RESEARCH ARTICLE

Dengue infection in India: A systematic review

and meta-analysis
Parasuraman Ganeshkumar1, Manoj V. Murhekar1*, Veeraraghavadoss Poornima2,
Velusamy Saravanakumar1, Krishnendu Sukumaran2, Anandan Anandaselvasankar2,
Denny John3, Sanjay M. Mehendale4
1 Department of Epidemiology, National Institute of Epidemiology, Chennai, Tamil Nadu, India, 2 School of
Public Health, Jawaharlal Institute of Postgraduate Medical Education and Research, Puducherry, India,
3 Campbell Collaboration, New Delhi, India, 4 Division of Epidemiology and Communicable Diseases, Indian
Council of Medical Research, New Delhi, India
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* mmurhekar@[Link]
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a1111111111
a1111111111 Abstract

Introduction
OPEN ACCESS
Dengue is the most extensively spread mosquito-borne disease; endemic in more than
Citation: Ganeshkumar P, Murhekar MV, Poornima 100 countries. Information about dengue disease burden, its prevalence, incidence
V, Saravanakumar V, Sukumaran K,
and geographic distribution is critical in planning appropriate control measures against
Anandaselvasankar A, et al. (2018) Dengue
infection in India: A systematic review and meta- dengue fever. We conducted a systematic review and meta-analysis of dengue fever in
analysis. PLoS Negl Trop Dis 12(7): e0006618. India
[Link]

Editor: Isabel Rodriguez-Barraquer, University of

California San Francisco, UNITED STATES Methods
Received: November 7, 2017 We searched for studies published until 2017 reporting the incidence, the prevalence or
case fatality of dengue in India. Our primary outcomes were (a) prevalence of laboratory
Accepted: June 19, 2018
confirmed dengue infection among clinically suspected patients, (b) seroprevalence in the
Published: July 16, 2018
general population and (c) case fatality ratio among laboratory confirmed dengue patients.
Copyright: © 2018 Ganeshkumar et al. This is an We used binomial–normal mixed effects regression model to estimate the pooled proportion
open access article distributed under the terms of
of dengue infections. Forest plots were used to display pooled estimates. The metafor pack-
the Creative Commons Attribution License, which
permits unrestricted use, distribution, and age of R software was used to conduct meta-analysis.
reproduction in any medium, provided the original
author and source are credited.

Data Availability Statement: All relevant data are

Results
within the paper and its Supporting Information Of the 2285 identified articles on dengue, we included 233 in the analysis wherein 180
files.
reported prevalence of laboratory confirmed dengue infection, seven reported seropreva-
Funding: The study was funded by the Department lence as evidenced by IgG or neutralizing antibodies against dengue and 77 reported case
of Bio-technology, Govt of India. The funders had
fatality. The overall estimate of the prevalence of laboratory confirmed dengue infection
no role in study design, data collection and
analysis, decision to publish, or preparation of the among clinically suspected patients was 38.3% (95% CI: 34.8%–41.8%). The pooled esti-
manuscript. mate of dengue seroprevalence in the general population and CFR among laboratory con-
Competing interests: The authors have declared firmed patients was 56.9% (95% CI: 37.5–74.4) and 2.6% (95% CI: 2–3.4) respectively.
that no competing interests exist. There was significant heterogeneity in reported outcomes (p-values<0.001).

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 Systematic review and meta-analysis of dengue fever in India

Conclusions
Identified gaps in the understanding of dengue epidemiology in India emphasize the need to
initiate community-based cohort studies representing different geographic regions to gener-
ate reliable estimates of age-specific incidence of dengue and studies to generate dengue
seroprevalence data in the country.

Author summary
Dengue fever, an extensively spread mosquito-borne disease, is endemic in more than 100
countries. Information about dengue disease burden, its prevalence and incidence and
geographic distribution is necessary to guide in planning appropriate control measures
including the dengue vaccine that has recently been licensed in a few countries. We per-
formed a systematic review and meta-analysis of published studies in India on dengue.
The overall estimate of the prevalence of laboratory confirmed dengue infection based on
testing of more than 200,000 clinically suspected patients from 180 Indian studies was
38.3%. The pooled estimate of dengue seroprevalence in the general population and CFR
among laboratory confirmed dengue patients was 56.9% and 2.6% respectively. There
were no community-based studies reporting incidence of dengue. Our review also identi-
fied certain knowledge gaps about dengue epidemiology in the country. Identified gaps in
the understanding of dengue epidemiology in India emphasize the need to initiate com-
munity-based cohort studies representing different geographic regions to generate reliable
estimates of age-specific incidence of dengue and studies to generate dengue seropreva-
lence data in the country.

