Nonlinear Analysis: Real World Applications 53 (2020) 103081

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Nonlinear Analysis: Real World Applications

www.elsevier.com/locate/nonrwa

A global mathematical model of malaria transmission dynamics

with structured mosquito population and temperature variations
Bakary Traoré, Ousmane Koutou, Boureima Sangaré ∗
Laboratoire de Mathématiques Informatique et Applications (La.M.I.A), UFR Sciences et Techniques,
Université Nazi BONI, 01 BP 1091 Bobo Dsso 01, Burkina Faso

article info abstract

Article history: In this paper, a mathematical model of malaria transmission which takes into
Received 16 August 2018 account the four distinct mosquito metamorphic stages is presented. The model
Received in revised form 15 December is formulated thanks to the coupling of two sub-models, namely the model of
2019 mosquito population and the model of malaria parasite transmission due to the
Accepted 16 December 2019 interaction between mosquitoes and humans. Moreover, considering that climate
Available online xxxx
factors have a great impact on the mosquito life cycle and parasite survival
Keywords: in mosquitoes, we incorporate seasonality in the model by considering some
Malaria transmission parameters which are periodic functions. Through a rigorous analysis via theories
Basic reproduction ratio and methods of dynamical systems, we prove that the global behavior of the model
Vector reproduction ratio depends strongly on two biological insightful quantities : the vector reproduction
Mosquito population ratio Rv and the basic reproduction ratio R0 . Indeed, if Rv < 1, mosquitoes
Temperature variations
and malaria die out; if Rv > 1 and R0 < 1, the disease-free periodic equilibrium
Global stability
is globally attractive; and if Rv > 1 and R0 > 1 the disease remains persistent.
Finally, using the reported monthly mean temperature of Burkina Faso, we perform
some numerical simulations to illustrate our theoretical results.
© 2019 Elsevier Ltd. All rights reserved.

1. Introduction

Malaria is a protozoan infection of red blood cells caused in the human body by five species of the genus
Plasmodium: P. falciparum, P. vivax, P. ovale, P. malariae and P. knowlesi. The parasites are generally
transmitted to the human host through the bite of an infectious female anopheline mosquito. The incidence
of malaria is approximately 300–500 million clinical cases, resulting in 1 million deaths each year, where
children under 5 are the most chiefly burdened. Of all infectious diseases, malaria continues to be one
of the biggest contributors to the global disease burdens in terms of suffering and death and keeps on
receiving worldwide attention [1,2]. In order to stop the spread of infectious diseases, Epidemic Dynamics
formulates mathematical models, based on the occurrence and progressions of diseases and the surroundings,

∗ Corresponding author.
E-mail addresses: traore.baky@outlook.fr (B. Traoré), koutousman@gmail.com (O. Koutou), mazou1979@yahoo.fr
(B. Sangaré).

https://doi.org/10.1016/j.nonrwa.2019.103081
1468-1218/© 2019 Elsevier Ltd. All rights reserved.
2 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

to characterize the infectious agents, to describe the transmission processes, to analyze the origins of the
diseases and the factors involved in the transmissions, and to predict the prevalence of the diseases and
their patterns. Thus, malaria is one of the first human diseases to be subject to mathematical inquiry [3–5].
Indeed, the mathematical modeling of malaria transmission began in the 20th century (1911) with the
first model of Ronald Ross [6]. Ross proposed a mechanistic transmission model including the human host
and the mosquito. In the early 1950s, Georges Macdonald [7] improved Ross’s model and introduced an
expression for the basic reproduction number. Since then, there has been a great deal of work about using
mathematical models to study malaria transmission [8–10]. The standard technique for developing math-
ematical descriptions of mosquito-plasmodium interactions is to model the system as a set of autonomous
ordinary differential equations. This is an immensely powerful approach which has led to many insights into
the factors that affect malaria prevalence and control. However, in the mathematical modeling of malaria,
two major points are often less investigated by authors.
The first point is the stage structure of the vector. While mathematical models for malaria transmission
growth abound in literature, the mosquito population has been assumed to be homogeneous, or its stage
structure has been simplified in most of the models. In fact, immature mosquitoes are not considered because
they do not fly and do not bite humans, so they do not participate in the infection cycle. However, since
the abundance and dispersal of adult females are the key factors for the disease transmission, then the
dispersal pattern of adult females needs to be studied and modeled. Thus, in order to have more realistic
models of mosquitoes, we need to include the immature stages. In particular, the different stages have
different responses to the environment and the regulating factors to the population. Moreover, the immature
control is a hotly recommended strategy in the fight against malaria, so, it is important to incorporate the
immature stages in the malaria models. Several recent works taking into account the stage structure of
mosquito have proved that including immature mosquitoes in the model has a profound impact on malaria
transmission [11–13].
The second point is the climate effects on the dynamics of vector population. Since mosquito biology
and disease ecology are strongly linked to environmental conditions, then the impacts of mosquito-borne
diseases increase with warm temperatures and extreme precipitations. There is an evidence to show that
climate change and increasing precipitation of the earths temperature will hasten maturation of the parasite
in mosquitoes and so increase the biting frequency and create favorable conditions for mosquito breeding.
In fact, increasing temperature is known to decrease the length of time spent in each of the immature stages
and to decrease the lifespan of adults. In addition, the death rate of the immature stages is strongly linked to
temperature. Clearly, temperature exhibits complex and opposing effects on different parts of the mosquito
life and transmission cycles. As such, mathematical models are needed which explicitly incorporate the
impact of temperature on each life stage if we wish to understand its effect on seasonal abundance [14–17].
Most recently, Wang et al. [18] have formulated a malaria model which includes immature mosquitoes and
climate effects. However, their model is limited due to the following aspects: the immature mosquitoes have
been grouped in a single compartment, the extrinsic incubation period in mosquitoes and human hosts have
been neglected and the oviposition rate of juvenile mosquito is assumed to be linear. Further, in a study,
Okuneye et al. [16] developed and analyzed several complex weather-driven mechanistic models that extend
the prior studies by incorporating a broader array of biological, ecological and epidemiological factors such as
the dynamics of immature mosquitoes, host age-structure, host immunity-boosting due to repeated exposure
to malaria infection and the effects of climate on the vector dynamics. Moreover, through sensitivity analysis
of basic reproduction ratio, they found some important parameters which influence malaria transmission in
the periodic environments. Despite its virtues, the model of Okuneye et al. does not include all the immature
stages of mosquito life cycle.
Motivated by the works done in [13,16,19], we formulate a mosquito-stage-structured malaria model by
taking into account the four distinct metamorphic stages of mosquitoes which is subject to temperature
 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 3

Fig. 1. Different stages of biological evolution of mosquito population.

variations. Thus, the model is a non-autonomous system of ordinary differential equations constructed thanks
to the coupling of two subsystems. The first subsystem describes the dynamics of mosquito population and
the second subsystem describes the dynamics of malaria transmission. In order to get qualitative dynamics,
we use the Floquet theory of periodical system [20], the theory of uniform persistence, the limiting system
and the theory of chain transitive set [21,22] to analyze the global dynamics of the model.
This paper is organized as follows. In Section 2, we formulate the model. In Section 3, we introduce some
basic results and then analyze the global behavior of the models. In Section 4, we perform some numerical
analysis in order to support our main results. In addition, we examine the impact of some control measures
to detect the most optimal for the country. A brief discussion is given in Section 5 to conclude this work
and some possible future works are presented.

2. Model formulation

2.1. Formulation of vector population growth dynamics

The complete metamorphosis of the mosquito entails goes through four distinct stages of development,
namely egg, larva, pupa, and adult mosquito stages (see Fig. 1). The first three stages are aquatic and the
last stage is aerial [23,24]. Malaria is transmitted to human through an effective bite from an infectious
female mosquito. Female mosquitoes take blood meals to carry out their egg production, and such blood
meals are the link between the human and the mosquito.
Adult females lay hundreds of eggs per oviposition. The eggs are laid singly directly on the surface of the
water. Hatching of eggs into larvae may occur either within a few days or may be delayed for several months
depending on the period (temperature) of the year during which the eggs are laid. Anopheles mosquitoes
develop through four larval sizes before pupating. Larvae are very small in the first size and increase in
size until reaching 5–6 mm by the completion of the fourth size. They feed on organic matters and algae.
Moreover, it has been observed that larvae are cannibal because they are able to eat earlier-stage larvae under
certain conditions [18,25]. Thus, after the larvae have completed moulting, depending on the temperature,
they become pupae. A pupa is a resting, non-feeding development stage. This is the time the pupa changes
into an adult. When the development is complete, depending on the temperature the pupal skin splits and
the adult mosquito emerges [26,27]. Therefore at each stage, mosquitoes leave the population through natural
death rates which depend on the climatic profile. Hence, in the model we divided the mosquito population
into two groups: adult mosquitoes denoted by Nv and immature mosquitoes. Immature mosquitoes are
4 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

Fig. 2. Transfer diagram of mosquito population growth: the solid arrows represent the transition from one class to another and the
dashed arrow represents the eggs laying of female mosquitoes.

also divided into three compartments: E, L and P which represent the number of eggs, larvae and pupae
respectively [28]. From Fig. 2, we obtain the following system:

Ė(t) = b(t)Nv (t) − (α1 (t) + γ1 (t))E(t),

⎧
⎪
⎪
⎨ L̇(t) = α (t)E(t) − (α (t) + γ (t))L(t),
⎪
1 2 2
(1)
⎪
⎪
⎪ Ṗ (t) = α2 (t)L(t) − (α3 (t) + γ3 (t))P (t),
⎩
Ṅv (t) = α3 (t)P (t) − γ4 (t)Nv (t).

