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History and Geographic Distribution of Chikungunya Virus

Written By

Maria Zavala-Colon and Juan A. Gonzalez-Sanchez

Submitted: January 15th, 2021Reviewed: June 1st, 2021Published: February 9th, 2022

DOI: 10.5772/intechopen.98662

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Abstract

Chikungunya fever (CHIKF) is a mosquito-borne disease caused by an arbovirus endemic to Africa and Asia. It was initially seen in the early 1950s at the boundary of Tanzania and Mozambique. Due to the ease with which its vectors propagate, the virus has spread to India, Europe, and recently it arrived in the Caribbean, eventually extending into North, Central, and South America. According to the World Health Organization (WHO), the most common clinical manifestations are abrupt fever, polyarthralgia, headache, maculopapular rash, myalgia, and nausea/vomiting. Severe joint pain and stiffness have been known to incapacitate some patients from a few days to several months after infection. The re-emergence of the CHIKV and its spread to new places around the globe has encouraged the development of new preventive, diagnostic, and treatment strategies. This chapter will discuss the history of CHIKV and expanding geographic distribution.

Keywords

  • chikungunya virus
  • fever
  • Aedes aegypti
  • history
  • geography
  • outbreaks

1. Introduction

The chinkungunya virus (CHIKV) is a single-stranded RNA arbovirus (genus Alphavirus, family Togaviridae) that is transmitted to humans by the bite of infected mosquitoes [1]. It causes chikungunya fever (CHIKF), an illness characterized by the sudden onset of fever and severe arthralgia known to cause chronic morbidity. The virus rarely causes a fatal infection; however, it is known to cause great morbidity to those affected, sometimes extending from weeks to years. “Chikungunya” is a word taken from the Makonde language in Tanzania which means “that which bends up” and refers to the bent posture observed in patients secondary to the severe pain in their joints [2]. The disease was first identified in Tanzania in 1952 by RW Ross. After its discovery, outbreaks of chikungunya typically occurred in Asia and Africa. However, in 2004, the CHIKV reached India and several islands in the Indian Ocean, causing major outbreaks that affected more than 1 million people [3]. Since then, the virus has reached new regions, including the Americas and Europe.

The clinical picture of CHIKV and dengue virus are indistinguishable and accurate diagnosis of these infections on clinical grounds alone is somewhat challenging. It is believed that the CHIKV has been present on the African continent for centuries, from back when science was not capable of identifying it [4]. Three distinct CHIKV genotypes have been identified, based on their geographic distribution: West-African, East/Central/South African (ECSA), and Asian isolates. They are responsible for major epidemics around the world, and the identification of the virus by its corresponding genotype is achieved through gene sequencing [5].

During inter-epidemic periods, the CHIKV is conserved through an enzootic cycle in places where it is endemic (such as Africa and Asia) and an urban cycle when the virus reaches the cities. In the enzootic cycle, continuous transmission of the pathogen occurs between wild animals and vectors. Non-human primates (NHP) serve as the reservoir for the virus, and the mosquitoes from the Aedes genusare the vectors responsible for the transmission of the virus. It is known that the CHIKV can use animals such as buffalos, rodents, and birds as hosts, but the critical host for enzootic circulation is not known with certainty [6].

A spillover of the virus can occur when people who live in rural areas close to these virus reservoir cycles are bitten by an infected mosquito. If these people then travel to urban areas in which there are viable vectors, more people could almost certainly be infected. In urban areas, the virus is transmitted by mosquitoes of the Aedes aegyptiand Aedes albopictusspecies. It is preserved and further spread in an autochthonous cycle in which continuous transmission occurs between mosquitoes and humans. In this type of transmission, infected mosquitoes transmit the virus to a person, enabling that individual to then contaminate the mosquitoes which feed on his or her blood, thus continuing the cycle [7].

The species A. aegyptiwas the principal vector involved in the outbreaks in Africa [8]. However, during the outbreaks in Asia, the territories of the Indian Ocean, Europe, and the Caribbean, A. albopictuswas identified as the principal vector. This change in the species of the vector occurred because the virus acquired a new mutation which enhanced its ability to use A. albopictusas a vector. This mosquito species, originally from Southeast Asia, has shown a great ability to adapt to other climates, allowing it to spread into places that are non-endemic for the CHIKV [5, 9]. For this reason, the CHIKV is a latent threat for many countries, and thus new diagnostic and preventive measures are in need.

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2. History

2.1 First sights

In 1952, the first CHIKV case was reported in the Makonde Plateaus region in Tanzania. The virus was isolated from the serum of several febrile patients and mosquitoes in 1953 by RW Ross [10]. Then in 1958, the first laboratory confirmed CHIKV outbreak in Asia was reported in Bangkok, Thailand [11]. Many countries in Southeast Asia, along with countries located in Central, Southern, and Western Africa continued to report sporadic outbreaks up to 1980. However, activity dwindled in the latter half of the 20th century.

