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Published in: Virology Journal 1/2023

Open Access 01-12-2023 | Research

Co-infection of distinct papillomavirus types in a captive North American porcupine

Authors: Bert Vanmechelen, Jennifer Lahoreau, Philippine Dendauw, Alexandra Nicolier, Piet Maes

Published in: Virology Journal | Issue 1/2023

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Abstract

Background

Only two cases of papillomavirus infections in North American porcupines (Erethizon dorsatum) have been described thus far, and molecular investigation linked these cases to two distinct papillomavirus species.

Methods

In this report, we present the clinical, histological and molecular investigation of a third case of a porcupine papillomavirus infection. Papillomatous lesions occurred on the upper and lower lip of an otherwise healthy three-year old female that was kept in captivity. Within one month, the lesions progressed into exophytic black nodules, followed by a temporary stabilization and ultimately spontaneous regression within seven months of their initial observation. PCR-based screening using specific primers for Erethizon dorsatum papillomavirus 1 and 2 revealed the presence of both these virus types, after which nanopore sequencing was used to determine the complete sequences of the two virus genomes.

Results

One of the genomes shares 99.9% similarity with the only known sequence for Erethizon dorsatum papillomavirus 1, while the second represents a distinct lineage of Erethizon dorsatum papillomavirus 2, sharing only 93.3% similarity with the previously discovered strain.