Introduction
Dengue is the most extensively spread mosquito-borne disease, transmitted by infected mos-
quitoes of Aedes species. Dengue infection in humans results from four dengue virus serotypes
(DEN-1, DEN-2, DEN-3, and DEN-4) of Flavivirus genus. As per the WHO 1997 classifica-
tion, symptomatic dengue virus infection has been classified into dengue fever (DF), dengue
haemorrhagic fever (DHF) and dengue shock syndrome (DSS). The revised WHO classifica-
tion of 2009 categorizes dengue patients according to different levels of severity as dengue
without warning signs, dengue with warning signs (abdominal pain, persistent vomiting, fluid
accumulation, mucosal bleeding, lethargy, liver enlargement, increasing haematocrit with
decreasing platelets) and severe dengue [1,2,3]. Dengue fever is endemic in more than 100
countries with most cases reported from the Americas, South-East Asia and Western Pacific
regions of WHO [1]. In India, dengue is endemic in almost all states and is the leading cause
of hospitalization. Dengue fever had a predominant urban distribution a few decades earlier,
but is now also reported from peri-urban as well as rural areas [4,5]. Surveillance for dengue
fever in India is conducted through a network of more than 600 sentinel hospitals under the
National Vector Borne Disease Control Program (NVBDCP) [6], Integrated Disease Surveil-
lance Program (IDSP) [7] and a network of 52 Virus Research and Diagnostic Laboratories
(VRDL) established by Department of Health Research [8]. In 2010, an estimated 33 million
cases had occurred in the country [9]. During 2016, the NVBDCP reported more than 100,000

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 Systematic review and meta-analysis of dengue fever in India

laboratory confirmed cases of dengue [6]. It is therefore possible that dengue disease burden is
grossly under-estimated in India.
High dengue disease burden and frequent outbreaks result in a serious drain on country’s
economy and stress on the health systems. In India, case detection, case management, and vec-
tor control are the main strategies for prevention and control of dengue virus transmission [6].
A new dengue vaccine is now available and several vaccines are in the process of development
[10, 11, 12]. Information about dengue disease burden, its prevalence, incidence and geo-
graphic distribution is necessary in decisions on appropriate utilization of existing and emerg-
ing prevention and control strategies. With this background, we conducted a systematic
review and meta-analysis to estimate the disease burden of dengue fever in India. We also
reviewed serotype distribution of dengue viruses in circulation, and estimated case fatality
ratios as well as proportion of secondary infections.

Methods
Search strategy and selection criteria
This systematic review is registered in PROSPERO (Reg. No. CRD 42017065625). We searched
Medline (PubMed), Cochrane Central, WHOLIS, Scopus, Science Direct, Ovid, Google
Scholar, POPLINE, Cost-Effectiveness Analysis (CEA) Registry and Paediatric Economic
Database Evaluation (PEDE) databases for articles published up to 2017. The main search
terms included incidence, prevalence, number of reported cases, mortality, disease burden,
cost of illness, or economic burden of dengue in India. The complete search strategy is
described in S1 Appendix. Back referencing of included studies in bibliography was also done
to identify additional studies.

Review approach
The search results were initially imported to Zotero software (Version [Link]) and duplicate
records were removed. During title screening, we examined relevant studies from various
databases. Our inclusion criterion was studies reporting dengue infection in India, not
restricted to setting, design, purpose and population. Titles thus selected were subjected to
abstract screening. Studies were considered eligible for further examination in full text if their
abstracts reported incidence, prevalence, number of reported cases, mortality or the burden of
dengue fever anywhere in India. Studies reporting complications of dengue, serotype details of
dengue virus as well as seroprevalence of dengue were also included. Using a pre-designed
data extraction form, two reviewers extracted details from selected studies independently. The
data, which differed between the reviewers, were resolved by consensus. Information about the
year of publication, study setting (hospital/laboratory based, or community-based), study loca-
tion, study period, laboratory investigations, number of suspected patients tested and positives,
age distribution of cases, and details of dengue serotypes were abstracted (S1 Dataset).
The primary outcome measures of interest were (a) prevalence (proportion) of laboratory
confirmed dengue infection among clinically suspected patients in hospital/laboratory based
or community-based studies, (b) seroprevalence of dengue in the general population and
(c) case fatality ratio among laboratory confirmed dengue patients. The diagnosis of acute den-
gue infection among the clinically suspected patients was based on any of the following labora-
tory criteria: (a) detection of non-structural protein-1 (NS1) antigen, (b) Immunoglobulin M
(IgM) antibodies against dengue virus (c) haemagglutination inhibition (HI) antibodies
against dengue virus, (d) Real-time polymerase chain reaction (RT-PCR) positivity or (e) virus
isolation. Seroprevalence of dengue was based on detection of IgG or neutralizing antibodies
against dengue virus. Studies providing prevalence (proportion) of laboratory confirmed

