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LIST OF TABLES
Table No. Particulars Page
Table 2.1
Epidemiological studies where dengue virus was
identified in India.
22
Table 2.2 Serum cytokine levels in the pathogenesis of dengue.
38
Table 2.3 WHO Newer Classification System of Disease Severity
(2009).
47
Table 2.4 Conditions that can mimic febrile phase of dengue
infection.
55
Table 2.5 Conditions that can mimic critical phase of dengue
infection.
56
Table 2.6
Advantages and limitations of different dengue diagnostic
tests.
60
Table 3.1 Details of NS1serotype specific RT-PCR assay primer
sets used for rapid detection and differentiation of dengue
virus serotypes 1, 2, 3 and 4 targeting NS1 region of the
viral genome.
106
Table 3.2 Protocol for CDC 1-4 real time RT-PCR assay reaction.
107
Table 3.3
Details of NS1 Serotype Specific RT-LAMP assay primer
sets used for rapid detection and differentiation of dengue
virus serotypes 1, 2, 3, and 4 targeting NS1 region of the
viral genome.
113
Table 4.1
Pilot study results of NS1 serotype specific RT-PCR,
CDC1-4 real time PCR and NS1 serotype specific RT-
LAMP assay for detection of DENV infection.
125
Table 4.2
Year wise distribution of suspected dengue cases
referred to Nizam’s Institute of Medical Sciences and Sir
Ronald Ross Institute of Tropical Medicine, Hyderabad,
for treatment from the regions in and around Hyderabad,
between July 2011 to December 2013.
128
Table 4.3
Year wise distribution of suspected dengue fever cases
and dengue fever positive cases referred to Nizam’s
Institute of Medical Sciences and Sir Ronald Ross
Institute of Tropical Medicine, Hyderabad, for treatment
from the regions in and around Hyderabad, between July
2011 to December 2013.
129
212
Table No. Particulars Page
Table 4.4
Year wise distribution of DENV seropositive cases
among in patients and out patients referred to Nizam’s
Institute of Medical Sciences and Sir Ronald Ross
Institute of Tropical Medicine, Hyderabad, for treatment
from the regions in and around Hyderabad, between July
2011 to December 2013.
130
Table 4.5
Serological test results by NS1 Ag, IgG and IgM
antibodies or combinations of antigen and antibodies in
the year 2011, 2012 and 2013.
131
Table 4.6
Comparative analysis of serological and molecular assays
for diagnosis of acute DENV infection.
135
Table 4.7
Inter run assay of in house developed NS1 serotype
specific RT-PCR assay for reproducibility by testing 5
samples by 2 investigators.
138
Table 4.8
Inter run assay of in house developed NS1 serotype
specific RT-PCR assay for reproducibility by testing 5
samples by 2 investigators.
144
Table 4.9
Inter run assay of NS1 RT-PCR for reproducibility by
testing 20 samples on 3 days.
145
Table 4.10
Intra run assay for repeatability from RNA of a DENV
positive patient for each serotype- 10 times, by the NS1
serotype specific RT-PCR assay, on the same day.
145
Table 4.11
Sensitivity of NS1serotype-specific dengue virus RT-
LAMP assay compared to NS1Ag, IgG + IgM antibody,
NS1 RT-PCR and CDC real time RT-PCR.
152
Table 4.12
Diagnostic performance of RT-LAMP assay against NS1
Ag and RT-PCR assay in dengue patients in tertiary care
hospital in Hyderabad.
152
Table 4.13
Sensitivity of the NS1 serotype specific RT-LAMP assay
related to number of days after onset of fever (N =148).
153
Table 4.14
Amplification time and annealing temperatures for 4
DENV-1, 4 DENV-2, 4 DENV-3 and 4 DENV-4 positive
samples in Genie II instrument.
156
Table 4.15
Reproducibility of DENV RT-LAMP assay by testing 1
sample of each serotype in 5 separate LAMP runs and
recording the time to positivity and Tm for each serotype.
162
213
Table No. Particulars Page
Table 4.16
Comparison of results obtained by the serological and
molecular assays among 175 hospitalized patients.
