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What Links Bats to Emerging Infectious Diseases?

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  • Matthew Jeffery
    http://www.sciencemag.org/cgi/content/full/310/5748/628?ijkey=CyFDQIJOUZ212&keytype=ref&siteid=sci Science, Vol 310, Issue 5748, 628-629 , 28 October 2005
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      http://www.sciencemag.org/cgi/content/full/310/5748/628?ijkey=CyFDQIJOUZ212&keytype=ref&siteid=sci

      Science, Vol 310, Issue 5748, 628-629 , 28 October
      2005
      Dobson, A. P.

      This article appears in the following Subject
      Collections:
      Virology

      [DOI: 10.1126/science.1120872]
      Perspectives
      VIROLOGY:
      What Links Bats to Emerging Infectious Diseases?
      Andrew P. Dobson*

      Three species of horseshoe bats (Rhinolophus spp.)
      have now been
      officially recorded as the natural
      reservoir host of the coronavirus that causes severe
      acute respiratory
      syndrome (SARS) [see the
      report by Li et al. on page 676 of this issue (1) and
      the report by Lau
      et al. (2)]. The emergence
      of this pathogen (SARS-CoV) in southern China in
      2002-2003 almost
      brought the burgeoning economy of
      Southeast Asia to its knees (3, 4). Bats are now known
      to be natural
      reservoir hosts to several
      other new emergent disease pathogens: Nipah and Hendra
      viruses (5) and
      potentially Ebola and Marburg
      viruses. They are also reservoirs to "older" and more
      well-known
      pathogens, such as rabies virus,
      which frequently resurge into human populations or
      domestic livestock.
      Fieldwork on SARS illustrates
      not only the crucial role that conservation
      organizations play in
      frontline research on emergent
      diseases, but also the shortcomings in our
      understanding of the
      etiology of these diseases.

      A key step in determining the threat imposed by new
      pathogens is
      identifying the route along which
      they are transmitted from their reservoir to new hosts
      such as domestic
      livestock or humans. In the
      case of pathogens that use bats as reservoirs, a
      common route seems
      likely. Bats' feeding habits are
      constrained by the aerodynamics of flight, so they
      can't ingest huge
      amounts of food. Yet many bats
      are frugivorous--that is, they meet their energy
      requirements by
      ingesting fruits. But instead of
      swallowing them, they chew them to extract the sugars
      and higher energy
      components, and then spit
      out the partially digested fruits, which drop to the
      ground. Other
      animal species can ingest these
      fruit remnants and may consequently become infected
      with virus
      particles in residual bat saliva. A
      small variant on this is required in the case of the
      insectivorous
      Rhinolophus bat species, but they
      also discard the heavier body parts of the insects
      they eat, which are
      then ingested by terrestrial
      foraging species. This provides a route for SARS-CoV
      to be infrequently
      transmitted to masked palm
      civets (Paguma larvata), the animals that were
      initially considered to
      be the potential virus
      reservoirs in the SARS epidemics. It would also
      explain how gorillas,
      chimpanzees, and duikers
      acquire Ebola virus during seasonal fruiting events
      when bats and
      primates feed in or below
      fruit-bearing trees. The animal pens of the pig farms
      where the Nipah
      virus outbreak in Malaysia was
      first reported were littered with partially digested
      fruits that were
      regurgitated from bats.
      Similar observations were reported at the site of the
      Hendra virus
      outbreak in Queensland,
      Australia. In Bangladesh, the Nipah virus has been
      shown to be
      transmitted directly from bats to
      humans. There, during the fruiting season, young boys
      climb trees to
      pick fruit. They frequently add
      fruit that is partially chewed by bats to their
      collections, which they
      then sell to the local
      salesmen. The fruit is pulped to produce a drink that
      is sold in
      neighboring villages. The Nipah
      outbreaks there often follow the trails of these
      bicycle-borne salesmen
      (6).

