On the Transmission Dynamics of Buruli Ulcer in Ghana: Insights Through a Mathematical Model Farai Nyabadza1 and Ebenezer Bonyah2*

On the Transmission Dynamics of Buruli Ulcer in Ghana: Insights Through a Mathematical Model Farai Nyabadza1 and Ebenezer Bonyah2*

Nyabadza and Bonyah BMC Res Notes (2015) 8:656 DOI 10.1186/s13104-015-1619-5 RESEARCH ARTICLE Open Access On the transmission dynamics of Buruli ulcer in Ghana: Insights through a mathematical model Farai Nyabadza1 and Ebenezer Bonyah2* Abstract Background: Mycobacterium ulcerans is know to cause the Buruli ulcer. The association between the ulcer and environmental exposure has been documented. However, the epidemiology of the ulcer is not well understood. A hypothesised transmission involves humans being bitten by the water bugs that prey on mollusks, snails and young fishes. Methods: In this paper, a model for the transmission of Mycobacterium ulcerans to humans in the presence of a pre- ventive strategy is proposed and analysed. The model equilibria are determined and conditions for the existence of the equilibria established. The model analysis is carried out in terms of the reproduction number R0. The disease free equilibrium is found to be locally asymptotically stable for R0 < 1. The model is fitted to data from Ghana. Results: The model is found to exhibit a backward bifurcation and the endemic equilibrium point is globally stable when R0 > 1. Sensitivity analysis showed that the Buruli ulcer epidemic is highly influenced by the shedding and clearance rates of Mycobacterium ulcerans in the environment. The model is found to fit reasonably well to data from Ghana and projections on the future of the Buruli ulcer epidemic are also made. Conclusions: The model reasonably fitted data from Ghana. The fitting process showed data that appeared to have reached a steady state and projections showed that the epidemic levels will remain the same for the projected time. The implications of the results to policy and future management of the disease are discussed. Keywords: Buruli ulcer, Transmission dynamics, Basic reproduction number, Sensitivity analysis, Stability Background This disease has dramatically emerged in several west Buruli ulcer is caused by pathogenic bacterium where African countries, such as Ghana, Cote d’Ivoire, Benin, infection often leads to extensive destruction of skin and and Togo in recent years [26]. soft tissue through the formation of large ulcers usu- The transmission mode of the ulcer is not well under- ally on the legs or arms [28]. It is a devastating disease stood, however residence near an aquatic environment caused by Mycobacterium ulcerans. The ulcer is fast has been identified as a risk factor for the ulcer in Africa becoming a debilitating affliction in many countries [3]. [6, 16, 25]. Transmission is thus likely to occur through It is named after a region called Buruli, near the Nile contact with the environment [20]. Recent studies in West River in Uganda, where in 1961 the first large number of Africa have implicated aquatic bugs as transmission vec- cases was reported. In Africa, close to 30,000 cases were tors for the ulcer [18, 24]. An attractive hypothesis for a reported between 2005 and 2010 [29]. Cote d’Ivoire, with possible mode of transmission to humans was proposed the highest incidence, reported 2533 cases in 2010 [27]. by Portaels et al. [22]: water-filtering hosts (fish, mollusks) concentrate the Mycobacterium ulcerans bacteria present *Correspondence: [email protected] in water or mud and discharge them again to this environ- 2 Department of Mathematics and Statistics, Kumasi Polytechnic, P. O. ment, where they are then ingested by aquatic predators Box 854, Kumasi, Ghana Full list of author information is available at the end of the article such as beetles and water bugs. These insects, in turn, © 2015 Nyabadza and Bonyah. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons. org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Nyabadza and Bonyah BMC Res Notes (2015) 8:656 Page 2 of 15 may transmit the disease to humans by biting [18]. Per- model. We also determine the steady states and ana- son to person transmission is less likely. Aquatic bugs are lysed their stability. The results of this paper are given in insects found throughout temperate and tropical envi- “Results”. Parameter estimation, sensitivity analysis and ronments with abundant freshwater. They prey, accord- the numerical results on the behavior of the model are ing to their size, on mollusks, snails, young fishes, and also presented in this section. The paper is concluded in the adults and larvae of other insects that they capture “Discussion”. with their raptorial front legs and bite with their rostrum. These insects can inflict painful bites on humans as well. Methods In Ghana, where Buruli ulcer is endemic, the water bugs Model