Mycobacterium ulcerans is an emerging environmental pathogen which causes chronic skin ulcers (i.e., Buruli ulcer) in otherwise healthy humans living in tropical countries, particularly those in Africa. In spite of epidemiological and PCR data linking M. ulcerans to water, the mode of transmission of this organism remains elusive. To determine the role of aquatic insects in the transmission of M. ulcerans, we have set up an experimental model with aquariums that mimic aquatic microenvironments. We report that M. ulcerans may be transmitted to laboratory mice by the bite of aquatic bugs (Naucoridae) that are infected with this organism. In addition, M. ulcerans appears to be localized exclusively within salivary glands of these insects, where it can both survive and multiply without causing any observable damage in the insect tissues. Subsequently, we isolated M. ulcerans from wild aquatic insects collected from a zone in the Daloa region of Ivory Coast where Buruli ulcer is endemic. Taken together, these results point to aquatic insects as a possible vector of M. ulcerans.
Mycobacterium ulcerans disease is common in some humid tropical areas, particularly in parts of West Africa, and current management is by surgical excision of skin lesions ranging from early nodules to extensive ulcers (Buruli ulcer). Antibiotic therapy would be more accessible to patients in areas of Buruli ulcer endemicity. We report a study of the efficacy of antibiotics in converting early lesions (nodules and plaques) from culture positive to culture negative. Lesions were excised either immediately or after treatment with rifampin orally at 10 mg/kg of body weight and streptomycin intramuscularly at 15 mg/kg of body weight daily for 2, 4, 8, or 12 weeks and examined by quantitative bacterial culture, PCR, and histopathology for M. ulcerans. Lesions were measured during treatment. Five lesions excised without antibiotic treatment and five lesions treated with antibiotics for 2 weeks were culture positive, whereas three lesions treated for 4 weeks, five treated for 8 weeks, and three treated for 12 weeks were culture negative. No lesions became enlarged during antibiotic treatment, and most became smaller. Treatment with rifampin and streptomycin for 4 weeks or more inhibited growth of M. ulcerans in human tissue, and it provides a basis for proceeding to a trial of antibiotic therapy as an alternative to surgery for early M. ulcerans disease.
Mycobacterium ulcerans is the causative agent of Buruli ulcer, one of the most common mycobacterial diseases of humans. Recent studies have implicated aquatic insects in the transmission of this pathogen, but the contributions of other elements of the environment remain largely unknown. We report here that crude extracts from two green algae added to the BACTEC 7H12B culture medium halved the doubling time of M. ulcerans and promoted biofilm formation. Using the 7H12B medium, modified by the addition of the algal extract, and immunomagnetic separation, we also demonstrate that M. ulcerans is associated with aquatic plants in an area of the Ivory Coast where Buruli ulcer is endemic. Genotype analysis showed that plant-associated M. ulcerans had the same profile as isolates recovered in the same region from both aquatic insects and clinical specimens. These observations implicate aquatic plants as a reservoir of M. ulcerans and add a new potential link in the chain of transmission of M. ulcerans to humans.Mycobacterium ulcerans is an emerging environmental pathogen (2). It is the etiologic agent of Buruli ulcer, a necrotic skin disease highly prevalent in many countries throughout west Africa and one of the most common mycobacterial diseases in humans after tuberculosis and leprosy (2). M. ulcerans is the only mycobacterium known to produce a toxin, a polyketide-derived macrolide called mycolactone (10, 11). The infection begins with a painless nodule or papule that spreads over the surrounding tissue. Ischemic and necrotized tissue disappears and is replaced by centralized ulceration of the limb. At present, the only effective treatment consists of excision of the lesions, and this is often followed by extensive skin grafting (6).Until very recently M. ulcerans had never been isolated in culture from the environment. Indirect evidence from epidemiological studies suggests that M. ulcerans is an environmental mycobacterium present in swampy areas. Humans are thought to be infected through minor wounds or skin abrasions via contact with mycobacterium-containing water (33). In a previous study we demonstrated that aquatic insects are a possible mode of transmission of M. ulcerans to humans. We showed that, in an experimental mouse model, aquatic insects (Naucoridae) were able to transmit an infection by biting, thereby inoculating bacilli that had accumulated in the salivary glands of the insects (16). We were then able to isolate in pure culture M. ulcerans from the salivary glands of Naucoridae captured in a region of endemicity in the Ivory Coast. However it seems unlikely that these insects are the only environmental source of M. ulcerans. In another recent study, data gathered using an M. ulcerans-specific PCR to survey environments of endemicity in southeastern Australia identified aquatic plants as a possible reservoir of this pathogen (30).In this report, we test the hypothesis that M. ulcerans is associated with aquatic plants by studying the effects of crude aquatic plant extracts on the growth of M. ulcer...