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 Systematic review and meta-analysis of dengue fever in India

dengue infection among clinically suspected patients were classified into (a) hospital/labora-
tory-based surveillance studies and (b) outbreak investigations or hospital/laboratory-based
surveillance studies when the outbreak was ongoing in the area, as mentioned in the original
research paper. Studies regarding outbreak investigations considered an increase in number of
reported cases of febrile illness in a geographical area, as the criteria for defining an outbreak.
The outbreak investigations included one or more of the following activities: active search for
case-patients in the community, calculation of attack rates for suspected case-patients, confir-
mation of aetiology and entomological investigations. For the case fatality ratio, the numerator
included reported number of deaths due to dengue and denominator as laboratory confirmed
dengue patients.
Our secondary outcomes of interest were the following: (a) proportion of primary and sec-
ondary infections among the laboratory confirmed dengue patients. This classification was
made based on the information about dengue serology provided in the paper. Primary dengue
infection was defined as acute infection, as indicated by qualitative detection of NS1 antigen,
and/or IgM or HI antibodies or RT-PCR positivity and absence of IgG antibodies against den-
gue virus. A case of acute infection as defined above, in presence of IgG antibodies, was con-
sidered as secondary dengue infection [2,13,14]. Some of the studies used the ratio of IgG to
IgM antibodies as the criteria for differentiating primary and secondary infections [14]; (b)
distribution of predominant and co-circulating dengue virus serotypes; (c) proportion of
severe dengue infections based on WHO 1997 or WHO 2009 criteria [1,2]. The category of
severe dengue infection included patients with DHF and DSS as per the WHO 1997 classifica-
tion as well as severe dengue infections classified as per the WHO 2009 classification and
(d) cost of illness, which included reported direct and indirect costs associated with dengue
hospitalization.

Risk of bias
The risk of bias was assessed using a modified Joanna Briggs Institute (JBI) appraisal checklist
for studies reporting prevalence data [15] and essential items listed in the Strengthening the
Reporting of Observational Studies in Epidemiology (STROBE) checklist [16]. The criteria for
assessing bias primarily included methods for selecting participants, methods for laboratory
testing, and outcome variables (Supplementary file S2 Appendix).

Statistical analysis
We conducted quantitative synthesis to derive meta-estimates of primary and secondary out-
comes (severity of disease and primary/ secondary infections) and qualitative synthesis to
describe the serotype distribution and economic burden due to dengue. We followed Meta-
analysis of Observational Studies in Epidemiology (MOOSE) guidelines [17]. For each study,
primary outcomes (prevalence of acute infection, seroprevalence and CFR) were summarized
as proportion and their 95% confidence intervals were computed. We used logit and inverse
logit transformations for variance stabilization of proportions [18]. Binomial–Normal mixed
effects regression model was used to estimate the pooled proportion of dengue infections. For-
est plots were used to display pooled estimates. Heterogeneity was tested using likelihood ratio
test. Funnel plots with logit prevalence on x-axis and standard errors on y-axis and Egger’s
test were used to evaluate publication bias. Independent variables potentially associated with
the prevalence of laboratory confirmed dengue were included as fixed-effects in univariate
and multivariate binomial meta-regression models. P <0.05 was considered statistically signif-
icant. Sensitivity analysis was carried out by leaving out one study at a time in the order of

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 Systematic review and meta-analysis of dengue fever in India

publication to check for consistency of pooled estimates. Analyses were performed in the R sta-
tistical programming language using the ‘metafor’ package [19,20].

Results
Characteristics of included studies
The search strategy initially identified 2,285 articles from different databases. After removal of
duplicates, 1,259 articles were considered for title and abstract screening. Seven hundred and
forty-six articles were excluded for reasons provided in Fig 1. Thus, 513 articles were found to
be eligible for full-text review. After the review of full-text articles, 233 studies were included
for the analysis [21–253]. The details of the studies included in the review are provided in the
PRISMA flowchart (Fig 1). None of the studies reported incidence of dengue fever.