2.2 Reemergence and increase dispersion of the chikungunya virus

For five decades, CHIKV was limited to sub-Saharan Africa and Southeast Asia. However, a new landscape developed at the beginning of the millennium. In 2004, an outbreak originated in Lamu Island on the coast of Kenya. Cases peaked in July, with an estimated 13,500 infected. In November, the disease reached Mombasa and the Comoros, resulting in a large outbreak that continued through 2005. It is estimated that 63% of the population may have been infected with CHIKV in Grande Comore. This epidemic continued to spread to other islands in the Indian ocean in the following 2 years [12].

Between 2005 and 2007 the island of Reunion experienced an outbreak that affected 38.8% of its 785,000 inhabitants [13]. Unusual clinical manifestations were reported, including neurologic complications, increased mortality rate, and 41 cases of mother-to-child CHICKV transmission in the context of intrapartum maternal viremia. The cause of this phenomenon was found to be a single alanine-to-valine acquired mutation in the envelope protein E1 glycoprotein at position 226 (E1-A226V) of the ECSA genotype of the CHIKV. The mutation increased the virus infectivity of the island’s native mosquitoes (A. albopictus). It led to greater and more effective dissemination of the disease due to the abundance of the arthropod vector [14]. Before the introduction of this mutation, the A. aegyptimosquito was the predominant vector used by the CHIKV. This mutation enabled the genotype to spread with a different vector, which is also present in other regions.

2.3 Asia

CHIKV has been circulating through Asia since the 1950s with sporadic outbreaks caused primarily by the Asian lineage. Significant expansion in its geographic distribution ensued from 2005 onwards. One of the countries with the highest disease burden was India. Between 2005 and 2006, the disease reemerged infecting 1.4 million individuals and dispersed to 17 of India’s 28 providences [3]. The ECSA genotype was responsible for the outbreak, and A. albopictuswas identified as the main vector in several areas. However, phylogenetic analysis indicates that this outbreak was due to a wild-type at E1–226, a different cluster to the La Reunion E1–226V lineage [15].

Other prominent outbreaks, caused by the ECSA lineage containing the E1–226 V mutation, were reported in Sri Lanka in 2006 (>36,000 cases), Malaysia in 2007, and in Thailand and Singapore in 2008–2009. In Cambodia, the first case of CHIKV was detected in 1961. The virus re-emerged in 2011 and a large outbreak occurred in the village of Trapeang Roka Kampong Speu Province in March 2012 [16].

The first imported sporadic case of the disease in China was described in Xishuangbanna, Yunnan Province, in 1987. The first documented community-based outbreak of CHIK fever was declared in the Xincun community of Wanjiang district in Dongguan city of Guangdong province on October 2010; 253 cases were recorded, of which 129 were laboratory confirmed. The outbreak was considered a local outbreak of CHIK fever caused by an imported case or vector, although the source is unclear [17].

According to the Indonesian Ministry of Health, chikungunya cases were initially reported in 1973 on Samarinda (Kalimantan island). The first virologically confirmed epidemic was reported in Jambi province of Sumatra island in June 1982. After a gap of approximately 20 years, the virus reappeared in Indonesia in 2001, causing outbreaks in 24 areas throughout Indonesia until 2004. Later, in 2009 and 2010, West and Central Indonesia were hit by the disease, causing 137,655 cases [18]. Studies suggest that the introduction of the ECSA genotype again is the culprit behind the massive outbreaks. After 2010, detected cases decreased dramatically. In 2011, CHIKV strains belonging to the Asian genotype and the ECSA genotype were circulating in different regions of Indonesia.

2.4 Europe

Since 2007, viremic travel-related cases have generated sporadic events of local CHIKV transmission throughout Europe. The first autochthonous outbreak was reported in the Emilia-Romagna region in north-eastern Italy in August 2007. The virus was introduced by a traveler from South-West India who carried the ECSA strain. Sequencing demonstrated the presence of the E1–226 V mutation. Local transmission was facilitated by high levels of A. albopictusin Italy when the index patient arrived. More than 200 laboratory-confirmed cases were reported of which one person died: an 83-year-old man with underlying medical conditions. Vector control measures and drop in temperature associated to seasonal change interrupted CHIKV transmission [19, 20].

In France three outbreaks have occurred in the last 10 years. The first was in September 2010 in southern France. The initial source was a 7-year-old girl that had returned from Rajasthan, India. Two local children contracted the disease. In October 2014, a 12-case outbreak was detected in a district of Montpellier, a town in the south of France colonized by the arthropod vector A. albopictussince 2010 [21]. An individual returning from central Africa living in the affected district was identified as the primary case. Subsequently, in 2017, 17 cases distributed in two clusters were reported by French authorities: 11 cases in Le Cannet-des-Maures and 6 cases in Taradeau. The virus circulating in France belongs to an ECSA sub-lineage that includes isolates from the Central African region (e.g. Gabon, Republic of Congo) and carries an adaptive E1-A226V mutation [22].

