|Year : 2017 | Volume
| Issue : 3 | Page : 355-360
Review on transovarial transmission potentiality of dengue vectors: An international perspective with special reference to North-Eastern region of India
Monika Soni1, Jitendra Sharma2
1 Centre for Studies in Biotechnology, Dibrugarh University, Dibrugarh, Assam, India
2 District Surveillance Unit, Office of The Joint Director of Health Services, Lakhimpur, Assam, India
|Date of Web Publication||12-Oct-2017|
District Surveillance Unit, Office of The Joint Director of Health Services, Lakhimpur - 787 001, Assam
Source of Support: None, Conflict of Interest: None
Despite extensive research in vaccine development, there is at present no known method of controlling dengue except by the mosquito vectors. Virologic surveillance which involves the detection of dengue virus (DENV) in human serum and followed by isolation of virus using cell culture or mosquito inoculation is used as an early warning symptom to predict the outbreak. The technique is not much effective as the virus is in the human population. However, if the virus is detected in mosquito before it can infect humans could be more effective approach. One of the great mysteries about the epidemiology of dengue is how the virus persists in the interepidemic period. So far, no such studies on dengue vectors have been conducted in the north-eastern region of India, especially in Assam and the dengue cases are increasing every year. There are no reports on the identification of active and potential role of dengue vector responsible for the transmission of dengue in this state. Such type of study will give an overall picture of potential dengue vector responsible for human DENV infection and the viral load carried by the mosquito species in different generations. Such study will be useful in helping the public health personnel.
Keywords: Dengue, epidemiology, vaccine, viral load
|How to cite this article:|
Soni M, Sharma J. Review on transovarial transmission potentiality of dengue vectors: An international perspective with special reference to North-Eastern region of India. Indian J Med Microbiol 2017;35:355-60
|How to cite this URL:|
Soni M, Sharma J. Review on transovarial transmission potentiality of dengue vectors: An international perspective with special reference to North-Eastern region of India. Indian J Med Microbiol [serial online] 2017 [cited 2019 Aug 17];35:355-60. Available from: http://www.ijmm.org/text.asp?2017/35/3/355/216621
| ~ Introduction|| |
Dengue fever also known as 'break bone' fever is an infectious tropical disease caused by the dengue virus (DENV). It is endemic in >110 countries. It infects 50–100 million people worldwide in a year, leading to half million hospitalisations and approximately 12,500–25,000 deaths. DENV is an RNA virus of the family Flaviviridae; genus Flavivirus. There are four strains of the virus, which are called serotypes, and these are referred to as DENV-1, DENV-2, DENV-3 and DENV-4. DENV is transmitted to humans by Aedes mosquitoes, and the two most frequent vector species are Aedes aegypti and Aedes albopictus.
Dengue epidemic tends to coincide with the rainy season as significant increases in mosquito larval populations were seen during this season. Furthermore, ambient temperature and relative humidity also plays an important role in viral propagation in mosquitoes. Apart from this, the infected mosquitoes can transmit the virus transovarially and eggs from infected female increase the vertical transmission even after several weeks of incubation at room temperature which indicates that if these eggs survive through interepidemic season, the emerging adults can initiate the human-mosquito-human cycle. This shows the possible role of Aedes mosquito in maintenance of virus through transovarian passage over different generations. However, the transovarially infected mosquitoes have shown a decrease in the rate of fertility and fecundity.
Female Aedes mosquito ingests the DENV from an infected host. After that, the DENV must develop or multiply inside the mosquito which is called extrinsic incubation period (EIP) and female must survive to a relatively old age before transmission can occur. The EIP of the DENV in Aedes aegypti is approximately 12–16 days, which means mosquito must survive longer than 12 days before it can transmit the virus to an uninfected person. However, in the meantime, there is no sensitive and reliable laboratory animal model for dengue, and currently usedin vitro assays for transmission may fail to detect small but transmissible amounts of virus at early times. Thus, the information regarding the ability of local vectors to transovarially transmits DENV will be useful in assisting the public health personnel and the general public in implementing a more effective campaign against dengue as well as their vectors.