Mosquitoes develop various approaches to avoid predation. The oviposition habitat selection is made to make
sure that the mosquito larvae can develop relatively unmolested. These selected habitats are largely devoid
of predators, thus offering a relatively secure refuge for larval development [29–32]. Indeed, if there are too
many eggs in the oviposition habitat or too few nutrients and water resources, then females laid less eggs or
choose another site. It seems reasonable to express this biological phenomenon with a mathematical model
which explicitly incorporates the idea of limited carrying capacity resources. This model should take into
account the availability of nutrients and the occupation by eggs or larvae of the available breeder sites [11,25].
Thus, the temperature-dependent per capita oviposition rate is given by
( )
E(t)
b(t) 1 − Nv (t),
KE

the number of eggs that survive and become larvae is given by

( )
L(t)
α1 (t) 1 − E(t),
KL

and the number of larvae that survive and become pupae is given by
( )
P (t)
α2 (t) 1 − L(t).
KP

Finally, the number of mosquitoes that survive from recruitment into one class, to the next is given by
the following sequence of ordinary differential equations:
( )
E(t)
⎧
⎪
⎪ Ė(t) = b(t) 1 − Nv (t) − (α1 (t) + γ1 (t))E(t),
⎪
⎪
⎪
⎪ KE
( )
⎨ L̇(t) = α (t) 1 − L(t) E(t) − (α (t) + γ (t))L(t),
⎪
⎪
⎪
1 2 2
KL (2)
( )
P (t)
⎪
⎪
⎪ Ṗ (t) = α2 (t) 1 − K L(t) − (α3 (t) + γ3 (t))P (t),
⎪
⎪
⎪
⎪
⎪
⎪ P
⎩
Ṅv (t) = α3 (t)P (t) − γ4 (t)Nv (t).
 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 5

Table 1
Biological description of model (2) parameters.
Parameters Biological descriptions
KE Carrying capacity of eggs
KL Carrying capacity of larvae
KP Carrying capacity of pupae
α1 (t) Temperature-dependent transfer rate from eggs to larvae
α2 (t) Temperature-dependent the transfer rate from larvae to pupae
α3 (t) Temperature-dependent transfer rate from pupae to adult
b(t) Temperature-dependent eggs laying rate per female
γ1 (t) Temperature-dependent death rate of eggs
γ2 (t) Temperature-dependent death rate of larvae
γ3 (t) Temperature-dependent death rate of pupae
γ4 (t) Temperature-dependent death rate of adult mosquitoes

Table 2
Parameters of malaria transmission model.
Parameters Biological descriptions
β(t) Temperature-dependent biting rate of mosquitoes
Λh Constant recruitment for humans
dh Human natural death rate
α Transfer rate of humans from exposed class to infectious class
κ Disease-induced death rate for humans
rh Recovery rate of humans
γ Per capita rate of loss of immunity for humans
νv Transfer rate of mosquitoes from exposed class to infectious class
cvh Probability of transmission of infection from Ih to Sh
chv Probability of transmission of infection from Ih to Sv
c̄hv Probability of transmission of infection from Rh to Sv

2.2. Formulation of malaria transmission model

In the presence of the disease, the human population is divided into four epidemiological categories
representing the state variables: the susceptible class Sh , the exposed class Eh , the infectious class Ih and
the immune (asymptomatic, but slightly infectious humans) class Rh . Indeed, individuals in the class Rh
are immune in the sense that they do not suffer from serious illness and do not contract clinical malaria, but
they still have low levels of Plasmodium in their blood stream and can transmit the infection to susceptible
mosquitoes [17,33,34].
Similarly, adult mosquitoes are divided into three compartments Sv , Ev and Iv that represent the
susceptible mosquitoes, the exposed mosquitoes and the infectious mosquitoes, respectively. When males
and females finish to mate, females will take blood meals for their eggs development. Thus, if a susceptible
mosquito bites an infectious human, the mosquito becomes infected and it moves into the class Ev . Some
time after, it becomes infectious and enters into the class Iv . Hence, this infectious mosquito can infect a
susceptible human through another bite. Some time after infection, the human becomes infectious. If he is
continually exposed to mosquito bites, he becomes immune. However, he can lose this immunity and become
susceptible if the exposure to infection is stopped. Humans leave the total population through natural death
rate and malaria death rate; and mosquitoes leave the population through natural death.
At any time t ≥ 0, the total size of humans and adults mosquitoes is given respectively by

Nh (t) = Sh (t) + Eh (t) + Ih (t) + Rh (t), (3)

Nv (t) = Sv (t) + Ev (t) + Iv (t). (4)

The parameters of the model are given in Table 1 (see Table 2).
6 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

It is assumed throughout this paper that:

(H1): all vector population measures refer to densities of female mosquitoes,
(H2): the mosquitoes bite only humans,
(H3): there is no direct transmission (blood transfusion or from mother to baby) of malaria,
(H4): all the new recruits are susceptible,
(H5): there is no immigration of infectious humans.
Using the standard incidence, we define respectively the infection incidence from mosquitoes to humans,
kh (t) and from humans to mosquitoes, kv (t):

Iv (t)
kh (t) = cvh β(t)
Nh (t)

and
Ih (t) Rh (t)
kv (t) = chv β(t) + c̄hv β(t) .
Nh (t) Nh (t)

where β(t) is the average number of bites per mosquito per unit time t. According to the above assumptions,
our model of malaria transmission is represented by Fig. 3.

2.3. Main model

Following the above assumptions, the number of individuals which survive from recruitment into one class,
to the next (see Fig. 3) is defined by the following sequence of ordinary differential equations:
( )
E(t)
⎧
⎪
⎪ Ė(t) = b(t) 1 − Nv (t) − (α1 (t) + γ1 (t))E(t),
⎪
⎪
⎪
⎪ KE
( )
L(t)
⎪
⎪
L̇(t) = α1 (t) 1 − E(t) − (α2 (t) + γ2 (t))L(t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪ KL
( )
P (t)
⎪
⎪
Ṗ (t) = α2 (t) 1 − L(t) − (α3 (t) + γ3 (t))P (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪ KP
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪ Ṡv (t) = α3 (t)P (t) − (γ4 (t) + kv (t))Sv (t),
⎪
⎪
⎪
⎨
Ėv (t) = kv (t)Sv (t) − (νv + γ4 (t))Ev (t), (5)
⎪
⎪
⎪
I˙v (t) = νv Ev (t) − γ4 (t)Iv (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
Ṡh (t) = Λh + γRh (t) − (dh + kh (t))Sh (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
Ėh (t) = kh (t)Sh (t) − (dh + α)Eh (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
I˙h (t) = αEh (t) − (dh + κ + rh )Ih (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
Ṙh (t) = rh Ih (t) − (dh + γ)Rh (t).
⎩

Since,

Sv (t) = Nv (t) − Ev (t) − Iv (t), ∀t ≥ 0,

 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 7

Fig. 3. Transfer diagram of malaria transmission to humans: the black dashed arrows indicate the direction of the infection and the
solid arrows represent the transition from one class to another.

then, system (5) reads as follows:

( )
E(t)
⎧
⎪
⎪ Ė(t) = b(t) 1 − Nv (t) − (α1 (t) + γ1 (t))E(t),
⎪
⎪
⎪
⎪ KE
( )
L(t)
⎪
⎪
L̇(t) = α1 (t) 1 − E(t) − (α2 (t) + γ2 (t))L(t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪ KL
( )
P (t)
⎪
⎪
Ṗ (t) = α2 (t) 1 − L(t) − (α3 (t) + γ3 (t))P (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪ KP
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪ Ṅv (t) = α3 (t)P (t) − γ4 (t)Nv (t),
⎪
⎪
⎪
⎨
Ėv (t) = kv (t)Nv (t) − kv (t)Iv (t) − (νv + γ4 + kv (t))Ev (t), (6)
⎪
⎪
I˙v (t) = νv Ev (t) − γ4 (t)Iv (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
Ṡh (t) = Λh + γRh (t) − (dh + kh (t))Sh (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
Ėh (t) = kh (t)Sh (t) − (dh + α)Eh (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
I˙h (t) = αEh (t) − (dh + κ + rh )Ih (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
Ṙh (t) = rh Ih (t) − (dh + γ)Rh (t),
⎩

with initial conditions:

E(0) > 0, L(0) > 0, P (0) > 0,

Sh (0) > 0, Eh (0) > 0, Ih (0) > 0, Rh (0) > 0,
Nv (0) > 0, Ev (0) > 0, Iv (0) > 0.

At any time t ≥ 0, we have:

Ṅh (t) = Λh − dh Nh (t) − κIh (t), (7)

Ṅv (t) = α3 (t)P (t) − γ4 (t)Nv (t). (8)
8 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

3. Preliminaries and main results

In this section, we focus on the global behavior of model (6). Before starting our study, we enumerate
some hypotheses and recall some fundamental results which will be used in our further analysis.
(H6): Constant parameters of the model are positive,
(H7): γ1 (t), γ2 (t), γ3 (t), γ4 (t), b(t) and β(t) are positive, continuous and periodic functions with the same
period ω.

3.1. Preliminaries

Let (Rn+ , Rn+ ) be the standard ordered n-dimensional Euclidean space with a norm ∥.∥.
For u, v ∈ Rn , we denote

u ≥ v, if u − v ∈ Rn+ ,
u > v, if u − v ∈ Rn+ \ {0},
u ≫ v, if u − v ∈ int(Rn+ ).

For a continuous positive ω-periodic function W, we define

Ŵ = sup W(t) and W̄ = inf W(t).

t∈[0,ω] t∈[0,ω]

Let us consider the following linear ordinary differential system:

ż(t) = N (t)z(t), (9)

where N (t) is a continuous, cooperative, irreducible and ω-periodic n × n matrix function. Let ΦN (t) be
( )
the fundamental solution matrix of (9) and ρ ΦN (ω) be the spectral radius of the matrix ΦN (ω). By the
( )
Perron–Frobenius theorem (see [35], Theorem A.3), ρ ΦN (ω) is the principal eigenvalue of ΦN (ω) which is
associated to the eigenvector v ∗ ≫ 0.
The following result is useful for our subsequent comparison arguments.

1
Lemma 3.1 ([36]). Let r = ω ln ρ(ΦN (ω)), then there exists a positive ω-periodic function v(t) such that
v(t)ert is a solution of (9).

Definition 3.1 ([1]). Let X be a metric space with metric d and g : X → X a continuous map. For any
x ∈ X , we denote
g n (x) = g(g n−1 (x)) for any integer n > 1 and g 1 (x) = g(x).
g is said to be compact in X if for any bounded set H ∈ X , the set

g(H) = {g(x) : x ∈ H}

is precompact in X .
g is said to be point dissipative if there is a bounded set B0 ∈ X such that B0 attracts each point in X .

lim d g n (x), B0 = 0 for any x0 ∈ X .

( )
n→∞

The positive semiorbit through x0 is defined by

γ + (x0 ) = {xn = g n (x0 ), n = 1, 2, . . .}

 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 9

and the negative semiorbit through x0 is defined as a sequence γ − (x0 ) = {xk } satisfying g(xk−1 ) = xk for
integers k ≤ 0.
The omega limit set of γ + (x0 ) is defined by

ω ′ (x0 ) = {c ∈ X : there is a sequence nk → ∞ such that lim xnk = c}

k→∞

and the alpha limit set of γ − (x0 ) is defined by

α′ (x0 ) = {c ∈ X : there is a sequence nk → −∞ such that lim xnk = c}.

k→∞

A nonempty set C ⊂ X is said to be invariant if g(C) ⊆ C. A nonempty invariant set M of X is called to

be isolated in X if it is the maximal invariant set in the neighborhood of itself.
For a nonempty set M of X , the set

W s (M ) := {x ∈ X : lim d(g n (x), M ) = 0}

n→∞

is called the stable set of M .

Let A1 and A2 be two isolated invariant sets. The set A1 is said to be chained to set A2 , written A1 → A2
if there exists a full orbit through some x ∈ / A1 ∪ A2 such that ω ′ (x) ⊂ A2 and α′ (x) ⊂ A1 .
A finite sequence {M1 , . . . , Mk } of isolated invariant sets is called a chain if M1 → M2 → M3 → ... → Mk ,
and if Mk = M1 then the chain is called a cycle. Let X0 be a nonempty open set of X . We denote

∂X0 = X \ X0 , and M∂ := {x ∈ ∂X0 : g n (x) ∈ ∂X0 , ∀ n ≥ 0}.

