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Bioeconomic management of invasive vector-borne diseases

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Abstract

Invasive insects, arthropods, and other invertebrates are of concern due to the role some play in introducing and transmitting pathogens via a pathogen–vector relationship. Indeed, vector-borne diseases represent a significant portion of emerging diseases. We compare and contrast three strategic approaches to managing a vector-borne pathogen: conventional strategies based on disease ecology without regard to economic tradeoffs and cost-effective strategies based on a bioeconomic framework. Conventional strategies entail managing the vector population below a threshold value based on R 0—the basic reproductive ratio of the pathogen, which measures a pathogen’s ability to invade uninfected systems. This does not account for post-infection dynamics, nor does it balance ecological and economic tradeoffs. Thresholds take on a more profound role under a bioeconomic paradigm: rather than unilaterally determining vector control choices, thresholds inform control choices and are influenced by them. Simulation results show cost-effective strategies can lower overall program costs and may be less sensitive to parameter estimation.

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Notes

  1. A reviewer points out that some may regard management of a post-infected scenario as pest management, but the process of biological invasion involves more than species introduction (Williamson and Fitter 1996). Focusing on post-introduction processes (i.e., establishment and spread) can help to prevent or slow further invasion into surrounding areas.

  2. Implicitly, we have assumed vaccination is not an option, which is often the case for emerging diseases. While the SI framework is a special case of more complex models involving recovered, immune, or exposed population compartments (e.g., SIS, SIR or SEIR models), the basic insights developed for our SI model—that the current state of infection matters and focusing on tradeoffs as opposed to eradication leads to qualitatively different results—are generally applicable to these more complex models. Also note that the vector may also transmit pathogen to sink hosts, causing damages, but these do not affect the basic disease dynamics between the vector and host populations that we model here (Chaves and Hernandez 2004).

  3. See Song et al. (2002) for an approach to combining infection dynamics on multiple time scales.

  4. If there are capacity constraints that only permit a y i (0) < y i *(0), then subsequent vector control pulses may be optimal within the interval t ∈ (0, τ]. We also note that for this problem if τ is large enough, then it is not optimal to engage in any management resulting in W = 0.

  5. Rising marginal costs are also a factor in determining the initial pulse harvest. The costs associated with a pulse harvest are cln(N i /[N i  − y i ]) (see Clark 2005). This implies that costs increase as a larger proportion of the vector population is initially harvested.

  6. For a sufficiently large τ it will be important to incorporate discounting and net natural growth within the host population, neither of which are currently included in our model. We hypothesize that including these factors will result in a time-varying positive level of vector control.

  7. Increases in α w effectively result in selective culling of infected host animals. As indicated in footnote 4, selective culling of infected hosts can in some circumstances be detrimental because this increases the probability that an infected vector randomly bites a susceptible (as opposed to infected) host.

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Acknowledgments

The authors gratefully acknowledge funding provided by the Economic Research Service-USDA cooperative agreement number 58-7000-6-0084 through ERS’ Program of Research on the Economics of Invasive Species Management (PREISM), and by NRI, USDA, CSREES, grant #2006-55204-17459. This work was conducted as part of the SPIDER working group at the National Institute for Mathematical and Biological Synthesis (NIMBioS), sponsored by the National Science Foundation and the U.S. Department of Agriculture through NSF Award #EF-0932858, with additional support from the University of Tennessee, Knoxville. The views expressed here are the authors and should not be attributed to ERS, USDA, or NIMBioS.

