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Fondazione Edmund Mach
                               San Michele all’Adige (I)




  Global Change and
  the World's Mountains
Perth, Scotland, 26-30 September 2010




       Climate change and biodiversity loss as
       drivers for zoonotic diseases emergence in
       the Alps: the case of tick- borne encephalitis


                              Annapaola Rizzoli, DVM, PhD
                      Roberto Rosà, Heidi Hauffe, Markus Neteler,
               Valentina Tagliapietra, Daniele Arnoldi, Francesca Cagnacci
Tick-borne encephalitis in Europe

  •Tick-borne encephalitis virus (TBEV) is a single-stranded RNA virus that
  belongs to the genus Flavivirus

  •Three subtypes: W European (WE), Siberian (SIB), and Far Eastern (FE)

  • Transmitted to humans mostly through the bite of an infected tick of the
  Ixodes species, primarily I. ricinus (European subtype) or I. persulcatus
  (Siberian and Far Eastern subtypes).

  • The prevalence of TBE increased
   by almost 400% in the last 30 years (14,000 cases/year)

  • TBE is endemic in temperate regions
  of Europe and Asia but new foci are discovered

  • Evidences of altitudinal shift in many regions
Network of independent but synergistic biological and non-biological factors
                                                           Examples of data from Estonia, Latvia, Lithuania, Slovenia and Czech Republic.




                                                                                                                                               Industria l employee s,

                                                                                                                                                % of pre -1990 le ve l
                                                                                                                                                                                      employees




                                                                                                                                                 Ind ustr ial outp ut,
                                                                                                                                                                         100          LT
                                                                                                                                                                            80
                                                                                                                                                                                                                                                                                                 Reduced                                                                                   Environmental
                                                          Socio-economic                                                                                                    60
                                                                                                                                                                                                                                                                                                 industrial                                                                                 awareness?
                                                             transition                                                                                                     40                                                                                                                    pollution
                                                                                                                                                                                       output LV
                                                                                                                                                                            20
                                                                                                                                                                                                                                                                                                                                                      Global brightening ??




                                                                                                                                                                                  1 97 0


                                                                                                                                                                                           1 98 0



                                                                                                                                                                                                    1 99 0


                                                                                                                                                                                                                                            2 00 0
                                          Decline of
                                          agriculture                                                                      Higher                                                                            Higher TBE incidence                                                                                                                                                          Sudden increase
                                                                                                                        unemployment                                                                                                                                                                                                                                                    in Spring temperature
                                                                                                       % unemployment


                                                                                                                        15                                                                                   60                                      LV
                                                                                                                                                 SI
   % of mean for 1986-88




                                                                                                                                                                                                             TBE cases/100,000 population
    Nationl catt le herd,




                            100
                                                                                                                        10
                                                                                                                                                                                                             40                                                                                                                                                                                                              ES      24            21-30.Apr




                                                                                                                                                                                                                                                                                                                                                         Mean daily max temp
                                                                                                  SI                                                                                                                                                                                                                                                                           8           1.Mar-20.Apr
                               80
                                                                                                                        5                                                 CZ                                                                                                                                                                                                                                                         20
                                                                                                                                                                                                                                                                                                                                                                               6
                               60
                                                                                                                                                                                                             20                                                                                                                                                                                                                      16
                                                                                                                        0                                                                                                                                                                                                                                                      4
                               40                                                                 CZ
                                                                                                                             1 97 0


                                                                                                                                      1 98 0


                                                                                                                                                      1 99 0


                                                                                                                                                                         2 00 0                                                                                                                                                                                                2                                                     12
                               20                                                                 LV                                                                                                              0




                                                                                                                                                                                                                                             197 0




                                                                                                                                                                                                                                                                           198 0




                                                                                                                                                                                                                                                                                                  199 0




                                                                                                                                                                                                                                                                                                                         200 0
                                                                                                                                                                                                                                                                                                                                                                               0                                                       8
                                          1970


                                                        1980


                                                                      1990


                                                                                    2000




                                                                                                                                                                                                             20
                                                                                                                                                                                                                                                     CZ                                                                                                                        -2                                                      4




                                                                                                                                                                                                                                                                                                                                                                                      1970


                                                                                                                                                                                                                                                                                                                                                                                                         1980


                                                                                                                                                                                                                                                                                                                                                                                                                      1990


                                                                                                                                                                                                                                                                                                                                                                                                                              2000



                                                                                                                                                                                                                                                                                                                                                                                                                                            1970


                                                                                                                                                                                                                                                                                                                                                                                                                                                          1980


                                                                                                                                                                                                                                                                                                                                                                                                                                                                    1990


                                                                                                                                                                                                                                                                                                                                                                                                                                                                              2000
                                                                                                                                                                                                              0
                                                                                                                        More wealth


