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Review on transovarial transmission potentiality of dengue vectors: An

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DOI: 10.4103/ijmm.IJMM_16_64

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 Impact Factor® for 2016: 1.149 ISSN 0255-0857

Volume 35 Number 3 July-September 2017

Indian Journal of
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Medical Microbiology
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• July-September 2017
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 Review Article

Review on Transovarial Transmission Potentiality of Dengue

Vectors: An International Perspective With Special Reference to
North-Eastern Region of India
Monika Soni, Jitendra Sharma1
Centre for Studies in Biotechnology, Dibrugarh University, Dibrugarh, 1District Surveillance Unit, Office of The Joint Director of Health Services, Lakhimpur, Assam, India

Abstract
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

Introduction after several weeks of incubation at room temperature which

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.[1] It infects 50–100 million people
worldwide in a year, leading to half million hospitalisations[2]
and approximately 12,500–25,000 deaths.[3] DENV is an RNA
virus of the family Flaviviridae; genus Flavivirus.[4] 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.[5]
DENV is transmitted to humans by Aedes mosquitoes, and
the two most frequent vector species are Aedes aegypti and
Aedes albopictus.[6]
Dengue epidemic tends to coincide with the rainy season
as significant increases in mosquito larval populations were
seen during this season.[7] Furthermore, ambient temperature
and relative humidity also plays an important role in viral
propagation in mosquitoes.[8] Apart from this, the infected
mosquitoes can transmit the virus transovarially[9] and eggs
from infected female increase the vertical transmission even
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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.[10]
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
Address for correspondence: Dr. Jitendra Sharma,
District Surveillance Unit, Office of The Joint Director of Health Services,
Lakhimpur - 787 001, Assam, India.
E‑mail: jitendra.du.biotech@gmail.com
This is an open access article distributed under the terms of the Creative Commons
Attribution‑NonCommercial‑ShareAlike 3.0 License, which allows others to remix, tweak,
and build upon the work non‑commercially, as long as the author is credited and the
new creations are licensed under the identical terms.
For reprints contact: reprints@medknow.com

How to cite this article: Soni M, Sharma J. Review on transovarial

DOI: transmission potentiality of dengue vectors: An international perspective
10.4103/ijmm.IJMM_16_64 with special reference to North-Eastern region of India. Indian J Med
Microbiol 2017:35;355-60.

© 2017 Indian Journal of Medical Microbiology | Published by Wolters Kluwer - Medknow 355
 Soni and Sharma: A future approach towards transovarial transmission study of dengue vectors in NE states of India
is approximately 12–16 days,[11] 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 used in 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
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.[12] 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. [13]
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.[14] 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.,[15] in China
to observe the transovarial transmission of DENV by
356 Indian Journal of Medical Microbiology  ¦  Volume 35  ¦  Issue 3  ¦  July-September 2017
Aedes aegypti and Aedes albopictus mosquitoes. Parental
females of Aedes albopictus and Aedes aegypti were orally
infected with DEN1‑4 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 DEN1-4.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., [16] 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., [17] 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[18] 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.,[19] 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.,[20] 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.,[21] on natural vertical transmission
 Soni and Sharma: A future approach towards transovarial transmission study of dengue vectors in NE states of India
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.[22] 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.[23] 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[24] 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
Indian Journal of Medical Microbiology  ¦  Volume 35  ¦  Issue 3  ¦  July-September 2017
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.[25] 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
357
 Soni and Sharma: A future approach towards transovarial transmission study of dengue vectors in NE states of India
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.,[26] 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.,[16] 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.,[27] 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.,[28] 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.[29,30] Entomological survey carried out in different
time periods reveals the prevalence of potential dengue vectors
in this region.[31‑35] 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.[36] 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
358 Indian Journal of Medical Microbiology  ¦  Volume 35  ¦  Issue 3  ¦  July-September 2017
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.,[32] 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.,[34] 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
 Soni and Sharma: A future approach towards transovarial transmission study of dengue vectors in NE states of India
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.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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360 Indian Journal of Medical Microbiology  ¦  Volume 35  ¦  Issue 3  ¦  July-September 2017

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