165
Table 4.17
Comparison of clinical findings in hospitalized patients
with Dengue fever (DF), Dengue hemorrhagic fever
(DHF), and Dengue shock syndrome (DSS).
166
Table 4.18
Comparison of unusual manifestations of dengue among
175 hospitalized patients.
168
Table 4.19
Comparison of unusual manifestations of dengue among
patients with DENV-2 and DENV-3 serotype.
169
Table 5.1
Standards followed in developing Dengue NS1 serotype
specific RT-LAMP assay.
178
214
LIST OF FIGURES
Figure No. Particulars Page
Figure 1.1
2009 WHO criteria for classification of dengue according to
levels of severity.
4
Figure 1.2 Diagnostic markers of dengue based on stage of illness. 6
Figure 2.1 Global distribution of dengue. 16
Figure 2.2 Dengue cases in India from 2007 to 2013. 23
Figure 2.3 States and their areas in India affected by dengue in the year
2013.
24
Figure 2.4 Distribution of number of dengue cases in states of India in 2013. 25
Figure 2.5 Case fatality rates of dengue among the states of India in 2012. 26
Figure 2.6 Dengue virus structure. 29
Figure 2.7 Dengue virus genome structure. 29
Figure 2.8 Dengue virus replication process. 35
Figure 2.9 The Aedes aegypti mosquito which transmits dengue infection. 39
Figure 2.10a Transmission cycle of dengue. 40
Figure 2.10b Transmission cycle of dengue. 41
Figure 2.11 Clinical course of dengue infection. 44
Figure 2.12
Clinical symptoms of dengue fever. 49
Figure 2.13 Direct and indirect laboratory diagnostic tests for dengue.
58
Figure 2.14 Major diagnostic markers for dengue infection.
59
Figure 2.15 Step I of LAMP Principle. 70
Figure 2.16 Step II of LAMP Principle. 70
Figure 2.17 Step III of LAMP Principle. 70
Figure 2.18 Step IV of LAMP Principle. 71
Figure 2.19 Step V of LAMP Principle. 71
Figure 2.20 Step VI of LAMP Principle. 71
Figure 2.21 Step VII of LAMP Principle.
72
Figure 2.22 Step VIII of LAMP Principle.
72
215
Figure No. Particulars Page Figure 2.23 Alternately inverted repeats of the target sequence on the same
strand formed after Lamp Cycling.
73
Figure 2.24
Amplified products using Loop Primers. 73
Figure 2.25 Configuration of primers for loop-mediated isothermal
amplification (LAMP).
76
Figure 2.26 Principle of a MAC-ELISA test. 84
Figure 2.27 Principle of Haemagglutination-inhibition assay. 88
Figure 3.1
Testing Algorithm for standardization of serological and
molecular assays in pilot Study.
93
Figure 3.2
Dengue Duo Rapid Test for detection of NS1 Ag and IgG and
IgM antibody.
95
Figure 3.3 Schematic presentation of RNA Isolation. 101
Figure 3.4 Selection of target for NS1 Serotype specific RT-PCR and RT-
LAMP assay.
104
Figure 3.5a
RT-LAMP primer details designed from Primer Explorer Version
4 from Eiken genome site.
110
Figure 3.5b
Loop Forward & Loop backward primers containing sequences
complementary to the single stranded loop region.
111
Figure 4.1
Agarose gel analysis of the DNA product from one step RT-PCR
after amplification with consensus primers Dl and D2. Lane 1 -
100 bp ladder, PC – Positive control, S2- DENV positive samples,
S3 & S4- DENV negative samples, NC- Negative control.
124
Figure 4.2
Amplification plots for real time LAMP of DENV serotypes
performed on the Genie II flourometer, which is monitored by
real-time measurement of fluorescence in the Y-axis versus
amplification time in X-axis. Shown from left to right are the
curves of positive control (PC), DENV-1, DENV-2, DENV-3 and
DENV-4.
126
Figure 4.3
Real time amplification of DENV-1,-2,-3 and 4 by CDC 1-4 real
time RT-PCR assay. Shown from left to right are the curves of,
DENV-1, DENV-2, DENV-3 and DENV-4. Rn in the Y-axis is
the specific normalized fluorescence of the reporter fluorophore,
which rises in each cycle (X-axis).
