Review
Tracing the path of Chikungunya virus—Evolution and adaptation

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Abstract

Chikungunya fever has caught fresh attention as it raves around the globe. Since the first report of a major outbreak in Kenya in 2004, the disease has travelled across the Indian Ocean to the Indian subcontinent and subsequently to south-east Asia, resulting in millions of cases. Incidentally, the pandemic is panning out in a post-genomic era equipped with advanced molecular and bioinformatics tools that have facilitated the tracing, tracking and dissection of the Chikungunya virus (CHIKV). The rapidly accumulated data and information have offered us a glimpse of the evolution and adaptation of the virus as the pandemic unfolds.

This paper reviews the history of the disease and current knowledge of the evolution of CHIKV. The virus is known to have emerged from the sylvatic cycle in Africa, resulting in three genotypes – Western African, Eastern/Central African and Asian. Evidence from Asia suggests that the virus has the potential to return to the forest. Integrating genetic signatures with spatial and temporal data, we present a network that shows the possible geographical routes of the recent spread of CHIKV. Though evolutionary constrains are imposed on arboviruses by their obligations to fulfil the biological criteria of two different hosts (vertebrates and mosquitoes) during the transmission cycle, CHIKV has accumulated biologically important mutations that facilitated the recently changed epidemiology. It is evident that the virus has adapted to Ae. albopictus, without compromising its fitness in Ae. aegypti and the human host. Besides the E1-A226V and E2-I211T mutations that have led to the virus’ adaptation to Ae. albopictus, we discuss the possible initial adaptation to urban Ae. aegypti and the role of environmental factors. CHIKV may continue to scorch regions with competent vectors, especially Ae. albopictus and a susceptible human population. A preemptive approach is necessary to combat this disease with very high epidemic potential.

Introduction

Chikungunya fever, a previously neglected mosquito borne disease, has caught fresh attention as it raves around the globe. Its first rumble came from Kenya and the Indian Ocean Islands, where hundreds of thousands of cases were reported from Comoros, Reunion, Seychelles, Mauritius and Mayotte in 2004–2005 (Cordel et al., 2006). At about the same time, India saw the beginning of an epidemic wave (Yergolkar et al., 2006) that continued to sweep across the subcontinent, where 1.39 million cases were reported in 2006, 60 thousands in 2007, 95 thousands in 2008 and about 67 thousands in 2009 (Ministry_of_Health_and_Family_Welfare, 2010). Neighbouring Sri Lanka and Maldives were also hit with tens of thousands of cases during the 2006–2009 period (Hapuarachchi et al., 2008, Kularatne et al., 2009, Yoosuf et al., 2009). In the summer of 2007, an autochthonous outbreak of more than 200 confirmed cases in Italy (Rezza et al., 2007) sent tremors through the European and American public health and scientific communities, as it signalled that the disease was no longer restricted to developing, tropical countries (Enserink, 2007). Since then, the disease continued to spread in south-east Asia, involving Malaysia in late 2006 (AbuBakar et al., 2007), Singapore in early 2008 (Hapuarachchi et al., 2010, Leo et al., 2009, Ng et al., 2009b), Thailand in 2008 (Thavara et al., 2009, Theamboonlers et al., 2009), Indonesia in 2009 (The Jakarta Post, 2010; available in http://www.promedmail.org; Archive no. 20100301.0677) and Myanmar in 2010 (Democratic Voice of Burma, 2010; available in http://www.promedmail.org; Archive no. 20100224.0617). Incidentally, the pandemic is panning out in a post-genomic era equipped with advanced molecular and bioinformatics tools that have facilitated the tracing, tracking and dissection of the virus, as it moves from population to population around the world. As a result, the number of full genome sequences in publicly accessible databases has increased from two in 2005 to 92 in March 2010. Along with genetic data, indexed publications have also increased significantly, with more than 500 new publications within the same period. The rapidly accumulated data and information have offered us a glimpse of the evolution and adaptation of the virus as the pandemic unfolds.

This paper reviews our current knowledge about the evolution of Chikungunya virus (CHIKV) in terms of its adaptation to human and mosquito hosts and recent spread across continents. We further discuss other host and environmental factors that favoured a change in the disease epidemiology causing the current pandemic. Finally, the article highlights the gaps, the possible future and the strategic need for controlling the vector borne diseases like chikungunya fever.

Section snippets

Virus and the disease

CHIKV is grouped within the Semliki Forest virus antigenic complex, which also consists of the better known O’nyong nyong virus, Mayaro virus and the Ross River virus. Together with new world encephalitis viruses, Aura virus, Barmah forest virus and rubella virus, CHIKV belongs to the genera, Alphavirus that currently includes 29 species of 7 antigenic complexes. The 11.8 kb genome of CHIKV, like other alphaviruses, consists of a linear, single stranded positive sense RNA. The 5′ two-thirds of

History

“It was last May 25, in the afternoon at 5:00 when I noted while talking with two good friends of mine, a gnawing pain in my right hand, and in the joints of the hand and arm, which gradually increased, extending to the shoulder and then over my whole body, so that at 9:00 that evening I was in my bed with a high fever… It's now been three weeks since I… was stricken by the illness, and because of that had to stay home for 5 days; but even until today I have continuously pain and stiffness in

Vehicle of transmission

During the 1950–1970s epidemics in Africa and Asia, it was evident that CHIKV was spread by mosquito vectors (Gilotra and Bhattacharya, 1968, Gilotra and Shah, 1967, McIntosh et al., 1963, Myers et al., 1965, Paterson and McIntosh, 1964, Sarkar et al., 1967, Shah et al., 1964, Weinbren et al., 1958). In Africa, CHIKV was typically maintained in a sylvatic cycle involving wild primates, forest-dwelling mosquitoes and perhaps rodents. It was subsequently introduced into the urban settings, where

Evolution of the East/Central African genotype

The huge amount of genetic and epidemiological data generated from this current pandemic has been used to understand the origin and the subsequent spread of the virus across continents. Genetic analyses of the virus strongly indicate that the current pandemic started following a chikungunya fever outbreak in Kenya in 2004 (Kariuki Njenga et al., 2008). The causative virus was a new lineage of the East/Central African genotype (Parola et al., 2006, Schuffenecker et al., 2006). Prior to 2004,

Evolution and adaptation

Evolutionary constrains are imposed on arboviruses by their obligations to fulfil the biological criteria of two different hosts (vertebrates and mosquitoes) during the transmission cycle. Coffey and co-authors showed that the Venezuelan Equine Encephalitis virus (VEEV), when serially passaged in rodent or mosquito hosts, acquired an increased replication rate in the specific host, but reduced its infectivity in the alternative host. Alternating passages between rodents and mosquitoes yielded

Conclusions

Current knowledge underscores the complexity of the vector–virus–environment interactions, and clearly demonstrates their role in changing the infectious disease epidemiology. Though previous studies have suggested that the major factors in determining the endemicity of chikungunya fever could be related to the species/strains of vectors present (Tesh et al., 1976), current findings suggest that the virus evolution also plays a key role in the epidemiology of the disease. As the current

Acknowledgements

We thank CEO of National Environment Agency, Mr. Andrew Tan and Director General of Public Health, Mr. Khoo Seow Poh, for their constant support and guidance. We also thank Prof. Scott Halstead, Dr. David Lee and Mr. Tan Cheong Huat, for discussion on epidemiology and entomology of Chikungunya.

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