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EClinicalMedicine 32 (2021) 100717

Contents lists available at ScienceDirect

EClinicalMedicine
journal homepage: https://www.journals.elsevier.com/eclinicalmedicine

Research Paper

Descriptive epidemiology of SARS-CoV-2 infection in Karnataka state,


South India: Transmission dynamics of symptomatic vs. asymptomatic
infections
Narendra Kumara,1, Shafeeq K. Shahul Hameeda,1, Giridhara R. Babub,
Manjunatha M. Venkataswamya, Prameela Dineshc, Prakash Kumar B.G.c, Daisy A. Johnb,
Anita Desaia, Vasanthapuram Ravia,*
a
Department of Neurovirology, National Institute of Mental Health And Neuro Sciences (NIMHANS), Hosur Road, Bengaluru 560029, India
b
Indian Institute of Public Health, Public Health Foundation of India, Bengaluru, India
c
State Surveillance Unit, Directorate of Health and Family Welfare, Government of Karnataka, India

A R T I C L E I N F O A B S T R A C T

Article History: Background: The huge surge in COVID-19 cases in Karnataka state, India, during early phase of the pandemic
Received 30 September 2020 especially following return of residents from other states and countries required investigation with respect
Revised 23 December 2020 to transmission dynamics, clinical status, demographics, comorbidities and mortality. Knowledge on the role
Accepted 23 December 2020
of symptomatic and asymptomatic cases in transmission of SARS-CoV-2 was not available.
Available online 6 January 2021
Methods: The study included all the cases reported from March 8 - May 31, 2020. Individuals with a history of
international or domestic travel from high burden states, Influenza-like Illness or Severe Acute Respiratory
Keywords:
Illness and high-risk contacts of COVID-19 cases were included. Detailed analysis based on contact tracing
SARS-CoV-2 virus
COVID-19
data available from the line-list of state surveillance unit was performed using cluster network analysis
Epidemiology software.
Karnataka Findings: Amongst the 3404 COVID-19 positive cases, 3096 (91%) were asymptomatic while 308 (9%) were
Symptomatic vs asymptomatic symptomatic. Majority of asymptomatic cases were in the age range of 16 and 45 years while symptomatic
cases were between 31 and 65 years. Mortality rate was especially higher among middle-aged and elderly
cases with co-morbidities, 34/38 (89¢4%). Cluster network analysis of 822 cases indicated that the secondary
attack rate, size of the cluster and superspreading events were higher when the source case was symptomatic
as compared to an asymptomatic.
Interpretation: Our findings indicate that both asymptomatic and symptomatic SARS-CoV-2 cases transmit
the infection, although symptomatic cases were the main driving force within the state during the beginning
of the pandemic. Considering the large proportion of asymptomatic cases, their ability to spread infection
cannot be overlooked. Notwithstanding the limitations and bias in identifying asymptomatic cases, the find-
ings have major implications for testing policies. Active search, early testing and treatment of symptomatic
elderly patients with comorbidities should be prioritized for containing the spread of COVID-19 and reducing
mortality.
Funding: Intermediate Fellowship, Wellcome Trust-DBT India Alliance to Giridhara R Babu, Grant number: IA/
CPHI/14/1/501499.
© 2020 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/)

1. Introduction associated with international travel among returnees from COVID-19


affected countries. Since then, Severe Acute Respiratory Syndrome
India reported the first case of coronavirus disease 2019 (COVID- Coronavirus 2 (SARS-CoV-2) infection has spread across all states. As
19) on January 30, 2020, in a medical student who travelled from of September 16, 2020, a total of 5020,359 SARS-CoV-2 infections
Wuhan, China [1]. In the beginning, COVID-19 cases in India were have been reported from India [2]. Karnataka, a state in the southern
part of India, has a population of 64¢41 million spread across 30
administrative units called districts. Karnataka state reported the first
* Corresponding author.
E-mail address: virusravi@gmail.com (V. Ravi). case of COVID-19 in an international traveler on March 8, 2020 [3]. In
1
Both these authors contributed equally to the manuscript. the subsequent three months (March 8 to May 31, 2020) the number

https://doi.org/10.1016/j.eclinm.2020.100717
2589-5370/© 2020 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
2 N. Kumar et al. / EClinicalMedicine 32 (2021) 100717