127
Figure 4.4
Year wise distribution of percentage of seropositive dengue cases
referred to Nizam’s Institute of Medical Sciences and Sir Ronald
129
216
Figure No. Particulars Page Ross Institute of Tropical Medicine, Hyderabad, for treatment
from the regions in and around Hyderabad, between July 2011 to
December 2013.
Figure 4.5
Year wise distribution of seropositive cases with primary and
secondary infection of dengue.
131
Figure 4. 6
Age wise distribution of positive dengue cases referred to
Nizam’s Institute of Medical Sciences and Sir Ronald Ross
Institute of Tropical Medicine, Hyderabad, for treatment from the
regions in and around Hyderabad, between July 2011 to
December 2013.
132
Figure 4.7
Monthly distribution of the positive dengue cases in 2011, 2012,
and 2013.
133
Figure 4.8
District wise distribution of dengue positive cases in states of
Andhra Pradesh & Telangana in 2011, 2012 and 2013.
134
Figure 4.9
Agarose gel analysis of the DNA product from one step RT-PCR
after amplification with consensus primers Dl and D2. Lane 1 -
100 bp ladder, PC – Positive control, S2- DENV positive samples,
S3 & S4-DENV negative samples, NC-Negative control (Main
study).
136
Figure 4.10
2 % Agarose gel electrophoresis demonstrating the correctly sized
amplicons generated by the four tube dengue NS1 serotype
specific RT-PCR. A: DENV1 (308 bp), B: DENV 2 (313 bp), C:
DENV 3 (270 bp), D: DENV4 (291 bp).
137
Figure 4.11
Sensitivity of NS1 serotype specific RT-PCR assay for the
detection of the DENV NS1 gene as observed by agarose gel
analysis with a detection limit of 1000 copy numbers for DENV
1(A) and DENV 2(B) and 100 copy number for DENV 3(C) and
DENV 4(D). Lane 1, 100-bp DNA ladder (Sigma); lanes 2 to 7,
different concentrations of virus ranging from 1 × 108 to 1 × 10
1
copy numbers in a serial 10-fold dilution pattern.
139
Figure 4.12
Sensitivities of the DENV NS1 serotype specific RT-PCR related
to number of days after onset of fever (Onset of fever is defined
as day 0 if blood samples were collected within the first 24 h
following the onset of fever).
140
Figure 4.13
Distribution of DENV serotypes among patients referred to
Nizam’s Institute of Medical Sciences and Sir Ronald Ross
Institute of Tropical Medicine, Hyderabad, for treatment from the
regions in and around Hyderabad in the year 2011, 2012 and
2013.
140
217
Figure No. Particulars Page
Figure 4.14
Phylogenetic tree of studied sequences with geographical strains
of DENV serotype 2 generated by neighbor-joining method. The
tree is based on NS1 regions (nt 86-398 bp) of the selected strains.
142
Figure 4.15
Phylogenetic tree of studied sequences with geographical strains
of DENV serotype 3 generated by neighbor-joining method. The
tree is based on NS1 regions (nt 128-397 bp) of the selected
strains. Each geographical strain is abbreviated by its accession
number followed by country and year of isolation.
143
Figure 4.16a
Sequence alignment among different genotypes of DENV-1
serotype.
147
Figure 4.16b
Sequence divergence among different genotypes of DENV-1
serotype.
147
Figure 4.16c
Sequence alignment among different genotypes of DENV-2
serotype.
148
Figure 4.16d
Sequence divergence among different genotypes of DENV-2
serotype.
148
Figure 4.16e
Sequence alignment among different genotypes of DENV-3
serotype.
149
Figure 4.16f
Sequence divergence among different genotypes of DENV-3
serotype.
149
Figure 4.16g
Sequence alignment among different genotypes of DENV-4
serotype.
150
Figure 4.16h
Sequence divergence among different genotypes of DENV-4
serotype.
150
Figure 4.17
Agarose gel electrophoresis of DENV serotype-specific RT-PCR
assay products on a 3% agarose gel employing F3 and B3 primers
of respective serotypes D1- DENV-1 RT-PCR assay product , 191
bp; D2- DENV-2 RT-PCR assay product,199bp; D3- DENV-3
RT-PCR assay product, 186bp; D4- DENV-4 RT-PCR assay
product185bp.
