Managing pathogen spillover at the wildlife-livestock interface

Kezia and Paul

with input from Ryan Miller, Steve Sweeney, Tom Besser, Frances Cassirer, and USDA Wildlife-Livestock Spillover workshop participants

Task

Develop a general quantitative model to describe pathogen spillover risk at the wildlife-livestock interface

Reservoir

Recipient

Index case

Onward transmission

Reservoir

Recipient

Index case

Onward transmission

(...or livestock into wildlife)

Potentially relevant factors

Between-host processes in reservoir

Interspecific contact processes

Pathogen establishment processes

Pulliam 2008; Lloyd-Smith et al. 2009; Plowright et al. 2015; Plowright et al. 2017

Reduce to a general-yet-useful framework that "works" for management

 

Between-host processes in recipient

Management

Between-host processes in reservoir

Interspecific contact processes

Pathogen establishment processes

Between-host processes in recipient

Test-cull

Vaccination

Movement

restrictions

Attractant management

Fencing

Biosecurity

Phytosanitary controls

Density reductions

Density reductions

Vaccination

Treatment

Increased "resilience"

e.g., nutrition, antibiotics

Vaccination

Movement restrictions

Zoning

Depopulation/

Stamping out

 

Management

Test-cull

Vaccination

Movement

restrictions

Attractant management

Fencing

Biosecurity

Phytosanitary controls

Density reductions

Density reductions

Vaccination

Treatment

Increased "resilience"

e.g., nutrition, antibiotics

Vaccination

Movement restrictions

Zoning

Depopulation/

Stamping out

 

Pathogen movement process in reservoir

Epidemic growth rate in recipient

Test-cull

Movement restrictions in reservoir

Attractant management

Density reductions

Treatment

Zoning in recipient

Depopulation/Stamping out

 

Phytosanitary controls

Biosecurity

Vaccination

Pathogen movement process in reservoir

Epidemic growth rate in recipient

Movement restrictions in reservoir

Attractant management

Density reductions

Zoning in recipient

Depopulation/Stamping out

 

Phytosanitary controls

Biosecurity

Vaccination

Pathogen movement rate in reservoir

Epidemic growth rate in recipient

Test/Cull reservoir

Treatment

Basic Premise

Spatiotemporal distribution of spillover risk hinges on:

  • Movement of pathogen in reservoir host
  • Epidemic growth rate (in either host spp.??)

Spatiotemporal distribution of spillover risk determines optimal management strategy

Specific hypotheses

  • Reservoir movement limited => regionalize/stamp-out
  • Low growth rate => manage reservoir prevalence
  • Reservoir movement high and epidemic growth rate high => biosecurity/vaccination on recipient

Less certainty in space

Less time to act

Distance host could move while infected

Epidemic growth rate

Reducing reservoir prevalence or density

Halting onward transmission

Reducing interspecific contact through  biosecurity on recipient

(Now in graphical form)

Three emergent research questions

1.  Where do actual systems fit on those axes?

3. Does the cost-benefit framework hold up?

2. What do management actions cost?

Where do actual systems fit?

Wildlife-Livestock systems

African swine fever

Canine distemper virus

Rinderpest

Tularemia

Rabies

Phocine distemper virus

Brucellosis

M.ovi

Avian influenza

Classical swine fever

Salmonella

Foot and Mouth disease

Echinococcus

Paratuberculosis

Scrapie

Anthrax

bTB

Q fever

West Nile virus

Pseudorabies virus

Bluetongue virus

Human systems

Measles

HIV

SARS

Polio

Rubella

Smallpox

Pertussis

Diphtheria

Chickenpox

Pathogen type

dsRNA viruses

Bluetongue

 

dsDNA viruses

African swine fever

Chickenpox

Smallpox

 

ssRNA viruses

Rinderpest

Rabies

Phocine, Canine distempers

Avian influenza

Classical swine fever

Food and Mouth disease

West Nile virus

Measles

SARS

Polio

Rubella

 

Tapeworm

Echinococcus

Bacteria

Tularemia

Q fever

Brucellosis

Movi

Salmonella

Movi

Anthrax

Paratuberculosis

Pertussis

Diphtheria

bTB

 

Pathogen type

Mode of transmission

Exudate discharge

Classical swine fever

Pseudorabies virus

Canine distemper virus

 