      The transmission dynamics of these emerging viruses
      can be readily
      modeled in a framework originally
      developed to examine the rate of spread of HIV-AIDS in
      populations with
      heterogeneous mixing of
      people with different levels of sexual activity (7).
      The key difference
      with using this approach to
      examine emergent diseases is that transmission of
      emergent pathogens
      between populations tends to be
      unidirectional (8). Thus, bats transmit SARS-CoV to
      palm civets, but
      not vice versa. This means that
      control of the disease has to focus on either
      controlling its abundance
      in its reservoir, preventing
      its spillover between hosts, or rapidly reducing its
      spread once it has
      infected humans or domestic
      livestock. This creates a dilemma for both public
      health and
      conservation biology: Should we attempt
      to control potentially emergent pathogens by focusing
      on their
      reservoir hosts, or should we try and
      prevent the spillover events that allow the pathogen
      to spread in a new
      population? A third option
      is to develop a vaccine to protect hosts in the
      spillover population.
      Unfortunately, because
      spillover is likely to be a random event, effective
      protection requires
      that all individuals in the
      spillover population become protected. We have never
      achieved this
      level of coverage for well-known
      pathogens that have fairly safe and effective vaccines
      (9).

      Figure 1 Bats, the great natural reservoir for
      viruses. Knowing
      more about bat ecology and
      immunology is crucial to controlling spillover of
      viruses and related
      diseases to humans.

      CREDIT: TIGGA KINGSTON/BOSTON UNIVERSITY

      The two viable alternatives are either to reduce the
      prevalence of the
      pathogen in the reservoir
      host, or to identify the conditions that lead to
      spillover and attempt
      to minimize these. The latter
      will involve surveying a diversity of wild species for
      potential
      pathogens and unraveling the
      changes in ecological conditions that lead to
      spillover events. In both
      these areas, conservation
      organizations seem to be playing almost as important a
      role as medical
      schools. This is both ironic
      and tragic given that conservation nongovernmental
      organizations have
      much smaller budgets and
      broader agendas than medical schools.

      Is it unusual that so many emergent diseases use bats
      as reservoirs?
      What's special about bats? We
      often forget that bats form a sizable proportion of
      mammalian
      diversity; the 916 extant species
      constitute about 20% of this diversity (10). Thus, if
      all potential
      reservoirs were created equal,
      we would expect almost as many emergent pathogens from
      bats as from
      small mammals. This is not the
      case; less than 2% of human pathogens have bats as
      natural reservoirs
      [bats may be persistently
      infected, yet never display any pathologies (11)].
      These data suggest
      that bats are not
      overrepresented in the numbers of pathogens that
      emerge from them. What
      is more conspicuous is the
      pronounced pathology of pathogens that spill over from
      bats and that
      most of these spillovers have
      occurred in the last 20 years. What might cause this?

      One obvious difference between bats and other mammals
      is that bats fly.
      This means that they have
      hollow bones, as do birds. But bone marrow is where
      most mammals
      produce the B cells of the immune
      system. Where do bats produce B cells? Unfortunately,
      we don't know
      enough about bat immunity to
      address this question. They may compensate by
      increasing B cell
      production in the marrow of their
      pelvis and legs, but we have little data on this. Bats
      are long-lived,
      highly gregarious, and can
      enter torpor. We do not know whether these traits
      allow these ancient
      mammals to differ from other
      mammals in the way they combat potential viral
      infections. Are there
      differences in the
      functionality or type of receptors required for
      infection? Are there
      bat antiviral proteins
      (interferons) that can stop viral replication as in
      other mammals, or
      do bats possess a mechanism to
      prevent their inactivation? Alternatively, we could
      ask if bats possess
      a novel innate immunity that
      allows them to cope with certain classes of viruses in
      ways that other
      mammals cannot. If the latter
      is the case, then what would studies of bat immunity
      tell us about new
      ways to attack and treat
      viral diseases? The literature is silent on this. Very
      few medical
      schools have experimental bat
      colonies, and work in this area may be a little
      "outside the box" for
      conservative funding agencies.