From the beginning of the pandemic, there has been considerable


Research in context
debate on the role of asymptomatic and symptomatic persons in
spreading the SARS-CoV-2 infection. Initially, the World Health Orga-
Evidence before this study
nization (WHO) inferred that the role of asymptomatic persons in
Understanding transmission dynamics in the spread of SARS- transmission was minimal [11,12]. However, the WHO acknowledged
CoV-2 is important for controlling the COVID-19 pandemic. We later that there is a growing body of evidence that even asymptom-
retrieved all English-language articles reporting the transmis- atic persons can spread the disease [13]. Previous reports suggest
sion dynamics of SARS-CoV-2 from symptomatic and asymp- that nearly 432% of the infections are spread through asymptomatic
tomatic cases through systematic searches of major databases persons [14,15]. Determining the role of asymptomatic persons in
that included PubMed, medRxiv, bioRxiv, arXiv, SSRN, Research viral transmission in low and middle-income countries (LMICs) is
Square and Wellcome Open Research for peer reviewed articles, very important. The urban areas in these countries have high popula-
preprints and research reports. Our search identified publica- tion density, poor personal hygiene, with ubiquitous crowding. In
tions that included terms related to ‘symptomatic’, ‘asymptom- this report, we describe the epidemiology of SARS-CoV-2 infection in
atic’, ‘transmission dynamics’, ‘covid-190 and ‘SARS-CoV-20 the southern state of Karnataka, India, during the lockdown phase
between January 1 - June 1, 2020. Data pertaining to the role of with special emphasis on transmission dynamics of symptomatic and
symptomatic and asymptomatic cases in transmission of SARS- asymptomatic cases.
CoV-2 during early phase of the pandemic was not available
from India or any LMIC with a similar setting. 2. Materials and methods

Added value of this study 2.1. Study population

The study provides evidence that: (i) Transmission of SARS-


The study included all cases diagnosed with COVID-19 in the Kar-
CoV-2 occurs both from asymptomatic and symptomatic cases.
nataka state, reported from March 8 - May 31, 2020. Case identifica-
(ii) Symptomatic index case results in higher secondary attack
tion was carried out by the staff of each district, which included the
rate, bigger size of the cluster and higher occurrence of overt
district surveillance officer and their teams, the Integrated Disease
clinical illness. (iii) SSE’s are more commonly associated with
Surveillance Programme (IDSP) team, and the urban health authori-
symptomatic index cases. (iv) COVID-19 mortality is higher in
ties of the major cities. Reporting of Influenza-Like Illness (ILI) and
elderly with comorbidities.
Severe Acute Respiratory Illness (SARI) cases was mandatory for even
private health care providers. The contacts of COVID-19 positive peo-
Implications of all the available evidence
ple who were in quarantine were monitored. With respect to domes-
The findings of this study have major implications for policies tic and international travellers, the state had a policy of quarantining
related to surveillance and testing. Active search and early and subsequent testing of all passengers exposed to a COVID-19 posi-
detection of symptomatic elderly patients with comorbidities tive case. Most of the travellers were from COVID-19 affected coun-
should be prioritized to reduce mortality. Further, testing of all tries or states within India. Upon arrival in to the state, they were
individuals in high risk settings to capture silent transmission immediately subjected to testing. If tested positive they were hospi-
by asymptomatic individuals should be an integral component talized and if negative, were quarantined for 14 days with a repeat
of the policy to prevent spread of SARS-CoV-2. test being carried out between 7th and 10th day of quarantine [16].

