DISEASE ECOLOGY IN MULTI-HOST SYSTEMS AT WILDLIFE/LIVESTOCK INTERFACESCONCEPTS AND APPLICATIONS
CARON, A. , GAIDET, N., CAPPELLE, J., MIGUEL, E., CORNELIS, D., GROSBOIS, V., DE GARINE-WICHATITKSY, M.
Presented to ILRI at an open seminar on the 10th of June 2015, Nairobi
GENERAL CONTEXT: AFRICAN SOCIO-ECOSYSTEMS
• Arid & Semi-arid ecosystems
• Coexistence of People & Nature
• Development & Biodiversity Conservation
• Emerging & neglected diseases
Wildlife/Livestock/Human interface
Pathogen transmission
CONCEPTS IN DISEASE ECOLOGY
• Reservoir
• Maintenance host
• Target Host Haydon et al. 2002, Ashford 1997, 2003
M T
Maintenance Host
Target Host
Spillover
Spillback
Critical Population Size
Susceptibility, Replicate, Excrete
Inter-species Contact Patterns
CONCEPTS IN DISEASE ECOLOGY
M T
Spillover
To prevent and control disease…
1. Host control 2. Contact control
e.g. vaccination or culling
ECOLOGY OF BUFFALO - CATTLE INTERACTIONS
IMPLICATIONS FOR DISEASE TRANSMISSION AT WILDLIFE/LIVESTOCK INTERFACES IN TFCAS
CARON, A. , DE GARINE-WICHATITSKY, M., MIGUEL, E., GROSBOIS, V., FOGGIN, C., HOFMEYR, M. CORNELIS, D.
An example of contact patterns at W/L interface & Implications
TRANSFRONTIER CONSERVATION AREAS
GLTFCA & KAZA TFCA
EXAMPLE: BOVINE TB SPREAD IN THE GREAT LIMPOPO TFCA
de Garine-Wichatitsky et al. 2010, Kock et al. 2014
DISEASE BURDEN AT THE WILDLIFE/LIVESTOCK INTERFACE IN THE GLTFCA
Unfenced Interface Malipati Pesvi
Buffalo Cattle Cattle
bTB (SCITT)
NA 1.03% 2/195, 0.0-2.4
1.68% 3/179, 0.0-3.6
FMD SAT 1 92.1%
35/38, 87.7-96.5 7.1%
5/70, 4.1-10.2 NA
SAT 2 68.4% 26/38, 60.9-75.9
1.4% 1/70, 0.0-2.8
NA
SAT 3 65.8% 25/38, 58.1-73.5
2.9% 2/70, 0.1-4.8
NA
Subtotal 94.7% 36/38, 91.1-98.3
10.0% 7/70, 6.4-13.6
NA
Br 0.0% 9.6% 16.0% (RBT & c-ELISA) 0/38, <7.8 55/575, 7.2-12.0 84/526, 12.8-19.1 RVF 5.3% 18.3% NA (I-ELISA) 2/38, 0.0-12.5 13/71, 9.2-27.4 Th IFA 3.7%
1/27, 0.0-11.0 3.2%
1(3)/31, 0.0-9.5 42.5%
17(5)/40, 27.0-58.0 RT-PCR 88.2%
15/17, 72.4-100.0 NA NA
LSD 0.0% 52.2% NA (VNT) 0/21, <14.1 35/67, 40.2-64.3
!
