Detection of SARS-CoV-2 in rectal swabs from dogs and cats in São João de Meriti, Rio de Janeiro, BrazilABSTRACT:
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infections have been reported in humans and various wild and domestic animals. The potential for SARS-CoV-2 transmission has been demonstrated in animal models. This study focused on the prevalence of SARS-CoV-2 RNA in domestic dogs and cats in São João de Meriti, Rio de Janeiro, Brazil.This study investigated the potential for domestic dogs and cats to be infected with SARS-CoV-2. Rectal swabs were collected from dogs and cats during routine veterinary visits between December 2020 and June 2021. Viral RNA was detected by real-time PCR, and Sanger sequencing was used to access the viral genome. A total of 650 samples were analyzed, with 48 (7.4%) testing positive for SARS-CoV-2. The positivite rate was 7.7% in dogs and 8.3% in cats. Fourteen animals exhibited clinical signs resembling COVID-19, the most prevalent being lack of appetite, vomiting, and diarrhea. The highest number of positive cases was observed in January 2021. One sample was successfully sequenced and identified as the Gamma (P.1) lineage. To the author’s knowledge, this is the largest Brazilian survey of SARS-CoV-2 in animals. It suggested that dogs and cats might be without clinical signs or present with mild clinical signs. There is no evidence that dogs and cats can spread SARS-CoV-2 back to humans.
Key words:
COVID-19; household animals; rectal swabs; dogs and cats
RESUMO:
As infecções pelo coronavírus da síndrome respiratória aguda grave 2 (SARS-CoV-2) foram relatadas não apenas em humanos, mas também em vários animais selvagens e domésticos. O potencial de transmissão do SARS-CoV-2 foi demonstrado em modelos animais. Este estudo enfoca a prevalência do RNA do SARS-CoV-2 em cães e gatos domésticos em São João de Meriti, Rio de Janeiro, Brasil. O objetivo deste estudo foi investigar o potencial de infecção de cães e gatos domésticos pelo SARS-CoV-2. Foram coletados swabs retais de cães e gatos durante visitas veterinárias de rotina entre dezembro de 2020 a junho de 2021. O RNA viral foi detectado por PCR em tempo real, e o sequenciamento de Sanger foi usado para analisar o genoma viral. Um total de 650 amostras foram analisadas, sendo 48 (7,4%) positivas para SARS-CoV-2. A taxa de positividade foi de 7,7% em cães e 8,3% em gatos. Quatorze animais apresentaram sinais clínicos semelhantes aos da COVID-19, sendo os mais prevalentes a falta de apetite, vômitos e diarreia. O maior número de casos positivos foi observado em janeiro de 2021. Uma amostra foi sequenciada com sucesso e identificada como pertencente à linhagem Gamma (P.1). No conhecimento dos autores, esta é a maior pesquisa brasileira sobre o SARS-CoV-2 em animais e sugere que os animais de estimação podem ser sem sinais clínicos ou apresentar sinais clínicos leves. Não há evidências de que cães e gatos possam disseminar o SARS-CoV-2 para os seres humanos.
Palavras-chave:
COVID-19; animais domésticos; swab retal; cães e gatos
INTRODUCTION
The novel coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2), emerged in December 2019 in Wuhan, China (HU et al., 2020; TANG et al., 2020). In Brazil, the first case of COVID-19 was recorded on 26 February 2020 in the state of São Paulo, affecting a 61-year-old man with a travel history to Italy (MELO et al., 2020).
SARS-CoV-2 infections have been reported not only in humans but also in a range of wild and domestic animals, such as nonhuman primates (GONÇALVES et al., 2021), deers (FENG et al., 2023), minks (OUDE MUNNINK et al., 2021), ferrets (RAČNIK et al., 2021), hamsters (SIA et al., 2020), lions (DUSSELDORP et al., 2023), cats and dogs (CUI et al., 2022; SHI et al., 2020; DE SOUZA BARBOSA et al., 2022). Various animal models have demonstrated the potential for SARS-CoV-2 transmission through direct contact, fomites, and aerosol (YEN et al., 2022). Although uncommon, animal-to-human transmission has been described in the literature, including cases of minks (OUDE MUNNINK et al., 2021), hamsters (YEN et al., 2022), and a cat (SILA et al., 2022) infecting their caretakers.
The close and continuous contact between domestic animals and their owners makes them a potential transmission source for some infectious diseases. Therefore, studying SARS-CoV-2 prevalence in the domestic environment is essential in understanding the viral dynamics and their impact on humans’ and animals’ individual and collective health. Epidemiological and longitudinal studies have commonly considered a small number of animals (CALVET et al., 2021; DILEEPAN et al., 2021; SIT et al., 2020). This study explored the prevalence of SARS-CoV-2 RNA in a larger sample size of domestic dogs and cats from São João de Meriti, the 8th most populous municipality (IBGE, 2020) of Rio de Janeiro, Brazil.