2.2. Case definitions


of COVID-19 cases steadily increased to 3404 in the state. The health
authorities of the state initiated laboratory-based surveillance, tradi- A suspect case of COVID-19 was essentially based on the crite-
tional infection control and public health strategies to contain the ria defined by the Ministry of Health and Family Welfare, Govern-
spread [4,5]. These included tracing, testing and tracking of contacts ment of India described elsewhere [17]. Briefly, any person with a
and isolating COVID-19 positive subjects [6]. The state implemented recent history of international travel (14 days), domestic travel
several public health measures, including retrospective contact trac- from high burden states of Maharashtra, Gujarat, Delhi, and Tamil
ing, survey for influenza-like illness and strengthening the laboratory Nadu and anyone within the state with symptoms of ILI and SARI
network under the Integrated Disease Surveillance Programme as well as known high-risk contacts of a confirmed COVID-19
(IDSP). Also, the state had more than 17 task forces set up under the patients were also included. Asymptomatic SARSCoV2 cases
Karnataka State Disaster Management [7]. Several innovative meas- were defined as those with positive SARSCoV2 RT-PCR in the
ures were taken to tackle COVID-19 in the initial months. For exam- absence of symptoms [18].
ple, invoking powers under Epidemic Diseases Control Act, the state
started using information from available apps to notify people about 2.3. Laboratory testing
their possible interaction with a COVID-19 positive person.
From March 25, 2020, the country was under complete lockdown Testing for SARS-CoV-2 was done initially at five laboratories
until May 31, 2020, in four phases [8]. The first phase of the lockdown in the state. This was quickly ramped up to 63 laboratories across
was from March 25, 2020, to April 14, 2020. The second phase of the state by May 31, 2020, resulting in an enhanced capacity for
lockdown was from April 15, 2020, to May 03, 2020, the third phase testing and identification of COVID-19 cases across Karnataka.
of lockdown from May 0417, and the fourth phase from May Nasopharyngeal and oropharyngeal swabs collected into virus
1831, 2020. From the beginning of the third phase, the Government transport medium from suspected cases were subjected to an RT-
of India issued guidelines permitting inter-district and inter-state PCR for detection of SARS-CoV-2 RNA using the Indian Council of
travel for stranded persons. Consequently, there was a huge surge of Medical Research (ICMR) guidelines for testing [19]. Three RT-PCR
COVID-19 positive cases from May 431, by which time most of the kits approved by ICMR were used in the study and the details are
residents of Karnataka (n = 93,073) from other states, especially from provided in Table S1. All positive and negative results were
those with a high burden of COVID-19 cases, returned home [9]. As of entered immediately upon their availability into the ICMR portal
September 16, 2020, a total of 8,932,699 samples have been tested in and shared with the district/state surveillance teams to facilitate
the state, of which 851,212 tested positive (9¢5%) [10]. immediate tracing of contacts.
N. Kumar et al. / EClinicalMedicine 32 (2021) 100717 3

Fig. 1. Distribution of case categories, number of cases and interventions undertaken. X axis depicts the timeline while Y axis depicts the number of COVID-19 positive cases. The
date wise interventions undertaken by the state of Karnataka is described. The category of patients and the progression in numbers is depicted in various colors in a wave pattern.

