Acta Tropica 153 (2016) 2127

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Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica

An epidemiological study of dengue in Delhi, India

Kumar Vikram a , B.N Nagpal a, , Veena Pande b , Aruna Srivastava a , Rekha Saxena a ,
Anup Anvikar a , Aparup Das a , Himmat Singh a , Anushrita a , Sanjeev K. Gupta a , N.R. Tuli c ,
Olivier Telle d , N.K. Yadav c , Neena Valecha a , Richard Paul d
a

National Institute of Malaria Research (ICMR), Delhi, India

Kumaun University, Nainital, India
Municipal Corporation of Delhi, India
d
Institut Pasteur, Paris, France
b
c

a r t i c l e

i n f o

Article history:
Received 5 June 2015
Received in revised form
19 September 2015
Accepted 27 September 2015
Available online 1 October 2015
Keywords:
Dengue
Index case
Asymptomatic infection
Primary dengue infection
Secondary dengue infection

a b s t r a c t
Delhi, the capital of India, is an important metropolitan hub for major nancial and sociocultural
exchanges, offering challenging threats to current public health infrastructure. In recent past, an upsurge
of dengue cases in Delhi posed a signicant menace to the existing dengue control policies. To reform
the control strategies and take timely intervention to prevent future epidemics, an epidemiological study
on the proportion of both asymptomatic and symptomatic dengue infections in selected population was
conducted. The aim of the study was to investigate and assess the epidemiology of dengue infection and
to estimate the proportion of asymptomatic and symptomatic dengue infections in Delhi. In this study,
around 50 conrmed dengue cases, a total of 2125 individuals as household and neighbourhood contacts,
with or without dengue febrile illness, were nger pricked and serologically detected as dengue positive
or negative using SD Duo Bioline Rapid Diagnostic Test (SD Inc, Korea) with NS1, IgM & IgG combo test,
which detected dengue virus antigen and antibodies to dengue virus in human blood. Out of 2125 individuals, 768 (36.1%) individuals showed positive dengue test with past (25.5%), primary (1.88%) or secondary
(8.8%) dengue infections. Higher percentage of IgG was found in age groups 1524 years and 2550 years
(36% each). Infants (<1 year) presented higher incidence of new infections (22% of NS1 + IgM positives) as
compared to adults. Further analysis revealed that out of the 226 newly infected cases (including NS1 and
IgM positives), 142 (63%) were asymptomatic and 84 (37%) were symptomatic, as per WHO guidelines.
Our ndings also suggest that out of the total population screened, 10.6% dengue infection was either
primary or secondary. On the basis of these results, it may be hypothesized that there are large number of
asymptomatic dengue infections in the community as compared to reported symptomatic cases in Delhi.
For the effective control of dengue transmission in such community like Delhi where dengue epidemics
have frequently been encountered, it is essential to ascertain the proportion of asymptomatic dengue
infections which may act as a reservoir for dengue transmission, as well as threat for developing dengue
haemorrhagic fever (DHF).
2015 Published by Elsevier B.V.

1. Introduction
Dengue infection is one of the most common arbo-viral diseases
worldwide. It is prevalent in most of the tropical and sub-tropical
countries and is caused by four serotypes (DEN-1, DEN-2, DEN-3
and DEN-4) in humans. All four serotypes can cause a spectrum
of illness ranging from inapparent or mild febrile dengue fever to

Corresponding author at: GIS, Taxonomy and OVBD Division, National Institute
of Malaria Research, New Delhi 110 077.
E-mail address: bnnagpal57@gmail.com (B.N Nagpal).
http://dx.doi.org/10.1016/j.actatropica.2015.09.025
0001-706X/ 2015 Published by Elsevier B.V.

severe and fatal haemorrhagic disease (Gubler, 1998; Whitehorn

and Farrar, 2010; Innis, 1995). It is transmitted mainly by Aedes
aegypti mosquito and also by Aedes albopictus (Whitehorn and
Farrar, 2010). Dengue fever represents high disease burden in
endemic countries (Gubler and Meltzer, 1999; Beatty et al., 2011;
Donald et al., 2013). An estimated 3.6 billion people live in high risk
areas worldwide. It is also presumed that over 230 million bear the
load of infection and approximately 2 million suffer with dengue
fever and its severe forms with 21,000 deaths as reported (Beatty
et al., 2008).
The incidence of dengue fever (DF) and dengue hemorrhagic fever (DHF) has increased dramatically over the last four