MATERIALS AND METHODS
Population and sample collection
The animals selected for this study were household dogs and cats from untested or without clinical signs tutors who attended routine veterinary appointments without discrimination regarding breed, age, or sex. The samples were collected by trained staff at a veterinary clinic in São João de Meriti, RJ, Brazil. Rectal swabs were collected, and samples were maintained in a Dulbecco′s Modified Eagle′s Medium (D777 - Sigma®) and stored at -20 °C (FERNÁNDEZ-BASTIT et al., 2021). Samples were collected and sent to the laboratory every week from December 2020 to June 2021.
RNA isolation and RT-PCR
Viral RNA was isolated using the Maxwell® 16 Viral Total Nucleic Acid Extraction Kit (Promega®), followed by detection of SARS-CoV-2 using the Fiocruz kit (Biomanguinhos, Rio de Janeiro, Brazil) in QuantStudio 5 real-time PCR system (Life Technologies®, CA).
In addition to providing technical training to our collaborating veterinarians on swab collection procedures, we used controls throughout the viral RNA isolation process. Specifically, for each set of samples, a swab containing only culture medium was processed as a negative control to reduce the risk of contamination. In addition, negative controls were incorporated during the RT-qPCR assays using nuclease-free water to confirm that any amplifications observed were attributable exclusively to the presence of SARS-CoV-2 genetic material. Together, these measures increase the accuracy of sample diagnoses, reducing the potential for false positive results.
Viral genome sequencing
Nested PCR reactions were conducted to amplify a region of the Wuhan-Hu-1 SARS-CoV-2 S gene (GENBANK acc# MN908947) using primers from the ARTIC network nCov-2019 V.3 primer set (ARTIC NETWORK, 2020). Sanger technology purified and sequenced PCR products using an automated ABI 3130xl Genetic Analyzer (THERMO FISHER SCIENTIFIC). Additional inner primers were included to cover the entire amplified region. Sequences were assembled to the Wuhan-Hu-1 SARS-CoV-2 S gene and edited with the Lasergene package (DNAStar, inc., Madison, WI).
RESULTS
Clinical signs
This study analyzed six hundred and fifty samples from December 2020 to June 2021. Of these, 436 (67.1%) were dogs, 132 (20.3%) were cats, and 82 (12.6%) whose species were not identified. Of the 650 samples, 590 (90.8%) were negative and 48 (7.4%) were positive for SARS-CoV-2. The positivity rate among dogs was 7.7% (33/436), while cats were 8.3% (11/132).
It was possible to retrieve clinical sign related information exclusively from some of the animals that tested positive for SARS-CoV-2, with 14 out of the 48 positive cases (1 cat and 13 dogs) exhibiting clinical signs (Figure 1). The most prevalent clinical sign observed was lack of appetite, affecting 5/14 (35.7%) animals. This was followed by vomiting and diarrhea, which affected 4/14 animals each (28.6%). Prostration was the most common clinical sign in 3/14 animals (21.4%). Cough was reported by 2/14 animals (14.3%), while other clinical signs such as somnolence, slimming, convulsion, cardiac changes, and abdominal pain each affected 1/14 (7.1%) animals (Figure 1). Figure 2 shows the percentages of samples analyzed and positive cases of covid-19 in dogs and cats compared to cases in humans.
Overview of clinical signs presented by the 14 animals (1 cat and 13 dogs) positive for SARS-CoV-2.
Graph showing the percentage of COVID-19 cases per epidemiological week for the dogs and cats (PETS) studied compared with human cases in São João de Meriti (SJM). Data obtained from the DATASUS - Tabnet system of the Brazilian Ministry of Health.
The tested samples’ cycle threshold (Ct) values ranged from 29 to 39 (Table 1). However, no difference was found between animals with and without clinical signs (P > 0.05).
SARS-CoV-2 lineage classification
Eighteen samples positive for SARS-CoV-2 were submitted to PCR to obtain the partial sequence of the Spike gene. However, only one sample (VET176) could be successfully amplified and sequenced, possibly due to the low Ct value (29) (Table 1) during diagnostics. Phylogenetic analysis classified the sample as belonging to the Gamma (P.1) lineage (Figure 3). The sample was isolated from a cat without clinical signs diagnosed in September 2021. The sequencing data is available at GISAID under ID EPI_ISL_6470123.
Maximum likelihood (ML) phylogenetic reconstruction of SARS-CoV-2 partial Spike gene sequence (VET176). To create the dataset, 87 representative sequences from different strains of the virus were retrieved from the GISAID database. The sequence described in this study (red arrow) evinces similarities to the VOC Gamma (P.1) sequences and is available at GISAID under ID EPI_ISL_6470123.
