A Critical Needs Assessment for Research in Companion Animals and Livestock Following the Pandemic of COVID-19 in Humans

Abstract

Problem:

The emergence of novel coronavirus (SARS-CoV-2) in Wuhan, China, in November 2019 and a growing body of information compel inquiry regarding the transmissibility of infection between humans and certain animal species. Although there are a number of issues to be considered, the following points are most urgent:

The potential for domesticated (companion) animals to serve as a reservoir of infection contributing to continued human-to-human disease, infectivity, and community spread.

The ramifications to food security, economy, and trade issues should coronavirus establish itself within livestock and poultry.

The disruption to national security if SARS-CoV-2 and its fairly well-established effects on smell (hyposmia/anosmia) to critical military service animals including explosive detector dog, narcotics detector dog, specialized search dog, combat tracker dog, mine detection dog, tactical explosive detector dog, improvised explosive device detector dog, patrol explosive detector dog, and patrol narcotics detector dog, as well as multipurpose canines used by special operations such as used by the U.S. customs and border protection agency (e.g., Beagle Brigade).

This article presents in chronological order data that both individually (as received independently from multiple countries) and collectively urge studies that elucidate the following questions.

What animal species can be infected with SARS-CoV-2, the likely sources of infection, the period of infectivity, and transmissibility between these animals and to other animal species and humans?

What are the best diagnostic tests currently available for companion animals and livestock?

What expressions of illness in companion and other animal species can serve as disease markers?

Although it is recognized that robust funding and methodology need to be identified to apply the best scientific investigation into these issues, there may be easily identifiable opportunities to capture information that can guide decision and study.

First, it may be possible to quickly initiate a data collection strategy using in-place animal gatekeepers, such as zookeepers, veterinarians, kennel owners, feed lots, and military animal handlers. If provided a simple surveillance form, their detection of symptoms (lethargy, hyposmia, anosmia, and others) might be quickly reported to a central data collection site if one were created.

Second, although current human COVID-19 disease is aligning around areas of population density and cluster events, it might be possible to overlay animal species density or veterinary reports that could signal some disease association in animals with COVID-19 patients. Unfortunately, although companion animals and zoo species have repeatedly served as sentinels for emerging infectious diseases, they do not currently fall under the jurisdiction of any federal agency and are not under surveillance.

Background: Companion Animals

The issue of the need to evaluate companion animals and their status with regards to SARS-CoV-2 was first raised on January 29 when a member of the senior expert team from China's National Health Commission stated on Chinese state television that pet owners should take extra care of their animals because (1) the virus “moves between mammals”; (2) if your animals “come into contact with the outbreak or people infected with the virus, then your pets should be put in quarantine”; and (3) “because the epidemic spreads between mammals, therefore we should take precaution against other mammals” (Safoora 2020). No scientific data were presented to support this statement but, nonetheless, it prompted a severe public response that resulted in many pet dogs and cats being killed and thousands being abandoned (Wan et al. 2020, Daniels 2020, Thomson 2020b).

This prompted the World Health Organization to state that “there is no evidence dogs and cats can be infected with the virus” (Thomson 2020a, Williams 2020). No scientific data were provided to support this statement about a novel zoonotic threat either. Despite this appeal, the culling of pets continued in China through February 21 (Albawaba 2020). On February 26, Hong Kong's Agriculture, Fisheries, and Conservation Department announced that a pet dog of a COVID-19 patient had tested “weak positive” through RT-PCR. The fact that the dog was asymptomatic along with the inability to recover live virus led to this finding being attributed to environmental contamination from the owner (Simin et al. 2020). However, on March 9, ProMED-mail posted the remarks of the associate director for the Joint Institute for Virology at Hong Kong University who stated “the dog's lack of symptoms showed the virus could live inside it, allowing the animal to secrete and spread the virus at the same time” (Simin et al. 2020).

On March 2, the French Agency for Food, Environmental and Occupational Health & Safety received a formal request from the Directorate General for Food to assess risks—specifically to give an opinion regarding the potential role of domestic animals (livestock animals and pets) in the spread of SARS-CoV-2. With the exception of work on infections undertaken in transgenic mice (Bao et al. 2020) expressing the human form of ACE2 receptor for the SARS-CoV-2, very few studies have described animals experimentally infected with SARS-CoV-2. They concluded that “additional studies on the interactions between SARS-CoV-2 and ACE2 homologues from various animal species, as well as studies on the distribution of ACE2 in tissue, are necessary to further knowledge on the possible transmission of infection to other species. However, cross-species transmission does not rely solely on the presence of the receptor but also on the presence of other cellular factors required for viral replication. Further studies should also be undertaken to identify these factors” (ANSES 2020).

