Coronaviruses (Coronaviridae) Affecting Ruminants, Non-Ruminant Herbivores and Companion Animals Health: A Review

Received 09 Jul, 2024

Accepted 06 Sep, 2024

Published 31 Dec, 2024

Coronaviruses have been extensively studied as causative agents for a range of respiratory, enteric and neurological diseases in animals, due to their significant potential impact on animal health and the economy. These viruses infect specific hosts, such as animals and humans, however, certain strains can infect both animals and humans. This article aims to provide detailed information on coronaviruses in ruminants, non-ruminants herbivores and companion animals, as well as to explore the impacts of these viruses on animal health and industries. Different types of published articles and books were reviewed to obtain the information. Extensive studies on various coronaviruses in different animal species, including ruminants, non-ruminant herbivores and companion animals have not only enhanced our understanding of coronavirus biology and ecology but also provided insights into the global distribution and origins of these viruses. Understanding the diverse range of coronaviruses found in both ruminant and non-ruminant herbivores, as well as in companion animals was highlighted in this review. Coronaviruses occurrence and variability are significantly underestimated. Therefore, there is a critical need to expand our knowledge of coronaviruses present in animals, to study their pathogenicity, transmission dynamics and disease prevalence and to effectively respond to the potential future emergence of new coronaviruses, particularly within economically important animal populations.

INTRODUCTION

Coronaviruses derive their name from the distinctive appearance of “corona” or crown-like spikes on their outer surface. These viruses belong to the subfamily Coronavirinae within the family Coronaviridae and the order Nidovirales^1,2. Among the four genera, coronaviruses of the Alphacoronavirus and Betacoronavirus genera affect ruminants, non-ruminants and companion animals³, such as bovine coronavirus (BCoV)⁴, rabbit enteric coronavirus (RECV)⁵, equine coronavirus (ECoV)⁶, feline coronavirus (FCoV)⁷, canine respiratory coronavirus (CRCoV)⁸ and canine enteric coronavirus (CECoV)⁹.

Table 1:

Types of coronaviruses that impact ruminants, non-ruminant herbivores and companion animal

Coronavirus species	Susceptible hosts	Targeted host cells	Tissues/organ
BCoV4	Cattle	Epithelial cells, enterocyte	Respiratory and enteric tracts
CECoV9	Dog	Enterocyte	Enteric tract
CRCoV8	Dog	Pneumocyte	Respiratory tract
ECoV6	Horse	Epithelial cells	Respiratory tract
FCoV7	Cat	Monocyte, macrophage, enterocyte	Respiratory and enteric tracts, and nervous system
RECV5	Rabbit	Enterocyte	Enteric tract
Source: Saif4, Descoteaux et al.5, Pusterla et al.6, Pedersen et al.7, Decaro and Buonavoglia8, Licitra et al.9

Coronavirus commonly causes respiratory and enteric diseases in various animals¹⁰. This review focuses on veterinary and economically important coronaviruses, emphasizing their origins, ecological distribution, genetic diversity, transmission and economic impact. Table 1 provides a list of coronaviruses affecting ruminants, non-ruminants and companion animals.

Bovine coronavirus (BcoV): The BCoV causes gastroenteritis, diarrhea and respiratory disease in young and newborn cattle, leading to enormous economic losses worldwide⁹. These financial losses are partly attributed to mortality rate, which can reach up to 69% in beef calves within 2 months of their arrival¹¹. Infected calves often exhibit diarrhea, while adult cattle may experience winter dysentery and respiratory disease¹². Calves can be infected with BCoV through both respiratory and oral routes¹³.

The virus is responsible for both respiratory and enteric diseases in cattle⁴. As a result, the virus can be detected in diarrheic fecal samples and respiratory droplets from calves and cattle, regardless of whether they have respiratory symptoms¹⁴. The BCoV replicates on the surface epithelial cells, particularly in the distal half of the villi, leading to cell death, sloughing off the dead cells and replacing by immature cells, which results in stunting and fusion of adjacent villi¹³. This deterioration in the intestinal surface area reduces the digestive and absorptive capacity of the intestine. Additionally, high mortality rates in BCoV-infected cattle are attributed to severe gastroenteritis manifested by bloody diarrhea in the feces, resulting from damage to the intestinal villi¹³. Moreover, BCoV infection can lead to severe or fatal disease in adult cattle when combined with other factors such as mucosal immunity deficiency, stress from transportation or co-infection with other secondary respiratory pathogens¹⁵.

The origin of BCoV remains uncertain. However, analysis of its genome has revealed a remarkably high nucleotide identity of 96% with human coronavirus OC43 (HCoV-OC43), suggesting a zoonotic transmission from bovines to humans¹⁶. There have been reports of BCoV being detected in a 6-year-old child with diarrhea, indicating a possible interspecies transmission to humans¹⁷.

Similar to other betacoronaviruses, BCoV displays high variability in both the structure and sequences of its genomes. Notably, a distinguishing genetic feature of BCoV is the presence of a hemagglutinin-esterase (HE) protein, which is not found on the surface of other betacoronaviruses¹⁸. The HE protein acts as the secondary viral attachment protein alongside the S protein¹⁵. Consequently, HE may contribute to the broad host range observed in betacoronavirus species¹⁵.

