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Abstract OBJECTIVES: Dengue/Dengue Hemorrhagic Fever (DHF) is the most rapidly spreading vector-borne infection all over
the world. Uttarakhand (India) is the prime destination for national and international tourists. Here we assessed the epidemiological
characteristics and entomological parameters of dengue/DHF in Uttarakhand (India) using in-depth statistical methods to measure
risk of dengue epidemics.
METHODS: we surveyed total 11 localities each in Nainital and Dehradun districts and calculated different entomological indices
and analyzed epidemiological characteristics of Dengue in these areas.
RESULTS: There was an epidemic of dengue during 2010 with total 4140 laboratory-confirmed dengue cases, about 5347% increase
of cases compared to preceding years. Out of six dengue-prone districts of Uttarakhand, Nainital and Dehradun were the worst
affected districts during this epidemic (Nainital = 862 and Dehradun = 2913; Total = 3775 cases), an incidence rate of 142.5 per
100000 population. The incidence rate in male (169.9 per 100000) is higher than in female (112.3 per 100000) and dengue cases were
predominant in the age group 21-30 years. Dehradun (77% of total cases) was more dengue prone area than Nainital. However, all
entomological indices are relatively higher in Nainital than Dehradun. Nevertheless, this difference in the indices is not significant
(p>0.05).
CONCLUSIONS: Therefore, we hypothesize that the epidemic intensity or severity of 2010-dengue outbreak in Nainital and
Dehradun are independent of entomological indices.
Keywords Dengue; Aedes; vector borne diseases; entomological index; India
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variation between countries and within each country. threshold of HI, BI & CI for forecast the outbreak
In 2010, World Health Organization (WHO) stratified etc.). The results of above study are presented in this
the current situation of Dengue/DHF in India under manuscript.
category A (earlier it was under category B up to
2009), which means a major public health problem, a
Methods
Study Area and its eco-environmental settings
leading cause of hospitalization and death among
Initially, the study was conducted in different parts of
children, shows cyclical epidemics in urban centers
Uttarakhand, however, finally, we focused our
spreading to rural areas with multiple virus serotypes
epidemiological and entomological surveillance in
circulating. In India, National Vector Borne Disease
Nainital and Dehradun, the two districts badly hit by
Control Program (NVBDCP) reported 28292
dengue epidemics in 2010. We analyzed the
laboratory-confirmed dengue cases in 2010 from 31
epidemiological history of dengue in the entire
out of 35 states in India (highest ever in a year). In
2011, 18,860 confirmed dengue cases were reported Uttarakhand state, and selected Nainital (exhibited a
and 169 deaths and in 2012, total 37,070 cases and low-middle epidemics in September 2009 with 51
227 deaths were attributable to dengue in India confirmed dengue cases) and Dehradun (exhibited an
(NVBDCP 2012). early signal of epidemics on August 2010 with 19
confirmed dengue cases) districts for investigations of
The northern states of India are badly affected by entomological measures of risk of dengue. The
dengue, although the intensity of transmission varies localities within these two districts for the
every 2-4 years. Uttarakhand is one of the dengue entomological survey were picked out based on
prone states in northern India, which has a history of dengue suspected cases reported during 2009-2010.
dengue epidemics since long with a heavy epidemic of Total 11 localities each in Nainital (viz. Forest
dengue/DHF in 2010. Moreover, Uttarakhand (India) compound, Kotdwar Rd., Khatyari, Gular Ghati,
is the prime destination of tourists from all over the Perumdara, 25 acres Colony, CCPM colony, Nageena
world. This also increases the travelers health risk. Colony, bungalow colony, Bindukhatta, Indiranagar)
Cultural tradition, socio-environmental conditions, and Dehradun (viz. Patel Nagar, Vikas Nagar,
and household circumstances often result in the Chandreshwar Nagar, Kailash gate, Shyampur,
absence or in the irregularity of water supply for a Aadarsh gram, Rani Pokhari, Reetha Mandi, Deep
significant part of the population in Uttarakhand, Nagar, Kedar Purum, Indra colony) districts were
causing the need to store water in reservoirs (Singh et chosen.
al. 2010). Moreover, due to a relatively dry climate in
summer seasons, people use water coolers (a cooling Topography: Uttarakhand lies within the Himalayan
device made up of metal/plastic having a water tank) region, with three distinct topographical belts - the
in their houses. These coolers are the potential place Shivaliks within the sub Himalayan tract [300-600 m
for Aedes mosquito breeding. Furthermore, because of Above Mean Sea Level, (AMSL)], the Himachal
irregular garbage collection in many areas, other ranges within the lower Himalayan region (1,500-2,700
breeding sites like plastic container, tin containers, m AMSL), and the Himadri ranges within the upper
bottles, water storage tanks, tire, and many unusual Himalayan region (4,800-6,000 m AMSL). The lower
breeding sites. hilly region, ranging between 600 m-1,800 m, and it is
within the region where the majority of the human
In this study, epidemiological characteristics of
populations live. Major parts of our study sites are
dengue/DHF and the entomological parameters were
located in this region.