Lemma 3.2 ([22]). Let g : X → X a continuous map. Assume that the following conditions hold:
(i) g is compact and point dissipative, and g(∂X0 ) ⊆ ∂X0 ,
(ii) there exists a finite sequence M = {M1 , . . . , Mk } of compact and isolated invariant sets such that
(a) Mi ∩ Mj = ∅ for any i, j = 1, 2, . . . , k and i ̸= j;
⋃ ′
⋃k
(b) x∈M∂ ω (x) ⊂ i=1 Mi ;
(c) no subset of M forms a cycle in ∂X0 ;
(d) W s (Mi ) ∩ X0 = ∅ for each 1 ≤ i ≤ k.
Then, g is uniformly persistent with respect to (X0 , ∂X0 ), that is, there exists a positive constant η such that
lim inf n→∞ d(g n (x), ∂X0 ) ≥ η.

Theorem 3.1 ([37,38]). Let G : Rn −→ R be a differential function and let f (x) be a vector fields. Let λ ∈ R
and let Γ = x ∈ Rn : G(x) ≤ λ be such that ∇G(x) ̸= 0 for all x ∈ x ∈ Rn : G(x) = λ = G−1 (λ). If
{ } { }

f (x), ∇G(x) ≤ 0 for all x ∈ G−1 (λ), then the set Γ is positively invariant.
⟨ ⟩

3.2. Dynamics analysis of vector population model

Let us consider the following system:

( )
E(t)
⎧
⎪ Ė(t) = b(t) 1 −
⎪ Nv (t) − (α1 (t) + γ1 (t))E(t),
⎪
⎪
⎪
⎪ KE
( )
⎨ L̇(t) = α (t) 1 − L(t) E(t) − (α (t) + γ (t))L(t),
⎪
⎪
⎪
1 2 2
KL (10)
( )
P (t)
⎪
⎪
Ṗ (t) = α2 (t) 1 − L(t) − (α3 (t) + γ3 (t))P (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪ KP
⎩
Ṅv (t) = α3 (t)P (t) − γ4 (t)Nv (t).
10 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

System (10) can be written as follows:

{ ( )
Ż1 (t) = f1 t, Z1 (t) ,
(11)
Z1 (0) > 0,

where
Z1 (t) = (E(t), L(t), P (t), Nv (t))T .

3.2.1. Positivity and boundedness of solutions

Lemma 3.3. For any positive initial condition φ1 = (E(0), L(0), P (0), Nv (0)), system (10) admits a unique
positive solution u1 (t, φ1 ) for all t ≥ 0. Moreover, the closed set
{ }
α̂3
∆1 = (E, L, P, Nv ) ∈ R4+ : E ≤ KE , L ≤ KL , P ≤ KP , Nv ≤ KP
γ̄4

is positively invariant and attracting under the flow described by system (10).

Proof . For any positive initial condition φ1 , the function f1 (t, φ1 ) is continuous in (t, φ1 ) and Lipschitzian
in φ1 . So, thanks to Theorem 2.2.1 and 2.2.3 of Hale and Verduyn Lunel [21], system (10) has a unique
solution u1 (t, φ1 ) on its maximal interval [0, tmax ) of existence.
In addition, for all t ≥ 0, let
{ }
e(t) = min E(t), L(t), P (t), Nv (t) .
/ R∗+ and e(t) > 0 for all t ∈ [0, t1 ).
Suppose that there exists t1 > 0 such that e(t1 ) ∈
If e(t) = Nv (t) then, from the fourth equation of system (10), we have

Ṅv (t) > −γ4 (t)Nv (t).

It then follows that ( ∫ t1 )

Nv (t1 ) > Nv (0) exp − γ4 (t)dt > 0,
0
which leads to a contradiction.
If e(t) = E(t) then, from the first equation of system (10), we have
( )
Ė(t) > − α1 (t) + γ1 (t) E(t).

It then follows that ( ∫ t1 ( )

)
E(t1 ) > E(0) exp − α1 (t) + γ1 (t) dt > 0,
0
which leads to a contradiction.
Similar contradictions can be obtained if e(t) = L(t) and e(t) = P (t). Hence, the solution u1 (t, φ1 ) is
positive. Moreover, let

Q1 = (E, L, P, Nv ) ∈ R4+ : E ≤ KE , Q2 = (E, L, P, Nv ) ∈ R4+ : L ≤ KL ,

{ } { }
{ α̂3 }
Q3 = (E, L, P, Nv ) ∈ R4+ : P ≤ KP , Q4 = (E, L, P, Nv ) ∈ R4+ : Nv ≤
{ }
KP .
γ̄4
Let us show that Q1 , Q2 , Q3 and Q4 are positively invariant.
Let

G1 (E, L, P, Nv ) = E, G2 (E, L, P, Nv ) = L, G3 (E, L, P, Nv ) = P and G4 (E, L, P, Nv ) = Nv .

 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 11

It is clear that Gi (E, L, P, Nv ) is differentiable for i = 1, 2, 3, 4. It then follows that:

∇G1 (E, L, P, Nv ) = (1, 0, 0, 0), ∇G2 (E, L, P, Nv ) = (0, 1, 0, 0),

∇G3 (E, L, P, Nv ) = (0, 0, 1, 0), ∇G4 (E, L, P, Nv ) = (0, 0, 0, 1).

Moreover, let

Γ1 = (E, L, P, Nv ) ∈ R4+ : E = KE , Γ2 = (E, L, P, Nv ) ∈ R4+ : L = KL ,

{ } { }
{ α̂3 }
Γ3 = (E, L, P, Nv ) ∈ R4+ : P = KP , Γ4 = (E, L, P, Nv ) ∈ R4+ : Nv =
{ }
KP .
γ̄4
Thus, if:
⟨ ⟩ ( )
• x ∈ Γ1 , then f1 (t, x), ∇G1 (x) = − α1 (t) + γ1 (t) < 0.
⟨ ⟩ ( )
• x ∈ Γ2 , then f1 (t, x), ∇G2 (x) = − α2 (t) + γ2 (t) < 0.
⟨ ⟩ ( )
• x ∈ Γ3 , then f1 (t, x), ∇G3 (x) = − α3 (t) + γ3 (t) < 0.
f1 (t, x), ∇G4 (x) = α3 (t)P (t) − γ4 (t) α̂γ̄43 KP ≤ α̂3 (P (t) − KP ) ≤ 0.
⟨ ⟩
• x ∈ Γ4 , then
So, thanks to Theorem 3.1, we conclude that the compact set ∆1 is positively invariant and then the
solution u1 (t, φ1 ) is bounded. It then follows that tmax = +∞. □

3.2.2. Vector reproduction ratio

We introduce the threshold dynamics for system (10) according to the theory developed by Wang and
Zhao [39] which is a generalization of Van den Driessche and James Watmough method, [40]. Linearizing
system (10) at the unique mosquito-free equilibrium H 0 = (0, 0, 0, 0), we obtain the following system:

Ė(t) = b(t)Nv (t) − (α1 (t) + γ1 (t))E(t),

⎧
⎪
⎪
⎨ L̇(t) = α (t)E(t) − (α (t) + γ (t))L(t),
⎪
1 2 2
(12)
⎪
⎪
⎪ Ṗ (t) = α2 (t)L(t) − (α3 (t) + γ 3 (t))P (t),
⎩
Ṅv (t) = α3 (t)P (t) − γ4 (t)Nv (t),

which can be written as follows: ( )

U̇1 (t) = F1 (t) − V1 (t) U1 (t)

with
U1 (t) = (E(t), L(t), P (t), Nv (t))T

and
α1 (t) + γ1 (t)
⎛ ⎞
0 0 0
⎜ −α1 (t) α2 (t) + γ2 (t) 0 0 ⎟
V1 (t) = ⎜ ⎟,
⎜ ⎟
⎝ 0 −α2 (t) α3 (t) + γ3 (t) 0 ⎠
0 0 −α3 (t) γ4 (t)
⎛ ⎞
0 0 0 b(t)
⎜ 0 0 0 0 ⎟
F1 (t) = ⎜
⎝ 0 0 0
⎟.
0 ⎠
0 0 0 0
For all t ≥ s, let Ỹ (t, s) be the evolution operator of the linear periodic system

ẏ = −V1 (t)y.
12 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

For each s ∈ R, the 4 × 4 matrix Ỹ (t, s) satisfies

Ẏ (t, s) = −V1 (t)Y (t, s), ∀t ≥ s, Y (s, s) = I, (13)

where I is the 4 × 4 identity matrix.

Let Cω be the ordered Banach space of all ω-periodic functions from R to R4 which is equipped with the
maximum norm ∥.∥ and the positive cone

C+
{ }
ω := ϕ ∈ Cω : ϕ(t) ≥ 0, ∀t ∈ R .

Suppose ϕ(s) ∈ Cω is the initial distribution of juvenile and adults mosquitoes. Then, F1 (s)ϕ(s) ∈ Cω is
the distribution of new juvenile mosquitoes in the breeding habits produced by the adult ones which were
introduced at time s. Hence, for any t ≥ s, Y (t, s)F1 (s)ϕ(s) is the distribution of those mosquitoes which
were newly born into the juvenile mosquito compartment at time s and remain alive. Thus,
∫ t ∫ ∞
ψ̃(t) = Y (t, s)F1 (s)ϕ(s)ds = Y (t, t − a)F1 (t − a)ϕ(t − a)da, a ∈ [0, ∞)
−∞ 0

is the distribution of new eggs at time t, hatched by all female adult mosquitoes ϕ(s) introduced at the
previous time s.
Let L : Cω −→ Cω be the linear operator defined by
∫ ∞
(Lϕ)(t) = Y (t, t − a)F1 (t − a)ϕ(t − a)da, ∀t ∈ R, ϕ ∈ Cω .
0

Then, the vector reproduction ratio is Rv := ρ(L), the spectral radius of L.

3.2.3. Global stability of mosquito-free equilibrium

Lemma 3.4 ([39]).

(i) Rv = 1 if and only if ρ(ΦF1 −V1 (ω)) = 1.
(ii) Rv < 1 if and only if ρ(ΦF1 −V1 (ω)) < 1.
(iii) Rv > 1 if and only if ρ(ΦF1 −V1 (ω)) > 1.
Hence, if Rv < 1 then the mosquito-free equilibrium is locally asymptotically stable.

Theorem 3.2. The mosquito-free equilibrium H 0 = (0, 0, 0, 0) is globally attractive if Rv < 1.