Saliva

Diphtheria

 

Bites

Rabies

 

Aerosolized

Foot and Mouth disease

Q fever

 

Respiratory droplets

Chickenpox

Rinderpest

Phocine distemper

M.ovi

Measles

SARS

Rubella

Smallpox

Pertussis

 

Fecal-oral

Echinococcus

Avian influenza

Salmonella

Polio

 

Vectored

African swine fever

Tularemia

West Nile virus

Bluetongue

 

Environmental

Anthrax

Paratuberculosis

Scrapie

bTB

 

 

Pathogen Reservoir host Time to recovery/death (days) Home range size (or foray distance) per Infectious period Potential movement during I
Avian influenza mallards 7  1400 km in 27 days median during fall migration (Krementz et al. JoFishWildlifeManage 2012) 360 km
Rabies raccoons ~ 35  25-190 ha annually (Prange et al. 2004 JMammal) (day-range 1.14 km, Carbone) 1-2 km
Brucellosis elk 730 13468 ha (Yellowstone over summer; Anderson 2005 Landscape Ecol). Carbone (2005) has "Cervus elaphus" day-range at 3.4 km (100 km?)
BHS pneumonia (bighorn?) sheep 20  25 km foray dist (O'Brien 2014 WildSocBull) 25 km
bTB white-tailed deer 730 1.34 km^2 for Females (Walter 2009); 77-202 ha (Campa 2011 WildSocBull) 15 km
Bluetongue (Culicoides spp.)  20.6 150 km
ASF warthogs 20-40 

Movement potential while infected

US commodity densities

(blue = low; orange = high)

Spatial structure varies dramatically across domestic livestock as well.

What does management cost?

Costs are relatively consistent across systems

Fencing -- IA State fencing cost document

Diagnostic costs for test-cull from Ames national diagnostic lab

Indemnity costs (e.g., what USDA pays to compensate for killing a livestock animal) published

Vaccine costs relatively consistent IF vaccine is developed and primary cost is vaccine, not delivery (several reviews)

Does the framework hold up?

Reservoir movement and disease

Interspecific contact & spillover

Recipient movement and disease

Parameters:

     Epidemic growth rate

     Contact structure

Natural disease process

Management experiments

t = 1

X

(\tau)
(τ)(\tau)
\tau = 1
τ=1\tau = 1

Deterministic disease updates

t = 1

t = 2

Hosts move according to kernel

Mover's infection status depends on prevalence

Stochastic movement updates

(\tau)
(τ)(\tau)
(\tau)
(τ)(\tau)
\tau = 2
τ=2\tau = 2
\tau = 1
τ=1\tau = 1

t = 2

Deterministic disease updates

Parameter space

Ro

Tail weight of dispersal kernel

(recovery rate fixed, so Ro determines epidemic growth rate)

Outputs

1) Number of reservoir patches infected

2) Number of recipient patches infected

3) Total recipients infected over whole simulation

Tail weight decreases from right to left

Beta decreases from bottom to top

Colors ramp according to first day cell became infected

Spillover

Random subset of patches chosen to harbor "recipient hosts"

Recipients get infected following random contacts with infected LOCAL reservoir hosts

Recipient map

Reservoir map

Recipient map

Management

Vaccination:

Depopulation:

Test-cull:

Biosecurity:

Adjust recipient SIR state-space so that R goes up, and S goes down

Reset recipient patch to S = 1, I = 0, R = 0

If prevalence exceeds some threshold...

Adjust reservoir SIR state-space so that R goes up, and S goes down

Decrease interspecific contact rates at designated patches

Apply management up to threshold "investment", then stop managing

Simulation structure

Grid the two parameters over log-space

Run 5 simulations with each management action at each parameter combination (total of 25 sims / param set)

Record median and range of outputs for each parameter set/management action

Record median and range of outputs for each parameter set/management action

Specify management $$ and livestock premise size

Using medians/ranges, determine which management action is "best" at each parameter combination

Increasingly aggregated

 

 

Increasingly aggregated

 

 

Transmission coefficient

(prop. to epidemic growth rate)

Transmission coefficient

(prop. to epidemic growth rate)

Three emergent research questions

1.  Where do actual systems fit on those axes?

3. Does the cost-benefit framework hold up?

2. What do management actions cost?

Can roughly be described with commonly-used tools

??? So far, so good...!