Primary outcomes
Prevalence (proportion) of laboratory confirmed dengue fever. Of the 233 studies
included in the analysis, 180 provided information about proportion of laboratory confirmed
dengue cases among clinically suspected patients [21–200]. This included 154 studies con-
ducted in hospital or laboratory setting [21–174] and 26 studies reporting outbreak investiga-
tions [175–200]. Of the 154 studies conducted in hospital/ laboratory setting, 40 were
conducted when an outbreak was ongoing in the area [135–74]. The diagnosis of acute dengue
infection was based on a single assay in 86 studies (IgM antibodies = 68, RT-PCR = 11, HI anti-
bodies = 4, virus isolation = 2, detection of NS1 antigen = 1) and more than one assay in 95
studies.
Case definitions used: Of the 154 studies conducted in hospital settings, WHO or NVBDCP
case definitions were used by 39 and 2 studies respectively. The remaining studies used case
definitions such as acute febrile illness/acute undifferentiated illness (n = 20), and clinically
suspected dengue fever (n = 93). Similarly, of the 26 reported outbreaks, investigators used
WHO or NVBDCP case definitions in 7 and 2 settings respectively, whereas acute febrile ill-
ness and clinically suspected dengue fever case definitions were used in 5 and 12 settings
respectively.
Place and time distribution of studies: Of the 154 studies conducted in hospital setting, 75,
41, 27 and 7 were from north, south, east and western Indian states respectively, whereas 3
studies were from north-eastern states. One study reported data from VRDL network, cover-
ing multiple regions in India [65]. Of the 26 outbreaks, most (10, 38.5%) were reported from
Southern states, followed by 9 (34.6%) in the north, 4 (15.4%) in the east, and 3 (11.5%) in the
north-eastern Indian states. Most (65, 42.2%) studies conducted in hospital settings were
between 2011–2017, while 48 (31.2%) were conducted between 2006–2010 and 41 (26.6%)
were conducted before 2006. Eighteen (69.2%) of the 26 outbreaks were reported after 2000.
Of the 180 studies which reported proportion of dengue cases, 74 studies (30%) provided
the details of laboratory confirmed cases by month with most (n = 60, 81%) reporting higher
dengue positivity between August and November months.
Age distribution of dengue cases: The age distribution of laboratory confirmed dengue
patients was available from 52 out of 180 studies. The pooled median age of laboratory con-
firmed dengue cases in these studies was 22 years (Fig 2). Fifteen (28.8%) studies reported the
median age of dengue cases below 15 years.
Estimates of prevalence (proportion): The overall estimate of the prevalence of laboratory
confirmed dengue infection in the random effects model based on testing of 213,285 clinically
suspected patients from 180 studies was 38.3% (95% CI: 34.8%–41.8%) (Fig 3). There was a
significant heterogeneity in the prevalence reported by the 180 studies (LRT p<0.001). The

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 Systematic review and meta-analysis of dengue fever in India

Fig 1. Flow diagram showing the article selection in the systematic review on dengue in India.
[Link]

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 Systematic review and meta-analysis of dengue fever in India

Fig 2. Distribution of median age of laboratory confirmed dengue cases by year of study, India.
[Link]

prevalence of laboratory confirmed dengue infection was higher in studies reporting outbreaks
or hospital-based surveillance studies during outbreaks (47.3%, 95% CI: 40.9–53.8) as com-
pared to hospital-based surveillance studies (33.6%, 95% CI: 29.9–37.5) (S1A and S1B Fig).
The attack rates of suspected dengue case patients were available in 8 out of the 26 outbreak
investigations reports. The attack rates ranged between 1.9% and 19.5%.
In the univariate mixed effect meta-regression model, odds of laboratory confirmation
were higher in case of outbreaks or hospital-based studies conducted during outbreaks
(OR = 1.8, 95% CI: 1.3–2.4). Studies which used WHO/ NVBDCP case definitions for enrol-
ment of patients also had higher odds of detecting laboratory confirmed dengue compared to
studies which used acute febrile illness/ clinically suspected dengue cases as case definitions.
Compared to studies conducted before 2006–10, studies conducted between 2011 and 2017
had higher odds of identifying laboratory confirmed patients (OR = 1.33, 95% CI: 0.93–1.9).
The odds of laboratory confirmation did not differ by region (Table 1). In the multivariate
meta-regression model constructed by including all covariates, case definition (WHO/
NVBDCP), type of study (hospital-based surveillance studies conducted during outbreaks or
outbreaks) and period of study (prior to 2005 and 2011–2017) were associated with higher
odds of dengue cases being laboratory confirmed.
Seroprevalence of dengue among healthy individuals. We included 7 studies reporting
seroprevalence of dengue based on detection of IgG (n = 5), neutralizing antibodies (n = 1) or
HI antibodies (n = 1) against dengue in the analysis [201–207]. These studies, conducted in 12
Indian states [Andaman and Nicobar islands (n = 1), Andhra Pradesh (n = 2), Tamil Nadu
(n = 3), Delhi (n = 4), West Bengal (n = 1), and Maharashtra (n = 1)], surveyed 6,551 individu-
als. The study population surveyed in these studies included healthy children (n = 2), general
population (n = 3), blood donors (n = 1) and neighbourhood contacts of dengue confirmed
cases (n = 1). The overall seroprevalence of dengue fever based on these studies was 56.9%
(95% CI: 37.5–74.4) (Fig 4). The age-specific prevalence of IgG antibodies was available in

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 Systematic review and meta-analysis of dengue fever in India