Conclusions

This report marks the first observation of a papillomavirus co-infection in a North American porcupine, although the individual contribution of the two virus types to the clinical presentation was not assessed.
Literature
1.
go back to reference Van Doorslaer K, Chen Z, Bernard H-U, Chan PKS, DeSalle R, Dillner J, et al. ICTV virus taxonomy profile: papillomaviridae. J Gen Virol. 2018;99(8):989–90.CrossRef Van Doorslaer K, Chen Z, Bernard H-U, Chan PKS, DeSalle R, Dillner J, et al. ICTV virus taxonomy profile: papillomaviridae. J Gen Virol. 2018;99(8):989–90.CrossRef
2.
go back to reference Bolatti EM, Viarengo G, Zorec TM, Cerri A, Montani ME, Hosnjak L, et al. Viral metagenomic data analyses of five new world bat species from Argentina: identification of 35 novel DNA viruses. Microorganisms. 2022;10(2):266.CrossRef Bolatti EM, Viarengo G, Zorec TM, Cerri A, Montani ME, Hosnjak L, et al. Viral metagenomic data analyses of five new world bat species from Argentina: identification of 35 novel DNA viruses. Microorganisms. 2022;10(2):266.CrossRef
3.
go back to reference McBride AA. Human papillomaviruses: diversity, infection and host interactions. Nat Rev Microbiol. 2022;20(2):95–108.CrossRef McBride AA. Human papillomaviruses: diversity, infection and host interactions. Nat Rev Microbiol. 2022;20(2):95–108.CrossRef
4.
go back to reference Cubie HA. Diseases associated with human papillomavirus infection. Virology. 2013;445(1):21–34.CrossRef Cubie HA. Diseases associated with human papillomavirus infection. Virology. 2013;445(1):21–34.CrossRef
5.
go back to reference Van Doorslaer K, Li Z, Xirasagar S, Maes P, Kaminsky D, Liou D, et al. The Papillomavirus Episteme: a major update to the papillomavirus sequence database. Nucleic Acids Res. 2016;45(D1):D499–506.CrossRef Van Doorslaer K, Li Z, Xirasagar S, Maes P, Kaminsky D, Liou D, et al. The Papillomavirus Episteme: a major update to the papillomavirus sequence database. Nucleic Acids Res. 2016;45(D1):D499–506.CrossRef
6.
go back to reference Van Doorslaer K. Evolution of the papillomaviridae. Virology. 2013;445(1):11–20.CrossRef Van Doorslaer K. Evolution of the papillomaviridae. Virology. 2013;445(1):11–20.CrossRef
7.
go back to reference Dolz G, Lecis R, Solorzano-Morales A, Aguilar-Vargas F, Solorzano-Scott T, Pena R, et al. Leopardus wiedii Papillomavirus type 1, a novel papillomavirus species in the tree ocelot, suggests Felidae Lambdapapillomavirus polyphyletic origin and host-independent evolution. Infect Genet Evol. 2020;81:104239.CrossRef Dolz G, Lecis R, Solorzano-Morales A, Aguilar-Vargas F, Solorzano-Scott T, Pena R, et al. Leopardus wiedii Papillomavirus type 1, a novel papillomavirus species in the tree ocelot, suggests Felidae Lambdapapillomavirus polyphyletic origin and host-independent evolution. Infect Genet Evol. 2020;81:104239.CrossRef
8.
go back to reference Gottschling M, Goker M, Stamatakis A, Bininda-Emonds OR, Nindl I, Bravo IG. Quantifying the phylodynamic forces driving papillomavirus evolution. Mol Biol Evol. 2011;28(7):2101–13.CrossRef Gottschling M, Goker M, Stamatakis A, Bininda-Emonds OR, Nindl I, Bravo IG. Quantifying the phylodynamic forces driving papillomavirus evolution. Mol Biol Evol. 2011;28(7):2101–13.CrossRef
9.
go back to reference Vanmechelen B, Maes RK, Sledge DG, Lockwood SL, Schwartz SL, Maes P. Genomic characterization of Erethizon dorsatum papillomavirus 2, a new papillomavirus species marked by its exceptional genome size. J Gen Virol. 2018;99(12):1699–704.CrossRef Vanmechelen B, Maes RK, Sledge DG, Lockwood SL, Schwartz SL, Maes P. Genomic characterization of Erethizon dorsatum papillomavirus 2, a new papillomavirus species marked by its exceptional genome size. J Gen Virol. 2018;99(12):1699–704.CrossRef
10.
go back to reference Schwartz S, Lockwood SL, Sledge D, Maes RK, Wise AG. Diagnosis and treatment of a novel papillomavirus in a North American porcupine (Erethizon dorsatum). Vet Rec Case Rep. 2018;6(2):e000609.CrossRef Schwartz S, Lockwood SL, Sledge D, Maes RK, Wise AG. Diagnosis and treatment of a novel papillomavirus in a North American porcupine (Erethizon dorsatum). Vet Rec Case Rep. 2018;6(2):e000609.CrossRef
11.
go back to reference Rector A, Tachezy R, Van Doorslaer K, MacNamara T, Burk RD, Sundberg JP, et al. Isolation and cloning of a papillomavirus from a North American porcupine by using multiply primed rolling-circle amplification: the Erethizon dorsatum papillomavirus type 1. Virology. 2005;331(2):449–56.CrossRef Rector A, Tachezy R, Van Doorslaer K, MacNamara T, Burk RD, Sundberg JP, et al. Isolation and cloning of a papillomavirus from a North American porcupine by using multiply primed rolling-circle amplification: the Erethizon dorsatum papillomavirus type 1. Virology. 2005;331(2):449–56.CrossRef
12.
go back to reference Campo MS. Papillomavirus and disease in humans and animals. Vet Comp Oncol. 2003;1(1):3–14.CrossRef Campo MS. Papillomavirus and disease in humans and animals. Vet Comp Oncol. 2003;1(1):3–14.CrossRef
13.
go back to reference Sundberg JP. Papillomavirus infections in animals. In: Syrjänen KJ, Gissmann L, Koss LG, editors. Papillomaviruses and human disease. Berlin Heidelberg: Springer; 1987. p. 40–103.CrossRef Sundberg JP. Papillomavirus infections in animals. In: Syrjänen KJ, Gissmann L, Koss LG, editors. Papillomaviruses and human disease. Berlin Heidelberg: Springer; 1987. p. 40–103.CrossRef
14.
go back to reference Roperto S, Cutarelli A, Corrado F, De Falco F, Buonavoglia C. Detection and quantification of bovine papillomavirus DNA by digital droplet PCR in sheep blood. Sci Rep. 2021;11(1):10292.CrossRef Roperto S, Cutarelli A, Corrado F, De Falco F, Buonavoglia C. Detection and quantification of bovine papillomavirus DNA by digital droplet PCR in sheep blood. Sci Rep. 2021;11(1):10292.CrossRef