Vaccines targeting BCoV are available to protect against respiratory and enteric disease in cattle and young calves¹⁸. Successful disease control has been reported in numerous countries through the parenteral vaccination of pregnant cows. A protective approach for the calves involves vaccinating pregnant cows in their third trimester will trigger the production of crucial maternal immunity required for the early-stage immunity of the calves¹⁸.

Rabbit enteric coronavirus (RECV): Coronavirus has been reported in commercial rabbitries¹⁹. Two distinct pathological forms of coronavirus infection have been observed in rabbits, namely; i) enteric disease (local form) and ii) pleural effusion and cardiomyopathy (systemic form)¹⁹. The enteric disease rising from RECV infection exhibits characteristic lesions and symptoms consistent with enteritis²⁰, while pleural effusion and cardiomyopathy were reported in a laboratory experiment¹⁹. The RECV is transmitted through the fecal-oral route. The virus primarily attaches to and replicates in the small intestine²¹.

Young rabbits aged between 3 and 10 weeks are particularly susceptible to RECV infection, although the virus may also be present in clinically healthy adult rabbits²². Clinical manifestations of RECV infections in rabbits include watery diarrhea, abdominal distension, anorexia and sudden death, although asymptomatic cases can also occur²³. Morbidity rates can range from 40 to 60%, with mortality rates may exceed 75% among affected rabbits²⁴. Microscopic examination may reveal intestinal villous blunting, crypt hypertrophy, complete M-cell necrosis and necrosis of villous epithelial cells overlying the gut-associated lymphoid tissue (GALT) in the small intestine²⁵.

According to recent research, various management strategies aimed at preventing RECV infections, such as delayed weaning and dietary modifications, have been considered¹⁹. Nevertheless, it has been found that the utilization of broad-spectrum antibiotic treatment and vaccination has not proven to be effective in managing and preventing the morbidity and mortality of rabbits²⁶.

Equine coronavirus (ECoV): The ECoV is the only strain of coronavirus that is known to infect and cause disease in horses. The virus was first isolated in North Carolina, USA in 1999²⁷ and since then, sporadic ECoV infections have been reported in various parts of the world²⁸. However, there is limited information available on the epidemiology and evolution of ECoV.

The most commonly observed clinical signs associated with ECoV infections include fever, anorexia and lethargy²⁹. Only about 10% of gastrointestinal diseases and 3% of neurological disorders in infected horses are reported. Mortality has been reported in severe cases of ECoV infection³⁰.

Transmission of ECoV occurs through the fecal-oral route, with horses becoming infected by ingesting contaminated feed and water³¹. Fecal samples are commonly used for diagnosing ECoV in both diarrheic and non-diarrheic horses³².

At present, there is no vaccine available for ECoV. However, several studies are exploring experimental vaccines against ECoV³³. The most effective way to control and prevent the spread of ECoV is through strict biosecurity measures and isolating sick horses in quarantine. Therefore, the only treatment for infected horses is supportive care to manage the symptoms until recovery³³.

Feline coronavirus (FCoV): The FCoVs primarily affect the intestinal tract of cats, but they can also lead to a fatal immune-mediated disease³⁴. The FCoVs belong to the genus Alphacoronavirus and the species Alphacoronavirus 1, alongside TGEV, PEDV, CCoV, HCoV-229E and HCoV-NL63³⁵. There are two biotypes of FCoV: Feline infectious peritonitis virus (FIPV) and feline enteric coronavirus (FECV). The FIPV causes feline infectious peritonitis (FIP), while FECV is responsible for feline enteric disease.

Two serotypes of FCoV existed: Serotype I and serotype II³⁶. Serotype I accounts for 80 to 95% FCoVs infections, while serotype II represents about 25%³⁷. The FIP is a progressive, immune-augmented and fatal disease³⁸. The FIP is characterized by the presence of fibrinous and granulomatous serositis, which is an inflammation of the serous membranes, a protein-rich serous effusion in body cavities and the formation of granulomatous lesions³⁹. This disease presents in two main forms: wet or effusive (exudative) and dry or non-effusive (proliferative)⁷. The FIPV primarily attaches and replicates in the epithelial cells of the pharynx or the jejunum of the intestinal tract³⁹. Acute infections with FIPV lead to viremia and rapid virus spread in the thorax and abdomen, often resulting in mortality⁴⁰.

Symptoms of FIPV infection in cats include anorexia, chronic fever, malaise and in some cases, neurological or ocular diseases⁴¹. In addition, FIP is a major cause of death among young domestic cats, with the highest incidence occurring in cats aged 3 months to 3 years^41,42. However, FIP can affect cats of any age, particularly those with suboptimal immune function⁴³.