Proof . For all t ≥ 0, since E(t) ≤ KE , L(t) ≤ KL and P (t) ≤ KP , we have:

E(t) L(t) P (t)

1− ≤ 1, 1 − ≤ 1 and 1 − ≤ 1.
KE KL KP
Thus, system (10) becomes:
⎧
⎪
⎪ Ė(t) ≤ b(t)Nv (t) − (α1 (t) + γ1 (t))E(t),
⎪
⎪
⎪
⎪
⎨ L̇(t) ≤ α1 (t)E(t) − (α2 (t) + γ2 (t))L(t),
⎪
⎪

Ṗ (t) ≤ α2 (t)L(t) − (α3 (t) + γ3 (t))P (t),

⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
Ṅv (t) = α3 (t)P (t) − γ4 (t)Nv (t).
⎩
 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 13

Let us consider the following auxiliary system:

⎧ ˙
⎪
⎪ Ẽ(t) = b(t)Ñv (t) − (α1 (t) + γ1 (t))Ẽ(t),
⎪
⎪
⎪
⎪
⎪ ˙
⎨ L̃(t) = α1 (t)Ẽ(t) − (α2 (t) + γ2 (t))L̃(t),
⎪
⎪

P̃˙ (t) = α2 (t)L̃(t) − (α3 (t) + γ3 (t))P̃ (t),

⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎩ ˙
⎪
Ñv (t) = α3 (t)P̃ (t) − γ4 (t)Ñv (t).

For the convenience, we will rewrite it as follows

˜˙ = F1 (t) − V1 (t) J(t),

˜
( )
J(t) (14)

with
˜ = (Ẽ(t), L̃(t), P̃ (t), Ñv (t))T .
J(t)
If Rv < 1, then from Lemma 3.4, ρ(ΦF1 −V1 (ω)) < 1. By Lemma 3.1, there exists a positive ω-periodic
˜ = v(t)ert with r = 1 ln ρ(ΦF −V (ω)). Since the function v(t) is bounded and
function v(t) such that J(t) ω 1 1
˜ → 0 as t → ∞. By applying the comparison theorem [41]
ρ(ΦF1 −V1 (ω)) < 1 then, we have r < 0 and J(t)
on system (14), we get
lim (E(t), L(t), P (t), Nv (t)) = (0, 0, 0, 0).
t→+∞

It then follows that the mosquito-free equilibrium H 0 is globally attractive which completes the proof. □

3.2.4. Persistence of mosquitoes

Let us define the following sets:

X := R4+ ,
X0 := {(E, L, P, Nv ) ∈ X : E > 0, L > 0, P > 0, Nv > 0},
∂X0 := {(E, L, P, Nv ) ∈ X : ELP Nv = 0}.

Let Φ(t) be the periodic semiflow generated by the periodic system (10) and S1 : X −→ X the Poincaré
map associated with system (10), namely:

S1 (φ1 ) = Φ(ω)φ1 = u1 (ω, φ1 ), ∀φ1 ∈ X.

S1m (φ1 ) = Φ(mω)φ1 = u1 (mω, φ1 ), ∀m ≥ 0.
{ }
It then follows that the study of the dynamics (10) reduces to that of the discrete dynamical system S1m
on X. Otherwise, note that for all φ1 ∈ X0 , Φ(t)(φ1 ) = u1 (t, φ1 ) ∈ X0 . Thus, Φ(t)(X0 ) ⊂ X0 , for all t ≥ 0.
So, X0 and ∂X0 are positively invariant. Therefore, Lemma 3.1 implies that discrete-time system S1 is point
dissipative.

Lemma 3.5. If Rv > 1, there exists δ > 0 such that when

φ1 − H 0  ≤ δ, for any φ1 ∈ X0 ,

 

one has
lim sup d S1k (φ1 ), H 0 ≥ δ.
( )
k→∞
14 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

Proof . Suppose by contradiction that

lim sup d S1k (φ1 ), H 0 < δ for some

( )
φ1 ∈ X0 . (15)
k→∞
( )
Then, there exists an integer k2 such that for all k ≥ k2 , d S1k (φ1 ), H 0 < δ. By the continuity of the solution
u1 (t, φ1 ), we have  ( k
u1 t, S1 (φ1 ) − u1 (t, H 0 ) ≤ α, ∀t ≥ 0 and α > 0.
) 

+ t1 , where t1 ∈ [0, ω] and k = ωt . ωt is the greatest integer less than or egal to ωt . If

[ ] [ ]
Let t = kω
 
φ1 − H 0  ≤ δ, then we get

u1 t, φ1 − u1 (t, H 0 ) = u1 t1 + kω, φ1 − u1 (t1 + kω, H 0 )

 ( )   ( ) 

= u1 t1 , S1k φ1 − u1 (t1 , H 0 ) ≤ α, for any t ≥ 0.

 ( ) 

It then follows that for all t ≥ 0,

0 ≤ E(t) ≤ α, 0 ≤ L(t) ≤ α and 0 ≤ P (t) ≤ α.

{ }
Thus, there exists α∗ = max α α α
KE , KL , KP such that

E(t) L(t) P (t)

1− ≥ 1 − α∗ , 1 − ≥ 1 − α∗ and 1 − ≥ 1 − α∗ , for all t ≥ 0.
KE KL KP
Furthermore, system (10) can be rewritten as follows:
Ė(t) ≥ b(t)(1 − α∗ )Nv (t) − (α1 (t) + γ1 (t))E(t),
⎧
⎪
⎪
⎨ L̇(t) ≥ α (t)(1 − α∗ )E(t) − (α (t) + γ (t))L(t),
⎪
1 2 2
∗
(16)
⎪
⎪
⎪ Ṗ (t) ≥ α2 (t)(1 − α )L(t) − (α 3 (t) + γ 3 (t))P (t),
⎩
Ṅv (t) = α3 (t)P (t) − γ4 (t)Nv (t).
Let us consider the following auxiliary linear system

Ṙ(t) = Mα∗ (t)R(t), (17)

where
R(t) = (E(t), L(t), P (t), Nv (t))T
and
b(t)(1 − α∗ )
( )
− α1 (t) + γ1 (t) 0 0
⎛ ⎞

α1 (t)(1 − α∗ )
( )
⎜ − α2 + γ2 (t) 0 0 ⎟
Mα∗ (t) = ⎜ ⎟.
⎜ ⎟
α2 (t)(1 − α∗ )
( )
⎝ 0 − α3 (t) + γ3 (t) 0 ⎠
0 0 α3 (t) −γ4 (t)
Since limα∗ →0+ ΦMα∗ (ω) = ΦF1 −V1 (ω) and by the continuity of the spectral radius, we have
( )
limα∗ →0+ ρ ΦMα∗ (ω) = ρ(ΦF1 −V1 (ω)). From Lemma 3.4 if Rv > 1, then ρ(ΦF1 −V1 (ω)) > 1 and
( ) ( )
limα∗ →0+ ρ ΦMα∗ (ω) > 1. It then follows that there exists α1 > 0 such that ρ ΦMα∗ (ω) > 1, for all
α ∈ [0, α1 ]. From Lemma 3.1, there exists a positive ω-periodic function v(t) such that R(t) = v(t)ert with
r = ω1 ln ρ ΦMα∗ (ω) . Since ρ ΦMα∗ (ω) > 1 and function v(t) is bounded, then r > 0 and R(t) → ∞ as
( ) ( )

t → ∞. By applying the comparison theorem on system (17), we get

lim |(E(t), L(t), P (t), Nv (t))| = ∞,

t→∞

which is in contradiction with (15). □

 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 15

Theorem 3.3. If Rv > 1, there exists η > 0 such that any solution (E(t), L(t), P (t), Nv (t)) with initial
condition φ1 ∈ X0 satisfies
lim inf E(t) ≥ η, lim inf L(t) ≥ η, lim inf P (t) ≥ η, lim inf Nv (t) ≥ η
t→∞ t→∞ t→∞ t→∞

and system (10) has at least one positive periodic solution.

Proof . Denote
M∂ = φ1 ∈ ∂X0 : S1k (φ1 ) ∈ ∂X0 , k ≥ 0 .
{ }

At first, we prove that M∂ = {(0, 0, 0, 0)}.

It is clear that {(0, 0, 0, 0)} ⊂ M∂ . So, we only need to show that M∂ ⊂ {(0, 0, 0, 0)}, which means that
for any initial condition φ1 ∈ ∂X0 ,
E(kω) = 0, or L(kω) = 0 or P (kω) = 0 or Nv (kω) = 0, ∀k ≥ 0.
Let φ1 ∈ ∂X0 . Suppose by contradiction that there exists an integer k1 ≥ 0 such that (E(k1 T ), L(k1 ω),
P (k1 ω), Nv (k1 ω))T > 0. Using the constant variation formula, we derive that
( ∫ t )[ ∫ t (∫ s ) ]
E(t) = exp − h1 (s)ds E(0) + b(s)Nv (s) exp h1 (τ )dτ ds , (18)
0 0 0
( ∫ t )[ ∫ t (∫ s ) ]
L(t) = exp − h2 (s)ds L(0) + α1 (s)E(s) exp h2 (τ )dτ ds , (19)
( ∫0 t )[ 0
∫ t (∫ 0
s ) ]
P (t) = exp − h3 (s)ds P (0) + α2 (s)L(s) exp h3 (τ )dτ ds , (20)
( ∫0 t )[ 0
∫ t ( 0
∫ s ) ]
Nv (t) = exp − γ4 (s)ds Nv (0) + α3 (s)P (s) exp − γ4 (τ )dτ ds , (21)
0 0 0
where
b(t)
h1 (t) = Nv (t) + α1 (t) + γ1 (t),
KE
α1 (t)
h2 (t) = E(t) + α2 (t) + γ2 (t),
KL
α2 (t)
h3 (t) = L(t) + α3 (t) + γ3 (t).
KP
Thus, taking k1 ω as the initial time in (18)–(21), we obtain that E(t) > 0, L(t) > 0, P (t) > 0 and Nv (t) > 0,
for all t > k1 ω, which contradicts the fact that ∂X0 is positively invariant so M∂ ⊂ {(0, 0, 0, 0)}. Hence, it
then follows that M∂ = {(0, 0, 0, 0)}.
Equality M∂ = {(0, 0, 0, 0)} implies that H 0 is a fixed point of S1 and acyclic in M∂ . Thus, every
solution in M∂ approaches to H 0 . Moreover, Lemma 3.5 implies that H 0 is an isolate invariant set in X and
W s (H 0 )∩X0 = ∅. Therefore, by Theorem 3.1.1 in [22], we finally obtain that S1 is uniformly persistent with
respect to (X0 , ∂X0 ). So, the periodic semiflow Φ(t) is also uniformly persistent. It then follows that there
exists η > 0 such that any solution (E(t), L(t), P (t), Nv (t)) with initial condition (E(0), L(0), P (0), Nv (0)) ∈
X0 satisfies
lim inf E(t) ≥ η, lim inf L(t) ≥ η, lim inf P (t) ≥ η, lim inf Nv (t) ≥ η.
t→∞ t→∞ t→∞ t→∞
Besides, thanks to Theorem 1.3.6 in [22], system (10) has at least one periodic solution u∗1 (t, φ∗1 ) with
φ∗1 = (E ∗ (0), L∗ (0), P ∗ (0), Nv∗ (0)) ∈ X0 . Since φ∗1 ∈ X0 , then from Eqs. (18)–(21) we obtain that
E ∗ (t) > 0, L∗ (t) > 0, P ∗ (t) > 0 and Nv∗ (t) > 0 for all t ≥ 0. Thus, the ω-periodic solution u∗1 (t, φ∗1 ) is
positive. □