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K. Vikram et al. / Acta Tropica 153 (2016) 2127

decades and approximately 50% of worlds population is at risk of

dengue virus infection (DENV) (Bennett et al., 2003; World Health
Organization, 1997,2004). High proximity of densely populated
areas provides ample opportunities for the transmission of diseases. Asias contribution is 70% (approx 67 million) toward the
apparent infections in the comprehensive global disease burden.
India contributes 34% to the global infection which amounts to
about 33 million infections (Chakravarti et al., 2012; Wichmann
et al., 2011; Kakkar, 2012). The prolic increase in incidence rate
over last decade has been connected to societal changes such as
population growth and increasing urbanization. Human population
(likely including infected hosts) and domestic & international travelers are constantly introducing new vectors and pathogens into
novel geographical areas.
DENV infection is endemic in many parts of India, and epidemics
are more frequent. Out of last six years, 2013 witnessed the worst
dengue outbreak in India with 75,808 dengue cases and 193 deaths
as reported by National Vector Borne Disease Control Programme
(NVBDCP). Since 1967, Delhi has experienced several outbreaks of
DENV infection (Broor et al., 1997; Dar et al., 1999) with the last
reported 5574 cases by Municiple Corporation of Delhi (MCD) in
2013. The DENV infection often shows no clinical manifestations
or mild illness in humans and is referred to as asymptomatic or
inapparent DENV infection (Simmons et al., 2012; World Health
Organization, 2009; Endy et al., 2011).
Currently, we know very little about the epidemiology of
subclinical infections such as frequency, factors determining the
symptomatic/asymptomatic outcome of infection, infectivity to
mosquitoes, duration of infection from symptomatic episode. The
role of individuals with asymptomatic infection in spreading the
virus needs to be addressed. Such epidemiological information
is crucial to predict local dengue epidemiology as asymptomatic
DENV infection represents dengue disease burden that goes undetected (Halstead et al., 1969; Deller et al., 1967). Bhatt et al.
estimated 96 million apparent DENV infections and 217392 million inapparent infections worldwide in 2010 (Bhatt et al., 2013).
Thus the estimation of disease burden has been identied as one of
important factors essential before the introduction of newly developed vaccines in a population (Mahoney and Maynard, 1999). The
data on disease burden provides the rationale for effective decision making to properly allocate resources, both with respect to
the needed regions for a specic disease and region with relative
burden of various diseases.
The present study has included household and neighbourhood
contacts of an index case to enable us to determine the proportion
of asymptomatic and symptomatic infections in the community.
These ndings of the study would assist in formulation of policy
for appropriate control of disease in Delhi.

2. Materials & methods

2.1. Study sites
The National Capital Territory of Delhi covers an area of
1484 km2 (573 sq mi), of which 783 km2 (302 sq mi) is designated
rural and 700 km2 (270 sq mi) urban, therefore, making it the
largest city in terms of area in the country (Mohan, 2002). According
to the 2011 Census of India, the population of Delhi is 16,753,235
(Census of India, 2011). The corresponding population density was
11,297 persons per km2 , with a sex ratio of 866 women per 1000
men, and a literacy rate of 86.34% (Economic Survey of Delhi
20052006). In Delhi, due to migration of 6.87 lakhs (approx) people from 2001 to 2011, the population has increased and this has
made Delhi as one of the fastest growing cities in the world (Economic Survey of Delhi, 201213).

