Research Article: A Sero-epidemiological Approach to Explore Transmission of Mycobacterium ulcerans

Date Published: January 25, 2016

Publisher: Public Library of Science

Author(s): Kobina Assan Ampah, Beatrice Nickel, Prince Asare, Amanda Ross, Daniel De-Graft, Sarah Kerber, Ralf Spallek, Mahavir Singh, Gerd Pluschke, Dorothy Yeboah-Manu, Katharina Röltgen, Pamela L. C. Small. http://doi.org/10.1371/journal.pntd.0004387

Abstract: The debilitating skin disease Buruli ulcer (BU) is caused by infection with Mycobacterium ulcerans. While various hypotheses on potential reservoirs and vectors of M. ulcerans exist, the mode of transmission has remained unclear. Epidemiological studies have indicated that children below the age of four are less exposed to the pathogen and at lower risk of developing BU than older children. In the present study we compared the age at which children begin to develop antibody responses against M. ulcerans with the age pattern of responses to other pathogens transmitted by various mechanisms. A total of 1,352 sera from individuals living in the BU endemic Offin river valley of Ghana were included in the study. While first serological responses to the mosquito transmitted malaria parasite Plasmodium falciparum and to soil transmitted Strongyloides helminths emerged around the age of one and two years, sero-conversion for M. ulcerans and for the water transmitted trematode Schistosoma mansoni occurred at around four and five years, respectively. Our data suggest that exposure to M. ulcerans intensifies strongly at the age when children start to have more intense contact with the environment, outside the small movement range of young children. Further results from our serological investigations in the Offin river valley also indicate ongoing transmission of Treponema pallidum, the causative agent of yaws.

Partial Text: Buruli ulcer (BU) is a neglected tropical skin disease presenting with a wide range of cutaneous manifestations, from non-ulcerated nodules, plaques or oedema to characteristic necrotizing ulcers [1]. While BU cases have been reported in more than 30 countries worldwide, most patients are from infection foci located in remote and rural tropical regions of West and Central Africa. BU is caused by infection with Mycobacterium ulcerans, a pathogen that has emerged from M. marinum by acquiring a plasmid conferring the capacity of producing the unique macrolide toxin mycolactone, accounting for much of the pathology of BU [2,3]. Until today, the mode of transmission of M. ulcerans has remained inconclusive, although proximity to aquatic habitats has long been identified as the major risk factor for contracting the disease [4]. Infection is thought to take place through either physical contact with undefined environmental reservoirs via skin abrasions or insect vectors [5–7].

Since only a minority of individuals exposed to M. ulcerans develops clinical BU, sero-epidemiological studies represent a valuable tool to assess the exposure of populations in BU endemic areas to the pathogen. In line with data obtained from previous sero-epidemiological investigations in BU endemic areas located in the Densu river basin of Ghana and in the Mapé river basin of Cameroon [11,15], we reconfirmed here for the population of the BU endemic Offin river valley that young children below four years of age are considerably less exposed to M. ulcerans than older children. In contrast, our serological data showed, as expected, that exposure to the mosquito transmitted malaria parasite P. falciparum and to soil-transmitted helminths of the genus Strongyloides takes place already in very young children, as indicated by an early development of humoral immune responses against these pathogens in some of the infants. The delay in exposure of M. ulcerans and the relatively abrupt onset are in stark contrast to the age-patterns for Plasmodium and Strongyloides. Contact with larvae-infested soil through faecal contamination is likely to be responsible for the observed early development of anti- Strongyloides serum IgG responses. Our results suggest that contact with M. ulcerans occurs outside the small movement range of infants, providing indirect evidence against mechanisms of transmission involving vectors or reservoirs present in the vicinity of the children’s homes. However, our data do not exclude an involvement of insect vectors commonly found at the periphery of villages close to water contact sites. We recognize that the age distribution of anti- P. falciparum serum antibodies depends not only on the mode of transmission, but also on the transmission intensity [27,28]. While there is some evidence that mosquitos may be involved in transmission of M. ulcerans in south-eastern Australia [29,30], it is overall unlikely that they play a major role as vectors in African BU endemic settings. This assumption is also supported by previous molecular epidemiological studies showing that transmission of newly emerging genetic variants of M. ulcerans is geographically highly clustered [31,32].

Source:

http://doi.org/10.1371/journal.pntd.0004387

 

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