The FECV is identified as a virulent biotype of FCoV and is considered the hypervirulent biotype precursor of FIPV⁴⁴. Studies reported that approximately 5% of persistently infected cats with FECV may develop FIP⁴⁵. This suggests that FIPV evolves from FECV through specific mutations in the viral genomes of individually infected cats⁴⁵. Unlike FIPV, FECV typically leads to mild enteritis⁴⁶, with many infections being subclinical. As a result, the virus can be detected in the feces a few days after infection and can persist for several months⁴⁷.

Cats are usually infected with FCoV through oro-nasal exposure by coming into contact with the virus in feces or with contaminated fomites⁴⁸. It is believed that the sharing of litter boxes among cats contributes to virus transmission⁴⁹.

The treatment of FCoV infections primarily aims to reduce the inflammatory and hyperimmune response. Moreover, various antivirals and immunosuppressants are being investigated for their potential efficacy in managing FIP cases⁵⁰. As a preventive measure, vaccines against FCoV are available and may provide some level of protection to cats that have not previously been exposed to FCoV⁵⁰.

Canine respiratory coronavirus (CRCoV): The CRCoV belongs to the genus Betacoronavirus and shares genetic similarities with BCoV and HCoV⁵¹. The CRCoV can infect dogs of all ages and breeds⁵².

Dogs usually get infected with CRCoV through airborne exposure to the bio-aerosols of respiratory secretions from infected dogs⁵².In addition, studies reported the presence of the virus in air samples, water troughs, toys in pens and on surfaces such as dog kennels, food and water bowls⁵³. The risk of CRCoV infection is heightened in environments where a large numbers of dogs are kept in close confinement, such as boarding kennels, shelter facilities and dog show kennels⁵⁴.

The virus induces acute or subacute respiratory disease in dogs, potentially leading to severe pneumonia and fatality. Common pathologic findings of CRCoV infection in dogs include mild inflammatory changes in the upper respiratory tract, particularly in the nares and the trachea⁵⁵. Infected dogs typically exhibit clinical signs such as cough, sneezing and nasal discharge. In addition, there is observed deterioration of the trachea surface cilia⁵⁶, which commonly occurs in CRCoV infections in dogs⁵⁷. This damage facilitates deeper penetration of the airways by co-infection with secondary respiratory pathogens, leading to more severe clinical cases⁵⁸.

Unfortunately, there is no commercially available vaccine for preventing CRCoV or reducing the clinical disease⁵². Moreover, no specific treatment for CRCoV infections can be applied. The only treatment approach involves supportive therapy based on the clinical signs. Stringent biosecurity measures, such as isolating sick dogs in quarantine, changing clothes and practicing thorough hand washing after handling the dogs become an alternative to curbing the spread of CRCoV⁵⁷.

Canine enteric coronavirus (CECoV): The CECoV belongs to the genus Alphacoronavirus within group 1 coronavirus species and is distinct from the group 2 CRCoV, sharing 69 and 21% identity in nucleotide and an amino acid sequences, respectively⁹. Notably, genetic similarities analysis associates CECoV with other group 1 coronaviruses such as FCoV and TGEV⁵⁷. The CECoV typically induces mild, self-limiting diarrhea in dogs, particularly in young puppies^59,60. Transmission of the virus can occur through the fecal-oral route⁶⁰. A study reported a high prevalence of CECoV infections in dogs living in densely populated environments like shelters or kennels⁶¹.

The CECoV infection dogs often lead to high morbidity but low mortality⁵⁴. Clinical manifestations of CECoV-infected dogs include vomiting, lethargy, loss of appetite and diarrhea⁶¹. Studies have indicated that the virus primarily attaches and replicates in the epithelial cells of the small intestine⁶¹. Gastroenteritis is a common clinical sign of CECoV infection, with severe cases potentially leading to mortality due to diarrhea⁵⁹. In addition, the virus has been observed to occasionally infect the respiratory tract in natural conditions⁶².

Currently, there is no specific treatment for CECoV infections. However, implementing strict biosecurity measures and providing supportive nursing care to infected dogs are recommended approaches⁶⁰.

CONCLUSION

This review highlights the diverse range of coronaviruses found in both ruminant and non-ruminant herbivores, as well as in companion animals. However, their occurrence and variability are significantly underestimated. Therefore, there is a critical need to expand our knowledge of coronaviruses present in animals, to comprehensively study their pathogenicity, transmission dynamics and disease prevalence and to effectively respond to the potential future emergence of new coronaviruses, particularly within economically important animal populations.

SIGNIFICANCE STATEMENT

This study on eco-biology, transmission and disease caused by the diverse range of coronaviruses in ruminants, non-ruminants and companion animals provides valuable insights into their impact on animal health and the economy. Understanding of these attributes is essential for preparing and managing effective diagnosis and control strategies. Moreover, this study will contribute to expanding the knowledge of coronaviruses in animals and facilitate proactive measures to address the potential future emergence of new coronaviruses, particularly among economically valuable animal populations.

ACKNOWLEDGMENTS

Author would like to thank the Director General of the Department of Veterinary Services Malaysia, Director of Veterinary Research Division, DVS and Director of Veterinary Research Institute for their kind permission to publish this paper.

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