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Appendix

Appendix

(A) Derivation of condition (7)

Upon imposing the requirement that h i  < 1, condition (6) indicates that

$$ 1 > \beta_{wi} \theta_{w} /\theta_{i} - (\beta_{wi} \theta_{w} + \delta_{i} ) = \beta_{wi} \theta_{w} (1/\theta_{i} - 1) - \delta_{i} . $$
(A1)

Condition (A1) can be re-written as

$$ \delta_{i} + 1 > \beta_{wi} \theta_{w} (1/\theta_{i} - 1) = \beta_{wi} \theta_{w} (N_{i} /I_{i} - I_{i} /I_{i} ) = \beta_{wi} \theta_{w} (S_{i} /I_{i} ). $$
(A2)

Write \( \theta_{w} = I_{w} /N_{w} \) and solve for S i :

$$ S_{i} < \left[ {\delta_{i} + 1} \right]{\frac{{I_{i} N_{w} }}{{\beta_{wi} I_{w} }}} = \left[ {\delta_{i} + 1} \right]{\frac{{\alpha_{w} K_{w} }}{{\beta_{iw} \beta_{wi} }}}{\frac{{I_{i} }}{{I_{w} }}}{\frac{{N_{w} }}{{K_{w} }}}{\frac{{\beta_{iw} }}{{\alpha_{w} }}}, $$
(A3)

where the last equality simply comes from multiplying both the numerator and the denominator by \( \alpha_{w} K_{w} \beta_{iw} \). Upon applying the distributive property, condition (A3) becomes

$$ S_{i} < \left[ {{\frac{{\alpha_{w} \delta_{i} K_{w} }}{{\beta_{iw} \beta_{wi} }}} + {\frac{{\alpha_{w} K_{w} }}{{\beta_{iw} \beta_{wi} }}}} \right]{\frac{{I_{i} }}{{I_{w} }}}{\frac{{N_{w} }}{{K_{w} }}}{\frac{{\beta_{iw} }}{{\alpha_{w} }}} = \left[ {N_{Ti} + {\frac{{\alpha_{w} K_{w} }}{{\beta_{iw} \beta_{wi} }}}} \right]{\frac{{I_{i} }}{{I_{w} }}}{\frac{{N_{w} }}{{K_{w} }}}{\frac{{\beta_{iw} }}{{\alpha_{w} }}}, $$
(A4)

which is condition (7).

(B) Optimal vector management

Problem (12) can be formulated as a linear control problem (i.e., the problem is linear in the control variable y i ). The Hamiltonian for the problem is:

$$ H = - {\frac{{cy_{i}^{{}} }}{{N_{i} }}} + \lambda_{w} \dot{S}_{w} + \mu_{w} \dot{I}_{w} + \lambda_{i} \dot{S}_{i} + \mu_{i} \dot{I}_{i} , $$
(B1)

where \( \lambda_{j} \) is the co-state variable associated with the susceptible stock of population j, and \( \mu_{j} \) is the co-state variable associated with the infected stock of population j (j = w,i).The marginal value of y i on the Hamiltonian is:

$$ {\frac{\partial H}{{\partial y_{i} }}} = - {\frac{c}{{N_{i} }}} - \lambda_{i} {\frac{{S_{i} }}{{N_{i} }}} - \mu_{i} {\frac{{I_{i} }}{{N_{i} }}} $$
(B2)

The marginal value in (B2) vanishes along a singular path. When the value is positive (negative), then h i should be set at its maximum (minimum) value. Generally, the system will not be on the singular path initially, which means an extremal control must be used to move the system as quickly as possible to the singular path (if one exists) (Clark 2005). As there is no upper bound on y i , harvests can only occur at a maximum rate for an instant. Harvests can persist at y i  = 0 or at the singular level for a longer time. Hence, except for an initial jump, we have

$$ y_{i} = \dot{y}_{i} = 0,\,{\text{or}}\quad \partial H/\partial y_{i} = 0. $$
(B3)

The remaining necessary conditions for problem (12) are:

$$ \dot{\lambda }_{w} = - {\frac{\partial H}{{\partial S_{w} }}} $$
(B4)
$$ \dot{\mu }_{w} = - {\frac{\partial H}{{\partial I_{w} }}} $$
(B5)
$$ \dot{\lambda }_{i} = - {\frac{\partial H}{{\partial S_{i} }}} $$
(B6)
$$ \dot{\mu }_{i} = - {\frac{\partial H}{{\partial I_{i} }}} $$
(B7)