2.4. Data collection parameter was calculated for asymptomatic and symptomatic
subjects and expressed as the k value [22,23]. As suggested
All the sociodemographic, clinical, and risk factor details recently [24] smaller values of k indicate greater heterogeneity,
(travel history, symptoms, comorbidities, etc.) of patients for and in general, k value<1 is associated with a high number of
every suspected case was collected on the day of sampling and ‘superspreaders’.
entered into a standardized line list by the surveillance teams in
the respective districts/cities. The line list also included informa- 2.6. Descriptive epidemiology of cases by time, place and person
tion about the type of sample, date of sample collection, date of
testing, type of RT PCR kit used, and the test results, as well as The frequencies of characteristics of cases were described by age,
the details of contacts. All contacts were traced based on the gender, residence, type of exposure (contact or travel), and symp-
information provided by the individual and subjected to testing toms. The presence of any symptoms at the time of specimen collec-
as per the national guidelines [20]. All the data was maintained tion was also recorded. The date of specimen collection was used to
in a centralized database by the State Surveillance Officer. Every draw the epidemic curve. The time trends were annotated with that
effort was made to ensure that missing data, if any, was collected of the implementation of various public health measures or key
from the subjects by the surveillance team. All the data were de- events related to the epidemic (Fig. 1).
identified before extraction and analysis. A subject who was
detected SARS-CoV-2 positive was given a P number. The lesser 2.7. Statistical analysis
the P number, the earlier the patient was detected either as a
source or as a contact of a known source. The study has been All the data were entered into the excel sheet and analyzed using
reported in accordance with the RECORD guidelines. the Statistical Package for Social Sciences (SPSS, version 26) to deter-
mine the significance of various parameters. The cluster network
2.5. Data analysis analysis was performed using Gephi (version 0¢9¢2) for analyzing the
transmission dynamics. Statistical significance was expressed as a p-
The data analysis from the line list was based on the date of value, calculated using the chi-square test, t-test for 95% confidence
collection of a sample from March 8 to May 31, 2020. The trends interval (CI).
in the positivity rate over time were described by calculating the
seven-day moving average. The number tested per million was 2.8. Funding
computed by using a State-specific population denominator. The
number of individual tests and contacts tested per confirmed case Giridhara R Babu is funded by an Intermediate Fellowship by the
was calculated. Laboratory accessibility was examined by sub- Wellcome Trust DBT India Alliance (Clinical and Public Health
tracting the date of specimen collection from the specimen research fellowship); grant number: IA/CPHI/14/1/501499.
receipt date. An indicator for contacts tested per case was esti-
mated by dividing the number of tests among contacts of cases 2.9. Role of the funding agency
with the number of positive cases. Contact tracing information
available in the line list was analyzed to determine the source of The funding agency of the study had no role in study design, data
infection. Based on the contact tracing information, cluster net- collection, data analysis, data interpretation, or writing of the article.
work analysis was performed and presented using Microsoft Excel All the authors had full access to all the data in the study and corre-
and Gephi network analysis software [21]. Secondary attack rates sponding author had final responsibility for submitting for publica-
were calculated using standard methods, and the dispersion tion.
4 N. Kumar et al. / EClinicalMedicine 32 (2021) 100717