At the same time, the Ministry of Health in Singapore released a statement discussing the theoretical possibility that COVID-19 could spread from animals to humans or vice versa but that they did not see pets as a “serious vector of transmission” and that there were “no plans to isolate, do contact tracing for pets, or exercise any form of quarantine for animals” (Mahmud 2020). On March 13, the IDEXX veterinary diagnostic laboratory announced that it had tested >3500 dog, cat, and equine specimens from across the United States and South Korea with their COVID-19 RT-qPCR and that they had no positives (IDEXX 2020) What the press release did not make clear, however, is the fact that although animals tested were from affected areas, it is “unknown if any of the animals lived in homes with people that had COVID-19” (ScienceNews 2020). WHO, CDC, and the AVMA accepted IDEXX's assertion that pets posed little risk to public health at face value. On March 13, WHO stated that “pets are generally safe from being infected with coronavirus” (Zhou 2020). But they recently admitted “that pets can get infected, but there is no evidence pets can spread the disease or that the disease can cause an animal to fall ill” (Zhou 2020). On March 16, the AVMA admitted it did not “have a clear answer as to whether SARS-CoV-2 can infect pets at this time…and there is no evidence that pets can become sick. Infectious disease experts, as well as CDC, OIE and WHO indicate there is no evidence to suggest that pet dogs and cats can be a source of infection with SARS-CoV-2, including spread to people” (AVMA 2020). On March 19, a second dog tested positive by RT-PCR in Hong Kong (ScienceNews 2020). The first dog was later found to be positive for SARS-CoV-2-specific antibodies confirming the initial test was not a false positive and that the dog had actually been infected (Systematic Reviews for Animals & Food 2020).

On March 27, the first positive cat was diagnosed with COVID-19 in Belgium (Brown 2020, Bryner 2020). Contrary to earlier assertions by health agencies that the virus could not cause illness in pets, the cat developed both respiratory and enteric symptoms and took 9 days to recover. Large amounts of antigen were repeatedly demonstrated in vomit and feces over multiple days, which led scientists to conclude that the cat had indeed been infected by SARS-CoV-2. The Scientific Committee in Belgium said it was “unable to assess the risk” of animal-to-human transmission but did not recommend testing pets until validated diagnostics were available (AFSCA 2020). Between March 27 and 30, scientists still said they considered pets to be “dead end hosts” (Stone 2020) that “the risk of animal to human transmission is very small” and that “animals are not vectors of the epidemic, so there is no reason to abandon your animal” while advising owners “not to rub their nose against their pets” (Brown 2020). On April 3, research was published on the BioRxiv website by Chinese researchers who studied 100 stray and house cats from Wuhan, China, for the presence of SARS-CoV-2-specific antibodies. They found ∼15% of them had antibodies in their blood that were specific to the novel coronavirus. On April 18, two cats reportedly tested positive for SARS-CoV-2 in New York. Both cats had owners who were COVID-19 positive, and both animals were exhibiting respiratory signs (Promed mail posted on April 18, 2020) (Zhang 2020).

On April 1, Chinese authors posted several preprint nonpeer-reviewed publications on transmission studies in animals (Shi et al. 2020a), a serological study in cats (Zhang et al. 2020), and ACE2 gene expression in animals (Sun et al. 2020). These studies are the first experimental studies in animals and provide valuable insights into SARS-CoV-2 infection in a variety of species. The transmission study showed that the virus replicates efficiently in cats, that it causes severe disease in juvenile cats, and that there is droplet transmission of the virus from infected to naïve cats. Both, RT-qPCR and immunohistochemistry assays revealed abundant RNA or antigen in respiratory and gut epithelium. The virus did not replicate efficiently in dogs, ducks, chickens, and pigs but did replicate efficiently in cats and ferrets (Shi et al. 2020). The authors said “surveillance for SARS-CoV-2 should be considered as an adjunct to elimination of COVID-19 in humans.” The gene expression study found that ACE2 was “highly expressed in skin, ear tips, lungs and retina of cats and in skin and retina of dogs.” “In addition, we also observed ACE2 expression in the lungs of cats and ferrets, which suggested that these animals may be more suitable for SARS-CoV-2 studies than rodent models” (Sun et al. 2020). As interesting as these studies are, it must be noted that they are small studies and are not peer reviewed at this time. One scientist stated that she doubts the results of the transmission study because they infected cats with very high doses of virus and they do not replicate nature (Zhen 2020).