The transversality conditions are:

$$ \lambda_{w} (\tau ) = {\frac{\partial V}{{\partial S_{w} }}} > 0 $$
(B8)
$$ \mu_{w} (\tau ) = 0 $$
(B9)
$$ \lambda_{i} (\tau ) = 0 $$
(B10)
$$ \mu_{i} (\tau ) = 0 $$
(B11)

Conditions (B10) and (B11), along with (B2), indicates that h i (τ) = 0. Taking the time derivative of the Hamiltonian yields:

$$ \begin{aligned} {\frac{\partial H}{\partial t}} & = {\frac{\partial H}{{\partial y_{i} }}}\dot{y}_{i} + \sum\limits_{j = w,i} {\left[ {{\frac{\partial H}{{\partial S_{j} }}}\dot{S}_{j} + {\frac{\partial H}{{\partial I_{j} }}}\dot{I}_{j} + {\frac{\partial H}{{\partial \lambda_{j} }}}\dot{\lambda }_{j} + {\frac{\partial H}{{\partial \mu_{j} }}}\dot{\mu }_{j} } \right]} \\ {\frac{\partial H}{\partial t}} & = 0 + \sum\limits_{j = w,i} {\left[ {{\frac{\partial H}{{\partial S_{j} }}}\dot{S}_{j} + {\frac{\partial H}{{\partial I_{j} }}}\dot{I}_{j} + \dot{S}_{j} \dot{\lambda }_{j} + \dot{I}_{j} \dot{\mu }_{j} } \right]} \\ {\frac{\partial H}{\partial t}} & = 0 + \sum\limits_{j = w,i} {\left[ {{\frac{\partial H}{{\partial S_{j} }}}\dot{S}_{j} + {\frac{\partial H}{{\partial I_{j} }}}\dot{I}_{j} + \dot{S}_{j} \left( { - {\frac{\partial H}{{\partial S_{j} }}}} \right) + \dot{I}_{j} \left( { - {\frac{\partial H}{{\partial I_{j} }}}} \right)} \right]} = 0. \\ \end{aligned} $$
(B12)

The second row of (B12) comes from condition (B3), while the third row comes from conditions (B4)–(B11). Hence, H is constant after possibly an initial pulse harvest. Define this constant value of H by χ, i.e., H = χ. Using the results H = χ and h i (τ) = 0, along with the transversality conditions (B8)–(B11), we have

$$ H(\tau ) = 0 + \lambda_{w} (\tau )\dot{S}_{w} (\tau ) = - {\frac{\partial V}{{\partial S_{w} (\tau )}}}\beta_{iw} I_{i} (\tau ){\frac{{S_{w} (\tau )}}{{N_{w} (\tau )}}} = \chi < 0, $$
(B13)

which means H(t) < 0 for all t ∈ [0, τ).

As H is a measure of economic welfare, the result H(τ) < 0 means that extending the time horizon to τ reduces welfare. It would be optimal to diminish the time horizon to some value \( \tau^{\prime} < \tau \), such that \( H(\tau^{\prime}) = 0 \), as setting \( H(\tau^{\prime}) = 0 \) means there is no value to extending the time horizon any further (Clark 2005). However, this is not possible since τ is biologically-determined and is therefore exogenously fixed. The implication is that it is optimal to take all actions as soon as possible: an impulse control at time t = 0. The intuition is as follows. First, there is no incentive to delay management because problem (12) is a linear control problem with no discounting. If discounting occurred at a very high rate, then future costs (and benefits) would be worth less and so one would want to wait to invest in vector controls. With no discounting, costs today and in the future are valued equally, so there is no penalty from investing early. But there is a penalty to investing later, as the only stock of concern, S w , can only decrease when the disease problem gets worse. So it is optimal for all vector reduction to take place immediately. The cost associated with an impulse control used for the initial cull is \( c\ln [N_{i0} /(N_{i0} - y_{i} (0))] \) (Clark 2005).To determine the optimal initial harvest, rewrite the problem as

