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Volume 27, Number 7—July 2021
Research Letter

Possible Human-to-Dog Transmission of SARS-CoV-2, Italy, 2020

Nicola DecaroComments to Author , Gabriele Vaccari, Alessio Lorusso, Eleonora Lorusso, Luca De Sabato, Edward I. Patterson, Ilaria Di Bartolo, Grant L. Hughes, Liana Teodori, Costantina Desario, Barbara Colitti, Dominga Ricci, Domenico Buonavoglia, Sergio Rosati, Vito Martella, Cesare Cammà, Umberto Agrimi, and Gabriella Elia
Author affiliations: University of Bari, Valenzano, Italy (N. Decaro, E. Lorusso, C. Desario, D. Buonavoglia, V. Martella, G. Elia); Istituto Superiore di Sanità, Rome, Italy (G. Vaccari, L. De Sabato, I. Di Bartolo, U. Agrimi); Istituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise “G. Caporale,” Teramo, Italy (A. Lorusso, L. Teodori, C. Cammà); Liverpool School of Tropical Medicine, Liverpool, UK (E.I. Patterson, G.L. Hughes); University of Turin, Turin, Italy (B. Colitti, S. Rosati); Ambulatorio Veterinario Dott.ssa Ricci Dominga, Andria, Italy (D. Ricci)

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Abstract

We detected severe acute respiratory syndrome coronavirus 2 in an otherwise healthy poodle living with 4 family members who had coronavirus disease. We observed antibodies in serum samples taken from the dog, indicating seroconversion. Full-length genome sequencing showed that the canine and human viruses were identical, suggesting human-to-animal transmission.

Coronavirus disease (COVID-19), caused by infection with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), emerged in humans in Wuhan, China, in late December 2019, probably because of spillover from an unidentified animal host (1). Dogs and cats, to which some coronaviruses are endemic (2), are also susceptible to SARS-CoV-2 infection (3,4). Although the spread of SARS-CoV-2 is maintained mainly by human-to-human transmission, the epidemiologic implications of animal susceptibility remain uncertain (4). We characterized the full genome of a SARS-CoV-2 isolate detected in a dog.

A female poodle, who was 1.5 years of age, lived with 4 family members in Bitonto, Italy. All family members had signs and symptoms of COVID-19, the illness caused by SARS-CoV-2 infection. High temperature (37.5°C–38.5°C), coughing, anosmia, and ageusia developed in the mother, who was 54 years of age, on October 31, 2020. The woman tested positive for SARS-CoV-2 by a rapid antigen test conducted on November 3, 2020. The local health authority collected nasopharyngeal swab samples and used molecular testing to confirm SARS-CoV-2 infection in the woman’s husband and 2 daughters. Clinical signs in the other family members ranged from mild fatigue and high temperatures (37.5°C–37.8°C) in the daughters to moderate respiratory signs and persistent high temperature (37.8°C–38.6°C) in the husband. This study was approved by the Ethics Committee of the Department of Veterinary Medicine at the University of Bari (approval no. 15/2020).

On November 4, 2020, the owners collected oral and nasal swab samples from the family’s poodle according to our instructions. The pooled samples tested positive for SARS-CoV-2 by real-time reverse transcription PCR selective for the N gene (5). During the next 11 days, the owners collected nasal, oral, and rectal swab samples from the dog. Of 20 samples collected during November 6–15, a total of 4 samples (all of which were collected during November 6–9) tested positive for SARS-CoV-2 (Table). Viral shedding occurred at low titers. We did not isolate the virus. The dog did not show any clinical signs, and no other pets lived in the household.

We tested a serum sample collected by the dog’s veterinarian on November 27 with 2 commercial multispecies ELISA tests: ID Screen SARS-CoV-2 Double Antigen Multi-species ELISA (ID.vet, https://www.id-vet.com) and Eradikit COVID19-Multispecies (In3Diagnostic, http://www.in3diagnostic.com). We also conducted a plaque reduction neutralization test (PRNT) (4) and a virus neutralization test (VNT) (6). We detected antibodies with the Eradikit (23%), PRNT (1:80), and VNT (1:10). We used serologic assays to confirm the presence of antibodies against SARS-CoV-2 in an additional serum sample collected on December 12, 2020; the antibody titers were 1:80 for PRNT and 1:20 for VNT (Table).