Background: Working Dogs

Several articles announced an unusual presentation of COVID-19 in asymptomatic people (Young 2020, Yeager 2020, Kwong et al. 2020, Lanse 2020). Patients who subsequently tested positive for COVID-19 reported an early loss of smell and taste. The American College of Otolaryngology proposed adding anosmia, hyposmia, dysgeusia, and ageusia to the list of screening items for COVID-19 patients (Young 2020). This raises the question of whether hyposmia/anosmia and ageusia/dysgeusia occur in animals, specifically in military working dogs, in beagle brigades at CBP and K9 first responder teams?

The U.S. government spends millions of dollars to train bomb-sniffing dogs essential to federal and local law enforcement capabilities (Homeland Security Today 2019, Nelson 2020). Dogs serve many roles in the military and as multipurpose canines as already mentioned. A fully trained bomb detection canine is likely worth over $150,000. Despite decades of trying, researchers have yet to develop a machine as exquisitely sensitive and discerning as a dog's nose (Murphy 2020). Dogs have 220 million scent receptors that is 44 times more than humans. What happens if working dogs lose their sense of smell? Unfortunately, the only susceptibility study published on dogs (Shi et al. 2020a) did not include histopathologic evaluation or immunohistochemical staining of the nasal passages in the experimentally SARS-CoV-2-infected dogs that were necropsied, so this remains an important but unanswered question. If hyposmia/anosmia does occur in dogs, it will have a devastating impact on U.S. national security. In contrast, if an effect of SARS-CoV-2 on smell is conclusively ruled out, perhaps dogs can be trained to detect people with COVID-19 and enhance surveillance for the disease (BBC 2020). Either way, there is a critical need for studies to investigate this issue.

Background: Livestock and Poultry

The COVID-19 pandemic is significantly impacting the U.S. food supply and agricultural systems. There is a need to develop and deploy rapid strategies that allow mitigation of threats from SARS-CoV-2 across the food and agriculture enterprise. It is critical to ensure the availability of a safe, nutritious, and abundant food supply for U.S citizens, and respective tools and technologies have to be developed to protect the food and agricultural supply chain, safety of our foods, health, and security of livestock, as well as the well-being of farmers, food service providers, and rural Americans. Therefore, reliable data are needed on the susceptibility of livestock (cattle, sheep, goats, horses, alternative livestock, and others) and poultry (chickens, turkey, ducks, and others) to SARS-CoV-2 and the potential transmissibility within a species and across species to guide politicians and other decision makers. The susceptibility of livestock and poultry that could act as virus reservoirs, might serve as animal models for COVID-19 or are possibly in close contact with infected humans, is still understudied. Recent work at the Harbin Veterinary Research Institute (Shi et al. 2020b) in China and the Friedrich-Loeffler-Institut (Swine Health Information Center 2020, Friedrich-Loeffler-Institut 2020) in Germany examined SARS-CoV-2 susceptibility of pigs, chickens, and ducks (only studied by Shi et al. 2020b). They reported that pigs, chickens, and ducks could not be productively infected by SARS-CoV-2 under the experimental conditions used in their work.

This raises many questions: What is the susceptibility of livestock and poultry to SARS-CoV-2? Do we know the potential transmission of SARS-CoV-2 from humans to livestock/poultry and among different livestock/poultry species? Do we have methods for detection and surveillance of SARS-CoV-2 in livestock/poultry?

Background: Zoo Species

As of today (April 19, 2020), a Malayan tiger, her sister, three African lions, and two Amur tigers at the Bronx Zoo developed clinical disease and tested positive for SARS-CoV-2. It is hypothesized that they contracted the virus from an asymptomatic COVID-19 positive keeper. This raises a host of questions. Did the large cats develop a dry cough? Given their large size, how much virus will they shed through the respiratory route? Will they shed virus in feces and urine? What will be the duration of shedding? The reports attribute their infection to the keeper but, once infected, will the cats be able to transmit the virus to other people? Will SARS-CoV-2 have an impact on reproduction of captive endangered species? What other species in a zoological collection can be infected by SARS-CoV-2? Are there potential reservoirs of SARS-CoV-2 in animals maintained in zoological collection? How can surveillance of zoo species be performed on a national basis? What diagnostic tests should be used to diagnose zoo species? These are many questions and many of them also apply to other animal species including companion animals and livestock.

Summary

Concerns about the need to investigate SARS-CoV-2 in companion animals was first shared with the “Red Dawn Breaking” COVID-19 group of federal officials and academics on February 13, 2020, by one of the authors (T.M.). It was then discussed with members of the Department of Homeland Security (DHS) between mid-March and early April by all authors. This information was pulled together in response to an informal e-mail from DHS and was submitted to DHS on April 6, 2020.

