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BATS AND HUMAN HEALTH

Ebola, SARS, Rabies and Beyond


Lisa A. Beltz
Malone University, Canton, Ohio, USA










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FOREWORD

A BRIEF INTRODUCTION TO UNIQUE FEATURES OF BATS IN RELATION TO INFECTIOUS DISEASES

Over the course of the past half century, a multitude of infectious diseases have come to the attention of the research and health communities. These infectious “emerging diseases” are composed of not only new human diseases or diseases of which we are newly aware, but also include some older infectious diseases that are increasing in virulence or in geographical locations. Emerging infections may be caused by bacteria, viruses, fungi, protozoa, or parasitic worms. The rate of emergence has been increasing and appears to be due to a combination of increased detection and recognition as well as increased numbers of microbial pathogens. It should be noted that we are also experiencing an increase in emerging diseases that are not of microbial origin and are due partially to increased recognition, but also due to changes in our lifestyles, to increased lifespans, and to the rescue of populations of people who previously would not have survived fetal development, infancy, or childhood. A few of these noninfectious emerging diseases include a variety of cancers, obesity‐related disorders, and neurological and developmental illnesses, but also fibromyalgia, systemic lupus erythematosus (lupus), temporomandibular joint disorder, a wide range of autoimmune diseases, and carpal tunnel syndrome. Furthermore, many older diseases of infectious origin are increasingly less common due to the efforts of the biomedical research community and health‐care professionals and include the “childhood diseases,” smallpox, polio, malaria, and rheumatic fever (resulting from immune responses to streptococcal infection), as well as cholera and diarrheal and respiratory diseases in developed areas of the world.

Other than increased detection, a number of factors contribute to the emergence of infectious diseases in human populations. For zoonotic diseases, these include increased contact with microbial reservoir hosts by elimination of their natural habitat plus the related urbanization of many animal species, increased numbers of humans traveling to or residing in formerly lightly inhabited regions, increased contact between previously separated animal species in live animal markets, and the movement of agricultural or companion areas throughout the world.

Bats have several characteristics that combine to make them uniquely qualified to serve as viral hosts. These characteristics are discussed in detail in several journal articles, reviews, and books (Omatsu et al. 2007; Wang et al. 2011; Hayman et al. 2013; Smith & Wang 2013; O’Shea et al. 2014; Racey 2015) and so will be mentioned only briefly here. Bats are among the largest and most diverse groups of mammals, second only to rodents. Bats are the only mammals capable of true flight. Large nightly increases in body temperature and energy use required by flight alternate with decreases in temperature and energy usage occurring during their daily torpor. This increase in body temperature is similar to the fever response and may select for viruses that are able to survive if transmitted to another mammalian host. Bats are known to host a number of viruses that do not cause serious disease in them, supporting the contention that bats are ideal reservoir hosts for many viruses. Lyssaviruses are the most important exception to nonpathogenic viruses of bats. Understanding the mechanisms behind lyssaviruses survival and pathogenicity in bats requires further study into the ways in which this group of viruses differs from other rhabdoviruses which are less pathogenic to bats. It is also very important to determine whether highly pathogenic viruses in humans which have been linked to zoonotic transmission from bats (the Ebola and Marburg filoviruses, henipaviruses, and the SARS‐ and MERS‐coronavirus), are more resistant to higher temperatures in vitro. In the case of filoviruses, this might indeed be the case since they cause hemorrhagic fever in humans.

Bat antiviral immune responses differ from those utilized by humans, with bats relying more heavily on protection by interferons, some of which are constitutively expressed (innate immune response) (Zhou et al. 2016), rather than the primary human reliance upon CD8+ T killer cells (adaptive immune response) and natural killer cells. This difference, as well as decreased immunity during hibernation in some species of temperate bats, has led to the suggestion that bats are able to control pathogenic viral activity while not clearing the infection, thus maintaining a state of persistent infection, as would be expected of a viral reservoir host. Many bats are long‐lived and many species are gregarious and roost in colonies that are composed of over a million bats, sometimes of different species. This facilitates both intraspecies and interspecies horizontal transfer of viruses. Vertical transfer of viruses occurs as well, allowing viruses to persist within colonies long‐term. Long distance migration in some bat species also allows wide geographical spread of infection.

While a large amount of attention has focused upon the potential roles of bats, rodents, and nonhuman primates as major reservoirs of emerging viral infections, many other animal species are responsible for direct or indirect zoonotic infection of humans by acting as either reservoir hosts or microbial vectors, as described in Chapter 15. This relatively limited focus on selective animal groups may be a double‐edged sword that, while detecting zoonotic reservoir host species, may also miss many other reservoir species. This approach may also focus on viruses of the targeted mammal populations that are similar to those causing disease in humans, but are unlikely to ever live up to their zoonotic potential. The focus on bats and rodents as potential disease reservoirs has also led to fear in the general public and killing or dispersing animal species that humans historically have viewed with fear and loathing. This misguided and generalized fear of bats further decreases the chance of survival for bat species that were already endangered by human activities, including the spread of white‐nose syndrome and construction of wind farms (Erickson et al. 2016).

