Bat virome

A biologist holding a bat at a Emerging Infectious Diseases Training Event in Panama

A bat-borne virus is any virus whose primary reservoir is any species of bat. The viruses include coronaviruses such as severe acute respiratory syndrome coronavirus (SARS-CoV) and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2); hantaviruses; lyssaviruses such as rabies virus and Australian bat lyssavirus; henipaviruses such as nipah virus and Hendra virus; Lassa virus; Ebola virus; and Marburg virus. Several bat-borne viruses are considered important emerging viruses.

Bat viromes

Bats are especially tolerant of viruses compared to terrestrial mammals. A single bat can host several different kinds of viruses without becoming ill, though some like the rabies virus do cause illness in bats. Most of the viruses harbored by bats are RNA viruses, though they are also known to have DNA viruses. Some research indicates that bats' immune systems have allowed them to cope with a variety of viruses. A 2018 study found that bats have a dampened STING response compared to other mammals, which could allow them to respond to viral threats without over-responding. Additionally, bats lack several inflammasomes found in other mammals. While inflammation is an immune response to viruses, excessive inflammation is damaging to the body, and viruses like severe acute respiratory syndrome coronavirus (SARS-CoV) are known to kill humans by inducing excessive inflammation. The authors stated, "The nature of the weakened, but not entirely lost, functionality of STING may have profound impact for bats to maintain the balanced state of 'effective response' but not 'over response' against viruses."

Bats have also been shown to be more susceptible to reinfection with the same viruses, whereas other mammals, especially humans, have a greater propensity for developing varying degrees of immunity. Their behavior and life history also make them "exquisitely suitable hosts of viruses and other disease agents", with long lifespans, the ability to enter torpor or hibernate, and their ability to traverse landscapes with daily and seasonal movement.

Bats and their viruses may be the subject of more research than viruses found in other mammal orders, an example of research bias. A 2015 review found that from 1999 to 2013, there were 300–1200 papers published about bat viruses annually, compared to 12–45 publications for marsupial viruses and only 1–9 studies for sloth viruses. The same review found that bats do not have significantly greater viral diversity than other mammal groups. Bats, rodents, and primates all harbored significantly more zoonotic viruses (which can be transmitted to humans) than other mammal groups, though the differences among the aforementioned three groups were not significant (bats have no more zoonotic viruses than rodents and primates).

Transmission

There are four main transmission routes for bat-borne viruses: droplet, airborne, contact, and fecal-oral transmission.

Zoonotic viruses

Coronaviruses

Bats harbor a great diversity of coronaviruses, with sampling by the EcoHealth Alliance in China alone identifying about 400 new strains of coronavirus. A study of coronavirus diversity harbored by bats in eastern Thailand revealed forty-seven coronaviruses. Several bat coronaviruses are known to be zoonotic, or transmissible to humans, including severe acute respiratory syndrome coronavirus (SARS-CoV) and Middle East respiratory syndrome-related coronavirus (MERS-CoV). Severe acute respiratory syndrome coronavirus 2 is another zoonotic coronavirus likely originating in bats.

SARS-CoV causes the disease severe acute respiratory syndrome (SARS) in humans. The first documented case of SARS was in November 2002 in Foshan, China. It became an epidemic, affecting 28 countries around the world with 8,096 cases and 774 deaths. The natural reservoir of SARS-CoV was identified as bats, with the Chinese rufous horseshoe bat considered a particularly strong candidate after a coronavirus was recovered from a colony that had 95% nucleotide sequence similarity to SARS-CoV. There was debate on whether or not animals like palm civets and raccoon dogs were intermediate hosts that facilitated the spread of the virus from bats to humans, or if humans acquired the virus directly from bats.

The first human case of Middle East respiratory syndrome (MERS) was in June 2012 in Jeddah, Saudi Arabia. As of November 2019, 2,494 cases of MERS have been reported in twenty-seven countries, resulting in 858 fatalities. It is believed that MERS-CoV originated in bats, though camels are likely the intermediate host through which humans became infected. Human-to-human transmission is possible, though does not easily occur.

In 2019, a food market that sold live wild game (called ye wei Chinese: 野味) (a "wet market") in Wuhan, China was linked to the outbreak of SARS-CoV-2. Through genetic analyses, scientists initially found the virus resembles those typically found in bats. Subsequent genetics studies suggest the virus may have been transmitted to people from pangolins, since the sequences of coronavirus from these animals have high similarity with SARS-CoV-2, and these species were sold in the market. However, there are also concerns from the scientific community about the validity of the genetics technique used (codon usage bias).

Lyssaviruses

Lyssaviruses include the rabies virus, Australian bat lyssavirus, and other related viruses, many of which are also harbored by bats. Unlike most other viruses in the family Rhabdoviridae, which are transmitted by arthropods, lyssaviruses are transmitted by mammals, most frequently through biting. All mammals are susceptible to lyssaviruses, though bats and carnivores are the most common natural reservoirs. The vast majority of human rabies cases are a result of the rabies virus, with only twelve other human cases attributed to other lyssaviruses as of 2015. After transmission has occurred, the average individual is asymptomatic for two months, though the incubation period can be as short as a week or as long as several years. Italian scientist Antonio Carini was the first to hypothesize that rabies virus could be transmitted by bats, which he did in 1911. This same conclusion was reached by Hélder Queiroz in 1934 and Joseph Lennox Pawan in 1936. Bats have an overall low prevalence of rabies virus, with a majority of surveys of apparently healthy individuals showing rabies incidence of 0–0.5%. Sick bats are more likely to be submitted for rabies testing than apparently healthy bats, known as sampling bias, with most studies reporting rabies incidence of 5–20% in sick or dead bats.

