Aquatic Invertebrates as Unlikely Vectors of Buruli Ulcer Disease

Abstract

Buruli ulcer is a necrotizing skin disease caused by Mycobacterium ulcerans and associated with exposure to aquatic habitats. To assess possible transmission of M. ulcerans by aquatic biting insects, we conducted a fi eld examination of biting water bugs (Hemiptera: Naucoridae, Belostomatidae, Nepidae) in 15 disease-endemic and 12 non-disease-endemic areas of Ghana, Africa. From collections of 22,832 invertebrates, we compared composition, abundance, and associated M. ulcerans positivity among sites. Biting hemipterans were rare and represented a small percentage (usually <2%) of invertebrate communities. No signifi cant differences were found in hemipteran abundance or pathogen positivity between disease-endemic and nondisease-endemic sites, and between abundance of biting hemipterans and M. ulcerans positivity. Therefore, although infection through insect bites is possible, little fi eld evidence supports the assumption that biting hemipterans are primary vectors of M. ulcerans. M ycobacterium ulcerans infection is an emerging skin disease often called Buruli ulcer (BU). Infection results in illness and lasting negative socioeconomic effects in rural areas of the tropics and subtropics (1). The pathologic changes, clinical signs and symptoms, and treatment have been reviewed elsewhere (2-5). In this article we evaluate fi eld evidence for the potential of aquatic invertebrates to be vectors of M. ulcerans.The exact mode of BU transmission remains unknown; however, past epidemiologic studies have associated BU with human activity near, or within, slow-fl owing or standing water bodies that have been created or disturbed by humans (2-4). Although several water-related risk factors have been recognized, none has been consistently reported, making it diffi cult to identify specifi c water-related risk activities (6-8). Most studies suggest that infection occurs through inoculation of M. ulcerans into skin lesions or insect bites (2,4,9-11). Portaels et al. (11) were the fi rst to propose that aquatic insects might serve as vectors of M. ulcerans. This hypothesis maintains that M. ulcerans is found in biofi lms of aquatic habitats and concentrated by grazing or fi lter-feeding invertebrates that are then consumed by predators known to bite humans (11). Initial evidence for this hypothesis used PCR detection of the insertion sequence IS2404 to document M. ulcerans' association with biting water bugs (Hemiptera), fi ltered concentrates of water, detritus, and aquatic plants (4,(12)(13)(14). These studies were important for understanding the possible environmental reservoirs of M. ulcerans. However, IS2404 is now understood to be not specifi c for M. ulcerans because this insertion sequence has been found in a number of other aquatic mycobacterial species, including M. marinum (15)(16)(17). When more discriminatory methods based on detection of variable number tandem repeats were used, many IS2404-positive environmental samples were reported to lack M. ulcerans (18). In light of these recent fi ndings, the relative fr...

Persistent Association of Mycobacterium ulcerans with West African Predaceous Insects of the Family Belostomatidae

“…The hypothesis that M. ulcerans is a vectored pathogen which is transmitted to humans via the bite of predaceous water bugs has received considerable attention (2,13,17,24). The interpretation of the data presented in earlier studies has been complicated by the following three major issues: (i) the insect species used were not African species, (ii) the primary M. ulcerans used was not representative of the classical M. ulcerans from Africa, and (iii) none of the studies have provided comprehensive quantitative data on the location of the bacterium within the insect.…”

“…A major breakthrough occurred with the successful culture of M. ulcerans from a water strider (Gerridae) collected in Benin by Francoise Portaels et al (22). None of the predaceous hempitera that were found to have positive PCR results for M. ulcerans DNA in Africa are hematophagous, and the percentage of biting hemiptera is often quite low in areas where the disease is endemic (2).…”

Landscape Fragmentation as a Risk Factor for Buruli Ulcer Disease in Ghana

“…11 Though its transmission mode is still unclear, it is generally recognized to be associated with aquatic habitats 11 and aquatic biting insects 12 as well as nonbiting aquatic invertebrates 11 although results are equivocal. 13 Other landscape disturbances, such as deforestation and agriculture, have also been linked to BU prevalence. In Benin, the dynamics of BU disease were correlated with human alterations to landscapes and natural land cover.…”

Correlation between Buruli Ulcer and Vector-borne Notifiable Diseases, Victoria, Australia

“…Since the 1980s, BU has emerged as a major public health problem in rural West and Central Africa (1), where some researchers have suggested a role for aquatic insects as either reservoirs or vectors of M. ulcerans (2,3). However, this hypothesis remains unproven (4).…”