| ~ National and International Status|| |
Dengue is currently one of the most important arthropod-borne diseases. The first case of probable dengue fever was recorded in a Chinese medical encyclopaedia from the Jin Dynasty (265–420 AD) which referred to a 'water poison' associated with flying insects. It was named as break-bone fever by Dr. Benjamin Rush, a Philadelphia doctor in 1780 on the basis of symptoms resembled in patients. During World War 2, it affected many military soldiers in the far East. In 1916 during an outbreak in New South Wales, found a record of mosquito Culex fatigans and Stegomyia fasciata. Thereafter, Culex fatigans was wrongly interpreted as the transmitting agent in the outbreak and later found that culicine mosquito Aedes aegypti is the transmitting agent. Dengue outbreak hits many countries such as 1943 and 1944 Hawaii, Oahu (DEN-1), 1949 Bangkok, 1958 Vietnam, 1960 Singapore, 1962 Malaysia, 1963 and 1964 India-Calcutta (DEN-2), 1964 Bangladesh (DEN-3), 1964 Tahiti, French Polynesia, 1966 SriLanka, 1968 Indonesia, 1970 Myanmar, 1977 Caribbean, 1978 Mexico, 1977 and 1979 Maldives, 1974–1980 peoples republic of China, 1980 USA, Texas and 1981 Cuba. Hyperendemic transmission is reported in Vietnam, Thailand, Indonesia, Pakistan, India, Malaysia and Philippines. Now, dengue has spread to all over the world with its vectors prevalent in many parts of the globe. Various studies have been undertaken to establish transovarial transmission phenomenon by mosquito vectors hypothesising the role played by them in interepidemic period.
In 1978 and 1979, Watts et al. studied on the possibility of transovarial transmission of DENV by Aedes aegypti and Aedes albopictus in urban and rural areas of Thailand. Mosquitoes were processed in 10–25 numbers per pool for detection of virus by plaque assay and immunofluorescence technique. Dengue-positive females showed no positivity in F1 generation. In contrast, it showed DEN-2 isolation from engorged mosquitoes collected from dengue-positive patient's house. Hence, their study concluded that dengue infections occurring throughout the year; accordingly, mosquito man cycle is maintained, and transovarial transmission is not an important maintenance mechanism for DENV transmission. In 1996, a study was conducted by Hailin et al., in China to observe the transovarial transmission of DENV by Aedes aegypti and Aedes albopictus mosquitoes. Parental females of Aedes albopictus and Aedes aegypti were orally infected with DEN],,, viruses. The study was carried out up to the second generation. The positivity rates of pools of Aedes albopictus in F1 generation were 10% (1/10) for DEN1, 22.22% (2/9) for DEN2, 33.33% (4/12) for DEN3 and 28.95% (11/38) for DEN4. In F1 generation, the minimum filial infection rates (FIR) of Aedes albopictus was successively 0.20%,0.71%,0.70% and 0.63% for DEN],,,. The positivity rates of pools and minimum FIR of Aedes albopictus in F2 generation were 35.29 % (6/17) and 0.93% for DEN4. The positivity rates of pools from Aedes aegypti in F1 and F2 generation were 60%(3/5) and 33.33% (3/9), and their minimum FIR in F1 and F2 generation were 0.63 % and 0.60% for DEN4, respectively. In 1997, Rohani et al., conducted a study in major towns of 12 states in peninsular Malaysia for detection of DENV from field collected Aedes aegypti and Aedes albopictus adults and larvae. Aedes albopictus cell culture (C6/36 clone) was used for isolation of DENV. Peroxidase anti-peroxidase (PAP) staning method was used for virus detection and further reconfirmed by reverse transcriptase polymerase chain reaction (RT-PCR). The study suggests the possibility of transovarial transmission of DENV by both Aedes aegypti and Aedes albopictus. Another study conducted in 2003 by Wanwasinpiyamongkol et al., on transovarial transformation by two morphological variants (the dark form and the pale form) of Aedes aegypti by artificial feeding of DEN-2 (16681) strain, results confirmed the persistence of DENV upto third generation. However, two different morphological forms did not show much difference in their transmission potential. In 2006, Salazar et al.'s study challenged Aedes aegypti mosquito with DENV-2 (Jamaica 1409) strain orally. Result showed multiple tissues infection with DENV. Real-time PCR was used for accurate viral particle detection. According to the study, the EIP is very relevant and also epidemiologically important. Study found EIP for the virus is reduced, as the salivary gland infection was detected after 4 days of infection with the virus. Akbar et al., in 2008, carried out a study on transovarial transmissibility of DENV in Aedes aegypti in Bandung, Indonesia. Study samples detected positive for DENV-2 