A thorough review of the literature concerning SARS-CoV-2 as it relates to companion animals was conducted. Although there was early indication that cats might be susceptible to SARS-CoV-2 infection based on their ACE2 receptor structure (Wan et al. 2020), no investigations were performed. Instead, there have been repeated assertions by WHO, CDC, and several veterinary entities that companion animals were “unlikely” to get infected with SARS-CoV-2. But then dogs and cats tested positive in Hong Kong and Belgium and recently cats in the United States (NY Times 2020). Although these same organizations also had stated that pets would not become ill, the cat in Belgium presented with clinical signs. More cats and dogs have since tested positive in Hong Kong and ∼15% of stray and house cats in Wuhan, China, have been found seropositive (Zhang, 2020). In addition to domestic cats and exotic felids, natural infections have now also been confirmed in mink at two farms in the Netherlands (ProMED 2020c). Along the way, the public messaging about companion animals has shifted from “there is no threat” to “in an abundance of caution, be sure to wash your hands after petting your animals and be careful not to let your dog lick your face.” Less than a week ago, Chinese researchers published a nonpeer-reviewed study that, if accurate, indicates that juvenile cats can not only become infected and develop serious disease but that they also efficiently transmit the infection to adjacent uninfected cats. If these findings can be replicated and verified, they raise serious implications for pet cats, cats in shelters, exotic felids in zoos, and possibly people. Tigers and lions in a U.S. zoo have tested positive for SARS-CoV-2, raising more questions about species susceptibility, duration of infection, viral shedding, and asymptomatic reservoirs.

In its February 3 Strategic Preparedness and Response Plan on COVID-19, WHO lists the need to “identify and reduce transmission from the animal source; address crucial unknowns regarding clinical severity, extent of transmission and infection, treatment options, and accelerate the development of diagnostics, therapeutics and vaccines; and communicate critical risk and event information to all communities and counter misinformation” as strategic objectives (World Health Organization 2020b). In the situation reports of February 5 and 22 (World Health Organization 2020a), WHO again states there is a need to “identify and reduce transmission from the animal source.” On April 3, OIE reported another positive cat in Hong Kong that has been quarantined and put under veterinary surveillance for 14 days. Under “Zoonotic impact” the report says “Zoonotic potential unknown at this time.” The recent Chinese studies conclude that “surveillance (in cats) for SARS-CoV-2 should be considered an adjunct to the elimination of COVID-19 in humans” (Shi et al. 2020a) and that “more studies are needed” (Zhang et al. 2020). We agree.

With regard to diagnostics, molecular diagnostic kits used for human COVD-19 testing can be easily adapted to animal testing—as long as the SARS-CoV-2 does not dramatically mutate after cross-species transmission from humans to animals. To determine whether such mutations are occurring, it is critical that next-generation sequencing technology be applied on SARS-CoV-2 samples recovered from animals. In terms of serological tests, the high-throughput indirect ELISA systems available already for humans cannot be used for animals. Novel validated indirect ELISA tests for individual animal species, and importantly competitive ELISA tests that can be used independent of the animal species are badly needed. Neutralization antibody tests, which are unfortunately labor and time consuming, can be adapted for animal sera. In addition, antigen detection assays for the presence of SARS-CoV-2 antigens in animal samples should be developed, since they can be used independent of animal species. The potential to use serological and antigen-based SARS-CoV-2 assays in a point of care environment, that is, in veterinary practices, zoos, kennels, at ports, airports, and border crossings, is enormous.

In the immediacy of the COVID-19 crisis, the focus has understandably been on human health. But we have ignored the opposite side of the coin of emerging zoonotic disease threats—the animals themselves. This lack of a One Health approach has resulted in an unnecessary delay in the investigation of important veterinary issues as they pertain to public health. Had we taken a proactive approach, we could have gotten ahead of this.

We are now faced with many urgent questions that can only be answered through investigative studies and surveillance. In the September 2000 GAO report “West Nile Virus Outbreak—Lessons for Public Health Preparedness” (GAO/HEHS-00-180 West Nile Virus Outbreak), the authors emphasized the need to “expect the unexpected.” With regard to SARS-CoV-2 in animals, this admonition seems to have been forgotten. Anecdotal information and assumptions are no substitute for stringent studies. Absence of evidence is not the same thing as evidence of absence.

Footnotes

Acknowledgments

The authors express sincere thanks to Stephen Higgs, Elin Gursky, and Bob McCreight for their suggestions and help in reviewing this article.

Author Disclosure Statement

No conflicting financial interests exist.

Funding Information

No funding was received for this article.

Appendix

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