Caron et al. 2013
OBJECTIVE: FREQUENCY AND INTENSITY OF CONTACTS BETWEEN CATTLE AN BUFFALO AT DIFFERENT WILDLIFE/LIVESTOCK INTERFACES IN TFCAS
PROTOCOL Material(&Methods(
(• Regular(blood(sampling(in(ca6le(and(opportunis7c(in(buffaloes(
Communal(area(• 45(GPS(collars(on(ca2le((
(1/herd)((GPS(point(every(hour(
Na>onal(parks(• 68(GPS(collars((on(buffalos((
(3/herd)((GPS(point(every(hour(
2009(2008( 2011(2010( 2013(
12B/12C(GNP(
6B/6C(GNP(
12B/6C(Crook(
20B/12C(Crook(
18B/9C(KNP(
Regular blood sampling in cattle populations and opportunistic buffaloes
2 INTERFACES IN THE GLTFCA
LIMPOPO RIVER ADULT FEMALES
Adult female HR: localised ratios Transboundary populations
No use of Sengwe corridor Buffalo population connectivity: none
INTERFACE BETWEEN BUFFALO & CATTLE
Cattle GPS point
Buffalo Home Range
DEFINITION OF CONTACTS BETWEEN BUFFALO & CATTLE —> E.G. FMD
Space & time window for Foot and Mouth Disease :
0-15d & 0-300m
So a contact occurs when a cattle position is recorded within 300 m of the buffalo position less than 15 days after the buffalos
position recording
IDENTIFYING CONTACTS
Cattle Home Range
Buffalo Home Range
Buffalo/Cattle contact
RELATIONSHIP BETWEEN CONTACT & FMD INCIDENCE IN CATTLE
0
0,1
0,2
0,3
0,4
0,5
0,6
0,7
0 0,5 1 1,5 2 2,5 3 3,5 4 4,5 5 5,5 6 6,5 7 7,5 8 8,5 9
Pred
icted
serological inciden
ce
log(number of contacts) [herd&period specific]
Estimated serological incidence rate over 4 month periodsas a function of contact rate
0→1/(0→1+0→0)329 transitions/164 individuals/32 herds
Miguel et al. 2013
MODEL CAN BE ADAPTED TO OTHER PATHOGENS
Contact definition:
• Can be adapted to different pathogens:
• bTB • Tick-borne diseases…
Different contact pattern according to pathogen chosen
de Garine-Wichatitsky et al. in prep
NEW PROTOCOL IN OCTOBER 2013
Adult female -> localised HR Adult male -> 2 tries -> 2 failures Young female hypothesis: n=19; between 2.5 and 4.5 years
Caron et al., Revision EID
SPEEDY, RARE AND SEASONAL PATTERN?
Caron et al., Revision EID
IMPLICATION FOR BUFFALO ECOLOGY & CONSERVATION
Ecology of the African buffalo
• Outbreeding behavior during rainy season
A case or not for the Sengwe Corridor?
Redefinition of the W/L interface?
• Not restrained to land-use boundaries • Relevance of boundaries of the GLTFCA
IMPLICATION FOR DISEASE MANAGEMENT
Clear and strong hypothesis to explain the spread of bTB from KNP to GNP
Measuring intensity and frequency of contacts?
• Who is migrating? How? How often?
How do we manage such « new » interface?
• E.g. FMD surveillance & control
BRIDGE HOSTS, A MISSING LINK IN DISEASE ECOLOGY IN MULTI-HOST SYSTEMS
IMPLICATIONS FOR AIV ECOLOGY AT WILD/DOMESTIC BIRD INTERFACE IN SOUTHERN AFRICA
CARON, A. , CAPPELLE, J., CUMMING, G.S, MUNDAVA, J., GROSBOIS, V., DE GARINE-WICHATITSKY, M., GAIDET, N.
An example of Conceptual Development & Implications
CONCEPTS IN DISEASE ECOLOGY
M T
Contact
Transmission
BBridge Host
Caron et al. 2015
So far, not properly defined
BRIDGE HOST PROPERTIES
• Contact with the maintenance host/community
• Contact with the target population
• Susceptible, able to replicate & excrete the pathogen = Host competence (excep. mechanic transmission)
BBridge Host Caron et al. 2015
MAINTENANCE - BRIDGE - TARGET SYSTEMS
Adapted from Haydon et al. 2002 Caron et al. 2015
AVIAN INFLUENZA VIRUSES AT WILD/DOMESTIC BIRD INTERFACE
IN AFRICA
AIV IN WILD BIRDS IN AFRICA
• Target population = domestic poultry
• Anseriforms (duck sp.) are known to be the maintenance host for LPAI worldwide
• In Africa, since 2006, results indicate similar role of ducks in LPAI epidemiology (Caron et al. 2011, Cumming et al. 2011, Gaidet et al. 2012, etc.)