$$ \begin{array}{*{20}c} {\mathop {\text{Max}}\limits_{{y_{i} (0)}} } & { - c\ln \left[ {{\frac{{N_{i0} }}{{N_{i0} - y_{i} (0)}}}} \right] + V(S_{w} (\tau ))} \\ \end{array} $$
(B14)

subject to the equations of motion and the initial conditions as before, except that now we have the following initial conditions for the vector populations: \( S_{i} (0^{ + } ) = S_{i0} (1 - y_{i} (0)/N_{i0} ) \) and \( I_{i} (0^{ + } ) = I_{i0} (1 - y_{i} (0)/N_{i0} ) \). The objective function in (B14) now does not depend on time, and the equations of motion no longer depend on human choices. We solve the equations of motion (1)–(4) as functions of the stock levels after the initial cull, and then rewrite problem (B14) as

$$ \begin{array}{*{20}c} {\mathop {\text{Max}}\limits_{{y_{i} (0)}} } & { - c\ln \left[ {{\frac{{N_{i0}^{{}} }}{{N_{i0}^{{}} - y_{i}^{{}} (0)}}}} \right] + V(S_{w} (\tau ,S_{w0} ,I_{w0} ,S_{i0} [1 - y_{i} (0)/N_{i0} ],I_{i0} [1 - y_{i} (0)/N_{i0} ]))} \\ \end{array} , $$
(B15)

or, more simply, as

$$ \begin{array}{*{20}c} {\mathop {\text{Max}}\limits_{{h_{i} (0)}} } & { - c\ln \left[ {{\frac{1}{{(1 - h_{i}^{{}} (0))}}}} \right] + V(S_{w} (\tau ,S_{w0} ,I_{w0} ,S_{i0} [1 - h_{i} (0)],I_{i0} [1 - h_{i} (0)]))} \\ \end{array} $$
(B16)

The optimality condition for this problem is:

$$ {\frac{c}{{(1 - h_{i}^{{}} (0))}}} = {\frac{{\partial V\left( {S_{w} \left( \tau \right)} \right)}}{{\partial S_{w} }}}\left[ { - {\frac{{\partial S_{w} }}{{\partial S_{i} (0^{ + } )}}}S_{i0} - {\frac{{\partial S_{w} }}{{\partial I_{i} (0^{ + } )}}}I_{i0} } \right] $$
(B17)

The left hand side of (B17) is the marginal cost of vector controls. Marginal costs approach infinity as the harvest rate \( h_{i} (0) \) approaches unity; hence it is not optimal to eradicate the vector population assuming the marginal benefits of eradication are finite. The right hand side is the marginal net benefit of vector controls in time period 0. Society benefits from a larger value of \( S_{w} (\tau ) \). This value is increased at the margin as \( I_{i} (0^{ + } ) \) is reduced (i.e., \( - \partial S_{w} /\partial I_{i} (0^{ + } ) > 0 \)), and it may increase or decrease as \( S_{i} (0^{ + } ) \) is reduced (i.e., \( - \partial S_{w} /\partial S_{i} (0^{ + } )_{ < }^{ \ge } 0 \)).

It is worth noting that the impacts of the initial cull will depend on the time horizon τ. The smaller is τ, the larger the impact of a given initial cull on \( S_{w} (\tau ) \), as the vector population will have less time to rebound and infect the host population. In contrast, a larger τ gives infected vectors more time to rebound and infect hosts after the initial cull. Our numerical sensitivity analysis indicates that the less control is required when τ is small, as having only few controls can yield effective protection of the host population in this case while keeping costs low. The optimal level of vector controls is initially increasing in τ, as vector control efforts are initially substituted for reduced protection effectiveness as τ is increased. If τ is too large, however, the level of control is reduced in response to reduced effectiveness; more hosts become infected while society saves from reduced control costs.

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Fenichel, E.P., Horan, R.D. & Hickling, G.J. Bioeconomic management of invasive vector-borne diseases. Biol Invasions 12, 2877–2893 (2010). https://doi.org/10.1007/s10530-010-9734-7

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