Ecological niche modelling of Hemipteran insects in Cameroon; the paradox of a vector-borne transmission for Mycobacterium ulcerans, the causative agent of Buruli ulcer

Abstract

BackgroundThe mode of transmission of the emerging neglected disease Buruli ulcer is unknown. Several potential transmission pathways have been proposed, such as amoebae, or transmission through food webs. Several lines of evidence have suggested that biting aquatic insects, Naucoridae and Belostomatidae, may act as vectors, however this proposal remains controversial.Materials and methodsHerein, based on sampling in Cameroon, we construct an ecological niche model of these insects to describe their spatial distribution. We predict their distribution across West Africa, describe important environmental drivers of their abundance, and examine the correlation between their abundance and Buruli ulcer prevalence in the context of the Bradford-Hill guidelines.ResultsWe find a significant positive correlation between the abundance of the insects and the prevalence of Buruli ulcer. This correlation changes in space and time, it is significant in one Camerounese study region in (Akonolinga) and not other (Bankim). We discuss notable environmental differences between these regions.ConclusionWe interpret the presence of, and change in, this correlation as evidence (though not proof) that these insects may be locally important in the environmental persistence, or transmission, of Mycobacterium. ulcerans. This is consistent with the idea of M. ulcerans as a pathogen transmitted by multiple modes of infection, the importance of any one pathway changing from region to region, depending on the local environmental conditions.

Modelling the spatial distribution of aquatic insects (Order Hemiptera) potentially involved in the transmission of Mycobacterium ulcerans in Africa

“…There is a lack of previous contributions exploring distribution patterns of aquatic hemipteran insects and their association with large-scale environmental and climate related factors. The few that have been carried out, aligned with our findings, indicated a preference of the four biting hemipteran families studied here for transformed ecosystems such as agricultural landscapes and rural settlements over forest or grasslands [ 24 ]. Although this suggests that land cover type influences hemipteran distribution patterns, it has previously been argued that due to the migration and dispersal abilities of this insect group, the land use in wide-scale terms may not actually limit its distribution in practice [ 64 ].…”

“…Insect vector-borne diseases commonly have a more restricted range than the organisms that carry them because transmission also relies on the presence of the infectious agent in the environment, which is influenced by many other biotic and abiotic factors [ 54 ]. A recent work has presented a model of the potential distribution of the Naucoridae and Belotomatidae insects in Cameroon based on a set of six environmental variables and records of presence of these insects in 36 sample sites across the country [ 24 ]. The authors also found a positive correlation between the environmental suitability for the presence of Naucoridae and Belostomatidae insects and BU prevalence, although they restrained from making any causative assumption.…”

“…Some previous contributions have defined particular ecological traits for these hemipteran families which may be related to the observed differences in their distributions [ 24 , 72 ]. Gerridae and Nepidae seemed to be the least tolerant families, as deduced by the lower global tolerance index from the results of the ENFA analysis (Table 4 ).…”

“…Furthermore, experimentally infected species of the Naucoridae have been shown to be capable of transmitting M. ulcerans to a mouse model, which subsequently developed pathological signs consistent with Buruli ulcer [ 23 ]. Recent modelling work has also suggested a positive association between environmental suitability for insects of the Naucoridae and Belostomatidae and BU prevalence in Cameroon [ 24 ].…”

Chemistry of natural waters and its relation to Buruli ulcer in Ghana

“…While the culturing of M. ulcerans from an aquatic invertebrate (Portaels et al, 2008) suggested a potential reservoir or vector for BU (e.g., Merritt et al, 2010), Benbow et al (2008) discounted predatory aquatic insects as a potential vector because the number of insects and presence of M. ulcerans in these insects are similar at BU-endemic and non-endemic sites. However, more recent work indicates that perhaps aquatic biting insects are indeed the cause, as suggested by correlations between biting insect distribution and prevalence of BU (Carolan et al, 2014a) and, more directly, one case study of a six-year old girl (Marion et al, 2014).…”