HOW TO IDENTIFY BRIDGE HOST FOR AIV?
BBridge Host
Contact with ducks
Contact with poultry
AIV competence
TOOLS AT DISPOSALHost competence Host contacts Resources
Method Receptivity Replication Excretion Contact/Maintenanc
Contact/Target
Experimental Infection
xxx xxx xxx xxx
Risk Analysis x x x
Serological investigation
x x x xx
Virological investigation
xx xx xx xx xx
Telemetry study
xxx xxx xxx
Bird ringing and
xx x x
Bird counts xx xx x
Molecular epidemiology
xx xx xx xx xx xxx
Need a combination of techniques (Epidemiology + Ecology)
Caron et al. 2015
STUDY SITE
Wild bird community
MODEL
Intensive Poultry Backyard poultry
Ostrich farms Waterfowl community
Bird count
B
B
Caron et al. 2009, 2010
SHARED COMMUNITY OF WILD BIRDS BETWEEN COMPARTMENTS
Caron et al. 2014
INTERACTIONS WERE DOMINATED BY A FEW SPECIES
Caron et al. 2014
SUSCEPTIBILITY OF POTENTIAL BRIDGE SPECIES IN LITERATURE
Red-billed quelea (Quelea quelea)
• potential H5N1 spreader (Breithaupt et al. 2010)
• positive for LPAI in Mali (Cappelle, pers. obs.)
Barn swallow (Hirunda rustica)
• positive for LPAI in Europe (Grosenova et al. 2008; Mizakova et al. 2008)
• positive for LPAI in Zambia and Zimbabwe (Caron, pers. obs.)
Cattle egret (Bulbucus ibis)
• positive for LPAI in Northern America (Squires et al. 2008)
SAMPLING OF POTENTIAL BRIDGE HOSTS
N=# AIV# NCD# WNV#Red$billed(Quelea(
206( 2(0.97%)( 15(7.28%)( 6((2.91%)(
Barn(swallow(
133( 4(3.00%)( 8(6.02%)( 2(1.50%)(
CaAle(egret(
166( 0(0.00%)( 1(0.60%)( 0(0.00%)(
Bridge Hosts For AIV
B
B
Caron et al. 2014
Adapted protocol
Timely for interactions
IMPLICATIONS FOR AIV MANAGEMENT
Control contacts between bridge and target populations
• Control on-farm wild bird attractors (food/water)
• Control building roosting site (swallow)
• Efficient quelea control (pest)
Intervention targeted at specific species & during period when interactions are high
CONCLUSION
Disease ecology at Wildlife/Livestock interface
Combined ecology and epidemiology sciences
Approach using « Epidemiological Functions »
• Maintenance function (maintenance host)
• Transmission function (maintenance, bridge hosts)
Caron et al. 2012, 2014, 2015
E.G. EBOLA
Bats Human
Bat sp. 1
Bat sp. 2 Bat
sp. 3Bushmeat Hunting
Others???
Antelopes
Pigs
Dogs
Apes
??????
???
???
de Garine-Wichatitsky et al. in prep
E.G. FMD
Buffalo CattleDirect contacts Fences?
Impala
Kudu
???
???
Goats
de Garine-Wichatitsky et al. in prep
TAKE HOME MESSAGE
Functional approaches applied to disease transmission
They need integrating more Ecology & Epidemiology
e.g. EID: Pathogen hunting is important —> but working on transmission dynamics is as much important
WHAT’S NEXT? ON-GOING?