Table 1 symptomatic cases, while 13% (7/54, 95% CI; 422) were asymptom-
Age group and gender of COVID-19 cases (Mean age 31¢26) (n = 3404). atic cases. Among the 38 symptomatic cases with comorbidities who
Age group Asymptomatic (%; 95% CI) Symptomatica (%; 95% CI) died, 89¢4% (34/38, 95% CI; 79¢699¢2) were among the middle-aged
and elderly. The cause of death among the seven asymptomatic cases
<15 542 (17¢5; 16¢2 - 18¢8) 17 (5¢5; 3¢0 - 8¢0)
is presented in Table S4. Overall, 39% (1340/3404) of cases recovered
1630 1149 (37¢1; 35¢4 - 38¢8) 61 (19¢8; 15¢3 - 24¢3)
3145 916 (29¢6; 28¢0 - 31¢2) 96 (31¢2; 26¢0 - 36¢4) and were discharged from the hospital, while 59% (2010/3404) were
4660 374 (12¢1; 11¢0 - 13¢2) 72 (23¢4; 18¢7 - 28¢1) active cases as of May 31, 2020. (not presented in the table).
>60 115 (3¢7; 3¢0 - 4¢4)) 62 (20¢1; 15¢6 - 24¢6) Fig. 2 shows the distribution of overall percent test positivity rate
Total 3096 308
and the source in 3137/3404 cases. The acquisition of SARS-CoV-2
Gender ratio (M:F) 1884 (69; 67¢370¢6): 211 (61; 55¢566¢4):
1212 (31; 29¢332¢6) 97 (39; 33¢544¢4)
infection could mostly be attributed to travel (2264, 72¢1%); domestic
a
travel (2136, 68%) and international (128, 4%) or as a known contact
Clinical manifestations of symptomatic cases are provided in supplementary
Table S2.
with a COVID-19 positive case (873, 27¢8%). In the remaining 267
cases (7¢8%), the precise reason behind the acquisition of infection
could not be ascertained. Amongst these 267 cases, 111 (41¢6%) pre-
3. Results sented with ILI / SARI with no information of contact with a COVID-
19 positive case. In the remaining 156 (58¢4%) cases, the source of
3.1. Testing infection was not traceable. However, the initial adjusted test positiv-
ity rate was 1% on March 8, 2020 which gradually declined to less
Figure S1 presents the district-wise distribution of cases. The than 1% until mid-April 2020, following which there was a steady
highest number of COVID-19 cases were identified in the capital city increased to 10% until the end of the study (Figure S2).
of Bengaluru, followed by Kalburgi, Mandya, Yadgir, Udupi, and Rai- As evident from Fig. 3, COVID-19 positive cases were initially
chur. During the study period, the Karnataka state was testing detected in the city of Bengaluru and subsequently spread to people
approximately 4377 per million, with a positivity rate of 1¢1%. The in the other districts, either by contact in Bengaluru or by travelling
total cases per million were 2708 in the state. Karnataka followed to other districts. The other hotspot districts were Gulbarga, Mysore
contact tracing diligently with the highest number of contacts (47¢4) and Dakshina Kannada, which had an independent source of infec-
traced for each positive case detected [4,18]. tion and local spread. The majority of the COVID-19 cases (68¢5%;
Description of cases by time, place, and person: The age, gender dis- 2264/3304) had a history of either international (5¢7%; 128/2264) or
tribution, and clinical details of all the COVID-19 cases in Karnataka domestic travel (94¢3% 2136/2264), which implies that this was the
are presented in Table 1. To understand the dynamics of SARS-CoV-2 main mode of introduction of SARS-CoV-2 into the state. Amongst
transmission within the state, we undertook a detailed analysis of those with a history of international travel 41/128 arrived at the city
the data available in the line list. Amongst the 3404 COVID-19 posi- of Bengaluru. Similarly 44/128 arrived into the other international
tive cases, 3096 (91%) were asymptomatic, while 308 (9%) were airport situated at Mangalore city of Dakshin Kannada district and
symptomatic. The age distribution revealed that 54¢6% (1691/3096, travelled to their hometowns. Domestic travel from other states of
95% CI; 52¢856¢3) of the asymptomatic cases were less than 30 years India to the districts of Yadgir, Mandya, Udupi, Raichur and Kalaburgi
of age compared to 25¢3% (78/308, 95% CI; 20¢430¢1); of symptom- accounted for more than 200 COVID-19 positive cases. Additionally
atic in this age group. On the other hand, 43¢5% (134/308, 95% CI; inter-district travel within the state from the city of Bengaluru to
3849) of the symptomatic were over 46 years of age compared to Davanagere district contributed to the spread of 124 COVID-19 posi-
15¢8% (489/3404, 95% CI; 14¢517) of the asymptomatics in this age tive cases. Overall, our analysis revealed that the city of Bengaluru
group. The percentage of symptomatic and asymptomatic in the age had the highest number of COVID-19 positive cases (378), followed
range 3145 were more or less similar (31¢2% and 29¢6% respec- by Kalaburgi (307), Mandya (284), and Yadgir(284), respectively.
tively) as shown in Table 1. The gender distribution revealed a male Amongst the 873 cases with a history of contact with a COVID-19
preponderance in both asymptomatic and symptomatic cases. positive case, 822 could be epidemiologically linked to 144 source
Table 2 presents the clinical status and outcome of the COVID-19 cases. The remaining 51/873 had a history of contact but could not be
cases in Karnataka. Overall, amongst the 3404 cases, the final out- precisely linked to a known source. Using the information available
come was available for 1394 (41%) at the end of the study period in the line-list, cluster network analysis was performed to derive
(May 31, 2020) while the remaining 2010 (59%) were active cases. dynamics of transmission (Fig. 4 and Table 3) from symptomatic and
Amongst those, where the outcome was available 7¢6% (106/1394, asymptomatic index cases. Amongst the 144 index cases, 32% (46)
95% CI; 6¢29) had a variety of comorbidities (Table S3). Further, the contributed to large clusters (>5 cases). As evident from Table 3, 69%
occurrence of comorbidities was ten-fold higher in symptomatic (32/46) index cases were symptomatic while 31% (14/46) were
cases, 29¢1% (73/251, 95% CI; 23¢334¢6), as compared to asymptom- asymptomatic. The size of each cluster ranged from 5 to 58 cases per
atic cases, 2¢9% (33/1143, 95% CI; 1¢83¢7). The instant case fatality cluster for symptomatic index cases (Mean 17¢03; 95% CI 15¢718¢4).
rate recorded in Karnataka was 3¢8% (54/1394, 95% CI; 2¢84¢8). On the other hand, the clusters resulting from asymptomatic cases
Amongst those who died, 87% (47/54, 95% CI; 7896) were range from 5 to 23 per cluster (Mean 8¢1; 95% CI 7¢29¢1). Amongst

Table 2
Comorbidities in COVID19 cases.

