Chikungunya Virus Transmission

Abstract

Chikungunya virus (CHIKV) is a mosquito-borneAlphavirus that causes Chikungunya fever (CHIKF) in humans. In 1952, the CHIKV was found in East Africa in a sylvatic and urban cycle between Aedes mosquitoes, and human and nonhuman primates in tropical regions. Since 2004, CHIKF has spread rapidly in Asia, Africa, Europe, and the Americas. Both Aedes aegypti and Aedes albopictus are known to be arboviral mosquito vectors of CHIKV. Ae. aegypti is mostly found within the tropics, whereby Ae. albopictus also occurs in temperate and cold temperate regions. Host-seeking female mosquitoes are infected after feeding on a viremic animal. The replication of CHIKV happens in the midgut and then enters the hemocoel before disseminating to the salivary glands of the mosquito. The disseminated virus can be transmitted by injecting infectious saliva into the host skin during blood feeding. In the naïve host body, CHIKV replicates in the dermal fibroblasts through blood circulation, and disseminates to other parts of the body such as brain cells, kidney, heart, lymphoid tissues, liver, and joints. Symptoms of CHIKV infection include high fever, rigors, headache, photophobia, and maculopapular rash. It is advised to avoid mosquito bites; also, larvae management systems should be applied in endemic environments.

1. Introduction

Chikungunya fever (CHIKF) is an arthropod-borne viral disease caused by the Chikungunya virus (CHIKV) which belongs to the Togaviridae family of genus Alphavirus. CHIKV is closely related to other Alphaviruses, including Ross River virus, Barmah Forest virus, O’nyong’nyong virus, the Sindbis group of viruses, and the Mayaro virus, all of which are known to cause arthritis. CHIKV has three genotypes that show different distribution geographically; Asian, West African, and East African [1].

The term “Chikungunya” was derived from the local word in the Makonde tribe based in the Southeastern part of Tanzania, meaning “disease that bends up the joints and causing pains” [2]. The CHIKV infection was first identified as an outbreak with an incidence rate estimated at 23%. It was reported for the period going from July 1952 to March 1953 in the Newala and Masasi districts in Southern Tanzania. The virus was isolated in early 1953 from the blood of several febrile patients. The CHIKV was initially found in East Africa in a sylvatic cycle between forest-dwelling Aedes mosquitoes and nonhuman primates in tropical and subtropical regions. Otherwise, a few isolations of CHIKV have been reported in other mammalian species including bats and squirrels [3].

2. Chikungunya vectors

2.1 Distribution

CHIKV is primarily transmitted by Stegomyia vector mosquitoes that belong to genus Aedes. Aedes mosquitoes are also known to be vectors of the dengue and the Zika fever viruses. Both Ae. aegypti and Ae. albopictus have been implicated in large outbreaks of CHIKF though they differ in distribution and occurrence. Ae. aegypti is mainly found within the tropics and subtropics regions. Furthermore, Ae. albopictus occurs in temperate and even cold temperate regions [4].

In Asia and the Indian Ocean regions, the main CHIKV vectors are Ae. aegypti and Ae. albopictus. In Africa, there is a larger range of Aedes species that are known to transmit CHIKV including Ae. furcifer-taylori, Ae. vittatus, Ae. fulgens, Ae. luteocephalus, Ae. dalzieli, Ae. vigilax, and Ae. camptorhynchites. In addition, Culex annulirostris, Mansonia uniformis, and Anopheles mosquitoes have occasionally been incriminated [5].

2.2 Ecology

The Aedes mosquitoes are known as container breeders meant that a female mosquito can lay eggs on collected water in an artificial and/or natural container. The Ae. albopictus species thrives in a wider range of natural water-filled breeding sites than Ae. aegypti, including coconut husks, cocoa pods, bamboo stumps, tree holes, plant axils, and rock pools, in addition to artificial containers such as vehicle tires, roof gutters, water storage buckets, and saucers beneath plant pots [6].

Ae. aegypti is more closely associated with human habitation and uses indoor breeding sites, including flower vases, water storage vessels, and concrete water tanks in bathrooms, as well as the same artificial outdoor habitats as Ae. albopictus [7, 8].

Adult, female mosquitoes can lay eggs on the inner walls of the containers with water, above the waterline. Eggs stick singly to container walls like glue and can survive drying out for up to 8 months, enabling them to survive cold winters and other adverse climatic conditions [9]. Aedes larvae hatch from the eggs and live in water, typically hanging upside down at an angle from the water surface, where they use a short thick respiratory siphon to take up oxygen from the air above the water. Larvae mature through four instars (stages), in the last stage developing into pupae, which subsequently change into adults that emerge at the water’s surface. Within 2 days of emerging, adult Aedes mosquitoes’ mate and females subsequently consume their first blood meal. Aedes mosquitoes prefer feeding on human blood during the daytime from early morning to a late afternoon outdoor, but Ae. aegypti can be active feeding indoor [10].

2.3 Host-seeking and blood-feeding behavior

Aedes mosquitoes are aggressive and silent, and prefer to feed outdoor during the daytime. Ae. aegypti, an important vector of human infectious diseases, shows a strong preference for human blood meals when compared to many other mosquitoes which feed on warm-blooded animals [11]. Temperature and nutrition are the environmental factors that affect mostly mosquito population growth. Biological signals can be captured from the mosquitoes surrounding environment and sensed through olfaction and other chemosensory organs, which play a major role in the modulation of mosquito behaviors such as hosts seeking, feeding, mating, oviposition, and reception of cues. Olfactory responses are initiated by activation of olfactory sensory neurons (OSNs) localized mainly on antennae, maxillary palps, mouthparts, and tarsi. These sensory appendages may perceive extremely diverse extrinsic stimuli, such as volatile and nonvolatile odors or pheromones, temperature, humidity, mild or noxious touch, gravity, to activate a complex mix of mosquito perception pathways [12].