Lemma 3.6 ([42]). If Rv > 1, then solution Nv∗ (t) of Eq. (8) with initial value Nv∗ (0) is bounded and globally
uniformly attractive on [0, ∞).
16 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

3.3. Dynamics analysis of malaria transmission model

The previous results indicate that the mosquito population will die out if Rv < 1, and if Rv > 1,
the mosquito population persists at the ω-periodic steady state (E ∗ (t), L∗ (t), P ∗ (t), Nv∗ (t)). Consequently,
when the parasite is introduced in human population or mosquito population, the dynamics of malaria
transmission model due to the interaction between humans and mosquitoes is given by the following limiting
system: ⎧
⎪
⎪ Ṡh (t) = Λh + γRh (t) − (dh + kh (t))Sh (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪ Ėh (t) = kh (t)Sh (t) − (dh + α)Eh (t),
⎪
⎪
⎪
⎨ I˙h (t) = αEh (t) − (dh + κ + rh )Ih (t),
⎪
⎪
⎪
(22)
Ṙ (t) = r I (t) − (d + γ)R (t),
⎪
h h h h h
⎪
⎪
⎪
⎪
⎪
⎪
⎪
Ėv (t) = kv (t)Nv∗ (t) − kv (t)Iv (t) − (νv + γ4 (t) + kv (t))Ev (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎩ ˙
Iv (t) = νv Ev (t) − γ4 (t)Iv (t).
System (22) can be written as follows:
{ ( )
Ż2 (t) = f2 t, Z2 (t) ,
(23)
Z2 (0) > 0,
where
Z2 (t) = (Sh (t), Eh (t), Ih (t), Rh (t), Ev (t), Iv (t))T .

3.3.1. Positivity and boundedness of solutions

Lemma 3.7. For any positive initial condition φ2 = (Sh (0), Eh (0), Ih (0), Rh (0), Ev (0), Iv (0)), system (22)
admits a unique positive solution u2 (t, φ2 ) for all t ≥ 0. Moreover, the closed set
{ }
6 Λh α̂3
∆2 = (Sh , Eh , Ih , Rh , Ev , Iv ) ∈ R+ : Nh ≤ , Ev + Iv ≤ KP .
dh γ̄4

is positively invariant and attracting under the flow described by system (22).

Proof . For any positive initial condition φ2 , the function f2 (t, φ2 ) is continuous in (t, φ2 ) and Lipschitzian
in φ2 . So, thanks to Theorems 2.2.1 and 2.2.3 of Hale and Verduyn Lunel [21], system (22) has a unique
solution u(t, φ2 ) on its maximal interval [0, tmax ) of existence.
In addition, for all t ≥ 0, let

e′ (t) = min Sh (t), Eh (t), Ih (t), Rh (t), Ev (t), Iv (t) .

{ }

Suppose that there exists t1 > 0 such that e′ (t1 ) ∈

/ R∗+ and e′ (t) > 0 for all t ∈ [0, t1 ).
′
If e (t) = Sh (t) then, from the second equation of system (22), we have

Ėh (t) > −(dh + α)Eh (t).

It then follows that

[ ]
Eh (t1 ) > Eh (0) exp −(dh + α)t1 > 0,
which leads to a contradiction.
 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 17

If e′ (t) = Eh (t) then, from the third equation of system (22), we have

I˙h (t) > −(dh + κ + rh )Eh (t).

It then follows that

[ ]
Ih (t1 ) > Ih (0) exp −(dh + κ + rh )t1 > 0,
which leads to a contradiction.
If e′ (t) = Ih (t) then, from the fourth equation of system (22), we have

Ṙh (t) > −(dh + γ)Rh (t).

It then follows that

[ ]
Rh (t1 ) > Rh (0) exp −(dh + γ)t1 > 0,
which leads to a contradiction.
Similar contradictions can be obtained if e′ (t) = Iv (t) and e′ (t) = Ev (t). Hence, the solution u2 (t, φ2 ) is
positive. Moreover, let
{ }
6 Λh
Q5 = (Sh , Eh , Ih , Rh , Ev , Iv ) ∈ R : Sh + Eh + Ih + Rh ≤ ,
dh
{ }
6 α̂3
Q6 = (Sh , Eh , Ih , Rh , Ev , Iv ) ∈ R : Ev + Iv ≤ KP
γ̄4
and
G5 (Sh , Eh , Ih , Rh , Ev , Iv ) = Sh + Eh + Ih + Rh , G6 (Sh , Eh , Ih , Rh , Ev , Iv ) = Ev + Iv .
It is clear that G5 and G6 are differentiable and we have:

∇G5 (Sh , Eh , Ih , Rh , Ev , Iv ) = (1, 1, 1, 1, 0, 0) and ∇G6 (Sh , Eh , Ih , Rh , Ev , Iv ) = (0, 0, 0, 0, 1, 1).

Moreover, let { }
Λh
Γ5 = (Sh , Eh , Ih , Rh , Ev , Iv ) ∈ R6 : Sh + Eh + Ih + Rh =
dh
and { }
6 α̂3
Γ6 = (Sh , Eh , Ih , Rh , Ev , Iv ) ∈ R : Ev + Iv = KP .
γ̄4
We have:
⟨ ⟩
f2 (t, x), ∇G5 (x) = Λh − dh Nh − γ3 Ih
≤ Λh − dh Nh .
f2 (t, x), ∇G6 (x) = kv (t)(Nv∗ (t) − Ev − Iv ) − dv(t)(Ev + Iv )
⟨ ⟩
( )
α̂3
≤ kv (t) KP − (Ev + Iv ) − γ4 (t)(Ev + Iv ).
γ̄4
Thus, if:
⟨ ⟩
• x ∈ Γ5 then, f2 (t, x), ∇G5 (x) ≤ 0,
⟨ ⟩
• x ∈ Γ6 then, f2 (t, x), ∇G6 (x) ≤ 0.
So, from Theorem 3.1, we conclude that the compact set ∆2 is positively invariant and then all the solutions
are nonnegative and bounded. □
18 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

3.3.2. Basic reproduction ratio

Using the same method as mentioned above, we derive the threshold dynamics associated to system
(22). Hence, by linearizing system (22) at the disease-free equilibrium W0 = (Sh∗ , 0, 0, 0, 0, 0), we obtain
the following system:

E˙h (t) = cvh β(t)Iv (t) − (dh + α)Eh (t),

⎧
⎪
⎪
⎪
⎪
⎪
I˙h (t) = αEh (t) − (dh + κ + rh )Ih (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
R˙h (t) = rh Ih (t) − (dh + γ)Rh (t),
⎨
(24)
⎪
⎪
N ∗ (t) N ∗ (t)
⎪
E˙v (t) = chv β(t) Sv ∗ Ih (t) + c̄hv β(t) Sv ∗ Rh (t) − (νv + γ4 (t))Ev (t),
⎪
⎪
⎪
⎪
h h
⎪
⎪
⎪
⎪
⎪
⎪
⎩ ˙
Iv (t) = νv Ev (t) − γ4 (t)Iv (t).

System (24) can be written as follows:

( )
U̇2 (t) = F2 (t) − V2 (t) U2 (t)

with
U2 (t) = (Eh (t), Ih (t), Rh (t), Ev (t), Iv (t))T

and ⎛ ⎞
0 0 0 0 cvh β(t)
⎜ 0 0 0 0 0
⎜ ⎟
⎟
⎜ ⎟
⎜ 0 0 0 0 0
F2 (t) = ⎜ ⎟,
⎟
∗ ∗
⎜ N
⎜ 0 chv β(t) v ∗(t) N (t) ⎟
Sh c̄hv β(t) Sv ∗ 0 0 ⎟
⎝ h ⎠
0 0 0 0 0
⎛ ⎞
dh + α 0 0 0 0
⎜ −α dh + κ + rh 0 0 0
⎜ ⎟
⎟
⎜ ⎟
V2 (t) = ⎜⎜ 0 −rh dh + γ 0 0 ⎟.
⎟
0 0 0 νv + γ4 (t) 0
⎜ ⎟
⎝ ⎠
0 0 0 −νv γ4 (t)

Let us assume that Ỹ (t, s), t ≥ s is the matrix solution of the linear ω-periodic system
{
Ỹ˙ (t, s) = −V2 (t)Ỹ (t, s), ∀t ≥ s,
(25)
Ỹ (s, s) = I,

where I is the 5 × 5 identity matrix.

Let Cω be the ordered Banach space of all ω-periodic functions from R to R5 which is equipped with the
{ }
maximum norm ∥.∥ and the positive cone C+ ω := ϕ ∈ Cω : ϕ(t) ≥ 0, ∀t ∈ R . Then, we can define a linear
operator L̃ : Cω −→ Cω by
∫ ∞
(L̃ϕ)(t) = Ỹ (t, t − a)F2 (t − a)ϕ(t − a)da, ∀t ∈ R, ϕ ∈ Cω . (26)
0

L̃ is the next infection operator, and the basic reproduction ratio is R0 = ρ(L̃), the spectral radius of L̃.
 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 19

3.3.3. Global stability of disease-free equilibrium

Lemma 3.8 ([14]).

(i) R0 = 1 if and only if ρ(ΦF2 −V2 (ω)) = 1.
(ii) R0 < 1 if and only if ρ(ΦF2 −V2 (ω)) < 1.
(iii) R0 > 1 if and only if ρ(ΦF2 −V2 (ω)) > 1.
Hence, if R0 < 1 then the disease-free equilibrium, W0 is locally asymptotically stable.

Theorem 3.4. The disease-free equilibrium W0 is globally attractive if R0 < 1 and κ = 0.

Proof . If κ = 0, then from Eq. (7), there exists a period T (ϵ) > 0 such that

Nh (t) ≥ Sh∗ − ϵ, ∀t ≥ T (ϵ).

Thus, for all t ≥ T (ϵ), we have

Nv∗ (t) Nv∗ (t)

kv (t)Nv∗ (t) ≤ chv β(t) I h (t) + c̄hv β(t) Rh (t).
Sh∗ − ϵ Sh∗ − ϵ

Hence, from system (22) we obtain the following system:

⎧
⎪
⎪ Ėh (t) ≤ cvh β(t)Iv (t) − (dh + α)Eh (t),
⎪
⎪
⎪
I˙h (t) = αEh (t) − (dh + rh )Ih (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎨
Ṙh (t) = rh Ih (t) − (dh + γ)Rh (t), (27)
⎪
⎪
N ∗ (t) N ∗ (t)
⎪
⎪
Ėv (t) ≤ chv β(t) S ∗v −ϵ Ih (t) + c̄hv β(t) S ∗v −ϵ Rh (t) − (νv + γ4 (t))Ev (t),
⎪
⎪
⎪
h h
⎪
⎪
⎪
⎪
⎪
⎪
⎩ ˙
Iv (t) = νv Ev (t) − γ4 (t)Iv (t).