Bats are the most common source of rabies in humans in North and South America, Western Europe, and Australia. In the United States, there were 19 cases of human rabies from 1997–2006, 17 of which were attributed to bats. In North America, about half of human rabies instances are cryptic, meaning that the patient has no known bite history. While it has been speculated that rabies virus could be transmitted through aerosols, studies of the rabies virus have concluded that this is only feasible in limited conditions. These conditions include a very large colony of bats in a hot and humid cave with poor ventilation. While two human deaths in 1956 and 1959 had been tentatively attributed to aerosolization of the rabies virus after entering a cave with bats, "investigations of the 2 reported human cases revealed that both infections could be explained by means other than aerosol transmission". It is instead generally thought that most instances of cryptic rabies are the result of an unknown bat bite. Bites from a bat can be so small that they are not visible without magnification equipment, for example. Outside of bites, rabies virus exposure can also occur if infected fluids come in contact with a mucous membrane or a break in the skin. Rabies virus has also been transmitted when an infected human unknowingly dies of rabies, and their organs are transplanted to others.

Hantaviruses

Hantaviruses, usually found in rodents and shrews, were discovered in two species of bats. The Mouyassué virus (MOUV) was isolated from banana pipistrelle bats captured near Mouyassué village in Cote d'Ivoire, West Africa. The Magboi virus was isolated from hairy slit-faced bats found near the Magboi River in Sierra Leone in 2011. They are single-stranded, negative sense, RNA viruses in the Bunyaviridae family.

Paramyxoviruses

Date palm sap collection, a primary exposure route for Nipah virus

Paramyxoviridae is a family that includes several zoonotic viruses naturally found in bats. Two are in the genus Henipavirus—Hendra virus and Nipah virus. Hendra virus was first identified in 1994 in Hendra, Australia. Four different species of flying fox have tested positive for Hendra virus: the gray-headed flying fox, spectacled flying fox, and black flying fox. Horses are the intermediate host between flying foxes and humans. Between 1994 and 2014, there were fifty-five outbreaks of Hendra virus in Australia, resulting in the death or euthanization of eighty-eight horses. Seven humans are known to have been infected by Hendra virus, with four fatalities. Six of the seven infected humans were directly exposed to the blood or other fluids of sick or dead horses (three were veterinarians), while the seventh case was a veterinary nurse who had recently irrigated the nasal cavity of a horse not yet exhibiting symptoms. It is unclear how horses become infected with Hendra virus, though it is believed to occur following direct exposure to flying fox fluids. There is also evidence of horse-to-horse transmission. In late 2012, a vaccine was released to prevent infection in horses. Vaccine uptake has been low, with an estimated 11–17% of Australian horses vaccinated by 2017.

The first human outbreak of Nipah virus was in 1998 in Malaysia. It was determined that flying foxes were also the reservoir of the virus, with domestic pigs as the intermediate host between bats and humans. Outbreaks have also occurred in Bangladesh, India, Singapore, and the Philippines. In Bangladesh, the primary mode of transmission of Nipah virus to humans is through the consumption of date palm sap. Pots set out to collect the sap are contaminated with flying fox urine and feces, and the bats also lick the sap streams flowing into the pots. It has been speculated that the virus may also be transmitted to humans by eating fruit partially consumed by flying foxes, or by coming into contact with their urine, though no definitive evidence supports this.

An additional zoonotic paramyxovirus that bats harbor is Menangle virus, which was first identified at a hog farm in New South Wales, Australia. Flying foxes were once again identified as the natural reservoirs of the virus, with the black, spectacled, and gray-headed seropositive for the virus. Two employees of the hog farm became sick with flu-like illnesses, later shown to be a result of the virus. Sosuga pararubulavirus is known to have infected one person—an American wildlife biologist who had conducted bat and rodent research in Uganda. The Egyptian fruit bat later tested positive for the virus, indicating that it is potentially a natural reservoir.

Filoviruses

The filoviruses are responsible for fatal hemorrhagic infections in humans and monkeys. These include Marburgviruses (MARV) and Ebolaviruses (EBOV).

Other viruses

Bats host several paramyxoviruses that are not known to affect humans. Bats are the reservoir of Cedar virus, a paramyxovirus first discovered in flying foxes South East Queensland. The zoonotic potential of Cedar virus is unknown. In Brazil in 1979, Mapuera virus was isolated from the saliva of the little yellow-shouldered bat. Mapuera virus has never been associated with disease in other animals or humans, but experimental exposure of mice to the virus resulted in fatality. Tioman virus has been isolated from the urine of the small flying fox, which causes fever in some domestic pigs after exposure, but no other symptoms. Tukoko virus has been detected from Leschenault's rousette in China. Bats have been suggested as the host of Porcine orthorubulavirus, though definitive evidence has not been collected.

See also

• Histoplasmosis

External links

• New York Dept. of Health: Bats and Rabies
• Centers for Disease Control and Prevention: Diseases spread by bats