Ae. aegypti and Ae. albopictus are the competent vectors of various infectious diseases, and their body size is much affected by temperature and nutrition. Mosquito body size is known to influence several attributes of vector ecology, fecundity, and multiple blood feeding [13]. Multiple feeding increases the risk of transmission by increasing the frequency of host contacts and can be of two types including supplementary and interrupted feeding. Supplementary feeding can happen as nutritional reserve depletion in teneral females, whereby interrupted feeding happens as host defense [14].

3. Chikungunya virus

3.1 Distribution

Since 2004, Chikungunya has spread rapidly and been identified in over 60 countries throughout Asia, Africa, Europe, and the Americas. In 2007, local transmission was reported for the first time in Europe and more specifically in northeastern Italy where a localized outbreak of 197 cases were recorded. In 2014, Europe faced its highest Chikungunya burden, with almost 1500 cases of which France and the UK were the most affected. France also confirmed four cases of locally-acquired Chikungunya infection in the southern part of the country [15].

In the year 2013, the first documented outbreak of Chikungunya with the autochthonous transmission in the Americas occurred [16]. In 2016, there were a total of 349,936 suspected cases and 146,914 laboratory-confirmed cases reported to the Pan African Health Organization (PAHO) regional office, which represented half of the burden compared to the previous year. In 2017, European Centre for Diseases Prevention and Control (ECDC) reported a total of 10 countries, with 548 cases of Chikungunya, of which 84% were confirmed cases. Italy bore more than 50% of the Chikungunya burden.

In Africa and Asia, Chikungunya outbreaks were also reported in Senegal (2015), Kenya (2004 and 2016), Tanzania (2008), Sudan (2018), Yemen (2019), and more recently in Cambodia and Chad (2020) [15, 16, 17].

3.2 Transmission

CHIKV can be transmitted in a sylvatic, enzootic, and urban cycle involving humans, nonhumans, and Ae. aegypti and Ae. albopictus mosquito species as shown in Figure 1.

Figure 1.

Showing Chikungunya virus transmission cycles.

In Africa, circulation in sylvatic, enzootic cycles involves several species of arboreal mosquito vectors that transmit among diverse nonhuman primates and possibly other amplifying hosts. Transmission of CHIKV occurs through a bite by infected Ae. aegypti or Ae. albopictus, although in the recent epidemic, some cases were the result of maternal–fetal transmission [12, 13, 18].

There is evidence that some animals, including non-primates, rodents, birds, and small mammals, may act as reservoirs of the virus, allowing re-emergence of the virus after periods of inactivity in humans [19].

3.3 Mosquito-virus relationship

The ability of arthropods to transmit pathogens depends on intrinsic and extrinsic factors and is expressed in two terms: (a) Vector competence, the ability of a vector to become infected and transmit after the pathogen is ingested in a blood meal, is often regulated for arboviruses at the level of midgut infection, and (b) Vectorial capacity, the number of infective bites arising from an infected host, as shown in Figure 2. Host-seeking female mosquitoes are infected after feeding on a viremic animal. CHIKV first replicates in the midgut and then enters the hemocoel before disseminating to the salivary glands. Midgut basal lamina reorganization during blood digestion mediates this dissemination process. The extrinsic incubation period is generally 2–5 days, suggesting that even vector populations with poor daily adult survival can transmit effectively. Females with a disseminated virus in their salivary glands can transmit by injecting infectious saliva into a naïve host during a subsequent blood meal, leading to horizontal transmission. Ae. aegypti feeding is often interrupted when it is disturbed during blood feeding, and it may then complete the meal on one or more hosts in the vicinity. This can lead this highly anthropophilic species to feed on multiple persons daily, increasing the risk of CHIKV infection and transmission to multiple hosts, greatly enhancing vectorial capacity. Vector competence of Ae. aegypti and Ae. albopictus shows variation according to the geographical origin of the mosquito population and CHIKV strain [1, 15]. Once infectious, the mosquito is believed to be capable of transmitting the virus for the rest of its life.

Figure 2.

Chikungunya virus in the host-vector transmission cycle.

3.4 Chikungunya pathogenesis

In order for the viral transmission to occur, the skin is a major portal of entry whereby the infested mosquito transmits CHIKV together with immunoregulatory proteins from the mosquito’s saliva while taking a blood meal. The local immune response (monocyte, keratocytes, and melanocytes) cannot prevent the virus from spreading to other tissues. Then, CHIKV replicates in the fibroblast cells of the skin then through the blood circulation, the viruses are disseminated to the brain cells, the kidney, heart, lymphoid tissues, liver, and joints. The incubation period is 2–4 days and is followed by a sudden onset of clinical disease with no prodromal phase. Symptoms of CHIKV infection include high fever, rigors, headache, photophobia, and a petechial rash or maculopapular rash. In addition, most infected individuals complain of severe joint pain that is often incapacitating due to the joint inflammation caused by arthralgia and rheumatoid arthritis (Figure 3) [16, 20].

Figure 3.

Chikungunya pathogenesis.

4. Recommendation

The use of a mosquito larvae management system would be a great approach to reduce vector population. The use of mosquito repellents, such as coils and lotions containing repellents, during the daytime will reduce arboviral transmissions. Governments could develop public awareness campaigns during outbreaks to educate populations on how to control the disease.