Outcome Asymptomatic (n = 1143) Symptomatic (n = 251) Total (%)

With comorbidity (%) Without comorbidity (%; 95% CI) With comorbidity (%; 95% CI) Without comorbidity (%; 95% CI)

Recovered 33 (100; NA) 1103 (99¢4; 98¢4 - 99¢5) 35 (48; 36¢5 - 59¢4) 169 (95; 91¢8 - 98¢2) 1340 (96¢1)
Died 0 7a (0¢6; 0¢2 - 1¢0) 38b (52; 40¢5 - 63¢4) 9 (5; 1¢8 - 8¢2) 54 (3¢9)
Total 33 1110 73 178 1394
NA-Not Applicable.
a
The causes of death in these 7 patients were unrelated to COVID-19; Myocardial infarction (3), Traumatic Brain Injury (2), Suicide (1), and Septic shock (1).
b
Among these 38 cases, 34 (89.4%) were above the age of 45 years.
N. Kumar et al. / EClinicalMedicine 32 (2021) 100717 5

Fig. 2. Distribution of case categories and overall test positivity. X axis depicts the timeline, Y axis depicts the overall test positivity rate while the Z axis depicts the number of
COVID-19 positive cases. Note there was a huge surge in the number of COVID-19 positive cases in the second half of May 2020.

the 545 cases originating from 32 symptomatic index cases, 41 were travel (5¢7%; 128/2264), thereby suggesting that this was the main
symptomatic, and 504 were asymptomatic. On the contrary, only 2/ mode of introduction of SARS-CoV-2 into the state. It is presumed
114 cases originating from 14 asymptomatic index cases manifested that these subjects had acquired the infection at the place where
symptoms (Table 3). The dispersion parameter (k value) of asymp- they initiated their travel. Alternatively, it is possible that they
tomatic cases was thrice that of symptomatic cases. Detailed cluster acquired it during their travel from fellow passengers, especially the
wise distribution of cases are mentioned in Table S6. Graphic repre- domestic travellers.
sentation of transmission dynamics in the large clusters (>5 cases) is From the detailed epidemiological analysis of data in this study, it
presented in Fig. 4. Overall, among the 545 cases resulting from emerges that both symptomatic and asymptomatic cases contributed
symptomatic source cases, 67.5% (368) cases were contributed by 12 to the transmission and spread of SARS-CoV-2 infection within the
superspreading events (SSEs) originating from symptomatic cases. state. An overwhelming majority of the COVID-19 cases in Karnataka
Whereas, two SSEs originating from asymptomatic cases contributed were asymptomatic at the time of specimen collection, and this is
to 16¢7% (19/114) cases (Fig. 4). Among the total 705 (46 source and similar to the results reported in India as well as other Asian coun-
659 secondary) cases which fall into clusters of 5 or more cases, 291 tries [25] and in stark contrast to what is reported in several western
accounted for within household transmission. The mean number of countries [26]. Most of the asymptomatic cases in this study were
cases per household was 3.06 (95%CI; 2.83.2) ranging between 2 young adults or middle-aged (Table 1: <46 years of age).
and 8 cases per household. Further, there was no significant differ- Our analysis suggests that the symptomatic cases were the prime
ence observed with respect to the number of transmission cycles drivers of the SARS-CoV-2 transmission within the state during the
between clusters resulting from symptomatic (Mean 1¢47; 95% CI early phase of the pandemic. The evidence for this is manifold: (i)
1¢151¢79) and asymptomatic (Mean 1¢18; 95% CI 0¢931¢42) index The mean secondary attack rate was 7¢1 for symptomatic cases (90
cases (data not presented). symptomatic source cases transmitted infection to 645) as compared
to 3¢1 for asymptomatic cases (54 asymptomatic source cases trans-
4. Discussion mitted infection to 177), and this difference was statistically signifi-
cant (Table S5). (ii) Cluster network analysis revealed that
This study describes the epidemiology of SARS-CoV-2 infections in symptomatic source patients contributed to 32 large clusters (>5
the state of Karnataka, South India. Before March 8, 2020, there were cases) with the mean size of each cluster being 17¢03 (range 558).
no COVID-19 cases in Karnataka. SARS-CoV-2 infection was intro- In contrast, the asymptomatic source cases contributed to 14 large
duced into the state by people travelling from foreign countries until clusters (Table 3 and Fig. 4) with the mean size of each cluster being
the country went into lockdown in the fourth week of March 2020 8¢1 (range 523). (iii) The proportion of secondary cases in the clus-
when international flights were not allowed into the country (Fig. 1). ters manifesting overt clinical illness was higher when the index case
What initially started as an infection in the capital city of Bengaluru was symptomatic compared to asymptomatic (Table 3 and Table S6).
at the beginning of March 2020, quickly spread to the other parts of (iv) The dispersion parameter for symptomatic source cases was
the state (Fig. 3). The majority of cases were mainly (68¢5%; 2264/ three-fold lower (k = 1¢2) as compared to asymptomatic source cases
3304) attributable to domestic (94¢3%, 2136/2264) and international (k = 3¢6), thereby, indicating the higher propensity of transmission
6 N. Kumar et al. / EClinicalMedicine 32 (2021) 100717

