Pathogen survival in the external environment and the evolution of virulence

Abstract

Recent studies have provided evolutionary explanations for much of the variation in mortality among human infectious diseases. One gap in this knowledge concerns respiratory tract pathogens transmitted from person to person by direct contact or through environmental contamination. The sit-and-wait hypothesis predicts that virulence should be positively correlated with durability in the external environment because high durability reduces the dependence of transmission on host mobility. Reviewing the epidemiological and medical literature, we confirm this prediction for respiratory tract pathogens of humans. Our results clearly distinguish a high-virulence high-survival group of variola (smallpox) virus, Mycobacterium tuberculosis, Cornynebacterium diphtheriae, Bordetella pertussis, Streptococcus pneumoniae, and influenza virus (where all pathogens have a mean percent mortality > or = 0.01% and mean survival time >10 days) from a low-virulence low-survival group containing ten other pathogens. The correlation between virulence and durability explains three to four times of magnitude of difference in mean percent mortality and mean survival time, using both across-species and phylogenetically controlled analyses. Our findings bear on several areas of active research and public health policy: (1) many pathogens used in the biological control of insects are potential sit-and-wait pathogens as they combine three attributes that are advantageous for pest control: high virulence, long durability after application, and host specificity; (2) emerging pathogens such as the 'hospital superbug' methicillin-resistant Staphylococcus aureus (MRSA) and potential bioweapons pathogens such as smallpox virus and anthrax that are particularly dangerous can be discerned by quantifying their durability; (3) hospital settings and the AIDS pandemic may provide footholds for emerging sit-and-wait pathogens; and (4) studies on food-borne and insect pathogens point to future research considering the potential evolutionary trade-offs and genetic linkages between virulence and durability.

Crossing the scale from within-host infection dynamics to between-host transmission fitness: a discussion of current assumptions and knowledge

“…If there is no trade-off between infection dynamics within a host and survival in the environment, the pathogen can optimize both stages [32]. However, it is quite likely that trade-offs between within-host infection dynamics and environmental stage occur at least for some pathogens or in certain situations [92], though again, there is a general lack of experimental data on that topic. One notable exception is a study on environmental survival and growth in phages, where a trade-off between the environmental persistence with replication efficiency in the bacterial host was demonstrated [118].…”

Non-pathogenic Neisseria: members of an abundant, multi-habitat, diverse genus

“…Potential environmental reservoirs and transmission have been invoked to explain the seasonal outbreaks of meningococcal disease in sub-Saharan Africa during the dry season; regional wind speeds and surface dust concentrations are good predictors of the incidence of meningitis (Pérez García-Pando et al, 2014), which further links meningitis epidemics in Africa with environmental risk factors (Martiny & Chiapello, 2013;Molesworth et al, 2003;Sultan et al, 2005). Further circumstantial evidence comes from studies of the persistence of N. meningitidis on environmental surfaces, which indicate that the bacterium can survive desiccation from hours to days (Downie, 1940;Swain & Martin, 2007;Tzeng et al, 2014;Walther & Ewald, 2004).…”

Environmental transmission of low pathogenicity avian influenza viruses and its implications for pathogen invasion

“…Further, in nature, virus persistence in the environment will be further complicated by local environmental conditions, such as temperature and salinity that degrade the infectious particle (31,32), which will have implications for virulence evolution due to novel opportunities for selection (33,34). In particular, virus persistence [or durability (33)] may trade off with traditional parameters such as the direct transmission rate (β) and the infectious period (γ ) giving rise to new challenges in virulence management. For these reasons, we conclude that environmental transmission warrants serious consideration in the study of avian influenza ecology and evolution.…”