The study was conducted in collaboration with Pasteur Institut, Paris, France and Municipal Corporation of Delhi (MCD). MCD
assisted in selection of 18 localities (suburbs) and their categorization as Low, Medium and High income group on the basis of socio
economic status, family annual income and housing pattern dened
by Delhi Development Authority (DDA). Six localties each from Low
Income Group (LIG) i.e. Mangolpuri, Budha Vihar, Prem Nagar, Hastsal Village, Najafgarh (Jai Vihar), Sangam Vihar; Medium Income
Group (MIG) i.e. Bapanagar, Madhu Vihar, Palam Colony, Kotala
MubarkPur, Raghubir Nagar, Rani Garden and High Income Group
(HIG) i.e. Paschim Vihar, Rajouri Garden, RK Puram, Kirti Nagar,
Vasant Kunj, Mukherjee Nagar were selected, as shown in the map
(Fig. 1).
2.2. Study design
A community based descriptive study was conducted in the
identied localities during the period June December, 2013. For
the diagnosis of dengue cases, MCD had identied 37 sentinel
hospitals in Delhi to facilitate management of such cases. Fifty conrmed cases of dengue reported by these sentinel hospitals, from
the identied 18 localities, covering maximum zones of Delhi, were
investigated. For the purpose of the study, index case is dened
as any serologically positive dengue case reported by MCD. After
the identication of index cases, all household and neighbourhood
contacts of a dengue case were screened for asymptomatic DENV
infection. Household contacts i.e. the index case and co-habiting
family members and neighborhood contacts i.e. those residents
living in close vicinity (within 200 m radius of the index case)
were included in the study (Mammen et al., 2008). Symptomatic
DENV infection was dened as fever with at least two symptoms of dengue (myalgia, headache, retro-ocular pain, arthralgia
and rash) as per WHO guidelines (World Health Organization,
2009). Asymptomatic DENV infectionno clinical signs or symptoms of disease as mentioned above in symptomatic infection
(World Health Organization, 2009).
The aim and procedure of the study was briey described to
all the participants and their legal guardians prior to taking their
consent for the enrollment in this study. Upon enrollment, ngerprick blood samples were obtained from all consenting individuals
and serologically tested. Each individual was also administered a
questionnaire including presence or absence of any dengue like
symptoms. All serologically positive symptomic dengue infections
were reffered to respective sentinel hospitals for further management while individuals with asymptomatic infections were
provided appropriate counselling.
2.3. Serological test
The rapid detection of DENV infection was performed by commercially available kits provided by Pasteur Institut, Paris, France.
Total 2125 individuals (household and neighborhood individuals)
with or without dengue febrile illness, were nger pricked and
serologically diagnosed as dengue positive or negative by using
SD BIOLINE Dengue Duo combo device (Standard Diagnostic Inc.,
Korea). The kit provides two windows, one detection of NS1 antigen and other for dengue specic IgM and IgG antibodies. All tests in
this study were carried out in accordance with the manufacturers
instructions and results were examined and interpreted accordingly; the blood sample of individuals containing IgM or/and NS1
were considered as primary/acute dengue infection, i.e. they were
infected by DENV for the rst time. The tests indicating IgG + IgM/
NS1 were considered as secondary infection, i.e. such patient was
already infected by dengue in past. If the individual was detected
positive for IgG but negative for other tests (IgM and NS1), were
considered as past infection or secondary DENV infection with

K. Vikram et al. / Acta Tropica 153 (2016) 2127

23

Fig. 1. Map of Delhi showing 18 localities included in the study.

symptoms. The presence color line (control) in each result window indicates a negative result. NS1 antigen is found from the rst
day and up to 9 days after onset of fever in sample of primary or
secondary dengue infected patients. Usually IgM does not become
detectable until 510 days after the onset of illness in cases of primary dengue infection and until 45 days after onset of illness in
secondary infections. In primary infections, IgG appear the 14th day
and persist for life. Secondary infections show that IgG rise with in
12 days after the onset of symptoms and induce IgM response
after 20 days of infection (as per SD Bioline Dengue Kit manual).
Limitation of the study: Those individuals in which only IgG
was found positive but without any symptoms of DENV infection
were considered as past infections, while those having symptoms
of DENV infection were considered as secondary infections.

2.4. Entomological surveys

A house-to house entomological survey was carried out in order
to detect A. aegypti breeding in all containers in domestic and
peridomestic areas of all selected localities by standard (WHO)
entomological techniques. The larvae were collected from each
locality, by using dipping and pipetting methods and emergence
was done in laboratory. The emerged adult mosquitoes were identied by using the standard keys of Barraud (1934). The House index
(HI), Breteau index (BI), Container index (CI) and Pupal index (PI)
were also calculated from these localities.

2.5. Statistical analysis

The data was entered in Excel 2007 and SPSS software package
(version 20) was used for statistical analysis. Group comparison for
prevalence of IgG and IgM and other clinical symptoms was done
using ANOVA.Odds ratio was calculated to ascertain the odds of
getting asymptomatic patients in three income groups.