assessed during the epidemic of dengue in 2010 to
determine the epidemic risk of dengue in Uttarakhand, General Climate: The climatic conditions change
India with the aim to establish better policies to with the increase of altitude, extending from sub-zero
control the dengue epidemics in these areas (e.g., temperatures at high altitudes in winter to moderate
improvement of water supply to minimize the temperatures in the lower tracts in summer. The
requirement of storage water, which are found to the territory has three distinct seasons - monsoon (June -
breeding place of Aedes aegypti; establish a local September), winter (October- February) and summer
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(March - May). Snowfall occurs between January and of dengue were based on the estimated mid-year total
March within the upper and lower Himalayan ranges. population and male/female population obtained from
the Office of Registrar General and Census Commissioner
Temperature and rainfall: Monthly maximum,
(Uttarakhand State), India.
minimum, and average temperatures and rainfall data
of Uttarakhand were collected from Indian Meteorological Entomological Surveillance
Department. In this article, we have included the We have chosen 11 localities each in Nainital and
temperature and rainfall data of Nainital and Dehradun Dehradun as mentioned above for entomological
districts only, as entomological surveys were carried survey. In these areas, we surveyed all potential
in these two districts only. Temperature and rainfall breeding sites in monsoon and post-monsoon months
data based on mean of the last 25 years (monthly from September to November 2010, immediately after
arithmetic averages) are presented graphically in the confirmations of an early outbreak of dengue in
result section. August 2010 with 19 confirmed dengue cases. All
non-hermetically closed containers containing any
Population: The Uttarakhand has a population of volume of water were considered as potential breeding
approximately 10,116,752 inhabitants. Nainital and sites. All water-holding containers were examined.
Dehradun are having an estimated population of Either the name/type of the containers (viz. Tire,
955,128 (494,115 males and 461,013 females) and cooler, fridge etc.) or construction materials (viz. Tin,
1,698,560 (893,222 males & 805,338 females) cement tank, clay pots, and plastic container)
inhabitants respectively (data source: Census India) classified the breeding sites. We recorded the number
(data source: Census of India 2011). of houses inspected, positive containers (with Aedes
pupae or larvae) and houses with 1 positive
Dengue fever and Epidemiological data container.
collection
We worked in collaboration with the Department of Statistical Analysis
Health, Govt. of Uttarakhand for this study. The dengue For all statistical analysis, we performed Kolmogorov-
case definition was adopted as per the recommendation of Smirnov (with Dallal- Wilkinson-Lilliefor P value),
World Health Organization Regional Office (Southeast D'Agostino & Pearson Omnibus and Shapiro-Wilk
Asia Regional Office 1999). Only the serologically normality test to see whether the data follow a
confirmed dengue cases, diagnosed using Rapid Gaussian distribution and implemented appropriate
Detection kit (NS1 Ag Ab Combo) and enzyme-linked statistical tests and calculated the corresponding P
immunosorbent assay in 2010 by different sentinel values. We calculated the total as well as sex wise
laboratories of the Department of Health, Govt. of incidence rates of reported indigenous cases of dengue
Uttarakhand were included in the analysis reported (combined of Nainital & Dehradun) based on the
here. All duplicate notifications were removed before estimated mid-year total population and male/female
analysis. We have also tried our level best to identify population respectively. We analyzed larval survey
cases with a history of travel within 10 preceding days data of different breeding sites based on the name/type
of the onset of illness to states where dengue also of the containers (viz. Tire, cooler, fridge, etc.);
occurred were classified as imported and were not construction materials (viz. Tin, cement tank, clay
included in the analysis. We have collected the pots, and plastic container) and three sigma limits
epidemiological report of dengue cases in Uttarakhand were applied to judge the significance of chance of
for the last five years (2006 to 2010) from the getting Aedes larvae. The three sigma limits were
Department of Health, Govt. of Uttarakhand. During applied to alert vector control operation process
epidemic in 2010, suspected cases were identified and regarding potential dangerous container for mosquito
a sero-epidemiologic survey was conducted in breeding following statistical quality measurement.