Now, let us consider the following auxiliary system,

z̃˙ = Aϵ (t)z̃(t) (28)

with
z̃(t) = (Ẽh (t), I˜h (t), R̃h (t), Ẽv (t), I˜v (t))T

and ⎛ ⎞
−(dh + α) 0 0 0 cvh β(t)
α −(dh + rh ) 0 0 0
⎜ ⎟
⎜ ⎟
⎜ ⎟
Aϵ (t) = ⎜
⎜ 0 rh −(dh + γ) 0 0 ⎟.
⎟
⎜ N ∗ (t) N ∗ (t) ⎟
⎜ 0 chv β(t) S ∗v −ϵ c̄hv β(t) S ∗v −ϵ −(νv + γ4 (t)) 0 ⎟
⎝ h h ⎠
0 0 0 −γ4 (t)
νv
) (( )
Moreover, by continuity of spectral radius, we have limϵ→0+ ρ ΦAϵ (ω) = ρ ΦF2 −V2 (ω) . In addition,
( )
from Lemma 3.8, if R0 < 1, then ρ(ΦF2 −V2 (ω)) < 1, thus, limϵ→0+ ρ ΦAϵ (ω) < 1. It then follows that
( )
there exists ϵ1 > 0 such that ρ ΦAϵ (ω) < 1 for all ϵ ∈ [0, ϵ1 ]. From Lemma 3.1, there exists a positive
( )
ω-periodic function v(t) such that z̃(t) = v(t)ert is a solution of (28). Since ρ ΦAϵ (ω) < 1, so r < 0.
20 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

Therefore, the ω-periodic function v(t) is bounded, hence z̃(t) → 0 as t → ∞. Applying the comparison
theorem to system (27), we get

lim (Eh (t), Ih (t), Rh (t), Ev (t), Iv (t)) = (0, 0, 0, 0, 0).

t→∞

Moreover, we have

lim (Sh (t) − Sh∗ ) = lim Nh (t) − Eh (t) − Ih (t) − Rh (t) − Sh∗ = 0.
( )
t→∞ t→∞

Hence, we have limt→∞ Sh (t) = Sh∗ .

It then follows that the disease-free equilibrium W0 is globally attractive which completes the proof. □

3.3.4. Persistence of malaria transmission

Let us consider the following sets:

Y := R6+ ,
{ }
Y0 := (Sh , Eh , Ih , Rh , Ev , Iv ) ∈ Y : Eh > 0, Ih > 0, Rh > 0, Ev > 0, Iv > 0 ,
{ }
∂Y0 := (Sh , Eh , Ih , Rh , Ev , Iv ) ∈ Y : Eh Ih Rh Ev Iv = 0 .

Let S2 : Y −→ Y be the Poincaré map associated with system (22).

Lemma 3.9. The sets Y0 and ∂Y0 are positively invariant with respect to system (22).

Proof . For any initial condition φ2 ∈ Y0 , by solving system (22) we obtain, for all t > 0,
( ∫ t )[ ∫ t (∫ τ ) ]
Sh (t) = exp − H2 (τ )dτ Sh (0) + H1 (τ ) exp H2 (s)ds dτ > 0, (29)
0 0 0
[ ∫ t ( ) ]
( )
Eh (t) = exp −(dh + α)t Eh (0) + kh (τ )Sh (τ ) exp (dh + α)τ dτ > 0, (30)
0
[ ∫ t ( ) ]
( )
Ih (t) = exp −(dh + κ + rh )t Ih (0) + αEh (τ ) exp (dh + κ + rh )τ dτ > 0 (31)
0
[ ∫ t ( ) ]
( )
Rh (t) = exp −(dh + γ)t Rh (0) + rh Ih (τ ) exp (dh + γ)τ dτ > 0, (32)
0
( ∫ t )[ ∫ t (∫ τ ) ]
Ev (t) = exp − H4 (τ )dτ Ev (0) + H3 (τ ) exp H4 (s)ds dτ > 0 (33)
0 0 0
( ∫ t )[ ∫ t (∫ τ ) ]
Iv (t) = exp − γ4 (τ )dτ Iv (0) + νv Ev (τ ) exp γ4 (s)ds dτ > 0, (34)
0 0 0

with

H1 (t) = Λh + Ih (t) + γRh (t), H2 (t) = kh (t) + dh ,

H3 (t) = kv (t) Nv∗ (t) − Iv (t) , H4 (t) = kv (t) + γ4 (t) + νv .
( )

So, it then follows that Y0 is positively invariant. Therefore, ∂Y0 is relatively closed in Y , then, ∂Y0 is also
positively invariant with respect to system (22). □
 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 21

Moreover, the compact set ∆2 attracts all positive orbits in Y , which implies that the discrete-time system
S2 : Y −→ Y is point dissipative.

Lemma 3.10. If R0 > 1, there exists ξ > 0 such that when

∥φ2 − W0 ∥ ≤ ξ, for any φ2 ∈ Y0 ,

one has
lim sup d S2n (φ2 ), W0 ≥ ξ.
( )
n→∞

Proof . Suppose by contradiction that

lim sup d S2n (φ2 ), W0 < ξ for some φ2 ∈ Y0 .

( )
n→∞

Then, it follows that there exists an integer N ≥ 1 such that for all n ≥ N we have

d S2n (φ2 ), W0 < ξ.

( )

( )
By the continuity of solution u2 t, φ2 , we have
 ( n ( )) ( )
u2 t, S2 φ2 − u2 t, W0  ≤ ε, ∀t ≥ 0, ε > 0.

Let t = nω + t′ , with t′ ∈ [0, ω] and n = ωt . ωt is the greatest integer less than or egal to t
[ ] [ ]
ω. Then, we
have
u2 t, φ2 − u2 t, W0  = u2 t′ , S2n φ2 − u t′ , W0  < ε.
 ( ) ( )  ( ( )) ( )

Hence, it follows that

Sh∗ − ε ≤ Sh (t) ≤ Sh∗ + ε.
Thus, there exists ζ(ε) > 0 such that

Sh (t) Nv∗ (t) N ∗ (t)

≥ 1 − ζ(ε) and ≥ v∗ .
Nh (t) Nh (t) Sh

From system (22) we have:

E˙h (t) ≥ cvh β(t)(1 − ζ(ε))Iv (t) − (dh + α)Eh (t),

⎧
⎪
⎪
⎪
⎪
⎪
I˙h (t) = αEh (t) − (κ + dh + rh )Ih (t),
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎨ ˙
⎪
Rh (t) = rh Ih (t) − (dh + γ)Rh (t),
⎪
⎪ ( )
Nv∗ (t)
⎪
˙
⎪
Ev (t) ≥ β(t) S ∗ chv Ih (t) + c̄hv Rh (t) − (νv + γ4 (t))Ev (t),
⎪
⎪
⎪
h
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎩ ˙
Iv (t) = νv Ev (t) − γ4 (t)Iv (t).

Now, let us consider the following auxiliary linear system

˙
h̃(t) = Nζ(ε) (t)h̃(t) (35)

with
h̃(t) = (Ẽh (t), I˜h (t), R̃h (t), Ẽv (t), I˜v (t))T
22 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

and
⎛ ⎞
−(dh + α) 0 0 0 cvh β(t)(1 − ζ(ε))
α −(dh + rh ) 0 0 0
⎜ ⎟
⎜ ⎟
⎜ ⎟
⎜ 0 rh −(dh + γ) 0 0 ⎟
Nζ(ε) (t) = ⎜ ⎟,
⎜ Nv∗ (t) Nv∗ (t) ⎟
0 chv β(t) c̄hv β(t) −(νv + γ4 (t)) 0
⎜ ⎟
Sh∗ Sh∗
⎜ ⎟
⎝ ⎠
0 0 0 νv −γ4 (t)
( )
Once again if R0 > 1, there exists σ > 0 such that ρ ΦNζ(ε) (ω) > 1 for all ζ(ε) ∈ [0, σ]. In this case
r > 0 and from Lemma 3.1 we get h̃(t) → ∞ as t → ∞. Thus, by applying the theorem of comparison, we
get
lim |(Eh (t), Ih (t), Rh (t), Ev (t), Iv (t))| = ∞.
t→∞
This leads to a contradiction. □

Theorem 3.5. If R0 > 1, then system (22) is uniformly persistent and there exists at least one positive
periodic solution.

Proof . Set
M∂ = φ2 ∈ ∂Y0 : S2n (φ2 ) ∈ ∂Y0 , for any n ≥ 0 .
{ }

Now, we aim to show that

{ }
M∂ = (Sh , 0, 0, 0, 0, 0) ∈ Y : Sh ≥ 0 . (36)
It is obvious that
{ }
M∂ ⊃ (Sh , 0, 0, 0, 0, 0) ∈ Y : Sh ≥ 0 ,
so, we only need to show that
{ }
M∂ ⊂ (Sh , 0, 0, 0, 0, 0) ∈ Y : Sh ≥ 0 ,
that means that for any initial condition φ2 ∈ ∂Y0 and n ≥ 0, we have Eh (nω) = 0 or Ih (nω) = 0 or
Rh (nω) = 0 or Ev (nω) = 0 or Iv (nω) = 0.
Let φ2 ∈ ∂Y0 . Suppose by contradiction that there exists an integer n1 ≥ 0 such that Eh (n1 ω) >
0, Ih (n1 ω) > 0, Rh (n1 ω) > 0, Ev (n1 ω) > 0 and Iv (n1 ω) > 0. Thus, by replacing the initial time t = 0
by t = n1 ω in (29)–(34) we get Sh (t) > 0, Eh (t) > 0, Ih (t) > 0, Rh (t) > 0, Ev (t) > 0, Iv (t) > 0. That
{ }
contradicts the fact that ∂Y0 is positively invariant. Hence, M∂ ⊂ (Sh , 0, 0, 0, 0, 0) ∈ Y : Sh ≥ 0 and then
the equality (36) is true.
The equality (36) implies that W0 is a fixed point of S2 and acyclic in M∂ , every solution in M∂ approaches
to W0 . Moreover, Lemma 3.10 implies that W0 is an isolate invariant set in Y and W s (W0 ) ∩ Y0 = ∅. By
Theorem 3.1.1 in [22], it then follows that S2 is uniformly persistent with respect to (Y0 , ∂Y0 ). So, the solution
of system (22) is uniformly persistent. It yields that system (22) has at least one periodic solution u∗2 (t, φ∗2 )
with φ∗2 ∈ Y0 . We further claim that u∗2 (t, φ∗2 ) is positive for all t ≥ 0.
Suppose that u∗2 (0, φ∗2 ) = 0. Then, from Eqs. (29)–(34) we have u∗2 (t, φ∗2 ) > 0 for all t > 0. By the
periodicity of the solution, we have u∗2 (0 + nω, φ∗2 ) = u∗2 (nω, φ∗2 ) = u∗2 (0, φ∗2 ) = 0 for all n ≥ 1. That leads
to a contradiction. □