3. Results
A total of 2125 individuals as household and neighbourhood
contacts consisted of 932 males and 1193 females from 18 localities
against the 50 index cases of Delhi were tested and analyzed with
the NS1IgMIgG RDT kit. The data was further grouped into three
income groups i.e. High, Medium and Low. In LIG 711 individulas
comprised of 314 males and 397 females, in MIG 870 individuals
comprised of 374 males and 496 females, in HIG 544 individulas comprised of 244 males and 300 females were serologically
tested for dengue infection. Out of total 2125 individulas tested, 768
individualscomprising 59% (451/768) females and 41% (317/768)
maleswere found positive for either IgG, IgM or NS1 test. We
noted that sero-prevalence of the DENV infection was equal to
36.14% of all tested individuals (768/2125). Out of the these, 542
(25.5% of all individuals tested) cases were past infections as they
were only IgG positive without any symptoms, 40 primary infections (1.88%) and 186 (8.8%) secondary dengue infections. Total 226
individuals(29.4%) were found positive for either primary or secondary dengue infection. It is to note that 63% of the primary and
secondary infections were asymptomatic(Table 1).
The study showed that individuals people in the age group of
1524 and 2550 had maximum (36% each) past or secondary infections. Individuals aged >50 years and young children aged 914
years had 35% past or secondary infections. Infants <1 year old
showed least (17%) past or secondary infections. On the contrary,
primary infection was found highest (22%) in the age group <1
year old. The proportion of primary cases generally declined with
increase in age (Fig. 2).
Out of 711 individuals tested from LIG, 212 were past infection
and 103 were primary/secondary out of which 72 were asymptomatic infections. For MIG, 232 were past infections and 81 were
either primary or secondary out of which 45 were asymptomatic.
While for HIG, 98 were past infections, 42 were either primary or
secondary out of which 25 were asymptomatic. Odds of getting
asymptomatic DENV infections in three income groups was esti-

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K. Vikram et al. / Acta Tropica 153 (2016) 2127

Table 1
Number and percentage of test positives to IgG, IgM and NS1 tests.
Test positives

No. of individuals

% of total

Sympt. (S)

Asympt. (AS)

Category of infection

Asymptomatic (per category) %

IgG
NS1
IgM
NS1 + IgM
IgM + IgG
NS1 + IgG
NS1 + IgM + IgG
IgG
Negative results

542
16
23
1
118
1
5
62
1357

25.5%
0.75%
1.08%
0.05%
5.55%
0.05%
0.24%
2.9%
63.86%

3
4
1
13
0
1
62

13
19
0
105
1
4

Past infection
Primary
infection
Secondary
infection

80%

Total

2125

100%

84

142

59%

63%

Fig. 2. Percentage of IgG and IgM or/and NS1 positive per age group.

mated. The odds of getting asymptomatic infections in LIG was 1.85

times greater than MIG (OR = 1.85, 95% CI- 1.013.41). The odds of
getting asymptomatic infections in HIG was 1.7 times greater than
MIG (OR = 1.17, 95% CI- 0.552.50). While comparing High Income
group to Low income it was found that odds of getting asymptomatic infections in LIG was 0.63 times greater than HIG (OR = 0.63,
95% CI- 0.301.33).
Further analysis of the spread over gender and various age
groups was performed and it was found that both symptomatic and
asymptomatic patients were found maximum in females belonging
to the age group of 2550 years (Fig. 3).
For 50 index cases, 155 individuals were included in household study and 1970 individuals were included in neighborhood
study. Out of 155 individuals in household study, 95 (61.3%) were
found test positive either for IgG, IgM or NS1 and of these 75 were
IgG positive indicating past infections and rest 20 were primary
or secondary infections. Of the total positive cases, 13 were asymptomatic (65%) & 7 (35%) were symptomatic. In neighborhood study,
out of 1970 individuals, 673 (34%) were tested positive either for
IgG, IgM or NS1 and out of which 467 were IgG positive. In other
words, out of 1970 individuals tested, 23.7% had past infections
and rest 206 (10.5%) were either primary or secondary infections
with 129 asymptomatic (63%) & 77 (37%) symptomatic infections.
The difference of asymptomatic and symptomatic infections in
both household and neighbourhood contacts was not signicant
(X2 = 0.04 (1), p < .05 = 0.83).
Data collected for 18 localities was pooled for 3 income groups
and 6 localities each were binned as per income groups. Between
the groups ANOVA was conducted to study the difference in prevalence of clinical symptoms. A signicant difference for myalgia
(p = 0.04) and insignicant difference in rashes, severe headache,