Other epidemiological functions (amplification, dilution)? (de Garine-Wichatitsky et al. in prep)
Include the animal/human interface (social science, economic aspects) (de Garine-Wichatitsky et al. 2012)
How to predict infectious transmission (EID)?
• Community of shared pathogens
• Rodent-borne diseases-based networks at rodent/human interfaces: transmission ecology in heterogeneous landscapes in Southeast Asia (Bordes et al. in prep)
• Patho-indicator of transmission (e.g. Commensal Escherichia coli populations)
• Escherichia coli populations sharing and antibiotic resistance gradient at a buffalo/cattle interface in southern Africa (Mercat et al. Revision, AEM)
REFERENCES- Caron, A., Cappelle, J., Cumming, G. S., de Garine-‐Wichatitsky, M., Gaidet, N. Bridge host, a missing link in disease ecology in multi-‐host systems. Veterinary Research, in press. - Caron, A., de Garine-‐Wichatitsky, M., Roger, F. 2014. Bovine tuberculosis: a double-‐edged issue at the human/livestock/wildlife interface in Africa. Empres-‐animal health 360 44(2): 10-‐13. -‐ Caron, A., Grosbois, V., Etter, E., Gaidet, N., de Garine-‐Wichatitsky, M. 2014. Bridge hosts for Avian In>luenza viruses at the wildlife/domestic interface: an ecoepidemiological framework implemented in southern Africa. Preventive Veterinary Medicine, 117 (590-‐600). -‐ Miguel, E., Boulinier, T., de Garine-‐Wichatitsky, M., Caron, A., Fritz, H., Grosbois, V. 2014. Characterising African tick communities at a wild-‐domestic interface using repeated sampling protocols and models. Acta Tropica, in press. -‐ Jori, F., Caron, A., Thompson, P. N., Dwarka, R., Foggin, C., de garine-‐Wichatitsky, M., Hofmeyr, M., Van Heerden, J. and Heath, L. 2014. Characteristics of Foot-‐and-‐Mouth disease viral strains circulating at the wildlife/livestock interface of the Great Limpopo Transforntier Area. Transboundary and Emerging Diseases, in press. - Kock, R., Kock, M., de Garine-‐Wichatitsky, M., Chardonnet, P., Caron, A. 2014. Livestock and buffalo (Syncerus caffer) interfaces in Africa: ecology of disease transmission and implications for conservation and development. In: Ecology, Evollution and Behaviour of wild Cattle. Implications for Conservation. Melletti, M. & Burton, J. (Editors). Cambridge University Press, Chapter 26. -‐ Miguel, E., V. Grosbois, A. Caron, D. Cornelis, T. Boulinier, H. Fritz, C. Foggin, P. Makaya, P. T. Tshabalala, and M. de Garine-‐Wichatitksy. 2013. Contact rates with buffalo explain foot-‐and mouth disease dynamics in cattle at the periphery of Transfrontier Conservation Areas in Southern Africa. Ecosphere, 4(4): art51. -‐ de Garine-‐Wichatitksy, M., A. Caron, R. Kock, R. Tschopp, M. Munyeme, M. Hofmeyr, and A. Michel. 