DISCUSSION
The pandemic of the 2019 novel coronavirus has brought up several questions about the mechanism of infection and clinical manifestations of the disease. The potential for dogs and cats to be infected by SARS-CoV-2 has raised concerns within the scientific community. Due to reports of infections in dogs and cats, research has been conducted to investigate cellular pathways in these animals that may be similar to those observed in humans.
The angiotensin-converting enzyme 2 (ACE2) acts as a functional receptor for the SARS-CoV-2 spike (S) protein, playing a critical role in the entry of the virus into the host cell (NI et al., 2020; GHEWARE et al., 2022). The ACE2 from different animals can interact with the SARS-CoV-2 S protein similarly to humans (ZHAO et al., 2020; PACH et al., 2021; WANG et al., 2023). The ACE-2 receptor shares 77% genetic identity between humans and dogs, and 86% between humans and cats, which may explain the higher susceptibility of cats to SARS-CoV-2 infection (DE MORAIS et al., 2020).
There is evidence that SARS-CoV exhibits tropism in the gastrointestinal site, which can be detected in intestinal biopsy and stool samples (LEUNG et al., 2003). The presence of SARS-CoV-2 RNA in rectal swabs is an attractive diagnostic approach since they may remain positive even after negative conversion of nasopharyngeal RT-PCR test (KIPKORIR et al., 2020; WANG et al., 2020; CALVET et al., 2021). However, there are reports of difficulties in identifying SARS-CoV-2 in rectal swab samples, some even in animals with high viral load (RUIZ-ARRONDO et al., 2021). A fundamental limitation of this study is that, although the detection of oropharyngeal/nasal samples of SARS-CoV-2 could provide a more comprehensive understanding of the infection, here it was only possible to obtain rectal swab samples due to their better acceptance by the animals and their owners at the time. Consequently, it was impossible to access serological data from the animals, which could have enhanced the results.
Consistent with what has been observed in the literature, most infected animals were without clinical signs. An American study has shown that only 17.6% of the SARS-CoV-2-positive animals had mild disease clinical signs such as sneezing, fever, and lethargy (HAMER et al., 2020). Despite the literature data pointing to a higher susceptibility of felines to present COVID-related clinical signs, only one cat in this study had clinical signs, presenting prostration and lack of appetite. Although, the clinical signs coincided with the viral infection in the animals, the lack of additional tests to rule out co-infections with other pathogens limits the ability to determine if the SARS-CoV-2 infection caused the clinical signs. In this study, clinical signs data were unavailable for all pets due to inconsistent reporting by veterinarians, leading to a focus on animals that tested positive for SARS-CoV-2. This selective approach may introduce bias in interpreting clinical signs causality, as data from negative or untested cases were lacking, potentially affecting the generalizability and accuracy of the findings.
The clinical signs manifestation is not directly related to the viral load since even animals with low Ct values remained without clinical signs (BARRS et al., 2020; SIT et al., 2020; BESSIÈRE et al., 2021). The highest number of positive cases was observed in January 2021, with two peaks in epidemiological weeks 2021/01 (17 cases) and 2021/05 (14 cases), followed by December 2020, when 17 cases were reported, spread over weeks 2020/50, 51 and 53 (Figure 2). Conversely, human epidemiological data collected from the Rio de Janeiro State health system database showed a higher incidence in epidemiological weeks 2021/19 and 2021/20. The reason for this difference is not apparent yet. Still, the epidemiological week 2021/5 was a transitional period in the dispersion of SARS-CoV-2 variants in the state of Rio de Janeiro, where Gamma overtook the Zeta variant (P.2) (P.1) in number of cases (MOREIRA et al., 2021). Therefore, future studies should be conducted to evaluate the ability of different SARS-CoV-2 variants to infect dogs and cats.
Viral genome sequencing of one of the samples identified as the Gamma variant is consistent with the epidemiological scenario when the sample was acquired. The Gamma variant was first described in December 2020 and associated with the second epidemic wave in Brazil. Due to multiple mutations in the S protein (including K417T, E484K, and N501Y), Gamma was considered a variant of concern (VOC) at the time of sample collection in the area (RESENDE et al., 2021).
This study represented the largest coronavirus detection survey conducted on domestic animals in Brazil, testing 650 dogs and cats. Our findings reinterpret the susceptibility of companion animals to SARS-CoV-2 infection but not the severe evolution of the disease.
Considering that COVID-19 is an infectious disease of great importance and several animal species, including dogs and cats, may be susceptible to viral infection, it is particularly important to monitor infected animals actively. The literature does not report any transmission cases from domestic animals to humans. Therefore, owners should maintain their dogs’ and cats’ care and welfare.
ACKNOWLEDGEMENTS
We would like to thank the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) Process E-26/010.000168/2020 for financial support and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
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Edited by
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Editors
Rudi Weiblen (0000-0002-1737-9817)José Valter Joaquim Silva Júnior (0000-0001-5932-0971)