retro-orbital pain (p > .05) inferred that rashes, severe headache

and retro-orbital pain were commonly observed in all three income
groups. Although the independent between groups ANOVA yielded
a signicant difference in prevelance of IgM F (2,2122) = 18.163,
p = .000 as well as IgG F (2,2122) = 22.447, p = .000 inferring that
prevelance of primary/ past or secondary dengue infections varied
among these income groups
All localities were found positive for A. aegypti mosquitoes irrespective of their income group but breeding was higher in low
income group. In HIG, the observed annual HI, BI, CI and PI were
3.22, 7.41, 3.44 and 0.91 respectively. In MIG, the observed annual
HI, BI, CI and PI were 4.33, 8.45, 4.14 and 1.21 respectively. Similarly, in LIG, annual HI, BI, CI and PI were calculated as 4.54, 9.45,
5.08 and 1.51.

4. Discussion
In present study, we have demonstrated that IgG was positive in
34.2% of all tested individuals (either past or secondary infections).
This is less than the percentage detected in Kolkata, where 73.51%
of tested individuals from 2005 to 2007 were IgG positive (Hati,
2009). In Rio de Janeiro (Honorio et al., 2009) similar percentage of
past antibodies were found in the population (between 67 and 85%
of positives IgG). This shows that population of Delhi has been less
exposed to dengue virus than some of other high endemic cities.
We can observe that with the increasing age of the individuals,
the positivity for IgG increased accept in age group >50 indicating
the past exposure of dengue infection. On the other hand the new
infection was observed more in young children and declined with
the advancement of age.

K. Vikram et al. / Acta Tropica 153 (2016) 2127

25

Fig. 3. Proportion of symptomatic and asymptomatic cases over various age groups in males and females.

Fig. 4. Mean lowest temperature recorded during day in Rio (Brasil), Bangkok (Thaland), Kolkata and Delhi (India).

The lesser proportion of past infections can be linked to climatic

factors. Urban areas like Kolkata, Bangkok or Rio de Janeiro have
relatively high temperatures during inter epidemic season (Fig. 4),
while Delhi experiences very low temperatures (under 15 C) during winter i.e. interepidemic season (November February). This
cold temperature impacts vector abundance and its ability to transmit virus during interepidemic period. Considering the extreme
temperature during summer (when temperature is above 45 C),
the temporal window for dengue virus to spread is observed to be
considerably less in comparison to other cities where round the
year transmission is observed (along with strong peaks as seen
after monsoon period). This conrms that Delhi reports more cases
with an efcient surveillance system as compared with other indian
cities (Mumbai, Chennai, Kolkata) which are ofcialy less affected
but have a favourable climatic environment for round the year
transmission. On the contrary, population of Delhi poses lesser
immunity to the virus. Hence future consequences can be bigger
than what was observed as temperature continues to rise during
winter seasons opening new avenues to the DENV.
Another important outcome of our study is to reveal the large
share of asymptomatic infections compared with symptomatic

infections. These results infer similar rate of asymptomatic DENV

infections as reported in previous studies carried out in Thailand,
Singapore (ratio of asymptomatic/symptomatic infections between
2:1 and 10:1) (Burke et al., 1988; Wilder-Smith et al., 2009) and also
with the ndings of other countries that large proportion of dengue
cases being asymptomatic which might lead to silent transmission
of the disease (Chen et al., 1996; Teixeira et al., 2002). Thus, on
the basis of these surveys its reasonable to say that the ratio of
asymptomatic/symptomatic DENV infection varies extensively. In
our study the type of infecting DENV was not determined since only
serologic testing was performed.
In dengue, the asymptomatic cases are more frequent than
the symptomatic cases although their role as potential reservoir is not known but their relative number varies according to
the geographical areas, the epidemiological context and individual immunological attributes as exemplied by different surveys
(Balmaseda et al., 2006; Halstead, 2006). In contrast, another
prospective study was conducted in Kamphaeng Phet, Northern Thailand, between 1998 and 2000 and the incidence of
asymptomatic DENV infection was reported nearly equal to the
symptomatic infections (Endy et al., 2002).