Mycobacterium ulcerans was first identified as the causative agent of Buruli ulcer; this cutaneous tissue-destructive process represents the third most important mycobacterial disease in humans after tuberculosis and leprosy. More recently other life traits were documented. M. ulcerans is mainly detected in humid tropical zones as part of a complex ecosystem comprising algae, aquatic insect predators of the genus Naucoris, and very likely their vegetarian preys. Coelomic plasmatocytes could be the first cells of Naucoris cimicoides to be involved in the infection process, acting as shuttle cells that deliver M. ulcerans to the salivary glands as suggested by both in vitro and in vivo approaches. Furthermore, a key element for the early and long-term establishment of M. ulcerans in Naucoridae is demonstrated by the fact that only mycolactone toxin-producing M. ulcerans isolates are able to invade the salivary glands, a site where they proliferate. Later, the raptorial legs of Naucoris are covered by M. ulcerans-containing material that displays features of biofilms.
Accumulative indirect evidence of the epidemiology of Mycobacterium ulcerans infections causing chronic skin ulcers (i.e., Buruli ulcer disease) suggests that the development of this pathogen and its transmission to humans are related predominantly to aquatic environments. We report that snails could transitorily harbor M. ulcerans without offering favorable conditions for its growth and replication. A novel intermediate link in the transmission chain of M. ulcerans becomes likely with predator aquatic insects in addition to phytophage insects. Water bugs, such as Naucoris cimicoides, a potential vector of M. ulcerans, were shown to be infected specifically by this bacterium after feeding on snails experimentally exposed to M. ulcerans.Mycobacterium ulcerans is the causative agent of Buruli ulcer, one of the most common mycobacterial diseases of humans. This environmental mycobacterium has been found in swampy and wetland habitats that are home to aquatic insects implicated in the transmission of this pathogen (3-7, 10). Recently, Marsollier et al. found that certain aquatic macrophytes stimulated the growth of M. ulcerans and that the bacterium had a strong tendency to form biofilms on the plants' surfaces (2). In this report, we demonstrate the following results: (i) a few aquatic snails may harbor M. ulcerans after consuming aquatic macrophytes where an M. ulcerans biofilm has developed, (ii) no mycobacterial growth was detected in aquatic snails, so they may be a passive host, and (iii) after having eaten experimentally infected snails, the salivary glands of biting naucorid water bugs were found to contain M. ulcerans.Experimental infection of snails. Tropical aquatic Pomacea canaliculata (Ampullariidae) and Planorbis planorbis (Planorbidae) snails 0.5 to 0.8 cm in total shell length were housed in an aquarium with water at a temperature of 28°C without aquatic vegetation and starved for 10 days. For a 24-h period, 30 snails were placed in additional aquaria containing aquatic vegetation covered by an M. ulcerans biofilm (strain number 1G897, isolated from a skin biopsy sample from a patient from French Guiana [1]) as previously described (2). The presence of an M. ulcerans biofilm on aquatic plants was confirmed by scanning electron microscopy (2). The number of acid-fast bacilli (AFB) on aquatic plants was evaluated by the method described by Shepard and Rae (9) at 10 6 bacilli/g of plant tissue. After this period, the snails were removed and placed in a noncontaminated aquarium without mycobacteria. At different intervals, four snails were sacrificed, the shells were removed, and the individual tissues were ground and homogenized. A PCR was performed for the detection of M. ulcerans as previously described (3,8). The AFB were counted and cultured with the methods described by Marsollier et al. (3). During the 72 h after feeding on vegetation-bound M. ulcerans cells, viable bacilli were found in the feces of the snails. Within the first 10 days of the experiment, a slight but nonsignificant increase in AF...
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