One health – an ecological and evolutionary framework for tackling Neglected Zoonotic Diseases

Abstract

Understanding the complex population biology and transmission ecology of multihost parasites has been declared as one of the major challenges of biomedical sciences for the 21st century and the Neglected Zoonotic Diseases (NZDs) are perhaps the most neglected of all the Neglected Tropical Diseases (NTDs). Here we consider how multihost parasite transmission and evolutionary dynamics may affect the success of human and animal disease control programmes, particularly neglected diseases of the developing world. We review the different types of zoonotic interactions that occur, both ecological and evolutionary, their potential relevance for current human control activities, and make suggestions for the development of an empirical evidence base and theoretical framework to better understand and predict the outcome of such interactions. In particular, we consider whether preventive chemotherapy, the current mainstay of NTD control, can be successful without a One Health approach. Transmission within and between animal reservoirs and humans can have important ecological and evolutionary consequences, driving the evolution and establishment of drug resistance, as well as providing selective pressures for spill‐over, host switching, hybridizations and introgressions between animal and human parasites. Our aim here is to highlight the importance of both elucidating disease ecology, including identifying key hosts and tailoring control effort accordingly, and understanding parasite evolution, such as precisely how infectious agents may respond and adapt to anthropogenic change. Both elements are essential if we are to alleviate disease risks from NZDs in humans, domestic animals and wildlife.

WidespreadTreponema pallidumInfection in Nonhuman Primates, Tanzania

“…Further studies on the spatial distribution of NHP infection with T. pallidum and advanced genetic characterization of simian strains are crucial for identifying NHPs as a possible reservoir for human infection ( 35 ). In light of the data and for a sustainable eradication of human yaws, a One Health approach in which animal and human health is investigated ( 36 ) is needed.…”

Roadmap to a One Health agenda 2030.

“…It is typically targeted with mass drug administration programmes, provision of safe water and sanitation, molluscicide use and education programmes to highlight risks [113]. However, recent changes in the species evolution and changing transmission ecology, including zoonotic spill overs and multi-host pathogenicity and hybridization have been demonstrated [114][115][116][117]. Thus, in the ever changing world of human and animal population growth, anthropogenic environmental changes, globalized movements of livestock and humans, the previous narrow, anthropocentric or disjointed sectoral approach to the control of schistosomiasis in humans will now require a paradigm shift, taking a wider view through an OH approach.…”

The human immune system’s response to carcinogenic and other infectious agents transmitted by mosquito vectors

“…M. tuberculosis is taken up by macrophages but prevents the fusion of the phagosome with the lysosome, protecting itself from the bactericidal actions of the lysosomal contents and Listeria, Toxoplasma gondii, Borrelia burgdorferi and Treponema pallidum can avoid elimination by antibodies (Janeway et al 2001). Parasites have the ability to successfully infect a wide range of host species of broad ancestry (Hellgren et al 2009;Webster et al 2016). Additionally, avian malaria parasites have developed evolutionary independence .…”

“…There are also reports of B. burgdorferi (the cause of Lyme disease) in Culex mosquitoes, (Anderson et al 2006;Zákovská et al 2002) and in Germany DNA of Borrelia afzelii, Borrelia bavariensis and Borrelia garinii has been detected in four distinct genera (Aedes, Culiseta, Culex and Ochlerotatus), with positive samples found in adult specimens from wild-caught larvae, suggesting transstadial and/or transovarial transmission (Melaun et al 2016). This adds additional complexity to the understanding of how a variety of host species contribute to transmission and human infection (Webster et al 2016). A biofilm in Lyme's disease has been discovered that boosts therapy resistance by nearly 1000 times (Sapi et al 2016).…”

“…This is not an easy task either, as illustated by several comprehensive reviews of the biological complexities involved in environmental mosquito control (Ferguson et al 2010;Benelli and Melhorn 2016;Webster et al 2016). The authors conclude that mosquitoes need to be controlled at multiple points in the continuum from egg to adult.…”