Fig 3. Prevalence (proportion) of laboratory confirmed dengue among clinically suspected patients in India. Error
bars indicate 95% confidence intervals. Diamonds show the pooled estimates with 95% confidence intervals based on
random effects (RE) model.
[Link]

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 Systematic review and meta-analysis of dengue fever in India

Table 1. Meta-regression of variables associated with the proportion of laboratory confirmed dengue infections, based on a univariate and multivariate model.
(n = 180).
Variable Univariate analysis Multivariate analysis

Odds Ratio (95% CI) P Odds Ratio (95% CI) P
Region
East Ref Ref
North 1.41 (0.93,2.15) 0.11 1.30 (0.89,1.98) 0.17
North-East 2.39 (0.97,5.88) 0.06 1.94 (0.81,4.65) 0.14
South 1.34 (0.85,2.11) 0.20 1.23 (0.79,1.90) 0.36
West 0.82 (0.36,1.88) 0.65 0.93 (0.42,2.06) 0.85
Study Type
Hospital based surveillance (HBS) Ref Ref
Outbreak/HBS during outbreak 1.78 (1.32,2.41) 0.00 1.65 (1.20,2.27) 0.00
Case Definition
AFI /Clinically suspected Ref Ref
WHO/NVBDCP 1.52 (1.09,2.12) 0.01 1.38 (1.01,1.91) 0.05
Year of study (midpoint) 0.97 (0.95,0.99)
Year of study (midpoint)
1982–2005 1.67 (1.14–2.47) 0.00 1.46 (1.01–2.14) 0.05
2006–2010 Ref Ref
2011–2017 1.33 (0.93–1.9) 0.12 1.45 (1.02–2.05) 0.04

Ref—Reference category; CI—Confidence interval; P –P value.

[Link]

three studies [201, 204, 206]. There was a significant heterogeneity in the seroprevalence
reported by the seven studies (LRT p<0.001). In the 3 studies which provided age specific sero-
prevalence, by the age of 9 years, 47.6% -73.4% children were reported to have developed IgG
or neutralizing antibodies against dengue (Table 2).
Case fatality ratios (CFR). Seventy-seven studies provided information about case fatality
ratios; most of them (n = 72, 93.5%) were conducted after 2000. The reported CFRs in these
studies ranged from 0% to 25%. There was a significant heterogeneity in the CFRs reported by
the 74 studies (LRT p<0.001). Twenty (25.9%) studies reported CFR of 2% or more. Three

Fig 4. Seroprevalence of dengue in India. Error bars indicate 95% confidence intervals. Diamonds show the pooled estimates with 95% confidence
intervals based on random effects (RE) model.
[Link]

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 Systematic review and meta-analysis of dengue fever in India

Table 2. Dengue seroprevalence by age, reported in 3 studies from India.

Garg et al (n = 2558) [201] Rodrı́guez-Barraquer et al (n = 800) [206] Padbidri et al (n = 717) [204]
Age (y) Seroprevalence (%) Age (y) Seroprevalence (%) Age (y) Sero-prevalence (%)
5 40.7% 5–9 77.1 0–9 47.6
6 50.9% 10–14 90.3 10–19 24.0
7 58.6% 15–19 91.7 20–29 26.8
8 67.4% 20–29 96.3 30–39 25.0
9 70.8% 30–40 98.8 > = 40 23.3
10 73.4%
Overall 59.6 (95% CI: 57
7–61
5) 93 (95% CI: 91.1–94.6) 25.4 (95%CI: 22.3–28.7)

Figure in square bracket indicate reference

[Link]

studies [30, 239, 195] which affected overall meta-estimates due to small denominator and
hence were excluded from analysis. The pooled estimate of CFR was 2.6% (95% CI: 2.0–3.4)
(Fig 5).