Nainital and Dehradun districts through state health For all areas, we calculated different entomological
services for laboratory-confirmation of suspected indices, viz. HI, CI, and BI and performed the
cases. The denominator for the calculation of total and Spearman rank correlation coefficient between the
sex wise incidence rates of reported indigenous cases different indices in all inspected areas. This statistical
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Results
The history of dengue epidemics in last five years
(2006 to 2010) in Uttarakhand is presented in Table 1
and Figure 1, which show an epidemic of dengue
during 2010 with total 4140 laboratory-confirmed
dengue cases, which means about 5347% increase of
dengue cases (Table 1). We observed that both numbers
of dengue cases and numbers of deaths due to dengue
are gradually increasing from 2006 to 2010. However,
percentage death rates due to dengue exhibit a
fluctuating trend (Table 1), although, Figure 1 shows
the direction towards the actual flow of dengue
epidemics in Uttarakhand during the past few years.
During the 2010 epidemic, our survey revealed that
Figure 1 Dengue cases and deaths in Uttarakhand (India)
out of six dengue prone districts of Uttarakhand state, during last five years. Both the number of cases and death has
Nainital (862 cases) and Dehradun (2913 cases) were been increased during last five years. However, the percentage
the worst dengue affected districts during the of deaths has decreased.
epidemics followed by Haridwar (257 cases), Pouri
Garwal (73 cases), Udham Singh Nagar (55 cases) and per 100000). Dengue cases are predominant in the age
Tehri Garwal (04 cases) (Figure 2). Total 3775 group 21-30 years (Table 2).
laboratory-confirmed dengue cases were registered
Monthly weather data in Nainital and Dehradun districts
from Nainital and Dehradun districts in 2010, an
(Figure 3) shows that temperature variation during the
incidence rate of 142.5 per 100000 populations (Table
year is moderate; Nainital has a relatively colder
2). It shows about 91.19% of total dengue cases in climate than Dehradun. However, rainfall variation
Uttarakhand were reported from these two districts. throughout the year is great. Although the rainy season
Table 2 summarizes the age and sex-specific distribution begins each year in late May or early June, most
of dengue cases in Nainital and Dehradun (combined) rainfall occurs in July and August and gradually
during 2010. The incidence rate in male (169.9 per decreases in September and October. February and
100000) is significantly higher than in female (112.3 NovemberJanuary was dry, with very little or no rain
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Table 1 Dengue cases and deaths in Uttarakhand in last five years (2006 to 2010)
Year Cases Death Death (%) Increase (+/-) Cases (%) Increase (+/-) Death (%)
2006 12 1 8.3% NA NA
2007 21 0 0.0% 75% -100%
2008 140 4 2.9% 567% 0%
2009 76 7 9.2% -46% 75%
2010 4140 8 0.2% 5347% 14%
NA, Not Applicable; Table shows the percentage of increase (+/-) of cases and deaths every year in respect to the preceding year.
Table 2 Age and sex specific distribution of dengue cases in Nainital and Dehradun (combined) in 2010
Sex No. of cases in different age groups (years) Total Incidence Rate
0-10 yrs. 11-20 yrs. 21-30 yrs. 31-40 yrs. 41-50 yrs. 51-60 yrs. 61-70 yrs. cases (per 100000)
Male 108 395 695 489 315 242 110 2354 169.9
Female 100 197 345 275 227 195 82 1421 112.3
Total 208 592 1040 764 542 437 192 3775 142.5
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Table 3 Summary of distribution of observed breeding sites for Aedes larvae and dengue cases in Nainital and Dehradun
Type of Container Nainital Dehradun Total
Tires 95% 20% 54%
Coolers 18% 27% 21%
Tin containers 51% 0% 51%
Cement tanks 44% 23% 31%
Clay pots 30% 19% 23%
Plastic containers 41% 25% 31%
Fridge vessels 0% 43% 43%
Total 41% 23% 30%
No of Dengue Cases 862 2913 3775
% cases 23% 77% 100%
Collection of all the data points (breeding sites) are independent in nature and do not feature the dependency over dengue cases or
deaths in the study area.