An outbreak in the Italian regions of Lazio and Calabriin was also reported in the summer of 2017. Between the months of August to November, 270 cases of CHIKV were confirmed. This latest epidemic outnumbered the outbreak that occurred near the Adianic coast a decade earlier. The CHIKV strain isolated from humans and A. albopictusmosquitoes in Italy in 2017 showed a high similitude with virus strains ravaging in India and Pakistan at that time and did not carry the A226V mutation [23, 24, 25].

Other countries in Europe, such as Spain, Portugal, Germany, and Russia, have reported cases of CHIKV in travelers; however, no cases of native transmission have occurred thus far. As such, the frequency of travel enhances the risk of local transmission in A. albopictus-infested European regions, highlighting the potential to establish transmission cycles. Although a massive influx of travelers returning from the Americas where the Asian CHIKV genotype has caused around one million cases, no Asian genotype-related autochthonous transmission of CHIKV has been reported in Europe.

2.5 America and the Caribbean

The first sighting of CHIKV infection in the Western Hemisphere was in 2010 in Rio de Janeiro, Brazil in an area with high propensity for dengue infection due to predominance of the competent vector A aegypti[26]. The first autochthonous case of CHIKV was confirmed on December 2013 in the Collectivity of Saint Martin. The outbreak was thought to be caused by the frequent travel of residents between the islands of the Caribbean [27]. Subsequently, most territories in the Caribbean reported locally acquired CHIKF cases. By 2017, CHIKV infection had spread to 45 countries and territories in the Caribbean, North, Central and South America and over 2.5 million suspected cases and confirmed [28]. Dominican Republic (41%) and Suriname (90.4%) experienced attack rates comparable to those noted in Malaysia (55.6%) and India (37.5%). But are far higher than the attack rate observed in La Reunion (16.5%) [29].

The CHIKV found in the Caribbean corresponds to the Asian strain, and its principal vector is the A. aegyptimosquito [30, 31]. This genotype, which does not have the A226V mutation in the E1 gene, has been widely reported in both Central America and South America. The introduction of these strains into the Americas could result in a wider spread of the virus, because the A. albopictusmosquito is present in most of these regions [4].

Several months after the CHIKV arrived at the Caribbean, the state of Florida, in the United States, reported 11 autochthonous cases during the summer of 2014 [4]. During that year, 243 imported cases were reported in 31 states, Puerto Rico, and the US Virgin Islands [32].

There were 475 imported CHIKF cases reported in countries belonging to the European Union during the period of 2008 to 2012 [33]. Most of these imported cases matched the times when outbreaks were occurring in endemic countries. For this reason, the establishment of the CHIKV in the Caribbean poses a great threat to European countries due to the high number of travelers from the latter to the former. This implies that more diagnostic and surveillance measures need to be implemented in regions where the CHIKV could thrive, in order to prevent further outbreaks in new places and regions where the virus has not reached before [34].

2.6 Where are we today?

CHIKV outbreaks continue to appear thought the world. In 2020, a total of 27, 540 cases were reported in three provinces in continental Africa (District of Abéché, Biltine, and Abdi) [35]. The most affected age group are those 15 years and over. The majority of cases developed a high fever, headache, and joint pain. In America and the Caribbean, countries such as Colombia, Costa Rica, Ecuador, El Salvador, Mexico, Nicaragua, Paraguay, Peru and Venezuela have detected cases of CHICKV. In the United States, 21 CHIKV cases have been reported to the CDC from travelers returning from an affected area. No cases acquired through presumed local mosquito-borne transmission. According to the European Center for Disease Prevention and Control the countries with the most reported cases in the last year are Thailand, India and Brazil (Figure 1).

Figure 1.

Countries with the most reported CHIKV cases in 2020 according to the ECDC.

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3. Conclusion

Once a local disease, CHIKV has spread to the majority of countries worldwide. Since its discovery in Tanzania in 1952, it has afflicted millions of people throughout tropical and sub-tropical regions. Individuals infected develop CHIKF characterized by severe polyarthralgia, headache, maculopapular rash, myalgia, and nausea/vomiting.

The first viremic wave took place between 1960 and 1980, affecting various regions in Africa and Southeast Asia. Evolution of the vector-borne RNA virus around 2005, lead to its dissemination into naïve areas such as America and Europe. Global expansion was also influenced by acquisition of a second competent vector A. albopictus, and travel of human carriers between affected and non-affected regions. As seen with the outbreaks in Europe, even temperate regions may experience severe outbreaks in the future.

CHIKV has become a global public health challenge. There are no current licensed vaccines and treatment strategies aim to relief symptoms. Therefore, re-emergence and spread to new places encourages further evaluation of the pathogenesis of this disease, in order to develop new preventive, diagnostic, and therapeutic options. For the time being, CHIKV outbreaks continue to be a threat and preparedness for the prevention and control of chikungunya outbreaks is key.

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Acknowledgments

Giovanni F. Ramírez-Arroyo, M.D.

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Conflict of interest

The authors declare no conflict of interest.

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Appendices and nomenclature

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Written By

Maria Zavala-Colon and Juan A. Gonzalez-Sanchez

Submitted: January 15th, 2021Reviewed: June 1st, 2021Published: February 9th, 2022