strains and hence concluded with a finding that the dengue vectors have the potentiality to transmit DENV transovarially in the wild. A different finding by Thongrungkiat et al., in 2010, Thailand, was carried out to find the transovarial transmission by two different morphological forms of Aedes aegypti from field-collected larvae raised to adults. Adult raised from field-collected larvae were kept at 28°C and pooled with 35 mosquitoes each for identification by RT-PCR. All four serotypes were reported with high percentage for DENV-4 strain. Minimum infection rate (MIR) varies for both the forms which also pose important concerns over molecular identification along with morphological identification procedure of these species. According to them, peak transmission season was 4 months before human infection starts. In 2011, in Bolivia, a study was conducted by Le Goff et al., on natural vertical transmission of DENV by field-collected Aedes aegypti mosquitoes. Using molecular identification method, both male and female showed positive infection with significantly higher prevalence in male than in female mosquitoes. Cocirculation of DENV-1 and 3 strain was reported. The observations suggested that vertical transmission of DENV may be detected in vectors at the peak of an outbreak as well as several months before, an epidemic occurs in human population. Similarly, in 2012, Martins et al. conducted a study on natural vertical transmission in Aedes aegypti and Aedes albopictus from Fortaleza, Ceara, Brazil. They found both the vectors positive for the DENV. Aedes albopictus was positive for DENV-3 and DENV-2 strain whereas Aedes aegypti for DENV-2 strain. Furthermore, there was cocirculation of type 2 and type 3 strain. In 2013, Sylvestre et al. studied on the potential impact of DENV infection on some Aedes aegypti by examining feeding behaviour, survival, oviposition success and fecundity. Mosquitoes were challenged orally by DEN-2 (16681). Study reported higher mortality in infected females compared to control. Furthermore, fecundity was reduced in infected population due to immune activation. A recent study by Cruz et al. in 2015 from Cuiaba, state of Mato Grosso, Brazil, was undertaken for the detection of natural transovarial transmission of DENV in Aedes aegypti. Detection by RT-PCR revealed DENV-4 infection in Aedes aegypti along with the mala pools with MIR 10.5%. Their study provided the first evidence of natural transovarial infection from Mato Grosso, suggesting a mechanism of virus maintenance during interepidemic periods in Cuiaba, a city where dengue epidemics are reported every year.
Majority of the studies are conducted in the field to report transovarial transmission potential of DENV in the mosquito vectors. Mosquito collection from dengue outbreak areas reported positive samples in epidemic as well as non-epidemic season. Aedes aegypti was found to be the established vector playing important role and reservoir of the virus in interepidemic period. However, few studies are also reporting that Aedes albopictus considered as a secondary vector for dengue, is now adapting to urban environment and playing role in dengue transmission. Laboratory studies conducted by challenging DENV orally clearly documented virus positivity up to third generation in Aedes aegypti. However, few virus strains are being utilised for oral infection by mosquitoes. The response of mosquitoes may vary with the virus isolate. Therefore, more laboratory studies utilising different isolates of virus could help in understating the pathogenic strain more adapted with the vector. Furthermore, more robust method for mosquito identification is required to ensure species-specific response of vector virus interaction.
| ~ National Perspective|| |
In the Indian subcontinent, the epidemiology of dengue fever seems to be very complex and scenario has substantially changed over almost the past six decades in terms of prevalent strains, affected geographical locations and severity of disease. The first existence of dengue fever was reported in 1946, since then for another 18 years, no cases of dengue were reported. First outbreak was reported during 1963 in Kolkata. The disease spread to northwards and reached Delhi in 1967 and Kanpur in 1968. Simultaneously it also involved the southern part of the country. In 1996, a major outbreak of Dengue/ Dengue hemorrhagic fever was reported from Delhi and 18 neighbouring states. The mostly affected states were Delhi, West Bengal, Kerala, Tamilnadu, Karnataka, Maharashtra, Rajasthan, Gujarat and Haryana. Gradually the whole country was involved with wide spread epidemics followed by endemic/hyper-endemic prevalence of all the four serotypes of DENV.