Figure

Maximum-likelihood tree comparing 108 strains of severe acute respiratory syndrome coronavirus 2 circulating among humans and canines. Tree shows 107 complete genomes downloaded from the GISAID database (https://www.gisaid.org) and the strains sequenced from an infected dog and family member in Italy (bold red text). The tree was built with IQ-TREE version 1.6.10 (http://www.iqtree.org) using the best fit model indicated by the Model Finder with 1,000 bootstrap replicates. Text at nodes indicates bootstrap values >70. Brackets to the right indicate clades. Scale bar indicates number of nucleotide substitutions per site.

Figure. Maximum-likelihood tree comparing 108 strains of severe acute respiratory syndrome coronavirus 2 circulating among humans and canines. Tree shows 107 complete genomes downloaded from the GISAID database (https://www.gisaid.org)...

We submitted the positive pooled oral and nasal swab samples from the dog and the oropharyngeal swab sample from the index patient, all of which were collected on November 4, for next-generation sequencing (7). Next-generation sequencing obtained total reads of 929,736 with a mean coverage of 4,300× for the index patient and 969,837 with a mean coverage of 1,800× for the dog. Complete genomes were obtained using the pipeline SARS-CoV-2 RECoVERY in the Galaxy public server ARIES (Istituto Superiore di Sanità, https://w3.iss.it/site/aries). The 2 SARS-CoV-2 genomes shared 100% nucleotide identity. The Pangolin COVID-19 Lineage Assigner (https://pangolin.cog-uk.io) and Nextclade (https://clades.nextstrain.org) assigned the sequences to the lineage B.1.177 (denoted by Nextclade as 20A.EU1) in Europe. Phylogenetic analysis confirmed the clustering of the 2 strains within the GV clade and the B.1.177 lineage already detected in Italy (Figure).

Despite the massive number of persons with SARS-CoV-2, only a few cases of active infection in pets have been reported (3). SARS-CoV-2–specific antibodies in pets have been reported on a few occasions, and higher seroprevalence rates have been found in animals from households in which family members have COVID-19 (4,6,8). The scarce reports of natural infection in dogs reflect their low susceptibility to SARS-CoV-2; for this infection, dogs are asymptomatic, produce limited titers, and have a reduced duration of viral shedding (9). Upon experimental infection, dogs shed SARS-CoV-2 at lower titers and for a shorter period than cats (10). Patterson et al. (4) found no actively infected dog or cat in a sampled population of 494 pets, including 67 dogs from households in which family members had COVID-19; however, SARS-CoV-2–specific antibodies were detected in a small proportion of pets (4). Delayed sampling of animals, caused by restrictions on human and animal movement during the pandemic, probably contributed to the negative results of molecular testing in that study. The infected poodle we report was monitored after the identification of the index case in the family, enabling the detection of SARS-CoV-2 RNA in swab samples collected during the observational follow-up. Because the canine virus shared 100% nucleotide identity with the virus detected in the index case, we believe human-to-dog transmission of the virus probably occurred in the household.

Dr. Decaro is professor in the Department of Veterinary Medicine at the University of Bari in Valenzano, Italy. His research interests include the study of viral pathogens of dogs and cats, especially coronaviruses and parvoviruses.

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Acknowledgments

We are grateful to Maria Stella Lucente, Cristiana Catella, Carlo Armenise, and Arturo Gentile for their excellent technical assistance. We thank Marco Crescenzi, Manuela Marra, and Maria Carollo for the Next Generation Sequencing through Ion GeneStudio S5 System.

N.D. was supported by grants of Fondazione CARIPLO—Misura a sostegno dello sviluppo di collaborazioni per l’identificazione di terapie e sistemi di diagnostica, protezione e analisi per contrastare l’emergenza Coronavirus e altre emergenze virali del future, project “Genetic characterization of SARS-CoV2 and serological investigation in humans and pets to define cats and dogs role in the COVID-19 pandemic (COVIDinPET)”. A.L was supported by the Italian Ministry of Health Ricerca Corrente 2020 "PanCO: epidemiologia e patogenesi dei coronavirus umani ed animali" and Ricerca Strategica 2020 “Suscettibilità dei mammiferi a SARS-COV-2: rischi di zoonosi inversa e possibilità in medicina traslazionale."

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References

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DOI: 10.3201/eid2707.204959

Original Publication Date: May 12, 2021

Table of Contents – Volume 27, Number 7—July 2021

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Nicola Decaro, Department of Veterinary Medicine, University of Bari, Strada provinciale per Casamassima Km 3, 70010 Valenzano (Bari), Italy

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