Tracing Mycobacterium ulcerans along an alimentary chain in Côte d’Ivoire: A one health perspective

Abstract

BackgroundMycobacterium ulcerans is an environmental mycobacterium responsible for an opportunistic, noncontagious tropical infection named Buruli ulcer that necrotizes the skin and the subcutaneous tissues. M. ulcerans is thought to penetrate through breached skin after contact with contaminated wetland environments, yet the exact biotopes where M. ulcerans occurs remain elusive, hence obscuring the epidemiological chain of transmission of this opportunistic pathogen. Methodology/Principal findingsPolymerase chain reaction investigations detected M. ulcerans in 39/46 (84.7%) rhizosphere specimens collected in 13 Buruli ulcer-endemic areas in Cô te d'Ivoire and 3/20 (15%) specimens collected in a nonendemic area (P = 5.73.E -7 ); only 3/63 (4.7%) sediment specimens from sediment surrounding the rhizospheres were positive in endemic area (P = 6.51.E -12 ). High-throughput sequencing further detected three PCR-positive plants, Croton hirtus, Corton kongensis and Oriza sativa var. japonica (rice), in the rectal content of two M. ulcerans-positive wild Thryonomys swinderianus grasscutters that were hunted in Buruli ulcer-endemic areas, while no PCR-positive plants were detected in the rectal content of two negative control animals that were farmed in a nonendemic area. Conclusions/SignificanceOur data suggest an alimentary chain of transmission of M. ulcerans from plants to T. swinderianus grasscutters and people that utilize T. swinderianus as bush meat in Buruli ulcerendemic areas in Cô te d'Ivoire. Guidance to adopt protective measures and avoid any direct contact with potentially contaminated rhizospheres and with grasscutter intestinal content when preparing the animals for cooking should be established for at-risk populations.

A need for null models in understanding disease transmission: the example ofMycobacterium ulcerans(Buruli ulcer disease)

“…Mainly impacting individuals in tropical and subtropical areas, BU endemicity spans over 30 countries (WHO 2018). The etiological agent, MU, is a member of an opportunistic group of environmental pathogens-mycolactone producingmycobacteria (MPMs)-that secrete a polyketide cytotoxic molecule that exhibits analgesic properties and causes tissue damage (George et al 1999;van der Werf et al 2003;Hammoudi et al 2020a). Molecular phylogenomic analyses corroborate a monophyletic clade containing the most important human mycobacterial pathogens, including MU, Mycobacterium tuberculosis, Mycobacterium leprae, Mycobacterium kansasii and Mycobacterium marinum.…”

Understanding the transmission of Mycobacterium ulcerans: A step towards controlling Buruli ulcer

“…In most cases, rodents likely ingest M . ulcerans while consuming aquatic plants without developing systemic infections [ 101 , 102 ]. There is minimal evidence that other animals in West Africa may be hosts of M .…”

Linking the Mycobacterium ulcerans environment to Buruli ulcer disease: Progress and challenges

“…Field investigations on presence of MU in mosquitoes in Africa Investigation into discrepancy regarding the presence of MU DNA in Australia and Africa. Marsupials and mammals Presence of MU in feces of mammals and marsupials in Australia [ 65 ] MU in feces of possums and marsupials that were identical to clinical strains [ [61] , [62] , [63] ] BU lesions in body parts of several mammals such as ringtail, brushtail and mountain brushtail possums, mouse, grass cutter, goats, dogs and other mammals in Australia and Africa [ 64 , 66 , 67 , 70 ] No studies have isolated viable MU from animal guts. MU was not detected from Benin in rodents and shrews and MU was not present in feces of domestic animals in Ghana [ 42 , 69 ] The asymptomatic colonization of MU in animal guts is intriguing and requires further investigation regarding effects of anaerobic conditions and temperature, among other conditions that might impact MU survival, growth and mycolactone production.…”

“…Similarly, BU lesions were observed in the tail of a mouse in a Ghanaian community [ 69 ] and detected in feces of Thryonomys swinderianus, a mammal that lives nearby water resources and rice fields in Cote d'Ivoire and other African countries [ 47 , 70 ]. BU characteristics and MU positivity have been reported in domestic animals such as goats and dogs in Benin [ 71 ], but not in rodents and shrews [ 72 ], and MU was not present in feces of domestic animals in Ghana [ 73 ].…”

“…In most MU environmental studies, MU has been detected in a variety of analyzed samples and positivity was higher in BU endemic regions compared to non-endemic regions [ 34 , 47 , 70 , 100 , 101 ]. Although in one study BU endemicity did not predict MU positivity, and was suggested to be attributed to passive surveillance [ 36 ].…”