151
Figure 4.18a
Sensitivity of the RT-LAMP assay as monitored by real-time
measurement of fluorescence. Shown from left to right are the
curves of decreasing concentrations of virus from 1×105 to 1×10
1
copy numbers of the template in a serial 10-fold dilution. The
detection limit for the assay was 100 copy numbers for DENV-1
and DENV-2.
154
218
Figure No. Particulars Page
Figure 4.18b
Sensitivity of the RT-LAMP assay as monitored by real-time
measurement of fluorescence. Shown from left to right are the
curves of decreasing concentrations of virus from 1×105 to 1×10
1
copy numbers of the template in a serial 10-fold dilution. The
detection limit for the assay was 10 copy numbers for DENV-3
and DENV-4.
154
Figure 4.18c
Sensitivity of RT-PCR for the detection of the DENV NS1 gene
as observed by agarose gel analysis with a detection limit of 1000
copy numbers for DENV-1 and DENV-2.
155
Figure 4.18d
Sensitivity of RT-PCR for the detection of the DENV NS1 gene
as observed by agarose gel analysis with a detection limit of 100
copy numbers for DENV-3 and DENV-4.
155
Figure 4.19a
Amplification Curve for real time LAMP of DENV-2 and DENV-
3 performed in Genie® II flourometer.
157
Figure 4.19b
Amplification Curve for real time LAMP of DENV-1 and DENV-
4 performed in Genie® II flourometer.
157
Figure 4.19c
Anneal Curve of the finished amplified product of DENV-2 and
DENV-3 in Genie® II flourometer. Single peak from each Tm
value is unique to DENV-2 and DENV-3 sequence amplified,
thus confirming amplification of correct product.
158
Figure 4.19d
Anneal Curve of the finished amplified product of DENV-1 and
DENV-4 in Genie® II flourometer. Single peak from each Tm
value is unique to DENV-1 and DENV-4 sequence amplified,
thus confirming amplification of correct product.
158
Figure 4.20
Agarose gel electrophoresis of dengue virus serotype-specific RT-
LAMP assay products on a 3% agarose gel. Lane 1- 100-bp DNA
ladder (Sigma Genosys, Japan); lane 2, DENV-1 RT-LAMP assay
amplification; lane 3, DENV-2 RT-LAMP assay amplification;
lane 4, DENV-3 RT-LAMP assay amplification; lane 5, DENV-4
RT-LAMP assay product, lane 6, negative control without target
RNA.
159
Figure 4.21
Visual detection of amplified LAMP products using SYBR green
I. The color changes from orange (negative reaction) to green
(positive reaction). D1- DENV-1, D2- DENV-2, D3- DENV-3,
D4- DENV-4, NC-Negative control.
159
Figure 4.22a
Phylogenetic tree of studied sequences with geographical strains
of DENV serotype 2 generated by neighbor-joining method. The
tree is based on NS1 regions (nt 86-398 bp for DENV-2) of the
selected strains.
160
219
Figure No. Particulars Page
Figure 4.22b
Phylogenetic tree of studied sequences with geographical strains
of DENV serotype 3 generated by neighbor-joining method. The
tree is based on NS1 regions (nt 86-398 bp for DENV-2 and nt
128-397 bp for DENV-3) of the selected strains.
161
Figure 4.23a
Real-time amplification of dengue virus by NS1 serotype-specific
RT-LAMP assay for DENV-1 and DENV-4 depicting the kinetics
of each serotype with regard to time of positivity. O.D - optical
density in Loopamp turbidimeter.
163
Figure 4.23b
Real-time amplification of dengue virus by NS1 serotype-specific
RT-LAMP assay for DENV-2 and DENV-3 depicting the kinetics
of each serotype with regard to time of positivity. O.D - optical
density in Loopamp turbidimeter.
164
Figure 4.24
Different bleeding manifestations in hospitalized patients with
Dengue fever (DF), Dengue hemorrhagic fever (DHF), and
Dengue shock syndrome (DSS).
167
Figure 4.25a X-RAY showing pleural effusion due to dengue viral infection.