Table 4 Percentage distribution of positive container and influence of types of containers for breeding of Aedes mosquitoes at
different localities surveyed in Nainital
Areas/ Localities Chances to be getting Aedes Larvae/pupae in different types of containers
Case (%)=23% Tires Coolers Tin containers Cement tanks Clay pots Plastic containers Fridge Total
Forest compound 0% 18% 0% 0% 100% 25% 0% 60%
Kotdwar Rd. 50% 33% 40% 33% 13% 0% 0% 24%
Khatyari 80% 30% 100% 91% 86% 90% 0% 87%
Gular Ghati 100% 0% 100% 0% 100% 100% 0% 100%
Perumdara 0% 20% 17% 0% 20% 0% 0% 12%
25 acers Colony 0% 20% 0% 38% 11% 11% 0% 14%
CCPM colony 0% 14% 11% 0% 24% 37% 0% 24%
Nageena Colony 0% 8% 10% 0% 8% 0% 0% 8%
bangali colony 0% 0% 33% 13% 3% 7% 0% 9%
Bindukhatta 0% 0% 0% 0% 14% 7% 0% 10%
Indiranagar 0% 0% 0% 8% 9% 7% 0% 8%
Nainital Total 95% 18% 51% 44% 30% 41% 0% 41%
Variance = 10% , 3 Sigma limit = 70%
Table indicates high-risk containers in terms of Aedes breeding; Digits in bold font highlight the highest percentage of containers
found positive for Aedes breeding in a given localities.
We observed a very high correlation between overall dynamics in Uttarakhand in the last few years,
HI and BI values (r 0.92, p<0.01). In most positive investigating the dengue/DHF epidemic in 2010 and
houses, more than one container with Aedes exploring how different types of containers act on the
larvae/pupae was found.
mosquito proliferation and how all this knowledge
Discussion may help in establishing better policies to control the
Dengue has been on the rise since the year 2010 with dengue epidemics. Apparently, the effective vector
epidemics reported in as many as 50 countries in 2010 control may be possible but not easy. In many
(WHO-South East Asian Regional Office 2010). In developing countries limited infrastructural facilities
this article, we analyzed the dengue transmission in programs to control the Aedes mosquitoes has
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Table 5 Percentage distribution of positive container and influence of types of containers for breeding of Aedes mosquitoes at
different localities surveyed in Dehradun
Areas/Localities Chances to be getting Aedes Larvae/pupae in different types of containers
Case (%) = 77% Tires Coolers Tin containers Cement tanks Clay pots Plastic Fridge Total
containers
Patel nagar 46% 0% 0% 41% 25% 12% 40% 26%
Vikas Nagar 0% 0% 0% 4% 3% 2% 0% 3%
Chandreshwar Nagar 25% 0% 0% 0% 17% 7% 14% 12%
Kailash gate 0% 0% 0% 0% 0% 0% 0% 0%
Shyampur 0% 0% 0% 0% 16% 14% 0% 14%
Aadarsh gram 0% 0% 0% 0% 26% 20% 0% 23%
Rani Pokhari 0% 0% 0% 0% 16% 10% 0% 14%
Reetha Mandi 0% 50% 0% 0% 52% 0% 74% 61%
Deep Nagar 0% 8% 0% 25% 7% 70% 29% 44%
Kedar Purum 10% 0% 0% 0% 13% 0% 37% 17%
Indra colony 0% 0% 0% 0% 0% 3% 0% 2%
Dehradun Total 20% 27% 0% 23% 19% 25% 43% 23%
Variance = 3%, 3 Sigma limit = 32%
Table indicates high-risk containers in terms of Aedes breeding; Digits in bold font highlight the highest percentage of containers
found positive for Aedes breeding in a given localities.
Figure 3 Summary of weather data from Nainital and Dehradun districts of Uttarakhand. Temperature (C) and rainfall (mm) data
based on mean of the last 25 years (monthly arithmetic averages).
resulted in a huge expansion of dengue vectors in The existence of detailed entomological surveillance
urban as well as rural habitats (Tauil 2002; Barcellos data before, during, and after the dengue epidemic in
et al. 2005; Medronho et al. 2009).
study sites may offer a unique opportunity to analyze
Here, we should acknowledge that technically the present cause and effect relationship. The entomological
study might have few missing values and limitations. data collection has been limited to
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Figure 4 Comparisons of entomological indices (HI, CI, and BI) in different localities in Nainital and Dehradun
water collections in artificial containers, which may reflecting the cultural habit of collecting rainwater,
ignore the natural breeding sites of Ae. albopictus. and the abundance of unmanaged water sources.
Moreover, we may not able to identify all imported These findings are consistent with those of Strickman
dengue cases, or detect asymptomatic dengue cases. and Kittayapong (2002).
