Environmental Distribution and Seasonal Prevalence of Mycobacterium ulcerans in Southern Louisiana

Abstract

dMycobacterium ulcerans is an emerging environmental pathogen that causes debilitating, ulcerative disease in humans and other vertebrates. The majority of human cases occur in tropical and temperate regions of Africa and Australia, and outbreaks of piscine mycobacteriosis caused by M. ulcerans have been reported in disparate geographic locations spanning the globe. While exposure to a natural body of water is the most common risk factor for human infection, the environmental distribution of M. ulcerans in aquatic habitats has not been extensively studied. Although no human cases have been reported in the United States, a strain of M. ulcerans has been identified as the cause of a piscine mycobacteriosis in Striped bass (Morone saxatilis) within the Chesapeake Bay. Infected fish exhibit bright red ventral and lateral dermal lesions. We observed a possible outbreak causing similar lesions on red drum (Sciaenops ocellatus) in wetlands of southern Louisiana and detected M. ulcerans-specific genetic markers in lesion samples from these fish. Based on these findings, we studied the geographic and seasonal prevalence of these markers across southern Louisiana. M. ulcerans was detected in each of the nine areas sampled across the state. M. ulcerans prevalence was significantly lower in the fall samples, and the low prevalence coincided with decreased nutrient levels and an increase in water temperature. To our knowledge, this is the first study of M. ulcerans biomarkers in the southern United States. Mycobacterium ulcerans is a pathogenic, toxin-producing bacterium that is the causative agent of Buruli ulcer (BU), a necrotizing skin infection in humans. Although the causative agent was discovered in the mid-1900s, BU remained a largely neglected tropical disease until the World Health Organization (WHO) established the Global Buruli Ulcer Initiative (GBUI) in 1998. M. ulcerans is currently recognized as a rapidly emerging pathogen. BU is endemic in 33 countries, with the highest number of cases occurring in tropical and subtropical regions of west and sub-Saharan Africa and Australia (1). In addition to human cases, M. ulcerans is responsible for disease in a wide range of other host species, including domestic and wild mammals (2-6), reptiles (7), amphibians (8), and fish (9, 10). Strains of M. ulcerans have increasingly been identified as the cause of piscine mycobacteriosis occurring in locations across the globe (9), including Israel (11), Europe (10,12), and the northeastern United States (13,14).Fundamental aspects of the ecology and epidemiology of M. ulcerans, including its environmental distribution, niche, host range, and mode of transmission and infection, are incompletely understood. The most definitive risk factor for BU is frequent contact with natural aquatic systems (15). This risk has been substantiated by studies that have shown that M. ulcerans is detected by PCR in samples collected from slow-flowing or stagnant bodies of water in areas with an incidence of BU (1). Within these aquatic environments,...

Buruli Ulcer, a Prototype for Ecosystem-Related Infection, Caused by Mycobacterium ulcerans

“…In French Guiana (South America), M. ulcerans DNA was detected for the first time in water (112). In Louisiana (United States), an area where Buruli ulcer is not endemic, M. ulcerans DNA was detected in water and biofilms (147).…”

“…It was shown that M. ulcerans followed seasonal dynamics and was present mainly in waters with a higher pH (188). In the United States, there were positive associations between pH levels and the concentrations of ammonia, dissolved oxygen, nitrate, nitrite, and sulfide in freshwater rivers where M. ulcerans DNA was detected in water and biofilms (147). Salinity is a major problem in tropical coastal regions having predominantly rice-based farming systems because of the intrusion of brackish water during the dry season through tidal movements and capillary rise from shallow saline groundwater.…”

“…Buruli ulcer has also been encountered in aquatic invertebrates, mosquitoes (13, 16, 19, 91, 107, 113, 139, 141, 149, 150, 152-154, 156, 193), crayfish (108), amoeba, mollusks, crustaceans, annelida (29,40,141,153), aerosols, water, biofilm, moss, detritus, feces, plants, and soil (13,29,39,63,93,106,107,112,113,(144)(145)(146)(147)210). The hypothesis most advanced to aggregate data issuing from the investigations on the environment is that M. ulcerans may be part of a food chain (211,212).…”

“…In Australia, both using insect repellent and wearing long trousers were found to reduce the odds of contracting Buruli ulcer (18). Wearing clothing such as pants in areas with M. ulcerans in the environment seems to prevent the disease, and this explains the fact that, despite the presence of M. ulcerans in Louisiana wetlands, no cases of Buruli ulcer have been reported in health facilities (147). The most plausible mode of transmission is skin trauma at sites contaminated by M. ulcerans strains (31).…”

Buruli Ulcer in Japan

“…IS2404-PCR detects the presence of IS2404 regardless of the pathogenicity of the detected mycobacteria, which alone has little power in predicting endemicity of BU. M. ulcerans DNA was detected by IS2404-PCR extensively across southern Louisiana, U.S., leading to the conclusion that the distribution of environmental M. ulcerans is not restricted to areas where BU is endemic [53].…”