                                                                                                                                                                                                                                             1970




                                                                                                                                                                                                                                                                1975




                                                                                                                                                                                                                                                                           1980




                                                                                                                                                                                                                                                                                          1985




                                                                                                                                                                                                                                                                                                  1990




                                                                                                                                                                                                                                                                                                                 1995




                                                                                                                                                                                                                                                                                                                          2000




                                                                                                                                                                                                                                                                                                                                        2005
                    nat ional land area




                                          50                                                                            & leisure                                                                                                                    SI
                                          40                                                                                                                                                                 20
                         % of tot al




                                                                                wooded LV
                                          30
                                                                                                                                                                                                                                                                                                                                                                               Increased co-feeding
                                                                                                                                                                                                                   0
                                                                                                                                                                                                                                                                                                                                                                               transmission of TBEV                                                   More hosts
                                                                                                                                                                                                                                            1970



                                                                                                                                                                                                                                                                          1980



                                                                                                                                                                                                                                                                                                 1990



                                                                                                                                                                                                                                                                                                                        2000
                                          20

                                          10
                                                                         field crops LV                                  Greater human                                                                                                                                                                                                                                                                                                               for adult ticks
                                            0
                                                                                                                        exposure to ticks                                                                            More infected ticks
                                                 1970


                                                               1980


                                                                             1990


                                                                                           2000




                                                                                                                                                                                                                                                                                                                                                                                                   20           LV                                          CZ
                                                                                                                           in forests?




                                                                                                                                                                                                                                                                                                                                                                               wild boar/1000 ha
                                                                                                                                                                                                                                                                                                                                                                                                                                                     20




                                                                                                                                                                                                                                                                                                                                                                                                   15




                                                                                                                                                                                                                                                                                                                                                                                   Roe deer &
                                                                                                                                                                                                                                                                                                                                                                                                                                                     15




                                                                                                                                                                                                                                                                                                                                                                                                   10                                                10




                                                                                                                                                                                                                                                                         100
                                                                                                                                                                                                                                                     Adult ticks , May




                                                                                                                                                                                                                                                                                                                                  LV                                                               5
                                                                             Regeneration of                                                                                                                                                                             80
                                                                                                                                                                                                                                                                                                                                                                                                                                                     5




                                                                                                                                      Increase in rodent                                                                                                                 60
                                                                                                                                                                                                                                                                                                                                                                                                   0                                                 0




                                                                             shrubs




                                                                                                                                                                                                                                                                                                                                                                                                        1970


                                                                                                                                                                                                                                                                                                                                                                                                                     1980


                                                                                                                                                                                                                                                                                                                                                                                                                             1990


                                                                                                                                                                                                                                                                                                                                                                                                                                     2000
                                                                                                                                      populations




                                                                                                                                                                                                                                                                                                                                                                                                                                                     1970



                                                                                                                                                                                                                                                                                                                                                                                                                                                                 1980



                                                                                                                                                                                                                                                                                                                                                                                                                                                                           1990



                                                                                                                                                                                                                                                                                                                                                                                                                                                                                     2000
                                                                                                                                                                                                                                                                         40

                                                                                                                                      (transmission hosts)                                                                                                               20
                                                                                                                                                                                                                                                                                   0
                                                                                                                                                                                                                                                                                   1970


                                                                                                                                                                                                                                                                                                          1980


                                                                                                                                                                                                                                                                                                                                 1990


                                                                                                                                                                                                                                                                                                                                               2000




                                                                                                                                                                                                                                                                                                                                                                               More ticks

 Courtesy: Sarah Randolph
Šumilo D, Randolph SE et al (2008) Revs Med Virol                                                                                                                                                                                                                                                                                                     Sumilo D, Randolph SE, et al PLoS ONE (2007) e500
Ecological factors affecting
Ecological factors
            TBEv circulation within natural foci




                                                   R0
Key hosts threshold density and TBE persistence
                     Parameter estimates obtained from Trentino data
Threshold density of               and from literature
     competent
    rodent hosts                                           10
                   Roe deer density (ha-1) – Log scale




                                                            1
                                                                                                                           “Diverting”
                                                                                                                             effect’
                                                                                            Range of observed                of deer
                                                          0.1                                  host density

                                                                       R0 < 1           R0 = 1              R0 > 1

                                                                                                                               Threshold
                                                         0.01                                                                density and a
                                                                                                                             positive effect
                                                                                                                                of deer
                                                                                                                             density on tick
                                                         0.001
                                                                                                                              abundance
                                                                 0.1                1                     10         100

                                                                                Rodent density (ha-1) – Log scale
TBE model
Complex dynamics in time and space




                                     m L NL 1L c1N LH1 N L (1   NL / k N k L )
                          R0,TBE 
                                                       dT  g N
Upsurge of TBE in northern Italy