      Knowing more about bats, and particularly more about
      bat ecology and
      immunology, is crucial if we
      are to develop new treatments and ways to control the
      viral diseases
      that are an increasing threat
      to humans. Assuming we can control these diseases by
      simply controlling
      bats is both naïve and
      short-sighted. Instead, we must recognize that
      increased rates of
      spillover-mediated pathogen
      transmission from bats to humans may simply reflect an
      increase in
      their contact through
      anthropogenic modification of the bat's natural
      environment. The
      emergence of Nipah virus and
      SARS-CoV epitomizes this situation. In regions where
      large areas of bat
      habitat have been converted
      to agricultural land or oil palm plantations, the
      surviving bat
      populations will be concentrated in
      the remaining patches of forest that provide the
      resources they need.
      When these patches of fruit
      trees are used as shade for intensive animal
      husbandry, then it is
      highly likely that the fruits and
      insects chewed by bats will find their way into the
      human food chain.

      The scientists who revealed the bat reservoir of
      SARS-CoV operate
      within a new intellectual
      paradigm. They call their discipline "conservation
      medicine" (12). It
      brings together the two areas
      of natural science that will be crucial to the future
      welfare of
      humans: health sciences (human,
      veterinary, and plant pathology) and the ecological
      sciences that
      monitor the health of populations,
      communities, and ecosystems. The Millenium Ecosystem
      Assessment has
      emphasized the dependence of
      human health and economic well-being on goods and
      services provided by
      the natural environment (13).
      This dependence can only be actively capitalized upon
      if we increase
      our understanding of the
      population dynamics and ecology of new and old
      infectious diseases.
      Conservation medicine is an idea
      whose time has come none too soon.

      References and Notes

      1. W. Li et al., Science 310, 676 (2005);
      published online 29
      September 2005
      (10.1126/science.1118391).
      2. S. K. P. Lau et al. Proc. Natl. Acad. Sci.
      U.S.A. 102, 14040
      (2005). [Medline]
      3. A. R. McLean, R. M. May, J. Pattison, R. A.
      Weiss, in SARS. A
      Case Study in Emerging
      Infections (Oxford Univ. Press, Oxford, 2005).
      [publisher's
      information]
      4. U. D. Parashar, L. J. Anderson, Int. J.
      Epidemiol. 33, 628
      (2004). [Medline]
      5. A. D. Hyatt, P. Daszak, A. A. Cunningham, H.
      Field, A. R. Gould,
      EcoHealth 1, 25 (2004).
      6. V. P. Hsu et al. Emerg. Infect. Dis. 10, 2082
      (2004). [Medline]
      Diseases) and it should be
      italicized.
      7. O. Diekmann, J. A. P. Heesterbeek, J. A. J.
      Metz, J. Math. Biol.
      28, 365 (1990). [Medline]
      8. A. P. Dobson, Am. Nat. 164, S64 (2004).
      [Abstract]
      9. D. J. Nokes, R. M. Anderson, Lancet 2, 1374
      (1988). [Medline]
      10. K. E. Jones, A. Purvis, A. MacLarnon, O. R.
      Bininda-Emonds, N.
      Simmons, Biol. Rev. 77, 223
      (2002). [Medline]
      11. M. E. J. Woolhouse, S. Gowtage-Sequeria, Emerg.
      Infect. Dis., in
      press.
      12. A. A. Aguirre, R. S. Ostfeld, G. M. Tabor, C.
      House, M. C.
      Pearl, in Conservation Medicine.
      Ecollogical Health in Practice (Oxford Univ. Press,
      Oxford, 2002).
      [publisher's information]
      13. Millenium Ecosystem Assessment. Ecosystems and
      Human Well-Being:
      A Framework for Assessment
      (Island Press, Washington, DC, 2003). [publisher's
      information]
      14. I am grateful to J. Childs, P. Daszak, A.
      Hyatt, S. Kutz, J.
      Rowenthal, and S. Luby for
      comments on an earlier draft of this essay. My
      research is funded by
      the NIH/NSF Ecology of
      Infectious Disease Program.

      10.1126/science.1120872
      The author is in the Department of Ecology and
      Evolutionary Biology,
      Princeton University,
      Princeton, NJ 08544-1003, USA. E-mail:
      dobber@...

      10.1126/science.1120872
      Include this information when citing this paper.

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      http://www.sciencemag.org/cgi/reprint/310/5748/628?ijkey=CyFDQIJOUZ212&keytype=ref&siteid=sci




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