   Laboklin GmbH & Co. KG, Bad Kissingen, Germany
,
Rachel E. Marschang
1   Laboklin GmbH & Co. KG, Bad Kissingen, Germany
› Author Affiliations

Dedication

This manuscript is dedicated to the memory of Prof. Erhard F. Kaleta, who contributed greatly the study of herpesviruses in a variety of species.

Abstract

In spring 2020, a severe disease outbreak with high morbidity and mortality was observed in a collection of 15 Horsfield’s tortoises (Testudo horsfieldii). Affected tortoises showed upper respiratory- and gastrointestinal tract signs, including rhinitis and stomatitis. Testudinid herpesvirus 1 (TeHV1) and Mycoplasma spp. were detected by PCR in oral swabs of affected animals. Histological examination of one deceased animal showed intranuclear inclusion bodies typical for herpesvirus infections in liver, spleen and oesophagus. The virus was likely introduced into the collection 2 years earlier by a clinically healthy Horsfield’s tortoise that was tested positive for TeHV1 by PCR.

Zusammenfassung

Im Frühling 2020 wurde in einer Gruppe von 15 Vierzehenschildkröten (Testudo horsfieldii) ein Krankheitsausbruch mit hoher Morbidität und Mortalität beobachtet. Betroffene Tiere zeigten vorwiegend Symptome des oberen Respirations- und Gastrointestinaltrakts wie Rhinitis und Stomatitis. Mittels PCR wurden bei erkrankten Tieren das Testudinid-Herpesvirus Typ 1 (TeHV1) und Mycoplasma spp. nachgewiesen. Die histologische Untersuchung einer verstorbenen Schildkröte ergab intranukleäre Einschlusskörperchen in Leber, Niere und Ösophagus, die für eine Herpesvirusinfektion typisch waren. Das Virus wurde vermutlich bereits 2018 durch ein klinisch unauffälliges Tier, das mittels PCR TeHV1-positiv getestet wurde, in den Bestand eingetragen.