Secondary outcomes
Primary and secondary dengue infection. A total of 49 studies provided data which
enabled classification of laboratory confirmed dengue into primary and secondary dengue
infections. The number of patients with acute dengue infections in these studies ranged
between 13 and 1752. Only two studies estimated the proportion of secondary infection based
on IgG to IgM ratio [174, 237]. The prevalence of secondary dengue infection was <10% in
6 studies, 10–25% in 9 studies, 26–50% in 12 studies, 51–75% in 17 studies and >75% in 5
studies. The overall proportion of secondary dengue infection among laboratory confirmed
patients was 42.9% (95%CI: 33.7–52.6) (Fig 6).
Proportion of severe cases. Information about severity of dengue was available in 49
studies. Most studies (n = 46, 93.9%) used the WHO 1997 classification while 3 studies used
the WHO 2009 classification for dengue severity. The reported proportion of severe dengue
cases among laboratory confirmed patients ranged between 1.4% and 97.4%. The overall pro-
portion of severe dengue among laboratory confirmed studies in the random effects model
was 28.9% (95% CI: 22.2–36.6) (Fig 7).
Serotypes of dengue virus. Information about dengue serotypes was available in 51 stud-
ies. These studies were conducted in 19 Indian states; with a regional distribution of north
(n = 28), south (n = 13), east (n = 4), northeast (n = 4), and west (n = 2). Thirty-eight (75%) of
the 51 studies reported circulation of more than one serotype. The predominant serotypes
reported in these studies were DEN-2 and DEN-1 in the northern region, DEN-2 and DEN-3
in the southern region, and DEN-1 and DEN-2 in the eastern and the western regions. In the
four studies reported from the north-eastern region, the predominant serotypes was DEN-3
followed by DEN-1 and DEN-2 serotypes (Table 3).
Economic burden. Direct and Indirect cost analysis: An estimate of direct and indirect
costs was reported in three studies. The average direct cost per case of dengue ranged between
USD 23.5 and USD 161 and the indirect cost was around USD 25 whereas the average cost of
hospitalization ranged between USD 186 and USD 432.2 [range 249-252]. The cost of dengue
treatment in the private health sector was two to four times higher than that in the public sec-
tor hospitals [249, 253].
Economic impact of dengue on National Economy: Three macro-level studies addressed the
economic impact of dengue faced by India [250, 251, 253]. It was estimated that the average

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 Systematic review and meta-analysis of dengue fever in India

Fig 5. Studies reporting case fatality ratio among laboratory confirmed dengue cases in India. Error bars indicate 95% confidence intervals.
Diamonds show the pooled estimates with 95% confidence intervals based on random effects (RE) model.
[Link]

total economic burden due to dengue in India was USD 27.4 million [251]. Another study esti-
mated that the total direct medical cost of dengue in 2012 was USD 548 million [253]. The
overall economic burden of dengue would be even higher if the cost borne by individual
patients is combined with the society level cost of dengue prevention, vector control, disease
control and its management, dengue surveillance as well as the cost of research and develop-
ment [250, 251, 253].

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 Systematic review and meta-analysis of dengue fever in India

Fig 6. Proportion of secondary infection among laboratory confirmed dengue cases in India. Error bars indicate 95% confidence intervals.
Diamonds show the pooled estimates with 95% confidence intervals based on random effects (RE) model.
[Link]

Publication bias and sensitivity analysis

Funnel plots and Egger’s test revealed no publication bias in the estimates of dengue preva-
lence in hospital-based surveillance studies, hospital-based surveillance studies during out-
breaks and outbreak investigations. CFR estimates, however, showed a significant publication
bias, and studies with high prevalence were more likely to be published. In the sensitivity anal-
ysis, the estimated pooled proportions were found to be consistent for all study outcomes. (S3
Appendix)

Discussion
The present study has estimated the burden of dengue fever based on published literature
from India spanning over five decades. Most of the published literature included in the analy-
sis were hospital/ laboratory-based surveillance studies or reports of dengue outbreak investi-
gations. Additionally the published data from VRDL network has been included in the
analysis [65, 96]. The data from the other two nationally representative surveillance platforms
could not be used for the analysis because surveillance data from NVBDCP only reports the
number of laboratory confirmed dengue cases, while the IDSP data is not available in the pub-
lic domain.

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 Systematic review and meta-analysis of dengue fever in India

Fig 7. Proportion of severe dengue infections among laboratory confirmed dengue cases in India.
[Link]

There was no community-based epidemiological study reporting the incidence of dengue

fever. Our analysis revealed that among the clinically suspected dengue fever patients, the esti-
mated prevalence of laboratory-confirmed dengue infection was 38%. The burden of dengue
was also variable in studies conducted in different settings. Our findings indicated that most of
the laboratory confirmed dengue cases in India occurred in young adults. Dengue positivity
was higher between the months of August and November, corresponding to monsoon and
post-monsoon season in most states in India.
In the meta-regression, studies that had used WHO/NVBDCP case definitions and the hos-
pital based studies conducted during outbreaks or studies reporting outbreaks were more
likely to have laboratory confirmation of dengue. The odds of laboratory confirmation were
also higher among studies conducted during the period of 2011 to 2017, as compared to stud-
ies conducted prior to the year 2000.
Information about seroprevalence of dengue in the general population is a useful indicator
for measuring endemicity of dengue fever. The dengue vaccine (CYD-TDV) manufactured by
Sanofi Pasteur has been introduced in two sub-national programs in Philippines and Brazil
[254] and it has been suggested that vaccine acts by boosting the naturally acquired immunity
[255]. WHO SAGE conditionally recommends the use of this vaccine for areas in which
dengue is highly endemic as defined by seroprevalence in the population targeted for vaccina-
tion [12, 256]. The results of the two vaccine trials and mathematical modelling suggest that