168
Figure 4.25b MRI of brain showing encephalitis due to dengue viral infection. 168
220
LIST OF PUBLICATIONS
1. M.Neeraja, V. Lakshmi, Vanjari Lavanya, E.N. Priyanka, M.M. Parida,
P.K. Dash,
Sashi Sharma, P.V.L. Rao, Gopal Reddy.
(2014). Rapid Detection and Differentiation
of Dengue virus Serotypes by NS1 specific Reverse Transcription Loop- Mediated
Isothermal Amplification (RT-LAMP) Assay in patients presenting to a tertiary care
hospital in Hyderabad. Journal of Virological Methods (Published online Nov 1st
2014, ahead of print Jan, 2015; 211, 22-31). DOI 10.1016/j.jviromet.2014.10.005.
2. M. Neeraja, Vemu Lakshmi, V.D Teja, V. Lavanya, E.N. Priyanka, K. Subhada,
M.M. Parida, P.K. Dash, Sashi Sharma, P.V.L. Rao, and Gopal Reddy (2014).
Unusual and rare manifestations of Dengue during Dengue outbreak in a tertiary care
hospital in South India. Archives of Virology 159: 1567–1573. DOI 10.1007/s00705-
014-2010-x.
3. Mamidi Neeraja, Vemu Lakshmi, V.D Teja, V. Lavanya, E.N. Priyanka, K.
Subhada, M.M. Parida, P.K. Dash, Sashi Sharma, P.V.L. Rao, and Gopal Reddy
(2013). Investigation of acute Dengue infection in Southern India employing Dengue
NS1 specific serological and molecular assays. International Journal of Recent
Scientific Research. 4(12): 2001-2008.
4. Mamidi Neeraja, Vemu Lakshmi, P.K. Dash, M.M. Parida, P.V.L. Rao.
(2013).
The Clinical, Serological and Molecular Diagnosis of Emerging Dengue Infection at a
Tertiary Care Institute in Southern, India. Journal of Clinical and Diagnostic
Research. 7(3): 457-461.
5. P. K. Dash, S. Sharma, A. Srivasatava, S.R. Santosh, M. M. Parida, M. Neeraja, M.
V. S. Subba laxmi, V. Lakshmi , P. V. L. Rao (2011). Emergence of dengue virus
type 4 (genotype I) in India. Epidemiology and Infection. 139(6): 857-61.
6. Paban Kumar Dash, Manmohan Parida, S.R. Santhosh, Parag Saxena, Ambuj
Srivastava, Mamidi Neeraja, V. Lakshmi, P.V. Lakshmana Rao (2008).
Development and evaluation of a 1-step duplex reverse transcription polymerase
chain reaction for differential diagnosis of chikungunya and dengue infection.
Diagnostic Microbiology and Infectious Disease. 62: 52–57.
7. Neeraja M, Lakshmi V, Teja VD, Umabala.P, Subbalakshmi MV. (2006).
Serodiagnosis of Dengue virus infection in patients presenting to a tertiary care
hospital. Indian Journal of Medical Microbiology. 24(4): 280-282.
221
PAPERS PRESENTED AT SYMPOSIA/CONFERENCE
1. Vemu Lakshmi, M. Neeraja, V. Lavanya, E.N. Priyanka, M.M.Parida,
P.K.Dash,
Sashi Sharma, P.V.L.Rao, Gopal Reddy. “ Rapid Detection and Serotyping of Dengue
by Reverse Transcription Loop-Mediated Isothermal Amplification Assay in patients
presenting to a tertiary care hospital” in ICAAC 2014, 54th
Interscience conference
on Antimicrobial Agents and Chemotherapy held from 5th
to 9th
September, 2014
at Walter E. Washington Convention Center, Washington D.C, U.S.A.
2. Sukanya Sudhaharan, Lavanya Vanjari, Mamidi Neeraja, Naga Priyanka Ede, Vemu
Lakshmi. “Evaluation of LAMP Assay for the detection of mecA and nuc genes in the
clinical isolates of Staphylococcus species. in XXXVIII National conference of
Indian association of Medical Microbiologists – MICROCON 2014, held at Birla
Auditorium, Jaipur, Rajasthan from 16th
to 19th, October, 2014.