3.4. Analysis of the main model

Now, we use the theory of chain transitive set [22] to lift the threshold type result for system (22) to
system (6).
 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 23

3.4.1. Positivity and boundedness of solutions

Lemma 3.11. For any positive initial condition φ = (φ1 , φ2 ), system (6) has a unique positive bounded
solution u(t, φ) on [0, +∞) with u(0) = φ. Moreover, the closed set ∆ = ∆1 × ∆2 is positively invariant for
system (6).
( )T
Proof . For any φ, we have f (t, φ) = f1 (t, φ1 ), f2 (t, φ2 ) is continuous in (t, φ) and lipschitzian in φ in
each compact of ∆. So, thanks to Theorems 2.2.1 and 2.2.3 in [21], system (6) has a unique solution v(t, φ)
on its maximal interval [0, σφ ) of existence. Since ∆1 and ∆2 are both respectively positively invariant under
(10) and (22), then ∆ is positively invariant for (6). Hence, the solution u(t, φ) is bounded. It then follows
that σφ = +∞. □

3.4.2. Stability of equilibria

If Rv < 1, then the disease-free equilibrium 0, 0, 0, 0, Sh∗ , 0, 0, 0, 0, 0 is globally attractive

( )
Theorem 3.6.
for system (6).

Proof . Let Φ̃(t) the periodic semiflow generated by the periodic system (6) and S the Poincaré map
associated with system (6), namely:

S(φ) = Φ̃(ω)φ = v(ω, φ),

S n (φ) = Φ̃(nω)ϕ = v(nω, φ), ∀n ≥ 0.

Let O be the omega limit set of the discrete-time orbit {Φ̃ n (φ)}n≥0 . Then, from Lemma 1.2.1 in [22], O
is an internally chain transitive set for Φ̃ n on ∆. If Rv < 1, then thanks to Theorem 3.2, we have
( )
lim E(nω, φ), L(nω, φ), P (nω, φ), Nv (nω, φ), Ev (nω, φ), Iv (nω, φ) = (0, 0, 0, 0, 0, 0).
n→∞

Then, there exists O′ ⊂ R4 such that O = {(0, 0, 0, 0, 0, 0)} × O′ . For any x = (xi )1≤i≤n ∈ O, there exists a
sequence nk → ∞ such that u(nk ω, φ) → x as k → ∞. Since,

0 ≤ Sh (nk ω, φ) ≤ Nh∗ , 0 ≤ Eh (nk ω, φ) ≤ Nh∗ ,

0 ≤ Ih (nk ω, φ) ≤ Nh∗ , 0 ≤ Rh (nk ω, φ) ≤ Nh∗ ,

then O′ ⊂ ∆2 . Moreover, it is obvious that

n n
Φ̃|O (0, 0, 0, 0, 0, 0, x5 , x6 , x7 , x8 ) = {(0, 0, 0, 0, 0, 0)} × Ψ|O ′ (x5 , x6 , x7 , x8 )

where {Ψ (t)}t≥0 is the semiflow associated to the following system:

Ṡh (t) = Λh + γRh (t) − dh Sh (t),

⎧
⎪
⎪
⎨ Ė (t) = −(d + α)E (t),
⎪
h h h
(37)
I
⎪ h
⎪ ˙ (t) = αE h (t) − (d h + κ + rh )Ih (t),
⎪
⎩
Ṙh (t) = rh Ih (t) − (dh + γ)Rh (t).

Since O is internally chain transitive set for Φ̃ n , it then follows that O′ is internally chain transitive set for
Ψ̃ n . In addition, from the second equation of system (37), we have:

lim Eh (t) = lim e−(dh +α)t = 0.

t→∞ t→∞
24 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

Thus, we obtain the following system:

I˙h (t) ≤ αEh (t),
{
(38)
Ṙh (t) ≤ rh Ih (t).

Using the comparison theorem, on system (38) we have:

( )
lim Ih (t), Rh (t) = (0, 0).
t→∞

It yields from the first equation of system (37) that limt→∞ Sh (t) = Λd h = Sh∗ . Hence, (Sh∗ , 0, 0, 0, ) is
h
globally attractive for system (37). So, from Theorem 1.2.1 in [22], we have O′ = (Sh∗ , 0, 0, 0, ) and then
O = (0, 0, 0, 0, Sh∗ , 0, 0, 0, 0, 0). □

(H8): Assume that the positive periodic solutions of systems (10) and (22) are globally attractive.

Theorem 3.7. Let (H8) hold. If κ = 0, Rv > 1 and R0 < 1, then the disease-free periodic equilibrium
( ∗
E (t), L∗ (t), P ∗ (t), Nv∗ (t), Sh∗ , 0, 0, 0, 0, 0 is globally attractive for system (6).
)

Proof . If Rv > 1, then thanks to Theorem 3.3, we have

lim E(nω, φ), L(nω, φ), P (nω, φ), Nv (nω, φ) = E ∗ (0), L∗ (0), P ∗ (0), Nv∗ (0) .
( ) ( )
n→∞

Then, there exists O′′ ⊂ R6 such that O = { E ∗ (0), L∗ (0), P ∗ (0), Nv∗ (0) } × O′′ .
( )

For any y = (yi )1≤i≤10 ∈ O, there exists a sequence nl → ∞ such that v(nl ω, φ) → y as l → ∞. Since,

0 ≤ Sh (nl ω, φ) ≤ Nh∗ , 0 ≤ Eh (nl ω, φ) ≤ Nh∗ , 0 ≤ Ih (nl ω, φ) ≤ Nh∗ ,

0 ≤ Rh (nl ω, φ) ≤ Nh∗ , 0 ≤ Ev (nl ω, φ) ≤ Nv∗ (nl ω, φ), 0 ≤ Iv (nl ω, φ) ≤ Nv∗ (nl ω, φ),

then O′′ ⊂ ∆2 . Moreover, let y ′ = (y5 , y6 , y7 , y8 , y9 , y10 ). It is obvious that

n
(E ∗ (0), L∗ (0), P ∗ (0), Nv∗ (0), y ′ ) = E ∗ (0), L∗ (0), P ∗ (0), Nv∗ (0) × Ψ̂|O
n ′
{( )}
Φ̃|O ′′ (y ),

where {Ψ̂ (t)}t≥0 is the semiflow associated to system (22). Hence, from Theorem 3.4, if R0 < 1 and κ = 0
then, the equilibrium W0 is globally attractive. So, from Theorem 1.2.1 in [22], we have O′′ = (Sh∗ , 0, 0, 0, 0, 0)
and then O = (E ∗ (0), L∗ (0), P ∗ (0), Nv∗ (0), Sh∗ , 0, 0, 0, 0, 0). □

Theorem 3.8. Let (H8) hold. If Rv > 1 and R0 > 1, then the endemic periodic equilibrium
( ∗
E (t), L∗ (t), P ∗ (t), Nv∗ (t), Sh∗ (t), Eh∗ (t), Ih∗ (t), Rh∗ (t), Ev∗ (t), Iv∗ (t) is globally attractive for system (6).
)

Proof . If Rv > 1, then thanks to Theorem 3.3, we have

lim E(nω, φ), L(nω, φ), P (nω, φ), Nv (nω, φ) = E ∗ (0), L∗ (0), P ∗ (0), Nv∗ (0) .
( ) ( )
n→∞

Then, there exists T ⊂ R6 such that O = { E ∗ (0), L∗ (0), P ∗ (0), Nv∗ (0) } × T . Thus, from Hirsch et al. [43]
( )

(see Theorem 3.1),

T = Sh∗ (0), Eh∗ (0), Ih∗ (0), Rh∗ (0), Ev∗ (0), Iv∗ (0) or T = (0, 0, 0, 0, 0, 0).
( )

Let us suppose that T = (0, 0, 0, 0, 0, 0). Then, it yields that u2 (t, φ2 ) → 0 as t → ∞. Hence, there exists
a period ω such that for any ϵ∗ > 0 and t ≥ ω,
 E(t), L(t), P (t), Nv (t) − (E ∗ (t), L∗ (t), P ∗ (t), Nv∗ (t)) < ϵ∗ .
( ) 
 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 25

Hence, from system (22) we have

˙ ∗
⎧
⎪ Eh (t) ≥ cvh β(t)(1 − ϵ )Iv (t) − (dh + α)Eh (t),
⎪
⎪ I˙h (t) = αEh (t) − (κ + dh + rh )Ih (t),
⎪
⎪
⎪
⎪
⎨ ˙
⎪
Rh (t) = rh Ih (t) − (dh + γ)Rh (t),
Nv∗ (t)
( )
˙
⎪
Ev (t) ≥ β(t) ∗ chv Ih (t) + c̄hv Rh (t) − (νv + γ4 (t))Ev (t),
⎪
⎪
⎪
⎪
⎪
⎪ Sh
⎪
⎩ ˙
Iv (t) = νv Ev (t) − γ4 (t)Iv (t).

If R0 > 1, then, from Theorem 3.5, system (22) admits a globally attractive fixed point Sh∗ (0), Eh∗ (0),
(

Ih∗ (0), Rh∗ (0), Ev∗ (0), Iv∗ (0) ≫ 0 for all φ2 in Y0 . So, system (22) is uniformly persistent, which leads to a
)

contradiction. It then follows that T = E ∗ (0), L∗ (0), P ∗ (0), Nv∗ (0) . □

( )

To finish this Section, we remark that when all coefficients are constant, system (5) reduces to an
autonomous system. In this case, the vector reproduction ratio Rv and the basic reproduction ratio, R0
read as follows:
bα1 α2 α3
Rv = , (39)
γ (γ + α1 )(γ2 + α2 )(γ3 + α3 )
√4 1
cvh ανv β 2 α3 KP
( )( )
1
R0 = c̄hv rh + chv (dh + γ) 1 − . (40)
Q1 Q2 Rv

with

Q1 = Sh∗ γ4 (νv + γ4 )(dh + γ)(dh + κ + rh )(dh + α),

α1 KE + KL (α2 + γ2 )
Q2 = 1 + (α3 + γ3 ) .
α1 α2 KL KE
It should be noted from equality (40) that R0 exists if and only if Rv > 1. Moreover, it is obvious that
the basic reproduction ratio R0 depends on the vector reproduction ratio Rv . Indeed, larger Rv is, larger
R0 becomes. This result shows the importance to take into account the immature mosquitoes in the model
because this parameter can be used as a control to eliminate the disease.