Aedes aegypti is the most common vector of DENV in India, followed by Aedes albopictus. Larval indices indicate that Aedes aegypti is well established in periurban areas and is beginning to displace Aedes albopictus. Due to rapid urbanisation, transport development and changing habitats, there is a great risk in expansion of disease areas. Controlling the vector population seems to be a good method for the prevention of vector-borne diseases, but effective mosquito control is virtually non-existent in most dengue-endemic countries. Considerable emphasis for the past 20 years has been placed on ultra-low-volume insecticide space sprays for adult mosquito control, a relatively ineffective approach for controlling Aedes aegypti. There are several reports from India which have demonstrated the resistance of mosquito vector with antilarval substances such as dichlorodiphenyltrichloroethane and dieldrin. Sooner or later mosquitoes develop insecticide resistance which leads to failure of control strategies. Increased travel by airplane provides the ideal mechanism for transporting DENV between population centres of the tropics, resulting in a constant exchange of DENV and other pathogens.
With no new mosquito control technology available, in recent years, public health authorities have emphasised disease prevention and mosquito control through community efforts to reduce larval breeding sources. Although this approach will probably be effective in the long run, it is unlikely to have impact on disease transmission in the near future. It is, therefore, a need to develop an improved, proactive, laboratory-based surveillance system that can provide early warning of an impending dengue epidemic.
DENV is maintained in nature through vertical and transovarial transmission. Transovarial transmission can be defined as the passage of the virus from one generation to the next through the ovaries-transovarian/transovarial transmission. The virus is maintained in mosquitoes and is responsible for re-emergence of disease from interepidemic to epidemic phase. The surveillance of DENV transovarial transmission in immature mosquito forms from the natural environment will suggest some potential for identifying disseminated dengue outbreak areas quickly. More importantly, rising transovarial transmission DENV infection rates can provide an early warning signal of an impending dengue epidemic so that pre-epidemic control/interventions can be implemented to suppress disease transmission and to prevent the disease spreading to new areas.
A study conducted by Joshi et al., in 2002, challenged Aedes aegypti with DENV strain (633798), isolates from Thailand in 1963. The study reported the persistence of virus up to seventh generation. Fecundity and fertility were reduced in infected population compared to controls. In a similar study by Angel and Joshi in 2008, collected Aedes aegypti, Aedes albopictus and Aedes vittatus from desert and non-desert districts of Rajasthan, India, from 2006 to 2007. Results found the presence of DENV in Aedes aegypti and Aedes albopictus mosquitoes. Aedes albopictus was found positive in winter season which is not considered as an active season for dengue transmission. Dengue serotype detected in mosquitoes is not mentioned, and indirect immunofluorescence assay (IFA) method was used for virus identification. Based on the observation, it was concluded that transovarial transmission is a crucial aetiological phenomenon responsible for persistence of DENV during the interepidemic period of the disease.
In 2008, a study was conducted by Rohani et al., on persistence of transovarial DENV-2 in a Selangor strain of Aedes aegypti mosquitoes. The infected mosquitoes were reared to the seventh generation; each generation was screened for the virus using immunological staining methods. The virus was detected up to the fifth generation. The study concluded that DENV-2 can be transmitted transovarially by Aedes aegypti mosquitoes until the fifth generation under laboratory conditions.
Another study by Thenmozhi et al., from Kerala, India, was carried out to detect transovarial transmission by Aedes albopictus in 2007. Samples showed positivity for DEN-2 strain collected in dry season. Enzyme-linked immunosorbent assay (ELISA) and IFA are the methods utilised in the detection process.
A study on natural vertical transmission of DENV by Aedes aegypti in Chennai (India) was carried out by Arunachalam et al., in 2008. Mosquitoes were found positive for DENV-2 and DENV-3 strain. High infectivity of males in dry season was reported. Transmission was mainly observed in summer months when dengue infections in humans are reported less.