formulation are present in swamps and rivers, where human activities We consider a constant human population NH (t), the such as farming, fishing, and bathing take place [18]. vector population of water bugs NV (t) and the fish pop- Research on Buruli ulcer has focused mainly on the ulation NF (t) at any time t. The total human population socio-cultural aspects of the disease. The research recom- is divided into three epidemiological subclasses of those mends the need for Information, Education and Commu- that are susceptible SH (t), the infected IH (t) and the nication (IEC) intervention strategies, to encourage early recovered who are still immune RH (t). Total population case detection and treatment with the assumption that of vector (water bug) at any time t is divided into two sub- once people gain knowledge they will take the appropri- classes to susceptible water bugs SV (t) and those that are ate action to access treatment early [2]. IEC is defined as infectious and can transmit the Buruli ulcer to humans, an approach which attempts to change or reinforce a set IV (t). The total population reservoir of small fish is also of behaviours to a targeted group regarding a problem. divided into two compartments of susceptible fishS F (t) The IEC strategy is preventive in that it has a potential of and infected fish IF (t). We also consider the role of the enhancing control of the ulcer [5]. It is also important to environment by introducing a compartment U, repre- note that Buruli ulcer is treatable with antibiotics. A com- senting the density of Mycobacterium ulcerans in the bination of rifampin and streptomycin administered daily environment. We make the following basic assumptions: for 8 weeks has the potential to eliminate Mycobacterium ulcerans bacilli and promote healing without relapse. • Mycobacterium ulcerans are transferred only from Mathematical models have been used to model the vector ( water bug) to the humans. transmission of many diseases globally. Many advances in • There is homogeneity of human, water bug and fish the management of diseases have been born from math- populations’ interactions. ematical modeling [11, 12, 14, 15]. Mathematical models • Infected humans recover and are temporarily can evaluate actual or potential control measures in the immune, but lose immunity. absence of experiments, see for instance [19]. To the best • Fish are preyed on by the water bugs. of our knowledge very few mathematical models have • Unlike some bacterial infections such as leprosy been formulated to analyse the transmission dynamics (caused by Mycobacterium leprae) and tuberculosis of Mycobacterium ulcerans. This could be largely due to (caused by Mycobacterium tuberculosis), which are the elusive epidemiology of the Buruli ulcer. Aidoo and characterized by person-to-person contact transmis- Osei [3] proposed a mathematical model of the SIR-type sion, it is hypothesized that Mycobacterium ulcerans in an endeavour to explain the transmission of Myco- is acquired through environmental contact and direct bacterium ulcerans and its dependence on arsenic. In person-to-person transmission is rare [20]. this paper, we propose a model which takes into account • Susceptible host (human population) can be infected the human population, water bugs as vectors and fish as through biting by an infectious vector (water bug). potential reservoirs of Mycobacterium ulcerans follow- We represent the effective biting rate that an infec- ing the transmission dynamics described in [8]. In addi- tious vector has to susceptible host as βH and tion we include the preventive control measures in a bid the incidence of new infections transmitted by to capture the IEC strategy. Our main aim is to study the water bugs is expressed by standard incidence rate dynamics of the Buruli ulcer in the presence of a preven- SH IV βH . One can interpret βH as a function of tive control strategy, while emphasizing the role of the NH vector (water bugs) and fish and their interaction with the biting frequency of the infected water bugs on the environment. The model is then validated using data humans, density of infectious water bugs per human, from Ghana. This is crucial in informing policy and sug- the probability that a bite will result in an infection gesting strategies for the control of the disease. and the efficacy of the IEC strategy. In particular we This paper is arranged as follows; in “Methods”, we βH (1 ǫ)τ αβ , ǫ (0, 1) can set = − H∗ where ∈ is the formulate and establish the basic properties of the efficacy of the IEC strategy,τ the number of water Nyabadza and Bonyah BMC Res Notes (2015) 8:656 Page 3 of 15 bugs per human host, α the biting frequency (the bit- New susceptibles enter the population at a rate of ing rate of humans by a single water bug) and βH∗ the µH NH .

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