15.
go back to reference De Falco F, Cutarelli A, D’Alessio N, Cerino P, Catoi C, Roperto S. Molecular epidemiology of ovine papillomavirus infections among sheep in southern Italy. Front Vet Sci. 2021;8:790392.CrossRef De Falco F, Cutarelli A, D’Alessio N, Cerino P, Catoi C, Roperto S. Molecular epidemiology of ovine papillomavirus infections among sheep in southern Italy. Front Vet Sci. 2021;8:790392.CrossRef
16.
go back to reference Lange CE, Jennings SH, Diallo A, Lyons J. Canine papillomavirus types 1 and 2 in classical papillomas: high abundance, different morphological associations and frequent co-infections. Vet J (London England: 1997). 2019;250:1–5.CrossRef Lange CE, Jennings SH, Diallo A, Lyons J. Canine papillomavirus types 1 and 2 in classical papillomas: high abundance, different morphological associations and frequent co-infections. Vet J (London England: 1997). 2019;250:1–5.CrossRef
17.
go back to reference Mira J, Herman M, Zakia LS, Olivo G, Araújo JP Jr, Borges AS, et al. Frequency of Equus caballus papillomavirus in equine aural plaques. J Vet Diagn Investig. 2018;30(4):565–8.CrossRef Mira J, Herman M, Zakia LS, Olivo G, Araújo JP Jr, Borges AS, et al. Frequency of Equus caballus papillomavirus in equine aural plaques. J Vet Diagn Investig. 2018;30(4):565–8.CrossRef
18.
go back to reference Savini F, Dal Molin E, Gallina L, Casà G, Scagliarini A. Papillomavirus in healthy skin and mucosa of wild ruminants in the Italian alps. J Wildl Dis. 2016;52(1):82–7.CrossRef Savini F, Dal Molin E, Gallina L, Casà G, Scagliarini A. Papillomavirus in healthy skin and mucosa of wild ruminants in the Italian alps. J Wildl Dis. 2016;52(1):82–7.CrossRef
19.
go back to reference Daudt C, da Silva FRC, Streck AF, Weber MN, Mayer FQ, Cibulski SP, et al. How many papillomavirus species can go undetected in papilloma lesions? Sci Rep. 2016;6:36480.CrossRef Daudt C, da Silva FRC, Streck AF, Weber MN, Mayer FQ, Cibulski SP, et al. How many papillomavirus species can go undetected in papilloma lesions? Sci Rep. 2016;6:36480.CrossRef
20.
go back to reference da Silva MA, Carvalho CC, Coutinho LC, Reis MC, de Aragão Batista MV, de Castro RS, et al. Co-infection of Bovine Papillomavirus and feline-associated Papillomavirus in bovine cutaneous warts. Transbound Emerg Dis. 2012;59(6):539–43.CrossRef da Silva MA, Carvalho CC, Coutinho LC, Reis MC, de Aragão Batista MV, de Castro RS, et al. Co-infection of Bovine Papillomavirus and feline-associated Papillomavirus in bovine cutaneous warts. Transbound Emerg Dis. 2012;59(6):539–43.CrossRef
21.
go back to reference Khalafalla AI, Ramadan RO, Rector A, Barakat S. Investigation on papillomavirus infection in dromedary camels in Al-Ahsa, Saudi Arabia. Open Vet J. 2017;7(2):174–9.CrossRef Khalafalla AI, Ramadan RO, Rector A, Barakat S. Investigation on papillomavirus infection in dromedary camels in Al-Ahsa, Saudi Arabia. Open Vet J. 2017;7(2):174–9.CrossRef
22.
go back to reference Rector A, Bossart GD, Ghim S-J, Sundberg JP, Jenson AB, Ranst MV. Characterization of a novel close-to-root papillomavirus from a florida manatee by using multiply primed rolling-circle amplification: trichechus manatus latirostris papillomavirus type 1. J Virol. 2004;78(22):12698–702.CrossRef Rector A, Bossart GD, Ghim S-J, Sundberg JP, Jenson AB, Ranst MV. Characterization of a novel close-to-root papillomavirus from a florida manatee by using multiply primed rolling-circle amplification: trichechus manatus latirostris papillomavirus type 1. J Virol. 2004;78(22):12698–702.CrossRef
23.
go back to reference Forslund O, Antonsson A, Nordin P, Stenquist B, Hansson BG. A broad range of human papillomavirus types detected with a general PCR method suitable for analysis of cutaneous tumours and normal skin. J Gen Virol. 1999;80(9):2437–43.CrossRef Forslund O, Antonsson A, Nordin P, Stenquist B, Hansson BG. A broad range of human papillomavirus types detected with a general PCR method suitable for analysis of cutaneous tumours and normal skin. J Gen Virol. 1999;80(9):2437–43.CrossRef
24.
go back to reference Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 2017;27(5):722–36.CrossRef Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 2017;27(5):722–36.CrossRef
25.
go back to reference Pace J, Youens-Clark K, Freeman C, Hurwitz B, Van Doorslaer K. PuMA: a papillomavirus genome annotation tool. Virus Evolut. 2020;6(2):veaa068.CrossRef Pace J, Youens-Clark K, Freeman C, Hurwitz B, Van Doorslaer K. PuMA: a papillomavirus genome annotation tool. Virus Evolut. 2020;6(2):veaa068.CrossRef
26.
go back to reference Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evolut. 2016;33(7):1870–4.CrossRef Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evolut. 2016;33(7):1870–4.CrossRef
27.
go back to reference Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform. 2004;5:113.CrossRef Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform. 2004;5:113.CrossRef
28.
go back to reference Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, et al. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol. 1999;73(1):152–60.CrossRef Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, et al. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol. 1999;73(1):152–60.CrossRef
Metadata
Title
Co-infection of distinct papillomavirus types in a captive North American porcupine
Authors
Bert Vanmechelen
Jennifer Lahoreau
Philippine Dendauw
Alexandra Nicolier
Piet Maes
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2023
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-023-01972-w

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