From the North-eastern (NE) part of India, DENV activity has been documented in Assam, Arunachal Pradesh and Nagaland., Entomological survey carried out in different time periods reveals the prevalence of potential dengue vectors in this region.,,,, All the seven states of the NE region of India are shown to be rich in known dengue vectors, namely, Aedes aegypti and Aedes albopictus. There have been no reports in the states about the study conducted for determining the transmission potential of dengue vectors prevailing in the region despite dengue cases reported earlier. It is necessary to conduct a study on transovarial transmission of DENV in Aedes aegypti and Aedes albopictus and to look for the potential vector species capable of transmitting the virus into successive generations and finally to suggest a suitable species-specific control.
The climate of Assam is typically 'tropical monsoon rainfall' type, with high levels of humidity and heavy rainfall. Its weather is characterised by heavy downpour and humidity. The hilly areas usually experience subalpine climatic condition, while excessive sultriness is observed in the plain lands of Assam. Although summer, winter and monsoons are the three seasons that visit the state, rainy season marks the most of the months of a year. However, temperature never goes beyond 35°C–38°C even in the summer months. The weather completely supports the breeding site for mosquitoes and as stated above, the DENV activity has been reported in Assam and other states of NE part in previous years. The disease is slowly re-emerging in the state which urges the need to carry out a detailed study about the root of causing the disease and to suggest a control strategy.
A study was conducted by Dutta et al., on distribution of potential dengue vectors in major townships along the national highways and trunk roads of NE India in 1998. During the study, surveys were conducted to detect breeding of Aedes mosquitoes in used/waste tire dumps piled outdoors by the tire repairing shops during summer season of 1996–1997. Breeding of both the potential vectors of dengue, namely, Aedes aegypti and Aedes albopictus were detected, prevalence rate being in the range of 30.0–88.0 (percentage of water-holding containers infested with larvae or pupae-container index value). The study revealed the preponderance of Aedes aegypti was considerably much higher than that of Aedes albopictus and the urban and semi-urban areas coming up along the side of the roads were observed to be infested with Aedes aegypti. The study indicates that waste tire dumps in every urban agglomeration should receive primary attention in view of their relative contribution to the abundance and dispersal of these vector mosquitoes.
Again another study conducted by Dutta et.al., on Solid waste pollution and breeding potential of dengue vectors in an urban and industrial environment of Assam in the year 1999. During the study period, solid waste pollution and its potential as a health hazard for vector-borne diseases were investigated in Assam. An entomological survey was conducted to evaluate the breeding potential of Aedes mosquitoes - the vector of dengue in different container habitats originating from solid waste materials frequently dumped. Profuse breeding of dengue vectors, namely, Aedes aegypti and Aedes albopictus has been detected in such solid waste materials which store rainwater. The study revealed that besides the air coolers in cities, the solid waste pollution is the major contributing factor in urban and industrial environments for the increase of the population density of the container breeding mosquitoes, thereby causing annoyance as well as posing a severe threat of transmitting DENV.
| ~ Conclusion|| |
It has been clear from the studies across the world that transovarial transmission of DENV by the primary vector of dengue Aedes aegypti is an ongoing phenomenon playing a significant role in interepidemic period. However, documentation of vertical transmission by Aedes albopictus could create an alarming situation as the vector is highly prevalent in North-East region of India along with other states in the country due to its favourable geographical habitats availability. Laboratory studies on transmission potential by both the vectors of dengue could help in better understanding of the potential species involved in the disease transmission. Previously, IFA and virus inoculation in Toxorhynchites mosquito were the virus detection methods available which demands expertise in mosquito inoculation techniques. However, with the advancement of viral diagnostic techniques such as ELISA and real-time PCR, more precise detection of virus serotype and copy number could be documented. However, the number of mosquitoes for pooling still varies and majority of studies reported more than ten numbers per pool which leads to approximate detection. Furthermore, temperature is an important factor which plays a major role in DENV transmission. Studies utilising temperature as a variable, to know the highest and the lowest temperature at which virus could be detected in mosquitoes and its transovarial transmission potential at these temperatures will enhance our knowledge on vector virus interaction. As transovarial transmission by available vector species in a dengue endemic setting could be the key etiological phenomenon responsible for re-emergence of disease from interepidemic to epidemic phase of disease onset, therefore, detail studies on this aspect may prove helpful in predicting the severity of the outbreak and designing species-specific control measure.
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Conflicts of interest
There are no conflicts of interest.
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