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 Systematic review and meta-analysis of dengue fever in India

Table 3. Circulating dengue virus serotypes by state and region, India, 1982–2015.
2000 and earlier 2001 to 2005 2006 to 2010 2011 and above
State by region 1982 1988 1996 1997 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015
East
Odisha [149] 2,3
Odisha [90] 2,1
West Bengal [123] 1,2
West Bengal [67] 1,4,3,2
North
Chandigarh [193] 2
Delhi [167] 1,2
Delhi [147] 2,1
Delhi [127] 1
Delhi [148] 3,1,2,4
Delhi [107] 2,3
Delhi[143] 3,1,2,4
Delhi [36] 1,2,3
Delhi [172] 1
Delhi [42] 1,2,4
Delhi [64] 2,1,3,4
Delhi [217] 2,4
Delhi [22] 2,1,3 2,1,3
Delhi [76] 2,3,4,1
Delhi [38] 3,2,1,4
Delhi [56] 3,1,2,4
Delhi [39] 1,2,3,4
Delhi [242] 1,2,3,4
Delhi [137] 2,4
Delhi [58] 1
Madhya Pradesh [163] 2
Madhya Pradesh [29] 4
Madhya Pradesh [176] 2
Madhya Pradesh [30] 4,1
Uttar Pradesh [243] 2,3,1,4
Uttar Pradesh [93] 2,3,1
Uttar Pradesh [82] 2,3,1
Uttar Pradesh [96] 1,3,2
North-east
Arunachal Pradesh [157] 3,
1,2
Assam, Nagaland, 1,2,3,4
Meghalaya, Manipur [50]
Manipur [183] 3,1,2,4
Manipur [196] 2
South
Andaman & Nicobar 3
[181]
Andaman & Nicobar 1,2
[144]
Andhra Pradesh [150] 4, 3
(Continued)

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 Systematic review and meta-analysis of dengue fever in India

Table 3. (Continued)

2000 and earlier 2001 to 2005 2006 to 2010 2011 and above
State by region 1982 1988 1996 1997 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015
Karnataka [131] 2,3,4,1
Kerala [138] 2
Kerala [244] 1,3,2
Kerala [73] 2,3,1,4
Kerala [80] 1,3,2
Puducherry [27] 3
Puducherry [153] 3
Tamil Nadu [189] 3
Telangana [162] 4,3
Telangana [86] 2,3,4,1
West
Maharashtra [186] 2,1
Maharashtra [98] 1,2,3

Key for coloured cell: Blue—One circulating serotype, Yellow—two co-circulating serotypes, Green—three co- circulating serotypes, Orange—four co- circulating
serotypes. Numbers mentioned in the cell indicate predominant serotypes, in descending order.

[Link]

optimal benefits of vaccination if seroprevalence in the age group targeted for vaccination was
in the range of 70% [255, 256]. In 2018, WHO revised the recommendation from population
sero-prevalence criteria to pre-vaccination screening strategy [257]. The pooled estimate based
on the seven studies conducted in India indicated a dengue seroprevalence of 57%. However,
this estimated seroprevalence is not representative of the country, as these studies were con-
ducted only in 12 Indian states, and some had used a convenience sampling method [201].
The computed pooled estimate of case fatality due to dengue in India was 2.6% with a high
variability in the reported CFRs. The CFR estimated in our study was higher than the estimate
of 1.14% (95% CI: 0.82–1.58) reported in the meta-analysis of 77 studies conducted globally; in
the 69 studies which adopted WHO 1997 dengue case classification, the pooled CFR was 1.1%
(0.8–1.6) while the pooled CFR for 8 studies which used the WHO 2009 case definition, the
pooled CFR was 1.6% (95% CI: 0.64–4.0) [258]. Higher CFR observed in our analysis could be
due to smaller sample sizes as 14 of the 35 studies that reported CFR of 2.6 or higher had a
sample size of 100 or less, while in the remaining 21 studies the denominator ranging between
101 and 400. Also, we only considered laboratory confirmed dengue cases in the denominator
for the calculation of CFR. As per the NVBDCP surveillance data, a total of 683,545 dengue
cases and 2,576 deaths were reported in India during 2009–2017 giving a CFR of 0.38% [6].
The lower CFR estimates from NVBDCP data could probably be on account of under-report-
ing of deaths due to dengue, or inclusion of higher number of mild cases in the denominator
[259]. As per the NVBDCP surveillance data, an average of 28,227 dengue cases and 154 deaths
were reported annually during 2009–2012. The number of dengue cases reported increased
thereafter, with an average of 100,690 cases per year during 2013–2017. However, the reported
number of deaths did not increase proportionately. The information about severity of dengue
cases is not available from NVBDCP surveillance data.
The published studies from India indicated circulation of all the four-dengue serotypes,
with DEN-2 and DEN-3 being the more commonly reported serotypes. Two third of the stud-
ies reported circulation of more than one serotype. Co-circulation of multiple serotypes was
particularly evident from the published studies in Delhi. More than two third (16/19) studies