Supplementary material



Publication History

Received: 01 July 2021

Accepted: 04 October 2021

Article published online:
03 December 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Gandar F, Wilkie GS, Gatherer D. et al. The Genome of a Tortoise Herpesvirus (Testudinid Herpesvirus 3) Has a Novel Structure and Contains a Large Region That Is Not Required for Replication In Vitro or Virulence In Vivo. J Virol 2015; 89: 11438-11456
  • 2 International Committee on Taxonomy of Viruses (ICTV). Virus Taxonomy Release 2020. On the internet: https://talk.ictvonline.org/ictv-​reports/ictv_9th_report/dsdna-viruses-2011/w/dsdna_viruses/89/herpesvirales (date: 29.06.2021)
  • 3 Martel A, Blahak S, Vissenaekens H. et al. Reintroduction of clinically healthy tortoises: the herpesvirus Trojan horse. J Wildl Dis 2009; 45: 218-220
  • 4 Origgi FC, Tecilla M, Pilo P. et al. A Genomic Approach to Unravel Host-Pathogen Interaction in Chelonians: The Example of Testudinid Herpesvirus 3. PLoS One 2015; 10: e0134897
  • 5 Marschang RE. Viruses infecting reptiles. Viruses 2011; 3: 2087-2126
  • 6 Kolesnik E, Obiegala A, Marschang RE. Detection of Mycoplasma spp., herpesviruses, topiviruses, and ferlaviruses in samples from chelonians in Europe. J Vet Diagn Invest 2017; 29: 820-832
  • 7 Marschang RE, Origgi FC, Stenglein MD. et al. Viruses and viral diseases of reptiles. In: Jacobson ER, Garner MM. eds. Infectious Diseases and Pathology of Reptiles, Volume 1. Color Atlas and Text. 2nd ed.. Boca Raton: CRC Press; 2020: 575-703
  • 8 Jacobson ER, Berry KH, Wellehan JFX. et al. Serologic and molecular evidence for Testudinid herpesvirus 2 infection in wild Agassiz’s desert tortoises, Gopherus agassizii. J Wildl Dis 2012; 48: 747-757
  • 9 Johnson AJ, Pessier AP, Wellehan JFX. et al. Identification of a novel herpesvirus from a California desert tortoise (Gopherus agassizii). Vet Microbiol 2005; 111: 107-116
  • 10 Bicknese EJ, Childress AL, Wellehan JFX. A novel herpesvirus of the proposed genus Chelonivirus from an asymptomatic bowsprit tortoise (Chersina angulata). J Zoo Wildl Med 2010; 41: 353-358
  • 11 Kolesnik E, Mittenzwei F, Marschang RE. Nachweis von Testudinid-Herpesvirus Typ 4 bei einer Pantherschildkröte (Stigmochelys pardalis). Tierarztl Prax Ausg K Kleintiere Heimtiere 2016; 44: 283-286
  • 12 VanDevanter DR, Warrener P, Bennett L. et al. Detection and analysis of diverse herpesviral species by consensus primer PCR. J Clin Microbiol 1996; 34: 1666-1671
  • 13 Teifke JP, Löhr CV, Marschang RE. et al. Detection of Chelonid herpesvirus DNA by nonradioactive in situ hybridization in tissues from tortoises suffering from stomatitis-rhinitis complex in Europe and North America. Vet Pathol 2000; 37: 377-385
  • 14 Murakami M, Matsuba C, Une Y. et al. Development of species-specific PCR techniques for the detection of tortoise herpesvirus. J Vet Diagn Invest 2001; 13: 513-516
  • 15 Brown MB, McLaughlin GS, Klein PA. et al. Upper respiratory tract disease in the gopher tortoise is caused by Mycoplasma agassizii. J Clin Microbiol 1999; 37: 2262-2269
  • 16 Papp T, Spann D, Marschang RE. Development and use of a real-time polymerase chain reaction for the detection of group II invertebrate iridoviruses in pet lizards and prey insects. J Zoo Wildl Med 2014; 45: 219-227
  • 17 Stilwell NK, Whittington RJ, Hick PM. et al. Partial validation of a TaqMan real-time quantitative PCR for the detection of ranaviruses. Dis Aquat Organ 2018; 128: 105-116
  • 18 Wellehan JFX, Childress AL, Marschang RE. et al. Consensus nested PCR amplification and sequencing of diverse reptilian, avian, and mammalian orthoreoviruses. Vet Microbiol 2009; 133: 34-42
  • 19 Origgi FC, Klein PA, Mathes K. et al. Enzyme-linked immunosorbent assay for detecting herpesvirus exposure in Mediterranean tortoises (spur-thighed tortoise Testudo graeca and Hermann’s tortoise Testudo hermanni). J Clin Microbiol 2001; 39: 3156-3163
  • 20 Leineweber C, Stöhr AC, Öfner S. et al. Changes in plasma chemistry parameters in Hermann’s tortoises (Testudo hermanni) influenced by season and sex. J Herpetol Med Surg 2019; 29: 113