Less certainty in space

Less time to act

Distance host could move while infected

Reducing reservoir prevalence or density

Halting onward transmission

Reducing interspecific contact through  biosecurity on recipient

Success??

Epidemic growth rate

Is this useful?

How far do I push the empirical side?

[ditto] the economic weeds?

...Did we know this already?

What does management cost?

Pathogen Median domestic operation size Median operations per producing county Proportion of counties with production Vaccine cost Treatment/Post-exposure prophylaxis cost Diagnostic cost Fencing cost Indemnity cost per animal
AI
bTB
Brucella Abortus
Rabies
EHD/ Bluetongue
Newcastle
M.ovi

Costs are relatively consistent across systems

Does the cost-benefit framework hold up?

County-scale (30mi x 30mi cells; 100x100 cell grid)

Reservoir and recipient populations

  • AcReservoir has constant density across all cells
  • Recipients also occur in a random subset of cells
    • e.g., counties with lots of poultry/beef/sheep operations

Disease dynamics (deterministic)

  • SIR disease process
    • recovery rate fixed to constant
    • transmission rate varies to generate different epidemic growth rates

Movements (stochastic)

  • Reservoir: Movement probabilities function of distance between cells
    • User-fixed sill beyond which no movements occur
    • P(Mover is infected) proportional to current cell prevalence
    • All infected movers cause determinist disease process to begin in their new cell.
  • Recipient: No movements

Spillover

  • Interspecific contacts occur between reservoir and recipients in same cell
  • P(Infectious contact) proportional to current reservoir prevalence in the cell

Management

  • Alter disease dynamics, interspecific contact rate, or P(transmission | contact)
  • Management actions applied under a user-specified budget
  • Only one form of management can be taken.

How to categorize systems?

- Pathogen type

- Mode of transmission (vectored, environmental, direct??)

- Host ecology (... but which host, wildlife or livestock?)

- Available tools (e.g., treatment, vaccination, diagnostics)

- Rate or structure of spread (e.g., travelling waves?)

\text{Epidemic growth rate = }\beta - \gamma
Epidemic growth rate = β−γ\text{Epidemic growth rate = }\beta - \gamma
\beta = R_{0}\times \frac{1}{\text{Time to recovery}}
β=R0×1Time to recovery\beta = R_{0}\times \frac{1}{\text{Time to recovery}}
Pathogen R-naught Time to recovery/death beta beta - gamma
Avian influenza 2.24  7 days  (1/7 = .14) .32 (calculated) .18
Rabies 2  ~ 35 days (5 weeks; e.g. Tinline 2002 PVM) (1/35 = 0.028) 0.18 in foxes (refs in Suppo et al 2000 PhilTrans) .152
Brucellosis ​1.46  2 years (1/730 = .0014) .002 for bison (FD; Dobson & Meagher) .0006
BHS pneumonia ~1.6 20 days?? (1/20 = .05) 0.08 .03
 
bTB 2 years?? based on most animals infected 1.5-2 yrs, survive 4-5 yrs? (1/730 = .0014) 0.043/12 = 0.0036 (from Cosgrove & Ramsey models... it's on a monthly scale) 0.002
Bluetongue temperture-dependent; ranges from <1 to 18  20.6 (for cattle; 1/20.6 = .048) in Graesbol 2012 Sci Reps; 8 days for sheep Luedke 1969 cited in Hartemink 2009) .864 .816
Newcastle disease virus
ASF ~1.58 20-40 days (Ferriera 2013 Vet Micro) (1/30 = .033)

1. Extract empirical estimates: Epidemic growth rate

Less certainty in space

Less time to act

Reducing reservoir prevalence

Halting onward transmission

Reducing interspecific contact

2. Identify costs associated with management categories

Management category Action Examples
Halting onward transmission Depopulation AI
Post-exposure treatment Rabies
Recipient movement controls Movi (e.g., translocations), brucellosis
Reducing reservoir prevalence Test/cull Brucellosis (WY); bTB
Reservoir vaccination Brucellosis; bTB
Reducing interspecific contact and susceptibility in recipient Fencing Brucellosis, bTB
Phytosanitary controls AI, EHD
Recipient vaccination AI, brucellosis, bTB, rabies
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