                   Graph showing numbers of mean annual incidence (n. of cases/100.000 inhabitants)
                   and annual TBE confirmed human cases in the positive provinces
Changes in climate



      MAP of TBE positive and TBE negative provinces




 • Increase of Avg.yr.Tmin on a 50yr
 period was 0.75 °C

 • Increase of Avg.yr.Tmax on a 50yr
 period was 1.7 °C

 • Decrease of Avg.yr.prec on a 50yr
 period was -180mm                                     Trends in annual total precipitation (top), annual minimum (middle)
                                                        and maximum (bottom) daily air temperature in the TBE-negative provinces (left panels)
                                                        and TBE-positive provinces (right panels) in northern Italy from 1950 to 2006
                                                       (Rizzoli et al., Plos one, 2009)
Changes in deer abundance
              Changes in roe deer density in provinces TBE positive (Trento
                       and Belluno) and TBE negative (Sondrio)

   7

   6

   5

   4                                                                                                                      Trento
                                                                                                                          Belluno
   3                                                                                                                      Sondrio
   2

   1

   0
   53

         65

               69

                     71

                           73

                                 75

                                       77

                                             79

                                                   81

                                                         83

                                                               85

                                                                     87

                                                                           89

                                                                                 91

                                                                                       93

                                                                                             95

                                                                                                   97

                                                                                                         99

                                                                                                               01

                                                                                                                     03
  19

        19

              19

                    19

                          19

                                19

                                      19

                                            19

                                                  19

                                                        19

                                                              19

                                                                    19

                                                                          19

                                                                                19

                                                                                      19

                                                                                            19

                                                                                                  19

                                                                                                        19

                                                                                                              20

                                                                                                                    20




                                                                                                         Boxplot of mean values of coppice to high forest ratio (cop.hfor)(left panel)
                                                                                                         and mean values of roe deer abundance (right panel) in TBE positive and TBE
                                                                                                         negative provinces of northern Italy (Rizzoli et al., Plos one, 2009)
Changes in forest cover and structure

   - 14% of the total wooded areas increased
         from 1950 to 2002
   - Major increase in
         - high stand mixed forest (184%)
         - broad leaf coppices (359%)
         - total mixed coppices (154%)




  Mean coppice and high forest cover recorded in TBE-negative provinces (left panel)
  and TBE-positive provinces (right panel) (Rizzoli et al., Plos one, 2009)
Conclusion

  Protection from natural hazards, including infectious diseases, and health
  protection are considered among the most relevant services provided by mountain
  ecosystems;

   Global changes, including the invasion by alien species, are favouring the
  emergence of several animal and zoonotic diseases in world’s mountains;

  Habitat changes and biodiversity loss favor TBD’s emergence: TBD’s pathogens
  circulation is in fact supported mostly by generalist species (rodents, large game
  species, I. ricinus)

  Urgent need to better understand the effects of multi-trophic interactions under a
  global change scenario across altitudinal gradients

  Emerging diseases in mountains should be addedd to the “emerging
  themes” to be covered by integrated research strategies because of their
  dramatic impact on well being and economy
Acknowledgements




              The Reseach Fund of
                the Autonomous
               Province of Trento




Contacts
annapaola.rizzoli@iasma.it

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Climate change and biodiversity loss as drivers for zoonotic diseases emergence in the Alps: the case of tick-borne encephalitis [Annapaola Rizzoli]