4. Numerical simulations

In this section, we present a series of numerical simulations in order to support our theoretical results,
to predict the trend of the disease, and to explore some control measures. We use the MATLAB technical
computing software with the fourth-order Runge–Kutta method to perform our numerical results.

4.1. Estimation of the parameters

We suppose that the life expectancy of humans for Burkina Faso in 2011 was 55 years. Thus, the human
natural death rate dh can be calculated as follows:
1
dh = = 0.00152 per month.
12 × 55
In addition, in Burkina Faso, the total size of human population in 2011 was 16, 248, 558, then, the
recruitment rate Λh is determined by

Λh = dh × 16, 248, 558 = 24, 698 humans per month.

26 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

Table 3
Values for constant parameters for malaria model.
Parameters Values Sources Dimensions
Λh 24,698 See text /month
dh 0.00152 See text /month
dp 0.0028 [17] /month
α 3.04 [17] /month
rh 0.0833 [17] /month
γ 0.0146 [17] /month
νv 2.523 [17] /month
cvh 0.022 [9] –
chv 0.48 [9] –
c̄hv 0.048 [9] –
KE 8 000 000 [25] –
KL 6 000 000 [25] –
KP 5 500 000 [25] –

Table 4
◦
Monthly mean temperature of Burkina Faso (in C).
Month January February March April May June
Temperature 25.8 28.77 31.11 30.75 29.54 27.50
Month July August September October November December
Temperature 25.95 25.04 25.57 27.32 28.33 25.36

Further, values of some constant parameters for malaria transmission model (6) are listed in Table 3 with
the references therein. Now, we estimate the periodic coefficients of the model. Thus, using the reported
monthly mean temperature, for ASECNA in Burkina Faso, from January 2011 to December 2015, we can
calculate the monthly mean temperature of Burkina Faso in Table 4.
Moreover, assuming that the average number of mosquito bites depends on their gonotrophic cycle which
is also a function of temperature θ, then, the temperature-dependent biting rate of mosquitoes reads as
follows [18]: √
β(θ) = 0.00609T (θ − 11.7) 42.3 − θ per month.
Similarly, the temperature-dependent death rate of adult mosquitoes and larvae reads respectively as
follows [17]:
( )
5−θ
γ4 (θ) = 3 + 29.564 exp per month,
2.7035
30
γ2 (θ) = per month.
−4.4 + 1.31θ − 0.03θ2
By considering that the egg-laying rate is proportional to the biting rate, eggs and pupae death rate are
proportional to the death rate of larvae, then we have:

b(T ) = 2.5β(θ), γ1 (θ) = 0.5γ2 (θ) and γ3 (θ) = 0.75γ2 (θ).

Similarly, we have:
α1 (θ) = 0.95b(θ), α2 (θ) = 0.5α1 (θ) and α3 (θ) = 0.8α2 (θ).
Furthermore, assuming that temperature varies as a function of time, then we use the CFTOOL of
MATLAB to get the best estimation of periodic functions β(t), γ4 (t), γ2 (t) of Burkina Faso as follows:
3 [ ( ) ( )]
∑ nπt nπt
β(t) = a0 + an sin + ãn cos per month
n=1
6 6

with

a0 = 10.16, a1 = 1.289, a2 = −0.06678, a3 = 0.3301,

 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 27

ã1 = 0.3614, ã2 = −1.097, ã3 = −0.4723.

3 [ ( ) ( )]
∑ nπt nπt
γ2 (t) = b0 + bn sin + b̃n cos per month
n=1
6 6
with

b0 = 3.443, b1 = 0.3287, b2 = 0.03792, b3 = −0.004983,

b̃1 = 0.08803, b̃2 = −0.2627, b̃3 = −0.1211.
3 [ ( ) ( )]
∑ nπt nπt
γ4 (t) = c0 + cn sin + c̃n cos per month
n=1
6 6
with

c0 = 3.008, c1 = −0.004631, c2 = 0.0009815, c3 = −0.0026,

c̃1 = −0.001408, c̃2 = 0.004167, c̃3 = 0.001817.

4.2. Numerical results

We use the values of Table 3 and the initial conditions: E(0) = 600, 000, L(0) = 300, 000, P (0) =
200, 000, Nv (0) = 24, 000, Sh (0) = 15, 000, 000, Eh (0) = 10, 000, Ih (0) = 50, 000, Rh (0) = 1, 188, 558,
Ev (0) = 10, 000, Iv (0) = 5, 000 to get the following results: Figs. 4–7.
Computing the two thresholds dynamics of the model, we get Rv = 4.8413 and R0 = 1.0364. Through
Fig. 4, we remark that mosquitoes and malaria persist. In addition systems (10) and (22) admit respectively
positive periodic solutions (E ∗ (t), L∗ (t), P ∗ (t), Nv∗ (t)) and (Sh∗ (t), Eh∗ (t), Ih∗ (t), Rh∗ (t), Ev∗ (t), Iv∗ (t)) which are
globally asymptotically stable. That observation illustrates the results of our Theorems 3.3 and 3.5.
Since the death rate induced by malaria in the country is very high, the government of Burkina Faso has
decided to introduce some measures of control in order to slow down the disease evolution. These control
measures concern three major points: vector control, prevention and treatment. Indeed, the vector control
consists in reducing the breeding sites of eggs, larvae and pupae KE , KL , Kp , respectively in addition to the
use of insecticides against adult mosquitoes. Concerning the prevention, it consists in avoiding the biting
of mosquitoes β(t) by using bed nets. Besides, the health authorities have made available to the infectious
populations some drugs to treat malaria. Therefore, we will study the effectiveness of prevention and vector
control in the eradication of malaria.
Firstly, we examine the impact of vector control on the transmission. Let us assume that 25% of eggs
breeding sites KE , 34% of larvae breeding sites KL and 37% of pupae breeding sites KP have been destroyed
by human populations through environmental sanitations. Then, we have the following results: Fig. 5.
Computing the vector reproduction ratio and the basic reproduction ratio, we obtain Rv = 4.8413
and R0 = 0.8465. We remark that despite the persistence of mosquitoes population (see Fig. 5(a)), the
disease will die out to both populations (see Fig. 5((c)–(f))). Furthermore, system (6) converges to the
periodic disease-free equilibrium E ∗ (t), L∗ (t), P ∗ (t), Nv∗ (t), Sh∗ , 0, 0, 0, 0, 0 which is globally attractive. That
( )

illustrates the result of our Theorem 3.7.

Now, let us replace the vector control by the prevention one. Thus, we assume that humans use bed nets
to avoid the biting of mosquitoes. Hence, if the use of bed nets allows to reduce the biting rate to 25% then
we obtain the following results: Fig. 6.
Computing the two thresholds dynamics of the model, we get Rv = 3.0907 and R0 = 0.7612. We note that
with a contact reduction rate of 25%, malaria will disappear from the country in the next thirty years (see
Fig. 6((c)–(f))). Thus, increasing this control would be a very effective means for a short-term eradication of
28 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

Fig. 4. Global behavior of system (6) for Rv > 1 and R0 > 1.

 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 29

Fig. 5. Global behavior of system (6) for KE = 6000 000, KL = 4000 000, KP = 3500 000, Rv > 1 and R0 < 1.

malaria in Burkina Faso. As a result, health authorities should be more involved in mass use of bed nets by
populations. However, in practice, the financial cost of this control is very high for the country. Therefore,
it would be more appropriate to combine the two types of control in order to obtain a more optimal result.
Computing the vector reproduction ratio, we get Rv = 0.9551. Thus, when we reduce the contact rate
by 61% and the larval sites by 50%, we notice that in less than 3 years the mosquitoes disappear from
the country (see Fig. 7((a)–(c)-(d)). Since, Rv < 1, then system (6) converges globally to the disease-free
equilibrium (0, 0, 0, 0, Sh∗ , 0, 0, 0, 0, 0). That illustrates our Theorem 3.6.

5. Conclusion

An important issue in developing mathematical models is to identify which biological factors are necessary
to include and which ones can be omitted. Thus, considering the impact of climate change on the mosquito
30 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

Fig. 6. Global behavior of system (6) for Rv > 1 and R0 < 1.

life cycle, we have formulated a deterministic mathematical model of malaria transmission by incorporating
seasonality. The vector population has been divided into juvenile stage and adult stage. This structure
enabled us to better understand the dynamics of mosquito population and malaria transmission dynamics.
In addition, taking into account the juvenile stage offers many advantages in the control of the disease
transmission. Two thresholds dynamics have been determined for the model: the vector reproduction ratio
Rv and the basic ratio R0 and it emerges from our analysis that the global behavior of the model depends
on those thresholds. Hence, we have shown that if:

(i) Rv < 1, mosquitoes disappear.

(ii) Rv > 1, and R0 < 1, mosquitoes persist but the disease dies out.
(iii) Rv > 1, and R0 > 1 mosquitoes and disease persist with seasonal variation.
 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081 31

Fig. 7. Global behavior of system (6) for KE = 4000 000, KL = 3000 000, KP = 2750 000 and Rv = 0.9551.

Using the monthly mean temperature of Burkina Faso and the formula related to mosquito life cycle,
we estimated the periodic coefficients of the model and then verified our theoretical results by numerical
simulations. Our numerical results indicated that there exist two important parameters which permit to
control malaria transmission in the country. The first control is the reduction of the periodic biting rate β(t)
and the second control concerns the reduction of carrying capacities of immature mosquitoes KE , KL and
KP . Indeed, if we reduce the biting rate to 25%, mosquitoes will persist but the disease will die out in the long
run. That observation is the same if we reduce eggs, larvae and pupae breeding sites respectively to 25%, 34%
and 37%. We remark that the reduction of carrying capacities has a great impact on the disease transmission.
First, it reduces the transfer rates of immature stages and increases their death rates, because if there is no
water, eggs cannot hatch. Furthermore, we showed that combining the two controls is more efficient and
more optimal in the fight against malaria transmission. Following the previous remarks, the eradication of
the disease can be achieved if the mosquito population is eradicated or if the basic reproduction ratio is less
than one. However, even if there is no malaria epidemic, we need to be vigilant because climate change can
lead to the re-emergence of malaria in some European and American countries.
In our model, we neglected the effects of climate on the mosquitoes breeding sites. However, it must be
noticed that these parameters depend on the climate profile. So, it would be more interesting to consider
them as functions of time. In addition, due to the complexity of ours systems, we have not established the
32 B. Traoré, O. Koutou and B. Sangaré / Nonlinear Analysis: Real World Applications 53 (2020) 103081

global stability of the positive periodic solution (see hypothesis (H8)), nevertheless, numerical simulations
indicate it clearly. As a future work we will investigate this open problem.

Acknowledgments

The authors are grateful to the editor and the anonymous referees for their insightful comments and
suggestions which contributed to improve the original version of the manuscript.
This work has been prepared with the support of the Department of Mathematics, Nazi BONI University.

Disclosure

The authors declare that there is no conflict of interest regarding the publication of this paper.

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