Fig. 3. Distribution and direction of transmission of COVID-19 cases in Karnataka State. Each dot represents a person with COVID-19. Primary cases are in red and secondary cases in
blue. Blue colored dots connected to primary cases using lines. The dots not connected by lines represent independent introduction from elsewhere. Bengaluru city was the epicen-
ter, had the highest density of COVID-19 cases, from where spread occurred to several districts in the state.
N. Kumar et al. / EClinicalMedicine 32 (2021) 100717 7

Fig. 4. Cluster diagram depicting symptomatic and asymptomatic COVID-19 cases in the Karnataka state, MarchMay 2020. Each case is represented as a dot: red dot indicates a
symptomatic case while yellow dots represent an asymptomatic case. The index case in each cluster is depicted as a larger dot and also indicated with the P number. The lesser the
P number, the earlier the patient was detected either as a source or as a contact of a known source. Note there were 46 clusters with five or more cases. The index case of majority
(32/46) of clusters was a symptomatic patient (red). Large open circles (depicted using interrupted lines) represent superspreading events (>6 cases originating from a
source). Overall, among the 545 cases resulting from symptomatic source cases, 67.5% (368) cases were contributed by 12 SSEs originating from symptomatic cases. Whereas, two
SSEs originating from asymptomatic cases contributed to 16.7% (19/114) cases.

Table 3
Cluster network analysisa depicting the clinical status of index cases and dispersion parameter of COVID19 cases.

Index case status Distribution of index cases Total number of cases Clinical status of cases Average number of cases per Dispersion parameter
(n = 46) associated with the index associated with the index cluster (95% CI) (k value)
case (n = 659) case (n = 659)

Symptomatic 32 (69%) 545 (82¢7%) Symptomatic (n = 41) 17¢03 (15¢718¢4) 1¢2


Asymptomatic(n = 504)
Asymptomatic 14 (31%) 114 (17¢3%) Symptomatic (n = 2) 8¢1 (7¢29¢1) 3¢6
Asymptomatic (n = 112)
a
Restricted to large clusters (>5 cases).
8 N. Kumar et al. / EClinicalMedicine 32 (2021) 100717