  • 1. Fondazione Edmund Mach San Michele all’Adige (I) Global Change and the World's Mountains Perth, Scotland, 26-30 September 2010 Climate change and biodiversity loss as drivers for zoonotic diseases emergence in the Alps: the case of tick- borne encephalitis Annapaola Rizzoli, DVM, PhD Roberto Rosà, Heidi Hauffe, Markus Neteler, Valentina Tagliapietra, Daniele Arnoldi, Francesca Cagnacci
  • 2. Tick-borne encephalitis in Europe •Tick-borne encephalitis virus (TBEV) is a single-stranded RNA virus that belongs to the genus Flavivirus •Three subtypes: W European (WE), Siberian (SIB), and Far Eastern (FE) • Transmitted to humans mostly through the bite of an infected tick of the Ixodes species, primarily I. ricinus (European subtype) or I. persulcatus (Siberian and Far Eastern subtypes). • The prevalence of TBE increased by almost 400% in the last 30 years (14,000 cases/year) • TBE is endemic in temperate regions of Europe and Asia but new foci are discovered • Evidences of altitudinal shift in many regions
  • 3. Network of independent but synergistic biological and non-biological factors Examples of data from Estonia, Latvia, Lithuania, Slovenia and Czech Republic. Industria l employee s, % of pre -1990 le ve l employees Ind ustr ial outp ut, 100 LT 80 Reduced Environmental Socio-economic 60 industrial awareness? transition 40 pollution output LV 20 Global brightening ?? 1 97 0 1 98 0 1 99 0 2 00 0 Decline of agriculture Higher Higher TBE incidence Sudden increase unemployment in Spring temperature % unemployment 15 60 LV SI % of mean for 1986-88 TBE cases/100,000 population Nationl catt le herd, 100 10 40 ES 24 21-30.Apr Mean daily max temp SI 8 1.Mar-20.Apr 80 5 CZ 20 6 60 20 16 0 4 40 CZ 1 97 0 1 98 0 1 99 0 2 00 0 2 12 20 LV 0 197 0 198 0 199 0 200 0 0 8 1970 1980 1990 2000 20 CZ -2 4 1970 1980 1990 2000 1970 1980 1990 2000 0 More wealth 1970 1975 1980 1985 1990 1995 2000 2005 nat ional land area 50 & leisure SI 40 20 % of tot al wooded LV 30 Increased co-feeding 0 transmission of TBEV More hosts 1970 1980 1990 2000 20 10 field crops LV Greater human for adult ticks 0 exposure to ticks More infected ticks 1970 1980 1990 2000 20 LV CZ in forests? wild boar/1000 ha 20 15 Roe deer & 15 10 10 100 Adult ticks , May LV 5 Regeneration of 80 5 Increase in rodent 60 0 0 shrubs 1970 1980 1990 2000 populations 1970 1980 1990 2000 40 (transmission hosts) 20 0 1970 1980 1990 2000 More ticks Courtesy: Sarah Randolph Šumilo D, Randolph SE et al (2008) Revs Med Virol Sumilo D, Randolph SE, et al PLoS ONE (2007) e500
  • 4. Ecological factors affecting Ecological factors TBEv circulation within natural foci R0
  • 5. Key hosts threshold density and TBE persistence Parameter estimates obtained from Trentino data Threshold density of and from literature competent rodent hosts 10 Roe deer density (ha-1) – Log scale 1 “Diverting” effect’ Range of observed of deer 0.1 host density R0 < 1 R0 = 1 R0 > 1 Threshold 0.01 density and a positive effect of deer density on tick 0.001 abundance 0.1 1 10 100 Rodent density (ha-1) – Log scale TBE model
  • 6. Complex dynamics in time and space m L NL 1L c1N LH1 N L (1   NL / k N k L ) R0,TBE  dT  g N
  • 7. Upsurge of TBE in northern Italy Graph showing numbers of mean annual incidence (n. of cases/100.000 inhabitants) and annual TBE confirmed human cases in the positive provinces
  • 8. Changes in climate MAP of TBE positive and TBE negative provinces • Increase of Avg.yr.Tmin on a 50yr period was 0.75 °C • Increase of Avg.yr.Tmax on a 50yr period was 1.7 °C • Decrease of Avg.yr.prec on a 50yr period was -180mm Trends in annual total precipitation (top), annual minimum (middle) and maximum (bottom) daily air temperature in the TBE-negative provinces (left panels) and TBE-positive provinces (right panels) in northern Italy from 1950 to 2006 (Rizzoli et al., Plos one, 2009)
  • 9. Changes in deer abundance Changes in roe deer density in provinces TBE positive (Trento and Belluno) and TBE negative (Sondrio) 7 6 5 4 Trento Belluno 3 Sondrio 2 1 0 53 65 69 71 73 75 77 79 81 83 85 87 89 91 93 95 97 99 01 03 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 20 20 Boxplot of mean values of coppice to high forest ratio (cop.hfor)(left panel) and mean values of roe deer abundance (right panel) in TBE positive and TBE negative provinces of northern Italy (Rizzoli et al., Plos one, 2009)
  • 10. Changes in forest cover and structure - 14% of the total wooded areas increased from 1950 to 2002 - Major increase in - high stand mixed forest (184%) - broad leaf coppices (359%) - total mixed coppices (154%) Mean coppice and high forest cover recorded in TBE-negative provinces (left panel) and TBE-positive provinces (right panel) (Rizzoli et al., Plos one, 2009)
  • 11. Conclusion Protection from natural hazards, including infectious diseases, and health protection are considered among the most relevant services provided by mountain ecosystems;  Global changes, including the invasion by alien species, are favouring the emergence of several animal and zoonotic diseases in world’s mountains; Habitat changes and biodiversity loss favor TBD’s emergence: TBD’s pathogens circulation is in fact supported mostly by generalist species (rodents, large game species, I. ricinus) Urgent need to better understand the effects of multi-trophic interactions under a global change scenario across altitudinal gradients Emerging diseases in mountains should be addedd to the “emerging themes” to be covered by integrated research strategies because of their dramatic impact on well being and economy
  • 12. Acknowledgements The Reseach Fund of the Autonomous Province of Trento Contacts annapaola.rizzoli@iasma.it