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K. Vikram et al. / Acta Tropica 153 (2016) 2127

To assess the eventual role of asymptomatic DENV infections

in the transmission of this disease, the quantication of viremia
level in such cases is important and remains to be evaluated. In
Singapore, Health authorities suggested that it is likely, although
its not proven that viremia is lower and shorter in duration in
asymptomatic persons than in symptomatic persons (WilderSmith et al., 2009). In another study which was performed in
Cambodia during 2006 and 2007, authors stated that the level
of viremia in asymptomatic DENV infections was not signicantly
lower than in all dengue conrmed cases (p = 0.145) (Duong et al.,
2011). On the basis of this study we can hypothesize that viremia
level of some asymptomatic DENV infections match the lowest level
of viremia of symptomatic cases. Keeping this thing in mind, it is
logically possible that such asymptomatic DENV infections can act
as source of new foci for disease transmission, if competent Aedes
mosquito colonies are existing in the areas with high asymptomatic
DENV infections. This nding illustrates the complexity of DENV
transmission in a population and the potential of asymptomatic
DENV infections to existing burden. Our results also showed that
the rate of secondary infection (8.7%) is 4.5 folds higher than that
of primary infection (1.8%) which indicates that these cases are
at higher risk of getting dengue haemorrhagic fever (DHF)/dengue
shock syndrome (DSS) (Vaughn et al., 2000).
Annually, approximately 70,000 people migrate to Delhi from
other states for personal economic progress. The rapid urbanization and development in Delhi provides ample opportunities for the
poor, semiskilled and unskilled rural population resulting in their
demand in secondary and tertiary economic sector. Such population is pulled in cities like Delhi and are forced to reside in extremely
unhygienic, unauthorized & slums designated areas. High volume
of human migration leads to unplanned urbanization in these areas
lacking adequate facilities & infrastructure for water supply and
waste management (Economic Survey of Delhi, 201213).
In recent years, the risk of dengue in Delhi has increased due
to poor water management leading to improper water storage
practices in such areas. A. aegypti, readily exploits such water
storage containers as larval habitats leading to proliferation of
Aedes-breeding sites (Vikram et al., 2015a,b). Such factors play
an important role in increasing the incidence of dengue fever
(Millennium Ecosystem Assessment Report, 2005). The intermittent supply of water, increasing numbers of water storage
containers and improper solid waste management are the major
concerns for dengue and vector control programmes in city of Delhi
which would need social mobilization at large for community participation for effective control of dengue.

5. Conclusion
The main aim of this study was to identify the proportion of
asymptomatic DENV infection in localities of Delhi. On the basis of
our data, we estimated the proportion to be 63% among individuals
of all 18 localities of Delhi. The risk of acquiring DENV infection is
signicantly higher in residents of low income group as compared
to medium income groups and high income groups of Delhi. Our
ndings suggests that 10.6% of the total population screened confered DENV infection either primary or secondary. On the basis of
these results, we can hypothesize the unestimated dengue infection
shouldered by 1.6 million people residing in Delhi.
This study facilitated collection of clinical information and rapid
detection of DENV infection in Delhi metropolitan area. The results
of this study can be helpful in planning and implementing adequate preventative measures against DENV infection in the city of
Delhi. There is a need for further study to demonstrate the role
of asymptomatic dengue infection in transmission of DENV in the
community.

Ethics
The study protocol and consent forms were approved by the
Scientic Advisory Committee and Ethics Review Committee of the
National Institute of Malaria Research, New Delhi, India.
Acknowlegment
Authors are thankful to Paster Institut, Paris, France for the funding support ANR. We are also thankful to MCD for helping us in
selection of study sites in Delhi. We thank the entire eld staff
for their careful performance in serological testing and data collection. We would like to thank Ms Shruti Bahadur for giving her
critical overview to the manuscript. Acknowledgement is also due
to Mr. Mrityunjay Prasad and Mr. Rakesh Jacob for data management. Institute Publication Committee is acknowledged for giving
consent for publication of manuscript vide Approval No. 027/2015.
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