Evolution and emergence of novel human infections

N Arinaminpathy,A R Mclean

doi:10.1098/rspb.2009.1059

N Arinaminpathy, A R Mclean

Open Access

https://doi.org/10.1098/rspb.2009.1059

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Abstract

Some zoonotic pathogens cause sporadic infection in humans but rarely propagate further, while others have succeeded in overcoming the species barrier and becoming established in the human population. Adaptation, driven by selection pressure in human hosts, can play a significant role in allowing pathogens to cross this species barrier. Here we use a simple mathematical model to study potential epidemiological markers of adaptation. We ask: under what circumstances could ongoing adaptation be signalled by large clusters of human infection? If a pathogen has caused hundreds of cases but with little transmission, does this indicate that the species barrier cannot be crossed? Finally, how can case reports be monitored to detect an imminent emergence event? We distinguish evolutionary scenarios under which adaptation is likely to be signalled by large clusters of infection and under which emergence is likely to occur without any prior warning. Moreover, we show that a lack of transmission never rules out adaptability, regardless of how many zoonoses have occurred. Indeed, after the first 100 zoonotic cases, continuing sporadic zoonotic infections without onward, human-to-human transmission offer little extra information on pathogen adaptability. Finally, we present a simple method for monitoring outbreaks for signs of emergence and discuss public health implications.

Highlights

Many novel human infections have zoonotic origins (Morens et al 2004; Wolfe et al 2007; Jones et al 2008)
HIV was acquired from African primates (Rambaut et al 2004; Keele et al 2006); SARS coronavirus has been linked to both bats (Li et al 2005) and palm civets (Guan et al 2003); and a recent new arenavirus which killed four out of five cases in Southern Africa is probably derived from rodents (Briese et al 2009)
BIOLOGICAL BARRIERS TO ADAPTATION If a pathogen causes many hundreds of cases yet fails to show any sustained human transmission, does this mean that it is incapable of adapting for human transmission? how many ‘failed’ human cases should occur for such a conclusion?

Summary

INTRODUCTION

Many novel human infections have zoonotic origins (Morens et al 2004; Wolfe et al 2007; Jones et al 2008). As discussed by Antia et al (2003) even a pathogen poorly transmitted among humans, and capable only of causing sporadic cases, can acquire adaptations to become capable of sustained human transmission Such adaptations could arise in response to the selective pressure exerted by the new host environment. The avian influenza subtype H5N1 has caused over 400 human cases (World Health Organization 2009), mostly through close contact with infected poultry (Beigel et al 2005). It has shown little or no transmission between humans, the possibility of its future adaptation to humans cannot be ruled out. We discuss some public health implications of this work

REPRODUCTIVE FITNESS AND OUTBREAK SIZES

THE MATHEMATICAL MODEL

WARNING SIGNS OF ADAPTATION

BIOLOGICAL BARRIERS TO ADAPTATION

EMERGENCE DETECTION

DISCUSSION AND CONCLUSION