However, our study successfully describes the dengue
We studied the prevalence of Aedes larvae in context
endemicity in Uttarakhand, characterizes the dengue
to dengue epidemics in Uttarakhand. During our
epidemics in 2010, and investigates the entomological
survey, all non-hermetically closed containers containing
measures of risk of dengue.
any volume of water were considered potential for
We observed that both numbers of dengue cases and mosquito breeding; the highest percentage of positive
numbers of deaths due to dengue are gradually containers for larvae/pupae has shown up in tires, tin
increasing from 2006 to 2010. This increase may be containers, Fridge vessels, Cement tanks and Plastic
associated with several reasons like increasing population, containers. Interestingly, the majority of these positive
unhygienic living, climate change, developed disease containers is related to water supply and garbage
reporting systems, better diagnostic facilities etc. collections. These findings are in line with those
Interestingly, it is evident from the month wise reported by Focks & Chadee (1997) and Medronho et
distribution of dengue cases (Figure 2) that a dengue al. (2009). It is worth noting that in some areas we
epidemic was more severe from September to found 100% of surveyed containers are positive for
November, just after the highest rainfall, probably mosquito breeding (Table 4).
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Table 6 Mean House Index (HI), Container Index (CI) and Breteau Index (BI) in Nainital and Dehradun during 2010 dengue epidemics
Statistics House Index (HI) Container Index (CI) Breteau Index (BI)
Nainital Dehradun Nainital Dehradun Nainital Dehradun
Mean 32.33 28.61 25.91 17.93 124.99 77.33
Std. Deviation 6.21 7.312 7.17 3.51 74.63 11.49
Std. Error 0.56 0.6649 0.65 0.32 6.79 1.045
Lower 95% CI 16.11 12.48 10.84 8.86 28.92 42.47
Upper 95% CI 54.15 51.35 47.44 30.16 288.66 122.54
Table also shows Standard Deviation, Standard Error of Mean and 95% Confidence Interval limits for the entomological indices
We found very high entomological indices (HI, CI, level or even country level, the threshold level of
and BI) for all areas. However, it is difficult to give a entomological indices for an outbreak of dengue
precise threshold level of entomological indices in should be set up locally at district or even city level
epidemiological context. Dengue outbreak had previously since all vector borne diseases are focal and local in
been recorded even in very low entomological indices nature. However, entomological indices are very
in Cuba (Pelaez et al. 2004), and Singapore (cf useful to understand the actual man-mosquito contact,
Sanchez et al. 2006). In this present study, we found abundance of adult mosquitoes, monitoring vector
that Dehradun (77% of cases) is more dengue prone control programs and use as a tool for forecasting
area than Nainital (23% cases) (Table 3). However, all outbreak, pinpointing and mapping high-risk areas.
entomological indices are relatively higher in Nainital
We observed a very high correlation between overall
than Dehradun (Table 6, and Figure 4). Moreover,
HI and BI values. A high correlation and divergence of
Mann-Whitney U nonparametric test revealed that the
HI and BI were also observed in West Indies
observed differences of these indices (HI, CI, and BI)
(Thongcharoen 1993), where it was also noticed that
between Nainital and Dehradun is not statistically
at low rate of Aedes infestation, the HI and BI were
significant (p>0.05). Therefore, we hypothesize that
nearly the same, whereas at higher infestation rate, a
the epidemic intensity or severity of 2010-dengue
divergence between the indices was observed. Therefore,
epidemic in Nainital and Dehradun are independent of
the high correlation and divergence between HI and
the rate of entomological indices. However, the layout
BI in the present study indicated high rates of Aedes
of housing structures differs between these two
infestation, which may ultimately responsible for the
districts; population density is higher or more
dengue epidemics in these areas.
clustered in Dehradun than the Nainital, which could
also make Dehradun more dengue prone than Nainital. Finally, Dengue/DHF is a burning health problem
There is always the possibility that other factors may throughout India, and cases and deaths were reported
influence the relationship between entomological from 31 states out of 35 during 2010. The results of
indices and intensity of dengue epidemics. These this study reinforce the practical importance of
factors may be vector competence, vector bionomics entomological surveillance in measuring the risk of
and composition, virulence of the virus, immunity dengue epidemics. Moreover, we have successfully
status of the population as whole or local health analyzed the epidemic characteristics of dengue/DHF,
authorities in reporting correct epidemic status. Some which indicates the association of dengue with the
studies have shown that entomological indices do cultural habit of collecting rainwater due to irregular
not seem to reliably assess dengue transmission risks water supply and the abundance of unmanaged water
(Bang & Pant 1972; Kay et al. 1987; Reiter & Gubler sources due to the irregular garbage collection. Therefore,
1997; Focks et al. 2000), other programs have used improving these public services can improve the
them successfully (Pontes et al. 2000) or continue to dengue situation.
recommend their use (WHO 1999).
Acknowledgment
We believe that where it is difficult to generalize the We are thankful to LS Chauhan, Director NCDC for
interpretation of the threshold indices at the global giving us the opportunity to carry out the study. We
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