2013. A review on bovine tuberculosis at the wildlife/livestock/human interface in sub-‐Saharan Africa. Epidemiology and Infections, 141: 1342-‐1356. -‐ Caron, A., Miguel, E., Gomo, C., Makaya, P., Pfukenyi, D., Hove, T., Foggin, C., de Garine-‐Wichatitsky, M. 2013. Relationship between burden of infection in ungulate populations and wildlife/livestock interfaces. Epidemiology & Infections, 141(7): 1522-‐1535. - de Garine-‐Wichatitsky, M., Miguel, E., Mukamuri, B., de Garine, I., Ancelcius, J., Pfukenyi, D., Caron. A. 2012. Coexisting with wildlife in Transfrontier Conservation Areas in Zimbabwe: cattle owners' awareness of disease risks and perception of the role played by wildlife. Comparative Imunology, Microbiology and Infectious Diseases, 36: 321-‐332. -‐ Caron, A., de Garine-‐Wichatitsky, M., Ndlovu, M., Cumming, G. S. 2012. Linking avian communities and avian in>luenza ecology in southern Africa using epidemiological functional groups. Veterinary Research, 43:73. -‐ Mundava, J., Caron, A., Gaidet, N., Couto, F. M., Couto, J. T., de Garine-‐Wichatitsky, M., Mundy, P. 2012. Factors in>luencing long-‐term and seasonal waterbird abundance and composition at 2 two adjacent lakes in Zimbabwe. Ostrich, 83(2): 69-‐77. -‐ Caron, A., de Garine-‐Wichatitsky, M., Morand, S. 2012. Using the community of pathogens to infer inter-‐speci>ic host epidemiological interactions at the wildlife/domestic interface. “New Frontiers of Molecular Epidemiology of Infectious Diseases”. Morand, S., Beaudeau F., Cabaret J. (Eds).,Part 5, 311-‐332. -‐ Gaidet, N., Caron, A. Cappelle, J., Balança, G., Mundava, J., Fofana, B., Hammoumi, S., Gil, P., Cattoli, G., Abolnik, C., Fereidouni, S.R., ould Elmamy, B., Hagemeijer, W., Mondain-‐Monval, J.Y., Tran, A., Grosbois, V., Cumming, G.S., Triplet, P., Newman, S.H., Dodman, T. 2012. Ecological drivers of aviain in>luenza virus infection in wildfowl in Afrotropical regions. Proc Roy Soc B, 279 (1731): 1131-‐1141. -‐ Cumming, G. S., Caron, A., Abolnik,C., Catolli, G., L.W. Bruinzeel, C.E. Burger, K. Cecchettin, N. Chiweshe, B.Mochotlhoane, G.L. Mutumi, M. Ndlovu. 2011. The ecology of In>luenza A viruses in wildbirds in southern Africa. EcoHealth 8(1): 4-‐13 -‐ Caron, A., Abolnik, C., Mundava, J., Gaidet, N., Burger, C.E.,Mochotlhoane, B., Bruinzeel, L., Ngoni, C., de Garine-‐Wichatitsky, M., Cumming, G. S. 2011. Persistence of Low Pathogenic Avian In>luenzaVirus in Waterfowl in an African Ecosystem. EcoHealth 8(1): 109-‐115 -‐ Caron, A., de Garine-‐Wichatitsky, M., Gaidet, N., Chiweshe, N., Cumming, G.S. 2010. Estimating dynamic risk factors for pathogen transmission using community-‐level bird census data at the wildlife/domestic interface. Ecology& Society, 15(3):25 -‐ de Garine-‐Wichatitsky, M., Caron, A., Gomo, C., Foggin, C.,Dutlow, K., Lane, E., Le Bel, S., Hofmeyr, M., Hlokwe, T. and Michel, A. 2010. Bovine tuberculosis in Buffaloes, Southern Africa. Emerg Inf Dis, 16 (5) 884-‐885. -‐ Caron, A., Gaidet N., de Garine-‐Wichatitsky, M., Morand, S., Cameron, E. 2009. Evolutionary Biology, Community Ecology and Avian In>luenza Research.Infections, Genetics & Evolution, 9: 298-‐303.
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IMPLICATIONS FOR AIV IN WILD BIRDS
More than just Anseriformes & Charadriiformes in AIV ecology
Other orders & species play an important role
• depending on ecosystem
• species ecology
Redefine wild bird surveillance for AIV
• Not blind sampling
• More eco-epidemiological approaches
Caron et al. 2012
Caron et al. in prep