3. M. Neeraja,
Vemu.Lakshmi, V.D.Teja,
V.Lavanya, E.N.Priyanka, K.Subhada,
M.M.Parida, P.K.Dash, Sashi Sharma, P.V.L.Rao ,
Gopal Reddy. “ Rapid Detection
and Serotyping of Dengue by Reverse Transcription Loop-Mediated Isothermal
Amplification Assay in patients presenting to a tertiary care hospital” in XVII Indian
Association Of Medical Microbiologists , Annual Conference (APCON) 2014 held
at KIMS Narketpally from 4th
& 5th
January, 2014.
4. M. Neeraja,
Vemu.Lakshmi, V.D.Teja,
V.Lavanya, E.N.Priyanka, K.Subhada,
M.M.Parida,
P.K.Dash, Sashi Sharma, P.V.L.Rao,
Gopal Reddy. “ Investigation of
acute Dengue infection in Southern India employing NS1 specific serological and
Molecular assays” in XXXVII National conference of Indian association of
Medical Microbiologists – MICROCON2013, held at HICC, Hyderabad from 21st
-
24th
November, 2013.
5. M. Neeraja,
Vemu.Lakshmi, V.D.Teja,
V.Lavanya, E.N.Priyanka, K.Subhada,
M.M.Parida,
P.K.Dash, Sashi Sharma, P.V.L.Rao,
Gopal Reddy. “ Evaluation of
Serotype specific Non-Structural-1 RT-PCR assay for rapid clinical diagnosis of
Dengue” in Brain Storming Conference on Dengue Scenario in India: Disease
burden, surveillance and control held at Centre for research in medical entomology
(Indian council of Medical research) Madurai from 25th
to 26th
July, 2013.
6. M. Neeraja,
Vemu.Lakshmi, V.D.Teja,
V.Lavanya, E.N.Priyanka, K.Subhada,
M.M.Parida, P.K.Dash, Sashi Sharma, P.V.L.Rao,
Gopal Reddy. “Changing trends in
serotypes and atypical manifestations of Dengue in a tertiary care hospital in
Hyderabad, A.P.” at XXXVI National conference of Indian association of Medical
222
Microbiologists – MICROCON2012, held at Lady Harding Medical College, New
Delhi from 22nd
to 25th
November, 2012.
WORKSHOPS ATTENDED
1. Attended workshop on “A Tour Of Molecular Techniques” in XXXVII National
conference of Indian association of Medical Microbiologists – MICROCON 2013,
held at HICC, Hyderabad from 21st
- 24th
November, 2013.
2. Attended workshop on “Molecular Techniques in Clinical Microbiology held at
Sanjay Gandhi Post Graduate Institute of Medical Sciences, Lucknow from 7-8th
March, 2009.
3. Attended workshop on “Use of Brit TB–PCR Kit ”, held at Department of
Microbiology, Nizam’s Institute of Medical Sciences, Hyderabad Conducted by
Board of Radiation and Isotope Technology at Centre for Cellular and Molecular
Biology, Hyderabad and Nizam’s Institute of Medical Sciences, On 13th
August,
2008.
4. Attended 5 Days training program on "Molecular Diagnosis of Arboviruses” with
special emphasis on Loop Mediated Isothermal Amplification and other PCR
technologies” in the Department of Virology, Defence Research & Development
Establishment, Ministry of Defence, Gwalior, from 02-05-2006 to 06-05-2006.
AWARDS
1. Won Dr. C.S. BHASKARAN, Junior Best paper Award for scientific paper on
“Molecular diagnosis of Chikungunya”, at X Indian Association of Medical
Microbiologists (AP) Chapter, held at Nizam’s Institute Of Medical Sciences,
Hyderabad, from 10th
to 11th
February, 2007.
2. Won 2nd Prize in BEST PAPER PRIZE FOR FREE PAPER SESSION for
scientific paper on “Rapid Detection and Serotyping of Dengue by Reverse
Transcription Loop-Mediated Isothermal Amplification Assay in patients
presenting to a tertiary care hospital” at XVII Indian Association of Medical
Microbiologists, Annual Conference (APCON) 2014, held at KIMS, Narketpally from
04-01-2014 to 05-01-2014.
223