from symptomatic cases especially associated with SSEs (>6 cases settings to capture ‘silent’ transmission by asymptomatic individuals
originating from an index case) [27]. should be an integral component of the policy to prevent spread of
Studies from western countries have observed that the true pro- SARS-CoV-2.
portion of asymptomatic cases is as low as 20% [28]. On the contrary,
several other studies have observed higher proportion of asymptom- Data sharing statement
atic cases especially in India [19,29-33]. Karnataka state had better
contact tracing in the country during the early stage of the pandemic Study data (in spreadsheet form, with included data definitions) is
by detecting 47¢4 contacts per confirmed COVID-19 case [19]. Hence, available with the Office of the State Surveillance Officer, Govern-
we believe that there was no bias in selection of cases which could ment of Karnataka. Data sharing requests are subject to approval by
have skewed the observation that more than 90% of cases were the Commissioner of Health and Family Welfare, Government of Kar-
asymptomatic. Indeed, it is merely a reflection of the COVID-19 sce- nataka. Data and other information can be requested by sending an e-
nario during the early stage of pandemic in the state of Karnataka. mail to the corresponding author at: virusravi@gmail.com.
Although, it may be argued that some of the asymptomatic cases may
have developed symptoms after 713 days, all the cases during the
Author contributions
lockdown period were hospitalized and were under medical observa-
tion for 14 days. Therefore the chances of misclassification was
NK and SKSH contributed equally to data collection, analysis and
unlikely [28,34]. Moreover, the selection of contacts or cases in the
preparation of manuscript, GRB contributed to analysis and review of
testing system was according to the national guidelines that man-
manuscript, MMV contributed to laboratory testing, data analysis
dated active search and testing for SARS-CoV-2 infection in each state
and review of the manuscript, PD and PKBG contributed to collection,
[20].
collation of data and preparation of line-list, DAJ contributed to data
There was no risk factor ascribed for acquisition of SARS-CoV-2 in
analysis and figures, AD contributed to data analysis, preparation and
267/3404 cases (7¢8%) in the present study. There are two likely
review of the manuscript and VR conceptualized the study and con-
explanations for this. Firstly, it may be argued that it is indicative of
tributed to data analysis, preparation and review of the manuscript.
“community transmission”. Recent reports of SARS-CoV-2 seropreva-
lence studies carried out across India have indicated that substantial
transmission has occurred in rural areas although it was higher in Declaration of Competing Interest
urban settings. Further, it was noted that a mere 3% of seropositive
individuals reported COVID-19 symptoms [35,36]. Secondly, owing The authors declare no conflict of interest.
to limitations in routine surveillance data collection, especially dur-
ing the early phase of the epidemic in India as reported by an earlier Acknowledgements
study, it is likely that the 267 cases are indicative of community
transmission [37]. The authors acknowledge the COVID laboratory and data manage-
There were two limitations to this study. Firstly, the study was ment team of Deptartmet of Neurovirology, NIMHANS (in alphabeti-
restricted to the early period of the pandemic when large number of cal order): John Bannerjee, Tina Damodar, Priti Das, Anson George,
infections occurred due to travel. As a result, complete contact tracing Kiran Hosallimath, Ruthu Nagaraju, Tanmoy Nandi, Amrita Pattanaik,
data was available only in 966/3404 (28¢4%) COVID-19 cases until Chitra Pattabiraman, Harsha PK, Risha Rasheed, Vijaykiran Reddy,
May 31, 2020. Although contact tracing for all cases would be ideal, Vijayalaksmi Reddy, Ashwini M A, Sourabh Suran as well as all the
given the reality of the rapid and extensive spread of SARS-CoV-2 staff of the ICMR approved SARS-CoV-2 testing laboratories in the
virus, there were numerous constraints and challenges in achieving state of Karnataka. The contributions of the state and district surveil-
this. Secondly, a key factor in the transmission of COVID-19 is the lance officers and their teams are also gratefully acknowledged.
high level of shedding of SARS-CoV-2 virus from the upper respira-
tory tract. Viral RNA shedding is higher at the time of symptom onset Supplementary materials
and declines after days or weeks [38]. The difficulty of distinguishing
asymptomatic cases from those who are pre-symptomatic is a major Supplementary material associated with this article can be found
stumbling block. Since longitudinal data on the occurrence of symp- in the online version at doi:10.1016/j.eclinm.2020.100717.
toms after the date of collection of specimens was available for the
quarantine period (14 days) of this study, it is plausible that a few
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