PLOS Neglected Tropical Diseases | [Link] July 16, 2018 15 / 29

 Systematic review and meta-analysis of dengue fever in India

from Delhi reported circulation of more than one serotype; and most of the studies conducted
in the last 10 years identified co-circulation of more than one serotype [Table 3]. Our review
also revealed that more than two-fifth of the laboratory confirmed infections were secondary
dengue infections and nearly one-fourth of the cases were severe in nature. Circulation of
numerous dengue serotypes is known to increase the probability of secondary infection, lead-
ing to a higher risk of severe dengue disease [260].
Our systematic review has certain limitations. First, our study included only peer-reviewed
literature from selected databases and we excluded grey literature which may have provided
additional data. Second, most of the studies on disease burden were hospital-based, with no
community-based studies estimating incidence. Hospital-based studies do not provide any
information about the community level transmission as hospitalization is a function of health-
seeking behaviour of the population. In absence of the information about health seeking
behaviour provided in these studies, we estimated the prevalence of dengue using number of
patients tested in the hospitals as the denominator. Third, the hospital-based studies used vary-
ing case definitions and laboratory tests to confirm dengue infection. Fourth, information
about the type of health facility (public or private), or residential status of patients (urban or
rural), and age was not uniformly reported and hence we did not estimate the dengue preva-
lence by these variables.
In conclusion, the findings of our systematic review indicate that dengue continues to be an
important public health problem in India, as evidenced by the high proportion of dengue posi-
tivity, severity and case fatality as well as co-circulation of multiple dengue virus serotypes.
Our review also identified certain research gaps in the understanding on dengue epidemiology
in the country. There is a need to initiate well planned community-based cohort studies repre-
senting different geographic regions of the country in order to generate reliable estimates of
age-specific incidence of dengue fever in India. As such studies are cost intensive, a national
level survey to estimate age-stratified dengue seroprevalence rates could be an alternative.
Such estimates could be used to derive the relative proportions of primary and secondary
infections using mathematical models [261]. Well planned studies in different geographic set-
tings are also needed to generate reliable data about economic burden from India. Although
the existing dengue surveillance platforms of NVBDCP, IDSP and VRDL are generating data
about dengue disease burden, these systems could be strengthened to also generate data about
dengue serotypes, severity, and primary and secondary infection from India.

Supporting information
S1 Appendix. Search criteria.
(PDF)
S2 Appendix. Critical appraisal checklist for quality assessment of studies.
(PDF)
S3 Appendix. Publication bias and sensitivity analysis.
(PDF)
S1 Dataset. Abstracted data of included studies.
(XLSX)
S1 Fig. Prevalence (proportion) of laboratory confirmed dengue among clinically sus-
pected patients by study type.
(PDF)

PLOS Neglected Tropical Diseases | [Link] July 16, 2018 16 / 29

 Systematic review and meta-analysis of dengue fever in India

S1 Checklist. PRISMA checklist.

(DOC)

Author Contributions
Conceptualization: Parasuraman Ganeshkumar, Manoj V. Murhekar, Sanjay M. Mehendale.
Data curation: Parasuraman Ganeshkumar, Manoj V. Murhekar, Veeraraghavadoss Poor-
nima, Krishnendu Sukumaran, Anandan Anandaselvasankar.
Formal analysis: Velusamy Saravanakumar.
Funding acquisition: Manoj V. Murhekar, Sanjay M. Mehendale.
Investigation: Parasuraman Ganeshkumar, Manoj V. Murhekar, Veeraraghavadoss Poor-
nima, Krishnendu Sukumaran.
Methodology: Parasuraman Ganeshkumar, Manoj V. Murhekar, Denny John, Sanjay M.
Mehendale.
Project administration: Parasuraman Ganeshkumar, Manoj V. Murhekar.
Software: Veeraraghavadoss Poornima, Velusamy Saravanakumar, Krishnendu Sukumaran,
Anandan Anandaselvasankar.
Supervision: Manoj V. Murhekar, Denny John.
Validation: Manoj V. Murhekar, Veeraraghavadoss Poornima, Krishnendu Sukumaran, Ana-
ndan Anandaselvasankar.
Visualization: Veeraraghavadoss Poornima, Krishnendu Sukumaran, Anandan
Anandaselvasankar.
Writing – original draft: Parasuraman Ganeshkumar, Manoj V. Murhekar.
Writing – review & editing: Manoj V. Murhekar, Denny John, Sanjay M. Mehendale.

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