  • 21 Leineweber C, Stöhr AC, Öfner S. et al. Reference intervals for plasma capillary zone electrophoresis in Hermann’s tortoises (Testudo hermanni) depending on season and sex. J Zoo Wildl Med 2019; 50: 611-618
  • 22 Sheldon JD, Stacy NI, Blake S. et al. Comparison of total leukocyte quantification methods in free-living Galapagos tortoises (Chelonoidis spp.). J Zoo Wildl Med 2016; 47: 196-205
  • 23 Vetere A, Bertocchi M, Pelizzone I. et al. Cytobrushing of the oral mucosa as a possible tool for early detection of testudinid herpesvirus in Horsfield’s tortoises with nonspecific clinical signs. J Vet Diagn Invest 2021; 33 (01) 116-119
  • 24 Soares JF, Chalker VJ, Erles K. et al. Prevalence of Mycoplasma agassizii and Chelonian herpesvirus in captive tortoises (Testudo sp.) in the United Kingdom. J Zoo Wildl Med 2004; 35: 25-33
  • 25 Salinas M, Francino O, Sánchez A. et al. Mycoplasma and herpesvirus PCR detection in tortoises with rhinitis-stomatitis complex in Spain. J Wildl Dis 2011; 47: 195-200
  • 26 Jacobson ER, Brown MB, Wendland LD. et al. Mycoplasmosis and upper respiratory tract disease of tortoises: a review and update. Vet J 2014; 201: 257-264
  • 27 Une Y, Uemura K, Nakano Y. et al. Herpesvirus infection in tortoises (Malacochersus tornieri and Testudo horsfieldii). Vet Pathol 1999; 36: 624-627
  • 28 Marschang RE. Isolierung und Charakterisierung von Irido-, Herpes- und Reoviren aus Landschildkröten sowie Beschreibung eines nicht charakterisierten zytopathogenen Agens [Dissertation]. Gießen: Justus-Liebig-Universität; 2000
  • 29 Stöhr AC, Marschang RE. Detection of a Tortoise Herpesvirus Type 1 in a Hermann’s Tortoise (Testudo hermanni boettgeri) in Germany. J Herpetol Med Surg 2010; 20: 61
  • 30 Origgi FC, Tecilla M. Immunology in reptiles. In: Jacobson ER, Garner MM. eds. Infectious Diseases and Pathology of Reptiles, Volume 1. Color Atlas and Text. 2nd ed.. Boca Raton: CRC Press; 2020: 215-266
  • 31 Haines H, Kleese WC. Effect of water temperature on a herpesvirus infection of sea turtles. Infect Immun 1977; 15: 756-759
  • 32 Marenzoni ML, Santoni L, Felici A. et al. Clinical, virological and epidemiological characterization of an outbreak of Testudinid Herpesvirus 3 in a chelonian captive breeding facility: Lessons learned and first evidence of TeHV3 vertical transmission. PLoS One 2018; 13: e0197169
  • 33 Origgi FC, Romero CH, Bloom DC. et al. Experimental transmission of a herpesvirus in Greek tortoises (Testudo graeca). Vet Pathol 2004; 41: 50-61
  • 34 Marschang RE, Milde K, Bellavista M. Virus isolation and vaccination of Mediterranean tortoises against a chelonid herpesvirus in a chronically infected population in Italy. Dtsch Tierarztl Wochenschr 2001; 108 (09) 376-379
  • 35 Steiner MA. Epiddemiologische Studien zur Kinetik von Herpesvirusantikörpern und Ausscheidung von Herpesviren in Beständen Europäischer Landschildkröten [Dissertation]. Gießen: Fachbereich der Veterinärmedizin der Justus-Liebig-Universität Gießen; 2010
  • 36 Hervas J, Sánchez-Cordón PJ, de Chacón Lara F. et al. Hepatitis associated with herpes viral infection in the tortoise (Testudo horsfieldii). J Vet Med B Infect Dis Vet Public Health 2002; 49 (02) 111-114
  • 37 Moore AR, Allender MC, MacNeill AL. Effects of ranavirus infection of red-eared sliders (Trachemys scripta elegans) on plasma proteins. J Zoo Wildl Med 2014; 45: 298-305
  • 38 Wellehan JFX, Divers SJ. Bacteriology. In: Divers SJ, Stahl SJ. eds. Mader’s Reptile and Amphibian Medicine and Surgery. 3rd ed.. Philadelphia: Saunders; 2019: 235-246
  • 39 Gandar F, Marlier D, Vanderplasschen A. In vitro and in vivo assessment of eprociclovir as antiviral treatment against testudinid herpesvirus 3 in Hermann’s tortoises (Testudo hermanni). Res Vet Sci 2019; 124: 20-23
  • 40 Marschang RE. Antiviral therapy. In: Divers SJ, Stahl SJ. eds. Mader’s Reptile and Amphibian Medicine and Surgery. 3rd ed.. Philadelphia: Saunders; 2019: 1160-1161
  • 41 Knotková Z, Doubek J, Knotek Z. et al. Blood cell morphology and plasma biochemistry in Russian tortoises (Agrionemys horsfieldii). Acta Vet Brno 2002; 71: 191-198