The fear of bat‐borne diseases and of bats in general overlooks the vital role that bats play, not only in nature, but also in human health and well‐being. Bats are major pollinators that are necessary to the continued survival of some plant species, including agave, a key economical crop in regions of Latin America. By consuming insects, some bat species also remove huge numbers of pests that consume crops, reducing the levels of toxic insecticides needed by the agricultural community, and delaying the development of pesticide resistance (reviewed by McCracken et al. 2012). Some insectivorous bats eat the equivalent of half their body weight per night and have been estimated to lower agriculture costs by billions of dollars per year in the United States (Hill & Smith 1992; Boyles et al. 2011). Their role in crop protection increases food production in areas of the world which cannot afford inorganic fertilizers. In addition to consuming insect pests, bat guano is used as organic fertilizer. Sale of bat guano is an important part of local economies in many parts of the world. Bats also play critical roles in the repopulation of ecosystems by distributing seeds to damaged areas.

While the majority of scrutiny on bat microbes has focused on viral diseases, bats, as well as other mammals, are infected by many other infectious agents. The increased attention on diseases of bats could, and perhaps should, be extended to other groups of microbes. A better understanding of the microbiome of bats could aid in conservation efforts as we better understand the microbes that threaten bats’ well‐being. The purpose of this book is to gather known information about microbes infecting bats and discuss their implications for human and bat health. As an aid to study this collection of the microbes that infect bats, spread‐sheets containing information about the bat microbes for each chapter that may be easily manipulated for research purposes are found in the companion website. The companion site also contains a master spread‐sheet that encompasses information from the chapter spread‐sheets as well as including information concerning the bats’ diets and geographical locations and further information about the respective microbes. It is hoped that these spread‐sheets may be of benefit to not only those who study bat and human infections, but also to the bat conservation community as microbial threats to bats are better understood.

REFERENCES

  1. Boyles JG, Cryan PM, McCracken GF, Kunz TH. 2011. Economic importance of bats in agriculture. Science. 332:41–42.
  2. Erickson RA, Thogmartin WE, Diffendorfer JE, Russell RE, Szymanski JA. 2016. Effects of wind energy generation and white‐nose syndrome on the viability of the Indiana bat. PeerJ. 4:e2830.
  3. Hayman DTS, Bowen RA, Cryan PM, McCracken GF, O’Shea TJ, Peel AJ, Gilbert A, Webb CT, Wood JLM. 2013. Ecology of zoonotic infectious diseases in bats: current knowledge and future directions. Zoonoses and Public Health. 60:2–21.
  4. Hill JE, Smith JD. 1992. Bats: A Natural History. University of Texas Press: Austin, TX.
  5. McCracken GF, Westbrook JK, Brown VA, Eldridge M, Federico P, Kunz TH. 2012. Bats track and exploit changes in insect pest populations. PLoS ONE. 7(8):e43839.
  6. Omatsu T, Watanabe S, Akashi H, Yoshikawa Y. 2007. Biological characters of bats in relation to natural reservoir of emerging viruses. Comparative Immunology, Microbiology & Infectious Diseases. 30:357–374.
  7. O’Shea TJ, Cryan PM, Cunningham AA, Fooks AR, Hayman DTS, Luis AD, Peel AJ, Plowright RK, Wood JLN. 2014. Bat flight and zoonotic viruses. Emerging Infectious Diseases. 20(5):741–745.
  8. Racey PA. 2015. The uniqueness of bats. In: Bats and Viruses: A New Frontier of Emerging Infectious Diseases. L‐F Wang and C Cowled (eds). Wiley Blackwell: Hoboken, NJ, pp. 1–22.
  9. Smith I, Wang L‐F. 2013. Bats and their virome: an important source of emerging viruses capable of infecting humans. Current Opinion in Virology. 3:84–91.
  10. Wang L‐F, Walker PJ, Poon LLM. 2011. Mass extinctions, biodiversity and mitochondrial function: are bats ‘special’ as reservoirs for emerging viruses? Current Opinion in Virology. 1:649–657.
  11. Zhou P, Tachedjian M, Wynne JW, Boyd V, Cui J, Smith I, Cowled C, Ng JHJ, Mok L, Michalski WP, Mendenhall IH, Tachedjian G, Wang L‐F, Baker ML. 2016. Contraction of the type I IFN locus and unusual constitutive expression of IFN‐α in bats. PNAS. 113(10):2696–2701.

ABOUT THE COMPANION WEBSITE

This book is accompanied by a companion website:

www.wiley.com/go/batsandhumanhealth

There you will find valuable material designed to enhance your learning, including:

  • Supplementary Materials
    • Database of Bat Species
  • Further reading
  • Useful websites
    • Bat Conservation Groups
    • Bat Photographs

Scan this QR code to visit the companion website.

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The password is “First word of First paragraph in Chapter 2.”

I
INTRODUCTION